Impact of the COVID-19 on asthma control among children: A systematic review

Abstract

In December 2019, the current outbreak of coronavirus disease 2019 (COVID-19) was reported in Wuhan, China. Asthmatic patients are thought to be more vulnerable to the more severe form of SARS-CoV-2 infection due to their weakened immune systems and increased risk of respiratory exacerbation when infected with respiratory viruses; however, there is little evidence to support this theory. The objective of this systematic review is to assess the impact of the COVID-19 lockdown during the pandemic on asthma management outcome measures among children and adolescents. To conduct the search, we used five bibliographic databases. The results were limited to those articles published between December 2019 and February 2022, selecting only articles published in English that included the study population (children aged 0–18 years). All study designs were considered. Independent assessments of the included studies’ quality were made and reported. Among the 945 results of the bibliographic search, only 21 articles were found to fit our eligibility criteria We organized the results from the studies according to the effect of the lockdown at the start of the COVID-19 pandemic on common outcomes, including the Pediatric Emergency Department Visits, hospitalization rates of pediatric asthmatic patients during the pandemic, asthma control, asthma exacerbations, psychological effects on patients, and caregivers’ concerns. The management of pediatric asthma improved more during the 2020 COVID-19 pandemic lockdown than in previous years.

Keywords

Asthma COVID-19 children health asthma management review

Introduction

In December 2019, the current outbreak of coronavirus disease 2019 (COVID-19) was reported in Wuhan, China.¹ The World Health Organization (WHO) classified the outbreak as a pandemic on March 11, 2020, as the disease was spreading rapidly in many countries.² COVID-19 pandemic is terrible and health disparities exist, connection with worse mortality/morbidity are seen in certain disease states, and although considered one of those disease states that conferred risk, this is no longer considered to be the case.

Asthma is common and like COVID_19 disparities exist, and COVID-19 did decrease access to care for cases other than COVID given that it filled hospitals and ICU. Since asthma is a disease that waxes and wanes with periodic exacerbations, we were concerned how asthma healthcare utilization and control fared through the critical years to date of the pandemic. The Centers for Disease Control and Prevention (CDC) claims that individuals suffering from asthma are considered at high risk for hospitalization and other severe outcomes from COVID-19.³ However, clinicians still lack full evidence on COVID-19 management, and the pandemic has prompted them to make decisions based on ambiguous data.

Since COVID-19 is transmissible infectious disease that require major interventions, comonly lockdowns, which are envisioned to have a positive impact on all transmissible infectious diseases, not just the COVID-19. This impact may be especially noticeable in pediatrics, where 28% of diagnoses in pediatric emergency departments (EDs) are related to a contagious illness.⁴ As expected, there has been a decrease in the overall number of pediatric hospital admissions and emergency department (ED) visits.⁵

Even though asthma death rates have decreased significantly over the last few decades, national and worldwide surveys continue to demonstrate that more than half of patients have inadequate asthma management. Asthma is a prevalent chronic medical illness that requires daily management, such as avoiding triggers and adhering to drug regimens.⁶ Yet, sufferers of this chronic condition may have less access to treatment as a result of limitations on general mobility, lockdowns, and the allocation of health services to care for patients with COVID-19.⁷ Due to their weakened immune systems and elevated risk of respiratory exacerbation when infected with respiratory viruses, asthma patients are thought to be more susceptible to the more severe form of SARS-CoV-2 infection; however, there is insufficient evidence to prove this theory.

A systematic review was conducted to evaluate the impact of the COVID-19 lockdown during the pandemic on asthma management outcomes among patients aged up to 18 years old. For instance, we examined asthma control tests (ACTs), asthma exacerbations, the number of pediatric emergency department (ED) admissions before and during the COVID-19 lockdown. We also aimed to understand the participants’ opinions about the psychological effects of COVID-19 on asthmatic children and the concerns of their caregivers during the pandemic.

Materials and methods

Eligibility criteria and definitions

This review followed the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines. Human studies involving study aged under 18 years published in English were considered. Each study in this systematic review included young people who had been diagnosed with asthma. The studies had to focus on the impact of the initial COVID-19 lockdowns on children with asthma and adolescent patients with regard to the health utilization and asthma control. Interventions that focused on COVID-19 and asthma with other comorbidities, such as obesity, were excluded.

Search strategy

To conduct the search, we used five bibliographic databases: MEDLINE (PubMed), Web of Science, Scopus, Embase, ProQuest (Health & Medical Collection). Reference lists from articles included in the literature review were manually searched to identify other possibly eligible studies. Articles could only be published between December 1, 2019, and February 15, 2022 (Table 1).

Table 1.

Search strategy.

Search no.	Search terms
1	Child * OR pediatric OR paediatric OR
1	adolescents OR teen * OR school OR PEDIATRICS
2	asthma OR ASTHMA
3	COVID-19 OR nCov OR novel coronavirus OR
3	Sars-Cov-2
4	self-manage * OR control OR self-efficacy OR
	adherence OR
	medication OR compliance OR observation
	OR judgement OR “action plan”
5	1 AND 2 AND 3 AND 4

Study selection

The titles and abstracts of all articles gathered by the search were evaluated by two reviewers after duplicates were removed. Studies that did not meet the aforementioned qualification criteria were excluded. The full texts of the remaining papers were obtained and critically reviewed for inclusion in the review.

