METHODS FOR THE IDENTIFICATION OF PATHOGENIC LISTERIA IN FOOD PRODUCTS

Main Article Content

Authors

S.Z. Eskendirova, National Center for Biotechnology

National Center for Biotechnology, 13/5 Korgalzhyn Highway, Astana, 010000, Kazakhstan

G.K. Kaukabayeva

National Center for Biotechnology, 13/5 Korgalzhyn Highway, Astana, 010000, Kazakhstan

S.E. Mukhlis

National Center for Biotechnology, 13/5 Korgalzhyn Highway, Astana, 010000, Kazakhstan

Zh.S. Akhmetkarimova

National Center for Biotechnology, 13/5 Korgalzhyn Highway, Astana, 010000, Kazakhstan

Abstract

Listeriosis is an infectious disease that affects both humans and animals and is caused by Listeria monocytogenes. It is characterized by multiple sources of pathogen entry, a wide range of transmission routes and factors, polymorphic clinical manifestations, and high mortality rates. L. monocytogenes is considered a unique foodborne pathogen due to its intracellular lifecycle and remarkable adaptive capabilities. The pathogenesis of listeriosis is largely driven by the virulence factors of L. monocytogenes, which enable incomplete phagocytosis, intracellular parasitism, rapid host cell invasion, and the development of antibiotic resistance. These virulence determinants act at various stages of the host infection cycle, enhancing the pathogen’s ability to evade immune responses and establish persistent infections. Given the pronounced polymorphism of clinical manifestations and the unique biology of the pathogen, improving laboratory diagnostic methods and developing targeted immunoprophylactic strategies are of paramount importance. This article reviews recent advances in the epizootiology, epidemiology, and pathogenesis of listeriosis. It also highlights key pathogenicity and virulence factors of L. monocytogenes as critical targets for the development of rapid identification techniques in food products. The implementation of modern rapid detection methods significantly reduces analysis time and increases the accuracy of results, even when the pathogen is present in low concentrations within the tested samples.

Keywords

Listeriosis, immunodiagnostics, pathogenesis, virulence, antibodies, pathogen

Article Details

References

Lopes-Luz L., Mendonça M., Bernardes Fogaça M., Kipnis A., Bhunia A.K., Bührer-Sékula S. Listeria monocytogenes: review of pathogenesis and virulence determinants-targeted immunological assays // Crit Rev Microbiol. – 2021. – Vol. 47. – P. 647-666. doi: 10.1080/1040841X.2021.1911930.

Matle I., Mbatha K.R., Madoroba E. A review of Listeria monocytogenes from meat and meat products: Epidemiology, virulence factors, antimicrobial resistance and diagnosis // Onderstepoort J Vet Res. – 2020. – Vol. 87. – Р. 1-20. doi: 10.4102/ojvr.v87i1.1869.

Quereda J.J., Morón-García A., Palacios-Gorba C., Dessaux C., García-Del Portillo F., Pucciarelli M.G., Ortega A.D. Pathogenicity and virulence of Listeria monocytogenes: A trip from environmental to medical microbiology // Virulence. – 2021. – Vol. 12. – P. 2509-2545. doi: 10.1080/21505594.2021.1975526.

Buchanan R.L., Gorris L.G.M., Hayman M.M., Jackson T.C., Whiting R.C. A review of Listeria monocytogenes: an update on outbreaks, virulence, dose-response, ecology, and risk assessments // Food Control. – 2016. – Vol.75. – P. 1-13. doi:10.1016/j.foodcont.2016.12.016.

Ferreira V., Wiedmann M., Teixeira P., Stasiewicz M.J. Listeria monocytogenes persistence in food-associated environments: epidemiology, strain characteristics, and implications for public health // J Food Prot. – 2014. – Vol. 77. – P. 150-170. doi: 10.4315/0362-028X.JFP-13-150.

Lee B.H., Cole S., Badel-Berchoux S., Guillier L., Felix B., Krezdorn N., Hébraud M., Bernardi T., Sultan I., Piveteau P. Biofilm Formation of Listeria monocytogenes Strains Under Food Processing Environments and Pan-Genome-Wide Association Study // Front Microbiol. – 2019. – Vol. 10. – Р. 2698. doi: 10.3389/fmicb.2019.02698.

