The COVID-19 global pandemic has put a strong lens on hygiene and the identification of risks that cause transmission of infection and disease. Of course COVID-19 is not the only airborne virus that the human population has to contend with. The air around us may appear to be clean, but it carries many types of microscopic particles, such as mineral particles, water droplets, pollen, various kinds of biological material and man-made pollutants, all of which cannot be seen by the human eye. These particles can transport microorganisms, allergens and toxins that cause a wide range of diseases in both humans and animals.
With the world caught in the midst of the COVID-19 pandemic and many scientists and governments engaged in debates over the routes of infection (droplet, fomite and aerosols) and means of protection, it’s timely to review how diseases can be transmitted through the air.
How particles become airborne
On a large scale, dust particles and liquid droplets can become airborne by mechanical action caused by fast-moving water and wind or other physical disturbance. Due to their small size and the action of air currents, they can remain suspended in the air for long periods and be carried large distances.
There are several ways in which infectious particles can become airborne.
- Physical disturbance such as sweeping floors, pouring liquids or solids, spraying, grinding, drilling, ploughing fields
- More specific industry-related disturbance: waste-sorting, composting, agricultural and food processing
- Wind outdoors or indoors
- Flushing toilets
The term bioaerosols is used to describe the small particles (0.001–100μm) that originate from plants or animals and contain organic matter, including living or dead pathogenic microorganisms.
On a smaller scale, human and animal respiratory activity – breathing, talking, shouting, singing, coughing, sneezing – creates droplets of varying sizes. It is well known that diseases such as chickenpox, flu, measles, mumps, whooping cough and tuberculosis are transmitted by inhaled airborne particles. But with recent pandemics such as the current COVID-19, SARS (caused by the same coronavirus species as COVID-19, but a different strain), MERS and swine flu, there has been greater interest in identifying all the routes of transmission and much research conducted into the potential role of airborne transmission.
Until July 2020, WHO based its advice for Personal Protective Equipment (PPE) for COVID-19 on direct droplet (>5µm) spread to a mucosal surface (eyes, mouth, nose) and indirect spread via contaminated surfaces only. Following an open letter signed by over 200 scientists urging the recognition of the potential for airborne spread of COVID-19 in microscopic respiratory droplets (termed microdroplets or aerosols), WHO has since acknowledged the possibility.
Inhaling airborne particles
A review by WHO of the dangers of airborne dust showed that the larger airborne dust particles (> 30μm) that are inhaled are mainly caught in the upper airways, especially when breathing through the nose with low breathing rates. They’re caught in the mucus lining the nasal passages and can be expelled.
The particles of medium size are caught in the airways between the head area and the upper lungs. These can also be easily ejected by the action of the cilia (hair-like cells) that line the air passages and mucus. This action is impaired by smoking, however.
The particles that reach the deepest part of the lungs, the alveolar region, are mainly less than 10μm in size. The particles deposited there peak at 2μm while smaller particles tend to be exhaled again. Breathing through the mouth greatly increases the amount of dust and larger particles deposited in the lower airways.
Infectious particles or droplets that are breathed in and trapped on mucus membranes in the mouth, nose, throat and lungs, however, can infect the tissues at that point, depending on the microorganism.
Exhaling infectious aerosol particles
Studies on patients with influenza show that low-speed air flow produced by inhaling and exhaling can create aerosol particles in the lungs and emit them in exhaled breath. Coughing produces a large number of influenza virus particles in each cough. Breathing was found to expel fewer virus particles per breath, but as it’s done more frequently than coughing, it produces a greater quantity of infectious material overall.
Coughing and sneezing produce high-speed air flow through the lungs, throat, nose and mouth. This can dislodge infected droplets of mucus and saliva and project them at high speed into the surrounding air. These droplets range in size from large visible blobs that quickly land nearby, to microscopic particles at micrometre scale that behave like clouds and swirl through the air for several metres. The air flow speeds for different respiratory activities have been measured.
