One night of total sleep deprivation promotes a state of generalized hyperalgesia: A surrogate pain model to study the relationship of insomnia and pain

Pain

Volumn 154, Issue 9, 2013, Pages 1613-1621

  Schuh Hofer, Sigrid ^a,b   Wodarski, Rachel ^c   Pfau, Doreen B ^a   Caspani, Ombretta ^a   Magerl, Walter ^a   Kennedy, Jeffrey D ^c   Treede, Rolf Detlef ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b UNIVERSITY OF TÜBINGEN   (Germany)

^c ELI LILLY AND COMPANY   (United States)

Author keywords

Central sensitization; Descending pain control; Fibromyalgia syndrome; Hyperalgesia; Quantitative sensory testing; Sleep deprivation

Indexed keywords

ADULT; ALLODYNIA; ARTICLE; CROSSOVER PROCEDURE; FEMALE; HEAT INTOLERANCE; HEAT SENSATION; HUMAN; HUMAN EXPERIMENT; HYPERALGESIA; INSOMNIA; NOCICEPTION; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; SCORING SYSTEM; SLEEP DEPRIVATION; SLEEP PATTERN; SOMATOSENSORY SYSTEM; SOMNOLENCE; TEMPORAL SUMMATION;

CENTRAL SENSITIZATION; DESCENDING PAIN CONTROL; FIBROMYALGIA SYNDROME; HYPERALGESIA; QUANTITATIVE SENSORY TESTING; SLEEP DEPRIVATION;

ADULT; ANXIETY; CROSS-OVER STUDIES; FEMALE; HUMANS; HYPERALGESIA; MALE; PAIN; PAIN MEASUREMENT; PAIN PERCEPTION; PAIN THRESHOLD; PHYSICAL STIMULATION; SLEEP DEPRIVATION; YOUNG ADULT;

EID: 84881668356     PISSN: 03043959     EISSN: 18726623     Source Type: Journal    
DOI: 10.1016/j.pain.2013.04.046     Document Type: Article

References (106)

