Progress 09/01/06 to 08/31/09
Outputs
OUTPUTS: Activities included analysis of strains implicated in the 1998-1999 and 2002 multistate outbreaks of listeriosis in terms of resistance to the heavy metal cadmium and to the quaternary ammonium disinfectant benzalkonium chloride (BC), as well as in terms of resistance to Listeria-specific bacteriophage (listeriaphage). Furthermore, we determined whether the plasmids associated with such resistance in the epidemic strains were stable, and whether plasmid content impacted the ability of the bacteria to form biofilms on stainless steel, and to tolerate specific environmental stresses. We examined responses of plasmid-harboring and plasmid-free paired strains to environmental stresses of special food safety relevance, including the ability of the bacteria to grow at low temperature, to tolerate repeated freezing and thawing, and to tolerate low pH. We assessed impact of temperature on resistance to cadmium and to BC, and on resistance to phage. We made significant progress in characterizing the molecular basis for the resistance to cadmium and to BC exhibited by epidemic and other strains. Since in the processing plant environment L. monocytogenes is often accompanied by strains of non-pathogenic Listeria spp., we determined prevalence of resistance to cadmium and to BC among strains of L. innocua and L. welshimeri from the environment of turkey processing plants. We also determined whether the resistance in non-pathogenic Listeria spp. was mediated by genes similar to those harbored by epidemic and other strains of L. monocytogenes. To adequately address the impact of resistance determinants among environmental strains of non-pathogenic Listeria spp. on resistance attributes of epidemic and other strains of L. monocytogenes, we determined dissemination potential of the resistance determinants via conjugations. Lastly, we made significant progress in elucidating the molecular basis for growth temperature-dependent resistance of ECII strains to listeriaphage, and we assessed the ECII-specific diagnostic potential of a panel of DNA probes derived from the genomic region associated with phage resistance, and identified in the course of this project. Events included group presentations in the regular Kathariou lab meeting; six seminars (three by the PI, and three student exit seminars) on research findings from the project, with feedback from individuals with different research backgrounds. One of the seminars by the PI was a keynote presentation at Food Micro 08 (Aberdeen, Scotland) and the other two were at the University of Wisconsin and University of Connecticut, respectively. Lastly, we have filed an invention disclosure related to the use of genetically modified ECII strains that have been constructed in our laboratory. Listeriaphage propagated form such strains is expected to be able to infect other L. monocytogenes, including ECII, even when the bacteria are grown at low temperature. PARTICIPANTS: A total of 34 individuals participated in this project. This included the PI, PI's lab manager, co-PI, nine collaborators, one postdoctoral scientist, ten graduate and 11 undergraduate students. A total of nine Ph.D. Dissertations and one Masters thesis have been supported partially or completely by the grant. Three Ph.D. dissertations (N. Carolina State University) and the M.Sc. thesis (N. Carolina State University) have been already completed. Progress is continuing on all others. Participating individuals were: S. Kathariou, PI; H. Wang, co-PI; C. Czyprynski, collaborator, Univ. of Wisconsin; N. Faith, collaborator, Univ. of Wisconsin; J. B. Luchansky, collaboratorŠ± USDA-ERRC; B. Neudeck, collaboratorŠ± Univ. of Tennessee; K. Sperry, collaborator, Dept of Health, NC; L. Wolff, collaborator, Dept of Health, NC; L. M. Graves, collaborator, CDC; B. Swaminathan, collaborator, CDC; P. Gerner-Smidt, collaborator, CDC; R. M. Siletzky, laboratory manager; D. Elhanafi, postdoctoral associate; Y. Cheng, graduate student; J.-W. Kim, Graduate student; S. Mullapudi, graduate student; R. Azizoglu, graduate student; S. White, graduate student; L. Zhang, graduate student; A. Wassinger, graduate student; S. Lee, graduate student; V. Dutta, graduate student; R. Sahaghian, graduate student; Z. Byrd, undergraduate student; J. Hieronymi, undergraduate student; L. Rutger, undergraduate student; L. McLees, undergraduate student; V.Thanawala, undergraduate student; M. Yonas, undergraduate student;S. Ratani, undergraduate student; S. Lanwermeyer, undergraduate student; S. Wilson, undergraduate student; B. Z. Huang, undergraduate student; J. Beane, undergraduate student. Extensive opportunities were provided for training and professional development for student and postdoctoral participants in the project. Students and the postdoctoral scientist presented their research at the Kathariou laboratory meetings, and were encouraged and guided to present their findings at local (University and state) and international meetings (ASM, IAFP, ISOPOL). They received safety training and acquired expertise in safe laboratory procedures during work with potential human pathogens. They