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Embolization using hydrogel-coated coils for pulmonary arteriovenous malformations
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ORIGINAL ARTICLE /Interventional imaging
Embolization using hydrogel-coated coils for pulmonary arteriovenous malformations T. Iguchi a,∗, T. Hiraki a, Y. Matsui a, H. Fujiwara b, J. Sakurai c, K. Baba d, S. Toyooka e, H. Gobara a, S. Kanazawa a a
Department of Radiology, Okayama University Medical School, 2-5-1 Shikata-cho kita-ku, Okayama 700-8558, Japan b Department of Radiology, Okayama City Hospital, Okayama 700-8557, Japan c Center for Innovative Clinical Medicine, Okayama University Hospital, Okayama 700-8558, Japan d Interventional Radiology Center, Okayama University Hospital, Okayama 700-8558, Japan e Department of General Thoracic Surgery, Okayama University Medical School, Okayama 700-8558, Japan
KEYWORDS Pulmonary arteriovenous fistulas; Lung; Arteriovenous malformation; Embolization
∗
Abstract Purpose: To prospectively evaluate the efficacy and safety of embolization using hydrogelcoated coils for the treatment of pulmonary arteriovenous malformations (PAVMs). Materials and methods: The outcomes of 21 PAVMs in 19 patients (3 men and 16 women; mean age, 58.8 ± 15.2 [SD] years; age range 14—78 years) treated by venous sac embolization (VSE) with additional feeding artery embolization were prospectively evaluated. For VSE, using one or more 0.018-inch hydrogel-coated coils was mandatory. Recanalization and/or reperfusion were evaluated by pulmonary arteriography 1 year after embolization. Results: The mean feeding artery and venous sac sizes were 4.0 mm and 8.5 mm, respectively. Embolization was successfully completed in 20/21 PAVMs, yielding a technical success rate of 95%. The feeding artery was also embolized in 17/20 successful PAVMs (85%). A technical failure occurred in one PAVM, where embolization was abandoned because of migration of one bare coil to the left ventricle. The mean numbers of hydrogel-coated coils and bare platinum detachable coils used for VSE were 3.3 ± 2.1 (SD) (range, 1—8) and 4.4 ± 3.9 (SD) (range, 1—17), respectively. The mean percentages of hydrogel-coated coils in number, length, and estimated volume were 42.9%, 33.3%, and 72.7% respectively. One patient with one PAVM was lost to follow-up after 3 months. Neither recanalization nor reperfusion was noted in the remaining 19 PAVMs (success rate, 19/19 [100%]). One grade 4 (coil migration) adverse event occurred, and it was treated without any sequelae.
Corresponding author. E-mail address: [email protected] (T. Iguchi).
https://doi.org/10.1016/j.diii.2019.10.008 2211-5684/© 2019 Soci´ et´ e franc ¸aise de radiologie. Published by Elsevier Masson SAS. All rights reserved.
Please cite this article in press as: Iguchi T, et al. Embolization using hydrogel-coated coils for pulmonary arteriovenous malformations. Diagnostic and Interventional Imaging (2019), https://doi.org/10.1016/j.diii.2019.10.008
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T. Iguchi et al. Conclusion: VSE using hydrogel-coated coils with additional feeding artery embolization is a safe and effective treatment for PAVM. © 2019 Soci´ et´ e franc ¸aise de radiologie. Published by Elsevier Masson SAS. All rights reserved.
Percutaneous transcatheter embolization is the gold standard for the treatment of pulmonary arteriovenous malformations (PAVMs) because it is effective in lowering the risk of embolism and other complications [1,2]. Feeding artery embolization (FAE) using coils is the conventional mode of treatment [3—6]. However, with recent advances in interventional techniques and equipment, venous sac embolization (VSE) seems to be safer and more feasible [7]. Some studies have reported the efficacy of VSE in the treatment of PAVMs [7—11], and one retrospective study showed that VSE is associated with a significantly lower reperfusion rate than FAE [7]. Hydrogel-coated coils, which were recently introduced, comprise a carrier platinum coil coated with an expandable hydrogel material that undergoes a nine-fold increase in volume when placed in a physiological environment [12]. Therefore, hydrogel-coated coils offer the advantage of a greater filling volume and, theoretically, a lower risk of recanalization than bare platinum coils [13]. The efficacy of these coils in the embolization of arteries or aneurysms has been reported [14—17]; it is speculated that they enhance the treatment efficacy of VSE for PAVMs when used with other types of coils, such as fibered or bare platinum coils. Some retrospective studies have evaluated the outcomes of transcatheter embolization using hydrogel-coated coils for PAVMs with both advantages (e.g., increase in packing density) and disadvantages (e.g., slight resistance in the coil delivery) [13,14,18]. However, more robust and prospective data are needed for determining the efficacy and safety of VSE using these coils accurately. The purpose of this study was to prospectively evaluate the efficacy and safety of VSE using hydrogel-coated coils with additional FAE for PAVMs.
Materials and methods This study was prospectively conducted at a single center between June 2014 and May 2017. The study was approved by the institutional review board (approval number, m29006) and conducted in accordance with the Declaration of Helsinki. All patients provided written informed consent before participation. The study has been registered in the University Hospital Medical Information Network Clinical Trials Registry (study ID: UMIN000014360).
Patient selection The inclusion criteria were as follows:
• presence of PAVM confirmed by chest computed tomography (CT) (slice thickness, ≤ 3 mm); • patient with a history of one or more of the following conditions: ◦ ◦ ◦ ◦ ◦
brain infarction and/or abscess, transient ischemic attack, hemoptysis, hypoxemia, feeding pulmonary artery diameter of ≥ 3 mm (≥ 2 mm in patients with hereditary hemorrhagic telangiectasia);
• adequate cardiac, hepatic, renal, respiratory, coagulation, and bone marrow functions; • an Eastern Cooperative Oncology Group performance status of 0—2; • a life expectancy ≥ 1 year. The exclusion criteria were as follows: • history of allergy to iodinated contrast material, active asthma, or pulmonary hypertension; • presence of single lung; • impaired contralateral lung function; • an estimated glomerular filtration rate of < 30 ml/min (excluding dialysis); • a Child—Pugh score ≥ 9; • heart failure (New York Heart Association classification, ≥ III); • uncontrollable malignant disease; • active infection or an active inflammatory process; • a body temperature ≥ 38 ◦ C; • pregnancy and, • ineligibility determined by the responding physician. Between June 2014 and May 2017, 4 patients (6 PAVMs) underwent surgery and 21 patients (28 PAVMs) underwent transcatheter embolization at our institution. In 28 PAVMs performed transcatheter embolization, 7 PAVMs were excluded according to the ineligibility determined by the responding physician: • patients’ refusal (n = 4 PAVMs [4 patients]), • patient’s arrhythmia (Wolff-Parkinson-White syndrome; n = 2 PAVMS [1 patient]), • small feeding pulmonary artery diameter (< 3 mm) (n = 1 PAVM [1 patient]) (Fig. 1). Therefore, 21 PAVMs in 19 patients (3 men, 16 women) with a mean age of 58.8 ± 15.2 (SD) years (range: 14—78 years) were eligible for inclusion (Table 1). Two patients have a history of hereditary hemorrhagic telangiectasia. Two PAVMs in two patients were treated in two separate sessions. The mean sizes of the feeding artery and venous sac
Please cite this article in press as: Iguchi T, et al. Embolization using hydrogel-coated coils for pulmonary arteriovenous malformations. Diagnostic and Interventional Imaging (2019), https://doi.org/10.1016/j.diii.2019.10.008
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Figure 1.
