Clinical Radiology xxx (2015) e1ee8
Contents lists available at ScienceDirect
Clinical Radiology journal homepage: www.clinicalradiologyonline.net
Transarterial embolisation of renal arteriovenous malformation: safety and efficacy in 24 patients with follow-up H.-J. Eom a, J.H. Shin a, *, Y.J. Cho b, D.H. Nam c, G.-Y. Ko a, H.-K. Yoon a a
Department of Radiology and Research Institute of Radiology, Asan Medical Center, University of Ulsan College of Medicine, Seoul, South Korea b Department of Radiology, Busan Paik Hospital, Inje University College of Medicine, Busan, South Korea c Department of Radiology, Kyung Hee University Hospital at Gangdong, School of Medicine, Kyung Hee University, Seoul, South Korea
art icl e i nformat ion Article history: Received 29 January 2015 Received in revised form 6 May 2015 Accepted 5 June 2015
AIM: To evaluate the efficacy and safety of renal artery embolisation (RAE) for renal arteriovenous malformation (AVM) as well as its outcomes. MATERIALS AND METHODS: The technical and clinical success rates, radiological and laboratory findings, and complications of RAE for 31 renal AVMs in 24 patients (M:F¼9:15, mean age 46 years) at two separate medical institutions were retrospectively evaluated. Technical success was defined as complete occlusion of feeding arteries with no residual nidus seen on post-treatment angiography. Clinical failure was defined as recurrence of haematuria, presence of AVM on follow-up ultrasound or computed tomography, repeated RAE or surgery for the control of haematuria. Overall clinical success was defined as resolution haematuria or disappearance of AVM on follow-up imaging after single or multiple sessions of RAE. RESULTS: Types of renal AVM were AVM, arterio-venous fistula (AVF) with intranidal aneurysm, and acquired AVF in 19, 1, and 4 patients, respectively. 18 patients (75%) underwent a single session of RAE, while 6 patients (25%) had two or more sessions of RAE. The level of embolisation was feeder, segmental artery, and main renal artery in 28 (90%), 2 (6%), and 1 (4%) procedures, respectively. Coil, n-butyl 2-cyanoacrylate, and polyvinyl alcohol were the most frequently chosen embolic materials and were used in 19, 14, and 8 procedures, respectively. The clinical success rate after initial RAE was 67% (16/24). Overall clinical success rate, including multisession RAE, was 88% (21/24). The technical success rate of 31 procedures was 65% (20/31). Among 11 technical failures in 10 patients, 4 achieved clinical success without additional RAE, 3 underwent second session RAE to achieve clinical success, and 3 patients underwent nephrectomy due to recurrence. CONCLUSION: RAE is a safe and effective treatment for renal AVM. Technical failure of RAE does not always lead to clinical failure and multiple embolisation sessions may be effective for recurrent renal AVM. Ó 2015 The Royal College of Radiologists. Published by Elsevier Ltd. All rights reserved.
* Guarantor and correspondent: J.H. Shin, Department of Radiology and Research Institute of Radiology, Asan Medical Center, University of Ulsan College of Medicine, Asanbyeongwon-gil 86, Seoul, 138-736, South Korea. Tel.: þ82 2 3010 4380; fax: þ82 2 476 0090. E-mail address: [email protected] (J.H. Shin). http://dx.doi.org/10.1016/j.crad.2015.06.079 0009-9260/Ó 2015 The Royal College of Radiologists. Published by Elsevier Ltd. All rights reserved.
Please cite this article in press as: Eom H-J, et al., Transarterial embolisation of renal arteriovenous malformation: safety and efficacy in 24 patients with follow-up, Clinical Radiology (2015), http://dx.doi.org/10.1016/j.crad.2015.06.079
e2
H.-J. Eom et al. / Clinical Radiology xxx (2015) e1ee8
Introduction Renal arteriovenous malformation (AVM) is a pathological communication between the arterial and venous circulation that bypasses capillary bed. AVM could be either congenital or acquired.1 Acquired AVM, arterio-venous fistula (AVF), tend to manifest as a single linear connecting vessel, comprise 70e80% of renal arteriovenous abnormalities and usually result from trauma, biopsy, surgery, malignancy, or inflammation.2 Two types of congenital renal AVM, cirsoid and cavernous type, are described. Cirsoid AVM should fulfil certain criteria, which includes no prior history of renal injury or disease and typical angiographic findings with tortuous vascular channels between segmental or interlobar renal arteries and veins.3 Cavernous AVM shows a single dilated vessels and is less common.4 Patients with renal AVM usually present with gross haematuria or flank pain with occasional accompanying hypertension or heart failure.3,5,6 Renal angiography is used to confirm the presence of renal AVM and in planning treatment. To date, renal AVM has been treated by surgery, such as nephrectomy. Endovascular approaches for treating AVM are gaining popularity.7 The introduction of smaller delivery catheters and more precise delivery of embolic materials have drastically reduced the morbidity associated with this technique.1,8e12 Therefore, currently, this treatment modality is becoming popular as it provides maximal preservation of functioning renal parenchyma as well as treating the disease and symptoms. Several case reports and case series of renal artery embolisation (RAE) and ablation of renal AVM have reported successful results1,13e15; however, there are few studies regarding the comprehensive analysis of clinical and radiological outcomes and effectiveness of multiple RAE sessions based on long-term follow-up data. The present study was undertaken to evaluate the efficacy and safety of RAE for renal AVM as well as its long-term outcomes.
Material and methods Patients From January 2001 to December 2014, 31 RAE procedures were performed for 24 renal AVMs in 24 patients at two, separate medical institutions. A total of 24 patients, i.e., 9 men (age range, 16e71 years; mean age 43 years) and 15 women (age range, 30e69 years; mean age 47 years) were included in this study. Clinical medical records were retrospectively reviewed for symptoms and signs of renal AVM, underlying medical status and baseline renal function, i.e., blood urea nitrogen/ creatinine (BUN/Cr). Imaging studies obtained before and after RAE, including computed tomography (CT) and ultrasound images, were reviewed. Angiographic findings, diameter of the renal AVM, embolisation level and embolic materials used were analysed by reviewing the medical
charts and angiography images. The longest diameter of the AVM nidus was measured from the angiographic images. Technical and clinical outcomes of RAE were assessed. The study was approved by the local ethics committee, and informed consent for data use was waived due to retrospective study design. Informed consent for the procedure was obtained from all patients before the procedure.
Embolisation technique Transcatheter RAE was performed by six, board-certified radiologists with 5e26 years of clinical experience in endovascular therapy. The right common femoral artery was routinely accessed and after selecting the right or left renal artery using a 0.035-inch hydrophilic guidewire (Radifocus; Terumo, Tokyo, Japan) and a standard 5-F catheter, renal arteriography was performed. Target vessels for embolisation were determined using digital subtraction angiography by identifying abnormal feeding arteries to the nidus. A microcatheter (Renegade, Boston Scientific, Cork, Ireland, or Microferret, Cook, Bloomington, IN, USA) was advanced into all identifiable target vessels, which were subsequently embolised using various embolic materials. Selection of embolic material was made on a case-bycase basis according to the decision of interventional radiologist at the time of procedure. Embolic materials, including coils, particles including polyvinyl alcohol (PVA) and gelatin-sponge particles (GSP), liquid embolics including alcohol and n-butyl 2-cyanoacrylate (NBCA), and vascular plugs, were used. In all patients, final arteriogram was performed to confirm successful occlusion of target vessels.
