Volume 10, Issue 2 (June 2023)                   J. Food Qual. Hazards Control 2023, 10(2): 103-112 | Back to browse issues page


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Raeisi M, Afshari A, Shirzad-Aski H, Seifi S, Hashemi M, Khoshbakht R, et al . The Occurrence of Serotypes and Virulence Genes of Listeria monocytogenes in Various Food Products. J. Food Qual. Hazards Control 2023; 10 (2) :103-112
URL: http://jfqhc.ssu.ac.ir/article-1-924-en.html
Toxicology Research Center, Medical Basic Sciences Research Institute, Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran, Department of Nutrition, School of Allied Medical Sciences, Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran , sma.noori@gmail.com
Abstract:   (512 Views)
Background: Given that controlling Listeria contamination is very important in food chain system, the knowledge of their prevalence in food is very important. Therefore, this study aims to examine the prevalence of important Listeria species in various food types and evaluate serotype distribution, as well as the study of the virulence factors of L. monocytogenes.
Methods: During July 2018 and January 2020, 900 food samples were collected in the North of Iran, including beef, chicken, fish, shrimp, milk and yogurt, green vegetables, mixed vegetable salad, Olivier salad, and cottage cheese. After isolation and identification steps, each bacterial DNA was extracted. Then, using specific primers, species, serotypes, and virulence genes of Listeria isolates were evaluated in the samples by Polymerase Chain Reaction (PCR) method.
Results: The test results of 136 samples (15.1%) were positive for Listeria spp. and the most contaminated food was beef (35%) followed by chicken (29%) and green vegetables (23%). The most isolated Listeria spp. was L. monocytogenes and L. ivanovii. Among L. monocytogenes isolates, the dominant serogroups were 1/2a and 4b; furthermore, all of the isolates of this species harbored four virulence genes, including hlyA, plc, iap, and actA.
Conclusion: These reports highlighted the importance of food safety in various food products, particularly raw meats and vegetables. Moreover, contamination of healthy foods such as fish and vegetables with Listeria is an indicator of public health.

DOI: 10.18502/jfqhc.10.2.12673
Full-Text [PDF 562 kb]   (353 Downloads)    
Type of Study: Original article | Subject: Special
Received: 21/08/10 | Accepted: 22/09/25 | Published: 23/06/28

References
1. Acciari V.A., Torresi M., Iannetti L., Scattolini S., Pomilio F., Decastelli L., Colmegna S., Muliari R., Bossù T., Proroga Y., Montagna C., Cardamone C., et al. (2017). Listeria monocytogenes in smoked salmon and other smoked fish at retail in Italy: frequency of contamination and strain characterization in products from different manufacturers. Journal of Food Protection. 80: 271-278. [DOI: 10.4315/0362-028X.JFP-15-599] [DOI:10.4315/0362-028X.JFP-15-599] [PMID]
2. Al S., Disli H.B., Hizlisoy H., Onmaz N.E., Yildirim Y., Gonulalan Z. (2022). Prevalence and molecular characterization of Listeria monocytogenes isolated from wastewater of cattle slaughterhouses in Turkey. Journal of Applied Microbiology. 132: 1518-1525. [DOI: 10.1111/jam.15261] [DOI:10.1111/jam.15261] [PMID]
3. Amajoud N., Leclercq A., Soriano J.M., Bracq-Dieye H., El Maadoudi M., Senhaji N.S., Kounnoun A., Moura A., Lecuit M., Abrini J. (2018). Prevalence of Listeria spp. and characterization of Listeria monocytogenes isolated from food products in Tetouan, Morocco. Food Control. 84: 436-441. [DOI: 10.1016/j.foodcont.2017.08.023] [DOI:10.1016/j.foodcont.2017.08.023]
4. Arslan S., Özdemir F. (2020). Prevalence and antimicrobial resistance of Listeria species and molecular characterization of Listeria monocytogenes isolated from retail ready-to-eat foods. FEMS Microbiology Letters. 367. [DOI: 10.1093/femsle/fnaa006] [DOI:10.1093/femsle/fnaa006] [PMID]
5. Benkerroum N., Oubel H., Sandine W.E. (2003). Effect of nisin on yogurt starter, and on growth and survival of Listeria monocytogenes during fermentation and storage of yogurt. International Journal of Food Safety. 1: 1-5.
