Skip to main content
Top
Published in: BMC Pediatrics 1/2018

Open Access 01-12-2018 | Research article

Exercise reduces body fat and improves insulin sensitivity and pancreatic β-cell function in overweight and obese male Taiwanese adolescents

Authors: Kuang-Chung Shih, Ching-Fai Kwok

Published in: BMC Pediatrics | Issue 1/2018

Login to get access

Abstract

Background

Improvements in insulin resistance and pancreatic β-cell function have been shown following exercise in adults with obesity; however, few adolescent-based studies have been conducted. This study examined the impact of exercise training on body fat and insulin sensitivity and secretion in overweight and obese adolescents.

Methods

The effects of a 12-week exercise program on the parameters of adiposity and glucose homeostasis were investigated in 47 overweight and obese male adolescents.

Results

After the exercise training program, body weight, body mass index, waist circumference, and body fat were significantly decreased (P < 0.001). Improvements in insulin sensitivity (HOMA-IR: 1.40 vs. 0.86, P < 0.001) and the disposition index (5.84 vs. 12.77, P < 0.001) were also observed. Compared to baseline, oral glucose tolerance tests showed reduced glucose and insulin levels at all time points following the exercise training (all P < 0.001). Subgroup analysis of overweight and obese adolescents with abnormal glucose tolerance revealed that there was no difference in plasma glucose levels as compared to the lean group.

