Arthritis Care & Research

Volume 73, Issue 10 p. 1436-1443

Original Article

Cognitive Function Trajectories in Association With the Depressive Symptoms Trajectories in Systemic Lupus Erythematosus Over Time

Zahi Touma,

Corresponding Author

Zahi Touma

[email protected]

orcid.org/0000-0001-5177-2076

Toronto Western Hospital and University of Toronto, Toronto, Ontario, Canada

Address correspondence to Zahi Touma, MD, PhD, Division of Rheumatology, Department of Medicine, Institute of Health Policy, Management and Evaluation, University of Toronto, Toronto, Ontario, Canada (email: [email protected]); or to Patricia Katz, PhD, Professor of Medicine and Health Policy, Division of Rheumatology, Department of Medicine, Philip R. Lee Institute for Health Policy Studies, University of California San Francisco, San Francisco, CA 94143 (email: [email protected]).

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Bahar Moghaddam,

Bahar Moghaddam

Toronto Western Hospital and University of Toronto, Toronto, Ontario, Canada

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Jiandong Su,

Jiandong Su

Toronto Western Hospital and University of Toronto, Toronto, Ontario, Canada

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Patricia Katz,

Corresponding Author

Patricia Katz

[email protected]

orcid.org/0000-0002-8146-2519

University of California San Francisco

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Zahi Touma,

Corresponding Author

Zahi Touma

[email protected]

orcid.org/0000-0001-5177-2076

Toronto Western Hospital and University of Toronto, Toronto, Ontario, Canada

Search for more papers by this author

Bahar Moghaddam,

Bahar Moghaddam

Toronto Western Hospital and University of Toronto, Toronto, Ontario, Canada

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Jiandong Su,

Jiandong Su

Toronto Western Hospital and University of Toronto, Toronto, Ontario, Canada

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Patricia Katz,

Corresponding Author

Patricia Katz

[email protected]

orcid.org/0000-0002-8146-2519

University of California San Francisco

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First published: 11 June 2020

https://doi.org/10.1002/acr.24349

Citations: 15

The Lupus Outcomes Study was supported by the NIH/National Institute of Arthritis and Musculoskeletal and Skin Diseases (grant AR053308). Dr. Touma’s work was supported by the Arthritis Society Salary Support and by the Canadian Rheumatology Association Arthritis Society Clinician Investigator Salary Award.

No potential conflicts of interest relevant to this article were reported.

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Abstract

Objective

Cognitive function may change over time in patients with systemic lupus erythematosus (SLE), and cognitive function trajectories have not been well studied. We aimed to identify cognitive function trajectories in SLE and describe them with depressive symptoms trajectories, and we also aimed to identify baseline factors associated with class membership in the dual trajectories.

Methods

Longitudinal data from the University of California San Francisco Lupus Outcomes Study were analyzed. Two outcome trajectories were studied jointly, the Hopkins Verbal Learning Test–Revised and the Center for Epidemiologic Studies Depression Scale (CES-D) (administered annually). Univariate/multivariable logistic regression analyses examined baseline factors associated with class memberships.

Results

A total of 755 patients were studied, and 4 latent classes were identified: 1) low CES-D scores and low cognitive scores (no depression plus cognitive impairment; 20%), 2) lowest CES-D scores and highest normal cognitive scores (no depression plus normal cognition; 48%), 3) highest CES-D scores and lowest cognitive scores (depression plus cognitive impairment; 9%), and 4) high CES-D scores and cognitive score at borderline (depression plus borderline cognition; 23%).

Conclusion

In all, 4 distinct classes of dual cognitive function and depressive symptoms were identified. Persistently low cognitive performance in 28% of patients (classes 1 and 3) did not significantly improve over 7 years. Cognitive impairment was associated with depression status in 9% of patients (class 3). Other factors also predicted latent class membership: ethnicity, education, disease activity, physical functioning, and bodily pain. These results highlight the importance of periodic assessment of cognitive function and of different aspects relevant for assessing and managing cognitive function over time in SLE.

Supporting Information

References

1Hanly JG. Diagnosis and management of neuropsychiatric SLE. Nat Rev Rheumatol 2014; 10: 338–47.
10.1038/nrrheum.2014.15
CASPubMedWeb of Science®Google Scholar
2 ACR Ad Hoc Committee on Neuropsychiatric Lupus Nomenclature. The American College of Rheumatology nomenclature and case definitions for neuropsychiatric lupus syndromes. Arthritis Rheum 1999; 42: 599–608.
10.1002/1529-0131(199904)42:4<599::AID-ANR2>3.0.CO;2-F
PubMedWeb of Science®Google Scholar
3Rayes HA, Tani C, Kwan A, Marzouk S, Colosimo K, Medina-Rosas J, et al. What is the prevalence of cognitive impairment in lupus and which instruments are used to measure it? A systematic review and meta-analysis. Semin Arthritis Rheum 2018; 48: 240–55.
10.1016/j.semarthrit.2018.02.007
PubMedWeb of Science®Google Scholar
4Hanly JG, Su L, Omisade A, Farewell VT, Fisk JD. Screening for cognitive impairment in systemic lupus erythematosus. J Rheumatol 2012; 39: 1371–7.
10.3899/jrheum.111504
PubMedWeb of Science®Google Scholar
5Hanly JG, Omisade A, Su L, Farewell V, Fisk JD. Assessment of cognitive function in systemic lupus erythematosus, rheumatoid arthritis, and multiple sclerosis by computerized neuropsychological tests. Arthritis Rheum 2010; 62: 1478–86.
10.1002/art.27404
PubMedWeb of Science®Google Scholar
6Denburg SD, Carbotte RM, Denburg JA. Psychological aspects of systemic lupus erythematosus: cognitive function, mood, and self-report. J Rheumatol 1997; 24: 998–1003.

