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Heart, Lung and Circulation

Ischaemic Stroke and the Echocardiographic “Bubble Study”: Are We Screening the Right Patients?

  • Author Footnotes
    1 This author takes responsibility for all aspects of the reliability and freedom from bias of the data presented and their discussed interpretation.
    Paul Maggiore
    Correspondence
    Corresponding author at: Department of Cardiology, Sir Charles Gairdner Hospital, Hospital Avenue, Nedlands WA 6009, Australia. Tel.: +61 086457 3333.
    Footnotes
    1 This author takes responsibility for all aspects of the reliability and freedom from bias of the data presented and their discussed interpretation.
    Affiliations
    Department of Cardiology, Sir Charles Gairdner Hospital, Perth, WA, Australia
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    1 This author takes responsibility for all aspects of the reliability and freedom from bias of the data presented and their discussed interpretation.
    Jamie Bellinge
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    1 This author takes responsibility for all aspects of the reliability and freedom from bias of the data presented and their discussed interpretation.
    Affiliations
    Department of Cardiology, Royal Perth Hospital, Perth, WA, Australia
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    1 This author takes responsibility for all aspects of the reliability and freedom from bias of the data presented and their discussed interpretation.
    David Chieng
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    1 This author takes responsibility for all aspects of the reliability and freedom from bias of the data presented and their discussed interpretation.
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    Department of Cardiology, Sir Charles Gairdner Hospital, Perth, WA, Australia
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    David White
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    1 This author takes responsibility for all aspects of the reliability and freedom from bias of the data presented and their discussed interpretation.
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    Department of Cardiology, Royal Perth Hospital, Perth, WA, Australia
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    Nick S.R. Lan
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    Department of Cardiology, Fiona Stanley Hospital, Perth, WA, Australia
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    Biyanka Jaltotage
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    Department of Cardiology, Fiona Stanley Hospital, Perth, WA, Australia
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    Umar Ali
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    1 This author takes responsibility for all aspects of the reliability and freedom from bias of the data presented and their discussed interpretation.
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    Department of Cardiology, Fiona Stanley Hospital, Perth, WA, Australia
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    Madeleine Gordon
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    Department of Cardiology, Fiona Stanley Hospital, Perth, WA, Australia
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    Kevin Chung
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    Department of Cardiology, Sir Charles Gairdner Hospital, Perth, WA, Australia
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    Paul Stobie
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    Department of Cardiology, Sir Charles Gairdner Hospital, Perth, WA, Australia
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    Justin Ng
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    Department of Cardiology, Sir Charles Gairdner Hospital, Perth, WA, Australia
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    Graeme J. Hankey
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    Department of Neurology, Sir Charles Gairdner Hospital, Perth, WA, Australia

    University of Western Australia School of Medicine, WA, Australia
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    Brendan McQuillan
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    1 This author takes responsibility for all aspects of the reliability and freedom from bias of the data presented and their discussed interpretation.
    Affiliations
    Department of Cardiology, Sir Charles Gairdner Hospital, Perth, WA, Australia

    University of Western Australia School of Medicine, WA, Australia
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    1 This author takes responsibility for all aspects of the reliability and freedom from bias of the data presented and their discussed interpretation.
Published:August 01, 2018DOI:https://doi.org/10.1016/j.hlc.2018.07.007

      Background

      Patent foramen ovale (PFO) is a potential mechanism for paradoxical embolism in cryptogenic ischaemic stroke or transient ischaemic attack (TIA). PFO is typically demonstrated with agitated saline (“bubble study”, BS) during echocardiography. We hypothesised that the BS is frequently requested in patients that have a readily identifiable cause of stroke, that any PFO detected is likely incidental, and its detection often does not alter management.

      Methods

      This was a retrospective observational study of patients with recent ischaemic stroke/TIA referred for a BS. Patient demographics, stroke risk factors, vascular/cerebral imaging results and transoesophageal echocardiogram (TOE) reports were recorded. A “modified” Risk of Paradoxical Embolism (RoPE) score was calculated. Change in management was defined as antiplatelet/anticoagulant therapy alteration or referral for PFO closure. Bubble Study complications were recorded.

      Results

      Among 715 patients with ischaemic stroke/TIA referred for a BS, 8.7% had atrial fibrillation and 9.2% had carotid stenosis ≥70%. At least three stroke risk factors were present in 39.3% and only 47.1% of patients screened had a “modified” RoPE score of >5. A PFO was detected in 248 patients of whom only 31% (77/248) had a subsequent change in management. Of BS performed, 1/924 patients (0.1%) suffered a TIA as a complication.

