You are on page 1of 12

Series

Maternal obesity 1
Preconceptional and maternal obesity: epidemiology and
health consequences
Lucilla Poston, Rishi Caleyachetty, Sven Cnattingius, Camila Corvalán, Ricardo Uauy, Sharron Herring, Matthew W Gillman

Obesity in women of reproductive age is increasing in prevelance worldwide. Obesity reduces fertility and increases Lancet DIabetes-Endocrinol 2016
time taken to conceive, and obesity-related comorbidities (such as type 2 diabetes and chronic hypertension) heighten Published Online
the risk of adverse outcomes for mother and child if the woman becomes pregnant. Pregnant women who are obese October 12, 2016
http://dx.doi.org/10.1016/
are more likely to have early pregnancy loss, and have increased risk of congenital fetal malformations, delivery of
S2213-8587(16)30217-0
large for gestational age infants, shoulder dystocia, spontaneous and medically indicated premature birth, and
See Online/Series
stillbirth. Late pregnancy complications include gestational diabetes and pre-eclampsia, both of which are associated http://dx.doi.org/10.1016/
with long-term morbidities post partum. Women with obesity can also experience difficulties during labour and S2213-8587(16)30278-9,
delivery, and are more at risk of post-partum haemorrhage. Long-term health risks are associated with weight retention http://dx.doi.org/10.1016/
S2213-8587(16)30107-3, and
after delivery, and inherent complications for the next pregnancy. The wellbeing of the next generation is also
http://dx.doi.org/10.1016/
compromised. All these health issues could be avoided by prevention of obesity among women of reproductive age, S2213-8587(16)30108-5
which should be viewed as a global public health priority. For women who are already obese, renewed efforts should be See Online/Comment
made towards improved management during pregnancy, especially of blood glucose, and increased attention to post- http://dx.doi.org/10.1016/
partum weight management. Effective interventions, tailored to ethnicity and culture, are needed at each of these S2213-8587(16)30098-5
stages to improve the health of women and their children in the context of the global obesity epidemic. This is the first in a Series of four
papers about maternal obesity

Introduction US National Health and Nutrition Examination Survey Division of Women’s Health,
Faculty of Life Sciences and
Obesity in women who enter pregnancy predicts short- (NHANES) of women aged 20–39 years yielded an
Medicine, King’s College
term and long-term adverse health outcomes for both the estimated prevalence of obesity of 31·8%.6 About half of London, London, UK
mother and her child, because maternal obesity can these women were in the lowest category of obesity (Prof L Poston PhD); Institute of
propagate intergenerational cycles of increasing obesity (class I; BMI 30–34·9 kg/m²), but a quarter were in Applied Health Research,
University of Birmingham,
and diabetes.1 Interruption of these cycles before, during, class II (35–39·9 kg/m²) and another quarter were in the Birmingham, UK
or after pregnancy might help to stem the rising tide of highest category (class III; >40 kg/m²).6 The prevalence of (R Caleyachetty PhD);
non-communicable diseases worldwide.2 Thus, under- obesity was substantially increased in non-white ethnic Department of Medicine Solna,
standing of the burden of maternal obesity and how it is groups, especially non-Hispanic black women (55·8%, Karolinska
Universitetssjukhuset,
changing over time is important in both high-income figure 1).6 The high prevalence of maternal obesity in the Stockholm, Sweden
and lower-income countries. USA reflects trends that began more than three decades (S Cnattingius MD); Institute of
In this Review, we describe the trends in the global ago: in the 1970s, the proportion of women aged Nutrition and Food
prevalence of obesity among women, especially those in 20–39 years with BMI more than 30 kg/m² was less than Technology, University of Chile,
Santiago, Chile
countries least able to accommodate the associated 10%, but by around 1990, the proportion had risen to (C Corvalán PhD); Division of
health-care costs. We have considered the influence of about 15% and by the mid-2000s it was more than 25%.7 Pediatrics, Faculty of Medicine,
obesity on reproductive health before and at the time of Prevalence of obesity among women of reproductive Pontifical Catholic University
conception, its influence on fertility, pregnancy loss and age varies in other high income countries. In England in of Chile, Santiago, Chile
(R Uauy PhD); Center for
the increasing risk of complications in late pregnancy 2013, 26% of 35–44-year-olds and 18% of women aged Obesity Research and
and at delivery. The impact on the health of the fetus and 25–34 years were classified as obese.8 Estimations of Education, Departments of
newborn baby is reviewed, and we also highlight the obesity among pregnant women or women older Medicine and Public Health,
heightened risk for longer-term maternal morbidity. than 20 years in 23 EU countries (from the European Temple University,
Philadelphia, PA, USA (R Uauy,
Peristat Database and WHO data) suggest that UK S Herring MD); and Office of the
Global trends in maternal obesity women have the highest prevalence of obesity in Europe Director, Environmental
High-income countries (25·2%) and those from Poland the lowest (7·1%; Influences on Child Health
Outcomes (ECHO), National
The obesity epidemic has ensnared all global sub- figure 2).9 The rise in obesity among European countries
Institutes of Health, Rockville,
populations. Current estimates suggest that by 2025 more has been rapid; to provide an example, in 1994–95, 6·4% MD, USA (M W Gillman MD)
than 21% of women in the world will be obese.3 In the of 30–44 year old women from Tromso in Norway were Correspondence to:
USA, and in other countries including the UK, no obese (BMI ≥ 30kg/m²), whereas in 2007–08, 16·4% of Prof Lucilla Poston, KCL Division
population-wide surveillance data directly estimate BMI such women were obese.10 In Australia in 2011–12, the of Women’s Health, St Thomas’
and thus obesity (BMI ≥30 kg/m²) just before pregnancy. prevalence of obesity among 35–44-year-olds was similar Hospital, London SE1 7EH, UK
lucilla.poston@kcl.ac.uk
In the absence of nationally representative data for pre- to the USA and the UK (approximately 27%), but was
pregnancy BMI, surveillance of women of reproductive lower in women aged 25–34 years at closer to 20%.11 In
age offers insights.4,5 In 2011–12, analyses of data from the east Asia, for example in South Korea, the proportion of

www.thelancet.com/diabetes-endocrinology Published online October 12, 2016 http://dx.doi.org/10.1016/S2213-8587(16)30217-0 1


Series

100 Overall
retention and childhood adiposity.13,14 A more common
Non-Hispanic white alternative is to ask women to self-report pre-pregnancy
90
Non-Hispanic black height and bodyweight. This approach can systematically
80 Hispanic
overestimate height and underestimate bodyweight,
70 although ranking of BMI across individuals is highly
Prevalence (%)

60 preserved and associations with health outcomes are not


50 substantially biased when this measure is used.15,16
40 In the USA, although data for self-reported pre-
pregnancy height and weight are not available nationally,
30
these data were available for more than 1 million
20
low-income women per year who participated in the
10 Pregnancy Nutrition Surveillance System (PNSS) until
0 2012. In the PNSS, the prevalence of pre-pregnancy obesity
1971–74 1976–80 1988–94 1999–2000 2003–04 2011–12
rose from 34·6% in 1988 to 53·7% in 2011.17 That these
Year
rates are similar to black women of reproductive age in the
Figure 1: Estimated prevalence of maternal obesity in the USA USA as a whole (2011–12; 56%)6 probably reflects wide
Percentage of women aged 20–39 years in the USA with BMI of more than disparities in socioeconomic position as well as causal
30 kg/m², overall and according to ethnic background. Data are from US
National Health and Nutrition Examination Surveys.3–5 Hispanic data are for associations related to ethnic backgrounds. Among these
Mexican–American women in 1999–2000 and 2003–04, and for Hispanic people low-income women, rates of excessive gestational weight
in 2011–12. gain also increased—from 37·4% in 1988 to 48·0% in
2011—while the prevalence of inadequate weight gain fell
from 33·0% in 1988 to 21·0% in 2011.17 These changes are
UK*
Ireland* partly attributable to increases in obesity, because regional
Spain* data indicate that a higher proportion of women with
Hungary*
Portugal*
obesity gain weight excessively compared with women
Scotland, UK who enter pregnancy at a normal bodyweight.18
Austria*
Netherlands*
Greece* Low-income and middle-income countries
Italy* Low-income and middle-income countries (LMICs) have
Germany experienced major changes in diet and physical activity
Wallomia, Belgium
Malta patterns during the past three decades in a process
Denmark termed nutrition transition.19 Typically, consumption of
Sweden
Flanders, Belgium
processed foods—characterised as energy dense (foods
Norway high in sugar and fat) but nutrient poor (providing low
Finland amounts of essential vitamins, minerals, and fibre)—has
Switzerland*
Brussels, Belgium increased in LMICs.19 These dietary changes are coupled
France with reductions in overall physical activity (labour and
Slovenia leisure). The resulting increase in sedentary time has
Poland
contributed to a progressive increase in energy balance
0·5 5·0 10·0 15·0 20·0 25·0 30·0
Prevalence of maternal obesity (%) leading to a global shift from undernutrition to
overnutrition and micronutrient deficits. Excess weight is
Figure 2: Distribution of maternal obesity from Euro-Peristat database not only frequent (table 1), but it is also more common
and WHO
Obesity defined as BMI of more than 30 kg/m². *From WHO database (2009; than being underweight among women of reproductive
includes all women aged 20 years or above as proxy for maternal obesity. age in most developing countries in Latin America, Asia,
Reproduced from Devlieger and colleagues, with permission from Elsevier.9 and even Africa.19,22,23
In LMICs, obesity was historically concentrated in
women of reproductive age with BMI more than women from urban areas, with high socioeconomic
30 kg/m² typically remains less than 10%, although status and education levels.24,25 However, obesity has
obesity estimates are slightly higher when lower Asia- followed a continuous upward trend, particularly among
specific definitions are used.12 rural and poorly educated women, suggesting that this
Valid measures are required to address the impact of gap will disappear.26–28 The rate at which obesity
pre-pregnancy obesity on health outcomes. Use of prevalence is increasing in LMICs has been faster than
measured heights and bodyweights in early pregnancy, that observed in developed countries, perhaps because
routinely collected in clinical practice and thus available women from LMICs seem to be more susceptible to an
from medical records, ignores early gestational weight obesogenic environment, thus raising concerns that this
gain, which itself predicts some maternal and child susceptibility will be reflected in a rapid upturn in
health outcomes such as maternal post-partum weight metabolic and cardiovascular risk.29

