Advanced search
Publication Cover
Expert Review of Anti-infective Therapy Volume 11, 2013 - Issue 3
Submit an article Journal homepage
5,031
Views
916
CrossRef citations to date
0
Altmetric
Review

Clinical relevance of the ESKAPE pathogens

Jack N Pendleton School of Pharmacy, Queen’s University Belfast, Medical Biology Centre, 97 Lisburn Road, Belfast, BT9 7BL, UK
,
Sean P Gorman School of Pharmacy, Queen’s University Belfast, Medical Biology Centre, 97 Lisburn Road, Belfast, BT9 7BL, UK
&
Brendan F Gilmore School of Pharmacy, Queen’s University Belfast, Medical Biology Centre, 97 Lisburn Road, Belfast, BT9 7BL, UK. [email protected]
Pages 297-308 | Published online: 10 Jan 2014

References

  • Rice LB. Federal funding for the study of antimicrobial resistance in nosocomial pathogens: no ESKAPE. J. Infect. Dis. 197(8), 1079–1081 (2008).
  • Boucher HW, Talbot GH, Bradley JS et al. Bad bugs, no drugs: no ESKAPE! An update from the Infectious Diseases Society of America. Clin. Infect. Dis. 48(1), 1–12 (2009).
  • Standing Medical Advisory Committee, Sub-Group on Antimicrobial Resistance. The path of least resistance. (1998).
  • WHO: Department of Communicable Disease Surveillance and Response. WHO Global Strategy for Containment of Antimicrobial Resistance. WHO/CDS/CSR/DRS/2001.2 (2001).
  • European Centre for Disease Prevention and Control/European Medicines Agency. ECDC/EMEA Joint Technical Report. The bacterial challenge: time to react. (2009).
  • European Centre for Disease Prevention and Control. Communication from the Commission to the European Parliament and the Council. Action plan against the rising threats from Antimicrobial Resistance. COM 748 (2011).
  • Infectious Diseases Society of America. Bad Bugs, No Drugs. As Antibiotic Discovery Stagnates. A Public Health Crisis Brews. (2004).
  • Madigan MT, Martinko JM. Bacterial genetics. In: Brock Biology of Microorganisms. Anonymous Pearson Prentice Hall, Pearson Education, Inc. Upper Saddle River, NJ, USA, 07458, 256–298 (2006).
  • Smith A. Bacterial resistance to antibiotics. In: Hugo and Russell’s Pharmaceutical Microbiology. Denyer SP, Hodges NA, Gorman SP (Eds). Blackwell Science Ltd, Oxford, UK, 220–232 (2007).
  • Kumar A, Schweizer HP. Bacterial resistance to antibiotics: active efflux and reduced uptake. Adv. Drug Deliv. Rev. 57(10), 1486–1513 (2005).
  • Nikaido H. Prevention of drug access to bacterial targets: permeability barriers and active efflux. Science 264(5157), 382–388 (1994).
  • Piddock LJV. Clinically relevant chromosomally encoded multidrug resistance efflux pumps in bacteria. Clin. Microbiol. Rev. 19(2), 382–402 (2006).
  • Ruiz J. Mechanisms of resistance to quinolones: target alterations, decreased accumulation and DNA gyrase protection. J. Antimicrob. Chemother. 51(5), 1109–1117 (2003).
  • Strahilevitz J, Jacoby GA, Hooper DC, Robicsek A. Plasmid-mediated quinolone resistance: a multifaceted threat. Clin. Microbiol. Rev. 22(4), 664–689 (2009).
  • Yong D, Toleman MA, Giske CG et al. Characterization of a new metallo-β-lactamase gene, bla(NDM-1), and a novel erythromycin esterase gene carried on a unique genetic structure in Klebsiella pneumoniae sequence type 14 from India. Antimicrob. Agents Chemother. 53(12), 5046–5054 (2009).
