Neurocognitive Function in Systemic Autoimmune and Rheumatic Diseases

  • Amy H. Kao
  • Carol M. Greco
  • Suzanne L. Gharib
  • Sue R. Beers
Chapter

Abstract

An autoimmune disease is a disorder in which the body’s immune system attacks itself. The dysregulation of the immune system associated with systemic autoimmune diseases can affect various organs systems, including the brain. This chapter will review the neuropsychological involvement and the resulting cognitive changes associated with three systemic autoimmune or rheumatic diseases: systemic lupus erythematosus (SLE), rheumatoid arthritis (RA), and primary Sjögren’s syndrome (SS). Diagnosis, neuropsychological assessment, and treatment planning are challenging since most of the disease manifestations are nonspecific. Due to the abundant literature on cognitive dysfunction in SLE as compared to the other two diseases, the discussion of cognition is focused mainly in SLE.

Keywords

Fatigue Depression Aspirin Glucocorticoid NMDA 

References

  1. 1.
    Danchenko N, Satia J, Anthony M. Epidemiology of systemic lupus erythematosus: a comparison of worldwide disease burden. Lupus. 2006;15(5):308–18.PubMedCrossRefGoogle Scholar
  2. 2.
    Ainiala H, Loukkola J, Peltola J, et al. The prevalence of neuropsychiatric syndromes in systemic lupus erythematosus. Neurology. 2001;57:496–99.PubMedCrossRefGoogle Scholar
  3. 3.
    Brey RL, Holliday SL, Saklad AR, et al. Neuropsychiatric syndromes in lupus: prevalence using standardized definitions. Neurology. 2002;58(8):1214–20.PubMedCrossRefGoogle Scholar
  4. 4.
    Hanly J, Fisk J, McCurdy G, et al. Neuropsychiatric syndromes in patients with systemic lupus erythematosus and rheumatoid arthritis. J Rheumatol. 2005;32(8):1459–1456.Google Scholar
  5. 5.
    Hanly JG, Urowitz MB, Sanchez-Guerrero J, et al. Neuropsychiatric events at the time of diagnosis of systemic lupus erythematosus: an international inception cohort study. Arthritis Rheum. 2007;56(1):265–73.PubMedCrossRefGoogle Scholar
  6. 6.
    Kovacs J, Urowitz MB, Gladman D. Dilemmas in neuropsychiatric lupus. Rheum Dis Clin North Am. 1993;19:795–819.PubMedGoogle Scholar
  7. 7.
    ACR Ad Hoc Committee on Neuropsychiatric Lupus Nomenclature. The American College of Rheumatology nomenclature and case definitions for neuropsychiatric lupus syndromes. Arthritis Rheum. 1999;42:599–608.CrossRefGoogle Scholar
  8. 8.
    Tan E, Cohen A, Fries J. The 1982 revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum. 1982;25:1271–77.PubMedCrossRefGoogle Scholar
  9. 9.
    Hochberg M. Updating the American College of Rheumatology revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum. 1997;40:1725.PubMedCrossRefGoogle Scholar
  10. 10.
    Kowal C, DeGiorgio LA, Nakaoka T, et al. Cognition and immunity: antibody impairs memory. Immunity. 2004;21(2):179–88.PubMedCrossRefGoogle Scholar
  11. 11.
    Huerta PT, Kowal C, DeGiorgio LA, et al. Immunity and behavior: antibodies alter emotion. Proc Natl Acad Sci USA. 2006;103(3):678–83.PubMedCrossRefGoogle Scholar
  12. 12.
    Lapteva L, Nowak M, Yarboro CH, et al. Anti-N-methyl-D-aspartate receptor antibodies, cognitive dysfunction, and depression in systemic lupus erythematosus. Arthritis Rheum. 2006;54(8):2505–14.PubMedCrossRefGoogle Scholar
  13. 13.
