Infection-Related Hospitalization Rates in Pediatric versus Adult Patients with End-Stage Renal Disease in the United States
Blanche M. Chavers*,,
Craig A. Solid,
David T. Gilbertson and
Allan J. Collins*,
* Department of Pediatrics, University of Minnesota, and United States Renal Data System, Minneapolis, Minnesota
Address correspondence to: Dr. Blanche M. Chavers, University of Minnesota, Department of Pediatrics, Mayo Mail Code 491, 420 Delaware Street SE, Minneapolis, MN 55455. Phone: 612-626-2922; Fax: 612-626-2791; E-mail: chave001{at}umn.edu
Received for publication April 27, 2006.
Accepted for publication December 8, 2006.
Infection is a common cause of morbidity and mortality in patientswith ESRD. Infection-related hospitalization (IH) incidenceamong US Medicare incident pediatric and adult dialysis andtransplant patients within 3 yr of presentation was comparedfrom 1996 to 2001: Hemodialysis (HD) patients (pediatric n =1469; adult n = 305,323); peritoneal dialysis (PD) patients(pediatric n = 982; adult n = 27,119), and kidney transplant(KTx) patients (pediatric n = 1108; adult n = 31,663). IH wereidentified from principal diagnosis codes; IH cumulative incidenceand rates were calculated from claims data. Cumulative incidenceof IH at 36 mo for incident pediatric patients with ESRD during1996 to 2001 was 39.9% in HD, 51.2% in PD, and 47.4% in KTxpatients (HD or PD versus KTx, P < 0.0001). Cumulative incidencefor adults was 52.6% in HD, 51.8% in PD, and 39.8% in KTx patients(HD or PD versus KTx, P < 0.0001). IH rates per 1000 patient-monthswere highest for pediatric KTx patients (adjusted rate ratio1.53 versus HD and 1.90 versus PD, P < 0.001 for each) andadult HD patients (adjusted rate ratio 1.20 versus KTx and 1.11versus PD, P < 0.001 for each). Within the first 36 mo ofincidence, IH rates are highest for incident pediatric KTx patientscompared with HD and PD patients, in contrast to findings foradult patients with ESRD. Pediatric KTx patients require infectionsurveillance after transplantation.
Infection is a significant cause of morbidity and mortalityin pediatric and adult patients with ESRD. It accounted for14.6% of deaths in all prevalent ESRD patients in the UnitedSates for 2000 through 2002 combined (1). It accounts for 15.6to 29.8% of deaths in pediatric patients with ESRD (1–3).Mortality rates as a result of infection are higher in adultdialysis and kidney transplant (KTx) patients compared withthe adult general population (4). Infection is a frequent causeof hospitalization in patients with ESRD (1,5–11). Factorsthat lead to increased risk for infection in these patientsinclude immune dysfunction, malnutrition, young or advancedage, comorbid conditions such as diabetes, vascular access devices,and immunosuppression (4,10–15). Detailed data are notavailable on the frequency of infection-related hospitalizations(IH) for a national population of children with ESRD by treatmentmodality, and no study has compared IH rates between childrenand adults with ESRD. We therefore investigated IH rates inpediatric and adult US Medicare dialysis and KTx patients todetermine the incidence and types of IH rates by treatment modality.
Data and Sources
Using the US Renal Data System (USRDS), we identified patientswho initiated hemodialysis (HD) or peritoneal dialysis (PD)as their first method of renal replacement therapy (RRT) during1996 to 2001 and who had Medicare as their primary payer onor before day 91 after initiation. For purposes of analysis,day 91 was treated as day 1. We also identified first-time KTxpatients whose transplants occurred during 1996 to 2001 andwho had Medicare as their primary payer on the transplant date.For these patients, we required a Medicare claim for the transplanthospitalization but did not require the transplant to be thefirst method of RRT; KTx patients may have received previousHD or PD. Demographic data, including age, gender, race, primarycause of ESRD, and cause of death were obtained from the Identification,Medical Evidence Report (Centers for Medicare & MedicaidServices [CMS]-2728), and Death Notification (CMS-2746) sectionsof the CMS Renal Beneficiary Utilization System.
