Semin Reprod Med 2021; 39(03/04): 111-132
DOI: 10.1055/s-0041-1732365
Review Article

Metabolic Conditions Including Obesity, Diabetes, and Polycystic Ovary Syndrome: Implications for Breastfeeding and Breastmilk Composition

1   Monash Centre for Health Research and Implementation (MCHRI), School of Public Health and Preventive Medicine, Monash University, Victoria, Australia
2   Department of Diabetes, Monash Health, Melbourne, Australia
,
Aya Mousa
1   Monash Centre for Health Research and Implementation (MCHRI), School of Public Health and Preventive Medicine, Monash University, Victoria, Australia
,
Anju Joham
1   Monash Centre for Health Research and Implementation (MCHRI), School of Public Health and Preventive Medicine, Monash University, Victoria, Australia
2   Department of Diabetes, Monash Health, Melbourne, Australia
,
1   Monash Centre for Health Research and Implementation (MCHRI), School of Public Health and Preventive Medicine, Monash University, Victoria, Australia
2   Department of Diabetes, Monash Health, Melbourne, Australia
› Institutsangaben
Funding and Support This work received no specific external funding. K.R. is supported by an emerging researcher fellowship from Monash Health and a postgraduate research scholarship from the National Health and Medical Research Council (NHMRC) of Australia. A.M. is supported by a biomedical research fellowship from the NHMRC A.J. is supported by an NHMRC CRE fellowship. H.J.T. is a NHMRC Medical Research Future Fund (MRFF) practitioner fellow.

Abstract

Breastfeeding is internationally recognized as the recommended standard for infant nutrition, informed by evidence of its multiple benefits for both mother and baby. In the context of common metabolic conditions such as polycystic ovary syndrome, diabetes (type 1, type 2, and gestational), and obesity, breastfeeding may be particularly beneficial for both mother and infant. However, there is evidence of delayed lactogenesis and reduced breastfeeding rates and duration in women with these conditions, and the effects of altered maternal metabolic environments on breastmilk composition (and potentially infant outcomes) are incompletely understood. In this review, we explore the relationships between maternal metabolic conditions, lactogenesis, breastfeeding, and breastmilk composition. We examine relevant potential mechanisms, including the central role of insulin both in lactogenesis and as a milk-borne hormone. We also describe the bioactive and hormonal components of breastmilk and how these may link maternal and infant health.

Authors' Contributions

K.R. reviewed and synthesized the literature, wrote the first draft of the manuscript, and revised and edited the manuscript. A.M., A.J., and H.J.T. reviewed and edited the manuscript. All authors contributed substantial intellectual input to the manuscript in line with ICMJE criteria for authorship and approved the final version for publication.




Publikationsverlauf

Artikel online veröffentlicht:
25. August 2021

© 2021. Thieme. All rights reserved.

Thieme Medical Publishers, Inc.
333 Seventh Avenue, 18th Floor, New York, NY 10001, USA

 
  • References

  • 1 Peila C, Gazzolo D, Bertino E, Cresi F, Coscia A. Influence of diabetes during pregnancy on human milk composition. Nutrients 2020; 12 (01) 12
  • 2 Smith CJ, Ryckman KK. Epigenetic and developmental influences on the risk of obesity, diabetes, and metabolic syndrome. Diabetes Metab Syndr Obes 2015; 8: 295-302
  • 3 Grummer-Strawn LM, Mei Z. Centers for Disease Control and Prevention Pediatric Nutrition Surveillance System. Does breastfeeding protect against pediatric overweight? Analysis of longitudinal data from the Centers for Disease Control and Prevention Pediatric Nutrition Surveillance System. Pediatrics 2004; 113 (02) e81-e86
  • 4 WHO Guidelines Approved by the Guidelines Review Committee. Guideline: Counselling of Women to Improve Breastfeeding Practices. Geneva: World Health Organization; 2018
  • 5 Kramer MS, Kakuma R. The optimal duration of exclusive breastfeeding: a systematic review. Adv Exp Med Biol 2004; 554: 63-77
  • 6 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-e
  • 7 Torloni MR, Betrán AP, Horta BL. et al. Prepregnancy BMI and the risk of gestational diabetes: a systematic review of the literature with meta-analysis. Obes Rev 2009; 10 (02) 194-203
