Listeria monocytogenes is a foodborne opportunistic pathogen, that causes outbreaks and fatal cases worldwide. However, only few studies have been published in Mexico reporting the prevalence of this pathogen in food. Therefore, the objective of this current study is to evaluate the prevalence of L. monocytogenes in cheese sold in Tamaulipas, Mexico, and its potential risk to the population. For this purpose, samples were taken in 100 stores during the months of February, June and October 2023, and a total of 300 cheese products in 10 municipalities of Tamaulipas, Mexico were collected. Identification was performed by culture and PCR. Ten virulence factors were also analyzed and susceptibility testing to 14 antibiotics was performed. As a result, a prevalence of L. monocytogenes was detected in 12%. The most frequently detected virulence factors were actA (83.3%, 30/36) and hly (83.3%, 30/36). The strains were resistant to only 9 of the 14 antibiotics tested. The strains showed resistance in higher percentage to sulfamethoxazole/trimethoprim (STX/TMP: 38.8%, 14/36), penicillin (PE: 16.6%, 6/36), tetracycline (TE: 13.8%, 5/36) and amoxicillin/clavulanic acid (AMC: 13.8%, 5/36). The results of the current study show the presence of L. monocytogenes in cheese products sold in Tamaulipas, Mexico. The low prevalence of L. monocytogenes and low resistance to antibiotics could imply a low risk for public health. However, it is necessary to implement monitoring of L. monocytogenes in food, to monitor its potential risk for the consumer.
Díaz Galindo EP, Valladares Carranza B, Gutiérrez Castillo ADC, Arriaga Jordan CM, Quintero-Salazar B, Cervantes Acosta P, et al. Caracterización de Queso Fresco Comercializado En Mercados Fijos y Populares de Toluca, Estado de México. Rev Mex Cienc Pecu 2017; 8: 139–146. https://doi.org/10.22319/rmcp.v8i2.4419.
De La Rosa-Hernández MC, Cadena-Ramírez A, Téllez-Jurado A, Gómez-Aldapa CA, Rangel-Vargas E, Chávez-Urbiola EA, et al. Presence of multidrug-resistant Shiga Toxin–producing Escherichia coli, enteropathogenic Escherichia coli, and enterotoxigenic Escherichia coli on fresh cheeses from local retail markets in Mexico. J Food Prot 2018; 81: 1748–1754. https://doi.org/10.4315/0362-028X.JFP-18-166.
Loeza-Lara PD, Medina-Estrada RI, Bravo-Monzón ÁE, Jiménez-Mejía R. Frequency and characteristics of ESBL-producing Escherichia coli isolated from Mexican fresh cheese. Food Sci Technol 2023; 43: e108222. https://doi.org/10.1590/fst.108222.
Wiśniewski P, Zakrzewski AJ, Zadernowska A, Chajęcka-Wierzchowska W. Antimicrobial resistance and virulence characterization of Listeria monocytogenes strains isolated from food and food processing environments. Pathogens 2022; 11: 1099. https://doi.org/10.3390/pathogens11101099.
Imre K, Ban-Cucerzan A, Herman V, Sallam KI, Cristina RT, Abd-Elghany SM, et al. Occurrence, pathogenic potential and antimicrobial resistance of Escherichia coli isolated from raw milk cheese commercialized in Banat region, Romania. Antibiotics 2022; 11: 721. https://doi.org/10.3390/antibiotics11060721.
Praça J, Furtado R, Coelho A, Correia CB, Borges V, Gomes JP, et al. Listeria monocytogenes, Escherichia coli and coagulase positive staphylococci in cured raw milk cheese from Alentejo region, Portugal. Microorganisms 2023; 11: 322. https://doi.org/10.3390/microorganisms11020322.
Gajewska J, Zakrzewski A, Chajęcka-Wierzchowska W, Zadernowska A. Meta-analysis of the global occurrence of S. aureus in raw cattle milk and artisanal cheeses. Food Control 2023; 147: 109603. https://doi.org/10.1016/j.foodcont.2023.109603.
