Vascular andhttp://ves.sagepub.com/ Endovascular Surgery
Endovascular Treatment of Major Abdominal Arteriovenous Fistulas: A Systematic Review Ghassan Nakad, Ghassan AbiChedid and Raed Osman VASC ENDOVASCULAR SURG published online 26 June 2014 DOI: 10.1177/1538574414540485 The online version of this article can be found at: http://ves.sagepub.com/content/early/2014/06/25/1538574414540485
Published by: http://www.sagepublications.com
Additional services and information for Vascular and Endovascular Surgery can be found at: Email Alerts: http://ves.sagepub.com/cgi/alerts Subscriptions: http://ves.sagepub.com/subscriptions Reprints: http://www.sagepub.com/journalsReprints.nav Permissions: http://www.sagepub.com/journalsPermissions.nav Citations: http://ves.sagepub.com/content/early/2014/06/25/1538574414540485.refs.html
>> OnlineFirst Version of Record - Jun 26, 2014 What is This?
Downloaded from ves.sagepub.com at PENNSYLVANIA STATE UNIV on August 12, 2014
Article
Endovascular Treatment of Major Abdominal Arteriovenous Fistulas: A Systematic Review
Vascular and Endovascular Surgery 1-8 ª The Author(s) 2014 Reprints and permission: sagepub.com/journalsPermissions.nav DOI: 10.1177/1538574414540485 ves.sagepub.com
Ghassan Nakad1, Ghassan AbiChedid2, and Raed Osman2
Abstract Purpose: To review the different outcomes of the endovascular repair of major abdominal arteriovenous fistulas (AVFs). Methods: An online systematic review of the literature was undertaken to identify all reported cases of endovascular repair of major AVFs, covering 9 major databases as well as relevant journals up to September 2013. Our own case was included. The primary outcome was technical success and mortality, the secondary outcome was the rate of complications and the operators’ recommendations. Results: Forty-eight articles were reviewed totaling a number of 54 patients including our own. The most common fistula site was the aortocaval segment. Aortic stent grafts were used in 78% of patients. Technical success was 94%. Intraoperative mortality was 0% with a 90-day mortality of 10%, half of which were not related to the primary pathology. Of the successful procedures, 12% of patients had major complications. One died before reintervention. All others had uneventful recoveries; 21% had minor complications treated conservatively. The majority of authors were in favor of this treatment modality. Keywords aortocaval, endovascular, arteriovenous fistula, aneurysm, aortic graft
Introduction Major abdominal arteriovenous fistulas (AVFs) are defined as anomalous communications between the aorta, iliac or renal arteries, the inferior vena cava (IVC), and iliac or renal veins. The most common AVF is aortocaval fistula (ACF). This condition is rare, involving less than 1% of abdominal aortic aneurysms (AAAs). It can be either primary due to a disease of the aorta or secondary due to iatrogenic, malignant, or traumatic causes.1 This condition is rapidly fatal if not treated, and repair of the arteriovenous communications is mandatory for restitution of a normal hemodynamic status. Traditional treatment consists of open surgical repair. This is associated with high morbidity and mortality. Endovascular treatment modalities are emerging, promising a safer, more efficient approach. Several isolated case reports of successful endovascular treatment have been published. We had the opportunity to treat a patient with an inflammatory AAA complicated by an infrarenal ACF. He presented to our institution with symptoms and signs of global with right predominant heart failure. He had a recent history of aortitis and retroperitoneal fibrosis. An abdominal angiocomputed tomography scan revealed the ACF at the level of the distal descending aorta just before the iliac bifurcation. The patient was stabilized medically then transferred few days later to the catheterization laboratory. After proper evaluation, under general anesthesia, a bifurcated ENDURANT aortic stent graft was implanted at the level of the fistula through catheterization of the surgically exposed femoral arteries, with successful and
complete exclusion of the fistula resulting in a fast uncomplicated patient recovery. No large case series or controlled trials are available to forward positive evidence in favor of this treatment modality. On this occasion, we undertook a systematic literature review to scope published reports of similarly treated cases to try and draw some conclusions regarding this therapy.
Research Protocol A systematic review of the literature was undertaken to identify all reported cases of endovascular repair of major AVFs, defined as an anomalous communication between the aorta, IVC, renal or iliac arteries and veins. An extensive Webbased review was performed by 2 independent authors, using the words ‘‘Endovascular with aortocaval fistula, aortorenal fistula, iliocaval fistula, iloiliac fistula.’’ The references of the retrieved articles were also scoped. Articles in languages other than English were translated. The online search covered all articles published till September 2013 in the following databases: Medline, Cochrane, Embase/Elsevier, Wiley online, Springer 1
Cardiology Department, Lebanese University, Beirut, Lebanon Lebanese University, Beirut, Lebanon
2
Corresponding Author: Ghassan Nakad, Lebanese University, Beirut, 6573-14, Lebanon. Email: [email protected]
Downloaded from ves.sagepub.com at PENNSYLVANIA STATE UNIV on August 12, 2014
2
Vascular and Endovascular Surgery
link, Researchgate, Science direct, Clinicaltrials.gov, and Google Scholary for relevant peer-reviewed journals. The search found 48 articles reporting 53 patients with major abdominal AVFs, treated by different endovascular modalities2-49. Including our case, a total of 54 patients were included in the analysis (Table 1). Inclusion criteria consisted of case report articles, with uniquely endovascular treatment administered as primary therapy. Book chapters and systematic reviews were excluded of our review along with 2 articles reporting a hybrid procedure (combining endovascular and surgical).50,51 The primary outcome measures were technical success (obliteration of the fistula, with or without complications, and not requiring open surgical conversion), perioperative, and 90-day mortality. The secondary outcome measures were procedurerelated complications, minor defined as requiring observation and major defined as requiring reintervention, and the operator’s retrospective personal recommendation regarding the administered therapy as follows: strongly in favor, in favor but with caution, awaiting further guidelines before recommending the technique, and no or negative recommendation. A comparative subanalysis is finally made to compare the mortality and complications rate in between patients receiving elective therapy defined as scheduled procedure versus urgent therapy defined as patients necessitating emergency intervention due to critical state or hemodynamic instability.
Data Analysis and Results In the reviewed cases, the mean age was 65 years (age range 21-85). Of 54 patients (1 patient gender was not recorded), 47 (88%) were males and 6 (12%) were females. The fistula site was the aortocaval segment in 74% (40 of 54) of patients, the iliocaval in 15% (8 of 54), the aortorenal in 5.5% (3 of 54), the iliocaval in 1.8% (1 of 54), renorenal in 1.8% (1 of 54), and the ilioiliac in 1.8% (1 of 54). Primary disease defined as aortic disease or adjacent erosive inflammatory or tumoral process resulted in development of 65% (35 of 54) of the cases; iatrogenic trauma (postlumbar disk surgery, postnephrectomy, postlaparotomy, or by erosion of IVC filter) was responsible of 15% (8 of 54) of cases. In 7.5% (4 of 54) of cases, prior open aortic repair was preformed; in another 7.5% (4 of 54) prior endovascular stenting was preformed and in 5% (3 of 54) previous abdominal trauma was noted. In all, 75% (41 of 54) of the procedures were done in stable patients, whereas 25% (13 of 54) were done in critical or hemodynamically compromised patients. Aortic stent grafts were used in 78% (42 of 54) of patients (19 bifurcated grafts, 1 thoracic graft, one 3-piece endograft, and 21 grafts were nonspecified). In those stented patients, 3 patients also received IVC stents (2 as primary intention, 1 to treat postoperative IVC thrombosis), 1 patient received an Amplatzer occluder, and in 1 case an additional ventricular septal defect occluder along with coiling was used. One patient
had an infrarenal AAA with ACF and was treated with a monoiliac stent graft. Straight grafts were used to treat iliac and renal fistulas in 6 patients, of which 1 patient was additionally treated with coiling embolization. Amplatzer occluder was used alone in 4 patients, patent ductus arteriosus occluder in 1 patient. Simple fistula coiling was achieved in 1 patient, and coiling with N-butyl cyaoacrylate and lipiodol was used in another. The technical success rate was 94% with persistence of the fistula in 3 cases. Perioperative mortality was noted to be 0% (1 case did not report patient’s outcome after failed procedure). In 15 cases, 90-day mortality was not reported. The mortality rate for the 38 remaining patients was 10% (4 of 38). In all, 2 patients died from hemodynamic collapse at days 1 and 2, and the other 2 patients died of sepsis not related to the procedure at days 3 and 35. Complications emerged in 35% (18 of 51) of patients with successful procedures. Major complications arose in 12% (6 of 51) of patients, consisting of type 1a endoleak, type 2 endoleak (2 patients), IVC thrombosis, and stent prolapse into the IVC enlarging the fistula. Those complications were successfully managed by endovascular therapy. A patient presented an endoleak from the iliac aneurysm but died before further therapy. Another patient had to undergo bowel resection after ischemic colitis on day 4 postoperatively. Minor complications occurred in 21% (11 of 51) of patients. They were limited to type 2 endoleaks, 1 patient had type 3 endoleak and another had consumption coagulopathy, and 1 had stress ulcer gastrointestinal bleed and pulmonary emboli. All minor complications were treated conservatively. Off note, complications occurred in 42% (5 of 12) patients of urgent cases, whereas it occurred in 26% (10 of 39) of patients of elective cases. Of the 3 patients, 2 who died were treated in an urgent setting. Authors’ retrospective opinion was largely in favor of endovascular treatment. The opinion of 44 authors including us was strongly in favor of the treatment modality. Two authors gave positive feedback while recommending the therapy with caution. One author awaited further studies before giving recommendations. No conclusion was reached from the authors whose procedures did not meet success.