worked as members of teams, thus developing team-working skills. They were guided in the process of preparing manuscripts, theses, and presentations (posters, oral presentations). They were guided in the critical analysis of relevant scientific literature. They were guided in becoming familiar with principles of research and professional ethics through continuous feedback and guidance, specific presentations, and attendance of relevant classes at the University. Assistance and guidance were provided in identifying professional and training opportunities upon completion of their involvement in the laboratory. TARGET AUDIENCES: The findings are targeted to the food safety and public health sector, who would be interested in the identification and characterization of special attributes associated with Listeria strains that cause epidemics of listeriosis; the food industry and environmental sanitation sector, since disinfectant use and exposure to disinfectant and heavy metals was shown to be a characteristic of lineages involved in several multistate outbreaks, as well as in isolates form the environment of food processing plants; to regulatory agencies and biotechnology sectors, since strains constructed in this work can optimize the use of phages as biocontrol for Listeria, and minimize the potential that phage controls can inadvertently select for especially problematic strains (e.g. Epidemic Clone II). The findings are also targeted to the microbiology, microbial ecology, bacterial genetics, and evolutionary biology communities, since they contribute to the elucidation of novel adaptations of bacterial foodborne pathogens, including resistance to disinfectants, biofilm formation, resistance to phage, and acquisition and control of accessory genetic elements such as plasmids. Our findings in these areas are of special relevance for Listeria, a foodborne pathogen especially problematic due to its ability to persistently colonize the environment of food processing plants and other niches where food may be stored or prepared. PROJECT MODIFICATIONS: Nothing significant to report during this reporting period.
Impacts
Strains from the 1998-99 multistate outbreak of foodborne listeriosis harbored a large (ca. 80 kb) plasmid that conferred resistance to the heavy metal cadmium and to the quaternary ammonium disinfectant, benzalkonium chloride (BC). The cadmium resistance cassette consisted of two novel genes, cadA cadC, which were distinct in DNA sequence from those earlier found in association with Tn5422. The BC resistance cassette was also identified in the plasmid from the 1998-1999 strains. It was shown to be highly conserved at the nucleotide sequence level among all tested BC-resistant strains of L. monocytogenes. Recombinant plasmids harboring this cassette conferred BC resistance to BC-susceptible strains. We found that resistance to cadmium and to BC was highly prevalent among isolates from food processing plants. Furthermore, all BC-resistant isolates were also resistant to cadmium. We found that strains resistant to both cadmium and BC were significantly more likely to harbor the novel cadA cadC genes than strains resistant to cadmium but susceptible to BC. The findings suggest that resistance to BC may be acquired by plasmid elements that already harbored cadA2, resulting in elements with dual resistances (as demonstrated with pLM80 of the strains from the 1998-99 outbreak). We have also detected these resistance cassettes in the genomes of non-pathogenic Listeria spp., and shown the potential of resistance to be disseminated via conjugations among these non-pathogenic strains. Biofilm assays with L. monocytogenes on stainless steel revealed that the strain from one of the multi-state outbreaks was superior in its fitness following establishment in biofilms and exposure to disinfectants. Resistance to cadmium and to BC was not impacted by growth temperature, but cells became highly susceptible to BC when grown in liquid medium. Thus, high levels of BC resistance require not only the genes in the BC resistance cassette but also bacterial cells that are grown on solid media. Certain stress responses were profoundly impacted by temperature of growth. Specifically, bacteria grown at 37C were markedly more resistant to repeated freezing and thawing than those grown at 4C or 25C. Furthermore, ECII strains were listeriaphage-resistant when grown at temperatures below 30C, whereas bacteria grown at 37C were susceptible. Deletion of a specific gene abolished this phenotype, allowing ECII strains to be susceptible to listeriaphage regardless of the temperature at which they were grown. Analysis of the sequence of the relevant gene revealed that it was present in the sequenced ECII strain but not in other sequenced genomes. DNA hybridizations involving multi-strain arrays on nylon membranes revealed that the gene was specific to ECII, and unique for this clonal group, thus identifying a valuable DNA probe for this epidemic clone. This DNA probe will facilitate monitoring and detection of ECII, and has been already successfully employed in our surveys of panels of isolates from human listeriosis.
