DOI QR코드

DOI QR Code

Prevalence, Serotype Diversity, Genotype and Antibiotic Resistance of Listeria monocytogenes Isolated from Carcasses and Human in Korea

  • Oh, Hyemin (Department of Food and Nutrition, Sookmyung Women's University) ;
  • Kim, Sejeong (Department of Food and Nutrition, Sookmyung Women's University) ;
  • Lee, Soomin (Department of Food and Nutrition, Sookmyung Women's University) ;
  • Lee, Heeyoung (Department of Food and Nutrition, Sookmyung Women's University) ;
  • Ha, Jimyeong (Department of Food and Nutrition, Sookmyung Women's University) ;
  • Lee, Jeeyeon (Department of Food and Nutrition, Sookmyung Women's University) ;
  • Choi, Yukyung (Department of Food and Nutrition, Sookmyung Women's University) ;
  • Choi, Kyoung-Hee (Department of Oral Microbiology, College of Dentistry, Wonkwang University) ;
  • Yoon, Yohan (Department of Food and Nutrition, Sookmyung Women's University)
  • Received : 2018.02.19
  • Accepted : 2018.06.03
  • Published : 2018.10.31

Abstract

This study investigated the prevalence of Listeria monocytogenes in slaughterhouses, and determined serovars and genotypes, and antibiotic resistance of the isolates obtained from slaughterhouses and humans in Korea. Two hundred ninety samples were collected from feces (n=136), carcasses [n=140 (cattle: n=61, swine: n=79)], and washing water (n=14) in nine slaughterhouses. Eleven human isolates were obtained from hospitals and the Korea Center for Disease Control and Prevention. Listeria monocytogenes was enriched and identified, using polymerase chain reaction (PCR) and 16S rRNA sequencing. Serovars and presence of virulence genes were determined, and genetic correlations among the isolates were evaluated by the restriction digest patterns of AscI. Antibiotic resistance of L. monocytogenes isolates were examined against 12 different antibiotics. Of 290 slaughterhouse samples, 15 (5.17%) carcass samples were L. monocytogenes positive. Most L. monocytogenes isolates possessed all the virulence genes, while polymorphisms in the actA gene were found between carcass and human isolates. Serovars 1/2a (33.3%) and 1/2b (46.7%) were the most frequent in carcass isolates. Genetic correlations among the isolates from carcass and clinical isolates were grouped within serotypes, but there were low geographical correlations. Most L. monocytogenes isolates were antibiotic resistant, and some strains showed resistance to more than four antibiotics. These results indicate that L. monocytogenes are isolated from carcass and human in Korea, and they showed high risk serotypes and antibiotic resistance. Therefore, intensive attentions are necessary to be aware for the risk of L. monocytogenes in Korea.

