Skip to main content

Advertisement

Log in

Antimicrobial Effect of Combination Treatment with High Pressure Processing and Mild Heat Against Foodborne Pathogens in Apple Puree

  • RESEARCH
  • Published:
Food and Bioprocess Technology Aims and scope Submit manuscript

Abstract

The objective of this study was to determine the antimicrobial effect of the combination treatment of high pressure processing (HPP) and mild heat against Escherichia coli O157:H7, Salmonella Typhimurium, and Listeria monocytogenes in apple puree. Also, we determined the levels of sub-lethally injured cells according to the treatment condition. Inoculated apple puree was treated at 300 or 400 MPa for up to 7 min at 20, 35, or 50 °C. Increasing the pressure level or treatment temperature resulted in larger reductions of foodborne pathogens. Moreover, the antimicrobial effect of the combination treatment was prominent in apple puree at pH 3.5 than pH 3.8. E. coli O157:H7 and L. monocytogenes exhibited more resistance to the combination treatment with HPP and mild heat than S. Typhimurium. Also, a high proportion of sub-lethally injured E. coli O157:H7 cells was observed. No significant differences in pH, soluble solid contents, and the color of apple puree between control and HPP and mild heat-treated samples were observed during storage for 28 d at 5 °C. This study provides insights into predicting the inactivation patterns of pathogenic bacteria in apple puree by the combination treatment with HPP and mild heat for practical applications.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Data Availability

Data will be made available on request.

References

  • Aktağ, I. G., & Gökmen, V. (2021). Investigations on the formation of α-dicarbonyl compounds and 5-hydroxymethylfurfural in fruit products during storage: New insights into the role of Maillard reaction. Food Chemistry, 363, 130280.

    Article  PubMed  Google Scholar 

  • Allison, A., Chowdhury, S., & Fouladkhah, A. (2018). Synergism of mild heat and high-pressure pasteurization against Listeria monocytogenes and natural microflora in phosphate-buffered saline and raw milk. Microorganisms, 6, 102.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Alpas, H., Kalchayanand, N., Bozoglu, F., & Ray, B. (2000). Interactions of high hydrostatic pressure, pressurization temperature and pH on death and injury of pressure-resistant and pressure-sensitive strains of foodborne pathogens. International Journal of Food Microbiology, 60, 33–42.

    Article  Google Scholar 

  • Argyri, A. A., Papadopoulou, O. S., Nisiotou, A., Tassou, C. C., & Chorianopoulos, N. (2018). Effect of high pressure processing on the survival of Salmonella Enteritidis and shelf-life of chicken fillets. Food Microbiology, 70, 55–64.

    Article  CAS  PubMed  Google Scholar 

  • Bozoglu, F., Alpas, H., & Kaletunç, G. (2004). Injury recovery of foodborne pathogens in high hydrostatic pressure treated milk during storage. FEMS Immunology and Medical Microbiology, 40, 243–247.

    Article  CAS  PubMed  Google Scholar 

  • Bulut, S. (2014). The effects of high-pressure processing at low and subzero temperatures on inactivation of microorganisms in frozen and unfrozen beef mince inoculated with Escherichia coli strain ATCC 25922. Food and Bioprocess Technology, 7, 3033–3044.

    Article  Google Scholar 

  • Buzrul, S., Alpas, H., Largeteau, A., & Demazeau, G. (2008). Inactivation of Escherichia coli and Listeria innocua in kiwifruit and pineapple juices by high hydrostatic pressure. International Journal of Food Microbiology, 124, 275–278.

    Article  CAS  PubMed  Google Scholar 

  • Callejón, R. M., Rodríguez-Naranjo, M. I., Ubeda, C., Hornedo-Ortega, R., Garcia-Parrilla, M. C., & Troncoso, A. M. (2015). Reported foodborne outbreaks due to fresh produce in the United States and European Union: Trends and causes. Foodborne Pathogens and Disease, 12, 32–38.

    Article  PubMed  Google Scholar 

  • Cap, M., Paredes, P. F., Fernández, D., Mozgovoj, M., Vaudagna, S. R., & Rodriguez, A. (2020). Effect of high hydrostatic pressure on Salmonella spp inactivation and meat-quality of frozen chicken breast. LWT, 118, 108873.

