Reference values for respiratory system impedance using impulse oscillometry in healthy preschool children.

Abstract

The normal values for lung resistance and lung capacity of children, as determined by impulse oscillometry (IOS), are different for children of different ethnicities. However, reference values there is no available reference value for Korean preschool children have yet to be determined. The aim of the present study was to determine the normal ranges of IOS parameters in Korean preschool children.
A total of 133 healthy Korean preschool children were selected from 639 children (aged 3 to 6 years) who attended kindergarten in Seongnam, Gyeonggi province, Korea. Healthy children were defined according to the European Respiratory Society (ERS) criteria. All subjects underwent lung function tests using IOS. The relationships between IOS value (respiratory resistance (Rrs) and reactance (Xrs) at 5 and 10 Hz and resonance frequency (RF)) and age, height, and weight were analyzed by simple linear and multiple linear regression analyses.
The IOS success rate was 89.5%, yielding data on 119 children. Linear regression identified height as the best predictor of Rrs and Xrs. Using stepwise multiple linear regressions based on age, height, and weight, we determined regression equations and coefficients of determination (R(2)) for boys (Rrs(5)=1.934-0.009×Height, R(2)=12.1%; Xrs(5)=0.774+0.006×Height-0.002×Age, R(2)=20.2% and for girls (Rrs(5)=2.201-0.012×Height, R(2)=18.2%; Xrs(5)=-0.674+0.004×Height, R(2)=10.5%).
This study provides reference values for IOS measurements of normal Korean preschool children. These provide a basis for the diagnosis and monitoring of preschool children with a variety of respiratory diseases.

Full text

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DOI: 10.3345/kjp.2011.54.2.64
Korean J Pediatr 2011;54(2):64-68
Original article
64
Reference values for respiratory system impedance
using impulse oscillometry in healthy preschool
children

Purpose: The normal values for lung resistance and lung capacity of
children, as determined by impulse oscillometry (IOS), are different for
children of different ethnicities. However, reference values there is no
available reference value for Korean preschool children have yet to be
determined. The aim of the present study was to determine the normal
ranges of IOS parameters in Korean preschool children.
Methods: A total of 133 healthy Korean preschool children were
selected from 639 children (aged 3 to 6 years) who attended
kindergarten in Seongnam, Gyeonggi province, Korea. Healthy
children were defined according to the European Respiratory Society
(ERS) criteria. All subjects underwent lung function tests using IOS.
The relationships between IOS value (respiratory resistance (Rrs) and
reactance (Xrs) at 5 and 10 Hz and resonance frequency (RF)) and age,
height, and weight were analyzed by simple linear and multiple linear
regression analyses.
Results: The IOS success rate was 89.5%, yielding data on 119
children. Linear regression identified height as the best predictor
of Rrs and Xrs. Using stepwise multiple linear regressions based on
age, height, and weight, we determined regression equations and
coefficients of determination (R2) for boys (Rrs5=1.934 –0.009×Height,
R2=12.1%; Xrs5=0.774+0.006×Height–0.002×Age, R2=20.2% and for
girls (Rrs5=2.201–0.012×Height, R2=18.2%; Xrs5=-0.674+0.004×Height,
R2=10.5%).
Conclusion: This study provides reference values for IOS measure-
ments of normal Korean preschool children. These provide a basis for
the diagnosis and monitoring of preschool children with a variety of
respiratory diseases.
Bundang-gu, Seongnam-si, Gyeonggi-do 463-712, Korea
Tel: +82.31-780-6262, Fax: +81.31-780-5239
E-mail: drmesh@gmail.com

Copyright © 2011 by The Korean Pediatric Society
Key words: Impulse oscillation system, Reference values, Airway resis-
tance, Preschool children
Jye Hae Park, M.D.1, Jung Won Yoon, M.D.1,
Youn Ho Shin, M.D.1, Hye Mi Jee, M.D.1,
Young Sun Wee, M.D.1, Sun Jung Chang, M.D.
