Microvascular surgical techniques of renal transplant in rats have evolved over the past 5 decades to achieve successful rat renal transplant; these modifications have included surgical techniques to address the anatomic variations in the renal blood vessels and those to reduce ischemic and operation durations. Here, we review the surgical techniques of renal transplant in rats and evaluate the advantages and disadvantages of individual techniques of vascular and ureteric anas­tomoses. For this review, we performed a systematic literature search using relevant medical subject heading terms and included appropriate publications in the review. Since the first description of a rat model of renal transplant by Bernard Fisher and his colleagues in 1965, which used end-to-side anastomosis between the renal vein and renal artery to the recipient inferior vena cava and aorta, several vascular and ureteric anastomosis techniques have been modified. Vascular anastomosis techniques now include end-to-end anastomosis, use of donor aortic and inferior vena cava conduits, sleeve and cuff anastomoses, and application of fibrin glue. Likewise, restoration of the urinary tract can now be achieved by direct anastomosis of the donor ureter to the recipient bladder, end-to-end anastomosis between the donor and recipient ureters, and donor bladder cuff to the recipient bladder. There are advantages and disadvantages attributable to individual techniques. The range of vascular and ureteric anastomosis techniques that has emerged reflects the need for mastering more than one technique to suit the vascular anatomy of individual animals and to reduce operating time for achieving successful outcomes after renal transplant.

Key words : Blood vessels, Microvascular surgery, Nephrectomy

Introduction

Experimental models of renal transplant (RT) in rats have played a crucial role in enhancing the understanding of transplant immunology, ischemia-reperfusion injury, acute and chronic rejection, and effects of immunosuppressive agents on short- and long-term outcomes after RT. Several experimental rat models of RT have been previously described.^1-4 Recently, Grau and associates observed changes of antibody-mediated rejection and transplant glomerulopathy in Fischer 344-to-Lewis rat renal allografts, which were shown to have histologic features and immune complex deposits similar to those shown in human transplant biopsies with transplant glomerulopathy.⁵ Renal transplant in the rat remains an essential experimental tool for transplant research because of a number of advantages, including (1) improved long-term survival due to the use of inbred strains, (2) lower cost of experimental animals, (3) simple animal maintenance that does not require sophisticated facilities, (4) less critical requirements for aseptic surgery, and (5) well-established surgical techniques of vascular and ureteric anastomoses for RT.⁶

A rodent model of RT was first described in the rat (Rattus norvegicus) in 1965 by Bernard Fisher and Sun Lee at the American College of Surgeons Meeting in Chicago in 1961, with results subse­quently published in 1965.⁷ Although the model is significantly different from human RT, the physiologic and immunologic outcomes for the kidney are similar.

A functioning RT requires establishment of vascular flow through arterial and venous anasto­moses between donor blood vessels and recipient systemic circulation and urinary tract drainage via anastomosis to the recipient urinary tract. The technical aspects of RT in rats have undergone modifications to overcome the small size of the vessels and anatomic variations in the number of renal vessels, resulting in reduced complications and improved outcomes. In humans, the site of RT is heterotopic with extraperitoneal placement of kidney in the iliac fossa. Kidney retrieved from deceased donors have a patch of aorta, called a “Carrel’s patch,” that is absent in kidneys obtained from living donors. The renal artery is anastomosed to the external iliac artery in most cases and to the internal iliac artery in some cases and the vein to the external iliac vein. The donor ureter is then anastomosed to the native bladder.⁸ Similar principles of RT are used in rat models developed for experimental studies.

Microvascular surgical techniques have evolved to the extent that the postoperative survival of renal grafts in rats has become routine. Several surgical techniques of RT have evolved over the previous 50 years to overcome technical failures, indicating that each technique has its own advantages and disadvantages, with none being perfect for a particular case.⁹ It is paramount to be familiar with and master a wide range of surgical techniques to adapt to the variable vascular anatomy of the donor kidneys.¹⁰ In this paper, we reviewed the surgical techniques of RT used in rat models and evaluated the advantages and disadvantages of the individual vascular and ureteric anastomosis techniques.

Literature Search Strategy

A systematic electronic literature search was performed in PubMed (1946 to present), which included the following terms: renal transplant, kidney transplant, rat, animal model, surgical techniques, vascular anastomosis, and ureteric anastomosis. An additional search was made in Google scholar. All abstracts were obtained and assessed for relevancy to the review, and complete manuscripts were obtained as print or electronic copies. Relevant references were compiled in EndNote software (version X.7.4; Thomson Reuters, Philadelphia, PA, USA).

