Presence of Listeria monocytogenes in ready-to-eat foods available in open markets, delicatessens and supermarkets, Bogotá, 2002-2008

Ana Isabel Muñoz, Mercedes Vargas, Ligia Otero, Graciela Díaz, Viviana Guzmán, .

Keywords: Listeria monocytogenes, enfermedades transmitidas por alimentos, listeriosis, salud pública

Abstract

Introduction. The increase in diseases transmitted by foods has become a public health problem. Listeria monocytogenes, the etiological agent of listeriosis or typical food poisoning, is considered to be among the most important food borne illnesses. High risk foods for L.monocytogenes have been recognized as foods already prepared for consumption and made available in retail outlets.
Objective. The presence of L. monocytogenes was identified in prepared foods found in open markets and delicatessens in the city of Bogotá.
Material and methods. A transverse descriptive study over a 7-year period, with an analytic component, in which 600 foods were analyzed--300 from delicatessens and 300 from open market places. Reference methods were used to determine the presence or absence of L. monocytogenes in 25 grams or milliliters a food sample.
Results. Of the 600 samples, 68 were positive for L. monocytogenes (11.3%). Twenty-six (38.2%) were taken from delicatessens and 42 (61.8%) from open market places. The serotype most frequently isolated was 4b, with 53 (78.0%) isolations. Fresh cheeses and matured cheeses showed greater contamination with L. monocytogenes than the other foods (p<0.001 in both cases).
Conclusions. The results indicate that prepared foods are vehicles for the transmission of the Listeria bacterium. These potentially high risk foods are candidates for control and monitoring by public health authorities. Programs must be instituted to implement surveillance norms that lead to the reduction and control of this microorganism and geared toward the prevention of food borne diseases.
Listeria monocytogenes; foodborne diseases; listeriosis; public health

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  • Ana Isabel Muñoz Laboratorio de Microbiología de Alimentos, Subdirección de Alimentos y Bebidas Alcohólicas, Instituto Nacional de Vigilancia de Medicamentos y Alimentos, Bogotá, D.C., Colombia
  • Mercedes Vargas Laboratorio de Microbiología de Alimentos, Subdirección de Alimentos y Bebidas Alcohólicas, Instituto Nacional de Vigilancia de Medicamentos y Alimentos, Bogotá, D.C., Colombia
  • Ligia Otero Laboratorio de Microbiología de Alimentos, Subdirección de Alimentos y Bebidas Alcohólicas, Instituto Nacional de Vigilancia de Medicamentos y Alimentos, Bogotá, D.C., Colombia
  • Graciela Díaz Laboratorio de Microbiología de Alimentos, Subdirección de Alimentos y Bebidas Alcohólicas, Instituto Nacional de Vigilancia de Medicamentos y Alimentos, Bogotá, D.C., Colombia
  • Viviana Guzmán Laboratorio de Microbiología de Alimentos, Subdirección de Alimentos y Bebidas Alcohólicas, Instituto Nacional de Vigilancia de Medicamentos y Alimentos, Bogotá, D.C., Colombia

References

1. Organización de las Naciones Unidas para la Agricultura y la Alimentación. Organización Mundial de la Salud. Evaluación de riesgos de Listeria monocytogenes en alimentos listos para el consumo: resumen interpretativo. Serie de evaluación de riesgos microbiológicos No. 4. Roma: FAO/OMS; 2004. p. 53.
2. Muñoz AI, Díaz G. Listeriosis. Santafé de Bogotá: INVIMA-INS; 1998. p. 64.
3. World Health Organization (WHO). Food borne listeriosis. WHO Working group. Bull World Health Organ. 1988;66:421-8.
4. Rocourt J. Risk factors for listeriosis. Food Control. 1996;7:195-202.
5. Food and Drug Administration, Center for Food Safety and Applied Nutrition, USDA/Food Safety and Inspection Service, Centers for Disease Control and Prevention. Draf assessment of the relative risk to public health from foodborne Listeria monocytogenes among selected categories of ready- to-eat foods. Interpretative summary p.1-24, 2001. Fecha de consulta: 14 de febrero de 2002. Disponible en: http://www.foodsafety.gov/~dms/lmrisk.html.
6. Division of Foodborne, Bacterial and Mycotic Diseases (DFBMD), Centers for Disease Control and Prevention. Listeriosis. Atlanta: CDC; 2008. p. 4. Fecha de consulta: 10 de mayo de 2009. Disponible en: http:// www.cdc.gov/nczved/dfbmd/disease_listing/listeriosis_gi.html.