    Harrison MJ, Ravdin LD, Lockshin MD. Relationship between serum NR2a antibodies and cognitive dysfunction in systemic lupus erythematosus. Arthritis Rheum. 2006;54(8):2515–22.PubMedCrossRefGoogle Scholar
  14. 14.
    Hanly J, Robichaud J, Fisk J. Anti-NR2 glutamate receptor antibodies and cognitive function in systemic lupus erythematosus. J Rheumatol. 2006;33(8):1553–58.PubMedGoogle Scholar
  15. 15.
    McLaurin EY, Holliday SL, Williams P, et al. Predictors of cognitive dysfunction in patients with systemic lupus erythematosus. Neurology. 2005;64(2):297–303.PubMedCrossRefGoogle Scholar
  16. 16.
    Tomietto P, Annese V, D‘agostini S, et al. General and specific factors associated with severity of cognitive impairment in systemic lupus erythematosus. Arthritis Rheum. 2007;57(8):1461–72.PubMedCrossRefGoogle Scholar
  17. 17.
    Tektonidou MG, Varsou N, Kotoulas G, et al. Cognitive deficits in patients with antiphospholipid syndrome: association with clinical, laboratory, and brain magnetic resonance imaging findings. Arch Intern Med. 2006;166(20):2278–84.PubMedCrossRefGoogle Scholar
  18. 18.
    Kent M, Alvarez F, Vogt E, et al. Monoclonal antiphosphatidylserine antibodies react directly with feline and murine central nervous system. J Rheumatol. 1997;24(9):1725–33.PubMedGoogle Scholar
  19. 19.
    Shoenfeld Y, Nahum A, Korczyn A, et al. Neuronal-binding antibodies from patients with antiphospholipid syndrome induce cognitive deficits following intrathecal passive transfer. Lupus. 2003;12(6):436–42.PubMedCrossRefGoogle Scholar
  20. 20.
    Caronti B, Pittoni V, Palladini G, et al. Anti-beta 2-glycoprotein I antibodies bind to central nervous system. J Neuro Sci. 1998;156(2):211–19.CrossRefGoogle Scholar
  21. 21.
    Caronti B, Calderaro C, Alessandri C, et al. Serum anti-beta2-glycoprotein I antibodies from patients with antiphospholipid antibody syndrome bind central nervous system cells. J Autoimmun. 1998;11(5):425–29.PubMedCrossRefGoogle Scholar
  22. 22.
    Terashi H, Uchiyama S, Hashimoto S, et al. Clinical characteristics of stroke patients with antiphospholipid antibodies. Cerebrovasc Dis. 2005;19(6):384–90.PubMedCrossRefGoogle Scholar
  23. 23.
    Nencini P, Baruffi M, Abbate R, et al. Lupus anticoagulant and anticardiolipin antibodies in young adults with cerebral ischemia. Stroke. 1992;23(2):189–93.PubMedCrossRefGoogle Scholar
  24. 24.
    Ferraccioli G, Poi ED, Gregorio FD, et al. Changes in regional cerebral blood flow after a cold hand test in systemic lupus erythematosus patients with Raynaud’s syndrome. Lancet. 1999;354(9196):2135–2136.PubMedCrossRefGoogle Scholar
  25. 25.
    Carbotte R, Denburg S, Denburg J. Cognitive dysfunction in systemic lupus erythematosus is independent of active disease. J Rheumatol. 1995;22(5):863–67.PubMedGoogle Scholar
  26. 26.
    Hanly J, Fisk J, Sherwood G, et al. Clinical course of cognitive dysfunction in systemic lupus erythematosus. J Rheumatol. 1994;21(10):1825–31.PubMedGoogle Scholar
  27. 27.
    Carlomagno S, Migliaresi S, Ambrosone L, et al. Cognitive impairment in systemic lupus erythematosus: a follow-up study. J Neurol. 2000;247:273–79.PubMedCrossRefGoogle Scholar
  28. 28.
