Journal of Obstetrics and Gynaecology

ISSN: 0144-3615 (Print) 1364-6893 (Online) Journal homepage: http://www.tandfonline.com/loi/ijog20

Hyperemesis gravidarum and its relation with

maternal body fat composition
Aydin Kosus, Ayla Eser, Nermin Kosus, Betul Usluogullari & Deniz Hizli
To cite this article: Aydin Kosus, Ayla Eser, Nermin Kosus, Betul Usluogullari & Deniz Hizli
(2016): Hyperemesis gravidarum and its relation with maternal body fat composition, Journal
of Obstetrics and Gynaecology, DOI: 10.3109/01443615.2016.1157153
To link to this article: http://dx.doi.org/10.3109/01443615.2016.1157153

Published online: 12 Apr 2016.

Submit your article to this journal

Article views: 15

View related articles

View Crossmark data

Full Terms & Conditions of access and use can be found at

http://www.tandfonline.com/action/journalInformation?journalCode=ijog20
Download by: [Laurentian University]

Date: 20 April 2016, At: 21:33

Journal of Obstetrics and Gynaecology, 2016; Early Online: 15

2016 Informa UK Limited, trading as Taylor & Francis Group
ISSN 0144-3615 print/ISSN 1364-6893 online
DOI: 10.3109/01443615.2016.1157153

ORIGINAL ARTICLE

Hyperemesis gravidarum and its relation with maternal body fat

composition
Aydin Kosus1, Ayla Eser1, Nermin Kosus1, Betul Usluogullari2 & Deniz Hizli1
Department of Obstetrics and Gynecology, Turgut Ozal University Hospital, Ankara, Turkey, 2Department of Obstetrics and Gynecology,
Cengiz Gokcek State Hospital, Gaziantep, Turkey

Downloaded by [Laurentian University] at 21:33 20 April 2016

The objective of this study was to determine if maternal body fat

composition and body mass index were associated with
hyperemesis gravidarum (HG) in the first trimester of pregnancy.
Healthy pregnant women (n 30) without nausea and vomiting
(control group) and women with HG (n 54; study group), all
with singleton pregnancy at 614 weeks gestational age, were
included. Body mass index was measured before and during
pregnancy. Visceral adipose tissue (VAT) and subcutaneous fat
thickness were measured during pregnancy. Comparison of the
groups revealed that VAT and pre-pregnancy body mass index
but not subcutaneous fat thickness were significantly higher in
the HG group versus controls. VAT and pre-pregnancy body mass
index predicted 83.8% and 67.1% of HG cases, respectively. VAT
and pre-pregnancy body mass index were correlated with the
development of hyperemesis gravidrum and hence could be
considered as predictive markers for HG.
Keywords: Hyperemesis gravidarum, body mass index, visceral
adipose tissue, subcutaneous fat thickness

Introduction
Nausea and vomiting affect up 7085% of women during
pregnancy (Wegrzyniak et al. 2012) and as such are usually
considered to be normal physiological responses to pregnancyassociated hormonal changes. These symptoms typically first
occur between 6 and 8 weeks gestation and resolve by 16
18 weeks (Wegrzyniak et al. 2012). However, a sub-group of
women experience nausea and vomiting symptoms throughout
their pregnancy and between 0.5% and 2% of pregnant women
experience hyperemesis gravidarum (HG) (Wegrzyniak et al.
2012), also known as persistent nausea and vomiting of
pregnancy (NVP). Symptoms of HG, described as unexplained
excessive nausea and vomiting during pregnancy, include severe
vomiting, muscle wasting, ketonuria, nutritional deficiency,
severe dehydration, electrolyte imbalance and either low weight
gain or weight loss (Verberg et al. 2005; Roseboom et al. 2011;
Veenendaal et al. 2011; Wegrzyniak et al. 2012). About 15%
women with HG require hospitalisation. While many etiopathogenic factors have been considered for HG, including endocrinehormonal factors, no specific causative factor has yet been
established (Aka et al. 2006).

The regulation of body weight is under homeostatic control.

