Microbiological Quality of Ready-to-eat Salads from Processing Plant to the Consumers

Carmela Calonico^1, , Vania Delfino¹, Giovanna Pesavento¹, Maria Mundo¹ and Antonella Lo Nostro¹

¹Department of Health Sciences, University of Florence, 50134, Florence, Italy

Cite this paper:
Carmela Calonico, Vania Delfino, Giovanna Pesavento, Maria Mundo and Antonella Lo Nostro. Microbiological Quality of Ready-to-eat Salads from Processing Plant to the Consumers. Journal of Food and Nutrition Research. 2019; 7(6):427-434. doi: 10.12691/jfnr-7-6-3

Abstract

This study aimed to assess the microbiological quality of ready-to-eat salads (Aerobic Colony Count, E. coli, yeasts and moulds, S. aureus, Salmonella spp., L. monocytogenes, C. perfringens) and the effect of temperature abuse on the microbial count. Ready-to-eat salads samples were produced and commercialized in Italy and sampled, from January 2017 to January 2018, both at different steps of the production process in an industry (n = 300) and in different supermarkets (n = 270). The pathogenic foodborne microorganisms Salmonella spp., Listeria monocytogenes, S. aureus and Clostridium spp. were not detected and only 2.98% of the 570 samples were contaminated by E. coli, a good hygiene indicator of fecal contamination. Ready-to-eat salads samples from the industry were less contaminated, both in percentage and concentration, than the supermarket ones, particularly due to high Aerobic Colony Count values: on the day of collection, 80% samples from the industry were satisfactory, opposed to 8.3% from the retailers; at the end of shelf life, 20% samples from the industry were unsatisfactory, opposed to 80% from the retailers. Although washing salads before consumption is not effective to eliminate pathogens internalized within the plant’s tissues, our results showed that it was useful in reducing the microbiological load, especially E. coli count. This study revealed that high microbial content in retail ready-to-eat salads samples was principally due to microbial multiplication occurring during storage and transportation from industry to retailers and then at home. More frequent monitoring of storage and transport temperatures would be necessary to ensure the required hygienic quality, as well as it should be clear the writing on the packaging that “products must be kept at a maximum temperature of 8°C”.

Keywords:
ready-to-eat salads food safety microbiological quality temperature abuse foodborne pathogens

This work is licensed under a Creative Commons Attribution 4.0 International License. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/

Figures

References:

