Nephrol Dial Transplant (2012) 27: 1978–1984
doi: 10.1093/ndt/gfr556
Advance Access publication 3 November 2011
Epidemiology of chronic kidney disease in children in Serbia
Amira Peco-Antić1,2, Radovan Bogdanović1,3, Dušan Paripović2, Aleksandra Paripović3, Nikola Kocev1,
Emilija Golubović4,5 and Biljana Milošević6,7; on behalf of the Serbian Pediatric Registry of Chronic Kidney
Disease (SPRECKID)
1
Faculty of Medicine, University of Belgrade, Belgrade, Serbia, 2Department of Nephrology, University Children’s Hospital, Belgrade,
Serbia, 3Department of Nephrology, Institute of Mother and Child Health care, Belgrade, Serbia, 4Faculty of Medicine, University of
Nis, Nis, Serbia, 5Department of Nephrology, Clinic of Children’s Internal Disease, Clinical Center of Nis, Nis, Serbia, 6Faculty of
Medicine, University of Novi Sad, Novi Sad, Serbia and 7Department of Nephrology, Institute of Children and Youth Health care, Novi
Sad, Serbia
Correspondence and offprint requests to: Amira Peco-Antić; E-mail: [email protected]
Abstract
Background. The epidemiological information from welldefined populations regarding childhood chronic kidney disease (CKD), particularly those concerning non-terminal
stages, are scanty. The epidemiology of CKD in children
is often based on renal replacement therapy (RRT) data,
which means that a considerable number of children in earlier stages of CKD are missed as they will reach end-stage
renal disease (ESRD) in adulthood. Here, we report the basic
epidemiological data on childhood CKD in Serbia, gathered
over the 10-year period of activity of the Serbian Pediatric
Registry of Chronic Kidney Disease.
Methods. Since 2000–09, data on incidence, prevalence,
aetiology, treatment modalities and outcome of children aged
0–18 years, with CKD Stages 2–4 and CKD Stage 5, were
collected by reporting index cases from paediatric centres.
Results. Three hundred and thirty-six children were registered (211 boys, 125 girls, male/female ratio 1.7). The median age at registration was 9.0 years [interquartile range
(IQR) 3–13]. Median follow-up was 4.0 years (IQR, 1–9).
The median glomerular filtration rate (GFR) at the time of the
registration was 39.6 mL/min/1.73m2 (IQR, 13.8–65.4). Median annual incidence of CKD 2–5 stages was 14.3 per million age-related population (p.m.a.r.p.), while those of CKD
2–4 or CKD 5 were 9.1 and 5.7 p.m.a.r.p., respectively. The
median prevalence of CKD 2–5 was 96.1 p.m.a.r.p., 52.8
p.m.a.r.p. in CKD 2–4 and 62.2 p.m.a.r.p. in CKD 5. The
main causes of CKD were congenital anomalies of kidney
and urinary tract and hereditary nephropathies. Kidney
survival was the worst in children with glomerular diseases and in those with advanced CKD. Haemodialysis
was the most common first modality of RRT. Mortality
rate was 4.5%, mainly due to cardiovascular and infectious complications.
Conclusions. Epidemiology of paediatric CKD in Serbia is
similar to that reported from developed European countries.
The knowledge of the epidemiology of earlier stages of CKD
is essential for both institution of renoprotective therapy and
planning of RRT, a fact of paramount importance in countries
with limited resources.
Keywords: end-stage renal disease; epidemiology; non-terminal renal
failure; renal replacement therapy
Introduction
The epidemiological reports on non-terminal stages of paediatric chronic kidney disease (CKD) from well-defined populations are rare [1–5]. The existing epidemiological data on
The Author 2011. Published by Oxford University Press on behalf of ERA-EDTA. All rights reserved.
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Epidemiology of CKD in children in Serbia
1979
CKD in children mainly focus on renal replacement therapy
(RRT) [6–11], which represent only part of the population
suffering from CKD during childhood, as a considerable
number of children with renal impairment will reach endstage renal disease (ESRD) in adulthood. Knowledge of the
epidemiology of earlier stages of CKD is crucial for early
detection, primary prevention and for the assessment of the
impact of renoprotective therapy. Furthermore, a populationbased paediatric CKD registry is necessary for planning of
RRT, which is highly dependent upon economy and availability of health care resources. This aspect is very important
for developing countries with limited financial capacities,
such as Serbia. Therefore, in 2000, the Serbian Pediatric
Nephrology Working Group established the Serbian Pediatric
Registry of Chronic Kidney Disease (SPRECKID). Here, we
report the basic epidemiological data resulting from the first
10 years of SPRECKID activity.
