Neurovascular Consequences of Systemic Disease – Collagen Vascular Disease

  • Stephen L. Holliday
  • Robin L. Brey


The neurovascular consequences of collagen vascular diseases are due in large part to two major causes: atherosclerosis and prothrombotic effects of antiphospholipid (aPL) antibodies. Patients with systemic lupus erythematosis (SLE) and rheumatoid arthritis (RA) can both develop premature atherosclerosis, and the study of patients with these disorders has been quite informative in understanding the relationship between inflammation, atherosclerosis, and cardio- and cerebrovascular disease outcomes (Manzi et al. 1997; Abou-Raya & Abou-Raya, 2006; Rhew & Ramsey-Goldman, 2006). In this chapter, we will discuss the evidence for the role of inflammation-induced atherosclerosis and aPL antibodies in neurovascular consequences of SLE, a prototypic collagen vascular disease.

Systemic lupus erythematosis is an autoimmune inflammatory disorder affecting multiple organ systems, which affects women nine times more frequently than men (Ward, 2004). The prevalence is approximately...


Systemic Lupus Erythematosis Systemic Lupus Erythematosis Patient Cognitive Dysfunction Lupus Anticoagulant Central Nervous System Manifestation 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


  1. Abou-Raya, A., & Abou-Raya, S. (2006). Inflammation: A pivotal link between autoimmune diseases and atherosclerosis. Autoimmunity Reviews, 5(5), 331–337.PubMedGoogle Scholar
  2. Abreu, M. R., Jakosky, A., Folgerini, M., Brenol, J. C., Xavier, R. M., & Kapczinsky, F. (2005). Neuropsychiatric systemic lupus erythematosus: Correlation of brain MR imaging, CT, and SPECT. Clinical Imaging, 29(3), 215–221.PubMedGoogle Scholar
  3. Afeltra, A., Garzia, P., Mitterhofer, A. P., Vadacca, M., Galluzzo, S., & Del Porto, F., et al. (2003). Neuropsychiatric lupus syndromes: Relationship with antiphospholipid antibodies. [see comment]. Neurology, 61(1), 108–110.PubMedGoogle Scholar
  4. Ainiala, H., Loukkola, J., Peltola, J., Korpela, M., & Hietaharju, A. (2001). The prevalence of neuropsychiatric syndromes in systemic lupus erythematosus. Neurology, 57(3), 496–500.PubMedGoogle Scholar
  5. Alcocer-Varela, J., Aleman-Hoey, D., & Alarcon-Segovia, D. (1992). Interleukin-1 and interleukin-6 activities are increased in the cerebrospinal fluid of patients with CNS lupus erythematosus and correlate with local late T-cell activation markers. Lupus, 1(2), 111–117.PubMedGoogle Scholar
  6. Allegri, F., Balestrieri, G., Cattaneo, R., Martinelli, M., Tincani, A., & Barcellini, W., et al. (1990). The plasma cofactor and anticardiolipin antibodies. Clinical & Experimental Rheumatology, 8(6), 613–615.Google Scholar
  7. Appenzeller S., Rondina J. M., Li L. M., Costallat, T. L., & Cendes F. (2005) Cerebral and corpus callosum atrophy in systemic lupus erythematosus. Arthritis & Rheumatism, 52(9), 2783–2789.Google Scholar
  8. The American College of Rheumatology nomenclature and case definitions for neuropsychiatric lupus syndromes (1999). Arthritis & Rheumatism, 42(4), 599–608.Google Scholar
  9. Baraczka, K., Pozsonyi, T., Szongoth, M., Nekam, K., Megyeri, A., Balogh, Z., et al. (1999). A study of increased levels of soluble vascular cell adhesion molecule-1 (sVCAM-1) in the cerebrospinal fluid of patients with multiple sclerosis and systemic lupus erythematosus. Acta Neurologica Scandinavica, 99(2), 95–99.PubMedGoogle Scholar