Definitions and study endpoints Clinical failure was defined as recurrence of haematuria, presence of AVM on follow-up ultrasound or CT, repeated RAE or surgery for the control of haematuria. Overall clinical success was defined as resolution of haematuria or disappearance of AVM on follow-up imaging after single or multiple sessions of RAE. Clinical outcome was assessed by reviewing the medical records and radiological examinations performed after RAE and by identifying any complications attributable to RAE. Technical success was defined as complete occlusion of fine feeding arteries, and thus, no residual AVM nidus or draining veins seen on immediate post-treatment angiography. Complication was classified as major or minor according to the guidelines of the Society of Interventional Radiology Standards of Practice Committee.16 Major complication included major therapy, an unexpected increase in the level of care or prolonged hospitalisation (>48 hours), permanent adverse sequelae or death. Minor complication included minor therapy such as overnight admission for observation only.
Please cite this article in press as: Eom H-J, et al., Transarterial embolisation of renal arteriovenous malformation: safety and efficacy in 24 patients with follow-up, Clinical Radiology (2015), http://dx.doi.org/10.1016/j.crad.2015.06.079
H.-J. Eom et al. / Clinical Radiology xxx (2015) e1ee8
e3
Figure 1 A 55-year-old woman with haematuria (patient 5). (a) Left renal artery angiogram shows AVM (arrow) with multiple, fine feeding vessels (arrowheads) arising from different segmental arteries. (b) Left renal artery angiogram obtained after coil embolisation shows residual opacification of the fine feeding vessels (arrows; technical failure); however, the haematuria resolved during the procedure. (c) Left renal artery angiogram obtained 1 month after the initial embolisation shows recanalisation of the feeders (arrows). The patient had recurrence of haematuria. (d) Several branches were embolised with NBCA and GSP. The final angiogram shows complete occlusion of the AVM nidus and no visible draining veins. (e) Coronal reconstructed CT image obtained 5 years after embolisation shows mild renal parenchymal atrophy (arrows) with complete obliteration of the AVM nidus. The patient was symptom-free.
Results Patient characteristics Clinical characteristics and outcomes of the 24 patients and 31 procedures are summarised in Table 1. 18 patients (75%) underwent a single session of RAE, whereas 6 patients (25%) had two or more sessions of RAE. Therefore, a total of 31 RAE procedures were performed in 24 patients. 17 patients (71%) had haematuria or flank pain, and 7 (29%) were asymptomatic. One patient had a single kidney with a past medical history of nephrectomy for renal cell carcinoma. All patients underwent CT or ultrasound before angiography. Among 22 patients who underwent CT, 16 patients
(72%) were given the correct diagnosis, 5 (23%) showed haematoma in renal pelvis and hydronephrosis, and in one patient (5%) AVM was diagnosed as an aneurysm. Among 10 patients who underwent ultrasound, 7 (70%) received the correct diagnosis, two (20%) failed to detect any abnormality, and in one patient (10%) AVM was diagnosed as an aneurysm. AVM diagnosed as an aneurysm was found to have an intranidal aneurysm on renal angiogram. Diagnostic renal angiography was performed after excluding other causes of haematuria, such as urinary tract infection or tumorous condition in the urinary bladder by performing laboratory tests or cystoscopy. Three patients (13%) developed AVF after partial nephrectomy for RCC at the resection margin and one patient
Please cite this article in press as: Eom H-J, et al., Transarterial embolisation of renal arteriovenous malformation: safety and efficacy in 24 patients with follow-up, Clinical Radiology (2015), http://dx.doi.org/10.1016/j.crad.2015.06.079
e4
Patient no./age/sex
1/44/F 2/61/F 3/42/F 4/67/F 5/55/F 6/50/M 7/30/F 8/38/M 9/16/M 10/24/M 11/53/M 12/48/F 13/41/F 14/34/F 15/39/F 16/49/F 17/28/M 18/51/M 19/59/F 20/71/M 21/36/F 22/34/F 23/69/F 24/55/M
Type
AVM AVM AVM AVM AVM AVM AVM AVM AVM AVM AVM AVM AVM AVM AVM AVM AVM AVF AVF AVF AVF AVM AVM AVF
Nidus (cm)
2.1 2.6 2.2 3.8 2.7 6.7 3.5 2.5 2.6 1.5 1.3 2.2 3 1 1.5 1 1.5 e e e e 2.3 3.5 e
Embolic materialsa
Coil/CoilþGSP/CoilþGSP CoilþPVA/NBCA CoilþPVA CoilþPVA Coil/NBCAþGSP CoilþNBCAþplug NBCA CoilþPVA/Coilþethanol PVAþGSP PVA Coil PVAþethanol/CoilþNBCA CoilþNBCAþethanol/NBCA NBCA Ethanol NBCA CoilþNBCA CoilþNBCA Coil PVAþNBCA NBCAþplug CoilþNBCA Coil Plug
Outcome Technical successa
Clinical successb
Y/Y/Y N/Y N N N/Y Y N Y/Y Y Y Y N/Y N/N Y Y Y N Y Y N Y Y N Y
Y Y Y Y Y Y N, nephrectomy Y Y Y Y Y N, nephrectomy Y Y Y Y Y Y N, nephrectomy Y Y Y Y
Follow-up (days)a
Remarks
34/199/566 573/1167 267 1455 2486 187 e 7/14 2118 16 1318 559/4 448/e 1855 564 97 315 795 301 e 276 104 447 1653
e Main renal artery embolisation in second RAE e e e e Renal vein balloon occlusion, pulmonary embolism e e e e e Nephrectomy e e Renal vein balloon occlusion, percutaneous NBCA e Biopsy site, transplanted kidney Nephrectomy site Nephrectomy site, unilateral kidney Intranidal aneurysm, renal vein plug occlusion e e Nephrectomy site
AVM, arteriovenous malformation; AVF, arteriovenous fistula; GSP, gelatin sponge particle; NBCA, n-butyl 2-cyanoacrylate; PVA, polyvinyl alcohol; ø, diameter. a The content of each embolisation session is separately displayed by using slash in cases of multiple RAE sessions. b Overall clinical success is displayed.
H.-J. Eom et al. / Clinical Radiology xxx (2015) e1ee8
Please cite this article in press as: Eom H-J, et al., Transarterial embolisation of renal arteriovenous malformation: safety and efficacy in 24 patients with follow-up, Clinical Radiology (2015), http://dx.doi.org/10.1016/j.crad.2015.06.079
Table 1 Clinical characteristics and RAE outcome in 24 patients.
H.-J. Eom et al. / Clinical Radiology xxx (2015) e1ee8
(4%) developed AVF after biopsy in a transplanted kidney. AVM was located in the right kidney in 16 patients (72%) and upper pole, mid-pole, and lower pole in 9 (42%), 6 (32%), and 5 (26%) patients, respectively. The mean size of AVM nidus on renal angiography was 2.5 cm (rangeSD, 1e6.70.8).
