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Microembolic signals in systemic lupus erythematosus and other cerebral small vessel diseases

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Abstract

Microembolic signals (MES) are detected by transcranial Doppler (TCD), and are mainly observed in cardiac and large-artery diseases; however they might also be observed in conditions affecting small vessels of the brain. We aimed to review the current medical literature related to MES assessed by TCD in patients with cerebral small vessel disease. We conducted a systematic review in PubMed and selected the articles with information on this topic. Systemic lupus erythematosus (SLE) is the disease with more articles; pooled data showed a frequency of MES of 14.9%. MES were more frequent in SLE patients with antiphospholipid antibodies and ischemic stroke. MES have also been described in other diseases such as primary antiphospholipid syndrome, Sneddon’s syndrome, and Behçet’s disease. Further studies assessing the significance of MES in the pathogenesis of neurological manifestations of these disorders is warranted.

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References

  1. Aaslid R, Markwalder TM, Nornes H (1982) Noninvasive transcranial Doppler ultrasound recording of flow velocity in basal cerebral arteries. J Neurosurg 57:769–774

    Article  CAS  PubMed  Google Scholar 

  2. Ad Hoc Committee on Lupus Response Criteria: cognition-subcommittee, Mikdashi JA, Esdaile JM, Alarcón GS, Crofford L, Fessler BJ, Shanberg L, Brunner H, Gall V, Kalden JR, Lockshin MD, Liang MH, Roberts N Jr, Schneider M (2007) Proposed response criteria for neurocognitive impairment in systemic lupus erythematosus clinical trials. Lupus 16:418–425

    Article  PubMed  Google Scholar 

  3. Austen W, Howry D (1964) Ultrasound as a method to detect bubbles or particulate matter in the arterial line during cardiopulmonary bypass. J Surg Res 5:283–284

    Article  Google Scholar 

  4. Baizabal-Carvallo JF, Cantú-Brito C, García-Ramos GS (2008) Acute neurolupus manifested by seizures is associated with high frequency of abnormal cerebral blood flow velocities. Cerebrovasc Dis 25:348–354

    Article  PubMed  Google Scholar 

  5. Brey RL, Escalante A (1998) Neurological manifestations of antiphospholipid antibody syndrome. Lupus 7(Suppl 2):67–74

    Article  Google Scholar 

  6. Cantú-Brito C, Baizabal-Carvallo JF, Alonso-Juárez M, García-Ramos GS (2009) The clinical significance of microembolic signals in systemic lupus erythematosus. Neurol Res (in press)

  7. Caplan LR (2003) Small deep brain infarcts. Stroke 34:658–659

    Google Scholar 

  8. Crutchfield K, Patronas NJ, Dambrosia JM, Frei KP, Banerjee TK, Barton NW, Schiffmann R (1998) Quantitative analysis of cerebral vasculopathy in patients with Fabry disease. Neurology 50:1746–1749

    CAS  PubMed  Google Scholar 

  9. Csépány T, Valikovics A, Fülesdi B, Kiss E, Szegedi G, Csiba L (1995) Transcranial Doppler may reveal asymptomatic cerebral vasculopathy in systemic lupus erythematosus. Cerebrovasc Dis 5:178–181

    Article  Google Scholar 

  10. Daffertshofer M, Ries S, Schminke U, Hennerici M (1996) High-intensity transient signals in patients with cerebral ischemia. Stroke 27:1844–1849

    CAS  PubMed  Google Scholar 

  11. Dahl A, Omdal R, Waterloo K, Joakimsen O, Jacobsen EA, Koldingsnes W, Mellgren SI (2006) Detection of cerebral embolic signals in patients with systemic lupus erythematosus. J Neurol Neurosurg Psychiatry 77:774–779

    Article  CAS  PubMed  Google Scholar 

  12. D’Cruz DP, Khamashta MA, Hughes GRV (2007) Systemic lupus erythematosus. Lancet 369:587–596

    Article  PubMed  Google Scholar 

  13. Del Sette M, Angeli S, Stara I, Finocchi C, Gandolfo C (1997) Microembolic signals with serial transcranial Doppler monitoring in acute focal ischemic deficit. A local phenomenon? Stroke 8:1311–1313

    Google Scholar 

  14. Dittrich R, Ringelstein B (2008) Ocurrence and clinical impact of microembolic signals during or after cardiosurgical procedures. Stroke 39:503–511

    Article  PubMed  Google Scholar 

  15. Droste DW, Dittrich R, Hermes S, Kemeny V, Schulte-Altedorneburg G, Hansberg T, Ringelstein EB (1999) Four-gated transcranial Doppler ultrasound in the detection of circulating microemboli. Eur J Ultrasound 9:117–125

    Article  CAS  PubMed  Google Scholar 

  16. Droste DW, Hansberg T, Kemeny V, Hammel D, Schulte-Altedorneburg G, Nabavi DG, Kaps M, Scheld HH, Ringelstein EB (1997) Oxygen inhalation can differentiate gaseous from nongaseous microemboli detected by transcranial Doppler ultrasound. Stroke 28:2453–2456

