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Ecological and genetic mechanisms of development of epidemiologically significant strains of sapronosis causative agents

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Abstract

Sapronosis is an infectious disease caused by pathogenic microorganisms that are natural inhabitants of soil and/or aquatic ecosystems. They are capable of exiting in the environment outside of the host for a long time. Causative agents of sapronosis are polypathogenic, i.e., they cause infections in a wide range of hosts. The aim of the work was to establish a place in the clonal species structure for Listeria monocytogenes and Yersinia pseudotuberculosis isolated from both patients in hospitals and wild rodents and hydrobionts in natural foci. A total of 42 L. monocytogenes and 29 Y. pseudotuberculosis isolates were studied. 17 L. monocy-togenes and 29 Y. pseudotuberculosis isolates were obtained from patients; 25 L. monocytogenes isolates were obtained from wild animals and soil. The isolates were characterized using Multilocus Sequence Typing (MLST). Previously published MLST schemes were applied, including an analysis of the sequences of internal regions of seven marker genes for general metabolism. All Y. pseudotuberculosis isolates were shown to belong to the clonal complex occurred in the Russian Far East, Japan, and China, while L. monocytogenes isolates were referred to several clonal complexes, some of which have a worldwide distribution. The genetic similarity between L. monocytogenes isolates that cause invasive infections in wild animals in natural listeriosis foci and isolates related to listeriosis outbreaks has been demonstrated. These results suggested that high virulence could be a selective trait that enables the efficient reproduction of sapronosis causative agents in natural ecosystems. The variability of virulence factors of L. monocytogenes isolated from the same natural focus and related to MLST type was indicated. A hypothesis has been suggested that links the polyhostality of sapronosis causative agents and the genetic variability in virulence factors. Based on this hypothesis, a correlation has been suggested between the sequences of virulence factors and the source of isolation. A model of the formation of epidemiologically significant strains of the causative agents in natural foci of sapronosis was constructed.

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References

  • Adgamov, R., Timchenko, N., Allenov, A., and Ermolaeva, S., Variability of inv Gene Fragment Encoding Functionally Important Domain of Invasion of Yersinia pseudotuberculosis, Mol. Gen. Mikrobiol. Virusol., 2010, vol. 25, no. 1, pp. 18–24.

    Article  Google Scholar 

  • Belyakov, V., Golubev, D., Kaminskii, G., and Tets, V., Samoregulyatsiya parazitarnykh sistem. Molekulyarnogeneticheskie mekhanizmy (Self-Regulation of Parasitic Systems. Molecular-Genetic Mechanisms), Moscow: Meditsina, 1987.

    Google Scholar 

  • Bibb, W.F., Gellin, B.G., Weaver, R., Schwartz, B., Plikaytis, B.D., Reeves, M.W., Pinner, R.W., and Broome, C.V., Analysis of Clinical and Food-Borne Isolates of Listeria monocytogenes in the United States by Multilocus Enzyme Electrophoresis and Application of the Method to Epidemiologic Investigations, Appl. Environ. Microbiol., 1990, vol. 56, no. 7, pp. 2133–2141.

    PubMed  CAS  Google Scholar 

  • Bierne, H., Sabet, C., Personnic, N., and Cossart, P., Internalins: A Complex Family of Leucine-Rich Repeat-Containing Proteins in Listeria monocytogenes, Microbes Infect., 2007, vol. 9, no. 10, pp. 1156–1166.

    Article  PubMed  CAS  Google Scholar 

  • Bonazzi, M., Lecuit, M., and Cossart, P., Listeria monocytogenes Internalin and E-Cadherin: From Structure to Pathogenesis, Cell. Microbiol., 2009, vol. 11, no. 5, pp. 693–702.

    Article  PubMed  CAS  Google Scholar 

  • Bueno, V.F., Banerjee, P., Banada, P.P., Jose de Mesquita, A., Lemes-Marques, E.G., and Bhunia, A.K., Characterization of Listeria monocytogenes Isolates of Food and Human Origins from Brazil Using Molecular Typing Procedures and in vitro Cell Culture Assays, Int. J. Environ. Health Res., 2010, vol. 20, no. 1, pp. 43–59.

