Int J Sports Med 2022; 43(09): 743-767
DOI: 10.1055/a-1720-0369
Review

Type and Intensity as Key Variable of Exercise in Metainflammation Diseases: A Review

Caique Figueiredo
1   Exercise and Immunometabolism Research Group, Postgraduation Program in Movement Sciences, Department of Physical Education, Universidade Estadual Paulista (UNESP), Presidente Prudente, São Paulo, Brazil
,
Camila S. Padilha
1   Exercise and Immunometabolism Research Group, Postgraduation Program in Movement Sciences, Department of Physical Education, Universidade Estadual Paulista (UNESP), Presidente Prudente, São Paulo, Brazil
,
Gilson P. Dorneles
2   Laboratory of Cellular and Molecular Immunology, Department of Health Basic Sciences, Federal University of Health Sciences of Porto Alegre, Porto Alegre, Brazil
,
Alessandra Peres
2   Laboratory of Cellular and Molecular Immunology, Department of Health Basic Sciences, Federal University of Health Sciences of Porto Alegre, Porto Alegre, Brazil
,
Karsten Krüger
3   Institute of Sports Science, Department of Exercise Physiology and Sports Therapy, University of Giessen, Giessen, Germany
,
José Cesar Rosa-Neto
4   Department of Cell and Developmental Biology, University of São Paulo, São Paulo, São Paulo, Brazil
,
Fabio S. Lira
1   Exercise and Immunometabolism Research Group, Postgraduation Program in Movement Sciences, Department of Physical Education, Universidade Estadual Paulista (UNESP), Presidente Prudente, São Paulo, Brazil
› Author Affiliations
Funding This study was supported by São Paulo Research Foundation (FAPESP) and Coordenação de Aperfeiçoamento Pessoal de Nível Superior – Brazil (CAPES) #001. CSP is granted with Post Doctorate scholarship from the FAPESP (Process 2018/23402–0), CF is granted with Doctorate scholarship from the FAPESP (Process 2019/26378– 6), FSL is granted with research grants from the FAPESP (Process 2018/19678–0).

Abstract

Monocyte and lymphocyte subpopulations exhibit functions that vary between the anti- and pro-inflammatory spectrum, such as classic CD16- and non-classical CD16+monocytes, as well as T helper 2 lymphocytes (Th2), the Th1/Th17 lymphocytes ratio, and T regulatory lymphocytes (Treg). Metabolic disease-associated inflammation is accompanied by an imbalance in monocyte and lymphocyte phenotypes and functionality, as well as a stronger proportion of inflammatory subpopulations. These changes appear to be important for the development and progression of diseases like diabetes and cardiovascular disease. On the other hand, the regular practice of physical exercise is an important tool to restore the functionality of monocytes and lymphocytes, and to balance the subtypes ratio. However, key variables regarding exercise prescription, such as the type of exercise, intensity, and volume differentially impact on the acute and chronic immune response in individuals diagnosed with meta-inflammation diseases. Here, we discuss the impact of different physical exercise protocols, acutely and chronically, on monocytes and lymphocytes of individuals with metabolic disease-associated inflammation. In this review, we focus on the best effects of different exercise protocols to dose the “exercise pill” in different inflammatory status.



Publication History

Received: 01 December 2021

Accepted: 09 December 2021

Accepted Manuscript online:
13 December 2021

Article published online:
18 February 2022

© 2022. Thieme. All rights reserved.

