Document Type : Research Paper
Authors
1 Ph.D. Student in Exercise Biochemistry and Metabolism, University of Mazandaran
2 Associate Professor of Exercise Physiology, University of Mazandaran
3 Assistant Professor, Cellular and Molecular Biology Research Center, Health Research Institute, Babol University of Medical Sciences
Abstract
By considering the growing trend of obesity, along with metabolic disorders among children, especially insulin-resistance (IR), the present study aimed to evaluate the effect of aerobic-training on the levels of spexin, lipid-accumulation product (LAP), visceral-adiposity (VAI), triglyceride-glucose (TyG) and McAuley indices among early-pubertal obese/overweight-girls. 32 obese/overweight-girls (age 9.62±0.75 years-old, weight 49.71±9.26 kg, BMI 25.40±2.92 kg/m2, Tanner-stage 2-3) voluntarily participated in this study, who were assigned into interval-walking (n=12), continuous-walking (n=11) and control (n=9) groups. The subjects were trained three-times/week for two-months (30-min walk in the continuous and interval-groups with 60-75%HRmax and 70-85%HRmax, respectively). Spexin concentration was measured by ELISA method, and visceral-adiposity and IR indices were calculated according to the equations. Factorial repeated-measured ANOVA was used for data analysis. Based on the results, the interaction-effect of time×group was statistically significant for the LAP (P=0.007), VAI (P=0.045), McAuley (P=0.026) and TyG (P=0.001), while it was insignificant for the spexin (P=0.836). Regarding the control group, the LAP, VAI, and TyG significantly increased (P=0.037, P=0.046, P=0.005, respectively) while a significant decrease happened for McAuley (P=0.030). In the continuous-walking group, a significant decrease was observed in LAP (P=0.002), and TyG (P=0.002), while VAI and McAuley levels tended to decrease (P=0.057) and increase (P=0.071), respectively. In the interval-walking group, there was insignificant change in the LAP, VAI, TyG, and McAuley (P=0.129, P=0.660, P=0.390, P=0.357, respectively). The findings showed that the continuous-walking for eight-weeks could reverse the increase in visceral-adiposity and IR indices in the control group, irrespective of the changes in serum levels of spexin.
Keywords
Main Subjects
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3. 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.
4. Pinhas‐Hamiel O, Lerner‐Geva L, Copperman NM, Jacobson MS. Lipid and insulin levels in obese children: changes with age and puberty. Obesity. 2007;15(11): 2825-31.
5. Pacini G. The hyperbolic equilibrium between insulin sensitivity and secretion. Nutr Metab Cardiovasc Dis. 2006;16(1):22-7.
6. Wan B, Wang X-R, Zhou Y-B, Zhang X, Huo K, Han Z-G. C12ORF39, a novel secreted protein with a typical amidation processing signal. Biosci Rep. 2010;30(1):1-10.
7. Walewski JL, Ge F, Gagner M, Inabnet WB, Pomp A, Branch AD, et al. Adipocyte accumulation of long-chain fatty acids in obesity is multifactorial, resulting from increased fatty acid uptake and decreased activity of genes involved in fat utilization. Obes Surg. 2010;20(1):93-107.
8. Walewski JL, Ge F, Lobdell Ht, Levin N, Schwartz GJ, Vasselli JR, et al. Spexin is a novel human peptide that reduces adipocyte uptake of long chain fatty acids and causes weight loss in rodents with diet-induced obesity. Obesity (Silver Spring). 2014;22(7):1643-52.
9. Kumar S, Hossain J, Nader N, Aguirre R, Sriram S, Balagopal PB. Decreased circulating levels of spexin in obese children. J Clin Endocrinol Metab. 2016;101(7):2931-6.
10. Kolodziejskii PA, Pruszynska-Oszmalek E, Korek E, Sassek M, Szczepankiewicz D, Kaczmarek P, et al. Serum levels of spexin and kisspeptin negatively correlate with obesity and insulin resistance in women. Physiol Res. 2018;67(1):45-56.
11. Venner AA, Lyon ME, Doyle-Baker PK. Leptin: A potential biomarker for childhood obesity? Clin Biochem. 2006;39(11):1047-56.