    Article  CAS  Google Scholar 

  • Chen, H. (2007). Temperature-assisted pressure inactivation of Listeria monocytogenes in Turkey breast meat. International Journal of Food Microbiology, 117, 55–60.

    Article  CAS  PubMed  Google Scholar 

  • Chien, S. Y., Sheen, S., Sommers, C., & Sheen, L. Y. (2019). Combination effect of high-pressure processing and essential oil (Melissa officinalis extracts) or their constituents for the inactivation of Escherichia coli in ground beef. Food and Bioprocess Technology, 12, 359–370.

    Article  CAS  Google Scholar 

  • Dallagnol, A. M., Barrio, Y., Cap, M., Szerman, N., Castellano, P., Vaudagna, S. R., & Vignolo, G. (2017). Listeria inactivation by the combination of high hydrostatic pressure and lactocin AL705 on cured-cooked pork loin slices. Food and Bioprocess Technology, 10, 1824–1833.

    Article  CAS  Google Scholar 

  • FDA U.S. (2004). Guidance for industry: juice hazard analysis critical control point hazards and controls guidance, 1st ed. Available at: https://www.fda.gov/regulatory-information/search-fda-guidance-documents/guidance-industry-juice-hazard-analysis-critical-control-point-hazards-and-controls-guidance-first. Accessed 22 Mar 2021.

  • Gill, A., & Ramaswamy, H. S. (2008). Application of high pressure processing to kill Escherichia coli O157 in ready-to-eat meats. Journal of Food Protection, 71, 2182–2189.

    Article  PubMed  Google Scholar 

  • Gouvea, F. S., Padilla-Zakour, O. I., Worobo, R. W., Xavier, B. M., Walter, E. H. M., & Rosenthal, A. (2020). Effect of high-pressure processing on bacterial inactivation in açaí juices with varying pH and soluble solids content. Innovative Food Science & Emerging Technologies, 66, 102490.

    Article  CAS  Google Scholar 

  • Huang, H. W., Lung, H. M., Yang, B. B., & Wang, C. Y. (2014). Responses of microorganisms to high hydrostatic pressure processing. Food Control, 40, 250–259.

    Article  Google Scholar 

  • Huang, R., Ye, M., Li, X., Ji, L., Karwe, M., & Chen, H. (2016). Evaluation of high hydrostatic pressure inactivation of human norovirus on strawberries, blueberries, raspberries and in their purees. International Journal of Food Microbiology, 223, 17–24.

    Article  PubMed  Google Scholar 

  • Huang, Y., Ye, M., & Chen, H. (2013). Inactivation of Escherichia coli O157:H7 and Salmonella spp. in strawberry puree by high hydrostatic pressure with/without subsequent frozen storage. International Journal of Food Microbiology, 160, 337–343.

    Article  ADS  PubMed  Google Scholar 

  • Institute of Food Technologists (IFT). (2000). Kinetics of microbial inactivation for alternative food processing technologies. Journal of Food Science, 65, 1–64 (Supplement).

  • Kalchayanand, N., Sikes, T., Dunne, C. P., & Ray, B. (1998). Factors influencing death and injury of foodborne pathogens by hydrostatic pressure-pasteurization. Food Microbiology, 15, 207–214.

    Article  Google Scholar 

  • Krug, M. D., Chapin, T. K., Danyluk, M. D., Goodrich-Schneider, R. M., Schneider, K. R., Harris, L. J., & Worobo, R. W. (2020). Outbreaks of foodborne disease associated with fruit and vegetable juices, 19222019. Food Science & Human Nutrition, 17.

  • Landl, A., Abadias, M., Sárraga, C., Viñas, I., & Picouet, P. A. (2010). Effect of high pressure processing on the quality of acidified Granny Smith apple purée product. Innovative Food Science & Emerging Technologies, 11, 557–564.

    Article  CAS  Google Scholar 

  • Le Gall, S., Even, S., & Lahaye, M. (2016). Fast estimation of dietary fiber content in apple. Journal of Agricultural and Food Chemistry, 64, 1401–1405.

    Article  PubMed  Google Scholar 

  • Lee, E. J., Kim, S. H., & Park, S. H. (2023). Effect of high hydrostatic pressure treatment on the inactivation and sublethal injury of foodborne pathogens and quality of apple puree at different pH. Food Microbiology, 114, 104302.

