Abstract
In this manuscript, we review literature describing the neuropsychological and brain imaging characteristics of systemic lupus erythematosus (SLE) patients. The findings are compared and contrasted with multiple sclerosis (MS) studies, revealing similarities and differences of interest to clinicians and researchers. While cognitive impairment is somewhat less common in SLE than MS, the diseases share a similar cognitive profile with deficits most prominent on tests emphasizing the speed of information processing, working memory, and visual/spatial learning, and memory. In early or more mildly affected patients, diffuse white matter damage, which may not be apparent on conventional brain imaging, plays a major role in clinical presentation and cognitive testing. The causes of white matter damage are very different, however, and in later stages of the disease MS and SLE appear to give rise to different forms of cerebral pathology. MS may be characterized by increasing brain atrophy affecting especially the cortical and deep gray matter, at least after conversion to secondary progressive course. There is less evidence for neurodegenerative changes in SLE, but patients are increasingly at risk for cerebrovascular disease. We conclude by offering some suggestions for future clinical and imaging research.
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Abbreviations
- ACR:
-
American College of Rheumatology
- APLA:
-
antiphospholipid antibodies
- APLS:
-
antiphospholipid antibody syndrome
- BVMTR:
-
Brief Visuospatial Memory Test-Revised
- COWAT:
-
Controlled Oral Word Association Test
- CND:
-
central nervous system
- CRP:
-
C-reactive protein
- CVLT2:
-
California Verbal Learning Test, second edition
- DKEFS:
-
Delis–Kaplan Executive Function System Sorting Test
- DTI:
-
diffusion tensor imaging
- DWI:
-
diffusion weighted imaging
- FLAIR:
-
fluid attenuated inversion recovery technique
- IL-6:
-
interleukin-6
- JLO:
-
Judgment of Line Orientation Test
- MACFIMS:
-
Minimal Assessment of Cognitive Function in MS
- MRI:
-
magnetic resonance imaging
- MRS:
-
magnetic resonance spectroscopy
- MS:
-
multiple sclerosis
- MTI:
-
magnetization transfer imaging
- MTR:
-
magnetization transfer ratio
- NAA:
-
N-acetyl aspartate
- NP:
-
neuropsychiatric
- PASAT:
-
Paced Auditory Serial Addition Test
- RA:
-
rheumatoid arthritis
- SDMT:
-
Symbol Digit Modalities Test
- SLE:
-
systemic lupus erythematosus
- TMT:
-
Trail Making Test
- WI:
-
weighted imaging
- WMS-III:
-
Wechsler Memory Scale, 3rd edition
References
Ainala, H., Loukkola, J., Peltola, J., Korpela, M., & Hietaharju, A. (2001). The prevalence of neuropsychiatric syndromes in systemic lupus erythematosus. Neurology, 57, 496–500.
Amato, M. P., Bartolozzi, M. L., Zipoli, V., Portaccio, E., Mortilla, M., Guidi, L., et al. (2004). Neocortical volume decrease in relapsing-remitting MS patients with mild cognitive impairment. Neurology, 63, 89–93.
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, 168–172.
American College of Rheumatology (1999). The American College of Rheumatology nomenclature and case definitions for neuropsychiatric lupus syndromes. Arthritis & Rheumatism, 42, 599–608.
Archibald, C. J., & Fisk, J. D. (2000). Information processing efficiency in patients with multiple sclerosis. Journal of Clinical & Experimental Neuropsychology, 22, 686–701.
Arnett, P. A., Rao, S. M., Bernardin, L., Grafman, J., Yetkin, F. Z., & Lobeck, L. (1994). Relationship between frontal lobe lesions and Wisconsin Card Sorting Test performance in patients with multiple sclerosis. Neurology, 44, 420–425.
Arnett, P. A., Rao, S. M., Bernardin, L., Luchetta, T., Frost, J., Meidenbauer, K., et al. (1997). Executive functions in multiple sclerosis: An analysis of temporal ordering, semantic encoding, and planning abilities. Neuropsychology, 11, 535–544.
Axford, J. S., Howe, F. A., Heron, C., & Griffiths, J. R. (2001). Sensitivity of quantitative (1)H magnetic resonance spectroscopy of the brain in detecting early neuronal damage in systemic lupus erythematosus. Annals of the Rheumatic Diseases, 60, 106–111.
Baum, K. A., Hopf, U., Nehrig, C., Stover, M., & Schorner, W. (1993). Systemic lupus erythematosus: Neuropsychiatric signs and symptoms related to cerebral MRI findings. Clinical Neurology & Neurosurgery, 95, 29–34.
Beatty, W. W. (2002). Fluency in multiple sclerosis: Which measure is best? Multiple Sclerosis, 8, 261–264.
Beatty, W. W., Goodkin, D. E., Monson, N., & Beatty, P. A. (1989). Cognitive disturbances in patients with relapsing remitting multiple sclerosis. Archives of Neurology, 46, 1113–1119.
Beatty, W. W., Goodkin, D. E., Monson, N., Beatty, P. A., & Hertsgaard, D. (1988). Anterograde and retrograde amnesia in patients with chronic progressive multiple sclerosis. Archives of Neurology, 45, 611–619.
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.
Beatty, W. W., & Monson, N. (1996). Problem solving by patients with multiple sclerosis: Comparison of performance on the Wisconsin and California Card Sorting Test. Journal of the International Neuropsychological Society, 2, 134–140.
