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Contrast transcranial Doppler examination in the acute phase of a paradoxical brain embolism associated with pulmonary thromboembolism
Case Report
Contrast Transcranial Doppler Examination in the Acute Phase of a Paradoxical Brain Embolism Associated With Pulmonary Thromboembolism Kazumi Kimura, md, Kazuo Minematsu, md, Katunori Isa, md, Kuniyasu Wada, md, Masahiro Yasaka, md, and Takenori Yamaguchi, md
The right-to-left shunt is often diagnosed by transcranial Doppler (TCD) with saline contrast with Valsalva’s maneuver or cough. In the acute phase of stroke, however, Valsalva’s maneuver or cough could not always be performed because of the patient’s aphasia or consciousness disturbance. We report an acute aphasic stroke patient with a pulmonary thromboembolism who is diagnosed as having a rightto-left shunt by using TCD with saline contrast without Valsalva’s maneuver or cough. In patients who have embolic stroke of undetermined cause, even if they cannot perform Valsalva’s maneuver or cough because of aphasia or consciousness disturbance, TCD with saline contrast in the acute phase of stroke may be helpful for diagnosis of a paradoxical embolism. Key Words: Patent foramen ovale—Highintensity transient signal—Contrast TCD—Pulmonary thromboembolism.
The diagnosis of a paradoxical brain embolism can be made in stroke patients if they have venous thrombosis or pulmonary thromboembolism and a right-to-left shunt, such as patent foramen ovale (PFO), atrial septal defect (ASD), and intrapulmonary arteriovenous fistura.1 Patients with an acute paradoxical brain embolism often have pulmonary thromboembolism. Recurrence of a brain embolism or pulmonary thromboembolism is not
From the Cerebrovascular Division, Department of Medicine, National Cardiovascular Center, Suita, Osaka, Japan. Received March 21, 2000; accepted May 23, 2000. Supported in part by Research Grants for Cardiovascular Diseases (8C-4, 9A-2, 9A-3, and 9A-8) from the Ministry of Health and Welfare of Japan, and by Special Coordinating Funds for Promoting Science and Technology (Strategic Promotion System for Brain Science) from the Science and Technology Agency of Japan. Address reprint requests to Masahiro Yasaka, MD, Cerebrovascular Division, Department of Medicine, National Cardiovascular Center, 5-7-1 Fujishirodai, Suita, Osaka 565-8565, Japan. Copyright © 2000 by National Stroke Association 1052-3057/00/0906-0001$3.00/0 doi:10.1053/jscd.2000.16608
rare during their acute phase of stroke. Once the diagnosis of a paradoxical embolism is established, recurrent episodes should be prevented by anticoagulation therapy.2,3 Therefore, the diagnosis of a paradoxical brain embolism should be made as quickly as possible. Transesophageal echocardiography (TEE) is the method of choice for the detection of a right-to-left cardiac shunt, particularly in combination with provocative methods, such as Valsalva’s maneuver and cough.4,5 However, TEE is not always applicable in acute stroke patients because it is a semi-invasive procedure and because stroke patients can not always comply with the request of Valsalva’s maneuver or cough. In recent studies, it was shown that transcranial Doppler (TCD) with saline contrast, which is able to detect air or contrast microbubbles passing through the intracranial arteries, is useful to detect the presence of a right-to-left shunt.6-9 To our knowledge, however, it remains unknown whether or not TCD with saline contrast during normal breathing without Valsalva’s maneuver or cough is helpful for the diagnosis of a paradoxical embolism in the acute phase of stroke.
Journal of Stroke and Cerebrovascular Diseases, Vol. 9, No. 6 (November-December), 2000: pp 313-316
313
314
Figure 1. A brain CT scan taken 2 days after the onset of symptoms shows a hypodense area in the territory of the ascending branches of the left MCA.
We report a patient with an acute paradoxical brain embolism through a PFO associated with acute pulmonary thromboembolism. We could diagnose the patient as having a paradoxical brain embolism by a TCD with saline contrast within days of stroke onset. Moreover, a follow-up TCD examination showed that the degree of right-to-left shunting was reduced after treatment with heparin.
