School Environmental Intervention Programs

Abstract

Exposure to indoor allergens and pollutants play a significant part in the development of asthma and its associated morbidity. Inner-city children with asthma are disproportionately affected by these exposures with increased asthma morbidity. While years of previous research have linked exposures in the urban home environment with significant childhood asthma disease, many of these allergens are also present in inner-city school environments. Therefore, evaluation of the school environment of patients with asthma is also essential. School-based environmental interventions may offer benefit for this problem and has the potential to help many children with asthma at once in a cost-effective manner. It is important that environmental health researchers continue to assess which interventions are most practical and result in the greatest measurable improvements.

Background

Exposure to indoor allergens and pollutants play a significant part in the development of atopic diseases, including asthma, allergic rhinitis, and atopic dermatitis. The degree of exposure to environmental allergens in addition to the atopic genetic predisposition of the individual influences the development of IgE (sensitization) and Th₂ responses. Classically, allergens cross-link preformed IgE on mast cells which leads to recruitment of Th₂ cells, basophils, and eosinophils, resulting in immediate and late allergic responses. There may be other biologic functions of allergens, however, that play a direct role in causing allergic inflammation, such as the involvement of allergen proteases¹ and the stimulation of pattern recognition receptors on epithelial cells,² to name a few. Studies indicate that more than 80% of school age children with asthma are sensitized to at least one indoor allergen and that allergic sensitization is a strong predictor of disease persistence in later life.^{3, 4} The timing of sensitization is also an important factor; Rubner and colleagues demonstrated that aeroallergen sensitization at younger ages was associated with an increased risk of asthma in later childhood.⁵ In addition, children are likely to become sensitized to the allergen that predominates in their local environment. Therefore, the effects of these individual allergens will vary depending on the socioeconomic status, weather, and geographical location, among the many factors.

While years of previous research have demonstrated the association between environmental exposures in the inner-city home environment and significant childhood asthma morbidity,^6–8 many of these allergens and pollutants are also present in urban school environments.^9–11 This is noteworthy since children spend 7 to 12 hours per day in school and daycare settings, representing an occupational model for children. The common indoor allergens include house dust mites, cockroach, rodents, furry pets such as cat and dog, and molds. Previous studies have identified unique inner-city allergen exposures in homes and schools as important risk factors for asthma morbidity,^{8, 12, 13} namely mouse and cockroach allergens, and demonstrated that interventions to reduce home exposure improve asthma outcomes.¹⁴ As such, several studies have investigated the effects of multifaceted intervention regimens in homes which include education, thorough cleaning, use of high-efficiency particulate arrestance (HEPA) filters, integrated pest management (IPM), and maintenance of these practices.^{14, 15} The environment outside of the home, especially in the United States (U.S.), is less well understood though. Literature reviews have discussed the limited school-based environmental intervention studies to date in the U.S. and highlight the need for them.^16–18 As a consequence, successful home-based strategies currently serve as the prototype for school-based environmental interventions.

In this article, we discuss common exposures encountered in schools, especially in urban areas where asthma morbidity and mortality is highest among children.¹⁹ We review the association between school environmental exposures and pediatric asthma morbidity. Additionally, we review school-based asthma management programs and environmental control and intervention strategies intended to improve asthma morbidity in the pediatric population.

The Importance of Indoor Environmental Exposure Control

The indoor environment is a significant reservoir of various exposures (allergens, pollutants, bacteria and viruses) with the ability to affect the development of asthma and its associated morbidity. This is supported by observational epidemiologic studies which identified early-life allergen exposures as risk factors for early allergic sensitization and the subsequent development of asthma.^{20, 21} It is difficult to know, however, whether environmental control methods have a role in the primary prevention of asthma; the results of several primary prevention trials have been mixed.^{3, 22, 23} Despite these findings, a Cochrane meta-analysis estimated that environmental control practices reduced the risk of current asthma by approximately 30–50% in children.²⁴ Therefore, while primary prevention is a goal we hope to attain, controlling environmental asthma triggers is beneficial for those with current asthma.

It is important that patients with asthma take all the essential actions recommended to reduce their exposure to indoor environmental asthma triggers.^{25, 26} A priority message from the National Asthma Education and Prevention Program (NAEPP) Expert Panel Report 3 guidelines for the management of asthma is that for any patient with persistent asthma, the clinician should: 1) identify allergen exposures; 2) use skin testing or in vitro testing to assess specific sensitivities to indoor allergens; and 3) implement environmental controls to reduce exposure to relevant allergens.²⁷ Healthcare providers have a responsibility to ask about environmental exposures and to ensure that patients have the knowledge and resources to implement environmental control measures. Low-cost environmental interventions are a reasonable first start with costly interventions reserved for after an allergy consultation is completed. Strategies for allergen avoidance should include a comprehensive targeted environmental control strategy which takes into account the patient’s sensitizations and exposures. It should be considered the first line of therapy for patients with indoor allergen sensitivities.

