Received: 15 February 2017
|
Revised: 31 March 2017
|
Accepted: 11 April 2017
DOI: 10.1111/vsu.12705
ORIGINAL ARTICLE - CLINICAL
A Carrel patch technique for renal transplantation in cats Casey Budgeon, DVM | Robert J. Hardie, DVM, Diplomate ACVS and ECVS | Jonathan F. McAnulty, DVM, MS, PhD Department of Surgical Sciences, University of Wisconsin-Madison, Madison, Wisconsin Correspondence Jonathan F. McAnulty, Department of Surgical Sciences, School of Veterinary Medicine, University of WisconsinMadison, 2015 Linden Drive, Madison, WI 53706. Email:
[email protected]
Abstract Objective: To evaluate the feasibility of a Carrel patch method in feline renal transplantation. Study design: Descriptive case series. Animals: Nine healthy donor cats and 9 client recipient cats with chronic renal failure. Methods: Renal transplantation was performed in 9 cats with chronic renal failure after collection of a donor’s left kidney with a Carrel patch technique. A patch of donor aortic wall was removed with either 2 or 1 renal artery (ies) (n 5 1 and 8 cats, respectively) central to the patch, with a cuff of tissue (1 mm) protruding from the base of the vessels. The Carrel patch was implanted in recipient cats with an end-toside artery-to-aorta anastomosis, in a simple-continuous pattern of 9-0 nylon. The renal vein and ureter were implanted as previously described. Results: All donors and recipients survived surgery without vascular complication. Conclusion: The Carrel patch is a novel approach allowing the harvest of kidneys with multiple renal arteries. The technique also simplified the implant procedure, potentially decreasing the risks of bleeding and thrombosis.
1 | INTRODUCTION Renal transplantation for treatment of feline chronic renal failure was first performed in 1987, and described by Gregory in 1992.1 The technique originally relied on an end-toend renal-to-iliac artery and ureteral drop-in anastomoses but has evolved substantially. Improvements in technique and patient management have decreased morbidity and mortality, and reduced the technical challenges associated with this procedure.2,3 The most common method currently used for renal transplantation in cats involves an end-to-side anastomosis of the renal artery to the aorta (aETS) and vein to the vena cava.3 This method reduced complications such as ipsilateral pelvic limb hypothermia, edema, pain, and paresis or paralysis, reported to occur in 12%-62% of cats operated with the original technique.1-4 The end-to-side method was also considered simpler and faster,4 although it did not eliminate all complications associated with vascular anastomoses, Veterinary Surgery. 2017;1–6.
particularly bleeding at the anastomosis site and thrombosis of the renal artery.5 An additional challenge in kidney graft implantation arises if the donor’s kidney has multiple arteries. In general, the left kidney is preferred for the greater length of its renal vein.1,6 The right kidney is selected for transplantation when the left kidney has multiple arteries or bifurcates close to the aorta. However, the right kidney poses a technical disadvantage due to a greater disparity in artery to vein length, and best fits the arrangement of vessels when implanted on the right side of the abdomen. In our experience, implantation of right kidneys with venous anastomosis on the right side is more technically challenging than for a left kidney placed on the left side of the abdomen. In addition, donor cats with multiple renal arteries for both kidneys would currently not be considered as donors. The Carrel patch is a vascular anastomosis technique first described in man by Alexis Carrel in 1905,7 and widely used
wileyonlinelibrary.com/journal/vsu
C 2017 The American College of Veterinary Surgeons V
|
1
2
|
BUDGEON
ET AL.
in vascular surgery, such as liver transplantation, multiple organ procurements, and correction of aneursyms.8,9 Applied to renal transplantation, the Carrel patch technique entails removal of a patch of aorta centered over the renal artery (or arteries). In humans, this method is thought to facilitate reimplantation10 over standard aETS anastomosis and reduce the risk of thrombus formation.7 This approach could allow the use of feline kidneys fed by multiple arteries, if found safe for the donor and recipient animal. The purpose of this study is to describe the Carrel patch technique for feline kidney transplantation, and report the short-term outcomes and complications in an initial case series.