    Caltagirone C, Gainotti G, Masullo C, et al. Validity of some neuropsychological tests in the assessment of mental deterioration. Acta Psychiatr Scand. 1979;60(1):50–56.PubMedCrossRefGoogle Scholar
  29. 29.
    de Quervain DJF, Roozendaal B, McGaugh JL. Stress and glucocorticoids impair retrieval of long-term spatial memory. Nature. 1998;394(6695):787–90.PubMedCrossRefGoogle Scholar
  30. 30.
    Keenan PA, Jacobson MW, Soleymani RM, et al. The effect on memory of chronic prednisone treatment in patients with systemic disease. Neurology. 1996;47(6):1396–402.PubMedCrossRefGoogle Scholar
  31. 31.
    Coluccia D, Wolf OT, Kollias S, et al. Glucocorticoid therapy-induced memory deficits: acute versus chronic effects. J Neurosci. 2008;28(13):3474–78.PubMedCrossRefGoogle Scholar
  32. 32.
    de Quervain DJF, Roozendaal B, Nitsch RM, et al. Acute cortisone administration impairs retrieval of long-term declarative memory in humans. Nat Neurosci. 2000;3(4):313–314.PubMedCrossRefGoogle Scholar
  33. 33.
    Holliday SL, Navarete G, Escalante A, et al. Demographic, symptomatic, and serologic predictors of cognitive function in systemic lupus erythematosus: preliminary results from SALUD. Abstract. J Int Neuropsychol Soc. 2000;6:231–232.Google Scholar
  34. 34.
    Gladman DD, Urowitz MB, Slonim D, et al. Evaluation of predictive factors for neurocognitive dysfunction in patients with inactive systemic lupus erythematosus. J Rheumatol. 2000;27:2367–71.PubMedGoogle Scholar
  35. 35.
    Glanz BI, Slonim D, Urowitz MB, et al. Pattern of neuropsychologic dysfunction in inactive systemic lupus erythematosus. Neuropsychiatry Neuropsychol Behav Neurol. 1997;10:232–38.PubMedGoogle Scholar
  36. 36.
    Hay EM, Black D, Huddy A, et al. Psychiatric disorder and cognitive impairment in systemic lupus erythematosus. Arthritis Rheum. 1992;35:411–16.PubMedCrossRefGoogle Scholar
  37. 37.
    Kozora E, Thompson LL, West SG, et al. Analysis of cognitive and psychological deficits in systemic lupus erythematosus patients without overt central nervous system disease. Arthritis Rheum. 1996;39(12):2035–45.PubMedCrossRefGoogle Scholar
  38. 38.
    Kozora E, Ellison MC, West S. Depression, fatigue, and pain in systemic lupus erythematosus (SLE): relationship to the American College of Rheumatology SLE neuropsychological battery. Arthritis Rheum. 2006;55:628–35.PubMedCrossRefGoogle Scholar
  39. 39.
    Carbotte RM, Denburg SD, Denburg JA. Prevalence of cognitive impairment in systemic lupus erythematosus. J Nerv Ment Dis. 1986;174:357–64.PubMedCrossRefGoogle Scholar
  40. 40.
    Wekking EM, Nossent JC, van Dam AP, et al. Cognitive and emotional disturbances in systemic lupus erythematosus. Psychother Psychosom. 1991;55:126–31.PubMedCrossRefGoogle Scholar
  41. 41.
    Monastero R, Bettini P, Del Zotto E, et al. Prevalence and pattern of cognitive impairment in systemic lupus erythematosus patients with and without overt neuropsychiatric manifestations. J Neurol Sci. 2001;184(1):33–39.PubMedCrossRefGoogle Scholar
  42. 42.
    Kozora E, Arciniegas DB, Filley CM, et al. Cognitive and neurologic status in patients with systemic lupus erythematosus without major neuropsychiatric syndromes. Arthritis Rheum. 2008;59(11):1639–46.PubMedCrossRefGoogle Scholar
  43. 43.