Wiktorczyk-Kapischke N, Skowron K, Grudlewska-Buda K, Wałecka-Zacharska E, Korkus J, Gospodarek-Komkowska E. Adaptive response of Listeria monocytogenes to the stress factors in the food processing environment. Front Microbiol 2021; 12: 710085. https://doi.org/10.3389/fmicb.2021.710085.
Churchill KJ, Sargeant JM, Farber JM, O’connor AM. Prevalence of Listeria monocytogenes in select ready-to-eat foods—Deli Meat, soft cheese, and packaged salad: a systematic review and meta-analysis. J Food Prot 2019; 82: 344–357. https://doi.org/10.4315/0362-028X.JFP-18-158.
Osek J, Wieczorek K. Listeria monocytogenes—how this pathogen uses its virulence mechanisms to infect the hosts. Pathogens 2022; 11: 1491. https://doi.org/10.3390/pathogens11121491.
Koopmans MM, Brouwer MC, Vázquez-Boland JA, Van De Beek D. Human listeriosis. Clin Microbiol Rev 2023; 36: e00060–19. https://doi.org/10.1128/cmr.00060-19.
Matereke LT, Okoh AI. Listeria monocytogenes virulence, antimicrobial resistance and environmental persistence: a review. Pathogens 2020; 9: 528. https://doi.org/10.3390/pathogens9070528.
Chen Y, Knabel SJ. Multiplex PCR for simultaneous detection of bacteria of the genus Listeria, Listeria monocytogenes, and major serotypes and epidemic clones of L. monocytogenes. Appl Environ Microbiol 2007; 73: 6299–6304.
Suárez M, González-Zorn B, Vega Y, Chico-Calero I, Vázquez-Boland JA. A role for ActA in epithelial cell invasion by Listeria monocytogenes. Cell. Microbiol. 2001; 3: 853–864. https://doi.org/10.1046/j.1462-5822.2001.00160.x.
Xu XK, Wu QP, Zhang JM, Deng MQ, Zhou YH. Studies on specific detection of Listeria monocytogenes in foods by duplex PCR. Chin J Health Lab Technol 2009; 19: 1199–1201.
Chen M, Wu Q, Zhang J, Wang J. Prevalence and characterization of Listeria monocytogenes isolated from retail-level ready-to-eat foods in South China. Food Control 2014; 38: 1–7.
Liu D, Lawrence ML, Austin FW, Ainsworth AJ. A multiplex PCR for species-and virulence-specific determination of Listeria monocytogenes. J Microbiol Methods 2007; 71: 133–140.
Clayton EM, Hill C, Cotter PD, Ross RP. Real-time PCR assay to differentiate listeriolysin S-positive and-negative strains of Listeria monocytogenes. Appl Environ Microbiol 2011; 77: 163–171.
Notermans SH, Dufrenne J, Leimeister-Wächter M, Domann E, Chakraborty T. Phosphatidylinositol-specific phospholipase C activity as a marker to distinguish between pathogenic and nonpathogenic Listeria species. Appl Environ Microbiol 1991; 57: 2666–2670.
Zhang W, Jayarao BM, Knabel SJ, Zhang W, Jayarao BM, Knabel SJ, et al. Multi-virulence-locus sequence typing of Listeria monocytogenes. Appl Environ Microbiol 2004; 70: 913–920. https://doi.org/10.1128/AEM.70.2.913.
CLSI Clinical and Laboratory Standards Institute. M100 Performance Standards for Antimicrobial Susceptibility Testing 2020.
EUCAST The European Committee on Antimicrobial Susceptibility Testing. Breakpoint Tables for Interpretation of MICs and Zone Diameters 2020.
Magiorakos A-P, Srinivasan A, Carey RB, Carmeli Y, Falagas ME, Giske CG, et al. Multidrug-resistant, extensively drug-resistant and Pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect 2012; 18: 268–281. https://doi.org/10.1111/j.1469-0691.2011.03570.x.
