Assessment of the microbial quality of ready-to-eat vegetable salads and berry fruit available on Polish market
Beata Kowalska
Department of Microbiology and Rhizosphere, The National Institute of Horticultural Research, Konstytucji 3 Maja 1/3, 96-100 Skierniewice, Polandhttps://orcid.org/0000-0001-7067-3233
Magdalena Szczech
Department of Microbiology and Rhizosphere, The National Institute of Horticultural Research, Konstytucji 3 Maja 1/3, 96-100 Skierniewice, Polandhttps://orcid.org/0000-0001-8408-6937
Abstract
The consumption and sale of ready-to-eat products, i.e., fresh-cut vegetable salads and fruit, have been growing tremendously in the present time. Therefore, the microbial safety of such products is of great concern. In the current study, a survey of general microbiological contamination (mesophilic bacteria, yeasts, molds, Enterobacteriaceae, coli bacteria, Enterococcus, Lactobacillus, and Escherichia coli) of fresh-cut vegetable salads and berry-packed fruits available in Polish supermarket was undertaken.
In ready-to-eat salads, the high number of mesophilic bacteria ranged from 6.43 to 8.56 log10 cfu g–1, and also Enterobacteriaceae with mean value from 3.45 to 4.08 log10 cfu g–1 was detected. Mesophilic bacteria, yeast, and Enterobacteriaceae were detected in all salad samples. The molds were detected in 45% of salad samples, and their mean number ranged from 0.63 log10 cfu g–1 in salads with carrot or beetroot to 1.80 log10 cfu g–1 in salads with rocket.
Berry fruit was also heavily microbiologically contaminated. In particular, the means of mesophilic bacteria, molds, and yeasts were high. The number of molds detected in fruit samples, especially in raspberry samples, could be alarming. Enterobacteriaceae, Enterococcus, and coli bacteria were detected in a few samples of berry fruit. None of the ready-to-eat salads and fruit samples were contaminated by Escherichia coli.
Based on the tests that were conducted, it was found that the microbiological quality was not satisfactory. The findings suggest that following hygienic measures during processing and handling, the microbiological quality of vegetable salads and berry fruit available in Polish markets should be improved.
Keywords:
food safety, microbiological safety, microbiological contamination, bacteria, fungi, mold, ready-to-eatReferences
Agriopoulou, S., Stamatelopoulou, E., Sachadyn-Król, M., Varzakas, T. (2020). Lactic acid bacteria as antibacterial agents to extend the helf life of fresh and minimally processed fruits and vegetables: quality and safety aspects. Microorganisms 8(6), 952. https://doi.org/10.3390/microorganisms8060952 DOI: https://doi.org/10.3390/microorganisms8060952
Alegbeleye, O., Alegbeleye, I., Oroyinka, M.O., Daramola, O.B., Ajibola, A.B., Alegbeleye, W.O., Adetunji, A.T., Afolabi, W.A., Oyedeji, O., Awe, A., Badmus, A., Oyeboade, J.T. (2023). Microbiological quality of ready to eat coleslaw marketed in Ibadan, Oyo-State, Nigeria. Int. J. Food Prop. 26(1), 666–682. https://doi.org/10.1080/10942912.2023.2173775 DOI: https://doi.org/10.1080/10942912.2023.2173775
Alegbeleye, O.O., Odeyemi, O.A., Strateva, M., Stratev, D. (2022). Microbial spoilage of vegetables, fruits and cereals. Appl. Food Res. 2(1), 100122. https://doi.org/10.1016/j.afres.2022.100122 DOI: https://doi.org/10.1016/j.afres.2022.100122
Alegbeleye, O.O., Singleton, I., Sant’Ana, A.S. (2018). Sources and contamination routes of microbial pathogens to fresh produce during field cultivation: a review. Food Microbiol. 73, 177–208. https://doi.org/10.1016/j.fm.2018.01.003 DOI: https://doi.org/10.1016/j.fm.2018.01.003
