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ORIGINAL ARTICLE AIRWAY DISEASES
Asthma control assessment in a pediatric population:
comparison between GINA/NAEPP guidelines, Childhood
Asthma Control Test (C-ACT), and physician’s rating
A. Deschildre
1
, I. Pin
2
, K. El Abd
1, 3
, S. Belmin-Larrar
4
, S. El Mourad
1
, C. Thumerelle
1
,
P. Le Roux
5
, C. Langlois
6
& J. de Blic
4
1
Unit!
e de pneumologie-allergologie p!
ediatrique, p^
ole enfant, clinique de p!
ediatrie Jeanne de Flandre, CHRU de Lille, Universit!
e Nord de
France, Lille;
2
P!
ediatrie, P^
ole Couple Enfants, CHU de Grenoble, INSERM U823, Institut Albert Bonniot, Universit!
e Joseph Fourier,
Grenoble, France;
3
P!
ediatrie, CHC Esp!
erance –Montegn!
ee, Li"
ege, Belgium;
4
Service de pneumologie et allergologie p!
ediatriques, AP-HP,
H^
opital Necker Enfants Malades Paris;
5
P!
ediatrie, groupe hospitalier du Havre, Le Havre;
6
D!
epartement de biostatistiques, CHRU de Lille,
Universit!
e Nord de France, Lille, France
To cite this article: Deschildre A, Pin I, El Abd K, Belmin-Larrar S, El Mourad S, Thumerelle C, Le Roux P, Langlois C, de Blic J. Asthma control assessment in
a pediatric population: comparison between GINA/NAEPP guidelines, Childhood Asthma Control Test (C-ACT), and physician’s rating. Allergy 2014; 69: 784–790.
Keywords
asthma; C-ACT; child; exacerbation; guide-
lines.
Correspondence
Antoine Deschildre, Unit!
e de pneumologie-
allergologie p!
ediatrique, p^
ole enfant, clinique
de p!
ediatrie Jeanne de Flandre, CHRU de
Lille, Universit!
e Nord de France, Lille,
France.
Tel.: +33 (0)320445072
Fax: +33 (0)320444107
E-mail: antoine.deschildre@chru-lille.fr
Accepted for publication 24 February 2014
DOI:10.1111/all.12402
Edited by: Marek Sanak
Abstract
Background: Guidelines recommend regular assessment of asthma control. The
Childhood Asthma Control Test (C-ACT) is a clinically validated tool.
Aim: To evaluate asthma control according to GINA2006, NAEPP, pediatrician’s
assessment (PA), and C-ACT in asthmatic children visiting their ambulatory pedi-
atrician or tertiary care pediatric pulmonologist.
Methods: Demographic data, treatment, and number of severe exacerbations dur-
ing the previous year were collected. Control was assessed using (i) strict GINA
2006 criteria, (ii) GINA without taking into account the exacerbation item, (iii)
NAEPP criteria, and (iv) PA. Children and parents filled out the C-ACT.
Results: Five hundred and twenty-five children completed the survey (mean age:
7.7 years; 28% ≤6 years). 78% had a controller treatment. 58% reported ≥1
severe exacerbation. C-ACT was ≤19 in 29.5%. Control was not achieved in
76.5%, 55%, 40%, and 34% according to GINA 2006 guidelines, NAEPP guide-
lines, GINA 2006 without exacerbation criteria, and PA, respectively. C-ACT
was significantly lower in children ≤6 years old (P=0.002) or with severe exac-
erbations (P<0.0001). According to PA, 89% of patients with a C-ACT >21
were controlled and 85% of patients with a C-ACT <17 not controlled.
Conclusion: We observed discrepancies between the different tools applied to assess
asthma control in children, and the impact of age and exacerbations. Cutoff point
of 19 of C-ACT was not associated with the best performance compared to PA.
Assessment of control should take into account symptoms and lung function as
suggested by the latest GINA guidelines as well as exacerbation over a long period.