7. United States Department of Agriculture. Food Safety and Inspection Service. Production and inspection. FSIS rule designed to reduce Listeria monocytogenes in ready to eat food meat and poultry. USA: FSIS; 2009. p. 3. Fecha de consulta: 3 de mayo de 2009. Disponible en: http://www.fsis.usda.gov/factsheets/fsis_rule_designed_to_reduce_listeria/index.asp.
8. Canadian Food Inspection Agency. Food safety facts on Listeria. Canada: CFIA; 2010 p. 4. Fecha de consulta: 10 de mayo de 2009. Disponible en: http://www.inspection.gc.ca/english/fssa/concen/cause/listeriae.shtml.
9. Evans MR, Swaminathan B, Graves LM, Altremann E, Klaenhammer TR, Fink RC, et al. Genetic markers unique to Listeria monocytogenes serotype 4b differentiate epidemic clone II (hot dog outbreak strains) from other linages. Appl Environ Microbiol. 2004;70:2383-90.
10. Gilbreth E, Call JE, Wallace M, Scott VN, Chen Y, Luchansky JB. Relatedness of Listeria monocytogenes isolated recovered from selected ready to eat foods and listeriosis patients in the United States. Appl Environ Microbiol. 2005;17:8115-22.
11. Volpe KE, Kathariou S, Edwards JS, Wolf LA. Multiple-locus variable-number tadem-repeat analysis as a tool for subtyping Listeria monocytogenes strain. J Clin Microbiol. 2008;46:1435-50.
12. Oteo J, Alós JI. Listeria y listeriosis. Fecha de consulta: 31 de mayo de 2009. Disponible en: http://www.seimc.org/control/revisiones/bacteriologia/listeria.pdf.
13. Mammina C, Aleo A, Romani C, Pellissier N, Nicoletti P, Pecile P, et al. Characterization of Listeria monocytogenes isolates from human listeriosis cases in Italy. J Clin Microbiol. 2009;47:2925-30.
14. Wikipedia. Listeriosis. Fecha de consulta: 31 de mayo de 2009. Disponible en: http://es.wikipedia.org/wiki/Listeriosis.
15. Food Drug Administration. Foodborne pathogenic microorganisms and natural toxins handbook. Listeria monocytogenes. Fecha de consulta: 31 de mayo de 2009. Disponible en:_http://www.fda.gov/Food/FoodSafety/FoodborneIllness/FoodborneIllnessFoodbornePathogensNaturalToxins/BadBugBook/ucm070064.htm.
16. U.S. Food and Drug Administration. Listeria monocytogenes: Draft guidance. Sec. 555.320. Washington, D.C.: FDA; 2008. p. 7. Fecha de consulta: 31 de mayo de 2009. Disponible en: http://www.fda.gov/ICECI/ComplianceManuals/CompliancePolicyGuidanceManual/ucm136694.htm.
17. U.S. Food and Drug Administration. Guidance for industry: Control of Listeria monocytogenes in refrigerated or frozen ready-to-eat foods; draf guidance. Washington: FDA; 2008. p. 26. Fecha de consulta: 31 de mayo de 2009. Disponible en: http://www.fda.gov/food/guidancecomplianceregulatoryinformation/guidancedocuments/foodprocessinghaccp/ucm073110.htm.
18. U.S. Food and Drug Administration. Listeria: Washington: FDA, 2008. p. 3. Fecha de consulta: 31 de mayo de 2009. Disponible en: http://www.fda.gov/ForConsumers/ByAudience/ForWomen/ucm118542.htm.
19. Medline Plus. Listeriosis: infecciones por Listeria. Biblioteca Nacional de Medicina de EE.UU. 2010. Fecha de consulta: 31 de mayo de 2010. Disponible en: http://www.nlm.nih.gov/medlineplus/spanish/listeriainfections.html.
20. Kim JW, Siletzky RM, Kathariou S. Hot ranges of Listeria -specific bacteriophages from the turkey processing plant environment in the United States. Appl Environ Microbiol. 2008;74:6623-30.
21. Organización Mundial de Sanidad Animal. Manual de la Organización Mundial de Sanidad Animal (OIE) sobre animales terrestres. Cap. 210.14. Listeria monocytogenes. Madrid: OIE; 2004. p. 16.