Data extraction

The following data were derived from each article: the articles’ author(s), study location, age group(s), sample size, and period of study; the study outcome and measures; and from the quantitative studies, the estimated effect size with 95% confidence interval (CI) was retrieved.

We structured the results from the studies according to the effect of the lockdown at the start of the COVID-19 pandemic on common outcomes, including the number of pediatric ED visits before and during the COVID-19 lockdown, hospitalization Rates of Pediatric Asthmatic Patients during the Pandemic, asthma control, asthma exacerbations, psychological effects on patients, and caregivers’ concerns.

Quality assessment

We used a tool that allowed us to assess studies that combined quantitative and qualitative methodologies to carry out the quality assessment. We adapted a scale from numerous published sources that addressed the topics important to quantitative and qualitative studies.⁸ An evaluation of the external validity, bias and reporting quality was conducted using a 12-question scoring tool. The tool allowed evaluation of respondent validation, multiple coding, and purposeful sampling for qualitative studies. Each article was assessed independently by two authors (AQ and RM). The researchers discussed their differences and sought agreement on the overall quality score before coming to a consensus.

Results

Nine hundred forty-five records were found after a literature search of five online databases. Seven hundred seventy-four articles were left after removing duplicate records; these were then screened to determine how applicable they were to the review. Seven hundred forty-nine articles were eliminated after the initial abstract screening, and the full manuscripts of 25 studies were examined for compliance with the inclusion criteria. A further four studies were excluded because the cutoff age of the participants was 21 years old^9,10 and because the participants were only recruited from a pediatrician’s or family physician’s practice.^11,12 After applying the exclusion criteria, 21 studies remained on the impact of the COVID-19 pandemic on asthmatic children (Figure 1).

Figure 1.

Preferred Reporting Items for Systematic Reviews and Meta-Analysis (PRISMA) flow chart of search methodology.

Nearly all of the studies were determined to be of reasonable quality because the recruitment methods were clear, participant characteristics were explicitly stated, data collection techniques were clearly defined, and data was collected systematically. The majority of the included studies were retrospective, with cohort, case-control, and cross-sectional designs. The studies focused on outcomes such as asthma control, asthma exacerbations, and the number of pediatric ED visits before and after the COVID-19 pandemic lockdown. The included studies also took into account the frequency and number of admissions, medication adherence, asthma exacerbations, psychological effects, and caregivers’ concerns (Table 2).

Table 2.

Characteristics of the included studies.

Author	Study location	Age group	sample size
Ochoa-Avilés et al.⁷	Ecuador	5–17 years	N = 213
Arsenault et al.¹³	Michigan, USA	<18	N* = 4865 in 2019 N* = 2129 in 2020 * total yearly visits
Guijon et al.¹⁴	California, USA	9.6 ± 4.6 years	N = 18,912 pediatric patients with asthma
Hurst et al.¹⁵	North Carolina, USA	5–17 years	N = 3959
Ulrich et al.¹⁶	Ohio, USA	2–18 years	N = 121,000–125,000 members.
Al-Iede et al.¹⁷	Jordan	4−17 years	N = 374 parents/caregivers N = 297 responded
Bover-Bauza et al.¹⁸	Spain.	<15 years	N* = 644 (pre-COVID-19). N = 158 Asthmatic children N* = 128 (COVID-19 era patient) N = 30 Asthmatic children. patients suffered respiratory pathology
Golan-Tripto et al.¹⁹	southern Israel	2–18 years	N (total) = 512 children N = 273 in 2019 N = 239 in 2020
Fan et al.²⁰	China	<18	N = 416 asthma exacerbation
Shi et al.²¹	Scotland	5–17 years	N total = 752,867 children N = 63,463 Asthmatic N = 4339 Asthmatic with COVID19
Papadopoulos et al.²²	15 countries	4–18 years	N = 1054 asthmatic N = 505 non-asthmatic
Di Riso et al.²³	Italy.	7–14 years for children	N = 45
Farzan et al.²⁴	New York, USA	2–18 years	N = 38 inpatients N = 95 outpatients
Ferraro et al.²⁵	Italy	12 ± 3 years	N = 92 asthmatic children
Jia et al.²⁶	China	4–17 years	N = 16 caregiver
Sánchez-Garcia et al.²⁷	Spain.	<18 years	N = 107 children.
Taytard et al.²⁸	France.	9.7 Median age.	N = 3419 files
Yucel et al.²⁹	Turkey	8.5 Mean age	N = 84 asthmatic
Caveney et al.³⁰	New York, USA	3−12 years	N = 93 caregivers of children
Clawson et al.³¹	Johns Hopkins University	5–17 years for children Parents ≥18	N = 321 N = 278 completed the questionnaire
Cekic et al.³²	Turkey	12–18 years	N = 125 Adolescents with asthma N = 98 Control

Pediatric emergency department visits

Eight observational studies counted the number of ED visits (Table 3), all of which were conducted in the United States among adolescents and children,^7,13
–16 with the exception of one each in Jordan, Spain, and Israel.^17
–19

Table 3.

