The Impact of Gestational Diabetes Mellitus on Human Milk Metabolic Hormones: A Systematic Review

Majed A Suwaydi, Xiaojie Zhou, Sharon L Perrella, Mary E Wlodek, Ching Tat Lai, Zoya Gridneva, Donna T Geddes, Majed A Suwaydi, Xiaojie Zhou, Sharon L Perrella, Mary E Wlodek, Ching Tat Lai, Zoya Gridneva, Donna T Geddes

Abstract

Gestational diabetes mellitus (GDM) is a common pregnancy complication with short- and long-term health consequences for the infant and mother. Breastfeeding is the recommended mode of feeding as it offers an opportunity to reduce the risk of GDM consequences, likely partially mediated through changes in human milk (HM) composition. This review systematically reviewed 12 identified studies that investigated the impact of GDM on concentrations of HM metabolic hormones. Meta-analysis was not possible due to significant heterogeneity in study designs and hormone measurement techniques. The risk of bias was assessed using the National Institute for Clinical Excellence (NICE) tool. The methodological qualities were medium in half of the studies, while 25% (3/12) of studies carried a high risk of bias. Significant relationships were reported between GDM and concentrations of HM ghrelin (3/3 studies), insulin (2/4), and adiponectin (2/6), which may play an integral role in infant growth and development. In conclusion, preliminary evidence suggests that GDM may alter HM metabolic hormone concentrations; however, these relationships may be limited to the early lactation stage.

Keywords: breastfeeding; gestational diabetes mellitus; human milk composition; infant; lactation; metabolic hormones; pregnancy; systematic review.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
PRISMA diagram of the studies of the systematic search and studies included. GDM, gestational diabetes mellitus; T1D, type 1 diabetes; T2D, type 2 diabetes.
Figure 2
Figure 2
Timing of human milk sample collection.
Figure 3
Figure 3
Summary of results of quantitative synthesis across stages of lactation for studies investigating differences between GDM and control group and/or relationships between GDM and concentrations of human milk hormones at different lactation stages (p < 0.05). Galante et al., 2021 combined concentration results at all time points for analysis with no time effect reported.
Figure 4
Figure 4
Risk of bias in studies assessing the relationship between concentrations of metabolic hormones in human milk and gestational diabetes mellitus using the National Institute for Clinical Excellence methodological checklist. “+, green,” low risk of bias; “×, red,” high risk of bias; “-, yellow,” unclear/medium risk of bias.