Case Report A 77-year-old right-handed man was admitted to the National Cardiovascular Center, Osaka, Japan, on May
K. KIMURA ET AL.
28, 1998 because of a sudden onset of aphasia and right hemiparesis. Eight years before this episode, he was implanted with a dual sensing, dual pacing, dual modes (inhibition and trigger) (DDD) pacemaker for the treatment of a complete atrioventricular block. He did not have any history of dyspnea before or after the stroke. His past medical history was unremarkable except for arrhythmia. At the time of admission, his blood pressure was 116/68 mm Hg with a regular heart rate of 66/min and a respiratory rate of 19/min. Neither pathologic breath sounds nor heart murmurs were heard, and no pitting edema was present in his lower extremities. Neurologic examinations showed that he had aphasia and right hemiparesis. Complete blood cell counts, liver and renal functions, serum cholesterol and blood glucose levels were normal. Although plasma levels of protein C and antithrombin III were within normal limits, D-dimer and thrombin-antithrombin III complex (TAT) were 2.0 g/mL and 19.1 g/L respectively, both higher than their normal levels. An arterial blood gas analysis showed hypoxemia, with a Pao2 of 68.9 mm Hg and a Paco2 of 36.6 mm Hg on room air. A chest radiograph was normal. An electrocardiogram showed a normal sinus rhythm. A cervical ultrasound examination with color-coded Doppler showed normal arterial morphologies and normal blood flow velocities in the common carotid and vertebral arteries on both sides. A computed tomography (CT) scan of the brain showed no abnormalities on the day of admission, but a hypodense area in the anterior part of the left middle cerebral artery (MCA) territory on the next day (Fig 1). Intra-arterial digital subtraction angiography performed 6 hours after stroke onset showed occlusion of the ascending branches of the left MCA. Both vertebral and carotid arteries, and the right intracranial vessels were normal. We presumed that the patient may have had a paradoxical brain embolism based on CT and angiographic findings, the presence of hypoxia, and a hypercoagulable state. Four days after stroke onset, a TCD with saline
Figure 2. TCD with saline contrast during normal breathing shows many HITs from the left MCA 12 to 20 seconds after the injection of a saline solution (9 mL) and air (1 mL) mixture. The study was performed 4 days after the onset of symptoms.
CONTRAST TCD IN ACUTE PARADOXICAL BRAIN EMBOLISM
315
Figure 3. Ventilation-perfusion lung scintigrams. (A) The study taken 4 days after stroke onset shows a perfusion defect in the right upper lung. The perfusion defect in the left upper lung is caused by the pacemaker. (B) The follow-up study taken 24 days after stroke onset shows no perfusion defect in the right upper lung.
contrast was performed to examine the presence of a right-to-left shunt. The TCD with saline contrast was performed with a mixture of saline solution (9 mL) and air (1 mL) agitated between 2 10-mL syringes that were connected by a 3-way stopcock. The solution was injected within 2 to 3 seconds into the right antecubital vein without provocative methods, such as Valsalva’s maneuver and cough. The TCD study showed 12 high-intensity transient signals (HITSs) from the left MCA during normal breathing (Fig 2). On the same day, a ventilationperfusion lung scintigrapm showed a perfusion defect in the right upper lung (Fig 3A), and a venogram showed a filling defect in the left popliteal vein. We then performed contrast TEE to look for the presence of PFO or ASD, and
an enlargement of right atrium. Contrast TEE showed a right-to-left cardiac shunt through the PFO, but the size of right atrium was normal. Therefore, he was diagnosed as having a paradoxical brain embolism through PFO associated with pulmonary thromboembolism. Deep vein thrombosis (DVT) in the left popliteal vein was considered as the common source of pulmonary thromboembolism and the brain embolism. Heparin (10,000 U/day) was administered 4 days after the patient’s admission. A follow-up TCD with saline contrast 24 days after the onset of symptoms detected only one HITS during normal breathing, and a follow-up ventilation-perfusion lung scintigram showed no perfusion defect in the right upper lung (Fig 3B). At this time, Pao2 (85.4 mm Hg on
316
K. KIMURA ET AL.
room air), D-dimer (0.3 g/mL), and TAT (1.36 g/L) were all within normal ranges. The patient’s neurologic deficits improved gradually, and he became able to walk independently. Forty days after his admission, he was discharged to his home.
