Hostname: page-component-6d856f89d9-jrqft Total loading time: 0 Render date: 2024-07-16T08:31:42.321Z Has data issue: false hasContentIssue false
  • English
  • Français

Effect of human milk formula with bovine colostrum supplementation on bone mineral density in infant cynomolgus macaques

Published online by Cambridge University Press:  17 October 2017

N. Tay ,
Y. C. Tan ,
K. Chng ,
C. Libedinsky ,
P. Gluckman  and
J. P. Buschdorf
N. Tay
Affiliation:
Singapore Institute for Clinical Sciences, Singapore, Singapore
Y. C. Tan
Affiliation:
Singapore Institute for Clinical Sciences, Singapore, Singapore
K. Chng
Affiliation:
Singapore Institute for Clinical Sciences, Singapore, Singapore
C. Libedinsky
Affiliation:
Singapore Institute for Clinical Sciences, Singapore, Singapore
P. Gluckman
Affiliation:
Singapore Institute for Clinical Sciences, Singapore, Singapore
J. P. Buschdorf*
Affiliation:
Singapore Institute for Clinical Sciences, Singapore, Singapore
*
*Address for correspondence: J. P. Buschdorf, Singapore Institute for Clinical Sciences, BLK 30 Medical Drive, Singapore, 117609, Singapore. (Email janpaul@sics.a-star.edu.sg)
Get access Rights & Permissions [Opens in a new window]

Abstract

Insulin-like growth factor 1 (IGF1) is a regulator of human growth during infancy and childhood, known to promote bone and muscle growth as well as lipid accumulation. This study aimed to investigate the effects of formula milk with or without IGF1 supplementation (in the form of pure IGF1 or bovine colostrum) on growth and body composition in infant cynomolgus macaques during the first 6 months of life. Three groups of infants were nursery-reared and received formula milk with or without IGF1 or bovine colostrum supplementation for 4 months, and a fourth group consisting of breast-fed infants was included for comparison (n=6 for each group). Ranked-based analysis of covariance was used to detect differences between adjusted means for sex. No differences in weight, height, fat mass, and fat-free mass could be detected between groups. However, bone mineral density (BMD) was significantly different between groups at the end of formula feeding. Infants that received bovine colostrum supplementation displayed higher mean BMD than infants of all other groups, with no differences between the latter three groups. In conclusion, our results suggest that supplementation with bovine colostrum can enhance BMD in formula-fed infants, an effect that apparently does not depend on IGF1. Bovine colostrum supplementation could be beneficial for long-term bone health in infants with suboptimal bone growth.

Keywords

bone mineral densitycynomolgusIGF1formula milk
Type
Original Article
Information
Journal of Developmental Origins of Health and Disease , Volume 9 , Issue 2 , April 2018 , pp. 172 - 181
Check for updates
Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