  10. Belmont, H. M., Abramson, S. B., & Lie, J. T. (1996). Pathology and pathogenesis of vascular injury in systemic lupus erythematosus. interactions of inflammatory cells and activated endothelium. Arthritis & Rheumatism, 39(1), 9–22.Google Scholar
  11. Bleiberg, J., Garmoe, W. S., Halpern, E. L., Reeves, D. L., & Nadler, J. D. (1997). Consistency of within-day and across-day performance after mild brain injury. Neuropsychiatry, Neuropsychology, & Behavioral Neurology, 10(4), 247–253.Google Scholar
  12. Bleiberg, J., Kane, R. L., Reeves, D. L., Garmoe, W. S., & Halpern, E. (2000). Factor analysis of computerized and traditional tests used in mild brain injury research. Clinical Neuropsychologist, 14(3), 287–294.PubMedGoogle Scholar
  13. Bleiberg, J., & Warden, D. (2005). Duration of cognitive impairment after sports concussion. Neurosurgery, 56(5), E1166.PubMedGoogle Scholar
  14. Blohorn, A., Guegan-Massardier, E., Triquenot, A., Onnient, Y., Tron, F., & Borg, J. Y., et al. (2002). Antiphospholipid antibodies in the acute phase of cerebral ischaemia in young adults: A descriptive study of 139 patients. Cerebrovascular Diseases, 13(3), 156–162.PubMedGoogle Scholar
  15. Brey, R. L. (2004). Management of the neurological manifestations of APS--what do the trials tell us? Thrombosis Research, 114(5–6), 489–499.PubMedGoogle Scholar
  16. Brey, R. L., Hart, R. G., Sherman, D. G., & Tegeler, C. H. (1990). Antiphospholipid antibodies and cerebral ischemia in young people. Neurology, 40(8), 1190–1196.PubMedGoogle Scholar
  17. Brey, R. L., Holliday, S. L., Saklad, A. R., Navarrete, M. G., Hermosillo-Romo, D., Stallworth, C. L., et al. (2002). Neuropsychiatric syndromes in lupus: Prevalence using standardized definitions. Neurology, 58(8), 1214–1220.PubMedGoogle Scholar
  18. Brey, R. L., Stallworth, C. L., McGlasson, D. L., Wozniak, M. A., Wityk, R. J., Stern, B. J., et al. (2002). Antiphospholipid antibodies and stroke in young women. Stroke, 33(10), 2396–2400.PubMedGoogle Scholar
  19. Campbell, A. L., Pierangeli, S. S., Wellhausen, S., & Harris, E. N. (1995). Comparison of the effects of anticardiolipin antibodies from patients with the antiphospholipid syndrome and with syphilis on platelet activation and aggregation. Thrombosis & Haemostasis, 73(3), 529–534.Google Scholar
  20. Cervera, R., Khamashta, M. A., Font, J., Sebastiani, G. D., Gil, A., & Lavilla, P., et al. (1999). Morbidity and mortality in systemic lupus erythematosus during a 5-year period. A multicenter prospective study of 1,000 patients. european working party on systemic lupus erythematosus. Medicine, 78(3), 167–175.PubMedGoogle Scholar
  21. Cervera, R., Khamashta, M. A., Font, J., Sebastiani, G. D., Gil, A., & Lavilla, P., et al. (2003). Morbidity and mortality in systemic lupus erythematosus during a 10-year period: A comparison of early and late manifestations in a cohort of 1,000 patients. Medicine, 82(5), 299–308.PubMedGoogle Scholar
  22. Cervera, R., Piette, J. C., Font, J., Khamashta, M. A., Shoenfeld, Y., & Camps, M. T., et al. (2002). Antiphospholipid syndrome: Clinical and immunologic manifestations and patterns of disease expression in a cohort of 1,000 patients. Arthritis & Rheumatism, 46(4), 1019–1027.Google Scholar
  23. 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(1), 36–46.Google Scholar
  24. Costallat, L., Bertolo, M., & Appenzeller, S. (2001). The american college of rheumatology nomenclature and case definitions for neuropsychiatric lupus syndromes: Analysis of 527 patients. Lupus, 10(S1), S32.Google Scholar
