Hurdle enhancement of acidic electrolyzed water antimicrobial efficacy on Bacillus cereus spores using ultrasonication

Applied Microbiology and Biotechnology

Volumn 104, Issue 10, 2020, Pages 4505-4513

  Lv, Ruiling ^a   Muhammad, Aliyu Idris ^a,b   Zou, Mingming ^a   Yu, Yue ^a   Fan, Lihua ^a   Zhou, Jianwei ^a,c   Ding, Tian ^a   Ye, Xingqian ^a   Guo, Mingming ^a   Liu, Donghong ^a,c  

^a ZHEJIANG UNIVERSITY   (China)

^b BAYERO UNIVERSITY   (Nigeria)

^c ZHEJIANG UNIVERSITY   (China)

Author keywords

Acidic electrolyzed water; Bacillus cereus spores; Synergistic inactivation; Ultrasound

Indexed keywords

BACTERIOLOGY; ENVIRONMENTAL TECHNOLOGY; TRANSMISSION ELECTRON MICROSCOPY; ULTRASONICS;

ACIDIC ELECTROLYZED WATERS; BACILLUS CEREUS SPORES; ENVIRONMENTAL REMEDIATION; INACTIVATION EFFECT; SCANNING AND TRANSMISSION ELECTRON MICROSCOPY; SYNERGISTIC INACTIVATION; ULTRASONIC TREATMENTS; ULTRASTRUCTURAL CHANGES;

BACILLUS CEREUS;

ACIDIC ELECTROLYZED WATER; ANTIBIOTIC AGENT; DISINFECTANT AGENT; FLUORESCENT DYE; OXIDIZING AGENT; SYTO 16 DYE; UNCLASSIFIED DRUG; ACID; ANTIINFECTIVE AGENT; WATER;

ANTIMICROBIAL ACTIVITY; BACTERIUM; ELECTRON DENSITY; FOOD INDUSTRY; HETEROGENEITY; HYDROLYSIS; REDUCTION; SPORE; ULTRASONICS;

ANTIBACTERIAL ACTIVITY; ARTICLE; BACILLUS CEREUS; BACTERIAL MEMBRANE; BACTERIAL SPORE; BACTERIAL SURVIVAL; BACTERIUM ADHERENCE; CELL ULTRASTRUCTURE; COLONY FORMING UNIT; COMPARATIVE STUDY; CONTROLLED STUDY; DECONTAMINATION; DENSITY; DISINFECTION; DRUG EFFICACY; DRUG MECHANISM; ELECTRON; EVALUATION STUDY; FLOW CYTOMETRY; HYDROLYSIS; INNER MEMBRANE; NONHUMAN; PROPIDIUM IODIDE ASSAY; SCANNING ELECTRON MICROSCOPY; SYNERGISTIC EFFECT; TRANSMISSION ELECTRON MICROSCOPY; ULTRASOUND; CHEMISTRY; DRUG EFFECT; ELECTROLYSIS; FOOD INDUSTRY; MICROBIAL VIABILITY; PH; PROCEDURES;

BACILLUS CEREUS;

ACIDS; ANTI-BACTERIAL AGENTS; BACILLUS CEREUS; DISINFECTANTS; ELECTROLYSIS; FOOD INDUSTRY; HYDROGEN-ION CONCENTRATION; MICROBIAL VIABILITY; SPORES, BACTERIAL; ULTRASONIC WAVES; WATER;

EID: 85082958035     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-020-10393-6     Document Type: Article

References (42)

