Chapter 12

BOVINE MYCOTIC ABORTION

(Species of Aspergillus, Absidia, Mucor and other moulds)

Bovine abortion associated with fungi has been reported from North America and Europe. Diagnosis is made on the presence of hyphae in the thickened and necrotic placental cotyledons, in the intercaruncular areas, and in the foetal stomach contents. Occasionally skin lesions are present on the foetus. Infection is thought to be primarily respiratory and to be derived from spores in mouldy hay and straw. Placental infection probably takes place by haematogenous spread with an incubation period of one to two months. The condition has been experimentally reproduced by the intravenous injection of spores. No treatment is known but recovery of the dam appears to be spontaneous.

Disease name: Bovine mycotic abortion.

Pathogens:

*pathogenic for experimental animals

Host: Cattle

Geographical Distribution: NorthAmerica and Europe. U. S. A. (T. Smith, 1920), Canada (Rowsell, 1955); Denmark (Bendixen & Plum, 1929), Norway (Iversen & Røed, 1950), Germany (Weidlich, 1952), Great Britain (Ainsworth & Austwick, 1955a, b), Italy (Ballarini, 1955), Netherlands (Engel & Van der Maas, 1955), Portugal (Moreira-Jacob & van Uden, 1955).

The first record of a fungus isolated from bovine foetal membranes was of Mucor rhizopodiformis (Rhizopus cohnii) found growing in a gravid uterus by Theobald Smith (1920). Gilman & Birch (1925) recorded actual abortion and Bendixen & Plum (1929) published a monograph on the disease. Until recently very little attention was paid to these papers, but the work has now been amply confirmed and knowledge of the disease considerably extended. Of the 18 species of fungi so far reported in association with abortions only about half are at present recognized pathogens, but almost all are able to grow at 37°C. In every case of the condition the fungus has been the only significant organism to be isolated from the foetus or its, membranes, often in pure culture, and no concurrent infection by Brucella abortus or Vibrio fetus has been reported.

Symptomatology

Present knowledge of mycotic abortion is limited to the foetus and its membranes, for no author has recorded any noticeable symptoms in the dam, either before or after the act of abortion. A tentative clinical diagnosis may be made on the appearance of the placenta and particularly the cotyledons, and also on the presence of skin lesions on the foetus. Bendixen & Plum (1929) described in detail the characters of the infected placenta, in which the cotyledons may retain much of their maternal portion and are greatly thickened, especially at the margins. Central necrosis is also a common feature. The intercaruncular areas sometimes have a leather-like consistency with discrete and confluent thickenings.

Weidlich (1952) first observed skin lesions on a foetus and isolated Aspergillus fumigatus from them, but according to Austwick & Venn (1957) they are probably an unusual feature, having been present on only two out of 43 infected foetuses. One of these foetuses was about seven months old and had discrete, raised areas on the skin of the back and head and the other, about 3-4 months old, had diffuse whitish and wrinkled areas on the skin of the flanks, the neck and the axillae.

Pathology

Direct microscopic examination of the cotyledons and intercaruncular areas by crush preparations reveals the presence of hyphae in the tissue. In the amniotic fluid and the foetal stomach contents groups of hyphae may be clearly visible to the naked eye as feathery clumps often mixed with plaque-like aggregations of squamous epithelial cells. Hyphae are also easily detected in the foetal skin lesions.

Histological examination of the affected cotyledons by Bendixen & Plum (1929) showed extensive hyperaemia and haemorrhage in early infections, with scattered infiltration of polymorphonuclear cells and eosinophiles. Later necrosis spread between the chorion and the placental tissue tending to cause their separation by the formation of an exudate rich in hyphae. In the thickened intercaruncular areas there was marked proliferation of the epithelium with loss of its surface layers. Foetal skin lesions have not been examined histologically.

Mycology

Fungi have been recovered from the placenta, the amniotic fluid, foetal stomach contents and foetal skin lesions. Very rarely have isolations been made from the other organs of the foetus; e.g. the lungs (Moreira-Jacob & van Uden, 1955). Austwick & Venn (1957) found that the best isolation method for foetal stomach contents was to smear them, using a glass spreader, on to a malt agar plate (containing 20 units of penicillin and 40 units of streptomycin per ml.) and to incubate at 37° C. Colonies frequently appeared within 24 hours depending on the species of fungus involved, and the plates were retained for one week.

Isolation from the placenta presents some difficulty, for this material has invariably been exposed to the air, and, more often than not, been dropped on the ground. In this way very heavy fungal contamination may complicate the interpretation of the cultural results, for most of the fungi associated with abortion are also present in the litter and air of cowsheds (Rolle &. Kolb, 1954). Generally the appearance of a fungus within 24 hours from pieces of a placenta plated on to malt agar (prepared as above), will indicate infection, provided the fungus isolated has the same hyphal morphology as that already seen in the material on direct examination. From the stomach contents the fungal growth is usually pure but there may be high bacterial contamination in foetuses aborted more than 24 hours before culture.

