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Carbohydrates, insulin resistance and diabetes mellitus

Human milk insulin is related to maternal plasma insulin and BMI: but other components of human milk do not differ by BMI

European Journal of Clinical Nutrition volume 71, pages 1094–1100 (2017)Cite this article

Subjects

Abstract

Background/Objectives:

The impact of maternal BMI and insulin sensitivity on bioactive components of human milk (HM) is not well understood. As the prevalence of obesity and diabetes rises, it is increasingly critical that we understand how maternal BMI and hormones associated with metabolic disease relate to concentrations of bioactive components in HM.

Subjects/Methods:

This longitudinal cohort design followed 48 breastfeeding mothers through the first four months of lactation, collecting fasting morning HM samples at 2-weeks and 1, 2, 3 and 4-months, and fasting maternal blood at 2-weeks and 4-months. Insulin, glucose, adipokines leptin and adiponectin, appetite regulating hormone ghrelin, marker of oxidative stress 8OHdG and inflammatory cytokines (IL-6, IL-8, and TNF-a) were measured in HM and maternal plasma.

Results:

A total of 26 normal weight (NW) (BMI=21.4±2.0 kg/m2) and 22 overweight/obese (OW/Ob) (BMI=30.4±4.2 kg/m2) were followed. Of all HM analytes measured, only insulin and leptin were different between groups – consistently higher in the OW/Ob group (leptin: P<0.001; insulin: P<0.03). HM insulin was 98% higher than maternal plasma insulin at 2-weeks and 32% higher at 4-months (P<0.001). Maternal fasting plasma insulin and HOMA-IR were positively related to HM insulin at 2-weeks (P<0.001, R2⩾0.38, n=31), and 4-months (P⩽0.005, R2⩾0.20, n=38).

Conclusions:

The concentrations of insulin in HM are higher than in maternal plasma and are related to maternal BMI and insulin sensitivity. With the exception of leptin, there were minimal other differences observed in HM composition across a wide range in maternal BMI.

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References

  1. Young BE, Johnson SL, Krebs NF . Biological determinants linking infant weight gain and child obesity: current knowledge and future directions. Adv Nutr 2012; 3: 675–686.

    Article  Google Scholar 

  2. Breastfeeding, AAoPSo. Breastfeeding and the use of human milk. Pediatrics 2012; 129: e827–e841.

    Article  Google Scholar 

  3. Kramer MS, Kakuma R . Optimal duration of exclusive breastfeeding. Cochrane Database Syst Rev 2012; 8: CD003517.

    Google Scholar 

  4. Owen CG, Martin RM, Whincup PH, Smith GD, Cook DG . Effect of infant feeding on the risk of obesity across the life course: a quantitative review of published evidence. Pediatrics 2005; 115: 1367–1377.

    Article  Google Scholar 

  5. Victora CG, Bahl R, Barros AJ, Franca GV, Horton S, Krasevec J et al. Breastfeeding in the 21st century: epidemiology, mechanisms, and lifelong effect. Lancet 2016; 387: 475–490.

    Article  Google Scholar 

  6. 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: 1043–1054.

    Article  CAS  Google Scholar 

  7. Horta BL, Loret de Mola C, Victora CG . Long-term consequences of breastfeeding on cholesterol, obesity, systolic blood pressure and type 2 diabetes: a systematic review and meta-analysis. Acta Paediatr 2015; 104: 30–37.

    Article  CAS  Google Scholar 

  8. 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: 362–371.

    Article  Google Scholar 

  9. 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 2008; 16: 389–395.

    Article  Google Scholar 

  10. Beyerlein A, von Kries R . Breastfeeding and body composition in children: will there ever be conclusive empirical evidence for a protective effect against overweight? Am J Clin Nutr 2011; 94 (6 Suppl), 1772S–1775SS.

    Article  CAS  Google Scholar 

  11. Barbosa L, Butte NF, Villalpando S, Wong WW, Smith EO . Maternal energy balance and lactation performance of Mesoamerindians as a function of body mass index. Am J Clin Nutr 1997; 66: 575–583.

    Article  CAS  Google Scholar 

  12. Ahuja S, Boylan M, Hart S, Roman-Shriver C, Spallholz J, Pence B et al. Glucose and Insulin Levels are Increased in Obese and Overweight Mothers' Breast-Milk. Food Nutr Sci 2011; 2: 201–206.

    CAS  Google Scholar 

  13. Andreas NJ, Hyde MJ, Gale C, Parkinson JR, Jeffries S, Holmes E et al. Effect of maternal body mass index on hormones in breast milk: a systematic review. PLoS One 2014; 9: e115043.

