Skip to main content
Top
Published in: Sports Medicine 6/2018

01-06-2018 | Systematic Review

The Effect of Chronic Exercise Training on Leptin: A Systematic Review and Meta-Analysis of Randomized Controlled Trials

Authors: Michael V. Fedewa, Elizabeth D. Hathaway, Christie L. Ward-Ritacco, Tyler D. Williams, Ward C. Dobbs

Published in: Sports Medicine | Issue 6/2018

Login to get access

Abstract

Background

Leptin is a hormone associated with satiety, lipid oxidation, energy expenditure, and energy homeostasis. To date, the current body of research examining the effect of chronic exercise training on leptin has yielded inconsistent results.

Objective

The purpose of this meta-analysis was to provide a quantitative estimate of the magnitude of change in leptin levels following participation in exercise interventions lasting ≥ 2 weeks.

Methods

All studies included were peer-reviewed and published in English. To be included, studies randomized human participants to an exercise training group or non-exercise comparison group for an exercise training intervention. Leptin levels were measured at baseline, during, and/or after completion of the exercise training program. Random-effects models were used to aggregate a mean effect size (ES) and 95% confidence intervals (CIs), and identify potential moderators.

Results

Seventy-two randomized controlled trials met the inclusion criteria and resulted in 107 effects (n = 3826). The mean ES of 0.24 (95% CI 0.16–0.32, p < 0.0001) indicated a decrease in leptin following an exercise training program. A decrease in %Fat (β = − 0.07, p < 0.01) was associated with a decrease in leptin after accounting for the type of control group (β = − 0.38, p < 0.0001) used in each study.