Characteristics of RAE Four patients who developed AVF after biopsy or partial nephrectomy (17%) showed a single linear connecting vessel. Among remaining 20 patients (83%) without medical or clinical history to suggest acquired AVF, angiography demonstrated cirsoid AVM (90%, Figs 1e2) in 18 patients, cavernous AVM (5%) in one patient, and AVF with intranidal aneurysm (5%) in one patient. Among 31 procedures, the level of embolisation was feeder, segmental artery, and main renal artery in 28 (90%), 2 (6%), and 1 (4%) procedures, respectively. In patients in whom super-selection of the feeders failed, segmental renal
e5
arteries were embolised. Embolisation of main renal artery was performed with coils and NBCA in one patient whose AVM was located near the renal hilum and had too many feeding vessels arising from different segmental arteries, hindering the complete occlusion of nidus. Renal vein was temporarily occluded using a balloon (Fig 2) during embolisation in two patients, and a vascular plug was deployed in one patient in order to prevent pulmonary embolism. Coil, NBCA, and PVA were the most frequently chosen embolic materials and were used in 19 (%), 14 (%), and 8 (%) procedures, respectively. A single embolic material was used in 12 (39%) procedures in the order of coil, NBCA, PVA, ethanol, and vascular plug in 5 (42%), 4 (33%), 1 (8%), 1 (8%), and 1 (8%) procedures, respectively. Combinations of embolic materials comprised coil and NBCA and coil and particles including PVA or GSP, in 8 (26%) and 6 (19%) procedures, respectively. Other combinations, such as GSP and PVA, PVA and ethanol, NBCA and plug, or more than three combinations were used. NBCA was diluted with iodised oil (Lipiodol; Andre Guerbet, Aulnay-Sous-Bois, France) at a
Figure 2 A 30-year-old woman with massive haematuria (patient 7). (a) Coronal reconstructed CT image shows an abnormally enhancing, tangled vascular lesion (arrows) localised at the hilum of the right kidney. (b) Right renal artery angiogram shows an AVM with multiple arterial feeders with a corkscrew appearance. (c) An occlusion balloon catheter (arrows) was used in renal vein to prevent reflux of the embolic material into pulmonary circulation. (d) Chest radiograph obtained 2 hours after the procedure with NBCA shows scattered NBCA droplets in both lungs.
Please cite this article in press as: Eom H-J, et al., Transarterial embolisation of renal arteriovenous malformation: safety and efficacy in 24 patients with follow-up, Clinical Radiology (2015), http://dx.doi.org/10.1016/j.crad.2015.06.079
e6
H.-J. Eom et al. / Clinical Radiology xxx (2015) e1ee8
ratio between 1:2 and 1:4. Only particulate embolic materials were used in two patients who had small AVM in the early study period. The size of PVA particles used in the procedures was not unified ranging from 40e150 to 700e1000 mm.
Outcome of RAE Patient clinical courses are summarised in Fig 3. The clinical success rate after initial RAE was 67% (16/24). The median follow-up period was 381 days (range, 16e2118 days) in these patients. The overall clinical success rate, including multisession RAE, was 88 % (21/24). The median follow-up period was 447 days (range, 4e2486 days) in these patients. Among 8 patients with clinical failure after initial RAE, 6 underwent second session RAE and the other two underwent nephrectomy. After the second session of RAE, 4 achieved clinical success, one underwent third session RAE without recurrence on follow-up, and the other underwent radical nephrectomy due to recurrence. The technical success rate, based on a total of 31 procedures, was 65% (20/31). Among 11 procedures that technically failed in 10 patients, 4 patients achieved clinical success without additional RAE, 3 underwent second session RAE to achieve clinical success, and 3 patients underwent nephrectomy due to recurrence. Final angiogram after initial technical failure showed minimal residual fine feeder vessels without a definite residual shunt, which was a common finding in cases that achieved clinical success after initial technical failure. Even with the technical success, clinical failure was observed in two procedures in one patient. The median follow-up period for recurrence after the technical success and failure was 117 (range, 34e199) and 238 (range, 7e448) days, respectively. The causes of technical failure were too many fine feeding vessels arising from different segmental arteries in 11 (92%, 11/12) procedures and a high-flow shunt in 1 (8%, 1/12) procedure. Regarding the complications, pulmonary embolism, which was classified as a major complication, occurred in one patient (Fig 2), despite the effort to occlude the renal
Figure 3 Technical and clinical outcome of single and multiple sessions of RAE.
vein using a balloon catheter as a preventive measure. NBCA was used as an embolic material in this patient. During the infusion of NBCA, the patient developed dyspnoea and her blood oxygen saturation level dropped to 95%. Chest radiography revealed disseminated embolic material in both lungs; however, the patient’s blood oxygen saturation level immediately restored to 100% with 6 l nasal prong oxygen inhalation and no more than temporary oxygen inhalation was required. Post-treatment complaints were mild ipsilateral flank pain, mild fever, and nausea, which were all successfully managed conservatively. In all patients, except for a patient with a single kidney who underwent nephrectomy due to clinical failure, BUN/Cr levels were within the normal range before and after RAE. Among 21 patients with overall clinical success, 15 had available follow-up CT or ultrasound. Renal AVM was obliterated with atrophic change of the renal parenchyma or showed disappearance of the nidus and early draining veins (Fig 1). The other three patients who did not achieve overall clinical success all underwent nephrectomy.