The goal of asthma treatment is to achieve and maintain
control (1–3). For Global Initiative for Asthma (GINA)
guidelines, controlled asthma was defined by minimal diurnal
symptoms and need for b2 agonists (≤2 week), absence of
nocturnal symptoms, no limitation of activities, and normal
forced expiratory volume in 1 s (FEV1) or peak expiratory
flow (PEF). In 2006, the definition included the absence of
exacerbation over the past year (1). National Asthma Educa-
tion and Prevention Program (NAEPP) guidelines (2007)
tolerated the occurrence of one exacerbation (2). Various
studies reported that control is not achieved in a large num-
ber of children and that exacerbations requiring unscheduled
physician’s visits, emergency treatment, or hospitalization
remained frequent (4, 5).
Asthma control score instruments have been developed
and validated for adults and also for children (6–9). The
Childhood Asthma Control Test (C-ACT) is designed for
children aged 4–11 years (7). Liu et al. have established that
Allergy 69 (2014) 784–790 ©2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd784
a score ≤19 indicates lack of control over the last 4 weeks
(7). However, higher cut points have been reported (10–12).
C-ACT does not take into account exacerbations.
The present study was performed to assess control according
to guidelines (GINA, NAEPP), C-ACT, and physician’s evalu-
ation in asthmatic children aged 4–11 years, followed up by
pediatric pulmonologists in tertiary centers or by ambulatory
pediatricians. We hypothesized that there are differences
according to the methods of assessment of control and that
taking into account exacerbation strengthens these differences.
Part of the results was presented as an abstract form in the
meeting of the American Thoracic Society, New Orleans, 2010.
Patients and methods
Study population
This was a prospective study including two populations of
asthmatic children aged 4–11 years, conducted between
October 2007 and April 2009, one recruited in four tertiary
pediatric pulmonology centers (Necker Enfants Malades hos-
pital, Paris; Lille and Grenoble University Hospital, Le Havre
hospital) and the other one recruited by general pediatricians
in the city of Lille and its region. Diagnosis of asthma was
made according to the French guidelines, with the same crite-
ria by general pediatricians and hospital centers. General pedi-
atricians were all participants of a structured network and
have participated to an educational program in asthma diag-
nosis, management, and treatment. They were consequently
trained in asthma diagnosis and management. This study was
approved by the Committee for Evaluation of Research
Protocols of the Soci!
et!
e de Pneumologie de Langue Franc
!aise.
Study protocol
Patients were included during a single visit. Children with a
chronic illness other than asthma were excluded. The pediatri-
cian conducting the visit filled a form containing historical
data, controller therapy –none, inhaled corticosteroids (ICS),
ICS and long-acting bronchodilators (LABA), leukotriene
receptor antagonist and immunotherapy, and the number of
severe exacerbations defined by systemic corticosteroid use,
emergency visits or hospitalization over the past 12 months.
Pulmonary function tests (PFTs) were performed for all
patients followed up in hospital. In children ≥7 years old,
forced vital capacity (FVC), FEV
1
, and FEV
1
/FVC were
measured and airway obstruction was defined by FEV
1
/
FVC <0.8 (1–3, 13). In children <7 years old, respiratory
resistances were measured by interrupter technique and air-
way obstruction was defined by resistances >150% of predic-
tive values (PV) (3, 14–16).
All children and their parents filled in a C-ACT question-
naire.
Asthma control assessment
Asthma control was assessed by the pediatrician, blinded to
the C-ACT score:
1According to the GINA 2006: diurnal and nocturnal
symptoms, short-acting b2-agonists use, and activity limi-
tation (past month), lung function if available, and any
exacerbations (past year) (GINA strict).
2According to the NAEPP: diurnal and nocturnal symp-
toms, short-acting b2-agonists use, and activity limitation
(past month), lung function if available, and exacerba-
tions (past year). The definition of well-controlled asthma
tolerated the occurrence of one exacerbation requiring
oral systemic corticosteroids during the past year.
3According to the GINA 2006 criteria but without the crite-
rion ‘exacerbation’ over the past 12 months (GINA symp-
toms).
A table listing all the criteria of control according to
GINA and NAEPP guidelines has been inserted on the
form. The assessment was made by the pediatrician during
the visit. Two physicians (KEA and SBL) reviewed all the
forms and validated the level of control.