Conclusion

These results suggest that engaging in chronic exercise training (≥ 2 weeks) is associated with a decrease in leptin levels for individuals regardless of age and sex. However, a greater decrease in leptin occurred with a decreased percentage of body fat.
Appendix
Available only for authorised users
Literature
1.
go back to reference Kelly T, Yang W, Chen C, Reynolds K, He J. Global burden of obesity in 2005 and projections to 2030. Int J Obes. 2008;32(9):1431–7.CrossRef Kelly T, Yang W, Chen C, Reynolds K, He J. Global burden of obesity in 2005 and projections to 2030. Int J Obes. 2008;32(9):1431–7.CrossRef
2.
go back to reference Ogden CL, Carroll MD, Fryar CD, Flegal KM. Prevalence of obesity among adults and youth: United States, 2011–2014. NCHS Data Brief. 2015;219:1–8. Ogden CL, Carroll MD, Fryar CD, Flegal KM. Prevalence of obesity among adults and youth: United States, 2011–2014. NCHS Data Brief. 2015;219:1–8.
3.
go back to reference Pi-Sunyer FX, Becker DM, Bouchard C, Carleton R, Colditz G, Dietz W, et al. Clinical guidelines on the identification, evaluation, and treatment of overweight and obesity in adults. Am J Clin Nutr. 1998;68(4):899–917.CrossRef Pi-Sunyer FX, Becker DM, Bouchard C, Carleton R, Colditz G, Dietz W, et al. Clinical guidelines on the identification, evaluation, and treatment of overweight and obesity in adults. Am J Clin Nutr. 1998;68(4):899–917.CrossRef
5.
go back to reference Klem ML, Wing RR, McGuire MT, Seagle HM, Hill JO. A descriptive study of individuals successful at long-term maintenance of substantial weight loss. Am J Clin Nutr. 1997;66(2):239–46.PubMedCrossRef Klem ML, Wing RR, McGuire MT, Seagle HM, Hill JO. A descriptive study of individuals successful at long-term maintenance of substantial weight loss. Am J Clin Nutr. 1997;66(2):239–46.PubMedCrossRef
6.
go back to reference Thorogood A, Mottillo S, Shimony A, Filion KB, Joseph L, Genest J, et al. Isolated aerobic exercise and weight loss: a systematic review and meta-analysis of randomized controlled trials. Am J Med. 2011;124(8):747–55.PubMedCrossRef Thorogood A, Mottillo S, Shimony A, Filion KB, Joseph L, Genest J, et al. Isolated aerobic exercise and weight loss: a systematic review and meta-analysis of randomized controlled trials. Am J Med. 2011;124(8):747–55.PubMedCrossRef
7.
go back to reference Pontzer H. Constrained total energy expenditure and the evolutionary biology of energy balance. Exerc Sport Sci Rev. 2015;43(3):110–6.PubMedCrossRef Pontzer H. Constrained total energy expenditure and the evolutionary biology of energy balance. Exerc Sport Sci Rev. 2015;43(3):110–6.PubMedCrossRef
8.
go back to reference Schwartz MW, Woods SC, Porte D, Seeley RJ, Baskin DG. Central nervous system control of food intake. Nature. 2000;404(6778):661–71.PubMedCrossRef Schwartz MW, Woods SC, Porte D, Seeley RJ, Baskin DG. Central nervous system control of food intake. Nature. 2000;404(6778):661–71.PubMedCrossRef
9.
go back to reference Klok MD, Jakobsdottir S, Drent ML. The role of leptin and ghrelin in the regulation of food intake and body weight in humans: a review. Obes Rev. 2007;8(1):21–34.PubMedCrossRef Klok MD, Jakobsdottir S, Drent ML. The role of leptin and ghrelin in the regulation of food intake and body weight in humans: a review. Obes Rev. 2007;8(1):21–34.PubMedCrossRef
10.
go back to reference Galic S, Oakhill JS, Steinberg GR. Adipose tissue as an endocrine organ. Mol Cell Endocrinol. 2010;316(2):129–39.PubMedCrossRef Galic S, Oakhill JS, Steinberg GR. Adipose tissue as an endocrine organ. Mol Cell Endocrinol. 2010;316(2):129–39.PubMedCrossRef
11.
go back to reference Hilton LK, Loucks AB. Low energy availability, not exercise stress, suppresses the diurnal rhythm of leptin in healthy young women. Am J Physiol Endocrinol Metab. 2000;278(1):E43–9.PubMedCrossRef Hilton LK, Loucks AB. Low energy availability, not exercise stress, suppresses the diurnal rhythm of leptin in healthy young women. Am J Physiol Endocrinol Metab. 2000;278(1):E43–9.PubMedCrossRef
12.
go back to reference Mars M, de Graaf C, de Groot CP, van Rossum CT, Kok FJ. Fasting leptin and appetite responses induced by a 4-day 65%-energy-restricted diet. Int J Obes (Lond). 2006;30(1):122–8.CrossRef Mars M, de Graaf C, de Groot CP, van Rossum CT, Kok FJ. Fasting leptin and appetite responses induced by a 4-day 65%-energy-restricted diet. Int J Obes (Lond). 2006;30(1):122–8.CrossRef
13.
go back to reference Keim NL, Stern JS, Havel PJ. Relation between circulating leptin concentrations and appetite during a prolonged, moderate energy deficit in women. Am J Clin Nutr. 1998;68(4):794–801.PubMedCrossRef Keim NL, Stern JS, Havel PJ. Relation between circulating leptin concentrations and appetite during a prolonged, moderate energy deficit in women. Am J Clin Nutr. 1998;68(4):794–801.PubMedCrossRef
14.
go back to reference Rosenbaum M, Murphy EM, Heymsfield SB, Matthews DE, Leibel RL. Low dose leptin administration reverses effects of sustained weight-reduction on energy expenditure and circulating concentrations of thyroid hormones. J Clin Endocrinol Metab. 2002;87(5):2391–4.PubMedCrossRef Rosenbaum M, Murphy EM, Heymsfield SB, Matthews DE, Leibel RL. Low dose leptin administration reverses effects of sustained weight-reduction on energy expenditure and circulating concentrations of thyroid hormones. J Clin Endocrinol Metab. 2002;87(5):2391–4.PubMedCrossRef
15.
go back to reference Rosenbaum M, Goldsmith R, Bloomfield D, Magnano A, Weimer L, Heymsfield S, et al. Low-dose leptin reverses skeletal muscle, autonomic, and neuroendocrine adaptations to maintenance of reduced weight. J Clin Investig. 2005;115(12):3579–86.PubMedPubMedCentralCrossRef Rosenbaum M, Goldsmith R, Bloomfield D, Magnano A, Weimer L, Heymsfield S, et al. Low-dose leptin reverses skeletal muscle, autonomic, and neuroendocrine adaptations to maintenance of reduced weight. J Clin Investig. 2005;115(12):3579–86.PubMedPubMedCentralCrossRef
16.
go back to reference Heymsfield SB, Greenberg AS, Fujioka K, Dixon RM, Kushner R, Hunt T, et al. Recombinant leptin for weight loss in obese and lean adults: a randomized, controlled, dose-escalation trial. JAMA. 1999;282(16):1568–75.PubMedCrossRef Heymsfield SB, Greenberg AS, Fujioka K, Dixon RM, Kushner R, Hunt T, et al. Recombinant leptin for weight loss in obese and lean adults: a randomized, controlled, dose-escalation trial. JAMA. 1999;282(16):1568–75.PubMedCrossRef
17.
go back to reference Myers MG Jr, Leibel RL, Seeley RJ, Schwartz MW. Obesity and leptin resistance: distinguishing cause from effect. Trends Endocrinol Metab. 2010;21(11):643–51.PubMedPubMedCentralCrossRef Myers MG Jr, Leibel RL, Seeley RJ, Schwartz MW. Obesity and leptin resistance: distinguishing cause from effect. Trends Endocrinol Metab. 2010;21(11):643–51.PubMedPubMedCentralCrossRef
18.
go back to reference Git KC, Adan RA. Leptin resistance in diet-induced obesity: the role of hypothalamic inflammation. Obes Rev. 2015;16(3):207–24.PubMedCrossRef Git KC, Adan RA. Leptin resistance in diet-induced obesity: the role of hypothalamic inflammation. Obes Rev. 2015;16(3):207–24.PubMedCrossRef
19.
go back to reference Hulver MW, Houmard JA. Plasma leptin and exercise: recent findings. Sports Med. 2003;33(7):473–82.PubMedCrossRef Hulver MW, Houmard JA. Plasma leptin and exercise: recent findings. Sports Med. 2003;33(7):473–82.PubMedCrossRef
20.
go back to reference Mezghanni N, Mnif M, Chtourou H, Chaabouni K, Masmoudi L, Lassoued A, et al. Effect of aerobic training on insulin resistance and C-reactive protein (CRP) levels and subcutaneous abdominal in obese women. Sport Sci Health. 2014;10(2):111–8.CrossRef Mezghanni N, Mnif M, Chtourou H, Chaabouni K, Masmoudi L, Lassoued A, et al. Effect of aerobic training on insulin resistance and C-reactive protein (CRP) levels and subcutaneous abdominal in obese women. Sport Sci Health. 2014;10(2):111–8.CrossRef
21.
go back to reference Fatouros IG, Tournis S, Leontsini D, Jamurtas AZ, Sxina M, Thomakos P, et al. Leptin and adiponectin responses in overweight inactive elderly following resistance training and detraining are intensity related. J Clin Endocrinol Metab. 2005;90(11):5970–7.PubMedCrossRef Fatouros IG, Tournis S, Leontsini D, Jamurtas AZ, Sxina M, Thomakos P, et al. Leptin and adiponectin responses in overweight inactive elderly following resistance training and detraining are intensity related. J Clin Endocrinol Metab. 2005;90(11):5970–7.PubMedCrossRef
22.
