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from the RCOG
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Volume 24 Issue 1 2022

Contents

Editorial 58 Preconception health in the well woman


SBA
3 Editorial Charlotte Brooks, Prasanna Raj Supramaniam, Monica Mittal
Kate Harding

Editor's Pick Education


4 Spotlight on… haemorrhage 67 The blind spot: value-based health care in obstetrics and
Hashviniya Sekar, Lauren Berg, Wai Yoong gynaecology
Osama Naji, Vivienne Souter, Edward Mullins, Jonathan
Gaughran, Yasser Diab, J Edward Fitzgerald, Tom Bourne,
Edward Morris
Commentary
7 TOGadvisor: the role of online feedback in obstetrics and
gynaecology
CPD
Lorraine S Kasaven, Srdjan Saso, Jara Ben Nagi, Karen Joash,
Joseph Yazbek, J Richard Smith, Tom Bourne, Benjamin P Jones 73 CPD questions for volume 24 issue 1

77 TOG ratings
Reviews
12 Female sexual dysfunction
SBA
Victoria Kershaw, Swati Jha MBRRACE-UK update
79 MBRRACE-UK update: Key messages from the UK and Ireland
24 Investigation and management of postcoital bleeding
SBA Confidential Enquiries into Maternal Death and Morbidity 2021
Gemma L Owens, Nick J Wood, Pierre Martin-Hirsch
Marian Knight
31 Cervical cancer in pregnancy: diagnosis, staging and treatment
SBA
Tamara Howe, Kate Lankester, Tony Kelly, Ryan Watkins,
Sonali Kaushik TOG reviewers 2020
40 Accessory cavitated uterine malformations (ACUMs): an 82 TOG reviewers 2020
SBA
unfamiliar cause of dysmenorrhoea
Thulasi Setty, Joel Naftalin, Davor Jurkovic And finally…
50 Pregnancy in underweight women: implications, management 84 Small world?
SBA and outcomes James Drife
Robert Burnie, Edward Golob, Sonji Clarke
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2
DOI: 10.1111/tog.12790 2022;24:58–66
The Obstetrician & Gynaecologist
Review
http://onlinetog.org

Preconception health in the well woman


Charlotte Brooks MBBS MRCOG,a Prasanna Raj Supramaniam MB ChB MSc MRCOG MAcadMEd,*
b,c

Monica Mittal BSc MBBS MRCOG MDd


a
Locum Consultant Obstetrician and Gynaecologist, Women’s and Children’s, Imperial College Healthcare NHS Trust, St Mary’s Hospital, Praed
Street, Paddington, London W2 1NY, UK
b
Consultant Gynaecologist, Subspecialist in Reproductive Medicine and Surgery, Women’s and Children’s, Oxford University Hospitals NHS
Foundation Trust, John Radcliffe Hospital, Oxford OX3 9DU, UK
c
Honorary Senior Clinical Lecturer, Endometriosis CaRe Oxford, Nuffield Department of Women’s and Reproductive Health, University of Oxford,
Oxford OX3 9DU, UK
d
Consultant Obstetrician and Gynaecologist, Subspecialist in Reproductive Medicine, Women’s and Children’s, Imperial College Healthcare NHS
Trust, St Mary’s Hospital, Praed Street, Paddington, London W2 1NY, UK
*Correspondence: Prasanna Raj Supramaniam. Email: prasannaraj@doctors.org.uk

Accepted on 18 December 2020. Published online 19 January 2022.

Key content moderate intensity activity per week, or 30 minutes of activity per
 It is important to focus on preconception care in the well woman day, or 75 minutes of intense activity per week.
because prevention is better than treatment, and interventions  Alcohol is a teratogen that can cause fetal growth restriction and
commenced in pregnancy may have limited benefit. facial malformations, learning and behavioural challenges and
 A lower socioeconomic status is associated with poorer maternal impairment to the central nervous system. Smoking in pregnancy
and neonatal outcomes, including gestational diabetes mellitus can lead to impaired fetal growth and adverse effects on the
(GDM), preterm birth (PTB), pre-eclampsia (PET), and small-for- immune system.
gestational-age babies.
Learning objectives
 Poor nutrition contributes to epigenetic dysregulation, which can
 To understand the importance of the preconception period.
alter gene expression and effect phenotypic change. A healthy diet  To evaluate key nutritional requirements in the
during pregnancy, high in grains and vegetables, may help to
preconception period.
reduce the risk of obesity, GDM, cardiovascular disease,  To critically evaluate the benefits and disadvantages of vaccination
hypertension, PET, and maternal anaemia; the benefits to the fetus
in the preconception period.
include the prevention of low birthweight, macrosomia, PTB
and stillbirth. Keywords: infections / nutritional health / preconception health /
 The minimum amount of aerobic activity recommended during pre-pregnancy counselling
the preconception and pregnancy period is either 150 minutes of

Please cite this paper as: Brooks C, Supramaniam PR, Mittal M. Preconception health in the well woman. The Obstetrician & Gynaecologist 2022;24:58–66. https://
doi.org/10.1111/tog.12790

The preconception period can be viewed from three


Introduction
different perspectives:
Preconception care is an important aspect of supporting  Public health: addressing risk factors such as smoking, diet
health improvements for individuals across their reproductive and obesity in the months to years preceding conception.
life.1 The global awareness of preconception health and care is  Individual: planning for a pregnancy in the months
currently low, but most women in low-, middle- and high- before conception.
income countries do plan for a pregnancy.2 This period of  Biological: the weeks to days before
planning provides the opportunity for education and embryological development.
intervention to improve preconception health and Preconception health is important for three main reasons:
subsequently, to reduce the incidence of maternal and  Parental lifestyle during the maturation phase of
neonatal morbidity and mortality. The challenge, however, gametes and embryo development can adversely affect
lies in accurately identifying the women who are most at risk. developmental programming.3
Women who are healthy at the time of conception are more  Maternal motivation is high at this time; therefore,
likely to have a successful pregnancy and healthy child.1 effective changes can be implemented.

58 ª 2022 Royal College of Obstetricians and Gynaecologists.


Brooks et al.

 Interventions commenced in pregnancy have only lower live birth rates per cycle of in vitro fertilisation
limited benefit.2 undertaken in a socioeconomically deprived cohort.12
Approximately 40% of all pregnancies are currently Many causative factors other than financial barriers to
unplanned; therefore, health interventions provided once a health care contributed to the differing outcomes, such as
woman has already decided to have a child can sometimes be longer working hours, cost of travelling to antenatal
too late. Many of the interventions are more effective when appointments, smoking, psychological stress and lower
implemented throughout the reproductive years of a educational standards leading to fewer attendances at
population.2,4 These interventions can be categorised into antenatal appointments.11
three groups:5
 Educational: general health advice, education on sexually
Environmental health
transmitted infections, counselling (faith-based groups or
individual counselling), and skills-building sessions. Environmental hazards are increasingly recognised as risk
 Promotion of contraception: education as well as the factors for poor perinatal outcomes. Chemical hazards such
distribution of contraception. as lead, mercury, carbon monoxide, pesticides and chlorine
 Combination of educational and contraception exposure can affect a developing fetus.13 The critical point of
promoting interventions. exposure is during fetal development and postnatally, rather
Programmes adopting multiple strategies (education, than preconceptually. Table 1 highlights the health effects of
contraception promotion and skill-building sessions), in chemicals with strategies to prevent exposure.
contrast to singular interventions have been shown to have a
greater impact.5
Nutritional health
In the Australian LIMIT study6 and the UPBEAT UK trial7
for example, a change in dietary behaviour with exercise and Interactions between genetics, epigenetics and external
diet interventions in overweight pregnant women was not factors such as nutrition can affect in utero developmental
correlated with a reduction in any adverse pregnancy processes, which can lead to adverse pregnancy outcomes and
outcomes such as gestational diabetes mellitus (GDM), pre- an increased risk of certain diseases in later life.2,16
eclampsia (PET), preterm births (PTB) or large-for- Nutritional factors and undernutrition are not thought to
gestational-age babies.2 These studies demonstrated that cause genetic changes at the DNA level, but are thought to
strategies relying on implementation at the public health contribute to epigenetic dysregulation, which can alter gene
level could take considerable time to reverse obesity. Thus, expression and effect phenotypic change. In embryogenesis,
better health outcomes are achieved with interventions DNA is demyelinated and then re-myelinated, during which
instigated at an earlier stage, allowing for physical, mental time reprogramming and epigenetic hallmarks can occur,
health and social issues to be discussed and addressed. This, leading to life-long effects. The Dutch famine is an example
overall, helps to empower women in making a more of how maternal malnutrition can lead to an increased risk of
informed decision about their family planning.8 obesity in progenies.3,16 This is echoed in animal models
This article summarises the current advice and demonstrating a correlation between fetal growth restriction
recommendations, along with any specific interventions. and obesity in later life.17,18 Furthermore, epigenetic
reprogramming leading to placental insufficiency has been
linked to a reduced expression of insulin-like growth factor 1
Socioeconomic factors
(IGF-1) by the liver, which, in turn, is associated
Preconception advice and the availability of facilities differs with obesity.19
between high and low socioeconomic statuses (SESs). A healthy diet during pregnancy, which is high in grains
Overall, however, a lower SES is associated with poorer and vegetables, may help to reduce the risk of obesity, GDM,
maternal and neonatal outcomes, including GDM, PTB, PET cardiovascular disease, hypertension, PET, and maternal
and small-for-gestational-age (SGA) babies.9,10 A Korean anaemia. The benefits to the fetus include the prevention of
study11 found that 29% of low SES women received low birthweight, macrosomia, PTB and stillbirth.20,21
inadequate antenatal care, with fewer antenatal visits and In many countries, obesity coexists with a continuing
poorer obstetric outcomes, compared with 11.4% of high SES problem of undernutrition and micronutrient deficiencies.
women. Women in the low SES group had a higher rate of Several studies have highlighted poor nutritional intake in
abortions (30.1% versus 20.7%, p < 0.001), caesarean both women contemplating pregnancy and those who are
delivery (45.8% versus 39.6%, p < 0.001), PET (1.5% currently pregnant, with most not meeting the
versus 0.6%, p < 0.001), PTB (2.1% versus 1.4% p < 0.001) recommendations for vegetable, grain, folate, iron, and
and obstetric haemorrhage (4.7% versus 3.9%, p = 0.017). calcium intake. Furthermore, 55% are said to exceed the
These findings were echoed by another study highlighting recommended daily fat intake.20,21 Comprehensive strategies

ª 2022 Royal College of Obstetricians and Gynaecologists. 59


Preconception health in the well woman

Table 1. Health effects following chemical exposure and strategies to prevent exposure.

Chemical Source Impact on health Prevention strategies

Lead Paint Low levels: cognitive Postpone conception for 3–6 months following exposure
Soil impairment Lead-free paint
Water High levels: aggression
and cognitive dysfunction

Mercury Ocean fish Child deficits in language, Follow the fish consumption guidelines from the
Swordfish attention, and memory Food Standards Agency14
Anxiety

Carbon Cigarette smoking Sudden fetal death Testing in early pregnancy


monoxide Faulty gas or Neurological deficits Smoking cessation of the woman and other members
heating appliances Premature birth in the household
Cars with faulty exhausts Repair/remove faulty items

Organic From ingestion/inhalation/ Lower intelligence quotient (IQ) Organic pollutants are stored in fat tissues; therefore,
pollutants dermal exposure Reduced memory in children aim to achieve a normal body mass index
Contaminated foods (BMI) before pregnancy

Modified from Gardella, 200115 and Ondeck and Focareta, 200913

are therefore needed to both reduce undernutrition and subsequently drive fetal adiposity and growth.3 Furthermore,
prevent obesity.21 the level of oxidative stress rises, with a subsequent increase
in the aneuploidy rate.3 These findings are supported by
Overweight/obesity studies conducted in donor oocyte cycles, in which poorer
Globally, the prevalence of obesity in women has risen from outcomes were seen in recipient women of normal BMI who
6% in 1975 to 15% in 2014.2 A body mass index (BMI) above received donor oocytes from women with a raised BMI.3
25 kg/m2 has been linked to multiple complications and
causes of maternal mortality, such as hypertensive disorders Undernutrition
of pregnancy, GDM, reduced fecundity and an increased risk Approximately 10–20% of all women are underweight; being
of miscarriages.2,23,24 The intrapartum and postpartum underweight is most prevalent in women of South Asian
periods are also complicated by increased anaesthetic risks, descent (24% in 2014).2 Stunted growth is often the result of
lower success rates from a trial of labour and an increased poor nutrition and famine since childhood. Maternal short
risk of infection.24 Fetal and neonatal adverse effects stature heightens the risk for obstructed labour, birth
include macrosomia, stillbirth, low birthweight, congenital asphyxia and obstetric fistula formation. Female
anomalies as well as neonatal hypoglycaemia secondary to undernutrition also contributes to 20% of maternal deaths
poor lactation.2 and is a significant risk factor for stillbirth, PTB, low
Obesity has been shown to adversely affect the birthweight and SGA babies.24
periconception developmental conditioning of the embryo.3 A maternal protein-deficient diet in the final few days of
It has been linked to higher concentrations of inflammatory oocyte maturation and up to the stage of embryo pre-
cytokines, hormones and metabolites, which can accumulate implantation is associated with chronic inflammation and
in the ovarian follicular fluid and affect oocyte development metabolic health in progeny. It can cause a decrease in
and maturation. Oocytes from obese women are smaller in pancreatic beta-cell mass and function, leading to glucose
size and have increased triglyceride levels. Mitochondrial intolerance in adult life.16 This has also been associated with
defects and impaired metabolic regulation have been increased weight, hypertension, and adiposity in later life.3
demonstrated in the oocytes of mice models in the
presence of raised lipid concentrations. The resultant Interventions and strategies
blastocyst from an oocyte of an obese female expresses Preconception weight normalisation is supported by a
reduced glucose consumption and raised insulin levels population-based cohort study, in which there was a 10%
compared with oocytes from healthy individuals, which can lower risk of stillbirth, PET, GDM and macrosomia with a

60 ª 2022 Royal College of Obstetricians and Gynaecologists.


Brooks et al.

10% decrease in pre-pregnancy BMI.2,25,26 Comparable be detrimental during this time. Contact sports, including
results were also seen in a study comparing women who those with the risk of falling, and scuba diving, however, are
had undergone bariatric surgery 2 years before conception to contraindicated during this period.25
those that had not of a similar BMI.2,11,12 The minimum amount of aerobic activity recommended is
The World Health Organization (WHO) has advised all either 150 minutes of moderate intensity activity per week, or
countries to adhere to the recommended 30 minutes of activity per day, or 75 minutes of intense
international/national dietary guidelines, as this will activity per week. Women are recommended to be active on
provide adequate macro and micro nutrition for a healthy most days of the week, with no session lasting longer than
diet. In turn, this will lead to positive effects on pregnancy 60 minutes.25
and birth outcomes, as well as the future health of the Strength sessions are recommended twice a week, on non-
offspring.1,20 Unfortunately, nonadherence remains an issue consecutive days, of 1–2 sets of 12–15 repetitions of each
in both high and low socioeconomic countries, with one in muscle group.25
three people experiencing undernutrition, malnutrition,
nutritional deficiencies or obesity.21 Noncompliance has
Vitamin supplementation
been attributed to low income, food availability, cultural
traditions, individual beliefs, age, education, environmental Duckworth (2012)31 highlighted the importance of adequate
and geographical factors. Older women, who do not smoke levels of the 13 essential vitamins (A, B series, C, D, E and K)
and have a higher level of education were predictors for in pregnancy. Here, we focus on folate, iron, and zinc levels.
better adherence.27
Dietary advice, nutritional education and counselling Folate
during pregnancy have been demonstrated to statistically Folate (B9) is essential in the manufacture of red and white
reduce excessive weight gain, reduce the risk of anaemia in blood cells in the bone marrow, for conversion of
late pregnancy by 30%, increase birthweight by 105 g and carbohydrates into energy and for production of DNA and
lower the risk of PTB by 19%.16,27,28 The overall quality of the RNA. Adequate levels are required for rapid cell replication
evidence, however, is low.20,27 during periods of fetal and placental growth. Deficiency can
In 2018, a Lancet review evaluated three strategies aimed at lead to macrocytic anaemia and reduced oxygen-carrying
improving health behaviours and nutrition before capacity of the blood, and subsequently, fatigue, weakness,
conception: supplementation; cash incentives; and and shortness of breath.32 It has also been linked to adverse
behavioural changes. The authors concluded that while fetal outcomes such as neural tube defects and anencephaly,
food fortification and supplements in pregnancy can congenital heart defects, growth restriction, low birthweight
provide the much-needed micronutrients to correct and preterm delivery.25,32
maternal deficiencies, the reports on benefits to child health
are conflicting.2,29 The supplements were acceptable to the Interventions and strategies
women, but compliance was poor for the same reasons The main intervention has been preconception folic acid
previously mentioned. Cash incentives have proven supplementation. Folic acid is converted to folate in the body
successful in other settings such as school enrolment, but and is the more stable product to manufacture and store.
no studies have addressed this in the context of health Supplementation with folic acid is internationally
behaviours. In contrast, studies addressing preconception recommended by the WHO for a minimum of 3 months
behavioural interventions demonstrated no favourable before conception and until 12 weeks’ gestation.33 It has been
impact on pregnancy outcomes.30 shown to prevent 69–78% of recurrent neural tube defects, as
Undernutrition in low SES settings is more complex. well as reduce the risk by 70%.2,24,29 Other benefits include
Broader health strategies over behavioural changes will the decreased risk of PET, stillbirth, neonatal death, SGA and
be required in the context of food not being as readily autism in children.2
available.30 Health strategies have a greater impact when the Interventions have either been targeted at the individual or
interventions are targeted; for example, by identifying the age through a collective provision of folic acid through food
and life phase of the individual. The motivation of the supplementation and public campaigns.29,34
individual is better recognised in these circumstances.30
Iron
Over 40% of women worldwide are anaemic in the
Exercise
preconception period. This is associated with an increased
A combination of aerobic and strength exercises is risk of maternal mortality. Maternal undernutrition and iron
recommended during the preconception and pregnancy deficiency account for 20% of maternal deaths worldwide.4 It
period. Moderate intensity activity has not been shown to is estimated that a population increase in maternal

ª 2022 Royal College of Obstetricians and Gynaecologists. 61


Preconception health in the well woman

haemoglobin of 1 g/dL could reduce the risk of mortality by Interventions and strategies
approximately 25%.35 Zinc supplementation has been associated with a 14% (RR
The iron status of a woman has manifold roles in the 0.86, 95% CI 0.76–0.97) reduction in PTB compared with
reproduction cycle. Anaemia has been shown to controls.40 This was predominantly seen in the low SES
detrimentally affect the birthweight, as well as the woman’s setting and could reflect poor nutrition as a whole. No other
recovery following delivery.24 Experimental animal models benefits from zinc supplementation have been identified.40
have demonstrated a 40–50% reduction in brain iron stores
in the postnatal period, with dietary iron restriction
during pregnancy.2
Tobacco use
Smoking in pregnancy can lead to impaired fetal growth and
Interventions and strategies adverse effects on the immune system. It has been linked to a
The main intervention includes iron supplementation or 28% increased incidence of late stillbirths plus neonatal
fortification of foods such as flour, rice, sugar, juice, fish or mortality. Furthermore, the birthweight has been shown to
soy sauce. Iron supplementation has been shown to have a be reduced by 170 g in those who smoke.41
greater impact on the population than food fortification.
Daily iron supplementation has reduced the incidence of low Interventions and strategies
birthweight by 20% (relative risk [RR] 0.80, 95% confidence Smoking cessation classes alone have been shown to reduce
interval [CI] 0.71–0.90) compared with controls, and iron the self-reported smoking rate by 88%; however, in reality,
deficiency maternal anaemia by 66% (RR 0.44, 95% CI 0.28– none of those questioned had stopped smoking. Written
0.68) at term compared with controls.36 The fortification of hand-outs and counselling had little impact in the
foods, however, is more cost effective, with high cost-benefit short term, but after 12 months, significantly more
ratios given the levels of deficiency in low SES.37 individuals remained smoke-free than those in the
The WHO has recommended weekly iron and folic acid control group.29
supplements in reproductive-aged populations, especially Individual-level planning, however, is not possible in
where the prevalence of anaemia is >20%.34 Iron unplanned pregnancies; thus, in these circumstances, advice
supplementation programmes, however, are poorly and action at the public health level is more beneficial. Public
implemented and have little global impact secondary to health strategies and education work to reduce risk
limited access and participation in antenatal care. Between behaviours; for example, by increasing taxation and
2007 and 2014, globally only 64% of women completed the minimum spend on cigarettes and alcohol purchases.2
WHO recommended minimum of four antenatal visits for
patients in low- and middle-income countries. In 2016, the
WHO changed its recommendation to eight
Alcohol
antenatal visits.35 The number of women worldwide who are thought to
Other interventions include delayed cord clamping, which consume alcohol is in the region of 20%. Ingestion of more
has been shown to reduce the risk of neonatal anaemia. The than seven standard units of alcohol per week is said to
WHO has recommended delaying cord clamping for up to 1 increase the risk of developmental and cognitive disability in
minute, with some evidence suggesting up to 3 minutes is the offspring.42 The consumption of more than 5 units of
beneficial in countries where the rates of infant iron alcohol in one setting has been shown to increase the risk of
deficiency anaemia are high.38 Furthermore, nutrition miscarriage, low birthweight and PTB.43 Alcohol
counselling and deworming in high-prevalence countries consumption has been linked to reduced absorption of
have shown some benefit, as hookworms can cause nutrients contributing to malnutrition.
gastrointestinal bleeding.35 Fetal alcohol spectrum disorder (FASD) or fetal alcohol
syndrome (FAS) are terms used to describe the effects of
Zinc prenatal exposure to alcohol on the brain and body of the
Zinc is essential in protein synthesis, nucleic acid fetus. Alcohol can effectively cross the placenta, meaning that
metabolism, cell division and in the immune system. the level of alcohol in the fetus’ blood will be similar to
Deficiency may contribute to intrauterine or systemic maternal alcohol blood levels within minutes of
infections, leading to PTB and low birthweight.2,39 The consumption. Approximately 1% of the population are
maternal impact of zinc deficiency includes postpartum thought to be affected by FASD. Alcohol is a teratogen that
haemorrhage and pregnancy-induced hypertension.40 can cause growth restriction and facial malformations,
The WHO estimates that approximately 8% of pregnant learning and behavioural challenges and impairment to the
women worldwide have an inadequate zinc intake.39 central nervous system.44,45

62 ª 2022 Royal College of Obstetricians and Gynaecologists.


Brooks et al.

Interventions and strategies Table 2. Maternal and neonatal effects of infections (modified from
Pharmaceutical, psychological, and educational strategies Lassi et al., 201447 and Janakiraman, 200848)
have all been described in the literature. Medications
include: disulfiram; naltrexone, which causes unpleasant Infection Maternal outcomes Neonatal outcomes

symptoms when combined with alcohol; and acamprosate,


which stimulates the inhibitory gamma-aminobutyric Cytomegalovirus None/mild viral infection Hearing loss
acid (GABA) receptors, preventing the sensation of Visual impairment
pleasure usually associated with the consumption of Learning disabilities
alcohol.42 Their safety profile, however, within pregnancy Epilepsy
Congenital
is unknown. malformations
A study comparing the effects of four counselling sessions
with personalised feedback (including a session on Toxoplasmosis None/mild viral infection None to severe
Miscarriage Neurological
contraception), with written information regarding the
impairment
risks of alcohol consumption and women’s health on Retinal lesions
behavioural changes, found a two-fold (odds ratio [OR] Congenital
2.11, 95% CI 1.47–3.03) lower incidence of an alcohol- malformations
Risk of infection
exposed pregnancy up to 9 months after the intervention, in
increases with
the group who received counselling sessions. This outcome, gestational
however, was based on a self-reported change age/severity decreases
in behaviour.29,46 with gestational age
Research on the efficacy of psychological and educational Rubella Miscarriage Birth defects (effects
interventions are limited owing to the heterogeneity of are severe
studies. Results relating to a reduction or total abstinence of <16 weeks’
alcohol were mixed, and there was little evidence that these gestation)
interventions were effective for reducing alcohol Hepatitis B None in pregnancy Transmission of
consumption in pregnancy.42 Long term risk of liver hepatitis
Pregnancy outcomes post-intervention have not been cancer
reported; however, it is plausible that by reducing overall
HIV None if the viral load is Transmission of the
alcohol consumption during pregnancy, this will reduce low disease
adverse neonatal effects.29
Zika Rash/viral Microcephaly
symptoms/headaches
Infections
Syphilis Primary: painless Stillbirth
Preconception counselling regarding infections is important ulcers/sores Congenital syphilis
for two reasons. Firstly, any woman with an infectious disease Secondary: widespread (skin lesions/failure to
rash thrive/seizures/
can often be treated to eliminate or minimise the risk of
If untreated can cause hepatosplenomegaly)
transmission to the newborn; as is the case for example, with long term neurological
HIV, hepatitis B and syphilis. In view of this, all women are problems
offered antenatal screening. Secondly, some pregnant women Miscarriage
are more susceptible to certain infections during pregnancy. Listeria Fever/viral Fetal and neonatal
These can be associated with greater morbidity and mortality symptoms/headaches infections are severe
to either the mother or neonate secondary to changes in the Diarrhoea and vomiting Stillbirth/preterm
immune system, heart, and lungs of the pregnant woman; as Miscarriage delivery
Case fatality of
is the case in influenza, whooping cough, rubella, 20–30%
toxoplasmosis, Zika and listeria.47 Pneumonia/
Table 2 summarises the maternal and neonatal outcomes sepsis/meningitis
from exposure to infections.

Interventions
Vaccinations during pregnancy allow the woman to make
antibodies to specific infections, which can then be passed pregnancy and should therefore be administered during the
through the placenta and/or breast milk to protect the preconception period. Preconception education on
neonate. Not all vaccinations, however, are safe during simple hygiene, lifestyle changes and foods to avoid during

ª 2022 Royal College of Obstetricians and Gynaecologists. 63


Preconception health in the well woman

Table 3. Infections and interventions (modified from Lassi et al., 201447; Janakiraman, 200848; and, Peyron et al., 201949)

Treatable with medications Vaccine that can be given during


Infection during the preconception period preconception Interventions to prevent infection

Cytomegalovirus No None Education in simple hygiene

Toxoplasmosis Preconception infection: treatment is None Avoid undercooked meat


not indicated Avoid handling cat litter
Periconception infection (1 month
prior to 1 month after conception):
the risk of infection is very low –
discussion with an obstetrician
regarding risk-benefit in performing
a diagnostic amniocentesis

Rubella No Yes No
Mumps/measles/rubella (MMR)

Hepatitis B Anti-virals to reduce viraemia Yes for high-risk individuals Education regarding the transmission of the
preconception disease process with lifestyle/behavioural
modifications

HIV Anti-retrovirals to reduce viraemia None Anti-retrovirals to lower viraemia


preconception Education regarding the transmission of the
disease process with lifestyle/behavioural
modifications

Zika No None Education regarding the transmission of the


disease process with health precautions

Syphilis Yes (penicillin) None Education regarding the transmission of the


disease process with lifestyle/behavioural
modifications

Listeria Not normally required None Avoid luncheon meats/hot dogs unless
cooked until steaming
Avoid pates/unpasteurised milk or cheeses/
cheeses with a mould rind

pregnancy are essential to prevent these infections.47 Table 3 care because of location or cost and a lack of awareness about
summarises these vaccinations and recommendations. where help can be obtained.50
Individuals must implement and maintain a healthy
lifestyle throughout their reproductive years. This can be
Conclusion
challenging, requiring input at many organisational levels.
Improving preconception health will undoubtedly improve Changes and strategies to encourage and improve the health
maternal and neonatal outcomes. Table 4 summaries key of individuals must be cultural and societal in nature, driven
areas of concern and highlights potential interventions. at a governmental level. Each SES and country have their own
Unfortunately, changing behaviours in pregnancy alone is health behaviours that can be improved; however, the single
often not sufficient. Studies have explored the main largest strategy to create the greatest impact is to improve
challenges facing preconception health improvement. access to higher-level education. Improved education
Firstly, women believe that conception is a natural event, worldwide will subsequently highlight the importance in
which has been successful for generations, thus limiting the reducing ‘risky’ behaviours (such as smoking, alcohol and
need for medical intervention or attention. Secondly, there is drug abuse) and health guideline adherence.22
a lack of awareness of the need for preconception care, or Interventions in key areas of concern in the preconception
that this service is available. Thirdly, barriers to the delivery period have proven to improve maternal and neonatal
of this service have been identified, such as limited access to outcomes. The mainstay of the intervention appears to be

64 ª 2022 Royal College of Obstetricians and Gynaecologists.


Brooks et al.

Table 4. Summary of key areas of concern and proposed References


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66 ª 2022 Royal College of Obstetricians and Gynaecologists.


DOI: 10.1111/tog.12792 2022;24:50–7
The Obstetrician & Gynaecologist
Review
http://onlinetog.org

Pregnancy in underweight women: implications,


management and outcomes
a b c
Robert Burnie MRCOG, Edward Golob MRCOG, Sonji Clarke FRCOG MA FHEA *
a
ST6, Queen Elizabeth Hospital, Woolwich, London SE18 4QH, UK
b
ST6, Kingston Hospital, Kingston upon Thames KT2 7QB, UK
c
Consultant Obstetrician, Guys and St Thomas’ Hospitals Foundation Trust, London SE1 7EH, UK
*Correspondence: Sonji Clarke. Email: sonji.clarke@gstt.nhs.uk

Accepted on 28 December 2020. Published online 18 January 2022.

Key Content  To understand the antenatal care of underweight women,


 Despite attention on obesity in pregnancy, within the UK and globally, including nutritional advice and when additional fetal surveillance
many women enter pregnancy underweight. There remains a paucity is required.
of evidence-based guidance on the optimal care of these women.  To understand the heterogeneity of underlying causes of low BMI
 Maternal underweight is associated with low birthweight and in pregnancy and the importance of gestational weight gain.
preterm birth, both spontaneous and iatrogenic, but appropriate
gestational weight gain may mitigate low body mass index (BMI). Ethical Issues
 Beware making assumptions about different ethnicities that will
 Although being underweight may be protective against several
antenatal and intrapartum complications, low BMI can be related interfere with offering the most appropriate care.
 Low BMI that is not managed as a risk issue during pregnancy is an
to underlying organic disease and/or eating disorders, or there may
be modifiable lifestyle factors that should be addressed avoidable cause of low birthweight and preterm birth.
 Women presenting with low BMI may have features in their
in pregnancy.
 BMI at booking should assist as a screening tool. Body image, history, such as certain mental health disorders, that mean they
genetic, socioeconomic and cultural factors may affect BMI, should be referred for safeguarding as a vulnerable
making underweight women a heterogeneous group requiring adult. The unborn child and other children may also
individualised assessment. need assessment.