2 www.thelancet.com/diabetes-endocrinology Published online October 12, 2016 http://dx.doi.org/10.1016/S2213-8587(16)30217-0


Series

Particularly striking rises in obesity among women in women than in men in most LMICs,23,30 which might
have occurred in some LMICs. 0·8 million women in be a consequence of complex sociocultural patterns
India were obese in 1975, but by 2014 this figure rose to including the woman’s role as the head of the family,
an estimated 20 million women—more than twice the weight gain associated with pregnancy, occupational
number of obese men.3 Indeed, obesity is more common activities, and cultural perceptions that relate larger body
size to fertility, healthfulness, and prosperity.
Prevalence of obesity Prevalence of Development in LMICs such as early life nutritional
in women of obesity in deficits followed by excesses (amplified by rapid
reproductive age* pregnant women
economic development) might also influence the
European region increased susceptibility of obesity in women.19 These
Albania, 2008–09 36·0% 21·2% factors require consideration when sex-specific
Armenia, 2005 15·5% 11·6 % preventive strategies are developed for use in these
Azerbaijan, 2006 17·9% 10·0% populations.30,31
Moldova, 2005 18·2% 12·7% Representative data for the prevalence of excess
Tajikistan, 2012 9·5% 5·0% bodyweight in pregnant women of LMICs are scarce;
Turkey, 2003 29·4% 20·7% estimates have been made based on the Demographic
Eastern Mediterranean region Health Survey of 52 LMICs between January, 2000, and
Egypt, 2008 39·6% 24·6% January, 2015 (table 1). Prevalence varied by WHO region;
Jordan, 2012 27·4% 31·0% overall these data indicate that excess bodyweight is now
Morocco, 2003–04 11·0% 12·5% frequent among pregnant women from LMICs in
Pakistan, 2012–13 15·0% 9·7% Europe, the eastern Mediterranean region and the
African region Americas. In Africa, obesity rates among pregnant
Benin, 2011–12 7·5% 7·2% women ranged from 0·7% to 26·8% according to the
Burkina Faso, 2010 3·3% 2·1% most reliable data (in some of these countries, response
Burundi, 2010 1·6% 0·9% rates were below 50%); as occurs in other regions,
Cameroon, 2011 12·2% 9·3% associated complications increase with obesity rates.32
Chad, 2004 1·5% 1·0% Also, obesity-related disorders might be more challenging
Congo (Brazzaville) 9·3% 5·8% to manage and therefore more serious in LMICs,
2011–12 considering that health systems in LMICs have
Democratic Republic of 2·6% 1·4% traditionally devoted their resources to problems of
Congo, 2007 infectious diseases. As described by Godfrey and
Ethiopia, 2011 1·0% 1·1% colleagues33 in this Series, maternal obesity is associated
Gabon, 2012 18·7% 22·5%
Ghana, 2008 9·3% 10·0%
Guinea, 2012 3·2% 4·0% Prevalence of obesity Prevalence of
in women of obesity in
Kenya, 2008–09 7·2% 6·7%
reproductive age* pregnant women
Lesotho, 2009 23·7% 26·8%
(Continued from previous column)
Liberia, 2007 5·7% 4·0%
Americas region
Madagascar, 2008–09 1·2% 0·7%
Bolivia, 2008 17·4% 20·3%
Malawi, 2010 4·2% 2·7%
Colombia, 2010 15·2% 16·1%
Mali, 2006 5·2% 4·3%
Guyana, 2009 22·0% 26·3%
Mozambique, 2011 4·2% 2·8%
Haiti, 2012 7·8% 6·4%
Namibia, 2006–07 12·0% 10·7%
Honduras, 2011–12 22·1% 22·0%
Niger, 2012 3·7% 3·0%
Nicaragua, 2001 18·0% 12·9%
Nigeria, 2008 6·0% 7·4%
Peru, 2012 17·9% 22·6%
Rwanda, 2010 2·2% 2·8%
Southeast Asia region
São Tomé and Príncipe, 12·2% 8·6%
2008–09 Bangladesh, 2011 2·9% 3·1%
Senegal, 2010–11 5·8% 5·5% India, 2006 2·8% 1·2%
Sierra Leone, 2008 9·3% 9·9% Maldives, 2009 11·1% 12·1%
Swaziland, 2006–07 23·0% 25·1% Nepal, 2011 2·2% 1·6%
Tanzania, 2010 6·2% 3·9% Timor-Leste, 2009–10 0·8% 0·9%
Uganda, 2011 4·2% 5·5%
Data are from World Obesity Federation20 and Demographic Health Surveys.21
Zambia, 2007 6·3% 4·2% *15–49 years of age.
Zimbabwe, 2010–11 10·6% 9·1%
Table 1: Prevalence of obesity in low-income and middle-income countries
(Table 1 continues in next column) among women of childbearing age and pregnant women by WHO region

www.thelancet.com/diabetes-endocrinology Published online October 12, 2016 http://dx.doi.org/10.1016/S2213-8587(16)30217-0 3


Series

with childhood obesity and associated metabolic and also reduces the chance of pregnancy success with
cardiovascular conditions.34,35 This association has seldom assisted reproductive technology. Women with obesity
been explored in LMICs and the resulting health experience a 68% reduction in livebirths from an
problems might be worse in LMICs than in high-income assisted reproductive technology cycle compared with
countries.36 women of normal weight.47,48

