1887

Abstract

Globally, healthcare-associated infections (HAI) are the most frequent adverse outcome in healthcare delivery. Although bacterial biofilms contribute significantly to the incidence of HAI, few studies have investigated the efficacy of common disinfectants against dry-surface biofilms (DSB). The objective of this study was to evaluate the bactericidal efficacy of seven Environmental Protection Agency (EPA)-registered liquid disinfectants against DSB of and . We hypothesized that overall, there will be significant differences among the bactericidal efficacies of tested disinfectants by product type and active ingredient class. We also hypothesized that depending on the species, higher bactericidal efficacies against DSB will be exhibited after 24 h of dehydration compared to 72 h. Wet-surface biofilms of and were grown following EPA-MLB-SOP-MB-19 and dehydrated for 24 and 72 h to establish DSB. Seven EPA-registered disinfectants were tested against dehydrated DSB following EPA-MLB-SOP-MB-20. Overall, quaternary ammonium plus alcohol, sodium dichloro-s-triazinetrione and hydrogen peroxide products were more efficacious against DSB than quaternary ammoniums for both tested species. While there was no significant difference in the log reductions between 24 and 72 h . biofilms, significantly higher log reductions were observed when products were challenged with 24 h . DSB compared to 72 h . DSB. Species type, active ingredient class and dry time significantly impact disinfectant efficacy against DSB of or .

Funding
This study was supported by the:
  • Diversey Inc., Fort Mill, SC, USA
    • Principle Award Recipient: HaleyF. Oliver
  • This is an open-access article distributed under the terms of the Creative Commons Attribution NonCommercial License.
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2022-03-11
2024-04-18
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References

  1. Al-Tawfiq JA, Tambyah PA. Healthcare associated infections (HAI) perspectives. J Infect Public Health 2014; 7:339–344 [View Article] [PubMed]
    [Google Scholar]
  2. World Health Organization Infection prevention and control; the burden of healthcare-associated infection worldwide. WHO; 2021 https://www.who.int/infection-prevention/publications/burden_hcai/en
  3. Magill SS, Edwards JR, Bamberg W, Beldavs ZG, Dumyati G et al. Multistate point-prevalence survey of health care-associated infections. N Engl J Med 2014; 370:1198–1208 [View Article] [PubMed]
    [Google Scholar]
  4. Center for Disease Control and Prevention Overview: healthcare-associated infections. CDC; 2020 https://www.cdc.gov/hai/data/index.html
  5. Suetens C, Latour K, Kärki T, Ricchizzi E, Kinross P et al. Prevalence of healthcare-associated infections, estimated incidence and composite antimicrobial resistance index in acute care hospitals and long-term care facilities: results from two European point prevalence surveys, 2016 to 2017. Euro Surveill 2018; 23:46 [View Article] [PubMed]
    [Google Scholar]
  6. World Health Organization WHO Guidelines on Hand Hygiene in Health Care: First Global Patient Safety Challenge Clean Care Is Safer Care. Geneva: WHO; 2009 https://www.ncbi.nlm.nih.gov/books/NBK144030 [PubMed]
  7. Bagheri Nejad S, Allegranzi B, Syed SB, Ellis B, Pittet D. Health-care-associated infection in Africa: a systematic review. Bull World Health Organ 2011; 89:757–765 [View Article] [PubMed]
    [Google Scholar]
  8. World Health Organization Report on the burden of endemic health care-associated Infection Worldwide: clean care is safer care. WHO; 2011 https://apps.who.int/iris/bitstream/handle/10665/80135/9789241501507_eng.pdf;jsessionid=B61B01FA0EEB0CD0B3496FDC5E507810?sequence=1