There is a communication between the body adipose tissue and
appetite centres of the central nervous system. This adipocyte
brain axis is important for appetite regulation (Sahu 2003;
Stanley et al. 2005). For example, adipose tissue releases
adipocytokines such as leptin, which cross the bloodbrain
barrier and activate signalling pathways which are important in
regulation of energy homeostasis and appetite (Wada et al. 2014).
It is now well accepted that distribution of fat, rather than fat
mass per se, is key to the metabolic disease complications
associated with obesity (Walker et al. 2014). Visceral adipose
tissue (VAT) is more active metabolically and is an independent
risk factor for development of obesity-associated comorbidities
such as cardiovascular disease and metabolic syndrome. The
metabolic impact of VAT compared to subcutaneous and ectopic
adipose tissue lies in the differences in storage and release of fatty
acids and synthesis and secretion of adipocytokines that regulate
insulin sensitivity and appetite (Fontana et al. 2007; CeperueloMallafre et al. 2009; Tishinsky et al. 2014; Walker et al. 2014).
There are some indications in the literature that being either
underweight or obese pre-pregnancy, as assessed by body mass
index (BMI), can contribute to development of HG (Vikanes
et al. 2013). However, while BMI is a useful measure of total
obesity and overweight or underweight, it can only be taken as a
measure of relative weight status and does not provide information regarding body fat distribution or adiposity.
Measurement of visceral or peripheral fat by ultrasound is an
easy, non-invasive method and avoids ionising radiation. Also,
ultrasound measurement of visceral adiposity is closely correlated with computed tomography derived measurements, showing high reliability of the method (Suzuki et al. 1993). In this
study, we measured VAT and subcutaneous fat tissue (SCFT) as
well as BMI in first trimester healthy pregnant women and in
women with HG and compared results of the two groups to
determine if there is any association of HG with maternal body
fat composition.

Materials and methods

This study was carried out in Turgut Ozal University Faculty of
Medicine, Obstetrics and Gynecology Department, between
November 2011 and November 2012. Pregnant volunteers in
their first trimester with HG (n 54) were taken as the study
group. Healthy pregnant volunteers (n 30) at the same
gestational age but without nausea and vomiting were taken as

Correspondence: Ayla Eser, Department of Obstetrics and Gynecology, Turgut Ozal University Hospital, Hosdere Cad. No: 145-147, Y. Ayranci, Ankara,
Turkey. E-mail: aylaacar76@yahoo.com.tr.

Downloaded by [Laurentian University] at 21:33 20 April 2016

A. Kosus et al.

the control group. Inclusion criteria were: singleton pregnancy

with a live embryo, gestational age 614 weeks, healthy women
without any medical disorders. The exclusion criteria were:
smokers or drug users (other than prenatal vitamin supplements)
in the index pregnancy, women with a previous history of
diabetes or any other systemic disease. Written and informed
consent was obtained from all women. Approval for this study
was obtained from the Local Institutional Review Board of the
Faculty of Medicine, Turgut Ozal University.
Hyperemesis was defined as persistent nausea and vomiting
associated with ketonuria and weight loss 45% of pre-pregnancy
weight. All relevant data including demographic information
(age, gravida, parity, BMI before and during pregnancy, obstetrical history and gestational week) were collected and recorded
for further analysis (Table 1). BMI was calculated as weight (kg)/
height (m2). All measurements were obtained in the morning,
after overnight fasting.
Fasting venous blood samples were taken from all subjects for
measurement of serum thyroid-stimulating hormone, free T3,
free T4, human chorionic gonadotrophin, blood urea, creatinine,
sodium, potassium, glucose, aspartate aminotransferase, alanine
transaminase and complete blood count to detect the severity of
emesis. Also, presence of ketonuria was controlled in the
morning urine sample by urine stripes.
All women underwent an ultrasound examination, which was
performed by the same operator. The study was performed by
using an Aloka Prosound SSD-3500SX (Aloka Holding Europe
AG, Switzerland) ultrasound machine with 3.5 MHz transabdominal and 6.5 MHz transvaginal probe. The gestational age
was calculated by modified Naegeles rule. Last menstrual periodderived gestational age was compared with ultrasound-derived
gestational age using CRL (Hadlock et al. 1992). The technique of
Armellini et al. (1990) was used to measure SCFT and VAT.
Subcutaneous fat depth was measured from the subcutaneous fat
layer to the outer border of the rectus abdominus muscle at the
level of the linea alba. Visceral fat depth was measured from the
inner border of the rectus abdominus muscle at the level of the
linea alba to the anterior wall of the abdominal aorta.
Application of excessive pressure over the abdominal wall was
avoided during the measurements.
A power analysis was conducted using an a level of 0.05, b
level of 0.20, a power of 80% and effect size of 0.30; a minimum
total sample size of 82 was needed. The Statistical Package
Program for the Social Sciences (SPSS 16.0; SPSS Inc., Chicago,
IL) was used for statistical analysis. Conformity of the measured
values to normal distribution was examined graphically and
using ShapiroWilks test. Test results failed to detect a normal
distribution pattern for the groups. Thus numbers and percentages were used for categorical variables, and median
(Interquartile range, IQR) values were used for the continuous
Table 1. Demographic and ultrasonographic parameters according to the
groups.

