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Thromb Haemost 2001; 85(01): 22-29
DOI: 10.1055/s-0037-1612658
DOI: 10.1055/s-0037-1612658
Review Article
Stroke in Young Adults: The Role of Paradoxical Embolism
Further Information
Publication History
Received
22 July 1999
Accepted after resubmission
03 August 2000
Publication Date:
08 December 2017 (online)
Summary
Stroke in young adults may be devastating and frequently no cause can be found. However, there is ample literature to suggest an association between cryptogenic stroke in young people and paradoxical embolisation via a venous to arterial circulation shunt (v-aCS), commonly due to patent foramen ovale (PFO). Although paradoxical embolisation is assumed to be a rare event, this review suggests that it is an important or even dominant cause of stroke in young people and that a transcranial Doppler (TCD) technique may be the investigation of choice to identify v-aCS.
Appendix I, II on pp. 26-7
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References
- 1 Petitti D, Sidney S, Quesenberry C, Bernstein A. Incidence of stroke and myocardial infarction in women of reproductive age. Stroke 1997; 28: 280-3.
- 2 Kristensen B, Malm J, Carlberg B, Stegmayr B, Backman C, Fagerlund M, Olsson T. Epidemiology and etiology of ischaemic stroke in young adults aged 18 to 44 years in northern Sweden. Stroke 1997; 28: 1702-9.
- 3 Rosendaal FR. Thrombosis in the young: Epidemiology and risk factors. A focus on venous thrombosis. Thromb Haemost 1997; 78: 1-6.
- 4 Chimowitz MI. Ischaemic stroke in the young. In: Primer on Cerebrovascular Diseases. Welch K, Caplan L, Reis D, Siesjo B, Weir B. eds. San Diego: Academic Press; 1997: 330-3.
- 5 Corrin B. Paradoxical embolism. Br Heart J 1964; 26: 549-53.
- 6 Moodie DS. Adult congenital heart disease. Current Science 1994; 137-42.
- 7 Movsowitz C, Podolsky LE, Meyerowitz CB, Jacobs LE, Kotler MN. Patent Foramen Ovale: A Nonfunctional Embry ological Remnant or a Potential Cause of Significant Pathology? (Review). J Am Soc Echo 1992; 5: 259-70.
- 8 Mas JL. Patent foramen ovale, atrial septal aneurysm and ischemic stroke in young adults. Eur Heart J 1994; 15: 446-9.
- 9 Falk RH. PFO or UFO? The role of a patent foramen ovale in cryptogenic stroke. Am Heart J 1991; 121: 1264-6.
- 10 Frisoni G, Monda VD, Bariselli M. Stroke due to paradoxical embolism. Ital J Neurol Sci 1990; 11: 61-4.
- 11 Martin G, Davis R. Paradoxical embolism. Journal of the Tennessee Medical Association 1995; March 103-4.
- 12 Aburahma A. Work up and management of patients with paradoxical emboli. The West Virginia Medical Journal 1996; 92: 260-4.
- 13 Lang I, Steurer G, Weissel M, Burbhuber O. Recurrent paradoxical embolism complicating severe thromboembolic pulmonary hypertension. Eur Heart J 1988; 9: 678-81.
- 14 Hull DH, Hirsh J, Carter CJ, Jay RM, Dodd PE, Ockleford PA, Coates G, Gill GJ, Turpie AG, Doyle DJ, Buller HR, Raskob GE. Pulmonary angiography, ventilation lung scanning and venography for clinically suspected pulmonary embolism and abnormal perfusion lung scan. Ann Int Med 1983; 98: 891-9.
- 15 Schminke U, Ries S, Daffertshofer M, Staedt U, Hennerici M. Patent Foramen Ovale: A Potential Source of Cerebral Embolism?. Cerebrovasc Dis 1995; 5: 133-8.
- 16 Warlow C, Ogston D, Douglas A. Deep venous thrombosis of the legs after strokes. Part 1. Incidence and predisposing factors. BMJ 1976; 1: 1178-81.
- 17 Stollberger C, Slany J, Schuster I, Leitner H, Winkler W-B, Karnik R. The prevalence of deep venous thrombosis in patients with suspected paradoxical embolism. Ann Int Med 1993; 119: 461-5.
