Impact of maternal metabolic abnormalities in pregnancy on human milk and subsequent infant metabolic development: methodology and design

Sylvia H Ley, Deborah L O'Connor, Ravi Retnakaran, Jill K Hamilton, Mathew Sermer, Bernard Zinman, Anthony J Hanley, Sylvia H Ley, Deborah L O'Connor, Ravi Retnakaran, Jill K Hamilton, Mathew Sermer, Bernard Zinman, Anthony J Hanley

Abstract

Background: Childhood obesity is on the rise and is a major risk factor for type 2 diabetes later in life. Recent evidence indicates that abnormalities that increase risk for diabetes may be initiated early in infancy. Since the offspring of women with diabetes have an increased long-term risk for obesity and type 2 diabetes, the impact of maternal metabolic abnormalities on early nutrition and infant metabolic trajectories is of considerable interest. Human breast milk, the preferred food during infancy, contains not only nutrients but also an array of bioactive substances including metabolic hormones. Nonetheless, only a few studies have reported concentrations of metabolic hormones in human milk specifically from women with metabolic abnormalities. We aim to investigate the impact of maternal metabolic abnormalities in pregnancy on human milk hormones and subsequently on infant development over the first year of life. The objective of this report is to present the methodology and design of this study.

Methods/design: The current investigation is a prospective study conducted within ongoing cohort studies of women and their offspring. Pregnant women attending outpatient obstetrics clinics in Toronto, Canada were recruited. Between April 2009 and July 2010, a total of 216 pregnant women underwent a baseline oral glucose tolerance test and provided medical and lifestyle history. Follow-up visits and telephone interviews are conducted and expected to be completed in October 2011. Upon delivery, infant birth anthropometry measurements and human breast milk samples are collected. At 3 and 12 months postpartum, mothers and infants are invited for follow-up assessments. Interim telephone interviews are conducted during the first year of offspring life to characterize infant feeding and supplementation behaviors.

Discussion: An improved understanding of the link between maternal metabolic abnormalities in pregnancy and early infant nutrition may assist in the development of optimal prevention and intervention strategies and in the protection of nutritionally vulnerable offspring who are at risk for obesity and diabetes later in life.

Figures

Figure 1
Figure 1
Conceptual model.
Figure 2
Figure 2
Schedule of four assessment visits and interim telephone calls from late pregnancy to 1-year postpartum.

