Musculoskeletal pain in Parkinson's disease: Association with dopaminergic deficiency in the caudate nucleus.


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:
16 Aug 2023
Historique:
revised: 09 07 2023
received: 08 05 2023
accepted: 01 08 2023
medline: 17 8 2023
pubmed: 17 8 2023
entrez: 17 8 2023
Statut: aheadofprint

Résumé

Musculoskeletal (MSK) pain affects over 80% of People with Parkinson's (PD, PwP) and may, in part, be dopaminergic in origin, as dopaminergic medication often leads to its relief. PwP who underwent striatal dopamine transporter visualization with a radiopharmaceutical DaTscan™ ( 53 PwP (30.2% female; age: 63.79 ± 11.31 years; disease duration (DD): 3.32 (0.31-14.41) years; Hoehn & Yahr stage (H&Y): 2 (1-4); Levodopa Equivalent Daily Dose (LEDD): 543.08 ± 308.94 mg) were assessed and included in this analysis. MSK pain was highly prevalent (71.7% of all participants, mean KPPS Item 1 score 5.34 ± 4.76) and did not correlate with the motor symptoms burden (SCOPA-Motor total score; p = 0.783) but showed a significant correlation with quality of life (PDQ-8, r Our findings suggest an association between MSK pain in PwP and the severity of dopaminergic deficiency in the caudate nucleus. In People with Parkinson's, musculoskeletal pain does not arise simply as a direct sequel to motor symptoms-instead, it is linked to the severity of dopaminergic depletion in the caudate nucleus.

Sections du résumé

BACKGROUND BACKGROUND
Musculoskeletal (MSK) pain affects over 80% of People with Parkinson's (PD, PwP) and may, in part, be dopaminergic in origin, as dopaminergic medication often leads to its relief.
METHODS METHODS
PwP who underwent striatal dopamine transporter visualization with a radiopharmaceutical DaTscan™ (
RESULTS RESULTS
53 PwP (30.2% female; age: 63.79 ± 11.31 years; disease duration (DD): 3.32 (0.31-14.41) years; Hoehn & Yahr stage (H&Y): 2 (1-4); Levodopa Equivalent Daily Dose (LEDD): 543.08 ± 308.94 mg) were assessed and included in this analysis. MSK pain was highly prevalent (71.7% of all participants, mean KPPS Item 1 score 5.34 ± 4.76) and did not correlate with the motor symptoms burden (SCOPA-Motor total score; p = 0.783) but showed a significant correlation with quality of life (PDQ-8, r
CONCLUSIONS CONCLUSIONS
Our findings suggest an association between MSK pain in PwP and the severity of dopaminergic deficiency in the caudate nucleus.
SIGNIFICANCE CONCLUSIONS
In People with Parkinson's, musculoskeletal pain does not arise simply as a direct sequel to motor symptoms-instead, it is linked to the severity of dopaminergic depletion in the caudate nucleus.

Identifiants

pubmed: 37587725
doi: 10.1002/ejp.2172
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : National Institute for Health Research
Organisme : Mental Health Biomedical Research Centre
Organisme : Dementia Unit at South London
Organisme : Maudsley NHS Foundation Trust
Organisme : King's College London

Informations de copyright

© 2023 The Authors. European Journal of Pain published by John Wiley & Sons Ltd on behalf of European Pain Federation - EFIC ®.