7-9
Discussion A PFO may be found in up to 42% to 52% of patients with strokes of undetermined etiology.10,11 Initially, we presumed that his stroke mechanism was embolic because of CT and angiographic findings. However, the source of emboli was undetermined. Blood examinations showed that he had hypoxemia and a hypercoagulable state. These data indicated that the patient might suffer from a paradoxical brain embolism associated with pulmonary thromboembolism. We therefore performed TCD with saline contrast to look for the presence of a rightto-left shunt. TCD with saline contrast during normal breathing without Valsalva’s maneuver or cough detected many HITSs, indicating the presence of a persistent right-to-left shunt. If TCD with saline contrast detects many HITSs without provocative conditions, the possibility of a large PFO or ASD, a PFO with an increase in right atrial pressure due to pulmonary hypertension, or a pulmonary arteriovenous fistula should be considered.12 TEE and subsequent studies confirmed a right-toleft cardiac shunt through the PFO and the presence of pulmonary thromboembolism and DVT, respectively. In this patient, TCD with saline contrast during normal breathing could detect many HITSs in the acute phase of stroke. A follow-up study after treatment with heparin could detect only a few HITSs during normal breathing, indicating that the degree of right-to-left shunting was reduced by the decrease in right atrial pressure because of the improvement of pulmonary thromboembolism. At the same time, a ventilation-perfusion lung scintigrapm became normal, and hypoxemia disappeared. These data indicated that the paradoxical brain embolism through PFO occurred because of a temporary increase in right atrial pressure by acute but clinically silent pulmonary thromboembolism from DVT. TCD with saline contrast should be performed as soon as possible after stroke onset in patients with an undetermined source of emboli because TCD with saline contrast does not always show HITS in the subacute phase of stroke. In patients with a PFO without an increase in right atrial pressure, TCD with saline contrast using provoca-
tive conditions often detects HITSs. However, if patients with a PFO have an increase in right atrial pressure, TCD with saline contrast without provocative conditions may detect HITSs. Therefore, in embolic stroke patients of undetermined etiology, even if they cannot perform Valsalva’s maneuver or cough because of aphasia or consciousness disturbance, TCD with saline contrast in the acute phase of stroke may be helpful for diagnosis of a paradoxical embolism.
References 1. Jones HR Jr, Caplan LR, Come PC, et al. Cerebral emboli of paradoxical origin. Ann Neurol 1983;13:314-319. 2. Gallus A, Jackaman J, Tillett J, et al. Safety and efficacy of warfarin started early after submassive venous thrombosis or pulmonary embolism. Lancet 1986;2:1293-1296. 3. Speechly-Dick ME, Middleton SJ, Foale RA. Impending paradoxical embolism: A rare but important diagnosis. Br Heart J 1991;65:163-165. 4. Di Tullio M, Sacco RL, Venketasubramanian N, et al. Comparison of diagnostic techniques for the detection of a patent foramen ovale in stroke patients. Stroke 1993; 24:1020-1024. 5. Hausmann D, Mugge A, Becht I, et al. Diagnosis of patent foramen ovale by transesophageal echocardiography and association with cerebral and peripheral embolic events. Am J Cardiol 1992;70:668-672. 6. Karnik R, Stollberger C, Valentin A, et al. Detection of patent foramen ovale by transcranial contrast Doppler ultrasound. Am J Cardiol 1992;69:560-562. 7. Anzola GP, Renaldini E, Magoni M, et al. Validation of transcranial Doppler sonography in the assessment of patent foramen ovale. Cerebrovasc Dis 1995;5:194-198. 8. Devuyst G, Despland PA, Bogousslavsky J, et al. Complementarity of contrast transcranial Doppler and contrast transesophageal echocardiography for the detection of patent foramen ovale in stroke patients. Eur J Neurol 1997;38:21-25. 9. 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. 10. Lechat P, Mas JL, Lascault G, et al. Prevalence of patent foramen ovale in patients with stroke. N Engl J Med 1988;318:1148-1152. 11. Di Tullio M, Sacco RL, Gopal A, et al. Patent foramen ovale as a risk factor for cryptogenic stroke. Ann Intern Med 1992;117:461-465. 12. Kimura K, Minematsu K, Wada K, et al. Transcranial Doppler of a paradoxical brain embolism associated with a pulmonary aretriovenous fistula. AJNR Am J Neuroradiol 1999;20:1881-1884.
