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Published ahead of print on December 6, 2006
Clin J Am Soc Nephrol 2: 100-106, 2007
© 2007 American Society of Nephrology
doi: 10.2215/CJN.01820506
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Epidemiology and Outcomes

Effects of Urinary Tract Infection on Outcomes after Renal Transplantation in Children

Vikas R. Dharnidharka*, Lawrence Y. Agodoa{dagger}, and Kevin C. Abbott{ddagger}

* Division of Pediatric Nephrology, University of Florida College of Medicine, Gainesville, Florida; {dagger} National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Bethesda, Maryland; and {ddagger} Nephrology Service, Walter Reed Army Medical Center, Washington, DC, and Uniformed Services University of the Health Sciences, Bethesda, Maryland

Address correspondence to: Dr. Vikas R. Dharnidharka, Division of Pediatric Nephrology, PO Box 100296, University of Florida Health Science Center, 1600 SW Archer Road, Gainesville, FL 32610-0296. Phone: 352-392-4434; Fax: 352-392-7107; E-mail: vikasmd{at}ufl.edu


   Abstract
Top
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 Conclusion
 Disclosures.
 References
 
Urinary tract infection (UTI) is the most common infection after kidney transplantation. A previous analysis showed that late (>6 mo after transplantation) UTI is associated with earlier graft loss in adults. It was hypothesized that children who are younger than 18 yr would be at higher risk to develop UTI and develop graft loss after both early and late UTI. The US Renal Data System database was analyzed from 1996 to 2000 for Medicare claims (composite of inpatient and outpatient) for UTI up to 36 mo after transplantation. SPSS software and Cox regression models were used to determine association of UTI and age after adjustment for covariates. Early UTI was defined as occurring <6 mo after transplantation, and late UTI was defined as occurring ≥6 mo after transplantation. The risk for graft loss after early UTI was elevated in all children (adjusted hazard ratio [AHR] 5.47; 95% confidence interval [CI] 1.93 to 15.4; P < 0.001) but not after late UTI (AHR 2.09; 95% CI 0.56 to 7.80; P = 0.27). Risk for posttransplantation death was not increased significantly after either early UTI (AHR 1.23; 95% CI 0.37 to 4.08) or late UTI (relative risk 2.22; 95% CI 0.90 to 5.44). Boys aged 2 to 5 (versus age 13 to <18 years) were at significantly higher risk for UTI. In girls, only those in the youngest age category (0 to 1) had higher risk for UTI. Children are at greater risk for graft loss after early but not necessarily late UTI. UTI was not an independent predictor of death in this population.


   Introduction
Top
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 Conclusion
 Disclosures.
 References
 
In adults, urinary tract infection (UTI) after renal transplantation has been associated with significant morbidity (1). The use of postoperative antibiotic prophylaxis has reduced dramatically the incidence of UTI after renal transplantation in the past few decades (2,3). Nevertheless, the rates of serious posttransplantation complications that are associated with UTI, such as bacterial septicemia, remain high for patients even in the modern era (4). Most centers generally stop antibiotic prophylaxis within 3 to 6 mo after kidney transplantation in adult and pediatric recipients (5). Late posttransplantation UTI (occurring >6 mo after transplantation) is widely considered to be "benign" on the basis of data from relatively small studies (6,7). However, more recent studies suggest that even late UTI after renal transplantation has definite risks (8). In adults, we demonstrated from a recent large data analysis of the US Renal Data System (USRDS) that late UTI in adult renal transplant recipients is associated with a higher risk for both graft loss and patient death (8); late UTI may not be as benign as previously believed. However, the impact of posttransplantation UTI on outcomes in children may not be identical to the impact in adults.

Children have a different distribution of causes of ESRD, such as a high proportion of congenital lesions such as reflux nephropathy or posterior urethral valves. In addition, primary bladder dysfunction frequently is associated with these congenital lesions. These factors may predispose to a higher incidence of UTI after transplantation in children. In fact, UTI is cited as the most common infection after renal transplantation in children who are older than 5 yr (9), yet, to our knowledge, no studies have analyzed the impact of early or late UTI on renal allograft survival in children. In adults, UTI are associated with other comorbid conditions, such as congestive heart failure, diabetes, and hospitalized infections. Comorbid conditions are far less common in children, and children may allow a more "focused" assessment of the impact of UTI on graft outcomes. To determine the effects of early or late posttransplantation UTI on pediatric patient survival and graft loss, we conducted a retrospective cohort study of the USRDS registry data on children who underwent renal transplantation in the United States between January 1, 1996, and July 31, 2000.