Benedetti, B., Rovaris, M., Judica, E., Donadoni, G., Ciboddo, G., & Filippi, M. (2007). Assessing “occult” cervical cord damage in patients with neuropsychiatric systemic lupus erythematosus using diffusion tensor MRI. Journal of Neurology, Neurosurgery & Psychiatry, 78, 893–895.
Benedict, R. H. B. (1997). Brief visuospatial memory test—Revised: Professional manual. Odessa, Florida: Psychological Assessment Resources, Inc.
Benedict, R. H. B. (2005). Effects of using same- versus alternate-form memory tests during short-interval repeated assessments in multiple sclerosis. Journal of the International Neuropsychological Society, 11, 727–736.
Benedict, R. H. B., Bakshi, R., Simon, J. H., Priore, R., Miller, C., & Munschauer, F. (2002a). Frontal cortex atrophy predicts cognitive impairment in multiple sclerosis. Journal of Neuropsychiatry & Clinical Neurosciences, 14, 44–51.
Benedict, R., & Bobholz, J. (2007). Multiple sclerosis. Seminars in Neurology, 27, 78–86.
Benedict, R. H. B., Bruce, J. M., Dwyer, M. G., Abdelrahman, N., Hussein, S., Weinstock-Guttman, B., et al. (2006b). Neocortical atrophy, third ventricular width, and cognitive dysfunction in multiple sclerosis. Archives of Neurology, 63, 1301–1306.
Benedict, R. H. B., Carone, D., & Bakshi, R. (2004a). Correlating brain atrophy with cognitive dysfunction, mood disturbances, and personality disorder in multiple sclerosis. Journal of Neuroimaging, 14, 36S–45S.
Benedict, R. H. B., Cookfair, D., Gavett, R., Gunther, M., Munschauer, F., Garg, N., et al. (2006c). Validity of the Minimal Assessment of Cognitive Function in Multiple Sclerosis (MACFIMS). Journal of the International Neuropsychological Society, 12, 549–558.
Benedict, R. H. B., Cox, D., Thompson, L. L., Foley, F. W., Weinstock-Guttman, B., & Munschauer, F. (2004b). Reliable screening for neuropsychological impairment in MS. Multiple Sclerosis, 10, 675–678.
Benedict, R. H. B., Fischer, J. S., Archibald, C. J., Arnett, P. A., Beatty, W. W., Bobholz, J., et al. (2002b). Minimal neuropsychological assessment of MS Patients: A consensus approach. Clinical Neuropsychologist, 16, 381–397.
Benedict, R. H. B., Shapiro, A., Priore, R. L., Miller, C., Munschauer, F. E., & Jacobs, L. D. (2001). Neuropsychological counseling improves social behavior in cognitively-impaired multiple sclerosis patients. Multiple Sclerosis, 6, 391–396.
Benedict, R. H. B., Wahlig, E., Bakshi, R., Fishman, I., Munschauer, F., Zivadinov, R., et al. (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.
Benedict, R. H. B., Weinstock-Guttman, B., Fishman, I., Sharma, J., Tjoa, C. W., & Bakshi, R. (2004c). Prediction of neuropsychological impairment in multiple sclerosis: Comparison of conventional magnetic resonance imaging measures of atrophy and lesion burden. Archives of Neurology, 61, 226–230.
Benedict, R. H. B., et al.; NMSS and MS Task Force (2006a). Assessment and management of cognitive impairment in multiple sclerosis. A monograph published by the National Multiple Sclerosis Society, New York.
Benton, A. L., & Hamsher, K. (1989). Multilingual aphasia examination. Iowa City: AJA Associates.
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.
Bermel, R. A., Bakshi, R., Tjoa, C., Puli, S. R., & Jacobs, L. (2002). Bicaudate ratio as a magnetic resonance imaging marker of brain atrophy in multiple sclerosis. Archives of Neurology, 59, 275–280.
Bo, L., Geurts, J., van der Valk, P., Polman, C., & Barkhof, F. (2007). Lack of correlation between cortical demyelination and white matter pathologic changes in multiple sclerosis. Archives of Neurology, 64, 76–80.
Bosma, G. P., Huizinga, T. W., Mooijaart, S. P., & Van Buchem, M. A. (2003). Abnormal brain diffusivity in patients with neuropsychiatric systemic lupus erythematosus. AJNR: American Journal of Neuroradiology, 24, 850–854.
Bosma, G. P., Middelkoop, H. A., Rood, M. J., Bollen, E. L., Huizinga, T. W., & van Buchem, M. A. (2002). Association of global brain damage and clinical functioning in neuropsychiatric systemic lupus erythematosus. Arthritis & Rheumatism, 46, 2665–2672.
Bosma, G. P., Rood, M. J., Huizinga, T. W., de Jong, B. A., Bollen, E. L., & van Buchem, M. A. (2000a). Detection of cerebral involvement in patients with active neuropsychiatric systemic lupus erythematosus by the use of volumetric magnetization transfer imaging. Arthritis & Rheumatism, 43, 2428–2436.
Bosma, G. P., Rood, M. J., Zwinderman, A. H., Huizinga, T. W., & van Buchem, M. A. (2000b). Evidence of central nervous system damage in patients with neuropsychiatric systemic lupus erythematosus, demonstrated by magnetization transfer imaging. Arthritis & Rheumatism, 43, 48–54.
Brownell, B., & Hughes, T. J. (1962). The distribution of plaques in the cerebrum in multiple sclerosis. Journal of Neurology, Neurosurgery, and Psychiatry, 25, 315–320.