Publications
- Sperry, K. E. , S. Kathariou, J. S. Edwards, and L. A. Wolf. 2008. Multiple-locus variable-number tandem-repeat analysis as a tool for subtyping Listeria monocytogenes strains. J. Clin. Microbiol. 46:1435-1450. Cheng, Y., N. Promadej, J. W. Kim, and S. Kathariou. 2008. Teichoic acid glycosylation mediated by gtcA is required for phage adsorption and susceptibility of Listeria monocytogenes serotype 4b. Appl. Environ. Microbiol. 74:1653-1655.
- Cheng, Y., R. M. Siletzky, and S. Kathariou. 2008. Genomic divisions / lineages, epidemic clones and population structure of Listeria monocytogenes. Book Chapter, Handbook of Listeria monocytogenes. Dongyou Liu (Ed), Taylor & Francis Group, Inc.
- Kim, J. W., and S. Kathariou. 2009. Temperature-dependent phage resistance of Listeria monocytogenes epidemic clone II. Appl. Environ. Microbiol. 75:2433-2438.
- Pan, Y, F. Breidt, Jr, and S. Kathariou. 2009. Competition of Listeria monocytogenes serotype 1/2a and 4b strains in mixed culture biofilms. Appl. Environ. Microbiol. Jul 31. [Epub ahead of print]
- Azizoglu, R. O., J. Osborne, S. Wilson, and S. Kathariou. 2009. Role of growth temperature on freeze-thaw tolerance of Listeria spp. Appl. Environ. Microbiol. 75:5315-5320.
- Faith, N., S. Kathariou, Cheng, Y., Promadej, N., Neudeck, B. L. , Zhang, Q., Luchansky, J., Czuprynski, C. 2008. The role of Listeria monocytogenes serotype 4b gtcA in gastrointestinal listeriosis in A/J mice. Foodborne Pathog Dis. 2008 Nov 9. Epub ahead of print].
- Kim, J. W., Siletzky, R. M., Kathariou, S. 2008. Host ranges of Listeria-specific bacteriophages from the turkey processing plant environment in the United States. Appl Environ. Microbiol. 74:6623-6630.
- Mullapudi, S., R. M. Siletzky, and S. Kathariou. 2008. Heavy metal and benzalkonium chloride resistance of Listeria monocytogenes from the environment of turkey processing plants. Appl. Environ. Microbiol. 74:1464-1468.
- Faith, N. G, S.Kathariou, R. Sahaghian, J. B. Luchansky, and C. J. Czuprynski. 2009. Virulence for mice, resistance to synthetic gastric fluid, and biofilm formation of Listeria monocytogenes H7550, a serotype 4b strain isolated from frankfurters associated with the 1998-1999 hotdog listeriosis outbreak. Abstract, Intern. Assoc. Food Prot. Annual Meeting, Grapevine, TX.
- White, S. L., R. M. Siletzky, and S. Kathariou. 2009. Prevalence of inlA premature stop codon mutations in Listeria monocytogenes from the environment of turkey processing plants. Abstract, American Society for Microbiology General Meeting, Philadelphia, PA.
- Wassinger A, Zhang L, Wang HH. 2009. Revealing Listeria monocytogenes Scott A Biofilm Attributes by Expression Analysis. IFT annual meeting poster presentation.
- Azizoglu, R. O., and S. Kathariou. 2007. Role of growth temperature on freeze-thaw resistance of Listeria monocytogenes. International Association for Food Protection, 94th Annual Meeting, July 6-11, Lake Buena Vista, FL.
- Kim, J. W., D. Elhanafi, and S. Kathariou. 2007. Partial analysis of genomic sequence among Listeriaphage 20422-1, 805405-1 (newly isolated in the US) and P100. International Association for Food Protection, 94th Annual Meeting, July 6-11, Lake Buena Vista, FL.
- Elhanafi, D., and S. Kathariou. 2007. Genetic characterization of benzalkonium chloride resistance mechanism in the food-borne pathogen Listeria monocytogenes. Abstract, 16th International Symposium on Problems of Listeriosis. ISOPOL XVI, March 20-23, 2007, Savannah, GA
- Faith, N.G., Cheng, Y., Kathariou, S. , Neudeck, B., Shi, L., and C. J. Czuprynski. 2008. Phenotypic characterization of gtcA transposon mutants of serotype 4b Listeria monocytogenes. Abstract, International Association for Food Protection, Columbus, OH.