Interpretation and Discussion Aortocaval fistula was first described by Syme in 1837.1 The first successful surgical repair was reported by Cooley in 1955.5 The first endovascular stent graft to exclude an ACF was successfully implanted in 1998,48 whereas coil embolization of an ACF had been performed successfully 2 years earlier in 1996.49 Newer techniques are being reported for the management of this complex condition in the aim to reduce the high rate of morbidity and mortality associated with ACF. In fact, in recent series, the mortality is reported to range from 12% to 25% in surgical repair.5 This is often complicated by the patient’s comorbidities. Arterialized veins and other pathological changes caused by the relatively chronic fistula
Downloaded from ves.sagepub.com at PENNSYLVANIA STATE UNIV on August 12, 2014
3
Downloaded from ves.sagepub.com at PENNSYLVANIA STATE UNIV on August 12, 2014
2
1
1
1
Elkassaby et al6 2013
2013
2013 2012 2012
2012
2012
Cavalcante7
Kayser8 Takkar et al9 Sinha et al10
Yuminaga et al11 Rapacciuolo et al12
75/F
64/M
1
1
2011 Nu´n˜ez De Arenas 15 Baeza et al LaBarbera 2011 et al16
30/M
49/M
78/F
1
1
1
Shankarappa 2011 et al19 Savastano 2010 et al20 Guzzardi et al21 2010
Covered stent in right common iliac artery
PDA occluder
Amplatzer occluder
Aortouniliac graft system/ aneurysm coiling with VSD device postcomplication Tri-Fab design bifurcated graft/ uni-iliac graft/bi-Fab uniliac graft/aortouni-iliac graft
AAA
Bifurcated stent-graft with temporary IVC filter
Right common iliac 2 Endovascular stent grafts
Persistent ACF after open surgical repair Iliac AVM
1
2010
von Heesen et al18
AAA
2011 4 (2002-2009) 70/M, 74/M, AAA/AAA/AAA/ 66/M, 77/M AAA
71/M
Endovascular prosthesis
Renal artery stump Ampaltzer vascular plug
Iliac artery
Elective Elective
Elective
Elective
0/NA
0/0
0/0
0/0
0/0
0/?
0/0 0/NA 0/0
0/0
Elective
Elective
Elective
0/0
0/0
0/?
Elective/ Day 3 (sepsis)/day 2 urgent/ (hemodynamic collapse)/ urgent/ day 1 (hemodynamic elective collapse)/0/0 Elective 0/?
Urgent
Elective
Elective
Elective
Elective
Elective
Elective Elective Elective
Elective
0/0
0/0 0/?
Day 35, nosocomial pneumonia with MODS
0/?
Elective Vs Urgent Mortality in Hospt/3 m
Bifurcated aortic stent graft with Elective simultaneous IVC stent
Aortic stent graft with IVC filter Bifurcated aortic stent graft
Bifurcated aortic stent graft in aorta and IVC postcomplication
Bifurcated aortic stent graft
Type of tt
Renal artery stump Amplatzer vascular plug AAA Excluder aortic endograft AAA Bifurcated aortic stent graft with suprarenal fixation Iliocaval fistula Bifurcated endovascular aortic stent graft AAA Amplatzer plug for ACF, 2 covered stent grafts from renal arteries till iliac postcomplication Infrarenal AAA Bifurcated aortic stent graft
AAA
AAA
AAA AAA
AAA
AAA
Site of Procedure
Akwei et al17
58/F
1
2012
Nogueira et al14
81/M
1
2012
81/M
62/M
63/M 63/M 60/F
53/M
84/M, 73/M
Thet et al13
1 1 1
1 1
2013 2013
Janczak et al4 Shah et al5
62/M 60/M
80/M
1
Age/Sex
61/M
Nbr of Patients
1
Year
2013 van de Luijtgaarden et al2 Bernstein et al3 2013
Author
Table 1. Published case reports of major abdominal AVMs treated with endovascular approach
Favorable
Authors Recommendation
Equally effective technique and less invasive Valid therapeutic option
Favorable
Procedure safe and effective Favorable
Transient endoleak type 2
Persistent fistula
0/?
0/?
0/endoleak, right internal iliac/0/ endoleak type 1a
(continued)
Attractive alternative to open surgery
Failed procedure
Favorable
Favorable
The safest treatment option for acute ACF in high-risk patients
Endoleak type 2 resolved after Further studies are coiling and VSD occlusion/NA warranted
0/0
Gastrointestinal bleed (stress ulcer). Pulmonary embolus 0/0
0/0
0/?
IVC thrombosis /type I endoleak Successful endovascular from the right hypogastric management of ACF artery /ischemic colitis/ and complication nosocomial pneumonia 0/0 Favorable Endoleak type 2 Successful endovascular management 0/0 Offers an ideal solution in patients with rAAA and ACF 0/0 Treatment is safe and effective 0/0 Favorable 0/NA Favorable 0/0 Favorable
Endoleak type 2
Complications in Hopst/3 m (Procedure Related)
4
Downloaded from ves.sagepub.com at PENNSYLVANIA STATE UNIV on August 12, 2014
1
1 1 1 1
1
2008
2009
2007 2008 2007 2007
2006
2006 2006
2005
Mitchel et al28
Clevert et al29 Taneja et al30 Leon et al31 Marchetti et al32 Pathak et al33
Kopp et al34 Hetzel et al35
Vetrhus et al36
Gandini et al
2002
1
61/F
1
44
85/M
1
Williamson 2002 et al42 Duxbury et al43 2002
67/M
64/M 66/M 73/M
1 1 1
Shaheen et al39 2005 2003 Burke et al40 Laureys et al41 2002
79/M
40/M
66/M, 80/M
68/M 81/M
75/M
64/? 52/M 80/M 67/M
34/M
1
1
2
1 1
1
56/M
40/M
79/M
62/M 21/M
76/?
Age/Sex
2005
Ferrari et al38
2005
1
2008
Cholenahalli et al26 Kwon et al27
Waldrop et al
1
Fujisawa et al25 2009
37
1 1
2009 2008
Janczak et al23 Du¨z et al24
1
2009
Juszkat et al22
Nbr of Patients
Year
Author
Table 1. (continued)
ACF with prior AAA open repair
ACF
Elective
Cuffed stent graft
Monoiliac stent graft AMPLATZER plug Aortic stent graft Bifurcated stent graft
Bifurcated stent graft (excluder), iliac embolization Thoracic stent graft
Self-expanding aortic stent graft
Iliac extension graft
Straight stent graft, bifurcated graft postcomplication Bifurcated stent graft
Elective
Elective
Elective
Urgent Urgent Elective
Elective
Elective/ urgent Urgent
Urgent Urgent
Urgent
Urgent Elective Elective Elective
Elective
Elective
Elective
Elective
0/0
0/?
0/0
0/0 0/0 0/?
0/0
0/0
0/0, 0/0
0/0 0/?
0/0
0/0 0/0 0/? 0/?
0/0
0/0
0/0
0/?
0/0 0/0
0/0
Elective Vs Urgent Mortality in Hospt/3 m
Aortic stent graph with IVC filter Elective Iliac stent graft Elective
Iliac extension graft
Type of tt
AAA Bifurcated stent graft Aorto iliac A with Iliac extension graft with left iliac prior embolization endovascular repair Aorto iliac/AAA Bifurcated stent graft/bifurcated stent graft ACF with prior Aortic extension cuff abdominal trauma Aortorenal with Aortic stent graft prior endovascular repair Aortorenal Bifurcated stent graft AAA Aortic stent graft Complicated Coiling iatrogenic iliocaval fistula Aortoiliac Bifurcated stent graft
AAA with prior open repair
AAA with iliac aneurysm ACF with prior abdominal trauma Infrarenal AA Renal artery stump AAA AAA
AAA/ endoprosthesis 2 y earlier AAA Iliocaval fistula postlumbar disk surgery AAA/ endoprosthesis 2y earlier Ilioiliac
Site of Procedure
Partial stent prolapse in IVC enlarging the fistula 0/0
0/0
0/0 Endoleak type 2 0/?
0/0
0/0
Endoleak type 2/0 ?/?
Endoleak type 2 0/?
Consumption coagulopathy/0
Endoleak type 3 0/0 0/? 0/?
Endoleak type 2
0/0
0/0
0/?
0/0 0/0
0/0
Complications in Hopst/3 m (Procedure Related)
Favorable
(continued)
Successful treatment
Favorable
Favorable Favorable Can be considered the treatment of choice
Favorable
Favorable
Favorable
Technically feasible alternative and confers many advantages Favorable Favorable
Successful procedure Favorable Favorable Favorable
Favorable
Good immediate and midterm success Favorable
Favorable
Favorable Favorable
Good option
Authors Recommendation
5
Downloaded from ves.sagepub.com at PENNSYLVANIA STATE UNIV on August 12, 2014
1
1
1
1
2000
1999
1998
1996
2013
Umscheid and Stelter46 Sultan et al47
Beveridge et al48 Cekirge et al49
Current case
67/M
65/F
71/M
77/M
74/M
61/M
Age/Sex
Aortocaval
Renocaval
Iliocaval
Aortorenal
AAA
Aortoiliac
Site of Procedure
Bifurcated stent graft with iliac embolization Gianturco coils and N-butyl cyaoacrylate with lipiodol Bifurcated stent graft
Straight stent graft
Elective
Elective
Elective
Elective
0/0
0/?