go back to reference Shalitin S, Ashkenazi-Hoffnung L, Yackobovitch-Gavan M, Nagelberg N, Karni Y, Hershkovitz E, et al. Effects of a twelve-week randomized intervention of exercise and/or diet on weight loss and weight maintenance, and other metabolic parameters in obese preadolescent children. Horm Res. 2009;72(5):287–301.PubMedCrossRef Shalitin S, Ashkenazi-Hoffnung L, Yackobovitch-Gavan M, Nagelberg N, Karni Y, Hershkovitz E, et al. Effects of a twelve-week randomized intervention of exercise and/or diet on weight loss and weight maintenance, and other metabolic parameters in obese preadolescent children. Horm Res. 2009;72(5):287–301.PubMedCrossRef
23.
go back to reference Lambert CP, Sullivan DH, Evans WJ. Effects of testosterone replacement and/or resistance training on interleukin-6, tumor necrosis factor alpha, and leptin in elderly men ingesting megestrol acetate: a randomized controlled trial. J Gerontol A Biol Sci Med Sci. 2003;58(2):165–70.PubMedCrossRef Lambert CP, Sullivan DH, Evans WJ. Effects of testosterone replacement and/or resistance training on interleukin-6, tumor necrosis factor alpha, and leptin in elderly men ingesting megestrol acetate: a randomized controlled trial. J Gerontol A Biol Sci Med Sci. 2003;58(2):165–70.PubMedCrossRef
24.
go back to reference Lucotti P, Monti LD, Setola E, Galluccio E, Gatti R, Bosi E, et al. Aerobic and resistance training effects compared to aerobic training alone in obese type 2 diabetic patients on diet treatment. Diabetes Res Clin Pract. 2011;94(3):395–403.PubMedCrossRef Lucotti P, Monti LD, Setola E, Galluccio E, Gatti R, Bosi E, et al. Aerobic and resistance training effects compared to aerobic training alone in obese type 2 diabetic patients on diet treatment. Diabetes Res Clin Pract. 2011;94(3):395–403.PubMedCrossRef
25.
go back to reference Kraemer RR, Chu H, Castracane VD. Leptin and exercise. Exp Biol Med. 2002;227(9):701–8.CrossRef Kraemer RR, Chu H, Castracane VD. Leptin and exercise. Exp Biol Med. 2002;227(9):701–8.CrossRef
26.
go back to reference Bouassida A, Zalleg D, Bouassida S, Zaouali M, Feki Y, Zbidi A, et al. Leptin, its implication in physical exercise and training: a short review. J Sports Sci Med. 2006;5(2):172–81.PubMedPubMedCentral Bouassida A, Zalleg D, Bouassida S, Zaouali M, Feki Y, Zbidi A, et al. Leptin, its implication in physical exercise and training: a short review. J Sports Sci Med. 2006;5(2):172–81.PubMedPubMedCentral
27.
go back to reference Bouassida A, Chamari K, Zaouali M, Feki Y, Zbidi A, Tabka Z. Review on leptin and adiponectin responses and adaptations to acute and chronic exercise. Br J Sports Med. 2010;44(9):620–30.PubMedCrossRef Bouassida A, Chamari K, Zaouali M, Feki Y, Zbidi A, Tabka Z. Review on leptin and adiponectin responses and adaptations to acute and chronic exercise. Br J Sports Med. 2010;44(9):620–30.PubMedCrossRef
29.
go back to reference Legakis IN, Mantzouridis T, Saramantis A, Lakka-Papadodima E. Rapid decrease of leptin in middle-aged sedentary individuals after 20 minutes of vigorous exercise with early recovery after the termination of the test. J Endocrinol Investig. 2004;27(2):117–20.CrossRef Legakis IN, Mantzouridis T, Saramantis A, Lakka-Papadodima E. Rapid decrease of leptin in middle-aged sedentary individuals after 20 minutes of vigorous exercise with early recovery after the termination of the test. J Endocrinol Investig. 2004;27(2):117–20.CrossRef
30.
go back to reference Zafeiridis A, Smilios I, Considine RV, Tokmakidis SP. Serum leptin responses after acute resistance exercise protocols. J Appl Physiol. 2003;94(2):591–7.PubMedCrossRef Zafeiridis A, Smilios I, Considine RV, Tokmakidis SP. Serum leptin responses after acute resistance exercise protocols. J Appl Physiol. 2003;94(2):591–7.PubMedCrossRef
31.
go back to reference Gomez-Merino D, Chennaoui M, Drogou C, Bonneau D, Guezennec CY. Decrease in serum leptin after prolonged physical activity in men. Med Sci Sports Exerc. 2002;34(10):1594–9.PubMedCrossRef Gomez-Merino D, Chennaoui M, Drogou C, Bonneau D, Guezennec CY. Decrease in serum leptin after prolonged physical activity in men. Med Sci Sports Exerc. 2002;34(10):1594–9.PubMedCrossRef
32.
go back to reference Moher D, Liberati A, Tetzlaff J, Altman D. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. BMJ. 2009;339:332–6.CrossRef Moher D, Liberati A, Tetzlaff J, Altman D. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. BMJ. 2009;339:332–6.CrossRef
33.
go back to reference Hasson RE, Adam TC, Davis JN, Kelly LA, Ventura EE, Byrd-Williams CE, et al. Randomized controlled trial to improve adiposity, inflammation, and insulin resistance in obese African-American and Latino youth. Obesity (Silver Spring). 2012;20(4):811–8.CrossRef Hasson RE, Adam TC, Davis JN, Kelly LA, Ventura EE, Byrd-Williams CE, et al. Randomized controlled trial to improve adiposity, inflammation, and insulin resistance in obese African-American and Latino youth. Obesity (Silver Spring). 2012;20(4):811–8.CrossRef
34.
go back to reference Mason C, Foster-Schubert KE, Imayama I, Xiao LR, Kong A, Campbell KL, et al. History of weight cycling does not impede future weight loss or metabolic improvements in postmenopausal women. Metab Clin Exp. 2013;62(1):127–36.PubMedCrossRef Mason C, Foster-Schubert KE, Imayama I, Xiao LR, Kong A, Campbell KL, et al. History of weight cycling does not impede future weight loss or metabolic improvements in postmenopausal women. Metab Clin Exp. 2013;62(1):127–36.PubMedCrossRef
35.
go back to reference Straznicky NE, Lambert EA, Grima MT, Eikelis N, Nestel PJ, Dawood T, et al. The effects of dietary weight loss with or without exercise training on liver enzymes in obese metabolic syndrome subjects. Diabetes Obes Metab. 2012;14(2):139–48.PubMedCrossRef Straznicky NE, Lambert EA, Grima MT, Eikelis N, Nestel PJ, Dawood T, et al. The effects of dietary weight loss with or without exercise training on liver enzymes in obese metabolic syndrome subjects. Diabetes Obes Metab. 2012;14(2):139–48.PubMedCrossRef
36.
go back to reference Nuri R, Moghaddasi M, Darvishi H, Izadpanah A. Effect of aerobic exercise on leptin and ghrelin in patients with colorectal cancer. J Cancer Res Ther. 2016;12(1):169–74.PubMedCrossRef Nuri R, Moghaddasi M, Darvishi H, Izadpanah A. Effect of aerobic exercise on leptin and ghrelin in patients with colorectal cancer. J Cancer Res Ther. 2016;12(1):169–74.PubMedCrossRef
37.
go back to reference Foster-Schubert KE, McTiernan A, Frayo RS, Schwartz RS, Rajan KB, Yasui Y, et al. Human plasma ghrelin levels increase during a one-year exercise program. J Clin Endocrinol Metab. 2005;90(2):820–5.PubMedCrossRef Foster-Schubert KE, McTiernan A, Frayo RS, Schwartz RS, Rajan KB, Yasui Y, et al. Human plasma ghrelin levels increase during a one-year exercise program. J Clin Endocrinol Metab. 2005;90(2):820–5.PubMedCrossRef
38.
go back to reference Kim HJ, Lee S, Kim TW, Kim HH, Jeon TY, Yoon YS, et al. Effects of exercise-induced weight loss on acylated and unacylated ghrelin in overweight children. Clin Endocrinol. 2008;68(3):416–22. Kim HJ, Lee S, Kim TW, Kim HH, Jeon TY, Yoon YS, et al. Effects of exercise-induced weight loss on acylated and unacylated ghrelin in overweight children. Clin Endocrinol. 2008;68(3):416–22.
39.
go back to reference Loria-Kohen V, Fernandez-Fernandez C, Bermejo LM, Morencos E, Romero-Moraleda B, Gomez-Candela C, et al. Effect of different exercise modalities plus a hypocaloric diet on inflammation markers in overweight patients: a randomised trial. Clin Nutr. 2013;32(4):511–8.PubMedCrossRef Loria-Kohen V, Fernandez-Fernandez C, Bermejo LM, Morencos E, Romero-Moraleda B, Gomez-Candela C, et al. Effect of different exercise modalities plus a hypocaloric diet on inflammation markers in overweight patients: a randomised trial. Clin Nutr. 2013;32(4):511–8.PubMedCrossRef
40.
go back to reference Marinho SM, Mafra D, Pelletier S, Hage V, Teuma C, Laville M, et al. In hemodialysis patients, intradialytic resistance exercise improves osteoblast function: a pilot study. J Ren Nutr. 2016;26(5):341–5.PubMedCrossRef Marinho SM, Mafra D, Pelletier S, Hage V, Teuma C, Laville M, et al. In hemodialysis patients, intradialytic resistance exercise improves osteoblast function: a pilot study. J Ren Nutr. 2016;26(5):341–5.PubMedCrossRef
41.
go back to reference de Piano A, de Mello MT, Sanches PD, da Silva PL, Campos RMS, Carnier J, et al. Long-term effects of aerobic plus resistance training on the adipokines and neuropeptides in nonalcoholic fatty liver disease obese adolescents. Eur J Gastroenterol Hepatol. 2012;24(11):1313–24.PubMed de Piano A, de Mello MT, Sanches PD, da Silva PL, Campos RMS, Carnier J, et al. Long-term effects of aerobic plus resistance training on the adipokines and neuropeptides in nonalcoholic fatty liver disease obese adolescents. Eur J Gastroenterol Hepatol. 2012;24(11):1313–24.PubMed
42.
