Neuropsychology Review

, Volume 18, Issue 2, pp 149–166

Neuropsychological Impairment in Systemic Lupus Erythematosus: A Comparison with Multiple Sclerosis

  • R. H. B. Benedict
  • J. L. Shucard
  • R. Zivadinov
  • D. W. Shucard
Article

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.

Keywords

Systemic lupus erythematosus Multiple sclerosis Cognition Memory Processing speed MRI Effect size 

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

  1. Ainala, H., Loukkola, J., Peltola, J., Korpela, M., & Hietaharju, A. (2001). The prevalence of neuropsychiatric syndromes in systemic lupus erythematosus. Neurology, 57, 496–500.Google Scholar
  2. 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.PubMedGoogle Scholar
  3. 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.PubMedGoogle Scholar
  4. American College of Rheumatology (1999). The American College of Rheumatology nomenclature and case definitions for neuropsychiatric lupus syndromes. Arthritis & Rheumatism, 42, 599–608.Google Scholar
  5. Archibald, C. J., & Fisk, J. D. (2000). Information processing efficiency in patients with multiple sclerosis. Journal of Clinical & Experimental Neuropsychology, 22, 686–701.Google Scholar
  6. 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.PubMedGoogle Scholar
  7. 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.PubMedGoogle Scholar
  8. 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.PubMedGoogle Scholar
  9. 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.Google Scholar
  10. Beatty, W. W. (2002). Fluency in multiple sclerosis: Which measure is best? Multiple Sclerosis, 8, 261–264.PubMedGoogle Scholar
  11. 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.PubMedGoogle Scholar
  12. 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.PubMedGoogle Scholar
  13. 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.Google Scholar
  14. 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.PubMedGoogle Scholar
  15. 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.Google Scholar
  16. Benedict, R. H. B. (1997). Brief visuospatial memory test—Revised: Professional manual. Odessa, Florida: Psychological Assessment Resources, Inc.Google Scholar
  17. 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.PubMedGoogle Scholar
  18. 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.Google Scholar
  19. Benedict, R., & Bobholz, J. (2007). Multiple sclerosis. Seminars in Neurology, 27, 78–86.PubMedGoogle Scholar
  20. 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.PubMedGoogle Scholar
  21. 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.PubMedGoogle Scholar
  22. 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.PubMedGoogle Scholar
  23. 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.PubMedGoogle Scholar
  24. 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.PubMedGoogle Scholar
  25. 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.Google Scholar
  26. 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.PubMedGoogle Scholar
  27. 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.PubMedGoogle Scholar
  28. 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.Google Scholar
  29. Benton, A. L., & Hamsher, K. (1989). Multilingual aphasia examination. Iowa City: AJA Associates.Google Scholar
  30. 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
  31. 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.PubMedGoogle Scholar
  32. 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.PubMedGoogle Scholar
  33. 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.PubMedGoogle Scholar
  34. 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.Google Scholar
  35. 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.Google Scholar
  36. 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.Google Scholar
  37. 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.PubMedGoogle Scholar
  38. 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.PubMedGoogle Scholar
  39. 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.PubMedGoogle Scholar
  40. 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.PubMedGoogle Scholar
  41. 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.PubMedGoogle Scholar
  42. 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.PubMedGoogle Scholar
  43. 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.PubMedGoogle Scholar
  44. 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.Google Scholar
  45. 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.PubMedGoogle Scholar
  46. 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.PubMedGoogle Scholar
  47. Cohen, J. (1988). Statistical power for the behavioral sciences. Hillsdale, NJ: Erlbaum.Google Scholar
  48. 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.Google Scholar
