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Research article

Food Microbiology and Biotechnology

Synergistic Effect of Slightly Acidic Electrolyzed Water and Ultrasound at Mild Heat Temperature in Microbial Reduction and Shelf-Life Extension of Fresh-Cut Bell Pepper

Ke Luo 1 and Deog-Hwan Oh 1*

Department of Food Science and Biotechnology and Institute of Bioscience and Biotechnology, Kangwon National University, Chuncheon 200-701, Republic of Korea

Received: May 11, 2015; Accepted: June 1, 2015

J. Microbiol. Biotechnol. 2015; 25(9): 1502-1509

Published September 28, 2015 https://doi.org/10.4014/jmb.1505.05021

Copyright © The Korean Society for Microbiology and Biotechnology.

Abstract

The objectives of this study were to evaluate the effect of combined treatments (slightly acidic electrolyzed water (SAEW), ultrasound (US), or mild heat (60°C)) on the growth of Listeria monocytogenes and Salmonella enterica serovar Typhimurium in fresh-cut bell pepper, and the shelf-life and sensory quality (color and texture) were followed during storage at 4ºC and 25°C. An additional 0.65, 1.72, and 2.70 log CFU/g reduction was achieved by heat treatments at 60°C for 1 min for DW, SAEW, and SAEW+US, respectively. Regardless of the type of pathogen, the combined treatment (SAEW+US+60°C) achieved a significantly (p < 0.05) longer lag time in all treatment groups. This combined treatment also prolonged the shelf-life of bell pepper up to 8 days and 30 h for the storage at 4ºC and 25ºC, respectively. There was also no significant difference in the color and hardness of treated (SAEW+US+60°C) bell pepper from that of control during the storage. This new hurdle approach is thus expected to improve the microbial safety of bell peppers during storage and distribution.

Keywords

Fresh-cut bell pepper, Slightly acidic electrolyzed water, Listeria monocytogenes, Salmonella enterica serovar Typhimurium, Ultrasound

