The interplay between cognition, depression, anxiety, and sleep in primary Sjogren's syndrome patients.


Journal

Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288

Informations de publication

Date de publication:
01 08 2022
Historique:
received: 15 11 2021
accepted: 25 07 2022
entrez: 1 8 2022
pubmed: 2 8 2022
medline: 4 8 2022
Statut: epublish

Résumé

Primary Sjögren's syndrome (pSS) is an autoimmune disease with frequent neurological involvement. Memory complaints are common, but their precise patterns remain unclear. We wanted to characterize patterns of neurocognitive profiles in pSS patients with cognitive complaints. Only pSS patients with memory complaints were included, prospectively. Cognitive profiles were compiled through a comprehensive cognitive evaluation by neuropsychologists. Evaluations of anxiety, depression, fatigue, sleep disorders and quality of life were performed for testing their interactions with cognitive profiles. All 32 pSS patients showed at least borderline cognitive impairment, and 17 (53%) exhibited a pathological cognitive profile: a hippocampal profile (37%), a dysexecutive profile (22%), and an instrumental profile (16%) (possible overlap). Regarding the secondary objectives: 37% of patients were depressed, and 48% exhibited a mild-to-severe anxiety trait. Sleep disorders were frequent (excessive daytime sleepiness (55%), high risk for sleep apnea (45%), and insomnia (77%)). Cognitive impairments could not be explained alone by anxiety, depression or sleep disorders. Fatigue level was strongly associated with sleep disorders. Our study highlights that cognitive complaints in pSS patients are supported by measurable cognitive impairments, apart from frequently associated disorders such as depression, anxiety or sleep troubles. Sleep disorders should be screened.

Identifiants

pubmed: 35915312
doi: 10.1038/s41598-022-17354-1
pii: 10.1038/s41598-022-17354-1
pmc: PMC9343365
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

13176

Informations de copyright

© 2022. The Author(s).

