Listeria monocytogenes translocates throughout the digestive tract in asymptomatic sheep

Abstract

Ruminants are fed forage which is often contaminated with Listeria, and frequently shed Listeria monocytogenes with their faeces. The present study was designed to localize the sites of infection in the digestive tract concomitant with Listeria faecal excretion in a sheep model. Ten Listeria-free sheep were inoculated per os with a dose of 10 10 c.f.u. of a pathogenic L. monocytogenes strain. Listeria received by two of the ten animals were radiolabelled with 111 indium oxine. The dissemination of the Listeria was assessed by in vivo imaging, by culture of bacteria in the faeces, organs and digesta samples taken at slaughter on days 1, 2, 6, 10 and 14 post-inoculation, and by measuring gamma radioactivity of samples on day 6. It was shown that Listeria spread through the entire volume of the forestomachs within 4 h, and through the whole gastrointestinal tract (GIT) within 24 h. Faecal shedding of Listeria lasted 10 days. Rumen, duodenum, jejunum, ileum, caecum and colon walls and digesta, mesenteric lymph nodes, liver and spleen were temporarily infected. However, Listeria persisted for at least 14 days in rumen digesta and retropharyngeal lymph nodes, and at a relatively high level (1610 4 c.f.u. g "1 ) in palatine tonsils. These findings suggest that L. monocytogenes can translocate from all parts of the GIT, with the rumen digesta, but not the gallbladder, serving as a reservoir. The results indicate that brief and low-level faecal excretion of L. monocytogenes is concomitant with a transitory asymptomatic infection in sheep. INTRODUCTIONThe Gram-positive bacterium Listeria monocytogenes is widespread in nature and frequently contaminates fodder (Fenlon, 1999). It is associated with several diseases (listeriosis) in both humans and animals (Low & Donachie, 1997). Humans generally become infected with L. monocytogenes by consuming contaminated food products (Slutsker & Schuchat, 1999). Sheep, cattle and goats often shed L. monocytogenes in their faeces without symptoms (Wesley, 1999). The farm sources of contamination for human foods such as milk are the animals themselves and the environment (McLauchlin, 1997). Since L. monocytogenes mastitis is rare (Jensen et al., 1996), raw milk is mainly contaminated from the environment, probably by faeces when farming and milking procedures are carried out under conditions of inadequate hygiene (Sanaa et al., 1993). Two-month-old lambs experimentally inoculated with a 6610 10 c.f.u. oral dose shed L. monocytogenes with faeces, but lambs inoculated with a 6610 6 c.f.u. dose did not (Lhopital et al., 1993). The lambs of both groups had detectable IgG antibodies to listeriolysin O (LLO), suggesting that a subclinical infection had occurred (Lhopital et al., 1993). Older sheep also orally inoculated with a 10 10 c.f.u. dose remained well, and triggered the production of anti-LLO antibodies (Baetz et al., 1996;Low & Donachie, 1991). We have recently shown that sheep given a 10 4 or 10 6 c.f.u. dose do not develop antibodies to LLO or IrpA (Zundel et al., 2006), unlike those...

Enteric listeriosis in a 10-month-old calf

“…The recovery of L. monocytogenes by itself is insufficient evidence of disease, as transient asymptomatic infection of sheep can occur. In such sheep L. monocytogenes can be cultured from samples collected throughout the gut, and even from the mesenteric lymph nodes, liver, and spleen (Zundel and Bernard 2006).…”

Listeria monocytogenes: survival and adaptation in the gastrointestinal tract

“…It is significant that L. monocytogenes can colonize the murine gall bladder following oral or intravenous administration (Hardy et al, 2004; Bron et al, 2006). It can also be isolated from the gall bladder in infected guinea pigs (Jensen et al, 2008) and turkeys (Huff et al, 2005), but not in infected sheep (Zundel and Bernard, 2006). There is also evidence suggesting that L. monocytogenes may be a rare cause of human cholecystitis (infection of the gall bladder) (Allerberger et al, 1989; Descy et al, 2012; Bruminhent et al, 2013).…”

Rhombencephalitis Caused byListeria monocytogenesin Humans and Ruminants: A Zoonosis on the Rise?

“…Ruminants, particularly cattle, contribute to amplification and dispersal of LM into the farm environment [120]. The bacteria can be shed in the feces of clinically affected animals, but also healthy carriers [90, 92, 107, 119, 128, 130, 339, 346, 347]. Raw milk might contain LM either as a consequence of bacterial shedding in the milk or due to exogenous contamination from the dairy farm environment [291, 340, 348–355].…”