Tables 1 and 2 display demographic characteristics of patientswho were excluded because Medicare was not their primary payer.Among pediatric patients, those who were excluded from the dialysiscohort were younger, more often of white race, and initiatingPD; those who were excluded from the transplant cohort wereolder and more often of white race. Excluded adult dialysispatients were younger, more often of nonwhite race, more oftenmale, and initiating PD; excluded adult KTx patients were younger,more often male, and more often of white race.
Table 2. Characteristics of adult incident dialysis and transplant patients
We examined Medicare claims for the first 12 to 36 mo afterday 91 for dialysis patients and for the first 12 to 36 mo aftertransplant date for transplant patients. Hospitalization typewas determined by the principal diagnosis code on the claim;Appendix A shows the International Classification of Diseases,Ninth Revision, Clinical Modification (ICD-9-CM) diagnosis codesthat were used to identify IH. Hospitalization rates were calculatedas the total number of each type of hospitalization dividedby the total time at risk during the first 12 mo, where thetime at risk excluded time spent in the hospital and time aftera patient’s death, loss of eligibility, or change in RRT(dialysis to transplant, or graft loss for transplant patients).Mortality rates were calculated by dividing the total numberof deaths by time at risk. Cumulative incidence included allpatients but counted only hospitalizations that occurred beforeloss of eligibility or change in RRT.
Statistical Analyses
Statistical significance was determined by 2 analysis when percentageswere compared or by a general linear model when hospitalizationor mortality rates were compared and adjusted for age, gender,race, primary cause of renal failure, length of time on RRT,and cohort year. Patients who appeared in multiple years werecounted only once in the characteristic totals, except for totalsby year and by modality, where one patient may contribute tomultiple years or modalities (e.g., a 1996 and 1997 dialysispatient could become a 1999 transplant patient). We used patient-yearsto account for patients who appeared in multiple years. Foreach year and treatment modality, continuous data for pediatricpatients and adults were compared with t test. Differences withP < 0.05 were considered statistically significant. All analyseswere performed using SAS software (version 8.2; Cary, NC).
Patient Distributions
Patient characteristics are shown in Tables 1 and 2. HD wasthe modality for 59.2% of pediatric dialysis patients and 91.6%of adult dialysis patients. The primary cause of ESRD was glomerulonephritisfor 31.9% of pediatric KTx patients and diabetes for 29.0% ofadult KTx patients. The percentage of patients who were on eachmodality remained fairly constant throughout the cohort years.
IH
Cumulative incidence of IH during the first 12 mo was 25.7%for pediatric patients compared with 30.8% for adult patients(Table 3). Pediatric and adult HD patients showed the greatestIH disparity: 21.3% for pediatric patients compared with 31.8%for adult patients (P < 0.0001). IH percentages were 23.4%for pediatric PD and 24.4% for adult PD patients (P = 0.05).For KTx patients, cumulative incidence of IH was significantlyhigher for pediatric patients (33.3%) than for adult patients(25.5%; P < 0.0001). Cumulative incidence of IH at 36 mois shown in Table 3. For dialysis patients, cumulative incidenceof IH for internal device infection was 22.0% for pediatricand 19.3% for adult patients, compared with 4.1% for pediatricand 4.8% for adult patients for urinary tract infection (UTI).The corresponding numbers for UTI for KTx patients were 16.8%for pediatric and 10.0% for adult patients.
