Abstract
OBJECTIVE To evaluate the outcome associated with unilateral nephrectomy in feline kidney donors.
DESIGN Retrospective case series.
ANIMALS 141 cats.
PROCEDURES Medical records of cats that underwent nephrectomy for renal donation were reviewed for information on signalment, date of renal donation, results of blood and urine analyses, infectious disease history, anesthetic protocols, intra- and postoperative complications, and postoperative analgesic protocols. Long-term follow-up data were obtained via client telephone interview and review of referring veterinarian medical records.
RESULTS All donors were healthy young adult cats with a median age of 1.5 years (range, 0.8 to 2 years). No cats died or were euthanized during the perioperative period. Intraoperative complications occurred in 2 cats, and postoperative complications occurred in 17. Median time from nephrectomy to hospital discharge was 3.6 days (range, 2 to 8 days). Long-term follow-up information was available for 99 cats, with a median interval between nephrectomy and follow-up of 10 years (range, 0.25 to 15 years). Six cats had a history of urinary tract disease including stable chronic kidney disease (n = 3), acute kidney injury (2), and cystitis (1). Nine cats were dead at follow-up; death was attributed to chronic renal failure in 2 and acute ureteral obstruction in 4.
CONCLUSIONS AND CLINICAL RELEVANCE Feline donor nephrectomy had an acceptably low perioperative morbidity in this series. Most cats (84%) for which follow-up information was available had no associated long-term effects. However, a small subset (7%) developed renal insufficiency or died of urinary tract disease.
Renal allograft transplantation has become a well-recognized treatment for end-stage renal disease in cats. Clinical transplantation is dependent on availability of living unrelated feline donors, which have provided kidneys with good to excellent graft survival in transplant recipients since the introduction of the procedure in 1984.1,2 Although the potential benefits of transplantation to the recipient are clear,1 controversy has existed regarding the use of living donors because of the potential morbidity and unknown long-term sequelae associated with unilateral nephrectomy. Of particular interest and concern is whether the procedure may be associated with development of kidney disease and premature death.3
Multiple studies4–6 have demonstrated acceptably low morbidity (10% to 20%) and mortality (0.03% to 0.06%) rates associated with donor nephrectomy in humans. It is still unclear, however, whether nephrectomy increases the risk of end-stage renal disease in donors. Although older studies4,6–9 examining renal function many years after donation have failed to document progressive renal injury, more recent reports have shown an increased risk of chronic kidney disease.10,11 Similar information for feline donors is currently limited, as the majority of reports have focused on transplant complications and outcomes in recipient cats.1,2,12–16 In the only study17 to date evaluating the long-term effects of unilateral nephrectomy in feline renal donors, follow-up was performed for 16 donors 24 to 67 months after surgery. Kidney function was clinically preserved in the majority (15/16) of donors; however, 1 cat was found to have chronic renal insufficiency 52 months after surgery. Since this report was published in 1995, more than 100 feline renal transplant procedures have been performed at our institution. Thus, more extensive follow-up on a larger group of donor cats is now available. Therefore, the objective of the study reported here was to document the immediate perioperative risks associated with unilateral nephrectomy in feline kidney donors and to examine whether renal function deteriorated over time.
Materials and Methods
Donor cat population
From 1998 to 2003, renal donor cats were obtained from either the York County Society for the Prevention of Cruelty to Animals or from a pathogenfree research breeding facility. Since 2004, all donor cats have been obtained exclusively from the SPCA. All cats were between 8 months and 2 years of age and underwent clinicopathologic testing (CBC, serum biochemical analysis, and blood type analysis), infectious disease testing (FeLV and FIV infection, dirofilariasis, toxoplasmosis, mycoplasmosis, and bartonellosis), urinalysis, and bacteriologic culture of urine prior to surgery. Cats used for kidney donation were those that had no evidence of underlying systemic, renal, infectious, or neoplastic disease on the basis of physical examination and results of clinical laboratory testing as described. Abdominal CT with renal angiography was performed in all cats for assessment of renal morphology and vasculature prior to the transplant procedure.18,19 Cats with renal parenchymal or vasculature abnormalities on CT (presence of renal infarction, multiple renal arteries) were considered unsuitable for donation. Similarly, cats with CT evidence of urolithiasis were also excluded. Donor cats were matched to recipients on the basis of results of major and minor crossmatching.
