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The prevalence of antiseptic tolerance genes among staphylococci and enterococci in a pediatric population

Published online by Cambridge University Press:  19 March 2019

Lauren M. Sommer
Affiliation:
Department of Pediatrics, Section of Infectious Diseases, Baylor College of Medicine and Texas Children’s Hospital, Houston, Texas
Jennifer L. Krauss
Affiliation:
Department of Pathology, Baylor College of Medicine and Texas Children’s Hospital, Houston, Texas
Kristina G. Hultén
Affiliation:
Department of Pediatrics, Section of Infectious Diseases, Baylor College of Medicine and Texas Children’s Hospital, Houston, Texas
James J. Dunn
Affiliation:
Department of Pathology, Baylor College of Medicine and Texas Children’s Hospital, Houston, Texas
Sheldon L. Kaplan
Affiliation:
Department of Pediatrics, Section of Infectious Diseases, Baylor College of Medicine and Texas Children’s Hospital, Houston, Texas
J. Chase McNeil*
Affiliation:
Department of Pediatrics, Section of Infectious Diseases, Baylor College of Medicine and Texas Children’s Hospital, Houston, Texas
*
Author for correspondence: J. Chase McNeil, Email: [email protected]

Abstract

Objective:

The smr and qacA/B genes in Staphylococcus aureus confer tolerance to antiseptics and are associated with nosocomial acquisition of infection and underlying medical conditions. Such antiseptic tolerance (AT) genes have also been reported in coagulase-negative staphylococci (CoNS) and enterococci, however, few data are available regarding their prevalence. We sought to describe the frequency of AT genes among bloodstream isolates of S. aureus, CoNS and enterococci at Texas Children’s Hospital (TCH).

Methods:

Banked CoNS, S. aureus and enterococci isolated from blood cultures collected bewteen October 1, 2016, and October 1, 2017, were obtained from the TCH clinical microbiology laboratory. All isolates underwent polymerase chain reaction (PCR) assay for the qacA/B and smr genes. Medical records were reviewed for all cases.

Results:

In total, 103 CoNS, 19 Enterococcus spp, and 119 S. aureus isolates were included in the study, and 80.6% of the CoNS possessed at least 1 AT gene compared to 37% of S. aureus and 43.8% of E. faecalis isolates (P < .001). Among CoNS bloodstream isolates, the presence of either AT gene was strongly associated with nosocomial infection (P < .001). The AT genes in S. aureus were associated with nosocomial infection (P = .025) as well as the diagnosis of central-line–associated bloodstream infection (CLABSI; P = .04) and recent hospitalizations (P < .001). We found no correlation with genotypic AT in E. faecalis and any clinical variable we examined.

Conclusions:

Antiseptic tolerance is common among bloodstream staphylococci and E. faecalis isolates at TCH. Among CoNS, the presence of AT genes is strongly correlated with nosocomial acquisition of infection, consistent with previous studies in S. aureus. These data suggest that the healthcare environment contributes to AT among staphylococci.

Type
Original Article
Copyright
© 2019 by The Society for Healthcare Epidemiology of America. All rights reserved. 

