Renal Transplantation in the First Year of Life: The Treatment of Choice for Infants With End-Stage Renal Disease

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1 Renal Transplantation in the First Year of Life: The Treatment of Choice for Infants With End-Stage Renal Disease John S. Najarian,1 P. Stephen Almond, Michael Mauer, Blanche Chavers, Thomas Nevins, Clifford Kashtan, and Arthur J. Matas J.S. Najarian, P.S. Almond, M. Mauer, B. Chavers, T. Nevins, C. Kashtan, A.J. Matas, University of Minnesota, Department of Surgery, Minneapolis, MN (J. Am. Soc. Nephrol. 1992; 2: ) ABSTRACT The treatment of choice for end-stage renal failure within the first year of life is controversial. Between September 1970 and February 1991, we performed 28 kidney transplants (27 primary, I retransplant, 23 living donor, 5 cadaver) in infants less than I yr of age (mean, 7 ± 2 months; range, 6 wk to 12 months). The 1-yr patient survival rate for living donor recipients was 100% versus 20% for cadaver recipients (P = ). The 1-yr graft survival rate for living donor recipients was 96% versus 20% for cadaver recipients (P = 0.001). The 1-yr patient survival rate for cyclosporin A (CSA) recipients (N = 12) was 100% versus 75% for non-csa recipients (P = 0.03). The 1-yr graft survival rate for CSA recipients was 92% versus 75% for non-csa recipients (P = 0.08). There was no difference in the number of rejection episodes or serum creatinine levels in CSA versus non-csa recipients. Compared with pretransplant values, the mean posttransplant standard deviation scores (SDS) for height (N= 18), weight (N= 22), and head circumference (N = 8) improved: height SDS from - I.9 to - I.5 (not significant); weight SDS from -2.5 to 0.6 (P< ); head circumference SDS from -2.0 to -0.7 (P = 0.01). Because no other renal replacement therapy can match these results, we conclude that renal transplantation is the treatment of choice for infants with end-stage renal failure. Key Words: Kidney transplantation, infant, kidney failure T ransplantation in the first year of life remains controversial. Most agree that a functioning Correspondence to J.S. Najarian, Department of Surgery, University of Minnesota, Box 195 UMHC, 516 Delaware Street 5E, Minneapolis, MN /02 12-S228$03.00/0 Journal of the American Society of Nephrology Copyright 1992 by the American Society of Nephrology renal allograft is the ultimate goal for all infants with end-stage renal disease (ESRD). Some centers, however, are loath to transplant infants, preferring dialysis instead until they reach a predetermined age and have an adequate cadaver donor. We prefer an alternative approach-immediate transplantation with an organ from a living related donor, whenever possible. In this report, we review our results with renal transplantation in the first year of life, paying particular attention to the most important factors in obtaining good results in this age group: perioperative care, donor source, and immunosuppressive protocol. MATERIALS AND METHODS Patient Selection Between September 20, 1 970, and February 21, , 27 infants 1 yr of age or less (6 wk to 12 months) received 28 renal transplants at the University of Minnesota. Data on these patients, obtained from their transplant charts, included age at the time of transplant, sex, donor source, transplant number, date of death, date of graft loss, serum creatinine level, cyclosporin A (CSA) dosage (in milligrams per kilogram per day), whole-blood CSA trough level (determined by HPLC), number of rejection episodes, number of readmissions, and discharge diagnoses. Surgical Technique The surgical approach and perioperative care have been described in detail elsewhere (1 ). Briefly, the abdomen is entered through a midline incision and the ascending colon is reflected medially. The distal aorta, vena cava, and iliac arteries and veins are mobilized. Proximally, the aorta and vena cava are occluded with a single vascular champ; distally. the iliac arteries and veins are occluded with vessel hoops. The patient is not heparinized. The renal artery and vein are anastomosed to the distal aorta and vena cava. Before reperfusion, the kidney is bathed in warm saline, the central venous pressure is raised to 15 cm of water, and mannitol (250 mg/kg) and furosemide (1 mg/kg) are administered. Ureteral anastomosis is performed by the Leadbetter-Pohitano technique. S228 Volume 2 Supplement