1. Flegal, KM, Carroll, MD, Ogden, CL, Curtin, LR. Prevalence and trends in obesity among US adults, 1999-2008. JAMA. 2010; 303, 235–241.Google Scholar
2. Ogden, CL, Carroll, MD, Curtin, LR, Lamb, MM, Flegal, KM. Prevalence of high body mass index in US children and adolescents, 2007–2008. JAMA. 2010; 303, 242–249.Google Scholar
3. Fagot-Campagna, A, Pettitt, DJ, Engelgau, MM, et al. Type 2 diabetes among North American children and adolescents: an epidemiologic review and a public health perspective. J Pediatr. 2000; 136, 664–672.Google Scholar
4. Freedman, DS, Dietz, WH, Srinivasan, SR, Berenson, GS. The relation of overweight to cardiovascular risk factors among children and adolescents: the Bogalusa Heart Study. Pediatrics. 1999; 103(Pt 1), 1175–1182.Google Scholar
5. Strauss, RS. Childhood obesity and self-esteem. Pediatrics. 2000; 105, e15.Google Scholar
6. Ben-Shlomo, Y, Kuh, D. A life course approach to chronic disease epidemiology: conceptual models, empirical challenges and interdisciplinary perspectives. Int J Epidemiol. 2002; 31, 285–293.Google Scholar
7. Dennison, BA, Edmunds, LS, Stratton, HH, Pruzek, RM. Rapid infant weight gain predicts childhood overweight. Obesity (Silver Spring). 2006; 14, 491–499.CrossRefGoogle ScholarPubMed
8. Ong, KK, Ahmed, ML, Emmett, PM, Preece, MA, Dunger, DB. Association between postnatal catch-up growth and obesity in childhood: prospective cohort study. BMJ. 2000; 320, 967–971.Google Scholar
9. Ong, KK, Loos, RJ. Rapid infancy weight gain and subsequent obesity: systematic reviews and hopeful suggestions. Acta Paediatr. 2006; 95, 904–908.Google Scholar
10. Faust, IM, Johnson, PR, Hirsch, J. Long-term effects of early nutritional experience on the development of obesity in the rat. J Nutr. 1980; 110, 2027–2034.Google Scholar
11. Plagemann, A, Harder, T, Rake, A, et al. Perinatal elevation of hypothalamic insulin, acquired malformation of hypothalamic galaninergic neurons, and syndrome x-like alterations in adulthood of neonatally overfed rats. Brain Res. 1999; 836, 146–155.Google Scholar
12. Oken, E, Gillman, MW. Fetal origins of obesity. Obes Res. 2003; 11, 496–506.CrossRefGoogle ScholarPubMed
13. Bernt, KM, Walker, WA. Human milk as a carrier of biochemical messages. Acta Paediatr Suppl. 1999; 88, 27–41.Google Scholar
14. Quigley, JD 3rd, Drewry, JJ. Nutrient and immunity transfer from cow to calf pre- and postcalving. J Dairy Sci. 1998; 81, 2779–2790.Google Scholar
15. Grummer-Strawn, LM, Mei, Z. 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, e81–e86.Google Scholar
16. Stettler, N, Stallings, VA, Troxel, AB, et al. Weight gain in the first week of life and overweight in adulthood: a cohort study of European American subjects fed infant formula. Circulation. 2005; 111, 1897–1903.Google Scholar
17. Victora, CG, Barros, F, Lima, RC, Horta, BL, Wells, J. Anthropometry and body composition of 18 year old men according to duration of breast feeding: birth cohort study from Brazil. BMJ. 2003; 327, 901.Google Scholar
18. Weng, SF, Redsell, SA, Swift, JA, Yang, M, Glazebrook, CP. Systematic review and meta-analyses of risk factors for childhood overweight identifiable during infancy. Arch Dis Child. 2012; 97, 1019–1026.Google Scholar
19. Yan, J, Liu, L, Zhu, Y, Huang, G, Wang, PP. The association between breastfeeding and childhood obesity: a meta-analysis. BMC Public Health. 2014; 14, 1267.Google Scholar
20. Michaelsen, KF, Greer, FR. Protein needs early in life and long-term health. Am J Clin Nutr. 2014; 99, 718S–722S.Google Scholar
21. Hauner, H, Rohrig, K, Petruschke, T. Effects of epidermal growth factor (EGF), platelet-derived growth factor (PDGF) and fibroblast growth factor (FGF) on human adipocyte development and function. Eur J Clin Invest. 1995; 25, 90–96.Google Scholar
22. Petruschke, T, Rohrig, K, Hauner, H. Transforming growth factor beta (TGF-beta) inhibits the differentiation of human adipocyte precursor cells in primary culture. Int J Obes Relat Metab Disord. 1994; 18, 532–536.Google ScholarPubMed
