Synergetic effects of ultrasound and slightly acidic electrolyzed water against Staphylococcus aureus evaluated by flow cytometry and electron microscopy

Ultrasonics Sonochemistry

Volumn 38, Issue , 2017, Pages 711-719

  Li, Jiao ^a   Ding, Tian ^a   Liao, Xinyu ^a   Chen, Shiguo ^a   Ye, Xingqian ^a   Liu, Donghong ^a  

^a ZHEJIANG UNIVERSITY   (China)

Author keywords

Electron microscopy; Flow cytometry; Slightly acidic electrolyzed water; Staphylococcus aureus; Synergetic effects; Ultrasound

Indexed keywords

BACTERIA; ELECTRON MICROSCOPY; ELECTRONS; ENVIRONMENTAL TECHNOLOGY; FLOW CYTOMETRY; FOOD PRESERVATION; HIGH RESOLUTION TRANSMISSION ELECTRON MICROSCOPY; SCANNING ELECTRON MICROSCOPY; TRANSMISSION ELECTRON MICROSCOPY;

ENVIRONMENTAL REMEDIATION; SCANNING AND TRANSMISSION ELECTRON MICROSCOPY; SLIGHTLY ACIDIC ELECTROLYZED WATERS; STAPHYLOCOCCUS AUREUS; STERILIZATION TECHNOLOGY; SYNERGETIC EFFECT; ULTRASOUND TREATMENTS; VIABLE BUT NON-CULTURABLE;

ULTRASONICS;

WATER;

ACIDITY; ARTICLE; BACTERIAL VIABILITY; BACTERIUM CULTURE; CELL ULTRASTRUCTURE; COLONY FORMING UNIT; DISINFECTION; ELECTROLYSIS; ELECTRON MICROSCOPY; FLOW CYTOMETRY; NONHUMAN; PRIORITY JOURNAL; STAPHYLOCOCCUS AUREUS; ULTRASOUND; CHEMISTRY; CYTOLOGY; DRUG EFFECT; INSTRUMENT STERILIZATION; MICROBIAL VIABILITY; PH; PHYSIOLOGY; PROCEDURES; ULTRASTRUCTURE;

ELECTROLYSIS; FLOW CYTOMETRY; HYDROGEN-ION CONCENTRATION; MICROBIAL VIABILITY; MICROSCOPY, ELECTRON; STAPHYLOCOCCUS AUREUS; STERILIZATION; ULTRASONIC WAVES; WATER;

EID: 84994181162     PISSN: 13504177     EISSN: 18732828     Source Type: Journal    
DOI: 10.1016/j.ultsonch.2016.08.029     Document Type: Article

References (46)

