President, British Aerobiology Federation, IACR-Rothamsted, United Kingdom
Published in: R. Spiewak (Editor): "Pollens and Pollinosis: Current Problems". Institute of Agricultural Medicine, Lublin (Poland) 1995, pages 11-15.
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There is a wide range of different components in the air we breathe, many of which can have important effects on the health of man and animals, both individually and through their interactions. They range from inorganic gaseous and particulate pollutants through microbial constituents to the pollens of higher plants. They differ chemically as well as in size, patterns of occurrence, concentration and the nature of their health effects. In this brief introduction to the Symposium on Pollens and Pollinosis, I wish to place the occurrence of pollens and pollinosis in the context of the total air biota and pollutants and their health effects, to show the relative importance of the different components both in the air spora and as allergens. I will also describe how numbers and types change with environmental and other factors, especially between outdoors and indoors.
Particulate pollutants important in aerobiology include smokes, dusts and diesel particles, condensation nuclei, radionuclides and pesticides. These may be carried on microbiological particles and also affect their viability. Individually, smoke particles are 0.001-0.1 µm diameter and condensation nuclei 0.1-20 µm allowing deep penetration into the lung but transport on other particles could alter their site of deposition. Much concern is felt at the risks presented by these man-made pollutants, some of which are thought to be carcinogenic.
Gaseous pollutants include ozone, carbon monoxide, nitrogen oxides and sulphur dioxide. Some of these are considered to provoke asthma but recent work in Mexico has shown that sulphur dioxide and nitrogen oxides interact with biological pollutants, both pollens and fungi, in provoking asthma while ozone show little correlation with asthma admissions to hospital.
Viruses and bacteriophage are often released into the atmosphere from human and animal sources and from sewage, but occasionally also from plant sources and through their application as biocontrol agents. Individual virus particles are 0.015-0.45 µm diameter but are usually airborne in larger particles as a result of aerosolisation in mucous or saliva expelled during coughing, sneezing and talking or in water when liquid films break during laboratory procedures or the processing of sewage. There is little data on the occurrence of viruses in air.
Bacteria are less numerous in the air than fungi. Single cells are 0.3-10 µm diameter but, like viruses, are probably rarely airborne as single cells but carried on rafts of plant material or skin squames or protected by solutes from the original aerosol droplet. Bacterial numbers are also larger in cities (up to 4000 m-3, average 850) than in rural areas (up to 3400 m-3, average 99). Plants are probably the most important sources of bacteria in the ambient air but other sources include soil cultivation, animal houses and the disposal of sewage and farm wastes.
Actinomycetes are bacteria which produce spores well-adapted for airborne dispersal, both singly and in aggregates. They are produced in largest numbers from mouldy stored products that have heated spontaneously to temperatures up to 65-70°C and can give concentrations up to 1010 spores m-3 in indoor environments where they have been implicated as causes of different forms of allergic alveolitis, including farmer's lung, bagassosis and, perhaps, mushroom worker's lung. They are few in number in outdoor air.
Fungi are ubiquitous in the environment but the major source for the air spora is undoubtedly growing plants and their decaying litter. Cladosporium and Alternaria are important colonisers of fresh plant litter and, with Sporobolomyces, of plant surfaces. They form the most numerous airborne fungal spore types through most of the world overall although they may be exceeded by other types in some regions or seasons. Soil also contain large numbers of microbes, including fungi, but these mostly only become airborne when soils are dry enough and winds strong enough for the soil to be blown. Fungi are much more numerous in the air than pollen grains but their smaller sizes (1-100 µm) means that their volume contribution to the bioaerosol is probably of the same order.