[1]	Pilone, V., Stasi, A. and Baselice, A., "Quality preferences and pricing of fresh-cut salads in Italy: new evidence from market data", British Food Journal. 2017, 119(7): 1473-1486.
[2]	Pinela, J., Barreira, J.C.M., Barros, L., Antonio, A.L., Carvalho, A.M., Oliveira, M.B.P.P. and Ferreira, I.C.F.R., “Postharvest quality changes in fresh-cut watercress stored under conventional and inert gas-enriched modified atmosphere packaging”, Postharvest Biology and Technology. 2016, 112: 55-63.
[3]	Brandao, M.L.L., Almeida, D.O., Bispo, F.C.P., Bricio, S.M.L., Marin, V.A. and Miagostovich, M.P., “Assessment of Microbiological Contamination of Fresh, Minimally Processed, and Ready-to-Eat Lettuces (Lactuca sativa), Rio de Janeiro State, Brazil”, Journal of Food Science. 2014, 79(5): M961-M966.
[4]	Italian Ministerial Decree n. 3746, “Attuazione dell’art. 4 della legge 13 maggio 2011 n. 77, recante disposizioni concernenti la preparazione, il confezionamento e la distribuzione dei prodotti ortofrutticoli di quarta gamma”, Gazzetta Ufficiale n. 186, 2014. Online. Available: https://www.politicheagricole.it/flex/cm/pages/ServeBLOB.php/L/IT/IDPagina/7763 Accessed 08 April 2019.
[5]	Hunter, P.J., Hand, P., Pink, D., Whipps, J. M. and Bending, G.D., “Both leaf properties and microbe-microbe interactions influence within species variation in bacterial population diversity and structure in the lettuce (Lactuca Species) phyllosphere”, Applied Environmental Microbiology. 2010, 76: 8117-8125.
[6]	Jay, J.M., Loessner, M.J. and Golden D.A., Modern Food Microbiology, 7th ed., Springer, 2009.
[7]	Erickson, M.C., Webb, C.C., Diaz-Perez, J.C., Phatak, S.C., Silvoy, J.J., Davey, L., Payton, A.S., Liao, J., Ma, L. and Doyle, M.P., “Surface and internalized Escherichia coli O157: H7 on field-grown spinach and lettuce treated with spray-contaminated irrigation water”, Journal of Food Protection. 2010, 73(6): 1023-1029.
[8]	Klerks, M.M., Franz, E., Van Gent-Pelzer, M., Zijlstra, C. and van Bruggen, A.H.C., “Differential interaction of Salmonella enteric serovars with lettuce cultivars and plant-microbe factors influencing the colonization efficiency”, The ISME Journal. 2007, 1(7): 620-631.
[9]	Klerks, M.M., Van Gent-Pelzer, M., Franz, E., Zijlstra, C. and Van Bruggen, A.H.C., “Physiological and molecular responses of Lactuca sativa to colonization by Salmonella enteric serovar Dublin”, Applied and Environmental Microbiology. 2007, 73(15): 4905-4914.
[10]	Meyer, K. M. and Leveau, J.H.J., “Microbiology of the phyllosphere: a playground for testing ecological concepts”, Oecologia. 2012, 168: 621-629.
[11]	Erickson, M.C., “Internalization of Fresh Produce by Foodborne Pathogens”, Annual Review of Food Science and Technology. 2012, 3: 283-310.
[12]	Niemira, B.A., “Relative efficacy of sodium hypochlorite wash versus irradiation to inactivate Escherichia coli O15: H7 internalized in leaves of Romaine lettuce and baby spinach”, Journal of Food Protection. 2007, 70(11): 2526-2532.
[13]	MacDonald, E., Einöder-Moreno, M., Borgen, K., Thorstensen Brandal, L., Diab, L., Fossli, Ø., Guzman Herrador, B., Hassan, A.A., Johannessen, G.S., Johansen, E.J., Jørgensen Kimo, R., Lier, T., Paulsen, B.L., Popescu, R., Tokle Schytte, C., Sæbø Pettersen, K., Vold, L., Ørmen, Ø., Wester, A.L., Wiklund, M. and Nygård, K., “National outbreak of Yersinia enterocolitica infections in military and civilian populations associated with consumption of mixed salad, Norway, 2014”, Euro Surveillance. 2016, 21: 34.
[14]	Vestrheim, D.F., Lange, H., Nygård, K., Borgen, K., Wester, A.L., Kvarme, M.L. and Vold, L., “Are ready-to-eat salads ready to eat? An outbreak of Salmonella Coeln linked to imported, mixed, pre-washed and bagged salad, Norway, November 2013”, Epidemiology and Infection. 2016, 144(8): 1756-60.
