Objectives: Multiple renal vessels are often detected in living and deceased organ donors. In the past, transplant with multiple renal vessel grafts has been a contraindication because of high vascular and urological complication rates. However, improvements in vascular reconstruction and anastomosis techniques have allowed graft function to be maintained for many years. Here, we retrospectively evaluated transplant of multiple renal vessel grafts and graft survival and postoperative vascular and urological complications.
Materials and Methods: From November 1975 to July 2020, there were 3136 renal transplants (716 deceased donors, 2420 living donors) performed in our center. There were 2167 living donors and 643 deceased donors with single renal vessel grafts and 253 living donors and 73 deceased donors with multiple renal vessel grafts. For anastomoses, external iliac, internal iliac, common iliac, and inferior epigastric arteries and external iliac veins were used. Cold ischemia time, anastomosis time, postoperative vascular and urological complications, acute tubular necrosis, creatinine clearance, serum creatinine levels, graft rejection episodes, and graft and patient survival rates were evaluated.
Results: With regard to creatinine clearance, cold ischemia and anastomosis time, acute tubular necrosis, rejection episodes, and 1-, 2-, and 5-year posttransplant serum creatinine levels, there were no significant differences between the groups. Graft survival rates in the single renal vessel group were 92.9% at 1 year posttransplant and 78.3% at 5 years posttransplant; rates in the multiple renal vessel group were 93.1% at 1 year and 79.7% at 5 years. The corresponding patient survival rates were 95.5% (1 year) and 92.9% (5 years) for the single renal vessel group and 96.9% (1 year) and 87.2% (5 years) for the multiple renal vessel group.
Conclusions: Improved anastomosis and reconstruction techniques have allowed the safe transplant of multiple renal vessel grafts that may remain functional for many years.
Key words : Renal artery, Renal veins, Surgical anastomosis
Kidney transplant is currently the best treatment for end-stage renal failure. Some studies have indicated that grafts with multiple renal vessels (MRV) have a higher risk of vascular and urological complications during and after transplant.1,2 Recently, with improvements in surgical materials and anastomosis techniques, complications have been reduced and graft life has been extended.3 Here, we aimed to evaluate cases from our center of kidney transplants with MRV grafts, with a focus on subsequent graft survival, as well as the vascular and urological complications in the postoperative period.
Materials and Methods
Between November 1975 and July 2020, there were 3316 renal transplant procedures performed in our center. Of these, 2221 (67%) were male recipients, and 1095 (33%) were female recipients, with mean age of 32.03 years. With regard to kidney grafts, 716 (22.8%) were from deceased donors, and 2420 (77.2%) were from living donors. According to our criteria, donor candidates must be relatives (up to 4th degree) or the spouse of the recipient. Also, we perform paired kidney exchange transplant for recipients who are sensitized to their donors or have ABO-incompatible donors.
For our analyses, we divided the grafts into 2 groups. The first group (n = 2810) consisted of grafts with single renal vessels (SRV). In the SRV group, 643 grafts (22.9%) were from deceased donors, and 2167 grafts (77.1%) were from living donors. In the MRV group (n = 326), 73 (22.4%) were from deceased donors, and 253 (77.6%) were from living donors (Table 1). Blood supply and drainage of the grafts were evaluated with Doppler ultrasonography on posttransplant days 3 and 7.
Recipients were compared in terms of graft cold ischemia time, anastomosis time, posttransplant vascular and urological complications, development of acute tubular necrosis (ATN), creatinine clearance, serum creatinine level, and graft and recipient survival.
Multiple renal vessel grafts comprised 157 multiple renal artery grafts and 169 multiple renal vein grafts, and the details are described below. Of the 169 multiple renal vein grafts, 142 had 2 veins, and 27 had 3 veins.
Multiple renal artery grafts
Of the 157 multiple renal artery grafts, 145 had 2 arteries, 10 had 3 arteries, 1 had 4 arteries, and 1 had 5 arteries.
Grafts with 2 arteries
There were 145 grafts with 2 renal arteries, and these were transplanted as follows.
In 46 of the grafts with 2 arteries, the first artery was end-to-end anastomosed to the internal iliac artery (IIA), and the second artery was end-to-side anastomosed to the external iliac artery (EIA).