Camp, S. J., Stevenson, V. L., Thompson, A. J., Miller, D. H., Borras, C., Auriacombe, S., et al. (1999). Cognitive function in primary progressive and transitional progressive multiple sclerosis: a controlled study with MRI correlates. Brain, 122, 1341–1348.
Carbotte, R. M. P. D., Denburg, S. D. P. D., & Denburg, J. A. F. (1986). Prevalence of cognitive impairment in systemic lupus erythematosus. The Journal of Nervous and Mental Disease, 174, 357–364.
Carbotte, R. M., Denburg, S. D., & Denburg, J. A. (1995). Cognitive dysfunction in systemic lupus erythematosus is independent of active disease. Journal of Rheumatology, 22, 863–867.
Carone, D., Benedict, R. H. B., Dwyer, M., Cookfair, D. L., Srinivasaraghavan, B., Tjoa, C. W., et al. (2006). Semiautomatic brain region extraction (SABRE) reveals superior cortical and deep gray matter atrophy in MS. Neuroimage, 29, 505–514.
Cercignani, M., Iannucci, 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.
Chard, D. T., Griffin, C. M., Parker, G. J., Kapoor, R., Thompson, A. J., & Miller, D. H. (2002). Brain atrophy in clinically early relapsing-remitting multiple sclerosis. Brain, 125, 327–337.
Chinn, R. J., Wilkinson, I. D., Hall-Craggs, M. A., Paley, M. N., Shortall, E., Carter, S., et al. (1997). Magnetic resonance imaging of the brain and cerebral proton spectroscopy in patients with systemic lupus erythematosus. Arthritis & Rheumatism, 40, 36–46.
Christodoulou, C., Krupp, L. B., Liang, Z., Huang, W., Melville, P., Roque, C., et al. (2003). Cognitive performance and MR markers of cerebral injury in cognitively impaired MS patients. Neurology, 60, 1793–1798.
Cifelli, A., Arridge, M., Jezzard, P., Esiri, M. M., Palace, J., & Matthews, P. M. (2002). Thalamic neurodegeneration in multiple sclerosis. Annals of Neurology, 52, 650–653.
Cohen, J. (1988). Statistical power for the behavioral sciences. Hillsdale, NJ: Erlbaum.
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.
Danner, M., Kasl, S. V., Abramson, J. L., & Vaccarino, V. (2003). Association between depression and elevated C-reactive protein. Psychosomatic Medicine, 65, 347–356.
Delis, D. C., Kaplan, E., & Kramer, J. H. (2001). Delis–Kaplan executive function system. San Antonio, Texas: Psychological Corporation.
Delis, D. C., Kramer, J. H., Kaplan, E., & Ober, B. A. (2000). California verbal learning test manual: Second edition, adult version. San Antonio, TX: Psychological Corporation.
Deloire, M. S., Bonnet, M. C., Salort, E., Arimone, Y., Boudineau, M., Petry, K. G., et al. (2006). How to detect cognitive dysfunction at early stages of multiple sclerosis? Multiple Sclerosis, 12, 445–452.
DeLuca, J., Barbieri-Berger, S., & Johnson, S. K. (1994). The nature of memory impairments in multiple sclerosis: Acquisition versus retrieval. Journal of Clinical & Experimental Neuropsychology, 16, 183–189.
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.
DeLuca, J., Johnson, S. K., & Natelson, B. H. (1993). Information processing efficiency in chronic fatigue syndrome and multiple sclerosis. Archives of Neurology, 50, 301–304.
Demaree, H. A., DeLuca, J., Gaudino, E. A., & Diamond, B. J. (1999). Speed of information processing as a key deficit in multiple sclerosis: Implications for rehabilitation. Journal of Neurology, Neurosurgery & Psychiatry, 67, 661–663.
Denburg, J. A., Carbotta, R. M., & Denburg, S. D. (1987a). Neuronal antibodies and cognitive function in systemic lupus erythematosus. Neurology, 37, 464–467.
Denburg, S. D., Carbotta, R. M., & Denburg, J. A. (1987b). Cognitive impairment in systemic lupus erythematosus: A neuropsychological study of individual and group deficits. Journal of Clinical and Experimental Neuropsychology, 9, 323–339.
Denburg, S. D., Carbotte, R. M., & Denburg, J. A. (1994). Corticosteroids and neuropsychological functioning in patients with systemic lupus erythematosus. Arthritis & Rheumatism, 37, 1311–1320.
Denburg, S. D., Carbotte, R. M., & Denburg, J. A. (1997a). Psychological aspects of systemic lupus erythematosus: Cognitive, function, mood, and self-report. The Journal of Rheumatology, 24, 998–1003.
Denburg, S. D., Carbotte, R. M., Denburg, J. A., Moore, P. M., & Lahita, R. G. (1997b). Cognition and mood in systemic lupus erythematosus. Annals of the New York Academy of Sciences (pp. 44–59). New York: The New York Academy of Sciences.
Denburg, S. D., Carbotte, R. M., Long, A. A., & Denburg, J. A. (1988). Neuropsychological correlates of serum lymphocytotoxic antibodies in systemic lupus erythematosus. Brain, Behavior, & Immunity, 2, 222–234.
Ellis, S. G., & Verity, M. A. (1979). Central nervous system involvement in systemic lupus erythematosus: a review of neuropathologic findings in 57 cases, 1955–1977. Seminars in Arthritis and Rheumatism, 8, 212–221.
Emori, A., Matsushima, E., Aihara, O., Ohta, K., Koike, R., Miyasaka, N., et al. (2005). Cognitive dysfunction in systemic lupus erythematosus. Psychiatry and Clinical Neurosciences, 59, 584–589.