- 18 Turpie A, Levine M, Hisch J, Carter C, Jay R, Powers P, Andrew M, Magnani HN, Hull RD, Gent M. Double blind randomised trial of ORG 10172 low molecular weight heparinoid in prevention of deep-vein thrombosis in thrombotic stroke. Lancet 1987; 1: 523-6.
- 19 McCarthy S, Turner J, Robertson D, Hawkey C, Macey D. Low dose heparin as a prophylaxis against deep-vein thrombosis after acute stroke. Lancet 1977; 2: 800-1.
- 20 Cramer S, Rordorf G, Kaufman J, Buonanno F, Koroshetz W, Schwamm L. Clinically occult pelvic vein thrombosis in cryptogenic stroke. Lancet 1998; 351: 1927-8.
- 21 Gilon D. Patent Foramen Ovale and Paradoxical Emboli as a Possible Mechanism of Stroke in Patients with Low FEV1. Stroke 1996; 27: 1920.
- 22 Konstantinides S, Geibel A, Kasper W, Olschewski M, Blumel L, Just H. Patent foramen ovale is an important predictor of adverse outcome in patients with major pulmonary embolism. Circulation 1998; 97: 1946-51.
- 23 Hagen PT, Scholz DG, Edwards WD. Incidence and size of patent foramen ovale during the first 10 decades of life: and autopsy study of 965 normal hearts. Mayo Clin Proc 1984; 59: 17-20.
- 24 Patten B. The closure of the foramen ovale. Am J Anat 1931; 48: 19-44.
- 25 Di Tullio M, Sacco RL, Massaro A, Venketasubramanian N, Sherman D, Hoffman M, Mohr JP, Homma S. Transcranial Doppler with contrast injection for the detection of patent foramen ovale in stroke patients. Int J Card Imag 1993; 9: 1-5.
- 26 Meissner I, Whisnant JP, Khandheria BK, Spittell PC, O’Fallon WM. et al. Prevalence of potential risk factors for stroke assessed by transoesophageal echocardiography and carotid ultrasonography: the SPARC Study. Mayo Clin Proc 1999; 74: 862-9.
- 27 Teague SM, Sharma MK. Detection of Paradoxical Cerebral Echo Contrast Embolization by Transcranial Doppler Ultrasound. Stroke 1991; 22: 740-5.
- 28 Jauss M, Kaps M, Keberle M, Haberbosch W, Dorndorf M. A Comparison of Transesophageal Echocardiography and Transcranial Doppler Sonography with Contrast Medium for Detection of Patent Foramen Ovale. Stroke 1994; 25: 1265-7.
- 29 Job F, Ringelstein E, Grafen Y, Flachskampf F, Doherty C, Stockmanns A, Hanrath P. Comparison of transcranial contrast Doppler sonography and transesophageal contrast echocardiography for the detection of patent foramen ovale in young stroke patients. Am J Cardiol 1994; 74: 381-4.
- 30 Droste DW, Reisener M, Kemeny V, Dittrich R, Schulte-Altedorneburg G, Stypmann J, Wichter T, Ringelstein EB. Contrast Transcranial Doppler Ultrasound in the Detection of Right-to-Left Shunts. Reproducibility, Comparison of 2 Agents, and Distribution of Microemboli. Stroke 1999; 30: 1014-8.
- 31 Zanette E, Mancini G, De Castro S, Solaro M, Cartoni D, Chiarotti F. Patent Foramen Ovale and Transcranial Doppler: Comparison of Different Procedures. Stroke 1996; 27: 2251-5.
- 32 Schwarze J, Sander D, Kukla C, Wittich I, Babikian V, Klingelhofer J. Methodological parameters influence the detection of right to left shunts by contrast transcranial Doppler ultrasonography. Stroke 1999; 30: 1234-9.
- 33 Stoddard MF, Keedy DL, Dawkins PR. The cough test is superior to the Valsalva maneuver in the deliniation of right-to-left shunting through a patent foramen ovale during contrast transesophageal echocardiography. Am Heart J 1993; 125: 185-9.
- 34 Cujec B, Polasek P, Voll C, Shuaib A. Transesophageal Echocardiography in the Detection of Potential Cardiac Source of Embolism in Stroke Patients. Stroke 1991; 22: 727-733.
