Int J Sports Med 2024; 45(12): 897-907
DOI: 10.1055/a-2348-0238
Physiology & Biochemistry

Acute Inflammatory Response to Eccentric Exercise in Young and Master Resistance-trained Athletes

1   Exercise and Immunometabolism Research Group, Postgraduate Program in Movement Sciences, Department of Physical Education, UNESP Campus de Presidente Prudente, Presidente Prudente, Brazil
2   Faculty of Sport Sciences and Physical Education, Research Center for Sport and Physical Activity, University of Coimbra, Coimbra, Portugal
3   Department of Exercise Physiology and Sports Therapy, Institute of Sport Science, Justus Liebig University Giessen, Giessen, Germany
,
4   Faculty of Sport Science, Ruhr University Bochum, Bochum, Germany
,
Matheus Uba Chupel
5   Biological Sciences Platform - Hurvitz Brain Sciences, Sunnybrook Research Institute, Toronto, Ontario, Canada
,
3   Department of Exercise Physiology and Sports Therapy, Institute of Sport Science, Justus Liebig University Giessen, Giessen, Germany
,
Christopher Weyh
3   Department of Exercise Physiology and Sports Therapy, Institute of Sport Science, Justus Liebig University Giessen, Giessen, Germany
,
6   Department of Systems Biology, Universidad de Alcala de Henares, Madrid, Spain
7   Physical Activity and Health Research Group (PaHerg), Research Institute of Hospital 12 de Octubre (imas12), Madrid, Spain
,
Alejandro Lucia
8   Faculty of Sport Sciences, Universidad Europea de Madrid, Madrid, Spain
9   Research Institute of the Hospital 12 de Octubre ('imas12'), Madrid, Spain
,
3   Department of Exercise Physiology and Sports Therapy, Institute of Sport Science, Justus Liebig University Giessen, Giessen, Germany
,
Thomas Reichel
3   Department of Exercise Physiology and Sports Therapy, Institute of Sport Science, Justus Liebig University Giessen, Giessen, Germany
› Author Affiliations

Abstract

This study aimed to compare the acute inflammatory response following high-intensity eccentric exercise between resistance-trained young and master athletes with similar performance levels. Resistance-trained young (n=8; 22±2 years) and master (n=8; 52±4 years) male athletes of a similar performance level performed a standardized high-intensity eccentric squat exercise protocol (10 sets of half-squats at 70% of 1-repetition maximum). The serum concentration of 20 biomarkers related to tissue damage, inflammation, remodeling, and repair was measured at baseline, immediately after exercise, and over a 72 h recovery period. Both groups experienced similar muscle damage as evidenced by a comparable increase in creatine kinase activity 24 h after exercise (p<0.001). Interleukin-6 (p=0.009) and growth hormone (p<0.001) increased immediately post-exercise in both groups. Monocyte chemoattractant protein-1 increased immediately post-exercise only in young athletes (p=0.003) and then decreased 24 h later. There were no significant differences for the remaining variables, including cell markers related to neutrophil/macrophage activation or pro/anti-inflammatory cytokines. Resistance-trained young and master athletes, matched for performance level, showed an overall similar inflammatory response to eccentric exercise, possibly reflecting regulatory mechanisms or immunological adaptations to chronic stimulation in master athletes.



Publication History

Received: 07 March 2024

Accepted: 11 June 2024

Article published online:
28 July 2024

© 2024. Thieme. All rights reserved.

