Abstract
Purpose
Acute high-intensity unaccustomed eccentric exercise performed by naive subjects is accompanied by disturbances in muscle damage biomarkers. The aim of the study was to investigate whether a causal relationship indeed exists between eccentric exercise and muscle damage.
Methods
Twenty-four men randomly assigned into a concentric only or an eccentric-only training group and performed 10 weeks of isokinetic resistance exercise (one session/week of 75 maximal knee extensors actions). Physiological markers of muscle function and damage (i.e., range of motion, delayed onset muscle soreness, isometric, concentric and eccentric peak torque) were assessed prior to and 1–3 and 5 days post each session. Biochemical markers of muscle damage (creatine kinase) and inflammation (C-reactive protein) were measured prior and 2 days post each session.
Results
After the first bout, eccentric exercise induced greater muscle damage compared to concentric exercise; however, during the nine following sessions, this effect progressively diminished, while after the 10th week of training, no alterations in muscle damage biomarkers were observed after either exercise protocol. Additionally, strength gains at the end of the training period were comparable between the two groups and were mode-specific.
Conclusion
(1) eccentric exercise per se does not affect muscle damage biomarkers; (2) muscle damage occurs as a result of muscle unaccustomedness to this action type; (3) exercise-induced muscle damage is not a prerequisite for increased muscle strength. Collectively, we believe that muscle unaccustomedness to high-intensity eccentric exercise, and not eccentric exercise per se, is the trigger for muscle damage as indicated by muscle damage biomarkers.
This is a preview of subscription content, access via your institution.
Data availability
There is availability of code, data and material of the present investigation.
Abbreviations
- CK:
-
Creatine kinase
- CRP:
-
C-reactive protein
- DOMS:
-
Delayed onset muscle soreness
- ROM:
-
Pain-free range of motion
References
Ando R, Nosaka K, Tomita A, Watanabe K, Blazevich AJ, Akima H (2018) Vastus intermedius vs vastus lateralis fascicle behaviors during maximal concentric and eccentric contractions. Scand J Med Sci Sports 28:1018–1026. https://doi.org/10.1111/sms.13022
Blazevich AJ, Cannavan D, Coleman DR, Horne S (2007) Influence of concentric and eccentric resistance training on architectural adaptation in human quadriceps muscles. J Appl Physiol (1985) 103:1565–1575. https://doi.org/10.1152/japplphysiol.00578.2007
Butterfield TA, Leonard TR, Herzog W (2005) Differential serial sarcomere number adaptations in knee extensor muscles of rats is contraction type dependent. J Appl Physiol (1985) 99:1352–1358. https://doi.org/10.1152/japplphysiol.00481.2005
Cadore EL, Gonzalez-Izal M, Grazioli R, Setuain I, Pinto RS, Izquierdo M (2018) Effects of concentric and eccentric strength training on fatigue induced by concentric and eccentric exercise. Int J Sports Physiol Perform. https://doi.org/10.1123/ijspp.2018-0254
Cermak NM, Noseworthy MD, Bourgeois JM, Tarnopolsky MA, Gibala MJ (2012) Diffusion tensor MRI to assess skeletal muscle disruption following eccentric exercise. Muscle Nerve 46:42–50. https://doi.org/10.1002/mus.23276
Chen TC, Chen HL, Lin MJ, Wu CJ, Nosaka K (2009) Muscle damage responses of the elbow flexors to four maximal eccentric exercise bouts performed every 4 weeks. Eur J Appl Physiol 106:267–275. https://doi.org/10.1007/s00421-009-1016-7
Chen TC, Chen HL, Pearce AJ, Nosaka K (2012) Attenuation of eccentric exercise-induced muscle damage by preconditioning exercises. Med Sci Sports Exerc 44:2090–2098. https://doi.org/10.1249/MSS.0b013e31825f69f3
Cook CS, McDonagh MJ (1995) Force responses to controlled stretches of electrically stimulated human muscle-tendon complex. Exp Physiol 80:477–490. https://doi.org/10.1113/expphysiol.1995.sp003862
de Oliveira HA et al (2018) Protective effects of photobiomodulation against resistance exercise-induced muscle damage and inflammation in rats. J Sports Sci 36:2349–2357. https://doi.org/10.1080/02640414.2018.1457419