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Flow chart diagram of patient inclusion and exclusion.
Table 1 Characteristics of 21 pulmonary arteriovenous malformations in 19 patients. Characteristics Type Location (lobe)
Diameter of feeding artery (mm) Diameter of venous sac (mm) Diameter of draining vein (mm) Feeding artery embolizationa
Simple/ Complex Right upper lobe Right middle lobe Right lower lobe Left upper lobe Left lower lobe Mean ± SD [range] Median (IQR)
19/21 (90%) 2/21 (10%) 2/21 (10%) 3/21 (14%) 4/21 (19%) 5/21 (24%) 7/21 (33%) 4.0 ± 0.8 [2.3—6.0] 4.0 (3.5—4.5)
Mean ± SD [range] 8.5 ± 3.0 [3.1—16.0] Median (IQR) 8.1 (7.0—9.3) Mean ± SD [range] 4.6 ± 0.9 [2.4—6.5] Median (IQR) 4.5 (4.1—5.2) Yes No
17/20 (85%) 3/20 (15%)
SD: standard deviation; IQR: interquartile range. a In one patient, embolization was abandoned.
were 4.0 ± 0.8 (SD) mm (range: 2.3—6.0 mm) and 8.5 ± 3.0 (SD) mm (range: 3.1—16.0 mm), respectively. Among the 21 PAVMs, eight were described in a previous study reporting the quality of lung CT images acquired after single-energy metal artifact reduction [19].
Study endpoints The primary endpoint was the efficacy of VSE using hydrogelcoated coils with additional FAE. The secondary endpoint was safety, as assessed by the evaluation of adverse events
(AEs). Efficacy was defined as the absence of recanalization and reperfusion on pulmonary arteriography performed 1 year after embolization. Recanalization was defined as venous sac blood flow from the recanalized artery that had undergone coil embolization, while reperfusion was defined as a venous sac or draining vein blood flow, regardless of the inflow route [7]. To identify the number of procedures required for evaluation of the efficacy rate, we performed one-sample binomial t-tests (null hypothesis H0, P = 0; alternative hypothesis H1, P = ). For an efficacy rate with 0 = 0.50 and = 0.80, values of ␣ = 0.05 and  = 0.20 yielded a sample size of 19. This number was increased by 10% in anticipation of protocol deviations. Therefore, we enrolled 21 PAVMs.
Transcatheter coil embolization Through the femoral vein sheath, pulmonary arteriography was performed using a 4- or 5-F angiographic catheter for the assessment of PAVMs. Immediately after femoral sheath insertion, 3000 or 4000 IU of heparin was intravenously administered for prophylactic anticoagulation, followed by additional administration of 1000 IU/h. The catheter was advanced into the feeding artery of PAVM, as close to the venous sac as possible. Subsequently, a microcatheter was advanced into the venous sac through the base catheter, and VSE was performed. A combination of one or more 0.018-inch hydrogel-coated coils (AZUR® ; Terumo, Tokyo, Japan) and 0.010—0.020-inch bare platinum detachable coils (Target® , Stryker Fremont; DELTAFILL® , MICRUSFRAME® S or MICRUSFRAME® C, Johnson & Johnson KK; or Penumbra Coil 400TM , Medico’s Hirata Inc.) was used for embolization. Subsequently, the microcatheter was pulled back to the distal feeding artery, and embolization was continued if the draining vein was still visualized by feeding arteriography. In each procedure, the operator decided which coils to use and attempted to use as many hydrogel-coated coils as possible. For FAE, fibered platinum pushable coils (Tornado® Embolization Coil or Hilal Embolization MicrocoilTM , Cook
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Figure 2. A 14-year-old male with a complex pulmonary arteriovenous malformation in left segment 4. A. Left A4 pulmonary arteriogram shows a pulmonary arteriovenous malformation (arrow). The maximum sizes of the venous sac and feeding arteries are 8.1 mm and 3.5 mm, respectively. B. Fluoroscopy shows one bare coil migration (arrow). C. Fluoroscopy shows that the migrated coil (arrow) is successfully retrieved using a snare.
Japan; or C-STOPPER® , Piolax Medical Devices) were also used at the operator’s discretion. After completion of the procedure, pulmonary arteriography was performed to confirm complete embolization.
Follow-up examination and efficacy assessment Physical examinations, laboratory tests (including blood counts and biochemical examinations) and chest radiography were performed 1 and 3 days, 1 and 6 months, and 1 year after embolization. Chest CT was performed 3 days and 1 and 6 months after embolization. After plain CT scanning, a non-ionic iodine contrast medium (300 mgI/mL and total dose of 600 mgI/kg) was administered intravenously at a rate of 3 ml/s, and CT images were acquired 14, 33, and 90 s after initiation of contrast material administration. From each data set, in addition to contiguous 5-mm transverse CT images of the whole thorax, contiguous thin-section (1mm thick) transverse CT images of the area of interest were reconstructed with both mediastinal and lung windows. To evaluate the efficacy of VSE using hydrogel-coated coils with additional FAE, pulmonary arteriography was performed using a catheter inserted via the femoral or cubital vein one year after embolization. Pulmonary arteriograms were divided into two groups according to the presence or absence of recanalization and reperfusion.
Safety assessment All AEs that occurred during the embolization and follow-up period were recorded and graded according to the Common Terminology Criteria for Adverse Events (ver. 4.0).
