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High intakes of skimmed milk, but not meat, increase serum IGF-I and IGFBP-3 in eight-year-old boys

Abstract

Objective: To examine whether a high protein intake (PI) from either milk or meat, at a level often seen in late infancy, could increase s-IGF-I and s-IGF-I/s-IGFBP-3 in healthy, prepubertal children. IGF-I levels are positively associated with growth velocity in children and some studies suggest that a high animal PI can stimulate growth. During protein deprivation IGF-I decrease, but it is unknown whether a high PI can increase s-IGF-I in well-nourished children.

Design: In all, 24 8-y-old boys were asked to take either 1.5 l of skimmed milk (n=12) or the same amount of protein as 250 g low fat meat (n=12) daily for 7 days. The remaining diet they could choose freely. At baseline and after 7 days, anthropometrical variables were measured, diet was registered (3-day weighed records), and s-IGF-I and s-IGFBP-3 (RIA) were determined after fast.

Results: PI increased by 61% in the milk group to 4.0 g/kg/day (P<0.0001) and by 54% in the meat group to 3.8 g/kg/day (P=0.001). The high milk intake increased s-IGF-I by 19% (P=0.001) and s-IGF-I/s-IGFBP-3 by 13% (P<0.0001). There were no increases in the meat group.

Conclusions: High intake of milk and not meat, increased concentrations of s-IGF-I and s-IGF-I/s-IGFBP-3 significantly. Compounds in milk and not a high PI as such seem to stimulate IGF-I. This might explain the positive effect of milk intake on growth seen in some studies.

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References

  • Allen NE, Appleby PN, Davey GK, Kaaks R, Rinaldi S & Key TJ (2002): The associations of diet with serum insulin-like growth factor I and its main binding proteins in 292 women meat-eaters, vegetarians, and vegans. Cancer Epidemiol. Biomarkers Prev. 11, 1441–1448.

    CAS  PubMed  Google Scholar 

  • Bang P, Eriksson U, Sara V, Wivall IL & Hall K (1991): Comparison of acid ethanol extraction and acid gel filtration prior to IGF-I and IGF-II radioimmunoassays: improvement of determinations in acid ethanol extracts by the use of truncated IGF-I as radioligand. Acta Endocrinol. (Copenh.) 124, 620–629.

    CAS  Article  Google Scholar 

  • Barker DJP (1992): Fetal and Infant Origin of Adult Disease. London: British Medical Association.

    Google Scholar 

  • Black RE, Williams SM, Jones IE & Goulding A (2002): Children who avoid drinking cow milk have low dietary calcium intakes and poor bone health. Am. J. Clin. Nutr. 76, 675–680.

    CAS  Article  Google Scholar 

  • Blum WF, Ranke MB, Kietzmann K, Gauggel E, Zeisel HJ & Bierich JR (1990): A specific radioimmunoassay for the growth hormone (GH)-dependent somatomedin-binding protein: its use for diagnosis of GH deficiency. J. Clin. Endocrinol. Metab. 70, 1292–1298.

    CAS  Article  Google Scholar 

  • Cadogan J, Eastell R, Jones N & Barker ME (1997): Milk intake and bone mineral acquisition in adolescent girls: randomised, controlled intervention trial. Br. Med. J. 315, 1255–1260.

    CAS  Article  Google Scholar 

  • Chan JM, Stampfer MJ, Giovannucci E, Gann PH, Ma J, Wilkinson P, Hennekens CH & Pollak M (1998): Plasma insulin-like growth factor-I and prostate cancer risk: a prospective study. Science 279, 563–566.

    CAS  Article  Google Scholar 

  • Clemmons DR, Seek MM & Underwood LE (1985): Supplemental essential amino acids augment the somatomedin-C/insulin- like growth factor I response to refeeding after fasting. Metabolism 34, 391–395.

    CAS  Article  Google Scholar 

  • Dardevet D, Manin M, Balage M, Sornet C & Grizard J (1991): Influence of low- and high-protein diets on insulin and insulin-like growth factor-1 binding to skeletal muscle and liver in the growing rat. Br. J. Nutr. 65, 47–60.

    CAS  Article  Google Scholar 

  • Daxenberger A, Breier BH & Sauerwein H (1998): Increased milk levels of insulin-like growth factor 1 (IGF-1) for the identification of bovine somatotropin (bST) treated cows. Analyst 123, 2429–2435.

    CAS  Article  Google Scholar 

  • Devine A, Rosen C, Mohan S, Baylink D & Prince RL (1998): Effects of zinc and other nutritional factors on insulin-like growth factor I and insulin-like growth factor binding proteins in postmenopausal women. Am. J. Clin. Nutr. 68, 200–206.

    CAS  Article  Google Scholar 

  • DiMeglio DP & Mattes RD (2000): Liquid versus solid carbohydrate: effects on food intake and body weight. Int. J. Obes. Relat. Metab. Disord. 24, 794–800.