Contrast Transcranial Doppler Examination in the Acute Phase of a Paradoxical Brain Embolism Associated With Pulmonary Thromboembolism Kazumi Kimura, md, Kazuo Minematsu, md, Katunori Isa, md, Kuniyasu Wada, md, Masahiro Yasaka, md, and Takenori Yamaguchi, md
The right-to-left shunt is often diagnosed by transcranial Doppler (TCD) with saline contrast with Valsalva’s maneuver or cough. In the acute phase of stroke, however, Valsalva’s maneuver or cough could not always be performed because of the patient’s aphasia or consciousness disturbance. We report an acute aphasic stroke patient with a pulmonary thromboembolism who is diagnosed as having a rightto-left shunt by using TCD with saline contrast without Valsalva’s maneuver or cough. In patients who have embolic stroke of undetermined cause, even if they cannot perform Valsalva’s maneuver or cough because of aphasia or consciousness disturbance, TCD with saline contrast in the acute phase of stroke may be helpful for diagnosis of a paradoxical embolism. Key Words: Patent foramen ovale—Highintensity transient signal—Contrast TCD—Pulmonary thromboembolism.
The diagnosis of a paradoxical brain embolism can be made in stroke patients if they have venous thrombosis or pulmonary thromboembolism and a right-to-left shunt, such as patent foramen ovale (PFO), atrial septal defect (ASD), and intrapulmonary arteriovenous fistura.1 Patients with an acute paradoxical brain embolism often have pulmonary thromboembolism. Recurrence of a brain embolism or pulmonary thromboembolism is not
From the Cerebrovascular Division, Department of Medicine, National Cardiovascular Center, Suita, Osaka, Japan. Received March 21, 2000; accepted May 23, 2000. Supported in part by Research Grants for Cardiovascular Diseases (8C-4, 9A-2, 9A-3, and 9A-8) from the Ministry of Health and Welfare of Japan, and by Special Coordinating Funds for Promoting Science and Technology (Strategic Promotion System for Brain Science) from the Science and Technology Agency of Japan. Address reprint requests to Masahiro Yasaka, MD, Cerebrovascular Division, Department of Medicine, National Cardiovascular Center, 5-7-1 Fujishirodai, Suita, Osaka 565-8565, Japan. Copyright © 2000 by National Stroke Association 1052-3057/00/0906-0001$3.00/0 doi:10.1053/jscd.2000.16608
rare during their acute phase of stroke. Once the diagnosis of a paradoxical embolism is established, recurrent episodes should be prevented by anticoagulation therapy.2,3 Therefore, the diagnosis of a paradoxical brain embolism should be made as quickly as possible. Transesophageal echocardiography (TEE) is the method of choice for the detection of a right-to-left cardiac shunt, particularly in combination with provocative methods, such as Valsalva’s maneuver and cough.4,5 However, TEE is not always applicable in acute stroke patients because it is a semi-invasive procedure and because stroke patients can not always comply with the request of Valsalva’s maneuver or cough. In recent studies, it was shown that transcranial Doppler (TCD) with saline contrast, which is able to detect air or contrast microbubbles passing through the intracranial arteries, is useful to detect the presence of a right-to-left shunt.6-9 To our knowledge, however, it remains unknown whether or not TCD with saline contrast during normal breathing without Valsalva’s maneuver or cough is helpful for the diagnosis of a paradoxical embolism in the acute phase of stroke.
Journal of Stroke and Cerebrovascular Diseases, Vol. 9, No. 6 (November-December), 2000: pp 313-316
313
314
Figure 1. A brain CT scan taken 2 days after the onset of symptoms shows a hypodense area in the territory of the ascending branches of the left MCA.
We report a patient with an acute paradoxical brain embolism through a PFO associated with acute pulmonary thromboembolism. We could diagnose the patient as having a paradoxical brain embolism by a TCD with saline contrast within days of stroke onset. Moreover, a follow-up TCD examination showed that the degree of right-to-left shunting was reduced after treatment with heparin.