  49. Danner, M., Kasl, S. V., Abramson, J. L., & Vaccarino, V. (2003). Association between depression and elevated C-reactive protein. Psychosomatic Medicine, 65, 347–356.PubMedGoogle Scholar
  50. Delis, D. C., Kaplan, E., & Kramer, J. H. (2001). Delis–Kaplan executive function system. San Antonio, Texas: Psychological Corporation.Google Scholar
  51. 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.Google Scholar
  52. 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.PubMedGoogle Scholar
  53. 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.Google Scholar
  54. 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.Google Scholar
  55. 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.PubMedGoogle Scholar
  56. 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.Google Scholar
  57. Denburg, J. A., Carbotta, R. M., & Denburg, S. D. (1987a). Neuronal antibodies and cognitive function in systemic lupus erythematosus. Neurology, 37, 464–467.PubMedGoogle Scholar
  58. 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.PubMedGoogle Scholar
  59. 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.Google Scholar
  60. 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.PubMedGoogle Scholar
  61. 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.Google Scholar
  62. 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.Google Scholar
  63. 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.PubMedGoogle Scholar
  64. 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.PubMedGoogle Scholar
  65. 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.PubMedGoogle Scholar
  66. 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.Google Scholar
  67. 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.PubMedGoogle Scholar
  68. Fischer, J. S. (1988). Using the Wechsler Memory Scale-Revised to detect and characterize memory deficits in multiple sclerosis. Clinical Neuropsychologist, 2, 149–172.Google Scholar
  69. 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.PubMedGoogle Scholar
  70. Fluture, A., Chaudhari, S., & Frishman, W. H. (2003). Valvular heart disease and systemic lupus erythematosus: Therapeutic implications. Heart Disease, 5, 349–353.PubMedGoogle Scholar
  71. 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.PubMedGoogle Scholar
  72. 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.PubMedGoogle Scholar
  73. 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.Google Scholar
  74. 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.PubMedGoogle Scholar
  75. 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.Google Scholar
  76. 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.Google Scholar
  77. 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.PubMedGoogle Scholar
  78. 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.PubMedGoogle Scholar
  79. Gronwall, D. M. A. (1977). Paced auditory serial addition task: A measure of recovery from concussion. Perceptual and Motor Skills, 44, 367–373.PubMedGoogle Scholar
  80. 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.PubMedGoogle Scholar
  81. 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.PubMedGoogle Scholar
  82. 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.PubMedGoogle Scholar
  83. 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.Google Scholar
  84. 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.PubMedGoogle Scholar
  85. 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.PubMedGoogle Scholar
  86. 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.PubMedGoogle Scholar
  87. Heaton, R. K. (1985). Neuropsychological findings in relapsing-remitting and chronic-progressive multiple sclerosis. Journal of Consulting & Clinical Psychology, 53, 103–110.Google Scholar
  88. 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.Google Scholar
  89. Johnson, R. T., & Richardson, E. P. (1968). The neurological manifestations of systemic lupus erythematosus. Medicine, 47, 337–369.PubMedGoogle Scholar
  90. Joseph, F. G., Lammie, G. A., & Scolding, N. J. (2007). CNS lupus: A study of 41 patients. Neurology, 69, 644–654.PubMedGoogle Scholar
  91. 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.Google Scholar
  92. Kao, A. H., Sabatine, J. M., & Manzi, S. (2003). Update on vascular disease in systemic lupus erythematosus. Current Opinion in Rheumatology, 15, 519–527.PubMedGoogle Scholar
  93. Kidd, D., Barkhof, F., McConnell, R., Algra, P. R., Allen, I. V., & Revesz, T. (1999). Cortical lesions in multiple sclerosis. Brain, 122, 17–26.PubMedGoogle Scholar
  94. 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.PubMedGoogle Scholar
  95. 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.Google Scholar
  96. 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.Google Scholar
  97. 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.Google Scholar
  98. 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.Google Scholar
