Volume 10, Part 1, February 1996

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TO WHAT EXTENT DO AIRBORNE FUNGAL SPORESCONTRIBUTE TO RESPIRATORY DISEASE AND

ALLERGIC REACTIONS IN HUMANS?

It is quite clear to anyone who has left laboratoryculture media exposed to the atmosphere, even verybriefly, that fungal spores are all around us andtherefore, that we must be breathing them in andout during our normal daily routines. For example,clearing leaves and windfalls in Autumn, it is ofteneasy to see clouds of spores dislodged from the sur-faces of rotting plant material. For the most part,these spores have little or no effect on us and weneed not consider them further. However, inhaledfungal spores can cause a number of conditions inhumans with various consequences. Allergicresponses, usually reactions to the proteins in thespore wall, can result in the development of a runnynose and eyes (allergic rhinitis), and asthma-likesymptoms which are especially distressing in indi-viduals who develop exaggerated allergic responses(hypersensit ive or atopic individuals ). Prolongedexposure to unusually large numbers of spores ,often as the result of occupational circumstances,can result in the development of allergic alveolitis.In addition, some fungal species are primarypathogens, invading the body through the respirato-ry tract, and others can act a secondary pathogens,invading in circumstances where the host is predis-posed to infection.

There is a range of particles that occur in out-door atmospheres which may give rise to allergicresponses in humans, e.g. dust, fibres and grit ,pollen grains from higher plants (particularly grass-es and trees) and also spores (both dry and slimyspores) of fungi and filamentous bacteria(Actinomycetes). The most abundant spores asso-ciated with allergenicity to occur in air arise fromfungi commonly found on leaf surfaces, for exampleCladosporium Link, Sporobolomyces Kluyver & v.Niel, which grows as yeast-like cells and forms largenumbers of spores (ballistospores), DidymellaSacc:Sacc and Alternaria Nees. Such spores mayact as allergens although no tissue invasion occurs.

Dry-spored fungi are often implicated in allergicresponses. However, it is not altogether clearwhether it is the numbers of the particles involved

or the volumes that are more important in inducingallergic responses in humans. It is interesting thatwhile the numbers of fungal spores recorded in airsamples may be high the spores themselves areextremely tiny. Although there may be larger num-bers of fungal spores in a given volume of air thanpollen grains, the volume concentrations of thosepollen grains may actually be larger. Fungal sporesare often only a few microns in diameter and themajority of spores that occur in breathable air areless than 100 !lm diameter. An average pollen grainoccupies the same volume as 200 Cladosporiumspores. Additionally, it is often the case that thosefungal spores produced in huge numbers are small-er in size. Large fungal spores such as those ofAlternaria spp. may become deposited in the nosewhereas smaller spores e.g. those of Aspergillus

species (3-5 11m diameter) may pass further downinto the respiratory tract because of their size.Sedimentation rates depend on a range of factorsincluding spore size, shape, wettability and thearchitecture of the spore wall.

Rainfall has a large effect on the occurrence ofspores in the air. Washout of larger spores occursrapidly but small particles will remain airborne forlonger although these too are picked up by raindrops. It has also been noted however, that acuteasthma attacks may occur immediately followingrain storms or within a few hours of heavy rainfall.It is likely that this effect can be attributed to asudden increase in water availability encouragingthe release of spores from fungal fruiting structures.The after-effect of a storm actually increases thenumber of new spores reaching the atmosphere. Inaddit ion, seasons and location have a marked effecton numbers of spores in the atmosphere and tosome extent the range of types of spore present.There can be marked fluctuations in numbers dueto differing local circumstances, such as the occur-rence of fungal crop disease and the concomitantincrease in release of spores from diseased plants.