6. Centers for Disease Control and Prevention (CDC). (2020). Listeria (Listeriosis). URL: https://www.cdc.gov/ Listeria.
7. 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: 10.1016/j.foodcont.2015.08.019] [DOI:10.1016/j.foodcont.2015.08.019]
8. Doumith M., Buchrieser C., Glaser P., Jacquet C., Martin P. (2004). Differentiation of the major Listeria monocytogenes serovars by multiplex PCR. Journal of Clinical Microbiology. 42: 3819-3822. [DOI: 10.1128/jcm.42.8.3819-3822.2004] [DOI:10.1128/JCM.42.8.3819-3822.2004] [PMID] [PMCID]
9. Du X.-J., Zhang X., Wang X.-Y., Su Y.-L., Li P., Wang S. (2017). Isolation and characterization of Listeria monocytogenes in Chinese food obtained from the central area of China. Food Control. 74: 9-16. [DOI: 10.1016/j.foodcont.2016.11.024] [DOI:10.1016/j.foodcont.2016.11.024]
10. El Hag M.M.A., El Zubeir I.E.M., Mustafa N.E.M. (2021). Prevalence of Listeria species in dairy farms in Khartoumstate (Sudan). Food Control. 123: 107699. [DOI: 10.1016/j.foodcont.2020.107699] [DOI:10.1016/j.foodcont.2020.107699]
11. European Food Safety Authority (EFSA)., European Centre for Disease Prevention and Control (ECDC). (2015). The European :union: summary report on trends and sources of zoonoses, zoonotic agents and food‐borne outbreaks in 2013. EFSA Journal. 13: 3991. [DOI: 10.2903/j.efsa.2015.3991] [DOI:10.2903/j.efsa.2015.3991]
12. Fallah A.A., Saei-Dehkordi S.S., Mahzounieh M. (2013). Occurrence and antibiotic resistance profiles of Listeria monocytogenes isolated from seafood products and market and processing environments in Iran. Food control. 34: 630-636. [DOI: 10.1016/j.foodcont.2013.06.015] [DOI:10.1016/j.foodcont.2013.06.015]
13. 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:10.1111/j.1365-2672.1991.tb02951.x] [PMID]
14. Indrawattana N., Nibaddhasobon T., Sookrung N., Chongsa-Nguan M., Tungtrongchitr A., Makino S.-I., Tungyong W., Chaicumpa W. (2011). Prevalence of Listeria monocytogenes in raw meats marketed in Bangkok and characterization of the isolates by phenotypic and molecular methods. Journal of Health, Population, and Nutrition. 29: 26-38. [DOI: 10.3329/jhpn.v29i1.7565] [DOI:10.3329/jhpn.v29i1.7565] [PMID] [PMCID]
15. International Standardization Organization (ISO) 11290-1. (1996). Microbiology of food and animal feeding stuffs-horizontal method for the detection and enumeration of Listeria monocytogenes-part 1: detection method. URL: https://www.iso.org/standard/ 19268.html.
