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Detection of Yersinia enterocolitica in food: an overview

  • V. Gupta
  • P. GulatiEmail author
  • N. Bhagat
  • M. S. Dhar
  • J. S. Virdi
Review

Abstract

Yersinia enterocolitica is a gastrointestinal pathogen which causes yersiniosis, an illness characterized by diarrhea, ileitis, and mesenteric lymphadenitis. Y. enterocolitica is transmitted via the feco-oral route by the consumption of contaminated food or water. Several phenotypic and genotypic methods have been developed to reliably detect Y. enterocolitica in food. However, the source of infection of many recently reported foodborne outbreaks remains obscure. The detection of this pathogen in food is a challenging task, since it shares similarities with other enteric bacteria. The presence of other microorganisms in the food samples makes it even more difficult to identify this slow-growing pathogen. Therefore, the present-day emphasis is on the development of sensitive, easily automated methods suitable for in-situ detection, allowing quick and cost-effective characterization of food samples. This review summarizes and compares the currently available cultural, immunological, and molecular methods, particularly in relation to their specific merits or demerits when implemented for the detection of Y. enterocolitica in food.

Keywords

Food Sample Multiplex Polymerase Chain Reaction Nest Polymerase Chain Reaction Foodborne Pathogen Yersinia Enterocolitica 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

We acknowledge Mr. Swarnendra Singh, National Institute of Immunology, New Delhi, India, for his critical reading, formatting, and editing, which helped to improve the manuscript.

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. 1.
    Ostroff S (1995) Yersinia as an emerging infection: epidemiologic aspects of yersiniosis. Contrib Microbiol Immunol 13:5–10PubMedGoogle Scholar
  2. 2.
    Sharma S, Sachdeva P, Virdi JS (2003) Emerging water-borne pathogens. Appl Microbiol Biotechnol 61:424–428CrossRefPubMedGoogle Scholar
  3. 3.
    Rosner BM, Stark K, Werber D (2010) Epidemiology of reported Yersinia enterocolitica infections in Germany, 2001–2008. BMC Public Health 10:337–343CrossRefPubMedCentralPubMedGoogle Scholar
  4. 4.
    Bottone EJ (1999) Yersinia enterocolitica: overview and epidemiologic correlates. Microbes Infect 1:323–333CrossRefPubMedGoogle Scholar
  5. 5.
    Leclercq A, Martin L, Vergnes ML et al (2005) Fatal Yersinia enterocolitica biotype 4 serovar O:3 sepsis after red blood cell transfusion. Transfusion 45:814–818CrossRefPubMedGoogle Scholar
  6. 6.
    Golubov A, Heesemann J, Rakin A (2003) Uncovering genomic differences in human pathogenic Yersinia enterocolitica. FEMS Immunol Med Microbiol 38:107–111CrossRefPubMedGoogle Scholar
  7. 7.
    Wauters G, Kandolo K, Janssens M (1987) Revised biogrouping scheme of Yersinia enterocolitica. Contrib Microbiol Immunol 9:14–21PubMedGoogle Scholar
  8. 8.
    Skurnik M, Rådström P, Knutsson R et al (2010) Yersinia. In: Liu D (ed) Molecular detection of foodborne pathogens. CRC Press, Boca Raton, pp 501–520Google Scholar
  9. 9.
    Schiemann DA (1989) Yersinia enterocolitica and Yersinia pseudotuberculosis. In: Doyle MP (ed) Foodborne bacterial pathogens. Marcel Dekker, New York, pp 601–672Google Scholar
  10. 10.
    Doherty A, Sheridan JJ, Allen P et al (1995) Growth of Yersinia enterocolitica O:3 on modified atmosphere packaged lamb. Food Microbiol 12:251–257CrossRefGoogle Scholar
  11. 11.
    Swaminathan B, Harmon MC, Mehlman IJ (1982) A review: Yersinia enterocolitica. J Appl Bacteriol 52:151–183CrossRefPubMedGoogle Scholar
  12. 12.