    Kozora E, Arciniegas D, Zhang L, et al. Neuropsychological patterns in systemic lupus erythematosus patients with depression. Arthritis Res Ther. 2007;9(3):R48.PubMedCrossRefGoogle Scholar
  44. 44.
    Peralta-Ramirez MI, Coin-Mejias MA, Jimenez-Alonso J, et al. Stress as a predictor of cognitive functioning in lupus. Lupus. 2006;15(12):858–64.PubMedCrossRefGoogle Scholar
  45. 45.
    Isshi K, Hirohata S. Differential roles of the anti-ribosomal P antibody and antineuronal antibody in the pathogenesis of central nervous system involvement in systemic lupus erythematosus. Arthritis Rheum. 1998;41(10):1819–27.PubMedCrossRefGoogle Scholar
  46. 46.
    Abdel-Nasser A, Ghaleb R, Mahmoud J, et al. Association of anti-ribosomal P protein antibodies with neuropsychiatric and other manifestations of systemic lupus erythematosus. Clin Rheumatol. 2008;27(11):1377–85.Google Scholar
  47. 47.
    Gerli R, Caponi L, Tincani A, et al. Clinical and serological associations of ribosomal P autoantibodies in systemic lupus erythematosus: prospective evaluation in a large cohort of Italian patients. Rheumatology. 2002;41(12):1357–66.PubMedCrossRefGoogle Scholar
  48. 48.
    Kozora E, Ellison MC, West S. Reliability and validity of the proposed American College of Rheumatology neuropsychological battery for systemic lupus erythematosus. Arthritis Rheum. 2004;51(5):810–18.PubMedCrossRefGoogle Scholar
  49. 49.
    Reeves D, Bleiberg J, Spector J. Validation of the ANAM battery in multi-center head injury studies [abstract]. Arch Clin Neuropsychol. 1993;8:356.Google Scholar
  50. 50.
    Reeves D, Kane R, Winter K. Automated neuropsychological assessment metrics (ANAM V3.11a/96). User’s manual: clinical and neurotoxicology subset. San Diego, CA: National Cognitive Foundation; 1996.Google Scholar
  51. 51.
    Petri M, Naqibuddin M, Carson K, et al. Cognitive function in a systemic lupus erythematosus inception cohort. J Rheumatol. 2008;35(9):1776–81.PubMedGoogle Scholar
  52. 52.
    Holliday S, Navarrete M, Hermosillo-Romo D, et al. Validating a computerized neuropsychological test battery for mixed ethnic lupus patients. Lupus. 2003;12(9):697–703.PubMedCrossRefGoogle Scholar
  53. 53.
    Roebuck-Spencer TM, Yarboro C, Nowak M, et al. Use of computerized assessment to predict neuropsychological functioning and emotional distress in patients with systemic lupus erythematosus. Arthritis Rheum. 2006;55(3):434–41.PubMedCrossRefGoogle Scholar
  54. 54.
    Ainiala H, Dastidar P, Loukkola J, et al. Cerebral MRI abnormalities and their association with neuropsychiatric manifestations in SLE: a population-based study. Scand J Rheumatol. 2005;34(5):376–82.PubMedCrossRefGoogle Scholar
  55. 55.
    Kozora E, Arciniegas DB, Filley CM, et al. Cognition, MRS neurometabolites, and MRI volumetrics in non-neuropsychiatric systemic lupus erythematosus: preliminary data. Cogn Behav Neurol. 2005;18(3):159–62.PubMedCrossRefGoogle Scholar
  56. 56.
    Appenzeller S, Li LM, Costallat LTL, et al. Evidence of reversible axonal dysfunction in systemic lupus erythematosus: a proton MRS study. Brain. 2005;128(12):2933–40.PubMedCrossRefGoogle Scholar
  57. 57.
