Advertisement

The Journal of Physiological Sciences

, Volume 66, Issue 1, pp 43–52 | Cite as

Delayed onset muscle soreness: Involvement of neurotrophic factors

  • Kazue MizumuraEmail author
  • Toru Taguchi
Mini-review

Abstract

Delayed-onset muscle soreness (DOMS) is quite a common consequence of unaccustomed strenuous exercise, especially exercise containing eccentric contraction (lengthening contraction, LC). Its typical sign is mechanical hyperalgesia (tenderness and movement related pain). Its cause has been commonly believed to be micro-damage of the muscle and subsequent inflammation. Here we present a brief historical overview of the damage-inflammation theory followed by a discussion of our new findings. Different from previous observations, we have observed mechanical hyperalgesia in rats 1–3 days after LC without any apparent microscopic damage of the muscle or signs of inflammation. With our model we have found that two pathways are involved in inducing mechanical hyperalgesia after LC: activation of the B2 bradykinin receptor–nerve growth factor (NGF) pathway and activation of the COX-2-glial cell line-derived neurotrophic factor (GDNF) pathway. These neurotrophic factors were produced by muscle fibers and/or satellite cells. This means that muscle fiber damage is not essential, although it is sufficient, for induction of DOMS, instead, NGF and GDNF produced by muscle fibers/satellite cells play crucial roles in DOMS.

Keywords

Delayed-onset muscle soreness Exercise Mechanical hyperalgesia Nerve growth factor Glial cell line-derived neurotrophic factor 

