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Comparison of Neuropsychological Impairment and Vocational Outcomes in Systemic Lupus Erythematosus and Multiple Sclerosis Patients

Published online by Cambridge University Press:  13 March 2012

Thomas J. Covey ,
Janet L. Shucard ,
David W. Shucard ,
Shane Stegen  and
Ralph H.B. Benedict
Thomas J. Covey
Affiliation:
Division of Cognitive and Behavioral Neurosciences, Department of Neurology, University at Buffalo, State University of New York School of Medicine and Biomedical Sciences, Buffalo, New York Neuroscience Program, University at Buffalo, State University of New York School of Medicine and Biomedical Sciences, Buffalo, New York
Janet L. Shucard
Affiliation:
Division of Cognitive and Behavioral Neurosciences, Department of Neurology, University at Buffalo, State University of New York School of Medicine and Biomedical Sciences, Buffalo, New York
David W. Shucard
Affiliation:
Division of Cognitive and Behavioral Neurosciences, Department of Neurology, University at Buffalo, State University of New York School of Medicine and Biomedical Sciences, Buffalo, New York Neuroscience Program, University at Buffalo, State University of New York School of Medicine and Biomedical Sciences, Buffalo, New York
Shane Stegen
Affiliation:
Division of Cognitive and Behavioral Neurosciences, Department of Neurology, University at Buffalo, State University of New York School of Medicine and Biomedical Sciences, Buffalo, New York
Ralph H.B. Benedict*
Affiliation:
Division of Cognitive and Behavioral Neurosciences, Department of Neurology, University at Buffalo, State University of New York School of Medicine and Biomedical Sciences, Buffalo, New York
*
Correspondence and reprint requests to: Ralph H.B. Benedict, Buffalo General Hospital, Department of Neurology, 100 High Street (E-2), Buffalo, New York 14203. E-mail: [email protected]
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Abstract

Systemic lupus erythematosus (SLE) and multiple sclerosis (MS) are chronic immunologic diseases that can cause cognitive dysfunction. MS is a central nervous system (CNS) disease characterized by demyelination and progressive brain atrophy. SLE is an autoimmune disease capable of damaging multiple organ systems, including the CNS. Cognitive disturbances are seen in both SLE and MS. The present study is concerned with understanding the similarities and differences between the cognitive profiles of SLE and MS as well as the relationship between cognitive impairment and vocational disability in these patients. We examined 47 SLE patients, 47 MS patients, and 44 healthy controls. The groups were well matched on demographics and the patient groups were also matched on disease duration and severity. Group comparisons revealed that generative verbal fluency and visual-spatial memory are more profoundly affected in MS than SLE; whereas depression, fatigue, and working memory deficits are similarly involved in both diseases. Logistic regression analysis revealed that executive function, in particular, was predictive of vocational outcomes in SLE and MS patients. (JINS, 2012, 18, 530–540)

Keywords

SLEMSNeuropsychologyCognitionAutoimmune diseaseWork disability
Type
Research Articles
Information
Journal of the International Neuropsychological Society , Volume 18 , Issue 3 , May 2012 , pp. 530 - 540
Copyright
Copyright © The International Neuropsychological Society 2012

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References