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References

Wisplinghoff, H, Seifert, H, Tallent, SM, Bischoff, T, Wenzel, RP, Edmond, MB. Nosocomial bloodstream infections in pediatric patients in United States hospitals: epidemiology, clinical features and susceptibilities. Pediatr Infect Dis J 2003;22:686691.CrossRefGoogle ScholarPubMed
Murray, MT, Krishnamurthy, G, Corda, R, et al. Surgical site infections and bloodstream infections in infants after cardiac surgery. J Thorac Cardiovasc Surg 2014;148:259265.CrossRefGoogle ScholarPubMed
Blackburn, RM, Henderson, KL, Minaji, M, Meuller-Pedobdy, B, Johnson, AP, Sharland, M. Exploring the epidemioogy of hospital-acquired bloodstream infections in children in England (January 2009–March 2010) by linkage of national hospital admissions and microbiological databases. J Pediatr Infect Dis Soc 2012;1:284292.CrossRefGoogle Scholar
Bleasdale, SC, Trick, WE, Gonzalez, IM, Lyles, RD, Hayden, MK, Weinstein, RA. Effectiveness of chlorhexidine bathing to reduce catheter-associated bloodstream infections in medical intensive care unit patients. Arch Intern Med 2007;167:20732079.CrossRefGoogle ScholarPubMed
Climo, MW, Yokoe, DS, Warren, DK, et al. Effect of daily chlorhexidine bathing on hospital-acquired infection. N Engl J Med 2013;368:533542.CrossRefGoogle ScholarPubMed
Lee, BY, Bartsch, SM, Wong, KF, et al. Beyond the intensive care unit (ICU): countywide impact of universal ICU Staphylococcus aureus decolonization. Am J Epidemiol 2016;183:480489.CrossRefGoogle ScholarPubMed
Milstone, AM, Elward, A, Song, X, et al. Daily chlorhexidine bathing to reduce bacteraemia in critically ill children: a multicentre, cluster-randomised, crossover trial. Lancet 2013;381:10991106.CrossRefGoogle ScholarPubMed
Toltzis, P, O’Riordan, M, Cunningham, DJ, et al. A statewide collaborative to reduce pediatric surgical site infections. Pediatrics 2014;134:e1174e1180.CrossRefGoogle ScholarPubMed
Mangram, AJ, Horan, TC, Pearson, ML, Silver, LC, Jarvis, WR. Guideline for prevention of surgical site infection, 1999. Hospital Infection Control Practices Advisory Committee. Infect Control Hosp Epidemiol 1999;20:250280.CrossRefGoogle ScholarPubMed
O’Grady, NP, Alexander, M, Burns, LA, et al. Guidelines for the prevention of intravascular catheter-related infections. Clin Infect Dis 2011;52:e162e193.CrossRefGoogle ScholarPubMed
Yokoe, DS, Anderson, DJ, Berenholtz, SM, et al. A compendium of strategies to prevent healthcare-associated infections in acute care hospitals: 2014 updates. Infect Control Hosp Epidemiol 2014;35 suppl 2:S21S31.CrossRefGoogle ScholarPubMed
Rouch, DA, Cram, DS, DiBerardino, D, Littlejohn, TG, Skurray, RA. Efflux-mediated antiseptic resistance gene qacA from Staphylococcus aureus: common ancestry with tetracycline- and sugar-transport proteins. Mol Microbiol 1990;4:20512062.CrossRefGoogle ScholarPubMed
Brown, MH, Skurray, RA. Staphylococcal multidrug efflux protein QacA. J Mol Microbiol Biotechnol 2001;3:163170.Google ScholarPubMed
Paulsen, IT, Brown, MH, Littlejohn, TG, Mitchell, BA, Skurray, RA. Multidrug resistance proteins QacA and QacB from Staphylococcus aureus: membrane topology and identification of residues involved in substrate specificity. Proc Natl Acad Sci USA 1996;93:36303635.CrossRefGoogle ScholarPubMed
Littlejohn, TG, DiBerardino, D, Messerotti, LJ, Spiers, SJ, Skurray, RA. Structure and evolution of a family of genes encoding antiseptic and disinfectant resistance in Staphylococcus aureus. Gene 1991;101:5966.CrossRefGoogle ScholarPubMed
Smith, K, Gemmell, CG, Hunter, IS. The association between biocide tolerance and the presence or absence of qac genes among hospital-acquired and community-acquired MRSA isolates. J Antimicrob Chemother 2008;61:7884.CrossRefGoogle ScholarPubMed
McNeil, JC, Hulten, KG, Kaplan, SL, Mahoney, DH, Mason, EO. Staphylococcus aureus infections in pediatric oncology patients: high rates of antimicrobial resistance, antiseptic tolerance and complications. Pediatr Infect Dis J 2013;32:124128.CrossRefGoogle ScholarPubMed
Suwantarat, N, Carroll, KC, Tekle, T, et al. High prevalence of reduced chlorhexidine susceptibility in organisms causing central line-associated bloodstream infections. Infect Control Hosp Epidemiol 2014;35:11831186.CrossRefGoogle ScholarPubMed
Warren, DK, Prager, M, Munigala, S, et al. Prevalence of qacA/B genes and mupirocin resistance among methicillin-resistant Staphylococcus aureus (MRSA) isolates in the setting of chlorhexidine bathing without mupirocin. Infect Control Hosp Epidemiol 2016;37:590597.CrossRefGoogle ScholarPubMed
McNeil, JC, Kok, EY, Vallejo, JG, et al. Clinical and molecular features of decreased chlorhexidine susceptibility among nosocomial Staphylococcus aureus isolates at Texas Children’s Hospital. Antimicrob Agents Chemother 2015;60:11211128.CrossRefGoogle ScholarPubMed