[15]	Centers for Disease Control and Prevention (CDC), “Multistate Outbreak of Listeriosis Linked to Packaged Salads Produced at Springfield, Ohio Dole Processing Facility (Final Update)”, 2016. Online. Available: https://www.cdc.gov/listeria/outbreaks/bagged-salads-01-16/index.html Accessed 08 April 2019
[16]	Stephan, R., Althaus, D., Kiefer, S., Lehner, A., Hatz, C., Schmutz, C., Jost, M., Gerber, N., Baumgartner, A., Hachler, H. and Mausezahl-Feuz, M., “Foodborne transmission of Listeria monocytogenes via ready-to-eat salad: A nationwide outbreak in Switzerland, 2013-2014”, Food Control. 2015, 57: 14-17.
[17]	Centers for Disease Control and Prevention (CDC), “Multistate Outbreak of Shiga toxin-producing Escherichia coli O157: H7 Infections Linked to Ready-to-Eat Salads (Final Update)”, 2013. Online. Available: http://www.cdc.gov/ecoli/2013/O157H7-11-13/index.html?s_cid=cs_002 Accessed 08 April 2019].
[18]	European Food Safety Authority and European Centre for Disease Prevention and Control, “The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2016”, EFSA Journal. 2017, 15(12): 5077.
[19]	Campos, J., Mourão, J., Pestana, N., Peixe, L., Novais, C. and Antunes, P., “Microbiological quality of ready-to-eat salads: an underestimated vehicle of bacteria and clinically relevant antibiotic resistance genes”, International Journal of Food Microbiology. 2013, 166(3): 464-470.
[20]	Mritunjay, S.K. and Kumar, V., “A study on prevalence of microbial contamination on the surface of raw salad vegetables”, 3 Biotech. 2017, 7(1): 13.
[21]	Althaus, D., Hofer, E., Corti, S., Julmi, A. and Stephan R., “Bacteriological Survey of Ready-to-Eat Lettuce, Fresh-Cut Fruit, and Sprouts Collected from the Swiss Market”, Journal of Food Protection. 2012, 75(7): 1338-1341.
[22]	Becker, B., Stoll, D., Schulz, P., Kulling, S. and Huch, M., “Microbial Contamination of Organically and Conventionally Produced Fresh Vegetable Salads and Herbs from Retail Markets in Southwest Germany”, Foodborne Pathogens and Disease. 2018.
[23]	Bencardino, D., Vitali, L.A. and Petrelli, D., “Microbiological evaluation of ready-to-eat iceberg lettuce during shelf-life and effectiveness of household washing methods”, Italian Journal of Food Safety. 2018, 7(1): 6913.
[24]	Fiedler, G., Kabisch, J., Bohnlein, C., Huch, M., Becker, B., Cho, G.S. and Franz, C.M.A.P., “Presence of Human Pathogens in Produce from Retail Markets in Northern Germany”, Foodborne Pathogens and Disease, 2017.
[25]	Ilyas, S., Qamar, M.U., Rasool, M.H., Abdulhaq, N. and Nawaz, Z., “Multidrug-resistant pathogens isolated from ready-to-eat salads available at a local market in Pakistan”, British Food Journal. 2016, 118(8): 2068-2075.
[26]	Marinelli, L., Maggi, O., Aurigemma, C., Tufi, D. and De Giusti, M., “Fresh vegetables and ready-to eat salad: phenotypic characterization of moulds and molecular characterization of yeasts”, Annali di Igiene: medicina preventiva e di comunità. 2012, 24(4): 301-309.
[27]	Mogren, L., Windstam, S., Boqvist, S., Vågsholm, I., Söderqvist, K., Rosberg, A.K., Lindén, J., Mulaosmanovic, E., Karlsson, M., Uhlig, E., Håkansson, A. and Alsanius, B., “The Hurdle Approach–A Holistic Concept for Controlling Food Safety Risks Associated With Pathogenic Bacterial Contamination of Leafy Green Vegetables”, Frontiers in microbiology. 2018, 9: 1965.
[28]	Codex Alimentarius Commission, “Recommended International Code of Practice General Principles of Food Hygiene CAC/RCP 1-1969”, Rev. 4-2003.
[29]	Kafetzopoulos, D.P., Psomas, E.L. and Kafetzopoulos, P.D., “Measuring the effectiveness of the HACCP Food Safety Management System”, Food Control. 2013, 33: 505-513.
[30]	Raspor, P., “Total food chain safety: how good practices can contribute?”, Trends in Food Science & Technology. 2008, 19: 405-412.
