The Effect of Exercise on Leptin, Insulin, Cortisol and Lipid Profiles in Obese Children
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1 The Journal of International Medical Research 2009; 37: [first published online as 37(5) 4] The Effect of Exercise on Leptin, Insulin, Cortisol and Lipid Profiles in Obese Children K KARACABEY Higher School of Physical Education and Sports, Gaziantep University, Gaziantep, Turkey This prospective, randomized study investigated the effect of exercise on leptin, insulin, cortisol and lipid profiles in obese children. A total of 40 obese boys aged years with a body mass index (BMI) 30 kg/m 2 were randomly separated into an exercise group (n = 20) that underwent a 12-week aerobic exercise programme and a non-exercise (control) group (n = 20). The BMI, low-density lipoprotein, cortisol, leptin and insulin levels were significantly lower in the exercise group after 12 weeks compared with baseline values, whereas highdensity lipoprotein levels were significantly higher. In contrast, in the control group, low-density lipoprotein, cortisol and leptin levels were significantly higher after 12 weeks compared with baseline values while high-density lipoprotein levels were significantly lower. These findings indicate the importance of regular exercise in the regulation of body weight and protection against cardiovascular risk factors in obese children. KEY WORDS: CHILDHOOD OBESITY; LEPTIN; INSULIN; BODY MASS INDEX; EXERCISE Introduction Many studies on the effects of exercise on coronary heart disease, stroke, hypertension, type 2 diabetes mellitus and lipid defects, conditions which are all more frequently encountered in obese people, have demonstrated that physical activity has a significant role in the treatment of obesity and preventing its related complications. 1 Obesity and excess weight cause serious health problems that can begin at a young age and continue throughout life, including cardiovascular disease, 2,3 some types of cancer, 4 6 diabetes 7 and increased mortality. 8,9 Obesity negatively affects the course of many diseases, and is also associated with psychological and psychosocial trauma. 10 This social dimension of obesity should not be ignored, since psychological and psychosocial factors can have a negative impact on health. The hormone leptin, a product of the Ob gene and secreted by adipose tissue, acts by decreasing food intake while increasing energy expenditure. 11 The leptin concentration in the blood is positively correlated with body fat mass 12,13 and is adjusted by nutritional status. 14 Nutrition indicators can be classified as having shortor long-term actions and may be related to hunger or repletion, thinness or fatness, and peripheral or central activity. Peripheral 1472
2 hunger indicators include glucose, cortisol and ghlerin, while peripheral repletion indicators include insulin, leptin, glucagon, bombesin, somatostatin and cholecystokinin. 15 Nutritional impairment leads to a fasting state and a substantial decrease in the circulating leptin concentration, while overfeeding results in an increase in circulating levels of leptin. 11 The hormonal changes observed in obese people can be explained by alterations in hypothalamic pituitary adrenal (HPA) activity and cortisol secretion. A defective HPA axis is thought to play a role in the development of obesity; central glucocorticoid receptor insufficiency has been proposed as a cause of obesity, and a relationship has been established between glucocorticoid receptor gene polymorphism and central obesity. 12 Obesity has been shown to be associated with a decrease in growth hormone and testosterone levels in males, and an increase in testosterone and androstenedione levels and a decrease in progesterone levels in females. 12 An increase in insulin level and the development of insulin resistance have also been shown to be linked to obesity. 16 Weight gain in childhood, even at moderate levels, tends to continue into adulthood and can cause serious problems. 17 The duration of obesity is an independent indicator for the effects of obesity on health. 16 The development of persistent obesity is more likely when weight gain occurs in early childhood, during the pre-pubertal development period or during adolescence. 