Learning Objectives Keywords: comorbidities / low BMI / pregnancy and anorexia /


 To understand the associations of low BMI in pregnancy and its pregnancy and pre-term delivery / underweight women
impact on maternal and fetal outcomes.

Please cite this paper as: Burnie R, Golob E, Clarke S. Pregnancy in underweight women: implications, management and outcomes. The Obstetrician &
Gynaecologist 2022;24:50–7. https://doi.org/10.1111/tog.12792

before, during and after pregnancy1 specifically excludes


Introduction
women with a BMI of less than 18.5 kg/m2.
Despite the obesity epidemic, within the UK and globally,
many women enter pregnancy underweight. Maternal
Epidemiology
underweight can be defined as having a body mass index
(BMI) of <18.5 kg/m2 at the start of pregnancy. A low BMI Approximately 3–4% of women in the UK enter pregnancy
may be ‘normal’ for the individual, but it could be associated underweight.2 However, worldwide, the burden of
with underlying organic disease, psychiatric illness or malnutrition lies in low- and middle-income countries. For
socioeconomic and lifestyle factors, which may need example, up to 30% of women of reproductive age, in most
addressing during the course of a pregnancy. While being countries in Sub-Saharan Africa, are underweight. Body
underweight can be protective against several antenatal and image, genetic, socioeconomic and cultural factors affect
intrapartum complications, it is associated with maternal and BMI, making underweight women a heterogeneous group.
fetal adverse outcomes, including low birthweight and However, large cohort data sets have indicated that
prematurity. Despite this, there remains a paucity of underweight pregnant women tend to be significantly
evidence-based guidance on the optimal care of these younger, single, in education, and not in paid employment.
women. Guidance published by the National Institute of In addition, there is evidence to suggest the prevalence of
Health and Care Excellence (NICE) on weight management smoking is higher in underweight women.2 In an American

50 ª 2022 Royal College of Obstetricians and Gynaecologists.


Burnie et al.

cohort study,3 being underweight pre-pregnancy was highly Gastrointestinal conditions leading to malabsorption, such
correlated with ethnicity. The study describes a disparity of as inflammatory bowel disease, or conditions associated with
maternal underweight of 8.6% in the Asian population and chronic inflammation, such as inflammatory arthropathies,
1.9% in the Black American population, drawing into are not uncommon in the pregnant population and may
question the validity of BMI as a measure of wellbeing, coexist with low BMI.
across a multi-ethnic population. Severe hyperemesis gravidarum often causes weight loss
The prevalence of the eating disorders (EDs) anorexia and poor weight gain and may be particularly detrimental in
nervosa (AN), bulimia nervosa (BN) and binge eating individuals who already have low starting body weight.8 It
disorder (BED) in the nonpregnant population has been can also be difficult to distinguish between vomiting in early
suggested as 9.2%, falling to between 5.1% and 7.5% during pregnancy and symptoms of ED. Inadequate nutritional
pregnancy.4 Women with AN are most likely to be associated intake is – of course – essential to address and the
with low booking BMI, while women with BN and BED often involvement of dieticians can be useful. Appropriate
have a BMI within the normal range or higher and may be nutritional supplementation with thiamine and other
less likely to be detected during pregnancy. vitamins should also be considered.
The prevalence of ED is steadily increasing and (despite
common belief) female sufferers can conceive. For many
Body mass index
women, pregnancy confers some protection from the effects
BMI is the commonest surrogate marker of nutritional status of the condition. Poorer pregnancy outcomes have been
in studies of pregnancy. BMI was conceived as a tool for reported in women with AN and specialised support should
estimating body fat percentage. The ideal BMI range of be provided through an ED service, if relapse of symptoms
18.5–25 kg/m2 is itself based on the evidence of lower, all- occurs during pregnancy.9
cause mortality in this group. Bhaskaran et al. (2018)5 BMI usually reflects a combination of genetic potential and
analysed mortality data from over 3.6 million UK cases and environmental exposure. Yates et al. (2013)10 used data from
found the lowest mortality in the BMI range 21–25. They population databases in Utah to analyse the rates of low BMI
noted that while the greatest risk was associated with class phenotype among individuals with low BMI relatives. They
2 obesity and above, the projected life expectancy at age 40 found a relative risk (RR) of 2.21 (95% confidence interval
for BMI <18.5 was 4.3 years lower than for those with a [CI] 2.13–2.28) for adults with BMI <18.5 with a first-degree
healthy weight. Arguably, for an Asian population, the relative with low BMI, with a slightly stronger association in
normal BMI range (19–25 in adults) should be lower. This the age range 25–65 years (RR 2.57, 95% CI 2.42–2.72).
would have the effect of reclassifying Asian people with lower The relationship between BMI and socioeconomic factors
BMI as ‘normal’ and higher BMI as ‘overweight’.6 It may is complex. In poorer countries, low BMI has predominantly
also contribute to missing pathology affecting weight within been considered a marker of poverty and undernutrition,
the Asian population, because lower BMI is assumed to while in richer countries there is an association between
be normal. lower socioeconomic status and raised BMI.11 This
The construct of BMI is unable to describe the cause association does not represent a linear cause, however, as
of a low BMI. Any individual can be under weight for high BMI for women has been presented as a cause, rather
various reasons; for some it will represent their ‘normal’ than the result, of lower socioeconomic status.11 While a
genetic potential, whereas for others it will be the result healthy BMI has been associated with higher socioeconomic
of a pathological process such as malnutrition, hyperemesis, status, in their analysis of the UK population Bhaskaran
EDs or chronic illness. Many authors have drawn et al.5 did not find an association between low BMI (<18.5)
attention to the different confounding factors associated and socioeconomic status.
with extremes of BMI in different communities, including
socioeconomic factors.2,7
Neonatal outcomes
Pregnancy places increased metabolic demands on the
Causes of low body mass index
mother; therefore, maternal nutritional status is thought to
Table 1 summarises the causes of low BMI. be important in fetal growth. The Dutch famine cohort
In the initial assessment, treatable causes of low BMI study12 demonstrated that periods of starvation in pregnancy
should be excluded before arriving at a determination of an result in an increase in low-birthweight (LBW) babies (<2500
idiopathic low BMI. Do not assume that because someone is g). The Barker hypothesis (1995)13 argued that these effects
oriental or of Asian ethnicity, a BMI less than 19 is normal; have enduring implications for the future cardiovascular and
this may miss the fact that EDs and other morbid states metabolic health of the individual. Extremes of bodyweight
relating to low BMI occur in these populations too. are therefore considered to be risk factors for negative fetal

ª 2022 Royal College of Obstetricians and Gynaecologists. 51


Pregnancy in underweight women

Table 1. Causes of low BMI

Cause of Potential effects on Pregnancy effect on


low BMI pregnancy underlying cause Assessment

Constitutional Consider risk of Should gain weight normally Refer to obstetrician


(normal) growth restriction Positive effect and body image Assess nutritional status, e.g. fat distribution and appearance
and preterm delivery Assess eating habits
Assess mental state and wellbeing
Consider bloods for nutritional screen.
Consider growth scans

Malnutrition Increased risk of fetal Anaemia – mixed pattern Regular blood counts to assess for anaemia
growth restriction Inadequate weight gain Ferritin, B12 and folate levels if haemoglobin falls to provide
Preterm delivery adequate and appropriate replacement
Refer to dietician
Consider fortified drinks and multivitamins
Screen for vitamin D deficiency and provide appropriate
supplementation
Weigh at regular intervals during pregnancy to confirm weight gain
Growth scans

Eating disorder Growth restriction risk All the associations with Regular weighing during pregnancy
Potential risk of malnutrition, observe for Growth scans
microcephaly in ketonuria and consider renal Consider referral to eating disorder specialist or perinatal mental
toddlers and liver profiles if a health team
suspicion of laxative abuse Dietician referral and nutritional supplementation
or forced emesis Refer to for anaesthetic review
suspected Ensure drug doses are adjusted, depending on weight at the time of
Higher risk of osteopaenia prescribing
Risk of hypokalaemic alkalosis Refer and recommend bone scan once breastfeeding complete
with acute kidney injury if Communicate concerns with GP
severe purging and forced
emesis.

Consider Possible growth Advanced disease if treatment Full blood count, renal and liver profiles
malignancy restriction not considered or declined Tumour markers depending on suspected malignancy
Iatrogenic preterm because of pregnancy Ultrasound/CT/MRI/PET scanning
delivery Difficulty investigating and Multidisciplinary team and specialist surgical/oncology involvement
managing malignancy

Uncontrolled FGR, IUD, PET Treat in conjunction with maternal medicine or endocrine specialist
hyperthyroidism Miscarriage Growth scans
Preterm labour/
delivery

Abbreviations: CT = computed tomography; FGR = fetal growth restriction; IUD = intrauterine death; MRI = magnetic resonance imaging;
PET = positron emission tomography

outcomes, with implications far into adulthood. It is statistically significant increase in LBW, in both developed
recognised that fetal outcome follows a U-shaped curve and developing countries (RR 1.48, 95% CI 1.29–1.68, and R
with respect to maternal BMI, with a BMI between 20 and 25 1.52, 95% CI 1.25–1.85, respectively). Interestingly, the
being associated with the lowest risk of complications. association with preterm birth was only statistically
The most consistently reported effect of low maternal BMI significant in developed countries. This could be globally
in the literature is an increased prevalence of LBW babies and significant as most preterm births occur in developing
late prematurity (34–37 weeks of gestation). In a large countries and prematurity is responsible for most early
systematic review published in 2011, Han et al. (2011)7 neonatal deaths. Robillard et al. (2018)14 published an
analysed data from over 1 million pregnancies in both observational cohort study of nearly 60 000 term
developed and developing countries. They reported a pregnancies in Reunion and argued that, within the normal

52 ª 2022 Royal College of Obstetricians and Gynaecologists.


Burnie et al.

BMI range of 19–25, the appropriate number of neonates who have a low BMI caused by malnutrition or disease. This
were born as either large or small for gestational age. With challenges the current practice of not routinely weighing
increasing BMI, the number of larger babies increases, and pregnant women, at least at the extremes of the BMI range.
with lower starting BMI, there are higher rates of low Perhaps monthly weighing for these groups of women
birthweight babies. In 2013, Jeric et al. (2013)15 presented should be considered.
data showing that, on average, babies born to women with a In addition to LBW and late prematurity, there is some
BMI <18.5 weighed 163 g less. However, the authors make no evidence to suggest that suboptimal gestational weight gain
comment on whether these babies were growth restricted, or a low BMI elevates the risk of placental abruption. For
small for gestational age (SGA) or born prematurely. fetal development, some cohort work has suggested an
Knight-Agarwal et al. (2016)16 presented data from association between a low BMI and risk of atrial septal
Australia, which associated low BMI with a higher risk of defect, isolated congenital diaphragmatic hernia and
LBW and late preterm delivery, but without any increase in gastroschisis.23,24 Neither causality nor the potential
neonatal morbidity. Sebire et al. (2001)17 published a aetiology of these associations has been established.
retrospective population study based on maternity records Most studies7,21 show a small but significant tendency for
in northwest London of 200 000 pregnancies. They found an women with a lower pre-pregnancy BMI to have smaller
increase in LBW and late prematurity, but noted that the data babies and late preterm deliveries. However, most of these
do not allow adequate analysis of potential confounders, such studies acknowledge difficulties in accounting for the effect of
as socioeconomic status and smoking. Sebire et al.17 also confounders associated with low BMI, particularly
discuss the clinical significance of this increase in LBW. The socioeconomic status. The value of BMI in Asian
observed shift in a normal distribution of fetal birthweight to populations has been challenged and analysis of low BMI
the left, they argue, probably represents a higher rate of women in exclusively Asian subgroups has not shown the
constitutionally small babies rather than growth restriction: same associations as in other groups. The concept of a
“[this shift in the normal distribution] suggests that intrinsic constitutionally low BMI, rather than a BMI that is
maternal control of fetal size correlating with maternal size inappropriately low because of a secondary cause, is also
occurs in such pregnancies, rather than a higher prevalence of important in terms of stratifying risk. The 2009 Institute of
utero-placental insufficiency resulting in intrauterine Medicine (IOM) recommendations on weight gain during
growth restriction”. pregnancy22 provide an adjunct for assessing adequate
Williams et al. (2010)18 demonstrated a reduction in nutritional status during pregnancy, rather than relying on
stillbirth risk with low BMI mothers, correlating with a just pre-pregnancy BMI.
reduction in the number of missed cases of fetal growth Guidance published in 2013 by the Royal College of
restriction. This perhaps intimates that increased surveillance Obstetricians and Gynaecologists (RCOG) on SGA25
in this group of women might protect against the risk fetal recognises BMI <20 as a minor risk factor for SGA, but
growth restriction and, crucially, if growth restriction were to considers the effect on size to be the same as being
occur in pregnancy, it is less likely to be missed. These overweight and less than that of being obese.
considerations are important if screening is instituted based
on low BMI as a risk factor.
Maternal implications and associations
Women with a low BMI are not a homogeneous group and
Healthy weight
being underweight may reduce the risk of various antenatal
Several papers have challenged the association between LBW and intrapartum complications.
and prematurity.19,20 It has been suggested that gestational Antenatally, women with a low BMI are less likely to
weight gain is a better marker of adaptation to the demands develop gestational hypertension, pre-eclampsia and
of pregnancy than BMI in isolation. Zanardo et al. (2016)21 gestational diabetes.2,17 They are also less likely to deliver
showed that pregnant women with normal gestational large-for-gestational-age babies and are significantly less
weight gain (as defined by guidance published in 2009 by likely to need delivery by caesarean section (whether
the Institute of Medicine),22 there was no increase in LBW emergency or elective). There is some evidence that
but a reduction in both fetal macrosomia and various postpartum haemorrhage rates are lower, as are rates of
maternal complications. If low BMI is the consequence of instrumental deliveries. Conversely, tocophobia may be part
chronic malnutrition caused by poverty, then the mother is of the underlying reason why a woman with low BMI might
less likely to gain adequate weight during the pregnancy request a caesarean delivery.
because of the continuing stresses of her environment. The Antenatal anaemia appears to be commoner in this
inclusion of gestational weight gain is another method for group;17 there is also evidence that underweight women are
separating cases of ‘healthy’ low BMI women from those at higher risk of obstetric anal sphincter injuries (OASI),

ª 2022 Royal College of Obstetricians and Gynaecologists. 53


Pregnancy in underweight women

although this is not uniformly seen in all cohorts. birthweight (less than 100 g in all but one study).19 Women
Underweight women also have an increased number of with very low BMI may benefit from dietician review and a
admissions in pregnancy (compared with women of normal prescription of fortified drinks.
weight), but fewer admissions than obese women.
Change in body shape and weight gain in pregnancy may Fetal surveillance
trigger relapse for ED. Cohort studies have shown trends Given the association with LBW babies, consideration of
towards an increase in relapse of ED postpartum, especially in additional fetal monitoring is warranted. RCOG guidance25
the first 6 months. This group of women is also at higher risk views BMI <20 as a minor risk factor for an SGA baby and, in
of postpartum depression and obsessive-compulsive disorder. isolation, would not recommend additional growth scans.
However, it may be pragmatic to consider additional growth
scans if the BMI was <19, given the wider clinical context.
Management
Certainly, concerns about poor gestational weight gain would
General considerations suggest a benefit of increased fetal surveillance.
Management of underweight women in pregnancy should be
holistic and guided by the underlying aetiology of the low
Management of women with eating
BMI. The BMI at booking should be used as part of the
disorders
screen to stratify a woman’s risk and to determine the type of
care she and her baby will need throughout the pregnancy Pre-conception counselling should ideally be offered to
and beyond. women with ED. Women with active EDs should be
Where there is an organic cause for being underweight, the treated and in remission before seeking to become pregnant.
appropriate multidisciplinary team (MDT) should be Enquiry should be made about the use of appetite
involved, with the obstetrician and midwife working with suppressants, laxatives or diuretics, which may be harmful
the teams to provide the best pregnancy outcome. in pregnancy. EDs can go undetected in primary care and
Appropriate gestational weight gain is important for good women with ED may be reluctant to disclose symptoms to
fetal outcomes in underweight women. However, in the healthcare providers. The first antenatal visit or obstetric
absence of any randomised clinical trial (RCT) evidence of a appointment is an opportunity to screen for their presence,
beneficial effect on pregnancy outcomes, NICE guidance1 so obstetricians should be aware of the signs suggestive of an
suggests that repeated weight measurements during underlying ED. In addition to a low BMI, difficulties
pregnancy should be confined to circumstances in which conceiving related to oligomenorrhoea or amenorrhoea, a
clinical management is likely to be influenced. lack of weight gain, hyperemesis or psychological problems
There is debate about the application of the IOM might raise suspicion of an underlying ED. Physical
guidelines22 on appropriate gestational weight gain to a examination may further help to differentiate a
multi-ethnic population. The guidelines advise an increased constitutionally thin, healthy woman from one with an
gestational weight gain of 12.5–18 kg for underweight women underlying ED. Signs may include nail damage or calluses
compared with 11.5–16 kg for normal weight women and 5– across finger joints from induced vomiting, thinning of hair
9 kg for obese women.1 or fine facial hair (lanugo), dental problems including enamel
erosion, and dry skin. Parotid enlargement (‘hamster sign’)
Nutritional advice can also suggest self-induced vomiting.
Individual energy requirements during pregnancy vary Ideally, women with a suspected or disclosed ED should
greatly, so it is difficult to stipulate a rigid calorie intake. book with an obstetrician with an interest in EDs and be
However, dieticians usually recommend an extra 200 kcal referred early to a specialist ED service. Liaison for this can
each day in the third trimester of pregnancy for all women.26 often take place through the local perinatal mental health team.
Advice on gaining weight safely includes the use of healthy It is essential to discuss with the woman how she is
high calorie foods such as porridge, nuts and whole milk. responding to her pregnancy and her thoughts about the
This should be given alongside standard advice on what effect that pregnancy weight gain may have, and does have,
constitutes a healthy diet, including basing meals on starchy on her, as an assessment for body dysmorphic disorder
carbohydrates, the need for five portions of fruits and (BDD). Early education is required on expected body shape
vegetables per day, with adequate daily protein intake. changes and the importance of ensuring adequate nutrient
Consideration needs to be given to iron, folic acid, vitamin intake for fetal wellbeing. Ceasing harmful behaviours, such
D and calcium supplementation, as with all pregnant women. as binge eating, self-induced vomiting, laxative use and
Additional supplementation of micronutrients is not usually excessive exercise should be encouraged and supported. In
required and should be dietician-led. Carbohydrate-rich addition, should psychological therapy be required, referrals
supplements had surprisingly modest effects on increasing should be dealt with quickly, during pregnancy.

54 ª 2022 Royal College of Obstetricians and Gynaecologists.


Burnie et al.

Advice on portion size, having regular structured meals managed with appropriate psychological input and requires
and not missing breakfast may be required. Longitudinal careful handling. Elective caesarean section is not necessarily
work in women with ED has found an increase in anaemia the most appropriate treatment and individualised
associated with deficiencies in vitamin and mineral intake, so assessment and management is key in these cases.
additional nutritional supplements should be considered, There is very limited good-quality evidence in management
depending on the anaemia and nutritional screen. approaches for comorbid disorders. However, current
literature suggests that the disorders should be treated
simultaneously, addressing underlying factors that are
Women with a dual diagnosis
common to both, such as difficulties with emotional
Pregnant women with an ED who have a dual diagnosis, such regulation (personality disorder), through a multidisciplinary
as a coexisting substance misuse disorder or other mental approach.30 Treatment may need to involve medical
illness, present additional management challenges. stabilisation in cases of severe ED, concurrently with
Frequently encountered comorbidities include depression, psychological treatments including cognitive behavioural
anxiety disorder and obsessive-compulsive disorder, alcohol therapy (CBT) and psycho-education. Antidepressants may
and substance misuse. It is therefore extremely important to have a limited role and should not be used in isolation.27
ensure that appropriate note is taken of the Whooley An extreme manifestation of AN can be hypokalaemic,
questions27 for these women as a screening tool for alkalotic renal failure, related to forced emesis accompanied
accompanying mood disorders. The use of the AUDIT-C by laxative misuse. This will require MDT management with
alcohol screening tool28 may also be indicated from the appropriate physician input as well as the ED team.
history and presentation.
Rates of substance misuse in individuals with EDs can be
Investigations
as high as 50%. There is a clear need to screen and, if
substance misuse is suspected, consent should be sought Table 2 summarises the investigations that may be required
from the woman for urine toxicology or hair strand testing. for low BMI.
Women with a dual diagnosis have poorer treatment
outcomes, increased complications, longer recovery times
and higher relapse rates.29 Caffeine, stimulants including
amphetamines, laxatives, and thyroid medication may be Table 2. Investigations for low BMI
used for appetite suppression, to aid weight loss or provide Parameter Investigations
energy. In addition, alcohol and other psychoactive
substances may be used for emotional regulation or in the
context of impulsive behaviours. Although the literature Baseline tests for Full blood count, renal profile, bone profile, liver
suggests separate aetiologies for ED and substance misuse low BMI profile

disorders, any shared common risk factors should be In presence of Ferritin, vitamin B12, folic acid (methyl malonic
explored; for example, traumatic childhood experiences. anaemia acid)
Dual diagnosis may also include BDD, a condition in (haemoglobin
<105 g/L)
which the sufferer considers part or all of their body to be
flawed, leading to anxiety and behaviours that focus on the Low threshold Vitamin D assay
perceived flaw. This presentation would warrant referral to
the perinatal mental health service for further psychological Low potassium ECG  chest X-ray – risk of cardiac arrhythmia
input and management with psychological support or
BMI <19 Consider regular weight minimum once each
medication – often antidepressants. trimester or monthly
Common to these disorders is potential resistance to
treatment and a reluctance to divulge symptoms because of Urinalysis Ketonuria may suggest purging and forced
emesis or starvation
feelings of guilt or shame. Obstetricians and midwives must
be prepared to ask difficult questions and be open to explore Arterial or venous Look for alkalosis, high pH and low potassium
these issues without judgement. blood gas
Other management challenges can include which service to
Postnatal bone Consider suggesting this to GP beyond 3 months
lead care (for example, substance misuse agencies or perinatal scan postnatal to assess bone density and risk of
mental health). Effective communication between members continuing osteopaenia/osteoporosis
of the multidisciplinary team is crucial.
Tocophobia may present as part of this constellation of Abbreviations: BMI = body mass index; ECG = electrocardiography;
symptoms. This psychological comorbidity should be GP = general practitioner

ª 2022 Royal College of Obstetricians and Gynaecologists. 55


Pregnancy in underweight women

‘Healthy Start’ vouchers are available to all pregnant women


Weight loss in pregnancy
under the age of 18 and to those over 18 who are in receipt of
Very occasionally, true weight loss is seen during pregnancy; state benefits. These can be spent on milk, fruit or vegetables.
however, this is very rare, even with women with ED. Weight Healthy Start vitamins for pregnant women (containing folic
loss can occur as part of the somatic signs and symptoms of acid and vitamins C and D) are also available. Women with
depression, but organic causes should be excluded. With the limited access to healthcare because of immigration status or
reproductive age shifting to the higher end of the range, language barriers also represent a vulnerable population
investigations to exclude cancer in pregnancy may be requiring additional input to ensure their nutritional needs
necessary. Stage 4 bowel cancer can occur in women of are met. These may be overlooked if it is assumed that their
normal reproductive age and has been described low BMI is associated with ethnic origin; indeed, this can be
during pregnancy. considered a form of systematic racism.
Other chronic conditions associated with weight loss, for
example, inflammatory bowel disease (IBD), can present for
Postnatal care
the first time in pregnancy.
Table 3 summarises the care that should be given to women
with low BMI postpartum.
Safeguarding
Depending on the aetiology, women with a low BMI may be
Conclusions
vulnerable adults who will require additional input from
safeguarding teams and social care to ensure that they and Women with a low BMI are a complex, heterogeneous group.
their unborn children are protected from abuse, harm or Booking BMI should be considered a screen for organic
neglect. An appropriate level of enquiry is needed to disease, EDs and other mental health issues, and used to
determine the wider socioeconomic context of their highlight women requiring additional, or multidisciplinary
pregnancy. For example, a pregnant woman with housing antenatal care, related to their complexity. An appropriate
issues might not have anywhere to cook. Women with level of enquiry into the socioeconomic context of their
limited access to their own financial means, perhaps because pregnancy is essential.
of unemployment, poverty or in the context of abusive While there is risk associated with low birthweight,
relationships, might find it difficult to buy food. In the UK, appropriate gestational weight gain may be more important

Table 3. Postnatal care

Expected neonatal
Presentation birthweight Level of postnatal care

Low booking BMI but Neonatal birthweight Normal postnatal care


appropriate weight most likely in normal
gain in pregnancy range

Low BMI (or weight Likely normal neonatal Support from primary care and multidisciplinary team managing cancer diagnosis.
loss) and malignancy birthweight Support breastfeeding until cancer treatment makes untenable

Low BMI and eating Increased risk of LBW Enhanced postnatal support such as early intervention health visiting31
disorders Assist with breastfeeding32
Observe for deterioration of mental health, particularly obsessive-compulsive
disorder/postnatal depression
Risk of resurgence of eating disorders33,34
Consider a MARF to social care/early intervention health visitor

Low BMI and Increased risk of LBW MARF to social care/involve no recourse service, if applicable
malnutrition Early intervention health visiting
Provide supplements and vitamins and fortified drinks
Communicate concerns to primary care
Postnatal depression related to social complexity

Abbreviations: BMI = body mass index; LBW = low birthweight; MARF = multi-agency referral.

56 ª 2022 Royal College of Obstetricians and Gynaecologists.


Burnie et al.

in determining fetal outcomes and may help clinicians to detect 14 Robillard PY, Dekker G, Boukerrou M, Le Moullec N, Hulsey TC. Relationship
between pre-pregnancy maternal BMI and optimal weight gain in singleton
women who would benefit most from serial growth scans. pregnancies. Heliyon 2018;4:e00615.
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Disclosure of interests 17 Sebire NJ, Jolly M, Harris J, Regan L, Robinson S. Is maternal underweight
There are no conflicts of interest. really a risk factor for adverse pregnancy outcome? A population- based
study in London. BJOG 2001;108:61–6.
18 Williams M, Southam M, Gardosi J. Antenatal detection of fetal growth
Contribution to authorship restriction and stillbirth risk in mothers with high and low body mass index.
SC instigated and edited the article. RB researched and wrote Arch Dis Childhood Fetal Neonatal Ed 2010;95:Fa92.
19 Torloni MR, Betran AP, Daher S, Widmer M, Dolan SM, Menon R, et al.
the article; EG wrote and researched the article. All authors Maternal BMI and preterm birth: a systematic review of the literature with
approved the final version. meta-analysis. J Matern Fetal Neonatal Med 2009;22:957–70.
20 Parker MG, Ouyang F, Pearson C, Gillman MW, Belfort MB, Hong X, et al.
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ª 2022 Royal College of Obstetricians and Gynaecologists. 57


DOI: 10.1111/tog.12787 2022;24:40–9
The Obstetrician & Gynaecologist
Review
http://onlinetog.org

Accessory cavitated uterine malformations (ACUMs): an


unfamiliar cause of dysmenorrhoea
Thulasi Setty MBChB MRCOG,
a
* Joel Naftalin MBChB MRCOG MD,
b
Davor Jurkovic FRCOG MD
b

a
Clinical Research Fellow in Gynaecology Ultrasound, Institute for Women’s Health, University College Hospital, London, UK
b
Consultant Gynaecologist, Institute for Women’s Health, University College Hospital, London, UK
*Correspondence: Thulasi Setty. Email: thulasi.setty@nhs.net

Accepted on 4 January 2021. Published online 18 January 2022.

Key Content Learning Objectives


 Accessory cavitated uterine malformations (ACUMs) are isolated  To know what ACUMs are and recognise them as a cause of
cavitated lesions within the lateral aspect of the myometrium, dysmenorrhoea and pelvic pain.
inferior to the attachment of the round ligament.  To be able to diagnose an ACUM with the use of ultrasound, MRI
 They are a rare M€ ullerian anomaly and are increasingly recognised and histological findings if surgically excised.
as a cause for severe dysmenorrhoea and pelvic pain.  To be able to counsel patients with ACUMs on the different
 ACUMs can be diagnosed with ultrasound and magnetic management options, including conservative, medical and surgery.
resonance imaging, where they appear as well-defined lesions
Ethical issues
with a central cavity containing haemorrhagic content,  All women with ACUMs are currently offered surgical excision,
surrounded by a myometrial mantle. On histological
but is it appropriate to offer this, to patients as young as 13 years
examination, the cavity is lined by functional endometrial glands
old, with no long-term data on the effect of surgery on
and stroma.
 Recognised treatments include hormonal suppression,
future fertility?
destruction of the endometrial lining by alcohol sclerotherapy, Keywords: accessory cavitated uterine malformation (ACUMs) /
or complete surgical excision, which has demonstrated dysmenorrhoea / juvenile cystic adenomyoma / M€
ullerian
curative results. anomaly / painful periods

Please cite this paper as: Setty T, Naftalin J, Jurkovic D. Accessory cavitated uterine malformations (ACUMs): an unfamiliar cause of dysmenorrhoea. The
Obstetrician & Gynaecologist 2022;24:40–9. https://doi.org/10.1111/tog.12787

series of four of their own cases. In 2012, the same authors


Introduction
coined the term ‘ACUM’ to describe these lesions, which –
Accessory cavitated uterine malformations (ACUMs) are until then – had no agreed name.3 Subsequent advances in
increasingly recognised myometrial lesions. They are imaging have allowed more detailed examinations of uterine
considered a rare but significant cause of severe architecture – more specifically, the myometrium – thereby
dysmenorrhoea, often in young women. ACUMs are increasing visualisation of this important but relatively
isolated cavitated lesions located within the lateral aspect of unknown pathology. This review summarises the existing
the myometrium, inferior to the attachment of the round literature on ACUMs, in particular demographics, clinical
ligament of the uterus. They are considered to be of presentation, diagnostic imaging and available treatment
embryological origin.1 The earliest description of an ACUM options, to increase knowledge and aid better detection of
was by Oliver2 in the early 20th Century: a patient presenting ACUMs in everyday clinical practice.
with dysmenorrhoea underwent surgical excision of a
tumour from the broad ligament, which was described as
Epidemiology
“a globular-shaped closed sac, containing chocolate-coloured
fluid, thick-walled and lined by cuboidal epithelium, which Currently, the literature on ACUMs is limited to case reports
resembled very closely the stroma of normal and case series and there have been no formal prospective
endometrium” (Figure 1).2 studies of the condition. The prevalence is therefore
Until 2010, there had only been occasional case reports in unknown, although, based on the scarcity of reported cases,
the literature describing this phenomenon. Then, Acien it is probably a rare abnormality. Possible reasons for the
et al.1 published a literature review of ACUMs alongside a paucity of evidence include poor recognition of the condition

40 ª 2022 Royal College of Obstetricians and Gynaecologists.


Setty et al.