Radoshevich L., Cossart P. Listeria monocytogenes: towards a complete picture of its physiology and pathogenesis // Nat Rev Microbiol. – 2018. – Vol. 16 – P. 32-46. doi: 10.1038/nrmicro.2017.126.

Roberts B.N., Chakravarty D., Gardner J.C. 3rd, Ricke S.C., Donaldson J.R. Listeria monocytogenes Response to Anaerobic Environments // Pathogens. – 2020. – Vol. 9. – Р.210. doi: 10.3390/pathogens9030210.

Orsi R.H., Bakker H.C, Wiedmann M. Listeria monocytogenes lineages: Genomics, evolution, ecology, and phenotypic characteristics // International Journal of Medical Microbiology. – 2011. – Vol. 301. – P. 79-96. doi: 10.1016/j.ijmm. 2010.05.002.

Kühn S., Enninga J. The actin comet guides the way: How Listeria actin subversion has impacted cell biology, infection biology and structural biology // Cell Microbiol. – 2020. – Vol. 22. – Р. 1-11. doi: 10.1111/cmi.13190.

Kuzembekova G.A., Kirkimbaeva Zh.S., Sarybaeva D.A., Zhylkaidar A.Zh., Murzabaev K.E. Epizootological characteristics of the country's territory for animal listeriosis // Science and education. ZKATU named after Zhangir-Khan. – 2024. – No.3. – P. 247-256. doi: 10.52578/2305-9397-2024-3-1-247-256.

Bai X., Liu D., Xu L., Tenguria S., Drolia R., Gallina N.L.F., Cox A.D., Koo O.K., Bhunia A.K. Biofilm-isolated Listeria monocytogenes exhibits reduced systemic dissemination at the early (12-24 h) stage of infection in a mouse model // NPJ Biofilms Microbiomes. – 2021. – Vol.7. – №.18. – Р. 1-16. doi: 10.1038/s41522-021-00189-5.

Bhunia A.K. Listeria monocytogenes // In: Foodborne Microbial Pathogens. Food Science Text Series: Springer, NY. – 2018. – 229 р. doi.10.1007/978-1-4939-7349-1_13.

Pouillot R., Klontz K. C., Chen Y., Burall L. S., Macarisin D., Doyle M., Bally K. M., Strain E., Datta A. R., Hammack T.S,, Van Doren J.M. Infectious Dose of Listeria monocytogenes in Outbreak Linked to Ice Cream // Emerg Infect Dis. – 2016. – Vol. 12. – P. 2113-2119. doi: 10.3201/eid2212.160165.

Wiktorczyk-Kapischke N., Skowron K., Wałecka-Zacharska E. Genomic and pathogenicity islands of Listeria monocytogenes-overview of selected aspects // Front. Mol. Biosci. – 2023. – Vol. 10. – P. 1161486. doi: 10.3389/fmolb.2023.1161486.

Duma M.N.; Ciupescu L.M.; Dan S.D.; Crisan-Reget O.L.; Tabaran A. Virulence and Antimicrobial Resistance of Listeria monocytogenes Isolated from Ready-to-Eat Food Products in Romania // Microorganisms. – 2024. – Vol. 12 – P. 954. doi:10.3390/microorganisms12050954.

Meireles D., Pombinho R., Cabanes D. Signals behind Listeria monocytogenes virulence mechanisms // Gut Microbes. – 2024. – Vol.16. – №1. – Р. 2369564. doi: 10.1080/19490976.2024.2369564.

Hain T., Ghai R., Billion A., Kuenne, C.T., Steinweg C., Izar B. Comparative genomics and transcriptomics of lineages I, II, and III strains of Listeria monocytogenes // BMC Genomics – 2012. – Vol.13. – P. 144. doi: 10.1186/1471- 2164-13-144.

Drolia R., Tenguria S., Durkes A.C., Turner J.R., Bhunia A.K. Listeria Adhesion Protein Induces Intestinal Epithelial Barrier Dysfunction for Bacterial Translocation // Cell Host Microbe. – 2018. – Vol.23. – P. 470-484. doi: 10.1016/j.chom.2018.03.004.