Maximum concentrations are about 106 spores m-3 air but are more usually about 104-105 m-3 and are generally dominated by Cladosporium by day and by Sporobolomyces by night. Many species have characteristic diurnal periodicities governed by the interaction between spore liberation mechanisms and environmental conditions. Thus some species have active liberation mechanisms dependent on turgid cells which require water, provided by dew or rain, for their operation so that their spores are most numerous at night or after rain. Other active mechanisms require drying conditions, either to give hygroscopic movement of sporophores that shakes off the spores or to cause contraction of unevenly thickened cells, until the tension within the cell causes a gas bubble to form and the cell suddenly to return to its original shape, catapulting off the spores. Liberation mechanisms dependent on drying give greatest spore concentrations soon after sunrise. Spores of many other fungi are released passively by mechanical disturbance, induced by wind disturbing leaves and twigs, and are most numerous around midday. Finally, spores of some fungi are passively dispersed by rainsplash. Rain has a marked effect on the occurrence of airborne spores. Falling raindrops vibrate vegetation when they impact and they spread out over the dry leaf surface, pushing a fast moving cushion of air before them that disperses spores into the air. Later, droplets falling onto fruiting bodies or water films on leaf surfaces disperse spores in splashes. The largest droplets follow ballistic trajectories and hardly become airborne while the smallest can evaporate and allow any spores that they carry to be dispersed by wind. Besides dispersing spores, rain removes spores from the atmosphere by impaction. Washout proceeds exponentially so that only 1% of 30 µm particles but 72% of 4 µm particles remain airborne after 120 minutes of rain falling at 2 mm h-1. Finally, rain provides water for ascospore release resulting in greatly increased numbers in the air after the rain has ceased. This may be associated with epidemic occurrence of acute asthma following thunderstorms.
Seasonal periodicities are often governed by climatic conditions or by stages of crop growth. In temperate regions, airborne spores are usually fewest during winter and spring and most abundant in summer when Cladosporium usually predominates by day and Sporobolomyces by night. Plant pathogenic fungi, in particular, have seasonal trends linked to crop growth cycles. For instance, Erysiphe is most abundant in England in June-July when the disease is most abundant on cereals, Ustilago during the flowering periods of their grass hosts and Phytophthora infestans in August-September, when weather conditions and growth stage of the potato crop favour late blight epidemics. Alternaria and Didymella are both most numerous close to harvest and a second peak of Cladosporium that may result from abundant growth may occur on cereal straws. Basidiospores become abundant during the autumn when heavy dews favour fruiting of many agarics. Conversely, Penicillium and Aspergillus are often most abundant in cities in winter.
Indoors, the numbers and types of airborne fungi are much more affected by the presence of local spore sources than out of doors. If there is no source, the types of airborne fungal spores will be similar to outdoors but their numbers will be smaller. With local spore sources, the types of airborne fungal spores will be determined by the nature of the source. Stored products often provide vast sources of spores in indoor and occupational environments. The numbers and types of fungi that they release into the air is determined by storage conditions, especially temperature and water availability, the extent of colonisation and the degree of disturbance. As water content increases in stored grain, hay, composts and other products, microbial respiration increases releasing energy, which causes heating if it cannot escape. This leads to an increasingly thermotolerant microflora, often dominated by actinomycetes and Aspergillus fumigatus. Spores and endotoxins from these sources present risks of occupational asthma and allergic and toxic alveolitis. In houses, moulds can grow in condensation on walls and window frames and in damp furnishings and carpet dust. Some of these are known to cause asthma and spores of others may carry mycotoxins. Air conditioning systems can both provide sources of bacteria, fungal spores, protozoa and other organisms, especially if they are humidified, and serve to circulate these microorganisms throughout buildings. They have often been implicated in building-related disease, including allergic alveolitis.
Algae may be dispersed from rocks, trees, soil and water by carriage on wind-blown soil particles, adherence to moss and fern spores, by rain splash of soil, by bursting bubbles and splashing from water surfaces in seas, rivers and sewage disposal plants, and by carriage in airborne foam. Gloeocapsa and other members of the Chroococcaceae have been found in concentrations of up to 110 dispersal units m-3 air, each unit composed of up to eight cells, but in southern England average daily concentrations at two sites to the west of London were only 7-11 cells m-3 air.
