Recommendations for Clinicians to Combat Environmental Disparities in Pediatric Asthma

Abstract

Topic Importance

Asthma is a common and complex lung disease in children, with disproportionally higher prevalence and related adverse outcomes among children in racial and ethnic minority groups and of lower socioeconomic position. Environmental factors, including unhealthy housing and school-based exposures, can contribute to increased asthma morbidity and widening disparities. This underscores a significant environmental justice issue and suggests the need for clinical interventions to reduce sources of environmental exposures and ultimately diminish the observed disparities in childhood asthma.

Review Findings

Unhealthy housing conditions, including secondhand tobacco smoke, allergen exposure, and indoor air pollution, can exacerbate asthma symptoms in children. Although unhealthy housing can occur anywhere, such situations most frequently occur in urban, low-income environments where renting is common. To reduce environmental triggers, clinicians can recommend smoking cessation, cleaning techniques to mitigate exposure, and even directly contacting landlords to address poor housing conditions. Children spend much of their time in schools, where this built environment is also a source of asthma triggers (eg, poor ventilation) and allergens (eg, mold and pests, chemicals). As such, a multidisciplinary approach is needed to adequately address the burden of childhood asthma to equitably reduce disparities to both harmful exposures and negative health outcomes.

Summary

Racial, ethnic, and socioeconomic disparities exist in asthma morbidity in children, and such disparities are driven in part by environmental factors at the housing and school level. Clinicians can make evidence-based recommendations to drive effective exposure reduction strategies to mitigate asthma morbidity and reduce observed disparities.

Asthma is a chronic and complex lung disease impacting roughly 5 million children in the United States.^1,2 Comorbidity among atopic diseases (eg, allergic rhinitis, food allergies) is common among children with asthma, contributing to complexities in treatment and management.³ Uncontrolled asthma or comorbid atopic disease has also been found to negatively impact child well-being, including contributing to missed days of school or impacting social interactions with peers.⁴ Findings using National Health Interview Survey data from 2007 to 2018 identified asthma prevalence to be roughly 8% among children ≤ 17 years of age, with higher prevalence observed among children who were Black, Hispanic, or multiracial compared with those who were White.^5,6 In fact, the prevalence of asthma for Black children was almost double that of White children.⁶ Additionally, authors reported that children of families with lower incomes also have higher prevalence estimates of asthma.⁶ Although the overall prevalence of childhood asthma is decreasing over time, the rate of decline is more pronounced among White children relative to other racial and ethnic groups, underscoring disparities in both prevalence and reduction of morbidity over time.⁶

No consistent root cause for asthma has been identified; however, early life assaults to the immune system are likely contributors to inflammation in the respiratory system. Indeed, there are genetic components to asthma susceptibility in children, attributed to patterns of familial diagnosis; however, genetics alone do not account for all cases of asthma incidence.⁷

Attempts to prevent asthma have been largely unsuccessful; however, there is some promise in preventing asthma development in young children by blocking IgE—as further explored in an ongoing randomized, double-blind clinical trial, Preventing Asthma in High Risk Kids (PARK).⁸ In the absence of risk reduction methods at the individual level, one could consider how reducing environmental exposures may prevent asthma-related outcomes. Evidence suggests a link between environmental contaminants with asthma development and symptom severity in children, including air pollution (indoor and outdoor),9, 10, 11 allergen exposure,^12,13 and chemical exposure.¹⁴ Consistent with many areas of environmental health, the uneven distribution of environmental contaminants often overlaps with predictors of health disparities, and childhood asthma is no different. These include factors that operate at the individual level (eg, access to healthy housing), including elements such as indoor air pollution and pest control, and those at the neighborhood level, specifically school-related exposures.

Here, we summarize the evidence from environmental studies with a focus on recommendations for clinicians and suggestions for reducing environmental health risk factors that contribute to disparities in asthma morbidity in children. Focusing on healthy housing and school-based factors, it is the goal of this review to bridge the gap between environmental disparities work and clinical practice to provide opportunities for clinical intervention to improve asthma outcomes in children and ultimately reduce disparities in childhood asthma.