Medical records review
The feline kidney transplantation medical records of the University of Pennsylvania Ryan Veterinary Hospital between January 1998 and December 2013 were reviewed to identify all renal donor cats that had undergone unilateral nephrectomy. Information collected from the medical records included signalment, date of nephrectomy, and results of preoperative clinicopathologic testing, urinalysis, and infectious disease testing. Anesthetic protocols, intra- and postoperative complications, and postoperative analgesia protocols were recorded for all cats.
Surgery
Unilateral nephrectomy was performed by a board-certified surgeon in all cases. The allograft was prepared by means of a previously described technique.20 Briefly, the left or right renal artery and vein were dissected free of all fat and adventitia, and the ureter was dissected to the level of the urinary bladder. Sterile paper templates were made of the donor artery and vein to determine appropriate size for the recipient venotomy and aortotomy. Vascular ligation and nephrectomy were performed after preparation of the recipient.
Owners of transplant recipient cats were required to adopt the donor cat after surgery. It was recommended that all donors be managed in home environments as regular pets and receive routine veterinary care. At yearly wellness visits, clinicopathologic testing was performed; additional diagnostic testing was recommended if abnormalities were detected or if otherwise clinically indicated. However, no standardized treatments or long-term screening were prescribed.
Follow-up
Follow-up information was obtained via client telephone interview and review of referring veterinarian medical records. Owners were questioned on whether their donor cat had any urinary tract health issues or other systemic disease following kidney donation. For cats that had died or had been euthanized, owners were questioned about the cause of death and necropsy reports were reviewed when available. Clinical laboratory data were recorded for all cats.
Results
During the study period, 141 cats underwent unilateral nephrectomy for kidney donation at the University of Pennsylvania (Figure 1). Median age of donor cats at the time of nephrectomy was 1.5 years (range, 0.8 to 2 years). Of the cats, 136 were neutered males and 5 were spayed females. All were domestic shorthairs. Median preoperative PCV and total protein concentration for the 141 cats were 37% (range, 29% to 48%) and 7 g/dL (range, 5.3 to 8.6 g/dL), respectively (Table 1). All 141 cats had BUN and creatinine concentrations prior to surgery less than the respective upper reference limits (median BUN concentration, 21 mg/dL [range, 14 to 29 g/dL]; median creatinine concentration, 1.2 mg/dL [range 0.8 to 1.8 mg/dL]). Median urine specific gravity for all cats was 1.048 (range, 1.020 to 1.060), and no cat had evidence of proteinuria or urinary tract infection. Results of routine infectious disease testing were negative in all cats. Normal renal morphology and vasculature were confirmed by means of CT with renal angiography in all cases.
Flow diagram illustrating the outcome for renal donor cats (n = 141) that underwent unilateral nephrectomy for renal donation between January 1998 and December 2013 at the University of Pennsylvania Veterinary Hospital. Perioperative morbidity was defined as development of complications during or within 5 days after surgery. Long-term follow-up occurred a median of 10 years after donor nephrectomy (range, 0.25 to 15 years).
Citation: Journal of the American Veterinary Medical Association 248, 3; 10.2460/javma.248.3.275
Anesthesia premedication, induction, and maintenance protocols were chosen at the discretion of the attending anesthesiologist and varied among cats. Perioperative antimicrobials were given at the time of anesthetic induction (cefazolin, 22 mg/kg [10 mg/lb], IV, q 2 h) to all cats. Cats were administered mannitol at the time of the initial abdominal incision (0.25 g/kg [0.11 g/lb], IV) and 20 minutes before nephrectomy (1 g/kg [0.45 g/lb], IV). The left kidney was removed in 135 cats, and the right kidney was removed in 6. None of the donor cats died or were euthanized during the perioperative period. Intraoperative complications (estimated blood loss > 5 mL) were seen in 2 of the 144 (1.4%) cats. In both cats, bleeding was controlled without the need for blood transfusion or additional surgery.