In 29 grafts, both arteries were end-to-side anastomosed to the EIA; in 26 grafts, both arteries were end-to-end anastomosed to the branches of IIA.
In 25 grafts, the first artery was end-to-end anastomosed to the IIA, and the second artery was end-to-end anastomosed to the inferior epigastric artery (IEA).
In 9 grafts, the first artery was end-to-side anastomosed to the EIA, and the second artery was end-to-end anastomosed to the IEA (Figure 1).
In 4 grafts, the ends of the 2 arteries were converted into a single duct; of these, 2 grafts were end-to-side anastomosed to the EIA, and 2 grafts were end-to-end anastomosed to the IIA.
In 4 grafts, the first artery was end-to-side anastomosed to the common iliac artery (CIA), and the second artery was end-to-end anastomosed to the IIA.
In 2 grafts, the first artery was end-to-side anastomosed to CIA, and the second artery was end-to-side anastomosed to the EIA.
Grafts with 3 arteries
There were 10 grafts with 3 arteries, and these were transplanted as follows.
In 4 grafts, the first 2 arteries were end-to-side anastomosed to the EIA, and the third artery was end-to-end anastomosed to IIA.
In 3 grafts, the first 2 arteries were end-to-side anastomosed to the EIA, and the third artery was end-to-end anastomosed to the IEA.
In 2 grafts, the ends of 2 arteries were converted into a single duct. In the first of these 2 combination grafts, the newly combined artery and the third artery were end-to-side anastomosed to the EIA; in the second of these 2 combination grafts, the newly combined artery was end-to-end anastomosed to the IIA, and the single artery was end-to-side anastomosed to the EIA.
In the tenth and final case of these 3-artery grafts, the first and second arteries were separately end-to-end anastomosed to the branches of the IIA, and the third artery was end-to-side anastomosed to the EIA.
Graft with 4 arteries
One graft had 4 arteries. The first artery was end-to-side anastomosed to the EIA. The second and third arteries were combined to be a single ostium. This single combined ostium and the end of the fourth artery were then converted into a new single duct and end-to-side anastomosed to the EIA.
Graft with 5 arteries
One graft had 5 arteries. The first and second arteries were end-to-end anastomosed to the branches of the IIA. The third and fourth arteries were end-to-side anastomosed to the EIA. The fifth artery was 0.6 mm in diameter, and so we ligated this fifth artery.
Multiple vein grafts
There were 169 renal grafts with multiple veins.
Of these, 142 grafts had 2 veins, and 27 grafts had 3 veins. These multiple renal vein grafts were transplanted as follows.
Grafts with 2 veins
There were 31 grafts with 2 renal veins. Both veins were end-to-side anastomosed to the external iliac vein (EIV) as a single ostium; otherwise, the 2 renal veins were sutured individually (Figures 2 and 3). The second veins of the other grafts were ligated.
Grafts with 3 veins
There were 27 grafts with 3 renal veins.
For 12 grafts, the first 2 larger veins were end-to-side anastomosed to the EIV, and the third vein was ligated.
In 15 grafts, the second and third veins were less than 5 mm in diameter and were safely ligated.
In 1 graft, the first vein was end-to-side anastomosed to the EIV, and the ends of the second and third veins were anastomosed to the EIV as a single ostium.
Grafts with multiple arteries and multiple veins
There were 4 grafts in the MRV group that had both multiple arteries and multiple veins. Two grafts had 3 arteries and 2 veins (Figure 4), 1 graft had 4 arteries and 2 veins (Figure 5), and 1 graft had 2 arteries and 2 veins (Figure 6).
Although the classical 4-quadrant anastomotic technique has been used as the anastomosis procedure until 1996, the 4-quadrant anastomotic technique modified by our team was used between 1996 and 2003 for arterial anastomosis.4,5 From 2003, the corner-saving technique developed by our team has been used.6 Decisions with regard to the artery for anastomoses are based on the atherosclerosis status and the flow rate of the recipient’s artery. For venous anastomosis we have used a 2-quadrant anastomotic technique.