References

    1. Hannon TS, Rao G, Arslanian SA. Childhood obesity and type 2 diabetes mellitus. Pediatrics. 2005;116:473–480. doi: 10.1542/peds.2004-2536.
    1. Sinha R, Fisch G, Teague B, Tamborlane WV, Banyas B, Allen K, Savoye M, Rieger V, Taksali S, Barbetta G. et al.Prevalence of impaired glucose tolerance among children and adolescents with marked obesity. N Engl J Med. 2002;346:802–810. doi: 10.1056/NEJMoa012578.
    1. Amed S, Dean HJ, Panagiotopoulos C, Sellers EAC, Hadjiyannakis S, Laubscher TA, Dannenbaum D, Shah BR, Booth GL, Hamilton JK. Type 2 diabetes, medication-induced diabetes, and monogenic diabetes in Canadian children: a prospective national surveillance study. Diabetes Care. 2010;33:786–791. doi: 10.2337/dc09-1013.
    1. 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. doi: 10.1542/peds.2004-1176.
    1. Arenz S, Ruckerl R, Koletzko B, von Kries R. Breast-feeding and childhood obesity - a systematic review. Int J Obes Relat Metab Disord. 2004;28:1247–1256. doi: 10.1038/sj.ijo.0802758.
    1. 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.
    1. Lucas A, Fewtrell MS, Cole TJ. Fetal origins of adult disease - the hypothesis revisited. Br Med J. 1999;319:245–249.
    1. Plagemann A. A matter of insulin: Developmental programming of body weight regulation. J Matern Fetal Neonatal Med. 2008;21:143–148. doi: 10.1080/14767050801929869.
    1. American Academy of Pediatrics. Breastfeeding and the use of human milk. Pediatrics. 2005;115:496–506. doi: 10.1542/peds.2004-2491.
    1. World Health Organization. Global strategies for infant and young child feeding. Book Global strategies for infant and young child feeding. (Editor ed.). City. 2003.
    1. AAP Committee on Nutrition. New York. 6 2009. Pediatric nutrition handbook.
    1. Butte NF. Impact of Infant Feeding Practices on Childhood Obesity. J Nutr. 2009;139:S412–S416.
    1. Adair LS. Methods appropriate for studying the relationship of breast-feeding to obesity. J Nutr. 2009;139:S408–S411.
    1. Hamosh M. Bioactive factors in human milk. Pediatr Clin North Am. 2001;48:69–86. doi: 10.1016/S0031-3955(05)70286-8.
    1. Houseknecht KL, McGuire MK, Portocarrero CP, McGuire MA, Beerman K. Leptin is present in human milk and is related to maternal plasma leptin concentration and adiposity. Biochem Biophys Res Commun. 1997;240:742–747. doi: 10.1006/bbrc.1997.7736.
    1. McGill HC, Mott GE, Lewis DS, McMahan CA, Jackson EM. Early determinants of adult metabolic regulation: effects of infant nutrition on adult lipid and lipoprotein metabolism. Nutr Rev. 1996;54:S31–S40. doi: 10.1111/j.1753-4887.1996.tb03868.x.
    1. Savino F, Liguori SA. Update on breast milk hormones: Leptin, ghrelin and adiponectin. Clin Nutr. 2008;27:42–47. doi: 10.1016/j.clnu.2007.06.006.
    1. Martin LJ, Woo JG, Geraghty SR, Altaye M, Davidson BS, Banach W, Dolan LM, Ruiz-Palacios GM, Morrow AL. Adiponectin is present in human milk and is associated with maternal factors. Am J Clin Nutr. 2006;83:1106–1111.
    1. Aydin S, Aydin S, Ozkan Y, Kumru S. Ghrelin is present in human colostrum, transitional and mature milk. Peptides. 2006;27:878–882. doi: 10.1016/j.peptides.2005.08.006.
    1. Aydin S, Geckil H, Karatas F, Donder E, Kumru S, Kavak EC, 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. Hartmann P, Cregan M. Lactogenesis and the effects of insulin-dependent diabetes mellitus and prematurity. J Nutr. 2001;131:S3016–S3020.
    1. Dabelea D, Mayer-Davis EJ, Lamichhane AP, D'Agostino RB, Liese AD Jr, Vehik KS, Narayan KMV, Zeitler P, Hamman RF. Association of intrauterine exposure to maternal diabetes and obesity with type 2 diabetes in youth: the SEARCH Case-Control Study. Diabetes Care. 2008;31:1422–1426. doi: 10.2337/dc07-2417.
