Divergent Effects of Short-Term, Very-Low-Calorie Diet on Insulin-Like Growth Factor-I and Insulin-Like Growth Factor Binding Protein-3 Serum Concentrations in Premenopausal Women with Obesity
Corresponding Author
Dr. Giovanni de Pergola
Istituto di Clinica Medica, Endocrinologia e Malattie Metaboliche, University of Bari, 70124 Bari, Italy
Istituto di Clinica Medica, Endocrinologia e Malattie Metaboliche, Piazza Giulio Cesare, 70124 Bari, Italy.Search for more papers by this authorMauro Zamboni
Servizio Clinicizzato di Geriatria de H'Universitá di Verona, Istituto di Clinica Medica, 37126 Verona, Italy.
Search for more papers by this authorNicola Pannacciulli
Istituto di Clinica Medica, Endocrinologia e Malattie Metaboliche, University of Bari, 70124 Bari, Italy
Search for more papers by this authorEmanuela Turcato
Servizio Clinicizzato di Geriatria de H'Universitá di Verona, Istituto di Clinica Medica, 37126 Verona, Italy.
Search for more papers by this authorFrancesco Giorgino
Istituto di Clinica Medica, Endocrinologia e Malattie Metaboliche, University of Bari, 70124 Bari, Italy
Search for more papers by this authorFabio Armellini
Servizio Clinicizzato di Geriatria de H'Universitá di Verona, Istituto di Clinica Medica, 37126 Verona, Italy.
Search for more papers by this authorFrancesco Logoluso
Istituto di Clinica Medica, Endocrinologia e Malattie Metaboliche, University of Bari, 70124 Bari, Italy
Search for more papers by this authorMarcello Sciaraffia
Istituto di Clinica Medica, Endocrinologia e Malattie Metaboliche, University of Bari, 70124 Bari, Italy
Search for more papers by this authorOttavio Bosello
Servizio Clinicizzato di Geriatria de H'Universitá di Verona, Istituto di Clinica Medica, 37126 Verona, Italy.
Search for more papers by this authorRiccardo Giorgino
Istituto di Clinica Medica, Endocrinologia e Malattie Metaboliche, University of Bari, 70124 Bari, Italy
Search for more papers by this authorCorresponding Author
Dr. Giovanni de Pergola
Istituto di Clinica Medica, Endocrinologia e Malattie Metaboliche, University of Bari, 70124 Bari, Italy
Istituto di Clinica Medica, Endocrinologia e Malattie Metaboliche, Piazza Giulio Cesare, 70124 Bari, Italy.Search for more papers by this authorMauro Zamboni
Servizio Clinicizzato di Geriatria de H'Universitá di Verona, Istituto di Clinica Medica, 37126 Verona, Italy.
Search for more papers by this authorNicola Pannacciulli
Istituto di Clinica Medica, Endocrinologia e Malattie Metaboliche, University of Bari, 70124 Bari, Italy
Search for more papers by this authorEmanuela Turcato
Servizio Clinicizzato di Geriatria de H'Universitá di Verona, Istituto di Clinica Medica, 37126 Verona, Italy.
Search for more papers by this authorFrancesco Giorgino
Istituto di Clinica Medica, Endocrinologia e Malattie Metaboliche, University of Bari, 70124 Bari, Italy
Search for more papers by this authorFabio Armellini
Servizio Clinicizzato di Geriatria de H'Universitá di Verona, Istituto di Clinica Medica, 37126 Verona, Italy.
Search for more papers by this authorFrancesco Logoluso
Istituto di Clinica Medica, Endocrinologia e Malattie Metaboliche, University of Bari, 70124 Bari, Italy
Search for more papers by this authorMarcello Sciaraffia
Istituto di Clinica Medica, Endocrinologia e Malattie Metaboliche, University of Bari, 70124 Bari, Italy
Search for more papers by this authorOttavio Bosello
Servizio Clinicizzato di Geriatria de H'Universitá di Verona, Istituto di Clinica Medica, 37126 Verona, Italy.