    Article  PubMed  CAS  Google Scholar 

  • Chen, J., Zhang, X., Mei, L., Jiang, L., and Fang, W., Prevalence of Listeria in Chinese Food Products from 13 Provinces between 2000 and 2007 and Virulence Characterization of Listeria monocytogenes Isolates, Foodborne Pathog. Dis., 2009, vol. 6, no. 1, pp. 7–12.

    Article  PubMed  Google Scholar 

  • Chenal-Francisque, V., Lopez, J., Cantinelli, T., Caro, V., Tran, C., Leclercq, A., Lecuit, M., and Brisse, S., Worldwide Distribution of Major Clones of Listeria monocytogenes, Emerg. Infect. Dis., 2011, vol. 17, no. 6, pp. 1110–1112.

    Article  PubMed  Google Scholar 

  • Chesnokova, M., Klimov, V., Ivanova, L., and Popov, A., Epidemiologicheskie aspekty psevdotuberkuleza v Rossii: iersinii i iersiniozy (Epidemiological Aspects of Pseudotuberculosis in Russia: Yersinias and Yersinioses), Tseneva, G., Ed., St. Petersburg, 2006.

  • Disson, O., Grayo, S., Huillet, E., Nikitas, G., LangaVives, F., Dussurget, O., Ragon, M., Le Monnier, A., Babinet, C., Cossart, P., and Lecuit, M., Conjugated Action of Two Species-Specific Invasion Proteins for Fetoplacental Listeriosis, Nature, 2008, vol. 455, no. 7216, pp. 1114–1118.

    Article  PubMed  CAS  Google Scholar 

  • Entecost, M., Otto, G., Theriot, J.A., and Amieva, M.R., Listeria monocytogenes Invades the Epithelial Junctions at Sites of Cell Extrusion, PLoS Pathog., 2006, vol. 2, no. 1, pp. 0029–0040.

    Google Scholar 

  • Eppinger, M., Rosovitz, M.J., Fricke, W.F., Rasko, D.A., Kokorina, G., Fayolle, C., Lindler, L.E., Carniel, E., and Ravel, J., The Complete Genome Sequence of Yersinia pseudotuberculosis Ip31758, the Causative Agent of Far-Eastern Scarlet-Like Fever, PLoS Genet., 2007, vol. 3, no. 8, pp. 1508–1523.

    Article  CAS  Google Scholar 

  • Ermolaeva, S., Litvin, V., and Pushkareva, V., Modern Development of Ideas of N.F. Gamaleya in Studying the Causative Agents of Sapronosis, in Sb. nauchnykh trudov NIIEM im. N.F. Gamalei RAMN (Collected Scientific Papers of the Gamaleya Research Institute of Epidemiology and Microbiology), Ginzburg, A.L., Ed., Moscow: OOO Dizain-studiya A4, 2009.

    Google Scholar 

  • Fox, E., O’Mahony, T., Clancy, M., Dempsey, R., O’Brien, M., and Jordan, K., Listeria monocytogenes in the Irish Dairy Farm Environment, J. Food Prot., 2009, vol. 72, no. 7, pp. 1450–1456.

    PubMed  Google Scholar 

  • Franciosa, G., Maugliani, A., Floridi, F., and Aureli, P., Molecular and Experimental Virulence of Listeria monocytogenes Strains Isolated from Cases with Invasive Listeriosis and Febrile Gastroenteritis, FEMS Immunol. Med. Microbiol., 2005, vol. 43, no. 3, pp. 431–439.

    Article  PubMed  CAS  Google Scholar 

  • Gintsburg, A., Shubin, F., Shovadaeva, G., Kulichenko, A., Yanishevskii, N., and Smirnov, G., A New Character of Pathogenicity Encoded by the pvm82 Plasmid of Yersinia pseudotuberculosis, Genetika, 1988, vol. 24, no. 9, pp. 1562–1571.

    PubMed  CAS  Google Scholar 

  • Grassl, G.A., Bohn, E., Muller, Y., Buhler, O.T., and Autenrieth, I.B., Interaction of Yersinia enterocolitica with Epithelial Cells: Invasin beyond Invasion, Int. J. Med. Microbiol., 2003, vol. 293, no. 1, pp. 41–54.

