Elective and Emergency Renal Angiomyolipoma Embolization ... - JVIR

CLINICAL STUDY

Elective and Emergency Renal Angiomyolipoma Embolization with Ethylene Vinyl Alcohol Copolymer: Feasibility and Initial Experience Urbano, MD, PhD, Laura Paul, MD, Manuel Cabrera, MD, Jose mez, MD Alberto Alonso-Burgos, MD, PhD, and Daniella Go ABSTRACT Purpose: To report preliminary experience with angiomyolipoma (AML) transcatheter arterial embolization using ethylene vinyl alcohol (EVOH) copolymer liquid embolic agent. Materials and Methods: Embolization was performed in 22 consecutive patients (mean age, 53.5 y; 16 women and 6 men) for symptomatic AMLs or AMLs > 4 cm. Mean AML size before treatment was 7 cm (range, 3.5–13 cm). Superselective embolization of all lesions using microcatheters was performed; EVOH copolymer was the only embolic agent used. Data collected included volume of EVOH copolymer used, AML size before and after treatment, bleeding control, rebleeding, renal function, and complications. Results: Twenty-seven embolizations were performed for 25 AMLs. In 3 patients, embolization of 2 different AMLs was performed. A mean volume of 2.5 mL (range, 1–8 mL) of 6% EVOH copolymer was administered per lesion. Of embolizations, 17 (63%) were elective, and 10 (37%) were urgent. For urgent cases, primary and secondary bleeding control rates were 80% and 100%, respectively. Two urgent embolizations had early rebleeding from different previously treated vessels and a successful second embolization was performed. Mean follow-up time was 37.7 months (range, 5–124 months). Rate of postembolization syndrome was 18.5%. Mean size reduction of 45.7% ± 21.5 over the maximum length of the AML before treatment was achieved. No AML regrowth occurred during follow-up. Minor and major complication rates were 7.4% and 0%, respectively. No rebleeding and no renal function impairment occurred during follow-up. Conclusions: AML embolization with EVOH copolymer is feasible, safe, and effective. EVOH copolymer could be another embolic option for AML treatment.

ABBREVIATIONS AML ¼ angiomyolipoma, DMSO ¼ dimethyl sulfoxide, EVOH ¼ ethylene vinyl alcohol, GFR ¼ glomerular filtration rate, PES ¼ postembolization syndrome, TS ¼ tuberous sclerosis

Renal angiomyolipoma (AML) is an uncommon benign tumor that occurs randomly or in association with tuberous sclerosis (TS) (1). Owing to the presence of fat tissue, this type of lesion exhibits specific radiologic characteristics on

From Interventional Radiology, Department of Medicine, Autonomous Unin, n 11, Majadahonda, Madrid 28221, Spain. versity of Madrid, c/ Jalo Received September 18, 2016; final revision received January 15, 2017; accepted January 26, 2017. Address correspondence to J.U.; E-mail: [email protected] None of the authors have identified a conflict of interest. © SIR, 2017 J Vasc Interv Radiol 2017; 28:832–839 http://dx.doi.org/10.1016/j.jvir.2017.01.017

computed tomography (CT) and magnetic resonance (MR) imaging, allowing reliable, noninvasive diagnosis (2,3). Most AMLs are asymptomatic and detected incidentally. Their size remains stable, or they grow slowly over the course of years (4). However, AMLs can cause severe spontaneous retroperitoneal bleeding, hematuria, and flank pain. Tumor size > 4 cm, intratumoral aneurysms > 5 mm, and TS are strongly associated with hemorrhage (5–7). Radical or partial nephrectomy for AML treatment is associated with the risk for perioperative bleeding and loss of renal function; therefore, selective nephron-sparing transcatheter arterial embolization is currently the treatment of choice (3,8). Embolizations of AMLs have been performed with different materials, alone or in combination. Polyvinyl alcohol microparticles, microspheres, coils, microcoils,

