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World J Pediatr, Vol 5 No 2 . May 15, 2009 . www.wjpch.com
122
World Journal of Pediatrics
Original article
Author Afliations: Department of Pediatrics, Children's Hospital, London
Health Science Centre, Schulich School of Medicine & Dentistry, University
of Western Ontario, 800 Commissioners Road East, London, Ontario N6A
7W9, Canada (Ooi CL, Sharma AP, Filler G); Department of Pathology and
Laboratory Medicine, Children's Hospital of Eastern Ontario, 401 Smyth
Road, Ottawa, Canada, K1H 8L1 (Lepage N); Sanquin Diagnostic Services,
Amsterdam, The Netherlands (Nieuwenhuys E)
Corresponding Author: Guido Filler, MD, PhD, FRCPC, Department of
Pediatrics, Children's Hospital, London Health Science Centre, London,
Ontario, Canada, N6A 5W9 (Tel: +1-519-685-8377; Fax: +1-519-685-8551;
Email: guido.ller@lhsc.on.ca)
doi:10.1007/s12519-009-0024-3
©2009, World J Pediatr. All rights reserved.
Background: Recent studies showing an improved
diagnosis of iron deciency (ID) with soluble transferrin
receptor (sTfR) and sTfR-ferritin index did not take
into account the age-dependency of sTfR and ferritin.
Moreover, there is a paucity of data on pediatric
reference intervals for sTfR and sTfR-ferritin index.
Methods: A study cohort of 436 apparently healthy
children was analyzed to establish reference intervals
for ferritin, transferrin, sTfR and sTfR-ferritin index.
To account for age-dependency, standard deviation
scores (Z-scores) for these markers were calculated. The
association between these parameters and C-reactive
protein (CRP) was analyzed.
Results: The Z-scores of ferritin, transferrin and
sTfR had a signicant association with CRP, whereas the
Z-score of sTfR-ferritin did not correlate with CRP. The
reference intervals of these parameters were reported.
Conclusion: Among the different markers of ID, the
Z-scores of sTfR, transferrin and ferritin, but not sTfR-
ferritin index, associate with the inammatory status.
World J Pediatr 2009;5(2):122-126
Key words: C-reactive protein;
ferritin;
reference interval;
soluble transferrin receptor;
soluble transferrin receptor-ferritin index;
transferrin
Introduction
Iron deciency (ID) is the most common nutritional
insufciency in the world.[1] It has been linked with
signicant auditory, visual, cognitive, behavioral,
motor and immune effects in children.[2] Marrow iron
estimation is the current gold standard to assess iron
status; however, its invasiveness limits its clinical
applicability.[2] Traditionally, serum ferritin, iron
and total iron binding capacity are used to diagnose
ID. The National Health and Nutrition Examination
Study III (NHANES III) denes ID based on the
presence of 2 of the following 3 parameters: ferritin
<10 μg/L, transferrin saturation <10% and erythrocyte
protoporphyrin >1.42 μmol/L.[3] Iron deciency anemia
is dened as ID plus hemoglobin <110 g/L.[3] The
presence of a concomitant inammation is recognized
as affecting the performance of these markers in
diagnosing ID.[4,5]
Serum soluble transferrin receptor (sTfR), a
monomer lacking 100 amino acids of the transferrin
receptor, is another relatively new marker to diagnose
ID.[6] A decrease in iron stores upregulates the
transferrin receptor, resulting in an increase in serum
sTfR levels.[4] Since there is an inverse relationship
between sTfR and ferritin in ID, different ratios based
on serum sTfR and ferritin levels have been proposed
to improve the performance over the either marker.[7-9]
Inammation can suppress erythropoiesis and
hamper the sTfR increase despite the presence of
ID.[10] Compared with ferritin and transferrin, sTfR
was found to have a better association with ID in
chronic infection,[11-13] acute infection,[14] and chronic
liver disorders.[15] In spite of a better association,
sTfR did not improve the diagnosis of ID in pregnant
women with HIV[16] or in general populations.[17,18]
Likewise, sTfR did not improve the diagnosis of ID
over full blood count and C-reactive protein (CRP) in
children with a high burden of infectious diseases.[19]
Moreover, serum sTfR has also been reported to have
an age-dependent increase in the childhood period.[16]
Currently available studies do not account for age-
dependency while assessing the relationship between
sTfR and inammation in children. The literature is
scarce on the pediatric reference intervals for sTfR and
Pediatric reference intervals for soluble transferrin
receptor and transferrin receptor-ferritin index
Cara Lianne Ooi, Nathalie Lepage, Ed Nieuwenhuys, Ajay Parkash Sharma, Guido Filler
London, Ontario, Canada
World J Pediatr, Vol 5 No 2 . May 15, 2009 . www.wjpch.com
123
Pediatric reference intervals for sTfR and sTfR-ferritin index
Original article
sTfR-ferritin index.
