Skip to content
1887

Access Microbiology open research platform logo Access Microbiology

Volume 7, Issue 12

Influence of antibiotic resistance on disinfectant tolerance of and Open Access

Abstract

Antimicrobial-resistant (AMR) bacteria are an increasing concern for human and animal medicine. As a result, biosecurity measures such as cleaning and disinfection are becoming heavily relied upon to eradicate and control AMR pathogens. However, evidence of co- and cross-resistance between antimicrobials and disinfectants is rising. The influence of AMR on disinfectant tolerance is poorly understood for pathogens of veterinary and public health importance. Therefore, this study aimed to compare disinfectant tolerance of fluoroquinolone-resistant , livestock-associated methicillin-resistant , multi-drug-resistant and vancomycin-resistant , with their antibiotic-susceptible counterparts. disinfectant efficacy was assessed, in the presence of organic matter, against a panel of eight disinfectants from six classes. The disinfectant efficacy varied widely depending on bacterial species and disinfectant class. Furthermore, approved disinfectant concentrations were not always deemed effective. All four bacterial species were typically most susceptible to aldehyde and/or quaternary ammonium compound-based products. Mixed evidence was found to suggest a role of AMR in disinfectant tolerance; no role of AMR was identified in , or , whereas a potential role was identified in .

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): antibiotic resistance , biocides , Campylobacter jejuni , Enterococcus faecium , Escherichia coli and Staphylococcus aureus
© 2025 Crown copyright
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
Loading

Article metrics loading...

/content/journal/acmi/10.1099/acmi.0.001098.v4
2025-12-22
2026-02-15

Metrics

Loading full text...

Full text loading...

/deliver/fulltext/acmi/7/12/acmi001098.v4.html?itemId=/content/journal/acmi/10.1099/acmi.0.001098.v4&mimeType=html&fmt=ahah

