Gestational weight gain across continents and ethnicity: systematic review and meta-analysis of maternal and infant outcomes in more than one million women

Gestational weight gain (GWG) is influenced by many factors including the obesogenic environment, prepregnancy body mass index (BMI), age, parity, smoking, socioeconomic status and comorbid medical conditions [1, 2]. Excess or insufficient GWG is associated with higher risks of adverse pregnancy outcomes, including preterm birth, macrosomia and caesarean delivery [3]. The US Institute of Medicine (IOM) developed GWG guidelines in 1990 and updated them in 2009 (Table 1), yet nearly three quarters of women now gain weight outside these guidelines [4, 5]. Given that lifestyle intervention improves outcomes, meeting GWG guidelines is an important target [6]. However, the IOM guidelines are based on data from primarily USA-dwelling, Caucasian and Black women, with limited ethnic diversity that may not be applicable to women from Europe and Asia. Given that Asia is the most populous continent, inhabited by 60% of the world’s population, applicability of GWG guidelines to Asian populations is an international public health priority.

At lower BMI, people from Asia have a greater risk for cardiovascular disease and diabetes [7, 8] than Caucasians, with a higher body fat percentage and greater central obesity [9]. During pregnancy, women from Asian countries have different risk profiles than Caucasian women. Asian-American women have a higher risk of gestational diabetes mellitus (GDM), caesarean section and low birthweight babies, and a lower risk of gestational hypertension and macrosomia compared to non-Hispanic white women [10]. Amongst Asian women, Korean and Taiwanese women have greater GWG and postpartum weight retention than women from other Asian countries [11]. In this context, GWG guidelines in Asian women may need to be considered differently; however, there is insufficient comparative research to date.

The 2009 IOM guidelines, although based on limited data, showed no ethnic differences in associations between GWG and pregnancy outcomes, whilst calling for further research [4]. Currently, there are no specific GWG guidelines for women from Asia. Most Asian studies use Caucasian-derived IOM GWG guidelines, and some use their own regional guidelines [12]. This creates heterogeneity and limits comparisons across regions, underpinning calls for new ethnic-specific regional GWG guidelines in China [13], highlighting gaps in current guidelines.

In this systematic review, meta-analysis and meta-regression, we aimed to explore ethnic differences in maternal prepregnancy BMI, GWG and health outcomes across the USA, Europe and Asia. In Asia, we also aimed to explore GWG and health outcomes using ethnic-specific regional BMI and World Health Organization (WHO) BMI categories.

This systematic review and meta-analysis was conducted according to the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) protocol. This protocol was registered with the PROSPERO International Prospective Register of Systematic reviews (registration number CRD42015023325). An analysis of all pooled data is published [5]. This study focused on ethnic differences in maternal BMI, GWG and maternal and neonatal outcomes.

The methods used for study eligibility, data extraction and risk of bias have been detailed previously [5] (search terms and search strategy are discussed in Additional files 1 and 2). Briefly, observational studies published in the English language between January 1999 and February 2017, with a sample size of more than 500 women were included. Studies assessing multiple pregnancies and pregnancies in women < 18 years were excluded. Inclusion required that studies present data examining the women by prepregnancy BMI category (underweight, normal weight, overweight, obese), stratified by the total pregnancy GWG (studies using weekly GWG were excluded). The odds ratio (OR) for each outcome had to be stratified by maternal BMI and GWG. Papers that mutually adjusted for BMI and GWG were excluded.

After identifying wide variations in prepregnancy BMI and GWG categories, meaningful interpretation and meta-analysis were not possible. Relevant authors were contacted to reanalyse and present data using consistent categories. Chinese and Korean studies used ethnic-specific BMI categories (China: underweight BMI < 18.5 kg/m², normal weight 18.5–23.9 kg/m², overweight 24–28 kg/m² and obese ≥ 28 kg/m²; Korea: underweight BMI < 18.5 kg/m², normal weight 18.5–22.9 kg/m², overweight 23–25 kg/m² and obese ≥ 25 kg/m²) whilst Japanese and Taiwanese studies used WHO BMI categories (underweight < 18.5 kg/m², normal weight 18.5–24.9 kg/m², overweight 25–29.9 kg/m² and obese ≥30 kg/m²).