Conclusions

A 12-week exercise training is effective in reducing body fat and improving insulin sensitivity and secretion. In addition, the benefits of the exercise intervention were even experienced by those with impaired glucose tolerance.
Literature
1.
go back to reference Li S, Chen W, Srinivasan SR, Xu J, Berenson GS. Relation of childhood obesity/cardiometabolic phenotypes to adult cardiometabolic profile: the Bogalusa Heart Study. Am J Epidemiol. 2012;176:S142–9.CrossRefPubMedPubMedCentral Li S, Chen W, Srinivasan SR, Xu J, Berenson GS. Relation of childhood obesity/cardiometabolic phenotypes to adult cardiometabolic profile: the Bogalusa Heart Study. Am J Epidemiol. 2012;176:S142–9.CrossRefPubMedPubMedCentral
2.
go back to reference Ogden CL, Carroll MD, Kit BK, Flegal KM. Prevalence of childhood and adult obesity in the United States, 2011–2012. J Am Med Assoc. 2014;311(8):806–14.CrossRef Ogden CL, Carroll MD, Kit BK, Flegal KM. Prevalence of childhood and adult obesity in the United States, 2011–2012. J Am Med Assoc. 2014;311(8):806–14.CrossRef
3.
go back to reference Casavalle PL, Lifshitz F, Romano LS, Pandolfo M, Caamaño A, Boyer PM, et al. Prevalence of dyslipidemia and metabolic syndrome risk factor in overweight and obese children. Pediatr Endocrinol Rev. 2014;12(2):213–23.PubMed Casavalle PL, Lifshitz F, Romano LS, Pandolfo M, Caamaño A, Boyer PM, et al. Prevalence of dyslipidemia and metabolic syndrome risk factor in overweight and obese children. Pediatr Endocrinol Rev. 2014;12(2):213–23.PubMed
4.
go back to reference Weyer C, Bogardus C, Mott DM, Pratley RE. The natural history of insulin secretory dysfunction and insulin resistance in the pathogenesis of type 2 diabetes mellitus. J Clin Investig. 1999;104(6):787–94.CrossRefPubMedPubMedCentral Weyer C, Bogardus C, Mott DM, Pratley RE. The natural history of insulin secretory dysfunction and insulin resistance in the pathogenesis of type 2 diabetes mellitus. J Clin Investig. 1999;104(6):787–94.CrossRefPubMedPubMedCentral
5.
go back to reference Festa A, Williams K, D’Agostino R Jr, Wagenknecht LE, Haffner SM. The natural course of beta-cell function in nondiabetic and diabetic individuals: the Insulin Resistance Atherosclerosis Study. Diabetes. 2006;55(4):1114–20.CrossRefPubMed Festa A, Williams K, D’Agostino R Jr, Wagenknecht LE, Haffner SM. The natural course of beta-cell function in nondiabetic and diabetic individuals: the Insulin Resistance Atherosclerosis Study. Diabetes. 2006;55(4):1114–20.CrossRefPubMed
6.
go back to reference Saad R, Gungor N, Arslanian S. Progression from normal glucose tolerance to type 2 diabetes in a young girl: longitudinal changes in insulin sensitivity and secretion assessed by the clamp technique and surrogate estimates. Pediatr Diabetes. 2005;6(2):95–9.CrossRefPubMed Saad R, Gungor N, Arslanian S. Progression from normal glucose tolerance to type 2 diabetes in a young girl: longitudinal changes in insulin sensitivity and secretion assessed by the clamp technique and surrogate estimates. Pediatr Diabetes. 2005;6(2):95–9.CrossRefPubMed
7.
go back to reference Kelly LA, Lane CJ, Weigensberg MJ, Koebnick C, Roberts CK, Davis JN, et al. Parental history and risk of type 2 diabetes in overweight Latino adolescents: a longitudinal analysis. Diabetes Care. 2007;30(10):2700–5.CrossRefPubMed Kelly LA, Lane CJ, Weigensberg MJ, Koebnick C, Roberts CK, Davis JN, et al. Parental history and risk of type 2 diabetes in overweight Latino adolescents: a longitudinal analysis. Diabetes Care. 2007;30(10):2700–5.CrossRefPubMed
8.