References

  1. 1.
    Asmussen E (1956) Observations on experimental muscular soreness. Acta Rheum Scand 2:109–116CrossRefPubMedGoogle Scholar
  2. 2.
    Armstrong RB (1984) Mechanisms of exercise-induced delayed onset muscular soreness: a brief review. Med Sci Sports Exerc 16:529–538PubMedGoogle Scholar
  3. 3.
    Newham DJ (1988) The consequences of eccentric contractions and their relationship to delayed onset muscle pain. Eur J Appl Physiol 57:353–359CrossRefGoogle Scholar
  4. 4.
    Graven-Nielsen T, Arendt-Nielsen L (2003) Induction and assessment of muscle pain, referred pain, and muscular hyperalgesia. Curr Pain Headache Rep 7:443–451CrossRefPubMedGoogle Scholar
  5. 5.
    Hayashi K, Ozaki N, Kawakita K, Itoh K, Mizumura K, Furukawa K, Yasui M, Hori K, Yi S-Q, Yamaguchi T, Sugiura Y (2011) Involvement of NGF in the rat model of persistent muscle pain associated with taut band. J Pain 12:1059–1068CrossRefPubMedGoogle Scholar
  6. 6.
    Sluka KA, Danielson J, Rasmussen L, DaSilva LF (2012) Exercise-induced pain requires NMDA receptor activation in the medullary raphe nuclei. Med Sci Sports Exerc 44:420–427PubMedCentralCrossRefPubMedGoogle Scholar
  7. 7.
    Chapman D, Newton M, Sacco P, Nosaka K (2006) Greater muscle damage induced by fast versus slow velocity eccentric exercise. Int J Sports Med 27:591–598CrossRefPubMedGoogle Scholar
  8. 8.
    Mori T, Agata N, Itoh Y, Miyazu-Inoue M, Sokabe M, Taguchi T, Kawakam K (2014) Stretch speed-dependent myofiber damage and functional deficits in rat skeletal muscle induced by lengthening contraction. Physiol Rep 2(11):e12213PubMedCentralCrossRefPubMedGoogle Scholar
  9. 9.
    Cheung K, Hume P, Maxwell L (2003) Delayed-onset muscle soreness: treatment strategies and performance factors. Sports Med 33:145–164CrossRefPubMedGoogle Scholar
  10. 10.
    Friden J, Lieber RL (1992) Structural and mechanical basis of exercise-induced muscle injury. Med Sci Sports Exerc 24:521–530CrossRefPubMedGoogle Scholar
  11. 11.
    Smith LL (1991) Acute inflammation: the underlying mechanism in delayed-onset muscle soreness. Med Sci Sports Exerc 23:542–551PubMedGoogle Scholar
  12. 12.
    Hough T (1902) Ergographic studies in muscular soreness. Am J Physiol 7:76–92Google Scholar
  13. 13.
    Newham DJ, Mills KR, Quigley BM, Edwards RHT (1983) Pain and fatigue after concentric and eccentric muscle contractions. Clin Sci 64:55–62CrossRefPubMedGoogle Scholar
  14. 14.
    Surmeier DJ, Reiner A, Levine MS, Ariano MA (1993) Are neostriatal dopamine receptors co-localized? Trends Neurosci 16:299–305CrossRefPubMedGoogle Scholar
  15. 15.
    Newham DJ, McPhail G, Mills KR, Edwards RHT (1983) Ultrastructural changes after concentric and eccentric contractions of human muscle. J Neurol Sci 61:109–122CrossRefPubMedGoogle Scholar
  16. 16.
    Friden J, Sjostrom M, Ekblom B (1981) A morphological study of delayed muscle soreness. Experientia 37:506–507CrossRefPubMedGoogle Scholar
  17. 17.
    Armstrong RB, Oglive RW, Schwane JA (1983) Eccentric exercise-induced injury to rat skeletal muscle. J Appl Physiol 54:80–93PubMedGoogle Scholar
  18. 18.
    Head SI, Bakker AJ, Liangas G (2004) EDL and soleus muscles of the C57BL6J/dy2j laminin-alpha 2-deficient dystrophic mouse are not vulnerable to eccentric contractions. Exp Physiol 89:531–539CrossRefPubMedGoogle Scholar
  19. 19.
    Friden J, Sjostrom M, Ekblom B (1983) Myofibrillar damage following intense eccentric exercise in man. Int J Sports Med 4(3):170–176CrossRefPubMedGoogle Scholar
  20. 20.
    Treede RD, Davis KD, Campbell JN, Raja SN (1992) The plasticity of cutaneous hyperalgesia during sympathetic ganglion blockade in patients with neuropathic pain. Brain 115:607–621CrossRefPubMedGoogle Scholar
  21. 21.
    MacIntyre DL, Sorichter S, Mair J, Berg A, McKenzie DC (2001) Markers of inflammation and myofibrillar proteins following eccentric exercise in humans. Eur J Appl Physiol 84:180–186CrossRefPubMedGoogle Scholar
  22. 22.