Georg Thieme Verlag KG
Rüdigerstraße 14, 70469 Stuttgart, Germany

 
  • References

  • 1 Cerqueira É, Marinho DA, Neiva HP. et al. Inflammatory Effects of High and Moderate Intensity Exercise – A Systematic Review. Front Physiol 2020; 10: 1550
  • 2 Peake JM, Neubauer O, Della Gatta PA. et al. Muscle damage and inflammation during recovery from exercise. J Appl Physiol Bethesda Md 1985 2017; 122: 559-570
  • 3 Baird MF, Graham SM, Baker JS. et al. Creatine-kinase- and exercise-related muscle damage implications for muscle performance and recovery. J Nutr Metab 2012; 2012: 960363 DOI: 10.1155/2012/960363.
  • 4 Tanaka H, Seals DR. Endurance exercise performance in Masters athletes: Age-associated changes and underlying physiological mechanisms. J Physiol 2008; 586: 55-63
  • 5 Valenzuela PL, Maffiuletti NA, Joyner MJ. et al. Lifelong Endurance Exercise as a Countermeasure Against Age-Related [Formula: see text] Decline: Physiological Overview and Insights from Masters Athletes. Sports Med Auckl NZ 2020; 50: 703-716
  • 6 Aguiar SS, Rosa TS, Sousa CV. et al. Influence of Body Fat on Oxidative Stress and Telomere Length of Master Athletes. J Strength Cond Res 2019; 35: 1693-1699
  • 7 Simoes H, Sousa C, dos Santos Rosa T. et al. Longer Telomere Length in Elite Master Sprinters: Relationship to Performance and Body Composition. Int J Sports Med 2017; 38: 1111-1116
  • 8 Minuzzi LG, Rama L, Chupel MU. et al. Effects of lifelong training on senescence and mobilization of T lymphocytes in response to acute exercise. Exerc Immunol Rev 2018; 24: 72-84
  • 9 Walsh NP. Recommendations to maintain immune health in athletes. Eur J Sport Sci 2018; 18: 820-831
  • 10 de Araújo AL, Silva LCR, Fernandes JR. et al. Elderly men with moderate and intense training lifestyle present sustained higher antibody responses to influenza vaccine. Age Dordr Neth 2015; 37: 105
  • 11 Schmidt J, Ferrauti A, Kellmann M. et al. Recovery From Eccentric Squat Exercise in Resistance-Trained Young and Master Athletes With Similar Maximum Strength: Combining Cold Water Immersion and Compression. Front Physiol 2021; 12: 665204 DOI: 10.3389/fphys.2021.665204.
  • 12 Campbell JP, Turner JE. Debunking the myth of exercise-induced immune suppression: Redefining the impact of exercise on immunological health across the lifespan. Front Immunol 2018; 9: 1-21
  • 13 Minuzzi LG, Rama L, Bishop NC. et al. Lifelong training improves anti-inflammatory environment and maintains the number of regulatory T cells in masters athletes. Eur J Appl Physiol 2017; 117: 1131-1140
  • 14 Mikkelsen UR, Couppé C, Karlsen A. et al. Life-long endurance exercise in humans: Circulating levels of inflammatory markers and leg muscle size. Mech Ageing Dev 2013; 134: 531-540
  • 15 Sellami M, Gasmi M, Denham J. et al. Effects of acute and chronic exercise on immunological parameters in the elderly aged: Can physical activity counteract the effects of aging?. Front Immunol 2018; 9: 1-17
  • 16 Aguiar SS, Sousa CV, Deus LA. et al. Oxidative stress, inflammatory cytokines and body composition of master athletes: The interplay. Exp Gerontol 2020; 130: 110806 DOI: 10.1016/j.exger.2019.110806.
  • 17 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
  • 18 Raeder C, Wiewelhove T, Westphal-Martinez MP. et al. Neuromuscular Fatigue and Physiological Responses After Five Dynamic Squat Exercise Protocols. J Strength Cond Res 2016; 30: 953 DOI: 10.1519/JSC.0000000000001181.
  • 19 Chazaud B. Inflammation and Skeletal Muscle Regeneration: Leave It to the Macrophages!. Trends Immunol 2020; 41: 481-492