go back to reference Bruce CR, Kriketos AD, Cooney GJ, Hawley JA. Disassociation of muscle triglyceride content and insulin sensitiity after exercise training in patients with type 2 diabetes. Diabetologia. 2004;47(1):23–30.CrossRefPubMed Bruce CR, Kriketos AD, Cooney GJ, Hawley JA. Disassociation of muscle triglyceride content and insulin sensitiity after exercise training in patients with type 2 diabetes. Diabetologia. 2004;47(1):23–30.CrossRefPubMed
9.
go back to reference O’Leary VB, Marchetti CM, Krishnan RK, Stetzer BP, Gonzalez F, Kirwan JP. Exercise-induced reversal of insulin resistance in obese elderly is associated with reduced visceral fat. J Appl Physiol. 2006;100(5):1584–9.CrossRefPubMed O’Leary VB, Marchetti CM, Krishnan RK, Stetzer BP, Gonzalez F, Kirwan JP. Exercise-induced reversal of insulin resistance in obese elderly is associated with reduced visceral fat. J Appl Physiol. 2006;100(5):1584–9.CrossRefPubMed
10.
go back to reference Jeon CY, Lokken RP, Hu FB, van Dam RM. Physical activity of moderate intensity and risk of type 2 diabetes: a systematic review. Diabetes Care. 2007;30(3):744–52.CrossRefPubMed Jeon CY, Lokken RP, Hu FB, van Dam RM. Physical activity of moderate intensity and risk of type 2 diabetes: a systematic review. Diabetes Care. 2007;30(3):744–52.CrossRefPubMed
11.
go back to reference Utzschneider KM, Carr DB, Barsness SM, Kahn SE, Schwartz RS. Diet-induced weight loss is associated with an improvement in beta-cell function in older men. J Clin Endocrinol Metab. 2004;89(6):2704–10.CrossRefPubMed Utzschneider KM, Carr DB, Barsness SM, Kahn SE, Schwartz RS. Diet-induced weight loss is associated with an improvement in beta-cell function in older men. J Clin Endocrinol Metab. 2004;89(6):2704–10.CrossRefPubMed
12.
go back to reference Bloem CJ, Chang AM. Short-term exercise improves beta-cell function and insulin rssistance in older people with impaired glucose tolerance. J Clin Endocrinol Metab. 2008;93(2):387–92.CrossRefPubMed Bloem CJ, Chang AM. Short-term exercise improves beta-cell function and insulin rssistance in older people with impaired glucose tolerance. J Clin Endocrinol Metab. 2008;93(2):387–92.CrossRefPubMed
13.
go back to reference Slentz CA, Tanner CJ, Bateman LA, Durheim MT, Huffman KM, Houmard JA, et al. Effects of exercise training intensity on pancreatic beta-cell function. Diabetes Care. 2009;32(10):1807–11.CrossRefPubMedPubMedCentral Slentz CA, Tanner CJ, Bateman LA, Durheim MT, Huffman KM, Houmard JA, et al. Effects of exercise training intensity on pancreatic beta-cell function. Diabetes Care. 2009;32(10):1807–11.CrossRefPubMedPubMedCentral
14.
go back to reference García-Hermoso A, Saavedra JM, Escalante Y, Sánchez-López M, Martínez-Vizcaíno V. Endocrinology and Adolescence: aerobic exercise reduces insulin resistance markers in obese youth: a meta-analysis of randomized controlled trials. Eur J Endocrinol. 2014;171(4):R163–71.CrossRefPubMed García-Hermoso A, Saavedra JM, Escalante Y, Sánchez-López M, Martínez-Vizcaíno V. Endocrinology and Adolescence: aerobic exercise reduces insulin resistance markers in obese youth: a meta-analysis of randomized controlled trials. Eur J Endocrinol. 2014;171(4):R163–71.CrossRefPubMed
15.
go back to reference Huang CJ, Kwok CF, Chou CH, Chou YC, Ho LT, Shih KC. The effect of exercise on lipid profiles and inflammatory markers in lean male adolescents: a prospective interventional study. J Investig Med. 2015;63(1):29–34.CrossRefPubMed Huang CJ, Kwok CF, Chou CH, Chou YC, Ho LT, Shih KC. The effect of exercise on lipid profiles and inflammatory markers in lean male adolescents: a prospective interventional study. J Investig Med. 2015;63(1):29–34.CrossRefPubMed
16.
go back to reference Shih KC, Janckila AJ, Kwok CF, Ho LT, Chou YC, Chao TY. Effects of exercise on insulin sensitivity, inflammatory cytokines, and serum tartrate-resistant acid phosphatase 5a in obese Chinese male adolescents. Metabolism. 2010;59(1):144–51.CrossRefPubMed Shih KC, Janckila AJ, Kwok CF, Ho LT, Chou YC, Chao TY. Effects of exercise on insulin sensitivity, inflammatory cytokines, and serum tartrate-resistant acid phosphatase 5a in obese Chinese male adolescents. Metabolism. 2010;59(1):144–51.CrossRefPubMed
