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Pulmonary Arteriovenous Malformation Treated with Embolotherapy: Systemic Collateral Supply at Multidetector CT Angiography after 2–20-year Follow-up¹

¹ From the Department of Thoracic Imaging, Calmette Hospital, University Center of Lille, Boulevard Jules Leclerc, 59037, Lille Cedex, France (P.Y.B., P.D., N.B., J.R., M.R.); Department of Medical Statistics, University of Lille, Lille, France (A.D.); and Department of Radiology, Cardiologic Hospital, Pessac, France (F.L.). Received September 10, 2004; revision requested November 18; revision received February 24, 2006; accepted March 22; final version accepted April 18. Address correspondence to M.R. (e-mail: mremy-jardin{at}chru-lille.fr).

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION References

 
Purpose: To retrospectively evaluate frequency of systemic arterial collateral supply to treated pulmonary arteriovenous malformations (PAVMs) in long-term follow-up with multi–detector row helical computed tomography (CT).

Materials and Methods: Institutional review board approval was obtained, with waiver of informed consent. Thirty-two patients (19 male, 13 female; mean age, 43 years) underwent follow-up multi–detector row helical CT angiography of the chest (collimation, 16 x 0.75 mm) 2 or more years after embolotherapy of PAVMs. The study group had a history of successful embolotherapy of 53 PAVMs and a mean of 9 years of follow-up (range, 2–20 years). A search for abnormal systemic arteries was based on analysis of thin-collimated contiguous transverse CT scans and two- and three-dimensional images including maximum intensity projections and volume-rendered images. Statistical comparison was performed with the Fisher exact test (categoric variables) and Wilcoxon rank sum test (continuous variables).

Results: At CT, 13 patients (group 1) had abnormally enlarged systemic arteries and 19 patients (group 2) had no abnormal arteries. In group 1, 32 abnormally enlarged arteries were seen—five bronchial and 27 nonbronchial arteries (14 inferior phrenic, six musculophrenic, five internal mammary, two intercostal). The degree of enlargement was moderate for 26 arteries and marked for six. There were no significant differences between groups for (a) clinical characteristics of patients, including history of surgery before or after embolotherapy (P = .7); (b) anatomic structures of treated PAVMs; and (c) embolization procedures and their effectiveness. The number of patients with features suggestive of lung infarction in the days or months after embolotherapy was significantly higher in group 1 (P = .04). On CT angiograms, the number of patients with features suggestive of sequelae of lung infarction was significantly higher in group 1 (P = .02). There were no symptomatic differences attributable to systemic collateral supply between groups; in particular, there was no hemoptysis in group 1.

Conclusion: Abnormally enlarged systemic arteries were present in 13 of 32 patients, in whom there was a significantly higher frequency of clinical and/or radiographic features suggestive of lung infarction after embolotherapy.

© RSNA, 2006

	INTRODUCTION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION References

 
A pulmonary arteriovenous malformation (PAVM) is an abnormal connection between a branch of a pulmonary artery and a pulmonary vein through a thin-walled aneurysmal sac (1,2). PAVMs are most commonly congenital in nature and have a strong relationship with the syndrome of hereditary hemorrhagic telangiectasia (HHT) (3,4). Since the early 1980s, embolotherapy performed by using stainless steel coils or detachable balloons has been accepted as the treatment of choice for the majority of patients with PAVMs; this procedure minimizes the risk of cerebral embolization and abscess formation without loss of pulmonary parenchyma (1,5–9). Authors of long-term follow-up studies have documented the efficacy of embolotherapy in the treatment of PAVMs, with permanent involution of the majority of treated malformations (2,8–13) and a limited proportion of reperfusion of PAVMs (1,2,13–17). However, a precise analysis of the outcome of treated PAVMs was not possible before the introduction of helical computed tomography (CT), which enabled analysis of the morphologic changes at the level of the pulmonary vessels (2,16).

The advent of multi–detector row helical CT has further improved this approach by enabling a simultaneous evaluation of pulmonary and systemic vessels during the same acquisition. Thus, the purpose of this study was to retrospectively evaluate the frequency of systemic arterial collateral supply to treated PAVMs after long-term follow-up with multi–detector row helical CT.

	MATERIALS AND METHODS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION References

 
Study Group
The criteria for inclusion in the present study included the following: (a) a previous history of embolotherapy of one or multiple PAVMs, (b) an interval of at least 2 years between treatment and follow-up, and (c) follow-up with multi–detector row helical CT angiography. The study group was obtained from an initial group of 63 patients who had undergone embolotherapy in the Department of Thoracic Imaging at Calmette Hospital between 1982 and 2003. Among them, 31 patients were not eligible for inclusion because of one or more of the following reasons: (a) the patient was lost to follow-up (n = 18); (b) the interval between embolotherapy and CT follow-up was less than 2 years (n = 6); (c) nonenhanced multi–detector row helical CT follow-up (n = 7) was performed because of a previous history of allergy to iodinated contrast agents (n = 4) or poor venous access (n = 2); or (d) pregnancy (n = 1).

Our study group included 32 patients (19 female and 13 male) with a mean age (± standard deviation) of 43 years ± 13.7 (range, 17–71 years). At the time of initial presentation, 21 patients (66%) were asymptomatic, which included 14 patients who were referred for chest abnormalities at radiography and seven patients who were referred in the context of a family screening program for HHT. The other 11 patients had symptoms that prompted them to seek medical attention, which included pulmonary (n = 3), cerebral (n = 7), or abdominal (n = 1) complaints. In 78% of the cases (25 patients), the diagnosis of HHT was established based on the presence of three of four key features for this diagnosis—namely, spontaneous recurrent epistaxis, telangiectases at characteristic sites, a visceral manifestation (gastrointestinal telangiectasis with or without bleeding, PAVM, hepatic arteriovenous malformation, cerebral arteriovenous malformation, or spinal arteriovenous malformation), and an affected first-degree relative (18).