    Article  PubMed  CAS  Google Scholar 

  • Grif, K., Heller, I., Wagner, M., Dierich, M., and Wurzner, R., A Comparison of Listeria monocytogenes Serovar 4b Isolates of Clinical and Food Origin in Austria by Automated Ribotyping and Pulsed-Field Gel Electrophoresis, Foodborne Pathog. Dis., 2006, vol. 3, no. 1, pp. 138–141.

    Article  PubMed  CAS  Google Scholar 

  • Grunin, I., Somov, G., and Zalmover, I., Far-East Scarlet-Like Fever, Voen.-Med. Zh., 1960, vol. 8, no. 2, pp. 62–65.

    PubMed  CAS  Google Scholar 

  • Hamzaoui, N., Kerneis, S., Caliot, E., and Pringault, E., Expression and Distribution of Beta1 Integrins in in vitro-Induced M Cells: Implications for Yersinia Adhesion to Peyer’a Patch Epithelium, Cell. Microbiol., 2004, vol. 6, no. 9, p. 817.

    Google Scholar 

  • He, J., Baldini, R.L., Deziel, E., Saucier, M., Zhang, Q., Liberati, N.T., Lee, D., Urbach, J., Goodman, H.M., and Rahme, L.G., The Broad Host Range Pathogen Pseudomonas aeruginosa Strain Pa14 Carries Two Pathogenicity Islands Harboring Plant and Animal Virulence Genes, Proc. Natl. Acad. Sci. USA, 2004, vol. 101, no. 8, pp. 2530–2535.

    Article  PubMed  CAS  Google Scholar 

  • Herd, M. and Kocks, C., Gene Fragments Distinguishing an Epidemic-Associated Strain from a Virulent Prototype Strain of Listeria monocytogenes Belong to a Distinct Functional Subset of Genes and Partially Crosshybridize with Other Listeria Species, Infect. Immun., 2001, vol. 69, no. 6, pp. 3972–3979.

    Article  PubMed  CAS  Google Scholar 

  • Ildirum, S., Lin, W., Hitchins, A.D., Jaykus, L., Altermann, E., Klaenhammer, T.R., and Kathariou, S., Epidemic Clone i-Specific Genetic Markers in Strains of Listeria monocytogenes Serotype 4b from Foods, Appl. Environ. Microbiol., 2004, vol. 70, no. 7, pp. 4158–4164.

    Article  Google Scholar 

  • Kalekar, S., Rodrigues, J., D’Costa, D., Doijad S., Ashok Kumar, J., Malik, S.V.S., Kalorey, D.R., Rawool, D.B., Hain, T., Chakraborty, T., and Barbuddhe, S.B., Genotypic Characterization of Listeria monocytogenes Isolated from Humans in India, Ann. Trop. Med. Parasitol., 2011, vol. 105, no. 5, pp. 351–358.

    Article  PubMed  CAS  Google Scholar 

  • Karpova, T., Firsova, T., Rodina, L., Tartakovskii, I., and Ermolaeva, S., Typing of Listeria monocytogenes Based on the Polymorphism of Genes Encoding the Pathogenicity Factors, Klin. Mikr. Antimikr. Khim., 2003, vol. 5, no. 3, pp. 251–258.

    Google Scholar 

  • Kathariou, S., Listeria monocytogenes Virulence and Pathogenicity, a Food Safety Perspective, J. Food Prot., 2002, vol. 65, no. 11, pp. 1811–1829.

    PubMed  Google Scholar 

  • Khelef, N., Lecuit, M., Bierne, H., and Cossart, P., Species Specificity of the Listeria monocytogenes InlB Protein, Cell. Microbiol., 2006, vol. 8, no. 3, pp. 457–470.

    Article  PubMed  CAS  Google Scholar 

  • Kiss, R., Tirczka, T., Szita, G., Bernath, S., and Csiko, G., Listeria monocytogenes Food Monitoring Data and Incidence of Human Listeriosis in Hungary, 2004, Int. J. Food Microbiol., 2006, vol. 112, no. 1, pp. 71–74.