    Black RE, Jackson RJ, Tsai T et al (1978) Epidemic Yersinia enterocolitica infection due to contaminated chocolate milk. N Engl J Med 298:76–79CrossRefPubMedGoogle Scholar
  13. 13.
    Shayegani M, Morse D, DeForge I et al (1983) Microbiology of a major foodborne outbreak of gastroenteritis caused by Yersinia enterocolitica serogroup O:8. J Clin Microbiol 17:35–40PubMedCentralPubMedGoogle Scholar
  14. 14.
    Lee TS, Lee SW, Seok WS et al (2004) Prevalence, antibiotic susceptibility, and virulence factors of Yersinia enterocolitica and related species from ready-to-eat vegetables available in Korea. J Food Prot 67:1123–1127PubMedGoogle Scholar
  15. 15.
    Tacket CO, Ballard J, Harris N et al (1985) An outbreak of Yersinia enterocolitica infections caused by contaminated tofu (soybean curd). Am J Epidemiol 121:705–711CrossRefPubMedGoogle Scholar
  16. 16.
    Tuori MR, Valtonen V (1983) Yersina enterocolitica outpatient epidemic. Duodecim 99:706–711PubMedGoogle Scholar
  17. 17.
    Aber R, McCarthy MA, Berman R et al (1982) An outbreak of Yersinia enterocolitica gastrointestinal illness among members of a Brownie troop in Centre County, Pennsylvania. In: Proceedings of the 22nd International Conference on Antimicrobial Agents and Chemotherapy, Miami, Florida, October 1982. American Society for Microbiology, pp 1–245Google Scholar
  18. 18.
    Barrett NJ (1986) Communicable disease associated with milk and dairy products in England and Wales: 1983–1984. J Infect 12:265–272CrossRefPubMedGoogle Scholar
  19. 19.
    Marjai E, Kálmán M, Kajáry I et al (1987) Isolation from food and characterization by virulence tests of Yersinia enterocolitica associated with an outbreak. Acta Microbiol Hung 34:97–109PubMedGoogle Scholar
  20. 20.
    Butt HL, Gordon DL, Lee-Archer T et al (1991) Relationship between clinical and milk isolates of Yersinia enterocolitica. Pathology 23:153–157CrossRefPubMedGoogle Scholar
  21. 21.
    Alsterlund R, Danielsson-Tham ML, Karp G et al (1995) An outbreak of Yersinia enterocolitica infection on the Bjärred Peninsula. Indications for risks of refrigerated food. Lakartidningen 92:1213–1214PubMedGoogle Scholar
  22. 22.
    Lee LA, Gerber AR, Lonsway DR (1990) Yersinia enterocolitica O:3 infections in infants and children, associated with the household preparation of chitterlings. N Engl J Med 322:984–987CrossRefPubMedGoogle Scholar
  23. 23.
    Greenwood MH, Hooper WL (1990) Excretion of Yersinia spp. associated with consumption of pasteurized milk. Epidemiol Infect 104:345–350CrossRefPubMedCentralPubMedGoogle Scholar
  24. 24.
    Greenwood MH, Hooper WL, Rodhouse JC (1990) The source of Yersinia spp. in pasteurized milk: an investigation at a dairy. Epidemiol Infect 104:351–360CrossRefPubMedCentralPubMedGoogle Scholar
  25. 25.
    Ackers ML, Schoenfeld S, Markman J et al (2000) An outbreak of Yersinia enterocolitica O:8 infections associated with pasteurized milk. J Infect Dis 181:1834–1837CrossRefPubMedGoogle Scholar
  26. 26.
    Abraham M, Pai M, Kang G et al (1997) An outbreak of food poisoning in Tamil Nadu associated with Yersinia enterocolitica. Indian J Med Res 106:465–468PubMedGoogle Scholar
  27. 27.
    Lynch M, Painter J, Woodruff R et al; Centers for Disease Control and Prevention (CDC) (2006) Surveillance for foodborne-disease outbreaks—United States, 1998–2002. MMWR Surveill Summ 55:1–42PubMedGoogle Scholar
  28. 28.
