Hostname: page-component-586b7cd67f-r5fsc Total loading time: 0 Render date: 2024-11-20T10:21:28.306Z Has data issue: false hasContentIssue false
  • English
  • Français

Dietary intake and the insulin-like growth factor system: effects of migration in two related populations in India and Britain with markedly different dietary intake

Published online by Cambridge University Press:  02 January 2007

AH Heald ,
R Sharma ,
SG Anderson ,
A Vyas ,
K Siddals ,
J Patel ,
D Bhatnagar ,
D Prabharkaran ,
A Rudenski  and
E Hughes
...Show all authors
AH Heald*
Affiliation:
University of Manchester, Salford Royal Hospitals University Trust, Hope Hospital, Stott Lane, Salford, Greater Manchester, M6 8HD, UK
R Sharma
Affiliation:
University of Manchester, Salford Royal Hospitals University Trust, Hope Hospital, Stott Lane, Salford, Greater Manchester, M6 8HD, UK
SG Anderson
Affiliation:
Clinical Epidemiology Group, University of Manchester Medical School, Manchester M13 9PT, UK
A Vyas
Affiliation:
Clinical Epidemiology Group, University of Manchester Medical School, Manchester M13 9PT, UK
K Siddals
Affiliation:
University of Manchester, Salford Royal Hospitals University Trust, Hope Hospital, Stott Lane, Salford, Greater Manchester, M6 8HD, UK
J Patel
Affiliation:
Clinical Epidemiology Group, University of Manchester Medical School, Manchester M13 9PT, UK
D Bhatnagar
Affiliation:
University Department of Medicine, Manchester Royal Infirmary, Manchester M13 9WL, UK
D Prabharkaran
Affiliation:
All India Institute of Medical Sciences, New Delhi, India
A Rudenski
Affiliation:
University of Manchester, Salford Royal Hospitals University Trust, Hope Hospital, Stott Lane, Salford, Greater Manchester, M6 8HD, UK
E Hughes
Affiliation:
Department of Clinical Biochemistry, Sandwell General Hospital, Birmingham, UK
P Durrington
Affiliation:
University Department of Medicine, Manchester Royal Infirmary, Manchester M13 9WL, UK
JM Gibson
Affiliation:
University of Manchester, Salford Royal Hospitals University Trust, Hope Hospital, Stott Lane, Salford, Greater Manchester, M6 8HD, UK
JK Cruickshank
Affiliation:
Clinical Epidemiology Group, University of Manchester Medical School, Manchester M13 9PT, UK
*
*Corresponding author: Email [email protected]
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.
Background

The insulin-like growth factor (IGF) system is implicated in the pathogenesis of diabetes and cardiovascular disease.

Objective

We report the effects of total energy intake on the IGF system in two populations with markedly different dietary macronutrient intake and cardiovascular event rate.

Design, subjects and setting

Dietary macronutrient intake was measured in a specific Gujarati migrant community in Sandwell, UK (n = 205) compared with people still resident in the same villages of origin in India (n = 246). Fasting IGF-I, IGF-binding protein (IGFBP)-1 and IGFBP-3, insulin and glucose (0 and 2-hour) were measured.

Results

Total energy and total fat intake were higher in UK migrants, as were IGFBP-3 and IGF-I (mean (95% confidence interval): 145.9 (138.1–153.6) vs. 100.9 (94.6–107.3) ng ml-1; F = 76.6, P < 0.001). IGFBP-1 was lower in UK migrants (29.5 (25.9–33.0) vs. 56.5 (50.6–62.5) μg l-1; F = 48.4, P < 0.001). At both sites, IGF-I correlated positively with total energy (Spearman's ρ = 0.45, P < 0.001) and total fat (ρ = 0.44, P < 0.001) as did IGFBP-3 with total energy (ρ = 0.21, P < 0.05) and fat (ρ = 0.26, P < 0.001). Conversely, in Indian Gujaratis, IGFBP-1 fell with increasing total energy (ρ = -0.27, P < 0.001) and fat intake (ρ = -0.26, P < 0.01) but not in UK Gujaratis. Multiple linear regression modelling showed that increasing quartiles of fat intake were associated with higher IGF-I (β = 0.42, P = 0.007) independent of age, body mass index, plasma insulin, fatty acids and 2-hour glucose.