  99. 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.PubMedGoogle Scholar
  100. 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.Google Scholar
  101. 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.Google Scholar
  102. Kujala, P. (1994). Automatic and controlled information processing in multiple sclerosis. Brain, 117, 1115–1126.PubMedGoogle Scholar
  103. 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.PubMedGoogle Scholar
  104. Kyttaris, V. C., & Tsokos, G. C. (2003). Uncovering the genetics of systemic lupus erythematosus. American Journal of Pharmacogenomics, 3, 193–202.PubMedGoogle Scholar
  105. Langdon, D. W., & Thompson, A. J. (1999). Multiple sclerosis: A preliminary study of selected variables affecting rehabilitation outcome. Multiple Sclerosis, 5, 94–100.PubMedGoogle Scholar
  106. 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.PubMedGoogle Scholar
  107. 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.PubMedGoogle Scholar
  108. 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.PubMedGoogle Scholar
  109. 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.Google Scholar
  110. Litvan, I., Grafman, J., Vendrell, P., & Martinez, J. (1988). Slowed information processing in multiple sclerosis. Archives of Neurology, 45, 281–285.PubMedGoogle Scholar
  111. 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.Google Scholar
  112. 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.PubMedGoogle Scholar
  113. 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.PubMedGoogle Scholar
  114. Minden, S. L. (1990). Memory impairment in multiple sclerosis. Journal of Clinical & Experimental Neuropsychology, 12, 566–586.Google Scholar
  115. Mochizuki, T., Aotsuka, S., & Satoh, T. (1999). Clinical and laboratory features of lupus patients with complicating pulmonary disease. Respiratory Medicine, 93, 95–101.PubMedGoogle Scholar
  116. 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.PubMedGoogle Scholar
  117. 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.Google Scholar
  118. 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.PubMedGoogle Scholar
  119. Newman, S. P. (1993). Cognitive changes in systemic lupus erythematosus. Bailliere’s Clnical Rheumatology, 7, 357–373.Google Scholar
  120. 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.Google Scholar
  121. 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.PubMedGoogle Scholar
  122. 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.PubMedGoogle Scholar
  123. 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.PubMedGoogle Scholar
  124. 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.PubMedGoogle Scholar
  125. 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.PubMedGoogle Scholar
  126. 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).Google Scholar
  127. 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.Google Scholar
  128. Peterson, P. L., Axford, J. S., & Isenberg, D. (2005). Imaging in CNS lupus. Best Practice & Research in Clinical Rheumatology, 19, 727–739.Google Scholar
  129. 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.PubMedGoogle Scholar
  130. 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.PubMedGoogle Scholar
  131. 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.PubMedGoogle Scholar
  132. 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.PubMedGoogle Scholar
  133. 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.PubMedGoogle Scholar
  134. 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.PubMedGoogle Scholar
  135. 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.PubMedGoogle Scholar
  136. 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.Google Scholar
  137. Rao, S. M. (1990). A manual for the brief, repeatable battery of neuropsychological tests in multiple sclerosis. New York: National Multiple Sclerosis Society.Google Scholar
  138. Rao, S. M. (1992). Neuropsychological screening battery for multiple sclerosis. Milwaukee, WI: Medical College of Wisconsin.Google Scholar
  139. 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.Google Scholar
  140. 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.PubMedGoogle Scholar
  141. 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.PubMedGoogle Scholar
  142. 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.PubMedGoogle Scholar
  143. 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.PubMedGoogle Scholar
  144. 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.PubMedGoogle Scholar
  145. Reitan, R. M. (1958). Validity of the Trail Making Test as an indicator of organic brain damage. Perceptual and Motor Skills, 8, 271–276.CrossRefGoogle Scholar
  146. Rey, A. (1964). L’Examen Clinique en Psychologie. Paris: Press Universitaire de France.Google Scholar
  147. 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.PubMedGoogle Scholar
