Skip to main content
Log in

Antibacterial effects of vinegar N6 and UV-C light-emitting diodes against Shiga toxin-producing and enterohemorrhagic Escherichia coli in fresh beef

  • Research Article
  • Published:
Food Science and Biotechnology Aims and scope Submit manuscript

Abstract

Some Escherichia coli serotypes cause diarrhea in infants and acute gastroenteritis. In this study, the incidence of Shiga toxin-producing (STEC) and enterohemorrhagic (EHEC) E. coli in 310 fresh raw beef samples and the presence of pathogenicity-associated virulence genes in the isolated strains were evaluated. The contamination rate reached 18.06% (STEC, 12.26%; EHEC, 5.81%). The highest rate of identified virulence genes was 8.38% for stx2 and 3.23% for stx2 and eae in STEC and EHEC, respectively. Vinegar N6 significantly lowered E. coli growth in beef samples, depending on its concentration (> 0.5%), treatment temperature (5 or 10 °C), and E. coli type (STEC, EHEC, or enteropathogenic), during 28 days of storage. However, no bactericidal effects were detected, unlike those observed for combined treatment with UV-C LED and vinegar N6. Treatment with vinegar N6 and UV-C LED together may significantly reduce E. coli growth in fresh beef, thereby improving food safety.

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

References

  • Adams M, Hall CJ. Growth inhibition of food-borne pathogens by lactic and acetic acids and their mixtures. International Journal of Food Science & Technology. 23: 287-292 (1988)

    Article  CAS  Google Scholar 

  • Baranyi J, Roberts TA. A dynamic approach to predicting bacterial growth in food. International Journal of Food Microbiology. 23: 277-294 (1994)

    Article  CAS  PubMed  Google Scholar 

  • Barlow RS, Gobius KS, Desmarchelier PM. Shiga toxin-producing Escherichia coli in ground beef and lamb cuts: Results of a one-year study. International Journal of Food Microbiology. 111: 1-5 (2006)

    Article  CAS  PubMed  Google Scholar 

  • Bhaskar S. Foodborne diseases—Disease burden. pp. 1-10. In: Food Safety in the 21st Century, 1st edn. Dudeja P, Gupta RK, Minhas AS (ed). Academic Press, Cambridge, MA, USA (2016)

    Google Scholar 

  • Burnens AP, Boss P, Ørskov F, et al. Occurrence and phenotypic properties of verotoxin producing Escherichia coli in sporadic cases of gastroenteritis. European Journal of Clinical Microbiology and Infectious Diseases. 11: 631-634 (1992)

    Article  CAS  PubMed  Google Scholar 

  • Dickson JS, Anderson ME. Microbiological decontamination of food animal carcasses by washing and sanitizing systems: A review. Journal of Food Protection. 55: 133-140 (1992)

    Article  PubMed  Google Scholar 

  • Ewing WH, Edwards PR. Edwards and Ewing’s Identification of Enterobacteriaceae, 4th edn. Elsevier, New York, NY, USA (1986)

    Google Scholar 

  • Fantelli K, Stephan R. Prevalence and characteristics of shigatoxin-producing Escherichia coli and Listeria monocytogenes strains isolated from minced meat in Switzerland. International Journal of Food Microbiology. 70: 63-69 (2001)

    Article  CAS  PubMed  Google Scholar 

  • Feng P, Weagant SD, Monday SR. Genetic analysis for virulence factors in Escherichia coli O104: H21 that was implicated in an outbreak of hemorrhagic colitis. Journal of Clinical Microbiology. 39: 24-28 (2001)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Food and Food Additives Convention. General test methods, microbial test methods, enterohaemorrhagic E. coli. Available from: https://www.foodsafetykorea.go.kr/foodcode/01_03.jsp?idx=387. Accessed Dec. 20, 2021

  • Friedrich AW, Bielaszewska M, Zhang WL, et al. Escherichia coli harboring Shiga toxin 2 gene variants: Frequency and association with clinical symptoms. Journal of Infectious Diseases. 185: 74-84 (2002)

    Article  CAS  PubMed  Google Scholar 

  • Harm W. Biological Effects of Ultraviolet Radiation, 1st edn. University Press, Cambridge, UK (1980)

    Google Scholar 

  • Heir E, Liland KH, Carlehög M, et al. Reduction and inhibition of Listeria monocytogenes in cold-smoked salmon by verdad N6, a buffered vinegar fermentate, and UV-C treatments. International Journal of Food Microbiology. 291: 48-58 (2019)

    Article  CAS  PubMed  Google Scholar 

  • Jajarmi M, Imani Fooladi AAI, Badouei MA, et al. Virulence genes, Shiga toxin subtypes, major O-serogroups, and phylogenetic background of Shiga toxin-producing Escherichia coli strains isolated from cattle in Iran. Microbial Pathogenesis. 109: 274-279 (2017)

    Article  CAS  PubMed  Google Scholar 

  • Kagambèga A, Martikainen O, Lienemann T, et al. Diarrheagenic Escherichia coli detected by 16-plex PCR in raw meat and beef intestines sold at local markets in Ouagadougou, Burkina Faso. International Journal of Food Microbiology. 153: 154-158 (2012a)