- Breathing: up to 1m/s
- Talking: 5m/s
- Coughing: 2–50m/s
- Sneezing: >100m/s
High-speed videos taken by researchers at MIT show that coughs and sneezes produce gas clouds in addition to flying droplets and sheets of mucus and saliva. They found that tiny droplets in the clouds travelled 5–200 times further than previously thought. The turbulence of the cloud keeps the smaller droplets suspended while the larger ones fall out. As droplets move through the air, they evaporate and shrink, which can leave behind droplet nuclei small enough to float through the air and be carried on air currents inside or outside buildings.
The MIT research showed that droplets 100 micrometres (about the width of human hair) in diameter travelled five times farther, while droplets 10μm in diameter (size of a typical cloud droplet) travelled 200 times further. Droplets smaller than 50μm in size can remain airborne long enough to reach ventilation systems where they can be spread farther around a building.
Several studies have found viable flu virus particles in respiratory droplets of these sizes and recently (July 2020), viable SARS-CoV-2 particles were also found in respiratory aerosol droplets produced by breathing, vocalisation (talking, shouting) and coughing.
Factors affecting infection risk
Multiple factors affect the infection risk and even the distance particles travel is also affected by numerous variables – not just their size and the effect of gravity.
- Distance from the infected person
- Length of time spent in the vicinity
- Infectious dose produced by an infected person
- Density of infectious particles in the air – and viral dose received
- Airflow in the vicinity
- Type of bacteria or virus — the viability and quantity of organisms needed to cause an infection vary greatly
- Particle aerodynamics, including diameter shape, velocity, electrical charge, composition, density
- Temperature and humidity
Not all people infected with viruses such as flu or coronavirus are infectious. There are critical periods during illness when virus production peaks. Less than half of flu patients released flu viruses into the air in a study by Wake Forest Baptist Medical Center. Around a fifth of patients studied were classified as “super spreaders” or “super emitters” because they produced up to 32 times more viruses than other emitters. They also had more severe illness, producing greater viral load in their bodies.
Studies of patients with COVID-19 have found differences in the viral output between patients of more than two orders of magnitude (x100), with the “super spreaders” achieving an output of over 100,000 virions per minute of speaking.
Toilet flush and the spread of pathogens
The risk of airborne disease transmission from toilets, even from one building to another through the sewerage system, was first demonstrated in 1907. In an experiment in the 1950s, a toilet was seeded with bacteria and agar plates used to collect aerosols settling out of the air. This found that the amount of aerosols increased with increasing flush energy and that the bacteria were still in the air eight minutes after the flush.
Airborne pathogens obtained from toilet plume
Research has shown, directly or indirectly, that several types of bacteria and viruses can contaminate the air from a flushing toilet.
- E. coli: In the 1970s, it was discovered that aerosols containing E. coli bacteria remained airborne and viable for at least 4–6 hours after flushing. In another experiment, toilets seeded with a bacterium and a virus (MS2 bacteriophage and poliovirus) were not completely free from the microorganisms after seven flushes and attempts to clean the bowl were only minimally effective in eliminating them.
- Salmonella: More recently, in 2000, it was found that Salmonella could be cultured from air samples near a toilet bowl after flushing. Salmonella also remained in the bowl water for more than 12 days and in a biofilm below the water line for 50 days after seeding the toilet with the bacteria. This shows that a biofilm may be able to maintain a supply of bacteria that infects the toilet bowl water and the aerosols created on flushing for much longer periods.
- Norovirus: The spread of Norovirus on ships, even after attempts to sanitise them following an outbreak, is thought to be a result of the ability of toilets to continue generating contaminated aerosols after multiple flushes and the resistance of Norovirus to cleaning and disinfection.
- Influenza: Some patients infected with the H1N1 strain of flu virus have diarrhoea and the virus has been detected in stool and urine, which means there is potential for airborne transmission by toilet plume.