Prior to the introduction of multi–detector row helical CT technology, each patient referred for the follow-up of treated PAVMs in our institution underwent a nonenhanced helical CT follow-up examination, which was indicated every 2–5 years, as recommended in the literature (2,19). Because contrast material–enhanced multi–detector row helical CT can provide additional information regarding the outcome of occluded PAVMs, the inclusion of a CT angiography study was approved by our institutional review board and ethics committee in the clinical context of treated PAVMs and patient care, with waiver of informed consent. Care was taken to avoid administration of contrast material where contraindications existed, such as renal insufficiency (ie, creatinemia level higher than 150 µmol/L), iodine intolerance, and use of metformin or biguanide in cases of diabetes mellitus. Owing to the presence of a right-to-left shunt through the PAVMs, specific attention was directed toward excluding residual air bubbles in the syringe of the power injector and its connecting tube before administration of contrast material. The present investigation was a retrospective review of pretherapeutic and follow-up imaging studies obtained in the study group.

Therapeutic Modalities of PAVMs
The study group comprised the following: (a) 24 patients who underwent embolotherapy alone; (b) six patients who first underwent surgery (one patient underwent resection of one right-sided and one left-sided PAVM, three underwent a segmentectomy, one underwent a right-sided lobectomy and an aneurysmal resection during the same procedure, and one underwent a lobectomy) and then underwent embolotherapy for the treatment of additional PAVMs; (c) and two patients, each with a single PAVM, who underwent embolotherapy and then surgery because of the interim growth of an additional feeding artery in one patient and the systemic reperfusion of the PAVM in the other patient, 3 and 2 years, respectively, after embolotherapy; these two cases have already been reported (16). The mean interval between surgery and multi–detector row helical CT angiography was 14.2 years ± 6.7 (range, 7–27 years); in the case of multiple surgical procedures, the date of the first procedure was considered for this calculation.

The 32 patients had a total of 62 PAVMs with feeding arteries 3 mm in diameter or larger, which justified embolotherapy (1). Apart from nine PAVMs that remained untreated, 53 PAVMs were treated with embolotherapy. Among them, 51 PAVMs were treated exclusively by means of embolization, whereas two PAVMs were treated initially by means of embolotherapy and then by means of surgery because of failure of the endovascular treatment. For each PAVM treated by means of embolotherapy, the pulmonary arterial circulation was occluded by using a similar technique that was based on the use of steel coils (Cook, Bloomington, Ind) deposited in the feeding artery after superselective catheterization with a 7-F radiopaque nontapered catheter with an end hole. Once flow had ceased, as noted by means of a test injection of contrast material or acquisition of a control angiogram, the procedure was stopped. For the purpose of the present investigation, the most proximal level of occlusion of the pulmonary arterial bed enabling cessation of the PAVM perfusion was retrospectively assessed on the follow-up conventional angiograms that were systematically obtained at the end of the embolization procedure.

In patients who underwent several embolization procedures, the time between procedures did not exceed 1 year. The mean interval between embolotherapy and multi–detector row helical CT angiography was 9 years ± 4.7 (range, 2–20 years); in case of multiple endovascular procedures, the date of the first procedure was considered for this calculation. The mean number of occluded PAVMs per patient was 1.65 ± 1 (range, 1–4 PAVMs), and the mean number of embolotherapy sessions per patient of was 1.17 ± 0.4 (range, 1–4 sessions).

On the basis of systematic follow-up by treating physicians in the 3 months following embolotherapy, the retrospective search for features suggestive of lung infarction that might have occurred in the days or months following embolotherapy was possible for each patient. The features suggestive of lung infarction included pleuritic chest pain that occurred as an isolated finding or in association with ipsilateral radiographic abnormalities.

Pretherapeutic Anatomic Characteristics of PAVMs Treated with Embolotherapy
The anatomic characteristics of the 53 PAVMs treated with embolotherapy were assessed on pretherapeutic CT scans (n = 51) or on pulmonary angiograms (n = 2) whenever CT was not performed prior to embolotherapy. Owing to technologic improvement over time, pretherapeutic evaluation with CT was obtained with sequential CT (Elscint 2400, Elscint, Haifa, Israel; or DRH, Siemens, Erlangen, Germany) for 10 PAVMs and helical CT (Somatom Plus and Volume Zoom; Siemens) for 41 PAVMs, all of which consisted of thick-collimation, contiguous, nonenhanced CT examinations.

The anatomic characteristics of the PAVMs were analyzed by means of consensus between two readers (one radiologist [P.Y.B.] and one pulmonologist [P.D.], with 5 and 2 years of experience, respectively, who were trained in the reading of CT scans of patients with PAVMs) who were also involved in the interpretations of postembolotherapy CT angiograms; in cases of discordant interpretations, final consensus was reached with a third reader (M.R.), who was a faculty radiologist with 15 years of experience in CT angiography of the chest.

The following parameters were analyzed by the readers: (a) size of the PAVM; (b) lobar location of the PAVM; (c) central or peripheral location of the PAVM within the lung parenchyma (peripheral lung was defined as the outer 4 cm of the lung parenchyma deep to the visceral pleura and central lung was defined as the more centrally located lung parenchyma); (d) angioarchitecture of the PAVM, which was assessed by using the CT criteria of Remy et al (2); in the simple type of PAVM, a single artery feeds an aneurysmal communication with a single draining vein, while in the complex type, one or more pulmonary artery branches communicate with a PAVM with two or more draining veins (in cases of complex PAVMs, the readers noted the number of feeding arteries); and (e) diameter of the feeding arteries (<3 mm, 3–5 mm, or >5 mm). On pretherapeutic CT scans, these parameters were analyzed on lung images with measurements made by using calipers. On diagnostic angiograms, this information was obtained from the analysis of unilateral pulmonary angiograms obtained with a conventional technique in each lung, completed by means of the analysis of the hyperselective angiograms obtained prior to the deposition of steel coils. Care was taken to measure the diameter of the PAVM and vascular pedicles on angiograms after correction of geometric magnification.

Multi–Detector Row Helical CT Angiography
CT protocol.—CT angiography was performed with a 16–detector row scanner (Sensation 16; Siemens) by using the following scanning parameters: collimation, 16 x 0.75 mm; pitch, 1.5; rotation time, 0.5 second; 120 kV; and 70–120 mAs. The region scanned extended from the cervicothoracic junction to the upper abdomen (ie, down to the level of the renal pedicles) in order to survey all systemic arteries potentially involved in an abnormal systemic collateral supply to the lungs. Every examination was performed at deep inspiration, and a dose-reduction technique based on online tube-current control (Care Dose system; Siemens) was applied.

