Neuropsychiatric systemic lupus erythematosus: Tools for the diagnosis

Autoimmunity Reviews

Volumn 13, Issue 8, 2014, Pages 831-839

  Zardi, Enrico Maria ^a   Taccone, Arianna ^a   Marigliano, Benedetta ^a   Margiotta, Domenico P E ^a   Afeltra, Antonella ^a  

^a UNIVERSITY CAMPUS BIO MEDICO   (Italy)

Author keywords

MRI; Neuropsychiatric SLE; SPECT

Indexed keywords

FLUORODEOXYGLUCOSE F 18;

CEREBROSPINAL FLUID ANALYSIS; COGNITION; CYTOKINE PRODUCTION; DIFFUSION WEIGHTED IMAGING; DOPPLER ECHOGRAPHY; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; MENTAL DISEASE; NEUROIMAGING; NEUROPSYCHIATRIC SYSTEMIC LUPUS ERYTHEMATOSUS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; REVIEW; SINGLE PHOTON EMISSION COMPUTER TOMOGRAPHY; SYSTEMIC LUPUS ERYTHEMATOSUS;

MRI; NEUROPSYCHIATRIC-SLE; SPECT;

ANIMALS; COLOR; HUMANS; LUPUS VASCULITIS, CENTRAL NERVOUS SYSTEM; MAGNETIC RESONANCE IMAGING; TOMOGRAPHY, EMISSION-COMPUTED, SINGLE-PHOTON; ULTRASONOGRAPHY, DOPPLER, TRANSCRANIAL;

EID: 84902180289     PISSN: 15689972     EISSN: 18730183     Source Type: Journal    
DOI: 10.1016/j.autrev.2014.04.002     Document Type: Review

References (155)

1. Bernatsky S., Clarke A., Gladman D.D., Urowitz M., Fortin P.R., Barr S.G., et al. Mortality related to cerebrovascular disease in systemic lupus erythematosus. Lupus 2006, 15:835-839.
2. McNicholl J.M., Glynn D., Mongey A.B.., Hutchinson M., Bresnihan B. A prospective study of neurophysiologic, neurologic and immunologic abnormalities in systemic lupus erythematosus. J Rheumatol 1994, 21:1061-1066.
3. The American College of Rheumatology nomenclature and case definitions for neuropsychiatric lupus syndromes. Arthritis Rheum 1999, 42:599-608.
4. Stojanovich L., Zandman-Goddard G., Pavlovich S., Sikanich N. Psychiatric manifestations in systemic lupus erythematosus. Autoimmun Rev 2007, 6:421-426.
5. Borchers A.T., Aoki C.A., Naguwa S.M., Keen C.L., Shoenfeld Y., Gershwin M.E. Neuropsychiatric features of systemic lupus erythematosus. Autoimmun Rev 2005, 4:329-344.
6. Castellino G., Govoni M., Giacuzzo S., Trotta F. Optimizing clinical monitoring of central nervous system involvement in SLE. Autoimmun Rev 2008, 7:297-304.
7. Shoenfeld Y., Alarcon-Segovia D., Buskila D., Abu-Shakra M., Lorber M., Sherer Y., et al. Frontiers of SLE: review of the 5th International Congress of Systemic Lupus Erythematosus, Cancun, Mexico, April 20-25, 1998. Semin Arthritis Rheum 1999, 29:112-130.
8. Greenwood D.L., Gitlits V.M., Alderuccio F., Sentry J.W., Toh B.H. Autoantibodies in neuropsychiatric lupus. Autoimmunity 2002, 35:79-86.
9. Borowoy A.M., Pope J.E., Silverman E., Fortin P.R., Pineau C., Smith C.D., et al. Neuropsychiatric lupus: the prevalence and autoantibody associations depend on the definition: results from the 1000 faces of lupus cohort. Semin Arthritis Rheum 2012, 42:179-185.
10. Goddard G.Z., Chapman J., Shoenfeld Y. Autoantibodies involved in neuropsychiatric SLE and antiphospholipid syndrome. Semin Arthritis Rheum 2007, 36:297-315.
11. Kimura A., Kanoh Y., Sakurai T., Koumura A., Yamada M., Hayashi Y., et al. Antibodies in patients with neuropsychiatric systemic lupus erythematosus. Neurology 2010, 74:1372-1379.
12. Gerli R., Caponi L., Tincani A., Scorza R., Sabbadini M.G., Danieli M.G., et al. Clinical and serological associations of ribosomal P autoAbs in systemic lupus erythematosus: prospective evaluation in a large cohort of Italian patients. Rheumatology (Oxford) 2002, 41:1357-1366.
13. Efthimiou P., Blanco M. Pathogenesis of neuropsychiatric systemic lupus erythematosus and potential biomarkers. Mod Rheumatol 2009, 19:457-468.