  25. Crowther, M. A., Ginsberg, J. S., Julian, J., Denburg, J., Hirsh, J., Douketis, J., et al. (2003). A comparison of two intensities of warfarin for the prevention of recurrent thrombosis in patients with the antiphospholipid antibody syndrome. New England Journal of Medicine, 349(12), 1133–1138.PubMedGoogle Scholar
  26. Csepany, T., Bereczki, D., Kollar, J., Sikula, J., Kiss, E., & Csiba, L. (2003). MRI findings in central nervous system systemic lupus erythematosus are associated with immunoserological parameters and hypertension. Journal of Neurology, 250(11), 1348–1354.PubMedGoogle Scholar
  27. Danchenko, N., Satia, J. A., & Anthony, M. S. (2006). Epidemiology of systemic lupus erythematosus: A comparison of worldwide disease burden. Lupus, 15(5), 308–318.PubMedGoogle Scholar
  28. DeGiorgio, L. A., Konstantinov, K. N., Lee, S. C., Hardin, J. A., Volpe, B. T., & Diamond, B. (2001). A subset of lupus anti-DNA antibodies cross-reacts with the NR2 glutamate receptor in systemic lupus erythematosus. Nature Medicine, 7(11), 1189–1193.PubMedGoogle Scholar
  29. del Zoppo, G. J., & Hallenbeck, J. M. (2000). Advances in the vascular pathophysiology of ischemic stroke. Thrombosis Research, 98(3), 73–81.PubMedGoogle Scholar
  30. Denburg, S. D., Carbotte, R. M., Ginsberg, J. S., & Denburg, J. A. (1997). The relationship of antiphospholipid antibodies to cognitive function in patients with systemic lupus erythematosus. Journal of the International Neuropsychological Society, 3(4), 377–386.PubMedGoogle Scholar
  31. Egerer, K., Feist, E., Rohr, U., Pruss, A., Burmester, G. R., & Dorner, T. (2000). Increased serum soluble CD14, ICAM-1 and E-selectin correlate with disease activity and prognosis in systemic lupus erythematosus. Lupus, 9(8), 614–621.PubMedGoogle Scholar
  32. Esdaile, J. M., Abrahamowicz, M., Grodzicky, T., Li, Y., Panaritis, C., du Berger, R., et al. (2001). Traditional framingham risk factors fail to fully account for accelerated atherosclerosis in systemic lupus erythematosus. Arthritis & Rheumatism, 44(10), 2331–2337.Google Scholar
  33. Futrell, N., Schultz, L. R., & Millikan, C. (1992). Central nervous system disease in patients with systemic lupus erythematosus. Neurology, 42(9), 1649–1657.PubMedGoogle Scholar
  34. Galli, M., Comfurius, P., Maassen, C., Hemker, H. C., de Baets, M. H., van Breda-Vriesman, P. J., et al. (1990). Anticardiolipin antibodies (ACA) directed not to cardiolipin but to a plasma protein cofactor. Lancet, 335(8705), 1544–1547.PubMedGoogle Scholar
  35. Gaynor, B., Putterman, C., Valadon, P., Spatz, L., Scharff, M. D., & Diamond, B. (1997). Peptide inhibition of glomerular deposition of an anti-DNA antibody. Proceedings of the National Academy of Sciences of the United States of America, 94(5), 1955–1960.PubMedGoogle Scholar
  36. Gharavi, A. E., & Pierangeli, S. S. (1998). Origin of antiphospholipid antibodies: Induction of aPL by viral peptides. Lupus, 7(Suppl 2), S52–S54.PubMedGoogle Scholar
  37. Gharavi, A. E., Pierangeli, S. S., Colden-Stanfield, M., Liu, X. W., Espinola, R. G., & Harris, E. N. (1999). GDKV-induced antiphospholipid antibodies enhance thrombosis and activate endothelial cells in vivo and in vitro. Journal of Immunology, 163(5), 2922–2927.Google Scholar
  38. Gharavi, E. E., Chaimovich, H., Cucurull, E., Celli, C. M., Tang, H., & Wilson, W. A., et al. (1999). Induction of antiphospholipid antibodies by immunization with synthetic viral and bacterial peptides. Lupus, 8(6), 449–455.PubMedGoogle Scholar