Results VSE using hydrogel-coated coils with additional FAE was successfully completed for 20 of the 21 PAVMs (95.2%). The remaining PAVM was complex type and considered a technical failure (Fig. 2). Although FAE was additionally attempted after VSE, one bare coil migrated to the left ventricle via a missed communication. Therefore, embolization was abandoned, and the coil was immediately and successfully retrieved using a snare. Re-embolization was performed
successfully 5 months later. Although embolizations were completed, the hydrogel-coated coil unraveled in two procedures; in the other two procedures, they could not be placed because they were trapped in the microcatheter. The mean number, total length, and total volume of hydrogel-coated coils used for VSE in the 20 successful PAVMs were 3.3 ± 2.1 (SD) (range, 1—8), 44.5 ± 37.6 (SD) (range, 4—140) cm, and 250.4 ± 214.5 (SD) (range, 23.4—820.0) mm3 , respectively; the mean percentages of hydrogelcoated coils used for VSE were 42.9% in number, 33.3% in length, and 72.7% in volume. Assuming a cylindrical coil shape, the volume of each coil was calculated using the following formula: coil volume = × (coil radius)2 × (coil length) [18]. Details of the coils used for VSE are shown in Table 2. FAE was also performed in 17 of the 20 successful PAVMs, with the mean number of hydrogel-coated coils, bare coils, and fibered coils used being 0.2 (range, 0—1), 1.9 (range, 0—4), and 1.0 (range, 0—6), respectively. One patient with one PAVM was lost to follow-up 3 months after complete embolization. Pulmonary arteriography, performed 1 year after the procedure, showed neither recanalization nor reperfusion in the remaining 19 PAVMs (Fig. 3). Arteriography was performed via the brachial vein for one PAVM because the patient complained of discomfort when the catheter passed the heart and refused to undergo direct pulmonary arteriography. For the remaining 18 PAVMs, left or right pulmonary arteriography was performed. Additionally, feeding pulmonary arteriography (n = 5 PAVMs), lower pulmonary arteriography (n = 7 PAVMs), and middle pulmonary arteriography (n = 1 PAVM) were performed where required. Among the 21 procedures, two grade 1 (fever and noncardiac chest pain), three grade 2 (headache, atrial fibrillation, and cerebral infarction), and one grade 4 (previously mentioned coil migration) AEs were recorded. No venous sac injury occurred. The one major AE (grade 4) was completely treated without any sequelae. One patient unexpectedly complained of dysarthria caused by cerebral infarction 11 h after the procedure. This AE was immediately and spontaneously improved; it has been reported elsewhere [20].
Discussion Since it was first reported in 1977 [21], transcatheter embolization has been accepted as a standard treatment
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Table 2 Details of coils used for the successful sac embolizaion of 20 pulmonary arteriovenous malformations in 18 patients.
Number
Length (cm) Volume (mm3 )
Mean ± SD (%) Median (IQR) Range Mean ± SD (%) Median (IQR) Range Mean ± SD (%) Median (IQR) Range
Hydrogel-coated coil
Bare platinum detachable coil
Total
3.3 ± 2.1 (42.9) 2 (2—5) 1—8 44.5 ± 37.6 (33.3) 35 (20—57.5) 4—140 250.4 ± 214.5 (72.7) 205 (117.2—285.6) 23.4—820.0
4.4 ± 3.9 (57.1) 3.5 (2—5.8) 1—17 89.3 ± 70.0 (66.7) 54.5 (37.8—165.8) 22—231 94.2 ± 80.0 (27.3) 55.1 (34.9—164.6) 20.3—281.9
7.7 ± 3.8 (100) 7 (5.3—10) 3—19 133.8 ± 83.2 (100) 97.5 (77.5—212) 36—315 344.6 ± 249.1 (100) 298.1 (189.7—370.9) 57.0—1043.4
SD: standard deviation; IQR: interquatile range. For calculation of hydrogel-coated coil volumes, full expansion of the coils was assumed.
Figure 3. 78-year-old woman with a simple pulmonary arteriovenous malformation in left segment 10. A. Left pulmonary arteriogram shows a pulmonary arteriovenous malformation (arrow). The sizes of the venous sac and feeding artery are 8.0 mm and 4.7 mm, respectively. B. Feeding arteriogram obtained immediately after venous sac embolization with additional feeding artery embolization shows the absence of a draining vein. The venous sac is filled with eight hydrogel-coated coils and two bare platinum detachable coils (arrow). The feeding artery was additionally embolized using two bare platinum detachable coils. C. Left pulmonary arteriogram obtained 1 year after venous sac embolization shows neither recanalization nor reperfusion.
for PAVM [1,2]; coils have been widely used for the mechanical occlusion of feeding arteries [3]. The reperfusion or recanalization rates of FAE using coils in patients with PAVMs were reported to range from 3% to 25% [3—6]. Efficacy was mainly evaluated by contrast-enhanced CT in these studies [3—6]. However, reperfusion/recanalization can be overlooked in some PAVMs because CT evaluation is generally based on changes in the size of the venous sac and draining veins rather than changes in the flow dynamics of the PAVM itself. Pulmonary arteriography is the most sensitive modality for examining the blood flow through lesions; it can detect simultaneous enhancements in the feeding artery and draining vein in reperfused PAVMs [22]. Additionally, pulmonary arteriography can distinguish recanalization from other forms of PAVM persistence (e.g., pulmonary-to pulmonary reperfusion) [23]. Accordingly, strict evaluation of the treatment outcomes by pulmonary arteriography performed 1 year after complete embolization showed neither recanalization nor reperfusion in any of the 19 PAVMs. Some recent studies have reported better results for VSE. Hayashi et al. reported that the long-term efficacy of VSE was higher (reperfusions, 0 of 15 PAVMs) than that of FAE
(reperfusions, 11 of 22 PAVMs; P < 0.01) [7]. Kajiwara et al. reported that VSE was technically successful in 47 of 50 PAVMs, with no reperfusions in 42 PAVMs based on CT findings (mean follow-up period, 16 months) [8]. They recommended the tight packing of the venous sac [8]. Conversely, Shimohira et al. reported a reperfusion rate of 49% after 24 months of performing both VSE and FAE [24]. Although the reason was not reported, it is possibly because tight packing of the venous sac was not performed. In the present study, the operator used as many hydrogel-coated coils as possible and, thereafter, added as many bare platinum coils as possible for VSE. Theoretical drawbacks of VSE may include rupture, thrombus formation during embolization, impairment of venous drainage from the normal lung because of coil protrusion into the normal pulmonary veins, and cost intensiveness (higher coil number) [7—10]. However, patients with PAVM who receive FAE alone potentially show reperfusion because of the growth of a missed or previously small accessory artery or collateral flow from the bronchial artery and other systemic arteries into the pulmonary artery that is beyond the level of embolization [3]. Since their