Drolia R., Bhunia A.K. Crossing the Intestinal Barrier via Listeria Adhesion Protein and Internalin A //Trends Microbiol. – 2019. – Vol.27. – №5. – P. 408-425. doi: 10.1016/j.tim.2018.12.007.

Hurley D., Luque-Sastre L., Parker C.T., Huynh S., Eshwar A.K., Nguyen S.V., Andrews N., Moura A., Fox E.M., Jordan K., Lehner A., Stephan R., Fanning S. Whole-Genome Sequencing-Based Characterization of 100 Listeria monocytogenes Isolates Collected from Food Processing Environments over a Four-Year Period // mSphere. – 2019. – Vol.4. – №4. – Р. 1-14. doi: 10.1128/mSphere.00252-19.

Johansson J., Freitag N.E. Regulation of Listeria monocytogenes Virulence // Microbiol Spectr. – 2019. – Vol. 4. – Р. 1-19. doi: 10.1128/microbiolspec.GPP3-0064-2019.

Gasanov U., Hughes D., Hansbro P.M. Methods for the isolation and identification of Listeria spp. and Listeria monocytogenes: a review // FEMS Microbiol Rev. – 2005. – Vol. 29. – №5. – P. 851-875. doi: 10.1016/j.femsre.2004.12.002.

Leong D., NicAogáin K., Luque-Sastre L., McManamon O., Hunt K., Alvarez- Ordóñez A. 3-year multi-food study of the presence and persistence of Listeria monocytogenes in 54 small food businesses in Ireland // International Journal of Food Microbiology – 2017. – Vol. 249. – P. 18-26. doi:10.1016/j.ijfoodmicro.2017.02.015.

Wang Y., Salazar J.K. Culture-Independent Rapid Detection Methods for Bacterial Pathogens and Toxins in Food Matrices // Compr Rev Food Sci Food Saf. – 2016. – Vol.15. – №.1. – P. 183-205. doi: 10.1111/1541-4337.12175.

Chen J.Q., Healey S., Regan P., Laksanalamai P., Hu Z. PCR-based methodologies for detection and characterization of Listeria monocytogenes and Listeria ivanovii in foods and environmental sources // Food Sci Human Wellness – 2017. – Vol.6. – P. 39-59. doi: 10.1016/j.fshw.2017.03.001.

Ryu J., Park S.H., Yeom Y.S., Shrivastav A., Lee S.H., Kim Y.R. Simultaneous detection of Listeria species isolated from meat processed foods using multiplex PCR // Food Control – 2017. – Vol.32. – P. 659-664. doi: 10.1016/j. foodcont.2013.01.048.

Shaker E.M., Hassanien A.A. PCR Techniques detection of some virulence associated genes in Listeria monocytogenes isolated from table eggs and clinical human samples // Assiut Veterinary Medical Journal – 2015. - Vol.61 – P. 219-225.

Chenal-Francisque V., Maury M.M., Lavina M., Touchon M., Leclercq A., Lecuit, M., Clonogrouping, a rapid multiplex pcr method for identification of major clones of Listeria monocytogenes // Journal of Clinical Microbiology. – 2015. – Vol.53 – P. 3355-3358. doi:10.1128/JCM.00738-15.

Hearty S., Leonard P., Quinn J., O’Kennedy R. Production,characterisation and potential application of a novel monoclonal antibody for rapid identification of virulent Listeria monocytogenes // J Microbiol Methods. – 2015. – Vol.66. – №.2. – P. 294-312. doi: 10.1016/j.mimet.2005.12.009.

Day J.B., Hammack T.S. Immuno-detection and differentiation of Listeria monocytogenes and Listeria ivanovii in stone fruits // J Appl Microbiol. – 2019. – Vol.127. - P. 1848-1858. doi: 10.1111/jam.14440.

Suryawanshi R. D., Malik S. V. S., Jayarao B., Chaudhari S. P., Savage E., Vergis J., Kurkure N. V., Barbuddhe S. B., Rawool D. B. Comparative diagnostic efficacy of recombinant LLO and PI-PLC-based ELISAs for detection of listeriosis in animals // Journal of Microbiological Methods. – 2017. – Vol. 137. – P. 40-45. doi: 10.1016/j.mimet.2017.04.005.

