Skip to main content
NCBI home page
The Journal of Clinical Investigation logoLink to The Journal of Clinical Investigation
. 1991 Jul;88(1):168–173. doi: 10.1172/JCI115274

Insulin resistance associated with lower rates of weight gain in Pima Indians.

B A Swinburn 1, B L Nyomba 1, M F Saad 1, F Zurlo 1, I Raz 1, W C Knowler 1, S Lillioja 1, C Bogardus 1, E Ravussin 1
PMCID: PMC296017  PMID: 2056116

Abstract

Insulin resistance is commonly associated with obesity and noninsulin-dependent diabetes. Whereas it predicts the development of diabetes, its effect on body weight change is unknown. We measured glucose disposal rates at submaximally- and maximally-stimulating insulin concentrations in 192 nondiabetic Pima Indians and followed their weight change over 3.5 +/- 1.8 y (mean +/- SD). Results: (a) Insulin-resistant subjects gained less weight than insulin-sensitive subjects (3.1 vs. 7.6 kg, P less than 0.0001). (b) The percent weight change per year correlated with glucose disposal at submaximally-(r = 0.19, P less than 0.01) and maximally-stimulating (r = 0.34, P less than 0.0001) insulin concentrations independent of sex, age, initial weight, and 24-h energy expenditure; the correlations were stronger for glucose oxidation than for glucose storage. (c) Weight gain was associated with an increase in insulin resistance more than four times that predicted from the cross-sectional data. We conclude that insulin resistance is associated with a reduced risk of weight gain in nondiabetic Pima Indians.