      Conclusions

      The echocardiographic BS is frequently performed in patients that have a readily identifiable cause of stroke and whose PFO unlikely relates to the stroke/TIA. Bubble Study findings resulted in a change in management in the minority. The procedure is safe but the complication rate warrants informed consent.

      Keywords

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      References

        • Tullio M.D.
        Patent foramen ovale: echocardiographic detection and clinical relevance in stroke.
        J Am Soc Echocardiogr. 2010; 23: 144-155
        • Meissner I.
        • Whisnant J.
        • Khandheria B.
        • Spittell P.
        • O’Fallon W.
        • Pascoe R.D.
        • et al.
        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. 1999; 74: 862-869
        • Penther P.
        Patent foramen ovale: an anatomical study. Apropos of 500 consecutive autopsies.
        Arch Mal Coeur Vaiss. 1994; 87: 15-21
        • Schroeckenstein R.
        • Wasenda G.
        • Edwards J.
        Valvular competent patent foramen ovale in adults.
        Minn Med. 1972; 55
        • Hagen P.
        • Scholz D.
        • Edwards W.
        Incidence and size of patent foramen ovale during the first 10 decades of life: an autopsy study of 965 normal hearts.
        Mayo Clin Proc. 1984; 59: 17-20
        • Sweeney L.
        • Rosenquist G.
        The normal anatomy of the atrial septum in the human heart.
        Am Heart J. 1979; 98
        • Saver J.
        Cryptogenic Stroke.
        N Eng J Med. 2016; 374: 2065-2074
        • Lee B.
        • Nam H.S.
        • Heo J.
        • Kim D.
        Yonsei stroke registry. Analysis of 1,000 patients with acute cerebral infarctions.
        Cerebrovasc Dis. 2001; 12: 145
        • Kent D.
        • Ruthazer R.
        • Weimar C.
        • Mas J.
        • Serena J.
        • Homma S.
        • et al.
        An index to identify stroke-related vs incidental patent foramen ovale in cryptogenic stroke.
        Neurology. 2013; 81: 619-625
        • Overell J.
        • Bone I.
        • Lees K.
        Interatrial septal abnormalities and stroke: a meta-analysis of case-control studies.
        Neurology. 2000; 55: 1172-1179
        • Porter T.
        • Abdelmoneim S.
        • Belcik J.
        • McCulloch M.
        • Mulvagh S.
        • Olson J.
        • et al.
        Guidelines for the cardiac sonographer in the performance of contrast echocardiography: a focused update from the American society of echocardiography.
        J Am Soc Echocardiogr. 2014; 27: 797-810
        • Romero J.
        • Frey J.
        • Schwamm L.
        • Demaerschalk B.
        • Chaliki H.
        • Parikh G.
        • et al.
        Cerebral ischemic events associated with ‘bubble study’ for Identification of right to left shunts.
        Stroke. 2009; 40: 2343-2348
        • Carroll J.
        • Saver J.
        • Thaler D.
        • Smalling R.
        • Berry S.
        • MacDonald L.
        • et al.
        Closure of patent foramen ovale versus medical therapy after cryptogenic stroke.
        N Eng J Med. 2013; 368: 1092-1100
        • Furlan A.
        • Reisman M.
        • Massaro J.
        • Mauri L.
        • Adams H.
        • Albers G.
        • et al.
        Closure or medical therapy for cryptogenic stroke with patent foramen ovale.
        N Eng J Med. 2012; 336: 991-999
        • Meier B.
        • Kalesan B.
        • Mattle H.
        • Khattab A.
        • Hildick-Smith D.
        • Dudek D.
        • et al.
        Percutaneous closure of patent foramen ovale in cryptogenic embolism.
        N Eng J Med. 2013; 368: 1083-1091
        • Udell J.
        • Opotowsky A.
        • Khairy P.
        • Silversides C.
        • Gladstone D.
        • O’Gara P.
        • et al.
        Patent foramen ovale closure vs medical therapy for stroke prevention: meta-analysis of randomized trials and review of heterogeneity in meta-analyses.
        Can J Cardiol. 2014; 30: 1216-1224
        • Saver J.
        • Carroll J.
        • Thaler D.
        • Smalling R.
        • Macdonald L.
        • Marks D.
        • Tirschwell D.
        Long–term Outcomes of patent foramen ovale closure or medical therapy after stroke.
        N Eng J Med. 2017; 377: 1022-1032
        • Mas J.-L.
        • Derumeaux G.
        • Guillon B.
        • Massardier E.
        • Hosseini H.
        • Mechtouff L.
        • et al.
        Patent foramen ovale closure or anticoagulation vs. antiplatelets after stroke.