Discussion Renal AVM is an uncommon cause of haematuria and is a diagnostic and therapeutic challenge in clinical practice. The present study revealed that single or multiple RAE sessions could be an effective and safe treatment strategy for patients with renal AVM. The technical success rate of 65% and the overall clinical success rate of 88% seem to be comparable to those reported in previous studies.1 Primary and secondary success rates were 73.7 and 94.7%, respectively, based on a review of 19 patients in 15 reports published in English and available in PubMed, regarding renal AVM embolisation performed from 1992 to 2012,1 although a direct comparison is difficult. Murata and colleagues14 reported 100% technical success and clinical success in their study of 14 treatment sessions in 12 patients; however, as their definition of technical success included not only complete but also an acceptable level of nidus occlusion and clinical success was defined as cessation of haematuria for 1 month, comparing their results with those of the present study is difficult. In the present study, technical failure was primarily due to multiple fine feeding vessels arising from different segmental arteries. It requires prolonged procedure time and there is a risk of excessive loss of functioning renal parenchymal. The operators chose not to embolise the main renal artery or multiple segmental arteries at the proximal level as it would result in a significant loss of functioning renal parenchyma, especially when they were located near the hilum. The results of this study reflect the difficulty of complete embolisation of multiple feeders while attempting to preserve renal parenchyma. Although the majority of patients with technical success achieved clinical success, it is interesting that there were some patients who met clinical success even after failing to embolise all the feeders. This could be due to occlusion of the bleeding foci among the numerous vascular tangles,
Please cite this article in press as: Eom H-J, et al., Transarterial embolisation of renal arteriovenous malformation: safety and efficacy in 24 patients with follow-up, Clinical Radiology (2015), http://dx.doi.org/10.1016/j.crad.2015.06.079
H.-J. Eom et al. / Clinical Radiology xxx (2015) e1ee8
even though the specific bleeding foci on angiography could not be predicted; however, complete AVM nidus occlusion seems to be essential in RAE, although recanalisation can occur despite complete occlusion of the nidus. It is suggested that RAE could be used as a temporary method to cease haematuria caused by renal AVM in emergency situations or when surgery cannot be performed. Multiple RAE sessions therefore could be required for the successful treatment of complicated renal AVMs.13,14 Almost all the patients had minor complications, including mild pain, nausea or fever for one or two days following the procedure. Among the patients with highflow shunts treated with NBCA, pulmonary embolism occurred in one patient, despite temporary renal vein occlusion using a balloon catheter. The risk of distal embolisation into the pulmonary circulation looms large in highflow AVFs and is increased by the high-flow velocity and flow-related ectasia of the fistulous tract along the venous end, preventing proper anchoring of the embolic materials.17 Various embolic materials have been used to occlude renal AVM. Some researchers have reported primary success using GSP or coils, although almost 50% of the previous reports have shown late, partial recanalisation through the development of collaterals.13,18 This can be explained by the fact that GSP is intended for temporary occlusion and allows recanalisation, and coils work only at the location at which they are deployed, they do not obliterate the nidus and allow development of collateral vessels.19 These are comparable with the result of the present study in that coils used as the sole embolic material resulted in AVM recurrence in two out of three cases; conversely, coils when used with a GSP resulted in AVM recurrence in one of two cases. Particle embolic materials, such as GSP or PVA, have a higher risk of pulmonary embolisation with high-flow shunts and are thus not recommended. NBCA diluted in Lipiodol conforms to the criteria of an instantaneous and effective embolic material that can be used to cure renal AVM, provided that NBCA can be delivered super-electively to the nidus.11,20 As seen in the present study, NBCA can be useful for obliterating the nidus or multiple fine feeding vessels in patients with a high-flow shunt; however, there is a risk of pulmonary embolism when shunt control is incomplete or the concentration of NBCA is inadequate at the time of the NBCA injection. In patients with haematuria, CT or ultrasound is usually performed in order to exclude disease entities such as tumours or vascular lesions. As the present study shows, in some cases there is no demonstrable lesion on CT or ultrasound to explain haematuria, and moreover, haematoma in the renal pelvis might be the only clue. Therefore, diagnostic renal angiography is recommended in patients with haematuria with no apparent cause on CT or ultrasound. Following RAE, renal parenchymal atrophy and disappearance of vascular lesions were observed on CT. These CT findings suggest successful treatment following RAE. In addition to the inherent limitations related to retrospective study design, the present study has several other limitations. First, a small number of study patients was
e7
enrolled; however, as this is a rare entity, the number is relatively large for a two-centre study. Second, the use of embolic materials was not randomised or controlled and was chosen at the operators’ discretion. Therefore, it is difficult to analyse the effect of embolic material on the outcome of RAE. Further research will be necessary to identify the optimal embolic material for renal AVM. Lastly, as six different interventional radiologists performed procedures, it is possible that their experience and technique differed. In conclusion, RAE is a safe and effective treatment of renal AVM. Technical failure of RAE does not always lead to clinical failure and multiple embolisation sessions may be effective treatment for recurred renal AVM.
Acknowledgments This research was supported by Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Science, ICT and future Planning (2014R1A2A2A01005857).
References 1. Zhang B, Jiang ZB, Huang MS, et al. The role of transarterial embolization in the management of hematuria secondary to congenital renal arteriovenous malformations. Urol Int 2013;91:285e90. 2. Tarif N, Mitwalli AH, Al Samayer SA, et al. Congenital renal arteriovenous malformation presenting as severe hypertension. Nephrol Dial Transplant 2002;17:291e4. 3. Crotty KL, Orihuela E, Warren MM. Recent advances in the diagnosis and treatment of renal arteriovenous malformations and fistulas. J Urol 1993;150:1355e9. 4. Takaha M, Matsumoto A, Ochi K, et al. Intrarenal arteriovenous malformation. J Urol 1980;124:315e8. 5. Yazaki T, Tomita M, Akimoto M, et al. Congenital renal arteriovenous fistula: case report, review of Japanese literature and description of nonradical treatment. J Urol 1976;116:415e8. 6. Tarkington MA, Matsumoto AH, Dejter SW, et al. Spectrum of renal vascular malformation. Urology 1991;38:297e300. 7. Seitz M, Waggershauser T, Khoder W. Congenital intrarenal arteriovenous malformation presenting with gross hematuria after endoscopic intervention: a case report. J Med Case Rep 2008;2:326. 8. Keller FS. Interventional radiology: new paradigms for the new millennium. J Vasc Interv Radiol 2000;11:677e81. 9. Defreyne L, Govaere F, Vanlangenhove P, et al. Cirsoid renal arteriovenous malformation treated by endovascular embolization with n-butyl 2-cyanoacrylate. Eur Radiol 2000;10:772e5. 10. Wetter A, Schlunz-Hendann M, Meila D, et al. Endovascular treatment of a renal arteriovenous malformation with Onyx. Cardiovasc Intervent Radiol 2012;35:211e4. 11. Beaujeux R, Saussine C, al-Fakir A, et al. Superselective endo-vascular treatment of renal vascular lesions. J Urol 1995;153:14e7. 12. Wikholm G, Svendsen P, Herlitz H, et al. Superselective transarterial embolization of renal arteriovenous malformations of cryptogenic origin. Scand J Urol Nephrol 1994;28:29e33. 13. Takebayashi S, Hosaka M, Kubota Y, et al. Transarterial embolization and ablation of renal arteriovenous malformations: efficacy and damages in 30 patients with long-term followup. J Urol 1998;159: 696e701. 14. Murata S, Onozawa S, Nakazawa K, et al. Endovascular embolization strategy for renal arteriovenous malformations. Acta Radiol 2014;55:71e7. 15. Schwartz MJ, Smith EB, Trost DW, et al. Renal artery embolization: clinical indications and experience from over 100 cases. BJU Int 2007;99:881e6.
Please cite this article in press as: Eom H-J, et al., Transarterial embolisation of renal arteriovenous malformation: safety and efficacy in 24 patients with follow-up, Clinical Radiology (2015), http://dx.doi.org/10.1016/j.crad.2015.06.079
e8
H.-J. Eom et al. / Clinical Radiology xxx (2015) e1ee8
16. Sacks D, McClenny TE, Cardella JF, et al. Society of Interventional Radiology clinical practice guidelines. J Vasc Interv Radiol 2003;14:S199e202. 17. Sundarakumar DK, Kroma GM, Smith CM, et al. Embolization of a large high-flow renal arteriovenous fistula using 03500 and 01800 detachable coils. Indian J Radiol Imaging 2013;23:151e4. 18. Nakamura H, Uchida H, Kuroda C, et al. Renal arteriovenous malformations: transcatheter embolization and follow-up. AJR Am J Roentgenol 1981;137:113e6.
19. Brown DB, Brandes SB. Radiofrequency ablation of a recanalized renal arteriovenous malformation. J Vasc Interv Radiol 2005;16:403e6. 20. Nurmi M, Satokari K, Puntala P, et al. Intra-arterial embolic occlusion of a bleeding intrarenal arteriovenous malformation: a case report. Scand J Urol Nephrol 1983;17:257e9.