Figure 1. A schematic demonstration of a uterus and ACUM within the right broad ligament from the original description published by Oliver
et al. in the Lancet in 1912.(2) B.L = broad ligament; F.T. = fallopian tube; R.L. = round ligament.

among gynaecologists, radiologists and sonographers; other authors have expressed concern that the term ‘mass’
variable quality of ultrasound, which remains the primary can have sinister connotations for patients. The term
diagnostic tool in gynaecology; and challenges in reaching ‘malformation’ has been proposed as a more specific and
a diagnosis. appropriate alternative, which might avoid unnecessary
Some authors have proposed that ACUMs can only be worry for what is, in fact, a benign lesion.8
diagnosed in women under the age of 30 years.3,4 However,
while 84% (78 out of 93 cases) of the reported cases are in
Aetiology
women under the age of 30 years, there are published cases of
ACUMs in older women.1–3,5–8 It has been suggested that the early occurrence of pain
The literature reveals a preponderance of cases in Japan, symptoms after menarche is evidence that ACUMs are a
with 16 out of 93 (17%) cases published by authors from congenital rather than acquired malformation.13 While the
Japan.4,9–14 This probably reflects increased clinician precise origin of ACUMs remains uncertain, all authors agree
awareness of the condition in Japan rather than a genuine that they represent a M€ ullerian duct abnormality.1,3 There are
increased prevalence of the condition within this population. two theories about how they develop: that they represent an
isolated M€ ullerian duct malformation, or a dysfunction of
the female gubernaculum.1
Nomenclature
During the fifth and sixth weeks of embryological
Various terms have been used to describe what we now call development, the genital system is indifferent and exists as
‘ACUMs’. These include ‘juvenile cystic adenomyoma’,4,9,13– two pairs of genital tracts: the mesonephric (Wolffian) ducts
24
‘isolated cystic adenomyoma’,5,10–12,25,26 ‘uterine-like and paramesonephric (M€ ullerian) ducts. Absence of
mass’,27,28 or ‘accessory uterine cavity’.2,29,30 In 2010, Acien testosterone cause the Wolffian ducts to regress in female
et al. reviewed the literature to determine how many embryos. The M€ ullerian ducts persist, fuse at the caudal end
published cases represented true ACUMs. Eighteen clinical and extend cranially with a central cavity, eventually forming
cases met their proposed criteria, as outlined in Box 1.1 a functional uterus.31 The unfused lateral arms form the
Initially termed as an ‘accessory cavitated uterine mass’,3 fallopian tubes.31 Remnants of the M€ ullerian ducts can lead
to congenital uterine anomalies, thus supporting the theory
that the origin of ACUMs might be associated with the
Box 1. Diagnostic criteria of ACUMs duplication and persistence of a M€ ullerian duct segment at
the level of the attachment of the round ligament.1
Location: The embryological female gubernaculum persists as the
 Solitary lesion located in the lateral myometrium or broad ligament round ligament of the uterus.32 Acien et al.32 hypothesise
 No communication with uterine cavity or fallopian tubes that the female gubernaculum is probably formed by muscle
Morphology:
fibres that are not derived from either the mesonephric or
paramesonephric ducts. They believe the attachment of the
 A cavitated lesion containing functional endometrium surrounded
gubernaculum to the M€ ullerian ducts induces the fusion and
by a myometrial mantle
normal development of the uterus. The fact that all published
Histology: cases of ACUMs describe their location in the insertion area
 Cavitated lesions filled with dark brown haemorrhagic content
or pathway of the round ligament substantiates this theory
 Lined with functional endometrium that ACUMs derive from maldevelopment of
 Myometrial mantle has concentric organisation of smooth muscle the gubernaculum.1,3,13,32,33

ª 2022 Royal College of Obstetricians and Gynaecologists. 41


Accessory cavitated uterine malformations

(TRUS) is an acceptable alternative. This is usually well


Clinical presentation
tolerated and has comparable image quality to TVUS.37
Severe dysmenorrhoea is the commonest presenting While some authors have described only requiring TVUS
symptom for women with ACUMs.3,7,12,13,15,23,34,35 The to make the diagnosis,8 quality of ultrasound remains highly
pain can be central or ipsilateral to the side of the ACUM variable. This is reflected in the literature, where most
and may be accompanied by chronic pelvic pain.1,3,8,21,28,34 authors routinely use additional imaging modalities to
The pain is thought to be caused by an accumulation of confirm the ACUM diagnosis.34,36
menstrual fluid from the functioning endometrium lining the
ACUM within what is an enclosed space. This would lead to Magnetic resonance imaging
increased pressure within the ACUM and subsequent Most published case reports and cases series of ACUMs have
stretching of the cavity.3,9,13,19,26,27 Pain often persists or been investigated using magnetic resonance imaging (MRI).
even increases after the onset of menstruation.34 Other MRI examinations include axial, coronal and sagittal T2-
symptoms reported by patients diagnosed with ACUMs weighted turbo spin echo images, T1-weighted spin echo
include dyspareunia1,4 and hypogastric pain,1,3 although it is images and axial fat suppressed T1-weight images with 3–4-
uncertain whether the ACUM was the primary cause of these mm section thickness. This ensures exclusion of M€ ullerian
symptoms. Currently, there are no descriptions of anomalies by clearly visualising both cornua.34 Peyron et al.34
asymptomatic ACUMs in the literature. Potential reasons concluded that all ACUMs could be identified on MRI as ‘a
for this might include challenges to diagnosis, and the functioning and non-communicating accessory horn, present
combination of a perceived requirement for histology to within the external myometrium or broad ligament in an
confirm diagnosis alongside the lack of an indication to otherwise normal uterus’. All ACUMs were found to have a
excise an asymptomatic lesion. Nevertheless, asymptomatic central cavity, each surrounded by a well-defined ring with
ACUMs are feasible and future prospective observational low T1 and T2 signal enhancements, which is similar to that
studies might confirm that a proportion cause no pain. There of the junctional zone.34 The surrounding cyst wall or
are no published data to suggest that ACUMs are associated myometrial mantle is seen as thickened and hypointense
with menorrhagia or subfertility, and ACUMs have been tissue on T2-weighted images, which demonstrates
diagnosed in parous women. Some authors have described a myometrial hypertrophy (Figure 3).26 In addition, the
clinically palpable, tender mass on bimanual vaginal cavities had a thin inner lining that moderately enhanced
examination, which could be mistaken for a fibroid or after gadolinium contrast and appeared hyperintense on T2-
ovarian cyst.1,13,25 weighted images, indistinct from endometrium.34 The
internal content of the cavities displayed high T1 signal
intensity, which remained after fat saturation and is
Investigations
indicative of haemorrhagic content.4,19,26,34,36 Some lesions
Ultrasound also displayed T2 shading, which is similarly seen
Transvaginal ultrasound (TVUS) remains the first-line with ovarian endometriomas, again confirming the
imaging tool in gynaecology, so it is particularly important haemorrhagic content of ACUMs.34 All cases had normal
to increase awareness of the ultrasound features of ACUMs. uterine cavities and no concomitant uterine or renal
ACUMs appear on ultrasound as well-circumscribed, tract anomalies.1,3,26,34,36
spherical, cavitated lesions, with a myometrial mantle and
echogenic fluid content (Figure 2).8,24,36 They are Assessment of uterine morphology
characteristically located in one of the lateral aspects of the Many authors have stated that an ACUM diagnosis can only be
anterior myometrium, inferior to the presumed insertion site made in the presence of a normal uterine cavity and once an
of the round ligament.8 The fluid content can either be obstructive congenital uterine anomaly has been excluded.1,3,4
‘ground glass’ in nature, like the typical appearance on Both hysterosalpingography (HSG) and hysteroscopy have
ultrasound of the contents of endometriomas, or been used to confirm a normal uterine cavity and fallopian
hyperechoic.3,4,7,8,14 The contents, being fluid, should be tubes in this population.4,7,10,12,13,15,21,34,38 Nevertheless,
avascular on Doppler examination, and the blood flow in the numerous other imaging modalities can be used to assess
myometrial mantle should be no different to the Doppler the uterine cavity, including 2D and 3D ultrasound,
assessment of the surrounding myometrium.8 ACUMs can be saline infusion sonohysterography (SIS), hysterosalpingo-
mistaken for obstructed congenital uterine anomalies, so two contrast-sonography (HyCoSy), MRI, and laparoscopy and
normal interstitial portions of the fallopian tubes must be dye test.39,40 Where there is no clear evidence to determine
visualised to confirm diagnosis. If TVUS is a relative or superiority of imaging modality, local preference will
absolute contraindication, a transrectal ultrasound scan determine the choice.

42 ª 2022 Royal College of Obstetricians and Gynaecologists.


Setty et al.

(a) (b)

(c) (d)

(e)

Figure 2. Location and anatomy of ACUM. Transverse transvaginal ultrasound image of uterus and an ACUM in the left lateral myometrium (a).
The ACUM (yellow arrow) can be seen lateral and inferior to the interstitial portion of the left fallopian tube (red arrow) and uterine cavity (white
arrow). Note the echogenic contents of ‘ground glass’ appearance within the ACUM. (b) Hyperechoic cavity content within the ACUM (yellow
arrow) on transverse transvaginal ultrasound image. (c) Transvaginal ultrasound image of a Doppler examination of an ACUM. Note the presence
of vascularity within the myometrial mantle, but absence within the cavitated part of the lesion. The structure of an ACUM is illustrated in images
(d) and (e), showing a central cavity ’C’, hyperechoic internal lining – similar to that of endometrium (yellow border) and a surrounding myometrial
mantle (MM, red border).

Intraoperative diagnostic features


Diagnosis of an ACUM is rare and often delayed. There are
documented cases of women with ACUMs undergoing
numerous diagnostic laparoscopies to investigate symptoms
of severe dysmenorrhoea and pelvic pain that failed to
diagnose the ACUM.1,8,17,27 ACUMs can be difficult to see
and are often missed if not actively looked for, with the
uterine contour being described as being entirely normal at
laparoscopy or even during laparotomy in some cases.11 In
most cases, an ACUM appears as an asymmetrical, often
subtle enlargement on the right or left lateral aspect of the
uterus, inferior to the insertion of the round ligament and
classically contains altered blood, which appears as dark
Figure 3. MRI of an ACUM. T2- weighted axial high-resolution MRI brown fluid.1,3,8,15,34 Intraoperative ultrasound examination
image showing the presence of an ACUM in the left lateral
can successfully locate the ACUM and aid excision from the
myometrium of the uterus (yellow arrow) with a normal uterine
cavity (white arrow). surrounding myometrium.8,10,11

ª 2022 Royal College of Obstetricians and Gynaecologists. 43


Accessory cavitated uterine malformations

Histology modalities such as high-resolution TVUS and pelvic MRI, it


Macroscopically, ACUMs have a ‘uterus-like’ organisation, can be difficult to differentiate ACUMs from other more
with a central cavity lined by endometrium and surrounded by common pathologies. The presence of a morphologically
a myometrial mantle.13 The largest case series to date8 reported normal uterine cavity is one defining feature of an
the mean outer cavity diameter of the ACUM to be 22.8 mm ACUM.1,3,4,34 This is to differentiate ACUMs from
(95% confidence interval [CI] 20.9–24.8 mm) and the mean obstructive and non-obstructive congenital uterine
internal cavity diameter of the ACUMs to be 14.1 mm (95% CI anomalies, such as unicornuate uteri with a rudimentary
12.2–16.1 mm). These measurements are consistent with other horn (Figure 4), or Robert’s uterus, which is defined as a
studies reporting similar dimensions.4,34 septate uterus with a noncommunicating hemi-cavity.
Microscopically, the cavity is lined with glands and stroma, ACUMs can be difficult to differentiate from fibroids
which positively stain for CD10, estrogen receptors (ER) and located in the lateral aspect of the myometrium when they
progesterone receptors (PR) – indicators of normal have altered central contents; for example, if they have
endometrial tissue.4,34 Peyron et al.34 describe a well- undergone cystic, haemorrhagic or fatty degeneration
ordered concentric orientation of smooth muscle fibres in (Figure 5).19,34 However, central degeneration rarely occurs
their surgically resected ACUM cases, which differentiates in fibroids of a similar size to ACUMs. Furthermore, fibroids
them from cystic adenomyosis, where the smooth fibres are that have undergone haemorrhagic degeneration can be
more disordered.8 Many authors report small foci of distinguished from ACUMs on MRI, because accumulation
adenomyosis within the myometrial mantle.1,3,4,10,14,36 of methaemoglobin in the obstructed veins at the periphery
of a fibroid with haemorrhagic degeneration produces a rim
that is hypointense in both T1- and T2-weighted images.19
Differential diagnoses
Up until 2010, many ACUMs were termed ‘juvenile cystic
Diagnosing ACUMs can be challenging, primarily because adenomyomas’ and treated as a rare form of adenomyosis.
there is unfamiliarity among clinicians, but also because of There are, however, features that distinguish ACUMs from
various differential diagnoses. Despite advances in imaging true cystic adenomyomas, with regards to clinical

(a)
(b)

(c)
(d)

Figure 4. Differentiating an ACUM from a unicornuate uterus. These images demonstrate the difference between a unicornuate uterus with a
functioning, non-communicating rudimentary horn and an ACUM. (a) A 3D-rendered coronal view of a right unicornuate uterine cavity (UC) with a
functional, non-communicating rudimentary horn (RH) with haematometra secondary to obstructed outflow. This can also be seen on 2D
transvaginal imaging (b). This is in contrast with a normally shaped uterine cavity with two interstitial portions (I) of the fallopian tube seen on a 3D
rendered coronal view of the uterus containing an ACUM in the lateral myometrium (c) and on a 2D ultrasound transverse view of the uterus (d).

44 ª 2022 Royal College of Obstetricians and Gynaecologists.


Setty et al.

(a) (b)

Figure 5. Differentiating an ACUM from a uterine fibroid. Transverse view of the uterus on transvaginal ultrasound sound showing a subserous
fibroid on the left lateral aspect of the uterus (orange arrow in image (a)). In comparison to the ACUM in image (b) (yellow arrow), there is an
absence of cavitation with a hyperechoic lining depicting endometrium and lack of myometrial mantle.

(a) (b)

Figure 6. Differentiating an ACUM from a cavitating adenomyoma. This is a sagittal view of an anteverted uterus on transvaginal ultrasound scan
demonstrating a cavitating adenomyoma in the anterior myometrium (orange arrow in image (a)). In comparison to the ACUM in image (b)
(yellow arrow), there is a lack of myometrial mantle, it is contiguous with the endometrial-myometrial junction (EMJ) of uterine cavity (white arrow)
and its location is in the central, anterior aspect of the uterus in contrast to the lateral location of the ACUM.

presentation, ultrasonographic appearance, surgical findings


Treatment
and histopathology (Figure 6, Table 1).1
Congenital uterine cysts, another differential diagnosis of Expectant
ACUMs, are epithelial-lined myometrial cysts. Unlike Currently, all published research confirms the benign nature
ACUMs, they contain simple fluid that appears anechoic of ACUMs and, in asymptomatic women, they can be
on ultrasound, rather than blood, and their location managed expectantly. However, the natural history of
within the myometrium is variable. They also lack a ACUMs is not known because most reported cases were
haemosiderin rim on histological examination, whereas managed by excisional surgery. Prospective observational
ACUMs are lined with endometrium and have studies are required to gain a greater understanding of the
haemorrhagic content.19,41 natural history of the condition.
ACUMs can be mistaken for ovarian endometriomas,34
particularly because endometriosis is a diagnosis actively Medical
sought in young women presenting with severe Given that pain is the primary symptom of ACUMs, simple
dysmenorrhoea and pelvic pain. An endometrioma within analgesics such as nonsteroidal anti-inflammatory drugs
an ovary adherent to the lateral aspect of the uterus (a not (NSAIDs) can be used. Many authors, however, describe
uncommon finding in endometriosis), could easily be these as being inadequate for controlling pain.4,13,15,17,21,34,38
mistaken for an ACUM. There are, however, characteristic The use of suppressive hormonal treatments have been
features to distinguish ovarian endometrioma, including the described, including continuous use of the oral contraceptive
presence of surrounding follicles within the ovarian cortex pill,19,20,29,42 levonorgestrel-releasing intrauterine system
and the absence of a thick peripheral ring of muscular (Mirena)8 or gonadotrophin-releasing hormone
tissue (Figure 7).34 (GnRH).4,10–13,20,24,34 Naftalin et al.8 found most patients

ª 2022 Royal College of Obstetricians and Gynaecologists. 45


Accessory cavitated uterine malformations

Table 1. Differences between ACUMs and true cystic adenomyomas.

Characteristics ACUMs True cystic adenomyoma

Demographics Tend to affect younger, nulliparous women. Tends to affect older, multiparous women7

Clinical presentation Severe menstrual pain and no association with heavy periods Heavy, painful periods1

Concomitant pathology Tend to be isolated lesions3 Usually found alongside other features of adenomyosis

Macroscopic histopathology Distinct border between myometrial mantle and Irregular and poorly defined borders47
findings surrounding myometrium34

Microscopic histopathology Concentric organisation of smooth muscle around cavity Surrounding myometrium lacks organisation
findings Endometrial glands and stroma seen to line cavity8 Absence of internal epithelial lining of cystic cavity7

Location In the lateral myometrium, inferior to the insertion of the Variable location within the myometrium,
round ligament and separate and distinct from often within or contiguous with the
the endometrial-myometrial junction34 endometrial-myometrial junction47

(a) (b)

Figure 7. Differentiating an ACUM from an ovarian endometrioma. (a) Transverse view of a uterus with an enlarged left ovary adherent to the
lateral aspect containing a unilocular cyst (orange arrow) with echogenic ‘ground glass’ content. The cyst is surrounded by normal ovarian tissue as
illustrated by the presence of follicles. There is also an absence of a myometrial mantle as seen with an ACUM (yellow arrow) on image (b).

in their cohort wanted to avoid surgery in the first instance,


Sclerotherapy
with 10 out of 17 patients opting against primary surgery. Six
of these patients chose hormonal treatments, with most Reports on TVUS-guided aspiration and sclerotherapy for
achieving sufficient pain relief to defer or avoid surgery. ovarian cysts, including endometriomas, have been published,
ACUMs are often diagnosed in young teenage girls for whom with varied results.43,44 Alcohol sclerotherapy can be an
surgery may not be the best primary treatment option. alternative to surgery, or be indicated where medical treatments
Branquinho19 and Fissea42 both describe teenage patients have failed. However, with this approach, patients must be made
presenting with severe cyclical pelvic pain, who were found to aware it is not curative. They should also be counselled on the
have a cystic, haemorrhagic lesion within the lateral risks of symptom recurrence and the probable need for further
myometrium meeting diagnostic imaging criteria for an intervention. It is, however, less invasive and does not carry the
ACUM. They were both treated with continuous oral same risks as laparoscopy or laparotomy.
contraceptives, which achieved adequate pain relief at 6- Sclerotherapy aims to destroy the cavity lining, resulting in
and 12-month follow-ups. inflammation and fibrosis with eventual obliteration.45
Other authors have reported similar success with Ethanol (95–99% concentration), in particular, has been
hormonal treatments, specifically the oral contraceptive pill shown to combine cytotoxic damage, hypertonic cellular
and GnRH treatments. However, many patients experienced dehydration and coagulation and thrombosis in the presence
recurrence of symptoms when the treatment of blood products.45 Naftalin et al.8 used sclerotherapy as a
stopped.3,4,10–13,15,24,33,34,38 primary treatment for ACUMs in four patients and described

46 ª 2022 Royal College of Obstetricians and Gynaecologists.


Setty et al.

open surgery, for reasons including quicker recovery with


Box 2. Transvaginal sclerotherapy procedure for ACUMs reduced postoperative pain and the reduced incidence of
 Perform under general anaesthetic
adhesions.8 However, this requires advanced laparoscopic
 Under continuous transvaginal ultrasound guidance, insert an 18- skills, including the ability to suture laparoscopically.
gauge needle through the anterior vaginal wall and myometrium, Nevertheless, with more hysterectomies and myomectomies
into the ACUM being completed laparoscopically, more gynaecological
 Aspirate intracavitary fluid (usually 2–3 mL) and send for cytological
analysis
surgeons should be sufficiently skilled to perform
 Instil 99% ethanol into the cavity laparoscopic ACUM excision.
Dividing the round ligament has been proposed as a means
to clearly identify the ascending branch of the uterine artery to
reduced pain in the immediate follow-up. Two patients, reduce the risk of inadvertent injury.4,19,33,34 Dissection of the
however, later required surgical resection when pain uterovesical fold has also been cited to facilitate safe access to
resumed. Box 2 outlines the TVUS-guided sclerotherapy the laterally placed ACUM.33 Vasopressin infiltration into the
procedure for ACUMs. Recognised risks of sclerotherapy uterine–ACUM serosal interface to aid with haemostasis has
include peritoneal leakage of the instilled alcohol; however, been reported by almost all authors.4,6,7,10,11,13–17,38,46 The
this is unlikely with ACUMs because the cavity is surrounded overlying serosa is incised with monopolar energy4,6 and
by myometrium.44 ACUM enucleation is performed in a circumferential manner
There are currently no long-term follow-up data on the along the ACUM–myometrial interface with the use of bipolar
success of sclerotherapy of ACUMs. Data extrapolated from energy; in contrast to a myomectomy, where dissection
its use in the treatment of ovarian endometriomas suggests advances along a pseudocapsule.6 If the boundaries of an
recurrence rates of 0–62.5% in a meta-analysis of 1102 ACUM are unclear, intraoperative ultrasound has been
patients over 15 studies with follow-up of 1–24 months. Rate described to facilitate delineation of the lesion and to aid
of recurrence was largely influenced by the time of ethanol excision.8,13 Intraoperative ultrasound can also help to avoid
washing, with risk of cyst recurrence significantly higher in inadvertent breach of the uterine cavity. Peyron et al.34
those with ethanol washings lasting less than 10 minutes.44 concluded that the mean distance of the ACUM from the
uterine cavity was 6 mm on MRI, illustrating how easily a
Surgery uterine cavity can be breached during surgical excision. While
Nonsurgical treatments are important in the treatment of no studies have reported this complication, theoretical
symptoms secondary to ACUMs, not least because they are sequelae would include intrauterine adhesions, development
less invasive and carry fewer risks than surgical excision. of adenomyosis, and increased risk of future intrapartum
Nevertheless, most published cases of ACUMs have been uterine rupture. Authors have described intraoperative
treated surgically with high success rates. All published cases assessment of the integrity of the uterine cavity post-excision
of surgery for ACUMs have reported almost complete using methylene blue dye chromopertubation.18,29,33,34
resolution of pain, with many patients remaining pain free ACUMs are benign lesions, so there is no recognised
until completion of follow-up.1,3,4,8,34,38 Excisions have been danger in spillage of the ACUM contents. They rarely exceed
performed both laparoscopically and by laparotomy. Acien 35 mm in mean diameter. Various techniques have been
et al.1,3 described performing a laparotomy for all eight of described for specimen retrieval, including the use of
their cases up until 2012. The operations were either excision colpotomy,4 morcellation10,15,23,46 and specimen
7,8,16,33
of the ACUM, or hysterectomy in those women with separate retrieval bags.
indications for hysterectomy. They described the advantage
of open surgery as being greater surgical precision, allowing Follow-up
better enucleation of ACUMs that can have indistinct surgical
planes.1,3 Given that ACUMs are close to important There is currently limited evidence to guide us on
structures such as the uterine artery, urinary bladder and appropriate follow-up of these patients. Both the natural
endometrial cavity, surgical precision of excision is of crucial history of ACUMs and the long-term impact of surgical
importance.33 Other authors, however, showed that excision remain unknown. Prospective longitudinal studies
sufficiently precise enucleation of the ACUM can be also are therefore required to further our understanding on
achieved at laparoscopy because of the image magnification whether they change with time, what impact they have on
and the use of fine dissection instruments. Combined with pregnancy and whether surgical excision has longer term
bidirectional blunt and sharp dissection, they achieved sequelae. Future research questions include how surgical
complete excision without spillage.33 Laparoscopic resection may affect fertility or pregnancy outcomes, and
enucleation of ACUMs has usually been favoured over whether a trial of labour is a safe option for these women.

ª 2022 Royal College of Obstetricians and Gynaecologists. 47


Accessory cavitated uterine malformations

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3 Acien P, Bataller A, Fernandez F, Acien MI, Rodrıguez JM, Mayol MJ. New
cyst of the uterus in an adolescent. Pediatr Radiol 2008;38:1239–42.
cases of accessory and cavitated uterine masses (ACUM): a significant cause
27 Liang Y-J, Hao Q, Wu Y-Z, Wu B. Uterus-like mass in the left broad ligament
of severe dysmenorrhea and recurrent pelvic pain in young women. Hum
misdiagnosed as a malformation of the uterus: a case report of a rare
Reprod 2012;27:683–94.
condition and review of the literature. Fertil Steril 2010;93:1347.e13–6.
4 Takeuchi H, Kitade M, Kikuchi I, Kumakiri J, Kuroda K, Jinushi M. Diagnosis,
28 David C, Burette J, Duminil L, Bonneau S, Janvier A, Hoeffel C, et al. Uterus-
laparoscopic management, and histopathologic findings of juvenile cystic
like mass: a case report. Eur J Obstet Gynecol Reprod Biol 2019;233:162–3.
adenomyoma: a review of nine cases. Fertil Steril 2010;94:862–8.
29 Potter DA, Schenken RS. Noncommunicating accessory uterine cavity. Fertil
5 Protopapas A, Milingos S, Markaki S, Loutradis D, Haidopoulos D,
Steril 1998;70:1165–6.
Sotiropoulou M, et al. Cystic uterine tumors. Gynecol Obstet Invest
30 Steinkampf MP, Manning MT, Dharia S, Burke KD. An accessory uterine
2008;65:275–80.
cavity as a cause of pelvic pain. Obstet Gynecol 2004;103:1058–61.
6 Peters A, Rindos NB, Guido RS, Donnellan NM. Uterine-sparing laparoscopic
31 Moore KL, Persaud T, Torchia M. The developing human: clinically oriented
resection of accessory cavitated uterine masses. J Minim Invasive Gynecol
embryology. 9th ed. Philadelphia, PA: Elsevier Saunders; 2012. p. 265.
2018;25:24–5.
32 Acien P, Sanchez del Campo F, Mayol M-J, Acien M. The female
7 Supermaniam S, Thye WL. Diagnosis and laparoscopic excision of accessory
gubernaculum: role in the embryology and development of the genital tract
cavitated uterine mass in young women: two case reports. Case Rep
and in the possible genesis of malformations. Eur J Obstet Gynecol Reprod
Womens Health 2020;26:e00187.
Biol 2011;159:426–32.
8 Naftalin J, Bean E, Saridogan E, Barton-Smith P, Arora R, Jurkovic D. Imaging
33 Bedaiwy MA, Henry DN, Elguero S, Pickett S, Greenfield M. Accessory and
in gynecological disease: clinical and ultrasound characteristics of accessory
cavitated uterine mass with functional endometrium in an adolescent:
cavitated uterine malformations. Ultrasound Obstet Gynecol
diagnosis and laparoscopic excision technique. J Pediatr Adolesc Gynecol
2021;57:821–8.
2013;26:e89–91.
9 Tamura M, Fukaya T, Takaya R, Ip CW, Yajima A. Juvenile adenomyotic cyst
34 Peyron N, Jacquemier E, Charlot M, Devouassoux M, Raudrant D, Golfier F,
of the corpus uteri with dysmenorrhea. Tohoku J Exp Med
et al. Accessory cavitated uterine mass: MRI features and surgical
1996;178:339–44.
correlations of a rare but under-recognised entity. Eur Radiol
10 Nabeshima H, Murakami T, Terada Y, Noda T, Yaegashi N, Okamura K. Total
2019;29:1144–52.
laparoscopic surgery of cystic adenomyoma under hydroultrasonographic
35 Garofalo A, Alemanno MG, Sochirca O, Pilloni E, Garofalo G, Chiado  Fiorio
monitoring. J Am Assoc Gynecol Laparosc 2003;10:195–9.
Tin M, et al. Accessory and cavitated uterine mass in an adolescent with

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severe dysmenorrhoea: From the ultrasound diagnosis to surgical treatment. 41 Brosens I, Gordts S, Habiba M, Benagiano G. Uterine cystic adenomyosis: a
J Obstet Gynaecol 2017;37:259–61. disease of younger women. J Pediatr Adolesc Gynecol 2015;28:420–6.
36 Jain N, Verma R. Imaging diagnosis of accessory and cavitated uterine 42 Fisseha S, Smith YR, Kumetz LM, Mueller GC, Hussain H, Quint EH. Cystic
mass, a rare mullerian anomaly. Indian J Radiol Imaging 2014;24: myometrial lesion in the uterus of an adolescent girl. Fertil Steril
178–81. 2006;86:716–8.
37 Timor-Tritsch IE, Monteagudo A, Rebarber A, Goldstein SR, Tsymbal T. 43 Kafali H, Eser A, Duvan CI, Keskin E, Onaran YA. Recurrence of ovarian cyst
Transrectal scanning: an alternative when transvaginal scanning is not after sclerotherapy. Minerva Ginecol 2011;63:19–24.
feasible. Ultrasound Obstet Gynecol 2003;21:473–9. 44 Cohen A, Almog B, Tulandi T. Sclerotherapy in the management of ovarian
38 Paul PG, Chopade G, Das T, Dhivya N, Patil S, Thomas M. Accessory endometrioma: systematic review and meta-analysis. Fertil Steril
cavitated uterine mass: a rare cause of severe dysmenorrhea in young 2017;108:117–24.e5.
women. J Minim Invasive Gynecol 2015;22:1300–3. 45 Albanese G, Kondo KL. Pharmacology of sclerotherapy. Semin Interv Radiol
39 Ludwin A, Pityn ski K, Ludwin I, Banas T, Knafel A. Two- and three- 2010;27:391–9.
dimensional ultrasonography and sonohysterography versus hysteroscopy 46 Panwar A, Davis AA, Lata K, Sharma S, Kriplani A. Laparoscopic
with laparoscopy in the differential diagnosis of septate, bicornuate, and management of accessory cavitated uterine mass: a report of two cases and
arcuate uteri. J Minim Invasive Gynecol 2013;20:90–9. review of literature. J Gynecol Surg 2020;36 [https://doi.org/10.1089/gyn.
40 Salim R, Jurkovic D. Assessing congenital uterine anomalies: the role of 2020.0019].
three-dimensional ultrasonography. Best Pract Res Clin Obstet Gynaecol 47 Bazot M, Deux JF, Dahbi N, Chopier J. Myometrium diseases. J Radiol
2004;18:29–36. 2001;82:1819–40.