Search for more papers by this authorRiccardo Giorgino
Istituto di Clinica Medica, Endocrinologia e Malattie Metaboliche, University of Bari, 70124 Bari, Italy
Search for more papers by this authorAbstract
DE PERGOLA, GIOVANNI, MAURO ZAMBONI, NICOLA PANNACCIULLI, EMANUELA TURCATO, FRANCESCO GIORGINO, FABIO ARMELLINI, FRANCESCO LOGOLUSO, MARCELLO SCIARAFFIA, OTTAVIO BOSELLO, RICCARDO GIORGINO. Divergent effects of short-term, very-low-calorie diet on insulinlike growth factor-I and insulin-like growth factor binding protein-3 serum concentrations in premenopausal women with obesity. Obes Res. 1998;6:408–415.
Objective: Insulin-like growth factor-I (IGF-I) and insulinlike growth factor binding protein-3 (IGFBP-3) serum concentrations provide a good measure of the biological effects of growth, hormone. The aims of the present study were to: (1) investigate the associations of IGF-I and IGFBP-3 with body fat mass and distribution, and (2) evaluate the effects of 3 weeks of very-low-calorie diet (VLCD) (318 kcal/day, with 40 g protein, 35 g carbohydrate, and 2 g fat) on IGF-I and IGFBP-3 serum concentrations.
Research Methods and Procedures: The study was performed in 21 nondiabetic premenopausal women with obesity (body mass index <27.0 kg/m2; age: ranging from 18 to 48 years). Body fat mass and distribution were measured by computed tomography.
Results: Before dietary treatment, IGF-I and IGFBP-3 serum concentrations were inversely associated with visceral adipose tissue (VAT) area (p<0.005 and p<0.05, respectively), but not with either total body fat or subcutaneous adipose tissue area. VLCD produced a significant decrease of body mass index (p<0.001), total body fat (p<0.001), VAT (p<0.005), subcutaneous adipose tissue (p<0.001), IGF-I concentrations (p<0.05), and an increase of IGFBP-3 serum levels (p<0.001). The association of VAT with either IGF-I or IGFBP-3 serum concentrations was not maintained following VLCD.
Discussion: Our study suggests that visceral adipose tissue, rather than adiposity per se, accounts for IGF-I and IGFBP-3 serum concentrations, and that rapid weight loss, possibly due to nutritional changes, results in lower IGF-I concentrations, higher IGFBP-3 concentrations, and abrogation of the inverse associations of VAT with IGF-I and IGFBP-3.
References
- 1 Williams T, Berelowitz M, Joffe SN, et al. Impairedgrowth hormone responses to growth hormone-releasing factor in obesity. N Engl J Med. 1984; 311: 1403–7.
- 2 Guier HP, Schmid C., Zapf J., Froesch ER. Effects of recombinant insulin-like growth factor-Ion insulin secretion and renal function in normal human subjects. Proc Natl Acad Sci USA. 1989; 86: 2868–72.
- 3 Juul A., Main K., Blum WF, Lindholm J., Ranke MB, Skakkebaek NE. The ratio between serum levels of insulin-like growthfactor (IGF-I) and the IGF binding proteins (IGFBP-1, 2 and 3) decreases with age in healthy adults and is increased in acromegalic patients. Clin Endocrinol. 1994; 41: 85–93.
- 4 Rosenbaum M., Gertner JM, Gidfar N., Hirsch J., Leibel RL. Effects of systemicgrowth hormone(GH) administration on regional adipose tissue in children with non-GH-deficient short stature. J Clin Endocrinol Metab. 1992; 75: 151–6.
- 5 Veldhuis JD, Iranmanesh A., Ho KKY, Waters MJ, Johnson ML, Lizarralde G. Dual effects in pulsatile growth hormone secretion and clearance subserve the hyposornatotropism of obesity in man. J Clin Endocrinol Metab. 1991; 72: 51–9.
- 6 Cordido F., Dieguez C., Casanueva FF. Effect of central cholinergic neurotransmission enhancement by pyridostigmine on the growth hormone secretion elicited by clonidine, arginine, or hypoglycemia in normal and obese subjects. J Clin Endocrinol Metab. 1990; 70: 1361–70.
- 7 Cordido F., Penalva A., Dieguez C., Casanueva FF. Massive growth hormone (GH) discharge in obese subjects after the combined administration of GH-releasing hormone and GHRP-6: evidence for a marked somatotroph secretory capability in obesity. J Clin Endocrinol Metab. 1993; 76: 819–23.