  • 8 Joham AE, Nanayakkara N, Ranasinha S. et al. Obesity, polycystic ovary syndrome and breastfeeding: an observational study. Acta Obstet Gynecol Scand 2016; 95 (04) 458-466
  • 9 Thong EP, Codner E, Laven JSE, Teede H. Diabetes: a metabolic and reproductive disorder in women. Lancet Diabetes Endocrinol 2020; 8 (02) 134-149
  • 10 Nommsen-Rivers LA. Does insulin explain the relation between maternal obesity and poor lactation outcomes? An overview of the literature. Adv Nutr 2016; 7 (02) 407-414
  • 11 Achong N, Duncan EL, McIntyre HD, Callaway L. The physiological and glycaemic changes in breastfeeding women with type 1 diabetes mellitus. Diabetes Res Clin Pract 2018; 135: 93-101
  • 12 Sparud-Lundin C, Wennergren M, Elfvin A, Berg M. Breastfeeding in women with type 1 diabetes: exploration of predictive factors. Diabetes Care 2011; 34 (02) 296-301
  • 13 Nguyen PTH, Pham NM, Chu KT, Van Duong D, Van Do D. Gestational diabetes and breastfeeding outcomes: a systematic review. Asia Pac J Public Health 2019; 31 (03) 183-198
  • 14 Woo JG, Martin LJ. Does breastfeeding protect against childhood obesity? Moving beyond observational evidence. Curr Obes Rep 2015; 4 (02) 207-216
  • 15 Harder T, Bergmann R, Kallischnigg G, Plagemann A. Duration of breastfeeding and risk of overweight: a meta-analysis. Am J Epidemiol 2005; 162 (05) 397-403
  • 16 Buyken AE, Karaolis-Danckert N, Remer T, Bolzenius K, Landsberg B, Kroke A. Effects of breastfeeding on trajectories of body fat and BMI throughout childhood. Obesity (Silver Spring) 2008; 16 (02) 389-395
  • 17 Li C, Kaur H, Choi WS, Huang TT, Lee RE, Ahluwalia JS. Additive interactions of maternal prepregnancy BMI and breast-feeding on childhood overweight. Obes Res 2005; 13 (02) 362-371
  • 18 Lund-Blix NA, Dydensborg Sander S, Størdal K. et al. Infant feeding and risk of type 1 diabetes in two large Scandinavian birth cohorts. Diabetes Care 2017; 40 (07) 920-927
  • 19 Binns C, James J, Lee MK. Trends in asthma, allergy and breastfeeding in Australia. Breastfeed Rev 2013; 21 (01) 7-8
  • 20 Güngör D, Nadaud P, LaPergola CC. et al. Infant milk-feeding practices and diabetes outcomes in offspring: a systematic review. Am J Clin Nutr 2019; 109 (Suppl. 07) 817S-837S
  • 21 Owen CG, Martin RM, Whincup PH, Smith GD, Cook DG. Does breastfeeding influence risk of type 2 diabetes in later life? A quantitative analysis of published evidence. Am J Clin Nutr 2006; 84 (05) 1043-1054
  • 22 Horta BL, de Lima NP. Breastfeeding and type 2 diabetes: systematic review and meta-analysis. Curr Diab Rep 2019; 19 (01) 1
  • 23 Tahir MJ, Haapala JL, Foster LP. et al. Association of full breastfeeding duration with postpartum weight retention in a cohort of predominantly breastfeeding women. Nutrients 2019; 11 (04) 11
  • 24 Kac G, Benício MH, Velásquez-Meléndez G, Valente JG, Struchiner CJ. Breastfeeding and postpartum weight retention in a cohort of Brazilian women. Am J Clin Nutr 2004; 79 (03) 487-493
  • 25 Janney CA, Zhang D, Sowers M. Lactation and weight retention. Am J Clin Nutr 1997; 66 (05) 1116-1124
  • 26 Baker JL, Gamborg M, Heitmann BL, Lissner L, Sørensen TI, Rasmussen KM. Breastfeeding reduces postpartum weight retention. Am J Clin Nutr 2008; 88 (06) 1543-1551
  • 27 Krause KM, Lovelady CA, Peterson BL, Chowdhury N, Østbye T. Effect of breast-feeding on weight retention at 3 and 6 months postpartum: data from the North Carolina WIC Programme. Public Health Nutr 2010; 13 (12) 2019-2026
  • 28 Stuebe AM. Does breastfeeding prevent the metabolic syndrome, or does the metabolic syndrome prevent breastfeeding?. Semin Perinatol 2015; 39 (04) 290-295
  • 29 Stuebe A. Associations among lactation, maternal carbohydrate metabolism, and cardiovascular health. Clin Obstet Gynecol 2015; 58 (04) 827-839
  • 30 Aune D, Norat T, Romundstad P, Vatten LJ. Breastfeeding and the maternal risk of type 2 diabetes: a systematic review and dose-response meta-analysis of cohort studies. Nutr Metab Cardiovasc Dis 2014; 24 (02) 107-115
  • 31 Rameez RM, Sadana D, Kaur S. et al. Association of maternal lactation with diabetes and hypertension: a systematic review and meta-analysis. JAMA Netw Open 2019; 2 (10) e1913401
