Received: 11 August 2021 | Accepted: 17 November 2021

DOI: 10.1002/ppul.25765

ORIGINAL ARTICLE: ASTHMA

Pediatric asthma symptom control during lockdown

for the COVID‐19 pandemic in Spring 2020: A prospective
community‐based study in Cyprus and Greece

Panayiotis Kouis PhD1 | Eleni Michaelidou MD, PhD2 | Paraskevi Kinni MSc1 |
Antonis Michanikou MSc1 | Pinelopi Anagnostopoulou MD, PhD1,3 |
Helen Dimitriou PhD2 | Kostas Karanicolas MSc1 | Andreas M. Matthaiou MD1 |
Souzana Achilleos PhD4 | Stefania I. Papatheodorou MD, PhD5 |
Petros Koutrakis PhD6 | Nicos Middleton PhD7 |
Emmanouil Galanakis MD, PhD | Panayiotis K. Yiallouros MD, PhD1
2

1
Respiratory Physiology Laboratory, Medical
School, University of Cyprus, Nicosia, Cyprus Abstract
2
Medical School, University of Crete, Objectives: To prospectively quantify at the community level changes in asthma
Heraklion, Greece
symptom control and other morbidity indices, among asthmatic schoolchildren in
3
Institute of Anatomy, University of Bern,
Bern, Switzerland response to coronavirus disease 2019 (COVID‐19) lockdown measures.
4
Cyprus International Institute for Methods: In Spring 2019 and Spring 2020, we prospectively assessed monthly
Environmental & Public Health, Cyprus changes in pediatric asthma control test (c‐ACT), asthma medication usage, infec-
University of Technology, Limassol, Cyprus
5
tions and unscheduled visits for asthma among schoolchildren with active asthma in
Department of Epidemiology, Harvard T.H.
Chan School of Public Health, Harvard Cyprus and Greece. We compared asthma symptom control and other morbidity
University, Boston, Massachusetts, USA
indices before and during lockdown measures, while participants’ time spent at
6
Department of Environmental Health,
home was objectively assessed by wearable sensors.
Harvard TH Chan School of Public Health,
Boston, Massachusetts, USA Results: A total of 119 asthmatic children participated in the study during Spring
7
Department of Nursing, Cyprus University of 2020. Compared to a mean baseline (pre‐COVID‐19 lockdown) c‐ACT score of
Technology, Limassol, Cyprus
22.70, adjusted mean increases of 2.58 (95% confidence interval [CI]: 1.91, 3.26,
Correspondence p < 0.001) and 3.57 (95% CI: 2.88, 4.27, p < 0.001) in the 2nd and 3rd monthly
Panayiotis Yiallouros, MD, PhD, Shacolas assessments were observed after implementation of lockdown measures. A mean
Educational Center of Clinical Medicine,
Palaios Dromos Lefkosias‐Lemesou 215/6, increase in c‐ACT score of 0.32 (95% CI: 0.17, 0.47, p < 0.001) was noted per 10%
2029 Aglantzia, Cyprus. increase in the time spent at home. Improvement was more profound in children
Email: yiallouros.panayiotis@ucy.ac.cy
with severe asthma, while significant reductions in infections, asthma medication
Funding information usage and unscheduled visits for asthma were also observed. During Spring 2019, 39
European Union LIFE Project MEDEA,
children participated in the study in the absence of lockdown measures and no
Grant/Award Number: LIFE16 CCA/CY/
000041; European Union LIFE, changes in c‐ACT or other indices of disease severity were observed.
Grant/Award Number: LIFE16 CCA/CY/
Conclusions: Clinically meaningful improvements in asthma symptom control, among
000041
asthmatic schoolchildren were observed during the COVID‐19 lockdown measures

This research was primarily done at Respiratory Physiology Laboratory, Medical School University of Cyprus, Nicosia, Cyprus.

386 | © 2021 Wiley Periodicals LLC wileyonlinelibrary.com/journal/ppul Pediatric Pulmonology. 2022;57:386–394.

