Original Articles Open access

Occurrence and molecular characteristics of Listeria monocytogenes isolated from ready-to-eat meats in Hanoi, Vietnam

Authors

Published
16 October 2020
Section
Original Articles
DOI
10.4081/ijfs.2020.8772

Abstract

Listeria monocytogenes represents one of the most serious threats to food safety. Several studies have shown that Ready-To- Eat (RTE) meats are an important vehicle responsible for listeriosis in human. In Vietnam, little is known about the occurrence and molecular characteristics of L. monocytogenes in meat products, which are essential for developing monitoring plans and control measures. In the present study, we investigated the occurrence of L. monocytogenes in 258 sausage and sliced meat samples collected during the period of 2013-2015 and determined the genetic diversity of the isolates using multi-locus sequence typing (MLST). Overall, L. monocytogenes was present in 19/129 (14.7 %) and 40/129 (31.0 %) sausage and sliced meat samples respectively, with the peak of occurrence being in summer. Furthermore, a minimum spanning tree was constructed based on MLST data of 47 isolates. A total of 15 sequence types were found, with five being novel. Notably, the majority of the isolates (34/47) belonged to the hypervirulent clonal complexes 1, 2, and 3.

Keywords

Supporting Agencies

Hanoi University of Science and Technology

References

  1. Alonso, A. N., Perry, K. J., Regeimbal, J. M., Regan, P. M., & Higgins, D. E. (2014). Identification of Listeria monocytogenes Determinants Required for Biofilm Formation. PLOS ONE, 9, e113696. doi:10.1371/journal.pone.0113696 DOI: https://doi.org/10.1371/journal.pone.0113696
  2. Asturiano Ristori, C., Estela Gravato Rowlands, R., Geraldes Martins, C., Luisa Barbosa, M., T U Yoshida, J., & Franco, B. (2014). Prevalence and Populations of Listeria monocytogenes in Meat Products Retailed in Sao Paulo, Brazil. Foodborne Pathog Dis, 11. doi:10.1089/fpd.2014.1809 DOI: https://doi.org/10.1089/fpd.2014.1809
  3. Aureli, P., Fiorucci, G. C., Caroli, D., Marchiaro, G., Novara, O., Leone, L., et al. (2000). An outbreak of febrile gastroenteritis associated with corn contaminated by Listeria monocytogenes. N Engl J Med, 342, 1236-1241. doi:10.1056/nejm200004273421702 DOI: https://doi.org/10.1056/NEJM200004273421702
  4. Berrang, M. E. (2010). Listeria monocytogenes biofilm formation on silver ion impregnated cutting boards. Food protection trends, v. 30(no. 3), pp. 168-160-2010 v.2030 no.2013.
  5. Cantinelli, T., Chenal-Francisque, V., Diancourt, L., Frezal, L., Leclercq, A., Wirth, T., et al. (2013). "Epidemic clones" of Listeria monocytogenes are widespread and ancient clonal groups. J Clin Microbiol, 51, 3770-3779. doi:10.1128/jcm.01874-13 DOI: https://doi.org/10.1128/JCM.01874-13
  6. Center for Disease Control and Prevention, CDC (2019). Listeria Outbreaks. Retrieved from https://www.cdc.gov/listeria/outbreaks/index.html
  7. Chen, M., Cheng, J., Zhang, J., Chen, Y., Zeng, H., Xue, L., et al. (2019). Isolation, Potential Virulence, and Population Diversity of Listeria monocytogenes From Meat and Meat Products in China. Frontiers in microbiology, 10, 946-946. doi:10.3389/fmicb.2019.00946 DOI: https://doi.org/10.3389/fmicb.2019.00946
  8. Dalzini, E., Bernini, V., Bertasi, B., Daminelli, P., Losio, M.-N., & Varisco, G. (2016). Survey of prevalence and seasonal variability of Listeria monocytogenes in raw cow milk from Northern Italy. Food Control, 60, 466-470. doi:https://doi.org/10.1016/j.foodcont.2015.08.019 DOI: https://doi.org/10.1016/j.foodcont.2015.08.019
