Article

Survival in Pediatric Dialysis and Transplant Patients

Susan M. Samuel,* Marcello A. Tonelli, Bethany J. Foster, R. Todd Alexander, Alberto Nettel-Aguirre,*
Andrea Soo,* Brenda R. Hemmelgarn,* and the Pediatric Renal Outcomes Canada Group

Summary
Background and objectives Long-term follow-up data are few in children with ESRD. We sought to describe
long-term survival, assess risk factors for death, and compare survival between two time periods in pediat-
ric ESRD patients.
*University of Calgary,
Calgary, Alberta,
Design, setting, participants, & measurements We used a population-based retrospective cohort utilizing Canada; Alberta
data from a national organ failure registry and from Canadas universal healthcare system. We included Childrens Hospital,
Calgary, Alberta,
843 children (ages, 0 to 18) initiating renal replacement therapy from 1992 to 2007 and followed them until
Canada; University of
death or date of last contact (median follow-up, 6.8 years; interquartile range, 3.0 to 10.6). We assessed risk Alberta, Edmonton,
factors for death and examined cause-specific mortality. Alberta, Canada; McGill
University, Montreal,
Quebec, Canada; and
Results During 5991 patient-years of follow-up, 107 (12.7%) patients died. Unadjusted cumulative survival
Montreal Childrens
for the cohort was: 91.7% (95% CI, 89.8 to 93.7%) at 5 years and 85.8% (95% CI, 82.8 to 88.8%) at 10 years. Hospital, Montreal,
Among patients commencing dialysis, overall adjusted survival was poorest among those who started dial- Quebec, Canada
ysis at age 1 year. No secular trends in survival were noted for either dialysis or transplant patients. The
proportion of incident patients receiving pre-emptive transplantation increased over time. Pre-emptively Correspondence: Dr.
transplanted patients did not demonstrate superior adjusted survival compared with those who spent 2 Susan M. Samuel, 2888
Shaganappi Trail NW,
years on dialysis before transplant (hazard ratio, 1.53; 95% CI, 0.63 to 3.67).
Alberta Childrens
Hospital, Calgary, AB
Conclusions No significant improvements in survival were observed among ESRD patients over the study T3B 6A8, Canada.
period. Time with transplant function had the strongest association with survival. Pre-emptive transplanta- Phone: 403-955-7439;
Fax: 403-955-2203;
tion was not associated with improved survival in adjusted models.
E-mail: s.samuel@
Clin J Am Soc Nephrol 6: 1094 1099, 2011. doi: 10.2215/CJN.04920610 albertahealthservices.ca.

Introduction nadian Institute for Health Information Discharge

Age-specific mortality rates for children treated with
dialysis and kidney transplantation are approxi-
mately 30 times higher than those in healthy children
(1). ESRD contributes to numerous sequelae in chil-
dren, including growth retardation, cognitive delay,
decreased exercise capacity, poor cardiovascular
health, and decreased quality of life (2 8). Substantial
improvements in pediatric dialysis and transplanta-
tion have occurred over the last four decades (1).
Established national and international registries doc-
ument excellent short term (1 to 2 years) survival
among children treated with dialysis and kidney
transplantation, as well as good allograft outcomes
(9 11). Longer-term patient outcomes are less well
described (12), especially in North America, because
of limited longitudinal data and lack of ongoing re-
porting to registries when patients are transferred
from pediatric to adult centers.
We performed a retrospective cohort study of pe-
diatric ESRD patients using a novel database (Cana-
dian Pediatric End-Stage Renal Disease Database) cre-
ated by linking data from the Canadian Organ
Replacement Register (CORR) with data from the Ca-
Abstract Database (13). CORR has prospectively col-
lected data related to organ donation and transplan-
tation in Canada since 1981 (14). We sought to de-
scribe long-term survival in the Canadian pediatric
ESRD population and to identify risk factors for
death. In addition, we aimed to assess changes in
survival over calendar time in this population.
