PAIN
Volume 143, Issue 3 , Pages 172-178 , June 2009

Deficiency in endogenous modulation of prolonged heat pain in patients with Irritable Bowel Syndrome and Temporomandibular Disorder

  • Christopher D. King

      Affiliations

    • Department of Community Dentistry & Behavioral Science, University of Florida College of Dentistry, 1329 SW 16th Street, Suite 5180, PO Box 103628, Gainesville, FL 32610-3628, USA
    • Comprehensive Center for Pain Research, University of Florida College of Dentistry, 1329 SW 16th St., Suite 5180, PO Box 103628, Gainesville, FL 32610-3628, USA
    • Corresponding Author InformationCorresponding author. Address: Department of Community Dentistry & Behavioral Science, University of Florida College of Dentistry, 1329 SW 16th St., Suite 5180, PO Box 103628, Gainesville, FL 32610-3628, USA. Tel.: +1 352 273 5971; fax: +1 352 273 5985.
  • ,
  • Fong Wong

      Affiliations

    • Department of Prosthodontics, University of Florida College of Dentistry, 1329 SW 16th St., Suite 5180, PO Box 103628, Gainesville, FL 32610-3628, USA
  • ,
  • Tom Currie

      Affiliations

    • Department of Prosthodontics, University of Florida College of Dentistry, 1329 SW 16th St., Suite 5180, PO Box 103628, Gainesville, FL 32610-3628, USA
  • ,
  • Andre P. Mauderli

      Affiliations

    • Department of Prosthodontics, University of Florida College of Dentistry, 1329 SW 16th St., Suite 5180, PO Box 103628, Gainesville, FL 32610-3628, USA
    • Comprehensive Center for Pain Research, University of Florida College of Dentistry, 1329 SW 16th St., Suite 5180, PO Box 103628, Gainesville, FL 32610-3628, USA
  • ,
  • Roger B. Fillingim

      Affiliations

    • Department of Community Dentistry & Behavioral Science, University of Florida College of Dentistry, 1329 SW 16th Street, Suite 5180, PO Box 103628, Gainesville, FL 32610-3628, USA
    • Comprehensive Center for Pain Research, University of Florida College of Dentistry, 1329 SW 16th St., Suite 5180, PO Box 103628, Gainesville, FL 32610-3628, USA
  • ,
  • Joseph L. Riley 3rd

      Affiliations

    • Department of Community Dentistry & Behavioral Science, University of Florida College of Dentistry, 1329 SW 16th Street, Suite 5180, PO Box 103628, Gainesville, FL 32610-3628, USA
    • Comprehensive Center for Pain Research, University of Florida College of Dentistry, 1329 SW 16th St., Suite 5180, PO Box 103628, Gainesville, FL 32610-3628, USA

Received 5 August 2008 ,Revised 28 October 2008 ,Accepted 1 December 2008.