ª 2022 Royal College of Obstetricians and Gynaecologists. 49


DOI: 10.1111/tog.12783 2022;24:31–9
The Obstetrician & Gynaecologist
Review
http://onlinetog.org

Cervical cancer in pregnancy: diagnosis, staging and


treatment
Tamara Howe MBBS MRCOG PGDipMedEd (Merit),a* Kate Lankester BM BCh MRCP FRCR PhD MAClinEd,b
Tony Kelly FRCOG, MD,c Ryan Watkins BMedSci BM BS MRCPCH,d Sonali Kaushik MBBS MRCOG MDe
a
Consultant in Obstetrics and Gynaecology, Division of Women’s and Children’s Health, Frimley Park Hospital, Portsmouth Rd, Frimley,
Camberley GU16 7UJ, UK
b
Consultant Oncologist, Sussex Cancer Centre, Royal Sussex County Hospital, Eastern Road, Brighton BN2 5BE, UK
c
Consultant in Obstetrics and Gynaecology, Division of Women’s and Children’s Health, Royal Sussex County Hospital, Eastern Road, Brighton
BN2 5BE, UK
d
Consultant Neonatologist, Division of Women’s and Children’s Health, Royal Sussex County Hospital, Eastern Road, Brighton BN2 5BE, UK
e
Consultant in Gynaecological Oncology, Division of Women’s and Children’s Health, Royal Sussex County Hospital, Eastern Road, Brighton BN2
5BE, UK
*Correspondence: Tamara Howe. Email: tamara.howe@nhs.net

Accepted on 12 April 2020. Published online 20 December 2021.

Key Content  To know the risks to the fetus in each trimester, with regard to the
 Cervical cancer is the commonest gynaecological malignancy various surgical and chemotherapeutic options available to treat
diagnosed in pregnancy. cervical cancer in pregnancy.
 Cancer symptoms may mimic complications of pregnancy, thus  To understand the psychological effects on a woman of a cancer
delaying diagnosis. diagnosis in pregnancy.
 Staging of cervical cancer in pregnancy is essential to determine an
Ethical Issues
individual management plan.  How should maternal and fetal risks be balanced while
 Treatment of cervical cancer in pregnancy is complex and depends
investigating and treating cervical cancer in pregnancy?
on the stage of cancer and the gestation of the pregnancy.
 Consideration of termination of pregnancy to allow timely
 Involvement of a multidisciplinary team is essential in the care of a
treatment, alternatively risking delay in treatment and progression
woman with cervical cancer in pregnancy.
of disease.
Learning Objectives
Keywords: cervical cancer / diagnosis / psychological impact /
 To understand how to diagnose, stage and treat cervical cancer
staging / treatment
in pregnancy.

Please cite this paper as: Howe T, Lankester K, Kelly T, Watkins R, Kaushik S. Cervical cancer in pregnancy: diagnosis, staging and treatment. The Obstetrician &
Gynaecologist 2022;24:31–9. https://doi.org/10.1111/tog.12783

Introduction Epidemiology
All cancers in pregnancy are rare, and individual clinicians Cancer of the cervix is the commonest gynaecological
will see very few during their careers. Despite advances in malignancy diagnosed in pregnancy, with an incidence rate
cancer management for pregnant women, many important of 0.1–12.0 per 10 000 pregnancies.2 The epidemiology of
questions remain unanswered by evidence-based cervical cancer is anticipated to change with the introduction
information. In most countries, obstetric and oncology of the human papilloma virus (HPV) vaccination for school
registries are not linked, making it a challenge to estimate children in 2008. Consequently, the predicted reduction in
the incidence of all types of cancer in pregnancy. It is for cervical cancer rates is as high as 55% in women aged 25–29
these reasons the International Network on Cancer, Infertility years, with the peak age of cancer diagnosis shifting from 25–
and Pregnancy (INCIP) was launched in 2005. With the 29 years in 2011–2015 to 55–59 years in 2036–2040.2 By
support of world experts, INCIP have generated extrapolating these population models of incidence trends,
comprehensive protocols and effective guidance for rates of cervical cancer within pregnancy will probably
pregnant cancer patients and their healthcare providers.1 also reduce.

ª 2021 Royal College of Obstetricians and Gynaecologists 31


Cervical cancer in pregnancy

The relative risk of cervical cancer is lower during include increased cervical mucus, cervical hyperaemia, gland
pregnancy than in nonpregnant women. This indicates a prominence and eversion of the columnar epithelium.7
delay in diagnosis or detection, a true lower risk, or a healthy Pregnancy itself does not influence cervical lesions, and
mother effect. Solid data on how pregnancy affects the progression of pre-invasive to invasive disease during
outcome of gynaecological cancers is missing, although a few pregnancy is rare (0.0–0.4%).8
reports have shown a poorer prognosis for patients diagnosed If invasive disease is suspected at colposcopy, an adequate
with cervical cancer during pregnancy.3,4 biopsy to make a diagnosis is crucial. It is important to
understand that a punch biopsy diagnosing CIN cannot
reliably exclude invasion.6 The risk of haemorrhage with a
Diagnosis of cervical cancer in pregnancy
diathermy loop is approximately 25%,9 so such biopsies should
Presenting symptoms only be undertaken in clinics or operating theatres where
Early-stage cancer of the cervix may be asymptomatic and appropriate facilities to manage haemorrhage are available.6
detected after an abnormal smear. The symptoms of cervical
cancer in pregnancy do not differ between pregnant and
Staging of cervical cancer in pregnancy
nonpregnant women. Cancer-related symptoms, such as
painless vaginal bleeding, pelvic and lower back pain and Cervical cancer invasion occurs locally, affecting the vagina,
urinary frequency, can resemble other common conditions parametrium and uterosacral ligaments as the first site of
related to pregnancy.5 spread. The bladder, rectum and pelvic and para-aortic lymph
Signs and symptoms of cervical cancer can include nodes may also be involved.10 Lymph node involvement is
anomalous vaginal bleeding and discharge, dyspareunia associated with a worse prognosis.11 The lymph nodes affected
and/or an abnormal appearance of the cervix. Local can include the obturator, external and internal illiacs, presacral
extension to the pelvic organs may cause other symptoms and the para-aortic lymph nodes. Distant metastatic spread to
including haematuria, urinary incontinence, lower limb the bones, lungs and liver may also occur.10
oedema and changes to bladder and bowel habit. More The International Federation of Gynaecology and
distant metastases may present with bone pain, or systemic Obstetrics (FIGO) 2018 staging system for cervical cancer is
symptoms such as loss of appetite, weight loss or fatigue. shown in Box 1.12 It is primarily based on clinical
Ureteric obstruction can cause flank or loin pain, with examination and can be employed for the staging of
subsequent oliguria or anuria as a result of renal failure.5 pregnant women.12

Examination and referral pathway Magnetic resonance imaging


All women presenting with bleeding in pregnancy should be Pelvic magnetic resonance imaging (MRI) is the first line for
examined and the cervix visualised. If a suspected cervical staging of cervical cancer in pregnancy. It is safe in pregnancy,
abnormality is identified, then they should be urgently at any gestation, as there is no ionising radiation. Therefore, if
referred to an experienced colposcopist or gynaecologist distant metastases are suspected, assessment by abdominal MRI
under the ‘two-week’ rule.6 can be considered. Pregnancy may pose challenges when
interpreting MRI. These difficulties can include dilated pelvic
Cervical screening in pregnancy veins being misinterpreted as pelvic adenopathy, or a reduction
Routine recall and test-of-cure (TOC) smear tests in pregnancy in image quality occurring because of fetal movements.13
can be deferred until 3 months after delivery. Pregnancy itself is The use of contrast is not essential in the staging of cervical
not a contraindication to a smear test. For women who require cancer. Gadolinium and iodinated contrast mediums can
follow-up after treatment of cervical glandular intraepithelial cross the placenta and be excreted into the amniotic fluid
neoplasia (CGIN) or cervical intraepithelial neoplasia (CIN) 2 from the fetus. Despite this, there is no evidence of
and 3, with involved or uncertain margins, cytology should not teratogenic or adverse fetal effects.14
be delayed until after pregnancy.6
Computed tomography
Colposcopy and excisional biopsy in pregnancy Computed tomography (CT) scans are usually contraindicated
Colposcopy is safe during pregnancy. The aim of colposcopy, during pregnancy to avoid a dose of radiation to the fetus.
where possible, is to exclude invasive disease and defer biopsy Therefore, CT should be considered as a second choice to
until after the woman has delivered. Colposcopic assessment MRI. However, it may be necessary to fully stage the patient;
during pregnancy requires a high degree of skill and should for example, if there is a high suspicion of lung or pleural
be undertaken by an experienced colposcopist.6 The spread. In such a case, the benefits would outweigh the risks to
physiological effects of pregnancy can make it more the fetus. If a CT scan (or X-ray) is required, then all efforts
challenging to accurately assess the cervix. These effects should be made to limit fetal exposure to radiation and to not

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Howe et al.

Radiographs
Box 1. 2018 FIGO staging of carcinoma of the cervix12
A chest radiograph may be considered to assess for lung
Stage I: metastases. Owing to the minimal risk to the fetus in
The carcinoma is strictly confined to the cervix uteri (extension to the pregnancy, the British Thoracic Society recommends an X-
corpus should be disregarded). ray of the thorax for the same indications as a
 IA Invasive carcinoma that can be diagnosed only by microscopy, nonpregnant woman.17
with maximum depth of invasion <5 mm

○ IA1 Measured stromal invasion <3 mm in depth Laparoscopic lymphadenectomy and sentinel lymph
○ IA2 Measured stromal invasion ≥3 mm and <5 mm in depth node biopsy
 IB invasive carcinoma with measured deepest invasion ≥5 mm Accurate nodal staging is essential to the prognosis and
(greater than stage IA) lesion limited to the cervix uteri
treatment of cervical cancer. For women with stage I disease,
○ IB1 Invasive carcinoma ≥5 mm of stromal invasion and <2 cm in laparoscopic lymphadenectomy may allow for risk
greatest dimension
○ IB2 Invasive carcinoma ≥2 cm and <4 cm in greatest dimension
stratification, with the aim of identifying whether or not a
○ IB3 Invasive carcinoma >4 cm in greatest dimension ‘safe’ pregnancy-saving policy can be undertaken. Positive
Stage II: lymph nodes would denote a need for urgent treatment, with
The carcinoma invades beyond the uterus, but has not extended onto surgery not being the first-line option.18 Negative lymph
the lower one-third of the vagina or to the pelvic wall.
nodes may allow time for fetal maturation. However,
 IIA Involvement limited to the upper two-thirds of the vagina performing a nodal resection after the 22nd week of
without parametrial involvement
gestation is not recommended owing to the insufficient
○ IIA1 Invasive carcinoma <4 cm in greatest dimension number of nodes retrieved, the size of the gravid uterus and
○ IIA2 Invasive carcinoma ≥4 cm in the greatest dimension overall risks of the surgery.1 There is no consensus on what
 IIB With parametrial involvement but not up to the pelvic wall
Stage III: period of delay is deemed safe and it is important to
The carcinoma involves the lower third of the vagina and/or extends to remember the risk of tumour progression is always present.19
the pelvic wall and/or causes hydronephrosis or non-functioning kidney The sentinel lymph node (SLN) is the first regional lymph
and/or involves pelvic and/or paraaortic lymph nodes.
node that directly drains the lymph from the primary
 IIIA Carcinoma involves the lower third of the vagina, with no tumour. The benefits of SLN detection are to gain
extension to the pelvic wall information on prognosis and reduction in unnecessary
 IIIB Extension to the pelvic wall and/or hydronephrosis or non-
functioning kidney (unless known to be due to another cause)
surgery, hence reducing overall morbidity. While the utility
 IIIC Involvement of pelvic and/or paraaortic lymph nodes, of SLN biopsy in early-stage cervix cancer has been proven
irrespective of tumour size and extent and taken up by some oncology centres, there is insufficient
○ IIIC1 Pelvic lymph node metastasis only data for its use in pregnant women with cervical cancer. At
○ IIIC2 Paraaortic lymph node metastasis present, SLN biopsy is not recommended in this population
Stage IV: and more trials are needed to clarify safety issues surrounding
The carcinoma has extended beyond the true pelvis or has involved
(biopsy proven) the mucosa of the bladder or rectum. A bullous
SLN biopsy in pregnancy.20
oedema, as such, does not permit a case to be allotted to stage IV.

 IVA Spread of the growth to adjacent organs Treatment of cervical cancer in pregnancy
 IVB Spread to distant organs
Treatment of stage IA1 without lymphovascular
space invasion
compromise the baby’s health. Radiologists should aim to plan Most stage IA cancers are diagnosed after excisional
scans in advance, monitor and minimise the length of treatment, so diagnosis is unlikely to be made during
scanning time and offer abdominal shielding and low-dose pregnancy. Provided there is no lymphovascular space
radiation where possible.15 invasion (LVSI), a stage IA1 cancer may be treated with a
cone biopsy. The optimum gestation for this treatment is
Ultrasound between 14 and 20 weeks. The depth of invasion and margins
Ultrasound may be used to assess maternal hydronephrosis. can be more accurately assessed from a single specimen with
It is considered safe for both mother and fetus if both minimal heat artefact. Therefore, a knife or laser cone is
the thermal and mechanical index are kept as low as advocated by some for this treatment. If the margins are
possible. However, as clinicians, we must remember that positive, then a second treatment should be considered.21
compression of the gravid uterus on the ureters and the Women should be encouraged and supported to aim for a
relaxation effect of progestogen on smooth muscle may vaginal birth if there are no obstetric contraindications.
result in physiological hydronephrosis being exhibited in The risk of pelvic lymph node metastases in stage IA1
90% of pregnancies.16 squamous cell carcinoma is 1% or less; this risk increases to

ª 2021 Royal College of Obstetricians and Gynaecologists 33


Cervical cancer in pregnancy

3–6% for stage IA2.22 The involvement of a specialist Overall, there is mounting evidence that radical
gynaecological pathology review will increase the detection trachelectomies result in higher rates of obstetric and
of LVSI and tumour volume. This may be beneficial in surgical complications and should not be undertaken
determining the need for pelvic lymph node dissection in during pregnancy. This being said, the 2020 British
early-stage disease. Gynaecological Cancer Society (BGCS) guidance on cervical
cancer in pregnancy discourages performing even simple
Treatment of stage IA1 with LVSI, IA2 and IB1 trachelectomies during pregnancy. Once again, this is a
The gold-standard treatment for stage IB1 and IB2 cervical consequence of the blood loss and poor fetal outcomes
cancer is radical hysterectomy and bilateral salpingectomy, associated with such a procedure.19
with or without bilateral oophorectomy (dependent on
future fertility wishes) with bilateral pelvic Stage IB2: <22 weeks of gestation
lymphadenectomy. Therefore, women must be fully In this scenario, a large loop excision of the transformation
counselled about the possibility of a higher oncogenic risk zone (LLETZ) or a radical trachelectomy may not be an
should they choose a different treatment.23 In early effective treatment option because of the size of the tumour.
pregnancy, women should be made aware of the option to For women who wish to continue with the pregnancy, NACT
terminate the pregnancy and the likely outcomes for the fetus may help to shrink and manage the disease (although only
should premature delivery occur. When deciding a treatment after completion of the first trimester). If she opts for a
pathway, the size of cervical lesion and the gestation of the termination, then a radical hysterectomy and pelvic
pregnancy are important considerations.1 lymphadenectomy can be performed with the fetus in situ.19
As previously discussed, for women who are under 22 weeks
of gestation, a staging lymphadenectomy should be performed. Stage IB2: >22 weeks of gestation
If the pelvic lymph node dissection (PLND) is positive, then a For women over 22 weeks of gestation, consideration
termination of pregnancy should be considered. For women should be given to allow time for fetal maturation; NACT
who wish to continue with the pregnancy, neoadjuvant will help provide this opportunity. Delivery should be by
chemotherapy (NACT) may help treat the disease (although caesarean section at an appropriate gestation. Once the baby
only after completion of the first trimester). If the lymph nodes has been safely delivered, a radical hysterectomy and pelvic
are negative, then a trachelectomy or delay in treatment until lymph node dissection should be undertaken. If the woman
after delivery can be discussed.1 It is important to acknowledge chooses to not undergo chemotherapy while pregnant, an
the risks associated with a trachelectomy requiring appropriate observational approach could be employed until delivery,
patient counselling and multidisciplinary team (MDT) when surgical treatment can be undertaken
discussion.19 After the 22nd week of gestation, treatment may simultaneously.24
include NACT, with the alternative option of delaying
treatment until after delivery.1 Stage IB3 and above
For women with cervical cancer at stage IB3 and above, NACT
Trachelectomy and cervical cerclage can help manage the disease. However, its efficiency has been
A simple trachelectomy is surgery to remove the cervix. This, investigated in only a few trials and further research is
compared with a radical procedure, involves removal of the warranted.25 The role of staging lymphadenectomy is
cervix, parametrium and upper vagina. When a gynaecological controversial26 and follow-up without NACT is not
oncologist is undertaking a vaginal, laparoscopic or robotic recommended because it is likely to compromise the
radical trachelectomy, cervical cerclage is routinely performed prognosis.1 Once fetal maturation is achieved, delivery by
as part of the procedure.19 lower segment caesarean section (LSCS) would be followed by
Women who have undergone an antenatal trachelectomy either surgery or radical chemoradiation (depending on initial
are at high risk (20–30%) of preterm delivery.23 A recent stage and response to chemotherapy treatment). Women with
systematic review recommended serial ultrasound scans to advanced metastatic disease have a poor prognosis. The
monitor for isthmic shortening or funnelling.23 However, it is intention of treatment at this stage becomes palliative with the
important to acknowledge the practical difficulties of aim of controlling the disease rather than cure.
performing such scans and the paucity of evidence in this Figure 1 summarises cervical cancer management
area. Fortnightly urine and genital screening have also been during pregnancy.
recommended from 16 weeks of gestation, with a consideration
for prophylactic antibiotics. Steroid injections for fetal lung Chemotherapy
maturation should be discussed at 24 weeks of gestation, with Chemotherapy is contraindicated in the first trimester of
the theoretical advice of limited activity in the second half of pregnancy. Interference with organogenesis has been
their pregnancy, minimising strain on the cerclage.23 associated with a 10–20% risk of major malformations.

34 ª 2021 Royal College of Obstetricians and Gynaecologists


Howe et al.

Figure 1. Flow chart summarising cervical cancer management during pregnancy.1 AC = adjuvant chemotherapy; DTAD = delayed treatment after
delivery; gw = gestational weeks; MRI = magnetic resonance imaging; NACT = neoadjuvant chemotherapy; NEG = negative; PLND = pelvic lymph
node dissection; POS = positive; ST = simple trachelectomy; TOP = termination of pregnancy.

Treatment after 14 weeks of gestation is considered safe, final dose of chemotherapy and the caesarean section is
with a fetal malformation rate comparable to the general recommended. This allows time for maternal (and fetal) bone
population.27 No significant long-term effects to the fetus marrow recovery.30 Chemotherapy is not recommended beyond
have been noted from the use of chemotherapy after this 35 weeks of gestation to reduce the risk of spontaneous labour
gestation; however, it is important to acknowledge that there occurring when a patient might be neutropenic.27
are no large trials of chemotherapy in pregnancy.28 In this Box 2 summarises recommendations for systemic
situation, correct dating of the pregnancy is essential. treatment and supportive medication.
Platinum agents (cisplatin and carboplatin) and taxanes Possibly, because of the physiological changes that occur
(such as paclitaxel) have efficacy in cervical cancer. The during pregnancy, the bioavailability of chemotherapy agents
carboplatin and paclitaxel regime is favoured over cisplatin may be altered. Despite the increase in maternal cardiac output,
and paclitaxel; it is better tolerated and there is less as well as hepatic and renal perfusion,31 no studies have
nephrotoxicity and ototoxicity.27,29 Carboplatin and demonstrated that standard dosing is too low in pregnancy.
paclitaxel can be given as a weekly or 3-weekly regimen.27 Importantly, no difference in survival has been observed.32
An advantage of the 3-weekly regimen is that it allows for
closer patient monitoring. Where necessary, this enables
Histopathological considerations
chemotherapy and anti-emetic dose adjustment. Close
collaboration between the oncology and obstetric teams is Of all cervical tumours, 85% are squamous cell in origin,
required. The timing of the caesarean section is important, to with the second commonest type being adenocarcinoma.
ensure the patient is not neutropenic. A 3-week gap between the There is an association between adenocarcinoma of the cervix

ª 2021 Royal College of Obstetricians and Gynaecologists 35


Cervical cancer in pregnancy

Box 2. Recommendations for systemic treatment and supportive Radiotherapy, fertility preservation and
medication for patients undergoing cancer treatment in premature menopause
pregnancy1
Detrimental effects of pelvic radiotherapy on the
 Dosing of chemotherapeutic drugs during pregnancy should be uterus
based on actual weight.
 The same dose/m2 or dose/kg2 should be used as in nonpregnant For women who require pelvic radiotherapy following their
patients. caesarean section (cancer at stage IB3 and above), it may be
 Chemotherapy is contraindicated in the first trimester of gestation appropriate to seek advice from a fertility specialist. There is
to avoid interference with organogenesis; fetal benefit of treatment
little evidence that an irradiated uterus can successfully and
delay should be balanced against maternal risk.
 After 14 weeks of gestation, administration of several anticancer safely carry a pregnancy. Uterine radiation-induced damage
drugs is feasible, including taxanes, platinum agents, anthracyclines, may occur by various mechanisms and involving different
etoposide and bleomycin, tissues. These processes include reduced blood flow within
 Chemotherapy is not recommended beyond 35 weeks of gestation;
myometrial and endometrial vessels caused by radiation-
it is important to give a 3-week window between the last cycle of
chemotherapy and delivery to allow both maternal and fetal bone induced fibrosis, as well as damage to muscle fibres and
marrow to recover. reduced pelvic floor muscle function.34
 Until safety data is available, target therapies should be avoided
during pregnancy.
 Metoclopramide, 5HT3 antagonists, ranitidne, proton pump
Detrimental effects of pelvic radiotherapy on the
inhibitors, methylprednisolone, prednisolone, or hydrocortisone ovaries and ovarian transposition
can be used if necessary. Ovarian injury as a consequence of uterine radiation-induced
damage depends not only on a patient’s age but also on the
total radiation dose and site of irradiation. Ovarian
transposition may be performed prior to pelvic radiation
and ovarian metastases, so it is therefore important to with the aim of preserving ovarian function. Transposing the
consider a bilateral salpingo-oophorectomy at the time of ovaries above the pelvic brim and outside the planned
radical hysterectomy. The decision for ovarian conservation radiotherapy field will allow subsequent retrieval of oocytes
must be explored thoroughly with the patient.33 for in vitro fertilisation and minimise the risk of premature
High-risk types of invasive cervical cancers include small menopause. Consideration of a bilateral salpingectomy at the
cell endocrine and clear cell carcinoma of the cervix. A time of surgery is important. The primary benefit of this is to
detailed discussion of rare histological subtypes of cervical reduce the risk of epithelial cancers in the future; however,
cancers and their treatment is beyond the scope of this additional benefits may include improved mobilisation of
article. Despite this, it is important to acknowledge that adnexae, avoidance of tubal damage and formation of
these cancers are more aggressive, metastasise early and hydrosalpinx from radiation therapy and
have a worse prognosis than squamous cell and postoperative adhesions.35
adenocarcinomas. For these reasons, treatment should It is important to counsel these women appropriately,
not be delayed, as this will offer the best chance of survival because the uterus will not support a pregnancy after a radical
to these women. Their care should involve a dedicated course of pelvic radiotherapy. Surrogacy, although only legal
expert gynaecological oncology pathologist with a in certain countries, would be the only option for these
supraregional team being considered to provide their women to have a biologically related child. Even after
overall treatment.19 successful transposition, transient or permanent ovarian
failure might occur. This might be secondary to
devascularisation at surgery, scatter radiation or gonadotoxic
Multidisciplinary team
chemotherapeutic agents. The decision to perform such a
Treatment of women with cervical cancer in pregnancy procedure will depend on the patient’s age, ovarian reserve,
should be undertaken by cancer experts in a cancer centre. desire for future pregnancies, willingness to take hormone
The specialists must be well informed and experienced, replacement therapy (HRT), comorbidities and prognosis.36
ensuring that the physiological changes of pregnancy,
which can make diagnosis and staging more challenging,
Obstetric care
are not detrimental to the patient’s care and final
prognosis.32 The MDT should comprise a gynaecological Timing and mode of delivery
oncology surgeon, medical and radiation oncologist, For patients who have undergone a trachelectomy, delivery
radiologist, histopathologist, neonatologist, psychologist, should be by planned or prelabour caesarean section. This is
specialist cancer nurse, midwife and fetal–maternal to prevent uterine rupture and massive haemorrhage and to
medicine specialist.1 reduce damage to reconstructive procedures.37 Traditionally,

36 ª 2021 Royal College of Obstetricians and Gynaecologists


Howe et al.

a vertical midline upper segment incision was


Psychological and ethical concerns
recommended;38 nowadays, if the lower segment is
sufficiently developed, there is growing evidence on the Psychological impact of a cancer diagnosis in
safety of the transverse incision. The surgery may be pregnancy
technically difficult, with haemorrhage anticipated. For Both pregnancy and cancer are life-changing events. If they
these reasons, an experienced surgeon is recommended to occur simultaneously, emotional and psychosocial stressors
be present.37 are likely to be amplified, so women diagnosed with cancer in
If a pregnancy preservation and NACT treatment plan is pregnancy are extremely vulnerable. While the physical
employed, then the aim should be to continue the pregnancy wellbeing of a woman is of high priority, it is equally as
until fetal maturation has taken place. The appropriate important to address the psychological aspect of her
gestation is considered to be at 34–36 weeks, with the aim of experience. Box 3 summarises recommendations for
minimising the complications of iatrogenic prematurity. psychosocial caregivers treating pregnant cancer patients
However, if earlier delivery was considered to be in the best and their families. Specialist cancer nurses are fundamental in
interests of the mother, this could be supported following a building and maintaining an open dialogue with women; this
discussion with a neonatologist.1 enables patients to process the information given, while
Mode of delivery on the oncological outcome of cervical allowing the specialist to assess their risk of depression.44
cancer is controversial. All options must be discussed with One qualitative study utilised semi-structured interviews to
these women, including obstetric contraindications to vaginal explore psychological experiences of women with a diagnosis
delivery. This being said, risks of vaginal delivery include the of gestational breast cancer. Two major themes identified were
possibility that a tumour may obstruct the birth canal or anxiety and conflict. These related, in particular, to the
cause excessive bleeding at delivery.39 In addition to this, woman’s concerns for the baby’s wellbeing, her own health
studies have shown tumour recurrence occurs more and the delivery of the child. Women who were already
frequently at episiotomy scars than abdominal wall mothers felt conflict between protecting the fetus versus the
incisions. It is for these reasons that caesarean section is need for treatment. Treatment would likely offer them a better
usually deemed a safer mode of delivery for these women. It chance of survival, enabling them to see their other children
is important to note that if the tumour itself is very large, grow up. There was a natural tendency for women to think
consideration to a wound-protective system or corporeal about the fetus rather than themselves.45
uterine incision would be beneficial. In this circumstance, Henry et al.46 investigated the long-term distress associated
performing a classical caesarean section is likely to reduce with a cancer diagnosis in pregnancy. Women remained
blood loss.19 ‘clinically distressed’ nearly 4 years after diagnosis compared
Corticosteroid cover should be given for fetal lung with 15% of women at 1-year post diagnosis who received a
maturation, as per National Institute for Health and Care nonpregnancy related diagnosis.46 The following factors were
Excellence (NICE) guidance,40 with the baby being associated with increased risk for long-term distress: preterm
delivered at an appropriate neonatal unit, dependent on birth, receiving fertility assistance to conceive during this
local neonatal network arrangements. Melanoma, pregnancy, not producing sufficient milk to breastfeed, being
haematopoietic and lung cancers are currently the only
cancers reported to metastasise to the placenta and fetus.
However, in such a scenario, it would be good practice to Box 3. Recommendations for psychosocial caregivers treating
send the placenta for histology to confirm no evidence pregnant cancer patients and their families1

of spread.41  Psychologists should be included in the interdisciplinary team of


caregivers for pregnant cancer patients.
Breastfeeding  Counselling should be offered to both the affected woman and her
Chemotherapeutic agents are known to cross into breast partner.
 Extensive education should be provided about the necessary medical
milk. It may cause neonatal leucopenia, increasing the risk steps and their implications on the outcome of the pregnancy, and
of infection to the baby, so breastfeeding is contraindicated the long-term effects on the physical and cognitive health of the
while undergoing chemotherapy. Advice from a pharmacist offspring.
should be sought prior to the decision to breastfeed, with a  Contact with other families who have experienced cancer during
pregnancy should be encouraged because this might help patients
minimum period of 14 days from the last chemotherapy and their families to cope more easily with their own emotions,
session before breastfeeding is commenced. This will allow thoughts and concerns.
time for clearance of the drug from the breast milk.42 There  In gynaecological cancers, hysterectomy and bilateral oophorectomy
can be performed. Thus, the interdisciplinary team should be aware
is evidence to suggest a period of lactation following a
of the possible psychological effects of this surgery, including
stressful pregnancy can be of psychological benefit to depression, loss of sexual pleasure and future child-bearing ability.
the woman.43

ª 2021 Royal College of Obstetricians and Gynaecologists 37


Cervical cancer in pregnancy

advised to terminate the pregnancy, having a caesarean 10 Eifel PJ, Berek JS, Thigpen JT. Cancer of cervix, vagina and vulva. In: DeVita
VT Jr, Hellman S, Rosenberg SA, editors. Cancer: principles and practice of
section for delivery and undergoing cancer surgery post oncology. Philadelphia, PA: Lippincott; 1997. p. 1433–75.
pregnancy. The research suggested that women affected by 11 Narayan K, McKenizie AF, Hicks RJ, Fisher R, Bernshaw D, Bau S. Relation
these risk factors should be referred for additional between FIGO stage, primary tumor volume, and presence of lymph node
metastases in cervical cancer patients referred for radiotherapy. Int J Gynecol
psychosocial support.46 Cancer 2003;13:657–63.
12 Singh N, Rous B, Ganesan R. 2018 FIGO staging system for cervical cancer:
Summary and comparison with 2009 FIGO staging system. Int J Gynecol
Conclusion Obstet 2019;145:129–35.
13 Balleyguier C, Fournet C, Ben Hassen W, Zareski E, Morice P, Haie-Meder C,
A diagnosis of cancer in pregnancy has a considerable effect et al. Management of cervical cancer detected during pregnancy: role of
on women, requiring both physical and psychological magnetic resonance imaging. Clin Imaging 2013;37:70–6.
14 Webb J, Thomsen H, Morcos S. The use of iodinated and gadolinium
support. Over the last 2 years, both the BGCS and the
contrast media during pregnancy and lactation. Eur Radiol
European Society of Medicine1 have published guidelines 2005;15:1234–40.
encompassing cervical cancer in pregnancy.1,19 With bodies 15 Morice P, Uzan C, Gouy S, Verschraegen C, Haie-Meder C. Gynaecological
cancers in pregnancy. Lancet 2012;379:558–69.
like INCIP working to advance cancer care for pregnant
16 International Commission on Radiological Protection (ICRP). The
women, the hope is that over time, our knowledge will 2007 recommendations of the International Commission on
continue to increase, enabling us to offer more effective and Radiological Protection. Annals of the ICRP. ICRP Publication 103.
Elsevier; 2007.
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17 Morice AH, McGarvey L, Pavord I. British Thoracic Society Cough Guideline
Group. Recommendations for the management of cough in adults. Thorax
Disclosure of interests 2006;61 Suppl 1:11–24.
18 Alouni S, Rida K, Mathevet P. Cervical cancer complicating pregnancy:
There are no conflicts of interest.
implications of laparoscopic lymphadenectomy. Gynecol Oncol
2008;108:472–7.
Contribution to authorship 19 British Gynaecological Cancer Society (BGCS). Cervical cancer guidelines:
recommendations for practice. London: BGCS; 2020 [https://www.bgcs.
SK instigated and edited the article. TH researched, wrote
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and edited the article. KL wrote and edited the article. TK pdf].
wrote and edited the article. RW wrote and edited the article. 20 Filippakis G, Zografos G. Contraindications of sentinel lymph node biopsy:
Are there any really? World J Surg Oncol 2007;5:10.
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21 Ellis P, Mould T. Fertility saving treatment in gynaecological oncology.
the manuscript. Obstet Gynaecol 2011;11:239–44.
22 Smith HO, Qualls CR, Romero AA, Webb JC, Dorin MH, Padilla LA, et al. Is
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ª 2021 Royal College of Obstetricians and Gynaecologists 39


DOI: 10.1111/tog.12780 2022;24:24–30
The Obstetrician & Gynaecologist
Review
http://onlinetog.org

Investigation and management of postcoital bleeding


Gemma L Owens BSc (Hons) MBBCh MRes PhD MRCOG,a,b* Nick J Wood MBBS MD MRCOG,
c

Pierre Martin-Hirsch MBChB MD, FRCOGc


a
ST6 in Obstetrics and Gynaecology, Department of Obstetrics and Gynaecology, Lancashire Teaching Hospitals NHS Foundation Trust,
Royal Preston Hospital, Sharoe Green Lane, Fulwood, Preston PR2 9HT, UK
b
NIHR Clinical Lecturer in Gynaecological Oncology, Division of Cancer Sciences, Faculty of Medicine, Biology and Health, University of
Manchester, Oxford Road, Manchester M13 9PL, UK
c
Consultant Gynaecological Oncologist, Department of Obstetrics and Gynaecology, Lancashire Teaching Hospitals NHS Foundation Trust,
Royal Preston Hospital, Sharoe Green Lane, Fulwood, Preston PR2 9HT, UK
*Correspondence: Gemma L Owens. Email: gemma.owens@manchester.ac.uk

Accepted on 7 December 2020. Published online 20 January 2022.