Preconceptional obesity and pregnancy Early pregnancy loss, fetal and infant death
complications Early pregnancy loss is more prevalent in women with
Pre-existing obesity-related disorders obesity than those of normal weight. A systematic review
The rise in obesity prevalence is considered to be the of reviews49 estimated the risk of miscarriage to be 30%
major determinant of the striking increase in pre-existing higher in pregnant women with obesity than in those
type 2 diabetes among pregnant women. Prevalence of with a healthy weight (pooled odds ratio [OR] 1·31,
pre-existing type 2 diabetes increased more than 4 times 95% CI 1·18–1·46). The probability of stillbirth is also
between 1994 and 2004 in the USA, surpassing the rates raised: the risk is doubled among women in the highest
of pre-existing type 1 diabetes (0·42% vs 0·33%).37,38 BMI category (2·19, 2·03–2·36) compared with women
Pregnant women with pre-existing diabetes are at with a normal BMI. Several pregnancy complications
increased risk of poor maternal, fetal, and neonatal associated with maternal obesity, notably gestational
outcomes, including pregnancy loss, perinatal mortality, diabetes and pre-eclampsia, have been implicated in fetal
fetal macrosomia, and congenital malformations.39 death and stillbirth.
Pregnancy increases the risk of diabetic retinopathy Accurate assessment of fetal size and detection of
progression in women with pre-existing diabetes by congenital anomalies during ultrasound scanning is
almost 2 times.40 Bramham and colleagues41 highlighted problematic in women with obesity,50 and fetal overgrowth
that chronic hypertension is also an increasing problem and congenital anomalies increase the risk of stillbirth.
in antenatal care. In comparison with general population The inability of mothers to detect reduced fetal
data from the USA, this review41 of 55 studies of pregnant movements could also contribute to delayed identification
women with pre-existing chronic hypertension showed of risk of stillbirth.51
an increased risk of superimposed pre-eclampsia Infant death—ie, within the first year of life—might
(25·9%, 95% CI 21·0–31·5), caesarean section (41·4%, also have origins associated with maternal obesity.49 A
35·5–47·7), preterm delivery (less than 37 weeks’ study52 of 11 294 neonatal deaths among 3 321 555 women
gestation; 28·1%, 22·6–34·4), low birthweight (less than revealed a linear association between maternal BMI and
2500 g; 16·9%, 13·1–21·5), neonatal unit admission neonatal death. A report of more than 250 000 obese
(20·5%, 15·7–26·4), and perinatal death (4·0%, 2·9–5·4). women from the USA found a U-shaped association
These statistics reinforce the need for early pregnancy between gestational weight gain and infant death in
screening for co-morbidities in women with precon- obese women. Among women with class I or class II
ceptional obesity and, as reviewed by Hanson and obesity, gestational weight gain as well as gestational
colleagues42 in this Series, the urgent need for a greater weight loss and very low weight gain were associated
emphasis on a multifaceted approach to achieve weight with infant death.53 In view of the current focus on
loss before conception in women of reproductive age. limitation of gestational weight gain in the management
of obese women, the previously unrecognised association
Fertility of adverse outcomes with low gestational weight gain
The worldwide prevalence of obesity-related infertility is and gestational weight loss should prompt caution
reflected by an exponential increase in related against overzealous regimens for weight control.
publications; 3000 articles on this subject were
published in 2014 compared with fewer than ten in Congenital anomalies
1980.43 Obese women who are intending to become Maternal obesity is reported to increase the risk of some
pregnant take longer on average to conceive,44 and time fetal defects and congenital anomalies.49 A 2009 meta-
to pregnancy increases with the degree of obesity. analysis54 showed that children of women with obesity are
Women with class III obesity (BMI ≥40 kg/m²) are at increased risk of neural tube defects (OR 1·87, 95% CI
almost 7 times more likely to take more than 12 months 1·62–2·15); hydrocephaly (1·68, 1·19–2·36); and
to conceive than those with a normal BMI (relative risk cardiovascular (1·30, 1·12–1·51), orofacial (such as cleft
[RR] 6·9, 95% CI 2·9–16·8).45 Ovulatory dysfunction, palate, 1·20, 1·03–1·40), and limb reduction anomalies
the most common infertility diagnosis among obese (1·34, 1·03–1·73) compared with healthy women of
women, appears to be independent of age or parity,46 recommended weight. A systematic review55 of 22 studies
and is likely to result from suboptimal glycaemic control reported associations of prenatal environmental risk
and insulin resistance associated with obesity. Assisted factors and infants born with anorectal malformations;
reproductive technology does not provide a simple maternal obesity was consistently associated with these
solution to obesity-related infertility because a high BMI uncommon congenital anomalies (1·64, 1·35–2·00). By

4 www.thelancet.com/diabetes-endocrinology Published online October 12, 2016 http://dx.doi.org/10.1016/S2213-8587(16)30217-0


Series

contrast, the risk of gastroschisis is reduced in pregnant of gestational diabetes.64 Undiagnosed pre-existing
women who are obese (0·17, 0·10–0·30).49,54 Although diabetes should also be considered as a confounder,
associations between maternal obesity and fetal although when women with a previous diagnosis of
abnormalities have been consistently observed, diabetes were excluded from a cohort of obese women,
interpretation should be cautious because preconceptional obesity class and the risk of gestational diabetes were
diabetes and uncertain maternal preconceptional folate linearly related compared with normal weight women
status could confound results.56 (overweight: RR 1·99, 95% CI 1·86–2·13; class I obesity:
2·94, 2·73–3·18; class II: 2·78, 2·5–3·01; and class III:
Birthweight 3·55, 3·26–3·86; p<0·001).58
High birthweight and large for gestational age infants The prevalence of gestational diabetes is increasing
are more common in pregnancies complicated by obesity worldwide. A longitudinal study65 in Colorado, USA,
than in those of normal weight women.49 Maternal reported a doubling of prevalence between 1994 and
obesity has been associated with a more than 2 times risk 2002, independent of ethnic origin. Populations in
of delivery of a large for gestational age infant LMICs with historically low frequencies of gestational
(>90th centile; OR 2·08, 95% CI 1·95–2·23), compared diabetes seem to be experiencing striking increases in
with normal weight women.57 Analysis of a 2002–08 gestational diabetes resulting from obesity, but reliable
retrospective US cohort of more than 12 000 women data are hard to obtain and comparison between
without any pre-existing chronic disease, including countries is confounded by a number of factors such as
diabetes, showed that maternal obesity (class I, II, and different diagnostic practices and prevalences in
III) was associated with several neonatal outcomes subpopulations; lack of discrimination between pre-
including large for gestational age, the risk of which existing type 1 and type 2 diabetes and gestational
increased by more than 30% from class I (relative diabetes; and by very high numbers of pregnant women
risk [RR] 1·74, 95% CI 1·65–1·83) to class III (2·32, whose gestational diabetes remains undiagnosed, which
2·14–2·52), when compared with a reference group of might amount to half of all cases in LMICs.66,67 A review68
normal weight women.58 Pre-pregnancy obesity increases that examined gestational diabetes in LMICs estimated
the risk of high birthweight (>4000 g; OR 2·00, that the highest population attributable risk (PAR) of
1·84–2·18) and of fetal macrosomia (defined in this study gestational diabetes from raised maternal BMI was in
as >4500 g; 3·23, 2·39–4·37),57 generally attributed to an Turkey (63%) followed by India (50%), Brazil (45%),
increase in fetal body fat mass.59 Although pre-pregnancy Thailand (31%), China (20%), and Iran (14%). The
obesity has generally been associated with reduced risk authors estimated that elimination of overweight or
of low birthweight, a few reports suggest an increased obesity before or early in pregnancy would result in 14%
risk of intrauterine growth restriction and small for to 35% fewer women with gestational diabetes, pre-
gestational age delivery (<10th centile),49 which could be eclampsia, or pregnancy-induced hypertension in Brazil,
associated with the increased prevalence of pre-eclampsia China, India, Iran, and Thailand.
in obese women.60,61
Sustained trends towards a reduction in average Pre-eclampsia, pregnancy-induced hypertension, and
population birthweights in the USA and elsewhere from thromboembolism
2000 onwards62 have been a surprise in view of the con- The risk of pregnancy-induced hypertension and pre-
comitant rise in obesity, although 2014 statistics suggest eclampsia is increased in pregnant women who are
this trend might be reversing.63 However, interpretation obese.58,69 Reviews, including a total of 54 case-control and
of these and other national or global trends in birthweight cohort studies, have concluded that obesity increases the
in relation to obesity prevalence is difficult because risk of pre-eclampsia by 3–10 times.49,70,71 In LMICs,
obstetric practice is likely to have an overriding influence, Rahman and colleagues68 reported that obesity was
including reduction of gestational age at delivery (and associated with an OR for pre-eclampsia of 3·87 (95% CI
therefore birthweight) through induction of labour or 3·48–4·29) in comparison with normal-weight women.
caesarean section. Some population studies72 in high-income countries have
suggested an increase in prevalence of pre-eclampsia in
Gestational diabetes line with increasing obesity. In the USA for example,
Maternal obesity is strongly associated with gestational obesity was reported to contribute to a 6·7 times (5·6–8·0)
diabetes,49 with reported risk increasing with BMI and increased risk of severe pre-eclampsia in 2010 compared
being 4–9 times greater than for normal weight women. with women who delivered in 1980. However, a reduction
The large range in risk estimate is most likely explained in smoking—shown to reduce rates of pre-eclampsia—
by global variations in diagnostic criteria for gestational and increased maternal age were also major contributors.
diabetes. With the rigorous International Association of The occurrence of venous thromboembolism increases
Diabetes in Pregnancy Study Groups criteria, now 4–5 times in pregnancy and the post-partum period.
adopted by WHO, as many as a quarter of women with Morgan and colleagues73 reviewed 12 studies published
obesity (mean BMI >36 kg/m²) could have a diagnosis between 2001 and 2009 that investigated obesity as a risk

www.thelancet.com/diabetes-endocrinology Published online October 12, 2016 http://dx.doi.org/10.1016/S2213-8587(16)30217-0 5


