Top

Published in:

01-01-2013 | Original Communication

Patent foramen ovale and atrial septal aneurysm can cause ischemic stroke in patients with antiphospholipid syndrome

Authors: Yasutaka Tanaka, Yuji Ueno, Nobukazu Miyamoto, Yoshiaki Shimada, Ryota Tanaka, Nobutaka Hattori, Takao Urabe

Published in: Journal of Neurology | Issue 1/2013

Abstract

The purpose of the present study was to evaluate the contributions of embolic etiologies, patent foramen ovale (PFO) and atrial septal aneurysm (ASA) to the pathogenesis of ischemic stroke in patients with antiphospholipid syndrome (APS). We performed transesophageal echocardiography (TEE) examination for consecutive stroke patients who had been diagnosed with APS (APS group) to detect potential embolic sources. APS was diagnosed based on the modified Sapporo criteria. The control stroke group comprised age- and sex-matched cryptogenic stroke patients undergoing TEE. We assessed and compared the clinical characteristics and TEE findings between stroke patients with APS and control stroke groups. Among 582 patients, nine patients (nine women; mean age, 50 ± 18 years) were classified into the APS group. In 137 patients undergoing TEE, 41 age-matched female stroke patients were recruited to the control stroke group. Prevalences of PFO and ASA were significantly higher in the APS group than in the control stroke group (89 vs. 41 %, p = 0.027; 67 vs. 20 %, p = 0.015, respectively). Multiple logistic regression analysis showed that PFO (odds ratio (OR), 13.71; 95 % confidence interval (CI), 1.01–185.62; p = 0.049) and ASA (OR, 8.06; 95 % CI, 1.17–55.59; p = 0.034) were independently associated with the APS group. PFO and ASA were strongly associated with the APS group, and could thus represent potential embolic sources in ischemic stroke patients with APS.

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

Miyakis S, Lockshin MD, Atsumi T, Branch DW, Brey RL, Cervera R, Derksen RH, de Groot PG, Koike T, Meroni PL, Reber G, Shoenfeld Y, Tincani A, Vlachoyiannopoulos PG, Krilis SA (2006) International consensus statement on an update of the classification criteria for definite antiphospholipid syndrome (APS). J Thromb Haemost 4:295–306PubMedCrossRef

Gromnica-Ihle E, Schossler W (2000) Antiphospholipid syndrome. Int Arch Allergy Immunol 123:67–76PubMedCrossRef

Wilson WA, Gharavi AE, Koike T, Lockshin MD, Branch DW, Piette JC, Brey R, Derksen R, Harris EN, Hughes GR, Triplett DA, Khamashta MA (1999) International consensus statement on preliminary classification criteria for definite antiphospholipid syndrome: report of an international workshop. Arthritis Rheum 42:1309–1311PubMedCrossRef

Matsuura E, Igarashi Y, Fujimoto M, Ichikawa K, Koike T (1990) Anticardiolipin cofactor(s) and differential diagnosis of autoimmune disease. Lancet 336:177–178PubMedCrossRef

Cervera R, Piette JC, Font J, Khamashta MA, Shoenfeld Y, Camps MT, Jacobsen S, Lakos G, Tincani A, Kontopoulou-Griva I, Galeazzi M, Meroni PL, Derksen RH, de Groot PG, Gromnica-Ihle E, Baleva M, Mosca M, Bombardieri S, Houssiau F, Gris JC, Quere I, Hachulla E, Vasconcelos C, Roch B, Fernandez-Nebro A, Boffa MC, Hughes GR, Ingelmo M (2002) Antiphospholipid syndrome: clinical and immunologic manifestations and patterns of disease expression in a cohort of 1,000 patients. Arthritis Rheum 46:1019–1027PubMedCrossRef

The antiphospholipid antibodies in stroke study (APASS) group (1993) Anticardiolipin antibodies are an independent risk factor for first ischemic stroke. Neurology 43:2069–2073CrossRef

Brey RL, Stallworth CL, McGlasson DL, Wozniak MA, Wityk RJ, Stern BJ, Sloan MA, Sherwin R, Price TR, Macko RF, Johnson CJ, Earley CJ, Buchholz DW, Hebel JR, Kittner SJ (2002) Antiphospholipid antibodies and stroke in young women. Stroke 33:2396–2400PubMedCrossRef

Munts AG, van Genderen PJ, Dippel DW, van Kooten F, Koudstaal PJ (1998) Coagulation disorders in young adults with acute cerebral ischaemia. J Neurol 245:21–25PubMedCrossRef

10.

Brey RL, Abbott RD, Curb JD, Sharp DS, Ross GW, Stallworth CL, Kittner SJ (2001) Beta(2)-glycoprotein 1-dependent anticardiolipin antibodies and risk of ischemic stroke and myocardial infarction: the Honolulu heart program. Stroke 32:1701–1706PubMedCrossRef

11.

