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Rheumatology International

, Volume 33, Issue 5, pp 1243–1253 | Cite as

Markers of acute neuropsychiatric systemic lupus erythematosus: a multidisciplinary evaluation

  • Essam A. Abda
  • Zahraa I. Selim
  • Moustafa E. M. Radwan
  • Nagham M. Mahmoud
  • Omar M. Herdan
  • Khalid A. Mohamad
  • Sherifa A. HamedEmail author
Original Article

Abstract

This study was aimed to assess: (1) the additive diagnostic utility of diffusion-weighted imaging (DWI) and magnetic resonance angiography (MRA) over conventional MRI in detecting brain lesions in patients with acute primary neuropsychiatric systemic lupus erythematosus (NPSLE), and (2) the relevance of their findings to the associated NP manifestations. Included were 34 patients with acute NPSLE with mean age of 33.26 ± 10.14 years and duration of illness of 3.33 ± 1.71 years. Clinical interviewing and psychiatric and cognitive evaluations were performed by applying the criteria of the diagnostic and statistical manual of mental health disorders criteria (DSM–IV), Stanford Binet Subset Testing, Mini-Mental State Examination and Wechsler Memory Scale-Revised. Serologic tests included looking for antinuclear antibodies, anti-double strand DNA, anti-phospholipid antibodies. Radiologic evaluation included conventional MRI, DWI and MRA. One or more NP manifestations were diagnosed in 28 patients, in which cognitive deficits were reported with headache, psychosis and CVS. Anti-phospholipid antibodies were reported in patients with CVS. Twenty patients (71.43 %) with primary NPSLE (n = 28) had MRI abnormalities in which hyperintense signals at subcortical and periventricular white matter and at the junction between the gray and white matter represented 75 % (n = 15) and with headache (n = 6), psychosis (n = 6) and acute confusional state (n = 3) with and without cognitive deficits, respectively. Moderate-sized infarctions with restricted diffusion in the distribution of middle cerebral arteries were represented in 35 % (n = 7) and with CVS, of them, 71.43 % (n = 5) had beading and focal narrowing of carotid arteries were consistent with vasculitis. Brain atrophy represented 20 % (n = 4) and with psychosis. Compared to those with normal MRI, patients with MRI abnormalities were older (P < 0.050) and had longer duration of illness (P < 0.050). To conclude, although DWI and MRA are helping in more precise etiopathologic diagnosis compared to conventional MRI, but their relevance to the present NP manifestations is still limited.

Keywords

Systemic lupus erythematosus Neuropsychiatric systemic lupus erythematosus Magnetic resonance imaging Diffusion-weighted imaging Magnetic resonance angiography 

Abbreviations

SLE

Systemic lupus erythematosus

NP

Neuropsychiatric

NPSLE

Neuropsychiatric systemic lupus erythematosus

CNS

Central nervous system

CVS

Cerebrovascular stroke

MRI

Magnetic resonance imaging

T1WI

T1-weighted imaging

FLAIR

Fluid attenuation recovery-weighted images

DWI

Diffusion-weighted imaging

MRA

Magnetic resonance angiography

DSM–IV

Diagnostic and statistical manual of mental health disorders 4th (edition)

SBST, 4th edition

Stanford Binet subsets testing (4th edition)

MMSE

Mini-mental state examination

WMS-R

Wechsler memory scale-revised

SLEDAI

Systemic lupus erythematosus disease activity index

ANA

Antinuclear antibodies

a-dsDNA-a

Antibodies to double-stranded DNA

aPL-a

Anti-phospholipid antibodies

Notes

Conflict of interest

We declare that this work has no conflict of interests. There is no involvement of sponsor for this work design, data collection, analysis, interpretation, drafting nor the decision to submit this paper for publication. All are authors’ responsibility.

