Calidad microbiológica de ensaladas de verduras listas para comer servidas en restaurantes de carne durante la pandemia de COVID-19 en Turquia
Resumen
Ensaladas de verduras listas–para–comer (EVLC) que se sirven con pita/lahmacun, tipos de kebab y tantuni de origen animal en los asadores de la cocina turca, ya que tienen el potencial de conllevar riesgos en términos de salud pública fueron evaluadas. Se investigaron las propiedades microbiológicas de REVS utilizando el método de placa de agar. La resistencia a los antimicrobianos de los patógenos transmitidos por los alimentos, incluidos Escherichia coli y Staphylococcus aureus, se probó mediante método de difusión por disco de Kirby–Bauer. Además, se detectó la presencia de importantes virus entéricos por Reacción en Cadena de la Polimerasa (RCP). El número de bacterias aeróbicas totales, bacterias coliformes, levaduras y mohos y Staphylococcus y Micrococcus spp. varió de menos de 1 a 6,40; 1 a 6,26; menos de 1 a 5,82 y de menos de 1 a 5,66 log10 Unidades Formadoras de Colonias·gramos-1 (UFC·g–1) en muestras EVLC, respectivamente. Ninguna muestra de EVLC analizadas en este estudio contenía Salmonella spp., mientras que E. coli y S. aureus se aislaron en el 38,1 % (16/42) y el 2,4 % (1/42), respectivamente. S. aureus fue resistente a la gentamicina, la kanamicina, el aztreonam y la ciprofloxacina en el ensayo de difusión en disco; sin embargo, no albergaba el gen mecA. Las cepas de E. coli (n=16) fueron resistentes (100 %) a los antibióticos aminoglucósidos y el 35,7 % (6/16) de los aislamientos produjeron beta lactamasa de espectro extendido (BLEE). blaTEM y blaCTXM8/25 se detectaron en dos aislados, mientras que un aislado portaba blaCTXM–1 y blaTEM juntos mediante RCP. De los EVLC, dos fueron evaluados como positivos para rotavirus (5 %), seis para hepatitis A (14 %), y virus de la hepatitis E (14 %). Estos resultados indican la alta carga de microorganismos, presencia de ESBL E. coli y patógenos virales entéricos en REVS, por lo que es importante realizar prácticas de higiene de rutina.
Descargas
Citas
ABADIAS, M.; USALL, J.; ANGUERA, M.; SOLSONA, C.; VIÑAS, I. Microbiological quality of fresh, minimally–processed fruit and vegetables, and sprouts from retail establishments. Int. J. Food Microbiol. 123: 121–129. 2008.
ABAKARI, G.; COBBINA, S.J.; YELELIERE, E. Microbial quality of ready–to–eat vegetable salads vended in the central business district of Tamale, Ghana. Int. J. Food Contam. 5: 3. 2018.
ABAY, S.; IRKIN, R.; AYDIN, F.; MÜŞTAK, H.K.; DIKER, K.S. The prevalence of major foodborne pathogens in ready–to–eat chicken meat samples sold in retail markets in Turkey and the molecular characterization of the recovered isolates. LWT–Food Sci. Technol. 81: 202–209. 2017.
AHMED, S.; SIDDIQUE, M.A.; RAHMAN, M.; BARI, M.L.; FERDOUSI, S. A study on the prevalence of heavy metals, pesticides, and microbial contaminants and antibiotics resistance pathogens in raw salad vegetables sold in Dhaka, Bangladesh. Heliyon. 5: e01205. 2019.
AKTAŞ, O.; AYDIN, H.; TIMURKAN, M.O. A molecular study on the prevalence and coinfections of Rotavirus, Norovirus, Astrovirus and Adenovirus in children with gastroenteritis. Minerva Pediatr. 71: 431–437. 2019.