Al-Musawi, A.T., Abu-Almaaly, R.A., Kereem, H.S. (2023). Fecal coliform bacteria in vegetable salads prepared in Baghdad restaurants. J. Pure Appl. Microbiol., 17(2), 1214–1220. https://doi.org/10.22207/JPAM.17.2.51 DOI: https://doi.org/10.22207/JPAM.17.2.51
Arienzo, A., Murgia, L., Fraudentali, I., Gallo, V., Angelini, R., Antonini, G. (2020). Microbial quality of ready-toeat leafy green salads during shelf-life and home-refrigeration. Foods 9(10), 1421. https://doi.org/10.3390/foods9101421 DOI: https://doi.org/10.3390/foods9101421
Balali, G.I., Yar, D.D., Dela, V.G.A., Adjei-Kusi, P. (2020). Microbial contamination, an increasing threat to the consumption of fresh fruits and vegetables in today’s world. Intern. J. Microbiol. 2020, 3029295. https://doi.org/10.1155/2020/3029295 DOI: https://doi.org/10.1155/2020/3029295
Berthold-Pluta, A., Garbowska, M., Stefańska, I., Pluta, A. (2017). Microbiological quality of selected ready-to-eat leaf vegetables, sprouts and non-pasteurized fresh fruit-vegetable juices including the presence of Cronobacter spp. Food Microbiol. 65, 221–230. https://doi.org/10.1016/j.fm.2017.03.005 DOI: https://doi.org/10.1016/j.fm.2017.03.005
Bhullar, M., Perry, B., Monge, A., Nabwiire, L., Shaw, A. (2021). Escherichia coli survival on strawberries and unpacked romaine lettuce washed using contaminated water. Foods 10(6), 1390. https://doi.org/10.3390/foods10061390 DOI: https://doi.org/10.3390/foods10061390
Bi, K., Liang, Y., Mengiste, T., Sharon, A. (2023). Killing softly: a roadmap of Botrytis cinerea pathogenicity. Trends Plant Sci. 28(2), 211–222. https://doi.org/10.1016/j.tplants.2022.08.024 DOI: https://doi.org/10.1016/j.tplants.2022.08.024
Caponigro, V., Ventura, M., Chiancone, I., Amato, L., Parente, E., Piro, F. (2010). Variation of microbial load and visual quality of ready-to-eat salads by vegetable type, season, processor and retailer. Food Microbiol. 27(8), 1071–1077. https://doi.org/10.1016/j.fm.2010.07.011 DOI: https://doi.org/10.1016/j.fm.2010.07.011
Commission Regulation (2005). Commission Regulation (EC) No 2073/2005 of November 2005 on Microbiological Criteria for Foodstuffs. Available: https://eur-lex.europa.eu/legal-content/EN/TXT/PDF/?uri=CELEX:02005R2073-20140601&from=DA [date of access: 2.12.2021].
Commission Regulation (2007). Commission Regulation (EC) No 1441/2007 of 5 December 2007 Amending Regulation (EC) No 2073/2005 on Microbiological Criteria Foodstuffs. Available: https://eur-lex.europa.eu/LexUriServ/LexUriServ.do?uri=OJ:L:2007:322:0012:0029:EN:PDF [date of access: 2.12.2021].
Dugan, F.M. (2006). The identification of fungi. An illustrated introduction with keys, glossary, and guide to literature. APS Press, USA.
EFSA (European Food Safety Authority). 2023. Annual report of the Scientific Network on Microbiological Risk Assessment. EFSA supporting publication 2023:EN-8451.Pp. 11. https://doi.org/10.2903/sp.efsa.2023.EN-8451 DOI: https://doi.org/10.2903/sp.efsa.2023.EN-8451
Finger, J.A.F.F., Santos, I.M., Silva, G.A., Bernardino, M.C., Pinto, U.M., Maffei, D.F. (2023). Minimally processed vegetables in Brazil: an overview of marketing, processing, and microbiological aspects. Foods 12(11), 2259. https://doi.org/10.3390/foods12112259 DOI: https://doi.org/10.3390/foods12112259
FAO/WHO (2003). Code of hygienic practice for fresh fruits and vegetables. CXC 53-2003. Codex Aliment.
