Year : 2013 | Volume
: 24 | Issue : 2 | Page : 247--253
The new technique of using the epigastric arteries in renal transplantation with multiple renal arteries
Mohammad Ali Amirzargar1, Hooshang Babolhavaeji1, Shahriar Amir Hosseini1, HabibMousavi Bahar1, Mahmood Gholyaf2, Farahnaz Dadras2, Farhad Khoshjoo2, Mahnaz Yavangi3, Nasibeh Amirzargar4,
1 Department of Urology, Hamadan University of Medical Sciences, Hamadan, Iran
2 Department of Nephrology, Hamadan University of Medical Sciences, Hamadan, Iran
3 Department of Gynecology, Hamadan University of Medical Sciences, Hamadan, Iran
4 Shahid Beheshti University of Medical Sciences, Tehran, Iran
Mohammad Ali Amirzargar
Department of Urology, Hamadan University of Medical Sciences, Hamadan
The most common anatomic variant seen in the donor kidneys for renal transplantation is multiple renal arteries (MRA), which can cause an increased risk of complications. We describe the long-term outcomes of 16 years of experience in 76 kidney transplantations with MRAs. In a new reconstruction technique, we remove arterial clamps after anastomosing the donor to the recipient«SQ»s main renal vessels, which cause backflow from accessory arteries to prevent thrombosis. By this technique, we reduce the ischemic times as well as the operating times. Both in live or cadaver donor kidneys, lower polar arteries were anastomosed to the inferior epigastric artery and upper polar arteries were anastomosed to the superior epigastric arteries. Injection of Papaverine and ablation of sympathic nerves of these arteries dilate and prevent them from post-operative spasm. Follow-up DTPA renal scan in all patients showed good perfusion and function of the transplanted kidney, except two cases of polar arterial thrombosis. Mean creatinine levels during at least two years of follow-up remained acceptable. Patient and graft survival were excellent. No cases of ATN, hypertension, rejection and urologic complications were found. In conclusion, this technique can be safely and successfully utilized for renal transplantation with kidneys having MRAs, and may be associated with a lower complication rate and better graft function compared with the existing techniques.
|How to cite this article:|
Amirzargar MA, Babolhavaeji H, Hosseini SA, Bahar H, Gholyaf M, Dadras F, Khoshjoo F, Yavangi M, Amirzargar N. The new technique of using the epigastric arteries in renal transplantation with multiple renal arteries.Saudi J Kidney Dis Transpl 2013;24:247-253
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Amirzargar MA, Babolhavaeji H, Hosseini SA, Bahar H, Gholyaf M, Dadras F, Khoshjoo F, Yavangi M, Amirzargar N. The new technique of using the epigastric arteries in renal transplantation with multiple renal arteries. Saudi J Kidney Dis Transpl [serial online] 2013 [cited 2019 Nov 16 ];24:247-253
Available from: http://www.sjkdt.org/text.asp?2013/24/2/247/109565
Kidney transplantation is the treatment of choice for the vast majority of patients with end-stage renal disease (ESRD). During the past few decades, graft and patient survival have significantly improved because of standardization in surgical technique and refinements in immunosuppressive therapy, organ preservation and antimicrobial therapy. One of the current challenges with donor grafts are the result of anatomic variants, including multiple renal arteries (MRA), multiple ureters, horse-shoe kidneys, en bloc pediatric kidney grafts or ureteral anastomosis to an ileal or colon conduit.  Of these variants, MRA is the most common. According to several autopsy series, its incidence ranges between 18% and 30% of all potential kidney donors.  MRA is unilaterally found in 25% of the population and bilaterally in 10%.  In renal grafts with a single artery, vascular complications range from 1 to 16%  and urologic complications occur in 2-10%.  But, renal transplantations with multiple arteries have been considered a relative contraindication due to an increased risk of vascular and urologic complications.  Compared with procuring kidneys with a single artery, the presence of multiple arteries may lead to longer operative times for more complicated dissection, and ischemic times are also longer because of the requirement for a more complex implantation. The complications of ureteral ischemia as a result of impaired perfusion due to loss of donor polar arteries make revascularization of these vessels attractive and a must do procedure. ,,
The transplant surgeon is required to use special vascular surgical techniques to transplant kidneys with anomalous arterial anatomy because of the limitations in kidney donors. Various techniques have been described for reconstruction of MRA.  The out-of-body vascular reconstruction (bench technique) or in situ reconstruction can be used. No significant difference in complications and graft survival rates were demonstrated between various techniques. ,
Our study describes the new surgical technique and long-term outcomes of live donor and cadaver renal allografts with multiple arteries in which the donor polar arteries was anastomosed to the recipient epigastric arteries after arterial declamping and injection of papaverine. The aim of this study was to compare the success and complication rate of this technique with the outcomes of other reconstruction techniques for multiple artery renal allotransplantation and the outcomes in which the donor kidney had single renal artery.
