Skip to main content

Advertisement

SpringerLink
Log in

Bacterial Injury Induced by High Hydrostatic Pressure

  • Published:
Food Engineering Reviews Aims and scope Submit manuscript

Abstract

In food processing, high hydrostatic pressure (HHP) can inactivate microbes, and the inactivation is either lethal or sublethal, depending on the intensity of HHP-induced stress. Inactivation of bacteria is a key to ensure food safety by HHP food processing. This manuscript reviews HHP-induced injury of bacteria such as Escherichia coli, Listeria monocytogenes, and (vegetative) Bacillus subtilis. The stress in the sublethal inactivation depends on HHP level, holding time, bacterial species/strain, and other environmental factors. The sublethal inactivation induces injury of bacteria, and the injured bacteria may recover under suitable conditions. The recovery behavior depends on nutrients surrounding the bacteria and the storage temperature. In the detection of HHP-injured bacteria, detection media and incubation temperature play important roles. Mechanisms involved in HHP-injured bacteria can be discussed from several viewpoints including membrane damage, reactive oxygen species, HHP resistance, ribosomes, metabolome, and colony-forming behavior. HHP-induced injury of molds, yeasts, parasites, and viruses has not been sufficiently studied.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  1. Hayashi R (1987) Possibility to apply high pressure to cooking, processing, pasteurization, and preservation. Shokuhin to Kaihatsu [Food Process Ingred] 22(7):55–62 (in Japanese)

  2. Kimura K, Ida M, Yosida Y et al (1994) Comparison of keeping quality between pressure-processed jam and heat-processed jam: changes in flavor components, hue, and nutrients during storage. Biosci Biotechnol Biochem 58(8):386–1391

    Article  Google Scholar 

  3. Balasubramaniam VM, Barbosa-Cánovas GV, Lelieved HLM (2016) High Pressure Processing of Foods. Springer, New York

    Book  Google Scholar 

  4. Yamamoto K (2017a) Food processing by high hydrostatic pressure. Biosci Biotechnol Biochem 81(4):672–679

    Article  CAS  PubMed  Google Scholar 

  5. Rendueles E, Omer MK, Alvseike O et al (2011) Microbiological food safety assessment of high hydrostatic pressure processing: a review. Lebenson Wiss Technol 44(5):1251–1260

    Article  CAS  Google Scholar 

  6. Schottroff F, Fröhling A, Zunabovic-Pichler M et al (2018) Sublethal injury and viable but non-culturable (VBNC) state in microorganisms during preservation of food and biological materials by non-thermal processes. Front Microbiol. https://doi.org/10.3389/fmicb.2018.02773

    Article  PubMed  PubMed Central  Google Scholar 

  7. Syed QA, Buffa M, Guamis B et al (2016) Factors affecting bacterial inactivation during high hydrostatic pressure processing of foods: A review. Crit Rev Food Sci Nutr 56(3):474–483

    Article  CAS  PubMed  Google Scholar 

  8. Wu VCH (2008) A review of microbial injury and recovery methods in food. Food Microbiol 25(6):735–744

    Article  CAS  PubMed  Google Scholar 

  9. Hoover DG, Metrick C, Papineau AM et al (1989) Biological effects on high hydrostatic pressure on food microorganisms. Food Technol 43:99–107

    Google Scholar 

  10. Mackey BM, Mañas P (2008) Inactivation of Escherichia coli by high pressure. In: Michiels C, Aertsen A, Bartlett D, Yayanos Y (eds) High Pressure Microbiology. ASM Press, Washington DC, pp 53–85

    Google Scholar 

  11. Needs EC, Capellas M, Bland AP et al (2000) Comparison of heat and pressure treatments of skim milk, fortified with whey protein concentrate, for set yogurt preparation: effects on milk proteins and gel structure. J Dairy Res 67(3):329–348

    Article  CAS  PubMed  Google Scholar 

  12. Aertsen A, Meersman F, Hendrickx MEG et al (2009) Biotechnology under high pressure: applications and implications. Trends Biotechnol 27(7):434–441

