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Ann Thorac Surg 1997;64:930-939
© 1997 The Society of Thoracic Surgeons
Departments of Diagnostic Radiology, Medicine, Pulmonary and Critical Care, and Neurology, Yale University School of Medicine, New Haven, Connecticut
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Abstract |
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 TopFootnotes Abstract IntroductionMaterial and MethodsResultsCommentAcknowledgmentsReferences |
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Methods. From a data base of 221 consecutive patients with PAVMs treated by embolotherapy between 1978 and 1995, 45 patients with 52 PAVMs, supplied by feeding arteries 8 mm in diameter or larger, were selected for a retrospective investigation.
Results. Of 45 patients with 52 large PAVMs, 38 patients (84%) with 44 PAVMs (85%) were cured by the first embolotherapy (mean follow-up, 4.7 years). Acute periprocedural complications included self-limited pleurisy (31%), angina secondary to air embolus (2%), and paradoxical embolization of a device during deployment (4%). None of these events led to short- or long-term sequelae. Seven patients (16%) had persistence of the PAVM attributable to either recanalization (n = 4) or interim accessory artery growth (n = 3). Two of these patients presented with ischemic stroke several years after the initial treatment. Persistent PAVMs (n = 8) were retreated successfully by a second procedure (n = 7), or a third procedure (n = 1) (mean follow-up, 5.9 and 5.3 years, respectively).
Conclusions. Embolotherapy of large PAVMs results in permanent occlusion in an overwhelming majority of patients. Continued patency due to recanalization or accessory artery growth is easily detected and treated.
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Introduction |
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TopFootnotesAbstractIntroductionMaterial and MethodsResultsCommentAcknowledgmentsReferences |
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Pulmonary arteriovenous malformations (PAVMs) are direct connections between a branch of a pulmonary artery and vein through a thin-walled aneurysm. They act as direct right-to-left shunts, resulting in dyspnea, fatigue, cyanosis, and polycythemia when the shunt is large. In addition, because the PAVM bypasses the capillary bed, the lung loses its filter function, thus allowing emboli and bacteria to pass directly into the systemic circulation, resulting in stroke or cerebral abscess [1].
Transcatheter embolization, using detachable balloons or stainless steel coils, is generally accepted as the treatment of choice for patients with multiple PAVMs, in whom surgical excision would sacrifice excessive lung tissue, as well as patients who are of poor surgical risk. Embolotherapy also provides potential advantages over surgical intervention, including lower postprocedural morbidity, and shorter hospital stays. Treatment for the solitary PAVM, however, remains a subject of debate.
As late as 1993, Puskas and colleagues [2] showed in a small series that surgical resection or ligation of PAVMs provides effective treatment of PAVMs. They contended that the risk of late balloon deflation, migration, and the lack of long-term follow-up favored operation as the treatment of choice. This study addresses the long-term efficacy issue by reporting the extended follow-up of patients treated for the largest, most complicated PAVMs in our experience. Several reports have previously described the immediate technical efficacy of embolotherapy with both balloons [3, 4] and coils [5, 6]; our study reports long-term follow-up.
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Material and Methods |
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TopFootnotesAbstractIntroductionMaterial and MethodsResultsCommentAcknowledgmentsReferences |
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The medical record was reviewed to obtain complete histories, physical examinations, laboratory test values, and procedural reports. All patients were contacted between October 1995 and October 1996. Current chest roentgenograms were requested as well as arterial blood gases. Updated clinical status was determined. Exercise intolerance in the history was defined as the presence of dyspnea, with or without exertion, or fatigue. Classification of PAVM angioarchitecture was based on an updated version of our 1983 description [7]. In our classification, a simple PAVM is supplied by one segmental artery, whereas the complex variety receives blood supply from two or more segmental arteries [7].
Technique
Technical details of embolization have been described previously at length [3, 4, 7]. All patients first underwent a complete diagnostic pulmonary angiogram with separate right and left injections before embolotherapy. This study provided the morphologic information needed to plan the embolization including approach and device selection. Patients were treated with either detachable balloons, coils, or both depending on vascular anatomy. In general, PAVMs with feeding artery diameters of 3 to 4 mm were treated with coils, those with feeding arteries ranging from 4 to 9 mm by detachable balloon only, and those more than 9 mm by either coils alone or by an overinflated detachable balloon impacted within a nest of coils.