Main outcomes.

Author	Period of study	Outcomes	Results	Findings
Ochoa-Avilés et al.⁷	Before lockdown: (December 12, 2019 to March 31, 2020) During lockdown :(April 1 to July 12, 2020)	Pediatric Emergency Department (PED) Visits Asthma Exacerbation (AE)	ER visits declined 89% during lockdown (compared to before lockdown (IRR 0.11, 95% CI 0.04–0.32, p < 0.001). No significant change in the number of reported AE during the lockdown measures compared to before. p < 0.152	Significantly declining in ER visits during the lockdown compared with the period before. No significant change.
Arsenault et al.¹³	Before lockdown : (March 16 to December 31) 2019 During lockdown : (March 16 to December 31) 2020.	(PED) Visits	Significantly reduction from 3923 to 1142 during the lockdown compared to before; p < 0.0001).	Pediatric ED visits decreased in the spring of 2020, which coincided with school closure
Guijon et al.¹⁴	January to March and April to June from 2017 to 2020	(PED) Visits Hospitalization Rates (HR)	Significantly greater changes reductions in PED visits during COVID-19 compared to 2017–2019 (p < 0.05). 78%reductions in HR during COVID-19 with (p < 0.05).	There was a significant reduction in hospitalization, emergency department visits, exacerbations, and albuterol and inhaled corticosteroid use during lockdown.
Hurst et al.¹⁵	March 1, 2019–February 29, 2020 March 1, 2020–February 28, 2021	(PED) Visits HR AE	Significantly reduction : 9.7% during lockdown to 21.0% before. (p < 0.01). Significantly reduction during the pandemic compared to before (1.6% vs 2.5%; p < 0.01). Significantly declining during the pandemic compared to the preceding (127 vs 504; p < 0.01).	The COVID19 pandemic coincided with dramatic shifts in healthcare utilization, including increased telehealth use and improved asthma outcomes in children. Social isolation may have also reduced asthma trigger exposure. All-cause healthcare encounters decreased significantly during the pandemic
Ulrich et al.¹⁶	From January to June for 2017–2020	(PED) Visits HR	PED visits decreased by 45.8% (p = 0.03) In 2020 (from January through June) compared to the 3-year average of 2017–2019 HR decreased by 50.5% (p = 0.03) from January to June in 2020	The reduction in asthma-related emergency department visits due to factors other than avoidance of health-care facilities. A variety of factors could explain the decrease in acute asthma health-care visits. Localized reductions in air pollution and viral exposure.
Al-Iede et al.¹⁷	From 5 to 12 September 2020. lockdown period: (March 17 to May 24, 2020) Before lockdown: (March 17–May 24, 2019)	(PED) Visits HR	ED visits decreased significantly from 137 to 80 during 10 week lockdown period compared to (p ≤ 0.0001). Significant reduction from 56 to 24 during a lockdown compared with the same period in the previous year (p ≤ 0.0001).	During the lockdown, there was a significant decrease in the number of ED visits and hospital admissions for acute asthma exacerbations.
Bover-Bauza et al.¹⁸	March 14 to April 15, 2019 (pre-COVID-19). March 14 to April 15, 2020 (COVID-19 era).	(PED) Visits	Estimated 82% lower than in 2019.	Lockdown measures have resulted in a significant decrease in emergency visits to the pediatric service.
Golan-Tripto et al.¹⁹	2020 A, B, C 2019 A, B, C A: pre-lockdown, (1 February 2020 to 14 March 2020), 2020 B: lockdown, (15 March 2020 to 15 May 2020) 2020 C: post-lockdown (16 May 2020 to 30 June 2020)	(PED) Visits HR	Fewer ED visits per day during lockdown (1.8 vs 1.43; p < 0.001). Significant increase: 47.1% (24 out of 51) in 2020 B compared with 33.7% in 2019 B (30 out of 89; p = 0.05).	Lockdown is associated with fewer ED visits for asthmatic patients. During the lockdown, ED visits were associated with a higher hospitalization rate and a longer length of saty.
Fan et al.²⁰	February to June 2016–2019 February to June 2020	AE HR	The AE during the COVID-19 pandemic are 13/85, compared to 24/54 before the pandemic. The number of severe AE per month decreased, while the number of mild AE per year increased (p = 0.004).	Result suggest that During the COVID-19 pandemic, most pathogens and air pollutants decreased. The frequency of severe asthma exacerbations in children was positively correlated with respiratory infections, but not with air pollutants.
Shi et al.²¹	Between March 1, 2020, and July 27, 2021	HR	HR = 1.5% from asthmatic children with confirmed COVID-19. HR = 0.9% from non-asthmatic children with confirmed COVID-19. The adjusted HR was 6·40 (95% CI 3.27–12.53) for those with poorly controlled asthma. 1·36 (1.02–1.80) for those with well-controlled asthma, compared with those with no asthma	Children with poorly controlled asthma had a higher rate of COVID-19 hospital admission than those with well-controlled asthma or those without asthma.
Papadopoulos et al.²²	March-June 2019 March-June 2020	HR AC	The HR dropped from 9.8% among asthmatic children in 2019 to 1.2% in 2020 with p < 0.001. 90.2% of the participants Improved or unchanged asthma control during pandemic. 9.8% reported worse asthma control. 65.9% experienced an improvement (p < 0.001).
Di Riso et al.²³	Survey online from 28th May to 23rd August 2020.Phone call scheduled in April–May 2020	ACPsychological Effects and Caregivers’ Concerns	80% showed well-asthma controlled	Mothers reported more Covid-19 related fears, and greater worries according to the resumption of their children’s activities.
Farzan et al.²⁴	March and July 2020 and six months prior.	AC	41% of the outpatients reported improved asthma control	Childrens with asthma did not progress to a more severe stage and required less care.Outpatients had better medication adherence and control, as well as a lower risk of hospitalization. Biological and behavioral factors may have mitigated against severe disease.
Ferraro et al.²⁵	March–April 2019March–April 2020	ACAEPsychological Effects and Caregivers’ Concerns	Significant increase in the level of asthma control in 2020 (March p = 0.023; April p = 0.007) compared with the same time period in the previous year.A significant inverse correlation was described between GINA score and ACT both in March 2020 (rs = −0.613, p < 0.001) and in April 2020 (rs = −0.629, p < 0.001).Four AEs were reported in March/April 2020 compared to ten AEs were reported in March/April 2019 (p = 0.095).	Both the case and the control groups show the same level of asthma control.
Jia et al.²⁶	May 2020	AC	50% of children have a good asthma control since the pandemic.
Sánchez-Garcia et al.²⁷	March 15, 2020 to June 15, 2020	AC	58 (54.2%) patients had well-controlled asthma during the 2020 pandemic, compared to 30 (28%) in 2019.15 (14%) patients had poorly controlled asthma during the 2020 pandemic, compared to 28 (26.2%) in 2019	The perception that better management of asthma was delivered during the pandemic by those working in cities with a high prevalence of COVID-19 versus other regions
Taytard et al.²⁸	2019: First, third, and fourth quarters.2020: First, third, and fourth quarters.	ACAE	Asthma was better controlled during Q4-2020 compared to Q4-2019 (p = 0.042)In 2020, the proportion of children with at least one exacerbation in the preceding 3 months was higher before the lockdown (Q1-2020 259/434 [59.7%] vs. Q1-2019 321/613 [52.4%]; p = 0.022) but lower after the reopening (Q3-2020 153/460 [33.3%] and Q4-2020 237/530 [44.7%] vs. Q3-2019 222/466 [47.6%] and Q4-2019 330/559 [59%], respectively, both p < 0.0001)	After the reopening, asthmatic children experienced fewer exacerbations, improved asthma symptom control, and improved lung function.
Yucel et al.²⁹	20192020	ACAE	Asthma control tests were significantly improved (p < 0.001).A significant reduction in asthma exacerbations during the lockdown (p < 0.001) compared with the same period in 2019.
Caveney et al.³⁰	April and November 2020	Psychological Effects and Caregivers’ Concerns
Clawson et al.³¹	June 2020 to August 2020	Psychological Effects and Caregivers’ Concerns		The pandemic is exacerbating inequities for BIPOC families, particularly those with asthmatic children.The importance of interventions that address the needs of underserved communities by providing the infrastructure, policies, and supports required to reduce health disparities during and after COVID-related interventions
Cekic et al.³²	March 2020 and March 2021		Psychological Effects and Caregivers’ Concerns	Asthmatic patients believed COVID-19 could be transmitted to them more easily.Mostly all asthmatic patients and controls asserted that they basically following the COVID-19 protection rules. Outside, both groups had high rates of wearing face masks and compliance with physical distancing.

