Skip to main content

Oxidative stress, inflammation, and muscle soreness in an 894-km relay trail run

European Journal of Applied Physiology volume 112, pages 1839–1848 (2012)Cite this article

Abstract

We describe the effects of multi-day relay trail running on muscle soreness and damage, and systemic immune, inflammatory, and oxidative responses. 16 male and 4 female athletes ran 894 km in 47 stages over 95 h, with mean (SD) 6.4 (1.0) stages per athlete and 19.0 (1.7) km per stage. We observed post–pre run increases in serum creatine kinase (qualified effect size extremely large, p = 0.002), IL-6 (extremely large, p < 0.001), urinary 8–isoprostane/creatinine (extremely large, p = 0.04), TNF-α (large, p = 0.002), leukocyte count (very large, p < 0.0001) and neutrophil fraction (very large, p < 0.001); and reductions in hemoglobin (moderate, p < 0.001), hematocrit (moderate, p < 0.001), and lymphocyte fraction (trivial, p < 0.001). An increase in ORAC total antioxidant capacity (TAC, small, p = 0.3) and decrease in urinary 8-OHdG/creatinine (small, p = 0.1) were not statistically significant. During the run, muscle soreness was most frequent in the quadriceps. The threshold for muscle pain (pain-pressure algometry) in the vastus lateralis and gastrocnemius was lower post-run (small, p = 0.04 and 0.03). Average running speed was correlated with algometer pain and leukocyte count (large, r = 0.52), and TAC was correlated with IL-6 (very large, r = 0.76) and 8-isoprostane/creatinine (very large, r = −0.72). Multi-day stage-racing increases inflammation, lipid peroxidation, muscle damage and soreness without oxidative DNA damage. High TAC is associated with reduced exercise-induced lipid peroxidation, but is not related to immune response or muscle damage.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

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

Fig. 1
Fig. 2

References

  • Alessio HM, Hagerman AE, Fulkerson BK, Ambrose J, Rice RE, Wiley RL (2000) Generation of reactive oxygen species after exhaustive aerobic and isometric exercise. Med Sci Sports Exerc 32:1576

    PubMed  Article  CAS  Google Scholar 

  • Ali A, Caine MP, Snow BG (2007) Graduated compression stockings: physiological and perceptual responses during and after exercise. J Sports Sci 25:413

    PubMed  Article  CAS  Google Scholar 

  • Bessa A, Nissenbaum M, Monteiro A, Gandra PG, Nunes LS, Bassini-Cameron A, Werneck-de-Castro JPS, de Macedo DV, Cameron LC (2008) High-intensity ultraendurance promotes early release of muscle injury markers. Br J Sports Med 42:889–893

    PubMed  Article  CAS  Google Scholar 

  • Borg G (2001) Borg’s range model and scales. Int J Sport Psych 32:110–126

    Google Scholar 

  • Braun W, Dutto D (2003) The effects of a single bout of downhill running and ensuing delayed onset of muscle soreness on running economy performed 48 h later. Eur J Appl Physiol 90:29–34

    PubMed  Article  Google Scholar 

  • Brenner IKM, Natale VM, Vasiliou P, Moldoveanu AI, Shek PN, Shephard RJ (1999) Impact of three different types of exercise on components of the inflammatory response. Eur J Appl Physiol 80:452–460

    Article  CAS  Google Scholar 

  • Cao G, Alessio HM, Cutler RG (1993) Oxygen-radical absorbance capacity assay for antioxidants. Free Radic Biol Med 14:303–311

    PubMed  Article  CAS  Google Scholar 

  • Cheung K, Hume PA, Maxwell L (2003) Delayed onset muscle soreness: treatment strategies and rerformance factors. Sports Med 33:145–164

    PubMed  Article  Google Scholar 

  • Dohi Y, Takase H, Sato K, Ueda R (2007) Association among C-reactive protein, oxidative stress, and traditional risk factors in healthy Japanese subjects. Int J Cardiol 115:63–66