Patients received 80–100 mL of contrast material that contained 300 mg of iodine per milliliter, with an injection rate of 4 mL/sec. The automatic bolus triggering software program available on our CT unit (Care Bolus; Siemens) was systematically applied with a circular region of interest positioned at the level of the ascending aorta and a threshold for triggering data acquisition preset at 100 HU.

From each data set, three series of images were systematically reconstructed: contiguous 3-mm-thick transverse CT scans viewed at mediastinal and lung window settings, oblique coronal and sagittal maximum intensity projections, and volume-rendered images of the thoracic vascular structures reconstructed from overlapping thin sections (0.75-mm-thick transverse sections reconstructed at 0.5 mm intervals). Three-dimensional reconstructions were generated at commercially available workstations (Wizard and Leonardo consoles; Siemens) by experienced technologists (5–10 years of experience with helical CT angiography). The transverse CT scans and three-dimensional reformations were printed as laser-film hard-copy images by using standardized lung and mediastinal window settings with a photographic format of 20 images per sheet of film.

Image interpretation.—Two of the readers who had been involved in the interpretations of pretherapeutic examination images retrospectively evaluated the CT angiograms by means of consensus (one radiologist [P.Y.B., with 5 years of experience] and one pulmonologist [P.D., with 2 years of experience] trained in the reading of CT scans of patients with PAVMs). In cases of discordant interpretations, final consensus was reached with a third reader (M.R.) who was a faculty radiologist with 15 years of experience with CT angiography of the chest. The CT images were reviewed as hard-copy images with the option of using a cine-mode display at the workstation if needed. The two readers were blinded to the clinical history of the patient.

CT parameters evaluated.—The first CT parameter evaluated was the abnormal enlargement of systemic arteries. CT angiograms were assessed for the presence of enlarged (diameter, >2 mm) right and/or left bronchial arteries that manifested as enhancing, small, round or curvilinear structures in the mediastinum and also identified along the bilateral main bronchi (20–22). Enlargement of bronchial arteries was graded as moderate when the bronchial artery diameter was between 2 and 4 mm and as marked when the diameter was larger than 4 mm, which was estimated by means of comparison with reference CT images of normal-sized, moderately enlarged, and markedly enlarged bronchial arteries on transverse sections (these reference images were not obtained in the study group); the number of abnormally enlarged right and/or left bronchial arteries was systematically recorded.

Nonbronchial systemic arteries are defined as arteries that enter the parenchyma via the pulmonary ligament or the adherent pleura; their course is not parallel to that of the bronchi (23). Abnormal enlargement of one or several of the following arteries was considered to be suggestive of a nonbronchial systemic arterial supply: the branches of the subclavian and axillary arteries, particularly the internal mammary arteries and their terminal branches (ie, the musculophrenic arteries); intercostal arteries; and the inferior phrenic arteries. Abnormal enlargement of these vessels on CT angiograms was estimated by comparison with reference CT images of normal-sized, moderately enlarged, and markedly enlarged nonbronchial systemic arteries on transverse sections by using the following grading system: Enlargement of the internal mammary arteries and intercostal arteries was defined as an arterial diameter of 2 mm or larger; the enlargement was graded as moderate when the arterial diameter was between 2 and 4 mm and as marked when the diameter was larger than 4 mm. Enlargement of musculophrenic arteries and inferior phrenic arteries was defined as an arterial diameter of 1 mm or larger; the enlargement was graded as moderate when the arterial diameter was between 1 and 3 mm and as marked when the diameter was larger than 3 mm. The number of abnormally enlarged nonbronchial systemic arteries was recorded for each hemithorax in each patient. When an abnormally enlarged bronchial or nonbronchial systemic artery was identified, its connection to the PAVM was sought.

The second CT parameter evaluated was the effectiveness of embolotherapy. Effectiveness was assessed on CT angiograms for the 51 PAVMs that were treated exclusively with embolotherapy. The remaining two PAVMs, which were initially treated with embolotherapy and then with surgery, were subsequently classified as failures of embolization. The evaluation of the 51 occluded PAVMs was performed by comparing the findings at follow-up with findings at diagnostic examination (at CT in 49 PAVMs and at pulmonary angiography [ie, whenever CT was not performed before embolotherapy] in two PAVMs). Owing to technologic improvement over time, pretherapeutic evaluation with CT was obtained by means of sequential CT (Elscint 2400, Elscint; or DRH, Siemens) for 10 PAVMs and by means of helical CT (Somatom Plus and Volume Zoom; Siemens) for 39 PAVMs. On multi–detector row helical CT angiograms, the parameters evaluated were the size of the PAVM (enlarged, decreased, or unchanged) and perfusion in the PAVM (present or absent). The size of the PAVM was considered substantially modified if a greater than 30% change in diameter was observed. A PAVM was considered no longer detectable on CT scans when it was not detected on at least two successive sections. Any abnormality in the occluded areas suggestive of sequelae of lung infarction—for example, pleural thickening or subpleural linear and/or rounded opacities—was recorded.

On the basis of the comparison of the findings at diagnostic examinations and those at multi–detector row helical CT, the effectiveness of embolotherapy was classified into four categories: (a) successful, in the presence of a marked retraction (more than 30%) or disappearance of the PAVM with no pulmonary or systemic perfusion; (b) partially successful, in the presence of a reduction in the size of the PAVM, with persistent pulmonary perfusion and a patent feeding artery beyond the level of deposited coils smaller than 3 mm in diameter, deemed to be too small to be reoccluded; (c) partially failed, in the presence of a substantial reduction in the size of the PAVM, persistent pulmonary perfusion, and a patent feeding artery (or arteries) beyond the level of deposited coils, larger than 3 mm in diameter, leading to an indication for repeat embolization; and (d) failed, when the PAVM was unchanged or enlarged with persistent pulmonary perfusion.

Statistical Analysis
Statistical analysis was performed with commercially available software (SAS; SAS Institute, Cary, NC). Comparisons between groups were performed with the Fisher exact test for nominal variables and the Wilcoxon rank sum test for continuous variables. A P value of less than .05 was considered to indicate a statistically significant difference.