4Finally, the pediatricians rated asthma as totally con-
trolled, well controlled, partially controlled, and uncon-
trolled (physician’s assessment). They were instructed to
base their ratings on how well the goals of asthma were
being met, as determined on the basis of information
from the patient history, physical examination, and lung
function test if available (3).
For the analysis, patients were divided into two groups,
either controlled (totally or well controlled) or not controlled
(partially controlled or uncontrolled)
C-ACT measurement
All children and their parents filled in a C-ACT question-
naire. We used the French version, translated by the MAPI-
research institute in Lyon, France. The physician did not see
or influence the responses. The C-ACT is divided into two
parts: four questions for the child on perception of asthma
control, limitation of activities, coughing and awakenings at
night (four response options), and three questions for the
caregiver over the past 4 weeks: daytime complaints, daytime
wheezing, and awakenings at night (six response options) (7).
C-ACT scores range from 0 to 27.
Statistical analysis
Continuous variables were described with mean and standard
deviation. Qualitative variables were analyzed as frequencies
and percentages.
To compare the two populations of asthmatic children
(tertiary hospitals and general pediatricians) and to compare
controlled to not controlled children, chi-square tests or Fish-
er’s exact tests were used for qualitative variables and the
Mann–Whitney test for continuous variables because the
distribution of the variables was not normal according to
Shapiro–Wilk test. The Spearman’s coefficient was used to
test the correlation between two continuous variables. The
coefficient of kappa was used to analyze concordance
between control assessed according to GINA, NAEPP, and
physician’s rating. Analyses by ROC curve were performed
Allergy 69 (2014) 784–790 ©2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd 785
Deschildre et al. Asthma control assessment in children
to determine a cutoff point that maximized the sensitivity
and specificity according to the different tools of assessment.
Accuracy was measured by the area under the ROC curve
(AUC). Decision trees were performed using the software
SIPINA to identify ACT cutoff points that best allowed classi-
fying controlled and not controlled children (SIPINA software;
Research Unit ERIC, Lyon 2 University, France). Statistical
analyses were performed by SAS 9.2 software (SAS Institute
Inc., Cary, NC). Graphs were made with Excel. A Pvalue
<0.05 was considered statistically significant.
Results
Five hundred and twenty-five children completed the study, of
whom 353 (67%) recruited in tertiary centers (Table 1). The
mean age was 7.7 years (SD, 2.2) and 145 (28%)
were ≤6 years. Children recruited at the hospital were more
frequently new patients (24.5% vs 9%, P<0.0001) and older
[7.9 years (SD, 2.23) vs 7.2 years (SD, 2.1), P: 0.002]. They had
used less frequently a controller therapy (75% vs 83.5%, P:
0.028) over the past year. At least one severe exacerbation in
the past year was reported by 64% of the children with hospi-
tal follow-up vs 46% for those with general pediatrician’s fol-
low-up (P<0.0001). The rate of exacerbations over the past
year was also higher in children with hospital follow-up [2.2
(SD, 3.2) vs 1.1 (SD, 1.83), P<0.0001]. Forty-two per cent of
the children had no exacerbation during the past year, while
21% had one and 26% at least three. For the 343 patients who
underwent PFTs, there was no airway obstruction in 242
(70.5%). For children aged ≥7 years (n=226), the mean
FEV
1
/FVC was 0.84 (SD, 0.09) and less than 0.8 in 73 (32%).
Evaluation of asthma control according to guidelines and
physician’s assessment
Both populations were grouped for control analysis. Control
was not achieved in 76.5%, 55%, 40%, and 34% of
children according to GINA strict criteria, NAEPP criteria,
GINA symptoms criteria, and physician’s assessment,
respectively. The concordance was poor between GINA
strict and GINA symptoms (j=0.34) and weak between
GINA strict and NAEPP (j=0.54). Among children who
performed PFTs, asthma was more often not controlled
according to GINA symptoms in children with abnormal
PFTs (51/101, 50.5%), than in those with normal PFTs (85/
242, 35%) (P=0.008), also according to the other tools
(GINA strict: P<0.0001, NAEPP: P=0.009 and physi-
cian’s assessment: P=0.0001).