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development in 2002 [12], both animal and clinical studies have reported the embolization of various aneurysms or arteries using hydrogel-coated coils. In one animal study, histological analysis of aneurysms embolized with hydrogelcoated coils indicated that most of the aneurysm cavity was filled with expanded hydrogel [25]. In another animal study, no difference was observed in recanalization between hydrogel-coated coils and fibered coils after 24 h or 7 days, although the percentage of thrombus on the surface of the occlusion was significantly lower with hydrogel-coated coils (42% thrombus, 42% platinum, and 16% hydrogel) than with fibered coils (69% thrombus and 31% platinum and fibers; P = 0.0047). This may account for a lower long-term recanalization rate [26]. In a prospective clinical study on embolization of intracranial aneurysms (HELPS trial), hydrogel-coated coils and platinum coils showed similar safety and recanalization rates [15,16]. Another prospective clinical study showed that hydrogel-coated coils and fibered coils were equally effective for the prophylactic occlusion of the gastroduodenal artery before radioembolization, although the number of coils used was higher in the fibered coil group than in the hydrogel-coated coil group [17]. However, hydrogel-coated coils have disadvantages, such as slight resistance during coil delivery and time limitation [13]. Venous sac injury is possible due to stiffness of these coils [18]. Furthermore, the repositioning time is ≤ 3 min, and the coils can fully expand within 20 min on contact with blood [13,27]. Therefore, it was difficult to complete sac embolization (i.e., flaming, filling, and finishing) using hydrogel-coated coils alone in the present study. A retrospective study reported that 56 of 57 PAVMs were successfully embolized using the hydrogel-coated coils that were used in our study (AZUR® ), with no recanalization noted during a mean follow-up period of 19 (range, 2—47) months [18]. This study reported that the expanded hydrogel polymer contributes to the increased coil volume and tightly embolizes the lesion and that hydrogel-coated coils may prevent recanalization after PAVM embolization [18]. Some complications of transcatheter PAVM embolization have been reported, such as coil migration, bleeding, pain, and thrombosis. In the present study, five minor and one major complications (coil migration) occurred and were treated without any sequelae. In two procedures, the hydrogel-coated coils could not be placed because they were trapped in the microcatheter, although the duration of this event was < 3 min. In our opinion, this did not happen because of expansion of the hydrogel material. Other interesting embolic devices include vascular plugs, microvascular plugs, and second-generation hydrogelcoated coils. Vascular plugs and microvascular plugs are reportedly useful materials for PAVM embolization [28,29]. However, the ideal treatment strategy for PAVMs remains controversial in terms of the embolized site (feeding artery vs. venous sac) and embolic device. Embolization with these recent embolic devices, including the hydrogel-coated coils used in the present study, may be expensive but effective. As another percutaneous treatment, David et al. reported a patient with CT-guided direct percutaneous treatment of a ruptured pulmonary artery pseudoaneurysm using N-butyl cyanoacrylate [30]. However, in this technique, there are possible risks of shower embolization when it is used for the treatment of PAVM.
There are some limitations to this single-center study. First, the hydrogel-coated coil volume was calculated by assuming the complete expansion of the coils. Second, embolization was not performed with hydrogel-coated coils alone. In conclusion, our findings suggest that VSE using hydrogel-coated coils with additional FAE is an effective treatment for PAVM.
Human and animal rights The authors declare that the work described has been carried out in accordance with the Declaration of Helsinki of the World Medical Association revised in 2013 for experiments involving humans as well as in accordance with the EU Directive 2010/63/EU for animal experiments.
Informed consent and patient details The authors declare that this report does not contain any personal information that could lead to the identification of the patient(s). The authors declare that they obtained a written informed consent from the patients and/or volunteers included in the article. The authors also confirm that the personal details of the patients and/or volunteers have been removed.
Funding This work did not receive any grant from funding agencies in the public, commercial, or not-for-profit sectors.
CRediT authorship contribution statement All authors attest that they meet the current International Committee of Medical Journal Editors (ICMJE) criteria for Authorship. Toshihiro Iguchi: Conceptualization, Methodology, Investigation, Data Curation, Writing — Original Draft, Visualization, Supervision. Takao Hiraki: Conceptualization, Methodology, Investigation, Resources, Writing — Review & Editing. Yusuke Matsui: Conceptualization, Methodology, Investigation, Data Curation, Writing — Original Draft, Visualization. Hiroyasu Fujiwara: Investigation, Resources, Writing — Review & Editing. Jun Sakurai: Validation, Writing — Review & Editing. Kenji Baba: Writing — Review & Editing. Shinichi Toyooka: Writing — Review & Editing. Hideo Gobara: Investigation, Resources, Writing — Review & Editing. Susumu Kanazawa: Writing — Review & Editing, Project Administration, Funding Acquisition.
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Disclosure of interest Dr. Iguchi, Dr. Hiraki, Dr. Matsui, and Dr. Baba received lecture fees from Termo. The other authors declare that they have no competing interest.
