Explorative sensory profile evaluation in central neuropathic pain following spinal cord injury.
Journal
European journal of pain (London, England)
ISSN: 1532-2149
Titre abrégé: Eur J Pain
Pays: England
ID NLM: 9801774
Informations de publication
Date de publication:
31 Aug 2024
31 Aug 2024
Historique:
revised:
12
08
2024
received:
13
02
2024
accepted:
13
08
2024
medline:
31
8
2024
pubmed:
31
8
2024
entrez:
31
8
2024
Statut:
aheadofprint
Résumé
Sensory profiling in neuropathic pain using quantitative sensory testing (QST) has not been extended to central neuropathic pain due to spinal cord injury (SCI). This study aims to fill this gap by evaluating sensory profiles in patients with neuropathic SCI pain. We retrospectively analysed consecutive QST data from 62 patients with neuropathic spinal cord injury pain (SCIP), following the German Research Network on Neuropathic Pain protocol. The study included at-level and below-level SCIP due to a spinal cord lesion, and at-level SCIP following a cauda equina lesion. QST parameters were compared between diagnostic groups. QST profiles of below-level SCIP (central neuropathic pain) were manually assigned to sensory phenotypes based on literature and expert opinion. No statistical difference in QST parameters between pain diagnoses was found. For central neuropathic pain (below-level SCIP), three phenotypes were descriptively observed: loss of function (59%), thermal and mechanical hyperalgesia combination (16%), and mechanical hyperalgesia (19%). The remaining 5% of patients did not fit a common pattern. There was no statistical difference in clinical and psychological variables between phenotypes. In a subgroup analysis, the loss of function phenotype weakly correlated with older age, longer time since injury, and longer pain duration. Here, we capture sensory phenotypes of central neuropathic pain following SCI. The limited sample size, high rate of missing values, and the retrospective nature of the study mean that results should be seen as strictly exploratory. Further research should replicate these findings and explore the significance of phenotypes. The evaluation of sensory phenotypes by quantitative sensory testing in central neuropathic pain due to SCI adds a new perspective on sensory phenotypes in comparison to peripheral neuropathic pain. The described thermal and mechanical hyperalgesia combination might represent involvement of the spinothalamic tract. In addition, there was a trend towards older age and longer time since injury in patients with loss of function.
Sections du résumé
BACKGROUND
BACKGROUND
Sensory profiling in neuropathic pain using quantitative sensory testing (QST) has not been extended to central neuropathic pain due to spinal cord injury (SCI). This study aims to fill this gap by evaluating sensory profiles in patients with neuropathic SCI pain.
METHOD
METHODS
We retrospectively analysed consecutive QST data from 62 patients with neuropathic spinal cord injury pain (SCIP), following the German Research Network on Neuropathic Pain protocol. The study included at-level and below-level SCIP due to a spinal cord lesion, and at-level SCIP following a cauda equina lesion. QST parameters were compared between diagnostic groups. QST profiles of below-level SCIP (central neuropathic pain) were manually assigned to sensory phenotypes based on literature and expert opinion.
RESULTS
RESULTS
No statistical difference in QST parameters between pain diagnoses was found. For central neuropathic pain (below-level SCIP), three phenotypes were descriptively observed: loss of function (59%), thermal and mechanical hyperalgesia combination (16%), and mechanical hyperalgesia (19%). The remaining 5% of patients did not fit a common pattern. There was no statistical difference in clinical and psychological variables between phenotypes. In a subgroup analysis, the loss of function phenotype weakly correlated with older age, longer time since injury, and longer pain duration.
CONCLUSIONS
CONCLUSIONS
Here, we capture sensory phenotypes of central neuropathic pain following SCI. The limited sample size, high rate of missing values, and the retrospective nature of the study mean that results should be seen as strictly exploratory. Further research should replicate these findings and explore the significance of phenotypes.
SIGNIFICANCE STATEMENT
CONCLUSIONS
The evaluation of sensory phenotypes by quantitative sensory testing in central neuropathic pain due to SCI adds a new perspective on sensory phenotypes in comparison to peripheral neuropathic pain. The described thermal and mechanical hyperalgesia combination might represent involvement of the spinothalamic tract. In addition, there was a trend towards older age and longer time since injury in patients with loss of function.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Informations de copyright
© 2024 European Pain Federation ‐ EFIC ®.