1. V.C. Abad, P.S. Sarinas, and C. Guilleminault Sleep and rheumatologic disorders Sleep Med Rev 12 2008 211 228
2. S.M. Alsaadi, J.H. McAuley, J.M. Hush, and C.G. Maher Prevalence of sleep disturbance in patients with low back pain Eur Spine J 20 2011 737 743
3. M.L. Andersen, S. Silva, R. Kawakami, and S. Tufik The effects of sleep deprivation and sleep recovery on pain thresholds of rats with chronic pain Sleep Sci 2 2009 82 87
4. P. Araujo, R. Mazaro-Costa, S. Tufik, and M.L. Andersen Impact of sex on hyperalgesia induced by sleep loss Horm Behav 59 2011 174 179
5. T. Arima, P. Sevensson, C. Rasmussen, K.D. Nielsen, A.M. Drewes, and L. Arendt-Nielsen The relationship between selective sleep deprivation, nocturnal jaw-muscle activity and pain in healthy men J Oral Rehabil 28 2001 140 148
6. W. Asakura, K. Matsumoto, H. Ohta, and H. Watanabe REM sleep deprivation decreases apomorphine-induced stimulation of locomotor activity but not stereotyped behavior in mice Gen Pharmacol 23 1992 337 341
7. M. Asikainen, J. Toppila, L. Alanko, D.J. Ward, D. Stenberg, and T. Porkka-Heiskanen Sleep deprivation increases brain serotonin turnover in the rat Neuroreport 8 1997 1577 1582
8. C.G. Bachmann, R. Rolke, U. Scheidt, C. Stadelmann, M. Sommer, G. Pavlakovic, S. Happe, R.D. Treede, and W. Paulus Thermal hypoaesthesia differentiates secondary restless legs syndrome associated with small fibre neuropathy from primary restless legs syndrome Brain 133 2010 762 770
9. H. Bahouq, F. Allali, H. Rkain, I. Hmamouchi, and N. Hajjaj-Hassouni Prevalence and severity of insomnia in chronic low back pain patients Rheumatol Int 33 2013 1277 1281
10. S. Banks, and D.F. Dinges Behavioral and physiological consequences of sleep restriction J Clin Sleep Med 3 2007 519 528
11. R. Basheer, M. Magner, R.W. McCarley, and P.J. Shiromani REM sleep deprivation increases the levels of tyrosine hydroxylase and norepinephrine transporter mRNA in the locus coeruleus Mol Brain Res 57 1998 235 240
12. A.T. Beck, C.H. Ward, M. Mendelson, J. Mock, and J. Erbaugh An inventory for measuring depression Arch Gen Psychiatry 4 1961 561 571
13. B.M. Bergmann, L.S. Seiden, C.A. Landis, M.A. Gilliland, and A. Rechtschaffen Sleep deprivation in the rat: XVIII. Regional brain levels of monoamines and their metabolites Sleep 17 1994 583 589
14. P.J. Bieling, M.M. Antony, and R.P. Swinson The state-trait anxiety inventory, trait version: structure and content re-examined Behav Res Ther 36 1998 777 788
15. A. Binder, M. Stengel, R. Maag, G. Wasner, R. Schoch, F. Moosig, B. Schommer, and R. Baron Pain in oxaliplatin-induced neuropathy - sensitisation in the peripheral and central nociceptive system Eur J Cancer 43 2007 2658 2663
16. K. Blumenstiel, A. Gerhardt, R. Rolke, C. Bieber, J. Tesarz, H.C. Friederich, W. Eich, and R.D. Treede Quantitative sensory testing profiles in chronic back pain are distinct from those in fibromyalgia Clin J Pain 27 2011 682 690
17. A.A. Borbély, P. Steigrad, and I. Tobler Effect of sleep deprivation on brain serotonin in the rat Behav Brain Res 1 1980 205 210
18. D. Buffum, T. Koetters, M. Cho, L. Macera, S.M. Paul, C. West, B. Aouizerat, L. Dunn, M. Dodd, K. Lee, B. Cooper, W. Wara, P. Swift, and C. Miaskowski The effects of pain, gender, and age on sleep/wake and circadian rhythm parameters in oncology patients at the initiation of radiation therapy J Pain 12 2011 390 400
19. D.J. Buysse, C.F. Reynolds 3rd, T.H. Monk, S.R. Berman, and D.J. Kupfer The Pittsburgh sleep quality index: a new instrument for psychiatric practice and research Psychiatry Res 28 1989 193 213