   Materials and Methods
Top
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 Conclusion
 Disclosures.
 References
 
Patients
Details of the files that were used for data abstraction for this study, as well as limitations of Medicare claims data, were described previously (10,11) and differ by year of selection and limitations of key variables. Files that were used and merged in our analysis were SAF.TXUNOS for the base transplant information, which was merged with SAF.TXFUUNOS for follow-up information, SAF.TXIUNOS for medication information, SAF.PATIENTS for dates and causes of death, SAF.RXHIST60 for follow-up dates and information on dialysis modality before the date of transplantation, SAF.MEDEVID for information on comorbid conditions and laboratory results at the time of first treatment for ESRD, and SAF.HOSP for Medicare claims and payment information. Physician supplier codes also were assessed. SAF.PAYHIST was used to verify the dates when patients filed Medicare institutional claims with Medicare as their primary payer. Files were merged using unique identifiers. In this study, the USRDS included follow-up (including dates of death) until October 31, 2001. However, the dates for which Medicare claims were available was December 31, 2000. Our study limited the analysis to kidney transplants that occurred in an individual recipient (one transplant assessed per recipient, which could include a repeat transplant or multiple-organ transplant) with documentation of Medicare as primary payer from January 1, 1996 to July 31, 2000.

Outcomes
Our primary dependent ("outcome") variables were (1) death from any cause and (2) graft loss (including death with function, as per conventional definitions). Our secondary outcome was time to the first Medicare claim for UTI.

Survival Times
Time to death was defined as time from the date of transplantation until death, censored for loss to follow-up (as indicated in USRDS treatment history files) or the end of the study period, which in this case was October 31, 2001. Time to graft loss was defined as the time from the date of transplantation until the date of graft loss, death, loss to follow-up, or the end of the study period (October 31, 2001). Time to Medicare claims for UTI was calculated primarily as the time from the date of transplantation until the date of the first Medicare claim for UTI (whether physician provider of institutional claim) that occurred after renal transplantation during the study period, with recipients censored at time of death, loss to follow-up, 3 yr after renal transplantation, or the end of the study period (December 31, 2000, the most recent date of Medicare claim available).

Independent Variables
Our primary independent variable was Medicare institutional claims for UTI after renal transplantation. Diagnosis was based on the International Classification of Diseases, Ninth Revision codes 590.x ("kidney infection," including pyelonephritis both acute and chronic), 595.0x ("acute cystitis"), or 599.x ("urinary tract infection," not otherwise specified). For assessment of differential effects of subgroups of UTI, namely pyelonephritis and hospitalization for a primary or secondary discharge diagnosis of UTI, separate analyses also assessed whether these outcomes had significant associations with death and graft loss independent of all UTI. "Late" UTI was defined as UTI that occurred >6 mo after transplantation. UTI also was assessed as a primary hospitalization discharge diagnosis and all-listed diagnosis of the same International Classification of Diseases, Ninth Revision codes as above. Patient characteristics and treatment factors were those at the date of transplantation. Information on urethral catheterization, postsurgical complications, antibiotic prophylaxis or treatment, and results of urinalyses including urine cultures was not available. The duration of dialysis before transplantation was defined as the time from the first recorded treatment for dialysis therapy until the date of transplantation. The serum creatinine level was obtained as the most recent serum creatinine level available before the end of the first 6 mo after renal transplantation. Other variables assessed included donor and recipient age, race, gender, weight, and body mass index (calculated from height and weight). Specific causes of ESRD assessed included diabetes, chronic pyelonephritis, chronic obstruction, polycystic kidney disease, and systemic lupus erythematosus (other causes were not excluded but were not identified specifically). Recipient age was categorized further as 0 to 1, 2 to 5, 6 to 12, and 13 to <18 yr. Treatment with peritoneal dialysis for any 60-d period before transplantation was obtained from patient treatment files.

