Power Ultrasound and Organic Acid-Based Hurdle Technology to Reduce Listeria monocytogenes and Salmonella enterica on Fresh Produce
Abstract
1. Introduction
2. Materials and Methods
2.1. Produce Selection and Preparation
2.2. Strains and Culture Conditions
2.3. Inoculation of Produce
2.4. Treatment of Produce
2.4.1. Treatment with Organic Acids
2.4.2. Treatment with Organic Acids and Power Ultrasound
2.5. Enumeration of L. monocytogenes and S. enterica
2.6. Statistical Analysis
3. Results
3.1. Efficacy of Water Alone or in Combination with Power Ultrasound to Reduce Pathogen Populations on Produce
3.2. Reduction in Pathogen Populations on Produce Treated with Organic Acids
3.3. Reduction in Pathogen Populations on Produce Treated with Organic Acids in Combination with Power Ultrasound
4. Discussion
Author Contributions
Funding
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Aiyedun, S.O.; Onarinde, B.A.; Swainson, M.; Dixon, R.A. Foodborne outbreaks of microbial infection from fresh produce in Europe and North America: A systematic review of data from this millennium. Int. J. Food Sci. Technol. 2021, 56, 2215–2223. [Google Scholar] [CrossRef]
- Carstens, C.K.; Salazar, J.K.; Darkoh, C. Multistate outbreaks of foodborne illness in the United States associated with fresh produce from 2010 to 2017. Front. Microbiol. 2019, 10, 2667. [Google Scholar] [CrossRef]
- Olaimat, A.N.; Holley, R.A. Factors influencing the microbial safety of fresh produce: A review. Food Microbiol. 2012, 32, 1–19. [Google Scholar] [CrossRef]
- Wang, H.; Zhou, B.; Feng, H. Chapter 2: Surface Characteristics of Fresh Produce and their Impact on Attachment and Removal of Human Pathogens on Produce Surfaces. In Decontamination of Fresh and Minimally Processed Produce; Gomez-Lopez, M., Ed.; Wiley-Blackwell: Ames, IA, USA, 2012. [Google Scholar]
- Beuchat, L.R.; Adler, B.B.; Lang, M.M. Efficacy of chlorine and a peroxyacetic acid sanitizer in killing Listeria monocytogenes on iceberg and Romaine lettuce using simulated commercial processing conditions. J. Food Prot. 2004, 67, 1238–1242. [Google Scholar] [CrossRef]
- Chinchkar, A.V.; Singh, A.; Singh, S.V.; Acharya, A.M.; Kamble, M.G. Potential sanitizers and disinfectants for fresh fruits and vegetables: A comprehensive review. J. Food Process. Preserv. 2022, 46, e16495. [Google Scholar] [CrossRef]
- Sethi, S.; Nayak, S.L.; Joshi, A.; Sharma, R.R. Chapter 5: Sanitizers for Fresh-cut Fruits and Vegetables. In Fresh-Cut Fruits and Vegetables: Technologies and Mechanisms for Safety Control; Siddiqi, M.W., Ed.; Elsevier-Academic Press: San Diego, CA, USA, 2020. [Google Scholar]
- Chaidez, C.; Castro-del Campo, J.; Heredia, B.; Contreras-Angulo, L.; Gonzalez-Aguilar, G.; Ayala-Zavala, J.F. Chapter 7: Chlorine. In Decontamination of Fresh and Minimally Processed Produce; Gomez-Lopez, M., Ed.; Wiley-Blackwell: Ames, IA, USA, 2012. [Google Scholar]
- Gonzalez-Aguilar, G.; Ayala-Zavala, J.F.; Chaidez-Quiroz, C.; Heredia, J.B.; Castro-del Campo, N. Chapter 12: Peroxyacetic acid. In Decontamination of Fresh and Minimally Processed Produce; Gomez-Lopez, M., Ed.; Wiley-Blackwell: Ames, IA, USA, 2012. [Google Scholar]