2 Najarian et al Immunosuppression Our immunosuppressive protocols have previously been described in detail (2). Before 1984, infants and children received azathioprine (AZA) (5 tapered to 2.5 mg/kg/day by posttransplant day 7); prednisone (PRED) (2 tapered to 0.5 mg/kg/day at 1 month, then to a maintenance dosage of 0.25 mg/kg/day at 1 yr posttransphant); Minnesota antihymphocyte globulin (MALG) (30 mg/kg/day for 14 days); and methylprednisolone (20 mg/kg/day for 3 days). All children were splenectomized and received three to five random donor blood transfusions pretransplant, most while receiving 1.5 mg/kg/day of AZA. Beginning in June 1 984, 1 5 patients were entered into a donor-specific transfusion (DST) protocol. Each patient was given three pretransplant DSTs, at biweekly intervals. A cross-match was performed 4 to 6 wk later, and if negative, the transplant was performed. Posttransplant, patients received AZA, MALG, and PRED. Children not receiving DSTs received sequential therapy: AZA (5 tapered to 2.5 mg/ kg/day by posttransplant day 7); PRED (2 tapered to 0.5 mg/kg/day at 1 month, then to a maintenance dosage of 0.25 mg/kg/day at 1 yr posttransplant); and MALG (20 mg/kg for 14 days). Cyclosporin A (CSA) (2.5 mg/kg twice a day) was added on postoperative days 1 0 to 1 2; CSA was tapered to 3 mg/kg by 3 months. CSA levels were obtained periodically, but the CSA dosage was not adjusted to maintain a predetermined CSA level. Splenectomy was abandoned in after a prospective. randomized study demonstrated no improvement in long-term survival rates (3). Recently. we reported that a significant portion (44%) of our pediatric recipients on sequential immunosuppression experienced at least one rejection episode (4). On the basis of this observation and on reports of increased pediatric cadaver renal allograft survival rates, we have changed our immunosuppressive protocols. Recipients with good graft function now begin CSA (2.5 mg/kg/twice a day) on posttransplant day 5 (instead of day 12). For living related donor (LRD) recipients, this dosage will be maintained. For cadaver (CAD) and retransplant recipients, the CSA dosage will be manipulated to maintain measurable CSA levels (i.e., >25 ng/dl by HPLC). In all patients, rejection episodes were documented by biopsy and were treated with recycling of the PRED taper (initially, 2 mg/kg/day, tapered to a maintenance dosage) and 10 to 14 days of MALG (20 mg/kg/day). values for American children (5): Data b L SDS = (patient value - mean value)/sd. Analysis Patient and graft survival rates were calculated by life table analysis, with the Gehan test used for statistical comparison (6). RESULTS Patient Demographics Of the 28 kidney transplants (27 primary, 1 retransplant) done in infants at the University of Mmnesota during the study period, 22 were from LRD, 5 were from CAD, and 1 was from a hiving unrelated donor. The mean age at the time of transplant was 7 ± 2 months. There were 1 1 girls and 1 6 boys. The causes of renal failure were obstructive uropathy (N = 7), hypoplasia (N = 5). oxalosis (N = 4), congenital nephrotic syndrome (N = 2), cortical necrosis (N = 2), ghomerulonephritis (N = 2), polycystic kidneys (N = 1), hydronephrosis (N = 2), reflux (N = 1), and unknown(n= 1). Patient and Graft Survival Rates Overall patient and graft survival rates are shown in Figure 1. For LRD recipients. the patient survival rate was 100% at 1 yr and 77% at 5 yr; for CAD recipients, itwas 20% at both 1 and 5 yr (P = ). For LRD recipients, the graft survival rate was 96% at 1 yr and 63% at 5 yr; for CAD recipients, it was 20%atboth 1 and5yr(p=0.001). Effect of Immunosuppressive Protocol Graft survival rates in infants on non-csa versus CSA % immunosuppression Survival are shown in Figure 2; patient survival rates are shown in Figure 3. For CSA recipients (N = 12), the patient survival rate was L s Survvsl 4 Patlsnt Growth and Development Data on growth were converted to standard deviation scores (SDS) by previously published normal so 80 Months Figure 1. Overall patient and graft survival rates in infants transplanted in the first year of life. Journal of the American Society of Nephrology S229