  9. Jamal M, Ahmad W, Andleeb S, Jalil F, Imran M et al. Bacterial biofilm and associated infections. J Chin Med Assoc 2018; 81:7–11 [View Article] [PubMed]
    [Google Scholar]
  10. Otter JA, Vickery K, Walker JT, deLancey Pulcini E, Stoodley P et al. Surface-attached cells, biofilms and biocide susceptibility: implications for hospital cleaning and disinfection. J Hosp Infect 2015; 89:16–27 [View Article] [PubMed]
    [Google Scholar]
  11. Chowdhury D, Tahir S, Legge M, Hu H, Prvan T et al. Transfer of dry surface biofilm in the healthcare environment: the role of healthcare workers’ hands as vehicles. J Hosp Infect 2018; 100:e85–e90 [View Article] [PubMed]
    [Google Scholar]
  12. Almatroudi A, Gosbell IB, Hu H, Jensen SO, Espedido BA et al. Staphylococcus aureus dry-surface biofilms are not killed by sodium hypochlorite: implications for infection control. J Hosp Infect 2016; 93:263–270 [View Article] [PubMed]
    [Google Scholar]
  13. Nkemngong CA, Voorn MG, Li X, Teska PJ, Oliver HF. A rapid model for developing dry surface biofilms of Staphylococcus aureus and Pseudomonas aeruginosa for in vitro disinfectant efficacy testing. Antimicrob Resist Infect Control 2020; 9:134 [View Article] [PubMed]
    [Google Scholar]
  14. Donlan RM. Role of biofilms in antimicrobial resistance. ASAIO J 2000; 46:S47–52 [View Article] [PubMed]
    [Google Scholar]
  15. Flemming HC, Wingender J. Relevance of microbial extracellular polymeric substances (EPSs)--Part I: Structural and ecological aspects. Water Sci Technol 2001; 43:1–8 [PubMed]
    [Google Scholar]
  16. Stoodley P, Hall-Stoodley L, Costerton B, DeMeo P, Shirtliff M et al. Biofilms, biomaterials, and device-related infections. handbook of polymer applications in medicine and medical devices New York: William Andrew; 2013
    [Google Scholar]
  17. Vickery K, Deva A, Jacombs A, Allan J, Valente P et al. Presence of biofilm containing viable multiresistant organisms despite terminal cleaning on clinical surfaces in an intensive care unit. J Hosp Infect 2012; 80:52–55 [View Article] [PubMed]
    [Google Scholar]
  18. 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]
  19. Stewart PS. Mechanisms of antibiotic resistance in bacterial biofilms. Int J Med Microbiol 2002; 292:107–113 [View Article] [PubMed]
    [Google Scholar]
  20. Saggu SK, Jha G, Mishra PC. Enzymatic degradation of biofilm by metalloprotease from Microbacterium sp. SKS10. Front Bioeng Biotechnol 2019; 7:192 [View Article] [PubMed]
    [Google Scholar]
  21. Almatroudi A, Hu H, Deva A, Gosbell IB, Jacombs A et al. A new dry-surface biofilm model: An essential tool for efficacy testing of hospital surface decontamination procedures. J Microbiol Methods 2015; 117:171–176 [View Article] [PubMed]
    [Google Scholar]
  22. Vickery K. Special issue: microbial biofilms in healthcare: formation, prevention and treatment. Materials (Basel) 2019; 12:E2001 [View Article] [PubMed]
    [Google Scholar]
  23. Ledwoch K, Said J, Norville P, Maillard J-Y. Artificial dry surface biofilm models for testing the efficacy of cleaning and disinfection. Lett Appl Microbiol 2019; 68:329–336 [View Article] [PubMed]
    [Google Scholar]
  24. Ledwoch K, Dancer SJ, Otter JA, Kerr K, Roposte D et al. Beware biofilm! Dry biofilms containing bacterial pathogens on multiple healthcare surfaces; a multi-centre study. J Hosp Infect 2018; 100:e47–e56 [View Article] [PubMed]
    [Google Scholar]
  25. Mandakhalikar KD, Rahmat JN, Chiong E, Neoh KG, Shen L et al. Extraction and quantification of biofilm bacteria: Method optimized for urinary catheters. Sci Rep 2018; 8:8069 [View Article] [PubMed]
    [Google Scholar]