Case Report A 77-year-old right-handed man was admitted to the National Cardiovascular Center, Osaka, Japan, on May
K. KIMURA ET AL.
28, 1998 because of a sudden onset of aphasia and right hemiparesis. Eight years before this episode, he was implanted with a dual sensing, dual pacing, dual modes (inhibition and trigger) (DDD) pacemaker for the treatment of a complete atrioventricular block. He did not have any history of dyspnea before or after the stroke. His past medical history was unremarkable except for arrhythmia. At the time of admission, his blood pressure was 116/68 mm Hg with a regular heart rate of 66/min and a respiratory rate of 19/min. Neither pathologic breath sounds nor heart murmurs were heard, and no pitting edema was present in his lower extremities. Neurologic examinations showed that he had aphasia and right hemiparesis. Complete blood cell counts, liver and renal functions, serum cholesterol and blood glucose levels were normal. Although plasma levels of protein C and antithrombin III were within normal limits, D-dimer and thrombin-antithrombin III complex (TAT) were 2.0 g/mL and 19.1 g/L respectively, both higher than their normal levels. An arterial blood gas analysis showed hypoxemia, with a Pao2 of 68.9 mm Hg and a Paco2 of 36.6 mm Hg on room air. A chest radiograph was normal. An electrocardiogram showed a normal sinus rhythm. A cervical ultrasound examination with color-coded Doppler showed normal arterial morphologies and normal blood flow velocities in the common carotid and vertebral arteries on both sides. A computed tomography (CT) scan of the brain showed no abnormalities on the day of admission, but a hypodense area in the anterior part of the left middle cerebral artery (MCA) territory on the next day (Fig 1). Intra-arterial digital subtraction angiography performed 6 hours after stroke onset showed occlusion of the ascending branches of the left MCA. Both vertebral and carotid arteries, and the right intracranial vessels were normal. We presumed that the patient may have had a paradoxical brain embolism based on CT and angiographic findings, the presence of hypoxia, and a hypercoagulable state. Four days after stroke onset, a TCD with saline
Figure 2. TCD with saline contrast during normal breathing shows many HITs from the left MCA 12 to 20 seconds after the injection of a saline solution (9 mL) and air (1 mL) mixture. The study was performed 4 days after the onset of symptoms.
CONTRAST TCD IN ACUTE PARADOXICAL BRAIN EMBOLISM
315
Figure 3. Ventilation-perfusion lung scintigrams. (A) The study taken 4 days after stroke onset shows a perfusion defect in the right upper lung. The perfusion defect in the left upper lung is caused by the pacemaker. (B) The follow-up study taken 24 days after stroke onset shows no perfusion defect in the right upper lung.
contrast was performed to examine the presence of a right-to-left shunt. The TCD with saline contrast was performed with a mixture of saline solution (9 mL) and air (1 mL) agitated between 2 10-mL syringes that were connected by a 3-way stopcock. The solution was injected within 2 to 3 seconds into the right antecubital vein without provocative methods, such as Valsalva’s maneuver and cough. The TCD study showed 12 high-intensity transient signals (HITSs) from the left MCA during normal breathing (Fig 2). On the same day, a ventilationperfusion lung scintigrapm showed a perfusion defect in the right upper lung (Fig 3A), and a venogram showed a filling defect in the left popliteal vein. We then performed contrast TEE to look for the presence of PFO or ASD, and
an enlargement of right atrium. Contrast TEE showed a right-to-left cardiac shunt through the PFO, but the size of right atrium was normal. Therefore, he was diagnosed as having a paradoxical brain embolism through PFO associated with pulmonary thromboembolism. Deep vein thrombosis (DVT) in the left popliteal vein was considered as the common source of pulmonary thromboembolism and the brain embolism. Heparin (10,000 U/day) was administered 4 days after the patient’s admission. A follow-up TCD with saline contrast 24 days after the onset of symptoms detected only one HITS during normal breathing, and a follow-up ventilation-perfusion lung scintigram showed no perfusion defect in the right upper lung (Fig 3B). At this time, Pao2 (85.4 mm Hg on
316
K. KIMURA ET AL.
room air), D-dimer (0.3 g/mL), and TAT (1.36 g/L) were all within normal ranges. The patient’s neurologic deficits improved gradually, and he became able to walk independently. Forty days after his admission, he was discharged to his home.
