Hostname: page-component-848d4c4894-m9kch Total loading time: 0 Render date: 2024-05-06T23:01:30.029Z Has data issue: false hasContentIssue false
  • English
  • Français

Cognitive Impairment in Patients With Neuropsychiatric and Non-neuropsychiatric Systemic Lupus Erythematosus: A Systematic Review and Meta-analysis

Published online by Cambridge University Press:  19 March 2018

Arantzazu Zabala ,
Monika Salgueiro ,
Oihane Sáez-Atxukarro ,
Javier Ballesteros ,
Guillermo Ruiz-Irastorza  and
Rafael Segarra
Arantzazu Zabala*
Affiliation:
Department of Neurosciences, School of Medicine and Nursing, University of the Basque Country (UPV/EHU), Leioa, Spain Department of Psychiatry, Cruces University Hospital, Osakidetza-Basque Health System, BioCruces Health Research Institute, Barakaldo, Spain Centro de Investigación Biomédica en Red de Salud Mental (CIBERSAM), Instituto de Salud Carlos III, Spain
Monika Salgueiro
Affiliation:
Department of Psychiatry, Cruces University Hospital, Osakidetza-Basque Health System, BioCruces Health Research Institute, Barakaldo, Spain
Oihane Sáez-Atxukarro
Affiliation:
Department of Neurosciences, School of Medicine and Nursing, University of the Basque Country (UPV/EHU), Leioa, Spain
Javier Ballesteros
Affiliation:
Department of Neurosciences, School of Medicine and Nursing, University of the Basque Country (UPV/EHU), Leioa, Spain Centro de Investigación Biomédica en Red de Salud Mental (CIBERSAM), Instituto de Salud Carlos III, Spain
Guillermo Ruiz-Irastorza
Affiliation:
Autoimmune Diseases Research Unit. Department of Internal Medicine, Cruces University Hospital, Osakidetza-Basque Health System, BioCruces Health Research Institute, Barakaldo, Spain
Rafael Segarra
Affiliation:
Department of Neurosciences, School of Medicine and Nursing, University of the Basque Country (UPV/EHU), Leioa, Spain Department of Psychiatry, Cruces University Hospital, Osakidetza-Basque Health System, BioCruces Health Research Institute, Barakaldo, Spain Centro de Investigación Biomédica en Red de Salud Mental (CIBERSAM), Instituto de Salud Carlos III, Spain
*
Correspondence and reprint requests to: Arantzazu Zabala, Department of Neuroscience-Psychiatry. Faculty of Medicine and Nursing, University of the Basque Country, Barrio Sarriena s/n, 48940 Leioa, Bizkaia, Spain. E-mail: arantzazu.zabala@ehu.eus
Get access Rights & Permissions [Opens in a new window]

Abstract

Objectives: Systemic lupus erythematosus (SLE) is a chronic autoimmune disease. Its most prevalent manifestation is neuropsychiatric SLE (NP-SLE), which is characterized by increased involvement of the nervous system, with relevant symptoms, such as marked cognitive deficits, which are directly involved in subsequent functional disability. The objective of this study is to identify and compare the profile of cognitive deficits in patients with NP-SLE and patients with non-neuropsychiatric SLE (nonNP-SLE) by means of a systematic review and meta-analysis. Methods: We performed a systematic literature search based on the key words “cogn* OR neurocogn* AND lupus AND neuropsychiatry*” and included articles published between April 1999 and December 2016. A total of 244 articles were retrieved. We excluded reviews and meta-analyses, experiments not performed in humans, and single case reports. We included studies that used standardized cognitive measures and had included at least the subgroups NP-SLE and non NP-SLE. Results: The meta-analysis was finally based on six studies, and 10 neuropsychological variables were examined. Significant differences were observed between the groups for six variables. In the remaining four variables, we observed marked heterogeneity between the groups or a low number of studies. Conclusions: The data obtained indicate greater cognitive impairment among NP-SLE patients than among nonNP-SLE patients, at least for the cognitive domains of visuomotor coordination, attention, executive function, visual learning and memory, and phonetic fluency. The identification and definition of cognitive deficits in SLE patients is necessary to develop adequate cognitive remediation programs to improve functional outcomes. (JINS, 2018, 24, 629–639)