  26. Sievert DM, Ricks P, Edwards JR, Schneider A, Patel J et al. Antimicrobial-resistant pathogens associated with healthcare-associated infections: summary of data reported to the National Healthcare Safety Network at the Centers for Disease Control and Prevention, 2009-2010. Infect Control Hosp Epidemiol 2013; 34:1–14 [View Article] [PubMed]
    [Google Scholar]
  27. Weiner LM, Webb AK, Limbago B, Dudeck MA, Patel J et al. Antimicrobial-Resistant Pathogens Associated With Healthcare-Associated Infections: Summary of Data Reported to the National Healthcare Safety Network at the Centers for Disease Control and Prevention, 2011-2014. Infect Control Hosp Epidemiol 2016; 37:1288–1301 [View Article] [PubMed]
    [Google Scholar]
  28. Zhang X, Bishop PL. Biodegradability of biofilm extracellular polymeric substances. Chemosphere 2003; 50:63–69 [View Article] [PubMed]
    [Google Scholar]
  29. Almatroudi A, Tahir S, Hu H, Chowdhury D, Gosbell IB et al. Staphylococcus aureus dry-surface biofilms are more resistant to heat treatment than traditional hydrated biofilms. J Hosp Infect 2018; 98:161–167 [View Article] [PubMed]
    [Google Scholar]
  30. Flemming HC, Wingender J. The biofilm matrix. Nat Rev Microbiol 2010; 8:623–633 [View Article] [PubMed]
    [Google Scholar]
  31. Environmental Protection Agency EPA MLB SOP MB-19: growing a biofilm using the CDC biofilm reactor. EPA; 2017 https://www.epa.gov/sites/production/files/2020-02/documents/mb-19-05.pdf
  32. Mehtar S, Hopman J, Duse A, Doll M. Patient areas and environmental cleaning. guide to infection control in the hospital brookline. Int J Infect Dis 20181–7
    [Google Scholar]
  33. Ledwoch K, Magoga M, Williams D, Fabbri S, Walsh J et al. Is a reduction in viability enough to determine biofilm susceptibility to a biocide?. Infect Control Hosp Epidemiol 2021; 42:1486–1492 [View Article] [PubMed]
    [Google Scholar]
  34. Center for Disease Control and Prevention Disinfection and sterilization CDC; 2019 https://www.cdc.gov/infectioncontrol/guidelines/disinfection/index.html
  35. Environmental Protection Agency Methods and guidance for testing the efficacy of antimicrobial products against biofilms on hard, non-porous surfaces EPA; 2017 https://www.epa.gov/pesticide-analytical-methods/methods-and-guidance-testing-efficacy-antimicrobial-products-against#efficacy-data
  36. Lineback CB, Nkemngong CA, Wu ST, Li X, Teska PJ et al. Hydrogen peroxide and sodium hypochlorite disinfectants are more effective against Staphylococcus aureus and Pseudomonas aeruginosa biofilms than quaternary ammonium compounds. Antimicrob Resist Infect Control 2018; 7:154 [View Article] [PubMed]
    [Google Scholar]
  37. Denyer SP, Stewart G. Mechanisms of action of disinfectants. Int Biodeterior Biodegradation 1998; 41:261–268 [View Article]
    [Google Scholar]
  38. Finnegan M, Linley E, Denyer SP, McDonnell G, Simons C et al. Mode of action of hydrogen peroxide and other oxidizing agents: differences between liquid and gas forms. J Antimicrob Chemother 2010; 65:2108–2115 [View Article] [PubMed]
    [Google Scholar]
  39. Jennings LK, Storek KM, Ledvina HE, Coulon C, Marmont LS et al. Pel is a cationic exopolysaccharide that cross-links extracellular DNA in the Pseudomonas aeruginosa biofilm matrix. Proc Natl Acad Sci U S A 2015; 112:11353–11358 [View Article] [PubMed]
    [Google Scholar]
  40. Fleming J. The benefits of alcohol-quaternary ammonium germicidal wBenefits of Alcohol-Quaternary Ammonium Germicidal Wipes; 2009 https://www.infectioncontroltoday.com/view/benefits-alcohol-quaternary-ammonium-germicidal-wipes
  41. Voorn MG, Goss SE, Nkemngong CA, Li X, Teska PJ et al. Cross-contamination by disinfectant towelettes varies by product chemistry and strain. Antimicrob Resist Infect Control 2020; 9:141 [View Article] [PubMed]