20. K.K. Cheng, and R.M. Yeung Impact of mood disturbance, sleep disturbance, fatigue and pain among patients receiving cancer therapy Eur J Cancer Care 22 2013 70 78
21. M. Chennaoui, F. Sauvet, C. Drogou, P. Van Beers, C. Langrume, and M. Guillard Effect of one night of sleep loss on changes in tumor necrosis factor alpha (TNF-alpha) levels in healthy men Cytokine 56 2011 318 324
22. J.C. Cole, D. Dubois, and M. Kosinski Use of patient-reported sleep measures in clinical trials of pain treatment: a literature review and synthesis of current sleep measures and a conceptual model of sleep disturbance in pain Clin Ther 29 2007 2580 2588
23. B.K. Coombes, L. Bisset, and B. Vicenzino Thermal hyperalgesia distinguishes those with severe pain and disability in unilateral lateral epicondylalgia Clin J Pain 28 2012 595 601
24. R.A. de Oliveira, G.M. Cunha, K.D. Borges, G.S. de Bruin, E.A. dos Santos-Filho, G.S. Viana, and V.M. de Bruin The effect of venlafaxine on behaviour, body weight and striatal monoamine levels on sleep-deprived female rats Pharmacol Biochem Behav 79 2004 499 506
25. J.A. Desmeules, C. Cedraschi, E. Rapiti, E. Baumgartner, A. Finckh, P. Cohen, P. Dayer, and T.L. Vischer Neurophysiologic evidence for a central sensitization in patients with fibromyalgia Arthritis Rheum 48 2003 1420 1429
26. A.M. Drewes, P. Rössel, L. Arendt-Nielsen, K.D. Nielsen, L.M. Hansen, L. Birket-Smith, and K. Stengaard-Pedersen Sleepiness does not modulate experimental joint pain in healthy volunteers Scand J Rheumatol 26 1997 399 400
27. A. Dhruva, S.M. Paul, B.A. Cooper, K. Lee, C. West, B.E. Aouizerat, L.B. Dunn, P.S. Swift, W. Wara, and C. Miaskowski A longitudinal study of measures of objective and subjective sleep disturbance in patients with breast cancer before, during, and after radiation therapy J Pain Symptom Manage 44 2012 215 228
28. ® 137 2008 202 207
29. P. Fadda, A. Tortorella, and W. Fratta Sleep deprivation decreases mu and delta opioid receptor binding in the rat limbic system Neurosci Lett 129 1991 315 317
30. S.M. Farooqui, J.W. Brock, and J. Zhou Changes in monoamines and their metabolite concentrations in REM sleep-deprived rat forebrain nuclei Pharmacol Biochem Behav 54 1996 385 391
31. I. Fißmer, T. Klein, W. Magerl, R.D. Treede, P.K. Zahn, and E.M. Pogatzki-Zahn Modality-specific somatosensory changes in a human surrogate model of postoperative pain Anesthesiology 115 2011 387 397
32. K. Garrett, A. Dhruva, T. Koetters, C. West, S.M. Paul, L.B. Dunn, B.E. Aouizerat, B.A. Cooper, M. Dodd, K. Lee, W. Wara, P. Swift, and C. Miaskowski Differences in sleep disturbance and fatigue between patients with breast and prostate cancer at the initiation of radiation therapy J Pain Symptom Manage 42 2011 239 250
33. ® 152 2011 548 556
34. R.H. Gerner, R.M. Post, J.C. Gilling, and W.E. Bunney Jr. Biological and behavioural effects of one night's sleep deprivation in depressed patients and normals J Psychiatr Res 15 1979 21 40
35. ® 153 2012 765 774
36. E. Gröne, A. Crispin, J. Fleckenstein, D. Irnich, R.-D. Treede, and P.M. Lang Test order of quantitative sensory testing facilitates mechanical hyperalgesia in healthy volunteers J Pain 13 2012 73 80
37. B. Gustorff, S. Anzenhofer, T. Sycha, S. Lehr, and H.G. Kress The sunburn pain model: the stability of primary and secondary hyperalgesia over 10 hours in a crossover setting Anesth Analg 98 2004 173 177
38. ® 119 2005 56 64
39. M. Haack, E. Sanchez, and J.M. Mullington Elevated inflammatory markers in response to prolonged sleep restriction are associated with increased pain experience in healthy volunteers Sleep 30 2007 1145 1152