    CAS  PubMed  Google Scholar 

  17. Fellgiebel A, Muller MJ, Ginsberg L (2006) CNS manifestations of Fabry’s disease. Lancet Neurol 5:791–795

    Article  PubMed  Google Scholar 

  18. Francès C, Papo T, Wechsler B, Laporte JL, Biousse V, Piette JC (1999) Sneddon syndrome with or without antiphospholipid antibodies. A comparative study in 46 patients. Medicine 78:209–219

    Article  PubMed  Google Scholar 

  19. Hanly JG, Walsh NM, Sangalang V (1992) Brain pathology in systemic lupus erythematosus. J Rheumatol 19:732–741

    CAS  PubMed  Google Scholar 

  20. Kawai M, Hiroata S (2000) Cerebrospinal fluid beta(2)-microglobulin in neuro-Behçet’s syndrome. J Neurol Sci 179:132–139

    Article  CAS  PubMed  Google Scholar 

  21. Kiernan RJ, Mueller J, Langston JW, van Dyke C (1987) The neurobehavioral cognitive status examination: a brief but quantitative approach to cognitive assessment. Ann Intern Med 107:481–485

    CAS  PubMed  Google Scholar 

  22. Kozora E, Hanly JG, Lapteva L, Filley CM (2008) Cognitive dysfunction in systemic lupus erythematosus. Past, present, and future. Arthritis Rheum 58:3286–3298

    Article  PubMed  Google Scholar 

  23. Kron J, Hamper UM, Petri M (2001) Prevalence of cerebral microemboli in systemic lupus erythematosus: transcranial Doppler. J Rheumatol 28:2222–2225

    CAS  PubMed  Google Scholar 

  24. Kumral E, Evyapan D, Aksu K, Keser G, Kabasakal Y, Balkir K (2002) Microembolus detection in patients with Takayasu’s arteritis. Stroke 33:712–716

    Article  PubMed  Google Scholar 

  25. Kumral E, Evyapan D, Oksel F, Keser G, Bereketoğlu MA, Balkir K (1999) Transcranial Doppler detection of microembolic signals in patients with Behçet’s disease. J Neurol 246:592–595

    Article  CAS  PubMed  Google Scholar 

  26. Kumral E, Evyapan D, Keser G, Kabasakal Y, Oksel F, Aksu K, Balkir K (2002) Detection of microembolic signals in patients with neuropsychiatric lupus erythematosus. Eur Neurol 47:131–135

    Article  CAS  PubMed  Google Scholar 

  27. Levine JS, Branch DW, Rauch J (2002) The antiphospholipid syndrome. N Engl J Med 346:752–763

    Article  CAS  PubMed  Google Scholar 

  28. Mazzucco S, Anzola GP, Ferrarini M, Taioli F, Olivato S, Burlina AP, Fabrizi GM, Rizzuto N (2009) Cerebral autosomal dominant arteriopathy with subcortical infarcts and leucoencephalopathy and right-to-left shunt: lack of evidence for an association in a prevalence study. Eur Neurol 61:46–49

    Article  CAS  PubMed  Google Scholar 

  29. McLean BN, Miller D, Thompson EJ (1995) Oligoclonal banding of IgG in CSF, blood–brain barrier function, and MRI findings in patients with sarcoidosis, systemic lupus erythematosus, and Behçet’s disease involving the nervous system. J Neurol Neurosurg Psychiatry 58:548–554

    Article  CAS  PubMed  Google Scholar 

  30. Mitsias P, Levine SR (1996) Cerebrovascular complications of Fabry′s disease. Ann Neurol 40:8–17

    Article  CAS  PubMed  Google Scholar 

  31. Moore DF, Altarescu G, Ling GSF, Jeffries N, Frei KP, Weibel T, Charria-Ortiz G, Ferri R, Arai AE, Brady RO, Schiffmann R (2002) Elevated cerebral blood flow velocities in Fabry disease with reversal after enzyme replacement. Stroke 33:525–531

    Article  PubMed  Google Scholar 

  32. Nakajima M, Kimura K, Shimode A, Miyashita F, Uchino M, Naritomi H, Minematsu K (2007) Microembolic signals within 24 hours of stroke onset and diffusion-weighted MRI abnormalities. Cerebrovasc Dis 23:282–288

    Article  PubMed  Google Scholar 

  33. Pfefferkorn T, von Stuckrad-Barre S, Herzog J, Gasser T, Hamann GF, Dichgans M (2001) Reduced cerebrovascular CO(2) reactivity in CADASIL: a transcranial Doppler sonography study. Stroke 32:17–21

    CAS  PubMed  Google Scholar 

  34. Rademacher J, Sohngen D, Specker C, Janda I, Sitzer M (1999) Cerebral microembolism, a disease marker for ischemic cerebrovascular events in the antiphospholipid syndrome of systemic lupus erythematosus? Acta Neurol Scand 99:356–361

