Impact of air pollution on intestinal redox lipidome and microbiome
Graphical abstract
Introduction
Air pollution has long been recognized as a risk factor for multiple diseases, increasing hospital admissions and all-cause mortality [1]. The World Health Organization ranks it as the 13th leading cause of worldwide mortality [2]. Cumulative evidence over the last two decades has linked air pollution with respiratory diseases such as asthma [3], cardiovascular diseases such as myocardial infarction and stroke [4], metabolic disorders such as obesity and diabetes [5], and cancers [6]. Air pollution is composed of a number of substances including gaseous components (e.g., carbon monoxide, carbon dioxide, ozone, nitric oxide, and sulfur dioxide), volatile organic compounds (e.g., benzene, acetone, and ethyl acetate), and particulate matter (PM), each of which has deleterious effects on human health [7]. The specific composition of air pollution varies across different locations, which results in great difficulties in the standardization of air pollution components and study design. The two most studied air pollutants are ozone and PM. Ozone-induced inflammation and tissue damage lead to the breakdown of tight junction integrity and increased cell permeability, which has been observed in both humans and animal models [8]. PM, the major component of adverse health effects by air pollution, contains a mixture of pollen, sulfates, nitrates, organic carbon, mineral dust, polycyclic aromatic hydrocarbons (PAHs), metals, ions, microbial particles, and spores, etc [9]. Sources of PM range from the combustion of fossil fuels (e.g., diesel exhaust, industrial emissions) to road dust and windblown soil [9]. According to the particle diameter, PM can be sub-classified into three categories, ultrafine particles (UFP, diameter <100 nm), fine particles (PM2.5, diameter < 2.5 μm), and coarse particles (PM10, diameter < 10 μm) [9]. PM with different sizes appears to possess different abilities to cause harmful effects. There is increasing evidence that particles with a smaller size pose a higher risk because of their high content of organic chemicals and pro-oxidative potential [10]. For example, UFP-exposed mice seem to develop accelerated atherosclerosis as compared to the PM2.5-mice [11].
In comparison to a plethora of studies investigating air pollution-mediated respiratory and cardiovascular diseases, there remains a paucity of literature examining the impact of air pollution on the intestinal system. With increasing epidemiological studies linking air pollution with pathologies of the gastrointestinal (GI) tract, how air pollutants exert their effects on the intestinal system has gained more attention in recent years. The GI tract is readily exposed to air pollutants through direct or indirect routes. Inhaled particles are quickly cleared from the lungs to the intestine by mucociliary transport [12]. After the initial inhalation, the localization of the inhaled particles varies depending on their size. Larger particles are more likely sequestered in the upper respiratory tract or the conducting lower airway, while smaller particles, especially those with an average diameter of less than 2.5 μm, could be engulfed by macrophage in the bronchioles and alveolar spaces [13]. The particles sequestered by the macrophages adsorbed in the mucus layer of the lower airways are then transported back to the oropharynx and consequently swallowed into the GI tract [14]. Another mechanism whereby PM gains access to the GI tract is by the direct dietary ingestion of food and water contaminated with urban and industrial air pollutants [15]. Within a typical Western diet, an individual consumes nearly 1012-1014 particles per day [16,17]. In addition, gaseous pollutants can also exert an impact on the GI tract through the induction of systematic inflammation [18]. Thus, the GI tract might be an important organ system in which air pollution incurs local inflammatory and redox responses, along with changes in the microbiota diversity (dysbiosis) to release cytokines and lipid metabolites to the systematic circulation. In this review, we introduce the links between air pollution and intestinal diseases, followed by highlighting the impact of air pollution on intestinal lipidome and microbiome.
Section snippets
Epidemiological associations between air pollution and intestinal diseases
Air pollution exposure has been associated with numerous intestinal diseases, including appendicitis [19], inflammatory bowel disease (IBD) [20], and colorectal cancer [21]. A study by Gilaad et al. analyzed 5191 adults who had been hospitalized with appendicitis between 1999 and 2006 by estimating the odds of appendicitis under short-term exposure of specific air pollutants, including gaseous components ozone, sulfur dioxide, nitrogen dioxide, carbon monoxide, and PM less than 10 μm and 2.5 μm
Impact of air pollution on intestinal redox lipidome
In addition to the liver and the adipose tissues, the intestine is a major organ system of lipid metabolism. One of its most important functions is the absorption of cholesterol. Nearly 30% of the cholesterol needed by the human body derives from the absorption of dietary or biliary cholesterol by the small intestine [31]. Intestine enterocytes also synthesize endogenous cholesterol [32]. Apolipoprotein A-I (ApoA-I) produced by the intestine accounts for approximately half of the total plasma
Impact of air pollution on the intestinal microbiome
More than 1014 microbes reside in the human GI tract and the collective genome of them is over 150-fold greater than that of its human host [69]. The human microbiome is mostly comprised of two major phyla, Bacteroidetes and Firmicutes, and several other phyla including Proteobacteria, Actinobacteria, Verrucomicrobia, Cyanobacteria, Fusobacteria, as well as the domain Archaea [70]. Accumulating evidence supports that the gut microbiome plays a crucial role in the development of many diseases,
Conclusions and future perspective
Air pollutants enter the GI tract either through the mucociliary clearance of inhaled pollutants or the intake of contaminated food and water. Once in the GI tract, air pollutants might have a direct effect on the intestinal epithelium where oxidation of intestinal lipids develops. Air pollutants can also impact the intestinal microbiota, thereby compromising the integrity of the intestinal barrier or producing various microbial metabolites that are released into the circulation to modulate
Declaration of competing interest
The authors declare no conflicts of interest.
Acknowledgement
This work is supported by the Startup research fund of Shenzhen Technology University for Rongsong Li and (LR&D MERIT REVIEW AWARD (I01 BX004356-01 and NIEHS R01ES029395 for Tzung Hsiai).
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