Georg Thieme Verlag
Rüdigerstraße 14, 70469 Stuttgart, Germany

 
  • References

  • 1 Alberti KG, Eckel RH, Grundy SM. et al. Harmonizing the metabolic syndrome: a joint interim statement of the International Diabetes Federation Task Force on Epidemiology and Prevention; National Heart, Lung, and Blood Institute; American Heart Association; World Heart Federation; International Atherosclerosis Society; and International Association for the Study of Obesity. Circulation 2009; 120: 1640-1645
  • 2 Lee IM, Shiroma EJ, Lobelo F. et al. Effect of physical inactivity on major non-communicable diseases worldwide: an analysis of burden of disease and life expectancy. Lancet 2012; 380: 219-229
  • 3 Hallal PC, Andersen LB, Bull FC. et al. Global physical activity levels: surveillance progress, pitfalls, and prospects. Lancet 2012; 380: 247-257
  • 4 Janochova K, Haluzik M, Buzga M. Visceral fat and insulin resistance - what we know?. Biomed Pap Med Fac Univ Palacky Olomouc Czech Repub 2018; 163: 19-27
  • 5 Barter P. Metabolic abnormalities: high-density lipoproteins. Endocrinol Metab Clin North Am 2004; 33: 393-403
  • 6 Romero-Gómez M, Zelber-Sagi S, Trenell M. Treatment of NAFLD with diet, physical activity and exercise. J Hepatol 2017; 67: 829-846
  • 7 Tanaka S, Nemoto Y, Takei Y. et al. High-fat diet-derived free fatty acids impair the intestinal immune system and increase sensitivity to intestinal epithelial damage. Biochem Biophys Res Commun 2020; 522: 971-977
  • 8 Von Ah Morano AE, Dorneles GP, Peres A. et al. The role of glucose homeostasis on immune function in response to exercise: The impact of low or higher energetic conditions. J Cell Physiol 2020; 235: 3169-3188
  • 9 Bernardi S, Marcuzzi A, Piscianz E. et al. The complex interplay between lipids, immune system and interleukins in cardio-metabolic diseases. Int J Mol Sci 2018; 19: 4058
  • 10 Zatterale F, Longo M, Naderi J. et al. Chronic adipose tissue inflammation linking obesity to insulin resistance and type 2 diabetes. Front Physiol 2020; 29: 10 1607
  • 11 Thomas TP, Grisanti LA. The dynamic interplay between cardiac inflammation and fibrosis. Front Physiol 2020; 11: 529075
  • 12 Goossens GH. The metabolic phenotype in obesity: fat mass, body fat distribution, and adipose tissue function. Obes Facts 2017; 10: 207-215
  • 13 Markofski MM, Flynn MG, Carrillo AE. et al. Resistance exercise training-induced decrease in circulating inflammatory CD14+CD16+monocyte percentage without weight loss in older adults. Eur J Appl Physiol 2014; 114: 1737-1748
  • 14 Durrer C, Francois M, Neudorf H. et al. Acute high-intensity interval exercise reduces human monocyte Toll-like receptor 2 expression in type 2 diabetes. Am J Physiol Regul Integr Comp Physiol 2017; 312: R529-R538
  • 15 Heymann F, Tacke F. Immunology in the liver--from homeostasis to disease. Nat Rev Gastroenterol Hepatol 2016; 13: 88-110
  • 16 DeFuria J, Belkina AC, Jagannathan-Bogdan M. et al. B cells promote inflammation in obesity and type 2 diabetes through regulation of T-cell function and an inflammatory cytokine profile. Proc Natl Acad Sci U S A 2013; 110: 5133-5138
  • 17 Duffaut C, Zakaroff-Girard A, Bourlier V. et al. Interplay between human adipocytes and T lymphocytes in obesity: CCL20 as an adipochemokine and T lymphocytes as lipogenic modulators. Arterioscler Thromb Vasc Biol 2009; 29: 1608-1614
  • 18 Jagannathan-Bogdan M, McDonnell ME, Shin H. et al. Elevated proinflammatory cytokine production by a skewed T cell compartment requires monocytes and promotes inflammation in type 2 diabetes. J Immunol 2011; 186: 1162-1172
  • 19 Breuer DA, Pacheco MC, Washington MK. et al. CD8+T cells regulate liver injury in obesity-related nonalcoholic fatty liver disease. Am J Physiol Gastrointest Liver Physiol 2020; 318: G211-G224