- Mullapudi, S., R. M. Siletzky, and S. Kathariou. 2007. Resistance to cadmium and to benzalkonium chloride among Listeria monocytogenes isolates from the environment of turkey processing plants. Abstract, 16th International Symposium on Problems of Listeriosis. ISOPOL XVI, March 20-23, 2007, Savannah, GA
- Azizoglu, R. O. 2009. Temperature-dependent freeze-thaw tolerance and genetic characterization of stress response mechanisms in Listeria spp. Ph.D. Thesis, North Carolina State University.
- Kim, J.-W. 2008. Temperature-dependent phage resistance in Listeria monocytogenes epidemic clone II strain. Ph.D. Thesis, North Carolina State University.
- Mullapudi, S. 2008. Phenotypic and genetic characterization of Listeria monocytogenes from the environment of turkey processing plants. M. Sc. Thesis, North Carolina State University.
- Cheng, Ying. 2007. Genetic characterization of genes specific to Listeria monocytogenes epidemic-associated serotype 4b strains. Ph.D. Thesis, North Carolina State University.
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Progress 09/01/07 to 08/31/08
Outputs
OUTPUTS: We have characterized a library of strains from the turkey processing plant environment in regard to their resistance to disinfectant and to heavy metals (cadmium arsenic), as well as in regard to their molecular fingerprints. Bioinformatics analyses were performed to determine prevalence of these systems in the chromosome or in mobile elements (plasmids) of Listeria. We investigated stability of cadmium resistance and disinfectant resistance phenotypes (and underlying genetic determinants) in several genetically distinct strains from the processing plant environments, as well as in strains from specific outbreaks of listeriosis. We have analyzed the strains from the turkey processing plants in terms of the prevalence of mutated internalin A genes, which harbor premature stop codons. The impact of internalin A premature stop codon mutations in environmental fitness of Listeria (especially in regard to survival and growth in raw and pasteurized milk) was assessed. The resistance of strains form the processing plant environments to Listeria specific phages was also determined. Phages were isolated from environmental samples derived from the turkey processing plants, and screened in terms of their ability to infect and kill Listeria strains from these environments. Strains from major outbreaks were extensively characterized in terms of their susceptibility to phage, to determine the suitability of phage as possible biocontrol for such strains. The genetic mechanisms underlying resistance to phage among strains from major outbreaks were investigated. The impact of growth conditions on freeze thawing tolerance of Listeria was also investigated. We genetically characterized two genomic regions that appears to undergo marked divergence in L. monocytogenes, and that harbor unique sequences in strains from different epidemic clones. We assessed the potential of specific sequences for accurate epidemic clone detection and monitoring. PARTICIPANTS: The project provided numerous opportunities for training in bacteriology, bacterial genetics and physiology, subtyping and determinations of susceptibility to antimicrobials, disinfectant, and heavy metals for five graduate students (Cheng Ying, Savitri Mullapudi, Sangmi Lee, Reha Azizoglu, Sheea White); one postdoctoral scientist (Driss Elhanafi); two undergraduate research interns (Simone Wilson, Jach Byrd); nine collaborating scientists (Nan Faith and Chuck Czuprynski, University of Wisconsin; Nattawan Promadej, university of Hawaii, currently at the Centers for Disease Control and Prevention; Q. Zhang and J. Luchansky, USDA-ARS; Brien Nudeck, University of Tennessee; Kate Sperry, Leslie Wolf and Justin Edwards, North Carolina Department of Health, Raleigh, NC); one visiting scientist (Natalia Markelova, Moscow State university, Russia). In addition, the laboratory manager, Robin Siletzky and the PI Sophia Kathariou participated in the project. TARGET AUDIENCES: Target audiences for the research project and findings thereof include individuals associated with food industry (especially managers of food processing plants) who will be interested in knowing the prevalence of disinfectant and phage resistance among Listeria strains from the environment of the processing plants. A second target audience would include individuals from regulatory agencies, e.g. agencies approving and monitoring use of phage for Listeria biocontrol and regulatory agencies involved in the formulation of improved risk assessments for Listeria in the food supply; accurate data on prevalence of potentially attenuated strains in the processing plants will be needed for improved risk assessments. A third target audience would include members of the scientific community, who would be interested in the population structure and genomic attributes of the organisms, the implications of the findings for the pathogens' evolution and environmental adaptations, the genetic basis for epidemic clone emergence and niche adaptation, and horizontal gene transfer of resistance determinants in Listeria. A fourth target audience would be members of the food safety community, who would be interested in multiple aspects of the findings related to the adaptations of the pathogens and their survival in the processing plants and in specific commodities; Listeria continues to be associated with significant disease burden in the United States and to pose serious economic threats to the ready to eat food industry. PROJECT MODIFICATIONS: Nothing significant to report during this reporting period.