Keywords

References

  1. Althaus D, Lehner A, Brisse S, Maury M, Tasara T, Stephan R. 2014. Characterization of Listeria monocytogenes strains isolated during 2011-2013 from human infections in Switzerland. Foodborne Pathog Dis 11:753-758. https://doi.org/10.1089/fpd.2014.1747
  2. Altuntas EG, Kocan D, Cosansu S, Ayhan K, Juneja VK, Materon L. 2012. Antibiotic and bacteriocin sensitivity of Listeria monocytogenes strains isolated from different foods. Food Nutr Sci 3:363-368.
  3. Brosch R, Chen J, Luchansky JB. 1994. Pulsed-field fingerprinting of listeriae: Identification of genomic divisions for Listeria monocytogenes and their correlation with serovar. Appl Environ Microbiol 60:2584-2592.
  4. Burall LS, Simpson AC, Datta AR. 2011. Evaluation of a serotyping scheme using a combination of an antibody-based serogrouping method and a multiplex PCR assay for identifying the major serotypes of Listeria monocytogenes. J Food Prot 74:403-409. https://doi.org/10.4315/0362-028X.JFP-10-355
  5. Byrne VDV, Hofer E, Vallim DC, Almeida RCDC. 2016. Occurrence and antimicrobial resistance patterns of Listeria monocytogenes isolated from vegetables. Braz J Microbiol 47:438-443. https://doi.org/10.1016/j.bjm.2015.11.033
  6. Carriere C, Allardet-Servent A, Bourg G, Audurier A, Ramuz M. 1991. DNA polymorphism in strains of Listeria monocytogenes. J Clin Microbiol 29:1351-1355.
  7. Carvalho F, Sousa S, Cabanes D. 2014. How Listeria monocytogenes organizes its surface for virulence. Front Cell Infect Microbiol 4:48.
  8. Centers for Disease Control and Prevention (CDC). 2013. Vital signs: Listeria illnesses, deaths, and outbreaks-United States, 2009-2011. Available from: http://www.cdc.gov/mmwr/preview/mmwrhtml/mm6222a4.htm#tab1. Accessed at April 4, 2016.
  9. Centers for Disease Control and Prevention (CDC). 2016. Listeria outbreaks. Available from: http://www.cdc.gov/listeria/outbreaks/index.html. Accessed at March 6, 2016.
  10. Chae MH, Nam HM, Jang GC, Kim HJ, Kim SR, Jung SC, Kang DJ, Kim JK, Lim SK. 2011. Antimicrobial resistance in Campylobacter jejuni and Campylobacter coli isolated from food animals and raw meats in slaughterhouse in Korea during 2010. Kor J Vet Publ Hlth 35:239-245.
  11. Chen J, Luo X, Jiang L, Jin P, Wei W, Liu D, Fang W. 2009. Molecular characteristics and virulence potential of Listeria monocytogenes isolates from Chinese food systems. Food Microbiol 26:103-111. https://doi.org/10.1016/j.fm.2008.08.003
  12. Clinical and Laboratory Standards Institute (CLSI). 2014. Performance standards for antimicrobial susceptibility testing; Twenty-fourth informational supplement (M100-S24).
  13. Conter M, Paludi D, Zanardi E, Ghidini S, Vergara A, Ianieri A. 2009. Characterization of antimicrobial resistance of foodborne Listeria monocytogenes. Int J Food Microbiol 128:497-500. https://doi.org/10.1016/j.ijfoodmicro.2008.10.018
  14. Corantin H, Quessy S, Gaucher ML, Lessard L, Leblanc D, Houde A. 2005. Effectiveness of steam pasteurization in controlling microbiological hazards of cull cow carcasses in a commercial plant. Can J Vet Res 69:200-207.
  15. Doumith M, Bucherieser C, Glaser P, Jaquet C, Martin P. 2004. Differentiation of the major Listeria monocytogenes serovars by multiplex PCR. J Clin Microbiol 42:3819-3822. https://doi.org/10.1128/JCM.42.8.3819-3822.2004
  16. Ennaji H, Timinouni M, Ennaji MM, Hassar M, Cohen N. 2008. Characterization and antibiotic susceptibility of Listeria monocytogenes isolated from poultry and red meat in Morocco. Infect Drug Resist 1:45-50.
  17. European Food Safety Authority (EFSA). 2007. The community summary report on trends and sources of zoonoses, zoonotic agents, antimicrobial resistance and foodborne outbreaks in the European Union in 2006. Available from: http://www.efsa.europa.eu/en/efsajournal/pub/130r. Accessed at March 27, 2016.
  18. European Food Safety Authority (EFSA). 2013a. Analysis of the baseline survey on the prevalence of Listeria monocytogenes in certain ready-to-eat foods in the EU, 2010-2011 Part A: Listeria monocytogenes prevalence estimates. EFSA J 11:3241. https://doi.org/10.2903/j.efsa.2013.3241
  19. European Food Safety Authority (EFSA). 2013b. The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2011. EFSA J 11:3129. https://doi.org/10.2903/j.efsa.2013.3129
  20. Fagerlund A, Langsrud S, Schirmer BCT, Moretro T, Heir E. 2016. Genome analysis of Listeria monocytogenes sequence type 8 strains persisting in salmon and poultry processing environments and comparison with related strains. Plos One 11:e0151117. https://doi.org/10.1371/journal.pone.0151117