  • 20 Lavin KM, Perkins RK, Jemiolo B. et al. Effects of aging and lifelong aerobic exercise on basal and exercise-induced inflammation. J Appl Physiol 2020; 128: 87-99
  • 21 de Souza Teixeira AA, Minuzzi LG, Lira FS. et al. Improvement in the anti-inflammatory profile with lifelong physical exercise is related to clock genes expression in effector-memory CD4+ T cells in master athletes. Exerc Immunol Rev 2021; 27: 67-83
  • 22 Minuzzi LG, Chupel MU, Rama L. et al. Lifelong exercise practice and immunosenescence: Master athletes cytokine response to acute exercise. Cytokine 2019; 115: 1-7
  • 23 Hayes LD, Herbert P, Sculthorpe NF. et al. Short-Term and Lifelong Exercise Training Lowers Inflammatory Mediators in Older Men. Front Physiol 2021; 12: 702248 DOI: 10.3389/fphys.2021.702248.
  • 24 Minuzzi LG, Rama L, Bishop NC. et al. Lifelong training improves anti-inflammatory environment and maintains the number of regulatory T cells in masters athletes. Eur J Appl Physiol 2017; 117: 1131-1140
  • 25 Mckendry J, Breen L, Shad BJ. et al. Muscle morphology and performance in master athletes: A systematic review and meta-analyses. Ageing Res Rev 2018; 45: 62-82
  • 26 Leslie E, Luna V, Gibson AL. Older Adult Aerobic Capacity, Muscular Strength, Fitness and Body Composition After 20+ Years of Exercise Training: A Systematic Review and Meta-Analysis. Int J Exerc Sci 2023; 16: 620-637
  • 27 Newton MJ, Morgan GT, Sacco P. et al. Comparison of responses to strenuous eccentric exercise of the elbow flexors between resistance-trained and untrained men. J Strength Cond Res 2008; 22: 597-607
  • 28 Buford TW, MacNeil RG, Clough LG. et al. Active muscle regeneration following eccentric contraction-induced injury is similar between healthy young and older adults. J Appl Physiol 2014; 116: 1481-1490
  • 29 Gordon JA, Hoffman JR, Arroyo E. et al. Comparisons in the Recovery Response From Resistance Exercise Between Young and Middle-Aged Men. J Strength Cond Res 2017; 31: 3454-3462
  • 30 Coudy-Gandilhon C, Gueugneau M, Chambon C. et al. A Single Bout of Ultra-Endurance Exercise Reveals Early Signs of Muscle Aging in Master Athletes. Int J Mol Sci 2022; 23: 3713
  • 31 Markus I, Constantini K, Goldstein N. et al. Age Differences in Recovery Rate Following an Aerobic-Based Exercise Protocol Inducing Muscle Damage Among Amateur, Male Athletes. Front Physiol 2022; 13: 916924
  • 32 Sprenkeler EGG, Zandstra J, van Kleef ND. et al. S100A8/A9 Is a Marker for the Release of Neutrophil Extracellular Traps and Induces Neutrophil Activation. Cells 2022; 11: 236 DOI: 10.3390/cells11020236.
  • 33 Matsushima K, Yang D, Oppenheim JJ. Interleukin-8: An evolving chemokine. Cytokine 2022; 153: 155828 DOI: 10.1016/j.cyto.2022.155828.
  • 34 Lu H, Huang D, Ransohoff RM. et al. Acute skeletal muscle injury: CCL2 expression by both monocytes and injured muscle is required for repair. FASEB J Off Publ Fed Am Soc Exp Biol 2011; 25: 3344-3355
  • 35 Yahiaoui L, Gvozdic D, Danialou G. et al. CC family chemokines directly regulate myoblast responses to skeletal muscle injury. J Physiol 2008; 586: 3991-4004
  • 36 Nicholas J, Voss JG, Tsuji J. et al. Time course of chemokine expression and leukocyte infiltration after acute skeletal muscle injury in mice. Innate Immun 2015; 21: 266-274
  • 37 Catoire M, Mensink M, Kalkhoven E. et al. Identification of human exercise-induced myokines using secretome analysis. Physiol Genomics 2014; 46: 256-267
  • 38 Hubal MJ, Chen TC, Thompson PD. et al. Inflammatory gene changes associated with the repeated-bout effect. Am J Physiol-Regul Integr Comp Physiol 2008; 294: R1628-R1637
