Evidence for sensitized fatigue pathways in patients with chronic fatigue syndrome

Pain

Volumn 156, Issue 4, 2015, Pages 750-759

  Staud, Roland ^a   Mokthech, Meriem ^a   Price, Donald D ^b   Robinson, Michael E ^c  

^a Departments of Medicine   (United States)

^b Oral and Maxillofacial Surgery   (United States)

^c UNIVERSITY OF FLORIDA   (United States)

Author keywords

Chronic Fatigue; Dynamometer; Forearm Occlusion; Handgrip; Metabolites

Indexed keywords

ADULT; ARTICLE; CHRONIC FATIGUE SYNDROME; CLINICAL ARTICLE; CONTROLLED STUDY; EXERCISE TEST; FATIGUE; FEMALE; HAND GRIP; HEAT HYPERALGESIA; HUMAN; MALE; MECHANICAL HYPERALGESIA; MUSCLE METABOLISM; PRIORITY JOURNAL; QUANTITATIVE SENSORY TESTING; VISUAL ANALOG SCALE; ADVERSE EFFECTS; ANALYSIS OF VARIANCE; EXERCISE; FOREARM; HAND STRENGTH; HYPERALGESIA; PAIN; PAIN MEASUREMENT; PAIN THRESHOLD; PATHOPHYSIOLOGY; PHYSICAL STIMULATION; PHYSIOLOGY; PSYCHOPHYSICS;

ANALYSIS OF VARIANCE; EXERCISE TEST; FATIGUE; FATIGUE SYNDROME, CHRONIC; FEMALE; FOREARM; HAND STRENGTH; HUMANS; HYPERALGESIA; MALE; PAIN; PAIN MEASUREMENT; PAIN THRESHOLD; PHYSICAL EXERTION; PHYSICAL STIMULATION; PSYCHOPHYSICS;

EID: 85003051713     PISSN: 03043959     EISSN: 18726623     Source Type: Journal    
DOI: 10.1097/j.pain.0000000000000110     Document Type: Article

References (58)