Materials and methods
The index cases were defined using the following criteria: (i) decreased
glomerular filtration rate (GFR) for at least 3 months <90 mL/min/1.73m2
for children >2 years and for younger ones, serum creatinine persistently
above mean 1 2D [12]; (ii) age <19 years at the time of registration and
(iii) written informed consent for data collection, reporting and storage.
All the Serbian centres potentially involved in caring of children and
adolescents with CKD were invited to report index cases. The Unit of
Pediatric Nephrology of University Children’s Hospital in Belgrade acted
as the national coordinating centre that developed the study standards,
processed the data and coordinated with regional principal investigators.
The data collection was structured into the SPRECKID core data set including date of birth, gender, cause of renal disease, referral region, body height
and body weight, serum creatinine, date of RRT initiation, treatment modality,
changes of therapy, death and its cause, and transfer of registry.
The children were reported on a prospective basis, but retrospective
check-up was also performed. New cases were reported using a standardized
registration form containing a predefined list of diagnoses classified into five
groups: congenital anomalies of the kidney and urinary tract (CAKUT),
hereditary renal disorders, glomerular diseases, miscellaneous causes and
CKD of unknown origin. Updating of the data was done every year.
The incidence was calculated as new cases per year, while point prevalence rate included all living patients followed in registry on 31 December of
the current year. Both incidence and prevalence were expressed per million
age-related populations (p.m.a.r.p.). The estimated number of paediatric
population ‘at risk’ (number of children between the age of 0–19 years)
for the morbidity analysis was derived from the 2002 state census according
to which, total population (not including Kosovo) was 7.498 million, while
population <19 years of age was 1.67 million [11].
The staging of CKD registered population was done according to CKD
classification described by the Clinical Practice Guidelines of the National
Kidney Foundation’s Kidney Disease Outcomes Quality Initiative (KDOQI
guidelines) [13]. Thus, registered population were categorized as those that
comprise CKD Stages 2–5; Stages from 2 to 4 were designated as non-terminal
chronic renal failure (CRF), while CKD Stage 5 (ESRD) was defined as either
GFR <15 mL/min/1.73m2 or a need for the initiation of kidney replacement
therapy by dialysis or transplantation. For children <2 years of age, the percentage of loss of kidney function in each stage of the KDOQI guidelines was
extrapolated taking into account the reference values of GFR in children <2
years [13]. The assessment of GFR was performed according to the Schwartz’s
formula [14]. Creatinine was measured by the Jaffe method in all centres.
Descriptive and analytical statistics were done by SPSS 19.0 software.
Data were described as frequencies and percentages for categorical variables
or as medians and interquartile ranges (IQRs) for continuous variables. The
IQR is the difference between the third and first quartiles. Because it uses the
middle 50% of the data, the IQR is not affected by extreme values. Comparisons between parametric variables were done by the t–test, while the
proportions were compared with v2 test. A P-value <0.05 was considered to
be statistically significant. Patients and kidney survival were analysed using
Kaplan–Meier life table method. Risk for progression to ESRD was assessed using multiple Cox proportional hazards regression.
Results
From January 2000 to December 2009, 336 children were
registered (211 boys, 125 girls, male/female ratio 1.7). The
median age at registration was 9.0 years (IQR 3–13). Median
age at the time of the diagnosis of CKD was 5.2 years (IQR,
0.9–11), while the age distribution was as follows: <1 year
25.3%, 1–5 years 25.9%, 6–10 years 22.9%, 11–15 years
21.1% and 4.8% were >15 years. Male gender predominated in all categories for all ages. Females were older than
males at the time of the diagnosis of CKD (7.1 4.9 versus
5.8 5.5; P < 0.05), while the age difference at the time of
registration (8.9 5.0 versus 8.1 5.9) was not statistically
significant. Median follow-up of the patients in registry was
4.0 years (IQR, 1–9); 16.5% of the patients were followed in
registry for 10 years.
