Skip to main content
SpringerLink
Log in

Changes in oxidative stress, inflammation and muscle damage markers following eccentric versus concentric cycling in older adults

  • Original Article
  • Published:
European Journal of Applied Physiology Aims and scope Submit manuscript

Abstract

Purpose

To compare concentric and eccentric cycling performed by older adults for metabolic demand and post-exercise oxidative stress, inflammation and muscle damage.

Methods

Eight male and two female healthy older adults (60.4 ± 6.8 years) performed 30 min of moderate-intensity concentric (CONC-M: 50% maximum power output; POmax) and eccentric cycling (ECC-M: 50% POmax) and high-intensity eccentric cycling (ECC-H: 100% POmax) in a randomized order. Average power output (PO), oxygen consumption (VO2), heart rate (HR) and rate of perceived exertion were recorded during cycling. Some indirect markers of muscle damage were assessed before, and immediately, 24 and 48 h after cycling. Markers of oxidative stress (malondialdehyde: MDA, protein carbonyl), antioxidant (total antioxidant capacity, glutathione peroxidase activity: GPx) and inflammation (IL-6, TNF-α) were measured before and 5 min after cycling.

Results

PO in ECC-H (202.6 ± 78.5 W) was > 50% greater (P < 0.05) than that of CONC-M (98.6 ± 33.1 W) and ECC-M (112.0 ± 42.1 W). VO2 and HR were also greater (P < 0.05) for ECC-H than CONC-M (50% and 17%, respectively) and ECC-M (40% and 23%, respectively). Muscle strength loss at 1 day post-exercise (8–22%), peak soreness (10–62 mm) and creatine kinase activity (30–250 IU/L) after ECC-H were greater (P < 0.05) than those after ECC-M and CONC-M. MDA decreased (P < 0.05) after CONC-M (− 28%) and ECC-M (− 22%), but not after ECC-H. GPx activity increased after all exercises similarly (20–27%). IL-6 increased (P < 0.05) only after ECC-H (18%).

Conclusion

Oxidative stress was minimal after eccentric cycling, but high-intensity eccentric cycling induced moderate muscle damage and inflammation, which is not desirable for older individuals.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Bernecker C, Scherr J, Schinner S, Braun S, Scherbaum WA, Halle M (2013) Evidence for an exercise induced increase of TNF-alpha and IL-6 in marathon runners. Scand J Med Sci Sports 23:207–214

    Article  CAS  PubMed  Google Scholar 

  • Berzosa C, Cebrian I, Fuentes-Broto L, Gomez-Trullen E, Piedrafita E, Martinez-Ballarin E, Lopez-Pingarron L, Reiter RJ, Garcia JJ (2011) Acute exercise increases plasma total antioxidant status and antioxidant enzyme activities in untrained men. J Biomed Biotech 2011:540458

    Article  CAS  Google Scholar 

  • Chasland LC, Green DJ, Maiorana AJ, Nosaka K, Haynes A, Dembo LG, Naylor LH (2017) Eccentric cycling: a promising modality for patients with chronic heart failure. Med Sci Sports Exer 49:646–651

    Article  Google Scholar 

  • Chen TC, Chen HL, Pearce AJ, Nosaka K (2012) Attenuation of eccentric exercise-induced muscle damage by preconditioning exercises. Med Sci Sports Exer 44:2090–2098

    Article  Google Scholar 

  • Chen TC, Hsieh CC, Tseng KW, Ho CC, Nosaka K (2017a) Effects of descending stair walking on health and fitness of elderly obese women. Med Sci Sports Exer 49:1614–1622

    Article  Google Scholar 

  • Chen TC, Tseng WC, Huang GL, Chen HL, Tseng KW, Nosaka K (2017b) Superior effects of eccentric to concentric knee extensor resistance training on physical fitness, insulin sensitivity and lipid profiles of elderly men. Front Physiol 8:209