Literature Search

The objective of this review is to outline the current body of evidence describing environmental disparities for asthma outcomes in children. Although there are many lines of evidence to consider, we identified two target areas for the focus of this review: first, access to healthy housing and second, school-based risk factors. Unlike other environmental determinants of health (ie, chemical exposures), we chose to focus on two topic areas with opportunities for clinical intervention. We used Google Scholar and PubMed to identify papers published since 2014 (past approximately 10 years). We identified additional papers via reference lists of previously identified articles.

Evidence Review

Describing the Racial and Economic Disparities in Asthma

Asthma morbidity and related adverse outcomes (ie, ED visits) are disproportionately distributed among racial and ethnic minority groups^5,6 and may be further exacerbated by lower socioeconomic position.⁶ Some evidence suggests racial differences in airway inflammatory phenotypes (eg, Black individuals may have more eosinophilic airway inflammation relative to White individuals) can contribute to differences in asthma morbidity, severity, and response to asthma-related treatments, suggesting a biological susceptibility.¹⁵ However, in one study that accounted for environmental and socioeconomic factors, the racial disparity in asthma-related ED visits was eliminated, suggesting policies and interventions targeted toward asthma risk reduction and treatment among Black populations could reduce the observed disparity in asthma morbidity.¹⁶ Another study reported that interventions focused on social determinants of health, including access to shelter, food, and utility assistance, contributed to substantial reductions in asthma-related ED visits among minority children living in poverty.¹⁷ The racial and ethnic disparities in childhood asthma morbidity are apparent and are likely driven by poverty-related socioeconomic factors and environmental exposures¹⁸ rather than biological differences. Furthermore, race is a social construct and not a biological variable. Indeed, genotyping work has identified differences in asthma severity. For example, individuals with an IL-4R $\alpha$-R576 variant demonstrated mixed T_H2-T_H17 cell inflammation, a phenotype regulated by Notch4 regularity T cells in airways, consistent among those with more severe asthma.^19,20 Additionally, gene-environment interactions have been identified (eg, interactions between IL-4R variant and endotoxin exposures) in relation to asthma severity.²¹ Although genotyping work in asthma (eg, that outlined in the Investigating Dupilumab’s Effect in Asthma by Genotype [IDEA] study among others) can inform genotype-driven approaches to treatment with biologics, directly impacting how clinicians can manage asthma symptoms within their patients, this work will not be the focus of our review. Although we agree that genetic variation can impact asthma-related outcomes, observed racial and ethnic disparities are primarily attributed to disparities in environmental exposures. Furthermore, although genetics work can help inform directed treatments, it does little to inform evidence-based policies or recommendations for risk reduction. To prioritize health promotion, we will review evidence of disparities in environmental exposures because such work can inform efforts to address these gaps and ultimately eliminate racial and ethnic disparities in childhood asthma. Although these disparities are striking, the underlying contributors present opportunities for targeted policies and interventions aimed at reducing and eliminating these observed disparities.

Healthy Housing and Disparities in Asthma Morbidity in Children

According to the World Health Organization, healthy housing promotes improving dwellings to reduce disease and poverty,and promotes sustainability with the ultimate goal of saving lives.² It is important to recognize that unhealthy housing can occur in any environment; however, indoor air quality (IAQ) concerns tend to occur more frequently in inner cities, highlighting an important public health concern given the frequency of renters in urban environments who may have limited control to make direct changes to their housing in an effort to promote child health.^13,22 Unhealthy housing, common in low-income households, can disproportionately expose children living in these conditions to factors that can exacerbate asthma symptoms.²³ For example, dust mite exposure is consistently associated with atopic disease and has even been causally implicated in asthma exacerbation among sensitized children.²² Pest allergen exposure is more common in inner-city housing than rural areas²⁴; however, mouse allergenic proteins Mus m 1 and Mus m 2 are detected in almost all homes in the United States.¹³ Results from a clinical trial from our group have reported that integrated pest control interventions are effective in significantly reducing mouse allergen levels in homes, indicating promise for evidence-based exposure reduction strategies.²⁵ Cockroach allergens Bla g 1 and Bla g 2 are also commonly detected in inner-city homes, and exposure to pest allergens (mouse and cockroach) have both been associated with increased hospitalizations for asthma and reductions in lung function.¹³ Emerging evidence suggests pest allergens, particularly mouse, may be the most harmful allergen related to asthma outcomes among sensitized children, suggesting exposure reduction strategies should be prioritized.²⁶ Mold exposure is also common in inner-city housing. Indoor mold exposure has broadly been associated with an increased risk of asthma morbidity in children.²⁷ For example, children living in homes with window air conditioning units, ubiquitously containing mold species Mucor, were more likely to have difficult-to-treat asthma relative to children who did not live in homes with window air conditioning units.^24,28