  21. Gerzova L, Babak V, Sedlar K, Faldynova M, Videnska P, Cejkova D, Jensen AN, Denis M, Kerouanton A, Ricci A, Cibin V, Osterberg J, Rychlik I. 2015. Characterization of antibiotic resistance gene abundance and microbiota composition in feces of organic and conventional pigs from four EU countries. Plos One 10:e0132892. https://doi.org/10.1371/journal.pone.0132892
  22. Graves LM, Swaminathan B. 2001. PulseNet standardized protocol for subtyping Listeria monocytogenes by macrorestriction and pulsed-field gel electrophoresis. Int J Food Microbiol 65:55-62. https://doi.org/10.1016/S0168-1605(00)00501-8
  23. Guerini MN, Brichta-Harhay DM, Shackelford SD, Arthur TM, Bosilevac JM, Kalchayanand N, Wheeler TL, Koohmaraie M. 2007. Listeria prevalence and Listeria monocytogenes serovar diversity at cull cow and bull processing plants in the United States. J Food Prot 70:2578-2582. https://doi.org/10.4315/0362-028X-70.11.2578
  24. Ha J, Oh H, Kim S, Lee J, Lee S, Lee H, Choi Y, Moon SS, Choi KH, Yoon Y. 2018. Effect of gene actA on the invasion efficiency of Listeria monocytogenes, as observed in healthy and senescent intestinal epithelial cells. J Microbiol Biotechnol 28:59-64. https://doi.org/10.4014/jmb.1710.10026
  25. Hadjilouka A, Andritsos ND, Paramithiotis S, Mataragas M, Drosinos EH. 2014. Listeria monocytogenes serotype prevalence and biodiversity in diverse food products. J Food Prot 77:2115-2120. https://doi.org/10.4315/0362-028X.JFP-14-072
  26. Health Insurance Review and Assessment Service (HIRAS). 2016. Disease statistics. Available from: http://opendata.hira.or.kr/op/opc/olap4thDsInfo.do. Accessed at April 4, 2016.
  27. Howard PJ, Harsono KD, Luchansky JB. 1992. Differentiation of Listeria monocytogenes, Listeria innocua, Listeria ivanovii, and Listeria seeligeri by pulsed-field gel electrophoresis. Appl Environ Microbiol 58:709-712.
  28. Hunter PR, Gaston MA. 1988. Numerical index of the discriminatory ability of typing systems: An application of Simpson's index of diversity. J Clin Microbiol 26:2465-2466.
  29. Jacquet C, Gouin E, Jeannel D, Cossart P, Rocourt J. 2002. Expression of actA, ami, inlB, and listeriolysin O in Listeria monocytogenes of human and food origin. Appl Environ Microbiol 68:616-622. https://doi.org/10.1128/AEM.68.2.616-622.2002
  30. Jang SS, Choo E, Han K, Miyamoto T, Heu S, Ryu S. 2006. Antibiotic resistance and genetic diversity of Listeria monocytogenes isolated from chicken carcasses in Korea. J Microbiol Biotechnol 16:1276-1284.
  31. Jang SS, Fleet GH, Cox JM. 2005. Pulsed-field gel electrophoresis for subtyping of Listeria monocytogenes. J Korean Soc Appl Biol Chem 48:58-64.
  32. Jaradat ZW, Schutze GE, Bhunia AK. 2002. Genetic homogeneity among Listeria monocytogenes strains from infected patients and meat products from two geographic locations determined by phenotyping, ribotyping and PCR analysis of virulence genes. Int J Food Microbiol 76:1-10. https://doi.org/10.1016/S0168-1605(02)00050-8
  33. Kathariou S. 2002. Listeria monocytogenes virulence and pathogenicity, a food safety perspective. J Food Prot 65:1811-1829. https://doi.org/10.4315/0362-028X-65.11.1811
  34. Khen BK, Lynch OA, Carroll J, McDowell DA, Duffy G. 2015. Occurrence, antibiotic resistance and molecular characterization of Listeria monocytogenes in the beef chain in the republic of Ireland. Zoonoses Public Hlth 62:11-17.
  35. Kim SR, Nam HM, Jang GC, Kim AR, Kang MS, Chae MH, Jung SC, Kang DJ, Kim JK, Lim SK. 2011. Antimicrobial resistance in Salmonella isolates from food animals and raw meats in Korea during 2010. Kor J Vet Publ Hlth 35:246-254.
  36. Lane DJ. 1991. 16S/23S rRNA sequencing. In Nucleic acid techniques in bacterial systematics. Stackebrandt E, Goodfellow M (ed). John Wiley and Sons, Chichester, UK. pp 115-175.
  37. Lim SK, Byun JR, Lee HS, Moon DC, Jang GC, Jung SC. 2014a. Antimicrobial resistance of Escherichia coli strains isolated from pigs and their farm environment in Korea. Prev Vet Med 38:61-68. https://doi.org/10.13041/jpvm.2014.38.3.61
  38. Lim SK, Lee JE, Lee HS, Nam HM, Moon DC, Jang GC, Park YJ, Jung YG, Jung SC, Wee SH. 2014b. Trends in antimicrobial sales for livestock and fisheries in Korea during 2003-2012. Korean J Vet Res 54:81-86. https://doi.org/10.14405/kjvr.2014.54.2.81