Despite their widespread occurrence, airborne moss and fern spores have been studied much less than pollens. Spores of ferns are released explosively when sporangia spring open as they dry during the early morning. Both sporangia and spores may be found on trap slides but the latter are far more numerous. Pteridium spores concentrations up to 1800 m-3 have been recorded but average concentrations of only 2-36 spores m-3 are more usual when there are only small sources near the trap. Average concentrations of airborne moss spores may be only 0.1-0.3 m-3. Clubmosses and horsetails are much more restricted in their distribution than mosses and ferns and there are few records of their occurrence in the air.
Pollen grains range in diameter from 10-100 µm. The most abundant types found in the air come from anemophilous plants but the few released by entomophilous plants may still be important causes of allergy. Many pollens have clearly defined seasons of abundance corresponding to the flowering periods of the plants from which they originate, although these seasons may be modified somewhat by weather conditions. Among the most numerous in many parts of the world are grasses but trees and other herbaceous plants can be important and are often associated with allergy. Time of liberation of pollen, both diurnal and seasonal, into the air is determined by when anthers dehisce but then dispersal is by mechanical disturbance. Thus, allergy to Betula is most frequent in March-April, to grass pollen in May-June and to Ambrosia (ragweed) in August-September. Diurnal maxima normally occur during the afternoon. Changing agricultural practice can result in changes in the airborne pollen spectrum. Thus, although the oilseed rape (Brassica napus) is entomophilous, increasing cultivation in Britain has increased both the amounts of airborne pollen and the incidence of allergy. Seasonal mean concentrations range from 20-130 pollens m-3 air but maximum concentrations may exceed 1500 m-3.
Airborne protozoa have been little studied for lack of convenient techniques. However, 0.1-0.2 protozoan cysts m-3 air have been recorded in Paris and an average of 2.5 m-3 on a river bank near Heidelberg. Their sources are mainly water and soil.
Aerobiology generally only considers arthropods that are incapable of determining the direction of their flight however, indoors, insect and mite fragments and especially their faecal material are often important allergens. House dust mites feed on human skin scales in bedding and carpets and allergen becomes airborne in particles averaging 7 µm, equivalent to the size of faecal pellets. There have been few measurements of their occurrence in air but immunoassay of samples collected on filters showed their occurrence correlated with asthma incidence. Allergy to house flies and locusts has also been associated with the occurrence of allergen in air samples.
Gram-negative bacteria are the source of endotoxins, lipopolysaccharide components of the cell walls of that are released into the environment by lysis. These have frequently been measured in air samples in occupational environments. On inhalation they can cause febrile reactions and they have been implicated in occupational lung diseases such as byssinosis and toxic pneumonitis. Sewage and similar aerosols may also be sources of endotoxin. Recently interest has extended to glucans, which are components of fungal cell walls and of some plant cells. They are considered to have similar irritant effects to endotoxin but little data has been published on their occurrence in air. Mycotoxins are toxic secondary metabolites of fungi which can be carried in their spores. Aflatoxins have been detected in air samples when maize grain infected by Aspergillus flavus has been handled during harvesting and in mills, giving concentrations up to 84-200 g aflatoxin g-1. Aflatoxins are highly carcinogenic and have been implicated in the excess of cancers found in some feed mills. They are also immunotoxic and may affect the response of the lung to other agents. A range of other toxins have been detected in spores but there is little data on their occurrence in the air. Fungal spores also contain enzymes which may contribute to their allergenicity.
There are many different components in air, both out of doors and indoors, which can have biological effects when inhaled. Most attention has been devoted to the allergenic pollens even though fungal spores are generally far more numerous. However, the importance of fungal spores as allergens could be underestimated because of variable and unstandardised diagnostic preparations which sometimes have been reported to lack the most important identified allergens. There has recently been increasing interest in the allergenicity of some groups of fungi, especially basidiospores, and it is to be hoped that this leads to better quality, standardised allergenic preparations. In the meantime, allergologists should not forget that components other than pollens may contribute to allergy either directly or through interactions with allergens.
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