	RESULTS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION References

 
Abnormal Enlargement of Systemic Arteries on Helical CT Angiograms
In 13 (41%) of 32 patients, multi–detector row helical CT angiography depicted the presence of abnormally enlarged systemic arteries (group 1), whereas in 19 patients (59%) no abnormal systemic arteries were depicted (group 2). In group 1, a total of 32 abnormally enlarged systemic arteries were identified, which included five bronchial arteries (16%) and 27 nonbronchial systemic arteries (84%). The 27 enlarged nonbronchial systemic arteries comprised 14 inferior phrenic arteries (52%), six musculophrenic arteries (22%), five internal mammary arteries (19%), and two intercostal arteries (7%). The degree of arterial enlargement was rated as moderate for 26 (81%) of 32 arteries and as marked for six (19%) of 32 arteries.

Abnormally enlarged systemic arteries were unilateral findings in 10 patients and bilateral findings in three patients. The number of abnormally enlarged systemic arteries per hemithorax was observed as follows: (a) one abnormal artery per side (n = 7), (b) two abnormal arteries per side (n = 3), (c) three abnormal arteries per side (n = 5), and (d) four abnormal arteries per side (n = 1). Five patients had a single enlarged systemic artery (inferior phrenic artery, n = 4; bronchial artery, n = 1); eight patients had between two and five abnormally enlarged systemic arteries (Fig 1).

View larger version (146K): [in this window] [in a new window] [Download PPT slide]   Figure 1a: CT scans in a 19-year-old woman with solitary right lower lobe PAVM occluded 3 years earlier. (a, b) Pretherapeutic nonenhanced transverse CT scans (10-mm-thick contiguous sequential images) show peripheral location of simple PAVM in anterior segment of right lower lobe. (c–i) Multi–detector row helical CT angiograms 3 years after successful embolization. (c, d) Transverse 3-mm-thick contiguous scans show numerous linear and nodular opacities of right lower lobe (single white arrow) and abnormal thickening of right major fissure (double white arrows) in close contact with occluded PAVM. In c, note part of the right inferior phrenic artery (black arrows) is coursing above the diaphragm. (e, f) Transverse 3-mm-thick contiguous scans and (g–i) oblique coronal 20-mm-thick contiguous maximum intensity projections of thoracoabdominal region show abnormal enlargement of right inferior phrenic artery (arrows), anastomosed with an enlarged right anterior intercostal artery (arrowheads), depicted in the vicinity of occluded PAVM. = Right musculophrenic artery.

View larger version (143K): [in this window] [in a new window] [Download PPT slide]   Figure 1b: CT scans in a 19-year-old woman with solitary right lower lobe PAVM occluded 3 years earlier. (a, b) Pretherapeutic nonenhanced transverse CT scans (10-mm-thick contiguous sequential images) show peripheral location of simple PAVM in anterior segment of right lower lobe. (c–i) Multi–detector row helical CT angiograms 3 years after successful embolization. (c, d) Transverse 3-mm-thick contiguous scans show numerous linear and nodular opacities of right lower lobe (single white arrow) and abnormal thickening of right major fissure (double white arrows) in close contact with occluded PAVM. In c, note part of the right inferior phrenic artery (black arrows) is coursing above the diaphragm. (e, f) Transverse 3-mm-thick contiguous scans and (g–i) oblique coronal 20-mm-thick contiguous maximum intensity projections of thoracoabdominal region show abnormal enlargement of right inferior phrenic artery (arrows), anastomosed with an enlarged right anterior intercostal artery (arrowheads), depicted in the vicinity of occluded PAVM. = Right musculophrenic artery.

View larger version (185K): [in this window] [in a new window] [Download PPT slide]   Figure 1c: CT scans in a 19-year-old woman with solitary right lower lobe PAVM occluded 3 years earlier. (a, b) Pretherapeutic nonenhanced transverse CT scans (10-mm-thick contiguous sequential images) show peripheral location of simple PAVM in anterior segment of right lower lobe. (c–i) Multi–detector row helical CT angiograms 3 years after successful embolization. (c, d) Transverse 3-mm-thick contiguous scans show numerous linear and nodular opacities of right lower lobe (single white arrow) and abnormal thickening of right major fissure (double white arrows) in close contact with occluded PAVM. In c, note part of the right inferior phrenic artery (black arrows) is coursing above the diaphragm. (e, f) Transverse 3-mm-thick contiguous scans and (g–i) oblique coronal 20-mm-thick contiguous maximum intensity projections of thoracoabdominal region show abnormal enlargement of right inferior phrenic artery (arrows), anastomosed with an enlarged right anterior intercostal artery (arrowheads), depicted in the vicinity of occluded PAVM. = Right musculophrenic artery.

View larger version (180K): [in this window] [in a new window] [Download PPT slide]   Figure 1d: CT scans in a 19-year-old woman with solitary right lower lobe PAVM occluded 3 years earlier. (a, b) Pretherapeutic nonenhanced transverse CT scans (10-mm-thick contiguous sequential images) show peripheral location of simple PAVM in anterior segment of right lower lobe. (c–i) Multi–detector row helical CT angiograms 3 years after successful embolization. (c, d) Transverse 3-mm-thick contiguous scans show numerous linear and nodular opacities of right lower lobe (single white arrow) and abnormal thickening of right major fissure (double white arrows) in close contact with occluded PAVM. In c, note part of the right inferior phrenic artery (black arrows) is coursing above the diaphragm. (e, f) Transverse 3-mm-thick contiguous scans and (g–i) oblique coronal 20-mm-thick contiguous maximum intensity projections of thoracoabdominal region show abnormal enlargement of right inferior phrenic artery (arrows), anastomosed with an enlarged right anterior intercostal artery (arrowheads), depicted in the vicinity of occluded PAVM. = Right musculophrenic artery.