    Article  CAS  PubMed  Google Scholar 

  35. Rapp JH, Pan XM, Neumann M, Hong M, Hollenbeck K, Liu J (2008) Microemboli composed of cholesterol crystals disrupt the blood–brain barrier and reduce cognition. Stroke 39:2354–2361

    Article  CAS  PubMed  Google Scholar 

  36. Ritter MA, Dittrich R, Thoenissen N, Ringelsten EB, Nabavi DG (2008) Prevalence and prognostic impact of microembolic signals in arterial sources of embolism. J Neurol 255:953–961

    Article  PubMed  Google Scholar 

  37. Ritter M, Dittrich R, Droste DW (2003) Microembolus detection in four patients with Fabry’s disease: further support for a primarily microangiopathic origin of early cerebrovascular symptoms. Eur Neurol 50:141–145

    Article  PubMed  Google Scholar 

  38. Roman MJ, Shanker B-A, Davis A, Lockshin MD, Sammaritano L, Simantov R, Crow MK, Schwartz JE, Paget SA, Devereux RB, Salmon JE (2003) Prevalence and correlations of accelerated atherosclerosis in systemic lupus erythematosus. New Engl J Med 349:2399–2406

    Article  CAS  PubMed  Google Scholar 

  39. Rovaris M, Viti B, Ciboddo G, Gerevini S, Capra R, Iannucci G, Comi G, Filippi M (2000) Brain involvement in systemic immune mediated diseases: magnetic resonance and magnetization transfer imaging study. J Neurol Neurosurg Psychiatry 68:170–177

    Article  CAS  PubMed  Google Scholar 

  40. Russell D (2002) Cerebral microemboli and cognitive impairment. J Neurol Sci 203–204:211–214

    Article  PubMed  Google Scholar 

  41. Russell D, Madden KP, Clark WM, Sandset PM, Zivin JA (1991) Detection of arterial emboli using Doppler ultrasound in rabbits. Stroke 22:253–258

    CAS  PubMed  Google Scholar 

  42. Sakai K, Nakajima T, Fukuhara N (2006) Transient elevation of the number of microembolic signal in a patient with primary antiphospholipid antibody syndrome. No To Shinkei 58:439–442

    PubMed  Google Scholar 

  43. Selnes OA, Goldsborough MA, Borowicz LM, McKhann GM (1999) Neurobehavioural sequelae of cardiopulmonary bypass. Lancet 353:1601–1606

    Article  CAS  PubMed  Google Scholar 

  44. Sitzer M, Söhngen D, Siebler M, Specker Ch, Rademacher J, Janda I, Aulich A, Steinmetz H (1995) Cerebral microembolism in patients with Sneddon’s syndrome. Arch Neurol 52:271–275

    CAS  PubMed  Google Scholar 

  45. Siva A, Altintas A, Saip S (2004) Behçet’s syndrome and the nervous system. Curr Opin Neurol 17:347–357

    Article  PubMed  Google Scholar 

  46. Specker C, Perniok A, Brauckmann U, Siebler M, Schneider M (1998) Detection of cerebral microemboli in APS––introducing a novel investigation method and implications of analogies with carotid artery disease. Lupus 7(Suppl 2):75–80

    Article  Google Scholar 

  47. Specker C, Rademacher J, Söhngen D, Sitzer M, Janda I, Siebler M, Steinmetz H, Schneider M (1997) Cerebral microemboli in patients with antiphospholipid syndrome. Lupus 6:638–644

    Article  CAS  PubMed  Google Scholar 

  48. Spencer MP, Campbell SD, Sealy JL, Henry FC, Lindbergh J (1969) Experiments on decompression bubbles in the circulation using ultrasonic and electromagnetic flowmeters. J Occup Med 11:238–244

    CAS  PubMed  Google Scholar 

  49. Spencer MP, Thomas GI, Nicholls SC, Sauvage LR (1990) Detection of middle cerebral artery emboli during carotid endarterectomy using transcranial Doppler ultrasonography. Stroke 21:415–423

    CAS  PubMed  Google Scholar 

  50. Tan EM, Cohen AS, Fries JF, Masi AT, McShane DJ, Rothfield NF, Schaller JG, Talal N, Winchester RJ (1982) The 1982 revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum 25:1271–1277

    Article  CAS  PubMed  Google Scholar 

  51. Wong KS, Gao S, Chan YL, Hansberg T, Lam WW, Droste DW, Kay R, Ringelstein EB (2002) Mechanisms of acute cerebral infarctions in patients with middle cerebral artery stenosis: a diffusion-weighted imaging and microemboli monitoring study. Ann Neurol 52:74–81

    Article  PubMed  Google Scholar 

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Correspondence to José Fidel Baizabal-Carvallo.

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Baizabal-Carvallo, J.F., Samson, Y. Microembolic signals in systemic lupus erythematosus and other cerebral small vessel diseases. J Neurol 257, 503–508 (2010). https://doi.org/10.1007/s00415-009-5421-y

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  • DOI: https://doi.org/10.1007/s00415-009-5421-y

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