  • 32 Gunderson EP, Hurston SR, Ning X. et al; Study of Women, Infant Feeding and Type 2 Diabetes After GDM Pregnancy Investigators. Lactation and progression to type 2 diabetes mellitus after gestational diabetes mellitus: a prospective cohort study. Ann Intern Med 2015; 163 (12) 889-898
  • 33 Feng L, Xu Q, Hu Z, Pan H. Lactation and progression to type 2 diabetes in patients with gestational diabetes mellitus: a systematic review and meta-analysis of cohort studies. J Diabetes Investig 2018; 9 (06) 1360-1369
  • 34 Ramos-Román MA. Prolactin and lactation as modifiers of diabetes risk in gestational diabetes. Horm Metab Res 2011; 43 (09) 593-600
  • 35 Ram KT, Bobby P, Hailpern SM. et al. Duration of lactation is associated with lower prevalence of the metabolic syndrome in midlife–SWAN, the study of women's health across the nation. Am J Obstet Gynecol 2008; 198 (03) 268.e1-268.e6
  • 36 Stuebe AM, Michels KB, Willett WC, Manson JE, Rexrode K, Rich-Edwards JW. Duration of lactation and incidence of myocardial infarction in middle to late adulthood. Am J Obstet Gynecol 2009; 200 (02) 138.e1-138.e8
  • 37 Stuebe AM, Mantzoros C, Kleinman K. et al. Duration of lactation and maternal adipokines at 3 years postpartum. Diabetes 2011; 60 (04) 1277-1285
  • 38 Chowdhury R, Sinha B, Sankar MJ. et al. Breastfeeding and maternal health outcomes: a systematic review and meta-analysis. Acta Paediatrica 2015; 104: 96-113
  • 39 Sriraman NK. The nuts and bolts of breastfeeding: anatomy and physiology of lactation. Curr Probl Pediatr Adolesc Health Care 2017; 47 (12) 305-310
  • 40 Brownell E, Howard CR, Lawrence RA, Dozier AM. Delayed onset lactogenesis II predicts the cessation of any or exclusive breastfeeding. J Pediatr 2012; 161 (04) 608-614
  • 41 Nommsen-Rivers LA, Chantry CJ, Peerson JM, Cohen RJ, Dewey KG. Delayed onset of lactogenesis among first-time mothers is related to maternal obesity and factors associated with ineffective breastfeeding. Am J Clin Nutr 2010; 92 (03) 574-584
  • 42 Nommsen-Rivers LA, Dolan LM, Huang B. Timing of stage II lactogenesis is predicted by antenatal metabolic health in a cohort of primiparas. Breastfeed Med 2012; 7 (01) 43-49
  • 43 Glover AV, Berry DC, Schwartz TA, Stuebe AM. The association of metabolic dysfunction with breastfeeding outcomes in gestational diabetes. Am J Perinatol 2018; 35 (14) 1339-1345
  • 44 Neubauer SH, Ferris AM, Chase CG. et al. Delayed lactogenesis in women with insulin-dependent diabetes mellitus. Am J Clin Nutr 1993; 58 (01) 54-60
  • 45 De Bortoli J, Amir LH. Is onset of lactation delayed in women with diabetes in pregnancy? A systematic review. Diabet Med 2016; 33 (01) 17-24
  • 46 Riddle SW, Nommsen-Rivers LA. A case control study of diabetes during pregnancy and low milk supply. Breastfeed Med 2016; 11 (02) 80-855
  • 47 Gunderson EP, Hedderson MM, Chiang V. et al. Lactation intensity and postpartum maternal glucose tolerance and insulin resistance in women with recent GDM: the SWIFT cohort. Diabetes Care 2012; 35 (01) 50-56
  • 48 Rasmussen KM, Kjolhede CL. Prepregnant overweight and obesity diminish the prolactin response to suckling in the first week postpartum. Pediatrics 2004; 113 (05) e465-e471
  • 49 Ostrom KM, Ferris AM. Prolactin concentrations in serum and milk of mothers with and without insulin-dependent diabetes mellitus. Am J Clin Nutr 1993; 58 (01) 49-53
  • 50 Akre J. Infant feeding. The physiological basis. Bull World Health Organ 1989; 67 (Suppl): 1-108
  • 51 Neville MC, Webb P, Ramanathan P. et al. The insulin receptor plays an important role in secretory differentiation in the mammary gland. Am J Physiol Endocrinol Metab 2013; 305 (09) E1103-E1114
  • 52 Berlato C, Doppler W. Selective response to insulin versus insulin-like growth factor-I and -II and up-regulation of insulin receptor splice variant B in the differentiated mouse mammary epithelium. Endocrinology 2009; 150 (06) 2924-2933
  • 53 Lemay DG, Ballard OA, Hughes MA, Morrow AL, Horseman ND, Nommsen-Rivers LA. RNA sequencing of the human milk fat layer transcriptome reveals distinct gene expression profiles at three stages of lactation. PLoS One 2013; 8 (07) e67531
  • 54 Matias SL, Dewey KG, Quesenberry Jr CP, Gunderson EP. Maternal prepregnancy obesity and insulin treatment during pregnancy are independently associated with delayed lactogenesis in women with recent gestational diabetes mellitus. Am J Clin Nutr 2014; 99 (01) 115-121