Full text

PDF
168

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Abbott W. G., Howard B. V., Christin L., Freymond D., Lillioja S., Boyce V. L., Anderson T. E., Bogardus C., Ravussin E. Short-term energy balance: relationship with protein, carbohydrate, and fat balances. Am J Physiol. 1988 Sep;255(3 Pt 1):E332–E337. doi: 10.1152/ajpendo.1988.255.3.E332. [DOI] [PubMed] [Google Scholar]
  2. Arner P. Control of lipolysis and its relevance to development of obesity in man. Diabetes Metab Rev. 1988 Aug;4(5):507–515. [PubMed] [Google Scholar]
  3. Best J. D., Taborsky G. J., Jr, Halter J. B., Porte D., Jr Glucose disposal is not proportional to plasma glucose level in man. Diabetes. 1981 Oct;30(10):847–850. doi: 10.2337/diab.30.10.847. [DOI] [PubMed] [Google Scholar]
  4. Bogardus C., Lillioja S., Howard B. V., Reaven G., Mott D. Relationships between insulin secretion, insulin action, and fasting plasma glucose concentration in nondiabetic and noninsulin-dependent diabetic subjects. J Clin Invest. 1984 Oct;74(4):1238–1246. doi: 10.1172/JCI111533. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bogardus C., Lillioja S., Mott D., Reaven G. R., Kashiwagi A., Foley J. E. Relationship between obesity and maximal insulin-stimulated glucose uptake in vivo and in vitro in Pima Indians. J Clin Invest. 1984 Mar;73(3):800–805. doi: 10.1172/JCI111274. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. D'Alessio D. A., Kavle E. C., Mozzoli M. A., Smalley K. J., Polansky M., Kendrick Z. V., Owen L. R., Bushman M. C., Boden G., Owen O. E. Thermic effect of food in lean and obese men. J Clin Invest. 1988 Jun;81(6):1781–1789. doi: 10.1172/JCI113520. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. DeFronzo R. A., Tobin J. D., Andres R. Glucose clamp technique: a method for quantifying insulin secretion and resistance. Am J Physiol. 1979 Sep;237(3):E214–E223. doi: 10.1152/ajpendo.1979.237.3.E214. [DOI] [PubMed] [Google Scholar]
  8. Felber J. P., Ferrannini E., Golay A., Meyer H. U., Theibaud D., Curchod B., Maeder E., Jequier E., DeFronzo R. A. Role of lipid oxidation in pathogenesis of insulin resistance of obesity and type II diabetes. Diabetes. 1987 Nov;36(11):1341–1350. doi: 10.2337/diab.36.11.1341. [DOI] [PubMed] [Google Scholar]
  9. Felig P. Insulin is the mediator of feeding-related thermogenesis: insulin resistance and/or deficiency results in a thermogenic defect which contributes to the pathogenesis of obesity. Clin Physiol. 1984 Aug;4(4):267–273. doi: 10.1111/j.1475-097x.1984.tb00802.x. [DOI] [PubMed] [Google Scholar]
  10. Flatt J. P. Importance of nutrient balance in body weight regulation. Diabetes Metab Rev. 1988 Sep;4(6):571–581. doi: 10.1002/dmr.5610040603. [DOI] [PubMed] [Google Scholar]
  11. Flatt J. P., Ravussin E., Acheson K. J., Jéquier E. Effects of dietary fat on postprandial substrate oxidation and on carbohydrate and fat balances. J Clin Invest. 1985 Sep;76(3):1019–1024. doi: 10.1172/JCI112054. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Grossman S. P. The role of glucose, insulin and glucagon in the regulation of food intake and body weight. Neurosci Biobehav Rev. 1986 Fall;10(3):295–315. doi: 10.1016/0149-7634(86)90015-1. [DOI] [PubMed] [Google Scholar]
  13. Herbert V., Lau K. S., Gottlieb C. W., Bleicher S. J. Coated charcoal immunoassay of insulin. J Clin Endocrinol Metab. 1965 Oct;25(10):1375–1384. doi: 10.1210/jcem-25-10-1375. [DOI] [PubMed] [Google Scholar]
  14. Jeanrenaud B. Neuroendocrine and metabolic basis of type II diabetes as studied in animal models. Diabetes Metab Rev. 1988 Sep;4(6):603–614. doi: 10.1002/dmr.5610040606. [DOI] [PubMed] [Google Scholar]
  15. KEYS A., BROZEK J. Body fat in adult man. Physiol Rev. 1953 Jul;33(3):245–325. doi: 10.1152/physrev.1953.33.3.245. [DOI] [PubMed] [Google Scholar]
  16. Knowler W. C., Pettitt D. J., Savage P. J., Bennett P. H. Diabetes incidence in Pima indians: contributions of obesity and parental diabetes. Am J Epidemiol. 1981 Feb;113(2):144–156. doi: 10.1093/oxfordjournals.aje.a113079. [DOI] [PubMed] [Google Scholar]
  17. Kolterman O. G., Gray R. S., Griffin J., Burstein P., Insel J., Scarlett J. A., Olefsky J. M. Receptor and postreceptor defects contribute to the insulin resistance in noninsulin-dependent diabetes mellitus. J Clin Invest. 1981 Oct;68(4):957–969. doi: 10.1172/JCI110350. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Nagulesparan M., Savage P. J., Knowler W. C., Johnson G. C., Bennett P. H. Increased in vivo insulin resistance in nondiabetic Pima Indians compared with Caucasians. Diabetes. 1982 Nov;31(11):952–956. doi: 10.2337/diacare.31.11.952. [DOI] [PubMed] [Google Scholar]
  19. OLDHAM P. D. A note on the analysis of repeated measurements of the same subjects. J Chronic Dis. 1962 Oct;15:969–977. doi: 10.1016/0021-9681(62)90116-9. [DOI] [PubMed] [Google Scholar]
  20. RANDLE P. J., GARLAND P. B., HALES C. N., NEWSHOLME E. A. The glucose fatty-acid cycle. Its role in insulin sensitivity and the metabolic disturbances of diabetes mellitus. Lancet. 1963 Apr 13;1(7285):785–789. doi: 10.1016/s0140-6736(63)91500-9. [DOI] [PubMed] [Google Scholar]
  21. Ravussin E., Lillioja S., Anderson T. E., Christin L., Bogardus C. Determinants of 24-hour energy expenditure in man. Methods and results using a respiratory chamber. J Clin Invest. 1986 Dec;78(6):1568–1578. doi: 10.1172/JCI112749. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Ravussin E., Lillioja S., Knowler W. C., Christin L., Freymond D., Abbott W. G., Boyce V., Howard B. V., Bogardus C. Reduced rate of energy expenditure as a risk factor for body-weight gain. N Engl J Med. 1988 Feb 25;318(8):467–472. doi: 10.1056/NEJM198802253180802. [DOI] [PubMed] [Google Scholar]
  23. Rodin J. Insulin levels, hunger, and food intake: an example of feedback loops in body weight regulation. Health Psychol. 1985;4(1):1–24. doi: 10.1037//0278-6133.4.1.1. [DOI] [PubMed] [Google Scholar]
  24. STEELE R. Influences of glucose loading and of injected insulin on hepatic glucose output. Ann N Y Acad Sci. 1959 Sep 25;82:420–430. doi: 10.1111/j.1749-6632.1959.tb44923.x. [DOI] [PubMed] [Google Scholar]
  25. Woods S. C., Porte D., Jr, Bobbioni E., Ionescu E., Sauter J. F., Rohner-Jeanrenaud F., Jeanrenaud B. Insulin: its relationship to the central nervous system and to the control of food intake and body weight. Am J Clin Nutr. 1985 Nov;42(5 Suppl):1063–1071. doi: 10.1093/ajcn/42.5.1063. [DOI] [PubMed] [Google Scholar]
  26. YALOW R. S., BERSON S. A. Immunoassay of endogenous plasma insulin in man. J Clin Invest. 1960 Jul;39:1157–1175. doi: 10.1172/JCI104130. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Yki-Järvinen H., Consoli A., Nurjhan N., Young A. A., Gerich J. E. Mechanism for underestimation of isotopically determined glucose disposal. Diabetes. 1989 Jun;38(6):744–751. doi: 10.2337/diab.38.6.744. [DOI] [PubMed] [Google Scholar]
  28. Zurlo F., Lillioja S., Esposito-Del Puente A., Nyomba B. L., Raz I., Saad M. F., Swinburn B. A., Knowler W. C., Bogardus C., Ravussin E. Low ratio of fat to carbohydrate oxidation as predictor of weight gain: study of 24-h RQ. Am J Physiol. 1990 Nov;259(5 Pt 1):E650–E657. doi: 10.1152/ajpendo.1990.259.5.E650. [DOI] [PubMed] [Google Scholar]

Articles from Journal of Clinical Investigation are provided here courtesy of American Society for Clinical Investigation

RESOURCES