17.
go back to reference Lee S, Bacha F, Hannon T, Kuk JL, Boesch C, Arslanian S. Effects of aerobic versus resistance exercise without caloric restriction on abdominal fat, intrahepatic lipid, and insulin sensitivity in obese adolescent boys: a randomized, controlled trial. Diabetes. 2012;61(11):2787–95.CrossRefPubMedPubMedCentral Lee S, Bacha F, Hannon T, Kuk JL, Boesch C, Arslanian S. Effects of aerobic versus resistance exercise without caloric restriction on abdominal fat, intrahepatic lipid, and insulin sensitivity in obese adolescent boys: a randomized, controlled trial. Diabetes. 2012;61(11):2787–95.CrossRefPubMedPubMedCentral
18.
go back to reference Chen W, Lin CC, Peng CT, Li CI, Wu HC, Chiang J, et al. Approaching healthy body mass index norms for children and adolescents from health-related physical fitness. Obes Rev. 2002;3(3):225–32.CrossRefPubMed Chen W, Lin CC, Peng CT, Li CI, Wu HC, Chiang J, et al. Approaching healthy body mass index norms for children and adolescents from health-related physical fitness. Obes Rev. 2002;3(3):225–32.CrossRefPubMed
19.
go back to reference Marshall WA, Tanner JM. Growth and physiological development during adolescence. Ann Rev Med. 1968;19:283–300.CrossRefPubMed Marshall WA, Tanner JM. Growth and physiological development during adolescence. Ann Rev Med. 1968;19:283–300.CrossRefPubMed
21.
go back to reference Matthews 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(7):412–9.CrossRefPubMed Matthews 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(7):412–9.CrossRefPubMed
22.
go back to reference Gastaldelli A, Ferrannini E, Miyazaki Y, Matsuda M, DeFronzo RA, San Antonio metabolism study. Beta-cell dysfunction and glucose intolerance: results from the San Antonio metabolism (SAM) study. Diabetologia. 2004;47(1):31–9.CrossRefPubMed Gastaldelli A, Ferrannini E, Miyazaki Y, Matsuda M, DeFronzo RA, San Antonio metabolism study. Beta-cell dysfunction and glucose intolerance: results from the San Antonio metabolism (SAM) study. Diabetologia. 2004;47(1):31–9.CrossRefPubMed
23.
go back to reference DeFronzo RA, Banerji MA, Bray GA, Buchanan TA, Clement S, Henry RR, et al. Determinants of glucose tolerance in impaired glucose tolerance at baseline in the Actos Now for Prevention of Diabetes (ACT NOW) study. Diabetologia. 2010;53(3):435–45.CrossRefPubMed DeFronzo RA, Banerji MA, Bray GA, Buchanan TA, Clement S, Henry RR, et al. Determinants of glucose tolerance in impaired glucose tolerance at baseline in the Actos Now for Prevention of Diabetes (ACT NOW) study. Diabetologia. 2010;53(3):435–45.CrossRefPubMed
24.
go back to reference Jensen CC, Cnop M, Hull RL, Fujimoto WY, Kahn SE, American Diabetes Association GENNID Study Group. Beta-cell function is a major contributor to oral glucose tolerance in high-risk relatives of four ethnic groups in the U.S. Diabetes. 2002;51(7):2170–8.CrossRefPubMed Jensen CC, Cnop M, Hull RL, Fujimoto WY, Kahn SE, American Diabetes Association GENNID Study Group. Beta-cell function is a major contributor to oral glucose tolerance in high-risk relatives of four ethnic groups in the U.S. Diabetes. 2002;51(7):2170–8.CrossRefPubMed
25.
go back to reference Giannini C, Weiss R, Cali A, Bonadonna R, Santoro N, Pierpont B, et al. Evidence for early defects in insulin sensitivity and secretion before the onset of glucose dysregulation in obese youths: a longitudinal study. Diabetes. 2012;61(3):606–14.CrossRefPubMedPubMedCentral Giannini C, Weiss R, Cali A, Bonadonna R, Santoro N, Pierpont B, et al. Evidence for early defects in insulin sensitivity and secretion before the onset of glucose dysregulation in obese youths: a longitudinal study. Diabetes. 2012;61(3):606–14.CrossRefPubMedPubMedCentral
