PAIN
Volume 151, Issue 2 , Pages 460-466 , November 2010

Neuropathic pain-like alterations in muscle nociceptor function associated with vibration-induced muscle pain

  • Xiaojie Chen

      Affiliations

    • Department Oral and Maxillofacial Surgery, University of California San Francisco, San Francisco, CA 94143, USA
  • ,
  • Paul G. Green

      Affiliations

    • Department Oral and Maxillofacial Surgery, University of California San Francisco, San Francisco, CA 94143, USA
  • ,
  • Jon D. Levine

      Affiliations

    • Department Oral and Maxillofacial Surgery, University of California San Francisco, San Francisco, CA 94143, USA
    • Department of Medicine, University of California San Francisco, San Francisco, CA 94143, USA
    • Corresponding Author InformationCorresponding author. Address: Department of Medicine and Oral and Maxillofacial Surgery, University of California San Francisco, San Francisco, CA 94143, USA. Tel.: +1 415 476 5108; fax: +1 415 476 6305.

Received 21 April 2010 ,Revised 3 August 2010 ,Accepted 4 August 2010.

References 

  1. Al-Shatti T, Barr AE, Safadi FF, Amin M, Barbe MF. Increase in inflammatory cytokines in median nerves in a rat model of repetitive motion injury. J Neuroimmunol. 2005;167:13–22
  2. Alessandri-Haber N, Dina OA, Yeh JJ, Parada CA, Reichling DB, Levine JD. Transient receptor potential vanilloid 4 is essential in chemotherapy-induced neuropathic pain in the rat. J Neurosci. 2004;24:4444–4452
  3. Alessandri-Haber N, Yeh JJ, Boyd AE, Parada CA, Chen X, Reichling DB, et al. Hypotonicity induces TRPV4-mediated nociception in rat. Neuron. 2003;39:497–511
  4. Aley KO, Levine JD. Multiple receptors involved in peripheral alpha 2, mu, and A1 antinociception, tolerance, and withdrawal. J Neurosci. 1997;17:735–744
  5. Arruda JL, Colburn RW, Rickman AJ, Rutkowski MD, DeLeo JA. Increase of interleukin-6 mRNA in the spinal cord following peripheral nerve injury in the rat: potential role of IL-6 in neuropathic pain. Brain Res Mol Brain Res. 1998;62:228–235
  6. Baron R. Neuropathic pain: a clinical perspective. Handb Exp Pharmacol. 2009;3–30
  7. Bermejo PE, Anciones B. Neuromodulators and therapeutic targets in neuropathic pain: from molecules to man. CNS Neurol Disord Drug Targets. 2009;8:175–183
  8. Borg-Stein J, Zaremski JL, Hanford MA. New concepts in the assessment and treatment of regional musculoskeletal pain and sports injury. PM R. 2009;1:744–754
  9. Bovenzi M, Giannini F, Rossi S. Vibration-induced multifocal neuropathy in forestry workers: electrophysiological findings in relation to vibration exposure and finger circulation. Int Arch Occup Environ Health. 2000;73:519–527
  10. Brenn D, Richter F, Schaible HG. Sensitization of unmyelinated sensory fibers of the joint nerve to mechanical stimuli by interleukin-6 in the rat: An inflammatory mechanism of joint pain. Arthritis & Rheumatism. 2007;56:351–359
  11. Burton AR, Birznieks I, Bolton PS, Henderson LA, Macefield VG. Effects of deep and superficial experimentally induced acute pain on muscle sympathetic nerve activity in human subjects. J Physiol. 2009;587:183–193
  12. Cederlund R, Iwarsson S, Lundborg G. Hand function tests and questions on hand symptoms as related to the Stockholm workshop scales for diagnosis of hand-arm vibration syndrome. J Hand Surg Br. 2003;28:165–171
  13. Cederlund R, Iwarsson S, Lundborg G. Quality of life in Swedish workers exposed to hand-arm vibration. Occup Ther Int. 2007;14:156–169
  14. Chang KY, Ho ST, Yu HS. Vibration induced neurophysiological and electron microscopical changes in rat peripheral nerves. Occup Environ Med. 1994;51:130–135
  15. Chang PF, Arendt-Nielsen L, Graven-Nielsen T, Svensson P, Chen AC. Comparative EEG activation to skin pain and muscle pain induced by capsaicin injection. Int J Psychophysiol. 2004;51:117–126