CASPubMedWeb of Science®Google Scholar
7Appenzeller S, Cendes F, Costallat LT. Cognitive impairment and employment status in systemic lupus erythematosus: a prospective longitudinal study. Arthritis Rheum 2009; 61: 680–7.
10.1002/art.24346
PubMedWeb of Science®Google Scholar
8Hanly JG, Cassell K, Fisk JD. Cognitive function in systemic lupus erythematosus: results of a 5-year prospective study [letter]. Arthritis Rheum 1997; 40: 1542–3.
10.1002/art.1780400825
CASPubMedWeb of Science®Google Scholar
9McCormick N, Trupin L, Yelin EH, Katz PP. Socioeconomic predictors of incident depression in systemic lupus erythematosus. Arthritis Care Res (Hoboken) 2018; 70: 104–13.
10.1002/acr.23247
PubMedWeb of Science®Google Scholar
10Julian LJ, Yazdany J, Trupin L, Criswell LA, Yelin E, Katz PP. Validity of brief screening tools for cognitive impairment in rheumatoid arthritis and systemic lupus erythematosus. Arthritis Care Res (Hoboken) 2012; 64: 448–54.
10.1002/acr.21566
PubMedWeb of Science®Google Scholar
11Moustafa AT, Moazzami M, Engel L, Bangert E, Hassanein M, Marzouk S, et al. Prevalence and metric of depression and anxiety in systemic lupus erythematosus: a systematic review and meta-analysis. Semin Arthritis Rheum 2020; 50: 84–94.
10.1016/j.semarthrit.2019.06.017
PubMedWeb of Science®Google Scholar
12Nantes SG, Su J, Dhaliwal A, Colosimo K, Touma Z. Performance of screening tests for cognitive impairment in systemic lupus erythematosus. J Rheumatol 2017; 44: 1583–9.
10.3899/jrheum.161125
PubMedWeb of Science®Google Scholar
13Petri M, Naqibuddin M, Carson KA, Wallace DJ, Weisman MH, Holliday SL, et al. Depression and cognitive impairment in newly diagnosed systemic lupus erythematosus. J Rheumatol 2010; 37: 2032–8.
10.3899/jrheum.091366
PubMedWeb of Science®Google Scholar
14Liu Z, Han L, Gahbauer EA, Allore HG, Gill TM. Joint trajectories of cognition and frailty and associated burden of patient-reported outcomes. J Am Med Dir Assoc 2018; 19: 304–309.
10.1016/j.jamda.2017.10.010
PubMedWeb of Science®Google Scholar
15Julian LJ, Yelin E, Yazdany J, Panopalis P, Trupin L, Criswell LA, et al. Depression, medication adherence, and service utilization in systemic lupus erythematosus. Arthritis Rheum 2009; 61: 240–6.
10.1002/art.24236
PubMedWeb of Science®Google Scholar
16Hochberg MC, for the Diagnostic and Therapeutic Criteria Committee of the American College of Rheumatology. Updating the American College of Rheumatology revised criteria for the classification of systemic lupus erythematosus [letter]. Arthritis Rheum 1997; 40: 1725.
10.1002/art.1780400928
CASPubMedGoogle Scholar
17Karlson EW, Daltroy LH, Rivest C, Ramsey-Goldman R, Wright EA, Partridge AJ, et al. Validation of a systemic lupus activity questionnaire (SLAQ) for population studies. Lupus 2003; 12: 280–6.
10.1191/0961203303lu332oa
CASPubMedWeb of Science®Google Scholar
18McHorney CA, Ware JE Jr, Lu JF, Sherbourne CD. The MOS 36-item Short-Form Health Survey (SF-36). III: tests of data quality, scaling assumptions, and reliability across diverse patient groups. Med Care 1994; 32: 40–66.
10.1097/00005650-199401000-00004
CASPubMedWeb of Science®Google Scholar
19Gaines JJ, Shapiro A, Alt M, Benedict RH. Semantic clustering indexes for the Hopkins Verbal Learning Test-Revised: initial exploration in elder control and dementia groups. Appl Neuropsychol 2006; 13: 213–22.
10.1207/s15324826an1304_2
PubMedWeb of Science®Google Scholar
20Radloff LS. The CES-D scale: a self-report depression scale for research in the general population. Appl Psychol Meas 1977; 1: 385–401.
10.1177/014662167700100306
PubMedWeb of Science®Google Scholar
21Nagin DS, Odgers CL. Group-based trajectory modeling in clinical research. Annu Rev Clin Psychol 2010; 6: 109–38.
10.1146/annurev.clinpsy.121208.131413
PubMedWeb of Science®Google Scholar
22Jones BL, Nagin DS. Advances in group-based trajectory modeling and an SAS procedure for estimating them. Sociol Methods Res 2007; 35: 542–71.
10.1177/0049124106292364
Web of Science®Google Scholar
23Hanly JG, Fisk JD, Sherwood G, Eastwood B. Clinical course of cognitive dysfunction in systemic lupus erythematosus. J Rheumatol 1994; 21: 1825–31.