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23. Kahn HS. The "lipid accumulation product" performs better than the body mass index for recognizing cardiovascular risk: A population-based comparison. BMC Cardiovasc Disord. 2005;5(1):26-36.
24. Amato MC, Giordano C, Galia M, Criscimanna A, Vitabile S, Midiri M, et al. Visceral adiposity index (VAI): a reliable indicator of visceral fat function associated with cardiometabolic risk. Diabetes Care. 2010;33(4):920-2.
25. Mirmiran P, Bahadoran Z, Azizi F. Lipid accumulation product is associated with insulin resistance, lipid peroxidation, and systemic inflammation in type 2 diabetic patients. Endocrinol Metab. 2014;29(4):443-9.
26. Lewanczuk RZ, Paty BW, Toth EL. Comparison of the [13C] glucose breath test to the hyperinsulinemic-euglycemic clamp when determining insulin resistance. Diabetes Care. 2004;27(2):441-7.
27. Huang TT-K, Johnson MS, Goran MI. Development of a prediction equation for insulin sensitivity from anthropometry and fasting insulin in prepubertal and early pubertal children. Diabetes Care. 2002;25(7):1203-10.
28. McAuley KA, Williams SM, Mann JI, Walker RJ, Lewis-Barned NJ, Temple LA, et al. Diagnosing insulin resistance in the general population. Diabetes Care. 2001;24(3):460-4.
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33. Lee S-H, Yang HK, Ha H-S, Lee J-H, Kwon H-S, Park Y-M, et al. Changes in metabolic health status over time and risk of developing type 2 diabetes: A prospective cohort study. Medicine. 2015;94(40):1705-12.
34. Navarro-González D, Sánchez-Íñigo L, Fernández-Montero A, Pastrana-Delgado J, Martinez JA. TyG index change is more determinant for forecasting type 2 diabetes onset than weight gain. Medicine. 2016;95(19):3646.
35. Marson EC, Delevatti RS, Prado AK, Netto N, Kruel LF. Effects of aerobic, resistance, and combined exercise training on insulin resistance markers in overweight or obese children and adolescents: A systematic review and meta-analysis. Prev Med. 2016;93:211-8.
36. Hong H-R, Jeong J-O, Kong J-Y, Lee S-H, Yang S-H, Ha C-D, et al. Effect of walking exercise on abdominal fat, insulin resistance and serum cytokines in obese women. J Exerc Nutrition Biochem. 2014;18(3):277.
37. Baghersalimi M, Fathi R, Khosravi A, Bahreini A, Shirazi A. The effect of single session of aerobic interval exercise on serum spexin levels in active young men. Physiology of Exercise and Physical Activity. 2017;10(2):37-46. (In Persian)
38. Cole TJ, Bellizzi MC, Flegal KM, Dietz WH. Establishing a standard definition for child overweight and obesity worldwide: International survey. BMJ. 2000;320(7244):1240.
39. Tanaka H, Monahan KD, Seals DR. Age-predicted maximal heart rate revisited. J Am Coll Cardiol. 2001;37(1):153-6.
40. Kahn HS. The lipid accumulation product is better than BMI for identifying diabetes: a population-based comparison. Diabetes Care. 2006;29(1):151-3.
41. Garcés MJ, Hernández J, Queipo G, Klünder-Klünder M, Bustos M, Herrera A, et al. Novel gender-specific visceral adiposity index for Mexican pediatric population. Rev Med Hosp Gen (Mex). 2014;77(4):153-9.
42. Guerrero-Romero F, Simental-Mendía LE, Gonzalez-Ortiz M, Martínez-Abundis E, Ramos-Zavala MaG, Hernandez-Gonzalez SO, et al. The product of triglycerides and glucose, a simple measure of insulin sensitivity Comparison with the euglycemic-hyperinsulinemic clamp. J Clin Endocrinol Metab. 2010;95(7):3347-51.
43. Lakens D. Calculating and reporting effect sizes to facilitate cumulative science: a practical primer for t-tests and ANOVAs. Front Psychol. 2013;4:863-75.
44. Lin C-y, Huang T, Zhao L, Zhong LL, Lam WC, Fan B-m, et al. Circulating spexin levels negatively correlate with age, BMI, fasting glucose, and triglycerides in healthy adult women. J Endocr Soc. 2018;2(5):409-19.