[31]	Italian Legislative Decree n. 31, “Decreto Legislativo 2 febbraio 2001, n. 31. Attuazione della direttiva 98/83/CE relativa alla qualità delle acque destinate al consumo umano”, Gazzetta Ufficiale 52, 41, 2001. Online. Available: http://www.camera.it/parlam/leggi/deleghe/01031dl.htm Accessed 08 April 2019.
[32]	European Commission, “Council Directive 98/83/EC, on the Quality of Water Intended for Human Consumption: calculation of derived activity concentrations”, Official Journal of the European Communities. 1998, L330: 32-54.
[33]	Amin, N., Olaimat, R. and Holley, A., “Factors influencing the microbial safety of fresh produce: A review”, Food Microbiology. 2012, 32(1): 1-19.
[34]	European Commission, “Commission Regulation No 2073 on microbiological criteria for foodstuffs”, Official Journal of the European Communities. 2005, L338: 1-26.
[35]	European Commission, “Commission Regulation No 852 on the hygiene of foodstuffs”, Official Journal of the European Communities. 2004, L139: 1-54.
[36]	Jol, S., Kassianenko, A., Wszol, K. and Oggel, J., “The Cold Chain, one link in Canada’s food safety initiatives”, Food Control. 2007, 18(6): 713-715.
[37]	Nieri, D., Pesavento, G., Ducci, B., Calonico, C. and Lo Nostro, A., "Monitoring of the cold chain compliance in a meal-processing facility through the correlation study between the outdoor temperatures and coliforms counts on raw meat”, International Journal of Food Science and Technology. 2014, 49: 928-935.
[38]	UNI EN ISO 4833-1, “Microbiology of the food chain - Horizontal method for the enumeration of microorganisms - Colony count at 30°C by the pour plate technique”, International Organization for Standardization, Geneve, Switzerland, 2013.
[39]	ISO 16649-2, “Microbiology of food and animal feeding stuffs - Horizontal method for the enumeration of beta-glucuronidase-positive Escherichia coli Colony-count technique at 44 degrees C using 5-bromo-4-chloro-3-indolyl beta-D-glucuronide”, International Organization for Standardization, Geneva, Switzerland, 2001.
[40]	ISO 21527-2, “Microbiology of food and animal feeding stuffs -Horizontal method for the enumeration of yeasts and moulds Colony count technique in products with water activity less than or equal to 0,95”, International Organization for Standardization, Geneva, Switzerland, 2008.
[41]	ISO 13720, “Meat and meat products – Enumeration of presumptive Pseudomonas spp.”, International Organization for Standardization, Geneva, Switzerland, 2010.
[42]	UNI EN ISO 6888-1, “Microbiology of food and animal feeding stuffs - Horizontal method for the enumeration of coagulase-positive staphylococci (Staphylococcus aureus and other species) - Part 1: Technique using Baird-Parker agar medium”, International Organization for Standardization, Geneve, Switzerland, 2004.
[43]	ISO 6579-1, “Microbiology of the food chain -Horizontal method for the detection, enumeration and serotyping of Salmonella. Part 1: Detection of Salmonella spp.”, International Organization for Standardization, Geneva, Switzerland, 2017.
[44]	UNI EN ISO 11290-1, “Microbiology of the food chain - Horizontal method for the detection and enumeration of Listeria monocytogenes and of Listeria spp. - Part 1: Detection method”, International Organization for Standardization, Geneve, Switzerland, 2005.
[45]	ISO 15213, “Microbiology of food and animal feeding stuffs - Horizontal method for the enumeration of sulfite-reducing bacteria growing under anaerobic conditions”, International Organization for Standardization, Geneva, Switzerland, 2003.
[46]	European Commission, “Commission Regulation No 1441 amending Regulation (EC) No 2073/2005 on microbiological criteria for foodstuffs”, Official Journal of the European Communities. 2007, L322: 12-29.
[47]	Health Protection Agency, “Guidelines for Assessing the Microbiological Safety of Ready-to-Eat Foods”, 2009. Online. Available: http://webarchive.nationalarchives.gov.uk/20140714111812/http:// www.hpa.org.uk/webc/HPAwebFile/HPAweb_C/1259151921557 Accessed 08 April 2019.