CASPubMedWeb of Science®Google Scholar
24Waterloo K, Omdal R, Husby G, Mellgren SI. Neuropsychological function in systemic lupus erythematosus: a five-year longitudinal study. Rheumatology (Oxford) 2002; 41: 411–5.
10.1093/rheumatology/41.4.411
CASPubMedWeb of Science®Google Scholar
25Ceccarelli F, Perricone C, Pirone C, Massaro L, Alessandri C, Mina C, et al. Cognitive dysfunction improves in systemic lupus erythematosus: results of a 10 years prospective study. PLoS One 2018; 13:e0196103.
10.1371/journal.pone.0196103
PubMedWeb of Science®Google Scholar
26Kwan A, Katz P, Touma Z. The assessment of anxiety and depression and its associated factors in SLE. Curr Rheumatol Rev 2019; 15: 90–8.
10.2174/1573397114666180926101513
PubMedWeb of Science®Google Scholar
27Huang X, Magder LS, Petri M. Predictors of incident depression in systemic lupus erythematosus. J Rheumatol 2014; 41: 1823–33.
10.3899/jrheum.140111
PubMedWeb of Science®Google Scholar
28Knight AM, Trupin L, Katz P, Yelin E, Lawson EF. Depression risk in young adults with juvenile- and adult-onset lupus: twelve years of followup. Arthritis Care Res (Hoboken) 2018; 70: 475–80.
10.1002/acr.23290
PubMedWeb of Science®Google Scholar
29Meara A, Davidson N, Steigelman H, Zhao S, Brock G, Jarjour WN, et al. Screening for cognitive impairment in SLE using the Self-Administered Gerocognitive Exam. Lupus 2018; 27: 1363–7.
10.1177/0961203318759429
CASPubMedWeb of Science®Google Scholar
30Doninger NA, Fink JW, Utset TO. Neuropsychologic functioning and health status in systemic lupus erythematosus: does ethnicity matter? J Clin Rheumatol 2005; 11: 250–6.
10.1097/01.rhu.0000182149.67967.cc
PubMedWeb of Science®Google Scholar
31Borowoy AM, Pope JE, Silverman E, Fortin PR, Pineau C, Smith CD, et al. Neuropsychiatric lupus: the prevalence and autoantibody associations depend on the definition: results from the 1000 faces of lupus cohort. Semin Arthritis Rheum 2012; 42: 179–85.
10.1016/j.semarthrit.2012.03.011
PubMedWeb of Science®Google Scholar
32Stern Y. Cognitive reserve: implications for assessment and intervention. Folia Phoniatr Logop 2013; 65: 49–54.
10.1159/000353443
PubMedWeb of Science®Google Scholar
33O’Shea DM, Langer K, Woods AJ, Porges EC, Williamson JB, O’Shea A, et al. Educational attainment moderates the association between hippocampal volumes and memory performances in healthy older adults. Front Aging Neurosci 2018; 10: 361.
10.3389/fnagi.2018.00361
PubMedWeb of Science®Google Scholar
34Knight MJ, Baune BT. Cognitive dysfunction in major depressive disorder. Curr Opin Psychiatry 2018; 31: 26–31.
10.1097/YCO.0000000000000378
PubMedWeb of Science®Google Scholar
35Nishiguchi Y, Takano K, Tanno Y. The need for cognition mediates and moderates the association between depressive symptoms and impaired effortful control. Psychiatry Res 2016; 241: 8–13.
10.1016/j.psychres.2016.04.092
PubMedWeb of Science®Google Scholar

Citing Literature

Volume73, Issue10

October 2021

Pages 1436-1443

Filename	Description
acr24349-sup-0001-TableS1.docxWord document, 27.3 KB	Table S1
acr24349-sup-0002-TableS2.docxWord document, 31.3 KB	Table S2

Cognitive Function Trajectories in Association With the Depressive Symptoms Trajectories in Systemic Lupus Erythematosus Over Time

Abstract

Objective

Methods

Results

Conclusion

Supporting Information

References

Citing Literature

References

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Cognitive Function Trajectories in Association With the Depressive Symptoms Trajectories in Systemic Lupus Erythematosus Over Time

Abstract

Objective

Methods

Results

Conclusion

Supporting Information

References

Citing Literature

References

Related

Information