Clinical ScienceFirst and second trimester gestational weight gains are most strongly associated with cord blood levels of hormones at delivery important for glycemic control and somatic growth☆
Introduction
Maternal weight gain during pregnancy is an important determinant of birth outcomes. Gestational weight gain (GWG) is directly associated with birth weight for gestation length, a marker of fetal growth, which [1], [2] is directly associated with child adiposity and long term risks of cancer and cardiometabolic health [3], [4], [5]. By alteration of the intrauterine environment, the amount and the timing of weight gained during pregnancy not only influence fetal growth [6], [7], [8], [9], [10] but also may result in persistent programming of child health [6], [7], [8], [11], as has been shown previously with other intrauterine exposures such as maternal smoking and gestational diabetes mellitus [12], [13].
Early, mid, and late pregnancy GWGs have different associations with fetal growth. Greater GWG in early pregnancy represents mainly maternal fat gain and might influence placental nutrient transfer differently than later GWG, which reflects fetal and placental growth and maternal fluid expansion in addition to maternal fat gain. Late pregnancy GWG has been consistently reported to be associated with birth weight [7], [11]. In our cohort, rates of GWG in all 3 trimesters were associated with higher fetal growth, with the greatest effect of 2nd trimester GWG [6]. We have also found that greater early and mid-pregnancy weight gain predicted offspring adiposity in mid-childhood, whereas 3rd trimester GWG did not [6], similar to results from other cohorts [8].
One of the pathways by which GWG might influence offspring growth and development is through changes in the regulation of mitogenic hormones and adipokines, including insulin, the insulin-like growth factor (IGF) axis, adiponectin, and leptin. We are not aware of prior studies that examined associations of trimester-specific GWG with multiple cord blood hormones, which might predict later health. Therefore, we conducted the present study to examine the extent to which trimester-specific rates of GWG are associated with cord blood hormone levels.
Section snippets
Methods
Between 1999 and 2002 we recruited pregnant women at 8 obstetric offices of Atrius Harvard Vanguard Medical Associates, a multispecialty group practice in eastern Massachusetts [14]. Exclusion criteria included multiple gestation, inability to answer questions in English, gestational age ≥ 22 weeks at recruitment, and plans to move away from the study area before delivery. All participating women provided written informed consent, and institutional review boards reviewed and approved the project
Results
Of the 978 women included in this analysis, mean ± SD age at enrollment was 31.8 ± 5.2 years and pre-pregnancy BMI was 24.9 ± 5.5 kg/m2. At enrollment, 30% were non-white, 63% were college graduates, 45% were nulliparous, 92% were married or cohabitating, and 60% reported a household income of >$70,000 per year (Table 1). Mean ± SD 1st, 2nd and 3rd trimester GWG rates were 0.22 ± 0.22, 0.49 ± 0.19 and 0.46 ± 0.22 kg/wk. Rate of GWG for the whole pregnancy was strongly correlated with rate of GWG in the 1st
Discussion
In this prospective study of almost 1000 mother–infant pairs, we found that greater 1st trimester GWG was associated with higher insulin and c-peptide and lower adiponectin, whereas greater 2nd trimester GWG was associated with higher IGF-1, IGF-2, IGFBP-3, and leptin. 3rd trimester GWG was not associated with cord blood hormones. This pattern suggest that 1st trimester weight gain may impact glucose and insulin regulation, whereas 2nd trimester gain may impact fetal and postnatal growth.
Our
Authors' Contributions
SRS, EO, and MWG contributed to the conception and design of the study; SRS, CM, MWG, and EO contributed to the acquisition of the data; SRS, AF, MFH, CM, MWG, and EO and contributed to the interpretation of the data; SRS performed statistical analyses; SRS drafted the manuscript; SRS has primary responsibility for the final content. All authors have read, critically revised, and approved the final manuscript.
