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The clear and persistent impact of air pollution on chronic respiratory diseases: a call for interventions

Isabella Annesi-Maesano, Francesco Forastiere, John Balmes, Erika Garcia, Jack Harkema, Stephen Holgate, Frank Kelly, Haneen Khreis, Barbara Hoffmann, Cara Nichole Maesano, Rob McConnell, David Peden, Kent Pinkerton, Tamara Schikowski, George Thurston, Laura S. Van Winkle, Christopher Carlsten
European Respiratory Journal 2021 57: 2002981; DOI: 10.1183/13993003.02981-2020
Isabella Annesi-Maesano
1Sorbonne Université and INSERM, Epidemiology of Allergic and Respiratory Diseases Dept, Institut Pierre Louis of Epidemiology and Public Health, Paris, France
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Francesco Forastiere
2Environmental Research Group, King's College, London, UK
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John Balmes
3University of California Berkeley-University of California San Francisco Joint Medical Program, Berkeley, CA, USA
4School of Public Health, University of California, Berkeley, CA, USA
5Dept of Medicine, School of Medicine, University of California, San Francisco, CA, USA
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Erika Garcia
6Dept of Preventive Medicine, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA
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Jack Harkema
7Dept of Pathobiology and Diagnostic Investigation, College of Veterinary Medicine, Michigan State University, East Lansing, MI, USA
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Stephen Holgate
8Clinical and Experimental Sciences, Faculty of Medicine, University of Southampton, Southampton, UK
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Frank Kelly
2Environmental Research Group, King's College, London, UK
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Haneen Khreis
9Center for Advancing Research in Transportation Emissions, Energy, and Health (CARTEEH), Texas A&M Transportation Institute (TTI), College Station, TX, USA
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Barbara Hoffmann
10Institute for Occupational, Social and Environmental Medicine, Center for Health and Society, Heinrich Heine University of Düsseldorf, Düsseldorf, Germany
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Cara Nichole Maesano
1Sorbonne Université and INSERM, Epidemiology of Allergic and Respiratory Diseases Dept, Institut Pierre Louis of Epidemiology and Public Health, Paris, France
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Rob McConnell
11University of Southern California, Preventive Medicine, Los Angeles, CA, USA
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David Peden
12Center for Environmental Medicine, Asthma and Lung Biology and Division of Allergy, Immunology and Rheumatology, Dept of Pediatrics, the School of Medicine, The University of North Carolina at Chapel Hill, Chapel Hill, NC, USA
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Kent Pinkerton
13Center for Health and the Environment, John Muir Institute of the Environment, University of California, Davis, CA, USA
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Tamara Schikowski
14IUF-Leibniz Research Institute for Environmental Medicine, Düsseldorf, Germany
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George Thurston
15New York University School of Medicine, Dept of Environmental Medicine, New York, NY, USA
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Laura S. Van Winkle
16Dept of Anatomy, Physiology and Cell Biology, School of Veterinary Medicine, University of California, Davis, Davis, CA, USA
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Christopher Carlsten
17Air Pollution Exposure Laboratory, Dept of Medicine, Division of Respiratory Medicine, The University of British Columbia, Vancouver, BC, Canada
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Abstract

Air pollution is responsible for chronic respiratory symptoms and diseases. Efforts to reduce air pollution exposure to protect public health, especially from emissions from both fossil fuel combustion and biomass combustion, are needed urgently. https://bit.ly/3hJtCze

Introduction

Air pollution is ubiquitous and is responsible for noticeable acute and chronic adverse health effects [1]. Heart diseases and stroke are the most common reasons for morbidity and mortality attributable to air pollution, followed by respiratory diseases, but recently other pathologies have been added to the list. Additionally, air pollution contributes to climate change, another threat to public health.

Air pollution sources are both anthropogenic (traffic, industry, combustion, etc.) and natural (wildfires, erosion, volcanic eruption, etc.). Calculating population exposure to air pollution is crucial to assessing the extent of health impacts of air pollution. One indicator, the exceedance of air quality standards in urban areas, shows percentages of citizens in the European urban population who are regularly exposed to levels of air pollutants exceeding both the World Health Organization (WHO) guidelines and the more local EU legal standards (figure 1).