Références

Bega, D., Kuo, P. H., Chalkidou, A., Grzeda, M. T., Macmillan, T., Brand, C., Sheikh, Z. H., & Antonini, A. (2021). Clinical utility of DaTscan in patients with suspected parkinsonian syndrome: A systematic review and meta-analysis. NPJ Parkinsons Disease, 7(1), 43. https://doi.org/10.1038/s41531-021-00185-8
Blanchet, P. J., & Brefel-Courbon, C. (2018). Chronic pain and pain processing in Parkinson's disease. Progress in Neuro-Psychopharmacology & Biological Psychiatry, 87(Pt B), 200-206. https://doi.org/10.1016/j.pnpbp.2017.10.010
Carbon, M., Ma, Y., Barnes, A., Dhawan, V., Chaly, T., Ghilardi, M. F., & Eidelberg, D. (2004). Caudate nucleus: Influence of dopaminergic input on sequence learning and brain activation in parkinsonism. NeuroImage, 21(4), 1497-1507. https://doi.org/10.1016/j.neuroimage.2003.12.014
Chaudhuri, K. R., Rizos, A., Trenkwalder, C., Rascol, O., Pal, S., Martino, D., Carroll, C., Paviour, D., Falup-Pecurariu, C., Kessel, B., Silverdale, M., Todorova, A., Sauerbier, A., Odin, P., Antonini, A., Martinez-Martin, P., & EUROPAR and the IPMDS Non Motor PD Study Group. (2015). King's Parkinson's disease pain scale, the first scale for pain in PD: An international validation. Movement Disorders, 30(12), 1623-1631. https://doi.org/10.1002/mds.26270
Dorsey, E. R., Sherer, T., Okun, M. S., & Bloem, B. R. (2018). The emerging evidence of the Parkinson pandemic. Journal of Parkinson's Disease, 8(s1), S3-S8. https://doi.org/10.3233/JPD-181474
Driscoll, M. E., Bollu, P. C., & Tadi, P. (2022). Neuroanatomy. Nucleus Caudate. In StatPearls.
EMA. (2010). https://www.ema.europa.eu/en/documents/product-information/datscan-epar-product-information_en.pdf
Farnikova, K., Krobot, A., & Kanovsky, P. (2012). Musculoskeletal problems as an initial manifestation of Parkinson's disease: A retrospective study. Journal of the Neurological Sciences, 319(1-2), 102-104. https://doi.org/10.1016/j.jns.2012.05.002
Ghosh, P., Imbriani, P., Caputi, N., Natoli, S., Schirinzi, T., di Lazzaro, G., Covington, L., Sparks, A. D., Salnikova, Y., Rukavina, K., Ray Chaudhuri, K., & Pisani, A. (2020). A dual centre study of pain in Parkinson's disease and its relationship with other non-motor symptoms. Journal of Parkinson's Disease, 10(4), 1817-1825. https://doi.org/10.3233/JPD-202088
Grigoriou, S., Martínez-Martín, P., Ray Chaudhuri, K., Rukavina, K., Leta, V., Hausbrand, D., Falkenburger, B., Odin, P., & Reichmann, H. (2021). Effects of safinamide on pain in patients with fluctuating Parkinson's disease. Brain and Behavior: A Cognitive Neuroscience Perspective, 11(10), e2336. https://doi.org/10.1002/brb3.2336
Hoehn, M. M., & Yahr, M. D. (1967). Parkinsonism: Onset, progression and mortality. Neurology, 17(5), 427-442. https://doi.org/10.1212/wnl.17.5.427
ICD-11. (2019/2021). International Classification of Diseases, Eleventh Revision (ICD-11), World Health Organization (WHO). https://icd.who.int/browse11. Licensed under Creative Commons Attribution-NoDerivatives 3.0 IGO licence (CC BY-ND 3.0 IGO)
Jääskeläinen, S. K., Lindholm, P., Valmunen, T., Pesonen, U., Taiminen, T., Virtanen, A., Lamusuo, S., Forssell, H., Hagelberg, N., Hietala, J., & Pertovaara, A. (2014). Variation in the dopamine D2 receptor gene plays a key role in human pain and its modulation by transcranial magnetic stimulation. Pain, 155(10), 2180-2187. https://doi.org/10.1016/j.pain.2014.08.029
Jenkinson, C., Fitzpatrick, R., Peto, V., Greenhall, R., & Hyman, N. (1997). The Parkinson's disease questionnaire (PDQ-39): Development and validation of a Parkinson's disease summary index score. Age and Ageing, 26(5), 353-357. https://www.ncbi.nlm.nih.gov/pubmed/9351479
Jeong, S. H., Lee, H. S., Jung, J. H., Baik, K., Lee, Y. H., Yoo, H. S., Sohn, Y. H., Chung, S. J., & Lee, P. H. (2021). White matter hyperintensities, dopamine loss, and motor deficits in De novo Parkinson's disease. Movement Disorders, 36(6), 1411-1419. https://doi.org/10.1002/mds.28510