    Article  CAS  PubMed  Google Scholar 

  • Linton, M., McClements, J. M. J., & Patterso, M. F. (1999). Inactivation of Escherichia coli O157:H7 in orange juice using a combination of high pressure and mild heat. Journal of Food Protection, 62, 277–279.

    Article  CAS  PubMed  Google Scholar 

  • Liu, Y., Gill, A., McMullen, L., & Gänzle, M. G. (2015). Variation in heat and pressure resistance of verotoxigenic and nontoxigenic Escherichia coli. Journal of Food Protection, 78, 111–120.

    Article  CAS  PubMed  Google Scholar 

  • Ma, J., Wang, H., Yu, L., Yuan, W., Fu, W., Gao, F., & Jiang, Y. (2019). Dynamic self-recovery of injured Escherichia coli O157: H7 induced by high pressure processing. LWT, 113, 108308.

    Article  CAS  Google Scholar 

  • Mertens, B., & Deplace, G. (1993). Engineering aspects of high-pressure technology in the food industry. Food Technology, 47, 164–169.

    Google Scholar 

  • Nakaura, Y., Morimatsu, K., Inaoka, T., & Yamamoto, K. (2019). Listeria monocytogenes cells injured by high hydrostatic pressure and their recovery in nutrient-rich or -free medium during cold storage. High Pressure Research, 39, 324–333.

    Article  ADS  CAS  Google Scholar 

  • Pérez-Baltar, A., Serrano, A., Bravo, D., Montiel, R., & Medina, M. (2019). Combined effect of high pressure processing with enterocins or thymol on the inactivation of Listeria monocytogenes and the characteristics of sliced dry-cured ham. Food and Bioprocess Technology, 12, 288–297.

    Article  Google Scholar 

  • Petrus, R. R., Churey, J. J., & Worobo, R. W. (2020). Challenging a range of high pressure processing parameters to inactivate pathogens in orange juice. High Pressure Research, 40, 537–542.

    Article  ADS  Google Scholar 

  • Pokhrel, P. R., Toniazzo, T., Boulet, C., Oner, M. E., Sablani, S. S., Tang, J., & Barbosa-Cánovas, G. V. (2019). Inactivation of Listeria innocua and Escherichia coli in carrot juice by combining high pressure processing, nisin, and mild thermal treatments. Innovative Food Science & Emerging Technologies, 54, 93–102.

    Article  CAS  Google Scholar 

  • Ritz, M., Freulet, M., Orange, N., & Federighi, M. (2000). Effects of high hydrostatic pressure on membrane proteins of Salmonella typhimurium. International Journal of Food Microbiology, 55, 115–119.

    Article  CAS  PubMed  Google Scholar 

  • Ritz, M., Pilet, M. F., Jugiau, F., Rama, F., & Federighi, M. (2006). Inactivation of Salmonella Typhimurium and Listeria monocytogenes using high-pressure treatments: Destruction or sublethal stress? Letters in Applied Microbiology, 42, 357–362.

    Article  CAS  PubMed  Google Scholar 

  • Rojo, M. C., Cristiani, M., Szerman, N., Gonzalez, M. L., Lerena, M. C., Mercado, L. A., & Combina, M. (2019). Reduction of Zygosaccharomyces rouxii population in concentrated grape juices by thermal pasteurization and hydrostatic high pressure processing. Food and Bioprocess Technology, 12, 781–788.

    Article  CAS  Google Scholar 

  • Seok, J. H., & Ha, J. W. (2021). Synergistic mechanism and enhanced inactivation exhibited by UVA irradiation combined with citric acid against pathogenic bacteria on sliced cheese. Food Control, 124, 107861.

    Article  CAS  Google Scholar 

  • Serra-Castelló, C., Possas, A., Jofré, A., Garriga, M., & Bover-Cid, S. (2022). Enhanced high hydrostatic pressure lethality in acidulated raw pet food formulations was pathogen species and strain dependent. Food Microbiology, 104, 104002.

    Article  PubMed  Google Scholar 

  • Sokołowska, B., Skapska, S., Niezgoda, J., Rutkowska, M., Dekowska, A., & Rzoska, S. J. (2014). Inactivation and sublethal injury of Escherichia coli and Listeria innocua by high hydrostatic pressure in model suspensions and beetroot juice. High Pressure Research, 34, 147–155.