    Article  PubMed  Google Scholar 

  • Korenberg, E., The Origin of Pathogens of Natural Focal Diseases, Priroda (Moscow, Russ. Fed.), 2006, no. 10, pp. 33–40.

    Google Scholar 

  • Lecuit, M., Dramsi, S., Gottardi, C., Fedor-Chaiken, M., Gumbiner, B., and Cossart, P., A Single Amino Acid in E-Cadherin Responsible for Host Specificity towards the Human Pathogen Listeria monocytogenes, EMBO J., 1999, vol. 18, no. 14, pp. 3956–3963.

    Article  PubMed  CAS  Google Scholar 

  • Litvin, V., Saprophytic Phase in the Ecology of Causative Agents of Infectious Diseases, Zh. Mikrobiol. Epidemiol. Immunobiol., 1985, no. 1, pp. 98–103.

    Google Scholar 

  • Litvin, V., Random Parasitism of Microorganisms, Zh. Mikrobiol. Epidemiol. Immunobiol., 1992, no. 1, pp. 52–55.

    Google Scholar 

  • Litvin, V., Gintsburg, A., Pushkareva, V., Romanova, Yu., and Boev, B., Epidemiologicheskie aspekty ekologii bakterii (Epidemiological Aspects of Bacterial Ecology), Prozorovskii, S., Ed., Moscow: Farmarus-Print, 1997.

  • Lomonaco, S., Chen, Y., and Knabel, S.J., Analysis of Additional Virulence Genes and Virulence Gene Regions in Listeria monocytogenes Confirms the Epidemiologic Relevance of Multi-Virulence-Locus Sequence Typing, J. Food Prot., 2008, vol. 71, no. 12, pp. 2559–2566.

    PubMed  CAS  Google Scholar 

  • Maiden, M.C.J., Multilocus Sequence Typing of Bacteria, Annu. Rev. Microbiol., 2006, vol. 60, pp. 561–588.

    Article  PubMed  CAS  Google Scholar 

  • Marino, M., Braun, L., Cossart, P., and Ghosh, P., A Framework for Interpreting the Leucine-Rich Repeats of the Listeria internalins, Proc. Natl. Acad. Sci. USA, 2000, vol. 97, no. 16, pp. 8784–8788.

    Article  PubMed  CAS  Google Scholar 

  • McLauchlin, J., Distribution of Serovars of Listeria monocytogenes Isolated from Different Categories of Patients with Listeriosis, Eur. J. Clin. Microbiol. Infect. Dis., 1990, vol. 9, no. 3, pp. 210–213.

    Article  PubMed  CAS  Google Scholar 

  • Mead, P.S., Dunne, E.F., Graves, L., Wiedmann, M., Patrick, M., Hunter, S., Salehi, E., Mostashari, F., Craig, A., Mshar, P., Bannerman, T., Sauders, B.D., Hayes, P., Dewitt, W., Sparling, P., Griffin, P., Morse, D., Slutsker, L., and Swaminathan, B., Nationwide Outbreak of Listeriosis due to Contaminated Meat, Epidemiol. Infect., 2006, vol. 134, no. 4, pp. 744–752.

    Article  PubMed  CAS  Google Scholar 

  • Meinersmann, R.J., Phillips, R.W., Wiedmann, M., and Berrang, M.E., Multilocus Sequence Typing of Listeria monocytogenes by Use of Hypervariable Genes Reveals Clonal and Recombination Histories of Three Lineages, Appl. Environ. Microbiol., 2004, vol. 70, no. 4, pp. 2193–2203.

    Article  PubMed  CAS  Google Scholar 

  • Nelson, K.E., Fouts, D.E., Mongodin, E.F., Ravel, J., DeBoy, R.T., Kolonay, J.F., Rasko, D.A., Angiuoli, S.V., Gill, S.R., Paulsen, I.T., Peterson, J., White, O., Nelson, W.C., Nierman, W., Beanan, M.J., Brinkac, L.M., Daugherty, S.C., Dodson, R.J., Durkin, A.S., Madupu, R., Haft, D.H., Selengut, J., Van Aken, S., Khouri, H., Fedorova, N., Forberger, H., Tran, B., Kathariou, S., Wonderling, L.D., Uhlich, G.A., Bayles, D.O., Luchansky, J.B., and Fraser, C.M., Whole Genome Comparisons of Serotype 4b and 1/2a Strains of the Food-Borne Pathogen Listeria monocytogenes Reveal New Insights into the Core Genome Components of This Species, Nucleic Acid Res., 2004, vol. 32, no. 8, pp. 2386–2395.

