Patent Foramen Ovale and Unexplained Stroke
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《新英格兰医药杂志》
To the Editor: Although Kizer and Devereux (Dec. 1 issue)1 have elaborated on the association between patent foramen ovale and cryptogenic stroke, the importance of cryptogenic stroke occurring during surgery was not mentioned. Paradoxical thrombi, and fat, amniotic, and air emboli have all been reported with neurologic sequelae in numerous surgical procedures.2 Venous air embolism and paradoxical air embolism are known complications of surgery when the patient is in the prone position during spinal procedures, resulting in substantial mortality, especially in pediatric patients.3,4,5 Rodriguez and coworkers6 have reported paradoxical cerebral emboli diagnosed with the use of transcranial Doppler analysis in two children with patent foramen ovale during spinal surgery. The risk of cerebral emboli after surgery and the optimal preoperative assessment and management of patent foramen ovale for patients who are at risk, such as children, require further study.
Maurice S. Albin, M.D.
University of Alabama School of Medicine
Birmingham, AL 35249-7424
malbin@bham.rr.com
John Wills, M.D.
Richard M. Schwend, M.D.
University of New Mexico School of Medicine
Albuquerque, NM 87192
References
Kizer JR, Devereux RB. Patent foramen ovale in young adults with unexplained stroke. N Engl J Med 2005;353:2361-2372.
Capan LM, Miller SM. Embolism II. Anesthesiol Clin North America 1993;12:1-203.
Pham Dang C, Pereon Y, Champin P, Delecrin J, Passuti J. Paradoxical air embolism from patent foramen ovale in scoliosis surgery. Spine 2002;27:E291-E295.
Horlocker TT, Wedel DJ, Cucchiara RF. Venous air embolism during spinal instrumentation and fusion in the prone position. Anesth Analg 1992;75:152-152.
Wills J, Schwend RM, Paterson A, Albin MS. Intraoperative visible bubbling of air may be the first sign of venous air embolism during posterior surgery for scoliosis. Spine 2005;30:E629-E635.
Rodriguez RA, Sinclair B, Weatherdon D, Letts M. Patent foramen ovale and brain microembolization during scoliosis surgery in adolescents. Spine 2001;26:1719-1721.
To the Editor: Kizer and Devereux suggest that transesophageal echocardiography is as accurate as contrast-enhanced transcranial Doppler ultrasonography in the detection of right-to-left shunts, but of limited use for the assessment of cardiac-associated features. This is only partially true, and some considerations must be mentioned to highlight the role of transcranial Doppler ultrasonography in screening patients with cryptogenic stroke. Transcranial Doppler ultrasonography is superior to transesophageal echocardiography in the detection of extracardiac shunts.1 A right-to-left shunt due to a pulmonary fistula or a small patent foramen ovale can be detected with transcranial Doppler examination even when bidimensional transesophageal echocardiography is negative; in such cases, transcranial Doppler evaluation should guide the full clinical assessment. In addition, there is evidence that the size of a patent foramen ovale as measured by transesophageal echocardiography does not necessarily correspond to how the shunt affects cerebral circulation as assessed by transcranial Doppler methods.2,3 Therefore, right-to-left shunts should be quantified with the use of transcranial Doppler ultrasonography. This practice would give a better estimate of the size of the right-to-left shunt as a predictor of stroke recurrence in therapeutic trials.4 For the same reason, and considering that it is minimally invasive, transcranial Doppler ultrasonography and not transthoracic echocardiography should be the gold standard for the evaluation of patent foramen ovale after transcatheter closure.3
Sara Mazzucco, M.D.
University of Verona
37100 Verona, Italy
sara.mazzucco@univr.it
Gian Paolo Anzola, M.D.
Ospedale Sant'Orsola Fatebenefratelli
25122 Brescia, Italy
References
Kimura K, Minematsu K, Nakajima M. Isolated pulmonary arteriovenous fistula without Rendu-Osler-Weber disease as a cause of cryptogenic stroke. J Neurol Neurosurg Psychiatry 2004;75:311-313.