Falcini, F., De Cristofaro, M. T. R., Ermini, M., Guarnieri, M., Massai, G., Olmastroni, M., et al. (1998). Regional cerebral blood flow in juvenile systemic lupus erythematosus: a prospective SPECT study. Journal of Rheumatology, 25, 583–588.
Filippi, M., Tortorella, C., Rovaris, M., Bozzali, M., Possa, F., Sormani, M. P., et al. (2000). Changes in the normal appearing brain tissue and cognitive impairment in multiple sclerosis. Journal of Neurology, Neurosurgery & Psychiatry, 68, 157–161.
Filley, C. M., Heaton, R. K., Nelson, L. M., Burks, J. S., Franklin, G. M., Filley, C. M., et al. (1989). A comparison of dementia in Alzheimer’s disease and multiple sclerosis. Archives of Neurology, 46, 157–161.
Fischer, J. S. (1988). Using the Wechsler Memory Scale-Revised to detect and characterize memory deficits in multiple sclerosis. Clinical Neuropsychologist, 2, 149–172.
Fisk, J. D., & Archibald, C. J. (2001). Limitations of the Paced Auditory Serial Addition Test as a measure of working memory in patients with multiple sclerosis. Journal of the International Neuropsychological Society, 7, 363–372.
Fluture, A., Chaudhari, S., & Frishman, W. H. (2003). Valvular heart disease and systemic lupus erythematosus: Therapeutic implications. Heart Disease, 5, 349–353.
Foong, J., Rozewicz, L., Quaghebeur, G., Davie, C. A., Kartsounis, L. D., Thompson, A. J., et al. (1997). Executive function in multiple sclerosis. The role of frontal lobe pathology. Brain, 120, 15–26.
Friedman, S. D., Stidley, C. A., Brooks, W. M., Hart, B. L., & Sibbitt, W. L. Jr. (1998). Brain injury and neurometabolic abnormalities in systemic lupus erythematosus. Radiology, 209, 79–84.
Ginsburg, K. S., Wright, E. A., Larson, M. G., Fossel, A. H., Albert, M., Schur, P. H., et al. (1992). A controlled study of the prevalence of cognitive dysfunction in randomly selected patients with systemic lupus erythematosus. Arthritis & Rheumatism, 35, 776–782.
Glanz, B. I., Schur, P. H., Lew, R. A., & Khoshbin, S. (2005). Lateralized cognitive dysfunction in patients with systemic lupus erythematosus. Lupus, 14, 896–902.
Glanz, B. I., Slonim, D., Urowitz, M. B., Gladman, D. D., Gough, J., & MacKinnon, A. (1997a). Pattern of neuropsychologic dysfunction in inactive systemic lupus erythematosus. Neuropsychiatry, Neuropsychology, & Behavioral Neurology, 10, 232–238.
Glanz, B. I., Slonim, D., Urowitz, M. B., Gladman, D. D., Gough, J., Math, M., et al. (1997b). Pattern of neuropsychologic dysfunction in inactive systemic lupus erythematosus. Neurpsychiatry, Neuropsychology, and Behavioral Neurology, 10, 232–238.
Govoni, M., Castellino, G., Padovan, M., Borrelli, M., Trotta, F., Govoni, M., et al. (2004). Recent advances and future perspective in neuroimaging in neuropsychiatric systemic lupus erythematosus. Lupus, 13, 149–158.
Grafman, J., Rao, S. M., Bernardin, L., & Leo, G. J. (1991). Automatic memory processes in patients with multiple sclerosis. Archives of Neurology, 48, 1072–1077.
Gronwall, D. M. A. (1977). Paced auditory serial addition task: A measure of recovery from concussion. Perceptual and Motor Skills, 44, 367–373.
Hachulla, E., Michon-Pasturel, U., Leys, D., Pruvo, J. P., Queyrel, V., Masy, E., et al. (1998). Cerebral magnetic resonance imaging in patients with or without antiphospholipid antibodies. Lupus, 7, 124–131.
Hanly, J. G., Fisk, J. D., Sherwood, G., & Eastwood, B. (1994). Clinical course of cognitive dysfunction in systemic lupus erythematosus. The Journal of Rheumatology, 21, 1825–1831.
Hanly, J. G., Fisk, J. D., Sherwood, G., Jones, E., Jones, J. V., & Eastwood, B. (1992). Cognitive impairment in patients with systemic lupus erythematosus. The Journal of Rheumatology, 19, 562–567.
Hanly, J. G., Liang, M. H., Moore, P. M., & Lahita, R. G. (1997). Cognitive disorders in systemic lupus erythematosus: Epidemiologic and clinical issues. Annals of the New York Academy of Sciences (pp. 60–68). New York: The New York Academy of Sciences.
Hauser, S. L., Oksenberg, J. R., Hauser, S. L., & Oksenberg, J. R. (2006). The neurobiology of multiple sclerosis: genes, inflammation, and neurodegeneration. Neuron, 52, 61–76.
Hay, E. M., Black, D., Huddy, A., Creed, F., Tomenson, B., Bernstein, R. M., et al. (1992). Psychiatric disorder and cognitive impairment in systemic lupus erythematosus. Arthritis and Rheumatism, 35, 411–416.
Hay, E. M., Huddy, A., Black, D., Mbaya, P., Tomenson, B., Bernstein, R. M., et al. (1994). A prospective study of psychiatric disorder and cognitive function in systemic lupus erythematosus. Annals of the Rheumatic Diseases, 53, 298–303.