After transplant, patients received standard triple immunosuppressive therapy (0.1 mg/kg tacrolimus or 5 mg/kg cyclosporine, 1.5 mg/kg prednisolone, and either 2 doses of 1 g mycophenolate mofetil or 2 doses of 720 mg mycophenolate sodium). Graft function was evaluated using daily clinical data and serum creatinine levels as well as renal Doppler ultrasonography performed on posttransplant days 3 and 7. In the period after discharge, graft function was evaluated at follow-up visits by measurement of serum creatinine levels and renal Doppler ultrasonography scans (Figure 7). Follow-up visits occurred once a week in the first 2 weeks, then once every 2 weeks for a 1-month period, once a month over the next 6 months, once every 3 months in the following year, and finally once every 6 months.
The Fisher exact test, the chi-square test, and Kaplan-Meier plots were used for evaluations and comparisons of data. We used IBM SPSS software for Windows for all calculations.
In our evaluation of MRV grafts, we noted in the early postoperative period that graft nephrectomy was performed in 1 patient to treat hyperacute rejection and in 2 patients to treat recurrent massive bleedings. In the early period after transplant, 4 patients required surgical exploration to resolve bleeding episodes. Of the patients who underwent surgical exploration, 2 had oozing-type bleeding, 1 had bleeding from the EIA, and 1 had bleeding from the renal venous anastomosis. All bleeding episodes were stopped with surgical sutures. Hematoma developed in 2 patients; however, in both patients, the hematoma resorbed during follow-up without additional procedures. Doppler ultrasonography performed early in the postoperative period showed polar arterial thrombosis in 6 patients. Because graft functions were not affected, patients required no further treatment. Nine patients developed a lymphocele at the surgical site, which we treated via catheter drainage. Urinary leakage occurred in 1 patient. Renal artery stenosis developed in 3 patients, and this required balloon angioplasty. Also, stent placement was required for 1 patient to treat recurrent angioplasties.
Table 2 shows results by group for creatinine clearance, serum creatinine levels, cold ischemia time, and incidences of posttransplant hypertension, acute rejection, ATN, and vascular and urological complications. No significant differences were detected between the groups in terms of creatinine clearance at 1 year (69 ± 26.2 vs 71 ± 27.6 mg/min), cold ischemia time (260 ± 189 vs 273 ± 171 min), or serum creatinine levels at 1 year (1.5 ± 1.09 vs 1.4 ± 1.13 mg/dL), 2 years (1.5 ± 1.06 vs 1.5 ± 1.12 mg/dL), and 5 years (1.8 ± 1.19 vs 1.7 ± 1.2 mg/dL) (P < .5 for all). In addition, no significant differences were detected in terms of posttransplant hypertension (P = .15), ATN (P = .61), or number of acute rejection episodes (P = .235).
The survival rates for the grafts were as follows: 92.9% at 1 year posttransplant and 78.3% at 5-years posttransplant for the SRV group, and 93.1% at 1 year posttransplant and 79.7% at 5 years posttransplant for the MRV group. The corresponding patient survival rates were 95.5% (1 year) and 92.9% (5 years) for the SRV group and 96.9% (1 year) and 87.2% (5 years) for the MRV group.
The ideal treatment method for end-stage renal failure is renal transplant. Ever since the first renal transplant, outcomes have dramatically improved with the discovery of organ perfusion and preservation solutions, the application of new surgical techniques, and the development of combined immunosuppressive regimens and antimicrobial agents.7,8
The presence of MRV, which was previously contraindicated because of the associated prolonged ischemia time and vascular anastomotic leaks, is no longer an indicator that would prevent transplant. The option for proceeding with transplant in cases with MRV has therefore increased the number of organs available for patients on wait lists. The rate of occurrence of multiple renal arteries in various autopsy series was found to be 23% and the occurrence rate of multiple veins was even less.9,10 In our series presented here, the rate of occurrence of multiple renal arteries was 5%.
We found no differences between MRV and SRV grafts in terms of long-term graft survival and function; therefore, we suggest that transplant of MRV grafts can be safely performed. However, some studies have found that MRV grafts, especially in cases of multiple renal arteries, could result in ATN because of prolonged ischemia time and surgery time.11,12 In our study, no significant differences were detected between SRV and MRV grafts in terms of the effects of ischemia time and anastomosis surgery time on graft survival and function.
