Comparison of the antimicrobial activities of roselle calyx extracts and chemical sanitizers directly onto contaminated cucumbers

Main Article Content

C.A. Gómez-Aldapa
M.R. Torres-Vitela
E. Rangel-Vargas
A. Villaruel-López
N.A. Santiesteban-López
A.M. Cruz-Gálvez
J. Castro-Rosas

Keywords

disinfection, roselle, Hibiscus sabdariffa, antibacterial, cucumber, Cucumis sativus

Abstract

Cucumbers are associated with foodborne disease caused by Salmonella. Fruits and vegetables in restaurants and homes in Mexico are disinfected using sodium hypochlorite and colloidal silver solution. However, a number of studies show that chemical agents used to eliminate pathogenic bacteria have a limited antimicrobial effect. Previous studies show that roselle calyx extracts have antimicrobial effects. Therefore, the present study examined the attachment of 14 foodborne bacteria to whole cucumber in the presence of Hibiscus sabdariffa calyx extracts, sodium hypochlorite, acetic acid, and colloidal silver. Cucumbers were inoculated with 14 bacteria: Listeria monocytogenesShigella flexneriStaphylococcus aureusSalmonella Typhimurium, Salmonella Typhi, Salmonella Montevideo, Salmonella Choleraesuis, Escherichia coli O157:H7, non-O157:H7-Shiga toxin-producing E. coli, enteropathogenic E. coli, enterotoxigenic E. coli, enteroinvasive E. coli, enteroaggregative E. coli, and Vibrio cholerae O1. The antibacterial effect of four roselle calyx extracts (in water, methanol, acetone, and ethyl acetate) and some chemical sanitisers including sodium hypochlorite, colloidal silver, and acetic acid were then examined. All foodborne bacteria successfully attached to cucumber. The acetonic and methanolic roselle extracts caused a greater reduction (up to 4 log cfu in some cases) in the concentration of all foodborne bacteria than sodium hypochlorite, colloidal silver, and acetic acid. Thus, roselle calyx extracts may be a potentially useful disinfectant for cucumbers in the field, in processing plants, and in restaurants and homes.