  • Queenan AM, Bush K. Carbapenemases: the versatile β-lactamases. Clin. Microbiol. Rev. 20(3), 440–58, table of contents (2007).
  • Wang X, Kim Y, Hong SH et al. Antitoxin MqsA helps mediate the bacterial general stress response. Nat. Chem. Biol. 7(6), 359–366 (2011).
  • Wang X, Wood TK. Toxin-antitoxin systems influence biofilm and persister cell formation and the general stress response. Appl. Environ. Microbiol. 77(16), 5577–5583 (2011).
  • Bhullar K, Waglechner N, Pawlowski A et al. Antibiotic resistance is prevalent in an isolated cave microbiome. PLoS ONE 7(4), e34953 (2012).
  • Khachatourians GG. Agricultural use of antibiotics and the evolution and transfer of antibiotic-resistant bacteria. CMAJ 159(9), 1129–1136 (1998).
  • Ercsey-Ravasz M, Toroczkai Z, Lakner Z, Baranyi J. Complexity of the international agro-food trade network and its impact on food safety. PLoS ONE 7(5), e37810 (2012).
  • Lewis K. Antibiotics: Recover the lost art of drug discovery. Nature 485(7399), 439–440 (2012).
  • Allegranzi B, Bagheri Nejad S, Combescure C et al. Burden of endemic health-care-associated infection in developing countries: systematic review and meta-analysis. Lancet 377(9761), 228–241 (2011).
  • National Audit Office. Healthcare across the UK: a comparison of the NHS in England, Scotland, Wales and Northern Ireland. (2012).
  • Macrae MB, Shannon KP, Rayner DM, Kaiser AM, Hoffman PN, French GL. A simultaneous outbreak on a neonatal unit of two strains of multiply antibiotic resistant Klebsiella pneumoniae controllable only by ward closure. J. Hosp. Infect. 49(3), 183–192 (2001).
  • Fontana C, Favaro M, Minelli S et al. Acinetobacter baumannii in intensive care unit: a novel system to study clonal relationship among the isolates. BMC Infect. Dis. 8, 79 (2008).
  • Brown DF, Hope R, Livermore DM et al.; BSAC Working Parties on Resistance Surveillance. Non-susceptibility trends among enterococci and non-pneumococcal streptococci from bacteraemias in the UK and Ireland, 2001–06. J. Antimicrob. Chemother. 62(Suppl. 2), ii75–ii85 (2008).
  • Hope R, Livermore DM, Brick G, Lillie M, Reynolds R; BSAC Working Parties on Resistance Surveillance. Non-susceptibility trends among staphylococci from bacteraemias in the UK and Ireland, 2001–06. J. Antimicrob. Chemother. 62(Suppl. 2), ii65–ii74 (2008).
  • Livermore DM, Hope R, Brick G, Lillie M, Reynolds R. Non-susceptibility trends among Enterobacteriaceae from bacteraemias in the UK and Ireland, 2001–06. J. Antimicrob. Chemother. 62, ii41–ii54 (2008).
  • Livermore DM, Hope R, Brick G, Lillie M, Reynolds R. Non-susceptibility trends among Pseudomonas aeruginosa and other non-fermentative Gram-negative bacteria from bacteraemias in the UK and Ireland, 2001–06. J. Antimicrob. Chemother. 62, ii55–ii63 (2008).
  • European Centre for Disease Prevention and Control. Annual Epidemiological Report on Communicable Diseases in Europe 2010 (2010).
  • European Centre for Disease Prevention and Control. Annual Epidemiological Report 2011 – Reporting on 2009 surveillance data and 2010 epidemic intelligence data. (2011).
  • Elsner H, Sobottka I, Mack D, Laufs R, Claussen M, Wirth R. Virulence factors of Enterococcus faecalis and Enterococcus faecium blood culture isolates. Eur. J. Clin. Microbiol. Infect. Dis. 19(1), 39–42 (2000).