22. Perroni MA. Listeria monocytogenes y su presencia en productos lácteos. Diaeta. 2008;26:37-43.
23. Centers for Disease Control and Prevention; National Center for Zoonotic, Vector-Borne, and Enteric Diseases. Listeriosis. Atlanta: CDC. (Your Online Source for credible). Fecha de consulta: 31 de mayo de 2009. Disponible en: http://www.cdc.gov/nczved/divisions/dfbmd/diseases/listeriosis/.
24. Stelten A, Nightingale KK. Development and implementation of a multiplex single -nucleotide polymorphism genotyping assay for detection of virulence attenuating mutations in the Listeria monocytogenes virulence-associated gene InlA. Appl Environ Microbiol. 2008;74:7365-75.
25. United States Department of Agriculture. Food Safety and Inspection Service. Protec your baby and yourself from listeriosis. USA: FSIS; 2006. Fecha de consulta: 31 de mayo de 2009. Disponible en: http://www.fsis.usda.gov/factsheets/Protect_Your_Baby/index.asp.
26. Álvarez CJ, Guerrero JA, Muñoz MN, López MP, Borbón ME, Espinosa J. Informe epidemiológico de la vigilancia de eventos grupo factores de riesgo ambiental-Colombia 2010. Bogotá: INS; 2010. p. 25.
27. Jay JM. Microbiología moderna de los alimentos. En: Listeriosis transmitidas por alimentos. Tercera edición. Zaragoza (España): Editorial Acribia, S.A., 1994. p. 601-49.
28. Food Safety Network. Listeria monocytogenes: What is L. monocytogenes? Canada: FSN, 2010. (FSN Food Riskes). Fecha de consulta: 30 de mayo de 2010. Disponible en: http://www.foodsafetynetwork.ca/aspx/public/publication_detail_global.aspx?languageid=1&contenttypeid=5&id=76.
29. Walker SJ, Archer P, Banks JG. Growth of Listeria monocytogenes at refrigeration temperatures. J Appl Bact. 1990;68:157-62.
30. Pan Y, Breidt F Jr, Kathariou S. Competition of Listeria monocytogenes serotype 1/2 a and 4 b strains in mixed-culture biofilms. Appl Environ Microbiol. 2009;75:5846-52.
31. Shen Y, Liu Y, Zhang Y, Cripe J, Conway W, Meng J, et al. Isolation and characterization of Listeria monocytogenes isolates from ready to eat foods in Florida. Appl Environ Microbiol. 2006;72:5073-6.
32. Gilmour MW, Graham M, Domselaar GV, Tyler S, Kent H, Trout-Yake KM, et al. High-throughput genome sequencing of two Listeria monocytogenes clinical isolates during a large foodborne outbreak. BMC Genomics. 2010;11:1471-85.
33. Cole NB, Jones MV, Holyoak C. The effect of pH, salt concentration and temperature on the survival and growth of Listeria monocytogenes. J Appl Bacterio. 1990;69:63-72.
34. Liu D, Lawrence LM, Gorski L, Mandrell RE, Ainsworth AJ, Austin FW. Listeria monocytogenes serotype 4b strains belonging to lineages I and III possess distinct molecular features. J Clin Microbiol. 2006;44:214-7.
35. Wong AC. Biofilms in food processing environments. J Dairy Sci. 1998;81:2765-70.
36. Nightingale KK, Windham K, Wiedmann M. Evolution and molecular phylogeny of Listeria monocytogenes isolated from human and animal listeriosis cases and foods. J Bacteriol. 2005;187:5537-51.
37. Berche P, Gaillard JL, Richard S. Invasiveness and intracellular growth of Listeria monocytogenes. Infection. 1988;16(Suppl.2):145-8.
38. Sánchez E, Pardo R. Listeriosis del sistema nervioso central, formas meníngeas agudas supurativas y romboencefálica. Acta Neurol Colomb. 1992;8:165-8.
39. Brun- Buisson CJ, de Gialluly E, Gherardi R, Otterbein G, Gray F, Rapin M. Fatal nonmeningitic Listeria rhomboencephalitis, report of two cases. Arch Int Med. 1985;145:1982-5.
40. Armstron D. Listeria monocytogenes. En: Mandel GL, Douglas RG, Benett JE, editors. Principles and practice of infectious diseases. 4th edition. New York: Churchill Livingtone; 1995. p. 1180-5.
41. Payán A, Estudillo M. Listeriosis neonatal: ¿enfermedad poco frecuente o no diagnosticada? Enfoque microbiológico. Colombia Médica.1994;25:69-72.