1. Alam M, Smirk FH. Observations in man upon a blood pressure raising reflex arising from the voluntary muscles. J Physiol 1937;89:372 83.
2. Borg G. Borg s perceived exertion and pain scales. Champaign, IL: Human Kinetics, 1998. p. 1 120.
3. Cannon JG, Angel JB, Ball RW, Abad LW, Fagioli L, Komaroff AL. Acute phase responses and cytokine secretion in chronic fatigue syndrome. J Clin Immunol 1999;19:414 21.
4. Clauw DJ, Chrousos GP. Chronic pain and fatigue syndromes: overlapping clinical and neuroendocrine features and potential pathogenic mechanisms. Neuroimmunomodulation 1997;4:134 53.
5. Coderre TJ, Katz J. Peripheral and central hyperexcitability: differential signs and symptoms in persistent pain. Behav Brain Sci 1997;20: 404 19.
6. Connor M, Naves LA, McCleskey EW. Contrasting phenotypes of putative proprioceptive and nociceptive trigeminal neurons innervating jaw muscle in rat. Mol Pain 2005;1:31.
7. Cui J, McQuillan P, Momen A, Blaha C, Moradkhan R, Mascarenhas V, Hogeman C, Krishnan A, Sinoway LI. The role of the cyclooxygenase products in evoking sympathetic activation in exercise. Am J Physiol Heart Circ Physiol 2007;293:H1861 8.
8. Fukuda K, Straus SE, Hickie I, Sharpe MC, Dobbins JG, Komaroff A. The chronic fatigue syndrome: A comprehensive approach to its definition and study. International Chronic Fatigue Syndrome Study Group. Ann Intern Med 1994;121:953 9.
9. Fulle S, Mecocci P, Fano G, Vecchiet J, Vecchini A, Racciotti D, Cherubini A, Pizzigallo E, Vecchiet L, Senin U, Beal MF. Specific oxidative alterations in vastus lateralis muscle of patients with the diagnosis of chronic fatigue syndrome. Free Radic Biol Med 2000;29:1252 9.
10. Gibson H, Carroll N, Clague JE, Edwards RH. Exercise performance and fatiguability in patients with chronic fatigue syndrome. J NeurolNeurosurg Psychiatry 1993;56:993 8.
11. Gibson W, Arendt-Nielsen L, Taguchi T, Mizumura K, Graven-Nielsen T. Increased pain from muscle fascia following eccentric exercise: Animal and human findings. Exp Brain Res 2009;194:299 308.
12. Gupta S, Aggarwal S, See D, Starr A. Cytokine production by adherent and non-Adherent mononuclear cells in chronic fatigue syndrome. J Psychiatr Res 1997;31:149 56.
13. Hoheisel U, Unger T, Mense S. Excitatory and modulatory effects of inflammatory cytokines and neurotrophins onmechanosensitive group IV muscle afferents in the rat. Pain 2005;114:168 76.
14. Holgate ST, Komaroff AL, Mangan D, Wessely S. Chronic fatigue syndrome: understanding a complex illness. Nat Rev Neurosci 2011;12: 539 44.
15. Immke DC, McCleskey EW. Lactate enhances the acid-sensing Na1 channel on ischemia-sensing neurons. Nat Neurosci 2001;4:869 70.
16. Kaufman MP, Longhurst JC, Rybicki KJ, Wallach JH, Mitchell JH. Effects of static muscular contraction on impulse activity of groups III and IV afferents in cats. J Appl Physiol Respir Environ Exerc Physiol 1983;55: 105 12.
17. Kawasaki Y, Zhang L, Cheng JK, Ji RR. Cytokine mechanisms of central sensitization: distinct and overlapping role of interleukin-1beta, interleukin-6, and tumor necrosis factor-Alpha in regulating synaptic and neuronal activity in the superficial spinal cord. J Neurosci 2008;28: 5189 94.
18. Kent-Braun JA, Sharma KR, Weiner MW, Massie B, Miller RG. Central basis of muscle fatigue in chronic fatigue syndrome. Neurology 1993;43: 125 31.
19. Koltyn KF, Arbogast RW. Perception of pain after resistance exercise. Br J Sports Med 1998;32:20 4.
20. Kuratsune H, Yamaguti K, Takahashi M, Misaki H, Tagawa S, Kitani T. Acylcarnitine deficiency in chronic fatigue syndrome. Clin Infect Dis 1994; 18(suppl 1):S62 7.
21. Lane RJ, Barrett MC, Taylor DJ, Kemp GJ, Lodi R. Heterogeneity in chronic fatigue syndrome: evidence from magnetic resonance spectroscopy of muscle. Neuromuscul Disord 1998;8:204 9.
22. Latremoliere A, Woolf CJ. Central sensitization: A generator of pain hypersensitivity by central neural plasticity. J Pain 2009;10:895 926.
23. Light AR, Hughen RW, Zhang J, Rainier J, Liu Z, Lee J. Dorsal root ganglion neurons innervating skeletal muscle respond to physiological combinations of protons, ATP, and lactate mediated by ASIC, P2X, and TRPV1. J Neurophysiol 2008;100:1184 201.
24. Light AR, White AT, Hughen RW, Light KC. Moderate exercise Increases expression for sensory, adrenergic, and immune genes in chronic fatigue syndrome patients but not in normal subjects. J Pain 2009;10:1099 112.
25. McCully KK, Natelson BH, Iotti S, Sisto S, Leigh JS Jr. Reduced oxidative muscle metabolism in chronic fatigue syndrome. Muscle Nerve 1996;19: 621 5.
26. McCully KK, Smith S, Rajaei S, Leigh JS, Natelson BH. Blood flow and muscle metabolism in chronic fatigue syndrome. Clin Sci (Lond) 2003; 104:641 7.
27. McCully KK, Smith S, Rajaei S, Leigh JS, Natelson BH. Muscle metabolism with blood flow restriction in chronic fatigue syndrome. J Appl Physiol 2004;96:871 8.
28. Meeus M, Nijs J. Central sensitization: A biopsychosocial explanation for chronic widespread pain in patients with fibromyalgia and chronic fatigue syndrome. Clin Rheumatol 2007;26:465 73.
29. Meeus M, Nijs J, Huybrechts S, Truijen S. Evidence for generalized hyperalgesia in chronic fatigue syndrome: A case control study. Clin Rheumatol 2010;29:393 8.