    PubMed  Article  Google Scholar 

  • Eston RG, Finney S, Baker S, Baltzopoulos V (1996) Muscle tenderness and peak torque changes after downhill running following a prior bout of isokinetic eccentric exercise. J Sports Sci 14:291–299

    PubMed  Article  CAS  Google Scholar 

  • Gundersen Y, Opstad P, Reistad T, Thrane I, Vaagenes P (2006) Seven days’ around the clock exhaustive physical exertion combined with energy depletion and sleep deprivation primes circulating leukocytes. Eur J Appl Physiol 97:151–157

    PubMed  Article  Google Scholar 

  • Hamill J, Freedson P, Clarkson P, Braun B (1991) Muscle soreness during running-biomechanical and physiological considerations. Int J Sport Biomech 7:125–137

    Google Scholar 

  • Harris C, Wilcox A, Smith G, Quinn C, Lawson L (1998) The effect of delayed onset muscular soreness (doms) on running kinematics [Abstract]. Med Sci Sports Exerc 22:S34

    Google Scholar 

  • Hopkins WG, Marshall SW, Batterham AM, Hanin J (2009) Progressive statistics for studies in sports medicine and exercise science. Med Sci Sports Exerc 41:3–13

    PubMed  Google Scholar 

  • Kim H, Lee Y, Kim C (2007) Biomarkers of muscle and cartilage damage and inflammation during a 200 km run. Eur J Appl Physiol 99:443–447

    PubMed  Article  CAS  Google Scholar 

  • Kim HJ, Jamart CC, Deldicque L, An G-L, Lee YH, Kim CK, Raymackers J-M, Francaux M (2011) Endoplasmic reticulum stress markers and ubiquitin-proteasome pathway activity in response to a 200-km run. Med Sci Sports Exerc 43:18–25

    PubMed  CAS  Google Scholar 

  • Kinnunen S, Hyyppä S, Lehmuskero A, Oksala N, Mäenpää P, Hänninen O, Atalay M (2005) Oxygen radical absorbance capacity (ORAC) and exercise-induced oxidative stress in trotters. Eur J Appl Physiol 95:550–556

    PubMed  Article  CAS  Google Scholar 

  • Knez WL, Coombes JS, Jenkins DG (2006) Ultra-endurance exercise and oxidative damage: implications for cardiovascular health. Sports Med 36:429–441

    PubMed  Article  Google Scholar 

  • Lafay S, Jan C, Nardon K, Lemaire B, Ibarra A, Roller M, Houvenaeghel M, Juhel C, Cara L (2009) Grape extract improves antioxidant status and physical performance in elite male athletes. J Sports Sci Med 8:468–480

    Google Scholar 

  • Malm C, Sjödin B, Sjöberg B, Lenkei R, Renström P, Lundberg IE, Ekblom B (2004) Leukocytes, cytokines, growth factors and hormones in human skeletal muscle and blood after uphill or downhill running. J Physiol 556:983–1000

    PubMed  Article  CAS  Google Scholar 

  • Mastaloudis A, Leonard SW, Traber MG (2001) Oxidative stress in athletes during extreme endurance exercise. Free Radic Biol Med 31:911–922

    PubMed  Article  CAS  Google Scholar 

  • Mastaloudis A, Morrow JD, Hopkins DW, Devaraj S, Traber MG (2004) Antioxidant supplementation prevents exercise-induced lipid peroxidation, but not inflammation, in ultramarathon runners. Free Radic Biol Med 36:1329–1341

    PubMed  Article  CAS  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. doi:1110.1249/1101.mss.1100b1013e318053e318057ba