Primary outcomes were (1) small for gestational age (SGA): < 10th percentile of birthweight for sex and gestational age, (2) pre-term birth: spontaneous birth < 37 weeks gestation, (3) large for gestational age (LGA): > 90th percentile of birthweight for sex and gestational age. Secondary outcomes were (1) macrosomia: birthweight > 4000 g, (2) caesarean section and (3) GDM.

From 5874 studies identified by the initial search, 302 studies were selected for full text review (Fig. 1) and 261 studies were excluded, using a priori selection criteria. Forty papers grouped women by prepregnancy BMI category (underweight, normal weight, overweight, obese), stratified by the total GWG for the pregnancy. One study [23] did not initially meet inclusion criteria because ORs were not stratified by both BMI and GWG. However, through collaborations, this data was available in the required format. Where required, authors were contacted for data reanalysis, and 13 collaborated (Additional file 2).

In total, 23 cohort studies [12, 14‐21, 23‐36] were included in this systematic review and meta-analysis, reporting data on more than 1 million women (n = 1,309,136).

In this study of 1,309,136 pregnancies, we present a systematic review, meta-analysis and meta-regression incorporating women from diverse ethnicities across three continents, contemporary cohorts and from across the BMI range. We explore ethnic differences in prepregnancy BMI, prevalence of GWG outside IOM guidelines and maternal and neonatal health outcomes between women living in the USA, western Europe and east Asia. Within Asia, we compare studies applying regional and WHO BMI categories. Women in the USA and Europe have higher prepregnancy BMI, higher prevalence of GWG above guidelines and lower rates of GWG below guidelines than women in Asia. However, when applying regional BMI categories, women in Asia have similar GWG above guidelines to the other continents, but retain lower prevalence of GWG below guidelines. GWG outside guidelines is associated with adverse health outcomes across all regions. A greater percentage of women in Asia had GWG below guidelines, using WHO BMI (60%) compared to regional BMI categories (16%), yet WHO BMI was not accompanied by increased risks of adverse outcomes.

Given that Asian women have greater risks of health complications at a lower BMI, Asian countries often use lower BMI cut-offs for overweight and obese categories. However in 2004, a WHO review of relevant evidence concluded there was no clear cut-off for overweight and obesity for those of Asian ethnicity, and thus WHO did not change their current BMI guidelines [37]. They did, however, identify trigger points of > 23 kg/m² and > 27.5 kg/m², representing increased and high risks respectively for public health action. In practice, BMI categories commonly used in China [16, 26, 31] are underweight BMI < 18.5 kg/m², normal weight 18.5–23.9 kg/m², overweight 24–28 kg/m² and obese ≥28 kg/m². In Korea, the classifications are underweight BMI < 18.5 kg/m², normal weight 18.5–22.9 kg/m², overweight 23–25 kg/m² and obese ≥25 kg/m² [12, 34]. Studies from Taiwan [38, 39] and Japan used WHO BMI categories [40] despite Japanese Society of Obesity guidelines that define obesity at a BMI ≥ 25 kg/m² [41]. The European Board and College of Obstetrics and Gynaecology (EBCOG) [42] notes difficulties in accurately comparing prevalence of prepregnancy BMI groups internationally with heterogeneity of data sets. However, comparison is important across regions to inform our understanding of relationships between GWG and pregnancy outcomes. To the best of our knowledge, this is the only systematic review comparing prepregnancy BMI and exploring relationships to GWG and health outcomes across international settings. We have compared Asian studies using regional and WHO BMI categories in assessment of prepregnancy BMI, GWG and pregnancy health outcomes to explore applicability of regional and WHO BMI categories in applying IOM GWG guidelines.