Volume 28 ▪ Number 6 ▪ June ▪ 2017

gelatin sponge, and liquid agents such as ethanol or ethiodized oil (Lipiodol; Guerbet, Villepinte, France) have been successfully used (9–12). Each embolic material has specific benefits and drawbacks. Recurrence rates (10%–39%), complications (2.9%–19.5%), and need for repeat embolization (9.1%–56.3%) vary among different studies (3). Selflimiting postembolization syndrome (PES), which is characterized by fever, flank pain, and leukocytosis, is the most frequent complication of embolization and occurs in up to 36% of cases (9). Ethylene vinyl alcohol (EVOH) copolymer is a liquid embolic agent with specific physicochemical properties. Slow and controlled release, progressive solidification, nonadherence, cohesiveness, high vascular penetration, and weak inflammatory effects are some theoretical properties of this product. Its good radiopacity and ability to be injected under real-time subtracted fluoroscopy should prevent nontarget embolizations (13). EVOH copolymer has also demonstrated high hemostatic ability in acute bleeding during embolization (14). The purpose of this study was to report preliminary experience with EVOH copolymer in preventive and emergency AML embolizations.

MATERIALS AND METHODS Study Design This study was a retrospective observational review of patients with renal AMLs who underwent arterial embolization with EVOH copolymer (Onyx; Medtronic, Minneapolis, Minnesota) between May 2006 and April 2016 at a single academic university hospital. Approval from the institutional review board and informed consent from each patient were obtained. The criteria for embolization included AML size > 4 cm, AML size > 3 cm in patients receiving anticoagulant therapy, and symptomatic AML of any size. Both elective and emergency treatments were included in the study. The final decision for treating an AML with embolization was made in agreement with the urology department. Liquid EVOH copolymer was chosen as the sole embolic agent for all cases in an intention-to-treat model. Embolization was the first therapeutic option in all cases. The volume of EVOH copolymer used, AML size before and after treatment, bleeding control, rebleeding, renal function, and complications were collected during the embolization procedure and from electronic medical records.

Patients and Tumors Superselective AML embolization was performed in 22 consecutive patients (16 women and 6 men; mean age 53.5 y; range, 30–80 y). TS was previously diagnosed in 6 patients. A single AML was present in 13 patients, and 9 patients had multiple and bilateral lesions. The mean tumor size before embolization was 7 cm (range, 3.5–13 cm). Baseline characteristics of the patients and tumors are presented in Table 1. Active bleeding was reported when contrast-enhanced extravasation was confirmed on CT.

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Embolization Technique Reformations during CT evaluation involving maximumintensity projections were used in all cases to perform noninvasive angiography and to tailor the embolization procedure. General anesthesia or deep sedation was used according to the anesthesiologist’s criteria. Antibiotic prophylaxis and nonsteroidal antiinflammatory drugs were routinely administered. Glomerular filtration rate (GFR) was measured in all patients before embolization. Embolization was performed with the intention of achieving AML devascularization. The bleeding site or feeding arteries as well as the dysplastic vasculature was filled with EVOH copolymer. The main renal artery was catheterized with a 6-F guiding catheter, and selective kidney angiography was performed using the best oblique projection. A 0.021-inch or 0.017-inch inside diameter dimethyl sulfoxide (DMSO)–compatible microcatheter (Rebar-18, Rebar-14; Medtronic) or Progreat 2.0 (Terumo Europe NV, Leuven, Belgium) microcatheter was coaxially advanced over a 0.014-inch Transcend floppy 205-cm-long steerable tip micro–guide wire (Boston Scientific, Natick, Massachusetts) as deeply as possible into the AML vasculature. Microcatheter dead space was flushed with DMSO. A 6% EVOH copolymer formulation (Onyx 18) was then injected through the microcatheter under fluoroscopic control. After the microcatheter was withdrawn, final control angiography was performed. For every patient, the AML EVOH copolymer embolization technique consisted of advancing the microcatheter as distally as possible into the AML dysplastic vasculature. Initially, EVOH copolymer flowed in an anterograde manner, filling the peripheral portion of the AML. Thereafter, EVOH copolymer had backward flow around the microcatheter into the more proximal and central components of the AML. Technical success, clinical success, nontarget embolization, and major and minor complications were defined according to the quality improvement guidelines for percutaneous transcatheter embolization (15). All patients underwent clinical examination and GFR testing at 1, 3, 6, 12, and 24 months. AML size after embolization was evaluated with nonenhanced CT or gadolinium-enhanced MR imaging at 6, 12, and 24 months. Because a strong streak artifact caused by EVOH copolymer prevents contrast-enhanced CT analysis, reduction in AML size was considered treatment success during CT follow-up studies (Fig 1a, b). The decision to use CT or MR imaging was made by the diagnostic radiology service based on the patient’s age and radiologist’s preference. The longest axis before treatment of all AML cases was compared with the longest axis after treatment, measured at the same place, at 24 months or at the end of follow-up.

