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Department of Surgery, Division of HPB and Transplant Surgery, Erasmus MC, University Medical Center Rotterdam, Rotterdam, The NetherlandsKidney and Pancreas Transplantation Unit, Padua University Hospital, Padua, Italy
Correspondence to: Department of Surgery, Division of HPB & Transplant Surgery, Erasmus MC, University Medical Centre Rotterdam, Dr. Molewaterplein 40, 3015 GD Rotterdam, The Netherlands
Department of Surgery, Division of HPB and Transplant Surgery, Erasmus MC, University Medical Center Rotterdam, Rotterdam, The NetherlandsDepartment of Gastroenterological Surgery, Okayama University Graduate School of Medicine, Dentistry, and Pharmaceutical Sciences, Okayama, Japan
Renal artery aneurysm (RAA) is a rare vascular disease. Kidney autotransplantation (KAT) is the treatment option when endovascular approach is not available. However, the evidence on KAT for RAA is mostly limited to small case series or reports. Here, we describe our 2 center experience of KAT for RAA, and provide the results of our systematic literature review to evaluate the outcomes.
Methods
A retrospective 2 center study was conducted in patients undergoing KAT for RAA between 2010 and 2018. Moreover, a systematic review was performed on medical databases to evaluate the outcomes of KAT for RAA.
Results
Nine patients were surgically treated at our institutions: eight with laparoscopic nephrectomy (LN), and 1 with open followed heterotopic KAT. All RAAs were ex-vivo reconstructed, and in 3 cases a vein graft was used for reconstruction. There were 2 postoperative major complications including 1 graft loss. In the systematic review, 102 studies with 355 patients were included. In 35 patients (9.9%) a minimal invasive approach was performed. The incidence of postoperative major complications and graft loss was 9.4% and 4.1%.
Conclusions
Our experiences showed that laparoscopic approach for nephrectomy followed heterotopic KAT was feasible with good postoperative outcomes. KAT is an effective treatment for RAA when endovascular approach is not feasible for interpretation of the outcomes, the quality and sample size of the evidence should be taken into consideration.
Renal artery aneurysm (RAA) is a rare vascular disease with an incidence of 0.1% in general population and a rate between 0.3% and 2.5% reported by angiographic and computed tomography studies.
Typically, RAA presents in women, in the sixth decade and afflicts more right sided kidneys rather than the left side probably due to high incidence of fibromuscular dysplasia.
Indications for treatment of RAA include diameter > 2 cm, female gender within childbearing age, symptoms as pain, hematuria, hypertension refractory to medications, renal artery stenosis, thromboembolism, dissection or rupture that occurs in 2-5% of known aneurysms.
Endovascular approaches, including coil embolization, balloon-assisted coil embolization, and stent grafting, in selected cases are effective with successful rates of 73% to 100% reported in large series with variable rates of morbidity (13–60%).
Surgical approaches for RAA, reserved for more complex lesions, include in-situ repair, and ex-vivo reconstruction with kidney autotransplantation (KAT).
The first report of KAT was in 1961 performed by Shackman and Dempster due to a unilateral renal artery stenosis and 1 year later Hardy et al. performed the first KAT for a ureteral injury.
Afterwards the adoption of these techniques has increased with recently application of minimal invasive approach. The postoperative hospital stay, pain and time to return to full function decreased with the introduction of laparoscopy in living donor nephrectomy.
The first experience of laparoscopic KAT series for RAA was reported by Gallagher et al. in 2008: seven patients with RAA treated with laparoscopic nephrectomy (LN), ex-vivo repair and KAT using the same Gibson incision for kidney extraction in the iliac fossa.
Nevertheless, the current literatures are limited to case reports or small case series with lacking data in terms of outcomes and strategy concerning RAA treatment in large numbers. Furthermore, previous reviews on KAT have reported all different indications without any strict focus on RAA treatment, long-term outcomes or comparison between open and minimal invasive surgical approach.
Here, we describe our 2 center experience of KAT for RAA, and provide the results of our systematic review to evaluate the outcomes of KAT for RAA.