Materials and Methods
In this prospective sequential experimental study, we investigated donor/recipient pairs who underwent kidney transplantation with MRAs from June 1994 to June 2010. The study was conducted according to a protocol approved by the local institutional ethical committees.
From 502 patients diagnosed with ESRD who were referred to our Department of Urology, 76 donors who had MRAs were enrolled into this study to compare the success and complication rates of our surgical technique with the outcomes of other reconstruction techniques. During the pre-operative donor evaluation, medical, surgical and psychosocial suitability for live donation was assessed. The potential donors who were eligible for inclusion in the study underwent full medical evaluation, including donor-recipient human leukocyte antigen matching and a cross-match test.
We included only primary adult kidney recipients to obtain a homogenous transplant study population. We excluded recipients of kidney transplants performed in conjunction with other organs, recipients of en bloc pediatric kidney transplants and pediatric kidney recipients. Written detailed informed consent was obtained from each patient before initiation of treatment. Operating time for donors and recipients was calculated as time from incision to skin closure. The total operating time (donor operating time plus recipient operating time) was also calculated to assess the overall effect of single versus MRAs on overall operating room use.
At the beginning of the operation, a Foley catheter was inserted and the donor was placed in a lateral decubitus position on the operating table. The kidney rest was elevated and the table was flexed to maximize exposure of the flank. Appropriate additional padding for the legs, arms and axilla was applied. The incision underneath the 12 th rib approaching the dorsal lumbar was performed. Throughout the operation, fluids were liberally administered to maintain the donor's urine output of at least 2 mL/kg/h. The kidney was preserved by hypothermic, and hyperosmolar washout solution. Anastomoses of MRA in recipients were performedwith several methods. In two cases, the polar renal artery was anastomosed to the main renal artery to a unique arterial ostium generated with the bench technique and the main renal artery was then anastomosed into the recipient vessel. In two cases, polar arterial anastomoses were performed to the common iliac artery, in two cases arterial anastomoses were performed to the external and internal iliac arteries and in two cases reconstruction was performed as end-to-side anastomosis of smaller accessory arteries to the main renal artery. In 68 cases, epigastric artery grafts were used to reconstruct MRAs. In this principal method, donor main renal artery was anastomosed to the recipient internal iliac artery and donor main renal vein was anastomosed to the recipient internal iliac vein. Then, we declamped the arteries to maintain blood and urine flow. Backflow from the accessory arteries prevented thrombosis. We also injected 5000 IU heparin subcutaneously during surgery, which was continued for three days after transplantation and was followed by warfarin administration. After clamping both sides of the epigastric artery, 0.5 cc papaverine as a smooth muscle relaxant was injected intraluminaly and the sympathic nerves of these arteries were ablated for dilatation and preventing post-operative arterial spasm. Finally, donor lower polar arteries were anastomosed to the inferior epigastric artery. In cases that the donor had triple renal arteries, the upper polar arteries were anastomosed to the superior epigastric arteries. Intraoperatively, the flow was measured by a flowmeter, which showed a high flow on the polar and the main renal arteries. Color Doppler ultrasonography was routinely performed on the second or third day after transplant in order to evaluate the vascular flow as well as the urinary system. In the post-operative course, renal DMSA scan and DTPA scan following intravenous injection of 12 mCi of Tc-99 was performed the next day and2 weeks and one month later.
Following the transplantation, all patients received standard triple-drug immunosuppressive therapy consisting of a calcineurin inhibitor (cyclosporine: sandimune), azathoprine (imuran) or mycophenolatemofetil (cellcept), and steroids (prednisolone). In addition, recipients of cadaver or living unrelated donor grafts received a seven-day induction course of either polyclonal or monoclonal antibodies.
Patients were followed-up at the outpatient unit, initially once a week during the first month after discharge from the hospital, then once a month for the following three months and then each six months for the entire life. All patients had at least two years' follow-up after transplantation by the end of 2010.
Routine laboratory tests including blood urea nitrogen (BUN), creatinine levels and complete blood count (CBC), especially for platelet count, were obtained. We compared the following variables: patient and graft survival, mean creatinine levels, incidence of acute tubular necrosis (ATN) and post-transplant hypertension, number of rejection episodes and the rates of early and late vascular and urologic complications. Delayed graft function was defined as the need of at least one dialysis session after transplant. The diagnosis of ATN was confirmed by renogram and ultrasound in all cases. Patients were considered to have hypertension if they were taking at least one anti-hypertensive medication or had a blood pressure 160/90 mmHg. The incidence of rejection was based on the first biopsy-proven rejection episode. Urologic complications included ureteral obstruction, urinary leak, calyceal fistula and ureteral necrosis. Vascular complications included renal artery or renal vein thrombosis, bleeding and arterial stenosis. Quality of graft function was assessed by estimated glomerular filtration rate (GFR). Graft loss was defined as the return to permanent dialysis or death.