  • 55 Gunderson EP. Breastfeeding after gestational diabetes pregnancy: subsequent obesity and type 2 diabetes in women and their offspring. Diabetes Care 2007; 30 (Suppl. 02) S161-S168
  • 56 Chapman T, Pincombe J, Harris M. Antenatal breast expression: a critical review of the literature. Midwifery 2013; 29 (03) 203-210
  • 57 Forster DA, McEgan K, Ford R. et al. Diabetes and antenatal milk expressing: a pilot project to inform the development of a randomised controlled trial. Midwifery 2011; 27 (02) 209-214
  • 58 Soltani H, Scott AM. Antenatal breast expression in women with diabetes: outcomes from a retrospective cohort study. Int Breastfeed J 2012; 7 (01) 18
  • 59 Forster DA, Moorhead AM, Jacobs SE. et al. Advising women with diabetes in pregnancy to express breastmilk in late pregnancy (Diabetes and Antenatal Milk Expressing [DAME]): a multicentre, unblinded, randomised controlled trial. Lancet 2017; 389 (10085): 2204-2213
  • 60 Pinheiro TV, Goldani MZ. IVAPSA Group. Maternal pre-pregnancy overweight/obesity and gestational diabetes interaction on delayed breastfeeding initiation. PloS One 2018; 13 (06) e0194879-e
  • 61 Chang YS, Glaria AA, Davie P, Beake S, Bick D. Breastfeeding experiences and support for women who are overweight or obese: a mixed-methods systematic review. Matern Child Nutr 2020; 16 (01) e12865
  • 62 Riviello C, Mello G, Jovanovic LG. Breastfeeding and the basal insulin requirement in type 1 diabetic women. Endocr Pract 2009; 15 (03) 187-193
  • 63 Stage E, Nørgård H, Damm P, Mathiesen E. Long-term breast-feeding in women with type 1 diabetes. Diabetes Care 2006; 29 (04) 771-774
  • 64 North EJ, Newman JD. Review of cardiovascular outcomes trials of sodium-glucose cotransporter-2 inhibitors and glucagon-like peptide-1 receptor agonists. Curr Opin Cardiol 2019; 34 (06) 687-692
  • 65 Andreas NJ, Kampmann B, Mehring Le-Doare K. Human breast milk: a review on its composition and bioactivity. Early Hum Dev 2015; 91 (11) 629-635
  • 66 Ballard O, Morrow AL. Human milk composition: nutrients and bioactive factors. Pediatr Clin North Am 2013; 60 (01) 49-74
  • 67 Okada M, Ohmura E, Kamiya Y. et al. Transforming growth factor (TGF)-alpha in human milk. Life Sci 1991; 48 (12) 1151-1156
  • 68 Butte NF, Garza C, Burr R, Goldman AS, Kennedy K, Kitzmiller JL. Milk composition of insulin-dependent diabetic women. J Pediatr Gastroenterol Nutr 1987; 6 (06) 936-941
  • 69 Hytten FE. Clinical and chemical studies in human lactation. BMJ 1954; 1 (4856): 249-255
  • 70 Donovan SM, Wang M, Monaco MH. et al. Noninvasive molecular fingerprinting of host-microbiome interactions in neonates. FEBS Lett 2014; 588 (22) 4112-4119
  • 71 Fields DA, Schneider CR, Pavela G. A narrative review of the associations between six bioactive components in breast milk and infant adiposity. Obesity (Silver Spring) 2016; 24 (06) 1213-1221
  • 72 Gila-Diaz A, Arribas SM, Algara A. et al. A review of bioactive factors in human breastmilk: a focus on prematurity. Nutrients 2019; 11 (06) 11
  • 73 Savino F, Fissore MF, Liguori SA, Oggero R. Can hormones contained in mothers' milk account for the beneficial effect of breast-feeding on obesity in children?. Clin Endocrinol (Oxf) 2009; 71 (06) 757-765
  • 74 Savino F, Liguori SA, Fissore MF, Oggero R. Breast milk hormones and their protective effect on obesity. Int J Pediatr Endocrinol 2009; 2009: 327505
  • 75 Kratzsch J, Bae YJ, Kiess W. Adipokines in human breast milk. Best Pract Res Clin Endocrinol Metab 2018; 32 (01) 27-38
  • 76 Payne DW, Peng LH, Pearlman WH. Corticosteroid-binding proteins in human colostrum and milk and rat milk. J Biol Chem 1976; 251 (17) 5272-5279
  • 77 Oberkotter LV, Tenore A, Pasquariello PS, Zavod W. A thyroxine-binding protein in human breast milk similar to serum thyroxine-binding globulin. J Clin Endocrinol Metab 1983; 57 (06) 1133-1139
  • 78 Hinde K, Skibiel AL, Foster AB, Del Rosso L, Mendoza SP, Capitanio JP. Cortisol in mother's milk across lactation reflects maternal life history and predicts infant temperament. Behav Ecol 2015; 26 (01) 269-281
  • 79 Hahn-Holbrook J, Le TB, Chung A, Davis EP, Glynn LM. Cortisol in human milk predicts child BMI. Obesity (Silver Spring) 2016; 24 (12) 2471-2474