Series

factor for venous thromboembolism in pregnancy or membranes, and spontaneous premature labour without
post partum. Nine studies reported an increased risk of premature rupture of the membranes. Premature births
venous thromboembolism in obese women during (medically indicated and spontaneous) increased with
pregnancy or post partum. Because of wide variability BMI class in both cohorts, the risk being greatest for
between studies and in the definition of obesity, an extremely early preterm births (22–27 weeks’ gestation;
overall OR was not estimated, but the range was class III in California OR 1·93, 95% CI 1·67–2·23;
estimated to be 1·4–5·3.73 class III in Sweden 2·73, 1·96–3·80). This increase was
in part due to iatrogenic delivery associated with diabetes
Labour and delivery and hypertensive disease, as illustrated by a substantial
Labour and delivery practices vary widely globally, but reduction in medically indicated preterm birth risk
women with obesity are consistently more likely to associated with obesity across all gestations following
deliver by caesarean section than are normal weight exclusion of women with these conditions. Despite this
women. A systematic review74 of 11 cohort studies contribution from iatrogenic deliveries, a strong
comprising 166 168 nulliparous women estimated an RR independent association remained between obesity and
of 2·26 (95% CI 2·0–2·51) for class I obesity and 3·38 extremely early spontaneous premature birth from
(2·49–4·57) for class II and III obesity (BMI ≥35·0 kg/m²) premature rupture of the membranes and from
compared with nulliparous women with a normal BMI. spontaneous labour at 22–27 weeks’ gestation. For
Caesarean section rates have increased across the world; example, for women with class III obesity the risk of
data from 121 countries show that between 1990 and spontaneous labour was more than doubled compared
2014, the global average caesarean section rate increased with normal weight women (California 2·21, 1·76–2·77;
from 6·7% to 19·1%, with LMICs showing a greater Sweden 2·38, 1·48–3·81). In more mature preterm
rise.75 However, attempts to estimate the fraction infants (26–36 weeks), maternal obesity either had no
attributable to the parallel rise in obesity is challenging effect or was protective of spontanteous preterm birth,
because local clinical practices and changing clinical suggesting a potential causal role for maternal obesity in
guidelines can play a part. In Brazil, for example, where the onset of very early preterm birth. An obesity-related
obesity has soared from 1·9 million to 18 million women increase in premature deliveries might also contribute to
between 1975 and 2014,3 the caesarean section rate is the higher number of neonatal inpatient episodes in
55·6%.75 This rise is unlikely to be entirely attributable to children born to obese women in comparison with
obesity alone, because most caesarean sections in Brazil normal weight mothers.78
are done for non-medical reasons, although one
Brazilian cohort study76 did list maternal BMI as a Mental health
contributing factor. Although obesity is associated with depression in non-
Obese women are also more likely to require induction pregnant individuals,82 little attention has been paid to
of labour,77 and to experience post-partum haemorrhage. mental health in obese pregnant women. Systematic
Obesity (BMI ≥30 kg/m²) has been associated with an reviews49,83 of women who are obese when they become
OR of 1·20 (1·16–1·24) and morbid obesity (BMI pregnant show that risk of elevated depression symptoms
≥40 kg/m²) with an RR of 1·43 (1·33–1·54) for post- is higher during pregnancy (OR 1·43, 95% CI 1·27–1·61)
partum haemorrhage,78 which might reflect the risk of and post partum (1·30, 1·20–1·42) than in women of
post-partum haemorrhage after caesarean section.79 normal weight. An increased incidence of depression
Other contributing factors might include bleeding from might affect physical outcomes because depression has
a larger than normal placental surface area that been independently associated with gestational diabetes,
accompanies obesity, and larger body tissue and plasma pre-eclampsia, preterm birth, and low birthweight.83,84
volume of distribution of uterotonic drugs.80
Post-partum consequences of maternal obesity
Premature birth Breastfeeding
Although premature birth is not widely recognised as an Systematic reviews85,86 have suggested that obesity is
adverse outcome associated with obesity, a 2015 review of associated with failure to initiate breastfeeding and a
reviews49 concluded that premature birth was associated reduction in breastfeeding duration. Physiological and
with maternal obesity. Distinction between medically psychological factors, as well as physical discomfort are
indicated and spontaneous preterm birth has rarely been potential contributory factors. Delayed onset of lactation
made, although high caesearean section rates might be is implicated,87 as well as high rates of caesarean section,
expected to skew towards an iatrogenic explanation. which have been associated with poorer breastfeeding
However, a study81 of two cohorts totalling 3·5 million outcomes.88 The weight and discomfort of large breasts89
births from California, USA, and Sweden, concluded and psychological factors including body image
that obesity increases the risk of medically indicated dissatisfaction and postnatal depression90 might play a
preterm birth, spontaneous premature birth part in shorter duration of breastfeeding compared with
accompanied by preterm premature rupture of the women of normal weight.

6 www.thelancet.com/diabetes-endocrinology Published online October 12, 2016 http://dx.doi.org/10.1016/S2213-8587(16)30217-0


Series

Post-partum weight retention and risks in next In summary, a dose–response association is generally
pregnancy seen between interpregnancy weight gain and risks of
If associations between pre-pregnancy or early pregnancy obesity-related pregnancy outcomes and perinatal com-
BMI and pregnancy complications are causal, weight plications in the next pregnancy, even if the weight gained
change between one pregnancy and the next is likely to is modest (ie, 2–3 BMI units). Although attempts to limit
influence risk of complications in the next pregnancy. weight gain in pregnancy have proven challenging,
More women gain rather than reduce weight between weight retention after pregnancy is an important and
pregnancies. A gain of at least 2 BMI units was reported in potentially modifiable target to achieve reduced risk of
21–46% women and weight loss of at least 2 BMI units in adverse outcomes in subsequent pregnancies.
5–17% of women in the studied populations.91–97 Weight
gain and weight loss are more common among women Long-term morbidity
who start pregnancy overweight or obese than among New or persistent obesity in the mother
normal weight women.94,97,98 However, interpregnancy Complications arising in pregnancies in which the
weight changes are generally quite modest and few women mother is obese might also have long-term consequences
reduce their bodyweight, which reduces the statistical for the health of the mother, and her child. As Godfrey
power of cohort analyses and can restrict conclusions. and colleagues33 discuss in this Series, the consequences
Population-based studies94,98–101 have shown that risks of for the health of the child, and the potential underlying
gestational diabetes and pregnancy-induced hypertensive mechanisms are reviewed, but we will focus here on the
diseases from one pregnancy to the next increase with risk of longer-term morbidities in the mother.
interpregnancy weight gain, and the risk of gestational Observational studies106 generally support an
diabetes in the next pregnancy can be more pronounced association between pregnancy and long-term adiposity
in women starting off with normal weight.94,100 Post- in the mother, particularly for women who already have
partum weight reduction in overweight or obese women obesity when beginning pregnancy, despite wide
reduces the risk of these disorders in the next variability in gestational weight gain among this group.
pregnancy.94,101 The risk of recurrent pre-eclampsia also Few pregnancy cohort studies have obtained serial
increases with interpregnancy weight gain and is measurements of post-partum weight to differentiate
reduced with weight loss.95 retention of gestational weight gain from subsequent
Mode of delivery during subsequent pregnancies is post-partum weight gain or loss, and thus, whether the
also affected by obesity or overweight. The risk of aetiology of persistent adiposity resulting from childbirth
caesarean section in the next pregnancy increases with is primarily due to excessive pregnancy weight gain
amount of interpregnancy weight gain,96,98,100 probably versus post-partum obesogenic lifestyle behaviours, or
including the risk of both emergency and non- an equal contribution from both is unclear. Overall, data
emergency caesarean deliveries.102 Interpregnancy comparing trends in the trajectory of weight gain among
weight gain in normal-weight women might decrease women with no births versus women with one or more
the probability of vaginal birth after a caesarean, and births reveal greater gains among women with
weight loss in overweight or obese women might children.107,108 Thus, pregnancy, especially the first
increase success rate of vaginal birth after a caesarean.97 pregnancy, is an independent risk factor for new or
Women who increase their weight from one pregnancy persistent obesity in women.106 Pregnancy is therefore a
to the next, from normal weight to overweight or obese, key risk factor for obesity among women, and one that is
increase their risk of medically indicated preterm birth in likely to contribute to the worldwide predominance of
the next pregnancy, whereas a BMI change from normal obesity in women compared with men.3
to underweight increases the risk of spontaneous preterm
birth.103 Risk of birth of a large for gestational age infant Metabolic dysfunction
also increases with interpregnancy weight gain, and The pregnancy complications associated with obesity
weight loss reduces the risk.93,98,100 The effect of might pose an added stress to the long-term metabolic
interpregnancy weight gain is stronger in women who health of obese mothers.109,110 After delivery, women with
start their first pregnancy with normal weight than in gestational diabetes are at increased risk for development
those who start overweight or obese.100 Maternal obesity is of type 2 diabetes; variance in risk of type 2 diabetes
associated with fetal congenital abnormalities including appears quite large, ranging from 2·6% to 70% when
cleft palate.104 Interpregnancy weight gain of more than evaluated from as early as 6 weeks after delivery to as late
3 BMI units has been associated with more than double as 28 years post partum.111 A 2016 systematic review112 of
the risk of cleft palate in the subsequent pregnancy.92 39 studies including 95 750 women with gestational
Interpregnancy weight gain increases stillbirth risk in a diabetes confirmed the association with type 2 diabetes,
second pregnancy91,100,105 in a dose–response manner;91 in and heightened risk of type 2 diabetes in women with an
overweight or obese women, interpregnancy weight loss early diagnosis of gestational diabetes (RR 2·13, 95% CI
reduces the risk of neonatal mortality in a subsequent 1·52–3·56), raised fasting glucose concentration (3·57,
pregnancy.91 2·98–4·04), increased HbA1c (2·56, 2·00 to 3·17), and in

www.thelancet.com/diabetes-endocrinology Published online October 12, 2016 http://dx.doi.org/10.1016/S2213-8587(16)30217-0 7


Series

Complications
Maternal
Preconception Hypertension, renal dysfunction, type 2 diabetes, infertility, in-vitro fertilisation failure
Pregnancy Pre-existing chronic hypertension or renal disease, pre-existing type 2 diabetes, miscarriage, gestational diabetes, gestational
hypertension, pre-eclampsia, venous thromboembolism, labour complications, caesarean section, depression, premature birth
Immediately postpartum Post-partum haemorrhage, venous thromboembolism, delayed onset of breastfeeding, shortened duration of breastfeeding
Persistent postpartum Weight gain or persistent obesity, hyperlipidaemia, type 2 diabetes*, ischaemic heart disease†, hypertension†, stroke†
Fetal or neonatal Macrosomia, large for gestational age, stillbirth, congenital malformation, shoulder dystocia, neonatal hypoglycaemia

*After gestational diabetes. †After pre-eclampsia.