RESULTS There were 27 embolizations performed for 25 AMLs. A mean volume of 2.5 mL (range, 1–8 mL) of 6% EVOH

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Urbano et al ▪ JVIR

Table 1. Patient Baseline Characteristics Patient No.

TS

AML Size (mm)

1

Sex/Age (y) F/60

Asymptomatic, incidental finding

Clinical Presentation

No

52

Isolated/Multiple Isolated

2

M/40

Acute massive retroperitoneal bleeding

No

40

Isolated

3

F/37

Intermittent flank discomfort

No

55

Isolated

4

M/55


No

98

Isolated

5

F/76

Acute massive retroperitoneal bleeding

No

130

Isolated

6

F/80


No

50

Isolated

7

F/56

Flank pain

Yes

120

Multiple

8 9

M/43 M/42

Intermittent flank discomfort Flank pain

Yes No

100 70

Multiple Isolated

10

M/38

Flank pain

No

70

Multiple

11

M/47

Acute massive hematuria

Yes

100/70*

Multiple

12

F/59

Intermittent flank discomfort

No

47

Multiple

13

M/61


No

35

Isolated

14

F/51

Flank discomfort

No

90

Multiple

15

F/58


No

63

Isolated

16 17

F/68 F/33

Asymptomatic, incidental finding Acute massive retroperitoneal bleeding

Yes Yes

45/45* 100/50*

Multiple Multiple

18

F/66

Flank discomfort

Yes

50

Multiple

19

F/65


No

43

Isolated

20

F/30

Flank pain

No

52

Isolated

21

F/72


No

42

Isolated

22

F/49

Flank discomfort

No

45

Multiple

AML ¼ angiomyolipoma; F ¼ female; M ¼ male; TS ¼ tuberous sclerosis. * Two AMLs treated in the same patient.

copolymer was administered per lesion; 37% of the procedures were emergency treatments (10 embolizations) for acute hemorrhage, and 63% (17 embolizations) were elective prophylactic treatments. In 1 patient with bilateral asymptomatic AMLs, both lesions were treated during the same session. In another patient with bilateral AMLs that started as acute bleeding, embolization of the bleeding lesion was done first, and the contralateral AML was treated 3 months later. In 1 bleeding patient, diagnosis was delayed by 3 days because a ureteric stone was suspected. All cases of acute bleeding required blood transfusions. Two bleeding patients were administered anticoagulation treatment because of atrial fibrillation. The other 2 bleeding patients were young women (age 30 and 33 y) who were using hormonal hyperstimulation owing to in vitro fertilization treatments. One of these women was 10 weeks pregnant and underwent an elective abortion 2 weeks after embolization. Intralesional aneurysms and exophytic locations were found in all cases of bleeding. The features of AML embolization are presented in Table 2.

Outcome Embolization with EVOH copolymer could be performed in all cases with a technical success rate of 100% on completion angiography. In urgent cases, primary and secondary bleeding control rates were 80% and 100%, respectively.

The clinical success rate within 30 days of embolization for bleeding patients was 100%. Early rebleeding in 2 patients was managed with a successful second embolization. In both cases, the bleeds were from vessels that did not initially receive embolization. A patient with TS, end-stage renal disease, and bilateral large AMLs required 3 urgent embolizations. This patient experienced rebleeding from a 10-cm AML in the lower pole of the right kidney that had received embolization 15 days previously and another rebleeding episode 1 year later that was caused by an untreated 7-cm AML in the upper pole of the same kidney. Because of the complexity and peculiarities of this patient, no preventive embolization was performed, and only the symptomatic AMLs were treated. In 1 case, liquid EVOH copolymer could be observed slowly diffusing out of the dysplastic AML feeding artery into the draining veins (Fig 2a–c). In 3 cases, embolization of a second arterial feeder was done via retrograde filling from EVOH copolymer injection in a separate artery. This allowed for treatment of 2 distinct arteries via a single injection. The mean hospitalization times for elective and emergency embolizations were 1.5 days (range, 1–3 d) and 10.4 days (range, 3–17 d), respectively. Intense PES manifesting as a sharp pain that required intravenous analgesia and prolonged hospitalization occurred in 18.5% (5 procedures) of cases. In 4 of these patients, a mild fever 38.5 C was noted.