Kerut EK, Norfleet WT, Plotnick GD, Giles TD. Patent foramen ovale: a review of associated conditions and the impact of physiological size. J Am Coll Cardiol 2001;38:613-623.
Anzola GP, Morandi E, Casilli F, Onorato E. Does transcatheter closure of patent foramen ovale really "shut the door?" A prospective study with transcranial Doppler. Stroke 2004;35:2140-2144.
Anzola GP, Zavarize P, Morandi E, Rozzini L, Parrinello G. Transcranial Doppler and risk of recurrence in patients with stroke and patent foramen ovale. Eur J Neurol 2003;10:129-135.
The authors reply: We appreciate the comments of Albin and colleagues regarding the importance of patent foramen ovale in stroke complicating surgical intervention. As Albin et al. point out, emboli consisting of a variety of substances and arising during surgical procedures1 can play havoc in the arterial circulation if permitted passage across the foramen.2 We did not discuss the problem of perioperative paradoxical embolism, however, because identification of the embolic substrate, directly or circumstantially, is more often feasible in the perioperative setting than in the classic instance of cryptogenic stroke, which was the focus of our review. Nevertheless, given the common occurrence of patent foramen ovale in the general population, we concur that additional study is warranted to characterize perioperative risk and to define optimal preoperative evaluation and management.
We thank Mazzucco and Anzola for highlighting differences in the diagnostic properties of contrast-enhanced transesophageal echocardiography and contrast-enhanced transcranial Doppler ultrasonography as reported in the literature. Some studies have indeed documented a higher sensitivity for contrast-enhanced transcranial Doppler ultrasonography in the detection of right-to-left shunts, but the accuracy of the two techniques for larger shunts is virtually identical.3
Because contrast-enhanced transcranial Doppler methods cannot be used reliably to distinguish between intracardiac and extracardiac shunting,3 it is not clear what proportion of right-to-left shunts detected by this method — in the absence of evidence of interatrial communication provided by two-dimensional transesophageal echocardiography — represents clinically insignificant pulmonary fistulas. Moreover, the clinical significance of a small patent foramen ovale that goes undetected by contrast-enhanced transesophageal echocardiography is uncertain. Thus, the assertion by Mazzucco and Anzola that right-to-left shunts should be quantified by contrast-enhanced transcranial Doppler ultrasonography requires proof of the incremental clinical usefulness of this approach, since transesophageal echocardiography is already warranted in younger patients with cryptogenic stroke to rule out other sources of cardioembolism.
In addition, because it is not possible to pinpoint the location of right-to-left shunts with the use of contrast-enhanced transcranial Doppler techniques, this method is at a disadvantage as compared with the use of noninvasive contrast-enhanced transthoracic echocardiography4 after transcatheter closure of a patent foramen. Studies that compare the accuracy and cost-effectiveness of different approaches that incorporate these methods, alone and in combination, are essential to define the optimal strategy. Pending additional evidence, the position expressed in our article accords with recent conclusions that, "whereas is useful for detection of right-to-left cardiac and extracardiac shunts . . . transesophageal echocardiography is superior, as it can provide direct information as to the site and nature of the shunt."5
Finally, Figure 3 of our article, which showed a superior location of the septum primum, and Figure 1, in which the septum primum appeared in an inferior position, may seem to be discordant. What appear to be two different locations are not the result of an error but instead are attributable to the semicircular, three-dimensional structure of the septum primum.
Jorge R. Kizer, M.D.
Richard B. Devereux, M.D.
Weill Medical College of Cornell University
New York, NY 10021
jok2007@med.cornell.edu
References
Capan LM, Miller SM. Monitoring for suspected pulmonary embolism. Anesthesiol Clin North America 2001;19:673-703.
Meacham RR III, Headley AS, Bronze MS, Lewis JB, Rester MM. Impending paradoxical embolism. Arch Intern Med 1998;158:438-448.
Droste DW, Silling K, Stypmann J, et al. Contrast transcranial Doppler ultrasound in the detection of right-to-left shunts: time window and threshold in microbubble numbers. Stroke 2000;31:1640-1645.