References

  1. 1.
    Salmon JE, Kimberly RP, Agarti VD (2003) Systemic lupus erythematosus: immunopathology. In: Hochberg MC, Silman A, Smolen JS, Weinblatt ME, Weisman MH (eds) Rheumatology, vol 2, 3rd edn. Mosby, London, pp 1297–1315Google Scholar
  2. 2.
    Danchenko N, Satia JA, Anthony MS (2006) Epidemiology of systemic lupus erythematosus: a comparison of worldwide disease burden. Lupus 15(5):308–318PubMedCrossRefGoogle Scholar
  3. 3.
    Hart HH, Grigor RR, Caughey DE (1983) Ethnic differences in the prevalence of systemic lupus erythematosus. Ann Rheum Dis 42(5):529–532PubMedCrossRefGoogle Scholar
  4. 4.
    American College of Rheumatology Ad Hoc Committee on Systemic Lupus Erythematosus Guidelines (1999) Guidelines for referral and management of systemic lupus erythematosus in adults. Arthritis Rheum 42:1785–1796CrossRefGoogle Scholar
  5. 5.
    Tucker LB, Menon S, Schaller JG, Isenberg DA (1995) Adult and childhood-onset systemic lupus erythematosus: a comparison of onset, clinical features, serology, and outcome. Br J Rheumatol 34(9):866–872PubMedCrossRefGoogle Scholar
  6. 6.
    ACR Ad Hoc Committee on Neuropsychiatric Lupus Nomenclature (1999) The American college of rheumatology nomenclature and case definitions for neuropsychiatric lupus syndromes. Arthritis Rheum 42(4):599–608CrossRefGoogle Scholar
  7. 7.
    Hanly JG (2004) ACR classification criteria for systemic lupus erythematosus: limitations and revisions to neuropsychiatric variables. Lupus 13(11):861–864PubMedCrossRefGoogle Scholar
  8. 8.
    Nomura K, Yamano S, Ikeda Y, Yamada H, Fujimoto T, Minami S, Fukui R, Takaoka M, Yamamoto Y, Dohi K (1999) Asymptomatic cerebrovascular lesions detected by magnetic resonance imaging in patients with systemic lupus erythematosus lacking a history of neuropsychiatric events. Intern Med 38(10):785–795PubMedCrossRefGoogle Scholar
  9. 9.
    Greenwood DL, Gitlits VM, Alderuccio F, Sentry JW, Toh BH (2002) Autoantibodies in neuropsychiatric lupus. Autoimmunity 35(2):79–86PubMedCrossRefGoogle Scholar
  10. 10.
    Hoffman IE, Peene I, Meheus L, Huizinga TW, Cebecauer L, Isenberg D, De Bosschere K, Hulstaert F, Veys EM, De Keyser F (2004) Specific antinuclear antibodies are associated with clinical features in systemic lupus erythematosus. Ann Rheum Dis 63(9):1155–1158PubMedCrossRefGoogle Scholar
  11. 11.
    Rahman A, Hiepe F (2002) Anti-DNA antibodies-overview of assays and clinical correlations. Lupus 11(12):770–773PubMedCrossRefGoogle Scholar
  12. 12.
    Sanna G, Bertolaccini ML, Cuadrado MJ, Laing H, Khamashta MA, Mathieu A, Hughes GR (2003) Neuropsychiatric manifestations in systemic lupus erythematosus: prevalence and association with anti-phospholipid antibodies. J Rheumatol 30(5):985–992PubMedGoogle Scholar
  13. 13.
    Scolding NJ, Joseph FG (2002) The neuropathology and pathogenesis of systemic lupus erythematosus. Neuropathol Appl Neurobiol 28(3):173–189PubMedCrossRefGoogle Scholar
  14. 14.
    Boumpas DT, Yamada H, Patronas NJ, Scott D, Klippel JH, Balow JE (1991) Pulse cyclophosphamide for severe neuropsychiatric lupus. Q J Med 81(296):975–984PubMedCrossRefGoogle Scholar
  15. 15.
    Chinn RJ, Wilkinson ID, Hall-Craggs MA, Paley MN, Shortall E, Carter S, Kendall BE, Isenberg DA, Newman SP, Harrison MJ (1997) Magnetic resonance imaging of the brain and cerebral proton spectroscopy in patients with systemic lupus erythematosus. Arthritis Rheum 40(1):36–46PubMedCrossRefGoogle Scholar
  16. 16.
    Bosma GP, Rood MJ, Huizinga TW, de Jong BA, Bollen EL, van Buchem MA (2000) Detection of cerebral involvement in patients with active neuropsychiatric systemic lupus erythematosus by the use of volumetric magnetization transfer imaging. Arthritis Rheum 43(11):2428–2436PubMedCrossRefGoogle Scholar
  17. 17.
    Moritani T, Shrier DA, Numaguchi Y, Takahashi C, Yano T, Nakai K, Zhong J, Wang HZ, Shibata DK, Naselli SM (2001) Diffusion-weighted echo-planar MR imaging of CNS involvement in systemic lupus erythematosus. Acad Radiol 8(8):741–753PubMedCrossRefGoogle Scholar
  18. 18.