References

    1. Ballard O., Morrow A.L. Human milk composition: Nutrients and bioactive factors. Pediatr. Clin. N. Am. 2013;60:49–74. doi: 10.1016/j.pcl.2012.10.002.
    1. WHO . Indicators for Assessing Infant and Young Child Feeding Practices: Definitions and Measurement Methods. World Health Organization; Geneva, Switzerland: The United Nations Children’s Fund (UNICEF); Geneva, Switzerland: 2021.
    1. Geddes D.T., Prescott S.L. Developmental origins of health and disease: The role of human milk in preventing disease in the 21(st) century. J. Hum. Lact. 2013;29:123–127. doi: 10.1177/0890334412474371.
    1. Di Cianni G., Miccoli R., Volpe L., Lencioni C., Del Prato S. Intermediate metabolism in normal pregnancy and in gestational diabetes. Diabetes Metab. Res. Rev. 2003;19:259–270. doi: 10.1002/dmrr.390.
    1. American Diabetes Association Professional Practice Committee 2. Classification and Diagnosis of Diabetes: Standards of Medical Care in Diabetes—2022. Diabetes Care. 2021;45:S17–S38. doi: 10.2337/dc22-S002.
    1. Plows J.F., Stanley J.L., Baker P.N., Reynolds C.M., Vickers M.H. The pathophysiology of gestational diabetes mellitus. Int. J. Mol. Sci. 2018;19:3342. doi: 10.3390/ijms19113342.
    1. Gunderson E.P., Lewis C.E., Lin Y., Sorel M., Gross M., Sidney S., Jacobs D.R., Jr., Shikany J.M., Quesenberry C.P., Jr. Lactation duration and progression to diabetes in women across the childbearing years: The 30-year CARDIA study. JAMA Intern. Med. 2018;178:328–337. doi: 10.1001/jamainternmed.2017.7978.
    1. Ortega-García J.A., Kloosterman N., Alvarez L., Tobarra-Sánchez E., Cárceles-Álvarez A., Pastor-Valero R., López-Hernández F.A., Sánchez-Solis M., Claudio L. Full Breastfeeding and Obesity in Children: A Prospective Study from Birth to 6 Years. Child. Obes. 2018;14:327–337. doi: 10.1089/chi.2017.0335.
    1. Chen C., Xu X., Yan Y. Estimated global overweight and obesity burden in pregnant women based on panel data model. PLoS ONE. 2018;13:e0202183. doi: 10.1371/journal.pone.0202183.
    1. Australian Institute of Health and Welfare . Incidence of Gestational Diabetes in Australia. AIHW; Canberra, Australia: 2019.
    1. Marchi J., Berg M., Dencker A., Olander E.K., Begley C. Risks associated with obesity in pregnancy, for the mother and baby: A systematic review of reviews. Obes. Rev. 2015;16:621–638. doi: 10.1111/obr.12288.
    1. Cho N.H., Shaw J.E., Karuranga S., Huang Y., da Rocha Fernandes J.D., Ohlrogge A.W., Malanda B. IDF diabetes atlas: Global estimates of diabetes prevalence for 2017 and projections for 2045. Diabetes Res. Clin. Pr. 2018;138:271–281. doi: 10.1016/j.diabres.2018.02.023.
    1. Gridneva Z., Kugananthan S., Hepworth A.R., Tie W.J., Lai C.T., Ward L.C., Hartmann P.E., Geddes D.T. Effect of Human Milk Appetite Hormones, Macronutrients, and Infant Characteristics on Gastric Emptying and Breastfeeding Patterns of Term Fully Breastfed Infants. Nutrients. 2016;9:15. doi: 10.3390/nu9010015.
    1. Gridneva Z., Kugananthan S., Rea A., Lai C.T., Ward L.C., Murray K., Hartmann P.E., Geddes D.T. Human milk adiponectin and leptin and infant body composition over the first 12 months of lactation. Nutrients. 2018;10:1125. doi: 10.3390/nu10081125.
    1. Badillo-Suárez P.A., Rodríguez-Cruz M., Nieves-Morales X. Impact of metabolic hormones secreted in human breast milk on nutritional programming in childhood obesity. J. Mammary Gland Biol. Neoplasia. 2017;22:171–191. doi: 10.1007/s10911-017-9382-y.
    1. Savino F., Liguori S.A., Fissore M.F., Oggero R. Breast milk hormones and their protective effect on obesity. Int. J. Pediatr. Endocrinol. 2009;2009:327505. doi: 10.1186/1687-9856-2009-327505.
    1. Ross M.G., Desai M. Developmental programming of appetite/satiety. Ann. Nutr. Metab. 2014;64((Suppl. 1)):36–44. doi: 10.1159/000360508.
    1. Peila C., Gazzolo D., Bertino E., Cresi F., Coscia A. Influence of diabetes during pregnancy on human milk composition. Nutrients. 2020;12:185. doi: 10.3390/nu12010185.
    1. The EndNote Team . EndNote, EndNote 20. Clarivate; Philadelphia, PA, USA: 2013.
    1. National Institute for Health and Care Excellence. The Social Care Guidance Manual: Methodological Checklists for Cohort Studies. [(accessed on 7 July 2021)]. Available online: .
