Maataloustieteellinen A ikakauskirja Vol. 62: 285—291, 1990 Spore exposure arising from stored hay, grain and straw MARJUT KOTIMAA Kuopio Regional Institute of Occupational Health, P.0.8. 93, SF-70701 Kuopio, Finland Abstract. The quantitativeand qualitative differences in microbe exposure arising from hay, grain and straw during the end of the indoor feeding period were investigated by using a six-stage fractionating impactor (model 10—800, Andersen Inc.). Straw samples (n =5) liberated significantly higher amounts of spores (3.7 x 106 cfu/m 3 air) in comparison to hay samples (n=33) and grain samples (n=2), which liberated 0.6x10s cfu/m 3 and 0.2xl06 cfu/m 3 , respectively. Thermotolerant and thermophilic microflora were typicalof the exposure originating from straw. Hay liberated about 10 % and grain only 0.7 %, the level of spores of thermotolerant fungi liberated from straw. The corresponding percentages of spores of thermophilic actino- mycetes were 5 % and 0.4 %. Thermoactinomyces vulgaris was the dominating microbe in the exposure caused by straw; Aspergillus umbrosus was the major species in the microflora liberated from hay and grain. Other Aspergillus (A.) species (A. fumigatus, A. ochraceus, A. flavus, A. repens, A. versicolor) and Penicillium (P.) species (P. expansum, P. piceum, P. citrinum, P. brevicompactum, P. echinulatum, P. verrucosum var. cydopium) occurred fre- quently, a/id in great amounts, in all the analysed materials. Spores of Cladosporium (C.) spe- cies (mainly C. herbarum, C. cladosporioides, and C. macrocarpum) were found frequently, and abundantly, during the handling of hay. The present results suggest that not only the tradi- tional causative agents of farmer’s lung disease but also other fungal and actinomycetespecies may be found in high’toncentrations during the handling of bedding and feeding stuffs, and that these fungal and actinomycete exposures may causerespiratory symptoms and other health problems in both man and animals. Special attention should be paid to decreasing the mois- ture content of hay and straw before storing in order to lower the risk of moulding during the indoor feeding period. Introduction Dust problems are typical of agricultural working environments. Dust exposure consists mostly of organic particles, which originate from feeding and bedding stuffs and from animals and their excrements. Organic com- ponents may include, e.g. animal dander, hair, feathers, manure, insects, mites, pollen, fungal spores or fragments of fungal hypha, bacteria and their endotoxins, mycotoxins and fodder particles. The amount and the quality of dust are affected by the branch of produc- tion, geographical location and the climatic conditions, and these factors are also related to the prevalence and the incidence of farm- 285 JOURNAL OF AGRICULTURAL SCIENCEIN FINLAND https://www.c-info.fi/en/info/?token=QwK-udKwr-QmbsKN.GmY8vLbkCKxNl8becyGKaQ._NOQDvAsYO2NQ1OaRk7Mjtf-NuhVbAabaIpGf517EDSvTUyU3ACPE0hrkPCV6oZoW7zEEXMQalP9uYB5RAaD6ajyone6-r4gSPIsjP1ZiSzJdoeTefZIHKtgHZ2s2Dez6rreoVoNZHryvfXGhlA9XdUenYk-6u3vDZc4PQ er’s lung (Terho et al. 1987, Vohlonen et al. 1987).Farmer’s lung disease is one type of al- lergic alveolitis caused by fungal and actino- mycete spores arising from mouldy plant ma- terial (Pepys 1969). The yearly incidence of allergic alveolitis in Finland has increased steadily from 101 cases in 1984 to 340 cases in 1988. The vast majori- ty of the cases occurs among farmers (Vaara- nen et al. 1985, 1986, 1987, 1988, 1989), es- pecially on dairy farms. Disease similar to farmer’s lung has also been reported in bo- vines and in horses (Pirie et al. 1971, Wise- man et al. 1973, Asmundsson et al. 1983). Hay has been accused of causing the