Air pollution, broadly, has been associated with an increased risk of asthma morbidity in children²⁹; however, for the purposes of this review, we will focus on indoor-related air pollutants. Within the United States, roughly 14% of children are exposed to secondhand tobacco smoke in their homes, with exposure most commonly occurring in inner-city and low-income homes.³⁰ Secondhand tobacco smoke exposure, of at least 1 h/wk, was associated with increased asthma symptoms, mediation utilization, inhaler use, and ED visits in children.³¹ In fact, having a caregiver who smoked tobacco or used e-cigarettes was associated with increased odds of hospitalization among children with asthma.³² Evidence suggests that efforts to promote smoke-free environments in personal and rental properties can lead to lower levels of asthma morbidity in children and may prevent severe outcomes (eg, ED visits) among children with existing asthma.²⁹ Radon, a natural gas, is known to cause adverse health effects in humans. Despite nationwide mandates to reduce radon exposure in homes, testing and mitigation efforts remain insufficient in low-income or rental properties.^18,33 Furthermore, even low levels of radon exposure were associated with an increased frequency of asthma diagnosis in children, indicating that no level of radon is safe.³⁴ Additionally, children who are overweight or obese may be more vulnerable to the effects of secondhand tobacco smoke and indoor air pollution, including nitrogen dioxide (NO₂).35, 36, 37

It is important to recognize that there are many other aspects related to the topic of healthy housing and pediatric asthma morbidity that we are unable to adequately address here. For example, food insecurity has been associated with asthma morbidity, with poverty further exacerbating these observed associations.^38,39 Childhood obesity has also been associated with asthma morbidity.⁴⁰ Additionally, elevated neighborhood levels of violence have been associated with adverse asthma-related outcomes,41, 42, 43, 44 with underlying mechanisms suggesting increased chronic stress (eg, stress related to poverty)45, 46, 47 and decreased physical activity,⁴⁸ which in turn can contribute to obesity.⁴⁹ Such observed associations persist even when accounting for availability and access to food.⁵⁰ We recognize that these topics have only been briefly addressed here and should be more thoroughly considered in future work.

School-Based Exposures and Disparities in Asthma Morbidity in Children

The Environmental Protection Agency (EPA) has established that IAQ in schools is essential, concluding that “good [IAQ] contributes to a favorable environment for students, performance of teachers and staff, and a sense of comfort, health and well-being. These elements combine to assist a school in its core mission- educating children.”⁵¹ However, despite the well-known benefits of having a school IAQ plan, the School Health Policies and Practices Study found that across a random sample of public school districts in the United States, fewer than one-half reported having a plan.^52,53 Children spend a significant amount of time in school, highlighting the importance of considering the role of allergen exposure in school environments on asthma morbidity. The School Inner-City Asthma Study-2 (SICAS-2) was designed to prospectively evaluate school-specific risk factors in asthma morbidity among urban children, under the framework of addressing inequities in asthma by focusing on the child’s built environment.⁵⁴