14. Hanly J.G., Urowitz M.B., Su L., Bae S.C., Gordon C., Clarke A., et al. Autoantibodies as biomarkers for the prediction of neuropsychiatric events in systemic lupus erythematosus. Ann Rheum Dis 2011, 70:1726-1732.
15. Barros S., de Carvalho J. Pathological gambling and primary antiphospholipid (Hughes) syndrome: a unique neuropsychiatric association. Lupus 2011, 20:1086-1089.
16. Zardi E.M., Zardi D.M., Lazarevic Z., Santucci S., D'Errico F., Carbone A., et al. Transient global amnesia as the first symptom of primary antiphospholipid syndrome: a case report. Int J Immunopathol Pharmacol 2012, 25:275-280.
17. Govoni M., Bombardieri S., Bortoluzzi A., Caniatti L., Casu C., Conti F., et al. Italian Society of Rheumatology. Factors and comorbidities associated with first neuropsychiatric event in systemic lupus erythematosus: does a risk profile exist? A large multicentre retrospective cross-sectional study on 959 Italian patients. Rheumatology (Oxford) 2012, 51:157-168.
18. Hanly J.G., Hong C., Smith S., Fisk J.D. A prospective analysis of cognitive function and anticardiolipin antibodies in systemic lupus erythematosus. Arthritis Rheum 1999, 42:728-734.
19. Menon S., Jameson-Shortall E., Newman S.P., Hall-Craggs M.R., Chinn R., Isenberg D.A. A longitudinal study of anticardiolipin antibody levels and cognitive functioning in systemic lupus erythematosus. Arthritis Rheum 1999, 42(4):735-741.
20. Afeltra A., Garzia P., Mitterhofer A.P., Vadacca M., Galluzzo S., Del Porto F., et al. Neuropsychiatric lupus syndromes: relationship with antiphospholipid antibodies. Neurology 2003, 61:108-110.
21. Steens S.C., Bosma G.P., Steup-Beekman G.M., le Cessie S., Huizinga T.W., van Buchem M.A. Association between microscopic brain damage as indicated by magnetization transfer imaging and anticardiolipin antibodies in neuropsychiatric lupus. Arthritis Res Ther 2006, 8:R38.
22. Katzav A., Shoenfeld Y., Chapman J. The pathogenesis of neural injury in animal models of the antiphospholipid syndrome. Clin Rev Allergy Immunol 2010, 38:196-200.
23. DeGiorgio L.A., Konstantinov K.N., Lee S.C., Hardin J.A., Volpe B.T., Diamond B. A subset of lupus anti-DNA antibodies cross-reacts with the NR2 glutamate receptor in systemic lupus erythematosus. Nat Med 2001, 7:1189-1193.
24. Jenks S.A., Sanz I. Altered B cell receptor signaling in human systemic lupus erythematosus. Autoimmun Rev 2009, 8:209-213.
25. Pisetsky D.S., Ullal A.J. The blood nucleome in the pathogenesis of SLE. Autoimmun Rev 2010, 10:35-37.
26. Cagnoli P.C., Sundgren P.C., Kairys A., Graft C.C., Clauw D.J., Gebarski S., et al. Changes in regional brain morphology in neuropsychiatric systemic lupus erythematosus. J Rheumatol 2012, 39:959-967.
27. Postal M., Costallat L.T., Appenzeller S. Neuropsychiatric manifestations in systemic lupus erythematosus: epidemiology, pathophysiology and management. CNS Drugs 2011, 25:721-736.
28. Tatsukawa H., Ishii K., Haranaka M., Kumagi M., Hino I., Yoshimatsu H. Evaluation of average amount of cerebral blood flow measured by brain perfusion index in patients with neuropsychiatric systemic lupus erythematosus. Lupus 2005, 14:445-449.
29. Hanly J.G., Walsh N.M., Sangalang V. Brain pathology in systemic lupus erythematosus. J Rheumatol 1992, 19:732-741.
30. Luyendijk J., Steens S.C., Ouwendijk W.J., Steup-Beekman G.M., Bollen E.L., van der Grond J., et al. Neuropsychiatric systemic lupus erythematosus: lessons learned from magnetic resonance imaging. Arthritis Rheum 2011, 63:722-732.
31. Brooks W.M., Sibbitt W.L., Kornfeld M., Jung R.E., Bankhurst A.D., Roldan C.A. The histopathologic associates of neurometabolite abnormalities in fatal neuropsychiatric systemic lupus erythematosus. Arthritis Rheum 2010, 62:2055-2063.
32. Bertsias G.K., Ioannidis J.P.A., Aringer M., Bollen E., Bombardieri S., Bruce I.N., et al. EULAR recommendations for the management of systemic lupus erythematosus with neuropsychiatric manifestation: report of a task force of the EULAR standing committee for clinical affairs. Ann Rheum Dis 2010, 69:2074-2082.