go back to reference Volpe SL, Kobusingye H, Bailur S, Stanek E. Effect of diet and exercise on body composition, energy intake and leptin levels in overweight women and men. J Am Coll Nutr. 2008;27(2):195–208.PubMedCrossRef Volpe SL, Kobusingye H, Bailur S, Stanek E. Effect of diet and exercise on body composition, energy intake and leptin levels in overweight women and men. J Am Coll Nutr. 2008;27(2):195–208.PubMedCrossRef
43.
go back to reference Abbenhardt C, McTiernan A, Alfano CM, Wener MH, Campbell KL, Duggan C, et al. Effects of individual and combined dietary weight loss and exercise interventions in postmenopausal women on adiponectin and leptin levels. J Intern Med. 2013;274(2):163–75.PubMedPubMedCentralCrossRef Abbenhardt C, McTiernan A, Alfano CM, Wener MH, Campbell KL, Duggan C, et al. Effects of individual and combined dietary weight loss and exercise interventions in postmenopausal women on adiponectin and leptin levels. J Intern Med. 2013;274(2):163–75.PubMedPubMedCentralCrossRef
44.
go back to reference Hedges L, Olkin I. Statistical methods for meta-analysis. 6th ed. San Diego: Academic Press; 1985. p. 79–201. Hedges L, Olkin I. Statistical methods for meta-analysis. 6th ed. San Diego: Academic Press; 1985. p. 79–201.
45.
go back to reference Gutin B, Ramsey L, Barbeau P, Cannady W, Ferguson M, Litaker M, et al. Plasma leptin concentrations in obese children: changes during 4-mo periods with and without physical training. Am J Clin Nutr. 1999;69(3):388–94.PubMedCrossRef Gutin B, Ramsey L, Barbeau P, Cannady W, Ferguson M, Litaker M, et al. Plasma leptin concentrations in obese children: changes during 4-mo periods with and without physical training. Am J Clin Nutr. 1999;69(3):388–94.PubMedCrossRef
46.
go back to reference Barbeau P, Gutin B, Litaker Ramsey LT, Cannady WE, Allison J, et al. Influence of physical training on plasma leptin in obese youths. Can J Appl Physiol. 2003;28(3):382–96.PubMedCrossRef Barbeau P, Gutin B, Litaker Ramsey LT, Cannady WE, Allison J, et al. Influence of physical training on plasma leptin in obese youths. Can J Appl Physiol. 2003;28(3):382–96.PubMedCrossRef
47.
go back to reference Gutin B, Owens S. Role of exercise intervention in improving body fat distribution and risk profile in children. Am J Hum Biol. 1999;11(2):237–47.PubMedCrossRef Gutin B, Owens S. Role of exercise intervention in improving body fat distribution and risk profile in children. Am J Hum Biol. 1999;11(2):237–47.PubMedCrossRef
48.
go back to reference Rosenthal R. Meta-analytic procedures for social research. 2nd ed. Newbury Park: SAGE Publications; 1991.CrossRef Rosenthal R. Meta-analytic procedures for social research. 2nd ed. Newbury Park: SAGE Publications; 1991.CrossRef
50.
go back to reference Hox J. Multilevel analysis: techniques and applications. 2nd ed. New York: Taylor & Francis; 2010. p. 205–32.CrossRef Hox J. Multilevel analysis: techniques and applications. 2nd ed. New York: Taylor & Francis; 2010. p. 205–32.CrossRef
51.
go back to reference Singer JD, Using SAS. PROC MIXED to fit multilevel models, hierarchical models, and individual growth models. J Educ Behav Stat. 1998;23(4):323–55.CrossRef Singer JD, Using SAS. PROC MIXED to fit multilevel models, hierarchical models, and individual growth models. J Educ Behav Stat. 1998;23(4):323–55.CrossRef
53.
go back to reference Rosenberg M. The file-drawer problem revisited: a general weighted method for calculating fail-safe numbers in meta-analysis. Evolution. 2005;59(2):464–8.PubMedCrossRef Rosenberg M. The file-drawer problem revisited: a general weighted method for calculating fail-safe numbers in meta-analysis. Evolution. 2005;59(2):464–8.PubMedCrossRef
54.
go back to reference Sterne JAC, Sutton AJ, Ioannidis JPA, Terrin N, Jones DR, Lau J, et al. Recommendations for examining and interpreting funnel plot asymmetry in meta-analyses of randomised controlled trials. 2011;343:1–8. Sterne JAC, Sutton AJ, Ioannidis JPA, Terrin N, Jones DR, Lau J, et al. Recommendations for examining and interpreting funnel plot asymmetry in meta-analyses of randomised controlled trials. 2011;343:1–8.
55.
go back to reference Begg CB, Berlin JA. Publication bias: a problem in interpreting medical data. J R Stat Soc Ser A Stat Soc. 1988;151(3):419–63.CrossRef Begg CB, Berlin JA. Publication bias: a problem in interpreting medical data. J R Stat Soc Ser A Stat Soc. 1988;151(3):419–63.CrossRef
56.
go back to reference Sterne JAC, Egger M. Funnel plots for detecting bias in meta-analysis: guidelines on choice of axis. J Clin Epidemiol. 2001;54(10):1046–55.PubMedCrossRef Sterne JAC, Egger M. Funnel plots for detecting bias in meta-analysis: guidelines on choice of axis. J Clin Epidemiol. 2001;54(10):1046–55.PubMedCrossRef
57.
go back to reference Klimcakova E, Kovacikova M, Stich V, Langin D. Adipokines and dietary interventions in human obesity. Obes Rev. 2010;11(6):446–56.PubMedCrossRef Klimcakova E, Kovacikova M, Stich V, Langin D. Adipokines and dietary interventions in human obesity. Obes Rev. 2010;11(6):446–56.PubMedCrossRef
58.
go back to reference Figueroa A, Vicil F, Sanchez-Gonzalez MA, Wong A, Ormsbee MJ, Hooshmand S, et al. Effects of diet and/or low-intensity resistance exercise training on arterial stiffness, adiposity, and lean mass in obese postmenopausal women. Am J Hypertens. 2013;26(3):416–23.PubMedCrossRef Figueroa A, Vicil F, Sanchez-Gonzalez MA, Wong A, Ormsbee MJ, Hooshmand S, et al. Effects of diet and/or low-intensity resistance exercise training on arterial stiffness, adiposity, and lean mass in obese postmenopausal women. Am J Hypertens. 2013;26(3):416–23.PubMedCrossRef
59.
go back to reference Bereket A, Kiess W, Lustig RH, Muller HL, Goldstone AP, Weiss R, et al. Hypothalamic obesity in children. Obes Rev. 2012;13(9):780–98.PubMedCrossRef Bereket A, Kiess W, Lustig RH, Muller HL, Goldstone AP, Weiss R, et al. Hypothalamic obesity in children. Obes Rev. 2012;13(9):780–98.PubMedCrossRef
60.
go back to reference Filozof C, Gonzalez C. Predictors of weight gain: the biological-behavioural debate. Obes Rev. 2000;1(1):21–6.PubMedCrossRef Filozof C, Gonzalez C. Predictors of weight gain: the biological-behavioural debate. Obes Rev. 2000;1(1):21–6.PubMedCrossRef
61.
go back to reference Lau PW, Kong Z, Choi C-R, Clare C, Chan DF, Sung RY, et al. Effects of short-term resistance training on serum leptin levels in obese adolescents. J Exerc Sci Fit. 2010;8(1):54–60.CrossRef Lau PW, Kong Z, Choi C-R, Clare C, Chan DF, Sung RY, et al. Effects of short-term resistance training on serum leptin levels in obese adolescents. J Exerc Sci Fit. 2010;8(1):54–60.CrossRef
62.
go back to reference Zhao J, Tian Y, Xu J, Liu D, Wang X, Zhao B. Endurance exercise is a leptin signaling mimetic in hypothalamus of Wistar rats. Lipids Health Dis. 2011;10:225.PubMedPubMedCentralCrossRef Zhao J, Tian Y, Xu J, Liu D, Wang X, Zhao B. Endurance exercise is a leptin signaling mimetic in hypothalamus of Wistar rats. Lipids Health Dis. 2011;10:225.PubMedPubMedCentralCrossRef
63.
go back to reference Guadalupe-Grau A, Perez-Gomez J, Olmedillas H, Chavarren J, Dorado C, Santana A, et al. Strength training combined with plyometric jumps in adults: sex differences in fat-bone axis adaptations. J Appl Physiol. 2009;106(4):1100–11.PubMedCrossRef Guadalupe-Grau A, Perez-Gomez J, Olmedillas H, Chavarren J, Dorado C, Santana A, et al. Strength training combined with plyometric jumps in adults: sex differences in fat-bone axis adaptations. J Appl Physiol. 2009;106(4):1100–11.PubMedCrossRef
64.
go back to reference Miller GD, Nicklas BJ, Davis CC, Ambrosius WT, Loeser RF, Messier SP. Is serum leptin related to physical function and is it modifiable through weight loss and exercise in older adults with knee osteoarthritis? Int J Obes Relat Metab Disord. 2004;28(11):1383–90.PubMedCrossRef Miller GD, Nicklas BJ, Davis CC, Ambrosius WT, Loeser RF, Messier SP. Is serum leptin related to physical function and is it modifiable through weight loss and exercise in older adults with knee osteoarthritis? Int J Obes Relat Metab Disord. 2004;28(11):1383–90.PubMedCrossRef
65.
go back to reference Farr OM, Gavrieli A, Mantzoros CS. Leptin applications in 2015: what have we learned about leptin and obesity? Curr Opin Endocrinol Diabetes Obes. 2015;22(5):353–9.PubMedPubMedCentralCrossRef Farr OM, Gavrieli A, Mantzoros CS. Leptin applications in 2015: what have we learned about leptin and obesity? Curr Opin Endocrinol Diabetes Obes. 2015;22(5):353–9.PubMedPubMedCentralCrossRef
66.
go back to reference Paz-Filho G, Wong ML, Licinio J. Ten years of leptin replacement therapy. Obes Rev. 2011;12(5):e315–23.PubMedCrossRef Paz-Filho G, Wong ML, Licinio J. Ten years of leptin replacement therapy. Obes Rev. 2011;12(5):e315–23.PubMedCrossRef
67.
