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Estimation of The Impact of Genital Warts On Health-Related PDF
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STI Online First, published on March 13, 2008 as 10.1136/sti.2007.029512
Sarah Woodhall,1,2 Tina Ramsey,2 Chun Cai,2 Simon Crouch,1 Mark Jit,3 Yvonne
Birks,1 W John Edmunds,3 Rob Newton,1 Charles JN Lacey2,4
Correspondence to:
Sarah Woodhall
Sexual Health and HIV Research Unit
Department of GU Medicine
31 Monkgate
York, YO31 7WA
Email: sarah.woodhall@hyms.ac.uk
Tel: 01904 721193
Fax: 01904 642116
Key words
Condylomata Acuminata, Quality of Life, Papillomavirus Vaccines, Human
papillomavirus, Genital warts
1
Copyright Article author (or their employer) 2008. Produced by BMJ Publishing Group Ltd under licence.
Downloaded from http://sti.bmj.com/ on March 26, 2018 - Published by group.bmj.com
ABSTRACT
Objectives One of the two new human papillomavirus (HPV) vaccines protects
against HPV types 6 and 11, which cause over 95% of genital warts, in addition to
protecting against HPV types 16 and 18. In anticipation of HPV vaccine
implementation, we measured the impact of genital warts on health-related quality of
life (HRQoL) to assess potential benefits of the quadrivalent over the bivalent
vaccine.
Methods Genitourinary medicine clinic patients ≥18 years old with a current
diagnosis of genital warts were eligible; 81 consented and were interviewed by a
member of the research team. A generic HRQoL questionnaire, the EQ-5D
(comprising of EQ-5D index and EQ visual analogue scale (VAS) scores), and a
disease-specific HRQoL instrument, the CECA10, were administered. Previously
established UK population norms were used as a control group for EQ-5D
comparisons.
Results Cases (with genital warts) had lower EQ VAS and EQ-5D index scores than
controls. After adjusting for age a mean difference between cases and controls ≤30
years old (n=70) of 13.9 points (95%CI, 9.9 to 17.6, p<0.001) for the EQ VAS and
0.039 points (95%CI, 0.005 to 0.068, p=0.02) on the EQ-5D index (also adjusted for
sex) was observed. The difference between cases and controls for the EQ VAS was
especially notable in young females.
Conclusions Genital warts are associated with a significant detriment to HRQoL. The
potential added benefit of preventing most cases of genital warts by HPV vaccination
should be considered in decisions about which HPV vaccine to implement in the UK.
2
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INTRODUCTION
Genital warts are the most commonly diagnosed viral sexually transmitted infection in
the UK. In 2006 over 80,000 first episode diagnoses were made in 2006 in
Genitourinary Medicine (GUM) clinics alone.4 The estimated peak incidence among
20 to 24 year old males is 794/100,000 and 767/100,000 in 16 to 19 year old females.5
The disease course may be protracted even with treatment. It has been estimated that
at least 25% of cases recur within three months and episodes can vary from weeks to
occasionally years in duration.6 Despite the heavy burden of disease, there has been
little research carried out to assess the impact of genital warts on health-related
quality of life (HRQoL)7. A small number of studies have assessed the way in which
people with genital warts are affected8-12 but few of these included a comparison
group or were designed for use in economic analyses. One study asked female
volunteers to rate the value of different health states related to HPV infection, but this
did not collect data from individuals who actually had genital warts.13 One Canadian
study has used the EQ-5D in 31 females with genital warts, as part of research into the
cost-effectiveness of HPV vaccination.14 We are unaware of any such study having
been carried out in the UK or Europe.
The potential for prevention through vaccination is considerable given that over 95%
of genital warts can be attributed to HPV types 6 and 11.3;15 This study was conducted
to provide data on the impact of genital warts on HRQoL, which could then be used in
analyses of the cost-effectiveness of HPV vaccination. Generic measures of HRQoL
can be used to compare outcomes across different health states and we therefore used
one such instrument (the EQ-5D16) to compare quality of life in patients with genital
warts to that in the general population.