While the home environment is important, consideration should be given to other places where the child spends time such as schools and daycares. It has been shown that schools can be a source of allergen exposure connected to asthma morbidity.¹² School-based environmental interventions may offer benefit for this problem and has the potential to help many children with asthma at once. A U.S. school-based environmental intervention study is currently underway to help answer this question, employing pest management techniques and high efficiency particulate arrestance (HEPA) air filters.²⁸

The School Environment

Indoor Allergens

Historically, the prevalent allergens discovered in inner-city home environments have been cockroach and mouse allergen,^{8, 29–33} both of which are also linked to higher asthma morbidity.^{8, 34, 35} These findings have translated to the urban school environment in the U.S. where the majority of school studies examining cockroach and mouse allergen levels have been conducted.^{9, 10, 36, 37} The School Inner-City Asthma Study (SICAS) is a National Institute of Health (NIH) and National Institute of Allergy and Infectious Disease (NIAID) funded, comprehensive, prospective study of inner-city school and classroom-specific exposures and asthma morbidity among students in the Northeastern U.S., adjusting for home exposures.³⁸ The SICAS results demonstrated substantial levels of mouse allergen in school classrooms compared to the same students’ homes,¹⁰ with exposure to mouse allergen in schools associated with increased asthma symptoms and decreased lung function.¹² Interestingly, cat and dog allergen levels were lower in these SICAS inner-city schools when compared to European school-based studies showing higher levels, likely due to passive transfer from students who owned pets in their homes.^{39, 40} Levels of cockroach and dust mite allergens were undetectable to very low in SICAS dust samples from both schools and homes. In contrast, school-based studies performed in southeast Texas, Baltimore and Manchester, England found detectable levels of cockroach allergen in all schools , suggesting that cockroach allergen levels vary by location even within a city, by race/ethnicity, and by gradation in poverty levels.^41–43 Moreover, both cockroach and dust mites require high humidity and warmth to survive. This highlights how geographic, socioeconomic, climatic, and cultural differences might influence the prevalence of allergens in varying environments.

Mold

Classroom activity leading to resuspension of particles, inadequate building maintenance, poor ventilation, and ambient air pollution taken together lends itself to a distinctive microenvironment of indoor particles and pollutants on which mold and allergens can be carried. The Health Effects of Indoor Air Pollutants (HITEA) research group in Europe demonstrated high levels of mold in schools, especially those with moisture damage.^{44, 45} These findings substantiate the results from the U.S. based SICAS, which found elevated levels of classroom mold in settled and airborne dust.⁴⁶ The HITEA research group recently showed that the immunotoxicological potency of settled dust samples collected from European schools differs largely between geographical locations and is likely influenced by moisture damage of the school buildings.⁴⁷ Further studies are needed to evaluate the association between immunotoxicological exposure from settled dust and respiratory health effects in children. Holst and colleagues showed that high classroom dampness in Danish schools was associated with increased wheezing and decreased spirometry in exposed students.⁴⁸ A Taiwanese study illustrated that mold exposure in classrooms correlated with asthma symptoms and a relief of symptoms on weekends and holidays, further supporting an occupational model for children.⁴⁹ In younger children, mold exposure in daycare centers was also associated with wheezing.⁵⁰ Finally, new research provides evidence that exposure to a wide diversity of mold species may actually be protective against atopy development.⁵¹ In a recent study, Rufo et al. showed that classrooms with increased fungal diversity scores showed a significantly lower prevalence of children with atopic sensitization, but not asthma.⁵² More studies are needed to evaluate the role of fungal diversity on the development of allergic diseases.

Endotoxin

Endotoxin is a component found in the outer membranes of gram-negative bacteria. It is associated with the presence of pets, rodents, dampness and mold. Endotoxin exposure has been linked to airway inflammation, early wheezing and asthma morbidity.^{53, 54} While the majority of studies have evaluated the effects of home and occupational endotoxin exposure on asthma, both U.S. and European school-based studies indicate that children with asthma are exposed to higher concentrations of endotoxin in their classrooms compared to home.^{55,56, 57} Lai et al. demonstrated in the SICAS cohort that inner-city children with asthma are exposed to high levels of classroom airborne endotoxin levels.⁵⁸ Moreover, after adjusting for home exposures, classroom endotoxin exposure was associated with an increase in asthma symptom days for children with non-atopic asthma. Alleviating school-related endotoxin exposures may be a way to lessen asthma morbidity in urban children.