One study was conducted in an inner-city children’s hospital in Detroit, Michigan. Data were collected over a full 1-year (365-day) period for both 2019 and 2020.¹³ Arsenault et al. stated that the number of ED visits significantly dropped from 3923 in 2019 to 1142 in 2020 when comparing the same period in both years (March 16–December 31; p < 0.0001). The total number of pediatric ED visits for asthma was 260 after school closures (March 15–May 31), compared to 1304 visits the previous year (2019). For the remainder of 2020, there were 1142 ED visits (March 16–December 31). However, there was no statistically significant difference between the 942 children who were seen in the ED for asthma before March 15 in 2019 and the 987 children who were seen there before schools closed on March 15, 2020 (January 1–March 15).¹³ A study carried out in Spain that involved 158 children with asthma aged <15 years estimated that the percentage of ED visits among asthmatics in 2020 was 82% lower than in 2019.¹⁸

In Jordan, Al-Iede et al.¹⁷ found a significant reduction in the number of ED visits from 137 to 80 during a 10-week lockdown period (March–May 2020) compared with the same time period in the previous year (March–May 2019) (p ≤ 0.0001). At Soroka University Medical Center, a single tertiary center in southern Israel, Golan-Tripto et al.¹⁹ reported that 512 children visited the ED for asthma exacerbation: 273 in 2019 (89 in 2019 B) and 239 in 2020 (51 in 2020 B) Table 3. When compared to the same calendar period in 2019, the lockdown period in 2020 demonstrated significantly fewer ED visits per day (1.8 vs 1.43; p < 0.001).