Applying WHO prepregnancy BMI categories, the USA had the greatest prevalence of overweight and obesity at 43%, consistent with trends from the 2013–2014 National Health and Nutrition Examination Survey (NHANES), with 37% of reproductive-aged women obese [43]. This is significant as, preconception, a higher BMI independently increases pregnancy complications including GDM, preeclampsia, caesarean section and LGA [44, 45]. In contrast, Asia had the greatest prevalence of women in normal weight and underweight categories. A lower BMI preconception is associated with increased risks including SGA [46]. The high prevalence of prepregnancy BMI outside of the healthful range shown here highlights the critical need to focus on achieving healthy preconception weight, especially in the USA, but also across Europe and Asia.

Women in the USA and Europe had higher GWG above guidelines than women in Asia. However, in studies applying ethnic-specific regional BMI categories, women in Asia had similar rates of GWG above guidelines. The prevalence of GWG above guidelines is consistent with observational studies [47‐50]. Excess GWG increases adverse pregnancy outcomes, independent of BMI, as demonstrated here, and also increases postpartum weight retention and obesity [45, 51]. A systematic review of postpartum weight retention in Asian women found that whilst prepregnancy BMI had an impact, GWG was the most important predictor [11], supporting the clinical relevance of our findings on long-term contribution to obesity. Here we have advanced the literature to highlight the high prevalence of GWG above guidelines across the USA, Europe and Asia and show the impact of using regional BMI categories on the application of IOM guidelines.

Exploring health outcomes by GWG, we combined USA and Europe to ensure adequate numbers for meta-analysis and compared USA/Europe to Asia. Across regions, GWG below guidelines was associated with a higher risk of SGA and preterm birth, compared to GWG within guidelines. Likewise across regions, GWG above guidelines was associated with a greater risk for LGA, macrosomia and caesarean section. For women in Asia, adverse outcomes were noted applying both regional and WHO BMI categories. We were generally unable to compare differences in adverse health outcomes because ORs between regions were similar with overlapping CIs. Further research using both regional and WHO BMI categories in all studies of GWG and health outcomes may be useful. We also support the recommendations for standardisation of GWG categories and core outcome parameters to enable more accurate comparisons for future studies [42, 52].

With high prepregnancy BMI, high rates of GWG above guidelines and clear adverse health outcomes shown here across the USA, Europe and Asia, and in our pooled data analysis [5], intervention is clearly vital. The Journal of the American Medical Association editorial accompanying our recent data analysis on GWG discussed barriers to healthful lifestyle intervention during pregnancy in addressing GWG and improving health outcomes [53]. Barriers included inadequate evidence of improvement of adverse pregnancy outcomes and modest changes in GWG. Yet, the largest individual patient data (IPD) analysis of 36 randomised controlled trials in pregnancy (~ 12,000 women) [6], recently published in The BMJ, demonstrates that even modest reduction in excessive GWG improves outcomes, reducing caesarean section, preterm birth and GDM, the latter being particularly modifiable with physical activity intervention. Reported results were independent of maternal characteristics including age, BMI, parity and ethnicity, enhancing generalisability of the findings. It appears that even modest changes to lifestyle and GWG effectively reduce adverse health outcomes, affirming the need for implementation of healthful lifestyle in routine antenatal care for public health impact [54].