KOUIS ET AL.
in Spring 2020. Improvements were independently associated with time spent at
home and were more profound in the children with severe asthma.
KEYWORDS
asthma, c‐ACT, COVID‐19, lockdown, SARS‐CoV‐2, schoolchildren
1 | INTRODUCTION
Αfter presenting in Wuhan, China, in December 2019, severe acute re-
spiratory syndrome coronavirus 2 (SARS‐CoV‐2) rapidly spread all over
the world and on March 11, 2020, World Health Organization char-
acterized coronavirus disease 2019 (COVID‐19) outbreak as a pandemic.1
In the absence of an effective vaccine in the first stages of the pandemic,
public health interventions at the community level were the only strategy
to control the spread of the virus. The interventions ranged from simple
isolation of disease carriers, quarantine of contacts and hand hygiene
measures to ban of mass gatherings, social distancing and finally to
complete lockdown and community quarantine.2–4 Although COVID‐19
in children was not as severe as in adults, the large‐scale public health
measures, especially the lockdowns, had important effects on social in-
teractions and physical activity amongst children and their families, as well
as on their education, access to health services and the way pediatric
medicine is practiced.5,6
Social distancing and other lockdown measures dramatically inter-
fered with spreading not only of SARS‐CoV‐2 but also of other pathogens
and decreased emergency department (ED) attendance and hospitaliza-
7–10
tion among children during this period. The sharp decline in pediatric
emergency visits and hospitalisations was largely attributed to reduction
in respiratory and gastrointestinal infections as air‐borne and droplet‐
transmitted diseases.11 Similarly, during the same period, pediatric asthma
encounters also demonstrated a dramatic decrease, well below historical
seasonal variation, in terms of hospitalizations, ED and outpatient vis-
its.12–14 However, large part of the reduction in attendances to hospitals,
ED and outpatients may be due to changes in health‐seeking behaviour
as a result of the public fear of visiting healthcare institutions.15 During
this period, most of routine checks in secondary and tertiary care were
substituted by remote assessments, employing video telemedicine and
telephone consultations.13,16 Overall, the exact impact of COVID‐19
lockdowns on asthma morbidity remains unknown, although prescriptions
of systemic steroids for asthma were also reduced, raising concerns
whether remote consultation is safeguarding asthmatic children, espe-
cially those with severe asthma that are difficult to assess remotely.13,16
In the context of complete lockdown measures, where assess-
ment of asthma burden remains difficult, the use of remote health
monitoring through validated tools for asthma symptom control
could overcome the limitations of the picture given by the asthma
encounters at the healthcare services level. Furthermore, the si-
multaneous use of wearable electronic sensors that objectively
quantify the behaviour and physical activity of asthmatic children
during this period could provide additional insights in the impact of
social distancing on asthma morbidity. The aim of this study was to
| 387
prospectively quantify at the community level changes in asthma
symptoms control in response to COVID‐19 lockdown measures in
asthmatic schoolchildren in Cyprus and Greece and relate the ob-
served changes with the time participants’ spent at home, as it was
objectively assessed by wearable sensors. In addition, we aimed to
examine during this period, changes in other relevant indices of dis-
ease severity such as the use of asthma medications, incidence of
infections and emergency healthcare visits.
2 | M A T E R I A L S AN D M E T H O D S
2.1 | Study population and setting
Primary school children, aged 6–11 years, with active asthma in Ni-
cosia, Cyprus and Crete, Greece were enrolled in the public health
intervention project LIFE‐MEDEA. LIFE‐MEDEA aims to evaluate
recommendations for reduction of exposure to particulate pollution
during desert dust storms (DDS) events. A detailed description of the
study design has been published previously.17 The study had two
data collection periods, the first in Spring (February–May) 2019 and
the second in Spring (February–May) 2020. Identification of eligible
children took place in the preceding Fall of each study period and
children were enrolled and followed up during the following Spring
(February–May) of 2019 and 2020. For the purposes of this study,
data were available from Cyprus in Spring 2019 and Spring 2020 and
from Greece in Spring 2020. Data on asthma symptom control were
not collected during Spring 2019 in Greece as a result of project
implementation difficulties. Ethical approvals were obtained from
relevant authorities in Cyprus and Greece and a written informed
consent was provided by the guardians of all participants at the time
of enrolment (Supporting Information File 1).
Participating children had a physician's diagnosis for asthma and met
at least one of the following eligibility criteria: daily intake of preventative
asthma medication, report of wheezing episodes, and/or unscheduled
healthcare visits for asthma during the past 12 months. In the absence of
previous clinical information on treatment, asthma control and exacer-
bations to define asthma severity,18 we calculated a surrogate measure of
asthma severity based on the number of eligibility criteria reported for
each participant. This surrogate measure was calculated as follows:
Physician's diagnosis plus one other eligibility criterion was defined as
asthma severity 1, physician's diagnosis plus two other eligibility criteria
was defined as asthma severity 2 and a physician's diagnosis plus 3
eligibility criteria was defined as asthma severity 3. Exclusion criteria in-
cluded lung disease other than asthma, cardiovascular disease or not
388 | KOUIS ET AL.