    Sakai T, Nakayama A, Hashida M et al (2005) Outbreak of food poisoning by Yersinia enterocolitica serotype O:8 in Nara prefecture: the first case report in Japan. Jpn J Infect Dis 58:257–258PubMedGoogle Scholar
  29. 29.
    Grahek-Ogden D, Schimmer B, Cudjoe KS et al (2007) Outbreak of Yersinia enterocolitica serogroup O:9 infection and processed pork, Norway. Emerg Infect Dis 13:754–756CrossRefPubMedCentralPubMedGoogle Scholar
  30. 30.
    MacDonald E, Heier B, Stalheim T et al (2011) Yersinia enterocolitica O:9 infections associated with bagged salad mix in Norway: February to April 2011. Euro Surveill 16. pii: 19866Google Scholar
  31. 31.
    European Centre for Disease Prevention and Control (ECDC) (2011) Annual epidemiological report: reporting on 2009 surveillance data and 2010 epidemic intelligence data. ECDC, StockholmGoogle Scholar
  32. 32.
    European Food Safety Authority (EFSA) (2012) The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2010. EFSA J 10:2597Google Scholar
  33. 33.
    Fredriksson-Ahomaa M, Korkeala H (2003) Low occurrence of pathogenic Yersinia enterocolitica in clinical, food, and environmental samples: a methodological problem. Clin Microbiol Rev 16:220–229CrossRefPubMedCentralPubMedGoogle Scholar
  34. 34.
    Schiemann DA, Olson SA (1984) Antagonism by gram-negative bacteria to growth of Yersinia enterocolitica in mixed culture. Appl Environ Microbiol 48:539–544PubMedCentralPubMedGoogle Scholar
  35. 35.
    Wauters G (1973) Improved methods for the isolation and the recognition of Yersinia enterocolitica. Contrib Microbiol Immunol 2:68–70Google Scholar
  36. 36.
    Schiemann DA (1979) Synthesis of a selective agar medium for Yersinia enterocolitica. Can J Microbiol 25:1298–1304CrossRefPubMedGoogle Scholar
  37. 37.
    Patel PD, Williams DW (1994) Evaluation of commercial kits and instruments for the detection of foodborne bacterial pathogens and toxins. In: Patel PD (ed) Rapid analysis techniques in food microbiology. Chapman & Hall, London, pp 87–88Google Scholar
  38. 38.
    Kapperud G, Vardund T, Skjerve E et al (1993) Detection of pathogenic Yersinia enterocolitica in foods and water by immunomagnetic separation, nested polymerase chain reactions, and colorimetric detection of amplified DNA. Appl Environ Microbiol 59:2938–2944PubMedCentralPubMedGoogle Scholar
  39. 39.
    Hochel I, Skvor J (2007) Characterization of rabbit antibodies for immunochemical detection of Yersinia enterocolitica. Folia Microbiol (Praha) 52:511–518CrossRefGoogle Scholar
  40. 40.
    Kaneko S, Maruyama T (1989) Evaluation of enzyme immunoassay for the detection of pathogenic Yersinia enterocolitica and Yersinia pseudotuberculosis strains. J Clin Microbiol 27:748–751PubMedCentralPubMedGoogle Scholar
  41. 41.
    Thibodeau V, Frost EH, Quessy S (2001) Development of an ELISA procedure to detect swine carriers of pathogenic Yersinia enterocolitica. Vet Microbiol 82:249–259CrossRefPubMedGoogle Scholar
  42. 42.
    Magliulo M, Simoni P, Guardigli M (2007) A rapid multiplexed chemiluminescent immunoassay for the detection of Escherichia coli O157:H7, Yersinia enterocolitica, Salmonella typhimurium, and Listeria monocytogenes pathogen bacteria. J Agric Food Chem 55:4933–4939CrossRefPubMedGoogle Scholar
  43. 43.
    Gui J, Patel IR (2011) Recent advances in molecular technologies and their application in pathogen detection in foods with particular reference to Yersinia. J Pathog 2011:310135. doi: 10.4061/2011/310135 CrossRefPubMedCentralPubMedGoogle Scholar
  44. 44.