18 This prospective, randomized study investigated the effects of exercise on serum leptin, insulin, cortisol and lipid profiles in obese children. Patients and methods PATIENTS Boys aged years with obesity, defined as a body mass index (BMI) of 30 kg/m 2, 19 and who were recruited from general paediatric outpatient clinics between 9 April and 30 June 2009 were included in the study. Exclusion criteria included the presence of cardiovascular, haematological or endocrinological disorders, or any other systemic disease. Patients receiving medications, with a history of recent intercurrent illness or who were currently participating in any organized physical activity training programme were also excluded from the study. The study conformed to the principles outlined in the Declaration of Helsinki and was approved by the Gaziantep University Local Research Ethics Committee. Written informed consent was obtained from the parents or guardians of all the patients involved in the study. All the study participants undertook the same diet programme. EXERCISE PROGRAMME The boys were randomly separated into an exercise group and a non-exercise control group. Those in the exercise group performed set exercises 3 days a week for 12 weeks. At each training session, those in the exercise group performed warm-up exercises lasting 5 10 min, followed by a min walking jogging exercise with a targeted heart rate reserve of 60 65%, and 5 10 min of relaxation exercises at the end of the exercise period. The heart rate reserve, used to calculate the intensity of exercise, was determined by counting heart beats at the carotid artery 10 s after the cessation of exercise and then using the Karvonen equation: 20 [heart rate maximum heart rate rest ) ( ) + heart rate rest ]. Heart rate was recorded throughout the exercise period using a Polar Pacer heart rate monitor (Polar Vantage, Kempele, Finland). 1473
3 PATIENT ASSESSMENTS Venous blood samples were taken from all patients in the exercise group at 08:00 h at the start of the study and at the same time of day on completion of the 12-week exercise programme. Samples were also taken from the control group at similar times. Serum was separated off as soon as possible and stored at 80 C until biochemical analysis. High-density lipoprotein (HDL) and lowdensity lipoprotein (LDL) levels were measured using an enzymatic colorimetric assay (Roche/Hitachi Modular; Hitachi, Tokyo, Japan). Insulin and cortisol levels were measured with an Immulite Analyser (Diagnostic Product Corp., Los Angeles, CA, USA), which uses chemiluminescence. Serum leptin levels were determined by enzymelinked immunosorbent assay (ELISA) in a Triturus ELISA analyser (Grifols International, Barcelona, Spain) using a human leptin kit (DRG Diagnostics, Marburg, Germany) according to the manufacturer s instruction. STATISTICAL ANALYSIS Data are reported as mean ± SD and were analysed using the SPSS statistical package, version 13.0 (SPSS Inc., Chicago, IL, USA) for Windows and using the paired samples t- test. A P-value of < 0.05 was considered to be statistically significant. Results A total of 40 obese boys were included in the study: 20 in the exercise group and 20 in the non-exercise, control group. Mean ± SD age was 11.8 ± 0.5 years in the exercise group and 11.2 ± 0.8 years in the control group, and mean ± SD height was 1.40 ± 0.1 m and 1.43 ± 0.2 m, respectively. There were no significant differences between the two groups. Changes in body weight, BMI and insulin, LDL, HDL, leptin and cortisol levels are given in Table 1. Compared with baseline, there were significant decreases in the exercise group after 12 weeks for weight (P = 0.01) and BMI (P = 0.001), but no changes in the TABLE 1: Changes in body weight, body mass index and various lipid and hormone levels in obese boys undergoing a 12-week exercise programme compared with controls Exercise group Control group (n = 20) (n = 20) Statistical Statistical 0 weeks significance 0 weeks significance (baseline) 12 weeks 0 vs 12 weeks (baseline) 12 weeks 0 vs 12 weeks Body weight (kg) 61.7 ± ± 7.1 P = ± ± 9.6 NS Body mass index (kg/m 2 ) 34.9 ± ± 2.7 P = ± ± 3.4 NS Insulin (mu/ml) 37.1 ± ± 6.1 P = ± ± 7.3 NS Low-density lipoprotein (mg/dl) 87.2 ± ± 9.4 P = ± ± 10.8 P = High-density lipoprotein (mg/dl) 51.9 ± ± 7.5 P = ± ± 3.4 P = Leptin (ng/ml) 23.3 ± ± 9.6 P = ± ± 8.3 P = Cortisol (mg/dl) 16.7 ± ± 0.4 P = ± ± 6.7 P = Values are means ± SD. NS, not statistically significant (P > 0.05). 1474
4 control group. There were also significant decreases after 12 weeks in the exercise group compared with baseline values for leptin (P = 0.001), cortisol (P = 0.001) and insulin levels (P = 0.04), whereas in the control group there were significant increases in leptin (P = 0.001) and cortisol (P = 0.001) levels over the study period. Statistically significant differences were also seen in lipid levels compared with baseline after 12 weeks of exercising: LDL levels decreased (P = 0.001) while HDL levels increased (P = 0.001). In contrast, in the control group, LDL levels increased (P = 0.002) and HDL levels decreased (P = 0.001) between the start and end of the 12-week study period. Discussion The hormone, leptin, regulates energy balance by increasing energy expenditure during exercise and, thereby, reducing total body fat: the effects of exercising on leptin levels are thought to be mediated by the sympatho-adrenergic system. 