Bioaerosol Components

For the reasons described above, high concentrations of bacteria and fungi are present in composts. For example, Dees and Ghiorse19 reported total counts in the order of lO10 cells per gram of compost [dry weight] measured using epifluorescence microscopy, with thermophilic heterotrophic aerobes measured

13 J.G. Kleyn and T.F. Wetzler, Can. J. Microbiol., 1981, 27, 748-753.

14 J. Lacey, Ann. Agric. Environ. Med., 1997, 4, 113-121.

15 A. Ghazifard, R. Kasra-Kermanshahi and Z.E. Far, Waste Manage. Res., 2001, 19, 257-261.

16 P.F. Strom, Appl. Environ. Microbiol., 1985, 50, 906-913.

17 T. Beffa, M. Blanc, P.-F. Lyon, G. Voght, M. Marchiani, J. Lott Fischer and M. Aragno, Appl. Environ. Microbiol, 1996, 62, 1723-1727.

18 P. D. Millner, P. B. Marsh, R. B. Snowden and J. F. Parr, Appl Environ. Microbiol, 1977,34,765-772.

19 P.M. Dees and W.C. Ghiorse, FEMS Microbiol. Ecol, 2001, 35, 207-216.

20 R.F. Herrmann and J.F. Shann, Microb. Ecol, 1997, 33, 78-85.

21 B. Hellmann, L. Zelles, A. Palojarvi and Q. Bai, Appl Environ. Microbiol, 1997, 63, 1011-1018.

22 L. Carpenter-Boggs, A. C. Kennedy and J. P. Reganold, Appl Environ. Microbiol, 1998,64,4062-4064.

23 M. Blanc, L. Marilley, T. Beffa, and M. Aragno, FEMS Microbiol. Ecol, 1999, 28, 141-149.

24 J. Kondroj and J.D. van Elsas, J. Microbiol Methods, 2001, 43, 197-212.

25 S. Peters, S. Koschinsky, F. Schweiger and C. C. Tebbe, Appl Environ. Microbiol, 2000,66,930-936.

in the order of 108 colony forming units (cfu) (g dry wt)_1. Lacey14 reported actinomycetes in mushroom composts in the order of 106 cfu (g dry wt)-1; Strom10 and Millner et a/.18 reported concentrations of Aspergillus fumigatus in excess of 105 cfu (g dry wt)-1 in composting sewage sludge, whilst Beffa et a/.17 reported concentrations of thermophilic bacteria related to the genus Thermus in the range of 107-1010 cells (g dry wt)-1. A cfu is defined as the unit of one or more cells or spores which when inoculated onto suitable growth medium grows to form a single colony.

Whenever composting materials are moved around, for example during the shredding, turning and screening processes, these micro-organisms can be aerosolised, forming what is termed a bioaerosol. Actively managed, medium- to large-scale composting harnesses the activity of indigenous micro-organisms commonly present in the soil that naturally decay, such as fallen leaves. Therefore, the microbial components of bioaerosols generated during the composting process contain many of the same micro-organisms that are commonly isolated from 'normal' outdoor air. The main difference is that of scale. The handling of large quantities of compost potentially can lead to the release into the air of large quantities of the bacteria, fungi and actinomycetes and their components, found in compost, as a bioaerosol.

Exposure to the micro-organisms found in compost could potentially cause ill-health in the people exposed to them either by infection, allergy or an adverse response to toxins. The composting process generates heat, so any human pathogens present in the raw materials, such as coliform bacteria from faecal material which could give rise to gastro-intestinal infection, should be rapidly killed off during the composting process.

Some of the micro-organisms which increase in number during the composting process are toxic and/or allergenic and still have the potential to cause problems when they are dead.

There are two main routes of exposure to compost micro-organisms: ingestion of the micro-organisms or inhalation of bioaerosols created during the handling of compost. Good hygiene practices such as wearing of gloves and provision of hand washing facilities on composting sites should control risks from ingestion. However, control of bioaerosols generated by composting processes is more complex.

In order to understand the potential health hazards associated with exposure to compost bioaerosols, it is first important to examine in detail the microbial components of bioaerosols generated during the handling of compost.