References

  1. Salam MdA, Al-Amin MdY, Salam MT, Pawar JS, Akhter N et al. Antimicrobial resistance: a growing serious threat for global public health. Healthcare 2023; 11:1946 [View Article]
     [Google Scholar]
  2. Coque TM, Cantón R, Pérez-Cobas AE, Fernández-de-Bobadilla MD, Baquero F. Antimicrobial resistance in the global health network: known unknowns and challenges for efficient responses in the 21st century. Microorganisms 2023; 11:1050 [View Article] [PubMed]
     [Google Scholar]
  3. WHO WHO list of medically important antimicrobials: a risk management tool for mitigating antimicrobial resistance due to non-human use. Geneva: World Health Organization; 2024
  4. European Parliament and the Council of the European Union Regulation (EU) 2019/ of the European Parliament and of the Council of 11 December 2018 on the manufacture, placing on the market and use of medicated feed, amending Regulation (EC) No 183/2005 of the European Parliament and of the Council and repealing Council Directive 90/167/EEC; 2018 http://data.europa.eu/eli/reg/2019/4/oj
  5. European Parliament and the Council of the European Union Regulation (EU) 2019/ of the European Parliament and of the Council of 11 December 2018 on veterinary medicinal products and repealing Directive 2001/82/EC; 2018 http://data.europa.eu/eli/reg/2019/6/oj
  6. Davies R, Wales A. Antimicrobial resistance on farms: a review including biosecurity and the potential role of disinfectants in resistance selection. Comp Rev Food Sci Food Safe 2019; 18:753–774 [View Article]
     [Google Scholar]
  7. Health and Safety Executive Controlling exposure to disinfectants used in the food and drink industries. n.d https://www.hse.gov.uk/food/occupational-health/disinfectants.htm accessed 28 March 2025
  8. McDonnell G, Russell AD. Antiseptics and disinfectants: activity, action, and resistance. Clin Microbiol Rev 1999; 12:147–179 [View Article] [PubMed]
     [Google Scholar]
  9. Nobrega DB, Tang KL, Caffrey NP, De Buck J, Cork SC et al. Prevalence of antimicrobial resistance genes and its association with restricted antimicrobial use in food-producing animals: a systematic review and meta-analysis. J Antimicrob Chemother 2021; 76:561–575 [View Article]
     [Google Scholar]
  10. Projahn M, Daehre K, Semmler T, Guenther S, Roesler U et al. Environmental adaptation and vertical dissemination of ESBL-/pAmpC-producing Escherichia coli in an integrated broiler production chain in the absence of an antibiotic treatment. Microb Biotechnol 2018; 11:1017–1026 [View Article] [PubMed]
     [Google Scholar]
  11. Chapman JS. Disinfectant resistance mechanisms, cross-resistance, and co-resistance. Int Biodeterior Biodegrad 2003; 51:271–276 [View Article]
     [Google Scholar]
  12. Maillard J-Y, Bloomfield S, Coelho JR, Collier P, Cookson B et al. Does microbicide use in consumer products promote antimicrobial resistance? A critical review and recommendations for a cohesive approach to risk assessment. Microbial Drug Resistance 2013; 19:344–354 [View Article]
     [Google Scholar]
  13. Buffet-Bataillon S, Tattevin P, Bonnaure-Mallet M, Jolivet-Gougeon A. Emergence of resistance to antibacterial agents: the role of quaternary ammonium compounds--a critical review. Int J Antimicrob Agents 2012; 39:381–389 [View Article] [PubMed]
     [Google Scholar]
  14. Maillard JY, Pascoe M. Disinfectants and antiseptics: mechanisms of action and resistance. Nat Rev Microbiol 2024; 22:4–17 [View Article] [PubMed]
     [Google Scholar]
  15. Maillard JY. Resistance of bacteria to biocides. Microbiol Spectr 2018; 6: [View Article] [PubMed]
     [Google Scholar]
  16. Chavan P, Vashishth R. Antimicrobial resistance in foodborne pathogens: consequences for public health and future approaches. Discov Appl Sci 2025; 7:623 [View Article]
     [Google Scholar]
