Review article
Impact of air quality on the gastrointestinal microbiome: A review

https://doi.org/10.1016/j.envres.2020.109485Get rights and content

Abstract

Background

Poor air quality is increasingly associated with several gastrointestinal diseases suggesting a possible association between air quality and the human gut microbiome. However, details on this remain largely unexplored as current available research is scarce. The aim of this comprehensive rigorous review was to summarize the existing reports on the impact of indoor or outdoor airborne pollutants on the animal and human gut microbiome and to outline the challenges and suggestions to expand this field of research.

Methods and results

A comprehensive search of several databases (inception to August 9, 2019, humans and animals, English language only) was designed and conducted by an experienced librarian to identify studies describing the impact of air pollution on the human gut microbiome. The retrieved articles were assessed independently by two reviewers. This process yielded six original research papers on the animal GI gastrointestinal microbiome and four on the human gut microbiome. β-diversity analyses from selected animal studies demonstrated a significantly different composition of the gut microbiota between control and exposed groups but changes in α-diversity were less uniform. No consistent findings in α or β-diversity were reported among the human studies. Changes in microbiota at the phylum level disclosed substantial discrepancies across animal and human studies.

Conclusions

A different composition of the gut microbiome, particularly in animal models, is associated with exposure to air pollution. Air pollution is associated with various taxa changes, which however do not follow a clear pattern. Future research using standardized methods are critical to replicate these initial findings and advance this emerging field.

Introduction

With increasing urbanization, there is a growing interest in the clinical and public health impact of air quality and the adverse impact of air pollution on health (Orru et al., 2017; Huang et al., 2018; Rajagopalan et al., 2018). Air pollutants consist of a complex mixture of different compounds, including gases (e.g. ozone, carbon dioxide, carbon monoxide, sulfur dioxide, nitric oxide) and particulate matter (heterogeneous mixture of pollen, sulfates, nitrates, polycyclic aromatic hydrocarbons (PAH), metals, ions, organic matter) (Seinfeld and Pandis) that arise from atmospheric oxidation processes, the combustion of fossil fuels and biomass, crustal and road dust resuspension (Belis et al., 2013; Zhang et al., 2017), industrial emissions (Clements et al., 2014; Taiwo et al., 2014) and agricultural emissions (Bowers et al., 2013). The adverse impact of poor air quality on health is far reaching (Salim et al., 2014a, 2014b; Schraufnagel et al., 2019a, 2019b; Schraufnagel et al., 2019a, 2019b). Specifically for human physiological indicators air pollution exposure has been demonstrated to impact blood pressure, heart rate and lung function, but less is understood about the impact of air pollution on the microorganisms surrounding and within us, the microbiome (He et al., 2011; Mordukhovich et al., 2015; Giorgini et al., 2016; Paulin and Hansel, 2016).

A microbiome is the catalogue of genes and genomes of all the micro-organisms inhabiting that specific environment (Marchesi and Ravel, 2015). Highly variable microbiomes are found at different sites in the environment and human body (Bowers et al., 2013; Emerson et al., 2017; Gilbert and Stephens, 2018). The gastrointestinal tract includes several microbiomes, with the largest diversity and abundance of micro-organisms residing in the colon, hereafter referred to as the gut microbiome. Development of the human gut microbiome starts during birth. After profound changes during the first few years of infancy, the mature gut microbiome stays relatively stable within a certain range but continues to vary as it remains prone to changes made by different external environments (Derrien et al., 2019).

Studies of differences in gut microbiomes between health and disease are hardly new, as in the 1680s Antonie van Leewenhoek compared oral and fecal microbiota between healthy and sick individuals (van Leeuwenhoek, Ursell, Metcalf et al., 2012). Recent technology developments in next generation sequencing (NGS) applied to the microbiome field in 16S rRNA sequencing and metagenomics enabled a dramatic expansion in microbiome research. However, to date few studies have focused on the impact of air quality on the human gut microbiome (Valles and Francino, 2018).

Air quality is expected to influence the gut microbiome because in some environments there is continuous exposure to high concentrations of airborne pollutants (Salim et al., 2014a, 2014b), such as in polluted urban areas (Hand et al., 2014; Zheng et al., 2016), near roadways (Apte et al., 2017), and in some indoor environments (Koehler et al., 2019). Of specific interest to this summary are microbes suspended in air with other air pollutants. The outdoor air microbiome varies biogeographically (Perring et al., 2015) and with meteorological conditions (Bowers et al., 2013), while the indoor air microbiome depends on building inhabitants, their activities (Barberán et al., 2015; Prussin and Marr, 2015), ventilation system design, building dampness, and the outdoor air microbiome. Airborne particles and microbes reach the gastrointestinal (GI) tract after ingestion of food and water containing such particles or after mucociliary transport mechanisms that expel them from the lungs following deposition during inhalation (Fig. 1) (Moller et al., 2004).