Jeong, S. H., Park, C. W., Lee, H. S., Kim, Y. J., Yun, M., Lee, P. H., Sohn, Y. H., & Chung, S. J. (2022). Patterns of striatal dopamine depletion and motor deficits in de novo Parkinson's disease. Journal of Neural Transmission (Vienna), 130, 19-28. https://doi.org/10.1007/s00702-022-02571-9
Lawn, T., Aman, Y., Rukavina, K., Sideris-Lampretsas, G., Howard, M., Ballard, C., Ray Chaudhuri, K., & Malcangio, M. (2021). Pain in the neurodegenerating brain: Insights into pharmacotherapy for Alzheimer disease and Parkinson disease. Pain, 162(4), 999-1006. https://doi.org/10.1097/j.pain.0000000000002111
Li, J., Zhu, B. F., Gu, Z. Q., Zhang, H., Mei, S. S., Ji, S. Z., Liu, S. Y., Han, C., Chen, H. Z., & Chan, P. (2021). Musculoskeletal pain in Parkinson's disease. Frontiers in Neurology, 12, 756538. https://doi.org/10.3389/fneur.2021.756538
Lien, W. H., Lien, W. C., Kuan, T. S., Wu, S. T., Chen, Y. T., & Chiu, C. J. (2017). Parkinson disease and musculoskeletal pain: An 8-year population-based cohort study. Pain, 158(7), 1234-1240. https://doi.org/10.1097/j.pain.0000000000000904
Liu, S. Y., Wu, J. J., Zhao, J., Huang, S. F., Wang, Y. X., Ge, J. J., Wu, P., Zuo, C. T., Ding, Z. T., & Wang, J. (2015). Onset-related subtypes of Parkinson's disease differ in the patterns of striatal dopaminergic dysfunction: A positron emission tomography study. Parkinsonism & Related Disorders, 21(12), 1448-1453. https://doi.org/10.1016/j.parkreldis.2015.10.017
Martikainen, I. K., Hagelberg, N., Jaaskelainen, S. K., Hietala, J., & Pertovaara, A. (2018). Dopaminergic and serotonergic mechanisms in the modulation of pain: In vivo studies in human brain. European Journal of Pharmacology, 834, 337-345. https://doi.org/10.1016/j.ejphar.2018.07.038
Martikainen, I. K., Nuechterlein, E. B., Peciña, M., Love, T. M., Cummiford, C. M., Green, C. R., Stohler, C. S., & Zubieta, J. K. (2015). Chronic back pain is associated with alterations in dopamine neurotransmission in the ventral striatum. The Journal of Neuroscience, 35(27), 9957-9965. https://doi.org/10.1523/JNEUROSCI.4605-14.2015
Martin, S. L., Jones, A. K. P., Brown, C. A., Kobylecki, C., Whitaker, G. A., El-Deredy, W., & Silverdale, M. A. (2022). Altered pain processing associated with administration of Dopamine Agonist and Antagonist in healthy volunteers. Brain Sciences, 12(3), 351. https://doi.org/10.3390/brainsci12030351
Martínez-Martín, P., Benito-León, J., Burguera, J. A., Castro, A., Linazasoro, G., Martínez-Castrillo, J. C., Valldeoriola, F., Vázquez, A., Vivancos, F., del Val, J., van Blercom, N., & Frades, B. (2005). The SCOPA-motor scale for assessment of Parkinson's disease is a consistent and valid measure. Journal of Clinical Epidemiology, 58(7), 674-679. https://doi.org/10.1016/j.jclinepi.2004.09.014
Oshiro, Y., Quevedo, A. S., McHaffie, J. G., Kraft, R. A., & Coghill, R. C. (2007). Brain mechanisms supporting spatial discrimination of pain. The Journal of Neuroscience, 27(13), 3388-3394. https://doi.org/10.1523/JNEUROSCI.5128-06.2007
Pasquini, J., Durcan, R., Wiblin, L., Gersel Stokholm, M., Rochester, L., Brooks, D. J., Burn, D., & Pavese, N. (2019). Clinical implications of early caudate dysfunction in Parkinson's disease. Journal of Neurology, Neurosurgery, and Psychiatry, 90(10), 1098-1104. https://doi.org/10.1136/jnnp-2018-320157
Perez-Lloret, S., Ciampi de Andrade, D., Lyons, K. E., Rodríguez-Blázquez, C., Chaudhuri, K. R., Deuschl, G., Members of the MDS committee on rating scales development, Cruccu, G., Sampaio, C., Goetz, C. G., Schrag, A., Martinez-Martin, P., & Stebbins, G. (2016). Rating scales for pain in Parkinson's disease: Critique and recommendations. Movement Disorders Clinical Practice, 3(6), 527-537. https://doi.org/10.1002/mdc3.12384