Statistical Analyses
All analyses were performed using SPSS 13.0 (SPSS, Chicago, IL). Files were merged and converted to SPSS files using DBMS/Copy (Conceptual Software, Houston, TX). Additional analyses were validated in Stata 9.0, Intercooled (College Station, TX). Analyses were performed with {chi}2 testing for categorical variables (Fisher exact test used for violations of Cochran assumptions) and t test for continuous variables (Mann-Whitney test was used for non-normally distributed variables). Statistical significance for univariate comparisons was defined as P < 0.05. Variables with P < 0.10 in univariate analysis for a relationship with development of a first Medicare claim for UTI were entered into multivariate analysis as covariates because of the possibility of negative confounding. Variables that were thought to have a known clinical reason to be associated with UTI were introduced into multivariate models even when univariate P values were >0.10, in accordance with established epidemiologic principles (12). Continuous variables were explored, and values that were believed to be inconsistent with clinical experience were excluded.

The independent association between patient factors and time to the first Medicare claim for UTI during the study period was examined using multivariate analysis with Cox regression (likelihood ratio method), controlling for variables that were entered into the model as described previously. Both formal and graphical assessments for all covariates in the final models were performed to verify the existence of proportional hazards. Multivariate analysis will exclude all patients with missing values, likely resulting in substantially smaller models than the entire study population. Continuous variables that were non-normally distributed also were assessed by quartiles. Models also substituted mean values for missing values of continuous variables ("interpolation"), to assess for potential bias that results from exclusion of patients with missing values. Hierarchically well-formed models were used for the assessment of interaction terms. Interaction terms that were found to be statistically significant in Cox regression analysis were presented stratified for each level of the covariate, as appropriate. The independent association of Medicare claims for UTI with patient mortality and graft loss was determined using Cox nonproportional hazards regression assessing the time of the first Medicare claim for UTI as a time-dependent variable, with times after the first Medicare claim for UTI coded as 1 and all other times coded as 0, as in previous reports (13,14). To assess for possible bias of repeated UTI affecting survival associated with late UTI, analysis of late UTI also excluded patients who were coded for UTI during an earlier period of the study. Analysis of the association between UTI and outcomes (death and graft loss) is complicated further by the fact that rates of UTI, death, and graft loss are not constant over time; in fact, rates of all three outcomes are more common early after transplantation than late. Therefore, late UTI was defined as UTI that occurred 6 mo or more after renal transplantation, and outcomes assessed were death or graft loss that occurred after the diagnosis of UTI, compared with recipients who did not develop UTI.


   Results
Top
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 Conclusion
 Disclosures.
 References
 
There were 52,235 recipients of renal transplants from January 1, 1996, to July 31, 2000, 2782 of whom were younger than age 18 yr. Of these, 870 pediatric patients had evidence of Medicare as primary payer at the time of transplantation. In comparison with non-Medicare primary pediatric patients, the Medicare primary pediatric patients were slightly older (mean age 11.9 ± 5 versus 11.3 ± 5 yr; P = 0.003 by t test), more likely black (35.2 versus 26.4%; P < 0.001 by {chi}2), but not significantly different by gender (27.5 versus 29% male; P = 0.35). During the study period, 265 (30.5%) pediatric patients had either inpatient or outpatient claims for UTI. The study cohort characteristics are shown in Table 1.


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  		Table 1. Demographic characteristics of study cohort with Medicare claims for UTI in renal transplant recipients between January 1, 1996, and July 31, 2000, with Medicare as primary payer, age ≤18 yra

 
Our initial Cox regression multivariate analyses comprised all claims for UTI (inpatient + outpatient combined = composite). These analyses focused on the effect of UTI on graft survival (Table 2) or patient survival (Table 3) and the role of covariates. Subsequently, we performed identical analyses of UTI effects on graft and patient survival and role of covariates for hospitalized UTI only (Tables 4 and 5, respectively). The purpose of analyzing separately for hospitalized UTI was to determine whether the more severe and clinically significant condition had a different impact on patient and graft survival. In the past, we have shown that hospitalization for infection has increased over time in pediatric kidney transplant patients and that infection now is the predominant cause for hospitalization (15).