3 lenal Transplant in the First Year of Life S Graft Survival p-.08 N Causes of Graft Loss A total of 1 1 grafts have been lost. For non-csa recipients. causes included death (N = 6), acute (N = 1) and chronic (N = 1) rejection, and recurrence of primary disease (N = 1 ; oxalosis). For CSA recipients. causes included rejection (N = 1 ) and arterial thrombosis(n= 1). 20 r laununosupprs$alofl Non-CU (n.i6) -4- CSA (n 12) so Months Figure 2. Graft survival rates for infants on non-csa versus CSA immunosuppression. S Patient Survival Retransplants Four patients were retransplanted at age 17 -J months, 29 months, 30 months, and 8 yr. All retrans- 80 plant recipients were alive with a functioning graft at the time of this report. Causes of Death A total of seven patients. all non-csa recipients, died posttransplant. Causes included generalized sepsis (N = 5), recurrence of primary disease (N = 1; oxahosis), and other (N = 1) P- Immunosuppr.sslOfl Non-CSA (n.16) -4- CU (n i2) so Months Figure 3. Patient survival rates for infants on non-csa versus CSA immunosuppression. Rejection Episodes and Function There were a total of 2 1 posttransplant rejection episodes: 1 3 in the non-csa recipients and 8 in the CSA recipients. Importantly, 19 patients (70%) have not been readmitted for rejection. Serum creatinine levels and CSA dosage are shown 80 in Table 1. There were no significant differences in serum creatinine levels between non-csa and CSA recipients. Readmissions 100% at 1 and 5 yr; for non-csa recipients it was 75% at 1 yr and 62% at 5 yr (P = 0.03). For CSA recipients (N = 16), the graft survival rate was 92% at both 1 and 5 yr; for non-csa recipients it was 75% at 1 yr and 50% at 5 yr (P = 0.08). There were a total of 74 readmissions. The mean (±SD) number of readmissions was 2.9 ± 3.0 (range, 0 to 11). The most common causes for readmission were infection (N = 23), rejection (N = 18), and dehydration (N = 11). TABLE 1. Serum creatinine levels and CSA dosage 1 yr 2 yr 3 yr 4 yr 5 yr 6 yr 7 yr 8 yr 9 yr Non-CSA Recipients Serum creatinine CSA Recipients Serum 0.87 ± ± ± ± ± ± ± ± creatinine 0.57 ± ± ± ± ± 0.36 ND#{176} ND ND ND CSA dosage 4.4 ± ± ± ± ± 0.85 ND ND ND ND Overall Serum creatinine 0.75 ± ± ± ± ± ± ± ± #{176}ND.not determined. S230 Volume 2 Supplement

4 Najarian et al Pr. Figure 4. SDS for length/height in 18 infants with complete data. The SDS decreased in 8 infants and increased in the remaining 10. The SDS (mean ± SD) was -1.9 ± 1.1 pretransplant (Pre) versus -1.5 ± 1.5 posttransplant (Post). Growth and Development Pretransplant and posttransplant SDS for height (N = 18) (Figure 4), weight (N = 22) (Figure 5), and head circumference (N = 8) (Figure 6) are shown for all patients on whom data were available. Compared with pretransplant values, the mean posttransphant 12 Post Pre Figure 6. SDS for head circumference in eight infants with complete data. The SDS was unchanged in one, decreased in one, and increased in the remaining six infants. The SDS (mean ± SD) was -2.0 ± 0.52 pretransplant (Pre) versus -0.7 ± 1.5 posttransplant (Post)(P= 0.01). SDS improved for all three measurements. The height SDS improved from ± 1. 1 pretransplant to ± 1.5 posttransplant. The weight SDS improved from -2.5 ± 1.2 pretransplant to 0.6 ± 3.2 posttransphant (P < ). The head circumference SDS improved from -2.0 ± 0.52 pretransplant to -0.7 ± 1.5 posttransplant (P = 0.01). Post x Pr. Figure 5. SDS for weight in 22 infants with complete data. The SDS decreased in 3 infants and increased in the remaining 19. The SDS (mean ± SD) was -2.5 ± 1.2 pretransplant (Pre) versus 0.6 ± 3.2 posttransplant (Post) (P < ). ) Post DISCUSSION Renal transplantation, although long recognized as the treatment of choice for ESRD, is frequently not considered as such for infants less than 1 yr of age. Instead, many transplant centers prefer to postpone transplantation until infants have reached a predetermined age and an adequate CAD donor becomes available (7,8). In the interim, patients are started on some form of dialysis, most commonly peritoneal dialysis. Postponing transplantation, largely because of initial reports suggesting poor results with transplantation in infants (9,10), rests on three assumptions: that dialysis maintains normal growth and development; that age at the time of transplant correlates with outcome; and that preemptive, LRD transplantation is not an option. One of the major goals of renal replacement therapy for infants should be to preserve growth and development potential. During the first 12 months of life, ghial proliferation within the central nervous system is at its highest level and correlates with head circumference (11). In addition, the annual rate of growth during this time is about four times higher than during any other time in life (8). Renal failure Journal of the American Society of Nephrology S231