  9. Desai, A. N., Anyoha, A., Madoff, L. C., & Lassmann, B. (2019). Changing epidemiology of Listeria monocytogenes outbreaks, sporadic cases, and recalls globally: A review of ProMED reports from 1996 to 2018. International Journal of Infectious Diseases, 84, 48-53. doi:10.1016/j.ijid.2019.04.021 DOI: https://doi.org/10.1016/j.ijid.2019.04.021
  10. Di Bonaventura, G., Piccolomini, R., Paludi, D., D'Orio, V., Vergara, A., Conter, M., et al. (2008). Influence of temperature on biofilm formation by Listeria monocytogenes on various food-contact surfaces: relationship with motility and cell surface hydrophobicity. J Appl Microbiol, 104, 1552-1561. doi:10.1111/j.1365-2672.2007.03688.x DOI: https://doi.org/10.1111/j.1365-2672.2007.03688.x
  11. Di Pinto, A., Novello, L., Montemurro, F., Bonerba, E., & Tantillo, G. J. N. M. (2010). Occurrence of Listeria monocytogenes in ready-to-eat foods from supermarkets in Southern Italy. 33, 249-252.
  12. European Food Safety Authority Panel on Biological Hazards, EFSA (2018). Listeria monocytogenes contamination of ready-to-eat foods and the risk for human health in the EU. EFSA Journal, 16, e05134. doi:10.2903/j.efsa.2018.5134 DOI: https://doi.org/10.2903/j.efsa.2018.5134
  13. ECDC-EFSA. (2019). Multi-country outbreak of Listeria monocytogenes sequence type 6 infections linked to ready-to-eatmeat products – 25 November 2019. EFSA Supporting Publications, 16(12), 1745E. doi:10.2903/sp.efsa.2019.EN-1745 DOI: https://doi.org/10.2903/sp.efsa.2019.EN-1745
  14. Elmali, M., Can, H. Y. i., & Yaman, H. (2015). Prevalence of Listeria monocytogenes in poultry meat %J Food Science and Technology. 35, 672-675.
  15. Furrer, B., Candrian, U., Hoefelein, C., & Luethy, J. (1991). Detection and identification of Listeria monocytogenes in cooked sausage products and in milk by in vitro amplification of haemolysin gene fragments. Journal of Applied Bacteriology, 70, 372-379. doi:10.1111/j.1365-2672.1991.tb02951.x DOI: https://doi.org/10.1111/j.1365-2672.1991.tb02951.x
  16. Jamali, H., Chai, L. C., & Thong, K. L. (2013). Detection and isolation of Listeria spp. and Listeria monocytogenes in ready-to-eat foods with various selective culture media. Food Control, 32, 19-24. doi:https://doi.org/10.1016/j.foodcont.2012.11.033 DOI: https://doi.org/10.1016/j.foodcont.2012.11.033
  17. Iannetti, L., Acciari, V. A., Antoci, S., Addante, N., Bardasi, L., Bilei, S., et al. (2016). Listeria monocytogenes in ready-to-eat foods in Italy: Prevalence of contamination at retail and characterisation of strains from meat products and cheese. Food Control, 68, 55-61. doi:https://doi.org/10.1016/j.foodcont.2016.03.036 DOI: https://doi.org/10.1016/j.foodcont.2016.03.036
  18. Kačániová, M., Kluz, M., Petrová, J., Mellen, M., & Kunová, S. J. M. C. A. (2015). Incidence of Listeria monocytogenes in meat product samples by real time PCR. 3, 1-5.
  19. Kocot, A. M., & Olszewska, M. A. (2017). Biofilm formation and microscopic analysis of biofilms formed by Listeria monocytogenes in a food processing context. LWT, 84, 47-57. doi:https://doi.org/10.1016/j.lwt.2017.05.042 DOI: https://doi.org/10.1016/j.lwt.2017.05.042
  20. Kurpas, M., Wieczorek, K., & Osek, J. (2018). Ready-to-eat Meat Products As a Source of Listeria Monocytogenes. Journal of veterinary research, 62, 49-55. doi:10.1515/jvetres-2018-0007