Age (years)
Gravida (n)
Parity (n)
Gest age (weeks)
Prepreg BMI (kg/m2)
Preg BMI (kg/m2)
SCFT (mm)
VAT (mm)

Control
(n 30)

Hyperemesis
(n 54)

30 (2437)
2 (14)
1 (02)
8 (612)
21.7 (18.230.5)
22.9 (22.134.0)
14.5 (726)
30 (1452)

27 (2139)
2 (16)
0.5 (04)
9 (613)
24.4 (18.739.9)
22.9 (16.238.1)
16 (626)
34 (1568)

p50.05 significant.
Statistically significant p values are given bold.

p Value
0.062
0.454
0.648
0.342
0.012
0.949
0.197
0.023

data. For groups that were not distributed normally, Mann

Whitney test was used for comparison. Chi-squared test was
used for comparison of categorical data. Logistic regression
analysis was performed to investigate confounding effects of
different parameters for prediction of HG. ROC analysis was
done to find the best cutoff point of BMI, VAT and SCFT for
determination of HG. p50.05 was considered to be statistically
significant.

Results
A total of 95 women were enrolled into the study. Nine patients
were excluded because all blood tests were not completed; two
further patients were excluded because they gave up the study
and did not accept ultrasound measurement of VAT and SCFT.
Demographic data of the remaining 84 cases are presented in
Table 1. There were no significant differences between the groups
with respect to age, gestational age, gravida and parity (Table 1).
Comparison of the groups revealed, however, that both prepregnancy BMI and the VAT were significantly higher in the HG
group compared to the control group (p50.05; Table 1). SCFT
was also higher in the HG group, but this difference was not
significant (Table 1).
After primary comparison of the groups, all volunteers were
divided into two groups according to values above or below the
overall median values of VAT of 33 mm and SCFT of 16 mm.
Evaluation of women according to the distribution of VAT was
revealed that 76.3% of cases with VAT 33 mm were in the HG
group, while only 23.7% of women with VAT  33 mm were in
the control group (p 0.042; Table 2). For cases with
SCFT 16 mm, 68.2% were in the HG group and 31.8% in the
control group, but this was not statistically significant (Table 3).
Logistic regression analysis was performed for determination
of factors important in prediction of HG development (Table 4).
Regression analysis with only VAT and SCFT values revealed
that VAT value was significantly important in prediction of HG
Table 2. Distribution of cases according to median VAT value.

Control
Count
% Group
% VAT
% of Total
Hyperemesis
Count
% Group
% VAT
% of Total

533 mm

33 mm

p Value

21
70.0
45.7
25.0

9
30.0
23.7
10.7

0.042

25
46.3
54.3
29.8

29
53.7
76.3
34.5

p50.05.
Statistically significant p values are given bold.

Table 3. Distribution of cases according to median SCFT value.

Control
Count
% Group
% SCFT
% Total
Hyperemesis
Count
% Group
% SCFT
% Total
p50.05 significant.

516 mm

16 mm

p Value

16
53.3
40.0
19.0

14
46.7
31.8
16.7

0.498

24
44.4
60.0
28.6

30
55.6
68.2
35.7

Hyperemesis gravidarum and its relation with maternal body fat composition
Table 4. The results of logistic regression analysis including values of SCFT
and VAT.

SCFT
VAT

SE

0.036
0.021

0.047
0.007

p value

Exp(B)

0.442
0.002

0.964
1.021

p50.05 significant.
Statistically significant p values are given bold.