Guel-García P, García De León FJ, Aguilera-Arreola G, Mandujano A, Mireles-Martínez M, Oliva-Hernández A, et al. Prevalence and antimicrobial resistance of Listeria monocytogenes in different raw food from Reynosa, Tamaulipas, Mexico. Foods 2024; 13: 1656. https://doi.org/10.3390/foods13111656.
Gérard A, El-Hajjaji S, Burteau S, Fall PA, Pirard B, Taminiau B, et al. Study of the microbial diversity of a panel of Belgian artisanal cheeses associated with challenge studies for Listeria monocytogenes. Food Microbiol 2021; 100: 103861. https://doi.org/10.1016/j.fm.2021.103861.
Dehnavi M, Akhodzadeh Basti A, Khanjari A, Rezaei E. Prevalence of Listeria monocytogenes in traditional cheeses obtained from food sale centers of Tehran, Iran. J Food Saf Hyg 2022. https://doi.org/10.18502/jfsh.v7i3.9133.
Martinez-Rios V, Dalgaard P. Prevalence of Listeria monocytogenes in European cheeses: a systematic review and meta-analysis. Food Control 2018; 84: 205–214. https://doi.org/10.1016/j.foodcont.2017.07.020.
Cufaoglu G, Ambarcioglu P, Ayaz ND. Meta-analysis of the prevalence of Listeria spp. and antibiotic resistant L. monocytogenes isolates from foods in Turkey. LWT 2021; 144: 111210. https://doi.org/10.1016/j.lwt.2021.111210.
Akrami-Mohajeri F, Derakhshan Z, Ferrante M, Hamidiyan N, Soleymani M, Conti GO, et al. The prevalence and antimicrobial resistance of Listeria spp in raw milk and traditional dairy products delivered in Yazd, Central Iran (2016). Food Chem Toxicol 2018; 114: 141–144. https://doi.org/10.1016/j.fct.2018.02.006.
Espinosa-Mata E, Mejía L, Villacís JE, Alban V, Zapata S. Detection and genotyping of Listeria monocytogenes in artisanal soft cheeses from Ecuador. Rev Argent Microbiol 2022; 54: 53–56. https://doi.org/10.1016/j.ram.2021.02.013.
Zafar N. Prevalence, molecular characterization and antibiogram study of Listeria monocytogenes isolated from raw milk and milk products. Pure Appl Biol 2020; 9. https://doi.org/10.19045/bspab.2020.90211.
Elavarasi S, Ramesh B, Sathiyamurthy K. Prevalence and antimicrobial resistance pattern of Listeria monocytogenes in ready to eat foods in Tamil Nadu, India. Indian J Sci Technol 2023; 16: 501–508. https://doi.org/10.17485/IJST/v16i7.1979.
Kayode AJ, Okoh AI. Assessment of multidrug-resistant Listeria monocytogenes in milk and milk product and one health perspective. PLOS ONE 2022; 17: e0270993. https://doi.org/10.1371/journal.pone.0270993.
Barría C, Singer RS, Bueno I, Estrada E, Rivera D, Ulloa S, et al. Tracing Listeria monocytogenes contamination in artisanal cheese to the processing environments in cheese producers in Southern Chile. Food Microbiol 2020; 90: 103499. https://doi.org/10.1016/j.fm.2020.103499.
McIntyre L, Wilcott L, Naus M. Listeriosis outbreaks in British Columbia, Canada, caused by soft ripened cheese contaminated from environmental sources. BioMed Res Int 2015; 2015: 1–12. https://doi.org/10.1155/2015/131623.
González-Córdova AF, Yescas C, Ortiz-Estrada ÁM, De La Rosa-Alcaraz MDLÁ, Hernández-Mendoza A, Vallejo-Cordoba B. Invited review: artisanal Mexican cheeses. J Dairy Sci 2016; 99: 3250–3262. https://doi.org/10.3168/jds.2015-10103.