    Article  PubMed  CAS  Google Scholar 

  • Oliver, S.P., Jayarao, B.M., and Almeida, R.A., Food-Borne Pathogens in Milk and the Dairy Farm Environment: Food Safety and Public Health Implications, Food-Borne Pathog. Dis., 2005, vol. 2, no. 2, pp. 115–129.

    Article  CAS  Google Scholar 

  • Ostrovskaya, O., Zaitseva, E., Pukhovskaya, N., Ivakhnishina, N., Musatov, I., Nagovitsyna, E., Vlasova, M., and Ivanov, L., Listeria Monocytogenes in Spontaneous Miscarriage and Perinatal Mortality, Dal’nevost. Med. Zh., 2011, no. 3, pp. 38–43.

    Google Scholar 

  • Pizarro-Cerdá, J. and Cossart, P., Subversion of Cellular Functions by Listeria monocytogenes, J. Pathol., 2006, vol. 208, no. 2, pp. 215–223.

    Article  PubMed  Google Scholar 

  • Platonov, A., Shipulin, G., and Platonova, O., Multilocus Sequence Typing: A New Method and the First Results in the Genotyping of Bacteria, Russ. J. Genet., 2000, vol. 36, no. 5, pp. 481–487.

    CAS  Google Scholar 

  • Pushkareva, V., Litvin, V., and Troitskaya, V., Listeria in Plants: An Experimental Study of Colonization, Abundance, and Variability, Zh. Mikrobiol. Epidemiol. Immunobiol., 1996, no. 5, pp. 10–12.

    Google Scholar 

  • Pushkareva, V., Litvin, V., and Ermolaeva, S., Pathogenic Listeria and Soil Protozoa: Coupling of Life Cycles, Usp. Sovrem. Biol., 2008, vol. 128, no. 2, pp. 8–15.

    Google Scholar 

  • Pushkareva, V.I. and Ermolaeva, S.A., Listeria monocytogenes Virulence Factor Listeriolysin O Favors Bacterial Growth in Co-Culture with the Ciliate Tetrahymena pyriformis, Causes Protozoan Encystment and Promotes Bacterial Survival Inside Cysts, BMC Microbiol., 2010, vol. 10, no. 1, pp. 26–37.

    Article  PubMed  Google Scholar 

  • Ragon, M., Wirth, T., Hollandt, F., Lavenir, R., Lecuit, M., Le Monnier, A., and Brisse, S., A New Perspective on Listeria monocytogenes Evolution, PLoS Pathog., 2008, vol. 4, no. 9, p. e10001461.

    Google Scholar 

  • Salcedo, C., Arreaza, L., Alcalá, B., de la Fuente, L., and Vázquez, J.A., Development of a Multilocus Sequence Typing Method for Analysis of Listeria monocytogenes Clones, J. Clin. Microbiol., 2003, vol. 41, no. 2, pp. 757–762.

    Article  PubMed  CAS  Google Scholar 

  • Shubin, F., The Epidemiological Aspects of a Pseudotuberculosis Polyclonal Infection, Zh. Mikrobiol. Epidemiol. Immunobiol., 1997, no. 5, pp. 22–25.

    Google Scholar 

  • Somov, G., Dal’nevostochnaya skarlatinopodobnaya likhoradka (Far-Eastern Scarlet-Like Fever), Moscow: Meditsina, 1979.

    Google Scholar 

  • Somov, G. and Buzoleva, L., Adaptatsiya patogennykh bakterii k abioticheskim faktoram okruzhayushchei sredy (Adaptation of Pathogenic Bacteria to the Abiotic Environmental Factors), Vladivostok: OAO Poligrafkombinat, 2004.

    Google Scholar 

  • Somov, G. and Litvin, V., Saprofitizm i parazitizm patogennykh bakterii (Saprofitizm and Parasitism of Pathogenic Bacteria), Novosibirsk: Nauka, 1988.

