Yersinia enterocolitica and Y. pseudotuberculosis which can cause yersiniosis in humans and animals are thought to be significant food-borne pathogens and be important as hygiene indicator in food safety. The pathogenic Y. enterocolitica serotypes/biotypes are O:3/4 and 3 variant VP negative, O:5, 27/2, O:8/1b, and O:9/2, have been reported worldwide. Y. pseudotuberculosis is distributed less widely than Y. enterocolitica. Isolation methods usually involve selective and recovery enrichment of the food sample followed by plating onto selective media, confirmation of typical colonies and testing for virulence properties of isolated strains. Recently, DNA-based methods, such as PCR assays, have been developed to detect pathogenic Y. enterocolitica and Y. pseudotuberculosis in foods more rapidly, and sensitivity than can be achieved by conventional culture methods. This paper reviews commercially available conventional and PCR-based procedures for the detection of pathogenic Yersinia in food. These methods are effective as the isolation and detection methods to target pathogenic Y. enterocolitica and Y. pseudotuberculosis in foods. 1. Overview Food-borne pathogenic Yersinia (Y. enterocolitica and Y. pseudotuberculosis) is facultative anaerobic, gram-negative Enterobacteriaceae and is isolated frequently from soil, water, animals, and foods [1–4]. Y. enterocolitica causes human infections whose symptoms include diarrhea, terminal ileitis, mesenteric lymphadenitis, arthritis, and septicemia. Y. pseudotuberculosis causes mesenteric lymphadenitis, diarrhea, and septicemia in humans. As a psychrophilic organism, Yersinia is able to grow at 4°C, and cold chain food products could offer a potential food safety hazard [3, 5, 6]. The pathogenic Y. enterocolitica serotypes/biotypes are O:3/4 and 3 variant VP negative, O:5, 27/2, O:8/1b, and O:9/2 have been reported worldwide [7, 8]. In Japan, O:3/3 variant VP negative is the most frequent cause of human yersiniosis [8]. In the United States, despite declining incidences of serotype O:8/1b infections, O:3/4 and O:5, 27/2 infections are on the increase [7]. In Europe, Serotype O:3 and O:9 infections account for over 90% of Y. enterocolitica infections. Y. pseudotuberculosis is distributed less widely than Y. enterocolitica and, although frequently isolated from animals, is rarely isolated from soil, water, and food [9–12]. A large outbreak of Y. pseudotuberculosis infection has been reported in Japan [13, 14]. In the Far East including Japan, Y. pseudotuberculosis various serotypes (1b, 2a, 2b, 2c, 3, 4a, 4b, 5a, 5b,
References
[1]
M. L. Ackers, S. Schoenfeld, J. Markman et al., “An outbreak of s O:8 infections associated with pasteurized milk,” Journal of Infectious Diseases, vol. 181, no. 5, pp. 1834–1837, 2000.
[2]
S. Aleksic, A. G. Steigerwalt, J. Bockemuhl, G. P. Huntley-Carter, and D. J. Brenner, “Yersinia rohdei sp. nov. isolated from human and dog feces and surface water,” International Journal of Systematic Bacteriology, vol. 37, no. 4, pp. 327–332, 1987.
[3]
C. C. G Aulisio, J. T. Stanfield, S. D. Weagant, and W. E. Hill, “Yersiniosis associated with tofu consumption: serological, biochemical and pathogenicity studies of Yersinia enterocolitica isolates,” Journal of Food Protection, vol. 46, pp. 226–230, 1983.
[4]
S. Sharma, P. Sachdeva, and J. S. Virdi, “Emerging water-borne pathogens,” Applied Microbiology and Biotechnology, vol. 61, no. 5-6, pp. 424–428, 2003.
[5]
H. Fukushima, K. Saito, M. Tsubokura, and K. Otsuki, “Yersinia spp. in surface water in Matsue, Japan,” Zentralblatt fur Bakteriologie Mikrobiologie und Hygiene, vol. 179, no. 3, pp. 235–247, 1984.
[6]
D. Grahek-Ogden, B. Schimmer, K. S. Cudjoe, K. Nyg？rd, and G. Kapperud, “Outbreak of Yersinia enterocolitica serogroup O:9 infection and processed pork, Norway,” Emerging Infectious Diseases, vol. 13, no. 5, pp. 754–756, 2007.
