Diagnostic approach to neuropsychiatric lupus erythematosus: what should we do?

References

• Liang MH, Corzillius M, Bae SC, et al. The American College of Rheumatology nomenclature and case definitions for neuropsychiatric lupus syndromes. Arthritis Rheum. 1999;42(4):599–608.
   PubMed Web of Science ®Google Scholar
• Hermosillo-Romo D, Brey RL. Neuropsychiatric involvement in systemic lupus erythematosus. Curr Rheumatol Rep. 2002;4(4):337–344.
   PubMedGoogle Scholar
• Nived O, Sturfelt G, Liang MH, et al. The ACR nomenclature for CNS lupus revisited. Lupus. 2003;12(12):872–876.
   PubMed Web of Science ®Google Scholar
• Emmer BJ, Steup-Beekman GM, Steens SC, et al. 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(5):1451–1457.
   PubMed Web of Science ®Google Scholar
• Steup-Beekman GM, Zirkzee EJ, Cohen D, et al. Neuropsychiatric manifestations in patients with systemic lupus erythematosus: epidemiology and radiology pointing to an immune-mediated cause. Ann Rheum Dis. 2013;72(Suppl 2):76–79.
   Web of Science ®Google Scholar
• Toledano P, Orueta R, Rodríguez-Pintó I, et al. Peripheral nervous system involvement in systemic lupus erythematosus: prevalence, clinical and immunological characteristics, treatment and outcome of a large cohort from a single center. Autoimmun Rev. 2017;16(7):750–755.
   PubMed Web of Science ®Google Scholar
• Hanly JG, Urowitz MB, Sanchez-Guerrero J, et al. Systemic Lupus International Collaborating Clinics. Neuropsychiatric Events at the Time of Diagnosis of Systemic Lupus Erythematosus: an International Inception Cohort Study. Arthritis Rheum. 2007;56(1):265–273.
   Google Scholar
• Hanly JG, Urowitz MB, Su L, et al. Prospective analysis of neuropsychiatric events in an international disease inception cohort of patients with systemic lupus erythematosus. Ann Rheum Dis. 2010;69(3):529–535.
   PubMed Web of Science ®Google Scholar
• Stojanovich L, Zandman-Goddard G, Pavlovich S, et al. Psychiatric manifestations in systemic lupus erythematosus. Autoimmun Rev. 2007;6(6):421–426.
   PubMed Web of Science ®Google Scholar
• Oomatia A, Fang H, Petri M, et al. Peripheral neuropathies in systemic lupus erythematosus: clinical features, disease associations, and immunologic characteristics evaluated over a twenty-five-year study period. Arthritis Rheumatol Hoboken NJ. 2014;66(4):1000–1009.
   PubMed Web of Science ®Google Scholar
• Tay SH, Mak A. Diagnosing and attributing neuropsychiatric events to systemic lupus erythematosus: time to untie the Gordian knot? Rheumatology (Oxford). 2017;56(suppl 1):i14–i23.
   PubMed Web of Science ®Google Scholar
• Borowoy AM, Pope JE, Silverman E, 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(2):179–185.
   PubMed Web of Science ®Google Scholar
• Govoni M, Bortoluzzi A, Padovan M, et al. The diagnosis and clinical management of the neuropsychiatric manifestations of lupus. J Autoimmun. 2016;74:41–72.
   PubMed Web of Science ®Google Scholar
• Klein-Gitelman M, Brunner HI. The impact and implications of neuropsychiatric systemic lupus erythematosus in adolescents. Curr Rheumatol Rep. 2009;11(3):212–217.
   PubMedGoogle Scholar
• Faria R, Gonçalves J, Dias R. Neuropsychiatric systemic lupus erythematosus involvement: towards a tailored approach to our patients? Rambam Maimonides Med J. 2017;8:1.
   Web of Science ®Google Scholar
• Gualtierotti R, Guarnaccia L, Beretta M, et al. Modulation of neuroinflammation in the central nervous system: role of chemokines and sphingolipids. Adv Ther. 2017;34(2):396–420.