0/0
?/?
0/0
0/0
Elective Vs Urgent Mortality in Hospt/3 m
Aortomonoiliac stent-graft, right Urgent iliac embolization, left iliac embolization, fem-fem bypass Bifurcated stent graft Urgent
Type of tt
0/0
0/?
Failed procedure, persistent fistula Endoleak
0/0
Persistent fistula, hypertension, graft thrombosis, graft stenosis
Complications in Hopst/3 m (Procedure Related)
Approach with considerable benefits
Failed procedure
Favorable
Authors Recommendation
Abbreviations: Nbr, number; hospt, hospital; m, month; AAA, abdominal aortic aneurysm; IVC, inferior vena cava; MODS, multiple organ dysfunction syndrome; ACF, aortocaval fistula; rAAA, ruptured abdominal aortic aneurysm; M, male; F, female; NA, not applicable; VSD, ventricular septal defect; PDA, patent ductus arteriosus; fem-fem, femoral-femoral; tt, treatment; AVM, Aorto venous malformation. Note. ? ¼ data not reported by published article.
1
1
2001
Lau et al45
Nbr of Patients
Year
Author
Table 1. (continued)
6
Vascular and Endovascular Surgery
lead to unavoidable massive intraoperative blood loss.1 In semielective cases, the mortality rate approaches 30%, especially in patients with cardiovascular decompensation.1 Two cases of hybrid surgical and endovascular approach have been described, aiming to reverse the negative hemodynamic effects of the ACF before subsequent surgery or simply because the anatomy was unsuitable for total endovascular repair.50,51 Compared to the complexity of the open repair procedure and the high-surgical risk, the endovascular repair of an ACF offers a less invasive procedure, limits the hemodynamic lability during intervention, and has a less risk for major blood loss. No guidelines are available for the endovascular treatment of major AVFs, as the pathology is rare and the therapy is relatively new. Hence, we present this systematic review to try and address the cause. Our literature analysis of the outcome after endovascular repair of major AVFs showed an obliteration of the AVF in 94% of cases. In the majority of those cases, the AVF was a true ACF. Bifurcated stent grafts were mostly used, especially in the newer reports. In contrast to the high mortality of open repair, there was no perioperative mortality in the reviewed 54 patients, with the mortality at 90 days rating at 10% (4 of 38) of reported cases, half of which was not directly related to the ACF (sepsis at days 3 and 35).3,17 We note that the technical procedure was a success, and the fistula was excluded in all patients who died. Of successfully treated patients, 12% had major complications and required endovascular reintervention, all of whom had subsequent uneventful recovery. One patient died before reintervention would be possible,17 and 21% of patients had minor self-limited complications. Type 2 endovascular leak was the most frequent encountered complication. A watchful wait approach was used in all but onepatient having this complication . All monitored type 2 leaks underwent thrombosis on later follow-up. We found neither evidence nor case reports to support the theoretical concern that the AVF might persist after endovascular treatment if type 2 leak is present. Our series of cases are in favor of the opposite claim. That remaining a theoretical possibility, an early close follow-up is required to guide reintervention in the occurrence of a persistent fistula or an aneurysm in further growth. Urgent procedures resulted in nearly double the rates of complications when compared to elective ones. Patients in shock have the worst outcomes. An article published by Ghilardi et al reviewed the outcomes of patients after open surgery. It stated a decrease in mortality from 50% to 25% if patients are operated on in a stable hemodynamic state.52 This correlates with our findings, as in our series, we noticed a reduction in complications for 42% in urgently performed procedures to 26% in elective ones. Of note is the importance of a correct diagnosis of the ACF, which promotes earlier treatment in a more stable patient. Bednarkiewicz et al. reported as much as 4 of 7 patients to be misdiagnosed in a preoperative setting.53 In the presented cases, 75% of the reported patients had a fistula in the aortocaval
segment, 65% of patients had a primary aortic disease or adjacent periaortic inflammation leading to aortic and venous erosion. Those patients have seldom been previously diagnosed with aortic diseases, and thus clinical awareness of the different and elusive presentation on an ACF is of importance to treat the patient early. The classical signs of ACF are triad of abdominal pain, pulsatile abdominal mass, and machinery-like abdominal bruit. These are found only in 50% to 80% of all cases.45 Other signs and symptoms including hematuria, oliguria, high-output congestive heart failure, scrotal or lower extremity edema with or without deep vein thrombosis, abdominal pain, chest pain, low back pain, tenesmus, priapism, poor peripheral pulses, and shock have all been reported.1,54 Forty-six authors strongly recommended the endovascular treatment of ACF, while no author gave a negative opinion. All opinions stated a higher benefit for the patients on short and mid term. We have to note that no follow-up was reported beyond 24 months, with a mean follow-up merely ranging 9 months in some reported cases. This leaves no room to draw conclusions regarding the long-term efficacy of such a treatment modality. Another concern is that of a biased publication. Our aforementioned figures are drawn from published successful cases in a majority. These represent the best outcomes of the treatment modality, considering that unsuccessful procedures are less likely to be published. Larger series or randomized controlled trials are needed to solidify the above-mentioned results.
Conclusion The presentation on major AVFs is elusive most of the times, as the diagnosis might not be a straight forward one. Good knowledge of this entity renders treatment more effective and less risky. Surgical treatment has long been the only available therapy, with high mortality and morbidity. Our single case experience and our literature review make us believe that the new emerging endovascular modalities seem to offer a safer and a more efficient approach compared to traditional open repair, with excellent short- and mid-term results. Long-term results, larger series, or randomized controlled trials are a must before reaching definite conclusions regarding this treatment modality. Declaration of Conflicting Interests The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Funding The author(s) received no financial support for the research, authorship, and/or publication of this article.
References 1. Brightwell RE, Pegna V, Boyne N. Aortocaval fistula: current management strategies. ANZ J Surg. 2013;83(1-2):31-35. 2. van de Luijtgaarden KM, Bastos Gonc¸alves F, Rouwet EV, Hendriks JM, Ten Raa S, Verhagen HJ. Conservative management of
Downloaded from ves.sagepub.com at PENNSYLVANIA STATE UNIV on August 12, 2014
Nakad et al
3.
4.
5.
6.
7.
8.
9.
10.
11.
12.
13.
14.
15.
16.
17.
7
persistent aortocaval fistula after endovascular aortic repair. J Vasc Surg. 2013;58(4):1080-1083. Bernstein J, Jimenez JC. Inferior vena cava thrombosis following endovascular repair of acute aortocaval fistula: a word of caution. Vasc Endovascular Surg. 2013;47(6):467-469 Janczak D, Chabowski M, Szydelko T, Garcarek J. Endovascular exclusion of a large spontaneous aortocaval fistula in a patient with a ruptured aortic aneurysm [published online March 19, 2013]. Vascular. 2013. Shah TR, Parikh P, Borkon M, et al. Endovascular repair of contained abdominal aortic aneurysm rupture with aortocaval fistula presenting with high-output heart failure. Vasc Endovascular Surg. 2013;47(1):51-56. Elkassaby M, Alawy M, Zaki M, Hynes N, Tawfick W, Sultan S. Total endovascular management of ruptured aortocaval fistula: Technical challenges and case report [published online September 2, 2013]. Vascular. 2013. Cavalcante LP, Bernardes MV, Rocha RD, et al. Endovascular treatment of late post-traumatic aortocaval fistula: case report. J Vasc Bras (Porto Alegre). 2013;12(1):75-80. Kayser O, Scha¨fer P. Transcatheter Amplatzer vascular plugembolization of a giant postnephrectomy arteriovenous fistula combined with an aneurysm of the renal pedicle by throughand-through, arteriovenous access. Ger Med Sci. 2013;11:Doc01. Takkar C, Choi L, Mastouri N, Kadambi PV. Aortocaval fistula: a rare cause of venous hypertension and acute renal failure. Case Rep Surg. 2012;2012:487079. Sinha S, Kember P, Currie I. Emergency endovascular repair of iatrogenic aortocaval fistula: a rare complication of laparoscopic surgery. Surg Laparosc Endosc Percutan Tech. 2012; 22(3):e159-e160 Yuminaga Y, Mohabbat W, Nguyen T, Thompson AM, Fisher CM. Simultaneous endovascular repair of an iatrogenic carotidjugular fistula and a large iliocaval fistula presenting with multiorgan failure: a case report. J Med Case Rep. 2012;6:33. doi: 10. 1186/1752-1947-6-33. Rapacciuolo A, De Angelis MC, di Pietro E, et al. Percutaneous treatment of a aorto-caval fistula in a old high risk patient. BMC Surg. 2012;12(suppl 1):S32. Thet Y, Ranjit A, Ravi R, Khand A. High output cardiac failure and paradoxical pulmonary emboli secondary to aortocaval fistula. Postgrad Med J. 2012;88(1044):613-614. Nogueira C, Machado R, Vaz C, Loureiro L, Tavares J, Almeida R. Unconventional endovascular treatment of iatrogenic ilio-cava fistula. Angiol Cir Vasc(Lisboa dez). 2012;8(4):177-180. Nu´n˜ez De Arenas Baeza GF, Haurie Girelli J, Gonza´lez Herraez JV, Garcı´a Leo´n A, Gutierrez Del Manzano JA. Tratamiento endovascular de fı´stula arteriovenosa del mun˜o´n renal postnefrectomı´a con Amplatzer vascular plug II. Angiologı´a. 2011;63(3): 145-147. LaBarbera M, Nathanson D, Hui P. Percutaneous closure of aortocaval fistula using the amplatzer muscular VSD occluder. J Invasive Cardiol. 2011;23(8):343-344. Akwei S, Altaf N, Tennant W, MacSweeney S, Braithwaite B. Emergency endovascular repair of aortocaval fistula–a single center experience. Vasc Endovasc Surg. 2011;45(5):442-446.