The majority of the patients were from Serbia (90.2%),
4.5% were from Bosnia and Herzegovina, 4.2% were from
Montenegro and 1.2% was from Republic of Macedonia.
Renal function and classification of CKD
The median GFR at the time of the registration was 39.6 mL/
min/1.73m2 (IQR, range 13.8–65.4). At the entry into the
study, 104 (31.0%) patients were in CKD Stage 2, 90
(26.8%) in CKD Stage 3, 45 (13.4%) in CKD Stage 4 and
97 (28.9%) were in CKD Stage 5. Thus, overall number of
CKD 2–4 patients at registration was 2.4 times those with CKD
5 patients. The distribution of the patients according to CKD
stage during the whole study period is presented in Table 1.
Incidence and prevalence
The median annual incidence of CKD Stages 2–5 for the 10year period was 14.3 p.m.a.r.p. (IQR, 10.9–20.4). It was
higher during the second (2005–09) than during the first
Table 1. Distribution of the patients’ prevalence according to the CKD stage
Study period
CKD stage,
number of the
patients (%)
2000
2001
2002
2003
2004
2005
2006
2007
2008
2009
CKD 2
CKD 3
CKD 4
CKD 5
Total
22 (21.4)
22 (21.4)
13 (12.6)
46 (44.7)
103
25 (21)
25 (21)
15 (12.6)
54 (45.4)
119
25 (18.9)
18 (21.2)
19 (14.4)
60 (45.5)
132
24 (16.7)
37 (25.7)
19 (13.2)
68 (44.4)
144
22 (14.2)
46 (29.7)
19 (12.3)
68 (43.9)
155
23 (14.1)
43 (26.4)
22 (13.5)
75 (48.5)
163
30 (16.8)
41 (22.9)
29 (16.2)
79 (44.1)
179
44 (25.4)
35 (20.2)
24 (13.9)
70 (40.5)
173
35 (20.2)
48 (27.7)
18 (10.4)
72 (41.6)
173
67 (30.2)
66 (29.7)
16 (7.2)
73 (32.9)
222
1980
A. Peco-Antić et al.
5-year period (2000–04) (18.6 8.7 versus 14.3 6.2, P <
0.01). Median annual prevalence for the 10-year period was
96.1 p.m.a.r.p. (IQR, 77.0–108.9). There was a slight increase
(30.9%) during the 2005–09 period compared to 2000–04
period
(78.2 12.2 versus 113.1 15.3; P < 0.001). The incidence
of CKD 2–4 was 9.1 p.m.a.r.p. (IQR, 7.3–11.9) and its prevalence was 52.8 p.m.a.r.p. (IQR, 42.0–63.8). Incidence of
CKD 5 was 5.7 p.m.a.r.p. (IQR, 4.2–9.4) and its prevalence
was 62.2 p.m.a.r.p. (IQR, 49.0–71.5), respectively.
Aetiology
In general, CAKUT accounted for 58.0% of CKD aetiology,
hereditary renal conditions for 14.6%, glomerular diseases
for 11.9%, other renal diseases for 14.6% and for 1.8%
causes of CKD remained unknown (Table 2). Thus, 72.6%
of all causes of CRF were congenital or hereditary. The
relative percentage of glomerular diseases increased from
7.9% in CRF patients to 21.6% in ESRD patients, while
CAKUT decreased from 63.6% in CRF to 44.3% in ESRD
patients. Males predominated in CAKUT, while females
were the majority among patients with glomerular diseases
(Table 1). Renal disease was diagnosed earlier in patients
with CAKUT and in those with hereditary nephropathies
than in patients with glomerular diseases (Table 2).
Renal replacement therapy
A total of 132 children were followed while on RRT. One
hundred and two patients started RRT during the study
period. The first modality of RRT was haemodialysis
(HD) in 83/102 (81.4%), peritoneal dialysis in 15/102
(14.7%) and transplantation (pre-emptive transplantation)
in 12/102 (11.7%) patients. The median age at the start of
dialysis was 9.8 years (IQR, 6.2–13.8). During the study
period, 81 patients were transplanted. Median age at the first
transplantation was 12.7 years (IQR, 7.8–16.1). The majority (64.2%) of the transplanted children received a graft from
a living-related donor. Median waiting time for transplantation was 15.1 months (IQR, 4.5–40.2).