    CAS  Article  Google Scholar 

  • Dreizen S, Currie C, Gilley EJ & Spies TD (1950): The effect of milk supplements on the growth of children with nutritive failure. 2. Height and weight changes. Growth 14, 189–211.

    CAS  PubMed  Google Scholar 

  • Dreizen S, Snodgrasse RM, Parker GS, Currie C & Spies TD (1954): Maturation of bone centers in hand and wrist of children with chronic nutritive failure. Effect of dietary supplements of reconstituted milk solids. Am. J. Dis. Child. 87, 429–439.

    CAS  Google Scholar 

  • Fall CH, Vijayakumar M, Barker DJ, Osmond C & Duggleby S (1995): Weight in infancy and prevalence of coronary heart disease in adult life. BMJ 310, 17–19.

    CAS  Article  Google Scholar 

  • Fomon SJ (1993): Protein, In Nutrition of Normal Infants. ed. SJ Fomon, pp 121–146. St. Louis: Mosby.

    Google Scholar 

  • Giovannucci E, Pollak MN, Platz EA, Willett WC, Stampfer MJ, Majeed N, Colditz GA, Speizer FE & Hankinson SE (2000): A prospective study of plasma insulin-like growth factor-1 and binding protein-3 and risk of colorectal neoplasia in women. Cancer Epidemiol. Biomarkers Prev. 9, 345–349.

    CAS  PubMed  Google Scholar 

  • Giovannucci E, Pollak M, Liu Y, Platz EA, Majeed N, Rimm EB & Willett WC (2003): Nutritional predictors of insulin-like growth factor I and their relationships to cancer in men. Cancer Epidemiol. Biomarkers Prev. 12, 84–89.

    CAS  PubMed  Google Scholar 

  • Hankinson SE, Willett WC, Colditz GA, Hunter DJ, Michaud DS, Deroo B, Rosner B, Speizer FE & Pollak M (1998): Circulating concentrations of insulin-like growth factor-I and risk of breast cancer. Lancet 351, 1393–1396.

    CAS  Article  Google Scholar 

  • Heaney RP, McCarron DA, Dawson-Hughes B, Oparil S, Berga SL, Stern JS, Barr SI & Rosen CJ (1999): Dietary changes favorably affect bone remodeling in older adults. J. Am. Diet. Assoc. 99, 1228–1233.

    CAS  Article  Google Scholar 

  • Holmes MD, Pollak MN, Willett WC & Hankinson SE (2002): Dietary correlates of plasma insulin-like growth factor I and insulin-like growth factor binding protein 3 concentrations. Cancer Epidemiol. Biomarkers Prev. 11, 852–861.

    CAS  PubMed  Google Scholar 

  • Isley WL, Underwood LE & Clemmons DR (1983): Dietary components that regulate serum somatomedin-C concentrations in humans. J. Clin. Invest. 71, 175–182.

    CAS  Article  Google Scholar 

  • Isley WL, Underwood LE & Clemmons DR (1984): Changes in plasma somatomedin-C in response to ingestion of diets with variable protein and energy content. J. Parenter. Enteral. Nutr. 8, 407–411.

    CAS  Article  Google Scholar 

  • Juskevich JC & Guyer CG (1990): Bovine growth hormone: human food safety evaluation. Science 249, 875–884.

    CAS  Article  Google Scholar 

  • Juul A, Bang P, Hertel NT, Main K, Dalgaard P, Jorgensen K, Muller J, Hall K & Skakkebaek NE (1994): 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. 78, 744–752.

    CAS  Google Scholar 

  • Juul A, Dalgaard P, Blum WF, Bang P, Hall K, Michaelsen KF, Muller J & Skakkebaek NE (1995): Serum levels of insulin-like growth factor (IGF)-binding protein-3 (IGFBP-3) in healthy infants, children, and adolescents: the relation to IGF-I, IGF-II, IGFBP-1, IGFBP-2, age, sex, body mass index, and pubertal maturation. J. Clin. Endocrinol. Metab. 80, 2534–2542.

    CAS  PubMed  Google Scholar 

  • Juul A, Scheike T, Davidsen M, Gyllenborg J & Jorgensen T (2002): Low serum insulin-like growth factor I is associated with increased risk of ischemic heart disease: a population-based case–control study. Circulation 106, 939–944.

    CAS  Article  Google Scholar 

  • Lampl M, Johnston FE & Malcolm LA (1978): The effects of protein supplementation on the growth and skeletal maturation of New Guinean school children. Ann. Hum. Biol. 5, 219–227.

    CAS  Article  Google Scholar 

  • Ma J, Pollak MN, Giovannucci E, Chan JM, Tao Y, Hennekens CH & Stampfer MJ (1999): Prospective study of colorectal cancer risk in men and plasma levels of insulin-like growth factor (IGF)-I and IGF-binding protein-3. J. Natl. Cancer Inst. 91, 620–625.

