Abstract
Background and aims
Recent evidence demonstrated that complex regional pain syndrome (CRPS) is associated with a larger than normal somatosensory (S1) representation of the healthy hand. The most intuitive mechanism for this apparent enlargement is increased, i.e. compensatory, use of the healthy hand. We investigated whether enlargement of the S1 representation of the healthy hand is associated with compensatory use in response to CRPS. Specifically, we were interested in whether the size of the S1 representation of the healthy hand is associated with the severity of functional impairment of the CRPS-affected hand. We were also interested in whether CRPS duration might be positively associated with the size of the representation of the healthy hand in S1.
Methods
Using functional magnetic resonance imaging (fMRI) data from our previous investigation, the size of the S1 representation of the healthy hand in CRPS patients (n = 12) was standardised to that of a healthy control sample (n = 10), according to hand dominance. Responses to questionnaires on hand function, overall function and self-efficacy were used to gather information on hand use in participants. Multiple regression analyses investigated whether the S1 representation was associated with compensatory use. We inferred compensatory use with the interaction between reported use of the CRPS-affected hand and (a) reported overall function, and (b) self-efficacy. We tested the correlation between pain duration and the size of the S1 representation of the healthy hand with Spearman’s rho.
Results
The relationship between the size of the S1 representation of the healthyh and and the interaction between use of the affected hand and overall function was small and non-significant ( β =-5.488×10-5, 95% C.I. –0.001, 0.001). The relationship between the size of the S1 representation of the healthy hand and the interaction between use of the affected hand and self-efficacy was also small and non-significant (β =-6.027×10-6, 95% C.I. –0.001, 0.001). The S1 enlargement of the healthy hand was not associated with pain duration (Spearman’s rho = –0.14, p = 0.67).
Conclusion
Our exploration did not yield evidence of any relationship between the size of the healthy hand representation in S1 and the severity of functional impairment of the CRPS-affected hand, relative to overall hand use or to self-efficacy. There was also no evidence of an association between the size of the healthy hand representation in S1 and pain duration. The enlarged S1 representation of the healthy hand does not relate to self-reported function and impairment in CRPS.
Implications
While this study had a hypothesis-generating nature and the sample was small, there were no trends to suggest compensatory use as the mechanism underlying the apparent enlargement of the healthy hand in S1. Further studies are needed to investigate the possibility that inter-hemispheric differences seen in S1 in CRPS may be present prior to the development of the disorder.
DOI of refers to article: http://dx.doi.org/10.1016/j.sjpain.2016.07.001.
Funding: FDP received support from an Australian Postgraduate Award and from an Early Career Fellowship from the National Health and Medical Research Council (NHMRC) ID 1091415. TRS received support from a fellowship from the Canadian Institutes of Health Research ID 223354 and from an Early Career Fellowship from NHMRC ID 1054041. TRS received travel and accommodation support from Eli Lilly Ltd. for speaking engagements in Western Canada (September 2014); this was unrelated to the present topic. GLM is supported by a Principal Research Fellowship from the NHMRC ID 1061279. GLM consults to Pfizer, Kaiser Permanente, Neuroorthopaedic Institute, and Workers’ Compensation Boards in Australia and North America. He receives payments for lectures and courses on pain and rehabilitation and he receives royalties for several books on pain. ML received support from the Federal Ministry of Education and Research (BMBF) NZL 11/005. JHM is supported by NHMRC Project ID 1047827. This work is supported by NHMRC Project Grant 630431.
Ethical issues: Please see Section 2.2.
Conflicts of interest: The authors report no potential conflicts of interest.