  • 80 Hollanders J, Dijkstra LR, van der Voorn B. et al. No association between glucocorticoid diurnal rhythm in breastmilk and infant body composition at 3 months. Nutrients 2019; 11 (10) 2351
  • 81 Vanky E, Nordskar JJ, Leithe H, Hjorth-Hansen AK, Martinussen M, Carlsen SM. Breast size increment during pregnancy and breastfeeding in mothers with polycystic ovary syndrome: a follow-up study of a randomised controlled trial on metformin versus placebo. BJOG 2012; 119 (11) 1403-1409
  • 82 Carlsen SM, Jacobsen G, Vanky E. Mid-pregnancy androgen levels are negatively associated with breastfeeding. Acta Obstet Gynecol Scand 2010; 89 (01) 87-94
  • 83 Biggs JSG, Hacker N, Andrews E, Munro C. Bromocriptine, methyl testosterone and placebo for inhibition of physiological lactation: a controlled study. Med J Aust 1978; 2 (3, Suppl): 23-25
  • 84 Vanky E, Isaksen H, Moen MH, Carlsen SM. Breastfeeding in polycystic ovary syndrome. Acta Obstet Gynecol Scand 2008; 87 (05) 531-535
  • 85 Harrison CL, Teede HJ, Joham AE, Moran LJ. Breastfeeding and obesity in PCOS. Expert Rev Endocrinol Metab 2016; 11 (06) 449-454
  • 86 Marasco L, Marmet C, Shell E. Polycystic ovary syndrome: a connection to insufficient milk supply?. J Hum Lact 2000; 16 (02) 143-148
  • 87 Moses RG, Morris GJ, Petocz P, San Gil F, Garg D. The impact of potential new diagnostic criteria on the prevalence of gestational diabetes mellitus in Australia. Med J Aust 2011; 194 (07) 338-340
  • 88 Manerkar K, Harding J, Conlon C, McKinlay C. Maternal gestational diabetes and infant feeding, nutrition and growth: a systematic review and meta-analysis. Br J Nutr 2020; 123 (11) 1201-1215
  • 89 Dritsakou K, Liosis G, Valsami G, Polychronopoulos E, Skouroliakou M. The impact of maternal- and neonatal-associated factors on human milk's macronutrients and energy. J Matern Fetal Neonatal Med 2017; 30 (11) 1302-1308
  • 90 Shapira D, Mandel D, Mimouni FB. et al. The effect of gestational diabetes mellitus on human milk macronutrients content. J Perinatol 2019; 39 (06) 820-823
  • 91 Kaushik S, Trivedi SS, Jain A, Bhattacharjee J. Unusual changes in colostrum composition in lactating Indian women having medical complications during pregnancy - a pilot study. Indian J Clin Biochem 2002; 17 (02) 68-73
  • 92 Ley SH, Hanley AJ, Sermer M, Zinman B, O'Connor DL. Associations of prenatal metabolic abnormalities with insulin and adiponectin concentrations in human milk. Am J Clin Nutr 2012; 95 (04) 867-874
  • 93 Yu X, Rong SS, Sun X. et al. Associations of breast milk adiponectin, leptin, insulin and ghrelin with maternal characteristics and early infant growth: a longitudinal study. Br J Nutr 2018; 120 (12) 1380-1387
  • 94 Aydin S, Geckil H, Karatas F. et al. Milk and blood ghrelin level in diabetics. Nutrition 2007; 23 (11-12): 807-811
  • 95 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 (12) 2236-2240
  • 96 Nunes M, da Silva CH, Bosa VL, Bernardi JR, Werlang ICR, Goldani MZ. NESCA Group. 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 (01) 410
  • 97 Andreas NJ, Hyde MJ, Gale C. et al. Effect of maternal body mass index on hormones in breast milk: a systematic review. PLoS One 2014; 9 (12) e115043
  • 98 Finkelstein SA, Keely E, Feig DS, Tu X, Yasseen III AS, Walker M. Breastfeeding in women with diabetes: lower rates despite greater rewards. A population-based study. Diabet Med 2013; 30 (09) 1094-1101
  • 99 Oza-Frank R, Chertok I, Bartley A. Differences in breast-feeding initiation and continuation by maternal diabetes status. Public Health Nutr 2015; 18 (04) 727-735
  • 100 Simmons D, Conroy C, Thompson CF. In-hospital breast feeding rates among women with gestational diabetes and pregestational Type 2 diabetes in South Auckland. Diabet Med 2005; 22 (02) 177-181
  • 101 Longmore DK, Barr ELM, Wilson AN. et al. Associations of gestational diabetes and type 2 diabetes during pregnancy with breastfeeding at hospital discharge and up to 6 months: the PANDORA study. Diabetologia 2020; 63 (12) 2571-2581
  • 102 Whitmore TJ, Trengove NJ, Graham DF, Hartmann PE. Analysis of insulin in human breast milk in mothers with type 1 and type 2 diabetes mellitus. Int J Endocrinol 2012; 2012: 296368
  • 103 Chiang JL, Kirkman MS, Laffel LMB, Peters AL. Type 1 Diabetes Sourcebook Authors. Type 1 diabetes through the life span: a position statement of the American Diabetes Association. Diabetes Care 2014; 37 (07) 2034-2054