    Pizza FX, Koh TJ, McGregor SJ, Brooks SV (2002) Muscle inflammatory cells after passive stretches, isometric contractions, and lengthening contractions. J Appl Physiol 92:1873–1878CrossRefPubMedGoogle Scholar
  23. 23.
    Buford TW, Cooke MB, Shelmadine BD, Hudson GM, Redd L, Willoughby DS (2009) Effects of eccentric treadmill exercise on inflammatory gene expression in human skeletal muscle. Appl Physiol Nutr Metab 34:745–753CrossRefPubMedGoogle Scholar
  24. 24.
    Crameri RM, Aagaard P, Qvortrup K, Langberg H, Olesen J, Kjaer M (2007) Myofibre damage in human skeletal muscle: effects of electrical stimulation versus voluntary contraction. J Physiol 583:365–380PubMedCentralCrossRefPubMedGoogle Scholar
  25. 25.
    Hayashi K, Abe M, Yamanaka A, Mizumura K, Taguchi T (2015) Degenerative histological alteration is not required for the induction of muscular mechanical hyperalgesia after lengthening contraction in rats. J Physiol Sci 65(suppl):S277Google Scholar
  26. 26.
    Nosaka K, Aldayel A, Jubeau M, Chen TC (2011) Muscle damage induced by electrical stimulation. Eur J Appl Physiol 111:2427–2437CrossRefPubMedGoogle Scholar
  27. 27.
    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 112:429–438CrossRefPubMedGoogle Scholar
  28. 28.
    Malm C, Sjodin TL, Sjoberg B, Lenkei R, Renstrom 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 556:983–1000PubMedCentralCrossRefPubMedGoogle Scholar
  29. 29.
    Singla N, Desjardins PJ, Cosca EB, Parulan C, Arriaga A, Poole KC, Batz DM, Chang PD (2015) Delayed-onset muscle soreness: a pilot study to assess analgesic study design features. Pain 156:1036–1045PubMedCentralPubMedGoogle Scholar
  30. 30.
    Schwane JA, Watrous BG, Johnson SR, Armstrong RB (1983) Is lactic acid related to delayed-onset muscle soreness? Phys Sportsmed 11:124–131Google Scholar
  31. 31.
    De Vries HA (1966) Quantitative electromyographic investigation of the spasm theory of muscle pain. Am J Phys Med 45:119–134CrossRefPubMedGoogle Scholar
  32. 32.
    Lieber RL, Friden J (1988) Selective damage of fast glycolytic muscle fibres with eccentric contraction of the rabbit tibialis anterior. Acta Physiol Scand 133:587–588CrossRefPubMedGoogle Scholar
  33. 33.
    Hikida RS, Staron RS, Hagerman C, Sherman WM, Costill DL (1983) Muscle fiber necrosis associated with human marathon runners. J Neurol Sci 59:185–203CrossRefPubMedGoogle Scholar
  34. 34.
    Meltzer HY, Kuncl RW, Yang V (1976) Incidence of Z band streaming and myofibrillar disruptions in skeletal muscle from healthy young people. Neurology 26:853–857CrossRefPubMedGoogle Scholar
  35. 35.
    Taguchi T, Matsuda T, Tamura R, Sato J, Mizumura K (2005) Muscular mechanical hyperalgesia revealed by behavioural pain test and c-Fos expression in the spinal dorsal horn after eccentric contraction in rats. J Physiol 564:259–268PubMedCentralCrossRefPubMedGoogle Scholar
  36. 36.
    Itoh K, Kawakita K (2002) Effect of indomethacin on the development of eccentric exercise-induced localized sensitive region in the fascia of the rabbit. Jpn J Physiol 52:173–180CrossRefPubMedGoogle Scholar
  37. 37.
    Fujii Y, Ozaki N, Taguchi T, Mizumura K, Sugiura Y (2008) TRP channels and ASICs mediate mechanical hyperalgesia in models of inflammatory muscle pain and delayed-onset muscle soreness. Pain 140:292–304CrossRefPubMedGoogle Scholar
  38. 38.
    Ota H, Katanosaka K, Murase S, Kashio M, Tominaga M, Mizumura K (2013) TRPV1 and TRPV4 play pivotal roles in delayed-onset muscle soreness. PLoS ONE 8:e65751PubMedCentralCrossRefPubMedGoogle Scholar
  39. 39.
    Fischer AA (1987) Pressure algometry over normal muscles. Standard values, validity and reproducibility of pressure threshold. Pain 30:115–126CrossRefPubMedGoogle Scholar
  40. 40.
    Andersen H, Arendt-Nielsen L, Danneskiold-Samsoe B, Graven-Nielsen T (2006) Pressure pain sensitivity and hardness along human normal and sensitized muscle. Somatosens Mot Res 23:97–109CrossRefPubMedGoogle Scholar
  41. 41.
