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Influence of phosphate-buffered sucrose solution on early graft function in feline renal autotransplantation
Research in Veterinary Science 97 (2014) 410–412
Contents lists available at ScienceDirect
Research in Veterinary Science j o u r n a l h o m e p a g e : w w w. e l s e v i e r. c o m / l o c a t e / r v s c
Influence of phosphate-buffered sucrose solution on early graft function in feline renal autotransplantation Masaaki Katayama a,*, Yasuhiko Okamura a, Shunsuke Shimamura b, Rieko Katayama a, Hiroaki Kamishina c, Yuji Uzuka a a
Division of Small Animal Surgery, Iwate University, 3-18-8 Ueda, Morioka, Iwate 020-8550, Japan Small Animal Internal Medicine, Co-Department of Veterinary Medicine, Faculty of Agriculture, Iwate University, 3-18-8 Ueda, Morioka, Iwate 020-8550, Japan c Division of Veterinary Clinical Radiology, Department of Veterinary Medicine, Faculty of Applied Biological Sciences, Gifu University, 1-1 Yanagido, Gifu, Gifu 501-1193, Japan b
A R T I C L E
I N F O
Article history: Received 10 May 2013 Accepted 20 July 2014 Keywords: Delayed graft function Feline Ischemia and reperfusion injury Kidney transplantation
A B S T R A C T
Graft perfusion with cold heparinized saline has known to induce ischemia and reperfusion injury in feline kidney transplantation. In this study, the effects of phosphate-buffered sucrose solution and heparinized saline solution on early kidney graft function were compared in feline kidney autotransplantation. Perfusion of grafts with or without hypothermic storage with chilled phosphate-buffered sucrose solution prevented ischemia and reperfusion injury despite a very short ischemic time. The results of our study suggest that phosphate-buffered sucrose perfusion and storage solution should be effective to reduce ischemia and reperfusion injury despite a very short ischemic time in feline kidney transplantation. © 2014 Elsevier Ltd. All rights reserved.
Kidney transplantation is a recognized therapeutic option for feline patients with end-stage kidney failure. In feline kidney transplantation, donor grafts are obtained exclusively from living healthy donors, which results in far shorter ischemic times for the harvested graft. Veterinary surgeons tend to ignore the application of organ perfusion and storage solution during transplantation procedures and typically use cold heparinized saline (HS) solution (Mehl et al., 2005, 2006). Although advantages of cooling the graft during the perfusion and transplantation process have been well documented in human transplantation, ex vivo kidney perfusion by cold HS solution may contribute to the damage associated with ischemia and reperfusion rather than preserving or protecting the graft in animal models (Ahmad et al., 2006; Mehl et al., 2006; Regner et al., 2010). Therefore, strategies to limit the deleterious effects of ischemia and reperfusion injury on grafts should be investigated. Kidney allografts hypothermically stored in phosphate-buffered sucrose (PBS) solution clearly demonstrate excellent long-term postoperative graft function in cats (McAnulty, 1998). However, the effects of PBS perfusion and storage solution on early graft function have not been reported. In this study, we compared the influences of PBS solution and HS solution on the prevention of ischemia and reperfusion injury despite very short ischemic periods in feline kidney transplantation.
* Corresponding author. Tel.: +81 19621 6208; Fax: +81 19 6216208. E-mail address: [email protected] (M. Katayama). http://dx.doi.org/10.1016/j.rvsc.2014.07.012 0034-5288/© 2014 Elsevier Ltd. All rights reserved.