Impacts
Our bioinformatics analysis revealed three different cadmium resistance gene cassettes in Listeria. We succeeded in identifying genes responsible for resistance to the quaternary ammonium disinfectant benzalkonium chloride (BC) on the large plasmid harbored by certain strains. The prototype for this plasmid is pLM80, identified during the genome sequencing of a strain implicated in the 1998-99 outbreak of listeriosis traced to contaminated hot dogs. Analysis of disinfectant resistance among Listeria strains from the environment of turkey processing plants revealed that all strains resistant to BC were also resistant to the heavy metal cadmium. A novel finding was that strains resistant both to BC and to cadmium had a higher likelihood of harboring one specific cadmium resistance cassette than strains which were only resistant to cadmium, but susceptible to BC. Serial passages of the strains under conditions that would lead to plasmid curing suggested that the resistance determinants were unusually stable in the majority of the environmental strains. However, loss of cadmium and BC resistance following such passages provided evidence of plasmid harborage. A number of the strains from the processing plants harbored internalin A genes with premature stop codons. Sequence analysis provided accurate information of the prevalence of the different stop cordon mutations among these strains, and identified several novel mutations, including in serotype 4b bacteria which previously were never reported to harbor such mutations. Comparative fitness studies assessed survival and growth of strains harboring such mutations in laboratory media and in raw as well as pasteurized milk. A high proportion of strains of serotype 1/2a and 1/2b were found resistant to wide host range phages isolated from the processing plants, as well as to other tested wide host ranges. In contrast, strains of serotype 4b were largely phage susceptible. Strains from one of the major epidemic clones were uniformly resistant to the phages under certain growth conditions, suggesting that resistance would be likely in the environment of the processing plants and in foods. These findings raise suggest great caution in possible uses of phage as biocontrol: such use might eliminate other strains, while leaving problematic epidemic strains unharmed. The genetic basis of phage resistance among the epidemic strains was investigated, and a novel gene cassette was identified using transposon mutagenesis. Analysis of freeze thawing tolerance following growth under different conditions revealed that cryotolerance was significantly enhanced following growth at 37C, a temperature that also permits virulence gene expression in Listeria. Genetic analysis of two regions that have unique genetic content in strains from major epidemic clones revealed possible roles of the genes in survival under specific stress conditions (e.g. low temperature and high salt; high temperature and nutrient depletion). DNA macroarray analyses identified sequences that can be used for unambiguous detection of epidemic clone II strains from clinical and environmental sources.
Publications
- Cheng, Y., Siletzky, R. M., and Kathariou, S. 2008. Genomic divisions / lineages, epidemic clones and population structure of Listeria monocytogenes. Handbook of Listeria monocytogenes. Dongyou Liu ( Ed), Taylor & Francis Group, Inc.
- Faith, N., Kathariou, S., Cheng, Y., Promadej, N., Neudeck, B. L. , Zhang, Q., Luchansky, J., Czuprynski, C. (2008). The role of L. monocytogenes serotype 4b gtcA in gastrointestinal listeriosis in A/J mice. Foodborne Pathog Dis. Nov 9. [Epub ahead of print]
- Kim, J. W., Siletzky, R. M., Kathariou, S. (2008). Host ranges of Listeria-specific bacteriophages from the turkey processing plant environment in the United States. Appl Environ Microbiol. 74:6623-30.
- Sperry, K. E. , Kathariou, S., Edwards J. S. , and Wolf, L. A. (2008). Multiple-locus variable-number tandem-repeat analysis as a tool for subtyping Listeria monocytogenes strains. J. Clin. Microbiol. 46:1435-1450.
- Mullapudi, S., Siletzky, R. M., and Kathariou, S. (2008). Heavy metal and benzalkonium chloride resistance of Listeria monocytogenes from the environment of turkey processing plants. Appl. Environ. Microbiol. 74:1464-1468.