  • 20 Silveira LS, Biondo LA, de Souza Teixeira AA. et al. Macrophage immunophenotype but not anti-inflammatory profile is modulated by peroxisome proliferator-activated receptor gamma (PPARγ) in exercised obese mice. Exerc Immunol Rev 2020; 26: 10-22
  • 21 Dorneles GP, da Silva IM, Peres A. et al. Physical fitness modulates the expression of CD39 and CD73 on CD4+CD25- and CD4+CD25+T cells following high intensity interval exercise. J Cell Biochem 2019; 120 10726-10736
  • 22 de Matos MA, Garcia BCC, Vieira DV. et al. High-intensity interval training reduces monocyte activation in obese adults. Brain Behav Immun 2019; 80: 818-824
  • 23 Ortega E. The “bioregulatory effect of exercise” on the innate/inflammatory responses. J Physiol Biochem 2016; 72: 361-369
  • 24 Dorneles GP, da Silva I, Boeira MC. et al. Cardiorespiratory fitness modulates the proportions of monocytes and T helper subsets in lean and obese men. Scand J Med Sci Sports 2019; 29: 1755-1765
  • 25 Chaput JP, Willumsen J, Bull F. et al. 2020 WHO guidelines on physical activity and sedentary behaviour for children and adolescents aged 5-17 years: summary of the evidence. Int J Behav Nutr Phys Act 2020; 17: 141
  • 26 Bull FC, Al-Ansari SS, Biddle S. et al. World Health Organization 2020 guidelines on physical activity and sedentary behaviour. Br J Sports Med 2020; 54: 1451-1462
  • 27 Antunes BM, Rosa-Neto JC, Batatinha HAP. et al. Physical fitness status modulates the inflammatory proteins in peripheral blood and circulating monocytes: role of PPAR-gamma. Sci Rep 2020; 10: 14094
  • 28 Antunes BM, Rossi FE, Oyama LM. et al. Exercise intensity and physical fitness modulate lipoproteins profile during acute aerobic exercise session. Sci Rep 2020; 10: 4160
  • 29 Cabral-Santos C, Gerosa-Neto J, Inoue DS. et al. Similar Anti-Inflammatory Acute Responses from Moderate-Intensity Continuous and High-Intensity Intermittent Exercise. J Sports Sci Med 2015; 14: 849-856
  • 30 Gerosa-Neto J, Monteiro PA, Inoue DS. et al. High- and moderate-intensity training modify LPS-induced ex-vivo interleukin-10 production in obese men in response to an acute exercise bout. Cytokine 2020; 136: 155249
  • 31 Figueiredo C, Antunes BM, Giacon TR. et al. Influence of Acute and Chronic High-Intensity Intermittent Aerobic Plus Strength Exercise on BDNF, Lipid and Autonomic Parameters. J Sports Sci Med 2019; 18: 359-368
  • 32 Lira FS, Antunes BM, Figueiredo C. et al. Impact of 5-week high-intensity interval training on indices of cardio metabolic health in men. Diabetes Metab Syndr 2019; 13: 1359-1364
  • 33 Slusher AL, Shibata Y, Whitehurst M. et al. Exercise reduced pentraxin 3 levels produced by endotoxin-stimulated human peripheral blood mononuclear cells in obese individuals. Exp Biol Med (Maywood) 2017; 242: 1279-1286
  • 34 Nickel T, Hanssen H, Emslander I. et al. Immunomodulatory effects of aerobic training in obesity. Mediators Inflamm 2011; 2011: 308965
  • 35 Dorneles GP, da Silva IM, Santos MA. et al. Immunoregulation induced by autologous serum collected after acute exercise in obese men: a randomized cross-over trial. Sci Rep 2020; 10: 21735
  • 36 Dorneles GP, da Silva IRV, Korb A. et al. High intensity interval exercise enhances the global HDAC activity in PBMC and anti-inflammatory cytokines of overweight-obese subjects. Obes Med 2016; 2: 25-30
  • 37 Dorneles GP, Boeira MCR, Schipper LL. et al. Acute strenuous exercise induces an imbalance on histone h4 acetylation/histone deacetylase 2 and increases the proinflammatory profile of pbmc of obese individuals. Oxid Med Cell Longev 2017; 2017: 1530230
  • 38 Huang CJ, Rodriguez AL, Visavadiya NP. et al. An exploratory investigation of apoptotic and autophagic responses in peripheral blood mononuclear cells following maximal aerobic exercise in obese individuals. Arch Physiol Biochem 2019. Online ahead of print. DOI: 10.1080/13813455.2019.1671875.
