Validation of a Worst-Case Scenario Method Adapted to the Healthcare Environment for Testing the Antibacterial Effect of Brass Surfaces and Implementation on Hospital Antibiotic-Resistant Strains
Abstract
:1. Introduction
2. Results
2.1. Normalization of the Inoculum
2.2. Spread vs. Non-Spread Inoculum
2.3. Bacterial Recovery Technique Following Exposure to Metal Surfaces
2.4. Setting of WCS Parameters and Validation on Two Reference Strains
2.5. Deployment of the WCS Protocol on 12 Antibiotic Resistant Strains of Bacteria
2.5.1. Gram Positive Bacteria
2.5.2. Gram Negative Bacteria
3. Discussion
4. Materials and Methods
4.1. Metal Samples
4.2. Sample Preparation
4.3. Bacterial Strains
4.4. Strain Preparation
4.5. Inoculum Preparation
4.6. Inoculum Deposit and Exposure
4.7. Neutralization
4.8. Enumeration
4.9. Filtration
4.10. Calculations
4.11. Statistical Analysis
4.12. Data Availability
5. Conclusions
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Centers for Disease Control and Prevention. Healthcare-Associated Infections (HAIs). 2017. Available online: https://www.cdc.gov/winnablebattles/report/hais.html (accessed on 25 March 2020).
- Li, M.; Zheng, A.; Duan, W.; Mu, X.; Liu, C.; Yang, Y.; Wang, X. How to apply SHA 2011 at a subnational level in China’s practical situation: Take children health expenditure as an example. J. Glob. Health 2018, 8, 010801. [Google Scholar] [CrossRef]
- Facciolà, A.; Pellicanò, G.F.; Visalli, G.; Paolucci, I.A.; Venanzi Rullo, E.; Ceccarelli, M.; D’Aleo, F.; Di Pietro, A.; Squeri, R.; Nunnari, G.; et al. The role of the hospital environment in the healthcare-associated infections: A general review of the literature. Eur. Rev. Med. Pharmacol. Sci. 2019, 23, 1266–1278. [Google Scholar] [CrossRef] [PubMed]
- Suleyman, G.; Alangaden, G.; Bardossy, A.C. The role of environmental contamination in the transmission of nosocomial pathogens and healthcare-associated infections. Curr. Infect. Dis. Rep. 2018, 20, 12. [Google Scholar] [CrossRef] [PubMed]
- Otter, J.A.; Yezli, S.; French, G.L. The role played by contaminated surfaces in the transmission of nosocomial pathogens. Infect. Control. Hosp. Epidemiol. 2011, 32, 687–699. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chyderiotis, S.; Legeay, C.; Verjat-Trannoy, D.; Le Gallou, F.; Astagneau, P.; Lepelletier, D. New insights on antimicrobial efficacy of copper surfaces in the healthcare environment: A systematic review. Clin. Microbiol. Infect. 2018, 24, 1130–1138. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zingg, W.; Park, B.J.; Storr, J.; Ahmad, R.; Tarrant, C.; Castro-Sanchez, E.; Perencevich, E.; Widmer, A.; Krause, K.H.; Kilpatrick, C.; et al. Technology for the prevention of antimicrobial resistance and healthcare-associated infections; 2017 Geneva IPC-Think Tank (Part 2). Antimicrob. Resist. Infect. Control. 2019, 8, 83. [Google Scholar] [CrossRef]
- Colin, M.; Klingelschmitt, F.; Charpentier, E.; Josse, J.; Kanagaratnam, L.; De Champs, C.; Gangloff, S.C. Copper alloy touch surfaces in healthcare facilities: An effective solution to prevent bacterial spreading. Materials 2018, 11, 2479. [Google Scholar] [CrossRef] [Green Version]
- Rosenberg, M.; Vija, H.; Kahru, A.; Keevil, C.W.; Ivask, A. Rapid in situ assessment of Cu-ion mediated effects and antibacterial efficacy of copper surfaces. Sci. Rep. 2018, 8, 8172. [Google Scholar] [CrossRef]