33. Monov S., Monova D. Classification criteria for neuropsychiatric systemic lupus erythematosus: do they need a discussion?. Hippokratia 2008, 12:103-107.
34. Jennekens F.G., Kater L. The central nervous system in systemic lupus erythematosus. Part 1. Clinical syndromes: a literature investigation. Rheumatology (Oxford) 2002, 41:605-618.
35. Karassa F.B., Afeltra A., Ambrozic A., Chang D.M., De Keyser F., Doria A., et al. Accuracy of anti-ribosomal P protein antibody testing for the diagnosis of neuropsychiatric systemic lupus erythematosus: an international meta-analysis. Arthritis Rheum 2006, 54:312-324.
36. Mitsikostas D.D., Sfikakis P.P., Goadsby P.J. A meta-analysis for headache in systemic lupus erythematosus: the evidence and the myth. Brain 2004, 127:1200-1209.
37. Sanna G., Piga M., Terryberry J.W., Peltz M.T., Giagheddu S., Satta L., et al. Central nervous system involvement in systemic lupus erythematosus: cerebral imaging and serological profile in patients with and without overt neuropsychiatric manifestations. Lupus 2000, 9:573-583.
38. Brey R.L., Holliday S.L., Saklad A.R., Navarrete M.G., Hermosillo-Romo D., Stallworth C.L., et al. Neuropsychiatric syndromes in lupus: prevalence using standardized definitions. Neurology 2002, 58:1214-1220.
39. Tan E.M., Cohen A.S., Fries J.F., Masi A.T., McShane D.J., Rothfield N.F., et al. The 1982 revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum 1982, 25:1271-1277.
40. Hochberg M.C. Updating the American College of Rheumatology revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum 1997, 40:1725.
41. Petri M., Orbai A.M., Alarcón G.S., Gordon C., Merrill J.T., Fortin P.R., et al. Derivation and validation of the Systemic Lupus International Collaborating Clinics classification criteria for systemic lupus erythematosus. Arthritis Rheum 2012, 64:2677-2686.
42. Rood M.J., Breedveld F.C., Huizinga T.W. The accuracy of diagnosing neuropsychiatric systemic lupus erythematosus in a series of 49 hospitalized patients. Clin Exp Rheumatol 1999, 17:55-61.
43. Emmer B.J., Steup-Beekman G.M., Steens S.C., Huizinga T.W., van Buchem M.A., van der Grond J. Correlation of magnetization transfer ratio histogram parameters with neuropsychiatric systemic lupus erythematosus criteria and proton magnetic resonance spectroscopy: association of magnetization transfer ratio peak height with neuronal and cognitive dysfunction. Arthritis Rheum 2008, 58:1451-1457.
44. Emmer B.J., Steens S.C., Steup-Beekman G.M., van der Grond J., Admiraal-Behloul F., Olofsen H., et al. Detection of change in CNS involvement in neuropsychiatric SLE: a magnetization transfer study. J Magn Reson Imaging 2006, 24:812-816.
45. Kitagawa Y., Gotoh F., Koto A., Okayasu H. Stroke in systemic lupus erythematosus. Stroke 1990, 21:1533-1539.
46. Huizinga T.W., Steens S.C., van Buchem M.A. Imaging modalities in central nervous system systemic lupus erythematosus. Curr Opin Rheumatol 2001, 13:383-388.
47. Govoni M., Castellino G., Padovan M., Borrelli M., Trotta F. Recent advances and future perspective in neuroimaging in neuropsychiatric systemic lupus erythematosus. Lupus 2004, 13:149-158.
48. Hanly J.G., Harrison M.J. Management of neuropsychiatric lupus. Best Pract Res Clin Rheumatol 2005, 19:799-821.
49. Sibbitt W.L., Sibbitt R.R., Brooks W.M. Neuroimaging in neuropsychiatric systemic lupus erythematosus. Arthritis Rheum 1999, 42:2026-2038.
50. McCune W.J., MacGuire A., Aisen A., Gebarski S. Identification of brain lesions in neuropsychiatric systemic lupus erythematosus by magnetic resonance scanning. Arthritis Rheum 1988, 31:159-166.
51. Brooks W.M., Sabet A., Sibbitt W.L., Barker P.B., van Zijl P.C., Duyn J.H., et al. Neurochemistry of brain lesions determined by spectroscopic imaging in systemic lupus erythematosus. J Rheumatol 1997, 24:2323-2329.
52. Sundgren P.C., Jennings J., Attwood J.T., Nan B., Gebarski S., McCune W.J., et al. MRI and 2D-CSI MR spectroscopy of the brain in the evaluation of patients with acute onset of neuropsychiatric systemic lupus erythematosus. Neuroradiology 2005, 47:576-585.
53. Friedman S.D., Stidley C.A., Brooks W.M., Hart B.L., Sibbitt W.L. Brain injury and neurometabolic abnormalities in systemic lupus erythematosus. Radiology 1998, 209:79-84.