METHODS
Study Design
A retrospective 2-center study was conducted in patients undergoing KAT for RAA at the Erasmus MC, Rotterdam, The Netherlands, and the Padua University Hospital, Padua, Italy, between January 2010 and December 2018. This study was approved by the Ethics Committee of the Erasmus MC, and written informed consent for this study was obtained from all patients at the Padua University Hospital. The present study was conducted in accordance with the tenets of the Declaration of Helsinki.
Clinical Data
The following demographic and clinical data of patients were collected: age, gender, comorbidity, symptom, the location of aneurysm, aneurysm diameter and morphology, the type of nephrectomy (laparoscopic or open), type of reconstruction, number of artery branches reconstructed, operative time, blood loss, postoperative complication (evaluated according to the Clavien-Dindo classification
), postoperative hospital stay, perioperative creatinine level, and graft survival. Postoperative major complication was defined as the Clavien-Dindo classification with grade III and IV. Graft loss was defined as graft failure with or without nephrectomy, or death. Graft survival was as time from KAT to last follow-up with normal kidney function. All patients were routinely monitored by laboratory values such as serum creatinine and estimated glomerular filtration rate. If anomalies were found, ultrasound and computed tomography imaging were performed.
Surgical Technique
Patients from the Erasmus MC and the Padua University Hospital were treated with similar laparoscopic approach for nephrectomy, as described previously.
In brief during LN, the colon was mobilized and the renal capsule was opened using an ultrasonic device. After identification and dissection of the ureter, the renal artery, and the renal vein, a Pfannenstiel incision was made. The ureter was clipped distally and divided. The renal artery and vein were divided using an endoscopic stapler (EndoGia, US Surgical, Norwalk, USA). The kidney was placed in an endobag and extracted through the Pfannenstiel incision. Afterwards, the kidney was flushed with UW and preserved in static cold storage.
Regarding the ex-vivo aneurysm repair, the first option was an end-to-end anastomosis after resecting the aneurysm. Other options included the use of a venous patch or vein graft after the aneurysmectomy. Kidney implantation was performed in a heterotopic fashion as a standard kidney allotransplantation: through the same kidney extraction incision. The kidney was placed in iliac fossa and vascular anastomosis with iliac vessel was performed. The renal vein was connected to external iliac vein in an end to side fashion (with Prolene 5-0 running suture) and, renal artery was connected to external iliac artery or internal iliac artery respectively in an end-to-side or end-to-end anastomosis (with Prolene 6-0 running suture). Ureteroneocystostomy was arranged with Lich-Gregoir technique with a double J catheter formerly inserted and removed after 4 weeks. One case was treated with open approach, throughout a midline incision.
A SYSTEMATIC LITERATURE REVIEW
Registration
No ethical approval or informed consent statement was required for this review article. The research registration unique identifying number for our research is UMIN000039450.
Search Strategy
The present study was reported in accordance with the Preferred Reporting Items for Systematic Reviewers and Meta-Analyses (PRISMA) guidelines.
A systematic literature search of Embase, Medline Ovid, Web of science, Cochrane CENTRAL, and Google scholar was conducted on the May 13, 2019 using the key words of kidney autotransplantation and renal artery aneurysm (see Supplementary Table 1). The search was conducted without any limitations regarding languages and the year of publication.
Inclusion and Exclusion Criteria
The present study included articles reporting data, operative findings and outcomes in patients undergoing KAT for RAA. In cases when multiple studies were published from the same institution, only the study including largest sample sizes with available data was included. Review articles, articles without sufficient data, conference abstracts, comments and animal studies were excluded.
Data Extraction
After removing duplicate records, abstracts were screened independently by 2 investigators (EC and KT) determining papers eligibility for analysis. The full-text articles were subsequently screened to meet the criteria for review. The extracted data included year of study publication, number of cases, patient information (age, gender, symptoms, comorbidity, presence of solitary kidney), operative findings (location, morphology, diameter, etiology of the aneurysm, number of renal branches reconstructed, prior endovascular treatment, nephrectomy and implantation approach, operative time, blood loss, ischemia time, and type of reconstruction) and outcomes (postoperative complications, graft loss, and postoperative hospital stay).