    Takahashi K, Taguchi T, Itoh K, Okada K, Kawakita K, Mizumura K (2005) Influence of surface anesthesia on the pressure pain threshold measured with different-sized probes. Somatosens Mot Res 22:299–305CrossRefPubMedGoogle Scholar
  42. 42.
    Takahashi K, Mizumura K (2004) 3-D finite element analysis of stresses in the epidermis and the muscle given by a transcutaneous pressure. Jpn J Physiol 54(Suppl):S175Google Scholar
  43. 43.
    Finocchietti S, Takahashi K, Okada K, Watanabe Y, Graven-Nielsen T, Mizumura K (2013) Deformation and pressure propagation in deep-tissue duiring mechanical painful pressure stimulation. Med Biol Eng Comput 51:113–122CrossRefPubMedGoogle Scholar
  44. 44.
    Finocchietti S, Andresen T, Arendt-Nielsen L, Graven-Nielsen T (2012) Pain evoked by pressure stimulation on the tibia bone—influence of probe diameter on tissue stress and strain. Eur J Pain 16:534–542CrossRefPubMedGoogle Scholar
  45. 45.
    Nasu T, Taguchi T, Mizumura K (2010) Persistent deep mechanical hyperalgesia induced by repeated cold stress in rats. Eur J Pain 14:236–244CrossRefPubMedGoogle Scholar
  46. 46.
    Taguchi T, Matsuda T, Mizumura K (2007) Change with age in muscular mechanical hyperalgesia after lengthening contraction in rats. Neurosci Res 57:331–338CrossRefPubMedGoogle Scholar
  47. 47.
    Murase S, Terazawa E, Hirate K, Yamanaka H, Kanda H, Noguchi K, Ota H, Queme F, Taguchi T, Mizumura K (2013) Upregulated glial cell line-derived neurotrophic factor through cyclooxygenase-2 activation in the muscle is required for mechanical hyperalgesia after exercise in rats. J Physiol 591:3035–3048PubMedCentralCrossRefPubMedGoogle Scholar
  48. 48.
    Hunt SP, Pini A, Evan G (1987) Induction of c-fos-like protein in spinal cord neurons following sensory stimulation. Nature 328:632–634CrossRefPubMedGoogle Scholar
  49. 49.
    Sugiura Y, Lee CL, Perl ER (1986) Central projections of identified, unmyelinated (C) afferent fibers innervating mammalian skin. Science 234:358–361CrossRefPubMedGoogle Scholar
  50. 50.
    Ling LJ, Honda T, Shimada Y, Ozaki N, Shiraishi Y, Sugiura Y (2003) Central projection of unmyelinated (C) primary afferent fibers from gastrocnemius muscle in the guinea pig. J Comput Neurol 461(2):140–150CrossRefGoogle Scholar
  51. 51.
    Graven-Nielsen T, Mense S (2001) The peripheral apparatus of muscle pain: evidence from animal and human studies. Clin J Pain 17:2–10CrossRefPubMedGoogle Scholar
  52. 52.
    Taguchi T, Sato J, Mizumura K (2005) Augmented mechanical response of muscle thin-fiber sensory receptors recorded from rat muscle-nerve preparations in vitro after eccentric contraction. J Neurophysiol 94:2822–2831CrossRefPubMedGoogle Scholar
  53. 53.
    Queme F, Taguchi T, Mizumura K, Graven-Nielsen T (2013) Muscular heat and mechanical pain sensitivity after lengthening contraction in humans and animals. J Pain 14:1425–1436CrossRefPubMedGoogle Scholar
  54. 54.
    Weerakkody NS, Whitehead NP, Canny BJ, Gregory JE, Proske U (2001) Large-fiber mechanoreceptors contribute to muscle soreness after eccentric exercise. J Pain 2:209–219CrossRefPubMedGoogle Scholar
  55. 55.
    Weerakkody NS, Percival P, Hickey MW, Morgan DL, Gregory JE, Canny BJ, Proske U (2003) Effects of local pressure and vibration on muscle pain from eccentric exercise and hypertonic saline. Pain 105:425–435CrossRefPubMedGoogle Scholar
  56. 56.
    Gibson W, Arendt-Nielsen L, Taguchi T, Mizumura K, Graven-Nielsen T (2009) Increased pain from muscle fascia following eccentric exercise: animal and human findings. Exp Brain Res 194:299–308CrossRefPubMedGoogle Scholar
  57. 57.
    Nagy JI, Iversen LL, Goedert M, Chapman D, Hunt SP (1983) Dose-dependent effects of capsaicin on primary sensory neurons in the neonatal rat. J Neurosci 3:399–406PubMedGoogle Scholar
  58. 58.
    Kubo A, Koyama M, Tamura R, Takagishi Y, Murase S, Mizumura K (2012) Absence of mechanical hyperalgesia after exercise (delayed-onset muscle soreness) in neonatally capsaicin-treated rats. Neurosci Res 73:56–60CrossRefPubMedGoogle Scholar
  59. 59.