1, Jung Hwa Sim, R.N.1, Hye Yung Yum, M.D.2,
and Man Yong Han, M.D.1
Department of Pediatrics1, CHA Bundang Medical
Center, CHA University, Seongnam, Gyeonggi-do,
Atopy Clinic2, Seoul Medical Center, Seoul, Korea
Received: 8 September 2010, Revised: 5 November 2010
Accepted: 17 December 2010
Corresponding author: Man Yong Han, M.D.
Department of Pediatrics, CHA Bundang Medical Center,
CHA University School of Medicine, 351 Yatap-dong,
This is an open-access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-
nc/3.0/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

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Korean J Pediatr 2011;54(2):64-68 • DOI: 10.3345/kjp.2011.54.2.64
65
Introduction
Pulmonary function tests (PFTs) are important for the evaluation
of respiratory problems in children. In particular, these tests allow
measurement of respiratory status by monitoring changes in lung
function of children with chronic lung diseases, such as asthma. In
addition, PFTs can be used to help to diagnosis children with chronic
lung diseases1). For the diagnosis and management of respiratory
disease, reference data of healthy children are needed to establish
baseline PFT results2).
Spirometric determination of forced expiratory volume in 1 se-
cond (FEV1) and forced vital capacity (FVC) are widely used to
evaluate airway obstruction, to diagnose and monitor various
respiratory diseases3). However, spirometry is difficult to perform
in young children due to their short attention span and limited
cooperation3-5). Thus, respiratory resistance obtained by the forced
oscillation technique (FOT) is commonly used in young children6,
7). The impulse oscillation system (IOS) is a commercial device
used to measure oscillatory resistance at multiple frequencies3). This
technique requires little patient cooperation because only tidal volume
breaths are required and children as young as 2 years can be readily
examined8). Thus, measurement of pulmonary resistance in preschool
children can be used to diagnose and manage respiratory diseases6, 9).
IOS is widely used by pediatric caregivers for the diagnosis
and management of respiratory and allergic diseases. Like other
pulmonary function values, IOS parameters have different normal
reference levels from different races and age groups2, 10-12). Several
reports have identified normal reference levels in Korean school-aged
children13, 14). However, there are no reports on reference values for
preschool children, thus making it difficult to diagnose and monitor
respiratory diseases in these children using IOS.
The aim of the present study was to determine reference values of
IOS measurements for Korean preschool children so that clinicians
can more readily diagnose and manage respiratory disease in this
group of patients.
Materials and methods
1. Subjects
This was a cross-sectional study of preschool children aged 3-6 yrs.
All subjects were attending one of five kindergartens in Seongnam
from May to July of 2009. Based on guidelines of the American
Thoracic Society (ATS)3) and European Respiratory Society (ERS)15),
subjects with the following characteristics were excluded: (i) personal
or family history of wheezing or asthma; (ii) personal history of
allergic rhinitis or atopic dermatitis; (iii) premature birth, low birth
weight, or history of ventilation or bronchopulmonary dysplasia;
(vi) exposure to passive smoking in the family; (v) obesity (body
mass index >95% of predicted or ≥ 25 kg/m2 16); (vii) recent upper
respiratory tract infection; and (viii) severe respiratory disease with
dyspnea. This study was approved by the ethics committee of CHA
University and written informed consent was obtained from the
parents of all participating children.
2. Health screening questionnaire
We collected patient information through a health screening
questionnaire administered to the parents of all participating
children. The questionnaire was designed to exclude children with
asthma, allergic disorders, or a family history of asthma. Our Korean
questionnaire17) was developed using an international asthma and
allergy questionnaire18). In addition, the survey assessed age, gender,
family smoking history, and any other previous respiratory therapies.
3. Impulse oscillation system
Impulse oscillometry was performed using the Master Screen
Spirometry-IOS Digital System (Jaeger Company, Würtzburg,
Germany). All IOS measurements were performed according to
methods described by the European Respiratory Society (ERS)15)
by one experienced operator. We measured the resistance at 5 Hz
(Rrs5) and 10 Hz (Rrs10), values routinely used to assess pulmonary
resistance, and reactance at 5 Hz (Xrs5) and 10 Hz (Xrs10), values that
reflect pulmonary compliance.