40. ® 145 2009 136 141
41. M. Haack, J. Scott-Sutherland, G. Santangelo, N.S. Simpson, N. Sethna, and J.M. Mullington Pain sensitivity and modulation in primary insomnia Eur J Pain 16 2012 522 533
42. M.T. Harvey, R.H. Kline, M.E. May, A.C. Roberts, M.G. Valdovinos, R.G. Wiley, and C.H. Kennedy Parametric analysis of thermal preference following sleep deprivation in the rat Neurosci Lett 485 2010 98 101
43. D.C. Hipólide, K.M. Moreira, K.B. Barlow, A.A. Wilson, J.N. Nobrega, and S. Tufik Distinct effects of sleep deprivation on binding to norepinephrine and serotonin transporters in rat brain Prog Neuropsychopharmacol Biol Psychiatry 29 2005 297 303
44. D.C. Hipólide, S. Tufik, R. Raymond, and J.N. Nobrega Heterogeneous effects of rapid eye movement sleep deprivation on binding to alpha- and beta-adrenergic receptor subtypes in rat brain Neuroscience 86 1998 977 987
45. I.M. Hurtig, R.I. Raak, S.A. Kendall, B. Gerdle, and L.K. Wahren Quantitative sensory testing in fibromyalgia patients and in healthy subjects: identification of subgroups Clin J Pain 17 2001 316 322
46. M.R. Irwin, R. Olmstead, C. Carrillo, N. Sadeghi, J.D. Fitzgerald, V.K. Ranganath, and P.M. Nicassio Sleep loss exacerbates fatigue, depression, and pain in rheumatoid arthritis Sleep 35 2012 537 543
47. P. Jennum, A.M. Drewes, A. Andreasen, and K.D. Nielsen Sleep and other symptoms in primary fibromyalgia and in healthy controls J Rheumatol 20 1993 1756 1759
48. ® 101 2003 229 235
49. B.L. Kennedy, J.J. Schwab, R.L. Morris, and G. Beldia Assessment of state and trait anxiety in subjects with anxiety and depressive disorders Psychiatr Q 72 2001 263 276
50. W.D. Killgore Effects of sleep deprivation on cognition Prog Brain Res 185 2010 105 129
51. ® 115 2005 227 233
52. ® 152 2011 818 824
53. J.M. Krueger, J.A. Majde, and D.M. Rector Cytokines in immune function and sleep regulation Handb Clin Neurol 98 2011 229 240
54. A. Korszun, E.A. Young, N.C. Engleberg, C.B. Brucksch, J.F. Greden, and L.A. Crofford Use of actigraphy for monitoring sleep and activity levels in patients with fibromyalgia and depression J Psychosom Res 52 2002 439 443
55. ® 68 1996 375 383
56. B. Kundermann, J. Spernal, M.T. Huber, J.C. Krieg, and S. Lautenbacher Sleep deprivation affects thermal pain thresholds but not somatosensory thresholds in healthy volunteers Psychosomat Med 66 2004 932 937
57. B. Kundermann, J.C. Krieg, W. Schreiber, and S. Lautenbacher The effect of sleep deprivation on pain Pain Res Manage 9 2004 25 32
58. C.A. Landis Sleep, pain, fibromyalgia and chronic fatigue syndrome Handb Clin Neurol 98 2011 613 637
59. P.C. Langley, C. Van Litsenburg, J.C. Cappelleri, and D. Carroll The burden associated with neuropathic pain in Western Europe J Med Econ 16 2013 85 95
60. G.J. Lavigne, A. Nashed, C. Manzini, and M.C. Carra Does sleep differ among patients with common musculoskeletal pain disorders? Curr Rheumatol Rep 13 2011 535 542
61. M.J. Lentz, C.A. Landis, J. Rothermel, and J.L.F. Shaver Effects of selective slow wave sleep disruption on musculoskeletal pain and fatigue in middle-aged women J Rheumatol 26 1999 1586 1592
62. ® 151 2010 220 225
63. M. Mackiewicz, P.J. Sollars, M.D. Ogilvie, and A.I. Pack Modulation of IL-1 beta gene expression in the rat CNS during sleep deprivation Neuroreport 7 1996 529 533
64. ® 151 2010 598 605
65. ® 150 2010 439 450
66. B.N. Mallick Singh A.REM sleep loss increases brain excitability: role of noradrenaline and its mechanism of action Sleep Med Rev 15 2011 165 178