Geographic Information System, Indoor Air Pollution and Air Quality

A growing body of work demonstrates that concentrations of many pollutants are higher indoors than outdoors,⁵⁹ and higher in urban settings when compared to rural ones.⁶⁰ Unlike the home environment, schools have fewer indoor sources of pollutants since most schools don’t have active cooking and smoking is prohibited. However, traffic pollution is an important source of particulate matter (PM), nitrogen dioxide (NO₂) and black carbon which can penetrate indoors and adversely affect the indoor air quality of schools.⁶¹ Gaffin et al. investigated the relationship of indoor to outdoor PM in the SICAS inner-city school classrooms. Using mixed effects linear models, they showed that the classroom was an important source of PM_2.5 and that the penetration of outdoor PM_2.5 particles varied by school.⁶² Another recent study from this group demonstrated that in children with asthma, indoor classroom NO₂ exposure was highly associated with an increase in airflow obstruction.⁶³ Other factors fueling the poor indoor air quality of schools are reduced ventilation,^{64, 65} inadequate building maintenance,⁶⁶ and exposure to janitorial cleaning products and the by-products of heating and cooling systems. The relationship between air pollution and asthma morbidity in children is well established.⁶⁷ Exposure to indoor pollutants is independently associated with increased respiratory symptoms and rescue asthma medication use in urban children with asthma.⁶⁸

In recent years, the ability to locate residences in space and obtain geocodable health data coupled with the use of geographic information system (GIS) has given researchers the enhanced ability to link exposure information to individual addresses. Most environmental exposure and health studies in patients with asthma use exposures averaged over the course of a day and do not take into account the spatial/temporal variability that likely occurs as a person moves from home, into transportation, and then school and work microenvironments. For instance, schools are typically centrally located within a community in close proximity to highways, heavy traffic routes, and commercial and industrial buildings. School locations also serve as a site for drop-off/pick-up, idling of cars, bus stops, potentially contributing to an increase in ambient air pollution. Kingsley et al. showed that approximately 3.2 million (6.5%) children across the United States attended schools located within 100 meters of a major roadway defined by the United States Census Bureau.⁶⁹ Air pollutants that are found near busy roads as a product of traffic exhaust, such as NO₂ and PM, have been shown to be associated with respiratory illness in children,^{70, 71} and the use of GIS has provided evidence that living in proximity to traffic increases the incidence of asthma⁷² and risk of exacerbations in both children and adults.⁷³

School-Based Asthma Management Programs

A number of national, state, and city governmental organizations such as the American Lung Association, Allergy and Asthma Foundation of America, National Heart, Blood and Lung Institute, the Center for Disease Control and Prevention’s National Asthma Control Program, and the U.S. Environmental Protection Agency (EPA) have developed a number of school-based asthma programs. The EPA created the Indoor Air Quality Tools for Schools Program with the aim of improving environmental conditions in schools. It provides recommended actions for teachers, facilities staff and school officials such as keeping ventilation units in classrooms free of clutter, reducing the number of items made of cloth in the classroom, removing classroom pets that cause allergic reactions or trigger asthma attacks in students, and reporting maintenance problems in classrooms immediately. These measures should be taken until more widespread multifaceted school intervention strategies are implemented. Additionally, the School-Based Asthma Management Program (SAMPRO™)⁷⁴ and the Centers for Disease Control and Prevention (CDC) Healthy Schools Program offer toolkits to schools. These toolkits help to develop asthma-friendly schools that provide appropriate school health services for students with asthma and a safe and healthy school environment to reduce asthma triggers. Moreover, it has been shown that state asthma programs play an important role in implementing multi-component, school-based asthma interventions due to their access to statewide asthma surveillance data, ability to translate policies into action, provide resources, and form connections between schools and community stakeholders.⁷⁵

In addition to these programs, school-based health centers (SBHCs) have been created to provide an ideal setting in which to incorporate environmental components into existing chronic disease programs. There are over 2,000 SBHCs throughout the country serving an ethnically diverse population of more than 2 million children, primarily in low-income areas. A large number of these centers offer asthma management. SBHC staff members can play a role in maintaining healthy indoor environments in school by increasing awareness, facilitating an indoor air quality assessment, or implement specific interventions to address mold, dust mites, pests, pets, and ventilation.