    1. Aydin S., Geckil H., Karatas F., Donder E., Kumru S., Kavak E.C., Colak R., Ozkan Y., Sahin I. Milk and blood ghrelin level in diabetics. Nutrition. 2007;23:807–811. doi: 10.1016/j.nut.2007.08.015.
    1. Aydin S. The presence of the peptides apelin, ghrelin and nesfatin-1 in the human breast milk, and the lowering of their levels in patients with gestational diabetes mellitus. Peptides. 2010;31:2236–2240. doi: 10.1016/j.peptides.2010.08.021.
    1. Ley S.H., Hanley A.J., Sermer M., Zinman B., O’Connor D.L. Associations of prenatal metabolic abnormalities with insulin and adiponectin concentrations in human milk. Am. J. Clin. Nutr. 2012;95:867–874. doi: 10.3945/ajcn.111.028431.
    1. Aydin S., Kuloglu T., Aydin S. Copeptin, adropin and irisin concentrations in breast milk and plasma of healthy women and those with gestational diabetes mellitus. Peptides. 2013;47:66–70. doi: 10.1016/j.peptides.2013.07.001.
    1. Aydin S., Celik O., Gurates B., Sahin I., Ulas M., Yilmaz M., Kalayci M., Kuloglu T., Catak Z., Aksoy A., et al. Concentrations of preptin, salusins and hepcidins in plasma and milk of lactating women with or without gestational diabetes mellitus. Peptides. 2013;49:123–130. doi: 10.1016/j.peptides.2013.09.006.
    1. Nunes M., da Silva C.H., Bosa V.L., Bernardi J.R., Werlang I.C.R., Goldani M.Z. Could a remarkable decrease in leptin and insulin levels from colostrum to mature milk contribute to early growth catch-up of SGA infants? BMC Pregnancy Childbirth. 2017;17:410. doi: 10.1186/s12884-017-1593-0.
    1. Yu X., Rong S.S., Sun X., Ding G., Wan W., Zou L., Wu S., Li M., Wang D. Associations of breast milk adiponectin, leptin, insulin and ghrelin with maternal characteristics and early infant growth: A longitudinal study. Br. J. Nutr. 2018;120:1380–1387. doi: 10.1017/S0007114518002933.
    1. Fatima S.S., Khalid E., Ladak A.A., Ali S.A. Colostrum and mature breast milk analysis of serum irisin and sterol regulatory element-binding proteins-1c in gestational diabetes mellitus. J. Matern. Fetal Neonatal Med. 2019;32:2993–2999. doi: 10.1080/14767058.2018.1454422.
    1. Ustebay S., Baykus Y., Deniz R., Ugur K., Yavuzkir S., Yardim M., Kalayci M., Çaglar M., Aydin S. Chemerin and dermcidin in human milk and their alteration in gestational diabetes. J. Hum. Lact. 2019;35:550–558. doi: 10.1177/0890334419837523.
    1. Galante L., Lagstrom H., Vickers M.H., Reynolds C.M., Rautava S., Milan A.M., Cameron-Smith D., Pundir S. Sexually dimorphic associations between maternal factors and human milk hormonal concentrations. Nutrients. 2020;12:152. doi: 10.3390/nu12010152.
    1. Galante L., Reynolds C.M., Milan A.M., Alexander T., Bloomfield F.H., Cameron-Smith D., Pundir S., Vickers M.H., Harding J., Meyer M., et al. Preterm human milk: Associations between perinatal factors and hormone concentrations throughout lactation. Pediatr. Res. 2021;89:1461–1469. doi: 10.1038/s41390-020-1069-1.
    1. Choi Y., Nagel E.M., Kharoud H., Johnson K.E., Gallagher T., Duncan K., Kharbanda E.O., Fields D.A., Gale C.A., Jacobs K., et al. Gestational diabetes mellitus is associated with differences in human milk hormone and cytokine concentrations in a fully breastfeeding united states cohort. Nutrients. 2022;14:667. doi: 10.3390/nu14030667.
    1. Iliodromiti S., Sassarini J., Kelsey T.W., Lindsay R.S., Sattar N., Nelson S.M. Accuracy of circulating adiponectin for predicting gestational diabetes: A systematic review and meta-analysis. Diabetologia. 2016;59:692–699. doi: 10.1007/s00125-015-3855-6.
    1. Howlader M., Sultana M.I., Akter F., Hossain M.M. Adiponectin gene polymorphisms associated with diabetes mellitus: A descriptive review. Heliyon. 2021;7:e07851. doi: 10.1016/j.heliyon.2021.e07851.
    1. Gomez-Diaz R.A., Gomez-Medina M.P., Ramirez-Soriano E., Lopez-Robles L., Aguilar-Salinas C.A., Saucedo R., Zarate A., Valladares-Salgado A., Wacher N.H. Lower plasma ghrelin levels are found in women with diabetes-complicated pregnancies. J. Clin. Res. Pediatr. Endocrinol. 2016;8:425–431. doi: 10.4274/jcrpe.2504.
    1. Cui L., Qiao T., Xu F., Li Z., Chen T., Su H., Chen G., Zhang L., Xu D., Zhang X. Circulating irisin levels of prenatal and postnatal patients with gestational diabetes mellitus: A systematic review and meta-analysis. Cytokine. 2020;126:154924. doi: 10.1016/j.cyto.2019.154924.