  • Bonten MJ, Hayden MK, Nathan C et al. Epidemiology of colonisation of patients and environment with vancomycin-resistant enterococci. Lancet 348(9042), 1615–1619 (1996).
  • Uttley AH, Collins CH, Naidoo J, George RC. Vancomycin-resistant enterococci. Lancet 1(8575–6), 57–58 (1988).
  • Shankar N, Baghdayan AS, Gilmore MS. Modulation of virulence within a pathogenicity island in vancomycin-resistant Enterococcus faecalis. Nature 417(6890), 746–750 (2002).
  • Van Wamel WJ, Hendrickx AP, Bonten MJ, Top J, Posthuma G, Willems RJ. Growth condition-dependent Esp expression by Enterococcus faecium affects initial adherence and biofilm formation. Infect. Immun. 75(2), 924–931 (2007).
  • Kluytmans J, van Belkum A, Verbrugh H. Nasal carriage of Staphylococcus aureus: epidemiology, underlying mechanisms, and associated risks. Clin. Microbiol. Rev. 10(3), 505–520 (1997).
  • Marrie TJ, Nelligan J, Costerton JW. A scanning and transmission electron microscopic study of an infected endocardial pacemaker lead. Circulation 66(6), 1339–1341 (1982).
  • Costerton JW, Stewart PS, Greenberg EP. Bacterial biofilms: a common cause of persistent infections. Science 284(5418), 1318–1322 (1999).
  • Boubaker K, Diebold P, Blanc DS et al. Panton–Valentine leukocidin and staphyloccoccal skin infections in schoolchildren. Emerging Infect. Dis. 10(1), 121–124 (2004).
  • Parsonnet J, Hansmann MA, Delaney ML et al. Prevalence of toxic shock syndrome toxin 1-producing Staphylococcus aureus and the presence of antibodies to this superantigen in menstruating women. J. Clin. Microbiol. 43(9), 4628–4634 (2005).
  • Lina G, Piémont Y, Godail-Gamot F et al. Involvement of Panton–Valentine leukocidin-producing Staphylococcus aureus in primary skin infections and pneumonia. Clin. Infect. Dis. 29(5), 1128–1132 (1999).
  • Vandenesch F, Naimi T, Enright MC et al. Community-acquired methicillin-resistant Staphylococcus aureus carrying Panton–Valentine leukocidin genes: worldwide emergence. Emerging Infect. Dis. 9(8), 978–984 (2003).
  • Liu GY, Essex A, Buchanan JT et al. Staphylococcus aureus golden pigment impairs neutrophil killing and promotes virulence through its antioxidant activity. J. Exp. Med. 202(2), 209–215 (2005).
  • Clauditz A, Resch A, Wieland KP, Peschel A, Götz F. Staphyloxanthin plays a role in the fitness of Staphylococcus aureus and its ability to cope with oxidative stress. Infect. Immun. 74(8), 4950–4953 (2006).
  • Chambers HF, Deleo FR. Waves of resistance: Staphylococcus aureus in the antibiotic era. Nat. Rev. Microbiol. 7(9), 629–641 (2009).
  • Appelbaum PC. Reduced glycopeptide susceptibility in methicillin-resistant Staphylococcus aureus (MRSA). Int. J. Antimicrob. Agents 30(5), 398–408 (2007).
  • Podschun R, Ullmann U. Klebsiella spp. as nosocomial pathogens: epidemiology, taxonomy, typing methods, and pathogenicity factors. Clin. Microbiol. Rev. 11(4), 589–603 (1998).
  • Amako K, Meno Y, Takade A. Fine structures of the capsules of Klebsiella pneumoniae and Escherichia coli K1. J. Bacteriol. 170(10), 4960–4962 (1988).
  • Bush K. Alarming β-lactamase-mediated resistance in multidrug-resistant Enterobacteriaceae. Curr. Opin. Microbiol. 13(5), 558–564 (2010).
  • Kumarasamy KK, Toleman MA, Walsh TR et al. Emergence of a new antibiotic resistance mechanism in India, Pakistan, and the UK: a molecular, biological, and epidemiological study. Lancet Infect. Dis. 10(9), 597–602 (2010).
