Prevalence of Listeria monocytogenes in dairy products in Turkey: A Meta-Analysis

Year 2023, Volume: 8 Issue: 3, 212 - 218, 31.12.2023

Berna Yanmaz

https://doi.org/10.24880/maeuvfd.1356384

Abstract

This study was aimed to conduct a meta-analysis to determine the seroprevalence of Listeria monocytogenes in dairy products in Turkey. A systematic literature search was conducted using the Medline/PubMed, Science Direct, Web of Science, and Scopus databases to identify studies reporting the seroprevalence of L. monocytogenes in dairy products. The search was conducted using the following keywords: (“ice cream” or “curd” or “cream” or “cheese” or “butter” or “yoğurt” or “dairy” or “milk”) and (“Listeriosis” or “Listeria monocytogenes” or “Listeria”) and (“Turkiye” or “Turkey”) and (“seropositivity” or “seroprevalence” or “prevalence”). A comprehensive meta-analysis included a total of 4766 dairy products from the 27 studies. The overall molecular prevalence of Listeria monocytogenes in dairy products in Turkey was estimated to be 7.4% (95% confidence interval [CI]: 4.7-10.7%). The I2 value of 93.5% (CI95%91.6–95.0) suggested high heterogeneity, with a τ2 of 3.4422 (CI95%-1.7091–8.5936), and an X2 statistic of 399.2 (P < 0.0001). In conclusion, this meta-analysis reveals a significant seroprevalence of L. monocytogenes in dairy products in Turkey. The findings highlight the need for improved control measures to minimize the risk of contamination and ensure consumer safety. By implementing rigorous hygiene practices, enhancing monitoring systems, and promoting collaborative efforts between industry and regulatory bodies, the dairy sector in Turkey can effectively mitigate the risks associated with L. monocytogenes and maintain high standards of food safety.