METHODS
Cases consisted of men and women attending the York GUM clinic during a three
month period. Adults aged ≥18 years old with a current diagnosis of genital warts
were eligible. This included those attending for a first or follow-up visit. All GUM
clinics in the UK collect data on the number of episodes of sexually transmitted
infections (STIs) on a quarterly basis and each diagnosis is assigned a KC60 code.17
The codes for genital warts are C11A (incident cases), C11B (recurrent genital warts)
and C11C (warts which persist for over 3 months). To prevent biasing the sample
towards newly diagnosed cases, patients assigned any KC60 code were eligible.
Consenting participants completed three questionnaires during an interview by a
3
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Wart severity was coded as ‘mild' (1-3 lesions), ‘moderate’ (4-7 lesions) or
'severe/multiple' (>7 lesions) according to the patient’s medical records, which were
completed as normal throughout the study period. The study was approved by the
South Humber Research Ethics Committee.
Case and control data were truncated at the age of thirty, due to the paucity of case
data above that age (only 14% of cases were aged 31 or over). EQ VAS scores were
analysed using generalised additive models to take into account non-linear age related
EQ VAS score effects. The difference between case and control score was adjusted
for age and interactions between age and case/control status. EQ-5D scores were
analysed with analysis of covariance with the difference between case and control
score being adjusted for age and sex. Model residuals were found to be non-normal;
therefore confidence intervals were validated using studentised bootstrap confidence
intervals. Differences amongst cases according to KC60 code, wart severity and type
of visit were tested using analysis of variance. Statistical analyses were performed
using R version 2.6.0 and SPSS version 14.0. Generalised additive models were fitted
with the mgcv library for R.19;20
RESULTS
81 cases (43 men, 38 women) were recruited with a mean age of 26 years (Table 1).
The nature of the clinic environment meant it was not practical to record all instances
of eligible patients declining an invitation to take part in the study. Whilst the exact
response rate is therefore not known, KC60 statistical returns for the clinic show that
179 diagnoses of C11A, C11B or C11C were made during the study period. There
were no significant differences in age or sex between our study population and the
4
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Table 1: Demographics and characteristics of study population with genital warts (cases)
Cases aged
All cases ≤30 years
n=81 n=70
Age
Mean 25.7 (±7.3) 23.3 (±3.8)
Gender
Male 53% (43) 54% (38)
Female 47% (38) 46% (32)
1
Participants were asked ‘Would you say your genital warts affect your quality of life?’ If ‘yes’ then they were
asked to say whether this was ‘slightly’, ‘significantly’ or ‘very significantly’.
When asked whether genital warts affected their quality of life, almost half of the
cases answered 'significantly' or 'very significantly' (Table 1). The unadjusted mean
EQ-5D index score amongst all cases was 0.90 (compared to 0.91 for controls) and 72
(compared to 86 for controls) on the EQ VAS.
For EQ VAS scores, the fitted model (and 95% confidence intervals) adjusting the
non-linear age effect is shown in Figure 1. After truncating the data at the age of
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thirty, compared to controls the EQ VAS was an average of 13.9 (95%CI, 9.9 to 17.6)
points lower among cases (p<0.001 based on 70 cases). Figure 2 shows the
distribution of case scores by age and sex. Young women in the sample exhibit lower
EQ VAS scores than men of the same age. After re-fitting the models for males and
females separately, male cases had EQ VAS scores an average of 10.9 points (95%CI,
5.7 to 15.5; p<0.001) lower than controls. Females had EQ VAS scores an average of
19.9 points (95%CI, 11.7 to 26.2; p<0.001) lower than controls. The EQ-5D index
was 0.039 points (95%CI, 0.005 to 0.078; p = 0.02) lower among cases than controls,
when adjusted for age and sex. Among cases, EQ VAS and EQ-5D scores did not
differ significantly by KC60 code, wart severity or type of visit (either first or follow-
up).