Keywords

Systemic lupus erythematosusNeuropsychiatric systemic lupus erythematosusCognitive impairmentNeuropsychologyReviewMeta-analysis
Type
Critical Review
Information
Journal of the International Neuropsychological Society , Volume 24 , Issue 6 , July 2018 , pp. 629 - 639
Copyright
Copyright © The International Neuropsychological Society 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Ainiala, H., Hietaharju, A., Loukkola, J., Peltola, J., Korpela, M., Metsänoja, R., & Auvinen, A. (2001). Validity of the new American College of Rheumatology criteria for neuropsychiatric lupus syndromes: A population-based evaluation. Arthritis and Rheumatism, 45, 419–423.Google Scholar
ACR - American College of Rheumatology. (1999). The American College of Rheumatology nomenclature and case definitions for neuropsychiatric lupus syndromes. Arthritis and Rheumatism, 42(4), 599–608.Google Scholar
Arnett, P. A., Smith, M. M., Barwick, F. H., Benedict, R. H., & Ahlstrom, B. P. (2008). Oralmotor slowing in multiple sclerosis: Relationship to neuropsychological tasks requiring an oral response. Journal of the International Neuropsychological Society, 14(3), 454–462.Google Scholar
Benedict, R. H. B., Shucard, J. L., Zivadinov, R., & Shucard, D. W. (2008). Neuropsychological impairment in systemic lupus erythematosus: A comparison with multiple sclerosis. Neuropsychology Reviews, 18(2), 149–166.Google Scholar
Borkowski, J. G., Benton, A. L., & Spreen, O. (1967). Word fluency and brain damage. Neuropsychologia, 5(2), 135–140.Google Scholar
Brey, R. (2007). Neuropsychiatric lupus. Clinical and imaging aspects. Bulletin of the NYU Hospital for Joint Diseases, 65(3), 194–199.Google Scholar
Butt, B. A., Farman, S., Khan, S. E. A., Saeed, M. A., & Ahmad, N. M. (2017). Cognitive dysfunction in patients with Systemic Lupus Erythematosus. Pakistan Journal of Medical Sciences, 33(1), 59–64.Google Scholar
Carbotte, R. M., Denburg, S. D., & Denburg, J. A. (1986). Prevalence of cognitive impairment in systemic lupus erythematosus. The Journal of Nervous and Mental Disease, 174, 357–364.Google Scholar
Carbotte, R. M., Denburg, S. D., & Denburg, J. A. (1995). Cognitive dysfunction in systemic lupus erythematosus is independent of active disease. The Journal of Rheumatology, 22, 863–867.Google Scholar
Carlomagno, S., Migliaresi, S., Ambrosone, L., Sannino, M., SangesG., Di G., Di, & Iorio, G. (2000). Cognitive impairment in systemic lupus erythematosus: A follow-up study. Journal of Neurology, 247, 273–279.Google Scholar
Corwin, J., & Bylsma, F.W. (1993). Translations of experts from Andre Rey’s psychological examination of traumatic encephalopathy an P.A. Ostherrieth’s “The Complex Figure Copy Test”. Clinical Neuropsychologist, 7, 3–15.Google Scholar
Delis, D. C., Kramer, J. H., Kaplan, E., & Oper, B. A. (1987). The California Verbal Learning Test manual. San Antonio: The Psychological Corporation.Google Scholar
Denburg, J. A., Carbotte, R. M., & Denburg, S. D. (1987a). Neuronal antibodies and cognitive function in systemic lupus erythematosus. Neurology, 37(3), 464–467.CrossRefGoogle ScholarPubMed
Denburg, S. D., Carbotte, R. M., & Denburg, J. A. (1987b). Cognitive impairment in SLE: A neuropsychological study of individual and group deficits. Journal of Clinical and Experimental Neuropsychology, 19, 323–339.Google Scholar
Emori, A., Matsushima, E., Aihara, O., Ohta, K., Koike, R., Miyasaka, N., & Kato, M. (2005). Cognitive dysfunction in systemic lupus erythematosus. Psychiatry and Clinical Neurosciences, 59(5), 584–589.Google Scholar
Golden, C. J. (1978). Stroop Color and Word test. Chicago: Stoelting.Google Scholar
Gulinello, M., & Putterman, C. (2011). The MRL/lpr mouse strain as a model for neuropsychiatric systemic lupus erythematosus. Journal of Biomedicine & Biotechnology, 2011, 207504.Google Scholar
Hanly, J. G., Fisk, J. D., Sherwood, G., & Eastwood, B. (1994). Clinical course of cognitive dysfunction in systemic lupus erythematosus. Journal of Rheumatology, 10, 1825–1831.Google Scholar
Hay, E. M., Black, D., Huddy, A., Creed, F., Tomenson, B., Bernstein, R. M., & Holt, P. J. (1992). Psychiatric disorder and cognitive impairment in systemic lupus erythematosus. Arthritis and Rheumatism, 35, 411–416.Google Scholar
Hay, E. M., Huddy, A., Black, D., Mbaya, P., Tomenson, B., Bernstein, R. M., & Creed, F. (1994). A prospective study of psychiatric disorder and cognitive function in systemic lupus erythematosus. Annals of the Rheumatic Diseases, 53, 298–303.Google Scholar