18. von Heesen M, Sperling J, Plusczyk T, et al. Multimodal approach in coincidence of covered ruptured abdominal aortic aneurysm and aortocaval fistula. Dtsch Med Wochenschr. 2010;135(46): 2296-2299. 19. Shankarappa RK, Panneerselvam A, Dwarakaprasad R, Chikkaswamy SB, Nayak MH, Nanjappa. Novel transcatheter closure of internal iliac arteriovenous malformation. Cardiovasc Interv Ther. 2011;26(2):138-141. 20. Savastano S, Mario B, Dall’acqua J, Mansi G. A right common iliac artery pseudoaneurysm with an iliac-caval arteriovenous fistula: a rare complication of the Recovery vena cava filter. Cardiovasc Intervent Radiol. 2010;33(3):667-669. 21. Guzzardi G, Fossaceca R, Divenuto I, Musiani A, Brustia P, Carriero A. Endovascular treatment of ruptured abdominal aortic aneurysm with aortocaval fistula. Cardiovasc Intervent Radiol. 2010;33(4): 853-856. 22. Juszkat R, Pukacki F, Zarzecka A, Kulesza J, Majewski W. Endovascular treatment of ruptured abdominal aneurysm into the inferior vena cava in patient after stent graft placement. Cardiovasc Intervent Radiol. 2009;32(4):776-780. 23. Janczak D, Pupka A, Garcarek J, Szyber P. The use of politetrafluoroethylene stent-graft and vena cava filter in the endovascular treatment of ruptured abdominal aortic aneurysm with aortocaval fistula. Polim Med. 2009;39(3):3-8. 24. Du¨z B, Kaplan M, Gu¨nay C, Ustu¨nso¨z B, Ug˘urel MS. Iliocaval arteriovenous fistula following lumbar disc surgery: endovascular treatment with a stentgraft. Turk Neurosurg. 2008; 18(3):245-248. 25. Fujisawa Y, Kurimoto Y, Morishita K, et al. Aortocaval fistula after endovascular stent-grafting of abdominal aortic aneurysm. J Cardiovasc Surg (Torino). 2009;50(3):387-389. 26. Cholenahalli NM, Prabhavathi, Kikkeri HS, et al. Iatrogenic iliac arteriovenous fistula following lumbar disc surgery. Post Kardiol Interw. 2008;4, 1(11):40-42. 27. Kwon SH, Oh JH, Park SJ, Park HC. Endovascular repair of a spontaneous right common iliac artery: inferior vena cava fistula due to infrarenal aortoiliac aneurysm. Vasc Endovascular Surg. 2008;42(3):279-283. 28. Mitchell ME, McDaniel HB, Rushton FW. Endovascular repair of a chronic aortocaval fistula using a thoracic aortic endoprosthesis. Ann Vasc Surg. 2009;23(1):150-152. 29. Clevert DA, Stickel M, Flach P, et al. Contrast-enhanced ultrasound in detection and follow-up of an infrarenal abdominal aortic aneurysm with aorto-caval fistula and endovascular treatment. Cardiovasc Intervent Radiol. 2007;30(3):480-484. 30. Taneja M, Lath N, Soo TB, et al. Renal artery stump to inferior vena cava fistula: unusual clinical presentation and transcatheter embolization with the Amplatzer vascular plug. Cardiovascular Interv Radiol. 2008;31(2 suppl):92-95. 31. Leon LR, Arslan B, Ley E, Labropoulos N. Endovascular therapy of spontaneous aortocaval fistulae associated with abdominal aortic aneurysms. Vascular. 2007;15(1):35-40. 32. Ascoli Marchetti A, Gandini R, Ippoliti A, et al. The endovascular management of open aortic surgery complications with emergency stentgraft repair in high-risk patients. J Cardiovasc Surg (Torino). 2007;48(3):315-321.
Downloaded from ves.sagepub.com at PENNSYLVANIA STATE UNIV on August 12, 2014
8
Vascular and Endovascular Surgery
33. Pathak S, Yusuf SW, Doyle TN, Francis IA, Hurst PA, Davidson C. Endovascular repair of a recurrent aortocaval fistula and astomotic false aneurysm. Br J Radiol. 2006;79(944):e62-e63. 34. Kopp R, Weidenhagen R, Hoffmann R, et al. Immediate endovascular treatment of an aortoiliac aneurysm ruptured into the inferior vena cava. Ann Vasc Surg. 2006;20(4):525-528. 35. Hetzel G, Gabriel P, Rompel O, Ritter W, Raithel D. Aortocaval fistula after stent-graft repair. J Endovasc Ther. 2006;13(1):117-120. 36. Vetrhus M, McWilliams R, Tan CK, Brennan J, Gilling-Smith G, Harris PL. Endovascular repair of abdominal aortic aneurysms with aortocaval fistula. Eur J Vasc Endovasc Surg. 2005;30(6): 640-643. 37. Waldrop JL, Dart BW, Barker DE. Endovascular stent graft treatment of a traumatic aortocaval fistula. Ann Vasc Surg. 2005; 19(4):562-565. 38. Ferrari M, Berchiolli R, Sardella SG, et al. Endovascular repair of an aorto–left renal vein fistula due to a ruptured abdominal aortic aneurysm after EVAR. J Endovasc Ther. 2005;12(4):512-505. 39. Shaheen RM, Kibbe MR, Eskandari MK. Endoluminal repair of an acute aortoleft renal vein fistula. Surgery. 2005;138(1):109-110. 40. Burke C, Mauro MA. SIR 2003 film panel case 8: aortocaval fistula supplied by a type II endoleak. J Vasc Interv Radiol. 2003; 14(6):813-817. 41. Laureys M, Tannouri F, Rommens J, Dussaussois L, Golzarian J. Percutaneous treatment of iatrogenic iliocaval fistula related to endograft placement for abdominal aortic aneurysm. J Vasc Interv Radiol. 2002;13(2 pt 1):211-213. 42. Williamson AE, Annunziata G, Cone LA, Smith J. Endovascular repair of a ruptured abdominal aortic and liac artery aneurysm with an acute iliocaval fistula secondary to lymphoma. Ann Vasc Surg. 2002;16(2):145-149. 43. Duxbury MS, Wells IP, Roobottom C, Marshall A, Lambert AW. Endovascular repair of spontaneous non-aneurysmal aortocaval fistula. Eur J Vasc Endovasc Surg. 2002;24(3):276-278. 44. Gandini R, Ippoliti A, Pampana E, Ascoli Marchetti A, Raimondo Pistolese G, Simonetti G. Emergency endograft placement for
45.
46.
47.
48.
49.
50.
51.
52.
53.
54.
recurrent aortocaval fistula after conventional AAA repair. J Endovasc Ther. 2002;9(2):208-211. Lau LL, O’Reilly MJ, Johnston LC, Lee B. Endovascular stentgraft repair of primary aortocaval fistula with an abdominal aortoiliac aneurysm. J Vasc Surg. 2001;33(2):425-428. Umscheid T, Stelter WJ. Endovascular treatment of an aortic aneurysm ruptured into the inferior vena cava. J Endovasc Ther. 2000;7(1):31-35. Sultan S, Madhavan P, Colgan MP, et al. Aorto–left renal vein fistula: is there a place for endovascular management? J Endovasc Surg. 1999;6(4):375-377. Beveridge CJ, Pleass HC, Chamberlain J, Wyatt MG, Rose JD. Aortoiliac aneurysm with arteriocaval fistula treated by a bifurcated endovascular stent-graft. Cardiovasc Intervent Radiol. 1998;21(3):244-246. Cekirge S, Oguzkurt L, Saatc¸i I, Boyvat F, Balkanci F. Embolization of a high-output postnephrectomy aortocaval fistula with Gianturco coils and cyanoacrylate. Cardiovasc Intervent Radiol. 1996;19(1):56-58. Raux M, Cochennec F, Kobeiter H, Bruguie`re E, Becquemin JP. Images in cardiovascular medicine: high-output heart failure. Circulation. 2010;121(16):e386-e387. Siepe M, Koeppe S, Euringer W, Schlensak C. Aorto-caval fistula from acute rupture of an abdominal aortic aneurysm treated with a hybrid approach. J Vasc Surg. 2009;49(6):1574-1576. Ghilardi G, Scorza R, Bortolani E, De Monti M, Longhi F, Ruberti U. Rupture of abdominal aortic aneurysms into the major abdominal veins. J Cardiovasc Surg (Torino). 1993;34(1):39-47. Bednarkiewicz M, Pretre R, Kalangos A, Khatchatourian G, Bruschweiler I, Faidutti B. Aortocaval fistula associated with abdominal aortic aneurysm: a diagnostic challenge. Ann Vasc Surg. 1997;11(5):464-466. Davidovic L, Dragas M, Cvetkovic S, Kostic D, Cinara I, Banzic I. Twenty years of experience in the treatment of spontaneous aorto-venous fistulas in a developing country. World J Surg. 2011;35(8):1829-1834.
