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Milk as a food for growth? The insulin-like growth factors link

Published online by Cambridge University Press:  02 January 2007

Imogen Rogers ,
Pauline Emmett ,
David Gunnell ,
David Dunger  and
Jeff Holly
Imogen Rogers*
Affiliation:
Unit of Paediatric and Perinatal Epidemiology, Division of Community Medicine, University of Bristol, 24 Tyndall Avenue, Bristol BS8 1TQ, UK
Pauline Emmett
Affiliation:
Unit of Paediatric and Perinatal Epidemiology, Division of Community Medicine, University of Bristol, 24 Tyndall Avenue, Bristol BS8 1TQ, UK
David Gunnell
Affiliation:
Department of Social Medicine, University of Bristol, Canynge Hall, Whiteladies Road, Bristol BS8 2PR, UK
David Dunger
Affiliation:
Department of Paediatrics, University of Cambridge, Addenbrookes Hospital, Level 8, Box 116, Cambridge CB2 2QQ, UK
Jeff Holly
Affiliation:
Division of Surgery, University of Bristol, Bristol BS8 2HW, UK
*
*Corresponding author: Email Imogen.Rogers@bristol.ac.uk
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Abstract

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Objective

The mechanisms underlying the association of insulin-like growth factor-I (IGF-I) and leg length (a marker of prepubertal growth) with cancer risk are uncertain. One hypothesis is that diet in early childhood might provide the link. The aim of the present study was to examine the association between early diet – in particular, the intakes of cows' milk and dairy products – and height, leg length and IGF-I levels at age 7–8 years.

Subjects

Children participating in the Avon Longitudinal Study of Parents and Children.

Design

Diet was assessed using a 3-day unweighed food record. Anthropometry, IGF-I and insulin-like growth factor-binding protein-3 (IGFBP-3) were measured by standard methods.

Results

Data on both diet and height were available for 744 children (404 boys) and on diet and IGF for 538 (295 boys). After adjusting for energy, both cows' milk and dairy product intakes were positively associated with IGF-I (P=0.040 and 0.027, respectively) and IGFBP-3 levels (P=0.082 and 0.067, respectively). These associations persisted on adjustment for potential confounders, but were abolished on controlling for protein intake. In energy-adjusted models there was only weak evidence of associations of milk and dairy product intakes with anthropometry. In boys only, dairy product intake was positively associated with leg length (equivalent to a 0.058 (0.002, 0.114) standard deviation score increase in leg length per 100 g increase in daily intake).

Conclusions

These data provide some evidence that variation in childhood milk and dairy product intakes underlies associations of leg length, IGF-I and cancer risk. The association appears to be due to the protein content of milk.

Keywords

Insulin-like growth factorsMilkDairy productsProteinChildrenGrowthLeg length
Type
Research Article
Information
Public Health Nutrition , Volume 9 , Issue 3 , May 2006 , pp. 359 - 368
Copyright
Copyright © The Authors 2006