The objectives of this study were to establish
pediatric reference intervals for sTfR and sTfR-ferritin
index and to assess the relationship of CRP with the
Z-scores of sTfR, ferritin, transferrin and the sTfR-
ferritin index.
Methods
Two-hundred and sixty patients undergoing minor
elective surgeries, including hernia repair (n=33),
circumcision (n=8), hypospadia surgery (n=3),
orchidopexy (n=10), minor otolaryngologic surgery
(n=35), tonsillectomy and/or adenectomy (n=50), minor
ophthalmological operation (n=3), minor orthopedic
intervention (n=41), minor dental surgery (n=20)
and other surgeries (n=57), were identied from the
operative record lists at the Children's Hospital of
Eastern Ontario (CHEO) and approached by a study
nurse at the preoperative anesthesia assessment visit.
Written informed consent for the collection of limited
anthropometric data and blood sampling was obtained
from the parents or from the consenting-minor patients.
This cohort was augmented by 176 samples, stored at
-20°C, collected for a previous study.[20] Age, gender
and the type of surgery were recorded. CHEO's
institutional review board gave full approval for the
study.
sTfR was measured as previously described.[21]
Ferritin, transferrin and CRP were measured by
immunonephelometry using BN ProSpec® and the
corresponding Dade Behring reagents. The sTfR-
ferritin index was calculated as the ratio of sTfR
concentration in μg/mL over the log of ferritin
concentration in μg/L as previously described.[22]
Wherever possible, simple descriptive statistics was
used. Data were tested for normal distribution using the
D'Agostino Pearson omnibus normality test. Normally
distributed parameters were reported as mean ±
standard deviation (SD); otherwise, the median and the
2.5th and 97.5th percentiles were recorded. In order to
account for age-dependency, we calculated Z-scores
for all parameters based on the mean and standard
deviation of each age group. The Pearson's correlation
coefcient was used for normally distributed data;
otherwise, we used the Spearman's rank correlation
coefcient to test for a relationship between parameters.
All statistical analyses were performed using GraphPad
Prism for Windows version 4.01 (GraphPad Software
Inc., San Diego, CA, USA), with the exception of the
percentiles for the central 95% condence interval
for which SPSS for Windows version 14.0 (SPSS Inc.,
Chicago, IL, USA) was used.
Results
Four-hundred and thirty-six children (245 males, 191
females) aged 0.4 months to 18 years were studied. As
no statistical difference was found between genders for
all age groups in all parameters (P>0.05), the data were
pooled within the age categories.
Ferritin levels were high in the rst 6 months, had
a decreasing trend, with a nadir at 18 to 24 months, and
a subsequent gradual return to common adult levels in
adolescence. Transferrin and sTfR values also showed
variation in different age groups.
In most age groups, the data were normally
distributed for sTfR and transferrin, whereas the data
for ferritin were not normally distributed. In order to
report the reference intervals for all parameters, we
recorded the median and central 95% reference interval
as well as the mean ± SD (Table). All these parameters
clearly showed an age-dependency, with the non-
parametric Spearman's rank correlation coefcient of
0.2278 for ferritin, 0.3066 for transferrin and 0.2390 for
sTfR (P<0.0001).