Abreu, M.R., Jakosky, A., Folgerini, M., Brenol, J.C., Xavier, R.M., Kapczinsky, F. (2005). Neuropsychiatric systemic lupus erythematosus: Correlation of brain MR imaging, CT, and SPECT. Clinical Imaging, 29(3), 215–221.CrossRefGoogle ScholarPubMed
Ainala, H., Loukkola, J., Peltola, J., Korpela, M., Hietaharju, A. (2001). The prevalence of neuropsychiatric syndromes in systemic lupus erythematosus. Neurology, 57, 496–500.CrossRefGoogle Scholar
Amato, M.P., Bartolozzi, M.L., Zipoli, V., Portaccio, E., Mortilla, M., Guidi, L., De Stefano, N. (2004). Neocortical volume decrease in relapsing-remitting MS patients with mild cognitive impairment. Neurology, 63(1), 89–93.CrossRefGoogle ScholarPubMed
Amato, M.P., Ponziani, G., Pracucci, G., Bracco, L., Siracusa, G., Amaducci, L. (1995). Cognitive impairment in early-onset multiple sclerosis: Pattern, predictors, and impact on everyday life in a 4-year follow-up. Archives of Neurology, 52(2), 168–172.CrossRefGoogle Scholar
Amato, M.P., Ponziani, G., Siracusa, G., Sorbi, S. (2001). Cognitive dysfunction in early-onset multiple sclerosis: A reappraisal after 10 years. Archives of Neurology, 58(10), 1602–1606.CrossRefGoogle ScholarPubMed
Appenzeller, S., Bonilha, L., Rio, P.A., Min Li, L., Costallat, L.T., Cendes, F. (2007). Longitudinal analysis of gray and white matter loss in patients with systemic lupus erythematosus. Neuroimage, 34(2), 694–701.CrossRefGoogle ScholarPubMed
Appenzeller, S., Cendes, F., Costallat, L.T. (2009). Cognitive impairment and employment status in systemic lupus erythematosus: A prospective longitudinal study. Arthritis Care & Research, 61(5), 680–687.CrossRefGoogle ScholarPubMed
Appenzeller, S., Vasconcelos Faria, A., Min Li, L., Costallat, L.T., Cendes, F. (2008). Quantitative magnetic resonance imaging analyses and clinical significance of hyperintense white matter lesions in systemic lupus erythematosus patients. Annals of Neurology, 64(6), 635–643.CrossRefGoogle ScholarPubMed
Archibald, C.J., Fisk, J.D. (2000). Information processing efficiency in patients with multiple sclerosis. Journal of Clinical & Experimental Neuropsychology, 22, 686–701.CrossRefGoogle ScholarPubMed
Arnett, P.A., Rao, S.M., Grafman, J., Bernardin, L., Luchetta, T., Binder, J.R., Lobeck, L. (1997). Executive functions in multiple sclerosis: An analysis of temporal ordering, semantic encoding, and planning abilities. Neuropsychology, 11, 535–544.CrossRefGoogle ScholarPubMed
Baker, K., Pope, J. (2009). Employment and work disability in systemic lupus erythematosus: A systematic review. Rheumatology, 48, 281–284.CrossRefGoogle ScholarPubMed
Beatty, W.W. (2002). Fluency in multiple sclerosis: Which measure is best? Multiple Sclerosis, 8, 261–264.CrossRefGoogle ScholarPubMed
Beatty, W.W., Hames, K.A., Blanco, C.R., Paul, R.H., Wilbanks, S.L. (1995). Verbal abstraction deficit in multiple sclerosis. Neuropsychology, (9), 198–205.CrossRefGoogle ScholarPubMed
Beck, A.T., Steer, R.A., Brown, G.K. (2000). BDI-fast screen for medical patients: Manual. San Antonio, TX: Psychological Corporation.Google Scholar
Belmont, H.M., Abramson, S.B., Lie, J.T. (1996). Pathology and pathogenesis of vascular injury in systemic lupus erythematosus: Interactions of inflammatory cells and activated endothelium. Arthritis and Rhematism, 39, 9–22.CrossRefGoogle ScholarPubMed
Benedict, R.H.B. (1997). Brief visuospatial memory test-revised: Professional manual. Odessa, FL: Psychological Assessment Resources, Inc.Google Scholar
Benedict, R.H.B., Bruce, J., Dwyer, M.G., Weinstock-Guttman, B., Tjoa, C., Tavazzi, E., Zivadinov, R. (2007). Diffusion-weighted imaging predicts cognitive impairment in multiple sclerosis. Multiple Sclerosis, 13(6), 722–730.CrossRefGoogle ScholarPubMed