disease, although other stored plant materials (feed- ing and bedding stuffs) used on farms are as susceptible to moulding as hay. The aim of the present study was to investigate quantita- tive and qualitative differences in microbe ex- posure arising from hay, grain and straw dur- ing the end of the indoor feeding period. Material and methods Material samples for aerobiological studies were taken at the end of indoor feeding pe- riod (in April and May) on the farms, which situated in Eastern Finland. Thirtythree farms were included in the study and hay samples were taken from baled hay, grain samples from grain which had been dried with un- heated forced air and straw samples from baled straw. All the material samples represented average quality, exceptionally mouldy or good quality batches were ex- cluded. A six-stage fractionating impactor (model 10-800, Andersen Inc., Georgia, USA) was used to take air samples for analysing the quality and the quantity of viable microflora (Andersen 1958). Samples were taken during the handling of hay (N = 33), grain (N = 2) and straw (N = 5), at a distance of half a metre from the farmer’s breathing zone. Each sample included four successive mea- surements. Two sets of Hagen-medium (malt extract-glucose-agar (Russel 1974) sup- plemented by 35 mg streptomycin and 35 mg Rose Bengal and diluted to 1000 ml medium) were used. One sample was incubated at 20 °C for the outgrowth of mesophilic fungi and the other was incubated at 40 °C to obtain colo- nies of thermotolerant fungi. NaCl-malt ex- tract agar (Terho 1978) (incubation at 20 °C) was used for Aspergillus (A.) glaucus group fungi, and half-strength Nutrient agar (Cor- baz et al. 1963) (incubation at 55 °C) for thermophilic actinomycetes. After incubation, the colonies were identified using a lightmicro- scope and counted. The positive hole correc- tion method of Andersen (1958) was used to count colonies before calculating the concen- trations, which are expressed as colony-form- ing units per cubic metre of air (cfu/m3 ). The sampling time per medium varied from 5 to 30 seconds, according to the visible mouldi- ness of the material. In evaluating the differ- ences in spore concentrations, one-way anal- ysis of variance was used after the logarith- mic transformation of calculated values. The Chi square test was applied to evaluate the differences in the frequencies of various mi- crobes. Results Handling of feeding and bedding stuffs caused a high level of exposure, from 104 to 107 cfu/m 3 . Both the lowest and the highest total spore value was measured dur- ing the handling of hay (19 000 cfu/m3 and 13 700 000 cfu/m3 , respectively) (Table 1). In all cases, straw liberated large amounts of spores, the differencebetween straw and other materials being statistically significant (F = 3.40, p<0.05). Compared to hay and straw, grain samples caused only slight ex- posure to spores. Thermotolerant and ther- mophilic microflora were typical of the ex- posure originating from straw. Hay liberated about 10 % and grain only 0.7 %, the level of spores of thermotolerant fungi liberated from straw. The corresponding percentages of 286 Table 1. The concentration of airborne spores of different microbe groups expressed as geometric means (x) of colony forming units per m 1 during the handling of various materials on farms. Microbe group Material Hay x 10J Straw x 10! Grain x 10! Mesophilic fungi 380 1900 160 range (9.7—6600) (520—6500) (38—650) Thermotolerant fungi 24 230 1.6 range (0.05—2000) (12—2600) (0.25—11) Thermophilic actinomycetes 36 670 1.6 range (0.07—5100) (100—3300) (0.39—11) Total 630 3700 160 range (19—14000) (2100—12000) (38—670) spores of thermophilic actinomycetes were 5% and 0.4 <7o (F = 3.79, p<0.05). Ther- moactinomyces vulgaris was the dominating microbe in the exposure caused by straw (F = 3.61, pcO.OOl); Aspergillus umbrosus was the major species in the microflora liber- ated from hay and grain (Table 2). Other Aspergillus species (A. fumigatus, A. ochraceus, A.flavus, A. repens, A. versicolor) and Penicillium species (P. expansum, P. piceum, P. citrinum, P. brevicompactum, P. echinulatum, P. verrucosum var. cyclopium) occurred frequently and in great amounts in all the analysed materials. Of the fungi that were found occasionally, or in minor concen- trations, Humicola sp. was significantly more common in straw than in hay or grain (F = 3.93, pc0.05, X 2 = 4.75, p<0.10) (Table 2). The spores of the Cladosporium species (mainly C. herbarum, C. cladosporioides and C. macrocarpum) were found frequently, and abundantly, during the handling of hay (F = 4.35, p<0.05, X 2 = 6.12, p<0.05). Discussion Each year, most cases of farmer’s lung are diagnosed during the end of the indoor feed- ing period (Terho et ai. 1980, Pether & Greatorex 1976). During that time the ex- posure to airborne spores is greater than at the beginning of the indoor feeding period and small-spored storage fungi are mainly encoun- tered (Kotimaa et ai. 1978, 1981). A similar incidence pattern has also been reported among bovines, which contract respiratory disorders after having been fed mouldy hay (Pirie et al. 1971, Wiseman et al. 1973). All samples were collected for this study during the season involving the highest exposure to spores, though there were noticeable differ- ences in the quality and the quantity of ex- posure to spores during the handling of dif- ferent materials. Straw bedding caused the highest spore con- centrations when compared to hay or grain; parallel results have also been published in other reports (Mulinge & Chester 1970, Lacey 1971). The role of straw as a factor in- creasing exposure to spores on farms has not recieved much attention so far. The great numbers of thermotolerant fungi and ther- mophilic actinomycetes indicate spontaneous heating resulting from the high moisture con- tent of stored material (Festenstein et al. 1965). Straw is collected, often by baling, when the weather is often rainy, or at least when the difference in temperature between the daytime and the night-time is great, and thus dew may provide sufficient moisture to initiate moulding. It has not been studied how straw could be collected and preserved with- out giving rise to conditions favourable to moulding. The quality of the microbe ex- posure originating from straw was much the same as that originating from hay and causing 287 288 Table 2. Concentration of the sporesof different taxons, expressed as geometric means(x) of colony forming units per mJ , and their prevalence (%) during the handling of stored hay, straw and grain. Taxon Material Hay Straw Grain x Range % x Range % x Range % Alternaria spp 8 o—l2000 30.3 0 0.0 0 0.0 Aspergillus spp 79 0—230 000 48.5 580 0—630 000 60.0 6 0—36 50.0 A. fumigatus 11 000 48—2 000 000 100.0 580 3 100—1 100 000 60.0 1 100 220—5 400 100.0 A. niger 12 o—l4o 000 30.3 7 0—22 000 20.0 0 0.0 A. umbrosus 76 000 1 000—5 900 000 100.0 50 000 1 700—5 200 000 100.0 84 000 37 000—190 000 100.0 Aur. pullulans 2 0—430 9.0 0 0.0 0 0.0 Botryotrichum sp 0 0.0 4 o—B6o 20.0 0 0,0 B. cinerea 2 o—l 000 15.2 15 o—l 700 40.0 0 0.0 Candida sp 2 o—2 400 6.1 0 0.0 0 0.0 Chaetomium sp 1 0— 36 3.0 0 0.0 0 0.0 Cladosporium spp 850 o—l4o 000 78.8 26 o—7 100 40.0 0 0.0 Gliocephalis sp 1 o—lB 000 3.0 0 0.0 0 0.0 Haplographium sp I 0— 1 500 3.0 0 0.0 0 0.0 Humicola spp 4 0—93 000 19.2 480 o—2 000 000 60.0 15 o—2lo 50.0 M. faeni 61 0—260 000 48.5 550 o—llo 000 40.0 150 