References

1Gunnell, D, Okasha, M, Davey Smith, G, Oliver, S, Sandhu, J, Holly, J. Height, leg length, and cancer risk: a systematic review. Epidemiologic Reviews 2001; 23: 313–42.CrossRefGoogle ScholarPubMed
2Gerver, W, Bruin, R. Relationship between height, sitting height and subischial leg length in Dutch children: presentation of normal values. Acta Paediatrica 1995; 84: 532–5.CrossRefGoogle ScholarPubMed
3Gunnell, D, Davey Smith, G, Holly, J, Frankel, S. Leg length and risk of cancer in the Boyd Orr cohort. British Medical Journal 1998; 317: 1350–1.CrossRefGoogle ScholarPubMed
4Gunnell, D. Commentary: Can adult anthropometry be used as a ‘biomarker’ for prenatal and childhood exposures? International Journal of Epidemiology 2002; 31: 390–4.CrossRefGoogle ScholarPubMed
5Butler, A, Le Roith, D. Control of growth by the somatropic axis: growth hormone and the insulin-like growth factors have related and independent roles. Annual Review of Physiology 2001; 63: 141–64.CrossRefGoogle ScholarPubMed
6Juul, A, Dalgaard, P, Blum, W. 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. Journal of Clinical Endocrinology and Metabolism 1995; 80: 2534–42.Google ScholarPubMed
7Chan, J, Stampfer, M, Giovannucci, E, Gann, PH, Ma, J, Wilkinson, P, et al. Plasma insulin-like growth factor-I and prostate cancer risk: a prospective study. Science 1998; 279: 563–6.CrossRefGoogle ScholarPubMed
8Wolk, A, Mantzoros, CS, Andersson, SO, Bergstrom, R, Signorello, LB, Lagiou, P, et al. Insulin-like growth factor I and prostate cancer risk: a population-based case-control study. Journal of the National Cancer Institute 1998; 90: 911–5.CrossRefGoogle Scholar
9Hankinson, S, Willett, W, Colditz, G, Hunter, D, Michaud, D, Deroo, B, et al. Circulating concentrations of insulin-like growth factor I and risk of breast cancer. Lancet 1998; 351: 1393–6.CrossRefGoogle ScholarPubMed
10Ma, J, Giovannucci, E, Pollak, M, Chan, J, Gaziano, J, Willett, W, et al. Milk intake, circulating levels of insulin-like growth factor-I, and risk of colorectal cancer in men. Journal of the National Cancer Institute 2001; 93: 1330–6.CrossRefGoogle ScholarPubMed
11Yu, H, Rohan, T. Role of the insulin-like growth factor family in cancer development and progression. Journal of the National Cancer Institute 2000; 92: 1472–89.CrossRefGoogle ScholarPubMed
12Giovannucci, E. Insulin, insulin-like growth factors and colon cancer: a review of the evidence. Journal of Nutrition 2001; 131(Suppl.): S3109–20.CrossRefGoogle ScholarPubMed
13Renehan, A, Zwahler, M, Minder, C, O'Dwyer, S, Shalet, S, Egger, M. Insulin-like growth factor (IGF)-I, IGF binding protein 3 and cancer risk: systematic review and meta-regression analysis. Lancet 2004; 363: 1346–53.CrossRefGoogle ScholarPubMed
14Kristal, AR, Cohen, J, Qu, P, Stanford, JL. Associations of energy, fat, calcium and vitamin D with prostate cancer risk. Cancer Epidemiology, Biomarkers & Prevention 2002; 11: 719–25.Google ScholarPubMed
15Giovannucci, E, Rimm, E, Stampfer, M, Colditz, G, Ascherio, A, Willett, W. Intake of fat, meat and fiber in relation to risk of colon cancer in men. Cancer Research 1994; 54: 2390–7.Google ScholarPubMed
16Kolonel, L. Fat, meat and prostate cancer. Epidemiologic Reviews 2001; 23: 72–81.CrossRefGoogle ScholarPubMed
17Chan, J, Giovannucci, E. Dairy products, calcium, vitamin D and risk of prostate cancer. Epidemiologic Reviews 2001; 23: 87–92.CrossRefGoogle ScholarPubMed
18World Cancer Research Fund (WCRF)/American Institute for Cancer Research (AICR). Food, Nutrition and the Prevention of Cancer: A Global Perspective. Washington, DC: WCRF/AICR, 1997.Google Scholar
19Trichopoulou, A, Katsouyanni, K, Stuver, S, Tzala, L, Gnardellis, C, Rimm, E, et al. Consumption of olive oil and specific food groups in relation to breast cancer risk in Greece. Journal of the National Cancer Institute 1995; 87: 110–6.CrossRefGoogle ScholarPubMed
20Chan, J, Giovannucci, E. Vegetables, fruits, associated micronutrients and risk of prostate cancer. Epidemiologic Reviews 2001; 23: 82–6.CrossRefGoogle ScholarPubMed
