ARTICLE IN PRESS doi:10.1510/icvts.2008.200386
Interactive CardioVascular and Thoracic Surgery 8 (2009) 654–660 www.icvts.org
ESCVS article - Vascular general
External iliac artery pseudoaneurysm complicating renal transplantation夞 Umberto M. Bracalea,*, Francesca Carbonea, Luca del Guercioa, Daniela Violaa, Francesco P. D’Armientob, Simone Maureac, Massimo Porcellinia, Giancarlo Bracalea Department of Vascular and Endovascular Surgery, University Federico II, via Pansini 5, 80131 Naples, Italy b Department of Pathology, University Federico II, Naples, Italy c Department of Radiology, University Federico II, Naples, Italy
a
Received 12 December 2008; received in revised form 20 February 2009; accepted 24 February 2009
Abstract Objective: To assess the etiology, management and outcome of iliac pseudoaneurysms following renal transplantation. Methods: Eleven patients who underwent repair between 1982 and 2007 were identified. Five (Group 1) presented pseudoaneurysm at the anastomosis of the donor renal and native iliac arteries, and six (Group 2) presented iliac pseudoaneurysm following transplant nephrectomy. Intraoperative cultures and immunohistochemical examinations were obtained from all surgical cases to determine the existence of a relationship between infection or transplant rejection and pseudoaneurysm formation. Results: Endovascular repair (EVR) was used to treat three patients, while eight patients underwent open repair (OR). Transplant nephrectomy was needed in all cases but one after anastomotic pseudoaneurysm repair. After pseudoaneurysm excision, arterial reconstruction was performed in all cases, with a limb salvage rate of 100%. At 30 days, no patients died in the EVR subgroup. In the OR subgroup, one patient died of sepsis (12.5%). Cultures taken from the pseudoaneurysm wall and content grew Candida albicans and E. coli in two febrile patients. Pathologic evaluation of donor renal arteries revealed evidence of chronic rejection in three patients (60%) in Group 1, and in two (33.3%) in Group 2. No patients in either Group presented late infection, failure of vascular reconstruction nor pseudoaneurysm recurrence. The follow-up ranges from 20 to 89 months. Conclusions: The etiology of pseudoaneurysms in this location is multifactorial, however, an association with chronic rejection must be considered. Though rare, the development of pseudoaneurysms at the donor renal-external iliac artery anastomosis results in high rates of transplant nephrectomy. Less invasive endovascular techniques offer a new therapeutic option in this challenging scenario notwithstanding the fact that they require further validation. 䊚 2009 Published by European Association for Cardio-Thoracic Surgery. All rights reserved. Keywords: Iliac artery; Pseudoaneurysm; Renal allograft; Endovascular repair; Open repair
1. Introduction External iliac artery pseudoaneurysms following renal transplantation are uncommon, with an incidence rate of -1% w1, 2x. Of these, most are complications of allograft nephrectomy w3x, with no apparent significant differences in occurrence between the extra-capsular and intra-capsular techniques w4x. Due to the few small series of patients and isolated case reports described in current literature, the occurrence and treatment of this potentially life-threatening complication, its etiology, indications for repair, management options and prognosis remain very controversial. A defective suture technique w5x or arterial dehiscence caused by local infection w6x certainly plays a role in iliac pseudoaneurysm formation in renal transplant patients, while immunogenic factors such chronic rejection, which has been hypothesized w7, 8x have yet to be proven. These 夞 Presented at the 57th International Congress of the European Society for Cardiovascular Surgery, Barcelona, Spain, April 24–27, 2008. *Corresponding author. Tel.: q39(0)817462629; fax: q39(0)817464732. E-mail address:
[email protected] (U.M. Bracale). 䊚 2009 Published by European Association for Cardio-Thoracic Surgery
pseudoaneurysms are usually asymptomatic yet can cause fever and anemia w9x, compression of adjacent structures w10x, renal dysfunction and graft loss w1x, or even precipitate a life-threatening hemorrhage due to acute rupture w3, 7, 8, 10, 11x. Therapeutic options include conventional open repair (OR) w7, 10x, endovascular repair (EVR) w8, 12– 14x, and more recently, ultrasound-guided percutaneous thrombin injection w15x (USG-PT). Herein we will report on our personal experience with 11 pseudoaneurysm patients in order to assess the causes, indications for repair, and the early and mid-term results of OR and EVR performed for the treatment of this challenging complication of renal transplantation. 2. Materials and methods A 25-year (1982–2007) retrospective review was carried out of all patients admitted to our institution with a diagnosis of external iliac artery pseudoaneurysm after kidney transplantation. These patients were referred to us from several Italian transplant centers. Patient data collected were demographics, date of transplant, rejection episodes, date and surgical nephrectomy