In 18,912 pediatric patients with asthma from the Children’s Hospital of Orange County network, the number of ED visits significantly decreased (by 90%) during the months of April–June 2020 compared with the same period in the three previous years (2017–2019). However, the reduction of visits to this department was not seen among African American patients.¹⁴ Similarly, the results of Hurst et al.’s study¹⁵ showed that the rate of patients with ED visits <24 h in duration decreased significantly during the pandemic.

A study of outpatients aged 5–17 years with acute asthma attacks between April 2019 and February 2020 conducted in three cities in Ecuador (Quito, Cuenca, and Portoviejo)⁷ documented an 89% decrease in the percentage of ED visits (p < 0.001) for all participants (N = 213). Consistent results were documented in another study of 121,000–125,000 members of this population between the ages of 2 and 18.¹⁶ From January to June of each year, there were a total of 636 ED visits for asthma in 2017, 614 in 2018, and 590 in 2019. By June 2020, the ED visits were down 45.8% (p = 0.03). The decrease in asthma-related ED visits was greater than the overall decrease in ED visits during the same time period, implying that the former decrease was due to factors other than avoidance of healthcare facilities.

Hospitalization rates of pediatric asthmatic patients during the pandemic

Since the COVID-19 pandemic began, numerous studies have highlighted that pediatric asthmatic patients’ hospitalization during the pandemic has decreased (Table 3). In our review, only 7 of 26 articles stated that the number of hospitalizations among asthmatic children during the pandemic dropped compared to preceding years,^{14
–17,20
–22} while 1 study refuted this assertion.¹⁹

In Guijon et al.’s study,¹⁴ there was a 78% reduction in the hospitalization rate of asthmatic pediatric patients during COVID-19 2020 compared with pre–COVID-19 2020. Hurts et al.¹⁵ reported that inpatient admissions decreased from 2.5% (March 1, 2020–February 28, 2021) to 1.6% (March 1, 2019–February 29, 2020; p < 0.01). Moreover, in Ulrich et al.’s study,¹⁶ there were 166, 182, and 177 inpatient admissions for asthma from January to June in 2017, 2018, and 2019, respectively, but for the same period in 2020, inpatient admission rates fell by 50.5% (p = 0.03).

According to Al-Iede et al.’s study,¹⁷ there was a decrease in the number of admissions of pediatric asthmatic patients from 56 to 24 during a 10-week lockdown period in 2020 compared to the same period the year before. However, Golan-Tripto et al.¹⁹ reported a significant increase in the hospitalization rate of this group during the lockdown: 47.1% in 2020 B compared with 33.7% in 2019 B (p = 0.05).

Fan et al.’s study,²⁰ which was conducted in Guangzhou Women and Children’s Hospital, China, showed a decrease in the number of patients hospitalized with infectious respiratory diseases from 146 per month before the pandemic to 42 per month during the pandemic (p = .004).

Shi et al.²¹ estimated the prevalence of COVID-19 among children with controlled and uncontrolled asthma using data from the Early Pandemic Evaluation and Enhanced Surveillance of COVID-19, Scotland. In a study sample of 63,463 asthmatic children aged 5–17 years, 4339 contracted COVID-19 between March 1, 2020, and July 27, 2021. A higher rate of COVID-19 hospital admission was found to be associated with poorly controlled asthma.

Papadopoulos et al.’s study²² of asthmatics (N = 1054) and non-asthmatics (N = 505) aged 4–18 years from 15 countries reported decreasing rates of hospitalization for children with acute asthma before and during the pandemic. The hospitalization rate significantly decreased from 9.8% in 2020 during the pandemic compared to the previous year (p < 0.001).

Asthma control

Regarding to asthma control, the included studies offering a unique insight how the changes resulting from COVID 19 have positively impacted on asthma control among children. Improvements in ACT scores were observed in eight studies in this review (Table 3). A study was conducted among outpatients with asthma aged 7–14 years with their mothers compared to a control sample from the Unit of Pediatric Allergy and Respiratory Medicine in the Women and Children’s Health Department, University of Padova, Italy.²³ After the lockdown, the participants were provided an online survey (from 28th May to 23rd August 2020). Of a clinical sample of 45 patients, 80% showed well-controlled asthma, as indicated by the Global Initiative for Asthma (GINA) score. However, 6.7% of the sample had uncontrolled asthma. In another study²⁴ conducted at Cohen Children’s Medical Center (CCMC) of the Northwell Health System, New York, consistent results were documented for 38 inpatients, 13 with asthma, and 95 outpatients with persistent asthma. During the onset of the pandemic (March–July 2020), 41% of the outpatients reported improved asthma control and decreased use of rescue inhalers compared to 6 months before.