23. Lucas, A, Sarson, DL, Blackburn, AM, et al. Breast vs bottle: endocrine responses are different with formula feeding. Lancet. 1980; 1, 1267–1269.CrossRefGoogle ScholarPubMed
24. Heinig, MJ, Nommsen, LA, Peerson, JM, Lonnerdal, B, Dewey, KG. Energy and protein intakes of breast-fed and formula-fed infants during the first year of life and their association with growth velocity: the DARLING Study. Am J Clin Nutr. 1993; 58, 152–161.Google Scholar
25. Ong, KK, Langkamp, M, Ranke, MB, et al. Insulin-like growth factor I concentrations in infancy predict differential gains in body length and adiposity: the Cambridge Baby Growth Study. Am J Clin Nutr. 2009; 90, 156–161.Google Scholar
26. Ravelli, AC, van der Meulen, JH, Osmond, C, Barker, DJ, Bleker, OP. Infant feeding and adult glucose tolerance, lipid profile, blood pressure, and obesity. Arch Dis Child. 2000; 82, 248–252.Google Scholar
27. de Zegher, F, Sebastiani, G, Diaz, M, et al. Body composition and circulating high-molecular-weight adiponectin and IGF-I in infants born small for gestational age: breast- versus formula-feeding. Diabetes. 2012; 61, 1969–1973.Google Scholar
28. Gluckman, PD. Clinical review 68: the endocrine regulation of fetal growth in late gestation: the role of insulin-like growth factors. J Clin Endocrinol Metab. 1995; 80, 1047–1050.Google ScholarPubMed
29. Le Roith, D, Bondy, C, Yakar, S, Liu, JL, Butler, A. The somatomedin hypothesis: 2001. Endocr Rev. 2001; 22, 53–74.Google Scholar
30. Liu, JL, LeRoith, D. Insulin-like growth factor I is essential for postnatal growth in response to growth hormone. Endocrinology. 1999; 140, 5178–5184.Google Scholar
31. Fernandez, AM, Dupont, J, Farrar, RP, et al. Muscle-specific inactivation of the IGF-I receptor induces compensatory hyperplasia in skeletal muscle. J Clin Invest. 2002; 109, 347–355.Google Scholar
32. Liu, JP, Baker, J, Perkins, AS, Robertson, EJ, Efstratiadis, A. Mice carrying null mutations of the genes encoding insulin-like growth factor I (Igf-1) and type 1 IGF receptor (Igf1r). Cell. 1993; 75, 59–72.Google ScholarPubMed
33. Scavo, LM, Karas, M, Murray, M, Leroith, D. Insulin-like growth factor-I stimulates both cell growth and lipogenesis during differentiation of human mesenchymal stem cells into adipocytes. J Clin Endocrinol Metab. 2004; 89, 3543–3553.Google Scholar
34. van der Eerden, BC, Karperien, M, Wit, JM. Systemic and local regulation of the growth plate. Endocr Rev. 2003; 24, 782–801.Google Scholar
35. Brabant, G, von zur Muhlen, A, Wuster, C, et al. Serum insulin-like growth factor I reference values for an automated chemiluminescence immunoassay system: results from a multicenter study. Horm Res. 2003; 60, 53–60.Google Scholar
36. Juul, A, Bang, P, Hertel, NT, et al. Serum insulin-like growth factor-I in 1030 healthy children, adolescents, and adults: relation to age, sex, stage of puberty, testicular size, and body mass index. J Clin Endocrinol Metab. 1994; 78, 744–752.Google Scholar
37. Beck, KD, Powell-Braxton, L, Widmer, HR, Valverde, J, Hefti, F. Igf1 gene disruption results in reduced brain size, CNS hypomyelination, and loss of hippocampal granule and striatal parvalbumin-containing neurons. Neuron. 1995; 14, 717–730.Google Scholar
38. Woods, KA, Camacho-Hubner, C, Savage, MO, Clark, AJ. Intrauterine growth retardation and postnatal growth failure associated with deletion of the insulin-like growth factor I gene. N Engl J Med. 1996; 335, 1363–1367.Google Scholar
39. Eremia, SC, de Boo, HA, Bloomfield, FH, Oliver, MH, Harding, JE. Fetal and amniotic insulin-like growth factor-I supplements improve growth rate in intrauterine growth restriction fetal sheep. Endocrinology. 2007; 148, 2963–2972.Google Scholar
40. Laron, Z, Anin, S, Klipper-Aurbach, Y, Klinger, B. Effects of insulin-like growth factor on linear growth, head circumference, and body fat in patients with Laron-type dwarfism. Lancet. 1992; 339, 1258–1261.Google Scholar