Materials and Methods
Study Design and Population
After obtaining institutional ethics approval from
the University of Calgary, we established a cohort of
all patients in nine Canadian provinces who initiated
renal replacement therapy (RRT) (dialysis or trans-
plant) at age 18 years between January 1, 1992 and
December 31, 2007. Patients from the province of
Quebec were not included because their data were not
available for release to investigators.
Data Sources
Detailed methods on the creation of the Canadian
Pediatric End-Stage Renal Disease Database for re-
search purposes using linked data from CORR and
Canadian Institute for Health Information Discharge

1094 Copyright 2011 by the American Society of Nephrology www.cjasn.org Vol 6 May, 2011
Clin J Am Soc Nephrol 6: 1094 1099, May, 2011 Survival in Pediatric Dialysis and Transplant Patients, Samuel et al. 1095

Abstract Database are provided in the supplemental meth- versus living), a time-dependent variable indicating the status
ods section (see the Appendix) and were published previ- of transplant function (functioning versus failed with return to
ously (13). dialysis) and duration of dialysis before first transplant.
The proportional-hazards assumption in all models was
Definitions of Outcomes tested on the basis of the scaled Schoenfeld residuals (15).
The patients were followed from initiation of RRT until All of the analyses were performed using R (The R Foun-
death, loss to follow-up, or the end of observation period dation for Statistical Computing, http://cran.r-projec-
(December 31, 2007). Follow-up for all incident patients t.org).
included time spent in both pediatric and adult ESRD
centers. The primary outcome was time to all-cause mor- Results
tality, with dates of death obtained from CORR and hos- Demographic Characteristics
pitalization data. If an in-hospital death date was known Between January 1, 1992 and December 31, 2007, 858
and a death date was not recorded in the registry, the pediatric patients began RRT in Canada. Fifteen multi-
in-hospital death date was defined as the death date (three organ transplant recipients were excluded; therefore, the
deaths in the cohort not recorded in CORR were recovered experience of 843 patients (5991 person-years) was ana-
from hospitalization data). lyzed. The median duration of follow-up was 6.83 (range,
Causes of death were obtained from CORR when avail- 3.00 to 10.62) years. Demographic characteristics of the
able. The major categories were: undetermined, cardiac, in- study cohort are outlined in Table 1. There were more boys
fection, malignancy, social, and other (stroke, respiratory (52.4%) than girls in the cohort. The most common cause of
failure, gastrointestinal causes, hemorrhage, accident, and ESRD was congenital anomalies of the kidney and urinary
multiorgan failure). If a cause of death was not recorded in tract (29.9%). The mean age SD at onset of RRT was
CORR and there was record of an in-hospital death for the 11.3 5.4 years.
same patient, then the most responsible diagnosis for Peritoneal dialysis (41.6%) was the most common index
admission as recorded in the hospital discharge record for RRT modality in the cohort. A total of 165 (19.6%) patients
that hospital admission was presumed to be the cause of underwent pre-emptive transplantation without prior di-
death. alysis; of these, 50 were from deceased donors. The pro-
portion of children undergoing pre-emptive kidney trans-
plantation increased over the calendar years (1992 to 2007)
Study Variables and approached 25% at the end of observation period in
Baseline demographic data evaluated include gender,
year 2007 (Figure 1; chi-squared test for trend P 0.001).
etiology of primary renal disease, and age at onset of renal
The most common index RRT modality for children older
replacement. Index RRT modality (hemodialysis, perito-
than 10 years was hemodialysis (46.2%), whereas perito-
neal dialysis, or pre-emptive transplantation), dates, and
neal dialysis was most common for children younger than
donor type for each transplant event and dates of allograft
10 years of age (54.5%).
failure were obtained from the database.
Overall, 691 patients received a total of 747 kidney trans-
plants (636 patients had one transplant, 54 patients had
Statistical Analyses two transplants, and one patient had three transplants).