C-ACT Score
The mean of C-ACT score was 21.1 (SD, 4.3) (Fig. 1). The
C-ACT score was ≤19 in 155 children (29.5%) and lower in
children with hospital follow-up [20.6 (SD, 4.6) vs 22.0 (SD,
3.6), P=0.0023]. A positive correlation was observed
between age and C-ACT score (r=0.093; P=0.033), and
the mean C-ACT score was significantly lower in children
aged ≤6 years [20.2 (SD, 4.4)], vs the older [21.5 (SD, 4.3)]
(P=0.002). C-ACT score was also significantly lower in case
of severe exacerbation during past year [20.2 (SD, 4.6) in
case of ≥1 exacerbation and 22.3 (SD, 3.6) in the absence of
exacerbation (P<0.0001)].
We did not find significant differences in the C-ACT scores
according to the treatment. The average C-ACT score was
21.1 (SD, 4.2) in patients without controller treatment
(P=0.80 vs the other children), 21.1 (SD, 4.4) for patients
treated with ICS (P=0.91) and 21.2 (SD, 4.2) for patients
treated with ICS-LABA (P=0.88).
ACT score and guidelines or physician assessment of control
C-ACT scores according to the different modalities are
described in Table 2. Whatever the criteria, C-ACT scores
were significantly higher in children with controlled asthma
(P<0.0001). To detect patients who were not controlled, a
cutoff point of ACT ≤19 was associated with a sensitivity of
36.5% and a specificity of 92.5% according to GINA strict
(AUC =0.727), 48% and 94% according to NAEPP
(AUC =0.801), 58% and 89.5% according to GINA symp-
toms (AUC =0.838), and 62% and 88% according to the
physician’s assessment (AUC =0.840), respectively.
The optimal cut point for not controlled asthma was ≤21
according to GINA symptoms (sensitivity: 76%, specificity:
81.5%), NAEPP (sensitivity: 81%, specificity: 70%), and
physician’s assessment (sensitivity: 71.5%, specificity: 83%).
This cutoff point was ≤22 according to the strict GINA
(sensitivity: 71.5%, specificity: 64.5%).
Finally, we analyzed the accuracy of the C-ACT score to
correctly classify asthma control (Fig. 2). According to the
GINA symptoms, 94% of patients with a C-ACT <14 were
considered to be not controlled, while 86% of patients with
C-ACT >21 were considered to be controlled. According to
the physician’s assessment, 85% of patients with a
C-ACT <17 were considered not controlled, while 89% of
patients with a C-ACT >21 were found to be controlled.
Table 1 Clinical characteristics of patients
Characteristics N=525
Age, years [mean (SD)] 7.7 (2.2)
Boys, n(%) 348 (66)
New patient n(%) 96 (19)
Controller therapy n(%)
No treatment 116 (22)
ICS only 132 (25.5)
ICS +LABA 226 (43.5)
LTA 36 (7)
Immunotherapy 26 (5)
Severe exacerbation’s rate [mean (SD)]
Past month 0.2 (0.6)
Past 3 months 0.7 (1.2)
Past 12 months 1.8 (2.9)
C-ACT [mean (SD)] 21.1 (4.3)
ICS: inhaled corticosteroids, LABA: long-acting beta 2 agonists,
LTA: leukotriene antagonists, C-ACT: Childhood Asthma Control
Test.
Allergy 69 (2014) 784–790 ©2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd786
Asthma control assessment in children Deschildre et al.
Discussion
This study focuses on the assessment of control using differ-
ent tools in a large population of asthmatic children and con-
firms the discrepancies between GINA, NAEPP, physician’s
assessment, and C-ACT score. Young age and exacerbations
were associated with the lack of control. We also observed
that the reference cutoff of 19 for the C-ACT was not associ-
ated with the best performances. However, C-ACT is a good
tool to assess asthma control in clinical practice, especially
for general practitioner.