McNeil, JC, Hulten, KG, Mason, EO, Kaplan, SL. Impact of health care exposure on genotypic antiseptic tolerance in Staphylococcus aureus infections in a pediatric population. Antimicrob Agents Chemother 2017;61:e0022317. doi: 10.1128/AAC.00223-17.CrossRefGoogle Scholar
Fritz, SA, Hogan, PG, Camins, BC, et al. Mupirocin and chlorhexidine resistance in Staphylococcus aureus in patients with community-onset skin and soft tissue infections. Antimicrob Agents Chemother 2013;57:559568.CrossRefGoogle ScholarPubMed
Johnson, JG, Saye, EJ, Jimenez-Truque, N, et al. Frequency of disinfectant resistance genes in pediatric strains of methicillin-resistant Staphylococcus aureus. Infect Control Hosp Epidemiol 2013;34:13261327.CrossRefGoogle ScholarPubMed
Reich, PJ, Boyle, MG, Hogan, PG, et al. Emergence of community-associated methicillin-resistant Staphylococcus aureus strains in the neonatal intensive care unit: an infection prevention and patient safety challenge. Clin Microbiol Infect 2016;22:645648.CrossRefGoogle ScholarPubMed
Chapman, AK, Aucott, SW, Gilmore, MM, Advani, S, Clarke, W, Milstone, AM. Absorption and tolerability of aqueous chlorhexidine gluconate used for skin antisepsis prior to catheter insertion in preterm neonates. J Perinatol 2013;33:768771.CrossRefGoogle ScholarPubMed
Johnson, J, Bracken, R, Tamma, PD, Aucott, SW, Bearer, C, Milstone, AM. Trends in chlorhexidine use in US neonatal intensive care units: results from a follow-up national survey. Infect Control Hosp Epidemiol 2016;37:11161118.CrossRefGoogle ScholarPubMed
Hijazi, K, Mukhopadhya, I, Abbott, F, et al. Susceptibility to chlorhexidine amongst multidrug-resistant clinical isolates of Staphylococcus epidermidis from bloodstream infections. Int J Antimicrob Agents 2016;48:8690.CrossRefGoogle ScholarPubMed
Bischoff, M, Bauer, J, Preikschat, P, Schwaiger, K, Molle, G, Holzel, C. First detection of the antiseptic resistance gene qacA/B in Enterococcus faecalis. Microb Drug Resist 2012;18:712.CrossRefGoogle ScholarPubMed
Prag, G, Falk-Brynhildsen, K, Jacobsson, S, Hellmark, B, Unemo, M, Soderquist, B. Decreased susceptibility to chlorhexidine and prevalence of disinfectant resistance genes among clinical isolates of Staphylococcus epidermidis. APMIS 2014;122:961967.CrossRefGoogle ScholarPubMed
Lepainteur, M, Royer, G, Bourrel, AS, et al. Prevalence of resistance to antiseptics and mupirocin among invasive coagulase-negative staphylococci from very preterm neonates in NICU: the creeping threat? J Hosp Infect 2013;83:333336.CrossRefGoogle ScholarPubMed
Soma, VL, Qin, X, Zhou, C, Adler, A, Berry, JE, Zerr, DM. The effects of daily chlorhexidine bathing on cutaneous bacterial isolates: a pilot study. Infect Drug Resist 2012;5:7578.CrossRefGoogle ScholarPubMed
Zhang, M, O’Donoghue, MM, Ito, T, Hiramatsu, K, Boost, MV. Prevalence of antiseptic-resistance genes in Staphylococcus aureus and coagulase-negative staphylococci colonising nurses and the general population in Hong Kong. J Hosp Infect 2011;78:113117.CrossRefGoogle ScholarPubMed
Hulten, KG, Kaplan, SL, Gonzalez, BE, et al. Three-year surveillance of community onset health care-associated Staphylococcus aureus infections in children. Pediatr Infect Dis J 2006;25:349353.CrossRefGoogle ScholarPubMed
Wang, SH, Hines, L, van Balen, J, et al. Molecular and clinical characteristics of hospital and community onset methicillin-resistant Staphylococcus aureus strains associated with bloodstream infections. J Clin MIcrobiol 2015;53:15991608.CrossRefGoogle ScholarPubMed
Hulten, KG, Kaplan, SL, Lamberth, LB, et al. Hospital-acquired Staphylococcus aureus infections at Texas Children’s Hospital, 2001–2007. Infect Control Hosp Epidemiol 2010;31:183190.CrossRefGoogle ScholarPubMed
Mermel, LA, Allon, M, Bouza, E, et al. Clinical practice guidelines for the diagnosis and management of intravascular catheter-related infection: 2009 Update by the Infectious Diseases Society of America. Clin Infect Dis 2009;49:145.CrossRefGoogle ScholarPubMed
Zingg, W, Hopkins, S, Gayet-Ageron, A, et al. Health-care-associated infections in neonates, children, and adolescents: an analysis of paediatric data from the European Centre for Disease Prevention and Control point-prevalence survey. Lancet Infect Dis 2017;17:381389.CrossRefGoogle ScholarPubMed
Truong-Bolduc, QC, Villet, RA, Estabrooks, ZA, Hooper, DC. Native efflux pumps contribute resistance to antimicrobials of skin and the ability of Staphylococcus aureus to colonize skin. J Infect Dis 2014;209:14851493.CrossRefGoogle ScholarPubMed
Ding, Y, Onodera, Y, Lee, JC, Hooper, DC. NorB, an efflux pump in Staphylococcus aureus strain MW2, contributes to bacterial fitness in abscesses. J Bacteriol 2008;190:71237129.CrossRefGoogle ScholarPubMed
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Sommer et al. supplementary material

Table S1

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Sommer et al. supplementary material

Table S2

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