42. Sánchez CE, Castillo A, Ortega C. Infección perinatal por Listeria. Reporte de un caso. Rev Col Obstet Ginecol. 2001;52:190-202.
43. Dalton CB, Austin CC, Sobel J, Hayes PS, Bibb WF, Graves LM, et al. An outbreak of gastroenteritis and fever due to Listeria monocytogenes in milk. N Engl J Med. 1997;336:100-5.
44. Salamina G, Dalle DE, Niccolini A, Poda G, Cesaroni D, Bucci M, et al. A foodborne outbreak of gastroenteritis involving Listeria monocytogenes. Epidemiol Infect. 1996;117:429-36.
45. Dalton CB, Med B, Austin CC, Sobel J, Hayes PS, Bibb WF, et al. An outbreak of gastroenteritis and fever due to Listeria monocytogenes in milk. N Engl J Med.1997;336:100-5.
46. United States Department of Agriculture. Food Safety and Inspection Service. At- risk populations. USA: FSIS; 2010. Fecha de consulta: 28 de mayo de 2010. Disponible en: http://ucfoodsafety.ucdavis.edu/Consumer_Advice/Foodborne_Illness_-_At_Risk_Populations/.
47. Kagkli DM, Iliopoulos V, Stergiou V, Lazaridou A, Nychas GJ. Differential Listeria monocytogenes strain survival and growth in katiti, a traditional Greek soft cheese, at different storage temperaturas. Appl Environ Microbiol. 2009;75:3621-6.
48. Borucki MK, Kim SH, Call DR, Smole SC, Pagotto F. Selective discrimination of Listeria monocytogenes epidemic strains by a mixed-genome DNA microarray compared to discrimination by pulse-field gel electrophoresis, ribotyping, and multilocus sequence typing. J Clin Microbiol. 2004;42:5270-6.
49. Nelson KE, Fouts DE, Mongodín EF, Ravel J, Deboy R, Kolonay JF, et al. Whole genome comparisons of serotype 4b and 1/2 a strains of the food-borne pothogen Listeria monocytogenes reveal new insights into the core genome components of this species. Nucleic Acids Res. 2004;32:2386-95.
50. Bruhn JB, Vogel BF, Gram L. Bias in the Listeria monocytogenes enrichment procedure: Linaje 2 strains out compete linaje 1 strains in University of Vermont selective enrichments. Appl Environ Microbiol. 2005;71:961-7.
51. Kathariou S. Listeria monocytogenes virulence and pathogenicity, a food safety perspective. J Food Prot. 2002;65:1811-29.
52. Wikipedia. Brote de listeriosis de 2008-2009 en Chile. Chile: Ministerio de Salud, 2010. Fecha de consulta: 29 de mayo de 2010. Disponible en: http://es.wikipedia.org/wiki/brote_de_listeriosis_de_2008-2009_en Chile.
53. Linnan MJ, Mascola L, Lou XD, Goulet V, May S, Salminen C, et al. Epidemic listeriosis associated with Mexican -style cheese. N Engl J Med. 1988;319;823-8.
54. Centers for Disease Control and Prevention. Outbreak of listeriosis associated with homemade Mexican-Style Cheese, North Carolina, October 2000, and January 2001. MMWR Morb Mortal Wkly Rep. 2001;50:560-2.
55. Fleming DW, Cochi SL, MacDonald KL, Brondum J, Hayes PS, Plikaytis BD, et al. Pasteurized milk as a vehicle of infection in an outbreak of listeriosis. N Engl Med. 1985;312:404-7.
56. McLauchlin J, Hall SM, Velani SK, Gilbert RJ. Human listeriosis and pate-a possible association. Brit Med J.1991;303:773-5.
57. Rocourt J. Listeria monocytogenes: The state of the science. Dairy Food Environ San. 1994;14:70-82.
58. Callejo R, Prieto M, Martínez C, Aguerre L, Rocco F, Martínez G. Manual de procedimientos: aislamiento, identificación, y caracterización de Listeria monocytogenes. Buenos Aires, Argentina: WHO Global Salm Surv; 2008. p. 39.
59. Schlech WF, Lavigne PM, Bortolussi RA, Allen AC, Haldane EV, Wort AJ, et al. Epidemic listeriosis-evidence for transmission by food. N Engl J Med. 1983;308:203-6.
60. Kerr KG, Dealler SF, Lancey RW. Materno fetal listeriosis from cook-chill and refrigerated food. Lancet. 1988;2:1113.