    Appenzeller S, Bonilha L, Rio PA, Min Li L, Costallat LT, Cendes F (2007) Longitudinal analysis of gray and white matter loss in patients with systemic lupus erythematosus. Neuroimage 34(2):694–701PubMedCrossRefGoogle Scholar
  19. 19.
    Pomper MG, Miller TJ, Stone JH, Tidmore WC, Hellmann DB (1999) CNS vasculitis in autoimmune disease: MR imaging findings and correlation with angiography. AJNR Am J Neuroradiol 20(1):75–85PubMedGoogle Scholar
  20. 20.
    Hernández-Molina G, Avila-Casado C, Cárdenas-Velázquez F, Hernández-Hernández C, Calderillo ML, Marroquín V, Soto-Abraham V, Recillas-Gispert C, Sánchez-Guerrero J (2010) Similarities and differences between primary and secondary Sjögren’s syndrome. J Rheumatol 37(4):800–808PubMedCrossRefGoogle Scholar
  21. 21.
    Nowicka-Sauer K, Czuszynska Z, Majkowicz M, Smolenska Z, Jarmoszewicz K, Olesinska M, Siebert J (2012) Neuropsychological assessment in mixed connective tissue disease: comparison with systemic lupus erythematosus. Lupus. 21(9):927–933PubMedCrossRefGoogle Scholar
  22. 22.
    American Psychiatric Association (1994) Diagnostic and statistical manual of mental disorders, 4th edn. American Psychiatric Association, Washington, DC, pp 317–391Google Scholar
  23. 23.
    Melika LK (1998) The Stanford. Binet intelligence scale: Arabic examiner’s handbook, 4th edn. Dar El Maref Publishing, EgyptGoogle Scholar
  24. 24.
    Al-Rajeh S, Ogunniyi A, Awada A, Daif A, Zaidan R (1999) Preliminary assessment of an Arabic version of the mini-mental state examination. Ann Saudi Med 19(2):150–152PubMedGoogle Scholar
  25. 25.
    Wechsler D (1987) Wechsler memory scales-revised. Psychological cooperation, New YorkGoogle Scholar
  26. 26.
    Hamed SA, Selim ZI, Elattar AM, Ahmed EA, Elsorogy YM, Mohamed HO (2012) Assessment of biocorrelates for brain involvement in female patients with rheumatoid arthritis. Clin Rheumatol 31(1):123–132PubMedCrossRefGoogle Scholar
  27. 27.
    Gladman DD, Ibanez D, Urowitz MB (2002) Systemic lupus erythematosus disease activity index. J Rheumatol 29(2):288–291PubMedGoogle Scholar
  28. 28.
    Ainiala H, Loukkola J, Peltola J, Korpela M, Hietaharju A (2001) The prevalence of neuropsychiatric syndromes in systemic lupus erythematosus. Neurology 57(3):496–500PubMedCrossRefGoogle Scholar
  29. 29.
    Kasitanon N, Louthrenoo W, Piyasirisilp S, Sukitawu W, Wichainun R (2002) Neuropsychiatric manifestations in Thai patients with systemic lupus erythematosus. Asian Pac J Allergy Immunol 20(3):179–185PubMedGoogle Scholar
  30. 30.
    Borhani Haghighi A, Haza SG (2010) Neuropsychiatric manifestations of systemic lupus erythematosus: Iranian experience. Ann Indian Acad Neurol 13(2):108–111PubMedCrossRefGoogle Scholar
  31. 31.
    Hanly JG, Cassell K, Fisk JD (1997) Cognitive function in systemic lupus erythematosus: results of a 5-year prospective study. Arthritis Rheum 40(8):1542–1543PubMedCrossRefGoogle Scholar
  32. 32.
    Leritz E, Brandt J, Minor M, Reis-Jensen F, Petri M (2000) Subcortical cognitive impairment in patients with systemic lupus erythematosus. J Int Neuropsychol Soc 6(7):821–825PubMedCrossRefGoogle Scholar
  33. 33.
    Kozora E, Arciniegas DB, Filley CM, West SG, Brown M, Miller D, Grimm A, Devore MD, Wingrove C, Zhang L (2008) Cognitive and neurologic status in patients with systemic lupus erythematosus without major neuropsychiatric syndromes. Arthritis Rheum 59(11):1639–1646PubMedCrossRefGoogle Scholar
  34. 34.
    Futrell N, Millikan C (1989) Frequency, etiology, and prevention of stroke in patients with systemic lupus erythematosus. Stroke 20(5):583–591PubMedCrossRefGoogle Scholar
  35. 35.
    Pego-Reigosa JM, Isenberg DA (2008) Psychosis due to systemic lupus erythematosus: characteristics and long-term outcome of this rare manifestation of the disease. Rheumatology 47(10):1498–1502PubMedCrossRefGoogle Scholar
  36. 36.
    Sfikakis PP, Mitsikostas DD, Manoussakis MN, Foukaneli D, Moutsopoulos HM (1998) Headache in systemic lupus erythematosus. Br J Rheumatol 37(3):300–303PubMedCrossRefGoogle Scholar
  37. 37.