Conclusion

In these genetically similar groups, migration to the UK and adoption of a different diet is associated with marked changes in the IGF system, suggesting that environmental factors profoundly modulate serum concentrations and actions of IGFs.

Keywords

Insulin-like growth factorsInsulin-like growth factor binding proteinsDietEthnicityMigration
Type
Research Article
Information
Public Health Nutrition , Volume 8 , Issue 6 , September 2005 , pp. 620 - 627
Copyright
Copyright © The Authors 2005

References

1Keys, A. Coronary heart disease – the global picture. Atherosclerosis 1975; 22: 149–92.Google Scholar
2Grande, F, Anderson, JT, Keys, A. Comparison of effects of palmitic and stearic acids in the diet on serum cholesterol in man. American Journal of Clinical Nutrition 1970; 23: 1184–93.CrossRefGoogle ScholarPubMed
3Sirtori, CR, Tremoli, E, Gatti, E, Montanari, G, Sirtori, M, Colli, S, et al. Controlled evaluation of fat intake in the Mediterranean diet: comparative activities of olive oil and corn oil on plasma lipids and platelets in high-risk patients. American Journal of Clinical Nutrition 1986; 44: 635–42.CrossRefGoogle ScholarPubMed
4Fath, KA, Alexander, RW, Delafontaine, P. Abdominal coarctation increases insulin-like growth factor I mRNA levels in rat aorta. Circulation Research 1993; 72: 271–7.CrossRefGoogle ScholarPubMed
5Ververis, JJ, Ku, L, Delafontaine, P. Regulation of insulin-like growth factor I receptors on vascular smooth muscle cells by growth factors and phorbol esters. Circulation Research 1993; 72: 1285–92.CrossRefGoogle ScholarPubMed
6Delafontaine, P. Insulin-like growth factor I and its binding proteins in the cardiovascular system. Cardiovascular Research 1995; 30: 825–34.CrossRefGoogle ScholarPubMed
7Duerr, RL, Huang, S, Miraliakbar, HR, Clark, R, Chien, KR, Ross J, Jr. Insulin-like growth factor-I enhances ventricular hypertrophy and function during the onset of experimental heart failure. Journal of Clinical Investigation 1995; 95: 619–27.Google Scholar
8Li, Q, Li, B, Wang, X, Leri, A, Jana, KP, Liu, Y, et al. Overexpression of insulin-like growth factor-I in mice protects from myocyte death after infarction, attenuating ventricular wall dilatation, wall stress and cardiac hypertrophy. Journal of Clinical Investigation 1997; 100: 1991–9.Google Scholar
9Mehrhof, FB, Müller, FU, Bergmann, MW, Li, P, Yibin Wang, Y, Schmitz, W, et al. In cardiomyocyte hypoxia, insulin-like growth factor-I-induced antiapoptotic signaling requires phosphatidylinositol-3-OH-kinase-dependent and mitogen-activated protein kinase-dependent activation of the transcription factor cAMP response element-binding protein. Circulation 2001; 104: 2088–94.CrossRefGoogle ScholarPubMed
10Vaessen, N, Heutink, P, Janssen, JA, Witteman, JC, Testers, L, Hofman, A, et al. A polymorphism in the gene for IGF-I: functional properties and risk for type 2 diabetes and myocardial infarction. Diabetes 2001; 50: 637–42.Google Scholar
11Juul, A. Serum levels of insulin-like growth factor-I and its binding proteins in health and disease. Growth Hormone and IGF Research 2003; 13: 113–70.CrossRefGoogle ScholarPubMed
12Sandhu, MS, Heald, AH, Gibson, JM, Cruickshank, JK, Dunger, DB, Wareham, NJ. Circulating concentrations of insulin-like growth factor-I and the development of glucose intolerance: a prospective observational study. Lancet 2002; 359: 1740–5.CrossRefGoogle ScholarPubMed