Table 5. The results of logistic regression analysis including SCFT, VAT and
BMI.

SCFT
VAT
Prepreg BMI
Preg BMI

SE

0.038
0.078
0.753
0.712

0.108
0.060
0.261
0.269

p value

Exp(B)

0.725
0.189
0.004
0.008

1.039
1.081
2.124
0.491

Downloaded by [Laurentian University] at 21:33 20 April 2016

p50.05 significant.
Statistically significant p values are given bold.

while SCFT value was not effective (Table 4). Logistic regression
analysis with VAT, SCFT and BMI showed that pre-pregnancy
BMI was important in HG development (p 0.004) (Table 5).
HG development was also affected negatively by BMI during
pregnancy. As pregnancy BMI increased, HG development
decreased significantly (p 0.008) (Table 5). ROC analysis
showed that use of pre-pregnancy BMI alone predicted 67.1%
of HG cases (AUC 0.671, p 0.014) while use of VAT alone
predicted 83.8% of them [AUC 0.638, p 0.032) (Table 6;
Figure 1)]. SCFT and BMI during pregnancy had very low
sensitivity and specificity, so they were not effective in prediction
of HG (AUC 0.573, p 0.255 and AUC 0.536, p 0.601,
respectively) (Table 6). Sensitivity and specificity values of
different cut off levels are shown in Table 6 and Figure 1.

Discussion
In this study, a group of pregnant women with HG were
compared with a control group that was matched for age,
gravidity, parity, gestational weeks and first trimester BMI to
determine differences in terms of body fat composition and
evaluate the predictive role of VAT, SCFT and BMI for the
development of HG.
In this study, we found that median VAT thickness was
significantly higher in the HG group than in the control group.
Similarly, the proportion of women having VAT higher than the
median value was significantly higher in the HG group as
compared to the control group. By contrast, no significant
difference was observed between groups in terms of SCFT
thickness. In this study we also found that VAT and prepregnancy BMI were important for prediction of HG, while
SCFT and BMI during pregnancy had very low sensitivity and
specificity, so were not considered effective in prediction.
Previous studies have shown that VAT is superior to SCFT as a
marker of adiposity and it is more closely related with the
metabolic consequences of obesity (Fox et al. 2007; Liu et al. 2010).
One explanation of this could be that VAT is associated more
strongly with the secretion of adipocytokines like leptin and
adiponectin, which are important determinants of energy metabolism and play a crucial role in modifying appetite, insulin
resistance, obesity, metabolic syndrome and diabetes (Fox et al.
2007; Liu et al. 2014; Wada et al. 2014). These modifying effects
may be relevant in HG development during pregnancy. In support
of this, it has been suggested in two recent reports that the
adipocytokines leptin and nesfatin might be involved in the

Table 6. The sensitivity and specificity values for different cut off values of
VAT, SCFT and BMI for prediction of hyperemesis gravidarum.
Asymptotic 95% CI
AUC
VAT
SCFT
Prepreg BMI
Preg BMI

0.638
0.573
0.671
0.536

SE
0.061
0.063
0.067
0.066

p value
0.032
0.255
0.014
0.601

Upper bound Lower bound

0.520
0.450
0.540
0.408

0.757
0.697
0.802
0.665

Cut off Sensitivity Specificity

VAT

SCFT

PreprBMI

Preg BMI

14.50
19.50
21.50
23.50
25.50
27.50
29.50
30.50
7.50
9.50
10.50
11.50
12.50
13.50
14.50
15.50
18.70
19.66
20.35
20.81
21.75
22.82
23.47
24.15
16.88
18.94
19.53
20.66
21.24
21.62
22.27
22.73

1.000
0.984
0.952
0.905
0.810
0.762
0.714
0.556
0.984
0.952
0.889
0.794
0.683
0.635
0.571
0.540
0.984
0.952
0.889
0.841
0.794
0.683
0.587
0.524
0.984
0.921
0.889
0.794
0.714
0.683
0.571
0.508

0.067
0.100
0.167
0.233
0.300
0.400
0.467
0.533
0.033
0.1
0.233
0.233
0.4
0.467
0.5
0.533
0.042
0.208
0.208
0.250
0.542
0.667
0.667
0.750
0.042
0.042
0.083
0.167
0.250
0.333
0.458
0.542

Statistically significant p values are given bold.

pathophysiology of HG (Albayrak et al. 2013; Gungor et al. 2013).

