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The paradoxical embolism phenomenon in patients with embolic cryptogenic stroke

https://doi.org/10.14412/2074-2711-2020-1-13-21

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Abstract

Patent foramen ovale (PFO) is an important cause of embolic cryptogenic stroke (ECS) in young patients. The main mechanism in this case is paradoxical embolism (PE), the basis for which is a right-to-left (R-L) shunt.
Objective: to comparatively characterize patients who have undergone ECS, with and without an R-L shunt, as evidenced by transcranial Doppler with the bubble test (TCD-BT).
Patients and methods. In 40 patients with acute ECS, an R-L shunt was sought using TCD-BT, followed by transesophageal echocardiography (TEE). The left atrial volume index (LAVI) was additionally calculated. Brain damage was analyzed by probabilistic mapping of foci according to magnetic resonance imaging.
Results and discussion. The mean age of the examined patients was 51.5 (39.5–60.0) years; of them there were 22 women and 18 men. An RL shunt was detected in 24 (60.0%) of patients with cryptogenic embolism that was mainly grades 2 and 3 (41.0 and 35.0%). TEE could visualize PFO (1.0 to 5.5 mm in size) in 16 (40%) patients and atrial septal aneurysm in 3 (7.5%). PFO was not found in 5 patients with positive results of TCD-BT, which may suggest that there is either a pulmonary shunt or a false-negative TEE. The patients with an R-L shunt versus those without an R-L-shunt showed lower LAVIs (23.9 and 26.5 mL/m2) (p=0.016). This fact may additionally confirm the causative role of PFO in the development of stroke, whereas higher LAVIs in the non R-L shunt subgroup should alert to the presence of atrial cardiopathy and initiate an appropriate diagnostic search for latent atrial fibrillation. According to the presence or absence of an R-L shunt, the groups did not significantly differ in gender, age, and clinical characteristics of the stroke. In patients with PFO, a lesion focus was most commonly localized in the middle cerebral artery bed (35.3%), cerebellum (23.5%), and posterior cerebral artery (17.6%). Five (29.0%) patients were ascertained to have several foci of acute stroke. There was a trend towards the larger size of cerebral infarction foci and their specific localization in the vertebrobasilar bed in PE, which determined the high (35.3%) incidence of ataxia with the onset of the disease.
Conclusion. PE causes ECS in 60.0% of cases. The distinctive feature of patients with an R-L shunt is lower LAVIs and a trend towards the larger size of cerebral infarction foci and their specific localization in the vertebrobasilar bed.

About the Authors

S. A. Mekhryakov
City Clinical Hospital Four
Russian Federation
26, Petropavlovskaya St., Perm 614990



A. A. Kulesh
City Clinical Hospital Four; Acad. E.A. Vagner Perm State Medical University, Ministry of Health of Russia
Russian Federation

26, Petropavlovskaya St., Perm 614990;

2, Kim St., Perm 614107



E. A. Pokalenko
City Clinical Hospital Four; Acad. E.A. Vagner Perm State Medical University, Ministry of Health of Russia
Russian Federation

26, Petropavlovskaya St., Perm 614990;

2, Kim St., Perm 614107 



L. I. Syromyatnikova
City Clinical Hospital Four; Acad. E.A. Vagner Perm State Medical University, Ministry of Health of Russia
Russian Federation

26, Petropavlovskaya St., Perm 614990;

2, Kim St., Perm 614107 



S. P. Kulikova
Higher School of Economics
Russian Federation
20, Myasnitskaya St., Moscow 101000



V. E. Drobakha
City Clinical Hospital Four; Acad. E.A. Vagner Perm State Medical University, Ministry of Health of Russia
Russian Federation

26, Petropavlovskaya St., Perm 614990;

2, Kim St., Perm 614107 



V. V. Shestakov
Acad. E.A. Vagner Perm State Medical University, Ministry of Health of Russia
Russian Federation
2, Kim St., Perm 614107



Yu. V. Karakulova
Acad. E.A. Vagner Perm State Medical University, Ministry of Health of Russia
Russian Federation
2, Kim St., Perm 614107



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41. Woods TD, Patel A. A critical review of patent foramen ovale detection using saline contrast echocardiography: when bubbles lie. J Am Soc Echocardiogr. 2006 Feb;19(2):215-22.

42. Droste DW, Lakemeier S, Wichter T, et al. Optimizing the technique of contrast transcranial Doppler ultrasound in the detection of right-to-left shunts. Stroke. 2002 Sep;33(9): 2211-6.

