School Exposure and Asthma

Abstract

Objective

Exposure to indoor allergens and pollutants is associated with worsened asthma morbidity. Previous research has examined indoor exposures in the home environment, but evaluation and understanding of the school environment is also needed. The objective of this article is to provide a comprehensive overview of common school exposures and the association between school exposures and pediatric asthma morbidity.

Data Sources

A comprehensive literature review was performed using PubMed scientific search engine.

Study Selections

Full-length, peer-reviewed studies published in English were considered for review. In vivo, in vitro, and animal studies were excluded. Studies of school exposure to cockroach, mouse, dust mite, dog, cat, molds, pollution, and endotoxin associated with asthma and asthma morbidity were considered.

Results

The current literature establishes an association between school exposure and pediatric asthma morbidity. There is a need for ongoing research to evaluate the effects of school-based environmental interventions on asthma morbidity.

Conclusion

It is evident that the indoor school environment is a significant reservoir of allergens, molds, pollutants, and endotoxin, and that there is a relationship between school exposure and pediatric asthma morbidity. School-based interventions have the potential for substantial individual, community, and public health benefit. It is important that researchers continue to study the health effects associated with school exposures and assess cost-effectiveness of multifaceted school-based interventions.

Introduction

Asthma is one of the most common chronic conditions seen in pediatrics, affecting more than 6 million children in the United States.¹ Asthma prevalence is higher among pediatric patients and minority and low income groups.¹ Asthma results in significant impact to patients’ health and quality of life, and comes with a substantial economic burden.² Children with asthma have higher healthcare utilization including higher rates of ED visits, hospitalizations, outpatient visits and prescription drugs compared with school-aged children without asthma.³

Exposure to indoor allergens and pollutants play a role in the development of atopic diseases including asthma, allergic rhinitis, and atopic dermatitis. This exposure and subsequent sensitization to indoor allergens is a risk factor for asthma control.⁴ Past studies have demonstrated that more than 80% of school-aged children with asthma are sensitized to at least one indoor allergen and that sensitization is a predictor of asthma persistence in later life.^{5, 6} The timing of sensitization is an important factor as a recent study demonstrated that younger aeroallergen sensitization was associated with increased asthma risk in later childhood.⁷ The location of exposure is also an important factor. Early research in this field focused on the home environment and asthma and found an association between environmental exposures in the inner-city home environment and childhood asthma morbidity.⁸ In recent years, research has expanded to consider exposure in schools and daycares, as children spend between 7 to 12 hours per day in this setting.^9–11 The classroom represents an occupational model for children and exposures in this environment have significant health effects.

In this article we discuss common school exposures and the association between exposures and pediatric asthma morbidity. A comprehensive literature review was performed in PubMed assessing school exposure and asthma. Full-length, peer-reviewed studies published in English were considered for review. In vivo, in vitro, and animal studies were excluded. Exposures of interest for the review included: cockroach, mouse, dust mite, dog, cat, molds, pollution, and endotoxin.

The School Environment

Cockroach

Cockroach is an important indoor allergen, especially in urban areas. The major cockroach allergens are Bla g 1 and Bla g 2. Rosenstreich et al. in a landmark study demonstrated that children sensitized and exposed to high levels of cockroach in inner-city homes had increased asthma morbidity.⁸ Furthermore, Amr et al. documented a significant positive correlation between cockroach exposure in the school and asthma prevalence.¹² In the urban school setting in the United States the prevalence of cockroach allergen has differed across studies. A group of early studies documented high prevalence of cockroach allergen in schools,^{9, 12, 13} and demonstrated that between 66–71% of dust samples from classrooms had detectable cockroach allergen. ^{9, 12} The highest levels of cockroach allergens were in teachers’ lounges, cafeterias, second grade classrooms, and kindergarten classrooms.¹² Although cockroach allergen was detected in schools, the median or mean concentrations were below the defined threshold effect associated with asthma symptoms (8 U/g).⁸