Keywords

cheese, dairy, milk, prevalence

Ethical Statement

not necessary

Thanks

Not applicable

References

• Abay, S., Aydin, F., & Sumerkan, A. B. (2012). Molecular typing of Listeria spp. isolated from different sources. Ankara Üniversitesi Veteriner Fakültesi Dergisi, 59(3), 183-190.
• Akin, A. C., Arikan, M. S., Polat, M., Mat, B., Cevrimli, M. B., Demirsöz, M., & Tekindal, M. A. (2022). Examining the production amount of milk and dairy products using network analysis in Turkey. Food Science and Technology, 42, e125821. https://doi.org/10.1590/fst.125821
• Aksoy, A., Sezer, Ç., Vatansever, L., & Gülbaz, G. (2018). Presence and antibiotic resistance of Listeria monocytogenes in raw milk and dairy products. Kafkas Üniversitesi Veteriner Fakültesi Dergisi, 24(3), 415-421. https://doi.org/10.9775/kvfd.2017.19081
• Andersson, C., Gripenland, J., & Johansson, J. (2015). Using the chicken embryo to assess virulence of Listeria monocytogenes and to model other microbial infections. Nature Protocols, 10: 1155–1164. https://doi.org/10.1038/nprot.2015.073
• Arslan, S., & Ozdemir, 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(4), fnaa006. https://doi.org/10.1093/femsle/fnaa006
• Arslan, S., & Ozdemir, F. (2008). Prevalence and antimicrobial resistance of Listeria spp. in homemade white cheese. Food control, 19(4), 360-363. https://doi.org/10.1016/j.foodcont.2007.04.009.
• Aydın, R., Gökmen, M., Kara, R., Önen, A., & Ektik, N. (2019). The prevalence and molecular characterization of Listeria monocytogenes in corn silage, feces and bulk tank milk samples in dairy cattle farms in Balikesir, Turkey. Israel Journal of Veterinary Medicine, 74(4): 184-189.
• Aygun, O., & Pehlivanlar, S. (2006). Listeria spp. in the raw milk and dairy products in Antakya, Turkey. Food Control, 17(8), 676-679. https://doi.org/10.1016/j.foodcont.2005.09.014.
• Babacan, O. (2020). Antibiotic susceptibility and phylogenetic analyses for the origins and serotypes of Listeria monocytogenes strains isolated from ice cream and cream cakes. Turkish Journal of Veterinary & Animal Sciences, 44(5), 1100-1109. https://doi.org/10.3906/vet-2003-116
• Bor, Ö. (2014). Economics of Dairy Farming in Turkey, International Journal of Food and Agricultural Economics, 2: 49-62. https://doi.org/10.22004/ag.econ.190811.
• Borenstein, M., Hedges, L. V., Higgins, J. P., & Rothstein, H. R. (2021). Introduction to meta-analysis. John Wiley & Sons.
• Bouras, E., Tsilidis, K. K., Pounis, G., & Haidich, A. B. (2019). Meta-analysis of nutrition studies. Analysis in nutrition research, 163-196. https://doi.org/10.1016/B978-0-12-814556-2.00007-5
• Cagri-Mehmetoglu, A., Yaldirak, G., Bodur, T., Simsek, M., Bozkir, H., & Eren, N. M. (2011). Incidence of Listeria monocytogenes and Escherichia coli O157: H7 in two Kasar Cheese processing environments. Food Control, 22(5), 762-766. https://doi.org/10.1016/j.foodcont.2010.11.011
• Cetinkaya, F., Elal Mus, T., Yibar, A., Guclu, N., Tavsanli, H., & Cibik, R. (2014). Prevalence, serotype identification by multiplex polymerase chain reaction and antimicrobial resistance patterns of Listeria monocytogenes isolated from retail foods. Journal of food safety, 34(1), 42-49. https://doi.org/10.1111/jfs.12093
• Cetinkaya, F., & Soyutemiz, G. E. (2007). Evaluation of Listeria monocytogenes populations during the manufacture and vacuum-packaged storage of kashar cheese. Acta Veterinaria Brno, 76(1), 143-148. https://doi.org/10.2754/avb200776010143
• Cokal, Y., Dagdelen, A., Cenet, O., & Gunsen, U. (2012). Presence of L. monocytogenes and some bacterial pathogens in two Turkish traditional foods, Mihalic cheese and Hosmerim dessert. Food Control, 26(2), 337-340. https://doi.org/10.1016/j.foodcont.2012.01.058
• Colak, H., Hampikyan, H., Bingol, E. B., & Ulusoy, B. (2007). Prevalence of L. monocytogenes and Salmonella spp. in tulum cheese. Food Control, 18(5), 576-579. https://doi.org/10.1016/j.foodcont.2006.02.004