All analyses were performed using the statistical software SPSS for Windows version 11.5. Continuous variables were expressed as means (standard deviation) or medians (range). A comparison of the effects of various reconstruction techniques on patients with MRA was performed by chi-square test and a comparison of the effect of each technique before and after it was conducted by paired t-test. P-values <0.05 were considered statistically significant.
We identified 502 donor-recipient pairs who underwent kidney transplants during a 16-year period. Of the 76 patients who received allografts with MRAs, 65% were male and 35% were female. The average recipient age was 44 ± 4.6 years (range 18-54 years); 73 cases of donors had double arteries and three cases had triple arteries. Seventy-four (97.3%) patients received grafts from living related (n =23) or living unrelated (n =51) donors. Two (2.6%) renal transplants were derived from brain-dead donors with multiple arteries. The mean follow-up was 5.7 years (two to ten years).
During operation, the warm ischemia time in our cardinal method was 44 ± 5.1 s (range 30-60 s) and the cold ischemia time was 17.8 ± 1.2 min (range 15-20 min). Warm and cold ischemic times in the other techniques were doubled (60-120 s and 30-45 min, respectively). Operating times for both donors and recipients in transplantation of MRAs with epigastric grafts were significantly shorter when compared with the other techniques.
In the principal group, no blood transfusion during operation was performed. We noted no significant differences in the immediate post-operative urine output when comparing the study groups. There was no significant difference in the length of hospitalization between the multiple artery groups and the single artery group (P >0.05). All donors were discharged after one to two days of post-operation and all recipients were discharged 14-30 days after transplantation.
DTPA renal scan, DMSA and color Doppler ultrasonography in all patients who had epigastric arteries anastomoses showed good perfusion and function of the transplanted kidney without urine leak. Successful revascularization of all areas of the transplanted graft was confirmed with DTPA scanning. Dynamic images showed normal perfusion of the transplanted kidney. Static views showed normal-sized transplant with homogeneous cortical radiotracer uptake with secretary and excretory function in proper times. No evidence of urinoma and rejection was seen.
Routine laboratory tests including mean creatinine levels, BUN, platelet count, mean systolic blood pressures and complication rates were allin acceptable ranges in our principal group. Mean creatinine levels at the first year and at the last follow-up were 1.79 ± 0.72 mg/dL and 1.98 ± 0.77 mg/dL, respectively. Early (on Days 1-6) and late (at 1, 3 and 6 months, and at 1, 2 and 3years) median serum creatinine levels were not significantly different for single versus MRA grafts. The mean systolic blood pressure at the last follow-up was 132.3 ± 24.8 mmHg.
Following epigastric anastomoses of accessory renal arteries before injection of papaverine and anticoagulant, two vascular complications occurred (2.6%) in the first week after transplantation, including lower pole renal artery thrombosis in one patient and upper pole renal artery thrombosis in one case of triple arteries that was successfully treated by anticoagulant therapy. In one of the recipients, post-operative bleeding from the anastomosis occurred, which stopped spontaneously without requiring surgery. There were no other complications including urologic complications.
We noted no delayed graft function in this group of recipients. Differences between rejection rates at six months, overall rejection rates and rejection-free survival rates were not sta-tistically significant for the single versus MRA groups. Graft survival rates at 1 and 5 years post-transplant were 100% in our technique. None of the recipients returned to dialysis.
After a follow-up of at least two years, all the recipients kept normal kidney function without ATN, renal artery embolism, vascular stenosis, urinary fistula and ureter necrosis. None of the recipients died from any of these complications.
In this study, we surveyed 76 kidney transplantations performed with MRAs. Our results showed shorter ischemic time during the operation without increased post-surgical complications and excellent patient and graft survival rates after anastomosing accessory arteries to epigasteric arteries after declamping and injection of papaverine.
According to several large autopsy series, the incidence of MRAs ranges from 18 to 30%.  Our 15% (76/502) rate of renal transplantations with MRAs from June 1994 to June 2010 is considerably lower than those of historical experiences. We found double arteries in 14% of the donors and triple arteries in 1%. Theoretically, there should be a higher risk of surgical and medical complications to the living donor as well as the recipient while using the renal graft with multiple arteries.  At the beginning of the renal transplantation era, using grafts with MRA was considered as a contraindication. Nowadays, multiple vessels are not considered as a major problem anymore, neither to open nor to laparoscopic nephrectomies. ,
Several techniques for bench or in situ reconstruction of MRAs have been described in order to reduce the incidence of complications: End-to-side anastomosis of the smaller artery to the main artery, side-to-side anastomosis of similar-sized arteries, anastomosis to the recipient internal, external or common iliac and hypogastric arteries were recommended. The proximal and distal ends of the inferior epigastric artery have also been used successfully for end-to-end anastomosis to small polar vessels with arterial inflow inferiorly from the femoral artery and superiorly from the internal mammary artery.  These technical refinements have significantly expanded the pool of cadaver, living related and living unrelated donors.