Donor Nephrectomy

For a successful RT, the kidney must be retrieved from the donor with precision, without causing injury to the renal artery and vein and with preservation of the blood supply of the ureter. Traction of the renal vessels and rough handling during mobilization of the kidney can lead to intimal injury, which predisposes to vascular thrombosis and ischemic infarction of the transplant. Under general or intraperitoneal anesthesia, through a midline laparotomy, the renal vessels, aorta, inferior vena cava (IVC), and ureter are mobilized, and the kidney is retrieved according to the proposed technique of RT (see Figure 1a). Sound knowledge of the anatomy of the retroperitoneum in the donor and recipient is paramount for successful retrieval and implantation techniques. Conventionally, the left kidney is used for transplant and the right kidney is discarded. Several authors have successfully used both kidneys retrieved from a single rat into 2 recipients, which can reduce the number of experimental animals by 50%, thereby achieving both ethical and economic advantages.¹¹ The kidneys are perfused in situ with any one of the available kidney perfusion solutions such as Marshall’s solution, University of Wisconsin solution, histidine-tryptophan-ketoglutarate, or Lifor solution (Lifeblood Medical, Inc., Adelphia, NJ, USA).^12,13

Right Native Nephrectomy in the Recipient Rat

It is common practice to perform left native neph­rectomy at the time of implantation of the transplanted kidney and then to perform right native nephrectomy after 10 days. The kidney is approached through a right flank incision and removed after ligating its pedicle with 3/0 Vicryl suture (Ethicon, Somerville, NJ, USA) (Figure 1b). However, simultaneous bilateral native neph­rectomies have been performed at the time of implantation of the native kidneys with successful outcomes.¹⁴ In another study, 1 week after RT, laparotomy was performed to inspect the transplanted kidney. If there was no evidence of vascular thrombosis and hydronephrosis, bilateral native nephrectomy was performed.¹⁵

Renal Transplantation

In the recipient, the implantation can be done in either an orthotopic or heterotopic position. In orthotopic RT, the kidney is transplanted in the normal place after undertaking native nephrectomy in the recipient, where end-to-end anastomoses between the renal vessels are performed. In heterotopic RT, the kidney is placed more caudally than the usual position in the flank, in which case the donor aortic and IVC cuffs are anastomosed to the recipient aorta and IVC (Figure 2). Under general anesthesia, access to the recipient aorta and IVC is gained through a midline incision. Left nephrectomy is performed to create space for the kidney transplant. The different surgical techniques of vascular and ureteric anastomoses in current practice are discussed below.

Vascular Anastomosis Techniques

End-to-side anastomosis
The first description of RT in rats was made by Fisher and Lee,7 which involved an end-to-side anastomosis between the right renal vein with a cuff of IVC and the renal artery with an aortic cuff to the recipient IVC and aorta (Figure 3a). Mobilization and occlusion of the aorta and IVC were required during vascular anastomoses. Subsequently, a similar technique was used by other authors, which achieved successful outcomes.^16,17 The ureter was anastomosed to the bladder through submucosal tunnelling, as in the Politano-Leadbetter technique. With this technique, the recipient’s right kidney is removed, with the left kidney removed after 7 days through a left flank incision.

End-to-end anastomosis
In 1969, French and Batchelor described a technique of orthotopic RT in rats, which involved direct end-to-end anastomosis of the renal vessels (Figure 3b). The left donor kidney was used because of the longer length of the renal vein.¹⁸ This technique avoided the need for mobilizing the recipient aorta and IVC, thus reducing the operating time. Splinting the renal vein with an epidural catheter has been used to visualize the venous lumen during the venous anastomosis.¹⁹ However, in the presence of multiple renal vessels, this technique has been associated with increased risk of vascular thrombosis.
Use of a donor aortic conduit Lee,²⁰ Stuart and associates,²¹ and White and associates²² described a technique whereby a segment of the donor aorta containing the renal artery was anastomosed to the side of the infrarenal aorta of the recipient (Figure 3c). This technique is particularly useful when there are 2 or more renal arteries present in the donor kidney. The renal vein was anastomosed end-to-side to the IVC. During the end-to-side anastomosis, the abdominal aorta and the IVC are clamped, thereby potentially leading to extensive ischemia-reperfusion injury of the recipient’s lower limbs and distant organs, particularly to the lungs. This complication is absent when end-to-end anastomosis of the renal vessels is carried out, where only the renal vessels are clamped.²³

Sleeve anastomosis technique
This technique was developed in an attempt to reduce the warm ischemia time where a suture attached to the end of the recipient’s artery is inserted to the lumen of the donor artery and pulled through the wall, thereby telescoping (sleeve/telescope technique) one into the other^24-27 (Figure 3d). Choi and associates28 compared the sleeved microvascular technique with the standard end-to-end technique and concluded that this technique was easier to perform, was equally effective, and reduced warm ischemia time. Lauritzen and associates have reported similar findings.²⁷

Cuff technique
The problems encountered after sutured vascular anastomoses were bleeding from the anastomoses sites and prolonged warm ischemia time. To obviate these problems, Kamada²⁹ and Savas and associates³⁰ described a nonsuturing technique (cuff technique) using small polyethylene cuffs for anastomosing the renal vessels and reported considerable reduction of warm ischemia time (mean of 12 min) (Figure 3e).