Abstract 473 | PDF Downloads 458

References

Aguilar, B.S., Giono, C.S. and Costarica, G.M., 1982. Phage typing of Staphylococcus aureus strains isolated from foods and patients with a clinical picture of food poisoning. Salud Pública de México 25: 419-421.
Alam, M., Rashed, S.M., Mannan, S.B., Islam, T., Lizarraga-Partida, M.L., Delgado, G., Morales-Espinosa, R., Mendez, J.L., Navarro, A., Watanabe, H., Ohnishi, M., Hasan, N.A., Huq, A., Sack, R.B., Colwell, R.R. and Cravioto, A., 2014. Occurrence in Mexico, 1998-2008, of Vibrio cholerae CTX+ El Tor carrying an additional truncated CTX prophage. Proceedings of the National Academy of Sciences 111: 9917-9922.
Ali, B.H., Al Wabel, N. and Blunden, G., 2005. Phytochemical, pharmacological and toxicological aspects of Hibiscus sabdariffa L.: a review. Phytotherapy Research 19: 369-375.
Al-Zenki, S., Al-Omirah, H. and Sidhu, J.S., 2012. Microbial safety and sanitation of fruits and fruit products. In: Sinha, N., Sidhu, J., Barta, J., Wu, J. and Cano, P. (eds.) Handbook of fruits and fruit processing (2nd Ed.). Wiley-Blackwell, Hoboken, NJ, USA, pp. 333-351.
Angelo, K.M., Chu, A., Anand, M., Nguyen, T.A., Bottichio, L., Wise, M., Williams, I., Seelman, S., Bell, R., Fatica, M., Lance, S., Baldwin, D., Shannon, K., Lee, H., Trees, E., Strain, E. and Gieraltowski, L., 2015. Outbreak of Salmonella Newport infections linked to cucumbers – United States, 2014. Morbidity and Mortality Weekly Report 64: 144-147.
Bautista-De León, H., Gómez-Aldapa, C.A., Rangel-Vargas, E., Vázquez-Barrios, E. and Castro-Rosas, J., 2013. Frequency of indicator bacteria, Salmonella and diarrhoeagenic Escherichia colipathotypes on ready-to-eat cooked vegetable salads from Mexican restaurants. Letters in Applied Microbiology 56: 414-420.
Beuchat, L.R. and Ryu, J.H., 1997. Produce handling and processing practices. Emerging Infectious Diseases 3: 459.
Beuchat, L.R. and Scouten, A.J., 2002. Combined effects of water activity, temperature and chemical treatments on the survival of Salmonella and Escherichia coli O157:H7 on alfalfa seeds. Journal of Applied Microbiology 92: 382-395.
Borrás-Linares, I., Fernández-Arroyo, S., Arráez-Roman, D., Palmeros-Suárez, P.A., Del Val-Díaz, R., Andrade-Gonzáles, I., Fernández-Gutiérrez A., Gómez-Leyva J.F. and Segura-Carretero, A., 2015. Characterization of phenolic compounds, anthocyanidin, antioxidant and antimicrobial activity of 25 varieties of Mexican Roselle (Hibiscus sabdariffa). Industrial Crops and Products 69: 385-394.
Castro-Rosas, J. and Escartin, E.F., 1999. Incidence and germicide sensitivity of Salmonella typhi and Vibrio cholerae O1 in alfalfa sprouts. Journal of Food Safety 19: 137-146.
Castro-Rosas, J. and Escartin, E.F., 2002. Adhesion and colonization of Vibrio cholerae O1 on shrimp and crab carapace. Journal of Food Protection 65: 492-498.
Castro-Rosas, J., Cerna-Cortes, J.F., Méndez-Reyes, E., Lopez-Hernandez, D., Gómez-Aldapa, C.A. and Estrada-García, T., 2012. Presence of faecal coliforms, Escherichia coli and diarrheagenic E. coli pathotypes in ready-to-eat salads, from an area where crops are irrigated with untreated sewage water. International Journal of Food Microbiology 156: 176-180.
Castro-Rosas, J., Gomez-Aldapa, C.A., Acevedo-Sandoval, O.A., Gonzalez-Ramirez, C.A., Villagomez-Ibarra, J.R., Chavarria-Hernandez, N., Villarruel-Lopez, A. and Torres-Vitela, M.R., 2011. Frequency and behavior of Salmonella and Escherichia coli on whole and sliced jalapeno and serrano peppers. Journal of Food Protection 74: 874-881.
Castro-Rosas, J., Santos-López, E.M., Gómez-Aldapa, C.A., González-Ramírez, C.A., Villagomez-Ibarra, J.R., Gordillo-Martínez., A.J., López, V.A. and Torres-Vitela, M.D., 2010. Incidence and behavior of Salmonella and Escherichia coli on whole and sliced zucchini squash (Cucurbita pepo) fruit. Journal of Food Protection 73: 1423-1429.
Centers for Disease Control and Prevention (CDC), 2013. Multistate outbreak of Salmonella Saintpaul infections linked to imported cucumbers. CDC, Atlanta, GA, USA. Available at: http://tinyurl.com/ybone9rr
Centers for Disease Control and Prevention (CDC), 2015. Multistate outbreak of Salmonella Poona infections linked to imported cucumbers. CDC, Atlanta, GA, USA. Available at: http://tinyurl.com/yc2rc7ud