    PubMed  PubMed Central  Google Scholar 

  • Cobley JN, Close GL, Bailey DM, Davison GW (2017) Exercise redox biochemistry: conceptual, methodological and technical recommendations. Redox biol 12:540–548

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Costamagna D, Costelli P, Sampaolesi M, Penna F (2015) Role of inflammation in muscle homeostasis and myogenesis. Mediators Inflamm 2015:805172

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Crossley E, Seri S, Stern JS, Robertson MM, Cavanna AE (2014) Premonitory urges for tics in adult patients with Tourette syndrome. Brain Dev 36:45–50

    Article  PubMed  Google Scholar 

  • Done AJ, Traustadottir T (2016) Aerobic exercise increases resistance to oxidative stress in sedentary older middle-aged adults. A pilot study. Age 38:505–512

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Douglas J, Pearson S, Ross A, McGuigan M (2017) Eccentric exercise: physiological characteristics and acute responses. Sports Med 47:663–675

    Article  PubMed  Google Scholar 

  • Elmer SJ, Madigan ML, Lastayo PC, Martin JC (2010) Joint-specific power absorption during eccentric cycling. Clin Biomech 25:154–158

    Article  Google Scholar 

  • Granic A, Davies K, Martin-Ruiz C, Jagger C, Kirkwood TBL, von Zglinicki T, Aihie Sayer A (2017) Grip strength and inflammatory biomarker profiles in very old adults. Age Ageing 46:976–982

    Article  PubMed  PubMed Central  Google Scholar 

  • James DA, Simjanovic M, Leadbetter R, Wearing S (2014) Design and test of a custom instrumented leg press for injury and recovery intervention. Procedia Eng 72:38–43

    Article  Google Scholar 

  • Lane-Cordova AD, Phillips SA, Baynard T, Woods JA, Motl RW, Fernhall B (2016) Effects of ageing and physical activity on blood pressure and endothelial function during acute inflammation. Exp Physiol 101:962–971

    Article  CAS  PubMed  Google Scholar 

  • Lastayo P, Marcus RL, Dibble L, Frajacomo F, Lindstedt SL (2014) Eccentric exercise in rehabilitation: safety, feasibility and application. J Appl Physiol 116:1426–1434

    Article  PubMed  Google Scholar 

  • Lastayo PC, Ewy GA, Pierotti DD, Johns RK, Lindstedt S (2003) The positive effects of negative work: increased muscle strength and decreased fall risk in a frail elderly population. J Gerontol 58:M419–424

    Article  Google Scholar 

  • Lastayo PC, Reich TE, Urquhart M, Hoppeler H, Lindstedt SL (1999) Chronic eccentric exercise: improvements in muscle strength can occur with little demand for oxygen. Am J Physiol 276:R611–R615

    Article  CAS  PubMed  Google Scholar 

  • Lavender AP, Nosaka K (2006) Comparison between old and young men for changes in makers of muscle damage following voluntary eccentric exercise of the elbow flexors. Appl Physiol Nutr Metab 31:218–225

    Article  PubMed  Google Scholar 

  • Lavender AP, Nosaka K (2008) A light load eccentric exercise confers protection against a subsequent bout of more demanding eccentric exercise. J Sci Med Sport 11:291–298

    Article  PubMed  Google Scholar 

  • Liu M, Timmons BW (2016) The effect of acute exercise on neutrophil reactive oxygen species production and inflammatory markers in healthy prepubertal and adult males. Pediatric Exer Sci 28:55–63

    Article  Google Scholar 

  • Margaritelis NV, Theodorou AA, Paschalis V, Veskoukis AS, Dipla K, Zafeiridis A, Panayiotou G, Vrabas IS, Kyparos A, Nikolaidis MG (2018) Adaptations to endurance training depend on exercise-induced oxidative stress: exploiting redox interindividual variability. Acta Physiol 22(2):e12898