Downloaded from ves.sagepub.com at PENNSYLVANIA STATE UNIV on August 12, 2014
Endovascular Treatment of Major Abdominal Arteriovenous Fistulas: A Systematic Review Ghassan Nakad, Ghassan AbiChedid and Raed Osman VASC ENDOVASCULAR SURG published online 26 June 2014 DOI: 10.1177/1538574414540485 The online version of this article can be found at: http://ves.sagepub.com/content/early/2014/06/25/1538574414540485
Published by: http://www.sagepublications.com
Additional services and information for Vascular and Endovascular Surgery can be found at: Email Alerts: http://ves.sagepub.com/cgi/alerts Subscriptions: http://ves.sagepub.com/subscriptions Reprints: http://www.sagepub.com/journalsReprints.nav Permissions: http://www.sagepub.com/journalsPermissions.nav Citations: http://ves.sagepub.com/content/early/2014/06/25/1538574414540485.refs.html
>> OnlineFirst Version of Record - Jun 26, 2014 What is This?
Downloaded from ves.sagepub.com at PENNSYLVANIA STATE UNIV on August 12, 2014
Article
Endovascular Treatment of Major Abdominal Arteriovenous Fistulas: A Systematic Review
Vascular and Endovascular Surgery 1-8 ª The Author(s) 2014 Reprints and permission: sagepub.com/journalsPermissions.nav DOI: 10.1177/1538574414540485 ves.sagepub.com
Ghassan Nakad1, Ghassan AbiChedid2, and Raed Osman2
Abstract Purpose: To review the different outcomes of the endovascular repair of major abdominal arteriovenous fistulas (AVFs). Methods: An online systematic review of the literature was undertaken to identify all reported cases of endovascular repair of major AVFs, covering 9 major databases as well as relevant journals up to September 2013. Our own case was included. The primary outcome was technical success and mortality, the secondary outcome was the rate of complications and the operators’ recommendations. Results: Forty-eight articles were reviewed totaling a number of 54 patients including our own. The most common fistula site was the aortocaval segment. Aortic stent grafts were used in 78% of patients. Technical success was 94%. Intraoperative mortality was 0% with a 90-day mortality of 10%, half of which were not related to the primary pathology. Of the successful procedures, 12% of patients had major complications. One died before reintervention. All others had uneventful recoveries; 21% had minor complications treated conservatively. The majority of authors were in favor of this treatment modality. Keywords aortocaval, endovascular, arteriovenous fistula, aneurysm, aortic graft
Introduction Major abdominal arteriovenous fistulas (AVFs) are defined as anomalous communications between the aorta, iliac or renal arteries, the inferior vena cava (IVC), and iliac or renal veins. The most common AVF is aortocaval fistula (ACF). This condition is rare, involving less than 1% of abdominal aortic aneurysms (AAAs). It can be either primary due to a disease of the aorta or secondary due to iatrogenic, malignant, or traumatic causes.1 This condition is rapidly fatal if not treated, and repair of the arteriovenous communications is mandatory for restitution of a normal hemodynamic status. Traditional treatment consists of open surgical repair. This is associated with high morbidity and mortality. Endovascular treatment modalities are emerging, promising a safer, more efficient approach. Several isolated case reports of successful endovascular treatment have been published. We had the opportunity to treat a patient with an inflammatory AAA complicated by an infrarenal ACF. He presented to our institution with symptoms and signs of global with right predominant heart failure. He had a recent history of aortitis and retroperitoneal fibrosis. An abdominal angiocomputed tomography scan revealed the ACF at the level of the distal descending aorta just before the iliac bifurcation. The patient was stabilized medically then transferred few days later to the catheterization laboratory. After proper evaluation, under general anesthesia, a bifurcated ENDURANT aortic stent graft was implanted at the level of the fistula through catheterization of the surgically exposed femoral arteries, with successful and
complete exclusion of the fistula resulting in a fast uncomplicated patient recovery. No large case series or controlled trials are available to forward positive evidence in favor of this treatment modality. On this occasion, we undertook a systematic literature review to scope published reports of similarly treated cases to try and draw some conclusions regarding this therapy.
Research Protocol A systematic review of the literature was undertaken to identify all reported cases of endovascular repair of major AVFs, defined as an anomalous communication between the aorta, IVC, renal or iliac arteries and veins. An extensive Webbased review was performed by 2 independent authors, using the words ‘‘Endovascular with aortocaval fistula, aortorenal fistula, iliocaval fistula, iloiliac fistula.’’ The references of the retrieved articles were also scoped. Articles in languages other than English were translated. The online search covered all articles published till September 2013 in the following databases: Medline, Cochrane, Embase/Elsevier, Wiley online, Springer 1
Cardiology Department, Lebanese University, Beirut, Lebanon Lebanese University, Beirut, Lebanon
2
Corresponding Author: Ghassan Nakad, Lebanese University, Beirut, 6573-14, Lebanon. Email: [email protected]
Downloaded from ves.sagepub.com at PENNSYLVANIA STATE UNIV on August 12, 2014
2
Vascular and Endovascular Surgery
link, Researchgate, Science direct, Clinicaltrials.gov, and Google Scholary for relevant peer-reviewed journals. The search found 48 articles reporting 53 patients with major abdominal AVFs, treated by different endovascular modalities2-49. Including our case, a total of 54 patients were included in the analysis (Table 1). Inclusion criteria consisted of case report articles, with uniquely endovascular treatment administered as primary therapy. Book chapters and systematic reviews were excluded of our review along with 2 articles reporting a hybrid procedure (combining endovascular and surgical).50,51 The primary outcome measures were technical success (obliteration of the fistula, with or without complications, and not requiring open surgical conversion), perioperative, and 90-day mortality. The secondary outcome measures were procedurerelated complications, minor defined as requiring observation and major defined as requiring reintervention, and the operator’s retrospective personal recommendation regarding the administered therapy as follows: strongly in favor, in favor but with caution, awaiting further guidelines before recommending the technique, and no or negative recommendation. A comparative subanalysis is finally made to compare the mortality and complications rate in between patients receiving elective therapy defined as scheduled procedure versus urgent therapy defined as patients necessitating emergency intervention due to critical state or hemodynamic instability.
Data Analysis and Results In the reviewed cases, the mean age was 65 years (age range 21-85). Of 54 patients (1 patient gender was not recorded), 47 (88%) were males and 6 (12%) were females. The fistula site was the aortocaval segment in 74% (40 of 54) of patients, the iliocaval in 15% (8 of 54), the aortorenal in 5.5% (3 of 54), the iliocaval in 1.8% (1 of 54), renorenal in 1.8% (1 of 54), and the ilioiliac in 1.8% (1 of 54). Primary disease defined as aortic disease or adjacent erosive inflammatory or tumoral process resulted in development of 65% (35 of 54) of the cases; iatrogenic trauma (postlumbar disk surgery, postnephrectomy, postlaparotomy, or by erosion of IVC filter) was responsible of 15% (8 of 54) of cases. In 7.5% (4 of 54) of cases, prior open aortic repair was preformed; in another 7.5% (4 of 54) prior endovascular stenting was preformed and in 5% (3 of 54) previous abdominal trauma was noted. In all, 75% (41 of 54) of the procedures were done in stable patients, whereas 25% (13 of 54) were done in critical or hemodynamically compromised patients. Aortic stent grafts were used in 78% (42 of 54) of patients (19 bifurcated grafts, 1 thoracic graft, one 3-piece endograft, and 21 grafts were nonspecified). In those stented patients, 3 patients also received IVC stents (2 as primary intention, 1 to treat postoperative IVC thrombosis), 1 patient received an Amplatzer occluder, and in 1 case an additional ventricular septal defect occluder along with coiling was used. One patient
had an infrarenal AAA with ACF and was treated with a monoiliac stent graft. Straight grafts were used to treat iliac and renal fistulas in 6 patients, of which 1 patient was additionally treated with coiling embolization. Amplatzer occluder was used alone in 4 patients, patent ductus arteriosus occluder in 1 patient. Simple fistula coiling was achieved in 1 patient, and coiling with N-butyl cyaoacrylate and lipiodol was used in another. The technical success rate was 94% with persistence of the fistula in 3 cases. Perioperative mortality was noted to be 0% (1 case did not report patient’s outcome after failed procedure). In 15 cases, 90-day mortality was not reported. The mortality rate for the 38 remaining patients was 10% (4 of 38). In all, 2 patients died from hemodynamic collapse at days 1 and 2, and the other 2 patients died of sepsis not related to the procedure at days 3 and 35. Complications emerged in 35% (18 of 51) of patients with successful procedures. Major complications arose in 12% (6 of 51) of patients, consisting of type 1a endoleak, type 2 endoleak (2 patients), IVC thrombosis, and stent prolapse into the IVC enlarging the fistula. Those complications were successfully managed by endovascular therapy. A patient presented an endoleak from the iliac aneurysm but died before further therapy. Another patient had to undergo bowel resection after ischemic colitis on day 4 postoperatively. Minor complications occurred in 21% (11 of 51) of patients. They were limited to type 2 endoleaks, 1 patient had type 3 endoleak and another had consumption coagulopathy, and 1 had stress ulcer gastrointestinal bleed and pulmonary emboli. All minor complications were treated conservatively. Off note, complications occurred in 42% (5 of 12) patients of urgent cases, whereas it occurred in 26% (10 of 39) of patients of elective cases. Of the 3 patients, 2 who died were treated in an urgent setting. Authors’ retrospective opinion was largely in favor of endovascular treatment. The opinion of 44 authors including us was strongly in favor of the treatment modality. Two authors gave positive feedback while recommending the therapy with caution. One author awaited further studies before giving recommendations. No conclusion was reached from the authors whose procedures did not meet success.
