Effect of maternal body mass index on hormones in breast milk: a systematic review

Nicholas J Andreas, Matthew J Hyde, Chris Gale, James R C Parkinson, Suzan Jeffries, Elaine Holmes, Neena Modi, Nicholas J Andreas, Matthew J Hyde, Chris Gale, James R C Parkinson, Suzan Jeffries, Elaine Holmes, Neena Modi

Abstract

Background: Maternal Body Mass Index (BMI) is positively associated with infant obesity risk. Breast milk contains a number of hormones that may influence infant metabolism during the neonatal period; these may have additional downstream effects on infant appetite regulatory pathways, thereby influencing propensity towards obesity in later life.

Objective: To conduct a systematic review of studies examining the association between maternal BMI and the concentration of appetite-regulating hormones in breast milk.

Method: Pubmed was searched for studies reporting the association between maternal BMI and leptin, adiponectin, insulin, ghrelin, resistin, obestatin, Peptide YY and Glucagon-Like Peptide 1 in breast milk.

Results: Twenty six studies were identified and included in the systematic review. There was a high degree of variability between studies with regard to collection, preparation and analysis of breast milk samples. Eleven of fifteen studies reporting breast milk leptin found a positive association between maternal BMI and milk leptin concentration. Two of nine studies investigating adiponectin found an association between maternal BMI and breast milk adiponectin concentration; however significance was lost in one study following adjustment for time post-partum. No association was seen between maternal BMI and milk adiponectin in the other seven studies identified. Evidence for an association between other appetite regulating hormones and maternal BMI was either inconclusive, or lacking.

Conclusions: A positive association between maternal BMI and breast milk leptin concentration is consistently found in most studies, despite variable methodology. Evidence for such an association with breast milk adiponectin concentration, however, is lacking with additional research needed for other hormones including insulin, ghrelin, resistin, obestatin, peptide YY and glucagon-like peptide-1. As most current studies have been conducted with small sample sizes, future studies should ensure adequate sample sizes and standardized methodology.

Conflict of interest statement

Competing Interests: NJA has received support from Medela to attend an educational conference, but declared no other conflict of interest. MJH has received support from Danone International to attend an educational conference, but declared no other conflict of interest. CG has received support from Pfizer Nutrition to attend an educational conference, but declared no other conflict of interest. In the last five years NM has received consultancy fees from Ferring Pharmaceuticals, speaker honorarium for an educational meeting funded by Nestle International in which they had no organisational involvement, and grants from the Medical Research Council, National Institute of Heath Research, Westminster Children’s Trust Fund, Child Growth Foundation, Action Medical Research, HCA International, Bliss, British Heart Foundation, and Department of Health. JRCP, SJ and EH declare no conflicts of interest. The competing interests declared do not alter the authors' adherence to PLOS ONE policies on sharing data and materials.

Figures

Figure 1. Flowchart of the search strategy…
Figure 1. Flowchart of the search strategy used in the review.
The relevant number of papers at each point is provided.