    Google Scholar 

  • Somov, G. and Rozhkova, L., Anthropogenic Transformation of Natural Foci of Pseudotuberculosis, Byull. Sib. Otd. Akad. Med. Nauk, 1983, no. 2, pp. 7–12.

    Google Scholar 

  • Somov, G., Varvashevich, T., and Timchenko, N., Psikhrofil’nost’ patogennykh bakterii (Psychrophilicity of Pathogenic Bacteria), Novosibirsk: Nauka, 1991.

    Google Scholar 

  • Spiik, A.K., Meijer, L.K., Ridderstad, A., and Pettersson, S., Interference of Eukaryotic Signalling Pathways by the Bacteria Yersinia Outer Protein YopJ, Immunol. Lett., 1999, vol. 68, nos. 2–3, pp. 199–203.

    Article  PubMed  CAS  Google Scholar 

  • Takeuchi, K., Mytle, N., Lambert, S., Coleman, M., Doyle, M.P., and Smith, M.A., Comparison of Listeria monocytogenes Virulence in a Mouse Model, J. Food Prot., 2006, vol. 69, no. 4, pp. 842–846.

    PubMed  Google Scholar 

  • Tan, M.W., Mahajan-Miklos, S., and Ausubel, F.M., Killing of Caenorhabditis elegans by Pseudomonas aeruginosa Used to Model Mammalian Bacterial Pathogenesis, Proc. Natl. Acad. Sci. USA, 1999, vol. 96, no. 2, pp. 715–720.

    Article  PubMed  CAS  Google Scholar 

  • Tartakovskii, I., Maleev, V., and Ermolaeva, S., Listerii: rol’ v infektsionnoi patologii cheloveka i laboratornaya diagnostika (Listeria: The Role in Infectious Human Pathology and Laboratory Diagnostics), Moscow: Meditsina dlya vsekh, 2002.

    Google Scholar 

  • Terskikh, V., Sapronosis (on the Diseases of Humans and Animals Caused by Microbes Capable of Reproducing in the Environment, which Is a Habitat for Them), Zh. Mikrobiol. Epidemiol. Immunobiol., 1958, vol. 29, no. 8, pp. 118–122.

    PubMed  CAS  Google Scholar 

  • Timchenko, N.F., Yersinia pseudotuberculosis Toxins, Zh. Mikrobiol. Epidemiol. Immunobiol., 2006, no. 6, pp. 83–89.

    Google Scholar 

  • Vazquez-Boland, J.A., Kuhn, M., Berche, P., Chakraborty, T., Dominguez-Bernal, G., Goebel, W., Gonzalez-Zorn, B., Wehland, J., and Kreft, J., Listeria Pathogenesis and Molecular Virulence Determinants, Clin. Microbiol. Rev., 2001, vol. 14, no. 3, pp. 584–640.

    Article  PubMed  CAS  Google Scholar 

  • Vitas, A.I. and Garcia-Jalon, V.A.E.I., Occurrence of Listeria monocytogenes in Fresh and Processed Foods in Navarra (Spain), Int. J. Food Microbiol., 2004, vol. 90, no. 3, pp. 349–356.

    Article  PubMed  CAS  Google Scholar 

  • Ward, T.J., Usgaard, T., and Evans, P., A Targeted Multilocus Genotyping Assay for Lineage, Serogroup, and Epidemic Clone Typing of Listeria monocytogenes, Appl. Environ. Microbiol., 2010, vol. 76, no. 19, pp. 6680–6684.

    Article  PubMed  CAS  Google Scholar 

  • Weis, J. and Seeliger, H.P., Incidence of Listeria monocytogenes in Nature, Appl. Microbiol., 1975, vol. 30, no. 1, pp. 29–32.

    PubMed  CAS  Google Scholar 

  • Welshimer, H.J. and Donker-Voet, J., Listeria monocytogenes in Nature, Appl. Microbiol., 1971, vol. 21, no. 3, pp. 516–519.

    PubMed  CAS  Google Scholar 

  • Wiedmann, M., Bruce, J.L., Keating, C., Johnson, A.E., McDonough, P.L., and Batt, C.A., Ribotypes and Virulence Gene Polymorphisms Suggest Three Distinct Listeria monocytogenes Lineages with Differences in Pathogenic Potential, Infect. Immun., 1997, vol. 65, no. 7, pp. 2707–2716.