4. Statistical analysis
Data are expressed as means and standard deviations. The sta-
ti cal data was calculated as means of three values. Within-test
repeatability was estimated by the coefficient of repeatability (CR)
and the coefficient of variation (CV)19). The CR was calculated as
2.83×within subject SD (2.83×SD) and CV was calculated as SD/
mean20). Linear regression analysis was used to assess the relationship
between IOS pulmonary function measures and anthropometric
data (height, weight, and age). Data were analyzed separately for boys
and girls, using multiple linear regressions and the ‘stepwise’ method
to identify the best predictors of respiratory resistance parameters.
When the ‘stepwise’ method is available, ‘enter’ method is used for
the best fitting equation. Data were analyzed using SPSS software
(version 17.0, Chicago, IL, USA). The significance level was 0.05 for
all comparisons.

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JH Park, et al. • Reference values using IOS in healthy preschool children
Results
1. Characteristics of children
We initially recruited 639 preschool children. The parents of 630
children (98.6%) were screened using the questionnaire. A total of 497
children were excluded based on our exclusion criteria, and 133 healthy
children, aged 3–6 years, were enrolled. The success rate of IOS was
89.9%, so our analysis ultimately considered data of 119 children.
Table 1 shows the characteristics of enrolled children stratified by
age. A total of 56% of the patients (n=67) were boys, mean age was 4.9
±0.86 years, mean height was 109.1±7.11 cm, and mean weight was
18.7±3.34 kg.
2. Relationships of IOS and anthropometric data
Within-test repeatability of Rrs5 indicated that CR was 0.175 and
CV was 6.1%. Linear regression analysis of IOS measures indicated
that Rrs5 was significantly associated with height, weight, and age.
Log-transformation of the IOS values and height did not improve
this relationship. In addition, height had the greatest correlation with
Table 1. Demographic Characteristics of Enrolled Children
Age
(years)
No. Male (%) Height (cm) Weight (kg)BSA (m
2) BMI (kg/m
2)
3 23 11 (47.8)100.3±4.7 15.6±1.8 0.65±0.0415.5±1.7
4 34 22 (64.7)107.0±4.917.6±2.5 0.72±0.0717.0±2.2
5 48 22 (45.8)112.6±4.819.6±2.1 0.78±0.0518.4±1.7
6 14 12 (85.7)117.1±3.723.3±4.30.87±0.0921.5±3.7
Total 119 67 (56.3) 109.12±7.118.7±3.3 0.75±0.0917.8±2.8
Data are expressed as means±SD
Abbreviations: BSA, body surface area; BMI, body mass index
Table 2. Regression Equations for All Variables versus Height
Coefficient of Height SE of coefficientInterceptSE of interceptR R2SE
Rrs5 (kPa/L/s)
Rrs10 (kPa/L/s)
Xrs5 (kPa/L/s)
Xrs10 (kPa/L/s)
RF (1/s)*
-0.009 0.0021.9340.251 0.3480.121 0.177
-0.007 0.002 1.5160.1930.337 0.114 0.136
0.0040.001 -0.6750.1110.340 0.116 0.079
0.0030.001-0.464 0.0870.3090.0960.617
-0.107 0.06331.100 6.8390.156 0.0244.830
AX (kPa/L) -0.0410.011 6.3681.212 0.3370.113 0.832
Abbreviations: R
resonant frequency; AX, area of the reactance curve less than zero.
*RF is adjusted to use the ‘enter’ method. Except RF, other are used the ‘stepwise’ method.