Please cite this article in press as: Eom H-J, et al., Transarterial embolisation of renal arteriovenous malformation: safety and efficacy in 24 patients with follow-up, Clinical Radiology (2015), http://dx.doi.org/10.1016/j.crad.2015.06.079
Contents lists available at ScienceDirect
Clinical Radiology journal homepage: www.clinicalradiologyonline.net
Transarterial embolisation of renal arteriovenous malformation: safety and efficacy in 24 patients with follow-up H.-J. Eom a, J.H. Shin a, *, Y.J. Cho b, D.H. Nam c, G.-Y. Ko a, H.-K. Yoon a a
Department of Radiology and Research Institute of Radiology, Asan Medical Center, University of Ulsan College of Medicine, Seoul, South Korea b Department of Radiology, Busan Paik Hospital, Inje University College of Medicine, Busan, South Korea c Department of Radiology, Kyung Hee University Hospital at Gangdong, School of Medicine, Kyung Hee University, Seoul, South Korea
art icl e i nformat ion Article history: Received 29 January 2015 Received in revised form 6 May 2015 Accepted 5 June 2015
AIM: To evaluate the efficacy and safety of renal artery embolisation (RAE) for renal arteriovenous malformation (AVM) as well as its outcomes. MATERIALS AND METHODS: The technical and clinical success rates, radiological and laboratory findings, and complications of RAE for 31 renal AVMs in 24 patients (M:F¼9:15, mean age 46 years) at two separate medical institutions were retrospectively evaluated. Technical success was defined as complete occlusion of feeding arteries with no residual nidus seen on post-treatment angiography. Clinical failure was defined as recurrence of haematuria, presence of AVM on follow-up ultrasound or computed tomography, repeated RAE or surgery for the control of haematuria. Overall clinical success was defined as resolution haematuria or disappearance of AVM on follow-up imaging after single or multiple sessions of RAE. RESULTS: Types of renal AVM were AVM, arterio-venous fistula (AVF) with intranidal aneurysm, and acquired AVF in 19, 1, and 4 patients, respectively. 18 patients (75%) underwent a single session of RAE, while 6 patients (25%) had two or more sessions of RAE. The level of embolisation was feeder, segmental artery, and main renal artery in 28 (90%), 2 (6%), and 1 (4%) procedures, respectively. Coil, n-butyl 2-cyanoacrylate, and polyvinyl alcohol were the most frequently chosen embolic materials and were used in 19, 14, and 8 procedures, respectively. The clinical success rate after initial RAE was 67% (16/24). Overall clinical success rate, including multisession RAE, was 88% (21/24). The technical success rate of 31 procedures was 65% (20/31). Among 11 technical failures in 10 patients, 4 achieved clinical success without additional RAE, 3 underwent second session RAE to achieve clinical success, and 3 patients underwent nephrectomy due to recurrence. CONCLUSION: RAE is a safe and effective treatment for renal AVM. Technical failure of RAE does not always lead to clinical failure and multiple embolisation sessions may be effective for recurrent renal AVM. Ó 2015 The Royal College of Radiologists. Published by Elsevier Ltd. All rights reserved.
* Guarantor and correspondent: J.H. Shin, Department of Radiology and Research Institute of Radiology, Asan Medical Center, University of Ulsan College of Medicine, Asanbyeongwon-gil 86, Seoul, 138-736, South Korea. Tel.: þ82 2 3010 4380; fax: þ82 2 476 0090. E-mail address: [email protected] (J.H. Shin). http://dx.doi.org/10.1016/j.crad.2015.06.079 0009-9260/Ó 2015 The Royal College of Radiologists. Published by Elsevier Ltd. All rights reserved.
Please cite this article in press as: Eom H-J, et al., Transarterial embolisation of renal arteriovenous malformation: safety and efficacy in 24 patients with follow-up, Clinical Radiology (2015), http://dx.doi.org/10.1016/j.crad.2015.06.079
e2
H.-J. Eom et al. / Clinical Radiology xxx (2015) e1ee8
Introduction Renal arteriovenous malformation (AVM) is a pathological communication between the arterial and venous circulation that bypasses capillary bed. AVM could be either congenital or acquired.1 Acquired AVM, arterio-venous fistula (AVF), tend to manifest as a single linear connecting vessel, comprise 70e80% of renal arteriovenous abnormalities and usually result from trauma, biopsy, surgery, malignancy, or inflammation.2 Two types of congenital renal AVM, cirsoid and cavernous type, are described. Cirsoid AVM should fulfil certain criteria, which includes no prior history of renal injury or disease and typical angiographic findings with tortuous vascular channels between segmental or interlobar renal arteries and veins.3 Cavernous AVM shows a single dilated vessels and is less common.4 Patients with renal AVM usually present with gross haematuria or flank pain with occasional accompanying hypertension or heart failure.3,5,6 Renal angiography is used to confirm the presence of renal AVM and in planning treatment. To date, renal AVM has been treated by surgery, such as nephrectomy. Endovascular approaches for treating AVM are gaining popularity.7 The introduction of smaller delivery catheters and more precise delivery of embolic materials have drastically reduced the morbidity associated with this technique.1,8e12 Therefore, currently, this treatment modality is becoming popular as it provides maximal preservation of functioning renal parenchyma as well as treating the disease and symptoms. Several case reports and case series of renal artery embolisation (RAE) and ablation of renal AVM have reported successful results1,13e15; however, there are few studies regarding the comprehensive analysis of clinical and radiological outcomes and effectiveness of multiple RAE sessions based on long-term follow-up data. The present study was undertaken to evaluate the efficacy and safety of RAE for renal AVM as well as its long-term outcomes.
Material and methods Patients From January 2001 to December 2014, 31 RAE procedures were performed for 24 renal AVMs in 24 patients at two, separate medical institutions. A total of 24 patients, i.e., 9 men (age range, 16e71 years; mean age 43 years) and 15 women (age range, 30e69 years; mean age 47 years) were included in this study. Clinical medical records were retrospectively reviewed for symptoms and signs of renal AVM, underlying medical status and baseline renal function, i.e., blood urea nitrogen/ creatinine (BUN/Cr). Imaging studies obtained before and after RAE, including computed tomography (CT) and ultrasound images, were reviewed. Angiographic findings, diameter of the renal AVM, embolisation level and embolic materials used were analysed by reviewing the medical
charts and angiography images. The longest diameter of the AVM nidus was measured from the angiographic images. Technical and clinical outcomes of RAE were assessed. The study was approved by the local ethics committee, and informed consent for data use was waived due to retrospective study design. Informed consent for the procedure was obtained from all patients before the procedure.
Embolisation technique Transcatheter RAE was performed by six, board-certified radiologists with 5e26 years of clinical experience in endovascular therapy. The right common femoral artery was routinely accessed and after selecting the right or left renal artery using a 0.035-inch hydrophilic guidewire (Radifocus; Terumo, Tokyo, Japan) and a standard 5-F catheter, renal arteriography was performed. Target vessels for embolisation were determined using digital subtraction angiography by identifying abnormal feeding arteries to the nidus. A microcatheter (Renegade, Boston Scientific, Cork, Ireland, or Microferret, Cook, Bloomington, IN, USA) was advanced into all identifiable target vessels, which were subsequently embolised using various embolic materials. Selection of embolic material was made on a case-bycase basis according to the decision of interventional radiologist at the time of procedure. Embolic materials, including coils, particles including polyvinyl alcohol (PVA) and gelatin-sponge particles (GSP), liquid embolics including alcohol and n-butyl 2-cyanoacrylate (NBCA), and vascular plugs, were used. In all patients, final arteriogram was performed to confirm successful occlusion of target vessels.