Lathrop A., Bailey T., Kim K., Bhunia A. Pathogen-specific antigen target for production of antibodies produced by comparative genomics // Antibody Technology Journal. – 2014 – Vol.4. – P. 13-22. doi: 10.2147/ANTI.S54848.

Xu L., Bai X., Bhunia AK. Current state of biosensors development and their application in foodborne pathogen detection // J Food Prot. – 2011. – Vol. 84. – P. 1213-1227. doi:10.4315/JFP-20-464.

Etty M.C., D’Auria S., Shankar S., Salmieri S., Coutu J., Baraketi A., Jamshidan M., Fraschini C., Lacroix M. New immobilization method of anti-PepD monoclonal antibodies for the detection of Listeria monocytogenes p60 protein – part A: optimization of a crosslinked film support based on chitosan and cellulose nanocrystals (CNC) // Reactive Functional Polymers. – 2011. – Vol. 146. – P. 104313-104313. doi: 10.1016/j.reactfunctpolym.2019.06.021.

Koo O.K., Aroonnual A., Bhunia A.K. Human heat-shock protein 60 receptor-coated paramagnetic beads show improved capture of Listeria monocytogenes in the presence of other Listeria in food // J Appl Microbiol. – 2011. – Vol. 111 – P. 93-104. doi: 10.1111/j.1365-2672.2011.05040.x.

Tu Z., Chen Q., Li Y., Xiong Y., Xu Y., Hu N., Tao Y. Identification and characterization of species-specific nanobodies for the detection of Listeria monocytogenes in milk // Anal Biochem. – 2016. – Vol. 7. – P. 1-7. doi: 10.1016/j.ab.2015.09.023.

Liu A., Xiong Q., Shen .L, Li W., Zeng Z., Li C., Liu S., Liu Y., Han G. A sandwich-type ELISA for the detection of Listeria monocytogenes using the well-oriented single chain Fv antibody fragment // Food Control. – 2017. – Vol. 79. – P. 156–161. doi:10.1016/j.foodcont.2017.03.042.

Cho I.H., Irudayaraj J. Lateral-flow immunoconcentration for rapid detection of Listeria monocytogenes // Anal Bioanal Chem. – 2013. – Vol. 405. – P. 3313-3319. doi: 10.1007/s00216-013-6742-3.

Du X.J., Zang Y.X., Liu H.B., Li P., Wang S. Recombinase Polymerase Amplification Combined with Lateral Flow Strip for Listeria monocytogenes Detection in Food // J Food Sci. – 2018. – Vol. 83. – P. 1041-1047. doi: 10.1111/1750-3841.14078.

Li F., Li F., Luo D., Lai W., Xiong Y., Xu H. Biotin-exposure-based immunomagnetic separation coupled with nucleic acid lateral flow biosensor for visibly detecting viable Listeria monocytogenes // Anal Chim Acta. – 2018. – Vol. 1017. – P. 48-56. doi: 10.1016/j.aca.2018.02.009

Hahm B.K., Kim H., Singh A.K., Bhunia A.K. Pathogen enrichment device (PED) enables one-step growth, enrichment and separation of pathogen from food matrices for detection using bioanalytical platforms // J Microbiol Methods. – 2015. – Vol.117. – P. 64-73. doi: 10.1016/j.mimet.2015.07.016.

Stambach N.R., Carr S.A., Cox C.R., Voorhees K.J. Rapid Detection of Listeria by Bacteriophage Amplification and SERS-Lateral Flow Immunochromatography // Viruses. – 2015. – Vol.3. – P. 6631-6641. doi: 10.3390/v7122962.

Wu Z. Simultaneous detection of Listeria monocytogenes and Salmonella Typhimurium by a SERS-based lateral flow immunochromatographic assay // Food Anal Methods. – 2025. – Vol.12. – P. 1086-1091. doi: 10.1007/s12161-019-01444-4.

Boerlin P., Boerlin-Petzold F., Jemmi T. Use of listeriolysin O and internalin A in a seroepidemiological study of listeriosis in Swiss dairy cows // J Clin Microbiol. – 2003. – Vol.3. – P. 1055-1061. doi: 10.1128/JCM.41.3.1055-1061.2003.