Fungi

During the handling of fresh green waste the micro-organisms present are predominantly the saprophytic 'field' fungi such as Cladosporium spp., Alternaria spp., and Verticillium that colonise plants during growth. As the composting process progresses, the numbers and types of associated contaminants change. Some fungal spores naturally present in low numbers may germinate and grow. These are referred to as 'storage fungi' because they flourish in stored organic materials. They include Aspergillus, Eurotium, Penicillium, Trichoderma, Absidia,

Mucor and Rhizopus species. These fungi can grow at lower water availability and predominate over the field fungi, which are less well suited to multiplication in these conditions. The increased metabolic activity can lead to spontaneous heating of the compost. This can result in a succession of microbial growths so that, if enough water is available, temperatures of 65 °C can be reached, allowing the growth of thermophilic and thermotolerant fungi.26-29

A. fumigatus is particularly important in the composting process due to its capacity to degrade cellulose and hemicelluloses. Its optimum growth temperature is 37 °C and good growth can occur between 30 and 52 °C. Consequently it is likely to be present in significant numbers. However, its presence is also an important consideration from a human health viewpoint. It is an allergenic fungus and is an opportunistic pathogen which can cause aspergillosis in immunocompromised subjects.30'31 A. fumigatus can also produce mycotoxins which are toxic, carcinogenic, and mutagenic. Other Aspergillus species, and other fungal species present in compost, such as Rhizopus, are also allergenic.

Bacteria

Bacteria can be divided into two main types: Gram-negative bacteria and Gram-positive bacteria. Gram-negative bacteria predominate in dusts of plant origin: bacteria such as Pseudomonas spp., Klebsiella spp., Pantoea agglomerans, Rahnella spp. and Alcaligenes spp. are commonly present.26 Gram-positive bacteria predominate in dusts of animal origin, but are also present in dusts of plant origin, bacteria such as Corynebacteria, Bacillus spp. and cocci such as Staphylococcus spp. Micrococcus spp. and Streptococcus spp.26 Gram-negative bacteria found in in dusts of animal origin include Acinetobacter and Enterobacter spp. Consequently, these species will be present in composts. Other Gram-negative bacteria of animal faecal origin, the coliform bacteria such as E. coli, Campylobacter and Salmonella species, could be present in compost feedstock depending on its origin. Composts prepared from animal manures obviously are most likely to contain coliforms, but organic waste may be contaminated by animal faeces.

The elevated temperatures achieved in composting should kill off coliform bacteria (see also details in Section 4, Case Studies), although it should be recognised that inadequate compost turning could lead to temperature stratification and survival of coliforms in cooler layers. This is particularly of concern with highly pathogenic strains of E. coli, such as the verocytotoxic E. coli 0157, which has been shown to survive for several days in soils.32,33 Workers handling composts from animal manures need to take additional hygiene precautions, such as thorough hand washing, and public access to composting animal

26 J. Dutkiewicz, Ann. Agric. Environ. Med., 1997, 4, 6-11, 11-16.

27 J. Lacey, in Occupational Pulmonary Disease: Focus on Grain Dust and Health, ed. J. A. Dosman and D.J. Cotton, 1980, pp. 189-200.

28 C.S. Darke, J. Knowelden, J. Lacey and A. Milford-Ward, Thorax, 1976, 31, 294-302.

29 J. Lacey and B. Crook, Ann. Occup. Hyg., 1988, 32, 513-533.

30 H. Allmers and X. Baur, Am. J. Ind. Med., 2000, 37, 438-442.

32 A. Maule, Symp. Ser. Soc. Appl. Microbiol., 2000, 29, 71S-78S.

33 L. D. Ogden, D. R. Fenlon, A.J. Vinten and D. Lewis, Int. J. Food Microbiol., 2001, 66, 111-117.

manures, such as on open farms, should be restricted. Other bacterial pathogens of animal origin include Leptospira, the causative agent of Weil's disease. This bacterium multiplies in the kidneys of infected rats and is spread in contaminated urine, causing infection in humans through entry via skin abrasions and mucus membranes. For this reason among others, vermin control on compost sites is important.

Bacteria, therefore, can be hazardous to health as pathogens, e.g. coliforms as described above, but the main route of infection is by ingestion. Respiratory infection caused by bacteria is unlikely to be a significant hazard in composting. However, bacteria present in airborne dust from composts could cause allergies and may be toxin producers (see endotoxin).

