Original Article
Combined treatment of ultraviolet-C and L. plantarum on Salmonella enteritidis and quality control of fresh-cut apple
An-Jun Chen,
Wei Luo,
Yun-Bo Luo,
Ben-Zhong Zhu,
An-Jun Chen
Department of Food Science and Nutritional Engineering, China Agricultural University, Beijing, 100083 China
Department of Food Science, Sichuan Agricultural University, Ya'an, 625014 China
Search for more papers by this authorWei Luo
Department of Food Science, Sichuan Agricultural University, Ya'an, 625014 China
Search for more papers by this authorYun-Bo Luo
Department of Food Science and Nutritional Engineering, China Agricultural University, Beijing, 100083 China
Search for more papers by this authorCorresponding Author
Ben-Zhong Zhu
Department of Food Science and Nutritional Engineering, China Agricultural University, Beijing, 100083 China
Correspondence Ben-Zhong Zhu, 17 Qinghua road east, Haidian District, Beijing, China. Email: [email protected]Search for more papers by this authorAn-Jun Chen,
Wei Luo,
Yun-Bo Luo,
Ben-Zhong Zhu,
An-Jun Chen
Department of Food Science and Nutritional Engineering, China Agricultural University, Beijing, 100083 China
Department of Food Science, Sichuan Agricultural University, Ya'an, 625014 China
Search for more papers by this authorWei Luo
Department of Food Science, Sichuan Agricultural University, Ya'an, 625014 China
Search for more papers by this authorYun-Bo Luo
Department of Food Science and Nutritional Engineering, China Agricultural University, Beijing, 100083 China
Search for more papers by this authorCorresponding Author
Ben-Zhong Zhu
Department of Food Science and Nutritional Engineering, China Agricultural University, Beijing, 100083 China
Correspondence Ben-Zhong Zhu, 17 Qinghua road east, Haidian District, Beijing, China. Email: [email protected]Search for more papers by this authorFunding information: National Science and Technology, China (“Twelfth Five Year” Project in Rural Areas), Grant/Award Number: 2012AA101606-03
Abstract
Outbreaks of foodborne illnesses are big problems associated with the consumption of fresh-cut fruits and vegetables. To enhance the safety of fresh-cut apples, this study combined ultraviolet (UV) irradiation and lactic acid bacteria (LAB) to eliminate and inhibit the growth of Salmonella enteritidis on fresh-cut apples. The results showed that the combination treatment of 0.96 kJ/m2 UV-C irradiation and subsequently dipping in about 5 log CFU/mL LAB suspension could reduce the population of Salmonella enteritidis by 2.67 ± 0.13 log CFU/g, which was about 2 log more reduction than distilled water treatment (the reduction was 0.36 ± 0.28 log CFU/g). During storage, Salmonella enteritidis remained stable in the combination treatment group while increased up to 5 log CFU/g in the control group. For the quality impact, the combination treatment did not decrease the color, firmness, and flavor of fresh-cut apples but slightly deteriorated the taste attributes.
Practical applications
The markets of fresh-cut fruits and vegetables have increased rapidly during recent decades. However, the rise of consumption of fresh-cut fruits and vegetables also increases outbreaks of foodborne illnesses. For the health concerns of chlorine, a commonly used disinfectant, healthier, and efficient methods should to be invented to replace the chlorine treatment. Ultraviolet (UV) light possesses high bactericidal ability and lactic acid bacteria (LAB) can inhibit the growth of other microorganisms during storage. The combination can significantly decrease and inhibit other microorganisms before and during storage. It has a promising prospect to be applied in the fresh-cut industry.
REFERENCES
- Abadias, M., Usall, J., Anguera, M., Solsona, C., & Viñas, I. (2008). Microbiological quality of fresh, minimally-processed fruit and vegetables, and sprouts from retail establishments. International Journal of Food Microbiology, 123(1), 121–129.
- Alegre, I., Abadias, M., Anguera, M., Oliveira, M., & Viñas, I. (2010). Factors affecting growth of foodborne pathogens on minimally processed apples. Food Microbiology, 27(1), 70–76.
- Alegre, I., Viñas, I., Usall, J., Anguera, M., & Abadias, M. (2011). Microbiological and physicochemical quality of fresh-cut apple enriched with the probiotic strain Lactobacillus rhamnosus GG. Food Microbiology, 28(1), 59–66.