    1. Canadian Diabetes Association Clinical Practice Guidelines ExpertCommittee. Canadian Diabetes Association 2008 Clinical practice guidelines for the prevention and management of diabetes in Canada. Can J Diabetes. 2008;32(Suppl 1):S1–S201.
    1. Hilson J, Rasmussen K, Kjolhede C. Maternal obesity and breast-feeding success in a rural population of white women. Am J Clin Nutr. 1997;66:1371–1378.
    1. Sebire NJ, Jolly M, Harris JP, Wadsworth J, Joffe M, Beard RW, Regan L, Robinson S. Maternal obesity and pregnancy outcome: a study of 287,213 pregnancies in London. Int J Obes Relat Metab Disord. 2001;25:1175–1182. doi: 10.1038/sj.ijo.0801670.
    1. Chapman D, Perez-Escamilla R. Identification of risk factors for delayed onset of lactation. J Am Diet Assoc. 1999;99:450–454. doi: 10.1016/S0002-8223(99)00109-1.
    1. Rasmussen KM. Association of maternal obesity before conception with poor lactation performance. Annu Rev of Nutr. 2007;27:103–121. doi: 10.1146/annurev.nutr.27.061406.093738.
    1. Ferris A, Neubauer S, Bendel R, Green K, Ingardia C, Reece E. Perinatal lactation protocol and outcome in mothers with and without insulin-dependent diabetes mellitus. Am J Clin Nutr. 1993;58:43–48.
    1. Hilson JA, Rasmussen KM, Kjolhede CL. High prepregnant body mass index is associated with poor lactation outcomes among white, rural women independent of psychosocial and demographic correlates. J Hum Lact. 2004;20:18–29. doi: 10.1177/0890334403261345.
    1. Rasmussen KM, Kjolhede CL. Prepregnant overweight and obesity diminish the prolactin response to suckling in the first week postpartum. Pediatrics. 2004;113:e465–e471. doi: 10.1542/peds.113.5.e465.
    1. Amir L, Donath S. A systematic review of maternal obesity and breastfeeding intention, initiation and duration. BMC Pregnancy Childbirth. 2007;7:9. doi: 10.1186/1471-2393-7-9.
    1. Hilson JA, Rasmussen KM, Kjolhede CL. Excessive weight gain during pregnancy is associated with earlier termination of breast-feeding among White women. J Nutr. 2006;136:140–146.
    1. Arthur P, Smith M, Hartmann P. Milk lactose, citrate, and glucose as markers of lactogenesis in normal and diabetic women. J Pediatr Gastroenterol Nutr. 1989;9:488–496. doi: 10.1097/00005176-198911000-00016.
    1. Neubauer S, Ferris A, Chase C, Fanelli J, Thompson C, Lammi-Keefe C, Clark R, Jensen R, Bendel R, Green K. Delayed lactogenesis in women with insulin-dependent diabetes mellitus. Am J Clin Nutr. 1993;58:54–60.
    1. 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;25:16–22. doi: 10.2337/diacare.25.1.16.
    1. 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;28:1457–1462. doi: 10.2337/diacare.28.6.1457.
    1. Casabiell X, Pineiro V, Tome MA, Peino R, Dieguez C, Casanueva FF. 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/jc.82.12.4270.
    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. Kierson JA, Dimatteo DM, Locke RG, Mackley AB, Spear ML. Ghrelin and cholecystokinin in term and preterm human breast milk. Acta Paediatr. 2006;95:991–995. doi: 10.1080/08035250600669769.
    1. Ilcol YO, Hizli B. Active and total ghrelin concentrations increase in breast milk during lactation. Acta Pædiatr. 2007;96:1632–1639. doi: 10.1111/j.1651-2227.2007.00493.x.
    1. Sahu A. Minireview: A hypothalamic role in energy balance with special emphasis on leptin. Endocrinology. 2004;145:2613–2620. doi: 10.1210/en.2004-0032.
    1. Horvath TL, Diano S, Sotonyi P, Heiman M, Tschop M. Minireview: ghrelin and the regulation of energy balance--a hypothalamic perspective. Endocrinology. 2001;142:4163–4169. doi: 10.1210/en.142.10.4163.