This study was approved by the Iwate University Animal Care and Use Committee (#200923). In this study, four healthy male (n = 2) and female (n = 2) cats were used. Their body weights ranged from 3.4 to 5.9 kg, and their ages ranged from 1 to 2 years. Prior to this study, all cats were confirmed to be healthy based on the results of a physical examination, complete blood count, biochemical profile, and urinalysis. The cats were allocated to two treatment groups, and each group included both genders. Each cat underwent a standard heterotopic kidney autotransplantation and contralateral nephrectomy. In this study, the left kidney was harvested and flushed with 20–30 mL of 4 °C cold PBS (PBS group) or heparinized saline (HS group) solution. The PBS solution contained 1000 U/L heparin, 53.6 mM Na2HPO4, 15.5 mM NaH2PO4, and 140 mM sucrose (pH 7.2) (Lam et al., 1989). The average warm ischemia times in the PBS and HS groups were 47 and 52 minutes, respectively. The renal vein was anastomosed to the vena cava in an end-to-side fashion with a simple continuous suture pattern using 10–0 nylon. The renal artery was anastomosed to the aorta in an end-to-side fashion with a simple interrupted suture pattern using 8–0 nylon. The ureter was anastomosed to the bladder mucosa with a modified ureteroneocystostomy technique with 8–0 nylon in a simple interrupted pattern. The transplanted kidney was stabilized by placement of sutures in a retroperitoneal pocket with 4–0 nylon in a simple interrupted pattern. The cats were continuously monitored for 24 hours, and butorphanol (0.4 mg/kg IV) was administered to control pain. Intravenous fluids were
M. Katayama et al./Research in Veterinary Science 97 (2014) 410–412
A
B
Fig. 1. Serum creatinine (A) and blood urea nitrogen (B) in feline kidney autografts treated with hypothermic phosphate-buffered sucrose (PBS) organ perfusion solution and heparinized saline (HS) solution during ischemia. Stippled areas represent the reference ranges based on our background laboratory data.
administered at a maintenance rate for 24 hours after surgery. The cats were monitored for 14 days after surgery. Urine production, appetite, and mental attitude were monitored daily. The blood urea nitrogen (BUN) concentration and urine specific gravity (USG) of each cat were measured daily for the first 3 days after surgery, then on days 6 and 9. The serum creatinine (sCre) and electrolyte levels were measured daily for the first 3 days, then on days 6, 9, 12, and 14. Fourteen days after surgery, the cats were euthanatized with an overdose of pentobarbital, and a complete necropsy was performed. Histopathologic examinations (hematoxylin- and eosin-stained sections) of the autograft and the contralateral kidney removed at surgery were performed. In this study, none of the variables monitored postoperatively were considered to be outside their normal reference ranges with the exception of sCre, BUN, and USG. All cats survived to 14 days. No abnormalities were noted during the daily physical examinations. The time courses of the sCre and BUN concentrations in both groups after transplantation are shown in Fig. 1A and B, respectively (normal reference ranges: sCre, 0.2–2.0 mg/dL; BUN, 12– 36 mg/dL). In the HS group, the sCre concentrations increased and peaked 2 days after transplantation (HS1, 5.6 mg/dL; HS2, 5.0 mg/ dL), then decreased to near preoperative levels (HS1, 1.2 mg/dL; HS2, 1.0 mg/dL) at day 12. The BUN concentration also increased and peaked at days 2–3, then gradually decreased (HS1, 32 mg/dL; HS2, 47 mg/dL). In the PBS group, the postoperative sCre and BUN concentrations were almost invariably within their normal reference
411
ranges. PBS 2 showed a slight increase in the sCre and BUN levels (2.0 and 49 mg/dL, respectively) at day 3, but these levels recovered at day 6 (1.1 and 26 mg/dL, respectively). USG was immediately decreased after surgery and recovered to around the preoperative values by day 6 in both groups. In all four cats, no histologic abnormalities were observed in the autograft or contralateral kidney with the exception of mild infiltration of mononuclear cells into the renal cortex. There were no significant histopathologic differences between the HS and PBS groups. Delayed graft function (DGF) has been consistently identified as an important risk factor for morbidity and mortality after human kidney transplantation. It has been defined as the need for dialysis within the first 7 days after transplantation (Perico et al., 2004). Although a consensus definition of DGF has not been developed in the field of veterinary transplantation because of the relatively short-term preservation period for kidney allograft, it was proposed that DGF should be defined as an sCre level of >3 mg/dL 3 days after surgery in feline renal transplantation (Schmiedt et al., 2008). In cats, the diameter of the ureter at the level of the bladder is 0.4 mm (Gregory et al., 1996), which makes anastomosis of the ureter to the bladder technically challenging. Therefore, the