Definitions and study endpoints Clinical failure was defined as recurrence of haematuria, presence of AVM on follow-up ultrasound or CT, repeated RAE or surgery for the control of haematuria. Overall clinical success was defined as resolution of haematuria or disappearance of AVM on follow-up imaging after single or multiple sessions of RAE. Clinical outcome was assessed by reviewing the medical records and radiological examinations performed after RAE and by identifying any complications attributable to RAE. Technical success was defined as complete occlusion of fine feeding arteries, and thus, no residual AVM nidus or draining veins seen on immediate post-treatment angiography. Complication was classified as major or minor according to the guidelines of the Society of Interventional Radiology Standards of Practice Committee.16 Major complication included major therapy, an unexpected increase in the level of care or prolonged hospitalisation (>48 hours), permanent adverse sequelae or death. Minor complication included minor therapy such as overnight admission for observation only.
Please cite this article in press as: Eom H-J, et al., Transarterial embolisation of renal arteriovenous malformation: safety and efficacy in 24 patients with follow-up, Clinical Radiology (2015), http://dx.doi.org/10.1016/j.crad.2015.06.079
H.-J. Eom et al. / Clinical Radiology xxx (2015) e1ee8
e3
Figure 1 A 55-year-old woman with haematuria (patient 5). (a) Left renal artery angiogram shows AVM (arrow) with multiple, fine feeding vessels (arrowheads) arising from different segmental arteries. (b) Left renal artery angiogram obtained after coil embolisation shows residual opacification of the fine feeding vessels (arrows; technical failure); however, the haematuria resolved during the procedure. (c) Left renal artery angiogram obtained 1 month after the initial embolisation shows recanalisation of the feeders (arrows). The patient had recurrence of haematuria. (d) Several branches were embolised with NBCA and GSP. The final angiogram shows complete occlusion of the AVM nidus and no visible draining veins. (e) Coronal reconstructed CT image obtained 5 years after embolisation shows mild renal parenchymal atrophy (arrows) with complete obliteration of the AVM nidus. The patient was symptom-free.
Results Patient characteristics Clinical characteristics and outcomes of the 24 patients and 31 procedures are summarised in Table 1. 18 patients (75%) underwent a single session of RAE, whereas 6 patients (25%) had two or more sessions of RAE. Therefore, a total of 31 RAE procedures were performed in 24 patients. 17 patients (71%) had haematuria or flank pain, and 7 (29%) were asymptomatic. One patient had a single kidney with a past medical history of nephrectomy for renal cell carcinoma. All patients underwent CT or ultrasound before angiography. Among 22 patients who underwent CT, 16 patients
(72%) were given the correct diagnosis, 5 (23%) showed haematoma in renal pelvis and hydronephrosis, and in one patient (5%) AVM was diagnosed as an aneurysm. Among 10 patients who underwent ultrasound, 7 (70%) received the correct diagnosis, two (20%) failed to detect any abnormality, and in one patient (10%) AVM was diagnosed as an aneurysm. AVM diagnosed as an aneurysm was found to have an intranidal aneurysm on renal angiogram. Diagnostic renal angiography was performed after excluding other causes of haematuria, such as urinary tract infection or tumorous condition in the urinary bladder by performing laboratory tests or cystoscopy. Three patients (13%) developed AVF after partial nephrectomy for RCC at the resection margin and one patient
Please cite this article in press as: Eom H-J, et al., Transarterial embolisation of renal arteriovenous malformation: safety and efficacy in 24 patients with follow-up, Clinical Radiology (2015), http://dx.doi.org/10.1016/j.crad.2015.06.079
e4
Patient no./age/sex
1/44/F 2/61/F 3/42/F 4/67/F 5/55/F 6/50/M 7/30/F 8/38/M 9/16/M 10/24/M 11/53/M 12/48/F 13/41/F 14/34/F 15/39/F 16/49/F 17/28/M 18/51/M 19/59/F 20/71/M 21/36/F 22/34/F 23/69/F 24/55/M
Type
AVM AVM AVM AVM AVM AVM AVM AVM AVM AVM AVM AVM AVM AVM AVM AVM AVM AVF AVF AVF AVF AVM AVM AVF
Nidus (cm)
2.1 2.6 2.2 3.8 2.7 6.7 3.5 2.5 2.6 1.5 1.3 2.2 3 1 1.5 1 1.5 e e e e 2.3 3.5 e
Embolic materialsa
Coil/CoilþGSP/CoilþGSP CoilþPVA/NBCA CoilþPVA CoilþPVA Coil/NBCAþGSP CoilþNBCAþplug NBCA CoilþPVA/Coilþethanol PVAþGSP PVA Coil PVAþethanol/CoilþNBCA CoilþNBCAþethanol/NBCA NBCA Ethanol NBCA CoilþNBCA CoilþNBCA Coil PVAþNBCA NBCAþplug CoilþNBCA Coil Plug
Outcome Technical successa
Clinical successb
Y/Y/Y N/Y N N N/Y Y N Y/Y Y Y Y N/Y N/N Y Y Y N Y Y N Y Y N Y
Y Y Y Y Y Y N, nephrectomy Y Y Y Y Y N, nephrectomy Y Y Y Y Y Y N, nephrectomy Y Y Y Y
Follow-up (days)a
Remarks
34/199/566 573/1167 267 1455 2486 187 e 7/14 2118 16 1318 559/4 448/e 1855 564 97 315 795 301 e 276 104 447 1653
e Main renal artery embolisation in second RAE e e e e Renal vein balloon occlusion, pulmonary embolism e e e e e Nephrectomy e e Renal vein balloon occlusion, percutaneous NBCA e Biopsy site, transplanted kidney Nephrectomy site Nephrectomy site, unilateral kidney Intranidal aneurysm, renal vein plug occlusion e e Nephrectomy site
AVM, arteriovenous malformation; AVF, arteriovenous fistula; GSP, gelatin sponge particle; NBCA, n-butyl 2-cyanoacrylate; PVA, polyvinyl alcohol; ø, diameter. a The content of each embolisation session is separately displayed by using slash in cases of multiple RAE sessions. b Overall clinical success is displayed.
H.-J. Eom et al. / Clinical Radiology xxx (2015) e1ee8
Please cite this article in press as: Eom H-J, et al., Transarterial embolisation of renal arteriovenous malformation: safety and efficacy in 24 patients with follow-up, Clinical Radiology (2015), http://dx.doi.org/10.1016/j.crad.2015.06.079
Table 1 Clinical characteristics and RAE outcome in 24 patients.
H.-J. Eom et al. / Clinical Radiology xxx (2015) e1ee8
(4%) developed AVF after biopsy in a transplanted kidney. AVM was located in the right kidney in 16 patients (72%) and upper pole, mid-pole, and lower pole in 9 (42%), 6 (32%), and 5 (26%) patients, respectively. The mean size of AVM nidus on renal angiography was 2.5 cm (rangeSD, 1e6.70.8).