Deceased donor kidneys with MRAs are routinely used for transplantation, and their long-term outcomes are reportedly not different from single artery grafts. The renal arteries from deceased donors are longer and are frequently attached to an aortic patch, which makes reconstruction technically easier. In living donor kidneys with MRAs, there is an increased risk of injury from more extensive dissection during the nephrectomy. The requirement for complicated vascular reconstruction and more difficult anastomosis at the time of implantation impose additional ischemic injury and subsequent reperfusion injury. In our study, the anastomosis of the polar arteries to the epigastric arteries after declamping avoids prolongation of the ischemia time that occurs with other surgical and microsurgical techniques of intracorporeal and ex vivo surgeries. By this technique, we reduce warm and cold ischemic times as well as the total operating times, which were reported to be significantly longer among patients with MRAs who operated by other techniques. ,,,,
The longer, technically more challenging procurement operation of kidneys with MRAs may also expose the donor to added risk for complications, such as more graft injury,  bleeding and the need for blood transfusion that were not seen during our principal surgical technique.  The post-implantation recovery from this injury may increase the incidence of ATN, which results in more inflammation, increased graft immunogenicity, more rejection episodes, premature graft loss and prolonged hospitalization. , These perioperative injuries may collectively lead to a reduced function and lower long-term survival in the transplanted kidneys with MRAs than the kidneys with single artery.  In the technique we used for reconstruction and anastomosis of MRAs, no problems in short- and long-term kidney graft outcomes were seen. Graft survival was excellent without any rejection. We used DTPA scan to evaluate perfusion and function of the transplanted kidneys. An angiogram of the renal arteries was not performed as a work-up of graft dysfunction in our patients because of its toxicity and invasion.
It is reported that use of multiple arteries in renal allografts is associated with a significantly higher mean serum creatinine at one year.  But, our results showed acceptable mean creatinine levels during at least two years of follow-up after transplantation by epigastric anastomosis.
Multiple artery renal transplants, especially triple artery transplants, and certain pedicle restorations are also associated with a high risk of vascular complications, , including arterial thrombosis, renal artery stenosis  and an increased risk for renovascular hypertension.  We observed two cases of arterial thrombosis, one in the superior pole and one in the inferior pole. It is possible that small accessory arteries could be thrombosed after transplant, and these might not have been recognized by routine ultrasound imaging.  Anythromboses of these small accessory vessels could decrease graft function and survival. But, good graft function following our technique showed a lesser possibility of small artery thrombosis, which can be as a result of backflow from the accessory arteries after declamping during surgery. Furthermore, we did not find a difference in the vascular complication rate between cadaver and living donor kidney grafts.
The presence of multiple arteries is a risk for late renal artery stenosis, especially in grafts with prolonged preservation time.  Anastomosing the smaller artery to the side of the dominant artery or performing two separate arterial anastomoses theoretically could run the risk of graft artery stenosis and ischemic injury, which might lead to poor graft survival.  In our technique, we injected 0.5 cc papaverine in the lumen of epigasteric arteries and ablated sympathic nerves of these arteries to dilate them and avoid post-operative arterial spasm.
Premature atherosclerotic occlusion of the small, accessory and lower polar arteries may hypothetically lead to late, ischemic, distal ureteral strictures.  There was a trend toward more ureteral complications in MRA reconstruction. A 17% incidence of ureteral complications among kidneys that had reimplanted accessory arteries was reported.  In particular, polar arteries can cause infarction, infection and urologic complications, such as calyceal or ureteral fistulas and ureteral necrosis, increasing morbidity and graft loss.  Urologic complications did not increase in our transplant recipients and there have been no signs of ureteral problems at all.
The small number of patients in groups with other surgical techniques precluded a meaningful comparison. Assessment of such an issue should be considered in future studies. This study is limited by its small sample size of more than two renal arteries. Evaluation of the effect of number of renal arteries on the outcomes can also be considered as the subject of future studies.
Based on our results, kidney grafts with multiple arteries can be implanted with short- and long-term results equal to those with single arteries. We found no difference between patient and graft survival, incidence of ATN, post-operative hypertension, rejection, vascular and urologic complications or serum creatinine levels.
In conclusion, the findings of this study suggest that live and cadaver donor kidneys with MRAs can be safely and successfully utilized for renal transplantation by anastomosing the accessory arteries to the epigastric arteries after declamping and injection of papaverine. Our technique may be associated with a lower risk of rejection, better graft function and superior long-term survival compared with other methods.
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