   PubMed Web of Science ®Google Scholar
• Namjou B, Kothari PH, Kelly JA, et al. Evaluation of the TREX1 gene in a large multi-ancestral lupus cohort. Genes Immun. 2011;12(4):270–279.
   PubMed Web of Science ®Google Scholar
• Blank T, Type PM. I interferon pathway in CNS homeostasis and neurological disorders. Glia. 2017;65(9):1397–1406.
   PubMed Web of Science ®Google Scholar
• Rice GI, Rodero MP, Crow YJ. Human disease phenotypes associated with mutations in TREX1. J Clin Immunol. 2015;35(3):235–243.
   PubMed Web of Science ®Google Scholar
• Kisla Ekinci RM, Balci S, Bisgin A, et al. A homozygote TREX1 mutation in two siblings with different phenotypes: chilblains and cerebral vasculitis. Eur J Med Genet. 2017;60(12):690–694.
   PubMed Web of Science ®Google Scholar
• Sonar SA, Shaikh S, Joshi N, et al. promotes transendothelial migration of CD4+ T cells across the blood-brain barrier. Immunol Cell Biol. 2017;95(9):843–853.
   PubMed Web of Science ®Google Scholar
• Asano T, Ito H, Kariya Y. Evaluation of blood-brain barrier function by quotient alpha2 macroglobulin and its relationship with interleukin-6 and complement component 3 levels in neuropsychiatric systemic lupus erythematosus. PLoS One. 2017;12(10):e0186414.
   PubMed Web of Science ®Google Scholar
• Hirohata S, Arinuma Y, Yanagida T, et al. Blood-brain barrier damages and intrathecal synthesis of anti-N-methyl-D-aspartate receptor NR2 antibodies in diffuse psychiatric/neuropsychological syndromes in systemic lupus erythematosus. Arthritis Res Ther. 2014;16(2):R77.
   PubMed Web of Science ®Google Scholar
• Jeltsch-David H, Muller S. Neuropsychiatric systemic lupus erythematosus: pathogenesis and biomarkers. Nat Rev Neurol. 2014;10(10):579–596.
   PubMed Web of Science ®Google Scholar
• Yelnik CM, Kozora E, Appenzeller S. Cognitive disorders and antiphospholipid antibodies. Autoimmun Rev. 2016;15(12):1193–1198.
   PubMed Web of Science ®Google Scholar
• Lapter S, Marom A, Meshorer A, et al. Amelioration of brain pathology and behavioral dysfunction in mice with lupus following treatment with a tolerogenic peptide. Arthritis Rheum. 2009;60(12):3744–3754.
   PubMed Web of Science ®Google Scholar
• Crupi R, Cambiaghi M, Spatz L, et al. Reduced adult neurogenesis and altered emotional behaviors in autoimmune-prone B-cell activating factor transgenic mice. Biol Psychiatry. 2010;67(6):558–566.
   PubMed Web of Science ®Google Scholar
• Iikuni N, Okamoto H, Yoshio T, et al. Raised monocyte chemotactic protein-1 (MCP-1)/CCL2 in cerebrospinal fluid of patients with neuropsychiatric lupus. Ann Rheum Dis. 2006;65(2):253–256.
   PubMed Web of Science ®Google Scholar
• Okamoto H, Katsumata Y, Nishimura K, et al. Interferon-inducible protein 10/CXCL10 is increased in the cerebrospinal fluid of patients with central nervous system lupus. Arthritis Rheum. 2004;50(11):3731–3732.
   PubMed Web of Science ®Google Scholar
• Brooks WM, Sibbitt WL, Kornfeld M, et al. The histopathologic associates of neurometabolite abnormalities in fatal neuropsychiatric systemic lupus erythematosus. Arthritis Rheum. 2010;62(7):2055–2063.
   PubMed Web of Science ®Google Scholar
• Postal M, Costallat LT, Appenzeller S. Neuropsychiatric manifestations in systemic lupus erythematosus: epidemiology, pathophysiology and management. CNS Drugs. 2011;25:721–736.
   PubMed Web of Science ®Google Scholar
• Tatsukawa H, Ishii K, Haranaka M, et al. Evaluation of average amount of cerebral blood flow measured by brain perfusion index in patients with neuropsychiatric systemic lupus erythematosus. Lupus. 2005;14(6):445–449.