- Grass, G.; Rensing, C.; Solioz, M. Metallic copper as an antimicrobial surface. Appl. Environ. Microbiol. 2011, 77, 1541–1547. [Google Scholar] [CrossRef] [Green Version]
- Różańska, A.; Chmielarczyk, A.; Romaniszyn, D.; Sroka-Oleksiak, A.; Bulanda, M.; Walkowicz, M.; Osuch, P.; Knych, T. Antimicrobial properties of selected copper alloys on Staphylococcus aureus and Escherichia coli in different simulations of environmental conditions: With vs. without organic contamination. Int. J. Environ. Res. Public Health 2017, 14, 813. [Google Scholar] [CrossRef] [Green Version]
- Jeanvoine, A.; Meunier, A.; Puja, H.; Bertrand, X.; Valot, B.; Hocquet, D. Contamination of a hospital plumbing system by persister cells of a copper-tolerant high-risk clone of Pseudomonas aeruginosa. Water Res. 2019, 157, 579–586. [Google Scholar] [CrossRef] [PubMed]
- Pal, C.; Asiani, K.; Arya, S.; Rensing, C.; Stekel, D.J.; Larsson, D.G.J.; Hobman, J.L. Metal resistance and its association with antibiotic resistance. Adv. Microb. Physiol. 2017, 70, 261–313. [Google Scholar] [CrossRef] [PubMed]
- Hasman, H.; Aarestrup, F.M. tcrB, a gene conferring transferable copper resistance in Enterococcus faecium: Occurrence, transferability, and linkage to macrolide and glycopeptide resistance. Antimicrob. Agents Chemother 2002, 46, 1410–1416. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Campos, J.; Cristino, L.; Peixe, L.; Antunes, P. MCR-1 in multidrug-resistant and copper-tolerant clinically relevant Salmonella 1,4,[5],12:i:- and S. Rissen clones in Portugal, 2011 to 2015. Eur. Surveill. 2016, 21. [Google Scholar] [CrossRef]
- Weaver, L.; Noyce, J.O.; Michels, H.T.; Keevil, C.W. Potential action of copper surfaces on meticillin-resistant Staphylococcus aureus. J. Appl. Microbiol. 2010, 109, 2200–2205. [Google Scholar] [CrossRef]
- Van Dijck, P.; Sjollema, J.; Cammue, B.P.; Lagrou, K.; Berman, J.; d′Enfert, C.; Andes, D.R.; Arendrup, M.C.; Brakhage, A.A.; Calderone, R.; et al. Methodologies for in vitro and in vivo evaluation of efficacy of antifungal and antibiofilm agents and surface coatings against fungal biofilms. Microb. Cell 2018, 5, 300–326. [Google Scholar] [CrossRef]
- Knobloch, J.K.; Tofern, S.; Kunz, W.; Schütze, S.; Riecke, M.; Solbach, W.; Wuske, T. “Life-like” assessment of antimicrobial surfaces by a new touch transfer assay displays strong superiority of a copper alloy compared to silver containing surfaces. PLoS ONE 2017, 12, e0187442. [Google Scholar] [CrossRef] [Green Version]
- Vincent, M.; Duval, R.E.; Hartemann, P.; Engels-Deutsch, M. Contact killing and antimicrobial properties of copper. J. Appl. Microbiol. 2018, 124, 1032–1046. [Google Scholar] [CrossRef] [Green Version]
- International Standard Organization. ISO 22196:2011 Measurement of Antibacterial Activity on Plastics and Other Non-Porous Surfaces. 2016. Available online: http://www.iso.org/cms/render/live/en/sites/isoorg/contents/data/standard/05/44/54431.html (accessed on 4 October 2018).
- Japanese Industrial Standard. JIS Z 2801 “Antimicrobial Products—Test for ANTIBACTERIAL Activity and Efficacy”. 2010. Available online: https://microchemlab.com/test/jis-z-2801-test-antimicrobial-activity-plastics (accessed on 4 October 2018).