Benedict, R.H.B., Fishman, I., McClellan, M.M., Bakshi, R., Weinstock-Guttman, B. (2003). Validity of the Beck Depression Inventory—Fast Screen in multiple sclerosis. Multiple Sclerosis, 9, 393–396.CrossRefGoogle ScholarPubMed
Benedict, R.H.B., Holtzer, R., Motl, R.W., Foley, F.W., Kaur, S., Hojnacki, D., Weinstock-Guttman, B. (2011). Upper and lower extremity motor function and cognitive impairment in Multiple Sclerosis. Journal of the International Neuropsychological Society, 17, 643–653.CrossRefGoogle ScholarPubMed
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 Review, 18(2), 149–166.CrossRefGoogle ScholarPubMed
Benedict, R.H.B., Wahlig, E., Bakshi, R., Fishman, I., Munschauer, F., Zivadinov, R., Weinstock-Guttman, B. (2005). Predicting quality of life in multiple sclerosis: Accounting for physical disability, fatigue, cognition, mood disorder, personality, and behavior change. Journal of the Neurological Sciences, 231, 29–34.CrossRefGoogle ScholarPubMed
Benton, A.L., Sivan, A.B., Hamsher, K., Varney, N.R., Spreen, O. (1994). Contributions to neuropsychological assessment (2nd ed.). New York: Oxford University Press.Google Scholar
Bosma, G.P., Rood, M.J., Zwinderman, A.H., Huizinga, T.W., van Buchem, M.A. (2000). Evidence of central nervous system damage in patients with neuropsychiatric systemic lupus erythematosus, demonstrated by magnetization transfer imaging. Arthritis and Rhematism, 43, 48–54.3.0.CO;2-H>CrossRefGoogle ScholarPubMed
Cercignani, M., Iannucchi, G., Rocca, M.A., Comi, G., Horsfield, M.A., Filippi, M. (2000). Pathologic damage in MS assessed by diffusion-weighted and magnetization transfer MRI. Neurology, 54, 1139–1144.CrossRefGoogle ScholarPubMed
Chipchase, S.Y., Lincoln, N.B., Radford, K.A. (2003). Measuring fatigue in people with multiple sclerosis. Disability and Rehabilitation, 25, 778–784.CrossRefGoogle ScholarPubMed
Comi, G., Filippi, M., Martinelli, V., Sirabian, G., Visciani, A., Campi, A., Canal, N. (1993). Brain magnetic resonance imaging correlates of cognitive impairment in multiple sclerosis. Journal of the Neurological Sciences, 115(Suppl 73), S66–S73.CrossRefGoogle ScholarPubMed
Covey, T.J., Zivadinov, R., Shucard, J.L., Shucard, D.W. (2011). Information processing speed, neural efficiency, and working memory performance in multiple sclerosis: Differential relationships with structural MRI. Journal of Clinical and Experimental Neuropsychology, 33, 1129–1145.CrossRefGoogle Scholar
D'Esposito, M., Onishi, K., Thompson, H., Robinson, K., Armstrong, C., Grossman, M. (1996). Working memory impairments in multiple sclerosis: Evidence from a dual-task paradigm. Neuropsychology, 10, 51–56.CrossRefGoogle Scholar
Delis, D.C., Kaplan, E., Kramer, J.H. (2001). Delis-Kaplan executive function system. San Antonio, TX: Psychological Corporation.Google Scholar
Delis, D.C., Kramer, J.H., Kaplan, E., Ober, B.A. (2000). California verbal learning test manual (2nd ed.). San Antonio, TX: Psychological Corporation.Google Scholar
DeLuca, J., Chelune, G., Tulsky, D.S., Lengenfelder, J., Chiaravalloti, N. (2004). Is speed of processing or working memory the primary information processing deficit in multiple sclerosis? Journal of Clinical & Experimental Neuropsychology, 26, 550–562.CrossRefGoogle ScholarPubMed
Denburg, S.D., Carbotte, R.M., Denburg, J.A. (1987). Cognitive impairment in systemic lupus erythematosus: A neuropsychological study of individual and group deficits. Journal of Clinical and Experimental Neuropsychology, 9(4), 323–339.CrossRefGoogle ScholarPubMed