Environmental Control and Intervention Strategies in Schools

There is a paucity of thorough data on school-based environmental interventions and health outcomes; the few studies that have been published are small and not adequately powered to comprehensively assess asthma morbidity outcomes and are summarized in Table I.^76–81 In an effort to reduce pet dander in schools, dedicated school clothing and banning pet ownership in Swedish schools showed that airborne cat allergen levels were on average 4–6 times lower in classes with school clothing or pet ownership ban compared with control classes.⁸¹ This particular school environmental intervention strategy may not be practical in the U.S., however. Other allergen avoidance measures such as removal of upholstery and curtains, increased cleaning, and replacement of bookshelves with cupboards to lessen allergen load offered no significant change in Swedish classroom cat allergen levels.⁸² There are 2 small longitudinal studies in Finland that showed improvement in asthma symptoms through reparation of air filtration systems and moisture damage in schools, and reduction in mold exposure and other building maintenance.^{79, 80} These studies are limited by the small number of schools that were studied. In one Australian school study, an intervention replacing unflued gas heaters with electric heaters effectively reduced NO₂ levels and improved asthma symptoms.⁷⁶

Table I.

School Environmental Intervention Studies

Study	Population	Design	Population/School Size	Intervention	Effectiveness of Intervention
Pilotto et al.76 (2004)	Children with asthma from primary schools (mean age 8–9 y; Australia)	Randomized control trial	18 schools, 10 control and 8 intervention schools 118 children, intervention group 45, control group 73	Replacement flued gas or electric heaters in schools	Reduction in NO2 exposure Reduction in asthma symptoms
Jhun et al.77 (2017)	Children with asthma (aged 6–10 y; US)	Randomized control trial (Pilot Study)	3 schools, 9 control and 9 intervention classrooms 25 children, intervention group 12, control group 13	Classroom based HEPA air cleaner intervention	Reductions in PM2.5 and BC Modest improvement in peak flow, no significant changes in FEV1 and asthma symptoms
Bernstein et al.78 (2005)	US	Randomized control trial (Pilot Study)	Day care A: 8 rooms Day care B: 6 rooms Intervention installed in half the rooms of each day care	Dehumidification plus day care room based HEPA air cleaner	Lower average dew point from baseline for both day care A and B Reduction in fungal spore counts for day care A only
Lignell et al.79 (2007)	Children (aged 7–12 y; Finland)	Longitudinal intervention study	1 Moisture damaged school 1 Non-damaged school Over 2,400 children returned surveys	Damaged school renovated for all identified problems, mechanical exhaust and supply air ventilation system installed	50% reduction in fungal concentrations Modest reduction in respiratory symptoms
Meklin et al.80 (2005)	Children (aged 6–17 y, Finland)	Longitudinal intervention study	2 Moisture damaged schools 2 Non-damaged schools Over 1,300 children returned surveys	Damaged schools thoroughly cleaned, repaired, and renovated, mechanical exhaust and supply ventilation system installed	Normalization of indoor air fungal concentrations Reduction in respiratory and other symptoms
Karlsson et al.81 (2004)	Sweden	Intervention study	3 schools, 6 classrooms in total, 3 control and 3 intervention classrooms from each school	1 class of children with no pets, 2 classes of children who changed into special school clothing upon arrival	4-fold to 6-fold lower airborne cat allergen levels in intervention classes compared with control classes

Abbreviations: NO₂, nitrogen dioxide; HEPA, high efficiency particulate arrestance; PM_2.5, particulate matter 2.5; BC, black carbon; FEV₁, forced expiratory volume in 1 second; US, United States

In a landmark study, Morgan and colleagues revealed that among inner-city children with atopic asthma, an individualized, home-based, multifaceted environmental intervention decreased exposure to indoor allergens, including cockroach and dust-mite allergens, leading to decreased asthma morbidity.¹⁴ As such, several studies have investigated the effects of multifaceted intervention regimens which include education, thorough cleaning, use of HEPA filters, integrated pest management, and maintenance of these practices.^{14, 15, 83} The term “multifaceted” has been used to describe interventions directed toward more than one asthma trigger or interventions with more than one component. Given the paucity of comprehensive data on school-based environmental interventions and health outcomes, these successful home-based strategies currently serve as the model for school-based interventions. For instance, the use of air filtration systems to reduce environmental exposures is a potential school-based intervention.⁸⁴ One pilot study showed that HEPA air filters reduced mold spore counts in daycare centers by 50%.⁷⁸