  • 39 Peres A, Da Silva IM, Santos M. et al. DNA damage in mononuclear cells following maximal exercise in sedentary and physically active lean and obese men. Eur J Sport Sci 2021; 21: 1073-1082
  • 40 Gibala MJ. Interval Training for Cardiometabolic Health: Why Such A HIIT?. Curr Sports Med Rep 2018; 17: 148-150
  • 41 Magid-Bernstein JR, Rohowsky-Kochan CM. Human CD39+Treg cells express Th17-associated surface markers and suppress IL-17 via a Stat3-dependent mechanism. J Interferon Cytokine Res 2017; 37: 153-164
  • 42 Mandapathil M, Hilldorfer B, Szczepanski MJ. et al. Generation and accumulation of immunosuppressive adenosine by human CD4+CD25highFOXP3+regulatory T cells. J Biol Chem 2010; 285: 7176-7186
  • 43 Romio M, Reinbeck B, Bongardt S. et al. Extracellular purine metabolism and signaling of CD73-derived adenosine in murine Treg and Teff cells. Am J Physiol Cell Physiol 2011; 301: C530-C539
  • 44 Gustafson MP, DiCostanzo AC, Wheatley CM. et al. A systems biology approach to investigating the influence of exercise and fitness on the composition of leukocytes in peripheral blood. J Immunother Cancer 2017; 5: 30
  • 45 Phillips MD, Flynn MG, McFarlin BK. et al. Resistive exercise blunts LPS-stimulated TNF-alpha and Il-1 beta. Int J Sports Med 2008; 29: 102-109
  • 46 Fortunato AK, Pontes WM, De Souza DMS. et al. Strength training session induces important changes on physiological, immunological, and inflammatory biomarkers. J Immunol Res 2018; 2018: 9675216
  • 47 Jajtner AR, Townsend JR, Beyer KS. et al. Resistance exercise selectively mobilizes monocyte subsets: role of polyphenols. med sci sports exerc 2018; 50: 2231-2241
  • 48 Wells AJ, Hoffman JR, Jajtner AR. et al. Monocyte recruitment after high-intensity and high-volume resistance exercise. Med Sci Sports Exerc 2016; 48: 1169-1178
  • 49 Schlagheck ML, Walzik D, Joisten N. et al. Cellular immune response to acute exercise: Comparison of endurance and resistance exercise. Eur J Haematol 2020; 105: 75-84
  • 50 Schenk A, Joisten N, Walzik D. et al. Acute exercise impacts AhR and PD-1 levels of CD8+T-cells-Exploratory results from a randomized cross-over trial comparing endurance versus resistance exercise. Eur J Appl Physiol 2021; 121: 637-644
  • 51 Bay ML, Heywood S, Wedell-Neergaard AS. et al. Human immune cell mobilization during exercise: effect of IL-6 receptor blockade. Exp Physiol 2020; 105: 2086-2098
  • 52 Graff RM, Kunz HE, Agha NH. et al. β2-Adrenergic receptor signaling mediates the preferential mobilization of differentiated subsets of CD8+T-cells, NK-cells and non-classical monocytes in response to acute exercise in humans. Brain Behav Immun 2018; 74: 143-153
  • 53 Gálvez I, Martín-Cordero L, Hinchado MD. et al. β2 Adrenergic regulation of the phagocytic and microbicide capacity of circulating monocytes: influence of obesity and exercise. Nutrients 2020; 12: 1438
  • 54 Gálvez I, Martín-Cordero L, Hinchado MD. et al. Obesity affects β2 adrenergic regulation of the inflammatory profile and phenotype of circulating monocytes from exercised animals. Nutrients 2019; 11: 2630
  • 55 Barnes MA, Carson MJ, Nair MG. Non-traditional cytokines: How catecholamines and adipokines influence macrophages in immunity, metabolism and the central nervous system. Cytokine 2015; 72: 210-219
  • 56 Macpherson RE, Huber JS, Frendo-Cumbo S. et al. Adipose tissue insulin action and IL-6 signaling after exercise in obese mice. Med Sci Sports Exerc 2015; 47: 2034-2042