21 The level of leptin in the exercise group decreased significantly in the present study. It has previously been shown that serum levels of leptin change with the intensity of exercise and the amount of the energy expended, 21 in addition to the effects of glucose, fatty acids, the sympathetic nervous system, insulin, glucocorticoids, growth hormones and catecholamines 20,22 24 on the synthesis and secretion of leptin. 25 The decrease in serum levels of leptin in the exercise group in the present study was likely to be related to the decrease in BMI. It has been shown that exercise that is irregular and of short duration does not cause any change in BMI, 19 and so would not be expected to produce a change in the leptin level. The findings from the present study are consistent with those reported in the literature. Essig et al. 26 found that leptin concentrations did not change soon after or 24 h after exercise at 70% maximum oxygen consumption (VO 2 max), but decreased to a level of 30% 48 h after exercising. Similarly, Olive and Miller 27 reported that the leptin concentration did not change immediately after exercising for 60 min at 70% VO 2 max, but decreased by 18% and 40% at 24 and 48 h after exercise, respectively. Gutin et al., 28 who demonstrated that plasma leptin concentrations in obese children decreased after a 4-month exercise programme (40 min/day for 5 days a week) and then increased after the next 4 months of exercise cessation, concluded that leptin levels reflect changes in energy balance. In other studies, 22,29 leptin has been shown to regulate glucose homoeostasis by reversing lipid accumulation and beneficially affecting insulin resistance and cell function. It has also been demonstrated that leptin has a stimulant effect on fat oxidation in obese people. 30 The findings in the present study and in previously published studies show that leptin levels decrease as a result of the decrease in adipose tissue mass due to chronic exercise. 27 The secretion of insulin was decreased in the exercise group after 12 weeks in the present study. A decrease in the secretion of insulin and an increase in the levels of counter-insulin regulatory hormones have previously been observed during exercise. 31 Exercise increases the uptake of glucose by muscle cells which, consequently, increases the oxidation of glucose. This effect seems to be independent of insulin. 31,32 It has been demonstrated that glucose consumption increases during exercise in patients with diabetes 33 and that glucose tolerance is increased both at rest and after exercise. 32 Several studies have reported an increased expression of leptin in obese humans both at 1475
5 the mrna and protein level. 34,35 A common finding of such studies is that the serum leptin level in humans is closely correlated with BMI or other measures of body fat, but is less closely correlated with serum insulin even though this association is still significant. 3,35 This relationship is weaker when intra-abdominal fat mass is taken into account, 36 possibly due to a lower expression of leptin in visceral adipose tissue. 37 Similar to the results obtained in experiments using animal models, both insulin and cortisol have been shown to be potent promoters of leptin production in cultured human adipocytes. 20,37,38 Insulin and, less remarkably, cortisol were found to have significant positive effects on serum leptin, whereas dehydroepiandrostenedione had a weaker negative influence in a multiple regression analysis using BMI as an index of degree of body fat. 39 These findings are in agreement with experimental data that demonstrate that both insulin and cortisol are stimulators of leptin expression in cultured human adipocytes. 40,41 The findings of the present study are consistent with studies demonstrating that insulin secretion is decreased in response to exercise, particularly in children, thereby increasing the peripheral consumption of glucose. 32 Exercising and intense training have been shown to increase hormone secretions (e.g. cortisol, adrenaline, noradrenaline, testosterone, growth hormone, insulin-like growth factor 1, insulin, glucose) and to regulate blood lipid levels, revealing the inter-related nature of the endocrine functions. 42 Essig et al. 26 suggested that changes in growth hormone, cortisol, insulin, testosterone, adrenaline and noradrenaline levels cause delayed leptin depletion. Cortisol degradation increases in obese individuals due to excess adipose tissue; the serum cortisol level is kept normal by the compensatory effects of adrenocorticotrophic hormone. 20,40 Anderson et al. 40 found no significant relationship between minimal weight loss and nocturnal cortisol secretion. In the present study, LDL levels decreased and HDL levels increased after 12 weeks of exercise. These changes are in line with those previously reported in the published literature. It has been reported elsewhere that exercising 5 7 days a week increased the HDL level, and that weekly regular exercise of running 1 km caused a 0.2 mg/dl increase in HDL and a 0.1 mg/dl decrease in LDL levels. 