    CAS  Article  Google Scholar 

  • Ma J, Giovannucci E, Pollak M, Chan JM, Gaziano JM, Willett W & Stampfer MJ (2001): Milk intake, circulating levels of insulin-like growth factor-I, and risk of colorectal cancer in men. J. Natl. Cancer Inst. 93, 1330–1336.

    CAS  Article  Google Scholar 

  • Nap RC, Mol JA & Hazewinkel HA (1993): Age-related plasma concentrations of growth hormone (GH) and insulin-like growth factor-I (IGF-I) in Great Dane pups fed different dietary levels of protein. Domest. Anim. Endocrinol. 10, 237–247.

    CAS  Article  Google Scholar 

  • Orr JB (1928): Milk consumption and the growth of school-children. Lancet i, 202–203.

    Article  Google Scholar 

  • Playford RJ, Macdonald CE & Johnson WS (2000): Colostrum and milk-derived peptide growth factors for the treatment of gastrointestinal disorders. Am. J. Clin. Nutr. 72, 5–14.

    CAS  Article  Google Scholar 

  • Rolland-Cachera MF (1995): Prediction of adult body composition from infant and child measurements, In Body Composition Techniques in Health and Disease. eds. PSW Davies & TJ Cole, pp 100–145. Cambridge: Cambridge University Press.

    Chapter  Google Scholar 

  • Rolland-Cachera MF, Deheeger M & Bellisle F (1999): Increasing prevalence of obesity among 18-year-old males in Sweden: evidence for early determinants. Acta Paediatr. 88, 365–367.

    CAS  Article  Google Scholar 

  • Schürch MA, Rizzoli R, Slosman D, Vadas L, Vergnaud P & Bonjour JP (1998): Protein supplements increase serum insulin-like growth factor-I levels and attenuate proximal femur bone loss in patients with recent hip fracture. A randomized, double-blind, placebo-controlled trial. Ann. Intern. Med. 128, 801–809.

    Article  Google Scholar 

  • Smith IF, Taiwo O & Payne-Robinson HM (1989): Plasma somatomedin-C in Nigerian malnourished children fed a vegetable protein rehabilitation diet. Eur. J. Clin. Nutr. 43, 705–713.

    CAS  PubMed  Google Scholar 

  • Smith WJ, Underwood LE & Clemmons DR (1995): Effects of caloric or protein restriction on insulin-like growth factor-I (IGF-I) and IGF-binding proteins in children and adults. J. Clin. Endocrinol. Metab. 80, 443–449.

    CAS  PubMed  Google Scholar 

  • Storm D, Eslin R, Porter ES, Musgrave K, Vereault D, Patton C, Kessenich C, Mohan S, Chen T, Holick MF & Rosen CJ (1998): Calcium supplementation prevents seasonal bone loss and changes in biochemical markers of bone turnover in elderly New England women: a randomized placebo-controlled trial. J. Clin. Endocrinol. Metab. 83, 3817–3825.

    CAS  PubMed  Google Scholar 

  • Thissen JP, Ketelslegers JM & Underwood LE (1994): Nutritional regulation of the insulin-like growth factors. Endocr. Rev. 15, 80–101.

    CAS  Google Scholar 

  • Wastney ME, Martin BR, Peacock M, Smith D, Jiang XY, Jackman LA & Weaver CM (2000): Changes in calcium kinetics in adolescent girls induced by high calcium intake. J. Clin. Endocrinol. Metab. 85, 4470–4475.

    CAS  PubMed  Google Scholar 

  • Xian CJ, Shoubridge CA & Read LC (1995): Degradation of IGF-I in the adult rat gastrointestinal tract is limited by a specific antiserum or the dietary protein casein. J. Endocrinol. 146, 215–225.

    CAS  Article  Google Scholar 

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Acknowledgements

The idea for this study came from a discussion between the authors. No author had a financial or personal conflict of interest related to this research or its source of funding.

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Guarantor: C Hoppe.

Contributors: CH conducted the statistical analyses and prepared the first draft of the manuscript in collaboration with CM and KFM. AJ was responsible for all IGF-I and IGFBP-3 measurements. All contributors participated in interpreting the results and were involved in preparing the final draft of the manuscript.

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Correspondence to C Hoppe.

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Hoppe, C., Mølgaard, C., Juul, A. et al. High intakes of skimmed milk, but not meat, increase serum IGF-I and IGFBP-3 in eight-year-old boys. Eur J Clin Nutr 58, 1211–1216 (2004). https://doi.org/10.1038/sj.ejcn.1601948

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Keywords

  • dietary protein
  • children
  • insulin-like growth factor-I
  • insulin-like growth factor binding protein-3
  • milk
  • meat

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