Abstract
Purpose
Suppressing inflammaging at an early stage in life via exercise might prevent chronic diseases later in life. The aim was to investigate the influence of resistance training at different external loads on inflammatory markers in healthy young adults.
Methods
Serum was collected for basal levels of cytokines (IL-1beta, IL-6, IL-8, sTNFR1, IL-1RA, IL-10 and GM-CSF) before and after 9 weeks exercise from 36 young (22 ± 2 years) healthy subjects who were randomized to three times weekly supervised resistance training at either HImax (n = 12, 1 × 10–12 repetitions at 80% 1RM), LO (n = 12, 1 × 10–12 repetitions at 40% 1RM), or LOmax (n = 12, 1 × 10–12 repetitions at 40% 1RM preceded by 60 repetitions at 20–25% 1RM) respectively.
Results
Overall, IL-8 increased (p < 0.001) and IL-6 decreased (p = 0.001) after training, but no significant time*group interaction was found (respectively, p = 0.283 and p = 0.058 for IL-8 and IL-6). When analyzed separately, IL-8 increased significantly in HImax (p = 0.022) and LOmax (p = 0.024); and IL-6 decreased significantly in LOmax (p = 0.009) and LO (p = 0.013). No significant overall time effect was observed for sTNFR1 and IL-1RA; however, in HImax sTNFR1 (p = 0.031) and IL-1RA (p = 0.014) increased significantly, but remained unchanged in LOmax and LO. IL-1beta, IL-10 and GM-CSF levels remained undetectable in most participants.
Conclusions
Nine weeks of resistance training—irrespective of the external load—have beneficial effects on circulating IL-8 and IL-6. In addition, training at high external load increases the anti-inflammatory cytokines sTNFR1 and IL-1RA. The results of this study show that resistance training has anti-inflammatory effects in healthy young persons and that the response of the different inflammatory mediators depends on the magnitude of the external load.
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References
Abellan van Kan G (2009) Epidemiology and consequences of sarcopenia. The journal of nutrition health aging 13(8):708–712
Aderka D, Engelmann H, Maor Y, Brakebusch C, Wallach D (1992) Stabilization of the bioactivity of tumor necrosis factor by its soluble receptors. J Exp Med 175(2):323–329
Azizbeigi K, Azarbayjani MA, Atashak S, Stannard SR (2015) Effect of moderate and high resistance training intensity on indices of inflammatory and oxidative stress. Res Sports Med 23(1):73–87
Bautmans I, Njemini R, Vasseur S et al (2005) Biochemical changes in response to intensive resistance exercise training in the elderly. Gerontology 51(4):253–265
Campbell KL, Campbell PT, Ulrich CM et al (2008) No reduction in C-reactive protein following a 12-month randomized controlled trial of exercise in men and women. Cancer Epidemiol Biomark Prevent 17(7):1714–1718
Cheema BS, Abas H, Smith BC et al (2011) Effect of resistance training during hemodialysis on circulating cytokines: a randomized controlled trial. Eur J Appl Physiol 111(7):1437–1445
Conraads VM, Beckers P, Bosmans J et al (2002) Combined endurance/resistance training reduces plasma TNF-alpha receptor levels in patients with chronic heart failure and coronary artery disease. Eur Heart J 23(23):1854–1860
Cordova C, Lopes ESF, Jr., Pires AS et al (2011) Long-term resistance training is associated with reduced circulating levels of IL-6, IFN-gamma and TNF-alpha in elderly women. Neuroimmunomodulation 18(3):165–170
Cornish SM, Johnson ST (2014) Systemic cytokine response to three bouts of eccentric exercise. Results Immunol 4:23–29
Dorshkind K, Montecino-Rodriguez E, Signer RA (2009) The ageing immune system: is it ever too old to become young again? Nat Rev Immunol 9(1):57–62
Fischer CP (2006) Interleukin-6 in acute exercise and training: what is the biological relevance? Exerc Immunol Rev 12:6–33
Forti LN, Njemini R, Beyer I et al (2014) Strength training reduces circulating interleukin-6 but not brain-derived neurotrophic factor in community-dwelling elderly individuals. Age (Dordr) 36(5):9704
Franceschi C, Capri M, Monti D et al (2007) Inflammaging and anti-inflammaging: a systemic perspective on aging and longevity emerged from studies in humans. Mech Ageing Dev 128(1):92–105