ALMUALLA, N.A.; LALEYE, L.C.; ABUSHELAIBI, A.A.; AL–QASSEMI, R.A.; WASESA, A.A.; BABOUCARR, J. Aspects of the microbiological quality and safety of ready–to–eat foods in Sharjah supermarkets in the United Arab Emirates. J. Food Prot. 73: 1328–1331. 2010.
ANDREWS, W.; HAMMACK, T. Chapter 5: Salmonella. 2007. US Food and Drug Administration (FDA) Bacteriological Analytical Manual (BAM). Online: https://bit.ly/3MjbSdi. 02–12–2021
AYCICEK, H.; CAKIROGLU, S.; STEVENSON, T.H. Incidence of Staphylococcus aureus in ready–to–eat meals from military cafeterias in Ankara, Turkey. Food Control. 16: 531–534. 2005.
AYDIN, H.; UYANIK, M.H.; KARAMESE, M.; TIMURKAN, M.O. Seroprevalence of hepatitis e virus in animal workers in nonporcine consumption region of Turkey. Future Virol. 11: 691–697. 2016.
BARAN, A.; ADıGÜZEL, M.C.; YÜKSEL, M. Prevalence of antibiotic–resistant and extended–spectrum beta–lactamase–producing Escherichia coli in chicken meat from eastern Turkey. Pak. Vet. J. 40: 355–359. 2020.
BARAN, A.; ERDOĞAN, A.; KAVAZ, A.; ADIGÜZEL, M.C. Some specific microbiological parameters and prevalence of Salmonella spp. in retail chicken meat from Erzurum Province, Turkey and characterization of antibiotic resistance of isolates. Biosci. J. 35: 878–891. 2019.
BAUTISTA‐DE LEÓN, H.; GÓMEZ‐ALDAPA, C.; RANGEL‐VARGAS, E.; VÁZQUEZ‐BARRIOS, E.; CASTRO‐ROSAS, J. Frequency of indicator bacteria, Salmonella and diarrhoeagenic Escherichia coli pathotypes on ready‐to‐eat cooked vegetable salads from M exican restaurants. Lett. Appl. Microbiol. 56: 414–420. 2013.
BENCARDINO, D.; VITALI, L.A.; PETRELLI, D. Microbiological evaluation of ready–to–eat iceberg lettuce during shelf–life and effectiveness of household washing methods. Ital. J. Food Saf. 7: 50–54. 2018.
CAMPOS, J.; MOURÃO, J.; PESTANA, N.; PEIXE, L.; NOVAIS, C.; ANTUNES, P. Microbiological quality of ready–to–eat salads: An underestimated vehicle of bacteria and clinically relevant antibiotic resistance genes. Int. J. Food Microbiol. 166: 464–470. 2013.
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. Microbiological quality of ready–to–eat vegetables collected in Mexico City: occurrence of aerobic–mesophilic bacteria, fecal coliforms, and potentially pathogenic nontuberculous mycobacteria. Biomed Res. Int. 2015: 789508. 2015.
CHAU, M.L.; AUNG, K.T.; HAPUARACHCHI, H.C.; LEE, P.S.V.; LIM, P.Y.; KANG, J.S.L.; NG, Y.; YAP, H.M.; YUK, H.-G.; GUTIÉRREZ, R.A. Microbial survey of ready–to–eat salad ingredients sold at retail reveals the occurrence and the persistence of Listeria monocytogenes Sequence Types 2 and 87 in pre–packed smoked salmon. BMC Microbiol. 17: 1–13. 2017.
CHENG, D.; ZOU, S.; LIAO, N.; SHI, X.; CHEN, J.; ZHANG, Y.; SUN, L.; ZHANG, R. Evaluation of an Extraction Method for the Detection of GI and GII Noroviruses in Fruit and Vegetable Salads. J. Food Sci. 83: 393–400. 2018.
CLERMONT, O.; BONACORSI, S.; BINGEN, E. Rapid and simple determination of the Escherichia coli phylogenetic group. Am. Soc. Mirobiol. 66: 4555–4558. 2000.