In contrast to these early studies, more recent studies in urban schools have found low to undetectable cockroach levels. The School Inner-City Asthma Study (SICAS 1) was a NIH/NIAID funded comprehensive prospective study of classroom and school specific exposures and asthma morbidity among students in urban schools in the Northeast, adjusting for exposure in the home.¹⁴ In this study measured levels of cockroach allergen (Bla g 2) were found to be undetectable to very low in the dust samples from both schools and homes.¹⁰ For those schools with detectable levels, the mean concentration of Bla g 2 did not exceed the threshold level associated with asthma.¹⁰ The finding of low cockroach levels in urban schools has been consistent in multiple SICAS studies.^{10, 15, 16} Additionally, a study assessing early childhood education centers in Arkansas reported undetectable levels of cockroach allergen (Bla g 1 or Bla g 2) in classrooms.¹⁷ The differences in cockroach allergen levels in schools may be due to the fact that allergens levels vary by location even within a city, by race/ethnicity, and by gradation in poverty levels.¹⁰ Despite these differences, no study has identified median or mean concentrations above the defined threshold effect associated with asthma symptoms.⁸

Mouse

Mouse allergen exposure is also an important indoor allergen in urban areas. The major mouse allergens identified are Mus m 1 and Mus m 2. Mouse allergen exposure in the inner-city home environment has been linked to higher asthma morbidity.^{18, 19} Recent studies have focused on the school environment given the significant amount of time children spend in the school setting. These studies have found that mouse allergen, not cockroach allergen, was the primary school based allergen.^{10, 15, 20} Studies by the SICAS research team have consistently detected higher levels of mouse allergen in schools compared to levels in the same students’ home environment,^{10, 14, 15} and that levels of mouse allergen in the school setting were similar to those seen in occupational laboratory animal settings.^{10, 21} Mouse allergen levels in inner-city schools were found to be higher when mouse droppings were seen in the classroom and lower in classrooms where there was no evidence of mice.²² That said, even within classrooms with no evidence of mice, there was still evidence of significant mouse allergen exposure exceeding the level linked to an increase in asthma symptoms and healthcare utilization.²² A recent study by Sheehan et al. demonstrated that exposure to mouse allergen in schools is associated with increased asthma symptoms and decreased lung function in inner-city children with asthma.²³ Given the prevalence of mouse exposure in the school setting and its association with asthma morbidity, additional research is needed to determine if reducing allergen exposure in mouse sensitized children results in improvements in asthma morbidity. The School Inner-City Asthma Intervention Study (SICAS 2), a NIH/NIAID randomized controlled clinical trial using environmental interventions modeled from successful home-based interventions, is currently underway with health outcomes results pending.²⁴

Dust mite

Dust mite allergens (Der f 1, Der p 1) are microscopic arthropods found in dust and products with woven material and have the propensity to thrive in humid, warm environments.²⁵ The suggested threshold level for sensitization to dust mite allergen is >2μg/g and for asthma symptoms is >10μg/g.^{4, 25} There is debate whether dust mite allergen exposure is associated with asthma development as some studies have demonstrated an association,^{5, 26} and others have not.^{27, 28} However, for children sensitized to dust mites, there is sufficient evidence of a causal relationship between exposure to dust mite allergen and exacerbations of asthma.²⁹

Dust mite levels in the school setting have been found to be similar or slightly lower than the corresponding levels in the home environment.³⁰ There is wide variation in dust mite allergen levels in the school setting, with the highest levels in the daycare center found in carpeted areas during the day when the center was occupied.³¹ However, the mean or median concentrations of dust mite allergens levels in school have not exceeded the previously determined threshold level associated with asthma symptoms.^{10, 11, 15, 16, 25} A direct association of dust mite allergen exposure in the school setting and asthma morbidity has not yet been identified.

Dog and Cat

Dogs and cats are the most common animals kept as domestic pets and often thought of as a member of the family. Can f 1 is the major dog allergen and Fel d 1 is the major cat allergen. These allergens can be carried on small airborne particles and adhere well to clothing and upholstery. The threshold allergen levels associated with sensitization are >1 μg/g for cat and >2 μg/g for dog, and the threshold levels associated with asthma symptoms in sensitized individuals are > 8 μg/g for cat and >10 μg/g for dog.^{32, 33} Pet ownership is of considerable interest at this time given its unclear role in the pathogenesis of asthma, with many factors to consider including the age at exposure, amount of allergen exposure, and sensitization status. However, for individuals already sensitized, exposure to cat and dog allergens are of significant concern and associated with asthma morbidity.^{29, 34}