2, coefficient of determination; Rrs5, resistance at 5 Hz; Rrs10, resistance at 10 Hz; Xrs5, reactance at 5 Hz; Xrs10, reactance at 10 Hz; RF,
Table 3. Impulse Oscillation System Predictive Equations for Boys and Girls
EquationsRR
2
SE of the estimate
Boy
Rrs5 (kPa/L/s)
Rrs10 (kPa/L/s)
Xrs5 (kPa/L/s)
Xrs10 (kPa/L/s)
RF (1/s)*
= 1.934-0.009×H 0.3480.1210.177
= 1.506-0.007×H 0.3350.112 0.136
= -0.774+0.006×H – 0.002×A 0.4500.202 0.062
= -0.464+0.003×H 0.309 0.0960.062
= 31.023-0.109×H-0.196×W+0.066×A 0.191 0.037 4.863
AX (kPa/L) = 6.368-0.041×H0.3370.1130.832
Girl
Rrs5 (kPa/L/s)
Rrs10 (kPa/L/s)
Xrs5 (kPa/L/s)
Xrs10 (kPa/L/s)
RF (1/s)*
= 2.201-0.012×H 0.427 0.1820.181
= 1.666-0.008× H 0.377 0.1420.149
= -0.674+0.004×H 0.3240.105 0.084
= -0.566+0.004×H 0.4280.1830.578
= 29.281-0.081×H-0.490×W+0.134×A0.268 0.0724.774
AX (kPa/L) = 7.116-0.048×H0.397 0.158 0.820
Abbreviations: R2, coefficient of determination; Rrs5, resistance at 5 Hz; Rrs10, resistance at 10 Hz; Xrs5, reactance at 5 Hz; Xrs10, reactance at 10 Hz; RF,
resonant frequency; AX, area of the reactance curve less than zero; H, height (cm); A, age (months); W, weight (kg)
*RF is adjusted to use the ‘enter’ method. Except RF, other are used the ‘stepwise’ method

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Korean J Pediatr 2011;54(2):64-68 • DOI: 10.3345/kjp.2011.54.2.64
67
Rrs5 (r=0.72). Table 2 shows the results of linear regression models for
all IOS variables with height.
3. IOS predictive equations for boys and girls
Table 3 shows the results of multiple linear regression equations
for age, height, and weight. Height was the strongest independent
variable for all IOS values. Rrs was negatively correlated with
height. For boys, Rrs5=(1.934–0.009×height), with a coefficient of
determination (R2) of 12.1%. For girls, Rrs5=(2.201–0.012×height),
with an R2 of 18.2%. Xrs was also positively correlated with height.
For boys, Xrs5=(-0.774+0.006×height–0.002×age), with R2 of 20.2%.
For girls, Xrs5=(-0.674+0.004×height), with R2 of 10.5%. Fig. 1 shows
a significant negative correlation between Rrs5 values and height for
all children.
Discussion
In this study, we determined IOS values for healthy preschool
Korean children, in whom spirometry is difficult to perform.
We obtained valid IOS measurements for 89.9% of the enrolled
children, a higher success rate than reported in previous studies12,
21). This discrepancy may be due to differences in inclusion and
exclusion criteria, differences in IOS techniques, and/or our use of one
experienced operator for all measurements. The European Respiratory
Society (ERS) and the American Thoracic Society (ATS) recommend
the selection of a normal population for reference values of respiration
measurements, with healthy children selected by a questionnaire
that screens for history of asthma and allergies and family history of
allergies. Our results indicate that it is relatively easy to perform IOS in
healthy children less than 6 years of age.
A description of the normal variability of IOS values is required to
define clinically relevant alterations. In this study, we reported within-
test variability as CR and CV. Our reported CR and CV values
were similar to values reported in previous studies9, 22-24). In addition,
our calculations of Rrs, Xrs, Fr, and AX using a regression equation
indicated that height was the only significant predictor, also consistent
with previous studies12, 23). Similar to previous studies, we found that
Rrs was negatively correlated with height and Xrs was positively
correlated with height6, 15, 23, 25). Interestingly, our regression coefficients
of Rrs with height are strikingly similar to those published by Hellinckx
et al.26), Frei et al.6) and Klug et al.24), but different from those published
by Ducharme et al.12) and Malberg et al.23). In particular, our study
indicated lower resistance values than several previous studies. Table
4 shows the comparison of reference equations of Rrs5 between the
present study and previous studies on healthy preschool children. This
difference may be caused by differences in age distribution, and/or racial
differences. A limitation of our study is that the R2 was less than 20%,
which is poorer than that reported in several other previous studies.