  • 104 Ludvigsson JF, Neovius M, Söderling J. et al. Maternal glycemic control in type 1 diabetes and the risk for preterm birth: a population-based cohort study. Ann Intern Med 2019; 170 (10) 691-701
  • 105 Arthur PG, Smith M, Hartmann PE. Milk lactose, citrate, and glucose as markers of lactogenesis in normal and diabetic women. J Pediatr Gastroenterol Nutr 1989; 9 (04) 488-496
  • 106 Larinkari J, Laatikainen L, Ranta T, Mörönen P, Pesonen K, Laatikainen T. Metabolic control and serum hormone levels in relation to retinopathy in diabetic pregnancy. Diabetologia 1982; 22 (05) 327-332
  • 107 Botta RM, Donatelli M, Bucalo ML, Bellomonte ML, Bompiani GD. Placental lactogen, progesterone, total estriol and prolactin plasma levels in pregnant women with insulin-dependent diabetes mellitus. Eur J Obstet Gynecol Reprod Biol 1984; 16 (06) 393-401
  • 108 Gaspard U, Sandront H, Luyckx A. Glucose-insulin interaction and the modulation of human placental lactogen (HPL) secretion during pregnancy. J Obstet Gynaecol Br Commonw 1974; 81 (03) 201-209
  • 109 Neubauer SH. Lactation in insulin-dependent diabetes. Prog Food Nutr Sci 1990; 14 (04) 333-370
  • 110 Sibiak R, Jankowski M, Gutaj P, Mozdziak P, Kempisty B, Wender-Ożegowska E. Placental lactogen as a marker of maternal obesity, diabetes, and fetal growth abnormalities: current knowledge and clinical perspectives. J Clin Med 2020; 9 (04) 1142
  • 111 Sorkio S, Cuthbertson D, Bärlund S. et al; TRIGR Study Group. Breastfeeding patterns of mothers with type 1 diabetes: results from an infant feeding trial. Diabetes Metab Res Rev 2010; 26 (03) 206-211
  • 112 Hummel S, Vehik K, Uusitalo U. et al; TEDDY Study Group. Infant feeding patterns in families with a diabetes history - observations from The Environmental Determinants of Diabetes in the Young (TEDDY) birth cohort study. Public Health Nutr 2014; 17 (12) 2853-2862
  • 113 Nucci AM, Virtanen SM, Sorkio S. et al; TRIGR Investigators. Regional differences in milk and complementary feeding patterns in infants participating in an international nutritional type 1 diabetes prevention trial. Matern Child Nutr 2017; 13 (03) 13
  • 114 Bitman J, Hamosh M, Hamosh P. et al. Milk composition and volume during the onset of lactation in a diabetic mother. Am J Clin Nutr 1989; 50 (06) 1364-1369
  • 115 van Beusekom CM, Zeegers TA, Martini IA. et al. Milk of patients with tightly controlled insulin-dependent diabetes mellitus has normal macronutrient and fatty acid composition. Am J Clin Nutr 1993; 57 (06) 938-943
  • 116 Jackson MB, Lammi-Keefe CJ, Jensen RG, Couch SC, Ferris AM. Total lipid and fatty acid composition of milk from women with and without insulin-dependent diabetes mellitus. Am J Clin Nutr 1994; 60 (03) 353-361
  • 117 Lammi-Keefe CJ, Jonas CR, Ferris AM, Capacchione CM. Vitamin E in plasma and milk of lactating women with insulin-dependent diabetes mellitus. J Pediatr Gastroenterol Nutr 1995; 20 (03) 305-309
  • 118 Oliveira AM, Cunha CC, Penha-Silva N, Abdallah VO, Jorge PT. [Interference of the blood glucose control in the transition between phases I and II of lactogenesis in patients with type 1 diabetes mellitus]. Arq Bras Endocrinol Metabol 2008; 52 (03) 473-481
  • 119 Lau C, Sullivan MK, Hazelwood RL. Effects of diabetes mellitus on lactation in the rat. Proc Soc Exp Biol Med 1993; 204 (01) 81-89
  • 120 Arthur PG, Kent JC, Hartmann PE. Metabolites of lactose synthesis in milk from women during established lactation. J Pediatr Gastroenterol Nutr 1991; 13 (03) 260-266
  • 121 Jovanovic-Peterson L, Fuhrmann K, Hedden K, Walker L, Peterson CM. Maternal milk and plasma glucose and insulin levels: studies in normal and diabetic subjects. J Am Coll Nutr 1989; 8 (02) 125-131
  • 122 Martin CR, Ling P-R, Blackburn GL. Review of infant feeding: key features of breast milk and infant formula. Nutrients 2016; 8 (05) 279
  • 123 Fahrenkrog S, Harder T, Stolaczyk E. et al. Cross-fostering to diabetic rat dams affects early development of mediobasal hypothalamic nuclei regulating food intake, body weight, and metabolism. J Nutr 2004; 134 (03) 648-654
  • 124 Plagemann A, Harder T, Franke K, Kohlhoff R. Long-term impact of neonatal breast-feeding on body weight and glucose tolerance in children of diabetic mothers. Diabetes Care 2002; 25 (01) 16-22