- José, J.S.; de Andrade, N.J.; Ramos, A.M.; Vanetti, M.C.D.; Stringheta, P.C.; Chaves, J.B.P. Decontamination by ultrasound application in fresh fruits and vegetables. Food Control 2014, 45, 36–50. [Google Scholar] [CrossRef]
- Bilek, S.E.; Turantaş, F. Decontamination efficiency of high power ultrasound in the fruit and vegetable industry, a review. Int. J. Food Microbiol. 2013, 166, 155–162. [Google Scholar] [CrossRef] [PubMed]
- Piyasena, P.; Mohareb, E.; McKellar, R. Inactivation of microbes using ultrasound: A review. Int. J. Food Microbiol. 2003, 87, 207–216. [Google Scholar] [CrossRef]
- Kovach, S.M. Research: Ensuring Cavitation in a Medical Device Ultrasonic Cleaner. Biomed. Instrum. Technol. 2019, 53, 280–285. [Google Scholar] [CrossRef]
- Zhou, X.; Salazar, J.K.; Fay, M.L.; Zhang, W. Efficacy of Power Ultrasound-Based Hurdle Technology on the Reduction of Bacterial Pathogens on Fresh Produce. Foods 2023, 12, 2653. [Google Scholar] [CrossRef]
- Rafeeq, S.; Ovissipour, R. The Effect Ultrasound and Surfactants on Nanobubbles Efficacy against Listeria innocua and Escherichia coli O157:H7, in Cell Suspension and on Fresh Produce Surfaces. Foods 2021, 10, 2154. [Google Scholar] [CrossRef]
- Wang, J.Y.; Wu, Z.X.; Wang, H.B. Combination of ultrasound-peracetic acid washing and ultrasound-assisted aerosolized ascorbic acid: A novel rinsing-free disinfection method that improves the antibacterial and antioxidant activities in cherry tomato. Ultrason. Sonochem. 2022, 86, 106001. [Google Scholar] [CrossRef] [PubMed]
- Turhan, E.U.; Polat, S.; Erginkaya, Z.; Konuray, G. Investigation of synergistic antibacterial effect of organic acids and ultrasound against pathogen biofilms on lettuce. Food Biosci. 2022, 47, 101643. [Google Scholar] [CrossRef]
- Jiang, Q.Y.; Zhang, M.; Xu, B. Application of ultrasonic technology in postharvested fruits and vegetables storage: A review. Ultrason. Sonochem. 2020, 69, 105261. [Google Scholar] [CrossRef]
- Huang, T.S.; Xu, C.; Walker, K.; West, P.; Zhang, S.; Weese, J. Decontamination efficacy of combined chlorine dioxide with ultrasonication on apples and lettuce. J. Food Sci. 2006, 71, M134–M139. [Google Scholar] [CrossRef]
- Sagong, H.G.; Lee, S.-Y.; Chang, P.-S.; Heu, S.; Ryu, S.; Choi, Y.-J.; Kang, D.-H. 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. [Google Scholar] [CrossRef]
- FDA. CFR-Code of Federal Regulations § 184 Direct Food Substances Affirmed as Generally Recognized as Safe (GRAS). 2024. Available online: https://www.accessdata.fda.gov/scripts/cdrh/cfdocs/cfcfr/CFRSearch.cfm?CFRPart=184&showFR=1&subpartNode=21:3.0.1.1.14.1 (accessed on 29 October 2024).
- Taylor, T.M.; Doores, S.X. Organic acids. In Antimicrobials in Foods, 4th ed.; Davidson, P.M., Taylor, T.M., David, J.R.D., Eds.; CRC Press: Boca Raton, FL, USA, 2020. [Google Scholar]
- CDC. Multistate Outbreak of Salmonella Poona Infections Linked to Imported Cucumbers. 2016. Available online: https://archive.cdc.gov/www_cdc_gov/salmonella/poona-09-15/index.html (accessed on 4 April 2019).