living for at least 5 days per week in the same household. Data from
confirmed or suspect COVID‐19 infection cases were excluded from
statistical analysis.
2.2 | Assessment of asthma symptom control
Asthma symptom control was assessed with the validated Greek
version of the pediatric asthma control test (c‐ACT),19 while a custom
questionnaire was also used to capture changes in other important
morbidity indices such as asthma medication usage, infections and
unscheduled healthcare visits for asthma. The c‐ACT is comprised of
seven items attaining a total score from 0 (poorest asthma control) to
20
27 (optimal asthma control). A change of two points and above in
the c‐ACT score has been previously found to be clinically mean-
ingful.19 Both questionnaires were administered through phone in-
terviews at baseline (February of each study period) and at monthly
intervals. The time periods of phone interviews across study periods
in Cyprus during Spring 2019 and Spring 2020 and Greece during
Spring 2020 were similar (Table S1).
2.3 | Daily monitoring of participants’ location and
physical activity
As part of the LIFE‐MEDEA project, participants were equipped with
wearable activity and location sensors embedded in a smartwatch to
assess adherence of asthmatic children to recommendations for reduction
of exposure to particulate pollution during DDS events. However, parti-
cipants were instructed to wear the smartwatch daily, during both DDS
and non‐DDS days and data collected were representative of their daily
routine during the whole study period. Continuous tracking of partici-
pants’ daily location and physical activity was carried out using the EM-
BRACETM smartwatch (Embrace Tech LTD, Cyprus), which is equipped
with multiple sensors such as pedometer, global positioning system (GPS)
and heart rate. As described previously,21 sensor data were collected and
synchronised per 5‐min intervals and transferred to a cloud‐based data-
base when the smartwatch was in range of the Wi‐Fi network inside the
participants’ home. For each participant, we defined the percentage of
time spent at home as the time with GPS signal within a radius of 100 m
of the participants’ home divided by 24 h. Location and physical activity
data were used to construct personal activity profiles for each participant

TABLE 1 Demographic and clinical characteristics of study participants

Asthmatic children Asthmatic children Asthmatic children

Parameter Cyprus 2019 (n = 39) Cyprus 2020 (n = 52) p valuea Greece 2020 (n = 67) p valueb

Demographic

Male gender 26 (67%) 35 (67%) 0.949 35 (52%) 0.098

c
Age, years 9.1 (1.7) 9.1 (1.7) 0.754 8.9 (2.1) 0.552
c
Weight, kg 37.5 (16.1) 35.7 (10.6) 0.151 36.6 (11.4) 0.638
c
Height, cm 137.7 (13.6) 136.9 (10.8) 0.123 135.3 (11.15) 0.429
2c
BMI, kg/m 19.0 (4.5) 18.8 (3.9) 0.567 19.6 (4.3) 0.249

Tobacco smoking exposure 5 (12.8%) 8 (15.4%) 0.120 13 (19.4%) 0.325

at home

Asthma eligibility criteria

Physician diagnosis of asthma 39 (100%) 52 (100%) 1.000 67 (100%) 1.000

Wheezing episodes 28 (72%) 35 (66%) 0.646 49 (73%) 0.489

Daily preventive medication 8 (21%) 10 (19%) 0.879 28 (42%) 0.008

Unscheduled physician visits for 25 (64%) 34 (64%) 0.899 38 (57%) 0.334

asthma

ER visits for asthma 4 (10%) 10 (19%) 0.120 19 (28%) 0.249

Asthma severity category

Asthma severity 1 19 (49%) 25 (47%) 0.952 27 (40%) 0.396

Asthma severity 2 16 (41%) 19 (36%) 0.663 30 (44%) 0.365

Asthma severity 3 4 (10%) 8 (15%) 0.496 10 (15%) 0.945

Abbreviation: BMI, body mass index.

