Advertisement

Prevalence and characterization of Listeria monocytogenes isolated from pork meat and on inert surfaces

  • Alejandro Miguel Figueroa-López
  • Ignacio Eduardo Maldonado-Mendoza
  • Jaime López-Cervantes
  • Abel Alberto Verdugo-Fuentes
  • Dante Alejandro Ruiz-Vega
  • Ernesto Uriel Cantú-SotoEmail author
Food Microbiology - Research Paper

Abstract

This study focuses on the prevalence of Listeria monocytogenes (Lm) in pork meat and on inert surfaces from slaughterhouses in Sonora, Mexico. A total of 21 Lm were obtained from 103 samples, giving a prevalence of 20.3%. The prevalence of Lm in pork loin was 15.9% and 20.8% for inert surfaces in Federal Inspection Type (FIT) slaughterhouses. For non-FIT slaughterhouses, the prevalence was 25.7%. PCR amplification of genomic DNA from the Lm isolates revealed the presence of the hlyA gene, suggesting a pathogenic nature for these isolates. The isolates obtained in this work all clustered with Lm, according to our phylogenetic analysis based on the 16S rDNA sequence. This Lm cluster indicates that Lm isolates 7-2, 4, 2-1, 10B, 8, 3, 3-3, and 9 share 16S rRNA identity with other Lm isolates that have been reported as foodborne pathogens (rR2-502, J1817, J1816, J1926) and that are involved in foodborne outbreaks. The most commonly detected serotypes were 1/2a and 1/2b. All isolates displayed differential responses to the assayed antibiotics, and most isolates were able to grow in the presence of penicillin G, or both penicillin and penicillin-derived (oxacillin) antibiotics.

Keywords

Pathogen occurrence Listeria monocytogenes Pork meat Antibiotics 

Notes

Acknowledgements

We thank Dr. Brandon Loveall of Improvence for English proofreading of the manuscript.

Funding

This work was supported by Mexico’s Consejo Nacional de Ciencia y Tecnología (CONACyT), the FESE Foundation (FESE/267/14), and the Instituto Tecnológico de Sonora (PROFAPI 2016-0016).