  148. 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.PubMedGoogle Scholar
  149. 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.Google Scholar
  150. 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.Google Scholar
  151. 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.PubMedGoogle Scholar
  152. 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.PubMedGoogle Scholar
  153. Schultheis, M. T., Garay, E., & DeLuca, J. (2001). The influence of cognitive impairment on driving performance in multiple sclerosis. Neurology, 56, 1089–1094.PubMedGoogle Scholar
  154. 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.Google Scholar
  155. Scolding, N. J., & Joseph, F. G. (2002). The neuropathology and pathogenesis of systemic lupus erythematosus. Neuropathology & Applied Neurobiology, 28, 173–189.Google Scholar
  156. 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.PubMedGoogle Scholar
  157. 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.PubMedGoogle Scholar
  158. 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.Google Scholar
  159. 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.PubMedGoogle Scholar
  160. 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.PubMedGoogle Scholar
  161. Sibbitt, W. L. Jr., Sibbitt, R. R., & Brooks, W. M. (1999). Neuroimaging in neuropsychiatric systemic lupus erythematosus.[see comment]. Arthritis & Rheumatism, 42, 2026–2038.Google Scholar
  162. Smith, A. (1982). Symbol digit modalities test: Manual. Los Angeles: Western Psychological Services.Google Scholar
  163. 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.PubMedGoogle Scholar
  164. 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.PubMedGoogle Scholar
  165. 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.PubMedGoogle Scholar
  166. 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.PubMedGoogle Scholar
  167. 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.PubMedGoogle Scholar
  168. Thornton, A. E. (1997). Memory impairment in multiple sclerosis: A quantitative review. Neuropsychology, 11, 357–366.PubMedGoogle Scholar
  169. 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.PubMedGoogle Scholar
  170. Trapp, B. D., Ransohoff, R., & Rudick, R. (1999). Axonal pathology in multiple sclerosis: Relationship to neurologic disability. Current Opinion in Neurology, 12, 295–302.PubMedGoogle Scholar
  171. Tsokos, G. C., & Liossis, S. N. (1998). Lymphocytes, cytokines, inflammation, and immune trafficking. Current Opinion in Rheumatology, 10, 417–425.PubMedGoogle Scholar
  172. 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
  173. Verma, S., Buchanan, M. R., & Anderson, T. J. (2003). Endothelial function testing as a biomarker of vascular disease. Circulation, 108, 2054–2059.PubMedGoogle Scholar
  174. Vidailhet, M., Piette, J. C., Wechsler, B., Bousser, M. G., & Brunet, P. (1990). Cerebral venous thrombosis in systemic lupus erythematosus. Stroke, 21, 1226–1231.PubMedGoogle Scholar
  175. 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.PubMedGoogle Scholar
  176. Vyse, T. J., & Kotzin, B. L. (1998). Genetic susceptibility to systemic lupus erythematosus. Annual Review of Immunology, 16, 261–292.PubMedGoogle Scholar
  177. Wechsler, D. (1997). Wechsler Adult Intelligence Scale (3rd ed.). San Antonio: Psychological Corporation.Google Scholar
  178. 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.PubMedGoogle Scholar
  179. Wekking, E. M. (1993). Psychiatric symptoms in systemic lupus erythematosus: An update. Psychosomatic Medicine, 55, 219–228.PubMedGoogle Scholar
  180. 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.CrossRefGoogle Scholar
  181. West, S. G. (1994). Neuropsychiatric lupus. Rheumatic Diseases Clinics of North America, 20, 129–158.PubMedGoogle Scholar
  182. Wishart, H. (1997). Neuropsychological aspects of multiple sclerosis: A quantitative review. Journal of Clinical & Experimental Neuropsychology, 19, 810–824.Google Scholar
  183. Zivadinov, R., & Bakshi, R. (2004). Role of MRI in multiple sclerosis I: Inflammation and lesions. Frontiers in Bioscience, 9, 665–683.PubMedGoogle Scholar
  184. 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.Google Scholar

Copyright information

© Springer Science+Business Media, LLC 2008

Authors and Affiliations

  • R. H. B. Benedict
    • 1
  • J. L. Shucard
    • 1
  • R. Zivadinov
    • 2
  • D. W. Shucard
    • 1
  1. 1.Division of Cognitive and Behavioral Neurosciences, State University of New York (SUNY) at Buffalo, School of Medicine, Jacobs Neurological InstituteBuffalo General HospitalBuffaloUSA
  2. 2.Buffalo Neuroimaging Analysis Center, Department of Neurology, State University of New York (SUNY) at Buffalo, School of Medicine, Jacobs Neurological InstituteBuffalo General HospitalBuffaloUSA

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