FIGURE 1
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FIGURE 1

Exceedance of air quality standards and guidelines in European urban areas (data from www.eea.europa.eu/themes/air/health-impacts-of-air-pollution). WHO: World Health Organization; PM2.5: particulate matter of diameter of 2.5 µm, PM10: particulate matter of diameter of 10 µm; BaP: benzo[a]pyrene. EU reference values (annual value): PM2.5: 25 µg·m−3, PM10: 40 µg·m−3, NO2: 40 µg·m−3, O3: 120 µg·m−3 (8-h mean); SO2: 125 µg·m−3 (24-h mean); BaP: 1 ng·m−3. WHO air quality guidelines: EU reference values (annual value): PM2.5: 10 µg·m−3, PM10: 20 µg·m−3, NO2: 40 µg·m−3, O3: 100 µg·m−3 (8-h mean); SO2: 20 µg·m−3 (24-h mean); BaP: 0.12 ng·m−3.

The situation is even worse at the world level where, according to WHO, 92% of the population is excessively exposed to fine particulate matter (PM). Developing countries are the most severely affected.

We highlight here recent epidemiological and toxicological data that support the link between air pollution and chronic respiratory diseases in a public health context and reiterate the importance of interventions that are driven by the ongoing need to improve air quality. To make this point, we summarise several meta-analyses or large studies that are best positioned to quantify these relationships, reflecting a logical framework described in recent review of the topic [2].

Not only does ambient air pollution exacerbate asthma but it is also related to new-onset asthma

Several recent meta-analyses of time-series and case-crossover design studies, covering various seasons and years, support a substantial role of air pollution on children's hospital admissions and emergency department visits for asthma [3, 4], and even asthma mortality [5]. Another recent meta-analysis strongly connected landscape fire smoke particulate matter of diameter <2.5 µm (PM2.5) and both asthma hospitalisations and emergency department visits [6]. Yet another meta-analysis highlights ozone as a seasonal trigger for asthma exacerbations and hospitalisations [7]. It is difficult to imagine that for all these spatio-temporally distinct events the air pollution factor was unimportant, as recently suggested [7], and that these findings are simply explained by a hidden allergen exposure that acts as the primary culprit. Indeed, there are studies showing that ground level ozone and PM2.5 have been associated with increased asthma exacerbations even in the absence of significant allergen exposure, and no such simultaneous association with allergens was found [8, 9]. Moreover, toxicological evidence supports air pollution's impact on asthma in the context of allergens [10, 11].

Most important, air pollution not only exacerbates asthma but it is also related to new-onset asthma in children. Indeed, existing epidemiological literature supports long-term exposure to traffic-related air pollution as a causal contributor to new onset of childhood asthma [2, 12, 13]. As a confirmation of the involvement of long-term air pollution, a survey in Southern California showed decreases in ambient nitrogen dioxide and PM2.5 between 1993 and 2014 were significantly associated with lower childhood asthma incidence [14]. Very recently, long-term exposure to air pollution, especially from traffic, was associated with adult-onset asthma, even at levels below the current limit values, in a population of 98 326 individuals followed-up over 16 years in Denmark and Sweden [15]. This study will critically inform the evidence for a causal role in adult-onset asthma at the population level, which recently was deemed insufficient in spite of suggestive evidence [15].

Furthermore, a view of the toxicological literature is instructive in that it strongly supports an interactive chain of events linking air pollution-induced pulmonary and systemic oxidative stress, and inflammatory events, with an associated risk of airway disease [16]. In adults with asthma, walking for 2 h along Oxford Street in London resulted in a significant but essentially asymptomatic reduction in lung function. Although the changes were small, they were greater than those provoked by walking in a nearby park and were more pronounced among study participants whose asthma was more severe [17]. These changes were accompanied by inflammatory changes in sputum and exhaled breath condensate. From the toxicological perspective, numerous studies in animal models support these findings in humans, deepening the plausibility by showing that exposure to either ambient PM or ozone both exacerbates and contributes to the development of pulmonary disease [18, 19].

Air pollution confers a greater risk for COPD

The importance of outdoor air pollution as a contributory cause of COPD is presently underestimated. However, the Global Exposure Mortality Model (GEMM), which captures data from 41 cohorts from 16 countries, showed a significant association between PM2.5 and COPD mortality after adjustment for major mortality risk factors, such as cigarette smoking, obesity and occupation [20]. Experimental studies are adding to the plausibility of air pollution's role in COPD [21].