  21. Linke, K., Rückerl, I., Brugger, K., Karpiskova, R., Walland, J., Muri-Klinger, S., et al. (2014). Reservoirs of listeria species in three environmental ecosystems. Applied and environmental microbiology, 80, 5583-5592. doi:10.1128/AEM.01018-14 DOI: https://doi.org/10.1128/AEM.01018-14
  22. Luchansky, J. B., Chen, Y., Porto-Fett, A. C. S., Pouillot, R., Shoyer, B. A., Johnson-DeRycke, R., et al. (2017). Survey for Listeria monocytogenes in and on Ready-to-Eat Foods from Retail Establishments in the United States (2010 through 2013): Assessing Potential Changes of Pathogen Prevalence and Levels in a Decade. J Food Prot, 80, 903-921. doi:10.4315/0362-028x.Jfp-16-420 DOI: https://doi.org/10.4315/0362-028X.JFP-16-420
  23. Martin, B., Perich, A., Gomez, D., Yanguela, J., Rodriguez, A., Garriga, M., et al. (2014). Diversity and distribution of Listeria monocytogenes in meat processing plants. Food Microbiol, 44, 119-127. doi:10.1016/j.fm.2014.05.014 DOI: https://doi.org/10.1016/j.fm.2014.05.014
  24. Maury, M. M., Tsai, Y.-H., Charlier, C., Touchon, M., Chenal-Francisque, V., Leclercq, A., et al. (2016). Uncovering Listeria monocytogenes hypervirulence by harnessing its biodiversity. Nature genetics, 48, 308-313. doi:10.1038/ng.3501 DOI: https://doi.org/10.1038/ng.3501
  25. Mohammed, H. O., Atwill, E., Dunbar, L., Ward, T., McDonough, P., Gonzalez, R., et al. (2010). The risk of Listeria monocytogenes infection in beef cattle operations. J Appl Microbiol, 108, 349-356. doi:10.1111/j.1365-2672.2009.04446.x DOI: https://doi.org/10.1111/j.1365-2672.2009.04446.x
  26. Ngo Chung Thuy, Patin, A., Truong Thi Giang, Pham Thi Ngoc, Tran Thi Hanh, & Le Bas, C. (2008). Occurrence of listeria monocytogenes in retail pork meat in Vietnam. Paper presented at the Proceedings of the PRISE Scientific Committee, Hanoi, Viet Nam.
  27. Oxaran, V., Lee, S. H. I., Chaul, L. T., Corassin, C. H., Barancelli, G. V., Alves, V. F., et al. (2017). Listeria monocytogenes incidence changes and diversity in some Brazilian dairy industries and retail products. Food Microbiol, 68, 16-23. doi:https://doi.org/10.1016/j.fm.2017.06.012 DOI: https://doi.org/10.1016/j.fm.2017.06.012
  28. Pohlert, T. (2015). trend: Non-Parametric Trend Tests and Change-Point Detection, R package version 0.0.1.
  29. Ragon, M., Wirth, T., Hollandt, F., Lavenir, R., Lecuit, M., Le Monnier, A., et al. (2008). A New Perspective on Listeria monocytogenes Evolution. PLOS Pathogens, 4, e1000146. doi:10.1371/journal.ppat.1000146 DOI: https://doi.org/10.1371/journal.ppat.1000146
  30. Rivoal, K., Queguiner, S., Boscher, E., Bougeard, S., Ermel, G., Salvat, G., et al. (2010). Detection of Listeria monocytogenes in raw and pasteurized liquid whole eggs and characterization by PFGE. Int J Food Microbiol, 138, 56-62. doi:10.1016/j.ijfoodmicro.2010.01.013 DOI: https://doi.org/10.1016/j.ijfoodmicro.2010.01.013
  31. Rogalla, D., & Bomar, P. (2019). Listeria Monocytogenes. Retrieved from https://www.ncbi.nlm.nih.gov/books/NBK534838/
  32. Sauders, B. D., Overdevest, J., Fortes, E., Windham, K., Schukken, Y., Lembo, A., et al. (2012). Diversity of Listeria species in urban and natural environments. Appl Environ Microbiol, 78, 4420-4433. doi:10.1128/aem.00282-12 DOI: https://doi.org/10.1128/AEM.00282-12
  33. Schlech, W. F., 3rd. (2000). Foodborne listeriosis. Clin Infect Dis, 31, 770-775. doi:10.1086/314008 DOI: https://doi.org/10.1086/314008
  34. Shimojima, Y., Ida, M., Nakama, A., Nishino, Y., Fukui, R., Kuroda, S., et al. (2016). Prevalence and contamination levels of listeria monocytogenes in ready-to-eat foods in Tokyo, Japan. The Journal of veterinary medical science, 78, 1183-1187. doi:10.1292/jvms.15-0708 DOI: https://doi.org/10.1292/jvms.15-0708