   PubMed Web of Science ®Google Scholar
• Hanly JG, Walsh NM, Sangalang V. Brain pathology in systemic lupus erythematosus. J Rheumatol. 1992;19(5):732–741.
   PubMed Web of Science ®Google Scholar
• Leung JW, Lau BW, Chan VS, et al. Abnormal increase of neuronal precursor cells and exacerbated neuroinflammation in the corpus callosum in murine model of systemic lupus erythematosus. Restor Neurol Neurosci. 2016;34(3):443–453.
   PubMed Web of Science ®Google Scholar
• Shoenfeld Y, Alarcon-Segovia D, Buskila D, 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(2):112–130.
   PubMed Web of Science ®Google Scholar
• Kempuraj D, Thangavel R, Selvakumar GP, et al. Brain and peripheral atypical inflammatory mediators potentiate neuroinflammation and neurodegeneration. Front Cell Neurosci. 2017;11:216.
   PubMed Web of Science ®Google Scholar
• Costallat LT, De Oliveira RM, Santiago MB, et al. Neuropsychiatric manifestations of systemic lupus erythematosus: the value of anticardiolipin, antigangliosides and antigalactocerebrosides antibodies. Clin Rheumatol. 1990;9(4):489–497.
   PubMed Web of Science ®Google Scholar
• Pradhan V, Patwardhan M, Rajadhyaksha A, et al. Neuropsychiatric manifestations and associated autoantibodies in systemic lupus erythematosus patients from Western India. Rheumatol Int. 2015;35(3):541–545.
   PubMed Web of Science ®Google Scholar
• Kiss E, Shoenfeld Y. Are anti-ribosomal P protein antibodies relevant in systemic lupus erythematosus? Clin Rev Allergy Immunol. 2007;32(1):37–46.
   PubMed Web of Science ®Google Scholar
• Ho RC, Thiaghu C, Ong H, et al. A meta-analysis of serum and cerebrospinal fluid autoantibodies in neuropsychiatric systemic lupus erythematosus. Autoimmun Rev. 2016;15(2):124–138.
   PubMed Web of Science ®Google Scholar
• Yoshio T, Masuyama J, Ikeda M, et al. Quantification of antiribosomal P0 protein antibodies by ELISA with recombinant P0 fusion protein and their association with central nervous system disease in systemic lupus erythematosus. J Rheumatol. 1995;22:1681–1687.
   PubMed Web of Science ®Google Scholar
• Sciascia S, Bertolaccini ML, Roccatello D, et al. Autoantibodies involved in neuropsychiatric manifestations associated with systemic lupus erythematosus: a systematic review. J Neurol. 2014;261(9):1706–1714.
   PubMed Web of Science ®Google Scholar
• Govoni M, Bombardieri S, Bortoluzzi A, 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(1):157–168.
   Google Scholar
• Katzav A, Shoenfeld Y, Chapman J. The pathogenesis of neural injury in animal models of the antiphospholipid syndrome. Clin Rev Allergy Immunol. 2010;38(2–3):196–200.
   PubMed Web of Science ®Google Scholar
• Sanna G, Bertolaccini ML, Cuadrado MJ, et al. Neuropsychiatric manifestations in systemic lupus erythematosus: prevalence and association with antiphospholipid antibodies. J Rheumatol. 2003;30(5):985–992.
   PubMed Web of Science ®Google Scholar
• Hawro T, Bogucki A, Krupińska-Kun M, et al. Intractable headaches, ischemic stroke, and seizures are linked to the presence of anti-β2GPI antibodies in patients with systemic lupus erythematosus. PLoS One. 2015;10(3):e0119911.
   PubMed Web of Science ®Google Scholar
• Delunardo F, Soldati D, Bellisario V, et al. Anti-GAPDH autoantibodies as a pathogenic determinant and potential biomarker of neuropsychiatric diseases. Arthritis Rheumatol. 2016;68(11):2708–2716.
   PubMed Web of Science ®Google Scholar
• DeGiorgio LA, Konstantinov KN, Lee SC, et al. A subset of lupus anti-DNA antibodies cross-reacts with the NR2 glutamate receptor in systemic lupus erythematosus. Nat Med. 2001;7(11):1189–1193.
