Abstract
Introduction: Renal artery aneurysm (RAA) is a rare vascular disease with a mortality rate of up to 80% upon rupture. This study aimed to investigate the safety and efficacy of ex situ repair and autotransplantation for endovascularly untreatable RAA. Methods: A retrospective nationwide cohort study was conducted in RAA patients undergoing ex situ repair and autotransplantation in the Netherlands. Surgical techniques, postoperative complications, and graft outcomes were assessed. Results: Ex situ repair was performed in 9 patients with 11 RAAs. Eight RAAs were located at the first bifurcation, one on the main trunk, one on the first branch, and one on the second branch. Nephrectomy was performed via laparoscopy (n = 7), robotic-assisted laparoscopy (n = 1), and laparotomy (n = 1). Postoperative complications were recorded in 4 patients, including bowel obstruction, delirium, pneumonia, and hydronephrosis due to double-J dislocation. The median estimated glomerular filtration rate was 83 mL/min/1.73 m2 pretransplant and 88 mL/min/1.73 m2 posttransplant. By an average follow-up of 32 months, 2 patients had died due to lung adenocarcinoma and stroke, while all autotransplanted kidneys had good patency and remained functional. Conclusions: Ex situ repair and autotransplantation are safe and feasible for endovascularly untreatable RAA cases. Larger cohorts with longer follow-up periods are necessary to further evaluate the role of this surgical approach.
Introduction
Renal artery aneurysm (RAA) is a rare vascular disease, with an incidence of 0.1% in the general population [1, 2]. Most aneurysms are small, asymptomatic, and diagnosed incidentally during examinations for other purposes [3]. When symptomatic, RAA patients present hypertension, flank pain, hematuria, or urinary collecting system obstruction. Complications of RAA include rupture, distal embolization, infarction, arterial dissection, and renal failure [2].
The indications for RAA treatment include symptomatic patients, women who are pregnant or of childbearing age, and aneurysms with a diameter greater than 2 cm [2]. Treatment strategies include endovascular and surgical repair, depending on the aneurysm size, morphology, and location. Surgical repair, including in-situ repair and ex situ repair, is indicated for complex aneurysms or those located at the bifurcation or distal branches. Additionally, nephrectomy remains a treatment option if other approaches fail.
Existing literature comparing endovascular and surgical techniques focuses on in-situ repair, although outcomes of ex situ repair might be superior [4]. Since Gallagher et al. [3] reported the first case series of ex situ repair and autotransplantation, clinical features and outcomes of this technique have been reported through small case series [5‒8]. Herein, we present a nationwide cohort study of 11 ex situ RAA repairs with autotransplantation in 9 patients, including 1 patient with three concomitant aneurysms.
Methods
A nationwide cohort study was conducted via the Dutch Kidney Transplant Study Group between January 2016 and December 2023. To identify RAA patients who underwent ex situ repair and autotransplantation, a national survey was conducted across all transplant centers qualified to perform kidney transplantation. Demographics, surgical records, and follow-ups were collected from electronic medical records by the operating surgeons.
The decision of ex situ repair and autotransplantation was made based on the collective expertise of the medical team and patient’s willingness. A comprehensive multidisciplinary meeting was organized to discuss possible treatment strategies, and these options were extensively discussed with the patient.
Primary outcome measure was the success of the procedures, defined by graft patency and renal function preservation. Secondary outcome measures included operative time, hospital stay, and postoperative complications, classified according to the Clavien-Dindo classification.
Surgical Techniques
The surgical procedure involves nephrectomy, ex situ aneurysm repair, and autotransplantation.
Nephrectomy
Nephrectomy was performed using a laparoscopic, robotic-assisted laparoscopic, or laparotomy technique. Laparotomy was performed in a single case where the RAA was in a transplanted kidney in the iliac fossa.
Nephrectomy was performed following the standard procedure for donor nephrectomy according to international guidelines [9]. For robotic-assisted laparoscopic nephrectomy, the da Vinci Xi surgical system was used. Port placement is shown in Figure 1. The kidney was extracted using a specimen retrieval bag through the modified Gibson incision, flushed with a cold University of Wisconsin solution, and stored on ice for aneurysm repair.