Denburg, S.D., Carbotte, R.M., Denburg, J.A. (1997). Psychological aspects of systemic lupus erythematosus: Cognitive, function, mood, and self-report. The Journal of Rheumatology, 24, 998–1003.Google ScholarPubMed
Denney, D.R., Sworowski, L.A., Lynch, S.G. (2005). Cognitive impairment in three subtypes of multiple sclerosis. Archives of Clinical Neuropsychology, 20(8), 967–981.CrossRefGoogle ScholarPubMed
Drew, M.A., Starkey, N.J., Isler, R.B. (2009). Examining the link between information processing speed and executive functioning in multiple sclerosis. Archives of Clinical Neuropsychology, 24, 47–58.CrossRefGoogle ScholarPubMed
Ellis, S.G., Verity, M.A. (1979). Central nervous system involvement in systemic lupus erythematosus: A review of neuropathologic findings in 57 cases. Seminars in Arthritis and Rheumatism, 8, 212–221.CrossRefGoogle ScholarPubMed
Emmer, B.J., Veer, I.M., Steup-Beekman, G.M., Huizinga, T.W., van der Grond, J., van Buchem, M.A. (2010). Tract-based spatial statistics on diffusion tensor imaging in systemic lupus erythematosus reveals localized involvement of white matter tracts. Arthritis & Rheumatism, 62, 3716–3721.CrossRefGoogle ScholarPubMed
Filley, C.M., Heaton, R.K., Nelson, L.M., Burks, J.S., Franklin, G.M. (1989). A comparison of dementia in Alzheimer's disease and multiple sclerosis. Archives of Neurology, 46, 157–161.CrossRefGoogle ScholarPubMed
Fitzgibbon, B.M., Fairhall, S.L., Kirk, I.J., Kalev-Zylinska, M., Pui, K., Dalbeth, N., McQueen, F.M. (2008). Functional MRI in NPSLE patients reveals increased parietal and frontal brain activation during a working memory task compared with controls. Rheumatology (Oxford), 47, 50–53.CrossRefGoogle ScholarPubMed
Foong, J., Rozewicz, L., Quaghebeur, G., Davie, C.A., Kartsounis, L.D., Thompson, A.J., Ron, M.A. (1997). Executive function in multiple sclerosis. The role of frontal lobe pathology. Brain, 120(Pt 1), 15–26.CrossRefGoogle ScholarPubMed
Forn, C., Belenguer, A., Parcet-Ibars, M.A., Avila, C. (2008). Information-processing speed is the primary deficit underlying the poor performance of multiple sclerosis patients in the Paced Auditory Serial Addition Test (PASAT). Journal of Clinical & Experimental Neuropsychology, 30(7), 789–796.CrossRefGoogle ScholarPubMed
Geurts, J., Barkhof, F. (2008). Gray matter pathology in multiple sclerosis. The Lancet Neurology, 7(9), 841–851.CrossRefGoogle Scholar
Glanz, B.I., Schur, P.H., Lew, R.A., Khoshbin, S. (2005). Lateralized cognitive dysfunction in patients with systemic lupus erythematosus. Lupus, 14(11), 896–902.CrossRefGoogle ScholarPubMed
Govoni, M., Castellino, G., Padovan, M., Borrelli, M., Trotta, F. (2004). Recent advances and future perspective in neuroimaging in neuropsychiatric systemic lupus erythematosus. Lupus, 13(3), 149–158.CrossRefGoogle ScholarPubMed
Gronwall, D.M. (1977). Paced auditory serial addition task: A measure of recovery from concussion. Perceptual and Motor Skills, 44, 367–373.CrossRefGoogle ScholarPubMed
Hachulla, E., Michon-Pasturel, U., Leys, D., Pruvo, J.P., Queyrel, V., Masy, E., Devulder, B. (1998). Cerebral magnetic resonance imaging in patients with or without antiphospholipid antibodies. Lupus, 7, 124–131.CrossRefGoogle ScholarPubMed
Hanly, J.G., Liang, M.H., Moore, P.M., Lahita, R.G. (1997). Cognitive disorders in systemic lupus erythematosus: Epidemiologic and clinical issues (pp. 60–68). New York: The New York Academy of Sciences.CrossRefGoogle Scholar