   PubMed Web of Science ®Google Scholar
• Chang EH, Volpe BT, Mackay M, et al. Selective Impairment of spatial cognition caused by autoantibodies to the N-methyl-D-aspartate receptor. EBioMedicine. 2015;2(7):755–764.
   PubMed Web of Science ®Google Scholar
• Ogawa E, Nagai T, Sakuma Y, et al. Association of antibodies to the NR1 subunit of N-methyl-D-aspartate receptors with neuropsychiatric systemic lupus erythematosus. Mod Rheumatol. 2016;26(3):377–383.
   PubMed Web of Science ®Google Scholar
• Arinuma Y. Antibodies and the brain: anti-N-methyl-D-aspartate receptor antibody and the clinical effects in patients with systemic lupus erythematosus. Curr Opin Neurol. 2018 Feb 22. DOI:10.1097/WCO.0000000000000554.
   PubMed Web of Science ®Google Scholar
• Yang Y, Yuan C, Shen SQ, et al. Autoantibodies to NR2A peptide of the glutamate/NMDA receptor in patients with seizure disorders in neuropsychiatric systemic lupus erythematosus. Mediators Inflamm. 2017;2017:5047898.
   PubMed Web of Science ®Google Scholar
• Perricone C, Pendolino M, Olivieri M, et al. Neuropsychiatric manifestations associated with anti-endothelial cell antibodies in systemic lupus erythematosus. Isr Med Assoc J. 2015;17(3):171–178.
   PubMed Web of Science ®Google Scholar
• George-Chandy A, Trysberg E, Eriksson K. Raised intrathecal levels of APRIL and BAFF in patients with systemic lupus erythematosus: relationship to neuro-psychiatric symptoms. Arthritis Res Ther. 2008;10:R97.
   PubMed Web of Science ®Google Scholar
• Gulati G, Iffland PH, Janigro D, et al. Anti-NR2 antibodies, blood-brain barrier, and cognitive dysfunction. Clin Rheumatol. 2016;35(12):2989–2997.
   PubMed Web of Science ®Google Scholar
• Huerta PT, Gibson EL, Rey C, et al. Integrative neuroscience approach to neuropsychiatric lupus. Immunol Res. 2015;63(1–3):11–17.
   PubMed Web of Science ®Google Scholar
• Feinglass EJ, Arnett FC, Dorsch CA, et al. Neuropsychiatric manifestations of systemic lupus erythematosus: diagnosis, clinical spectrum, and relationship to other features of the disease. Medicine (Baltimore). 1976;55:323–339.
   PubMed Web of Science ®Google Scholar
• Hochberg MC. Updating the American College of Rheumatology revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum. 1997;40(9):1725.
   PubMed Web of Science ®Google Scholar
• Petri M, Orbai AM, Alarcon GS, et al. Derivation and validation of the Systemic Lupus International Collaborating Clinics classification criteria for systemic lupus erythematosus. Arthritis Rheum. 2012;64(8):2677–2686.
   PubMed Web of Science ®Google Scholar
• Pamfil C, Fanouriakis A, Damian L, et al. EULAR recommendations for neuropsychiatric systemic lupus erythematosus vs usual care: results from two European centres. Rheumatology (Oxford). 2015;54(7):1270–1278.
   PubMed Web of Science ®Google Scholar
• Alessi H, Dutra LA, Braga PN, et al. Neuropsychiatric Lupus in clinical practice. Arq Neuropsiquiatr. 2016;74(12):1021–1030.
   PubMed Web of Science ®Google Scholar
• Tselios K, Gladman DD, Su J, et al. Evolution of risk factors for atherosclerotic cardiovascular events in systemic lupus erythematosus: a longterm prospective study. J Rheumatol. 2017. Nov 1. pii: jrheum.161121. DOI:10.3899/jrheum.161121.
   PubMed Web of Science ®Google Scholar
• Singer HS. Autoantibody-associated movement disorders in children: proven and Proposed. Semin Pediatr Neurol. 2017;24(3):168–179.
