Preview

Rheumatology Science and Practice

Advanced search

Functional magnetic resonance imaging for chronic pain in patients with rheumatic diseases

https://doi.org/10.14412/1995-4484-2019-612-617

Abstract

Along with tissue damage, inflammation, and degenerative processes, central sensitization (spinal and supraspinal neuronal hyperactivity resulting from continuous nociceptive stimulation) plays an important role in the pathogenesis of chronic pain in rheumatic diseases (RDs). Functional magnetic resonance imaging (fMRI) makes it possible to visualize the central nervous system (CNS) parts involved in nociception and to diagnose central sensitization and its associated emotional and cognitive aspects of the experience of pain. Thus, fMRI for rheumatoid arthritis has revealed activation predominantly in the medial pain system, including the anterior cingulate gyrus, prefrontal cortex, and insula — the CNS structures that do not participate in the primary sensory discrimination assessment of pain, but determine its emotional assessment and the formation of pain behavior. The fMRI technique makes it possible to better understand the central mechanisms of chronic pain in RDs, to more accurately select drug and non-drug treatments, and to monitor their efficiency.

About the Authors

E. S. Filatova
V.A. Nasonova Research Institute of Rheumatology
Russian Federation

Ekaterina Filatova

34A, Kashirskoe Shosse, Moscow 115522


Competing Interests: not


A. E. Karateev
V.A. Nasonova Research Institute of Rheumatology
Russian Federation

34A, Kashirskoe Shosse, Moscow 115522


Competing Interests: not


A. M. Lila
V.A. Nasonova Research Institute of Rheumatology; Russian Medical Academy of Continuing Professional Education, Ministry of Health of Russi
Russian Federation

2/1, Barrikadnaya St., Build. 1, Moscow 125993; 34A, Kashirskoe Shosse, Moscow 115522


Competing Interests: not


E. L. Nasonov
V.A. Nasonova Research Institute of Rheumatology; .M. Sechenov First Moscow State Medical University (Sechenov University), Ministry of Health of Russia
Russian Federation

34A, Kashirskoe Shosse, Moscow 115522; 8, Trubetskaya St., Build. 2, Moscow 119991


Competing Interests: not


References

1. Nasonov EL, editor. Rossiyskie klinicheskie rekomendatsii. Revmatologiya [Russian clinical recommendations. Rheumatology]. Moscow: GEOTAR-Media; 2017. 464 p. (In Russ.). ISBN 978-5-9704-4261-6

2. Piradov MA, Tanashyan MM, Krotenkova MV, et al. Advanced neuroimaging technologies. KlinicheskayaNevrologiya. 2015;9(4):11-8 (In Russ.)].

3. Shtark MB, Korostyshevskaya AM, Rezakova MV, et al. Functional magnetic resonance imaging and neuroscience. UspekhiFiziologicheskikh Nauk. 2012;43(1):3-29 (In Russ.).

4. Ogawa S, Lee TM. Magnetic resonance imaging of blood vessels at high fields: In vivo and in vitro measurements and image simulation. Magn Reson Med. 1990;16(1):9-18. doi:10.1002/mrm.1910160103

5. Glover GH, Lai S. Self-navigated spiral fMRI: Interleaved versus single-shot. Magn Reson Med. 1998;39:361-8. doi: 10.1002/mrm.1910390305

6. Treede RD, Kenshalo DR, Gracely RH, et al. The cortical representation of pain. Pain. 1999;79:105-11. doi: 10.1016/S0304-3959(98)00184-5

7. Melzack R. From the gate to the neuromatrix. Pain. 1999;6:121-6. doi: 10.1016/S0304-3959(99)00145-1

8. Bowsher D. Termination of the central pain pathway in man: the conscious appreciation of pain. Brain. 1957;80(4):606-22. doi: 10.1093/brain/80.4.606

9. Kulkarni B, Bentley DE, Elliott R, et al. Attention to pain localization and unpleasantness discriminates the functions of themedi-al and lateral pain systems. Eur JNeurosci. 2005;21:3133-42. doi: 10.1111/j.1460-9568.2005.04098.x

10. Porro CA, Cettolo V, Francescato MP, et al. Temporal and intensity coding of pain in human cortex. J Neurophysiol. 1998;80(6):3312-20. doi: 10.1152/jn.1998.80.6.3312

11. Apkarian AV, Bushnell MC, Treede R-D, et al. Human brain mechanisms of pain perception and regulation in health and disease. Eur J Pain. 2005;9(4):463-84. doi: 10.1016/j.ejpain.2004.11.001

12. Seifert F, Maihafner C. Central mechanisms of experimental and chronic neuropathic pain: Findings from functional imaging studies. Cell Mol Life Sci. 2009;66:375-90. doi: 10.1007/s00018-008-8428-0

13. Baron R, Baron Y, Disbrow E, et al. Brain processing of capsaicin-induced secondary hyperalgesia: a functional MRI study. Neurology. 1999;53:548-57. doi: 10.1212/WNL.53.3.548