Donor aortic and IVC conduits
In this technique, both the donor aorta and IVC are used as conduits to perform an end-to-side venous anastomosis with the recipient aorta and IVC. In one study, graft survival was 87% at 3 days and 80% at 120 days. Patency was 80% at 120 days, and histologic examination revealed normal renal architecture and parenchyma, with no evidence of ischemic injury. This technique offers a refinement of previous techniques and is reliable, flexible, and can be easily learned by novice microvascular surgeons (Figure 3f and 3g).^31,32 The advantages of employing aortic and IVC conduits are summarized in Table 1 and Table 2.

Combination of techniques
The use of a combination of the sleeve technique for the artery, cuff technique for the vein, and over-a-stent technique for the ureter effectively reduces the operating and warm ischemia durations.³³ In a study involving 20 rats, total vascular (artery and vein) anastomosis time was 5.35 ± 0.59 minutes, of which the artery time was 4.30 ± 0.40 minutes and the vein time was 1.05 ± 0.20 minutes. The ureter anastomosis time was 1.0 ± 0.1 minutes. This has been claimed to be the fastest technique published in the literature.

Application of fibrin glue
To reduce the warm ischemia time, the renal artery can be anastomosed using 5 to 6 interrupted 10/0 nylon sutures and fibrin glue devoid of thrombin, which is applied to the anastomosis site instead of the conventional 8 to 9 sutures. In one study, the warm ischemia time was 23.9 ± 0.9 versus 29.7 ± 1.1 minutes (P < .01), and the patency of the vessels was well maintained.³⁴

Ureteric Anastomosis Techniques

Restoration of the urinary tract represents one of the major problems in rat RT, as the extremely narrow caliber of the ureter leads to complications such as urine leak, ureteric necrosis, and ureteric stenosis, resulting in possible death or deterioration of renal function from hydronephrosis. The techniques employed include direct implantation of the ureter to the urinary bladder, anastomosis of cuff of donor bladder containing ureter to the recipient bladder, and end-to-end anastomosis between the donor and recipient ureters.

Direct implantation
Direct implantation of the donor ureter into the recipient bladder can be performed by piercing the bladder with a 21-gauge needle, allowing the tip of a curved artery forceps to be inserted through the bladder. The ureter is pushed through the hole in the bladder and the periureteral tissue is stitched to the exterior wall of the bladder. The donor ureter is allowed to retract inside the bladder (Figure 4a).^7,35

The paraureteric blood vessels, which are often the source of postoperative hematuria, should be ligated. In another technique, the end of the ureter is tunnelled through the bladder and anchored to the wall with 6/0 Vicryl suture. The cystotomy is closed with similar material.⁷ Alternatively, the spatulated ureter is anastomosed to the bladder mucosa with 3 to 4 interrupted 10/0 nylon sutures, and the anastomosis is buried by placing a purse-string suture in the bladder wall around the anastomosis site.¹⁵

Bladder cuff
An anastomosis between the cuff of donor bladder attached to the ureter and the dome of the recipient bladder facilitates the procedure, making anasto­mosis easy and thus eliminating the need for stenting (Figure 4b).^36,37 The donor bladder cuff is anasto­mosed end-to-end to the dome of the recipient bladder after excising a cuff. A full thickness end-to-end anastomosis is carried out by using continuous 6/0 Vicryl sutures. The cuff of the donor bladder should be kept as small as possible to avoid ischemic necrosis. The presence of bleeding from the donor bladder at the time of nephrectomy can confirm an intact ureteric blood supply. This technique is easier to perform, although it has shown risk of ischemic necrosis of the donor bladder cuff, urine leak, and fatal outcomes.³⁵

End-to-end anastomosis
French and Batchelor¹⁸ and White and associates²² performed direct end-to-end anastomosis of donor and recipient ureters with no splinting of the ureteric anastomosis (Figure 4c). This technique was based on preliminary experiences with 34 rat kidney transplants showing success in 32 transplants. The end-to-end technique requires a more meticulous technique because of the inherent risk of necrosis leading to urine leak, stricture, and obstruction caused by blood clots, leading to hydronephrosis with consequent graft loss.

