Patients with pain disorder show gray-matter loss in pain-processing structures: A voxel-based morphometric study

Psychosomatic Medicine

Volumn 71, Issue 1, 2009, Pages 49-56

  Valet, Michael ^a   Gündel, Harald ^b,c   Sprenger, Till ^a   Sorg, Christian ^a   Mühlau, Mark ^a   Zimmer, Claus ^c   Henningsen, Peter ^c   Tölle, Thomas R ^a  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^b HANNOVER MEDICAL SCHOOL   (Germany)

^c TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

Classification; Idiopathic chronic pain; Orbitofrontal cortex; Pain disorder; Ventromedial prefrontal cortex; Voxel based morphometry

Indexed keywords

ADULT; AGED; ARTICLE; BECK DEPRESSION INVENTORY; CINGULATE GYRUS; CLINICAL ARTICLE; COMORBIDITY; CONTROLLED STUDY; DIAGNOSTIC AND STATISTICAL MANUAL OF MENTAL DISORDERS; FEMALE; GRAY MATTER; HUMAN; INSULA; MORPHOMETRICS; NEUROIMAGING; NUCLEAR MAGNETIC RESONANCE IMAGING; PAIN; PREFRONTAL CORTEX; PRIORITY JOURNAL; PSYCHOLOGICAL ASPECT; AGE; ANTHROPOMETRY; BRAIN CORTEX; DEPRESSION; EPIDEMIOLOGY; GERMANY; IMAGE PROCESSING; MAJOR DEPRESSION; MIDDLE AGED; PATHOLOGY; SOMATOFORM DISORDER;

ADULT; AGE FACTORS; AGED; ANTHROPOMETRY; CEREBRAL CORTEX; CONFOUNDING FACTORS (EPIDEMIOLOGY); DEPRESSION; DEPRESSIVE DISORDER, MAJOR; FEMALE; GERMANY; GYRUS CINGULI; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MIDDLE AGED; PAIN; PREFRONTAL CORTEX; SOMATOFORM DISORDERS;

EID: 65549122637     PISSN: 00333174     EISSN: 15347796     Source Type: Journal    
DOI: 10.1097/PSY.0b013e31818d1e02     Document Type: Article

References (78)