    Narayana P. Magnetic resonance spectroscopy in the monitoring of multiple sclerosis. J Neuroimaging. 2005;15(4 Suppl):46S–57S.PubMedCrossRefGoogle Scholar
  58. 58.
    Appenzeller S, Li LM, Costallat LTL, et al. Neurometabolic changes in normal white matter may predict appearance of hyperintense lesions in systemic lupus erythematosus. Lupus. 2007;16(12):963–71.PubMedCrossRefGoogle Scholar
  59. 59.
    Kao C-H, Lan J-L, ChangLai S-P, et al. The role of FDG-PET, HMPAO-SPET and MRI in the detection of brain involvement in patients with systemic lupus erythematosus. Eur J Nucl Med Mol Imaging. 1999;26(2):129–34.CrossRefGoogle Scholar
  60. 60.
    Kao C-H, Ho Y-J, Lan J-L, et al. 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 Rheum. 1999;42(1):61–68.PubMedCrossRefGoogle Scholar
  61. 61.
    Grunwald F, Schomburg A, Badali A, et al. 18FDG PET and acetazolamide-enhanced 99mTc-HMPAO SPET in systemic lupus erythematosus. Eur J Nucl Med. 1995;22:1073–77.PubMedCrossRefGoogle Scholar
  62. 62.
    Rocca MA, Agosta F, Mezzapesa DM, et al. An fMRI study of the motor system in patients with neuropsychiatric systemic lupus erythematosus. NeuroImage. 2006;30(2):478–84.PubMedCrossRefGoogle Scholar
  63. 63.
    Fitzgibbon BM, Fairhall SL, Kirk IJ, et al. Functional MRI in NPSLE patients reveals increased parietal and frontal brain activation during a working memory task compared with controls. Rheumatology. 2008;47(1):50–53.PubMedCrossRefGoogle Scholar
  64. 64.
    Bombardier C, Gladman D, Urowitz M, et al. Derivation of the SLEDAI: a disease activity index for lupus patients. The Committee on Prognosis Studies in SLE. Arthritis Rheum. 1992;35(6):630–40.PubMedCrossRefGoogle Scholar
  65. 65.
    DiFrancesco MW, Holland SK, Ris MD, et al. Functional magnetic resonance imaging assessment of cognitive function in childhood-onset systemic lupus erythematosus: a pilot study. Arthritis Rheum. 2007;56(12):4151–63.PubMedCrossRefGoogle Scholar
  66. 66.
    Gladman D, Ginzler E, Goldsmith C, et al. The development and initial validation of the systemic lupus international collaborating clinics/American college of rheumatology damage index for systemic lupus erythematosus. Arthritis Rheum. 1996;39(3):363–69.PubMedCrossRefGoogle Scholar
  67. 67.
    Robbins T, James M, Owen A, et al. Cambridge neuropsychological test automated battery (CANTAB): a factor analytic study of a large sample of normal elderly volunteers. Dementia. 1994;5(5):266–81.PubMedGoogle Scholar
  68. 68.
    Robbins T, James M, Owen A, et al. A study of performance on tests from the CANTAB battery sensitive to frontal lobe dysfunction in a large sample of normal volunteers: implications for theories of executive functioning and cognitive aging. Cambridge Neuropsychological Test Automated Battery. J Int Neuropsychol Soc. 1998;4(5):474–90.PubMedCrossRefGoogle Scholar
  69. 69.
    Chase HW, Clark L, Sahakian BJ, et al. Dissociable roles of prefrontal subregions in self-ordered working memory performance. Neuropsychologia. 2008;46(11):2650–61.PubMedCrossRefGoogle Scholar
  70. 70.
    Bartolini M, Candela M, Brugni M, et al. Are behaviour and motor performances of rheumatoid arthritis patients influenced by subclinical cognitive impairments? A clinical and neuroimaging study. Clin Exp Rheumatol. 2002;20(4):491–97.PubMedGoogle Scholar
  71. 71.