- Allende, A., Martínez, B., Selma, V., Gil, M. I., Suárez, J. E., & Rodríguez, A. (2007). Growth and bacteriocin production by lactic acid bacteria in vegetable broth and their effectiveness at reducing Listeria monocytogenes in vitro and in fresh-cut lettuce. Food Microbiology, 24(7), 759–766.
- Allende, A., McEvoy, J. L., Luo, Y., Artes, F., & Wang, C. Y. (2006). Effectiveness of two-sided UV-C treatments in inhibiting natural microflora and extending the shelf-life of minimally processed ‘Red Oak Leaf’ lettuce. Food Microbiology, 23(3), 241–249.
- Berger, C. N., Sodha, S. V., Shaw, R. K., Griffin, P. M., Pink, D., Hand, P., & Frankel, G. (2010). Fresh fruit and vegetables as vehicles for the transmission of human pathogens. Environmental Microbiology, 12(9), 2385–2397.
-
Beuchat, L.,
Farber, J.,
Garrett, E.,
Harris, L.,
Parish, M.,
Suslow, T., &
Busta, F. (2003). Standardization of a method to determine the efficacy of sanitizers in inactivating human pathogenic microorganisms on raw fruits and vegetables1. Comprehensive Reviews in Food Science and Food Safety, 2(s1), 174–178.
10.1111/j.1541-4337.2003.tb00034.x Google Scholar
-
Bintsis, T.,
Litopoulou-Tzanetaki, E., &
Robinson, R. K. (2000). Existing and potential applications of ultraviolet light in the food industry–a critical review. Journal of the Science of Food and Agriculture, 80(6), 637–645.
10.1002/(SICI)1097-0010(20000501)80:6<637::AID-JSFA603>3.0.CO;2-1 CAS PubMed Web of Science® Google Scholar
- Cálix-Lara, T. F., Rajendran, M., Talcott, S. T., Smith, S. B., Miller, R. K., Castillo, A., … Taylor, T. M. (2014). Inhibition of Escherichia coli O157: H7 and Salmonella enterica on spinach and identification of antimicrobial substances produced by a commercial lactic acid bacteria food safety intervention. Food Microbiology, 38, 192–200.
-
Chun, H.-H.,
Kim, J.-Y., &
Song, K. B. (2010). Inactivation of foodborne pathogens in ready-to-eat salad using UV-C irradiation. Food Science and Biotechnology, 19(2), 547–551.
10.1007/s10068-010-0076-0 Google Scholar
- Da Silva Felício, M., Hald, T., Liebana, E., Allende, A., Hugas, M., Nguyen-The, C., … McLauchlin, J. (2015). Risk ranking of pathogens in ready-to-eat unprocessed foods of non-animal origin (FoNAO) in the EU: Initial evaluation using outbreak data (2007-2011). International Journal of Food Microbiology, 195, 9–19.
- Deering, A. J., Mauer, L. J., & Pruitt, R. E. (2012). Internalization of E. coli O157: H7 and Salmonella spp. in plants: A review. Food Research International, 45(2), 567–575.
- Escalona, V. H., Aguayo, E., Martínez-Hernández, G. B., & Artés, F. (2010). UV-C doses to reduce pathogen and spoilage bacterial growth in vitro and in baby spinach. Postharvest Biology and Technology, 56(3), 223–231.
- Fonseca, J. M., & Rushing, J. W. (2006). Effect of ultraviolet-C light on quality and microbial population of fresh-cut watermelon. Postharvest Biology and Technology, 40(3), 256–261.
- Gómez, P., Alzamora, S., Castro, M., & Salvatori, D. (2010). Effect of ultraviolet-C light dose on quality of cut-apple: Microorganism, color and compression behavior. Journal of Food Engineering, 98(1), 60–70.
- González-Aguilar, G. A., Villegas-Ochoa, M. A., Martínez-Téllez, M., Gardea, A., & Ayala-Zavala, J. F. (2007). Improving antioxidant capacity of fresh-cut mangoes treated with UV-C. Journal of Food Science, 72(3), S197–S202.
-
Graça, A.,
Salazar, M.,
Quintas, C., &
Nunes, C. (2013). Low dose UV-C illumination as an eco-innovative disinfection system on minimally processed apples. Postharvest Biology and Technology, 85, 1–7.
10.1016/j.postharvbio.2013.04.013 Google Scholar
- Guan, W., Fan, X., & Yan, R. (2013). Effect of combination of ultraviolet light and hydrogen peroxide on inactivation of Escherichia coli O157: H7, native microbial loads, and quality of button mushrooms. Food Control, 34(2), 554–559.