45. Hodges SK, Teague AM, Dasari PS, Short KR. Effect of obesity and type 2 diabetes, and glucose ingestion on circulating spexin concentration in adolescents. Pediatr Diabetes. 2018;19(2):212-6.
46. Kumar S, Hossain MJ, Javed A, Kullo IJ, Balagopal PB. Relationship of circulating spexin with markers of cardiovascular disease: A pilot study in adolescents with obesity. Pediatr Obes. 2018;13(6):374-80.
47. Sanchez-Garrido MA, Tena-Sempere M. Metabolic control of puberty: Roles of leptin and kisspeptins. Horm Behav. 2013;64(2):187-94.
48. Liu Y, Li S, Qi X, Zhou W, Liu X, Lin H, et al. A novel neuropeptide in suppressing luteinizing hormone release in goldfish, Carassius auratus. Mol Cell Endocrinol. 2013;374(1-2):65-72.
49. Caumo A, Perseghin G, Brunani A, Luzi L. New insights on the simultaneous assessment of insulin sensitivity and β-cell function with the HOMA2 method. Diabetes Care. 2006;29(12):2733-4.
50. Balducci S, Cardelli P, Pugliese L, D’Errico V, Haxhi J, Alessi E, et al. Volume-dependent effect of supervised exercise training on fatty liver and visceral adiposity index in subjects with type 2 diabetes: The Italian diabetes exercise study (IDES). Diabetes Res Clin Pract. 2015;109(2):355-63.
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2. Mayer-Davis EJ, Lawrence JM, Dabelea D, Divers J, Isom S, Dolan L, et al. Incidence trends of type 1 and type 2 diabetes among youths, 2002–2012. N Engl J Med. 2017;376(15):1419-29.
3. 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.
4. Pinhas‐Hamiel O, Lerner‐Geva L, Copperman NM, Jacobson MS. Lipid and insulin levels in obese children: changes with age and puberty. Obesity. 2007;15(11): 2825-31.
5. Pacini G. The hyperbolic equilibrium between insulin sensitivity and secretion. Nutr Metab Cardiovasc Dis. 2006;16(1):22-7.
6. Wan B, Wang X-R, Zhou Y-B, Zhang X, Huo K, Han Z-G. C12ORF39, a novel secreted protein with a typical amidation processing signal. Biosci Rep. 2010;30(1):1-10.
7. Walewski JL, Ge F, Gagner M, Inabnet WB, Pomp A, Branch AD, et al. Adipocyte accumulation of long-chain fatty acids in obesity is multifactorial, resulting from increased fatty acid uptake and decreased activity of genes involved in fat utilization. Obes Surg. 2010;20(1):93-107.
8. Walewski JL, Ge F, Lobdell Ht, Levin N, Schwartz GJ, Vasselli JR, et al. Spexin is a novel human peptide that reduces adipocyte uptake of long chain fatty acids and causes weight loss in rodents with diet-induced obesity. Obesity (Silver Spring). 2014;22(7):1643-52.
9. Kumar S, Hossain J, Nader N, Aguirre R, Sriram S, Balagopal PB. Decreased circulating levels of spexin in obese children. J Clin Endocrinol Metab. 2016;101(7):2931-6.
10. Kolodziejskii PA, Pruszynska-Oszmalek E, Korek E, Sassek M, Szczepankiewicz D, Kaczmarek P, et al. Serum levels of spexin and kisspeptin negatively correlate with obesity and insulin resistance in women. Physiol Res. 2018;67(1):45-56.
11. Venner AA, Lyon ME, Doyle-Baker PK. Leptin: A potential biomarker for childhood obesity? Clin Biochem. 2006;39(11):1047-56.
12. Crujeiras AB, Carreira MC, Cabia B, Andrade S, Amil M, Casanueva FF. Leptin resistance in obesity: An epigenetic landscape. Life Sci. 2015;140:57-63.
13. Ge JF, Walewski JL, Anglade D, Berk PD. Regulation of hepatocellular fatty acid uptake in mouse models of fatty liver disease with and without functional leptin signaling: Roles of NfKB and SREBP-1C and the effects of spexin. Semin Liver Dis. 2016;36(4):360-72.