13Cruickshank, JK, Heald, AH, Anderson, SG, Cade, JE, Sampayo, J, Riste, LK, et al. The epidemiology of the insulin-like growth factor system in 3 ethnic groups. American Journal of Epidemiology 2001; 154: 504–13.CrossRefGoogle Scholar
14Juul, A, Scheike, T, Davidsen, M, Gyllenborg, J, Jørgensen, T. Low serum insulin-like growth factor-I is associated with increased risk of ischaemic heart disease: a population-based case–control study. Circulation 2002; 106: 939–44.Google Scholar
15Laughlin, GA, Barrett-Connor, E, Criqui, MH, Kirtz-Silverstein, D. The prospective association of insulin like growth factor-I and IGF-binding protein-1 levels with all cause and cardiovascular disease mortality in older adults: The Rancho-Bernardo study. Journal of Clinical Endocrinology and Metabolism 2004; 89: 114–20.CrossRefGoogle ScholarPubMed
16Heald, AH, Cade, JE, Cruickshank, JK, Anderson, S, White, A, Gibson, JM. The influence of dietary intake on the insulin-like growth factor (IGF) system across three ethnic groups: a population-based study. Public Health Nutrition 2003; 6: 175–80.Google Scholar
17Harding, S. Mortality of migrants from the Indian subcontinent to England and Wales: effect of duration of residence. Epidemiology 2003; 14: 287–9.CrossRefGoogle ScholarPubMed
18Richardson, MT, Leon, AS, Jacobs, DR Jr, Ainsworth, BE, Serfass, R. Ability of the Caltrac accelerometer to assess daily physical activity levels. Journal of Cardiopulmonary Rehabilitation 1995; 15: 107–13.CrossRefGoogle ScholarPubMed
19Westwood, M, Gibson, JM, Davies, AJ, Young, RJ, White, A. The phosphorylation pattern of insulin-like growth factor binding protein-1 in normal plasma is different from that in amniotic fluid and changes during pregnancy. Journal of Clinical Endocrinology and Metabolism 1994; 79: 1735–41.Google ScholarPubMed
20Yates, AP, Laing, I. Age-related increase in haemoglobin A1c and fasting plasma glucose is accompanied by a decrease in beta cell function without change in insulin sensitivity: evidence from a cross-sectional study of hospital personnel. Diabetic Medicine 2002; 19: 254–8.Google Scholar
21Matthews, DR, Hosker, JP, Rudenski, AS, Naylor, BA, Treacher, DF, Turner, RC. Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 1985; 28: 412–9.CrossRefGoogle ScholarPubMed
22Ferrannini, E, Mari, A. How to measure insulin sensitivity. Journal of Hypertension 1998; 16: 895–906.CrossRefGoogle ScholarPubMed
23Underwood, LE, Clemmons, DR, Maes, M, D'Ercole, AJ, Ketelslegers, JM. Regulation of somatomedin-C/insulin-like growth factor I by nutrients. Hormone Research 1986; 24: 166–76.CrossRefGoogle ScholarPubMed
24Clemmons, DR, Klibanski, A, Underwood, LE, McArthur, JW, Ridgway, EC, Beitins, IZ, et al. Reduction of plasma immunoreactive somatomedin-C during fasting in humans. Journal of Clinical Endocrinology and Metabolism 1981; 53: 1247–50.Google Scholar
25Kirschner, BS, Sutton, MM. Somatomedin-C levels in growth impaired children and adolescents with chronic inflammatory bowel disease. Gastroenterology 1986; 91: 830–6.CrossRefGoogle ScholarPubMed
26Kaklamani, VG, Linos, A, Kaklamani, E, Markaki, I, Koumantaki, Y, Mantzoros, CS. Dietary fat and carbohydrates are independently associated with circulating insulin-like growth factor 1 and insulin-like growth factor-binding protein 3 concentrations in healthy adults. Journal of Clinical Oncology 1999; 17: 3291–8.CrossRefGoogle ScholarPubMed