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Study (HELPS trial): procedural safety and operator-assessed efficacy results. AJNR Am J Neuroradiol 2008;29:217—23. White PM, Lewis SC, Gholkar A, Sellar RJ, Nahser H, Cognard C, et al. Hydrogel-coated coils versus bare platinum coils for the endovascular treatment of intracranial aneurysms (HELPS): a randomised controlled trial. Lancet 2011;377:1655—62. Maleux G, Deroose C, Fieuws S, Van Cutsem E, Heye S, Bosmans H, et al. Prospective comparison of hydrogel-coated microcoils versus fibered platinum microcoils in the prophylactic embolization of the gastroduodenal artery before yttrium-90 radioembolization. J Vasc Interv Radiol 2013;24:797—803. Shimohira M, Kawai T, Hashizume T, Muto M, Kitase M, Shibamoto Y. Usefulness of hydrogel-coated coils in embolization of pulmonary arteriovenous malformations. Cardiovasc Intervent Radiol 2018;41:848—55. Asano Y, Tada A, Shinya T, Masaoka Y, Iguchi T, Sato S, et al. Utility of second-generation single-energy metal artifact reduction in helical lung computed tomography for patients with pulmonary arteriovenous malformation after coil embolization. Jpn J Radiol 2018;36:285—94. Komaki T, Hiraki T, Kanazawa S. Brain infarction after embolization of a pulmonary arteriovenous malformation with metallic coils. Diagn Interv Imaging 2017;98:747—8. Porstmann W. Therapeutic embolization of arteriovenous pulmonary fistula by catheter technique. In: Kelop O, editor. Current Concepts in Pediatric Radiology. Berlin, Germany: Springer; 1977. p. 23—31. Boussel L, Cernicanu A, Geerts L, Gamondes D, Khouatra C, Cottin V, et al. 4D time-resolved magnetic resonance angiography for noninvasive assessment of pulmonary arteriovenous malformations patency. J Magn Reson Imaging 2010;32:1110—6. Woodward CS, Pyeritz RE, Chittams JL, Trerotola SO. Treated pulmonary arteriovenous malformations: patterns of persistence and associated retreatment success. Radiology 2013;269:919—26. Shimohira M, Kawai T, Hashizume T, Ohta K, Nakagawa M, Ozawa Y, et al. Reperfusion rates of pulmonary arteriovenous malformations after coil embolization: evaluation with timeresolved MR angiography or pulmonary angiography. J Vasc Intervent Radiol 2015;26:856—64. Ding YH, Dai D, Lewis DA, Cloft HJ, Kallmes DF. Angiographic and histologic analysis of experimental aneurysms embolized with platinum coils, matrix, and HydroCoil. AJNR Am J Neuroradiol 2005;26:1757—63. Fohlen A, Namur J, Ghegediban H, Laurent A, Wassef M, Pelage JP. Peripheral embolization using hydrogel-coated coils versus fibered coils: short-term results in an animal model. Cardiovasc Intervent Radiol 2018;42:305—12. Cantón G, Levy DI, Lasheras JC. Changes in the intraaneurysmal pressure due to hydro coil embolization. AJNR Am J Neuroradiol 2005;26:904—7. Tau N, Atar E, Mei-Zahav M, Bachar GN, Dagan T, Birk E, et al. Amplatzer vascular plugs versus coils for embolization of pulmonary arteriovenous malformations in patients with hereditary hemorrhagic telangiectasia. Cardiovasc Intervent Radiol 2016;39:1110—4. Bailey CR, Arun A, Towsley M, Choi WK, Betz JF, MacKenzie S, et al. MVP TM micro vascular plug system for the treatment of pulmonary arteriovenous malformations. Cardiovasc Intervent Radiol 2019;42:389—95. David A, Liberge R, Perret C, Frampas E, Douane F. CT-guided direct percutaneous treatment of a ruptured pulmonary artery pseudoaneurysm using N-butyl cyanoacrylate. Diagn Interv Imaging 2017;98:903—4.
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ORIGINAL ARTICLE /Interventional imaging
Embolization using hydrogel-coated coils for pulmonary arteriovenous malformations T. Iguchi a,∗, T. Hiraki a, Y. Matsui a, H. Fujiwara b, J. Sakurai c, K. Baba d, S. Toyooka e, H. Gobara a, S. Kanazawa a a
Department of Radiology, Okayama University Medical School, 2-5-1 Shikata-cho kita-ku, Okayama 700-8558, Japan b Department of Radiology, Okayama City Hospital, Okayama 700-8557, Japan c Center for Innovative Clinical Medicine, Okayama University Hospital, Okayama 700-8558, Japan d Interventional Radiology Center, Okayama University Hospital, Okayama 700-8558, Japan e Department of General Thoracic Surgery, Okayama University Medical School, Okayama 700-8558, Japan
KEYWORDS Pulmonary arteriovenous fistulas; Lung; Arteriovenous malformation; Embolization
∗
Abstract Purpose: To prospectively evaluate the efficacy and safety of embolization using hydrogelcoated coils for the treatment of pulmonary arteriovenous malformations (PAVMs). Materials and methods: The outcomes of 21 PAVMs in 19 patients (3 men and 16 women; mean age, 58.8 ± 15.2 [SD] years; age range 14—78 years) treated by venous sac embolization (VSE) with additional feeding artery embolization were prospectively evaluated. For VSE, using one or more 0.018-inch hydrogel-coated coils was mandatory. Recanalization and/or reperfusion were evaluated by pulmonary arteriography 1 year after embolization. Results: The mean feeding artery and venous sac sizes were 4.0 mm and 8.5 mm, respectively. Embolization was successfully completed in 20/21 PAVMs, yielding a technical success rate of 95%. The feeding artery was also embolized in 17/20 successful PAVMs (85%). A technical failure occurred in one PAVM, where embolization was abandoned because of migration of one bare coil to the left ventricle. The mean numbers of hydrogel-coated coils and bare platinum detachable coils used for VSE were 3.3 ± 2.1 (SD) (range, 1—8) and 4.4 ± 3.9 (SD) (range, 1—17), respectively. The mean percentages of hydrogel-coated coils in number, length, and estimated volume were 42.9%, 33.3%, and 72.7% respectively. One patient with one PAVM was lost to follow-up after 3 months. Neither recanalization nor reperfusion was noted in the remaining 19 PAVMs (success rate, 19/19 [100%]). One grade 4 (coil migration) adverse event occurred, and it was treated without any sequelae.
Corresponding author. E-mail address: [email protected] (T. Iguchi).
https://doi.org/10.1016/j.diii.2019.10.008 2211-5684/© 2019 Soci´ et´ e franc ¸aise de radiologie. Published by Elsevier Masson SAS. All rights reserved.
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T. Iguchi et al. Conclusion: VSE using hydrogel-coated coils with additional feeding artery embolization is a safe and effective treatment for PAVM. © 2019 Soci´ et´ e franc ¸aise de radiologie. Published by Elsevier Masson SAS. All rights reserved.
Percutaneous transcatheter embolization is the gold standard for the treatment of pulmonary arteriovenous malformations (PAVMs) because it is effective in lowering the risk of embolism and other complications [1,2]. Feeding artery embolization (FAE) using coils is the conventional mode of treatment [3—6]. However, with recent advances in interventional techniques and equipment, venous sac embolization (VSE) seems to be safer and more feasible [7]. Some studies have reported the efficacy of VSE in the treatment of PAVMs [7—11], and one retrospective study showed that VSE is associated with a significantly lower reperfusion rate than FAE [7]. Hydrogel-coated coils, which were recently introduced, comprise a carrier platinum coil coated with an expandable hydrogel material that undergoes a nine-fold increase in volume when placed in a physiological environment [12]. Therefore, hydrogel-coated coils offer the advantage of a greater filling volume and, theoretically, a lower risk of recanalization than bare platinum coils [13]. The efficacy of these coils in the embolization of arteries or aneurysms has been reported [14—17]; it is speculated that they enhance the treatment efficacy of VSE for PAVMs when used with other types of coils, such as fibered or bare platinum coils. Some retrospective studies have evaluated the outcomes of transcatheter embolization using hydrogel-coated coils for PAVMs with both advantages (e.g., increase in packing density) and disadvantages (e.g., slight resistance in the coil delivery) [13,14,18]. However, more robust and prospective data are needed for determining the efficacy and safety of VSE using these coils accurately. The purpose of this study was to prospectively evaluate the efficacy and safety of VSE using hydrogel-coated coils with additional FAE for PAVMs.