Dieli-Conwright CM, Spektor TM, Rice JC, Sattler FR, Schroeder ET (2009) Hormone therapy attenuates exercise-induced skeletal muscle damage in postmenopausal women. J Appl Physiol 107:853–858. https://doi.org/10.1152/japplphysiol.00404.2009
Enoka RM (1996) Eccentric contractions require unique activation strategies by the nervous system. J Appl Physiol (1985) 81:2339–2346. https://doi.org/10.1152/jappl.1996.81.6.2339
Evans WJ, Cannon JG (1991) The metabolic effects of exercise-induced muscle damage. Exerc Sport Sci Rev 19:99–125
Farthing JP, Chilibeck PD (2003) The effects of eccentric and concentric training at different velocities on muscle hypertrophy. Eur J Appl Physiol 89:578–586. https://doi.org/10.1007/s00421-003-0842-2
Faulkner JA, Brooks SV, Opiteck JA (1993) Injury to skeletal muscle fibers during contractions: conditions of occurrence and prevention. Phys Ther 73:911–921. https://doi.org/10.1093/ptj/73.12.911
Flann KL, LaStayo PC, McClain DA, Hazel M, Lindstedt SL (2011) Muscle damage and muscle remodeling: no pain, no gain? J Exp Biol 214:674–679. https://doi.org/10.1242/jeb.050112
Franchi MV et al (2014) Architectural, functional and molecular responses to concentric and eccentric loading in human skeletal muscle. Acta Physiol (Oxf) 210:642–654. https://doi.org/10.1111/apha.12225
Franchi MV et al (2015) Early structural remodeling and deuterium oxide-derived protein metabolic responses to eccentric and concentric loading in human skeletal muscle. Physiol Rep 3:e12593. https://doi.org/10.14814/phy2.12593
Franchi MV, Reeves ND, Narici MV (2017) Skeletal muscle remodeling in response to eccentric vs concentric loading: morphological, molecular, and metabolic adaptations. Front Physiol 8:447. https://doi.org/10.3389/fphys.2017.00447
Franchi MV et al (2018) Regional regulation of focal adhesion kinase after concentric and eccentric loading is related to remodelling of human skeletal muscle. Acta Physiol (Oxf) 223:e13056. https://doi.org/10.1111/apha.13056
Friden J, Sjostrom M, Ekblom B (1983) Myofibrillar damage following intense eccentric exercise in man. Int J Sports Med 4:170–176. https://doi.org/10.1055/s-2008-1026030
Geremia JM, Baroni BM, Bini RR, Lanferdini FJ, de Lima AR, Herzog W, Vaz MA (2019) Triceps surae muscle architecture adaptations to eccentric training. Front Physiol 10:1456. https://doi.org/10.3389/fphys.2019.01456
Guilhem G, Doguet V, Hauraix H, Lacourpaille L, Jubeau M, Nordez A, Dorel S (2016) Muscle force loss and soreness subsequent to maximal eccentric contractions depend on the amount of fascicle strain in vivo. Acta Physiol (Oxf) 217:152–163. https://doi.org/10.1111/apha.12654
Hessel AL, Lindstedt SL, Nishikawa KC (2017) Physiological mechanisms of eccentric contraction and its applications: a role for the giant titin protein. Front Physiol 8:70. https://doi.org/10.3389/fphys.2017.00070
Hicks KM, Onambele-Pearson GL, Winwood K, Morse CI (2017) Muscle-tendon unit properties during eccentric exercise correlate with the creatine kinase response. Front Physiol 8:657. https://doi.org/10.3389/fphys.2017.00657
Hilliard-Robertson PC, Schneider SM, Bishop SL, Guilliams ME (2003) Strength gains following different combined concentric and eccentric exercise regimens. Aviat Space Environ Med 74:342–347
Hoffman BW, Cresswell AG, Carroll TJ, Lichtwark GA (2016) Protection from muscle damage in the absence of changes in muscle mechanical behavior. Med Sci Sports Exerc 48:1495–1505. https://doi.org/10.1249/MSS.0000000000000920
Hoppeler H (2016) Moderate load eccentric exercise; a distinct novel training modality. Front Physiol 7:483. https://doi.org/10.3389/fphys.2016.00483
Hortobagyi T (2003) The positives of negatives: clinical implications of eccentric resistance exercise in old adults. J Gerontol A Biol Sci Med Sci 58:M417-418. https://doi.org/10.1093/gerona/58.5.m417
Hortobagyi T, Hill JP, Houmard JA, Fraser DD, Lambert NJ, Israel RG (1996) Adaptive responses to muscle lengthening and shortening in humans. J Appl Physiol (1985) 80:765–772. https://doi.org/10.1152/jappl.1996.80.3.765
Hyldahl RD, Hubal MJ (2014) Lengthening our perspective: morphological, cellular, and molecular responses to eccentric exercise. Muscle Nerve 49:155–170. https://doi.org/10.1002/mus.24077
