Presence of indicator bacteria, Shiga toxin-producing Escherichia coli, and nontuberculous mycobacteria in oregano
DOI:
https://doi.org/10.5327/fst.27923Palavras-chave:
oregano, microbiological quality, shiga toxin-producing E. coli, nontuberculous mycobacteriaResumo
Limited data are available regarding microbial contamination in oregano. This study aimed to evaluate the microbiological quality and presence of diarrheagenic Escherichia coli pathotypes and nontuberculous mycobacteria (NTM) in 85 oregano samples purchased from different markets in Mexico City. All samples analyzed were positive for aerobic-mesophilic bacteria, with limits ranging from 1.14 to 6.5 log CFU/g. A total of 67, 41, and 9 samples were positive for total coliforms, fecal coliforms, and E. coli, respectively, present at concentrations ranging from <3 to >1,100 MPN/g. One sample harbored Shiga toxin-producing E. coli strains positive for the Shiga toxin 2 (stx2) locus at a concentration of 3 MPN/g. NTM species were recovered from 15 samples and included M. fortuitum (six), M. smegmatis (two), M. conceptionense (one), M. porcinum (one), M. parafortuitum (one), M. flavescens (one), M. goodii (one), and two strains that could not be identified. Measures to diminish the high levels of microorganisms and pathogenic bacteria in this food item might be advisable. Good hygiene practices, good manufacturing practices, and hazard analysis and critical control points must be applied throughout the chain of production to ensure the safety of oregano.
Downloads
Referências
Adekambi, T., Colson, P., & Drancourt, M. (2003). rpoB-based identification of nonpigmented and late-pigmenting rapidly growing mycobacteria. Journal of Clinical Microbiology, 41(12), 5699-5708. https://doi.org/10.1128/JCM.41.12.5699-5708.2003
Angulo, C. A., Flores, J. D. A., Tejeida, J. C., & Ocampo, V. R. (2004). Oregano: oro verde del semidesierto. In Lopez, C., Chanfon, S., Segura, G., eds. La riqueza de los bosques mexicanos: mas alla de la madera, experiencias de comunidades rurales (pp. 60-65). SEMARNAT.
Argueta, C., Yoder, S., Holtzman, A. E., Aronson, T. W., Glover, N., Berlin, O. G., Stelma, G. N., Jr., Froman, S., & Tomasek, P. (2000). Isolation and identification of nontuberculous mycobacteria from foods as possible exposure sources. Journal of Food Protection, 63(7), 930-933. https://doi.org/10.4315/0362-028x-63.7.930
Cerna, J. F., Nataro, J. P., & Estrada-Garcia, T. (2003). Multiplex PCR for detection of three plasmid-borne genes of enteroaggregative Escherichia coli strains. Journal of Clinical Microbiology, 41(5), 2138-2140. https://doi.org/10.1128/JCM.41.5.2138-2140.2003
Cerna-Cortes, J. F., Cortes-Cueto, A. L., Cano-Gaona, M. R., Leon-Montes, N., Helguera-Repetto, A. C., Rivera-Gutierrez, S., Salas-Rangel, L. P., Castro-Rosas, J., & Gonzalez, Y. M. J. A. (2016). Microbiological quality and occurrence of nontuberculous mycobacteria in fresh-squeezed orange juice samples purchased from street vendors in Mexico City. Journal of Food Protection, 79(12), 2190-2195. https://doi.org/10.4315/0362-028X.JFP-16-197
Cerna-Cortes, J. F., Cortes-Cueto, A. L., Villegas-Martinez, D., Leon-Montes, N., Salas-Rangel, L. P., Rivera-Gutierrez, S., Lopez-Hernandez, D., Helguera-Repetto, A. C., Fernandez-Rendon, E., & Gonzalez, Y. M. J. A. (2019). Bacteriological quality of bottled water obtained from Mexico City small water purification plants: Incidence and identification of potentially pathogenic nontuberculous mycobacteria species. International Journal of Food Microbiology, 306, 108260. https://doi.org/10.1016/j.ijfoodmicro.2019.108260
Cerna-Cortes, J. F., Leon-Montes, N., Cortes-Cueto, A. L., Salas-Rangel, L. P., Helguera-Repetto, A. C., Lopez-Hernandez, D., Rivera-Gutierrez, S., Fernandez-Rendon, E., & Gonzalez-y-Merchand, J. A. (2015). Microbiological quality of ready-to-eat vegetables collected in mexico city: Occurrence of aerobic-mesophilic bacteria, fecal coliforms, and potentially pathogenic nontuberculous mycobacteria. BioMed Research International, 2015, 789508. https://doi.org/10.1155/2015/789508