    Article  CAS  PubMed  Google Scholar 

  13. Meersman F, Smeller L, Heremans K (2006) Protein stability and dynamics in the pressure–temperature plane. Biochim Biophys Acta 1764(3):346–354

    Article  CAS  PubMed  Google Scholar 

  14. Moussa M, Perrier-Cornet J-M, Gervais P (2007) Damage in Escherichia coli cells treated with a combination of high hydrostatic pressure and subzero temperature. Appl Environ Microbiol 73(20):6508–6518

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Takahashi S, Sugimoto N (2013) Effect of pressure on the stability of G-quadruplex DNA: thermodynamics under crowding conditions. Angew Chem Int Ed 52:13774–13778

    Article  CAS  Google Scholar 

  16. Zimmerman SB, Trach SO (1991) Estimation of macromolecule concentrations and excluded volume effects for the cytoplasm of Escherichia coli. J Mol Biol 222(3):599–620

    Article  CAS  PubMed  Google Scholar 

  17. Lullien-Pellerin V, Balny C (2002) High-pressure as a tool to study some proteins’ properties: conformational modification, activity and oligomeric dissociation. Innov Food Sci Emerg Technol 3(3):209–221

    Article  CAS  Google Scholar 

  18. Matsuki H, Goto M, Tada K et al (2013) Thermotropic and barotropic phase behavior of phosphatidylcholine bilayers. Int J Mol Sci 14(2):2282–2302

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Aertsen A, De Spiegeleer P, Vanoirbeek K et al (2005) Induction of oxidative stress by high hydrostatic pressure in Escherichia coli. Appl Environ Microbiol 71(5):2226–2231

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Hite BH (1899) The effect of pressure in the preservation of milk. West Virg Agric Exp Sta Bull 58:15–35

    Google Scholar 

  21. Daryaei H, Yousef AE, Balasubramaniam VM (2016) Microbiological aspects of high-pressure processing of food: inactivation of microbial vegetative cells and spores. In: Balasubramaniam VM, Barbosa-Cánovas GV, Lelieved HLM (eds) High Pressure Processing of Foods. Springer, New York, pp 271–294

    Chapter  Google Scholar 

  22. Reitermayer D, Kafka TA, Lenz CA et al (2018) Interrelation between Tween and the membrane properties and high pressure tolerance of Lactobacillus plantarum. BMC Microbiol 18:72. https://doi.org/10.1186/s12866-018-1203-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Ludwig H, Schreck C (1997) The inactivation of vegetative bacteria by pressure. In: Heremans K (ed) High pressure research in the biosciences and biotechnology. Leuven University Press, Leuven, pp 221–224

    Google Scholar 

  24. Cebrián G, Mañas P, Condón S (2016) Comparative resistance of bacterial foodborne pathogens to non-thermal technologies for food preservation. Front Microbiol 7(734):1–17

    Google Scholar 

  25. Mackey BM, Forestiére K, Isaacs N (1995) Factors affecting the resistance of Listeria monocytogenes to high hydrostatic pressure. Food Biotechnol 9(1–2):1–11

    Article  CAS  Google Scholar 

  26. Alpas H, Kalchayanand N, Bozoglu F et al (1999) Variation in resistance to hydrostatic pressure among strains of food-borne pathogens. Appl Environ Microbiol 65(9):4248–4251

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Black EP, Huppertz THM, Kelly AL et al (2007) Baroprotection of vegetative bacteria by milk constituents: a study of Listeria innocua. Int Dairy J 17(2):104–110

    Article  CAS  Google Scholar 

  28. Koseki S, Mizuno Y, Yamamoto K (2008) Use of mild-heat treatment following high-pressure processing to prevent recovery of pressure-injured Listeria monocytogenes in milk. Food Microbiol 25:288–293

    Article  CAS  PubMed  Google Scholar 

  29. Kimura K, Morimatsu K, Inaoka T et al (2017) Injury and recovery of Escherichia coli ATCC25922 cells treated by high hydrostatic pressure at 400–600 MPa. J Biosci Bioeng 123(6):698–706

    Article  CAS  PubMed  Google Scholar 

  30. Yamamoto K (2017b) “Koatsu shokuhin kakou niokeru shokuhin anzensei kakuho” (Food safety assurance in high pressure food processing). Food Packag 58(9):530–537 (in Japanese)