  • Poirel L, Revathi G, Bernabeu S, Nordmann P. Detection of NDM-1-producing Klebsiella pneumoniae in Kenya. Antimicrob. Agents Chemother. 55(2), 934–936 (2011).
  • Poirel L, Al Maskari Z, Al Rashdi F, Bernabeu S, Nordmann P. NDM-1-producing Klebsiella pneumoniae isolated in the Sultanate of Oman. J. Antimicrob. Chemother. 66(2), 304–306 (2011).
  • Brink AJ, Coetzee J, Clay CG et al. Emergence of New Delhi metallo-β-lactamase (NDM-1) and Klebsiella pneumoniae carbapenemase (KPC-2) in South Africa. J. Clin. Microbiol. 50(2), 525–527 (2012).
  • Poirel L, Lagrutta E, Taylor P, Pham J, Nordmann P. Emergence of metallo-β-lactamase NDM-1-producing multidrug-resistant Escherichia coli in Australia. Antimicrob. Agents Chemother. 54(11), 4914–4916 (2010).
  • Solé M, Pitart C, Roca I et al. First description of an Escherichia coli strain producing NDM-1 carbapenemase in Spain. Antimicrob. Agents Chemother. 55(9), 4402–4404 (2011).
  • Pfeifer Y, Witte W, Holfelder M, Busch J, Nordmann P, Poirel L. NDM-1-producing Escherichia coli in Germany. Antimicrob. Agents Chemother. 55(3), 1318–1319 (2011).
  • Kaper JB, Nataro JP, Mobley HL. Pathogenic Escherichia coli. Nat. Rev. Microbiol. 2(2), 123–140 (2004).
  • Kochar S, Sheard T, Sharma R et al. Success of an infection control program to reduce the spread of carbapenem-resistant Klebsiella pneumoniae. Infect. Control Hosp. Epidemiol. 30(5), 447–452 (2009).
  • Schwaber MJ, Carmeli Y. Mortality and delay in effective therapy associated with extended-spectrum β-lactamase production in Enterobacteriaceae bacteraemia: a systematic review and meta-analysis. J. Antimicrob. Chemother. 60(5), 913–920 (2007).
  • Biendo M, Laurans G, Lefebvre JF, Daoudi F, Eb F. Epidemiological study of an Acinetobacter baumannii outbreak by using a combination of antibiotyping and ribotyping. J. Clin. Microbiol. 37(7), 2170–2175 (1999).
  • Vila J, Martí S, Sánchez-Céspedes J. Porins, efflux pumps and multidrug resistance in Acinetobacter baumannii. J. Antimicrob. Chemother. 59(6), 1210–1215 (2007).
  • Kramer A, Schwebke I, Kampf G. How long do nosocomial pathogens persist on inanimate surfaces? A systematic review. BMC Infect. Dis. 6, 130 (2006).
  • Houang ET, Sormunen RT, Lai L, Chan CY, Leong AS. Effect of desiccation on the ultrastructural appearances of Acinetobacter baumannii and Acinetobacter lwoffii. J. Clin. Pathol. 51(10), 786–788 (1998).
  • Choi CH, Lee EY, Lee YC et al. Outer membrane protein 38 of Acinetobacter baumannii localizes to the mitochondria and induces apoptosis of epithelial cells. Cell. Microbiol. 7(8), 1127–1138 (2005).
  • Adair FW, Geftic SG, Gelzer J. Resistance of Pseudomonas to quaternary ammonium compounds. I. Growth in benzalkonium chloride solution. Appl. Microbiol. 18(3), 299–302 (1969).
  • Nikaido H. Molecular basis of bacterial outer membrane permeability revisited. Microbiol. Mol. Biol. Rev. 67(4), 593–656 (2003).
  • Livermore DM. Multiple mechanisms of antimicrobial resistance in Pseudomonas aeruginosa: our worst nightmare? Clin. Infect. Dis. 34(5), 634–640 (2002).
  • Morero NR, Monti MR, Argaraña CE. Effect of ciprofloxacin concentration on the frequency and nature of resistant mutants selected from Pseudomonas aeruginosa mutS and mutT hypermutators. Antimicrob. Agents Chemother. 55(8), 3668–3676 (2011).