Pirker, W. (2003). Correlation of dopamine transporter imaging with parkinsonian motor handicap: How close is it? Movement Disorders, 18(Suppl 7), S43-S51. https://doi.org/10.1002/mds.10579
Qamar, M. A., Sauerbier, A., Politis, M., Carr, H., Loehrer, P., & Chaudhuri, K. R. (2017). Presynaptic dopaminergic terminal imaging and non-motor symptoms assessment of Parkinson's disease: Evidence for dopaminergic basis? NPJ Parkinsons Disease, 3, 5. https://doi.org/10.1038/s41531-016-0006-9
Rizos, A., Martinez-Martin, P., Odin, P., Antonini, A., Kessel, B., Kozul, T. K., Todorova, A., Douiri, A., Martin, A., Stocchi, F., Dietrichs, E., Chaudhuri, K. R., & EUROPAR and the IPDMDS non-Motor PD Study Group. (2014). Characterizing motor and non-motor aspects of early-morning off periods in Parkinson's disease: An international multicenter study. Parkinsonism & Related Disorders, 20(11), 1231-1235. https://doi.org/10.1016/j.parkreldis.2014.09.013
Rukavina, K., Batzu, L., Boogers, A., Abundes-Corona, A., Bruno, V., & Chaudhuri, K. R. (2021). Non-motor complications in late stage Parkinson's disease: Recognition, management and unmet needs. Expert Review of Neurotherapeutics, 21(3), 335-352. https://doi.org/10.1080/14737175.2021.1883428
Rukavina, K., Cummins, T. M., Chaudhuri, K. R., & Bannister, K. (2021). Pain in Parkinson's disease: Mechanism-based treatment strategies. Current Opinion in Supportive and Palliative Care, 15(2), 108-115. https://doi.org/10.1097/SPC.0000000000000546
Rukavina, K., Leta, V., Sportelli, C., Buhidma, Y., Duty, S., Malcangio, M., & Ray Chaudhuri, K. (2019). Pain in Parkinson's disease: New concepts in pathogenesis and treatment. Current Opinion in Neurology, 32(4), 579-588. https://doi.org/10.1097/WCO.0000000000000711
Rukavina, K., Ocloo, J., Skoric, M. K., Sauerbier, A., Thomas, O., Staunton, J., King's Parkinson's Disease Pain Scale Group, Awogbemila, O., Trivedi, D., Rizos, A., & Chaudhuri, K. R. (2022). Ethnic disparities in treatment of chronic pain in individuals with Parkinson's disease living in the United Kingdom. Movement Disorders Clinical Practice, 9(3), 369-374. https://doi.org/10.1002/mdc3.13430
Schade, S., Mollenhauer, B., & Trenkwalder, C. (2020). Levodopa equivalent dose conversion factors: An updated proposal including opicapone and safinamide. Movement Disorders Clinical Practice, 7(3), 343-345. https://doi.org/10.1002/mdc3.12921
Storch, A., Schneider, C. B., Wolz, M., Stürwald, Y., Nebe, A., Odin, P., Mahler, A., Fuchs, G., Jost, W. H., Chaudhuri, K. R., Koch, R., Reichmann, H., & Ebersbach, G. (2013). Nonmotor fluctuations in Parkinson disease: Severity and correlation with motor complications. Neurology, 80(9), 800-809. https://doi.org/10.1212/WNL.0b013e318285c0ed
Varrone, A., Dickson, J. C., Tossici-Bolt, L., Sera, T., Asenbaum, S., Booij, J., Kapucu, O. L., Kluge, A., Knudsen, G. M., Koulibaly, P. M., Nobili, F., Pagani, M., Sabri, O., Vander Borght, T., van Laere, K., & Tatsch, K. (2013). European multicentre database of healthy controls for [123I]FP-CIT SPECT (ENC-DAT): Age-related effects, gender differences and evaluation of different methods of analysis. European Journal of Nuclear Medicine and Molecular Imaging, 40(2), 213-227. https://doi.org/10.1007/s00259-012-2276-8
Weintraub, D., Newberg, A. B., Cary, M. S., Siderowf, A. D., Moberg, P. J., Kleiner-Fisman, G., Duda, J. E., Stern, M. B., Mozley, D., & Katz, I. R. (2005). Striatal dopamine transporter imaging correlates with anxiety and depression symptoms in Parkinson's disease. Journal of Nuclear Medicine, 46(2), 227-232. https://www.ncbi.nlm.nih.gov/pubmed/15695780
Wunderlich, A. P., Klug, R., Stuber, G., Landwehrmeyer, B., Weber, F., & Freund, W. (2011). Caudate nucleus and insular activation during a pain suppression paradigm comparing thermal and electrical stimulation. Open Neuroimaging Journal, 5, 1-8. https://doi.org/10.2174/1874440001105010001