Janardhan V, Wolf PA, Kase CS, Massaro JM, D’Agostino RB, Franzblau C, Wilson PW (2004) Anticardiolipin antibodies and risk of ischemic stroke and transient ischemic attack: the Framingham Cohort and Offspring Study. Stroke 35:736–741PubMedCrossRef

12.

Nojima J, Kuratsune H, Suehisa E, Kitani T, Iwatani Y, Kanakura Y (2004) Strong correlation between the prevalence of cerebral infarction and the presence of anti-cardiolipin/beta2-glycoprotein I and anti-phosphatidylserine/prothrombin antibodies-co-existence of these antibodies enhances ADP-induced platelet activation in vitro. Thromb Haemost 91:967–976PubMed

13.

Pierangeli SS, Harris EN (2003) Probing antiphospholipid-mediated thrombosis: the interplay between anticardiolipin antibodies and endothelial cells. Lupus 12:539–545PubMedCrossRef

14.

Lonnebakken MT, Gerdts E (2008) Libman–Sacks endocarditis and cerebral embolization in antiphospholipid syndrome. Eur J Echocardiogr 9:192–193PubMedCrossRef

15.

Lockshin M, Tenedios F, Petri M, McCarty G, Forastiero R, Krilis S, Tincani A, Erkan D, Khamashta MA, Shoenfeld Y (2003) Cardiac disease in the antiphospholipid syndrome: recommendations for treatment. Committee consensus report. Lupus 12:518–523PubMedCrossRef

16.

Williamson JM, Dalton RS, Chester JF (2008) Popliteal venous aneurysm causing pulmonary embolism and paradoxical embolisation in a patient with antiphospholipid syndrome. Eur J Vasc Endovasc Surg 36:227–229PubMedCrossRef

17.

Okura H, Tomon M, Nishiyama S, Yoshikawa T (2000) Patent foramen ovale and “Catastrophic” Antiphospholipid syndrome. Intern Med 39:83PubMedCrossRef

18.

Ago T, Ooboshi H, Kitazono T, Imamura T, Takada J, Ibayashi S, Iida M (2004) Brain infarction associated with antiphospholipid antibody syndrome caused by paradoxical embolism through patent foramen ovale. J Neurol 251:757–759PubMedCrossRef

19.

Thompson T, Evans W (1930) Paradoxical embolism. Q J Med 23:135–137CrossRef

20.

Meissner I, Whisnant JP, Khandheria BK, Spittell PC, O’Fallon WM, Pascoe RD, Enriquez-Sarano M, Seward JB, Covalt JL, Sicks JD, Wiebers DO (1999) Prevalence of potential risk factors for stroke assessed by transesophageal echocardiography and carotid ultrasonography: the SPARC study. Stroke prevention: assessment of risk in a community. Mayo Clin Proc 74:862–869PubMedCrossRef

21.

Mas JL, Arquizan C, Lamy C, Zuber M, Cabanes L, Derumeaux G, Coste J (2001) Recurrent cerebrovascular events associated with patent foramen ovale, atrial septal aneurysm, or both. N Engl J Med 345:1740–1746PubMedCrossRef

22.

Bonati LH, Kessel-Schaefer A, Linka AZ, Buser P, Wetzel SG, Radue EW, Lyrer PA, Engelter ST (2006) Diffusion-weighted imaging in stroke attributable to patent foramen ovale: significance of concomitant atrial septum aneurysm. Stroke 37:2030–2034PubMedCrossRef

23.

Fujimoto S, Toyoda K, Jinnouchi J, Yasaka M, Kitazono T, Okada Y (2011) Differences in diffusion-weighted image and transesophageal echocardiographical findings in cardiogenic, paradoxical and aortogenic brain embolism. Cerebrovasc Dis 32:148–154PubMedCrossRef

24.

Ueno Y, Shimada Y, Tanaka R, Miyamoto N, Tanaka Y, Hattori N, Urabe T (2010) Patent foramen ovale with atrial septal aneurysm may contribute to white matter lesions in stroke patients. Cerebrovasc Dis 30:15–22PubMedCrossRef

25.

Botto N, Spadoni I, Giusti S, Ait-Ali L, Sicari R, Andreassi MG (2007) Prothrombotic mutations as risk factors for cryptogenic ischemic cerebrovascular events in young subjects with patent foramen ovale. Stroke 38:2070–2073PubMedCrossRef

26.

Iguchi Y, Kimura K, Kobayashi K, Ueno Y, Inoue T (2006) Ischaemic stroke with malignancy may often be caused by paradoxical embolism. J Neurol Neurosurg Psychiatry 77:1336–1339PubMedCrossRef

27.

Oku K, Atsumi T, Bohgaki M, Amengual O, Kataoka H, Horita T, Yasuda S, Koike T (2009) Complement activation in patients with primary antiphospholipid syndrome. Ann Rheum Dis 68:1030–1035PubMedCrossRef

28.

Adams HP Jr, Bendixen BH, Kappelle LJ, Biller J, Love BB, Gordon DL, Marsh EE 3rd (1993) Classification of subtype of acute ischemic stroke. Definitions for use in a multicenter clinical trial. TOAST Trial of Org 10172 in Acute Stroke Treatment. Stroke 24:35–41PubMedCrossRef

29.