Cerna-Cortes, J.F., Gómez-Aldapa, C.A., Rangel-Vargas, E., Ramirez-Cruz, E. and Castro-Rosas, J., 2013. Presence of indicator bacteria, Salmonella and diarrheagenic Escherichia coli pathotypes on mung bean sprouts from public markets in Pachuca, Mexico. Food Control 31: 280-283.
Cerna-Cortes, J.F., Gómez-Aldapa, C.A., Rangel-Vargas, E., Torres-Vitela, M.R., Villarruel-López, A. and Castro-Rosas, J., 2012. Presence of some indicator bacteria and diarrheagenic E. colipathotypes on jalapeno and serrano peppers from popular markets in Pachuca City, Mexico. Food Microbiology 32: 444-447.
Chao, C.Y. and Yin, M.C., 2008. Antibacterial effects of roselle calyx extracts and protocatechuic acid in ground beef and apple juice. Foodborne Pathogens and Disease 6: 201-206.
Choi, S.Y., Rashed, S.M., Hasan, N.A., Alam, M., Islam, T., Sadique, A., Johura, F.T., Eppinger, M., Ravel, J., Huq, A., Cravioto, A. and Colwel, R.R., 2016. Phylogenetic diversity of Vibrio cholerae associated with endemic cholera in Mexico from 1991 to 2008. mBio 7: e02160-15.
Code of Federal Regulation (CFR), 2017. §172.510 Natural flavoring substances and natural substances used in conjunction with flavors. Federal Register, Washington, DC, USA. Available at: http://tinyurl.com/yce5dyo2
Comisión Federal para la Protección contra Riesgos Sanitarios (COFEPRIS), 2015. 6 pasos de la salud con prevención. Secretaría de Salud, Mexico. COFEPRIS, Mexico City, Mexico. Available at: http://tinyurl.com/y8fletqm
Estrada-Garcia, T., Lopez-Saucedo, C., Thompson-Bonilla, R., Abonce, M., Lopez-Hernandez, D., Santos, J.I., Rosado, J.L., Dupont, H.L. and Long, K.Z., 2009. Association of diarrheagenic Escherichia colipathotypes with infection and diarrhea among Mexican children and association of atypical enteropathogenic E. coli with acute diarrhea. Journal of Clinical Microbiology 47: 93-98.
Flisser, A., Velasco-Villa, A., Martínez-Campos, C., González-Domínguez, F., Briseño-García, B., García-Suárez, R., Caballero-Servín, A., Hernández-Monroy, I., García-Lozano, H., Gutiérrez-Cogco, L., Rodríguez-Angeles, G., López-Martínez, I., Galindo-Virgen, S., Vázquez-Campuzano, R., Balandrano-Campos, S., Guzmán-Bracho, C., Olivo-Díaz, A., De la Rosa, J., Magos, C., Escobar-Gutiérrez, A. and Correa, D., 2002. Infectious diseases in Mexico. A survey from 1995-2000. Archives of Medical Research 33: 343-350.
García-Gómez, R., Chávez-Espinosa, J., Mejía-Chávez, A. and Duran-de-Bazua, C., 2002. Microbiological determinations of some vegetables from the Xochimilco zone in Mexico City, Mexico. Revista Latinoamericana de Microbiología 44: 24-30.
Gil, M.I., Selma, M.V., López-Gálvez, F. and Allende, A., 2009. Fresh-cut product sanitation and wash water disinfection: problems and solutions. International Journal of Food Microbiology 134: 37-45.
Gómez-Aldapa, C.A., Cerna-Cortes, J.F., Rangel-Vargas, E., Torres-Vitela, M.R., Villarruel-López, A., Gutiérrez-Alcántara, E.J. and Castro-Rosas, J., 2016a. Presence of multidrug-resistant Shiga toxin-producing Escherichia coli, enteropathogenic E. coli and enterotoxigenic E. coli, on raw nopalitos (Opuntia ficus-indicaL.) and in Nopalitos salads from local retail markets in Mexico. Foodborne Pathogens and Disease13: 269-274.
Gómez-Aldapa, C.A., Segovia-Cruz, J.A., Cerna-Cortes, J.F., Rangel-Vargas, E., Salas-Rangel, L.P., Gutiérrez-Alcántara, E.J. and Castro-Rosas, J., 2016b. Prevalence and behavior of multidrug-resistant Shiga toxin-producing Escherichia coli, enteropathogenic E. coli and enterotoxigenic E. coli on coriander. Food Microbiology 59: 97-103.
Greenberg, A.E., Clesceri, L.S. and Eaton, A.D., 1992. Standard methods for the examination of water and wastewater (18th Ed.). American Public Health Association, Washington, DC, USA.
Gutiérrez-Alcántara, E.J., Gómez-Aldapa, C.A., Román-Gutiérrez, A.D., Rangel-Vargas, E., González-Olivares, L.G. and Castro-Rosas, J., 2016a. Antimicrobial activity of roselle Hibiscus Sabdariffa calyx extracts on culture media and carrots against multidrug-resistant Salmonella strains isolated from raw carrots. Journal of Food Safety 36: 450-458.
Gutiérrez-Alcántara, E.J., Rangel-Vargas, E., Gómez-Aldapa, C.A., Falfan-Cortes, R.N., Rodríguez-Marín, M.L., Godínez-Oviedo, A., Cortes-López, H. and Castro-Rosas, J., 2016b. Antibacterial effect of roselle extracts (Hibiscus sabadariffa), sodium hypochlorite and acetic acid against multidrug-resistant Salmonella strains isolated from tomatoes. Letters in Applied Microbiology62: 177-184.
