Listeriosis in Ruminants: Circling Disease and Silage-Associated Infection

Introduction

Listeriosis represents a significant bacterial disease complex affecting domestic ruminants worldwide, caused primarily by the facultative intracellular pathogen Listeria monocytogenes. The disease manifests in several clinical forms, with encephalitic listeriosis (commonly termed "circling disease") being the most recognized in sheep and goats, followed by septicemic, abortive, and enteric forms. The strong epidemiological association with consumption of poorly preserved silage has been documented for decades, making listeriosis a classic silage-associated infection in cattle, sheep, and goats [1, 2]. A systematic review and meta-analysis by Lopez-Almela et al. [1] confirmed that the overall prevalence of listeriosis in ruminants ranges from 2% to 15% depending on geographic region, diagnostic method, and animal species, with sheep showing higher encephalitic form rates than cattle.

Recent genomic and epidemiological investigations have expanded the understanding of Listeria species diversity in livestock environments, including the identification of potentially virulent Listeria innocua strains [3] and the characterization of Listeria ivanovii subsp. londoniensis from ovine farms [4]. This article provides an exhaustive reference on listeriosis in ruminants, integrating classical knowledge with contemporary molecular findings, diagnostic advancements, and control strategies.

Etiology and Pathogen Biology

The genus Listeria comprises at least six species, with L. monocytogenes being the principal pathogen in ruminants. Listeria ivanovii is occasionally associated with disease, primarily abortion and enteritis in sheep [4]. Listeria innocua is historically considered non-pathogenic, but genomic characterization of isolates from cattle farm environments has revealed the presence of virulence-associated genes, including truncated versions of inlA and inlB, raising questions about its pathogenic potential [3].

Key Virulence Factors

The pathogenesis of L. monocytogenes hinges on a suite of virulence determinants that facilitate intracellular survival and cell-to-cell spread. The internalin family (InlA, InlB) mediates invasion of host cells. In ruminant neurolisteriosis, the trigeminal ganglion serves as a critical entry point following oral or nasal exposure. Lv et al. [5] demonstrated the synergistic roles of InlA, InlB, and listeriolysin O (LLO) in ovine-derived L. monocytogenes LM90SB2 infection of trigeminal ganglion neurons. InlA binds to E-cadherin on epithelial cells, while InlB interacts with c-Met receptor, facilitating internalization. Once inside the phagosome, LLO mediates escape into the cytosol.

The surface protein ActA is essential for actin-based motility, enabling direct cell-to-cell spread without exposure to the extracellular environment. This mechanism underlies the ability of L. monocytogenes to traverse the blood-brain barrier and establish infection in the brainstem, leading to the characteristic clinical syndrome of circling disease [6, 2].

Comparative Infection Pathways

Comparative infection pathways between humans and ruminants exhibit both similarities and differences. Teixeira et al. [7] highlighted that in ruminants, the oral route via contaminated silage is predominant, while human listeriosis is often foodborne from dairy or meat products. The tropism for the central nervous system (CNS) in ruminants is more pronounced, possibly due to species-specific differences in E-cadherin expression and the efficiency of retrograde axonal transport from the oral cavity to the brainstem [5, 7].

Epidemiology

Host Range and Geographic Distribution

Listeriosis affects a broad range of domestic ruminants, with sheep, goats, and cattle being the most frequently reported species. Wareth et al. [8] analyzed the current situation of animal listeriosis in Germany over 2024-2025 and found a sustained incidence of encephalitic cases in small ruminants, alongside sporadic bovine abortions and mastitis. The authors emphasized the need for a structured surveillance system in the animal health sector, as listeriosis is underreported in many countries [8].

Global prevalence estimates from the systematic review by Lopez-Almela et al. [1] indicate that the overall proportion of listeriosis in ruminant populations is approximately 5.4% (95% CI: 3.2-8.1), with higher rates in small ruminants than cattle. Regional variation is significant; for example, studies from Egypt [9] and Jordan [10] report high prevalence and multidrug resistance, while Uruguayan bovine cases [11] show a predominance of lineage II strains.