Outcome for children with CKD
During the study period, 15 (4.5%) patients died, 99
(29.4%) were lost to further follow-up in registry, mainly
due to the transfer to adult centres, while the 222 (66.1%)
remained to further follow-up. Four patients died in preterminal renal failure due to primary disease (2/4 malignant
tumour) or severe co-morbidity (2/4 developmental delay
and malnutrition). Two patients died at the start of HD,
while the remaining nine patients died during chronic HD
treatment; seven of them died due to cardiovascular complications and the other 2/9 patients died due to severe
infection. The majority (60%) of the dialysed patients died
soon after they had been transferred to adult dialysis
centres.
A critical period of age for rapid progression of CRF was
during puberty, leading to almost 75% of the patients to the
ESRD at 18 years (Figure 1a). Kidney survival was the
worst in children with glomerular diseases and in those
with advanced CKD stage (Figure 1b and c). Prognostic
value of age at the time of diagnosis of CRF, CKD stage
and primary disease in progression to ESRD was found by
Cox multiple (Figure 2).
Discussion
CKD is now recognized as a growing health problem due to
the rapidly increasing trend of its prevalence [15–20].
There is not enough reliable data on the epidemiology of
the earlier stages of CKD. According to the report of the
Third National Health and Nutrition Examination Survey
(NHANES III), the prevalence of adult patients with early
stages of CKD (CKD 1–4; 10.8%) is ~50 times greater than
the prevalence of the terminal stage (CKD 5; 0.2%) [19].
There is no comparable data for children. Our results
showed that prevalence of CKD Stages 2–4 is 2.4 times
greater than the prevalence of CKD Stage 5. The actual
proportion could be higher than the value we found as
CKD is often asymptomatic in its early stages and therefore
is under-diagnosed and under-reported. Furthermore, it is
certain that our data underestimated the true morbidity from
CRF in adolescents, as some of these patients might be
cared and followed up by adult nephrologists. On the other
hand, the prevalence rate for ESRD patients in this study
may be partially overestimated related to the addition of
data from patients aged 20–24 years to the prevalent group
due to their longer follow-up in paediatric centres and delayed transfer to the adults centres. Turkish and Belgian
authors reported even lower CKD 2–4/CKD 5 patients’
ratio (2.06 and 1.71, respectively) [4, 5]. Nevertheless,
Table 2. Primary renal disease by stage, gender and agea
CKD 2–4
ESRD
Primary renal
diseases
Number
%
Male/female
Median age
(IQR), years
CAKUT
HN
GN
Miscellaneous causes
Unknown
Total
152
32
19
32
4
239
63.6
13.4
7.9
13.4
1.7
100
2.8
1.6
0.7
1.1
0.3
3.0 (0.5–8.9)
5.5 (0.5–8.9)
12 (8.5–13.4)
6.1 (2.0–11.7)
12.3 (7.1–15.5)
a
HN, hereditary nephropathies; GN, glomerular diseases.
Number
%
Male/female
Median age
(IQR) years
43
17
21
14
2
97
44.3
17.5
21.6
14.4
2.1
100
2.7
1.1
0.5
0.7
0/2
8 (0.9–11.0)
5.0 (3.5–9.7)
10.0 (6.0–13.7)
1.9 (0.6–5.0)
4.7 (3.5–4.7)
Per cent of
total
(n ¼ 336)
58.00
14.6
11.9
13.6
1.8
100
Epidemiology of CKD in children in Serbia
1981
Fig. 1. (a) Estimated kidney survival in patients with CKD by age. (b) Kidney survival according to primary disease. (c) Kidney survival according to
CKD stage.
the comparison of epidemiology of CRF in children is
rather difficult due to the methodological differences in
case definitions. With median annual incidence of 14.3
p.m.a.r.p. and point prevalence of 96.1.p.m.a.r.p., our data
are comparable to those reported from other European countries, such as France [21], Italy [1], Belgium [5] and Turkey
[4] (Table 3).