Habib, I., Al-Rifai, R.H., Mohamed, M.I., Ghazawi, A., Abdalla, A., Lakshmi, G., Agamy, N., Khan, M. (2023). Contamination level and phenotypic and genomic characterization of antimicrobial resistance in Escherichia coli isolated from fresh salad vegetables in the United Arab Emirates. Trop. Med. Infect. Dis. 8(6), 294. https://doi.org/10.3390/tropicalmed8060294 DOI: https://doi.org/10.3390/tropicalmed8060294
Hua, L., Yong, C., Zhanquan, Z., Boqiang, L., Guozheng, Q., Shiping, T. (2018). Pathogenic mechanisms and control strategies of Botrytis cinerea causing post-harvest decay in fruits and vegetables. Food Qual. Saf. 2(3), 111–119. https://doi.org/10.1093/fqsafe/fyy016 DOI: https://doi.org/10.1093/fqsafe/fyy016
Ibrahim, S.A., Ayivi, R.D., Zimmerman, T., Siddiqui, S.A., Altemimi, A.B., Fidan, H., Esatbeyoglu, T., Bakhshayesh, R.V. (2021). Lactic acid bacteria as antimicrobial agents: food safety and microbial food spoilage prevention. Foods 10(12), 3131. https://doi.org/10.3390/foods10123131 DOI: https://doi.org/10.3390/foods10123131
Kłapeć, T., Wójcik-Fatla, A., Farian, E., Kowalczyk, K., Cholewa, G., Cholewa, A., Dutkiewicz, J. (2021). Levels of filamentous fungi and selected mycotoxins in leafy and fruit vegetables and analysis of their potential health risk for consumer. Ann. Agric. Environ. Med. 28(4), 585–594. https://doi.org/10.26444/aaem/143031 DOI: https://doi.org/10.26444/aaem/143031
Kłapeć, T., Wójcik-Fatla, A., Farian, E., Kowalczyk, K., Cholewa, G., Cholewa, A., Dutkiewicz, J. (2022). Mycobiota and mycotoxins in various kinds of vegetables and fruits as potential health risk factors for consumer – summary of multiyear study. Ann. Agric. Environ. Med. 29(2), 316–320. https://doi.org/10.26444/aaem/150522 DOI: https://doi.org/10.26444/aaem/150522
Kowalska, B., (2023). Fresh vegetables and fruit as a source of Salmonella bacteria. Ann. Agric. Environ. Med., 30(1), 9–14. https://doi.org/10.26444/aaem/156765 DOI: https://doi.org/10.26444/aaem/156765
Kowalska, B., Szczech, M. (2022). Differences in microbiological quality of leafy green vegetables. Ann. Agric. Environ. Med., 29(2), 238–245. https://doi.org/10.26444/aaem/149963 DOI: https://doi.org/10.26444/aaem/149963
Kumar, S., Yadav, M., Devi, A., Uniyal, M., Kumar, V., Sehrawat, N., Singh, R. (2022). Assessment of pathogenic microorganisms associated with vegetable salads. Asian J. Biol. Life Sci., 11(1), 1–7. https://doi.org/10.5530/ajbls.2022.11.1 DOI: https://doi.org/10.5530/ajbls.2022.11.1
Luna-Guevara, J.J., Arenas-Hernandez, M.M.P., Martinez de la Peňa, C., Silva, J. L., Luna-Guevara, M.L. (2019). The role of pathogenic E. coli in fresh vegetables: behavior, contamination factors, and preventive measures. Intern. J. Microbiol., 2894328. https://doi.org/10.1155/2019/2894328 DOI: https://doi.org/10.1155/2019/2894328
Łepecka, A., Zielińska, D., Szymański, P., Buras, I., Kołożyn-Krajewska, D. (2022) Assessment of the microbial quality of ready-to-eat salads – are there any reasons for concern about public health? Int. J. Environ. Res. Public Health 19(3), 1582. https://doi.org/10.3390/ijerph19031582 DOI: https://doi.org/10.3390/ijerph19031582
Machado-Moreira, B., Richards, K., Brennan, F., Abram, F., Burgess, C.M.J. (2019). Microbial contamination of fresh produce: what, where, and how? Comp. Rev. Food Sci. Food Saf. 18(6), 1727–1750. https://doi.org/10.1111/1541-4337.12487 DOI: https://doi.org/10.1111/1541-4337.12487