41 In addition, in the present study, weight and BMI both fell in the exercise group after 12 weeks. Mertens et al. 36 reported that a 12-month daily walking programme in eight male and four female obese subjects was associated with a reduction in mean weight from 70.7 kg to 65.6 kg and in mean ± SD BMI from 27.2 ± 1.3 kg/m 2 to 25.2 ± 1.7 kg/m 2. Likewise, Nindl et al. 43 concluded that regular and long-term exercise reduced body weight and BMI in obese women. The results of the present study highlight the significance of exercise programmes, as well exercising itself, in the treatment of obesity. The programme implemented in this study, which was long-term (12 weeks) and included aerobic routines, is likely to have been the driving force behind the positive effect on BMI. Obesity develops as triglyceride deposits increase in adipose tissue, with a consequential decrease in the insulin response in muscle and adipose tissue. 12,17 Resistance to insulin is undoubtedly one of the most significant mechanisms causing complications of obesity. 12 The present study showed that positive changes were observed in body weight, body composition and blood lipid levels in children aged years after
6 weeks of regular exercise. These findings, which are consistent with the literature, indicate the significance of regular exercising in the regulation of body weight and prevention of obesity. Protection against cardiovascular risk factors, by decreasing LDL and increasing HDL, can be facilitated by training programmes, nutritional intervention and other similar lifestyle changes. The most important benefit of implementing an exercise regime alongside dietary intervention is that of keeping body proteins intact while mobilizing fats. In conclusion, a significant decrease in the risk of chronic disease associated with obesity and, consequently, an increase in quality of life, is achievable if the pharmacological treatment of obesity is combined with the adoption of exercise as a routine lifestyle habit together with dietary intervention. Acknowledgements The author would like to thank Erdal Zorba and Cengiz Taskin, (Higher School of Physical Education and Sports, Gazi and Gaziantep University), Nevin Ilhan and Suleyman Aydin (Department of Biochemistry, Firat University Medical Centre, Elazig, Turkey) and Figen Ciloglu (GENLAB Medical Diagnostics and Research Laboratory, Istanbul, Turkey, and Vice- President of the Society of Multidisciplinary Research in Science and Technology) for their contributions to this study. Conflicts of interest The authors had no conflicts of interest to declare in relation to this article. Received for publication 12 June 2009 Accepted subject to revision 15 June 2009 Revised accepted 18 September 2009 Copyright 2009 Field House Publishing LLP References 1 Barness LA: Obesity in children. Fetal Pediatr Pathol 2007; 26: Manson JE, Colditz GA, Stampfer MJ, et al: A prospective study of obesity and risk of coronary heart disease in women. N Engl J Med 1990; 322: Rexrode KM, Hennekens CH, Willett WC, et al: A prospective study of body mass index, weight change, and risk of stroke in women. JAMA 1997; 277: Huang Z, Hankinson SE, Colditz GA, et al: Dual effects of weight and weight gain on breast cancer risk. JAMA 1997; 278: Shoff SM, Newcomb PA: Diabetes, body size, and risk of endometrial cancer. Am J Epidemiol 1998; 148: Törnberg SA, Carstensen JM: Relationship between Quetelet s index and cancer of breast and female genital tract in 47,000 women followed for 25 years. Br J Cancer 1994; 69: McCall A, Raj R: Exercise for prevention of obesity and diabetes in children and adolescents. Clin Sports Med 2009; 28: Manson JE, Willett WC, Stampfer MJ, et al: Body weight and mortality among women. N Engl J Med 1995; 333: Willett WC, Dietz WH, Colditz GA: Guidelines for healthy weight. N Engl J Med 1999; 341: Fine JT, Colditz GA, Coakley EH, et al: A prospective study of weight change and healthrelated quality of life in women. JAMA 1999; 282: Caro JF, Sinha MK, Kolaczynski JW, et al: Leptin: the tale of an obesity gene. Diabetes 1996; 45: Wadden TA, Stunkard AJ (eds): Handbook of Obesity Treatment, 1st edn. New York: Guilford Press, 2004; pp Nagy TR, Gower BA, Trowbridge CA, et al: Effects of gender, ethnicity, body composition, and fat distribution on serum leptin concentrations in children. J Clin Endocrinol Metab 1997; 82: Rosenbaum M, Nicolson M, Hirsch J, et al: Effects of weight change on plasma leptin concentrations and energy expenditure. J Clin Endocrinol Metab 1997; 82: Lustig RH: The neuroendocrinology of childhood obesity. Pediatr Clin North Am 2001; 48: McCance DR, Pettitt DJ, Hanson RL, et al: Glucose, insulin concentrations and obesity in childhood and adolescence as predictors of NIDDM. Diabetologia 1994; 37: Sgro M, McGuigan MR, Pettigrew S, et al: The 1477
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