- Guerrero-Beltr, J., & Barbosa-C, G. (2004). Advantages and limitations on processing foods by UV light. Food Science and Technology International, 10(3), 137–147.
-
Harris, L.,
Farber, J.,
Beuchat, L.,
Parish, M.,
Suslow, T.,
Garrett, E., &
Busta, F. (2003). Outbreaks associated with fresh produce: Incidence, growth, and survival of pathogens in fresh and fresh-cut produce. Comprehensive Reviews in Food Science and Food Safety, 2(s1), 78–141.
10.1111/j.1541-4337.2003.tb00031.x Google Scholar
- Hassenberg, K., Huyskens-Keil, S., & Herppich, W. (2013). Impact of postharvest UV-C and ozone treatments on microbiological properties of white asparagus (Asparagus officinalis L.). Journal of Applied Botany and Food Quality, 85(2), 174.
-
Kim, Y.,
Kim, M., &
Song, K. B. (2009). Combined treatment of fumaric acid with aqueous chlorine dioxide or UV-C irradiation to inactivate Escherichia coli O157: H7, Salmonella enterica serovar typhimurium, and Listeria monocytogenes inoculated on alfalfa and clover sprouts. LWT-Food Science and Technology, 42(10), 1654–1658.
10.1016/j.lwt.2009.05.022 Google Scholar
-
Kim, Y.-H.,
Jeong, S.-G.,
Back, K.-H.,
Park, K.-H.,
Chung, M.-S., &
Kang, D.-H. (2013). Effect of various conditions on inactivation of Escherichia coli O157: H7, Salmonella typhimurium, and Listeria monocytogenes in fresh-cut lettuce using ultraviolet radiation. International Journal of Food Microbiology, 166(3), 349–355.
10.1016/j.ijfoodmicro.2013.08.010 Google Scholar
- Leverentz, B., Conway, W. S., Alavidze, Z., Janisiewicz, W. J., Fuchs, Y., Camp, M. J., … Sulakvelidze, A. (2001). Examination of bacteriophage as a biocontrol method for Salmonella on fresh-cut fruit: A model study. Journal of Food Protection, 64(8), 1116–1121.
- López-Rubira, V., Conesa, A., Allende, A., & Artés, F. (2005). Shelf life and overall quality of minimally processed pomegranate arils modified atmosphere packaged and treated with UV-C. Postharvest Biology and Technology, 37(2), 174–185.
- Luo, W., Chen, M., Chen, A., Dong, W., Hou, X., & Pu, B. (2015). Isolation of lactic acid bacteria from pao cai, a Chinese traditional fermented vegetable, with inhibitory activity against Salmonella associated with fresh-cut apple, using a modelling study. Journal of Applied Microbiology, 118(4), 998–1006.
- Mahawar, M., Singh, A., & Jalgaonkar, K. (2013). Utility of apple pomace as a substrate for various products: A review (Retraction of vol 90, pg 597, 2012). Food and Bioproducts Processing, 91(C 4), 700–700.
- Manzocco, L., Da Pieve, S., Bertolini, A., Bartolomeoli, I., Maifreni, M., Vianello, A., & Nicoli, M. C. (2011). Surface decontamination of fresh-cut apple by UV-C light exposure: Effects on structure, colour and sensory properties. Postharvest Biology and Technology, 61(2), 165–171.
- Manzocco, L., Da Pieve, S., & Maifreni, M. (2011). Impact of UV-C light on safety and quality of fresh-cut melon. Innovative Food Science & Emerging Technologies, 12(1), 13–17.
- Manzocco, L., Dri, A., & Quarta, B. (2009). Inactivation of pectic lyases by light exposure in model systems and fresh-cut apple. Innovative Food Science & Emerging Technologies, 10(4), 500–505.
- Manzocco, L., Quarta, B., & Dri, A. (2009). Polyphenoloxidase inactivation by light exposure in model systems and apple derivatives. Innovative Food Science & Emerging Technologies, 10(4), 506–511.
- Mukhopadhyay, S., Ukuku, D., Juneja, V., & Fan, X. (2014). Effects of UV-C treatment on inactivation of Salmonella enterica and Escherichia coli O157: H7 on grape tomato surface and stem scars, microbial loads, and quality. Food Control, 44, 110–117.
- Oms-Oliu, G., Rojas-Graü, M. A., Gonzalez, L. A., Varela, P., Soliva-Fortuny, R., Hernando, M. I. H., … Martín-Belloso, O. (2010). Recent approaches using chemical treatments to preserve quality of fresh-cut fruit: A review. Postharvest Biology and Technology, 57(3), 139–148.