postoperative swelling at the anastomosis site can frequently induce ureteral obstruction in the early postoperative period. This is considered to be a potential cause of DGF in feline renal transplantation (Mehl et al., 2005). However, Mehl et al. (2006) reported that DGF occurred in the feline kidney transplant model without ureteral implantation, which indicates that ischemia and reperfusion injury, rather than ureteral obstruction, may be a primary cause of DGF in cats. Hypothermic storage with a preservation solution using phosphate as a buffer and sucrose as an impermeant solute (PBS) achieves superior results in terms of short- and medium-term renal preservation (Lam et al., 1989; McAnulty, 1998). Sucrose is a large molecule, and its size enhances its ability as an osmotic agent because it is less likely to penetrate the cell membrane even during long periods of storage. The use of a hyperosmotic solution is thought to reduce the degree of cellular swelling by balancing the intracellular colloid osmotic pressure, which protects the graft. In addition to cold storage, the efficacy of PBS solution for warm ischemic graft injury was also reported (Ahmad et al., 2006). In our study, the sCre levels in the PBS group tended to be invariable in the early postoperative period compared with those in the HS group. This indicates that PBS can prevent ischemia and reperfusion injury, affecting early graft function despite a short ischemic time. The vascular anastomosis time should be no longer than 1 hour in feline kidney transplantation (McAnulty, 1998). The cooled graft gradually warms up until the anastomoses are completed. A prolonged anastomosis time results in the progression of warm ischemic injury. Schmiedt et al. (2010) reported that a feline kidney autotransplant model treated with 0.5 or 3 hours of cold storage with PBS solution revealed immediate postoperative increases in the sCre levels (mean, 3.1 mg/dL). In that study, the mean vascular anastomosis time was 83 minutes. In our study, the sCre levels were almost stable after surgery in two autografts. The mean anastomosis time was 47 minutes among our PBS-treated cats. Therefore, vascular anastomosis times may partially contribute to the incidence of ischemia and reperfusion injury in feline kidney transplantation. In conclusion, the results of our study show that flushing and preservation of the kidney with cold PBS solution could prevent DGF in feline kidney transplantation. This suggests that despite a short ischemic period, the type of flushing and preservation solution used during kidney transplantation in cats may influence the early functional status of the post-transplant graft. A larger-scale prospective study is warranted to more extensively explore the impact of PBS solution on early kidney graft function in cats, because of the small number of animals used in this study.
412
M. Katayama et al./Research in Veterinary Science 97 (2014) 410–412
References Ahmad, N., Pratt, J.R., Potts, D.J., Lodge, J.P.A., 2006. Comparative efficacy of renal preservation solutions to limit functional impairment after warm ischemic injury. Kidney International 69, 884–893. Gregory, C.R., Lirtzman, R.A., Kochin, E.J., Rooks, R.L., Kobayashi, D.L., Seshadri, R., et al., 1996. A mucosal apposition technique for ureteroneocystostomy after renal transplantation in cats. Veterinary Surgery 25, 13–17. Lam, F.T., Mavor, A.I., Potts, D.J., Giles, G.R., 1989. Improved 72-hour renal preservation with phosphate-buffered sucrose. Transplantation 47, 767–771. McAnulty, J.F., 1998. Hypothermic storage of feline kidneys for transplantation: successful ex vivo storage up to 7 hours. Veterinary Surgery 27, 312–320. Mehl, M.L., Kyles, A.E., Pollard, R., Jackson, J., Kass, P.H., Griffey, S.M., et al., 2005. Comparison of 3 techniques for ureteroneocystostomy in cats. Veterinary Surgery 34, 114–119.
Mehl, M.L., Kyles, A.E., Reimer, S.B., Flynn, A.K., Pollard, R.E., Nyland, T., et al., 2006. Evaluation of the effects of ischemic injury and ureteral obstruction on delayed graft function in cats after renal autotransplantation. Veterinary Surgery 35, 341–346. Perico, N., Cattaneo, D., Sayegh, M.H., Remuzzi, G., 2004. Delayed graft function in kidney transplantation. Lancet 364, 1814–1827. Regner, K.R., Nilakantan, V., Ryan, R.P., Mortensen, J., White, S.M., Shames, B.D., et al., 2010. Protective effect of Lifor solution in experimental renal ischemia-reperfusion injury. The Journal of Surgical Research 164, e291–e297. Schmiedt, C.W., Holzman, G., Schwarz, T., McAnulty, J.F., 2008. Survival, complications, and analysis of risk factors after renal transplantation in cats. Veterinary Surgery 37, 683–695. Schmiedt, C.W., Mercurio, A., Vandenplas, M., McAnulty, J.F., Hurley, D.J., 2010. Effects of renal autograft ischemic storage and reperfusion on intraoperative hemodynamic patterns and plasma renin concentrations in clinically normal cats undergoing renal autotransplantation and contralateral nephrectomy. American Journal of Veterinary Research 71, 1220–1227.