- 35 Lee RJ, Bartzokis T, Yeoh TK, Grogin HR, Choi D. Schnittger Enhanced Detection of Intracardiac Sources of Cerebral Emboli by Transesophageal Echocardiography. Stroke 1991; 22: 734-9.
- 36 Pearson AC, Labovitz AJ, Tatineni S, Gomez CR. Superiority of Transesophageal Echocardiography in Detection Cardiac Source of Embolism in Patients with Cerebral Ischemia of Uncertain Etiology. JACC 1991; 17: 66-72.
- 37 DeRook FA, Comess KA, Albers GW, Popp RL. Transesophageal Echocardiography in the Evaluation of Stroke. Ann Int Med 1992; 117: 922-31.
- 38 Zhao BW, Mizushige K, Xian TC, Matsuo H. Incidence and clinical significance of interatrial shunting in patients with atrial septal aneurysm detected by contrast transesophageal echocardiography. Angiology 1999; 50: 745-53.
- 39 Leung DY, Black IW, Cranney GB, Walsh WF, Grimm RA, Stewart WJ, Thomas JD. Selection of Patients for Transesophageal Echocardiography After Stroke and Systemic Embolic Events. Stroke 1995; 26: 1820-4.
- 40 Kuhl HP, Hoffmann R, Merx MW, Franke A, Klotzsch C, Lepper W, Reineke T. et al. Transthoracic echocardiography using second harmonic imaging. Diagnostic alternative to transesophageal echocardiography for the detection of atrial right to left shunt in patients with cerebral embolic events. JACC 1999; 34: 1823-9.
- 41 Venketasubramanian N, Sacco RL, Tullio MD, Sherman D, Homma S, Mohr JP. Vascular distribution of paradoxical emboli by transcranial Doppler. Neurology 1993; 43: 1533-5.
- 42 Anzola G, Renaldini E, Magoni M, Costa A, Cobelli M, Guindani M. Validation of Transcranial Doppler Sonography in the Assessment of Patent Foramen Ovale. Cerebrovasc Dis 1995; 5: 194-8.
- 43 Droste DW, Kriete J-U, Stypmann J, Castrucci M, Wichter T, Tietje R, Weltermann B, Young P, Ringelstein EB. Contrast Transcranial Doppler Ultrasound in the Detection of Right-to-Left Shunts. Comparison of Different Procedures and Different Contrast Agents. Stroke 1999; 30: 1827-32.
- 44 Klotzsch C, Janssen G, Berlit P. Transesophageal echocardiography and contrast-TCD in the detection of a patent foramen ovale: Experiences with 111 patients. Neurology 1994; 44: 1603-1606.
- 45 Di Tullio M, Sacco RL, Gopal A, Mohr JP. Patent Foramen Ovale as a Risk Factor for Cryptogenic Stroke. Ann Int Med 1992; 117: 461-5.
- 46 Tong DC, Albers GW. Transcranial Doppler-Detected Microemboli in Patients with Acute Stroke. Stroke 1995; 26: 1588-92.
- 47 Di Tullio M, Sacco RL, Venketasubramanian N, Sherman D, Mohr JP, Homma S. Comparison of Diagnostic Techniques for the Detection of a Patent Foramen Ovale in Stroke Patients. Stroke 1993; 24: 1020-4.
- 48 Itoh T, Matsumoto M, Handa N, Maeda H, Hougaku H, Tsukamoto Y, Tanouchi J, Kamada T. Paradoxical Embolism as a Cause of Ischemic Stroke of Uncertain Etiology. Stroke 1994; 25: 771-5.
- 49 Van Camp G, Schulze D, Cosyns B, Vandenbossche JL. Relation between Patent Foramen Ovale and Unexplained Stroke. Am J Cardiol 1993; 71: 596-8.
- 50 Homma S, Di Tullio MR, Sacco RL, Mihalatos D, Mandri GL, Mohr JP. Characteristics of Patent Foramen Ovale Associated with Cryptogenic Stroke. Stroke 1994; 25: 582-6.
- 51 Hausmann D, Mugge A, Danial WG. Identification of Patent Foramen Ovale Permitting Paradox Embilism. JACC 1995; 26: 1030-7.
- 52 Steiner MM, Di Tullio MR, Rundeck T, Gan R, Chen X, Liguori C, Brainin M, Homma S, Sacco RL. Patent Foramen Ovale Size and Embolic Brain Imaging Findings Among Patients with Ischemic Stroke. Stroke 1998; 29: 944-8.