  17. Denyer SP, Maillard JY. Cellular impermeability and uptake of biocides and antibiotics in Gram-negative bacteria. J Appl Microbiol 2002; 92 Suppl:35S–45S [PubMed]
     [Google Scholar]
  18. Russell AD, Gould GW. Resistance of Enterobacteriaceae to preservatives and disinfectants. J Appl Bacteriol 1988; 65: [View Article]
     [Google Scholar]
  19. Zhao A, Sun J, Liu Y. Understanding bacterial biofilms: from definition to treatment strategies. Front Cell Infect Microbiol 2023; 13:1137947 [View Article] [PubMed]
     [Google Scholar]
  20. Bridier A, Briandet R, Thomas V, Dubois-Brissonnet F. Resistance of bacterial biofilms to disinfectants: a review. Biofouling 2011; 27:1017–1032 [View Article] [PubMed]
     [Google Scholar]
  21. Ciofu O, Tolker-Nielsen T. Tolerance and resistance of Pseudomonas aeruginosa biofilms to antimicrobial agents-how P. aeruginosa can escape antibiotics. Front Microbiol 2019; 10:913 [View Article] [PubMed]
     [Google Scholar]
  22. Costa SS, Viveiros M, Rosato AE, Melo-Cristino J, Couto I. Impact of efflux in the development of multidrug resistance phenotypes in Staphylococcus aureus. BMC Microbiol 2015; 15:232 [View Article]
     [Google Scholar]
  23. Lyon BR, Skurray R. Antimicrobial resistance of Staphylococcus aureus: genetic basis. Microbiol Rev 1987; 51:88–134 [View Article] [PubMed]
     [Google Scholar]
  24. Grande Burgos MJ, Fernández Márquez ML, Pérez Pulido R, Gálvez A, Lucas López R. Virulence factors and antimicrobial resistance in Escherichia coli strains isolated from hen egg shells. Int J Food Microbiol 2016; 238:89–95 [View Article] [PubMed]
     [Google Scholar]
  25. Davin-Regli A, Bolla J-M, James CE, Lavigne J-P, Chevalier J et al. Membrane permeability and regulation of drug “influx and efflux” in enterobacterial pathogens. Curr Drug Targets 2008; 9:750–759 [View Article] [PubMed]
     [Google Scholar]
  26. Chuanchuen R, Beinlich K, Hoang TT, Becher A, Karkhoff-Schweizer RR et al. Cross-resistance between triclosan and antibiotics in Pseudomonas aeruginosa is mediated by multidrug efflux pumps: exposure of a susceptible mutant strain to triclosan selects nfxB mutants overexpressing MexCD-OprJ. Antimicrob Agents Chemother 2001; 45:428–432 [View Article] [PubMed]
     [Google Scholar]
  27. Morita Y, Murata T, Mima T, Shiota S, Kuroda T et al. Induction of mexCD-oprJ operon for a multidrug efflux pump by disinfectants in wild-type Pseudomonas aeruginosa PAO1. J Antimicrob Chemother 2003; 51:991–994 [View Article] [PubMed]
     [Google Scholar]
  28. Fernández-Cuenca F, Tomás M, Caballero-Moyano F-J, Bou G, Martínez-Martínez L et al. Reduced susceptibility to biocides in Acinetobacter baumannii: association with resistance to antimicrobials, epidemiological behaviour, biological cost and effect on the expression of genes encoding porins and efflux pumps. J Antimicrob Chemother 2015; 70:3222–3229 [View Article] [PubMed]
     [Google Scholar]
  29. Rajamohan G, Srinivasan VB, Gebreyes WA. Novel role of Acinetobacter baumannii RND efflux transporters in mediating decreased susceptibility to biocides. J Antimicrob Chemother 2010; 65:228–232 [View Article] [PubMed]
     [Google Scholar]
  30. Wales AD, Gosling RJ, Bare HL, Davies RH. Disinfectant testing for veterinary and agricultural applications: a review. Zoonoses Public Health 2021; 68:361–375 [View Article] [PubMed]
     [Google Scholar]
  31. Fraise AP, Lambert PA, Maillard JY. eds Russell, Hugo & Ayliffe’s Principles and Practice of Disinfection, Preservation & Sterilization Oxford, UK: Blackwell Publishing Ltd; 2004 [View Article]
     [Google Scholar]
  32. Sharma M, Nunez-Garcia J, Kearns AM, Doumith M, Butaye PR et al. Livestock-associated methicillin resistant Staphylococcus aureus (LA-MRSA) clonal complex (CC) 398 isolated from UK animals belong to European lineages. Front Microbiol 2016; 7:1741 [View Article] [PubMed]