    Article  PubMed  Google Scholar 

  • Kagambèga A, Martikainen O, Siitonen A, et al. Prevalence of diarrheagenic Escherichia coli virulence genes in the feces of slaughtered cattle, chickens, and pigs in Burkina Faso. Microbiologyopen. 1: 276-284 (2012b)

    Article  PubMed  PubMed Central  Google Scholar 

  • Kegode RB, Doetkott DK, Khaitsa ML, et al. Occurrence of Campylobacter species, Salmonella species and generic Escherichia coli in meat products from retail outlets in the Fargo metropolitan area. Journal of Food Safety. 28: 111-125 (2008)

    Article  Google Scholar 

  • Ketcham A, Freddolino PL, Tavazoie S. Intracellular acidification is a hallmark of thymineless death in E. coli. PLoS Genetics. 18: e1010456 (2022)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee GY, Jang HI, Hwang IG, et al. Prevalence and classification of pathogenic Escherichia coli isolated from fresh beef, poultry, and pork in Korea. International Journal of Food Microbiology. 134: 196-200 (2009)

    Article  CAS  PubMed  Google Scholar 

  • McDaniel TK, Jarvis KG, Donnenberg MS, et al. A genetic locus of enterocyte effacement conserved among diverse enterobacterial pathogens. Proceedings of the National Academy of Sciences of the United States of America. 92: 1664-1668 (1995)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ministry of Food and Drug Safety. Korean food code. MFDS Notification; No. 4.16; MFDS: Cheongju, Korea (2021)

  • Moore K, Damrow T. Outbreak of acute gastroenteritis attributable to Escherichia coli serotype O104: H21—Helena. Morbidity and Mortality Weekly Report. 44: 501-503 (1995)

    Google Scholar 

  • Oguma K, Katayama H, Ohgaki S. Photoreactivation of Escherichia coli after low- or medium-pressure UV disinfection determined by an endonuclease sensitive site assay. Applied and Environmental Microbiology. 68: 6029-6035 (2002)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Paton AW, Woodrow MC, Doyle RM, et al. Molecular characterization of a Shiga toxigenic Escherichia coli O113:H21 strain lacking eae responsible for a cluster of cases of hemolytic-uremic syndrome. Journal of Clinical Microbiology. 37: 3357-3361 (1999)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pinela J, Ferreira, ICFR. Nonthermal physical technologies to decontaminate and extend the shelf-life of fruits and vegetables: Trends aiming at quality and safety. Critical Reviews in Food Science and Nutrition. 57: 2095-2111 (2017)

    Article  CAS  PubMed  Google Scholar 

  • Pradel N, Livrelli V, De Champs C, et al. Prevalence and characterization of Shiga toxin-producing Escherichia coli isolated from cattle, food, and children during a one-year prospective study in France. Journal of Clinical Microbiology. 38: 1023-1031 (2000)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reynolds ES. The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. Journal of Cell Biology. 17: 208-212 (1963)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Riley LW, Remis RS, Helgerson SD, et al. Hemorrhagic colitis associated with a rare Escherichia coli serotype. New England Journal of Medicine. 308: 681-685 (1983)

    Article  CAS  PubMed  Google Scholar 

  • Salaheen S, Kim SW, Karns JS, et al. Metagenomic analysis of the fecal microbiomes from Escherichia coli O157: H7-shedding and non-shedding cows on a single dairy farm. Food Control. 102: 76-80 (2019)

    Article  Google Scholar 

  • Scheutz F, Nielsen EM, Frimodt-Møller J, et al. Characteristics of the enteroaggregative Shiga toxin/verotoxin-producing Escherichia coli O104: H4 strain causing the outbreak of haemolytic uraemic syndrome in Germany, May to June 2011. Eurosurveillance. 16: 19889 (2011)

    Article  PubMed  Google Scholar 

  • Song K, Mohseni M, Taghipour F. Application of ultraviolet light-emitting diodes (UV-LEDs) for water disinfection: A review. Water Research. 94: 341-349 (2016)

    Article  CAS  PubMed  Google Scholar 

  • Song K, Taghipour F, Mohseni M. Microorganisms inactivation by continuous and pulsed irradiation of ultraviolet lightemitting diodes (UV-LEDs). Chemical Engineering Journal. 343: 362-370 (2018).

    Article  CAS  Google Scholar 

  • Willshaw GA, Smith HR, Roberts D, et al. Examination of raw beef products for the presence of Vero cytotoxin producing Escherichia coli, particularly those of serogroup O157. Journal of Applied Bacteriology. 75: 420-426 (1993)

    Article  CAS  PubMed  Google Scholar 

  • Würtele MA, Kolbe T, Lipsz M, et al. Application of GaN-based ultraviolet-C light emitting diodes–UV LEDs–for water disinfection. Water Research. 45: 1481-1489 (2011)

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We would like to thank Editage (www.editage.co.kr) for English language editing.

Funding

This study was funded by the Pulmuone Institute of Technology as a part of their annual research budget; hence, no grant number is available.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Young Min Park.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Additional information

Publisher's Note

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

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 22 kb)

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

Ro, E.Y., Choi, M.R., Park, Y.M. et al. Antibacterial effects of vinegar N6 and UV-C light-emitting diodes against Shiga toxin-producing and enterohemorrhagic Escherichia coli in fresh beef. Food Sci Biotechnol 32, 1205–1214 (2023). https://doi.org/10.1007/s10068-023-01260-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10068-023-01260-x

Keywords

Navigation