https://doi.org/10.4081/ijfs.2020.8772

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

Vol. 9 No. 3 (2020)
Submitted: 18 December 2019
Accepted: 5 March 2020
Published: 16 October 2020
Listeria monocytogenes, Ready-to-eat meats, Sausage, Sliced meat, Epidemiology, Multi-locus sequence typing
Abstract Views: 866
PDF: 443
HTML: 29
Publisher's note
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.

Authors

Thuy Phung
School of Biotechnology and Food Technology, Hanoi University of Science and Technology, Hanoi, Viet Nam.
Tung Tran
http://orcid.org/0000-0002-2270-5656
School of Biotechnology and Food Technology, Hanoi University of Science and Technology, Hanoi, Viet Nam.
Dung Pham
School of Biotechnology and Food Technology, Hanoi University of Science and Technology, Hanoi, Viet Nam.
Anh To
School of Biotechnology and Food Technology, Hanoi University of Science and Technology, Hanoi, Viet Nam.
Hoa Le
hoa.lequang@hust.edu.vn
School of Biotechnology and Food Technology, Hanoi University of Science and Technology, Hanoi, Viet Nam.

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.

Dimensions

Altmetric

PlumX Metrics

Downloads

Download data is not yet available.

Citations

Crossref
Scopus
Google Scholar
Europe PMC
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
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
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
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.
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
Center for Disease Control and Prevention, CDC (2019). Listeria Outbreaks. Retrieved from https://www.cdc.gov/listeria/outbreaks/index.html
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
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
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
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
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.
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
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
Elmali, M., Can, H. Y. i., & Yaman, H. (2015). Prevalence of Listeria monocytogenes in poultry meat %J Food Science and Technology. 35, 672-675.
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
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
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
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.
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
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
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
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
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
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
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
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.
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
Pohlert, T. (2015). trend: Non-Parametric Trend Tests and Change-Point Detection, R package version 0.0.1.
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
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
Rogalla, D., & Bomar, P. (2019). Listeria Monocytogenes. Retrieved from https://www.ncbi.nlm.nih.gov/books/NBK534838/
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
Schlech, W. F., 3rd. (2000). Foodborne listeriosis. Clin Infect Dis, 31, 770-775. doi:10.1086/314008 DOI: https://doi.org/10.1086/314008
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
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
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
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.
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.
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
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
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
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
WHO, World Health Organization (2019). Listeriosis– Spain. Retrieved from https://www.who.int/csr/don/16-september-2019-listeriosis-spain/en/
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
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).
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

Supporting Agencies

Hanoi University of Science and Technology

How to Cite

1.
Phung T, Tran T, Pham D, To A, Le H. Occurrence and molecular characteristics of <em>Listeria monocytogenes</em> isolated from ready-to-eat meats in Hanoi, Vietnam. Ital J Food Safety [Internet]. 2020 Oct. 16 [cited 2024 Nov. 21];9(3). Available from: https://www.pagepressjournals.org/ijfs/article/view/8772

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.