• Cossart, P. (2011). Illuminating the landscape of host–pathogen interactions with the bacterium Listeria monocytogenes. Proceedings of the National Academy of Sciences, United States of America, 108(49), 19484–19491. https://doi.org/10.1073/pnas.1112371108
• Durmaz, H., Avci, M., & Aygün, O. (2015). The presence of Listeria species in corn silage and raw milk produced in Southeast Region of Turkey. Kafkas Üniversitesi Veteriner Fakültesi Dergisi, 21(1), 41-44. https://doi.org/10.9775/kvfd.2014.11664
• Egger, M., Smith, G. D., Schneider, M., & Minder, C. (1997) Bias in meta- analysis detected by a simple, graphical test. BMJ, 315(7109), pp. 629-634. https://doi.org/10.1136/bmj.315.7109.629
• Ekici, G., Dümen, E., Bayrakal, G. M., & Ergin, S. (2019). Molecular identification of Listeria monocytogenes and Escherichia coli O157: H7 isolated from fresh kashar cheese and milk creme. Kafkas Üniversitesi Veteriner Fakültesi Dergisi, 25(2), 215-219. https://doi.org/10.9775/kvfd.2018.20702
• Falardeau, J., Trmčić, A., & Wang, S. (2021). The occurrence, growth, and biocontrol of Listeria monocytogenes in fresh and surface‐ripened soft and semisoft cheeses. Comprehensive Reviews in Food Science and Food Safety, 20(4), 4019-4048. https://doi.org/10.1111/1541-4337.12768
• Gulel, G. T., Gucukoglu, A., Cadirci, O., Saka, E., & Alisarli, M. (2020). Serotyping and antibiotic resistance of Listeria monocytogenes isolated from raw water buffalo milk and milk products. Journal of Food Science, 85(9), 2889-2895. https://doi.org/10.1111/1750-3841.15376
• Guner, A., & Telli, N. (2011). A survey on the presence of Listeria monocytogenes in various semi-hard cheeses from different regions of Turkey. Journal of Animal and Veterinary Advances, 10(14), 1890-4. https://doi.org/10.3923/javaa.2011.1890.1894
• Jiang, X., Jiang, C., Yu, T., Jiang, X., Kang, R., Ren, S., Chen, H., Zhang, Y., Li, Y., Meng, H., & Wang, H. (2022). Phenyllactic acid application to control Listeria monocytogenes biofilms and its growth in milk and spiced beef. International Journal of Food Microbiology, 381, 109910. https://doi.org/10.1016/j.ijfoodmicro.2022.109910
• Kahraman, T., Ozmen, G., Ozinan, B., & Omer Goksoy, E. (2010). Prevalence of Salmonella spp. and Listeria monocytogenes in different cheese types produced in Turkey. British Food Journal, 112(11), 1230-1236. https://doi.org/10.1108/00070701011088214
• Karadal, F., & Yildirim, Y. (2014). Antimicrobial susceptibility and serotype distribution of Listeria monocytogenes isolates obtained from raw milk cheese samples sold in Nigde. Ankara Üniversitesi Veteriner Fakültesi Dergisi, 61(4), 255-260. https://doi.org/10.1501/Vetfak_0000002639
• Kelley, G. A., & Kelley, K. S. (2019). Systematic reviews and meta-analysis in nutrition research. British Journal of Nutrition, 122(11), 1279-1294. https://doi.org/10.1017/S0007114519002241
• Kevenk, T. O., & Gulel, G. T. (2016). Prevalence, antimicrobial resistance and serotype distribution of Listeria monocytogenes isolated from raw milk and dairy products. Journal of Food Safety, 36(1), 11-18. https://doi.org/10.1111/jfs.12208
• Kevenk, T. O., & Koluman, A. (2022). Seasonal effect on L. monocytogenes prevalence in meat and dairy products assessed by VIDAS LMO2 and ISO 11290: 1 methods. International Food Research Journal 29(4), 929 – 936. https:/dx.doi.org/10.47836/ifrj.29.4.20
• Lee, Y. H. (2019). Strengths and limitations of meta-analysis. The Korean Journal of Medicine, 94(5), 391-395. https://doi.org/10.3904/kjm.2019.94.5.391
• Matyar, F., Guzeldag, G., & Mercimek, H. A. (2010). Multiple antibiotic resistance among Listeria monocytogenes in retail foods, in Adana, Turkey. Italian Journal of Food Science, 22(4), 467-472.
