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Adipokines in Early and Mid-Pregnancy and Subsequent Risk of Gestational Diabetes

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Adipokines in Early and Mid-Pregnancy and Subsequent Risk of Gestational Diabetes Epidemiology/Health Services Research BMJ Open Diab Res Care: first published as 10.1136/bmjdrc-2020-001333 on 2 August 2020. Downloaded from Open access Original research Adipokines in early and mid-pregnancy and subsequent risk of gestational diabetes: a longitudinal study in a multiracial cohort Ellen C Francis ,1,2 Mengying Li ,2 Stefanie N Hinkle,2 Yaqi Cao,3 Jinbo Chen,3 Jing Wu,4 Yeyi Zhu,5,6 Haiming Cao,7 Karen Kemper,8 Lior Rennert,8 Joel Williams,8 Michael Y Tsai,9 Liwei Chen,10 Cuilin Zhang2 To cite: Francis EC, Li M, ABSTRACT Hinkle SN, et al. Adipokines in Introduction Several adipokines are implicated in the Significance of this study early and mid- pregnancy and pathophysiology of gestational diabetes mellitus (GDM), subsequent risk of gestational however, longitudinal data in early pregnancy on many What is already known about this subject? diabetes: a longitudinal adipokines are lacking. We prospectively investigated the ► Some adipokines have been implicated in the patho- study in a multiracial cohort. physiology of gestational diabetes mellitus (GDM), BMJ Open Diab Res Care association of a panel of adipokines in early and mid- pregnancy with GDM risk. however, longitudinal adipokine data beginning in 2020;8:e001333. doi:10.1136/ the first trimester of human pregnancy are lacking bmjdrc-2020-001333 Research design and methods Within the National Institute of Child Health and Human Development (NICHD) Fetal and this impedes our understanding of their associ- Growth Studies-Singletons cohort (n=2802), a panel of 10 ation with GDM risk. Additional material is ► adipokines (plasma fatty acid binding protein-4 (FABP4), What are the new findings? published online only. To view chemerin, interleukin-6 (IL-6), leptin, soluble leptin receptor please visit the journal online ► We found that as early as 10-14 gestational weeks, (sOB- R), adiponectin, omentin-1, vaspin, and retinol binding understudied adipokines such as fatty acid binding (http:// dx. doi. org/ 10. 1136/ protein-4) were measured at gestational weeks (GWs) bmjdrc- 2020- 001333). protein-4 and chemerin were significantly associat- 10–14, 15–26, 23–31, and 33–39 among 107 GDM cases ed with risk of developing GDM. (ascertained on average at GW 27) and 214 non- GDM ► Inclusion of adipokines in a predictive model im- controls. Conditional logistic regression was used to estimate Received 5 March 2020 proved the area under the curve value beyond con- Revised 7 May 2020 ORs of each adipokine and GDM, controlling for known GDM ventional risk factors and glucose. Accepted 18 May 2020 risk factors including pre- pregnancy body mass index. Adipokines were prospectively correlated with car- Results Throughout pregnancy changes in chemerin, sOB-R, ► diometabolic markers. adiponectin, and high-molecular - weight adiponectin (HMW- http://drc.bmj.com/ adiponectin) concentrations from 10–14 to 15–26 GWs How might these results change the focus of were significantly different among GDM cases compared research or clinical practice? with non- GDM controls. In early and mid- pregnancy, FABP4, ► Findings from this study have the potential to im- chemerin, IL-6 and leptin were positively associated with prove our understanding of the pathogenesis of GDM increased GDM risk. For instance, at 10–14 GWs, the OR and inform future efforts in disease prediction. comparing the highest versus lowest quartile (ORQ4–Q1) of FABP4 was 3.79 (95% CI 1.63 to 8.85). In contrast, in both on September 30, 2021 by guest. Protected copyright. early and mid-pregnanc y adiponectin (eg, ORQ4–Q1 0.14 (0.05, 0.34) during 10–14 GWs) and sOB- R (ORQ4–Q1 0.23 glucose intolerance resulting from insufficient (0.11, 0.50) during 10–14 GWs) were inversely related to insulin secretion relative to pregnancy induced GDM risk. At 10–14 GWs a model that included conventional insulin resistance,1 is associated with both GDM risk factors and FABP4, chemerin, sOB-R, and HMW- short- term and long-term adverse maternal adiponectin improved the estimated prediction (area under 2 the curve) from 0.71 (95% CI 0.66 to 0.77) to 0.77 (95% CI and offspring health outcomes. In the USA, © Author(s) (or their 0.72 to 0.82). GDM is typically screened for between 24 and employer(s)) 2020. Re- use 28 gestational weeks (GWs), leaving only the permitted under CC BY-NC. No Conclusions A panel of understudied adipokines including commercial re- use. See rights FABP4, chemerin, and sOB-R may be implicated in the third trimester for intervention or treatment. and permissions. Published pathogenesis of GDM with significant associations detected Prediagnostic markers of GDM risk in early by BMJ. approximately 10–18 weeks before typical GDM screening. pregnancy are warranted and could have patho- For numbered affiliations see physiological relevance and inform efforts into end of article. earlier diagnoses and