Jubeau M, Muthalib M, Millet GY, Maffiuletti NA, Nosaka K (2012) Comparison in muscle damage between maximal voluntary and electrically evoked isometric contractions of the elbow flexors. Eur J Appl Physiol 112:429–438. https://doi.org/10.1007/s00421-011-1991-3
Katz B (1939) The relation between force and speed in muscular contraction. J Physiol 96:45–64. https://doi.org/10.1113/jphysiol.1939.sp003756
Kirwan JP, Hickner RC, Yarasheski KE, Kohrt WM, Wiethop BV, Holloszy JO (1992) Eccentric exercise induces transient insulin resistance in healthy individuals. J Appl Physiol (1985) 72:2197–2202. https://doi.org/10.1152/jappl.1992.72.6.2197
Klossner S, Dapp C, Schmutz S, Vogt M, Hoppeler H, Fluck M (2007) Muscle transcriptome adaptations with mild eccentric ergometer exercise. Pflugers Arch 455:555–562. https://doi.org/10.1007/s00424-007-0303-6
Konow N, Azizi E, Roberts TJ (2012) Muscle power attenuation by tendon during energy dissipation. Proc Biol Sci 279:1108–1113. https://doi.org/10.1098/rspb.2011.1435
Lacome M, Avrillon S, Cholley Y, Simpson BM, Guilhem G, Buchheit M (2019) Hamstring eccentric strengthening program: does training volume matter? Int J Sports Physiol Perform. https://doi.org/10.1123/ijspp.2018-0947
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:R611-615. https://doi.org/10.1152/ajpregu.1999.276.2.R611
LaStayo PC, Pierotti DJ, Pifer J, Hoppeler H, Lindstedt SL (2000) Eccentric ergometry: increases in locomotor muscle size and strength at low training intensities. Am J Physiol Regul Integr Comp Physiol 278:R1282-1288. https://doi.org/10.1152/ajpregu.2000.278.5.R1282
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 A Biol Sci Med Sci 58:M419-424. https://doi.org/10.1093/gerona/58.5.m419
Lau WY, Blazevich AJ, Newton MJ, Wu SS, Nosaka K (2015) Reduced muscle lengthening during eccentric contractions as a mechanism underpinning the repeated-bout effect. Am J Physiol Regul Integr Comp Physiol 308:R879-886. https://doi.org/10.1152/ajpregu.00338.2014
Lieber RL, Friden J (1988) Selective damage of fast glycolytic muscle fibres with eccentric contraction of the rabbit tibialis anterior. Acta Physiol Scand 133:587–588. https://doi.org/10.1111/j.1748-1716.1988.tb08446.x
Lieber RL, Shah S, Friden J (2002) Cytoskeletal disruption after eccentric contraction-induced muscle injury. Clin Orthop Relat Res. https://doi.org/10.1097/00003086-200210001-00011
Lindstedt SL (2016) Skeletal muscle tissue in movement and health: positives and negatives. J Exp Biol 219:183–188. https://doi.org/10.1242/jeb.124297
Maeo S, Yamamoto M, Kanehisa H (2016) Downhill walking training with and without exercise-induced muscle damage similarly increase knee extensor strength. J Sports Sci 34:2018–2026. https://doi.org/10.1080/02640414.2016.1149607
Margaritelis NV, Theodorou AA, Baltzopoulos V, Maganaris CN, Paschalis V, Kyparos A, Nikolaidis MG (2015) Muscle damage and inflammation after eccentric exercise: can the repeated bout effect be removed? Physiol Rep 3:e12648. https://doi.org/10.14814/phy2.12648
Margaritelis NV, Theodorou AA, Kyparos A, Nikolaidis MG, Paschalis V (2019) Effect of body composition on redox homeostasis at rest and in response to exercise: the case of underfat women. J Sports Sci 37:1630–1637. https://doi.org/10.1080/02640414.2019.1578450
McHugh MP, Connolly DA, Eston RG, Gleim GW (1999) Exercise-induced muscle damage and potential mechanisms for the repeated bout effect. Sports Med 27:157–170. https://doi.org/10.2165/00007256-199927030-00002
Nishikawa KC, Lindstedt SL, LaStayo PC (2018) Basic science and clinical use of eccentric contractions: history and uncertainties. J Sport Health Sci 7:265–274. https://doi.org/10.1016/j.jshs.2018.06.002
Nosaka K, Newton M (2002) Concentric or eccentric training effect on eccentric exercise-induced muscle damage. Med Sci Sports Exerc 34:63–69. https://doi.org/10.1097/00005768-200201000-00011
Nosaka K, Clarkson PM, McGuiggin ME, Byrne JM (1991) Time course of muscle adaptation after high force eccentric exercise. Eur J Appl Physiol Occup Physiol 63:70–76. https://doi.org/10.1007/BF00760804