    Article  CAS  Google Scholar 

  • McKay BR, De Lisio M, Johnston AP, O'Reilly CE, Phillips SM, Tarnopolsky MA, Parise G (2009) Association of interleukin-6 signalling with the muscle stem cell response following muscle-lengthening contractions in humans. PloS one 4:e6027

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Michailidis Y, Jamurtas AZ, Nikolaidis MG, Fatouros IG, Koutedakis Y, Papassotiriou I, Kouretas D (2007) Sampling time is crucial for measurement of aerobic exercise-induced oxidative stress. Med Sci Sports Exerc 39:1107–1113

    Article  CAS  PubMed  Google Scholar 

  • Monteiro-Junior RS, de Maciel-Pinheiro Tarso P, da Matta Mello Portugal E, da Silva Figueiredo LF, Terra R, Carneiro LSF, Rodrigues VD, Nascimento OJM, Deslandes AC, Laks J (2018) Effect of exercise on inflammatory profile of older persons: systematic review and meta-analyses. J Phys Act Health 15:64–71

    Article  PubMed  Google Scholar 

  • Moylan JS, Reid MB (2007) Oxidative stress, chronic disease, and muscle wasting. Muscle Nerve 35:411–429

    Article  CAS  PubMed  Google Scholar 

  • Nikolaidis M (2017) The effects of resistance exercise on muscle damage, position sense, and blood redox status in young and elderly individuals. Geriatrics 2(3):20

    Article  PubMed Central  Google Scholar 

  • Nikolaidis MG, Kyparos A, Spanou C, Paschalis V, Theodorou AA, Panayiotou G, Grivas GV, Zafeiridis A, Dipla K, Vrabas IS (2013) Aging is not a barrier to muscle and redox adaptations: applying the repeated eccentric exercise model. Exp Gerontol 48:734–743

    Article  CAS  PubMed  Google Scholar 

  • Nikolaidis MG, Margaritelis NV, Paschalis V et al (2015) Common questions and tentative answers on how to assess oxidative stress after antioxidant supplementation and exercise. In: Lamprecht M (ed) Antioxidants in sport nutrition, chap 14. CRC Press/Taylor & Francis, Boca Raton (FL)

    Google Scholar 

  • Nikolaidis MG, Paschalis V, Giakas G, Fatouros IG, Koutedakis Y, Kouretas D, Jamurtas AZ (2007) Decreased blood oxidative stress after repeated muscle-damaging exercise. Med Sci Sports Exer 39:1080–1089

    Article  CAS  Google Scholar 

  • Nordin TC, Done AJ, Traustadottir T (2014) Acute exercise increases resistance to oxidative stress in young but not older adults. Age 36:9727

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Park KS, Lee MG (2015) Effects of unaccustomed downhill running on muscle damage, oxidative stress, and leukocyte apoptosis. J Exerc Nutr Biochem 19:55–63

    Article  Google Scholar 

  • Paulsen G, Mikkelsen UR, Raastad T, Peake JM (2012) Leucocytes, cytokines and satellite cells: what role do they play in muscle damage and regeneration following eccentric exercise? Exerc Immunol Rev 18:42–97

    PubMed  Google Scholar 

  • Penailillo L, Blazevich A, Numazawa H, Nosaka K (2013) Metabolic and muscle damage profiles of concentric versus repeated eccentric cycling. Med Sci Sports Exer 45:1773–1781

    Article  CAS  Google Scholar 

  • Penailillo L, Blazevich AJ, Nosaka K (2017) Factors contributing to lower metabolic demand of eccentric compared with concentric cycling. J Appl Physiol 123:884–893

    Article  CAS  PubMed  Google Scholar 

  • Pokora I, Kempa K, Chrapusta SJ, Langfort J (2014) Effects of downhill and uphill exercises of equivalent submaximal intensities on selected blood cytokine levels and blood creatine kinase activity. Biol sport 31:173–178

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Powers SK, Nelson WB, Hudson MB (2011) Exercise-induced oxidative stress in humans: cause and consequences. Free Radic Biol Med 51:942–950