a
Comparisons between asthmatic children in Cyprus participating in Spring 2019 and Spring 2020.
b
Comparisons between asthmatic children participating during Spring 2020 in Cyprus and Greece.
c
Values are presented as mean (SD), comparisons were made using independent t‐test. ER, emergency department; Asthma Severity 1: Physician diagnosis
plus one other eligibility criterion, Asthma Severity 2: Physician diagnosis plus two other eligibility criteria, Asthma Severity 3: Physician diagnosis plus
three or more other eligibility criteria.
KOUIS ET AL. | 389

in Cyprus and Greece and assess the compliance of asthmatic children to
the implemented public health interventions and lockdown for the pan-
demic.21 The public health interventions implemented at each site were
comparable both in terms of magnitude and timing and are presented in
detail in the online Supplement. A more detailed description of the lo-
cation and physical activity data collected, the method of analysis and an
overview of how activity of asthmatic children was modified during the
COVID‐19 lockdown have been presented previously.21
2.4 | Statistical analysis
children from Greece tended to more frequently take daily pre-
ventive medication (19% vs. 42%, p = 0.008) in comparison with
children in Cyprus, probably reflecting differences in asthma man-
agement at the two sites. Cypriot children participating in the study
during Spring 2019 and Spring 2020 were similar in terms of age,
gender and asthma severity. In both countries, no confirmed or
suspect COVID‐19 infection was recorded among our cohort during
the study period. A detailed description of participant characteristics
and comparisons between the different groups is presented in
Table 1. The distribution of key demographic and clinical character-
istics across the asthma severity categories is presented in Table S2.

Demographic and clinical characteristics of participants are sum-

marised for each country separately and compared using the in- 3.2 | Improvement in c‐ACT score in Spring 2020
dependent t and χ test for continuous and categorical variables
2

respectively. To prospectively assess the impact of COVID‐19 lock- Overall, during Spring 2020, c‐ACT score in asthmatic children improved
down measures on asthma symptoms control, the mean change in between pre‐COVID‐19 baseline and subsequent assessments during
c‐ACT score was calculated using a mixed effect model. The model COVID‐19 lockdown measures (Figure 1A). Improvement in c‐ACT score
included the period of assessment as the fixed effect term and a between assessments remained statistically significant after adjusting for
random intercept for each participant, while adjusting for age, gen- gender, age, intervention group, country and asthma severity. Among all
der, intervention group, country and asthma severity. Potential dif- participants, the mean baseline c‐ACT score was 22.70 and demonstrated
ferential effects on c‐ACT score across asthma severity categories, or an adjusted mean increase of 2.58 in the second assessment and 3.57 in
between the two countries, or the 2 years (for the case of Cyprus) the third assessment. The stepwise improvement in c‐ACT score was also
were examined using interactions terms and subgroup analyses ad- significant when analysed separately in each of the two countries. In
justing also for the effect of temperature. A similar mixed effect Cyprus, compared to a baseline c‐ACT score of 24.52, a mean increase
model, adjusted for age, gender intervention group, country and was observed in both the second (1.64) and third assessment (2.98).
asthma severity, was also employed to assess the relationship be-
tween percentage of time spent at home and c‐ACT score. For
comparison of the frequencies of other morbidity indices (asthma
medication, infections and unscheduled healthcare visits for asthma)
between the baseline and subsequent assessments, a logistic re-
gression model was used, adjusted for age, gender, intervention
group, country and asthma severity. Odd Ratios (OR) and 95% con-
fidence intervals (CI) are reported. Lastly, for asthmatic children in
Cyprus, data on c‐ACT score and other morbidity indices were
available for both Spring 2019 and Spring 2020. Thus, we repeated all
analyses separately to confirm that the trends noticed in 2020 were
not observed in the absence of COVID‐19 lockdown measures in
Spring 2019. Statistical comparisons were performed using STATA
16 (StataCorp.) and IBM SPSS Statistics 25 (SPSS Inc.). Statistical
significance was set at p < 0.05. A detailed description of the multi-
variable models used is available in Supporting Information File S1.