  39. Gonzalez-Crespo, M. R., Blanco, F. J., Ramos, A., Ciruelo, E., Mateo, I., Lopez Pino, M. A., et al. (1995). Magnetic resonance imaging of the brain in systemic lupus erythematosus. British Journal of Rheumatology, 34(11), 1055–1060.PubMedGoogle Scholar
  40. Greco, C. M., Rudy, T. E., & Manzi, S. (2004). Effects of a stress-reduction program on psychological function, pain, and physical function of systemic lupus erythematosus patients: A randomized controlled trial. Arthritis & Rheumatism, 51(4), 625–634.Google Scholar
  41. Haas, L. F. (1982). Stroke as an early manifestation of systemic lupus erythematosus. Journal of Neurology, Neurosurgery & Psychiatry, 45(6), 554–556.Google Scholar
  42. Hallenbeck, J. M., Hansson, G. K., & Becker, K. J. (2005). Immunology of ischemic vascular disease: Plaque to attack. Trends in Immunology, 26(10), 550–556.PubMedGoogle Scholar
  43. Hanly, J. G. (2001). Neuropsychiatric lupus. Current Rheumatology Reports, 3(3), 205–212.PubMedGoogle Scholar
  44. Hanly, J. G., Hong, C., Smith, S., & Fisk, J. D. (1999). A prospective analysis of cognitive function and anticardiolipin antibodies in systemic lupus erythematosus. Arthritis & Rheumatism, 42(4), 728–734.Google Scholar
  45. Hanly, J. G., Walsh, N. M., Fisk, J. D., Eastwood, B., Hong, C., Sherwood, G., et al. (1993). Cognitive impairment and autoantibodies in systemic lupus erythematosus. British Journal of Rheumatology, 32(4), 291–296.PubMedGoogle Scholar
  46. Hanly, J. G., Walsh, N. M., & Sangalang, V. (1992). Brain pathology in systemic lupus erythematosus. Journal of Rheumatology, 19(5), 732–741.PubMedGoogle Scholar
  47. Harrison, M., Ravdin, L., Volpe, B., Diamond, B., & Lockshin, M. (2004). Anti-NR2 antibody does not identify cognitive impairment in a general SLE population. Arthritis and Rheumatism, 50(9), S596.Google Scholar
  48. Ho, K. T., Ahn, C. W., Alarcon, G. S., Baethge, B. A., Tan, F. K., Roseman, J., et al. (2005). Systemic lupus erythematosus in a multiethnic cohort (LUMINA): XXVIII. factors predictive of thrombotic events. Rheumatology, 44(10), 1303–1307.PubMedGoogle Scholar
  49. Holliday, S. L., Navarrete, M. G., Hermosillo-Romo, D., Valdez, C. R., Saklad, A. R., Escalante, A., et al. (2003). Validating a computerized neuropsychological test battery for mixed ethnic lupus patients. Lupus, 12(9), 697–703.PubMedGoogle Scholar
  50. Hughes, G. (1983). Thrombosis, abortion, cerebral disease and lupus anticoagulant. British Medical Journal, 187, 1088–1089.Google Scholar
  51. Jara, L. J., Irigoyen, L., Ortiz, M. J., Zazueta, B., Bravo, G., & Espinoza, L. R. (1998). Prolactin and interleukin-6 in neuropsychiatric lupus erythematosus. Clinical Rheumatology, 17(2), 110–114.PubMedGoogle Scholar
  52. Karassa, F. B., Ioannidis, J. P., Boki, K. A., Touloumi, G., Argyropoulou, M. I., Strigaris, K. A., et al. (2000). Predictors of clinical outcome and radiologic progression in patients with neuropsychiatric manifestations of systemic lupus erythematosus. American Journal of Medicine, 109(8), 628–634.PubMedGoogle Scholar
  53. Kelley, V. R., & Wuthrich, R. P. (1999). Cytokines in the pathogenesis of systemic lupus erythematosus. Seminars in Nephrology, 19(1), 57–66.PubMedGoogle Scholar
  54. Khamashta, M. A., Cuadrado, M. J., Mujic, F., Taub, N. A., Hunt, B. J., & Hughes, G. R. (1995). The management of thrombosis in the antiphospholipid-antibody syndrome. New England Journal of Medicine, 332(15), 993–997.PubMedGoogle Scholar