View larger version (104K): [in this window] [in a new window] [Download PPT slide]   Figure 1e: CT scans in a 19-year-old woman with solitary right lower lobe PAVM occluded 3 years earlier. (a, b) Pretherapeutic nonenhanced transverse CT scans (10-mm-thick contiguous sequential images) show peripheral location of simple PAVM in anterior segment of right lower lobe. (c–i) Multi–detector row helical CT angiograms 3 years after successful embolization. (c, d) Transverse 3-mm-thick contiguous scans show numerous linear and nodular opacities of right lower lobe (single white arrow) and abnormal thickening of right major fissure (double white arrows) in close contact with occluded PAVM. In c, note part of the right inferior phrenic artery (black arrows) is coursing above the diaphragm. (e, f) Transverse 3-mm-thick contiguous scans and (g–i) oblique coronal 20-mm-thick contiguous maximum intensity projections of thoracoabdominal region show abnormal enlargement of right inferior phrenic artery (arrows), anastomosed with an enlarged right anterior intercostal artery (arrowheads), depicted in the vicinity of occluded PAVM. = Right musculophrenic artery.

View larger version (101K): [in this window] [in a new window] [Download PPT slide]   Figure 1f: CT scans in a 19-year-old woman with solitary right lower lobe PAVM occluded 3 years earlier. (a, b) Pretherapeutic nonenhanced transverse CT scans (10-mm-thick contiguous sequential images) show peripheral location of simple PAVM in anterior segment of right lower lobe. (c–i) Multi–detector row helical CT angiograms 3 years after successful embolization. (c, d) Transverse 3-mm-thick contiguous scans show numerous linear and nodular opacities of right lower lobe (single white arrow) and abnormal thickening of right major fissure (double white arrows) in close contact with occluded PAVM. In c, note part of the right inferior phrenic artery (black arrows) is coursing above the diaphragm. (e, f) Transverse 3-mm-thick contiguous scans and (g–i) oblique coronal 20-mm-thick contiguous maximum intensity projections of thoracoabdominal region show abnormal enlargement of right inferior phrenic artery (arrows), anastomosed with an enlarged right anterior intercostal artery (arrowheads), depicted in the vicinity of occluded PAVM. = Right musculophrenic artery.

View larger version (94K): [in this window] [in a new window] [Download PPT slide]   Figure 1g: CT scans in a 19-year-old woman with solitary right lower lobe PAVM occluded 3 years earlier. (a, b) Pretherapeutic nonenhanced transverse CT scans (10-mm-thick contiguous sequential images) show peripheral location of simple PAVM in anterior segment of right lower lobe. (c–i) Multi–detector row helical CT angiograms 3 years after successful embolization. (c, d) Transverse 3-mm-thick contiguous scans show numerous linear and nodular opacities of right lower lobe (single white arrow) and abnormal thickening of right major fissure (double white arrows) in close contact with occluded PAVM. In c, note part of the right inferior phrenic artery (black arrows) is coursing above the diaphragm. (e, f) Transverse 3-mm-thick contiguous scans and (g–i) oblique coronal 20-mm-thick contiguous maximum intensity projections of thoracoabdominal region show abnormal enlargement of right inferior phrenic artery (arrows), anastomosed with an enlarged right anterior intercostal artery (arrowheads), depicted in the vicinity of occluded PAVM. = Right musculophrenic artery.

View larger version (100K): [in this window] [in a new window] [Download PPT slide]   Figure 1h: CT scans in a 19-year-old woman with solitary right lower lobe PAVM occluded 3 years earlier. (a, b) Pretherapeutic nonenhanced transverse CT scans (10-mm-thick contiguous sequential images) show peripheral location of simple PAVM in anterior segment of right lower lobe. (c–i) Multi–detector row helical CT angiograms 3 years after successful embolization. (c, d) Transverse 3-mm-thick contiguous scans show numerous linear and nodular opacities of right lower lobe (single white arrow) and abnormal thickening of right major fissure (double white arrows) in close contact with occluded PAVM. In c, note part of the right inferior phrenic artery (black arrows) is coursing above the diaphragm. (e, f) Transverse 3-mm-thick contiguous scans and (g–i) oblique coronal 20-mm-thick contiguous maximum intensity projections of thoracoabdominal region show abnormal enlargement of right inferior phrenic artery (arrows), anastomosed with an enlarged right anterior intercostal artery (arrowheads), depicted in the vicinity of occluded PAVM. = Right musculophrenic artery.

View larger version (110K): [in this window] [in a new window] [Download PPT slide]   Figure 1i: CT scans in a 19-year-old woman with solitary right lower lobe PAVM occluded 3 years earlier. (a, b) Pretherapeutic nonenhanced transverse CT scans (10-mm-thick contiguous sequential images) show peripheral location of simple PAVM in anterior segment of right lower lobe. (c–i) Multi–detector row helical CT angiograms 3 years after successful embolization. (c, d) Transverse 3-mm-thick contiguous scans show numerous linear and nodular opacities of right lower lobe (single white arrow) and abnormal thickening of right major fissure (double white arrows) in close contact with occluded PAVM. In c, note part of the right inferior phrenic artery (black arrows) is coursing above the diaphragm. (e, f) Transverse 3-mm-thick contiguous scans and (g–i) oblique coronal 20-mm-thick contiguous maximum intensity projections of thoracoabdominal region show abnormal enlargement of right inferior phrenic artery (arrows), anastomosed with an enlarged right anterior intercostal artery (arrowheads), depicted in the vicinity of occluded PAVM. = Right musculophrenic artery.

View larger version (101K): [in this window] [in a new window] [Download PPT slide]   Figure 2a: CT scans in a 58-year-old woman with two right lower lobe PAVMs occluded 16 years earlier. (a–c) Transverse CT scans. (a) Pretherapeutic nonenhanced scan of first PAVM (5-mm-thick sequential image), in anterobasal segment of right lower lobe. Occlusion of this complex PAVM supplied by anterobasal and laterobasal segmental arteries of right lower lobe required two sessions. (b) Follow-up nonenhanced scan (5-mm-thick sequential image) 3 months after embolotherapy shows large area of increased attenuation in anterior segment of right lower lobe in the absence of clinical complaint by patient. Three years later, second AVM (simple angioarchitecture, posterobasal segment of right lower lobe) was treated with embolotherapy. Successful embolization, obtained in one session, was followed by transient episode of right-sided pleuritic chest pain and fever. (c) Follow-up thin-section scan at time of clinical complaint shows areas of ground-glass attenuation in posterobasal and laterobasal segments of right lower lobe. (d–f) Multi–detector row helical CT angiograms obtained 16 years after embolotherapy of the first PAVM. (d) Transverse 3-mm-thick scan and (e, f) coronal 20-mm-thick maximum intensity projections illustrate the presence of an enlarged right inferior phrenic artery (arrows) and abnormal dilatation of right bronchial artery (arrowheads).