- 53 Serena J, Segura T, Perez-Ayuso M, Bassaganyas J, Molins A, Davalos A. The need to quantify right to left shunt in acute ischaemic stroke. A case control study. Stroke 1998; 29: 1322-8.
- 54 Louie EK, Konstadt SN, Rao TLK, Scanlon PJ. Transesophageal Echo-cardiographic Diagnosis of Right to Left Shunting Across the Foramen Ovale in Adults Without Prior Stroke. JACC 1993; 21: 1231-6.
- 55 Roijer A, Lindgren A, Rudling O, Wallins L, Olsson SB, Johansson BB, Eskilsson J. Potential cardioembolic sources in an elderly population without stroke – A transthoracic and transoesophageal echocardiographic study in randomly selected volunteers. Eur Heart J 1996; 17: 1103-11.
- 56 Ranoux D, Cohen A, Cabanes L, Amarenco P, Bousser MG, Mas JL. Patent Foramen Ovale: Is Stroke due to Paradoxical Embolism?. Stroke 1993; 24: 31-4.
- 57 Mas JL, Zuber M. Recurrent cerebrovascular events in patients with patent foramen ovale, atrial septal aneurysm or both, and cryptogenic stroke or transient ischemic attack. Am Heart J 1995; 130: 1083-8.
- 58 Bogousslavsky J, Garazi S, Jeanrenaud X, Aebischer N, Melle GV. Stroke recurrence in patients with patent foramen ovale: The Lausanne Study. Neurol 1996; 1301-5.
- 59 Bridges ND, Hellenbrand W, Latson L, Filiano J, Newburger JW, Lock JE. Transcatheter Closure of Patent Foramen Ovale after Presumed Paradoxical Embolism. Circulation 1992; 86: 1902-8.
- 60 Devuyst G, Bogousslavsky J, Ruchat P, Jeanrenaud X, Despland PA, Regli F, Aebischer N, Karpuz HM, Castillo V, Guffi M, Sadeghi H. Prognosis after stroke followed by surgical closure of patent foramen ovale: A prospective follow-up study with brain MRI and simultaneous transesophageal and transcranial Doppler ultrasound. Neurology 1996; 47: 1162-6.
- 61 Homma S, Di Tullio MR, Sacco RL, Sciacca RR, Smith C, Mohr JP. Surgical closure of patent foramen ovale in cryptogenic stroke patients. Stroke 1997; 28: 2376-81.
- 62 Chatterjee T, Aeschbacher B, Meier B. Ischaemic attacks and patent foramen ovale: Transcatheter closure of patent foramen ovale in adults with cryptogenic systemic embolism. J Int Cardiol 1999; 12: 59-64.
- 63 Dhillon R, Thanopoulos B, Tsaousis G, Triposkiadis F, Kyriakidis M, Redington A. Transcatheter closure of atrial septal defects in adults with the Amplatzer septal occluder. Heart 1999; 82: 559-62.
- 64 Dearani JA, Baran S, Ugurlu MD, Gordon K, Danielson MD, Daly RC, McGregor CGA. et al. Surgical patent foramen ovale closure for prevention of paradoxical embolism-related cerebrovascular ischemic events. Circulation 1999; 100 suppl II II-171-II-175.
- 65 Hoepp HW, Deutsch JH, La Rosee K, Schnabel P, Terhaggen G, Schneider CA, Korsten J, Babic UU. Transcatheter closure of atrial-septal defects and patent foramen ovale in adults: optimal anatomic adaptation of occlusion device. Am H J 1999; 138: 941-9.
- 66 Chan KC, Godman MJ, Walsh K, Wilson N, Redington A, Gibbs JL. Transcatheter closure of atrial septal defect and interatrial communications with a new self expanding nitinol double disc device (Amplatzer septal occluder): multicentre UK experience. Heart 1999; 82: 300-6
- 67 Chambers J. Should percutaneous devices be used to close a patent foramen ovale after cerebral infarction or TIA?. Heart 1999; 82: 537-8.
- 68 Nendaz M, Sarasin F, Junod A, Bogousslavsky J. Preventing stroke recurrence in patients with patent foramen ovale: Antithrombotic therapy, foramen closure, or therapeutic abstention? A decision analytic perspective. Am Heart J 1998; 135: 532-41.