COULIBALY–KALPY, J.; AGBO, E.A.; DADIE, T.A.; DOSSO, M. Microbiological quality of raw vegetables and ready to eat products sold in Abidjan (Côte d'Ivoire) markets. Afr. J. Microbiol. Res. 11: 204–210. 2017.
EMILSE, P.V.; MATÍAS, V.; CECILIA, M.L.; OSCAR, G.M.; GISELA, M.; GUADALUPE, D.; ELIZABETH, R.V.; VICTORIO, P.J.; RODNEY, C.; VIVIANA, N.S.; ANGÉLICA, B.P. Enteric virus presence in green vegetables and associated irrigation waters in a rural area from Argentina. A quantitative microbial risk assessment. LWT–Food Sci. Technol. 144: 111201. 2021.
EVELYNE, T.; ATTIEN, P.; MOROH, A.J. L.; HAZIZ, S.; KOUAME, D.N.; KAMBIRE, O.; BABA–MOUSSA, L.; GUESSENND, N.; DAKO, E.; DADIE, A.T. Prevalence and characterization of Salmonella isolated from vegetables salads and ready to eat raw mixed vegetable salads in Abidjan, Cte dIvoire. J. Microbiol. Antimicrob. 14: 15–25. 2022.
FAOUR–KLINGBEIL, D.; MURTADA, M.; KURI, V.; TODD, E.C.D. Understanding the routes of contamination of ready–to–eat vegetables in the Middle East. Food Control. 62: 125–133. 2016.
FINDIK, A.; AKAN, N.; ONUK, E.E.; ÇAKIROĞLU, D.; CIFTCI, A. Methicillin resistance profile and molecular typing of Staphylococcus aureus strains isolated from noses of the healthy dogs. Kafkas Univ. Vet. Fak. Derg. 15: 925–930. 2009.
FREITAG, C.; MICHAEL, G.; LI, J.; KADLEC, K.; WANG, Y.; HASSEL, M.; SCHWARZ, S. Occurrence and characterisation of ESBL–encoding plasmids among Escherichia coli isolates from fresh vegetables. Vet. Microbiol. 219: 63–69. 2018.
GILBERT, R.; DE LOUVOIS, J.; DONOVAN, T.; LITTLE, C.; NYE, K.; RIBEIRO, C.; RICHARDS, J.; ROBERTS, D.; BOLTON, F. Guidelines for the microbiological quality of some ready–to–eat foods sampled at the point of sale. PHLS Advisory Committee for Food and Dairy Products. Commun. Dis. Pub. Healt. 3: 163–167. 2000.
GIRI, S.; KUDVA, V.; SHETTY, K.; SHETTY, V. Prevalence and Characterization of Extended–Spectrum β–Lactamase–Producing Antibiotic–Resistant Escherichia coli and Klebsiella pneumoniae in Ready–to–Eat Street Foods. Antibiotics. 10: 850–850. 2021.
GÓMEZ–ALDAPA, C.A.; RANGEL–VARGAS, E.; CASTRO–ROSAS, J. Frequency and Correlation of Some Enteric Indicator Bacteria and Salmonella in Ready–to–Eat Raw Vegetable Salads from Mexican Restaurants. J. Food Sci. 78: M1201–M1207. 2013.
GURLER, Z.; PAMUK, S.; YILDIRIM, Y.; ERTAS, N. The microbiological quality of ready–to–eat salads in Turkey: A focus on Salmonella spp. and Listeria monocytogenes. Int. J. Food Microbiol. 196: 79–83. 2015.
HUANG, F.F.; HAQSHENAS, G.; GUENETTE, D.K.; HALBUR, P.G.; SCHOMMER, S.K.; PIERSON, F.W.; TOTH, T.E.; MENG, X.J. Detection by reverse transcription–PCR and genetic characterization of field isolates of swine hepatitis E virus from pigs in different geographic regions of the United States. J. Clin. Microbiol. 40: 1326–1332. 2002.
