Salmonella and other enterobacteria isolated from fresh meat of rattlesnake Crotalus spp
Main Article Content
Abstract
Fresh rattlesnake meat is consumed as food by some people. It’s known that Salmonella exists in some reptiles including rattlesnakes; however, the microbiological quality of fresh meat is unknown. Therefore the main objective of this study is to determine the presence of Salmonella associated with fresh rattlesnake meat, as well as recognized other enterobacteria species. Nine rattlesnakes were collected from the wild and samples were obtained from each individual for analysis. Salmonella colonies were isolated by NOM-114-SSA1-1994 methodology, then they were verified by the API-20E kit and VITEK-2 automated microbiology system. Eight samples (88.88%) resulted as Salmonella, 15 colonies were isolated by the first method. With API-20E kit and VITEK-2 the presence of Salmonella was confirmed in 11 strains from seven samples (77.33%). VITEK-2 was more specific determining Salmonella enterica ssp arizonae in seven strains from four samples of fresh rattlesnake meat. The results of this study can warn about the consumption of rattlesnake meat, thus, maybe decreased the anthropogenic impact over the rattlesnakes. In conclusion, Salmonella was isolated as well as other member of the Enterobacteriaceae from fresh rattlesnake meat samples. It’s recommended not to eat fresh rattlesnake meat because it represents a risk for human health. Complementary methods were useful for the determination of enterobacteria, especially Salmonella.
Article Details
How to Cite
Gatica-Colima, A. (2011). Salmonella and other enterobacteria isolated from fresh meat of rattlesnake Crotalus spp. Revista Latinoamericana De Recursos Naturales, 7(2), 78-88. Retrieved from https://revista.itson.edu.mx/index.php/rlrn/article/view/194
Section
Original Article
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.
References
Aiken, A. M., Lane, C. y Adak, G. K., 2010. Risk of Salmonella infection with exposure to reptiles in England, 2004-2007. Euro Surveill (en http:/www.eurosurveillance.org).
Almeida, C., Schuch, D., Gelli, D., Cuéllar, J., Diez, A. y Escamilla, J., 1996. Contaminación microbiana de los alimentos vendidos en la vía pública: en ciudades de América Latina y características socio-económicas de sus vendedores y consumidores. Pan American Health Organization, World Health Organization, Pan American Sanitary Bureau.
Analytab, 1989. API-20E Analytical Profile Index, Enterobacteriaceae and other Gram-negative bacteria. 9 ed. (actualización V9.1). Analytab Products. Plain View, N. Y.
Babu, K., Sonnenberg, M., Kathpalia, S., Ortega, P., Swiatlo, A. y Kocka, F., 1990. Isolation of Salmonella from dried rattlesnake preparations. Journal of Clinical Microbiology, 28: 361-362.
Caldwell, M. E. y Ryerson, D., 1939. Salmonellosis in certain reptiles. The Journal of Infectious Diseases, 65(3): 242-245.
Chiodini, R. J., 1982. Transovarian passage, visceral distribution, and pathogenicity of Salmonella in snakes. Infection and Immunity, 36: 710-713.
Chiodini, R. J. y Sundberg, J. P., 1981. Salmonellosis in reptiles: a review. American Journal of Epidemiology, 113: 494-499.
Corrente, M., Madio, A., Friedrich, K. G., Greco, G., Desario, C., Tagliabue, S., D’Incau, M., Campolo, M. y Buonavoglia, C., 2004. Isolation of Salmonella strains from reptile faeces and comparison of different culture media. Journal of Applied Microbiology, 96: 709-715.
Croop, J. M., Shapiro, B., Alpert, G., Campos, J. M. y Zavod, W., 1984. Arizona hinshawii osteomyelitis associated with a pet snake. Pediatric Infectious Disease Journal, 3: 188.
Diario Oficial de la Federación (DOF). 2002. Norma Oficial Mexicana NOM-114-SSA1-1994, Bienes y servicios. Método para la determinación de Salmonella en alimentos.