Heaton, R.K. (1985). Neuropsychological findings in relapsing-remitting and chronic-progressive multiple sclerosis. Journal of Consulting & Clinical Psychology, 53, 103–110.CrossRefGoogle ScholarPubMed
Houtchens, M.K., Benedict, R.H.B., Killiany, R., Sharma, J., Jaisani, Z., Singh, B., Bakshi, R. (2007). Thalamic atrophy and cognition in multiple sclerosis. Neurology, 69, 113–123.CrossRefGoogle ScholarPubMed
Johnson, R.T., Richardson, E.P. (1968). The neurological manifestations of systemic lupus erythematosus: A clinical-pathological study of 24 cases and review of the literature. Medicine, 47, 337–369.CrossRefGoogle Scholar
Kozora, E., Arciniegas, D.B., Filley, C.M., West, S.G., Brown, M., Miller, D., Zhang, L. (2008). Cognitive and neurologic status in patients with systemic lupus erythematosus without major neuropsychiatric syndromes. Arthritis Care & Research, 59(11), 1639–1646.CrossRefGoogle ScholarPubMed
Kozora, E., Filley, C.M. (2011). Cognitive dysfunction and white matter abnormalities in systemic lupus erythematosus. Journal of the International Neuropsychological Society, 17, 1–8.CrossRefGoogle ScholarPubMed
Kozora, E., Hanly, J.G., Lapteva, L., Filley, C.M. (2008). Cognitive dysfunction in systemic lupus erythematosus: Past, present, and future. Arthritis & Rheumatism, 58(11), 3286–3298.CrossRefGoogle ScholarPubMed
Krupp, L.B., LaRocca, N.G., Muir-Nash, J., Steinberg, A.D. (1989). The fatigue severity scale. Application to patients with multiple sclerosis and systemic lupus erythematosus. Archives of Neurology, 46, 1121–1123.CrossRefGoogle ScholarPubMed
Kurtzke, J.F. (1983). Rating neurologic impairment in multiple sclerosis: An expanded disability status scale (EDSS). Neurology, 33, 1444–1452.CrossRefGoogle ScholarPubMed
Kutzelnigg, A., Lucchinetti, C.F., Stadelmann, C., Bruck, W., Rauschka, H., Bergmann, M., Lassmann, H. (2005). Cortical demyelination and diffuse white matter injury in multiple sclerosis. Brain, 128, 2705–2712.CrossRefGoogle ScholarPubMed
Lengenfelder, J., Bryant, D., Diamond, B.J., Kalmar, J.H., Moore, N.B., DeLuca, J. (2006). Processing speed interacts with working memory efficiency in multiple sclerosis. Archives of Clinical Neuropsychology, 21(3), 229–238.CrossRefGoogle ScholarPubMed
Leritz, E., Brandt, J., Minor, M., Reis-Jensen, F., Petri, M. (2000). “Subcortical” cognitive impairment in patients with systemic lupus erythematosus. Journal of the International Neuropsychological Society, 6, 821–825.CrossRefGoogle ScholarPubMed
Liang, M.H., Socher, S.A., Larson, M.G., Schur, P.H. (1989). Reliability and validity of six systems for the clinical assessment of disease activity in systemic lupus erythematosus. Arthritis and Rheumatism, 32, 1107–1118.CrossRefGoogle ScholarPubMed
Lin, X., Tench, C.R., Morgan, P.S., Constantinescu, C.S. (2008). Use of combined conventional and quantitative MRI to quantify pathology related to cognitive impairment in multiple sclerosis. Journal of Neurology, Neurosurgery, and Psychiatry, 79, 437–441.CrossRefGoogle ScholarPubMed
Loukkola, J., Laine, M., Ainiala, H., Peltola, J., Metsanoja, 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 & Experimental Neuropsychology, 25(1), 145–151.CrossRefGoogle ScholarPubMed
Lublin, F.D., Reingold, S.C. (1996). Defining the clinical course of multiple sclerosis: Results of an international survey. Neurology, 46(4), 907–911.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Morrow, S.A., Drake, A., Zivadinov, R., Munschauer, F., Weinstock-Guttman, B., Benedict, R.H. (2010). Predicting loss of employment over three years in multiple sclerosis: Clinically meaningful cognitive decline. Clinical Neuropsycholgy, 7, 1–15.Google Scholar