Frydelund-Larsen L, Penkowa M, Akerstrom T, Zankari A, Nielsen S, Pedersen BK (2007) Exercise induces interleukin-8 receptor (CXCR2) expression in human skeletal muscle. Exp Physiol 92(1):233–240
Gleeson M, Bishop NC, Stensel DJ, Lindley MR, Mastana SS, Nimmo MA (2011) The anti-inflammatory effects of exercise: mechanisms and implications for the prevention and treatment of disease. Nat Rev Immunol 11(9):607–615
Ho SS, Dhaliwal SS, Hills AP, Pal S (2013) Effects of chronic exercise training on inflammatory markers in Australian overweight and obese individuals in a randomized controlled trial. Inflammation 36(3):625–632
Izquierdo M, Ibanez J, Calbet JA et al (2009) Cytokine and hormone responses to resistance training. Eur J Appl Physiol 107(4):397–409
Jankord R, Jemiolo B (2004) Influence of physical activity on serum IL-6 and IL-10 levels in healthy older men. Med Sci Sports Exerc 36(6):960–964
Karabulut M, Sherk VD, Bemben DA, Bemben MG (2013) Inflammation marker, damage marker and anabolic hormone responses to resistance training with vascular restriction in older males. Clin Physiol Funct Imaging 33(5):393–399
Kohut ML, McCann DA, Russell DW et al (2006) Aerobic exercise, but not flexibility/resistance exercise, reduces serum IL-18, CRP, and IL-6 independent of beta-blockers, BMI, and psychosocial factors in older adults. Brain Behav Immun 20(3):201–209
Markovitch D, Tyrrell RM, Thompson D (2008) Acute moderate-intensity exercise in middle-aged men has neither an anti- nor proinflammatory effect. J Appl Physiol 105(1):260–265
Mathur N, Pedersen BK (2008) Exercise as a mean to control low-grade systemic inflammation. Mediators Inflamm. doi:10.1155/2008/109502
Nielsen AR, Pedersen BK (2007) The biological roles of exercise-induced cytokines: IL-6, IL-8, and IL-15. Appl Physiol Nutrit Metab Phys Appl Nutrit et Metab 32(5):833–839
Nieman DC (2012) Clinical implications of exercise immunology. J Sport Health Sci 1(1):12–17
Nieman DC, Henson DA, Smith LL et al (2001) Cytokine changes after a marathon race. J Appl Physiol 91(1):109–114
Olson TP, Dengel DR, Leon AS, Schmitz KH (2007) Changes in inflammatory biomarkers following one-year of moderate resistance training in overweight women. Int J Obes (Lond) 31(6):996–1003
Onambele-Pearson GL, Breen L, Stewart CE (2010) Influence of exercise intensity in older persons with unchanged habitual nutritional intake: skeletal muscle and endocrine adaptations. Age 32(2):139–153
Ostrowski K, Rohde T, Asp S, Schjerling P, Pedersen BK (1999) Pro- and anti-inflammatory cytokine balance in strenuous exercise in humans. J Physiol 515(Pt 1):287–291
Ostrowski K, Rohde T, Asp S, Schjerling P, Pedersen BK (2001) Chemokines are elevated in plasma after strenuous exercise in humans. Eur J Appl Physiol 84(3):244–245
Peake JM, Kukuljan S, Nowson CA, Sanders K, Daly RM (2011) Inflammatory cytokine responses to progressive resistance training and supplementation with fortified milk in men aged 50 + years: an 18-month randomized controlled trial. Eur J Appl Physiol 111(12):3079–3088
Peake JM, Suzuki K, Hordern M, Wilson G, Nosaka K, Coombes JS (2005) Plasma cytokine changes in relation to exercise intensity and muscle damage. Eur J Appl Physiol 95(5–6):514–521
Pedersen BK (2006) The anti-inflammatory effect of exercise: its role in diabetes and cardiovascular disease control. Essays Biochem 42:105–117
Pedersen BK, Febbraio MA (2008) Muscle as an endocrine organ: focus on muscle-derived interleukin-6. Physiol Rev 88(4):1379–1406
Pedersen BK, Febbraio MA (2012) Muscles, exercise and obesity: skeletal muscle as a secretory organ. Nat Rev Endocrinol 8(8):457–465
Pedersen BK, Saltin B (2015) Exercise as medicine - evidence for prescribing exercise as therapy in 26 different chronic diseases. Scand J Med Sci Sports 25(Suppl 3):1–72
Pedersen M, Steensberg A, Keller C et al (2004) Does the aging skeletal muscle maintain its endocrine function? Exerc Immunol Rev 10:42–55
Pereira GB, Tibana RA, Navalta J et al (2013) Acute effects of resistance training on cytokines and osteoprotegerin in women with metabolic syndrome. Clin Physiol Funct Imaging 33(2):122–130
Petersen AM, Pedersen BK (2005) The anti-inflammatory effect of exercise. J Appl Physiol 98(4):1154–1162