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technique, date of pseudoaneurysm diagnosis, pseudoaneurysm site and size, type of anesthesia, postoperative length of stay (LOS), perioperative mortality and morbidity, survival outcome, and cause of death. In the last 12 years endovascular treatment was offered to all anatomically suitable patients. Intraoperative cultures of the vascular bed and samples of the pseudoaneurysm and donor renal artery were obtained from all surgical cases. Sections were embedded in paraffin and stained with either hematoxylin and eosin (H and E), and a combination of Masson’s trichrome and Weigert’s elastic stain. Because immunohistochemical examination was not feasible at that time, paraffin blocks were collected over a 25-year study period, and additional transverse sections were recently obtained and stained immunohistochemically (PAP-method), using the following cell type-specific antibodies: CD20 for B lymphocytes, CD3 for T lymphocytes, CD4 for T helper and CD8 for T suppressor lymphocytes (Dako, Glostrup, Denmark). Patients in both groups were followed by clinical investigation and Duplex scan at 1, 6, and 12 months, and annually thereafter for three years. Three patients in the Group 1 and two in the Group 2 were subsequently lost to followup. The latter three patients in the Group 2 are still followed-up at the time of this review. 3. Results Eleven patients who had an external iliac artery pseudoaneurysm complicating renal transplantation were identified. Of these, five patients (45.4%; 3 men) developed a pseudoaneurysm at the anastomotic site (Group 1; Table 1) and the remaining six (54.6%; 4 men) following transplant nephrectomy (five extracapsular, one intracapsular) (Group 2; Table 2). The mean patient age was 47.8 years (range
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39–67 years) in Group 1 and 44.7 years (range 28–61 years) in Group 2. Ten patients had received their renal transplant from a cadaver, and one from a living donor. The mean time lapse between the renal transplantation or graftectomy and pseudoaneurysm diagnosis was 14.1 months (range 78 days–49 months) and 9.6 months (range 13 days–37 months), respectively. Standard immunosuppression had been administered in the Group 1 patients; while in Group 2 patients immunosuppressive medication had been discontinued following nephrectomy. No differences were observed in patient demographics, comorbidity, risk factors nor ASA grade between Groups 1 and 2, nor between subgroups OR and EVR. Two patients were asymptomatic, and the pseudoaneurysm was diagnosed in a routine duplex ultrasound examination; seven patients were admitted for a pulsatile or tender mass in iliac fossa and local compression symptoms, two had fever, and the remaining two patients presented a ruptured pseudoaneurysm. Arteriography and computed tomography (CT) scans were obtained in most patients early in the study period whereas computed tomography angiography (CTA) (Fig. 1) and magnetic resonance angiography (MRA) (Fig. 2) were used alone in the latter part of the study. Within the last years of the study, a conventional angiography was carried out on only the three patients who had undergone interventional procedures. Pseudoaneurysm diameter was similar between Groups 1 and 2 (mean, 7.1 cm vs. 5.9 cm) and between the OR and EVR subgroups (mean, 6.8 cm vs. 5.5 cm). During the operations it was revealed that pseudoaneurysms following an extracapsular transplant nephrectomy was an extension of the donor renal artery stump. In the patient who had undergone an intracapsular allograft removal, the pseudoaneurysm was secondary to a vein patch repair disruption owing to infection.
Table 1 Clinical data of patients with pseudoaneurysm following renal transplantation (Group 1) Pt Age no. (years)y sex
Interval between Rejection Clinical Tx and diagnosis of presentation pseudoaneurysm
1
43yMale
7 months
2
39yFemale 49 months
None
3
40yFemale 78 days
None
4
67yMale
5 months
Chronic
5
50yMale
7 months
Chronic
Chronic
Local discomfort, pulsatile mass Asymptomatic
Treatmentydate
Excision, polyester interposition graft, Tn (1982) Excision, polyester interposition graft, hypogastric artery autotransplantation (1987) Fever, local Excision, PTFE pain, tender crossover femoralmass femoral graft, Tn (1992) Sudden Stent-grafting abdominal pain, (Hemobahn*, hypotension 8 mm=5 cm) DrainageyTn (5 days later) (1999) Anemia, Excision, silver local pain, coated collagen tender mass polyester† interposition graft, Tn (2005)
Intraoperative Major culture complications
LOS (day) Outcome
Negative
11
Alive: 61 months Contralateral Tx
Negative
9
Alive: 39 months
Candida albicans
Pneumonia
13
Alive: 43 months Contralateral Tx
Negative
Wound infection and dehiscence
18
Died: MI (27 months) Contralateral Tx
Negative
Iliac fossa abscess 10 and wound infection sepsis
Died: MOF (10 days)
Pt, patient; Tx, transplant; Tn, transplant nephrectomy; MOF, multiple organ failure; MI, myocardial infarction; *W.L. Gore and Associates, Flagstaff, Arizona; InterGard Silver prosthesis (Datascope InterVascular, La Ciotat, France).