Quality Assessment
The methodological quality and synthesis of case series and case reports were used to evaluate the quality of the included studies.
Data are presented as mean with standard deviation and median with the interquartile range (IQR) for continuous variables. The outcomes between open and LN were compared. Categorical data are represented as proportions. Differences between groups were examined by Fisher's exact test or Chi-square test for categorical variables and the Mann-Whitney U test for continuous variables. JMP (version 11, SAS Institute, Cary, NC) was used for the analysis.
RESULTS
Patients
In total, 9 patients with RAA were surgically treated at each institution from 2010 to 2018. All 9 patients underwent KAT for RAA. The demographic characteristics of 9 patients undergoing KAT for RAA are demonstrated in Table I. Seven patients were treated with pure LN, 1 was with hand-assisted nephrectomy and 1 was with midline laparotomy. The mean age was 60 ± 8 (median 60, IQR 52–66.5) years, 5 patients had hypertension, 2 patients were symptomatic with abdominal pain and in 7 patients the diagnosis was incidental. All aneurysms had a saccular morphology, in 7 patients RAA was located on the left side and 2 on the right side with a mean diameter of 3.6 ± 1.6 (median 3.1, IQR 2.6–4.3) cm. In 1 case, multiple aneurysms were present. No patients had previous history of endovascular procedures for RAA.
Table IThe demographic characteristics of patients undergoing kidney autotransplantation for renal artery aneurysm at the Erasmus MC and the Padova University Hospital between 2010 and 2018
In six cases, after resecting the aneurysm, an end-to-end arterial anastomosis was performed, as described in Figure 1. In 3 cases, a vein graft (gonadal or saphenous vein) was used as venous interponate. In a case 3, the gonadal vein was used to replace resected artery between the main renal artery and the branch. In case 4 and 5, the saphenous vein patch was used to cover the removed artery wall. Regarding the implantation of the kidney, an end-to-end anastomosis between renal artery and hypogastric artery was performed in 5 cases, and an end-to-side anastomosis between renal artery and iliac artery was in 4 cases.
Fig. 1A case of 68 year-old male with renal artery aneurysm (Case 8). (A) Computed tomography image shows a 3 cm saccular renal artery aneurysm partly thrombosed at the first bifurcation of the left kidney. (B) After laparoscopic nephrectomy of the left kidney, renal artery aneurysm was identified and prepared for ex-vivo renal artery reconstruction on the bench table. (C) After resecting the aneurysm, an end-to-end anastomosis was performed.
Mean operative time was 348 ± 133 (median 370, IQR 203–455) minutes. Five patients had complications: 3 minor complication (wound dehiscence, hydrocele and bowel obstruction) and 2 major complications (acute flogosis of inguinal hernia and vein thrombosis) with 1 graft loss. Mean postoperative hospital stay was 7.4 ± 1.6 (median 8, IQR 6–8.5) days. Mean preoperative creatinine level was 71.1 ± 11.9 (median 67, IQR 64–85) µmol/L, and the creatinine level after a mean follow-up of 15.7 months was 76.7 ± 13.5 (median 79, IQR 65–87) µmol/L. Out of 9 patients, 1 patient was lost to follow-up.
A SYSTEMATIC LITERATURE REVIEW
Search Results and Study Characteristics
A systematic search of the literature identified 706 articles of which 102 articles met our inclusion criteria (Fig. 2). The summary of all included studies and our experiences is represented in Table II. Out of 102 papers, 67 (66%) were single case reports and 5 articles
Editor's choice - ex vivo renal artery repair with kidney autotransplantation for renal artery branch aneurysms: long-term results of sixty-seven procedures.
were case series with more 10 patients reported. Forty-two papers were published before year 2000. Seventeen articles reported laparoscopic approach for nephrectomy, with the largest laparoscopic series of 7 patients published in 2008
A successful extracorporal liquidation of the renal artery aneurysm with reconstruction of the artery and autotransplantation of the kidney in treatment of renovascular hypertension.