67. B.N. Mallick, S. Singh, and A. Singh Mechanism of noradrenaline-induced stimulation of Na-K ATPase activity in the rat brain: implications on REM sleep deprivation-induced increase in brain excitability Mol Cell Biochem 336 2010 3 16
68. M. Marty, S. Rozenberg, B. Duplan, P. Thomas, B. Duquesnoy, and F. Allaert Section Rachis de la Société Française de Rhumatologie. Quality of sleep in patients with chronic low back pain: a case-control study Eur Spine J 17 2008 839 844
69. M.E. May, M.T. Harvey, M.G. Valdovinos, R.H. Kline, R.G. Wiley, and C.H. Kennedy Nociceptor and age specific effects of REM sleep deprivation induced hyperalgesia Behav Brain Res 159 2005 89 94
70. J.D. Minkel, S. Banks, O. Htaik, M.C. Moreta, C.W. Jones, E.L. McGlinchey, N.S. Simpson, and D.F. Dinges Sleep deprivation and stressors: evidence for elevated negative affect in response to mild stressors when sleep deprived Emotion 12 2012 1015 1020
71. H. Moldofsky, P. Scarisbrick, R. England, and H. Smythe Musculosketal symptoms and non-REM sleep disturbance in patients with "fibrositis syndrome" and healthy subjects Psychosomat Med 37 1975 341 351
72. H. Moldofsky, and P. Scarisbrick Induction of neurasthenic musculoskeletal pain syndrome by selective sleep stage deprivation Psychosomat Med 38 1976 35 44
73. C. Morin, M.C. Bushnell, M.B. Luskin, and A.D. Craig Disruption of thermal perception in a multiple sclerosis patient with central pain Clin J Pain 18 2002 191 195
74. D.C. Nascimento, M.L. Andersen, D.C. Hipolide, J.N. Nobrega, and S. Tufik Pain hypersensitivity induced by paradoxical sleep deprivation is not due to altered binding to brain mu-opioid receptors Behav Brain Res 178 2007 216 220
75. S.A. Older, D.F. Battafarano, C.L. Danning, J.A. Ward, E.P. Grady, S. Derman, and I.J. Russell The effects of delta wave sleep interruption on pain thresholds and fibromyalgia-like symptoms in healthy subjects; correlations with insulin-like growth factor I J Rheumatol 25 1998 1180 1186
76. S.H. Onen, A. Alloui, A. Eschalier, and C. Dubray Vocalization thresholds related to noxious paw pressure are decreased by paradoxical sleep deprivation and increased after sleep recovery in rat Neurosci Lett 291 2000 25 28
77. S.H. Onen, A. Alloui, D. Jourdan, A. Eschalier, and C. Dubray Effects of rapid eye movement (REM) sleep deprivation on pain sensitivity in the rat Brain Res 900 2001 261 267
78. S.H. Onen, A. Alloui, A. Gross, A. Eschallier, and C. Dubray The effects of total sleep deprivation, selective sleep interruption and sleep recovery on pain tolerance thresholds in healthy subjects J Sleep Res 10 2001 35 42
79. ® 147 2009 72 83
80. M. Rizzi, P. Sarzi-Puttini, F. Atzeni, F. Capsoni, A. Andreoli, M. Pecis, S. Colombo, M. Carrabba, and M. Sergi Cyclic alternating pattern: a new marker of sleep alteration in patients with fibromyalgia? J Rheumatol 31 2004 1193 1199
81. T. Roehrs, M. Hyde, B. Blaisdell, M. Greenwald, and T. Roth Sleep loss and REM sleep loss are hyperalgesic Sleep 29 2006 145 151
82. S. Roizenblatt, H. Moldofsky, A.A. Benedito-Silva, and S. Tufik Alpha sleep characteristics in fibromyalgia Arthritis Rheum 44 2001 222 230
83. S. Roizenblatt, N.S. Neto, and S. Tufik Sleep disorders and fibromyalgia Curr Pain Headache Rep 15 2011 347 357
84. ® 123 2006 231 243
85. M.T. Smith, P.J. Quartana, R.M. Okonkwo, and A. Nasir Mechanisms by which sleep disturbance contributes to osteoarthritis pain: a conceptual model Curr Pain Headache Rep 13 2009 447 454
86. M.T. Smith, R.R. Edwards, D.U. McCann, and J.A. Haythornthwaite The effects of sleep deprivation on pain inhibition and spontaneous pain in women Sleep 30 2007 494 505