Interpretation and Discussion Aortocaval fistula was first described by Syme in 1837.1 The first successful surgical repair was reported by Cooley in 1955.5 The first endovascular stent graft to exclude an ACF was successfully implanted in 1998,48 whereas coil embolization of an ACF had been performed successfully 2 years earlier in 1996.49 Newer techniques are being reported for the management of this complex condition in the aim to reduce the high rate of morbidity and mortality associated with ACF. In fact, in recent series, the mortality is reported to range from 12% to 25% in surgical repair.5 This is often complicated by the patient’s comorbidities. Arterialized veins and other pathological changes caused by the relatively chronic fistula
Downloaded from ves.sagepub.com at PENNSYLVANIA STATE UNIV on August 12, 2014
3
Downloaded from ves.sagepub.com at PENNSYLVANIA STATE UNIV on August 12, 2014
2
1
1
1
Elkassaby et al6 2013
2013
2013 2012 2012
2012
2012
Cavalcante7
Kayser8 Takkar et al9 Sinha et al10
Yuminaga et al11 Rapacciuolo et al12
75/F
64/M
1
1
2011 Nu´n˜ez De Arenas 15 Baeza et al LaBarbera 2011 et al16
30/M
49/M
78/F
1
1
1
Shankarappa 2011 et al19 Savastano 2010 et al20 Guzzardi et al21 2010
Covered stent in right common iliac artery
PDA occluder
Amplatzer occluder
Aortouniliac graft system/ aneurysm coiling with VSD device postcomplication Tri-Fab design bifurcated graft/ uni-iliac graft/bi-Fab uniliac graft/aortouni-iliac graft
AAA
Bifurcated stent-graft with temporary IVC filter
Right common iliac 2 Endovascular stent grafts
Persistent ACF after open surgical repair Iliac AVM
1
2010
von Heesen et al18
AAA
2011 4 (2002-2009) 70/M, 74/M, AAA/AAA/AAA/ 66/M, 77/M AAA
71/M
Endovascular prosthesis
Renal artery stump Ampaltzer vascular plug
Iliac artery
Elective Elective
Elective
Elective
0/NA
0/0
0/0
0/0
0/0
0/?
0/0 0/NA 0/0
0/0
Elective
Elective
Elective
0/0
0/0
0/?
Elective/ Day 3 (sepsis)/day 2 urgent/ (hemodynamic collapse)/ urgent/ day 1 (hemodynamic elective collapse)/0/0 Elective 0/?
Urgent
Elective
Elective
Elective
Elective
Elective
Elective Elective Elective
Elective
0/0
0/0 0/?
Day 35, nosocomial pneumonia with MODS
0/?
Elective Vs Urgent Mortality in Hospt/3 m
Bifurcated aortic stent graft with Elective simultaneous IVC stent
Aortic stent graft with IVC filter Bifurcated aortic stent graft
Bifurcated aortic stent graft in aorta and IVC postcomplication
Bifurcated aortic stent graft
Type of tt
Renal artery stump Amplatzer vascular plug AAA Excluder aortic endograft AAA Bifurcated aortic stent graft with suprarenal fixation Iliocaval fistula Bifurcated endovascular aortic stent graft AAA Amplatzer plug for ACF, 2 covered stent grafts from renal arteries till iliac postcomplication Infrarenal AAA Bifurcated aortic stent graft
AAA
AAA
AAA AAA
AAA
AAA
Site of Procedure
Akwei et al17
58/F
1
2012
Nogueira et al14
81/M
1
2012
81/M
62/M
63/M 63/M 60/F
53/M
84/M, 73/M
Thet et al13
1 1 1
1 1
2013 2013
Janczak et al4 Shah et al5
62/M 60/M
80/M
1
Age/Sex
61/M
Nbr of Patients
1
Year
2013 van de Luijtgaarden et al2 Bernstein et al3 2013
Author
Table 1. Published case reports of major abdominal AVMs treated with endovascular approach
Favorable
Authors Recommendation
Equally effective technique and less invasive Valid therapeutic option
Favorable
Procedure safe and effective Favorable
Transient endoleak type 2
Persistent fistula
0/?
0/?
0/endoleak, right internal iliac/0/ endoleak type 1a
(continued)
Attractive alternative to open surgery
Failed procedure
Favorable
Favorable
The safest treatment option for acute ACF in high-risk patients
Endoleak type 2 resolved after Further studies are coiling and VSD occlusion/NA warranted
0/0
Gastrointestinal bleed (stress ulcer). Pulmonary embolus 0/0
0/0
0/?
IVC thrombosis /type I endoleak Successful endovascular from the right hypogastric management of ACF artery /ischemic colitis/ and complication nosocomial pneumonia 0/0 Favorable Endoleak type 2 Successful endovascular management 0/0 Offers an ideal solution in patients with rAAA and ACF 0/0 Treatment is safe and effective 0/0 Favorable 0/NA Favorable 0/0 Favorable
Endoleak type 2
Complications in Hopst/3 m (Procedure Related)
4
Downloaded from ves.sagepub.com at PENNSYLVANIA STATE UNIV on August 12, 2014
1
1 1 1 1
1
2008
2009
2007 2008 2007 2007
2006
2006 2006
2005
Mitchel et al28
Clevert et al29 Taneja et al30 Leon et al31 Marchetti et al32 Pathak et al33
Kopp et al34 Hetzel et al35
Vetrhus et al36
Gandini et al
2002
1
61/F
1
44
85/M
1
Williamson 2002 et al42 Duxbury et al43 2002
67/M
64/M 66/M 73/M
1 1 1
Shaheen et al39 2005 2003 Burke et al40 Laureys et al41 2002
79/M
40/M
66/M, 80/M
68/M 81/M
75/M
64/? 52/M 80/M 67/M
34/M
1
1
2
1 1
1
56/M
40/M
79/M
62/M 21/M
76/?
Age/Sex
2005
Ferrari et al38
2005
1
2008
Cholenahalli et al26 Kwon et al27
Waldrop et al
1
Fujisawa et al25 2009
37
1 1
2009 2008
Janczak et al23 Du¨z et al24
1
2009
Juszkat et al22
Nbr of Patients
Year
Author
Table 1. (continued)
ACF with prior AAA open repair
ACF
Elective
Cuffed stent graft
Monoiliac stent graft AMPLATZER plug Aortic stent graft Bifurcated stent graft
Bifurcated stent graft (excluder), iliac embolization Thoracic stent graft
Self-expanding aortic stent graft
Iliac extension graft
Straight stent graft, bifurcated graft postcomplication Bifurcated stent graft
Elective
Elective
Elective
Urgent Urgent Elective
Elective
Elective/ urgent Urgent
Urgent Urgent
Urgent
Urgent Elective Elective Elective
Elective
Elective
Elective
Elective
0/0
0/?
0/0
0/0 0/0 0/?
0/0
0/0
0/0, 0/0
0/0 0/?
0/0
0/0 0/0 0/? 0/?
0/0
0/0
0/0
0/?
0/0 0/0
0/0
Elective Vs Urgent Mortality in Hospt/3 m
Aortic stent graph with IVC filter Elective Iliac stent graft Elective
Iliac extension graft
Type of tt
AAA Bifurcated stent graft Aorto iliac A with Iliac extension graft with left iliac prior embolization endovascular repair Aorto iliac/AAA Bifurcated stent graft/bifurcated stent graft ACF with prior Aortic extension cuff abdominal trauma Aortorenal with Aortic stent graft prior endovascular repair Aortorenal Bifurcated stent graft AAA Aortic stent graft Complicated Coiling iatrogenic iliocaval fistula Aortoiliac Bifurcated stent graft
AAA with prior open repair
AAA with iliac aneurysm ACF with prior abdominal trauma Infrarenal AA Renal artery stump AAA AAA
AAA/ endoprosthesis 2 y earlier AAA Iliocaval fistula postlumbar disk surgery AAA/ endoprosthesis 2y earlier Ilioiliac
Site of Procedure
Partial stent prolapse in IVC enlarging the fistula 0/0
0/0
0/0 Endoleak type 2 0/?
0/0
0/0
Endoleak type 2/0 ?/?
Endoleak type 2 0/?
Consumption coagulopathy/0
Endoleak type 3 0/0 0/? 0/?
Endoleak type 2
0/0
0/0
0/?
0/0 0/0
0/0
Complications in Hopst/3 m (Procedure Related)
Favorable
(continued)
Successful treatment
Favorable
Favorable Favorable Can be considered the treatment of choice
Favorable
Favorable
Favorable
Technically feasible alternative and confers many advantages Favorable Favorable
Successful procedure Favorable Favorable Favorable
Favorable
Good immediate and midterm success Favorable
Favorable
Favorable Favorable
Good option
Authors Recommendation
5
Downloaded from ves.sagepub.com at PENNSYLVANIA STATE UNIV on August 12, 2014
1
1
1
1
2000
1999
1998
1996
2013
Umscheid and Stelter46 Sultan et al47
Beveridge et al48 Cekirge et al49
Current case
67/M
65/F
71/M
77/M
74/M
61/M
Age/Sex
Aortocaval
Renocaval
Iliocaval
Aortorenal
AAA
Aortoiliac
Site of Procedure
Bifurcated stent graft with iliac embolization Gianturco coils and N-butyl cyaoacrylate with lipiodol Bifurcated stent graft
Straight stent graft
Elective
Elective
Elective
Elective
0/0
0/?