Contents lists available at ScienceDirect
Research in Veterinary Science j o u r n a l h o m e p a g e : w w w. e l s e v i e r. c o m / l o c a t e / r v s c
Influence of phosphate-buffered sucrose solution on early graft function in feline renal autotransplantation Masaaki Katayama a,*, Yasuhiko Okamura a, Shunsuke Shimamura b, Rieko Katayama a, Hiroaki Kamishina c, Yuji Uzuka a a
Division of Small Animal Surgery, Iwate University, 3-18-8 Ueda, Morioka, Iwate 020-8550, Japan Small Animal Internal Medicine, Co-Department of Veterinary Medicine, Faculty of Agriculture, Iwate University, 3-18-8 Ueda, Morioka, Iwate 020-8550, Japan c Division of Veterinary Clinical Radiology, Department of Veterinary Medicine, Faculty of Applied Biological Sciences, Gifu University, 1-1 Yanagido, Gifu, Gifu 501-1193, Japan b
A R T I C L E
I N F O
Article history: Received 10 May 2013 Accepted 20 July 2014 Keywords: Delayed graft function Feline Ischemia and reperfusion injury Kidney transplantation
A B S T R A C T
Graft perfusion with cold heparinized saline has known to induce ischemia and reperfusion injury in feline kidney transplantation. In this study, the effects of phosphate-buffered sucrose solution and heparinized saline solution on early kidney graft function were compared in feline kidney autotransplantation. Perfusion of grafts with or without hypothermic storage with chilled phosphate-buffered sucrose solution prevented ischemia and reperfusion injury despite a very short ischemic time. The results of our study suggest that phosphate-buffered sucrose perfusion and storage solution should be effective to reduce ischemia and reperfusion injury despite a very short ischemic time in feline kidney transplantation. © 2014 Elsevier Ltd. All rights reserved.
Kidney transplantation is a recognized therapeutic option for feline patients with end-stage kidney failure. In feline kidney transplantation, donor grafts are obtained exclusively from living healthy donors, which results in far shorter ischemic times for the harvested graft. Veterinary surgeons tend to ignore the application of organ perfusion and storage solution during transplantation procedures and typically use cold heparinized saline (HS) solution (Mehl et al., 2005, 2006). Although advantages of cooling the graft during the perfusion and transplantation process have been well documented in human transplantation, ex vivo kidney perfusion by cold HS solution may contribute to the damage associated with ischemia and reperfusion rather than preserving or protecting the graft in animal models (Ahmad et al., 2006; Mehl et al., 2006; Regner et al., 2010). Therefore, strategies to limit the deleterious effects of ischemia and reperfusion injury on grafts should be investigated. Kidney allografts hypothermically stored in phosphate-buffered sucrose (PBS) solution clearly demonstrate excellent long-term postoperative graft function in cats (McAnulty, 1998). However, the effects of PBS perfusion and storage solution on early graft function have not been reported. In this study, we compared the influences of PBS solution and HS solution on the prevention of ischemia and reperfusion injury despite very short ischemic periods in feline kidney transplantation.
* Corresponding author. Tel.: +81 19621 6208; Fax: +81 19 6216208. E-mail address: [email protected] (M. Katayama). http://dx.doi.org/10.1016/j.rvsc.2014.07.012 0034-5288/© 2014 Elsevier Ltd. All rights reserved.