Demographic and baseline clinical characteristics were The proportion of allografts from living donors was 43.7%
described with means (SD), medians (interquartile ranges
[IQR]), or proportions. A significance level of 0.05 was
set for all statistical testing. Time from start of renal re- Table 1. Characteristics of pediatric end-stage renal disease
patients in Canada between 1992 and 2007
placement (index date) to death or date of last follow-up
(n 843)
was analyzed using the Kaplan-Meier method and Cox
proportional-hazards models. Trends in index RRT modal- Characteristic Number (%)
ity over calendar years were examined using a chi-squared
test for trends in proportions. Gender (male) 442 (52.4)
We examined two overlapping but distinct groups: those Age at onset of RRT, in years
0 to 0.9 63 (7.5)
who initiated dialysis and those who received a transplant
1.0 to 4.9 84 (10.0)
using Cox proportional-hazards models. The first model 5.0 to 9.9 148 (17.6)
determined differences in survival by age at onset of dial- 10.0 to 14.9 281 (33.3)
ysis (categorized as 1 year, 1 to 10 years, and 10 to 18 15.0 to 17.9 267 (31.7)
years) and period of start of dialysis (1992 to 1999 and 2000 Index modality of RRT
to 2007). The patients were censored at transplant, loss to peritoneal dialysis 351 (41.6)
follow-up, or study end (December 31, 2007). The model hemodialysis 327 (38.8)
was adjusted for gender and primary renal disease (con- pre-emptive transplant 165 (19.6)
genital versus other). We used interaction terms to deter- Etiology of ESRD
mine whether the effect of age at onset of dialysis varied by congenital anomalies of the 242 (28.7)
calendar period (1992 to 1999 versus 2000 to 2007). kidney and urinary tract
glomerulonephritis/ 244 (28.9)
The second Cox proportional-hazards model focused on
autoimmune
the interval after first transplant. We examined differences
genetic 112 (13.3)
in survival by period of transplant (1992 to 1999 versus 2000 other/unknown 245 (29.1)
to 2007) adjusting for first transplant donor source (deceased
1096 Clinical Journal of the American Society of Nephrology
Figure 1. | Trends in initial renal replacement modality among pe-
diatric ESRD patients in Canada. A chi-squared test was used to test
for trends in proportions (P < 0.001).
in 1992 to 1999 and increased to 57.2% during 2000 to 2007
(P 0.001). The median time to first deceased-donor trans-
plant from start of dialysis was 1.34 years (IQR, 0.75 to
2.62) between 1992 and 1999 compared with 1.75 years
(IQR, 1.00 to 2.77) between 2000 and 2007 (P 0.22). The
median time to first living-donor transplant dropped sig-
nificantly from 1.00 year (IQR, 0.58 to 1.91) between 1992
and 1999 to 0.83 year (IQR, 0.41 to 1.58) between 2000 and
2007 (P 0.02).
All-Cause Mortality
During 5991 person years of follow-up, there were 107
deaths, for a crude mortality rate of 17.9 per 1000 person-
years (95% confidence interval [CI], 14.5 to 21.2). Of these
107 deaths, 59 were in the interval between dialysis initi-
ation and first transplant (crude mortality rate, 45.2 per
1000 person years; 95% CI, 33.7 to 56.7). Twenty-three
deaths occurred with graft function (crude mortality rate,
5.5 deaths per 1000 person years; 95% CI, 3.2 to 7.7) and 25
after graft failure and return to dialysis (crude mortality
rate, 49.8 per 1000 person years; 95% CI, 30.3 to 69.3). The
unadjusted 5-year cumulative survival for the cohort was
Table 2. Characteristics of patients who died according to renal replacement modality at death
Variable
Median age at onset of RRT (IQR) in years
Males (n, %)
Median age at death (IQR) in years
Causes of death (n, %)
cardiac
infection
malignancy
social
undetermined
other
91.7% (95% CI, 89.8 to 93.7%), and the 10-year survival was
85.8% (95% CI, 82.8 to 88.8%). When patients who survived
to transplant were considered separately, the unadjusted
5-year survival was 96.8% (95% CI, 95.4 to 98.3%), and
unadjusted 10-year survival was 89.1% (95% CI: 85.7 to
92.7%).
The median age at death was 16.8 years (IQR, 7.0 to 21.9).