- CDC. Multistate outbreak of listeriosis associated with Jensen Farms cantaloupe—United States, August–September 2011. MMWR 2011, 60, 1357–1358. [Google Scholar]
- CDC. 2014 Outbreak of Listeria Infections Linked to Commercially Produced, Prepackaged Caramel Apples Made from Bidart Bros. Apples. 2015. Available online: https://archive.cdc.gov/www_cdc_gov/listeria/outbreaks/caramel-apples-12-14/index.html (accessed on 19 March 2015).
- José, J.F.B.D.; de Medeiros, H.S.; Bernardes, P.C.; de Andrade, N.J. Removal of Salmonella enterica Enteritidis and Escherichia coli from green peppers and melons by ultrasound and organic acids. Int. J. Food Microbiol. 2014, 190, 9–13. [Google Scholar] [CrossRef]
- Liao, C.H.; Sapers, G.M. Attachment and growth of Salmonella Chester on apple fruits and in vivo response of attached bacteria to sanitizer treatments. J. Food Prot. 2000, 63, 876–883. [Google Scholar] [CrossRef] [PubMed]
- Park, S.H.; Choi, M.R.; Park, J.W.; Park, K.H.; Chung, M.S.; Ryu, S.; Kang, D.H. 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. [Google Scholar] [CrossRef]
- Khouja, B.A.; Mathias, H.; Joshi, M.; Fay, M.L.; Korade, S.; Wong, C.W.Y.; Stewart, D.S.; Zhou, X.; Zhang, W.; Salazar, J.K. Power Ultrasound- and Organic Acid-Based Hurdle Technology to Reduce Listeria monocytogenes and Salmonella enterica on Whole Apples and Peaches. Foods 2025, 14, 1744. [Google Scholar] [CrossRef] [PubMed]
- Hashemi, S.M.B.; Abhari, K.; Khaneghah, A.M. The combined effects of ultrasound and lactic acid in inactivating microorganisms on fresh radish (Raphans raphanistrum subsp. sativus): Microbiological and quality changes. Food Sci. Nutr. 2020, 8, 162–169. [Google Scholar] [CrossRef] [PubMed]
- José, J.F.B.D.; Ramos, A.M.; Vanetti, M.C.D.; de Andrade, N.J. Inactivation of Salmonella Enteritidis on cherry tomatoes by ultrasound, lactic acid, detergent, and silver nanoparticles. Can. J. Microbiol. 2021, 67, 259–270. [Google Scholar] [CrossRef] [PubMed]
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2025 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Fay, M.L.; Biswas, P.; Zhou, X.; Khouja, B.A.; Stewart, D.S.; Wong, C.W.Y.; Zhang, W.; Salazar, J.K. Power Ultrasound and Organic Acid-Based Hurdle Technology to Reduce Listeria monocytogenes and Salmonella enterica on Fresh Produce. Microbiol. Res. 2025, 16, 172. https://doi.org/10.3390/microbiolres16080172
Fay ML, Biswas P, Zhou X, Khouja BA, Stewart DS, Wong CWY, Zhang W, Salazar JK. Power Ultrasound and Organic Acid-Based Hurdle Technology to Reduce Listeria monocytogenes and Salmonella enterica on Fresh Produce. Microbiology Research. 2025; 16(8):172. https://doi.org/10.3390/microbiolres16080172
Chicago/Turabian StyleFay, Megan L., Priya Biswas, Xinyi Zhou, Bashayer A. Khouja, Diana S. Stewart, Catherine W. Y. Wong, Wei Zhang, and Joelle K. Salazar. 2025. "Power Ultrasound and Organic Acid-Based Hurdle Technology to Reduce Listeria monocytogenes and Salmonella enterica on Fresh Produce" Microbiology Research 16, no. 8: 172. https://doi.org/10.3390/microbiolres16080172
APA StyleFay, M. L., Biswas, P., Zhou, X., Khouja, B. A., Stewart, D. S., Wong, C. W. Y., Zhang, W., & Salazar, J. K. (2025). Power Ultrasound and Organic Acid-Based Hurdle Technology to Reduce Listeria monocytogenes and Salmonella enterica on Fresh Produce. Microbiology Research, 16(8), 172. https://doi.org/10.3390/microbiolres16080172