27Ferraris, RP, Cao, QX, Prabhakaram, S. Chronic but not acute energy restriction increases intestinal nutrient transport in mice. Journal of Nutrition 2001; 31: 779–86.Google Scholar
28Morgan, EH, Oates, PS. Mechanisms and regulation of intestinal iron absorption. Blood Cells, Molecules & Disease 2002; 29: 384–99.Google Scholar
29Gal-Garber, O, Mabjeesh, SJ, Sklan, D, Uni, Z. Partial sequence and expression of the gene for and activity of the sodium transporter in the small intestine of fed, starved and re-fed chickens. Journal of Nutrition 2000; 130: 2174–9.CrossRefGoogle Scholar
30O'Brien, DP, Nelson, LA, Huang, FS, Warner, BW. Intestinal adaptation: structure, function and regulation. Seminars in Paediatric Surgery 2001; 10: 56–64.Google Scholar
31Lee, PD, Giudice, LC, Conover, CA, Powell, DR. Insulin-like growth factor binding protein-1: recent findings and new directions. Proceedings of the Society for Experimental Biology and Medicine 1997; 216: 319–57.CrossRefGoogle ScholarPubMed
32Cruickshank, JK, Cooper, J, Burnett, M, Macduff, J, Drubra, U. Ethnic differences in fasting plasma C-peptide and insulin in relation to glucose tolerance and blood pressure. Lancet 1991; 338: 842–7.CrossRefGoogle ScholarPubMed
33McKeigue, PM, Shah, B, Marmot, MG. Relation of central obesity and insulin resistance with high diabetes prevalence and cardiovascular risk in South Asians. Lancet 1991; 337: 382–6.Google Scholar
34Bang, P, Brandt, J, Degerblad, M, Enberg, G, Kaijser, L, Thoren, M, et al. Exercise induced changes in insulin-like growth factors and their low molecular weight binding protein in healthy subjects and patients with growth hormone deficiency. European Journal of Clinical Investigation 1990; 20: 285–92.CrossRefGoogle ScholarPubMed
35Allen, NE, Appleby, PN, Kass, R, Rinaldi, S, Davey, GK, Key, TJ. Life style determinants of serum insulin-like growth factor-I, C-peptide and hormone binding protein levels in British women. Cancer Causes & Control 2003; 14: 65–74.CrossRefGoogle ScholarPubMed
36Hopkins, NJ, Jakeman, PM, Hughes, SC, Holly, JM. Changes in circulating insulin-like growth factor-binding protein-1 during prolonged exercise: effect of carbohydrate feeding. Journal of Clinical Endocrinology and Metabolism 1994; 79: 1887–90.Google ScholarPubMed
37Cohen, LA, Choi, KW, Wang, CX. Influence of dietary fat, calorie restriction and voluntary exercise on N -nitrosomethylurea-induced tumorigenesis in rats. Cancer Research 1988; 48: 4276–83.Google Scholar
38Hursting, SD, Perkins, SN, Phang, JM. Calorie restriction delays spontaneous tumorigenesis in p53-knockout transgenic mice. Proceedings of the National Academy of Sciences of the USA 1994; 91: 7036–40.CrossRefGoogle ScholarPubMed
39Mukherjee, P, Sotnikov, AV, Mangian, HJ, Zhou, JR, Visek, WJ, Clinton, SK. Energy intake and prostate tumor growth, angiogenesis and vascular endothelial growth factor expression. Journal of the National Cancer Institute 1999; 91: 512–23.CrossRefGoogle ScholarPubMed
40Dunn, SE, Kari, FW, French, J, Leininger, JR, Travlos, J, Wilson, R, et al. Dietary restriction reduces insulin-like growth factor-I levels, which modulates apoptosis, cell proliferation, and tumor progression in p53-deficient mice. Cancer Research 1997; 57: 4667–72.Google Scholar