- 69 Anand SS, Yusuf S. Oral anticoagulant therapy in patients with coronary artery disease: A meta-analysis. JAMA 1999; 282: 2058-65.
- 70 World Health Organisation Scientific Group. World Health Organisation Scientific Group Meeting on Cardiovascular Disease and Steroid Hormone Contraceptives: Summary of Conclusions. Weekly Epidemiology Record 1997; 48: 361-3.
- 71 Cabanes L, Mas J, Cohen A, Amarenco P, Cabanes P, Oubaru P, Chedru F, Guerin F, Bousser M, Recondo JD. 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: 1865-73.
- 72 Nighoghossian N, Perinetti M, Barthelet M, Adeleine P. Trouillas Transesophageal echocardiography in patients less than 60 years of age without obvious cardiac source of embolism. Neurol Res 1995; 17: 368-72.
- 73 Besson G, Bogousslavsky J, Hommel M, Stauffer JC, Siche JP. Patent foramen ovale in young stroke patients with mitral valve prolapse. Acta Neurol Scand 1994; 89: 23-6.
- 74 Cross J, Castro P, Jennet W. Cerebral strokes associated with pregnancy and the puerperium. BMJ 1968; n: 214-8.
- 75 Kittner SJ, Stern BJ, Feeser BR, Hebel JR, Nagey DA, Buchholz D, Earley CJ, Johnson CJ, Macho RF, Slone MA, Wityk RJ, Wozniak MA, Price TR, Sherwin R. Pregnancy and the risk of stroke. New Eng J Med 1996; 335: 768-74.
- 76 Longstreth WT, Rosendaal FR, Siscovick DS, Vos HL, Schwartz SM, Psaty BM, Raghunathen TE, Koepsell TD, Reitsma PH. Risk of stroke in young women and two prothrombotic mutations: factor V Leiden and prothrombin gene variant (G20210A). Stroke 1998; 29: 577-80.
- 77 Zenz W, Bodo Z, Plotho J, Streif W, Male C, Bernert G, Rauter L, Ebetsberger G, Kaltenbrunner K, Kurnik P, Lischka A, Paky F, Ploier R, Hofler G, Mannhalter C, Muntean W. Factor V Leiden and prothrombin gene G 20210 A variant in children with ischemic stroke. Thromb Haemost 1998; 80: 763-6.
- 78 Jones EJ, Calafiore P, Donnan GA, Tonkin AM. Evidence that patent foramen ovale is not a risk factor for cerebral ischaemia in the elderly. Am J Cardiol. 1994; 74: 596-9.
- 79 Harvey JR, Teague SM, Anderson JL, Voyles WF, Thadani U. Clinically silent atrial septal defects with evidence for cerebral embolization. Ann Int Med. 1986; 105: 695-7.
- 80 Webster MWI, Chancellor AM, Smith HJ, Swift D, Sharpe D, Bass N. Patent foramen ovale in young stroke patients. Lancet 1988; July 2 11-2.
- 81 de Belder MA, Tourikis L, Leech G, Camm AJ. Risk of patent foramen ovale for thromboembolic events in all age groups. Am J Cardiol. 1992; 69: 1316-20.
- 82 Chen W, Lin S, Cheng J, Lein W. The frequency of patent foramen ovale in patients with ischemic stroke: A transesophageal echocardiographic study. Journal of the Formosan Medical Association. 1991; 90: 744-8.
- 83 Rauh G, Fischereder M, Spengel FA. Transesophageal echocardiography in patients with focal cerebral ischemia of unknown cause. Stroke 1995; 27: 691-4.
- 84 Luotolahti M, Saraste M, Hartiala J. Saline contrast and colour Doppler transoesophageal echocardiography in detecting a patent foramen ovale and right-to-left shunts in stroke patients. Clinical Physiology. 1995; 15: 265-73.
- 85 Lechat P, Mas JL, Lascault G, Loron P, Theard M, Klimczac M, Drobinski G, Thomas D, Grosgogeat Y. Prevalence of patent foramen ovale in patients with stroke. New Eng J Med. 1988; 318: 1148-52.
- 86 Vella MA, Sulke AN, Rodrigues CA, McNabb WR, Lewis RR. Patent foramina ovale in elderly stroke patients. Postgraduate Medical Journal. 1991; 67: 745-6.