References 

  1. Berman SM, Naliboff BD, Suyenobu B, Labus JS, Stains J, Ohning G, et al. Reduced brainstem inhibition during anticipated pelvic visceral pain correlates with enhanced brain response to the visceral stimulus in women with irritable bowel syndrome. J Neurosci. 2008;28:349–359
  2. Bragdon EE, Light KC, Costello NL, Sigurdsson A, Bunting S, Bhalang K, et al. Group differences in pain modulation: pain-free women compared to pain-free men and to women with TMD. Pain. 2002;96:227–237
  3. Cadden SW. The ability of inhibitory controls to ‘switch-off’ activity in dorsal horn convergent neurones in the rat. Brain Res. 1993;628:65–71
  4. Coderre TJ, Katz J. Peripheral and central hyperexcitability: differential signs and symptoms in persistent pain. Behav Brain Sci. 1997;20:404–419
  5. Coghill RC, Mayer DJ, Price DD. Wide dynamic range but not nociceptive-specific neurons encode multidimensional features of prolonged repetitive heat pain. J Neurophysiol. 1993;69:703–716
  6. Dworkin SF, LeResche L. Research diagnostic criteria for temporomandibular disorders: review, criteria, examinations and specifications, critique. J Craniomandib Disord. 1992;6:301–355
  7. Edwards RR. Individual differences in endogenous pain modulation as a risk factor for chronic pain. Neurology. 2005;65:437–443
  8. Edwards RR, Fillingim RB, Ness TJ. Age-related differences in endogenous pain modulation: a comparison of diffuse noxious inhibitory controls in healthy older and younger adults. Pain. 2003;101:155–165
  9. Edwards RR, Ness TJ, Fillingim RB. Endogenous opioids, blood pressure, and diffuse noxious inhibitory controls: a preliminary study. Percept Mot Skills. 2004;99:679–687
  10. Edwards RR, Ness TJ, Weigent DA, Fillingim RB. Individual differences in diffuse noxious inhibitory controls (DNIC): association with clinical variables. Pain. 2003;106:427–437
  11. Edwards RR, Sarlani E, Wesselmann U, Fillingim RB. Quantitative assessment of experimental pain perception: multiple domains of clinical relevance. Pain. 2005;114:315–319
  12. Eide PK. Wind-up and the NMDA receptor complex from a clinical perspective. Eur J Pain. 2000;4:5–15
  13. Geel SE. The fibromyalgia syndrome: musculoskeletal pathophysiology. Semin Arthritis Rheum. 1994;23:347–353
  14. Girdler SS, Maixner W, Naftel HA, Stewart PW, Moretz RL, Light KC. Cigarette smoking, stress-induced analgesia and pain perception in men and women. Pain. 2005;114:372–385
  15. Goffaux P, Redmond WJ, Rainville P, Marchand S. Descending analgesia – when the spine echoes what the brain expects. Pain. 2007;130:137–143
  16. Grill JD, Coghill RC. Transient analgesia evoked by noxious stimulus offset. J Neurophysiol. 2002;87:2205–2208
  17. Kosek K, Ordeberg G. Lack of pressure pain modulation by heterotopic noxious conditioning stimulation in patients with painful osteoarthritis before, but not following, surgical pain relief. Pain. 2000;88:69–78
  18. Kosek K, Hansson P. Modulatory influence on somatosensory perception from vibration and heterotopic noxious conditioning stimulation (HNCS) in fibromyalgia patients and healthy subjects. Pain. 1997;70:41–51
  19. Koyama Y, Koyama T, Kroncke AP, Coghill RC. Effects of stimulus duration on heat induced pain: the relationship between real-time and post-stimulus pain ratings. Pain. 2004;107:256–266
  20. Lautenbacher S, Rollman GB. Possible deficiencies of pain modulation in fibromyalgia. Clin J Pain. 1997;13:189–196
  21. Le Bars D, Chitour D, Kraus E, Clot AM, Dickenson AH, Besson JM. The effect of systemic morphine upon diffuse noxious inhibitory controls (DNIC) in the rat: evidence for a lifting of certain descending inhibitory controls of dorsal horn convergent neurons. Brain Res. 1981;215:257–274
  22. Le Bars D, Dickenson AH, Besson JM. Diffuse noxious inhibitory controls (DNIC). I. Effects on dorsal horn convergent neurones in the rat. Pain. 1979;6:283–304