    1. Wellen KE, Hotamisligil GS. Inflammation, stress, and diabetes. J Clin Invest. 2005;115:1111–1119.
    1. Bielicki J, Huch R, von Mandach U. Time-course of leptin levels in term and preterm human milk. Eur J Endocrinol. 2004;151:271–276. doi: 10.1530/eje.0.1510271.
    1. 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;14:1371–1377. doi: 10.1038/oby.2006.155.
    1. 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. doi: 10.1097/EDE.0b013e3181567ed4.
    1. Woo JG, Guerrero ML, Altaye M, Ruiz-Palacios GM, Martin LJ, Dubert-Ferrandon A, Newburg DS, Morrow AL. Human milk adiponectin is associated with infant growth in two independent cohorts. Breastfeed Med. 2009;4:101–9. doi: 10.1089/bfm.2008.0137.
    1. Sobhani I, Bado A, Vissuzaine C, Buyse M, Kermorgant S, Laigneau JP, Attoub S, Lehy T, Henin D, Mignon M. et al.Leptin secretion and leptin receptor in the human stomach. Gut. 2000;47:178–183. doi: 10.1136/gut.47.2.178.
    1. Mix H, Widjaja A, Jandl O, Cornberg M, Kaul A, Göke M, Beil W, Kuske M, Brabant G, Manns M. et al.Expression of leptin and leptin receptor isoforms in the human stomach. Gut. 2000;47:481–486. doi: 10.1136/gut.47.4.481.
    1. Barrenetxe J, Villaro AC, Guembe L, Pascual I, Munoz-Navas M, Barber A, Lostao MP. Distribution of the long leptin receptor isoform in brush border, basolateral membrane, and cytoplasm of enterocytes. Gut. 2002;50:797–802. doi: 10.1136/gut.50.6.797.
    1. Yoneda K, Tomimoto A, Endo H, Iida H, Sugiyama M, Takahashi H, Mawatari H, Nozaki Y, Fujita K, Yoneda M. et al.Expression of adiponectin receptors, AdipoR1 and AdipoR2, in normal colon epithelium and colon cancer tissue. Oncol Rep. 2008;20:479–483.
    1. Goldman AS. Modulation of the gastrointestinal tract of infants by human milk. Interfaces and interactions. An evolutionary perspective. J Nutr. 2000;130:S426–S431.
    1. Goldman AS, Chheda S, Garofalo R, Schmalstieg FC. Cytokines in human milk: properties and potential effects upon the mammary gland and the neonate. J Mammary Gland Biol Neoplasia. 1996. pp. 251–258.
    1. Koldovský O. The potential physiological significance of milk-borne hormonally active substances for the neonate. J Mammary Gland Biol Neoplasia. 1996;1:317–323. doi: 10.1007/BF02018084.
    1. Bouret SG, Draper SJ, Simerly RB. Trophic action of leptin on hypothalamic neurons that regulate feeding. Science. 2004;304:108–110. doi: 10.1126/science.1095004.
    1. Retnakaran R, Qi Y, Sermer M, Connelly PW, Hanley AJG, Zinman B. Glucose intolerance in pregnancy and future risk of pre-diabetes or diabetes. Diabetes Care. 2008;31:2026–2031. doi: 10.2337/dc08-0972.
    1. Retnakaran R, Qi Y, Sermer M, Connelly PW, Zinman B, Hanley AJ. Pre-gravid physical activity and reduced risk of glucose intolerance in pregnancy: the role of insulin sensitivity. Clin Endocrinol. 2009;70:615–622. doi: 10.1111/j.1365-2265.2008.03393.x.
    1. Retnakaran R, Qi Y, Sermer M, Connelly PW, Hanley AJ, Zinman B. The antepartum glucose values that predict neonatal macrosomia differ from those that predict postpartum prediabetes or diabetes: implications for the diagnostic criteria for gestational diabetes. J Clin Endocrinol Metab. 2009;94:840–845. doi: 10.1210/jc.2008-2434.
    1. Hamilton JK, Odrobina E, Yin J, Hanley AJ, Zinman B, Retnakaran R. Maternal insulin sensitivity during pregnancy predicts infant weight gain and adiposity at 1 year of age. Obesity (Silver Spring) 2010;18:340–346. doi: 10.1038/oby.2009.231.
    1. Dewey KG, Nommsen-Rivers LA, Heinig MJ, Cohen RJ. Risk factors for suboptimal infant breastfeeding behavior, delayed onset of lactation, and excess neonatal weight loss. Pediatrics. 2003;112:607–619. doi: 10.1542/peds.112.3.607.