1. Hennekinne, J.A., De Buyser, M.L., Dragacci, S., et al. Staphylococcus aureus and its food poisoning toxins: characterization and outbreak investigation. Fems Microbiol. Rev. 36 (2012), 815–836.
2. Que, Y.A., Moreillon, P., Infective endocarditis. Nat. Rev. Cardiol. 8 (2011), 322–336.
3. Argudin, M.A., Mendoza, M.C., Rodicio, M.R., Food poisoning and Staphylococcus aureus enterotoxins. Toxins 2 (2010), 1751–1773.
4. European Food Safety Authority, The European Union summary report on trends and sources of Zoonoses, Zoonotic agents and food-borne outbreaks in 2009. EFSA J., 9, 2011, 2090.
5. Schelin, J., et al. The formation of Staphylococcus aureus enterotoxin in food environments and advances in risk assessment. Virulence 2 (2011), 580–592.
6. Center for disease control and prevention (USA), CDC estimates of foodborne illness in the United States. http://www.cdc.gov/foodborneburden/2011-foodborne-estimates.html (accessed 29.07.16).
7. Foladori, P., Laura, B., Gianni, A., Giuliano, Z., Effects of sonication on bacteria viability in wastewater treatment plants evaluated by flow cytometry–fecal indicators, wastewater and activated sludge. Water Res. 41 (2007), 235–243.
8. Rastogi, N.K., Opportunities and challenges in application of ultrasound in food processing. Crit. Rev. Food Sci. Nutr. 51 (2011), 705–722.
9. Ashokkumar, M., The characterization of acoustic cavitation bubbles – an overview. Ultrason. Sonochem. 18 (2011), 864–872.
10. Gao, S., Lewis, G.D., Ashokkumar, M., Hemar, Y., Inactivation of microorganisms by low-frequency high-power ultrasound: 2. A simple model for the inactivation mechanism. Ultrason. Sonochem. 21 (2014), 454–460.
11. Bilek, S.E., Turantas, F., Decontamination efficiency of high power ultrasound in the fruit and vegetable industry, a review. Int. J. Food Microbiol. 166 (2013), 155–162.
12. Chandrapala, J., Oliver, C., Kentish, S., Ashokkumar, M., Ultrasonics in food processing – food quality assurance and food safety. Trends Food Sci. Tech. 26 (2012), 88–98.
13. Brilhante De Sao Jose, J.F., de Andrade, N.J., Ramos, A.M., Dantas Vanetti, M.C., Stringheta, P.C., Paes Chaves, J.B., Decontamination by ultrasound application in fresh fruits and vegetables. Food Control 45 (2014), 36–50.
14. Ananta, E., Voigt, D., Zenker, M., Heinz, V., Knorr, D., Cellular injuries upon exposure of Escherichia coli and Lactobacillus rhamnosus to high-intensity ultrasound. J. Appl. Microbiol. 99 (2005), 271–278.
15. Li, J., Ahn, J., Liu, D., Chen, S., Ye, X., Ding, T., Evaluation of ultrasound-induced damage to Escherichia coli and Staphylococcus aureus by Flow cytometry and transmission electron microscopy. Appl. Environ. Microbiol. 82 (2016), 1828–1837.
16. Gao, S., Lewis, G.D., Ashokkumar, M., Hemar, Y., Inactivation of microorganisms by low-frequency high-power ultrasound: 1. Effect of growth phase and capsule properties of the bacteria. Ultrason. Sonochem. 21 (2014), 446–453.
17. Kentish, S., Feng, H., Applications of power ultrasound in food processing. Annu. Rev. Food Sci. Technol. 5 (2014), 263–284.
18. Ayyildiz, O., Sanik, S., Ileri, B., Effect of ultrasonic pretreatment on chlorine dioxide disinfection efficiency. Ultrason. Sonochem. 18 (2011), 683–688.
19. Sango, D.M., Abela, D., McElhatton, A., Valdramidis, V.P., Assisted ultrasound applications for the production of safe foods. J. Appl. Microbiol. 116 (2014), 1067–1083.
20. Issa-Zacharia, A., Kamitani, Y., Miwa, N., Muhimbula, H., Iwasaki, K., Application of slightly acidic electrolyzed water as a potential non-thermal food sanitizer for decontamination of fresh ready-to-eat vegetables and sprouts. Food Control 22 (2011), 601–607.
21. Cao, W., Zhu, Z.W., Shi, Z.X., Wang, C.Y., Li, B.M., Efficiency of slightly acidic electrolyzed water for inactivation of Salmonella enteritidis and its contaminated shell eggs. Int. J. Food Microbiol. 130 (2009), 88–93.
22. Guentzel, J.L., Liang, L.K., Callan, M.A., Emmons, S.A., Dunham, V.L., Reduction of bacteria on spinach, lettuce, and surfaces in food service areas using neutral electrolyzed oxidizing water. Food Microbiol. 25 (2008), 36–41.
23. Ding, T., Xuan, X., Li, J., Chen, S., Liu, D., Ye, X., et al. Disinfection efficacy and mechanism of slightly acidic electrolyzed water on Staphylococcus aureus in pure culture. Food Control 60 (2016), 505–510.
24. Forghani, F., Oh, D.H., Hurdle enhancement of slightly acidic electrolyzed water antimicrobial efficacy on Chinese cabbage, lettuce, sesame leaf and spinach using ultrasonication and water wash. Food Microbiol. 36 (2013), 40–45.