14. Maihofner C, Schmelz M, Forster C, et al. Neural activation during experimental allodynia: a functional magnetic resonance imaging study. Eur J Neurosci. 2004;19:3211-8. doi: 10.1111/j.1460-9568.2004.03437.x

15. Maihofner C, Handwerker HO. Differential coding of hyperalgesia in the human brain: a functional MRI study. Neuroimage. 2005;28:996-1006. doi: 10.1016/j.neuroimage.2005.06.049

16. Zambreanu L, Wise RG, Brooks JC, et al. A role for the brainstem in central sensitisation in humans. Evidence from functional magnetic resonance imaging. Pain. 2005;114:397-407. doi: 10.1016/j.pain.2005.01.005

17. Baliki MN, Geha PY, Apkarian AV, et al. Beyond feeling: chronic pain hurts the brain, disrupting the default-mode network dynamics. JNeurosci. 2008;28:1398-403. doi: 10.1523/JNEU-ROSCI.4123-07.2008

18. Karateev AE, Nasonov EL. Chronic pain and central sensitization in immuno-inflammatory rheumatic diseases: pathogenesis, clinical manifestations, the possibility of using targeted disease modifying antirheumatic drugs. Nauchno-Prakticheskaya Revmatologiya = Rheumatology Science and Practice. 2019;57(2):197-209 (In Russ.). doi: 10.14412/1995-4484-2019-197-209

19. Kidd BL. Osteoarthritis and joint pain. Pain. 2006 Jul;123(1-2):6-9. doi: 10.1016/j.pain.2006.04.009

20. Jones AK, Friston K, Frackowiak RS. Localization of responses to pain in human cerebral cortex. Science. 1992;255:215-6. doi: 10.1126/science.1553549

21. Jones AK, Brown WD, Friston KJ, et al. Cortical and subcortical localization of response to pain in man using positron emission tomography. Proc R Soc Lond B Biol Sci. 1991;244:39-44. doi: 10.1098/rspb.1991.0048

22. Kennedy DP, Courchesne E. Functional abnormalities of the default network during self- and other-reflection in autism. Soc Cogn Affect Neurosci. 2008;3:177-90. doi: 10.1093/scan/nsn011

23. Kalk NJ, Schweinhardt P, et al. Functional magnetic resonance imaging of central processing of clinical and experimental pain in rheumatoid arthritis. Abstracts 11th World Congress on Pain. August 21-26. Sydney: N.S.W.; 2005. P. 108.

24. Seifert F, Jungfer I, Schmelz M, et al. Representation of UV-B-induced thermal and mechanical hyperalgesia in the human brain: A functional MRI study. Hum Brain Mapp. 2008;29(12):1327-42. doi: 10.1002/hbm.20470

25. Bickel A, Dorfs S, Schmelz M, et al. Effects of antihyperalgesic drugs on experimentally induced hyperalgesia in man. Pain. 1998;76:317-25. doi: 10.1016/S0304-3959(98)00062-1

26. Wasner G, Schattschneider J, Binder A, et al. Topical menthol — a human model for cold pain by activation and sensitization of C nociceptors. Brain. 2004;127:1159-71. doi: 10.1093/brain/awh134

27. Seifert F, Maihofner C. Representation of cold allodynia in the human brain — a functional MRI study. Neuroimage. 2007;35:1168-80. doi: 10.1016/j.neuroimage.2007.01.021

28. Jones AKP, Derbyshire SWG. Reduced cortical responses to noxious heat in patients with rheumatoid arthritis. Ann Rheum Dis. 1997;56:601-7. doi: 10.1136/ard.56.10.601

29. Keefe FJ, Caldwell DS, Martinez S, et al. Analyzing pain in rheumatoid arthritis patients. Pain coping strategies in patients who have had knee replacement surgery. Pain. 1991;46(2):153-60. doi: 10.1016/0304-3959(91)90070-E

30. [Nasonov EL, Olyunin YuA, Lila AM. Rheumatoid arthritis: the problems of remission and therapy resistance. Nauchno-Prakticheskaya Revmatologiya = Rheumatology Science and Practice. 2018;56(3):263-71 (In Russ.)]. doi: 10.14412/1995-4484-2018-263-271

31. Schweinhardt P, Kalk N, Wartolowska K, et al. Investigation into the neural correlates of emotional augmentation of clinical pain. Neuroimage. 2008;40(2):759-66. doi: 10.1016/j.neuroim-age.2007.12.016

32. Nahit ES, Pritchard CM, Cherry NM, et al. The influence of work related psychosocial factors and psychological distress on regional musculoskeletal pain: a study of newly employed workers. J Rheumatol. 2001;28(6):1378-84.