Evidence from SICAS-2 consistently found that school exposures to mouse and mold allergens, endotoxins, and pollutants, all directly impacted asthma morbidity among inner-city children.^26,55 Such work was the first step in laying the groundwork for interventions focused on pest management strategies, found effective in reducing asthma morbidity.⁵⁶ Integrated pest management (IPM) uses a risk reduction-focused approach to reduce the presence of pests and other allergens.⁵⁶ Pests include rodents (mice and rats), cockroaches, and mites, and exposure to them has been associated with increases in asthma morbidity.57, 58, 59, 60 Exposure to mouse allergens within the school setting is associated with decreased lung function and increased symptoms of asthma.²⁶ Implementation of an IPM plan in a school setting was associated with the microbial community structure and changes in the classroom microbiome.^56,61 One study reported that implementation of IPM practices including the placement of nontoxic bait traps, cleaning, trash removal, and educational handouts resulted in a significant reduction of school absences due to asthma relative to the control group. However, over time, levels of mouse allergens in schools have decreased over time.⁶² The effects of mouse allergen on lung function in children may also be exacerbated by other factors (eg, higher plasma IL-6 levels, increased BMI⁶³), suggesting that a more comprehensive strategy—beyond pest control management—may be necessary to alleviate asthma symptoms in some children who may have increased susceptibility.

Findings from SICAS-2 and other studies have reported that the presence of some fungi in the indoor setting is associated with asthma exacerbations and symptoms, particularly sensitization to Alternaria species.^22,64,65 To assess the utility of high-efficiency particulate air filtration-based school interventions for mold and moisture control, one study that applied the Environmental Relative Moldiness Index and tested students lung function reported reduced Environmental Relative Moldiness Index and improved FEV₁ results among students who received the intervention relative to those who received the sham control.⁶⁶ Furthermore, the students sensitized to Alternaria species and exposed to high concentrations of fungi had more asthma symptom days relative to other sensitized students that were exposed to lower concentrations.⁶⁴

Proper maintenance of heating, ventilation, and air conditioning infrastructure is essential to maintain the quality of indoor air by reducing the concentration of pollutants with fresh air intake. Relative to classrooms with good ventilation, students in classrooms with poor ventilation were more likely to have decreased concentration and to be less attentive.⁶⁷ Adequate indoor air ventilation in the school setting has been significantly associated with math test results such that improvements (increases) in ventilation rates are associated with greater test results.⁶⁸ It is estimated that by doubling the ventilation rate, the speed at which children can complete school work increases by 14%, national test scores increase by 5%, and child daily attendance increases by 1%.^69,70 Furthermore, a study examining the presence of mold and asthma in the school setting reported that students attending schools with air conditioning had significantly reduced asthma prevalence relative to students who attended schools without air conditioning.⁷¹ Improving air ventilation can also reduce exposure to indoor air pollutants, including NO₂. Findings from SICAS-2 observed an association between decreased lung function with higher levels of classroom NO₂ exposure.⁷² Proximity to heavily trafficked roadways in both schools and homes may also increase exposure to air pollutants indoors, contributing to increased asthma morbidity in children.⁷³ As such, school-based interventions to improve school ventilation systems provide an actionable step to improve student test results, increase student speed, and reduce absences for many children concurrently.^74,75

Effective cleaning and maintenance of school buildings include proper dust control, selection of green cleaning materials, visual inspections for leaks, and standardized cleaning protocols. The selection of smart materials is also crucial to maintaining IAQ that is conducive to student academic success and health. Although the maintenance of a clean, dust-free environment can be beneficial for asthma control, exposure to some cleaning products containing endocrine disrupting chemicals or propylene glycol and glycol ethers have been associated with increased risk of asthma and eczema due to airway inflammation.76, 77, 78, 79 Thus, the EPA recommends that schools keep an inventory of cleaning products, have a selection of low-emitting products, and purchase cleaning products that are the “least toxic.” Finally, source control and chemical management involve the creation of a chemical management and waste plan, minimizing exposure to pollutants while children are in school, and regular testing for radon.

The guidelines provided by the EPA provide schools with the necessary resources to quantify the IAQ, take steps to improve the indoor air, and, as a result, improve the health outcomes of students, especially those suffering from asthma.