Ex situ Repair and Autotransplantation
Various techniques used for the reconstruction of renal arteries are depicted in Figure 2. The type of suture most commonly used was 6-0 or 7-0 prolene, depending on the size of the artery or arterial branches. In all cases, optical magnification (typically using surgical loupes at ×2.5 to ×4) was required to ensure precise anastomosis.
Kidney autotransplantation was performed in a heterotopic position through the kidney extraction incision (Gibson incision). For kidneys with multiple arterial branches, a side-to-side anastomosis was performed following an end-to-side anastomosis to the external iliac artery. The choice of technique was thus tailored based on the length and number of the remaining renal arteries and the patient’s specific anatomy.
Results
Ex situ repair was performed in 9 patients (8 female and 1 male) with a median age of 61 years (Table 1). Seven patients had additional comorbidities, including hypertension (n = 5), aortic valve replacement (n = 2), and chronic obstructive pulmonary disease (n = 1). Six patients were asymptomatic, with RAAs discovered incidentally by CT scans performed for other conditions. Three patients were symptomatic, presenting with flank pain that prompted the initial diagnostic CT scan. One patient had a solitary kidney, and another had a history of kidney transplantation. Preoperative blood pressures ranged from 125 to 180 mm Hg systolic and 75–110 mm Hg diastolic. The estimated glomerular filtration rate (eGFR) was 47 mL/min/1.73 m2 in the transplant recipient and 83 mL/min/1.73 m2 (range 70–94) in the other patients.
Age, median (range), years | 61 (51–68) |
Sex, n (%) | |
Male | 1 (11) |
Female | 8 (89) |
BMI, median (range), kg/m2 | 26 (17–30) |
ASA classification, median (range) | 2 (1–3) |
Symptoms, n (%) | |
Asymptomatic | 6 (67) |
Flank pain | 3 (33) |
Aneurysm characteristicsa | |
Laterality, n (%) | |
Left | 7 (64) |
Rightb | 4 (36) |
Size, median (range), cm | 2.7 (0.8–7.4) |
Location, n (%) | |
First bifurcation | 8 (73) |
Main trunk | 1 (9) |
First branch | 1 (9) |
Second branch | 1 (9) |
Prior treatment, n (%) | |
Untreated | 8 (89) |
Coil embolization | 1 (11) |
Age, median (range), years | 61 (51–68) |
Sex, n (%) | |
Male | 1 (11) |
Female | 8 (89) |
BMI, median (range), kg/m2 | 26 (17–30) |
ASA classification, median (range) | 2 (1–3) |
Symptoms, n (%) | |
Asymptomatic | 6 (67) |
Flank pain | 3 (33) |
Aneurysm characteristicsa | |
Laterality, n (%) | |
Left | 7 (64) |
Rightb | 4 (36) |
Size, median (range), cm | 2.7 (0.8–7.4) |
Location, n (%) | |
First bifurcation | 8 (73) |
Main trunk | 1 (9) |
First branch | 1 (9) |
Second branch | 1 (9) |
Prior treatment, n (%) | |
Untreated | 8 (89) |
Coil embolization | 1 (11) |
aThese variables are based on the number of aneurysms and not on the number of patients.
bThis variable includes the kidney graft in the right iliac fossa.
RAAs were located on the left side in 5 cases. One patient had multiple aneurysms, including a large aneurysm with a diameter of 7.4 cm and two smaller ones. The remaining patients had single aneurysms greater than 2 cm. One patient underwent unsuccessful coil embolization before surgical intervention, while the others were untreated before the final treatment.
Most nephrectomies were performed laparoscopically (n = 8), with 1 patient undergoing robotic-assisted nephrectomy. The kidney transplant recipient underwent a transplantectomy through laparotomy prior to ex situ repair and retransplantation.