16. Jalali M., Abedi D. (2008). Prevalence of Listeria species in food products in Isfahan, Iran. International Journal of Food Microbiology. 122: 336-340. [DOI: 10.1016/j.ijfoodmicro.2007.11.082] [DOI:10.1016/j.ijfoodmicro.2007.11.082] [PMID]
17. Koskar J., Kramarenko T., Meremäe K., Kuningas M., Sõgel J., Mäesaar M., Anton D., Lillenberg M., Roasto M. (2019). Prevalence and numbers of Listeria monocytogenes in various ready-to-eat foods over a 5-year period in Estonia. Journal of Food Protection. 82: 597-604. [DOI: 10.4315/0362-028X.JFP-18-383] [DOI:10.4315/0362-028X.JFP-18-383] [PMID]
18. Kramarenko T., Roasto M., Meremäe K., Kuningas M., Põltsama P., Elias T. (2013). Listeria monocytogenes prevalence and serotype diversity in various foods. Food Control. 30: 24-29. [DOI: 10.1016/j. foodcont.2012.06.047] [DOI:10.1016/j.foodcont.2012.06.047]
19. Little C.L., Taylor F.C., Sagoo S.K., Gillespie I.A., Grant K., McLauchlin J. (2007). Prevalence and level of Listeria monocytogenes and other Listeria species in retail pre-packaged mixed vegetable salads in the UK. Food Microbiology. 24: 711-717. [DOI: 10.1016/ j.fm.2007.03.009] [DOI:10.1016/j.fm.2007.03.009]
20. Liu D. (2006). Identification, subtyping and virulence determination of Listeria monocytogenes, an important foodborne pathogen. Journal of Medical Microbiology. 55: 645-659. [DOI: 10.1099/jmm.0.46495-0] [DOI:10.1099/jmm.0.46495-0] [PMID]
21. Lotfollahi L., Chaharbalesh A., Rezaee M.A., Hasani A. (2017). Prevalence, antimicrobial susceptibility and multiplex PCR-serotyping of Listeria monocytogenes isolated from humans, foods and livestock in Iran. Microbial Pathogenesis. 107: 425-429. [DOI: 10.1016/j.micpath.2017.04.029] [DOI:10.1016/j.micpath.2017.04.029] [PMID]
22. Mena C., Almeida G., Carneiro L., Teixeira P., Hogg T., Gibbs P.A. (2004). Incidence of Listeria monocytogenes in different food products commercialized in Portugal. Food Microbiology. 21: 213-216. [DOI: 10.1016/S0740-0020(03)00057-1] [DOI:10.1016/S0740-0020(03)00057-1]
23. Mohajer F., Khanzadi S., Keykhosravy K., Noori S.M.A., Azizzadeh M., Hashemi M. (2021). Impact of gelatin nanogel coating containing thymol and nisin on the microbial quality of rainbow trout fillets and the inoculated Listeria monocytogenes. Aquaculture Research. 52: 3958-3965. [DOI: 10.1111/are.15239] [DOI:10.1111/are.15239]
24. Momtaz H., Yadollahi S. (2013). Molecular characterization of Listeria monocytogenes isolated from fresh seafood samples in Iran. Diagnostic Pathology. 8: 149. [DOI:10.1186/1746-1596-8-149] [PMID] [PMCID]
25. Nightingale K.K., Schukken Y.H., Nightingale C.R., Fortes E.D., Ho A.J., Her Z., Grohn Y.T., McDonough P.L., Wiedmann M. (2004). Ecology and transmission of Listeria monocytogenes infecting ruminants and in the farm environment. Applied and Environmental Microbiology. 70: 4458-4467. [DOI: 10.1128/AEM.70.8.4458-4467.2004] [DOI:10.1128/AEM.70.8.4458-4467.2004] [PMID] [PMCID]
26. Notermans S.H., Dufrenne J., Leimeister-WäChter M., Domann E., Chakraborty T. (1991). Phosphatidylinositol-specific phospholipase C activity as a marker to distinguish between pathogenic and nonpathogenic Listeria species. Applied and Environmental Microbiology. 57: 2666-2670. [DOI: 10.1128/aem.57.9.2666-2670.1991] [DOI:10.1128/aem.57.9.2666-2670.1991] [PMID] [PMCID]
27. Nüesch-Inderbinen M., Bloemberg G.V., Müller A., Stevens M.J.A., Cernela N., Kollöffel B., Stephan R. (2021). Listeriosis caused by persistence of Listeria monocytogenes serotype 4b sequence type 6 in cheese production environment. Emerging Infectious Diseases. 27: 284-288. [DOI: 10.3201/eid2701.203266] [DOI:10.3201/eid2701.203266] [PMID] [PMCID]