Intraoperative evaluation of blood perfusion by laser-assisted indocyanine green angiography after ex vivo vascular reconstruction of intrahilar renal artery aneurysm.
Editor's choice - ex vivo renal artery repair with kidney autotransplantation for renal artery branch aneurysms: long-term results of sixty-seven procedures.
MT, main trunk aneurysm; FB, first bifurcation aneurysm; L, first branch, second branch, or intraparenchymal aneurysm; Multiple, multiple renal artery aneurysm; LN, laparoscopic nephrectomy; E, Heterotopic; and O, Orthotop
The methodological quality of included case series is shown in Table II and supplementary Table 2. The mean total score of the included studies was 3 (range 0–5).
Patient Characteristics
There were a total of 355 patients including our cases who underwent KAT for RAA. The study population consisted of 132 (37.2%) males, 171 (48.2%) females, and 52 (14.6%) cases with unavailable data. The mean age was 42.7 years. Open approach for nephrectomy was performed in 320 (90.1%) patients, via a midline, para-median or lumbotomy approach. In contrast, minimal invasive approach was observed in 35 (9.9%) patients with pure laparoscopic, hand-assisted or retroperitoneoscopic technique.
Aneurysm Characteristics
Saccular aneurysm was most frequently observed with a mean diameter of 2.5 cm. The location of aneurysm in 355 patients was as follows: main trunk (n = 13, 3.7%), first bifurcation (n = 113, 31.8%), first branch, second branch, or intraparenchymal aneurysm (n = 35, 9.9%), multiple (n = 21, 5.9%), and unknown (n = 173, 48.7%).
Type of Aneurysm Repair
Several techniques regarding aneurysm repair were reported.
Out of 355 patients, data on type of aneurysm repair were available in 267 patients including 215 with an autologous graft or a synthetic patch. An autologous graft was often used as a patch graft: hypogastric artery, superficial femoral artery, renal artery, saphenous vein, gonadal vein, or ovarian vein. In only 3 cases, a synthetic patch was used.
Aneurysm repair without graft patch was observed in approximately 20% of cases.
Postoperative Outcomes
Data regarding postoperative major complication (Clavien Dindo III or IV) was available in 95 studies (n = 307) with the incidence of major complications of 9.4%. Mean postoperative hospital stay in large series was reported to be 8 to 11 days. No in-hospital mortality after KAT was identified.
Long-term Outcomes
No study reported on aneurysm recurrence after KAT during follow-up. In only 1 case, the dilation of the gonadal vein patch after KAT was identified.
The overall incidence of graft loss was 4.1% including early or late graft loss (12 cases out of 290). However, there were only 29 studies (n = 137) showing outcomes after more than 1-year follow-up. The largest series by Duprey et al. reported that the primary and primary-assisted patency of KAT were 88% and 91%, and the overall patient survival rate was 100%, 98%, and 89% at 5, 10, 15 years.
Editor's choice - ex vivo renal artery repair with kidney autotransplantation for renal artery branch aneurysms: long-term results of sixty-seven procedures.
The present study reports our 2-center experiences of KAT for RAA as the largest laparoscopic case series published so far, showing surgical technique and outcomes. We found that laparoscopic approach for nephrectomy followed by heterotopic KAT was feasible. In addition, this systematic review identified 102 articles including 355 patients undergoing KAT for RAA, and demonstrated that KAT for RAA was an effective procedure with good outcomes.
With respect to strategy for RAA, there is no treatment guideline for RAA. Endovascular treatment for RAA would be the first option, owing to minimal invasiveness benefits, especially for simple aneurysms located at main artery, first branch or parenchymal RAAs.
Even in ruptured aneurysms, endovascular approach might play a rule with coil embolization or endovascular stenting in case of hemodynamic stability and favorable anatomy.
However, data with long-term follow-up is lacking in patients treated with endovascular procedure for RAA, and the fact that the persistence of residual flow accounted for 15% of cases should be recognized.
Editor's choice - ex vivo renal artery repair with kidney autotransplantation for renal artery branch aneurysms: long-term results of sixty-seven procedures.