Auteurs

Katarina Rukavina (K)

Institute of Psychiatry, Psychology & Neuroscience at King's College London, London, UK.
Parkinson's Foundation Centre of Excellence, King's College Hospital NHS Foundation Trust, London, UK.

Nicola Mulholland (N)

Department of Nuclear Medicine, King's College Hospital NHS Foundation Trust, London, UK.

Benjamin Corcoran (B)

Department of Nuclear Medicine, King's College Hospital NHS Foundation Trust, London, UK.

Magdalena Krbot Skoric (MK)

Laboratory for Cognitive and Experimental Neurophysiology, Department of Neurology, University Hospital Center Zagreb, Zagreb, Croatia.

Juliet Staunton (J)

Institute of Psychiatry, Psychology & Neuroscience at King's College London, London, UK.
Parkinson's Foundation Centre of Excellence, King's College Hospital NHS Foundation Trust, London, UK.

Silvia Rota (S)

Institute of Psychiatry, Psychology & Neuroscience at King's College London, London, UK.
Parkinson's Foundation Centre of Excellence, King's College Hospital NHS Foundation Trust, London, UK.

Pavlos Zinzalias (P)

Institute of Psychiatry, Psychology & Neuroscience at King's College London, London, UK.
Parkinson's Foundation Centre of Excellence, King's College Hospital NHS Foundation Trust, London, UK.

Kit Wu (K)

Parkinson's Foundation Centre of Excellence, King's College Hospital NHS Foundation Trust, London, UK.

Anna Fieldwalker (A)

Institute of Psychiatry, Psychology & Neuroscience at King's College London, London, UK.

Kirsty Bannister (K)

Institute of Psychiatry, Psychology & Neuroscience at King's College London, London, UK.

Alexandra Rizos (A)

Institute of Psychiatry, Psychology & Neuroscience at King's College London, London, UK.
Parkinson's Foundation Centre of Excellence, King's College Hospital NHS Foundation Trust, London, UK.

K Ray Chaudhuri (KR)

Institute of Psychiatry, Psychology & Neuroscience at King's College London, London, UK.
Parkinson's Foundation Centre of Excellence, King's College Hospital NHS Foundation Trust, London, UK.

Classifications MeSH