References

  1. Ajlouni S, Sibrani H, Premier R, Tomkins B. 2006. Ultrasonication and fresh produce (cos lettuce) preservation. J. Food Sci. 71:62-68.
    CrossRef
  2. Aytac SA, Ben U, Cengiz C, Mercanoglu Taban B. 2010. Evaluation of Salmonella and Listeria monocytogenes contamination on leafy green vegetables. J. Food Agric. Environ. 8: 275-279.
  3. Baranyi J, Roberts TA. 1994. A dynamic approach to predicting bacterial growth in food. Int. J. Food Microbiol. 23:277-294.
    CrossRef
  4. Behravesh CB, Jones TF, Vugia DJ, Long C, Marcus R, Smith K, et al. 2011. Deaths associated with bacterial pathogens transmitted commonly through food: Foodborne Diseases Active Surveillance Network (FoodNet), 1996-2005. J. Infect Dis. 204: 263-267.
    Pubmed CrossRef
  5. Baumann A, Martin SE, Feng H. 2005. Power ultrasound treatment of Listeria monocytogenes in apple cider. J. Food Prot. 68: 2333-2340.
    Pubmed
  6. Brilhante São José JF, Dantas Vanetti MC. 2012. Effect of ultrasound and commercial sanitizers in removing natural contaminants and Salmonella enterica Typhimurium on cherry tomatoes. Food Control 24: 95-99.
    CrossRef
  7. Cao S, Hu Z, Pang B, Wang H, Xie H, Wu F. 2010. Effect of ultrasound treatment on fruit decay and quality maintenance in strawberry after harvest. Food Control 21: 529-532.
    CrossRef
  8. 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: 88-93.
    Pubmed CrossRef
  9. Castro SM, Saraiva JA, Lopes-da-Silva JA, Delgadillo I, Loey AV, Smout C, Hendrickx M. 2008. Effect of thermal blanching and of high pressure treatments on sweet green and red bell pepper fruits (Capsicum annuum L.). Food Chem. 107: 1436-1449.
    CrossRef
  10. Crawford AE. 1963. A practical introduction to ultrasonic cleaning. Ultrasonics 1: 65-69.
    CrossRef
  11. Farber JM, Peterkin PI. 1991. Listeria monocytogenes, a foodborne pathogen. Microbiol. Rev. 55: 476-511.
    Pubmed PMC
  12. Forghani F, Rahman SME, Park MS, Park JH, Park J, Song KB, Oh DH. 2013. Ultrasonication enhanced low concentration electrolyzed water efficacy on bacteria inactivation and shelf life extension on lettuce. Food Sci. Biotechnol. 22: 131-136.
    CrossRef
  13. Forghani F, Oh DH. 2013b. 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: 40-45.
    Pubmed CrossRef
  14. Gogate PR, Kabadi AM. 2009. A review of applications of cavitation in biochemical engineering/biotechnology. Biochem. Eng. J. 44: 60-72.
    CrossRef
  15. Gómez-López VM, Devlieghere F, Ragaert P, Debevere J. 2007. Shelf-life extension of minimally processed carrots by gaseous chlorine dioxide. Int. J. Food Microbiol. 116: 221-227.
    Pubmed CrossRef
  16. Huang Y R, H ung YC, Hsu SY, Huang YW, H wang D F. 2008. Application of electrolyzed water in the food industry. Food Control 19: 329-345.
    CrossRef
  17. Jayasooriya SD, Bhandari BR, Torley P, D’Arcy BR. 2004. Effect of high power ultrasound waves on properties of meat: a review. Int. J. Food Prop. 7: 301-319.
    CrossRef
  18. Koide S, Shitanda D, Note M, Cao W. 2011. Effects of mildly heated, slightly acidic electrolyzed water on the disinfection and physicochemical properties of sliced carrot. Food Control 22: 452-456.
    CrossRef
  19. Koseki S, Yoshida K, Kamiani Y, Isobe S, Itoh K. 2004. Effect of mild heat pretreatment with alkaline electrolyzed water on the efficacy of acidic electrolyzed water against Escherichia coli O157:H7 and Salmonella on lettuce. Food Microbiol. 21: 559-566.
    CrossRef
  20. León-Félix J, Martínez-Bustillos R, Báez-Sa udo M, PerazaGaray F, Chaidez C. 2010. Norovirus contamination of bell pepper from handling during harvesting and packing. Food Environ. Virol. 2: 211-217.
    CrossRef
  21. Leverentz B, Conway WS, Camp MJ, Janisiewicz WJ, Abuladze T, Yang M, et al. 2003. Biocontrol of Listeria monocytogenes on fresh-cut produce by treatment with lytic bacteriophages and a bacteriocin. Appl. Environ. Microbiol. 69: 4519-4526.
    Pubmed PMC CrossRef
  22. Mañas P, Pagán R, Raso J. 2000. Predicting lethal effect of ultrasonic waves under pressure treatments on Listeria monocytogenes ATCC 15313 by power measurements. J. Food Sci. 65: 663-667.
    CrossRef
  23. Mansur AR, Tango CN, Kim GH, Oh DH. 2015. Combined effects of slightly acidic electrolyzed water and fumaric acid on the reduction of foodborne pathogens and shelf life extension of fresh pork. Food Control 47: 277-284.
    CrossRef
  24. McEvoy JL, Luo Y, Conway W, Zhou B, Feng H. 2009. Potential of Escherichia coli O157:H7 to grow on field-cored lettuce as impacted by postharvest storage time and temperature. Int. J. Food Microbiol. 128: 506-509.
    Pubmed CrossRef
  25. Nan S, Li Y, Li B, Wang C, Cui X, Cao W. 2010. Effect of slightly acidic electrolyzed water for inactivating Escherichia coli O157:H7 and Staphylococcus aureus analyzed by transmission electron microscopy. J. Food Prot. 73: 2211-2216.
    Pubmed
  26. Rahman SM, Jin YG, Oh DH. 2011. Combination treatment of alkaline electrolyzed water and citric acid with mild heat to ensure microbial safety, shelf-life and sensory quality of shredded carrots. Food Microbiol. 28: 484-491.
    Pubmed CrossRef
  27. Sagong HG, Lee SY, Chang PS, Heu S, Ryu S, Choi YJ, Kang DH. 2011. 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. 145: 287-292.
    Pubmed CrossRef
  28. Sant’Ana AS, Franco BDGM, Schaffner DW. 2012. Modeling the growth rate and lag time of different strains of Salmonella enterica and Listeria monocytogenes in ready-to-eat lettuce. Food Microbiol. 30: 267-273.
    Pubmed CrossRef
  29. São J osé JFB, Andrade N J, Ramos A M, V anetti M CD , Stringheta PC, Chaves JBP. 2014. Decontamination by ultrasound application in fresh fruits and vegetables. Food Control 45: 36-50.
  30. São José JFB, Medeiros HS, Bernardes PC, Andrade NJ. 2014. Removal of Salmonella enterica Enteritidis and Escherichia coli from green peppers and melons by ultrasound and organic acids. Int. J. Food Microbiol. 190: 9-13.
    Pubmed CrossRef
  31. Scouten AJ, Beuchat LR. 2002. Combined effects of chemical, heat and ultrasound treatments to kill Salmonella and Escherichia coli O157:H7 on alfalfa seeds. J. Appl. Microbiol. 92: 668-674.
    Pubmed CrossRef
  32. Seymour IJ, Burfoot D, Smith RL, Cox LA, Lockwood A. 2002. Ultrasound decontamination of minimally processed fruits and vegetables. Int. J. Food Sci. Technol. 37: 547-557.
    CrossRef
  33. Srey S, Jahid IK, Ha SD. 2013. Biofilm formation in food industries: a food safety concern. Food Control 31: 572-585.
    CrossRef
  34. Torlak E, Sert D. 2013. Combined effect of benzalkonium chloride and ultrasound against Listeria monocytogenes biofilm on plastic surface. Lett. Appl. Microbiol. 57: 220-226.
    Pubmed CrossRef
  35. Van Poucke K, Monbaliu S, Munaut F, Heungens K, De Saeger S, Van Hove F. 2012. Genetic diversity and mycotoxin production of Fusarium lactis species complex isolates from sweet pepper. Int. J. Food Microbiol. 153: 28-37.
    Pubmed CrossRef
  36. Yang Z, Cao S, Cai Y, Zheng Y. 2011. Combination of salicylic acid and ultrasound to control postharvest blue mould caused by Penicillium expansum in peach fruit. Innov. Food Sci. Emerg. Technol. 12: 310-314.
    CrossRef

