Efficacy of surface disinfectant cleaners against emerging highly resistant gram-negative bacteria

BMC Infectious Diseases

Günter Kampf³  Christiane Ostermeyer²  Anastasija Schlicht¹  Mirja Reichel⁴ 

[1] Labor L + S AG, Mangelsfeld 4, 5, 6, 97708, Bad Bocklet-Groβenbrach, Germany;Microbiology, Bode Chemie GmbH, Melanchthonstr. 27, 22525 Hamburg, Germany;Institut für Hygiene und Umweltmedizin, Ernst-Moritz-Arndt Universität Greifswald, Walther-Rathenau-Straβe 49a, 17475 Greifswald, Germany;Bode Science Center, Bode Chemie GmbH, Melanchthonstr. 27, 22525 Hamburg, Germany

关键词: Pan-drug resistance;    Multidrug resistance;    Gram-negative bacteria;    Surface disinfection cleaner;   

Others  :  1127691
DOI  :  10.1186/1471-2334-14-292

 received in 2014-02-21, accepted in 2014-05-21,  发布年份 2014

【 摘 要 】

Background

Worldwide, the emergence of multidrug-resistant gram-negative bacteria is a clinical problem. Surface disinfectant cleaners (SDCs) that are effective against these bacteria are needed for use in high risk areas around patients and on multi-touch surfaces. We determined the efficacy of several SDCs against clinically relevant bacterial species with and without common types of multidrug resistance.

Methods

Bacteria species used were ATCC strains; clinical isolates classified as antibiotic-susceptible; and multi-resistant clinical isolates from Klebsiella oxytoca, Klebsiella pneumoniae, and Serratia marcescens (all OXA-48 and KPC-2); Acinetobacter baumannii (OXA-23); Pseudomonas aeruginosa (VIM-1); and Achromobacter xylosoxidans (ATCC strain). Experiments were carried out according to EN 13727:2012 in quadruplicate under dirty conditions. The five evaluated SDCs were based on alcohol and an amphoteric substance (AAS), an oxygen-releaser (OR), surface-active substances (SAS), or surface-active-substances plus aldehydes (SASA; two formulations). Bactericidal concentrations of SDCs were determined at two different contact times. Efficacy was defined as a log₁₀ ≥ 5 reduction in bacterial cell count.

Results

SDCs based on AAS, OR, and SAS were effective against all six species irrespective of the degree of multi-resistance. The SASA formulations were effective against the bacteria irrespective of degree of multi-resistance except for one of the four P. aeruginosa isolates (VIM-1). We found no general correlation between SDC efficacy and degree of antibiotic resistance.

Conclusions

SDCs were generally effective against gram-negative bacteria with and without multidrug resistance. SDCs are therefore suitable for surface disinfection in the immediate proximity of patients. Single bacterial isolates, however, might have reduced susceptibility to selected biocidal agents.