    Boix F, Rosenborg L, Hilgenfeldt U, Knardahl S (2002) Contraction-related factors affect the concentration of a kallidin-like peptide in rat muscle tissue. J Physiol 544:127–136PubMedCentralCrossRefPubMedGoogle Scholar
  60. 60.
    Wilson SR, Boix F, Holm A, Molander P, Lundanes E, Greibrokk T (2005) Determination of bradykinin and arg-bradykinin in rat muscle tissue by microdialysis and capillary column-switching liquid chromatography with mass spectrometric detection. J Sep Sci 28:1751–1758CrossRefPubMedGoogle Scholar
  61. 61.
    Koda H, Mizumura K (2002) Sensitization to mechanical stimulation by inflammatory mediators, by second messengers possibly mediating these sensitizing effects, and by mild burn in canine visceral nociceptors in vitro. J Neurophysiol 87:2043–2051PubMedGoogle Scholar
  62. 62.
    Mense S, Meyer H (1988) Bradykinin-induced modulation of the response behaviour of different types of feline group III and IV muscle receptors. J Physiol 398:49–63PubMedCentralCrossRefPubMedGoogle Scholar
  63. 63.
    Mizumura K, Sugiura T, Katanosaka K, Banik RK, Kozaki Y (2009) Excitation and sensitization of nociceptors by bradykinin: what do we know– Exp Brain Res 196:53–65CrossRefPubMedGoogle Scholar
  64. 64.
    Murase S, Terazawa E, Queme F, Ota H, Matsuda T, Hirate K, Kozaki Y, Katanosaka K, Taguchi T, Mizumura K (2010) Bradykinin and nerve-growth factor play pivotal roles in muscular mechanical hyperalgesia after exercise (delayed-onset muscle soreness). J Neurosci 30:3752–3761CrossRefPubMedGoogle Scholar
  65. 65.
    Turrini P, Gaetano C, Antonelli A, Capogrossi MC, Aloe L (2002) Nerve-growth factor induces angiogenic activity in a mouse model of hindlimb ischemia. Neurosci Lett 323:109–112CrossRefPubMedGoogle Scholar
  66. 66.
    Amano T, Yamakuni T, Okabe N, Sakimura K, Takahashi Y (1991) Production of nerve-growth factor in rat skeletal muscle. Neurosci Lett 132:5–7CrossRefPubMedGoogle Scholar
  67. 67.
    Andersen H, Arendt-Nielsen L, Svensson P, Danneskiold-Samsoe B, Graven-Nielsen T (2008) Spatial and temporal aspects of muscle hyperalgesia induced by nerve-growth factor in humans. Exp Brain Res 191:371–382CrossRefPubMedGoogle Scholar
  68. 68.
    Tomiya A, Aizawa T, Nagatomi R, Sensui H, Kokubun S (2004) Myofibers express IL-6 after eccentric exercise. Am J Sports Med 32:503–508CrossRefPubMedGoogle Scholar
  69. 69.
    Harrington AW, Ginty DD (2013) Long-distance retrograde neurotrophic factor signalling in neurons. Nat Rev Neurosci 14:177–187CrossRefPubMedGoogle Scholar
  70. 70.
    Di Castro A, Drew LJ, Wood JN, Cesare P (2006) Modulation of sensory neuron mechanotransduction by PKC- and nerve-growth factor-dependent pathways. Proc Natl Acad Sci USA 103:4699–4704PubMedCentralCrossRefPubMedGoogle Scholar
  71. 71.
    Malik-Hall M, Dina OA, Levine JD (2005) Primary afferent nociceptor mechanisms mediating NGF-induced mechanical hyperalgesia. Eur J Neurosci 21(12):3387–3394CrossRefPubMedGoogle Scholar
  72. 72.
    Bonnington JK, McNaughton PA (2003) Signalling pathways involved in the sensitisation of mouse nociceptive neurones by nerve-growth factor. J Physiol 551:433–446PubMedCentralCrossRefPubMedGoogle Scholar
  73. 73.
    Zhang X, Huang J, McNaughton PA (2005) NGF rapidly increases membrane expression of TRPV1 heat-gated ion channels. EMBO J 24:4211–4223PubMedCentralCrossRefPubMedGoogle Scholar
  74. 74.
    Zhu W, Oxford GS (2007) Phosphoinositide-3-kinase and mitogen activated protein kinase signaling pathways mediate acute NGF sensitization of TRPV1. Mol Cell Neurosci 34:689–700PubMedCentralCrossRefPubMedGoogle Scholar
  75. 75.
    Murase S, Yamanaka Y, Kanda H, Mizumura K (2012) COX-2, nerve-growth factor (NGF) and glial cell-derived neurotrophic factor (GDNF), which play pivotal roles in delayed-onset muscle soreness (DOMS), are produced by exercised skeletal muscle. J Physiol Sci 62(suppl):S179Google Scholar
  76. 76.
    Murase S, Kato K, Taguchi T, Mizumura K (2014) Glial cell line-derived neurotrophic factor sensitized the mechanical response of muscular thin-fiber afferents in rats. Eur J Pain 18:629–638CrossRefPubMedGoogle Scholar