During our 18-year transcatheter experience of closing PAVMs, the types of embolic devices have evolved and varied in availability. The original silicone mini-balloon (Becton-Dickenson) was used from 1978 until 1990. Patient 8 (Table 1
), treated in 1981, was the only patient with 12.9- and 10.2-mm diameter arteries occluded with a hand-tied, latex balloon filled with silicone gel. The detachable silicone balloon from Interventional Therapeutics Corporation (Fremont, CA) was used from 1991 to 1993. The latex gold-valve balloon (Ingenor, Paris, France) was used from 1994 to June 1996. The DSB is currently manufactured by TARGET Therapeutics (Fremont, CA) and is available worldwide except in the United States where it is still used under an investigational device exemption. As stainless steel coils were available before the device regulatory act of 1976, a premarket approval has never been required and they were continually available throughout the study. Use of coils, particularly the Gianturco Anderson Wallace coil, is widespread and their technical efficacy is well documented.
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Follow-up
Routine clinical follow-up consisted of history, chest roentgenograms or body computed tomographic scans, and arterial blood gas measurement. Follow-up in patients treated after 1991, when we began an investigational device exemption for the new detachable silicone balloon, included chest roentgenograms and arterial blood gases at 1 month, 6 to 12 months, and every 3 to 5 years thereafter.
Primary emphasis on evaluation of treatment was placed on chest roentgenograms because of universal availability. Although a less than perfectly sensitive or specific exam, the chest roentgenogram has proven, in our experience, to be an effective method of follow-up when combined with clinical history, physical examination, and arterial blood gases [3, 4, 7–10]. Resolution of the PAVM was considered complete if the aneurysm disappeared or was markedly diminished in size with corroboration by stable postocclusion arterial oxygen tension values (Figs 1 and 2). Arterial blood oxygen content has been used extensively by ourselves and others to evaluate results. Changes in serial oxygen content reflect the total shunt attributable to all PAVMs and not necessarily the large feeding artery PAVMs of interest. For this reason, blood gas measurements were used primarily as an adjunctive mode of assessment and, when discrepant, led to more precise studies such as computed tomography or angiography.
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). Smaller PAVMs (3 to 7.9 mm in diameter) in these patients did not enter data analysis, nor did subsequent admissions for the treatment of PAVMs other than the original, large artery PAVMs.
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) or at least 70% reduction in size of both the PAVM and draining vein accompanied by stable arterial oxygen tension values (Figs 2 and 3). To assess serial partial pressure of oxygen measurements, values were grouped into four time brackets: within 0 to 1 year, 1 to 5 years, 6 to 9 years, and greater than 10 years after the initial treatment date. It was presumed that patients who were asymptomatic during a given time bracket and lacked arterial blood gas measurement, but registered a normal partial pressure of oxygen in a later time bracket, had normal blood oxygenation in the previous time period. Partial pressure of oxygen values were then applied to the previous time bracket for data analysis.
To examine the possibility of an improvement of long-term outcome with increased physician technical experience, a possible "learning curve" effect, data analysis included division of the study group into those treated before 1988 and those treated thereafter. Patients were also divided into those with solitary and multiple PAVMs to evaluate the possible effect of multiplicity and complexity on recurrence. In this series, patients with solitary PAVMs were those who presented with one large PAVM as the primary manifestation of pulmonary disease. Patients with additional PAVMs supplied by arteries larger than 3 mm and less than 8 mm in diameter, were classified as "multiple" in status, as they too had to be treated. The 
2 test was used to evaluate the statistical significance of both these factors.
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Results |
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TopFootnotesAbstractIntroductionMaterial and MethodsResultsCommentAcknowledgmentsReferences |
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In the 45 patients comprising the study group, 52 PAVMs with feeding arteries exceeding 8 mm were occluded. Table 1 illustrates treatment profiles and follow-up. Of the 52 PAVMs, 35 (67%) were classified as simple, whereas 17 (33%) were complex. The lower lobes were the site of 69% of large PAVMs. An additional 45 smaller PAVMs (<8 mm) were also occluded, yielding a total of 97 treated PAVMs. An overinflated detachable silicone balloon, impacted in coils, was used to occlude 21 PAVMs (40%), a detachable silicone balloon only in 15 PAVMs (29%), and coils only in 16 PAVMs (31%). The technical success rate was 98% in that only one PAVM was not occluded successfully on the initial attempt. Follow-up ranged from 0.8 to 14 years and was complete in all patients. Current chest roentgenograms (1995 or 1996) were obtained from the 42 living patients. In the 3 patients who had since died from other medical conditions, examinations obtained during their terminal illness were reviewed.