Exposure to Can f 1 and Fel d 1 can occur in the home, school, and public spaces.^{32, 33, 35} Multiple studies have detected cat and dog allergens in the school and daycare settings. Within these studies, dog and cat allergen levels have been found to vary widely, with higher levels in carpeted and upholstered areas.^{12, 33, 35} Additionally, studies have found that cat and dog allergen levels are higher in schools than in homes where no pets are present, and levels have been found to exceed threshold value associated with sensitization.^{11, 32, 33, 36} Past SICAS studies have demonstrated that cat and dog allergens were commonly detected in schools, but the absolute levels were relatively low and below the levels associated with asthma symptoms.^{10, 15, 23} These findings were potentially due to the low prevalence of household pet owners in the inner-city setting,²³ as the number of pet owners is one of the strongest predictors of elevated cat and dog allergen levels in schools.^{11, 37}

Pet allergen exposure in schools has been demonstrated to be associated with increased asthma morbidity. A study by Almqqvist et al. demonstrated that cat allergen was transported into schools and that this indirect exposure may be associated with worsening of asthma for students with cat allergy.³⁴ An early study by Lonnkvist et al., demonstrated higher concentrations of cat and dog allergens in schools compared to homes, and found that in children with mild asthma and animal dander allergy there was a significantly increased bronchial sensitivity to methacholine after one school week.³⁸ It was thought that the effects seen may be related to continuous exposure to animal allergens; however, this was not causally linked.³⁸

Mold

Molds are known to grow in moist, warm environments and exposure occurs via multiple routes including inhalation, skin contact, or ingestion. Fungal exposures in the home are associated with increased risk of asthma and asthma morbidity.^{39, 40} In a systematic review, Mendell et al. demonstrated that indoor dampness or mold was consistently associated with increased asthma morbidity.⁴⁰ Threshold allergen exposure levels associated with asthma symptoms in sensitized individuals is not known and these levels will vary between different fungal species. Additionally, it is important to note that fungi are potent immunomodulators and have effects on asthma independent of their potential to act as antigens.⁴¹

The school is a unique microenvironment also at risk for development of mold. The Health Effects of Indoor Air Pollutants (HITEA) research group in Europe demonstrated high levels of mold in schools, especially those with moisture damage.^{42, 43} In the United States, Baxi et al. demonstrated that schools are a source of mold exposure and that visible mold may be a predictor for higher mold spore counts.⁴⁴ Furthermore they found that the classroom microenvironment varies in quantity of fungal spores and species among classrooms within the same school.⁴⁴ Variation in the environment would also be expected between schools, school districts, regions, and countries given different climatic and cultural conditions.⁴³ Studies have also found an association of mold in a classroom environment and asthma morbidity.^{45, 46} Chen et al. demonstrated that classroom Aspergillus/Penicillium and basidiospores were found to be associated with childhood asthma and asthma with symptoms reduced on holidays.⁴⁵ Holst et al. showed that high classroom dampness in Danish schools was associated with increased wheezing and decreased spirometry in exposed students.⁴⁶ Research is now focused on the diversity of mold exposure and there is growing evidence that exposure to a wide diversity of mold species may actually be protective against atopy development.⁴⁷ That said, these findings should not influence the need for fungal remediation in identified high risk homes or schools. Additional studies are needed to determine if reducing mold exposure in the school setting will results in improvement in asthma morbidity.

Indoor Air Pollution and Air Quality

Air pollution is an important modifiable factor associated with asthma. Exposure to indoor air pollution is associated with risk of asthma development⁴⁸ and increased asthma morbidity.⁴⁹ In the school setting, pollutant exposures includes particulate matter (PM), nitrogen dioxide (NO₂), black carbon (BC), ozone (O₃), bioaerosols, volatile organic compounds, carbon dioxide, and others which can adversely affect the indoor air quality of schools.⁵⁰ Annessi-Maesano et al. demonstrated that about one third of school children were exposed to high concentrations of air pollutants in the classroom as defined by the World Health Organization for PM2.5 and NO_2.⁵¹

Traffic pollution is an important source of exposure in the school as many schools are in close proximity to a major roadway⁵² and that schools also serves as pick up and drop off locations, with frequent idling of cars and buses.⁵³ Other factors that influence the indoor air quality of schools are related to the built environment including ventilation and building maintenance.⁵⁴ Additionally, classroom activity has been found to re-suspends indoor air particles thereby increasing exposure.⁵⁵ In a SICAS study, Gaffin et al. assessed the relationship between indoor and outdoor levels of PM_2.5 and BC, and demonstrated a relationship between measured indoor classroom levels of PM_2.5 and BC and outdoor levels.⁵⁶ Furthermore, using mixed effects modeling, it was demonstrated that the classroom was an important source of PM_2.5 exposure for children and suggested that indoor sources contribute to PM_2.5 exposure.⁵⁶