  16. Chen X, Tanner K, Levine JD. Mechanical sensitization of cutaneous C-fiber nociceptors by prostaglandin E2 in the rat. Neurosci Lett. 1999;267:105–108
  17. Chetter IC, Kent PJ, Kester RC. The hand arm vibration syndrome: a review. Cardiovasc Surg. 1998;6:1–9
  18. Dahlin LB, Lundborg G. Vibration-induced hand problems: role of the peripheral nerves in the pathophysiology. Scand J Plast Reconstr Surg Hand Surg. 2001;35:225–232
  19. Datta Munshi JS, Ojha J, Mittal AK. Succinic dehydrogenase activity of the respiratory muscles of a fresh-water teleost, Bagarius bagarius (Ham.) (Sisoridae, Pisces). Acta Anat (Basel). 1975;92:543–559
  20. Dina OA, Parada CA, Yeh J, Chen X, McCarter GC, Levine JD. Integrin signaling in inflammatory and neuropathic pain in the rat. Eur J Neurosci. 2004;19:634–642
  21. Dina OA, Green PG, Levine JD. Role of interleukin-6 in chronic muscle hyperalgesic priming. Neuroscience. 2008;152:521–525
  22. Dina OA, Joseph EK, Levine JD, Green PG. Mechanisms Mediating Vibration-induced Chronic Musculoskeletal Pain Analyzed in the Rat. J Pain. 2010;167:369–377
  23. Eatock RA, Corey DP, Hudspeth AJ. Adaptation of mechanoelectrical transduction in hair cells of the bullfrog’s sacculus. J Neurosci. 1987;7:2821–2836
  24. Fallon KE. Musculoskeletal injuries in the ultramarathon: the 1990 Westfield Sydney to Melbourne run. Br J Sports Med. 1996;30:319–323
  25. Finsterer J. Mitochondrial neuropathy. Clin Neurol Neurosurg. 2005;107:181–186
  26. Flatters SJ, Fox AJ, Dickenson AH. Spinal interleukin-6 (IL-6) inhibits nociceptive transmission following neuropathy. Brain Res. 2003;984:54–62
  27. Friden J. Vibration damage to the hand: clinical presentation, prognosis and length and severity of vibration required. J Hand Surg Br. 2001;26:471–474
  28. Gemne G. Diagnostics of hand-arm system disorders in workers who use vibrating tools. Occup Environ Med. 1997;54:90–95
  29. Govindaraju SR, Curry BD, Bain JL, Riley DA. Comparison of continuous and intermittent vibration effects on rat-tail artery and nerve. Muscle Nerve. 2006;34:197–204
  30. Haanpaa ML, Backonja MM, Bennett MI, Bouhassira D, Cruccu G, Hansson PT, et al. Assessment of neuropathic pain in primary care. Am J Med. 2009;122:S13–21
  31. Hirata M, Sakakibara H. Sensory nerve conduction velocities of median, ulnar and radial nerves in patients with vibration syndrome. Int Arch Occup Environ Health. 2007;80:273–280
  32. Ho ST, Yu HS. Ultrastructural changes of the peripheral nerve induced by vibration: an experimental study. Br J Ind Med. 1989;46:157–164
  33. Hoheisel U, Unger T, Mense S. Excitatory and modulatory effects of inflammatory cytokines and neurotrophins on mechanosensitive group IV muscle afferents in the rat. Pain. 2005;114:168–176
  34. House R, Wills M, Liss G, Switzer-McIntyre S, Manno M, Lander L. Upper extremity disability in workers with hand-arm vibration syndrome. Occup Med (Lond). 2009;59:167–173
  35. Hughes JM, Wirth O, Krajnak K, Miller R, Flavahan S, Berkowitz DE, et al. Increased oxidant activity mediates vascular dysfunction in vibration injury. J Pharmacol Exp Ther. 2009;328:223–230
  36. Juntunen J, Matikainen E, Seppalainen AM, Laine A. Peripheral neuropathy and vibration syndrome. A clinical and neurophysiological study of 103 patients. Int Arch Occup Environ Health. 1983;52:17–24
  37. Khasar SG, Gold MS, Dastmalchi S, Levine JD. Selective attenuation of mu-opioid receptor-mediated effects in rat sensory neurons by intrathecal administration of antisense oligodeoxynucleotides. Neurosci Lett. 1996;218:17–20
  38. Khasar SG, Gold MS, Levine JD. A tetrodotoxin-resistant sodium current mediates inflammatory pain in the rat. Neurosci Lett. 1998;256:17–20
  39. Kidd BL. What are the mechanisms of regional musculoskeletal pain?. Baillieres Best Pract Res Clin Rheumatol. 1999;13:217–230