    Article  ADS  Google Scholar 

  • Somolinos, M., García, D., Pagán, R., & Mackey, B. (2008). Relationship between sublethal injury and microbial inactivation by the combination of high hydrostatic pressure and citral or tert-butyl hydroquinone. Applied and Environmental Microbiology, 74, 7570–7577.

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  • Tamber, S. (2018). Population-wide survey of Salmonella enterica response to high pressure processing reveals a diversity of responses and tolerance mechanisms. Applied and Environmental Microbiology, 84, e01673-e1717.

    Article  ADS  PubMed  PubMed Central  Google Scholar 

  • Teixeira, J. S., Maier, M. B., Miller, P., Gänzle, M. G., & McMullen, L. M. (2016). The effect of growth temperature, process temperature, and sodium chloride on the high-pressure inactivation of Listeria monocytogenes on ham. European Food Research and Technology, 242, 2021–2029.

    Article  CAS  Google Scholar 

  • Toledo, J., Pulido, R. P., Abriouel, H., Grande, M. J., & Gálvez, A. (2012). Inactivation of Salmonella enterica cells in Spanish potato omelette by high hydrostatic pressure treatments. Innovative Food Science & Emerging Technologies, 14, 25–30.

    Article  Google Scholar 

  • Ukuku, D., Zhang, H., Bari, M., Yamamoto, K., & Kawamoto, S. (2009). Leakage of intracellular UV materials of high hydrostatic pressure–injured Escherichia coli O157:H7 strains in tomato juice. Journal of Food Protection, 72, 2407–2412.

    Article  CAS  PubMed  Google Scholar 

  • Wang, L., Pan, J., Xie, H., Yang, Y., & Lin, C. (2010). Inactivation of Staphylococcus aureus and Escherichia coli by the synergistic action of high hydrostatic pressure and dissolved CO2. International Journal of Food Microbiology, 144, 118–125.

    Article  CAS  PubMed  Google Scholar 

  • Wang, L., Pan, J., Xie, H., Yang, Y., Dianfei, Z., & Zhaona, Z. (2012). Pasteurization of fruit juices of different pH values by combined high hydrostatic pressure and carbon dioxide. Journal of Food Protection, 75, 1873–1877.

    Article  ADS  CAS  Google Scholar 

  • Xu, Z., Wang, Y., Ren, P., Ni, Y., & Liao, X. (2016). Quality of banana puree during storage: A comparison of high pressure processing and thermal pasteurization methods. Food and Bioprocess Technology, 9, 407–420.

    Article  CAS  Google Scholar 

  • Zhao, L., Wang, Y., Qiu, D., & Liao, X. (2014). Effect of ultrafiltration combined with high-pressure processing on safety and quality features of fresh apple juice. Food and Bioprocess Technology, 7, 3246–3258.

    Article  Google Scholar 

  • Zhu, H., Xu, Y., Qi, G., Wang, S., & Wang, H. (2020). Modeling the combined effect of high hydrostatic pressure and mild heat on the sub-lethal injury of Listeria monocytogenes by Box-Behnken design. Journal of Food Process Engineering, 43, e13480.

    Article  Google Scholar 

  • Zou, H., Lin, T., Bi, X., Zhao, L., Wang, Y., & Liao, X. (2016). Comparison of high hydrostatic pressure, high-pressure carbon dioxide and high-temperature short-time processing on quality of mulberry juice. Food and Bioprocess Technology, 9, 217–231.

    Article  CAS  Google Scholar 

Download references

Funding

This research was supported by the Basic Science Research Program through the National Research Foundation of Korea (NRF), funded by the Ministry of Education (NRF-2022R1I1A3053647). This study was carried out with the support of the ‘R&D Program for Forest Science Technology (Project No. 2021332C10-2123A01)’ provided by the Korea Forest Service (Korea Forestry Promotion Institute).

Author information

Authors and Affiliations

Authors

Contributions

Eun-Jung Lee: Investigation, Writing – original draft. Sang-Hyun Park: Conceptualization, Writing – review & editing, Resources, Supervision, Funding acquisition.

Corresponding author

Correspondence to Sang Hyun Park.

Ethics declarations

Competing Interests

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lee, E.J., Park, S.H. Antimicrobial Effect of Combination Treatment with High Pressure Processing and Mild Heat Against Foodborne Pathogens in Apple Puree. Food Bioprocess Technol 17, 736–746 (2024). https://doi.org/10.1007/s11947-023-03168-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11947-023-03168-0

Keywords

Navigation