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Progress 09/01/06 to 08/31/07
Outputs
OUTPUTS: The objectives of this project were to compare genome content between 1998-99 and 2002 outbreak strains and isolates with ECII genetic markers obtained from two different processing plants; to further investigate the impact of temperature on resistance of ECII bacteria to listeriaphage from the processing plant environment, and to elucidate the underlying mechanism; to determine possible impact of temperature on resistance of ECII bacteria to disinfectants and on formation of biofilms; and to characterize stability and self-mobilization of the ECII plasmid pLM80, and to determine the possible role of this plasmid and selected plasmid-borne genes in resistance to disinfectants and biofilm formation. We have provided conclusive evidence that the 1998-99 and the 2002 outbreak strains were members of the same clonal group. In addition, we identified and characterized intriguing differences, localized on the large plasmids harbored by strains from the two outbreaks. We identified
and validated a novel probe (chromosomal locus) that appears to be highly discriminatory for identification of ECII strains. We confirmed that all ECII strains, regardless of source, demonstrate the unusual temperature-dependent resistance to listeriaphage from the processing plant environment. We have also partially characterize these phages, and found that they are highly similar to P100 (GRAS status listeriaphage). To characterize the genetic mechanism underlying the observed resistance to phage, we constructed and screened mutant libraries of Tn916E, Tn917, and, mariner transposon. Two mutants were identified (one Tn916E, one mariner), and are being characterized. We have identifying a novel gene cassette mediating resistance to BC. We have confirmed the location of this cassette, and a cassette mediating resistance to cadmium, on large plasmids. Plasmid mobilizations, curing, and biofilm assays are continuing.
PARTICIPANTS: Individuals who worked on this project included three graduate and two undergraduate students, one postdoctoral scientist, and our laboratory manager. The project included collaborations with the Centers for Disease Control and Prevention, the North Carolina Department of Health, and USDA-ARS. It also involved collaborations with scientists from several universities, including Ohio State University, the University of Wisconsin, University of Tennessee, Michigan State University, and Virginia Tech. The project provided opportunities for academic and research training essential for the three students pursuing their Ph.D. (two students), as well as for the postdoctoral scientist and the undergraduate students.
TARGET AUDIENCES: Our target audiences are: The Public Health and Food Safety sector, specifically stakeholders involved in the monitoring and prevention of human illness due to Listeria, and in reduction of this pathogen's burden in foods, especially those that are highly processed, ready to eat, cold-stored food commodities. The food processing industry, especially those sectors dedicated to production of foods that are at risk for Listeria contamination. Consumers groups, who need information on food safety issues associated with specific commodities for which Listeria contamination may pose special risks, such as contaminated soft cheeses, hot dogs, deli meats, and other highly processed specialty products.
Impacts
Listeria continues to be troublesome pathogen, due to its high case fatality rate, its ability to colonize the environment of food processing plants, often persisting there for several years, and its ability to grow in the cold. In the course of the project we have discovered that the disease burden of ECII strains (apparently sporadic cases) has increased in years subsequent to the 2002 outbreak. Prompt identification and effective monitoring of these troublesome strains will contribute to prevention of outbreaks and reduction of disease burden. Our findings related to listeriaphage resistance and disinfectant resistance will be valuable for understanding of the ecology of these organisms, and for their reductions and control in the processing plant environment.
Publications
- Cheng, Y., N. Promadej, J.-W. Kim, and S. Kathariou. 2008. Teichoic acid glycosylation mediated by gtcA is required for phage adsorption and susceptibility of Listeria monocytogenes serotype 4b. Accepted, Appl. Environ. Microbiol.
- Cheng, Y., L. Yue, D. Elhanafi, and S. Kathariou. 2007. Absence of serotype-specific surface antigen in laboratory variants of epidemic-associated Listeria monocytogenes strains. Appl. Environ. Microbiol. 6313-6.Aug 3; [Epub ahead of print]
- Bazaco, M. C., J. D. Eifert, R. C. Williams, and S. Kathariou. 2007. Quantitative recovery of Listeria monocytogenes and select salmonella serotypes from environmental sample media. J AOAC Int. 90:250-257.
- Faith, N. G., S. Kathariou, B. L. Neudeck, J. B. Luchansky, and C. J. Czuprynski. 2007. A P60 mutant of Listeria monocytogenes is impaired in its ability to cause infection in intragastrically inoculated mice. Microbial Pathog. 42:237-241.
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