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  		Table 2. AHR for graft loss in transplant recipients who were younger than 18 yr with all UTI after transplantation (inpatient + outpatient)a

 

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  		Table 3. Cox regression analysis for risk for posttransplant death after all UTI in transplant recipients who were younger than 18 yr

 

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  		Table 4. AHR for graft loss in transplant recipients who were younger than 18 yr of age and had hospitalized UTI

 

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  		Table 5. Cox regression analysis for risk for posttransplantation death after hospitalized UTI in transplant recipients who were younger than 18 yr age and had either early or late UTIa

 
As shown in Table 2, early composite UTI in children was associated with a significantly higher adjusted hazard ratio (AHR) for graft loss (P = 0.007). Within this pediatric age group, recipient black race and deceased donor source were associated significant risk factors but not recipient age, history of peritoneal dialysis, or recipient gender. In contrast to early composite UTI, late composite UTI >6 mo after transplantation was not associated with a significantly higher AHR for graft loss (Table 2). Covariates that were associated significantly with late composite UTI included recipient black race and recipient age but not recipient gender, deceased donor source, or history of peritoneal dialysis.

Table 4 shows the factors that are independently associated with earlier graft loss after development of early hospitalized UTI. The AHR for earlier graft loss was significantly higher. Covariates that were associated significantly with early hospitalized UTI included recipient age and delayed graft function. However, other covariates, such as recipient or donor gender or race or primary diagnoses such as chronic pyelonephritis and obstructive uropathy, were not significantly associated. Again, in contrast to early hospitalized UTI, the development of late hospitalized UTI was not associated with a significantly higher AHR for earlier graft loss (Table 4). The covariates that were associated significantly with late hospitalized UTI were the same as early hospitalized UTI: Recipient age and delayed graft function.

Tables 3 and 5 depict the effects of UTI on patient survival. As shown in Table 3, neither early nor late composite UTI had a significant effect on patient survival. In contrast, early hospitalized UTI was associated with a significantly higher AHR of patient death (Table 5). Late hospitalized UTI was not associated with a higher AHR for patient death.

Finally, we stratified the pediatric age group into smaller groups and determined the AHR for developing UTI by 3 yr after transplantation, using age 13 to <18 as the reference group. As shown in Table 6, among girls, the youngest childhood age category (0 to 1) had the highest and significant AHR for developing UTI. In contrast, among boys, those who were aged 2 to 5 were at significantly higher risk for UTI compared with reference.


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  		Table 6. AHR for children who developed UTI by 3 yr after transplantation, distributed by recipient gender and age category (reference category age 13 to <18)

 

   Discussion
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
Conclusion
 Disclosures.
 References
 
UTI is the most common infection seen after kidney transplantation, although different studies report widely varying incidence rates (8,16,17). The effect of early or late UTI after kidney transplantation on graft life and patient mortality has been controversial, with some studies reporting adverse effects of UTI on both parameters (18), whereas other studies did not (16,19). Risk factors for developing UTI after kidney transplantation also have varied among studies. The risk factors reported have included female recipient gender, white or black race, deceased donor source of kidney, reflux kidney disease, and use of azathioprine or cyclosporin A (16,20).

In our previous analysis of the USRDS database for UTI in adult kidney transplant recipients, the cumulative incidence of early UTI was 17% for both genders (8). By 3 yr after transplantation, the cumulative incidence was 60% in adult female recipients and 47% in adult male recipients. Recent articles from single centers have reported similar frequencies, suggesting that the use of Medicare claims reporting is a valid measure (21,22). In our previous study of adults, the occurrence of late UTI >6 mo after transplantation was associated with a significantly higher AHR for both graft loss and patient death. Factors that were associated with a higher risk for developing UTI after kidney transplantation in the adult population included female gender; black race; primary renal disease being chronic obstruction, chronic pyelonephritis, or polycystic kidney disease; recipient history of diabetes; and acute rejection episode within the first 6 mo. These results essentially were the same whether the UTI was coded in an outpatient or a composite (inpatient + outpatient) manner.

In our study, which was focused on childhood recipients who were younger than 18 yr, the biggest contrast that we found was that early, not late, composite UTI was associated with a significantly higher AHR for graft loss. Neither early nor late composite UTI was associated with a significantly higher AHR for patient death. However, when the analysis was limited to hospitalized UTI only, both early and late UTI were associated with a significantly higher AHR for graft loss. Early hospitalized UTI also was associated with a higher risk for patient death. Overall, age younger than 18 yr was not a significant risk factor for UTI in comparison with older age, but gender and age differences became more apparent when the under-18 age group was stratified in greater detail. Some of the risk factors for developing UTI that were seen in adults held true for children as well. Delayed graft function, defined as need for dialysis in the first week after transplantation, not only increases the risk for catheter-associated bacteremia but also prolongs the transplant hospitalization stay and is associated with greater length of bladder catheterization. Diabetes increases the risk for UTI in adult kidney transplant studies, but the incidence of preexisting diabetes in children who need kidney transplants is very low.