View larger version (116K): [in this window] [in a new window] [Download PPT slide]   Figure 2b: CT scans in a 58-year-old woman with two right lower lobe PAVMs occluded 16 years earlier. (a–c) Transverse CT scans. (a) Pretherapeutic nonenhanced scan of first PAVM (5-mm-thick sequential image), in anterobasal segment of right lower lobe. Occlusion of this complex PAVM supplied by anterobasal and laterobasal segmental arteries of right lower lobe required two sessions. (b) Follow-up nonenhanced scan (5-mm-thick sequential image) 3 months after embolotherapy shows large area of increased attenuation in anterior segment of right lower lobe in the absence of clinical complaint by patient. Three years later, second AVM (simple angioarchitecture, posterobasal segment of right lower lobe) was treated with embolotherapy. Successful embolization, obtained in one session, was followed by transient episode of right-sided pleuritic chest pain and fever. (c) Follow-up thin-section scan at time of clinical complaint shows areas of ground-glass attenuation in posterobasal and laterobasal segments of right lower lobe. (d–f) Multi–detector row helical CT angiograms obtained 16 years after embolotherapy of the first PAVM. (d) Transverse 3-mm-thick scan and (e, f) coronal 20-mm-thick maximum intensity projections illustrate the presence of an enlarged right inferior phrenic artery (arrows) and abnormal dilatation of right bronchial artery (arrowheads).

View larger version (115K): [in this window] [in a new window] [Download PPT slide]   Figure 2c: CT scans in a 58-year-old woman with two right lower lobe PAVMs occluded 16 years earlier. (a–c) Transverse CT scans. (a) Pretherapeutic nonenhanced scan of first PAVM (5-mm-thick sequential image), in anterobasal segment of right lower lobe. Occlusion of this complex PAVM supplied by anterobasal and laterobasal segmental arteries of right lower lobe required two sessions. (b) Follow-up nonenhanced scan (5-mm-thick sequential image) 3 months after embolotherapy shows large area of increased attenuation in anterior segment of right lower lobe in the absence of clinical complaint by patient. Three years later, second AVM (simple angioarchitecture, posterobasal segment of right lower lobe) was treated with embolotherapy. Successful embolization, obtained in one session, was followed by transient episode of right-sided pleuritic chest pain and fever. (c) Follow-up thin-section scan at time of clinical complaint shows areas of ground-glass attenuation in posterobasal and laterobasal segments of right lower lobe. (d–f) Multi–detector row helical CT angiograms obtained 16 years after embolotherapy of the first PAVM. (d) Transverse 3-mm-thick scan and (e, f) coronal 20-mm-thick maximum intensity projections illustrate the presence of an enlarged right inferior phrenic artery (arrows) and abnormal dilatation of right bronchial artery (arrowheads).

View larger version (140K): [in this window] [in a new window] [Download PPT slide]   Figure 2d: CT scans in a 58-year-old woman with two right lower lobe PAVMs occluded 16 years earlier. (a–c) Transverse CT scans. (a) Pretherapeutic nonenhanced scan of first PAVM (5-mm-thick sequential image), in anterobasal segment of right lower lobe. Occlusion of this complex PAVM supplied by anterobasal and laterobasal segmental arteries of right lower lobe required two sessions. (b) Follow-up nonenhanced scan (5-mm-thick sequential image) 3 months after embolotherapy shows large area of increased attenuation in anterior segment of right lower lobe in the absence of clinical complaint by patient. Three years later, second AVM (simple angioarchitecture, posterobasal segment of right lower lobe) was treated with embolotherapy. Successful embolization, obtained in one session, was followed by transient episode of right-sided pleuritic chest pain and fever. (c) Follow-up thin-section scan at time of clinical complaint shows areas of ground-glass attenuation in posterobasal and laterobasal segments of right lower lobe. (d–f) Multi–detector row helical CT angiograms obtained 16 years after embolotherapy of the first PAVM. (d) Transverse 3-mm-thick scan and (e, f) coronal 20-mm-thick maximum intensity projections illustrate the presence of an enlarged right inferior phrenic artery (arrows) and abnormal dilatation of right bronchial artery (arrowheads).

View larger version (134K): [in this window] [in a new window] [Download PPT slide]   Figure 2e: CT scans in a 58-year-old woman with two right lower lobe PAVMs occluded 16 years earlier. (a–c) Transverse CT scans. (a) Pretherapeutic nonenhanced scan of first PAVM (5-mm-thick sequential image), in anterobasal segment of right lower lobe. Occlusion of this complex PAVM supplied by anterobasal and laterobasal segmental arteries of right lower lobe required two sessions. (b) Follow-up nonenhanced scan (5-mm-thick sequential image) 3 months after embolotherapy shows large area of increased attenuation in anterior segment of right lower lobe in the absence of clinical complaint by patient. Three years later, second AVM (simple angioarchitecture, posterobasal segment of right lower lobe) was treated with embolotherapy. Successful embolization, obtained in one session, was followed by transient episode of right-sided pleuritic chest pain and fever. (c) Follow-up thin-section scan at time of clinical complaint shows areas of ground-glass attenuation in posterobasal and laterobasal segments of right lower lobe. (d–f) Multi–detector row helical CT angiograms obtained 16 years after embolotherapy of the first PAVM. (d) Transverse 3-mm-thick scan and (e, f) coronal 20-mm-thick maximum intensity projections illustrate the presence of an enlarged right inferior phrenic artery (arrows) and abnormal dilatation of right bronchial artery (arrowheads).