3 | RESULTS

3.1 | Characteristics of study participants

A total of 119 asthmatic children (52 from Cyprus and 67 from

Greece) took part in the study during Spring 2020. Children in both
countries were similar in terms of age, gender, body mass index,
tobacco smoking exposure at home, use of ER visits, unscheduled
visits to physicians for asthma and asthma severity. However,
F I G U R E 1 Observed changes in ACT score and other asthma
morbidity indices across the three assessment periods during Spring
2020. ACT, asthma control test [Color figure can be viewed at
wileyonlinelibrary.com]
390 | KOUIS ET AL.

Similarly, in Greece, compared to a baseline score of 23.53, a mean in-
crease of 3.30 and 4.07 were observed in second and third assessment
respectively. Although the improvement was somewhat steeper in
Greece compared to Cyprus, there was no significant interaction effect by
country on this relationship (p = 0.106) (Table 2).
In a mixed effects model, after controlling for gender, age, year,
intervention group and asthma severity, we found an independent posi-
tive effect of the percentage of time spent at home on c‐ACT score. This
effect was equal to a mean increase of 0.32 (95% CI: 0.17, 0.47,
p < 0.001) in c‐ACT score per 10% increase in the time spent at home.
We also found that the improvement recorded in c‐ACT score in
Spring 2020, was different across the asthma severity categories
(p value for interaction: 0.007) (Figure S1 and Table 3).
3.3 | Improvement in c‐ACT score in Spring 2020
in comparison to Spring 2019
For Cyprus, where c‐ACT test data were available for Spring of
2019 and Spring 2020 (with COVID‐19 lockdown), the adjusted
analysis for each year demonstrated a significant improvement in
c‐ACT score during 2020 but not in Spring 2019 (Figure S2).
More specifically, compared to a baseline of 24.52 in Spring
2020, a mean increase of 1.64 in the second assessment and 2.98
in the third assessment were observed. In contrast, in Spring
2019 and compared to a baseline of 22.79, there was a
nonsignificant change in the second and third assessment,
respectively (Table 4).

TABLE 2 Adjusted mean change in ACT score across the three assessment periods during Spring 2020

Population a
Parameter β Coefficient (95% CI)b Compared to baseline Compared to previous level

All subjects (n = 119) First (baseline) ACT 22.70 (20.08, 25.33) – –

Second ACT 2.58 (1.91, 3.26) <0.001 <0.001

Third ACT 3.57 (2.88, 4.27) <0.001 0.005

Cyprus (n = 52) First (baseline) ACT 24.52 (21.26, 27.79) – –

Second ACT 1.64 (0.64, 2.65) 0.001 0.001

Third ACT 2.98 (1.99, 3.97) <0.001 0.009

Greece (n = 67) First (baseline) ACT 23.53 (20.54, 26.52) – –

Second ACT 3.30 (2.41, 4.19) <0.001 <0.001

Third ACT 4.07 (3.13, 5.02) <0.001 0.108

Abbreviations: ACT, asthma control test; CI, confidence interval.

a
The interaction term ACT#Country was not statistically significant (p = 0.106).
b
Analysis adjusted for gender, age, intervention group, country, temperature and asthma severity.

T A B L E 3 Asthma severity subgroup analysis for the adjusted mean change in ACT score across the three assessment periods during
Spring 2020

Asthma severitya Parameter β Coefficient (95% CI)b Compared to baseline Compared to previous level

Asthma severity 1 (n = 52) First (baseline) ACT 22.43 (19.14, 25.71) – –

Second ACT 2.32 (1.26, 3.39) <0.001 <0.001

Third ACT 2.93 (1.83, 4.03) <0.001 0.280

Asthma severity 2 (n = 49) First (baseline) ACT 19.35 (14.86, 23.83) – –

Second ACT 2.47 (1.54, 3.41) <0.001 <0.001

Third ACT 3.62 (2.66, 4.57) <0.001 0.020

Asthma severity 3 (n = 18) First (baseline) ACT 16.07 (8.49, 23.66) – –

Second ACT 3.72 (1.84, 5.60) <0.001 <0.001

Third ACT 5.63 (3.68, 7.58) <0.001 0.055

Abbreviations: ACT, asthma control test; CI, confidence interval.