1. Ansari JA, Ismail M, Farid M (2017) Investigation of the use of ultrasonication followed by heat for spore inactivation. Food Bioprod Process 104:32–39. 10.1016/j.fbp.2017.04.005
2. Begley M, Hill C (2015) Stress Adaptation in Foodborne Pathogens. Annu Rev Food Sci Technol 6(1):191–210
3. Black EP, Setlow P, Hocking AD, Stewart CM, Kelly AL, Hoover DG (2007) Response of spores to high-pressure processing. Compr Rev Food Sci Food Saf 6(4):103–119. 10.1111/j.1541-4337.2007.00021.x
4. Cao W, Zhu ZW, Shi ZX, Wang CY, Li BM (2009) Efficiency of slightly acidic electrolyzed water for inactivation of Salmonella enteritidis and its contaminated shell eggs. Int J Food Microbiol 130(2):88–93. 10.1016/j.ijfoodmicro.2008.12.021
5. Chemat F, Zill H, Khan MK (2011) Applications of ultrasound in food technology: processing, preservation and extraction. Ultrason Sonochem 18(4):813–835. 10.1016/j.ultsonch.2010.11.023
6. Chowdhury P, Viraraghavan T (2009) Sonochemical degradation of chlorinated organic compounds, phenolic compounds and organic dyes - a review. Sci Total Environ 407(8):2474–2492. 10.1016/j.scitotenv.2008.12.031
7. Ding T, Ge Z, Shi J, Xu YT, Jones CL, Liu DH (2015) Impact of slightly acidic electrolyzed water (SAEW) and ultrasound on microbial loads and quality of fresh fruits. LWT Food Sci Technol 60(2):1195–1199. 10.1016/j.lwt.2014.09.012
8. Driks A (2003) The dynamic spore. PNAS 100(6):3007–3009. 10.1073/pnas.0730807100
9. Du SP, Zhang ZH, Xiao LL, Lou Y, Pan YJ, Zhao Y (2016) Acidic electrolyzed water as a novel transmitting medium for high hydrostatic pressure reduction of bacterial loads on shelled fresh shrimp. Front Microbiol:7. 10.3389/fmicb.2016.00305
10. Evelyn, Silva FVM (2015a) Use of power ultrasound to enhance the thermal inactivation of Clostridium perfringens spores in beef slurry. Int J Food Microbiol 206:17–23. 10.1016/j.ijfoodmicro.2015.04.013
11. Evelyn E, Silva FVM (2015b) Thermosonication versus thermal processing of skim milk and beef slurry: modeling the inactivation kinetics of psychrotrophic Bacillus cereus spores. Food Res Int 67:67–74. 10.1016/j.foodres.2014.10.028
12. Evelyn, Silva FVM (2016) High pressure processing pretreatment enhanced the thermosonication inactivation of Alicyclobacillus acidoterrestris spores in orange juice. Food Control 62:365–372. 10.1016/j.foodcont.2015.11.007
13. Evelyn, Silva FVM (2018) Differences in the resistance of microbial spores to thermosonication, high pressure thermal processing and thermal treatment alone. J Food Eng 222:292–297. 10.1016/j.jfoodeng.2017.11.037
14. Forghani F, Oh DH (2013) 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(1):40–45. 10.1016/j.fm.2013.04.002
15. Gopal N, Hill C, Ross PR, Beresford TP, Fenelon MA, Cotter PD (2015) The prevalence and control of Bacillus and related spore-forming bacteria in the dairy industry. Front Microbiol 6(1418). 10.3389/fmicb.2015.01418
16. Han D, Hung YC, Bratcher CL, Monu EA, Wang YF, Wang LX (2018) Formation of sublethally injured Yersinia enterocolitica, Escherichia coli O157:H7, and Salmonella enterica Serovar Enteritidis cells after neutral electrolyzed oxidizing water treatments. Appl Environ Microbiol 84(17). 10.1128/aem.01066-18
17. Harimawan A, Zhong SP, Lim CT, Ting YP (2013) Adhesion of B. subtilis spores and vegetative cells onto stainless steel - DLVO theories and AFM spectroscopy. J Colloid Interface Sci 405:233–241. 10.1016/j.jcis.2013.05.031
18. Henriques AO, Moran CP (2007) Structure, assembly, and function of the spore surface layers. Annu Rev Microbiol 61:555–588
19. Jose J, de Andrade NJ, Ramos AM, Vanetti MCD, Stringheta PC, Chaves JBP (2014) Decontamination by ultrasound application in fresh fruits and vegetables. Food Control 45:36–50. 10.1016/j.foodcont.2014.04.015
20. Kentish S, Feng H (2014) Applications of Power Ultrasound in Food Processing. Annu Rev Food Sci Technol 5(1):263–284
21. Khanal SN, Anand S, Muthukumarappan K (2014) Evaluation of high-intensity ultrasonication for the inactivation of endospores of 3 bacillus species in nonfat milk. J Dairy Sci 97(10):5952–5963. 10.3168/jds.2014-7950
22. Li J, Ding T, Liao XY, Chen SG, Ye XQ, Liu DH (2017) Synergetic effects of ultrasound and slightly acidic electrolyzed water against Staphylococcus aureus evaluated by flow cytometry and electron microscopy. Ultrason Sonochem 38:711–719. 10.1016/j.ultsonch.2016.08.029
23. Lv R, Mingming Z, Chen W, Wang D, Zhou J, Ding T, Ye X, Liu D (2019a) A hurdle approach of acidic electrolyzed water simultaneous with ultrasound to inactivate Bacillus cereus. J Food Process Preserv 43(10):e14148. 10.1111/jfpp.14148