Recommendations for Clinicians

Evidence from epidemiologic and observational studies can help inform clinician approaches to reducing asthma morbidity, particularly related to racial and socioeconomic disparities, in children outside of traditional clinical appointments. Recommendations and suggestions for how clinicians can apply these recommendations based on specific asthma triggers are summarized in Table 1 and Figure 1. For example, some evidence has found that landlords are more amenable to requests to improve housing conditions when requests come from physicians vs tenants.^80,81 This should encourage clinicians to engage with patients and their families to have conversations regarding potential environmental triggers for asthma morbidity in children and empower clinicians to have direct impacts on reducing environmental exposures. However, clinicians should also keep in mind that there is no one-size-fits-all approach when it comes to reducing environmental exposures for decreasing asthma morbidity. To have substantial impacts on reducing asthma morbidity, extensive interventions targeting environmental exposures must be used at both home and in schools.⁵⁶ Ultimately, a multidisciplinary approach that engages multiple stakeholders, perhaps one grounded in the Consolidated Framework for Implementation Research, is essential to tackle asthma and its variety of environmental triggers.82, 83, 84 It should also be noted that these recommendations should serve as a starting point to engage clinicians in possible new ways they can intervene to address environmental disparities as a method to reduce asthma morbidity in children. It is also noteworthy that many of these recommendations targeting environmental justice issues will have positive impacts on child health broadly and are not limited to asthma morbidity. Although family- and patient-specific recommendations should be individualized based on the specific needs and circumstances of the child, clinicians should practice their own judgments based on their expertise. We also encourage clinicians to consider other ways to target environmental disparities and disparities in childhood asthma morbidity, including advocating for system-level changes (eg, expansion of state Medicaid managed care programs, screening programs through local Departments of Health).

Table 1.

Recommendations and Suggestions for Clinician to Patients and Their Caregivers for Preventing and Reducing Asthma Morbidity in Children Relative to Unhealthy Housing and School-Related Factors

Asthma Trigger	Recommendation	References
	Environmental-focused recommendations
Pests (mouse and cockroach)	To effectively reduce pest allergen exposure: •Integrated pest management strategies including removal of food sources, eliminating entry points, and removing existing pests.12 •Filling of holes, vacuuming, the use of low-toxicity traps, sealing cracks to prevent reentry, and cleaning of allergen resevoirs.8,25 •IPM strategies in homes and schools can lead to significant reductions in both mouse and cockroach allergen levels, which can improve asthma-related outcomes.85	Matsui et al (2017)12 Phipatanakul et al (2004)25 Phipatanakul et al (2021)8 Sadreameli et al (2021)85
Mold	Mold risk reduction strategies: •Reducing moisture and removing contaminated areas through adequate cleaning and ventilation and limiting use of window air conditioning units.24,28 •However, the success of cleaning interventions on preventing asthma-related outcomes in children is weak.13	Lee et al (2023)24 Vesper et al (2023)28 Maciag et al (2022)13
Dust mites	•As many as 84% of homes in the United States have detectable levels of dust mites, with higher levels in older homes with carpeting and no air conditioning.13 Ways to reduce exposure to dust mites: •Removal of carpeting particularly in the bedroom. •If removal is not possible, regular vacuuming can reduce dust mite levels.	Maciag et al (2022)13
Tobacco smoke exposure	To reduce exposure to tobacco smoke: •No indoor tobacco smoking for residents or guests, including e-cigarettes and vaping. •Requesting landlords require tobacco smoke-free dwellings and properly reinforce these rules to prevent secondhand exposure across units. •Request adequate cleaning when moving into a new unit where the previous tenants were tobacco users. •The creation of public policies to implement smoke-free public spaces will further prevent exposure.10,22	Naja et al (2018)10 Kanchongkittiphon et al (2015)22
Air pollution (PM2.5, black carbon, radon)	To reduce exposure to traffic-related pollutants (both particulate matter and black carbon): •Prevention of school bus idling in front of schools.9,10 •Increasing the distance of schools from major roadways.73 •Frequent testing of radon levels.11 •Implementation of HEPA filters in classrooms.9,56	Jhun et al (2017)9 Naja et al (2018)10 Banzon et al (2023)11 Phipatanakul et al (2021)56 Hauptman et al (2020)73
	Asthma-related recommendations
School-supervised asthma therapy	•Partnerships with school nurses provide an opportunity to increase medication adherence, improvement in asthma outcomes, and adherence to asthma management plans.72 •School-based screening to reduce health care utilization86 •Nurse supervised inhaled corticosteroids at school and school-centered health partnerships.87	Shillan et al (2022)72 Trivedi et al (2018)86 Louisias et al (2017)87
Dedicated severe asthma programs: home visits	Dedicated severe asthma programs that use multidisciplinary approaches to address social determinants of health to reduce health care utilization and improve self-management.17	Leibel et al (2020)17
Medical-legal partnerships	Pediatricians can leverage their expertise with little time and no cost to write letters on behalf of patients to their landlords encouraging the repair and maintenance of housing conditions that may be exacerbating asthma symptoms.80,81	Lax et al (2021)80 Workman et al (2021)81