[7]
E. J. Bottone, “Yersinia enterocolitica: overview and epidemiologic correlates,” Microbes and Infection, vol. 1, no. 4, pp. 323–333, 1999.
[8]
H. Fukushima, “Yersinia enterocolitica,” in Foodborne Infection and Food Microbiology, H. Nakanishi and T. Maruyama, Eds., pp. 315–334, Chuouhoki-shuppan, Tokyo, Japan, 2009.
[9]
H. Fukushima, “Direct isolation of Yersinia enterocolitica and Yersinia pseudotuberculosis from meat,” Applied and Environmental Microbiology, vol. 50, no. 3, pp. 710–712, 1985.
[10]
H. Fukushima, “Direct isolation of Yersinia pseudotuberculosis from fresh water in Japan,” Applied and Environmental Microbiology, vol. 58, no. 8, pp. 2688–2690, 1992.
[11]
M. Inoue, H. Nakashima, T. Mori, R. Sakazaki, K. Tamura, and M. Tsubokura, “Yersinia pseudotuberculosis infection in the mountain area,” Contributions to microbiology and immunology, vol. 12, pp. 307–310, 1991.
[12]
K. Shiozawa, T. Nishina, Y. Miwa, T. Mori, S. Akahane, and K. Ito, “Colonization in the tonsils of swine by Yersinia enterocolitica,” Contributions to Microbiology and Immunology, vol. 12, pp. 63–67, 1991.
[13]
M. Inoue, H. Nakashima, and O. Ueba, “Community outbreak of Yersinia pseudotuberculosis,” Microbiology and Immunology, vol. 28, no. 8, pp. 883–891, 1984.
[14]
M. Tsubokura, K. Otsuki, K. Sato et al., “Special features of distribution of Yersinia pseudotuberculosis in Japan,” Journal of Clinical Microbiology, vol. 27, no. 4, pp. 790–791, 1989.
[15]
H. Fukushima, “Yersinia pseudotuberculosis,” in Foodborne Infection and Food Microbiology, H. Nakanishi and T. Maruyama, Eds., pp. 335–346, Chuouhoki-shuppan, Tokyo, Japan, 2009.
[16]
H. Fukushima, Y. Matsuda, R. Seki et al., “Geographical heterogeneity between Far Eastern and western countries in prevalence of the virulence plasmid, the superantigen Yersinia pseudotuberculosis-derived mitogen, and the high-pathogenicity island among Yersinia pseudotuberculosis strains,” Journal of Clinical Microbiology, vol. 39, no. 10, pp. 3541–3547, 2001.
[17]
M. Fredriksson-Ahomaa and H. Korkeala, “Low occurrence of pathogenic Yersinia enterocolitica in clinical, food, and environmental samples: a methodological problem,” Clinical Microbiology Reviews, vol. 16, no. 2, pp. 220–229, 2003.
[18]
H. Fukushima, K. Katsube, Y. Hata, R. Kishi, and S. Fujiwara, “Rapid separation and concentration of food-borne pathogens in food samples prior to quantification by viable-cell counting and real-time PCR,” Applied and Environmental Microbiology, vol. 73, no. 1, pp. 92–100, 2007.
[19]
C. C. G. Aulisio, I. J. Mehlman, and A. C. Sanders, “Alkali method for rapid recovery of Yersinia enterocolitica and Yersinia pseudotuberculosis from foods,” Applied and Environmental Microbiology, vol. 39, no. 1, pp. 135–140, 1980.
[20]
D. A. Schiemann, “Alkatolerance of Yersinia enterocolitica as a basis for selective isolation from food enrichments,” Applied and Environmental Microbiology, vol. 46, no. 1, pp. 22–27, 1983.
[21]
J. S. Paterson and R. Cook, “A method for the recovery of Pateurella pseudotuberculosis from faeces,” The Journal of Pathology and Bacteriology, vol. 85, pp. 241–242, 1963.
[22]
Anonymous, “Microbiology of food and animal feeding stuffs—horizontal method for the detection of presumptive pathogenic Yersinia enterocolitica,” EN ISO 10273:2003, International Organization for Standardization, Geneva, Switzerland, 2003.
[23]
E. de Boer and J. F. M. Nouws, “Slaughter pigs and pork as a source of human pathogenic Yersinia enterocolitica,” International Journal of Food Microbiology, vol. 12, no. 4, pp. 375–378, 1991.