Cobos-Marin, L., Montes-Vargas, J., Rivera-Gutierrez, S., Licea-Navarro, A., Gonzalez-y-Merchand, J. A., & Estrada-Garcia, I. (2003). A novel multiplex-PCR for the rapid identification of Mycobacterium bovis in clinical isolates of both veterinary and human origin. Epidemiology and Infection, 130(3), 485-490. https://doi.org/10.1017/s095026880300829x
Dinh Thanh, M., Frentzel, H., Fetsch, A., Krause, G., Appel, B., & Mader, A. (2018). Tenacity of Bacillus cereus and Staphylococcus aureus in dried spices and herbs. Food Control, 83, 75-84. https://doi.org/10.1016/j.foodcont.2016.12.027
Donohue, M. J. (2018). Increasing nontuberculous mycobacteria reporting rates and species diversity identified in clinical laboratory reports. BMC Infectious Diseases, 18(1), 163. https://doi.org/10.1186/s12879-018-3043-7
EFSA BIOHAZ Panel, Koutsoumanis, K., Allende, A., Alvarez-Ordóñez, A., Bover-Cid, S., Chemaly, M., Davies, R., De Cesare, A., Herman, L., Hilbert, F., Lindqvist, R., Nauta, M., Peixe, L., Ru, G., Simmons, M., Skandamis, P., Suffredini, E., Jenkins, C., Monteiro Pires, S., Morabito, S., Niskanen, T., Scheutz, F., da Silva, F. M. T., Messens, W, & Bolton, D. (2020). Pathogenicity assessment of shiga toxin-producing Escherichia coli (STEC) and the public health risk posed by contamination of food with STEC. European Food Safety Authority Journal, 18(1), e05967. https://doi.org/10.2903/j.efsa.2020.5967
Escobar-Escamilla, N., Ramirez-Gonzalez, J. E., Gonzalez-Villa, M., Torres-Mazadiego, P., Mandujano-Martinez, A., Barron-Rivera, C., Backer, C. E., Fragoso-Fonseca, D. E., Olivera-Diaz, H., Alcantara-Perez, P., Hernandez-Solis, A., Cicero-Sabido, R., & Cortes-Ortiz, I. A. (2014). hsp65 phylogenetic assay for molecular diagnosis of nontuberculous mycobacteria isolated in Mexico. Archives of Medical Research, 45(1), 90-97. https://doi.org/10.1016/j.arcmed.2013.12.004
Falkinham, J. O., 3rd. (2021). Ecology of nontuberculous mycobacteria. Microorganisms, 9(11), 2262. https://doi.org/10.3390/microorganisms9112262
Falkinham, J. O., 3rd. (2022). Nontuberculous mycobacteria in the environment. Tuberculosis, 137, 102267. https://doi.org/10.1016/j.tube.2022.102267
Food and Agriculture Organization (FAO), & World Health Organization (WHO). (2022). Control measures for Shiga toxin-producing Escherichia coli (STEC) associated with meat and dairy products. Meeting report. Retrieved from https://www.fao.org/documents/card/en/c/cc2402en
Frentzel, H., Kraushaar, B., Krause, G., Bodi, D., Wichmann-Schauer, H., Appel, B., & Mader, A. (2018). Phylogenetic and toxinogenic characteristics of Bacillus cereus group members isolated from spices and herbs. Food Control, 83, 90-98. https://doi.org/10.1016/j.foodcont.2016.12.022
Garbowska, M., Berthold-Pluta, A., & Stasiak-Rozanska, L. (2015). Microbiological quality of selected spices and herbs including the presence of Cronobacter spp. Food Microbiology, 49, 1-5. https://doi.org/10.1016/j.fm.2015.01.004
Garcia, S., Iracheta, F., Galvan, F., & Heredia, N. (2001). Microbiological survey of retail herbs and spices from Mexican markets. Journal of Food Protection, 64(1), 99-103. https://doi.org/10.4315/0362-028x-64.1.99
Gobierno de Mexico (2013). Crea INIFAP nueva tecnología para la producción de orégano resistente a fenómenos climáticos. Retrieved from https://www.gob.mx/agricultura%7Csanluispotosi/es/articulos/crea-inifap-nueva-tecnologia-para-la-produccion-de-oregano-resistente-a-fenomenos-climaticos-140314
Gomes, T. A., Elias, W. P., Scaletsky, I. C., Guth, B. E., Rodrigues, J. F., Piazza, R. M., Ferreira, L. C., & Martinez, M. B. (2016). Diarrheagenic Escherichia coli. Brazilian Journal of Microbiology, 47(Suppl. 1), 3-30. https://doi.org/10.1016/j.bjm.2016.10.015
Huerta, C. (1997). Oregano mexicano: oro vegetal. Biodiversitas, 15, 8-13.