Key Content Learning Objectives


 Postcoital bleeding is a common gynaecological symptom affecting  To review causes of postcoital bleeding.
up to 9% of women.  To appreciate the importance of diagnostic tests in the assessment
 Postcoital bleeding is commoner in women with invasive cervical of postcoital bleeding.
cancer than the general population; however, most women with  To understand the management options for women with an
postcoital bleeding will not have an underlying malignancy. identifiable cause of their postcoital bleeding and the management
 Knowledge of how to investigate and manage postcoital bleeding is of recurrent or persistent postcoital bleeding in the absence
imperative to provide optimal care and ensure patient safety. of pathology.
 It is essential that all gynaecologists are aware of referral pathways
Keywords: cancer / cervical pathology / postcoital bleeding
for suspected cervical malignancy.

Please cite this paper as: Owens GL, Wood NJ, Martin-Hirsch P. Investigation and management of postcoital bleeding. The Obstetrician & Gynaecologist
2022;24:24–30. https://doi.org/10.1111/tog.12780

presenting with postcoital bleeding, in the absence of a


Introduction
national guideline.
Postcoital bleeding is defined as nonmenstrual bleeding or
spotting occurring immediately after sexual intercourse.
Assessment of women with postcoital
Estimates of the prevalence of postcoital bleeding in the
bleeding
community range from 0.7 to 9.0%, with an annual
cumulative incidence of 6% in premenopausal women.1 Postcoital bleeding typically arises from contact with lesions
Although postcoital bleeding is considered a cardinal on the cervix, vagina or vulva, whereas endometrial
symptom of cervical cancer, its positive predictive value is pathology usually leads to intermenstrual or heavy
low. Of those who present to primary care with postcoital menstrual bleeding. Often, postcoital bleeding and
bleeding, only 1 in 44 000 women aged 20–24 and 1 in 2400 intermenstrual bleeding coexist. Causes of postcoital
women aged 45–54 will have cervical cancer.2 Nevertheless, bleeding are outlined in Box 1. Most women with
the principal aim of investigating women with postcoital postcoital bleeding will have a benign condition, such as a
bleeding is to exclude cervical cancer. cervical polyp, ectropion, urogenital atrophy or cervicitis
A coroner’s inquest into the death of a 49-year-old woman secondary to chlamydial infection. However, postcoital
diagnosed with cervical cancer in 2017 identified key failings bleeding can also be associated with cervical cancer and,
in the management of her case. These included failure to understandably, causes anxiety in women presenting with
report the smear test accurately and failure on two further this symptom. It is therefore essential that women are
occasions to recognise a clinically obvious cervical cancer. carefully assessed to exclude serious pathology.
Sadly, this case highlights inconsistencies in the investigation There are clear guidelines on which women warrant an
and management of postcoital bleeding within the UK. The urgent referral to secondary care (Table 1).3,4 Colposcopy
purpose of this review is to outline common causes of referral for every case of postcoital bleeding is unfeasible,
postcoital bleeding and to provide a framework for history expensive and – most of all – distressing for the women
taking, examination and initial investigation of women concerned.5 The cervical screening programme guidelines

24 ª 2021 Royal College of Obstetricians and Gynaecologists


Owens et al.

History
Box 1. Causes of postcoital bleeding
A thorough clinical history and examination can help to elicit
Benign conditions risk factors and signs suggestive of underlying pathology. The
 Urogenital atrophy history should enquire about:
 Benign vascular tumours of the genital tract, e.g. haemangiomas, A-
V malformation  The patient’s age
 Cervical or endometrial polyps  The duration, frequency and amount of bleeding
 Cervical ectropion
 Menstrual history, including normal bleeding pattern and
 Cervical endometriosis
last menstrual period
Infection  The presence of other gynaecological symptoms, such as
 Vulvovaginitis secondary to candidiasis or trichomonas
 Cervicitis secondary to chlamydia or gonorrhoea vaginal discharge, pelvic pain and dyspareunia
 Endometritis in presence of intrauterine coil device (IUCD)  Contraceptive history and use of other hormonal therapy
Vulval
(for example, hormone replacement therapy, tamoxifen)
 Vulval dermatoses, e.g. lichen sclerosus  History of human papilloma virus (HPV) immunisation
 Genital warts  Cervical screening history, including date and result of last
 Genital ulcers, e.g. herpes, chancroid screening test
 Syphilis
 Lymphogranuloma venereum
 Details of any previous colposcopy and treatment
 Sexual history, including any previous history of sexually
Malignancy
transmitted infections (where appropriate)
 Vulval cancer
 Vaginal cancer  Relevant past medical and surgical history, including
 Cervical cancer bleeding disorders
 Endometrial cancer  Current medications, particularly use of anticoagulants
Other  Other relevant risk factors, such as smoking status.
 Trauma and genital piercings
 Bleeding disorders A sexual risk assessment is particularly pertinent in women
 Foreign bodies aged 25 years or younger, in whom there is a higher prevalence
 Sexual abuse of chlamydia. Further guidance on this is available via the
 Pregnancy-related
 Female genital mutilation (FGM)
British Association for Sexual Health and HIV (BASHH).6 All
patients should be screened for domestic and/or sexual abuse
because trauma to the genital tract can result in postcoital
bleeding. Fear or embarrassment may mean that women do not
Table 1. Indications for referral to secondary care
volunteer this information, so the question needs to be asked.
The ‘HARK’ questions are a simple way to sensitively enquire
Urgency of about intimate partner violence (Table 2).7 Specific guidance
Situation referral
on identifying and responding to disclosures of domestic abuse
has been developed by the Department of Health and
Women presenting with symptoms of cervical Within 2 weeks Social Care.8,9
cancer (e.g. unexplained postcoital bleeding or
persistent vaginal discharge) Examination
Women presenting with postcoital bleeding should have an
Abnormal appearance to cervix or vaginal on Within 2 weeks
speculum examination abdominal examination and careful inspection of the vulval
skin before proceeding to a speculum examination. Vulval
inspection may identify vulval dermatoses, excoriation,
ulceration, fissuring, female genital mutilation or genital
piercings. A Cusco speculum should be used to inspect the
recommend that women presenting with postcoital bleeding vaginal walls for atrophic changes, lacerations, prolapse or
should first be examined by a gynaecologist who is ulcerated lesions. Note any vaginal discharge or the presence
experienced in the management of cervical disease, and of a foreign body. Visual inspection of the cervix may identify
then referred on to colposcopy if cancer is suspected.3 a cervical ectopy or a polyp. Most invasive cancers causing
Women with a clinically suspicious cervical lesion should postcoital bleeding are clinically apparent on speculum
ideally be referred directly to colposcopy, although this may examination.10 Findings suggestive of cervical cancer
vary depending on local service demands. A diagnostic include ulceration, friable tissue, contact bleeding or a
pathway for women presenting with postcoital bleeding is craggy irregular mass. The examination should be
outlined in Figure 1. concluded with a bimanual examination to palpate the

ª 2021 Royal College of Obstetricians and Gynaecologists 25


Investigation and management of postcoital bleeding

Postcoital bleeding

History and physical examination

Microbiology swabs Cervical screening test Clinically Normal cervix but


if overdue abnormal cervix persistant PCB or
coexisting IMB

If positive, treat
infection and refer Abnormal result
onto GUM for Consider
contact tracing transvaginal USS
+/- pipelle biopsy
Colposcopy +/- hysteroscopy

Figure 1. A diagnostic pathway for investigation of postcoital bleeding. Abbreviations: GUM = genitourinary medicine; IMB = intermenstrual
bleeding; PCB = postcoital bleeding; USS = ultrasound scan.

infection. If gonorrhoea is suspected, an endocervical swab for


Table 2. ‘HARK’ questions to screen for intimate partner violence
antimicrobial sensitivity testing should be taken in addition to the
vulvovaginal swab. These tests do not need to be repeated if they
‘HARK’ In the last year. . . have already been completed in primary care.
A cervical screening test can be taken if the patient is aged
25 years or older and has not been screened within the normal
Humiliation Have you been humiliated or emotionally abused in
other ways by your partner or ex-partner?
screening interval. This is a screening rather than a diagnostic
test: it is not appropriate in patients with a suspicious cervix on
Afraid Have you been afraid of your partner or ex-partner? examination; these women require urgent colposcopic
assessment. Rarely, endometrial pathology can present with
Rape Have you been raped or forced to have any kind of
sexual activity by your partner or ex-partner? postcoital bleeding. If the cervix is clinically normal, consider a
transvaginal ultrasound, pipelle endometrial biopsy and/or an
Kick Have you been kicked, hit, slapped or otherwise outpatient hysteroscopy to exclude endometrial pathology,
physically hurt by your partner or ex-partner?
especially in women with coexisting intermenstrual bleeding.
One advantage of a diagnostic hysteroscopy is the ability to
visualise the endocervical canal; however, this procedure is
usually reserved for women with an irregular or thickened
cervix, assess uterine size and adnexal lesions and evaluate for endometrium on scan, or with persistent symptoms in the
cervical excitation – a clinical feature of pelvic absence of other pathology.11
inflammatory disease.
When is referral to colposcopy indicated?
Initial investigations
It is important to exclude pregnancy in any woman of reproductive The national cervical screening programme has now
age presenting with abnormal bleeding. Cervicitis secondary to introduced HPV primary testing in England, Scotland and
chlamydial infection is a common cause of postcoital bleeding in Wales. If high-risk HPV is detected, cytology will then be
young women,1 thus a vulvovaginal swab should be taken for performed to check for abnormal cells. Women require
nucleic acid amplification tests (NAATs) in those at risk of onward referral to colposcopy if they are found to have

26 ª 2021 Royal College of Obstetricians and Gynaecologists


Owens et al.

abnormal cytology, including borderline changes, low-grade cervical biopsy should be performed and treatment delayed
dyskaryosis, high-grade dyskaryosis, possible invasive cancer until the histology is known.
or glandular changes. Women also require colposcopy if they
have two sequential inadequate tests, or the cervix cannot be Cervical polyps
identified on speculum examination.3 In the context of Cervical polyps are usually asymptomatic and found
postcoital bleeding, women require a colposcopic assessment incidentally on speculum examination but can also
within 2 weeks if the appearance of the cervix is suspicious present with bleeding after intercourse. On examination,
on examination. The NHS cervical screening programme they appear as pedunculated fleshly lobular structures and
advocates women with persistent postcoital bleeding or can arise from the endocervical canal, ectocervix, or from
vaginal discharge in the absence of other pathology to be an endometrial polyp prolapsing through the cervical
“referred for examination by a gynaecologist experienced in canal. They are friable and easily bleed on contact.
the management of cervical disease (for example, a cancer Polyps are thought to arise from chronic inflammation
lead gynaecologist)”. Gynaecologists may refer these women or after an atypical response to hormonal stimulation.
on for symptomatic colposcopic examination outside the They most frequently present in perimenopausal and
cervical screening programme if cancer is suspected.3 postmenopausal women.14
Symptomatic polyps and cases with coexisting abnormal
cervical cytology should be removed and sent for histological
Causes and management of postcoital
examination to exclude malignancy.15 Most cervical polyps
bleeding
measure less than a few centimetres in diameter and can be
Cervical ectropion avulsed during speculum examination. The polyp should be
A cervical ectropion is a normal physiological finding. grasped at its base using polyp forceps and twisted off.
Cervical eversion results in the friable, mucus-secreting Haemostasis can usually be achieved with silver nitrate.
glandular epithelium of the endocervix being exposed on Larger or broad-based polyps may require removal with loop
the ectocervix. It classically appears as a red disc around the diathermy at colposcopy.
external cervical os. It is often seen after menarche, during Symptomatic cervical polyps can be associated with
pregnancy and in women taking the combined oral endometrial polyps and hyperplasia, particularly in
contraceptive pill, arising as a result of cervical remodelling perimenopausal and postmenopausal women. Endometrial
in response to estrogen. Exposure to the vaginal milieu abnormalities have been reported in up to 55% of
eventually transforms the glandular epithelium into postmenopausal women with cervical polyps, advocating
squamous epithelium in a process called squamous that these women should be offered hysteroscopy and
metaplasia. The exposed columnar epithelium is susceptible endometrial sampling, in addition to avulsion of the
to trauma and contact bleeding during intercourse or polyp.16 The risk of dysplasia or malignancy in cervical
examination. Women with cervical ectopy may present polyps is estimated to be 0.0–1.7%,15 thus conservative
with increased mucopurulent vaginal discharge and management may be appropriate in asymptomatic women.
postcoital bleeding, or may be asymptomatic.12 On
speculum examination, a cervical ectropion may cause Cervicitis, endometritis and pelvic inflammatory
contact bleeding, making it difficult to exclude significant disease
disease without colposcopy referral. As mentioned above, postcoital bleeding in younger women
Women should be informed regarding the physiological is more likely to arise from cervicitis secondary to a sexually
nature of the condition. Given this reassurance, the patient transmitted infection (STI). Chlamydia is the commonest
may decide not to have any further treatment. If applicable, bacterial STI and is estimated to affect up to 7% of women
changing the combined oral contraceptive to the under the age of 25 years.17 Risk factors for infection include
progestogen-only pill may resolve symptoms. Women with age under 25 years, a new sexual partner, more than one
persistent or troublesome symptoms can be offered sexual partner in the preceding year and inconsistent use of
cryocautery or diathermy to the cervix. However, the risk barrier contraception. Chlamydia can be detected using
of recurrence should be highlighted, especially in the context NAATs, either from a vulvovaginal swab or urine. First-line
of exogenous hormones. In addition, women should be treatment for women with suspected or confirmed
informed of potential side effects to treatment, including chlamydial infection is azithromycin 1 g orally as a single
copious vaginal discharge until healing is complete and dose, followed by 500 mg once daily for 2 days, or
cervical stenosis.13 If the woman has had regular and negative doxycycline 100 mg twice a day for 7 days.18 Single-dose
cervical screening and the doctor is satisfied with the treatments are associated with better compliance. Women
diagnosis of an ectropion, then cryocautery should be should be advised to abstain from intercourse until treatment
performed in the gynaecology clinic. If in any doubt, a is complete and should be referred on to a local sexual health

ª 2021 Royal College of Obstetricians and Gynaecologists 27


Investigation and management of postcoital bleeding

service for screening for other STIs and partner notification. High-risk subtypes of the human papillomavirus (hrHPV)
Test of cure is not usually required unless there are account for nearly all cervical cancers. HPV-16 and HPV-18
compliance issues, or the patient is pregnant. Less are the commonest pathogenic subtypes, accounting for over
frequently, gonorrhoea may cause postcoital bleeding. Like 70% of cervical cancers. It is estimated that 70% of women
chlamydia, it is best detected using NAATs on a vulvovaginal will contract HPV in their lifetime. Most will clear the
swab. First-line treatment of uncomplicated gonorrhoea is infection; however, persistence of HPV DNA can lead to the
ceftriaxone 1 g intramuscularly as a single dose. Test of cure development of dysplasia and invasive cancer. The causal
is advised for all confirmed cases of gonorrhoea because of association between hrHPV and cervical cancer led to the
the increasing prevalence of antibiotic-resistant strains.18 All introduction of the HPV vaccination programme in 2008,
women who test positive for gonorrhoea should also be with the aim to prevent the acquisition of HPV infection. The
referred on to local sexual health services for further testing current immunisation programme comprises two doses of
and partner notification. Gardasil, the quadrivalent HPV vaccine, which protects
If endometritis or pelvic inflammatory disease (PID) is against HPV-6, HPV-11, HPV-16 and HPV-18.23 The
suspected, broad-spectrum antibiotic therapy should be programme initially targeted 12 and 13-year-old girls but
commenced without delay. Microbiology swabs should has since been extended to include boys of the same age.
ideally be obtained before commencing antibiotic therapy. Indications for colposcopy were discussed earlier in this
Long-term complications of untreated PID include chronic review. Women with low-grade lesions (CIN1) can be offered
pelvic pain, adhesions, ectopic pregnancy and subfertility. surveillance with further screening in 12 months. On the
Antibiotic regimens recommended by BASHH18 aim to other hand, women with lesions consistent with high-grade
ensure treatment of all potential causative microbes, disease (CIN2/3) should be offered excisional treatment at
including gonorrhoea, chlamydia and anaerobes. If the the first visit (‘see and treat’). Excisional treatment is
patient is clinically unwell, they will require inpatient associated with a two-fold relative increase in the risk of
admission and initial treatment with intravenous preterm birth, but the absolute risk remains low.24 Women
antibiotics. The latest recommended inpatient and with invasive disease should be referred to a tertiary cancer
outpatient antibiotic regimens are listed in Table 3.18 centre for further assessment and management.

Cervical cancer Vulval and vaginal lesions


The prevalence of cervical intraepithelial neoplasia (CIN) and Urogenital atrophy results from estrogen deficiency and
cancer among women with postcoital bleeding is estimated to is commonest in postmenopausal women. It typically
be 3–18%.11 A retrospective study of 314 women with presents with vulvovaginal dryness and irritation, decreased
postcoital bleeding identified 12 cases of invasive cancer lubrication, superficial dyspareunia and, occasionally,
(3.8%) and 54 cases of CIN (17.2%). In this cohort, there postcoital bleeding secondary to trauma during intercourse.
were ten cervical or vaginal cancers, of which eight were Examination findings consistent with vaginal atrophy include
clinically apparent on speculum examination and four had pale and dry vaginal mucosa with contact bleeding on the
a normal smear before onward referral for further vaginal walls or cervix. Treatment includes the use of vaginal
investigation.19 A further retrospective study of 142 women moisturisers, lubricants, topical estrogens, dehydroepiandrosterone
with postcoital bleeding reported no cases of invasive cancer, (DHEA), ospemifene and laser.
but 27 cases of CIN (19.6%), of which 15 were high-grade Vulval dermatoses such as lichen planus, lichen sclerosus
disease (CIN2/3).20 and contact dermatitis may cause postcoital bleeding
The incidence of cervical cancer has fallen significantly associated with fissuring of the skin. Patients with these
since the introduction of the NHS cervical screening conditions should be advised to avoid soap and potential
programme in 1988;21 however, approximately 3200 new irritants. Regular use of emollients and topical steroids
cases of cervical cancer are still diagnosed each year in the reduces inflammation and improves skin integrity. Vulval
UK.22 Currently, all women aged 25–64 years are routinely biopsies should be considered if there are pigmented lesions,
invited for cervical screening. Women are recalled every ulcerated or eroded areas, or if the patient fails to respond to
3 years until the age of 50, when the screening interval treatment following initial diagnosis. Lichen sclerosus is
increases to every 5 years. Screening invitations cease after associated with a 4.0–6.7% risk of developing squamous cell
the age of 65, unless the woman has previously had a cervical carcinoma of the vulva and requires annual review.25 Vulval
abnormality or positive HPV test. These women should intraepithelial neoplasia (VIN) and vulval cancer typically
continue to be recalled until they have completed follow-up. present with vulval irritation or a palpable lesion, but may
HIV-positive women are at higher risk of developing cervical also cause unscheduled bleeding. These lesions may present
dysplasia or invasive cancer owing to immunosuppression, so as thickened white or pigmented mucosal plaques, warty
therefore require annual screening.3 lesions, or as persistent ulcers, and may be unifocal or diffuse.

28 ª 2021 Royal College of Obstetricians and Gynaecologists


Owens et al.

Table 3. Recommended antibiotic regimens for the treatment of


No underlying cause
pelvic inflammatory disease Approximately, 50% of women presenting to primary
care with postcoital bleeding will have no obvious
Setting First-line antibiotic regimens underlying cause.19 These women can be reassured that 60%
of women experience a spontaneous resolution of symptoms
Outpatient Intramuscular ceftriaxone 1 g as a single dose + oral
within 6 months.27
doxycycline 100 mg twice daily for 14 days + oral
metronidazole 400 mg twice daily for 14 days
Summary
OR
Oral ofloxacin* 400 mg twice daily for 14 days + oral Postcoital bleeding is a common gynaecological symptom
metronidazole 400 mg twice daily for 14 days and is rarely associated with malignancy. There is
inconsistency in the management of postcoital bleeding
OR
among gynaecologists.28 Patients presenting with postcoital
Oral moxifloxacin* 400 mg once daily for 14 days
bleeding require a thorough history and examination to
Inpatient Intravenous ceftriaxone 2 g daily + intravenous or oral formulate a differential diagnosis and guide further
doxycycline 100 mg twice daily until 24 hours after investigations. A cervical screening test should only be
clinical improvement
performed if one is due as part of the NHS cervical
Followed by oral doxycycline 100 mg twice daily for
14 days + oral metronidazole 400 mg twice daily for screening programme. Women with a previously negative
14 days screening test have a greatly reduced risk of cervical cancer.
However, a previous negative result does not exclude the
OR
Intravenous clindamycin 900 mg three times a day +
possibility of malignancy and should not delay referral to
intravenous gentamicin 2 mg/kg loading dose followed colposcopy if there is a clinical suspicion of cervical cancer.
by 1.5 mg/kg three times a day until 24 hours after
clinical improvement Disclosure of interests
Followed by oral clindamycin 450 mg four times a day or
oral doxycycline 100 mg twice daily for 14 days + oral
PMH is the current President of the British Society for
metronidazole 400 mg twice daily for 14 days Colposcopy and Cervical Pathology. NJW is current Secretary
for the British Gynaecological Cancer Society. GLO has no
*Ofloxacin and moxifloxacin should be avoided if high risk of conflicts of interest.
gonococcal pelvic inflammatory disease

Contribution to authorship
GLO and PMH made substantial contributions to the
concept and design of the article. All authors drafted and
Lesions should be biopsied rather than excised and should
edited the article and approved the final version.
include the area of epithelium where there is transition of
normal to abnormal tissue. If vulval cancer is strongly
suspected on examination, urgent referral to a tertiary cancer
Supporting Information
centre should not be delayed while awaiting the biopsy result.
Rarely, postcoital bleeding may be the presenting symptom Additional supporting information may be found in the
for other cancers of the female genital tract. Vaginal online version of this article at http://wileyonlinelibrary.
intraepithelial neoplasia (VAIN) and vaginal cancer are com/journal/tog
usually asymptomatic, but many women report spotting
Infographic S1. Postcoital bleeding
following intercourse and unusual vaginal discharge. VAIN
appears as white or red mucosal plaques, whereas vaginal
cancer presents as a persistent ulcerated lesion, usually on the References
posterior aspect of the upper third of the vagina. Women
1 Phadnis S, Walker P. Modern management of postcoital and intermenstrual
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Finally, postcoital bleeding may occur following trauma to and risk of cervical cancer. Br J Gen Pract 2006;56:453–60.
3 Public Health England. Cervical screening: programme and colposcopy
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40 years sustained some kind of vaginal trauma during management].
4 National Insitute for Health and Care Excellence (NICE). Suspected cancer:
consensual intercourse. In cases of traumatic bleeding, recognition and referral. NICE guideline NG12. London: NICE; 2017 [https://
surgical repair is the standard of care. www.nice.org.uk/guidance/ng12].

ª 2021 Royal College of Obstetricians and Gynaecologists 29


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5 Fraser IS, Petrucco OM. Management of intermenstrual and postcoital 17 Macleod J, Salisbury C, Low N, McCarthy A, Sterne JAC, Holloway A,
bleeding, and an appreciation of the issues arising out of the recent case of et al. Coverage and uptake of systematic postal screening for genital
O’Shea versus Sullivan and Macquarie pathology. Aust N Z J Obstet Chlamydia trachomatis and prevalence of infection in the United
Gynaecol 1996;36:67–73. Kingdom general population: cross sectional study. BMJ
6 British Association for Sexual Health and HIV (BASSH). Sexual history taking 2005;330:940.
and STI testing guidelines. Macclesfield: BASSH [https://www. 18 British Association for Sexual Health and HIV (BASHH). BASSH guidelines.
bashhguidelines.org/current-guidelines/sexual-history-taking-sti-testing- Macclesfield: BASSH; 2018 [https://bashh.org/guidelines].
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7 Sohal H, Eldridge S, Feder G. The sensitivity and specificity of four questions significant pathology in women attending a general gynaecological service
(HARK) to identify intimate partner violence: a diagnostic accuracy study in for postcoital bleeding. BJOG 2001;108:103–6.
general practice. BMC Fam Pract 2007;8:49. 20 Abu J, Davies Q, Ireland D. Should women with postcoital bleeding be
8 Department of Health. Health visiting and school nursing programmes: referred for colposcopy? J Obstet Gynaecol 2006;26:45–7.
supporting implementation of the new service model. No.5: Domestic 21 Albrow R, Kitchener H, Gupta N, Desai M. Cervical screening in
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Domestic_Violence_A3_Posters_WEB.pdf]. England: 2017. London: ONS; 2019 [https://www.ons.gov.uk/
9 Department of Health. Responding to domestic abuse. A resource for health peoplepopulationandcommunity/healthandsocialcare/
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publishing.service.gov.uk/government/uploads/system/uploads/attachment_ 2017].
data/file/597435/DometicAbuseGuidance.pdf]. 23 Public Health England (PHE). HPV vaccination. Information for healthcare
10 Godfrey MAL, Nikolopoulos M, Povolotskaya N, Chenoy R, Wuntakal R. professionals. London: Public Health England; 2019 [https://assets.
Postcoital bleeding: what is the incidence of significant gynaecological publishing.service.gov.uk/government/uploads/system/uploads/
pathology in women referred for colposcopy? Sex Reprod Healthc attachment_data/file/813014/PHE_HPV_universal_programme_guidance.
2019;22:100462. pdf].
11 Tarney CM, Han J. Postcoital bleeding: a review on etiology, diagnosis, and 24 Kyrgiou M, Athanasiou A, Kalliala IEJ, Paraskevaidi M, Mitra A, Martin-Hirsch
management. Obstet Gynecol Int 2014;2014:192087. PIP, et al. Obstetric outcomes after conservative treatment for cervical
12 Goldacre MJ, Loudon N, Watt B, Grant G, Loudon JD, McPherson K, et al. intraepithelial lesions and early invasive disease. Cochrane Database Syst Rev
Epidemiology and clinical significance of cervical erosion in women 2017;(11):CD012847.
attending a family planning clinic. Br Med J 1978;1:748–50. 25 Krapf JM, Mitchell L, Holton MA, Goldstein AT. Vulvar lichen sclerosus:
13 Kong GW, Yim SF, Cheung TH, Chung TKH. Cryotherapy as the treatment current perspectives. Int J Womens Health 2020;12:11–20.
modality of postcoital bleeding: a randomised clinical trial of efficacy and 26 Astrup BS, Ravn P, Lauritsen J, Thomsen JL. Nature, frequency and duration
safety. Aust N Z J Obstet Gynaecol 2009;49:517–24. of genital lesions after consensual sexual intercourse–implications for legal
14 Tanos V, Berry KE, Seikkula J, Raad EA, Stavroulis A, Sleiman Z, et al. The proceedings. Forensic Sci Int 2012;219:50–6.
management of polyps in female reproductive organs. Int J Surg 27 Shapley M, Jordan K, Croft PR. An epidemiological survey of
2017;43:7–16. symptoms of menstrual loss in the community. Br J Gen Pract
15 MacKenzie IZ, Naish C, Rees CM, Manek S. Why remove all cervical polyps 2004;54:359–63.
and examine them histologically? BJOG 2009;116:1127–9. 28 Alfhaily F, Ewies AA. Postcoital bleeding: a study of the current practice
16 Stamatellos I, Stamatopoulos P, Bontis J. The role of hysteroscopy in the amongst consultants in the United Kingdom. Eur J Obstet Gynecol Reprod
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2007;276:299–303.

30 ª 2021 Royal College of Obstetricians and Gynaecologists


DOI: 10.1111/tog.12778 2022;24:12–23
The Obstetrician & Gynaecologist
Review
http://onlinetog.org

Female sexual dysfunction


a b
Victoria Kershaw MRCOG, Swati Jha MD FRCOG *
a
Subspecialty Trainee in Urogynaecology, Sheffield Teaching Hospitals NHS Foundation Trust, Level 4, Jessop Wing, Tree Root Walk, Sheffield S10
2SF, UK
b
Consultant Gynaecologist, Subspecialist in Urogynaecology, Sheffield Teaching Hospitals NHS Foundation Trust, Level 4, Jessop Wing, Tree Root
Walk, Sheffield S10 2SF, UK
*Correspondence. Swati Jha. Email: swati.jha1@nhs.net

Accepted on 31 July 2020. Published online 11 November 2021.