  55. Komatsu, N., Kodama, K., Yamanouchi, N., Okada, S., Noda, S., Nawata, Y., et al. (1999). Decreased regional cerebral metabolic rate for glucose in systemic lupus erythematosus patients with psychiatric symptoms. European Neurology, 42(1), 41–48.PubMedGoogle Scholar
  56. Kovacs, J. A., Urowitz, M. B., & Gladman, D. D. (1993). Dilemmas in neuropsychiatric lupus. Rheumatic Diseases Clinics of North America, 19(4), 795–814.PubMedGoogle Scholar
  57. Kowal, C., DeGiorgio, L. A., Nakaoka, T., Hetherington, H., Huerta, P. T., Diamond, B., et al. (2004). Cognition and immunity; antibody impairs memory. Immunity, 21(2), 179–188.PubMedGoogle Scholar
  58. Kozora, E., Laudenslager, M., Lemieux, A., & West, S. (2001). Inflammatory and hormonal measures predict neuropsychological functioning in systemic lupus erythematosus and rheumatoid arthritis patients. Journal of the International Neuropsychological Society, 7(6), 745–754.PubMedGoogle Scholar
  59. Kozora E., Ellison MC., & West S. (2004). Reliability and validity of the proposed American College of Rheumatology neuropsychological battery for systemic lupus erythematosus. Arthritis & Rheumatism, 51(5), 810–818.Google Scholar
  60. Kozora E., Arciniegas D. B., Filley, C. M., Ellison M. C., West S. G., Brown M. S. & Simon J. H. (2005). Cognition, MRS neurometabolites, and MRI volymetrics in non-neuropsychiatric systemic lupus erythematosis: preliminary data. Cognitive and Behavioral Neurology, 18, 159–162.PubMedGoogle Scholar
  61. Lanthier, S., Kirkham, F. J., Mitchell, L. G., Laxer, R. M., Atenafu, E., Male, C., et al. (2004). Increased anticardiolipin antibody IgG titers do not predict recurrent stroke or TIA in children. Neurology, 62(2), 194–200.PubMedGoogle Scholar
  62. Leritz, E., Brandt, J., Minor, M., Reis-Jensen, F., & Petri, M. (2002). Neuropsychological functioning and its relationship to antiphospholipid antibodies in patients with systemic lupus erythematosus. Journal of Clinical & Experimental Neuropsychology: Official Journal of the International Neuropsychological Society, 24(4), 527–533.Google Scholar
  63. Levine, S. R., Brey, R. L., Tilley, B. C., Thompson, J. L., Sacco, R. L., Sciacca, R. R., et al. (2004). Antiphospholipid antibodies and subsequent thrombo-occlusive events in patients with ischemic stroke. JAMA, 291(5), 576–584.PubMedGoogle Scholar
  64. Libby, P. (2001). Managing the risk of atherosclerosis: The role of high-density lipoprotein. American Journal of Cardiology, 88(12A), 3 N–8 N.Google Scholar
  65. Maier, S. F., Goehler, L. E., Fleshner, M., & Watkins, L. R. (1998). The role of the vagus nerve in cytokine-to-brain communication. Annals of the New York Academy of Sciences, 840, 289–300.PubMedGoogle Scholar
  66. 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(5), 408–415.Google Scholar
  67. Matsuda, J., Gohchi, K., Gotoh, M., Tsukamoto, M., & Saitoh, N. (1994). Circulating intercellular adhesion molecule-1 and soluble interleukin 2-receptor in patients with systemic lupus erythematosus. European Journal of Haematology, 52(5), 302–303.PubMedGoogle Scholar
  68. Matsuura, E., Igarashi, Y., Fujimoto, M., Ichikawa, K., & Koike, T. (1990). Anticardiolipin cofactor(s) and differential diagnosis of autoimmune disease. Lancet, 336(8708), 177–178.PubMedGoogle Scholar
