Objectives: Incidence of vascular anomalies in donor kidneys varies from 18% to 30% and presents a challenge for a transplant surgeon in kidney transplant. Here we present our personal experience for man­agement of the complicated and unexpected cases.

Materials and Methods: A total of 250 kidney transplants (226 living, 24 deceased) were performed in a period of 24 years; mean donor age was 55 years (range, 25-86 years), and mean recipient age was 38.6 years (range, 14-66 years). We analyzed the surgical techniques, complications and outcomes, rejection episodes, kidney function, and graft and patient survival rates.

Results: Of 250 nephrectomies, 209 had a single artery (83.6%), 34 had 2 arteries (13.6%), and 7 had 3 arteries (2.8%). Of 34 double arteries, 14 had 2 main arteries, 15 had a main and a polar artery, and 5 had an aortic Carrel patch after deceased donation. According to the size, type, and position, the anastomoses were performed with branches of hypogastric, epigastric inferior, iliac external, and main renal artery, intracorporeally or in bench surgery. Regarding veins, 1 double inferior vena cava, 1 left-side inferior vena cava, 4 retroaortic, 2 circumaortic, 10 large lumbar veins draining into the left renal veins, and 8 cases with 2 or more different size renal veins were managed. In 9 cases with short right renal vein, an extension with vena cava (a “Barry cavoplasty”) was performed in deceased donor organs. No serious surgical complications related to vascular anomalies were observed. There were no statistical differences in 1-, 6-, and 12-month graft survival rates between the groups with or without vascular anomalies.

Conclusions: Vascular anomalies should no longer be considered a contraindication for transplant, if careful anastomosis is performed in every case to avoid ischemia and further complications. Therefore, management of vascular anomalies could be a graft-saving procedure.

Key words : Graft survival, Organ donation, Surgical techniques, Vascular anomalies

Introduction

The surgical reconstruction of the blood circulation is one of the most important parts of transplant surgery, including living donor (LD) and deceased donor (DD) organs. The anatomic region of the kidneys and blood supply system is prone to common congenital malformations, as well as uncommon malformations, any of which may present a challenge for transplant surgeons. The efficacy of the surgical correction and adaptation of the local arterial and venous blood supply are crucial to achieving short- and long-term graft survival. In the past, most cases with arterial anomalies (multiple) were a genuine contraindication for kidney transplant, especially in living donor transplant.¹ The problem of multiple renal arteries (MRA) is associated with other surgical problems in kidney transplant recipients, such as delayed graft function, acute rejection, and increased urological and vascular complications. Some of these problems are discussed in the literature, such as renal infarcts, ureteral necrosis and ureteral fistula, hemorrhage, and hematoma, as well as thrombosis.

The presence of MRA is the most frequently encountered anatomic variation in kidneys.^2-4 Incidence of unilateral and bilateral MRA during kidney transplant is 23% and 10%, respectively.² Autopsy studies have suggested that the prevalence rate of MRA is 18% to 30%, with 15% being bilateral.⁵ A variety of methods have been described to transplant these MRA kidneys, including micro­vascular surgery. Here we review the available operative techniques, the relative merits and indications, and the reasons for our preferences.

The venous anomalies, such as double veins with different size, retroaortic veins, and circumaortic veins, as well as anomalies in venous and vena cava position, are important considerations in kidney transplant surgery and can cause difficulties in open surgery and laparoscopic surgery. Although venous anomalies are not common in kidney transplant surgery, these present a real clinical dilemma if discovered during the surgical procedure.^6-10

Today, MRA are no longer considered a contraindication for transplant, even in living donor nephrectomies.^11-13 With current advances in vascular surgical techniques, kidneys with MRA are engrafted without hesitation in cases when the blood vessels supply more than 5% to 10% of renal parenchyma.¹⁴

With the inclusion of all possible kidneys for transplant with MRA and other vascular anomalies, including those with arteries and veins inadvertently damaged during donor kidney removal, the potential donor pool is expanded, and more organs are available for the increasing number of patients on wait lists.^15,16

The worldwide popularity of laparoscopic donor nephrectomy, with the accumulation of surgical and technical experience, is now extended to donor organs with MRA, but MRA remain a technically challenging condition, especially for right-side kidney procedures.¹⁷