References
[1] Bruehl SP. An update on the pathophysiology of complex regional pain syndrome. Anesthesiology 2010;113:713–25.10.1097/ALN.0b013e3181e3db38Search in Google Scholar
[2] Marinus J, Moseley GL, Birklein F, Baron R, Maihofner C, Kingery WS, van Hilten JJ. Clinical features and pathophysiology of complex regional pain syndrome. Lancet Neurol 2011;10:637–48.10.1016/S1474-4422(11)70106-5Search in Google Scholar
[3] Schwenkreis P, Maier C, Tegenthoff M. Functional imaging of central nervous system involvement in complex regional pain syndrome. Am J Neuroradiol 2009;30:1279–84.10.3174/ajnr.A1630Search in Google Scholar
[4] Juottonen K, Gockel M, Silen T, Hurri H, Hari R, Forss N. Altered central sensorimotor processing in patients with complex regional pain syndrome. Pain 2002;98:315–23.10.1016/S0304-3959(02)00119-7Search in Google Scholar
[5] Maihöfner C, Handwerker HO, Neundörfer B, Birklein F. Patterns of cortical reorganization in complex regional pain syndrome. Neurology 2003;61:1707–15.10.1212/01.WNL.0000098939.02752.8ESearch in Google Scholar PubMed
[6] Pleger B, Tegenthoff M, Schwenkreis P, Janssen F, Ragert P, Dinse HR, Völker B, Zenz M, Maier C. Mean sustained pain levels are linked to hemispherical side-to-side differences of primary somatosensory cortex in the complex regional pain syndrome I. Exp Brain Res 2004;155:115–9.10.1007/s00221-003-1738-4Search in Google Scholar PubMed
[7] Vartiainen NV, Kirveskari E, Forss N. Central processing of tactile and nociceptive stimuli in complex regional pain syndrome. Clin Neurophysiol 2008;119:2380–8.10.1016/j.clinph.2008.06.008Search in Google Scholar PubMed
[8] Di Pietro F, McAuley JH, Parkitny L, Lotze M, Wand BM, Moseley GL, Stanton TR. Primary somatosensory cortex function in complex regional pain syndrome: a systematic review and meta-analysis. J Pain 2013;14:1001–18.10.1016/j.jpain.2013.04.001Search in Google Scholar PubMed
[9] Di Pietro F, McAuley JH, Parkitny L, Lotze M, Wand BM, Moseley GL, Stanton TR. Primary motor cortex function in complex regional pain syndrome: a systematic review and meta-analysis. J Pain 2013;14:1270–88.10.1016/j.jpain.2013.07.004Search in Google Scholar PubMed
[10] McCabe CS, Haigh RC, Ring EF, Halligan PW, Wall PD, Blake DR. A controlled pilot study of the utility of mirror visual feedback in the treatment of complex regional pain syndrome (type 1). Rheumatology 2003;42:97–101.10.1093/rheumatology/keg041Search in Google Scholar PubMed
[11] Moseley GL. Graded motor imagery is effective for long-standing complex regional pain syndrome: a randomised controlled trial. Pain 2004;108:192–8.10.1016/j.pain.2004.01.006Search in Google Scholar
[12] Di Pietro F, Stanton TR, Moseley GL, Lotze M, McAuley JH. Interhemispheric somatosensory differences in chronic pain reflect abnormality of the Healthy side. Hum Brain Mapp 2015;36:508–18.10.1002/hbm.22643Search in Google Scholar
[13] Elbert T, Pantev C, Wienbruch C, Rockstroh B, Taub E. Increased cortical representation of the fingers of the left hand in string players. Science 1995;270:305–7.10.1126/science.270.5234.305Search in Google Scholar
[14] Pascual-Leone A, Torres F. Plasticity of the sensorimotor cortex representation of the reading finger in Braille readers. Brain 1993;116:39–52.10.1093/brain/116.1.39Search in Google Scholar
[15] Merzenich MM, Kaas JH, Wall J, Nelson RJ, Sur M, Felleman D. Topographic reorganization of somatosensory cortical areas 3b and 1 in adult monkeys following restricted deafferentation. Neuroscience 1983;8:33–55.10.1016/0306-4522(83)90024-6Search in Google Scholar