a
The interaction term ACT#Severity was statistically significant (p = 0.006).
b
Adjusted analysis for gender, age, intervention group and country.
KOUIS ET AL. | 391

T A B L E 4 Subgroup analysis for the adjusted mean change in ACT score across the three assessment periods during Spring 2019
(no COVID‐19 lockdown) and Spring 2020 (COVID‐19 lockdown)

Study perioda Parameter β Coefficient (95% CI)b Compared to baseline Compared to previous level

Cyprus Spring 2019 (n = 39) First (baseline) ACT 22.79 (15.50, 27.00) – –

Second ACT −0.52 (−1.77, 0.73) 0.389 0.389

Third ACT 0.44 (−1.29, 2.17) 0.438 0.102

Cyprus Spring 2020 (n = 52) First (baseline) ACT 24.52 (21.26, 27.79) – –

Second ACT 1.64 (0.64, 2.65) 0.001 0.001

Third ACT 2.98 (1.99, 3.97) <0.001 0.009

Abbreviations: ACT, asthma control test; CI, confidence interval.

a
The interaction term ACT#Year was statistically significant (p = 0.001).
b
Adjusted analysis for gender, age, severity, intervention group, temperature.

T A B L E 5 Change in risk for other

All subjects—Spring 2020
morbidity indices across the three Odds ratio (95% confidence
assessment periods during Spring 2020 Parameter Period interval)a Significance
Any asthma medication First (baseline) 1.00 –
assessment

Second assessment 0.60 (0.33, 1.09) 0.095

Third assessment 0.43 (0.24, 0.77) 0.004

Any infection First (baseline) 1.00

assessment

Second assessment 0.32 (0.18, 0.56) <0.001

Third assessment 0.05 (0.02, 0.13) <0.001

Unscheduled clinician First (baseline) 1.00 –

visits assessment

Second assessment 0.39 (0.21, 0.72) 0.003

Third assessment 0.04 (0.01, 0.11) <0.001

a
Adjusted for age, gender, country, intervention group and asthma severity.