  • 57 Ludzki AC, Krueger EM, Baldwin TC. et al. Acute aerobic exercise remodels the adipose tissue progenitor cell phenotype in obese adults. Front Physiol 2020; 11: 903
  • 58 McCormick JJ, King KE, Dokladny K. et al. Effect of acute aerobic exercise and rapamycin treatment on autophagy in peripheral blood mononuclear cells of adults with prediabetes. Can J Diabetes 2019; 43: 457-463
  • 59 de Matos MA, Duarte TC, Ottone Vde O. et al. The effect of insulin resistance and exercise on the percentage of CD16(+) monocyte subset in obese individuals. Cell Biochem Funct 2016; 34: 209-216
  • 60 Babendreyer A, Molls L, Dreymueller D. et al. Shear stress counteracts endothelial CX3CL1 induction and monocytic cell adhesion. mediators inflamm 2017; 2017: 1515389
  • 61 Koivisto VA, Felig P. Alterations in insulin absorption and in blood glucose control associated with varying insulin injection sites in diabetic patients. Ann Intern Med 1980; 92: 59-61
  • 62 Barry JC, Shakibakho S, Durrer C. et al. Hyporesponsiveness to the anti-inflammatory action of interleukin-10 in type 2 diabetes. Sci Rep 2016; 6: 21244
  • 63 Alizadeh S, Mazloom H, Sadeghi A. et al. Evidence for the link between defective autophagy and inflammation in peripheral blood mononuclear cells of type 2 diabetic patients. J Physiol Biochem 2018; 74: 369-379
  • 64 Wonner R, Wallner S, Orsó E. et al. Effects of acute exercise on monocyte subpopulations in metabolic syndrome patients. Cytometry B Clin Cytom 2018; 94: 596-605
  • 65 Wang M, Chen F, Wang J. et al. Th17 and Treg lymphocytes in obesity and Type 2 diabetic patients. Clin Immunol 2018; 197: 77-85
  • 66 Kelly KR, Haus JM, Solomon TP. et al. A low-glycemic index diet and exercise intervention reduces TNF(alpha) in isolated mononuclear cells of older, obese adults. J Nutr 2011; 141: 1089-1094
  • 67 Farzanegi P, Dana A, Ebrahimpoor Z. et al. Mechanisms of beneficial effects of exercise training on non-alcoholic fatty liver disease (NAFLD): Roles of oxidative stress and inflammation. Eur J Sport Sci 2019; 19: 994-1003
  • 68 Barry JC, Simtchouk S, Durrer C. et al. Short-term exercise training alters leukocyte chemokine receptors in obese adults. Med Sci Sports Exerc 2017; 49: 1631-1640
  • 69 Barry JC, Simtchouk S, Durrer C. et al. Short-term exercise training reduces anti-inflammatory action of interleukin-10 in adults with obesity. Cytokine 2018; 111: 460-469
  • 70 Bartlett DB, Shepherd SO, Wilson OJ. et al. Neutrophil and monocyte bactericidal responses to 10 weeks of low-volume high-intensity interval or moderate-intensity continuous training in sedentary adults. Oxid Med Cell Longev 2017; 2017: 8148742
  • 71 Colato A, Abreu F, Medeiros M. et al. Effects of concurrent training on inflammatory markers and expression of CD4, CD8, and HLA-DR in overweight and obese adults. J Exerc Sci Fit 2014; 12: 55-61
  • 72 Streese L, Khan AW, Deiseroth A. et al. High-intensity interval training modulates retinal microvascular phenotype and DNA methylation of p66Shc gene: a randomized controlled trial (EXAMIN AGE). Eur Heart J 2020; 41: 1514-1519
  • 73 LaPerriere A, Antoni MH, Ironson G. et al. Effects of aerobic exercise training on lymphocyte subpopulations. Int J Sports Med 1994; 3: 127-130
  • 74 Antunes BM, Campos EZ, Dos Santos RVT. et al. Anti-inflammatory response to acute exercise is related with intensity and physical fitness. J Cell Biochem 2019; 120: 5333-5342