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Figure 1. Asymptomatic incidental finding in a 55-year-old man with a 9.8-cm AML in the right kidney. (a) Axial CT image obtained before embolization. An inhomogeneous exophytic renal mass with low-attenuation areas of intratumoral fat can be seen. (b) Nonenhanced CT control image obtained 32 months after embolization. A strong streak artifact prevented analysis of AML enhancement. A significant reduction in AML size is depicted.

Table 2. Features of AML Arterial Embolization with EVOH Copolymer Feature

Value

Patients

22

AMLs treated

25

AMLs with exophytic location

19

AMLs with central location

6

AMLs with intralesional aneurysms

13

Embolizations

27

Elective embolizations

18

Emergency embolizations in symptomatic patients

10

Patients with flank pain and retroperitoneal bleeding

10

Patients with gross hematuria

2

Patients receiving anticoagulant treatment

2

Female patients receiving hormonal hyperstimulation

2

Units of PRBC needed in bleeding patients

4.7 (2–10)*

Volume (mL) of EVOH copolymer used per lesion

2.5 (1–8)*

Note–Values are numbers unless otherwise indicated. AML ¼ angiomyolipoma; EVOH ¼ ethylene vinyl alcohol; PRBC ¼ packed red blood cells. * Mean (range).

Follow-up Patients were followed until September 2016 or until they died. One patient was lost to follow-up. The mean follow-up time of the remaining 21 patients was 36.7 months (range, 5–124 months). There was no tumor regrowth during the follow-up period. A mean size

reduction of 45.7% ± 21.5 over the maximum length of the AML before treatment was achieved (Fig 3a–d). For both emergency and elective embolizations, the long-term rebleeding rate was 0%. The minor complication rate was 7.4%. A patient with a 10-cm, acutely bleeding AML had a 5-cm collection of partial fat liquefaction that was incidentally found on imaging during 6-month follow-up (Fig 4a, b). Drainage was not necessary, and no further treatment was warranted because the patient’s physical examination results and laboratory values were unremarkable. In another patient, a small amount of EVOH copolymer refluxed into the normal renal arteries, causing an asymptomatic nontarget embolization. No major complication due to the embolization technique or EVOH copolymer occurred. Most importantly, GFRs after treatment demonstrated baseline renal function in all patients immediately and during follow-up. A patient with a GFR of 13 mL/min underwent kidney transplantation 25 months after embolization. Another patient with a GFR of 26 mL/min died 17 months after treatment as a result of a stroke; however, renal function was stable. There were no cases of conversion to open or laparoscopic nephrectomy. The 30-day mortality rate was 0%. A patient with cirrhosis died of liver failure 21 months after AML embolization. The remaining patients were alive at the end of the follow-up period.

DISCUSSION The present study shows the efficacy of the EVOH copolymer during selective arterial embolization for preventive and emergency treatment of AMLs. The 6% EVOH copolymer formulation (Onyx 18) was used for all patients



Figure 2. Images from a 51-year-old woman with a sporadic 9-cm exophytic AML. The patient reported flank discomfort, and embolization was planned. (a) Selective digital subtraction angiography of the right kidney revealing a vascular exophytic and bulky mass with dysplastic and aneurysmal vessels. (b) Completion angiography after superselective embolization with EVOH copolymer demonstrating AML devascularization and full preservation of the normal renal parenchyma. (c) Unsubtracted image after embolization showing EVOH copolymer distribution. Cast filling dysplastic and aneurysmal arteries (arrows) and cast of EVOH copolymer filling wide and smooth vessels corresponding to the venous drainage of the AML (asterisks).

because it was believed that it would penetrate deeper than higher viscosity formulations, promoting complete embolization (13,16). The procedure was demonstrated to be safe and to preserve renal function in all patients, with a major complication rate of 0% and a minor complication rate of 7.4%. The results were durable, with no rebleeding or tumor growth during long-term follow-up. There is no consensus in the literature regarding the choice of embolization agent for AML treatment, and there are no prospective and comparative studies to date to establish a strong recommendation (3,9). Embolization with EVOH copolymer has shown a high technical success rate similar to that of other embolic agents (17–20). There are few reports of AML embolization with Onyx in the literature, and based on the present study, EVOH copolymer could be included as a potential alternative embolic agent for AML treatment (21,22). Tumor regrowth after embolization has been associated with TS, patient age, and tumor size (23). Recurrence also depends on the technique and embolic agent used and