[48]	Ce. I. R. S. A., Centro Interdipartimentale di Ricerca e documentazione sulla Sicurezza Alimentare, “Linee Guida per l'analisi del rischio nel campo della microbiologia degli alimenti”, 2013. Online. Available: http://www.ceirsa.org/docum/allegato_punto4.pdf Accessed 08 April 2019
[49]	Abadias, M., Usall, J., Anguera, M., Solsona, C. and Viñas, I., “Microbiological quality of fresh, minimally-processed fruit and vegetables, and sprouts from retail establishments”, International Journal of Food Microbiology. 2008, 123: 121-129.
[50]	Caponigro, V., Ventura, M., Chiancone, I., Amato, L., Parente, E. and Piro, F., “Variation of microbial load and visual quality of ready-to-eat salads by vegetable type, season, processor and retailer”, Food Microbiology. 2010, 27(8): 1071-1077.
[51]	De Giusti, M., Aurigemma, C., Marinelli, L., Tufi, D., De Medici, D., Di Pasquale, S., De Vito, C. and Boccia, A., “The evaluation of the microbial safety of fresh ready-to-eat vegetables produced by different technologies in Italy”, Journal of Applied Microbiology. 2010, 109(3): 996-1006.
[52]	Gómez-López, V.M., Marín, A., Medina-Martínez, M.S., Gil, M.I. and Allende, A., “Generation of trihalomethanes with chlorine-based sanitizers and impact on microbial, nutritional and sensory quality of baby spinach”, Postharvest Biology and Technology. 2013, 85: 210-217.
[53]	Losio, M.N., Pavoni, E., Bilei, S., Bertasi, B., Bovec, D., Capuano, F., Farneti, S., Blasi, G., Comin, D., Cardamone, C., Decastelli, L., Delibato, E., De Santis, P., Di Pasquale, S., Gattuso, A., Goffredo, E., Fadda, A., Pisanu, M. and De Medici, D., “Microbiological survey of raw and ready-to-eat leafy green vegetables marketed in Italy”, International Journal of Food Microbiology. 2015, 210: 88-91.
[54]	Weng, S.C., Luo, Y., Lib, J., Zhou, B., Jacangelo, J.G. and Schwab, K.J., “Assessment and speciation of chlorine demand in fresh-cut produce wash water”, Food Control. 2016, 60: 543-551.
[55]	Reynolds, K.A., Mena, K.D. and Gerba, C.P., “Risk of waterborne illness via drinking water in the United States”, Reviews of Environmental Contamination and Toxicology. 2008, 192: 117-158.
[56]	Owoseni, M.C., Olaniran, A.O. and Okoh, A.I., “Chlorine Tolerance and Inactivation of Escherichia coli recovered from Wastewater Treatment Plants in the Eastern Cape, South Africa”, Applied Sciences. 2017, 7(8): 810.
[57]	Ignat, A., Manzocco, L., Maifreni, M. and Nicoli, M.C., “Decontamination efficacy of neutral and acidic electrolyzed water in fresh-cut salad washing journal of food processing and preservation”, Journal of Food Processing and Preservation. 2016, 40(5): 874-881
[58]	Jevsnik, M., Hlebec, V. and Raspor, P., “Consumers’ awareness of food safety from shopping to eating”, Food Control. 2008, 19(8): 737-745.
[59]	Pérez-Rodríguez, F., Castro, R., Posada-Izquierdo, G.D., Valero, A., Carrasco, E., García-Gimeno, R.M. and Zurera, G., “Evaluation of hygiene practices and microbiological quality of cooked meat products during slicing and handling at retail”, Meat Science. 2010, 86(2): 479-485.
[60]	Oliveira, M., Usall, J., Viñas, I., Anguera, M., Gatius, F. and Abadias, M., “Microbiological quality of fresh lettuce from organic and conventional production”, Food Microbiology. 2010, 27(5): 679-684.
[61]	Warriner, K., Huber, A., Namvar, A., Fan, W. and Dunfield, K., “Recent advances in the microbial safety of fresh fruits and vegetables”, Advances in Food and Nutrition Research. 2009, 57: 155-208.
[62]	Silva, S.R.P., Verdin, S.E.F., Pereira, D.C., Schatkoski, A.M., Rott, M.B. and Corcao, G., “Microbiological quality of minimally processed vegetables sold in Porto Alegre, Brazil”, Brazilian Journal of Microbiology. 2007, 38(4): 594-598.