Kerr AJ, Buck T, Chia K, et al. Transmitral Doppler: a new transthoracic contrast method for patent foramen ovale detection and quantification. J Am Coll Cardiol 2000;36:1959-1966.
Sloan MA, Alexandrov AV, Tegeler CH, et al. Assessment: transcranial Doppler ultrasonography: report of the Therapeutics and Technology Assessment Subcommittee of the American Academy of Neurology. Neurology 2004;62:1468-1481.
Maurice S. Albin, M.D.
University of Alabama School of Medicine
Birmingham, AL 35249-7424
malbin@bham.rr.com
John Wills, M.D.
Richard M. Schwend, M.D.
University of New Mexico School of Medicine
Albuquerque, NM 87192
References
Kizer JR, Devereux RB. Patent foramen ovale in young adults with unexplained stroke. N Engl J Med 2005;353:2361-2372.
Capan LM, Miller SM. Embolism II. Anesthesiol Clin North America 1993;12:1-203.
Pham Dang C, Pereon Y, Champin P, Delecrin J, Passuti J. Paradoxical air embolism from patent foramen ovale in scoliosis surgery. Spine 2002;27:E291-E295.
Horlocker TT, Wedel DJ, Cucchiara RF. Venous air embolism during spinal instrumentation and fusion in the prone position. Anesth Analg 1992;75:152-152.
Wills J, Schwend RM, Paterson A, Albin MS. Intraoperative visible bubbling of air may be the first sign of venous air embolism during posterior surgery for scoliosis. Spine 2005;30:E629-E635.
Rodriguez RA, Sinclair B, Weatherdon D, Letts M. Patent foramen ovale and brain microembolization during scoliosis surgery in adolescents. Spine 2001;26:1719-1721.
To the Editor: Kizer and Devereux suggest that transesophageal echocardiography is as accurate as contrast-enhanced transcranial Doppler ultrasonography in the detection of right-to-left shunts, but of limited use for the assessment of cardiac-associated features. This is only partially true, and some considerations must be mentioned to highlight the role of transcranial Doppler ultrasonography in screening patients with cryptogenic stroke. Transcranial Doppler ultrasonography is superior to transesophageal echocardiography in the detection of extracardiac shunts.1 A right-to-left shunt due to a pulmonary fistula or a small patent foramen ovale can be detected with transcranial Doppler examination even when bidimensional transesophageal echocardiography is negative; in such cases, transcranial Doppler evaluation should guide the full clinical assessment. In addition, there is evidence that the size of a patent foramen ovale as measured by transesophageal echocardiography does not necessarily correspond to how the shunt affects cerebral circulation as assessed by transcranial Doppler methods.2,3 Therefore, right-to-left shunts should be quantified with the use of transcranial Doppler ultrasonography. This practice would give a better estimate of the size of the right-to-left shunt as a predictor of stroke recurrence in therapeutic trials.4 For the same reason, and considering that it is minimally invasive, transcranial Doppler ultrasonography and not transthoracic echocardiography should be the gold standard for the evaluation of patent foramen ovale after transcatheter closure.3
Sara Mazzucco, M.D.
University of Verona
37100 Verona, Italy
sara.mazzucco@univr.it
Gian Paolo Anzola, M.D.
Ospedale Sant'Orsola Fatebenefratelli
25122 Brescia, Italy
References
Kimura K, Minematsu K, Nakajima M. Isolated pulmonary arteriovenous fistula without Rendu-Osler-Weber disease as a cause of cryptogenic stroke. J Neurol Neurosurg Psychiatry 2004;75:311-313.
Kerut EK, Norfleet WT, Plotnick GD, Giles TD. Patent foramen ovale: a review of associated conditions and the impact of physiological size. J Am Coll Cardiol 2001;38:613-623.
Anzola GP, Morandi E, Casilli F, Onorato E. Does transcatheter closure of patent foramen ovale really "shut the door?" A prospective study with transcranial Doppler. Stroke 2004;35:2140-2144.