21Freudenheim, JL, Marshall, J, Vena, J, Laughlin, J, Brasure, J, Swanson, M, et al. Premenopausal breast cancer risk and intake of vegetables, fruits and related nutrients. Journal of the National Cancer Institute 1996; 88: 340–8.CrossRefGoogle ScholarPubMed
22Key, T, Allen, N, Spencer, E, Travis, R. The effect of diet on risk of cancer. Lancet 2002; 360: 861–8.CrossRefGoogle ScholarPubMed
23Giovannucci, E, Pollak, M, Liu, Y, Platz, E, Majeed, N, Rimm, E, et al. Nutritional predictors of insulin-like growth factor I and their relationships to cancer in men. Cancer Epidemiology, Biomarkers & Prevention 2003; 12: 84–9.Google ScholarPubMed
24Gunnell, D, Oliver, S, Peters, T, Donovan, J, Persad, R, Maynard, M, et al. Are diet–prostate cancer associations mediated by the IGF axis? A cross-sectional analysis of diet, IGF-I and IGFBP-3 in middle-aged men. British Journal of Cancer 2003; 88: 1682–6.CrossRefGoogle Scholar
25Holmes, M, Pollak, M, Willett, W, Hankinson, S. Dietary correlates of plasma insulin-like growth factor I and insulin-like growth factor binding protein 3 concentrations. Cancer Epidemiology, Biomarkers & Prevention 2002; 11: 852–61.Google ScholarPubMed
26Allen, N, Appleby, P, Davey, G, Kaaks, R, Rinaldi, S, Key, T. 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 Epidemiology, Biomarkers & Prevention 2002; 11: 1441–8.Google ScholarPubMed
27Signorello, L, Kuper, H, Lagiou, P, Mucci, L, Trichopoulos, D, Adami, HO. Lifestyle factors and insulin-like growth factor I levels among elderly men. European Journal of Cancer Prevention 2000; 9: 173–8.CrossRefGoogle ScholarPubMed
28Mucci, L, Tamimi, R, Lagiou, P, Trichopoulou, A, Benetou, V, Spanos, E, et al. Are dietary influences on the risk of prostate cancer mediated through the insulin-like growth factor system? BJU International 2001; 87: 814–20.CrossRefGoogle ScholarPubMed
29Heaney, RP, McCarron, D, Dawson-Huges, B, Oparil, S, Berga, S, Stern, J, et al. Dietary changes favorably affect bone remodeling in older adults. Journal of the American Dietetic Association 1999; 99: 1228–33.CrossRefGoogle ScholarPubMed
30Cadogan, J, Eastell, R, Jones, N, Barker, M. Milk intake and bone mineral acquisition in adolescent girls: randomised, controlled intervention trial. British Medical Journal 1997; 315: 1255–60.CrossRefGoogle ScholarPubMed
31Hoppe, C, Mølgaard, C, Juul, A, Michaelsen, K. High intakes of skimmed milk, but not meat, increase serum IGF-I and IGFBP-3 in eight-year-old boys. European Journal of Clinical Nutrition 2004; 58: 1211–6.CrossRefGoogle Scholar
32Frankel, S, Gunnell, DJ, Peters, TJ, Maynard, M, Davey Smith, G. Childhood energy intake and adult mortality from cancer: the Boyd Orr Cohort Study. British Medical Journal 1998; 316: 499–504.CrossRefGoogle ScholarPubMed
33Hoppe, C, Udam, T, Lauritzen, L, Mølgaard, C, Juul, A, Michaelsen, K. Animal protein intake, serum insulin-like growth factor I, and growth in healthy 2.5-y-old Danish children. American Journal of Clinical Nutrition 2004; 80: 447–52.CrossRefGoogle Scholar
34Golding, J, Pembrey, M, Jones, R. ALSPAC Study Team. ALSPAC – The Avon Longitudinal Study of Parents and Children. I. Study methodology. Paediatric and Perinatal Epidemiology 2001; 15: 74–87.CrossRefGoogle Scholar
35 ALSPAC website, http://www.alspac.bris.ac.ukGoogle Scholar
36Price, GM, Paul, AA, Key, FB, Harter, AC, Cole, TJ, Day, KC, et al. Measurement of diet in a large national survey: comparison of computerised and manual coding of records in household measures. Journal of Human Nutrition and Dietetics 1995; 8: 417–28.CrossRefGoogle Scholar
37Holland, B, Welch, AA, Unwin, ID, Buss, DH, Paul, AA, Southgate, DAT. McCance & Widdowson's The Composition of Foods, 5th ed. Cambridge: The Royal Society of Chemistry, 1991.Google Scholar
38Holland, B, Unwin, ID, Buss, DH. Cereals and Cereal Products. Third Supplement to McCance & Widdowson's The Composition of Foods, 4th ed. Cambridge: The Royal Society of Chemistry, 1988.Google Scholar
39Holland, B, Unwin, ID, Buss, DH. Milk Products and Eggs. Fourth Supplement to McCance & Widdowson's The Composition of Foods, 4th ed. Cambridge: The Royal Society of Chemistry, 1989.Google Scholar
40Holland, B, Unwin, ID, Buss, DH. Vegetables, Herbs and Spices. Fifth Supplement to McCance & Widdowson's The Composition of Foods, 4th ed. Cambridge: The Royal Society of Chemistry, 1991.CrossRefGoogle Scholar