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Article

Research article

J. Microbiol. Biotechnol. 2015; 25(9): 1502-1509

Published online September 28, 2015 https://doi.org/10.4014/jmb.1505.05021

Copyright © The Korean Society for Microbiology and Biotechnology.

Synergistic Effect of Slightly Acidic Electrolyzed Water and Ultrasound at Mild Heat Temperature in Microbial Reduction and Shelf-Life Extension of Fresh-Cut Bell Pepper

Ke Luo 1 and Deog-Hwan Oh 1*

Department of Food Science and Biotechnology and Institute of Bioscience and Biotechnology, Kangwon National University, Chuncheon 200-701, Republic of Korea

Received: May 11, 2015; Accepted: June 1, 2015

Abstract

The objectives of this study were to evaluate the effect of combined treatments (slightly acidic
electrolyzed water (SAEW), ultrasound (US), or mild heat (60°C)) on the growth of Listeria
monocytogenes and Salmonella enterica serovar Typhimurium in fresh-cut bell pepper, and the
shelf-life and sensory quality (color and texture) were followed during storage at 4ºC and
25°C. An additional 0.65, 1.72, and 2.70 log CFU/g reduction was achieved by heat treatments
at 60°C for 1 min for DW, SAEW, and SAEW+US, respectively. Regardless of the type of
pathogen, the combined treatment (SAEW+US+60°C) achieved a significantly (p < 0.05) longer
lag time in all treatment groups. This combined treatment also prolonged the shelf-life of bell
pepper up to 8 days and 30 h for the storage at 4ºC and 25ºC, respectively. There was also no
significant difference in the color and hardness of treated (SAEW+US+60°C) bell pepper from
that of control during the storage. This new hurdle approach is thus expected to improve the
microbial safety of bell peppers during storage and distribution.

