Zusammenfassung
In dieser Studie wurde über einen fünfjährigen Zeitraum (2013–2017) das Vorkommen von humanpathogenen Yersinia enterocolitica in gewürztem Schweinehackfleisch, Schweinefleisch zur Hackfleischherstellung und streichfähigen, kurz gereiften Rohwürsten in Sachsen untersucht. Der Erreger konnte in 11,5% der zum Rohverzehr bestimmten Hackfleischerzeugnisse (n = 2.145) nachgewiesen werden. Rohware zur Hackfleischherstellung (n = 62) erbrachte eine Nachweisquote von 22,6%. Auch in 1,9% der Zwiebelmettwürste (n = 104) wurde Yersinia enterocolitica detektiert. Bei der Verteilung der Biovar/Serovar-Konstellationen entfielen 84,8% auf 4/O:3; 7,2% auf 2/O:9; 5,3% auf 2/O:57, 27 und 2,7% auf 3/O:3. Die hohen Nachweisquoten zeigen, dass die Krankheitserreger in verzehrfertigen Schweinefleischprodukten in Sachsen häufiger vorkommen als bisher angenommen. Neben der Ermittlung der Prävalenz wird gezeigt, dass die verwendete Methode geeignet ist, um Lebensmittel mit verhältnismäßigem Aufwand auf humanpathogene Varianten zu untersuchen. Es werden weiterhin wirksame Maßnahmen benötigt, um einen Eintrag der Yersinien in die Lebensmittelkette zu vermeiden.
Abstract
In this study, the occurrence of human pathogenic Yersinia enterocolitica in spiced minced meat, pork for production of minced meat and soft, short ripened, raw sausages in Saxony, Germany, was investigated over a 5-year period (2013–2017). The pathogen could be isolated in 11.5% of ready-to-eat minced meat samples (n = 2,145). Pork for production of minced meat (n = 62) was positive in 22.6% and raw sausages (n = 104) in 1.9% of the cases. The distribution of biovars/serovars is the following: 84.8% for 4/O:3; 7.2% for 2/O:9; 5.3% for 2/O:5,27 and 2.7% for 3/O:3. The high proportion of positive samples indicates that the appearance of this pathogen in the products investigated in Saxony is more frequent than widely assumed. Moreover, it is shown that the applied method is suitable for the simple detection of pathogenic types in food. The results accentuate the remaining need for measures to prevent this pathogen from entering the food chain.
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References
Arrausi-Subiza M, Ibabe JC, Atxaerandio R, Juste RA, Barral M (2014) Evaluation of different enrichment methods for pathogenic Yersinia species detection by real time PCR. BMC Vet Res 10:192. https://doi.org/10.1186/s12917-014-0192-9
BfR (2015) Sicher verpflegt, Besonders empfindliche Personengruppen in Gemeinschaftseinrichtungen. BfR. https://www.bfr.bund.de/cm/350/sicher-verpflegt-besonders-empfindliche-personengruppen-in-gemeinschaftseinrichtungen.pdf. Aufgerufen am 30. Dezember 2018
Bonardi S, Paris A, Bassi L, Salmi F, Bacci C, Riboldi E, Boni E, D’incau M, Tagliabue S, Brindani F (2010) Detection, semiquantitative enumeration, and antimicrobial susceptibility of Yersinia enterocolitica in pork and chicken meats in Italy. J Food Prot 73:1785–1792. https://doi.org/10.4315/0362-028X-73.10.1785
Bonardi S, Bassi L, Brindani F, D’Incau M, Barco L, Carra E, Pongolini S (2013) Prevalence, characterization and antimicrobial susceptibility of Salmonella enterica and Yersinia enterocolitica in pigs at slaughter in Italy. Int J Food Microbiol 163:248–257. https://doi.org/10.1016/j.ijfoodmicro.2013.02.012
Bucher M, Meyer C, Grötzbach B, Wacheck S, Stolle A, Fredriksson-Ahomaa M (2008) Epidemiological data on pathogenic Yersinia enterocolitica in Southern Germany during 2000-2006. Foodborne Pathog Dis 5:273–280. https://doi.org/10.1089/fpd.2007.0076
DGE (2015) DGE-Qualitätsstandard für die Verpflegung in Tageseinrichtungen für Kinder. DGE. https://www.fitkid-aktion.de/fileadmin/user_upload/medien/DGE_Qualitaetsstandard_FITKID.pdf. Aufgerufen am 30. Dezember 2018