[24]
H. Fukushima, “New selective agar medium for isolation of virulent Yersinia enterocolitica,” Journal of Clinical Microbiology, vol. 25, no. 6, pp. 1068–1073, 1987.
[25]
K. Kandolo and G. Wauters, “Pyrazinamidase activity in Yersinia enterocolitica and related organisms,” Journal of Clinical Microbiology, vol. 21, no. 6, pp. 980–982, 1985.
[26]
W. J. Laird and D. C. Cavanaugh, “Correlation of autoagglutination and virulence of Yersiniae,” Journal of Clinical Microbiology, vol. 11, no. 4, pp. 430–432, 1980.
[27]
T. Bogdanovich, E. Carniel, H. Fukushima, and M. Skurnik, “Use of O-antigen gene cluster-specific PCRs for the identification and O-genotyping of Yersinia pseudotuberculosis and s,” Journal of Clinical Microbiology, vol. 41, no. 11, pp. 5103–5112, 2003.
[28]
H. Fukushima, K. Maruyama, I. Omori, K. Ito, and S. Kaneko, “Isolation of sucrose-negative Yersinia enterocolitica biotype 3 serotype O3 strains and their pathogenicity,” Current Microbiology, vol. 17, no. 4, pp. 199–202, 1988.
[29]
G. Wauters, M. Janssens, A. G. Steigerwalt, and D. J. Brenner, “Yersinia mollaretii sp. nov. and Yersinia bercovieri sp. nov., formerly called Yersinia enterocolitica biogroups 3A and 3B,” International Journal of Systematic Bacteriology, vol. 38, no. 4, pp. 424–429, 1988.
[30]
B. W. Blais and L. M. Phillippe, “Comparative analysis of yadA and ail polymerase chain reaction methods for virulent Yersinia enterocolitica,” Food Control, vol. 6, no. 4, pp. 211–214, 1995.
[31]
B. W. Wren and S. Tabaqchali, “Detection of pathogenic Yersinia enterocolitica by the polymerase chain reaction,” Lancet, vol. 336, no. 8716, p. 693, 1990.
[32]
H. Nakajima, M. Inoue, T. Mori, K. I. Itoh, E. Arakawa, and H. Watanabe, “Detection and identification of Yersinia pseudotuberculosis and pathogenic Yersinia enterocolitica by an improved polymerase chain reaction method,” Journal of Clinical Microbiology, vol. 30, no. 9, pp. 2484–2486, 1992.
[33]
M. Fredriksson-Ahomaa, A. Stolle, and H. Korkeala, “Molecular epidemiology of Yersinia enterocolitica infections,” FEMS Immunology and Medical Microbiology, vol. 47, no. 3, pp. 315–329, 2006.
[34]
A. D. Jourdan, S. C. Johnson, and I. V. Wesley, “Development of a fluorogenic 5' nuclease PCR assay for detection of the ail gene of pathogenic Yersinia enterocolitica,” Applied and Environmental Microbiology, vol. 66, no. 9, pp. 3750–3755, 2000.
[35]
A. Vishnubhatla, D. Y. C. Fung, R. D. Oberst, M. P. Hays, T. G. Nagaraja, and S. J. A. Flood, “Rapid 5' nuclease (TaqMan) assay for detection of virulent strains of Yersinia enterocolitica,” Applied and Environmental Microbiology, vol. 66, no. 9, pp. 4131–4135, 2000.
[36]
H. Fukushima, Y. Tsunomori, and R. Seki, “Duplex real-time SYBR green PCR assays for detection of 17 species of food- or waterborne pathogens in stools,” Journal of Clinical Microbiology, vol. 41, no. 11, pp. 5134–5146, 2003.
[37]
P. Wolffs, B. Norling, and P. R？dstr？m, “Risk assessment of false-positive quantitative real-time PCR results in food, due to detection of DNA originating from dead cells,” Journal of Microbiological Methods, vol. 60, no. 3, pp. 315–323, 2005.
[38]
K. Sen, “Rapid identification of Yersinia enterocolitica in blood by the 5' nuclease PCR assay,” Journal of Clinical Microbiology, vol. 38, no. 5, pp. 1953–1958, 2000.
[39]
H. Fukushima, J. Kawase, Y. Etoh, et al., “Simultaneous screening of 24 target genes of foodborne pathogens in 35 foodborne outbreaks using multiplex Real-Time SYBR Green PCR analysis,” International Journal of Microbiology, vol. 2010, Article ID 864817, 18 pages, 2010.