Keywords: Fresh-cut bell pepper, Slightly acidic electrolyzed water, Listeria monocytogenes, Salmonella enterica serovar Typhimurium, Ultrasound

References

  1. Ajlouni S, Sibrani H, Premier R, Tomkins B. 2006. Ultrasonication and fresh produce (cos lettuce) preservation. J. Food Sci. 71:62-68.
    CrossRef
  2. Aytac SA, Ben U, Cengiz C, Mercanoglu Taban B. 2010. Evaluation of Salmonella and Listeria monocytogenes contamination on leafy green vegetables. J. Food Agric. Environ. 8: 275-279.
  3. Baranyi J, Roberts TA. 1994. A dynamic approach to predicting bacterial growth in food. Int. J. Food Microbiol. 23:277-294.
    CrossRef
  4. Behravesh CB, Jones TF, Vugia DJ, Long C, Marcus R, Smith K, et al. 2011. Deaths associated with bacterial pathogens transmitted commonly through food: Foodborne Diseases Active Surveillance Network (FoodNet), 1996-2005. J. Infect Dis. 204: 263-267.
    Pubmed CrossRef
  5. Baumann A, Martin SE, Feng H. 2005. Power ultrasound treatment of Listeria monocytogenes in apple cider. J. Food Prot. 68: 2333-2340.
    Pubmed
  6. Brilhante São José JF, Dantas Vanetti MC. 2012. Effect of ultrasound and commercial sanitizers in removing natural contaminants and Salmonella enterica Typhimurium on cherry tomatoes. Food Control 24: 95-99.
    CrossRef
  7. Cao S, Hu Z, Pang B, Wang H, Xie H, Wu F. 2010. Effect of ultrasound treatment on fruit decay and quality maintenance in strawberry after harvest. Food Control 21: 529-532.
    CrossRef
  8. 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: 88-93.
    Pubmed CrossRef
  9. Castro SM, Saraiva JA, Lopes-da-Silva JA, Delgadillo I, Loey AV, Smout C, Hendrickx M. 2008. Effect of thermal blanching and of high pressure treatments on sweet green and red bell pepper fruits (Capsicum annuum L.). Food Chem. 107: 1436-1449.
    CrossRef
  10. Crawford AE. 1963. A practical introduction to ultrasonic cleaning. Ultrasonics 1: 65-69.
    CrossRef
  11. Farber JM, Peterkin PI. 1991. Listeria monocytogenes, a foodborne pathogen. Microbiol. Rev. 55: 476-511.
    Pubmed KoreaMed
  12. Forghani F, Rahman SME, Park MS, Park JH, Park J, Song KB, Oh DH. 2013. Ultrasonication enhanced low concentration electrolyzed water efficacy on bacteria inactivation and shelf life extension on lettuce. Food Sci. Biotechnol. 22: 131-136.
    CrossRef
  13. Forghani F, Oh DH. 2013b. 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: 40-45.
    Pubmed CrossRef
  14. Gogate PR, Kabadi AM. 2009. A review of applications of cavitation in biochemical engineering/biotechnology. Biochem. Eng. J. 44: 60-72.
    CrossRef
  15. Gómez-López VM, Devlieghere F, Ragaert P, Debevere J. 2007. Shelf-life extension of minimally processed carrots by gaseous chlorine dioxide. Int. J. Food Microbiol. 116: 221-227.
    Pubmed CrossRef
  16. Huang Y R, H ung YC, Hsu SY, Huang YW, H wang D F. 2008. Application of electrolyzed water in the food industry. Food Control 19: 329-345.
    CrossRef
  17. Jayasooriya SD, Bhandari BR, Torley P, D’Arcy BR. 2004. Effect of high power ultrasound waves on properties of meat: a review. Int. J. Food Prop. 7: 301-319.
    CrossRef
  18. Koide S, Shitanda D, Note M, Cao W. 2011. Effects of mildly heated, slightly acidic electrolyzed water on the disinfection and physicochemical properties of sliced carrot. Food Control 22: 452-456.
    CrossRef
  19. Koseki S, Yoshida K, Kamiani Y, Isobe S, Itoh K. 2004. Effect of mild heat pretreatment with alkaline electrolyzed water on the efficacy of acidic electrolyzed water against Escherichia coli O157:H7 and Salmonella on lettuce. Food Microbiol. 21: 559-566.
    CrossRef