Funding
Project Viva is supported by the National Institutes of Health (R01HD034568). Dr. Oken is additionally supported by K24 HD069408 and P30 DK092924. Dr. Fleisch is additionally supported by K23ES024803. Dr. Mantzoros is additionally supported by K24 DK081913.
Conflicts of Interest
None.
References (40)
- et al.
Role of the prenatal environment in the development of obesity
J Pediatr
(1998) - et al.
Timing of excessive weight gain during pregnancy modulates newborn anthropometry
J Obstet Gynaecol Can
(2016) - et al.
Gestational glucose tolerance and cord blood leptin levels predict slower weight gain in early infancy
J Pediatr
(2011) - et al.
Serum adiponectin in young adults—interactions with central adiposity, circulating levels of glucose, and insulin resistance: the CARDIA study
Ann Epidemiol
(2004) - et al.
A prospective study of maternal prenatal weight and offspring cardiometabolic health in mid-childhood
Ann Epidemiol
(2014) - et al.
Growth and development of human adipose tissue during early gestation
Early Hum Dev
(1983) - et al.
IGF2: epigenetic regulation and role in development and disease
Cytokine Growth Factor Rev
(2008) The National Academies Collection: reports funded by National Institutes of Health
- et al.
Point of diminishing returns: when does gestational weight gain cease benefiting birthweight and begin adding to maternal obesity?
J Matern Fetal Med
(1996) - et al.
Fetal origins of obesity
Obes Res
(2003)
Gestational weight gain and child adiposity at age 3 years
Am J Obstet Gynecol
Greater early and mid-pregnancy gestational weight gains are associated with excess adiposity in mid-childhood
Obesity (Silver Spring)
Trimester of maternal gestational weight gain and offspring body weight at birth and age five
Matern Child Health J
Trimester-specific gestational weight gain and infant size for gestational age
PLoS One
Associations of maternal prepregnancy body mass index and gestational weight gain with cardio-metabolic risk factors in adolescent offspring: a prospective cohort study
BJOG
Associations of maternal prenatal smoking with child adiposity and blood pressure
Obes Res
Intrauterine exposure to diabetes conveys risks for type 2 diabetes and obesity: a study of discordant sibships
Diabetes
Cohort profile: project viva
Int J Epidemiol
Associations of maternal material hardships during childhood and adulthood with prepregnancy weight, gestational weight gain, and postpartum weight retention
J Womens Health (Larchmt)
Cited by (39)
Cord blood Per- and polyfluoroalkyl substances, placental steroidogenic enzyme, and cord blood reproductive hormone
2019, Environment InternationalCitation Excerpt :The standardized coefficient (β) and its 95% confidence interval (95% CI) were estimated from multi-variable linear regression models for the associations of cord blood PFASs with reproductive hormones and steroidogenic enzymes. When we assessed the relationships between exposure to PFASs and reproductive hormones, we included confounders for these analyses if they were related to reproductive development (Adamcova et al., 2018; Cantarutti et al., 2017; Fleisch et al., 2017; Itoh et al., 2016; Lassance et al., 2015; Maisonet et al., 2015; Procianoy and de Oliveira-Filho, 1996; Rifas-Shiman et al., 2017; Vested et al., 2013) in the literature and associated (p < 0.15) with either of the reproductive hormone (i.e. maternal age, pre-pregnancy BMI, gestational age, infant gender, mode of delivery, passive smoking during pregnancy, and household income level), or consistently associated with reproductive development (Jarvela et al., 2012; Rohrmann et al., 2009) in the literature even if not in our data [i.e. parity]. However, few epidemiological studies have investigated the associations of exposure to PFASs and placental steroidogenic enzymes.
Circulating maternal and umbilical cord steroid hormone and insulin-like growth factor concentrations in twin and singleton pregnancies
2019, Journal of Developmental Origins of Health and DiseaseRecent Insights and Recommendations for Preventing Excessive Gestational Weight Gain
2024, Journal of Clinical Medicine
- ☆
The views expressed in this article do not necessarily represent the views of the US Government, the Department of Health and Human Services or the National Institutes of Health.