Transcranial Doppler Ultrasonography and Transesophageal Echocardiography in the Investigation of Pulmonary Arteriovenous Malformation in a Patient With Hereditary Hemorrhagic Telangiectasia Presenting With Stroke
Background Hereditary hemorrhagic telangiectasia (HHT) is associated with a high incidence of pulmonary arteriovenous malformations (PAVMs), which can be the underlying cause for cerebral ischemia or brain abscess. The diagnosis of these malformations may be difficult, as clinical or radiological findings may be absent. Transcranial Doppler ultrasound (TCD) with saline contrast and transesophageal echocardiography (TEE) with saline contrast are useful in identifying patients with right-to-left shunts and may help identify PAVMs.
Case Description A 68-year-old woman with HHT presented with two strokes over a 1-year period. After the first stroke, a transthoracic echocardiogram with saline contrast demonstrated significant right-to-left shunt that was interpreted as a patent foramen ovale. After the second stroke, a TCD contrast study confirmed this right-to-left shunt; however, a TEE contrast study discovered an extracardiac shunt. Pulmonary angiography revealed a left lower lobe PAVM and three telangiectasias involving the right lung. The PAVM was subsequently embolized. Postembolization radiographic imaging showed complete occlusion of the feeding vessel to the PAVM. However, repeated contrast TCD and TEE demonstrated persistent right-to-left shunting.
Conclusions In our patient, stroke may have resulted from peripheral venous emboli passing through the PAVM or from endogenous thromboemboli originating within the PAVM. TCD and TEE contrast studies were helpful in judging the efficacy of catheter embolization therapy of PAVM. TCD and TEE with saline contrast may be clinically useful follow-up examinations for recurrence or development of new PAVMs.
- cerebral arteriovenous malformations
- echocardiography, transesophageal
- telangiectasia, hereditary hemorrhagic
Hereditary hemorrhagic telangiectasia, or Osler-Weber-Rendu disease, is an autosomal, dominant, inherited disorder with high penetrance.1 It is characterized by multiple dermal, mucosal, and visceral telangiectasias associated with recurrent bleeding.2 Epistaxis is the most common form of presentation, although gastrointestinal hemorrhage, hematuria, or hemoptysis can occur.3
Neurological involvement in HHT is not uncommon, reported in approximately 4% to 12% of patients.4 5 6 Symptoms may be caused by central nervous system complications of associated PAVMs.3 6 A major right-to-left pulmonary shunt may provide the access for air embolism to the brain3 or for peripheral septic emboli to bypass the natural pulmonary capillary filter and lodge in the cerebral circulation, causing brain abscess.2 3 7 8 9 10 11 12 Paradoxical emboli from a PAVM causing cerebral infarction have also been described.13 14 15 TCD and TEE with saline contrast can detect right-to-left cardiac or pulmonary shunts.16 17 18 In the present article, we describe a patient with HHT, recurrent stroke, and PAVM in whom TCD and TEE with saline contrast were useful in detecting a significant right-to-left shunt before pulmonary angiography was performed. Furthermore, TCD and TEE both demonstrated residual right-to-left shunt after catheter embolization of the PAVM.
A 68-year-old left-handed woman developed acute vertigo with a right frontal headache and balance problems. There was no loss of consciousness, seizure activity, palpitations, or head injury. She noticed blurred vision in both left visual fields, as well as weakness and numbness of the left arm and leg. One year previously, she had suffered a stroke with Broca’s aphasia and mild left-side weakness. Investigations, including complete blood count, coagulation profile, cranial CT scan, and duplex Doppler carotid ultrasonography, were normal. Transthoracic echocardiography with saline contrast showed a significant right-to-left shunt that was interpreted as diagnostic of patent foramen ovale. She was taking antiplatelet medications at discharge.