  40. Kiguchi N, Maeda T, Kobayashi Y, Saika F, Kishioka S. Involvement of inflammatory mediators in neuropathic pain caused by vincristine. Int Rev Neurobiol. 2009;85:179–190
  41. Koike H, Watanabe H, Inukai A, Iijima M, Mori K, Hattori N, et al. Myopathy in thiamine deficiency: analysis of a case. J Neurol Sci. 2006;249:175–179
  42. Koike H, Iijima M, Mori K, Yamamoto M, Hattori N, Watanabe H, et al. Neuropathic pain correlates with myelinated fibre loss and cytokine profile in POEMS syndrome. J Neurol Neurosurg Psychiatry. 2008;79:1171–1179
  43. Krajnak K, Miller GR, Waugh S, Johnson C, Li S, Kashon ML. Characterization of frequency-dependent responses of the vascular system to repetitive vibration. J Occup Environ Med. 2010;52:584–594
  44. Krishnan K, Adams PT. Bilateral orbital tumors and lacrimal gland involvement in Waldenstrom’s macroglobulinemia. Eur J Haematol. 1995;55:205–206
  45. Kurozawa Y, Nasu Y. Current perception thresholds in vibration-induced neuropathy. Arch Environ Health. 2001;56:254–256
  46. Latko WA, Armstrong TJ, Franzblau A, Ulin SS, Werner RA, Albers JW. Cross-sectional study of the relationship between repetitive work and the prevalence of upper limb musculoskeletal disorders. Am J Ind Med. 1999;36:248–259
  47. Lee KM, Jeon SM, Cho HJ. Interleukin-6 induces microglial CX3CR1 expression in the spinal cord after peripheral nerve injury through the activation of p38 MAPK. Eur J Pain 2009;In Press, Corrected Proof:.
  48. Leschnik M, Weikel J, Mostl K, Revilla-Fernandez S, Wodak E, Bago Z, et al. Subclinical infection with avian influenza A (H5N1) virus in cats. Emerg Infect Dis. 2007;13:243–247
  49. Lindenlaub T, Sommer C. Cytokines in sural nerve biopsies from inflammatory and non-inflammatory neuropathies. Acta Neuropathol. 2003;105:593–602
  50. Loewenstein WR, Mendelson M. Components of receptor adaptation in a pacinian corpuscle. J Physiol. 1965;177:377–397
  51. Loffredo MA, Yan JG, Kao D, Zhang LL, Matloub HS, Riley DA. Persistent reduction of conduction velocity and myelinated axon damage in vibrated rat tail nerves. Muscle Nerve. 2009;39:770–775
  52. Lotti M, Moretto A. Organophosphate-induced delayed polyneuropathy. Toxicol Rev. 2005;24:37–49
  53. Ludwig J, Binder A, Steinmann J, Wasner G, Baron R. Cytokine expression in serum and cerebrospinal fluid in non-inflammatory polyneuropathies. J Neurol Neurosurg Psychiatry. 2008;79:1268–1273
  54. Lundborg G, Dahlin LB, Danielsen N, Hansson HA, Necking LE, Pyykko I. Intraneural edema following exposure to vibration. Scand J Work Environ Health. 1987;13:326–329
  55. Ma W, Quirion R. Up-regulation of interleukin-6 induced by prostaglandin E from invading macrophages following nerve injury: an in vivo and in vitro study. J Neurochem. 2005;93:664–673
  56. Melhorn JM. Cumulative trauma disorders and repetitive strain injuries. The future. Clin Orthop Relat Res. 1998;107–126
  57. Mense S. Muscle pain: mechanisms and clinical significance. Dtsch Arztebl Int. 2008;105:214–219
  58. Meyer RA, Campbell JN. Myelinated nociceptive afferents account for the hyperalgesia that follows a burn to the hand. Science. 1981;213:1527–1529
  59. Meyer RA, Campbell JN, Raja SN. Peripheral neural mechanisms of nociception. In:  Wall PD,  Melzack R editor. Textbook of Pain. Edinburgh: Churchill Livingstone; 1994;p. 13–44
  60. Mirbod SM, Inaba R, Iwata H. Operating vibrating tools and prevalence of subjective complaints in vibration syndrome. Cent Eur J Public Health. 1995;3:97–102
  61. Misawa A, Yasuda M. Combined chemotherapy with weekly paclitaxel and carboplatin for recurrent and refractory epithelial ovarian cancer–phase I study. Gan To Kagaku Ryoho. 2006;33:1445–1452
  62. Nasu T, Taguchi T, Mizumura K. Persistent deep mechanical hyperalgesia induced by repeated cold stress in rats. Eur J Pain. 2010;14:236–244