Indoors, airborne spores may represent a differ-ent mix of species. In the home environment there

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Volume 10, Part 1, February 1996

are usually less spores than outdoors and fewerspecies will be represented. In office buildings, thetype of ventilation system and the amount of airdisturbance will influence the species range andnumbers of spores present. Air conditioning sys-tems can markedly influence the distribution ofspores and humidifiers may encourage sporulationof particular species (often actinomycetes), repre-senting an additional source of contamination. Therepresentative microflora of an indoor occupationalenvironment will be related to the work being car-ried out and to the actual conditions. Damp grainand hay are particularly hazardous sources ofspores (A. fumigatus and A. versicolor) during stor-age and at harvest. Moulded hay will give rise tolarge spore clouds when disturbed and has beenreported to contain 109 propagules per gram of hay.Materials stored for use in food manufacture (par-ticularly grains, flours, nuts, meals, ripeningcheeses and raw materials such as fruits) may alsoharbour fungal spores. Mushroom farms, saw mills,paper mills, composting areas, waste disposal sitesand processing plants where fungal contaminationmay occur, are all areas where potentially greaternumbers of allergenic particles may be present.Allergic conditions can arise as the result of pro-longed and/or repeated exposure to unusually highconcentrations of spores, sometimes representing aparticular occupational hazard. For example, Maltworker's lung, caused by Aspergillus clavatus, A.[umigaius and A. flavus (allergic aspergillosis),Farmer's lung caused by spores from the actino-mycetes Micropolyspora faeni andThermoactinomyces vulgaris and Cheese washer'slung, caused by Penicillium casei spores. In addi-tion, exposure to some fungal metabolites, particu-larly enzymes (proteases, amylase, cellulase) canalso result in the development of allergic responses,affecting those in occupations such as baking andthe fermentation industries. Toxins (mycotoxins)produced by some fungal species have also beenimplicated in the development of respiratory prob-lems although there is little information to supportthis theory.

Some fungi can act as secondary pathogens onhumans. This can result from the growth of specieswhich would normally colonise dead and decayingmaterial (saprophytic fungi) taking the opportunityto growas pathogens. Aspergillus [umigatus occurscommonly on dead organic material in compostheaps and in stored grains and hay where it canwithstand the higher temperatures reached by the

decomposing plant material. It is therefore alsoable to grow at body temperature. A. fumigatuscauses allergic reactions but does not invadehealthy tissues. It can however, act as a secondarypathogen, affecting patients where lung tissueshave been previously diseased. Spaces within dam-aged lung tissue and plugs of excess mucus may becolonised, causing severe allergic reactions andforming a ball of mycelium (aspergilloma) eventual-ly resulting in severe breathing difficulties. Moredeeply seated infections can develop in very ill andhighly susceptible patients where A. fumigatusbecomes invasive. This only occurs when immuno-logical defenses are severely disrupted such as intransplant patients.

Primary infections by fungi can also occur viathe respiratory tract. Some fungi, often found inwarm regions of the world, are invasive pathogens.Coccidioides immitis causes 'Valley fever' in dryregions of Southern USA and Mexico; Histoplasmacapsulatum causes Histoplasmosis in Central USA;Blastomyces dermatitidis causes Blastomycosis inEastern USA and Canada and Paracoccidioidesbrasiliensis causes Paracoccidioidomycoses inCentral/South America. These species form sporesin soils, plant debris and bird droppings disturbanceof which causes spores to become airborne.Inhalation of spores can give rise to lung infectionswhich in many cases may heal spontaneously, espe-cially in healthy individuals, and pass undetected.Indeed it is probable that huge numbers of peopleare affected without note. However, in more sus-ceptible patients the infections may spread throughthe blood stream (rapidly becoming systemic) andmay eventually cause extensive tissue destruction.Where susceptibility to infection is high and resis-tance lowthis may have fatal consequences.

Most people will never encounter any systemicmycoses and, with care, most allergic reactions canalso be avoided or minimised. Nevertheless, it isimportant that the effects of exposure and sensiti-zation are taken seriously and monitored, so thatcontrol measures may be implemented if necessary.

Susan IsaacDepartment of Genetics & Microbiology,

Life Sciences Building, University of Liverpool,Crown Street, Liverpool, L69 3BX