28. Oliveira M., Usall J., Viñas I., Solsona C., Abadias M. (2011). Transfer of Listeria innocua from contaminated compost and irrigation water to lettuce leaves. Food Microbiology. 28: 590-596. [DOI: 10.1016/j.fm.2010.11.004] [DOI:10.1016/j.fm.2010.11.004] [PMID]
29. Osman K.M., Samir A., Orabi A., Zolnikov T.R. (2014). Confirmed low prevalence of Listeria mastitis in she-camel milk delivers a safe, alternative milk for human consumption. Acta Tropica. 130: 1-6. [DOI: 10.1016/j.actatropica.2013.10.001] [DOI:10.1016/j.actatropica.2013.10.001] [PMID]
30. Paziak-Domańska B., Bogusławska E., Więckowska-Szakiel M., Kotłowski R., Różalska B., Chmiela M., Kur J., Dąbrowski W., Rudnicka W. (1999). Evaluation of the API test, phosphatidylinositol-specific phospholipase C activity and PCR method in identification of Listeria monocytogenes in meat foods. FEMS Microbiology Letters. 171: 209-214. [DOI: 10.1111/j.1574-6968.1999.tb13434.x] [DOI:10.1111/j.1574-6968.1999.tb13434.x] [PMID]
31. Raeisi M., Khoshbakht R., Ghaemi E.A., Bayani M., Hashemi M., Seyedghasemi N.S., Shirzad-Aski H. (2017). Antimicrobial resistance and virulence-associated genes of Campylobacter spp. isolated from raw milk, fish, poultry, and red meat. Microbial Drug Resistance. 23: 925-933. [DOI: 10.1089/mdr.2016. 0183] [DOI:10.1089/mdr.2016.0183] [PMID]
32. Rahimi E., Ameri M., Momtaz H. (2010). Prevalence and antimicrobial resistance of Listeria species isolated from milk and dairy products in Iran. Food Control. 21: 1448-1452. [DOI: 10.1016/j.foodcont.2010.03.014] [DOI:10.1016/j.foodcont.2010.03.014]
33. Rawool D.B., Malik S.V.S., Barbuddhe S.B., Shakuntala I., Aurora R. (2007). A multiplex PCR for detection of virulence associated genes in Listeria monocytogenes. International Journal of Food Safety. 9: 56-62.
34. Ryu J., Park S.H., Yeom Y.S., Shrivastav A., Lee S.-H., Kim Y.-R., Kim H.-Y. (2013). Simultaneous detection of Listeria species isolated from meat processed foods using multiplex PCR. Food Control. 32: 659-664. [DOI: 10.1016/j.foodcont.2013.01.048] [DOI:10.1016/j.foodcont.2013.01.048]
35. Shi W., Qingping W., Jumei Z., Moutong C., Zéan Y. (2015). Prevalence, antibiotic resistance and genetic diversity of Listeria monocytogenes isolated from retail ready-to-eat foods in China. Food Control. 47: 340-347. [DOI: 10.1016/j.foodcont.2014.07.028] [DOI:10.1016/j.foodcont.2014.07.028]
36. Snapir Y.M., Vaisbein E., Nassar F. (2006). Low virulence but potentially fatal outcome-Listeria ivanovii. European Journal of Internal Medicine. 17: 286-287. [DOI: 10.1016/j.ejim.2005.12.006] [DOI:10.1016/j.ejim.2005.12.006] [PMID]
37. Suárez M., González-Zorn B., Vega Y., Chico-Calero I., Vázquez-Boland J.-A. (2001). A role for ActA in epithelial cell invasion by Listeria monocytogenes. Cellular Microbiology. 3: 853-864. [DOI: 10.1046/j.1462-5822.2001.00160.x] [DOI:10.1046/j.1462-5822.2001.00160.x] [PMID]
38. Todd E.C.D., Notermans S. (2011). Surveillance of listeriosis and its causative pathogen, Listeria monocytogenes. Food Control. 22: 1484-1490. [DOI: 10.1016/j.foodcont.2010.07.021] [DOI:10.1016/j.foodcont.2010.07.021]
39. Townsend A., Strawn L.K., Chapman B.J., Dunn L.L. (2021). A systematic review of Listeria species and Listeria monocytogenes prevalence, persistence, and diversity throughout the fresh produce supply chain. Foods. 10: 1427. [DOI: 10.3390/foods10061427] [DOI:10.3390/foods10061427] [PMID] [PMCID]
40. Wieczorek K., Osek J. (2017). Prevalence, genetic diversity and antimicrobial resistance of Listeria monocytogenes isolated from fresh and smoked fish in Poland. Food Microbiology. 64: 164-171. [DOI: 10.1016/j.fm.2016.12.022] [DOI:10.1016/j.fm.2016.12.022] [PMID]

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