Références
Backonja, M. M., Attal, N., Baron, R., Bouhassira, D., Drangholt, M., Dyck, P. J., Edwards, R. R., Freeman, R., Gracely, R., Haanpaa, M. H., Hansson, P., Hatem, S. M., Krumova, E. K., Jensen, T. S., Maier, C., Mick, G., Rice, A. S., Rolke, R., Treede, R. D., … Ziegler, D. (2013). Value of quantitative sensory testing in neurological and pain disorders: NeuPSIG consensus. Pain, 154(9), 1807–1819. https://doi.org/10.1016/j.pain.2013.05.047
Baron, R., Maier, C., Attal, N., Binder, A., Bouhassira, D., Cruccu, G., Finnerup, N. B., Haanpaa, M., Hansson, P., Hullemann, P., Jensen, T. S., Freynhagen, R., Kennedy, J. D., Magerl, W., Mainka, T., Reimer, M., Rice, A. S., Segerdahl, M., Serra, J., … Treede, R. D. (2017). Peripheral neuropathic pain: A mechanism‐related organizing principle based on sensory profiles. Pain, 158(2), 261–272. https://doi.org/10.1097/j.pain.0000000000000753
Braunwalder, C., Ehrmann, C., Hodel, J., Müller, R., von Matt, D., & Fekete, C. (2022). Pain trajectories during initial rehabilitation after spinal cord injury: Do psychosocial resources and mental health predict trajectories? Archives of Physical Medicine and Rehabilitation, 103(7), 1294–1302. https://doi.org/10.1016/j.apmr.2022.01.149
Braunwalder, C., Müller, R., Kunz, S., Tough, H., Landmann, G., & Fekete, C. (2021). Psychosocial resources and chronic pain in individuals with spinal cord injury: Evidence from the second Swiss national community survey. Spinal Cord, 59(4), 410–418. https://doi.org/10.1038/s41393‐020‐00577‐2
Bryce, T. N., Biering‐Sorensen, F., Finnerup, N. B., Cardenas, D. D., Defrin, R., Lundeberg, T., Norrbrink, C., Richards, J. S., Siddall, P., Stripling, T., Treede, R. D., Waxman, S. G., Widerstrom‐Noga, E., Yezierski, R. P., & Dijkers, M. (2012). International spinal cord injury pain classification: Part I. Background and description. March 6‐7, 2009. Spinal Cord, 50(6), 413–417. https://doi.org/10.1038/sc.2011.156
Burke, D., Fullen, B. M., Stokes, D., & Lennon, O. (2017). Neuropathic pain prevalence following spinal cord injury: A systematic review and meta‐analysis. European Journal of Pain, 21(1), 29–44. https://doi.org/10.1002/ejp.905
Capossela, S., Landmann, G., Ernst, M., Stockinger, L., & Stoyanov, J. (2023). Assessing the feasibility of a multimodal approach to pain evaluation in early stages after spinal cord injury. International Journal of Molecular Sciences, 24(13), 11122 https://www.mdpi.com/1422‐0067/24/13/11122
Demant, D. T., Lund, K., Finnerup, N. B., Vollert, J., Maier, C., Segerdahl, M. S., Jensen, T. S., & Sindrup, S. H. (2015). Pain relief with lidocaine 5% patch in localized peripheral neuropathic pain in relation to pain phenotype: A randomised, double‐blind, and placebo‐controlled, phenotype panel study. Pain, 156(11), 2234–2244. https://doi.org/10.1097/j.pain.0000000000000266
Demant, D. T., Lund, K., Vollert, J., Maier, C., Segerdahl, M., Finnerup, N. B., Jensen, T. S., & Sindrup, S. H. (2014). The effect of oxcarbazepine in peripheral neuropathic pain depends on pain phenotype: A randomised, double‐blind, placebo‐controlled phenotype‐stratified study. Pain, 155(11), 2263–2273. https://doi.org/10.1016/j.pain.2014.08.014
Edwards, R. R., Dworkin, R. H., Turk, D. C., Angst, M. S., Dionne, R., Freeman, R., Hansson, P., Haroutounian, S., Arendt‐Nielsen, L., Attal, N., Baron, R., Brell, J., Bujanover, S., Burke, L. B., Carr, D., Chappell, A. S., Cowan, P., Etropolski, M., Fillingim, R. B., … Yarnitsky, D. (2016). Patient phenotyping in clinical trials of chronic pain treatments: IMMPACT recommendations. Pain, 157(9), 1851–1871. https://doi.org/10.1097/j.pain.0000000000000602