Population
The population consisted of children attending tertiary cen-
ters but also general pediatric clinics but the criteria of diag-
nosis and management of asthma were homogeneous among
physicians. The population is characterized by the young age
(28% ≤6 years). Most children took a controller therapy
(ICS and LABA in 43%), representing a population with
more severe asthma compared to the general asthmatic popu-
lation, which can be explained by the hospital recruitment.
The level of control was low and similar to the result of the
French study ELIOS performed mainly in general practice
(controlled asthma in only 26% of 3483 children aged
4–15 years) (4).
Exacerbations
Exacerbations were frequent and patients with exacerbations
in the past year failed to achieve the same level of control
compared to children with no recent exacerbation. By tolerat-
ing one exacerbation per year as proposed by NAEPP guide-
lines, 45% of the patients reached good control (2). By
separating exacerbation criteria from the others (symptoms,
activity limitation, b2 short-acting agonists use, and lung
function), as suggested by recent GINA guidelines, 60% of
children were rated as controlled. Severe exacerbations do
not concern all children, as illustrated in the CAMP study
(30% of patients without any exacerbation) but they are one
of the main characteristics of severe asthma (17–20). A past
history of exacerbation is a major risk factor for recurrence,
as reported by Covar et al. in the PACT study and Wu et al.
in the CAMP study (21, 22).
0%
1%
2%
3%
4%
5%
6%
7%
8%
9%
10%
11%
12%
13%
789101112131415161718192021222324252627
Score ACT
Figure 1 Distribution of C-ACT scores.
Table 2 Control levels according to the different modalities of
assessment
n(%)
ACT
[mean (SD)] Pvalue
GINA strict
Controlled* 123 (23.5) 23.5 (2.7) P<0.0001
Not controlled†401 (76.5) 20.3 (4.5)
GINA symptoms
Controlled* 314 (60) 23.1 (3.08) P<0.0001
Not controlled†211 (40) 18.1 (4.27)
NAEPP
Controlled* 234 (45) 23.5 (2.6) P<0.0001
Not controlled†287 (55) 19.1 (4.5)
Physician’s assessment
Controlled* 336 (66) 22.9 (3.03) P<0.0001
Not controlled†171 (34) 17.8 (4.31)
*Controlled: totally or well controlled.
†Not controlled: partially controlled or uncontrolled.
Allergy 69 (2014) 784–790 ©2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd 787
Deschildre et al. Asthma control assessment in children
C-ACT Score
The C-ACT cutoff point of 19 proposed by Liu et al. to iden-
tify inadequately controlled asthma was not the best determi-
nant in our study (7). Initially, it was calculated in a
population of 343 children followed up in a tertiary center
(specificity: 83%, sensitivity: 71.5%, compared to physician’s
assessment) (7). This cut point has been discussed by several
studies conducted in different countries and languages (10–
12). Therefore, translation or parents’/children’s perception is
probably not involved. Indeed, translations of the C-ACT
score have been formally validated and the symptoms which
are described in the C-ACT score are universal. In a popula-
tion of 113 Chinese children, among whom 35% were con-
trolled according to GINA criteria, Leung et al. defined a
cutoff ≤24, compared to the GINA (sensitivity: 66%; speci-
ficity: 63%) (10). Koolen et al. evaluated asthma control in
173 Dutch children (84 aged 4–11 years) (11). Only 17% of
them were controlled according to GINA criteria. The
C-ACT cutoff point of 19 obtained a sensitivity of 33% and a
specificity of 100%, compared to the GINA, and the cut-off
point of 22 achieved the best performance (sensitivity: 82%,
specificity: 85%). Two other studies were conducted in two
groups of Turkish asthmatic children (12, 23). Yavuz et al.
determined the role of C-ACT and fractional concentration of
exhaled nitric oxide (FeNO) in identifying children whose
asthma was not controlled (76 children, aged 6–11 years,
mean: 8.7 years) (12). C-ACT score was better than FeNO,
and an optimal cutoff point of 22 was also found (sensitivity:
69%; specificity: 77%). In a larger group (314 patients, mean
age: 9.0 !1.9 years, ranging between 4.3 and 11.8 year),
Erkoc
!oglu et al. evaluated the consistency of GINA criteria
and C-ACT on the determination of asthma control (23). In
this group, 51% were controlled according to C-ACT and
54.8% according to GINA criteria. If the cutoff point of 20
had the highest compatibility between GINA and C-ACT,
there was inconsistency in 26.7% (84/314) of the patients.