Cats received a balanced electrolyte solution IV at a rate of 1 to 3 mL/kg/h (0.45 to 1.36 mL/lb/h) for the first 24 hours after surgery. Analgesia (buprenorphine, 0.01 to 0.02 mg/kg [0.0045 to 0.009 mg/lb], IV, q 6 to 8 h; methadone, 0.1 to 0.2 mg/kg [0.045 to 0.09 mg/lb], IV, q 4 to 6 h; or fentanyl, 2 to 5 μg/kg/min [0.9 to 2.3 μg/lb/min], IV) was provided as needed for the first 24 to 48 hours after surgery, after which cats received buprenorphine (0.01 to 0.02 mg/kg, PO, q 8 to 12 h) sublingually. Postoperative complications were seen in 17 of 144 (12%) cats and included incisional site seroma (n = 6), incisional site hematoma (2), upper respiratory tract infection (6), corneal ulceration (3), and diarrhea (4). These complications were seen within the first 5 days after surgery and required minimal or no treatment. The median time from surgery to hospital discharge was 3.6 days (range, 2 to 8 days).
Long-term follow-up information was available for 99 of the 144 (69%) cats, and 90 of these cats (91%) were alive at the time of follow-up. The median interval between nephrectomy and final follow-up was 10 years (range, 0.25 to 15 years). The median age of the cats at the time of final follow-up was 12.2 years (range, 3.5 to 15 years). Seventy-seven of the 99 (84%) cats were considered clinically normal at the time of final follow-up on the basis of history since nephrectomy and results of physical examinations performed by their primary care veterinarians. Results of clinicopathologic testing performed within 1 year of final follow-up were available for 52 of the cats, and results of urinalyses were available for 36 (Table 1). Median PCV (37.6%), total protein concentration (7 g/dL), BUN concentration (26.2 mg/dL), and creatinine concentration (1.5 mg/dL) were within reference limits. Median urine specific gravity was 1.035 (range, 1.010 to 1.050). Seven of the 36 (19%) cats for which urinalysis results were available had evidence of proteinuria; the median urine specific gravity in these 7 cats was 1.030 (range, 1.012 to 1.045).
Results of preoperative and follow-up clinicopathologic testing and urinalysis for renal donor cats (n = 141) that underwent unilateral nephrectomy for renal donation between January 1998 and December 2013 at the University of Pennsylvania Veterinary Hospital.
| Variable | Reference interval | Preoperative (n = 141) | Follow-up (n = 52) |
|---|---|---|---|
| Creatinine (mg/dL) | 1.0–2.0 | 1.2 (0.8–1.8) | 1.5 (0.9–1.8) |
| BUN (mg/dL) | 15–32 | 21 (14–29) | 26.2 (18–34) |
| Total protein (g/dL) | 6–8.6 | 7 (5.3–8.6) | 7 (5.5–7.6) |
| PCV (%) | 31.7–48 | 37 (29–48) | 37.6 (32–48) |
| Urine specific gravity | NA | 1.048 (1.020–1.060) | 1.035 (1.010–1.050)* |
Data are presented as median (range).
Represents results for 36 cats.
NA = Not applicable.