Ernst, M., Ljutow, A., Stockinger, L., Stoyanov, J., & Landmann, G. (2021). Variability in clinical and neurophysiological evaluation of pain development following acute spinal cord injury: A case report. Spinal Cord Series And Cases, 7(1), 72. https://doi.org/10.1038/s41394‐021‐00435‐0
Finnerup, N. B., & Baastrup, C. (2012). Spinal cord injury pain: Mechanisms and management. Current Pain and Headache Reports, 16(3), 207–216. https://doi.org/10.1007/s11916‐012‐0259‐x
Finnerup, N. B., Jensen, M. P., Norrbrink, C., Trok, K., Johannesen, I. L., Jensen, T. S., & Werhagen, L. (2016). A prospective study of pain and psychological functioning following traumatic spinal cord injury. Spinal Cord, 54(10), 816–821. https://doi.org/10.1038/sc.2015.236
Finnerup, N. B., Johannesen, I. L., Fuglsang‐Frederiksen, A., Bach, F. W., & Jensen, T. S. (2003). Sensory function in spinal cord injury patients with and without central pain. Brain, 126(Pt 1), 57–70. https://doi.org/10.1093/brain/awg007
Finnerup, N. B., Norrbrink, C., Trok, K., Piehl, F., Johannesen, I. L., Sørensen, J. C., Jensen, T. S., & Werhagen, L. (2014). Phenotypes and predictors of pain following traumatic spinal cord injury: A prospective study. The Journal of Pain, 15(1), 40–48. https://doi.org/10.1016/j.jpain.2013.09.008
Frettlöh, J., Maier, C., Gockel, H., & Hüppe, M. (2003). Validation of the German Mainz pain staging system in different pain syndromes. Schmerz, 17(4), 240–251. https://doi.org/10.1007/s00482‐003‐0227‐9 (Validität des Mainzer Stadienmodells der Schmerzchronifizierung bei unterschiedlichen Schmerzdiagnosen.).
Gerbershagen, U. (1986). Organized treatment of pain. Determination of status. Internist (Berl), 27(7), 459–469. (Organisierte Schmerzbehandlung. Eine Standortbestimmung.).
Gierthmuhlen, J., Maier, C., Baron, R., Tolle, T., Treede, R. D., Birbaumer, N., Huge, V., Koroschetz, J., Krumova, E. K., Lauchart, M., Maihofner, C., Richter, H., & Westermann, A. (2012). Sensory signs in complex regional pain syndrome and peripheral nerve injury. Pain, 153(4), 765–774. https://doi.org/10.1016/j.pain.2011.11.009
Hansen, C., Hopf, H. C., & Treede, R. D. (1996). Paradoxical heat sensation in patients with multiple sclerosis. Evidence for a supraspinal integration of temperature sensation. Brain, 119(Pt 5), 1729–1736. https://doi.org/10.1093/brain/119.5.1729
Kirshblum, S. C., Burns, S. P., Biering‐Sorensen, F., Donovan, W., Graves, D. E., Jha, A., Johansen, M., Jones, L., Krassioukov, A., Mulcahey, M. J., Schmidt‐Read, M., & Waring, W. (2011). International standards for neurological classification of spinal cord injury (revised 2011). The Journal of Spinal Cord Medicine, 34(6), 535–546. https://doi.org/10.1179/204577211x13207446293695
Krause, T., Asseyer, S., Geisler, F., Fiebach, J. B., Oeltjenbruns, J., Kopf, A., Villringer, K., Villringer, A., & Jungehulsing, G. J. (2016). Chronic sensory stroke with and without central pain is associated with bilaterally distributed sensory abnormalities as detected by quantitative sensory testing. Pain, 157(1), 194–202. https://doi.org/10.1097/j.pain.0000000000000354
Landmann, G., Berger, M. F., Stockinger, L., & Opsommer, E. (2017). Usefulness of laser‐evoked potentials and quantitative sensory testing in the diagnosis of neuropathic spinal cord injury pain: A multiple case study. Spinal Cord, 55(6), 575–582. https://doi.org/10.1038/sc.2016.191