Of the 45 patients with 52 PAVMs treated, 38 patients (84%) and 44 PAVMs (85%) achieved successful long-term resolution of the PAVM, with mean follow-up of 4.7 years. Although long-term arterial blood gas follow-up was not performed in each patient, the data obtained did show remarkable stability. Overall arterial blood gas oxygen levels improved by 49% (p < 0.05), from an average of 56.6 mm Hg before embolization to 84.1 mm Hg immediately after embolization. For those patients with follow-up arterial blood gases taken within 1 year, between 1 and 5 years, between 6 and 9 years, and more than 9 years, the mean follow-up values were 86.3 (n = 27, p < 0.05), 84.8 (n = 17, p < 0.05), 88.3 (n = 7), and 82.2 (n = 4), respectively.
Of the 45 patients in our study, only 7 patients (16%) with 8 PAVMs (15%) had persistence of the originally occluded PAVM. Of the eight persistent PAVMs, five (10%) had recanalization of the originally occluded feeding artery, whereas three (5%) exhibited interval growth of an accessory vessel. All persistent PAVMs were retreated successfully by a second procedure (7 of 8 PAVMs, 87.5%) or a third procedure (1 of 8 PAVMs, 12.5%), with a mean follow-up of 5.8 and 5.3 years, respectively. Unfortunately, 2 of these patients (4.4%) experienced interim ischemic strokes. One of these patients experienced recanalization of the originally occluded artery, whereas the other patient demonstrated interim growth of an accessory feeding artery.
Four patients (9%), or 5 of 52 PAVMs (10%) had recanalization of the originally occluded feeding artery (Table 2). All 4 of these patients vaguely reported the recurrence of dyspnea and fatigue within 1 year, if not several weeks after the embolization. One patient (No. 7) suffered an interim stroke 2 years after initial treatment, and was thereafter admitted for repeat occlusion. Of these five recanalized PAVMs, two (40%) had been occluded by balloon only, two (40%) by coils only, and one (20%) by balloon/coil nest occlusion. In all patients, repeat angiography demonstrated either deflation of the balloon or flow through the originally placed coils.
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Three years later, in 1988, the patient returned with complaints of shortness of breath worsening over the past 5 months. Repeat study showed continued occlusion of the right upper lobe PAVM and persistence of the right lower lobe PAVM, as well as the existence of an additional right mid lobe PAVM that had been missed previously because of overlapping anatomy. Both were occluded with nests of multiple 8- to 12-mm coils. Patient reported improvement of symptoms for 1 week followed by the slow return of symptoms over 1 year. Repeat study in 1990 showed another recanalization of the right lower lobe PAVM, as well as newly diagnosed pulmonary hypertension (pulmonary artery pressure, 70/32 mm Hg), which was later confirmed to be attributable to mitral stenosis. The right lower lobe PAVM was reoccluded with the addition of several more large coils. The patient underwent balloon mitral valvuloplasty and has since been asymptomatic. Follow-up chest roentgenogram 5 years after embolization showed resolution of all previously occluded PAVMs.
Three patients (7%), with three PAVMs (5%), exhibited persistence of the PAVM secondary to interval growth of accessory vessels. Two of the patients presented with dyspnea, and 1 patient presented with embolic stroke (No. 31) (Tables 1 and 2). These patients returned for accessory vessel embolization and subsequent resolution of the PAVM with a mean follow-up of 6.7 years (Fig 3).
To investigate an improvement in long-term outcome with operator experience, patients were also divided into those treated in the years up to 1988 and those treated thereafter. Sixteen patients, with 19 PAVMs, were treated in the first period, of which there were two episodes of recanalization (12.5% of patients, 16% of PAVMs). Twenty-nine patients with 33 PAVMs were treated in the second period, yielding two episodes of recanalization (7% of patients, 6% of PAVMs). This improvement was not statistically significant.