Materials and methods This study was prospectively conducted at a single center between June 2014 and May 2017. The study was approved by the institutional review board (approval number, m29006) and conducted in accordance with the Declaration of Helsinki. All patients provided written informed consent before participation. The study has been registered in the University Hospital Medical Information Network Clinical Trials Registry (study ID: UMIN000014360).
Patient selection The inclusion criteria were as follows:
• presence of PAVM confirmed by chest computed tomography (CT) (slice thickness, ≤ 3 mm); • patient with a history of one or more of the following conditions: ◦ ◦ ◦ ◦ ◦
brain infarction and/or abscess, transient ischemic attack, hemoptysis, hypoxemia, feeding pulmonary artery diameter of ≥ 3 mm (≥ 2 mm in patients with hereditary hemorrhagic telangiectasia);
• adequate cardiac, hepatic, renal, respiratory, coagulation, and bone marrow functions; • an Eastern Cooperative Oncology Group performance status of 0—2; • a life expectancy ≥ 1 year. The exclusion criteria were as follows: • history of allergy to iodinated contrast material, active asthma, or pulmonary hypertension; • presence of single lung; • impaired contralateral lung function; • an estimated glomerular filtration rate of < 30 ml/min (excluding dialysis); • a Child—Pugh score ≥ 9; • heart failure (New York Heart Association classification, ≥ III); • uncontrollable malignant disease; • active infection or an active inflammatory process; • a body temperature ≥ 38 ◦ C; • pregnancy and, • ineligibility determined by the responding physician. Between June 2014 and May 2017, 4 patients (6 PAVMs) underwent surgery and 21 patients (28 PAVMs) underwent transcatheter embolization at our institution. In 28 PAVMs performed transcatheter embolization, 7 PAVMs were excluded according to the ineligibility determined by the responding physician: • patients’ refusal (n = 4 PAVMs [4 patients]), • patient’s arrhythmia (Wolff-Parkinson-White syndrome; n = 2 PAVMS [1 patient]), • small feeding pulmonary artery diameter (< 3 mm) (n = 1 PAVM [1 patient]) (Fig. 1). Therefore, 21 PAVMs in 19 patients (3 men, 16 women) with a mean age of 58.8 ± 15.2 (SD) years (range: 14—78 years) were eligible for inclusion (Table 1). Two patients have a history of hereditary hemorrhagic telangiectasia. Two PAVMs in two patients were treated in two separate sessions. The mean sizes of the feeding artery and venous sac
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Flow chart diagram of patient inclusion and exclusion.
Table 1 Characteristics of 21 pulmonary arteriovenous malformations in 19 patients. Characteristics Type Location (lobe)
Diameter of feeding artery (mm) Diameter of venous sac (mm) Diameter of draining vein (mm) Feeding artery embolizationa
Simple/ Complex Right upper lobe Right middle lobe Right lower lobe Left upper lobe Left lower lobe Mean ± SD [range] Median (IQR)
19/21 (90%) 2/21 (10%) 2/21 (10%) 3/21 (14%) 4/21 (19%) 5/21 (24%) 7/21 (33%) 4.0 ± 0.8 [2.3—6.0] 4.0 (3.5—4.5)
Mean ± SD [range] 8.5 ± 3.0 [3.1—16.0] Median (IQR) 8.1 (7.0—9.3) Mean ± SD [range] 4.6 ± 0.9 [2.4—6.5] Median (IQR) 4.5 (4.1—5.2) Yes No
17/20 (85%) 3/20 (15%)
SD: standard deviation; IQR: interquartile range. a In one patient, embolization was abandoned.
were 4.0 ± 0.8 (SD) mm (range: 2.3—6.0 mm) and 8.5 ± 3.0 (SD) mm (range: 3.1—16.0 mm), respectively. Among the 21 PAVMs, eight were described in a previous study reporting the quality of lung CT images acquired after single-energy metal artifact reduction [19].
Study endpoints The primary endpoint was the efficacy of VSE using hydrogelcoated coils with additional FAE. The secondary endpoint was safety, as assessed by the evaluation of adverse events
(AEs). Efficacy was defined as the absence of recanalization and reperfusion on pulmonary arteriography performed 1 year after embolization. Recanalization was defined as venous sac blood flow from the recanalized artery that had undergone coil embolization, while reperfusion was defined as a venous sac or draining vein blood flow, regardless of the inflow route [7]. To identify the number of procedures required for evaluation of the efficacy rate, we performed one-sample binomial t-tests (null hypothesis H0, P = 0; alternative hypothesis H1, P = ). For an efficacy rate with 0 = 0.50 and = 0.80, values of ␣ = 0.05 and  = 0.20 yielded a sample size of 19. This number was increased by 10% in anticipation of protocol deviations. Therefore, we enrolled 21 PAVMs.
Transcatheter coil embolization Through the femoral vein sheath, pulmonary arteriography was performed using a 4- or 5-F angiographic catheter for the assessment of PAVMs. Immediately after femoral sheath insertion, 3000 or 4000 IU of heparin was intravenously administered for prophylactic anticoagulation, followed by additional administration of 1000 IU/h. The catheter was advanced into the feeding artery of PAVM, as close to the venous sac as possible. Subsequently, a microcatheter was advanced into the venous sac through the base catheter, and VSE was performed. A combination of one or more 0.018-inch hydrogel-coated coils (AZUR® ; Terumo, Tokyo, Japan) and 0.010—0.020-inch bare platinum detachable coils (Target® , Stryker Fremont; DELTAFILL® , MICRUSFRAME® S or MICRUSFRAME® C, Johnson & Johnson KK; or Penumbra Coil 400TM , Medico’s Hirata Inc.) was used for embolization. Subsequently, the microcatheter was pulled back to the distal feeding artery, and embolization was continued if the draining vein was still visualized by feeding arteriography. In each procedure, the operator decided which coils to use and attempted to use as many hydrogel-coated coils as possible. For FAE, fibered platinum pushable coils (Tornado® Embolization Coil or Hilal Embolization MicrocoilTM , Cook
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Figure 2. A 14-year-old male with a complex pulmonary arteriovenous malformation in left segment 4. A. Left A4 pulmonary arteriogram shows a pulmonary arteriovenous malformation (arrow). The maximum sizes of the venous sac and feeding arteries are 8.1 mm and 3.5 mm, respectively. B. Fluoroscopy shows one bare coil migration (arrow). C. Fluoroscopy shows that the migrated coil (arrow) is successfully retrieved using a snare.