Actinomycetes

In addition to bacteria as described above, actinomycetes are also found in these environments. Actinomycetes are filamentous Gram-positive bacteria that are commonly found associated with soil and plant materials. Thermophilic actinomycetes, with a growth temperature range of 30-60 °C, thrive in wet compost that has begun the self heating process. Therefore they can be used as indicator organisms for self heating of organic material, and as indicator organisms for the presence of bioaerosols generated from compost.26'27'29 The most common species present are Saccharopolyspora (Faenia) rectivirgula, Saccharomonospora spp. including S. viridis, Thermoactinomyces thalpophilus, Thermoactinomyces vulgaris and Thermomonospora spp. Mesophilic species such as Streptomyces are also commonly present in high numbers.

Thermophilic actinomycete species are recognised respiratory allergens. Actinomycetes produce thousands of very small spores (1-3 /mi diameter) which easily become airborne in large numbers when heavily colonised material is disturbed. Their small size means that they are potentially capable of penetrating deep into the human lung. They are primarily responsible for occupational allergic diseases such as Farmers' Lung Disease and Mushroom Workers' Lung Disease, which are forms of extrinsic allergic alveolitis.

Endotoxin

Endotoxin is found in the outer layer of the cell walls of all Gram-negative bacteria and some blue-green algae. Endotoxin is the fragments of the bacterial cell wall that contain lipopolysaccharide (LPS) as well as other compounds naturally occurring in the cell wall.34 Gram-negative bacteria are present in the oral cavities and intestinal tracts of humans and animals; they also live on the surfaces of animals and plants. Consequently the general population is exposed to low levels of endotoxin and it is found in house dust.

Endotoxin is present in occupational settings, mainly as a component of organic dusts such as those of vegetable origin contaminated with Gram-negative bacteria (e.g. grain and cotton dust), dusts containing animal faeces e.g. in swine

34 R. R. Jacobs, D. Heederik, J. Douwes and U. Zahringer, Int. J. Occup. Environ. Health, 1997,3, S6-S7.

Table 2 Summary of airborne occupational endotoxin exposure

Industry/activity

Mean airborne endotoxin concentration (ng m~3)

Reference

Waste water treatment

0.6-310

35

Waste handling

0-17.4E

36-38

Agriculture

0-770000

39

Cotton industry

66-6936

40

Biotechnology

0.33-162.8

41

Machining MWF

0.1—767pE

39

Fibreglass wash water

0.4-27 800

42

Offices

0.018-1200

43

E Nanograms calculated from Endotoxin Units by dividing by 10. p Personal sampling.

E Nanograms calculated from Endotoxin Units by dividing by 10. p Personal sampling.

confinement buildings and poultry houses) and sewage sludge. Endotoxin is also present in compost as a result of the presence of Gram-negative bacteria and therefore is made airborne in dust from compost handling. The amount of airborne endotoxin in different occupational environments varies widely. Some typical examples are summarised in Table 2.

Inhalation of endotoxin causes both short term illness (flu-like symptoms, fever, myalgia, and malaise, e.g. organic dust toxic syndrome) and long term illness (e.g. chronic bronchitis, chronic obstructive pulmonary disease and long term decline in lung function). The acute clinical symptom response to endotoxin inhalation occurs 6-12 hours after exposure and lasts about 4 hours. Chronic exposure to endotoxin has been linked to work related symptoms and chronic decreases in lung function such as chronic inflammation leading to chronic bronchitis and reduced lung function.

Mycotoxins

Mycotoxins are non-volatile low molecular weight toxic secondary metabolites produced by fungi. Mycotoxins can be carcinogenic, neurotoxic and teratogenic. The most common route of exposure is ingestion. The toxins can cause acute or chronic disease in vertebrate animals,44 and may contribute to occupational lung disease in workers exposed to organic dusts. Aspergillus spp., including A.

3 5 J. Liesivuori, M. Kotimaa, S. Laitinen, K. Louhelainen, J. Ponni, R. Sarantila and K. Husman, Am. J. Ind. Med., 1994, 25, 123-124.

36 K. Heldal and M. Bergum, Ann. Agric. Environ. Med., 1997, 4, 45-51.

37 T. Sigsgaard, P. Malmros, L. Nersting and C. Pedersen, Am. Rev. Resp. Dis., 1994,149,1407-1412.

38 T. Sigsgaard, J.C. Hansen and P. Malmros, Ann. Agric. Environ. Med., 1997, 4, 107-112.

39 Health and Safety Laboratory, J.R. M. Swan, 1999, unpublished data.

40 J.C.G. Simpson, R.McL. Niven, C.A.C. Pickering, L.A. Oldham, A.M. Fletcher and H.C. Francis, Ann. Occup. Hyg., 1999, 43, 107-115.