In Ferraro et al.’s study,²⁵ the GINA scores were calculated for March and April of 2019 and 2020 for the analysis of asthma control. In March 2020, 53 children (57.6%) had their asthma under control to the same extent as the previous year, 27 (29.3%) had better asthma control, and 12 (13%) had worse asthma control. These results varied slightly in April 2020, with 53 (57.6%), 30 (32.6%), and 9 (9.8%) children demonstrating the same, better, and worse levels of asthma control as the year before, respectively. For the entire group of patients, the GINA score was significantly lower in March 2020 compared to March 2019 (p = 0.023) and in April 2020 compared to April 2019 (p = 0.007), both of which indicate better control.²⁵

An observational study was conducted in Jinan, China, which involved 16 caregivers of children with persistent asthma aged 4–17 years.²⁶ In a subjective assessment of their children’s asthma control status, the majority of caregivers participating in the study reported that their children had mild or no symptoms and that the level of asthma control had been maintained or even improved since the pandemic.

Papadopoulos et al.’s study²² of asthmatics (N = 1054) and non-asthmatics (N = 505) aged 4–18 years from 15 countries reported the following rates of asthma control during the pandemic: 90.2% improved or unchanged, 9.8% worse, and 65.9% improved. Notably, one in every three children with asthma (33.2%) reported an improvement in control that exceeded the test’s minimal clinically significant difference.

A study conducted in Spain among asthmatic children under the age of 18 at Nio Jess University Children’s Hospital found that every item assessed to measure asthma control according to GINA improved between March and June 2020 when compared to the same period in 2019, with significant improvements in daily symptoms and activity limitation (p < 0.01).²⁷

Taytard et al.′s study²⁸ was conducted in France at Trousseau University Hospital. The authors retrieved 3419 files of children with persistent asthma referred from the first, third, and fourth quarters of 2019 (1871 files) and 2020 (1548 files). The median (IQR) age of the entire population (2165) was 9.7 years (6.8; 13.1). When compared to the fourth quarter of 2019, asthma was better controlled during the same period in 2020 (a more relaxed lockdown occurred from the end of October to mid-December 2020.) In Turkey, Yucel et al.²⁹ also examined childhood asthma control (N = 84), noting that the improvement of ACTs coincided with the lockdown to limit the spread of COVID-19 (p < 0.001).

In conclusion, asthma control enhanced during the lockdown, likely as a result of reduced exposure to common asthma triggers brought on by the confinement. Additionally, some patients’ response to the maintenance therapy increased because of symptoms or fear and anxiety associated with the COVID-19 pandemic, whereas other patients’ response decreased because of symptoms or probably effective disease control.

Asthma exacerbation

Six studies included in our review assessed asthma exacerbation (Table 3). Fan et al.²⁰ reported that during the COVID-19 pandemic, most pathogens and air pollutants decreased. The frequency of severe asthma exacerbations in children was positively correlated with respiratory infections but not with air pollutants. Moreover, Hurst et al.¹⁵ investigated the effects of stay-at-home and social-distancing measures on asthma exacerbation rates during the first year of the COVID-19 pandemic. Asthma exacerbations in their study necessitated medical attention, SARS-CoV-2 testing and results, and antibiotic prescriptions. The authors noticed a slight increase in asthma exacerbation rates that corresponded with the timing of reopening orders, implying that reduced social distancing could have been a factor in these rates.

In another study, Ochoa-Avilés et al.⁷ held monthly follow-ups with parents and guardians for a 12-month post-study period, either in person or by phone, to record the occurrence of asthma exacerbations and symptoms. The asthma exacerbation outcome was measured by the number of parentally reported acute asthma attacks or wheezing episodes accompanied by respiratory distress. The researchers discovered that the number of reported asthma exacerbations did not change significantly with lockdown measures when compared to before such measures were enacted (p = 0.252).

In Ferraro et al.’s research, the authors examined asthma exacerbations (AEs), which are defined as an increase in asthma symptoms that necessitates at least 3 days of oral steroids. They found that AEs decreased in March/April 2020 compared to the same period in the preceding year (p = 0.095).

Taytard et al.²⁸ defined moderate exacerbations as acute asthma symptoms that required at least 2 days in a row of relievers, while severe exacerbations required at least 3 days of oral corticosteroids. Compared to 2019, the proportion of children with at least one exacerbation in the previous 3 months was significantly higher in 2020 before the lockdown (p = 0.022) but lower after reopening (p = 0.0001). In addition, Yucel et al.²⁹ reported that asthma exacerbations were reduced (p < 0.001) when compared to the same period in the previous year 2019.

Psychological effects and caregivers’ concerns

Five of the included studies discussed the psychological effects of the COVID-19 pandemic on asthmatic children. Caveney et al.³⁰ investigated the impact of the pandemic on families with children who had persistent asthma, while also examining caregiver concerns. According to the COVID-19 survey questions administered to 93 caregivers of children with asthma, aged 3–12, more than half (>50%) of the parents restricted their child’s physical activity to prevent asthma symptoms. Anxiety about COVID-19 was linked to activity limitations, financial hardship, difficulty obtaining asthma medications, and nocturnal asthma symptoms.