Japan; or C-STOPPER® , Piolax Medical Devices) were also used at the operator’s discretion. After completion of the procedure, pulmonary arteriography was performed to confirm complete embolization.
Follow-up examination and efficacy assessment Physical examinations, laboratory tests (including blood counts and biochemical examinations) and chest radiography were performed 1 and 3 days, 1 and 6 months, and 1 year after embolization. Chest CT was performed 3 days and 1 and 6 months after embolization. After plain CT scanning, a non-ionic iodine contrast medium (300 mgI/mL and total dose of 600 mgI/kg) was administered intravenously at a rate of 3 ml/s, and CT images were acquired 14, 33, and 90 s after initiation of contrast material administration. From each data set, in addition to contiguous 5-mm transverse CT images of the whole thorax, contiguous thin-section (1mm thick) transverse CT images of the area of interest were reconstructed with both mediastinal and lung windows. To evaluate the efficacy of VSE using hydrogel-coated coils with additional FAE, pulmonary arteriography was performed using a catheter inserted via the femoral or cubital vein one year after embolization. Pulmonary arteriograms were divided into two groups according to the presence or absence of recanalization and reperfusion.
Safety assessment All AEs that occurred during the embolization and follow-up period were recorded and graded according to the Common Terminology Criteria for Adverse Events (ver. 4.0).
Results VSE using hydrogel-coated coils with additional FAE was successfully completed for 20 of the 21 PAVMs (95.2%). The remaining PAVM was complex type and considered a technical failure (Fig. 2). Although FAE was additionally attempted after VSE, one bare coil migrated to the left ventricle via a missed communication. Therefore, embolization was abandoned, and the coil was immediately and successfully retrieved using a snare. Re-embolization was performed
successfully 5 months later. Although embolizations were completed, the hydrogel-coated coil unraveled in two procedures; in the other two procedures, they could not be placed because they were trapped in the microcatheter. The mean number, total length, and total volume of hydrogel-coated coils used for VSE in the 20 successful PAVMs were 3.3 ± 2.1 (SD) (range, 1—8), 44.5 ± 37.6 (SD) (range, 4—140) cm, and 250.4 ± 214.5 (SD) (range, 23.4—820.0) mm3 , respectively; the mean percentages of hydrogelcoated coils used for VSE were 42.9% in number, 33.3% in length, and 72.7% in volume. Assuming a cylindrical coil shape, the volume of each coil was calculated using the following formula: coil volume = × (coil radius)2 × (coil length) [18]. Details of the coils used for VSE are shown in Table 2. FAE was also performed in 17 of the 20 successful PAVMs, with the mean number of hydrogel-coated coils, bare coils, and fibered coils used being 0.2 (range, 0—1), 1.9 (range, 0—4), and 1.0 (range, 0—6), respectively. One patient with one PAVM was lost to follow-up 3 months after complete embolization. Pulmonary arteriography, performed 1 year after the procedure, showed neither recanalization nor reperfusion in the remaining 19 PAVMs (Fig. 3). Arteriography was performed via the brachial vein for one PAVM because the patient complained of discomfort when the catheter passed the heart and refused to undergo direct pulmonary arteriography. For the remaining 18 PAVMs, left or right pulmonary arteriography was performed. Additionally, feeding pulmonary arteriography (n = 5 PAVMs), lower pulmonary arteriography (n = 7 PAVMs), and middle pulmonary arteriography (n = 1 PAVM) were performed where required. Among the 21 procedures, two grade 1 (fever and noncardiac chest pain), three grade 2 (headache, atrial fibrillation, and cerebral infarction), and one grade 4 (previously mentioned coil migration) AEs were recorded. No venous sac injury occurred. The one major AE (grade 4) was completely treated without any sequelae. One patient unexpectedly complained of dysarthria caused by cerebral infarction 11 h after the procedure. This AE was immediately and spontaneously improved; it has been reported elsewhere [20].
Discussion Since it was first reported in 1977 [21], transcatheter embolization has been accepted as a standard treatment
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Table 2 Details of coils used for the successful sac embolizaion of 20 pulmonary arteriovenous malformations in 18 patients.
Number
Length (cm) Volume (mm3 )
Mean ± SD (%) Median (IQR) Range Mean ± SD (%) Median (IQR) Range Mean ± SD (%) Median (IQR) Range
Hydrogel-coated coil
Bare platinum detachable coil
Total
3.3 ± 2.1 (42.9) 2 (2—5) 1—8 44.5 ± 37.6 (33.3) 35 (20—57.5) 4—140 250.4 ± 214.5 (72.7) 205 (117.2—285.6) 23.4—820.0
4.4 ± 3.9 (57.1) 3.5 (2—5.8) 1—17 89.3 ± 70.0 (66.7) 54.5 (37.8—165.8) 22—231 94.2 ± 80.0 (27.3) 55.1 (34.9—164.6) 20.3—281.9
7.7 ± 3.8 (100) 7 (5.3—10) 3—19 133.8 ± 83.2 (100) 97.5 (77.5—212) 36—315 344.6 ± 249.1 (100) 298.1 (189.7—370.9) 57.0—1043.4
SD: standard deviation; IQR: interquatile range. For calculation of hydrogel-coated coil volumes, full expansion of the coils was assumed.
Figure 3. 78-year-old woman with a simple pulmonary arteriovenous malformation in left segment 10. A. Left pulmonary arteriogram shows a pulmonary arteriovenous malformation (arrow). The sizes of the venous sac and feeding artery are 8.0 mm and 4.7 mm, respectively. B. Feeding arteriogram obtained immediately after venous sac embolization with additional feeding artery embolization shows the absence of a draining vein. The venous sac is filled with eight hydrogel-coated coils and two bare platinum detachable coils (arrow). The feeding artery was additionally embolized using two bare platinum detachable coils. C. Left pulmonary arteriogram obtained 1 year after venous sac embolization shows neither recanalization nor reperfusion.