Reports of associations between air pollution and GI system diseases suggest a causal effect (Ananthakrishnan et al., 2017; Shouval and Rufo, 2017). Rodent studies of dietary- and inhalation-based exposure to particulate matter demonstrate toxic impacts of particle exposure in the gastrointestinal organs and the liver (Moller et al., 2008; Li et al., 2015). Epidemiologic studies of various gastrointestinal diseases have identified relationships between: ozone and appendicitis (Kaplan et al., 2009; Kaplan et al., 2013); carbon monoxide and gastroenteric disorders (Orazzo et al., 2009); various air pollutants and irritable bowel diseases (Kaplan et al., 2010; Ananthakrishnan et al., 2011; Opstelten et al., 2016); abdominal pain and carbon monoxide, nitrogen dioxide, sulfur dioxide, and PM2.5 (Kaplan et al., 2012); gastric ulcers and PM2.5 (Wong et al., 2016); and gastric cancer and PM2.5 (Nagel et al., 2018), as well as sulfur and zinc components of PM2.5 (Weinmayr et al., 2018).

Additional research is needed to determine mechanisms leading to observed relationships between gastrointestinal diseases and air pollution, though some hypotheses have been proposed (Beamish et al., 2011). Relationships between gaseous oxidants, such as ozone, and inflammation-related GI disorders may occur due to inhalation of oxidants leading to systemic inflammation, akin to what is observed in cardiorespiratory health effects of oxidant exposure. Particulate matter deposition in the lungs may also contribute to systemic inflammation, but particles also enter the GI tract as they are expelled from the lungs via mucociliary transport and are subsequently swallowed. During this transport, particles may interact with epithelial cells leading to the observed GI system health effects. For example, Wong et al. (2016) suggest PM2.5 interactions with the gastric mucosal defense system may lead to formation of ulcers (Wong et al., 2016). While there is suggestive evidence of a relationship between both gaseous and particulate air pollution and gastrointestinal diseases, the role of the human gut microbiome and how it may be modified by air pollutants in the pathogenesis of such diseases remains largely unknown.

The goal of this review was to summarize the existing reports on the impact of indoor or outdoor airborne pollutants on the gut microbiome of animals and humans, and to outline the challenges and suggestions to expand and improve this field of research.

Section snippets

Data sources and search strategies

A comprehensive literature search of several electronic databases from inception to August 9, 2019 was conducted. The search included animal studies, limited to English language. The databases included Ovid MEDLINE(R) and Epub Ahead of Print, In-Process & Other Non-Indexed Citations and Daily, Ovid Embase, Ovid Cochrane Central Register of Controlled Trials, Ovid Cochrane Database of Systematic Reviews, and Scopus. The search strategy was designed and executed by an experienced librarian

Study identification

A total of seven hundred and eighty-two potentially relevant studies were identified through database searching and an additional 396 were identified through other methods (Fig. 2). After the first screening, forty-five articles were included in the full text review. Thirty-five articles were excluded after full text review: thirteen did not meet the inclusion criteria, seven were review articles, fourteen were conference abstracts and one was a book. This process yielded 10 original research

Discussion

In the present review, we applied rigorous methods to evaluate current knowledge on the associations between air quality and gut microbiome. Our search identified a small number of animal and human studies, which lend themselves to a narrative summary but not to a systematic review. As the impact of air quality on human health is increasingly recognized, we deemed it important to summarize the emerging evidence pertaining to the link between the microbiome and air quality. Findings from both

Conclusion

This comprehensive literature review indicates that exposure to air pollution is associated with a mildly altered composition of the gut microbiome, particularly in animal models. Air pollution is associated with various changes in taxa abundance, though there is little consistency between the studies. As there are few relevant studies available, future research using advanced methods will be critical to potentially replicate initial findings and identify new leads to advance the emerging field

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgments

We thank Deborah Strain for secretarial assistance. This research was made possible by the support of Delos Living, LLC and Mayo Clinic. The sponsors had no oversight of the content of the manuscript.

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