   PubMed Web of Science ®Google Scholar
• Fang H, Lan L, Qu Y, et al. Differences between central nervous system infection and neuropsychiatric systemic lupus erythematosus in patients with systemic lupus erythematosus. J Int Med Res. 2017 1;Jan:300060517722695.
   Google Scholar
• Nishimura K, Omori M, Sato E, et al. New-onset psychiatric disorders after corticosteroid therapy in systemic lupus erythematosus: an observational case-series study. J Neurol. 2014;261(11):2150–2158.
   PubMed Web of Science ®Google Scholar
• Bertsias GK, Ioannidis JP, Aringer M, 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(12):2074–2082.
   PubMed Web of Science ®Google Scholar
• Monov S, Monova D. Classification criteria for neuropsychiatric systemic lupus erythematosus: do they need a discussion? Hippokratia. 2008;12(2):103–107.
   PubMed Web of Science ®Google Scholar
• Hanly JG. The neuropsychiatric SLE SLICC inception cohort study. Lupus. 2008;17(12):1059–1063.
   PubMed Web of Science ®Google Scholar
• Hanly JG, Urowitz MB, Su L, et al. Systemic Lupus International Collaborating Clinics. Short-Term Outcome of Neuropsychiatric Events in Systemic Lupus Erythematosus upon Enrollment into an International Inception Cohort Study. Arthritis Rheum. 2008;59(5):721–729.
   Google Scholar
• Bortoluzzi A, Scirè CA, Bombardieri S, et al. Study Group on Neuropsychiatric Systemic Lupus Erythematosus of the Italian Society of Rheumatology. Development and Validation of a New Algorithm for Attribution of Neuropsychiatric Events in Systemic Lupus Erythematosus. Rheumatology (Oxford). 2015;54(5):891–898.
   Google Scholar
• Fanouriakis A, Pamfil C, Rednic S, et al. Is it primary neuropsychiatric systemic lupus erythematosus? Performance of existing attribution models using physician judgment as the gold standard. Clin Exp Rheumatol. 2016;34(5):910–917.
   PubMed Web of Science ®Google Scholar
• Bortoluzzi A, Fanouriakis A, Appenzeller S, et al. Validity of the Italian algorithm for the attribution of neuropsychiatric events in systemic lupus erythematosus: a retrospective multicentre international diagnostic cohort study. BMJ Open. 2017;7(5):e015546.
   PubMed Web of Science ®Google Scholar
• Govoni M, Bortoluzzi A. Lupus or not lupus? Neuropsychiatric symptom attribution in systemic lupus erythematosus. Rheumatology (Oxford). 2017;56(10):1639–1640.
   PubMed Web of Science ®Google Scholar
• Zardi EM, Taccone A, Marigliano B, et al. Neuropsychiatric systemic lupus erythematosus: tools for the diagnosis. Autoimmun Rev. 2014;13(8):831–839.
   PubMed Web of Science ®Google Scholar
• Hamming L, Van Der Meulen R, Vergouwen A, et al. Myelopathy in systemic lupus erythematosus: a case report and a review of the literature. Neth J Med. 2015;73(6):290–292.
   PubMed Web of Science ®Google Scholar
• Netto TM, Zimmermann N, Rueda-Lopes F, et al. Neuropsychiatric lupus: classification criteria in neuroimaging studies. Can J Neurol Sci. 2013;40(3):284–291.
   PubMed Web of Science ®Google Scholar
• Roldan CA, Gelgand EA, Qualls CR, et al. Valvular heart disease is associated with nonfocal neuropsychiatric systemic lupus erythematosus. J Clin Rheumatol. 2006;12(1):3–10.
   PubMed Web of Science ®Google Scholar
• Roldan CA, Gelgand EA, Qualls CR, et al. Valvular heart disease by transthoracic echocardiography is associated with focal brain injury and central neuropsychiatric systemic lupus erythematosus. Cardiology. 2007;108(4):331–337.
   PubMed Web of Science ®Google Scholar
• Roldan CA, Sibbitt WL, Qualls CR, et al. Libman-Sacks endocarditis and embolic cerebrovascular disease. JACC Cardiovasc Imaging. 2013;6(9):973–983.