Few studies have evaluated the association of school based pollutant exposure and asthma morbidity. Gaffin et al. demonstrated that indoor classroom exposure of NO₂ was associated with airflow obstruction in children with asthma.⁵⁷ In a panel study, Yoda et al. demonstrated that increased indoor levels of O₃ in schools were associated with a significant decrease in peak expiratory flow and FEV₁ in children with asthma.⁵⁸ There is minimal data related to the impacts of school-based intervention on indoor air quality and health outcomes. An early study by Pilotto et al. demonstrated that an intervention replacing unflued gas heaters with electric heaters in schools reduced NO₂ levels and improved asthma symptoms.⁵⁹ A pilot study by Jhun et al. found that implementation of a classroom based air cleaner intervention resulted in significant reductions in of PM_2.5 and BC.⁶⁰ However, this study found no significant changes in FEV₁ or asthma symptoms between asthmatic children in the intervention group and controls.⁶⁰ Guerriero et al. sought to quantify the potential economic benefit of reducing indoor NO₂ levels in primary schools in London and demonstrated that reducing indoor school NO₂ exposure would lead to a reduction in 82 asthma exacerbations per year.⁶¹ The resultant estimated cost savings was between £2,500–60,000 ($3,392–81,413) per school dependent on perspective (£2,500 for child’s perspective and £60,000 for parent’s perspective).⁶¹ Further research is needed to assess the effect of school based pollution remediation on asthma morbidity.

Endotoxin

Endotoxin or lipopolysaccharide (LPS) is a component of the outer membrane of Gram-negative bacteria. Endotoxin exposure in the home environment has been associated with both the development of early childhood wheezing and increased asthma morbidity in children with asthma.^{26, 62} Endotoxin has been identified as an important exposure in the home, occupational, and school settings. Studies have documented that endotoxin levels are higher in schools compared to the corresponding home environment.^{63, 64} Endotoxin levels in the schools were found to be higher in lower grades and in higher occupancy classrooms, and these findings differed by country.⁶⁵ Sheehan et al. demonstrated that in the SICAS cohort inner-city children with asthma were exposed to higher concentration of endotoxin at school compared to home.⁶³ Additionally, Jacobs et al. found higher endotoxin levels in Dutch schools compared to home, and suggested that endotoxin exposure in the schools may be associated with non-atopic asthma symptoms.⁶⁴ Lai et al. demonstrated that classroom specific endotoxin levels frequently exceeded recommended occupational limits for adults.⁶⁶ In this SICAS cohort study, they demonstrated that higher school airborne endotoxin levels were associated with increased asthma symptom days in children with non-atopic asthma, after controlling for the home environment.⁶⁶ Further evaluation of mitigation strategies to decrease school related endotoxin exposures and asthma control is needed.⁶⁶

Multiple exposures

The indoor school environment is complex with many potential exposures that can influence asthma and asthma control. As multiple exposures occur simultaneously it can be challenging to know causal factors verse bystander effect. Banda et al. assessed the relationship of environmental exposures with asthma exacerbations and hospitalizations and demonstrated that having more than one classroom trigger increased the likelihood of worsened asthma morbidity in 5–11 year-old children.⁶⁷ Given this, it is imperative that studies assess multiple potential exposures in the home and school setting and build appropriate statistical models to account for these exposures.

Gene-Environment Interaction

Environmental exposure is an important aspect of asthma development and morbidity, but it is important to recognize that asthma is a complex disease with an intricate play between environmental factors and genetics. Gene-environment interactions play a critical role in asthma incidence and severity. Multiple gene-environment interactions have been identified in childhood asthma, but few studies have assessed the gene-environment interaction within the school environment. A recent study by Lai et al. demonstrated a gene-environment interaction between an interleukin 4 receptor genetic variant (IL4Rα-Q576R), school endotoxin exposure, and asthma.⁶⁸ This study demonstrated that the effect of classroom endotoxin levels on asthma symptom days varied by genotype and found that high classroom endotoxin levels were associated with increased asthma symptoms for the R/R genotype and less asthma symptoms for children with the Q/Q genotype.⁶⁸ This research demonstrates the importance of assessing the gene-environment interaction relating to school exposure and asthma, and further research in this area is needed.