2 | MATERIALS AND METHODS 2.1 | Selection and screening Medical records of all renal donor cats operated between 1995 and 2016 were reviewed to assess the incidence of multiple left renal arteries or bilateral double arteries as detected by angiography or during surgery. Preoperative evaluation of recipients included a complete blood count, serum chemistry profile, urinalysis with culture and sensitivity, thyroid hormone (T4) level, feline leukemia virus (FeLV), and feline immunodeficiency virus (FIV) status, toxoplasmosis titers, blood type, ECG and echocardiogram, blood pressure measurement (and appropriate treatment if hypertensive), thoracic and abdominal radiographs, and abdominal ultrasound. If needed, dental prophylaxis was performed prior to transplantation. Recipients were transfused with matched packed red blood cells or whole blood prior to surgery. All cats were administered cyclosporine A per os (starting at 4 mg/kg and adjusted based on trough levels) 2 days prior to transplantation, and cyclosporine trough levels were monitored daily thereafter.3,11 All donors were screened for blood type and compatibility with the recipient cat. A general health assessment included complete blood count, serum chemistry profile, urinalysis with culture and sensitivity, FeLV and FIV status, abdominal radiographs and ultrasound, and toxoplasmosis titers.
2.2 | Surgical technique The anesthesia protocol was determined by the attending anesthesiologist based on previous recommendations.2,12 Donor cats were positioned in dorsal recumbency and a ventral midline celiotomy performed. The right and left kidneys were examined for gross pathology. The left kidney was used in all cats. Perirenal fat was dissected to expose the renal artery and vein. The ureter was transected and ligated
F I G U R E 1 Use of a Carrel patch technique to harvest a left kidney with a double renal artery
near its entrance to the bladder (n 5 1), or resected along with the ureteral papilla (n 5 8).2 All preparations were completed prior to vessel occlusion, to minimize the time of occlusion of the donor aorta and warm ischemia of the graft. A Satinsky vascular clamp was placed on the aorta, tangential to its long axis, to isolate the renal artery(s) of the left kidney without occluding the right renal vessels (Figure 1). The aorta was incised lateral to the renal artery(s) with a specialized scalpel blade (Beaver mini-blade 6900, BeaverVisitec, Waltham, Massachusetts) and the incision extended around the multiple or single renal vessels with a Vannas scissor, leaving up to 1 mm of tissue protruding from the base of the vessels, as described for the Carrel patch.6 If multiple arteries were present, both vessels were retained within a single elongate patch. The renal vein was clamped and transected close to the vena cava via standard techniques. After removal, the vessels of the obtained kidney were flushed with cold sucrose-phosphate preservative,13 and submerged in cold solution on ice until the graft was implanted. With double arteries, each vessel stoma within the excised Carrel patch was sequentially flushed with preservative solution. The donor aorta was repaired using 9-0 nylon in an overlapping simple continuous pattern and the Satinsky vascular clamp removed (Figure 2). The renal vein was ligated with 4-0 silk, the surgery site inspected for hemorrhage and the abdomen closed in a routine manner. In the recipient, transplantation was performed with standard techniques.11 Venous anastomosis was performed first, via end-to-side anastomosis using 10-0 braided polyester suture as previously described,3,6 after partial occlusion of the vena cava using a Codman #7 Sundt slimline temporary aneurysm clip (Codman and Shurtleff, Inc, Raynham,
BUDGEON
ET AL.