Loh, E., Mirkowski, M., Agudelo, A. R., Allison, D. J., Benton, B., Bryce, T. N., Guilcher, S., Jeji, T., Kras‐Dupuis, A., Kreutzwiser, D., Lanizi, O., Lee‐Tai‐Fuy, G., Middleton, J. W., Moulin, D. E., O'Connell, C., Orenczuk, S., Potter, P., Short, C., Teasell, R., … Mehta, S. (2022). The CanPain SCI clinical practice guidelines for rehabilitation management of neuropathic pain after spinal cord injury: 2021 update. Spinal Cord, 60(6), 548–566. https://doi.org/10.1038/s41393‐021‐00744‐z
Lütolf, R., Rosner, J., Curt, A., & Hubli, M. (2021). Identifying Discomplete spinal lesions: New evidence from pain‐autonomic interaction in spinal cord injury. Journal of Neurotrauma, 38(24), 3456–3466. https://doi.org/10.1089/neu.2021.0280
Magerl, W., Krumova, E. K., Baron, R., Tolle, T., Treede, R. D., & Maier, C. (2010). Reference data for quantitative sensory testing (QST): Refined stratification for age and a novel method for statistical comparison of group data. Pain, 151(3), 598–605. https://doi.org/10.1016/j.pain.2010.07.026
Mahnig, S., Landmann, G., Stockinger, L., & Opsommer, E. (2016). Pain assessment according to the international spinal cord injury pain classification in patients with spinal cord injury referred to a multidisciplinary pain center. Spinal Cord, 54(10), 809–815. https://doi.org/10.1038/sc.2015.219
Maier, C., Baron, R., Tölle, T. R., Binder, A., Birbaumer, N., Birklein, F., Gierthmühlen, J., Flor, H., Geber, C., Huge, V., Krumova, E. K., Landwehrmeyer, G. B., Magerl, W., Maihöfner, C., Richter, H., Rolke, R., Scherens, A., Schwarz, A., Sommer, C., … Treede, D. R. (2010). Quantitative sensory testing in the German research network on neuropathic pain (DFNS): Somatosensory abnormalities in 1236 patients with different neuropathic pain syndromes. Pain, 150(3), 439–450. https://doi.org/10.1016/j.pain.2010.05.002
Müller, R., Landmann, G., Béchir, M., Hinrichs, T., Arnet, U., Jordan, X., & Brinkhof, M. W. G. (2017). Chronic pain, depression and quality of life in individuals with spinal cord injury: Mediating role of participation. Journal of Rehabilitation Medicine, 49(6), 489–496. https://doi.org/10.2340/16501977‐2241
Nilges, P., & Essau, C. (2015). Depression, anxiety and stress scales: DASS—A screening procedure not only for pain patients. Schmerz, 29(6), 649–657. https://doi.org/10.1007/s00482‐015‐0019‐z Die Depressions‐Angst‐Stress‐Skalen: Der DASS—ein Screeningverfahren nicht nur für Schmerzpatienten.
Opsommer, E., Korogod, N., Stockinger, L., & Landmann, G. (2021). Multimodal sensory evaluation of neuropathic spinal cord injury pain: An experimental study. Spinal Cord, 59(8), 842–854. https://doi.org/10.1038/s41393‐020‐00607‐z
Pfau, D. B., Krumova, E. K., Treede, R. D., Baron, R., Toelle, T., Birklein, F., Eich, W., Geber, C., Gerhardt, A., Weiss, T., Magerl, W., & Maier, C. (2014). Quantitative sensory testing in the German research network on neuropathic pain (DFNS): Reference data for the trunk and application in patients with chronic postherpetic neuralgia. Pain, 155(5), 1002–1015. https://doi.org/10.1016/j.pain.2014.02.004
Rolke, R., Baron, R., Maier, C., Tolle, T. R., Treede, R. D., Beyer, A., Binder, A., Birbaumer, N., Birklein, F., Botefur, I. C., Braune, S., Flor, H., Huge, V., Klug, R., Landwehrmeyer, G. B., Magerl, W., Maihofner, C., Rolko, C., Schaub, C., … Wasserka, B. (2006). Quantitative sensory testing in the German research network on neuropathic pain (DFNS): Standardized protocol and reference values. Pain, 123(3), 231–243. https://doi.org/10.1016/j.pain.2006.01.041
Siddall, P. J., McClelland, J. M., Rutkowski, S. B., & Cousins, M. J. (2003). A longitudinal study of the prevalence and characteristics of pain in the first 5 years following spinal cord injury. Pain, 103(3), 249–257. https://doi.org/10.1016/s0304‐3959(02)00452‐9