In another study, adjusted leptin levels have been suggested as a
good marker for prediction of HG (Demir et al. 2006), while leptin
levels have also been significantly associated with the development
of HG in pregnant women (Aka et al. 2006).
Results of our study suggest that pre-pregnancy BMI is
important for prediction of HG. There are few studies in the
literature on this subject and a lack of consensus. One study
suggested that HG is associated with symptoms of depression
and anxiety rather than pre-pregnancy BMI or any factors
associated with eating attitudes and body image (Annagur et al.
2014). Results of another study suggested that early pregnancy
BMI was negatively correlated with glycaemic control but not
development of HG (Suzuki & Takeuchi 2005). Low maternal
BMI, however, has been implicated in HG development in
several studies. Inadequate weight gain in the first trimester, as
assessed by comparison of pre-pregnancy BMI and BMI during
first trimester, has been significantly associated with HG
(Ogunyemi et al. 1998). Meanwhile, low maternal weight as
defined by pre-pregnancy BMI 520 kg/m2 was also associated
with increased risk in a large Swedish study, as compared to ideal
weight, overweight or obese women (Cedergren et al. 2008).
Results of another study implicated both underweight and obese
pre-pregnancy BMI in significantly increased risk of developing
HG, independent of confounding factors (Vikanes et al. 2013).

Downloaded by [Laurentian University] at 21:33 20 April 2016

A. Kosus et al.

Figure 1. Sensitivity and specificity values for different cut off levels of VAT, SCFT, pre-pregnancy and pregnancy BMI.

This is consistent with the observations in our study showing

that higher pre-pregnancy BMI was significantly associated with
HG. BMI during pregnancy, on the other hand, had minimal
effect in HG prediction.
Many etiopathogenic factors have been considered for HG.
However, no specific causative factor has yet been established
(Aka et al. 2006). Risk factors that have been recently suggested
include inflammatory conditions such as infection with
Helicobacter pylori, which was identified as a potential risk
factor in a recent study of 175 pregnant women (Kazemzadeh
et al. 2014), although others suggest that Helicobacter pylori
may not be strongly predictive of HG (Vikanes et al. 2013).
Other recent studies have implicated hormonal factors. For
example, in one study on 32 women hospitalised for HG
compared to 29 control women, high androgen and low
androstenedione levels were associated with HG. (Helseth et al.
2014) Meanwhile, other recent studies on HG subjects
compared to women with normal pregnancies suggested
increased levels of ghrelin, a hormone that increases food
intake through central mechanisms; the observed increased
levels in HG may be a part of an attempted compensatory
mechanism (Albayrak et al. 2013; Oru et al. 2013). The
association of potential inflammatory and hormonal mechanisms, including those associated with ghrelin and with the
adipocytokines, is consistent with our observation of correlation
of adiposity, as indicated by VAT, with HG. VAT in our study
has comparable or superior predictive value to, e.g. levels of
ghrelin, androgen or androstenedione hormones (Albayrak
et al. 2013; Oru et al. 2013; Helseth et al. 2014).

There are some limitations of this study. Although the sample

size was calculated by power analysis as sufficient for this study,
larger studies allowing patient groups to be separated on the
basis of meaningful subgroups of underweight, normal, overweight and obese are needed. Also, pre-pregnancy VAT and
SCFT measurements were not available, nor were adipose tissue
specific hormones or adipocytokine levels measured. These are
indicated for future studies.
In conclusion HG is a complex, multifactorial condition with
many potential etiological factors (Verberg et al. 2005; Roseboom
et al. 2011; Tamay & Kuu 2011; Veenendaal et al. 2011;
Wegrzyniak et al. 2012). More recently, the emphasis has been
laid on the pathogenic role of adipocytokines that are secreted
mainly by the metabolically more active visceral fat (Aka et al.
2006; Fox et al. 2007; Albayrak et al. 2013; Gungor et al. 2013;
Vikanes et al. 2013; Liu et al. 2014). The current study has added
into the existing pool of information that maternal visceral fat
thickness during the first trimester is a strong predictor of HG.
VAT or hormones and cytokines secreted from it might be
important in energy balance and eating disorders during
pregnancy. This information could be used for development of
new strategies in prediction and treatment of HG. Reliability and
reproducibility of the study can be readily further examined to
test its clinical utility, since it is an easily measurable parameter
during early pregnancy ultrasound scanning. Secondly, this study
suggests that pre-pregnancy BMI is also a significant predictor
of HG, though its sensitivity is lower than for VAT.
Recommendations about weight control should be given to
women with high or low BMI before becoming pregnant. This