Otte, A., Weiner, S.M., Peter, H.H., Mueller-Brand, J., Goetz, M., Moser, E., Nitzsche, E.U. (1997). Brain glucose utilization in systemic lupus erythematosus with neuropsychiatric symptoms: A controlled positron emission tomography study. European Journal of Nuclear Medicine, 24, 787–791.CrossRefGoogle ScholarPubMed
Panopalis, P., Julian, L., Yazdany, J., Gillis, J.Z., Trupin, L., Hersh, A., Yelin, E. (2007). Impact of memory impairment on employment status in persons with systemic lupus erythematosus. Arthritis and Rheumatism, 57(8), 1453–1460.CrossRefGoogle ScholarPubMed
Parmenter, B.A., Shucard, J.L., Benedict, R.H.B., Shucard, D.W. (2006). Working memory deficits in multiple sclerosis: Comparison between the n-back task and the Paced Auditory Serial Addition Test. Journal of the International Neuropsychological Society, 12, 677–687.CrossRefGoogle ScholarPubMed
Parmenter, B.A., Shucard, J.L., Shucard, D.W. (2007). Information processing deficits in multiple sclerosis: A matter of complexity. Journal of the International Neuropsychological Society, 13, 417–423.CrossRefGoogle ScholarPubMed
Piras, M.R., Magnano, I., Canu, E.D., Paulus, K.S., Satta, W.M., Soddu, A., Aiello, I. (2003). Longitudinal study of cognitive dysfunction in multiple sclerosis: Neuropsychological, neuroradiological, and neurophysiological findings. Journal of Neurology, Neurosurgery, & Psychiatry, 74(7), 878–885.CrossRefGoogle ScholarPubMed
Pirko, I., Lucchinetti, C.F., Sriram, S., Bakshi, R. (2007). Gray matter involvement in multiple sclerosis. Neurology, 68, 634–642.CrossRefGoogle ScholarPubMed
Polman, C.H., Reingold, S.C., Edan, G., Filippi, M., Hartung, H.P., Kappos, L., Wolinsky, J.S. (2005). Diagnostic criteria for multiple sclerosis: 2005 revisions to the “McDonald Criteria”. Annals of Neurology, 58(6), 840–846.CrossRefGoogle Scholar
Qualls, C.E., Bliwise, N.G., Stringer, A.Y. (2000). Short forms of The Benton Judgment of Line Orientation Test: Development and psychometric properties. Archives of Clinical Neuropsychology, 15(2), 159–163.Google ScholarPubMed
Rao, S.M. (1991). A manual for the brief, repeatable battery of neuropsychological tests in multiple sclerosis. New York, NY: National Multiple Sclerosis Society.Google Scholar
Rao, S.M., Leo, G.J., Bernardin, L., Unverzagt, F. (1991). Cognitive dysfunction in multiple sclerosis. I. Frequency, patterns, and prediction. Neurology, 41, 685–691.CrossRefGoogle ScholarPubMed
Rao, S.M., Leo, G.J., Ellington, L., Nauertz, T., Bernardin, L., Unveragt, F. (1991). Cognitive dysfunction in multiple sclerosis. II. Impact on employment and social functioning. Neurology, 41, 692–696.CrossRefGoogle ScholarPubMed
Roca, M., Torralva, T., Meli, F., Fiol, M., Calcagno, M.L., Carpintiero, S., Correale, J. (2008). Cognitive deficits in multiple sclerosis correlate with changes in fronto-subcortical tracts. Multiple Sclerosis, 14, 364–369.CrossRefGoogle ScholarPubMed
Rogers, J.M., Panegyres, P.K. (2007). Cognitive impairment in multiple sclerosis: Evidence-based analysis and recommendations. Journal of Clinical Neuroscience, 14, 919–927.CrossRefGoogle Scholar
Rovaris, M., Iannucci, G., Falautano, M., Possa, F., Martinelli, V., Comi, G., Filippi, M. (2002). Cognitive dysfunction in patients with mildly disabling relapsing-remitting multiple sclerosis: An exploratory study with diffusion tensor MR imaging. Journal of the Neurological Sciences, 195(2), 103–109.CrossRefGoogle ScholarPubMed