To our knowledge, the only study that is similar to our study was a small, single-center analysis of 47 children with 58 renal transplants from 1997 to 2000 (23). In this study, with a mean follow-up time of 3.5 yr, 32% of the children developed UTI, but there was no increased risk for UTI associated with recipient gender, donor source, or primary disease. The small sample size in this study may have prevented some of the risk factors from being elucidated. More recently, Van der Weide et al. (24) studied children with renal transplants and found that UTI were associated with a worse renal function even 2 mo after the UTI, suggesting long-term damage.

Limitations of this study are similar to our previous study in adult kidney transplant recipients. The diagnosis and coding of UTI was by center report, and criteria that were used for diagnosis or coding variations are not known. UTI may be merely a marker for sicker patients and not itself a cause for either graft loss or patient death. This point may serve to explain why both early and late hospitalized UTI were significant risk factors for graft loss and patient death in our study, whereas composite UTI were not. Data on antibiotic prophylaxis use are not captured reliably in Medicare claims files and therefore could not be analyzed. We were unable to control for bladder dysfunction (other than as cause of ESRD), intermittent catheterization, and antibiotic prophylaxis. In addition, for children, Medicare serves as the primary insurance coverage for only some children in the first 3 yr after kidney transplantation. In many children, Medicaid rather than Medicare may be the primary insurance coverage. The USRDS files to which we had access for this study did not reliably capture Medicaid claims.


   Conclusion
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Conclusion
Disclosures.
 References
 
Our study of the USRDS database and Medicare claims files for UTI show that children are affected differently by UTI than adult kidney transplant recipients. Early composite or hospitalized UTI has significant adverse effects on graft survival, and early hospitalized UTI also increases risk for patient death. Kidney transplant professionals focus mainly on reducing the risk for acute rejection. Our studies suggest that reducing the risks for UTI would be beneficial as well.


   Disclosures.
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Conclusion
 Disclosures.
References
 
None.


   Acknowledgments
 
V.R.D. is supported in part by National Institutes of Health grant 1R21DK069535.

This study was presented in part at the 37th annual meeting of the American Society of Nephrology, October 29 through November 1, 2004, in St. Louis, MO.


   Footnotes
 
Published online ahead of print. Publication date available at www.cjasn.org.

The opinions expressed in this article are solely those of the authors and do not represent an endorsement by the Department of Defense or the National Institutes of Health. This is a US government work; there are no restrictions on its use.

Received May 25, 2006. Accepted November 3, 2006.


   References
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Conclusion
 Disclosures.
 References
 

  1. Schmaldienst S, Dittrich E, Horl WH: Urinary tract infections after renal transplantation. Curr Opin Urol12 :125 –130,2002[CrossRef][Medline]
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  9. Chavers BM, Gillingham KJ, Matas AJ: Complications by age in primary pediatric renal transplant recipients. Pediatr Nephrol11 :399 –403,1997[CrossRef][Medline]
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  11. Abbott KC, Oglesby RJ, Hypolite IO, Kirk AD, Ko CW, Welch PG, Agodoa LY, Duncan WE: Hospitalizations for fractures after renal transplantation in the United States. Ann Epidemiol11 :450 –457,2001[CrossRef][Medline]
  12. Szklo M, Nieto FJ: Stratification and adjustment: Multivariate analysis in epidemiology. In: Epidemiology: Beyond the Basics, Gaithersburg, Aspen Publishers,2000 , p257
  13. Ball AM, Gillen DL, Sherrard D, Weiss NS, Emerson SS, Seliger SL, Kestenbaum BR, Stehman-Breen C: Risk of hip fracture among dialysis and renal transplant recipients. JAMA288 :3014 –3018,2002[Abstract/Free Full Text]
  14. Ojo AO, Meier-Kriesche HU, Hanson JA, Leichtman A, Magee JC, Cibrik D, Wolfe RA, Port FK, Agodoa L, Kaufman DB, Kaplan B: The impact of simultaneous pancreas-kidney transplantation on long-term patient survival. Transplantation71 :82 –90,2001[CrossRef][Medline]
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