Characteristics of RAE Four patients who developed AVF after biopsy or partial nephrectomy (17%) showed a single linear connecting vessel. Among remaining 20 patients (83%) without medical or clinical history to suggest acquired AVF, angiography demonstrated cirsoid AVM (90%, Figs 1e2) in 18 patients, cavernous AVM (5%) in one patient, and AVF with intranidal aneurysm (5%) in one patient. Among 31 procedures, the level of embolisation was feeder, segmental artery, and main renal artery in 28 (90%), 2 (6%), and 1 (4%) procedures, respectively. In patients in whom super-selection of the feeders failed, segmental renal
e5
arteries were embolised. Embolisation of main renal artery was performed with coils and NBCA in one patient whose AVM was located near the renal hilum and had too many feeding vessels arising from different segmental arteries, hindering the complete occlusion of nidus. Renal vein was temporarily occluded using a balloon (Fig 2) during embolisation in two patients, and a vascular plug was deployed in one patient in order to prevent pulmonary embolism. Coil, NBCA, and PVA were the most frequently chosen embolic materials and were used in 19 (%), 14 (%), and 8 (%) procedures, respectively. A single embolic material was used in 12 (39%) procedures in the order of coil, NBCA, PVA, ethanol, and vascular plug in 5 (42%), 4 (33%), 1 (8%), 1 (8%), and 1 (8%) procedures, respectively. Combinations of embolic materials comprised coil and NBCA and coil and particles including PVA or GSP, in 8 (26%) and 6 (19%) procedures, respectively. Other combinations, such as GSP and PVA, PVA and ethanol, NBCA and plug, or more than three combinations were used. NBCA was diluted with iodised oil (Lipiodol; Andre Guerbet, Aulnay-Sous-Bois, France) at a
Figure 2 A 30-year-old woman with massive haematuria (patient 7). (a) Coronal reconstructed CT image shows an abnormally enhancing, tangled vascular lesion (arrows) localised at the hilum of the right kidney. (b) Right renal artery angiogram shows an AVM with multiple arterial feeders with a corkscrew appearance. (c) An occlusion balloon catheter (arrows) was used in renal vein to prevent reflux of the embolic material into pulmonary circulation. (d) Chest radiograph obtained 2 hours after the procedure with NBCA shows scattered NBCA droplets in both lungs.
Please cite this article in press as: Eom H-J, et al., Transarterial embolisation of renal arteriovenous malformation: safety and efficacy in 24 patients with follow-up, Clinical Radiology (2015), http://dx.doi.org/10.1016/j.crad.2015.06.079
e6
H.-J. Eom et al. / Clinical Radiology xxx (2015) e1ee8
ratio between 1:2 and 1:4. Only particulate embolic materials were used in two patients who had small AVM in the early study period. The size of PVA particles used in the procedures was not unified ranging from 40e150 to 700e1000 mm.
Outcome of RAE Patient clinical courses are summarised in Fig 3. The clinical success rate after initial RAE was 67% (16/24). The median follow-up period was 381 days (range, 16e2118 days) in these patients. The overall clinical success rate, including multisession RAE, was 88 % (21/24). The median follow-up period was 447 days (range, 4e2486 days) in these patients. Among 8 patients with clinical failure after initial RAE, 6 underwent second session RAE and the other two underwent nephrectomy. After the second session of RAE, 4 achieved clinical success, one underwent third session RAE without recurrence on follow-up, and the other underwent radical nephrectomy due to recurrence. The technical success rate, based on a total of 31 procedures, was 65% (20/31). Among 11 procedures that technically failed in 10 patients, 4 patients achieved clinical success without additional RAE, 3 underwent second session RAE to achieve clinical success, and 3 patients underwent nephrectomy due to recurrence. Final angiogram after initial technical failure showed minimal residual fine feeder vessels without a definite residual shunt, which was a common finding in cases that achieved clinical success after initial technical failure. Even with the technical success, clinical failure was observed in two procedures in one patient. The median follow-up period for recurrence after the technical success and failure was 117 (range, 34e199) and 238 (range, 7e448) days, respectively. The causes of technical failure were too many fine feeding vessels arising from different segmental arteries in 11 (92%, 11/12) procedures and a high-flow shunt in 1 (8%, 1/12) procedure. Regarding the complications, pulmonary embolism, which was classified as a major complication, occurred in one patient (Fig 2), despite the effort to occlude the renal
Figure 3 Technical and clinical outcome of single and multiple sessions of RAE.
vein using a balloon catheter as a preventive measure. NBCA was used as an embolic material in this patient. During the infusion of NBCA, the patient developed dyspnoea and her blood oxygen saturation level dropped to 95%. Chest radiography revealed disseminated embolic material in both lungs; however, the patient’s blood oxygen saturation level immediately restored to 100% with 6 l nasal prong oxygen inhalation and no more than temporary oxygen inhalation was required. Post-treatment complaints were mild ipsilateral flank pain, mild fever, and nausea, which were all successfully managed conservatively. In all patients, except for a patient with a single kidney who underwent nephrectomy due to clinical failure, BUN/Cr levels were within the normal range before and after RAE. Among 21 patients with overall clinical success, 15 had available follow-up CT or ultrasound. Renal AVM was obliterated with atrophic change of the renal parenchyma or showed disappearance of the nidus and early draining veins (Fig 1). The other three patients who did not achieve overall clinical success all underwent nephrectomy.