There may also be differences to consider within Asia. Comparing Asian studies, prepregnancy BMI was similar. Overall, 16% of Chinese women were underweight, 74% normal weight and 9% overweight and obese. These values are lower than those of recent cohort studies, where 15–28% of reproductive-aged women in China are above healthy weight [13, 47]. This contrasted with Japan, with 18%, 71% and 11% respectively. In China 53% of women gained above GWG guidelines consistent with the USA and Europe. In Japan GWG below guidelines was 64%, with only 7% above. These differences arguably occur because WHO BMI categories were applied in Japan. Differences may also relate to ethnic variation. In Singapore, difference in GWG between ethnicities was postulated to be due to difference in diet quality and psychosocial factors [55]. However we postulate that the degree of observed difference primarily related to application of BMI categories. Asian studies have already suggested the need for specific guidelines [56]. In 2000, Chinese-specific guidelines for GWG [57] were developed, but have not been commonly adopted, with most Asian studies using mainly Caucasian-derived IOM GWG guidelines [55]. A call has been made for multi-centre collaboration to create optimal GWG guidelines for Asian women using modified BMI categories [58]. Here however, we demonstrate that applying regional BMI categories generated GWG patterns and health outcomes similar to those in the USA/Europe. With regional BMI categories, apparent higher risks of macrosomia and caesarean section were demonstrated. Overall our data are reassuring for clinicians and policy makers that IOM GWG guidelines are applicable in women of Asian background, provided regional BMI categories are used, to avoid overestimation of GWG below recommendations that are not accompanied by increased risks of adverse outcomes.

Limitations of our study include the lack of cohorts from developing countries and the exclusion of non-English language articles. It did not include studies from eastern Europe and south Asian countries, which have historical and ethnic differences from adjacent western European and east Asian countries respectively, yet this is the broadest systematic review and meta-analysis performed to date. For the meta-analysis, we combined the USA and Europe into one group, due to inadequate reported outcomes. Within each study there may be heterogeneity regarding race/ethnicity, and results should not be interpreted that the sample represented the country of origin. The European and Asian studies did not provide demographic data, and we have assumed the populations in these studies to be largely homogeneous. Studies from the USA do include some women from Asia, and where reported proportions are small, reporting is inconsistent, limiting capacity to interpret the overall prevalence of Asian women in US and European studies. Preterm birth was not adjusted for gestational age, potentially resulting in less total gestational weight gain than would have been otherwise attained. Meta-analyses for GDM could not be performed due to deficiencies in the primary data sets. Heterogeneity among studies may affect the reliability of the results, although this was only relevant for the effect of GWG below guidelines in SGA and LGA in USA/Europe. Lastly, we included studies published before 2009 IOM guidelines, so treating physicians and midwives may have had different GWG targets and guidelines compared to studies from after that time.

Strengths are the inclusion of common maternal and infant risks associated with GWG below and above the IOM 2009 guidelines across the entire prepregnancy BMI spectrum, with an analysis across three continents. Notably, a quarter of the women in these studies were from Asia. This is the only systematic review that has compared Asian studies applying regional compared to WHO BMI categories. We searched four databases, performed a thorough risk of bias appraisal and sought international collaboration to facilitate reanalysis, enabling broad inclusion of data in excess of 1.3 million pregnant women. The collaboration with authors has enabled data in a more homogeneous format for meta-analysis, with unprecedented data integration and meta-analysis.

In this study of 1,309,136 pregnancies, incorporating women from diverse ethnicities, contemporary cohorts and from across the BMI range, we show that women from the USA and Europe have higher prepregnancy BMI than those from Asia (even when applying regional BMI categories). In the USA and Europe, GWG above guidelines appeared higher than in Asia and GWG below guidelines was highest in Asia. However in Asian studies applying regional BMI categories, GWG above guidelines was similar across the USA, Europe and Asia. In Asia, regional BMI categories may be more applicable than WHO BMI categories when applying IOM GWG guidelines. Across all prepregnancy BMI categories and in different ethnicities, insufficient GWG is associated with increased risk of SGA and preterm birth and excess GWG with increased risk of LGA, macrosomia and caesarean section. Risks associated with excess GWG may be higher in women from Asia. These findings have practice and policy implications. This work attests to the broad applicability of the 2009 IOM guidelines, when Asian regional BMI categories are applied. As lifestyle interventions in pregnancy increase attainment of recommended GWG and show health benefits, IOM implementation of GWG guidelines and pregnancy lifestyle interventions should be considered broadly across maternity care [59, 60].