GLOBAL MARKET RESEARCH AND PUBLIC OPINION SPECIALIST (IPSOS). Beverage products drew attention in the purchase of fast moving consumer goods in the household. 2020. Online: https://bit.ly/3TcnS2w. 02–02–2022.
JANALÍKOVÁ, M.; PLEVA, P.; PAVLÍČKOVÁ, S.; LECOMTE, M.; GODILLON, T.; HOLKO, I. Characterization of Escherichia coli strains isolated from raw vegetables. Potr. S. J. F. Sci. 12: 304–312. 2018.
KHAN, W.; IRSHAD, M.; REHMAN, G.; HUSSAIN, A. HAV in fresh vegetables: a hidden health risk in district Mardan, Pakistan. SpringerPlus. 3: 675. 2014.
KIM, J.S.; BANG, O.K.; CHANG, H.C. Examination of microbiological contamination of ready–to–eat vegetable salad. J. Food Hyg. Saf. 19: 60–65. 2004.
LAMMIE, S.L.; HUGHES, J.M. Antimicrobial resistance, food safety, and one health: the need for convergence. Annu. Rev. Food Sci. Technol. 7: 287–312. 2016.
LE, Q.P.; UEDA, S.; NGUYEN, T.N.H.; DAO, T.V.K.; VAN HOANG, T.A.; TRAN, T.T.N.; HIRAI, I.; NAKAYAMA, T.; KAWAHARA, R.; DO, T.H. Characteristics of extended–spectrum β–lactamase–producing Escherichia coli in retail meats and shrimp at a local market in Vietnam. Foodborne Pathog. Dis. 12: 719–725. 2015.
LIU, S.; KILONZO–NTHENGE, A. Prevalence of multidrug–resistant bacteria from US–grown and imported fresh produce retailed in chain supermarkets and ethnic stores of Davidson County, Tennessee. J. Food Prot. 80: 506–514. 2017.
MAKINDE, O.M.; AYENI, K.I.; SULYOK, M.; KRSKA, R.; ADELEKE, R.A.; EZEKIEL, C.N. Microbiological safety of ready–to–eat foods in low–and middle–income countries: A comprehensive 10–year (2009 to 2018) review. Compr. Rev. Food Sci. 19: 703–732. 2020.
MERCANOGLU–TABAN, B.; HALKMAN, A.K. Do leafy green vegetables and their ready–to–eat [RTE] salads carry a risk of foodborne pathogens? Anaerobe. 17: 286–287. 2011.
MIR, S.A.; SHAH, M.A.; MIR, M.M.; DAR, B.N.; GREINER, R.; ROOHINEJAD, S. Microbiological contamination of ready–to–eat vegetable salads in Developing Countries and potential solutions in the supply chain to control microbial pathogens. Food Control. 85: 235–244. 2018.
NAJAFI, H.; MOHAMMAD, B.; BAHREINI, M. Microbiological quality of mixed fresh–cut vegetable salads and mixed ready–to–eat fresh herbs in Mashhad, Iran. Intern. Conf. Nutr. Food Sci. 39: 62–66. 2012.
PAMUK, Ş.; GÜRLER, Z.; YILDIRIM, Y.; ERTAŞ, N.J.K.U.V.F.D. The microbiological quality of ready to eat salads sold in Afyonkarahisar, Turkey. Kafkas Univ. Vet. Fakult. Dergisi 19: 1001–1006. 2013.
PARADA–FABIÁN, J.C.; JUÁREZ–GARCÍA, P.; NATIVIDAD–BONIFACIO, I.; VÁZQUEZ–SALINAS, C.; QUIÑONES–RAMÍREZ, E.I. Identification of Enteric Viruses in Foods from Mexico City. Food Environ. Virol. 8: 215–220. 2016.