- Agence Française de Normalisation. Surfaces à Propriétés Biocides—Méthode d’évaluation de l’activité Bactéricide de Base d’une Surface Non Poreuse NF S90–700. 2019. Available online: https://norminfo.afnor.org/norme/NF%20S90-700/surfaces-a-proprietes-biocides-methode-devaluation-de-lactivite-bactericide-de-base-dune-surface-non-poreuse/126063 (accessed on 20 May 2019).
- United States Environmental Protection Agency. Test Method for Efficacy of Copper Alloy Surfaces as a Sanitizer. 2008. Available online: https://www.copperalloystewardship.com/sites/default/files/upload/media-library/files/pdfs/us/epa_sanitizer_test_method_copper_alloy_surfaces.pdf (accessed on 4 October 2018).
- Salas, J.R.; Jaberi-Douraki, M.; Wen, X.; Volkova, V.V. Mathematical modeling of the “inoculum effect”: Six applicable models and the MIC advancement point concept. FEMS Microbiol Lett 2020, 367, fnaa012. [Google Scholar] [CrossRef]
- Bruzaud, J.; Tarrade, J.; Celia, E.; Darmanin, T.; Taffin de Givenchy, E.; Guittard, F.; Herry, J.M.; Guilbaud, M.; Bellon-Fontaine, M.N. The design of superhydrophobic stainless steel surfaces by controlling nanostructures: A key parameter to reduce the implantation of pathogenic bacteria. Mater. Sci. Eng. C Mater. Biol. Appl. 2017, 73, 40–47. [Google Scholar] [CrossRef]
- Garrett, T.R.; Bhakoo, M.; Zhang, Z. Bacterial adhesion and biofilms on surfaces. Progr. Nat. Sci 2008, 18, 1049–1056. [Google Scholar] [CrossRef]
- Kotay, S.M.; Donlan, R.M.; Ganim, C.; Barry, K.; Christensen, B.E.; Mathers, A.J. Droplet rather than aerosol-mediated dispersion is the primary mechanism of bacterial transmission from contaminated hand-washing sink traps. Appl. Environ. Microbiol. 2019, 18, 1049–1056. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Monsen, T.; Lövgren, E.; Widerström, M.; Wallinder, L. In vitro effect of ultrasound on bacteria and suggested protocol for sonication and diagnosis of prosthetic infections. J. Clin. Microbiol. 2009, 47, 2496–2501. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- van Hout, D.; Verschuuren, T.D.; Bruijning-Verhagen, P.C.J.; Bosch, T.; Schürch, A.C.; Willems, R.J.L.; Bonten, M.J.M.; Kluytmans, J.A.J.W. Extended-spectrum beta-lactamase (ESBL)-producing and non-ESBL-producing Escherichia coli isolates causing bacteremia in the Netherlands (2014–2016) differ in clonal distribution, antimicrobial resistance gene and virulence gene content. PLoS ONE 2016, 15, e0227604. [Google Scholar] [CrossRef] [Green Version]
- Arnold, R.S.; Thom, K.A.; Sharma, S.; Phillips, M.; Kristie Johnson, J.; Morgan, D.J. Emergence of Klebsiella pneumoniae carbapenemase-producing bacteria. South. Med. J. 2011, 104, 40–45. [Google Scholar] [CrossRef] [Green Version]
- Wilson, B.M.; El Chakhtoura, N.G.; Patel, S.; Saade, E.; Donskey, C.J.; Bonomo, R.A.; Perez, F. Carbapenem-resistant Enterobacter cloacae in patients from the US veterans health administration, 2006–2015. Emerg. Infect. Dis. 2017, 23, 878–880. [Google Scholar] [CrossRef]
- Centers for Disease Control and Prevention. ESBL-Producing Enterobacteriaceae in Healthcare Settings. 2019. Available online: https://www.cdc.gov/hai/organisms/ESBL.html (accessed on 11 June 2019).