Key content  To appreciate the reasons why all women attending a gynaecology
 Female sexual dysfunction (FSD) is defined as any sexual clinic should have their sexual function assessed to establish
complaint or problem resulting from disorders of desire, arousal, a baseline.
orgasm or sexual pain that causes marked distress or  To establish realistic expectations of outcomes on sexual function
interpersonal difficulty. following treatment of gynaecological problems.
 Various gynaecological problems such as pelvic organ prolapse and
Ethical issues
endometriosis affect sexual function and this impacts on
 Failure to inform women of the risk of deterioration in sexual
their treatment.
function following gynaecological surgery can lead to litigation.
 Management often requires the need to address different
 Some essential treatments, such as vulvectomy or prophylactic
components of the sexual dysfunction.
 Women wish to keep their options relating to sexual function open
oophorectomy, will result in adverse effects on sexual function,
and women should make informed choices regarding
well past the menopause, and more women are presenting in later
their treatment.
life with FSD.
Keywords: dyspareunia / female sexual dysfunction / genitopelvic
Learning objectives

pain disorders / hypoactive sexual desire disorders / orgasmic
To know how to assess FSD in clinical practice.
disorders

Please cite this paper as: Kershaw V, Jha S. Female sexual dysfunction. The Obstetrician & Gynaecologist 2022;24:12–23.https://doi.org/10.1111/tog.12778

called genitopelvic pain/penetration disorder. Changes to


Introduction
the terminology are shown in Table 1.
Expressions of sexuality and intimacy are some of the most Several other organisations, including the World Health
complex aspects of human behaviour, and sexual function is Organization, International Statistical Classification of
an important component of quality of life.1 Sexual Diseases and Related Health Problems (ICD-10), the
dysfunction is more common in women than men, yet it is International Consultation of Sexual Medicine (ICSM),
less frequently investigated.2 Left untreated, sexual problems the International Urogynecological Association (IUGA) and
are associated with decreased quality of life, depression and the International Continence Society (ICS), have also
interpersonal conflicts.3 attempted to define FSD.6 Although FSD is perhaps best
The Diagnostic and Statistical Manual of Mental Disorders regarded as a spectrum of disorders with considerable
(DSM) defines female sexual dysfunction (FSD) as “any sexual overlap between them,1 there is consensus that the main
complaint or problem resulting from disorders of desire, subcategories of FSD are sexual desire/arousal disorders,
arousal, orgasm, or sexual pain that causes marked distress or orgasmic dysfunction and sexual pain disorder. Sexual
interpersonal difficulty”.4 To qualify as a dysfunction, the disorders may be lifelong, acquired, generalised
problem must be present more than 75% of the time, for more or situational.4
than 6 months, causing significant distress. The National Surveys of Sexual Attitudes and Lifestyles
In the DSM-5, there were several updates to the (NATSAL) are among the largest surveys of sexual behaviour
classification described in the previous version (DSM-4).5 in the world. They have been carried out in the UK every
Female hypoactive desire and female arousal disorder were 10 years since 1990. The third survey (2010–2012) showed
merged and are now called sexual desire/arousal disorder. continuation of sexual activity into later life, emphasising the
Female orgasmic disorder remained unchanged. The need for attention to sexual health irrespective of age.7 The
formerly separate dyspareunia and vaginismus are now fourth survey was commenced in May 2020.

12 ª 2021 Royal College of Obstetricians and Gynaecologists


Kershaw and Jha

dimensions and complex biopsychosocial influences. It is


Table 1. Categories of female sexual dysfunction
now recognised not to be a simple linear progression of
DSM-4 DSM-5 processes, beginning with desire and ending in resolution – a
concept first introduced by Masters and Johnson in
the 1960s.2
Desire disorders Desire/arousal disorders
Hypoactive sexual desire disorder Merged desire and arousal
The circular model described by Basson14 (Figure 1)
Sexual aversion disorder into single category acknowledges the interplay of the sexual responses of both
Deleted sexual aversion the mind and the body. Approximately 30% and 50% of
disorder women may reach orgasm during vaginal penetration and
Arousal disorders direct clitoral stimulation, respectively.15 However, in
Basson’s model, orgasm is not essential for sexual fulfilment.
Orgasm disorder Female orgasm disorder In partnered sexual relationships, feelings of love and
emotional intimacy are important to initiate and maintain
Sexual pain disorders Genito-pelvic pain/
Dyspareunia: pelvic pain with intercourse penetration disorder sexual satisfaction.16 Mental wellbeing is a robust predictor of
Vaginismus: pelvic floor muscle spasm Merged dyspareunia and sexual desire and responsiveness; women who defined
leading to pain and obstruction with vaginismus themselves as being in good mental health were less likely
penetration
to report distress about their sexual relationship than women
who reported lower mental wellbeing scores.17 Studies have
Abbreviation: DSM = Diagnostic and Statistical Manual of Mental shown a high correlation between low desire and measures of
Disorders
low self-image, mood instability and tendency towards
anxiety.18 In addition, several factors are commonly cited
as distractions from sexual activity, including concerns
This article provide an update on FSD terminology, an regarding one’s own/partner’s arousal, fear of pregnancy,
understanding of the various gynaecological problems and fear of sexually transmitted disease and lack of privacy.8
their effects on sexual function, as well as the impact of Conservative societal stereotypes with traditional gender-
gynaecological treatments. We also assess the effectiveness of based expectations exert a profound effect on women’s
various therapeutic modalities for this condition. sexuality. In some cultures, women may be expected to be
Psychosexual counselling is outwith the remit of submissive recipients of sex, leading to negative consequences
this article. regarding arousal and orgasm. Although these views are
generally fading, they remain prevalent in some societies.19
Epidemiology
Causes of female sexual dysfunction
Epidemiological studies have indicated a prevalence of sexual
problems in women of between 30% and 60%. The Healthy sexual function involves a complex interplay between
commonest sexual problem is lack of interest in sex, anatomical, vascular, neurological, hormonal and
followed by inability to experience orgasm and painful psychological factors. Thus, aetiology of FSD is broad and
intercourse.1,8 Studies use different criteria for defining FSD, often multifactorial. Table 2 categorises medical,
hence it is difficult to know the true prevalence. However, gynaecological and psychosocial disorders that may affect
only 21% of women with sexual problems sought help.1 sexual function; however, several other medical illnesses can
Every general practitioner (GP) will see several women or also affect sexual function in some way. Various medications
couples per year presenting with sexual problems.9 In women have also been implicated in FSD (Box 1).
attending a gynaecology clinic, the prevalence of sexual
concerns has reportedly been as high as 98%.10 Despite this,
Clinical assessment
FSD can be overlooked. It is often disguised as unresolved
complaints and requests for repeated investigations.11 Patients presenting with gynaecological problems commonly
Furthermore, clinicians often avoid discussing sexual have underlying sexual dysfunction. This can be caused by
problems, citing reasons such as limited time and training, physical problems, psychological factors or a combination of
embarrassment and absence of effective treatment options.12,13 both. However, patients are often reluctant to volunteer this
information. There is frequently an aspiration that treatment
of gynaecological issues will alleviate sexual problems, but it
Normal sexual response cycle
is important for patients to have realistic expectations of
The female sexual response cycle is poorly understood and what can be achieved prior to undergoing any form of
challenging to define owing to multiple overlapping treatment. This is only possible if a baseline assessment of

ª 2021 Royal College of Obstetricians and Gynaecologists 13


Female sexual dysfunction

Willingness to
become receptive

Motivation
Sexual stimuli with
appropriate context
Multple reasons and
Spontaneous ‘innate’
incentives for
desire
insitigation of or
agreeing to sex
Psychological and
biological processing

Nonsexual rewards: Sexual satisfaction


emotional intimacy, with/without orgasm
well-being,
Subjective
from sexual avoidance arousal

Arousal and responsive


sexual desire

Figure 1. Sex reponse cycle14

sexual function is conducted, which should form part of any


Impact of obstetric conditions/
routine gynaecological consultation.
gynaecological problems
Taking a brief sexual history during a new patient visit can
help to identify issues and indicate to the patients that Pregnancy and childbirth
discussion of sexual concerns is welcome. In a busy Sexual desire can often decrease during pregnancy.1 This
gynaecology clinic, where the presenting complaint is not commonly persists into the postnatal period, with factors such
FSD, a few quick screening questions such as, ‘Do you have as the demands of caring for a new baby, fatigue, hormonal
any concerns about your sex life?’ will help identify any changes, perineal wound healing, breastfeeding, postnatal
underlying problem and can be used to begin the depression and change in body image all being implicated.
conversation (Table 3).20 The LOFTI acronym (listening, Indeed,sexual problemsappear to bepermanentlyincreasedafter
observing, feelings, thinking and interpreting)21 has been childbirth, with 83% experiencing problems in the first
proposed when assessing sexual problems in women 3 months, declining to 64% at 6 months, but never reaching
attending with underlying psychosexual problems. levels comparable to nulliparous women (38%). It is widely
Clinicians must not make any assumptions about the reportedthatmodeofdeliveryis relatedto postnataldyspareunia,
patient’s sexual behaviour. It is best to mirror the patient’s with operative vaginal delivery being particularly implicated,
sexual vocabulary so she can relate and understand the carrying at least a two-fold increased risk compared with
discussion. Some women may respond best to open spontaneous vaginal delivery.25 Furthermore, operative vaginal
questions, while others may feel more comfortable giving delivery is associated with a persistent rate of dyspareunia of
more precise answers to specific questions.19 Others may find 14% at 12 months. The protective effect of caesarean section on
it easier to complete a written sexual function questionnaire, sexual function appears to be limited to the first 6 months of
such as the Female Sexual Function Index.22 There are also the postnatal period compared with spontaneous vaginal
condition-specific questionnaires to assess sexual function. delivery with an intact perineum (3.4% dyspareunia).26
For example, the Prolapse and Incontinence Sexual Function
Questionnaire (PISQ-31)23 and the IUGA Revised version Menopause
(PISQ-IR)24 are routinely used in many urogynaecology The prevalence of FSD in postmenopausal women varies
clinics. Quality of life questionnaires also provide a useful from 68–86%. In a study of women aged 40–69 years, 71%
quantitative measure of baseline sexual function and can be reported they were sexually active.27 In this age group,
repeated following interventions to assess response. common sexual complaints include loss of desire, decreased
Aspects to consider when a more detailed history, frequency of sex, dyspareunia, vaginal dryness and
examination and investigation is required are shown dysfunction of the male partner. In a study of women aged
in Box 2. 40–62 years, age was found to negatively influence all

14 ª 2021 Royal College of Obstetricians and Gynaecologists


Kershaw and Jha

Table 2. Causes of female sexual dysfunction Table 2. (Continued)

Group Subgroup Examples Group Subgroup Examples

Medical Cardiovascular Atherosclerosis Menopause


Hypertension
Ischaemic heart disease Psychosocial Age
Peripheral vascular disease Obesity
Diabetes Smoking, alcohol, drug misuse
Heart failure Socioeconomic class
Relationship difficulties
Neurological Spinal cord injury Life stressors
Stroke Mental health disorders, e.g.
Parkinsonism depression, anxiety, obsessive
Multiple sclerosis compulsive disorder
Diabetic neuropathy Sexual abuse
Traumatic memories
Endocrine Thyroid disease Negative body image
Hyperprolactinaemia Suppressive societal stereotypes
Adrenal insufficiency
Hypopituitarism

Gastrointestinal Inflammatory bowel disease


Faecal incontinence
Irritable bowel syndrome
Liver failure

Rheumatological Inflammatory arthritis Box 1. Medications implicated in female sexual dysfunction


Systemic lupus erythematosus
 Anti-androgens, e.g. cimetidine, spironolactone
Miscellaneous Breast cancer  Anticonvulsants
Chronic kidney disease  Anticholinergics
 Antidepressants, e.g. selective serotonin reuptake inhibitors (SSRIs)
Pelvic Gynaecological Prolapse  Anti-estrogens, e.g. tamoxifen, gonadotrophin-releasing hormone
disorders Fibroids (GnRH) analogues
Endometriosis  Antihistamines
Sexually transmitted infections  Antihypertensives
Gynaecological cancer/precancer  Aromatase inhibitors, e.g. letrozole
Infertility  Sedatives and hypnotics
Childbirth  Hormonal contraception
Congenital mullerian anomalies  Sympathomimetic amines
Previous gynaecological surgery  Metoclopramide
 Metronidazole
Urological Overactive bladder  Cyclophosphamide
Stress urinary incontinence
Urological cancer

Functional Vaginismus domains of sexual function, while menopause only affected


Chronic pelvic pain pain and lubrication.1 It seems that ageing itself, and the
Painful bladder syndrome
associated effects on physical and psychological health status,
Vulval Vulvovaginal atrophy can have a more significant impact on sexual function than
disorders Lichen sclerosus/planus the menopause itself.
Systemic dermatoses affecting the
vulva
Sexually transmitted infections Subfertility
Female genital mutilation In couples who are trying to conceive, the goal-orientated
Previous vulval surgery approach to sex can result in the measurement of success or
failure of sexuality in terms of the ability to produce a child,
Hormonal Premenstrual syndrome
Pregnancy rather than the pleasure derived from it. When struggling to
Breastfeeding conceive, the woman may harbour feelings of being defective,
Premature ovarian failure or experience loss of self-worth and body image, leading to a
decreased sexual desire, sexual arousal disorders and

ª 2021 Royal College of Obstetricians and Gynaecologists 15


Female sexual dysfunction

Table 3. Screening questions for assessment of female sexual Box 2. Clinical assessment of female sexual dysfunction
dysfunction
History
Screening question Further assessment
 Medical history
 Current medication
Do you have anyconcerns If answer no, no further questions  Obstetric history
regarding your sex life?  Systems review
 Psychiatric history
Are you currently sexually active? If answer no, ask  Social circumstances
“Is that related to your current  Current life stressors
health problems?"  History of sexual abuse and female genital mutilation

Examination
Are the problems with: Assess for desire/arousal disorder
 General examination with particular attention to vascular and
 Sexual desire/libido Assess for female orgasm disorder
neurological systems
 Sexual arousal (including
 Inspection for vulvar pathology
vaginal lubrication problems)
 Speculum examination to inspect condition of vagina and cervix and
 Orgasm
assess for prolapse
 Gentle bimanual examination to elicit tender points and scarring,
Are you experiencing any pain Assess for genitourinary syndrome
assess for pelvic mass
related to intercourse of menopause (GSM), vulval
 Assess pelvic floor tone
(penetration or deep pelvic)? dermatoses pelvic floor muscle
 Cotton bud evaluation od vestibule for localised tenderness if
dysfunction, pelvic pathology
indicated by history
If anything changes, feel free to Gives permission to patient to Investigations
ask in future broach the subject in future
 Follicle-stimulating hormone or estradiol if symptoms of deficiency
consultations.
and not known to be menopausal
 Free androgen index and sex hormone binding globulin
 Thyroid function tests if features of thyroid disease
 Prolactin if amenorrhoea/galactorrhoea
 Ferritin if features of iron deficiency
 Test for hyperlipidaemia and diabetes if indicated by clinical
assessment
anorgasmia. Scheduling sexual activity when trying to  Sexual health screen if indicated
conceive can also be a problem.1

Pelvic floor dysfunction Patients should be informed of this as part of the


Up to 50% of women presenting with urogynaecological consent process, so they understand that sexual function
problems report FSD.1 Stress urinary incontinence (SUI), could worsen as a result of surgery. Altered perception of
overactive bladder and other lower urinary tract symptoms genital health after surgery, with associated fear of
can have a negative effect on all domains of sexual function. damaging themselves, can also have a negative impact on
Fear of odour, embarrassment, loss of self-esteem and coital FSD. However, despite the theoretical risks, on the whole
incontinence can all have a considerable impact. Up to one- sexual dysfunction improves following both prolapse
third of women with pelvic organ prolapse (POP) also report repair and stress incontinence surgery.
FSD. Women with POP are more likely to report A recent systematic review examining the effect of native
embarrassment and avoidance of sex, dyspareunia, dryness tissue prolapse repair on sexual function showed that 47%
(53%), lack of sensation (60%), vaginal obstruction (59%), improved, 39% remained unchanged, 18% deteriorated and
orgasmic disorders and coital urinary/faecal incontinence.28 4% reported de novo dyspareunia – although this review was
Suffering with both prolapse and incontinence has a unable to separate results by compartment.30 Increased
cumulative negative effect on sexual function in all postoperative dyspareunia was found consistently when
domains. FSD does not appear to correlate with a anterior and posterior repairs were combined in the same
particular compartment of prolapse. procedure; many gynaecologists may consider a two-stage
Kuhn et al.29 showed that desire, lubrication and sexual procedure for sexually active women requiring repair to both
satisfaction improved significantly, and orgasm remained compartments. When performing pelvic floor repair, ensure
unchanged, in women who used a pessary for POP and were that vaginal length is maintained, excessive vaginal excision
sexually active. is avoided and introital calibre is preserved.31 Regarding
In the surgical treatment of POP and SUI, vaginal vault prolapse, sacrospinous fixation was asso-
reconstructing local anatomy and alleviating symptoms ciated with higher rates of dyspareunia than abdominal
does not necessarily ensure optimal sexual function. mesh sacrocolpopexy.32

16 ª 2021 Royal College of Obstetricians and Gynaecologists


Kershaw and Jha

A systematic review noted that following surgery for SUI is more debilitating to sexual function than radical
(mid-urethral tape/colposuspension/autologous fascial sling), hysterectomy. The growing interest in FSD after pelvic
coital incontinence probably improves.33 Overall sexual surgery has led to the development of nerve-sparing
function probably remains unchanged, although there is a surgical techniques.
small possibility of improvement or even deterioration
following surgery. The retropubic or obturator approach Female genital mutilation
does not influence sexual function.33 Female genital mutilation (FGM) types 2 and 3 can affect all
Some studies show promising results regarding the effect aspects of sexual function and are associated with post
of sacral nerve stimulation and percutaneous tibial nerve traumatic stress disorder (PTSD), low self-esteem, disturbed
stimulation on FSD in patients undergoing treatment for self-identity, desire/arousal disorders and orgasmic disorders,
pelvic floor dysfunction.34,35 as well as pain and obstruction during intercourse.39
Management should be multifaceted, with a combination
Dysfunctional uterine bleeding and pelvic pain of approaches including psychotherapy. However, despite
Endometriosis, fibroids and adenomyosis may be associated best efforts, some women will have permanent dysfunction.
with dyspareunia. Erratic, heavy or painful menstrual Psychosexual counselling may be required to address
bleeding can also affect sexual function considerably. their problems.
Sexual function after hysterectomy has been studied Many of the surgical treatments described for the
extensively. It has been hypothesised that damage to the treatment of underlying gynaecological problems can
autonomic nerve endings of the cervicovaginal area and induce psychosexual problems postoperatively because of
vaginal shortening may interfere with lubrication, orgasm factors such as loss of fertility, disfigurement, depression and
and sexual pleasure.36 In addition, hysterectomy may have anxiety about one’s desirability as a sexual partner.40 Anxiety
psychological effects, leading to loss of feminine identity and regarding a return of normal sexual function heightens these
self-esteem. The largest prospective study to date is the problems. A period of psychosexual adaptation is often
Maryland Women’s Health Study, which found that, at required before sexual function returns to normal. Partners
24 months post-hysterectomy, there was increased frequency may also be affected psychologically owing to concerns about
of sexual activity and improvement in dyspareunia, orgasm, causing harm following surgery.41
libido and vaginal dryness.37 The surgical approach
(abdominal, vaginal, laparoscopic) did not affect sexual
Management
outcomes. The method of vaginal cuff closure did not impact
on sexual function.31 Furthermore, a randomised controlled A multidisciplinary approach is often required when
trial (RCT) comparing total versus subtotal hysterectomy managing FSD.19 For example, a patient suffering from
found no difference in postoperative dyspareunia, quality of genitopelvic pain disorder (vaginismus) may benefit from
orgasm or sexual satisfaction. Concomitant oophorectomy cognitive behavioural therapy (CBT), vaginal dilator use,
can, however, be implicated in FSD, particularly in lubricants, pelvic floor physiotherapy and relaxation
premenopausal women, because of the resultant abrupt techniques. Even after treatment of an underlying
reduction in estrogen and testosterone production. Hormone medical/gynaecological cause, the history of FSD may
replacement therapy (HRT) is usually recommended for have longer lasting psychological effects and the patient
patients under the age of 50 years undergoing bilateral may still benefit from psychosexual counselling/
oophorectomy. Replacement testosterone can also be offered psychological interventions.
if necessary.
General principles
Gynaecological precancer/cancer
Patients with an abnormal cervical smear result were  Educating the patient (and partner, where relevant) about
found to have a negatively affected sexual function in all normal physiological response and anatomy may be
domains and more negative feelings towards necessary. Physiological changes related to ageing and
their partners.38 implicated medical conditions should be explained.
There is a high prevalence of FSD amongst gynaecological  Lifestyle modifications, nonpharmacological therapies and
cancer patients, with 74% reporting low sexual desire and psychosexual counselling may be considered first-line
40% suffering from dyspareunia. There are direct effects of intervention in cases where aetiology is not physical.
disease and treatment, as well as psychological and  Review medications and, in conjunction with the GP/
behavioural changes that disrupt sexual function. prescriber, consider alternatives or reduced doses of
Complaints in this patient group include vaginal dryness, medications implicated in FSD.
short vagina, inelastic vagina and dyspareunia. Radiotherapy  Treatment of underlying gynaecological/medical condition.

ª 2021 Royal College of Obstetricians and Gynaecologists 17


Female sexual dysfunction

never achieved orgasm to learn how to do so without the


Lifestyle modifications
pressure of interacting with their partner.
Weight loss, smoking cessation, reduction in alcohol Frequent masturbation in couples was associated with
consumption, establishing a healthy diet and a regular relationship dissatisfaction, suggesting that it may not be
exercise regime are all valuable interventions for improving healthy for a couple to replace partnered sexual activity with
FSD and health.42 individual sexual activity. Indeed, there is evidence to suggest
Dedicating specific time to spend with their partner can that partnered sexual activity may create a higher level of
also help to improve women’s quality of sexual life.43 emotional wellbeing.19
Clitoral vacuum/therapy devices are handheld, battery-
Nonpharmacological therapies operated devices with a small, soft plastic cup that applies a
gentle vacuum over the clitoris and a low-level vibratory
Physiotherapy sensation to cause increased blood flow.52 They are designed
Pelvic floor exercises that focus on the functional control of to be used three or more times a week for approximately
each muscle in the pelvis can be helpful for women suffering 5 minutes at a time. Small studies have shown that use of this
from genitopelvic pain disorder.44 Practising contracting and device may improve arousal and orgasm;53 however, these
relaxing the pelvic floor can help bring this under voluntary have not been tested in well-conducted trials.
control. Deep pelvic relaxation is important to practice when Vibration devices are designed for both clitoral and vaginal
also using vaginal dilator therapy. stimulation. A relationship between vibrator use and positive
Pelvic floor physiotherapy is also part of the first-line sexual functioning has been reported.19
management of SUI and first-stage POP.45 Following a 6-
month course of pelvic floor physiotherapy, 39% of women
reported an improvement in sexual function. Pelvic floor Psychotherapies
exercises were associated with increased control, strength and Cognitive behavioural therapy/sex therapy
awareness of the pelvic floor, improved self-confidence, Cognitive behavioural therapy (CBT)/sex therapy focuses on
sensation of a ‘tighter’ vagina, improved libido and orgasms, identifying and modifying maladaptive thoughts,
resolution of pain with intercourse and heightened sexual expectations and behaviours that negatively affect sexual
gratification for partners.46 No difference was found between functioning. Strategies are suggested to improve the couple’s
standard physiotherapy and electrical stimulation.47 emotional connection and communication, but the evidence
Zahariou48 evaluated the effect of pelvic floor muscle is controversial.54 When couples are being consulted, they are
training on sexual function in a group of women with SUI. encouraged to focus on the strengths as well as weaknesses in
All domains of the FSFI were significantly improved their relationship. Homework assignments are given for the
12 months after treatment. couple to practice skills, such as turning the idea of sexual
In a study of healthy women, strong or moderate pelvic obligation into pleasure, learning to focus on sensations
floor muscle contractions were associated with significantly rather than anxieties and communicating openly with their
higher scores on both orgasm and arousal domains of the partner. One approach is the use of sensate focus techniques,
FSFI compared with women with weak contractions.49 consisting initially of nonsexual physical touch with gradual
progression toward sexual touch. Partners are encouraged to
Vaginal dilators provide feedback about what touches are pleasurable to help
Dilators can be useful for women who experience involuntary reduce performance-related anxiety.55
pelvic muscle contraction (vaginismus) or vaginal stenosis.
Beginning with a small device, the dilators gradually increase Psychosexual counselling
in size until, ultimately, intercourse is introduced.50 Results The aim of psychosexual counselling is to understand and
are better when this is supervised, either by a specialist nurse manage emotional factors, which are not always experienced
or women’s health physiotherapist, to provide the support at a conscious level, but interfere with sexual performance
these patients require. Better outcomes have been reported and enjoyment. Counselling sessions are aimed at assessing
when used in conjunction with topical estrogen cream for the attitudes, anxieties and fantasies relevant to
menopausal women.51 understanding the sexual problem in conjunction with a
detailed physical examination. This may take place over
Self-stimulation and devices several consultations. During the consultation, issues relating
The benefits of self-stimulation have been reported in to the impact of upbringing and memories of family, social
literature, as women learn more about their sexual response life and religious beliefs56 on sexual function may be
cycle and become more familiar with their body. uncovered. Past relationships, self-esteem, previous sexual
Masturbation is an effective way for women who have abuse and trauma are also explored. Details of psychosexual

18 ª 2021 Royal College of Obstetricians and Gynaecologists


Kershaw and Jha

counselling are out with the remit of this article, but have vasomotor symptoms and vulvovaginal atrophy, systemic
been previously discussed in The Obstetrician & HRT would be appropriate62 following adequate discussion
Gynaecologist.21 However, all gynaecologists should have with the patient.
basic training in providing psychodynamic therapy and Following breast cancer treatment, women who are on
identifying patients who require formal input from a aromatase inhibitors for adjuvant therapy (as opposed to
psychosexual counsellor. tamoxifen) are more likely to suffer with sexual dysfunction.
Psychosexual counselling is practised by clinicians, This can affect compliance and there may be a place for the
including gynaecologists with adequate training (for use of local estrogens in this cohort following adequate
example, from the Institute of Psychosexual Medicine, discussion with the patient and her oncologist.63
IPM). It is available in many, but not all, areas on the
NHS. It adopts a psychodynamic approach, which attempts Intravaginal prasterone
to connect the mind to the body.21 For gynaecologists who Prasterone is a steroid precursor, which is converted to
lack training, it remains essential to recognise which women estrogen and androgens. Several studies have shown a
require input from a trained psychosexual counsellor. moderate benefit for vulvovaginal atrophy, although
prasterone has not been compared directly with other
Yoga, relaxation techniques, hypnotherapy treatments such as topical estrogen.
Since stress and fatigue contribute to FSD, stress
management activities such as yoga or meditation may be Ospemifene
beneficial. Furthermore, hypnosis and relaxation therapies Ospemifene is a selective estrogen receptor modulator, which
have been cited as promising interventions for vaginismus, is licensed for the treatment of vulvovaginal atrophy in
but there is no conclusive evidence to support their use women for whom topical estrogen is not suitable. This is
at present.57 supported by a systematic review and meta-analysis, which
found that ospemifene is an effective treatment for
dyspareunia secondary to vulvovaginal atrophy.64 However,
Medical therapies
the contraindications for ospemifene are similar to those for
Lubricants and vaginal moisturisers estrogen, including breast cancer, endometrial hyperplasia
Women who are menopausal, breastfeeding and/or suffering and history of venous thromboembolism, thereby limiting
with a genital arousal disorder may lack vaginal lubrication its use.
and experience dyspareunia.58 Topical lubricants and vaginal
moisturisers can be used to relieve these symptoms. These Tibolone
treatments can be used as required at the time of intercourse, Tibolone is a synthetic steroid with estrogenic, progestogenic
in addition to regular treatment with topical estrogen if and androgenic properties, commonly used for the treatment
appropriate. Women should be advised to use a lubricant of menopausal symptoms. A study by Nijland et al.65
that is physiologically similar to natural vaginal secretions.59 demonstrated that tibolone improved overall sexual
function, increased frequency of sex and reduced sexually
Hormones related personal distress in postmenopausal women with
FSD.45 However, tibolone is associated with a higher
Estrogen increased risk of stroke than other HRT options.66
A fall in estradiol levels can result in vaginal smooth muscle
atrophy and increased vaginal acidity, leading to Testosterone
discomfort.60 Systemic HRT in isolation may not always Testosterone production naturally declines after the
address these problems and vaginal estrogen may still be menopause. Low levels of testosterone are associated with
required to treat FSD related to vulvovaginal atrophy. decreased libido, arousal and orgasm. Testosterone therapy in
Topical estrogen is currently available in the form of a the form of a transdermal patch or gel has resulted in
vaginal ring, vaginal creams and vaginal pessaries. significant improvement in various domains of sexual
Breastfeeding women experiencing hormonal imbalance function in postmenopausal women,67 although there is a
caused by estrogen deficiency can also benefit from topical lack of long-term safety data and several undesirable side
estrogen as a treatment for dyspareunia and vaginal effects, including alopecia, hirsutism, acne, breast pain,
dryness.61 Reassurance may be given that symptoms will headache, adverse liver function, lipid profile change,
improve following cessation of breastfeeding. increased risk of cardiovascular disease, insulin resistance
The use of systemic estrogen in the form of HRT must be and metabolic syndrome. It is perhaps best suited to patients
considered carefully for the treatment of FSD alone. suffering from surgical menopause or a medical condition
However, for women suffering from a combination of resulting in androgen deficiency. In surgical menopause there

ª 2021 Royal College of Obstetricians and Gynaecologists 19


Female sexual dysfunction

is an abrupt 50% reduction in production of testosterone in Oxytocin and progesterone have no role in the treatment
contrast to the gradual decline in ovarian and adrenal of FSD.
androgen production that ordinarily occurs naturally
with age. Drug therapy
Guidelines published by the National Institute for Health Several drugs have been used for the management of FSD,
and Care Excellence (NICE)62 and Cochrane reviews68 on with variable results. These are discussed in Table 4.
menopause now recommend considering testosterone
supplementation as HRT for women with low sexual desire Surgical
if estrogen replacement alone is not effective. The American No operation is designed to improve sexual dysfunction and
College of Obstetrics and Gynecology42 suggests that, if evidence for a positive effect is lacking.
prescribed, a 3–6-month trial is recommended, with
assessment of testosterone levels at baseline and after 3–6 Lasers
weeks of initial use to ensure levels remain within the normal Women suffering from breast cancer are a particularly
range. It also suggests that if continuing therapy is used, vulnerable group, with a high prevalence of lubrication
follow-up clinical evaluation and testosterone measurement difficulties, dyspareunia and a low level of sexual desire.69
should take place every 6 months to assess for Topical estrogen is sometimes used off licence in this group
androgen excess. of women, but there is unwillingness to prescribe this long

Table 4. Drug therapy for female sexual dysfunction

Drug
group Examples Mechanism Evidence

Vasodilators Sildenafil (Viagra) Increases availability of cyclic guanosine Evidence for sildenafil is mixed
monophosphate (cGMP), which mediates vascular Has been shown to be beneficial in FSD secondary to
smooth muscle relaxation via nitric oxide signalling spinal cord injury and SSRI use
resulting in genital engorgement Large RCT of women with sexual arousal disorder
reported no benefit
Not licensed for FSD79

L-arginine, prostaglandin, All currently under investigation, no definitive


phentolamine, evidence to support use at present
vasoactive intestinal
peptide (VIP)

Dopamine Bupropion, Act centrally to influence behavioural states Dopamine agonists are effective in improving desire
agonists apomorphine, Given the central action of these drugs there is a in women with hypoactive desire disorder
cabergoline high occurrence of side effects, such as nausea, Cabergoline can improve FSD secondary to
vomiting and headaches antipsychotic-induced hyperprolactinaemia
Bupropion can help FSD related to SSRI use
Sublingual/intranasal apomorphine is currently
under investigation in the hope with will be quicker
acting and associated with few side effects

Serotonin Flibanserin Acts central to influence mood and behavioural FDA-approved from 2015 for treatment of
1a agonist/ states hypoactive desire disorder, although a systematic
2a review showed minimal or no improvement in
antagonist symptoms and a high rate of adverse effects
including dizziness, fatigue and nausea
Must abstain from alcohol to avoid hypotension/
syncope
Not licensed in UK

Muscle Tizanidine Centrally active alpha-2 agonist used as a muscle Superior to placebo in treating high-tone pelvic floor
relaxant relaxant dysfunction

Abbreviations: FDA = US Food and Drug Administration; FSD = female sexual dysfunction; RCT = randomised controlled trial; SSRI = selective
serotonin reuptake inhibitor

20 ª 2021 Royal College of Obstetricians and Gynaecologists


Kershaw and Jha

term. Lubricants and vaginal moisturisers have limited injection given was a 5-ml mixture of 0.25% bupivacaine, 2%
efficacy when used alone in women for the treatment of lidocaine, and 40 mg of triamcinolone per trigger point.
severe vulvovaginal atrophy. Three months after injections, 72% of women reported
Preliminary data for both erbium and carbon dioxide improvement.75 Other combinations of medications have
vaginal lasers in the treatment of vulvovaginal atrophy are also been used. The authors’ own preference is to use
promising. These may be an alternative for breast cancer bupivacaine, hyaluronidase and depot-medrone.
patients, but should not be introduced into clinical practice
without more robust evidence. In a recent systematic review, Botox injections to the pelvic floor muscles
vaginal laser therapy was effective in treating vulvovaginal Refractory vaginismus may respond to Botox injections
atrophy in breast cancer survivors, with improvement in into the puborectalis and pubococcygeus.76,77 This should be
dyspareunia, vaginal dryness and sexual function.70 There is used in adequately selected cases with appropriate patient
therefore an urgent need for RCTs to assess the long-term counselling because the evidence for its use is limited to very
safety and efficacy of lasers. specific conditions.