Materials and Methods

We retrospectively analyzed 250 kidney transplant recipients (226 LD and 24 DD) during the period of 1987 to 2011 at the University Clinics of Urology, Nephrology and Transfusiology at the Clinical Centre in Skopje, North Macedonia. Among 226 living donors, 202 were parents of recipients, while 24 were unrelated donors who were spouses (17), mothers-in-law (4), fathers-in-law (2), and a brother-in-law (1). According to the policy at our center, the suitable donors (living and deceased) were accepted with a minimum of 50% of human leukocyte antigen compatibility and complement-dependent cytotoxicity cross-match negativity. For imaging a vascular structure of the kidneys (arterial and venous), a standard angiography, computed tomography angiography, or magnetic resonance imaging angiography was performed.

The final decision regarding which kidney should be removed was based on the established criteria that the donor should retain the better kidney and that the donor nephrectomy should be performed on the side that is the least complicated, to reduce risk to the donor.¹⁸ The standard transplant procedure was performed for all kidney transplant recipients, ie, end-to-end or end-to-side arterial anastomosis with hypogastric or iliac external artery and end-to-side venous anastomosis with external iliac vein. Ureterovesicular anastomosis was performed using the Lich-Gregoire procedure in all kidney transplant recipients. All vascular anastomoses were performed by a well-skilled transplant surgeon who used optical loupes with the standard ×2.5 magnification and standard surgical instruments and materials, including monofilament nonabsorbable suture (5-0, 6-0, 7-0, or 8-0). All grafts were transplanted into iliac fosse via extraperitoneal access. Most of the cases with vascular anomalies (arterial and venous) were successfully managed during the surgery procedure by performing microvascular anastomoses. In a few complicated cases, bench surgery was needed.²

A quadruple sequential immunosuppression (antithymocyte globulin, basiliximab, and daclizumab as an induction and triple-drug maintenance therapy with calcineurin inhibitors, mycophenolate mofetil, and steroids) was introduced in all patients regardless of the immunological risk of the kidney transplant recipient.¹⁹ The demographic and clinical charac­teristics of the donors and recipients are presented in Table 1.

Survival rates of patients and grafts, delayed graft function, rejection rate, bleeding episodes and hematomas, vascular and urological complications, and cold and warm ischemia times were analyzed during the study. The results were compared with patients who had single renal arteries and veins, which was considered as the control group.

Results

Of 250 donor nephrectomies (84% left side and 16% right side), 209 donor organs had a single renal artery and 41 had MRA (34 donor organs had 2 arteries, and 7 donor organs had 3 arteries). With regard to the venous system, 242 kidneys had a single vein (96.8%), and 8 donor kidneys had 2 or more different size renal veins. Among the donors with a single vein, the specific different venous anatomic position had been determined, ie, retroaortic left vein in 4 cases (3 with type 1, and 1 with type 4) and circumaortic (collar) left renal veins in 2 cases. In 10 LDs a large lumbar vein was drained into renal vein, and in 9 DDs a short right renal vein was discovered and resolved.

Surgical and microsurgical techniques of intra­corporeal in situ and ex vivo bench surgery anastomotic techniques were applied.²

Before and during the preparation of the LD and recipient pair, arterial anatomy was carefully evaluated for both, usually by computed tomography angiography.20 With regard to our center’s policy to accept expanded criteria donors (eg, elderly, marginal), the renal vascular anatomy of the donor was an important consideration for the final decision to transplant, and a plan was established to manage potential MRA or atherosclerotic plaques on the donor renal arteries and recipient pelvic arteries.

Arterial reconstruction
Ex vivo bench surgery anastomotic technique was used in 13 cases and in 28 intracorporeal in situ reconstructions. In the case of 2 main arteries (12 LD), end-to-end anastomosis to the branches of the internal iliac artery was used. In 2 cases, a double-barrel technique (side-to-side conjoined artery to artery anastomosis) was performed. Fifteen LD had main and polar arteries (7 upper polar and 8 lower polar), and among these were 3 that were anastomosed into the main artery. Four smaller upper polar arteries, which supply less than 10% of the kidney surface area, were ligated. Five lower polar arteries were anastomosed end-to-end with the epigastric inferior artery, 1 end-to-side with external iliac artery, 1 end-to-side to main renal artery, and 1 was ligated. Despite the ligation of the lower polar artery, we did not observe any ureteral consequences. In 5 DD, an aortic Carrel patch was used for end-to-side to external/common iliac artery anastomosis. In a single patient, an aortic patch between 2 widely separated arteries was created to approach these and revascularize with a single suitable Carrel aortic patch.