    Oh BK, Lee W, Chun BS et al (2005) Surface plasmon resonance immunosensor for the detection of Yersinia enterocolitica. Colloids Surf A Physicochem Eng Asp 257–258:369–374CrossRefGoogle Scholar
  45. 45.
    Nesbakken T, Kapperud G, Dommarsnes K et al (1991) Comparative study of a DNA hybridization method and two isolation procedures for detection of Yersinia enterocolitica O:3 in naturally contaminated pork products. Appl Environ Microbiol 57:389–394PubMedCentralPubMedGoogle Scholar
  46. 46.
    Myers KM, Gaba J, Al-Khaldi SF (2006) Molecular identification of Yersinia enterocolitica isolated from pasteurized whole milk using DNA microarray chip hybridization. Mol Cell Probes 20:71–80CrossRefPubMedGoogle Scholar
  47. 47.
    Giannino ML, Aliprandi M, Feligini M et al (2009) A DNA array based assay for the characterization of microbial community in raw milk. J Microbiol Methods 78:181–188CrossRefPubMedGoogle Scholar
  48. 48.
    Goverde RLJ, Jansen WH, Brunings HA et al (1993) Digoxigenin-labelled inv- and ail-probes for the detection and identification of pathogenic Yersinia enterocolitica in clinical specimens and naturally contaminated pig samples. J Appl Bacteriol 74:301–313CrossRefPubMedGoogle Scholar
  49. 49.
    Durisin MD, Ibrahim A, Griffiths MW (1997) Detection of pathogenic Yersinia enterocolitica in milk and pork using a DIG-labelled probe targeted against the yst gene. Int J Food Microbiol 37:103–112CrossRefPubMedGoogle Scholar
  50. 50.
    Fredriksson-Ahomaa M, Stolle A, Korkeala H (2006) Molecular epidemiology of Yersinia enterocolitica infections. FEMS Immunol Med Microbiol 47:315–329CrossRefPubMedGoogle Scholar
  51. 51.
    Nakajima H, Inoue M, Mori T et al (1992) Detection and identification of Yersinia pseudotuberculosis and pathogenic Yersinia enterocolitica by an improved polymerase chain reaction method. J Clin Microbiol 30:2484–2486PubMedCentralPubMedGoogle Scholar
  52. 52.
    Weynants V, Jadot V, Denoel PA et al (1996) Detection of Yersinia enterocolitica serogroup O:3 by a PCR method. J Clin Microbiol 34:1224–1227PubMedCentralPubMedGoogle Scholar
  53. 53.
    Garzetti D, Susen R, Fruth A et al (2014) A molecular scheme for Yersinia enterocolitica patho-serotyping derived from genome-wide analysis. Int J Med Microbiol 304:275–283CrossRefPubMedGoogle Scholar
  54. 54.
    Jourdan AD, Johnson SC, Wesley IV (2000) Development of a fluorogenic 5′ nuclease PCR assay for detection of the ail gene of pathogenic Yersinia enterocolitica. Appl Environ Microbiol 66:3750–3755CrossRefPubMedCentralPubMedGoogle Scholar
  55. 55.
    Boyapalle S, Wesley IV, Hurd HS et al (2001) Comparison of culture, multiplex, and 5′ nuclease polymerase chain reaction assays for the rapid detection of Yersinia enterocolitica in swine and pork products. J Food Prot 64:1352–1361PubMedGoogle Scholar
  56. 56.
    Wu VCH, Fung DY, Oberst RD (2004) Evaluation of a 5′-nuclease (TaqMan) assay with the thin agar layer oxyrase method for the detection of Yersinia enterocolitica in ground pork samples. J Food Prot 67:271–277PubMedGoogle Scholar
  57. 57.
    Fredriksson-Ahomaa M, Hartmann B, Scheu P et al (2007) Detection of pathogenic Yersinia enterocolitica in meat using real-time PCR. J Cons Prot Food Saf 2:202–208Google Scholar
  58. 58.
    Mäde D, Reiting R, Strauch E et al (2008) A real-time PCR for detection of pathogenic Yersinia enterocolitica in food combined with an universal internal amplification control system. J Cons Prot Food Saf 3:141–151Google Scholar
  59. 59.