Références

Maciel, G. et al. Hospitalisation rates among patients with primary Sjögren’s syndrome: a population-based study, 1995–2016. RMD Open 4, e000575 (2018).
pubmed: 29531781 pmcid: 5845402 doi: 10.1136/rmdopen-2017-000575
Manzo, C., Martinez-Suarez, E., Kechida, M., Isetta, M. & Serra-Mestres, J. Cognitive function in primary Sjögren’s syndrome: A systematic review. Brain Sci. 9, 85 (2019).
pmcid: 6523842 doi: 10.3390/brainsci9040085
Delalande, S. et al. Neurologic manifestations in primary Sjögren syndrome: A study of 82 patients. Medicine (Baltimore) 83, 280–291 (2004).
doi: 10.1097/01.md.0000141099.53742.16
Morreale, M. et al. Neurological involvement in primary Sjögren syndrome: A focus on central nervous system. PLoS ONE 9, e84605 (2014).
pubmed: 24465419 pmcid: 3896357 doi: 10.1371/journal.pone.0084605
Blanc, F. et al. Cognitive dysfunction and dementia in primary Sjögren’s syndrome. ISRN Neurol. 2013, 501327 (2013).
pubmed: 24224097 pmcid: 3793286 doi: 10.1155/2013/501327
Koçer, B. et al. Cognition, depression, fatigue, and quality of life in primary Sjögren’s syndrome: Correlations. Brain Behav. 6, e00586 (2016).
pubmed: 28032007 pmcid: 5167008 doi: 10.1002/brb3.586
Faurholt-Jepsen, M. et al. Patient-evaluated cognitive function measured with smartphones and the association with objective cognitive function, perceived stress, quality of life and function capacity in patients with bipolar disorder. Int. J. Bipolar Disord. 8, 31 (2020).
pubmed: 33123812 pmcid: 7596112 doi: 10.1186/s40345-020-00205-1
Gairy, K., Knight, C., Anthony, P. & Hoskin, B. Burden of illness among subgroups of patients with primary Sjögren’s syndrome and systemic involvement. Rheumatology (Oxford) https://doi.org/10.1093/rheumatology/keaa508 (2020).
doi: 10.1093/rheumatology/keaa508
Riega-Torres, J. C. L. et al. Cognitive dysfunction in Sjögren’s syndrome using the montreal cognitive assessment questionnaire and the automated neuropsychological assessment metrics: A cross-sectional study. Int. J. Rheum. Dis. 23, 1019–1023 (2020).
pubmed: 32608054 doi: 10.1111/1756-185X.13889
Tezcan, M. E. et al. Primary Sjögren’s syndrome is associated with significant cognitive dysfunction. Int. J. Rheum. Dis. 19, 981–988 (2016).
pubmed: 27455357 doi: 10.1111/1756-185X.12912
Albrecht, K. et al. Comorbidity and health care utilisation in persons with Sjögren’s syndrome: A claims data analysis. Clin. Exp. Rheumatol. 38(Suppl 126), 78–84 (2020).
pubmed: 33025885
Yeh, T.-C. et al. Risk of obstructive sleep apnea in patients with Sjögren syndrome and Behçet’s disease: A nationwide, population-based cohort study. Sleep Breath. 24, 1199–1205 (2020).
pubmed: 31900884 doi: 10.1007/s11325-019-01953-w
Shiboski, C. H. et al. 2016 American college of rheumatology/European league against rheumatism classification criteria for primary Sjögren’s syndrome: A consensus and data-driven methodology involving three international patient cohorts. Ann. Rheum. Dis. 76, 9–16 (2017).
pubmed: 27789466 doi: 10.1136/annrheumdis-2016-210571
Seror, R. et al. Validation of EULAR primary Sjögren’s syndrome disease activity (ESSDAI) and patient indexes (ESSPRI). Ann. Rheum. Dis. 74, 859–866 (2015).
pubmed: 24442883 doi: 10.1136/annrheumdis-2013-204615
Poitrenaud, J., Eustache, F. & Agniel, A. Neuropsychologie Clinique des Démences : Evaluations et Prise en Charge (Solal, 1995).
Thomas-Anterion, C., Honore-Masson, S., Berne, G., Ruel, J. & Laurent, B. Le questionnaire de plainte cognitive (QPC) : Un outil de recherche de plainte suspecte d’évoquer une maladie d’Alzheimer. In L’année gérontologique, pp. 56–65 (2003).
Folstein, M. F., Folstein, S. E. & McHugh, P. R. ‘Mini-mental state’. A practical method for grading the cognitive state of patients for the clinician. J. Psychiatr. Res. 12, 189–198 (1975).