    PubMed  Article  CAS  Google Scholar 

  • Miyata M, Kasai H, Kawai K, Yamada N, Tokudome M, Ichikawa H, Goto C, Tokudome Y, Kuriki K, Hoshino H, Shibata K, Suzuki S, Kobayashi M, Goto H, Ikeda M, Otsuka T, Tokudome S (2008) Changes of urinary 8-hydroxydeoxyguanosine levels during a two-day ultramarathon race period in japanese non-professional runners. Int J Sports Med 29:27–33

    PubMed  Article  CAS  Google Scholar 

  • Neubauer O, König D, Wagner KH (2008) Recovery after an Ironman triathlon: sustained inflammatory responses and muscular stress. Eur J Appl Physiol 104:417–426

    PubMed  Article  Google Scholar 

  • Neubauer O, Reichhold S, Nics L, Hoelzl C, Valentini J, Stadlmayr B, Knasmüller S, Wagner KH (2010) Antioxidant responses to an acute ultra-endurance exercise: impact on DNA stability and indications for an increased need for nutritive antioxidants in the early recovery phase. Br J Nutr 104:1129–1138

    PubMed  Article  CAS  Google Scholar 

  • Newham DJ, McPhail G, Mills KR, Edwards RHT (1983) Ultrastructural changes after concentric and eccentric contractions of human muscle. J Neurol Sci 61:109–122

    PubMed  Article  CAS  Google Scholar 

  • Nieman DC, Dumke CL, Henson DA, McAnulty SR, Gross SJ, Lind RH (2005) Muscle damage is linked to cytokine changes following a 160-km race. Brain Behav Immun 19:398–403

    PubMed  Article  CAS  Google Scholar 

  • Packer L (1997) Oxidants, antioxidant nutrients and the athlete. J Sports Sci 15:353–363

    PubMed  Article  CAS  Google Scholar 

  • Powers SK, Ji LL, Leeuwenburgh C (1999) Exercise training-induced alterations in skeletal muscle antioxidant capacity: a brief review. Med Sci Sports Exerc 31:987–997

    PubMed  Article  CAS  Google Scholar 

  • Praticò D, Tangirala RK, Rader DJ, Rokach J, FitzGerald GA (1998) Vitamin E suppresses isoprostane generation in vivo and reduces atherosclerosis in ApoE-deficient mice. Nat Med 4:1189

    PubMed  Article  Google Scholar 

  • Radák Z, Pucsuk J, Boros S, Josfai L, Taylor AW (2000) Changes in urine 8-hydroxydeoxyguanosine levels of super-marathon runners during a four-day race period. Life Sci 66:1763–1767

    PubMed  Article  Google Scholar 

  • Ristow M, Zarse K, Oberbach A, Klöting N, Birringer M, Kiehntopf M, Stumvoll M, Kahn CR, Blüher M (2009) Antioxidants prevent health-promoting effects of physical exercise in humans. Proc Natl Acad Sci USA 106:8665–8670

    PubMed  Article  CAS  Google Scholar 

  • Schwedhelm E, Bartling A, Lenzen H, Tsikas D, Maas R, Brummer J, Gutzki F-M, Berger J, Frolich JC, Boger RH (2004) Urinary 8-iso-prostaglandin f2α as a risk marker in patients with coronary heart disease: a matched case-control study. Circulation 109:843–848

    PubMed  Article  CAS  Google Scholar 

  • Smith LL (1992) Causes of delayed onset muscle soreness and the impact on athletic performance: a review. J Strength Cond Res 6:135–141

    Google Scholar 

  • Starkie RL, Rolland J, Angus DJ, Anderson MJ, Febbraio MA (2001) Circulating monocytes are not the source of elevations in plasma IL-6 and TNF-α levels after prolonged running. Am J Physiol Cell Physiol 280:C769–C774

    PubMed  CAS  Google Scholar 

  • Suzuki K, Peake J, Nosaka K, Okutsu M, Abbiss C, Surriano R, Bishop D, Quod M, Lee H, Martin D, Laursen P (2006) Changes in markers of muscle damage, inflammation and HSP70 after an Ironman triathlon race. Eur J Appl Physiol 98:525–534