33. Flodin P, Martinsen S, Altawil R, et al. Intrinsic Brain Connectivity in Chronic Pain: A resting-state fMRI Study in patients with rheumatoid arthritis. Front Hum Neurosci. 2016;10:107. doi: 10.3389/fnhum.2016.00107

34. Boettger MK, Hensellek S, Richter F, et al. Antinociceptive effects of tumor necrosis factor alpha neutralization in a rat model of antigen-induced arthritis: evidence of a neuronal target. Arthritis Rheum. 2008;58:2368-78. doi: 10.1002/art.23608

35. Hess A, Axmannb R, Rechb J, et al. Blockade of TNF-a rapidly inhibits pain responses in the central nervous system. Proc Natl Acad Sci. 2011;108(9):3731-6. doi: 10.1073/pnas.1011774108

36. Rech J, Hess A, Finzel S, et al. Association of brain functional magnetic resonance activity with response to tumor necrosis factor inhibition in rheumatoid arthritis. Arthritis Rheum. 2013;65(2):325-33. doi: 10.1002/art.37761

37. Basu N, Kaplan CM, Ichesco E, et al. Neurobiologic features of fibromyalgia are also present among rheumatoid arthritis patients. Arthritis Rheum. 2018;70:1000-7. doi: 10.1002/art.40451

38. Kaplan CM, Schrepf A, Ichesco E, et al. Inflammation is associated with pro-nociceptive brain connections in rheumatoid arthritis patients with concomitant fibromyalgia. Arthritis Rheum. 2019 Aug 5. doi: 10.1002/art.41069

39. Basu N, Kaplan CM, Ichesco E, et al. Functional and structural magnetic resonance imaging correlates of fatigue in patients with rheumatoid arthritis. Rheumatology (Oxford). 2019 Oct 1;58(10):1822-30. doi: 10.1093/rheumatology/kez132

40. Schrepf A, Kaplan CM, Ichesco E, et al. A multi-modal MRI study of the central response to inflammation in rheumatoid arthritis. Nat Commun. 2018 Jun 8;9(1):2243. doi: 10.1038/s41467-018-04648-0

41. Gibson S, Littlejohn G, Gorman M, et al. Altered heat pain thresholds and cerebral event-related potentials following painful CO2 laser stimulation in subjects with fibromyalgia syndrome. Pain. 1994;58(2):185-93. doi: 10.1016/0304-3959(94)90198-8

42. Lorenz J, Grasedyck K, Bromm B. Middle and long latency somatosensory evoked potentials after painful laser stimulation in patients with fibromyalgia syndrome. Electroencephalogr Clin Neurophysiol. 1996;100(2):165-8. doi: 10.1016/0013-4694(95)00259-6

43. Stevens A, Batra A, Ko tter I, et al. Both pain and EEG response to cold pressor stimulation occurs faster in fibromyalgia patients than in control subjects. Psychiatry Res. 2000;97(2-3):237-47. doi: 10.1016/S0165-1781(00)00223-7

44. Cook DB, Lange G, Ciccone DS, et al. Functional imaging of pain in patients with primary fibromyalgia. J Rheumatol. 2004;31(2):364-78.

45. Staud R, Smitherman ML. Peripheral and central sensitization in fibromyalgia: pathogenetic role. Curr Pain Headache Rep. 2002;6(4):259-66. doi: 10.1007/s11916-002-0046-1

46. Jones AKP, Huneke NTM, Lloyd DM, et al. Role of Functional Brain Imaging in Understanding Rheumatic Pain. Curr Rheumatol Rep. 2012;14:557. doi: 10.1007/s11926-012-0287-x

47. Wik G, Fischer H, Finer B, et al. Retrospenial cortical deactivation during painful stimulation of fibromyalgia patients. Int J Neurosci. 2006;116(1):1-8. doi: 10.1080/00207450690962208

48. Jensen KB, Kosek E, Petzke F, et al. Evidence of dysfunctional pain inhibition in fibromyalgia reflected in rACC during provoked pain. Pain. 2009;144(1-2):95-100. doi: 10.1016/j.pain.2009.03.018

49. Pujol J, Lopez-Sola M, Ortiz H, et al. Mapping brain response to pain in fibromyalgia patients using temporal analysis of FMRI. PLoSOne. 2009;4(4):5224. doi: 10.1371/journal.pone.0005224

50. Crombez G, Eccleston C, van den Broeck A, et al. Hypervigilance to pain in fibromyalgia: the mediating role of pain intensity and catastrophic thinking about pain. Clin J Pain. 2004;20:98-102. doi: 10.1097/00002508-200403000-00006

51. Gracely RH, Geisser ME, Giesecke T, et al. Pain catastrophizing and neural responses to pain among persons with fibromyalgia. Brain. 2004;127(4):835-43. doi: 10.1093/brain/awh098

52. Robinson ME, Craggs JG, Price DD, et al. Gray matter volumes of pain-related brain areas are decreased in fibromyalgia syndrome. J Pain. 2011;12(4):436-43. doi: 10.1016/j.jpain.2010.10.003


Review

For citations:


Filatova E.S., Karateev A.E., Lila A.M., Nasonov E.L. Functional magnetic resonance imaging for chronic pain in patients with rheumatic diseases. Rheumatology Science and Practice. 2019;57(6):612-617. (In Russ.) https://doi.org/10.14412/1995-4484-2019-612-617

Views: 925


Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 License.


ISSN 1995-4484 (Print)
ISSN 1995-4492 (Online)