Diario Oficial de la Federación (DOF). 2010. Norma Oficial Mexicana NOM-059-SEMARNAT-2010, Protección ambiental-Especies nativas de México de flora y fauna silvestres-Categorías de riesgo y especificaciones para su inclusión, exclusión o cambio-Lista de especies en riesgo. México, D. F.
Edel, W. y Kampelmacher, E. H., 1969. Salmonella isolation in nine European laboratories using a standardized technique. Bulletin World Health Organization, 41(2): 297-306.
Farmer, J. J. III., Davis, B. R., Hickman-Brenner, F. W., McWhorter, A., Huntley-Carter, G. P., Asbury, M. A., Riddle, C., Wathen-Grady, H. G., Elias, C., Fanning, G. R., Steigerwalt, A. G., O’Hara, C. M., Morris, G. K., Smith, P. B. y Brenner, D. J., 1985. Biochemical identification of new species and biogroups of Enterobacteriaceae isolated from clinical specimens. Journal of Clinical Microbiology, 21: 46-76.
Ferreira, R. Jr., Siqueira, A., Campagner, M., Salerno, T., Soares, T., Lucheis, S., Paes, A. y Barraviera, B., 2009. Comparison of wildlife and captivity rattlesnakes (Crotalus durissus terrificus) microbiota. Pesquisa Veterinária Brasileira, 29: 999-1003.
Fitzgerald, L., Painter, C. W., Reuter, A. y Hoover, C., 2004. Collection, Trade, and Regulation of Reptiles and Amphibians of the Chihuahuan Desert Ecoregion. TRAFFIC North America. World Wildlife Fund, Washington, D. C.
Goldstein, E., Citron, D., González, H. y Russell, F., 1979. Bacteriology of rattlesnake venom and implications for theraphy. The Journal of Infectious Diseases, 140: 818-821.
Goyan, P. y Sucher, K., 1990. Diet counseling in a multicultural society. The Diabetes Educator, 16: 127-131.
Herrera-Arias, F. C. y Santos-Buelga, J. A., 2005. Prevalencia de Salmonella spp en pescado fresco expedido en Pamplona (Norte de Santander). Bistua, 3(2): 34-42.
Hoff, G. y White, F. H., 1977. Salmonella in reptiles: Isolation from free-ranging lizards (Reptilia, Lacertilia) in Florida. Journal of Herpetology, 11: 123-129.
Holt, J., Krieg, N., Sneath, P., Staley, J. y Williams, S., 1994. Bergey’s Manual of Determinative Bacteriology. Ninth edition. Lippincott Williams & Wilkins. Wolters Kluwer Co., Philadelphia.
Klauber, L. M., 1982. Rattlesnakes. Their Habits, Life Histories, and Influence on Mankind. University of California Press. Berkeley, Los Angeles, CA.
Magnino, S., Colin, P., Dei-Cas, E., Madsen, M., McLauchlin, J., Nöckler, K., Prieto-Maradona, M., Tsigarida, E., Vanopdenbosh, E. y Van Peteghem, C., 2009. Biological risks associated with consumption of reptile products. International Journal of Food Microbiology, 134: 163-175.
Martínez-Barreda, C., Gallegos-Antúnez, D. C., Bar, W., Márquez de Bar, G., Fernández-Cano, R. y Ruíz-Reyes, G., 1999. Reptiles “mascotas”: una fuente potencial de infecciones por Salmonella. Enfermedades Infecciosas y Microbiología, 19: 266-269.
Mathewson, J. J., 1979. Enterobacteriaceae Isolated from Iguanid Lizards of West-Central Texas. Applied and Environmental Microbiology, 38(3): 402-405.
Mermin, J., Hutwagner, L., Vugia, D., Shallow, S., Daily, P., Bender, J., Koehler, J., Marcus, R. y Angulo F., 2004. Reptiles, Amphibians, and Human Salmonella Infection: A Population-Based, Case-Control Study. Clinical Infectious Diseases, 38 (Suppl 3): 253-261.