In this context, many papers seem to ignore complexity of exposure variability and how this may influence vulnerability. A recent study on the effect of air pollution on daily mortality in 652 cities worldwide found strong effects, particularly in locations with lower annual mean PM2.5 concentrations [22], on respiratory mortality. In contrast, a meta-analysis of several studies conducted in China found an inverse linear relationship between the risk of mortality and annual PM10 and NO2 concentration [23], begging explanation. While this pattern is unusual, flattening of the curve is well-described and perhaps there exists a saturation mechanism that alters exposure–response gradients, which remains an important area for further study. Regardless, the equal toxicity assumption in the computation of integrated exposure–response functions for particulate matter is increasingly recognised as problematic. Additionally, a better incorporation of particulate matter composition and source into models is also needed as we grapple with the best approach to optimising health benefits, especially given changes due to the climate crisis and its associated increase in air pollution.

Stronger evidence exists on the link between biomass and COPD. A third of the world's population, that is, around 2.5 billion people, relies on the traditional use of solid biomass for cooking and heating. Several meta-analyses [23–29] indicate that biomass fuel exposure is associated with diverse respiratory symptoms and diseases, including chronic bronchitis and COPD in non-smokers and in women. In the latest meta-analysis, which included 35 eligible studies for a total of 73 122 participants in diverse regions of the world, exposure to indoor air pollution due to solid biomass fuels increased the risk of COPD [29]. More recently, a large multi-country study reports an association between exposure to household air pollution and risk of COPD [30]. However, the GOLD study failed to find a significant association in the entire population, in spite of showing strong statistically significant effect estimates for chronic phlegm in women after adjusting for smoking [31].

While further studies, with improved data on potential confounders, are warranted, the urgent need to reduce biomass fuel exposure remains pressing and should not be delayed, in accordance with Sustainable Development Goals on equality, health and access to sustainable energy. Exposure to biomass has detrimental effects on the lungs in women. Women with biomass-induced COPD tend to have lifelong exposure, which starts in utero and continues into childhood and adulthood. This is particularly true in less-developed countries, where these women have limited access to “clean” fuels and so tend to burn pre-processed woods, charcoal, animal dung, coal or crops for cooking on a daily basis. Importantly, when women are exposed, so are very young children who suffer and die from respiratory infections. In addition, anatomical and physiological differences between men and women place women at higher risk of respiratory diseases, beginning in early life. Instead of questioning whether these toxic particles are a major contributor to respiratory health outcomes in women leading to permanent airflow obstruction [32], a recommendation for better studies in developing countries would be more appropriate.

From the toxicological point of view, a noteworthy study from California demonstrated wildfire smoke to be significantly more toxic compared to ambient PM from the same California location taken a year earlier [33]. A more recent study [34] further delineates unique features of biomass burning that contribute to its toxicity.

Air pollution also impacts other respiratory diseases

Few studies have examined the effects of air pollution upon other respiratory diseases and they have focused on small numbers of patients. Most data are available on idiopathic pulmonary fibrosis and suggest that the level of exposure to air pollutants may influence the incidence of fibrosis [35, 36], the occurrence of acute exacerbation [37, 38], decline in respiratory function [39] and even death [38]. Several pathogenic mechanisms may be involved in the deleterious effect of air pollutants in IPF. For example, prolonged exposure to fine particles could induce local lung inflammation, oxidative stress, telomere erosion, or related epigenetic effects [40], which collectively are important mechanisms in pulmonary fibrogenesis typical of IPF. Furthermore, air pollution has been identified as a contributor to an elevated exacerbation risk in bronchiectasis [41] and cystic fibrosis [42], as well as to incident pulmonary sarcoidosis [43]. However, additional studies are needed to allow for a sufficient bulk of data and a broader understanding of these processes.

Ways to reduce air pollution

In spite of whether or not there is exhaustive evidence for the link between air pollution and the development of chronic respiratory diseases, we do not have, to quote Bradford Hill who pioneered the criteria for determining a causal association, the “freedom to ignore the knowledge we already have, or to postpone the action that it appears to demand at a given time.”