This may be due to our small number of studied subjects. Comparing
to previous school-aged children in Korea, Korean school studies13, 14),
our regression equations at multiple frequencies were similar to their
reference values, especially about the Rrs5.
In line with other studies, we confirmed that IOS is an effective
and easily performed noninvasive technique that is well suited for
lung function measurements in young children. Reference values
for IOS are important for the interpretation of pulmonary function
test measures, and are needed for the diagnosis and management
of respiratory diseases1). The measurement of respiratory input
impedance using IOS has significant clinical value in children with a
variety of respiratory disorders27). This study is the first to provide IOS
data for healthy Korean preschool children and can be used as a basis
for the diagnosis and assessment of prognosis of pulmonary function
in children with chronic pulmonary disorders and asthma.
In conclusion, we have determined reference values of IOS mea-
sure ments generated from a group of healthy Korean preschool child-
Rrs5(kPa/L/s)
Height (cm)
Fig. 1. Correlation between height and respiratory resistance at 5 Hz
(Rrs5). The regression equation was Rrs5 (kPa/L/s) = 1.934–0.009 ×
Height (cm); the coefficient of determination was 12.1%.
Table 4. Overview of the Regression Equations of Rrs at 5 Hz in Healthy
Preschool Children
Published normative dataEquations
Lebecque P, et al 19911.361-0.00621*H
Hellinckx J, et al 19982.064-0.009528*H
Stanescu D, et al 1979 2.416-0.0127*H
Ducharme FM, et al 1998 10.990-2.370*(log H)
Present study 1.934-0.009*H
Malberg LP, et al 2002 8.286-1.786*(log H)
Abbreviations: Rrs, respiratory resistance; H, height (cm)

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JH Park, et al. • Reference values using IOS in healthy preschool children
ren. Our IOS reference values are different from those for preschool
children of other ethnic groups, and are essential for the diagnosis
and treatment of various respiratory diseases. We suggest that future
studies be performed with larger populations of Korean preschool
children to confirm our findings.
Acknowledgment
The questionnaire used, the Korean version of ISAAC, was
provided by the Korean Academy of Pediatric Allergy and
Respiratory Diseases.
References
1) Stanojevic S, Stocks J, Hankinson J, Coates A, Pan H, Rosenthal M, et
al. Reference ranges for spirometry across all ages: a new approach. Am J
Respir Crit Care Med 2008;177:253-60.
2) Ip M, Karlberg J, Luk K, Leong J. Lung function reference values in
Chinese children and adolescents in Hong Kong. I. Spirometric values
and comparison with other populations. Am J Respir Crit Care Med
2000;162:424-9.
3) Beydon N, Lombardi E, Allen J, Arets H, Aurora P, Bisgaard H, et al.
An official American Thoracic Society/European Respiratory Society
statement: pulmonary function testing in preschool children. Am J Respir
Crit Care Med 2007;175:1304-45.
4) Eigen H, Bieler H, Grant D, Christoph K, Terrill D, Heilman DK, et
al. Spirometric pulmonary function in healthy preschool children. Am J
Respir Crit Care Med 2001;163:619-23.
5) Kanengiser S, Dozor AJ. Forced expiratory maneuvers in children aged 3
to 5 years. Pediatr Pulmonol 1994;18:144-9.
6) Frei J, Jutla J, Kramer G, Hatzakis GE, Ducharme FM, Davis GM.
Impulse oscillometry: reference values in children 100 to 150 cm in height
and 3 to 10 years of age. Chest 2005;128:1266-73.
7) Schweitzer C, Moreau-Colson C, Marchal F. Respiratory impedance
response to a deep inhalation in asthmatic children with spontaneous
airway obstruction. Eur Respir J 2002;19:1020-5.
