Concurrent Ascaris infection modulates host immunity resulting in impaired control of Salmonella infection in pigs

Author:

Midha Ankur1ORCID,Oser Larissa1,Schlosser-Brandenburg Josephine1,Laubschat Alexandra1,Mugo Robert M.1,Musimbi Zaneta D.1,Höfler Philipp1,Kundik Arkadi1,Hayani Rima1,Adjah Joshua1,Groenhagen Saskia1,Tieke Malte1,Elizalde-Velázquez Luis E.1,Kühl Anja A.2,Klopfleisch Robert3,Tedin Karsten4ORCID,Rausch Sebastian1,Hartmann Susanne1

Affiliation:

1. Department of Veterinary Medicine, Institute of Immunology, Centre for Infection Medicine, Freie Universität Berlin, Berlin, Germany

2. Charité Universitätsmedizin Berlin, Corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, iPATH.Berlin, Core unit of Charité, Campus Benjamin Franklin, Berlin, Germany

3. Department of Veterinary Medicine, Institute of Veterinary Pathology, Freie Universität Berlin, Berlin, Germany

4. Department of Veterinary Medicine, Institute of Microbiology and Epizootics, Centre for Infection Medicine, Freie Universität Berlin, Berlin, Germany

Abstract

ABSTRACT Ascaris is one of the most widespread helminth infections, leading to chronic morbidity in humans and considerable economic losses in pig farming. In addition, pigs are an important reservoir for the zoonotic salmonellosis , where pigs can serve as asymptomatic carriers. Here, we investigated the impact of an ongoing Ascaris infection on the immune response to Salmonella in pigs. We observed higher bacterial burdens in experimentally coinfected pigs compared to pigs infected with Salmonella alone. The impaired control of Salmonella in the coinfected pigs was associated with repressed interferon gamma responses in the small intestine and with the alternative activation of gut macrophages evident in elevated CD206 expression. Ascaris single and coinfection were associated with a rise of CD4 - CD8α + FoxP3 + Treg in the lymph nodes draining the small intestine and liver. In addition, macrophages from coinfected pigs showed enhanced susceptibility to Salmonella infection in vitro and the Salmonella- induced monocytosis and tumor necrosis factor alpha production by myeloid cells was repressed in pigs coinfected with Ascaris . Hence, our data indicate that acute Ascaris infection modulates different immune effector functions with important consequences for the control of tissue-invasive coinfecting pathogens. IMPORTANCE In experimentally infected pigs, we show that an ongoing infection with the parasitic worm Ascaris suum modulates host immunity, and coinfected pigs have higher Salmonella burdens compared to pigs infected with Salmonella alone. Both infections are widespread in pig production and the prevalence of Salmonella is high in endemic regions of human Ascariasis, indicating that this is a clinically meaningful coinfection. We observed the type 2/regulatory immune response to be induced during an Ascaris infection correlates with increased susceptibility of pigs to the concurrent bacterial infection.

Funder

Deutsche Forschungsgemeinschaft

Publisher

American Society for Microbiology

Reference67 articles.

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