41 R. B. Palchak, R. Cohen, M. Ainslie and C. LaxHoerner, Am. Ind. Hyg. Assoc. J., 1988,8,420-421.

42 D. K. Milton, J. Amsel, C. E. Reed, P. L. Enright, L. R. Brown, G. L. Aughenbaugh and P. R. Morey, Am. J. Ind. Med., 1995, 28, 469-488.

43 E. Kateman, D. Heederik, T. M. Pal, M. Smeets,T. Smid and M. Spitteier, Scand. J. Work Environ. Health, 1990, 16, 428-433.

44 S. Gravesen, J. C. Frisvad and R. A. Samson, Microfungi, Munksgaard, Copenhagen, 1994.

fumigatus, and Penicillium spp. produce mycotoxins and both are usually present in the dust generated during the handling of compost. Their possible role in causing respiratory symptoms is not fully understood and the presence of mycotoxins in compost dust has not been widely studied. Fischer et al.45'46 have investigated the presence of secondary metabolites associated with fungi, in particular A. fumigatus mycotoxins, in bioaerosols from composting facilities in Germany. Cultured isolates of A. fumigatus produced a range of mycotoxins. Extracts of total dust and bioaerosols from a composting hall contained two A. fumigatus mycotoxins, two tryptoquivaline (which has tremorgenic properties) and trypacidin. They did not find the most toxic mycotoxins produced by A. fumigatus (gliotoxin and verruculogen) in the bioaerosols. In one study Fischer45 did not find mycotoxins in samples of airborne spores, organic dusts and bioaerosols from composting sites. The results indicated that fungal spore counts need to be above 107 m~3 air to enable detection of fungal metabolites or toxins.

It is not known what occupational health risks are posed by the fungal metabolites in compost bioaerosols; their toxigenic potential needs further investigation.

Glucans

(l->3)-/?-D-glucan is a polyglucose compound in the cell walls of fungi, some bacteria and plants. It is a potent inflammatory agent that induces non-specific inflammatory reactions and may also be a respiratory immunomodulatory agent. Exposure to (1 ->3)-/?-D-glucans has been associated with an increased prevalence of atopy, decreases in forced expiratory volume (FEVi), and adverse respiratory health effects in the indoor and occupational environment.47 49 There is also evidence that (l-^-jS-D-glucans may enhance pre-existing inflammation.47

(l->3)-/?-D-glucans may be involved in contributing to the inflammatory responses resulting in respiratory symptoms and adverse lung function effects in response to the inhalation of bioaerosols.

Volatile Organic Compounds

Volatile organic compounds (VOCs) are generated by many sources in the compost mixture including micro-organisms. Eitzer50 found that most VOCs were emitted during the early stages of processing. Emissions were concentrated at the tipping floors where waste arrives, at the shredder and at the initial active composting region. VOC concentrations, even 'worst case' samples collected right next to the compost, were well below USA permissible workplace levels. They also found great similarities between facilities operating under differing

45 G. Fischer, R. Ostrowski and W. Dott, Chemosphere, 1999, 38, 1745-1755.

46 G. Fischer, R. Schwalbe, M. Moller, R. Ostrowski and W. Dott, Chemosphere, 1999,39, 795-810.

47 J. Douwes, I. Wouters and H. Dubbeld, Am. J. Ind. Med., 2000, 37, 459-468.

48 P.S. Thorn and R. Rylander, Am. J. Resp. Crit. Care Med., 1998, 157, 1798-1803.

49 D. Fogelmark and R. Rylander, Int. J. Exp. Pathol., 1994, 74, 85-90.

50 b. Eitzer, Environ. Sci. Technol., 1995, 29, 896-902.

conditions, their sites ranging from aerated in-vessel systems to open windrows.

Fischer46 screened 13 fungal species frequently isolated from a composting facility for microbial VOCs. They identified various hydrocarbons and terpenes. However, these are not necessarily produced when the fungi are growing in the environment.

A wide variety of VOCs can also originate from plant material. There is not enough information available on exposure to microbial VOCs to enable any assessment of potential health risks.

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