PELLICER, K.; COPES, J.; MALVESTITI, L.; ECHEVERRÍA, M.G.; NOSETTO, E.O.; STANCHI, N.O. Ready to eat salads: an analysis of health and safety conditions. Analecta Vet. 22: 4–6. 2002.
PINGULKAR, K.; KAMAT, A.; BONGIRWAR, D. Microbiological quality of fresh leafy vegetables, salad components and ready–to–eat salads: an evidence of inhibition of Listeria monocytogenes in tomatoes. Int. J. Food Sci. Nutr. 52: 15–23. 2001.
PURPARI, G.; MACALUSO, G.; DI BELLA, S.; GUCCIARDI, F.; MIRA, F.; DI MARCO, P.; LASTRA, A.; PETERSEN, E.; LA ROSA, G.; GUERCIO, A. Molecular characterization of human enteric viruses in food, water samples, and surface swabs in Sicily. Int. J. Infect. Dis. 80: 66–72. 2019.
RACHIDA, S.; TAYLOR, M.B. Potentially Infectious Novel Hepatitis A Virus Strains Detected in Selected Treated Wastewater Discharge Sources, South Africa. Viruses. 12: 1468. 2020.
RAHMAN, M.; ALAM, M.–U.; LUIES, S.K.; KAMAL, A.; FERDOUS, S.; LIN, A.; SHARIOR, F.; KHAN, R.; RAHMAN, Z.; PARVEZ, S.M. Contamination of fresh produce with antibiotic–resistant bacteria and associated risks to human health: A scoping review. Int. J. Environ. Res. Public Health. 19: 360. 2021.
RODRÍGUEZ–LÁZARO, D.; ŁEPECKA, A.; ZIELÍNSKA, D.; SZYMÁNSKI, P.; BURAS, I.; KOŁO, D. Assessment of the Microbiological Quality of Ready–to–Eat Salads–Are There Any Reasons for Concern about Public Health? Int. J. Environ. Res. Public Health. 19: 1582–1582. 2022.
SAKSENA, R.; MALIK, M.; GAIND, R. Bacterial contamination and prevalence of antimicrobial resistance phenotypes in raw fruits and vegetables sold in Delhi, India. J. Food Saf. 40: e12739. 2020.
SALLEH, N.A.; RUSUL, G.; HASSAN, Z.; REEZAL, A.; ISA, S.H.; NISHIBUCHI, M.; RADU, S. Incidence of Salmonella spp. in raw vegetables in Selangor, Malaysia. Food Control. 14: 475–479. 2003.
ŞANLıBABA, P.; TEZEL, B.U.; ÇAKMAK, G.A. Prevalence and antibiotic resistance of Listeria monocytogenes isolated from ready–to–eat foods in Turkey. J. Food Qual. 2018: 7693782. 2018.
SAPKOTA, S.; ADHIKARI, S.; PANDEY, A.; KHADKA, S.; ADHIKARI, M.; KANDEL, H.; PATHAK, S. Multi–drug resistant extended–spectrum beta–lactamase producing E. coli and Salmonella spp. on raw vegetable salads served at hotels and restaurants in Bharatpur, Nepal. BMC Res. Notes. 12: 1–6. 2019.
SARKAR, C.; WEBSTER, C.; GALLACHER, J. Are exposures to ready–to–eat food environments associated with type 2 diabetes? A cross–sectional study of 347 551 UK Biobank adult participants. Lancet Planet. Health. 2: e438–e450. 2018.
SEO, Y. H.; JANG, J. H.; MOON, K. D.J.F.S. Occurrence and characterization of enterotoxigenic Staphylococcus aureus isolated from minimally processed vegetables and sprouts in Korea. Food Sci. Biotechnol. 19: 313–319. 2010.