    Lambertz ST, Nilsson C, Hallanvuo S et al (2008) Real-time PCR method for detection of pathogenic Yersinia enterocolitica in food. Appl Environ Microbiol 74:6060–6067CrossRefPubMedCentralPubMedGoogle Scholar
  60. 60.
    Ikeda M, Yamaguchi N, Tani K et al (2006) Detection of food poisoning bacteria in fresh vegetables using DNA microarray. J Health Sci 52:36–42CrossRefGoogle Scholar
  61. 61.
    Bang J, Beuchat LR, Gu MB et al (2010) Identification of Yersinia enterocolitica using a random genomic DNA microarray chip. Lett Appl Microbiol 51:665–670CrossRefPubMedGoogle Scholar
  62. 62.
    Kim DH, Lee BK, Kim YD et al (2010) Detection of representative enteropathogenic bacteria, Vibrio spp., pathogenic Escherichia coli, Salmonella spp., Shigella spp., and Yersinia enterocolitica, using a virulence factor gene-based oligonucleotide microarray. J Microbiol 48:682–688CrossRefPubMedGoogle Scholar
  63. 63.
    Tomita N, Mori Y, Kanda H et al (2008) Loop-mediated isothermal amplification (LAMP) of gene sequences and simple visual detection of products. Nat Protoc 3:877–882CrossRefPubMedGoogle Scholar
  64. 64.
    Mori Y, Nagamine K, Tomita N et al (2001) Detection of loop-mediated isothermal amplification reaction by turbidity derived from magnesium pyrophosphate formation. Biochem Biophys Res Commun 289:150–154CrossRefPubMedGoogle Scholar
  65. 65.
    Gao H, Lei Z, Jia J et al (2009) Application of loop-mediated isothermal amplification for detection of Yersinia enterocolitica in pork meat. J Microbiol Methods 77:198–201CrossRefPubMedGoogle Scholar
  66. 66.
    Li Y, Jiang M, Liu W et al (2010) Loop-mediated isothermal amplification method targets to the phoP gene for detection of Yersinia enterocolitica. Mol Cell Probes 24:68–71CrossRefPubMedGoogle Scholar
  67. 67.
    Bai S, Zhao J, Zhang Y et al (2010) Rapid and reliable detection of 11 food-borne pathogens using thin-film biosensor chips. Appl Microbiol Biotechnol 86:983–990CrossRefPubMedGoogle Scholar
  68. 68.
    Greenwood JR, Flanigan SM, Pickett MJ et al (1975) Clinical isolation of Yersinia enterocolitica: cold temperature enrichment. J Clin Microbiol 2:559–560PubMedCentralPubMedGoogle Scholar
  69. 69.
    de Boer E (1992) Isolation of Yersinia enterocolitica from foods. Int J Food Microbiol 17:75–84Google Scholar
  70. 70.
    Schiemann DA (1983) Alkalotolerance of Yersinia enterocolitica as a basis for selective isolation from food enrichments. Appl Environ Microbiol 46:22–27PubMedCentralPubMedGoogle Scholar
  71. 71.
    Lee WH, Harris ME, McClain D et al (1980) Two modified selenite media for the recovery of Yersinia enterocolitica from meats. Appl Environ Microbiol 39:205–209PubMedCentralPubMedGoogle Scholar
  72. 72.
    Wauters G, Goossens V, Janssens M et al (1988) New enrichment method for isolation of pathogenic Yersinia enterocolitica serogroup O:3 from pork. Appl Environ Microbiol 54:851–854PubMedCentralPubMedGoogle Scholar
  73. 73.
    Toora S, Budu-Amoako E, Ablett RF et al (1994) Isolation of Yersinia enterocolitica from ready-to-eat foods and pork by a simple two step procedure. Food Microbiol 11:369–374CrossRefGoogle Scholar
  74. 74.
    Hussein HM, Fenwick SG, Lumsden JS (2001) A rapid and sensitive method for the detection of Yersinia enterocolitica strains from clinical samples. Lett Appl Microbiol 33:445–449CrossRefPubMedGoogle Scholar
  75. 75.