7-9
Discussion A PFO may be found in up to 42% to 52% of patients with strokes of undetermined etiology.10,11 Initially, we presumed that his stroke mechanism was embolic because of CT and angiographic findings. However, the source of emboli was undetermined. Blood examinations showed that he had hypoxemia and a hypercoagulable state. These data indicated that the patient might suffer from a paradoxical brain embolism associated with pulmonary thromboembolism. We therefore performed TCD with saline contrast to look for the presence of a rightto-left shunt. TCD with saline contrast during normal breathing without Valsalva’s maneuver or cough detected many HITSs, indicating the presence of a persistent right-to-left shunt. If TCD with saline contrast detects many HITSs without provocative conditions, the possibility of a large PFO or ASD, a PFO with an increase in right atrial pressure due to pulmonary hypertension, or a pulmonary arteriovenous fistula should be considered.12 TEE and subsequent studies confirmed a right-toleft cardiac shunt through the PFO and the presence of pulmonary thromboembolism and DVT, respectively. In this patient, TCD with saline contrast during normal breathing could detect many HITSs in the acute phase of stroke. A follow-up study after treatment with heparin could detect only a few HITSs during normal breathing, indicating that the degree of right-to-left shunting was reduced by the decrease in right atrial pressure because of the improvement of pulmonary thromboembolism. At the same time, a ventilation-perfusion lung scintigrapm became normal, and hypoxemia disappeared. These data indicated that the paradoxical brain embolism through PFO occurred because of a temporary increase in right atrial pressure by acute but clinically silent pulmonary thromboembolism from DVT. TCD with saline contrast should be performed as soon as possible after stroke onset in patients with an undetermined source of emboli because TCD with saline contrast does not always show HITS in the subacute phase of stroke. In patients with a PFO without an increase in right atrial pressure, TCD with saline contrast using provoca-
tive conditions often detects HITSs. However, if patients with a PFO have an increase in right atrial pressure, TCD with saline contrast without provocative conditions may detect HITSs. Therefore, in embolic stroke patients of undetermined etiology, even if they cannot perform Valsalva’s maneuver or cough because of aphasia or consciousness disturbance, TCD with saline contrast in the acute phase of stroke may be helpful for diagnosis of a paradoxical embolism.
References 1. Jones HR Jr, Caplan LR, Come PC, et al. Cerebral emboli of paradoxical origin. Ann Neurol 1983;13:314-319. 2. Gallus A, Jackaman J, Tillett J, et al. Safety and efficacy of warfarin started early after submassive venous thrombosis or pulmonary embolism. Lancet 1986;2:1293-1296. 3. Speechly-Dick ME, Middleton SJ, Foale RA. Impending paradoxical embolism: A rare but important diagnosis. Br Heart J 1991;65:163-165. 4. Di Tullio M, Sacco RL, Venketasubramanian N, et al. Comparison of diagnostic techniques for the detection of a patent foramen ovale in stroke patients. Stroke 1993; 24:1020-1024. 5. Hausmann D, Mugge A, Becht I, et al. Diagnosis of patent foramen ovale by transesophageal echocardiography and association with cerebral and peripheral embolic events. Am J Cardiol 1992;70:668-672. 6. Karnik R, Stollberger C, Valentin A, et al. Detection of patent foramen ovale by transcranial contrast Doppler ultrasound. Am J Cardiol 1992;69:560-562. 7. Anzola GP, Renaldini E, Magoni M, et al. Validation of transcranial Doppler sonography in the assessment of patent foramen ovale. Cerebrovasc Dis 1995;5:194-198. 8. Devuyst G, Despland PA, Bogousslavsky J, et al. Complementarity of contrast transcranial Doppler and contrast transesophageal echocardiography for the detection of patent foramen ovale in stroke patients. Eur J Neurol 1997;38:21-25. 9. 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. 10. Lechat P, Mas JL, Lascault G, et al. Prevalence of patent foramen ovale in patients with stroke. N Engl J Med 1988;318:1148-1152. 11. Di Tullio M, Sacco RL, Gopal A, et al. Patent foramen ovale as a risk factor for cryptogenic stroke. Ann Intern Med 1992;117:461-465. 12. Kimura K, Minematsu K, Wada K, et al. Transcranial Doppler of a paradoxical brain embolism associated with a pulmonary aretriovenous fistula. AJNR Am J Neuroradiol 1999;20:1881-1884.