[16] Nelson AJ, Chen R. Digit somatotopy within cortical areas of the postcentral gyrus in humans. Cereb Cortex 2008;18:2341–51.10.1093/cercor/bhm257Search in Google Scholar PubMed
[17] Jones LA, Lederman SJ. Neurophysiology of hand function. In: Human hand function. New York: Oxford University Press; 2006. p. 24–43.10.1093/acprof:oso/9780195173154.003.0003Search in Google Scholar
[18] Tommerdahl M, Delemos KA, Whitsel BL, Favorov OV, Metz CB. Response of anterior parietal cortex to cutaneous flutter versus vibration. J Neurophysiol 1999;82:16–33.10.1152/jn.1999.82.1.16Search in Google Scholar PubMed
[19] Butterworth S, Francis S, Kelly E, McGlone F, Bowtell R, Sawle GV. Abnormal cortical sensory activation in dystonia: an fMRI study. Mov Disord 2003;18:673–82.10.1002/mds.10416Search in Google Scholar PubMed
[20] Francis ST, Kelly EF, Bowtell R, Dunseath WJR, Folger SE, McGlone F. fMRI of the responses to vibratory stimulation of digit tips. Neuroimage 2000;11:188–202.10.1006/nimg.2000.0541Search in Google Scholar PubMed
[21] Nelson AJ, Staines WR, Graham SJ, McIlroy WE. Activation in SI and SII: the influence of vibrotactile amplitude during passive and task-relevant stimulation. Cogn Brain Res 2004;19:174–84.10.1016/j.cogbrainres.2003.11.013Search in Google Scholar
[22] Eickhoff SB, Stephan KE, Mohlberg H, Grefkes C, Fink GR, Amunts K, Zilles K. A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data. Neuroimage 2005;25:1325–35.10.1016/j.neuroimage.2004.12.034Search in Google Scholar
[23] Weibull A, Björkman A, Hall H, Rosén B, Lundborg G, Svensson J. Optimizing the mapping of finger areas in primary somatosensory cortex using functional MRI. Magn Reson Imaging 2008;26:1342–51.10.1016/j.mri.2008.04.007Search in Google Scholar
[24] Jung P, Baumgärtner U, Magerl W, Treede R-D. Hemispheric asymmetry of hand representation in human primary somatosensory cortex and handedness. Clin Neurophysiol 2008;119:2579–86.10.1016/j.clinph.2008.04.300Search in Google Scholar
[25] MacDermid JC. Development of a scale for patient rating of wrist pain and disability. J Hand Ther 1996;9:178–83.10.1016/S0894-1130(96)80076-7Search in Google Scholar
[26] Beaton DE, Wright JG, Katz JN. Development of the QuickDASH: comparison of three item-reduction approaches. J Bone Joint Surg 2005;87:1038–46.Search in Google Scholar
[27] Nicholas MK. Self-efficacy and chronic pain. In: Annual conference of the British Psychological Society. 1989.Search in Google Scholar
[28] Bandura A. Self-efficacy: toward a unifying theory of behavioral change. Psychol Rev 1977;84:191–215.10.1037/0033-295X.84.2.191Search in Google Scholar
[29] Arnstein P. The mediation of disability by self efficacy in different samples of chronic pain patients. Disabil Rehabil 2000;22:794–801.10.1080/09638280050200296Search in Google Scholar
[30] van der Pas SC, Verbunt JA, Breukelaar DE, van Woerden R, Seelen HA. Assessment of arm activity using triaxial accelerometry in patients with a stroke. Arch Phys Med Rehabil 2011;92:1437–42.10.1016/j.apmr.2011.02.021Search in Google Scholar
[31] O’Connor D, Kortman B, Smith A, Ahern M, Smith M, Krishnan J. Correlation between objective and subjective measures of hand function in patients with rheumatoid arthritis. J Hand Ther 1999;12:323–9.10.1016/S0894-1130(99)80071-4Search in Google Scholar