  • Castanheira M, Deshpande LM, Mathai D, Bell JM, Jones RN, Mendes RE. Early dissemination of NDM-1- and OXA-181-producing Enterobacteriaceae in Indian hospitals: report from the SENTRY Antimicrobial Surveillance Program, 2006–2007. Antimicrob. Agents Chemother. 55(3), 1274–1278 (2011).
  • Dellit TH, Owens RC, McGowan JE Jr et al.; Infectious Diseases Society of America; Society for Healthcare Epidemiology of America. Infectious Diseases Society of America and the Society for Healthcare Epidemiology of America guidelines for developing an institutional program to enhance antimicrobial stewardship. Clin. Infect. Dis. 44(2), 159–177 (2007).
  • Department of Health Advisory Committee on Antimicrobial Resistance and Healthcare Associated Infection (ARHAI). Antimicrobial Stewardship: ‘Start Smart – Then Focus’ (2011).
  • Stone SP, Fuller C, Savage J et al. Evaluation of the national Cleanyourhands campaign to reduce Staphylococcus aureus bacteraemia and Clostridium difficile infection in hospitals in England and Wales by improved hand hygiene: four year, prospective, ecological, interrupted time series study. BMJ 344, e3005 (2012).
  • Innovative Medicines Initiative. 6th Call for proposals 2012 – Version 1.3. IMI-GB-DEC-2012-12 (2012).
  • Cathcart GR, Quinn D, Greer B et al. Novel inhibitors of the Pseudomonas aeruginosa virulence factor LasB: a potential therapeutic approach for the attenuation of virulence mechanisms in pseudomonal infection. Antimicrob. Agents Chemother. 55(6), 2670–2678 (2011).
  • Infectious Diseases Society of America. The 10 × ‘20 initiative: pursuing a global commitment to develop 10 new antibacterial drugs by 2020. Clin. Infect. Dis. 50(8), 1081–1083 (2010).
  • Swaney SM, Aoki H, Ganoza MC, Shinabarger DL. The oxazolidinone linezolid inhibits initiation of protein synthesis in bacteria. Antimicrob. Agents Chemother. 42(12), 3251–3255 (1998).
  • Thorne GM, Alder J. Daptomycin: a novel lipopeptide antibiotic. Clin. Microbiol. Newslett. 24(5), 33–40 (2002).
  • Peterson LR. A review of tigecycline – the first glycylcycline. Int. J. Antimicrob. Agents 32(Suppl. 4), S215–S222 (2008).
  • Butler MS, Cooper MA. Antibiotics in the clinical pipeline in 2011. J. Antibiot. 64(6), 413–425 (2011).
  • Tsiodras S, Gold HS, Sakoulas G et al. Linezolid resistance in a clinical isolate of Staphylococcus aureus. Lancet 358(9277), 207–208 (2001).
  • Wilson P, Andrews JA, Charlesworth R et al. Linezolid resistance in clinical isolates of Staphylococcus aureus. J. Antimicrob. Chemother. 51(1), 186–188 (2003).
  • Hayden MK, Rezai K, Hayes RA, Lolans K, Quinn JP, Weinstein RA. Development of daptomycin resistance in vivo in methicillin-resistant Staphylococcus aureus. J. Clin. Microbiol. 43(10), 5285–5287 (2005).
  • Mangili A, Bica I, Snydman DR, Hamer DH. Daptomycin-resistant, methicillin-resistant Staphylococcus aureus bacteremia. Clin. Infect. Dis. 40(7), 1058–1060 (2005).
  • Navon-Venezia S, Leavitt A, Carmeli Y. High tigecycline resistance in multidrug-resistant Acinetobacter baumannii. J. Antimicrob. Chemother. 59(4), 772–774 (2007).
  • Fenical W, Jensen PR. Developing a new resource for drug discovery: marine actinomycete bacteria. Nat. Chem. Biol. 2(12), 666–673 (2006).
  • Laport MS, Santos OC, Muricy G. Marine sponges: potential sources of new antimicrobial drugs. Curr. Pharm. Biotechnol. 10(1), 86–105 (2009).