EFSA (2007) Monitoring and identification of human enteropathogenic Yersinia spp. EFSA J 595:1–30. https://doi.org/10.2903/j.efsa.2007.595
EFSA, ECDC (2017) The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2016. EFSA J 15:5077. https://doi.org/10.2903/j.efsa.2017.5077
Fondrevez M, Minvielle B, Labbé A, Houdayer C, Rose N, Esnault E, Denis M (2014) Prevalence of pathogenic Yersinia entero-colitica in slaughter-aged pigs during a one-year survey, 2010–2011, France. Int J Food Microbiol 174:56–62. https://doi.org/10.1016/j.ijfoodmicro.2013.12.027
Fredriksson-Ahomaa M, Hielm S, Korkeala H (1999) High prevalence of yadA-positive Yersinia enterocolitica in pig tongues and minced meat at the retail level in Finland. J Food Prot 62:123–127. https://doi.org/10.4315/0362-028X-62.2.123
Fredriksson-Ahomaa M, Bucher M, Hank C, Stolle A, Korkeala H (2001) High prevalence of Yersinia enterocolitica 4:O3 on pig offal in Southern Germany: a slaughtering tech-nique problem. Syst Appl Microbiol 24:457–463. https://doi.org/10.1078/0723-2020-00055
Fredriksson-Ahomaa M, Stolle A, Stephan R (2007) Prevalence of pathogenic Yersinia enterocolitica in pigs slaughtered at a Swiss abattoir. Int J Food Microbiol 119:207–212. https://doi.org/10.1016/j.ijfoodmicro.2007.07.050
Gürtler M, Alter T, Kasimir S, Linnebur M, Fehlhaber K (2005) Prevalence of Yersinia enterocolitica in fattening pigs. J Food Prot 68:850–854. https://doi.org/10.4315/0362-028X-68.4.850
ISO 10273:2003, Microbiology of food and animal feeding stuffs—Horizontal method for the detection of presumptive Yersinia enterocolitica
ISO/TS 18867:2015, Microbiology of the food chain—polymerase chain reaction (PCR) for the detection of food-borne pathogens—detection of pathogenic Yersinia enterocolitica and Yersinia pseudotuberculosis
ISO 10273:2017, Microbiology of the food chain—Horizontal method for the detection of pathogenic Yersinia enterocolitica
Ivanovic J, Mitrovic R, Janjic J, Boskovic M (2015) Inactivation of Yersinia enterocolitica in fermented sausages during fermentation. J Agric Sci Technol 5:626–634. https://doi.org/10.17265/2161-6264/2015.09.005
Koch CU (2003) Ein Beitrag zur Epidemiologie und Verbreitung von pathogenen Yersinia enterocolitica 4/O :3 in Münchener Metzgereien. Dissertation. Ludwig-Maximilians-Universität München
Kraushaar B, Dieckmann R, Wittwer M, Knabner D, Konietzny A, Mäde D, Strauch E (2011) Characterization of a Yersinia enterocolitica biotype 1A strain harbouring an ail gene. J Appl Microbiol 111:997–1005. https://doi.org/10.1111/j.1365-2672.2011.05112.x
Laukkanen-Ninios R, Fredriksson-Ahomaa M, Korkeala H (2014) En-teropathogenic yersinia in the pork production chain: challenges for control. Compr Rev Food Sci Food Saf 13:1165–1191. https://doi.org/10.1111/1541-4337.12108
Lindqvist R, Lindblad M (2009) Inactivation of Escherichia coli, Listeria monocytogenes and Yersinia enterocolitica in fermented sausages during maturation/storage. Int J Food Microbiol 129:59–67. https://doi.org/10.1016/j.ijfoodmicro.2008.11.011
Mäde D, Reiting R, Strauch E, Ketteritzsch K, Wicke A (2008) A real-time PCR for detection of pathogenic Yersinia enterocolitica in food combined with an Universal Internal Amplification Control System. J Verb Lebensm 3:141–151. https://doi.org/10.1007/s00003-008-0341-9
Messelhäusser U, Kampf P, Colditz J, Bauer H, Schreiner H, Holler C, Busch U (2011) Qualitative and quantitative detection of human pathogenic Yersinia enterocolitica in different food matrices at retail level in Bavaria. Foodborne Pathog Dis 8:39–44. https://doi.org/10.1089/fpd.2010.0589