Past medical history was significant for an episode of pneumonia with severe cough and severe hemoptysis 4 years previously. A 1.5-cm-diameter coin lesion in the left lower lobe was noted on chest x-ray with no change over a subsequent 2-year follow-up. Further questioning elicited a history of frequent epistaxis present for several years. Prophylactic cauterization of nasal vessels was necessary every 2 months. A history of frequent epistaxis was reported in her father, her son, and one or two relatives on the paternal side. She was unaware of the presence of telangiectasias in any of her family members.
On examination, multiple telangiectasias of the tongue and lips were noted. Similar telangiectasias were seen over the abdominal wall. A left homonymous superior quadrantanopsia was detected. The left hip flexor was minimally weak. On walking, mild circumduction of the left leg was noted. Deep tendon reflexes were brisk bilaterally with a slight increase on the left. Plantar responses were downgoing bilaterally. The remainder of the neurological examination was normal. Cardiac and pulmonary examinations were normal. There was no clubbing. Laboratory investigations including complete blood count, arterial blood gases, and coagulation profile were normal. She was diagnosed with HHT and a right cortical stroke.
A chest x-ray showed the 1.5-cm-diameter coin lesion in the left lower lobe with two vessels leading toward this nodule consistent with feeding and draining structures (Fig 1⇓).
A CT scan of the head showed an old right basal ganglia lacunar infarct. A new right posterior temporal and occipital infarct with a small area of increased density above the right petrous tip was present, which was consistent with a small hemorrhagic infarct, presumably secondary to an embolus.
Duplex Doppler carotid ultrasound results were unchanged from the previous study. A duplex Doppler ultrasound of the legs showed no evidence of a deep venous thrombosis.
TCD with saline contrast demonstrated a significant right-to-left shunt (Fig 2A⇓ and 2B⇓). TEE with saline contrast excluded a patent foramen ovale and an atrial septal defect but did demonstrate significant entry of saline contrast into the left atrium by route of the pulmonary veins; therefore, PAVM was deduced to be present.
Selective pulmonary angiography was undertaken. Angiography of the right main pulmonary artery demonstrated the presence of three small arteriovenous malformations: one each in the right upper lobe, right middle lobe, and right lower lobe. Radiographically, these appeared to be telangiectasias. Angiography of the left main pulmonary artery revealed a large simple H-type fistulous PAVM (Fig 3A⇓). No other arteriovenous malformations were seen.
The PAVM was embolized with multiple Gianturco Wallace coils. Imaging performed at the conclusion of the embolization procedure showed satisfactory total occlusion of the feeding vessel to the PAVM (Fig 3B⇑).
After embolization of the PAVM, contrast TCD showed persistent right-to-left shunt with no apparent difference in the intensity of the contrast effect (Fig 2C⇑). Repeated contrast TEE showed minimal residual extracardiac shunt entering from the right pulmonary veins (Fig 4⇓) and complete absence of saline contrast entering the left atrium from the left pulmonary veins.
No further neurological events have occurred in the subsequent 6 months after embolization of the PAVM.
The frequency of HHT is estimated to be 1 or 2 per 100 000.8 Rodes19 recognized the association between PAVM and HHT in 1938. In reported series, 30% to 50% of patients with PAVM have a family history of HHT, and 66% have telangiectasias on clinical examination. Thirty-six percent of patients with single PAVMs and 57% with multiple lesions are associated with HHT.2 3 8 20 21
In a review of the literature spanning 93 years and 91 patients, Roman et al3 reported that the most common neurological changes in HHT resulted from the presence of a PAVM; 41% of the patients with PAVM and HHT had neurological manifestations.
In a prospective study of 135 patients with HHT using MRI of the brain and pulmonary angiography, Fayad et al22 found that the presence of PAVM, but not cerebral vascular malformations, increased the risk for cerebral infarct and brain abscess.