Jarchow-MacDonald, A., Smith, M., Seagar, A. L., Russell, C. D., Claxton, P., Laurenson, I. F., & Moncayo-Nieto, O. L. (2023). Changing incidence and characteristics of nontuberculous mycobacterial infections in Scotland and comparison with Mycobacterium tuberculosis complex incidence (2011 to 2019). Open Forum Infectious Diseases, 10(1), ofac665. https://doi.org/10.1093/ofid/ofac665
Jesser, K. J., & Levy, K. (2020). Updates on defining and detecting diarrheagenic Escherichia coli pathotypes. Current Opinion in Infectious Diseases, 33(5), 372-380. https://doi.org/10.1097/QCO.0000000000000665
Kendall, B. A., & Winthrop, K. L. (2013). Update on the epidemiology of pulmonary nontuberculous mycobacterial infections. Seminars in Respiratory and Critical Care Medicine, 34(1), 87-94. https://doi.org/10.1055/s-0033-1333567
Kim, H. J., & Song, W. J. (2023). Inactivation of Escherichia coli O157: H7 in foods by emerging technologies: a review. Letters in Applied Microbiology, 76(1), ovac007. https://doi.org/10.1093/lambio/ovac007
Kirschner, P., Springer, B., Vogel, U., Meier, A., Wrede, A., Kiekenbeck, M., Bange, F. C., & Bottger, E. C. (1993). Genotypic identification of mycobacteria by nucleic acid sequence determination: report of a 2-year experience in a clinical laboratory. Journal of Clinical Microbiology, 31(11), 2882-2889. https://doi.org/10.1128/jcm.31.11.2882-2889.1993
Koh, W. J. (2013). Epidemiology of pulmonary non-tuberculous mycobacterial infections: Need to identify environmental sources. International Journal of Tuberculosis and Lung Disease, 17(6), 713. https://doi.org/10.5588/ijtld.13.0289
Kumar, C., Shrivastava, K., Singh, A., Chauhan, V., & Varma-Basil, M. (2021). Skin and soft-tissue infections due to rapidly growing mycobacteria: An overview. International Journal of Mycobacteriology, 10(3), 293-300. https://doi.org/10.4103/ijmy.ijmy_110_21
Liu, Y., Thaker, H., Wang, C., Xu, Z., & Dong, M. (2022). Diagnosis and treatment for shiga toxin-producing Escherichia coli associated hemolytic uremic syndrome. Toxins, 15(1), 10. https://doi.org/10.3390/toxins15010010
Lopez-Luis, B. A., Sifuentes-Osornio, J., Perez-Gutierrez, M. T., Chavez-Mazari, B., Bobadilla-Del-Valle, M., & Ponce-de-Leon, A. (2020). Nontuberculous mycobacterial infection in a tertiary care center in Mexico, 2001-2017. Brazilian Journal of Infectious Diseases, 24(3), 213-220. https://doi.org/10.1016/j.bjid.2020.04.012
Lopez-Saucedo, C., Cerna, J. F., Villegas-Sepulveda, N., Thompson, R., Velazquez, F. R., Torres, J., Tarr, P. I., & Estrada-Garcia, T. (2003). Single multiplex polymerase chain reaction to detect diverse loci associated with diarrheagenic Escherichia coli. Emerging Infectious Diseases, 9(1), 127-131. https://doi.org/10.3201/eid0901.010507
Marochi-Telles, J. P., Muniz, R., Jr., Sztajnbok, J., & Cosme-de Oliveira, A. (2020). Disseminated Mycobacterium avium on HIV/AIDS: Historical and current literature review. AIDS Reviews, 22(1), 9-15. https://doi.org/10.24875/AIDSRev.20000104
Orona, C. I., Salvador, A. A. J., Espinoza, A. J. de J., Vázquez, C. (2017). Recoleccion y comercializacion del oregano (Lippia spp) en el semi-desierto mexicano, un caso de estudio: reserva ecologica municipal sierra y cañon de Jimulco, Mexico. Revista Mexicana de Agronegocios, 41, 684-695. Retrieved from https://www.redalyc.org/journal/141/14153918003/html/
Pafumi, J. (1986). Assessment of the microbiological quality of spices and herbs. Journal of Food Protection, 49(12), 958-963. https://doi.org/10.4315/0362-028X-49.12.958
Pascual, M. E., Slowing, K., Carretero, E., Sanchez Mata, D., & Villar, A. (2001). Lippia: traditional uses, chemistry and pharmacology: a review. Journal of Ethnopharmacology, 76(3), 201-214. https://doi.org/10.1016/s0378-8741(01)00234-3