    Article  Google Scholar 

  14. Fields DA, Demerath EW . Relationship of insulin, glucose, leptin, IL-6 and TNF-alpha in human breast milk with infant growth and body composition. Pediatr Obes 2012; 7: 304–312.

    Article  CAS  Google Scholar 

  15. Samuel VT, Shulman GI . Mechanisms for insulin resistance: common threads and missing links. Cell 2012; 148: 852–871.

    Article  CAS  Google Scholar 

  16. Gorski JN, Dunn-Meynell AA, Hartman TG, Levin BE . Postnatal environment overrides genetic and prenatal factors influencing offspring obesity and insulin resistance. Am J Physiol Regul Integr Comp Physiol 2006; 291: R768–R778.

    Article  CAS  Google Scholar 

  17. Oben JA, Mouralidarane A, Samuelsson AM, Matthews PJ, Morgan ML, McKee C et al. Maternal obesity during pregnancy and lactation programs the development of offspring non-alcoholic fatty liver disease in mice. J Hepatol 2010; 52: 913–920.

    Article  CAS  Google Scholar 

  18. Du Y, Yang M, Lee S, Behrendt CL, Hooper LV, Saghatelian A et al. Maternal western diet causes inflammatory milk and TLR2/4-dependent neonatal toxicity. Genes Dev 2012; 26: 1306–1311.

    Article  CAS  Google Scholar 

  19. Mayer-Davis EJ, Rifas-Shiman SL, Zhou L, Hu FB, Colditz GA, Gillman MW . Breast-feeding and risk for childhood obesity: does maternal diabetes or obesity status matter? Diabetes Care 2006; 29: 2231–2237.

    Article  Google Scholar 

  20. Beyerlein A, Toschke AM, von Kries R . Breastfeeding and childhood obesity: shift of the entire BMI distribution or only the upper parts? Obesity 2008; 16: 2730–2733.

    Article  Google Scholar 

  21. Ogden CL, Carroll MD, Lawman HG, Fryar CD, Kruszon-Moran D, Kit BK et al. Trends in Obesity Prevalence Among Children and Adolescents in the United States, 1988-1994 Through 2013-2014. JAMA 2016; 315: 2292–2299.

    Article  CAS  Google Scholar 

  22. Weyermann M, Brenner H, Rothenbacher D . Adipokines in human milk and risk of overweight in early childhood: a prospective cohort study. Epidemiology 2007; 18: 722–729.

    Article  Google Scholar 

  23. Fein SB, Labiner-Wolfe J, Shealy KR, Li R, Chen J, Grummer-Strawn LM . Infant Feeding Practices Study II: study methods. Pediatrics 2008; 122 (Suppl 2), S28–S35.

    Article  Google Scholar 

  24. Lawrence RA, Lawrence RM . Breastfeeding - A Guide for the Medical Professional. Elsevier Mosby: Maryland Heights, MO, USA, 2011.

    Google Scholar 

  25. Schuster S, Hechler C, Gebauer C, Kiess W, Kratzsch J . Leptin in maternal serum and breast milk: association with infants' body weight gain in a longitudinal study over 6 months of lactation. Pediatr Res 2011; 70: 633–637.

    Article  CAS  Google Scholar 

  26. Miralles O, Sanchez J, Palou A, Pico C . A physiological role of breast milk leptin in body weight control in developing infants. Obesity 2006; 14: 1371–1377.

    Article  CAS  Google Scholar 

  27. Eilers E, Ziska T, Harder T, Plagemann A, Obladen M, Loui A . Leptin determination in colostrum and early human milk from mothers of preterm and term infants. Early Hum Dev 2011; 87: 415–419.

    Article  CAS  Google Scholar 

  28. Shehadeh N, Khaesh-Goldberg E, Shamir R, Perlman R, Sujov P, Tamir A et al. Insulin in human milk: postpartum changes and effect of gestational age. Arch Dis Child Fetal Neonatal Ed 2003; 88: F214–F216.

    Article  CAS  Google Scholar 

  29. 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: 867–874.

    Article  CAS  Google Scholar 

  30. Koldovsky O . Hormones in milk. Vitam Horm 1995; 50: 77–149.

    Article  CAS  Google Scholar 

  31. Shields BM, Knight B, Shakespeare L, Babrah J, Powell RJ, Clark PM et al. Determinants of insulin concentrations in healthy 1-week-old babies in the community: applications of a bloodspot assay. Early Hum Dev 2006; 82: 143–148.