School environmental intervention studies that are prospective, longitudinal, randomized, double-blinded controlled trials using sham interventions as controls are needed as the majority of studies performed to date have been small and cross-sectional with no control for home exposures.^{9, 36, 39, 41–43, 85, 86} Given the SICAS findings of high mouse allergen levels in school classrooms,^{10, 12} a NIH/NIAID School Inner-City Asthma Intervention Study (ClinicalTrials.gov NCT02291302), (SICAS 2), using environmental control strategies modeled from successful home-based interventions, is underway with health outcomes results pending.²⁸ This randomized, controlled trial is comprehensively evaluating the role of a school-based environmental intervention and is adequately powered to assess asthma outcomes, adjusting for home exposures. The research group conducted a pilot study prior to launching the main study and demonstrated that a classroom-based air cleaner intervention led to significant reductions in particulate matter with diameter of <2.5 μm and black carbon, compared to sham filters.⁷⁷ The use of HEPA air filters to reduce indoor pollutant particles and its associated allergens is currently being studied in SICAS 2. Another feasible school-based intervention is IPM. IPM is a multidisciplinary approach that uses a range of pest control methods such as: 1) monitoring pest populations with sticky traps to find out where they are living and hiding (reservoirs); 2) blocking pest access and entryways; 3) eliminating food and water (facilitating factors); 4) selectively applying low-toxicity pesticides. Nalyanya and colleagues demonstrated that IPM implementation in select North Carolina schools was not only more effective at controlling cockroaches than conventional pest control but lead to long-term reductions in allergen concentrations.⁸⁷

Challenges of School Environmental Intervention Studies

The school environment is a complex microenvironment of indoor allergens, pollutants, and particles with more potentially significant environmental exposures than in the home. The predominating environmental exposures in individual schools across the country will likely vary due to differing geographic, climate and socioeconomic conditions, and distance from major highways and roadways, among the many factors. Therefore, a single school environmental intervention strategy may not be realistic or generalizable for all schools, making the implementation of school environmental intervention strategies complicated. To adequately show improved asthma outcomes, these variable exposures need to be taken into consideration when designing school intervention studies. Studies suggest that environmental interventions are likely cost-effective but implementation and buy-in to do this necessary research in schools in order to prove its benefit is a challenge.⁸⁸ However, while previous home intervention studies target a single individual or family, the school has the potential to intervene on a community of children, and if effective, should be much more cost-effective.

Other unique challenges include the logistics of implementing these interventions in a classroom setting in an unobtrusive way. For instance, HEPA filters need to be both physically and acoustically tolerable for students. While it is possible for some school-based interventions to be blinded, such as sham versus active filters in the classrooms, large-scale interventions might be more difficult to blind. In addition, certain interventions such as IPM cannot be randomized from classroom to classroom but could be randomized between schools. Lastly, and of paramount importance to the success of these school-based environmental intervention studies is the commitment and community buy-in from senior school administrators, principals, teachers, school nurses, facilities management, as well as the students and their families.

Conclusions

Environmental control measures can and should supplement good asthma medical care. As in home environments, it is unlikely that a single school or classroom-based environmental exposure is exclusively responsible for asthma morbidity, given that asthma involves a number of factors. Both home and school environmental control approaches taken together have the ability to optimize asthma health outcomes, understanding that this approach might be more cost prohibitive. Our SICAS 2 study is attempting to focus on comprehensively evaluating school-specific environmental interventions and health outcomes, adjusting for exposure in the home as an initial step. From a public health perspective, the school environment could be considered as a target for primary and secondary prevention of allergic disorders including asthma. While it is more practical and cost-effective to perform environmental interventions on a single school affecting many children at once than the many individual homes in a community, there are challenges with designing school intervention studies to target the vast environmental exposures across schools in the U.S. in a meaningful way to improve asthma outcomes and there are the prohibitive costs associated with these studies.. It is important that environmental health researchers continue to assess which school environmental interventions are most practical and result in the greatest measurable improvements. Furthermore, research should further examine the relationship between allergen exposure in schools and resulting health effects, in order to develop an accurate exposure-risk model specific to the school environment.

Abbreviations

IgE

Immunoglobulin E

Th₂

T helper 2

HEPA

high efficiency particulate arrestance

IPM

integrated pest management

NAEPP

National Asthma Education and Prevention Program

SICAS

School Inner-City Asthma Study

NIH

National Institutes of Health

NIAID

National Institute of Allergy and Infectious Disease

HITEA

The Health Effects of Indoor Air Pollutants

PM

particulate matter, NO₂, nitrogen dioxide

GIS

geographic information system

EPA

Environmental Protection Agency

SAMPRO

School-Based Asthma Management Program

CDC

Centers for Disease Control and Prevention

SBHC

school-based health centers