Genital cosmetic surgery Genital reconstructive surgery


Several surgical procedures have been developed that are In women undergoing distorting genital surgery, various
advertised as improving sexual function by altering the surgical techniques are employed to preserve/give provision
appearance and/or the function of the female genital tract. for sexual function in these patients. These may include local
Such procedures include labioplasty, vaginoplasty, perineoplasty and regional flaps and grafts, although further description of
and laser rejuvenation. They probably have an effect on body surgical reconstructive options is beyond the remit of
image, rather than a clinical effect. Evidence supporting the this article.
efficacy and safety of these procedures on sexual function
is lacking.6 Conclusion
FSD is a common condition with considerable detrimental
Vestibulectomy
effects on quality of life, but is unfortunately often
In vestibulectomy, the painful tissues of the vestibule are
overlooked by clinicians. As gynaecologists we must strive
identified and removed. An RCT by Bergeron et al.71 reported
to identify and explore sexual problems with our patients as
significantly less dyspareunia in patients with localised
we are uniquely placed to do so. This also allows for
vulvodynia who underwent vestibulectomy than those treated
evidence-based counselling regarding any future
with CBT and electromyographic biofeedback. However, in a
gynaecological treatment, including likely outcomes the
study by Das et al.,72 outcomes on long-term sexual function
patient can expect for their sexual function.
were more variable, with only 57% patients being satisfied
postoperatively. It is now rarely performed in the UK.
Disclosure of interests
SJ is an Associate Editor for The Obstetrician & Gynaecologist;
Fenton’s procedure
she was excluded from editorial discussions and had no
Fenton’s procedure can be offered when a patient experiences
involvement in the decision to publish.
dyspareunia secondary to narrowing, or skin-splitting at the
posterior fourchette, usually secondary to obstetric scarring.
Contribution to authorship
It is used rarely for vulval dermatoses, such as lichen
VK researched, wrote and edited the manuscript. SJ
sclerosus. However, benefit from this procedure is probably
instigated, researched, wrote and edited the manuscript.
modest and there is a paucity of evidence. Worsening of
Both authors approved the final version.
dyspareunia is a potential risk. A small study of 24 women by
Chandru73 showed that at 12 months postoperatively, 14
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ª 2021 Royal College of Obstetricians and Gynaecologists 23


DOI: 10.1111/tog.12789 2022;24:7–11
The Obstetrician & Gynaecologist
Commentary
http://onlinetog.org

TOGadvisor: the role of online feedback in obstetrics and


gynaecology
Lorraine S Kasaven BSc (Hons) MRCOG PGCert,a* Srdjan Saso PhD MRCOG,b Jara Ben Nagi MRCOG MD,c,d
Karen Joash BSc (Hons) MRCOG MSc PGCert, Joseph Yazbek MD MRCOG,f J Richard Smith MD FRCOG,g
e

Tom Bourne PhD FRCOG FAIUM,h Benjamin P Jones BSc (Hons) MRCOG PhDi
a
Clinical Research Fellow, Department of Cancer and Surgery, Imperial College London, UK and Department of Cutrale Perioperative and Ageing
Group, Imperial College London, UK
b
Honorary Clinical Lecturer, Department of Surgery and Cancer, Imperial College London, UK and Gynaecological Oncology Consultant, Queen
Charlotte’s and Chelsea Hospital, Imperial College NHS Trust, London W12 OHS, UK
c
Honorary Clinical Senior Lecturer, Department of Cancer and Surgery, Imperial College London, UK
d
Consultant Gynaecologist and Reproductive Medicine and Surgery Specialist, Centre for Reproductive and Genetic Health, London W1W 5QS, UK
e
Consultant Obstetrician and Gynaecologist, Queen Charlotte’s and Chelsea Hospital, Imperial College NHS Trust, London W12 OHS, UK
f
Honorary Clinical Senior Lecturer, Department of Cancer and Surgery, Imperial College London, UK and Consultant Gynaecological Oncology
Surgeon, Queen Charlotte’s and Chelsea Hospital, Imperial College NHS Trust, London W12 OHS, UK
g
Honorary Senior Lecturer, Imperial College London, UK and Consultant Gynaecological Oncology Surgeon, Queen Charlotte’s and Chelsea
Hospital, Imperial College NHS Trust, London W12 OHS, UK
h
Professor of Gynaecology, Imperial College London, UK and Consultant Gynaecologist at Queen Charlottes and Chelsea Hospital, Imperial College
NHS Trust, London W12 OHS, UK
i
Obstetrics and Gynaecology Trainee Registrar, Queen Charlotte’s and Chelsea Hospital, Imperial College NHS Trust, London W12 OHS, UK
*Correspondence: Lorraine S Kasaven. Email: lk226@doctors.org.uk

Accepted on 23 February 2021.

Please cite this paper as: Kasaven LS, Saso S, Ben Nagi J, Joash K, Yazbek J, Richard Smith J et al. TOGadvisor: the role of online feedback in obstetrics and
gynaecology. The Obstetrician & Gynaecologist 2022;24:7–11. https://doi.org/10.1111/tog.12789

at least £23 billion of consumer spending per year.2 In


Introduction
medicine, systematic patient feedback has been shown to help
In recent years there has been an exponential rise in online trainees identify areas of improvement, resulting in enhanced
feedback from patients reporting health experiences.1 While interpersonal skills.3 Institutionally, feedback can improve
undoubtedly facilitated by increased availability of and access healthcare provision and quality of services. This is
to the internet, a series of institutional changes within the epitomised by the fact that clinical outcomes are associated
UK’s National Health Service (NHS) has compounded the with patient satisfaction,4 to an extent whereby hospitals
uptake. In 2004, NHS trusts were obliged to report service rated poorly have higher mortality rates.5 However, evidence
outcomes to the Healthcare Commission to be published remains inconsistent regarding the association between
online, allowing public access to information. In 2007, the online ratings and quality of care,6 and there are various
launch of the NHS website provided a platform for patients ethical arguments that require consideration prior to
to evaluate clinicians and hospitals online. Consequently, in increased implementation. The aim of this commentary is
2016, NHS England implemented a strategy to incorporate to discuss and summarise these considerations.
technology into the future of the NHS, supporting digital
transformation to revolutionise the way health care is
Perceptions of online feedback
provided. The emphasis on a patient-centred approach has
facilitated the development of numerous physician feedback The successful implementation of new healthcare initiatives
websites, including iWantGreatCare, Care Opinion depends on the attitudes of the stakeholders involved.7 It is
and Doctoralia. therefore essential to consider healthcare professionals’
Feedback is integral to improving standards across perceptions of online feedback. Despite the intention to
disciplines. In the travel and hospitality industries, online improve health care, many healthcare professionals remain
feedback is fundamental and has been estimated to influence sceptical, with reluctance to embrace feedback websites.8 In a

ª 2022 The Authors. The Obstetrician & Gynaecologist published by John Wiley & Sons Ltd on behalf of Royal College of Obstetricians and Gynaecologists. 7
This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium,
provided the original work is properly cited.
TOGadvisor: the role of online feedback in obstetrics and gynaecology

survey of 1000 doctors, 57% perceived that online feedback is regulation.1 Such professional vulnerability is compounded
generally negative.9 However, analysis of 228 113 online further by doctors’ duty of candour to maintain
comments revealed a markedly higher frequency of positive confidentiality, thus restricting their ability to contextualise
evaluative words compared with negative (75% versus comments or defend themselves.
25%),10 suggesting attitudes may be influenced by Professional bodies, including the Medical Defence
unrealistically negative misconceptions.1 Moreover, a Union, provide guidance for doctors receiving negative
number of studies have demonstrated the motivations for online feedback. This includes responding to feedback
providing online feedback are often to praise a service, rather positively, addressing policies of the service provider
than to complain.11 publishing the comments, or requesting the right to be
The core drivers of online feedback are undoubtedly the forgotten online – acknowledged by the Court of Justice of
doctor and patient, with a shared goal to assess healthcare the European Union – through subtraction of search results
standards and improve quality of care. Figure 1 illustrates a from search engines including Google, Bing and Yahoo.15
model of online feedback encompassing these drivers, in Currently, there are a lack of distinctive considerations of
addition to a number of factors required by healthcare law specific to medical professionals seeking action against
providers deemed integral to improving patient experience, defamation.16 However, doctors can take legal action if
as described by the NHS Trust Development Authority online comments are perceived to injure the reputation or
framework for enhancing patient experience.12 discredit the individual in the estimation of peers within
Patients who give online feedback usually retain their society.16 Legal action does not guarantee a successful
anonymity, which facilitates the expression of honest outcome and may take a number of months to resolve,
opinions,13 thereby enhancing autonomy and empowering associated with expensive costs. Publicity from pursuing
them to leave negative or critical comments.1 Furthermore, legal action against libel may also draw further attention to
social media platforms such as Facebook, Instagram and the defamatory comment. Therefore, a number of doctors
Twitter are bound by statutory rights including the freedom may be discouraged from pursuing legal action. The
of speech.14 Therefore, members of the public are within Defamation Act 2013 provides a number of defences that
their rights to post uncensored content in the absence of peer may also be difficult to challenge. Evidence from consumer
review. Many doctors perceive the ability to write markets demonstrates that online responses to negative
unregulated comments as dangerous, exposing them to feedback improve satisfaction among those complaining17
professional vulnerability and risk of online bullying or and improve perceptions of trustworthiness.18 This further
defamation.1 Although NHS Choices report regulations are highlights the disadvantages doctors face. As such, the
in place to protect clinicians by removing inflammatory initiative to respond to online feedback in a regulated and
remarks, concerns remain regarding implementation in confidential manner may improve patient satisfaction and
practice and the inability to respond prior to publication,6 rebuild patient–doctor trust.
resulting in many doctors demanding more formal
Impact on doctors
Capacity and While positive feedback can enhance reputation and
capability to
Leadership potentiate career prospects, negative or malicious feedback
effectively collect
feedback in the public domain can conversely have a lasting negative
impact on a clinician’s career. Significant psychological
burden such as reduced confidence and self-esteem may
Patient Doctor arise, which in turn could impact clinical practice. Doctors
who receive complaints are twice as likely to report suicidal
thoughts, 77% more likely to suffer moderate to severe
depression and have twice the risk of moderate to severe
Reporting and Service Healthcare Analysis and anxiety.19 Moreover, data from more than 10 000 doctors
publication outcomes standards triangulation reported 45% of doctors felt powerless, 42% emotionally
distressed and 21% unsupported when dealing with patient
complaints.20 Reports of clinicians personally acquiring court
orders to remove online reviews21 highlight similar issues
Driving quality
that may arise as a consequence of negative online feedback.
improvement and
learning Obstetrics and gynaecology has one of the highest attrition
rates of all specialties (30%).22 A study of more than 3000
Figure 1. Model of online feedback obstetrics and gynaecology doctors in the UK identified that

8 ª 2022 The Authors. The Obstetrician & Gynaecologist published by John Wiley & Sons Ltd on behalf of Royal College of Obstetricians and Gynaecologists.
Kasaven et al.

36% fulfilled the criteria for burnout.23 The widespread from work colleagues, which anonymously assess clinical
implementation of online feedback may encourage performance and nontechnical competencies such as
comparison between peers, promoting competitive – rather professionalism and communication. As evidence suggests
than collaborative – working relationships, which may colleagues’ perceptions of a physician’s workplace behaviour
potentiate further the challenges of working in the correlate significantly with clinical performance,29 it could be
specialty. It is therefore unsurprising that the British argued that such assessments, which are completed by
Medical Association (BMA) have raised concerns regarding healthcare professionals governed by good clinical practice
slander and opposed clinician rating sites.24 and regulated by educational supervisors, would be more
For those working in private practice, there may also be appropriate in the public domain. Such a system would
significant financial implications for doctors exposed to poor negate many of the limitations associated with patient
reviews or suboptimal ratings. This is exemplified by data feedback and may provide a more robust online presence for
highlighting that patients who were exposed to a neighbour’s doctors. Alternatively, self-reported patient questionnaires
negative physician review were significantly less likely to can be considered a feasible feedback tool, although their
choose the physician than those exposed to a positive usage is limited by a lack of validity and reliability.30
recommendation only.25 However, doctors interpersonal skills questionnaires (DISQs)
are associated with high internal consistency that fulfils the
criteria for various types of validity, and as such they can be
Limitations
considered as a feedback tool.31,32 The efficacy of self-
Online feedback refers predominantly to interpersonal reported patient questionnaires is likely to be improved
skills, rather than clinical care received.10 It could be further, by collecting feedback immediately following the
argued that ratings focusing primarily on interpersonal doctor encounter and including regular reassessment by
skills do not correlate with professional competency, new patients.30
thereby bringing into question the validity of patient
feedback.6 This is reaffirmed by the fact online ratings of
Conclusion
doctors do not predict quality of care or peer assessment of
clinical performance.26 Questions have been raised There are multifactorial, varying and contrasting advantages
regarding how representative online feedback is of the and disadvantages of online feedback in obstetrics and
entire population,27 as those who post online comments gynaecology, as summarised in Box 1. Many doctors
are predominantly younger in age.28 Furthermore, the use remain sceptical about its implementation, owing to fears
of clinician rating websites is reliant upon the cognitive of negative, unregulated comments. Moreover, as positive
capability of the user and as such may exacerbate feedback does not necessarily constitute excellent clinical
inequality between educated and less educated patients, care, its role in the healthcare profession remains uncertain.
or indeed lower socioeconomic groups who do not have However, feedback, whether positive or negative, remains
access to the internet. essential for continued personal, professional and
Following a complaint, clinical practice has been shown to institutional improvement. With the continued uptake in
be more defensive,23 including healthcare professionals online platforms and the ongoing plans to transform the
performing more investigations, over referring or NHS into a digitalised healthcare system, it may be an
prescribing, avoiding performing procedures or not inevitable part of the future of being a doctor in obstetrics
accepting high-risk patients.19 Doctors may make the and gynaecology. An example of this is the COVID-19
correct clinical decision in the best interests of the patient, pandemic, which has demanded widespread restructuring of
but if the patient does not agree, an inappropriately negative NHS services and adaptation to the clinical care delivered
review may be left. For example, a woman with chronic pelvic within the specialty. Patients are increasingly encouraged to
pain expecting further investigation such as a diagnostic engage with technology and the internet, permitting a
laparoscopy in the first instance, may not agree with the number of elective services to continue. We may therefore
suggestion of a therapeutic trial of hormonal medication as anticipate an escalation in the application and relevance of
first-line treatment. Following such scenarios, doctors may social media and online feedback during this pandemic,
change their perfectly appropriate clinical practice to avoid which may continue for the foreseeable future. In a
future negative or malicious reviews. specialty where less face-to-face interaction is expected
from elective clinical work, online feedback will be
paramount in aiding professional development. As such,
Role in professional development
continued debate and ethical reflection is vital, with a view
Obstetrics and gynaecology trainees are required to complete to increasing regulation and enhancing protection for
work-based assessments, including team observation forms healthcare professionals.

ª 2022 The Authors. The Obstetrician & Gynaecologist published by John Wiley & Sons Ltd on behalf of Royal College of Obstetricians and Gynaecologists. 9
TOGadvisor: the role of online feedback in obstetrics and gynaecology

3 Greco M, Brownlea A, McGovern J. Impact of patient feedback on the


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 Evidence suggests that patient feedback can be used more hospital quality. Arch Intern Med 2012;172:435–6.
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 Patient ratings can be used to measure healthcare standards and 7 Ross J, Stevenson F, Lau R, Murray E. Factors that influence the
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ª 2022 The Authors. The Obstetrician & Gynaecologist published by John Wiley & Sons Ltd on behalf of Royal College of Obstetricians and Gynaecologists. 11
DOI: 10.1111/tog.12781 2022;24:67–72
The Obstetrician & Gynaecologist
Education
http://onlinetog.org

The blind spot: value-based health care in obstetrics and


gynaecology
Osama Naji MD MRCOG,a* Vivienne Souter MD FRCOG,b Edward Mullins PhD MRCOG,c
Jonathan Gaughran MRCS MRCOG,d Yasser Diab MSc MRCOG,e J Edward Fitzgerald BA MSc MRCS FRSPH,f
Tom Bourne PhD FRCOG FAIUM,g Edward Morris MD PRCOGh
a
Consultant Gynaecologist, Guy’s and St Thomas’ Hospital, London, UK
b
Medical Director, Obstetrical Care Outcomes Assessment Programme (OBCOAP), Foundation for Health Care Quality, Seattle, Washington, USA
c
NIHR Academic Clinical Lecturer in O&G, Imperial College London, UK
d
Doctorate Research Fellow in Gynaecology, Guy’s and St Thomas’ Hospital, London, UK
e
Lead of Service, Gynaecology Department, Guy’s and St Thomas’ Hospital, London, UK
f
Head of Healthcare, KPMG Islands Group, London, UK
g
Professor of Practice, Women’s Health, Imperial College London, UK
h
Consultant Gynaecologist, Norwich, UK and President, Royal College of Obstetricians and Gynaecologists, London, UK
*Correspondence: Osama Naji. Email: o.naji@alumni.imperial.ac.uk

Accepted on 14 February 2021. Published online 7 January 2022.

Key content Learning Objectives


 Continuing financial constraints on the UK’s National Health  To understand the principles of value-based health care.
Service means the need for clinicians to provide high-quality care  To highlight the importance of adopting ‘cost-conscious’ care
in a cost-effective way has never been greater. within daily clinical practice.
 While the medical education system equips doctors with skills to  To learn the differences between ‘cost’, ‘charge’, ‘price’
provide safe clinical care, it should also provide an understanding and ‘reimbursement.
of healthcare costs and cost-effectiveness analysis.  To encourage developing value-based competencies for future
 Value-based care is becoming a key paradigm in women’s health medical workforce through utilising out of programme placements
services, where clinicians must employ strategies for delivering and digital resources.
value, rationalising costs and capitalising on the use of
Ethical Issues
emerging technologies. 
 The calculation of value of an intervention for providers and
The ethical obligation of clinicians to consider cost may encompass
justice and equity. However, the impact of practicing value-based
service users may differ; care must be taken to ensure this concept
health care is yet to be evaluated.
is adapted for, and not imposed on healthcare systems.
 Engaging trainees in systems transformation and embedding the Keywords: cost effectiveness / health care costs / health economics /
concepts of ‘do no financial harm’ are essential to ensure value based health care
sustainable healthcare services.

Please cite this paper as: Naji O, Souter V, Mullins E, Gaughran J, Diab Y, Fitzgerald JE, Bourne T, Morris E. The blind spot: value-based health care in obstetrics
and gynaecology. The Obstetrician & Gynaecologist 2022;24:67–72. https://doi.org/10.1111/tog.12781

A key barrier to determining the value of health care is the


Introduction
lack of metrics at a national level, which could provide
Healthcare spending is currently the single greatest outlay for feedback on the investment made in health care. A composite
the UK Government. It has increased dramatically in the past health index, comprising health outcome measures,
65 years from 7.7% of total public expenditure in 1955/56 to modifiable risk factors and the social determinants of
17.9% in 2018/19 (Figure 1).1 This upward trend in healthcare health is under consideration by the Office for National
costs is likely to continue given the ageing population and Statistics.2 Potential shortcomings of this measure include the
increasing service costs. The Office for Budget Responsibility selection and availability of indices and the use to which
(OBR) predicts health expenditure will rise further from 7.2% policymakers may put them; however, it would be a step
of the national income today to 10.2% in the next 20 years. towards valuing health as an asset at a national level.3
This equates to an excess of £66 billion. Therefore, developing The high proportion of the UK budgetary spend on health
strategies for sustainable healthcare funding is critical for the care could drive a shift to value-based care and the search for
National Health Service (NHS).1 more effective and affordable solutions. New artificial

ª 2021 Royal College of Obstetricians and Gynaecologists 67


Value-based health care in obstetrics and gynaecology

Figure 1. Annual UK public spending on health in real terms (2019–2020 prices) and as a percentage of national income. Reproduced with
permission from the Institute of Fiscal Studies.1

intelligence (AI) technologies, for example, are growing more come to restart the conversation about the role of doctors in
advanced paradigms to empower patients; healthcare healthcare spending. In this article we shed light on the basic
professionals need to adopt AI as a way to quickly analyse principles of value-based care. We explain the importance of
large amounts of patient data to gain insights about patient acquiring a good level of healthcare financial literacy to
populations. To utilise those insights, interaction is needed deliver not only safe and effective women’s clinical care, but
between data, technology and healthcare experts. Indeed, also value for those who deliver, receive and pay for that care.
models have been proposed in which computer-generated
analytics are augmented by human decision-making and
Definition and perspectives
algorithms are informed by medical experts.3
The General Medical Council (GMC) states that one of a In 2006, Michael Porter, Professor of Health Economics at
doctor’s duties in the workplace is to “use resources Harvard Business School, published the book Redefining
efficiently for the benefit of patients and the public”. Health Care: Creating Value-Based Competition on Results.
However, the role of clinicians, both in training and at This book invites transition to a system of value-based health
consultant level, in determining national healthcare care (VBHC). This has become a controversial issue in the
expenditure has been largely absent over the past 20 years. healthcare sector, with many organisations struggling with
Unfortunately, there is little provision in the medical the questions of where to start, how to define value and how
education system to help address this challenge; healthcare to make the value of health care more transparent.5 VBHC is
professionals must be familiar with basic statistics without fundamentally focused on what constitutes ‘value’ for
formal training in interpreting cost-effectiveness records. patients and it is defined as, “Patient-relevant outcomes,
This is not because of their lack of interest in healthcare costs, divided by the costs per patient across the full cycle of care to
since nearly 80% of physicians believe that controlling these achieve these outcomes”. It seeks to maximise the value of
costs is a part of their responsibilities, but rather to care for patients, while at the same time reducing the cost of
historically regarding administrative and cost-controlling this care (Figure 2).
proposals as restrictive to the scope of their daily
clinical practice.4
Today women represent 51% of the UK population and
47% of the workforce.2 Therefore, it is important that future
obstetricians and gynaecologists are equipped to understand
cost information just as they must understand complex
maternal medicine and other genomic treatments. This will
not be achieved by merely providing them with cost data, but
rather the skill set to interpret these data to facilitate optimal
decision-making. With the current competing healthcare
needs and limited resources facing the NHS, the time has Figure 2. Calculation of patient values.

68 ª 2021 Royal College of Obstetricians and Gynaecologists


Naji et al.

Although the concept of VBHC emanated from the US  Information and communications technology solutions
healthcare system, the principles are universal. The UK, like are urgently required to ensure efficiency savings without
many other countries with a state-dominated healthcare compromising quality.
structure, had historically lower costs and favourable  To invest in future training programmes that match future
mortality statistics. However, the NHS is now facing an service needs in a value-based, cost-saving environment.
accelerated rate of cost increases like those in the United
States, with new evidence suggesting alarming quality
Value-based maternity care: health
problems that are comparable to the US model. It is
outcome measures
therefore important to stress that lower quality does not
save money; conversely, it often leads to complications Confirming value requires measuring outcomes and costs.
necessitating additional care and ultimately substantially When evaluating clinical outcome measures, maternity care
raising healthcare and indirect costs.5 is exceptional in that it involves two patients: the pregnant
person and their baby. Patient input is also a key component
to evaluating quality in pregnancy care. Although periodic
Is VBHC achievable in the NHS?
patient surveys evaluating maternity care are undertaken in
The UK has long been on the front line among European the UK, there is no standardised method on how to best
countries looking to expand their use of VBHC. A key to measure patient-reported outcome measures (PROMs) and
shifting the focus to ‘value’ is reducing variation in the patient-reported experience measures (PREMs).9 The US
care pathway. In the wake of devolution of health care in childbirth experience survey published by Gregory et al.10
1999, the NHS has experimented with pay-for-performance found that patient characteristics (parity, demographics and
models to identify and eliminate localised variation in pregnancy complications) were – perhaps surprisingly – not
treatment pathways. This seemed to be ineffective and, closely correlated with patient satisfaction with childbirth
since then, the NHS continued to be the subject of care in hospital. However, patients who felt they received
periodic structural reforms.6 An important step towards understandable explanations from their doctor said that staff
standardising care within the NHS was establishment of members were compassionate, that they knew how to care for
the influential National Institute for Health and Care themselves and their baby on discharge and were overall
Excellence (NICE) in 1999. NICE had two specific roles: more satisfied with their care.
approval of prescription medicines through technology Recognising a lack of standardised outcome measures as a
appraisal and provision of evidence-based guidelines on barrier to applying VBHC in maternity care, the International
various topics. A relevant example is the NICE Consortium for Health Outcomes Measurement (ICHOM)
recommendation for the wider use of long-acting proposed a standardised set of perinatal outcome measures
reversible contraception (LARC) after commissioning a that includes both maternal and newborn clinical outcomes
cost-effectiveness analysis based on a decision analytic and PROMs.11 The clinical measures focus on adverse
model.7 The NHS, by law, must fund medicines that NICE outcomes such as maternal death, intensive care unit
approves within 90 days of its published decision. On the admission, blood transfusion and neonatal injury and death.
other hand, the Health and Social Care Act (2012) was Positive clinical outcomes, such as undisturbed birth, which
designed to put clinicians in charge of commissioning has also been identified by providers and consumers as an
healthcare services, replacing 152 primary care trusts with important perinatal quality indicator, are not included. The
211 specialised Clinical Commissioning Groups (CCGs). patient reported measures include five patient surveys across
These reforms are widely credited with increasing, rather the antepartum period and up to 6 months postpartum.
than decreasing healthcare costs.8 ICHOM also identified 13 ‘case-mix’ factors that are patient
In 2011 the Royal College of Obstetricians and characteristics or risk factors (for example, maternal age,
Gynaecologists (RCOG) published its Expert Advisory parity, body mass index, pre-existing medical conditions),
Group Report High Quality Women’s Healthcare. This was which may influence the rate of ICHOM outcome measures.
in response to the NHS reforms, and workforce and financial It is important to account for case-mix factors to allow fair
pressures, acknowledging that delivery of women’s health comparison of quality measures among different healthcare
services in the current configurations is unsustainable.8 The systems. The ICHOM measure set currently lacks
key recommendations were: implementation and validation studies, but is a positive
 Commissioning women’s health care through a managed move towards developing a comprehensive perinatal
women’s health network to facilitate better coordination of quality standard.
services, standardisation of delivery and improved VBHC requires consideration of the cost in addition to
clinical outcomes. quality. Currently, several innovative models of care have

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Value-based health care in obstetrics and gynaecology

been proposed to improve quality, decrease costs and


Table 1. Summary of differences between various financial
promote PROMs/PREMs. These are delivered through transactions. Reproduced with permission from the AMA Journal of
incorporation of mid-level clinicians, community midwives Ethics.16
and, additionally, holistic patient-centred care, group
Term Definition
prenatal visits, patient engagement in self-monitoring
and telemedicine.12
Cost The expense incurred to providers to deliver
healthcare services to patients
Costs of care
Charge or Price The amount asked by a provider for a healthcare
In 2012/13, maternity care alone was responsible for service
approximately £2.6 billion of NHS spending, corresponding
to approximately £3,700 per birth and representing 2.8% of all Reimbursement A payment made by a third party to a provider, this
may be for every service delivered, every hospital
healthcare expenses.13 Most women receiving maternity care
stay, or each episode of hospital admission
in the NHS have favourable outcomes and positive
experiences of care. However, the Government has pledged
to make further improvements in women’s health care. For
example, since 2007 there has been an increase in midwifery-
led units, more consultant involvement in care, and progress units for procedures often considered to be day cases.16 This
has been made in line with the Government’s commitment to represents a huge challenge to provide standardised, efficient
improve outcomes. The Department of Health has set a and quality care. However, with challenges often come
‘Maternity Safety Ambition’ to halve the rate of stillbirth, opportunities. NHS RightCare is an initiative to decrease
neonatal death, maternal deaths and brain injuries by 2025 unnecessary variation in care, improve population health and
and to reduce the preterm birth rate to 6% in the same time promote fairer health care in terms of access, patient
span.14 Investments made in the Maternity Transformation experience and outcomes. Its goal is for everyone to have
Programme, hopefully balanced by a decrease in medicolegal appropriate, timely care in the optimal healthcare settings
costs, could potentially improve quality of care and reduce and to utilise resources as effectively and efficiently as
adverse outcomes.15 However, reforming the payment system possible.18 There are several quality metrics for this
for maternity care remains key and value-based interventions programme, but for the scope of this article we focus on
in maternity care services have received relatively three important points from obstetrics and gynaecology
little attention. training and education perspectives:
 Engaging more trainees with support from executive-level
leaders in projects related to both PROMs and PREMs.
Gynaecology services: right person, right
This will give them permission to innovate, help unlock
place, first time
problems and feed learning and insights back into
In 2017/18, there were 3 690 908 attendances to outpatient the system.
gynaecology services, with a 78% attendance rate, which  Helping trainees through integrated educational
decreased from 82% in 2007/08.16 This trend may indicate a programmes to better understand healthcare cost terms
rise in hospital or patient cancellation rates, or a pure to differentiate between value measures and quality
reduction in the need for outpatient services. Therefore, the measures. We summarise some of the common terms
entire ranges of elective care services needs urgent redesign at in Table 1.19
the system level to achieve better demand management that  Assisting newly appointed consultants through fast-track
could improve patient care, both from the value of patient health management courses to equip them with the skill
perspectives and from the efficiency standpoint. The NHS sets required to lead with sufficient financial acumen.
Long Term Plan sets out ambitions to alternative models of
care to avoid up to 30% of face-to-face appointments17.
VBHC competency
These include addressing the needs of local populations and
targeting interventions for those people most at risk. Traditionally, it has been routine practice for UK trainees in
Technology offers promising possibilities to support this obstetrics and gynaecology to learn to provide the best
transformation. Below are some of the challenges and possible care for women and expectant mothers, leaving the
opportunities in gynaecology care. cost considerations aside. The time to revisit this concept is
There is geographical and socioeconomic variation in both due. The ‘best possible’ needs to be taken in the full meaning:
access and service provision to several gynaecology services, it must be safe, effective and also valuable – in other words,
and this leads to variation in hospital stay between different ‘worth it’ for the woman and her baby.20

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Naji et al.

defined method for providing both value for money and


Table 2. Innovative approaches to promote VBHC approach among
frontline clinicians. Reproduced with permission from the Journal of quality assurance.23 In 2016, as part of the NHS Mandate,
Graduate Medical Education.23 NHS England developed the Clinical Entrepreneur Training
Programme. This is another promising step designed to offer
Approach Description
opportunities for junior doctors from various specialties to
nurture their entrepreneurial interests during clinical
I-CARE Traditional, morning report-style teaching training. The programme provides entrepreneurial support,
Interactive Cost- run by senior clinicians to conduct a safe including access to mentors and coaches, internships and
Awareness Resident diagnostic evaluation at a low expense introductions to commercial organisations.
Exercise
Reflecting the GMC guidelines promoting excellence in
SOAP-V Included V for value medical education and training, the Royal College of
Modified Subjective- The model prompts trainees to consider if Surgeons of England (RCS) has stated that suitable
Objective-Assessment- ordering a test would change
surgeons can acquire healthcare management experience in
Plan management of the patient and if the
patient’s values were incorporated into many different settings, including the private sector.24 An
the care plan example is the joint partnership between RCS and McKinsey
& Company for a 1-year fellowship in healthcare
OR-SCORE Providing surgeons with feedback on the
management. In this programme, trainees receive
Operating Room costs of their surgical cases to reduce
Surgical Cost Reduction unnecessary waste structured training and practical experience through
It provides price transparency of surgical working on client-facing projects in healthcare
preparation time, surgical time and improvement and reforms in the NHS.25 Trainees in
supply costs in a snapshot, followed by
discussions to coach surgeons practising
obstetrics and gynaecology could be supported to follow
at higher costs suit by facilitating out-of-programme placements and
training partnerships with other stakeholders in both
government and the private sectors.