Mitchell, M. A. y Shane, S. M., 2001. Salmonella in Reptiles. Seminars in Avian and Exotic Pet Medicine, 10: 25-35.
Murphy, J. B. y Armstrong, B. L., 1978. Maintenance of Rattlesnake in Captivity. University of Kansas Museum of Natural History. Special Publication No 3. Lawrence, Kansas.
Noskin, G. y Clarke, J., 1990. Salmonella arizonae Bacteremia as the presenting manifestation of human immunodeficiency virus infection following rattlesnake meat ingestion. Reviews of Infectious Diseases, 12: 514-517.
O’Hara, C. y Miller, J. M., 2003. Evaluation of the Vitek 2 ID-GNB Assay for Identification of Members of the Family Enterobacteriaceae and Other Nonenteric Gram-Negative Bacilli and Comparison with the Vitek GNI+ Card. Journal of Clinical Microbiology, 41(5): 2096-2101.
Pisani, G. y Villa, J., 1974. Guía de técnicas de preservación de anfibios y reptiles. Society for the Study of Amphibians and Reptiles. Miscellaneos Publications. No. 2, Lawrence, Kansas.
Pita-Fernández, S., Pérteagas-Díaz, S. y Valdés-Cañedo, F., 2004. Medidas de frecuencia de enfermedad. Fisterra (en http://www.fisterra.com/mbe/investiga/medidas_frecuencia/med_frec2.pdf).
Ramsey, E. C., Daniel, G. B., Tryon, B. W., Merryman, J. I., Morris, P. J. y Bemis. D. A., 2002. Osteomyelitis associated with Salmonella enterica ss arizonae in a colony of ridgenose rattlesnakes (Crotalus willardi). Journal of Zoo and Wildlife Medicine, 33: 301-310.
Readel, A., Phillips, C. A. y Goldberg, T., 2008. Absence of cloacal shedding of Salmonella in wild red-eared sliders (Trachemys scripta elegans). Herpetological Review, 39(4): 427-430.
Riley, K. B., Antoniskis, D., Maris, R. y Leedom, J. M., 1988. Rattlesnake capsules-associated Salmonella arizona infections. Archives Internal Medicine, 148: 1207-1210.
Robles-Reyes, R., Eusebio-Hernández, M. G. y Avilés-Ruiz, D., 2001. Evaluation of the RevealTM Quick Test for Salmonella detection in raw chicken meat. Revista Latinoamericana de Microbiología, 43(2): 76-83.
Rodríguez, M. O., 1996. Detección de Salmonella enterica subsp. arizonae como microbiota de serpientes en cautiverio mediante métodos microbiológicos convencionales e hibridización del ADN utilizando como sonda el gene ompC de Salmonella enterica subsp enterica serovar typhi. Tesis de Médico Veterinario Zootecnista, Universidad Nacional Autónoma de México. México, D.F.
Roggendorf, M. y Muller, H. E., 1976. Enterobakterien bei Reptilien. Zentbl. Bakt. Parasitkde. 1 (Abt. Orig. A), 236: 22-35.
Sadler, W. W., Brownell, J. R. y Fanelli, M. J., 1969. Influence of age and inoculum level on shed pattern of Salmonella typhimurium in chickens. Avian Dissease, 13: 793-803.
Schaefer, W. H., 1934. Diagnosis of sex in snakes. COPEIA, 4: 181.
Schmitt, M., 1952. “Meat’s Meat”: An account of the flesh-eating habits of western americans. Western Folklore, 11: 185-203.
Sheridan, B. S., Wilson, G. R. y Weldon, P. J., 1989. Aerobic bacteria from the skin of the rattlesnake, Crotalus atrox. Journal of Herpetolology, 23: 200-202.
Simonsen, B., Bryan F. L, Christian, J. H. B, Roberts, T. A., Tompkin, R. B. y Silliker, J. H., 1987. Report from the International Commission on Microbiological Specifications for Foods (ICMSF). Prevention and control of food-borne Salmonellosis through application of hazard analysis critical point (HACCP). International Journal of Food Microbiology, 4: 227-247.