References

    1. Cripps RL, Archer ZA, Mercer JG, Ozanne SE (2007) Early life programming of energy balance. Biochem Soc Trans 35:1203–1204.
    1. Lucas A (2005) Long-term programming effects of early nutrition – implications for the preterm infant. J Perinatol 25 Suppl 2 S2–S6.
    1. Owen CG, Martin RM, Whincup PH, Smith GD, Cook DG (2005) Effect of infant feeding on the risk of obesity across the life course: a quantitative review of published evidence. Pediatrics 115:1367–1377.
    1. Harder T, Bergmann R, Kallischnigg G, Plagemann A (2005) Duration of breastfeeding and risk of overweight: a meta-analysis. Am J Epidemiol 162:397–403.
    1. Arenz S, Ruckerl R, Koletzko B, von Kries R (2004) Breast-feeding and childhood obesity–a systematic review. Int J Obes Relat Metab Disord 28:1247–1256.
    1. Li R, Magadia J, Fein SB, Grummer-Strawn LM (2012) Risk of bottle-feeding for rapid weight gain during the first year of life. Arch Pediatr Adolesc Med 166:431–436.
    1. Hamosh M (2001) Bioactive factors in human milk. Pediatr Clin North Am 48:69–86.
    1. Houseknecht KL, McGuire MK, Portocarrero CP, McGuire MA, Beerman K (1997) Leptin is present in human milk and is related to maternal plasma leptin concentration and adiposity. Biochem Biophys Res Commun 240:742–747.
    1. Martin LJ, Woo JG, Geraghty SR, Altaye M, Davidson BS, et al. (2006) Adiponectin is present in human milk and is associated with maternal factors. Am J Clin Nutr 83:1106–1111.
    1. Aydin S, Ozkan Y, Kumru S (2006) Ghrelin is present in human colostrum, transitional and mature milk. Peptides 27:878–882.
    1. Aydin S, Ozkan Y, Erman F, Gurates B, Kilic N, et al. (2008) Presence of obestatin in breast milk: relationship among obestatin, ghrelin, and leptin in lactating women. Nutrition 24:689–693.
    1. Savino F, Sorrenti M, Benetti S, Lupica MM, Liguori SA, et al. (2012) Resistin and leptin in breast milk and infants in early life. Early Hum Dev 88:779–782.
    1. Shehadeh N, Khaesh-Goldberg E, Shamir R, Perlman R, Sujov P, et al. (2003) Insulin in human milk: postpartum changes and effect of gestational age. Arch Dis Child Fetal Neonatal Ed 88:F214–216.
    1. Schueler J (2013) Presence and dynamics of leptin, GLP-1, and PYY in human breast milk at early postpartum. Obesity (Silver Spring) 21:1451–1458.
    1. Berseth CL, Michener SR, Nordyke CK, Go VL (1990) Postpartum changes in pattern of gastrointestinal regulatory peptides in human milk. Am J Clin Nutr 51:985–990.
    1. Agostoni C (2005) Ghrelin, leptin and the neurometabolic axis of breastfed and formula-fed infants. Acta Paediatrica 94:523–525.
    1. Considine RV, Sinha MK, Heiman ML, Kriauciunas A, Stephens TW, et al. (1996) Serum immunoreactive-leptin concentrations in normal-weight and obese humans. N Engl J Med 334:292–295.
    1. Degawa-Yamauchi M, Bovenkerk JE, Juliar BE, Watson W, Kerr K, et al. (2003) Serum resistin (FIZZ3) protein is increased in obese humans. J Clin Endocrinol Metab 88:5452–5455.
    1. Lovejoy J, DiGirolamo M (1992) Habitual dietary intake and insulin sensitivity in lean and obese adults. Am J Clin Nutr 55:1174–1179.
    1. Coppola A, Marfella R, Coppola L, Tagliamonte E, Fontana D, et al. (2009) Effect of weight loss on coronary circulation and adiponectin levels in obese women. Int J Cardiol 134:414–416.
    1. Cummings DE, Weigle DS, Frayo RS, Breen PA, Ma MK, et al. (2002) Plasma ghrelin levels after diet-induced weight loss or gastric bypass surgery. N Engl J Med 346:1623–1630.
    1. Lippl F, Erdmann J, Lichter N, Tholl S, Wagenpfeil S, et al. (2008) Relation of plasma obestatin levels to bmi, gender, age and insulin. Horm Metab Res 40:806–812.
    1. Alvarez Bartolome M, Borque M, Martinez-Sarmiento J, Aparicio E, Hernandez C, et al. (2002) Peptide YY secretion in morbidly obese patients before and after vertical banded gastroplasty. Obes Surg 12:324–327.
    1. Madsbad S (2014) The role of glucagon-like peptide-1 impairment in obesity and potential therapeutic implications. Diabetes Obes Metab 16:9–21.
    1. Doneray H, Orbak Z, Yildiz L (2009) The relationship between breast milk leptin and neonatal weight gain. Acta Paediatr 98:643–647.
    1. Savino F, Liguori SA, Lupica MM (2010) Adipokines in breast milk and preterm infants. Early Hum Dev Jul;86 Suppl1:77–80.
    1. Weyermann M, Beermann C, Brenner H, Rothenbacher D (2006) Adiponectin and leptin in maternal serum, cord blood, and breast milk. Clin Chem 52:2095–2102.