26.
go back to reference van der Heijden GJ, Toffolo G, Manesso E, Sauer PJ, Sunehag AL. Aerobic exercise increases peripheral and hepatic insulin sensitivity in sedentary adolescents. J Clin Endocrinol Metab. 2009;94(11):4292–9.CrossRefPubMedPubMedCentral van der Heijden GJ, Toffolo G, Manesso E, Sauer PJ, Sunehag AL. Aerobic exercise increases peripheral and hepatic insulin sensitivity in sedentary adolescents. J Clin Endocrinol Metab. 2009;94(11):4292–9.CrossRefPubMedPubMedCentral
27.
go back to reference van der Heijden GJ, Wang ZJ, Chu Z, Toffolo G, Manesso E, Sauer PJ, et al. Strength exercise improves muscle mass and hepatic insulin sensitivity in obese youth. Med Sci Sports Exerc. 2010;42(11):1973–80.CrossRefPubMedPubMedCentral van der Heijden GJ, Wang ZJ, Chu Z, Toffolo G, Manesso E, Sauer PJ, et al. Strength exercise improves muscle mass and hepatic insulin sensitivity in obese youth. Med Sci Sports Exerc. 2010;42(11):1973–80.CrossRefPubMedPubMedCentral
28.
go back to reference Nassis GP, Papantakou K, Skenderi K, Triandafillopoulou M, Kavouras SA, Yannakoulia M, et al. Aerobic exercise training improves insulin sensitivity without changes in body weight, body fat, adiponectin, and inflammatory markers in overweight and obese girls. Metabolism. 2005;54(11):1472–9.CrossRefPubMed Nassis GP, Papantakou K, Skenderi K, Triandafillopoulou M, Kavouras SA, Yannakoulia M, et al. Aerobic exercise training improves insulin sensitivity without changes in body weight, body fat, adiponectin, and inflammatory markers in overweight and obese girls. Metabolism. 2005;54(11):1472–9.CrossRefPubMed
29.
go back to reference Shaibi GQ, Cruz ML, Ball GD, Weigensberg MJ, Salem GJ, Crespo NC, et al. Effects of resistance training on insulin sensitivity in overweight Latino adolescent males. Med Sci Sports Exerc. 2006;38(7):1208–15.CrossRefPubMed Shaibi GQ, Cruz ML, Ball GD, Weigensberg MJ, Salem GJ, Crespo NC, et al. Effects of resistance training on insulin sensitivity in overweight Latino adolescent males. Med Sci Sports Exerc. 2006;38(7):1208–15.CrossRefPubMed
30.
go back to reference Abrams P, Levitt Katz LE, Moore RH, Xanthopoulos MS, Bishop-Gilyard CT, Wadden TA, et al. Threshold for improvement in insulin sensitivity with adolescent weight loss. J Pediatr. 2013;163(3):785–90.CrossRefPubMed Abrams P, Levitt Katz LE, Moore RH, Xanthopoulos MS, Bishop-Gilyard CT, Wadden TA, et al. Threshold for improvement in insulin sensitivity with adolescent weight loss. J Pediatr. 2013;163(3):785–90.CrossRefPubMed
31.
go back to reference Sigal RJ, Alberga AS, Goldfield GS, Prud’homme D, Hadjiyannakis S, Gougeon R, et al. Effects of aerobic training, resistance training, or both on percentage body fat and cardiometabolic risk markers in obese adolescents: the healthy eating aerobic and resistance training in youth randomized clinical trial. JAMA Pediatr. 2014;168(11):1006–14.CrossRefPubMed Sigal RJ, Alberga AS, Goldfield GS, Prud’homme D, Hadjiyannakis S, Gougeon R, et al. Effects of aerobic training, resistance training, or both on percentage body fat and cardiometabolic risk markers in obese adolescents: the healthy eating aerobic and resistance training in youth randomized clinical trial. JAMA Pediatr. 2014;168(11):1006–14.CrossRefPubMed
32.
go back to reference Reaven GM, Chen YD, Hollenbeck CB, Sheu WH, Ostrega D, Polonsky KS. Plasma insulin, C-peptide, and proinsulin concentrations in obese and nonobese individuals with varying degrees of glucose tolerance. J Clin Endocrinol Metab. 1993;76(1):44–8.PubMed Reaven GM, Chen YD, Hollenbeck CB, Sheu WH, Ostrega D, Polonsky KS. Plasma insulin, C-peptide, and proinsulin concentrations in obese and nonobese individuals with varying degrees of glucose tolerance. J Clin Endocrinol Metab. 1993;76(1):44–8.PubMed