  • 39 Harmon BT, Orkunoglu-Suer EF, Adham K. et al. CCL2 and CCR2 variants are associated with skeletal muscle strength and change in strength with resistance training. J Appl Physiol 2010; 109: 1779-1785
  • 40 Blanc RS, Kallenbach JG, Bachman JF. et al. Inhibition of inflammatory CCR2 signaling promotes aged muscle regeneration and strength recovery after injury. Nat Commun 2020; 11: 4167
  • 41 Ahmadi M, Karlsen A, Mehling J. et al. Aging is associated with an altered macrophage response during human skeletal muscle regeneration. Exp Gerontol 2022; 169: 111974
  • 42 Sorensen JR, Kaluhiokalani JP, Hafen PS. et al. An altered response in macrophage phenotype following damage in aged human skeletal muscle: Implications for skeletal muscle repair. FASEB J Off Publ Fed Am Soc Exp Biol 2019; 33: 10353-10368
  • 43 Skytthe MK, Graversen JH, Moestrup SK. Targeting of CD163+ Macrophages in Inflammatory and Malignant Diseases. Int J Mol Sci 2020; 21: 5497 DOI: 10.3390/ijms21155497.
  • 44 Caldow MK, Cameron-Smith D, Levinger P. et al. Inflammatory markers in skeletal muscle of older adults. Eur J Appl Physiol 2013; 113: 509-517
  • 45 Della Gatta PA, Garnham AP, Peake JM. et al. Effect of exercise training on skeletal muscle cytokine expression in the elderly. Brain Behav Immun 2014; 39: 80-86
  • 46 Balan E, Diman A, Everard A. et al. Endurance training alleviates MCP-1 and TERRA accumulation at old age in human skeletal muscle. Exp Gerontol 2021; 153: 111510 DOI: 10.1016/j.exger.2021.111510.
  • 47 Aguiar SS, Sousa CV, Santos PA. et al. Master athletes have longer telomeres than age-matched non-athletes. A systematic review, meta-analysis and discussion of possible mechanisms. Exp Gerontol 2021; 146: 111212 DOI: 10.1016/j.exger.2020.111212.
  • 48 Schnyder S, Handschin C. Skeletal muscle as an endocrine organ: PGC-1α, myokines and exercise. Bone 2015; 80: 115-125
  • 49 Kanda H, Tateya S, Tamori Y. et al. MCP-1 contributes to macrophage infiltration into adipose tissue, insulin resistance, and hepatic steatosis in obesity. J Clin Invest 2006; 116: 1494-1505
  • 50 Oliveira AG, Araujo TG, Carvalho BM. et al. Acute exercise induces a phenotypic switch in adipose tissue macrophage polarization in diet-induced obese rats. Obes Silver Spring. Md 2013; 21: 2545-2556
  • 51 Chazaud B. Inflammation and Skeletal Muscle Regeneration: Leave It to the Macrophages!. Trends Immunol 2020; 41: 481-492
  • 52 Clifford BK, Kaakoush NO, Tedla N. et al. The effect of exercise intensity on the inflammatory profile of cancer survivors: A randomised crossover study. Eur J Clin Invest 2023; 53: e13984
  • 53 Nash D, Hughes MG, Butcher L. et al. IL-6 signaling in acute exercise and chronic training: Potential consequences for health and athletic performance. Scand J Med Sci Sports 2023; 33: 4-19
  • 54 Nieman DC, Wentz LM. The compelling link between physical activity and the body’s defense system. J Sport Health Sci 2019; 8: 201-217
  • 55 Izquierdo M, Ibañez J, Calbet JAL. et al. Cytokine and hormone responses to resistance training. Eur J Appl Physiol 2009; 107: 397-409
  • 56 Mitchell CJ, Churchward-Venne TA, Bellamy L. et al. Muscular and Systemic Correlates of Resistance Training-Induced Muscle Hypertrophy. PLoS ONE 2013; 8: e78636 DOI: 10.1371/journal.pone.0078636.
  • 57 Santos Junior ERT, de Salles BF, Dias I. et al. Classification and Determination Model of Resistance Training Status. Strength Cond J 2021; 43: 77-86
  • 58 Gøran P, Paulsen G, Mikkelsen UR. et al. Leucocytes, cytokines and satellite cells: What role do they play in muscle damage and regeneration following eccentric exercise?. Exerc Immunol Rev 2012; 18: 42-97