41. Laron, Z, Ginsberg, S, Lilos, P, Arbiv, M, Vaisman, N. Long-term IGF-I treatment of children with Laron syndrome increases adiposity. Growth Horm IGF Res. 2006; 16, 61–64.Google Scholar
42. Field, T, Diego, M, Hernandez-Reif, M, et al. Insulin and insulin-like growth factor-1 increased in preterm neonates following massage therapy. J Dev Behav Pediatr. 2008; 29, 463–466.Google Scholar
43. Hoppe, C, Udam, TR, Lauritzen, L, et al. Animal protein intake, serum insulin-like growth factor I, and growth in healthy 2.5-y-old Danish children. Am J Clin Nutr. 2004; 80, 447–452.Google Scholar
44. Hill, DJ, Hogg, J. Growth factors and the regulation of pre- and postnatal growth. Baillieres Clin Endocrinol Metab. 1989; 3, 579–625.Google Scholar
45. Madsen, AL, Larnkjaer, A, Molgaard, C, Michaelsen, KF. IGF-I and IGFBP-3 in healthy 9 month old infants from the SKOT cohort: breastfeeding, diet, and later obesity. Growth Horm IGF Res. 2011; 21, 199–204.Google Scholar
46. Socha, P, Grote, V, Gruszfeld, D, et al. Milk protein intake, the metabolic-endocrine response, and growth in infancy: data from a randomized clinical trial. Am J Clin Nutr. 2011; 94(Suppl), 1776S–1784S.Google Scholar
47. Xu, RJ. Development of the newborn GI tract and its relation to colostrum/milk intake: a review. Reprod Fertil Dev. 1996; 8, 35–48.Google Scholar
48. Van Ginneken, C, Van Haver, E, Oste, M, Weyns, A. The presence of EGF and IGF-1-receptors in the small intestine of fetal, neonatal and weaned piglets. Livestock Sci. 2007; 108, 57–60.Google Scholar
49. Rao, RK, Philipps, AF, Williams, CS, McCracken, DM, Koldovsky, O. Luminal stability of insulin-like growth factors I and II in developing rat gastrointestinal tract. J Pediatr Gastroenterol Nutr. 1998; 26, 179–185.Google Scholar
50. Kimura, T, Murakawa, Y, Ohno, M, Ohtani, S, Higaki, K. Gastrointestinal absorption of recombinant human insulin-like growth factor-I in rats. J Pharmacol Exp Ther. 1997; 283, 611–618.Google Scholar
51. Xu, RJ, Wang, T. Gastrointestinal absorption of insulin-like growth factor-I in neonatal pigs. J Pediatr Gastroenterol Nutr. 1996; 23, 430–437.Google Scholar
52. Baumrucker, CR, Blum, JW. Effects of dietary recombinant human insulin-like growth factor-I on concentrations of hormones and growth factors in the blood of newborn calves. J Endocrinol. 1994; 140, 15–21.Google Scholar
53. Kim, WK, Ryu, YH, Seo, DS, Lee, CY, Ko, Y. Effects of oral administration of insulin-like growth factor-I on circulating concentration of insulin-like growth factor-I and growth of internal organs in weanling mice. Biol Neonate. 2006; 89, 199–204.Google Scholar
54. Burrin, DG, Davis, TA, Fiorotto, ML, Reeds, PJ. Role of milk-borne vs endogenous insulin-like growth factor I in neonatal growth. J Anim Sci. 1997; 75, 2739–2743.Google Scholar
55. Corpeleijn, WE, van Vliet, I, de Gast-Bakker, DA, et al. Effect of enteral IGF-1 supplementation on feeding tolerance, growth, and gut permeability in enterally fed premature neonates. J Pediatr Gastroenterol Nutr. 2008; 46, 184–190.Google Scholar
56. Donovan, SM, Odle, J. Growth factors in milk as mediators of infant development. Annu Rev Nutr. 1994; 14, 147–167.Google Scholar
57. Widdowson, EM, Colombo, VE, Artavanis, CA. Changes in the organs of pigs in response to feeding for the first 24 h after birth II. The digestive tract. Biol Neonate. 1976; 28, 272–281.Google Scholar
58. Widdowson, EM, Crabb, DE. Changes in the organs of pigs in response to feeding for the first 24 h after birth I. The internal organs and muscles. Biol Neonate. 1976; 28, 261–271.Google Scholar
59. Burrin, DG, Shulman, RJ, Reeds, PJ, Davis, TA, Gravitt, KR. Porcine colostrum and milk stimulate visceral organ and skeletal muscle protein synthesis in neonatal piglets. J Nutr. 1992; 122, 1205–1213.Google Scholar
60. Francis, GL, Upton, FM, Ballard, FJ, McNeil, KA, Wallace, JC. Insulin-like growth factors 1 and 2 in bovine colostrum. Sequences and biological activities compared with those of a potent truncated form. Biochem J. 1988; 251, 95–103.Google Scholar