    Feldmann R, Weglage J, Roth J, et al. Systemic juvenile rheumatoid arthritis: cognitive function and social adjustment. Ann Neurol. 2005;58(4):605–09.PubMedCrossRefGoogle Scholar
  72. 72.
    Dick B, Eccleston C, Crombez G. Attentional functioning in fibromyalgia, rheumatoid arthritis, and musculoskeletal pain patients. Arthritis Rheum. 2002;47(6):639–44.PubMedCrossRefGoogle Scholar
  73. 73.
    DeLuca J, Christodoulou C, Diamond B, et al. Working memory deficits in chronic fatigue syndrome: differentiating between speed and accuracy of information processing. J Int Neuropsychol Soc. 2004;10(1):101–09.PubMedCrossRefGoogle Scholar
  74. 74.
    Brown SC, Glass JM, Park DC. The relationship of pain and depression to cognitive function in rheumatoid arthritis patients. Pain. 2002;96(3):279–84.PubMedCrossRefGoogle Scholar
  75. 75.
    Smith G, Bondi MNormal aging, mild cognitive impairment, and Alzheimer’s disease. In: Morgan J, Ricker J, editors. Textbook of clinical neuropsychology. New York, NY: Taylor & Francis; 2008. pp. 762–780.Google Scholar
  76. 76.
    Kozora E, Laudenslager M, Lemieux A, et al. Inflammatory and hormonal measures predict neuropsychological functioning in systemic lupus erythematosus and rheumatoid arthritis patients. J Int Neuropsychol Soc. 2001;7(6):745–54.PubMedCrossRefGoogle Scholar
  77. 77.
    Orman B, Sterin-Borda L, De Couto Pita A, Reina S, Borda E. Anti-brain cholinergic auto antibodies from primary Sjögren syndrome sera modify simultaneously cerebral nitric oxide and prostaglandin biosynthesis. Int Immunopharmacol. 2007;7(12):1535–43.Google Scholar
  78. 78.
    Mauch E, Volk C, Kratzsch G, et al. Neurological and neuropsychiatric dysfunction in primary Sjogren’s syndrome. Acta Neurol Scand. 1994;89(1):31–35.PubMedCrossRefGoogle Scholar
  79. 79.
    Belin C, Moroni C, Caillat-Vigneron N, et al. Central nervous system involvement in Sjogren’s syndrome: evidence from neuropsychological testing and HMPAO-SPECT. Ann Med Interne. 1999;150(8):598–604.Google Scholar
  80. 80.
    Malinow KL, Molina R, Gordon B, et al. Neuropsychiatric dysfunction in primary Sjogren’s syndrome. Ann Intern Med. 1985;103(3):344–50.PubMedGoogle Scholar
  81. 81.
    Alexander EL. Neurologic disease in Sjogren’s syndrome: mononuclear inflammatory vasculopathy affecting central/peripheral nervous system and muscle. A clinical review and update of immunopathogenesis. Rheum Dis Clin North Am. 1993;19(4):869–908.PubMedGoogle Scholar
  82. 82.
    Harboe E, Tjensvoll AB, Maroni S, et al. Neuropsychiatric syndromes in patients with systemic lupus erythematosus and primary Sjogren’s syndrome – A comparative population-based study. Ann Rheum Dis. 2008; ard.2008.098301.Google Scholar
  83. 83.
    Bertoli A, Fernandez M, Alarcon G, et al. Systemic lupus erythematosus in a multiethnic US cohort LUMINA (XLI): factors predictive of self-reported work disability. Ann Rheum Dis. 2007;66(1):12–17.PubMedCrossRefGoogle Scholar
  84. 84.
    Utset TO, Chohan S, Booth SA, et al. Correlates of formal work disability in an urban university systemic lupus erythematosus practice. J Rheumatol. 2008;35:1046–52.PubMedGoogle Scholar
  85. 85.