- Coronavirus: SARS-CoV-1 was found by WHO to be the cause of a ”superspreading event” in a Hong Kong apartment that resulted in 342 people becoming infected and 42 deaths. The Hong Kong government found that the spread of the virus was likely caused by virus-laden aerosols originating in the sewage system and drawn through dry U-bends in the bathroom floor drains of other apartments by bathroom exhaust fans. Some aerosol particles may have then have been expelled to the outside of the multistory building and carried upward to other apartment blocks.
The ability of viable microorganisms to be spread through a waste water plumbing system by aerosols was later confirmed in an experiment that set up a full-scale, two-floor test rig. This showed the dangers of interconnected systems and the need to design plumbing systems to prevent contaminated aerosols escaping in different parts of a building.
What are dust particles?
Dust is considered to consist of solid particles with dimensions ranging from below 1 μm to at least 100 micrometres in diameter. Particles greater than 50μm diameter do not remain airborne for long in still air, dropping about 7cm per second. Larger airborne particles can stay in the air longer, however, depending on origin, physical characteristics and ambient conditions. The settling rate for airborne dust particles less than 1μm in size is considered to be negligible, so effectively float in the air.
In urban areas, a large proportion of dust is from vehicles and industrial pollution. There are also cases where desert sand has been carried by wind – even across the Atlantic from the Sahara. Vast areas of forest are burnt each year, generating enormous quantities of smoke that can spread hundreds or thousands of miles away.
In 2019, hundreds of thousands of fires were detected by satellite in Siberia, Indonesia, Brazil, sub-Saharan Africa and Australia. The smoke from fires in Siberia was estimated to cover an area the size of the 27 EU countries.
There are many types of dust in the natural and human environment and a wide range of health problems caused by them. Examples of materials in airborne dusts (also termed suspended particulate matter) that can cause health problems include the following.
- Minerals: crystalline silica, coal, cement
- Toxic metals: lead, cadmium, nickel, beryllium
- Other chemicals: many bulk chemicals, pesticides
- Organic dusts: flour, wood, cotton, tea, pollen
- Biohazards: bacteria and viruses, moulds and spores (infection and allergies)
- Sand and soil
- Volcanic ash
Farming activities can generate large amounts of inorganic and organic dust from ploughing, combine harvesting, grass cutting and moving grain. Cleaning and maintenance activities in buildings can generate dust by activities such as sweeping and drilling. Infestations of birds and rodents can result in a build-up of material with hazardous microorganisms such as Salmonella and Leptospira, which can become airborne when disturbed.
Microbes in dust
People in the developed world spend most of their lives inside buildings and yet relatively little is known about the microbes commonly present in homes and offices. A study of 1,200 homes across the US found that there were distinct bacterial communities inside and out, but that fungal communities found inside were more related to those found in the environment outside the home.
The fungal communities varied with climatic and geographical region, but the bacterial communities in dust found indoors were dependent on the number of people, the female-male ratio and the presence of pets. Other studies have found a relationship to household insects, differences in ventilation, building design, the environmental characteristics found in buildings and prior water damage from flooding.
Fungi that were more abundant in the home than outdoors included common household moulds such as Aspergillus and Penicillium. Bacteria found indoors were mainly associated with human skin (such as Staphylococcus or Streptococcus) and faeces. There were also different bacteria if women were present (Lactobacillus, Bifidobacterium, for instance) and in male-dominated households where there were more Corynebacterium, Dermabacter (skin-associated) and Roseburia (faecal-associated) bacteria. When pets were present, bacteria associated with mouths and faeces of dogs and cats were more abundant.
Wind-borne dust and risks of disease
[Image: NASA simulation showing: dust blown from the Sahara westwards across the Atlantic; smoke from the Pacific northwest blown east to Europe, together with salt spray from the north Atlantic Ocean. Source: NASA Goddard Space Flight Center (https://svs.gsfc.nasa.gov/12772)]
Wind can carry microorganisms from soil into the local environment and over long distances in dust. A genetic analysis of dust particles up to 10 micrometres extracted from a Beijing smog found a common soil bacterium was the most abundant microorganism. Pneumonia-causing Streptococcus pneumonia and the allergenic fungus Aspergillus fumigatus, along with faecal bacteria, were also present. Air sampled in urban Milan found 10,000 microorganism particles per m3 of air, consisting mainly of soil-inhabiting bacteria and chloroplasts from plants.