  63. Papir-Kricheli D, Frey J, Laufer R, Gilon C, Chorev M, Selinger Z, et al. Behavioural effects of receptor-specific substance P agonists. Pain. 1987;31:263–276
  64. Parada CA, Yeh JJ, Joseph EK, Levine JD. Tumor necrosis factor receptor type-1 in sensory neurons contributes to induction of chronic enhancement of inflammatory hyperalgesia in rat. Eur J Neurosci. 2003;17:1847–1852
  65. Parada CA, Yeh JJ, Reichling DB, Levine JD. Transient attenuation of protein kinase Cepsilon can terminate a chronic hyperalgesic state in the rat. Neuroscience. 2003;120:219–226
  66. Pritchard MH, Pugh N, Wright I, Brownlee M. A vascular basis for repetitive strain injury. Rheumatology (Oxford). 1999;38:636–639
  67. Radwin RG, Armstrong TJ, Vanbergeijk E. Vibration exposure for selected power hand tools used in automobile assembly. Am Ind Hyg Assoc J. 1990;51:510–518
  68. Rodriguez-Revenga L, Madrigal I, Pagonabarraga J, Xuncla M, Badenas C, Kulisevsky J, et al. Penetrance of FMR1 premutation associated pathologies in fragile X syndrome families. Eur J Hum Genet. 2009;17:1359–1362
  69. Ronin DI, Wu YC, Sahgal V, MacLean IC. Intractable muscle pain syndrome, osteomalacia, and axonopathy in long-term use of phenytoin. Arch Phys Med Rehabil. 1991;72:755–758
  70. Schneider W, Slugg RM, Turnquist BP, Meyer RA, Campbell JN. An electromechanical stimulator system for neurophysiological and psychophysical studies of pain. J Neurosci Methods. 1995;60:61–68
  71. Serra J, Campero M, Ochoa J, Bostock H. Activity-dependent slowing of conduction differentiates functional subtypes of C fibres innervating human skin. J Physiol. 1999;515:799–811
  72. Stromberg T, Dahlin LB, Lundborg G. Hand problems in 100 vibration-exposed symptomatic male workers. J Hand Surg Br. 1996;21:315–319
  73. Summer GJ, Puntillo KA, Miaskowski C, Dina OA, Green PG, Levine JD. TrkA and PKC-epsilon in thermal burn-induced mechanical hyperalgesia in the rat. J Pain. 2006;7:884–891
  74. Summer GJ, Romero-Sandoval EA, Bogen O, Dina OA, Khasar SG, Levine JD. Proinflammatory cytokines mediating burn-injury pain. Pain. 2008;135:98–107
  75. Svensson P, Graven-Nielsen T. Craniofacial muscle pain: review of mechanisms and clinical manifestations. J Orofac Pain. 2001;15:117–145
  76. Takeuchi T, Futatsuka M, Imanishi H, Yamada S. Pathological changes observed in the finger biopsy of patients with vibration-induced white finger. Scand J Work Environ Health. 1986;12:280–283
  77. Takeuchi T, Takeya M, Imanishi H. Ultrastructural changes in peripheral nerves of the fingers of three vibration-exposed persons with Raynaud’s phenomenon. Scand J Work Environ Health. 1988;14:31–35
  78. Torkkeli PH, Sekizawa S, French AS. Inactivation of voltage-activated Na(+) currents contributes to different adaptation properties of paired mechanosensory neurons. J Neurophysiol. 2001;85:1595–1602
  79. Torre V, Ashmore JF, Lamb TD, Menini A. Transduction and adaptation in sensory receptor cells. J Neurosci. 1995;15:7757–7768
  80. Treede RD, Meyer RA, Raja SN, Campbell JN. Evidence for two different heat transduction mechanisms in nociceptive primary afferents innervating monkey skin. J Physiol. 1995;483:747–758
  81. Wahlstrom J, Burstrom L, Hagberg M, Lundstrom R, Nilsson T. Musculoskeletal symptoms among young male workers and associations with exposure to hand-arm vibration and ergonomic stressors. Int Arch Occup Environ Health. 2008;81:595–602
  82. Wang Y, Nesbitt JE, Fuentes NL, Fuller GM. Molecular cloning and characterization of the rat liver IL-6 signal transducing molecule, gp130. Genomics. 1992;14:666–672
  83. Yassi A. Repetitive strain injuries. Lancet. 1997;349:943–947

PII: S0304-3959(10)00472-0

doi: 10.1016/j.pain.2010.08.004

PAIN
Volume 151, Issue 2 , Pages 460-466 , November 2010