【 授权许可】

   
2014 Reichel et al.; licensee BioMed Central Ltd.

【 参考文献 】

• [1]Wellington EM, Boxall AB, Cross P, Feil EJ, Gaze WH, Hawkey PM, Johnson-Rollings AS, Jones DL, Lee NM, Otten W, Thomas CM, Williams AP: The role of the natural environment in the emergence of antibiotic resistance in gram-negative bacteria. Lancet Infect Dis 2013, 13(2):155-165.
• [2]Vonberg RP, Wolter A, Chaberny IF, Kola A, Ziesing S, Suerbaum S, Gastmeier P: Epidemiology of multi-drug-resistant gram-negative bacteria: data from an university hospital over a 36-month period. Int J Hyg Environ Health 2008, 211(3–4):251-257.
• [3]Savard P, Carroll KC, Wilson LE, Perl TM: The challenges of carbapenemase-producing enterobacteriaceae and infection prevention: protecting patients in the chaos. Infect Control Hosp Epidemiol 2013, 34(7):730-739.
• [4]Magiorakos AP, Suetens C, Monnet DL, Gagliotti C, Heuer OE: The rise of carbapenem resistance in Europe: just the tip of the iceberg? Antimicrobial Resistance and Infection Control 2013, 2(1):6. BioMed Central Full Text
• [5]Meyer E, Schwab F, Schroeren-Boersch B, Gastmeier P: Dramatic increase of third-generation cephalosporin-resistant E. coli in German intensive care units: secular trends in antibiotic drug use and bacterial resistance, 2001 to 2008. Crit Care 2010, 14(3):R113. BioMed Central Full Text
• [6]Kumarasamy KK, Toleman MA, Walsh TR, Bagaria J, Butt F, Balakrishnan R, Chaudhary U, Doumith M, Giske CG, Irfan S, Krishnan P, Kumar AV, Maharjan S, Mushtaq S, Noorie T, Paterson DL, Pearson A, Perry C, Pike R, Rao B, Ray U, Sarma JB, Sharma M, Sheridan E, Thirunarayan MA, Turton J, Upadhyay S, Warner M, Welfare W, Livermore DM: Emergence of a new antibiotic resistance mechanism in India, Pakistan, and the UK: a molecular, biological, and epidemiological study. Lancet Infect Dis 2010, 10(9):597-602.
• [7]Tamma PD, Savard P, Pal T, Sonnevend A, Perl TM, Milstone AM: An outbreak of extended-spectrum beta-lactamase-producing Klebsiella pneumoniae in a neonatal intensive care unit. Infect Control Hosp Epidemiol 2012, 33(6):631-634.
• [8]Mosqueda N, Espinal P, Cosgaya C, Viota S, Plasensia V, Lerma FA, Montero M, Gomez J, Horcajada JP, Vila J, Roca I: Globally expanding carbapenemase finally bursts in Spain: Nosocomial outbreak of Acinetobacter baumannii producing a plasmid-encoded OXA-23 in Barcelona, Spain. Antimicrob Agents Chemother 2013, 57(10):5155-5157.
• [9]Edelstein MV, Skleenova EN, Shevchenko OV, D'Souza JW, Tapalski DV, Azizov IS, Sukhorukova MV, Pavlukov RA, Kozlov RS, Toleman MA, Walsh TR: Spread of extensively resistant VIM-2-positive ST235 Pseudomonas aeruginosa in Belarus, Kazakhstan, and Russia: a longitudinal epidemiological and clinical study. Lancet Infect Dis 2013, 13(10):867-876.
• [10]Tacconelli E, Cataldo MA, Dancer SJ, De Angelis G, Falcone M, Frank U, Kahlmeter G, Pan A, Petrosillo N, Rodriguez-Bano J, Singh N, Venditti M, Yokoe DS, Cookson B: ESCMID guidelines for the management of the infection control measures to reduce transmission of multidrug-resistant Gram-negative bacteria in hospitalized patients. Clin Microbiol Infect 2014, 20(Suppl 1):1-55.
• [11]Magiorakos AP, Srinivasan A, Carey RB, Carmeli Y, Falagas ME, Giske CG, Harbarth S, Hindler JF, Kahlmeter G, Olsson-Liljequist B, Paterson DL, Rice LB, Stelling J, Struelens MJ, Vatopoulos A, Weber JT, Monnet DL: Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect 2012, 18(3):268-281.
• [12]Anonym: Minnesota department of health recommendations for the management of carbapenem-resistant enterobacteriaceae in long-term care facilities. In Infectious Disease Epidemiology PaCD, vol. St. Paul, MN, USA: Minnesota Department of Health; 2012.
• [13]Anonym: Hygienemaßnahmen bei Infektionen oder Besiedelung mit multiresistenten gramnegativen Stäbchen. Bundesgesundheitsblatt 2012, 55(10):1311-1354.
