Listeria monocytogenes is a bacterium capable of surviving and multiplying in a wide range of environments including moist soil, the gastro-intestinal tract of normal animals and in silage that has been exposed to air and has a pH of above 4.5. A range of serovars can cause several disease entities in animals (Quinn et al 1994, Radostits et al 2007, Zachary 2007). In Australian sheep, these entities include meningo-encephalitis, abortions and stillbirths, septicaemia, enteritis (Glastonbury, 1990) and, rarely, post-dipping myelitis (Seaman et al, 1990). Of these entities, abortions and neonatal mortality are most commonly reported in Australia (McDonald 1967, Broadbent 1972, Hughes 1975). Elsewhere, encephalitis, often associated with silage feeding, is more common (Woolford 1990, Zachary 2007). This case, in which 40 of 1700 sheep died after being fed silage, supports the observation that livestock vary in susceptibility to L. monocytogenes, with mature sheep and in particular pregnant ewes being most susceptible.
On 18/09/2006, one of us (Dr Ruth Thompson) took a call from a producer who reported 25 dead sheep subsequent to feeding silage in a drought feedlot. He was feeding cattle and 1700 sheep of all ages including pregnant ewes. This producer routinely made silage and fed it to cattle but this was his first experience in feeding silage to sheep. The cattle were fed silage in bins or spread on the ground. When fed to the sheep the silage was mixed with grain and chopped hay.
This silage was stored in a 400 tonne above ground stack, which was considered to be air free and well stored under plastic, soil and tyres. The silage had been fed to cattle with no problems noted. The owner had previously fed silage from small bags to the sheep uneventfully but lost 25 sheep after commencing feeding from the 400 tonne above ground pile. There were no losses in any other groups of animals.
All affected sheep were from 2 - 5 years of age. Clinical signs started with central nervous system involvement. The producer described a range of signs in affected sheep, including circling, nystagmus, recumbency and apparent blindness. Most progressed over several days to recumbency then death. While many of the affected sheep were pregnant, no abortions or stillbirths were seen.
A merino ewe in good condition and at an advanced stage of pregnancy was presented for examination. It was unable to stand and could sit in sternal recumbency but tended to fall to one side. Nystagmus was observed.
The ewe was euthanased for autopsy. The forestomachs were full but the intestines had little ingesta, suggesting stasis. The liver was pale yellow-orange, with rounded edges. A full term, viable foetus was present.
Brain sections from the cerebrum, cerebellum, brain stem (at the level of thalamus, lateral geniculate body, superior colliculi, caudal cerebellar peduncles and obex) and cervical spinal cord were examined. The meninges in brain and spinal cord sections showed a moderate non-suppurative meningitis. Blood vessels in all brain stem sections and the cerebellum had mononuclear perivascular cuffs, most severe in the caudal brainstem sections. In the parenchyma of all brain stem sites and the cervical spinal cord, glial nodules (consisting of glial cells admixed with varying numbers of neutrophils) could be seen, most prominent in the caudal brainstem sections. Additionally, in the caudal brainstem sites, microabscesses (necrotic foci with neutrophil infiltration) were present, as well as a more extensive area of malacia infiltrated by neutrophils and surrounded by glial cells and macrophages.
Other findings in the brain included Wallerian degeneration in the cerebellar white matter and axonal degeneration in the cervical spinal cord; a single protozoal form in the cerebral cortex was considered to be an incidental finding. The liver showed moderate hydropic degeneration of hepatocytes. There were no significant findings in the heart, kidney and small intestine.
No bacteria could be detected on a Gram stained caudal brainstem section. On routine culture of cervical spinal cord there was scant pure growth of Listeria monocytogenes. Listeria spp. were not isolated from the liver.
A pathological diagnosis of moderate non-suppurative meningitis and severe subacute pyogranulomatous encephalitis was made.
Glial nodules and microabscesses in the brainstem, most prominent in the caudal brainstem, are considered to be pathognomonic for listeriosis. Further confirmation was obtained by culturing the organism from the spinal cord. Culture is not successful in all cases. Gram positive organisms could not be detected in this case. The organism is sometimes present in small numbers and only in some lesions.
The owner ceased feeding silage to his sheep, but sheep continued to die from listeriosis for three weeks after cessation of silage feeding; in total, 40 sheep died. No abortions were observed. The batch of silage was diluted with hay before continuing to feed it to the cattle, which suffered no adverse consequences. The owner continues to feed silage to his cattle but has not subsequently fed silage to sheep and commented that he would investigate testing silage for Listeria before feeding it to sheep in future.
Ensilage is a valuable method of fodder conservation. If well made from quality crops or pastures, it is nutritious and palatable. However, like just about every other feedstuff, crop or pasture fed to livestock it has some risks, one of which is Listeria. There are two ways of managing this risk. The first is to make silage in a manner least favourable to Listeria. Unfortunately, while this is also consistent with good practice, it is difficult to achieve completely in practice. Silage that is compacted so that it undergoes anaerobic fermentation, has a pH under 4.5 and has no incorporated soil is least conducive to Listeria growth.
The second option in managing the risk of Listeria is to feed it to the least susceptible livestock. Woolford (1990) noted that silage-associated listeriosis is mainly confined to sheep. In this case, pregnant ewes were most susceptible, while young sheep and cattle were not affected.
At least based on present knowledge, we believe it is not practical to test silage for Listeria. It is likely to be unevenly distributed, favouring areas of aerobic decomposition. Silage may also contain strains of Listeria of low pathogenicity or present at low levels, making it safe to feed to appropriate classes of livestock.
A further point of interest in this case is that no ewes were seen to abort. As these sheep were run in a feedlot, abortions should have been more obvious than usual. Listeria monocytogenes is commonly implicated in abortions and neonatal mortality in sheep either sporadically or in epizootics. However, there are strain differences.
There are several species of Listeria, including L. monocytogenes and L. ivanovii. L ivanovii only causes abortions in sheep and cattle. Within Listeria monocytogenes however, are a wide range of strains of varying pathogenicity causing a range of disease syndromes in a range of hosts (Quinn et al 1994). The organism appears to be ubiquitous and an opportunistic pathogen of humans and animals (Gudmundsdottir et al 2004). Some of the strains of L monocytogenes only cause abortions in sheep, while others cause both encephalitis and abortions (Hughes, 1975). Wagner et al (2005) reported a case in sheep fed silage in which all three entities (encephalitis, abortions and septicaemia) occurred. In this case, only encephalitis occurred, despite the infection being confined to pregnant ewes.
Listeria monocytogenes is a potential zoonosis. Both sheep and cattle can develop sub-clinical mastitis and secrete L. monocytogenes in the milk. This is a public health risk. However correctly made cheese has a low pH inimical to Listeria survival and pasteurisation presumably kills Listeria (Winter et al 2004, Wagner et al 2005). However, Hughes (1975) warns that, since Listeria is ubiquitous and is commonly carried in the faeces of man, listerial infection in man should not automatically be assumed to be of zoonotic origin. Hughes (1975) also cautions that in ovine abortion or lamb mortality investigations in particular, Listeria may be associated with other pathogens. He warns that in this instance the isolation of L. monocytogenes from merely one or two cases does not constitute sound epidemiological evidence necessary to ascribe an unusual incidence of events to the effects of that microbe.