Carpentier B, Cerf O. Review - persistence of Listeria monocytogenes in food industry equipment and premises. Int J Food Microbiol 2011; 145: 1–8. https://doi.org/10.1016/j.ijfoodmicro.2011.01.005.
Zakaria AI, Sabala RF. Potential public health hazards related to consumption of poultry contaminated with antibiotic resistant Listeria monocytogenes in Egypt. BMC Microbiol 2024; 24: 41. https://doi.org/10.1186/s12866-024-03183-x.
Cao X, Wang Y, Wang Y, Ye C. Isolation and characterization of Listeria monocytogenes from the Black-Headed gull feces in Kunming, China. J Infect Public Health 2018; 11: 59–63. https://doi.org/10.1016/j.jiph.2017.03.003.
Quereda JJ, Morón-García A, Palacios-Gorba C, Dessaux C, García-del Portillo F, Pucciarelli MG, et al. Pathogenicity and virulence of Listeria monocytogenes: a trip from environmental to medical microbiology. Virulence 2021; 12: 2509–2545. https://doi.org/10.1080/21505594.2021.1975526.
Rippa A, Bilei S, Peruzy MF, Marrocco MG, Leggeri P, Bossù T, et al. Antimicrobial resistance of Listeria monocytogenes strains isolated in food and food-processing environments in Italy. Antibiotics 2024; 13: 525. https://doi.org/10.3390/antibiotics13060525.
Radoshevich L, Cossart P. Listeria monocytogenes: towards a complete picture of its physiology and pathogenesis. Nat Rev Microbiol 2018; 16: 32–46. https://doi.org/10.1038/nrmicro.2017.126.
Lecuit M. Listeria monocytogenes, a model in infection biology. Cell. Microbiol. 2020; 22. https://doi.org/10.1111/cmi.13186.
Lopes-Luz L, Mendonça M, Bernardes Fogaça M, Kipnis A, Bhunia AK, Bührer-Sékula S. Listeria monocytogenes : review of pathogenesis and virulence determinants-targeted immunological assays. Crit Rev Microbiol 2021; 47: 647–666. https://doi.org/10.1080/1040841X.2021.1911930.
Lakicevic BZ, Den Besten HMW, De Biase D. Landscape of stress response and virulence genes among Listeria monocytogenes strains. Front Microbiol 2022; 12: 738470. https://doi.org/10.3389/fmicb.2021.738470.
Swaminathan B, Gerner-Smidt P. The epidemiology of human listeriosis. Microbes Infect 2007; 9: 1236–1243. https://doi.org/10.1016/j.micinf.2007.05.011.
Baquero F, F Lanza V, Duval M., Coque TM. Ecogenetics of antibiotic resistance in Listeria monocytogenes. Mol Microbiol 2020; 113: 570–579. https://doi.org/10.1111/mmi.14454.
Anwar TM, Pan H, Chai W, Ed-Dra A, Fang W, Li Y, et al. Genetic diversity, virulence factors, and antimicrobial resistance of Listeria monocytogenes from food, livestock, and clinical samples between 2002 and 2019 in China. Int J Food Microbiol 2022; 366: 109572. https://doi.org/10.1016/j.ijfoodmicro.2022.109572.
Dickstein Y, Oster Y, Shimon O, Nesher L, Yahav D, Wiener-Well Y, et al. Antibiotic treatment for invasive nonpregnancy-associated listeriosis and mortality: a retrospective cohort study. Eur J Clin Microbiol Infect Dis 2019; 38: 2243–2251. https://doi.org/10.1007/s10096-019-03666-0.
Olaimat AN, Al‐Holy MA, Shahbaz HM, Al‐Nabulsi AA, Abu Ghoush MH, Osaili TM, et al. Emergence of antibiotic resistance in Listeria monocytogenes isolated from food products: a comprehensive review. Compr Rev Food Sci Food Saf 2018; 17: 1277–1292. https://doi.org/10.1111/1541-4337.12387.
Temple ME, Nahata MC. Treatment of listeriosis. Ann Pharmacother 2000; 34: 656–661. https://doi.org/10.1345/aph.19315.