Rovaris, M., Viti, B., Ciboddo, G., Gerevini, S., Capra, R., Iannucci, G., Filippi, M. (2000). Brain involvement in systemic immune mediated diseases: Magnetic resonance and magnetisation transfer imaging study. Journal of Neurology, Neurosurgery, & Psychiatry, 68, 170–177.CrossRefGoogle ScholarPubMed
Sanfilipo, M.P., Benedict, R.H., Weinstock-Guttman, B., Bakshi, R. (2006). Gray and white matter brain atrophy and neuropsychological impairment in multiple sclerosis. Neurology, 66(5), 685–692.CrossRefGoogle ScholarPubMed
Shucard, J.L., Lee, W.H., Hamlin, A.S., Shucard, D.W. (2011). The relationship between processing speed and working memory demand in systemic lupus erythematosus: Evidence from a visual N-Back Task. Neuropsychology, 25, 45–52.CrossRefGoogle ScholarPubMed
Shucard, J.L., Parrish, J., Shucard, D.W., McCabe, D., Benedict, R.H.B., Ambrus, J. (2004). Working memory and processing speed deficits in systemic lupus erythematosus as measured by the paced auditory serial addition test. Journal of the International Neuropsychological Society, 10, 35–45.CrossRefGoogle ScholarPubMed
Sibbitt, W.L. Jr., Sibbitt, R.R., Brooks, W.M. (1999). Neuroimaging in neuropsychiatric systemic lupus erythematosus. Arthritis and Rheumatism, 42, 2026–2038.3.0.CO;2-J>CrossRefGoogle ScholarPubMed
Smith, A. (1982). Symbol digit modalities test: Manual. Los Angeles: Western Psychological Services.Google Scholar
Steens, S.C., Admiraal-Behloul, F., Bosma, G.P., Steup-Beekman, G.M., Olofsen, H., Le Cessie, S., Van Buchem, M.A. (2004). Selective gray matter damage in neuropsychiatric lupus. Arthritis and Rheumatism, 50(9), 2877–2881.CrossRefGoogle ScholarPubMed
Swirsky-Sacchetti, T., Field, H.L., Mitchell, D.R., Seward, J., Lublin, F., Knobler, R., Gonzalez, C.F. (1992). The sensitivity of the Mini-Mental State Exam in the white matter dementia of multiple sclerosis. Journal of Clinical Psychology, 48, 779–786.3.0.CO;2-B>CrossRefGoogle ScholarPubMed
Swirsky-Sacchetti, T., Mitchell, D.R., Seward, J., Gonzales, C., Lublin, F., Knobler, R., Field, H.L. (1992). Neuropsychological and structural brain lesions in multiple sclerosis. Neurology, 42, 1291–1295.CrossRefGoogle ScholarPubMed
Tan, E.M., Cohen, A.S., Fries, J.F., Massi, A.T., McShane, D.J., Rothfield, N.F. (1982). The 1982 revised criteria for the classification of systemic lupus erythematosus. Arthritis & Rheumatism, 25, 1271–1277.CrossRefGoogle ScholarPubMed
Tekok-Kilic, A., Benedict, R.H.B., Weinstock-Guttman, B., Dwyer, M., Carone, D., Srinivasaraghavan, B., Zivadinov, R. (2007). Independent contributions of cortical gray matter atrophy and ventricle enlargement for predicting neuropsychological impairment in multiple sclerosis. Neuroimage, 36, 1294–1300.CrossRefGoogle ScholarPubMed
Trapp, B.D., Peterson, J., Ransohoff, R.M., Rudick, R., Mork, S., Bo, L. (1998). Axonal transection in the lesions of multiple sclerosis. New England Journal of Medicine, 338, 278–285.CrossRefGoogle ScholarPubMed
Vasilesios, K.C., Krishnan, S., Tsokos, G.C. (2006). Systems biology in systemic lupus erythematosus: Integrating genes, biology and immune function. Autoimmunity, 39, 705–709.Google Scholar
Vleugels, L., Lafosse, C., van Nunen, A., Nachtergaele, S., Ketelaer, P., Charlier, M., Vandenbussche, E. (2000). Visuoperceptual impairment in multiple sclerosis patients diagnosed with neuropsychological tasks. Multiple Sclerosis, 6, 241–254.CrossRefGoogle ScholarPubMed
Zhang, L., Harrison, M., Heier, L.A., Zimmerman, R.D., Ravdin, L., Lockshin, M., Ulug, A.M. (2007). Diffusion changes in patients with systemic lupus erythematosus. Magnetic Resonance Imaging, 25, 399–405.CrossRefGoogle ScholarPubMed