Comparisons of IH Rates by Modality and Age
IH rates for any infection were highest for pediatric KTx patientsand adult HD patients. The adjusted rate ratios (RR) of pediatricKTx patients to HD and PD patients were 1.53 and 1.90, respectively(P < 0.0001; Tables 4 and 5). Among KTx patients, the IHrate for pediatric patients was twice that of their adult counterparts(adjusted RR 1.99; P < 0.0001). For adults, the HD patientadjusted RR was 1.20 versus KTx patients (P < 0.0001) and1.11 versus PD patients (P < 0.0001). Adjusted IH RR forUTI were significantly higher for KTx patients in both the pediatricand adult populations, ranging from 3.90 (adults, versus HD)to 13.7 (pediatric patients, versus PD). For all modalities,pediatric patients had significantly higher adjusted IH RR forUTI. Models were re-run after patients with <30 d at riskduring the follow-up time were removed, because these patientsmay have inflated rates as a result of minimal time at risk.This sensitivity analysis showed no significant change in theresults.
Deaths
Deaths during hospitalization were more frequent among dialysispatients than KTx patients in both the pediatric and adult patientgroups, a result that also was found in the comparison of overalladjusted mortality rates (Tables 6 and 7). There was no significantdifference in overall hospitalization deaths between the pediatricHD and PD patient groups (4.6 versus 4.2%; P = 0.70), but overalladjusted mortality seems higher in HD than PD patients (adjustedRR 2.12 for pediatric patients, P = 0.0012; 1.23 for adults,P < 0.0001). For adults, overall hospitalization deaths weremore frequent in PD than in HD patients (16.9 versus 13.6%;P < 0.0001). For pediatric patients, IH deaths were morefrequent in HD patients than in PD patients (8.5 versus 4.6%;P = 0.0380) or KTx patients (2.4%; P < 0.0001), but therewas no significant difference between PD and KTx patients. Foradult patients, IH deaths were more frequent in PD patientsthan in HD patients (23.1 versus 21.5%; P = 0.0004) or KTx patients(8.8%; P < 0.0001) and more frequent in HD patients thanin KTx patients (P < 0.0001). No deaths related to UTI hospitalizationoccurred in pediatric patients. For adults, death during UTIhospitalization was more frequent in dialysis than in KTx patients(8.5% HD, 9.0% PD, 1.7% KTx; P < 0.0001) but did not differbetween PD and HD patients. For pediatric patients, death duringhospitalization for device infection occurred in 2.8% of HDpatients and in no PD patients. For adult patients, death duringhospitalization for device infection was nearly twice as frequentin PD patients compared with HD patients (20.4 versus 11.3%;P < 0.0001). Overall adjusted mortality rates followed apattern similar to that of hospitalization deaths, with theexceptions shown in Tables 6 and 7.
Our data show that hospitalization for infection is common inincident US pediatric and adult patients with ESRD, with 12-mocumulative incidence between 25 and 31% for both groups. Previousstudies reported IH rates in adults with ESRD to vary between13 and 35% (5–8,16). The IH rates for this national sampleof 332,442 adult incident dialysis patients are similar to the35% reported for a contemporary US adult HD cohort (6). OurIH rate of 39.8% over 3 yr in a national sample of 31,663 adultKTx patients is somewhat higher than the 18.5% reported in asingle-center study of 220 adult KTx patients who received atransplant between 1990 and 1999 (8). However, infection alsowas the major cause of hospitalization for those study patients.Although the USRDS database pertains to a national population,it is unclear how IH rates would have been affected by the inclusionof excluded patients. Both old age and young age are risk factorsfor infection in patients with ESRD, and excluded pediatricand adult dialysis patients were younger than included patients.
To our knowledge, ours is the first study to compare IH ratesfor both pediatric and adult US incident patients with ESRDand the first to examine IH rates by treatment modality forchildren with ESRD. We found variation in rates of IH by ageand by ESRD modality. Adult HD patients had a 10 to 12% highercumulative incidence of IH than did pediatric HD patients. Thereason for this difference is unexplained; risk factors forinfection, such as access device application, affinity of organismsfor foreign materials, dialyzer membrane interaction, uremia,nasal and skin colonization with bacteria, vitamin D deficiency,and malnutrition are common to both adults and children (12–14,17).A possible explanation is that most adult patients with ESRDare treated with hemodialysis and the waiting lists for transplantationare long, whereas nearly three fourths of pediatric patientswith ESRD receive a transplant within 3 yr of developing ESRD.We found little difference in the incidence of IH between adultand pediatric PD patients.