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44. Johansson MC, Eriksson P, Guron CW, Dellborg M. Pitfalls in diagnosing PFO: characteristics of false-negative contrast injections during transesophageal echocardiography in patients with patent foramen ovales. J Am Soc Echocardiogr. 2010 Nov;23(11):1136-42. doi: 10.1016/j.echo.2010.08.004. Epub 2010 Sep 20.

45. Pristipino C, Sievert H, D'Ascenzo F, et al. European position paper on the management of patients with patent foramen ovale. General approach and left circulation thromboembolism. Eur Heart J. 2019 Oct 7;40(38):3182-3195. doi: 10.1093/eurheartj/ehy649.

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47. Suslina ZA, Fonyakin AV, Chechetkin AO, et al. Paradoxal embolisms in patients with ischemic stroke. Klinicheskaya meditsina. 2008;(9):35-9. (In Russ.).

48. Tsang TS, Abhayaratna WP, Barnes ME, et al. Prediction of cardiovascular outcomes with left atrial size: is volume superior to area or diameter? J Am Coll Cardiol. 2006 Mar 7;47(5): 1018-23. Epub 2006 Feb 9.

49. Mojadidi MK, Bogush N, Caceres JD, et al. Diagnostic accuracy of transesophageal echocardiogram for the detection of patent foramen ovale: a meta-analysis. Echocardiography. 2014 Jul;31(6):752-8. doi: 10.1111/echo.12462. Epub 2013 Dec 23.

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51. Glebov MV. Ischemic stroke and paradoxal cerebral embolism. Dis... cand. med. sci. Moscow; 2009.

52. Kamel H, Okin PM, Elkind MS, Iadecola C. Atrial fibrillation and mechanisms of stroke: time for a new model. Stroke. 2016 Mar;47(3): 895-900. doi: 10.1161/STROKEAHA.115.012004. Epub 2016 Jan 19.

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54. Jordan K, Yaghi S, Poppas A, et al. Left Atrial Volume Index Is Associated With Cardioembolic Stroke and Atrial Fibrillation Detection After Embolic Stroke of Undetermined Source. Stroke. 2019 Aug;50(8): 1997-2001. doi: 10.1161/STROKEAHA.119.025384. Epub 2019 Jun 13.

55. Del Sette M, Dinia L, Rizzi D, et al. Diagnosis of Right-to-Left Shunt With Transcranial Doppler and Vertebrobasilar Recording. Stroke. 2007 Aug;38(8):2254-6. Epub 2007 Jun 28.

56. Rigatelli G, Zuin M, Adami A, et al. Left atrial enlargement as a marker of significant high-risk patent foramen ovale. nt J Cardiovasc Imaging. 2019 Nov;35(11):

57. Serena J, Segura T, Perez-Ayuso MJ, et al. The need to quantify right-to-left shunt in acute ischemic stroke: A case-control study. Stroke. 1998 Jul;29(7):1322-8.

58. Lang RM, Badano LP, Mor-Avi V, et al. Recommendations for Cardiac Chamber Quantification by Echocardiography in Adults: An Update from the American Society of Echocardiography and the European Association of Cardiovascular Imaging. J Am Soc Echocardiogr. 2015 Jan;28(1):1-39.e14. doi: 10.1016/j.echo.2014.10.003.

59. 2049-2056. doi: 10.1007/s10554-019-01666-x. Epub 2019 Jul 19.

60. Kent DM, Ruthazer R, Weimar C, et al. An index to identify stroke-related vs incidental patent foramen ovale in cryptogenic stroke. Neurology. 2013 Aug 13;81(7):619-25. doi: 10.1212/WNL.0b013e3182a08d59. Epub 2013 Jul 17.

61. Mitchell C, Rahko PS, Blauwet LA, et al. Guidelines for Performing a Comprehensive Transthoracic Echocardiographic Examination in Adults: Recommendations from the American Society of Echocardiography. J Am Soc Echocardiogr. 2019 Jan;32(1):1-64. doi: 10.1016/j.echo.2018.06.004. Epub 2018 Oct 1.

62. Ozdemir AO, Tamayo A, Munoz C, et al. Cryptogenic stroke and patent foramen ovale: clinical clues to paradoxical embolism. J Neurol Sci. 2008 Dec 15;275(1-2):121-7. doi: 10.1016/j.jns.2008.08.018. Epub 2008 Sep 26.

63. Di Tullio MR, Sacco RL, Sciacca RR, Homma S. Left atrial size and the risk of ischemic stroke in an ethnically mixed population. Stroke. 1999 Oct;30(10):2019-24.

64. Yaghi S, Moon YP, Mora-McLaughlin C, et al. Left atrial enlargement and stroke recurrence: the northern manhattan stroke study. Stroke. 2015 Jun;46(6):1488-93. doi: 10.1161/STROKEAHA.115.008711. Epub 2015 Apr 23.