Heaton, R. K. (1985). Neuropsychological findings in relapsing-remitting and chronic-progressive multiple sclerosis. Journal of Consulting & Clinical Psychology, 53, 103–110.
Huizinga, T. W. J., Steens, S. C. A., Van Buchem, M. A. (2001). Imaging modalities in central nervous system systemic lupus erythematosus. Current Opinion in Rheumatology, 13, 383–388.
Johnson, R. T., & Richardson, E. P. (1968). The neurological manifestations of systemic lupus erythematosus. Medicine, 47, 337–369.
Joseph, F. G., Lammie, G. A., & Scolding, N. J. (2007). CNS lupus: A study of 41 patients. Neurology, 69, 644–654.
Kao, C. H., Ho, Y. J., Lan, J. L., Changlai, S. P., Liao, K. K., & Chieng, P. U. (1999). Discrepancy between regional cerebral blood flow and glucose metabolism of the brain in systemic lupus erythematosus patients with normal brain magnetic resonance imaging findings. Arthritis & Rheumatism, 42, 61–68.
Kao, A. H., Sabatine, J. M., & Manzi, S. (2003). Update on vascular disease in systemic lupus erythematosus. Current Opinion in Rheumatology, 15, 519–527.
Kidd, D., Barkhof, F., McConnell, R., Algra, P. R., Allen, I. V., & Revesz, T. (1999). Cortical lesions in multiple sclerosis. Brain, 122, 17–26.
Knight, R. G., Devereux, R. C., & Godfrey, H. P. D. (1997). Psychosocial consequences of caring for a spouse with multiple sclerosis. Journal of Clinical and Experimental Neuropsychology, 19, 7–19.
Kozora, E., Arciniegas, D. B., Filley, C. M., Ellison, M. C., West, S. G., Brown, M. S., et al. (2005). Cognition, MRS neurometabolites, and MRI volumetrics in non-neuropsychiatric systemic lupus erythematosus: Preliminary data. Cognitive & Behavioral Neurology, 18, 159–162.
Kozora, E., Arciniegas, D. B., Zhang, L., West, S., Kozora, E., Arciniegas, D. B., et al. (2007). Neuropsychological patterns in systemic lupus erythematosus patients with depression. Arthritis Research & Therapy, 9, R48.
Kozora, E., Ellison, M. C., & West, S. (2004). Reliability and validity of the proposed American College of Rheumatology neuropsychological battery for systemic lupus erythematosus [see comment]. Arthritis & Rheumatism, 51, 810–818.
Kozora, E., Ellison, M. C., West, S., Kozora, E., Ellison, M. C., & West, S. (2006). Depression, fatigue, and pain in systemic lupus erythematosus (SLE): Relationship to the American College of Rheumatology SLE neuropsychological battery. Arthritis & Rheumatism, 55, 628–635.
Kozora, E., Laudenslager, M., Lemieux, A., & West, S. G. (2001). Inflammatory and hormonal measures predict neuropsychological functioning in systemic lupus erythematosus and rheumatoid arthritis patients. Journal of the International Neuropsychological Society, 7, 745–754.
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 & Rheumatism, 39, 2035–2045.
Kozora, E., West, S. G., Kotzin, B. L., Julian, L., Porter, S., Bigler, E., et al. (1998). Magnetic resonance imaging abnormalities and cognitive deficits in systemic lupus erythematosus patients without overt central nervous system disease. Arthritis & Rheumatism, 41, 41–47.
Kujala, P. (1994). Automatic and controlled information processing in multiple sclerosis. Brain, 117, 1115–1126.
Kutzelnigg, A., Lucchinetti, C. F., Stadelmann, C., Bruck, W., Rauschka, H., Bergmann, M., et al. (2005). Cortical demyelination and diffuse white matter injury in multiple sclerosis. Brain, 128, 2705–2712.
Kyttaris, V. C., & Tsokos, G. C. (2003). Uncovering the genetics of systemic lupus erythematosus. American Journal of Pharmacogenomics, 3, 193–202.
Langdon, D. W., & Thompson, A. J. (1999). Multiple sclerosis: A preliminary study of selected variables affecting rehabilitation outcome. Multiple Sclerosis, 5, 94–100.
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.
Leritz, E., Brandt, J., Minor, M., Reis-Jensen, F., & Petri, M. (2002). Neuropsychological functioning and its relationship to antiphospolipid antibodies in patients with systemic lupus erythematosus. Journal of Clinical and Experimental Neuropsychology, 24, 527–533.
Lim, M. K., Suh, C. H., Kim, H. J., Cho, Y. K., Choi, S. H., Kang, J. H., et al. (2000). Systemic lupus erythematosus: Brain MR imaging and single-voxel hydrogen 1 MR spectroscopy. Radiology, 217, 43–49.
Lin, W. Y., Wang, S. J., Yen, T. C., & Lan, J. L. (1997). Technetium-99m-HMPAObrain SPECT in systemic erythematosus with CNS involvement. Jouranal of Nuclear Medicine, 38, 1112–1115.
Litvan, I., Grafman, J., Vendrell, P., & Martinez, J. (1988). Slowed information processing in multiple sclerosis. Archives of Neurology, 45, 281–285.
Loukkola, J., Laine, M., Ainiala, H., Peltola, J., Metsanoja, R., Auvinen, A., et al. (2003). Cognitive impairment in systemic lupus erythematosus and neuropsychiatric systemic lupus erythematosus: A population-based neuropsychological study. Journal of Clinical & Experimental Neuropsychology, 25, 145–151.