go back to reference Pan H, Guo J, Su Z. Advances in understanding the interrelations between leptin resistance and obesity. Physiol Behav. 2014;130:157–69.PubMedCrossRef Pan H, Guo J, Su Z. Advances in understanding the interrelations between leptin resistance and obesity. Physiol Behav. 2014;130:157–69.PubMedCrossRef
68.
go back to reference Brinkoetter M, Magkos F, Vamvini M, Mantzoros CS. Leptin treatment reduces body fat but does not affect lean body mass or the myostatin–follistatin–activin axis in lean hypoleptinemic women. Am J Physiol Endocrinol Metab. 2011;301(1):E99–104.PubMedPubMedCentralCrossRef Brinkoetter M, Magkos F, Vamvini M, Mantzoros CS. Leptin treatment reduces body fat but does not affect lean body mass or the myostatin–follistatin–activin axis in lean hypoleptinemic women. Am J Physiol Endocrinol Metab. 2011;301(1):E99–104.PubMedPubMedCentralCrossRef
69.
go back to reference Donnelly JE, Blair SN, Jakicic JM, Manore MM, Rankin JW, Smith BK. American College of Sports Medicine Position Stand. Appropriate physical activity intervention strategies for weight loss and prevention of weight regain for adults. Med Sci Sports Exerc. 2009;41(2):459–71.PubMedCrossRef Donnelly JE, Blair SN, Jakicic JM, Manore MM, Rankin JW, Smith BK. American College of Sports Medicine Position Stand. Appropriate physical activity intervention strategies for weight loss and prevention of weight regain for adults. Med Sci Sports Exerc. 2009;41(2):459–71.PubMedCrossRef
70.
go back to reference Swift DL, Johannsen NM, Lavie CJ, Earnest CP, Church TS. The role of exercise and physical activity in weight loss and maintenance. Prog Cardiovasc Dis. 2014;56(4):441–7.PubMedCrossRef Swift DL, Johannsen NM, Lavie CJ, Earnest CP, Church TS. The role of exercise and physical activity in weight loss and maintenance. Prog Cardiovasc Dis. 2014;56(4):441–7.PubMedCrossRef
71.
go back to reference Garber CE, Blissmer B, Deschenes MR, Franklin BA, Lamonte MJ, Lee IM, et al. American College of Sports Medicine position stand. Quantity and quality of exercise for developing and maintaining cardiorespiratory, musculoskeletal, and neuromotor fitness in apparently healthy adults: guidance for prescribing exercise. Med Sci Sports Exerc. 2011;43(7):1334–59.PubMedCrossRef Garber CE, Blissmer B, Deschenes MR, Franklin BA, Lamonte MJ, Lee IM, et al. American College of Sports Medicine position stand. Quantity and quality of exercise for developing and maintaining cardiorespiratory, musculoskeletal, and neuromotor fitness in apparently healthy adults: guidance for prescribing exercise. Med Sci Sports Exerc. 2011;43(7):1334–59.PubMedCrossRef
73.
go back to reference Stewart LA, Tierney JF. To IPD or not to IPD? Advantages and disadvantages of systematic reviews using individual patient data. Eval Health Prof. 2002;25(1):76–97.PubMedCrossRef Stewart LA, Tierney JF. To IPD or not to IPD? Advantages and disadvantages of systematic reviews using individual patient data. Eval Health Prof. 2002;25(1):76–97.PubMedCrossRef
74.
go back to reference McAuley L, Pham B, Tugwell P, Moher D. Does the inclusion of grey literature influence estimates of intervention effectiveness reported in meta-analyses? Lancet. 2000;356(9237):1228–31.PubMedCrossRef McAuley L, Pham B, Tugwell P, Moher D. Does the inclusion of grey literature influence estimates of intervention effectiveness reported in meta-analyses? Lancet. 2000;356(9237):1228–31.PubMedCrossRef
75.
go back to reference Hopewell S, McDonald S, Clarke MJ, Egger M. Grey literature in meta-analyses of randomized trials of health care interventions. Cochrane Database Syst Rev. 2007;(2):MR000010. Hopewell S, McDonald S, Clarke MJ, Egger M. Grey literature in meta-analyses of randomized trials of health care interventions. Cochrane Database Syst Rev. 2007;(2):MR000010.
76.
go back to reference Conn VS, Valentine JC, Cooper HM, Rantz MJ. Grey literature in meta-analyses. Nurs Res. 2003;52(4):256–61.PubMedCrossRef Conn VS, Valentine JC, Cooper HM, Rantz MJ. Grey literature in meta-analyses. Nurs Res. 2003;52(4):256–61.PubMedCrossRef
77.
go back to reference Lemeshow AR, Blum RE, Berlin JA, Stoto MA, Colditz GA. Searching one or two databases was insufficient for meta-analysis of observational studies. J Clin Epidemiol. 2005;58(9):867–73.PubMedCrossRef Lemeshow AR, Blum RE, Berlin JA, Stoto MA, Colditz GA. Searching one or two databases was insufficient for meta-analysis of observational studies. J Clin Epidemiol. 2005;58(9):867–73.PubMedCrossRef
78.
go back to reference Whiting P, Westwood M, Burke M, Sterne J, Glanville J. Systematic reviews of test accuracy should search a range of databases to identify primary studies. J Clin Epidemiol. 2008;61(4):357–64.PubMedCrossRef Whiting P, Westwood M, Burke M, Sterne J, Glanville J. Systematic reviews of test accuracy should search a range of databases to identify primary studies. J Clin Epidemiol. 2008;61(4):357–64.PubMedCrossRef
79.
go back to reference Papaioannou D, Sutton A, Carroll C, Booth A, Wong R. Literature searching for social science systematic reviews: consideration of a range of search techniques. Health Info Libr J. 2010;27(2):114–22.PubMedCrossRef Papaioannou D, Sutton A, Carroll C, Booth A, Wong R. Literature searching for social science systematic reviews: consideration of a range of search techniques. Health Info Libr J. 2010;27(2):114–22.PubMedCrossRef
80.
go back to reference Linder SK, Kamath GR, Pratt GF, Saraykar SS, Volk RJ. Citation searches are more sensitive than keyword searches to identify studies using specific measurement instruments. J Clin Epidemiol. 2015;68(4):412–7.PubMedCrossRef Linder SK, Kamath GR, Pratt GF, Saraykar SS, Volk RJ. Citation searches are more sensitive than keyword searches to identify studies using specific measurement instruments. J Clin Epidemiol. 2015;68(4):412–7.PubMedCrossRef
81.
go back to reference Ackel-D’Elia C, Carnier J, Bueno CR, Campos RMS, Sanches PL, Clemente APG, et al. Effects of different physical exercises on leptin concentration in obese adolescents. Int J Sports Med. 2014;35(2):164–71.PubMed Ackel-D’Elia C, Carnier J, Bueno CR, Campos RMS, Sanches PL, Clemente APG, et al. Effects of different physical exercises on leptin concentration in obese adolescents. Int J Sports Med. 2014;35(2):164–71.PubMed
82.
go back to reference Afshar R, Emany A, Saremi A, Shavandi N, Sanavi S. Effects of intradialytic aerobic training on sleep quality in hemodialysis patients. Iran J Kidney Dis. 2011;5(2):119–23.PubMed Afshar R, Emany A, Saremi A, Shavandi N, Sanavi S. Effects of intradialytic aerobic training on sleep quality in hemodialysis patients. Iran J Kidney Dis. 2011;5(2):119–23.PubMed
83.
go back to reference Ahmadizad S, Ghorbani S, Ghasemikaram M, Bahmanzadeh M. Effects of short-term nonperiodized, linear periodized and daily undulating periodized resistance training on plasma adiponectin, leptin and insulin resistance. Clin Biochem. 2014;47(6):417–22.PubMedCrossRef Ahmadizad S, Ghorbani S, Ghasemikaram M, Bahmanzadeh M. Effects of short-term nonperiodized, linear periodized and daily undulating periodized resistance training on plasma adiponectin, leptin and insulin resistance. Clin Biochem. 2014;47(6):417–22.PubMedCrossRef
84.
go back to reference Akbarpour M. The effect of aerobic training on serum adiponectin and leptin levels and inflammatory markers of coronary heart disease in obese men. Biol Sport. 2013;30(1):21–7.PubMedPubMedCentralCrossRef Akbarpour M. The effect of aerobic training on serum adiponectin and leptin levels and inflammatory markers of coronary heart disease in obese men. Biol Sport. 2013;30(1):21–7.PubMedPubMedCentralCrossRef
85.
go back to reference Almenning I, Rieber-Mohn A, Lundgren KM, Løvvik TS, Garnæs KK, Moholdt T. Effects of high intensity interval training and strength training on metabolic, cardiovascular and hormonal outcomes in women with polycystic ovary syndrome: a pilot study. PLoS One. 2015;10(9):e0138793.PubMedPubMedCentralCrossRef Almenning I, Rieber-Mohn A, Lundgren KM, Løvvik TS, Garnæs KK, Moholdt T. Effects of high intensity interval training and strength training on metabolic, cardiovascular and hormonal outcomes in women with polycystic ovary syndrome: a pilot study. PLoS One. 2015;10(9):e0138793.PubMedPubMedCentralCrossRef
86.
go back to reference Ara I, Perez-Gomez J, Vicente-Rodriguez G, Chavarren J, Dorado C, Calbert JAL, et al. Serum free testosterone, leptin and soluble leptin receptor changes in a 6-week strength-training programme. Br J Nutr. 2006;96(6):1053–9.PubMedCrossRef Ara I, Perez-Gomez J, Vicente-Rodriguez G, Chavarren J, Dorado C, Calbert JAL, et al. Serum free testosterone, leptin and soluble leptin receptor changes in a 6-week strength-training programme. Br J Nutr. 2006;96(6):1053–9.PubMedCrossRef
87.