    1. Perez-Perez A., Vilarino-Garcia T., Guadix P., Duenas J.L., Sanchez-Margalet V. Leptin and nutrition in gestational diabetes. Nutrients. 2020;12:1970. doi: 10.3390/nu12071970.
    1. Maghbooli Z., Hossein-Nezhad A., Rahmani M., Shafaei A.R., Larijani B. Relationship between leptin concentration and insulin resistance. Horm. Metab. Res. 2007;39:903–907. doi: 10.1055/s-2007-992812.
    1. Casabiell X., Pineiro V., Tome M.A., Peino R., Dieguez C., Casanueva F.F. Presence of leptin in colostrum and/or breast milk from lactating mothers: A potential role in the regulation of neonatal food intake. J. Clin. Endocrinol. Metab. 1997;82:4270–4273. doi: 10.1210/jcem.82.12.4590.
    1. Kugananthan S., Gridneva Z., Lai C.T., Hepworth A.R., Mark P.J., Kakulas F., Geddes D.T. Associations between maternal body composition and appetite hormones and macronutrients in human milk. Nutrients. 2017;9:252. doi: 10.3390/nu9030252.
    1. Weyermann M., Beermann C., Brenner H., Rothenbacher D. Adiponectin and leptin in maternal serum, cord blood, and breast milk. Clin. Chem. 2006;52:2095–2102. doi: 10.1373/clinchem.2006.071019.
    1. Hassiotou F., Savigni D., Hartmann P., Geddes D. Mammary cells synthesize appetite hormones that may contribute to breastmilk (38.8) FASEB J. 2014;28:38.8. doi: 10.1096/fasebj.28.1_supplement.38.8.
    1. Andreas N.J., Hyde M.J., Gale C., Parkinson J.R.C., Jeffries S., Holmes E., Modi N. Effect of maternal body mass index on hormones in breast milk: A systematic review. PLoS ONE. 2014;9:e115043. doi: 10.1371/journal.pone.0115043.
    1. Kugananthan S., Lai C.T., Gridneva Z., Mark P.J., Geddes D.T., Kakulas F. Leptin levels are higher in whole compared to skim human milk, supporting a cellular contribution. Nutrients. 2016;8:711. doi: 10.3390/nu8110711.
    1. Mohsen A.H., Sallam S., Ramzy M.M., Hamed E.K. Investigating the Relationship between Insulin-like Growth Factor-1 (IGF-1) in diabetic mother’s breast milk and the blood serum of their babies. Electron. Physician. 2016;8:2546–2550. doi: 10.19082/2546.
    1. Ringholm L., Vestgaard M., Laugesen C.S., Juul A., Damm P., Mathiesen E.R. Pregnancy-induced increase in circulating IGF-I is associated with progression of diabetic retinopathy in women with type 1 diabetes. Growth Horm. IGF Res. 2011;21:25–30. doi: 10.1016/j.ghir.2010.12.001.
    1. Suwaydi M.A., Wlodek M.E., Lai C.T., Prosser S.A., Geddes D.T., Perrella S.L. Delayed secretory activation and low milk production in women with gestational diabetes: A case series. BMC Pregnancy Childbirth. 2022;22:350. doi: 10.1186/s12884-022-04685-0.
    1. Shah K.B., Fields D.A., Pezant N.P., Kharoud H.K., Gulati S., Jacobs K., Gale C.A., Kharbanda E.O., Nagel E.M., Demerath E.W., et al. Gestational diabetes mellitus is associated with altered abundance of exosomal MicroRNAs in human milk. Clin. Ther. 2022;44:172–185.e171. doi: 10.1016/j.clinthera.2022.01.005.
    1. Clausen T.D., Mathiesen E.R., Hansen T., Pedersen O., Jensen D.M., Lauenborg J., Damm P. High prevalence of type 2 diabetes and pre-diabetes in adult offspring of women with gestational diabetes mellitus or type 1 diabetes: The role of intrauterine hyperglycemia. Diabetes Care. 2008;31:340–346. doi: 10.2337/dc07-1596.
    1. Mayer-Davis E.J., Rifas-Shiman S.L., Zhou L., Hu F.B., Colditz G.A., Gillman M.W. Breast-feeding and risk for childhood obesity: Does maternal diabetes or obesity status matter? Diabetes Care. 2006;29:2231–2237. doi: 10.2337/dc06-0974.
    1. Schaefer-Graf U.M., Hartmann R., Pawliczak J., Passow D., Abou-Dakn M., Vetter K., Kordonouri O. Association of breast-feeding and early childhood overweight in children from mothers with gestational diabetes mellitus. Diabetes Care. 2006;29:1105–1107. doi: 10.2337/dc05-2413.
    1. Uebel K., Pusch K., Gedrich K., Schneider K.T., Hauner H., Bader B.L. Effect of maternal obesity with and without gestational diabetes on offspring subcutaneous and preperitoneal adipose tissue development from birth up to year-1. BMC Pregnancy Childbirth. 2014;14:138. doi: 10.1186/1471-2393-14-138.
    1. Suwaydi M.A., Gridneva Z., Perrella S.L., Wlodek M.E., Lai C.T., Geddes D.T. Human milk metabolic hormones: Analytical methods and current understanding. Int. J. Mol. Sci. 2021;22:8708. doi: 10.3390/ijms22168708.

Source: PubMed

Sponsorzy i współpracownicy

Warunki medyczne

Interwencje lekowe

3
Subskrybuj