0/0
?/?
0/0
0/0
Elective Vs Urgent Mortality in Hospt/3 m
Aortomonoiliac stent-graft, right Urgent iliac embolization, left iliac embolization, fem-fem bypass Bifurcated stent graft Urgent
Type of tt
0/0
0/?
Failed procedure, persistent fistula Endoleak
0/0
Persistent fistula, hypertension, graft thrombosis, graft stenosis
Complications in Hopst/3 m (Procedure Related)
Approach with considerable benefits
Failed procedure
Favorable
Authors Recommendation
Abbreviations: Nbr, number; hospt, hospital; m, month; AAA, abdominal aortic aneurysm; IVC, inferior vena cava; MODS, multiple organ dysfunction syndrome; ACF, aortocaval fistula; rAAA, ruptured abdominal aortic aneurysm; M, male; F, female; NA, not applicable; VSD, ventricular septal defect; PDA, patent ductus arteriosus; fem-fem, femoral-femoral; tt, treatment; AVM, Aorto venous malformation. Note. ? ¼ data not reported by published article.
1
1
2001
Lau et al45
Nbr of Patients
Year
Author
Table 1. (continued)
6
Vascular and Endovascular Surgery
lead to unavoidable massive intraoperative blood loss.1 In semielective cases, the mortality rate approaches 30%, especially in patients with cardiovascular decompensation.1 Two cases of hybrid surgical and endovascular approach have been described, aiming to reverse the negative hemodynamic effects of the ACF before subsequent surgery or simply because the anatomy was unsuitable for total endovascular repair.50,51 Compared to the complexity of the open repair procedure and the high-surgical risk, the endovascular repair of an ACF offers a less invasive procedure, limits the hemodynamic lability during intervention, and has a less risk for major blood loss. No guidelines are available for the endovascular treatment of major AVFs, as the pathology is rare and the therapy is relatively new. Hence, we present this systematic review to try and address the cause. Our literature analysis of the outcome after endovascular repair of major AVFs showed an obliteration of the AVF in 94% of cases. In the majority of those cases, the AVF was a true ACF. Bifurcated stent grafts were mostly used, especially in the newer reports. In contrast to the high mortality of open repair, there was no perioperative mortality in the reviewed 54 patients, with the mortality at 90 days rating at 10% (4 of 38) of reported cases, half of which was not directly related to the ACF (sepsis at days 3 and 35).3,17 We note that the technical procedure was a success, and the fistula was excluded in all patients who died. Of successfully treated patients, 12% had major complications and required endovascular reintervention, all of whom had subsequent uneventful recovery. One patient died before reintervention would be possible,17 and 21% of patients had minor self-limited complications. Type 2 endovascular leak was the most frequent encountered complication. A watchful wait approach was used in all but onepatient having this complication . All monitored type 2 leaks underwent thrombosis on later follow-up. We found neither evidence nor case reports to support the theoretical concern that the AVF might persist after endovascular treatment if type 2 leak is present. Our series of cases are in favor of the opposite claim. That remaining a theoretical possibility, an early close follow-up is required to guide reintervention in the occurrence of a persistent fistula or an aneurysm in further growth. Urgent procedures resulted in nearly double the rates of complications when compared to elective ones. Patients in shock have the worst outcomes. An article published by Ghilardi et al reviewed the outcomes of patients after open surgery. It stated a decrease in mortality from 50% to 25% if patients are operated on in a stable hemodynamic state.52 This correlates with our findings, as in our series, we noticed a reduction in complications for 42% in urgently performed procedures to 26% in elective ones. Of note is the importance of a correct diagnosis of the ACF, which promotes earlier treatment in a more stable patient. Bednarkiewicz et al. reported as much as 4 of 7 patients to be misdiagnosed in a preoperative setting.53 In the presented cases, 75% of the reported patients had a fistula in the aortocaval
segment, 65% of patients had a primary aortic disease or adjacent periaortic inflammation leading to aortic and venous erosion. Those patients have seldom been previously diagnosed with aortic diseases, and thus clinical awareness of the different and elusive presentation on an ACF is of importance to treat the patient early. The classical signs of ACF are triad of abdominal pain, pulsatile abdominal mass, and machinery-like abdominal bruit. These are found only in 50% to 80% of all cases.45 Other signs and symptoms including hematuria, oliguria, high-output congestive heart failure, scrotal or lower extremity edema with or without deep vein thrombosis, abdominal pain, chest pain, low back pain, tenesmus, priapism, poor peripheral pulses, and shock have all been reported.1,54 Forty-six authors strongly recommended the endovascular treatment of ACF, while no author gave a negative opinion. All opinions stated a higher benefit for the patients on short and mid term. We have to note that no follow-up was reported beyond 24 months, with a mean follow-up merely ranging 9 months in some reported cases. This leaves no room to draw conclusions regarding the long-term efficacy of such a treatment modality. Another concern is that of a biased publication. Our aforementioned figures are drawn from published successful cases in a majority. These represent the best outcomes of the treatment modality, considering that unsuccessful procedures are less likely to be published. Larger series or randomized controlled trials are needed to solidify the above-mentioned results.
Conclusion The presentation on major AVFs is elusive most of the times, as the diagnosis might not be a straight forward one. Good knowledge of this entity renders treatment more effective and less risky. Surgical treatment has long been the only available therapy, with high mortality and morbidity. Our single case experience and our literature review make us believe that the new emerging endovascular modalities seem to offer a safer and a more efficient approach compared to traditional open repair, with excellent short- and mid-term results. Long-term results, larger series, or randomized controlled trials are a must before reaching definite conclusions regarding this treatment modality. Declaration of Conflicting Interests The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Funding The author(s) received no financial support for the research, authorship, and/or publication of this article.
References 1. Brightwell RE, Pegna V, Boyne N. Aortocaval fistula: current management strategies. ANZ J Surg. 2013;83(1-2):31-35. 2. van de Luijtgaarden KM, Bastos Gonc¸alves F, Rouwet EV, Hendriks JM, Ten Raa S, Verhagen HJ. Conservative management of
Downloaded from ves.sagepub.com at PENNSYLVANIA STATE UNIV on August 12, 2014
Nakad et al
3.
4.
5.
6.
7.
8.
9.
10.
11.
12.
13.
14.
15.
16.
17.
7
persistent aortocaval fistula after endovascular aortic repair. J Vasc Surg. 2013;58(4):1080-1083. Bernstein J, Jimenez JC. Inferior vena cava thrombosis following endovascular repair of acute aortocaval fistula: a word of caution. Vasc Endovascular Surg. 2013;47(6):467-469 Janczak D, Chabowski M, Szydelko T, Garcarek J. Endovascular exclusion of a large spontaneous aortocaval fistula in a patient with a ruptured aortic aneurysm [published online March 19, 2013]. Vascular. 2013. Shah TR, Parikh P, Borkon M, et al. Endovascular repair of contained abdominal aortic aneurysm rupture with aortocaval fistula presenting with high-output heart failure. Vasc Endovascular Surg. 2013;47(1):51-56. Elkassaby M, Alawy M, Zaki M, Hynes N, Tawfick W, Sultan S. Total endovascular management of ruptured aortocaval fistula: Technical challenges and case report [published online September 2, 2013]. Vascular. 2013. Cavalcante LP, Bernardes MV, Rocha RD, et al. Endovascular treatment of late post-traumatic aortocaval fistula: case report. J Vasc Bras (Porto Alegre). 2013;12(1):75-80. Kayser O, Scha¨fer P. Transcatheter Amplatzer vascular plugembolization of a giant postnephrectomy arteriovenous fistula combined with an aneurysm of the renal pedicle by throughand-through, arteriovenous access. Ger Med Sci. 2013;11:Doc01. Takkar C, Choi L, Mastouri N, Kadambi PV. Aortocaval fistula: a rare cause of venous hypertension and acute renal failure. Case Rep Surg. 2012;2012:487079. Sinha S, Kember P, Currie I. Emergency endovascular repair of iatrogenic aortocaval fistula: a rare complication of laparoscopic surgery. Surg Laparosc Endosc Percutan Tech. 2012; 22(3):e159-e160 Yuminaga Y, Mohabbat W, Nguyen T, Thompson AM, Fisher CM. Simultaneous endovascular repair of an iatrogenic carotidjugular fistula and a large iliocaval fistula presenting with multiorgan failure: a case report. J Med Case Rep. 2012;6:33. doi: 10. 1186/1752-1947-6-33. Rapacciuolo A, De Angelis MC, di Pietro E, et al. Percutaneous treatment of a aorto-caval fistula in a old high risk patient. BMC Surg. 2012;12(suppl 1):S32. Thet Y, Ranjit A, Ravi R, Khand A. High output cardiac failure and paradoxical pulmonary emboli secondary to aortocaval fistula. Postgrad Med J. 2012;88(1044):613-614. Nogueira C, Machado R, Vaz C, Loureiro L, Tavares J, Almeida R. Unconventional endovascular treatment of iatrogenic ilio-cava fistula. Angiol Cir Vasc(Lisboa dez). 2012;8(4):177-180. Nu´n˜ez De Arenas Baeza GF, Haurie Girelli J, Gonza´lez Herraez JV, Garcı´a Leo´n A, Gutierrez Del Manzano JA. Tratamiento endovascular de fı´stula arteriovenosa del mun˜o´n renal postnefrectomı´a con Amplatzer vascular plug II. Angiologı´a. 2011;63(3): 145-147. LaBarbera M, Nathanson D, Hui P. Percutaneous closure of aortocaval fistula using the amplatzer muscular VSD occluder. J Invasive Cardiol. 2011;23(8):343-344. Akwei S, Altaf N, Tennant W, MacSweeney S, Braithwaite B. Emergency endovascular repair of aortocaval fistula–a single center experience. Vasc Endovasc Surg. 2011;45(5):442-446.