Although the rates per 1000 patient-months of access-relatedIH were similar for children and adults, a greater percentageof IH was due to access devices in pediatric HD patients thanin adult HD patients (43 versus 27%; data not shown). Otherstudies have reported access-related IH incidence to range from1.5 to 23% in adult HD patients (5,6,18). A higher percentageof pediatric patients undergo dialysis with catheters for vascularaccess compared with adults. For 2002, approximately 40 to 50%of adult patients with ESRD initiated dialysis with catheterscompared with 78% for pediatric patients who were younger than13 yr and 44% for those who were 13 yr and older, which mayexplain partially the increased incidence of IH in pediatricHD patients (19). In a retrospective cohort study of nearly7500 adult HD patients, the use of a venous catheter for dialysiswas associated with a higher incidence of death as a resultof infection (3.4%) compared with use of a graft (1.2%) or afistula (0.8%; P < 0.001) (15).
Our results show that IH rates for any infection during thefirst 12 mo after initiation of ESRD therapy are highest forpediatric KTx patients compared with adult KTx patients andwith pediatric and adult dialysis patients. The adjusted rateof IH for pediatric KTx patients is between one-and-a-half andtwo times that for pediatric dialysis patients and almost twicethat of adult KTx patients.
We did not break down instances of IH by type of infection becauseoften the specific organism was unknown. The most common infectiondiagnoses included the specification "organism NOS." Therefore,we were unable to classify the infection as bacterial, viral,or fungal. It is unclear how new protocols with immunosuppressionfor transplant patients will affect future rates. However, NorthAmerican Pediatric Renal Transplant Cooperative Study (NAPRTCS)data show that despite changes in induction and maintenanceimmunosuppression protocols for pediatric patients since 1987,a more recent year of transplantation is associated with increasedIH (11). Similarly, although intuitively the "Fistula First"protocol for dialysis patients should reduce the rate of accessinfections in the future, our analysis is based on diagnosiscodes that do not distinguish between access infections forcatheters, fistulas, or grafts; attributing infections for KTxpatients to central lines therefore also is impossible. Morespecific data collection is needed to assess these differences.
Few studies examine IH rates in children with ESRD. Furth etal. (20) reported hospitalization risk for 1112 prevalent pediatricESRD patients, 44% dialysis and 54% KTx, who were aged 17 yror younger, had growth failure (defined as >2 SD below themean in height for age and gender), and participated in a 1990special USRDS Pediatric Growth and Development study. Overall,73% of patients were hospitalized during 5 yr of follow-up,and infection accounted for 53% of the hospitalizations (20).IH rates were not compared by type of dialysis modality. A retrospectivestudy using NAPRTCS data evaluated morbidity and mortality in1942 children, 69% PD and 31% HD, who had anemia (defined ashematocrit <33%) and initiated dialysis between 1992 and2001 (9). Overall, 857 patients, 44% PD and 46% HD, were hospitalizedwithin 12 mo of start of dialysis (9). At 7 to 12 mo after thestart of dialysis, infection was the cause of 27% of hospitalizationsfor nonanemic PD patients, 28% for anemic PD patients, 3% fornonanemic HD patients, and 21% for anemic HD patients (9). Causesof IH were not examined.
A recent report from NAPRTCS compared hospitalization incidencefor infection and rejection during a 2-yr period for 6701 childrenwho received transplants between 1987 and 2000 (11). In theNAPRTCS study, the percentage of IH increased slightly overallfrom 38% in 1987 to 40% in 2000 (11). We found no significantvariation in IH rates for pediatric KTx patients for each calendaryear between 1996 and 2001. NAPRTCS is a voluntary registry,and the reporting of hospitalizations or cause of hospitalizationmay have been incomplete.