The future
With the current upsurges in digital health, an integration It has been estimated that up to 30% of total healthcare
of VBHC into undergraduate medical curriculums is needed. spending is wasted.26 In the UK, perhaps one development to
Albeit in a different healthcare system, most US medical capture in the post-COVID era is utilisation of the virtual
schools now integrate discussions of cost, value and world and digital technology. The implementation of
effectiveness into their curricula. A recent survey by the telephone clinics in several NHS hospitals is an important
Association of American Medical Colleges (AAMC)21 found step, provided appropriate patient selection; it can certainly
that 129 of 140 responding medical schools had offered a provide high-value care, good patient satisfaction and
course on the cost of health care during the 2013/14 academic acceptable costs to both the environment and the
year. In 2015, Gupta and colleagues from the USA 22 healthcare system. Healthcare professionals in obstetrics
developed the ‘Teaching Value in Healthcare Learning and gynaecology must be equipped to influence and drive
Network’; an online Google+ community. Its aim was to health policy for the benefit of the women they care for.
create a short-term platform to disseminate innovation to Furthermore, future trainees will have a responsibility to
provide high-value care to educators and system leaders. The ensure women’s healthcare is cost-effective and sustainable –
network had three components: particularly considering that obstetrics and gynaecology
 Thirty-minute webinar discussions with national leaders occupied almost 50% of the total value spent by the NHS
in healthcare on overall clinical negligence claims in the 2019/20 financial
 Online discussion forum to facilitate sharing slides year accounts.27 If universal coverage provided by the NHS
 Online storehouse for disseminating materials related to for women’s health services is to continue, training in value-
value innovations based health care delivery is needed. Therefore, dedicating
Both speakers and members of the network reported great the early years of the training curriculum to build
satisfaction with the format and usefulness of the innovations foundations of health care financial literacy, basic
shared. We summarise some of the topics discussed management and simulation training can set up a suitable
in Table 2.22 platform to build on, and will ensure that UK obstetrics and
In UK postgraduate obstetrics and gynaecology training, a gynaecology training remains an attractive and forward-
welcome step forward over the past 10 years was ‘simulation- thinking specialty for both domestic and
based education’ (SBE), which has proved to be a well- international graduates.

ª 2021 Royal College of Obstetricians and Gynaecologists 71


Value-based health care in obstetrics and gynaecology

Disclosure of interests 10 Gregory KD, Korst LM, Saeb S, Greene N, Fink A, Fridman M, et al.
Childbirth-specific patient-reported outcomes as predictors of hospital
TB is supported by the National Institute for Health Research satisfaction. Am J Obstet Gynecol 2019;220:201.e1–19.
(NIHR), Biomedical Research Centre based at Imperial 11 Nijagal MA, Wissig S, Stowell C, Olson E, Amer-Wahlin I, Bonsel G, et al.
College Healthcare NHS Trust and Imperial College Standardized outcome measures for pregnancy and childbirth, an ICHOM
proposal. BMC Health Serv Res 2018;18:953.
London. The views expressed are those of the author(s) 12 Gareau S, L opez-De Fede A, Loudermilk BL, Cummings TH, Hardin, JW,
and not necessarily those of the NHS, the NIHR or the Picklesimer AH, et al. Group prenatal care results in Medicaid savings with
Department of Health. better outcomes: a propensity score analysis of centering pregnancy
participation in South Carolina. Matern Child Health J 2016;20:1384–93.
13 Department of Health. Maternity Services in England Report. London:
Contribution to authorship National Audit Office; 2013 [https://www.nao.org.uk/wp-content/uploads/
ON drafted the manuscript. All authors participated in 2013/11/10259-001-Maternity-Services-Book-1.pdf].
14 Department of Health. Safer maternity care: the national maternity safety
concept discussions, revised and amended/revised strategy – progress and next steps. London: Department of Health; 2017
subsequent versions and approved the final version [https://assets.publishing.service.gov.uk/government/uploads/system/
for submission. uploads/attachment_data/file/662969/Safer_maternity_care_-_progress_
and_next_steps.pdf].
15 NHS England. Maternity Transformation Programme update. London: NHS
England; 2018 [https://www.england.nhs.uk/wp-content/uploads/2018/05/
References 04-pb-24-05-2018-maternity-transformation-programme.pdf].
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DOI: 10.1111/tog.12786 2022;24:79–81
The Obstetrician & Gynaecologist
MBRRACE-UK update
http://onlinetog.org

MBRRACE-UK update: Key messages from the UK and


Ireland Confidential Enquiries into Maternal Death and
Morbidity 2021

The latest report from the UK and Ireland Confidential the leading cause of direct maternal death during or up to
Enquiries into Maternal Deaths and morbidity, the eighth in 6 weeks after the end of pregnancy. Maternal suicide
the now annual report format, includes surveillance and remains the leading cause of direct deaths occurring within
Confidential Enquiries covering the period 2017–19.1 The a year after the end of pregnancy.
report also includes reviews into the care of women who died
during or after pregnancy in the Republic of Ireland as well as
Key messages for care
the UK. Following the annual topic-specific format, this
report includes topic-specific reviews into the care of women Care of older mothers
who died from mental health-related causes, venous  The older women whose care was examined fell broadly
thromboembolism, homicide and malignancy. The report into two groups. Some were women who had several
also includes a Morbidity Confidential Enquiry into the care previous children; their pregnancy was often unplanned,
of women who gave birth aged over 45 years. many were late to engage with maternity services and often
they chose to make decisions against the advice of those
caring for them. Half were women who had conceived
Key facts and figures
through assisted reproduction techniques, frequently with
 There was a statistically nonsignificant decrease in the donated embryos and often had multiple pregnancies.
overall maternal death rate in the UK between 2014–16 Many of these women had not undergone a pre-pregnancy
and 2017–19, which is now 8.79 per 100 000 maternities assessment and embarked on pregnancy with pre-existing
(95% confidence interval [CI] 7.58–10.12). There remains medical conditions such as hypertension and other cardiac
a greater than four-fold difference in maternal mortality risk factors. For women who choose to embark on assisted
rates among women from Black ethnic backgrounds and reproduction treatment, there is always an opportunity for
an almost two-fold difference among women from Asian pre-pregnancy assessment and optimisation of a woman’s
ethnic backgrounds compared with white women. Women health. This may include weight reduction, smoking
who live in the 20% most deprived areas have double the cessation and changes to medication. The risks of
maternal mortality rate of women who live in the 20% pregnancy should be clearly described including the
most affluent areas. chance of needing iatrogenic preterm delivery with its
 The majority of women who died had multiple co- associated neonatal complications.
morbidities. Eight percent of the women who died during  The majority of older pregnant women whose care was
or up to a year after pregnancy in the UK in 2017–19 were reviewed for the purposes of this report had pre-existing
at severe and multiple disadvantages. The main elements co-morbidities, assisted reproduction, obesity, or all three.
of multiple disadvantage were a mental health diagnosis, Several had pregnancies additionally complicated by
substance use and domestic abuse. multiple pregnancy. On the basis of this multitude of
 Cardiac disease remains the largest single cause of maternal risk factors in addition to older maternal age, the majority
deaths. Neurological causes (epilepsy and stroke) are the should be offered aspirin to prevent pre-eclampsia,
second most common cause of maternal death. There screening for gestational diabetes, serial growth scans and
remains a concerning number of deaths due to Sudden thromboprophylaxis antenatally and/or postnatally.
Unexpected Death in Epilepsy (SUDEP). Guidance relevant to the care of older pregnant women,
 There was a statistically nonsignificant decrease in due to their multiple risks, is contained within multiple
maternal death rates from direct causes between 2014–16 guidelines, and fewer than a third of women received care
and 2017–19. Thrombosis and thromboembolism remain in line with every relevant guideline. In view of the

ª 2021 Royal College of Obstetricians and Gynaecologists 79


MBRRACE-UK update

increasing numbers of women giving birth at older ages, it medication has been discontinued in advance of, or
would be helpful to have a single collated source of during, pregnancy, it is important to ensure women have
recommendations for the care specifically of older women. an early postnatal review to determine whether they should
Until such a collated source exists, it is important to be recommence medication.
aware of all relevant preventive interventions  Women with substance misuse are often more vulnerable
and investigations. and at greater risk of relapse in the postnatal period, even
 Older women, particularly those who conceive if they have shown improvement in pregnancy. They
spontaneously (rather than with donor eggs), are more should be reviewed for re-engagement in the early
likely to have a fetus with trisomy 21 or other postpartum period where they have been involved with
chromosomal abnormality. It is important that other addictions services in the immediate preconception period
aspects of their care are not delayed while investigations or during pregnancy.
are performed. Consultant appointments and evidence-
based effective preventive interventions such as aspirin Care of women with cancer
should not await the results of prenatal diagnosis.  Several women became pregnant during or shortly after
 Although older women becoming pregnant spontaneously completing cancer treatment and no one had discussed
may be less likely to receive pre-pregnancy counselling, the contraception. All medical staff, of whatever specialty,
opportunity to provide post-pregnancy counselling is should be aware that women of reproductive age may
equally important for future pregnancies and for joining become pregnant during treatment for mental and
up obstetric and medical care to optimise a woman’s long- physical health conditions and therefore need
term health. contraceptive advice. All staff should be able to provide
that advice.
Care of women with mental health problems and  Several women died from metastatic melanoma diagnosed
multiple adversity during pregnancy. Most of the women who died had a
 There were many examples where women should have relatively short gap between completion of their cancer
been referred to specialist services and were not. It was treatment and their pregnancy. When the pregnancy was
striking how few women were engaged with specialist planned, it was unclear whether women had received any
community services. Where pathways into care were not pre-pregnancy advice. Women should receive specialist
clear, there was, at times, confusion over which service had advice regarding the gap after treatment before becoming
been engaged and delays in referral to the specialist mental pregnant – a space of 2 years is recommended for most
health team. As services expand further, including the cancers where guidance exists. It is important to recognise
development of maternity psychological therapies teams, it that the gap is not because pregnancy is thought to impact
will be important to ensure new services are fully on the course of the disease but because recurrence risks
embedded within clear care pathways. These pathways are greatest in the 2 years after initial diagnosis and
should take into account all other aspects of perinatal pregnancy may impact on the treatment options the
mental health provision, including specialist roles within women can receive.
midwifery and obstetric services, in order to avoid any  Guidance is needed on how quickly women should be seen
confusion over roles and responsibilities. in an obstetric consultant clinic after pregnancy is
 Over one-third of women who died by suicide had diagnosed following a previous cancer diagnosis. Several
experienced a pregnancy or postnatal loss event and more women were not seen until mid-late second trimester by
than half of women who died from substance misuse had a which time discussions about continuing the pregnancy
similar loss event. Women are even more at risk after a could not be undertaken. Women with active or very
perinatal loss event, including child removal, and good recent cancer treatment should be seen by an obstetric
communication and care coordination are consultant in the first trimester to allow discussion of
therefore essential. individual risks and choices.
 There were a number of examples of failure to prescribe or  There were several examples where imaging was not done,
deprescribing because the woman was pregnant. There both for diagnosis and staging. The reluctance to use
were also women who were on prescribed medication on appropriate imaging led to a delay making diagnoses and
discovering the pregnancy and who made the decision to resulted in some women presenting on multiple occasions
discontinue. For several, there was no re-evaluation in the with worsening symptoms, some of which, such as
postnatal period, when they were more likely to be vomiting and fatigue, were attributed to pregnancy.
vulnerable to relapse, of whether they would benefit Additionally, where symptoms had been attributed to
from recommencing medication, either prophylactically or pregnancy, they were not followed up postnatally. It is
to manage emergent symptoms. If psychotropic essential to ensure symptoms of possible cancer are

80 ª 2021 Royal College of Obstetricians and Gynaecologists


MBRRACE-UK update

followed up postnatally. If they do not resolve, they are conversely, the additional risk women are placed under
unlikely to be due to pregnancy. during pregnancy by clinician behaviours which focus on
concerns over a woman’s pregnancy rather than concerns
Prevention and management of thromboembolism over a woman herself. This emphasises again the need for
 Women’s risks, before, during and after pregnancy, are not care pre-pregnancy, during pregnancy and after pregnancy by
static. Periods of increased risk of venous the multidisciplinary team skilled in pregnancy medicine.
thromboembolism (VTE) occur during and after The morbidity enquiry into the care of women giving birth at
pregnancy, which underpins recommendations to aged 45 or over illustrated many of the complexities of
reassess VTE risk at every opportunity. Several women intersecting risk and risk perception. Pregnancy at advanced
had episodes of hospital admission, concurrent maternal age is known to be associated with higher rates of
gastrointestinal infections when they became dehydrated maternal mortality, higher rates of pregnancy loss and other
or periods of immobility, when their risk of VTE was pregnancy complications, and yet the average age at first
raised. This risk was either not recognised, because childbirth continues to increase. Very few women planning
reassessment was not carried out, or not acted on. pregnancy at an advanced maternal age had a clearly
Assessment of VTE risk is an expected standard for any documented discussion over the potential health impacts to
hospital admission. This applies to all healthcare settings in them or their unborn child.
secondary care (maternity, surgical, medical) and mental Beginning to address these wider cultural and structural
health hospitals. biases affecting women’s care on the basis of their pregnancy
 Assessors observed wide variation in the tools used to or the potential to become pregnant is fundamental to the
document VTE risk, some of which did not reflect national prevention of maternal mortality. These issues intersect with
guidance and therefore risk was assessed incorrectly. A other biases women experience due to their ethnicity,
recommendation made previously in these reports was the socioeconomic status, co-morbidities, language, disability
need for a tool to make risk scoring consistent. This review or social complexity. Addressing these structural biases must
again emphasises that not only is a tool required, but that start with early medical, midwifery and nursing education.
there is a need to ensure the tool is consistent across all
systems and routes of use (paper or electronic). Marian Knight MA DPhil FFPH FRCP Edin FRCOG
 Assessors noted that several women who died were likely MBRRACE-UK Maternal Programme Lead, NIHR Professor of Maternal
to have been omitting their low molecular weight heparin and Child Population Health, National Perinatal Epidemiology Unit,
prophylaxis partially or completely, and it is important Nuffield Department of Population Health, University of Oxford, Old Rd
Campus, Oxford, OX3 7LF, UK
that women’s adherence with administration is taken into Email: marian.knight@npeu.ox.ac.uk
account in any antenatal or postnatal assessment.

Reference
Conclusions
1 Knight M, Bunch K, Tuffnell D, Patel R, Shakespeare J, Kotnis R, Kenyon S,
The recurring theme identified in this report revolves around Kurinczuk JJ (Eds.) on behalf of MBRRACE-UK. Saving Lives, Improving
risk and the fact that risk is not static, but dynamic. There is a Mothers’ Care - Lessons learned to inform maternity care from the UK and
Ireland Confidential Enquiries into Maternal Deaths and Morbidity 2017–19.
need for recognition of the role that pre- and post-pregnancy Oxford: National Perinatal Epidemiology Unit, University of Oxford 2021.
actions can have in significantly decreasing risk, and, Available at: www.npeu.ox.ac.uk/mbrrace-uk

ª 2021 Royal College of Obstetricians and Gynaecologists 81


DOI: 10.1111/tog.12794 2022;24:73–6
The Obstetrician & Gynaecologist
CPD
http://onlinetog.org

CPD questions for volume 24 issue 1

CPD credits can be claimed for the following questions With regard to the impact of menopause on
online via the TOG CPD submission system in the RCOG sexual function,
CPD ePortfolio. You must be a registered CPD participant of
7. age negatively influences all domains of
the RCOG CPD programme (available in the UK and
sexual function. ThFh
worldwide) in order to submit your answers.
8. approximately 50% of women aged 40 to
Completion of TOG true/false questions can be claimed as a
69 years are sexually active. ThFh
Specific Learning Event. Participants can claim two credits per
set of questions if at least 70% of questions have been answered With regard to the relationship between pelvic floor
correctly. CPD participants are advised to consider whether the dysfunction and sexual function,
articles are still relevant for their CPD, in particular if there are 9. up to one-third of women with pelvic organ
more recent articles on the same topic available and if clinical prolapse report sexual problems. ThFh
guidelines have been updated since publication. 10. experiencing both prolapse and incontinence
Please direct all questions or problems to the CPD Office. has a cumulative negative effect on
Tel: +44 (0)20 7772 6307 or email: cpd@rcog.org.uk. sexual function. ThFh
The blue symbol denotes which source the questions refer 11. after native tissue prolapse repair, the most
to including the RCOG journals, TOG and BJOG, and RCOG likely outcome is no change in
guidance, such as Green-top Guidelines (GTGs) and sexual function. ThFh
Scientific Impact Papers (SIPs). All of the above sources are 12. sacrospinous fixation is associated with lower
available to RCOG Members and Fellows via the RCOG rates of dyspareunia compared with
website. RCOG Members, Fellows and Associates have full abdominal sacrocolpopexy. ThFh
access to TOG content via the TOG app (available for iOS
and Android). With regard to the impact of hysterectomy on
sexual function,
13. the vaginal route is associated with worsening
TOG Female sexual dysfunction dyspareunia compared with other routes. ThFh
14. subtotal hysterectomy is associated with less
With regard to sexual dysfunction,
dyspareunia than total hysterectomy. ThFh
1. it is more common in men than women. ThFh 15. laparoscopic vaginal cuff closure is associated
2. it is investigated more in men than women. ThFh with lower rates of dyspareunia. ThFh
3. for a diagnosis to be made, symptoms must be
In the treatment of female sexual dysfunction,
present for more than 50% of the time and for
more than 6 months and cause 16. weight loss in obese patients has been shown
significant distress. ThFh to help improve sexual function. ThFh
4. about 10–20% of women are affected. ThFh 17. both systemic and vaginal estrogen have been
used effectively to treat sexual dysfunction
With regard to the impact of pregnancy and childbirth on
related to vulvovaginal atrophy. ThFh
sexual function,
18. systemic progesterone may be offered to
5. sexual desire often increases patients with a history of estrogen-dependent
during pregnancy. ThFh cancer to improve sexual function. ThFh
6. when compared with spontaneous vaginal 19. in surgical menopause, there is an abrupt 50%
delivery with an intact perineum, the reduction is testosterone production. ThFh
protective effect of caesarean section on sexual 20. Botox injections into the perineum is a
function is limited to the first 6 months of the recognised treatment option for
postnatal period. ThFh refractory vaginismus. ThFh

ª 2022 Royal College of Obstetricians and Gynaecologists 73


CPD

TOGInvestigation and management of TOG Cervical cancer in pregnancy: diagnosis,


postcoital bleeding staging and management
Recognised causes of postcoital bleeding include, Cervical cancer,
1. cervical ectropion. ThFh 1. is the commonest gynaecological malignancy
2. endometriosis. ThFh diagnosed in pregnancy. ThFh
3. cervical intraepithelial neoplasia. ThFh 2. incidence rates are set to plateau over the
4. submucosal fibroids. ThFh next 10 years. ThFh
5. chlamydial infection. ThFh 3. symptoms differ in pregnancy when compared
with the nonpregnant patient. ThFh
Initial investigations of postcoital bleeding in women in
4. invades locally first (affecting the vagina,
the reproductive age group should include,
parametrium and uterosacral ligaments). ThFh
6. urinary pregnancy test. ThFh 5. has the potential to metastasize to the fetus. ThFh
7. cervical screening test in those under 25 years
During pregnancy,
of age. ThFh
8. swabs to test for sexually 6. routine recall smear tests are best deferred
transmitted infections. ThFh until 3 months postpartum. ThFh
9. colposcopy. ThFh 7. colposcopic assessment of the cervix as part of
10. endometrial pipelle biopsy. ThFh managing positive cervical screening results is
best deferred until postpartum. ThFh
Regarding cervical cancer,
8. an excisional biopsy of the cervix has an
11. it is the leading cause of postcoital bleeding in increased risk of haemorrhage. ThFh
women under age 25. ThFh 9. the use of FIGO staging of cervical cancer is
12. a negative screening test excludes diagnosis. ThFh not recommended. ThFh
13. it is predominantly caused by HPV-6 and 10. magnetic resonance imaging is the first-line
HPV-11. ThFh method for staging of cervical cancer. ThFh
14. HIV-positive women should be 11. sentinel lymph node biopsy is considered an
screened annually. ThFh important step in staging of cervical cancer. ThFh
15. about 1 in 2400 women aged under 25
With regard to the management of patients diagnosed with
presenting to primary care with
cervical cancer in pregnancy,
postcoital bleeding will have this as
the cause. ThFh 12. delivery is best by caesarean section. ThFh
13. termination of pregnancy is recommended
Regarding management of postcoital bleeding,
prior to commencing treatment. ThFh
16. a cervical biopsy is recommended before 14. it is best provided by an experienced
offering cryotherapy for a multidisciplinary team. ThFh
cervical ectropion. ThFh 15. they are at higher risk of postnatal depression. ThFh
17. hysteroscopy and endometrial sampling is 16. it is recommended that the placenta is sent
indicated in peri- and postmenopausal for histology. ThFh
women with a cervical polyp. ThFh 17. the option to undergo ovarian transposition
18. nonpregnant women diagnosed with before treatment should be discussed with the
chlamydia require test of cure following aim of preserving ovarian function. ThFh
completion of treatment. ThFh
Neoadjuvant chemotherapy,
19. if a lower genital tract cancer is suspected,
knowing the biopsy results is 18. is a contraindication to breastfeeding. ThFh
essential before referral to a tertiary 19. is required at a higher dose in pregnancy. ThFh
cancer centre. ThFh 20. is the first-line treatment choice for patients
20. ospemifene is a recognised treatment in cases diagnosed with stage 1A cervical cancer
secondary to atrophic vaginitis. ThFh in pregnancy. ThFh

74 ª 2022 Royal College of Obstetricians and Gynaecologists


CPD

19. a recognised complication of sclerotherapy is


TOGAccessory cavitated uterine peritoneal leakage of the instilled alcohol. ThFh
malformations (ACUMs): an unfamiliar 20. studies have reported intrauterine adhesions
cause of severe dysmenorrhoea following surgical treatment. ThFh
Accessory cavitation uterine malformations (ACUMs),
1. are lesions involving the uterine cavity. ThFh TOGPregnancy in underweight women:
2. contain a central cavity lined with implications, management and outcomes
functional endometrium. ThFh
Conditions associated with a body mass index (BMI)
3. contain clear fluid in the cavity. ThFh
of <19.5 kg/m2 include,
4. are typically found inferior to the attachment
of the round ligament. ThFh 1. hypothyroidism. ThFh
5. are surrounded by a myometrial mantle with a 2. hyperthyroidism. ThFh
concentric arrangement of smooth 3. malnutrition. ThFh
muscle fibres. ThFh 4. anorexia nervosa. ThFh
5. gestational diabetes. ThFh
With regard to the current understanding of the aetiology
and clinical characteristics of ACUMs, BMI below 19.5 kg/m2 is associated with,
6. they are thought to arise from duplication and 6. cardiac anomalies in the fetus. ThFh
persistence of the Wolffian ducts. ThFh 7. preterm delivery. ThFh
7. they are seen to mostly affect 8. fetal growth restriction. ThFh
peri-menopausal women. ThFh 9. pre-eclampsia. ThFh
8. the most common presenting symptom Pregnant women with low BMI,
is dysmenorrhea. ThFh
9. pelvic pain as a symptom is thought to be due 10. are more likely to develop postpartum
to the stretching of the cavity from the cyclical haemorrhage after delivery. ThFh
accumulation of blood. ThFh 11. are more likely to be over the age of 40 years. ThFh
12. are less likely to have
With regard to investigation of patients suspected to intrapartum complications. ThFh
have ACUMs,
Complications associated with hyperthyroidism in
10. transvaginal ultrasound examination of the pregnancy include,
pelvis will show a characteristic fluid content
of the cavity. ThFh 13. preterm labour. ThFh
11. a defining ultrasound characteristic is 14. an increased risk of intrauterine fetal death. ThFh
increased vascularity within the cavity. ThFh 15. early onset pre-eclampsia. ThFh
12. on magnetic resonance imaging, the Women with a known eating disorder in pregnancy,
myometrial mantle appears hypointense on
16. are at risk of relapse during pregnancy. ThFh
T2-weighted images. ThFh
17. should be screened for additional mental
13. histologically, the lining of the cavity contains
health disorders. ThFh
glands and stroma. ThFh
Signs that may suggest an underlying eating
Differential diagnoses of ACUMs include,
disorder include,
14. a unicornuate uterus with a functioning
18. male pattern hair loss. ThFh
rudimentary horn. ThFh
19. parotid enlargement (hamster sign). ThFh
15. a haemorrhagic degenerating fibroid. ThFh
20. fine facial hair. ThFh
With regard to the treatment of ACUMs,
16. hormonal suppression has been shown to Preconception health in the well
TOG
alleviate pain symptoms. ThFh woman
17. the levonorgestrel intrauterine system is the
treatment of choice in young patients. ThFh With regard to preconception care,
18. there is evidence that laparoscopic surgical 1. it improves maternal and neonatal outcomes. ThFh
excision has a better outcome than 2. more than 50% of all pregnancies are
laparotomy excision. ThFh currently unplanned. ThFh

ª 2022 Royal College of Obstetricians and Gynaecologists 75


CPD

3. a high socioeconomic status is associated with 12. female undernutrition contributes to 20% of
poorer maternal and neonatal outcomes. ThFh maternal deaths worldwide. ThFh
4. interventions during the maturation phase of 13. zinc deficiency has been linked to
gametes has no impact on preterm births. ThFh
obstetric outcomes. ThFh
Concerning interventions in preconception care,
With regard to maternal behaviour before and
14. the recommended minimum amount of aerobic
during pregnancy,
activity per day is 30 min of intense activity. ThFh
5. smoking in pregnancy has been associated 15. a population increase in maternal
with a 20% increased incidence of haemoglobin of 1 g/dL has been shown to
late stillbirths. ThFh reduce the risk of mortality by
6. ingestion of three standard units of alcohol approximately 35%. ThFh
per week increases the risk of
With regard to infections in pregnancy,
developmental and cognitive disability in
the offspring. ThFh 16. Zika virus has been shown to cause
7. folic acid supplementation has been shown to microcephaly in the fetus. ThFh
prevent the recurrence risk of neural tube 17. genital herpes is a recognised cause of
defects by up to 75%. ThFh encephalitis in the newborn. ThFh
8. fortification of food with iron has been shown 18. the combination of pyrimethamine and
to have a greater impact on pregnancy than sulfonamides is safe to administer in the first
iron supplementation. ThFh trimester for the management of
toxoplasmosis infection. ThFh
With regard to nutritional health,
With regard to exposure to chemicals and their impact
9. the prevalence of obesity in women globally is
on health,
estimated to be more than 20%. ThFh
10. a body mass index of 22 kg/m2 has been 19. high lead levels are associated with
associated with multiple preterm birth. ThFh
obstetric complications. ThFh 20. high mercury levels in the mother are
11. stunted growth is often the result of associated with child deficits in language,
adequate nutrition. ThFh attention and memory. ThFh

76 ª 2022 Royal College of Obstetricians and Gynaecologists

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