To investigate the effect of disease multiplicity on patient outcome, we also divided patients into those with solitary PAVMs and those exhibiting multiplicity. Of the 23 patients presenting with solitary PAVMs, 21 patients (91%), or 21 PAVMs (91%), were permanently cured by the first transcatheter embolotherapy. Twenty-two patients, with 29 large PAVMs, presented with multiple PAVMs. In this subset, 17 patients (77%), or 23 PAVMs (79%) were permanently occluded after one embolization. This improvement with solitary PAVMs was not statistically significant. In addition, 45 PAVMs (with arteries 3 to 7.9 mm in diameter), were occluded in the patients with multiple PAVMs. Although the 45 additional PAVMs were not included in our data analysis, no episodes of recanalization were noted among them.
Finally, 8 patients within our study group were treated for PAVMs using the gold valve balloon, a device with a radiopaque marker allowing radiographic location after deflation. All of these patients have been treated within the last 2 to 3 years with no reports of the return of symptoms thus far. Follow-up chest roentgenograms in all these patients show deflation of the balloon, most deflating by 1 month after occlusion, and resolution of the PAVM. In none of these cases did the balloon migrate after deflation (Fig 1).
Complications
SELF-LIMITED PLEURISY.
Fourteen patients (31%) experienced self-limited pleurisy, which occurred within the first week after embolization, most often within the first 48 hours. Pleurisy lasted between 3 and 6 days and was sometimes accompanied by a mild fever. Postprocedural pleurisy most likely results from thrombosis of a pleural-based aneurysm or several normal branches with subsequent localized pulmonary infarction.
AIR EMBOLUS.
Air embolus occurs when the catheter wedges during coil occlusion and air is introduced during repeated introduction of coils [4]. This phenomenon is much more common when occluding small PAVMs, 3 to 4 mm in diameter, with coils rather than DSB [7]. Resulting symptoms included perioral paresthesia, angina, or transient electrocardiographic changes lasting up to 20 minutes. Only 1 patient (2%) experienced angina during embolization. This patient was treated with oxygen by mask and intravenous atropine for bradycardia. All changes were reversible, and the procedure was completed.
PARADOXICAL EMBOLIZATION OF A DEVICE.
Paradoxical device embolization occurred in 2 patients (4%) early in our experience [3]. In the first patient, inadvertent detachment occurred during maneuvering of an inflated balloon within the aneurysm rather than in the feeding artery. The balloon subsequently traveled to and lodged within the posterior division of the left internal iliac artery and was associated with no symptoms. In the second patient, a balloon migrated to a peripheral branch of the hepatic artery during the procedure without sequelae. No attempt was made to retrieve the balloon, and these patients suffered no long-term effects. In addition, no late migration (>24 hours) of either balloons or coils was encountered in our study.
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Comment |
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TopFootnotesAbstractIntroductionMaterial and MethodsResultsCommentAcknowledgmentsReferences |
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Of the 45 patients treated and 52 feeding arteries occluded, 84% of patients and 85% of PAVMs were permanently occluded and cured on the first attempt, with a mean follow-up of 4.7 years. Only 4 patients (9%) with 5 PAVMs (10%) had recanalization of an originally occluded feeding artery. These patients were retreated with a secondary permanent occlusion rate of 80% and a mean follow-up of 5.3 years. Patients with interval growth of an accessory vessel (7% of patients, 5% of PAVMs) were likewise retreated with a secondary permanent occlusion rate of 100% and a mean follow-up of 6.7 years. None of the patients in this series, nor any in our experience, required operation because of failed embolotherapy.
Two important teaching points are illustrated by the 2 patients who experienced a stroke in the interval between their initial and their second embolization to retreat a still patent PAVM. First, all feeding vessels exceeding a critical diameter of 3 mm must be occluded. Patient 31 was treated before our establishment of the size threshold [7, 8], and retrospective examination of the first diagnostic angiogram revealed a feeding artery of 3.5 mm left unoccluded for perceived insignificance [7, 8]. Regular follow-up is therefore necessary to document resolution of the PAVM. Second, it has been documented that untreated PAVMs grow with time and accessory arteries capable of supplying the occluded PAVM may not be demonstrated at the time of the first embolotherapy [10–12]. In high-risk patients, such as those with hereditary hemorrhagic telangiectasia, diligent follow-up is required to monitor enlargement of previously undetected or clinically insignificant PAVMs. We recommend chest roentgenograms and arterial blood gas measurements at 1 month and 1 year after occlusion, and spiral computed tomography every 3 to 5 years thereafter to monitor growth of small PAVMs.