Table 2 shows responses for each dimension of the EQ-5D. Most of the detriment to
HRQoL amongst the cases can be attributed to two dimensions of the EQ-5D:
pain/discomfort and anxiety/depression. In response to the CECA10, cases indicated
the highest level of agreement with the statements: ‘I am anxious to know whether I
am going to recover from the infection for good’ (mean = 2.1, on a scale of 1 to 5,
where 1 indicates complete agreement and 5 complete disagreement), ‘I feel worried
during sexual relations’ (mean = 2.3) and ‘I worry about whether the warts will get
worse or whether there will be some complications’ (mean = 2.3). Respondents
reported the highest level of disagreement with the statement ‘Knowing that I have the
illness affects me in my daily life’ (mean = 3.4). Compared to males, female cases had
a lower mean score on every item of the CECA10. Females also had a higher,
statistically significant level of agreement on two items of the CECA10: ‘My state of
mind is upset’ (p=0.003) and ‘I avoid sexual relations’ (p=0.016) (full results
provided in the Appendix). There was a moderate positive correlation between the EQ
VAS and the CECA10 (r=0.37, p<0.01). A weaker relationship was seen between the
EQ-5D index and CECA10 scores (r=0.26, p=0.02).
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Table 2: Comparison of individual EQ-5D dimensions between the study participants with
genital warts at baseline and the UK general population reference values
Cases Controls1
n=81 n=19722
Mobility
I have no problems in walking about 94% (76) 92% (1822)
I have some problems in walking about 6% (5) 8% (147)
I am confined to bed 0% (0) 0.2% (3)
Self Care
I have no problems with self-care 98% (79) 98% (1930)
I have some problems washing or dressing myself 2% (2) 2% (40)
I am unable to wash or dress myself 0% (0) 0.1% (2)
Usual activities
I have no problems with performing my usual activities 95% (77) 91% (1799)
I have some problems with performing my usual activities 5% (4) 8% (154)
I am unable to perform my usual activities 0% (0) 1% (19)
Pain/Discomfort
I have no pain or discomfort 75% (61) 80% (1568)
I have moderate pain or discomfort 25% (20) 19% (373)
I have extreme pain or discomfort 0% (0) 2% (31)
Anxiety/Depression
I am not anxious or depressed 74% (60) 84% (1647)
I am moderately anxious or depressed 22% (18) 15% (301)
I am extremely anxious or depressed 4% (3) 1% (24)
1
1993 UK population values of the EQ-5D provided by the EuroQol executive office, based on the
UK-TTO value set.
2
5 controls had missing values for one or more of the dimensions and were therefore excluded.
DISCUSSION
We studied unselected cases of genital warts attending a GUM clinic in York, a city
of ~200,000 population. We are not aware of any attributes of these cases which make
them different to cases presenting at other centres in the UK. We observed slight
differences in the proportions of new, recurrent and persistent cases in our total
sample compared to data overall from England, but our ≤30 year old sample appeared
very similar to the national picture (York total vs. York ≤30 yrs vs. England: C11A –
49%, 54%, 56%; C11B – 33%, 31%, 31%; C11C – 17%, 14%, 13%).5
People with genital warts reported a lower HRQoL than the reference sample of the
UK population. This was especially evident for the EQ VAS score. The small number
of studies carried out to date estimate between a 5% and 30% reduction in utility
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attributed to genital warts13;14;21;22 and the EQ-5D and EQ VAS results reported here
are consistent with these estimates.