  • 75 Soltani N, Marandi SM, Kazemi M. et al. Combined all-extremity high-intensity interval training regulates immunometabolic responses through toll-like receptor 4 adaptors and A20 downregulation in obese young females. Obes Facts 2020; 13: 415-431
  • 76 Baturcam E, Abubaker J, Tiss A. et al. Physical exercise reduces the expression of RANTES and its CCR5 receptor in the adipose tissue of obese humans. Mediators Inflamm 2014; 2014: 627150
  • 77 Wadley AJ, Roberts MJ, Creighton J. et al. Higher levels of physical activity are associated with reduced tethering and migration of pro-inflammatory monocytes in males with central obesity. Exerc Immunol Rev 2021; 27: 54-66
  • 78 Woods JA, Ceddia MA, Wolters BW. et al. Effects of 6 months of moderate aerobic exercise training on immune function in the elderly. Mech Ageing Dev 1999; 109: 1-19
  • 79 Colato A, Fraga L, Dorneles G. et al. Impact of aerobic water running training on peripheral immune-endocrine markers of overweight-obese women. Sci Sports 2017; 32: 46-53
  • 80 Nickel T, Emslander I, Sisic Z. et al. Modulation of dendritic cells and toll-like receptors by marathon running. Eur J Appl Physiol 2012; 112: 1699-1708
  • 81 van der Zalm IJB, van der Valk ES, Wester VL. et al. Obesity-associated T-cell and macrophage activation improve partly after a lifestyle intervention. Int J Obes (Lond) 2020; 44: 1838-1850
  • 82 Habermann N, Makar KW, Abbenhardt C. et al. No effect of caloric restriction or exercise on radiation repair capacity. Med Sci Sports Exerc 2015; 47: 896-904
  • 83 Farinha JB, Steckling FM, Stefanello ST. et al. Response of oxidative stress and inflammatory biomarkers to a 12-week aerobic exercise training in women with metabolic syndrome. Sports Med Open 2015; 1: 19
  • 84 Westcott WL. Resistance training is medicine: effects of strength training on health. Curr Sports Med Rep 2012; 11: 209-216
  • 85 Garber CE, Blissmer B, Deschenes MR. 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: 1334-1359
  • 86 da Silva IM, Santos MA, Galvão SL. et al. Blood flow restriction impairs the inflammatory adaptations of strength training in overweight men: a clinical randomized trial. Appl Physiol Nutr Metab 2020; 45: 659-666
  • 87 Bartholomeu-Neto J, Brito CJ, Nóbrega OT. et al. Adaptation to resistance training is associated with higher phagocytic (but not oxidative) activity in neutrophils of older women. J Immunol Res 2015; 2015: 724982
  • 88 Schaun MI, Dipp T, Rossato Jda S. et al. The effects of periodized concurrent and aerobic training on oxidative stress parameters, endothelial function and immune response in sedentary male individuals of middle age. Cell Biochem Funct 2011; 29: 534-542
  • 89 Quiroga R, Nistal E, Estébanez B. et al. Exercise training modulates the gut microbiota profile and impairs inflammatory signaling pathways in obese children. Exp Mol Med 2020; 52: 1048-1061
  • 90 Soltani N, Esmaeil N, Marandi SM. et al. Assessment of the effect of short-term combined high-intensity interval training on TLR4, NF-κB and IRF3 expression in young overweight and obese girls. Public Health Genomics 2020; 23: 26-36
  • 91 Campbell PT, Wener MH, Sorensen B. et al. Effect of exercise on in vitro immune function: a 12-month randomized, controlled trial among postmenopausal women. J Appl Physiol (1985) 2008; 104: 1648-1655