To account for the age-dependency, we calculated
the Z-scores for ferritin, transferrin, sTfR and sTfR-
ferritin index. The slopes of the regression line between
the age and the Z-scores of ferritin, transferrin, sTfR,
and sTfR-ferritin index did not signicantly differ from
zero, indicating that the Z-score calculations introduced
no bias (P values between 0.70 and 0.96).
The level of CRP ranged from undetectable values
to a maximum of 37.06 mg/L. Although all the patients
in this study were asymptomatic and apparently
healthy, 17 (3.9%) of them had an elevated CRP level.
The distribution of elevated level of CRP was relatively
even among the age groups (range, 0.0%-12.8%). The
level of CRP was not normally distributed; therefore,
the relationship between CRP and the other parameters
was analyzed using the non-parametric Spearman's
rank correlation coefcient. Ferritin and transferrin
both correlated signicantly with CRP (Spearman's
rank, r=0.1283 and 0.1230; P<0.0085 and P<0.0116).
Interestingly, there was a signicant correlation
between CRP and sTfR (Spearman's rank, r=0.2390,
P<0.0001, Fig. 1), and also between CRP and sTfR
Z-score (Spearman's rank, r=0.2077, P<0.0001). CRP
did not have a signicant correlation with sTfR-ferritin
index (Spearman's rank, r=0.02790, P=0.5732, Fig. 2)
or with sTfR-ferritin index Z-score (Spearman's rank,
r=-0.01628, P=0.7424).
Discussion
The main objectives of this study were to establish
sTfR and sTfR-ferritin index reference intervals for the
World J Pediatr, Vol 5 No 2 . May 15, 2009 . www.wjpch.com
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World Journal of Pediatrics
Original article
sTfR: soluble transferrin receptor.
Table. Pediatric reference intervals for transferrin, ferritin, soluble
transferrin receptor, and the soluble transferrin receptor-ferritin index
nMedian 2.5th
percentile
97.5th
percentile
Mean ± SD
0.4 to 6 months
Transferrin (g/L) 13 2.38 1.77 6.07 2.93±1.20
Ferritin (μg/L) 13 102.66 3.28 336.34 148.45±106.84
sTfR (mg/L) 13 1.52 1.26 3.17 1.78±0.58
sTfR/log(ferritin) 13 0.74 0.57 4.81 1.25±1.29
6 to 12 months
Transferrin (g/L) 17 2.82 1.04 3.83 2.74±0.65
Ferritin (μg/L) 17 31.61 5.04 56.55 29.31±14.51
sTfR (mg/L) 17 1.66 1.12 2.91 1.75±0.41
sTfR/log(ferritin) 17 1.22 0.81 2.96 1.36±0.57
12 to 18 months
Transferrin (g/L) 16 3.27 2.02 4.31 3.19±0.66
Ferritin (μg/L) 16 13.29 6.48 102.03 30.38±30.05
sTfR (mg/L) 16 1.89 1.37 2.52 1.90±0.39
sTfR/log(ferritin) 16 1.51 0.82 2.70 1.58±0.54
18 months to 2 years
Transferrin (g/L) 21 3.15 2.22 4.06 3.06±0.45
Ferritin (μg/L) 21 17.82 8.89 53.88 22.22±12.69
sTfR (mg/L) 20 1.72 1.33 2.93 1.82±0.39
sTfR/log(ferritin) 20 1.46 0.97 2.34 1.45±0.34
2 to 3 years
Transferrin (g/L) 47 2.73 1.96 4.26 2.83±0.52
Ferritin (μg/L) 47 17.36 2.55 81.29 21.80±15.74
sTfR (mg/L) 46 1.70 0.98 2.91 1.71±0.41
sTfR/log(ferritin) 46 1.32 0.65 5.55 1.61±1.01
3 to 4 years
Transferrin (g/L) 39 2.76 1.76 4.13 2.81±0.56
Ferritin (μg/L) 39 26.26 3.14 192.00 36.94±38.54
sTfR (mg/L) 38 1.57 1.08 2.55 1.63±0.34
sTfR/log(ferritin) 38 1.19 0.67 4.29 1.28±0.64
4 to 6 years
Transferrin (g/L) 76 2.69 2.04 4.78 2.88±0.72