F I G U R E 2 Closure of the donor aorta after procurement of a kidney for transplant using the Carrel patch technique
Massachusetts). The renal artery(s) was anastomosed to the recipient aorta by applying a Cooley neonatal vascular clamp, to isolate a segment of the aorta and excising a portion of aortic wall approximating the size of the donor patch. The patch was sutured with 9/0 nylon in 2 simple continuous suture patterns. The ureter was implanted with a neoureterocystostomy6 in 1 cat, or via extravesicular implantation of the ureteral papilla2 in the remaining 8 cats. The renal capsule was fixed to a fold of peritoneum with 5-0 polyglactin 910 sutures. The abdomen was then closed in a routine fashion. The donor and recipient cats were monitored for pain and cardiovascular stability as per the hospital standard of care and provided routine postoperative supportive care. In the donor cats, postoperative blood urea nitrogen (BUN) and creatinine measurements were obtained daily until returned to normal. Postoperative monitoring of the recipient cats was similar and included additional serum chemical profiles in addition to general fluid status, blood pressure, cyclosporine levels, mentation, and ultrasound of the urinary system to assess graft viability as per our standard practices. Serum creatinine is reported here as a surrogate indicator of renal function in the donor and recipient cats. Data are reported as descriptive data or when appropriate as mean 6 SD.
3 | RESULTS Potential donor cats, rejected as donors due to bilateral double vessels detected by imaging before any surgery, could not be identified in our records. For this study, 81 records of donor cats were identified and assessed. Eight cats had a double renal artery of the left kidney (10%), prompting removal of the right kidney in 7 of these cats. A single cat had double renal arteries for the right and left kidneys and was the first case managed with the Carrel patch method.
|
3
Eighteen cats (9 donors and 9 recipients) that either donated a kidney using a Carrel patch or received such kidneys are included in this report. In this series, all recipients were female spayed domestic shorthair cats, ranging in age from 3 to 12 years. Donor cats were provided by the recipient cats’ owners (n 5 2) or obtained from a commercial purpose bred facility (n 5 7). Donors were domestic shorthair cats, 6 male and 3 female, ranging from 6 to 22 months of age. The left kidney was used with the Carrel patch in all cats, one of which had a double renal artery that was not detected upon preoperative imaging, the remainder having a single renal artery. All donor cats survived surgery with no intraoperative complications related to the donor surgery or the vascular resection site noted. Hemorrhage from the donor aortic incision site after closure was minimal and occurred primarily through the suture holes; bleeding stopped with gentle pressure of a cotton tipped applicator after 1-2 minutes. There was no apparent perioperative or postoperative hemorrhage or other vascular compromise in any of the animals. No instances of arterial or venous thrombosis occurred. All donors recovered from surgery without complication. Creatinine levels increased mildly postoperatively in all donor cats but remained within the normal reference ranges, except in 2 cats with maximum postoperative creatinine values of 2.3 and 3.4 mg/dL. Overall, the donor cats had a median preoperative serum creatinine of 1.0 mg/dL (range, 0.9-1.4 mg/dL). Postoperatively, the donor cats had median peak creatinine values of 1.5 mg/dL (range, 1.1-3.4 mg/dL). All donor cats had serum creatinine levels within the reference range at time of suture removal (median value of 1.1 mg/dL; range, 1.0-1.6 mg/dL). All recipient cats survived surgery and were discharged from the hospital. There were no intraoperative complications related to the arterial or venous implant sites. There were no hemorrhagic, thrombotic, or embolic postoperative complications in any of the recipient cats. Subjectively, the arterial anastomosis sites appeared to bleed less during surgery and had fewer or no revision sutures to control hemorrhage at the anastomotic suture line compared to our previous experience with the accepted standard method of end-to-side anastomosis of the transected renal artery. Problems observed during recipient recovery included hypertension in 3 cats and was managed by the administration of hydralazine in a regimen previously described.14 Recipient graft function seemed effective based on posttransplant recipient serum creatinine and blood urea nitrogen levels, urine specific gravity, and Doppler ultrasound evaluations of allograft blood flow. All recipient cats had a marked improvement in postoperative creatinine levels, with all values falling within the normal reference ranges at an average of 3.3 days after transplantation (range, 1-14 days, SD 4.09
4
|
days). The median creatinine value at discharge for all recipient cats was 1.1 mg/dL (range, 0.8-1.8 mg/dL), (reference range, 0.9-2.3 mg/dL).