was 40% in some studies (3,24). Using particles or alcohol, low-fat content and large size were predictors of volume reduction, with no differences found between TS and sporadic AML (19). Rebleeding rates were also highly variable. Lenton et al (25) reported a 40% repeat embolization rate after acute treatment using particles. However, Ramon et al (17) did not note any hemorrhage during follow-up when using a mixture of ethanol and microparticles. EVOH copolymer showed a 0% rate of long-term rebleeding and tumor shrinkage in all patients during a mean follow-up time of 36.7 months. After urgent embolization in 2 cases, there was early rebleeding, but from a previously untreated vessel; therefore, a successful second embolization was performed. EVOH copolymer has a high hemostatic effect and works regardless of the coagulation status of the patient. EVOH copolymer is a very effective embolic agent for bleeding, not only for immediate control but also for the long-term prevention of rebleeding (14,26). Dysplastic aneurysmal vessels are frequently seen in AMLs and are the main cause of tumor rupture and active bleeding (5). Microcoils were


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Figure 3. Bilateral treated AMLs. Urgent embolization was performed in the left kidney, and an elective embolization was performed 3 months later in the right kidney. (a, b) Axial contrast-enhanced CT images obtained before treatment showing well-defined, lowattenuation masses that measured 5 cm in the right kidney and 8.1 cm in the left kidney. (b) High-attenuation fluid collection surrounding the left kidney due to spontaneous acute retroperitoneal bleeding (asterisks). (c, d) T1-weighted MR imaging with contrast enhancement 6 months after embolization on the right side and 9 months after embolization on the left side. Significant shrinkage of both tumors can be seen.

used when aneurysms were detected. A combination of microparticles for the distal vascular bed and coils for the occlusion of aneurysm and feeding vessels has been shown to be relatively effective in reducing retroperitoneal bleeding caused by a ruptured AML (5,7,19,20). EVOH copolymer can also be used for creating a proximal and distal occlusion using a sandwich technique or filling the aneurysm sack in a manner similar to the packing technique with coils (13,26). To achieve complete embolization of the distal vascular bed of the AML, microparticles and absolute alcohol are widely used. Microparticles are used when high flow is present, and alcohol is slowly infused when the flow is lower or through an occlusion balloon or mixed with ethiodized oil (9,11,20). EVOH copolymer can be used either with free flow or with blocked flow (13,14). Results using different embolic agents have shown no evidence regarding the superiority of any single agent in terms of AML volume reduction (3,9). Hocquelet et al (19) reported

a mean volume reduction of 72% after embolization with particles or alcohol. Sheth et al (23) reported values of 67.9% for sporadic AML and 47.7% for TS when using calibrated microspheres. In this study, the maximum length of the AML, not the volume, achieved a mean size reduction of 45.7% ± 21.5. Because of its properties, EVOH copolymer could be pushed forward to try to fill the distal vascular bed of the AML; in this way, it would have an effect similar to that of microparticles. In some cases, retrograde filling of an independent feeding artery was observed when the injection of EVOH copolymer was performed from a distant and different feeding artery. This phenomenon allows treatment of 2 tumoral pedicles with a single EVOH copolymer injection. In some cases, it was also observed that EVOH copolymer slowly diffused into the AML draining veins, achieving the most complete embolization. Arteriovenous fistulas may be present as part of the dysplastic and tortuous AML vasculature, mainly in



Figure 4. Incidental finding of an asymptomatic partial fat liquefaction after embolization of a 10-cm AML with acute bleeding that was discovered during 6 months of MR imaging evaluation. (a) Coronal T2-weighted gradient echo sequence demonstrating a 5.6-cm hyperintense collection occupying the caudal portion of the treated tumor. (b) Left kidney ultrasound of the same area.