3.4 | Change in other morbidity indices in
Spring 2020
For a set of other important morbidity indices (use of any asthma
medication, report of any infection, unscheduled healthcare visits for
asthma), we calculated separate ORs using data from all participants
in Spring 2020 after adjusting for age, gender, intervention group,
country and asthma severity (Figure 1B and Table 5). Compared to
baseline (pre‐COVID‐19), there was a statistically significant reduc-
tion in the use of any asthma medication, report of any infection and
unscheduled healthcare visits.
3.5 | Change in other morbidity indices in Spring
2020 in comparison to Spring 2019
Using available data from Cyprus, we repeated the analysis of other
important morbidity indices for Spring 2019 and Spring 2020. During
Spring 2019 there were no significant changes in the use of any
asthma medication, any infection and unscheduled healthcare visits in
contrast to the significant reductions in these indices noted during
Spring 2020 in Cyprus (Table S2).
4 | D IS CU SS IO N
This is the first study that prospectively quantified at the community
level, changes in asthma symptom control, among children with
asthma during the COVID‐19 lockdown measures in Spring 2020,
benefiting from the prior recruitment of patients for the ongoing
MEDEA project, before the spread of the pandemic.17 We docu-
mented significant improvements from the pre‐COVID‐19 baseline
c‐ACT score in Cyprus and Greece, in the range of 2.59 and 3.55
points during the first 2 months after introduction of lockdown
measures. These improvements are clinically meaningful as they are
above the 2‐points threshold difference, which is considered as
392 | KOUIS
minimally important.19 Interestingly, asthma severity had significant
interaction effect on the relationship between the period of assess-
ment and c‐ACT score, demonstrating higher improvements in the
most severe cases in the range of 3.72 and 5.58 points after in-
troduction of lockdown measures. As the most severe cases scored
lower baseline mean values in comparison to the milder cases (19.93
vs. 24.72), possibly they had more room for improvement in the
conditions that prevailed during the lockdown period, and eventually
resulted to higher magnitude improvements in c‐ACT score.
Although not identical, public health interventions implemented at
each site were comparable both in terms of magnitude and timing. The
direct association of lockdown measures with asthma symptom control
was confirmed by recovering an independent positive effect of time
spent at home percentage on c‐ACT score, as quantified by wearable
sensors that continuously tracked personal location and physical activity
of participants throughout Spring 2020 in both countries.21 The impact of
lockdown measures on pediatric asthma morbidity parameters including
symptom control, asthma medication intake and unscheduled healthcare
usage was further confirmed by examining the Spring 2019 data from
participants in Cyprus, who took part in the study in the previous year,
where there was there was no significant change in these parameters
between the three assessments performed over the same period of the
year. Our data, collected prospectively at the community level before and
after the emergence of COVID‐19, confirmed data published previously
from pediatric asthma hospitalizations, ED and outpatient visits that had
demonstrated a dramatic decrease during this period, below historical
12–14
seasonal variation. Retrospective studies that rely on electronic
22,23
healthcare records are subject to known inherent limitations, but also
they may be affected by changes in health‐seeking behaviour, public
beliefs and fears that develop in the context of a health crisis of this
magnitude.
During the same period, reduced respiratory morbidity was de-
monstrated in other pediatric chronic lung diseases, where re-
spiratory viral infections are a common trigger of pulmonary
exacerbations, suggesting that COVID‐19 restrictions might have led
to reduced exposure to viruses in general, not just SARS‐CoV2.24,25
Unfortunately, laboratory testing for respiratory viruses was not part
of our study protocol and data on viral infections pre‐ and during the
lockdown measures period were only available through questionnaire
responses. In both countries, participants reported a dramatic re-
duction of any infection during the assessments in Spring 2020, in
contrast to the report of no significant changes in incidence of any
infections during Spring 2019 in Cyprus. Moreover, this work is also
characterised by some limitations, especially in terms of the em-
ployed measure of disease severity and lack of Spring 2019 data from
Greece. Most definitions of severe asthma require a combination of
detailed information on asthma symptom control, prescribed treat-
ment and asthma exacerbations.18 However, since the asthmatic
children in this study were recruited from primary schools at the
community level, detailed clinical information on their condition was
not available. In this context, we used a surrogate measure of disease
severity based on the number of eligibility criteria reported for each
participant that is not validated, as other factors known to influence
ET AL.
disease severity were not considered. Similarly, external validity of
the study is somewhat affected by the nonavailability of ACT as-
sessments from 2019 in Greece. However, for our main analysis for
2020, data from Greece are in concordance with data from Cyprus
and confirm that improvement in asthma symptom control was ob-
served during the COVID‐19 lockdown measures. Finally, the dif-
ference in the use of daily asthma controller medication across the
two countries (Greece: 42% vs. Cyprus: 19%) was only partly re-
flected in the cACT score at baseline (Greece: 23.53 vs. Cyprus:
24.52). Although guidelines recommend to escalate asthma treat-
ment until the achievement of good symptom control and a fair cACT
score,26 we think that part of the difference in the use of asthma
controller medication may also reflect differences in asthma man-
agement at the two sites. Despite this observation, the effect of