Clawson et al.³¹ examined the different psychosocial impacts of COVID-19 using focus groups comprised of 278 parents of both asthmatic and healthy children. In this study, the authors divided the participants into four groups: (a) non-Hispanic White (NHW) parents of asthmatic children; (b) Black, Indigenous, and People of Color (BIPOC) parents of healthy children; (c) BIPOC parents of asthmatic children; and (d) NHW parents of healthy children (referent). In addition, COVID-19 resulted in increased parent-reported resource losses for both BIPOC groups and greater decreases in healthcare access for both asthma groups when compared to the healthy NHW group. Parents of asthmatic children from both BIPOC and NHW backgrounds expressed more concern about resource losses as a result of COVID-19–related illnesses.

Similarly, the focus groups (mothers of children with asthma) in Di Riso et al.’s study²³ reported having COVID-19–related fears and growing concerns as their children’s activities resumed after the lockdown. They also reported a general decline in their psychological wellbeing during the lockdown. In the authors’ analysis of the clinical sample, the multivariate regression model showed that a worsening of the mothers’ and children’s physical wellbeing was associated with a worsening of the children’s psychological wellbeing during the lockdown. Hence, special programs to assist caregivers of chronically ill children should be developed. The analysis revealed that the mothers of asthmatic children were more concerned about contagion than the mothers of non-asthmatic children, but there was no difference in psychological functioning between the two cohorts.

Ferraro et al.²⁵ evaluated psychological functioning during the lockdown in a subgroup of asthmatic children recruited through the completion of the Strengths and Difficulties Questionnaire (SDQ) – children’s version. The results revealed a significant positive correlation between the GINA test scores and SDQ emotional symptoms (r = 0.299), but no other significant correlations were found.

A study of outpatients aged 12–18 years, 125 with persistent asthma, and 98 healthy participants were included. In Cekic et al.’s study,³² the participants’ level of concern about COVID-19 was measured using a questionnaire. Further, asthmatic patients believed that COVID-19 could be transmitted more easily to them. Almost all asthmatic patients and controls claimed to follow the COVID-19 protection rules. Outside, both groups wore face masks and followed physical distancing guidelines. The level of concern about the patient’s health status and about being affected in their treatment was significantly higher than that of those who did not have asthma.

Discussion

Asthma is the most common non-communicable disease, affecting up to 4.4% of the world’s population. Its recurrent nature involves frequent hospitalizations and ED visits. Asthma exacerbation can be triggered by respiratory viruses, resulting in an increase in the severity of the infectious condition.¹² In the past, the coronavirus was thought to be a trigger for an asthma attack; the same assumption was true for the flu virus.¹⁵ However, with the novel coronavirus SARS-CoV-2, there is controversy about the putative role of asthma as a preexisting condition that can exacerbate disease progression and the impact of COVID-19 on asthmatic children.

We conducted this systematic review to assess the impact of the lockdown duringCOVID-19 pandemic compared with the same previous period on the number of PED visits, HR, AC, AE and psychological effects and caregiver’s concerns.

The number of PED visitors and HR dropped, and better medication adherence, avoidance of healthcare facilities due to COVID-19 concerns, improved air quality, decreased participation in sports and exercise, reduced exposure to outdoor aeroallergens, and reduced viral exposure as a result of schools and daycare facilities being closed are some of the potential causes of PED asthmatic attacks. Additionally, due to the possibility of COVID-19 exposure in medical settings, parents may not have brought their kids to PEDs. However, one study refuted that result.¹⁹ This could be due to the low socioeconomic status of the study populations, as well as the crowded living conditions and restricted access to medical treatment in some of the communities examined. Social isolation was less likely to occur in those areas, and even during the lockdown, the exposure to external allergens was probably not much decreased.¹⁹ The hospitalization rate could also be clarified by the caregivers’ fear of bringing their children to the hospital due to the risk of SARS-CoV-2 exposure.²⁵ Increased treatment adherence is another crucial factor in this rate.

The COVID-19 outbreak and its responses have had a significant impact on asthma control in this age group. Even the results of the c-ACT scores had different manifestation. However Asthmatic children in the reviewed studies reported generally satisfactory asthma control during the lockdown.^{12,25
–28,33} For instance, Papadopoulos et al. used a large sample size to demonstrate improved results. Jia et al.’s measure of good control was the proportion of participants with scores greater than or equal to 20. Yucel et al. use the ratio of a score of less than 20. In the follow-up studies, this issue needs to be dealt with. Overall, c-ACT results indicated that asthma symptoms decreased during the pandemic. In fact, both asthma control and increased treatment adherence were significantly improved during the COVID-19 pandemic compared to the preceding period.

Our review highlighted a significant reduction in AE among youth with asthma during lockdown. According to the short-term studies have confirmed a number of explanations for the dramatic decline in AE during the pandemic, which include better air quality; a change in health-seeking habits brought on by COVID-19 fear; disruptions in the delivery of healthcare; and less exposure to other viruses.

This analysis suggests that changes in health-seeking behavior due to fear of COVID-19, healthcare disruptions, and improved air quality are unlikely to explain a consistent and sustained reduction in asthma exacerbations by demonstrating a significant and sustained reduction in asthma exacerbations over 18 months (since the first lockdown), during periods with varied pandemic-related public health measures. More research is needed to design and develop rational interventions that will assures the low rate of asthma exacerbations continues after the COVID-19 pandemic.