The median duration of dialysis therapy among those who
died without having received a transplant was 1.00 year
(IQR, 0.33 to 3.66). Median time to death after first graft
failure was 2.83 years (IQR, 0.91 to 5.08) among the 25
patients who died while on dialysis after first or subse-
quent graft failures. The demographic characteristics of
those who died, according to status of renal replacement at
death (dialysis only, transplant with function, and return
to dialysis after graft failure), are given in Table 2. Twenty-
five percent of deaths in the cohort were in-hospital deaths.
Mortality on Dialysis. In the adjusted model for mortal-
ity in the interval between dialysis initiation and first trans-
plant (censor at transplant), age 1 year at the start of renal
replacement was associated with poorer survival com-
pared with age 10 years (hazard ratio [HR], 7.82; 95% CI,
3.97 to 15.44) (Table 3). The association between age at RRT
onset and survival did not differ significantly by calendar
period of dialysis. The interaction term between age at
onset and period of dialysis was NS, indicating that the
relationship between survival and age group at the start of
dialysis did not vary by calendar period of dialysis.
Mortality after Transplantation. In the adjusted model,
patients who received their transplant between 2000 and
2007 had a 50% lower risk of death compared with those
transplanted between 1992 and 1999 (Table 4); however,
this difference was not statistically significant (HR, 0.50;
95% CI, 0.21 to 1.17). There was no significant difference in
survival by donor source (living versus deceased donor) of
first transplant (HR, 1.13; 95% CI, 0.58 to 2.21). Graft failure
with return to dialysis was strongly associated with greater
mortality risk in the adjusted model compared with a
functioning graft (HR, 7.17; 95% CI, 3.86 to 13.34). The
median time to graft failure in deceased-donor transplant
recipients was 4.75 years (IQR, 1.33 to 6.96), and that in
living-donor recipients was 4.87 years (IQR, 1.17 to 7.86).
Repeat kidney transplantation was not associated with a
change in adjusted survival, and therefore the time-depen-
Dialysis Functioning Dialysis after
before
Graft Graft Failure
Transplant (n 23) (n 25)
(n 59)
9.0 (0.415.6) 12.0 (6.914.6) 13.3 (9.916.3)
33 (55.9) 11 (47.8) 11 (44.0)
11.8 (1.318.8) 16.3 (14.122.0) 22.9 (19.224.8)
11 (18.6) 2 (8.7) 10 (40.0)
8 (13.6) 4 (17.4) 1 (4.0)
2 (3.4) 8 (34.8) 0
7 (11.9) 0 2 (8.0)
16 (27.1) 3 (13.0) 4 (16.0)
15 (25.4) 6 (26.1) 8 (32.0)
Clin J Am Soc Nephrol 6: 1094 1099, May, 2011
Table 3. Adjusted hazard ratios for mortality during interval between dialysis initiation and first transplant
Risk Factor
Age at start of dialysis
1 year
1 to 10 years
10 to 18 years
Period of start of dialysis (2000 to 2007 versus 1992 to 1999)
Etiology of renal disease) (other versus congenital anomalies)a
Gender (male versus female)
a
Other causes include: glomerulonephritis, genetic, and miscellaneous other causes of ESRD in children.
Table 4. Adjusted hazard ratios for mortality following transplant
Risk Factor
Time without renal allograft function (return to dialysis)
First transplant donor type (living versus deceased)
Period of transplant (2000 to 2007 versus 1992 to 1999)
Time spent on dialysis prior to first transplant
pre-emptive transplant
1 year
1 to 2 years
2 years
Figure 2. | Kaplan-Meier graph of overall survival according to time
spent on dialysis before first renal transplant.
dent variable indicating a repeat transplant was not re-
tained in the final model.