We found evidence to support the hypothesis that the detriment to HRQoL measured
on the EQ VAS and EQ-5D index can be attributed to the current diagnosis of genital
warts. Firstly, the majority of the detriment to HRQoL measured on the EQ-5D
registered in the anxiety/depression dimension. This is consistent with what is known
about the experience of genital warts, in that most of the associated morbidity is
thought to be psychological.8-12 The relationship between STI diagnosis and
psychological impact may not be straightforward, as previous studies of patients
attending sexual health clinics have shown high levels of psychological morbidity
amongst those with and without an active diagnosis.8;23 The correlation in the cases
with genital warts seen between the EQ VAS score, a generic measure, and the
CECA10, a disease-specific measure (and to a lesser extent that between the EQ-5D
index and CECA10), however, suggests that the detriment to HRQoL registered using
the EQ-5D tool was associated with genital warts.
This is the first study to use a standardised measure of HRQoL in patients with genital
warts in the UK, and to compare these results to a UK population to quantify the
extent to which genital warts affect an individual. As well as studies of sexual health
clinic patients in general, a substantial body of research exists on the psychological
impact of genital herpes in particular. While herpes is a more painful condition than
genital warts, both are viral, recurring and visible STIs. As in our study of genital
warts, genital herpes is associated with reduced HRQoL and a relatively high
incidence of anxiety and depression.8;24-26 These studies have also provided some
evidence that the psychological impact of an STI diagnosis may be greater in women
than in men.26-27 The origin of these differences is presently unclear but may be due to
factors such as concerns about sexual infectivity and reproductive health. Further
research would be required to explore these issues more fully and to address the
differential nature of perceptions of the diagnosis in males and females.
The main limitation of this study was the size of our case group. The study was only
designed to look at an overall difference between cases and controls, and as such we
were unable to investigate fully the potential impact of sex, KC60 code (including the
over-sampling of recurrent cases), wart severity or type of visit (first or follow-up) on
HRQoL outcomes.
The EQ-5D index only registered a small difference in HRQoL between cases and
controls. The EQ-5D was designed as a generic tool and may not have accurately
captured the loss of HRQoL associated with having genital warts. The five
dimensions of the tool are not as relevant to genital warts as they are to other
conditions. An alternative generic tool is the Short Form 36 (SF-36), which covers a
wider variety of domains and has been used successfully in genital herpes24;25, and
may be more appropriate for future research in this area.
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prospective study with active follow up of incident cases of genital warts would be
required to investigate this further, as well as to explore whether HRQoL changed
over the course of an episode. The recurrent nature of genital warts and the potential
for a single episode to persist for several months, or even years, means that even a
small difference in HRQoL caused by genital warts could have a considerable impact
on the loss of quality adjusted life years (QALYs).
The burden of disease from genital warts is substantial, both in terms of incidence of
infection, cost of treatment,29-30 the chronic nature of the condition and, as
demonstrated by this study, the detriment to health-related quality of life attributable
to genital warts. The potential added benefit of preventing the majority of cases of
genital warts by HPV vaccination should be considered in decisions about which HPV
vaccine to implement in the UK.
9
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Acknowledgements
We thank the clients and the staff at Monkgate Sexual Health Clinic, York, for
making the study possible, Professor Paul Kind for his advice on the use of EQ-5D,
the EuroQol executive office for the provision of the UK population norms dataset,
and Dr Xavier Badia for his permission to use, and assistance with, the CECA10.
Key messages
• Data on the effect of genital warts on health-related quality of life are needed
for economic evaluation of HPV vaccination.
• The burden of disease from genital warts is substantial, both in terms of the
detriment to health-related quality of life, incidence of infection, cost of
treatment and chronic nature of the condition.
• The potential added benefit of preventing the majority of cases of genital warts
by HPV vaccination should be considered in decisions about HPV vaccine
implementation.
Word Count
2,474
Competing Interests
None
Funding
This work was supported by funding from a Department of Health Grant: "Studies to
inform the design, implementation and monitoring of a human papillomavirus
vaccination programme in England", Grant number 039/0030. The funding body were
not involved in the design of the study, nor the analysis or write-up, and were not
involved in the decision to submit the manuscript.