Animal studies of the pathology of balloon occlusion do not reveal late migration of balloons deflating 21 days or longer after placement [9]. Once a detachable silicone balloon is securely placed in an artery, organized thrombus forms on either side of the balloon extending to the first proximal and distal arterial branch point. Balloons therefore, act like absorbable sutures and need not remain inflated after thrombosis. The animal experience is borne out by our long-term studies in humans in which Sitko and colleagues [10] demonstrated that 83 of 85 detachable silicone balloons placed in patients remained inflated 2 to 4 years after placement. In our study, we had 2 patients exhibiting return of symptoms at roughly 1.5 and 3 years. Although we are without a definite explanation, we contend that "late" balloon deflation actually occurs at a much earlier date and goes undetected, perhaps attributable to partial artery thrombosis and the protracted, gradual return of symptoms. Follow-up data from Sitko [10] and Pollak [4] and their colleagues confirm our experimental observations in animals and support the concept of a 21-day threshold for permanent occlusion.
This understanding of the pathology of balloon embolization forms the basis of chest roentgenogram-based follow-up. In the vast majority of patients, the aneurysm retracts and is replaced by a fibrous scar on chest roentgenogram. In a small percentage of patients, particularly those with very large PAVMs, remnant fibrous tissue or calcified thrombus (Fig 2) may be large enough to resemble persistent flow through an aneurysm on a chest roentgenogram. When this occurs, corroboration of occlusion by arterial oxygen tension or angiography is necessary to rule out persistent flow. In our experience, the chest roentgenogram, in combination with arterial oxygen tension when available or necessary, has provided excellent results. Of the 38 patients with 44 PAVMS in our study permanently cured by the first treatment, the aneurysm subtended by the occluding device disappeared in 40 PAVMs, whereas only 4 patients with four PAVMs had slight residual or calcified thrombus. Resolution of the PAVM was corroborated by arterial oxygen values that did not change significantly from values immediately after occlusion.
In addition, balloon "disappearance" on a chest roentgenogram does not mean balloon migration. Loss of contrast material by either balloon rupture or slow leakage will make the balloon radiographically undetectable despite secure placement and fixation in organized thrombus. Our experience with the gold-valve balloon illustrates this point well (Fig 1). This device has a radioopaque marker within the balloon that allows localization regardless of inflation status. From our experience, gold valve balloons usually deflate at 1 month after deployment secondary to a slow leak. Early follow-up radiographs from our gold valve balloon-treated patients demonstrated that all deflated balloons remained securely in place, as indicated by the radioopaque bead within the deflated shell (see Fig 1).
Our only experiences with balloon or coil migration have occurred during deployment. This can be secondary to misjudgment of balloon location, suboptimal fluoroscopic views, difficulty of access secondary to complex tortuous anatomy, or undersizing of the balloon or coil for the artery. Although the improvement in long-term outcome with operator experience and disease simplicity was not statistically significant in this report, we believe that a larger study group would yield statistical significance. We therefore, advocate the establishment of specialized "centers of excellence" where PAVM embolotherapy is performed frequently enough to acquire proficiency.
Proper device selection is also critical. We strongly believe that operators should have equal access to and facility with both detachable balloons and coils, as each have respective advantages in certain anatomic settings [7]. Devices must also be of proper size. Balloons should not be inflated to volumes beyond the manufacturer's specifications, and isoosmotic contrast material should be used to fill the balloon as silicone is a semipermeable membrane [13]. Our group prefers detachable balloons as they allow both flow direction and immediate, complete, cross-sectional occlusion.
In summary, our long-term follow-up study suggests that embolotherapy is safe and durable, with persistent PAVMs easily retreated by an overnight admission and a secondary embolization procedure. It is clear that embolotherapy proves to be efficacious with even the largest solitary PAVMs and therefore, constitutes a universal, primary mode of therapy. Surgical resection of a solitary PAVM is also efficacious [2], but the advantages of transcatheter embolotherapy, including lower procedural morbidity, shorter time in the hospital, and rapid return to work, favor embolotherapy. Furthermore, the procedure is repeated easily over time as other PAVMs with arteries 3 mm or greater in diameter develop. This is the size associated with paradoxic embolization and neurologic events [7]. Regular follow-up is necessary to document resolution and to monitor interval growth of small PAVMs.
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Acknowledgments |
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TopFootnotesAbstractIntroductionMaterial and MethodsResultsCommentAcknowledgmentsReferences |
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Address reprint requests to Dr White, Department of Diagnostic Radiology, 333 Cedar St, PO Box 208042, New Haven, CT 06520-8042.
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