65. Huang YY, Shao B, Ni XD, Li JC. 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 Jul;23(6):1690-5. doi: 10.1016/j.jstrokecerebrovasdis.2014.01.017. Epub 2014 Apr 13.

66. Yaghi S, Bartz TM, Kronmal R, et al. Left atrial diameter and vascular brain injury on MRI: the cardiovascular health study Neurology. 2018 Sep 25;91(13):e1237-e1244. doi: 10.1212/WNL.0000000000006228. Epub 2018 Aug 29.

67. Nam KW, Guk HS, Kwon HM, Lee YS. Diffusion-Weighted Imaging Patterns According to the Right-to-Left Shunt Amount in Cryptogenic Stroke. Cerebrovasc Dis. 2019; 48(1-2):45-52. doi: 10.1159/000502882. Epub 2019 Sep 6.

68. Barnes ME, Miyasaka Y, Seward JB, et al. Left atrial volume in the prediction of first ischemic stroke in an elderly cohort without atrial fibrillation. Mayo Clin Proc. 2004 Aug; 79(8):1008-14.

69. Nakayama R, Takaya Y, Akagi T, et al. Identification of High-Risk Patent Foramen Ovale Associated With Cryptogenic Stroke: Development of a Scoring System. J Am Soc Echocardiogr. 2019 Jul;32(7):811-816. doi: 10.1016/j.echo.2019.03.021. Epub 2019 May 23.

70. Webster MW, Chancellor AM, Smith HJ, et al. Patent foramen ovale in young stroke patients. Lancet. 1988 Jul 2;2(8601):11-2.

71. Russo C, Jin Z, Liu R, et al. LA volumes and reservoir function are associated with subclinical cerebrovascular disease: the CABL (Cardiovascular Abnormalities and Brain Lesions) study. JACC Cardiovasc Imaging. 2013 Mar;6(3):313-23. doi: 10.1016/j.jcmg.2012.10.019.

72. Van Camp G, Schulze D, Cosyns B, Vandenbossche JL. Relation between patent foramen ovale and unexplained stroke. Am J Cardiol. 1993 Mar 1;71(7):596-8.

73. Tsang TS, Abhayaratna WP, Barnes ME, et al. Prediction of cardiovascular outcomes with left atrial size: is volume superior to area or diameter? J Am Coll Cardiol. 2006 Mar 7;47(5): 1018-23. Epub 2006 Feb 9.

74. Saric M, Armour AC, Arnaout MS, et al. Guidelines for the Use of Echocardiography in the Evaluation of a Cardiac Source of Embolism. J Am Soc Echocardiogr. 2016 Jan; 29(1):1-42. doi: 10.1016/j.echo.2015.09.011.

75. Yaghi S, Kamel H, Elkind MSV. Atrial cardiopathy: a mechanism of cryptogenic stroke. Expert Rev Cardiovasc Ther. 2017 Aug; 15(8):591-599. doi: 10.1080/14779072.2017.1355238. Epub 2017 Jul 27.

76. Kamel H, Okin PM, Elkind MS, Iadecola C. Atrial fibrillation and mechanisms of stroke: time for a new model. Stroke. 2016 Mar;47(3): 895-900. doi: 10.1161/STROKEAHA.115.012004. Epub 2016 Jan 19.

77. Woods TD, Patel A. A critical review of patent foramen ovale detection using saline contrast echocardiography: when bubbles lie. J Am Soc Echocardiogr. 2006 Feb;19(2):215-22.

78. Johansson MC, Eriksson P, Guron CW, Dellborg M. Pitfalls in diagnosing PFO: characteristics of false-negative contrast injections during transesophageal echocardiography in patients with patent foramen ovales. J Am Soc Echocardiogr. 2010 Nov;23(11):1136-42. doi: 10.1016/j.echo.2010.08.004. Epub 2010 Sep 20.

79. Jordan K, Yaghi S, Poppas A, et al. Left Atrial Volume Index Is Associated With Cardioembolic Stroke and Atrial Fibrillation Detection After Embolic Stroke of Undetermined Source. Stroke. 2019 Aug;50(8): 1997-2001. doi: 10.1161/STROKEAHA.119.025384. Epub 2019 Jun 13.

80. Rigatelli G, Zuin M, Adami A, et al. Left atrial enlargement as a marker of significant high-risk patent foramen ovale. nt J Cardiovasc Imaging. 2019 Nov;35(11):

81. Silvestry FE, Cohen MS, Armsby LB, et al; American Society of Echocardiography; Society for Cardiac Angiography and Interventions. Guidelines for the echocardiographic assessment of atrial septal defect and patent foramen ovale: from the American Society of Echocardiography and Society for Cardiac Angiography and Interventions. J Am Soc Echocardiogr. 2015 Aug;28(8):910-58. doi: 10.1016/j.echo.2015.05.015.