Mendoza, I.C., Luna, E.O., Pozo, M.D., Vásquez, M.V., Montoya, D.C., Moran, G.C., Romero, L.G., Yépez, X., Salazar, R., Romero-Peňa, M., Leόn, J.C. (2022). Conventional and non-conventional disinfection methods to prevent microbial contamination in minimally processed fruits and vegetables. LWT 165, 113714. https://doi.org/10.1016/j.lwt.2022.113714 DOI: https://doi.org/10.1016/j.lwt.2022.113714
Mir, S.A., Shah, M.A., Mir, M.M., Dar, B.N., Greiner, R., Roohinejad, S. (2018). Microbial contamination of ready-to-eat vegetables salads in developing countries and potential solutions in the supply chain to control microbial pathogens. Food Control, 85, 235–244. https://doi.org//10.1016/j.foodcont.2017.10.006 DOI: https://doi.org/10.1016/j.foodcont.2017.10.006
Murali, A.P., Trząskowska, M., Trafialek, J. (2023). Microorganisms in organic food-issues to be addressed. Microorganisms, 11(6), 1557. https://doi.org/10.3390/microorganisms11061557 DOI: https://doi.org/10.3390/microorganisms11061557
Nousiainen, L.L., Joutsen, S., Lunden, J., Hanninen, M.L., Fredriksson-Ahomaa, M. (2016). Bacterial quality and safety of packaged fresh leafy vegetables at the retail level in Finland. Int. J. Food Microbiol., 232, 73–79. https://doi.org/10.1016/j.ijfoodmicro.2016.05.020 DOI: https://doi.org/10.1016/j.ijfoodmicro.2016.05.020
Olaimat, A.N., Holley, R.A. (2012). Factors influencing the microbial safety of fresh produce: a review. Food Microbiol., 32(1), 1–19. https://doi.org/10.1016/j.fm.2012.04.016 DOI: https://doi.org/10.1016/j.fm.2012.04.016
Ortiz-Solá, J., Viňas, I., Colás-Medá, P., Anguera, M., Abadias, M. (2020). Occurrence of selected viral and bacterial pathogens and microbiological quality of fresh and frozen strawberries sold in Spain. Int. J. Food Microbiol., 314, 108392. https://doi.org/10.1016/j.ijfoodmicro.2019.108392 DOI: https://doi.org/10.1016/j.ijfoodmicro.2019.108392
Palumbo, M., Attolico, G., Capozzi, V., Cozzolino, R., Corvino, A., de Chiara, M.L.V., Pace, B., Pelosi, S., Ricci, I., Romaniello, R., Cefola, M. (2022). Emerging postharvest technologies to enhance the shelf-life of fruit and vegetables: an overview. Foods 11(23), 3925. https://doi.org/10.3390/foods11233925 DOI: https://doi.org/10.3390/foods11233925
Raffo, A., Paoletti, F. (2022). Fresh-cut vegetables processing: environmental sustainability and food safety issues in a comprehensive perspective. Front. Sustain. Food Syst., 5, 681459. https://doi.org/10.3389/fsufs.2021.681459 DOI: https://doi.org/10.3389/fsufs.2021.681459
Sobiczewski, P., Iakimova, E.T. (2022). Plant and human pathogenic bacteria exchanging their primary host environments. J. Hortic. Res. 30(1), 11–30. https://doi.org/10.2478/johr-2022-0009 DOI: https://doi.org/10.2478/johr-2022-0009
Szczech, M., Kowalska, B., Smolińska, U., Maciorowski, R., Oskiera, M., Michalska, A. (2018). Microbial quality of organic and conventional vegetables from Polish farms. Int. J. Food Microbiol., 286, 155–161. https://doi.org/10.1016/j.ijfoodmicro.2018.08.018 DOI: https://doi.org/10.1016/j.ijfoodmicro.2018.08.018