  39. Lim SK, Nam HM, Jang GC, Kim SR, Chae MH, Jung SC, Kang DJ, Kim JK. 2011. Antimicrobial resistance in Staphylococcus aureus isolated from raw meats in slaughterhouse in Korea during 2010. Kor J Vet Publ Hlth 35:231-238.
  40. Makino SI, Kawamoto K, Takeshi K, Okada Y, Yamasaki M, Yamamoto S, Igimi S. 2005. An outbreak of food-borne listeriosis due to cheese in Japan, during 2001. Int J Food Microbiol 104:189-196. https://doi.org/10.1016/j.ijfoodmicro.2005.02.009
  41. Mathakiya RA, Roy A, Nandasana KN, Koringa PG, Joshi CG. 2009. Evaluation of a rapid molecular method for detection of Listeria monocytogenes directly from broth culture. Vet World 2:177-178.
  42. Meloni D, Piras F, Mureddu A, Fois F, Consolati SG, Lamon S, Mazzette R. 2013. Listeria monocytogenes in five Sardinian swine slaughterhouses: Prevalence, serotype, and genotype characterization. J Food Prot 76:1863-1867. https://doi.org/10.4315/0362-028X.JFP-12-505
  43. Morvan A, Moubareck C, Leclercq A, Herve-Bazin M, Bremont S, Lecuit M, Courvalin P, Monnier AL. 2010. Antimicrobial resistance of Listeria monocytogenes strains isolated from humans in France. Antimicrob Agents Chemother 54:2728-2731. https://doi.org/10.1128/AAC.01557-09
  44. Muhterem-Uyar M, Dalmasso M, Bolocan AS, Hernandez M, Kapetanakou AE, Kuchta T, Manios SG, Melero B, Minarovicova J, Nicolau AI, Rovira J, Skandamis PN, Jordan K, Rodriguez-Lazaro D, Stessl B, Wagner M. 2015. Environmental sampling for Listeria monocytogenes control in food processing facilities reveals three contamination scenarios. Food Control 51:94-107. https://doi.org/10.1016/j.foodcont.2014.10.042
  45. Neves E, Lourenco A, Silva AC, Coutingo R, Brito L. 2008. Pulsed-field gel electrophoresis (PFGE) analysis of Listeria monocytogenes isolates from different sources and geographical origins and representative of the twelve serovars. Syst Appl Microbiol 31:387-392. https://doi.org/10.1016/j.syapm.2008.08.005
  46. Okutani A, Okada Y, Yamamoto S, Igimi S. 2004. Nationwide survey of human Listeria monocytogenes infection in Japan. Epidemiol Infect 132:769-772. https://doi.org/10.1017/S0950268804001967
  47. Perez-Trallero E, Zigorraga C, Artieda J, Alkorta M, Marimon JM. 2014. Two outbreaks of Listeria monocytogenes infection, Northern Spain. Emerg Infect Dis 20:2155-2157. https://doi.org/10.3201/eid2012.140993
  48. Pesavento G, Ducci B, Nieri D, Comodo N, Nostro AL. 2010. Prevalence and antibiotic susceptibility of Listeria spp. isolated from raw meat and retail foods. Food Control 21:708-713. https://doi.org/10.1016/j.foodcont.2009.10.012
  49. Sofos JN, Geornaras I. 2010. Overview of current meat hygiene and safety risks and summary of recent studies on biofilms, and control of Esherichia coli O157:H7 in nonintact, and Listeria monocytogenes in ready-to-eat, meat products. Meat Sci 86:2-14. https://doi.org/10.1016/j.meatsci.2010.04.015
  50. Sokolovic Z, Schuller S, Bohne J, Baur A, Rdest U, Dickneite C, Nichterlein T, Goebel W. 1996. Differences in virulence and in expression of PrfA and PrfA-regulated virulence genes of Listeria monocytogenes strains belonging to serogroup 4. Infect Immun 64:4008-4019.
  51. Srinivasan V, Nam HM, Nguyen LT, Tamilselvam B, Murinda SE, Oliver SP. 2005. Prevalence of antimicrobial resistance genes in Listeria monocytogenes isolated from dairy farms. Foodborne Pathog Dis 2:201-211. https://doi.org/10.1089/fpd.2005.2.201
  52. Swaminathan B, Gerner-Smidt P. 2007. The epidemiology of human listeriosis. Microbes Infect 9:1236-1243. https://doi.org/10.1016/j.micinf.2007.05.011
  53. Weisburg WG, Barns SM, Pelletier DA, Lane DJ. 1991. 16S Ribosomal DNA amplification for phylogenetic study. J Bacteriol 173:697-703. https://doi.org/10.1128/jb.173.2.697-703.1991
  54. Wesley IV, Harmon KM, Dickson JS, Schwartz AR. 2002. Application of a multiplex polymerase chain reaction assay for the simultaneous confirmation of Listeria monocytogenes and other Listeria species in turkey sample surveillance. J Food Prot 65:780-785. https://doi.org/10.4315/0362-028X-65.5.780
  55. Wiedmann M, Bruce JL, Keating C, Johnson AE, McDonough PL, Batt CA. 1997. Ribotypes and virulence gene polymorphisms suggest three distinct Listeria monocytogenes lineages with differences in pathogenic potential. Infect Immun 65:2707-2716.
  56. Yucel N, Citak S, Onder M. 2005. Prevalence and antibiotic resistance of Listeria species in meat products in Ankara, Turkey. Food Microbiol 22:241-245. https://doi.org/10.1016/j.fm.2004.03.007