33.
go back to reference Ferrannini E, Natali A, Bell P, Cavallo-Perin P, Lalic N, Mingrone G. Insulin resistance and hypersecretion in obesity. European Group for the Study of Insulin Resistance (EGIR). J Clin Investig. 1997;100(5):1166–73.CrossRefPubMedPubMedCentral Ferrannini E, Natali A, Bell P, Cavallo-Perin P, Lalic N, Mingrone G. Insulin resistance and hypersecretion in obesity. European Group for the Study of Insulin Resistance (EGIR). J Clin Investig. 1997;100(5):1166–73.CrossRefPubMedPubMedCentral
34.
go back to reference Muscelli E, Camastra S, Catalano C, Galvan AQ, Ciociaro D, Baldi S, et al. Metabolic and cardiovascular assessment in moderate obesity: effect of weight loss. J Clin Endocrinol Metab. 1997;82(9):2937–43.CrossRefPubMed Muscelli E, Camastra S, Catalano C, Galvan AQ, Ciociaro D, Baldi S, et al. Metabolic and cardiovascular assessment in moderate obesity: effect of weight loss. J Clin Endocrinol Metab. 1997;82(9):2937–43.CrossRefPubMed
35.
go back to reference Tuominen JA, Ebeling P, Koivisto VA. Exercise increases insulin clearance in healthy man and insulin-dependent diabetes mellitus patients. Clin Physiol. 1997;17(1):19–30.CrossRefPubMed Tuominen JA, Ebeling P, Koivisto VA. Exercise increases insulin clearance in healthy man and insulin-dependent diabetes mellitus patients. Clin Physiol. 1997;17(1):19–30.CrossRefPubMed
36.
go back to reference Donath MY, Ehses JA, Maedler K, Schumann DM, Ellingsgaard H, Eppler E, et al. Mechanisms of beta-cell death in type 2 diabetes. Diabetes. 2005;54:S108–13.CrossRefPubMed Donath MY, Ehses JA, Maedler K, Schumann DM, Ellingsgaard H, Eppler E, et al. Mechanisms of beta-cell death in type 2 diabetes. Diabetes. 2005;54:S108–13.CrossRefPubMed
37.
go back to reference Kelly LA, Lane CJ, Weigensberg MJ, Toledo-Corral CM, Goran MI. Pubertal changes of insulin sensitivity, acute insulin response, and β-cell function in overweight Latino youth. J Pediatr. 2011;158(3):442–6.CrossRefPubMedPubMedCentral Kelly LA, Lane CJ, Weigensberg MJ, Toledo-Corral CM, Goran MI. Pubertal changes of insulin sensitivity, acute insulin response, and β-cell function in overweight Latino youth. J Pediatr. 2011;158(3):442–6.CrossRefPubMedPubMedCentral
38.
go back to reference Matsuda M, DeFronzo RA. Insulin sensitivity indices obtained from oral glucose tolerance testing: comparison with the euglycemic insulin clamp. Diabetes Care. 1999;22(9):1462–70.CrossRefPubMed Matsuda M, DeFronzo RA. Insulin sensitivity indices obtained from oral glucose tolerance testing: comparison with the euglycemic insulin clamp. Diabetes Care. 1999;22(9):1462–70.CrossRefPubMed
39.
go back to reference Casazza K, Phadke RP, Fernandez JR, Watanabe RM, Goran MI, Gower BA. Obesity attenuates the contribution of African admixture to the insulin secretory profile in peripubertal children: a longitudinal analysis. Obesity. 2009;17(7):1318–25.PubMedPubMedCentral Casazza K, Phadke RP, Fernandez JR, Watanabe RM, Goran MI, Gower BA. Obesity attenuates the contribution of African admixture to the insulin secretory profile in peripubertal children: a longitudinal analysis. Obesity. 2009;17(7):1318–25.PubMedPubMedCentral
Metadata
Title
Exercise reduces body fat and improves insulin sensitivity and pancreatic β-cell function in overweight and obese male Taiwanese adolescents
Authors
Kuang-Chung Shih
Ching-Fai Kwok
Publication date
01-12-2018
Publisher
BioMed Central
Published in
BMC Pediatrics / Issue 1/2018
Electronic ISSN: 1471-2431
DOI
https://doi.org/10.1186/s12887-018-1025-y

Other articles of this Issue 1/2018

BMC Pediatrics 1/2018 Go to the issue