for PAVM [1,2]; coils have been widely used for the mechanical occlusion of feeding arteries [3]. The reperfusion or recanalization rates of FAE using coils in patients with PAVMs were reported to range from 3% to 25% [3—6]. Efficacy was mainly evaluated by contrast-enhanced CT in these studies [3—6]. However, reperfusion/recanalization can be overlooked in some PAVMs because CT evaluation is generally based on changes in the size of the venous sac and draining veins rather than changes in the flow dynamics of the PAVM itself. Pulmonary arteriography is the most sensitive modality for examining the blood flow through lesions; it can detect simultaneous enhancements in the feeding artery and draining vein in reperfused PAVMs [22]. Additionally, pulmonary arteriography can distinguish recanalization from other forms of PAVM persistence (e.g., pulmonary-to pulmonary reperfusion) [23]. Accordingly, strict evaluation of the treatment outcomes by pulmonary arteriography performed 1 year after complete embolization showed neither recanalization nor reperfusion in any of the 19 PAVMs. Some recent studies have reported better results for VSE. Hayashi et al. reported that the long-term efficacy of VSE was higher (reperfusions, 0 of 15 PAVMs) than that of FAE
(reperfusions, 11 of 22 PAVMs; P < 0.01) [7]. Kajiwara et al. reported that VSE was technically successful in 47 of 50 PAVMs, with no reperfusions in 42 PAVMs based on CT findings (mean follow-up period, 16 months) [8]. They recommended the tight packing of the venous sac [8]. Conversely, Shimohira et al. reported a reperfusion rate of 49% after 24 months of performing both VSE and FAE [24]. Although the reason was not reported, it is possibly because tight packing of the venous sac was not performed. In the present study, the operator used as many hydrogel-coated coils as possible and, thereafter, added as many bare platinum coils as possible for VSE. Theoretical drawbacks of VSE may include rupture, thrombus formation during embolization, impairment of venous drainage from the normal lung because of coil protrusion into the normal pulmonary veins, and cost intensiveness (higher coil number) [7—10]. However, patients with PAVM who receive FAE alone potentially show reperfusion because of the growth of a missed or previously small accessory artery or collateral flow from the bronchial artery and other systemic arteries into the pulmonary artery that is beyond the level of embolization [3]. Since their
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development in 2002 [12], both animal and clinical studies have reported the embolization of various aneurysms or arteries using hydrogel-coated coils. In one animal study, histological analysis of aneurysms embolized with hydrogelcoated coils indicated that most of the aneurysm cavity was filled with expanded hydrogel [25]. In another animal study, no difference was observed in recanalization between hydrogel-coated coils and fibered coils after 24 h or 7 days, although the percentage of thrombus on the surface of the occlusion was significantly lower with hydrogel-coated coils (42% thrombus, 42% platinum, and 16% hydrogel) than with fibered coils (69% thrombus and 31% platinum and fibers; P = 0.0047). This may account for a lower long-term recanalization rate [26]. In a prospective clinical study on embolization of intracranial aneurysms (HELPS trial), hydrogel-coated coils and platinum coils showed similar safety and recanalization rates [15,16]. Another prospective clinical study showed that hydrogel-coated coils and fibered coils were equally effective for the prophylactic occlusion of the gastroduodenal artery before radioembolization, although the number of coils used was higher in the fibered coil group than in the hydrogel-coated coil group [17]. However, hydrogel-coated coils have disadvantages, such as slight resistance during coil delivery and time limitation [13]. Venous sac injury is possible due to stiffness of these coils [18]. Furthermore, the repositioning time is ≤ 3 min, and the coils can fully expand within 20 min on contact with blood [13,27]. Therefore, it was difficult to complete sac embolization (i.e., flaming, filling, and finishing) using hydrogel-coated coils alone in the present study. A retrospective study reported that 56 of 57 PAVMs were successfully embolized using the hydrogel-coated coils that were used in our study (AZUR® ), with no recanalization noted during a mean follow-up period of 19 (range, 2—47) months [18]. This study reported that the expanded hydrogel polymer contributes to the increased coil volume and tightly embolizes the lesion and that hydrogel-coated coils may prevent recanalization after PAVM embolization [18]. Some complications of transcatheter PAVM embolization have been reported, such as coil migration, bleeding, pain, and thrombosis. In the present study, five minor and one major complications (coil migration) occurred and were treated without any sequelae. In two procedures, the hydrogel-coated coils could not be placed because they were trapped in the microcatheter, although the duration of this event was < 3 min. In our opinion, this did not happen because of expansion of the hydrogel material. Other interesting embolic devices include vascular plugs, microvascular plugs, and second-generation hydrogelcoated coils. Vascular plugs and microvascular plugs are reportedly useful materials for PAVM embolization [28,29]. However, the ideal treatment strategy for PAVMs remains controversial in terms of the embolized site (feeding artery vs. venous sac) and embolic device. Embolization with these recent embolic devices, including the hydrogel-coated coils used in the present study, may be expensive but effective. As another percutaneous treatment, David et al. reported a patient with CT-guided direct percutaneous treatment of a ruptured pulmonary artery pseudoaneurysm using N-butyl cyanoacrylate [30]. However, in this technique, there are possible risks of shower embolization when it is used for the treatment of PAVM.
There are some limitations to this single-center study. First, the hydrogel-coated coil volume was calculated by assuming the complete expansion of the coils. Second, embolization was not performed with hydrogel-coated coils alone. In conclusion, our findings suggest that VSE using hydrogel-coated coils with additional FAE is an effective treatment for PAVM.
Human and animal rights The authors declare that the work described has been carried out in accordance with the Declaration of Helsinki of the World Medical Association revised in 2013 for experiments involving humans as well as in accordance with the EU Directive 2010/63/EU for animal experiments.
Informed consent and patient details The authors declare that this report does not contain any personal information that could lead to the identification of the patient(s). The authors declare that they obtained a written informed consent from the patients and/or volunteers included in the article. The authors also confirm that the personal details of the patients and/or volunteers have been removed.
Funding This work did not receive any grant from funding agencies in the public, commercial, or not-for-profit sectors.
CRediT authorship contribution statement All authors attest that they meet the current International Committee of Medical Journal Editors (ICMJE) criteria for Authorship. Toshihiro Iguchi: Conceptualization, Methodology, Investigation, Data Curation, Writing — Original Draft, Visualization, Supervision. Takao Hiraki: Conceptualization, Methodology, Investigation, Resources, Writing — Review & Editing. Yusuke Matsui: Conceptualization, Methodology, Investigation, Data Curation, Writing — Original Draft, Visualization. Hiroyasu Fujiwara: Investigation, Resources, Writing — Review & Editing. Jun Sakurai: Validation, Writing — Review & Editing. Kenji Baba: Writing — Review & Editing. Shinichi Toyooka: Writing — Review & Editing. Hideo Gobara: Investigation, Resources, Writing — Review & Editing. Susumu Kanazawa: Writing — Review & Editing, Project Administration, Funding Acquisition.
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Disclosure of interest Dr. Iguchi, Dr. Hiraki, Dr. Matsui, and Dr. Baba received lecture fees from Termo. The other authors declare that they have no competing interest.
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Please cite this article in press as: Iguchi T, et al. Embolization using hydrogel-coated coils for pulmonary arteriovenous malformations. Diagnostic and Interventional Imaging (2019), https://doi.org/10.1016/j.diii.2019.10.008