pubmed: 1202204 doi: 10.1016/0022-3956(75)90026-6
Van der Linden, M. et al. L’épreuve de rappel libre/rappel indicé à 16 items (RL/RI-16). in Vol. L’évaluation des Troubles de la Mémoire. Présentation de Quatre Tests de Mémoire Episodique (Avec Leur Etalonnage) (Marseille : Solal, 2004).
Wechsler, D. Wechsler Adults Intelligence Scale WAIS-III (Editions du Centre de Psychologie Appliquée, 2000).
Tombaugh, T. Trail making test A and B: Normative data stratified by age and education. Arch. Clin. Neuropsychol. 19, 203–214 (2004).
pubmed: 15010086 doi: 10.1016/S0887-6177(03)00039-8
Berry, D., Allen, R. & Schmitt, F. Rey-Osterrieth complex figure: Psychometric characteristics in a geriatric sample. Clin. Neuropsychol. 5(2), 143–153 (1991).
doi: 10.1080/13854049108403298
Cardebat, D., Doyon, B., Puel, M., Goulet, P. & Joanette, Y. Formal and semantic lexical evocation in normal subjects performance and dynamics of production as a function of sex, age and educational level. Acta Neurol. Belg. 90, 207–217 (1990).
pubmed: 2124031
Stroop, J. Studies of interference in serial verbal reactions. J. Exp. Psychol. 18(6), 643–662 (1935).
doi: 10.1037/h0054651
Warrington, E. K. & Merle, J. The Visual Object and Space Perception Battery (Thames Valley Test Company, 1991).
Deloche, G. & Hannequin, D. Test de Dénomination Orale D’images. (les Editions du Centre de Psychologie Appliquée).
Peigneux, P. et al. A neuropsychological and functional brain imaging study of visuo-imitative apraxia. Rev. Neurol. (Paris) 156, 459–472 (2000).
Chalder, T. et al. Development of a fatigue scale. J. Psychosom. Res. 37, 147–153 (1993).
pubmed: 8463991 doi: 10.1016/0022-3999(93)90081-P
Schwarz, R., Krauss, O. & Hinz, A. Fatigue in the general population. Onkologie 26, 140–144 (2003).
pubmed: 12771522
Netzer, N. C., Stoohs, R. A., Netzer, C. M., Clark, K. & Strohl, K. P. Using the Berlin questionnaire to identify patients at risk for the sleep apnea syndrome. Ann. Intern. Med. 131, 485–491 (1999).
pubmed: 10507956 doi: 10.7326/0003-4819-131-7-199910050-00002
Johns, M. W. A new method for measuring daytime sleepiness: The Epworth sleepiness scale. Sleep 14, 540–545 (1991).
pubmed: 1798888 doi: 10.1093/sleep/14.6.540
Bastien, C. H., Vallières, A. & Morin, C. M. Validation of the Insomnia Severity Index as an outcome measure for insomnia research. Sleep Med. 2, 297–307 (2001).
pubmed: 11438246 doi: 10.1016/S1389-9457(00)00065-4
Beck, A. T., Ward, C. H., Mendelson, M., Mock, J. & Erbaugh, J. An inventory for measuring depression. Arch. Gen. Psychiatr. 4, 561–571 (1961).
pubmed: 13688369 doi: 10.1001/archpsyc.1961.01710120031004
Kosmadakis, C. S., Bungener, C., Pierson, A., Jouvent, R. & Widlöcher, D. Translation and validation of the revised social anhedonia scale (SAS Social Anhedonia Scale, M.L. Eckblad, L.J. Chapman et al., 1982). Study of the internal and concurrent validity in 126 normal subjects. Encephale 21, 437–443 (1995).
pubmed: 8674468
Gray-Little, B., Williams, V. & Hancock, T. An itemresponse theory analysis of the Rosenberg self-esteem scale. Personal. Soc. Psychol. Bull. 23(5), 443–451 (1997).
doi: 10.1177/0146167297235001
Spielberger, C. D. State-Trait Anxiety Inventory for Adults Sampler Set: Manual, Instrument and Scoring Guide (Mind Garden Inc, 1983).
Seeliger, T. et al. Cognitive impairment in patients with Neuro-Sjögren. Ann. Clin. Transl. Neurol. https://doi.org/10.1002/acn3.51123 (2020).
doi: 10.1002/acn3.51123 pubmed: 32628345 pmcid: 7448149
Yoshikawa, K. et al. Prevalence of Sjögren’s syndrome with dementia in a memory clinic. J. Neurol. Sci. 322, 217–221 (2012).
pubmed: 22901967 doi: 10.1016/j.jns.2012.07.060