4 | DISCUSSION The renal artery, with respect to its diameter and length, remains a major factor influencing the success of a feline renal transplant. Short vessels complicate the procedure, and even under optimal conditions, their small diameter predisposes them to thrombosis or inaccurate apposition resulting in bleeding. For this reason, larger donor cats are preferred for their larger kidneys and renal arteries, and kidneys with double arteries have not been utilized due to the very small size of the vessels supplying those grafts. Similarly, kidneys with renal arteries that branch close to the origin at the aorta also generate technical challenges and are not preferred when using standard techniques. This was noted by Bernsteen et al in 2000, stating “it is imperative to harvest a kidney with a single renal artery. . .when the blood supply consists of two or more segmental arteries, the kidney cannot be used for transplantation.”3 This approach contrasts with that for humans, where “when given the choice of a living left donor kidney with two arteries or a right kidney with one, most surgeons choose the former.”15 One approach for preoperative assessment of the vascular anatomy relies on computed tomographic angiography (CTA) or an early phase conventional intravenous urogram (IVU). These studies may identify vascular variations prior to surgery, improving preoperative planning and donor selection.16-18 In humans, CTA has a reported accuracy of > 97% for arteries and 96%-100% for veins.17 A study in cats reported a 92% agreement between CTA and surgical anatomy of the left renal vasculature.18 When IVU was used to screen donors, a relatively high incidence (10%) of failure to detect unacceptable renal vascular conformation resulted in such detection only at the time of surgery.19 The low incidence of bilateral multiple arteries, additional cost, and anesthetic considerations may prompt surgeons to refrain from obtaining a preoperative CTA and IVU. In addition, bilateral multiple arteries may be missed on preoperative imaging. These situations may lead to a donor surgery failing to provide a useable renal allograft perfused by a single vessel. The Carrel patch technique described in this report addresses this issue and may eliminate the need for preoperative angiography, except in those cases where a parenchymal anomaly of one or both kidneys is suspected based on ultrasonographic examination. The rejection of feline donors with multiple renal arteries is in sharp contrast to standard practices in human renal transplantation, where multiple renal arteries are found in 15%-30% of kidneys16,20,21 and seldom considered a
BUDGEON
ET AL.
contraindication to transplantation. In these cases, excision of the renal artery via a Carrel patch is commonly applied.16,20 In cats, this technique eliminates the need to utilize the right kidney, accommodating surgeons’ preference for the left kidney, based on vessel length and arrangement relative to the aorta and vena cava. The frequency of cats with double renal arteries is unknown. In our review of case records, 10% of donor cats (8 cats) had a double left renal artery, one of which (1.2% overall) had bilateral double arteries. However, the actual incidence of double arteries in otherwise normal cats is probably underestimated as our study excluded cats with evidence of bilateral renal arteries on preoperative angiography, and therefore rejected as donors. In the current report, the right arterial configuration was not explored in any donor or recipient, except in 1 cat. Prior to adoption of the Carrel method, the right kidney was utilized for a graft in 7 cats with double left renal arteries. In the eighth cat, the left kidney was collected with a Carrel patch (the first of this series) since bilateral double arteries were discovered at surgery. The Carrel patch technique addressed challenges associated with multiple arteries in that donor cat, and was subsequently used in all subsequent transplantations. Based on our experience, we believe that the Carrel patch technique may also be advantageous to transplant left kidneys supplied by a single artery. Graft destruction and patient mortality secondary to thromboembolic events remain significant complications of feline renal transplantation. A thrombus may form secondary to exposure of collagen through a gap in the endothelium at the anastomotic site. Methods based on a transversely transected renal artery impose a 90degree angle at the end-to-side implant site, complicating accurate apposition of the endothelium at the microtopographical level. The Carrel patch technique may reduce the risk of thrombosis and leakage by moving the suture line away from the entrance to the renal artery. This technique is preferred for transplantation of cadaver allografts in man.6,22 In theory, reducing the angle of contact between the vessel tissue and aortic wall may facilitate endothelial apposition, reducing the risk of thrombus formation. This concept provides a rationale for the use of the Carrel patch in a variety of human cardiovascular and transplantation procedures, as a strategy to prevent vascular thrombosis and stenosis.22-26 We have found the placement of these patches into the aortic sidewall technically easier than the anastomosis of transversely resected renal arteries. Several aspects of the collection of a kidney from a living donor using a Carrel patch may facilitate a successful outcome. First, surgeons must be aware of the relatively small feline aorta and limited availability of tissue, particularly in the transverse plane (circumferentially). For this reason, our harvest of the Carrel patch involves a very discrete
BUDGEON
|
ET AL.