    [Google Scholar]
  42. West AM, Nkemngong CA, Voorn MG, Wu T, Li X et al. Surface area wiped, product type, and target strain impact bactericidal efficacy of ready-to-use disinfectant Towelettes. Antimicrob Resist Infect Control 2018; 7:122 [View Article] [PubMed]
    [Google Scholar]
  43. Toté K, Horemans T, Vanden Berghe D, Maes L, Cos P. Inhibitory effect of biocides on the viable masses and matrices of Staphylococcus aureus and Pseudomonas aeruginosa biofilms. Appl Environ Microbiol 2010; 76:3135–3142 [View Article] [PubMed]
    [Google Scholar]
  44. Tiwari S, Rajak S, Mondal DP, Biswas D. Sodium hypochlorite is more effective than 70% ethanol against biofilms of clinical isolates of Staphylococcus aureus . Am J Infect Control 2018; 46:e37–e42 [View Article] [PubMed]
    [Google Scholar]
  45. Wesgate R, Robertson A, Barrell M, Teska P, Maillard J-Y. Impact of test protocols and material binding on the efficacy of antimicrobial wipes. J Hosp Infect 2019; 103:e25–e32 [View Article] [PubMed]
    [Google Scholar]
  46. Amaeze N, Akinbobola A, Chukwuemeka V, Abalkhaila A, Ramage G et al. Development of a high throughput and low cost model for the study of semi-dry biofilms. Biofouling 2020; 36:403–415 [View Article] [PubMed]
    [Google Scholar]
  47. Abdallah M, Khelissa O, Ibrahim A, Benoliel C, Heliot L et al. Impact of growth temperature and surface type on the resistance of Pseudomonas aeruginosa and Staphylococcus aureus biofilms to disinfectants. Int J Food Microbiol 2015; 214:38–47 [View Article] [PubMed]
    [Google Scholar]
  48. Chang W-S, van de Mortel M, Nielsen L, Nino de Guzman G, Li X et al. Alginate production by Pseudomonas putida creates a hydrated microenvironment and contributes to biofilm architecture and stress tolerance under water-limiting conditions. J Bacteriol 2007; 189:8290–8299 [View Article] [PubMed]
    [Google Scholar]
  49. Ghafoor A, Hay ID, Rehm BHA. Role of exopolysaccharides in Pseudomonas aeruginosa biofilm formation and architecture. Appl Environ Microbiol 2011; 77:5238–5246 [View Article] [PubMed]
    [Google Scholar]
  50. Allesen-Holm M, Barken KB, Yang L, Klausen M, Webb JS et al. A characterization of DNA release in Pseudomonas aeruginosa cultures and biofilms. Mol Microbiol 2006; 59:1114–1128 [View Article] [PubMed]
    [Google Scholar]
  51. Hay ID, Remminghorst U, Rehm BHA. MucR, a novel membrane-associated regulator of alginate biosynthesis in Pseudomonas aeruginosa . Appl Environ Microbiol 2009; 75:1110–1120 [View Article] [PubMed]
    [Google Scholar]
  52. Pier GB, Coleman F, Grout M, Franklin M, Ohman DE et al. Role of alginate O acetylation in resistance of mucoid Pseudomonas aeruginosa to opsonic phagocytosis. Infect Immun 2001; 69:1895–1901 [View Article] [PubMed]
    [Google Scholar]
  53. Colvin KM, Gordon VD, Murakami K, Borlee BR, Wozniak DJ et al. The pel polysaccharide can serve a structural and protective role in the biofilm matrix of Pseudomonas aeruginosa . PLoS Pathog 2011; 7:e1001264 [View Article] [PubMed]
    [Google Scholar]
  54. McDonnell G, Russell AD. Antiseptics and disinfectants: activity, action, and resistance. Clin Microbiol Rev 1999; 12:147–179 [View Article]
    [Google Scholar]
  55. Bloomfield SF. Chlorine and iodine formulations. In Ascenzi MJ. eds Handbook of Disinfectants and Antiseptics New York, NY: Marcel Dekker, Inc; 1996 pp 133–158
    [Google Scholar]
  56. Block SS. Peroxygen compounds. In Disinfection, Sterilization, and Preservation, 4th ed. Philadelphia, Pa: Lea & Febiger; 1991 pp 167–181
    [Google Scholar]
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