Liliang, P.-C. et al. Population-based study suggests an increased risk of Alzheimer’sdisease in Sjögren’s syndrome. Clin. Rheumatol. 37, 935–941 (2018).
pubmed: 29243055 doi: 10.1007/s10067-017-3940-y
Lin, T.-M. et al. Autoimmune rheumatic diseases increase dementia risk in middle-aged patients: A nationwide cohort study. PLoS ONE 13, e0186475 (2018).
pubmed: 29304089 pmcid: 5755737 doi: 10.1371/journal.pone.0186475
Goulabchand, R. et al. Hospitalization risks for neurological disorders in primary Sjögren’s syndrome patients. J. Clin. Med. 11, 1979 (2022).
pubmed: 35407586 pmcid: 9000167 doi: 10.3390/jcm11071979
Hou, T.-Y. et al. Higher risk of dementia in primary Sjogren’s syndrome. Ann. Clin. Transl. Neurol. 6, 633–641 (2019).
pubmed: 31019988 pmcid: 6469245 doi: 10.1002/acn3.737
Pego-Reigosa, J. M., Restrepo Vélez, J., Baldini, C., Fernández, R.-F. & de Larrinoa, Í. Comorbidities (excluding lymphoma) in Sjögren’s syndrome. Rheumatology (Oxford) 60, 2075–2084 (2021).
doi: 10.1093/rheumatology/key329
Manzo, C., Serra-Mestres, J. & Isetta, M. Comment on: Comorbidities (excluding lymphoma) in Sjögren’s syndrome. Rheumatology https://doi.org/10.1093/rheumatology/keab602 (2021).
doi: 10.1093/rheumatology/keab602 pubmed: 34819707 pmcid: 8768041
Segal, B. et al. Primary Sjögren’s Syndrome: health experiences and predictors of health quality among patients in the United States. Health Qual Life Outcomes 7, 46 (2009).
pubmed: 19473510 pmcid: 2693523 doi: 10.1186/1477-7525-7-46
Liu, Z. et al. Health-related quality of life and psychological status of women with primary Sjögren’s syndrome: A cross-sectional study of 304 Chinese patients. Medicine (Baltimore) 96, e9208 (2017).
doi: 10.1097/MD.0000000000009208
Cui, Y. et al. Anxiety and depression in primary Sjögren’s syndrome: a cross-sectional study. BMC Psychiatr. 18, 1–8 (2018).
doi: 10.1186/s12888-018-1715-x
Hsieh, M.-C., Hsu, C.-W., Lu, M.-C. & Koo, M. Increased risks of psychiatric disorders in patients with primary Sjögren’s syndrome-a secondary cohort analysis of nationwide, population-based health claim data. Clin. Rheumatol. 38, 3195–3203 (2019).
pubmed: 31372849 doi: 10.1007/s10067-019-04705-z
Azarfar, A., Ahmed, A. & Bég, S. Prevalence of anxiety, depression, sleep disturbance, fibromyalgia, obesity, and gastroesophageal disease in patients with rheumatic diseases. Curr. Rheumatol. Rev. https://doi.org/10.2174/1573397116666201211124815 (2020).
doi: 10.2174/1573397116666201211124815
Segal, B. et al. Prevalence, severity, and predictors of fatigue in subjects with primary Sjögren’s syndrome. Arthritis Rheum. 59, 1780–1787 (2008).
pubmed: 19035421 pmcid: 3106978 doi: 10.1002/art.24311
Karageorgas, T. et al. Fatigue in primary Sjögren’s syndrome: Clinical, laboratory, psychometric, and biologic associations. Arthritis Care Res. (Hoboken) 68, 123–131 (2016).
doi: 10.1002/acr.22720
Dardin, L. P. et al. Correlation of sleep quality with fatigue and disease activity among patients with primary Sjögren’s syndrome: A cross-sectional study. Sao Paulo Med. J. 138, 146–151 (2020).
pubmed: 32159602 doi: 10.1590/1516-3180.2019.0251.r1.1912019
Cui, Y. et al. Prevalence, correlates, and impact of sleep disturbance in Chinese patients with primary Sjögren’s syndrome. Int. J. Rheum. Dis. 23, 367–373 (2020).
pubmed: 31763772 doi: 10.1111/1756-185X.13678
Usmani, Z. A. et al. Sleep disordered breathing in patients with primary Sjögren’s syndrome: A group controlled study. Sleep Med. 13, 1066–1070 (2012).
pubmed: 22841036 doi: 10.1016/j.sleep.2012.06.010
Davies, K. et al. Fatigue in primary Sjögren’s syndrome (pSS) is associated with lower levels of proinflammatory cytokines: A validation study. Rheumatol. Int. 39, 1867–1873 (2019).