    PubMed  Article  CAS  Google Scholar 

  • Timmons BW, Tarnopolsky MA, Snider DP, Bar-Or O (2006) Immunological changes in response to exercise: influence of age, puberty, and gender. Med Sci Sports Exerc 38:293

    PubMed  Article  CAS  Google Scholar 

  • Valavanidis A, Vlachogianni T, Fiotakis C (2009) 8-hydroxy-2′ -deoxyguanosine (8-OHdG): A Critical Biomarker of Oxidative Stress and Carcinogenesis. J Environ Sci Health C Environ Carcinog Ecotoxicol Rev 27:120–139

    PubMed  CAS  Google Scholar 

  • Wagner K-H, Reichhold S, Hölzl C, Knasmüller S, Nics L, Meisel M, Neubauer O (2010) Well-trained, healthy triathletes experience no adverse health risks regarding oxidative stress and DNA damage by participating in an ultra-endurance event. Toxicology 278:211–216

    PubMed  Article  CAS  Google Scholar 

  • Wallberg L, Mikael Mattsson C, Enqvist J, Ekblom B (2010) Plasma IL-6 concentration during ultra-endurance exercise. Eur J Appl Physiol

  • Wu LL, Chiou C–C, Chang P-Y, Wu JT (2004) Urinary 8-OHdG: a marker of oxidative stress to DNA and a risk factor for cancer, atherosclerosis and diabetics. Clin Chim Acta 339:1–9

    PubMed  Article  CAS  Google Scholar 

  • Yamada M, Suzuki K, Kudo S, Totsuka M, Nakaji S, Sugawara K (2002) Raised plasma G-CSF and IL-6 after exercise may play a role in neutrophil mobilization into the circulation. J Appl Physiol 92:1789–1794

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

Nestle/Powerbar donated bars, drinks and clothing. We would like to thank all the volunteers who made the race and study possible with a special thanks to Allyson Donato, Donald and Rosemary Chew, Mark Tamminga, Joany Verschuuren, the VanDorp family, Stacie Smith, Tracey McLaughlin, Barb Campbell, Richard Ehrlich, and Imperial Oil Ltd. for their gracious assistance with the relay logistics.

Conflict of interest

Life Science Nutritionals contributed financially toward costs associated with the race (transport, food, supplies). The analytical costs were funded from a grant from Natural Sciences and Engineering Research Council of Canada.

Author information

Authors and Affiliations

  1. School of Sport and Exercise, Massey University, Pvt Box 756, Wellington, 6021, New Zealand

    David S. Rowlands & J. G. Green

  2. Department of Pediatrics and Medicine, McMaster University, Hamilton, Canada

    E. Pearce, A. Aboud & M. A. Tarnopolsky

  3. Kinesiology, McMaster University, Hamilton, Canada

    J. B. Gillen & M. J. Gibala

  4. Adventure Science, Calgary, Canada

    S. Donato

  5. McMaster Centre for Climate Change, McMaster University, Hamilton, Canada

    J. M. Waddington

Authors
  1. David S. Rowlands
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. E. Pearce
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. A. Aboud
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. J. B. Gillen
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. M. J. Gibala
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. S. Donato
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. J. M. Waddington
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. J. G. Green
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. M. A. Tarnopolsky
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to David S. Rowlands.

Additional information

Communicated by William J. Kraemer.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Rowlands, D.S., Pearce, E., Aboud, A. et al. Oxidative stress, inflammation, and muscle soreness in an 894-km relay trail run. Eur J Appl Physiol 112, 1839–1848 (2012). https://doi.org/10.1007/s00421-011-2163-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00421-011-2163-1

Keywords

  • TNF-α
  • IL-6
  • ORAC
  • 8-isoprostane
  • 8-OHdG
  • DOMS