30. Meeus M, Nijs J, Meirleir KD. Chronic musculoskeletal pain in patients with the chronic fatigue syndrome: A systematic review. Eur J Pain 2007; 11:377 86.
31. Mense S. Nervous outflow from skeletal muscle following chemical noxious stimulation. J Physiol (Lond) 1977;267:75 88.
32. Mense S, Schmidt RF. Activation of group IV afferent units from muscle by algesic agents. Brain Res 1974;72:305 10.
33. Molliver DC, Immke DC, Fierro L, Pare M, Rice FL, McCleskey EW. ASIC3, an acid-sensing ion channel, is expressed in metaboreceptive sensory neurons. Mol Pain 2005;1:35.
34. Moss RB, Mercandetti A, Vojdani A. TNF-Alpha and chronic fatigue syndrome. J Clin Immunol 1999;19:314 6.
35. Naves LA, McCleskey EW. An acid-sensing ion channel that detects ischemic pain. Braz J Med Biol Res 2005;38:1561 9.
36. Nicolay CW, Walker AL. Grip strength and endurance: influences of anthropometric variation, hand dominance, and gender. Int J Ind Ergonom 2006;36:605 10.
37. Nijs J, Meeus M, Van Oosterwijck J, Ickmans K, Moorkens G, Hans G, De Clerck LS. In the mind or in the brain? Scientific evidence for central sensitisation in chronic fatigue syndrome. Eur J Clin Invest 2012;42: 203 12.
38. Patarca-Montero R, Antoni M, Fletcher MA, Klimas NG. Cytokine and other immunologic markers in chronic fatigue syndrome and their relation to neuropsychological factors. Appl Neuropsychol 2001;8:51 64.
39. Pollak KA, Swenson JD, Vanhaitsma TA, Hughen RW, Jo D, Light KC, Schweinhardt P, Amann M, Light AR. Exogenously applied muscle metabolites synergistically evoke sensations of muscle fatigue and pain in human subjects. Exp Physiol 2014;99:368 80.
40. Price DD, Bush FM, Long S, Harkins SW. A comparison of pain measurement characteristics of mechanical visual analogue and simple numerical rating scales. PAIN 1994;56:217 26.
41. Price DD, Dubner R. Mechanisms of first and second pain in the peripheral and central nervous systems. J Invest Dermatol 1977;69:167 71.
42. Price DD, Hu JW, Dubner R, Gracely RH. Peripheral suppression of first pain and central summation of second pain evoked by noxious heat pulses. PAIN 1977;3:57 68.
43. Riley MS, O Brien CJ, McCluskey DR, Bell NP, Nicholls DP. Aerobic work capacity in patients with chronic fatigue syndrome. BMJ 1990;301: 953 6.
44. Rotto DM, Kaufman MP. Effect of metabolic products of muscular contraction on discharge of group III and IV afferents. J Appl Physiol (1985) 1988;64:2306 13.
45. Sargent C, Scroop GC, Nemeth PM, Burnet RB, Buckley JD. Maximal oxygen uptake and lactate metabolism are normal in chronic fatigue syndrome. Med Sci Sports Exerc 2002;34:51 6.
46. Staud R, Weyl EE, Bartley E, Price DD, Robinson ME. Analgesic and antihyperalgesic effects of muscle injections with lidocaine or saline in patients with fibromyalgia syndrome. Eur J Pain 2014;18:803 12.
47. Staud R, Weyl EE, Price DD, Robinson ME. Mechanical and heat hyperalgesia highly predict clinical pain intensity in patients with chronic musculoskeletal pain syndromes. J Pain 2012;13:725 35.
48. ter Wolbeek M, van Doornen LJP, Kavelaars A, van de Putte EM, Schedlowski M, Heijnen CJ. Longitudinal analysis of pro-And antiinflammatory cytokine production in severely fatigued adolescents. Brain Behav Immun 2007;21:1063 74.
49. Van Oosterwijck J, Nijs J, Meeus M, Lefever I, Huybrechts L, Lambrecht L, Paul L. Pain inhibition and postexertional malaise in myalgic encephalomyelitis/chronic fatigue syndrome: An experimental study. J Intern Med 2010;268:265 78.
50. Vecchiet J, Cipollone F, Falasca K, Mezzetti A, Pizzigallo E, Bucciarelli T, De Laurentis S, Affaitati G, De Cesare D, Giamberardino MA. Relationship between musculoskeletal symptoms and blood markers of oxidative stress in patients with chronic fatigue syndrome. Neurosci Lett 2003;335: 151 4.
51. Vecchiet L, Montanari G, Pizzigallo E, Iezzi S, de Bigontina P, Dragani L, Vecchiet J, Giamberardino MA. Sensory characterization of somatic parietal tissues in humans with chronic fatigue syndrome. Neurosci Lett 1996;208:117 20.
52. Waldmann R, Bassilana F, de WJ, Champigny G, Heurteaux C, Lazdunski M. Molecular cloning of a non-inactivating proton-gated Na1 channel specific for sensory neurons. J Biol Chem 1997;272:20975 8.
53. Waldmann R, Champigny G, Bassilana F, Heurteaux C, Lazdunski M. A proton-gated cation channel involved in acid-sensing.Nature 1997;386:173 7.
54. Whiteside A, Hansen S, Chaudhuri A. Exercise lowers pain threshold in chronic fatigue syndrome. PAIN 2004;109:497 9.
55. Wong R, Lopaschuk G, Zhu G, Walker D, Catellier D, Burton D, Teo K, Collins-Nakai R, Montague T. Skeletal muscle metabolism in the chronic fatigue syndrome. In vivo assessment by 31P nuclear magnetic resonance spectroscopy. Chest 1992;102:1716 22.
56. Yagi J, Wenk HN, Naves LA, McCleskey EW. Sustained currents through ASIC3 ion channels at the modest pH changes that occur during myocardial ischemia. Circ Res 2006;99:501 9.
57. Yarnitsky D, Simone DA, Dotson RM, Cline MA, Ochoa JL. Single C nociceptor responses and psychophysical parameters of evoked pain: effect of rate of rise of heat stimuli in humans. J Physiol 1992;450: 581 92.
58. Yeomans DC, Proudfit HK. Nociceptive responses to high and low rates of noxious cutaneous heating are mediated by different nociceptors in the rat: electrophysiological evidence. PAIN 1996;68:141 50.