In 7 donors (5 LD and 2 DD), 3 arteries were found. Of 5 LD, 3 kidneys had 3 hilar arteries. Two arteries were anastomosed end-to-end with the branches of hypogastric artery, and the third artery was anastomosed end-to-side with the external iliac artery. For 2 LD with 2 main arteries and 1 lower pole artery, the arteries were anastomosed end-to-end with the branches of the hypogastric artery and lower polar artery end-to-end with the epigastric inferior artery. For 2 DD with 3 renal arteries, the arteries were anastomosed with an aortic Carrel patch end-to-side to the external/common iliac artery (Table 2, Figure 1).

Venous reconstruction
Similar to arterial anatomy variations, venous variations have been observed with as many as 8 accessory veins. In this case, 7 veins were ligated; however, for 1 vein, an end-to-side anastomosis into the main renal vein was necessary. An extension of a short right renal vein was created with an adherent caval patch in 9 DD cases.

Regarding anatomy position variations in LD cases, 4 retroaortic left renal veins were detected (type 1 joining IVC in the orthotopic position in 3 cases, and type 4 joining IVC close to the union of the common iliac vein in 1 case). Two circumaortic left collar veins were observed for which the main and dominate vessel was the preaortic branch. After careful surgical assessment and investigation, the smaller retroaortic branch was ligated without complications. The other anatomic variations included large lumbar veins draining to the left renal veins, which were carefully ligated. Curiously, among the cases presented in our study, the congenital anomalies of affected IVC were observed in 2 LD left nephrectomy, ie, the left side in one and a double IVC in the other (Table 3, Figures 2 and 3).

The surgical approach to the venous system anomalies should be performed with care equal to that for arterial reconstruction; there are surprisingly high numbers of congenital variations (Figures 4 and 5). In many cases, the venous reconstruction presents a real surgical dilemma, and yet it may be the best solution.

Discussion

The present worldwide organ shortage causes 20 deaths every day, and every 10 minutes someone new is added to the wait lists; therefore, every available organ is important and has the potential to save a human life. No available kidneys should be considered unsuitable for transplant if there is a possibility for their successful use. Organ shortage remains a major problem, especially in developing countries, where the rate of transplant is significantly lower than in the developed world.²¹ Our task as surgeons is to perform any possible surgical procedure to best facilitate a successful kidney transplant. With this practice, the percentage of marginal donors (eg, donors with vascular anomalies, controlled hypertension, and urological problems, as well as elderly donors) can be increased.^15,16

Vascular anomalies in donors and recipients, which were long considered to be a contraindication for transplant, are now increasingly accepted because of improvements in surgical techniques and imaging procedures.¹¹ Usually, MRA are identified from the results of the donor angiography. Our center’s policy is to use a donor kidney with MRA only if the presentation is bilateral or if the kidney has a single artery that cannot be used for medical and ethical reasons.^19,22 The introduction of bench ex vivo surgery or intracorporeal microsurgery enables most arterial anomalies to be reconstructed and reanastomosed with good short- and long-term outcomes that are equal to those with single artery.² Arterial reconstruction is performed according to known experiences in transplant surgery using techniques that best fit the situation and with which the surgeon feels most comfortable. The reconstruction of the arterial supply of the graft is a difficult surgical procedure that may require the introduction of an ex vivo microsurgery procedure (bench) in some cases; hence, this approach may represent a clinical dilemma. When a donor kidney has 2 arteries of unequal size, it is preferable to anastomose these arteries separately rather than perform an end-to-side bench surgery, which carries the potential risk of compromising the lumen of the larger renal artery. Care must be taken with intrahilar dissection and vascular anastomosis, which may jeopardize ureteral blood supply. Lower polar arteries must be anastomosed with attention to the risk that occlusion of lower polar arteries may cause ischemia, infarction, and urology complications such as caliceal or ureteral necrosis and fistulae. Regarding the use of inferior epigastric artery, it is especially suitable for anastomosis with an injured length of lower polar artery to avoid further ureteral complications on the same side. Therefore, the inferior epigastric artery should be carefully prepared from the start of surgical incision to secure sufficient length. On the other hand, the inferior epigastric artery is rarely involved with atherosclerosis, and wall thickness and diameter are almost the same with the polar arteries. Any eventual anastomosis with epigastric arteries should be performed only after removal of the vascular clamps on the main vessels to avoid the prolongation of warm ischemia time. In the present study, no ureteral fistula was observed.^2,21,23-25 With DD cases, the reimplantation of MRA on a common Carrel patch is the preferable technique. The arterial reconstructive procedure is presented in Figure 1.