Table 2: Short-term and long-term outcomes associated with obesity in pregnancy

lipoprotein-cholesterol—emerging as early as 1 year after


Panel: Research priorities delivery.115,116 These findings might persist for more than
1 Research to develop effective strategies to prevent obesity in women of reproductive 10 years of follow-up.117,118
age, including a focus on weight management in adolescents. The risk of pre-eclampsia is increased in obese
2 Implementation research to show that strategies to prevent and manage obesity in women, which itself is associated with life-long risk of
women of reproductive age in high-income countries are as effective and practical in maternal cardiovascular disease, as well as risks for the
low-income and middle-income countries (LMICs). child’s cardiovascular health. After pre-eclampsia, the
3 Nationally representative estimates of the prevalence of obesity and its associated risk of hypertension increases 4 times, and risk of
conditions, particularly gestational diabetes, are needed in LMICs (eg, through the ischaemic heart disease and stroke doubles, although
INDEPTH network or similar initiatives), to improve estimation of health and economic what proportion of this heightened susceptibility is
burden and allow political prioritisation. attributable to existing pre-pregnancy cardiovascular
4 Prevention of post-partum weight retention in obese women and those with a normal risk is unknown.119 Long-term adverse effects in the
BMI would reduce the risk of maternal and fetal complications in the next pregnancy. offspring include hypertension, vascular dysfunction,
Research is needed to develop effective evidence-based interventions to reduce weight and stroke.120 Whether control of weight in pregnancy
retention, with evaluation of clinical outcomes in a subsequent pregnancy. and the early post-partum period results in long-term
5 Research to determine whether preconception, pregnancy, or post-partum improvements in maternal (or child) cardiovascular risk
interventions reduce the risk of later cardiovascular and metabolic disease in obese factors is also unknown. However, weight loss between
women. pregnancies does reduce risk of pregnancy-induced
6 Research to establish clinical management pathways in primary care for obese and hypertension and recurrent pre-eclampsia in the
normal weight women who have gestational diabetes and pre-eclampsia, including subsequent pregnancy,95 which has the potential to end
health economic evaluation. the cycle of cardiometabolic disease for mothers and
their children (table 2).

those treated with insulin (3·66, 2·78–4·82). A woman’s Discussion


BMI (1·95, 1·60–2·31), her family history of diabetes Obesity challenges the health of the mother and has
(1·70, 1·47–1·97), non-white ethnicity (1·49, 1·14–1·94), much wider and long-lasting consequences than are
and advanced age (1·20, 1·09–1·34) also increased the generally appreciated by either health professionals or
risk. Gestational weight gain was not associated with women themselves. Most women with obesity who
development of type 2 diabetes.112 At the population level, intend to conceive are not aware of the risks of infertility,
gestational diabetes, being increasingly prevalent, or of the myriad risks of complications that might ensue
probably has a causal role in the escalating rates of type 2 if conception is successful. The evidence for almost all
diabetes among women, and as detailed by Ma and outcomes we report in this Series paper is very high.
colleagues113 in this Series, clinicians should adhere to However, large-scale observational studies are still
recommended guidelines for appropriate post-partum needed to determine the scale of the problem in LMICs—
screening. Beyond this approach, new strategies are particularly in relation to gestational diabetes. Improved
needed for continued monitoring for type 2 diabetes and diagnosis and treatment of gestational diabetes is
early treatment. important as the prevalence of obesity increases.
The options for management of pre-pregnancy obesity
Cardiovascular effects are either to prevent its complications once pregnancy
Obese women have greater increases in central adiposity starts or to reduce BMI before pregnancy. Many health
and fat mass accrual during the post-partum period than professionals have called for efforts to intervene precon-
do healthy weight women,114 predisposing them to ceptionally among obese women, so that more women
elevations in blood pressure and low density lipo- enter pregnancy at a healthy weight.2,121 The complexities
proprotein-cholesterol, and to reductions in high density of this problem and suggested approaches are reviewed in

8 www.thelancet.com/diabetes-endocrinology Published online October 12, 2016 http://dx.doi.org/10.1016/S2213-8587(16)30217-0


Series

pregnancy complications have emerged, but whether


Search strategy and selection criteria these reflect pre-existing cardiovascular risk, or whether
We searched MEDLINE, with no date range for English interventions in the preconception period, during
language articles, using the search terms “obesity and pregnancy, or post partum reduce risk, remains to be
pregnancy”, or “obesity women”, or “maternal obesity”, or “ determined. No evidence exists for an effective long-term
gestational weight gain”, in combination with the terms post-partum management programme for detection and
“developing countries”, “pre-pregnancy BMI”, effective treatment of long-term cardiovascular and
“preconception”, “trends”, “prevalence”, “LMIC countries”, metabolic risk in obese women who have suffered from
“outcomes”, “fertility”, “miscarriage or early pregnancy loss”, pre-eclampsia or gestational diabetes.
gestational diabetes”, “pre-eclampsia”, “caesarean section”, These unmet needs require renewed vigour, and focus
“breast feeding”, “birthweight”, “congenital anomaly or of effort (panel), if the escalation of suboptimal health is
malformation”, “mental health”, “gestational weight gain”, to be reversed among mothers affected by obesity, and
“premature birth”, “venous thromboembolism”, “long-term”, their children. A pragmatic solution to prevent the adverse
“postpartum weight retention”, “child obesity”, “child health consequences of preconceptional and maternal
outcomes”, “cardiovascular risk factors”, “hypertension”, and obesity is to promote interventions in all three windows of
“hyperlipidemia”. When we searched MEDLINE for opportunity—preconception, pregnancy, and post
“interpregnancy weight change”, we found 35 articles and partum—and to build appropriate pathways of care.122
included 14 articles in which “interpregnancy weight change” Contributors
was either the exposure or the outcome. For prevalence of LP and MWG had overall responsibility for the writing of the manuscript.
SC, CC, RU, and SH contributed equally to the literature search and
obesity, the search was limited to articles presenting results
writing of the manuscript. RC undertook the research for and provided
based on representative data. For prevalence in low-income figure 2. All authors agreed the final draft of the manuscript.
and middle-income countries, we also used data we knew Declaration of interests
was available from key authors (ie, Caleyachetty R, Institute LP reports grants from Abbott Nutrition and NESTEC, outside the
of Applied Health Research, University of Birmingham, submitted work. SH reports grants from the US National Institutes of
Birmingham, UK). We mainly selected publications in the past Health, Doris Duke Charitable Foundation, and Health Resources and
Services Administration during the conduct of the study.
5 years, but did not exclude commonly referenced and highly
regarded older publications. We also searched the reference Acknowledgments
We thank Julie Johnson McGrath (Obesity Prevention Program, Harvard
lists of articles identified by this search strategy and selected Pilgrim Health Care Institute, Boston, MA, USA) for her help and
those we judged relevant. Review articles and book chapters efficiency in preparation of this manuscript.
are cited to provide readers with more details and more References
references than are covered in this Series paper. 1 Gillman M. Interrupting intergenerational cycles of maternal
obesity. In: Fewtrell M, Haschke F, Prescott S, eds. Preventive
aspects of early nutrition. Nestlé Nutr Inst Workshop Ser; 85: 59–69.
2 Davies SC. Annual Report of the Chief Medical Officer, 2014,
greater depth by Hanson and colleagues42 in this Series. In The Health of the 51%: Women London: Department of Health;
view of the many women worldwide who enter pregnancy 2015. https://www.gov.uk/government/uploads/system/uploads/
with obesity, the need for effective management and attachment_data/file/544470/CMO_annual_report_2014.pdf
(accessed May 4, 2016).
interventions in pregnancy will remain until such time as 3 NCD Risk Factor Collaboration. Worldwide trends in diabetes since
pre-conceptional strategies are successful, a point 1980: a pooled analysis of 751 population-based studies with
discussed in more detail by Ma and colleagues113 in this 4·4 million participants. Lancet 2016; 387: 1513–30.
4 Flegal KM, Carroll MD, Kuczmarski RJ, Johnson CL.
Series. Randomised controlled trials of behavioural Overweight and obesity in the United States: prevalence and trends,
interventions in early pregnancy to reduce weight gain or 1960–1994. Int J Obes Relat Metab Disord 1998; 22: 39–47.
prevent gestational diabetes have been without sub- 5 Ogden CL, Carroll MD, Curtin LR, McDowell MA, Tabak CJ,
Flegal KM. Prevalence of overweight and obesity in the United
stantive improvement in adverse maternal–fetal health States, 1999–2004. JAMA 2006; 295: 1549–55.
outcomes. However, clinical guidelines should be 6 Ogden CL, Carroll MD, Kit BK, Flegal KM. Prevalence of childhood
enforced, especially in relation to glycaemic control, in and adult obesity in the United States, 2011–2012. JAMA 2014;
311: 806–14.
which focus should be placed on rigorous adherence to
7 Rasmussen KM. Public health policies relating to obesity in
recommendations, especially diagnosis and treatment of childbearing women. In: Gillman MW and Poston L, eds.
gestational diabetes in obese women. Another feasible Maternal obesity. Cambridge: Cambridge University Press, 2012:
approach is to target weight management post partum 237–42.
8 Moody A. Health survey for England 2013: adult anthropometric
because weight retention after one pregnancy increases measures, overweight and obesity. Health and Social Care
the risk of adverse outcomes in the next. The post-partum Information Service, 2014. http://digital.nhs.uk/catalogue/
period offers an amenable window of opportunity, as PUB03023/heal-surv-eng-2010-resp-heal-ch10-adul-anth.pdf
(accessed Sept 10, 2016).
women with newborn infants have more frequent contact 9 Devlieger R, Benhalima K, Damm P, et al. Maternal obesity in
with health professionals and interventions that should Europe: where do we stand and how to move forward?: A scientific
not be recommended in pregnancy (eg, weight loss) are paper commissioned by the European Board and College of
Obstetrics and Gynaecology (EBCOG).
appropriate in the post-partum period. The long-term Eur J Obstet Gynecol Reprod Biol 2016; 201: 203–08.
consequences of obesity for maternal health and