54. Sibbitt W.L., Haseler L.J., Griffey R.H., Hart B.L., Sibbitt R.R., Matwiyoff N.A. Analysis of cerebral structural changes in systemic lupus erythematosus by proton MR spectroscopy. AJNR Am J Neuroradiol 1994, 15:923-928.
55. Sabet A., Sibbitt W.L., Stidley C.A., Danska J., Brooks W.M. Neurometabolite markers of cerebral injury in the antiphospholipid antibody syndrome of systemic lupus erythematosus. Stroke 1998, 29:2254-2260.
56. Ishikawa O., Ohnishi K., Miyachi Y., Ishizaka H. Cerebral lesions in systemic lupus erythematosus detected by magnetic resonance imaging. Relationship to anticardiolipin antibody. J Rheumatol 1994, 21:87-90.
57. Jarek M.J., West S.G., Baker M.R., Rak K.M. Magnetic resonance imaging in systemic lupus erythematosus patients without a history of neuropsychiatric lupus erythematosus. Arthritis Rheum 1994, 37:1609-1613.
58. Sewell K.L., Livneh A., Aranow C.B., Grayzel A.I. Magnetic resonance imaging versus computed tomographic scanning in neuropsychiatric systemic lupus erythematosus. Am J Med 1989, 86:625-626.
59. Sibbitt W.L., Sibbitt R.R., Griffey R.H., Eckel C., Bankhurst A.D. Magnetic resonance and computed tomographic imaging in the evaluation of acute neuropsychiatric disease in systemic lupus erythematosus. Ann Rheum Dis 1989, 48:1014-1022.
60. Sibbitt W.L., Schmidt P.J., Hart B.L., Brooks W.M. Fluid attenuated Inversion Recovery (FLAIR) imaging in neuropsychiatric systemic lupus erythematosus. J Rheumatol 2003, 30:1983-1989.
61. Jennings J.E., Sundgren P.C., Attwood J., McCune J., Maly P. Value of MRI of the brain in patients with systemic lupus erythematosus and neurologic disturbance. Neuroradiology 2004, 46:15-21.
62. Monastero R., Bettini P., Del Zotto E., Cottini E., Tincani A., Balestrieri G., et al. Prevalence and pattern of cognitive impairment in systemic lupus erythematosus patients with and without overt neuropsychiatric manifestations. J Neurol Sci 2001, 184:33-39.
63. Provenzale J.M., Barboriak D.P., Allen N.B., Ortel T.L. Patients with antiphospholipid antibodies: CT and MR findings of the brain. AJR Am J Roentgenol 1996, 167:1573-1578.
64. Zirkzee E.J., Steup-Beekman G.M., van der Mast R.C., Bollen E.L., van der Wee N.J., Baptist E., et al. Prospective study of clinical phenotypes in neuropsychiatric systemic lupus erythematosus; multidisciplinary approach to diagnosis and therapy. J Rheumatol 2012, 39:2118-2126.
65. Karassa F.B., Ioannidis J.P., Boki K.A., Touloumi G., Argyropoulou M.I., Strigaris K.A., et al. Predictors of clinical outcome and radiologic progression in patients with neuropsychiatric manifestations of systemic lupus erythematosus. Am J Med 2000, 109:628-634.
66. Stimmler M.M., Coletti P.M., Quismorio F.P. Magnetic resonance imaging of the brain in neuropsychiatric systemic lupus erythematosus. Semin Arthritis Rheum 1993, 22:335-349.
67. Bell C.L., Partington C., Robbins M., Graziano F., Turski P., Kornguth S. Magnetic resonance imaging of central nervous system lesions in patients with lupus erythematosus. Correlation with clinical remission and antineurofilament and anticardiolipin antibody titers. Arthritis Rheum 1991, 34:432-441.
68. Sibbitt W.L., Brooks W.M., Kornfeld M., Hart B.L., Bankhurst A.D., Roldan C.A. Magnetic resonance imaging and brain histopathology in neuropsychiatric systemic lupus erythematosus. Semin Arthritis Rheum 2010, 40:32-52.
69. de Leeuw F.E., de Groot J.C., Oudkerk M., Witteman J.C., Hofman A., van Gijn J., et al. Hypertension and cerebral white matter lesions in a prospective cohort study. Brain 2002, 125:765-772.
70. Sanna G., D'Cruz D., Cuadrado M.J. Cerebral manifestations in the antiphospholipid (Hughes) syndrome. Rheum Dis Clin North Am 2006, 32:465-490.
71. Roldan C.A., Gelgand E.A., Qualls C.R., Sibbitt W.L. Valvular heart disease by transthoracic echocardiography is associated with focal brain injury and central neuropsychiatric systemic lupus erythematosus. Cardiology 2007, 108:331-337.