Unlike CRF (non-terminal CKD), ESRD is better defined and recognized. According to data from the literature,
paediatric ESRD constitute only a few per cent of the total
ESRD patient population [7, 19, 20]. In Serbia, adjusted
incidence and prevalence rates of ESRD in adults in 2008
were 179.9 and 599.06 per million of total population
(p.m.t.p.), respectively [23], while in the same period, corresponding numbers for children were 2.03 and 9.7
p.m.t.p., respectively. Thus, paediatric ESRD constituted
1.6% of the total ESRD patients in Serbia. Compared to
the data from other paediatric studies [5–11, 22], with
ESRD incidence of median 5.7 p.m.a.r.p. (IQR, 4.2–9.4),
Serbia belongs to the same category as the Netherlands (5.8
p.m.a.r.p.) [10], Belgium (6.2 p.m.a.r.p.) [5] and France
(7.5 p.m.a.r.p.) [22]. The highest incidence rates of ESRD
for children were reported from the USA, New Zealand and
Austria, at 14.8, 13.6 and 12.4 per million populations,
respectively [6], while the lowest (4 p.m.a.r.p.) was found
in Japan [11]. Median prevalence of CKD 5 of 62.2
1982
A. Peco-Antić et al.
p.m.a.r.p. (IQR, 49.0–71.5) in our study is comparable to
data from the majority of European countries as reported by
the Annual Data Report from the United States Renal Data
System for the 0–19 age group in 2003 [6], but higher than
the overall point prevalence (33.6 p.m.a.r.p.) for age groups
0–14 in 2007, as recently reported by the European Registry for Paediatric Nephrology/European Renal AssociationEuropean Dialysis and Transplant Association [7].
The predominance of male patients (m/f ¼ 1.7) in our
study is in accordance with data from other paediatric CRF
registries worldwide [1–5, 20, 21, 22, 24–28]. This age
distribution may be explained by the influence of the main
causes of CKD in children, such as CAKUT and hereditary
renal disorders, which are more prevalent in boys than in
girls (Table 2). These disorders were recognized earlier
than glomerular ones whose frequency increased with increasing age and CKD stage, reaching the second rank of
Fig. 2. The effect of age, gender, stage of CKD and causes of CKD on kidney
survival analysed by Cox proportional hazards regression. G, glomerular
disease; H, hereditary nephropathy; C, CAKUT; M, miscellaneous causes
age at CKD, age at diagnosis of CKD (in years).
ESRD causes (Table 2). Similar findings were also reported
by other authors from developed parts of the world [20]. In
our study, only 1.8% of the patients’ primary renal disease
remained unknown. While paediatric registries have reduced the number of children with ‘no diagnosis’ from
39% in 1976 [29] to fewer than 5% in the recent years
[1], the adult registries still report corresponding rates
of 20–27% that may be attributed to under-diagnosed
CAKUT in adults [30].
RRT for children with ESRD in Serbia has been carried
out in one specialized paediatric centre (at University
Children’s Hospital in Belgrade) since 1980; RRT consisted of chronic HD in the beginning, but, from 1986,
encompassed kidney transplantation and chronic peritoneal
dialysis [31]. In general, HD was the first modality of RRT
in the majority of patients. Although HD is still the favoured mode of dialysis in incident ESRD patients, transplantation has been the most common form of RRT in
prevalent patients since 2005. Cadaveric kidney transplantation in children in Serbia started only in 2004, and the
majority of kidney transplantations are still carried out from
live related donors. The rate of pre-emptive transplantation
has been low (11.7%) but the median waiting time was <2
years (15.1 months).
Like other authors [1], we found that progression of CRF
is increased during puberty. It seems dependent on baseline
GFR or aetiology as the faster progression was documented
in CKD 4 than in CKD 2–3 patients as well as in those with
glomerulopathies than in those with CAKUT.
The mortality rate of 4.5% in our patients was similar to
that reported by other authors [5]; 26.7% of patients died
in pre-terminal renal failure due to primary disease or
severe coexisting morbidities, whereas remaining patients
died while on HD due to cardiovascular and infectious
complications. Data from literature show that cardiovascular and infectious complications are the main cause of
increased mortality in ESRD paediatric patients, which is
still 30–150 times higher than among children without
ESRD [32–34].