- Chmielarczyk, A.; Pilarczyk-Żurek, M.; Kamińska, W.; Pobiega, M.; Romaniszyn, D.; Ziółkowski, G.; Wójkowska-Mach, J.; Bulanda, M. Molecular epidemiology and drug resistance of Acinetobacter baumannii isolated from hospitals in southern Poland: ICU as a risk factor for XDR strains. Microb. Drug Resist. 2016, 22, 328–335. [Google Scholar] [CrossRef]
- Harding, C.M.; Hennon, S.W.; Feldman, M.F. Uncovering the mechanisms of Acinetobacter baumannii virulence. Nat. Rev. Microbiol. 2018, 16, 91–102. [Google Scholar] [CrossRef]
- Serra, C.; Bouharkat, B.; Tir Touil-Meddah, A.; Guénin, S.; Mullié, C. MexXY multidrug efflux system is more frequently overexpressed in ciprofloxacin resistant French clinical isolates compared to hospital environment ones. Front. Microbiol. 2019, 10, 366. [Google Scholar] [CrossRef]
- Bondarczuk, K.; Piotrowska-Seget, Z. Molecular basis of active copper resistance mechanisms in Gram-negative bacteria. Cell Biol Toxicol 2013, 29, 397–405. [Google Scholar] [CrossRef] [Green Version]
- Vincent, M.; Hartemann, P.; Engels-Deutsch, M. Antimicrobial applications of copper. Int. J. Hyg. Environ. Health 2016, 219, 585–591. [Google Scholar] [CrossRef] [PubMed]
- Hans, M.; Mathews, S.; Mücklich, F.; Solioz, M. Physicochemical properties of copper important for its antibacterial activity and development of a unified model. Biointerphases 2016, 11, 18902. [Google Scholar] [CrossRef] [PubMed]
Tested Parameters | Inoculum Count (log10) | Recovery on Brass (log10) | |
---|---|---|---|
Inocula | 2S24H a | 9.5 ± 0.17 b | 4.4 ± 0.85 |
2S48H | 9.4 ± 0.13 | 4.5 ± 0.66 ** | |
3S24H | 9.4 ± 0.13 | 3.7 ± 1.26 * | |
3S48H | 9.3 ± 0.11 | 2.8 ± 1.24 *,** | |
Deposit | 9 µL, spread | 6.0 ± 0.20 | 1.9 ± 0 ** |
1 µL, non-spread | 6.1 ± 0.11 | 2.74 ± 1.06 ** | |
Recovery Volume (Letheen Broth) | 10 mL | 6.1 ± 0.09 | 0.7 ± 1.28 |
20 mL | 6.3 ± 0.10 | 0.9 ± 1.57 | |
Recovery Technique | Ultrasonication | 6.1 ± 0.02 | 2.3 ± 0.61 |
Glass beads | 6.1 ± 0.02 | 2.0 ± 0.61 |
Strain Number | Bacterial Species | Resistance Mechanisms | Sampling Origin | Sampling Year |
---|---|---|---|---|
ABAM14 | Acinetobacter baumannii | Oxa-23, AmpC, TEM | Rectal | 2016 |
ABAM41 | Acinetobacter baumannii | Oxa-23, AmpC, ArmA | Environment | 2017 |
EFUMAM2 | Enteroccus faecium | VanA | Rectal | 2017 |
EFISAM2 | Enterococcus faecalis | VanB | Rectal | 2014 |
ECLOAM1 | Enterobacter cloacae | Carbapenemase (Oxa-48) Extended-spectrum β-lactamase | External Quality Control | 2019 |
ECOLAM1 | Escherichia coli | Extended-spectrum β-lactamase | Rectal | 2019 |