- Painter, J. A., Hoekstra, R. M., Ayers, T., Tauxe, R. V., Braden, C. R., Angulo, F. J., & Griffin, P. M. (2013). Attribution of foodborne illnesses, hospitalizations, and deaths to food commodities by using outbreak data, United States, 1998–2008. Emerging Infectious Diseases, 19(3), 407–415.
- Pasha, I., Saeed, F., Sultan, M. T., Khan, M. R., & Rohi, M. (2014). Recent developments in minimal processing: A tool to retain nutritional quality of food. Critical Reviews in Food Science and Nutrition, 54(3), 340–351.
- Patel, J., & Sharma, M. (2010). Differences in attachment of Salmonella enterica serovars to cabbage and lettuce leaves. International Journal of Food Microbiology, 139(1), 41–47.
- Ramos, B., Miller, F., Brandão, T. R., Teixeira, P., & Silva, C. L. (2013). Fresh fruits and vegetables—An overview on applied methodologies to improve its quality and safety. Innovative Food Science & Emerging Technologies, 20, 1–15.
- Rupasinghe, H. V., Boulter-Bitzer, J., Ahn, T., & Odumeru, J. A. (2006). Vanillin inhibits pathogenic and spoilage microorganisms in vitro and aerobic microbial growth in fresh-cut apples. Food Research International, 39(5), 575–580.
- Rydlo, T., Miltz, J., & Mor, A. (2006). Eukaryotic antimicrobial peptides: Promises and premises in food safety. Journal of Food Science, 71(9), R125–R135.
- Schenk, M., Guerrero, S., & Alzamora, S. M. (2008). Response of some microorganisms to ultraviolet treatment on fresh-cut pear. Food and Bioprocess Technology, 1(4), 384–392.
- Siroli, L., Patrignani, F., Serrazanetti, D. I., Tabanelli, G., Montanari, C., Gardini, F., & Lanciotti, R. (2015). Lactic acid bacteria and natural antimicrobials to improve the safety and shelf-life of minimally processed sliced apples and lamb's lettuce. Food Microbiology, 47, 74–84.
- Sommers, C. H., Sites, J. E., & Musgrove, M. (2010). Ultraviolet light (254 nm) inactivation of pathogens on foods and stainless steel surfaces. Journal of Food Safety, 30(2), 470–479.
- Song, H.-J., Choi, D.-W., & Song, K. B. (2011). Effect of aqueous chlorine dioxide and UV-C treatment on the microbial reduction and color of cherry tomatoes. Horticulture, Environment, and Biotechnology, 52(5), 488–493.
- Syamaladevi, R. M., Lupien, S. L., Bhunia, K., Sablani, S. S., Dugan, F., Rasco, B., … Ross, C. (2014). UV-C light inactivation kinetics of Penicillium expansum on pear surfaces: Influence on physicochemical and sensory quality during storage. Postharvest Biology and Technology, 87, 27–32.
- Tejero-Sariñena, S., Barlow, J., Costabile, A., Gibson, G. R., & Rowland, I. (2012). In vitro evaluation of the antimicrobial activity of a range of probiotics against pathogens: Evidence for the effects of organic acids. Anaerobe, 18(5), 530–538.
- Toivonen, P. M., & Brummell, D. A. (2008). Biochemical bases of appearance and texture changes in fresh-cut fruit and vegetables. Postharvest Biology and Technology, 48(1), 1–14.
- Tran, L. T., Taylor, J. S., & Constabel, C. P. (2012). The polyphenol oxidase gene family in land plants: Lineage-specific duplication and expansion. BMC Genomics, 13(1), 395.
- Trias, R., Bañeras, L., Badosa, E., & Montesinos, E. (2008). Bioprotection of golden delicious apples and Iceberg lettuce against foodborne bacterial pathogens by lactic acid bacteria. International Journal of Food Microbiology, 123(1), 50–60.
- Vescovo, M., Torriani, S., Orsi, C., Macchiarolo, F., & Scolari, G. (1996). Application of antimicrobial-producing lactic acid bacteria to control pathogens in ready-to-use vegetables. Journal of Applied Bacteriology, 81(2), 113–119.
- Wang, Q., Cao, Y., Zhou, L., Jiang, C.-Z., Feng, Y., & Wei, S. (2015). Effects of postharvest curing treatment on flesh colour and phenolic metabolism in fresh-cut potato products. Food Chemistry, 169, 246–254.