Microbiome

There are other potentially modifiable exposures associated with asthma morbidity beyond the exposures discussed above. One factor that has been the focus of many recent studies is the relationships between the microbiome and allergic asthma. Advances in this field is related to the ability to rapidly identify microbes via next generation sequencing of 16S ribosomal rRNA gene sequences with linkage to large databases to identify bacteria.⁶⁹ There is great breadth of research assessing microbiota composition and the relationship with asthma. That said, the role of the microbiome in the school setting and its relationship with asthma it not fully understood. A recent study looking at archived environmental samples, demonstrated that microbiome sequencing is feasible in archived samples.⁷⁰ This offers the potential to assess how the microbial environment influences health from previously archived samples from public schools.⁷⁰ Additionally, the effect of school based interventions on microbiota composition is not well understood. A recent commentary raised the concern that the use of high efficiency particulate arrestance (HEPA) filters in the school setting may compromise environmental biodiversity.⁷¹ However, it is too early to know the effect of the HEPA filter intervention on environmental biodiversity, and this cannot be confirmed or refuted at this time. Further understanding of the effects of interventions on asthma morbidity is needed.

Environmental Intervention Strategies in the School

It is evident that the indoor school environment is a significant reservoir of allergens, molds, pollutants, and endotoxin, and that there is a relationship between school exposure and pediatric asthma morbidity. The studies highlighting school exposure and asthma morbidity are summarized in Table 1. To reduce school exposure and the associated health effects, multifaceted interventions in the schools are a promising proposition with hopes to provide long term benefit for those children with asthma. The cost-effectiveness of these interventions is not currently known. However, multifaceted school-based environmental interventions may offer benefit in controlling exposures in the school environment with the potential to help many children.⁷²

Several studies have investigated the effects of multifaceted intervention regimens in the home environment including education, thorough cleaning, use of HEPA filters, integrated pest management, and maintenance of these practices. Morgan et al. in a landmark study revealed that an individualized, home-based, multifaceted environmental intervention decreased exposure to indoor allergens, including cockroach and dust-mite allergens, leading to decreased asthma morbidity among inner-city children with atopic asthma.⁷³ Furthermore, a systematic review of 23 studies demonstrated that home-based, multi-trigger, multicomponent interventions with an environmental focus are effective in improving overall quality of life and productivity in children and adolescents with asthma.⁷⁴ In this systematic review, it was found that multi-trigger, multicomponent interventions in children were associated with decrease asthma morbidity as measured by asthma symptom days, asthma related missed school days, and healthcare utilization.⁷⁴ These and additional studies are highlighted in the recent article titled, “NIAID, NIEHS, NHLBI, and MCAN Workshop Report: The indoor environment and childhood asthma—implications for home environmental intervention in asthma prevention and management”.⁷⁵ Please see this comprehensive workshop report for further details regarding home interventions and implications for asthma prevention and mangement.⁷⁵

Successful home based strategies serve as the model for school-based interventions. In the school setting, there are a small number of studies looking at school-based environmental interventions and asthma morbidity. More research on school-based interventions and asthma morbidity is needed at this time. To optimally study school-based interventions there are many elements that must be considered prior to initiation: 1) Engagement and commitment from the patient and families who will take part in the interventions, 2) Engagement and commitment from the school system including senior school administrators, principals, teachers, school nurses, facilities management, and others, 3) Exposure information collected in the school and in the home environment, 4) Optimal study design with a prospective longitudinal randomized double-blind controlled trials, using sham interventions as controls, and 5) Implement interventions in a classroom setting in an unobtrusive way.^{14, 24} These elements present logistical challenges for implementation of school-based interventions; however, the potential benefits could impact a school or school system and reduce exposure for many children compared to individual’s families impacted by home-based interventions.

The next phase of SICAS, the School Inner-City Asthma Intervention Study (SICAS 2), is a NIH/NIAID randomized controlled clinical trial using an environmental intervention of classroom HEPA filters and school wide integrated pest management (IPM) to comprehensively determine health benefits on reducing asthma morbidity, adjusting for exposure in the home (ClinicalTrials.gov NCT02291302).²⁴ The study is ongoing and results are pending. The study will help determine efficient, cost-effective interventions for inner-city children with asthma in the school setting, since it may be possible to intervene in a community of children through the school environment as opposed to the individual level by intervening in the home.²⁴

Multifaceted interventions in the school environment are a promising approach to decrease exposure and improve asthma control. It is also important to recognize that no two schools are the same as they differ in region, climate, humidity, proximity to roadways and highways, ventilation, funding, maintenance, and multiple other factors. There is also great variability within the walls of the school as there are differences in classrooms, differences in children comprising each class, and heterogeneity with children’s type and severity of asthma. These factors are important to consider as a one size fits all approach to environmental interventions strategies may not be possible. That said, intervention programs do have the potential to reduce exposures in children with asthma and present an opportunity for individual, community, and public health benefit.