Ferritin (μg/L) 76 23.98 5.26 108.98 31.34±23.48
sTfR (mg/L) 76 1.50 1.10 2.74 1.61±0.42
sTfR/log(ferritin) 76 1.12 0.69 2.34 1.22±0.41
6 to 9 years
Transferrin (g/L) 64 2.55 2.05 4.86 2.70±0.56
Ferritin (μg/L) 58 27.83 3.61 78.90 29.99±16.33
sTfR (mg/L) 64 1.40 0.93 2.63 1.50±0.37
sTfR/log(ferritin) 58 0.99 0.60 5.26 1.18±0.88
9 to 12 years
Transferrin (g/L) 44 2.64 1.86 4.19 2.70±0.51
Ferritin (μg/L) 44 31.29 4.84 242.21 40.20±38.71
sTfR (mg/L) 44 1.42 0.81 2.67 1.46±0.32
sTfR/log(ferritin) 44 0.94 0.35 2.27 1.03±0.35
12 to 18 years
Transferrin (g/L) 86 2.79 2.08 4.00 2.85±0.49
Ferritin (μg/L) 86 29.39 2.76 108.86 36.79±23.78
sTfR (mg/L) 85 1.34 0.91 1.91 1.37±0.24
sTfR/log(ferritin) 85 0.92 0.67 3.05 1.00±0.46
Fig. 2. The relationship between the soluble transferrin ferritin index [sTfR/
log(ferritin)] and C-reactive protein (CRP) in 436 apparently healthy
children. There was no signicant correlation between the two parameters.
sTfR/log(ferritin)
0.1 1 10 100
10
1
0
CRP (mg/L)
Fig. 1. The relationship between soluble transferrin receptor (sTfR)
concentration and C-reactive protein (CRP) in 436 apparently
healthy children. There was a signicant correlation between the two
parameters (Spearman's rank, r=0.2390, P<0.0001).
sTfR (mg/L)
0.1 1 10 100
3.0
2.5
2.0
1.5
1.0
0.0
CRP (mg/L)
new Dade Behring assay and to assess the relationship
of CRP with sTfR, ferritin, transferrin and sTfR-
ferritin index.
There is a paucity of data on pediatric reference
intervals for sTfR and sTfR-ferritin index. We are
unaware of any previous publications on pediatric
reference intervals for sTfR using the Dade Behring
assay. Kratovil et al[23] published age-dependent
reference intervals in 183 children, using the
Quantikine IVD sTfR Immunoassay kit. Their
reference ranges reported were 1.37-2.85 mg/L for 6 to
24 months, 1.05-3.05 mg/L for 2 to 6 years, 1.16-2.72
mg/L for 7 to 12 years, 0.97-2.60 mg/L for 13 to 17
years, and 0.84-2.32 mg/L for ≥18 years.[23] Our data
compared favorably with these reference intervals.
Additionally, we reported the reference ranges under
the age of 6 months, and expanded on other age groups
from a larger study cohort. Malope et al[22] reported
in a study with sTfR measured by enzyme-linked
immunosorbent assay a Log sTfR: ferritin ratio >2.55
for ID and <2.55 for anemia of inammation as the
World J Pediatr, Vol 5 No 2 . May 15, 2009 . www.wjpch.com
125
Pediatric reference intervals for sTfR and sTfR-ferritin index
Original article
cut-off to diagnose ID in children aged 1-6 years. Our
results have a reasonable agreement with their cut-
offs; however, we observed an age-dependency of
sTfR-ferritin index, similar to that of sTfR observed by
Kratovil et al.[23]
The utility of sTfR in diagnosing ID in the presence
of inammation has been debated lately. To evaluate
this issue further, we assessed the relationship of CRP
with sTfR and sTfR-ferritin index in apparently healthy
children. We also measured the traditional markers
of ID, transferrin and ferritin in our study cohort. To
improve on previous studies, we accounted for the age
dependency of these parameters by calculating their
Z-scores.