110—210 100.0 Mucor spp 1 900 0—720 000 90.9 870 0—43 000 80.0 29 o—B6o 50.0 P. variolii 16 o—s300 42.4 14 o—2 600 40.0 46 o—2 100 50.0 Penicillium spp 34 000 o—2 300 000 93.9 20 000 7 900—2 900 000 100.0 7 000 110—460 000 100.0 Rhizopus spp 7 o—2 500 33.3 45 o—l 500 60.0 0 0.0 S. brevicaulis 2 o—l3o 000 12.1 0 0.0 0 0.0 Sporobolomyces sp 2 0— 2 700 6.1 0 0.0 0 0.0 Streptomyces spp 86 0—42 000 60.6 37 o—2l 000 40.0 15 o—2lo 50.0 T. sacchari 1 o—l3o 3.0 0 0.0 0 0.0 T. vulgaris 19 000 48—5 000 000 100.0 560 000 9 400—3 000 000 100.0 1 100 110—11 000 100.0 Th. viridis 0 0.0 12 o—2lo 000 20.0 0 0.0 Trichophyton sp 3 0—5 100 21.2 0 0.0 0 0.0 Tr. viride 5 o—6 200 24.2 19 o—2 100 40.0 0 0,0 Trichosporonoides sp 1 0— 1 200 3.0 0 0.0 0 0.0 myc.ster. and unidentified 34 o—lo 000 54.5 1 100 95—26 000 100.0 0 0.0 Yeasts 55 o—l2000 60.6 13 0—760 40.0 36 o—l 300 50.0 A. = Aspergillus, Aur. = Aureobasidium, B.=Bolrytis, M. = Micropolyspora, P. = Paecilomyces, S. = Scopulariopsis, T. = Thermoactinomyces, Th. = Thermomonospora, Tr. = Trichoderma, myc.ster. = mycelia sterilia farmer’s lung, as described by Gregory & Lacey (1963). The hay samples in this study included both good quality and extensively moldy batches, which indicates great variation in the micro- biological quality of baled hay on different farms. The presence of Cladosporium and Al- ternaria species, however, indicates that the storage of hay probably promotes less micro- biological deterioration than the storage of straw. If weather conditions during hay- making are unfavourable, the high moisture content of the hay allows the development of abundant thermotolerant and thermophilic microflora, e.g. A. fumigatus, T. vulgaris and M. faeni. The last-mentioned species requires a fairly high moisture content (47 %) of the material to grow (Cross et al. 1968). Such a high moisture content is rare in the climatic conditions of Finland, which may explain the rare occurrence of M. faeni in Finnish hay samples (Kotimaa et al. 1983, Mustonen et al. 1984). However, if hay is baled, the mois- ture content of hay is more critical as to moulding, because less water evaporates from tightly baled hay than from loosely collected hay. Evidently, the grain material of this study was of good microbiological quality, although the samples were driedby forced unheated air. The level of exposure has been found to be higher during the handling of cool-air-dried grain compared to the handling of grain preserved and stored with other methods, e.g. drying with heated forced air (Mustonen et al. 1983). Our results imply that, at least in dry threshing season, cool air drying may be effective enough to prevent moulding of grain. There were only few thermophilic Strep- tomyces species, which are characteristic of self-heated grain (Festenstein et al. 1965). Species that occurred frequently, and in great amounts, in all the investigated materials were the fungi of the genera Aspergillus, Penicil- lium and Mucor, and thermophilic actinomy- cetes from the genus Streptomyces (especial- ly in hay and straw) and T. vulgaris. The diagnosis of farmer’s lung disease is based on symptoms, radiographic findings, lung function tests and the presence of micro- bial antibodies in serum (Rylander 1985). An antigen panel of four microbes (A. um- brosus, A. fumigatus, T. vulgaris and M. faeni) is used in serological tests for suspected cases of allergic alveolitis in Finland (Terho 1978, Husman et al. 1987). The present results show that different species of Penicil- lium, Aspergillus, Mucor, and Streptomyces are at least as important as the above-men- tioned species in the exposure occurring in agricultural working environments. It has been assumed that thermophilic actinomycetes