Turnbull, P. B. C., 1979. Food poisoning with special reference to Salmonella: its epidemiology, pathogenesis and control. Journal of Clinical Gastroenterology, 8: 663-714.
Varnam, A. H. y Evans, M. G., 1991. Food borne Pathogens. An Illustrated Text. Wolf Publishing. Ltd. London.
Waterman, S. H., Juárez, G., Carr, S. J. y Kilman, L., 1990. Salmonella arizona infections in Latinos associated with rattlesnake folk medicine. American Journal of Public Health, 80: 286-289.
Zaidi, M. B., McDermott, P. F., Fedorka-Cray, P., León, V., Canche, C., Hubert, S. K., Abbott, J., León, M., Zhao, S., Headrick M. y Tollefson, L., 2006. Nontyphoidal Salmonella from Human Clinical Cases, Asymtomatic Children, and Raw Retail Meats in Yucatan, México. Clinical Infectoius Diseases, 42: 21-28.
Almeida, C., Schuch, D., Gelli, D., Cuéllar, J., Diez, A. y Escamilla, J., 1996. Contaminación microbiana de los alimentos vendidos en la vía pública: en ciudades de América Latina y características socio-económicas de sus vendedores y consumidores. Pan American Health Organization, World Health Organization, Pan American Sanitary Bureau.
Analytab, 1989. API-20E Analytical Profile Index, Enterobacteriaceae and other Gram-negative bacteria. 9 ed. (actualización V9.1). Analytab Products. Plain View, N. Y.
Babu, K., Sonnenberg, M., Kathpalia, S., Ortega, P., Swiatlo, A. y Kocka, F., 1990. Isolation of Salmonella from dried rattlesnake preparations. Journal of Clinical Microbiology, 28: 361-362.
Caldwell, M. E. y Ryerson, D., 1939. Salmonellosis in certain reptiles. The Journal of Infectious Diseases, 65(3): 242-245.
Chiodini, R. J., 1982. Transovarian passage, visceral distribution, and pathogenicity of Salmonella in snakes. Infection and Immunity, 36: 710-713.
Chiodini, R. J. y Sundberg, J. P., 1981. Salmonellosis in reptiles: a review. American Journal of Epidemiology, 113: 494-499.
Corrente, M., Madio, A., Friedrich, K. G., Greco, G., Desario, C., Tagliabue, S., D’Incau, M., Campolo, M. y Buonavoglia, C., 2004. Isolation of Salmonella strains from reptile faeces and comparison of different culture media. Journal of Applied Microbiology, 96: 709-715.
Croop, J. M., Shapiro, B., Alpert, G., Campos, J. M. y Zavod, W., 1984. Arizona hinshawii osteomyelitis associated with a pet snake. Pediatric Infectious Disease Journal, 3: 188.
Diario Oficial de la Federación (DOF). 2002. Norma Oficial Mexicana NOM-114-SSA1-1994, Bienes y servicios. Método para la determinación de Salmonella en alimentos.
Diario Oficial de la Federación (DOF). 2010. Norma Oficial Mexicana NOM-059-SEMARNAT-2010, Protección ambiental-Especies nativas de México de flora y fauna silvestres-Categorías de riesgo y especificaciones para su inclusión, exclusión o cambio-Lista de especies en riesgo. México, D. F.
Edel, W. y Kampelmacher, E. H., 1969. Salmonella isolation in nine European laboratories using a standardized technique. Bulletin World Health Organization, 41(2): 297-306.
Farmer, J. J. III., Davis, B. R., Hickman-Brenner, F. W., McWhorter, A., Huntley-Carter, G. P., Asbury, M. A., Riddle, C., Wathen-Grady, H. G., Elias, C., Fanning, G. R., Steigerwalt, A. G., O’Hara, C. M., Morris, G. K., Smith, P. B. y Brenner, D. J., 1985. Biochemical identification of new species and biogroups of Enterobacteriaceae isolated from clinical specimens. Journal of Clinical Microbiology, 21: 46-76.