†
54yFemale
28yMale
46yMale
48yMale
31yFemale
61yMale
1
2
3
4
5
6
Acute rejection, sepsis
Chronic rejection
Arterial thrombosis
Acute rejection
Vein thrombosis
Chronic rejection
Indication for Tn
Intracapsular
Extracapsular
Extracapsular
Extracapsular
Extracapsular
Extracapsular
Surgical technique
13 days
5 months
6 months
71 days
7 months
37 months
Interval between Tn and diagnosis of pseudoaneurysm
Fever, sudden abdominal pain, hypotension
Local pain, pulsatile mass
Fever, anemia, local pain and tender mass
Local discomfort, pulsatile mass
Asymptomatic
Local pain, pulsatile mass
Clinical presentation Excision, polyester interposition graft (1983) Excision, polyester interposition graft (1989) Stent-grafting (Passager*) (1997) Excision, silver collagen coated polyester graft (2001) Stent-grafting (Hemobahn**) (2004) Excision, silver collagen coated polyester† crossover femoral-femoral graft (2007)
Treatmentydate
12
Wound infection
E. coli
10
3
11
9
LOS (day)
2
Bleeding stress ulcer
Major complications
Negative
Negative
Negative
Negative
Negative
Intraoperative culture
Pt, patient; Tn, transplant nephrectomy; *Meadox, Oakland, NJ; **W. L. Gore and Associates, Flagstaff, Arizona; †InterGard Silver prosthesis (Datascope InterVascular, La Ciotat, France.
Age (years)y sex
Pt no.
Alive (9 months)
Alive (31 months) Contralateral Tx
Alive (57 months) Contralateral Tx
Alive (35 months) Contralateral Tx
Alive (41 months) Contralateral Tx
Died: cerebrovascular hemorrhage (75 months)
Outcome
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Table 2 Clinical information of patients with pseudoaneurysm following transplant nephrectomy (Group 2)
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Fig. 2. MRA showing a pseudoaneurysm at the anastomosis between the renal artery and the right external iliac artery. There is no contrast enhancement of the transplant kidney (arrows).
Fig. 1. CTA showing a 12=8 cm large extrarenal pseudoaneurysm at the transplant anastomotic site.
After the pseudoaneurysm excision, six patients underwent arterial reconstruction with an interposition graft to restore inflow into the lower limb. Following proximal and distal ligation of the external iliac artery, a femoral-femoral bypass was performed in another two high-grade fever patients with arterial anastomotic disruption and evidence of local infection. General anesthesia was used in five patients and epidural anesthesia in three.
In the last 12 years, three pseudoaneurysms (1 in Group 1, 2 in Group 2) were treated with a stent-graft deployment. Passager grafts (Meadox, Oakland, NJ) were placed in two patients, and Hemobahn graft (W.L. Gore and Associates, Flagstaff, AZ) in one. The procedures were performed via an ipsilateral femoral cut down under local anesthesia; the covered stents used were 8–10 mm in diameter and 50 or 60 mm in length. In one patient, two endoprostheses were implanted to exclude a pseudoaneurysm complicating extracapsular transplant nephrectomy, which was most likely caused by a clip falling off the donor renal artery stump (Fig. 3). Another patient underwent a two-stage procedure for treatment of a ruptured pseudoaneurysm, including stentgrafting followed by delayed surgical drainage of the hematoma and transplant nephrectomy.
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Fig. 3. Angiogram before (a) and after stent-graft implantation (b) of an external iliac artery false aneurysm following extracapsular transplant nephrectomy. Dislodgment of a metal clip at level of the donor renal artery stump is visualized.