large tumors. When using absolute alcohol or microparticles, severe respiratory complications have been reported in up to 2% of cases (12). EVOH copolymer creates a cohesive embolic cast that is gradually released in a controlled way; therefore, pulmonary migration should be less likely than with other liquid agents. Moreover, in contrast to microparticles or alcohol, EVOH copolymer is a radiopaque product that allows the operator to precisely monitor the embolization in real time. A common consequence of AML embolization is PES, with reported occurrence rates of 36%–80% (3,9). The preliminary data of EVOH copolymer embolization have shown a lower incidence rate of PES (18.5%). Minor complications comprised 7.4% of cases. Asymptomatic partial fat liquefaction was diagnosed by follow-up MR imaging, but no further treatment was required. Fat necrosis liquefaction after AML embolization requiring percutaneous drainage has been reported (19,21). In another patient, asymptomatic nontarget embolization occurred because EVOH copolymer refluxed into a normal arterial branch. Major complication rates after AML transarterial embolization ranged from 0% to 19% (11,12,17,19,27). In this cohort of patients, no major kidney infarction or renal function impairment was found during the follow-up period. No major complications, such as vascular injuries, retroperitoneal bleeding triggered by embolization, pleural effusion, or abscess formation, occurred. The mortality rate was 0%, and no patient needed nephrectomy during the follow-up period. Childbearing is a risk factor for AML rupture and acute bleeding (3,28). Two emergency embolizations were performed in young women. One of the women was 10 weeks pregnant, and the fetus survived the acute episode; however, a therapeutic abortion was performed later. These cases are challenging, and conservative management for ruptured AMLs during pregnancy may be considered in hemodynamically stable patients (29). EVOH copolymer has several important drawbacks. In general, it is an expensive embolic material, but its cost varies based on specific regional and national environments.

EVOH copolymer and DMSO cause a burning pain when injected into peripheral arteries; therefore, general anesthesia or deep sedation is required. In theory, severe arterial vasospasm related to DMSO can occur. It is technically mandatory to perform a very slow injection. EVOH copolymer can be delivered only through a microcatheter, which cannot be used later for infusing microcoils or microparticles. If different EVOH copolymer injections are needed, occasionally several microcatheters are also needed, which increases the cost of the procedure. Moreover, because of the streak artifact, CT density changes in AMLs treated with EVOH copolymer prevent intratumoral contrast enhancement. The main limitation of this study was its retrospective, single-center nature and its small sample size. The follow-up time was variable, and 1 patient was lost to follow-up. The population was also heterogeneous, with patients with TS and without TS and acute and elective treatments analyzed together. In conclusion, AML embolization with EVOH copolymer is feasible, safe, and effective. EVOH copolymer could be another embolic option for the treatment of AML that may be very effective in cases of acute bleeding. This study discusses some features of EVOH copolymer that seem to demonstrate certain potential advantages over other embolic agents used for AML treatment.

REFERENCES 1. Bissler JJ, Kingswood JC. Renal angiomyolipomata. Kidney Int 2004; 66: 924–934. 2. Jinzaki M, Silverman SG, Akita H, Nagashima Y, Mikami S, Oya M. Renal angiomyolipoma: a radiological classification and update on recent developments in diagnosis and management. Abdom Imaging 2014; 39: 588–604. 3. Flum AS, Hamoui N, Said MA, et al. Update on the diagnosis and management of renal angiomyolipoma. J Urol 2016; 195:834–846. 4. Bhatt JR, Richard PO, Kim NS, et al. Natural history of renal angiomyolipoma (AML): most patients with large AMLs >4cm can be offered active surveillance as an initial management strategy. Eur Urol 2016; 70:85–90. 5. Yamakado K, Tanaka N, Nakagawa T, Kobayashi S, Yanagawa M, Takeda K. Renal angiomyolipoma: relationships between tumor size, aneurysm formation, and rupture. Radiology 2002; 225:78–82.