72. Kruit M.C., van Buchem M.A., Hofman P.A., Bakkers J.T., Terwindt G.M., Ferrari M.D., et al. Migraine as a risk factor for subclinical brain lesions. JAMA 2004, 291:427-434.
73. Sachdev P., Chen X., Wen W. White matter hyperintensities in mid-adult life. Curr Opin Psychiatry 2008, 21:268-274.
74. Brey R.L. Neuropsychiatric lupus: clinical and imaging aspects. Bull NYU Hosp Jt Dis 2007, 65:194-199.
75. Cuadrado M.J., Khamashta M.A., Ballesteros A., Godfrey T., Simon M.J., Hughes G.R. Can neurologic manifestations of Hughes (antiphospholipid) syndrome be distinguished from multiple sclerosis? Analysis of 27 patients and review of the literature. Medicine (Baltimore) 2000, 79:57-68.
76. Cotton F., Bouffard-Vercelli J., Hermier M., Tebib J., Vital Durand D., Tran Minh V.A., et al. MRI of central nervous system in a series of 58 systemic lupus erythematosus (SLE) patients with or without overt neuropsychiatric manifestations. Rev Med Interne 2004, 25:8-15.
77. Muscal E., Traipe E., de Guzman M.M., Myones B.L., Brey R.L., Hunter J.V. Cerebral and cerebellar volume loss in children and adolescents with systemic lupus erythematosus: a review of clinically acquired brain magnetic resonance imaging. J Rheumatol 2010, 37:1768-1775.
78. Amoroso A., Del Porto F., Garzia P., Mariotti A., Addessi M.A., Afeltra A. Primary antiphospholipid syndrome and cerebral atrophy: a rare association?. Am J Med Sci 1999, 317:425-428.
79. Appenzeller S., Li L.M., Costallat L.T., Cendes F. Evidence of reversible axonal dysfunction in systemic lupus erythematosus: a proton MRS study. Brain 2005, 128:2933-2940.
80. Axford J.S., Howe F.A., Heron C., Griffiths J.R. Sensitivity of quantitative (1)H magnetic resonance spectroscopy of the brain in detecting early neuronal damage in systemic lupus erythematosus. Ann Rheum Dis 2001, 60:106-111.
81. Bosma G.P., Steens S.C., Petropoulos H., Admiraal-Behloul F., van den Haak A., Doornbos J., et al. Multisequence magnetic resonance imaging study of neuropsychiatric systemic lupus erythematosus. Arthritis Rheum 2004, 50:3195-3202.
82. Steens S.C., Admiraal-Behloul F., Bosma G.P., Steup-Beekman G.M., Olofsen H., Le Cessie S., et al. Selective gray matter damage in neuropsychiatric lupus. Arthritis Rheum 2004, 50:2877-2881.
83. Castellino G., Padovan M., Bortoluzzi A., Borrelli M., Feggi L., Caniatti M.L., et al. Single photon emission computed tomography and magnetic resonance imaging evaluation in SLE patients with and without neuropsychiatric involvement. Rheumatology (Oxford) 2008, 47:319-323.
84. Zhang X., Zhu Z., Zhang F., Shu H., Li F., Dong Y. Diagnostic value of single-photon-emission computed tomography in severe central nervous system involvement of systemic lupus erythematosus: a case-control study. Arthritis Rheum 2005, 53:845-849.
85. Weiner S.M., Otte A., Schumacher M., Klein R., Gutfleisch J., Brink I., et al. Diagnosis and monitoring of central nervous system involvement in systemic lupus erythematosus: value of F-18 fluorodeoxyglucose PET. Ann Rheum Dis 2000, 59:377-385.
86. Popescu A., Kao A.H. Neuropsychiatric systemic lupus erythematosus. Curr Neuropharmacol 2011, 9:449-457.
87. DiFrancesco M.W., Holland S.K., Ris M.D., Adler C.M., Nelson S., DelBello M.P., et al. Functional magnetic resonance imaging assessment of cognitive function in childhood-onset systemic lupus erythematosus: a pilot study. Arthritis Rheum 2007, 56:4151-4163.
88. Rocca M.A., Agosta F., Mezzapesa D.M., Ciboddo G., Falini A., Comi G., et al. An fMRI study of the motor system in patients with neuropsychiatric systemic lupus erythematosus. Neuroimage 2006, 30:478-484.
89. Wolinsky J.S., Narayana P.A. Magnetic resonance spectroscopy in multiple sclerosis: window into the diseased brain. Curr Opin Neurol 2002, 15:247-251.
90. Petrella J.R., Townsend B.A., Jha A.P., Ziajko L.A., Slavin M.J., Lustig C., et al. Increasing memory load modulates regional brain activity in older adults as measured by fMRI. J Neuropsychiatry Clin Neurosci 2005, 17:75-83.