   PubMed Web of Science ®Google Scholar
• Azarpazhooh MR, Mokhber N, Orouji E, et al. Microembolic signals in patients with systemic lupus erythematosus.Can. J Neurol Sci. 2010;37(3):371–375.
   Web of Science ®Google Scholar
• Zardi EM, Spoto S, Locorriere L, et al. Platypnoea-orthodeoxia syndrome in the elderly: a difficult-to-make diagnosis of intracardiac right-to-left shunt. Scott Med J. 2017;62(3):122–125.
   PubMed Web of Science ®Google Scholar
• Lim ST, Murphy SJX, Smith DR, et al. Clinical outcomes and a high prevalence of abnormalities on comprehensive arterial and venous thrombophilia screening in TIA or ischaemic stroke patients with a patent foramen ovale, an inter-atrial septal aneurysm or both. J Neurol Sci. 2017;377:227–233.
   PubMed Web of Science ®Google Scholar
• Gupta SK, Shetkar SS, Ramakrishnan S, et al. Saline contrast echocardiography in the era of multimodality imaging–importance of “Bubbling It Right”. Echocardiography. 2015;32(11):1707–1719.
   PubMed Web of Science ®Google Scholar
• Arntzen KA, Schirmer H, Johnsen SH, et al. Carotid artery plaque progression and cognitive decline: the Tromsø study 1994-2008. Eur J Neurol. 2012;19(10):1318–1324.
   PubMed Web of Science ®Google Scholar
• Zardi EM, Di Geso L, Afeltra A, et al. An ultrasound automated method for non-invasive assessment of carotid artery pulse wave velocity. J Invest Med. 2017 Sep 2. DOI:10.1136/jim-2017-000430.
   PubMed Web of Science ®Google Scholar
• Ikeda N, Dey N, Sharma A, et al. Automated segmental-IMT measurement in thin/thick plaque with bulb presence in carotid ultrasound from multiple scanners: stroke risk assessment. Comput Methods Programs Biomed. 2017;141:73–81.
   PubMed Web of Science ®Google Scholar
• Aaslid R, Markwalder TM, Nornes H. Noninvasive transcranial Doppler ultrasound recording of flow velocity in basal cerebral arteries. J Neurosurg. 1982;57(6):769–774.
   PubMed Web of Science ®Google Scholar
• Zardi EM, Vernieri F, Navarini L, et al. Systemic lupus erythematosus patients with and without neuropsychiatric manifestations: a neck and transcranial duplex sonography study. Int J Immunopathol Pharmacol. 2012;25(4):1157–1165.
   PubMed Web of Science ®Google Scholar
• Zardi EM, Afeltra A. How to predict subclinical atherosclerosis in systemic lupus erythematosus. Rheumatology (Oxford). 2011;50(5):821–823.
   PubMed Web of Science ®Google Scholar
• Di Geso L, Zardi EM, Afeltra A, 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(5):881–884.
   PubMed Web of Science ®Google Scholar
• D’Andrea A, Conte M, Cavallaro M, et al. Transcranial Doppler ultrasonography: from methodology to major clinical applications. World J Cardiol. 2016;8(7):383–440.
   PubMed Web of Science ®Google Scholar
• Malojcic B, Giannakopoulos P, Sorond FA, et al. Ultrasound and dynamic functional imaging in vascular cognitive impairment and Alzheimer’s disease. BMC Med. 2017;15:27.
   PubMed Web of Science ®Google Scholar
• Markus HS. Cerebral perfusion and stroke. J Neurol Neurosurg Psychiatry. 2004;75(3):353–361.
   PubMed Web of Science ®Google Scholar
• Davey R, Bamford J, Emery P. The role of endothelial dysfunction in the pathogenesis of neuropsychiatric systemic lupus erythematosus. Lupus. 2010;19(7):797–802.
   PubMed Web of Science ®Google Scholar
• Cantú-Brito C, Baizabal-Carvallo JF, Alonso-Juárez M, et al. The clinical significance of microembolic signals in patients with systemic lupus erythematosus. Neurol Res. 2010;32(2):134–138.