1. Waller E, Scheidt CE. Somatoform disorders as disorders of affect regulation: a development perspective. Int Rev Psychiatry 2006;18: 13-24.
2. Meyer C, Rumpf HJ, Hapke U, Dilling H, John U. Lifetime prevalence of mental disorders in general adult population. Results of TACOS study. Nervenarzt 2000;71:535-42.
3. Gündel H, Valet M, Sorg C, Huber D, Zimmer C, Sprenger T, Tölle TR. Altered cerebral response to noxious heat stimulation in patients with somatoform pain disorder. Pain 2008;137:413-21.
4. Stoeter P, Bauermann T, Nickel R, Corluka L, Gawehn J, Vucurevic G, Vossel G, Egle UT. Cerebral activation in patients with somatoform pain disorder exposed to pain and stress: an fMRI study. Neuroimage 2007;36:418-30.
5. Cook DB, Lange G, Ciccone DS, Liu WC, Steffener J, Natelson BH. Functional imaging of pain in patients with primary fibromyalgia. J Rheumatol 2004;31:364-78.
6. Gracely RH, Petzke F, Wolf JM, Clauw DJ. Functional magnetic resonance imaging evidence of augmented pain processing in fibromyalgia. Arthritis Rheum 2002;46:1333-43.
7. Wik G, Fischer H, Finer B, Bragee B, Kristianson M, Fredrikson M. Retrospenial cortical deactivation during painful stimulation of fibromyalgic patients. Int J Neurosci 2006;116:1-8.
8. Giesecke T, Gracely RH, Grant MA, Nachemson A, Petzke F, Williams DA, Clauw DJ. Evidence of augmented central pain processing in idiopathic chronic low back pain. Arthritis Rheum 2004;50:613-23.
9. Bonaz B, Baciu M, Papillon E, Bost R, Gueddah N, Le Bas JF, Fournet J, Segebarth C. Central processing of rectal pain in patients with irritable bowel syndrome: an fMRI study. Am J Gastroenterol 2002;97:654-61.
10. Kwan CL, Diamant NE, Pope G, Mikula K, Mikulis DJ, Davis KD. Abnormal forebrain activity in functional bowel disorder patients with chronic pain. Neurology 2005;65:1268-77.
11. Berman SM, Naliboff BD, Suyenobu B, Labus JS, Stains J, Ohning G, Kilpatrick L, Bueller JA, Ruby K, Jarcho J, Mayer EA. 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;28:349-59.
12. Schmidt-Wilcke T, Luerding R, Weigand T, Jurgens T, Schuierer G, Leinisch E, Bogdahn U. Striatal grey matter increase in patients suffering from fibromyalgia - a voxel-based morphometry study. Pain 2007;132(Suppl 1):S109-S116.
13. Kuchinad A, Schweinhardt P, Seminowicz DA, Wood PB, Chizh BA, Bushnell MC. Accelerated brain gray matter loss in fibromyalgia patients: premature aging of the brain? J Neurosci 2007;27:4004-7.
14. Apkarian AV, Sosa Y, Sonty S, Levy RM, Harden RN, Parrish TB, Gitelman DR. Chronic back pain is associated with decreased prefrontal and thalamic gray matter density. J Neurosci 2004;24:10410-5.
15. Schmidt-Wilcke T, Leinisch E, Ganssbauer S, Draganski B, Bogdahn U, Altmeppen J, May A. Affective components and intensity of pain correlate with structural differences in gray matter in chronic back pain patients. Pain 2006;125:89-97.
16. Mechelli A, Price CJ, Friston KJ, Ashburner J. Voxel-based morphometry of the human brain: methods and applications. Curr Med Imaging Rev 2005;1:1-9.
17. Ashburner J, Friston KJ. Voxel-based morphometry - the methods. Neuroimage 2000;11:805-21.
18. Baron JC, Chetelat G, Desgranges B, Perchey G, Landeau B, de la Sayette V, Eustache F. In vivo mapping of gray matter loss with voxel-based morphometry in mild Alzheimer's disease. Neuroimage 2001;14:298-309.
19. Muhlau M, Weindl A, Wohlschlager AM, Gaser C, Stadtler M, Valet M, Zimmer C, Kassubek J, Peinemann A. Voxel-based morphometry indicates relative preservation of the limbic prefrontal cortex in early Huntington disease. J Neural Transm 2007;114:367-72.