  • 92 Ibrahim NS, Ooi FK, Chen CK. et al. Effects of probiotics supplementation and circuit training on immune responses among sedentary young males. J Sports Med Phys Fitness 2018; 58: 1102-1109
  • 93 Timmerman KL, Flynn MG, Coen PM. et al. Exercise training-induced lowering of inflammatory (CD14+CD16+) monocytes: a role in the anti-inflammatory influence of exercise?. J Leukoc Biol 2008; 84: 1271-1278
  • 94 Coen PM, Flynn MG, Markofski MM. et al. Adding exercise to rosuvastatin treatment: influence on C-reactive protein, monocyte toll-like receptor 4 expression, and inflammatory monocyte (CD14+CD16+) population. Metabolism 2010; 59: 1775-1783
  • 95 Balducci S, Zanuso S, Nicolucci A. 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: 608-617
  • 96 Robinson E, Durrer C, Simtchouk S. et al. Short-term high-intensity interval and moderate-intensity continuous training reduce leukocyte TLR4 in inactive adults at elevated risk of type 2 diabetes. J Appl Physiol (1985) 2015; 119: 508-516
  • 97 Reyna SM, Tantiwong P, Cersosimo E. et al. Short-term exercise training improves insulin sensitivity but does not inhibit inflammatory pathways in immune cells from insulin-resistant subjects. J Diabetes Res 2013; 2013: 107805
  • 98 Wenning P, Kreutz T, Schmidt A. et al. Endurance exercise alters cellular immune status and resistin concentrations in men suffering from non-insulin-dependent type 2 diabetes. Exp Clin Endocrinol Diabetes 2013; 121: 475-482
  • 99 Faude O, Kindermann W, Meyer T. Lactate threshold concepts: how valid are they?. Sports Med 2009; 39: 469-490
  • 100 Philippe M, Gatterer H, Burtscher M. et al. Concentric and eccentric endurance exercise reverse hallmarks of T-cell senescence in pre-diabetic subjects. Front Physiol 2019; 10: 684
  • 101 Liu Y, Liu SX, Cai Y. et al. Effects of combined aerobic and resistance training on the glycolipid metabolism and inflammation levels in type 2 diabetes mellitus. J Phys Ther Sci 2015; 27: 2365-2371
  • 102 Annibalini G, Lucertini F, Agostini D. et al. Concurrent aerobic and resistance training has anti-inflammatory effects and increases both plasma and leukocyte levels of IGF-1 in late middle-aged type 2 diabetic patients. Oxid Med Cell Longev 2017; 2017: 3937842
  • 103 Martins CC, Bagatini MD, Cardoso AM. et al. Exercise training positively modulates the ectonucleotidase enzymes in lymphocytes of metabolic syndrome patients. Int J Sports Med 2016; 37: 930-936
  • 104 Mastelic-Gavillet B, Navarro Rodrigo B, Décombaz L. et al. Adenosine mediates functional and metabolic suppression of peripheral and tumor-infiltrating CD8+T cells. J Immunother Cancer 2019; 7: 257
  • 105 Sakowicz-Burkiewicz M, Pawelczyk T. Recent advances in understanding the relationship between adenosine metabolism and the function of T and B lymphocytes in diabetes. J Physiol Pharmacol 2011; 62: 505-512
  • 106 Steckling FM, Farinha JB, Figueiredo FDC. et al. High-intensity interval training improves inflammatory and adipokine profiles in postmenopausal women with metabolic syndrome. Arch Physiol Biochem 2019; 125: 85-91
  • 107 Dietz WH, Baur LA, Hall K. et al. Management of obesity: improvement of health-care training and systems for prevention and care. Lancet 2015; 385: 2521-2533
  • 108 Grundy SM. What is the contribution of obesity to the metabolic syndrome?. Endocrinol Metab Clin North Am 2004; 33: 267-282
  • 109 Breit SN, Brown DA, Tsai VW. The GDF15-GFRAL pathway in health and metabolic disease: friend or foe?. Annu Rev Physiol 2021; 83: 127-151