portion of the aortic wall, generally 1 mm or less, around the vessel. A slight narrowing of the aorta is observed after its closure, but this change has not been detrimental in our experience. In addition, we recommend shaping the patch in a slightly elongated ellipse, parallel to the long axis of the aorta, even in kidneys with a single vessel. This configuration simplifies the closure of the aorta by eliminating small folds (similar to dog ears in skin reconstruction), that may create sites of leakage. Removal of the patch is easiest and most precise with a Vannas or other microsurgical scissor, rather than a scalpel, once the aorta has been entered. If needed, the ends of an elongated patch may be trimmed to match the fenestration site on the recipient aorta. Postoperative elevations in serum creatinine in all donors were compatible with our previous experience, and would generally be considered mild (increase of 0.2 mg/dL over preoperative values). The elevation was significant but transient in 2 cats, most likely related to swelling of the tissues adjacent to the ureteral stoma in the bladder rather than damage to the contralateral kidney, since partial occlusion of the aorta does not impair perfusion of the contralateral kidney. These transient increases have been seen in both our clinical donors prior to adoption of the Carrel method and in an experimental study describing the ureteral papilla donor technique.2 In summary, the Carrel patch technique for anastomosis of the renal artery in feline renal transplantation is a viable technique that allows both acquisition of a donor kidney with multiple renal arteries and exclusive use of left kidneys. This technique facilitates arterial implantation in the recipient cat and may decrease risks of leakage of the anastomotic suture line and renal artery thrombosis. However, a larger population would be needed to test the ability of this technique to decrease complication rates. In our center, we have adopted the Carrel patch technique to harvest all kidneys used for renal transplantation.
R EFE RE NC ES [1] Gregory CR, Gourley IM, Kochin EJ, Broaddus TW. Renal transplantation for treatment of end-stage renal failure in cats. J Am Vet Med Assoc. 1992;201:285-291. [2] Hardie RJ, Schmiedt C, Phillips L, McAnulty J. Ureteral papilla implantation as a technique for neoureterocystostomy in cats. Vet Surg. 2005;34:393-398. [3] Bernsteen L, Gregory CR, Kyles AE, Wooldridge JD, Valverde CR. Renal transplantation in cats. Clin Tech Small Anim Pract. 2000;15:40-45. [4] Mathews KG, Gregory CR. Renal transplants in cats: 66 cases (1987-1996). J Am Vet Med Assoc. 1997;211:1432-1436. [5] Bernsteen L, Gregory CR, Pollard RE, Griffey SM, Menwrath V. Comparison of two surgical techniques for renal transplantation in cats. Vet Surg. 1999;28:417-420. [6] Gregory CR, Bernsteen L. Organ transplantation in clinical veterinary practice. In: Slatter D, ed. Textbook of Small Animal Surgery. 3rd ed. Philaphelia, PA: Saunders; 2003:122-136. [7] Carrel A, Guthrie CC. Anastomosis of blood vessels by the patching method and transplantation of the kidney. 1906 [classical article]. Yale J Biol Med. 2001;74:243-247. [8] Andraus W, Haddad LBP, Ducatti L, Martino RB, Santos VR, D’Albuquerque LA. Artery reconstruction in liver transplantation: the best reconstruction of right hepatic artery variation. Arq Bras Cir Dig. 2013;26:62-65. [9] Hashimoto W, Hashizume K, Ariyoshi T, et al. Ten years of aortic root replacement using a modified bentall procedure with a Carrel patch and inclusion technique. Ann Vasc Dis. 2011;4: 32-36. [10] Cosimi AB, Ko DSC. Donor nephrectomy. In: Morris PJ, Knechtle SJ, eds. Kidney Transplantation. 6th ed. Philadelphia, PA: Saunders; 2008. [11] Schmiedt CW, Holzman G, Schwarz T, McAnulty JF. Survival, complications, and analysis of risk factors after renal transplantation in cats. Vet Surg. 2008;37:683-695. [12] Danielson KC, Hardie RJ, McAnulty JF. Outcome of donor cats after unilateral nephrectomy as part of a clinical kidney transplant program. Vet Surg. 2015;44:914-919. [13] McAnulty JF. Hypothermic storage of feline kidneys for transplantation: successful ex vivo storage up to 7 hours. Vet Surg. 1998;27:312-320.