20. Burton EJ, McKeith IG, Burn DJ, Williams ED, O'Brien JT. Cerebral atrophy in Parkinson's disease with and without dementia: a comparison with Alzheimer's disease, dementia with Lewy bodies and controls. Brain 2004;127:791-800.
21. Saykin AJ, Wishart HA, Rabin LA, Santulli RB, Flashman LA, West JD, McHugh TL, Mamourian AC. Older adults with cognitive complaints show brain atrophy similar to that of amnestic MCI. Neurology 2006;67: 834-42.
22. Minnerop M, Specht K, Ruhlmann J, Schimke N, Abele M, Weyer A, Wullner U, Klockgether T. Voxel-based morphometry and voxel-based relaxometry in multiple system atrophy - a comparison between clinical subtypes and correlations with clinical parameters. Neuroimage 2007;36: 1086-95.
23. Maguire EA, Gadian DG, Johnsrude IS, Good CD, Ashburner J, Frackowiak RS, Frith CD. Navigation-related structural change in the hippocampi of taxi drivers. Proc Natl Acad Sci U S A 2000;97:4398-403.
24. Gaser C, Schlaug G. Brain structures differ between musicians and non-musicians. J Neurosci 2003;23:9240-5.
25. Mechelli A, Crinion JT, Noppeney U, O'Doherty J, Ashburner J, Frackowiak RS, Price CJ. Neurolinguistics: structural plasticity in the bilingual brain. Nature 2004;431:757.
26. Ilg R, Wohlschlager AM, Gaser C, Liebau Y, Dauner R, Woller A, Zimmer C, Zihl J, Muhlau M. Gray matter increase induced by practice correlates with task-specific activation: a combined functional and morphometric magnetic resonance imaging study. J Neurosci 2008;28: 4210-5.
27. Kroenke K, Sharpe M, Sykes R. Revising the classification of somato-form disorders: key questions and preliminary recommendations. Psychosomatics 2007;48:277-85.
28. Sykes R. Somatoform disorders in DSM-IV: mental or physical disorders? J Psychosom Res 2006;60:341-4.
29. Strassnig M, Stowell KR, First MB, Pincus HA. General medical and psychiatric perspectives on somatoform disorders: separated by an uncommon language. Curr Opin Psychiatry 2006;19:194-200.
30. Henningsen P, Zipfel S, Herzog W. Management of functional somatic syndromes. Lancet 2007;369:946-55.
31. Wittchen HU, Wunderlich U, Gruschwitz S, Zaudig M. Strukturiertes klinisches Interview für DSM-IV, Achse I (SKID). Göttingen: Hogrefe Verlag; 1997.
32. Edinburgh. Edinburgh Handedness Inventory. Neuropsychologia 1971;9: 97-113.
33. Rief W, Hiller W, Heuser J. Das Screening für somatoforme Störungen (SOMS - the screening for somatoform disorders) - Manual zum Fragebogen. Bern: Verlag Hans Huber; 1997.
34. Geissner E. The pain perception scale - a differentiated and change-sensitive scale for assessing chronic and acute pain. Rehabilitation (Stuttg) 1995;34:XXXV-XLIII.
35. Wolfe F, Smythe HA, Yunus MB, Bennett RM, Bombardier C, Goldenberg DL, Tugwell P, Campbell SM, Abeles M, Clark P, et al. The American College of Rheumatology 1990 Criteria for the Classification of Fibromyalgia. Report of the Multicenter Criteria Committee. Arthritis Rheum 1990;33:160-72.
36. Comment in Arthritis Rheum 1990;33:1863-4; Arthritis Rheum 1991;34:128.
37. Beck AT, Steer RA, Garbin MG. Psychometric properties of the Beck depression inventory: twenty-five years of evaluation. Clin Psychol Rev 1998;8:77-100.
38. Good CD, Johnsrude IS, Ashburner J, Henson RN, Friston KJ, Frackowiak RS. A voxel-based morphometric study of ageing in 465 normal adult human brains. Neuroimage 2001;14:21-36.
39. Cuadra MB, Cammoun L, Butz T, Cuisenaire O, Thiran JP. Comparison and validation of tissue modelization and statistical classification methods in T1-weighted MR brain images. IEEE Trans Med Imaging 2005;24:1548-65.
40. Genovese CR, Lazar NA, Nichols T. Thresholding of statistical maps in functional neuroimaging using the false discovery rate. Neuroimage 2002;15:870-8.