The majority of RAAs (73%) were located at the first bifurcation of the renal artery (RA), while the remaining were located in the main trunk (n = 1), first branch (n = 1), and second branch of the anterior RA (n = 1). All aneurysms were saccular. After aneurysmectomy, a combined end-to-end and end-to-side arterial anastomosis was performed in 4 cases. The hypogastric artery was used to bridge the arterial defect in 2 cases and direct end-to-end anastomosis was performed in 2 cases. A side-to-side coadaptation was performed for implantation in 1 case. In the case of an aneurysm located in the main trunk, it was in close proximity to the first bifurcation of superior and inferior arterial branches, making endovascular treatment not possible without sacrificing one of the branches.
The median operative time was 5.5 h (range 3–9), with median warm ischemia time (WIT) of 23 min (range 13–33) and estimated blood loss of 300 mL (range 100–550). The median length of hospital stay was 8 days (range 6–85), with the 85-day stay attributed to pneumonia. Four patients had postoperative complications, including postoperative delirium, bowel obstruction, pneumonia (grade II), and hydronephrosis due to double-J dislocation (grade IIIa).
At a mean follow-up of 32 months, postoperative eGFR was 31 mL/min/1.73 m2 in the patient with kidney transplant history. The renal function of other patients was stable, with an average eGFR of 88 mL/min/1.73 m2 (range 63–93). No patient required temporary dialysis. Renal duplex ultrasonography confirmed good arterial patency in all patients. Representative pre- and postoperative CT scans are shown in Figure 3. Postoperative blood pressures ranged from 110 to 150 mm Hg systolic and 60–95 mm Hg diastolic. Three patients had an improvement in blood pressure control, with a decrease of 11–35 mm Hg systolic and 19–25 mm Hg diastolic. Both asymptomatic and symptomatic patients achieved excellent graft patency. However, asymptomatic patients exhibited better postoperative renal function and a lower frequency of complications. By the end of follow-up, 2 patients died due to lung adenocarcinoma and stroke, both with a functioning autotransplanted kidney.
Discussion
In our cohort, RAA predominantly affects individuals in their middle to older age (range 51–68 years) and females (89%). This aligns with existing literature showing a typical presentation in their sixth decade and associated with fibromuscular dysplasia which is more prevalent in females [2]. Additionally, 67% of patients were asymptomatic at diagnosis, which aligns with previous studies reporting symptomatic presentation in 4%–23% of cases. Hypertension is often the primary cardiovascular risk factor as 56% of patients were observed with hypertension.
Although endovascular RAA repair has gained acceptance for treating proximal aneurysms at the main renal trunk, studies have reported 8–17% of the patients undergoing endovascular repair experienced aneurysm reperfusion, with 4.4% requiring a secondary procedure [10, 11]. In more complex cases, endovascular intervention results in high incidences of postembolization syndrome and segmental renal ischemia. Consequently, in these cases, surgical treatment remains the gold standard.
To ensure adequate blood flow, different arterial reconstruction techniques have been applied. Previous studies have reported the use of the saphenous vein or gonadal vein as interposition grafts between the arterial stump and iliac artery [3, 5, 6]. These vein grafts are ease for harvest and flexible. However, due to the inherent structural and functional limitations, vein grafts carry a higher risk of occlusion, intimal hyperplasia, and aneurysms when exposed to arterial pressures [12]. Harvesting the hypogastric artery is more complex and invasive compared to the vein graft, but it provides long-term durability and patency, making it ideal for high-pressure arterial systems. However, the long-term risk of buttock claudication should be monitored.
One patient in our cohort underwent robotic-assisted nephrectomy, which is a promising alternative to traditional laparoscopic surgery. Compared to laparoscopic nephrectomy, robotic-assisted nephrectomy shows similar postoperative complications but shorter hospital stay [13, 14]. For complex vascular anastomoses, robotic surgery has proven superior over traditional laparoscopic surgery as it allows for a more ergonomic approach and recreates the hand-eye coordination that is lost in laparoscopic surgery [15]. For nephrectomy, larger cohort studies are warranted to investigate if robotic-assisted nephrectomy can reduce the morbidity and improve outcome.