Manzi, S., Meilahn, E. N., Rairie, J. E., Conte, C. G., Medsger, T. A. Jr., Jansen-McWilliams, L., et al. (1997). Age-specific incidence rates of myocardial infarction and angina in women with systemic lupus erythematosus: Comparison with the Framingham Study. American Journal of Epidemiology, 145, 408–415.
Miller, D. H., Buchanan, N., Barker, G., Morrissey, S. P., Kendall, B. E., Rudge, P., et al. (1992). Gadolinium-enhanced magnetic resonance imaging of the central nervous system in systemic lupus erythematosus. Journal of Neurology, 239, 460–464.
Minden, S. L. (1990). Memory impairment in multiple sclerosis. Journal of Clinical & Experimental Neuropsychology, 12, 566–586.
Mochizuki, T., Aotsuka, S., & Satoh, T. (1999). Clinical and laboratory features of lupus patients with complicating pulmonary disease. Respiratory Medicine, 93, 95–101.
Mok, C. C., Lau, C. S., & Wong, R. W. (2001). Neuropsychiatric manifestations and their clinical associations in southern Chinese patients with systemic lupus erythematosus. Journal of Rheumatology, 28, 766–771.
Monastero, R., Bettini, P., Del Zotto E., Cottini, E., Tincani, A., Balestrieri, G., Cattaneo, R., Camarda, R., Vignolo, L. A., 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, Feb 15.
Morgen, K., Sammer, G., Courtney, S. M., Wolters, T., Melchior, H., Blecker, C. R., et al. (2006). Evidence for a direct association between cortical atrophy and cognitive impairment in relapsing-remitting MS. Neuroimage, 30, 891–898.
Newman, S. P. (1993). Cognitive changes in systemic lupus erythematosus. Bailliere’s Clnical Rheumatology, 7, 357–373.
Nossent, J. C., Hovestadt, A., Schonefeld, D. H. W., & Swaak, A. J. G. (1991). Single-photon-emission computed tomography of the brain in the evaluation of cerebral lupus. Arthritis & Rheumatism, 34, 1397–1403.
Nuttall, S. L., Heaton, S., Piper, M. K., Martin, U., & Gordon, C. (2003). Cardiovascular risk in systemic lupus erythematosus—Evidence of increased oxidative stress and dyslipidaemia. Rheumatology, 42, 758–762.
O’Brien, A., Gaudino-Goering, E., Shawaryn, M., Komaroff, E., Moore, N. B., & DeLuca, J. (2007). Relationship of the Multiple Sclerosis Neuropsychological Questionnaire (MSNQ) to functional, emotional, and neuropsychological outcomes. Archives of Clinical Neuropsychology, 22, 933–948.
Otte, A., Weiner, S. M., Peter, H. H., Mueller, B. J., Goetze, M., Moser, E., et al. (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.
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.
Parmenter, B. A., Shucard, J. L., & Shucard, D. W. (2007a). Information processing deficits in multiple sclerosis: A matter of complexity. Journal of the International Neuropsychological Society, 13, 417–423.
Parmenter, B. A., Weinstock-Guttman, B., Garg, N., Munschauer, F., & Benedict, R. H. B. (2007b). Screening for cognitive impairment in MS using the Symbol Digit Modalities Test. Multiple Sclerosis (in press).
Parmenter, B. A., Zivadinov, R., Kerenyi, L., Gavett, R., Weinstock-Guttman, B., Dwyer, M., et al. (2007c). Validity of the Wisconsin Card Sorting and Delis–Kaplan Executive Function System (DKEFS) Sorting Tests in multiple sclerosis. Journal of Clinical & Experimental Neuropsychology, 29, 215–223.
Peterson, P. L., Axford, J. S., & Isenberg, D. (2005). Imaging in CNS lupus. Best Practice & Research in Clinical Rheumatology, 19, 727–739.
Peterson, J. W., Bo, L., Mork, S., Chang, A., & Trapp, B. D. (2001). Transected neurites, apoptotic neurons, and reduced inflammation in cortical multiple sclerosis lesions. Annals of Neurology, 50, 389–400.
Peterson, P. L., Howe, F. A., Clark, C. A., Axford, J. S., Peterson, P. L., Howe, F. A., et al. (2003). Quantitative magnetic resonance imaging in neuropsychiatric systemic lupus erythematosus. Lupus, 12, 897–902.
Peyser, J. M., Rao, S. M., LaRocca, N. G., & Kaplan, E. (1990). Guidelines for neuropsychological research in multiple sclerosis. Archives of Neurology, 47, 94–97.
Pirko, I., Lucchinetti, C. F., Sriram, S., Bakshi, R., Pirko, I., Lucchinetti, C. F., et al. (2007). Gray matter involvement in multiple sclerosis. Neurology, 68, 634–642.
Polman, C. H., Reingold, S. C., Edan, G., Filippi, M., Hartung, H. P., Kappos, L., et al. (2005). Diagnostic criteria for multiple sclerosis: 2005 revisions to the “McDonald criteria”. Annals of Neurology, 58, 840–846.
Prinster, A., Quarantelli, M., Orefice, G., Lanzillo, R., Brunetti, A., Mollica, C., et al. (2006). Grey matter loss in relapsing-remitting multiple sclerosis: A voxel-based morphometry study. Neuroimage, 29, 859–867.
Rademacher, J., Sohngen, D., Specker, C., Janda, I., & Sitzer, M. (1999). Cerebral microembolism, a disease marker for ischemic cerebrovascular events in the antiphospholipid syndrome of systemic lupus erythematosus? Acta Neurologica Scandinavica, 99, 356–361.