18. von Heesen M, Sperling J, Plusczyk T, et al. Multimodal approach in coincidence of covered ruptured abdominal aortic aneurysm and aortocaval fistula. Dtsch Med Wochenschr. 2010;135(46): 2296-2299. 19. Shankarappa RK, Panneerselvam A, Dwarakaprasad R, Chikkaswamy SB, Nayak MH, Nanjappa. Novel transcatheter closure of internal iliac arteriovenous malformation. Cardiovasc Interv Ther. 2011;26(2):138-141. 20. Savastano S, Mario B, Dall’acqua J, Mansi G. A right common iliac artery pseudoaneurysm with an iliac-caval arteriovenous fistula: a rare complication of the Recovery vena cava filter. Cardiovasc Intervent Radiol. 2010;33(3):667-669. 21. Guzzardi G, Fossaceca R, Divenuto I, Musiani A, Brustia P, Carriero A. Endovascular treatment of ruptured abdominal aortic aneurysm with aortocaval fistula. Cardiovasc Intervent Radiol. 2010;33(4): 853-856. 22. Juszkat R, Pukacki F, Zarzecka A, Kulesza J, Majewski W. Endovascular treatment of ruptured abdominal aneurysm into the inferior vena cava in patient after stent graft placement. Cardiovasc Intervent Radiol. 2009;32(4):776-780. 23. Janczak D, Pupka A, Garcarek J, Szyber P. The use of politetrafluoroethylene stent-graft and vena cava filter in the endovascular treatment of ruptured abdominal aortic aneurysm with aortocaval fistula. Polim Med. 2009;39(3):3-8. 24. Du¨z B, Kaplan M, Gu¨nay C, Ustu¨nso¨z B, Ug˘urel MS. Iliocaval arteriovenous fistula following lumbar disc surgery: endovascular treatment with a stentgraft. Turk Neurosurg. 2008; 18(3):245-248. 25. Fujisawa Y, Kurimoto Y, Morishita K, et al. Aortocaval fistula after endovascular stent-grafting of abdominal aortic aneurysm. J Cardiovasc Surg (Torino). 2009;50(3):387-389. 26. Cholenahalli NM, Prabhavathi, Kikkeri HS, et al. Iatrogenic iliac arteriovenous fistula following lumbar disc surgery. Post Kardiol Interw. 2008;4, 1(11):40-42. 27. Kwon SH, Oh JH, Park SJ, Park HC. Endovascular repair of a spontaneous right common iliac artery: inferior vena cava fistula due to infrarenal aortoiliac aneurysm. Vasc Endovascular Surg. 2008;42(3):279-283. 28. Mitchell ME, McDaniel HB, Rushton FW. Endovascular repair of a chronic aortocaval fistula using a thoracic aortic endoprosthesis. Ann Vasc Surg. 2009;23(1):150-152. 29. Clevert DA, Stickel M, Flach P, et al. Contrast-enhanced ultrasound in detection and follow-up of an infrarenal abdominal aortic aneurysm with aorto-caval fistula and endovascular treatment. Cardiovasc Intervent Radiol. 2007;30(3):480-484. 30. Taneja M, Lath N, Soo TB, et al. Renal artery stump to inferior vena cava fistula: unusual clinical presentation and transcatheter embolization with the Amplatzer vascular plug. Cardiovascular Interv Radiol. 2008;31(2 suppl):92-95. 31. Leon LR, Arslan B, Ley E, Labropoulos N. Endovascular therapy of spontaneous aortocaval fistulae associated with abdominal aortic aneurysms. Vascular. 2007;15(1):35-40. 32. Ascoli Marchetti A, Gandini R, Ippoliti A, et al. The endovascular management of open aortic surgery complications with emergency stentgraft repair in high-risk patients. J Cardiovasc Surg (Torino). 2007;48(3):315-321.
Downloaded from ves.sagepub.com at PENNSYLVANIA STATE UNIV on August 12, 2014
8
Vascular and Endovascular Surgery
33. Pathak S, Yusuf SW, Doyle TN, Francis IA, Hurst PA, Davidson C. Endovascular repair of a recurrent aortocaval fistula and astomotic false aneurysm. Br J Radiol. 2006;79(944):e62-e63. 34. Kopp R, Weidenhagen R, Hoffmann R, et al. Immediate endovascular treatment of an aortoiliac aneurysm ruptured into the inferior vena cava. Ann Vasc Surg. 2006;20(4):525-528. 35. Hetzel G, Gabriel P, Rompel O, Ritter W, Raithel D. Aortocaval fistula after stent-graft repair. J Endovasc Ther. 2006;13(1):117-120. 36. Vetrhus M, McWilliams R, Tan CK, Brennan J, Gilling-Smith G, Harris PL. Endovascular repair of abdominal aortic aneurysms with aortocaval fistula. Eur J Vasc Endovasc Surg. 2005;30(6): 640-643. 37. Waldrop JL, Dart BW, Barker DE. Endovascular stent graft treatment of a traumatic aortocaval fistula. Ann Vasc Surg. 2005; 19(4):562-565. 38. Ferrari M, Berchiolli R, Sardella SG, et al. Endovascular repair of an aorto–left renal vein fistula due to a ruptured abdominal aortic aneurysm after EVAR. J Endovasc Ther. 2005;12(4):512-505. 39. Shaheen RM, Kibbe MR, Eskandari MK. Endoluminal repair of an acute aortoleft renal vein fistula. Surgery. 2005;138(1):109-110. 40. Burke C, Mauro MA. SIR 2003 film panel case 8: aortocaval fistula supplied by a type II endoleak. J Vasc Interv Radiol. 2003; 14(6):813-817. 41. Laureys M, Tannouri F, Rommens J, Dussaussois L, Golzarian J. Percutaneous treatment of iatrogenic iliocaval fistula related to endograft placement for abdominal aortic aneurysm. J Vasc Interv Radiol. 2002;13(2 pt 1):211-213. 42. Williamson AE, Annunziata G, Cone LA, Smith J. Endovascular repair of a ruptured abdominal aortic and liac artery aneurysm with an acute iliocaval fistula secondary to lymphoma. Ann Vasc Surg. 2002;16(2):145-149. 43. Duxbury MS, Wells IP, Roobottom C, Marshall A, Lambert AW. Endovascular repair of spontaneous non-aneurysmal aortocaval fistula. Eur J Vasc Endovasc Surg. 2002;24(3):276-278. 44. Gandini R, Ippoliti A, Pampana E, Ascoli Marchetti A, Raimondo Pistolese G, Simonetti G. Emergency endograft placement for
45.
46.
47.
48.
49.
50.
51.
52.
53.
54.
recurrent aortocaval fistula after conventional AAA repair. J Endovasc Ther. 2002;9(2):208-211. Lau LL, O’Reilly MJ, Johnston LC, Lee B. Endovascular stentgraft repair of primary aortocaval fistula with an abdominal aortoiliac aneurysm. J Vasc Surg. 2001;33(2):425-428. Umscheid T, Stelter WJ. Endovascular treatment of an aortic aneurysm ruptured into the inferior vena cava. J Endovasc Ther. 2000;7(1):31-35. Sultan S, Madhavan P, Colgan MP, et al. Aorto–left renal vein fistula: is there a place for endovascular management? J Endovasc Surg. 1999;6(4):375-377. Beveridge CJ, Pleass HC, Chamberlain J, Wyatt MG, Rose JD. Aortoiliac aneurysm with arteriocaval fistula treated by a bifurcated endovascular stent-graft. Cardiovasc Intervent Radiol. 1998;21(3):244-246. Cekirge S, Oguzkurt L, Saatc¸i I, Boyvat F, Balkanci F. Embolization of a high-output postnephrectomy aortocaval fistula with Gianturco coils and cyanoacrylate. Cardiovasc Intervent Radiol. 1996;19(1):56-58. Raux M, Cochennec F, Kobeiter H, Bruguie`re E, Becquemin JP. Images in cardiovascular medicine: high-output heart failure. Circulation. 2010;121(16):e386-e387. Siepe M, Koeppe S, Euringer W, Schlensak C. Aorto-caval fistula from acute rupture of an abdominal aortic aneurysm treated with a hybrid approach. J Vasc Surg. 2009;49(6):1574-1576. Ghilardi G, Scorza R, Bortolani E, De Monti M, Longhi F, Ruberti U. Rupture of abdominal aortic aneurysms into the major abdominal veins. J Cardiovasc Surg (Torino). 1993;34(1):39-47. Bednarkiewicz M, Pretre R, Kalangos A, Khatchatourian G, Bruschweiler I, Faidutti B. Aortocaval fistula associated with abdominal aortic aneurysm: a diagnostic challenge. Ann Vasc Surg. 1997;11(5):464-466. Davidovic L, Dragas M, Cvetkovic S, Kostic D, Cinara I, Banzic I. Twenty years of experience in the treatment of spontaneous aorto-venous fistulas in a developing country. World J Surg. 2011;35(8):1829-1834.
Downloaded from ves.sagepub.com at PENNSYLVANIA STATE UNIV on August 12, 2014