Six of the 90 (7%) cats that were alive at the time of follow-up had a history of urinary tract disease. Specifically, renal insufficiency had been diagnosed on the basis of results of clinicopathologic testing in 3 of the 6 cats a median of 6.2 years (range, 5 to 11 years) after nephrectomy. Follow-up median BUN and creatinine concentrations in these 3 cats were 52 mg/dL (range, 41 to 59 mg/dL) and 2.5 mg/dL (range, 2.3 to 3.8 mg/dL), respectively, and the median urine specific gravity was 1.010 (range, 1.010 to 1.012). Two of the 6 cats had episodes of acute renal injury 4 and 6 years following kidney donation; the interval between the acute renal injury episodes and follow-up was 5 and 6.5 years. One of these 2 cats was examined by its primary care veterinarian 4 years after kidney donation because of an acute onset of vomiting and lethargy, at which time serum biochemical testing indicated severe azotemia (BUN concentration, 92 mg/dL; creatinine concentration, 4.9 mg/dL). Results of abdominal imaging were unremarkable, and the underlying cause of renal injury was never determined. The cat's clinical signs and high BUN and creatinine concentrations resolved with dialysis treatment. At the time of follow-up (6.5 years after kidney donation), BUN (28 mg/dL) and creatinine (1.6 mg/dL) concentrations in this cat were within reference limits. The second cat was evaluated at a specialty veterinary hospital 6 years after kidney donation because of an acute onset of lethargy and inappetence. The cat was found to be azotemic (BUN concentration, 70 mg/dL; creatinine concentration, 4.5 mg/dL) with bacterial growth on urine culture. Abdominal ultrasonography showed no evidence of urinary tract obstruction. Renal injury was attributed to pyelonephritis, which resolved with IV fluid therapy and antimicrobial treatment. At the time of follow-up (10 years after nephrectomy), BUN (32 mg/dL) and creatinine (1.4 mg/dL) concentrations were within reference limits. In the remaining cat with evidence of urinary tract disease, idiopathic cystitis was diagnosed 3 years after nephrectomy on the basis of intermittent lower urinary tract signs (stranguria, hematuria) in the absence of abnormal bloodwork or bacterial growth on urine culture. According to the owner, clinical signs were self-limiting and resolved without treatment.
Nine of the 90 (10%) cats alive at the time of follow-up a median of 10 years (range, 0.25 to 15 years) after donation had a history of nonurinary tract illness, including hyperthyroidism (n = 2), diabetes mellitus (1), hypertrophic cardiomyopathy (3), eosinophilic dermatitis (1), chronic uveitis with secondary glaucoma (1), and feline asthma (1).
Nine of the 144 (9%) cats were dead at the time of follow-up. Death was attributed to urinary tract disease in 6 of these 9 cats; 4 cats died of acute ureteral obstruction and 2 died of chronic renal disease. In the cats that died of acute ureteral obstruction, death occurred a median of 7 years following kidney donation (range, 3 to 8 years). Obstructive calcium oxalate ureteroliths were identified on necropsy in all of the cats. The 2 cats with chronic renal failure were euthanized 12 and 13 years after kidney donation. A necropsy was not performed on either of these cats. Of the remaining 3 cats that were dead at the time of follow-up, 1 died of feline infectious peritonitis 4 months after kidney donation, and the other 2 died of unknown causes 4 and 12 years after nephrectomy.
Discussion
Results of the present study which retrospectively evaluated the outcome for renal donor cats that had undergone unilateral nephrectomy between January 1998 and December 2013 suggested that there is an acceptably low perioperative morbidity rate associated with kidney donation in cats. The majority of cats for which follow-up was available had no apparent delayed or long-term adverse effects related to donation; however, a small number ultimately developed renal insufficiency or died of urinary tract disease. As such, it is still unclear whether living feline donors as a group are at higher risk of renal sequelae, and judicious screening and careful selection of donor cats must be continued.