Mortality after Pre-emptive Transplantation. Figure 2
shows Kaplan-Meier graphs of overall survival according
to time spent on dialysis before kidney transplantation. In
unadjusted analyses, pre-emptive transplantation was as-
sociated with better survival compared with those who
spent 2 years on dialysis before first transplant (log rank,
P 0.04). However, in the adjusted model for survival
Survival in Pediatric Dialysis and Transplant Patients, Samuel et al. 1097
Hazard Ratio
(95% Confidence Intervals)
7.82 (3.97 to 15.44)
1.47 (0.70 to 3.12)
1.00 (Reference)
1.18 (0.69 to 2.03)
1.34 (0.69 to 2.60)
0.94 (0.54 to 1.62)
Hazard Ratio
(95% Confidence Intervals)
7.17 (3.86 to 13.34)
1.13 (0.58 to 2.21)
0.50 (0.21 to 1.17)
1.00 (Reference)
0.44 (0.19 to 1.05)
1.01 (0.40 to 2.54)
1.53 (0.63 to 3.67)
among transplant patients, no such association was ob-
served, as shown in Table 2. Because of the strong effect of
RRT modality (functioning transplant versus dialysis)
noted in the transplant model, we performed additional
analyses examining the association between pre-emptive
transplantation and the composite outcome of time to first
allograft failure or death, adjusting for period of transplant
and donor type. We found no significant differences
among those who were pre-emptively transplanted, as
compared with those who spent 2 years on dialysis (ad-
justed HR, 1.19; 95% CI, 0.71 to 1.99).
Causes of Death
The cause of death was classified as undetermined, car-
diac, infection-related, malignancy-related, social, and
other. There were no cases where the cause of death was
missing; 23 deaths (21.5%) were recorded as having unde-
termined causes in the registry; no further information on
cause of death could be obtained from the data source.
Cardiac deaths constituted 27.4% of all known causes of
death (myocardial ischemia and infarction (n 4), hyper-
kalemia (n 4), other causes of cardiac failure (n 4),
cardiac arrest cause unknown (n 10), and fluid overload
(n 1)). Infections (bacterial or viral) were the causes of
death in 13 (15.5%) patients. Ten (11.9%) patients died of
malignancy. Of these, two patients had hematopoietic ma-
lignancies according to hospital discharge diagnoses, and
for the remainder, the primary site of malignancy was not
recorded. Social causes of death, including death caused by
drugs, alcohol, suicide, patient refusing treatment, or ther-
apy ceased, also contributed to a significant portion of the
deaths (10.7%). Other causes of death including respira-
tory, gastrointestinal, cerebrovascular accident, hemor-
1098 Clinical Journal of the American Society of Nephrology
rhage, and accident make up the remainder of the known
causes of death (34.5%). Table 2 shows causes of death by
status of renal replacement at death. Malignancy (34.8%)
and infection (17.4%) were the most common causes of
death among the 23 patients who died with renal allograft
function.
Discussion
We studied long-term mortality among incident pediat-
ric end-stage renal disease patients treated in Canada be-
tween 1992 and 2007 using data from a national organ
failure registry within a universal health care system.
Overall, 10-year survival for the entire cohort was 86%. The
most important risk factors for mortality were dialysis as
the RRT modality and age less than 1 year of age at the
start of RRT. No significant improvements in survival after
transplantation were observed in 2000 to 2007 compared
with 1992 to 1999.
We considered survival in two distinct intervals: dialysis
initiation to first transplant and after first transplant. Be-
cause we had no information on eligibility for transplant or
wait listing, the interval between dialysis initiation and
first transplant included patients who may have been in-
eligible for transplant for various reasons (age or comor-
bidity) and therefore at higher risk for mortality. The sur-
vival estimates obtained in this study provide clinicians
with important information that can be used when coun-
seling families of children starting dialysis. Consistent with
reports from the Australia and New Zealand ESRD regis-
try and Great Ormond Street Hospital (United Kingdom)
(1,16), we found worse survival in children 1 year old at
the start of dialysis compared with older children.
The lack of significant improvements observed in sur-
vival among pediatric renal-transplant recipients is consis-
tent with recent United States Renal Data System and
North American Pediatric Renal Transplant Cooperative
Study annual reports (10,11). These findings call for further
studies describing causes and mechanisms of death among
pediatric transplant recipients and to address emerging
threats to allograft function, such as BK virus, and to
establish tailored immunosuppression strategies for best
long-term allograft survival among pediatric renal-trans-
plant recipients (17).
Peritoneal dialysis continues to be most common modal-
ity for initiating renal replacement therapy in Canada.
