Abstract
Objective
This study assessed the risk of Parkinson disease (PD) in patients with primary Sjögren’s syndrome (pSS) using a nationwide, population-based cohort during a 15-year follow-up period.
Method
We identified 17,028 patients with pSS by using the catastrophic illness registry in the Taiwan National Health Insurance Research Database, and 68,094 matched non-pSS controls.
Results
The pSS cohort showed a higher incidence of PD development than did the non-pSS cohort (1.60% vs. 1.17%, p = 0.0001). The adjusted hazard ratio (aHR) of developing PD was 1.23 times greater in the pSS group than in the non-pSS group. When stratified by sex, age, and comorbidities, the female patients with pSS and patients aged between 61 and 70 years were associated with a higher PD risk (aHR 1.28 and aHR 1.30, respectively). Patients with pSS with no other comorbidity had a higher risk of PD (aHR: 2.17), compared with the non-pSS patients with no other comorbidity. When comparing non-pSS patients without or with comorbidity with pSS without or with comorbidity, pSS patients with comorbidity had highest risk of PD (aHR: 3.814).
Conclusions
All of the above findings suggested that pSS is an independent risk factor for the development of PD.
Key Points •The patients with pSS had 1.23 times risk of Parkinson disease than the non-pSS group. •The female patients with pSS and patients aged between 61 and 70 years were associated with a higher PD risk (aHR 1.28 and aHR 1.30, respectively). •The pSS patients with comorbidity had highest risk of PD (aHR: 3.814). |
Similar content being viewed by others
References
Kapoor S (2014) Parkinsonism: an under-recognized neurological complication of Sjogren's syndrome. J Neurol Sci 338:235. https://doi.org/10.1016/j.jns.2013.12.014
Poewe W, Seppi K, Tanner CM, Halliday GM, Brundin P, Volkmann J, Schrag AE, Lang AE (2017) Parkinson disease. Nat Rev Dis Primers 3:17013. https://doi.org/10.1038/nrdp.2017.13
Hirsch EC, Hunot S (2009) Neuroinflammation in Parkinson's disease: a target for neuroprotection? Lancet Neurol 8:382–397. https://doi.org/10.1016/S1474-4422(09)70062-6
Wang Q, Liu Y, Zhou J (2015) Neuroinflammation in Parkinson's disease and its potential as therapeutic target. Transl Neurodegener 4:19. https://doi.org/10.1186/s40035-015-0042-0
Carvajal Alegria G, Guellec D, Mariette X, Gottenberg JE, Dernis E, Dubost JJ, Trouvin AP, Hachulla E, Larroche C, le Guern V, Cornec D, Devauchelle-Pensec V, Saraux A (2016) Epidemiology of neurological manifestations in Sjogren's syndrome: data from the French ASSESS Cohort. RMD Open 2:e000179. https://doi.org/10.1136/rmdopen-2015-000179
Visser LH, Koudstaal PJ, van de Merwe JP (1993) Hemiparkinsonism in a patient with primary Sjogren's syndrome. A case report and a review of the literature. Clin Neurol Neurosurg 95:141–145
Cebrian C, Loike JD, Sulzer D (2015) Neuroinflammation in Parkinson's disease animal models: a cell stress response or a step in neurodegeneration? Curr Top Behav Neurosci 22:237–270. https://doi.org/10.1007/7854_2014_356
Gagne JJ, Power MC (2010) Anti-inflammatory drugs and risk of Parkinson disease: a meta-analysis. Neurology 74:995–1002. https://doi.org/10.1212/WNL.0b013e3181d5a4a3
Rocha NP, de Miranda AS, Teixeira AL (2015) Insights into neuroinflammation in Parkinson's disease: from biomarkers to anti-inflammatory based therapies. Biomed Res Int 2015:628192. https://doi.org/10.1155/2015/628192
Thakur P, Nehru B (2015) Inhibition of neuroinflammation and mitochondrial dysfunctions by carbenoxolone in the rotenone model of Parkinson's disease. Mol Neurobiol 51:209–219. https://doi.org/10.1007/s12035-014-8769-7