91. Fuller R.A., Westmoreland S.V., Ratai E., Greco J.B., Kim J.P., Lentz M.R., et al. A prospective longitudinal in?vivo 1H MR spectroscopy study of the SIV/macaque model of neuroAIDS. BMC Neurosci 2004, 5(5):10.
92. West S.G., Emlen W., Wener M.H., Kotzin B.L. Neuropsychiatric lupus erythematosus: a 10-year prospective study on the value of diagnostic tests. Am J Med 1995, 99:153-163.
93. Chinn R.J., Wilkinson I.D., Hall-Craggs M.A., Paley M.N., Shortall E., Carter S., et al. Magnetic resonance imaging of the brain and cerebral proton spectroscopy in patients with systemic lupus erythematosus. Arthritis Rheum 1997, 40:36-46.
94. Davie C.A., Feinstein A., Kartsounis L.D., Barker G.J., McHugh N.J., Walport M.J., et al. Proton magnetic resonance spectroscopy of systemic lupus erythematosus involving the central nervous system. J Neurol 1995, 242:522-528.
95. Colamussi P., Trotta F., Ricci R., Cittanti C., Govoni M., Barbarella G., et al. Brain perfusion SPET and proton magnetic resonance spectroscopy in the evaluation of two systemic lupus erythematosus patients with mild neuropsychiatric manifestations. Nucl Med Commun 1997, 18:269-273.
96. Sibbitt W.L., Sibbitt R.R. Magnetic resonance spectroscopy and positron emission tomography scanning in neuropsychiatric systemic lupus erythematosus. Rheum Dis Clin North Am 1993, 19:851-868.
97. Sibbitt W.L., Haseler L.J., Griffey R.R., Friedman S.D., Brooks W.M. Neurometabolism of active neuropsychiatric lupus determined with proton MR spectroscopy. AJNR Am J Neuroradiol 1997, 18:1271-1277.
98. Davie C.A., Hawkins C.P., Barker G.J., Brennan A., Tofts P.S., Miller D.H., et al. Serial proton magnetic resonance spectroscopy in acute multiple sclerosis lesions. Brain 1994, 117:49-58.
99. Brenner R.E., Munro P.M., Williams S.C., Bell J.D., Barker G.J., Hawkins C.P., et al. The proton NMR spectrum in acute EAE: the significance of the change in the Cho:Cr ratio. Magn Reson Med 1993, 29:737-745.
100. Häussinger D., Laubenberger J., vom Dahl S., Ernst T., Bayer S., Langer M., et al. Proton magnetic resonance spectroscopy studies on human brain myo-inositol in hypo-osmolarity and hepatic encephalopathy. Gastroenterology 1994, 107:1475-1480.
101. Videen J.S., Michaelis T., Pinto P., Ross B.D. Human cerebral osmolytes during chronic hyponatremia. A proton magnetic resonance spectroscopy study. J Clin Invest 1995, 95:788-793.
102. Kozora E., Filley C.M. Cognitive dysfunction and white matter abnormalities in systemic lupus erythematosus. J Int Neuropsychol Soc 2011, 22:1-8.
103. Balaban R.S., Ceckler T.L. Magnetization transfer contrast in magnetic resonance imaging. Magn Reson Q 1992, 8:116-137.
104. Le Bihan D. Molecular diffusion nuclear magnetic resonance imaging. Magn Reson Q 1991, 7:1-30.
105. Rovaris M., Filippi M. The value of new magnetic resonance techniques in multiple sclerosis. Curr Opin Neurol 2000, 13:249-254.
106. Otte A., Weiner S.M., Hoegerle S., Wolf R., Juengling F.D., Peter H.H., et al. Neuropsychiatric systemic lupus erythematosus before and after immunosuppressive treatment: a FDG PET study. Lupus 1998, 7:57-59.
107. Breitbach S.A., Alexander R.W., Daltroy L.H., Liang M.H., Boll T.J., Karlson E.W., et al. Determinants of cognitive performance in systemic lupus erythematosus. J Clin Exp Neuropsychol 1998, 20:157-166.
108. Denburg S.D., Denburg J.A. Cognitive dysfunction and antiphospholipid antibodies in systemic lupus erythematosus. Lupus 2003, 12:883-890.
109. Borrelli M., Tamarozzi R., Colamussi P., Govoni M., Trotta F., Lappi S. Evaluation with MR, perfusion MR and cerebral flowSPECT in NPSLE patients. Radiol Med 2003, 105:482-489.
110. Tatum W.O., Alavi A., Stecker M.M. Technetium-99m-HMPAO SPECT in partial status epilepticus. J Nucl Med 1994, 35:1087-1094.
111. Castellino G., Bortoluzzi A., Padovan M., Borrelli M., Feggi L., Govoni M. Repeated brain conventional MRI and SPECT evaluation in systemic lupus erythematosus patients with and without neuropsychiatric involvement: a follow up study. Lupus 2011, 20:1387-1395.