www.thelancet.com/diabetes-endocrinology Published online October 12, 2016 http://dx.doi.org/10.1016/S2213-8587(16)30217-0 9


Series

10 Jacobsen BK, Aars NA. Changes in body mass index and the 31 Goryakin Y, Lobstein T, James WP, Suhrcke M. The impact of
prevalence of obesity during 1994–2008: repeated cross-sectional economic, political and social globalization on overweight and
surveys and longitudinal analyses. The Tromso Study. BMJ Open obesity in the 56 low and middle income countries. Soc Sci Med
2015; 5: e007859. 2015; 133: 67–76.
11 Keating C, Backholer K, Gearon E, et al. Prevalence of class-I, 32 Onubi OJ, Marais D, Aucott L, Okonofua F, Poobalan AS.
class-II and class-III obesity in Australian adults between 1995 and Maternal obesity in Africa: a systematic review and meta-analysis.
2011–12. Obes Res Clin Pract 2015; 9: 553–62. J Public Health (Oxf) 2015; published online Oct 20. DOI:10.1093/
12 Kang HT, Shim JY, Lee HR, Park BJ, Linton JA, Lee YJ. Trends in pubmed/fdv138.
prevalence of overweight and obesity in Korean adults, 1998–2009: 33 Godfrey KM, Reynolds RM, Prescott SL, et al. Influence of maternal
the Korean National Health and Nutrition Examination Survey. obesity on the long-term health of offspring. Lancet Diabetes Endocrinol
J Epidemiol 2014; 24: 109–16. 2016; published online Oct 12. http://dx.doi.org/10.1016/S2213-
13 Karachaliou M, Georgiou V, Roumeliotaki T, et al. Association of 8587(16)30107-3.
trimester-specific gestational weight gain with fetal growth, 34 Norman JE, Reynolds RM. The consequences of obesity and excess
offspring obesity, and cardiometabolic traits in early childhood. weight gain in pregnancy. Proc Nutr Soc 2011; 70: 450–56.
Am J Obstet Gynecol 2015; 212: 502.e1–14. 35 Williams CB, Mackenzie KC, Gahagan S. The effect of maternal
14 Walter JR, Perng W, Kleinman KP, Rifas-Shiman SL, obesity on the offspring. Clin Obstet Gynecol 2014; 57: 508–15.
Rich-Edwards JW, Oken E. Associations of trimester-specific 36 Mitchell S, Shaw D. The worldwide epidemic of female obesity.
gestational weight gain with maternal adiposity and systolic blood Best Pract Res Clin Obstet Gynaecol 2015; 29: 289–99.
pressure at 3 and 7 years postpartum. Am J Obstet Gynecol 2015; 37 Albrecht SS, Kuklina EV, Bansil P, et al. Diabetes trends among
212: 499.e1–12. delivery hospitalizations in the U.S., 1994–2004. Diabetes Care 2010;
15 Bodnar LM, Siega-Riz AM, Simhan HN, Diesel JC, Abrams B. 33: 768–73.
The impact of exposure misclassification on associations between 38 Middleton P, Crowther CA, Simmonds L. Different intensities of
prepregnancy BMI and adverse pregnancy glycaemic control for pregnant women with pre-existing diabetes.
outcomes. Obesity (Silver Spring) 2010; 18: 2184–90. Cochrane Database Syst Rev 2016; 5: CD008540.
16 Shin D, Chung H, Weatherspoon L, Song WO. Validity of 39 Inkster ME, Fahey TP, Donnan PT, Leese GP, Mires GJ,
prepregnancy weight status estimated from self-reported height and Murphy DJ. Poor glycated haemoglobin control and adverse
weight. Matern Child Health J 2014; 18: 1667–74. pregnancy outcomes in type 1 and type 2 diabetes mellitus:
17 [United States] Centers for Disease Control Pediatric and Pregnancy systematic review of observational studies.
Nutrition Surveillance System. Pregnancy nutrition surveillance, BMC Pregnancy Childbirth 2006; 6: 30.
summary of trends in maternal health indicators. Table 16D. 2011. 40 Morrison JL, Hodgson LA, Lim LL, Al-Qureshi S.
http://www.cdc.gov/pednss/pnss_tables/pdf/national_table16.pdf Diabetic retinopathy in pregnancy: a review.
(accessed May 1, 2016). Clin Experiment Ophthalmol 2016; 44: 321–34.
18 Hunt KJ, Alanis MC, Johnson ER, Mayorga ME, Korte JE. 41 Bramham K, Parnell B, Nelson-Piercy C, Seed PT, Poston L,
Maternal pre-pregnancy weight and gestational weight gain and Chappell LC. Chronic hypertension and pregnancy outcomes:
their association with birthweight with a focus on racial differences. systematic review and meta-analysis. BMJ 2014; 348: g2301.
Matern Child Health J 2013; 17: 85–94.
42 Hanson M, Barker M, Dodd JM, et al. Interventions to prevent
19 Popkin BM, Adair LS, Ng SW. Global nutrition transition and the maternal obesity before conception, during pregnancy, and post
pandemic of obesity in developing countries. Nutr Rev 2012; partum. Lancet Diabetes Endocrinol 2016; published online Oct 12.
70: 3–21. http://dx.doi.org/10.1016/S2213-8587(16)30108-5.
20 World Obesity Federation. World map of obesity. 2015. http://www. 43 Fontana R, Torre SD. The deep correlation between energy
worldobesity.org/resources/world-map-obesity/ (accessed May 4, metabolism and reproduction: a view on the effects of nutrition for
2016). women fertility. Nutrients 2016; 8: 87.
21 The DHS Program. Demographic and health surveys. 44 Gesink Law DC, Maclehose RF, Longnecker MP. Obesity and time
https://dhsprogram.com/ (accessed May 1, 2016). to pregnancy. Hum Reprod 2007; 22: 414–20.
22 Mendez MA, Monteiro CA, Popkin BM. Overweight exceeds 45 Hassan MA, Killick SR. Negative lifestyle is associated with a
underweight among women in most developing countries. significant reduction in fecundity. Fertil Steril 2004; 81: 384–92.
Am J Clin Nutr 2005; 81: 714–21.
46 Chavarro JE, Rich-Edwards JW, Rosner BA, Willett WC. Diet and
23 Ng M, Fleming T, Robinson M, et al. Global, regional, and national lifestyle in the prevention of ovulatory disorder infertility.
prevalence of overweight and obesity in children and adults during Obstet Gynecol 2007; 110: 1050–58.
1980–2013: a systematic analysis for the Global Burden of Disease
47 Moragianni VA, Jones SM, Ryley DA. The effect of body mass index
Study 2013. Lancet 2014; 384: 766–81.
on the outcomes of first assisted reproductive technology cycles.
24 Lopez-Arana S, Burdorf A, Avendano M. Trends in overweight by Fertil Steril 2012; 98: 102–08.
educational level in 33 low- and middle-income countries: the role
48 Sim KA, Partridge SR, Sainsbury A. Does weight loss in overweight
of parity, age at first birth and breastfeeding. Obes Rev 2013;
or obese women improve fertility treatment outcomes? A systematic
14: 806–17.
review. Obes Rev 2014; 15: 839–50.
25 Subramanian SV, Perkins JM, Ozaltin E, Davey Smith G. Weight of
49 Marchi J, Berg M, Dencker A, Olander EK, Begley C.
nations: a socioeconomic analysis of women in low- to
Risks associated with obesity in pregnancy, for the mother and
middle-income countries. Am J Clin Nutr 2011; 93: 413–21.
baby: a systematic review of reviews. Obes Rev 2015; 16: 621–38.
26 Jaacks LM, Slining MM, Popkin BM. Recent underweight and
50 Best KE, Tennant PW, Bell R, Rankin J. Impact of maternal body
overweight trends by rural-urban residence among women in
mass index on the antenatal detection of congenital anomalies.
low- and middle-income countries. J Nutr 2015; 145: 352–57.
BJOG 2012; 119: 1503–11.
27 Jones-Smith JC, Gordon-Larsen P, Siddiqi A, Popkin BM. Is the
51 Hijazi ZR, East CE. Factors affecting maternal perception of fetal
burden of overweight shifting to the poor across the globe? Time
movement. Obstet Gynecol Surv 2009; 64: 489–97.
trends among women in 39 low- and middle-income countries
(1991–2008). Int J Obes (Lond) 2012; 36: 1114–20. 52 Aune D, Saugstad OD, Henriksen T, Tonstad S. Maternal body
mass index and the risk of fetal death, stillbirth, and infant
28 Lopez-Arana S, Avendano M, van Lenthe FJ, Burdorf A. Trends in
death: a systematic review and meta-analysis. JAMA 2014;
overweight among women differ by occupational class: results from
311: 1536–46.
33 low- and middle-income countries in the period 1992–2009.
Int J Obes (Lond) 2014; 38: 97–105. 53 Bodnar LM, Siminerio LL, Himes KP, et al. Maternal obesity and
gestational weight gain are risk factors for infant death.
29 Popkin BM, Slining MM. New dynamics in global obesity facing
Obesity (Silver Spring) 2016 24: 490–98.
low- and middle-income countries. Obes Rev 2013;
14 (suppl 2): 11–20. 54 Stothard KJ, Tennant PW, Bell R, Rankin J. Maternal overweight
and obesity and the risk of congenital anomalies: a systematic
30 Kanter R, Caballero B. Global gender disparities in obesity: a review.
review and meta-analysis. JAMA 2009; 301: 636–50.
Adv Nutr 2012; 3: 491–98.