82. 2049-2056. doi: 10.1007/s10554-019-01666-x. Epub 2019 Jul 19.

83. Mojadidi MK, Bogush N, Caceres JD, et al. Diagnostic accuracy of transesophageal echocardiogram for the detection of patent foramen ovale: a meta-analysis. Echocardiography. 2014 Jul;31(6):752-8. doi: 10.1111/echo.12462. Epub 2013 Dec 23.

84. Kent DM, Ruthazer R, Weimar C, et al. An index to identify stroke-related vs incidental patent foramen ovale in cryptogenic stroke. Neurology. 2013 Aug 13;81(7):619-25. doi: 10.1212/WNL.0b013e3182a08d59. Epub 2013 Jul 17.

85. Ozdemir AO, Tamayo A, Munoz C, et al. Cryptogenic stroke and patent foramen ovale: clinical clues to paradoxical embolism. J Neurol Sci. 2008 Dec 15;275(1-2):121-7. doi: 10.1016/j.jns.2008.08.018. Epub 2008 Sep 26.

86. Huang YY, Shao B, Ni XD, Li JC. 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 Jul;23(6):1690-5. doi: 10.1016/j.jstrokecerebrovasdis.2014.01.017. Epub 2014 Apr 13.

87. Nam KW, Guk HS, Kwon HM, Lee YS. Diffusion-Weighted Imaging Patterns According to the Right-to-Left Shunt Amount in Cryptogenic Stroke. Cerebrovasc Dis. 2019; 48(1-2):45-52. doi: 10.1159/000502882. Epub 2019 Sep 6.

88. Nakayama R, Takaya Y, Akagi T, et al. Identification of High-Risk Patent Foramen Ovale Associated With Cryptogenic Stroke: Development of a Scoring System. J Am Soc Echocardiogr. 2019 Jul;32(7):811-816. doi: 10.1016/j.echo.2019.03.021. Epub 2019 May 23.

89. Webster MW, Chancellor AM, Smith HJ, et al. Patent foramen ovale in young stroke patients. Lancet. 1988 Jul 2;2(8601):11-2.

90. Van Camp G, Schulze D, Cosyns B, Vandenbossche JL. Relation between patent foramen ovale and unexplained stroke. Am J Cardiol. 1993 Mar 1;71(7):596-8.

91. Saric M, Armour AC, Arnaout MS, et al. Guidelines for the Use of Echocardiography in the Evaluation of a Cardiac Source of Embolism. J Am Soc Echocardiogr. 2016 Jan; 29(1):1-42. doi: 10.1016/j.echo.2015.09.011.

92. Woods TD, Patel A. A critical review of patent foramen ovale detection using saline contrast echocardiography: when bubbles lie. J Am Soc Echocardiogr. 2006 Feb;19(2):215-22.

93. Johansson MC, Eriksson P, Guron CW, Dellborg M. Pitfalls in diagnosing PFO: characteristics of false-negative contrast injections during transesophageal echocardiography in patients with patent foramen ovales. J Am Soc Echocardiogr. 2010 Nov;23(11):1136-42. doi: 10.1016/j.echo.2010.08.004. Epub 2010 Sep 20.

94. Silvestry FE, Cohen MS, Armsby LB, et al; American Society of Echocardiography; Society for Cardiac Angiography and Interventions. Guidelines for the echocardiographic assessment of atrial septal defect and patent foramen ovale: from the American Society of Echocardiography and Society for Cardiac Angiography and Interventions. J Am Soc Echocardiogr. 2015 Aug;28(8):910-58. doi: 10.1016/j.echo.2015.05.015.

95. Mojadidi MK, Bogush N, Caceres JD, et al. Diagnostic accuracy of transesophageal echocardiogram for the detection of patent foramen ovale: a meta-analysis. Echocardiography. 2014 Jul;31(6):752-8. doi: 10.1111/echo.12462. Epub 2013 Dec 23.


For citation:


Mekhryakov S.A., Kulesh A.A., Pokalenko E.A., Syromyatnikova L.I., Kulikova S.P., Drobakha V.E., Shestakov V.V., Karakulova Y.V. The paradoxical embolism phenomenon in patients with embolic cryptogenic stroke. Neurology, Neuropsychiatry, Psychosomatics. 2020;12(1):13-21. (In Russ.) https://doi.org/10.14412/2074-2711-2020-1-13-21

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ISSN 2074-2711 (Print)
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