View larger version (172K): [in this window] [in a new window] [Download PPT slide]   Figure 2f: CT scans in a 58-year-old woman with two right lower lobe PAVMs occluded 16 years earlier. (a–c) Transverse CT scans. (a) Pretherapeutic nonenhanced scan of first PAVM (5-mm-thick sequential image), in anterobasal segment of right lower lobe. Occlusion of this complex PAVM supplied by anterobasal and laterobasal segmental arteries of right lower lobe required two sessions. (b) Follow-up nonenhanced scan (5-mm-thick sequential image) 3 months after embolotherapy shows large area of increased attenuation in anterior segment of right lower lobe in the absence of clinical complaint by patient. Three years later, second AVM (simple angioarchitecture, posterobasal segment of right lower lobe) was treated with embolotherapy. Successful embolization, obtained in one session, was followed by transient episode of right-sided pleuritic chest pain and fever. (c) Follow-up thin-section scan at time of clinical complaint shows areas of ground-glass attenuation in posterobasal and laterobasal segments of right lower lobe. (d–f) Multi–detector row helical CT angiograms obtained 16 years after embolotherapy of the first PAVM. (d) Transverse 3-mm-thick scan and (e, f) coronal 20-mm-thick maximum intensity projections illustrate the presence of an enlarged right inferior phrenic artery (arrows) and abnormal dilatation of right bronchial artery (arrowheads).

Comparison of Patients with and Those without Abnormally Enlarged Systemic Arteries
Clinical characteristics.—As shown in Table 1, there was no significant difference in the mean age, sex, and number of patients with HHT diagnosed at the time of initial presentation between patients in group 1 and those in group 2. No significant difference was found in the number of patients treated with surgery before or after embolotherapy between group 1 (n = 4) and group 2 (n = 4) (P = .7).

	DISCUSSION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION References

Although systemic supply to PAVMs can be congenital in origin (25), it has also been suggested to develop as a response to surgical (26) or percutaneous (14,16,17) treatment. Laffey et al (26) have noted the potential relationship between surgery and abnormal systemic supply to PAVMs. Their explanation was based on a similar situation existing in the right-to-left shunt present in patients with cyanotic diseases, in which thoracotomy often incites a transpleural supply to the lung from systemic vessels. Keeping this explanation in mind, we compared the frequency of patients treated by means of surgery in groups 1 and 2 but failed to demonstrate any significant difference.

Seven cases of occluded PAVMs fed by systemic arteries after embolotherapy have been reported in the literature (13,14,16,17). In one of these cases, the young age of the patient and the continued lung growth at this age was the proposed explanation for the occurrence of the left-to-left shunt created by the systemic collateral supply beyond the level of embolization (13). In the remaining six cases (14,16,17), it has been suggested that the relative postprocedural local ischemia could trigger the development of a systemic supply to the malformations. Our results support this hypothesis. In our study, we observed that the number of patients with features suggestive of lung infarction in the days or months following embolotherapy and the number of patients with features suggestive of sequelae of lung infarction on CT angiograms were significantly higher in group 1 than in group 2 in the absence of a previous history of pleural disease. This potential explanation could be reinforced by the fact that the mean number of occluded PAVMs per patient was significantly higher in group 1 than in group 2.

Enlargement of systemic arteries after embolotherapy could be compared with similar findings observed in patients with chronic thromboembolic pulmonary hypertension, which is an acquired cause of chronic lung ischemia. In an investigation of 22 consecutive patients with chronic thromboembolic pulmonary hypertension, Remy-Jardin et al (27) identified abnormally enlarged systemic arteries on multi–detector row helical CT angiograms in 16 patients (73%), which is a significantly higher proportion in comparison with two (14%) of 14 patients with primary pulmonary hypertension.

The physiologic importance of the systemic perfusion of a PAVM depends on the status of the PAVM. When the feeding artery is patent, the right-to-left shunt of the PAVM is compensated in part by flow from the systemic component. A definitive treatment with endovascular therapy requires occlusion of both the pulmonary and the systemic feeding arteries. When the systemic arterial supply is identified after successful embolotherapy, it is responsible for a left-to-left shunt. Sagara et al (14) speculated that the presence of such a systemic supply to the malformation placed patients at risk for future hemoptysis. Lee et al (12) followed up patients with large PAVMs treated by means of embolotherapy for up to 20 years, and they reported the absence of late hemoptysis as long as the PAVM is obliterated. In our experience, which was based on a similar follow-up period in patients treated by means of embolotherapy, we have not encountered hemoptysis to date. However, the CT findings of our investigation raise questions regarding management in these asymptomatic patients. In the absence of clinical complaints, it would be difficult to justify diagnostic systemic arteriography for the evaluation of connections between the systemic and pulmonary arterial circulations. The second justification for systemic arteriography could be the occlusion of enlarged systemic arteries. However, the absence of clinical complaints and the lack of follow-up documentation to prove that such a systemic supply increases in size over years exclude a priori any preventive endovascular treatment.

Several limitations of this study should be underlined. First, because none of these patients underwent CT or conventional systemic angiography prior to embolotherapy, it is not possible to relate the presence of enlarged systemic arteries to embolotherapy. Second, our technique of embolotherapy led to the occlusion of a few side branches of the artery feeding the malformation in order to avoid any accidental migration of the occlusive material. The decision to occlude a PAVM by means of deposition of material immediately adjacent to the aneurysmal sac would have spared normal lung around the malformation, a situation that might influence the systemic collateral supply in the vicinity of treated malformations.

In conclusion, our investigation documented the presence of abnormally enlarged systemic arteries in 13 (41%) of 32 patients who underwent multi–detector row helical CT angiography for the follow-up of occluded PAVMs. In this group of patients, the frequency of clinical events suggestive of lung infarction in the days or months after embolotherapy and the frequency of CT features suggestive of sequelae of lung infarction on CT angiograms were significantly higher than those observed in the group of patients without abnormal enlargement of systemic arteries. Improved knowledge of the frequency of congenital and acquired systemic arterial supply to PAVMs, as well as predictive factors for the latter situation, requires precise mapping of systemic arteries prior to embolotherapy.

	FOOTNOTES

 

Abbreviations: HHT = hereditary hemorrhagic telangiectasia • PAVM = pulmonary arteriovenous malformation

Authors stated no financial relationship to disclose.

Author contributions: Guarantors of integrity of entire study, J.R., M.R.; study concepts/study design or data acquisition or data analysis/interpretation, all authors; manuscript drafting or manuscript revision for important intellectual content, all authors; manuscript final version approval, all authors; literature research, P.Y.B., P.D., J.R., M.R.; clinical studies, P.Y.B., P.D., N.B., F.L., J.R., M.R.; statistical analysis, A.D.; and manuscript editing, P.Y.B., J.R., M.R.