  • 125 Plagemann A, Harder T, Kohlhoff R. et al. Impact of early neonatal breast-feeding on psychomotor and neuropsychological development in children of diabetic mothers. Diabetes Care 2005; 28 (03) 573-578
  • 126 Rodekamp E, Harder T, Kohlhoff R, Franke K, Dudenhausen JW, Plagemann A. Long-term impact of breast-feeding on body weight and glucose tolerance in children of diabetic mothers. Diabetes Care 2005; 28 (06) 1457-1462
  • 127 Rodekamp E, Harder T, Kohlhoff R, Franke K, Dudenhausen JW, Plagemann A. Long-term impact of breast-feeding on body weight and glucose tolerance in children of diabetic mothers: role of the late neonatal period and early infancy. Diabetes Care 2005; 28 (06) 1457-1462
  • 128 Plagemann A, Harder T. Fuel-mediated teratogenesis and breastfeeding. Diabetes Care 2011; 34 (03) 779-781
  • 129 Kulski JK, Hartmann PE. Milk insulin, GH and TSH: relationship to changes in milk lactose, glucose and protein during lactogenesis in women. Endocrinol Exp 1983; 17 (3-4): 317-326
  • 130 Shehadeh N, Khaesh-Goldberg E, Shamir R. et al. Insulin in human milk: postpartum changes and effect of gestational age. Arch Dis Child Fetal Neonatal Ed 2003; 88 (03) F214-F216
  • 131 Young BE, Patinkin Z, Palmer C. et al. Human milk insulin is related to maternal plasma insulin and BMI: but other components of human milk do not differ by BMI. Eur J Clin Nutr 2017; 71 (09) 1094-1100
  • 132 Ahuja S, Boylan M, Hart SL. et al. Glucose and insulin levels are increased in obese and overweight mothers breastmilk. Food Nutr Sci 2011; 2 (03) DOI: 10.4236/fns.2011.23027.
  • 133 Shehadeh N, Sukhotnik I, Shamir R. Gastrointestinal tract as a target organ for orally administered insulin. J Pediatr Gastroenterol Nutr 2006; 43 (03) 276-281
  • 134 Shulman RJ. Effect of enteral administration of insulin on intestinal development and feeding tolerance in preterm infants: a pilot study. Arch Dis Child Fetal Neonatal Ed 2002; 86 (02) F131-F133
  • 135 Sukhotnik I, Shehadeh N, Mogilner J. et al. Beneficial effects of oral insulin on intestinal recovery following ischemia-reperfusion injury in rat. J Surg Res 2005; 128 (01) 108-113
  • 136 Lucas A, Cole TJ. Breast milk and neonatal necrotising enterocolitis. Lancet 1990; 336 (8730): 1519-1523
  • 137 Ou J, Courtney CM, Steinberger AE, Tecos ME, Warner BW. Nutrition in necrotizing enterocolitis and following intestinal resection. Nutrients 2020; 12 (02) 12
  • 138 Lemas DJ, Young BE, Baker II PR. et al. Alterations in human milk leptin and insulin are associated with early changes in the infant intestinal microbiome. Am J Clin Nutr 2016; 103 (05) 1291-1300
  • 139 Adiv OE, Mandel H, Shehadeh N, Knopf C, Shen-Or Z, Shamir R. Influence of co-administration of oral insulin and docosahexaenoic acid in mice. J Nutr Biochem 2004; 15 (10) 638-643
  • 140 Fields DA, Demerath EW. Relationship of insulin, glucose, leptin, IL-6 and TNF-α in human breast milk with infant growth and body composition. Pediatr Obes 2012; 7 (04) 304-312
  • 141 Young BE, Levek C, Reynolds RM. et al. Bioactive components in human milk are differentially associated with rates of lean and fat mass deposition in infants of mothers with normal vs. elevated BMI. Pediatr Obes 2018; 13 (10) 598-606
  • 142 Tiittanen M, Paronen J, Savilahti E. et al; Finnish TRIGR Study Group. Dietary insulin as an immunogen and tolerogen. Pediatr Allergy Immunol 2006; 17 (07) 538-543
  • 143 Shehadeh N, Gelertner L, Blazer S, Perlman R, Solovachik L, Etzioni A. Importance of insulin content in infant diet: suggestion for a new infant formula. Acta Paediatr 2001; 90 (01) 93-95
  • 144 Skyler JS, Krischer JP, Wolfsdorf J. et al. Effects of oral insulin in relatives of patients with type 1 diabetes: The Diabetes Prevention Trial–Type 1. Diabetes Care 2005; 28 (05) 1068-1076
  • 145 Bagley D. Positive results announced in type 1 diabetes clinical trial of microbe-based therapy. Endocrine News 2020; ; October: 11
  • 146 Hidayat K, Zou SY, Shi BM. The influence of maternal body mass index, maternal diabetes mellitus, and maternal smoking during pregnancy on the risk of childhood-onset type 1 diabetes mellitus in the offspring: systematic review and meta-analysis of observational studies. Obes Rev 2019; 20 (08) 1106-1120