Pyeloureterostomy
In one study, instead of dividing the ureter in the middle between the kidney and bladder (method 1), the anastomosis was performed close to the renal pelvis after cutting the ureter obliquely (method 2), which enlarged the diameter of the ureteric anastomosis by 2-fold. The incidence of stenosis of ureteric anastomosis was 12.5% (3/24) using method 1, whereas this complication was avoided completely (0/45) using method 2. Furthermore, the risk of injury to the ureter was reduced, as isolation of the ureter was limited.³⁸

Preservation of gonadal artery
To preserve the ureteric blood supply, the donor gonadal artery can be left intact in continuity with the aorta or the renal artery, with the distal end being ligated.³⁹

Ureteric stents
End-to-end anastomosis of the donor and recipient ureters with the use of 5/0 plain catgut as ureteric stent has yielded successful outcomes.⁴⁰ However, urinary tract calculi formation and infection remain inherent risks with nonabsorbable stents.⁴¹

Discussion

Several modifications in RT surgical techniques in rats have been made to overcome the problems posed by occurrence of variations in vascular anatomy, to reduce the warm ischemia time, to achieve high success rates in transplant survival, to prevent RT complications (hemorrhage, vascular thrombosis, aneurysm formation, urine leak, and paraplegia), and to shorten the learning curve of the surgeon. The use of surgical techniques that can be performed with a short warm ischemia time contributes to a better allograft outcome. However, the tolerance of the transplant to warm ischemia time is also dependent on the species of the rat.⁴²

Various microvascular techniques of arterial anastomosis have been described, including end-to-end anastomosis between donor-to-recipient renal arteries (sutured, cuffed, or sleeved techniques), end-to-side anastomosis between the donor recipient artery with an aortic patch to the recipient aorta, interposition of donor aortic segment with the renal artery between the transacted segment of recipient aorta, and end-to-side anastomosis between donor aortic conduit containing renal artery and the recipient aorta.^{7,40,41,43,44} The presence of more than 1 renal artery, which is not uncommon, makes end-to-end anastomosis impossible because of the narrow caliber and risk of thrombosis.45 Karatazas and associates used donor aortic conduit attached to the renal artery and anastomosed end-to-side to the recipient abdominal aorta, which resulted in a survival rate of 87% at 15 days with no evidence of ischemic injury on histology.¹⁵

Blom and Orloff have described their experience of using donor IVC as a conduit to perform an end-to-side venous anastomosis in kidney transplant in rats. Survival was 87% at 3 days and 80% at 120 days. Patency was 80% at 120 days, and histologic examination revealed normal renal architecture and parenchyma, with no evidence of ischemic injury. This technique offers a refinement of previous techniques, is reliable and flexible, and can be easily learned by novice microvascular surgeons.³¹

Mastering all surgical techniques of restoration of continuity of the urinary tract by end-to-end anastomosis, with or without stent placement, ureter-bladder patch to recipient bladder, and ureteric implantation into the bladder increases the chance of successful ureterovesical anastomosis and prevents complications such as urine leak, ureteric stenosis, hydronephrosis, calculi formation, pyelonephritis, pyonephrosis, and death. Preservation of the blood supply to the ureter is paramount in avoiding ureteric necrosis, stenosis, and urine leak. Gentle handling of the ureter with preservation of periureteric fat and visible blood vessels is important. Preserving the testicular artery in the donor aortic stump helps to maintain blood supply of the ureter.⁴⁰ A well-organized training program with a staged micro­vascular anastomosis skill development curriculum has been shown to be beneficial to the trainees.⁹

We have reviewed the published literature on the surgical techniques of RT in the rat and have shown that there are several variations regarding vascular and ureteric anastomosis techniques. It is essential to understand the advantages and disadvantages of each technique and adopt a method that would be technically reproducible, leading to a viable trans­plant. Learning more than 1 technique of vascular and ureteric anastomoses is essential, allowing one to transplant kidneys with anatomic variations, thereby increasing the possibility of maximum utilization of kidney and animals.

For the development of a successful and repro­ducible model of RT in rats, it is essential for the surgical team to acquire expertise in this field, which comprises a steep learning curve. It is imperative to have an understanding of anesthesia, maintenance of fluid balance, and temperature regulation in addition to having mastery of the precise microvascular surgical technique, as these all have significant effects on outcomes. However, a technique adopted in a particular institution should be mastered fully to produce reproducible and reliable results for a particular model.

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