  31. Davis C (2014) Enumeration of probiotic strains: review of culture-dependent and alternative techniques to quantify viable bacteria. J Microbiol Methods 103:9–17

    Article  CAS  PubMed  Google Scholar 

  32. Wilkinson MG (2018) Flow cytometry as a potential method of measuring bacterial viability in probiotic products: a review. Trends Food Sci Technol 78:1–10

    Article  CAS  Google Scholar 

  33. Kell DB, Kaprelyants AS, Weichart DH et al (1998) Viability and activity in readily culturable bacteria: a review and discussion of the practical issues. Antonie Van Leeuwenhoek Int J Gen Mol Microbiol 73:169–187

    Article  CAS  Google Scholar 

  34. Oliver JD (2005). The viable but nonculturable state in bacteria. J Microbiol 43 (S): 93–100.

  35. Earnshaw RG, Appleyard J, Hurst RM (1995) Understanding physical inactivation processes: combined preservation opportunities using heat, ultrasound and pressure. Int J Food Microbiol 28(2):197–219

    Article  CAS  PubMed  Google Scholar 

  36. Tsuchido T, Kanda K, Shibasaki I (1975) Enhancement of sporicidal activity of an amphoteric surfactant by heating. J Ferment Technol 53(12):862–868

    CAS  Google Scholar 

  37. Nakamura M, Saito K, Katayama T et al (2004) Radiation-heat synergism for inactivation of Alicyclobacillus acidoterrestris spores in citrus juice. J Food Prot 67(11):2538–2543

    Article  Google Scholar 

  38. Koseki S, Yamamoto K (2006) Recovery of Escherichia coli ATCC25922 in phosphate buffered saline after treatment with high hydrostatic pressure. Int J Food Microbiol 110:108–111

    Article  CAS  PubMed  Google Scholar 

  39. Morimatsu K, Inaoka T, Nakaura Y et al (2019) Injury and recovery of Escherichia coli cells in phosphate-buffered saline after high hydrostatic pressure treatment. Food Sci Technol Res 25(3):479–484

    Article  CAS  Google Scholar 

  40. Gounot A-M (1986) Psychrophilic and psychrotrophie microorganisms. Experientia 42:1192–1197

    Article  CAS  PubMed  Google Scholar 

  41. Nakaura Y, Morimatsu K, Inaoka T et al (2019) Listeria monocytogenes cells injured by high hydrostatic pressure and their recovery in nutrient-rich or -free medium during cold storage. High Pressure Res 39(2):324–333

    Article  CAS  Google Scholar 

  42. Nasiłowska J, Sokołowska B, Fonberg-Broczek M (2018) Long-term storage of vegetable juices treated by high hydrostatic pressure: assurance of the microbial safety. BioMed Res Int. https://doi.org/10.1155/2018/7389381

    Article  PubMed  PubMed Central  Google Scholar 

  43. Ray B (1979) Methods to detect stressed microorganisms. J Food Prot 42(4):346–355

    Article  PubMed  Google Scholar 

  44. Hartsell SE (1951) The longevity and behavior of pathogenic bacteria in frozen foods: the influence of plating media. Am J Public Health Nations Health 41(9):1072–1077

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Nakane M, Fuchu H, Nakaura Y et al (2019) Effect of plating and incubation conditions on the detection of lactic acid bacteria after high hydrostatic pressure treatment. High Press Res 39(2):334–343

    Article  CAS  Google Scholar 

  46. Chuang S, Sheen S, Sommers CH et al (2020) Survival evaluation of Salmonella and Listeria monocytogenes on selective and nonselective media in ground chicken meat subjected to high hydrostatic pressure and carvacrol. J Food Prot 83(1):37–44

    Article  CAS  PubMed  Google Scholar 

  47. Mañas P, Pagán R (2005) Microbial inactivation by new technologies of food preservation. J Appl Microbiol 98(6):1387–1399

    Article  PubMed  Google Scholar 

  48. Calabrese JP, Bissonnette GK (1990) Improved membrane filtration method incorporating catalase and sodium pyruvate for detection of chlorine-stressed coliform bacteria. Appl Environ Microbiol 56(11):3558–3564