In our study, the optimal C-ACT cutoff point that cor-
rectly predicted not controlled children was 22 (GINA strict)
or 21 (GINA symptoms, NAEPP, physician’s assessment).
Furthermore, a C-ACT score <14 (GINA symptoms)
or <17 (physician assessment) improved the accuracy to
detect that asthma was not controlled. Liu et al. have also
established a second cutoff point <13 to detect very poorly
controlled asthma, associated with poorer outcomes (asthma
severity, lung function, level of treatment) (24).
Discrepancies between C-ACT score and GINA can be
explained by different approaches toward taking into account
asthma manifestations: no details on daily or nocturnal
asthma symptoms but strict definition in term of frequency
in GINA guidelines, more accurate definition but also more
tolerant for the frequency in C-ACT; impact of the criterion
‘exacerbation’ over the past year in the 2006 GINA guide-
lines; and a shift toward partial control in case of one exacer-
bation over the previous 12 months even if good control of
symptoms. This strengthens that the tolerance of one exacer-
bation per year proposed in the NAEPP definition of con-
trolled asthma, and the definition of control without this
criterion in the current GINA guidelines, may help to achieve
a more accurate definition (1, 2).
We reported age and past history of exacerbations as
important features of control level. In a large US study con-
ducted in general pediatricians, which included 2429 asthmat-
ics (4–17 years), the youngest patients had the worse scores,
which may reflect poor asthma control and a greater risk of
exacerbations, but also highlights the difficulty of measuring
the level of control in this population (25). Indeed, data are
collected from parents who underestimate asthma burden
and impact on the child’s life (26). Liu et al. have shown that
parents rated asthma as mild in 30% of uncontrolled asth-
matics according to C-ACT score (25). C-ACT has the
advantage to be easy to administer, even in the early age and
to question directly the children, with caregiver assistance.
Liu et al. have also showed that 35% of patients consulting
6%
34%
86%
15%
51%
89%
94%
66%
14%
85%
49%
11%
10%
20%
30%
40%
50%
60%
70%
80%
90%
100%
Controlled Not controlled
GINA symptoms Physician’s assessment
C-ACT < 14 14–21 > 21 < 17 17–21 > 21
(n) (31) (217) (277) (71) (167) (269)
% of patients
Figure 2 Performance of C-ACT cutoff points for correctly classifying asthma control according to the GINA symptoms criteria and to the
physician’s assessment.
Allergy 69 (2014) 784–790 ©2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd788
Asthma control assessment in children Deschildre et al.
for nonrespiratory-related complaints had a C-ACT score
of ≤19, vs 54% of those consulting for a reason related to
asthma (25). Thus, assessment of asthma control using a vali-
dated instrument should be performed at every visit, regard-
less of the reason.
The definition of control by GINA includes a functional cri-
terion, FEV
1
or PEF <or ≥80% of predicted value), which is
not the case with the C-ACT. In our study, it should be noted
that among the patients with an obstruction on PFTs, assessed
by FEV
1
/FVC ratio or airway resistances, 50% were consid-
ered controlled according to GINA symptoms criteria. That
emphasizes that the functional criteria used by the GINA are
not the best to assess respiratory function in childhood. The
FEV
1
/FVC or distal airways flows are more accurate parame-
ters in the evaluation of obstruction. In a study including 367
children with mild to moderate persistent asthma, Nair et al.
showed that up to 45% had abnormal PFTs and that this
result led to step-up treatment in 10–20% of them (27).
In conclusion, C-ACT is a supplementary tool in control
assessment and may be useful in daily medical practice, at
any time of the management, particularly in the youngest.
However, we confirm the discrepancies between the different
measurements available to assess asthma control in children
and the fact that generally used C-ACT cut-off point might
underestimate a part of the children whose asthma is not
controlled. Finally, C-ACT does not include lung function,
which is recommended on a regular basis. Evaluation of the
exacerbations over a longer period is also necessary in order
to anticipate and limit the risk.
