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. 2016 Dec 31;25(6):1801–1804. doi: 10.1007/s10068-016-0274-5

Effects of malic acid or/and grapefruit seed extract for the inactivation of common food pathogens on fresh-cut lettuce

Jin-Hee Kim 2, Ki-Hyun Kwon 1, Se-Wook Oh 2,✉
PMCID: PMC6049248  PMID: 30263478

Abstract

This study investigated the antimicrobial activity of malic acid (MA), grapefruit seed extract (GSE), and combined (MA+GSE) treatment against Escherichia coli O157:H7, Salmonella Typhimurium, and Listeria monocytogenes on fresh-cut lettuce. The antimicrobial effects of 1% MA and 0.5% GSE alone and in combination (1% MA+0.5% GSE) were tested on artificially inoculated lettuce during storage at 5°C for 14 days. The maximum reductions of E. coli O157:H7, S. Typhimurium, and L. monocytogenes were 4.96, 4.80, and 3.95 log CFU/g observed with MA+GSE during storage for 14 days, respectively. MA+GSE showed the greatest reduction against in E. coli O157:H7 and L. monocytogenes. These results indicate that the combined treatment was more effective than MA and GSE alone treatment. Therefore, it suggests that MA + GSE could be used as an effective intervention method for improving microbiological safety of fresh-cut lettuce.

Keywords: malic acid, grapefruit seed extract, foodborne pathogens, lettuce, reduction