• Mazaheri, T., Cervantes-Huamán, B. R., Bermúdez-Capdevila, M., Ripolles-Avila, C., & Rodríguez-Jerez, J. J. (2021). Listeria monocytogenes biofilms in the food industry: is the current hygiene program sufficient to combat the persistence of the pathogen? Microorganisms, 9(1), 181. https://doi.org/10.3390/microorganisms9010181
• Moher, D., Liberati, A., Tetzlaff, J., Altman, D. G., & Prisma Group, T. (2009). Preferred reporting items for systematic reviews and meta-analyses: the Prisma statement. Annals of internal medicine, 151(4), 264-269. https://doi.org/10.7326/0003-4819-151-4-200908180-00135
• Nardi, V. A. M., Teixeira, R., Ladeira, W. J., & de Oliveira Santini, F. (2020). A meta-analytic review of food safety risk perception. Food Control, 112, 107089. https://doi.org/10.1016/j.foodcont.2020.107089
• Ntuli, V., Sibanda, T., Elegbeleye, J. A., Mugadza, D. T., Seifu, E., & Buys, E. M. (2023). Dairy production: microbial safety of raw milk and processed milk products. In Present Knowledge in Food Safety (pp. 439-454). Academic Press.
• Oktem, A. B., Bayram, G., Ceylan, A. E., & Yentur, G. (2006). Prevalence of Listeria monocytogenes in some Turkish foodstuffs. Journal of food quality, 29(1), 76-86. https://doi.org/10.1111/j.1745-4557.2006.00057.x
• Ramaswarmy, V., Cresence, V. M., Rejitha, J. S., Lekshmi, M. U., Dharsana, K. S., Prasad, S. P. & Vijila, H. M. (2007). Listeria–review of epidemiology and pathogenesis. Journal of Microbiology Immunology and Infection, 40(1), 4–13.
• Ricci, A., Allende, A., Bolton, D., Chemaly, M., Davies, R., Fernández Escámez, P.S., Girones, R., Herman, L., Koutsoumanis, K., Nørrung, B., Robertson, L., Ru, G., Sanaa, M., Simmons, M., Skandamis, P., Snary, E., Speybroeck, N., Ter Kuile, B., Threlfall, J.,… Lindqvist, R. (2018) Listeria monocytogenes contamination of ready-to-eat foods and the risk for human health in the EU. EFSA Panel on Biological Hazards (Biohaz). EFSA Journal, 16:1–173. https://doi.org/10.2903/j.efsa.2018.5134
• Sagun, E., Sancak, Y. C., İsleyici, Ö., & Ekici, K. (2001). The presence and prevalence of Listeria species in milk and herby cheese in and around Van. Turkish Journal of Veterinary & Animal Sciences, 25(1), 15-19.
• Sanlıbaba, P., Tezel, B. U., & Cakmak, G. A. (2018). Detection of Listeria spp. in raw milk and dairy products retailed in Ankara. Gıda, 43(2), 273-282. https://doi.org/10.15237/gida.GD17107
• Tasci, F., Turutoglu, H., & Ogutcu, H. (2010). Investigations of Listeria species in milk and silage produced in Burdur province. Kafkas Üniversitesi Veteriner Fakültesi Dergisi, 16: 93-97.
• Turhan, U. E. (2019). The presence of pathogenic bacteria in traditional cheese sold in local market in Hatay province, Turkey. Applied Ecology and Environmental Research, 17(3), 7135-45. http://dx.doi.org/10.15666/aeer/1703_71357145
• Türkiye İstatistik Kurumu. Hayvancılık İstatistikleri Veri Tabanı (2022). Çiğ süt üretim istatistikleri. https://data.tuik.gov.tr/Bulten/Index?p=Cig-Sut-Uretim-Istatistikleri-2020-2021-45861.
• Ulusoy, B. H., & Chirkena, K. (2019). Two perspectives of Listeria monocytogenes hazards in dairy products: the prevalence and the antibiotic resistance, Food Quality and Safety, 3(4), 233–241. https://doi.org/10.1093/fqsafe/fyz035
• Wang, N. (2018). Conducting meta-analyses of proportions in R. Research Gate: College Station, TX, USA. World health Organization, WHO. (2018). Listeriosis, 20 February, 2018. https://www.who.int/news-room/fact-sheets/detail/listeriosis (Accessed 26 June 2023).
• Yonar, H., Yonar, A., Mishra, P., Abotaleb, M., Al Khatib, A. M. G., Makarovskikh, T., & Cam, M. (2022). Modeling and forecasting of milk production in different breeds in Turkey. Indian Journal of Animal Sciences, 92(1), 105-111.
• Yigin, A., Kılıc Altun, S., Demirci, M., Eser, N., & Yoldas, A. (2020). Utilization of real-time PCR method for identification of Listeria spp. from homemade white cheese originating from Southeast of Turkey. Applied Ecology and Environmental Research, 18(4), 5673-5682. http://dx.doi.org/10.15666/aeer/1804_56735682