pubmed: 31250166 pmcid: 6791914 doi: 10.1007/s00296-019-04354-0
Howard Tripp, N. et al. Fatigue in primary Sjögren’s syndrome is associated with lower levels of proinflammatory cytokines. RMD Open 2, e000282 (2016).
pubmed: 27493792 pmcid: 4964201 doi: 10.1136/rmdopen-2016-000282
Omdal, R., Mellgren, S. I. & Norheim, K. B. Pain and fatigue in primary Sjögren’s syndrome. Rheumatology (Oxford) https://doi.org/10.1093/rheumatology/kez027 (2019).
doi: 10.1093/rheumatology/kez027
Mekinian, A. et al. Primary Sjögren’s syndrome: Central and peripheral nervous system involvements. Clin. Exp. Rheumatol. 38(Suppl 126), 103–109 (2020).
pubmed: 33095149
Fauchais, A.-L., Magy, L. & Vidal, E. Central and peripheral neurological complications of primary Sjögren’s syndrome. Presse Med. 41, e485-493 (2012).
pubmed: 22840992 doi: 10.1016/j.lpm.2012.06.002
de Oliveira, F. R. et al. Neurological and inflammatory manifestations in Sjögren’s syndrome: The role of the Kynurenine metabolic pathway. Int. J. Mol. Sci. 19, 3953 (2018).
pmcid: 6321004 doi: 10.3390/ijms19123953
Del Papa, N. et al. The role of interferons in the pathogenesis of Sjögren’s syndrome and future therapeutic perspectives. Biomolecules 11, 251 (2021).
pubmed: 33572487 pmcid: 7916411 doi: 10.3390/biom11020251
Tjensvoll, A. B. et al. Neurofilament light is a biomarker of brain involvement in lupus and primary Sjögren’s syndrome. J. Neurol. https://doi.org/10.1007/s00415-020-10290-y (2020).
doi: 10.1007/s00415-020-10290-y pubmed: 33128084 pmcid: 7990817
Zhang, X.-D. et al. Altered hippocampal functional connectivity in primary Sjögren syndrome: A resting-state fMRI study. Lupus 29, 446–454 (2020).
pubmed: 32075510 doi: 10.1177/0961203320908936
Lauvsnes, M. B. et al. Loss of cerebral white matter in primary Sjögren’s syndrome: A controlled volumetric magnetic resonance imaging study. Eur. J. Neurol. 21, 1324–1329 (2014).
pubmed: 24943133 doi: 10.1111/ene.12486
Le Guern, V. et al. Cognitive function and 99mTc-ECD brain SPECT are significantly correlated in patients with primary Sjogren syndrome: a Case-control study. Ann. Rheum. Dis. 69, 132–137 (2010).
pubmed: 19158115 doi: 10.1136/ard.2008.090811
Miyamoto, S. T., Valim, V. & Fisher, B. A. Health-related quality of life and costs in Sjögren’s syndrome. Rheumatology (Oxford) https://doi.org/10.1093/rheumatology/key370 (2019).
doi: 10.1093/rheumatology/key370
Cornec, D. et al. Severe health-related quality of life impairment in active primary Sjögren’s syndrome and patient-reported outcomes: Data from a large therapeutic trial. Arthritis Care Res (Hoboken) 69, 528–535 (2017).
doi: 10.1002/acr.22974
Cui, Y. et al. The impact of disease activity and psychological status on quality of life for Chinese patients with primary Sjögren’s syndrome. Patient Prefer. Adherence 12, 1513–1519 (2018).
pubmed: 30174416 pmcid: 6110269 doi: 10.2147/PPA.S163417
Alunno, A. et al. Discrepancy between subjective symptoms, objective measures and disease activity indexes: The lesson of primary Sjögren’s syndrome. Clin. Exp. Rheumatol. 36(Suppl 112), 210–214 (2018).
pubmed: 30156545
Mæland, E., Miyamoto, S. T., Hammenfors, D., Valim, V. & Jonsson, M. V. Understanding fatigue in Sjögren’s syndrome: Outcome measures biomarkers and possible interventions. Front. Immunol. 12, 703079 (2021).
pubmed: 34249008 pmcid: 8267792 doi: 10.3389/fimmu.2021.703079
Bender, R. & Lange, S. Adjusting for multiple testing–when and how?. J. Clin. Epidemiol. 54, 343–349 (2001).
pubmed: 11297884 doi: 10.1016/S0895-4356(00)00314-0
Segal, B. M., Rhodus, N., Moser Sivils, K. L. & Solid, C. A. Validation of the brief cognitive symptoms index in Sjögren syndrome. J. Rheumatol. 41, 2027–2033 (2014).
pubmed: 25225280 doi: 10.3899/jrheum.140362