5 Penal Transplant in the First Year of Life adversely affects these processes, causing significant decreases in head circumference and linear growth from which, in the absence of catch-up growth. the infant can never recover. The optimal renal replacement therapy should, therefore, be initiated before uremia develops and should allow for growth and development characteristic of this age. Dialysis initiated in the first year of life does not preserve development potential. In a recent report, Bird and Semmler ( 1 2), using the Bayhey Scales of Infant Development, evaluated the cognitive and motor development of 1 0 infants who had ESRD from birth and who were treated with either continuous ambulatory peritoneal dialysis (CAPD) or continuous cycling peritoneal dialysis. All infants demonstrated significant delays in both cognitive and motor development. Salusky et al. (8) noted a significant decrease in the SDS for height. from ± 1.32 down to ± 1.36, in eight infants (mean age. 5.8 ± 2.3 months) who were maintained on continuous cycling peritoneal dialysis. Similarly, the SDS for weight and head circumference also declined, though not significantly. Kohaut et al. (7) reported on nine infants who developed ESRD within 3 months after birth and who were treated initially with CAPD. The mean height SDS decreased from pre-capd to post-capd. The mean head circumference SDS decreased from pre-capd to post-capd. Of these nine infants, two died while on CAPD. The remaining seven eventually received renal transplants; six were alive with functioning grafts at the time of this report. Importantly, both measurements improved posttransplant. These results demonstrate that dialysis cannot maintain normal growth and development in infants less than 1 yr of age. Dialysis advocates suggest that growth hormones will improve growth on dialysis, but these hormones would also be used to further improve the growth of renal transplant recipients (13,14). A successful renal transplant in the first year of life allows for more normal growth and development during infancy. In 1986, So et al. (15) reported on growth and development in 9 of 1 3 infants who were transplanted at our institution in the first year of life and then monitored for 4 months to 7.5 yr. Mental development was normal in all seven of the infants who were reassessed posttransplant with the Bayhey Scales, and motor development was normal in five. In the six patients who did not have oxalosis, the mean increase in SDS for height was 1.4 and for head circumference was 2.2. This study confirms and extends these initial findings (Figure 4). Transplant age in and of itself has also been touted as a barrier to successful transplantation. In 1985, Alexander (9) summarized early results of transplantation in infants <1 yr as discouraging. In his review, 16 infants had received 18 kidneys, only 4 of which were functioning at the time of his report; 11 (69%) of the 1 6 infants had died. More recently, however, Nevins reported on 1 3 primary transplants in infants (16). In this series, only two patients died (from overwhelming pneumococcal sepsis and recurrent oxalosis) and an additional two kidneys were lost (to chronic rejection and oxalosis). The report of Nevins, demonstrating improved survival rates in infants, suggests that age in and of itself may not be the limiting factor to successful transplantation. Kim et al. (1 7) confirmed this suspicion statistically by finding no correlation between transplant age and patient survival. A closer comparison of the reports by Alexander and Nevins suggests that donor source, immunosuppression, and transplant center may be the deciding factors in transplant outcome. In the report of Alexander, 1 5 of 1 8 allografts were from pediatric CAD donors (including 4 anencephahic donors), with only 3 from LRD. Recent reports have demonstrated that, in infant recipients, renal allografts procured from pediatric and anencephahic donors do poorly in infants. In 1990, Gomez-Campdera et al. (18) reported on five infant renal transplants from anencephalic donors, four of which never functioned; in , Arbus et al. (1 9) found that 1 -yr CAD graft survival rates in infants improved from 47% for 2- yr-old donors to 57% for 1 8-yr-old donors. The grafts from the younger donors were usually lost because of technical problems. In the report of Nevins, 1 1 of 1 3 infants received adult LRD kidneys, and all of the transplants were done at the University of Minnesota. The introduction of CSA and immunosuppressive protocols based on it have resulted in improved CAD graft survival rates. At our institution, 1 -yr patient and graft survival rates for CAD graft recipients (infants <2 yr; N = 5) on sequential immunosuppression are 100% (1). Ettenger et al. (20), reporting on 23 recipients 6 yr. have also found significant