87. M.T. Smith, M.L. Perlis, M.S. Smith, D.E. Giles, and T.P. Carmody Sleep quality and presleep arousal in chronic pain J Behav Med 23 2000 1 13
88. C.D. Spielberger, R.L. Gorsuch, and R.E. Lushene Manual for the state-trait anxiety inventory 1970 Consulting Psychologists Press Palo Alto, CA
89. N.K. Tang, C.E. Goodchild, A.N. Sanborn, J. Howard, and P.M. Salkovskis Deciphering the temporal link between pain and sleep in a heterogeneous chronic pain patient sample: a multilevel daily process study Sleep 35 2012 675 687A
90. R.M. Taylor-Gjevre, J.A. Gjevre, B. Nair, R. Skomro, and H.J. Lim Components of sleep quality and sleep fragmentation in rheumatoid arthritis and osteoarthritis Musculoskelet Care 9 2011 152 159
91. A. Theadom, M. Cropley, and K.L. Humphrey Exploring the role of sleep and coping in quality of life in fibromyalgia J Psychosomat Res 62 2007 145 151
92. ® 148 2010 36 42
93. R.D. Treede, R.A. Meyer, S.N. Raja, and J.N. Campbell Peripheral and central mechanisms of cutaneous hyperalgesia Prog Neurobiol 38 1992 397 421
94. K. Tsuchiya, M. Toru, and T. Kobayashi Sleep deprivation: changes of monoamines and acetylcholine in rat brain Life Sci 8 1969 867 873
95. A.T. van de Water, J. Eadie, and D.A. Hurley Investigation of sleep disturbance in chronic low back pain: an age- and gender-matched case-control study over a 7-night period Man Ther 16 2011 550 556
96. G. Wasner, J. Schattschneider, A. Binder, and R. Baron Topical menthol - a human model for cold pain by activation and sensitization of C nociceptors Brain 127 2004 1159 1171
97. H. Wei, B. Hao, J.L. Huang, A.N. Ma, X.Y. Li, Y.X. Wang, and A. Pertovaara Intrathecal administration of a gap junction decoupler, an inhibitor of Na(+)-K(+)-2Cl(-) cotransporter or a GABA(A) receptor agonist attenuates mechanical pain hypersensitivity induced by REM sleep deprivation in the rat Pharmacol Biochem Behav 97 2010 377 383
98. H. Wei, A. Ma, Y.X. Wang, and A. Pertovaara Role of spinal 5-HT receptors in cutaneous hypersensitivity induced by REM sleep deprivation Pharmacol Res 57 2008 469 475
99. H. Wei, W. Zhao, Y.X. Wang, and A. Pertovaara Pain-related behavior following REM sleep deprivation in the rat: influence of peripheral nerve injury, spinal glutamatergic receptors and nitric oxide Brain Res 1148 2007 105 112
100. W. Wesemann, N. Weiner, M. Rotsch, and E. Schulz Serotonin binding in rat brain: circadian rhythm and effect of sleep deprivation J Neural Transm (Suppl.) 18 1983 287 294
101. W. Wesemann, and N. Weiner Regulation of cerebral serotonin binding and metabolism in sleep-deprived rats Behav Brain Res 6 1982 79 84
102. W. Wesemann, M. Rotsch, E. Schulz, and P. Zöfel Circadian rhythm of serotonin binding in rat brain - II. Influence of sleep deprivation and imipramine Chronobiol Int 3 1986 141 146
103. W.D. Willis Jr. Central nervous system mechanisms for pain modulation Appl Neurophysiol 48 1985 153 165
104. A. Xu, E. Sakurai, A. Kuramasu, J. Zhang, J. Li, N. Okamura, D. Zhang, T. Yoshikawa, T. Watanabe, and K. Yanai Roles of hypothalamic subgroup histamine and orexin neurons on behavioral responses to sleep deprivation induced by the treadmill method in adolescent rats J Pharmacol Sci 114 2010 444 453
105. S. Yehuda, B. Sredni, R.L. Carasso, and D. Kenigsbuch-Sredni REM sleep deprivation in rats results in inflammation and interleukin-17 elevation J Interferon Cytokine Res 29 2009 393 398
106. D.C. Zelman, N.A. Brandenburg, and M. Gore Sleep impairment in patients with painful diabetic peripheral neuropathy Clin J Pain 22 2006 681 685