14. Agha M, Agha R. The rising prevalence of obesity: part A: impact on public health. Int J Surg Oncol. 2017;2(7):17.
15. Gu L, Ma Y, Gu M, Zhang Y, Yan S, Li N, et al. Spexin peptide is expressed in human endocrine and epithelial tissues and reduced after glucose load in type 2 diabetes. Peptides. 2015;71:232-9.
16. Ma A, Bai J, He M, Wong AO. Spexin as a Neuroendocrine Signal with Emerging Functions. Gen Comp Endocrinol. 2018;265:90-6.
17. Mirabeau O, Perlas E, Severini C, Audero E, Gascuel O, Possenti R, et al. Identification of novel peptide hormones in the human proteome by hidden Markov model screening. Genome Res. 2007;17(3):320-7.
18. Sassek M, Kolodziejski PA, Szczepankiewicz D, Pruszynska-Oszmalek E. Spexin in the physiology of pancreatic islets: Mutual interactions with insulin. Endocrine. 2018;63(3):1-7.
19. Sassek M, Kolodziejski PA, Strowski MZ, Nogowski L, Nowak KW, Mackowiak P. Spexin modulates functions of rat endocrine pancreatic cells. Pancreas. 2018;47(7):904-9.
20. Galic S, Oakhill JS, Steinberg GR. Adipose tissue as an endocrine organ. Mol Cell Endocrinol. 2010;316(2):129-39.
21. Sandeep S, Gokulakrishnan K, Velmurugan K, Deepa M, Mohan V. Visceral & subcutaneous abdominal fat in relation to insulin resistance & metabolic syndrome in non-diabetic south Indians. Indian J Med Res. 2010;131:629-35.
22. Després J-P, Lemieux I, Bergeron J, Pibarot P, Mathieu P, Larose E, et al. Abdominal obesity and the metabolic syndrome: Contribution to global cardiometabolic risk. Arterioscler Thromb Vasc Biol. 2008;28(6):1039-49.
23. Kahn HS. The "lipid accumulation product" performs better than the body mass index for recognizing cardiovascular risk: A population-based comparison. BMC Cardiovasc Disord. 2005;5(1):26-36.
24. Amato MC, Giordano C, Galia M, Criscimanna A, Vitabile S, Midiri M, et al. Visceral adiposity index (VAI): a reliable indicator of visceral fat function associated with cardiometabolic risk. Diabetes Care. 2010;33(4):920-2.
25. Mirmiran P, Bahadoran Z, Azizi F. Lipid accumulation product is associated with insulin resistance, lipid peroxidation, and systemic inflammation in type 2 diabetic patients. Endocrinol Metab. 2014;29(4):443-9.
26. Lewanczuk RZ, Paty BW, Toth EL. Comparison of the [13C] glucose breath test to the hyperinsulinemic-euglycemic clamp when determining insulin resistance. Diabetes Care. 2004;27(2):441-7.
27. Huang TT-K, Johnson MS, Goran MI. Development of a prediction equation for insulin sensitivity from anthropometry and fasting insulin in prepubertal and early pubertal children. Diabetes Care. 2002;25(7):1203-10.
28. McAuley KA, Williams SM, Mann JI, Walker RJ, Lewis-Barned NJ, Temple LA, et al. Diagnosing insulin resistance in the general population. Diabetes Care. 2001;24(3):460-4.
29. Moon S, Park JH, Jang E-J, Park Y-K, Yu JM, Park J-S, et al. The Cut-off Values of Surrogate Measures for Insulin Sensitivity in a Healthy Population in Korea according to the Korean National Health and Nutrition Examination Survey (KNHANES) 2007–2010. J Korean Med Sci. 2018;33(29):197-207.
30. Unger G, Benozzi SF, Perruzza F, Pennacchiotti GL. Triglycerides and glucose index: a useful indicator of insulin resistance. Endocrinol Nutr. 2014;61(10):533-40.
31. Nor NSM, Lee S, Bacha F, Tfayli H, Arslanian S. Triglyceride glucose index as a surrogate measure of insulin sensitivity in obese adolescents with normoglycemia, prediabetes, and type 2 diabetes mellitus: comparison with the hyperinsulinemic–euglycemic clamp. Pediatr Diabetes. 2016;17(6):458-65.