One likely reason for these findings is the implementation of COVID-19 lockdown measures, such as school closings,¹³ which limited viral disease transmissions and reduced potential exposure to asthma triggers, including viral infections, outdoor allergens, and physical activities; another explanation is the reduction in air pollution brought on by the closure of industry and the decline in vehicle traffic.³⁴ Many studies have yielded real data that the lockdown prompted by the pandemic had a positive effect on this group of patients. However, staying at home may have exposed the children to toxic indoor settings more frequently.

Social factors must be taken into account, such as malnutrition, which is associated with an increase in COVID-19 infections,³⁵ in addition to the families’ socioeconomic level. Therefore, it is crucial that healthcare programs target these social groups to overcome these gaps and appropriately inform parents in order to improve world health.

Another explanation of our findings is that the treatment of asthma with inhaled corticosteroids, combined with better adherence and an increase in prevention over the years, has led to a reduction in episodes of respiratory failure, absorption, and allergy-related immune imbalances.²⁵ In addition, international asthma and allergy associations have been effective in rapidly producing and publishing COVID-19 guidelines that provide guidance to healthcare professionals regarding the management of asthma patients, as well as to reach the general public.^36,37 These actions can have a beneficial impact on asthma control and motivate patients to follow social-distancing protocols, thus minimizing the risk of contracting COVID-19.

We must remember that while clinical trials on children are not yet possible, their protection and immunity can only be achieved through the development of a COVID-19 vaccine for this age group.³ SARS-CoV-2 infection and severe disease manifestations are possible in children of all ages. Children are also vulnerable to the COVID-19’s downstream effects, which include social isolation and school disruption. The development of a pediatric COVID-19 vaccine has the potential to prevent disease, mitigate downstream effects, and allow children to re-engage in their world.

Vaccination may benefit children both directly and indirectly. In light of the recently published adult COVID-19 vaccine clinical trial results for safety and immunogenicity, children should be permitted to participate in clinical trials parallel to ongoing adult phase 3 clinical trials in a careful, methodical, and transparent manner.³⁸ Because of the ease with which the virus spreads in public environments, this vaccine is especially important for students returning to school. Stay-at-home directives have also had a significant negative impact on children and adolescents, including lower vaccination rates, postponed medical condition management, prolonged exposure to indoor air pollutants, and effects on mental health. Some children and young people’s overall asthma control may be improved by going back to school. Finally, it is important to note that there has not been much research on children, which is a problem that needs to be solved because the lack of data skews the study’s findings.

This review has a number of limitations: there is still a shortage of information about asthma and COVID-19 in children; the short duration of follow-up. In addition, there was significant heterogeneity across studies in this study, which could be attributed to different definitions of outcomes

Conclusions

Regarding the degree of disease control, the COVID-19 pandemic lockdown had a significant effect on children with asthma. The reduction in exposure to common asthma triggers brought on by confinement is probably what contributed to the improvement in the level of control during the lockdown. Some patients reduced their maintenance medication, probably because of the high degree of disease control. Overall, the results imply that better asthma control may have been attained through increased medication adherence motivated by improved asthma control awareness and decreased exposure to asthma triggers, particularly respiratory infections, PA, and outdoor allergens, as a result of the COVID-19 outbreak. Importantly, we noticed a marked decline in asthma flare-ups, which suggests that the pandemic’s effects helped children with asthmatic conditions.

The COVID-19 pandemic has presented caregivers with numerous difficulties related to social issues, access to healthcare, and fears and concerns about the health of their children who have persistent asthma. Caregivers were likelier to restrict their child’s physical activity to prevent symptoms, which could aggravate asthma and increase the need for medical attention, as they reported feeling more concerned about how COVID-19 might affect their child’s asthma. Despite the current pandemic, it is crucial to address caregiver concerns, assess the most effective preventive asthma treatment, and promote healthy physical activity when providing medical care to children with asthma.

Future research should seek to fully evaluate the specific factors that contributed to improved outcomes in children with asthma, particularly those that could be leveraged after the COVID-19 pandemic is over, such as the use of telehealth for care delivery.

Supplemental Material

sj-docx-1-phj-10.1177_22799036231197186 – Supplemental material for Impact of the COVID-19 on asthma control among children: A systematic review

Supplemental material, sj-docx-1-phj-10.1177_22799036231197186 for Impact of the COVID-19 on asthma control among children: A systematic review by Mai Hamadneh, Alaa Alquran and Rami Manna in Journal of Public Health Research

Footnotes

Author contributions

Conceptualization, M.H. and A.A.; Search protocol, A.A. and M.H.; Quality Assessment, A.A. and RM.; Writing-Original Draft Preparation, M.H., A.A., RM; Writing-Review & Editing, M.H. and A.A.

Declaration of conflicting interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) received no financial support for the research, authorship, and/or publication of this article.

Institutional review board statement

The study did not require ethical approval.

ORCID iD

Alaa Alquran

Supplemental material

Supplemental material for this article is available online.

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