Silage as the Primary Risk Factor

The link between listeriosis and silage feeding is well-established. Poorly fermented silage, especially with pH above 5.0, permits growth of L. monocytogenes. Silage-associated outbreaks typically occur in winter and early spring when animals are housed and fed conserved forage. Koncurat and Sukalic [2] reviewed that the bacterium can multiply in silage under aerobic conditions, particularly in surface layers exposed to air after opening. Enteric listeriosis in ewes grazing stubble has also been reported, suggesting alternative transmission routes [12].

Environmental Reservoirs and Transmission

L. monocytogenes is ubiquitous in soil, water, and vegetation. Wastewater and natural environments serve as reservoirs for lineage I clones that predominate in ruminant and human cases [13]. Direct transmission between animals is rare, but fecal shedding can contaminate feed and water. Vertical transmission can lead to abortion. The role of vectors such as ticks in transmission is negligible, unlike the situation with Mycoplasma bovis in feedlot cattle.

Clinical Signs: Circling Disease and Other Presentations

Encephalitic Form (Circling Disease)

The neurological form, commonly called "circling disease," is most frequent in sheep and goats. It results from ascending infection along the trigeminal nerve after oral inoculation. Initial signs include depression, anorexia, and fever. Unilateral cranial nerve deficits ensue, with head tilt, facial paralysis, drooping ear, and deviation of the muzzle. The hallmark sign is compulsive circling toward the affected side. Progression to recumbency, opisthotonos, and death occurs within 4-14 days without treatment [2, 14]. Ovine listerial encephalitis was noted as a common diagnosis in the first quarter of 2023 in the UK [14], highlighting its seasonal clustering.

Septicemic Form

More common in young ruminants, especially lambs and calves. Clinical signs include fever, depression, diarrhea, and rapid progression to septic shock. Mortality is high. This form may be associated with lineage I strains [13].

Abortive Form

L. monocytogenes and L. ivanovii can cause late-term abortion in sheep, goats, and cattle. Infection occurs via the hematogenous route after ingestion. The dam may show no other signs, but retained placenta and metritis can occur.

Enteric and Mastitic Forms

Enteric listeriosis presents with diarrhea, dehydration, and weight loss, often in ewes on poor-quality silage [12]. Mastitis, sometimes subclinical, can lead to contamination of milk. A case of cholangiohepatitis due to L. monocytogenes was reported in a lactating Holstein cow [15], expanding the spectrum of clinical presentations.

Pathology

Gross Lesions

In the encephalitic form, gross lesions may be absent or subtle. On careful examination, small foci of malacia and microabscesses may be visible in the brainstem. The trigeminal nerve root may appear swollen. In septicemic cases, multiple necrotic foci may be present in the liver, spleen, and myocardium. Aborted fetuses show autolysis and occasionally focal hepatic necrosis.

Histopathology

The hallmark histologic lesion is microabscessation with perivascular cuffing in the medulla oblongata and pons. Lesions are characterized by accumulations of macrophages, neutrophils, and occasional eosinophils. Gram-positive rods may be seen intracellularly. In septicemic cases, multifocal necrosis with bacterial colonies is present.

Diagnostics

Clinical and Epidemiological Suspicion

A presumptive diagnosis is based on clinical signs (circling, facial paralysis) combined with a history of silage feeding. However, differential diagnoses include rabies, listeriosis, and other causes of neurologic disease such as polioencephalomalacia, coenurosis, and brain abscess. In goats, neurolisteriosis can be confirmed by fluorescent antibody test (FAT), immunohistochemistry (IHC), or PCR [16]. Rissi et al. [16] compared FAT, IHC, and PCR in 25 goats with neurolisteriosis and found PCR to be the most sensitive method (96% versus 84% for IHC and 76% for FAT), with high agreement among all three tests for formalin-fixed tissues.

Molecular Diagnostics

PCR targeting the hly gene (encoding listeriolysin O) or the iap gene (encoding invasion-associated protein) is the gold standard for detection in tissue, milk, and silage. Quantitative real-time PCR allows quantification of bacterial load. Whole genome sequencing (WGS) is increasingly used for typing and surveillance, as demonstrated by Cheong et al. [17] in small ruminants from integrated crop-livestock systems, and by Rivu et al. [3] for detection of virulence traits in L. innocua.