Lechat P, Mas JL, Lascault G, Loron P, Theard M, Klimczac M, Drobinski G, Thomas D, Grosgogeat Y (1988) Prevalence of patent foramen ovale in patients with stroke. N Engl J Med 318:1148–1152PubMedCrossRef

30.

Moon RE, Camporesi EM, Kisslo JA (1989) Patent foramen ovale and decompression sickness in divers. Lancet 1:513–514PubMedCrossRef

31.

Cariou R, Tobelem G, Soria C, Caen J (1986) Inhibition of protein C activation by endothelial cells in the presence of lupus anticoagulant. N Engl J Med 314:1193–1194PubMedCrossRef

32.

Simantov R, LaSala JM, Lo SK, Gharavi AE, Sammaritano LR, Salmon JE, Silverstein RL (1995) Activation of cultured vascular endothelial cells by antiphospholipid antibodies. J Clin Invest 96:2211–2219PubMedCrossRef

33.

Matsuura E, Lopez LR (2008) Autoimmune-mediated atherothrombosis. Lupus 17:878–887PubMedCrossRef

34.

Rajamani K, Chaturvedi S, Jin Z, Homma S, Brey RL, Tilley BC, Sacco RL, Thompson JL, Mohr JP, Levine SR (2009) Patent foramen ovale, cardiac valve thickening, and antiphospholipid antibodies as risk factors for subsequent vascular events: the PICSS-APASS study. Stroke 40:2337–2342PubMedCrossRef

35.

Dodge SM, Hassell K, Anderson CA, Keller J, Groves B, Carroll JD (2004) Antiphospholipid antibodies are common in patients referred for percutaneous patent foramen ovale closure. Catheter Cardiovasc Interv 61:123–127PubMedCrossRef

36.

Lamy C, Giannesini C, Zuber M, Arquizan C, Meder JF, Trystram D, Coste J, Mas JL (2002) Clinical and imaging findings in cryptogenic stroke patients with and without patent foramen ovale: the PFO-ASA study. Atrial septal aneurysm. Stroke 33:706–711PubMedCrossRef

37.

Rigatelli G (2007) Patent foramen ovale: the evident paradox between the apparently simple treatment and the really complex pathophysiology. J Cardiovasc Med (Hagerstown) 8:300–304CrossRef

38.

Berthet K, Lavergne T, Cohen A, Guize L, Bousser MG, Le Heuzey JY, Amarenco P (2000) Significant association of atrial vulnerability with atrial septal abnormalities in young patients with ischemic stroke of unknown cause. Stroke 31:398–403PubMedCrossRef

39.

Aguilar JA, Summerson C (2000) Intracardiac thrombus in antiphospholipid antibody syndrome. J Am Soc Echocardiogr 13:873–875PubMedCrossRef

40.

Coppock MA, Safford RE, Danielson GK (1988) Intracardiac thrombosis, phospholipid antibodies, and two-chambered right ventricle. Br Heart J 60:455–458PubMedCrossRef

41.

Rigatelli G, Aggio S, Cardaioli P, Braggion G, Giordan M, Dell’avvocata F, Chinaglia M, Roncon L, Chen JP (2009) Left atrial dysfunction in patients with patent foramen ovale and atrial septal aneurysm: an alternative concurrent mechanism for arterial embolism. JACC Cardiovasc Interv 2:655–662PubMedCrossRef

Title: Patent foramen ovale and atrial septal aneurysm can cause ischemic stroke in patients with antiphospholipid syndrome
Authors: Yasutaka Tanaka
Yuji Ueno
Nobukazu Miyamoto
Yoshiaki Shimada
Ryota Tanaka
Nobutaka Hattori
Takao Urabe
Publication date: 01-01-2013
Publisher: Springer-Verlag
Published in: Journal of Neurology / Issue 1/2013
Print ISSN: 0340-5354
Electronic ISSN: 1432-1459
DOI: https://doi.org/10.1007/s00415-012-6613-4

Keynote webinar | Spotlight on sleep in brain health

Springer Medicine

Patent foramen ovale and atrial septal aneurysm can cause ischemic stroke in patients with antiphospholipid syndrome

Abstract

Keynote webinar | Spotlight on sleep in brain health

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 1/2013

Hypertrophic olivary degeneration on magnetic resonance imaging in mitochondrial syndromes associated with POLG and SURF1 mutations

Cognitive and MRI correlates of orthostatic hypotension in Parkinson’s disease

Sativex long-term use: an open-label trial in patients with spasticity due to multiple sclerosis

A novel mutation I215V in the PRNP gene associated with Creutzfeldt–Jakob and Alzheimer’s diseases in three patients with divergent clinical phenotypes

Prevalence, timing, risk factors, and mechanisms of anterior cerebral artery infarctions following subarachnoid hemorrhage

Communications of the European Neurological Society