Nesbakken T, Kapperud G, Dommarsnes K, Skurnik M, Hornes E (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 57:389–394
Ortiz Martínez P, Fredriksson-Ahomaa M, Pallotti A, Rosmini R, Houf K, Korkeala H (2011) Variation in the prevalence of enteropathogenic yersinia in slaughter pigs from Belgium, Italy, and Spain. Foodborne Pathog Dis 8:445–450. https://doi.org/10.1089/fpd.2009.0461
Petsios S, Fredriksson-Ahomaa M, Sakkas H, Papadopoulou C (2016) Conventional and molecular methods used in the detection and subtyping of Yersinia enterocolitica in food. Int J Food Microbiol 237:55–72. https://doi.org/10.1016/j.ijfoodmicro.2016.08.015
RKI (2012) Yersiniose - Risikofaktoren in Deutschland. Epidemiol Bull 6:47–54
RKI (2017) Yersiniose. In: Diercke M (ed) Infektionsepidemiologisches Jahrbuch meldepflichtiger Krankheiten für 2016. RKI, Berlin, pp 226–229
Sihvonen LM, Hallanvuo S, Haukka K, Skurnik M, Siitonen A (2011) The ail gene is present in some Yersinia enterocolitica biotype 1A strains. Foodborne Pathog Dis 8:455–457. https://doi.org/10.1089/fpd.2010.0747
Stamm I, Hailer M, Depner B, Kopp PA, Rau J (2013) Yersinia en-terocolitica in diagnostic fecal samples from european dogs and cats: identification by fourier transform infrared spectroscopy and matrix-assisted laser desorption ionization-time of flight mass spectrometry. J Clin Microbiol 51:887–893. https://doi.org/10.1128/Jcm.02506-12
Tennant SM, Grant TH, Robins-Browne RM (2003) Pathogenicity of Yersinia enterocolitica biotype 1A. FEMS Immunol Med Microbiol 38:127–137. https://doi.org/10.1016/S0928-8244(03)00180-9
Thisted Lambertz S, Danielsson-Tham M-L (2005) Identification and characterization of pathogenic yersinia enterocolitica isolates by PCR and pulsed-field gel electrophoresis. Appl Environ Microbiol 71:3674–3681. https://doi.org/10.1128/AEM.71.7.3674-3681.2005
Thisted Lambertz S, Granath K, Fredriksson-Ahomaa M, Johansson K-E, Danielsson-Tham M-L (2007) Evaluation of a combined culture and PCR method (NMKL-163A) for detection of presumptive pathogenic Yersinia enterocolitica in pork products. J Food Prot 70:335–340. https://doi.org/10.4315/0362-028X-70.2.335
Van Damme I, Berkvens D, Botteldoorn N, Dierick K, Wits J, Pochet B, De Zutter L (2013) Evaluation of the ISO 10273:2003 method for the isolation of human pathogenic Yersinia enterocolitica from pig carcasses and minced meat. Food Microbiol 36:170–175. https://doi.org/10.1016/j.fm.2013.05.007
Vanantwerpen G, Houf K, Van Damme I, Berkvens D, De Zutter L (2013) Estimation of the within-batch prevalence and quantification of human pathogenic Yersinia enterocolitica in pigs at slaughter. Food Control 34:9–12. https://doi.org/10.1016/j.foodcont.2013.04.005
Wicke A, Paulsen P, Ketteritzsch K, Mäde D (2018) Nachweis und Beurteilung von pathogenen Yersinia enterocolitica in Lebensmitteln. Rundschau für Fleischhygiene und Lebensmittelüberwachung 2:46–47
Acknowledgements
Wir danken dem Konsiliarlabor Yersinia unter Leitung von Herrn Dr. Stefan Hertwig für die zuverlässige Typisierung der Isolate sowie Daniel Pilz, Heike Bwalya, Heike Scholz, Josephine Voigt und Sandra Müller für ihre hervorragende technische Unterstützung.
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Ferl, M., Mäde, D. & Braun, P.G. Combined molecular biological and microbiological detection of pathogenic Yersinia enterocolitica in spiced ground pork, meat for production of ground pork and raw sausages. J Consum Prot Food Saf 15, 27–35 (2020). https://doi.org/10.1007/s00003-019-01257-x
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DOI: https://doi.org/10.1007/s00003-019-01257-x