  • 147 Morceli G, França EL, Magalhães VB, Damasceno DC, Calderon IM, Honorio-França AC. Diabetes induced immunological and biochemical changes in human colostrum. Acta Paediatr 2011; 100 (04) 550-556
  • 148 Arita Y, Kihara S, Ouchi N. et al. Paradoxical decrease of an adipose-specific protein, adiponectin, in obesity. Biochem Biophys Res Commun 1999; 257 (01) 79-83
  • 149 Martin LJ, Woo JG, Geraghty SR. et al. Adiponectin is present in human milk and is associated with maternal factors. Am J Clin Nutr 2006; 83 (05) 1106-1111
  • 150 Newburg DS, Woo JG, Morrow AL. Characteristics and potential functions of human milk adiponectin. J Pediatr 2010; 156 (2, Suppl): S41-S46
  • 151 Savino F, Lupica MM, Benetti S, Petrucci E, Liguori SA, Cordero Di Montezemolo L. Adiponectin in breast milk: relation to serum adiponectin concentration in lactating mothers and their infants. Acta Paediatr 2012; 101 (10) 1058-1062
  • 152 Woo JG, Guerrero ML, Guo F. et al. Human milk adiponectin affects infant weight trajectory during the second year of life. J Pediatr Gastroenterol Nutr 2012; 54 (04) 532-539
  • 153 Luoto R, Laitinen K, Nermes M, Isolauri E. Impact of maternal probiotic-supplemented dietary counseling during pregnancy on colostrum adiponectin concentration: a prospective, randomized, placebo-controlled study. Early Hum Dev 2012; 88 (06) 339-344
  • 154 Woo JG, Guerrero ML, Altaye M. et al. Human milk adiponectin is associated with infant growth in two independent cohorts. Breastfeed Med 2009; 4 (02) 101-109
  • 155 Brunner S, Schmid D, Zang K. et al. Breast milk leptin and adiponectin in relation to infant body composition up to 2 years. Pediatr Obes 2015; 10 (01) 67-73
  • 156 Weyermann M, Brenner H, Rothenbacher D. Adipokines in human milk and risk of overweight in early childhood: a prospective cohort study. Epidemiology 2007; 18 (06) 722-729
  • 157 Anderson J, McKinley K, Onugha J, Duazo P, Chernoff M, Quinn EA. Lower levels of human milk adiponectin predict offspring weight for age: a study in a lean population of Filipinos. Matern Child Nutr 2016; 12 (04) 790-800
  • 158 Aydin S, Ozkan Y, Erman F. et al. Presence of obestatin in breast milk: relationship among obestatin, ghrelin, and leptin in lactating women. Nutrition 2008; 24 (7-8): 689-693
  • 159 Ilcol YO, Hizli B. Active and total ghrelin concentrations increase in breast milk during lactation. Acta Paediatr 2007; 96 (11) 1632-1639
  • 160 Cesur G, Ozguner F, Yilmaz N, Dundar B. The relationship between ghrelin and adiponectin levels in breast milk and infant serum and growth of infants during early postnatal life. J Physiol Sci 2012; 62 (03) 185-190
  • 161 Aydin S, Aydin S, Ozkan Y, Kumru S. Ghrelin is present in human colostrum, transitional and mature milk. Peptides 2006; 27 (04) 878-882
  • 162 Kon IY, Shilina NM, Gmoshinskaya MV, Ivanushkina TA. The study of breast milk IGF-1, leptin, ghrelin and adiponectin levels as possible reasons of high weight gain in breast-fed infants. Ann Nutr Metab 2014; 65 (04) 317-323
  • 163 Smith-Kirwin SM, O'Connor DM, De Johnston J, Lancey ED, Hassink SG, Funanage VL. Leptin expression in human mammary epithelial cells and breast milk. J Clin Endocrinol Metab 1998; 83 (05) 1810-1813
  • 164 Palou M, Picó C, Palou A. Leptin as a breast milk component for the prevention of obesity. Nutr Rev 2018; 76 (12) 875-892
  • 165 Miralles O, Sánchez J, Palou A, Picó C. A physiological role of breast milk leptin in body weight control in developing infants. Obesity (Silver Spring) 2006; 14 (08) 1371-1377
  • 166 Andreas NJ, Hyde MJ, Herbert BR. et al. Impact of maternal BMI and sampling strategy on the concentration of leptin, insulin, ghrelin and resistin in breast milk across a single feed: a longitudinal cohort study. BMJ Open 2016; 6 (07) e010778
  • 167 Chan D, Goruk S, Becker AB. et al. Adiponectin, leptin and insulin in breast milk: associations with maternal characteristics and infant body composition in the first year of life. Int J Obes 2018; 42 (01) 36-43
  • 168 Quinn EA, Largado F, Borja JB, Kuzawa CW. Maternal characteristics associated with milk leptin content in a sample of Filipino women and associations with infant weight for age. J Hum Lact 2015; 31 (02) 273-281
  • 169 Uysal FK, Onal EE, Aral YZ, Adam B, Dilmen U, Ardiçolu Y. Breast milk leptin: its relationship to maternal and infant adiposity. Clin Nutr 2002; 21 (02) 157-160