Anzola GP, Zavarize P, Morandi E, Rozzini L, Parrinello G. Transcranial Doppler and risk of recurrence in patients with stroke and patent foramen ovale. Eur J Neurol 2003;10:129-135.
The authors reply: We appreciate the comments of Albin and colleagues regarding the importance of patent foramen ovale in stroke complicating surgical intervention. As Albin et al. point out, emboli consisting of a variety of substances and arising during surgical procedures1 can play havoc in the arterial circulation if permitted passage across the foramen.2 We did not discuss the problem of perioperative paradoxical embolism, however, because identification of the embolic substrate, directly or circumstantially, is more often feasible in the perioperative setting than in the classic instance of cryptogenic stroke, which was the focus of our review. Nevertheless, given the common occurrence of patent foramen ovale in the general population, we concur that additional study is warranted to characterize perioperative risk and to define optimal preoperative evaluation and management.
We thank Mazzucco and Anzola for highlighting differences in the diagnostic properties of contrast-enhanced transesophageal echocardiography and contrast-enhanced transcranial Doppler ultrasonography as reported in the literature. Some studies have indeed documented a higher sensitivity for contrast-enhanced transcranial Doppler ultrasonography in the detection of right-to-left shunts, but the accuracy of the two techniques for larger shunts is virtually identical.3
Because contrast-enhanced transcranial Doppler methods cannot be used reliably to distinguish between intracardiac and extracardiac shunting,3 it is not clear what proportion of right-to-left shunts detected by this method — in the absence of evidence of interatrial communication provided by two-dimensional transesophageal echocardiography — represents clinically insignificant pulmonary fistulas. Moreover, the clinical significance of a small patent foramen ovale that goes undetected by contrast-enhanced transesophageal echocardiography is uncertain. Thus, the assertion by Mazzucco and Anzola that right-to-left shunts should be quantified by contrast-enhanced transcranial Doppler ultrasonography requires proof of the incremental clinical usefulness of this approach, since transesophageal echocardiography is already warranted in younger patients with cryptogenic stroke to rule out other sources of cardioembolism.
In addition, because it is not possible to pinpoint the location of right-to-left shunts with the use of contrast-enhanced transcranial Doppler techniques, this method is at a disadvantage as compared with the use of noninvasive contrast-enhanced transthoracic echocardiography4 after transcatheter closure of a patent foramen. Studies that compare the accuracy and cost-effectiveness of different approaches that incorporate these methods, alone and in combination, are essential to define the optimal strategy. Pending additional evidence, the position expressed in our article accords with recent conclusions that, "whereas is useful for detection of right-to-left cardiac and extracardiac shunts . . . transesophageal echocardiography is superior, as it can provide direct information as to the site and nature of the shunt."5
Finally, Figure 3 of our article, which showed a superior location of the septum primum, and Figure 1, in which the septum primum appeared in an inferior position, may seem to be discordant. What appear to be two different locations are not the result of an error but instead are attributable to the semicircular, three-dimensional structure of the septum primum.
Jorge R. Kizer, M.D.
Richard B. Devereux, M.D.
Weill Medical College of Cornell University
New York, NY 10021
jok2007@med.cornell.edu
References
Capan LM, Miller SM. Monitoring for suspected pulmonary embolism. Anesthesiol Clin North America 2001;19:673-703.
Meacham RR III, Headley AS, Bronze MS, Lewis JB, Rester MM. Impending paradoxical embolism. Arch Intern Med 1998;158:438-448.
Droste DW, Silling K, Stypmann J, et al. Contrast transcranial Doppler ultrasound in the detection of right-to-left shunts: time window and threshold in microbubble numbers. Stroke 2000;31:1640-1645.
Kerr AJ, Buck T, Chia K, et al. Transmitral Doppler: a new transthoracic contrast method for patent foramen ovale detection and quantification. J Am Coll Cardiol 2000;36:1959-1966.
Sloan MA, Alexandrov AV, Tegeler CH, et al. Assessment: transcranial Doppler ultrasonography: report of the Therapeutics and Technology Assessment Subcommittee of the American Academy of Neurology. Neurology 2004;62:1468-1481.