Discussion Renal AVM is an uncommon cause of haematuria and is a diagnostic and therapeutic challenge in clinical practice. The present study revealed that single or multiple RAE sessions could be an effective and safe treatment strategy for patients with renal AVM. The technical success rate of 65% and the overall clinical success rate of 88% seem to be comparable to those reported in previous studies.1 Primary and secondary success rates were 73.7 and 94.7%, respectively, based on a review of 19 patients in 15 reports published in English and available in PubMed, regarding renal AVM embolisation performed from 1992 to 2012,1 although a direct comparison is difficult. Murata and colleagues14 reported 100% technical success and clinical success in their study of 14 treatment sessions in 12 patients; however, as their definition of technical success included not only complete but also an acceptable level of nidus occlusion and clinical success was defined as cessation of haematuria for 1 month, comparing their results with those of the present study is difficult. In the present study, technical failure was primarily due to multiple fine feeding vessels arising from different segmental arteries. It requires prolonged procedure time and there is a risk of excessive loss of functioning renal parenchymal. The operators chose not to embolise the main renal artery or multiple segmental arteries at the proximal level as it would result in a significant loss of functioning renal parenchyma, especially when they were located near the hilum. The results of this study reflect the difficulty of complete embolisation of multiple feeders while attempting to preserve renal parenchyma. Although the majority of patients with technical success achieved clinical success, it is interesting that there were some patients who met clinical success even after failing to embolise all the feeders. This could be due to occlusion of the bleeding foci among the numerous vascular tangles,
Please cite this article in press as: Eom H-J, et al., Transarterial embolisation of renal arteriovenous malformation: safety and efficacy in 24 patients with follow-up, Clinical Radiology (2015), http://dx.doi.org/10.1016/j.crad.2015.06.079
H.-J. Eom et al. / Clinical Radiology xxx (2015) e1ee8
even though the specific bleeding foci on angiography could not be predicted; however, complete AVM nidus occlusion seems to be essential in RAE, although recanalisation can occur despite complete occlusion of the nidus. It is suggested that RAE could be used as a temporary method to cease haematuria caused by renal AVM in emergency situations or when surgery cannot be performed. Multiple RAE sessions therefore could be required for the successful treatment of complicated renal AVMs.13,14 Almost all the patients had minor complications, including mild pain, nausea or fever for one or two days following the procedure. Among the patients with highflow shunts treated with NBCA, pulmonary embolism occurred in one patient, despite temporary renal vein occlusion using a balloon catheter. The risk of distal embolisation into the pulmonary circulation looms large in highflow AVFs and is increased by the high-flow velocity and flow-related ectasia of the fistulous tract along the venous end, preventing proper anchoring of the embolic materials.17 Various embolic materials have been used to occlude renal AVM. Some researchers have reported primary success using GSP or coils, although almost 50% of the previous reports have shown late, partial recanalisation through the development of collaterals.13,18 This can be explained by the fact that GSP is intended for temporary occlusion and allows recanalisation, and coils work only at the location at which they are deployed, they do not obliterate the nidus and allow development of collateral vessels.19 These are comparable with the result of the present study in that coils used as the sole embolic material resulted in AVM recurrence in two out of three cases; conversely, coils when used with a GSP resulted in AVM recurrence in one of two cases. Particle embolic materials, such as GSP or PVA, have a higher risk of pulmonary embolisation with high-flow shunts and are thus not recommended. NBCA diluted in Lipiodol conforms to the criteria of an instantaneous and effective embolic material that can be used to cure renal AVM, provided that NBCA can be delivered super-electively to the nidus.11,20 As seen in the present study, NBCA can be useful for obliterating the nidus or multiple fine feeding vessels in patients with a high-flow shunt; however, there is a risk of pulmonary embolism when shunt control is incomplete or the concentration of NBCA is inadequate at the time of the NBCA injection. In patients with haematuria, CT or ultrasound is usually performed in order to exclude disease entities such as tumours or vascular lesions. As the present study shows, in some cases there is no demonstrable lesion on CT or ultrasound to explain haematuria, and moreover, haematoma in the renal pelvis might be the only clue. Therefore, diagnostic renal angiography is recommended in patients with haematuria with no apparent cause on CT or ultrasound. Following RAE, renal parenchymal atrophy and disappearance of vascular lesions were observed on CT. These CT findings suggest successful treatment following RAE. In addition to the inherent limitations related to retrospective study design, the present study has several other limitations. First, a small number of study patients was
e7
enrolled; however, as this is a rare entity, the number is relatively large for a two-centre study. Second, the use of embolic materials was not randomised or controlled and was chosen at the operators’ discretion. Therefore, it is difficult to analyse the effect of embolic material on the outcome of RAE. Further research will be necessary to identify the optimal embolic material for renal AVM. Lastly, as six different interventional radiologists performed procedures, it is possible that their experience and technique differed. In conclusion, RAE is a safe and effective treatment of renal AVM. Technical failure of RAE does not always lead to clinical failure and multiple embolisation sessions may be effective treatment for recurred renal AVM.
Acknowledgments This research was supported by Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Science, ICT and future Planning (2014R1A2A2A01005857).
References 1. Zhang B, Jiang ZB, Huang MS, et al. The role of transarterial embolization in the management of hematuria secondary to congenital renal arteriovenous malformations. Urol Int 2013;91:285e90. 2. Tarif N, Mitwalli AH, Al Samayer SA, et al. Congenital renal arteriovenous malformation presenting as severe hypertension. Nephrol Dial Transplant 2002;17:291e4. 3. Crotty KL, Orihuela E, Warren MM. Recent advances in the diagnosis and treatment of renal arteriovenous malformations and fistulas. J Urol 1993;150:1355e9. 4. Takaha M, Matsumoto A, Ochi K, et al. Intrarenal arteriovenous malformation. J Urol 1980;124:315e8. 5. Yazaki T, Tomita M, Akimoto M, et al. Congenital renal arteriovenous fistula: case report, review of Japanese literature and description of nonradical treatment. J Urol 1976;116:415e8. 6. Tarkington MA, Matsumoto AH, Dejter SW, et al. Spectrum of renal vascular malformation. Urology 1991;38:297e300. 7. Seitz M, Waggershauser T, Khoder W. Congenital intrarenal arteriovenous malformation presenting with gross hematuria after endoscopic intervention: a case report. J Med Case Rep 2008;2:326. 8. Keller FS. Interventional radiology: new paradigms for the new millennium. J Vasc Interv Radiol 2000;11:677e81. 9. Defreyne L, Govaere F, Vanlangenhove P, et al. Cirsoid renal arteriovenous malformation treated by endovascular embolization with n-butyl 2-cyanoacrylate. Eur Radiol 2000;10:772e5. 10. Wetter A, Schlunz-Hendann M, Meila D, et al. Endovascular treatment of a renal arteriovenous malformation with Onyx. Cardiovasc Intervent Radiol 2012;35:211e4. 11. Beaujeux R, Saussine C, al-Fakir A, et al. Superselective endo-vascular treatment of renal vascular lesions. J Urol 1995;153:14e7. 12. Wikholm G, Svendsen P, Herlitz H, et al. Superselective transarterial embolization of renal arteriovenous malformations of cryptogenic origin. Scand J Urol Nephrol 1994;28:29e33. 13. Takebayashi S, Hosaka M, Kubota Y, et al. Transarterial embolization and ablation of renal arteriovenous malformations: efficacy and damages in 30 patients with long-term followup. J Urol 1998;159: 696e701. 14. Murata S, Onozawa S, Nakazawa K, et al. Endovascular embolization strategy for renal arteriovenous malformations. Acta Radiol 2014;55:71e7. 15. Schwartz MJ, Smith EB, Trost DW, et al. Renal artery embolization: clinical indications and experience from over 100 cases. BJU Int 2007;99:881e6.
Please cite this article in press as: Eom H-J, et al., Transarterial embolisation of renal arteriovenous malformation: safety and efficacy in 24 patients with follow-up, Clinical Radiology (2015), http://dx.doi.org/10.1016/j.crad.2015.06.079
e8
H.-J. Eom et al. / Clinical Radiology xxx (2015) e1ee8
16. Sacks D, McClenny TE, Cardella JF, et al. Society of Interventional Radiology clinical practice guidelines. J Vasc Interv Radiol 2003;14:S199e202. 17. Sundarakumar DK, Kroma GM, Smith CM, et al. Embolization of a large high-flow renal arteriovenous fistula using 03500 and 01800 detachable coils. Indian J Radiol Imaging 2013;23:151e4. 18. Nakamura H, Uchida H, Kuroda C, et al. Renal arteriovenous malformations: transcatheter embolization and follow-up. AJR Am J Roentgenol 1981;137:113e6.
19. Brown DB, Brandes SB. Radiofrequency ablation of a recanalized renal arteriovenous malformation. J Vasc Interv Radiol 2005;16:403e6. 20. Nurmi M, Satokari K, Puntala P, et al. Intra-arterial embolic occlusion of a bleeding intrarenal arteriovenous malformation: a case report. Scand J Urol Nephrol 1983;17:257e9.
Please cite this article in press as: Eom H-J, et al., Transarterial embolisation of renal arteriovenous malformation: safety and efficacy in 24 patients with follow-up, Clinical Radiology (2015), http://dx.doi.org/10.1016/j.crad.2015.06.079