    1. Whitmore TJ, Trengove NJ, Graham DF, Hartmann PE (2012) Analysis of insulin in human breast milk in mothers with type 1 and type 2 diabetes mellitus. Int J Endocrinol 2012:296368.
    1. Smith-Kirwin SM, O'Connor DM, De Johnston J, Lancey ED, Hassink SG, et al. (1998) Leptin expression in human mammary epithelial cells and breast milk. J Clin Endocrinol Metab 83:1810–1813.
    1. Kierson JA, Dimatteo DM, Locke RG, Mackley AB, Spear ML (2006) Ghrelin and cholecystokinin in term and preterm human breast milk. Acta Paediatr 95:991–995.
    1. Liberati A, Altman DG, Tetzlaff J, Mulrow C, Gotzsche PC, et al. (2009) The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: explanation and elaboration. PLoS Med 6:e1000100.
    1. Lonnerdal B, Havel PJ (2000) Serum leptin concentrations in infants: effects of diet, sex, and adiposity. Am J Clin Nutr 72:484–489.
    1. Vukavic T (1984) Timing of the gut closure. J Pediatr Gastroenterol Nutr 3:700–703.
    1. Bielicki J, Huch R, von Mandach U (2004) Time-course of leptin levels in term and preterm human milk. Eur J Endocrinol 151:271–276.
    1. Bronsky J, Karpisek M, Bronska E, Pechova M, Jancikova B, et al. (2006) Adiponectin, adipocyte fatty acid binding protein, and epidermal fatty acid binding protein: proteins newly identified in human breast milk. Clin Chem 52:1763–1770.
    1. Bronsky J, Mitrova K, Karpisek M, Mazoch J, Durilova M, et al. (2011) Adiponectin, AFABP, and leptin in human breast milk during 12 months of lactation. J Pediatr Gastroenterol Nutr 52:474–477.
    1. Dundar NO, Anal O, Dundar B, Ozkan H, Caliskan S, et al. (2005) Longitudinal investigation of the relationship between breast milk leptin levels and growth in breast-fed infants. J Pediatr Endocrinol Metab 18:181–187.
    1. Eilers E, Ziska T, Harder T, Plagemann A, Obladen M, et al. (2011) Leptin determination in colostrum and early human milk from mothers of preterm and term infants. Early Hum Dev 87:415–419.
    1. Miralles O, Sanchez J, Palou A, Pico C (2006) A physiological role of breast milk leptin in body weight control in developing infants. Obesity (Silver Spring) 14:1371–1377.
    1. Ucar B, Kirel B, Bor O, Kilic FS, Dogruel N, et al. (2000) Breast milk leptin concentrations in initial and terminal milk samples: relationships to maternal and infant plasma leptin concentrations, adiposity, serum glucose, insulin, lipid and lipoprotein levels. J Pediatr Endocrinol Metab 13:149–156.
    1. Uysal FK, Onal EE, Aral YZ, Adam B, Dilmen U, et al. (2002) Breast milk leptin: its relationship to maternal and infant adiposity. Clin Nutr 21:157–160.
    1. Weyermann M, Brenner H, Rothenbacher D (2007) Adipokines in human milk and risk of overweight in early childhood: a prospective cohort study. Epidemiology 18:722–729.
    1. Fields DA, Demerath EW (2012) Relationship of insulin, glucose, leptin, IL-6 and TNF-alpha in human breast milk with infant growth and body composition. Pediatr Obes.
    1. Schuster S, Hechler C, Gebauer C, Kiess W, Kratzsch J (2011) Leptin in maternal serum and breast milk: association with infants' body weight gain in a longitudinal study over 6 months of lactation. Pediatr Res 70:633–637.
    1. Brunner S, Schmid D, Zang K, Much D, Knoeferl B, et al. (2014) Breast milk leptin and adiponectin in relation to infant body composition up to 2 years. Pediatr Obes.
    1. Dundar NO, Dundar B, Cesur G, Yilmaz N, Sutcu R, et al. (2010) Ghrelin and adiponectin levels in colostrum, cord blood and maternal serum. Pediatr Int 52:622–625.
    1. Ley SH, Hanley AJ, Sermer M, Zinman B, O'Connor DL (2012) Associations of prenatal metabolic abnormalities with insulin and adiponectin concentrations in human milk. Am J Clin Nutr 95:867–874.
    1. Luoto R, Laitinen K, Nermes M, Isolauri E (2012) Impact of maternal probiotic-supplemented dietary counseling during pregnancy on colostrum adiponectin concentration: a prospective, randomized, placebo-controlled study. Early Hum Dev 88:339–344.
    1. Luoto R, Kalliomaki M, Laitinen K, Delzenne NM, Cani PD, et al. (2011) Initial dietary and microbiological environments deviate in normal-weight compared to overweight children at 10 years of age. J Pediatr Gastroenterol Nutr 52:90–95.
    1. Woo JG, Guerrero ML, Altaye M, Ruiz-Palacios GM, Martin LJ, et al. (2009) Human milk adiponectin is associated with infant growth in two independent cohorts. Breastfeed Med 4:101–109.
    1. Ahuja S (2011) Glucose and Insulin Levels are Increased in Obese and Overweight Mothers' Breast-milk. Food and Nutrition Sciences 2:201–206.
    1. Aydin S (2010) 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 31:2236–2240.