Auteurs

Radjiv Goulabchand (R)

Internal Medicine Department, CHU Nîmes, Place du Pr Debre, 30029, Nîmes Cedex, France. radjiv.goulabchand@chu-nimes.fr.
University of Montpellier, Montpellier, France. radjiv.goulabchand@chu-nimes.fr.
Inserm U1183, Institute for Regenerative Medicine and Biotherapy, St Eloi Hospital, Montpellier, France. radjiv.goulabchand@chu-nimes.fr.

Elodie Castille (E)

University of Montpellier, Montpellier, France.
Department of Internal Medicine and Multi-Organic Diseases, St Eloi Hospital, Montpellier University Hospital, Montpellier, France.

Sophie Navucet (S)

Department of Neurology, Memory Research and Resources Alzheimer Center, Gui de Chauliac Hospital, Montpellier University Hospital, Montpellier, France.
INM, Inserm, University of Montpellier, Montpellier, France.

Damien Etchecopar-Etchart (D)

Faculté de Médecine-Secteur Timone, EA 3279: CEReSS-Centre d'Etude et de Recherche sur les Services de Santé et la Qualité de vie, Aix-Marseille Université, Marseille, France.
Fondation FonaMental, Créteil, France.

Aurélie Matos (A)

Department of Neurology, Memory Research and Resources Alzheimer Center, Gui de Chauliac Hospital, Montpellier University Hospital, Montpellier, France.
INM, Inserm, University of Montpellier, Montpellier, France.

Alexandre Maria (A)

University of Montpellier, Montpellier, France.
Inserm U1183, Institute for Regenerative Medicine and Biotherapy, St Eloi Hospital, Montpellier, France.
Department of Internal Medicine and Multi-Organic Diseases, St Eloi Hospital, Montpellier University Hospital, Montpellier, France.

Laure Anne Gutierrez (LA)

University of Montpellier, Montpellier, France.
Department of Neurology, Memory Research and Resources Alzheimer Center, Gui de Chauliac Hospital, Montpellier University Hospital, Montpellier, France.
INM, Inserm, University of Montpellier, Montpellier, France.

Alain Le Quellec (A)

University of Montpellier, Montpellier, France.
Department of Internal Medicine and Multi-Organic Diseases, St Eloi Hospital, Montpellier University Hospital, Montpellier, France.

Nicolas Menjot de Champfleur (NM)

Department of Neuroradiology, I2FH, Institut d'Imagerie Fonctionnelle Humaine, Gui de Chauliac Hospital, Montpellier University Hospital, Montpellier, France.
Laboratoire Charles Coulomb, University of Montpellier, Montpellier, France.

Audrey Gabelle (A)

University of Montpellier, Montpellier, France.
Department of Neurology, Memory Research and Resources Alzheimer Center, Gui de Chauliac Hospital, Montpellier University Hospital, Montpellier, France.
INM, Inserm, University of Montpellier, Montpellier, France.

Philippe Guilpain (P)

University of Montpellier, Montpellier, France.
Inserm U1183, Institute for Regenerative Medicine and Biotherapy, St Eloi Hospital, Montpellier, France.
Department of Internal Medicine and Multi-Organic Diseases, St Eloi Hospital, Montpellier University Hospital, Montpellier, France.

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