Live donor kidney transplantation is currently the gold standard for end-stage renal disease in human patients.3,21,22 Compared with dialysis, kidney transplantation offers an improved quality of life and decreased mortality rate.4 Furthermore, live donor transplants offer substantially superior graft function and survival, compared with cadaver kidney transplantation in human patients.3 However, nephrectomy is associated with at least some risk to the donor. Specifically, both the perioperative morbidity and mortality rates and the long-term (potentially negative) consequences of living with 1 kidney must be considered.3,4,22–24 This has resulted in considerable ethical controversy in the human medical field with regard to live donor kidney transplantation.3,25–29
In humans, open donor nephrectomy has been associated with a 0.03% to 0.06% mortality rate and an approximately 10% to 20% overall morbidity rate perioperatively.4,5,30 The main causes of reported deaths during or immediately following nephrectomy in humans include pulmonary embolism, myocardial infarction, and cardiac arrhythmias.4 Major perioperative complications associated with donor nephrectomy are documented in 0.23% to 3.3% of cases and include intra- or postoperative bleeding, splenic laceration, venous thrombosis, pulmonary embolism, pneumothorax, and peripheral nerve damage.5,30 Minor complications including low-grade incisional infection, pain, and postoperative incisional herniation are reported in approximately 10% to 15% of patients.4 In the present study, we report low perioperative morbidity and mortality rates in feline donor cats. Specifically, no cats died during the perioperative period. The only intraoperative complication in this study was notable bleeding, which was seen in 2 of 144 (1.4%) cats. All other complications were seen postoperatively (incisional site seroma, n = 6; incisional site hematoma, 2; upper respiratory tract infection, 6; corneal ulceration, 3; and diarrhea, 4) and were considered self-limiting. Thus, we suggest that nephrectomy in healthy donor cats is a reasonably safe procedure with minimal life-threatening risk. It should be noted, however, that all donor nephrectomies in this study were performed by a board-certified surgeon with experience in microvascular surgery. This may have influenced the low morbidity and mortality rates found in association with the procedure.
In addition to the perioperative risks of nephrectomy in donor patients, there is considerable concern with regard to the potentially deleterious long-term effects of living with 1 kidney. Studies30–32 in human donors have shown that following nephrectomy, the remaining kidney hypertrophies by 20% to 30% and glomerular filtration rate increases by approximately 40%. These changes result in adaptive hyperfiltration of the kidney, which is maintained for many years following the nephrectomy procedure.31,32 It has been suggested that renal hyperfiltration may have deleterious effects on human donors including hypertension, proteinuria, and an accelerated decrease in renal function with age.29,30
Multiple studies29–32 have confirmed the presence of renal hyperfiltration in human donors. Likewise, hypertension and proteinuria have also been identified in up to 60% and 56% of donors, respectively.30–39 Blood pressure was not routinely evaluated in our donor cat population at the time of follow-up in this study; thus, the incidence of hypertension in this group of cats is unknown. However, because untreated hypertension is considered a risk factor for the development of nephrosclerosis and renal failure, we suggest that routine monitoring would be prudent to facilitate early detection and treatment of affected cats. Of the 99 cats for which long-term follow-up was available, 36 had a recent (within 12 months) urinalysis available for review, and 7 of the 36 (19%) had proteinuria. The clinical importance of this finding in feline donors is unclear. Results of studies8,9,36,37 in human donors suggest that the incidence of proteinuria does not vary significantly from the incidence in matched controls, and importantly, proteinuria does not appear to progress to renal failure. Future studies are needed to determine the consequences, if any, of proteinuria in the feline donor population.
Studies have also evaluated the risk of progressive renal deterioration and the development of end-stage renal disease in living human donors with conflicting results. Several older reports4,6–9,40–42 support the notion that, in an individual with 2 normal kidneys, unilateral nephrectomy does not lead to an increased risk of progressive renal deterioration. Particularly, in a study6 evaluating living kidney donors with 20 years or more of follow-up, no significant differences were found when mean serum creatinine concentrations for donors versus siblings that had not donated were compared. However, recent studies10,11,29 have documented an increased relative risk of end-stage renal disease in human donors, albeit the incidence still remains low.