References

  1. 1.
    Weller D, Andrus A, Wiedmann M, den Bakker H (2015) Listeria booriae sp. nov. and Listeria newyorkensis sp. nov., from food processing environments in the USA. Int J Syst Evol Microbiol 65(1):286–292.  https://doi.org/10.1099/ijs.0.070839-0 Google Scholar
  2. 2.
    Hyden P, Pietzka A, Lennkh A, Murer A, Springer B, Blaschitz M, Indra A, Huhulescu S, Allerberger F, Ruppitsch W, Sensen CW (2016) Whole genome sequence-based serogrouping of Listeria monocytogenes isolates. J Biotechnol 235:181–186.  https://doi.org/10.1016/j.jbiotec.2016.06.005 Google Scholar
  3. 3.
    Thévenot D, Dernburg A, Vernozy-Rozand C (2006) An updated review of Listeria monocytogenes in the pork meat industry and its products. J Appl Microbiol 101(1):7–17.  https://doi.org/10.1111/j.1365-2672.2006.02962.x Google Scholar
  4. 4.
    Dhama K, Karthik K, Tiwari R, Shabbir MZ, Barbuddhe S, Malik SVS, Singh RK (2015) Listeriosis in animals, its public health significance (food-borne zoonosis) and advances in diagnosis and control: a comprehensive review. Vet Q 35(4):211–235.  https://doi.org/10.1080/01652176.2015.1063023 Google Scholar
  5. 5.
    Alimentarius C. Guidelines on the application of general pronciples of food hygiene to the control of Listeria monocytogenes in foods. http://www.fao.org/fao-who-codexalimentarius/codex-texts/guidelines/es/
  6. 6.
    Puga C, SanJose C, Orgaz B (2016) Biofilm development at low temperatures enhances Listeria monocytogenes resistance to chitosan. Food Control 65:143–151.  https://doi.org/10.1016/j.foodcont.2016.01.012 Google Scholar
  7. 7.
    O’Driscoll B, Gahan C, Hill C (1996) Adaptive acid tolerance response in Listeria monocytogenes: isolation of an acid-tolerant mutant which demonstrates increased virulence. Appl Environ Microbiol 62(5):1693–1698. http://aem.asm.org/content/62/5/1693.abstract Google Scholar
  8. 8.
    Poimenidou SV, Chatzithoma D-N, Nychas G-J, Skandamis PN (2016) Adaptive response of Listeria monocytogenes to heat, salinity and low pH, after habituation on cherry tomatoes and lettuce leaves. PLoS One 11(10):e0165746.  https://doi.org/10.1371/journal.pone.0165746 Google Scholar
  9. 9.
    Liu F, Du L, Zhao T, Zhao P, Doyle MP (2017) Effects of phenyllactic acid as sanitizing agent for inactivation of Listeria monocytogenes biofilms. Food Control 78:72–78.  https://doi.org/10.1016/j.foodcont.2017.02.050 Google Scholar
  10. 10.
    Van den Elzen A, Snijders J (1993) Critical points in meat production lines regarding the introduction of Listeria monocytogenes. Vet Q 15(4):143–145.  https://doi.org/10.1080/01652176.1993.9694393 Google Scholar
  11. 11.
    Scallan E, Hoekstra R, Angulo F et al (2011) Foodborne illness acquired in the United States—major pathogens. Emerg Infect Dis 17(1):7–15.  https://doi.org/10.3201/eid1701.P11101 Google Scholar
  12. 12.
    Weatherill S. Report of the independent investigator into the 2008 Listeriosis outbreak. Canada H, ed. 2009:vii. http://publications.gc.ca/collections/collection_2009/agr/A22-508-2009E.pdf
  13. 13.
    SAGARPA. Crecen 9.5 por ciento exportaciones de carne de porcino: SAGARPA. social U de comunicación, ed. 2017. http://www.sagarpa.gob.mx/Delegaciones/jalisco/boletines/Paginas/2017B03015.aspx
  14. 14.
    Castañeda-Ruelas G, Eslava-Campos C, Castro-del Campo N, León-Félix J, Chaidez-Quiroz C (2014) Listeriosis en México: importancia clínica y epidemiológica. Salud Publica Mex 56:654–659 http://www.scielosp.org/pdf/spm/v56n6/v56n6a16.pdf Google Scholar
  15. 15.
    Rubio-Lozano M, Martínez-Bruno J, Hernández-Castro R et al (2013) Detección de Listeria monocytogenes, Salmonella y Yersinia enterocolitica en carne de res en puntos de venta en México. Rev Mex Cienc Pecu 4(1):107–115Google Scholar
  16. 16.
    Moreno-Enriquez R, Garcia-Galaz A, Acedo-Felix E et al (2007) Prevalence, types, and geographical distribution of Listeria monocytogenes from a survey of retail Queso Fresco and associated cheese processing plants and dairy farms in Sonora, Mexico. J Food Prot 70(11):2596–2601Google Scholar
  17. 17.
    SSA. 2014 Productos y servicios. Métodos de prueba microbiológicos. Determinación de microorganismos indicadores. Determinación de microorganismos patógenos. (SSA1) C de R y FS, ed. ;NOM-210-SS. http://www.economia-noms.gob.mx/normas/noms/2010/210ssa12015.pdf