    1. Toronto Public Health. Book Toronto Perinatal and Child Health Survey 2003 (Editor ed.) City: Toronto Public Health; 2005. Toronto Perinatal and Child Health Survey 2003.
    1. Chalmers B, Levitt C, Heaman M, O'Brien B, Sauve R, Kaczorowski J. Breastfeeding rates and hospital breastfeeding practices in Canada: a national survey of women. Birth. 2009;36:122–132. doi: 10.1111/j.1523-536X.2009.00309.x.
    1. National Diabetes Data Group. Classification and diagnosis of diabetes mellitus and other categories of glucose intolerance. Diabetes. 1979;28:1039–1057.
    1. Block G, Hartman AM, Dresser CM, Carroll MD, Gannon J, Gardner L. A data-based approach to diet questionnaire design and testing. Am J Epidemiol. 1986;124:453–469.
    1. Block G, Coyle LM, Hartman AM, Scoppa SM. Revision of dietary analysis software for the Health Habits and History Questionnaire. Am J Epidemiol. 1994;139:1190–1196.
    1. Block G, Thompson FE, Hartman AM, Larkin FA, Guire KE. Comparison of two dietary questionnaires validated against multiple dietary records collected during a 1-year period. J Am Diet Assoc. 1992;92:686–693.
    1. Block G, Woods M, Potosky A, Clifford C. Validation of a self-administered diet history questionnaire using multiple diet records. J Clin Epidemiol. 1990;43:1327–1335. doi: 10.1016/0895-4356(90)90099-B.
    1. Boucher B, Cotterchio M, Kreiger N, Nadalin V, Block T, Block G. Validity and reliability of the Block98 food-frequency questionnaire in a sample of Canadian women. Public Health Nutr. 2006;9:84–93. doi: 10.1079/PHN2005763.
    1. Siega-Riz AM, Savitz DA, Zeisel SH, Thorp JM, Herring A. Second trimester folate status and preterm birth. Am J Obstet Gynecol. 2004;191:1851–1857. doi: 10.1016/j.ajog.2004.07.076.
    1. Saldana TM, Siega-Riz AM, Adair LS. Effect of macronutrient intake on the development of glucose intolerance during pregnancy. Am J Clin Nutr. 2004;79:479–486.
    1. Gibson RS. Principles of nutritional assessment. 2. Oxford University Press; 2005.
    1. Prevention CFDCA. Third National Health and Nutrition Examiniation (NHANES III) Anthropometric Procedures Video. 2003.
    1. Chapman DJ, Perez-Escamilla R. Maternal perception of the onset of lactation is a valid, public health indicator of lactogenesis stage II. J Nutr. 2000;130:2972–2980.
    1. Medicine ACoS. ACSM's Resource manual for guidelines for exercise testing and prescription. 4. Lippincott Williams and Wilkins; 2001.
    1. Schmelzle HR, Fusch C. Body fat in neonates and young infants: validation of skinfold thickness versus dual-energy X-ray absorptiometry. Am J Clin Nutr. 2002;76:1096–1100.
    1. Goran M, Driscoll P, Johnson R, Nagy T, Hunter G. Cross-calibration of body-composition techniques against dual-energy X- ray absorptiometry in young children. Am J Clin Nutr. 1996;63:299–305.
    1. Matsuda M, DeFronzo R. Insulin sensitivity indices obtained from oral glucose tolerance testing: comparison with the euglycemic insulin clamp. Diabetes Care. 1999;22:1462–1470. doi: 10.2337/diacare.22.9.1462.
    1. Retnakaran R, Qi Y, Goran MI, Hamilton JK. Evaluation of proposed oral disposition index measures in relation to the actual disposition index. Diabet Med. 2009;26:1198–1203. doi: 10.1111/j.1464-5491.2009.02841.x.
    1. Smith-Kirwin SM, O'Connor DM, Johnston J, de Lancy E, Hassink SG, Funanage VL. Leptin expression in human mammary epithelial cells and breast milk. J Clin Endocrinol Metab. 1998;83:1810–1813. doi: 10.1210/jc.83.5.1810.

Source: PubMed

Sponsors et collaborateurs

Les conditions médicales

Interventions en matière de drogue

3
S'abonner