HEPA = high efficiency particulate air; IPM = integrated pest management, PM2.5 = particulate matter ≤ 2.5 micrometers in diameter.

Figure 1.

Environmental-focused recommendations and suggestions for clinicians to parents and caregivers for preventing and reducing asthma morbidity in children. AC = air conditioning; HEPA = high efficiency particulate air.

Closing Section

Asthma is a chronic and lifelong condition that disproportionally impacts Black, Hispanic, and/or multiracial children and children in families of lower socioeconomic position more so than children who are White or of higher socioeconomic position.⁵ Racial and economic disparities in childhood asthma can be explained, in part, due to disparities in environmental exposures, including—but not limited to—access to healthy housing and school-based exposures. Physicians can assist in reducing sources of pests and improving IAQ to promote healthy housing as a method to reduce asthma exacerbations. This can include educating patients’ families about pest management,⁸⁵ mold risk reduction and cleaning,¹³ and the effects of tobacco smoke exposure.¹⁸ Evidence has also shown that landlords are more amenable to improving housing conditions when receiving correspondence from physicians compared with complaints from tenants alone.^80,81 Physicians can also work with patients to improve environmental conditions in school settings. This can include partnering with school nurses to assist in the supervision of school-based asthma therapies to improve continuity of quality care.^86,87 Physicians can also partake in multidisciplinary asthma programs to address social determinants of health through home visit programs.¹⁷ Although environmental exposures both at home and school settings are not the only known causes for asthma in children, the exposures in these settings have been repeatedly found to exacerbate asthma-related outcomes among children. Additionally, differential exposures to these factors are likely contributors to the racial and economic disparities observed in childhood asthma. To promote health for all children, we urge physicians to play an active role in reducing asthma triggers throughout a child’s life by partaking in and encouraging evidence-based practices.

Summary

Asthma is the most common childhood disease, with prevalence and related outcomes occurring more frequently in racial and ethnic minority groups and low-income children relative to White peers. Environmental sources of exposure, including unhealthy housing and school-related factors, can contribute to asthma morbidity and severity of outcomes. Additionally, these exposures are disproportionately burdensome to minority and low-income populations. Clinicians can use a multifaceted approach to address not only the clinical presentation of asthma and its associated symptoms, but also its social determinants and opportunities to intervene to reduce environmental exposures and triggers. The development of exposure reduction strategies to mitigate exposure and prevent asthma morbidity in children is an important step in promoting health equity. The future of asthma management and care in school-aged children can be best addressed through the formation of multidisciplinary partnerships to address the reduction of asthma triggers throughout all aspects of a child’s life, including the home environment and school environment.

Funding/Support

This study was supported by the NHLBI [Grant K01HL171354 to M. J.-B.] and the NIAID [Grants K24AI106822, U01AI110397 to W. P.].

Financial/Nonfinancial Disclosures

The authors have reported to CHEST the following: W. P. reports personal fees from Sanofi, Regeneron, Novartis, Genentech, GSK, and Astra Zeneca, outside the submitted work. None declared (M. A. P., N. B. H., M. J.-B.).