        N Eng J Med. 2017; 377: 1011-1021
        • Søndergaard L.
        • Kasner S.
        • Rhodes J.
        • Andersen G.
        • Iversen H.
        • Nielsen-Kudsk J.
        • et al.
        Patent foramen ovale closure or antiplatelet therapy for cryptogenic stroke.
        N Eng J Med. 2017; 377: 1033-1042
        • Messé S.
        • Gronseth G.
        • Kent D.
        • Kizer J.
        • Homma S.
        • Rosterman L.
        Practice advisory: recurrent stroke with patent foramen ovale (update of practice parameter) Report of the guideline development, dissemination, and implementation subcommittee of the American academy of neurology.
        Neurology. 2016; 87: 815-821
        • Adams H.
        • Bendixen B.
        • Kappelle L.
        • Biller J.
        • Love B.
        • Gordon D.
        • et al.
        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. 1993; 24: 35
        • Huang Y.-Y.
        • Shao B.
        • Ni X.-D.
        • Li J.-C.
        Differential lesion patterns on T2-weighted magnetic resonance imaging and fluid-attenuated inversion recovery sequences in cryptogenic stroke patients with patent foramen ovale.
        J Stroke Cerebrovasc Dis. 2014; 23: 1690-1695
        • Knauth M.
        • Ries S.
        • Pohimann S.
        • Kerby T.
        • Forsting M.
        • Daffertshofer M.
        Cohort study of multiple brain lesions in sport divers: role of a patent foramen ovale.
        BMJ. 1997; 314: 701-705
        • Ropper A.
        Tipping point for patent foramen ovale closure.
        N Eng J Med. 2017; 377: 1093-1095
        • Hart R.
        • Diener H.C.
        • Coutts S.
        • Easton J.
        • Granger C.
        • O’Donnell M.
        Embolic strokes of undetermined source: the case for a new clinical construct.
        Lancet Neurol. 2014; 13: 429-438
        • Tsivgoulis G.
        • Stamboulis E.
        • Sharma V.
        • Heliopoulos I.
        • Voumvourakis K.
        • Teoh H.
        • et al.
        Safety of transcranial Doppler ‘bubble study’ for identification of right to left shunts: an international multicentre study.
        J Neurol Neurosurg Psychiatry. 2011; 82: 1206-1208
        • Sorensen S.
        • Aguilar H.
        • Reichert W.
        • Goldstein M.
        • Thoen D.
        • Thomas H.
        Transient neurological symptoms during contrast transcranial Doppler right-to-left shunt testing in patients with cryptogenic neurological disease.
        J Interven Cardiol. 2010; 23: 284-290
        • Lechat P.
        • Mas J.
        • Lascault G.
        • Loron P.
        • Theard M.
        • Klimczac M.
        • et al.
        Prevalence of patent foramen ovale in patients with stroke.
        N Eng J Med. 1988; 318: 1148-1152
        • Webster M.
        • Chancellor A.
        • Smith H.
        • Swift D.
        • Sharpe D.
        • Bass N.
        • et al.
        Patent foramen ovale in young stroke patients.
        Lancet. 1988; 332: 11-12
        • Cabanes L.
        • Mas J.
        • Cohen A.
        • Amarenco P.
        • Cabanes P.
        • Oubary P.
        • et al.
        Atrial septal aneurysm and patent foramen ovale as risk factors for cryptogenic stroke in patients less than 55 years of age. A study using transesophageal echocardiography.
        Stroke. 1993; 24: 1865-1873
        • Belder M.D.
        • Tourikis L.
        • Leech G.
        • Camm A.
        Risk of patent foramen ovale for thromboembolic events in all age groups.
        Am J Cardiol. 1992; 1992: 1316-1320
        • Tullio M.D.
        • Sacco R.
        • Gopal A.
        • Mohr J.
        • Homma S.
        Patent foramen ovale as a risk factor for cryptogenic stroke.
        Ann Intern Med. 1992; 117: 461-465
        • Hausmann D.
        • Mugge A.
        • Becht I.
        • Daniel W.
        Diagnosis of patent foramen ovale by transesophageal echocardiography and association with cerebral and peripheral embolic events.
        Am J Cardiol. 1992; 70: 668-672
        • Handke M.
        • Harloff A.
        • Olschewski M.
        • Hetzel A.
        • Geibel A.
        Patent foramen ovale and cryptogenic stroke in older patients.
        N Eng J Med. 2007; 357: 2262-2268
        • Meissner I.
        • Khandheria B.K.
        • Heit J.
        • Petty G.
        • Sheps S.
        • Schwartz G.
        • et al.
        Patent foramen ovale: innocent or guilty? Evidence from a prospective population-based study.
        J Am Coll Cardiol. 2006; 47: 440-445