Phillips MD, Flynn MG, McFarlin BK, Stewart LK, Timmerman KL (2010) Resistance training at eight-repetition maximum reduces the inflammatory milieu in elderly women. Med Sci Sports Exerc 42(2):314–325
Phillips MD, Patrizi RM, Cheek DJ, Wooten JS, Barbee JJ, Mitchell JB (2012) Resistance training reduces subclinical inflammation in obese, postmenopausal women. Med Sci Sports Exerc 44(11):2099–2110
Riechman SE, Balasekaran G, Roth SM, Ferrell RE (2004) Association of interleukin-15 protein and interleukin-15 receptor genetic variation with resistance exercise training responses. J Appl Physiol (1985) 97(6):2214–2219
Van Roie E, Bautmans I, Boonen S, Coudyzer W, Kennis E, Delecluse C (2013) Impact of external resistance and maximal effort on force-velocity characteristics of the knee extensors during strengthening exercise: a randomized controlled experiment. Nat Strength Condit Assoc 27(4):1118–1127
Rojas Vega S, Knicker A, Hollmann W, Bloch W, Struder HK (2010) Effect of resistance exercise on serum levels of growth factors in humans. Horm Metab Res 42(13):982–986
Simpson RJ, Cosgrove C, Ingram LA et al (2008) Senescent T-lymphocytes are mobilised into the peripheral blood compartment in young and older humans after exhaustive exercise. Brain Behav Immun 22(4):544–551
Simpson RJ, Lowder TW, Spielmann G, Bigley AB, LaVoy EC, Kunz H (2012) Exercise and the aging immune system. Ageing Res Rev 11(3):404–420
Smith LL, Anwar A, Fragen M, Rananto C, Johnson R, Holbert D (2000) Cytokines and cell adhesion molecules associated with high-intensity eccentric exercise. Eur J Appl Physiol 82(1–2):61–67
Steensberg A, Fischer CP, Keller C, Moller K, Pedersen BK (2003) IL-6 enhances plasma IL-1ra, IL-10, and cortisol in humans. Am J Physiol Endocrinol Metab 285(2):E433–E437
Steensberg A, Keller C, Starkie RL, Osada T, Febbraio MA, Pedersen BK (2002) IL-6 and TNF-alpha expression in, and release from, contracting human skeletal muscle. Am J Physiol Endocrinol Metab 283(6):E1272–E1278
Stewart LK, Flynn MG, Campbell WW et al (2007) The influence of exercise training on inflammatory cytokines and C-reactive protein. Med Sci Sports Exerc 39(10):1714–1719
Thompson PD, Arena R, Riebe D, Pescatello LS, American College of Sports M (2013) ACSM’s new preparticipation health screening recommendations from ACSM’s guidelines for exercise testing and prescription, ninth edition. Curr Sports Med Rep 12(4):215–217
Thompson D, Markovitch D, Betts JA, Mazzatti D, Turner J, Tyrrell RM (2010) Time course of changes in inflammatory markers during a 6-mo exercise intervention in sedentary middle-aged men: a randomized-controlled trial. J Appl Physiol 108(4):769–779
Valiathan R, Ashman M, Asthana D (2016) Effects of ageing on the immune system: infants to elderly. Scand J Immunol 83(4):255–266
Varadhan R, Yao W, Matteini A et al (2014) Simple biologically informed inflammatory index of two serum cytokines predicts 10 year all-cause mortality in older adults. J Gerontol A Biol Sci Med Sci 69(2):165–173
Walsh NP, Gleeson M, Shephard RJ et al (2011) Position statement. Part one: Immune function and exercise. Exerc Immunol Rev 17:6–63
Zoppini G, Targher G, Zamboni C et al (2006) Effects of moderate-intensity exercise training on plasma biomarkers of inflammation and endothelial dysfunction in older patients with type 2 diabetes. Nutrit Metab Cardiovasc Dis 16(8):543–549
Acknowledgements
We would like to acknowledge the Research Foundation Flanders, Belgium (FWO-Vlaanderen), as E. Van Roie was a Ph.D. Fellow of FWO. The results of the present study do not constitute an endorsement by ACSM. The authors have no other declarations of interest to report.
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Communicated by Fabio Fischetti.
Louis Nuvagah Forti and Evelien Van Roie contributed equally to the paper and should be indexed as shared first authorship.
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Forti, L.N., Van Roie, E., Njemini, R. et al. Effects of resistance training at different loads on inflammatory markers in young adults. Eur J Appl Physiol 117, 511–519 (2017). https://doi.org/10.1007/s00421-017-3548-6
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DOI: https://doi.org/10.1007/s00421-017-3548-6