Several mitigation and prevention interventions may be proposed to reduce air pollution exposure in order to protect public health, some with strong evidence [44, 45]. The most important are summarised according to the activities sector and type of actor in table 1. Air pollution reduction and improvement in air quality should be advocated through industrial upgrading, agricultural method changes, vehicle and fuel renovation and interventions, healthy city development and intervention at population-based level, which include health education, intensive and individualised intervention in view of lowering of personal exposure, pre-emptive measures, and patient rehabilitation [45].

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TABLE 1

Interventions to improve air quality

Prioritising air pollution reduction measures is in line with efforts to mitigate global warming, which itself presents further pressures on respiratory health, including increased particulate matter, allergens, and heat stress on the cardiorespiratory system. In both cases, delays in action based on misleading focus on uncertainties surrounding a core of solid evidence for causal harm are unacceptable.

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Footnotes

  • Conflict of interest: I. Annesi-Maesano has nothing to disclose.

  • Conflict of interest: F. Forastiere has nothing to disclose.

  • Conflict of interest: J. Balmes is the Physician-Member of the California Air Resources Board, the agency within the California EPA that is responsible for air quality regulation in the state.

  • Conflict of interest: E. Garcia has nothing to disclose.

  • Conflict of interest: J. Harkema has nothing to disclose.

  • Conflict of interest: S. Holgate reports grants from UKRI, during the conduct of the study.

  • Conflict of interest: F. Kelly has nothing to disclose.

  • Conflict of interest: H. Khreis has nothing to disclose.

  • Conflict of interest: B. Hoffmann has nothing to disclose.

  • Conflict of interest: C.N. Maesano has nothing to disclose.

  • Conflict of interest: R. McConnell reports grants from NIH, during the conduct of the study.

  • Conflict of interest: D. Peden has received grant support from NIEHS, EPA and the NSF, but no commercial entity which constitutes a conflict of interest for this manuscript.

  • Conflict of interest: K. Pinkerton has received research funding from the Phillip Morris Research Management Group from 2003 to 2007, educational funds from the American Thoracic Society to teach a postgraduate course in nanoparticle health effects, and a grant support from the National Institute for Environmental Health Sciences and the California Tobacco-Related Research Program to conduct research in models of tobacco-induced disease in rodents and non-human primates.

  • Conflict of interest: T. Schikowski has nothing to disclose.

  • Conflict of interest: G. Thurston has nothing to disclose.

  • Conflict of interest: L.S. Van Winkle has nothing to disclose.

  • Conflict of interest: C. Carlsten has nothing to disclose.

  • Received August 6, 2020.
  • Accepted November 9, 2020.
  • Copyright © ERS 2021.
https://www.ersjournals.com/user-licence

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The clear and persistent impact of air pollution on chronic respiratory diseases: a call for interventions
Isabella Annesi-Maesano, Francesco Forastiere, John Balmes, Erika Garcia, Jack Harkema, Stephen Holgate, Frank Kelly, Haneen Khreis, Barbara Hoffmann, Cara Nichole Maesano, Rob McConnell, David Peden, Kent Pinkerton, Tamara Schikowski, George Thurston, Laura S. Van Winkle, Christopher Carlsten
European Respiratory Journal Mar 2021, 57 (3) 2002981; DOI: 10.1183/13993003.02981-2020

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The clear and persistent impact of air pollution on chronic respiratory diseases: a call for interventions
Isabella Annesi-Maesano, Francesco Forastiere, John Balmes, Erika Garcia, Jack Harkema, Stephen Holgate, Frank Kelly, Haneen Khreis, Barbara Hoffmann, Cara Nichole Maesano, Rob McConnell, David Peden, Kent Pinkerton, Tamara Schikowski, George Thurston, Laura S. Van Winkle, Christopher Carlsten
European Respiratory Journal Mar 2021, 57 (3) 2002981; DOI: 10.1183/13993003.02981-2020
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  • Article
    • Abstract
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    • Not only does ambient air pollution exacerbate asthma but it is also related to new-onset asthma
    • Air pollution confers a greater risk for COPD
    • Air pollution also impacts other respiratory diseases
    • Ways to reduce air pollution
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