61. Blum, JW, Baumrucker, CR. Insulin-like growth factors (IGFs), IGF binding proteins, and other endocrine factors in milk: role in the newborn. Adv Exp Med Biol. 2008; 606, 397–422.Google Scholar
62. Mero, A, Miikkulainen, H, Riski, J, et al. Effects of bovine colostrum supplementation on serum IGF-I, IgG, hormone, and saliva IgA during training. J Appl Physiol (1985). 1997; 83, 1144–1151.Google Scholar
63. Eriksson, U, Duc, G, Froesch, ER, Zapf, J. Insulin-like growth factors (IGF) I and II and IGF binding proteins (IGFBPs) in human colostrum/transitory milk during the first week postpartum: comparison with neonatal and maternal serum. Biochem Biophys Res Commun. 1993; 196, 267–273.CrossRefGoogle ScholarPubMed
64. Conover, WJ. Practical Nonparametric Statistics , 3rd edn, 1999. John Wiley & Sons, Inc.: New York.Google Scholar
65. Hinde, K, Power, ML, Oftedal, OT. Rhesus macaque milk: magnitude, sources, and consequences of individual variation over lactation. Am J Phys Anthropol. 2009; 138, 148–157.Google Scholar
66. Lonnerdal, B, Keen, CL, Glazier, CE, Anderson, J. A longitudinal study of rhesus monkey (Macaca mulatta) milk composition: trace elements, minerals, protein, carbohydrate, and fat. Pediat Res. 1984; 18, 911–914.Google Scholar
67. Laudenslager, ML, Natvig, C, Cantwell, H, Neville, MC, Reite, ML. Estimates of milk constituents from lactating bonnet macaque (Macaca radiata) mothers between two and seven months post-partum. J Med Primatol. 2010; 39, 368–373.Google Scholar
68. Baker, JL, Michaelsen, KF, Rasmussen, KM, Sorensen, TI. Maternal prepregnant body mass index, duration of breastfeeding, and timing of complementary food introduction are associated with infant weight gain. Am J Clin Nutr. 2004; 80, 1579–1588.Google Scholar
69. Dewey, KG. Nutrition, growth, and complementary feeding of the breastfed infant. Pediatr Clin North Am. 2001; 48, 87–104.Google Scholar
70. Houle, VM, Schroeder, EA, Odle, J, Donovan, SM. Small intestinal disaccharidase activity and ileal villus height are increased in piglets consuming formula containing recombinant human insulin-like growth factor-I. Pediatr Res. 1997; 42, 78–86.Google Scholar
71. Ma, L, Xu, RJ. Oral insulin-like growth factor-I stimulates intestinal enzyme maturation in newborn rats. Life Sci. 1997; 61, 51–58.Google Scholar
72. Molgaard, C, Larnkjaer, A, Mark, AB, Michaelsen, KF. Are early growth and nutrition related to bone health in adolescence? The Copenhagen Cohort Study of infant nutrition and growth. Am J Clin Nutr. 2011; 94(Suppl), 1865S–1869S.Google Scholar
73. Wood, CL, Stenson, C, Embleton, N. The developmental origins of osteoporosis. Curr Genomics. 2015; 16, 411–418.Google Scholar
74. Kind, KL, Owens, JA, Lok, F, et al. Intravenous infusion of insulin-like growth factor I in fetal sheep reduces hepatic IGF-I and IGF-II mRNAs. Am J Physiol. 1996; 271(Pt 2), R1632–R1637.Google Scholar
75. Butler, AA, Ambler, GR, Breier, BH, et al. Growth hormone (GH) and insulin-like growth factor-I (IGF-I) treatment of the GH-deficient dwarf rat: differential effects on IGF-I transcription start site expression in hepatic and extrahepatic tissues and lack of effect on type I IGF receptor mRNA expression. Mol Cell Endocrinol. 1994; 101, 321–330.Google Scholar
76. Gluckman, PD, Butler, AA. Endocrine/paracrine interactions following administration of insulin-like growth factor I. Acta Paediatr. 1994; 399, 180–182.Google Scholar
77. Vacher, PY, Bestetti, G, Blum, JW. Insulin-like growth factor I absorption in the jejunum of neonatal calves. Biol Neonate. 1995; 68, 354–367.Google Scholar
78. Gale, C, Logan, KM, Santhakumaran, S, et al. Effect of breastfeeding compared with formula feeding on infant body composition: a systematic review and meta-analysis. Am J Clin Nutr. 2012; 95, 656–669.Google Scholar
Supplementary material: File

Tay et al. supplementary material

Table S1

Download Tay et al. supplementary material(File)
File 35.4 KB