61. Shwartz B, Hexter D, Broome CV, Higtower AW, Hirschhorn RB, Porter JD. Investigation of an outbreak of listeriosis: New hypothesis for the etiology of epidemic Listeria monocytogenes infection. J Infect Dis. 1989;159:680-5.
62. Goulet V, Lepautre A, Rocourt J. Epidémie de listériose en France-Bilan final et resultats de l'enquête épidémiologique. Bull Epid Hebdom. 1993;4:13-4.
63. Wulff G, Gram L, Ahrens P, Vogel BF. One group of genetically similar Listeria monocytogenes strains frequently dominates and persists in several fish slaughter- and smokehouses. Appl Environ Microbiol. 2006;72:4313-22.
64. Food Safety and Inspection Service .U.S. Department of Agriculture. Microbiological testing programs for ready-to-eat (RTE) meat and poultry products. Washington: FSIS, 2005.
65. Yildirim S, Lin W, Hitchen AD, Jaykus LA, Alterman E, Klaenhammer TR, et al. Epidemic clone 1-specific genetic markers in strains of Listeria monocytogenes serotype 4b from foods. Appl Environ Microbiol. 2004;70:4158-64.
66. Cruz CD, Silvestre FA, Kinoshita EM, Landgraf M, Franco BDGM, Destro MT. Epidemiological survey of Listeria monocytogenes in a gravlas salmon processing line. Braz J Microbiol. 2008;39:375-83.
67. United States Department of Agriculture. Percent positive Listeria monocytogenes test for RTE meat and poultry, CY 2008. USA: FSIS; 2009.
68. Najjar MB, Chikindas M, Montville T. Changes in Listeria monocytogenes membrane fluidity in response to temperatures stress. Appl Environ Microbiol. 2007;73:6429-35.
69. Yoon Y, Kendall PA, Belk KE, Scanga JA, Smith GC, Sofos JN. Modeling the grow/no-growth boundaries of postprocessing Listeria monocytogenes contamination on frankfurters and Bologna treated with latica cid. Appl Environ Microbiol. 2009;75:353-8.
70. Food and Drug Administration. Bacteriologycal analytical manual online. Detection and enumeration of Listeria monocytogenes in foods. U.S.A: FDA, 2003. Fecha de consulta: 27 de mayo de 2009. Disponible en: http://www.fda.gov/food/scienceresearch/laboratorymethods/bacteriologicalanalyticalmanualbam/ucm071400.htm.
71. Food Drug and Administration. Método adaptado para detección de Listeria monocytogenes en carnes y derivados cárnicos, huevos, pollos: metodología de la Food Drug Administration para la detección de Listeria monocytogenes en alimentos. USA: BAM; 2003. p. 30.
72. Food and Agriculture Organization of the United Nations. World Health Organization. Codex Alimentarius commission. Annex II: Microbiological criterio for Listeria monocytogenes in ready-to-eat food. (CX /FH 08/40/5, October 2008). Codex Committee on Food Hygiene, fortieth session. Guatemala: FAO/WHO; 2008. p. 8.
73. Seeliger HP, Hönne K. Serotyping of Listeria monocytogenes and related species. Vol.13. In: Bergan T, Novis J, eds. Methods in microbiology. Capítulo 11. London, New York: Academic Press, 1979. p.31-49
74. Institut Pasteur. Centre National de Référence des Listeria. Centre collaborateur de L´oms pour la listeriose d´origene alimentaire. Laboratoire des Listeria. Protocole de serotypie. Paris: Institut Pasteur, 1997 : 22p.
75. Departamento Administrativo Nacional de Estadística. Necesidades básicas insatisfechas -NBI. Bogotá: Dane, 2008. Fecha de consulta: 10 de junio de 2010. Disponible en: http: // www.dane.gov.co/daneweb_VO9/index.php.
76. República de Colombia. Departamento Nacional de Planeación. Consejo Nacional de Política Económica y Salud. Documento Conpes 3375. Política nacional de sanidad agropecuaria e inocuidad de alimentos para el sistema de medidas sanitarias y fitosanitarias. Bogotá D. C: DNP, 2005. 39p.
How to Cite
1.
Muñoz AI, Vargas M, Otero L, Díaz G, Guzmán V. Presence of Listeria monocytogenes in ready-to-eat foods available in open markets, delicatessens and supermarkets, Bogotá, 2002-2008. biomedica [Internet]. 2011 Mar. 31 [cited 2024 May 17];31(3):428-39. Available from: https://revistabiomedica.org/index.php/biomedica/article/view/394
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