- 8 Bengtsson BA, Eden S., Lonn L., et al. Treatment of adults with growth hormone (GH) deficiency with recombinant human GH. J Clin Endocrinol Metab. 1993; 76: 309–17.
- 9 Jorgensen JOL, Vahl N., Hansen TB, Thuesen L., Hagen C., Christiansen JS. Growth hormone versus placebo treatment for one year in growth hormone deficient adults: increase in exercise capacity and normalization of body composition. Clin Endocrinol. 1996; 45: 681–8.
- 10 Marin P., Kvist H., Lindstedt G., Sjöström L., Bjorntorp P. Low concentrations of insulin-like growth factor-I in abdominal obesity. Int J Obes Relat Metab Disord. 1993; 17: 83–9.
- 11 Rasmussen HR, Frystyk J., Andersen T., Breum L., Christiansen JS, Hilsted J. The impact of obesity, body fat distribution and energy restriction on insulin-like growth factor-I (IGF-I), IGF-binding protein-3, insulin and growth hormone. Metabolism. 1994; 43: 315–9.
- 12 Blum WF, Albertsson-Wikland K., Rosberg S., Ranke MB. Serum levels of insulin-like growth factor-I (IGF-I) and IGF binding protein 3 (IGFBP-3) reflect spontaneous growth hormone secretion. J Clin Endocrinol Metab. 1993; 76: 1610–16.
- 13 Cohick WS, Clemmons DR. The insulin-like growth factors. Annu Rev Physiol. 1993; 55: 131–53.
- 14 LeRoith D., Clemmons D., Nissley P., Rechler MM. Insulinlike growth factors in health and disease. Ann Intern Med. 1992; 116: 854–62.
- 15 Russel-Jones DL, Umpleby M. Protein anabolic action of insulin, growth hormone and insulin-like growth factor-I. Eur J Endocrinol. 1996; 135: 631–42.
- 16 Pell JM, Bates PC. Differential actions of growth hormone and insulin-like growth factor-I on tissue protein metabolism in dwarf mice. Endocrinology. 1992; 130: 1942–50.
- 17 Turkalj I., Keller U., Ninnis R., Vosmeer S., Stauffacher W. Effect of increasing doses of recombinant human insulin-like growth factor-I on glucose, lipid, and leucine metabolism in man. J Clin Endocrinol Metab. 1992; 75: 1186–91.
- 18 Drop SLS. Report on the nomenclature of the IGF binding proteins. J Clin Endocrinol Metab. 1992; 72: 1215–6.
- 19 Soliman AT, Hassan AE, Aref MK, Hintz RL, Rosenfeld RG, Rogol AD. Serum insulin-like growth factor I and II concentrations and growth hormone and insulin responses to arginine infusion in children with protein-energy malnutrition before and after nutritional rehabilitation. Pediatr Res. 1986; 20: 1122–30.
- 20 Straus DS, Takemoto CD. Effect of dietary protein deprivation on insulin-like growth factor (IGF)-I and -II, IGF binding protein-2 and serum albumin gene expression in rat. Endocrinology. 1990; 127: 1849–60.
- 21 De Pergola G., Cospite MR, Giagulli VA, et al. Insulin-like growth factor-1 (IGF-I) and dehydroepiandrosterone sulphate in obese women. Int J Obes. 1993; 17: 481–3.
- 22 Baxter RC. Insulin-like growth factor (IGF) binding proteins: the role of serum IGFBP's in regulating IGF availability. Acta Pediatr Scand. 1991; 372 (Suppl.): 107–14.
- 23 Sara VR, Hall K. Insulin-like growth factors and their binding proteins. Physiol Rev. 1990; 70: 591–614.
- 24 Thissen JP, Ketelslegers JM, Underwood LE. Nutritional regulation of the insulin-like growth factors. Endocr Rev. 1994; 15: 80–101.
- 25 Gama R., Teale JD, Marks V. The effect of synthetic very-low-calorie diets on the GH-IGF-1 axis in obese subjects. Clin Chim Acta. 1990; 188: 31–8.
- 26 Committee on Medical Aspects of Food Policy: Report of the Working Group on Very Low Calorie Diets. The use of very-low-calorie diets in obesity. Rep Health Soc Subj (Lond.) 1987; 31: 1–43.
- 27 Kvist H., Tylen U., Sjöström L. Adipose tissue volume determinations in women by computed tomography: technical considerations. Int J Obes Relat Metab Disord. 1986; 10: 53–67.