    Scofield L, Reinlib L, Alarcon GS, et al. Employment and disability issues in systemic lupus erythematosus: a review. Arthritis Rheum. 2008;59(10):1475–79.PubMedCrossRefGoogle Scholar
  86. 86.
    Katz P, Morris A, Trupin L, et al. Disability in valued life activities among individuals with systemic lupus erythematosus. Arthritis Rheum. 2008;59(4):465–73.PubMedCrossRefGoogle Scholar
  87. 87.
    Utset TO, Fink J, Doninger NA. Prevalence of neurocognitive dysfunction and other clinical manifestations in disabled patients with systemic lupus erythematosus. J Rheumatol. 2006;33(3):531–38.PubMedGoogle Scholar
  88. 88.
    Panopalis P, Julian L, Yazdany J, et al. Impact of memory impairment on employment status in persons with systemic lupus erythematosus. Arthritis Rheum. 2007;57(8):1453–60.PubMedCrossRefGoogle Scholar
  89. 89.
    Kozora E, West SG, Forrest S, et al. Attention and depression in systemic lupus erythematosus. 59th Annual Meeting of American Psychosomatic Society: 2001 March 7–10 2001.Google Scholar
  90. 90.
    Geuskens GA, Hazes JMW, Barendregt PJ, et al. Work and sick leave among patients with early inflammatory joint conditions. Arthritis Rheum. 2008;59(10):1458–66.PubMedCrossRefGoogle Scholar
  91. 91.
    Katz P, Morris A, Yelin E. Subclinical disability in valued life activities among individuals with rheumatoid arthritis. Arthritis Rheum. 2008;59(10):1416–23.PubMedCrossRefGoogle Scholar
  92. 92.
    Kozora E, Thompson LL, West SG, et al. Analysis of cognitive and psychological deficits in systemic lupus erythematosus patients without overt central nervous system disease. Arthritis Rheum. 1996;39(12): 2035–45.PubMedCrossRefGoogle Scholar
  93. 93.
    Harrison MJ, Morris KA, Horton R, et al. Results of intervention for lupus patients with self-perceived cognitive difficulties. Neurology. 2005;65(8):1325–27.PubMedCrossRefGoogle Scholar
  94. 94.
    Stroop J. Studies of interference in serial verbal reactions. J Exp Psychol. 1935;18:643–62.CrossRefGoogle Scholar
  95. 95.
    Delis D, Kramer J, Kaplan E, et al. California verbal learning test. 2nd ed. San Antonio, TX: Psychological Corporation; 2000.Google Scholar
  96. 96.
    Osterrieth P. Le test de copie d’une figure complex. Arch Psychol. 1944;30:286–356.Google Scholar
  97. 97.
    Wechsler D. Wechsler adult intelligence scale. 3rd ed. San Antonio, TX: Psychological Corporation; 1997.Google Scholar
  98. 98.
    Denburg S, Carbotte R, Ginsberg J, et al. The relationship of antiphospholipid antibodies to cognitive function in patients with systemic lupus erythematosus. J Int Neuropsychol. 1997;3:377–86.Google Scholar
  99. 99.
    McLaurin EY, Holliday SL, Williams P, et al. Predictors of cognitive dysfunction in patients with systemic lupus erythematosus. Neurology. 2005;64(2):297–303.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2010

Authors and Affiliations

  • Amy H. Kao
    • 1
  • Carol M. Greco
    • 2
  • Suzanne L. Gharib
    • 1
  • Sue R. Beers
    • 3
  1. 1.Division of Rheumatology and Clinical ImmunologyUniversity of Pittsburgh School of MedicinePittsburghUSA
  2. 2.University of Pittsburgh School of MedicinePittsburghUSA
  3. 3.Department of PsychiatryUniversity of Pittsburgh School of MedicinePittsburghUSA

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