     [Google Scholar]
  33. Stubberfield E, AbuOun M, Sayers E, O’Connor HM, Card RM et al. Use of whole genome sequencing of commensal Escherichia coli in pigs for antimicrobial resistance surveillance, United Kingdom, 2018. Eurosurveillance 2019; 24: [View Article]
     [Google Scholar]
  34. Animal and Plant Health Agency APHA efficacy methodologies; 2016
  35. R Core TeamR: a language and environment for statistical computing Vienna, Austria: R Foundation for Statistical Computing; 2021 https://www.R-project.org/
  36. Wickham H. ggplot2: Elegant Graphics for Data Analysis, 2nd ed Cham: Springer international publishing; 2016 p 1
     [Google Scholar]
  37. Wickham H. stringr: simple, consistent wrappers for common string operations1.5.2 2009 https://CRAN.R-project.org/package=stringr accessed 15 September 2025
  38. Sarkar D. lattice: Trellis graphics for R0.22-7 2001 https://CRAN.R-project.org/package=lattice accessed 19 September 2025
  39. Mycock G. Methicillin/antiseptic-resistant Staphylococcus aureus. Lancet 1985; 326:949–950 [View Article]
     [Google Scholar]
  40. Sarwar S, Saleem S, Shahzad F, Jahan S. Identifying and elucidating the resistance of Staphylococcus aureus isolated from hospital environment to conventional disinfectants. Am J Infect Control 2023; 51:178–183 [View Article] [PubMed]
     [Google Scholar]
  41. Wassenaar TM, Ussery D, Nielsen LN, Ingmer H. Review and phylogenetic analysis of qac genes that reduce susceptibility to quaternary ammonium compounds in Staphylococcus species. Eur J Microbiol Immunol 2015; 5:44–61 [View Article] [PubMed]
     [Google Scholar]
  42. al-Masaudi SB, Day MJ, Russell AD. Antimicrobial resistance and gene transfer in Staphylococcus aureus. J Appl Bacteriol 1991; 70:279–290 [View Article] [PubMed]
     [Google Scholar]
  43. Anderson RL, Carr JH, Bond WW, Favero MS. Susceptibility of vancomycin-resistant enterococci to environmental disinfectants. Infect Control Hosp Epidemiol 1997; 18:195–199 [View Article] [PubMed]
     [Google Scholar]
  44. Kampf G, Höfer M, Wendt C. Efficacy of hand disinfectants against vancomycin-resistant enterococci in vitro. J Hosp Infect 1999; 42:143–150 [View Article] [PubMed]
     [Google Scholar]
  45. Sakagami Y, Kajimura K. Bactericidal activities of disinfectants against vancomycin-resistant enterococci. J Hosp Infect 2002; 50:140–144 [View Article] [PubMed]
     [Google Scholar]
  46. Schwaiger K, Harms KS, Bischoff M, Preikschat P, Mölle G et al. Insusceptibility to disinfectants in bacteria from animals, food and humans-is there a link to antimicrobial resistance?. Front Microbiol 2014; 5:88 [View Article] [PubMed]
     [Google Scholar]
  47. Migneault I, Dartiguenave C, Bertrand MJ, Waldron KC. Glutaraldehyde: behavior in aqueous solution, reaction with proteins, and application to enzyme crosslinking. Biotechniques 2004; 37:790–796 [View Article] [PubMed]
     [Google Scholar]
  48. Lepelletier D, Maillard JY, Pozzetto B, Simon A. Povidone iodine: properties, mechanisms of action, and role in infection control and Staphylococcus aureus decolonization. Antimicrob Agents Chemother 2020; 64:e00682-20 [View Article] [PubMed]
     [Google Scholar]
  49. Prindle RF. Phenolic compounds. In Disinfection, Sterilization, and Preservation Philadelphia: Lea & Febiger; 1983 pp 19–224
     [Google Scholar]
  50. Gaurav A, Gupta V, Shrivastava SK, Pathania R. Mechanistic insights into synergy between nalidixic acid and tetracycline against clinical isolates of Acinetobacter baumannii and Escherichia coli. Commun Biol 2021; 4:542 [View Article] [PubMed]
     [Google Scholar]
  51. Buffet-Bataillon S, Tattevin P, Maillard JY, Bonnaure-Mallet M, Jolivet-Gougeon A. Efflux pump induction by quaternary ammonium compounds and fluoroquinolone resistance in bacteria. Future Microbiol 2016; 11:81–92 [View Article] [PubMed]