ACKNOWLEDGMENT The authors acknowledge the assistance of William Cruzen in preparing the illustrations for this manuscript.
C O NFL IC T O F I NT E RE S T The authors declare no conflicts of interest related to this report.
[14] Kyles AE, Gregory CR, Wooldridge JD, et al. Management of hypertension controls postoperative neurologic disorders after renal transplantation in cats. Vet Surg. 1999;28:436-441. [15] Allen RDM. Vascular complications after kidney transplantation. In: Morris PJ, Knechtle SJ, eds. Kidney Transplantation: Principles and Practice. 6th ed. Philadelphia, PA: Saunders; 2008: 439-461. [16] Liu PS, Platt JF. CT angiography of the renal circulation. Radiol Clin North Am. 2010;48:347-365. [17] Pozniak MA, Lee FTJ. Computed tomographic angiography in the peroperative evaluation of potential renal transplant donors. Curr Opin Urol. 1999;9:165-170.
ORCID Jonathan F. McAnulty DVM, MS, PhD 0000-0003-1970-6946
5
http://orcid.org/
[18] Caceres AV, Zwingenberger AL, Aronson LR, Mai W. Characterization of normal feline renal vascular anatomy with dual-
6
|
BUDGEON
phase CT angiography. Vet Radiol Ultrasound. 2008;49:350356. [19] Bouma JL, Aronson LR, Keith DG, Saunders HM. Use of computed tomography renal angiography for screening feline renal transplant donors. Vet Radiol Ultrasound. 2003;44:636641. [20] Kobayashi K, Censullo ML, Rossman LL, Kyriakides PN, Kahan BD, Cohen AM. Interventional radiologic management of renal transplant dysfunction: indications, limitations, and technical considerations. Radiographics. 2007;27:11091130. [21] Troppmann C, Wiesmann K, McVicar JP, Wolfe BM, Perez RV. Increased transplantation of kidneys with multiple renal arteries in the laparoscopic liver donor nephrectomy era. Arch Surg. 2001;136:897-907. [22] Mazzucchi E, Souza AA, Nahas WC, Antonopoulos IM, Piovesan AC, Arap S. Surgical complications after renal transplantation in grafts with multiple arteries. Int Braz J Urol. 2005;31: 125-130.
ET AL.
[23] Merion RM, Burtch GD, Ham JM, Turcotte JG, Campbell DA. The hepatic artery in liver transplantation. Transplantation. 1989;48:438-443. [24] Matheus WE, Reis LO, Ferreira U, et al. Kidney transplant anastomosis: internal or external iliac artery. Urol J. 2009;6:260-266. [25] Rajan DK, Stavropoulos SW, Shlansky-Goldberg RD. Management of transplant renal artery stenosis. Semin Intervent Radiol. 2004;21:259-269. [26] du Toit DF, Saaiman A. Anatomical importance of infrarenal aortic branches in conventional and endovascular surgery: a review. Clin Anat. 2000;13:54-62.
How to cite this article: Budgeon C, Hardie RJ, McAnulty JF. A Carrel patch technique for renal transplantation in cats. Veterinary Surgery. 2017;00:1-6. https://doi.org/10.1111/vsu.12705