go back to reference Arciero PJ, Baur D, Connelly S, Ormsbee MJ. Timed-daily ingestion of whey protein and exercise training reduces visceral adipose tissue mass and improves insulin resistance: the PRISE study. J Appl Physiol. 2014;117(1):1–10.PubMedCrossRef Arciero PJ, Baur D, Connelly S, Ormsbee MJ. Timed-daily ingestion of whey protein and exercise training reduces visceral adipose tissue mass and improves insulin resistance: the PRISE study. J Appl Physiol. 2014;117(1):1–10.PubMedCrossRef
88.
go back to reference Arciero PJ, Gentile CL, Pressman R, Everett M, Ormsbee MJ, Martin J, et al. Moderate protein intake improves total and regional body composition and insulin sensitivity in overweight adults. Metabolism. 2008;57(6):757–65.PubMedCrossRef Arciero PJ, Gentile CL, Pressman R, Everett M, Ormsbee MJ, Martin J, et al. Moderate protein intake improves total and regional body composition and insulin sensitivity in overweight adults. Metabolism. 2008;57(6):757–65.PubMedCrossRef
89.
go back to reference Arikawa AY, Thomas W, Schmitz KH, Kurzer MS. Sixteen weeks of exercise reduces C-reactive protein levels in young women. Med Sci Sports Exerc. 2011;43(6):1002–9.PubMedCrossRef Arikawa AY, Thomas W, Schmitz KH, Kurzer MS. Sixteen weeks of exercise reduces C-reactive protein levels in young women. Med Sci Sports Exerc. 2011;43(6):1002–9.PubMedCrossRef
90.
go back to reference Balducci S, Zanuso S, Nicolucci A, Fernando F, Cavallo S, Cardelli P, et al. Anti-inflammatory effect of exercise training in subjects with type 2 diabetes and the metabolic syndrome is dependent on exercise modalities and independent of weight loss. Nutr Metab Cardiovasc Dis. 2010;20(8):608–17.PubMedCrossRef Balducci S, Zanuso S, Nicolucci A, Fernando F, Cavallo S, Cardelli P, et al. Anti-inflammatory effect of exercise training in subjects with type 2 diabetes and the metabolic syndrome is dependent on exercise modalities and independent of weight loss. Nutr Metab Cardiovasc Dis. 2010;20(8):608–17.PubMedCrossRef
91.
go back to reference Bijeh N, Hosseini SA, Hejazi K. The effect of aerobic exercise on serum C—reactive protein and leptin levels in untrained middle-aged women. Iran J Public Health. 2012;41(9):36–41.PubMedPubMedCentral Bijeh N, Hosseini SA, Hejazi K. The effect of aerobic exercise on serum C—reactive protein and leptin levels in untrained middle-aged women. Iran J Public Health. 2012;41(9):36–41.PubMedPubMedCentral
92.
go back to reference Boudou P, Sobngwi E, Mauvais-Jarvis F, Vexiau P, Gautier JF. Absence of exercise-induced variations in adiponectin levels despite decreased abdominal adiposity and improved insulin sensitivity in type 2 diabetic men. Eur J Endocrinol. 2003;149(5):421–4.PubMedCrossRef Boudou P, Sobngwi E, Mauvais-Jarvis F, Vexiau P, Gautier JF. Absence of exercise-induced variations in adiponectin levels despite decreased abdominal adiposity and improved insulin sensitivity in type 2 diabetic men. Eur J Endocrinol. 2003;149(5):421–4.PubMedCrossRef
93.
go back to reference Christensen JO, Svendsen OL, Hassager C, Christiansen C. Leptin in overweight postmenopausal women: no relationship with metabolic syndrome X or effect of exercise in addition to diet. Int J Obes Relat Metab Disord. 1998;22(3):195–9.PubMedCrossRef Christensen JO, Svendsen OL, Hassager C, Christiansen C. Leptin in overweight postmenopausal women: no relationship with metabolic syndrome X or effect of exercise in addition to diet. Int J Obes Relat Metab Disord. 1998;22(3):195–9.PubMedCrossRef
94.
go back to reference Chyu M-C, Dagda RY, Doctolero S, Chaung E, Von Bergen V, Zhang Y, et al. Effects of martial arts exercise on body composition, serum biomarkers and quality of life in overweight/obese premenopausal women: a pilot study. Clin Med Insights Womens Health. 2013;6:55–65.PubMedPubMedCentral Chyu M-C, Dagda RY, Doctolero S, Chaung E, Von Bergen V, Zhang Y, et al. Effects of martial arts exercise on body composition, serum biomarkers and quality of life in overweight/obese premenopausal women: a pilot study. Clin Med Insights Womens Health. 2013;6:55–65.PubMedPubMedCentral
95.
go back to reference Colakoglu S, Colakoglu M, Taneli F, Cetinoz F, Turkmen M. Cumulative effects of conjugated linoleic acid and exercise on endurance development, body composition, serum leptin and insulin levels. J Sports Med Phys Fit. 2006;46(4):570–7. Colakoglu S, Colakoglu M, Taneli F, Cetinoz F, Turkmen M. Cumulative effects of conjugated linoleic acid and exercise on endurance development, body composition, serum leptin and insulin levels. J Sports Med Phys Fit. 2006;46(4):570–7.
96.
go back to reference Daryanoosh F, Mehrabani G, Shikhani H. The effect of aerobic and resistance exercises on hormonal changes in non-athlete students at Shiraz University, Southern Iran. Iran Red Crescent Med. 2010;12(2):127–32. Daryanoosh F, Mehrabani G, Shikhani H. The effect of aerobic and resistance exercises on hormonal changes in non-athlete students at Shiraz University, Southern Iran. Iran Red Crescent Med. 2010;12(2):127–32.
97.
go back to reference Dede ND, Ipekci SH, Kebapcilar L, Arslan M, Kurban S, Yildiz M, et al. Influence of exercise on leptin, adiponectin and quality of life in type 2 diabetics. Turk J Endocrinol Metab. 2015;19(1):7–13.CrossRef Dede ND, Ipekci SH, Kebapcilar L, Arslan M, Kurban S, Yildiz M, et al. Influence of exercise on leptin, adiponectin and quality of life in type 2 diabetics. Turk J Endocrinol Metab. 2015;19(1):7–13.CrossRef
98.
go back to reference Deibert P, Solleder F, König D, Vitolins MZ, H-h Dickhuth, Gollhofer A, et al. Soy protein based supplementation supports metabolic effects of resistance training in previously untrained middle aged males. Aging Male. 2011;14(4):273–9.PubMedCrossRef Deibert P, Solleder F, König D, Vitolins MZ, H-h Dickhuth, Gollhofer A, et al. Soy protein based supplementation supports metabolic effects of resistance training in previously untrained middle aged males. Aging Male. 2011;14(4):273–9.PubMedCrossRef
99.
go back to reference Dong-il SEO, Wi-Young SO, Dong Jun S. Changes in insulin resistance and adipokines in obese women following a 12-week programme of combined exercise training. S Afr J Res Sport Phys Educ Recreat. 2016;38(1):139–47. Dong-il SEO, Wi-Young SO, Dong Jun S. Changes in insulin resistance and adipokines in obese women following a 12-week programme of combined exercise training. S Afr J Res Sport Phys Educ Recreat. 2016;38(1):139–47.
100.
go back to reference Eftekhari E, Zafari A, Gholami M. Physical activity, lipid profiles and leptin. J Sports Med Phys Fit. 2016;56(4):465–9. Eftekhari E, Zafari A, Gholami M. Physical activity, lipid profiles and leptin. J Sports Med Phys Fit. 2016;56(4):465–9.
101.
go back to reference Fazelifar S, Ebrahim K, Sarkisian V. Effect of exercise training and detraining on serum leptin levels in obese young boys. Med Sport. 2013;66(3):325–37. Fazelifar S, Ebrahim K, Sarkisian V. Effect of exercise training and detraining on serum leptin levels in obese young boys. Med Sport. 2013;66(3):325–37.
102.
go back to reference Frank LL, Sorensen BE, Yasui Y, Tworoger SS, Schwartz RS, Ulrich CM, et al. Effects of exercise on metabolic risk variables in overweight postmenopausal women: a randomized clinical trial. Obes Res. 2005;13(3):615–25.PubMedCrossRef Frank LL, Sorensen BE, Yasui Y, Tworoger SS, Schwartz RS, Ulrich CM, et al. Effects of exercise on metabolic risk variables in overweight postmenopausal women: a randomized clinical trial. Obes Res. 2005;13(3):615–25.PubMedCrossRef
103.
go back to reference Friedenreich CM, Neilson HK, Woolcott CG, McTiernan A, Wang Q, Ballard-Barbash R, et al. Changes in insulin resistance indicators, IGFs, and adipokines in a year-long trial of aerobic exercise in postmenopausal women. Endocr Relat Cancer. 2011;18(3):357–69.PubMedPubMedCentralCrossRef Friedenreich CM, Neilson HK, Woolcott CG, McTiernan A, Wang Q, Ballard-Barbash R, et al. Changes in insulin resistance indicators, IGFs, and adipokines in a year-long trial of aerobic exercise in postmenopausal women. Endocr Relat Cancer. 2011;18(3):357–69.PubMedPubMedCentralCrossRef
104.
go back to reference García-Unciti M, Izquierdo M, Idoate F, Gorostiaga E, Grijalba A, Ortega-Delgado F, et al. Weight-loss diet alone or combined with progressive resistance training induces changes in association between the cardiometabolic risk profile and abdominal fat depots. Ann Nutr Metab. 2012;61(4):296–304.PubMedCrossRef García-Unciti M, Izquierdo M, Idoate F, Gorostiaga E, Grijalba A, Ortega-Delgado F, et al. Weight-loss diet alone or combined with progressive resistance training induces changes in association between the cardiometabolic risk profile and abdominal fat depots. Ann Nutr Metab. 2012;61(4):296–304.PubMedCrossRef
105.
