12 November 2020

A breath of fresh microbes

Allergies Asthma Clinical Respiratory

The concept of microbiomes and their effect on human health has gained mainstream credibility over the past decade – just look at the kombucha aisle in your supermarket.

Microbiomes of the gut and the skin, in particular, and their interactions with other organs, have been increasingly linked to human health status.

Now, most recently, scientists have begun investigating at another microbial community, called the aerobiome – that is, the airborne microbial communities we live in and breathe in every day.

Recent research by scientists from the University of Tasmania has found urban environments alter people’s exposure to the aerobiome, which has potentially important, but underexplored, health impacts.

“People living in urban environments can inhale approximately 100 million bacteria each day. This microbial exposure helps shape our internal microbiomes and seems to be connected to the rise in allergic and inflammatory diseases in urban areas”, says Emily J. Flies, lead author and lecturer at University of Tasmania’s School of Natural Sciences.

Researchers examined various studies that compared the abundance and diversity of airborne fungal and bacterial communities and its health effects across urban and rural areas.

But the potential health impacts are hard to estimate as to date there has been no synthesis of how urban aerobiomes are different, particularly with respect to the diversity and abundance of microbes.

While many studies have examined indoor microbiomes, this research study explores outdoor microbiomes in cities. “Outdoor microbiomes in urban areas contribute substantially to the indoor microbiomes and impact our health, but not much is known about them. So we chose to focus on that knowledge gap,” Flies tells Allergy and Respiratory Republic.

The study indicates that urban aerobiomes differ in ways that may have adverse impacts on health.

“However, there is significant variation in land use within urban areas and presumably important differences in aerobiome composition as well. For example, in our 2017 study and 2019 study, we showed biodiverse urban green spaces may be able to alter the aerobiome in localised ways that benefit health,” says Flies.

Researchers predicted that urban aerobiomes would have lower abundance and diversity of microbes compared with rural areas. They say it is important to acknowledge the extreme ecological variability within the coarse categories of “urban” and “rural”.

“Given that land use and land cover can impact on aerobiomes at even fine scales e.g. 50 metres, these landscape categories are an extremely rough metric with which to make comparisons. However, urban areas consistently differ from rural areas in having less dirt, and vegetation exposed to the air, and these are two of the main sources of airborne microbes,” explains Flies.

Fit to breathe

There is still debate over how to characterise “healthy” microbial exposure. The “hygiene hypothesis” suggests that exposure to an abundance of microbes can prevent allergies, while other studies have shown that exposure to an abundance of certain microbes, fungi in particular, can promote or exacerbate allergies or asthma.

In contrast, the “biodiversity hypothesis” suggests that exposure to a diversity of microbes is key to healthy immune system development. There is empirical support for both of these hypotheses, so researchers explored the abundance and diversity of the urban aerobiome.

Consistent with expectations, researchers found 57% of the studies identified higher levels of airborne microbes (more abundant microbes) in rural areas, where soil and vegetation can more easily contribute microbes to the air, compared with urban areas. Approximately 22% found that microbes were more abundant in urban areas and 22% found no difference.

“Microbial diversity was under-reported in studies, but when those comparisons were made (in 12 out of the 30 analyses examined), 67% found the rural aerobiomes to be more biodiverse, four studies (33%) found no difference in diversity, and no studies found diversity to be higher in urban areas.

“Only two studies experimentally examined the impact of urban and rural aerobiomes on human health outcomes; both found rural aerobiomes shifted immune function away from allergic (Th2-type) responses,” Flies tells ARR.

Another study has shown that after exposure to urban green spaces (air, leaves and soil) there was a higher diversity of microbes on the skin and in the nose of humans.

“Diversity in the aerobiome and other environmental sources can directly affect diversity of the human body. It has been hypothesised that exposure to higher diversity outdoor environments can reduce immune responses to harmless substances, thus reducing the chance of an allergic reaction, for example, to pollens.

“This is especially important during intense early-life immune system training, where the immune system determines what is and is not a threat to the body. This can play a role in long-term health outcomes i.e. prevalence of non-communicable diseases,” says Caitlin Alyssa Selway, lead author of that study and doctorate candidate at the Department of Molecular and Biomedical Science at the University of Adelaide.

The study also noted microbial diversity on the skin and nose would deplete by the next morning or following a shower.

“This suggests that outdoor exposure needs to occur almost daily to maintain high diversity for the skin and nose. However, more testing is required to determine if more exposure will reduce the chance of developing immune-mediated diseases, such as allergies, asthma, and atopic dermatitis,” Selway tells ARR.

The study also suggests ways – such as eating from home or community-planted vegetable gardens, incorporating indoor plants into an office space or at home, planting roof-top gardens on apartment buildings, or living with a dog that spends time outdoors – to increase outdoor exposure and subsequent diversity.