  69. McGrath, H., Jr. (2005). Elimination of anticardiolipin antibodies and cessation of cognitive decline in a UV-A1-irradiated sustemic lupus erythematosis patient. Lupus, 14 (10), 859–861.PubMedGoogle Scholar
  70. McLaurin, E. Y., Holliday, S. L., Williams, P., & Brey, R. L. (2005). Predictors of cognitive dysfunction in patients with systemic lupus erythematosus. Neurology, 64(2), 297–303.PubMedGoogle Scholar
  71. Menon, S., Jameson-Shortall, E., Newman, S. P., Hall-Craggs, M. R., Chinn, R., & Isenberg, D. A. (1999). A longitudinal study of anticardiolipin antibody levels and cognitive functioning in systemic lupus erythematosus. Arthritis & Rheumatism, 42(4), 735–741.Google Scholar
  72. Meroni, P. L., Del Papa, N., Raschi, E., Panzeri, P., Borghi, M. O., Tincani, A., et al. (1998). Beta2-glycoprotein I as a 'cofactor' for anti-phospholipid reactivity with endothelial cells. Lupus, 7(Suppl 2), S44–S47.PubMedGoogle Scholar
  73. Mikdashi, J., & Handwerger, B. (2004). Predictors of neuropsychiatric damage in systemic lupus erythematosus: Data from the maryland lupus cohort. Rheumatology, 43(12), 1555–1560.PubMedGoogle Scholar
  74. Miyakis, S., Giannakopoulos, B., & Krilis, S. A. (2004). Beta 2 glycoprotein I--function in health and disease. Thrombosis Research, 114(5–6), 335–346.PubMedGoogle Scholar
  75. Miyakis, S., Lockshin, M. D., Atsumi, T., Branch, D. W., Brey, R. L., & Cervera, R., et al. (2006). International consensus statement on an update of the classification criteria for definite antiphospholipid syndrome (APS). Journal of Thrombosis & Haemostasis, 4(2), 295–306.Google Scholar
  76. 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(4), 766–771.PubMedGoogle Scholar
  77. Morris, R. G., Anderson, E., Lynch, G. S., & Baudry, M. (1986). Selective impairment of learning and blockade of long-term potentiation by an N-methyl-d-aspartate receptor antagonist, AP5. Nature, 319(6056), 774–776.PubMedGoogle Scholar
  78. Navarrete, G., & Brey, R. (2000). Neuropsychiatric systemic lupus erythematosus. Current Treatment Options in Neurology, 2(5), 473–485.PubMedGoogle Scholar
  79. Nencini, P., Baruffi, M. C., Abbate, R., Massai, G., Amaducci, L., & Inzitari, D. (1992). Lupus anticoagulant and anticardiolipin antibodies in young adults with cerebral ischemia. Stroke, 23(2), 189–193.PubMedGoogle Scholar
  80. Omdal, R., Brokstad, K., Waterloo, K., Koldingsnes, W., Jonsson, R., & Mellgren, S. I. (2005). Neuropsychiatric disturbances in SLE are associated with antibodies against NMDA receptors. European Journal of Neurology, 12(5), 392–398.PubMedGoogle Scholar
  81. Otte, A., Weiner, S. M., Peter, H. H., Mueller-Brand, 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(7), 787–791.PubMedGoogle Scholar
  82. Ozawa, S., Kamiya, H., & Tsuzuki, K. (1998). Glutamate receptors in the mammalian central nervous system. Progress in Neurobiology, 54, 581–618.PubMedGoogle Scholar
  83. Pierangeli, S. S., & Harris, E. N. (1994). Antiphospholipid antibodies in an in vivo thrombosis model in mice. Lupus, 3(4), 247–251.PubMedGoogle Scholar
  84. Provenzale, J. M., Heinz, E. R., Ortel, T. L., Macik, B. G., Charles, L. A., & Alberts, M. J. (1994). Antiphospholipid antibodies in patients without systemic lupus erythematosus: Neuroradiologic findings. Radiology, 192(2), 531–537.PubMedGoogle Scholar
  85. Reeves, D., Kane, R., & Winter, K. (1996). Automated neuropsychological assessment metrics (ANAM V3.11a/96) user's manual: Clinical and neurotoxicology subset (report no. NCRF-SR-96-01). San Diego CA: National Cognitive Foundation.Google Scholar