Ramasamy, D., Benedict, R. H. B., Dwyer, M., Stosic, M., Fritz, D., & Zivadinov, R. (2007). Extent of subcortical and cortical atrophy and disease severity in patients with multiple sclerosis. A case control study. Multiple Sclerosis, 13, S180.
Rao, S. M. (1990). A manual for the brief, repeatable battery of neuropsychological tests in multiple sclerosis. New York: National Multiple Sclerosis Society.
Rao, S. M. (1992). Neuropsychological screening battery for multiple sclerosis. Milwaukee, WI: Medical College of Wisconsin.
Rao, S. M., Grafman, J., DiGiulio, D., Mittenberg, W., Bernardin, L., Leo, G. J., et al. (1993). Memory dysfunction in multiple sclerosis: Its relation to working memory, semantic encoding, and implicit learning. Neuropsychology, 7, 364–374.
Rao, S. M., Hammeke, T. A., McQuillen, M. P., Khatri, B. O., & Lloyd, D. (1984). Memory disturbance in chronic progressive multiple sclerosis. Archives of Neurology, 41, 625–631.
Rao, S. M., Leo, G. J., Bernardin, L., & Unverzagt, F. (1991a). Cognitive dysfunction in multiple sclerosis. I. Frequency, patterns, and prediction. Neurology, 41, 685–691.
Rao, S. M., Leo, G. J., Ellington, L., Nauertz, T., Bernardin, L., & Unveragt, F. (1991b). Cognitive dysfunction in multiple sclerosis. II. Impact on employment and social functioning. Neurology, 41, 692–696.
Rao, S. M., Leo, G. J., Haughton, V. M., Aubin-Faubert, P. S., & Bernardin, L. (1989a). Correlation of magnetic resonance imaging with neuropsychological testing in multiple sclerosis. Neurology, 39, 161–166.
Rao, S. M., Leo, G. J., & St. Aubin-Faubert, P. (1989b). On the nature of memory disturbance in multiple sclerosis. Journal of Clinical and Experimental Neuropsychology, 11, 699–712.
Reitan, R. M. (1958). Validity of the Trail Making Test as an indicator of organic brain damage. Perceptual and Motor Skills, 8, 271–276.
Rey, A. (1964). L’Examen Clinique en Psychologie. Paris: Press Universitaire de France.
Roman, M. J., Shanker, B. A., Davis, A., Lockshin, M. D., Sammaritano, L., Simantov, R., et al. (2003). Prevalence and correlates of accelerated atherosclerosis in systemic lupus erythematosus. New England Journal of Medicine, 349, 2399–2406.
Rovaris, M., Bozzali, M., Rodegher, M., Tortorella, C., Comi, G., Filippi, M., et al. (1999). Brain MRI correlates of magnetization transfer imaging metrics in patients with multiple sclerosis. Journal of the Neurological Sciences, 166, 58–63.
Rovaris, M., Viti, B., Ciboddo, G., Gerevini, S., Capra, R., Iannucci, G., et al. (2000). Brain involvement in systemic immune mediated diseases: magnetic resonance and magnetisation transfer imaging study. Journal of Neurology, Neurosurgery & Psychiatry, 68, 170–177.
Ryan, L., Clark, C. M., Klonoff, H., Li, D., & Paty, D. (1996). Patterns of cognitive impairment in relapsing-remitting multiple sclerosis and their relationship to neuropathology on magnetic resonance images. Neuropsychology, 10, 176–193.
Sabet, A., Sibbitt, W. L. Jr., Stidley, C. A., Danska, J., & Brooks, W. M. (1998). Neurometabolite markers of cerebral injury in the antiphospholipid antibody syndrome of systemic lupus erythematosus. Stroke, 29, 2254–2260.
Schmidt, R., Schmidt, H., Curb, J. D., Masaki, K., White, L. R., & Launer, L. J. (2002). Early inflammation and dementia: A 25-year follow-up of the Honolulu–Asia Aging Study. Annals of Neurology, 52, 168–174.
Schultheis, M. T., Garay, E., & DeLuca, J. (2001). The influence of cognitive impairment on driving performance in multiple sclerosis. Neurology, 56, 1089–1094.
Schultheis, M. T., Garay, E., Millis, S. R., & DeLuca, J. (2002). Motor vehicle crashes and violations among drivers with multiple sclerosis. Archives of Physical Medicine & Rehabilitation, 83, 1175–1178.
Scolding, N. J., & Joseph, F. G. (2002). The neuropathology and pathogenesis of systemic lupus erythematosus. Neuropathology & Applied Neurobiology, 28, 173–189.
Selzer, F., Sutton-Tyrrell, K., Fitzgerald, S., Tracy, R., Kuller, L., & Manzi, S. (2001). Vascular stiffness in women with systemic lupus erythematosus. Hypertension, 37, 1075–1082.
Sepulcre, J., Sastre-Garriga, J., Cercignani, M., Ingle, G. T., Miller, D. H., & Thompson, A. J. (2006). Regional gray matter atrophy in early primary progressive multiple sclerosis: A voxel-based morphometry study. Archives of Neurology, 63, 1175–1180.
Shucard, J. L. P., Gaines, J. J. P., Ambrus, J. J. M. D., & Shucard, D. W. P. (2007). C-reactive protein and cognitive deficits in systemic lupus erythematosus. Cognitive & Behavioral Neurology, 20, 31–37.