  20. León-Félix J, Martínez-Bustillos R, Báez-Sa udo M, PerazaGaray F, Chaidez C. 2010. Norovirus contamination of bell pepper from handling during harvesting and packing. Food Environ. Virol. 2: 211-217.
    CrossRef
  21. Leverentz B, Conway WS, Camp MJ, Janisiewicz WJ, Abuladze T, Yang M, et al. 2003. Biocontrol of Listeria monocytogenes on fresh-cut produce by treatment with lytic bacteriophages and a bacteriocin. Appl. Environ. Microbiol. 69: 4519-4526.
    Pubmed KoreaMed CrossRef
  22. Mañas P, Pagán R, Raso J. 2000. Predicting lethal effect of ultrasonic waves under pressure treatments on Listeria monocytogenes ATCC 15313 by power measurements. J. Food Sci. 65: 663-667.
    CrossRef
  23. Mansur AR, Tango CN, Kim GH, Oh DH. 2015. Combined effects of slightly acidic electrolyzed water and fumaric acid on the reduction of foodborne pathogens and shelf life extension of fresh pork. Food Control 47: 277-284.
    CrossRef
  24. McEvoy JL, Luo Y, Conway W, Zhou B, Feng H. 2009. Potential of Escherichia coli O157:H7 to grow on field-cored lettuce as impacted by postharvest storage time and temperature. Int. J. Food Microbiol. 128: 506-509.
    Pubmed CrossRef
  25. Nan S, Li Y, Li B, Wang C, Cui X, Cao W. 2010. Effect of slightly acidic electrolyzed water for inactivating Escherichia coli O157:H7 and Staphylococcus aureus analyzed by transmission electron microscopy. J. Food Prot. 73: 2211-2216.
    Pubmed
  26. Rahman SM, Jin YG, Oh DH. 2011. Combination treatment of alkaline electrolyzed water and citric acid with mild heat to ensure microbial safety, shelf-life and sensory quality of shredded carrots. Food Microbiol. 28: 484-491.
    Pubmed CrossRef
  27. Sagong HG, Lee SY, Chang PS, Heu S, Ryu S, Choi YJ, Kang DH. 2011. 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. 145: 287-292.
    Pubmed CrossRef
  28. Sant’Ana AS, Franco BDGM, Schaffner DW. 2012. Modeling the growth rate and lag time of different strains of Salmonella enterica and Listeria monocytogenes in ready-to-eat lettuce. Food Microbiol. 30: 267-273.
    Pubmed CrossRef
  29. São J osé JFB, Andrade N J, Ramos A M, V anetti M CD , Stringheta PC, Chaves JBP. 2014. Decontamination by ultrasound application in fresh fruits and vegetables. Food Control 45: 36-50.
  30. São José JFB, Medeiros HS, Bernardes PC, Andrade NJ. 2014. Removal of Salmonella enterica Enteritidis and Escherichia coli from green peppers and melons by ultrasound and organic acids. Int. J. Food Microbiol. 190: 9-13.
    Pubmed CrossRef
  31. Scouten AJ, Beuchat LR. 2002. Combined effects of chemical, heat and ultrasound treatments to kill Salmonella and Escherichia coli O157:H7 on alfalfa seeds. J. Appl. Microbiol. 92: 668-674.
    Pubmed CrossRef
  32. Seymour IJ, Burfoot D, Smith RL, Cox LA, Lockwood A. 2002. Ultrasound decontamination of minimally processed fruits and vegetables. Int. J. Food Sci. Technol. 37: 547-557.
    CrossRef
  33. Srey S, Jahid IK, Ha SD. 2013. Biofilm formation in food industries: a food safety concern. Food Control 31: 572-585.
    CrossRef
  34. Torlak E, Sert D. 2013. Combined effect of benzalkonium chloride and ultrasound against Listeria monocytogenes biofilm on plastic surface. Lett. Appl. Microbiol. 57: 220-226.
    Pubmed CrossRef
  35. Van Poucke K, Monbaliu S, Munaut F, Heungens K, De Saeger S, Van Hove F. 2012. Genetic diversity and mycotoxin production of Fusarium lactis species complex isolates from sweet pepper. Int. J. Food Microbiol. 153: 28-37.
    Pubmed CrossRef
  36. Yang Z, Cao S, Cai Y, Zheng Y. 2011. Combination of salicylic acid and ultrasound to control postharvest blue mould caused by Penicillium expansum in peach fruit. Innov. Food Sci. Emerg. Technol. 12: 310-314.
    CrossRef