lockdown measures and social distancing was statistically similar at
the two sites (interaction test for effect modification by country was
not significant, p = 0.106).
Overall, despite concerns raised by decreases in the use of
asthma medications and the reliability of remote assessments during
the restriction measures of the COVID‐19 pandemic,13–16 in this
population of children with active asthma, all metrics of asthma
morbidity including c‐ACT score, report of infections, use of asthma
medications and unscheduled healthcare visits for asthma demon-
strated the same trend towards a significantly reduced short‐term
morbidity burden. In contrast, during the COVID‐19 pandemic and
especially during strict lockdown measures, chronic respiratory pa-
tients experience psychological distress,27 as a result of fear of
contagion, stigma, frustration and boredom, as well as due to in-
adequate access to healthcare and other necessities.28 Furthermore,
for children with asthma and other chronic respiratory conditions,
many studies also highlight the deterioration of mental health29 and
report of psychological fatigue.30 However, for certain chronic dis-
eases, such as Primary Ciliary Dyskinesia, both parental and patient
stress levels appeared not to be affected.31 Nevertheless, among the
general paediatric population, it should not be overseen that social
distancing and lockdown measures have been consistently associated
with adverse psychological effects,32,33 as well as with reduced
physical activity34–36 and increased use of TV and electronic de-
vices.36,37 Future studies could further examine the physical and
mental health trade‐off resulting from social distancing in asthmatic
children and examine the optimal methods to provide social and
psychological support. In addition, it is imperative to better under-
stand and enhance the self‐management skills of children with
asthma and their caregivers in the context of social distancing mea-
sures.38 This approach can be further complemented by the devel-
opment and implementation of robust telemedicine networks that
will allow close follow‐up of asthmatic children. As demonstrated by
several studies, this pandemic has led to the successful deployment
of such systems that were characterised by improved interplay be-
tween patients, caregivers and clinicians.39–41 However, the long‐
term utility and cost effectiveness of such systems, as well as their
legal, ethical and cultural implications under nonpandemic conditions,
should be better studied and quantified.42
KOUIS ET AL.
5 | C ONC LUS I ON
In summary, in a community‐based study we prospectively
quantified clinically meaningful short‐term improvement in
asthma symptom control, among children with active asthma
during the COVID‐19 lockdown measures in Spring 2020, that
were independently associated with the percentage of time spent
at home and was more profound in the children with more severe
asthma. A similar improved trend was noted in the short‐term
report of infections, use of asthma medications and unscheduled
healthcare visits for asthma.
A C KN O W L E D G M E N T S
The authors are grateful to all the participants and their families as
well as to the teaching and administrative personnel of participating
primary schools in Cyprus and Greece. The study was financed by the
European Union LIFE Project MEDEA (LIFE16 CCA/CY/000041).
CO NFL I CT OF INTERES T S
The authors declare that there are no conflict of interests.
ETHICS APPROV AL AND I NFORMED CONSE NT
Administrative and ethics approvals were obtained from the Cyprus
Ministry of Health (YY5.34.01.7.6E) and the Cyprus National
Bioethics Committee (ΕΕΒΚ/ΕΠ/2016.01.23). In Greece, the study
has received administrative and ethics approval from the Scientific
Committee (25/04/2018, No.: 1748) and the Governing Board of the
University General Hospital of Heraklion (25/22/08/2018). Guar-
dians of all subjects provided a written informed consent prior par-
ticipation of children in the study.
AUTHORS CONTRIBUTIO NS
Panayiotis Kouis: Project administration, methodology, software,
data curation, visualisation, formal analysis, writing‐original draft
preparation; Eleni Michaelidou: methodology, data curation, vi-
sualisation, formal analysis, writing—review and editing; Para-
skevi Kinni: data curation, software, visualisation, writing—
review and editing; Andreas M. Matthaiou: data curation, soft-
ware, visualisation, writing—review and editing; Pinelopi
Anagnostopoulou: data curation, formal analysis, writing—review
and editing; Helen Dimitriou: Project administration, data cura-
tion, writing—review and editing; Kostas Karanicolas: Data
curation, writing—review and editing; Andreas M. Matthaiou:
data curation, writing—review and editing; Souzana Achilleos:
data curation, visualisation, writing—review and editing, software,
writing—review and editing; Stefania I. Papatheodorou: metho-
dology, writing—review and editing; Petros Koutrakis: metho-
dology; writing—review and editing; Nicos Middleton:
visualisation, formal analysis, writing—review and editing;
Emmanouil Galanakis: methodology, writing—review and editing,
supervision; Panayiotis K. Yiallouros: conceptualization, metho-
dology; writing—review and editing, funding acquisition,
supervision.
| 393
DATA AVAILABILITY STATEMENT
The study dataset is available from the corresponding author upon
reasonable request.
ORC I D
Panayiotis Kouis http://orcid.org/0000-0003-0511-5352
Pinelopi Anagnostopoulou http://orcid.org/0000-0003-2597-8016
Nicos Middleton https://orcid.org/0000-0001-6358-8591
Panayiotis K. Yiallouros https://orcid.org/0000-0002-8339-9285
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SUPP ORTING INFO RM ATION
Additional supporting information may be found in the online version
of the article at the publisher’s website.
How to cite this article: Kouis P, Michaelidou E, Kinni P, et al.
Pediatric asthma symptom control during lockdown for the
COVID‐19 pandemic in Spring 2020: a prospective
community‐based study in Cyprus and Greece. Pediatric
Pulmonology. 2022;57:386‐394. doi:10.1002/ppul.25765