    Head CB, Whitty DA, Ratnam S (1982) Comparative study of selective media for recovery of Yersinia enterocolitica. J Clin Microbiol 16:615–621PubMedCentralPubMedGoogle Scholar
  76. 76.
    Tan LK, Ooi PT, Carniel E et al (2014) Evaluation of a modified cefsulodin–irgasan–novobiocin agar for isolation of Yersinia spp. PLoS One 9(8):e106329. doi: 10.1371/journal.pone.0106329 CrossRefPubMedCentralPubMedGoogle Scholar
  77. 77.
    Weagant SD (2008) A new chromogenic agar medium for detection of potentially virulent Yersinia enterocolitica. J Microbiol Methods 72:185–190CrossRefPubMedGoogle Scholar
  78. 78.
    Denis M, Houard E, Labbé A et al (2011) A selective chromogenic plate, YECA, for the detection of pathogenic Yersinia enterocolitica: specificity, sensitivity, and capacity to detect pathogenic Y. enterocolitica from pig tonsils. J Pathog 2011:296275. doi: 10.4061/2011/296275 CrossRefPubMedCentralPubMedGoogle Scholar
  79. 79.
    Renaud N, Lecci L, Courcol RJ et al (2013) CHROMagar Yersinia, a new chromogenic agar for screening of potentially pathogenic Yersinia enterocolitica isolates in stools. J Clin Microbiol 51:1184–1187CrossRefPubMedCentralPubMedGoogle Scholar
  80. 80.
    Devenish JA, Schiemann DA (1981) An abbreviated scheme for identification of Yersinia enterocolitica isolated from food enrichments on CIN (cefsulodin–irgasan–novobiocin) agar. Can J Microbiol 27:937–941CrossRefPubMedGoogle Scholar
  81. 81.
    Johnson JL (1998) Isolation and identification of pathogenic Yersinia enterocolitica from meat and poultry products. In: Dey BP, Lattuada CP (eds) USDA/FSIS microbiology laboratory guidebook. US Department of Agriculture, Washington, DC, 28 ppGoogle Scholar
  82. 82.
    Malorny B, Tassios PT, Rådström P et al (2003) Standardization of diagnostic PCR for the detection of foodborne pathogens. Int J Food Microbiol 83:39–48CrossRefPubMedGoogle Scholar
  83. 83.
    Knutsson R, Fontanesi M, Grage H et al (2002) Development of a PCR-compatible enrichment medium for Yersinia enterocolitica: amplification precision and dynamic detection range during cultivation. Int J Food Microbiol 72:185–201CrossRefPubMedGoogle Scholar
  84. 84.
    Wolffs P, Knutsson R, Norling B et al (2004) Rapid quantification of Yersinia enterocolitica in pork samples by a novel sample preparation method, flotation, prior to real-time PCR. J Clin Microbiol 42:1042–1047CrossRefPubMedCentralPubMedGoogle Scholar
  85. 85.
    Kuhm AE, Suter D, Felleisen R et al (2009) Identification of Yersinia enterocolitica at the species and subspecies levels by Fourier transform infrared spectroscopy. Appl Environ Microbiol 75:5809–5813CrossRefPubMedCentralPubMedGoogle Scholar
  86. 86.
    Stephan R, Cernela N, Ziegler D et al (2011) Rapid species specific identification and subtyping of Yersinia enterocolitica by MALDI-TOF mass spectrometry. J Microbiol Methods 87:150–153CrossRefPubMedGoogle Scholar

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© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • V. Gupta
    • 1
    • 2
  • P. Gulati
    • 1
    Email author
  • N. Bhagat
    • 2
  • M. S. Dhar
    • 2
  • J. S. Virdi
    • 2
  1. 1.Medical Microbiology and Bioprocess Technology Laboratory, Department of MicrobiologyMaharshi Dayanand UniversityRohtakIndia
  2. 2.Microbial Pathogenicity Laboratory, Department of MicrobiologyUniversity of Delhi, South CampusNew DelhiIndia

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