• [14]Block SS: Disinfection, sterilization, and preservation. 4th edition. Philadelphia: Lea & Febiger; 1991.
• [15]Boyce JM, Pittet D: Guideline for hand hygiene in health-care settings, Recommendations of the healthcare infection control practices advisory committee and the HICPAC/SHEA/APIC/IDSA hand hygiene task force. MMWR - Morbidity & Mortality Weekly Report 2002, 51:1-45.
• [16]Gebel J, Sonntag HG, Werner HP, Vacata V, Exner M, Kistemann T: The higher disinfectant resistance of nosocomial isolates of Klebsiella oxytoca: how reliable are indicator organisms in disinfectant testing? Journal of Hospital Infection 2002, 50(4):309-311.
• [17]Kampf G, Degenhardt S, Lackner S, Jesse K, von Baum H, Ostermeyer C: Poorly processed reusable surface disinfection tissue dispensers may be a source of infection. BMC Infect Dis 2014, 14:37. BioMed Central Full Text
• [18]Gortner L, Borkhardt A, Reiss I, Rüden H, Daschner F: Higher disinfectant resistance of nosocomial isolates of Klebsiella oxytoca: indicator organisms in disinfectant testing are not reliable. Journal of Hospital Infection 2003, 53(2):153-155.
• [19]EN 13727:2012: Chemical disinfectants and antiseptics. Quantitative suspension test for the evaluation of bactericidal activity in the medical area. Test method and requirements (phase 2, step 1). Brussels: CEN - Comité Européen de Normalisation; 2012.
• [20]Namba Y, Suzuki A, Takeshima N, Kato N: Comparative study of bectericidal activities of six different disinfectants. Nagoya J Med Sci 1985, 47:101-112.
• [21]Fazlara A, Ekhtelat M: The disinfectant effects of benzalkonium chloride on some important foodborne pathogens. American-Eurasian Journal of Agricultural & Environmental Science 2012, 12(1):23-29.
• [22]McDonnell G, Russell AD: Antiseptics and disinfectants: activity, action, and resistance. Clin Microbiol Rev 1999, 12(1):147-179.
• [23]Ali Y, Kimura A, Coffey MJ, Tyle P: Pharmaceutical suspensions - from formulation development to manufacturing. In Edited by Alok K, Kulshreshtha AK, Onkar N, Singh ON, Wall GM. 2010.
• [24]Shimizu M, Okuzumi K, Yoneyama A, Kunisada T, Araake M, Ogawa H, Kimura S: In vitro antiseptic susceptibility of clinical isolates from nosocomial infections. Dermatology 2002, 204(Suppl 1):21-27.
• [25]Majtan V, Majtanova L: Antibacterial efficacy of disinfectants against some gramnegative bacteria. Cent Eur J Public Health 2002, 10(3):104-106.
• [26]Weber DJ, Rutala WA, Sickbert-Bennett EE: Outbreaks associated with contaminated antiseptics and disinfectants. Antimicrob Agents Chemother 2007, 51(12):4217-4224.
• [27]Miyagi F, Timenetsky J, Alterthum F: Evaluation of bacterial contamination in disinfectants for domestic use. Rev Saude Publica 2000, 34(5):444-448.
• [28]Lee JC, Fialkow PJ: Benzalkonium chloride-source of hospital infection with gram-negative bacteria. JAMA 1961, 177:708-710.
• [29]Vanholder R, Vanhaecke E, Ringoir S: Pseudomonas septicemia due to deficient disinfectant mixing during reuse. Int J Artif Organs 1992, 15(1):19-24.
• [30]Reiss I, Borkhardt A, Fussle R, Sziegoleit A, Gortner L: Disinfectant contaminated with Klebsiella oxytoca as a source of sepsis in babies. Lancet 2000, 356(9226):310.
• [31]Russell AD, Tattawasart U, Maillard JY, Furr JR: Possible link between bacterial resistance and use of antibiotics and biocides. Antimicrob Agents Chemother 1998, 42(8):2151.
• [32]Russell AD: Introduction of biocides into clinical practice and the impact on antibiotic-resistant bacteria. J Appl Microbiol 2002, 92(Suppl):121S-135S.
• [33]Pagedar A, Singh J, Batish VK: Efflux mediated adaptive and cross resistance to ciprofloxacin and benzalkonium chloride in Pseudomonas aeruginosa of dairy origin. J Basic Microbiol 2011, 51(3):289-295.
• [34]Tattawasart U, Maillard JY, Furr JR, Russell AD: Development of resistance to chlorhexidine diacetate and cetylpyridinium chloride in Pseudomonas stutzeri and changes in antibiotic susceptibility. J Hosp Infect 1999, 42(3):219-229.