32. Vieira-Ribeiro SA, Fonseca PC, Andreoli CS, Ribeiro AQ, Hermsdorff HH, Pereira PF, et al. The TyG index cutoff point and its association with body adiposity and lifestyle in children. J Pediatr (Rio J). 2018;95(2):217-23.
33. Lee S-H, Yang HK, Ha H-S, Lee J-H, Kwon H-S, Park Y-M, et al. Changes in metabolic health status over time and risk of developing type 2 diabetes: A prospective cohort study. Medicine. 2015;94(40):1705-12.
34. Navarro-González D, Sánchez-Íñigo L, Fernández-Montero A, Pastrana-Delgado J, Martinez JA. TyG index change is more determinant for forecasting type 2 diabetes onset than weight gain. Medicine. 2016;95(19):3646.
35. Marson EC, Delevatti RS, Prado AK, Netto N, Kruel LF. Effects of aerobic, resistance, and combined exercise training on insulin resistance markers in overweight or obese children and adolescents: A systematic review and meta-analysis. Prev Med. 2016;93:211-8.
36. Hong H-R, Jeong J-O, Kong J-Y, Lee S-H, Yang S-H, Ha C-D, et al. Effect of walking exercise on abdominal fat, insulin resistance and serum cytokines in obese women. J Exerc Nutrition Biochem. 2014;18(3):277.
37. Baghersalimi M, Fathi R, Khosravi A, Bahreini A, Shirazi A. The effect of single session of aerobic interval exercise on serum spexin levels in active young men. Physiology of Exercise and Physical Activity. 2017;10(2):37-46. (In Persian)
38. Cole TJ, Bellizzi MC, Flegal KM, Dietz WH. Establishing a standard definition for child overweight and obesity worldwide: International survey. BMJ. 2000;320(7244):1240.
39. Tanaka H, Monahan KD, Seals DR. Age-predicted maximal heart rate revisited. J Am Coll Cardiol. 2001;37(1):153-6.
40. Kahn HS. The lipid accumulation product is better than BMI for identifying diabetes: a population-based comparison. Diabetes Care. 2006;29(1):151-3.
41. Garcés MJ, Hernández J, Queipo G, Klünder-Klünder M, Bustos M, Herrera A, et al. Novel gender-specific visceral adiposity index for Mexican pediatric population. Rev Med Hosp Gen (Mex). 2014;77(4):153-9.
42. Guerrero-Romero F, Simental-Mendía LE, Gonzalez-Ortiz M, Martínez-Abundis E, Ramos-Zavala MaG, Hernandez-Gonzalez SO, et al. The product of triglycerides and glucose, a simple measure of insulin sensitivity Comparison with the euglycemic-hyperinsulinemic clamp. J Clin Endocrinol Metab. 2010;95(7):3347-51.
43. Lakens D. Calculating and reporting effect sizes to facilitate cumulative science: a practical primer for t-tests and ANOVAs. Front Psychol. 2013;4:863-75.
44. Lin C-y, Huang T, Zhao L, Zhong LL, Lam WC, Fan B-m, et al. Circulating spexin levels negatively correlate with age, BMI, fasting glucose, and triglycerides in healthy adult women. J Endocr Soc. 2018;2(5):409-19.
45. Hodges SK, Teague AM, Dasari PS, Short KR. Effect of obesity and type 2 diabetes, and glucose ingestion on circulating spexin concentration in adolescents. Pediatr Diabetes. 2018;19(2):212-6.
46. Kumar S, Hossain MJ, Javed A, Kullo IJ, Balagopal PB. Relationship of circulating spexin with markers of cardiovascular disease: A pilot study in adolescents with obesity. Pediatr Obes. 2018;13(6):374-80.
47. Sanchez-Garrido MA, Tena-Sempere M. Metabolic control of puberty: Roles of leptin and kisspeptins. Horm Behav. 2013;64(2):187-94.
48. Liu Y, Li S, Qi X, Zhou W, Liu X, Lin H, et al. A novel neuropeptide in suppressing luteinizing hormone release in goldfish, Carassius auratus. Mol Cell Endocrinol. 2013;374(1-2):65-72.
49. Caumo A, Perseghin G, Brunani A, Luzi L. New insights on the simultaneous assessment of insulin sensitivity and β-cell function with the HOMA2 method. Diabetes Care. 2006;29(12):2733-4.
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