prevention. Correspondence to INTRODUCTION Adipokines mediate crosstalk between Dr Cuilin Zhang; Gestational diabetes mellitus (GDM), a adipose tissue and key organs and tissues zhangcu@ mail. nih. gov common pregnancy complication marked by involved in glucose homeostasis, such as the BMJ Open Diab Res Care 2020;8:e001333. doi:10.1136/bmjdrc-2020-001333 1 BMJ Open Diab Res Care: first published as 10.1136/bmjdrc-2020-001333 on 2 August 2020. Downloaded from Epidemiology/Health Services Research skeletal muscle, liver, and pancreas.3 Adipokines also performed in accordance with the relevant guidelines modulate multiple pathways for insulin signaling and and regulations. secretion, lipid metabolism, inflammatory responses, and A total of 107 GDM cases were identified and matched endothelial function.3 Among women with pregnancies to 214 controls on a 1:2 ratio based on maternal age complicated by GDM, a disruption in these regulatory (±2 years), race/ethnicity, and GW of blood collection pathways is observed,4 suggesting that adipokines may (±2 weeks).17 Women were classified with GDM if their play a role in the etiology of GDM. oral glucose tolerance test results met the Carpenter- Commonly studied adipokines such as leptin and Coustan criteria of at least two diagnostic plasma glucose adiponectin have been repeatedly associated with GDM measurements at or above the defined thresholds (fasting risk, indicating their potential roles in the pathophysi- 5.3 mmol/L, 1 hour 10.0 mmol/L, 2 hours 8.6 mmol/L, ology of GDM.3 5 Accumulating data from animal and in 3 hours 7.8 mmol/L)18 19 or if medication- treated GDM vitro studies suggested that other adipokines such as fatty was reported on their medical record. acid binding protein-4 (FABP4), chemerin, soluble leptin receptor (sOB- R), omentin-1, vaspin, and retinol binding Biomarker assessment protein-4 (RBP4) are implicated in insulin signaling3 and For the blood samples collected before the diagnosis of insulin sensitivity,6 however, the lack of human prospec- GDM (10–14 and 15–26 GWs) biomarkers were assayed tive studies focused on these adipokines and GDM risk among all cases and controls. For blood samples collected with early to mid- pregnancy data have hindered our infer- at 23–31 and 33–39 GWs, biomarkers were assayed in ence into their pathophysiological relevance.7–15 Further, all cases (n=107) and one randomly selected control there is a lack of data from studies among diverse racial/ (n=107). ethnic populations, with the majority conducted among Assay method and details on coefficients of varia- Asian women.8–15 Only one study was conducted among a tions (CV) of plasma adipokines (FABP4, chemerin, diverse population, however, it included a small number IL-6, leptin, sOB-R, adiponectin, HMW-adiponectin, of women with GDM (n=48).7 omentin-1, vaspin, and RBP4), and plasma glucose In the current study, we investigated the longitu- metabolism and cardiometabolic biomarkers (ie, glucose, dinal changes in a panel of 10 adipokines (ie, FABP4, insulin, high- sensitivity c- reactive protein (hsCRP), total chemerin, IL-6, leptin, sOB-R, adiponectin and high- cholesterol, high- density lipoprotein (HDL) cholesterol, molecular- weight adiponectin (HMW- adiponectin), and triglycerides) can be found in online supplementary omentin-1, vaspin, and RBP4) throughout pregnancy, table 1. All CVs were ≤18.0%. and prospectively examined concentrations of them in Covariates early to mid- pregnancy (before the diagnosis of GDM) Maternal sociodemographic characteristics were collected in association with the risk of GDM. To better under- from detailed questionnaires at enrollment. Risk factors stand the pathophysiology of any observed association for GDM selected a priori as covariates included: family between adipokines and GDM, we further investigated history of diabetes (yes/no), nulliparity (yes/no), and the prospective correlations of levels of adipokines in 2 prepregnancy body mass index (BMI; kg/m ). Prepreg- http://drc.bmj.com/ the first trimester with second trimester levels of clinical nancy BMI was calculated based on self-reported weight cardiometabolic biomarkers (ie, glucose, insulin, and and measured height during enrollment. Self-reported lipids) prior to GDM diagnosis. prepregnancy weight was highly correlated with weight measured by study personnel during the enrollment visit (r=0.97).20 All models were adjusted for the continuous RESEARCH DESIGN AND METHODS measures of the case/control matching factors of age on September 30, 2021 by guest. Protected copyright. Study population and design and GW at blood draw, which were matched only within This study used data from a nested case-control study a range. of GDM within the prospective Eunice Kennedy Shriver National Institute of Child Health and Human Develop- Statistical analyses 16 ment (NICHD) Fetal Growth Studies-Singletons cohort Differences in participant baseline characteristics by which enrolled 2802 pregnant women between GWs 8 GDM status were assessed using mixed- effect linear and 13 from 12 US clinical centers from 2009 to 2013.
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