Hyperemesis gravidarum and its relation with maternal body fat composition
might also decrease complications related to eating disorders and
help prevention of some more serious late complications which
are indirectly related to eating habits, such as gestational
hypertension, intrauterine growth disorders, diabetes and premature or post-term delivery.
Declaration of interest: The authors declare no conflict of
interest. Our study is presented as a poster presentation at
Turkey Maternal Fetal Medicine and Perinatology Society IX.
National Congress that was held in Istanbul Harbiye Military
Museum between 24 and 27 September 2014.

Downloaded by [Laurentian University] at 21:33 20 April 2016

References
Aka N, Atalay S, Sayharman S, Kilic D, Kose G, Kucukozkan T. 2006. Leptin
and leptin receptor levels in pregnant women with hyperemesis
gravidarum. The Australian & New Zealand Journal of Obstetrics &
Gynaecology 46:274277.
Albayrak M, Karatas A, Demiraran Y, Erman H, Topuz S, Biyik I, et al.
2013. Ghrelin, acylated ghrelin, leptin and PYY-3 levels in hyperemesis
gravidarum. Journal of Maternal-Fetal and Neonatal Medicine 26:
866870.
Annagur BB, Kerimoglu OS, Gunduz S, Tazegul A. 2014. Are there any
differences in psychiatric symptoms and eating attitudes between
pregnant women with hyperemesis gravidarum and healthy pregnant women? Journal of Obstetrics and Gynaecology Research
40:10091014.
Armellini F, Zamboni M, Rigo L, Todesco T, Bergamo-Andreis IA, Procacci
C, et al. 1990. The contribution of sonography to the measurement of
intra-abdominal fat. Journal of Clinical Ultrasound 18:563567.
Cedergren M, Brynhildsen J, Josefsson A, Sydsjo A, Sydsjo G. 2008.
Hyperemesis gravidarum that requires hospitalization and the use of
antiemetic drugs in relation to maternal body composition. American
Journal of Obstetrics and Gynecology 198:412.e1412.e5.
Ceperuelo-Mallafre V, Naf S, Escote X, Caubet E, Gomez JM, Miranda M,
et al. 2009. Circulating and adipose tissue gene expression of zinc-alpha2glycoprotein in obesity: its relationship with adipokine and lipolytic gene
markers in subcutaneous and visceral fat. The Journal of Clinical
Endocrinology and Metabolism 94:50625069.
Demir B, Erel CT, Haberal A, Ozturk N, Guler D, Kocak M. 2006. Adjusted
leptin level (ALL) is a predictor for hyperemesis gravidarum. European
Journal of Obstetrics & Gynecology and Reproductive Biology
124:193196.
Fontana L, Eagon JC, Trujillo ME, Scherer PE, Klein S. 2007. Visceral fat
adipokine secretion is associated with systemic inflammation in obese
humans. Diabetes 56:10101013.
Fox CS, Massaro JM, Hoffmann U, Pou KM, Maurovich-Horvat P, Liu C-Y,
et al. 2007. Abdominal visceral and subcutaneous adipose tissue
compartments: association with metabolic risk factors in the
Framingham Heart Study. Circulation 116:3948.
Gungor S, Gurates B, Aydin S, Sahin I, Kavak SB, Kumru S, et al. 2013.
Ghrelins, obestatin, nesfatin-1 and leptin levels in pregnant women with
and without hyperemesis gravidarum. Clinical Biochemistry 46:828830.
Hadlock FP, Shah YP, Kanon DJ, Lindsey JV. 1992. Fetal crown-rump
length: reevaluation of relation to menstrual age (5-18 weeks) with highresolution real-time US. Radiology 182:501505.