    Article  CAS  PubMed  Google Scholar 

  • Powers SK, Radak Z, Ji LL (2016) Exercise-induced oxidative stress: past, present and future. J Physiol 594:5081–5092

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sacheck JM, Milbury PE, Cannon JG, Roubenoff R, Blumberg JB (2003) Effect of vitamin E and eccentric exercise on selected biomarkers of oxidative stress in young and elderly men. Free Radic Biol Med 34:1575–1588

    Article  CAS  PubMed  Google Scholar 

  • Spirlandeli AL, Deminice R, Jordao AA (2014) Plasma malondialdehyde as biomarker of lipid peroxidation: effects of acute exercise. Int J Sports Med 35:14–18

    CAS  PubMed  Google Scholar 

  • Theodorou AA, Panayiotou G, Paschalis V, Nikolaidis MG, Kyparos A, Mademli L, Grivas GV, Vrabas IS (2013) Stair descending exercise increases muscle strength in elderly males with chronic heart failure. BMC Res Notes 6:87

    Article  PubMed  PubMed Central  Google Scholar 

  • Toft AD, Jensen LB, Bruunsgaard H, Ibfelt T, Halkjaer-Kristensen J, Febbraio M, Pedersen BK (2002) Cytokine response to eccentric exercise in young and elderly humans. Am J Physiol Cell Physiol 283:C289–295

    Article  CAS  PubMed  Google Scholar 

  • Vincent KR, Vincent HK, Braith RW, Lennon SL, Lowenthal DT (2002) Resistance exercise training attenuates exercise-induced lipid peroxidation in the elderly. Eur J Appl Physiol 87:416–423

    Article  CAS  PubMed  Google Scholar 

  • Webb R, Hughes MG, Thomas AW, Morris K (2017) The ability of exercise-associated oxidative stress to trigger redox-sensitive signalling responses. Antioxidants (Basel, Switzerland) 6:63

    Google Scholar 

  • Woods JA, Wilund KR, Martin SA, Kistler BM (2012) Exercise, inflammation and aging. Aging Dis 3:130–140

    PubMed  Google Scholar 

Download references

Acknowledgements

This work was funded by research Grants awarded to L.P. (#11150293) by CONICYT of Chile.

Funding

This work was funded by a research Grant (Fondo Nacional de Desarrollo Científico y Tecnológico) awarded to L.P. (#11150293) by CONICYT of Chile.

Author information

Authors and Affiliations

  1. Exercise Science Laboratory, School of Kinesiology, Faculty of Medicine, Universidad Finis Terrae, 1509 Pedro de Valdivia Av., Providencia, Santiago, Chile

    Roberto González-Bartholin, Karen Mackay, Denisse Valladares, Hermann Zbinden-Foncea & Luis Peñailillo

  2. Centre for Exercise and Sports Science Research, School of Medical and Health Sciences, Edith Cowan University, Joondalup, WA, Australia

    Kazunori Nosaka

Authors
  1. Roberto González-Bartholin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Karen Mackay
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Denisse Valladares
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hermann Zbinden-Foncea
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Kazunori Nosaka
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Luis Peñailillo
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

LP and KN conceived and designed the research. RG and KM conducted the experiments. HZ and DV contributed the biochemical analyses. RG and LP analysed the data. RG wrote the manuscript. All authors read and approved the manuscript.

Corresponding author

Correspondence to Luis Peñailillo.

Ethics declarations

Conflict of interest

There were no conflicts of interest.

Additional information

Communicated by Michalis G. Nikolaidis.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

González-Bartholin, R., Mackay, K., Valladares, D. et al. Changes in oxidative stress, inflammation and muscle damage markers following eccentric versus concentric cycling in older adults. Eur J Appl Physiol 119, 2301–2312 (2019). https://doi.org/10.1007/s00421-019-04213-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00421-019-04213-7

Keywords

Search

Navigation