Copyright
The Corresponding Author has the right to grant on behalf of all authors and
does grant on behalf of all authors, an exclusive licence (or non exclusive
for government employees) on a worldwide basis to the BMJ Publishing Group Ltd
to permit this article (if accepted) to be published in STI and any other
BMJPGL products and sub-licences such use and exploit all subsidiary rights,
as set out in our licence http://sti.bmjjournals.com/ifora/licence.pdf).
10
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Figure 1: EQ VAS scores at baseline for the study population with genital warts
compared to the UK general population
Estimated mean and 95% Confidence Intervals for EQ VAS scores for 18-30 year
olds. Derived using a general additive model, adjusted for interactions between age
and case/control status. Confidence intervals for the mean difference between cases
and controls were calculated by the bootstrap.
Figure 2: EQ VAS scores at baseline for the study population with genital warts
Distribution of case EQ VAS scores by age and sex. Young women in the sample
exhibit lower EQ VAS scores than men of the same age.
11
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References
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Male Female p2
n=43 n=383
Mean overall score (CECA10) 48.5 39.9 0.096
Mean emotional subscale (CECA6) 47.7 38.2 0.083
Mean sexual subscale (CECA4) 49.7 42.9 0.290
I worry about whether the Agree 58% (25) 68% (26) 0.322
warts will get worse or Neither agree nor disagree 19% (8) 16% (6)
whether there will be some
Disagree 23% (10) 16% (6)
complications
1
Respondents answered on a Likert scale of 1 to 5, where 1 = completely agree and 5 = completely disagree.
These scores have been recoded into 1-2 = agree, 3 = neither agree nor disagree and 4-5 = disagree, for the
purposes of this presentation and analysis.
2
P values derived from independent sample t tests for CECA10/CECA6/CECA4 and from Mantel-Haenzsel trend
test for individual items.
3
Missing value for one female for question 8, therefore n=37 for overall CECA10 score, CECA4 and question 8
(‘I feel worried during sexual relations’).
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Topic Articles on similar topics can be found in the following collections
Collections Dermatology (234)
Other viral STIs (149)
Drugs: infectious diseases (3182)
Vaccination / immunisation (185)
Notes
OBITUARY At the inception of the NHS he became one 1979–81. His wit and good humour pro-
of its first consultants. duced many fond memories. The present
William Fowler (1913–2008) In 1951 he and his family, now increased president recalls how in 1988, at the 50th
by two other sons, Donald born in 1946 and anniversary dinner, Willie and another med-
William (Willie) Fowler was born in Renfrew Ian in 1948, moved to Wolverhampton in ical man complained they could not hear the
on 4 June 1913. He was the son of James and the west Midlands. A daughter, Catherine, speaker. The MC informed them that they
Kate Fowler whose home was Calderbank, was born in 1955. couldn’t hear the speaker because of the
then a village near to Airdrie in Lanarkshire. At the Wolverhampton Royal Hospital he noise they themselves were making!
James, from being a boy soldier, now worked took up the post of consultant in venereal It was in freemasonry that Willie found
for his grandfather in the local steelworks. diseases. Within a relatively short period of expression for his natural generosity to others
Willie’s early years were during the First time, he became the consultant responsible and helping those in need. His father and
World War. While his father was fighting in for both Wolverhampton and Birmingham grandfather had both been masons, the latter
the trenches, Willie stayed for a time on a centres for the treatment of these diseases. being initiated in 1895, his father in 1950 and
relation’s farm in West Calder. His schooling (In common with many other unfashionable Willie himself in 1958. He was installed
was at Airdrie Academy, where he developed terms ‘‘venereal disease’’ is now subsumed Master of Faith and Works Lodge in 1972.
a lifelong love of literature fostered by his in genitourinary medicine!) He presented one of his own sons for
use of his grandfather’s extensive library. In Wolverhampton he developed the initiation in 1976. Willie’s oratory contained
Sportswise, he became highly proficient at Venereal Diseases Research Laboratory much wry humour, one visiting Grand Lodge
football, acquired notoriety for the ferocity which became the Reference Laboratory for Officer proclaiming that Brother Fowler’s
of his tackles, felling much larger men than Syphilis Serology in the West Midlands until delivery was superb, it was just a pity that
his own diminutive five feet two inches! the mid-nineties. the rest of them couldn’t speak Scottish!