41. Apkarian AV, Bushnell MC, Treede RD, Zubieta JK. Human brain mechanisms of pain perception and regulation in health and disease. Eur J Pain 2005;9:463-84.
42. Tracey I, Mantyh PW. The cerebral signature for pain perception and its modulation. Neuron 2007;55:377-91.
43. Schmidt-Wilcke T, Leinisch E, Straube A, Kampfe N, Draganski B, Diener HC, Bogdahn U, May A. Gray matter decrease in patients with chronic tension type headache. Neurology 2005;65:1483-6.
44. Taki Y, Kinomura S, Awata S, Inoue K, Sato K, Ito H, Goto R, Uchida S, Tsuji I, Arai H, Kawashima R, Fukuda H. Male elderly subthreshold depression patients have smaller volume of medial part of prefrontal cortex and precentral gyrus compared with age-matched normal subjects: a voxel-based morphometry. J Affect Disord 2005;88:313-20.
45. Nugent AC, Milham MP, Bain EE, Mah L, Cannon DM, Marrett S, Zarate CA, Pine DS, Price JL, Drevets WC. Cortical abnormalities in bipolar disorder investigated with MRI and voxel-based morphometry. Neuroimage 2006;30:485-97.
46. Yoshikawa E, Matsuoka Y, Yamasue H, Inagaki M, Nakano T, Akechi T, Kobayakawa M, Fujimori M, Nakaya N, Akizuki N, Imoto S, Murakami K, Kasai K, Uchitomi Y. Prefrontal cortex and amygdala volume in first minor or major depressive episode after cancer diagnosis. Biol Psychiatry 2006;59:707-12.
47. Valet M, Sprenger T, Boecker H, Willoch F, Rummeny E, Conrad B, Erhard P, Tolle TR. Distraction modulates connectivity of the cingulofrontal cortex and the midbrain during pain - an fMRI analysis. Pain 2004;109:399-408.
48. Sprenger T, Valet M, Boecker H, Henriksen G, Spilker ME, Willoch F, Wagner KJ, Wester HJ, Tolle TR. Opioidergic activation in the medial pain system after heat pain. Pain 2006;122:63-7.
49. Petrovic P, Ingvar M. Imaging cognitive modulation of pain processing. Pain 2002;95:1-5.
50. Petrovic P, Kalso E, Petersson KM, Ingvar M. Placebo and opioid analgesia - imaging a shared neuronal network. Science 2002;295: 1737-40.
51. Faymonville ME, Laureys S, Degueldre C, DelFiore G, Luxen A, Franck G, Lamy M, Maquet P. Neural mechanisms of antinociceptive effects of hypnosis. Anesthesiology 2000;92:1257-67.
52. Seminowicz DA, Davis KD. Cortical responses to pain in healthy individuals depends on pain catastrophizing. Pain 2006;120:297-306.
53. Fumal A, Laureys S, Di Clemente L, Boly M, Bohotin V, Vandenheede M, Coppola G, Salmon E, Kupers R, Schoenen J. Orbitofrontal cortex involvement in chronic analgesic-overuse headache evolving from episodic migraine. Brain 2006;129:543-50.
54. Grachev ID, Fredrickson BE, Apkarian AV. Abnormal brain chemistry in chronic back pain: an in vivo proton magnetic resonance spectroscopy study. Pain 2000;89:7-18.
55. Schmidt-Wilcke T, Ganssbauer S, Neuner T, Bogdahn U, May A. Subtle grey matter changes between migraine patients and healthy controls. Cephalalgia 2007.
56. Devinsky O, Morrell MJ, Vogt BA. Contributions of anterior cingulate cortex to behaviour. Brain 1995;118(Pt 1):279-306.
57. Augustine JR. Circuitry and functional aspects of the insular lobe in primates including humans. Brain Res Brain Res Rev 1996;22:229-44.
58. Derbyshire SW, Vogt BA, Jones AK. Pain and Stroop interference tasks activate separate processing modules in anterior cingulate cortex. Exp Brain Res 1998;118:52-60.
59. Peyron R, Garcia-Larrea L, Gregoire MC, Costes N, Convers P, Lavenne F, Mauguiere F, Michel D, Laurent B. Haemodynamic brain responses to acute pain in humans: sensory and attentional networks. Brain 1999;122: 1765-80.
60. Rainville P, Duncan GH, Price DD, Carrier B, Bushnell MC. Pain affect encoded in human anterior cingulate but not somatosensory cortex. Science 1997;277:968-71.