Huerta, P. T., Gibson, E. L., Rey, C., Huerta, T. S., & Huerta, P. T. (2015). Integrative neuroscience approach to neuropsychiatric lupus. Immunology Research, 63(1-3), 11–17.Google Scholar
Jeltsch-David, H., & Muller, S. (2014). Neuropsychiatric systemic lupus erythematosus: Pathogenesis and biomarkers. Nature Reviews Neurology, 10, 579–596.CrossRefGoogle ScholarPubMed
Kozora, E., Thompson, L. L., West, S. G., & Kotzin, B. L. (1996). Analysis of cognitive and psychological deficits in systemic lupus erythematosus patients without overt central nervous system disease. Arthritis and Rheumatism, 39, 2035–2045.Google Scholar
Kozora, E., Ellison, M. C., & West, S. (2004). Reliability and validity of the proposed American College of Rheumatology neuropsychological battery for systemic lupus erythematosus. Arthritis and Rheumatism, 51(5), 810–818.Google Scholar
Kozora, E., Arciniegas, D. B., Filley, C. M., West, S. G., BrownM., Miller M., Miller, . . . Zhang, L. (2008). Cognitive and neurologic status in patients with systemic lupus erythematosus without neuropsychiatric syndromes. Arthritis and Rheumatism, 59(11), 1639–1646.Google Scholar
Loukkola, J., Laine, M., Ainiala, H., Peltola, J., Metsänoja, R., Auvinen, A., & Hietaharju, A. (2003). Cognitive impairment in systemic lupus erythematosus and neuropsychiatric systemic lupus erythematosus: A population-based neuropsychological study. Journal of Clinical and Experimental Neuropsychology, 25(1), 145–151.Google Scholar
Magro-Checa, C., Zirkzee, E. J., Huizinga, T. W., & Steup-Beekman, G. M. (2016). Management of neuropsychiatric systemic lupus erythematosus: Current approaches and future perspectives. Drugs, 76(4), 459–483.Google Scholar
Meszaros, Z. S., Perl, A., & Faraone, S. V. (2012). Psychiatric symptoms in systemic lupus erythematosus: A systematic review. The Journal of Clinical Psychiatry, 73(7), 993–1001.Google Scholar
Mikdashi, J. A., Esdaile, J. M., Alarcón, G. S., Crofford, L., Fessler, B. J., Shanberg, L., & Schneider, M. (2007). Proposed response criteria for neurocognitive impairment in systemic lupus erythematosus clinical trials. Lupus, 16(6), 418–425.Google Scholar
Monastero, R., Bettini, P., Del Zotto, E., Cottini, E., Tincani, A., Balestrieri, G., & Padovani, A. (2001). Prevalence and pattern of cognitive impairment in systemic lupus erythematosus patients with and without overt neuropsychiatric manifestations. Journal of the Neurological Sciences, 184(1), 33–39.Google Scholar
Monov, S., & Monova, D. (2008). Classification criteria for neuropsychiatric systemic lupus erythematosus: Do they need a discussion? Hippokratia, 12, 103–107.Google Scholar
Nowicka-Sauer, K., Czuszyńska, Z., Majkowicz, M., Smoleńska, Ż., Jarmoszewicz, K., Olesińska, M., & Siebert, J. (2012). Neuropsychological assessment in mixed connective tissue disease: Comparison with systemic lupus erythematosus. Lupus, 21(9), 927–933.Google Scholar
Nowicka-Sauer, K., Czuszynska, Z., Smolenska, Z., & Siebert, J. (2011). Neuropsychological assessment in systemic lupus erythematosus patients: Clinical usefulness of first-choice diagnostic tests in detecting cognitive impairment and preliminary diagnosis of neuropsychiatric lupus. Clinical and Experimental Rheumatology, 29(2), 299–306.Google Scholar
Reitan, R. M., & Wolfson, D. (1988). The Halstead-Reitan Neuropsychology Test Battery. Tucson: Neuropsychological Press.Google Scholar
Sabbadini, M. G., Manfredi, A. A., Bozzolo, E., Ferrario, L., Rugarli, C., Scorza, R., & Passaleva, A. (1999). Central nervous systemic involvement in systemic lupus erythematosus patients without overt neuropsychiatric manifestations. Lupus, 8, 11–19.Google Scholar
Stojanovich, L., Zandman-Goddard, G., Pavlovich, S., & Sikanich, N. (2007). Psychiatric manifestations in systemic lupus erythematosus. Autoimmunity Reviews, 6(6), 421–426.Google Scholar
Unlu, O., Zuily, S., & Erkan, D. (2016). The clinical significance of antiphospholipid antibodies in systemic lupus erythematosus. European Journal of Rheumatology, 3(2), 75–84.Google Scholar
Wechsler, D. (1981). Wechsler Adult Intelligence Scale-Revised manual. San Antonio: The Psychological Corporation.Google Scholar
Yelnik, C. M., Kozora, E., & Appenzeller, S. (2016). Cognitive disorders and antiphospholipid antibodies. Autoimmunity Reviews, 15(12), 1193–1198.Google Scholar