  23. Le Bars D, Dickenson AH, Besson JM. Diffuse noxious inhibitory controls (DNIC). II. Lack of effect on non-convergent neurones, supraspinal involvement and theoretical implications. Pain. 1979;6:305–327Bars D, Gozariu M, Cadden SW. Animal models of nociception. Pharmacol Rev. 2001;53:597–652
  24. Le Bars D, Villanueva L, Bouhassira D, Willer JC. Diffuse noxious inhibitory controls (DNIC) in animals and in man. Patol Fiziol Eksp Ter. 1992;4:55–65
  25. Longstreth GF, Thompson WG, Chey WD, Houghton LA, Mearin F, Spiller RC. Functional bowel disorders. Gastroenterology. 2006;130:1480–1491
  26. Maixner W, Fillingim R, Booker D, Sigurdsson A. Sensitivity of patients with painful temporomandibular disorders to experimentally evoked pain. Pain. 1995;63:341–351
  27. Maixner W, Fillingim R, Sigurdsson A, Kincaid S, Silva S. Sensitivity of patients with painful temporomandibular disorders to experimentally evoked pain: evidence for altered temporal summation of pain. Pain. 1998;76:71–81
  28. Malykhina AP. Neural mechanisms of pelvic organ cross-sensitization. Neuroscience. 2007;149:660–672
  29. Mechlin MB, Maixner W, Light KC, Fisher JM, Girdler SS. African Americans show alterations in endogenous pain regulatory mechanisms and reduced pain tolerance to experimental pain procedures. Psychosom Med. 2005;67:948–956
  30. Moshiree N, Maixner W, Robinson ME, Gaible R, Verne GN. Thermal and visceral hypersensitivity in irritable bowel syndrome patients with and without fibromyalgia. Clin J Pain. 2007;23:323–330
  31. Naert AL, Kehlet H, Kupers R. Characterization of a novel model of tonic heat pain stimulation in healthy volunteers. Pain. 2008;138:163–171
  32. Pielsticke A, Haag G, Zaudig M, Lautenbacher S. Impairment of pain inhibition in chronic tension-type headache. Pain. 2005;118:215–223
  33. Price DD. Psychological and neural mechanisms of the affective dimension of pain. Science. 2000;288:1769–1772
  34. Price DD, McHaffie JG. Effects of heterotopic conditioning stimuli on first and second pain: a psychophysical evaluation in humans. Pain. 1988;34245–34252
  35. Price DD, Verne GN, Schwartz JM. Plasticity in brain processing and modulation of pain. Prog Brain Res. 2006;157:333–352
  36. 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
  37. Price DD, Zhou Q, Moshiree B, Robinson ME, Verne GN. Peripheral and central contributions to hyperalgesia in irritable bowel syndrome. J Pain. 2006;7:529–535
  38. Price DD, Staud R, Robinson ME, Mauderli AP, Cannon R, Vierck CJ. Enhanced temporal summation of second pain and its central modulation in fibromyalgia patients. Pain. 2002;99:49–59
  39. Ram KC, Eisenberg E, Haddad M, Pu D. Oral opioid use alters DNIC but not cold pain perception in patients with chronic pain – new perspective of opioid-induced hyperalgesia. Pain. 2008;139:431–438
  40. Rodrigues AC, Verne GN, Schmidt S, Mauderli AP. Hypersensitivity to cutaneous thermal nociceptive stimuli in irritable bowel syndrome. Pain. 2005;115:5–11
  41. Sandrini G, Rossi P, Milanov I, Serrao M, Cecchini AP, Nappi G. Abnormal modulatory influence of diffuse noxious inhibitory controls in migraine and chronic tension-type headache patients. Cephalalgia. 2006;26:782–789
  42. Sarlani E, Garrett PH, Grace EG, Greenspan JD. Temporal summation of pain characterizes women but not men with temporomandibular disorders. J Orofac Pain. 2007;21:309–317
  43. Sarlani E, Grace EG, Reynolds MA, Greenspan JD. Evidence for up-regulated central nociceptive processing in patients with masticatory myofascial pain. J Orofac Pain. 2004;18:41–55
  44. Sigurdsson A, Maixner W. Effects of experimental and clinical noxious counterirritants on pain perception. Pain. 1994;57:265–275