     [Google Scholar]
  52. Oethinger M, Podglajen I, Kern WV, Levy SB. Overexpression of the marA or soxS regulatory gene in clinical topoisomerase mutants of Escherichia coli. Antimicrob Agents Chemother 1998; 42:2089–2094 [View Article] [PubMed]
     [Google Scholar]
  53. Olliver A, Vallé M, Chaslus-Dancla E, Cloeckaert A. Role of an acrR mutation in multidrug resistance of in vitro-selected fluoroquinolone-resistant mutants of Salmonella enterica serovar Typhimurium. FEMS Microbiol Lett 2004; 238:267–272 [View Article] [PubMed]
     [Google Scholar]
  54. Oethinger M, Kern WV, Jellen-Ritter AS, McMurry LM, Levy SB. Ineffectiveness of topoisomerase mutations in mediating clinically significant fluoroquinolone resistance in Escherichia coli in the absence of the AcrAB efflux pump. Antimicrob Agents Chemother 2000; 44:10–13 [View Article] [PubMed]
     [Google Scholar]
  55. Ricci V, Tzakas P, Buckley A, Piddock LJV. Ciprofloxacin-resistant Salmonella enterica serovar Typhimurium strains are difficult to select in the absence of AcrB and TolC. Antimicrob Agents Chemother 2006; 50:38–42 [View Article] [PubMed]
     [Google Scholar]
  56. Beier RC, Byrd JA, Andrews K, Caldwell D, Crippen TL et al. Disinfectant and antimicrobial susceptibility studies of the foodborne pathogen Campylobacter jejuni isolated from the litter of broiler chicken houses. Poult Sci 2021; 100:1024–1033 [View Article] [PubMed]
     [Google Scholar]
  57. Feodoroff B, de Haan CPA, Ellström P, Sarna S, Hänninen M-L et al. Clonal distribution and virulence of Campylobacter jejuni isolates in blood. Emerg Infect Dis 2013; 19:1653–1655 [View Article] [PubMed]
     [Google Scholar]
  58. Sproston EL, Wimalarathna HML, Sheppard SK. Trends in fluoroquinolone resistance in Campylobacter. Microb Genom 2018; 4:e000198 [View Article] [PubMed]
     [Google Scholar]
  59. Alotaibi SMI, Ayibiekea A, Pedersen AF, Jakobsen L, Pinholt M et al. Susceptibility of vancomycin-resistant and -sensitive Enterococcus faecium obtained from Danish hospitals to benzalkonium chloride, chlorhexidine and hydrogen peroxide biocides. J Med Microbiol 2017; 66:1744–1751 [View Article] [PubMed]
     [Google Scholar]
  60. Rodgers JD, McCullagh JJ, McNamee PT, Smyth JA, Ball HJ. An investigation into the efficacy of hatchery disinfectants against strains of Staphylococcus aureus associated with the poultry industry. Vet Microbiol 2001; 82:131–140 [View Article] [PubMed]
     [Google Scholar]
  61. Willinghan EM, Sander JE, Thayer SG, Wilson JL. Investigation of bacterial resistance to hatchery disinfectants. Avian Diseases 1996; 40:510 [View Article]
     [Google Scholar]
  62. Jang Y, Lee K, Yun S, Lee M, Song J et al. Efficacy evaluation of commercial disinfectants by using Salmonella enterica serovar Typhimurium as a test organism. J Vet Sci 2017; 18:209–216 [View Article] [PubMed]
     [Google Scholar]
  63. Taylor JH, Rogers SJ, Holah JT. A comparison of the bactericidal efficacy of 18 disinfectants used in the food industry against Escherichia coli O157:H7 and Pseudomonas aeruginosa at 10 and 20 oC. J Appl Microbiol 1999; 87:718–725 [View Article]
     [Google Scholar]
/content/journal/acmi/10.1099/acmi.0.001098.v4
Loading
Influence of antibiotic resistance on disinfectant tolerance of Escherichia coli, Staphylococcus aureus, Enterococcus faecium and Campylobacter jejuni
Access Microbiology 7, 001098.v4 (2025); https://doi.org/10.1099/acmi.0.001098.v4
/content/journal/acmi/10.1099/acmi.0.001098.v4
/content/journal/acmi/10.1099/acmi.0.001098.v4
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An error occurred
Approval was partially successful, following selected items could not be processed due to error