Smith, S. M., Dworkin, R. H., Turk, D. C., Baron, R., Polydefkis, M., Tracey, I., Borsook, D., Edwards, R. R., Harris, R. E., Wager, T. D., Arendt‐Nielsen, L., Burke, L. B., Carr, D. B., Chappell, A., Farrar, J. T., Freeman, R., Gilron, I., Goli, V., Haeussler, J., … Witter, J. (2017). The potential role of sensory testing, skin biopsy, and functional brain imaging as biomarkers in chronic pain clinical trials: IMMPACT considerations. The Journal of Pain, 18(7), 757–777. https://doi.org/10.1016/j.jpain.2017.02.429
Vogel, C., Rukwied, R., Stockinger, L., Schley, M., Schmelz, M., Schleinzer, W., & Konrad, C. (2017). Functional characterization of At‐level hypersensitivity in patients with spinal cord injury. The Journal of Pain, 18(1), 66–78. https://doi.org/10.1016/j.jpain.2016.10.003
Vollert, J., Maier, C., Attal, N., Bennett, D. L. H., Bouhassira, D., Enax‐Krumova, E. K., Finnerup, N. B., Freynhagen, R., Gierthmuhlen, J., Haanpaa, M., Hansson, P., Hullemann, P., Jensen, T. S., Magerl, W., Ramirez, J. D., Rice, A. S. C., Schuh‐Hofer, S., Segerdahl, M., Serra, J., … Baron, R. (2017). Stratifying patients with peripheral neuropathic pain based on sensory profiles: Algorithm and sample size recommendations. Pain, 158(8), 1446–1455. https://doi.org/10.1097/j.pain.0000000000000935
Von Korff, M., Ormel, J., Keefe, F. J., & Dworkin, S. F. (1992). Grading the severity of chronic pain. Pain, 50(2), 133–149. https://doi.org/10.1016/0304‐3959(92)90154‐4
Ware, J., Jr., Kosinski, M., & Keller, S. D. (1996). A 12‐item Short‐form health survey: Construction of scales and preliminary tests of reliability and validity. Medical Care, 34(3), 220–233. https://doi.org/10.1097/00005650‐199603000‐00003
Wasner, G., Lee, B. B., Engel, S., & McLachlan, E. (2008). Residual spinothalamic tract pathways predict development of central pain after spinal cord injury. Brain, 131(Pt 9), 2387–2400. https://doi.org/10.1093/brain/awn169
Wrigley, P. J., Press, S. R., Gustin, S. M., Macefield, V. G., Gandevia, S. C., Cousins, M. J., Middleton, J. W., Henderson, L. A., & Siddall, P. J. (2009). Neuropathic pain and primary somatosensory cortex reorganization following spinal cord injury. Pain, 141(1–2), 52–59. https://doi.org/10.1016/j.pain.2008.10.007
Wrigley, P. J., Siddall, P. J., & Gustin, S. M. (2018). New evidence for preserved somatosensory pathways in complete spinal cord injury: A fMRI study. Human Brain Mapping, 39(1), 588–598. https://doi.org/10.1002/hbm.23868
Yarnitsky, D., & Ochoa, J. L. (1990). Release of cold‐induced burning pain by block of cold‐specific afferent input. Brain, 113(Pt 4), 893–902. https://doi.org/10.1093/brain/113.4.893
Younis, S., Maarbjerg, S., Reimer, M., Wolfram, F., Olesen, J., Baron, R., & Bendtsen, L. (2016). Quantitative sensory testing in classical trigeminal neuralgia‐a blinded study in patients with and without concomitant persistent pain. Pain, 157(7), 1407–1414. https://doi.org/10.1097/j.pain.0000000000000528
Zanette, G., Cacciatori, C., & Tamburin, S. (2010). Central sensitization in carpal tunnel syndrome with extraterritorial spread of sensory symptoms. Pain, 148(2), 227–236. https://doi.org/10.1016/j.pain.2009.10.025
Zeilig, G., Enosh, S., Rubin‐Asher, D., Lehr, B., & Defrin, R. (2012). The nature and course of sensory changes following spinal cord injury: Predictive properties and implications on the mechanism of central pain. Brain, 135(Pt 2), 418–430. https://doi.org/10.1093/brain/awr270
Zigmond, A. S., & Snaith, R. P. (1983). The hospital anxiety and depression scale. Acta Psychiatrica Scandinavica, 67(6), 361–370. https://doi.org/10.1111/j.1600‐0447.1983.tb09716.x