  35. Stonsaovapak, S., & Boonyaratanakornkit, M. (2010). PREVALENCE AND ANTIMICROBIAL RESISTANCE OF LISTERIA SPECIES IN FOOD PRODUCTS IN BANGKOK, THAILAND. 30, 154-161. doi:10.1111/j.1745-4565.2009.00197.x DOI: https://doi.org/10.1111/j.1745-4565.2009.00197.x
  36. Szczawiński, J., Ewa Szczawińska, M., Łobacz, A., Tracz, M., & Jackowska-Tracz, A. (2017). Modelling the Growth Rate of Listeria Monocytogenes in Cooked Ham Stored at Different Temperatures. Journal of veterinary research, 61, 45-51. doi:10.1515/jvetres-2017-0006 DOI: https://doi.org/10.1515/jvetres-2017-0006
  37. Tabit, F. (2018). Contamination, Prevention and Control of Listeria monocytogenes in Food Processing and Food Service Environments. In: Nyila M.A. eds. Listeria Monocytogenes. IntechOpen.
  38. Thuc, N. M., Hung, T. M., Le, T. T., & Anh, T. K. (2008). Primary investigation of Listeria monocytogenes infection in foods in Hanoi market using polymerase chain reaction. Vietnam Journal of Science and Technology, 46, 67-77.
  39. Uhlich, G. A., Luchansky, J. B., Tamplin, M. L., Molina-Corral, F. J., Anandan, S., & Porto-Fett, A. C. S. (2006). Effect of storage temperature on the growth of Listeria Monocytogenes on Queso Blanco slices*. 26, 202-214. doi:10.1111/j.1745-4565.2006.00043.x DOI: https://doi.org/10.1111/j.1745-4565.2006.00043.x
  40. Véghová, A., Minarovičová, J., Koreňová, J., Drahovská, H., & Kaclíková, E. (2017). Prevalence and tracing of persistent Listeria monocytogenes strains in meat processing facility production chain. Journal of Food Safety, 37(2), e12315. doi:10.1111/jfs.12315 DOI: https://doi.org/10.1111/jfs.12315
  41. Walker, S. J., Archer, P., & Banks, J. G. (1990). Growth of Listeria monocytogenes at refrigeration temperatures. J Appl Bacteriol, 68, 157-162. doi:10.1111/j.1365-2672.1990.tb02561.x DOI: https://doi.org/10.1111/j.1365-2672.1990.tb02561.x
  42. Wang, H., Luo, L., Zhang, Z., Deng, J., Wang, Y., Miao, Y., et al. (2018). Prevalence and molecular characteristics of Listeria monocytogenes in cooked products and its comparison with isolates from listeriosis cases. Front Med, 12, 104-112. doi:10.1007/s11684-017-0593-9 DOI: https://doi.org/10.1007/s11684-017-0593-9
  43. WHO, World Health Organization (2019). Listeriosis– Spain. Retrieved from https://www.who.int/csr/don/16-september-2019-listeriosis-spain/en/
  44. Wu, S., Wu, Q., Zhang, J., Chen, M., & Guo, W. (2016). Analysis of Multilocus Sequence Typing and Virulence Characterization of Listeria monocytogenes Isolates from Chinese Retail Ready-to-Eat Food. Frontiers in microbiology, 7, 168-168. doi: 10.3389/fmicb.2016.00168 DOI: https://doi.org/10.3389/fmicb.2016.00168
  45. Xuan Binh, D., Minh, N., & Thi Nguyet, D. (2017). Prevalence of Listeria monocytogenes, E. coli, Salmonella Spp. and Staphylococcus aureus Bacteria Contamination on Meat at Public Market in the North of Vietnam (Vol. 5).
  46. Zhang, X., Niu, Y., Liu, Y., Lu, Z., Wang, D., Cui, X., et al. (2019). Isolation and Characterization of Clinical Listeria monocytogenes in Beijing, China, 2014–2016. 10. doi: 10.3389/fmicb.2019.00981 DOI: https://doi.org/10.3389/fmicb.2019.00981

Metrics

Citations and online attention from Dimensions, Altmetric and PlumX.

PlumX Metrics

License

PAGEPress has chosen to apply the Creative Commons Attribution NonCommercial 4.0 International License (CC BY-NC 4.0) to all manuscripts to be published.