Conclusion

The school environment is where children spend a significant amount of their day, and this environment is a reservoir of multiple environmental exposures. It is imperative to continue to study the health effects associated with school exposures, including asthma. It is also important that health researchers continue to work to assess the impacts of school-based interventions and the cost-effectiveness of these interventions.

From a public health perspective, interventions at the school level have the potential to benefit students and faculty. Successful home based strategies serve as the model for school-based interventions and involve a comprehensive multifaceted approach. There are challenges in designing school-based intervention studies and there are significant costs associated with these studies. SICAS 2 is currently underway as a prospective randomized, blinded, sham-controlled school environmental intervention trial to determine the efficacy of a school-based intervention to improve asthma control. This study will help determine efficient, cost-effective interventions in the school setting for inner-city children with asthma. If effective, these interventions may be considered in other school environments in hopes to provide long-term benefit for children with asthma.

Table I.

School Environmental Exposure and Asthma Morbidity

Study	Population	Design	Population/School Size	Results
Sheehan et al.23 (2017)	Children with asthma (aged 4–13 y; US)	Prospective cohort	284 students enrolled from 37 inner-city elementary schools.	Mouse allergen levels higher in schools than in homes. Mouse allergen detected in 99.5% of school dust samples. Higher mouse allergen in schools was associated with asthma symptoms and lower FEV1.
Almqvist et al.34 (2001)	Children with asthma and cat sensitization (aged 6–12 y; Sweden)	Prospective	410 children enrolled from 5 pediatric allergy clinics.	Children in class with more cat owners had increased asthma morbidity after school started (decreased PEF and increased asthma symptoms, use of medications, and risk of exacerbation).
Chen et al.45 (2014)	Children (aged 6–15 y; Taiwan)	Cross sectional	6,346 (of 7,154) children with completed surveys from 44 schools.	Classroom Aspergillus/Penicillium and basidiospores correlated with current asthma and asthma with symptoms reduced on holidays or weekends (ASROH).
Holst et al.46 (2016)	Children (aged 6–10 y; Denmark)	Cross sectional	330 (of 417) children with completed surveys from 15 schools.	Classroom dampness was associated with lower lung function and a higher risk of wheezing. Microbial components driving the effect was not identified.
Gaffin et al.57 (2017)	Children with asthma (aged 4–13 y; US)	Prospective cohort	296 students enrolled from 37 inner-city elementary schools.	Indoor classroom NO2 level was associated with airflow obstruction.
Jacobs et al.64 (2013)	Children (aged 6–12 y; Netherlands)	Case Control	169 students (66 cases and 103 controls) from 10 schools.	Endotoxin levels higher in schools than in homes. Endotoxin in schools may be associated with non-atopic asthmatic symptoms.
Lai et al.66 (2015)	Children with asthma (aged 4–13 y; US)	Prospective cohort	248 students enrolled from 37 inner-city elementary schools.	Endotoxin levels higher in schools than in homes. School endotoxin exposure was associated with asthma morbidity for children with non-atopic asthma.
Lai et al.68 (2017)	Children with asthma (aged 4–13 y; US)	Prospective cohort	236 students enrolled from 37 inner-city elementary schools.	Classroom endotoxin levels on asthma symptom days varied by genotype (IL4R variant).

Abbreviations: US: United States; FEV₁: forced expiratory volume 1 second; PEF: peak expiratory flow; ASROH: asthma with symptoms reduced on holidays or weekend; NO₂: nitrogen dioxide.

Abbreviations

SICAS 1

School Inner-City Asthma Study

NIH

National Institutes of Health

NIAID

National Institute of Allergy and Infectious Disease

SICAS 2

School Inner-City Asthma Intervention Study

HITEA

The Health Effects of Indoor Air Pollutants

PM_2.5

particulate matter 2.5

NO₂

Nitrogen dioxide

BC

Black carbon

O₃

ozone

FEV₁

forced expiratory volume 1 second

HEPA

high efficiency particulate arrestance

IPM

Integrated pest management

NIEHS

National Institute of Environmental Health Sciences

NHLBI

National Heart, Lung, and Blood Institute

MCAN

Merck Childhood Asthma Network

CHILD

Canadian Healthy Infant Longitudinal Development Study