In our study sample, CRP had a signicant
association with ferritin as well as with transferrin.
Ferritin is a recognized positive acute phase reactant,
whereas inammation decreases transferrin production.
The ferritin peak observed in the rst 6 months was
consistent with previously reported high ferritin at
birth and early infancy.[24]
While assessing the effect of inammation on
sTfR, sTfR showed a positive association with CRP.
This association persisted even after accounting for
the age-dependency of sTfR. As is already known,
ID stimulates an increase in sTfR levels due to
the compensatory increase in erythropoiesis.[6-12]
Conversely, inammation can also decrease sTfR
production, thus lowering its serum level in rheumatoid
arthritis,[25] inammatory bowel disease,[26] and other
inammatory disorders.[27] A similar acute phase
reactant potential of sTf R was also reported in children
with a high load of infection and inammation.[18]
Because there is an opposing effect of ID and
inammation on sTfR production, the relative severity
of ID and inammation can affect the relationship
between sTfR and CRP in a study sample.
To explore this relationship further, we evaluated
the association between CRP and sTfR-ferritin index.
Based on an increase in sTfR level from stimulated
erythropoiesis and a decrease in ferritin levels with
reduced iron stores, an sTfR-ferritin ratio has been
proposed to be a better marker for ID than either sTfR
or ferritin alone.[27] In the presence of inammation,
the acute-phase decrease in sTfR level and an opposite
increase in serum ferritin can affect the diagnostic
accuracy of this ratio. In our study cohort, sTfR-ferritin
index did not have a signicant association with CRP,
even though CRP correlated signicantly with sTfR
and ferritin individually. Possibly this could be due to
the reverse direction of the change in sTfR and ferritin
with inammation. Previous studies have also shown
a better performance of sTfR-ferritin index over either
sTfR or ferritin in diagnosing ID in the presence
of inammation.[22,28] The statistically insignicant
association between sTfR-ferritin index and CRP, even
after calculating the respective Z-scores, was the novel
nding from our study. This observation suggests an
independence of sTfR-ferritin index from inammation
even after accounting for the age-dependency of these
variables.
Our study has a few limitations. Instead of a study
sample from the community at large, we enrolled our
subjects during a hospital visit. The inclusion prior
to an elective minor procedure minimized signicant
confounding from a major comorbidity on our
reference intervals. Otherwise, all included subjects
were clinically asymptomatic and the incidence of
elevated CRP was low (3.9%). Understandably, marrow
iron testing improves the quantication of the iron
status. Considering the primary focus of our study,
the lack of marrow iron quantication should not alter
the relative relationship among the studied ID indices
and CRP. The screening investigations also excluded
any suggestion of hemolysis to affect the sTfR levels.
Considering the selection of apparently healthy
children, our results cannot be extrapolated to the
inammatory states.
In summary, inammation associates signicantly
with sTfR, ferritin and transferrin in healthy children,
even after accounting for the age-dependency of these
variables. sTfR-ferritin index appears to be independent
from inammation. The applicability of our ndings
to the patients with inammatory conditions needs
further validation.
Funding: The study was supported by grants from Dade Behring
GmbH, Marburg, Germany and Dade Behring Inc., Mississauga,
ON, Canada.
Ethical approval: The Institutional Review Board of the
Children's Hospital of Eastern Ontariogave gave full approval for
the study.
Competing interest: None.
Contributors: Lepage N, Niewenhuys E and Filler G designed
and executed the study. Ooi CL and Filler G performed the
analysis and wrote the manuscript and it was critically edited
and revised by the other two co-authors. Sharma AP and Filler G
prepared the nal version.
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Received July 7, 2008
Accepted after revision February 19, 2009