10 www.thelancet.com/diabetes-endocrinology Published online October 12, 2016 http://dx.doi.org/10.1016/S2213-8587(16)30217-0


Series

55 Zwink N, Jenetzky E, Brenner H. Parental risk factors and anorectal 77 Sebire NJ, Jolly M, Harris JP, et al. Maternal obesity and pregnancy
malformations: systematic review and meta-analysis. outcome: a study of 287 213 pregnancies in London.
Orphanet J Rare Dis 2011; 6: 25. Int J Obes Relat Metab Disord 2001; 25: 1175–82.
56 Correa A, Marcinkevage J. Prepregnancy obesity and the risk of 78 Heslehurst N, Simpson H, Ells LJ, et al. The impact of maternal
birth defects: an update. Nutr Rev 2013; 71 (suppl 1): S68–77. BMI status on pregnancy outcomes with immediate short-term
57 Yu Z, Han S, Zhu J, Sun X, Ji C, Guo X. Pre-pregnancy body mass obstetric resource implications: a meta-analysis. Obes Rev 2008;
index in relation to infant birth weight and offspring 9: 635–83.
overweight/obesity: a systematic review and meta-analysis. 79 Usha Kiran TS, Hemmadi S, Bethel J, Evans J. Outcome of
PLoS One 2013; 8: e61627. pregnancy in a woman with an increased body mass index. BJOG
58 Kim SS, Zhu Y, Grantz KL, et al. Obstetric and neonatal risks 2005; 112: 768–72.
among obese women without chronic disease. Obstet Gynecol 2016; 80 Oteng-Ntim E, Doyle P. Maternal outcomes in obese pregnancies.
128: 104–12. In: Gillman MW, Poston L, eds. Maternal obesity. Cambridge, UK:
59 Sewell MF, Huston-Presley L, Super DM, Catalano P. Cambridge University Press, 2012: 35–44.
Increased neonatal fat mass, not lean body mass, is associated with 81 Gould JB, Mayo J, Shaw GM, Stevenson DK, for the March
maternal obesity. Am J Obstet Gynecol 2006; 195: 1100–03. of Dimes Prematurity Research Center at Stanford
60 McDonald SD, Han Z, Mulla S, Beyene J, Knowledge Synthesis G. University School of Medicine. Swedish and American studies
Overweight and obesity in mothers and risk of preterm birth and show that initiatives to decrease maternal obesity could play a
low birth weight infants: systematic review and meta-analyses. BMJ key role in reducing preterm birth. Acta Paediatr 2014;
2010; 341: c3428. 103: 586–91.
61 Radulescu L, Munteanu O, Popa F, Cirstoiu M. The implications 82 Luppino FS, de Wit LM, Bouvy PF, et al. Overweight, obesity, and
and consequences of maternal obesity on fetal intrauterine growth depression: a systematic review and meta-analysis of longitudinal
restriction. J Med Life 2013; 6: 292–98. studies. Arch Gen Psychiatry 2010; 67: 220–29.
62 Oken E. Secular trends in birthweight. Nestle Nutr Inst Workshop Ser 83 Molyneaux E, Poston L, Ashurst-Williams S, Howard LM.
2013; 71: 103–14. Obesity and mental disorders during pregnancy and postpartum:
63 [United States] Centers for Disease Control and Prevention National a systematic review and meta-analysis. Obstet Gynecol 2014;
Vital Statistics System Birth Data. http://www.cdc.gov/nchs/births. 123: 857–67.
htm (accessed May 4, 2016). 84 Grote NK, Bridge JA, Gavin AR, Melville JL, Iyengar S, Katon WJ.
64 Poston L, Bell R, Croker H, et al. Effect of a behavioural A meta-analysis of depression during pregnancy and the risk of
intervention in obese pregnant women (the UPBEAT study): preterm birth, low birth weight, and intrauterine growth restriction.
a multicentre, randomised controlled trial. Arch Gen Psychiatry 2010; 67: 1012–24.
Lancet Diabetes Endocrinol 2015; 3: 767–77. 85 Amir LH, Donath S. A systematic review of maternal obesity and
65 Dabelea D, Snell-Bergeon JK, Hartsfield CL, et al. breastfeeding intention, initiation and duration.
Increasing prevalence of gestational diabetes mellitus (GDM) over BMC Pregnancy Childbirth 2007; 7: 9.
time and by birth cohort: Kaiser Permanente of Colorado GDM 86 Turcksin R, Bel S, Galjaard S, Devlieger R. Maternal obesity and
Screening Program. Diabetes Care 2005; 28: 579–84. breastfeeding intention, initiation, intensity and duration:
66 Goldenberg RL, McClure EM, Harrison MS, Miodovnik M. a systematic review. Matern Child Nutr 2014; 10: 166–83.
Diabetes during pregnancy in low- and middle-income countries. 87 Nommsen-Rivers LA, Chantry CJ, Peerson JM, Cohen RJ,
Am J Perinatol 2016; published online May 16. Dewey KG. Delayed onset of lactogenesis among first-time
DOI:0.1055/s-0036-1584152. mothers is related to maternal obesity and factors associated
67 Jiwani A, Marseille E, Lohse N, Damm P, Hod M, Kahn JG. with ineffective breastfeeding. Am J Clin Nutr 2010; 92: 574–84.
Gestational diabetes mellitus: results from a survey of country 88 Ahluwalia IB, Li R, Morrow B. Breastfeeding practices:
prevalence and practices. J Matern Fetal Neonatal Med 2012; does method of delivery matter? Matern Child Health J 2012;
25: 600–10. 16 (suppl 2): 231–37.
68 Rahman MM, Abe SK, Kanda M, et al. Maternal body mass index 89 Walker M. Influence of the maternal anatomy and physiology on
and risk of birth and maternal health outcomes in low- and lactation. In: Breastfeeding management for the clinician; using
middle-income countries: a systematic review and meta-analysis. the evidence. Sudbury, MA: Jones and Bartlett Publishers,
Obes Rev 2015; 16: 758–70. 2006: 51–82.
69 Huda SS, Forrest R, Paterson N, Jordan F, Sattar N, Freeman DJ. 90 Barnes J, Stein A, Smith T, Pollock JI. Extreme attitudes to body
In preeclampsia, maternal third trimester subcutaneous adipocyte shape, social and psychological factors and a reluctance to breast
lipolysis is more resistant to suppression by insulin than in healthy feed. ALSPAC Study Team. Avon Longitudinal Study of Pregnancy
pregnancy. Hypertension 2014; 63: 1094–101. and Childhood. J R Soc Med 1997; 90: 551–59.
70 Salihu HM, De La Cruz C, Rahman S, August EM. Does maternal 91 Cnattingius S, Villamor E. Weight change between successive
obesity cause preeclampsia? A systematic review of the evidence. pregnancies and risks of stillbirth and infant mortality:
Minerva Ginecol 2012; 64: 259–80. a nationwide cohort study. Lancet 2015; 387: 558–65.
71 Wang Z, Wang P, Liu H, et al. Maternal adiposity as an independent 92 Villamor E, Sparen P, Cnattingius S. Risk of oral clefts in relation to
risk factor for pre-eclampsia: a meta-analysis of prospective cohort prepregnancy weight change and interpregnancy interval.
studies. Obes Rev 2013; 14: 508–21. Am J Epidemiol 2008; 167: 1305–11.
72 Ananth CV, Keyes KM, Wapner RJ. Pre-eclampsia rates in the 93 Jain AP, Gavard JA, Rice JJ, Catanzaro RB, Artal R, Hopkins SA.
United States, 1980–2010: age-period-cohort analysis. BMJ 2013; The impact of interpregnancy weight change on birthweight in
347: f6564. obese women. Am J Obstet Gynecol 2013; 208: 205.e1–7.
73 Morgan ES, Wilson E, Watkins T, Gao F, Hunt BJ. Maternal 94 Ehrlich SF, Hedderson MM, Feng J, Davenport ER, Gunderson EP,
obesity and venous thromboembolism. Int J Obstet Anesth 2012; Ferrara A. Change in body mass index between pregnancies and the
21: 253–63. risk of gestational diabetes in a second pregnancy. Obstet Gynecol
74 Poobalan AS, Aucott LS, Gurung T, Smith WC, Bhattacharya S. 2011; 117: 1323–30.
Obesity as an independent risk factor for elective and 95 Mostello D, Jen Chang J, Allen J, Luehr L, Shyken J, Leet T.
emergency caesarean delivery in nulliparous women—systematic Recurrent preeclampsia: the effect of weight change between
review and meta-analysis of cohort studies. Obes Rev 2009; pregnancies. Obstet Gynecol 2010; 116: 667–72.
10: 28–35. 96 Paramsothy P, Lin YS, Kernic MA, Foster-Schubert KE.
75 Betran AP, Ye J, Moller AB, Zhang J, Gulmezoglu AM, Torloni MR. Interpregnancy weight gain and cesarean delivery risk in women with
The increasing trend in caesarean section rates: global, regional and a history of gestational diabetes. Obstet Gynecol 2009; 113: 817–23.
national estimates: 1990–2014. PLoS One 2016; 11: e0148343. 97 Callegari LS, Sterling LA, Zelek ST, Hawes SE, Reed SD.
76 Bernardi JR, Pinheiro TV, Mueller NT, et al. Cesarean delivery and Interpregnancy body mass index change and success of term
metabolic risk factors in young adults: a Brazilian birth cohort vaginal birth after cesarean delivery. Am J Obstet Gynecol 2014;
study. Am J Clin Nutr 2015; 102: 295–301. 210: 330.e1–7.