41Holland, B, Unwin, ID, Buss, DH. Fruit and Nuts. First Supplement to McCance & Widdowson's The Composition of Foods, 5th ed. Cambridge: The Royal Society of Chemistry, 1992.CrossRefGoogle Scholar
42Holland, B, Welch, AA, Buss, DH. Vegetable Dishes. Second Supplement to McCance & Widdowson's The Composition of Foods, 5th ed. Cambridge: The Royal Society of Chemistry, 1992.Google Scholar
43Holland, B, Brown, J, Buss, DH. Fish and Fish Products. Third Supplement to McCance & Widdowson's The Composition of Foods, 5th ed. Cambridge: The Royal Society of Chemistry, 1993.CrossRefGoogle Scholar
44Chan, W, Brown, J, Buss, DH. Miscellaneous Foods. Fourth Supplement to McCance & Widdowson's The Composition of Foods. 5th ed. Cambridge: The Royal Society of Chemistry, 1994.CrossRefGoogle Scholar
45Chan, W, Brown, J, Lee, SM, Buss, DH. Meat, Poultry and Game. Fifth Supplement to McCance & Widdowson's The Composition of Foods, 5th ed. Cambridge: The Royal Society of Chemistry, 1995.CrossRefGoogle Scholar
46Chan, W, Brown, J, Church, SM, Buss, DH. Meat Products and Dishes. Sixth Supplement to McCance & Widdowson's The Composition of Foods, 5th ed. Cambridge: The Royal Society of Chemistry, 1996.CrossRefGoogle Scholar
47Cameron, N. The methods of auxological anthropometry. In: Falkner, F, Tanner, JM, eds. Human Growth: A Comprehensive Treatise 3. New York/London: Plenum Press, 1986; 3–46.Google Scholar
48Lemmey, A, Maddison, P, Breslin, A, Cassar, P, Hasso, N, McCann, R, et al. Association between insulin-like growth factor status and physical activity levels in rheumatoid arthritis. Journal of Rheumatology 2001; 28: 29–34.Google ScholarPubMed
49Willett, W, Stampfer, M. Total energy intake: implications for epidemiologic analyses. American Journal of Epidemiology 1986; 124: 17–27.CrossRefGoogle ScholarPubMed
50Garnett, S, Cowell, C, Bradford, D, Lee, J, Tao, C, Petrauskas, V, et al. Effects of gender, body composition and birth size on IGF-I in 7- and 8-year-old children. Hormone Research 1999; 52: 221–9.CrossRefGoogle ScholarPubMed
51Torun, B, Davies, P, Livingstone, MBE, Paolisso, M, Sackett, R, Spurr, GB. Energy requirements and dietary energy recommendations for children and adolescents 1 to 18 years old. European Journal of Clinical Nutrition 1996; 50(Suppl.1): S37–81.Google ScholarPubMed
52Freeman, JV, Cole, TJ, Chinn, S, Jones, PRM, White, EM, Preece, MA. Cross sectional stature and weight reference curves for the UK, 1990. Archives of Disease in Childhood 1995; 73: 17–24.CrossRefGoogle ScholarPubMed
53Gunnell, D, Oliver, SE, Donovan, JL, Peters, TJ, Gillatt, D, Persad, R, et al. Do height-related variations in insulin-like growth factors underlie the associations of stature with adult chronic disease? Journal of Clinical Endocrinology and Metabolism 2004; 89: 213–8.CrossRefGoogle ScholarPubMed
54DeLellis, K, Rinaldi, S, Kaaks, R, Kolonel, L, Henderson, B, Le Marchand, L. Dietary and lifestyle correlates of plasma insulin-like growth factor-I (IGF-I) and IGF binding protein 3 (IGFBP-3): The Multiethnic Cohort. Cancer Epidemiology, Biomarkers & Prevention 2004; 13: 1444–51.CrossRefGoogle Scholar
55Bingham, SA, Gill, C, Welch, A, Day, K, Cassidy, A, Khaw, KT, et al. Comparison of dietary assessment methods in nutritional epidemiology: weighed records v. 24?h recalls, food-frequency questionnaires and estimated-diet records. British Journal of Nutrition 1994; 72: 619–43.CrossRefGoogle Scholar
56Thissen, J, Ketelslegers, J, Underwood, L. Nutritional regulation of the insulin-like growth factors. Endocrine Reviews 1994; 15: 80–101.Google ScholarPubMed
57Juul, A, Scheike, F, Davidsen, M, Gyllenborg, J, Jorgensen, T. Low serum insulin-like growth factor I is associated with increased risk of ischaemic heart disease. Circulation 2002; 106: 939–44.CrossRefGoogle Scholar
58Sandhu, M, Heald, A, Gibson, J, Cruickshank, J, Dunger, DB, Wareham, N. Circulating concentrations of insulin-like growth factor-I and development of glucose intolerance: a prospective observational study. Lancet 2002; 359: 1740–5.CrossRefGoogle ScholarPubMed