What doesn’t kill you

The Colorado State University’s Aerobiome Discovery Network (ADN) defines the aerobiome as the compilation of airborne microorganisms.

“The dispersal, transmission and exposure of these microorganisms can have significant consequences, particularly in the spread of disease, but also potentially culminating in non-pathogenic exposures that may have variable consequences on health,” one of ADN’s principal investigators, Angela Bosco-Lauth, tells ARR.

“For example, human pathogens such as Coxiella burnetii, which cause the zoonotic disease Q fever, have been known to spread on air currents for several kilometres. Highest infection risk occurs within 5km of sources in rural areas and over smaller distances in urban areas.

“However, what we don’t know is if exposure to airborne microbiota could have health benefits, such as stimulation of the immune system through small-scale exposures.”

She says diversity may actually lead to increased incidence of disease.

“But again, non-pathogenic exposures could have a more positive impact, such as increasing the diversity of epitopes that lead to immune tolerance,” she says. “For example, there is a hypothesis that repeated low-level exposure to certain microorganisms can allow the host to develop immunity without overwhelming the body with a true infection.

“But for airborne microorganisms, this concept deserves further investigation and proof. We know that airborne microorganisms can have specific impacts on health and the environment, for example by pathogen transmission and ice nucleation, but we really don’t understand how or if airborne organisms interact with each other or what other roles they may play.”

While the aerobiome may not be a well-defined concept, the air we breathe contains a lot of particles and gases, which have potential effects on health, says Guy Marks, head of the Respiratory and Environmental Epidemiology group at the Woolcock Institute of Medical Research in Sydney.

He says these particles and gases can be divided into three categories:

First, biological particles that cause diseases such as influenza, tuberculosis, SARS and COVID-19, which are transmitted via the air from person to person.

Second, environmental pathogens in water sources and soil, for example Legionella bacteria in the airconditioning systems of large buildings.

Third, biological pathogens that cause disease through other mechanisms, including allergens from dust mites, pollen, moulds and animal dander.

Besides the above, there are aerobiological threats that occur from the environment and through non-infectious sources of disease.

“For example, thunderstorm asthma when an aeroallergen like ryegrass [Lolium perenne] pollen grains, ruptured by rain and moisture, releases fine allergen-bearing starch-granules,” says Marks, who is also President of the International Union Against Tuberculosis and Lung Disease. “When inhaled into the airways these tiny allergenic particles cause very severe attacks of asthma in susceptible individuals. One such event resulted in 10 deaths in Melbourne in November 2016.”

Carbon-based particles from diesel and other internal combustion engines, and combustion of vegetation as in forest fires, can also be inhaled with detrimental health effects. People may be exposed to occupational hazards whereby chemicals, asbestos, heavy metals, pesticides and other substances can be inhaled, causing harm to lungs and other organs.

Australians, on average, spend more than 90% of their time indoors, be it in homes, schools, recreational buildings, restaurants, public buildings, offices, or inside cars. But the importance of indoor air quality is often overlooked. By 2061, an estimated 74% Australians are expected to live in a capital city.

Back in 1998, the CSIRO estimated that the cost of poor indoor air quality in Australia may be as high as $12 billion per year. In 2015, nearly 2,600 (1.6%) deaths and 0.8% of the burden of disease in Australia was attributed to (particulate matter) PM2.5 air pollution.

“Fine airborne particles, PM2.5, can penetrate deep into the airways and lungs, inducing oxidative stress and inflammation and even translocate into the bloodstream causing adverse health consequences. These particulates can decrease lung function, cause chronic obstructive pulmonary disease, cardiovascular and cardiopulmonary diseases and mortality”, says Sotiris Vardoulakis, Professor of Global Environmental Health at the Australian National University in Canberra.

“Increasing airtightness of dwellings could have negative effects by increasing indoor concentrations of pollutants, such as PM2.5, carbon dioxide and radon, derived from indoor or ground sources, and biological contamination.

“Climate change may further exacerbate aerobiome-related health risks with changes to the indoor environment that can affect indoor air quality or promote the growth and propagation of pathogenic organisms. Therefore, we need well-designed urban green spaces and energy efficient buildings, which can help mitigate climate change and at the same time improve outdoor and indoor air quality,” Vardoulakis tells ARR.

However, there is a lack of empirical studies directly testing how human immune systems respond differently to aerobiomes from urban and rural areas.

“Such studies are necessary to help characterise the important features of aerobiomes, for example abundance, diversity and/or the presence of certain microbes or categories of microbes, before we can begin to apply this knowledge in ways that can benefit human health,” says Flies.

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