   PubMed Web of Science ®Google Scholar
• Bortoluzzi A, Padovan M, Azzini C, et al. Brain unidentified bright objects (“UBO”) in systemic lupus erythematosus: sometimes they come back. A Study of Microembolism by cMRI and Transcranial Doppler Ultrasound. Lupus. 2016;25(2):193–198.
   Google Scholar
• Kumral E, Evyapan D, Keser G, et al. Detection of microembolic signals in patients with neuropsychiatric lupus erythematosus. Eur Neurol. 2002;47(3):131–135.
   PubMed Web of Science ®Google Scholar
• Panerai RB, Eyre M, Potter JF. Multivariate modeling of cognitive-motor stimulation on neurovascular coupling: transcranial Doppler used to characterize myogenic and metabolic influences. Am J Physiol Regul Integr Comp Physiol. 2012;303(4):R395–407.
   PubMed Web of Science ®Google Scholar
• Bleton H, Perera S, Sejdić E. Cognitive tasks and cerebral blood flow through anterior cerebral arteries: a study via functional transcranial Doppler ultrasound recordings. BMC Med Imaging. 2016;16:22.
   PubMed Web of Science ®Google Scholar
• Baizabal-Carvallo JF, Samson Y. Microembolic signals in systemic lupus erythematosus and other cerebral small vessel diseases. J Neurol. 2010;257(4):503–508.
   PubMed Web of Science ®Google Scholar
• Jennings JE, Sundgren PC, Attwood J, et al. Value of MRI of the brain in patients with systemic lupus erythematosus and neurologic disturbance. Neuroradiology. 2004;46(1):15–21.
   PubMed Web of Science ®Google Scholar
• Mc CWJ, MacGuire A, Aisen A, et al. Identification of brain lesions in neuropsychiatric systemic lupus erythematosus by magnetic resonance scanning. Arthritis Rheum. 1988;31(2):159–166.
   PubMed Web of Science ®Google Scholar
• Luyendijk J, Steens SC, Ouwendijk WJ, et al. Neuropsychiatric systemic lupus erythematosus: lessons learned from magnetic resonance imaging. Arthritis Rheum. 2011;63(3):722–732.
   PubMed Web of Science ®Google Scholar
• Pierpaoli C. Quantitative brain MR. Top Magn Reson Imaging. 2010;21(2):63.
   PubMedGoogle Scholar
• Sarbu N, Alobeidi F, Toledano P, et al. Brain abnormalities in newly diagnosed neuropsychiatric lupus: systematic MRI approach and correlation with clinical and laboratory data in a large multicenter cohort. Autoimmun Rev. 2015;14(2):153–159.
   PubMed Web of Science ®Google Scholar
• Zimmermann N, Goulart Corrêa D, Tukamoto G, et al. Brain morphology and cortical thickness variations in systemic lupus erythematosus patients: differences among neurological, psychiatric, and nonneuropsychiatric manifestations. J Magn Reson Imaging. 2017;46(1):150–158.
   PubMed Web of Science ®Google Scholar
• Emmer BJ, Van Osch MJ, Wu O, et al. Perfusion MRI in neuro-psychiatric systemic lupus erthemathosus. J Magn Reson Imaging. 2010;32(2):283–288.
   PubMed Web of Science ®Google Scholar
• Papadaki E, Fanouriakis A, Kavroulakis E, et al. Neuropsychiatric lupus or not? Cerebral hypoperfusion by perfusion-weighted MRI in normal-appearing white matter in primary neuropsychiatric lupus erythematosus. Ann Rheum Dis. 2018;77(3):441–448.
   PubMed Web of Science ®Google Scholar
• Mikdashi JA. Altered functional neuronal activity in neuropsychiatric lupus: a systematic review of the fMRI investigations. Semin Arthritis Rheum. 2016;45(4):455–462.
   PubMed Web of Science ®Google Scholar
• Kording F, Weidensteiner C, Zwick S, et al. Simultaneous assessment of vessel size index, relative blood volume, and vessel permeability in a mouse brain tumor model using a combined spin echo gradient echo echo-planar imaging sequence and viable tumor analysis. J Magn Reson Imaging. 2014;40(6):1310–1318.