  86. Reeves, D., Vleiberg, J., Roebuck-Spencer, T., Cernich, A., Schwab, K., Ivins, B., Salazar, A., Harvey, S., Brown, F, Warden, D. (2006). Reference values for performance on the Automated Neuropsychological Assessment Metrics V3.0 in an active duty military sample. Military Medicine, 171(10), 982–984.PubMedGoogle Scholar
  87. Rhew, E. Y., & Ramsey-Goldman, R. (2006). Premature atherosclerotic disease in systemic lupus erythematosus--role of inflammatory mechanisms. Autoimmunity Reviews, 5(2), 101–105.PubMedGoogle Scholar
  88. Rivest, C., Lew, R. A., Welsing, P. M., Sangha, O., Wright, E. A., Roberts, W. N., et al. (2000). Association between clinical factors, socioeconomic status, and organ damage in recent onset systemic lupus erythematosus. Journal of Rheumatology, 27(3), 680–684.PubMedGoogle Scholar
  89. Roebuck-Spencer, T. M., Yarboro, C., Nowak, M., Takada, K., Jacobs, G., Lapteva, L., et al. (2006). Use of computerized assessment to predict neuropsychological functioning and emotional distress in patients with systemic lupus erythematosus. Arthritis & Rheumatism, 55(3), 434–441.Google Scholar
  90. 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(25), 2399–2406.PubMedGoogle Scholar
  91. Rosove, M. H., & Brewer, P. M. (1992). Antiphospholipid thrombosis: Clinical course after the first thrombotic event in 70 patients. Annals of Internal Medicine, 117(4), 303–308.PubMedGoogle Scholar
  92. Sailer, M., Burchert, W., Ehrenheim, C., Smid, H. G., Haas, J., Wildhagen, K., et al. (1997). Positron emission tomography and magnetic resonance imaging for cerebral involvement in patients with systemic lupus erythematosus. Journal of Neurology, 244(3), 186–193.PubMedGoogle Scholar
  93. Schmidt, R., Auer-Grumbach, P., Fazekas, F., Offenbacher, H., & Kapeller, P. (1995). Anticardiolipin antibodies in normal subjects. neuropsychological correlates and MRI findings. Stroke, 26(5), 749–754.PubMedGoogle Scholar
  94. Sfikakis, P. P., Charalambopoulos, D., Vayiopoulos, G., Oglesby, R., Sfikakis, P., & Tsokos, G. C. (1994). Increased levels of intercellular adhesion molecule-1 in the serum of patients with systemic lupus erythematosus. Clinical & Experimental Rheumatology, 12(1), 5–9.Google Scholar
  95. Shovman, O., Gilburd, B., & Shoenfeld, Y. (2006). The role of inflammatory cytokines in the pathogenesis of systemic lupus erythematosus-related atherosclerosis: A novel target for treatment? Journal of Rheumatology, 33(3), 445–447.PubMedGoogle Scholar
  96. Sibbitt, W. L.,Jr, Sibbitt, R. R., & Brooks, W. M. (1999). Neuroimaging in neuropsychiatric systemic lupus erythematosus. Arthritis & Rheumatism, 42(10), 2026–2038.Google Scholar
  97. Singh, K., Gaiha, M., Shome, D. K., Gupta, V. K., & Anuradha, S. (2001). The association of antiphospholipid antibodies with ischaemic stroke and myocardial infarction in young and their correlation: A preliminary study. Journal of the Association of Physicians of India, 49, 527–529.PubMedGoogle Scholar
  98. Spronk, P. E., Bootsma, H., Huitema, M. G., Limburg, P. C., & Kallenberg, C. G. (1994). Levels of soluble VCAM-1, soluble ICAM-1, and soluble E-selectin during disease exacerbations in patients with systemic lupus erythematosus (SLE); a long term prospective study. Clinical & Experimental Immunology, 97(3), 439–444.Google Scholar
  99. Strater, R., Becker, S., von Eckardstein, A., Heinecke, A., Gutsche, S., Junker, R., et al. (2002). Prospective assessment of risk factors for recurrent stroke during childhood – a 5-year follow-up study. Lancet, 360(9345), 1540–1545.PubMedGoogle Scholar