go back to reference Giannopoulou I, Fernhall B, Carhart R, Weinstock RS, Baynard T, Figueroa A, et al. Effects of diet and/or exercise on the adipocytokine and inflammatory cytokine levels of postmenopausal women with type 2 diabetes. Metabolism. 2005;54(7):866–75.PubMedCrossRef Giannopoulou I, Fernhall B, Carhart R, Weinstock RS, Baynard T, Figueroa A, et al. Effects of diet and/or exercise on the adipocytokine and inflammatory cytokine levels of postmenopausal women with type 2 diabetes. Metabolism. 2005;54(7):866–75.PubMedCrossRef
106.
go back to reference Heyman E, Toutain C, Delamarche P, Berthon P, Briard D, Youssef H, et al. Exercise training and cardiovascular risk factors in type 1 diabetic adolescent girls. Pediatr Exerc Sci. 2007;19(4):408–19.PubMedCrossRef Heyman E, Toutain C, Delamarche P, Berthon P, Briard D, Youssef H, et al. Exercise training and cardiovascular risk factors in type 1 diabetic adolescent girls. Pediatr Exerc Sci. 2007;19(4):408–19.PubMedCrossRef
107.
go back to reference Hopkins SA, Baldi JC, Cutfield WS, McCowan L, Hofman PL. Effects of exercise training on maternal hormonal changes in pregnancy. Clin Endocrinol (Oxf). 2011;74(4):495–500.CrossRef Hopkins SA, Baldi JC, Cutfield WS, McCowan L, Hofman PL. Effects of exercise training on maternal hormonal changes in pregnancy. Clin Endocrinol (Oxf). 2011;74(4):495–500.CrossRef
108.
go back to reference Karim S, Afiq A. Does regular aerobic training affect basal leptin level (difference between male and female)? Afr J Microbiol Res. 2011;5(31):5591–5. Karim S, Afiq A. Does regular aerobic training affect basal leptin level (difference between male and female)? Afr J Microbiol Res. 2011;5(31):5591–5.
109.
go back to reference Kelly AS, Steinberger J, Olson TP. Denael. In the absence of weight loss, exercise training does not improve adipokines or oxidative stress in overweight children. Metabolism. 2007;56(7):1005–9.PubMedCrossRef Kelly AS, Steinberger J, Olson TP. Denael. In the absence of weight loss, exercise training does not improve adipokines or oxidative stress in overweight children. Metabolism. 2007;56(7):1005–9.PubMedCrossRef
110.
go back to reference Kerksick C, Thomas A, Campbell B, Taylor L, Wilborn C, Marcello B, et al. Effects of a popular exercise and weight loss program on weight loss, body composition, energy expenditure and health in obese women. Nutr Metab (Lond). 2009;6:23.PubMedPubMedCentralCrossRef Kerksick C, Thomas A, Campbell B, Taylor L, Wilborn C, Marcello B, et al. Effects of a popular exercise and weight loss program on weight loss, body composition, energy expenditure and health in obese women. Nutr Metab (Lond). 2009;6:23.PubMedPubMedCentralCrossRef
111.
go back to reference Kim YS, Nam JS, Yeo DW, Kim KR, Suh SH, Ahn CW. The effects of aerobic exercise training on serum osteocalcin, adipocytokines and insulin resistance on obese young males. Clin Endocrinol. 2015;82(5):686–94.CrossRef Kim YS, Nam JS, Yeo DW, Kim KR, Suh SH, Ahn CW. The effects of aerobic exercise training on serum osteocalcin, adipocytokines and insulin resistance on obese young males. Clin Endocrinol. 2015;82(5):686–94.CrossRef
113.
go back to reference Kosydar-Piechna M, Bilińska M, Janas J, Piotrowicz R. Influence of exercise training on leptin levels in patients with stable coronary artery disease: a pilot study. Cardiol J. 2010;17(5):477–81.PubMed Kosydar-Piechna M, Bilińska M, Janas J, Piotrowicz R. Influence of exercise training on leptin levels in patients with stable coronary artery disease: a pilot study. Cardiol J. 2010;17(5):477–81.PubMed
114.
go back to reference Ku YH, Han KA, Ahn H, Kwon H, Koo BK, Kim HC, et al. Resistance exercise did not alter intramuscular adipose tissue but reduced retinol-binding protein-4 concentration in individuals with type 2 diabetes mellitus. J Int Med Res. 2010;38(3):782–91.PubMedCrossRef Ku YH, Han KA, Ahn H, Kwon H, Koo BK, Kim HC, et al. Resistance exercise did not alter intramuscular adipose tissue but reduced retinol-binding protein-4 concentration in individuals with type 2 diabetes mellitus. J Int Med Res. 2010;38(3):782–91.PubMedCrossRef
115.
go back to reference Ligibel JA, Giobbie-Hurder A, Olenczuk D, Campbell N, Salinardi T, Winer EP, et al. Impact of a mixed strength and endurance exercise intervention on levels of adiponectin, high molecular weight adiponectin and leptin in breast cancer survivors. Cancer Causes Control. 2009;20(8):1523–8.PubMedCrossRef Ligibel JA, Giobbie-Hurder A, Olenczuk D, Campbell N, Salinardi T, Winer EP, et al. Impact of a mixed strength and endurance exercise intervention on levels of adiponectin, high molecular weight adiponectin and leptin in breast cancer survivors. Cancer Causes Control. 2009;20(8):1523–8.PubMedCrossRef
116.
go back to reference Loimaala A, Groundstroem K, Rinne M, Nenonen A, Huhtala H, Parkkari J, et al. Effect of long-term endurance and strength training on metabolic control and arterial elasticity in patients with type 2 diabetes mellitus. Am J Cardiol. 2009;103(7):972–7.PubMedCrossRef Loimaala A, Groundstroem K, Rinne M, Nenonen A, Huhtala H, Parkkari J, et al. Effect of long-term endurance and strength training on metabolic control and arterial elasticity in patients with type 2 diabetes mellitus. Am J Cardiol. 2009;103(7):972–7.PubMedCrossRef
117.
go back to reference Markofski MM, Carrillo AE, Timmerman KL, Jennings K, Coen PM, Pence BD, et al. Exercise training modifies ghrelin and adiponectin concentrations and is related to inflammation in older adults. J Gerontol A Biol Sci Med Sci. 2014;69(6):675–81.PubMedCrossRef Markofski MM, Carrillo AE, Timmerman KL, Jennings K, Coen PM, Pence BD, et al. Exercise training modifies ghrelin and adiponectin concentrations and is related to inflammation in older adults. J Gerontol A Biol Sci Med Sci. 2014;69(6):675–81.PubMedCrossRef
118.
go back to reference Mason C, Xiao L, Imayama I, Duggan CR, Campbell KL, Kong A, et al. The effects of separate and combined dietary weight loss and exercise on fasting ghrelin concentrations in overweight and obese women: a randomized controlled trial. Clin Endocrinol. 2015;82(3):369–76.CrossRef Mason C, Xiao L, Imayama I, Duggan CR, Campbell KL, Kong A, et al. The effects of separate and combined dietary weight loss and exercise on fasting ghrelin concentrations in overweight and obese women: a randomized controlled trial. Clin Endocrinol. 2015;82(3):369–76.CrossRef
119.
go back to reference McNeil J, Schwartz A, Rabasa-Lhoret R, Lavoie JM, Brochu M, Doucet E. Changes in leptin and peptide YY do not explain the greater-than-predicted decreases in resting energy expenditure after weight loss. J Clin Endocrinol Metab. 2015;100(3):E443–52.PubMedCrossRef McNeil J, Schwartz A, Rabasa-Lhoret R, Lavoie JM, Brochu M, Doucet E. Changes in leptin and peptide YY do not explain the greater-than-predicted decreases in resting energy expenditure after weight loss. J Clin Endocrinol Metab. 2015;100(3):E443–52.PubMedCrossRef
120.
go back to reference Mendham A, Duffield R, Marino F, Coutts A. Small-sided games training reduces CRP, IL-6 and leptin in sedentary, middle-aged men. Eur J Appl Physiol. 2014;114(11):2289–97.PubMedCrossRef Mendham A, Duffield R, Marino F, Coutts A. Small-sided games training reduces CRP, IL-6 and leptin in sedentary, middle-aged men. Eur J Appl Physiol. 2014;114(11):2289–97.PubMedCrossRef
121.
go back to reference Mendham AE, Duffield R, Marino F, Coutts AJ. A 12-week sports-based exercise programme for inactive Indigenous Australian men improved clinical risk factors associated with type 2 diabetes mellitus. J Sci Med Sport. 2015;18(4):438–43.PubMedCrossRef Mendham AE, Duffield R, Marino F, Coutts AJ. A 12-week sports-based exercise programme for inactive Indigenous Australian men improved clinical risk factors associated with type 2 diabetes mellitus. J Sci Med Sport. 2015;18(4):438–43.PubMedCrossRef
122.
go back to reference Okada S, Hiuge A, Makino H, Nagumo A, Takaki H, Konishi H, et al. Effect of exercise intervention on endothelial function and incidence of cardiovascular disease in patients with type 2 diabetes. J Atheroscler Thromb. 2010;17(8):828–33.PubMedCrossRef Okada S, Hiuge A, Makino H, Nagumo A, Takaki H, Konishi H, et al. Effect of exercise intervention on endothelial function and incidence of cardiovascular disease in patients with type 2 diabetes. J Atheroscler Thromb. 2010;17(8):828–33.PubMedCrossRef
123.
go back to reference Pil-Byung C, Shin-Hwan Y, Il-Gyu K, Gwang-Suk H, Jae-Hyun Y, Han-Joon L, et al. Effects of exercise program on appetite-regulating hormones, inflammatory mediators, lipid profiles, and body composition in healthy men. J Sports Med Phys Fit. 2011;51(4):654–63. Pil-Byung C, Shin-Hwan Y, Il-Gyu K, Gwang-Suk H, Jae-Hyun Y, Han-Joon L, et al. Effects of exercise program on appetite-regulating hormones, inflammatory mediators, lipid profiles, and body composition in healthy men. J Sports Med Phys Fit. 2011;51(4):654–63.