We found IH rates for UTI to be high for both adult and pediatricKTx patients. In the single-center study of 164 pediatric KTxpatients, UTI was the most common cause of IH beyond the first2 wk after transplantation (10). The larger NAPRTCS study ofpediatric KTx patients did not report IH data by site of infection(11). In a retrospective cohort study of 28,942 adult MedicareKTx patients in the USRDS database between January 1, 1996,and July 31, 2000, 28% had claims for UTI during a hospitalization(21). UTI was coded as the primary discharge diagnosis in 25%of the 8812 KTx patients with inpatient claims for it.
Deaths during IH were more frequent for dialysis patients thanfor KTx patients in both the adult and pediatric patient groups.For pediatric dialysis patients, deaths during IH were morefrequent for HD than for PD patients. In the pediatric dialysisstudy by Warady and Ho (9), infection was the primary causeof death in 21% of anemic patients and 18% of nonanemic patients.However, infection-related deaths were not analyzed by hospitalizationstatus, cause of hospitalization at the time of death, or typeof dialysis. Infection as a major cause of death among pediatricpatients with ESRD is well documented (1–3,9,20,22–24).However, we could not find previous pediatric studies that evaluatedpatients with ESRD for IH deaths or analyzed infection-relateddeaths by type of treatment modality. For adult dialysis patients,deaths during IH were more frequent in PD than in HD patients.A study from the 1990s compared cause of death among a largenational sample of prevalent adult dialysis patients using USRDSdata and found a 40% higher infection-related death rate forPD patients (4.8 per 100 patient-years) compared with HD patients(3.4 per 100 patient-years) (25). Although the findings aresimilar to ours, their analysis was not limited to deaths duringIH.
A potential limitation of our study is that we examined IH usingonly ICD-9-CM codes that listed infection as the primary diagnosisfor hospitalization. This limitation is offset, however, bythe fact that the national Medicare data contain relativelycomplete hospitalization records. We relied on information thatwas contained in the CMS Death Notification (CMS-2746) for causeof death; these forms may contain some inaccuracies. The criteriafor admission to hospital may differ between pediatric and adultpatients. Finally, we did not analyze for adequacy of dialysis.Despite the limitations, a large national study such as thisone may be the only way to assess the complications that weaddress.
Our study of incident US patients with ESRD shows that pediatricpatients have a high burden of hospitalizations from infection.Compared with adults, pediatric patients have fewer IH on HDand more IH after KTx. These results indicate opportunity forimprovement in reducing infection and IH rates in patients withESRD. In particular, pediatric KTx patients require more infectionsurveillance and likely require prolonged prophylactic antibiotictreatment after transplantation. A focus of future researchshould include analysis of secondary infections during hospitalizationsin patients with ESRD and differences in IH death rates forPD and HD patients.
The data reported here were supplied by the USRDS. This studywas performed as a deliverable under contract N01-DK-9-2343(National Institute of Diabetes and Digestive and Kidney Diseases,National Institutes of Health, Bethesda, MD). The authors haveno conflict of interest with its subject matter.
We thank our USRDS colleagues Beth Forrest for manuscript preparationand submission assistance and Nan Booth, MSW, MPH, for editorialassistance.
Footnotes
Published online ahead of print. Publication date availableat www.jasn.org.
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Abstract
Introduction
2 analysis when percentages were compared or by a general linear model when hospitalization or mortality rates were compared and adjusted for age, gender, race, primary cause of renal failure, length of time on RRT, and cohort year. Patients who appeared in multiple years were counted only once in the characteristic totals, except for totals by year and by modality, where one patient may contribute to multiple years or modalities (e.g., a 1996 and 1997 dialysis patient could become a 1999 transplant patient). We used patient-years to account for patients who appeared in multiple years. For each year and treatment modality, continuous data for pediatric patients and adults were compared with t test. Differences with P < 0.05 were considered statistically significant. All analyses were performed using SAS software (version 8.2; Cary, NC). 