Cited by

  1. Development of Kinetic Models and Their Applications to Describe the Resistance of Listeria monocytogenes in Napa Cabbage Kimchi to Fermentation Conditions vol.26, pp.1, 2018, https://doi.org/10.3136/fstr.26.53
  2. Enhanced Antibacterial Activity of Silver Nanoparticles Combined with Hydrogen Peroxide Against Multidrug-Resistant Pathogens Isolated from Dairy Farms and Beef Slaughterhouses in Egypt vol.13, pp.None, 2018, https://doi.org/10.2147/idr.s271261
  3. Influence of milk microbiota on Listeria monocytogenes survival during cheese ripening vol.8, pp.9, 2018, https://doi.org/10.1002/fsn3.1806
  4. High Prevalence of Listeria monocytogenes in Smoked Duck: Antibiotic and Heat Resistance, Virulence, and Genetics of the Isolates vol.41, pp.2, 2021, https://doi.org/10.5851/kosfa.2021.e2
  5. Prevalence, Characterization, and Antimicrobial Susceptibility of Listeria monocytogenes from Raw Beef and Slaughterhouse Environments in Korea vol.18, pp.6, 2018, https://doi.org/10.1089/fpd.2020.2903
  6. Dynamic model to describe kinetic behavior of Listeria monocytogenes in smoked salmon vol.41, pp.5, 2018, https://doi.org/10.1111/jfs.12925
  7. Identification of Microbial Flora in Dry Aged Beef to Evaluate the Rancidity during Dry Aging vol.9, pp.11, 2018, https://doi.org/10.3390/pr9112049
  8. Development of antimicrobial hydrogel with edible formulations to control foodborne pathogens on food surfaces consumed raw vol.74, pp.None, 2021, https://doi.org/10.1016/j.ifset.2021.102845