112. Giovacchini G., Mosca M., Manca G., Della Porta M., Neri C., Bombardieri S., et al. Cerebral blood flow in depressed patients with systemic lupus erythematosus. J Rheumatol 2010, 37(9):1844-1851.
113. Qiu J., Hu S.Y., Zuo X.X. Single photon emission computed tomography evaluation for severe neuropsychiatric systemic lupus erythematosus. Clin Exp Rheumatol 2013, 31:159.
114. Ishimori M.L., Pressman B.D., Wallace D.J., Weisman M.H. Posterior reversible encephalopathy syndrome: another manifestation of CNS SLE?. Lupus 2007, 16:436-443.
115. Fong K.Y., Thumboo J. Neuropsychiatric lupus: clinical challenges, brain-reactive autoantibodies and treatment strategies. Lupus 2010, 19:1399-1403.
116. Okamoto H., Kobayashi A., Yamanaka H. Cytokines and chemokines in neuropsychiatric syndromes of systemic lupus erythematosus. J Biomed Biotechnol 2010, 2010:268436.
117. Kao C.H., Ho Y.J., Lan J.L., Changlai S.P., Liao K.K., Chieng P.U. 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, 42:61-68.
118. Rennen H.J., Boerman O.C., Oyen W.J., Corstens F.H. Imaging infection/inflammation in the new millennium. Eur J Nucl Med 2001, 28:241-252.
119. Hamilton J.A., Tak P.P. The dynamics of macrophage lineage populations in inflammatory and autoimmune diseases. Arthritis Rheum 2009, 60:1210-1221.
120. Basu S., Kumar R., Alavi A. PET and PET-CT imaging in infection and inflammation: its critical role in assessing complications related to therapeutic interventions in patients with cancer. Indian J Cancer 2010, 47:371-379.
121. Lee S.W., Park M.C., Lee S.K., Park Y.B. The efficacy of brain (18)F-fluorodeoxyglucose positron emission tomography in neuropsychiatric lupus patients with normal brain magnetic resonance imaging findings. Lupus 2012, 21:1531-1537.
122. Stoppe G., Wildhagen K., Seidel J.W., Meyer G.J., Schober O., Heintz P., et al. Positron emission tomography in neuropsychiatric lupus erythematosus. Neurology 1990, 40:304-308.
123. Krakauer M., Law I. FDG PET brain imaging in neuropsychiatric systemic lupus erythematosus with choreic symptoms. Clin Nucl Med 2009, 34:122-123.
124. Levine S.R., Deegan M.J., Futrell N., Welch K.M. Cerebrovascular and neurologic disease associated with antiphospholipid antibodies: 48 cases. Neurology 1990, 40:1181-1189.
125. Di Geso L., Zardi E.M., Afeltra A., Salaffi F., Carotti M., Gutierrez M., et al. Comparison between conventional and automated software-guided ultrasound assessment of bilateral common carotids intima-media thickness in patients with rheumatic diseases. Clin Rheumatol 2012, 31:881-884.
126. Cacciapaglia F., Zardi E.M., Coppolino G., Buzzulini F., Margiotta D., Arcarese L., et al. Stiffness parameters, intima-media thickness and early atherosclerosis in systemic lupus erythematosus patients. Lupus 2009, 18:249-256.
127. Zardi E.M., Afeltra A. Endothelial dysfunction and vascular stiffness in systemic lupus erythematosus: are they early markers of subclinical atherosclerosis?. Autoimmun Rev 2010, 9:684-686.
128. Zardi E.M., Afeltra A. How to predict subclinical atherosclerosis in systemic lupus erythematosus. Rheumatology (Oxford) 2011, 50:821-823.
129. Vadacca M., Zardi E.M., Margiotta D., Rigon A., Cacciapaglia F., Arcarese L., et al. Leptin, adiponectin and vascular stiffness parameters in women with systemic lupus erythematosus. Intern Emerg Med 2013, 8:705-712.
130. Wright S.A., O'Prey F.M., Hamilton P.K., Lockhart C.J., McCann A., McHenry M.T., et al. Colour Doppler ultrasound of the ocular circulation in patients with systemic lupus erythematosus identifies altered microcirculatory haemodynamics. Lupus 2009, 18:950-957.
131. Waterloo K., Omdal R., Sjöholm H., Koldingsnes W., Jacobsen E.A., Sundsfjord J.A., et al. Neuropsychological dysfunction in systemic lupus erythematosus is not associated with changes in cerebral blood flow. J Neurol 2001, 485:595-602.
132. Huang W.S., Chiu P.Y., Tsai C.H., Kao A., Lee C.C. Objective evidence of abnormal regional cerebral blood flow in patients with systemic lupus erythematosus on Tc-99m ECD brain SPECT. Rheumatol Int 2002, 22:178-181.