Wu MC, Xu X, Chen SM, Tyan YS, Chiou JY, Wang YH, Lin LC, Chen CM, Wei JC (2017) Impact of Sjogren's syndrome on Parkinson's disease: a nationwide case-control study. PLoS One 12:e0175836. https://doi.org/10.1371/journal.pone.0175836
Chang CC, Lin TM, Chang YS, Chen WS, Sheu JJ, Chen YH, Chen JH (2018) Autoimmune rheumatic diseases and the risk of Parkinson disease: a nationwide population-based cohort study in Taiwan. Ann Med 50:83–90. https://doi.org/10.1080/07853890.2017.1412088
Ju UH, Liu FC, Lin CS, Wen-Yen Huang WY et al (2019) Risk of Parkinson disease in Sjögren syndrome administered ineffective immunosuppressant therapies: a nationwide population-based study. Medicine 98:14. https://doi.org/10.1097/MD.0000000000014984
Cheng TM (2015) Reflections on the 20th anniversary of Taiwan's single-payer National Health Insurance System. Health Aff (Millwood) 34:502–510. https://doi.org/10.1377/hlthaff.2014.1332
Weng MY, Huang YT, Liu MF, Lu TH (2011) Incidence and mortality of treated primary Sjogren's syndrome in Taiwan: a population-based study. J Rheumatol 38:706–708. https://doi.org/10.3899/jrheum.100883
Garcia-Carrasco M et al (2002) Primary Sjogren syndrome: clinical and immunologic disease patterns in a cohort of 400 patients. Medicine (Baltimore) 81:270–280
Morgen K, McFarland HF, Pillemer SR (2004) Central nervous system disease in primary Sjogrens syndrome: the role of magnetic resonance imaging. Semin Arthritis Rheum 34:623–630
Hassin-Baer S, Levy Y, Langevitz P, Nakar S, Ehrenfeld M (2007) Anti-beta2-glycoprotein I in Sjogren's syndrome is associated with parkinsonism. Clin Rheumatol 26:743–747. https://doi.org/10.1007/s10067-006-0398-8
Kobayashi S, Yamaguchi S, Suzuki T, Yamauchi K, Tsunematsu T (1986) Central nervous system involvement in primary Sjogren's syndrome. Rinsho Shinkeigaku 26:1009–1016
Mochizuki H, Okano M, Masaki T, Nagata N, Kamakura K (1997) A case of Sjogren's syndrome with a high titer of anticardiolipin antibody that developed as parkinsonism. Rinsho Shinkeigaku 37:57–59
Funding
This study received support from Wan Fang Hospital and Taipei Medical University (108TMU-WFH-20, DP2-108-21121-01-I-12).
Author information
Authors and Affiliations
Contributions
Hui-Ching Hsu and Tsung-Yun Hou contributed to study conception and design, article drafting, critical article revision for crucial intellectual content, and the final approval of the submitted version. Tzu-Min Lin and Yu-Sheng Chang contributed to data interpretation, critical article revision for crucial intellectual content, and the final approval of the submitted version. Wei-Sheng Chen and Pei-i Kuo contributed to data analysis, critical article revision for crucial intellectual content, and the final approval of the submitted version. Yi-Chun Lin contributed to data analysis, article drafting, and the final approval of the submitted version. Chi-Ching Chang and Jin-Hua Chen was responsible for study conception and design, complete data analysis, critical article revision for crucial intellectual content, and correspondence for the final approval of the submitted version.
Corresponding authors
Ethics declarations
Disclosures
None.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Hsu, HC., Hou, TY., Lin, TM. et al. Higher risk of Parkinson disease in patients with primary Sjögren’s syndrome. Clin Rheumatol 39, 2999–3007 (2020). https://doi.org/10.1007/s10067-020-05053-z
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10067-020-05053-z