Acknowledgments
We would like to thank all the pediatricians involved in this
study and especially the pediatricians of the A3PI (Associa-
tion Asthme Allergie Pneumologie Infantiles) network.
Funding
The survey has been funded by a grant from GSK France.
Conflicts of interest
A. Deschildre has received honoraria for lectures and expert
advises by NOVARTIS, GSK, MSD, TEVA, ALK, travel
assistance to attend a conference from GSK, Novartis, Mead
Johnson. J. de BLIC has received honoraria for lectures and
expert advises by ALK, CHIESI, GSK, MSD, Mundi-
Pharma, Stallerge
`nes and TEVA, travel assistance to attend a
conference from CHIESI, GSK, ALK. The other authors of
the paper declare no conflicts of interest.
Author contributions
All the authors had a substantial contribution to the concep-
tion and design, acquisition of data, analysis and interpreta-
tion of data. They contributed to the draft writing and
revised it critically. They finally approved the version to be
published.
References
1. GINA. http://www.ginasthma.com.
2. Expert Panel Report 3 (EPR3): guidelines
for the diagnosis and management of
asthma. Bethesda, MD: National Institutes
of Health, National Heart, Lung, and Blood
Institute, 2007 (http://www.nhlbi.nih.gov/
guidelines/asthma/asthgdln.htm).
3. de Blic J, Deschildre A; pour le Groupe de
Recherche sur les Avanc!
ees en Pneumo-
P!
ediatrie (GRAPP). Suivi de l’enfant
asthmatique: d!
efinition et outils de mesure.
Rev Mal Respir 2008;25:695–704.
4. de Blic J, Boucot I, Pribil C, Robert J, Huas
D, Marguet C. Control of asthma in children:
still unacceptable? A French cross-sectional
study. Respir Med 2009;103:1383–1391.
5. Fuhrman C, Dubus JC, Marguet C,
Delacourt C, Thumerelle C, de Blic J et al.
Report, Global Strategy for Asthma Man-
agement and Prevention; Hospitalizations
for asthma in children are linked to under-
treatment and insufficient asthma education.
J Asthma 2011;48:565–571.
6. Nathan RA, Sorkness CA, Kosinski M,
Schatz M, Li JT, Marcus P et al. Develop-
ment of the asthma control test: a survey for
assessing asthma control. J Allergy Clin
Immunol 2004;113:59–65.
7. Liu AH, Zeiger R, Sorkness C, Mahr T,
Ostrom N, Burgess S et al. Development
and cross-sectional validation of the
Childhood Asthma Control Test. J Allergy
Clin Immunol 2007;119:817–825.
8. Murphy KR, Zeiger RS, Kosinski M,
Chipps B, Mellon M, Schatz M et al. Test
for respiratory and asthma control in kids
(TRACK): a caregiver-completed
questionnaire for preschool-aged children.
J Allergy Clin Immunol 2009;123:833–839.
9. Juniper EF, Gruffydd-Jones K, Ward S,
Svensson K. Asthma control questionnaire
in children validation, measurement
properties, interpretation. Eur Respir J
2010;36:1410–1416.
10. Leung TF, Ko FW, Sy HY, Wong E, Li
CY, Yung E et al. Identifying uncontrolled
asthma in young children: clinical scores or
objective variables? J Asthma 2009;46:
130–135.
11. Koolen BB, Pijnenburg MW, Brackel HJ,
Landstra AM, van den Berg NJ, Merkus PJ
et al. Comparing Global Initiative for
Asthma (GINA) criteria with the Childhood
Asthma Control Test (C-ACT) and Asthma
Control Test (ACT). Eur Respir J
2011;38:561–566.
12. Yavuz ST, Civelek E, Sahiner UM, Buyuk-
tiryaki AB, Tuncer A, Karabulut E et al.
Identifying uncontrolled asthma in children
with the childhood asthma control test or
exhaled nitric oxide measurement. Ann
Allergy Asthma Immunol 2012;109:36–40.