	References

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION References

 

1. White RI Jr, Pollak JS, Wirth JA. Pulmonary arteriovenous malformations: diagnosis and transcatheter embolotherapy. J Vasc Interv Radiol 1996;7:787–804.[Medline]
2. Remy J, Remy-Jardin M, Wattinne L, et al. Pulmonary arteriovenous malformations: evaluation with CT of the chest before and after treatment. Radiology 1992;182:809–816.[Abstract/Free Full Text]
3. Gossage JR, Kanj G. Pulmonary arteriovenous malformations: a state-of-the art review. Am J Respir Crit Care Med 1998;158:643–661.[Free Full Text]
4. Shovlin CL, Letarte M. Hereditary haemorrhagic telangiectasis and pulmonary arteriovenous malformations: issues in clinical management and review of pathogenic mechanisms. Thorax 1999;54:714–729.[Free Full Text]
5. Porstman W. Therapeutic embolization of arteriovenous fistula by catheter technique. In: Kelop O, ed. Current concepts in pediatric radiology. Berlin, Germany: Springer, 1977; 23–31.
6. Taylor BG, Cockerill EM, Manfredi F, Klatte EC. Therapeutic embolization of the pulmonary artery in pulmonary arteriovenous fistula. Am J Med 1978;64:360–365.[CrossRef][Medline]
7. Terry PB, Barth KH, Kaufman SL, et al. Balloon embolization for treatment of pulmonary arteriovenous fistulas. N Engl J Med 1980;302:1189–1190.[Medline]
8. White RI Jr, Lynch-Nyhan A, Terry P, et al. Pulmonary arteriovenous malformations: techniques and long-term outcome of embolotherapy. Radiology 1988;169:663–669.[Abstract/Free Full Text]
9. Hartnell GG, Jackson JE, Allison DJ. Coil embolization of pulmonary arteriovenous malformations. Cardiovasc Intervent Radiol 1990;13:347–350.[Medline]
10. Haitjema TJ, Overtoom TTC, Westermann CJJ, et al. Embolisation of pulmonary arteriovenous malformations: results and follow-up in 32 patients. Thorax 1995;50:719–723.[Abstract]
11. Dutton JA, Jackson JE, Hughes JM, et al. Pulmonary arteriovenous malformations: results of treatment with coil embolization in 53 patients. AJR Am J Roentgenol 1995;165:1119–1125.[Abstract/Free Full Text]
12. Lee DW, White RI Jr, Eggling TK, et al. Embolotherapy of large pulmonary arteriovenous malformations: long-term results. Ann Thorac Surg 1997;64:930–940.[Abstract/Free Full Text]
13. Pollak JS, Saluja S, Thabet A, Henderson KJ, Denbow N, White RW Jr. Clinical and anatomic outcomes after embolotherapy of pulmonary arteriovenous malformations. J Vasc Interv Radiol 2006;17:35–45.[CrossRef][Medline]
14. Sagara K, Miyazono N, Inoue H, Ueno K, Nishida H, Nakajo M. Recanalization after coil embolotherapy of pulmonary arteriovenous malformations: study of long-term outcome and mechanism for recanalization. AJR Am J Roentgenol 1998;170:727–730.[Abstract]
15. White RI Jr. Recanalization after embolotherapy of pulmonary arteriovenous malformations: significance? outcome? [editorial]. AJR Am J Roentgenol 1998;171:1704.[Medline]
16. Remy J, Remy-Jardin M, Giraud F, Wattinne L. Angioarchitecure of pulmonary arteriovenous malformations: clinical utility of three-dimensional helical CT. Radiology 1994;191:657–664.[Abstract/Free Full Text]
17. Wispelaere JF, Trigaux JP, Weynants P, Delos M, Coene BD. Systemic supply to a pulmonary arteriovenous malformation: potential explanation for recurrence. Cardiovasc Intervent Radiol 1996;19:285–287.[CrossRef][Medline]
18. Shovlin CL, Guttmacher AE, Buscarini E, et al. Diagnostic criteria for hereditary hemorrhagic telengiectasia (Rendu-Osler-Weber syndrome). Am J Med Genet 2000;91:66–67.[CrossRef][Medline]
19. White RI Jr, Pollak JS. Pulmonary arteriovenous malformations: diagnosis with three-dimensional helical CT—a breakthrough without contrast media. Radiology 1994;191:613–614.[Free Full Text]
20. Furuse M, Saito K, Kunieda E, et al. Bronchial arteries: CT demonstration with arteriographic correlation. Radiology 1987;162:393–398.[Abstract/Free Full Text]
21. Kauczor HU, Schwickert HC, Mayer E, Schweden F, Schild HH, Thelen M. Spiral CT of bronchial arteries in chronic thromboembolism. J Comput Assist Tomogr 1994;18:855–861.[Medline]
22. Song JW, Im JG, Shim YS, Park JH, Yeon KM, Han MC. Hypertrophied bronchial artery at thin-section CT in patients with bronchiectasis: correlation with CT angiographic findings. Radiology 1998;208:187–191.[Abstract/Free Full Text]
23. Remy J, Remy-Jardin M. Bronchial bleeding. In: Dondelinger RF, Rossi P, Kurdziel JC, Wallace S, eds. Interventional radiology. Stuttgart, Germany: Thieme, 1990; 325–341.
24. Remy-Jardin M, Bouaziz N, Dumont Ph, Brillet PY, Bruzzi J, Remy J. Bronchial and nonbronchial systemic arteries at multi–detector row helical CT angiography: comparison with conventional angiography. Radiology 2004;233(3):741–749.[Abstract/Free Full Text]
25. Bosher LH, Blake A, Byrd BR. An analysis of the pathologic anatomy of pulmonary arteriovenous aneurysms with particular reference to the applicability of local excision. Surgery 1959;45:91–104.[Medline]
26. Laffey KJ, Tomashow B, Jaretzki A, Martin EC. Systemic supply to a pulmonary arteriovenous malformation: a relative contraindication to surgery. AJR Am J Roentgenol 1985;145:720–722.[Free Full Text]
27. Remy-Jardin M, Duhamel A, Deken V, Bouaziz N, Dumont P, Remy J. Systemic collateral supply in patients with chronic thromboembolic and primary pulmonary hypertension: assessment with multi–detector row helical CT angiography. Radiology 2005;235:274–281.[Abstract/Free Full Text]

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