When an endovascular approach is not feasible, surgical treatment should be considered as the second line treatment. There are 2 option regarding RAA repair: in-situ or ex-vivo repair.
These approaches are not recommended for multiple or complex aneurysms, especially located in artery bifurcations, right mid renal artery or whence distal vascular control might be challenging and long ischemia time are required to perform anastomosis.
To date, no randomized controlled trial has been performed to compare outcomes between in-situ and ex-vivo RAA repair. However, superior patency rates in ex-vivo repair have been reported compared to those in in-situ repair.
Regarding the ureter management in KAT, there is more risk of leakage or stenosis when the ureter is divided. In contrast, the ureter needs to be long enough to take out the kidney and reconstruct the vessels in cases with non-divided technique of the ureter. This technique can be easier in cases with open approach for nephrectomy or non-obese cases.
The use of open or laparoscopic approach for nephrectomy in complex RAA requiring ex-vivo RAA repair depends on availability and experience. In the overall outcome of this complex surgery, the most decisive factor would be excellent outcomes in vascular reconstructive surgery. Currently, LN is widely described as the gold standard both in cancer patients and kidney donors since shorter hospital stay, less pain and decreased time to return to full function than open nephrectomy, and these benefits can also be applied to KAT.
In our experiences, LN with ex-vivo renal artery reconstruction followed heterotopic KAT was feasible for complex RAA. The present systematic review overviewed the current evidence regarding KAT for RAA, and demonstrated that the use of LN for RAA was still limited, without comparative studies assessing both techniques.
Finally, the primary nephrectomy would be another option especially in cases of previous endovascular treatment, repetitive and refractory renovascular hypertension, and multiple complex or ruptured RAA.
However kidneys should be preserved as much as possible in patients with bilateral RAA or in hemodynamically stable patients with ruptured RAA.
This systematic review has some limitations. Inherent to the low incidence of the condition, the study design was retrospective and covered mostly empirical evidence from case reports and small case series without proper control. Due to of its low incidence, 1 can assume that KAT for RAA is underdiagnosed and underreported, presenting a potential publication bias. Moreover, several data were unavailable, in particular long-term follow-up. Actually 47 studies out of 102 did not report on follow-up period because of focusing on surgical and short-term outcomes, and the rest demonstrated outcomes with a mean follow-up of 21 months. Therefore, we could not perform meta-analysis of long-term outcomes such as graft patency and graft survival by comparing open and LN. Accordingly, further well-designed studies with proper control as well as long-term follow-up should be conducted.
CONCLUSIONS
The present study demonstrated our experiences of KAT for RAA. Laparoscopic approach for nephrectomy was feasible with good postoperative outcomes. Despite the difficulty of interpreting the fragmented and empirical evidence on KAT for RAA and the limitations, our systematic review shows that KAT is an effective treatment for RAA when other therapeutic strategies are not available. The use of open or laparoscopic approach for nephrectomy could depend on availability and experience.
AUTHOR CONTRIBUTIONS
Concept and study design: EC, KT and RCM; acquisition of data: EC, KT, HJANK, LF, PR and RCM; Drafting of the manuscript: EC and KT; Critical revision of the manuscript for important intellectual content: HJANK, JNMI, LF, PR and RCM. All authors have approved the final version of the article.
FUNDING
None.
We thank Wichor M. Bramer (Biomedical Information Specialists) from the Medical Library in Erasmus MC, Erasmus University Medical Centre Rotterdam (Rotterdam, the Netherlands) for his assistance with the literature search.
A successful extracorporal liquidation of the renal artery aneurysm with reconstruction of the artery and autotransplantation of the kidney in treatment of renovascular hypertension.
Intraoperative evaluation of blood perfusion by laser-assisted indocyanine green angiography after ex vivo vascular reconstruction of intrahilar renal artery aneurysm.
Editor's choice - ex vivo renal artery repair with kidney autotransplantation for renal artery branch aneurysms: long-term results of sixty-seven procedures.
Evaluated according to the Clavien-Dindo Classifications.
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