[32] Jung P, Baumgärtner U, Bauermann T, Magerl W, Gawehn J, Stoeter P, Treede R-D. Asymmetry in the human primary somatosensory cortex and handedness. Neuroimage 2003;19:913–23.10.1016/S1053-8119(03)00164-2Search in Google Scholar
[33] Sörös P, Knecht S, Imai T, Gürtler S, Lütkenhöner B, Ringelstein EB, Henningsen H. Cortical asymmetries of the human somatosensory hand representation in right- and left-handers. Neurosci Lett 1999;271:89–92.10.1016/S0304-3940(99)00528-5Search in Google Scholar
[34] Weibull A, Flondell M, Rosen B, Bjorkman A. Cerebral and clinical effects of short-term hand immobilisation. Eur J Neurosci 2011;33:699–704.10.1111/j.1460-9568.2010.07551.xSearch in Google Scholar PubMed
[35] Amunts K, Schlaug G, Schleicher A, Steinmetz H, Dabringhaus A, Roland PE, Zilles K. Asymmetry in the human motor cortex and handedness. Neuroimage 1996;4:216–22.10.1006/nimg.1996.0073Search in Google Scholar PubMed
[36] Volkmann J, Schnitzler A, Witte OW, Freund H-J. Handedness and asymmetry of hand representation in human motor cortex. J Neurophysiol 1998;79: 2149–54.10.1152/jn.1998.79.4.2149Search in Google Scholar PubMed
[37] Ragert P, Nierhaus T, Cohen LG, Villringer A. Interhemispheric interactions between the human primary somatosensory cortices. PLoS ONE 2011;6:e16150.10.1371/journal.pone.0016150Search in Google Scholar PubMed PubMed Central
[38] Schwenkreis P, Scherens A, Rönnau A-K, Höffken O, Tegenthoff M, Maier C. Cortical disinhibition occurs in chronic neuropathic, but not in chronic nociceptive pain. BMC Neurosci 2010;11:1–10.10.1186/1471-2202-11-73Search in Google Scholar PubMed PubMed Central
[39] Lenz M, Hoffken O, Stude P, Lissek S, Schwenkreis P, Reinersmann A, Frettloh J, Richter H, Tegenthoff M, Maier C. Bilateral somatosensory cortex disinhibition in complex regional pain syndrome type I. Neurology 2011;77: 1096–101.10.1212/WNL.0b013e31822e1436Search in Google Scholar PubMed
[40] Moseley GL, Gallace A, Spence C. Space-based, but not arm-based, shift in tactile processing in complex regional pain syndrome and its relationship to cooling of the affected limb. Brain 2009;132:3142–51.10.1093/brain/awp224Search in Google Scholar PubMed
[41] Moseley GL, Gallace A, Iannetti GD. Spatially defined modulation of skin temperature and hand ownership of both hands in patients with unilateral complex regional pain syndrome. Brain 2012;135:3676–86.10.1093/brain/aws297Search in Google Scholar PubMed
[42] Moseley GL, Gallace A, Di Pietro F, Spence C, Iannetti GD. Limb-specific autonomic dysfunction in complex regional pain syndrome modulated by wearing prism glasses. Pain 2013;154:2463–8.10.1016/j.pain.2013.07.026Search in Google Scholar PubMed
[43] Moseley GL, Gallagher L, Gallace A. Neglect-like tactile dysfunction in chronic back pain. Neurology 2012;79:327–32.10.1212/WNL.0b013e318260cba2Search in Google Scholar PubMed
[44] Stanton TR, Lin C-WC, Smeets RJEM, Taylor D, Law R, Lorimer Moseley G. Spatially defined disruption of motor imagery performance in people with osteoarthritis. Rheumatology 2012;51:1455–64.10.1093/rheumatology/kes048Search in Google Scholar PubMed
[45] Reid E, Wallwork SB, Harvie D, Chalmers KJ, Gallace A, Spence C, Moseley GL. A new kind of spatial inattention associated with chronic limb pain? Ann Neurol 2016;79:701–4.10.1002/ana.24616Search in Google Scholar PubMed
Appendix A. Supplementary data
Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/j.sjpain.2016.06.004.
© 2016 Scandinavian Association for the Study of Pain