• [35]Soumet C, Fourreau E, Legrandois P, Maris P: Resistance to phenicol compounds following adaptation to quaternary ammonium compounds in Escherichia coli. Vet Microbiol 2012, 158(1–2):147-152.
• [36]Russell AD: Bacterial adaptation and resistance to antiseptics, disinfectants and preservatives is not a new phenomenon. J Hosp Infect 2004, 57(2):97-104.
• [37]Chuanchuen R, Beinlich K, Hoang TT, Becher A, Karkhoff-Schweizer RR, Schweizer HP: 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(2):428-432.
• [38]Heir E, Langsrud S, Sidhu MS, Steinbakk M: Can disinfectants contribute to antibiotic resistance? Tidsskrift for den Norske laegeforening : tidsskrift for praktisk medicin, ny raekke 2001, 121(27):3201-3206.
• [39]Sidhu MS, Heir E, Leegaard T, Wiger K, Holck A: Frequency of disinfectant resistance genes and genetic linkage with beta-lactamase transposon Tn552 among clinical staphylococci. Antimicrob Agents Chemother 2002, 46(9):2797-2803.
• [40]Zhao WH, Chen G, Ito R, Kimura S, Hu ZQ: Identification of a plasmid-borne blaIMP-11 gene in clinical isolates of Escherichia coli and Klebsiella pneumoniae. J Med Microbiol 2012, 61(Pt 2):246-251.
• [41]Weber DJ, Rutala WA: Use of germicides in the home and the healthcare setting: is there a relationship between germicide use and antibiotic resistance? Infect Control Hosp Epidemiol 2006, 27(10):1107-1119.
• [42]Tschudin-Sutter S, Frei R, Kampf G, Tamm M, Pflimlin E, Battegay M, Widmer AF: Emergence of glutaraldehyde-resistant Pseudomonas aeruginosa. Infect Control Hosp Epidemiol 2011, 32(12):1173-1178.
• [43]Kampf G, Ostermeyer C, Tschudin-Sutter S, Widmer AF: Resistance or adaptation? How susceptible is a 'glutaraldehyde-resistant' Pseudomonas aeruginosa isolate in the absence of selection pressure? J Hosp Infect 2013, 84(4):316-318.
• [44]Kaulfers PM, Marquardt A: Demonstration of formaldehyde dehydrogenase activity in formaldehyde-resistant Enterobacteriaceae. FEMS Microbiol Lett 1991, 63(2–3):335-338.
• [45]Wollmann A, Kaulfers PM: Formaldehyde-resistance in Enterobacteriaceae and Pseudomonas aeruginosa: identification of resistance genes by DNA-hybridization. Zentralbl Hyg Umweltmed 1991, 191(5–6):449-456.
• [46]Kaulfers PM: Epidemiology and reasons for microbial resistance to biocides. Zentralbl Hyg Umweltmed 1995, 197(1–3):252-259.
• [47]Kampf G, Hollingsworth A: Validity of the four European test strains of prEN 12054 for the determination of comprehensive bactericidal activity of an alcohol-based hand rub. Journal of Hospital Infection 2003, 55(3):226-231.
• [48]Kampf G, Hollingsworth A: Comprehensive bactericidal activity of an ethanol-based hand gel in 15 seconds. Ann Clin Microbiol Antimicrob 2008, 7:2. BioMed Central Full Text
• [49]Kampf G, Kramer A: Epidemiologic background of hand hygiene and evaluation of the most important agents for scrubs and rubs. Clin Microbiol Rev 2004, 17(4):863-893.
• [50]prEN 14885: Chemical disinfectants and antiseptics. Application of European standards for chemical disinfectants and antiseptics. Brussels: CEN - Comité Européen de Normalisation; 2013.
• [51]prEN 16615: Chemical disinfectants and antiseptics - Quantitative test method for the evaluation of bactericidal and yeasticidal activity on non-porous surfaces with mechanical action employing wipes in the medical area (4-field-test) - Test method and requirements (phase 2, step 2). Brussels: CEN - Comité Européen de Normalisation; 2013.
• [52]Ott E, Saathoff S, Graf K, Schwab F, Chaberny I: The prevalence of nosocomial and community acquired infections in a university hospital— an observational study. Dtsch Arztebl Int 2013, 110(31–32):533-540.
• [53]Desinfektionsmittelkommission im VAH: Flächendesinfektion/Surface disinfection. In Desinfektionsmittel-Liste des VAH. Edited by VAH. Wiesbaden: mhp-Verlag; 2012.