Ferreira, R. Jr., Siqueira, A., Campagner, M., Salerno, T., Soares, T., Lucheis, S., Paes, A. y Barraviera, B., 2009. Comparison of wildlife and captivity rattlesnakes (Crotalus durissus terrificus) microbiota. Pesquisa Veterinária Brasileira, 29: 999-1003.
Fitzgerald, L., Painter, C. W., Reuter, A. y Hoover, C., 2004. Collection, Trade, and Regulation of Reptiles and Amphibians of the Chihuahuan Desert Ecoregion. TRAFFIC North America. World Wildlife Fund, Washington, D. C.
Goldstein, E., Citron, D., González, H. y Russell, F., 1979. Bacteriology of rattlesnake venom and implications for theraphy. The Journal of Infectious Diseases, 140: 818-821.
Goyan, P. y Sucher, K., 1990. Diet counseling in a multicultural society. The Diabetes Educator, 16: 127-131.
Herrera-Arias, F. C. y Santos-Buelga, J. A., 2005. Prevalencia de Salmonella spp en pescado fresco expedido en Pamplona (Norte de Santander). Bistua, 3(2): 34-42.
Hoff, G. y White, F. H., 1977. Salmonella in reptiles: Isolation from free-ranging lizards (Reptilia, Lacertilia) in Florida. Journal of Herpetology, 11: 123-129.
Holt, J., Krieg, N., Sneath, P., Staley, J. y Williams, S., 1994. Bergey’s Manual of Determinative Bacteriology. Ninth edition. Lippincott Williams & Wilkins. Wolters Kluwer Co., Philadelphia.
Klauber, L. M., 1982. Rattlesnakes. Their Habits, Life Histories, and Influence on Mankind. University of California Press. Berkeley, Los Angeles, CA.
Magnino, S., Colin, P., Dei-Cas, E., Madsen, M., McLauchlin, J., Nöckler, K., Prieto-Maradona, M., Tsigarida, E., Vanopdenbosh, E. y Van Peteghem, C., 2009. Biological risks associated with consumption of reptile products. International Journal of Food Microbiology, 134: 163-175.
Martínez-Barreda, C., Gallegos-Antúnez, D. C., Bar, W., Márquez de Bar, G., Fernández-Cano, R. y Ruíz-Reyes, G., 1999. Reptiles “mascotas”: una fuente potencial de infecciones por Salmonella. Enfermedades Infecciosas y Microbiología, 19: 266-269.
Mathewson, J. J., 1979. Enterobacteriaceae Isolated from Iguanid Lizards of West-Central Texas. Applied and Environmental Microbiology, 38(3): 402-405.
Mermin, J., Hutwagner, L., Vugia, D., Shallow, S., Daily, P., Bender, J., Koehler, J., Marcus, R. y Angulo F., 2004. Reptiles, Amphibians, and Human Salmonella Infection: A Population-Based, Case-Control Study. Clinical Infectious Diseases, 38 (Suppl 3): 253-261.
Mitchell, M. A. y Shane, S. M., 2001. Salmonella in Reptiles. Seminars in Avian and Exotic Pet Medicine, 10: 25-35.
Murphy, J. B. y Armstrong, B. L., 1978. Maintenance of Rattlesnake in Captivity. University of Kansas Museum of Natural History. Special Publication No 3. Lawrence, Kansas.
Noskin, G. y Clarke, J., 1990. Salmonella arizonae Bacteremia as the presenting manifestation of human immunodeficiency virus infection following rattlesnake meat ingestion. Reviews of Infectious Diseases, 12: 514-517.
O’Hara, C. y Miller, J. M., 2003. Evaluation of the Vitek 2 ID-GNB Assay for Identification of Members of the Family Enterobacteriaceae and Other Nonenteric Gram-Negative Bacilli and Comparison with the Vitek GNI+ Card. Journal of Clinical Microbiology, 41(5): 2096-2101.