  • 110 Reaven G. The metabolic syndrome or the insulin resistance syndrome? Different names, different concepts, and different goals. Endocrinol Metab Clin North Am 2004; 33: 283-303
  • 111 Wisniewski PJ, Dowden RA, Campbell SC. Role of dietary lipids in modulating inflammation through the gut microbiota. Nutrients 2019; 11: 117
  • 112 Moreira AP, Texeira TF, Ferreira AB. Influence of a high-fat diet on gut microbiota, intestinal permeability and metabolic endotoxaemia. Br J Nutr 2012; 108: 801-809
  • 113 Reilly SM, Saltiel AR. Adapting to obesity with adipose tissue inflammation. Nat Rev Endocrinol 2017; 13: 633-643
  • 114 Hansen D, Niebauer J, Cornelissen V. et al. Exercise prescription in patients with different combinations of cardiovascular disease risk factors: a consensus statement from the EXPERT working group. Sports Med 2018; 48: 1781-1797
  • 115 Donnelly JE, Blair SN, Jakicic JM. et al. American college of sports medicine. 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: 459-471
  • 116 Chastin SF, Egerton T, Leask C. et al. Meta-analysis of the relationship between breaks in sedentary behavior and cardiometabolic health. Obesity (Silver Spring) 2015; 23: 1800-1810
  • 117 Verboven K, Hansen D. Critical reappraisal of the role and importance of exercise intervention in the treatment of obesity in adults. Sports Med 2021; 51: 379-389
  • 118 Cabral-Santos C, de Lima Junior EA, Fernandes IMDC. et al. Interleukin-10 responses from acute exercise in healthy subjects: A systematic review. J Cell Physiol 2019; 234: 9956-9965
  • 119 Silveira LS, Antunes BM, Minari AL. et al. Macrophage polarization: implications on metabolic diseases and the role of exercise. Crit Rev Eukaryot Gene Expr 2016; 26: 115-132
  • 120 Padilha CS, Figueiredo C, Minuzzi LG. et al. Immunometabolic responses according to physical fitness status and lifelong exercise during aging: New roads for exercise immunology. Ageing Res Rev 2021; 68: 101341
  • 121 Gillen JB, Gibala MJ. Is high-intensity interval training a time-efficient exercise strategy to improve health and fitness?. Appl Physiol Nutr Metab 2014; 39: 409-412
  • 122 Sultana RN, Sabag A, Keating SE. et al. The effect of low-volume high-intensity interval training on body composition and cardiorespiratory fitness: a systematic review and meta-analysis. Sports Med 2019; 49: 1687-1721
  • 123 Elenkov IJ, Wilder RL, Chrousos GP. et al. The sympathetic nerve – an integrative interface between two supersystems: the brain and the immune system. Pharmacol Rev 2000; 52: 595-638
  • 124 Segerstrom SC, Miller GE. Psychological stress and the human immune system: a meta-analytic study of 30 years of inquiry. Psychol Bull 2004; 130: 601-630
  • 125 Sakamoto K, Goodyear LJ. Invited review: intracellular signaling in contracting skeletal muscle. J Appl Physiol (1985) 2002; 93: 369-383
  • 126 Lujan HL, DiCarlo SE. Physical activity, by enhancing parasympathetic tone and activating the cholinergic anti-inflammatory pathway, is a therapeutic strategy to restrain chronic inflammation and prevent many chronic diseases. Med Hypotheses 2013; 80: 548-552
  • 127 Borovikova LV, Ivanova S, Zhang M. et al. Vagus nerve stimulation attenuates the systemic inflammatory response to endotoxin. Nature 2000; 405: 458-462
  • 128 Gallowitsch-Puerta M, Pavlov VA. Neuro-immune interactions via the cholinergic anti-inflammatory pathway. Life Sci 2007; 80: 2325-2329