91Higginbotham, K.L., Burris, K.P., Zivanovic, S., Davidson, P.M. and Stewart Jr., C.N., 2014a. Antimicrobial activity of Hibiscus sabdariffa aqueous extracts against Escherichia coli O157:H7 and Staphylococcus aureus in a microbiological medium and milk of various fat concentrations. Journal of Food Protection 77: 262-268.
Higginbotham, K.L., Burris, K.P., Zivanovic, S., Davidson, P.M. and Stewart, C.N., 2014b. Aqueous extracts of Hibiscus sabdariffa calyces as an antimicrobial rinse on hot dogs against Listeria monocytogenesand methicillin-resistant Staphylococcus aureus. Food Control 40: 274-277.
Jaroni, D. and Ravishankar, S., 2012. Bactericidal effects of roselle (Hibiscus sabdariffa) against foodborne pathogens in vitro and on romaine lettuce and alfalfa sprouts. Quality Assurance and Safety of Crops & Foods4: 33-40.
Jeffree, C.E., 2008. The fine structure of the plant cuticle. In: Riederer, M. and Müller, C. (eds.) Annual plant reviews. Vol. 23. Biology of the plant cuticle. Blackwell Publishing, Oxford, UK.
Jung, J., 2015. Quantification of Salmonella transfer from cucumber skin to flesh and peeler during peeling. In: International Association for Food Protection (ed.) Proceedings of the Annual Meeting of IAFP, July 31-August 3, 2015, St. Louis, MO, USA, pp. 89.
Liu, K.S., Tsao, S.M. and Yin, M.C., 2005. In vitro antibacterial activity of roselle calyx and protocatechuic acid. Phytotherapy Research 19: 942-945.
Moore, K.L., Patel, J., Jaroni, D., Friedman, M. and Ravishankar, S., 2011. Antimicrobial activity of apple, hibiscus, olive, and hydrogen peroxide formulations against Salmonella enterica on organic leafy greens. Journal of Food Protection 74: 1676-1683.
Mounnissamy, V.M., Kavimani, S. and Gunasegaran, R., 2002. Antibacterial activity of gossypetin isolated from Hibiscus sabdariffa. Antiseptic: Journal of Medicine and Surgery 99: 81-82.
Mrityunjoy, A., Kaniz, F., Fahmida, J., Shanzida, J.S., Aftab, U.M. and Rashed, N., 2013. Prevalence of Vibrio cholerae in different food samples in the city of Dhaka, Bangladesh. International Food Research Journal 20: 1017-1222.
Ölmez, H. and Kretzschmar, U., 2009. Potential alternative disinfection methods for organic fresh-cut industry for minimizing water consumption and environmental impact. LWT – Food Science and Technology42: 686-693.
Parrilla, M.C., Vázquez, J.L., Saldate, E.O. and Nava, L.M., 1993. Brotes de toxiinfecciones alimentarias de origen microbiano y parasitario. Salud Pública de México35: 456-463.
Quiroz-Santiago, C., Rodas-Suárez, O.R., Carlos, R.V., Fernández, F.J., Quiñones-Ramírez, E.I. and Vázquez-Salinas, C., 2009. Prevalence of Salmonella in vegetables from Mexico. Journal of Food Protection 72: 1279-1282.
Rangel-Vargas, E., Gómez-Aldapa, C.A., Torres-Vitela, M.R., Villarruel-López, A., Gordillo-Martínez, A.J. and Castro-Rosas, J., 2015. Presence of non-O157 Shiga toxin-producing Escherichia coli, enterotoxi-genic E. coli, enteropathogenic E. coli and Salmonellaserotypes on alfalfa sprouts. Journal of Food Protection 78: 609-614.
Secretaría de Salud, 2015. Concentrado de materiales educativos y de comunicación de riesgos. Secretaría de Salud. Mexico City, Mexico. Available at: http://tinyurl.com/y9zzrb3h
Secretaría de Salud, 2016. Enfermedades infecciosas y parasitarias del aparato digestivo. Boletín epidemiológico. Sistema Nacional de Vigilancia Epidemiológica, Mexico City, Mexico. Available at: http://tinyurl.com/y9amwjrg
Sepulveda, J., Valdespino, J.L. and Garcia-Garcia, L., 2006. Cholera in Mexico: the paradoxical benefits of the last pandemic. International Journal of Infectious Diseases 10: 4-13.
Soto Beltran, M., Jimenez Edeza, M., Viera, C., Martinez, C.I. and Chaidez, C., 2013. Sanitizing alternatives for Escherichia coli and Salmonella Typhimurium on bell peppers at household kitchens. International Journal of Environmental Health Research 23: 331-341.
Torres-Vitela, M.R., Gómez-Aldapa, C.A., Cerna-Cortes, J.F., Villarruel-López, A., Rangel-Vargas, E. and Castro-Rosas, J., 2013. Presence of indicator bacteria, diarrheagenic E. coli pathotypes and Salmonellain fresh carrot juice from Mexican restaurants. Letters in Applied Microbiology56: 180-185.