improvement in 1 -yr graft survival rates with quadruple immunosuppression (MALG/CSA/AZA/PRED), compared with CSA/PRED or AZA/PRED protocols. National statistics reflect a similar trend: 2-yr patient survival rates for recipients between the ages of 0 to 4 have improved from 80% in 1984 to 89.2% in 1987 (21). Nevertheless, there is concern over the administration of a known nephrotoxic drug to recipients who will depend on renal replacement therapy for their entire lives. This study demonstrates that, at 5 yr posttransphant, there is no significant difference in renal allograft function between CSA and non- CSA recipients. Renal transplantation in infants is a major focus at our institution. We currently perform 25% of all infant renal transplants in the United States (1). Success follows experience. Experience has taught us that, compared with infants on dialysis, infants with a functioning allograft live longer, have a higher S232 Volume 2 Supplement

6 Najarian et al growth rate, and are smarter, based on Bayley Scales of Infant Development. Renal transplantation is, therefore, the treatment of choice for infants <1 yr of age with ESRD. Transplantation should not be postponed on the basis of recipient age, but rather on the basis of weight. The smallest infant we have transplanted weighed 5 kg. Transplantation should not be postponed in order to find an adequate CAD donor. Living related transplants offer the best patient and graft survival rates and therefore should be encouraged. REFERENCES 1. Najarian JS, Frey DJ, Matas AJ, et at.: Renal transplantation in infants. Ann Surg 1 990;2 12: Chavers BM, Matas AJ, Nevins TE, et at. Results of pediatric kidney transplantation at the University of Minnesota. In: Terasaki Ph, ed. Clinical Transplants. Los Angeles: UCLA Tissue Typing Laboratory; 1 989:25a Sutherland DER, Fryd DS, So SKS, et at.: Longterm effect of splenectomy versus no splenectomy in renal transplant patients. Transplantation 1 984;38: Almond PS, Matas A, Gillingham K, et at.: Pediatric renal transplants-results with sequential immunosuppression. Transplantation 1992; 53: Hamill PVV, Drizd TA, Johnson CL, et at.: NCHS Growth Curves for Children. DHEW publications (PHS) Washington, D.C.: U.S. Government Printing Office; Gehan E: A generalized Wilcoxon test comparing arbitrarily singly-censored samples. Biometrika 1 965;52: Kohaut EC, Wheichel J, Waldo FB, Dietheim AG: Aggressive therapy of infants with renal failure. Pediatr Nephrol 1987; 1: Salusky lb. Lilien T, Anchondo M, Nelson PA, Fine R: Experience with continuous cycling peritoneah dialysis during the first year of life. Pediatr Nephrol 1987; 1: Alexander S. Treatment of infants with ESRD. In: Fine RN, Gruskin AB, eds. End Stage Renal Disease in Children. Philadelphia: WB Saunders Co; 1984: Moel DI, Butt K: Renal transplantation in children less than 2 years of age. J Pediatr ;99: Polinsky MS, Kaiser BA, Stover JB, Frankenfield M, Baluarte HJ: Neurohogic development of children with severe chronic renal failure from infancy. Pediatr Nephroh 1 987; 1: Bird AK, Semmler CJ: The early developmental and neurological sequelae of children with kidney failure treated by CAPD/CCPD. Pediatr Res 1 986;20:446A Kamil ES, Yadin 0, Ettenger RB, et at. : Growth after renal transplantation-a potential role for growth hormone therapy. Clin Transplant :i99 1 ;5: Tejani A, Ingulli E: Growth in children posttransplantation and methods to optimize posttransplant growth. Chin Transplant ;5: So 5K, Chang PN, Najarian JS, Mauer SM, Simmons RL, Nevins TE: Growth and development in infants after renal transplantation. J Pediatr 1986;1 10: Nevins TE: Transplantation in infants less than 1 year of age. Pediatr Nephrol 1 987; 1: Kim MS, Jabs K, Harmon W: Long-term patient survival in a pediatric renal transplantation program. Transplantation 1991 ;51 : Gomez-Campdera FJ, Robles NR, Anaya F, et at.: Kidney transplantation from anencephalic donors. Report of 5 cases and a review of the literature. Child Nephrol Urol 1990; 10: Arbus DS, Rochon J, Thompson D: Survival of cadaveric renal transplant grafts from young donors and in young recipients. Pediatr Nephrol 1991;5: Ettenger RB, Rosenthal JT, Marik J, et at.: Successful cadaveric renal transplantation in infants and young children. Transplant Proc 1989;21: O U.S. Renal Data System. USRDS 1990 Annual Data Report. Bethesda, MD: The National Institutes of Health, National Institutes of Diabetes and Digestive and Kidney Disease; Journal of the American Society of Nephrology S233

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