This study was approved by the Iwate University Animal Care and Use Committee (#200923). In this study, four healthy male (n = 2) and female (n = 2) cats were used. Their body weights ranged from 3.4 to 5.9 kg, and their ages ranged from 1 to 2 years. Prior to this study, all cats were confirmed to be healthy based on the results of a physical examination, complete blood count, biochemical profile, and urinalysis. The cats were allocated to two treatment groups, and each group included both genders. Each cat underwent a standard heterotopic kidney autotransplantation and contralateral nephrectomy. In this study, the left kidney was harvested and flushed with 20–30 mL of 4 °C cold PBS (PBS group) or heparinized saline (HS group) solution. The PBS solution contained 1000 U/L heparin, 53.6 mM Na2HPO4, 15.5 mM NaH2PO4, and 140 mM sucrose (pH 7.2) (Lam et al., 1989). The average warm ischemia times in the PBS and HS groups were 47 and 52 minutes, respectively. The renal vein was anastomosed to the vena cava in an end-to-side fashion with a simple continuous suture pattern using 10–0 nylon. The renal artery was anastomosed to the aorta in an end-to-side fashion with a simple interrupted suture pattern using 8–0 nylon. The ureter was anastomosed to the bladder mucosa with a modified ureteroneocystostomy technique with 8–0 nylon in a simple interrupted pattern. The transplanted kidney was stabilized by placement of sutures in a retroperitoneal pocket with 4–0 nylon in a simple interrupted pattern. The cats were continuously monitored for 24 hours, and butorphanol (0.4 mg/kg IV) was administered to control pain. Intravenous fluids were
M. Katayama et al./Research in Veterinary Science 97 (2014) 410–412
A
B
Fig. 1. Serum creatinine (A) and blood urea nitrogen (B) in feline kidney autografts treated with hypothermic phosphate-buffered sucrose (PBS) organ perfusion solution and heparinized saline (HS) solution during ischemia. Stippled areas represent the reference ranges based on our background laboratory data.
administered at a maintenance rate for 24 hours after surgery. The cats were monitored for 14 days after surgery. Urine production, appetite, and mental attitude were monitored daily. The blood urea nitrogen (BUN) concentration and urine specific gravity (USG) of each cat were measured daily for the first 3 days after surgery, then on days 6 and 9. The serum creatinine (sCre) and electrolyte levels were measured daily for the first 3 days, then on days 6, 9, 12, and 14. Fourteen days after surgery, the cats were euthanatized with an overdose of pentobarbital, and a complete necropsy was performed. Histopathologic examinations (hematoxylin- and eosin-stained sections) of the autograft and the contralateral kidney removed at surgery were performed. In this study, none of the variables monitored postoperatively were considered to be outside their normal reference ranges with the exception of sCre, BUN, and USG. All cats survived to 14 days. No abnormalities were noted during the daily physical examinations. The time courses of the sCre and BUN concentrations in both groups after transplantation are shown in Fig. 1A and B, respectively (normal reference ranges: sCre, 0.2–2.0 mg/dL; BUN, 12– 36 mg/dL). In the HS group, the sCre concentrations increased and peaked 2 days after transplantation (HS1, 5.6 mg/dL; HS2, 5.0 mg/ dL), then decreased to near preoperative levels (HS1, 1.2 mg/dL; HS2, 1.0 mg/dL) at day 12. The BUN concentration also increased and peaked at days 2–3, then gradually decreased (HS1, 32 mg/dL; HS2, 47 mg/dL). In the PBS group, the postoperative sCre and BUN concentrations were almost invariably within their normal reference
411
ranges. PBS 2 showed a slight increase in the sCre and BUN levels (2.0 and 49 mg/dL, respectively) at day 3, but these levels recovered at day 6 (1.1 and 26 mg/dL, respectively). USG was immediately decreased after surgery and recovered to around the preoperative values by day 6 in both groups. In all four cats, no histologic abnormalities were observed in the autograft or contralateral kidney with the exception of mild infiltration of mononuclear cells into the renal cortex. There were no significant histopathologic differences between the HS and PBS groups. Delayed graft function (DGF) has been consistently identified as an important risk factor for morbidity and mortality after human kidney transplantation. It has been defined as the need for dialysis within the first 7 days after transplantation (Perico et al., 2004). Although a consensus definition of DGF has not been developed in the field of veterinary transplantation because of the relatively short-term preservation period for kidney allograft, it was proposed that DGF should be defined as an sCre level of >3 mg/dL 3 days after surgery in feline renal transplantation (Schmiedt et al., 2008). In cats, the diameter of the ureter at the level of the bladder is 0.4 mm (Gregory et al., 1996), which makes anastomosis of the ureter to the bladder technically challenging. Therefore, the