25. Afari, G.K., Hung, Y., King, C.H., Hu, A., Reduction of Escherichia coli O157:H7 and Salmonella Typhimurium DT 104 on fresh produce using an automated washer with near neutral electrolyzed (NEO) water and ultrasound. Food Control 63 (2016), 246–254.
26. Aurass, P., Prager, R., Flieger, A., EHEC, EAEC O104:H4 strain linked with the, German outbreak of haemolytic uremic syndrome enters into the viable but non-culturable state in response to various stresses and resuscitates upon stress relief. Environ. Microbiol. 13:2011 (2011), 3139–3148.
27. Wang, Y., Hammes, F., De Roy, K., Verstraete, W., Boon, N., Past, present and future applications of flow cytometry in aquatic microbiology. Trends Biotechnol. 28 (2010), 416–424.
28. Vives-Rego, J., Lebaron, P., Nebe-von, G., Caron, Current and future applications of flow cytometry in aquatic microbiology. Fems Microbiol. Rev. 24 (2000), 429–448.
29. Falcioni, T., Papa, S., Gasol, J.M., Evaluating the flow-cytometric nucleic acid double-staining protocol in realistic situations of planktonic bacterial death. Appl. Environ. Microbiol. 74 (2008), 1767–1779.
30. Ayari, S., Dussault, D., Hayouni, E.A., Vu, K.D., Hamdi, M., Lacroix, M., Response of Bacillus cereus vegetative cells after exposure to repetitive sublethal radiation processing in combination with nisin. Food Microbiol. 32 (2012), 361–370.
31. Morono, Y., Terada, T., Kallmeyer, J., Inagaki, F., An improved cell separation technique for marine subsurface sediments: applications for high-throughput analysis using flow cytometry and cell sorting. Environ. Microbiol. 15 (2013), 2841–2849.
32. Davey, H.M., Hexley, P., Red but not dead? Membranes of stressed Saccharomyces cerevisiae are permeable to propidium iodide. Environ. Microbiol. 13 (2011), 163–171.
33. Xu, Y., Zhang, L., Bailina, Y., Ge, Z., Ding, T., Ye, X., et al. Effects of ultrasound and/or heating on the extraction of pectin from grapefruit peel. J. Food Eng. 126 (2014), 72–81.
34. Zhao, W., Yang, R., Shen, X., Zhang, S., Chen, X., Lethal and sublethal injury and kinetics of Escherichia coli, Listeria monocytogenes and Staphylococcus aureus in milk by pulsed electric fields. Food Control 32 (2013), 6–12.
35. Antolinos, V., Esteban, M., Ros-Chumillas, M., Huertas, J., Periago, P.M., Palop, A., et al. Assessment of the of acid shock effect on viability of Bacillus cereus and Bacillus weihenstephanensis using flow cytometry. Food Res. Int. 66 (2014), 306–312.
36. Drakopoulou, S., Terzakis, S., Fountoulakis, M.S., Mantzavinos, D., Manios, T., Ultrasound-induced inactivation of gram-negative and gram-positive bacteria in secondary treated municipal wastewater. Ultrason. Sonochem. 16 (2009), 629–634.
37. Luo, K., Oh, D.H., Inactivation kinetics of Listeria monocytogenes and Salmonella enterica serovar Typhimurium on fresh-cut bell pepper treated with slightly acidic electrolyzed water combined with ultrasound and mild heat. Food Microbiol. 53 (2016), 165–171.
38. Ding, T., Ge, Z., Shi, J., Xu, Y., Jones, C.L., Liu, D., Impact of slightly acidic electrolyzed water (SAEW) and ultrasound on microbial loads and quality of fresh fruits. LWT – Food Sci. Technol. 60 (2015), 1195–1199.
39. Forghani, F., Eskandari, M., Oh, D.H., Application of slightly acidic electrolyzed water and ultrasound for microbial decontamination of Kashk. Food Sci. Biotechnol. 24 (2015), 1011–1016.
40. Wordon, B.A., Mortimer, B., McMaster, L.D., Comparative real-time analysis of Saccharomyces cerevisiae cell viability, injury and death induced by ultrasound (20kHz) and heat for the application of hurdle technology. Food Res. Int. 47 (2012), 134–139.
41. Gogate, P.R., Kabadi, A.M., A review of applications of cavitation in biochemical engineering/biotechnology. Biochem. Eng. J. 44 (2009), 60–72.
42. Oliver, J.D., Recent findings on the viable but nonculturable state in pathogenic bacteria. Fems Microbiol. Rev. 34 (2010), 415–425.
43. Pinto, D., Santos, M.A., Chambel, L., Thirty years of viable but nonculturable state research: unsolved molecular mechanisms. Crit. Rev. Microbiol. 41 (2013), 61–76.
44. Declerck, P., Vanysacker, L., Hulsmans, A., Lambert, N., Liers, S., Ollevier, F., Evaluation of power ultrasound for disinfection of both Legionella pneumophila and its environmental host Acanthamoeba castellanii. Water Res. 44 (2010), 703–710.
45. Nan, S., Yongyu, L.I., Baoming, L.I., Wang, C., Cui, X., Cao, W., Effect of slightly acidic electrolyzed water for inactivating Escherichia coli O157:H7 and Staphylococcus aureus analyzed by transmission electron microscopy. J. Food Prot. 73 (2010), 2211–2216.
46. Piyasena, P., Mohareb, E., McKellar, R.C., Inactivation of microbes using ultrasound: a review. Int. J. Food Microbiol. 87 (2003), 207–216.