In the present study, 3 of the 99 (3%) cats for which long-term follow-up was available had signs of chronic renal insufficiency at the time of follow-up, and 2 of the 99 (2%) were euthanized because of signs of chronic renal failure. It should be noted, however, that 42 of the 141 (30%) donor cats in this study were lost to long-term follow-up and not all donor cats for which follow-up information was available had regular bloodwork performed over the course of their lifespans. Thus, the true rate of chronic renal disease and renal failure in this population of cats may be different than what is reported here. The incidence of chronic renal insufficiency in nonnephrectomized, older cats is unknown but was estimated to be between 4.5% and 9.6% in 1 report.43 Because the donor cats in the present study were carefully screened preoperatively and excluded from donation if evidence of renal or systemic disease was identified, we would expect that the risk of renal disease among the donor population should be lower than the risk in the general population. Regardless, we did identify a subset of renal donor cats that eventually developed renal insufficiency. This finding emphasizes the need for continued careful donor screening for health conditions related to kidney disease preoperatively and judicious long-term follow-up.
Four of 99 (4%) cats for which follow-up was available died as a result of acute ureteral obstruction with ureteroliths. Ureteral calculi in cats is a relatively new clinical condition, with the first report44 on a series of cats published in 1998. Interestingly, there has been a dramatic increase in the frequency of upper urinary tract stones diagnosed in cats evaluated at veterinary teaching hospitals from 1981 onward.45 This change parallels the increase in occurrence of calcium oxalate urolithiasis, as opposed to struvite urolithiasis, in cats.46 The reasons underlying such a dramatic change in the composition of feline uroliths is still unclear, and to date, a cause-and-effect relationship has yet to be established. Because it has been reported that approximately 90% of feline ureteroliths are composed of calcium oxalate,47 knowledge of underlying contributing factors to ureterolith formation is essential for stone prophylaxis in cats to prevent life-threatening obstructive uropathy.
The incidence rate for urolithiasis in the general cat population has not been well established but may be between 0.2% and 3%.47 It is possible that feline ureteroliths and ureteral obstruction are underdiagnosed in the general cat population for several reasons. Specifically, the majority of cats with unilateral ureteroliths, ureteral obstruction, or both may lack clinical signs48–50 In fact, many stones are found incidentally on abdominal imaging performed for unrelated disease processes.50 In addition, clinical signs of upper urinary tract obstruction are often nonspecific (ie, reduced appetite, vomiting, lethargy, and weight loss), and metabolic derangements (electrolyte abnormalities and azotemia) are mild in cats with unilateral disease.44,48–50
Results of a 1997 study51 in human patients indicated that stones < 3 mm in diameter will pass spontaneously in approximately 90% of cases such that obstructive uropathy may be less of a concern. In contrast, the small diameter of the feline ureter makes spontaneous passage of stones less likely and obstruction more concerning.49 Because obstructive uropathy, particularly in feline kidney donors, can result in renal failure and even death and because clinical signs of upper urinary tract obstruction are often insidious, we suggest that more stringent postoperative monitoring may be beneficial in this cat population. This could include yearly urinalysis to monitor for abnormalities that may precipitate stone formation including crystalluria, abnormal urine pH, or both as well as yearly abdominal radiography to assess for urolithiasis. And for any donor cat with nonspecific signs or signs attributable to urinary tract dysfunction, prompt clinicopathologic testing and abdominal imaging are imperative.
There were clear limitations to the present study, particularly with regard to its retrospective nature and the fact that a considerable percentage of our donor population (42/141 [30%] cats) was lost to follow-up. Additionally, follow-up was not standardized between cats. For these reasons, the results reported here may have underestimated the true incidence of urinary tract disease in the feline donor population. Future studies that assess donor cats prospectively in a standardized manner would help to ensure all cats are adequately evaluated and may provide better insight into the true prevalence of renal disease in this population. Additionally, a study comparing donor cats with an age-matched, nonnephrectomized control group may provide additional information on the true risk of nephrectomy. Because it remains uncertain whether living feline donors as a group are at higher risk of renal sequelae, regular evaluation at routine intervals over the course of the donor lifespan is strongly recommended.
ABBREVIATION
| SPCA | Society for the Prevention of Cruelty to Animals |
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