    McCune WJ, MacGuire A, Aisen A, Gebarski S (1988) Identification of brain lesions in neuropsychiatric systemic lupus erythematosus by magnetic resonance scanning. Arthritis Rheum 31(2):159–166PubMedCrossRefGoogle Scholar
  38. 38.
    Sibbitt WL Jr, Sibbitt RR, Griffey RH, Eckel C, Bankhurst AD (1989) Magnetic resonance and computed tomographic imaging in the evaluation of acute neuropsychiatric disease in systemic lupus erythematosus. Ann Rheum Dis 48(12):1014–1022PubMedCrossRefGoogle Scholar
  39. 39.
    Jennings JE, Sundgren PC, Attwood J, McCune J, Maly P (2004) Value of MRI of the brain in patients with systemic lupus erythematosus and neurologic disturbance. Neuroradiology 46(1):15–21PubMedCrossRefGoogle Scholar
  40. 40.
    Abreu MR, Jakosky A, Folgerini M, João Carlos TB, Ricardo MX, Kapczinsky F (2005) Neuropsychiatric systemic lupus erythematosus: correlation of brain MR imaging, CT, and SPECT. Clin Imaging 29(3):215–221PubMedCrossRefGoogle Scholar
  41. 41.
    Kyu CO, Woo MB, Han WJ (2008) MR manifestations of the brain in neuropsychiatric systemic lupus erythematosus patients. J Korean Radiol Soc 58:1–7Google Scholar
  42. 42.
    Appenzeller S, Kobayashi E, Costallat LT, Zanardi VD, Ribeiro Neto JM, Damasceno BP, Cendes F (2000) Magnetic resonance imaging in the evaluation of patients with aseptic meningoencephalitis and connective tissue disorders. Arq Neuropsiquiatr 58(1):45–51PubMedCrossRefGoogle Scholar
  43. 43.
    Mizukami K, Shiraishi H, Tanaka Y, Terashima Y, Kawai N, Baba A, Arai T, Koizumi J (1992) CNS changes in neuro-Behçet’s disease: CT, MR, and SPECT findings. Comput Med Imaging Graph 16(6):401–406PubMedCrossRefGoogle Scholar
  44. 44.
    Davey R, Bamford J, Emery P (2010) The role of endothelial dysfunction in the pathogenesis of neuropsychiatric systemic lupus erythematosus. Lupus 19(7):797–802PubMedCrossRefGoogle Scholar
  45. 45.
    West SG (2002) SLE and the nervous system. In: Wallace DJ, Hahn BH (eds) Dubois’ lupus erythematosus. Williams & Wilkins, Philadelphia, pp 693–738Google Scholar
  46. 46.
    Bosma GP, Middelkoop HA, Rood MJ, Bollen EL, Huizinga TW, van Buchem MA (2002) Association of global brain damage and clinical functioning in neuropsychiatric systemic lupus erythematosus. Arthritis Rheum 46(10):2665–2672PubMedCrossRefGoogle Scholar
  47. 47.
    Menon S, Jameson-Shortall E, Newman SP, Hall-Craggs MR, Chinn R, Isenberg DA (1999) A longitudinal study of anticardiolipin antibody levels and cognitive functioning in systemic lupus erythematosus. Arthritis Rheum 42(4):735–741PubMedCrossRefGoogle Scholar
  48. 48.
    Denburg SD, Denburg JA (2003) Cognitive dysfunction and antiphospholipid antibodies in systemic lupus erythematosus. Lupus 12(12):883–890PubMedCrossRefGoogle Scholar
  49. 49.
    Conti F, Alessandri C, Perricone C, Scrivo R, Rezai S, Ceccarelli F, Spinelli FR, Ortona E, Marianetti M, Mina C, Valesini G (2012) Neurocognitive dysfunction in systemic lupus erythematosus: association with antiphospholipid antibodies, disease activity and chronic damage. PLoS ONE 7(3):e33824PubMedCrossRefGoogle Scholar
  50. 50.
    Gómez-Puerta JA, Martín H, Amigo MC, Aguirre MA, Camps MT, Cuadrado MJ, Hughes GR, Khamashta MA (2005) Long-term follow-up in 128 patients with primary antiphospholipid syndrome: do they develop lupus? Medicine (Baltimore) 84(4):225–230CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  • Essam A. Abda
    • 1
  • Zahraa I. Selim
    • 2
  • Moustafa E. M. Radwan
    • 3
  • Nagham M. Mahmoud
    • 3
  • Omar M. Herdan
    • 4
  • Khalid A. Mohamad
    • 5
  • Sherifa A. Hamed
    • 5
    Email author
  1. 1.Department of Rheumatology and RehabilitationAssiut University HospitalAssiutEgypt
  2. 2.Sohag Faculty of MedicineSouth Valley UniversitySohagEgypt
  3. 3.Department of RadiologyAssiut University HospitalAssiutEgypt
  4. 4.Department of Internal MedicineAssiut University HospitalAssiutEgypt
  5. 5.Department of Neurology and Psychiatry, Faculty of MedicineAssiut University HospitalAssiutEgypt

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