postoperative swelling at the anastomosis site can frequently induce ureteral obstruction in the early postoperative period. This is considered to be a potential cause of DGF in feline renal transplantation (Mehl et al., 2005). However, Mehl et al. (2006) reported that DGF occurred in the feline kidney transplant model without ureteral implantation, which indicates that ischemia and reperfusion injury, rather than ureteral obstruction, may be a primary cause of DGF in cats. Hypothermic storage with a preservation solution using phosphate as a buffer and sucrose as an impermeant solute (PBS) achieves superior results in terms of short- and medium-term renal preservation (Lam et al., 1989; McAnulty, 1998). Sucrose is a large molecule, and its size enhances its ability as an osmotic agent because it is less likely to penetrate the cell membrane even during long periods of storage. The use of a hyperosmotic solution is thought to reduce the degree of cellular swelling by balancing the intracellular colloid osmotic pressure, which protects the graft. In addition to cold storage, the efficacy of PBS solution for warm ischemic graft injury was also reported (Ahmad et al., 2006). In our study, the sCre levels in the PBS group tended to be invariable in the early postoperative period compared with those in the HS group. This indicates that PBS can prevent ischemia and reperfusion injury, affecting early graft function despite a short ischemic time. The vascular anastomosis time should be no longer than 1 hour in feline kidney transplantation (McAnulty, 1998). The cooled graft gradually warms up until the anastomoses are completed. A prolonged anastomosis time results in the progression of warm ischemic injury. Schmiedt et al. (2010) reported that a feline kidney autotransplant model treated with 0.5 or 3 hours of cold storage with PBS solution revealed immediate postoperative increases in the sCre levels (mean, 3.1 mg/dL). In that study, the mean vascular anastomosis time was 83 minutes. In our study, the sCre levels were almost stable after surgery in two autografts. The mean anastomosis time was 47 minutes among our PBS-treated cats. Therefore, vascular anastomosis times may partially contribute to the incidence of ischemia and reperfusion injury in feline kidney transplantation. In conclusion, the results of our study show that flushing and preservation of the kidney with cold PBS solution could prevent DGF in feline kidney transplantation. This suggests that despite a short ischemic period, the type of flushing and preservation solution used during kidney transplantation in cats may influence the early functional status of the post-transplant graft. A larger-scale prospective study is warranted to more extensively explore the impact of PBS solution on early kidney graft function in cats, because of the small number of animals used in this study.
412
M. Katayama et al./Research in Veterinary Science 97 (2014) 410–412
References Ahmad, N., Pratt, J.R., Potts, D.J., Lodge, J.P.A., 2006. Comparative efficacy of renal preservation solutions to limit functional impairment after warm ischemic injury. Kidney International 69, 884–893. Gregory, C.R., Lirtzman, R.A., Kochin, E.J., Rooks, R.L., Kobayashi, D.L., Seshadri, R., et al., 1996. A mucosal apposition technique for ureteroneocystostomy after renal transplantation in cats. Veterinary Surgery 25, 13–17. Lam, F.T., Mavor, A.I., Potts, D.J., Giles, G.R., 1989. Improved 72-hour renal preservation with phosphate-buffered sucrose. Transplantation 47, 767–771. McAnulty, J.F., 1998. Hypothermic storage of feline kidneys for transplantation: successful ex vivo storage up to 7 hours. Veterinary Surgery 27, 312–320. Mehl, M.L., Kyles, A.E., Pollard, R., Jackson, J., Kass, P.H., Griffey, S.M., et al., 2005. Comparison of 3 techniques for ureteroneocystostomy in cats. Veterinary Surgery 34, 114–119.
Mehl, M.L., Kyles, A.E., Reimer, S.B., Flynn, A.K., Pollard, R.E., Nyland, T., et al., 2006. Evaluation of the effects of ischemic injury and ureteral obstruction on delayed graft function in cats after renal autotransplantation. Veterinary Surgery 35, 341–346. Perico, N., Cattaneo, D., Sayegh, M.H., Remuzzi, G., 2004. Delayed graft function in kidney transplantation. Lancet 364, 1814–1827. Regner, K.R., Nilakantan, V., Ryan, R.P., Mortensen, J., White, S.M., Shames, B.D., et al., 2010. Protective effect of Lifor solution in experimental renal ischemia-reperfusion injury. The Journal of Surgical Research 164, e291–e297. Schmiedt, C.W., Holzman, G., Schwarz, T., McAnulty, J.F., 2008. Survival, complications, and analysis of risk factors after renal transplantation in cats. Veterinary Surgery 37, 683–695. Schmiedt, C.W., Mercurio, A., Vandenplas, M., McAnulty, J.F., Hurley, D.J., 2010. Effects of renal autograft ischemic storage and reperfusion on intraoperative hemodynamic patterns and plasma renin concentrations in clinically normal cats undergoing renal autotransplantation and contralateral nephrectomy. American Journal of Veterinary Research 71, 1220–1227.