- 28 Kvist H., Chowdhury B., Grangard U., Tylen U., Sjöström L. Total and visceral adipose tissue volumes derived from measurements with computed tomography in adult men and women: predictive equations. Am J Clin Nutr. 1988; 48: 1351–61.
- 29 Sjöström L., Kvist H., Tylen U. Methodological aspects of measurements of adipose tissue distribution. In: J. Vague, P. Bjorntorp, B. Guy-Grand, M. Rebuffé-Scrive, P. Vague, eds. Metabolic Complication of Human Obesities. Amsterdam: Excerpta Medica; 1985; 13–9.
- 30 Sjöström L., Kvist H., Cederblad A., Tylen U. Determination of total adipose tissue and body fat in women by computed tomography, 40K and tritium. Am J Physiol. 1986; 250: E736–45.
- 31 Sjöström L. Methods for measurements of total and visceral adipose tissue volume and relationships between visceral fat and disease in 1006 severely obese subjects. In: Y. Omura, S. Tarui, S. Inoue, T. Shimazu, eds. Progress in Obesity Research 1990. London: J. Libbey; 1991; 323–34.
- 32 Zamboni M., Armellini F., Turcato E., et al. Effect of weight loss on regional body fat distribution in premenopausal women. Am J Clin Nutr. 1993; 58: 29–34.
- 33 De Pergola G., Zamboni M., Sciaraffia M., et al. Body fat accumulation is possibly responsible for lower dehydroepiandrosterone circulating levels in premenopausal obese women. Int J Obes Relat Metab Disord. 1996; 20: 1105–10.
- 34 Report of the Expert Committee on the Diagnosis and Classification of Diabetes Mellitus. Diabetes Care. 1997; 20: 1183–97.
- 35 Zapf J., Hauri C., Waldvogel M., et al. Recombinant human insulin-like growth factor I induces its own specific carrier protein in hypophysectomized and diabetic rats. Proc Natl Acad Sci USA. 1989; 86: 3813–7.
- 36 Thorén M., Hilding A., Baxter RC, Degerblad M., Wivall-Helleryd IL, Hall K. Serum insulin-like growth factor I (IGF-I), IGF-binding protein-1 and −3, and the acid-labile subunit as serum markers of body composition during growth hormone (GH) therapy in adults with GH deficiency. J Clin Endocrinol Metab. 1997; 82: 223–8.
- 37 Elmer CA, Schalch DS. Nutritional-induced changes in hepatic insulin-like growth factor I gene expression in rats. Endocrinology. 1987; 120: 832–4.
- 38 Boney CM, Moats-Staats BM, Stiles AD, D'Ercole AJ. Expression of insulin-like growth factor-I (IGF-I) and IGF-binding proteins during adipogenesis. Endocrinology. 1994; 135: 1863–8.
- 39 Smith SR. The endocrinology of obesity. Endocrinol Metab Clin North Am. 1996; 25: 921–42.
- 40 Vikman K., Isgaard J., Edén S. Growth hormone regulation of insulin-like growth factor-I mRNA in rat adipose tissue and isolated adipocytes. J Endocrinol. 1991; 131: 139–45.
- 41 Rasmussen MH, Hvidberg A., Juul A., et al. Massive weight loss restores 24-hour growth hormone release profiles and serum insulin-like growth factor-1 levels in obese subjects. J Clin Endocrinol Metab. 1995; 80: 1407–15.
- 42 Smith WJ, Underwood LE, Clemmons DR. Effects of caloric restriction on insulin-like growth factor-I (IGF-I) and IGF binding proteins in children and adults. J Clin Endocrinol Metab. 1995; 80: 443–9.
- 43 Sommer A., Maack CA, Spratt SK. Molecular genetics and actions of recombinant insulin-like growth factor binding protein-3. In: EM Spencer, ed. Modern Concepts of Insulin-Like Growth Factors. New York: Elsevier; 1991.
- 44 Schwarz AJ, Brasel JA, Hintz RL, Mohan S., Cooper DM. Acute effect of brief low- and high-intensity exercise on circulating insulin-like growth factor (IGF) I, II, and IGF-binding protein-3 and its proteolysis in young healthy men. J Clin Endocrinol Metab. 1996; 81: 3492–7.