    PubMed  CAS  Google Scholar 

  • Yushchuk, N., Tseneva, G., Karetkina, G., and Brodov, L., Iersiniozy (Yersinioses), Moscow: Meditsina, 2003.

    Google Scholar 

  • Zaitseva, E. and Somov, G., Microbiological Characterization of Listeria monocytogenes Isolated from Various Biotic and Abiotic Objects in Primorsky Krai, Zh. Mikrobiol. Epidemiol. Immunobiol., 2006, no. 2, pp. 3–6.

    Google Scholar 

  • Zaitseva, E., Pukhovskaya, N., Musatov, Yu., Ivanov, L., Ermolaeva, S., and Somov, G., Molecular-Genetic Characteristics and Epidemiological Significance of Listeria monocytogenes Strains Isolated from Pregnant Women and from Abortion Material in the Russian Far East, Klin. Mikrobiol. Antimikrob. Khimioter., 2007, vol. 9, no. 1, pp. 81–89.

    Google Scholar 

  • Zaytseva, E., Ermolaeva, S., and Somov, G.P., Low Genetic Diversity and Epidemiological Significance of Listeria monocytogenes Isolated from Wild Animals in the Far East of Russia, Infect. Genet. Evol., 2007, vol. 7, no. 6, pp. 736–742.

    Article  PubMed  CAS  Google Scholar 

  • Zaitseva, E., Ermolaeva, S., Pukhovskaya, N., Musatov, Yu., Ivanov, L., and Somov, G., Distribution of Listeria monocytogenes and Its Role in Infectious Diseases in the Far East of Russia, Tikhookean. Med. Zh., 2010, no. 4, pp. 19–24.

    Google Scholar 

  • Zhang, S., Zhang, Z., Liu, S., Bingham, W., and Wilson, F., Fatal Yersiniosis in Farmed Deer Caused by Yersinia pseudotuberculosis Serotype O:3 Encoding a Mannosyltransferase-Like Protein Wbyk, J. Vet. Diagn. Invest., 2008, vol. 20, no. 3, pp. 356–359.

    Article  PubMed  Google Scholar 

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Authors and Affiliations

  1. Gamalei Research Institute of Epidemiology and Microbiology, Moscow, Russia

    R. R. Adgamov, V. I. Pushkareva & S. A. Ermolaeva

  2. Research Institute of Epidemiology and Microbiology, Far Eastern Branch, Russian Academy of Medical Sciences, Vladivostok, Russia

    N. F. Timchenko & E. A. Zaitseva

  3. Russian Research Institute of Veterinary Virology and Microbiology, Russian Academy of Agricultural Sciences, Pokrov, Russia

    D. V. Kolbasov & I. Yu. Egorova

  4. Khabarovsk Antiplague Station, Russian Agency for Health and Consumer Rights, Khabarovsk, Russia

    N. M. Pukhovskaya, Yu. S. Musatov & L. I. Ivanov

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  1. R. R. Adgamov
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  2. N. F. Timchenko
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  3. E. A. Zaitseva
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  4. V. I. Pushkareva
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  6. I. Yu. Egorova
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  7. N. M. Pukhovskaya
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  8. Yu. S. Musatov
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  9. L. I. Ivanov
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  10. S. A. Ermolaeva
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Correspondence to R. R. Adgamov.

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Original Russian Text © R.R. Adgamov, N.F. Timchenko, E.A. Zaitseva, V.I. Pushkareva, D.V. Kolbasov, I.Yu. Egorova, N.M. Pukhovskaya, Yu.S. Musatov, L.I. Ivanov, S.A. Ermolaeva, 2012, published in Uspekhi Sovremennoi Biologii, 2012, Vol. 132, No. 6, pp. 551–567.

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Adgamov, R.R., Timchenko, N.F., Zaitseva, E.A. et al. Ecological and genetic mechanisms of development of epidemiologically significant strains of sapronosis causative agents. Biol Bull Rev 3, 125–138 (2013). https://doi.org/10.1134/S2079086413020023

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