SHAH, M.S.; EPPINGER, M.; AHMED, S.; SHAH, A.A.; HAMEED, A.; HASAN, F. Multidrug–resistant diarrheagenic E. coli pathotypes are associated with ready–to–eat salad and vegetables in Pakistan. J. Appl. Biol. Chem. 58: 267–273. 2015.
SHIN, H.; PARK, H.; SEO, D.J.; JUNG, S.; YEO, D.; WANG, Z.; PARK, K.H.; CHOI, C. Foodborne Viruses Detected Sporadically in the Fresh Produce and Its Production Environment in South Korea. Foodborne Pathog. Dis. 16: 411–420. 2019.
TABAN, B.M.; AYTAC, S.A.; AKKOC, N.; AKCELIK, M. Characterization of antibiotic resistance in Salmonella enterica isolates determined from ready–to–eat (RTE) salad vegetables. Braz. J. Microbiol. 44: 385–391. 2013.
TERIO, V.; BOTTARO, M.; PAVONI, E.; LOSIO, M.N.; SERRAINO, A.; GIACOMETTI, F.; MARTELLA, V.; MOTTOLA, A.; DI PINTO, A.; TANTILLO, G. Occurrence of hepatitis A and E and norovirus GI and GII in ready–to–eat vegetables in Italy. Int. J. Food Microbiol. 249: 61–65. 2017.
TURKISH FOOD CODEX (TFC). Microbiological Criteria Notification. T.C. Resmi Gazete. 2009: 62001. 2009.
TIMURKAN, M.; AYDIN, H.; AKTAŞ, O. Frequency and molecular characterization of human norovirus in Erzurum, Turkey. Turk. J. Med. Sci. 47: 960–966. 2017.
USUI, M.; OZEKI, K.; KOMATSU, T.; FUKUDA, A.; TAMURA, Y. Prevalence of extended–spectrum β–lactamase–producing bacteria on fresh vegetables in Japan. J. Food Prot. 82: 1663–1666. 2019.
VAN DER POEL, W.H.M. Food and environmental routes of Hepatitis E virus transmission. Curr. Opin. Virol. 4: 91–96. 2014.
VERRAES, C.; VAN BOXSTAEL, S.; VAN MEERVENNE, E.; VAN COILLIE, E.; BUTAYE, P.; CATRY, B.; DE SCHAETZEN, M. A.; VAN HUFFEL, X.; IMBERECHTS, H.; DIERICK, K. Antimicrobial resistance in the food chain: a review. Int. J. Environ. Res. Public Health. 10: 2643–2669. 2013.
WAYNE, P. Clinical and Laboratory Standards Institute. Performance standards for antimicrobial susceptibility testing; CLSI supplement M100. Pp. 362. 2019.
XYLIA, P.; BOTSARIS, G.; CHRYSARGYRIS, A.; SKANDAMIS, P.; TZORTZAKIS, N. Variation of microbial load and biochemical activity of ready–to–eat salads in Cyprus as affected by vegetable type, season, and producer. Food Microbiol. 83: 200–210. 2019.
YANG, J.; ZHANG, Z.; ZHOU, X.; CUI, Y.; SHI, C.; SHI, X. Prevalence and characterization of antimicrobial resistance in Salmonella enterica isolates from retail foods in Shanghai, China. Foodborne Pathog. Dis. 17: 35–43. 2020.
YILMAZ, A.; BOSTAN, K.; ALTAN, E.; MURATOGLU, K.; TURAN, N.; TAN, D.; HELPS, C.; YILMAZ, H. Investigations on the frequency of norovirus contamination of ready–to–eat food items in Istanbul, Turkey, by using real–time reverse transcription PCR. J. Food Prot. 75: 840–843. 2011.
Derechos de autor 2022 Alper Baran, Mehmet Cemal Adigüzel, Hakan Aydin
Esta obra está bajo licencia internacional Creative Commons Reconocimiento-NoComercial-CompartirIgual 4.0.