Dust storms in Africa and Asia have significantly increased in recent years, with storms in the Sahara affecting southern and central Europe, the Caribbean and Florida — where half of airborne particles in summer come from North Africa. Saharan storms have been shown to cause an increase in asthma in Greece, Italy and Trinidad.
Other studies have shown Asian dust storms have increased respiratory diseases, including asthma in east China, the Korean peninsula, Japan, Kuwait and Iraq. Asthma-causing allergens found in desert dusts include fungal spores, dust mites, pollen, pollutants and organic detritus, with house dust mites the major cause. Microorganisms in dusts have been shown to withstand harsh environmental conditions of transport through the atmosphere of high and very low temperatures, UV radiation and desiccation. Avian flu has also been linked to dust storms from central Asia.
Kawasaki disease is a sometimes fatal condition that causes inflammation of the blood vessels in young children. It is thought to be triggered by respiratory viral infections. Outbreaks have been linked to winds blowing from central Asia across Japan and reaching as far as Hawaii and California. Rapid increases in cases among young children and adolescents were linked to the influenza H1N1 pandemic in 2009 and more recently to the COVID-19 pandemic.
Can fungal spores cause disease?
Fungal spores are common in the outdoor and indoor environment. Many species of fungus have tiny spores that disperse through air currents, which also means the spores are of suitable size (a few micrometres) to be inhaled into the lungs. Fungi feed on organic matter, so any organic material with warm and moist conditions can provide a growing medium.
The good news is that healthy people are unlikely to be affected in normal conditions where the concentration of spores in the air is low and the species present are not regarded as pathogenic. There are situations, however, where the concentration of spores and the species of fungus greatly increase the risk of infection or an allergic reaction causing asthma.
The most common fungi that cause disease are as follows.
- Aspergillus fumigatus: very widespread in soil and most decaying organic matter and can cause a group of conditions called aspergillosis – the most common cause of airborne fungal disease; it can affect lungs, eyes, skin, sinuses and other organs
- Histoplasma capsulatum: thrives on bird and bat droppings and can survive for years in dry conditions
- Cryptococcus neoformans: present in pigeon and bat droppings and can cause a serious illness called cryptococcal meningitis in some people
In the outdoor environment, fungal spores are produced on decaying organic matter such as compost, manure, hay, grass, soil, dead wood, fallen leaves, rotting food, faeces, dead animals, and living plants infected with parasitic fungi. Any disturbance of these can create a high concentration of spores in the air.
In the indoor environment, there are many products used in buildings on which fungi will grow if they are wet or damp, including:
- soil in potted plants
- bathroom fixtures such as shower heads and curtains
- carpets and furniture
- food and food waste
- paper and cardboard products
- textiles and leather
- moist surfaces such as walls
Conditions that produce damp or wet conditions and encourage growth of fungi are:
- poor air circulation
- direct spray around showers, on curtains and walls
- condensation on windows, walls and ceilings
- leaking plumbing and drainage systems
- air conditioning and heating systems
- roof leaks
- ground seepage through walls and floors
All these can be prevented by ensuring adequate ventilation and maintenance of buildings and fittings.
Wind-borne fungal spores
Wind-borne fungal spores lifted from soil can also be a health threat over large geographic areas, but has been little studied. In some arid areas of California, Utah, Nevada, Arizona, New Mexico and Texas, an infection called Valley Fever or desert rheumatism caused by airborne spores of a soil fungus, Coccidioides immitis, causes around 2,000–20,000 reported infections a year, but is thought to be widely under-reported. The fungus is also known to be present in Washington, Mexico and parts of South America.
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