8) Bisgaard H, Pedersen S, Anhoj J, Agertoft L, Hedlin G, Gulsvik A, et
al. Determinants of lung function and airway hyperresponsiveness in
asthmatic children. Respir Med 2007;101:1477-82.
9) Bisgaard H. Lung function measurement in awake young children. Eur
Respir J 1995;8:2067-75.
10) Nielsen KG, Bisgaard H. Lung function response to cold air challenge in
asthmatic and healthy children of 2-5 years of age. Am J Respir Crit Care
Med 2000;161:1805-9.
11) Nielsen KG, Bisgaard H. Discriminative capacity of bronchodilator
response measured with three different lung function techniques in
asthmatic and healthy children aged 2 to 5 years. Am J Respir Crit Care
Med 2001;164:554-9.
12) Ducharme FM, Davis GM, Ducharme GR. Pediatric reference values for
respiratory resistance measured by forced oscillation. Chest 1998;113:1322-
8.
13) Wee YS, Jung DW, Park HW, Shin YH, Han MY. Reference values for
respiratory system impedance using impulse oscillometry in school-aged
children in Korea. Korean J Pediatr 2007;50:862-7.
14) Hur HY, Kim HY, Jung DW, Shin YH, Han MY. A comparison between
impulse oscillometry system and spirometry for spirometry for detecting
airway obstruction in children. Korean J Pediatr 2008;51:842-7.
15) Oostveen E, MacLeod D, Lorino H, Farre R, Hantos Z, Desager K, et
al. The forced oscillation technique in clinical practice: methodology,
recommendations and future developments. Eur Respir J 2003;22:1026-
41.
16) Lee SY, Kang YJ, Jang MJ, Kim JH, Moon JS, Lee CG, et al. The
metho dology for developing the 2007 Korean growth charts and blood
pressure nomogram in Korean children and adolescents. Korean J Pediatr
2008;51:26-32.
17) Hong SJ, Lee SY, Kim KE. The prevalences of asthma and allergic diseases
in Korean children. Korean J Pediatr 2008;51:343-50.
18) Asher MI, Keil U, Anderson HR, Beasley R, Crane J, Martinez F, et al.
International Study of Asthma and Allergies in Childhood (ISAAC):
rationale and methods. Eur Respir J 1995;8:483-91.
19) Chinn S. Statistics in respiratory medicine. 2. Repeatability and method
comparison. Thorax 1991;46:454-6.
20) Bland JM, Altman DG. Statistical methods for assessing agreement
between two methods of clinical measurement. Lancet 1986;327:307-10.
21) Ducharme FM, Davis GM. Measurement of respiratory resistance in the
emergency department: feasibility in young children with acute asthma.
Chest 1997;111:1519-25.
22) Ducharme FM, Davis GM. Respiratory resistance in the emergency
department: a reproducible and responsive measure of asthma severity.
Chest 1998;113:1566-72.
23) Malmberg LP, Pelkonen A, Poussa T, Pohianpalo A, Haahtela T,
Turpeinen M. Determinants of respiratory system input impedance and
bronchodilator response in healthy Finnish preschool children. Clin
Physiol Funct Imaging 2002;22:64-71.
24) Klug B. Specifiic airway resistance, interrupter resistance, and respiratory
impedance in healthy children aged 2-7 years. Pediatr Pulmonol 1998;
25:322-31.
25) Dencker M, Malmberg LP, Valind S, Thorsson O, Karlsson MK,
Pelkonen A, et al. Reference values for respiratory system impedance by
using impulse oscillometry in children aged 2-11 years. Clin Physiol Funct
Imaging 2006;26:247-50.
26) Hellinckx J, De Boeck K, Demedts M. Evaluation of impulse oscillation
system: comparison with forced oscillation technique and body plethys-
mography. Eur Respir J 2001;18:564-70.
27) Mauer MP, Cummings KR. Impulse oscillometry and respiratory symp-
toms in World Trade Center responders. Lung 2009;188:107-13.