13. Zapletal A, Motoyama EK, Van DE, Woe-
stijne KP. Maximum expiratory flow volume
curves and airway conductance in children
and adolescents. J Appl Physiol 1969;26:
308–316.
14. Beydon N, Amsallem F, Bellet M, Boule M,
Chaussain M, Denjean A, French Pediatric
Programme Hospitalier de Recherche
Clinique Group. Pre/postbronchodilator
interrupter resistance values in healthy
young children. Am J Respir Crit Care Med
2002;165:1388–1394.
15. Beydon N, Pin I, Matran R, Chaussain M,
Boul!
e M, Alain B et al. Pulmonary function
tests in preschool children with asthma. Am
J Respir Crit Care Med 2003;168:640–644.
16. Klug B, Bisgaard H. Specific airway resis-
tance, interrupter resistance, and respiratory
impedance in healthy children aged 2–
7 years. Pediatr Pulmonol 1998;25:322–331.
17. Bacharier LB, Phillips BR, Bloomberg GR,
Zeiger RS, Paul IM, Krawiec M et al.
Allergy 69 (2014) 784–790 ©2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd 789
Deschildre et al. Asthma control assessment in children
Severe intermittent wheezing in preschool
children: a distinct phenotype. J Allergy Clin
Immunol 2007;119:604–610.
18. Hedlin G, Bush A, Lødrup Carlsen K,
Wennergren G, de Benedictis FM, Melen E
et al. Problematic severe asthma in children,
not one problem but many: a GA2LEN
initiative. Eur Respir J 2010;36:196–201.
19. The Childhood Asthma Management Pro-
gram Research Group. Long-term effects of
budesonide or nedocromil in children with
asthma. N Engl J Med 2000;343:1054–1063.
20. Strunk RC, Sternberg AL, Szefler SJ, Zeiger
RS, Bender B, Tonascia J; Childhood
Asthma Management Program (CAMP)
Research Group. Long-term budesonide or
nedocromil treatment, once discontinued,
does not alter the course of mild to
moderate asthma in children and adoles-
cents. J Pediatr 2009; 154:682–687.
21. Covar RA, Szefler SJ, Zeiger RS, Sorkne ss
CA, Moss M, Mauger DT et al. Factors
associated with asthma exacerbations during
a long-term clinical trial of controller medi-
cations in children. J Allergy Clin Immunol
2008;122:741–747.
22. Wu AC, Tantisira K, Li L, Schuemann B,
Weiss ST, Fuhlbrigge AL; Childhood
Asthma Management Program Research
Group. Predictors of symptoms are different
from predictors of severe exacerbations from
asthma in children. Chest 2011; 140:100–107.
23. Erkoc
!o#
glu M, Akan A, Civelek E, Kan R,
Azkur D, Kocabas!CN. Consistency of
GINA criteria and childhood asthma control
test on the determination of asthma control.
Pediatr Allergy Immunol 2012;23:34–39.
24. Liu AH, Zeiger RS, Sorkness CA, Ostrom
NK, Chipps BE, Rosa K et al. The Child-
hood Asthma Control Test: retrospective
determination and clinical validation of a
cut point to identify children with very
poorly controlled asthma. J Allergy Clin
Immunol 2010;126:267–273.
25. Liu AH, Gilsenan AW, Stanford RH, Lin-
court W, Ziemiecki R, Ortega H. Status of
asthma control in pediatric primary care:
results from the pediatric Asthma Control
Characteristics and Prevalence Survey
Study (ACCESS). J Pediatr 2010;157:
276–281.
26. Blanc FX, Postel-Vinay N, Boucot I, De
Blic J, Scheinmann P. The AIRE Study:
data analysis of 753 European children
with asthma. Rev Mal Respir 2002;19:
585–592.
27. Nair SJ, Daigle KL, DeCuir P, Lapin CD,
Schramm CM. The influence of pulmonary
function testing on the management of asthma
in children. J Pediatr 2005;147:797–801.
Allergy 69 (2014) 784–790 ©2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd790
Asthma control assessment in children Deschildre et al.