Patzi-Vargas, S., Zaidi, M., Bernal-Reynaga, R., Leon-Cen, M., Michel, A., & Estrada-Garcia, T. (2013). Persistent bloody diarrhoea without fever associated with diffusely adherent Escherichia coli in a young child. Journal of Medical Microbiology, 62(12), 1907-1910. https://doi.org/10.1099/jmm.0.062349-0
Pavlik, I., Ulmann, V., & Falkinham, J. O., 3rd. (2022a). Nontuberculous mycobacteria: Ecology and impact on animal and human health. Microorganisms, 10(8), 1516. https://doi.org/10.3390/microorganisms10081516
Pavlik, I., Ulmann, V., Hubelova, D., & Weston, R. T. (2022b). Nontuberculous mycobacteria as sapronoses: A review. Microorganisms, 10(7), 1345. https://doi.org/10.3390/microorganisms10071345
Pavlik, I., Ulmann, V., & Weston, R. T. (2021). Clinical relevance and environmental prevalence of Mycobacterium fortuitum group members. comment on mugetti et al. gene sequencing and phylogenetic analysis: powerful tools for an improved diagnosis of fish mycobacteriosis caused by Mycobacterium fortuitum group members. Microorganisms, 9(11), 2345. https://doi.org/10.3390/microorganisms9112345
Rivero-Cruz, I., Duarte, G., Navarrete, A., Bye, R., Linares, E., & Mata, R. (2011). Chemical composition and antimicrobial and spasmolytic properties of Poliomintha longiflora and Lippia graveolens essential oils. Journal of Food Science, 76(2), C309-317. https://doi.org/10.1111/j.1750-3841.2010.02022.x
Sospedra, I., Soriano, J. M., & Manes, J. (2010). Assessment of the microbiological safety of dried spices and herbs commercialized in Spain. Plant Foods for Human Nutrition, 65(4), 364-368. https://doi.org/10.1007/s11130-010-0186-0
Telenti, A., Marchesi, F., Balz, M., Bally, F., Bottger, E. C., & Bodmer, T. (1993). Rapid identification of mycobacteria to the species level by polymerase chain reaction and restriction enzyme analysis. Journal of Clinical Microbiology, 31(2), 175-178. https://doi.org/10.1128/jcm.31.2.175-178.1993
Tong, T., Wang, P., Shi, H., Li, F., & Jiao, Y. (2022). Radio frequency inactivation of E. coli O157: H7 and Salmonella Typhimurium ATCC 14028 in black pepper (piper nigrum) kernels: Thermal inactivation kinetic study and quality evaluation. Food Control, 132, 108553. https://doi.org/10.1016/j.foodcont.2021.108553
U.S. Food and Drug Administration (2021). Bacteriological analytical manual. U.S. Food and Drug Administration. Retrieved from https://www.fda.gov/food/laboratory-methods-food/bacteriological-analytical-manual-bam
Wang, P. H., Pan, S. W., Wang, S. M., Shu, C. C., & Chang, C. H. (2022). The impact of nontuberculous mycobacteria species on mortality in patients with nontuberculous mycobacterial lung disease. Frontiers in Microbiology, 13, 909274. https://doi.org/10.3389/fmicb.2022.909274
Witkowska, A. M., Hickey, D. K., Alonso-Gomez, M., & Wilkinson, M. G. (2011). The microbiological quality of commercial herb and spice preparations used in the formulation of a chicken supreme ready meal and microbial survival following a simulated industrial heating process. Food Control, 22(3-4), 616-625. https://doi.org/10.1016/j.foodcont.2010.10.014
Yang, S. C., Lin, C. H., Aljuffali, I. A., & Fang, J. Y. (2017). Current pathogenic Escherichia coli foodborne outbreak cases and therapy development. Archives of Microbiology, 199(6), 811-825. https://doi.org/10.1007/s00203-017-1393-y
Yoder, S., Argueta, C., Holtzman, A., Aronson, T., Berlin, O. G., Tomasek, P., Glover, N., Froman, S., & Stelma, G., Jr. (1999). PCR comparison of Mycobacterium avium isolates obtained from patients and foods. Applied and Environmental Microbiology, 65(6), 2650-2653. https://doi.org/10.1128/AEM.65.6.2650-2653.1999