24. Lv R, Zou M, Chantapakul T, Chen W, Muhammad AI, Zhou J, Ding T, Ye X, Liu D (2019b) Effect of ultrasonication and thermal and pressure treatments, individually and combined, on inactivation of Bacillus cereus spores. Appl Microbiol Biotechnol 1. 10.1007/s00253-018-9559-3
25. Lv R, Zou M, Chen W, Zhou J, Ding T, Ye X, Liu D (2019c) Ultrasound: enhance the detachment of exosporium and decrease the hydrophobicity of Bacillus cereus spores. LWT Food Sci Technol 108473. 10.1016/j.lwt.2019.108473
26. Mathys A, Chapman B, Bull M, Heinz V, Knorr D (2007) Flow cytometric assessment of Bacillus spore response to high pressure and heat. Innovative Food Sci Emerg Technol 8(4):519–527. 10.1016/j.ifset.2007.06.010
27. Ngnitcho PFK, Tango CN, Khan I, Daliri EBM, Chellian R, Oh DH (2018) The applicability of Weibull model for the kinetics inactivation of Listeria monocytogenes and Escherichia coli O157: H7 on soybean sprouts submitted to chemical sanitizers in combination with ultrasound at mild temperatures. LWT Food Sci Technol 91:573–579. 10.1016/j.lwt.2018.01.073
28. Palacios P, Burgos J, Hoz L, Sanz B, Ordóñez JA (1991) Study of substances released by ultrasonic treatment from Bacillus stearothermophilus spores. J Appl Bacteriol 71(5):445–451. 10.1111/j.1365-2672.1991.tb03815.x
29. Reineke K, Mathys A, Heinz V, Knorr D (2013a) Mechanisms of endospore inactivation under high pressure. Trends Microbiol 21(6):296–304. 10.1016/j.tim.2013.03.001
30. Reineke K, Schlumbach K, Baier D, Mathys A, Knorr D (2013b) The release of dipicolinic acid - the rate-limiting step of Bacillus endospore inactivation during the high pressure thermal sterilization process. Int J Food Microbiol 162(1):55–63. 10.1016/j.ijfoodmicro.2012.12.010
31. Ribeiro MC, Fernandes MD, Kuaye AY, Jimenez-Flores R, Gigante M (2017) Preconditioning of the stainless steel surface affects the adhesion of Bacillus cereus spores. Int Dairy J 66:108–114. 10.1016/j.idairyj.2016.11.015
32. Rood L, Koutoulis A, Bowman JP, Evans DE, Stanley RA, Kaur M (2018) Control of microbes on barley grains using peroxyacetic acid and electrolysed water as antimicrobial agents. Food Microbiol 76:103–109. 10.1016/j.fm.2018.05.002
33. Soni A, Oey I, Silcock P, Bremer P (2016) Bacillus spores in the food industry: a review on resistance and response to novel inactivation technologies. Compr Rev Food Sci Food Saf 15(6):1139–1148. 10.1111/1541-4337.12231
34. Tremarin A, Brandao TRS, Silva CLM (2017) Application of ultraviolet radiation and ultrasound treatments for Alicyclobacillus acidoterrestris spores inactivation in apple juice. LWT Food Sci Technol 78:138–142. 10.1016/j.lwt.2016.12.039
35. Tseng S, Abramzon N, Jackson JO, Lin WJ (2012) Gas discharge plasmas are effective in inactivating Bacillus and Clostridium spores. Appl Microbiol Biotechnol 93(6):2563–2570. 10.1007/s00253-011-3661-0
36. Wang LP, Xia Q, Li YF (2017a) The effects of high pressure processing and slightly acidic electrolysed water on the structure of Bacillus cereus spores. Food Control 79:94–100. 10.1016/j.foodcont.2017.03.036
37. Wang LP, Xia Q, Li YF (2017b) Synergistic effects of high pressure processing and slightly acidic electrolysed water on the inactivation of Bacillus cereus spores. Int J Food Sci Technol 52(11):2429–2435. 10.1111/ijfs.13527
38. Wells-Bennik MHJ, Eijlander RT, den Besten HMW, Berendsen EM, Warda AK, Krawczyk AO, Groot MNN, Xiao YH, Zwietering MH, Kuipers OP, Abee T (2016) Bacterial Spores in Food: Survival, Emergence, and Outgrowth. Annu Rev Food Sci Technol 7(1):457–482
39. Westphal AJ, Price PB, Leighton TJ, Wheeler KE (2003) Kinetics of size changes of individual Bacillus thuringiensis spores in response to changes in relative humidity. PNAS 100(6):3461–3466. 10.1073/pnas.232710999
40. Xuan XT, Fan YF, Ling JG, Hu YQ, Liu DH, Chen SG, Ye XQ, Ding T (2017) Preservation of squid by slightly acidic electrolyzed water ice. Food Control 73:1483–1489. 10.1016/j.foodcont.2016.11.013
41. Zhang Z, Jiang B, Liao X, Yi J, Hu X, Zhang Y (2012) Inactivation of Bacillus subtilis spores by combining high-pressure thermal sterilization and ethanol. Int J Food Microbiol 160(2):99–104. 10.1016/j.ijfoodmicro.2012.10.009
42. Zhang CL, Li BM, Jadeja R, Hung YC (2016) Effects of electrolyzed oxidizing water on inactivation of Bacillus subtilis and Bacillus cereus spores in suspension and on carriers. J Food Sci 81(1):M144–M149. 10.1111/1750-3841.13169