  • Burgess JG, Jordan EM, Bregu M, Mearns-Spragg A, Boyd KG. Microbial antagonism: a neglected avenue of natural products research. J. Biotechnol. 70(1–3), 27–32 (1999).
  • Falagas ME, Kasiakou SK. Colistin: the revival of polymyxins for the management of multidrug-resistant Gram-negative bacterial infections. Clin. Infect. Dis. 40(9), 1333–1341 (2005).
  • Li J, Nation RL, Turnidge JD et al. Colistin: the re-emerging antibiotic for multidrug-resistant Gram-negative bacterial infections. Lancet Infect. Dis. 6(9), 589–601 (2006).
  • Falagas ME, Kastoris AC, Kapaskelis AM, Karageorgopoulos DE. Fosfomycin for the treatment of multidrug-resistant, including extended-spectrum β-lactamase producing, Enterobacteriaceae infections: a systematic review. Lancet Infect. Dis. 10(1), 43–50 (2010).
  • Hall-Stoodley L, Costerton JW, Stoodley P. Bacterial biofilms: from the natural environment to infectious diseases. Nat. Rev. Microbiol. 2(2), 95–108 (2004).
  • Andrews JM. Determination of minimum inhibitory concentrations. J. Antimicrob. Chemother. 48(Suppl. 1), 5–16 (2001).
  • Clinical and Laboratory Standards Institute. Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically; approved standard – seventh edition (M7-A7) (2006).
  • Clinical and Laboratory Standards Institute. Methods for dilution antimicrobial susceptibility testing of anaerobic bacteria; approved standard – seventh edition (M11-A7). (2007).
  • Costerton JW. Introduction to biofilm. Int. J. Antimicrob. Agents 11(3–4), 217–221; discussion 237 (1999).
  • Davies D. Understanding biofilm resistance to antibacterial agents. Nat. Rev. Drug Discov. 2(2), 114–122 (2003).
  • Ceri H, Olson ME, Turner RJ. Needed, new paradigms in antibiotic development. Expert Opin. Pharmacother. 11(8), 1233–1237 (2010).
  • Lyczak JB, Cannon CL, Pier GB. Lung infections associated with cystic fibrosis. Clin. Microbiol. Rev. 15(2), 194–222 (2002).
  • Parsek MR, Singh PK. Bacterial biofilms: an emerging link to disease pathogenesis. Annu. Rev. Microbiol. 57, 677–701 (2003).
  • Widmer AF, Frei R, Rajacic Z, Zimmerli W. Correlation between in vivo and in vitro efficacy of antimicrobial agents against foreign body infections. J. Infect. Dis. 162(1), 96–102 (1990).
  • Monzón M, Oteiza C, Leiva J, Amorena B. Synergy of different antibiotic combinations in biofilms of Staphylococcus epidermidis. J. Antimicrob. Chemother. 48(6), 793–801 (2001).
  • National Institute for Health and Clinical Excellence. NICE public health guidance 36 – prevention and control of healthcare-associated infections. PH36 (2011).
  • Moir DT, Opperman TJ, Butler MM, Bowlin TL. New classes of antibiotics. Curr. Opin. Pharmacol. 12(5), 535–544 (2012).

Websites

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Order Reprints Request Corporate Permissions

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

Request Academic Permissions

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.

Related research

People also read lists articles that other readers of this article have read.

Recommended articles lists articles that we recommend and is powered by our AI driven recommendation engine.

Cited by lists all citing articles based on Crossref citations.
Articles with the Crossref icon will open in a new tab.