6. Seyam RM, Bissada NK, Kattan SA, et al. Changing trends in presentation, diagnosis and management of renal angiomyolipoma: comparison of sporadic and tuberous sclerosis complex-associated forms. Urology 2008; 72:1077–1082. 7. Ouzaid I, Autorino R, Fatica R, et al. Active surveillance for renal angiomyolipoma: outcomes and factors predictive of delayed intervention. BJU Int 2014; 114:412–417. 8. Boorjian SA, Frank I, Inman B, et al. The role of partial nephrectomy for the management of sporadic renal angiomyolipoma. Urology 2007; 70: 1064–1068. 9. Murray TE, Doyle F, Lee M. Transarterial embolization of angiomyolipoma: a systematic review. J Urol 2015; 194:635–639. G, Camun ~ez F, Casco n E, Barbero MJ. 10. Urbano J, Echenagusía A, Simo Embolization of symptomatic renal angiomyolipomas. Radiología 1997; 39:171–175. 11. Bishay VL, Crino PB, Wein AJ, et al. Embolization of giant renal angiomyolipomas: technique and results. J Vasc Interv Radiol 2010; 21: 67–72. 12. Villalta JD, Sorensen MD, Durack JC, Kerlan RK, Stoller ML. Selective arterial embolization of angiomyolipomas: a comparison of smaller and larger embolic agents. J Urol 2011; 186:921–927. 13. Saeed Kilani M, Izaaryene J, Cohen F, et al. Ethylene vinyl alcohol copolymer (Onyx) in peripheral interventional radiology: indications, advantages and limitations. Diagn Interv Imaging 2015; 96:319–326. 14. Urbano J, Cabrera JM, Franco A, Alonso-Burgos A. Selective arterial embolization with ethylene-vinyl alcohol copolymer for control of massive lower gastrointestinal bleeding: feasibility and initial experience. J Vasc Interv Radiol 2014; 25:839–846. 15. Angle JF, Siddiqi NH, Wallace MJ, et al. Quality improvement guidelines for percutaneous transcatheter embolization: Society of Interventional Radiology Standards of Practice Committee. J Vasc Interv Radiol 2010; 21:1479–1486. 16. Guimaraes M, Wooster M. Onyx (ethylene-vinyl alcohol copolymer) in peripheral applications. Semin Intervent Radiol 2011; 28:350–356. 17. Ramon J, Rimon U, Garniek A, et al. Renal angiomyolipoma: long-term results following selective arterial embolization. Eur Urol 2009; 55: 1155–1161.

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18. Andersen PE, Thorlund MG, Wennevik GE, Pedersen RL, Lund L. Interventional treatment of renal angiomyolipoma: immediate results and clinical and radiological follow-up of 4.5 years. Acta Radiol Open 2015; 4: 2058460115592442. 19. Hocquelet A, Cornelis F, Le Bras Y, et al. Long-term results of preventive embolization of renal angiomyolipomas: evaluation of predictive factors of volume decrease. Eur Radiol 2014; 24:1785–1793. 20. Chatziioannou A, Gargas D, Malagari K, et al. Transcatheter arterial embolization as therapy of renal angiomyolipomas: the evolution in 15 years of experience. Eur J Radiol 2012; 81:2308–2312. 21. Raskin D, Dotan Z, Rimon U. Long-term recurrence of renal angiomyolipoma angiogenic component after ethylene vinyl alcohol copolymer embolization. J Vasc Interv Radiol 2015; 26:1904–1906. 22. Thulasidasan N, Sriskandakumar S, Ilyas S, Sabharwal T. Renal angiomyolipoma: mid- to long-term results following embolization with onyx. Cardiovasc Intervent Radiol 2016; 39:1759–1764. 23. Sheth RA, Feldman AS, Paul E, Thiele EA, Walker TG. Sporadic versus tuberous sclerosis complex-associated angiomyolipomas: predictors for long-term outcomes following transcatheter embolization. J Vasc Interv Radiol 2016; 27:1542–1549. 24. Kothary N, Soulen MC, Clark TW, et al. Renal angiomyolipoma: long-term results after arterial embolization. J Vasc Interv Radiol 2005; 16:45–50. 25. Lenton J, Kessel D, Watkinson AF. Embolization of renal angiomyolipoma: immediate complications and long-term outcomes. Clin Radiol 2008; 63:864–870. 26. Kolber MK, Shukla PA, Kumar A, Silberzweig JE. Ethylene vinyl alcohol copolymer (Onyx) embolization for acute hemorrhage: a systematic review of peripheral applications. J Vasc Interv Radiol 2015; 26:809–815. 27. Chan CK, Yu S, Yip S, Lee P. The efficacy, safety and durability of selective renal arterial embolization in treating symptomatic and asymptomatic renal angiomyolipoma. Urology 2011; 77:642–648. 28. Preece P, Mees B, Norris B, Christie M, Wagner T, Dundee P. Surgical management of haemorrhaging renal angiomyolipoma in pregnancy. Int J Surg Case Rep 2015; 7C:89–92. 29. Gyimadu AO, Kara O, Basaran D, Esinler I. Conservative management of a retroperitoneal hemorrhage following a ruptured renal angiomyolipoma in pregnancy. J Obstet Gynaecol Res 2011; 37:156–159.