KPNAM1 | Klebsiella pneumoniae | Extended-spectrum β-lactamase | Rectal | 2019 |
KPNAM2 | Klebsiella pneumoniae | Carbapenemase (KPC) | Rectal | 2019 |
AM85 | Pseudomonas aeruginosa | Overexpression of efflux pump | Sputum | 2008 |
PAAM10 | Pseudomonas aeruginosa | Carbapenemase (VIM) | Colostomy | 2017 |
SAAM33 | Staphylococcus aureus | MecA, Overexpression of efflux pump | Tracheal | 2012 |
SAAM118 | Staphylococcus aureus | MecA | Nasal | 2019 |
Strain | CFU/Sample (log10) | Reduction (%) | |||
---|---|---|---|---|---|
Stainless Steel | Brass | Copper | Brass/Stainless Steel | Copper/Stainless Steel | |
ABAM41 | 5.1 ± 5.20 a | 1.2 ± 1.43 | 3.8 ± 3.99 | 99.95 ± 0.051 a,* | 93.15 ± 11.517 * |
ABAM14 | 0 | 0 | 0 | ND b | ND |
EFISAM2 | 0 | 0 | 0 | ND | ND |
EFUMAM2 | 3.0 ± 3.31 | −0.1 ± 0.30 | 3.1 ± 3.42 | 99.92 ± 0.010 *,† | 60.66 ± 53.297 **,† |
ECLOAM1 | 5.0 ± 4.83 | 2.2 ± 2.67 | 2.1 ± 2.41 | 99.44 ± 0.913 *,† | 99.73 ± 0.342 *,† |
ECOLAM1 | 4.9 ± 4.93 | 1.5 ± 1.89 | 3.9 ± 4.26 | 99.34 ± 0.373 *,† | 89.13 ± 3.093 *,† |
KPNAM2 | 5.0 ± 5.01 | 1.8 ± 2.20 | 1.9 ± 2.18 | 99.16 ± 0.582 * | 98.03 ± 2.343 * |
KPNAM1 | 3.8 ± 3.86 | 1.1 ± 1.34 | 1.8 ± 2.11 | 99.77 ± 0.160 * | 99.95 ± 0.068 * |
AM85 | 4.7 ± 4.82 | 0 | −0.5 ± −0.01 | 100.00± 0 * | 99.95 ± 0.094 * |
PAAM10 | 4.6 ± 5.01 | −0.5 ± −0.34 | −0.5 ± −0.16 | 99.97 ± 0.043 * | 100.00 ± 0.001 * |
SAAM33 | 5.2 ± 5.54 | 2.3 ± 2.45 | 2.0 ± 2.34 | 99.85 ± 0.129 *,‡ | 99.97 ± 0.053 *,‡ |
SAAM118 | 5.1 ± 5.24 | 2.7 ± 3.04 | 2.3 ± 2.67 | 99.63 ± 0.524 * | 99.91 ± 0.061 * |
© 2020 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Dauvergne, E.; Lacquemant, C.; Adjidé, C.; Mullié, C. Validation of a Worst-Case Scenario Method Adapted to the Healthcare Environment for Testing the Antibacterial Effect of Brass Surfaces and Implementation on Hospital Antibiotic-Resistant Strains. Antibiotics 2020, 9, 245. https://doi.org/10.3390/antibiotics9050245
Dauvergne E, Lacquemant C, Adjidé C, Mullié C. Validation of a Worst-Case Scenario Method Adapted to the Healthcare Environment for Testing the Antibacterial Effect of Brass Surfaces and Implementation on Hospital Antibiotic-Resistant Strains. Antibiotics. 2020; 9(5):245. https://doi.org/10.3390/antibiotics9050245
Chicago/Turabian StyleDauvergne, Emilie, Corinne Lacquemant, Crespin Adjidé, and Catherine Mullié. 2020. "Validation of a Worst-Case Scenario Method Adapted to the Healthcare Environment for Testing the Antibacterial Effect of Brass Surfaces and Implementation on Hospital Antibiotic-Resistant Strains" Antibiotics 9, no. 5: 245. https://doi.org/10.3390/antibiotics9050245