Nosaka K, Aldayel A, Jubeau M, Chen TC (2011) Muscle damage induced by electrical stimulation. Eur J Appl Physiol 111:2427–2437. https://doi.org/10.1007/s00421-011-2086-x
Paschalis V, Nikolaidis MG, Theodorou AA, Panayiotou G, Fatouros IG, Koutedakis Y, Jamurtas AZ (2011) A weekly bout of eccentric exercise is sufficient to induce health-promoting effects. Med Sci Sports Exerc 43:64–73. https://doi.org/10.1249/MSS.0b013e3181e91d90
Paschalis V et al (2013) Stair descending exercise using a novel automatic escalator: effects on muscle performance and health-related parameters. PLoS ONE 8:e56218. https://doi.org/10.1371/journal.pone.0056218
Penailillo L, Blazevich AJ, Nosaka K (2015) Muscle fascicle behavior during eccentric cycling and its relation to muscle soreness. Med Sci Sports Exerc 47:708–717. https://doi.org/10.1249/MSS.0000000000000473
Reeves ND, Narici MV (2003) Behavior of human muscle fascicles during shortening and lengthening contractions in vivo. J Appl Physiol (1985) 95:1090–1096. https://doi.org/10.1152/japplphysiol.01046.2002
Reeves ND, Maganaris CN, Longo S, Narici MV (2009) Differential adaptations to eccentric versus conventional resistance training in older humans. Exp Physiol 94:825–833. https://doi.org/10.1113/expphysiol.2009.046599
Schwane JA, Johnson SR, Vandenakker CB, Armstrong RB (1983) Delayed-onset muscular soreness and plasma CPK and LDH activities after downhill running. Med Sci Sports Exerc 15:51–56
Teague BN, Schwane JA (1995) Effect of intermittent eccentric contractions on symptoms of muscle microinjury. Med Sci Sports Exerc 27:1378–1384
Theodorou AA et al (2011) No effect of antioxidant supplementation on muscle performance and blood redox status adaptations to eccentric training. Am J Clin Nutr 93:1373–1383. https://doi.org/10.3945/ajcn.110.009266
Theodorou AA et al (2013) Stair descending exercise increases muscle strength in elderly males with chronic heart failure. BMC Res Notes 6:87. https://doi.org/10.1186/1756-0500-6-87
Walker S, Trezise J, Haff GG, Newton RU, Hakkinen K, Blazevich AJ (2020) Increased fascicle length but not patellar tendon stiffness after accentuated eccentric-load strength training in already-trained men. Eur J Appl Physiol. https://doi.org/10.1007/s00421-020-04462-x
Wareham NJ, Jakes RW, Rennie KL, Schuit J, Mitchell J, Hennings S, Day NE (2003) Validity and repeatability of a simple index derived from the short physical activity questionnaire used in the European Prospective Investigation into Cancer and Nutrition (EPIC) study. Public Health Nutr 6:407–413. https://doi.org/10.1079/PHN2002439
Wernbom M, Augustsson J, Thomee R (2007) The influence of frequency, intensity, volume and mode of strength training on whole muscle cross-sectional area in humans. Sports Med 37:225–264. https://doi.org/10.2165/00007256-200737030-00004
Westing SH, Cresswell AG, Thorstensson A (1991) Muscle activation during maximal voluntary eccentric and concentric knee extension. Eur J Appl Physiol Occup Physiol 62:104–108. https://doi.org/10.1007/bf00626764
Funding
None.
Author information
Authors and Affiliations
Contributions
PV and NMG conceived and designed research; MNV, TAA, PNC, KA, NMG, PV performed formal analysis and investigation; PV wrote the manuscript—original draft preparation. All authors read and approved the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethics approval
This study was performed in line with the principles of the Declaration of Helsinki. Approval was granted by the Ethics Committee of the local University (ERC-002/2019).
Consent to participate
Informed consent was obtained from all individual participants included in the study.
Consent for publication
No personal data are published.
Additional information
Communicated by Nicolas Place.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Margaritelis, N.V., Theodorou, A.A., Chatzinikolaou, P.N. et al. Eccentric exercise per se does not affect muscle damage biomarkers: early and late phase adaptations. Eur J Appl Physiol 121, 549–559 (2021). https://doi.org/10.1007/s00421-020-04528-w
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00421-020-04528-w
Keywords
- Concentric
- Eccentric
- Exercise
- Muscle damage
- Strength