The 18 species of fungi recovered from foetuses and placentas cannot all be described here for they differ widely in character. Seven of them are Phycomycetes, 9 Fungi Imperfecti (including one species of yeast and two imperfect states of known Ascomycetes), and one a Basidiomycete. The single Actinomycete (Nocardia asteroides) isolated by Fey et al, (1954) deserves special mention for it will not grow on malt agar as described but will appear on blood agar plates prepared for bacteriological examination. The chief fungus associated with mycotic abortion is Aspergillus fumigatus which has been reported from over 60% of the cases. Absidia ramosa and A. corymbifera are also frequent isolates but the remaining species are rarely reported.

In the foetal stomach contents and the placenta the hyphae of Aspergillus fumigatus are narrow, branching, septate and 1.5-3.0 micra wide. In culture the fruiting structures of this fungus appear as small bluish-green heads with the typical structure of an Aspergillus. The Absidia spp. have hyphae 2.5-7.5 micra wide, of a different appearance, being much branched, non-septate and irregular in outline with numerous swellings. The cultural appearance is also characteristic in its fluffy white growth and the pear-shaped sporangia containing large numbers of spores. The shape of the sporangia distinguishes them from many species of Mucor which have globose sporangia, but the non-septate hyphae are a mucoraceous feature. Yeasts appear as round, oval or elongated budding cells and in culture usually form bacteria-like colonies which are opaque and may produce abundant mycelium in the agar. Other species of fungi also produce characteristic hyphae in pathological material, but isolation is always required for final identification.

Pathogenicity for experimental animals has been established in the case of those species marked with an asterisk in the list of pathogens, but the remaining 10 species have not yet been tested. Gilman & Birch (1925) first injected a pregnant cow with the spores of a Mucor sp. and produced abortion; Bendixen & Plum (1929) made further attempts by intravenous inoculation and were successful in five out of six cases using Aspergillus fumigatus and Absidia ramosa, the abortions taking place 1-2 months after inoculation. The sixth cow of the series died from what appeared to be pulmonary aspergillosis six days after inoculation, but even in this animal there was evidence of the early stages of placental invasion. Experimental feeding of cultures of these two fungi was without result.

Serology

No serological techniques have yet been used in the diagnosis of the disease.

Epidemiology

The epidemiology of the infection is imperfectly understood, but there is every indication that infection is originally derived from the spores of fungi present in large numbers in "mouldy" hay, straw, and feeding stuffs and hence also in the air of cow-sheds (Rolle & Kolb, 1954; Ainsworth & Austwick, 1955 a, b). Support for this assumption is given by the winter rise in incidence of the disease, Ainsworth & Austwick (1955a) having stated that 75% of the cases reported during the A.R.C. Survey of Animal Mycoses occurred between November and May, which corresponds roughly to the time of hay feeding. van Ulsen (1955) also noted that the percentage of cases doubled after the wet summer of 1954 when conditions for hay making were poor. Bendixen & Plum(1929) considered that infection was primarily pulmonary but only transient in the lungs, spreading haematogenously to the placenta. Jungherr (1935) also thought that infection was respiratory and metastasized to the uterus, rather than ascending the genital tract. Indeed there is no evidence that infection is by the latter route. Rollinson & Haq (1948) reported the isolation of Absidia corymbifera from the preputial washings of a bull and the cervical mucus of a cow it had served, and Ainsworth & Austwick (1955a) gave a list of mould species isolated from the same sites in cases of infertility. Neither paper indicated whether the isolates were derived from spores or from groups of hyphae; a distinction which would have helped to differentiate active growth in the organ concerned from mere contamination. Further work is required on the portal of entry of infection and on the level of spore intake which is likely to set up the condition in susceptible, pregnant cows (see also Chapter 1, Mammalian Aspergillosis).

Treatment

No clinical symptoms have been observed in the dam before or after abortion and no treatment has ever been given to affected animals. As far as known, cows which abort fungus-infected foetuses may calve normally on the next occasion, but this may not always be so (Venn, 1956; personal communication). At present the spontaneous "recovery" of the dam is assumed to follow the regeneration of the uterine wall.

If the 5% infection rate for aborted bovine foetuses reported by Plum (1932) and by Austwick & Venn (1957) is general in temperate countries, measures to reduce this type of abortion are urgently needed, but until subclinical infection of the cow can be detected and the epidemiology is elucidated, some control of the condition might be effected by exercising greater care in the feeding of mouldy hay to pregnant animals. Treatment of hay with fungicides during hay making in order to reduce subsequent mould growth might also help (Kennedy & Schenk, 1954).

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