  100. Stoll, G., & Bendszus, M. (2006). Inflammation and atherosclerosis: Novel insights into plaque formation and destabilization. Stroke, 37(7), 1923–1932.PubMedGoogle Scholar
  101. Sun, S. S., Liu, F. Y., Tsai, J. J., Yen, R. F., Kao, C. H., & Huang, W. S. (2003). Using 99mTc HMPAO brain SPECT to evaluate the effects of anticoagulant therapy on regional cerebral blood flow in primary antiphospholipid antibody syndrome patients with brain involvement-a preliminary report. Rheumatology International, 23(6), 301–304.PubMedGoogle Scholar
  102. Tietjen, G. E., Day, M., Norris, L., Aurora, S., Halvorsen, A., Schultz, L. R., et al. (1998). Role of anticardiolipin antibodies in young persons with migraine and transient focal neurologic events: A prospective study. Neurology, 50(5), 1433–1440.PubMedGoogle Scholar
  103. Toschi, V., Motta, A., Castelli, C., Paracchini, M. L., Zerbi, D., & Gibelli, A. (1998). High prevalence of antiphosphatidylinositol antibodies in young patients with cerebral ischemia of undetermined cause. Stroke, 29(9), 1759–1764.PubMedGoogle Scholar
  104. Toubi, E., Khamashta, M. A., Panarra, A., & Hughes, G. R. (1995). Association of antiphospholipid antibodies with central nervous system disease in systemic lupus erythematosus. American Journal of Medicine, 99(4), 397–401.PubMedGoogle Scholar
  105. Urowitz, M. B., Bookman, A. A., Koehler, B. E., Gordon, D. A., Smythe, H. A., & Ogryzlo, M. A. (1976). The bimodal mortality pattern of systemic lupus erythematosus. American Journal of Medicine, 60(2), 221–225.PubMedGoogle Scholar
  106. van Goor, M. P., Alblas, C. L., Leebeek, F. W., Koudstaal, P. J., & Dippel, D. W. (2004). Do antiphospholipid antibodies increase the long-term risk of thrombotic complications in young patients with a recent TIA or ischemic stroke? Acta Neurologica Scandinavica, 109(6), 410–415.PubMedGoogle Scholar
  107. Ward, M. M. (1999). Premature morbidity from cardiovascular and cerebrovascular diseases in women with systemic lupus erythematosus. Arthritis & Rheumatism, 42(2), 338–346.Google Scholar
  108. Ward, M. M. (2004). Prevalence of physician-diagnosed systemic lupus erythematosus in the united states. J Women’s Health, 13(6), 713–718.Google Scholar
  109. Weiner, S. M., Otte, A., Schumacher, M., Klein, R., Gutfleisch, J., Brink, I., et al. (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(5), 377–385.PubMedGoogle Scholar
  110. West, S. G., Emlen, W., Wener, M. H., & Kotzin, B. L. (1995). Neuropsychiatric lupus erythematosus: A 10-year prospective study on the value of diagnostic tests. American Journal of Medicine, 99(2), 153–163.PubMedGoogle Scholar
  111. Wu, J. T., & Wu, L. L. (2006). Linking inflammation and atherogenesis: Soluble markers identified for the detection of risk factors and for early risk assessment. Clinica Chimica Acta, 366(1–2), 74–80.Google Scholar
  112. Zaccagni, H., Fried, J., Cornell, J., Padilla, P., & Brey, R. L. (2004). Soluble adhesion molecule levels, neuropsychiatric lupus and lupus-related damage. Frontiers in Bioscience, 9, 1654–1659.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2009

Authors and Affiliations

  1. 1.University of Texas Health Science CenterSan AntonioUSA
  2. 2.Department of Medicine/NeurologyUniversity of Texas Health Science Center at San AntonioSan AntonioUSA

Personalised recommendations