Developments in surgical anastomotic techniques have allowed renal artery anastomoses to be performed differently on different arteries. Preferably, the main renal artery is end-to-side anastomosed to the EIA, end-to-side or end-to-end anastomosed to the IIA, or end-to-end anastomosed to the IEA. Although greater arterial length is an advantage in anastomoses to the IIA, incompatibility between the arteries to be anastomosed in terms of diameter is a disadvantage.13 Moreover, in multiple renal artery grafts, anastomosis of all arteries to the IIA may be difficult. Because CIA and EIA lumens are wide and long, these arteries readily enable the anastomosis of the main renal artery and polar arteries. The IEA is also a good alternative for the anastomosis of polar arteries.
Releasing the vascular clamps after main renal artery anastomosis prevents the unnecessary extension of ischemia time during the anastomosis of the polar arteries and decreases the risk of ATN.14 In our center, we use this method during transplant of multiple renal artery grafts. In deceased donors, multiple renal arteries can be removed by means of the Carrel aortic patch technique, in the form of a single opening.5 This allows for the anastomosis to be performed as a single opening, thus avoiding complications that may be caused by prolonged ischemia and anastomosis time. In our center, we also prefer the Carrel aortic patch method in MRV grafts from deceased donors. Another option is to join at back-table walls of 2 renal arteries as side-to-side anastomosis and create a single opening before transplant. However, this method is not widely preferred because it can result in thrombosis in both arteries.15 If the main renal artery or polar arteries are short or if there is iatrogenic injury to an artery, then polytetrafluoroethylene grafts can be used with confidence.13 In our case series, we did not need to use polytetrafluoroethylene grafts. If a polar artery has a very narrow diameter that is not suitable for anastomosis, then it can be ligated if the area it perfuses is insignificant.15 In our case series, there were no complications in 7 patients who had their polar arteries ligated.
Renal artery stenosis is a late complication that disrupts posttransplant graft function and can cause de novo hypertension in the patient. Interventional radiological methods play an important role in the diagnosis and treatment of patients with this complication.16 In our case series, after diagnoses were confirmed by angiography in 3 patients who had renal artery stenosis detected via Doppler ultrasonography during routine follow-up, treatments were successfully performed with interventional radiological methods. Surgical revision was not required.
The literature suggests that, if the graft has multiple renal veins and the smaller vein diameter is less than 5 mm, then the smaller vein can be ligated.10,17 This did not pose a risk. But if the all veins are the same caliber, the veins must be implanted as a single ostium or individually. Similar to the examples in the literature, we ligated 153 accessory veins of 126 grafts because the accessory vein diameters were less than 5 mm. In the postoperative period, we did not see any complication due to ligation of accessory veins.
Our results show that, in experienced hands with improved anastomosis techniques, kidney transplant with MRV grafts can be performed with a level of success similar to that of SRV grafts. Transplant of MRV grafts is no longer a contraindication, and survival rate of MRV grafts is similar to that of SRV grafts.
DOI : 10.6002/ect.2020.0339
From the Department of General Surgery, Baskent University, Ankara, Turkey
Acknowledgements: The authors have not received any funding or grants in support of the presented research or for the preparation of this work and have no potential declarations of interest.
Corresponding author: Mehmet Haberal, Baskent University, Department of General Surgery, Yukarı Bahçelievler, Mareşal Fevzi Çakmak Sok. No: 45, 06490 Çankaya/Ankara
Figure 1. Graft With 2 Arteries
Figure 2. Graft With 2 Veins
Figure 3. Graft With 2 Veins
Figure 4. Graft With 3 Arteries and 2 Veins
Figure 5. Graft With 4 Arteries and 2 Veins
Figure 6. Graft With 2 Arteries and 2 Veins
Figure 7. Doppler Image and Spectral Waveform of the Main Renal Artery in a Transplanted Kidney With 3 Arteries 2 Years After Transplant
Table 1. Arteries and Veins According to Number of Renal Vessels
Table 2. Comparison of Group Features After Transplant