In our study, the incidence of MRA (16.4%) was low compared with other studies.^2,5 The reason for this may be the large number of living-related and living-unrelated donors in our program.²²

The percentage of venous anomalies was much lower (3.2%) than arterial anomalies. Most venous anomalies were multiple renal veins or retroaortic and circumaortic collar veins. In our experience, the 2 components of the circumaortic veins must be identified, and this is not always an easy task. In every case of circumaortic veins, we decided to ligate a slightly smaller vein, usually a retroaortic component. We did not observe any complication of importance after the ligation.^7,8,10 A special challenge was presented by the position and structure of venous system anomalies discovered incidentally (drainage of large lumbar veins into the left renal vein, double IVC, and left-side IVC) (Figure 2). Therefore, modern imaging techniques, including multidetector computed tomography angiography, could reveal not only arterial anomalies but also different complicated venous system variations.^9,10 The presentation of the venous variations before surgery to an experienced radiologist and transplant surgeon could be especially important in the final decision regarding kidney choice (ie, left or right). In our series of venous anomalies, of particular interest were the cases of double IVC and left-side IVC because of the short renal veins from both sides that could be represent a surgical problem.^9,10 In case of en bloc binephrectomy in DDs, the problem of short right renal veins could be solved by so-called “Barry cavoplasty,” which we have used successfully in 9 cases of our DD transplant program.²⁶

The venous variations and anomalies are a specific challenge for the transplant surgeon and represent a real clinical dilemma. The total number of more than 60 cases with vascular anomalies in our experience confirms that these cases could represent a serious problem for transplant surgeons, especially in laparoscopic LD27,28 and DD nephrectomy. Theoretically, the transplant team could expect more complications such as prolonged cold ischemia time, second warm ischemia time, time of reanastomosis, higher rate of vascular and urology complications, readmissions, long-term hospitalization, and addi­tional surgery. In analyses of surgical complications (Table 4), we observed no differences between the group with vascular anomalies and the group with single artery and vein.

Most of the complications presented in our study are typical, ie, common in routine transplant surgery. The percentage of 2% renal artery thrombosis in the whole group of patients corresponds with previous results.²⁹ Of note, we did not observe any episode of thrombosis after reconstruction surgery in the group with MRA. Regarding late artery stenosis, our rate is 6%, which is in accordance with published data.30 Similar to the case of artery thrombosis, we did not find any differences between group 1 and group 2. However, we observed these complications at the beginning of our transplant program. The routine method of treatment of late artery stenosis was percutaneous balloon dilatation or stenting. The urinary fistulas arose mostly as a complication of vascular irrigation of ureter in 5.6% of our cohort, but this complication was not associated with the cases of MRA. The routine treatment was terminoterminal anastomosis with ipsilateral or contralateral ureter of the same side. According to our experience, reconstructive surgery of the accessory lower polar artery is mandatory.

When we compared results from kidney transplant recipients who had a single artery anastomosis, we did not find any significant differences in serum creatinine levels at 1, 6, and 12 months and graft survival rate at 12 months (Table 5).

Conclusions

Donors with vascular anomalies are often considered unsuitable for transplant; however, these donors can be suitable sources of valuable organs. The use of modern imaging techniques before surgery could identify most arterial and venous anomalies, providing valuable information for the decision regarding which kidney should be removed, that is, the left or right. We recommend the use of multidetector computed tomography angiography as a standard procedure in the assessment of donor suitability. An experienced transplant team at a high professional level is necessary to successfully manage the variety of different vascular anomalies, especially in living kidney donors, and to prevent short- and long-term complications in kidney transplant recipients.

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