  77. 77.
    Sugimoto Y, Narumiya S (2007) Prostaglandin E receptors. J Biol Chem 282:11613–11617CrossRefPubMedGoogle Scholar
  78. 78.
    Ota H, Katanosaka K, Murase S, Narumiya S, Mizumura K (2015) Contribution of EP2 receptor to generation of delayed-onset muscle soreness. J Physiol Sci 65(Suppl):S234Google Scholar
  79. 79.
    Mizumura K, Taguchi T, Murase S (2014) Facilitation of mechanical response of muscle nociceptors after exercise: Involvement of neurotrophic factors. In: Graven-Nielsen T, Arendt-Nielsen L (eds) Musculoskeletal pain: Basic mechanisms and implications, IASP Press, Washington DC, pp 223–235Google Scholar
  80. 80.
    Priestley JV, Michael GJ, Averill S, Liu M, Willmott N (2002) Regulation of nociceptive neurons by nerve-growth factor and glial cell line derived neurotrophic factor. Can J Physiol Pharmacol 80:495–505CrossRefPubMedGoogle Scholar
  81. 81.
    McHugh MP, Connolly DA, Eston RG, Gleim GW (1999) Exercise-induced muscle damage and potential mechanisms for the repeated bout effect. Sports Med 27:157–170CrossRefPubMedGoogle Scholar
  82. 82.
    McHugh MP (2003) Recent advances in the understanding of the repeated bout effect: the protective effect against muscle damage from a single bout of eccentric exercise. Scand J Med Sci Sports 13:88–97CrossRefPubMedGoogle Scholar
  83. 83.
    Urai H, Murase S, Mizumura K (2013) Decreased nerve-growth factor upregulation is a mechanism for reduced mechanical hyperalgesia after the second bout of exercise in rats. Scand J Med Sci Sports 23:e96–101CrossRefPubMedGoogle Scholar
  84. 84.
    Itoh K, Okada K, Kawakita K (2004) A proposed experimental model of myofascial trigger points in human muscle after slow eccentric exercise. Acupunct Med 22:2–12CrossRefPubMedGoogle Scholar
  85. 85.
    Lau WY, Blazevich AJ, Newton MJ, Wu SS, Nosaka K (2015) Changes in electrical pain threshold of fascia and muscle after initial and secondary bouts of elbow flexor eccentric exercise. Eur J Appl Physiol 115:959–968CrossRefPubMedGoogle Scholar
  86. 86.
    Tesarz J, Hoheisel U, Wiedenhofer B, Mense S (2011) Sensory innervation of the thoracolumbar fascia in rats and humans. Neuroscience 194:302–308CrossRefPubMedGoogle Scholar
  87. 87.
    Taguchi T, Yasui M, Kubo A, Abe M, Kiyama H, Yamanaka A et al (2013) Nociception originating from the crural fascia in rats. Pain 154:1103–1114CrossRefPubMedGoogle Scholar
  88. 88.
    Chen HL, Nosaka K, Pearce AJ, Chen TC (2012) Two maximal isometric contractions attenuate the magnitude of eccentric exercise-induced muscle damage. Appl Physiol Nutr Metab 37:680–689CrossRefPubMedGoogle Scholar
  89. 89.
    Chen HL, Nosaka K, Chen TC (2011) Muscle damage protection by low-intensity eccentric contractions remains for 2 weeks but not 3 weeks. Eur J Appl Physiol 112:555–565CrossRefPubMedGoogle Scholar
  90. 90.
    Chen TC, Tseng WC, Huang GL, Chen HL, Tseng KW, Nosaka K (2013) Low-intensity eccentric contractions attenuate muscle damage induced by subsequent maximal eccentric exercise of the knee extensors in the elderly. Eur J Appl Physiol 113:1005–1015CrossRefPubMedGoogle Scholar
  91. 91.
    Urakawa S, Takamoto K, Nakamura T, Sakai S, Matsuda T, Taguchi T, Mizumura K, Ono T (2015) Manual therapy ameliorates delayed-onset muscle soreness and alters muscle metabolites in rats. Physiol Rep 3(2):e12279PubMedCentralCrossRefPubMedGoogle Scholar
  92. 92.
    Farr T, Nottle C, Nosaka K, Sacco P (2002) The effects of therapeutic massage on delayed-onset muscle soreness and muscle function following downhill walking. J Sci Med Sport 5:297–306CrossRefPubMedGoogle Scholar

Copyright information

© The Physiological Society of Japan and Springer Japan 2015

Authors and Affiliations

  1. 1.Department of Physical Therapy, College of Life and Health SciencesChubu UniversityKasugaiJapan
  2. 2.Department of Neuroscience II, Research Institute of Environmental MedicineNagoya UniversityNagoyaJapan

Personalised recommendations