In four other Group 1 patients submitted to OR, the allograft had to be removed while a pseudoaneurysm excision followed by an allograft autotransplantation at the level of the internal iliac artery was performed in only one patient. The mean postoperative LOS for patients who underwent a one-stage procedure was 10.7 days (range 9–13 days) in Group 1 and 7.8 days (range 2–12 days) in Group 2 with the LOS being briefer in the EVR subgroup than the OR subgroup (2.5 days vs. 10.6 days). The LOS for the last patient in Group 1 who received a two-stage procedure was 18 days due to a wound infection and dehiscence complicating transplant nephrectomy. Postoperative complications occurred in three patients in Group 1 and in two patients in Group 2 (Tables 1 and 2) leading to a morbidity rate of 60% and 33.3%, respectively. All the complications occurred in the OR subgroup (50%) while no complications resulted in the EVR subgroup. None of the patients suffered limb loss. One patient in Group 1 died of sepsis 10 days after OR, and no death occurred in Group 2 and in the EVR subgroup. Intraoperative cultures of the vascular bed showed the presence of Candida albicans and E. coli in two febrile patients. Pathologic evaluation of the pseudoaneurysm specimens revealed marked fibrosis and varying degrees of fragmentation of elastic fibers. Out of the samples from donor renal arteries, three from the Group 1 patients (No. 1, 4, 5) and two from Group 2 patients (No. 2, 4) had histologic evidence of chronic rejection, with complete loss of endothelial cells, disruption of elastic fibers and fibrosis, endoluminal thrombosis, and immunohistochemical positive reaction with CD4 (Fig. 4). The mean follow-up was 42.5 months (range 27–61 months) in Group 1 and 50.3 months (range 20–89 months) in Group 2. During the follow-up, three patients in Group 1 and four in Group 2 underwent a second renal transplantation while one patient in each group remained in a regular hemodialysis program. No patient presented late infection or occlusion of arterial reconstruction nor pseudoaneurysm recurrence. Although two late deaths (1 in Group 1, 1 in Group 2) occurred during the follow-up period, none were related to the previous surgical or interventional procedures.
Fig. 4. Immunohistochemical stain for CD4 (T-cell), 250=. Photomicrograph of donor renal artery demonstrating diffuse CD4q T-cell infiltration.
4. Discussion To date, no large series are available to define the etiology, natural history, management and outcome of this rare complication. To our knowledge, this study is the first to compare transplant patients who underwent surgical or endovascular treatment for both iliac anastomotic pseudoaneurysm and pseudoaneurysm following transplant nephrectomy. Moreover, immunohistochemical study of pseudoaneurysm and of donor renal artery specimens collected over the time-period was conducted in order to evaluate the role of the rejection process in the pathogenesis of pseudoaneurysms. Although intrarenal small aneurysms are reported in association with acute or chronic rejection, no experimental nor clinical data have suggested an immunological cause for extrarenal aneurysms in transplant patients. Our series shows evidence of chronic rejection, with presence of CD4 T-cell mediated rejection response, at level of donor renal artery in three patients presenting anastomotic pseudoaneurysm at an average interval of 6.3 months, and at level of renal artery stump in two presenting pseudoaneurysm at a median of 6.5 months after an extracapsular transplant nephrectomy. The indication for urgent graft removal in these two patients was the early occlusion of renal vessels while immunosuppression was progressively withdrawn upon the return of the patients to dialysis. These data are similar to these shown of the clinical use of arterial allografts for limb salvage w16x or aortic aneurysm repair, as well as in the treatment of prosthetic graft infection w17x, with frequent aneurysmal degeneration because of immunologic rejection. On the contrary, no allograft degradation was found in transplanted patients receiving immunosuppressive treatment w18x. The indications for pseudoaneurysm repair and treatment modalities are at present subject to debate. In the absence of infection, asymptomatic small pseudoaneurysm can be managed conservatively with regular monitoring w2x, while recent reports advocate that pseudoaneurysm presenting symptoms w10x with a size of 2.5 cm, and progressive enlargement and rupture need to
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be treated w7x. However, in one patient a mycotic aneurysm was treated conservatively with no complications during a 38-month follow-up w19x. Due to the presence of symptoms and pseudoaneurysms of a large diameter, all eleven of our transplanted patients underwent surgical or EVR of pseudoaneurysms and no patient was treated conservatively. Another point to be mentioned is the need of nephrectomy in the majority of renal transplant patients affected with anastomotic pseudoaneurysm due to resistant rejection, function failure or infection. When not required, surgical resection with patch angioplasty w20x or reanastomosis w21x could save the allograft. Conversely, an interposition graft or extra-anatomic reconstruction following pseudoaneurysm excision leads to graft loss w3x, unless a kidney autotransplantation when feasible. During the surgical repair of an extrarenal pseudoaneurysm at the anastomotic site, all except one of our patients required a transplant