The choice between in situ and ex situ repair remains open. Recent studies of in-situ RAA repair have reported durations of surgery of 3–6 h, WIT of 10–60 min, and blood loss of 25–400 mL [15, 16]. We reported a longer surgery duration and more blood loss but a shorter WIT. Despite the longer surgery duration, ex situ repair offers several advantages. First, although intracorporeal transarterial renal hypothermia is performed during in-situ repair [16, 17], complex cases still require longer WIT. Second, extracorporeal flushing with cold preservation solution ensures better protection, while renal cortex remains around 20°C under intracorporeal hypothermic perfusion during in-situ repair [18]. Additionally, the extensive expertise required for in-situ repair limits its widespread adoption.
In our study, all cases involved transection of the ureter. Autotransplantation without transection is another option, in which the renal vessels are anastomosed with the ureter intact [5, 7, 19]. Nephrectomy without ureteral transection avoids the complications related to ureteroneocystostomy. However, resecting the ureter simplifies the graft cooling and arterial reconstruction as these procedures are conducted on the back table, instead of on the patient’s skin during surgery. To our knowledge, no studies to date have compared the clinical outcomes of ex situ repair with and without ureter transection.
RAA is associated with impaired renal function and hypertension due to RA compression, microembolization in the distal renal parenchyma, and hemodynamic changes from turbulent blood flow in the aneurysm [20]. Our results demonstrated a mild improvement in renal function following ex situ repair and autotransplantaion. Three out of 5 patients exhibited improved blood pressure, while 2 patients had no significant improvement. Such different therapeutic effects are also reported in other studies [3, 5, 8]. Our findings suggest that successful surgical revascularization plays an important role in improving renal hemodynamics. However, for non-renovascular hypertension, the impact of aneurysm repair is limited, consistent with observations from in-situ RAA repair studies [17].
Another option for RAA patients necessitating nephrectomy is to donate the removed kidney. The study by Ceuppens et al. [21] shows that patients with benign kidney disorders, including RAAs, can successfully donate kidneys as unspecified donors following nephrectomy. Before considering donation, it is important to ensure the individual has sufficient renal function in the remaining kidney and no contraindications to donation. For RAA patients, the presence of multiple arterial aneurysms and the potential risk of aneurysm development in the remaining kidney should be carefully assessed. All ethical and medical considerations must be addressed, and patients should be fully informed about the risks, benefits, and the need for regular post-donation follow-up.
Given the technical complexity and low frequency of ex situ repair for RAAs, we recommend that these procedures be performed in specialized transplant centers. These centers should have a multidisciplinary team comprising experienced transplant and vascular surgeons, as well as nephrologists. Additionally, we propose conducting such nationwide survey at regular intervals (i.e., every 5 years). This approach would not only help enlarge the cohort size but would also enable the prolongation of follow-ups, thereby improving data integrity and providing a more comprehensive understanding of long-term outcomes.
Conclusion
In this study, we reported surgical techniques and clinical outcomes of ex situ RAA repair and autotransplantation based on a nationwide cohort. As a supplement to in-situ repair, ex situ repair and autotransplantation are safe and feasible for endovascularly untreatable RAAs. The limited follow-up and sample size require larger studies to validate its therapeutic efficacy.
Acknowledgment
We thank Dr. Junfeng Huang for the assistance in schematic drawings.
Statement of Ethics
The study was conducted in accordance with the Declaration of Helsinki and approved by the Ethics Committee of EMC (MEC-2018-1401). Written informed consent was waived by the Ethics Committee of EMC due to the retrospective nature of the study and the use of de-identified patient data.
Conflict of Interest Statement
The authors have no conflicts of interest to declare.
Funding Sources
This study was not supported by any sponsor or funder.
Author Contributions
Y.F. participated in conception, design, and writing of the manuscript. H.J.A.N.K. and R.W.F.d.B. participated in analysis, interpretation, and critical revision. D.K.d.V., B.J.P., M.C.W., I.F.J.T., J.v.L., M.M.I., and R.A.P. participated in data collection and critical revision. R.C.M. participated in conception, design, data collection, and critical revision.
Data Availability Statement
The data that support the findings of this study are not publicly available due to reasons of sensitivity and are available from the corresponding author upon reasonable request.