Limitations of this study are related to potential underand incomplete reporting. Registry data was submitted on a
voluntary basis so potential for under-reporting exists. Furthermore, information was collected mainly from paediatric
centres, and therefore, information on individuals aged
Table 3. Epidemiology of CRF in Serbia compared with other countriesa
Primary renal
disease (%)
Country
(reference)
Period
Number of Age
Gender Definition of
patients
(years) M/F
CRF
France [21]
Sweden [22]
Italy [1]
Belgium [5]
Turkey [4]
Spain [3]
Serbia
1975–90
1986–94
1990–2000
2001–05
2005
2007–08
2000–09
127
118
1197
143
282
605
336
a
0–16
0.5–16
0–20
0–20
0–19
0–18
0–19
1.35
1.6
2.03
1.3
1.3
1.9
1.7
sCr >175 lmol/L
CCr <30 mL/min/1.73m2
CCr <75 mL/min/1.73m2
CCr <60 mL/min/1.73m2
CCr 75 mL/min/1.73m2
CCr <90 mL/min/1.73m2
CCr <90 mL/min/1.73m2
Incidence
(p.m.a.r.p.)b
Prevalence
(p.m.a.r.p.)c
10.5
7.7
12.1
11.9
10.9
8.66
14.3 (10.9–20.4)
29.0
21
74.7
CAKUT HN GN Other
53.5
34
57.6
59
57.7
71.06
59
96.1 (77.0–109.9) 58
16.5
35
15.5
19
17.2
11
14.6
22.5
14.5
6.8
13
16
3
11.9
sCr, serum creatinine; CCr, creatinine clearance; CRF, pre-terminal chronic renal failure; HN, hereditary nephropathy; GN, glomerulopathies.
Mean or median (as reported) cases per million age-related population.
c
Point prevalence for the end of the investigation.
b
7.5
16.5
20.1
9
9.1
27
15.2
Epidemiology of CKD in children in Serbia
15–17 years could be incomplete. Despite these limitations,
this research database resulted in a rich and useful data
source on non-terminal CKD in children in Serbia, which
are still lacking.
Conclusion
SPRECKID provided valuable information concerning the
epidemiology of mild to severe CKD in children in Serbia
during the period 2000–09. Incidence, prevalence and aetiology of paediatric CKD in Serbia are similar to those
reported from developed European countries. In contrast
to RRT from these countries, HD was a preferred mode
of RRT for children in Serbia, while pre-emptive transplantation and chronic peritoneal dialysis are still underused.
Mortality rate was in acceptable range (4.5%), mainly due
to cardiovascular and infectious complications.
Acknowledgements. The study was supported by the Ministry of Science
and Environmental Protection, Government of Serbia, 175079.
We thank Jelena Bubalo, Mirjana Kostić, Maja Kovačević, Divna
Kruščić, Gordana Miloševski-Lomić, Predrag Miljković, Bilsana Mulić,
Marko Petrović, Jovana Putnik, Snežana Radisavljević, Brankica Spasojević, Nataša Stajić, Vesna Stojanović, Milesa Dapić for their help in
making SPRECKID.
A.P.-A. took part in conception, design, analysis and interpretation of
data, drafting of the article, provided intellectual content and gave final
approval of the enclosed version to be published. R.B. took part in conception, design, analysis and interpretation of data, revising of the article,
provided intellectual content and gave final approval of the enclosed version to be published. D.P. took part in analysis and interpretation of data,
revising of the article, provided intellectual content and gave final approval
of the enclosed version to be published. A.P. took part in analysis and
interpretation of data, revising of the article, provided intellectual content
and gave final approval of the enclosed version to be published. N.K. took
part in analysis and interpretation of data, revising of the article, provided
intellectual content and gave final approval of the enclosed version to be
published. E.G. took part in analysis and interpretation of data, revising of
the article, provided intellectual content and gave final approval of the
enclosed version to be published. B.M. took part in analysis and interpretation of data, revising of the article, provided intellectual content and gave
final approval of the enclosed version to be published.
Conflict of interest statement. None declared.
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Received for publication: 19.4.11; Accepted in revised form: 19.8.11