124.
go back to reference Reseland JE, Anderssen SA, Solvoll K, Hjermann I, Urdal P, Holme I, et al. Effect of long-term changes in diet and exercise on plasma leptin concentrations. Am J Clin Nutr. 2001;73(2):240–5.PubMedCrossRef Reseland JE, Anderssen SA, Solvoll K, Hjermann I, Urdal P, Holme I, et al. Effect of long-term changes in diet and exercise on plasma leptin concentrations. Am J Clin Nutr. 2001;73(2):240–5.PubMedCrossRef
125.
go back to reference Rokling-Andersen MH, Reseland JE, Veieroed MB, Anderssen SA, Jr Jacobs, Urdal P, et al. Effects of long-term exercise and diet intervention on plasma adipokine concentrations. Am J Clin Nutr. 2007;86(5):1293–301.PubMedCrossRef Rokling-Andersen MH, Reseland JE, Veieroed MB, Anderssen SA, Jr Jacobs, Urdal P, et al. Effects of long-term exercise and diet intervention on plasma adipokine concentrations. Am J Clin Nutr. 2007;86(5):1293–301.PubMedCrossRef
126.
go back to reference Rosety-Rodriguez M, Camacho A, Rosety I, Fornieles G, Rosety MA, Diaz AJ, et al. Low-grade systemic inflammation and leptin levels were improved by arm cranking exercise in adults with chronic spinal cord injury. Arch Phys Med Rehabil. 2014;95(2):297–302.PubMedCrossRef Rosety-Rodriguez M, Camacho A, Rosety I, Fornieles G, Rosety MA, Diaz AJ, et al. Low-grade systemic inflammation and leptin levels were improved by arm cranking exercise in adults with chronic spinal cord injury. Arch Phys Med Rehabil. 2014;95(2):297–302.PubMedCrossRef
127.
go back to reference Sardar MA, Hejazi SM, Abedini R. The effects of an eight-week aerobic exercise training program on serum leptin and cardiovascular risk factors among obese men with type II diabetes. Life Sci J. 2012;9(3):2518–23. Sardar MA, Hejazi SM, Abedini R. The effects of an eight-week aerobic exercise training program on serum leptin and cardiovascular risk factors among obese men with type II diabetes. Life Sci J. 2012;9(3):2518–23.
128.
go back to reference Shah K, Armamento-Villareal R, Parimi N, Chode S, Sinacore DR, Hilton TN, et al. Exercise training in obese older adults prevents increase in bone turnover and attenuates decrease in hip bone mineral density induced by weight loss despite decline in bone-active hormones. J Bone Miner Res. 2011;26(12):2851–9.PubMedPubMedCentralCrossRef Shah K, Armamento-Villareal R, Parimi N, Chode S, Sinacore DR, Hilton TN, et al. Exercise training in obese older adults prevents increase in bone turnover and attenuates decrease in hip bone mineral density induced by weight loss despite decline in bone-active hormones. J Bone Miner Res. 2011;26(12):2851–9.PubMedPubMedCentralCrossRef
129.
go back to reference Sheikholeslami-Vatani D, Siahkouhian M, Hakimi M, Ali-Mohammadi M. The effect of concurrent training order on hormonal responses and body composition in obese men. Sci Sport. 2015;30(6):335–41.CrossRef Sheikholeslami-Vatani D, Siahkouhian M, Hakimi M, Ali-Mohammadi M. The effect of concurrent training order on hormonal responses and body composition in obese men. Sci Sport. 2015;30(6):335–41.CrossRef
130.
go back to reference Straznicky NE, Lambert EA, Nestel PJ, McGrane MT, Dawood T, Schlaich MP, et al. Sympathetic neural adaptation to hypocaloric diet with or without exercise training in obese metabolic syndrome subjects. Diabetes. 2010;59(1):71–9.PubMedCrossRef Straznicky NE, Lambert EA, Nestel PJ, McGrane MT, Dawood T, Schlaich MP, et al. Sympathetic neural adaptation to hypocaloric diet with or without exercise training in obese metabolic syndrome subjects. Diabetes. 2010;59(1):71–9.PubMedCrossRef
131.
go back to reference Suksom D, Phanpheng Y, Soogarun S, Sapwarobol S. Step aerobic combined with resistance training improves cutaneous microvascular reactivity in overweight women. J Sports Med Phys Fit. 2015;55(12):1547–54. Suksom D, Phanpheng Y, Soogarun S, Sapwarobol S. Step aerobic combined with resistance training improves cutaneous microvascular reactivity in overweight women. J Sports Med Phys Fit. 2015;55(12):1547–54.
132.
go back to reference Tan S, Wang J, Cao L, Guo Z, Wang Y. Positive effect of exercise training at maximal fat oxidation intensity on body composition and lipid metabolism in overweight middle-aged women. Clin Physiol Funct Imaging. 2016;36(3):225–30.PubMedCrossRef Tan S, Wang J, Cao L, Guo Z, Wang Y. Positive effect of exercise training at maximal fat oxidation intensity on body composition and lipid metabolism in overweight middle-aged women. Clin Physiol Funct Imaging. 2016;36(3):225–30.PubMedCrossRef
133.
go back to reference Trapp EG, Chisholm DJ, Freund J, Boutcher SH. The effects of high-intensity intermittent exercise training on fat loss and fasting insulin levels of young women. Int J Obes. 2008;32(4):684–91.CrossRef Trapp EG, Chisholm DJ, Freund J, Boutcher SH. The effects of high-intensity intermittent exercise training on fat loss and fasting insulin levels of young women. Int J Obes. 2008;32(4):684–91.CrossRef
134.
go back to reference Turner JE, Markovitch D, Betts JA, Thompson D. Nonprescribed physical activity energy expenditure is maintained with structured exercise and implicates a compensatory increase in energy intake. Am J Clin Nutr. 2010;92(5):1009–16.PubMedCrossRef Turner JE, Markovitch D, Betts JA, Thompson D. Nonprescribed physical activity energy expenditure is maintained with structured exercise and implicates a compensatory increase in energy intake. Am J Clin Nutr. 2010;92(5):1009–16.PubMedCrossRef
135.
go back to reference van Gemert WA, May AM, Schuit AJ, Oosterhof BY, Peeters PH, Monninkhof EM. Effect of weight loss with or without exercise on inflammatory markers and adipokines in postmenopausal women: the SHAPE-2 trial, a randomized controlled trial. Cancer Epidemiol Biomark Prev. 2016;25(5):799–806.CrossRef van Gemert WA, May AM, Schuit AJ, Oosterhof BY, Peeters PH, Monninkhof EM. Effect of weight loss with or without exercise on inflammatory markers and adipokines in postmenopausal women: the SHAPE-2 trial, a randomized controlled trial. Cancer Epidemiol Biomark Prev. 2016;25(5):799–806.CrossRef
136.
go back to reference Venojärvi M, Wasenius N, Manderoos S, Heinonen OJ, Hernelahti M, Lindholm H, et al. Nordic walking decreased circulating chemerin and leptin concentrations in middle-aged men with impaired glucose regulation. Ann Med. 2013;45(2):162–70.PubMedCrossRef Venojärvi M, Wasenius N, Manderoos S, Heinonen OJ, Hernelahti M, Lindholm H, et al. Nordic walking decreased circulating chemerin and leptin concentrations in middle-aged men with impaired glucose regulation. Ann Med. 2013;45(2):162–70.PubMedCrossRef
137.
go back to reference Villareal DT, Shah K, Banks MR, Sinacore DR, Klein S. Effect of weight loss and exercise therapy on bone metabolism and mass in obese older adults: a one-year randomized controlled trial. J Clin Endocrinol Metab. 2008;93(6):2181–7.PubMedPubMedCentralCrossRef Villareal DT, Shah K, Banks MR, Sinacore DR, Klein S. Effect of weight loss and exercise therapy on bone metabolism and mass in obese older adults: a one-year randomized controlled trial. J Clin Endocrinol Metab. 2008;93(6):2181–7.PubMedPubMedCentralCrossRef
138.
go back to reference Winzer BM, Paratz JD, Whitehead JP, Whiteman DC, Reeves MM. The feasibility of an exercise intervention in males at risk of oesophageal adenocarcinoma: a randomized controlled trial. PLoS One. 2015;10(2):e0117922.PubMedPubMedCentralCrossRef Winzer BM, Paratz JD, Whitehead JP, Whiteman DC, Reeves MM. The feasibility of an exercise intervention in males at risk of oesophageal adenocarcinoma: a randomized controlled trial. PLoS One. 2015;10(2):e0117922.PubMedPubMedCentralCrossRef
139.
go back to reference Yang C, Chen J, Wu F, Li J, Liang P, Zhang H, et al. Effects of 60-day head-down bed rest on osteocalcin, glycolipid metabolism and their association with or without resistance training. Clin Endocrinol. 2014;81(5):671–8.CrossRef Yang C, Chen J, Wu F, Li J, Liang P, Zhang H, et al. Effects of 60-day head-down bed rest on osteocalcin, glycolipid metabolism and their association with or without resistance training. Clin Endocrinol. 2014;81(5):671–8.CrossRef
Metadata
Title
The Effect of Chronic Exercise Training on Leptin: A Systematic Review and Meta-Analysis of Randomized Controlled Trials
Authors
Michael V. Fedewa
Elizabeth D. Hathaway
Christie L. Ward-Ritacco
Tyler D. Williams
Ward C. Dobbs
Publication date
01-06-2018
Publisher
Springer International Publishing
Published in
Sports Medicine / Issue 6/2018
Print ISSN: 0112-1642
Electronic ISSN: 1179-2035
DOI
https://doi.org/10.1007/s40279-018-0897-1

Other articles of this Issue 6/2018

Sports Medicine 6/2018 Go to the issue