  18. 18.
    Scotter SL, Langton S, Lombard B, Schulten S, Nagelkerke N, in‘t Veld PH, Rollier P, Lahellec C (2001) Validation of ISO method 11290 part 1 — detection of Listeria monocytogenes in foods. Int J Food Microbiol 64(3):295–306.  https://doi.org/10.1016/S0168-1605(00)00462-1 Google Scholar
  19. 19.
    Momtaz H, Yadollahi S (2013) Molecular characterization of Listeria monocytogenes isolated from fresh seafood samples in Iran. Diagn Pathol 8(1):149.  https://doi.org/10.1186/1746-1596-8-149 Google Scholar
  20. 20.
    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. J Appl Bacteriol 70(5):372–379.  https://doi.org/10.1111/j.1365-2672.1991.tb02951.x Google Scholar
  21. 21.
    Cordero-Ramírez JD, López-Rivera R, Figueroa-Lopez AM, Mancera-López ME, Martínez-Álvarez JC, Apodaca-Sánchez MÁ, Maldonado-Mendoza IE (2013) Native soil bacteria isolates in Mexico exhibit a promising antagonistic effect against Fusarium oxysporum f. sp. radicis-lycopersici. J Basic Microbiol 53(10):838–847.  https://doi.org/10.1002/jobm.201200128 Google Scholar
  22. 22.
    Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Mol Biol Evol 33(7):1870–1874.  https://doi.org/10.1093/molbev/msw054 Google Scholar
  23. 23.
    de Vasconcelos Byrne V, Hofer E, Vallim DC, de Castro Almeida RC (2016) Occurrence and antimicrobial resistance patterns of Listeria monocytogenes isolated from vegetables. Braz J Microbiol 47(2):438–443.  https://doi.org/10.1016/j.bjm.2015.11.033 Google Scholar
  24. 24.
    CLSI (2018) Performance standards for antimicrobial disk susceptibility tests. CLSI standar:M02Google Scholar
  25. 25.
    Carpentier B, Cerf O (2011) Review-persistence of Listeria monocytogenes in food industry equipment and premises. Int J Food Microbiol 145(1):1–8.  https://doi.org/10.1016/j.ijfoodmicro.2011.01.005 Google Scholar
  26. 26.
    Thévenot D, Delignette-Muller M, Christieans S, Vernozy-Rozand C (2005) Prevalence of Listeria monocytogenes in 13 dried sausage processing plants and their products. Int J Food Microbiol 102(1):85–94.  https://doi.org/10.1016/j.ijfoodmicro.2004.12.008 Google Scholar
  27. 27.
    Chasseignaux E, Gérault P, Toquin M, Salvat G, Colin P, Ermel G (2002) Ecology of Listeria monocytogenes in the environment of raw poultry meat and raw pork meat processing plants. FEMS Microbiol Lett 210(2):271–275.  https://doi.org/10.1111/j.1574-6968.2002.tb11192.x Google Scholar
  28. 28.
    Salvat G, Toquin M, Michel Y, Colin P (1995) Control of Listeria monocytogenes in the delicatessen industries: the lessons of a listeriosis outbreak in France. Int J Food Microbiol 25(1):75–81.  https://doi.org/10.1016/0168-1605(94)00087-M Google Scholar
  29. 29.
    Peccio A, Autio T, Korkeala H, Rosmini R, Trevisani M (2003) Listeria monocytogenes occurrence and characterization in meat-producing plants. Lett Appl Microbiol 37(3):234–238.  https://doi.org/10.1046/j.1472-765X.2003.01384.x Google Scholar
  30. 30.
    Liu H, Lu L, Pan Y, Sun X, Hwang CA, Zhao Y, Wu VCH (2015) Rapid detection and differentiation of Listeria monocytogenes and Listeria species in deli meats by a new multiplex PCR method. Food Control 52:78–84.  https://doi.org/10.1016/J.FOODCONT.2014.12.017 Google Scholar
  31. 31.
    Gedde MM, Higgins DE, Tilney LG, Portnoy DA (2000) Role of listeriolysin O in cell-to-cell spread of Listeria monocytogenes. Infect Immun 68(2):999–1003.  https://doi.org/10.1128/iai.68.2.999-1003.2000 Google Scholar
  32. 32.
    Law J, Ab Mutalib N, Chan K, Lee L (2015) An insight into the isolation, enumeration, and molecular detection of Listeria monocytogenes in food. Front Microbiol 6(1227).  https://doi.org/10.3389/fmicb.2015.01227
  33. 33.
    Hellberg R, Martin K, Keys A, Haney C, Shen Y, Smiley R (2013) 16S rRNA partial gene sequencing for the differentiation and molecular subtyping of Listeria species. Food Microbiol 36(2):231–240.  https://doi.org/10.1016/j.fm.2013.06.001 Google Scholar
  34. 34.
    Liu D (2006) Identification, subtyping and virulence determination of Listeria monocytogenes, an important foodborne pathogen. J Med Microbiol 55(6):645–659.  https://doi.org/10.1099/jmm.0.46495-0 Google Scholar
  35. 35.