nephrectomy due to irreversible rejection (2) or local infection (1), while the one patient received an allograft autotransplantation to maintain stable renal function. At present, questions remain regarding the need of concomitant vascular reconstruction after surgical pseudoaneurysm excision. Eng et al. w3x reported no limb loss following external iliac artery ligation, while three out of 14 cases of the series of Gorey et al. w22x required subsequent elective reconstruction for claudication. Furthermore, an above-knee amputation was reported in a 25year-old woman who developed foot ischemia three months after external iliac artery ligation w2x. In the case of critical leg ischemia following transplant nephrectomy with suspected local infection, an antibiotic impregnated prosthetic graft was preferred by Eng et al. w3x using an extra-anatomical route. Two febrile patients out of our study were infected and received simultaneous artery ligation and crossover femoral-femoral graft w6x using a polytetrafluoroethylene (PTFE) and a silver-coated polyester prosthesis, respectively. In the additional six patients who had no clinical suspicion of infection, we performed an interposition polyester grafting after pseudoaneurysm excision. Of particular interest was the fact that all seven of our prosthetic grafts remained patent during an average followup of 52.5 months, with no evidence of stenosis, infection or pseudoaneurysm recurrence. As a result, we can recommend distal revascularization following aneurysmectomy. During the past decade, EVR has evolved into the treatment of choice for both external iliac anastomotic pseudoaneurysm, with renal artery exclusion and subsequent transplant loss, and pseudoaneurysm following transplant nephrectomy w8, 11–13x. The procedure can be considered a valuable therapeutic option even in emergency situations w14x; adjunctive percutaneous drainage of retroperitoneal blood collection w12x or combined open surgical drainage and transplant nephrectomy may be required once a patient’s condition is stabilized, as was the case in one of our patients presenting a ruptured iliac pseudoaneurysm who had undergone a successful two-stage procedure.
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In contrast, Eng et al. w3x performed emergency surgical control of hemorrhage and simultaneous allograft nephrectomy in two patients with ruptured anastomotic pseudoaneurysms. One of the patients (50%) died from a secondary hemorrhage originating from the infected vascular stump. A successful placement of covered stents has also been reported for the treatment of pseudoaneurysms due to bacterial or fungal infection w13, 23x, but Liapis et al. w24x described a Palmaz stent infection requiring open pseudoaneurysm excision and stent removal in an immunocompromised patient. During the last 12 years, we have performed stent-grafting in three renal transplant patients to exclude a pseudoaneurysm, but did not do so in febrile patients so as to minimize the risk of stent-graft infection. In our series, there were no post-EVR complications, no death at 30 days and the LOS (2.5 days vs. 10.6 days) was shorter. More recently, successful USG-PT was described in the treatment of a large anastomotic pseudoaneurysm after failure of kidney transplant w15x. A combined USG-PT and covered stent placement across an end-to-end renal-tointernal iliac artery anastomosis was also used for the successful exclusion of a pseudoaneurysm. An adjunctive balloon dilatation of the branches of the transplant artery improved the intrarenal flow while preserving the kidney w23, 25x. The present study has found differences in 30-day results between Group 1 and Group 2 patients undergoing repair of a pseudoaneurysm. The incidence of postoperative complications was higher in patients who had anastomotic pseudoaneurysm repair, compared with those who received treatment for a pseudoaneurysm following transplant nephrectomy. In addition, the LOS tends to be longer in Group 1 than in Group 2 (10.7 days vs. 5.9 days, respectively). The difference in early outcome could partly be explained by the coexistence of kidney rejection and immunosuppression causing a greater risk of infection and inadequate response to stress. The combined transplant nephrectomy could have contributed to the high morbidity and mortality rate of our Group 1 patients while it is unlikely that the difference in pseudoaneurysm size (7.1 cm vs. 5.9 cm) has influenced the outcome of the repair. Infection was the main cause of postoperative complications in our surgical patients and one patient died of sepsis. This study is limited by its retrospective nature and the small group of 11 patients. Another potential limitation is that we included patients with both iliac anastomotic pseudoaneurysm in transplant patients and pseudoaneurysm following transplant nephrectomy. In addition, treatment options were substantially different during the second half of the study period. Therefore, long-term follow-up is not available. In light of these limitations, our findings suggest that chronic rejection of donor renal artery may play a role in the development of 45% of the observed cases of pseudoaneurysms complicating kidney transplantation in our study. Though rare, the development of pseudoaneurysms at the donor renal-external iliac artery anastomosis results in high rates of transplant nephrectomy. The choice of OR or EVR in these pseudoaneurysms has yet to be fully delineated;
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