The right-to-left shunt from a PAVM may contribute to decreased arterial oxygen saturation causing symptoms of headache, syncope, diplopia, vertigo, visual and auditory disturbances, dysarthria, focal or generalized seizures, and paresthesias and pareses. Postulated mechanisms for stroke include cerebral thrombosis secondary to polycythemia from hypoxia; air embolism to the brain from the entrance of air into the circulation through a defect in the wall of the PAVM, especially during episodes of hemoptysis; thromboemboli arising within the pulmonary fistula; and septic emboli bypassing the filter of the pulmonary circulation passing directly into the systemic arterial circulation, causing brain abscesses.3 The incidence of brain abscess with PAVM has been reported to vary between 5% and 6%.8
In our patient, we postulate that peripheral venous emboli may have crossed the PAVM or that thromboemboli may have arisen from within the PAVM itself, resulting in embolic infarction. Stanley and Hunter,23 in the pre-CT era, reported a patient and his mother with HHT, PAVM, and presumed embolic strokes. The patient had several episodes of limb weakness and numbness. A cerebral angiogram was normal with no evidence of intracranial pathology. He remained symptom-free for 1 year after thoracotomy and removal of the PAVM. The patient’s mother had developed an acute episode of right hemiplegia with slow resolution over 2 years. After lobectomy for a PAVM, she remained symptom-free for 17 years. Love et al21 described a 49-year-old man presenting with strokes, HHT, and PAVM. Surgical resection of the PAVM resulted in an 18-month symptom-free follow-up period. These three patients would support our theory that peripheral venous emboli or endogenous thromboemboli may cross the PAVM, resulting in stroke.
With the high degree of neurological complications associated with PAVM and a large right-to-left shunt, it would seem prudent to find a safe and relatively simple but effective method for identifying the presence of such a shunt. In our patient, transthoracic echocardiography with saline contrast performed after the first stroke was inadequate in defining the cause of the right-to-left shunt; TEE was able to disprove the previously misdiagnosed patent foramen ovale. Pulmonary angiography has traditionally been recognized as the definitive test for identification of PAVMs,20 21 24 25 and embolization has been proven to successfully occlude feeding vessels.20 25 However, our patient’s case demonstrates that pulmonary angiography can adequately delineate the appearance of PAVMs but is unable to correlate the anatomic appearance with the physiological degree of right-to-left shunt.
Both TCD and TEE with saline contrast are useful for detection of right-to-left shunts in patients with cerebral ischemia. They may be useful procedures for assessing the effectiveness of embolization therapy of PAVMs and in following up patients for possible recurrence or development of new PAVMs. TEE has the advantage of defining the etiology of the shunt, such as atrial septal defect, patent foramen ovale, and PAVM. However, TCD with saline contrast is a simple bedside procedure and involves minimal discomfort for the patient compared with TEE. Contrast TCD also provides evidence of direct potential involvement of the cerebral arterial circulation.17
TCD contrast studies may be a useful preliminary, noninvasive, bedside tool for detecting the presence of a potentially treatable right-to-left shunt in families with HHT. If a shunt is detected by TCD, definitive testing with TEE contrast studies would demonstrate the exact mechanism of the shunt.
Selected Abbreviations and Acronyms
|HHT||=||hereditary hemorrhagic telangiectasia|
|PAVM||=||pulmonary arteriovenous malformation|
|TCD||=||transcranial Doppler ultrasound|
This study was supported in part by The Heart and Stroke Foundation of Canada and by a postgraduate clinical research fellowship from the College of Medicine Academic Enrichment Fund, University of Saskatchewan, Saskatoon, Saskatchewan (Dr Yeung).
Reprint requests to A. Shuaib, MD, Department of Medicine, Division of Neurology, Royal University Hospital, University of Saskatchewan, 103 Hospital Dr, Saskatoon, Saskatchewan, Canada S7N 0W8.
- Received April 11, 1995.
- Revision received June 26, 1995.
- Accepted June 26, 1995.
- Copyright © 1995 by American Heart Association
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