    1. Aydin S, Geckil H, Karatas F, Donder E, Kumru S, et al. (2007) Milk and blood ghrelin level in diabetics. Nutrition 23:807–811.
    1. Gale C, Logan KM, Santhakumaran S, Parkinson JR, Hyde MJ, et al. (2012) Effect of breastfeeding compared with formula feeding on infant body composition: a systematic review and meta-analysis. Am J Clin Nutr 95:656–669.
    1. Oddy WH (2012) Infant feeding and obesity risk in the child. Breastfeed Rev 20:7–12.
    1. Martin RM, Patel R, Kramer MS, Guthrie L, Vilchuck K, et al. (2013) Effects of promoting longer-term and exclusive breastfeeding on adiposity and insulin-like growth factor-I at age 11.5 years: a randomized trial. JAMA 309:1005–1013.
    1. Savino F, Liguori SA, Petrucci E, Lupica MM, Fissore MF, et al. (2010) Evaluation of leptin in breast milk, lactating mothers and their infants. Eur J Clin Nutr 64:972–977.
    1. Savino F, Liguori SA, Oggero R, Silvestro L, Miniero R (2006) Maternal BMI and serum leptin concentration of infants in the first year of life. Acta Paediatr 95:414–418.
    1. Parsons TJ, Power C, Manor O (2001) Fetal and early life growth and body mass index from birth to early adulthood in 1958 British cohort: longitudinal study. BMJ 323:1331–1335.
    1. Savino F, Lupica MM, Benetti S, Petrucci E, Liguori SA, et al. (2012) Adiponectin in breast milk: relation to serum adiponectin concentration in lactating mothers and their infants. Acta Paediatr 101:1058–1062.
    1. Newburg DS, Woo JG, Morrow AL (2010) Characteristics and potential functions of human milk adiponectin. J Pediatr 156:S41–46.
    1. Bronsky J, Mitrova K, Nevoral J, Zamecnik J (2012) Immunoexpression of type-1 adiponectin receptor in the human intestine. Cesk Patol 48:165–166.
    1. Casabiell X, Pineiro V, Tome MA, Peino R, Dieguez C, et al. (1997) 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 82:4270–4273.
    1. Sanchez J, Oliver P, Miralles O, Ceresi E, Pico C, et al. (2005) Leptin orally supplied to neonate rats is directly uptaken by the immature stomach and may regulate short-term feeding. Endocrinology 146:2575–2582.
    1. Pico C, Sanchez J, Oliver P, Miralles O, Ceresi E, et al. (2007) Role of leptin present in maternal milk in the control of energy balance during the post-natal period. Genes Nutr 2:139–141.
    1. Sanchez J, Priego T, Palou M, Tobaruela A, Palou A, et al. (2008) Oral supplementation with physiological doses of leptin during lactation in rats improves insulin sensitivity and affects food preferences later in life. Endocrinology 149:733–740.
    1. Priego T, Sanchez J, Palou A, Pico C (2010) Leptin intake during the suckling period improves the metabolic response of adipose tissue to a high-fat diet. Int J Obes (Lond) 34:809–819.
    1. Hirsova D, Koldovsky O (1969) On the question of the absorption of insulin from the gastrointestinal tract during postnatal development. Physiol Bohemoslov 18:281–284.
    1. Shehadeh N, Sukhotnik I, Shamir R (2006) Gastrointestinal tract as a target organ for orally administered insulin. J Pediatr Gastroenterol Nutr 43:276–281.
    1. Nilsson L, Binart N, Bohlooly YM, Bramnert M, Egecioglu E, et al. (2005) Prolactin and growth hormone regulate adiponectin secretion and receptor expression in adipose tissue. Biochem Biophys Res Commun 331:1120–1126.
    1. Jovanovic-Peterson L, Fuhrmann K, Hedden K, Walker L, Peterson CM (1989) Maternal milk and plasma glucose and insulin levels: studies in normal and diabetic subjects. J Am Coll Nutr 8:125–131.
    1. Mayfield J (1998) Diagnosis and classification of diabetes mellitus: new criteria. Am Fam Physician 58: 1355–1362, 1369–1370.
    1. Toshinai K, Yamaguchi H, Sun Y, Smith RG, Yamanaka A, et al. (2006) Des-acyl ghrelin induces food intake by a mechanism independent of the growth hormone secretagogue receptor. Endocrinology 147:2306–2314.
    1. Stengel A, Keire D, Goebel M, Evilevitch L, Wiggins B, et al. (2009) The RAPID method for blood processing yields new insight in plasma concentrations and molecular forms of circulating gut peptides. Endocrinology 150:5113–5118.
    1. Zhang N, Yuan C, Li Z, Li J, Li X, et al. (2011) Meta-analysis of the relationship between obestatin and ghrelin levels and the ghrelin/obestatin ratio with respect to obesity. Am J Med Sci 341:48–55.
    1. Savino F, Benetti S, Lupica MM, Petrucci E, Palumeri E, et al. (2012) Ghrelin and obestatin in infants, lactating mothers and breast milk. Horm Res Paediatr 78:297–303.

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