   PubMed Web of Science ®Google Scholar
• Jensen JH, Chandra R. MR imaging of microvasculature. Magn Reson Med. 2000;44(2):224–230.
   PubMed Web of Science ®Google Scholar
• Harrison NA, Cooper E, Dowell NG, et al. Quantitative magnetization transfer imaging as a biomarker for effects of systemic inflammation on the brain. Biol Psychiatry. 2015;78(1):49–57.
   PubMed Web of Science ®Google Scholar
• Alexander AL, Lee JE, Lazar M, et al. Diffusion tensor imaging of the brain. Neurotherapeutics. 2007;4(3):316–329.
   PubMed Web of Science ®Google Scholar
• Sarbu N, Toledano P, Calvo A, et al. Advanced MRI techniques: biomarkers in neuropsychiatric lupus. Lupus. 2017;26:510–516.
   PubMed Web of Science ®Google Scholar
• Shastri R, Shah G, Wang P, et al. MR diffusion tractography to identify and characterize microstructural white matter tract changes in systemic lupus erythematosus patients. Acad Radiol. 2016;23(11):1431–1440.
   PubMed Web of Science ®Google Scholar
• Capizzano AA, Schuff N, Amend DL, et al. Subcortical ischemic vascular dementia: assessment with quantitative MR imaging and 1H MR spectroscopy. Am J Neuroradiol. 2000;21(4):621–630.
   PubMed Web of Science ®Google Scholar
• Lin W-Y, Wang SJ, Yen TC, et al. Technetium-99m-HMPAO brain SPECT in systemic lupus erythematosus with CNS involvement. J Nucl Med. 1997;38(7):1112–1115.
   PubMed Web of Science ®Google Scholar
• Liberatore M, Morreale M, Megna V, et al. Role of brain perfusion SPECT with 99mTc HMPAO in the assessment of response to drug therapy in patients with autoimmune vasculitis: a prospective study. N Am J Med Sci. 2015;7(4):135–142.
   PubMed Web of Science ®Google Scholar
• Kao CH, Lan JL, ChangLai SP, 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. 1999 Feb;26(2):129–134.
   PubMedGoogle Scholar
• Cagnoli P, Harris RE, Frechtling D, et al. Reduced Insular Glutamine and N-acetylaspartate in systemic lupus erythematosus: a single-voxel (1)H-MR spectroscopy study. Acad Radiol. 2013;20(10):1286–1296.
   PubMed Web of Science ®Google Scholar
• Stoppe G, Wildhagen K, Seidel JW, et al. Positron emission tomography in neuropsychiatric lupus erythematosus. Neurology. 1990;40(2):304–308.
   PubMed Web of Science ®Google Scholar
• Kao CH, Ho YJ, Lan JL, 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.
   PubMed Web of Science ®Google Scholar
• Weiner SM, Otte A, Schumacher M, 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(5):377–385.
   PubMed Web of Science ®Google Scholar
• Mauro D, Barbagallo G, D’Angelo S, et al. Role of positron emission tomography for central nervous system involvement in systemic autoimmune diseases: status and perspectives. Curr Med Chem. 2017 May 23. DOI:10.2174/0929867324666170523144402.
   PubMed Web of Science ®Google Scholar
• Brainin M, Barnes M, Baron JC, et al. Guidance for the preparation of neurological management guidelines by EFNS scientifi c task forces – revised recommendations. Eur J Neurol. 2004;11(9):577–581.
   PubMed Web of Science ®Google Scholar
• Hirohata S, Kanai Y, Mitsuo A, Tokano Y, Hashimoto H; NPSLE Research Subcommittee. Accuracy of cerebrospinal fluid IL-6 testing for diagnosis of lupus psychosis. A Multicenter Retrospective Study. Clin Rheumatol. 2009;28(11):1319–1323.
   PubMed Web of Science ®Google Scholar
• Riviere E, Cohen Aubart F, Maisonobe T, et al. Clinicopathological features of multiple mononeuropathy associated with systemic lupus erythematosus: a multicenter study. J Neurol. 2017;264(6):1218–1226.
   PubMed Web of Science ®Google Scholar