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Czechowicz S, Santos O, Zottola E (1996) Recovery of thermally-stressed Escherichia coli O157:H7 by media supplemented with pyruvate. Int J Food Microbiol 33(2–3):275–284

    Article  CAS  PubMed  Google Scholar 

  50. McDonald LC, Hackney CR, Ray B (1983) Enhanced recovery of injured Escherichia coli by compounds that degrade hydrogen peroxide or block its formation. Appl Environ Microbiol 45(2):360–365

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Mizunoe Y, Wai SN, Takade A et al (1999) Restoration of culturability of starvation-stressed and low-temperature-stressed Escherichia coli O157 cells by using H2O2-degrading compounds. Arch Microbiol 172:63–67

    Article  CAS  PubMed  Google Scholar 

  52. Morishige Y, Fujimori K, Amano F (2013) Differential resuscitative effect of pyruvate and its analogues on VBNC (viable but non-culturable) Salmonella. Microbes Environ 28(2):180–186

    Article  PubMed  PubMed Central  Google Scholar 

  53. Inaoka T, Kimura K, Morimatsu K et al (2017) Characterization of high hydrostatic pressure-injured Bacillus subtilis cells. Biosci Biotechnol Biochem 81(6):1235–1240

    Article  CAS  PubMed  Google Scholar 

  54. Welch TJ, Farewell A, Neidhardt FC et al (1993) Stress response of Escherichia coli to elevated hydrostatic pressure. J Bacteriol 175(22):7170–7177

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Aertsen A, Vanoirbeek K, De Spiegeleer P et al (2004) Heat shock protein-mediated resistance to high hydrostatic pressure in Escherichia coli. Appl Environ Microbiol 70(5):2660–2666

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Nguyen HTM, Akanuma G, Tu HTM et al (2020) Ribosome reconstruction during recovery from high hydrostatic pressure-induced injury in Bacillus subtilis. Appl Environ Microbiol 86(1):e01640-e1719. https://doi.org/10.1128/AEM.01640-19

    Article  CAS  Google Scholar 

  57. Zundel MA, Basturea GN, Deutscher MP (2009) Initiation of ribosome degradation during starvation in Escherichia coli. RNA 15(5):977–983

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Kaplan R, Apirion D (1975) The fate of ribosomes in Escherichia coli cells starved for a carbon source. J Biol Chem 250(5):1854–1863

    Article  CAS  PubMed  Google Scholar 

  59. Davis BD, Luger SM, Tai PC (1986) Role of ribosome degradation in the death of starved Escherichia coli cells. J Bacteriol 166(2):439–445

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Kimura K, Inaoka T, Yamamoto K (2018) Metabolome analysis of Escherichia coli ATCC25922 cells treated with high hydrostatic pressure at 400 and 600 MPa. J Biosci Bioeng 126(5):611–616

    Article  CAS  PubMed  Google Scholar 

  61. Pandya Y, Jewett FF Jr, Hoover DG (1995) Concurrent effects of high hydrostatic pressure, acidity and heat on the destruction and injury of yeasts. J Food Prot 58(3):301–304

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Food Research Institute, National Agriculture and Food Research Organization, 2-1-12 Kannondai, Tsukuba, Ibaraki, 305-8642, Japan

    Kazutaka Yamamoto, Xue Zhang, Takashi Inaoka, Keitarou Kimura & Yoshiko Nakaura

  2. Graduate School of Agriculture, Ehime University, 3-5-7 Tarumi, Matsuyama, Ehime, 790-8566, Japan

    Kazuya Morimatsu

Authors
  1. Kazutaka Yamamoto
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xue Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Takashi Inaoka
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kazuya Morimatsu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Keitarou Kimura
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yoshiko Nakaura
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kazutaka Yamamoto.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s Note

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yamamoto, K., Zhang, X., Inaoka, T. et al. Bacterial Injury Induced by High Hydrostatic Pressure. Food Eng Rev 13, 442–453 (2021). https://doi.org/10.1007/s12393-020-09271-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12393-020-09271-8

Keywords

Search

Navigation