    Al-Nabulsi A, Osaili T, Awad A, Olaimat A, Shaker R, Holley R (2015) Occurrence and antibiotic susceptibility of Listeria monocytogenes isolated from raw and processed meat products in Amman, Jordan. CyTA-J Food 13(3):346–352.  https://doi.org/10.1080/19476337.2014.982191 Google Scholar
  36. 36.
    Beumer R, Hazeleger W (2003) Listeria monocytogenes: diagnostic problems. FEMS Immunol Med Microbiol 35(3):191–197.  https://doi.org/10.1016/S0928-8244(02)00444-3 Google Scholar
  37. 37.
    Chen Y, Strain E, Allard M, Brown E (2011) Genome sequences of Listeria monocytogenes strains J1816 and J1-220 associated with human outbreaks. J Bacteriol 193(13):3424–3425.  https://doi.org/10.1128/JB.05048-11 Google Scholar
  38. 38.
    Figueroa-López AM, Cordero-Ramírez JD, Martínez-Álvarez JC, López-Meyer M, Lizárraga-Sánchez GJ, Félix-Gastélum R, Castro-Martínez C, Maldonado-Mendoza IE (2016) Rhizospheric bacteria of maize with potential for biocontrol of Fusarium verticillioides. Springerplus. 5(1):330.  https://doi.org/10.1186/s40064-016-1780-x Google Scholar
  39. 39.
    Castañeda-ruelas GM, Campo NC, Félix JL et al (2013) Prevalence , levels , and relatedness of Listeria monocytogenes isolated from raw and ready-to-eat foods at retail markets in Culiacan , Sinaloa , Mexico. J Microbiol Res 3(2):92–98.  https://doi.org/10.5923/j.microbiology.20130302.06 Google Scholar
  40. 40.
    Davis JA, Jackson CR (2009) Comparative antimicrobial susceptibility of Listeria monocytogenes, L. innocua, and L. welshimeri. Microb Drug Resist 15(1):27–32.  https://doi.org/10.1089/mdr.2009.0863 Google Scholar
  41. 41.
    Moreno LZ, Paixao R, Gobbi DD et al (2014) Characterization of antibiotic resistance in Listeria spp. isolated from slaughterhouse environments, pork and human infections. J Infect Dev Ctries 8(4):416–423.  https://doi.org/10.3855/jidc.4188 Google Scholar
  42. 42.
    Dajani AS (2002) Beta-lactam resistance: clinical implications for pediatric patients. J Int Med Res 30(1_suppl):2A–9A.  https://doi.org/10.1177/14732300020300S102 Google Scholar
  43. 43.
    Harakeh S, Saleh I, Zouhairi O, Baydoun E, Barbour E, Alwan N (2009) Antimicrobial resistance of Listeria monocytogenes isolated from dairy-based food products. Sci Total Environ 407(13):4022–4027.  https://doi.org/10.1016/j.scitotenv.2009.04.010 Google Scholar
  44. 44.
    Ramaswamy V, Cresence VM, Rejitha JS et al (2007) Listeria review of epidemiology and pathogenesis. J Microbiol Immunol Infect 40(1):4–13Google Scholar
  45. 45.
    Conter M, Paludi D, Zanardi E, Ghidini S, Vergara A, Ianieri A (2009) Characterization of antimicrobial resistance of foodborne Listeria monocytogenes. Int J Food Microbiol 128(3):497–500.  https://doi.org/10.1016/j.ijfoodmicro.2008.10.018 Google Scholar
  46. 46.
    Wang X-M, Lü X-F, Yin L, Liu HF, Zhang WJ, Si W, Yu SY, Shao ML, Liu SG (2013) Occurrence and antimicrobial susceptibility of Listeria monocytogenes isolates from retail raw foods. Food Control 32(1):153–158.  https://doi.org/10.1016/j.foodcont.2012.11.032 Google Scholar
  47. 47.
    Katzung BG (2007) Chapter 34. Chloramphenicol, tetracyclines, macrolides, clindamycin, & streptogramins. In: Trevor AJ, Katzung BG, Kruidering-Hall M (eds) Katzung & Trevor’s pharmacology: examination & broad review. 11th ed. McGraw-Hill, San Francisco, United States of AmericaGoogle Scholar
  48. 48.
    Gómez D, Azón E, Marco N, Carramiñana JJ, Rota C, Ariño A, Yangüela J (2014) Antimicrobial resistance of Listeria monocytogenes and Listeria innocua from meat products and meat-processing environment. Food Microbiol 42:61–65.  https://doi.org/10.1016/j.fm.2014.02.017 Google Scholar

Copyright information

© Sociedade Brasileira de Microbiologia 2019

Authors and Affiliations

  • Alejandro Miguel Figueroa-López
    • 1
  • Ignacio Eduardo Maldonado-Mendoza
    • 2
  • Jaime López-Cervantes
    • 1
  • Abel Alberto Verdugo-Fuentes
    • 1
  • Dante Alejandro Ruiz-Vega
    • 1
  • Ernesto Uriel Cantú-Soto
    • 1
    Email author
  1. 1.Departamento de Biotecnología y Ciencias AlimentariasInstituto Tecnológico de SonoraCiudad ObregónMexico
  2. 2.Departamento de Biotecnología AgrícolaInstituto Politécnico Nacional. CIIDIR-Unidad SinaloaGuasaveMexico

Personalised recommendations