  45. Spielberger C, Gorsuch R, Lushene R. Manual for the state-trait anxiety inventory. Palo Alto, CA: Consulting Psychologist Press; 1970;
  46. Song GH, Venkatraman V, Ho KY, Chee MW, Yeoh KG, Wilder-Smith CH. Cortical effects of anticipation and endogenous modulation of visceral pain assessed by functional brain MRI in irritable bowel syndrome patients and healthy controls. Pain. 2006;126:79–90
  47. Staud R, Robinson ME, Vierck CJ, Price DD. Diffuse noxious inhibitory controls (DNIC) attenuate temporal summation of second pain in normal males but not in normal females or fibromyalgia patients. Pain. 2003;101:167–174
  48. Staud R, Robinson ME, Vierck CJ, Cannon RL, Mauderli AP, Price DD. Ratings of experimental pain and pain-related negative affect predict clinical pain in patients with fibromyalgia syndrome. Pain. 2003;105:215–222
  49. Staud R, Vierck CJ, Cannon RL, Mauderli AP, Price DD. Abnormal sensitization and temporal summation of second pain (wind-up) inpatients with fibromyalgia syndrome. Pain. 2001;91:165–175
  50. Svensson P, List T, Hector G. Analysis of stimulus-evoked pain in patients with myofascial temporomandibular pain disorders. Pain. 2001;92:399–409
  51. Talbot JD, Duncan GH, Bushnell MC. Effects of diffuse noxious inhibitory controls (DNICs) on the sensory-discriminative dimension of pain perception. Pain. 1989;36:231–238
  52. Talbot JD, Duncan GH, Bushnell MC, Boyer M. Diffuse noxious inhibitory controls (DNICs): psychophysical evidence in man for intersegmental suppression of noxious heat perception by cold pressor pain. Pain. 1987;30:221–232
  53. 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
  54. Verne GN, Robinson ME, Price DD. Hypersensitivity to visceral and cutaneous pain in the irritable bowel syndrome. Pain. 2001;93:7–14
  55. Verne GN, Himes NC, Robinson ME, Gopinath KS, Briggs BW, Crosson B, et al. Central representation of visceral and cutaneous hypersensitivity in the irritable bowel syndrome. Pain. 2003;103:99–110
  56. Villanueva L, Le Bars D. The activation of bulbo-spinal controls by peripheral nociceptive inputs: diffuse noxious inhibitory controls. Biol Res. 1995;28:113–125
  57. Washington LL, Gibson SJ, Helme RD. Age-related differences in the endogenous analgesic response to repeated coldwater immersion in human volunteers. Pain. 2000;89:89–96
  58. Wilder-Smith CH, Robert-Yap J. Abnormal endogenous pain modulation and somatic and visceral hypersensitivity in female patients with irritable bowel syndrome. World J Gastroenterol. 2007;13:3699–3704
  59. Wilder-Smith CH, Schindler D, Lovblad K, Redmond SM, Nirkko A. Brain functional magnetic resonance imaging of rectal pain and activation of endogenous inhibitory mechanisms in irritable bowel syndrome patient subgroups and healthy controls. Gut. 2004;53:1595–1601
  60. Willer JC, Albe-Fessard D. Electrophysiological evidence for a release of endogenous opiates in stress-induced ‘analgesia’ in man. Brain Res. 1980;198:419–426
  61. Willer JC, De Broucker T, Le Bars D. Encoding of nociceptive thermal stimuli by diffuse noxious inhibitory controls in humans. J Neurophysiol. 1989;62:1028–1038
  62. Willer JC, Dehen H, Cambier J. Stress-induced analgesia in humans: endogenous opioids and naloxone-reversible depression of pain reflexes. Science. 1981;212:689–691
  63. Willer JC, Le Bars D, De Broucker T. Diffuse noxious inhibitory controls in man: involvement of an opioidergic link. Eur J Pharmacol. 1990;182:347–355
  64. Willer JC, Roby A, Le Bars D. Psychophysical and electrophysiological approaches to the pain-relieving effects of heterotopic nociceptive stimuli. Brain. 1984;107:1095–1112
  65. Yamada K, Nabeshima T. Stress-induced behavioral responses and multiple opioid systems in the brain. Behav Brain Res. 1995;67:133–145

PII: S0304-3959(08)00765-3

doi: 10.1016/j.pain.2008.12.027

PAIN
Volume 143, Issue 3 , Pages 172-178 , June 2009