www.thelancet.com/diabetes-endocrinology Published online October 12, 2016 http://dx.doi.org/10.1016/S2213-8587(16)30217-0 11


Series

98 Bogaerts A, Van den Bergh BR, Ameye L, et al. Interpregnancy 113 Ma RCW, Schmidt MI, Tam WH, McIntyre HD, Catalano PM.
weight change and risk for adverse perinatal outcome. Clinical management of pregnancy in the obese mother: before
Obstet Gynecol 2013; 122: 999–1009. conception, during pregnancy, and post partum. Lancet Diabetes
99 Bogaerts A, Devlieger R, Van den Bergh BR, Witters I. Obesity and Endocrinol 2016; published online Oct 12. http://dx.doi.org/10.1016/
pregnancy, an epidemiological and intervention study from a S2213-8587(16)30278-9.
psychosocial perspective. Facts Views Vis Obgyn 2014; 6: 81–95. 114 Soltani H, Fraser RB. A longitudinal study of maternal
100 Villamor E, Cnattingius S. Interpregnancy weight change and risk anthropometric changes in normal weight, overweight and obese
of adverse pregnancy outcomes: a population-based study. Lancet women during pregnancy and postpartum. Br J Nutr 2000;
2006; 368: 1164–70. 84: 95–101.
101 Whiteman VE, Aliyu MH, August EM, et al. Changes in 115 Kew S, Ye C, Hanley AJ, et al. Cardiometabolic implications of
prepregnancy body mass index between pregnancies and risk of postpartum weight changes in the first year after delivery.
gestational and type 2 diabetes. Arch Gynecol Obstet 2011; Diabetes Care 2014; 37: 1998–2006.
284: 235–40. 116 Lewis CE, Funkhouser E, Raczynski JM, Sidney S, Bild DE,
102 Whiteman VE, McIntosh C, Rao K, Mbah AK, Salihu HM. Howard BV. Adverse effect of pregnancy on high density lipoprotein
Interpregnancy BMI change and risk of primary caesarean delivery. (HDL) cholesterol in young adult women. The CARDIA Study.
J Obstet Gynaecol 2011; 31: 589–93. Coronary Artery Risk Development in Young Adults.
103 Whiteman VE, Rao K, Duan J, Alio A, Marty PJ, Salihu HM. Am J Epidemiol 1996; 144: 247–54.
Changes in prepregnancy body mass index between pregnancies 117 Gunderson EP, Lewis CE, Murtaugh MA, Quesenberry CP,
and risk of preterm phenotypes. Am J Perinatol 2011; 28: 67–74. Smith West D, Sidney S. Long-term plasma lipid changes associated
104 Blanco R, Colombo A, Suazo J. Maternal obesity is a risk factor for with a first birth: the Coronary Artery Risk Development in Young
orofacial clefts: a meta-analysis. Br J Oral Maxillofac Surg 2015; Adults study. Am J Epidemiol 2004; 159: 1028–39.
53: 699–704. 118 Fraser A, Tilling K, Macdonald-Wallis C, et al. Associations of
105 Whiteman VE, Crisan L, McIntosh C, et al. Interpregnancy body gestational weight gain with maternal body mass index, waist
mass index changes and risk of stillbirth. Gynecol Obstet Invest 2011; circumference, and blood pressure measured 16 y after pregnancy:
72: 192–95. the Avon Longitudinal Study of Parents and Children (ALSPAC).
Am J Clin Nutr 2011; 93: 1285–92.
106 Gunderson EP. Childbearing and obesity in women: weight before,
during, and after pregnancy. Obstet Gynecol Clin North Am 2009; 119 National Collaborating Centre for Women’s and Children’s Health
36: 317–32. (UK). Hypertension in pregnancy: the management of hypertensive
disorders during pregnancy: National Institute for Health and Care
107 Smith DE, Lewis CE, Caveny JL, Perkins LL, Burke GL, Bild DE.
Excellence (NICE) clinical guidelines, No. 107. London: Royal
Longitudinal changes in adiposity associated with pregnancy.
College of Obstetricians and Gynecologists, 2010.
The CARDIA Study. Coronary Artery Risk Development in Young
Adults Study. JAMA 1994; 271: 1747–51. 120 Davis EF, Lazdam M, Lewandowski AJ, et al. Cardiovascular risk
factors in children and young adults born to preeclamptic
108 Williamson DF, Madans J, Pamuk E, Flegal KM, Kendrick JS,
pregnancies: a systematic review. Pediatrics 2012; 129: e1552–61.
Serdula MK. A prospective study of childbearing and 10-year weight
gain in US white women 25 to 45 years of age. 121 Catalano P, deMouzon SH. Maternal obesity and metabolic risk to
Int J Obes Relat Metab Disord 1994; 18: 561–69. the offspring: why lifestyle interventions may have not achieved the
desired outcomes. Int J Obes (Lond) 2015; 39: 642–49.
109 Kim C. Maternal outcomes and follow-up after gestational diabetes
mellitus. Diabet Med 2014; 31: 292–301. 122 Opray N, Grivell RM, Deussen AR, Dodd JM.
Directed preconception health programs and interventions for
110 Catalano PM. Obesity, insulin resistance, and pregnancy outcome.
improving pregnancy outcomes for women who are overweight or
Reproduction 2010; 140: 365–71.
obese. Cochrane Database Syst Rev 2015; 7: CD010932.
111 Kim C, Newton KM, Knopp RH. Gestational diabetes and the
incidence of type 2 diabetes: a systematic review. Diabetes Care 2002;
25: 1862–68.
112 Rayanagoudar G, Hashi AA, Zamora J, Khan KS, Hitman GA,
Thangaratinam S. Quantification of the type 2 diabetes risk in
women with gestational diabetes: a systematic review and
meta-analysis of 95 750 women. Diabetologia 2016; 59: 1403–11.

12 www.thelancet.com/diabetes-endocrinology Published online October 12, 2016 http://dx.doi.org/10.1016/S2213-8587(16)30217-0

You might also like