He was awarded a Carnegie Scholarship to He remained in this post until his retirement Willie Fowler was in many ways an
study medicine at Glasgow University, in 1977. During his time the units became anomaly. Victorian in outlook and with a
graduating in 1935. From there, he spent centres of international excellence, with Willie strict self-imposed moral code he demanded
his residential year at the Glasgow Royal in much demand as an adviser to government, the best of himself and the others who worked
Infirmary, where his wicked sense of international conference delegate and as senior or lived with him. In return he gave unflinch-
humour was often allowed full sway! lecturer at Birmingham University. In recogni- ing support, advice and friendship. Friendships
He worked then at the Blackpool Victoria tion of his service to his speciality, in 1972–4 he
that in many instances lasted his lifetime.
Hospital as a registrar. It was here he met and was elected president of the Medical Society
In 1999, due to increasing frailty, Willie
soon married Connie Corris, a striking and for the Study of Venereal Diseases.
and Connie moved to Cornwall to be cared
determined redhead from the Isle of Man. She Indeed, in 1998, over 22 years after his
for by one of their sons and his wife.
was to be his wife for the next 69 years. retirement, the genitourinary medicine depart-
Willie died peacefully surrounded by his
Following a very short time together, he ment, now at New Cross in Wolverhampton,
family on 4 January 2008. He leaves his wife
was appointed a district medical officer in was named the Fowler Centre in his honour.
Connie, their four children, seven grand-
the then Rhodesia. Connie was to join him, In common with many highly intelligent children and 11 great grandchildren.
but in 1939 realising that war was imminent men, Willie had numerous other interests with He is deeply missed.
he returned to the United Kingdom to join which he was passionately concerned. In the
the Royal Army Medical Corps. 1950s he was a very keen vegetable and fruit T M Wanas
Their first son James was born in June grower, not only producing record crops, but in Correspondence to: T M Wanas, Sabrina Road,
1940 at the height of the Glasgow blitz. scientific style, developing propagation techni- Wightwick, Wolverhampton WV6 8BP, UK;
Willie served for a short time as an MO at ques years ahead of their widespread use. wanas123@btinternet.com
Rosyth Docks and Spurn Point enduring Golf was to become very important to
daily German aerial attack. him and he joined South Staffs Golf Club in
1951. He was to remain an active playing
CORRECTION
He was then posted abroad to Iraq and
India. Husband and wife were not to see member until the late 1990s. He was helped doi:10.1136/sti.2008.029512.corr1
each other for 5 years. in this by moving into a house adjoining the
During the war Connie and James spent golf course with its own private gate onto There was an error in the competing interests
time at the same Scottish farm as Willie had one of the tees! section of an article published in the June
done during the First World War. Willie and Connie were both excellent issue of the journal (Woodhall S, Ramsey T,
Serving in India he was involved with ballroom dancers; on many occasions their Cai C, et al. Estimation of the impact of
treating skin diseases, eventually heading his foxtrot clearing the dance floor as others genital warts on health-related quality of life.
own unit with the rank of Major. looked on. In addition, his Scottish roots Sex Transm Infect 2008;84:161–6). The state-
On his return home in 1945 he was were maintained by their membership of the ment should read: ‘‘CJNL has in the past acted
appointed an honorary consultant at the Wolverhampton Caledonian Society, which as a consultant for Merck, Sanofi Pasteur
Leeds General Infirmary and York Hospital. they joined in 1958. He became president in MSD, GSK, 3M Pharmaceuticals and Stiefel.’’