Helseth R, Ravlo M, Carlsen SM, Vanky EE. 2014. Androgens and

hyperemesis gravidarum: a case-control study. European Journal of
Obstetrics, Gynecology, and Reproductive Biology 175:167171.
Kazemzadeh M, Kashanian M, Baha B, Sheikhansari N. 2014. Evaluation of
the relationship between Helicobacter Pylori infection and hyperemesis
gravidarum. Medical Journal of the Islamic Republic of Iran 28:72.
Liu J, Fox CS, Hickson DA, May WD, Hairston KG, Carr JJ, et al. 2010.
Impact of abdominal visceral and subcutaneous adipose tissue on
cardiometabolic risk factors: the Jackson Heart Study. The Journal of
Clinical Endocrinology and Metabolism 95:54195426.
Liu J, Coady S, Carr JJ, Hoffmann U, Taylor HA, Fox CS. 2014. Differential
associations of abdominal visceral, subcutaneous adipose tissue with
cardiometabolic risk factors between African and European Americans.
Obesity 22:811818.
Ogunyemi D, Hullett S, Leeper J, Risk A. 1998. Prepregnancy body mass
index, weight gain during pregnancy, and perinatal outcome in a rural
black population. Journal of Maternal-Fetal and Neonatal Medicine 7:
190193.
Oru AS, Mert I, Akturk M, Aslan E, Polat B, Buyukkagnici U, et al. 2013.
Ghrelin and motilin levels in hyperemesis gravidarum. Archives of
Gynecology and Obstetrics 287:10871092.
Roseboom TJ, Ravelli AC, van der Post JA, Painter RC. 2011. Maternal
characteristics largely explain poor pregnancy outcome after hyperemesis
gravidarum. European Journal of Obstetrics & Gynecology and
Reproductive Biology 156:5659.
Sahu A. 2003. Leptin signaling in the hypothalamus: emphasis on energy
homeostasis and leptin resistance. Frontiers in Neuroendocrinology
24:225253.
Stanley S, Wynne K, McGowan B, Bloom S. 2005. Hormonal regulation of
food intake. Physiological Reviews 85:11311158.
Suzuki R, Watanabe S, Hirai Y, Akiyama K, Nishide T, Matsushima Y, et al.
1993. Abdominal wall fat index, estimated by ultrasonography, for
assessment of the ratio of visceral fat to subcutaneous fat in the abdomen.
The American Journal of Medicine 95:309314.
Suzuki S, Takeuchi T. 2005. HbA1C levels in Japanese women during early
pregnancy. Archives of Gynecology and Obstetrics 273:174175.
Tamay AG, Kuu NK. 2011. Hyperemesis gravidarum: current aspect.
Journal of Obstetrics and Gynaecology 31:708712.
Tishinsky JM, De Boer AA, Dyck DJ, Robinson LE. 2014. Modulation of
visceral fat adipokine secretion by dietary fatty acids and ensuing changes
in skeletal muscle inflammation. Applied Physiology, Nutrition, and
Metabolism 39:2837.
Veenendaal MV, van Abeelen AF, Painter RC, van der Post JA, Roseboom
TJ. 2011. Consequences of hyperemesis gravidarum for offspring: a
systematic review and meta-analysis. Bjog 118:13021313.
Verberg MF, Gillott DJ, Al-Fardan N, Grudzinskas JG. 2005. Hyperemesis
gravidarum, a literature review. Human Reproduction Update 11:527539.
Vikanes AV, Stoer NC, Gunnes N, Grjibovski AM, Samuelsen SO,
Magnus P, et al. 2013. Helicobacter pylori infection and severe
hyperemesis gravidarum among immigrant women in Norway: a casecontrol study. European Journal of Obstetrics & Gynecology and
Reproductive Biology 167:4146.
Wada N, Hirako S, Takenoya F, Kageyama H, Okabe M, Shioda S. 2014.
Leptin and its receptors. Journal of Chemical Neuroanatomy
61-62:191199.
Walker GE, Marzullo P, Ricotti R, Bona G, Prodam F. 2014. The
pathophysiology of abdominal adipose tissue depots in health and
disease. Hormone Molecular Biology and Clinical Investigation 19:5774.
Wegrzyniak LJ, Repke JT, Ural SH. 2012. Treatment of hyperemesis
gravidarum. Rev Obstet Gynecol 5:7884.