Pisani, G. y Villa, J., 1974. Guía de técnicas de preservación de anfibios y reptiles. Society for the Study of Amphibians and Reptiles. Miscellaneos Publications. No. 2, Lawrence, Kansas.
Pita-Fernández, S., Pérteagas-Díaz, S. y Valdés-Cañedo, F., 2004. Medidas de frecuencia de enfermedad. Fisterra (en http://www.fisterra.com/mbe/investiga/medidas_frecuencia/med_frec2.pdf).
Ramsey, E. C., Daniel, G. B., Tryon, B. W., Merryman, J. I., Morris, P. J. y Bemis. D. A., 2002. Osteomyelitis associated with Salmonella enterica ss arizonae in a colony of ridgenose rattlesnakes (Crotalus willardi). Journal of Zoo and Wildlife Medicine, 33: 301-310.
Readel, A., Phillips, C. A. y Goldberg, T., 2008. Absence of cloacal shedding of Salmonella in wild red-eared sliders (Trachemys scripta elegans). Herpetological Review, 39(4): 427-430.
Riley, K. B., Antoniskis, D., Maris, R. y Leedom, J. M., 1988. Rattlesnake capsules-associated Salmonella arizona infections. Archives Internal Medicine, 148: 1207-1210.
Robles-Reyes, R., Eusebio-Hernández, M. G. y Avilés-Ruiz, D., 2001. Evaluation of the RevealTM Quick Test for Salmonella detection in raw chicken meat. Revista Latinoamericana de Microbiología, 43(2): 76-83.
Rodríguez, M. O., 1996. Detección de Salmonella enterica subsp. arizonae como microbiota de serpientes en cautiverio mediante métodos microbiológicos convencionales e hibridización del ADN utilizando como sonda el gene ompC de Salmonella enterica subsp enterica serovar typhi. Tesis de Médico Veterinario Zootecnista, Universidad Nacional Autónoma de México. México, D.F.
Roggendorf, M. y Muller, H. E., 1976. Enterobakterien bei Reptilien. Zentbl. Bakt. Parasitkde. 1 (Abt. Orig. A), 236: 22-35.
Sadler, W. W., Brownell, J. R. y Fanelli, M. J., 1969. Influence of age and inoculum level on shed pattern of Salmonella typhimurium in chickens. Avian Dissease, 13: 793-803.
Schaefer, W. H., 1934. Diagnosis of sex in snakes. COPEIA, 4: 181.
Schmitt, M., 1952. “Meat’s Meat”: An account of the flesh-eating habits of western americans. Western Folklore, 11: 185-203.
Sheridan, B. S., Wilson, G. R. y Weldon, P. J., 1989. Aerobic bacteria from the skin of the rattlesnake, Crotalus atrox. Journal of Herpetolology, 23: 200-202.
Simonsen, B., Bryan F. L, Christian, J. H. B, Roberts, T. A., Tompkin, R. B. y Silliker, J. H., 1987. Report from the International Commission on Microbiological Specifications for Foods (ICMSF). Prevention and control of food-borne Salmonellosis through application of hazard analysis critical point (HACCP). International Journal of Food Microbiology, 4: 227-247.
Turnbull, P. B. C., 1979. Food poisoning with special reference to Salmonella: its epidemiology, pathogenesis and control. Journal of Clinical Gastroenterology, 8: 663-714.
Varnam, A. H. y Evans, M. G., 1991. Food borne Pathogens. An Illustrated Text. Wolf Publishing. Ltd. London.
Waterman, S. H., Juárez, G., Carr, S. J. y Kilman, L., 1990. Salmonella arizona infections in Latinos associated with rattlesnake folk medicine. American Journal of Public Health, 80: 286-289.
Zaidi, M. B., McDermott, P. F., Fedorka-Cray, P., León, V., Canche, C., Hubert, S. K., Abbott, J., León, M., Zhao, S., Headrick M. y Tollefson, L., 2006. Nontyphoidal Salmonella from Human Clinical Cases, Asymtomatic Children, and Raw Retail Meats in Yucatan, México. Clinical Infectoius Diseases, 42: 21-28.