would be more potent in causing allergic alveolitis than other microbes involved in moulding (Wardrop et al. 1977). There have been cases of allergic alveolitis where the aetio- logical agents have been mesophilic fungi (Terho & Lacey 1979), e.g. spores of Penicil- lium (Fergusson et al. 1984, Solley & Hyatt 1980). Thus any kind of moulding causing high concentrations of airborne spores should be considered an undesirable phenomenon. References Andersen, A.A. 1958. New sampler for the collection, sizing and enumeration of viable airborne particles. J. Bacteriol. 76: 471—484. Asmundsson, T., Gunnarsson, E. & Johannesson, T. 1983. “Haysickness” in Icelandic horses: Precipitin tests and other studies. Equine Vet. J. 15: 229—232. Cross, T., Maciver, A.M. & Lacey, J. 1968. The ther- mophilic actinomycetes in mouldy hay: Micropoly- spora faeni sp.nov. J. Gen. Microbiol. 50: 351 —359. Corbaz, R., Gregory, P.H. & Lacey, M.E. 1963. Ther- mophilic and mesophilic actinomycetes in mouldy hay. J. Gen. Microbiol. 32: 449—455. 289 Ferousson, R.J., Milne, L.J.R., & Crompton, G.K. 1984. Penicillium allergic alveolitis: Faulty installa- tion of central heating. Thorax 39: 294—298. Festenstein, G.N., Lacey, J., Skinner, F.A., Jenkins, P.A. & Pepys, J. 1965. Self-heating of hay and grain in Dewar flasks and the development of farmer’s lung antigens. J. Gen. Microbiol. 41: 389—407. Gregory, P.H. & Lacey, M.E. 1963. Mycological exami- nation of dust from mouldy hay associated with farm- er’s lung disease. J. Gen, Microbiol. 30: 75—88. Husman, K., Vohlonen, L, Terho, E.O. & Mäntyjärvi, R.A. 1987. Precipitins against microbes in mouldy hay in the sera of farmers with farmer’s lung or chronic bronchitis and of healthy farmers. Eur. J. Respir. Dis., Suppl. 152, 71: 122—127. Kotimaa, M., Kärenlampi, L., Terho, E.0., Husman, K. & Tupi, K. 1984. Exposure to biological dusts in agrigulture. Part 2. At the end of the indoor feeding season for cattle. (In Finnish with Swedish and Eng- lish summaries.) Publications of the Institute of Oc- cupational Health No. 142., Institute of Occupational Health, Helsinki. —, Mustonen, M. & Husman, K. 1983. The effect of ADD-H preservative (ammonium propionate on the moulding of baled hay. J. Sci. Agric. Soc. Finland 55: 371—383. —, Tupi, K., Kärenlampi, L., Terho, E.0., Alanko, K. & Husman, K. 1978. Exposure to biological dusts in agriculture. Part 1. At the beginning of the indoor feeding season for cattle. (In Finnish with Swedish and English summaries.) Publications of the Institute of Occupational Health No. 141., Institute of Occupa- tional Health, Helsinki, Lacey, J. 1971. The microbiology of moist barley stor- age in unsealed silos. Ann. appi. Biol. 69: 187—212. Mulinoe, S.K. & Chesters, C.G.C. 1970. Ecology of fungi associated with moist stored barley grain. Ann. appi. Biol. 65: 277—284. Mustonen, M., Husman, K., Kotimaa, M. & Kärenlam- pi, L. 1983. Molds and actinomycetes in grain: The concentrations of spores in work environments. (In Finnish with Swedish and English summaries.) Pub- lications of the Institute of Occupational Health 1: 46—60, 69—70, 72—73. , Kotimaa, M., Terho, E.0., Husman, K. & Kären- lampi, L. 1984. The preservation methods of hay and silage and the mold exposure. (In Finnish with Swedish and English summaries.) Publications of the Institute of Occupational Health No. 206, Institute of Occupa- tional Health, Helsinki. Pepys, J. 1969. Hypersensitivity diseases of the lungs due to fungi and organic dusts. In: Monographs in Al- lergy, Vol. 4, P. Kallos, M, Hasek, T.M. Inderbitzin, P.A. Miescher and B.H. Waksman, eds. S. Karger, Basel. Pether, J.V.S. & Greatorex, F.B. 1976. Farmer’s lung disease in Somerset. Br. J. Ind. Med. 33: 265—268. Pirie, H.M., Dawson, C.0., Breeze, R.G., Wiseman, A. & Hamilton, J. 1971, A Bovine disease similar to farmer’s lung: Extrinsic allergic alveolitis. Vet. Rec. 88: 346—351. Russel, R.S. 1974. Mycology guidebook. University of Washington Press, Seattle. Rylander, R. 1985. Organic dusts and lung reactions exposure characteristics and mechanisms for disease. Scand. J. Work Environ. Health 11: 199—206, Solley, G.O. & Hyatt, R.E. 1980. Hypersensitivity pneumonitis induced by Penicillium species. J. Allergy Clin. Immunol. 