However, when compared with Australia and New Zea-
land data, Canadian children were more likely to initiate
renal replacement on hemodialysis (32.7% in Australia/
New Zealand versus 38.8% in Canada) (18). There are nu-
merous factors that play a role in the selection of initial
modality among children including school attendance dur-
ing the day, level of cognitive function, distance from a
nephrology unit, family, and socioeconomic circum-
stances.
We found that approximately one quarter of incident
patients in Canada underwent pre-emptive kidney trans-
plantation during the latter years of observation. Although
a survival advantage was observed among pre-emptively
transplanted patients compared with those who spent 2
years on dialysis before first transplant in the unadjusted
analysis, this benefit was not observed in adjusted models
accounting for graft function. The relatively short period of
time spent on dialysis before first transplant in those who
were not pre-emptively transplanted likely played a role in
minimizing the mortality risks associated with dialysis.
Although overall survival among pediatric transplant pa-
tients is strongly associated with transplant function irre-
spective of first or repeat transplant status, clinicians do
not have advance knowledge of transplant function in a
particular patient. Therefore, the crude mortality data as
demonstrated by Kaplan-Meier curves may serve as a ref-
erence to guide discussions regarding risks and benefits of
time spent on dialysis before first transplant.
McDonald and Craig (1) published the largest retrospec-
tive review of 1634 children and adolescents with ESRD
and found that 30% of patients with initial kidney trans-
plant function died from cardiac disease. Because the im-
portance of cardiovascular death among pediatric ESRD
patients is well known and documented, it is critical to
address modifiable cardiovascular risk factors for death
such as long-term burden of hypertension, fluid overload,
as well the additive effects on diabetes mellitus and hyper-
lipidemia (19 22). Malignancy is an important cause of
death among patients with transplant function and ac-
counted for 34.8% of mortality among patients with a
functioning transplant. Therefore, assessing and mitigating
the oncogenic potential of modern immunosuppression
will be critical to improve survival among pediatric trans-
plant patients.
There are a number of limitations in our study given its
observational nature. The use of registry and administra-
tive data limited our ability to collect or assess the impor-
tance of various clinical variables that may affect mortality
such as time to development of diabetes and other comor-
bidities. Unfortunately the registry does not contain data
on transplant waiting list status. We were limited by the
small number of patients in certain age categories and
relatively few events, and we acknowledge that analysis of
dialysis and transplant intervals may be underpowered to
detect a small improvement in survival over time. The
determination of the cause of death from registry data is
potentially problematic. Previous studies indicate that
agreement between death certificates and data from dial-
ysis registries is poor, perhaps because kidney failure is
often listed as the cause of death on the former or because
many patients die at home (where cause of death cannot
readily be ascertained) (23,24). Furthermore, we identified
25% of deaths as in-hospital deaths. This percentage could
be an underestimation because hospital records were avail-
able by linkage using personal health numbers for only
74.1% of patients in the cohort (13). We are also unable to
capture deaths not reported to the registry or deaths out of
hospital.
In conclusion, we present comprehensive long-term
mortality data for Canadian pediatric ESRD patients. Sur-
vival has remained static for pediatric ESRD patients over
the period of observation. The survival benefit of pre-
emptive transplantation was not observed in adjusted
models; nevertheless, there may be other advantages of
pre-emptive transplantation in a pediatric patient. Further
evaluation is necessary to elucidate factors that may be
associated with increased risk of death in this population.
Clin J Am Soc Nephrol 6: 1094 1099, May, 2011
Acknowledgments
This study was funded by operating grants received from the
Alberta Childrens Hospital Foundation and Alberta Health Ser-
vices. The authors thank the director and personnel of the Cana-
dian Organ Replacement Register (Dr. John Gill, Lilyanna Trpeski,
Yingbo Na, and Robert Williams) for their assistance in creating
the data set used in this study. This work submitted in abstract
form was accepted for an oral presentation at the Canadian Soci-
ety of Nephrology 2010 annual meeting in Montreal, Canada.
Disclosures
None.
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Received: June 3, 2010 Accepted: January 9, 2011
Published online ahead of print. Publication date available at
www.cjasn.org.
Supplemental information for this article is available online at
http://www.cjasn.org/.