Toe, E., Dadie, A., Dako, E., Loukou, G. (2017). Bacteriological quality and risk factors for contamination of raw mixed vegetable salads served in collective catering in Abidjan (Ivory Coast). Adv. Microbiol., 7(6), 405–419. https://doi.org/10.4236/aim.2017.76033 DOI: https://doi.org/10.4236/aim.2017.76033
Thomas, G.A., Gil, T.P., Müller, C.T., Rogers, H.J., Berger, C.N. (2024). From field to plate: how do bacterial enteric pathogens interact with ready-to-eat and vegetables, causing disease outbreaks? Food Microbiol., 117, 104389. https://doi.org/10.1016/j.fm.2023.104389 DOI: https://doi.org/10.1016/j.fm.2023.104389
Tournas, V.H., Katsoudas, E. (2005). Mould and yeast flora in fresh berries, grapes and citrus fruits. Int. J. Food Microbiol., 105(1), 11–17. https://doi.org/10.1016/j.ijfoodmicro.2005.05.002 DOI: https://doi.org/10.1016/j.ijfoodmicro.2005.05.002
Uhlig, E., Kjellström, A., Oscarsson, E., Nurminen, N., Nabila, Y., Paulsson, J., Lupan, T., Velpuri, N.S.B.P., Molin, G., Håkansson, Å. (2022). The live bacterial load and microbiota composition of prepacked “ready-to-eat” leafy greens during household conditions, with special reference to E. coli. Int. J. Food Microbiol., 377, 109786. https://doi.org/10.1016/j.ijfoodmicro.2022.109786 DOI: https://doi.org/10.1016/j.ijfoodmicro.2022.109786
Wajahat, S.S. (2023). Emerging trends and advancements in the biopreservation of fruits. J. Hortic. Res., 31(1), 1–24. https://doi.org/10.2478/johr-2023-0006 DOI: https://doi.org/10.2478/johr-2023-0006
Williamson, B., Tudzynski, B., Tudzynski, P., Van Kan, J.A.L. (2007). Botrytis cinerea: the cause of grey mould disease. Mol. Plant Pathol., 8(5), 561–580. https://doi.org/10.1111/j.1364-3703.2007.00417.x DOI: https://doi.org/10.1111/j.1364-3703.2007.00417.x
Xylia, P., Botsaris, G., Chrysargyris, A., Skandamis, P., Tzortzakis, N. (2019). Variation of microbial load and biochemical activity of ready-to-eat salads in Cyprus as affected by vegetables type, season, and producer. Food Microbiol., 83, 200–210. https://doi.org/10.1016/j.fm.2019.05.013 DOI: https://doi.org/10.1016/j.fm.2019.05.013
Xylia, P., Botsaris, G., Skandamis, P., Tzortzakis, N. (2021). Expiration date of ready-to-eat salads: effects on microbial load and biochemical attributes. Foods 10(5), 941. https://doi.org/10.3390/foods10050941 DOI: https://doi.org/10.3390/foods10050941
Younus, M.I., Sabuj, A.A.M., Haque, Z.F., Sayem, S.M., Majumder, S., Parvin, M.S. Islam, M.A., Saha, S. (2020). Microbial risk assessment of ready-to-eat mixed vegetable salads from different restaurants of Bangladesh Agricultural University campus. J. Adv. Vet. Anim. Res., 7(1), 34–41. https://doi.org/10.5455/javar.2020.g390 DOI: https://doi.org/10.5455/javar.2020.g390
Zhang, H., Yamamoto, E., Murphy, J., Locas, A. (2020). Microbiological safety of ready-to-eat fresh-cut fruits and vegetables sold on the Canadian retail market. Int. J. Food Microbiol., 335, 108855. https://doi.org/10.1016/j.ijfoodmicro.2020.108855 DOI: https://doi.org/10.1016/j.ijfoodmicro.2020.108855
Department of Microbiology and Rhizosphere, The National Institute of Horticultural Research, Konstytucji 3 Maja 1/3, 96-100 Skierniewice, Poland https://orcid.org/0000-0001-7067-3233
Department of Microbiology and Rhizosphere, The National Institute of Horticultural Research, Konstytucji 3 Maja 1/3, 96-100 Skierniewice, Poland https://orcid.org/0000-0001-8408-6937
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