Serological Tests

An ActA-based competitive ELISA has been developed for specific diagnosis of ovine listeriosis [6]. This assay detects antibodies against the ActA surface protein, which is highly conserved among pathogenic L. monocytogenes strains. Compared to whole-cell ELISAs, the ActA-based ELISA showed 93% sensitivity and 97% specificity for detecting infected sheep [6]. This test is useful for herd-level screening.

Culture and Isolation

Isolation of L. monocytogenes from brainstem, liver, or placenta remains the definitive diagnostic method. Cold enrichment at 4 degrees Celsius for 2-8 weeks is sometimes used for heavily contaminated samples. Selective agars such as PALCAM and Oxford agar are standard. However, culture sensitivity is lower than PCR, especially if animals have been treated with antibiotics.

Antimicrobial Susceptibility Testing

Given the emergence of multidrug resistance, AST is recommended. Obaidat and AlShehabat [10] reported high levels of resistance to tetracycline, streptomycin, and ciprofloxacin in L. monocytogenes from sheep and goat flocks in Jordan, with association to water sources. Sotohy et al. [9] also found significant antibiotic resistance in Egyptian isolates.

The diagnostic workflow for ovine neurolisteriosis is illustrated below.

graph TD
    A[Clinical signs: circling, head tilt, facial paralysis], > B[History of silage feeding?]
    B, > C[Perform neurological exam]
    C, > D[Collect CSF and blood]
    D, > E[PCR for L. monocytogenes hly gene]
    E, > F[Positive?]
    F, >|Yes| G[Confirm with culture or IHC]
    F, >|No| H[Consider differentials: rabies, PEM, coenurosis]
    G, > I[Report and treat]
    H, > J[Additional testing: rabies FAT, thiamine levels]

Treatment

Antimicrobial Therapy

Early and aggressive antimicrobial therapy is critical for encephalitic listeriosis. Penicillin G (high dose, 20,000-40,000 IU/kg IV or IM every 6 hours) is the drug of choice. Oxytetracycline or erythromycin are alternatives. Combination therapy with aminoglycosides has been suggested but carries nephrotoxicity risk. Treatment should continue for 7-14 days. Supportive care including non-steroidal anti-inflammatory drugs and fluid therapy is essential.

Prognosis

Prognosis is guarded to poor once recumbency develops. Even with treatment, mortality rates in encephalitic cases can exceed 50%. Early recognition and treatment improve outcomes. For septicemic and enteric forms, response to therapy varies.

Control and Prevention

Silage Management

Proper ensiling techniques are the cornerstone of prevention. Silage should be harvested at appropriate dry matter, chopped to ensure compaction, and sealed to exclude air. The pH should drop below 4.5 within days. Bunkers should be covered and weighted. Feed-out should remove at least 10-15 cm per day to limit aerobic spoilage. Any moldy or spoiled silage should be discarded.

Vaccination

A live attenuated DIVA (Differentiating Infected from Vaccinated Animals) vaccine has been developed and shown to protect sheep against L. monocytogenes challenge [18]. The vaccine is based on deletion of the actA gene, allowing serological differentiation using ActA-based ELISA [6]. While not yet commercially available, this approach offers promise for endemic flocks.

Herd Biosecurity

Quarantine of new animals, rodent control (rodents shed Listeria in feces), and provision of clean water are important. In outbreaks, removal of silage and thorough disinfection of feeding equipment reduce transmission.

Surveillance and Reporting

As advocated by Wareth et al. [8], a structured surveillance system for animal listeriosis is needed to monitor trends and detect emergence of resistant strains. WGS-based surveillance enables tracking of lineages and clones across livestock, environment, and human cases [17, 13].

Conclusion

Listeriosis in ruminants remains a significant cause of neurological disease, abortion, and septicemia, with a well-described association with silage feeding. The clinical picture of circling disease, though classic, requires confirmatory laboratory diagnosis using PCR, IHC, or culture. Advances in serological diagnostics such as ActA-based ELISA and DIVA vaccines offer new tools for control. Genomic characterization has revealed the complexity of Listeria populations in livestock environments, including the presence of virulence-associated traits in non-pathogenic species. Future veterinary approaches should integrate molecular surveillance, antimicrobial stewardship, and improved silage management to reduce the burden of this disease.

References

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