65: 65—70. Terho, E.O. 1978. Microbiological and serological studies on farmer’s lung disease. Publications of the University of Kuopio, Medicine, Series Original Reports 1/1978. University of Kuopio, Kuopio. —, Heinonen, 0.P., Lammi, S. & Laukkanen, V. 1987. Incidence ofclinically confirmed farmer’s lung in Fin- land and its relation to meteorological factors. Eur. J. Respir. Dis., Suppl. 152, 71: 47—63. & Lacey, J. 1979. 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Vohlonen, 1., Tupi, K., Terho, E.O. & Husman, K. 1987. Prevalence and incidence of chronic bronchitis and farmer’s lung with respect to the geographical location of the farm and to the work of farmers. Eur. J. Respir. Dis., Suppl. 152, 71: 37—46. Wardrop, V.E., Blyth, W. & Grant, W.B. 1977. Farm- er’s lung in a group of Scottish dairy farms. Br, J. Ind. Med. 34: 186—195. Wiseman, A., Selman, 1.E., Dawson, C.0., Breeze, R.G. & Pirie, H.M. 1973. Bovine farmer’s lung: A clinical syndrome in a herd of cattle. Vet. Rec. 93: 410—417. Ms received August, 8, 1989 290 SELOSTUS Varastoidun heinän, viljan ja oljen käsittelystä aiheutuva itiöaltislus Marjut Kotimaa Kuopion aluetyöterveyslaitos, PL 93, 70701 Kuopio Työssä tutkittiin tavanomaisissa tilaolosuhteissa heinän, viljan ja kuivikkeina käytettävien olkien käsittelyn aiheut- tamaa homepölyaltistusta sisäruokintakauden lopulla. ll- manäytteet mikrobien määrittämiseksi kerättiin kuusivaihe-impaktoria (malli 10-800, Andersen Inc.) käyt- täen. Kuivikeolkien (n =5) aiheuttama homepölyaltistus (3.7x10s cfu/m 3) oli merkittävästi suurempi kuin heinien (n =33) (0.6 x 10s cfu/m 5) tai rehuviljan (u =2) (0.2x10 s cfu/m 3). Spontaania lämpenemistä osoittavien termo- tolerantlien sienten ja termofiilisten aktinomykeettien esiintyminen oli ominaista oljille. Heinästä irronneiden termotoleranttien sienten itiöiden määrä oli vain noin 10 % ja viljasta irronneiden alle 1 % olkeen verrattuna, termofiilisten aktinomykeettien itiöitä irtosi heinästä vas- taavasti noin 5 % ja viljasta 0.4 % oljesta irronneisiin määriin verrattuna. Kuivikeolkien aiheuttaman itiöaltistuksen valtalaji oli Thermoaclinomyces vulgaris, heinän ja viljan puolestaan Aspergillus umbrosus. Kaikissa materiaaleissa esiintyi run- saasti erilaisia varastosieninä tunnettuja Aspergillus- ja Peniciiiium -suvun lajeja (mm. Aspergillus (A.) fumiga- tus, A. ochraceus, A. flavus, A. repens, A. versicolor, Peniciiiium (P.) expansum, P. piceum, P. citrinum, P. brevicompaclum, P. echinulalum, P. verrucosum var. cyclopium). Heinissä esiintyi tyypillisesti myös ns. pelto- sieninä pidettyjä Ciadosporium-suvun lajeja, kuten Cla- dosporium (C.) herbarum, C. cladosporioides ja C. ma- crocarpum. Saadut tulokset osoittavat, että rehujen jakui- vikkeiden käsittely maataloudessa altistaa perinteisesti ho- mepölykeuhkonaiheuttajina tunnettujen mikrobien lisäksi mm. monille Penicillium-suvun homeille. Kuivikeolkien mikrobiologinen laatu oli huono heinään ja viljaan ver- rattuna, heinän laatuvaihtelu oli suurta. Tulokset tuke- vat sitä käsitystä, että varastokuivureita tarvitaan sekä heinän että kuivikeolkien kuivaamiseen, jotta näiden ma- teriaalien homehtumisriski ja altistumisen aiheuttamat ter- veysriskit voitaisiin minimoida. 291