133. Aaslid R., Markwalder T.M., Nornes H. Noninvasive transcranial Doppler ultrasound recording of flow velocity in basal cerebral arteries. J Neurosurg 1982, 57:769-774.
134. Gosling R.G., King D.H. Arterial assessment by Doppler-shift ultrasound. Proc R Soc Med 1974, 67:447-449.
135. Arnolds B.J., von Reutern G.M. Transcranial Doppler sonography. Examination technique and normal reference values. Ultrasound Med Biol 1986, 21:115-123.
136. Greene E.R., Yonan K.A., Sharrar J.M., Sibbitt W.L., Roldan C.A. Middle cerebral artery resistivity and pulsatility indices in systemic lupus erythematosus: evidence for hyperperfusion. Lupus 2012, 21:380-385.
137. Zardi E.M., Vernieri F., Navarini L., Taccone A., Sambataro G., Alemanno P., et al. Systemic lupus erythematosus patients with and without neuropsychiatric manifestations: a neck and transcranial duplex sonography study. Int J Immunopathol Pharmacol 2012, 25:1157-1165.
138. Tsivgoulis G., Alexandrov A.V., Sloan M.A. Advances in transcranial Doppler ultrasonography. Curr Neurol Neurosci Rep 2009, 9:46-54.
139. Markus H.S. Cerebral perfusion and stroke. J Neurol Neurosurg Psychiatry 2004, 75:353-361.
140. Davey R., Bamford J., Emery P. The role of endothelial dysfunction in the pathogenesis of neuropsychiatric systemic lupus erythematosus. Lupus 2010, 19:797-802.
141. West S.G. Lupus and the central nervous system. Curr Opin Rheumatol 1996, 8:408-414.
142. Hess D.C. Cerebral lupus vasculopathy. Mechanisms and clinical relevance. Ann N Y Acad Sci 1997, 823:154-168.
143. Baizabal-Carvallo J.F., Samson Y. Microembolic signals in systemic lupus erythematosus and other cerebral small vessel diseases. J Neurol 2010, 257:503-508.
144. Russell D., Madden K.P., Clark W.M., Sandset P.M., Zivin J.A. Detection of arterial emboli using Doppler ultrasound in rabbits. Stroke 1991, 22:253-258.
145. Spencer M.P., Thomas G.I., Nicholls S.C. Detection of middle cerebral artery emboli during carotid endarterectomy using transcranial Doppler ultrasonography. Stroke 1990, 21:415-423.
146. Specker C., Rademacher J., Söhngen D., Sitzer M., Janda I., Siebler M., et al. Cerebral microemboli in patients with antiphospholipid syndrome. Lupus 1997, 6:638-644.
147. Rademacher J., Söhngen D., Specker C., Janda I., Sitzer M. Cerebral microembolism, a disease marker for ischemic cerebrovascular events in the antiphospholipid syndrome of systemic lupus erythematosus?. Acta Neurol Scand 1999, 99:356-361.
148. Specker C., Perniok A., Brauckmann U., Siebler M., Schneider M. Detection of cerebral microemboli in APS-introducing a novel investigation method and implications of analogies with carotid artery disease. Lupus 1998, 7:S75-S80.
149. Azarpazhooh M.R., Mokhber N., Orouji E., Chambers B.R., Hatef M.R., Rezaieyazdi Z., et al. Microembolic signals in patients with systemic lupus erythematosus. Can J Neurol Sci 2010, 37:371-375.
150. Kron J., Hamper U.M., Petri M. Prevalence of cerebral microemboli in systemic lupus erythematosus: transcranial Doppler. J Rheumatol 2001, 28:2222-2225.
151. Kumral E., Evyapan D., Keser G., Kabasakal Y., Oksel F., Aksu K., et al. Detection of microembolic signals in patients with neuropsychiatric lupus erythematosus. Eur Neurol 2002, 47:131-135.
152. Cantú-Brito C., Baizabal-Carvallo J.F., Alonso Juarez M., García-Ramos G. The clinical significance of microembolic signals in patients with systemic lupus erythematosus. Neurol Res 2010, 32:134-138.
153. Dahl A., Omdal R., Waterloo K., Joakimsen O., Jacobsen E.A., Koldingsnes W., et al. Detection of cerebral embolic signals in patients with systemic lupus erythematosus. J Neurol Neurosurg Psychiatry 2006, 77:774-779.
154. Baizabal-Carvallo J.F., Cantú-Brito C., García-Ramos G. Acute neurolupus manifested by seizures is associated with high frequency of abnormal cerebral blood flow velocities. Cerebrovasc Dis 2008, 25:348-354.
155. Toledano P., Sarbu N., Espinosa G., Bargalló N., Cervera R. Neuropsychiatric systemic lupus erythematosus: magnetic resonance imaging findings and correlation with clinical and immunological features. Autoimmun Rev 2013, 12:1166-1170.