Shucard, J. L., Parrish, J., Shucard, D. W., McCabe, D., Benedict, R. H. B., & Ambrus, J. (2004a). 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.
Shucard, J. L., Parrish, J., Shucard, D. W., McCabe, D. C., Benedict, R. H., & Ambrus, J. Jr. (2004b). 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.
Sibbitt, W. L. Jr., Sibbitt, R. R., & Brooks, W. M. (1999). Neuroimaging in neuropsychiatric systemic lupus erythematosus.[see comment]. Arthritis & Rheumatism, 42, 2026–2038.
Smith, A. (1982). Symbol digit modalities test: Manual. Los Angeles: Western Psychological Services.
Snyder, P. J., Cappelleri, J. C., Archibald, C. J., & Fisk, J. D. (2001). Improved detection of differential information-processing speed deficits between two disease-course types of multiple sclerosis. Neuropsychology, 15, 617–625.
Stoppe, G., Wildhagen, K., Seidel, J. W., Meyer, G. J., Schober, O., Heintz, P., et al. (1990). Positron emission tomography in neuropsychiatric lupus erythematosus. Neurology, 40, 304–308.
Swirsky-Sacchetti, T., Field, H. L., Mitchell, D. R., Seward, J., Lublin, F. D., Knobler, R. L., et al. (1992). The sensitivity of the Mini-Mental State Exam in the white matter dementia of multiple sclerosis. Journal of Clinical Psychology, 48, 779–786.
Tekok-Kilic, A., Benedict, R. H. B., Weinstock-Guttman, B., Dwyer, M., Carone, D., Srinivasaraghavan, B., et al. (2007). Independent contributions of cortical gray matter atrophy and ventricle enlargement for predicting neuropsychological impairment in multiple sclerosis. Neuroimage, 36, 1294–1300.
Teunissen, C. E., van Boxtel, M. P., Bosma, H., Bosmans, E., Delanghe, J., De Bruijn, C., et al. (2003). Inflammation markers in relation to cognition in a healthy aging population. Journal of Neuroimmunology, 134, 142–150.
Thornton, A. E. (1997). Memory impairment in multiple sclerosis: A quantitative review. Neuropsychology, 11, 357–366.
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.
Trapp, B. D., Ransohoff, R., & Rudick, R. (1999). Axonal pathology in multiple sclerosis: Relationship to neurologic disability. Current Opinion in Neurology, 12, 295–302.
Tsokos, G. C., & Liossis, S. N. (1998). Lymphocytes, cytokines, inflammation, and immune trafficking. Current Opinion in Rheumatology, 10, 417–425.
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.
Verma, S., Buchanan, M. R., & Anderson, T. J. (2003). Endothelial function testing as a biomarker of vascular disease. Circulation, 108, 2054–2059.
Vidailhet, M., Piette, J. C., Wechsler, B., Bousser, M. G., & Brunet, P. (1990). Cerebral venous thrombosis in systemic lupus erythematosus. Stroke, 21, 1226–1231.
Vleugels, L., Lafosse, C., van Nunen, A., Nachtergaele, S., Ketelaer, P., Charlier, M., et al. (2000). Visuoperceptual impairment in multiple sclerosis patients diagnosed with neuropsychological tasks. Multiple Sclerosis, 6, 241–254.
Vyse, T. J., & Kotzin, B. L. (1998). Genetic susceptibility to systemic lupus erythematosus. Annual Review of Immunology, 16, 261–292.
Wechsler, D. (1997). Wechsler Adult Intelligence Scale (3rd ed.). San Antonio: Psychological Corporation.
Weiner, S. M., Otte, A., Schumacher, M., Klein, R., Gutfleisch, J., Brink, I., Otto, P., Nitzsche, E. U., Moser, E., & Peter, H. H. (2000). Diagnosis and monitoring of central nervous system involvement in systemic lupus erythematosus: value of F-18 fluorodeoxyglucose PET. Annals of the Rheumatic Diseases, 59, 377–385.
Wekking, E. M. (1993). Psychiatric symptoms in systemic lupus erythematosus: An update. Psychosomatic Medicine, 55, 219–228.
Wekking, E. M., Nossent, J. C., van Dam, A. P., & Sdwaak, A. J. (1991). Cognitive and emotional disturbances in systemic lupus erythematosus. Psychotherapy & Psychosomatics, 55, 126–131.
West, S. G. (1994). Neuropsychiatric lupus. Rheumatic Diseases Clinics of North America, 20, 129–158.
Wishart, H. (1997). Neuropsychological aspects of multiple sclerosis: A quantitative review. Journal of Clinical & Experimental Neuropsychology, 19, 810–824.
Zivadinov, R., & Bakshi, R. (2004). Role of MRI in multiple sclerosis I: Inflammation and lesions. Frontiers in Bioscience, 9, 665–683.
Zivadinov, R., Sepcic, J., Nasuelli, D., De Masi, R., Bragadin, L. M., Tommasi, M. A., et al. (2001). A longitudinal study of brain atrophy and cognitive disturbances in the early phase of relapsing-remitting multiple sclerosis. Journal of Neurology, Neurosurgery & Psychiatry, 70, 773–780.
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Benedict, R.H.B., Shucard, J.L., Zivadinov, R. et al. Neuropsychological Impairment in Systemic Lupus Erythematosus: A Comparison with Multiple Sclerosis. Neuropsychol Rev 18, 149–166 (2008). https://doi.org/10.1007/s11065-008-9061-2
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DOI: https://doi.org/10.1007/s11065-008-9061-2