61. Tölle TR, Kaufmann T, Siessmeier T, Lautenbacher S, Berthele A, Munz F, Zieglgansberger W, Willoch F, Schwaiger M, Conrad B, Bartenstein P. Region-specific encoding of sensory and affective components of pain in the human brain: a positron emission tomography correlation analysis. Ann Neurol 1999;45:40-7.
62. Nitschke JB, Sarinopoulos I, Mackiewicz KL, Schaefer HS, Davidson RJ. Functional neuroanatomy of aversion and its anticipation. Neuroimage 2006;29:106-16.
63. Craig AD, Chen K, Bandy D, Reiman EM. Thermosensory activation of insular cortex. Nat Neurosci 2000;3:184-90.
64. Singer T, Seymour B, O'Doherty J, Kaube H, Dolan RJ, Frith CD. Empathy for pain involves the affective but not sensory components of pain. Science 2004;303:1157-62.
65. Chen S, Xia W, Li L, Liu J, He Z, Zhang Z, Yan L, Zhang J, Hu D. Gray matter density reduction in the insula in fire survivors with posttraumatic stress disorder: a voxel-based morphometric study. Psychiatry Res 2006;146:65-72.
66. Villarreal G, Hamilton DA, Petropoulos H, Driscoll I, Rowland LM, Griego JA, Kodituwakku PW, Hart BL, Escalona R, Brooks WM. Reduced hippocampal volume and total white matter volume in posttraumatic stress disorder. Biol Psychiatry 2002;52:119-25.
67. Yamasue H, Kasai K, Iwanami A, Ohtani T, Yamada H, Abe O, Kuroki N, Fukuda R, Tochigi M, Furukawa S, Sadamatsu M, Sasaki T, Aoki S, Ohtomo K, Asukai N, Kato N. Voxel-based analysis of MRI reveals anterior cingulate gray-matter volume reduction in posttraumatic stress disorder due to terrorism. Proc Natl Acad Sci U S A 2003;100:9039-43.
68. Emdad R, Bonekamp D, Sondergaard HP, Bjorklund T, Agartz I, Ingvar M, Theorell T. Morphometric and psychometric comparisons between non-substance-abusing patients with posttraumatic stress disorder and normal controls. Psychother Psychosom 2006;75:122-32.
69. Okada T, Tanaka M, Kuratsune H, Watanabe Y, Sadato N. Mechanisms underlying fatigue: a voxel-based morphometric study of chronic fatigue syndrome. BMC Neurology 2004;4:14.
70. de Lange FP, Kalkman JS, Bleijenberg G, Hagoort P, van der Meer JW, Toni I. Gray matter volume reduction in the chronic fatigue syndrome. Neuroimage 2005;26:777-81.
71. Buchel C, Dolan RJ, Armony JL, Friston KJ. Amygdala-hippocampal involvement in human aversive trace conditioning revealed through event-related functional magnetic resonance imaging. J Neurosci 1999;19:10869-76.
72. Geuze E, Westenberg HG, Jochims A, de Kloet CS, Bohus M, Vermetten E, Schmahl C. Altered pain processing in veterans with posttraumatic stress disorder. Arch Gen Psychiatry 2007;64:76-85.
73. Ploghaus A, Narain C, Beckmann CF, Clare S, Bantick S, Wise R, Matthews PM, Rawlins JN, Tracey I. Exacerbation of pain by anxiety is associated with activity in a hippocampal network. J Neurosci 2001;21: 9896-903.
74. Hobson AR, Aziz Q. Brain processing of esophageal sensation in health and disease. Gastroenterol Clin North Am 2004;33:69-91.
75. Derbyshire SW, Jones AK, Creed F, Starz T, Meltzer CC, Townsend DW, Peterson AM, Firestone L. Cerebral responses to noxious thermal stimulation in chronic low back pain patients and normal controls. Neuroimage 2002;16:158-68.
76. Frohlich C, Jacobi F, Wittchen HU. DSM-IV pain disorder in the general population. An exploration of the structure and threshold of medically unexplained pain symptoms. Eur Arch Psychiatry Clin Neurosci 2006;256:187-96.
77. Draganski B, Gaser C, Busch V, Schuierer G, Bogdahn U, May A. Neuroplasticity: changes in grey matter induced by training. Nature 2004;427:311-2.
78. Teutsch S, Herken W, Bingel U, Schoell E, May A. Changes in brain gray matter due to repetitive painful stimulation. Neuroimage 2008;42:845-9. Epub 2008 Jul 7.