References

  • 1.Xu W, Qu W, Huang K, Guo F, Yang J, Zhao H, Luo Y. Antibacterial effect of grapefruit seed extract on food-borne pathogens and its application in the preservation of minimally processed vegetables. Postharvest Biol. Tec. 2007;45:126–133. doi: 10.1016/j.postharvbio.2006.11.019. [DOI] [Google Scholar]
  • 2.Park SH, Choi MR, Park JW, Park KH, Chung MS, Ryu S, Kang DH. Use of organic acids to inactivate Escherichia coli O157: H7, Salmonella Typhimurium, and Listeria monocytogenes on organic fresh apples and lettuce. J. Food Sci. 2011;76:M293–M298. doi: 10.1111/j.1750-3841.2011.02205.x. [DOI] [PubMed] [Google Scholar]
  • 3.Beuchat LR. Ecological factors influencing survival and growth of human pathogens on raw fruits and vegetables. Microbes Infect. 2002;4:413–423. doi: 10.1016/S1286-4579(02)01555-1. [DOI] [PubMed] [Google Scholar]
  • 4.Côté C, Quessy S. Persistence of Escherichia coli and Salmonella in surface soil following application of liquid hog manure for production of pickling cucumbers. J. Food Protect. 2005;68:900–905. doi: 10.4315/0362-028X-68.5.900. [DOI] [PubMed] [Google Scholar]
  • 5.Ackers ML, Mahon BE, Leahy E, Goode B, Damrow T, Hayes PS, Bibb WF, Rice DH, Barrett TJ, Hutwagner L. An outbreak of Escherichia coli O157: H7 infections associated with leaf lettuce consumption. J. Infect. Dis. 1998;177:1588–1593. doi: 10.1086/515323. [DOI] [PubMed] [Google Scholar]
  • 6.Stine SW, Song I, Choi CY, Gerba CP. Effect of relative humidity on preharvest survival of bacterial and viral pathogens on the surface of cantaloupe, lettuce, and bell peppers. J. Food Protect. 2005;68:1352–1358. doi: 10.4315/0362-028X-68.7.1352. [DOI] [PubMed] [Google Scholar]
  • 7.Choi MR, Jeong SG, Liu Q, Ban GH, Lee SY, Park JW, Kang DH. Effect of thiamine dilaurylsulfate against Escherichia coli O157: H7, Salmonella Typhimurium, Listeria monocytogenes and Bacillus cereus spores in custard cream. LWT-Food Sci. Technol. 2015;60:320–324. doi: 10.1016/j.lwt.2014.09.040. [DOI] [Google Scholar]
  • 8.Beuchat LR. Pathogenic microorganisms associated with fresh produce. J. Food Protect. 1996;59:204–216. doi: 10.4315/0362-028X-59.2.204. [DOI] [PubMed] [Google Scholar]
  • 9.Cooley M, Carychao D, Crawford-Miksza L, Jay MT, Myers C, Rose C, Keys C, Farrar J, Mandrell RE. Incidence and tracking of Escherichia coli O157: H7 in a major produce production region in California. PLoS ONE. 2007;2:e1159. doi: 10.1371/journal.pone.0001159. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 10.Little C, Gillespie I. Prepared salads and public health. J. Appl. Microbiol. 2008;105:1729–1743. doi: 10.1111/j.1365-2672.2008.03801.x. [DOI] [PubMed] [Google Scholar]
  • 11.Sivapalasingam S, Friedman CR, Cohen L, Tauxe RV. Fresh produce: A growing cause of outbreaks of foodborne illness in the United States, 1973 through 1997. J. Food Protect. 2004;67:2342–2353. doi: 10.4315/0362-028X-67.10.2342. [DOI] [PubMed] [Google Scholar]
  • 12.Gómez-López VM, Marín A, Medina-Martínez MS, Gil MI, Allende A. Generation of trihalomethanes with chlorine-based sanitizers and impact on microbial, nutritional and sensory quality of baby spinach. Postharvest Biol. Tec. 2013;85:210–217. doi: 10.1016/j.postharvbio.2013.05.012. [DOI] [Google Scholar]
  • 13.Akbas M, Ölmez H. Inactivation of Escherichia coli and Listeria monocytogenes on iceberg lettuce by dip wash treatments with organic acids. Lett. Appl. Microbiol. 2007;44:619–624. doi: 10.1111/j.1472-765X.2007.02127.x. [DOI] [PubMed] [Google Scholar]
  • 14.Raybaudi-Massilia RM, Mosqueda-Melgar J, Martín-Belloso O. Antimicrobial activity of malic acid against Listeria monocytogenes, Salmonella Enteritidis and Escherichia coli O157: H7 in apple, pear and melon juices. Food Control. 2009;20:105–112. doi: 10.1016/j.foodcont.2008.02.009. [DOI] [Google Scholar]
  • 15.Sagong HG, Lee SY, Chang PS, Heu S, Ryu S, Choi YJ, Kang DH. Combined effect of ultrasound and organic acids to reduce Escherichia coli O157: H7, Salmonella Typhimurium, and Listeria monocytogenes on organic fresh lettuce. Int. J. Food Microbiol. 2011;145:287–292. doi: 10.1016/j.ijfoodmicro.2011.01.010. [DOI] [PubMed] [Google Scholar]
  • 16.Singla R, Ganguli A, Ghosh M. An effective combined treatment using malic acid and ozone inhibits Shigella spp. on sprouts. Food Control. 2011;22:1032–1039. doi: 10.1016/j.foodcont.2010.12.012. [DOI] [Google Scholar]
  • 17.Eswaranandam S, Hettiarachchy N, Johnson M. Antimicrobial activity of citric, lactic, malic, or tartaric acids and nisin-incorporated soy protein film against Listeria monocytogenes, Escherichia coli O157: H7, and Salmonella gaminara. J. Food Sci. 2004;69:FMS79–FMS84. [Google Scholar]
  • 18.Heggers JP, Cottingham J, Gusman J, Reagor L, McCoy L, Carino E, Cox R, Zhao J-G. The effectiveness of processed grapefruit-seed extract as an antibacterial agent: II. Mechanism of action and in vitro toxicity. J. Altern. Complem. Med. 2002;8:333–340. doi: 10.1089/10755530260128023. [DOI] [PubMed] [Google Scholar]
  • 19.Reagor L, Gusman J, McCoy L, Carino E, Heggers JP. The effectiveness of processed grapefruit-seed extract as an antibacterial agent: I. An in vitro agar assay. J. Altern. Complem. Med. 2002;8:325–332. doi: 10.1089/10755530260128014. [DOI] [PubMed] [Google Scholar]
  • 20.Saito M, Hosoyama H, Ariga T, Kataoka S, Yamaji N. Antiulcer activity of grape seed extract and procyanidins. J. Agr. Food Chem. 1998;46:1460–1464. doi: 10.1021/jf9709156. [DOI] [Google Scholar]
  • 21.Poimenidou SV, Bikouli VC, Gardeli C, Mitsi C, Tarantilis PA, Nychas G-J, Skandamis PN. Effect of single or combined chemical and natural antimicrobial interventions on Escherichia coli O157: H7, total microbiota and color of packaged spinach and lettuce. Int. J. Food Microbiol. 2016;220:6–18. doi: 10.1016/j.ijfoodmicro.2015.12.013. [DOI] [PubMed] [Google Scholar]
  • 22.Anang DM, Rusul G, Bakar J, Ling FH. Effects of lactic acid and lauricidin on the survival of Listeria monocytogenes, Salmonella enteritidis and Escherichia coli O157: H7 in chicken breast stored at 4°C. Food Control. 2007;18:961–969. doi: 10.1016/j.foodcont.2006.05.015. [DOI] [Google Scholar]
  • 23.Kim SY, Kang DH, Kim JK, Ha YG, Hwang JY, Kim T, Lee SH. Antimicrobial activity of plant extracts against Salmonella Typhimurium, Escherichia coli O157: H7, and Listeria monocytogenes on fresh lettuce. J. Food Sci. 2011;76:M41–M46. doi: 10.1111/j.1750-3841.2010.01926.x. [DOI] [PubMed] [Google Scholar]
  • 24.Ramos-Villarroel A, Martín-Belloso O, Soliva-Fortuny R. Combined effects of malic acid dip and pulsed light treatments on the inactivation of Listeria innocua and Escherichia coli on fresh-cut produce. Food Control. 2015;52:112–118. doi: 10.1016/j.foodcont.2014.12.020. [DOI] [Google Scholar]
  • 25.Lee HJ, Kim TC, Kim SJ, Park SJ. Bruising injury of persimmon (Diospyros kaki cv. Fuyu) fruits. Sci. Hortic.-Amsterdam. 2005;103:179–185. doi: 10.1016/j.scienta.2004.04.016. [DOI] [Google Scholar]
  • 26.Cvetnic Z, Vladimir-Knezevic S. Antimicrobial activity of grapefruit seed and pulp ethanolic extract. Acta Pharmaceut. 2004;54:243–250. [PubMed] [Google Scholar]
  • 27.Stratford M, Eklund T. Organic acids and esters. In: Russell NJ, Gould GW, editors. Food Preservatives. New York City, NY, USA: Springer US; 2003. pp. 48–84. [Google Scholar]
  • 28.Doores S. Organic acids. In: Branen AL, Davidson PM, editors. Antimicrobials in Foods. New York City, NY, USA: Marcel Dekker; 1993. pp. 95–136. [Google Scholar]

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