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Exposure to Rumen Protozoa Leads to Enhancement of Pathogenicity of and Invasion by Multiple-Antibiotic-Resistant Salmonella enterica Bearing SGI1

Mark A. Rasmussen, Steve A. Carlson,^* Sharon K. Franklin, Zoe P. McCuddin, Max T. Wu, and Vijay K. Sharma

Pre-harvest Food Safety and Enteric Disease Research Unit, National Animal Disease Center, USDA, Agricultural Research Service, Ames, Iowa 50010

Received 17 December 2004/ Returned for modification 12 February 2005/ Accepted 15 March 2005

Multiple-antibiotic-resistant Salmonella enterica serotype Typhimurium is a food-borne pathogen that has been purported to be more virulent than antibiotic-sensitive counterparts. The paradigm for this multiresistant/hyperpathogenic phenotype is Salmonella enterica serotype Typhimurium phage type DT104 (DT104). The basis for the multiresistance in DT104 is related to an integron structure designated SGI1, but factors underlying hyperpathogenicity have not been completely identified. Since protozoa have been implicated in the alteration of virulence in Legionella and Mycobacterium spp., we attempted to assess the possibility that protozoa may contribute to the putative hypervirulence of DT104. Our study reveals that DT104 can be more invasive, as determined by a tissue culture invasion assay, after surviving within protozoa originating from the bovine rumen. The enhancement of invasion was correlated with hypervirulence in a bovine infection model in which we observed a more rapid progression of disease and a greater recovery rate for the pathogen. Fewer DT104 cells were recovered from tissues of infected animals when protozoa were lysed by preinfection chemical defaunation of the bovine or ovine rumen. The protozoan-mediated hypervirulence phenotype was observed only in DT104 and other Salmonella strains, including serovars Agona and Infantis, possessing SGI1.

Editor: J. D. Clements

M.A.R. and S.A.C. contributed equally to this work.

Present address: Walter Reed Army Institute of Research, Silver Spring, MD 20910.

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