    Article  CAS  Google Scholar 

  32. Lemas DJ, Young BE, Baker PR 2nd, Tomczik AC, Soderborg TK, Hernandez TL 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: 1291–1300.

    Article  CAS  Google Scholar 

  33. Shehadeh N, Sukhotnik I, Shamir R . Gastrointestinal tract as a target organ for orally administered insulin. J Pediatr Gastroenterol Nutr 2006; 43: 276–281.

    Article  CAS  Google Scholar 

  34. Martin LJ, Woo JG, Geraghty SR, Altaye M, Davidson BS, Banach W et al. Adiponectin is present in human milk and is associated with maternal factors. Am J Clin Nutr 2006; 83: 1106–1111.

    Article  CAS  Google Scholar 

  35. Ilcol YO, Hizli B . Active and total ghrelin concentrations increase in breast milk during lactation. Acta Paediatr 2007; 96: 1632–1639.

    Article  Google Scholar 

  36. Karatas Z, Durmus Aydogdu S, Dinleyici EC, Colak O, Dogruel N . Breastmilk ghrelin, leptin, and fat levels changing foremilk to hindmilk: is that important for self-control of feeding? Eur J Pediatr 2011; 170: 1273–1280.

    Article  CAS  Google Scholar 

  37. Savino F, Benetti S, Lupica MM, Petrucci E, Palumeri E, Cordero di Montezemolo L . Ghrelin and obestatin in infants, lactating mothers and breast milk. Horm Res Paediatr 2012; 78: 297–303.

    Article  CAS  Google Scholar 

  38. Lam PM, Mistry V, Marczylo TH, Konje JC, Evans MD, Cooke MS . Rapid measurement of 8-oxo-7,8-dihydro-2'-deoxyguanosine in human biological matrices using ultra-high-performance liquid chromatography-tandem mass spectrometry. Free Radic Biol Med 2012; 52: 2057–2063.

    Article  CAS  Google Scholar 

  39. Groer MW, Shelton MM . Exercise is associated with elevated proinflammatory cytokines in human milk. J Obstet Gynecol Neonatal Nurs 2009; 38: 35–41.

    Article  Google Scholar 

  40. Garofalo R . Cytokines in human milk. J Pediatr 2010; 156 (2 Suppl), S36–S40.

    Article  CAS  Google Scholar 

  41. Young BE, Patinkin Z, Pyle L, de la Houssaye B, Davidson B, Geraghty S et al. Markers of Oxidative Stress in Human Milk do Not Differ by Maternal BMI but are Related to Infant Growth Trajectories. Matern Child Health J 2017; e-pub ahead of print 30 January 2017; doi:10.1007/s10995-016-2243-2.

    Article  Google Scholar 

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Acknowledgements

We wish to deeply thank the mothers and infants who participated in this research. We also acknowledge Claire Westcott, BS; Catherine Chartier-Logan, MPH; Melanie Reece, PhD; and Regina Reynolds, MD for support with study execution. We would also like to thank the National Institute of Health (NIH)/NICHD F32-HD0978068 (PI: BEY); Thrasher Research Fund Early Career Award (PI: BEY); Center for Women’s Health Research at the University of Colorado Anschutz Medical Campus (PI: BEY); Colorado Clinical & Translational Sciences Institute (CCTSI) with the Development and Informatics Service Center (DISC) grant support (Colorado CTSI Grant Number NIH/NCATS UL1-TR001082; PI: BEY); NIH/NIDDK K24-DK083772 (PI: NFK); NIH/NIDDK T32-DK007658-21 (PI: NFK).

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Authors and Affiliations

  1. Department of Pediatrics, Section of Nutrition, School of Medicine, University of Colorado, Aurora, CO, USA

    B E Young, Z Patinkin, C Palmer & N F Krebs

  2. Department of Pediatrics, Section of Neonatology, School of Medicine, University of Colorado, Aurora, CO, USA

    B de la Houssaye & J E Friedman

  3. Department of Medicine, Division of Endocrinology, Metabolism, and Diabetes, School of Medicine, University of Colorado, Aurora, CO, USA

    L A Barbour, T Hernandez & J E Friedman

  4. Department of Obstetrics and Gynecology, Division of Maternal-Fetal Medicine, School of Medicine, University of Colorado, Aurora, CO, USA

    L A Barbour & T Hernandez

  5. College of Nursing, University of Colorado, Aurora, CO, USA

    T Hernandez

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Young, B., 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 71, 1094–1100 (2017). https://doi.org/10.1038/ejcn.2017.75

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