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Antibiotics and gastrointestinal colonization by vancomycin-resistant enterococci

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Abstract

Although several classes of antimicrobial agents have been associated with colonization or infection with glycopeptide-resistant enterococci (GRE) in individual clinical studies, the agents most commonly implicated are extended-spectrum cephalosporins and compounds with potent activity against anaerobic bacteria, including ticarcillin–clavulanic acid. In some clinical studies, formulary alterations designed to minimize the use of extended-spectrum cephalosporins or ticarcillin–clavulanic acid have resulted in significant decreases in colonization and infection by GRE. Experimental data using a mouse model of GRE gastrointestinal colonization indicate that persistence of high-level GRE colonization of the mouse gastrointestinal tract is promoted by exposure to agents with potent activity against anaerobic bacteria, suggesting that reduction of competing flora is the major factor leading to persistence of high-level colonization. One study performed in humans is consistent with this model and suggests that high levels of colonization may promote spread of resistant organisms in the nosocomial setting. Establishing colonization with GRE in uncolonized mice correlates with exposure to agents that are (a) secreted into the bile in significant concentrations and (b) have negligible activity against the colonizing enterococcal strain. Differences between piperacillin–tazobactam and ceftriaxone in the establishment model can be attributed directly to differences in their anti-enterococcal activity. Modification of antimicrobial prescribing practices may play an important role in facilitating successful infection control efforts to limit GRE in the nosocomial setting.

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References

  1. Carmeli Y, Eliopoulos G, Mozaffari E, Samore M (2002) Health and economic outcomes of vancomycin-resistant enterococci. Arch Intern Med 162:2223–2328

    Article  PubMed  Google Scholar 

  2. Graffunder EM, Venezia RA (2002) Risk factors associated with nosocomial methicillin-resistant Staphylococcus aureus (MRSA) infection including previous use of antimicrobials. J Antimicrob Chemother 49:999–1005

    Article  PubMed  CAS  Google Scholar 

  3. Harbarth S, Liassine N, Dharan S, Herrault P, Auckenthaler R, Pittet D (2000) Risk factors for persistent carriage of methicillin-resistant Staphylococcus aureus. Clin Infect Dis 31:1380–1385

    Article  PubMed  CAS  Google Scholar 

  4. Weber SG, Gold HS, Hooper DC, Karchmer AW, Carmeli Y (2003) Fluoroquinolones and the risk for methicillin-resistant Staphylococcus aureus in hospitalized patients. Emerg Infect Dis 9:1415–1422

    PubMed  Google Scholar 

  5. Murray BE (1990) The life and times of the enterococcus. Clin Microbiol Rev 3:46–65

    PubMed  CAS  Google Scholar 

  6. Finegold SM, Sutter VL (1978) Fecal flora in different populations, with special reference to diet. Am J Clin Nutr 31:S116–S122

    PubMed  CAS  Google Scholar 

  7. Cooper GS, Shlaes DM, Salata RA (1994) Intraabdominal infection: differences in presentation and outcome between younger patients and the elderly. Clin Infect Dis 19:146–148

    PubMed  CAS  Google Scholar 

  8. Weigelt JA, Easley SM, Thal ER, Palmer LD, Newman VS (1993) Abdominal surgical wound infection is lowered with improved perioperative Enterococcus and Bacteroides therapy. J Trauma 34:579–585

    Article  PubMed  CAS  Google Scholar 

  9. Pallares R, Pujol M, Pena C, Ariza J, Martin R, Gudiol, F (1993) Cephalosporins as a risk factor for nosocomial Enterococcus faecalis bacteremia. Arch Intern Med 153:1581–1586

    Article  PubMed  CAS  Google Scholar 

  10. Hershberger E, Donabedian S, Konstantinou K, Zervos MJ (2004) Quinupristin-dalfopristin resistance in Gram-positive bacteria: mechanism of resistance and epidemiology. Clin Infect Dis 38:92–98

    Article  PubMed  CAS  Google Scholar 

  11. Zervos MJ, Schaberg DR (1985) Reversal of in vitro susceptibility of enterococci to trimethoprim-sulfamethoxazole by folinic acid. Antimicrob Agents Chemother 28:446–448

    PubMed  CAS  Google Scholar 

  12. Singh KV, Murray BE (2005) Differences in the Enterococcus faecalis lsa locus that influence susceptibility to quinupristin–dalfopristin and clindamycin. Antimicrob Agents Chemother 49:32–39

    Article  PubMed  CAS  Google Scholar 

  13. Moellering RC, Weinberg AN (1971) Studies on antibiotic synergism against enterococci: II. Effect of various antibiotics on the uptake of 14C-labelled streptomycin by enterococci. J Clin Invest 50:2580–2584

    PubMed  CAS  Google Scholar 

  14. Williamson R, Calderwood SB, Moellering RCJ, Tomasz A (1983) Studies on the mechanism of intrinsic resistance to β-lactam antibiotic in group D streptococci. J Gen Microbiol 129:813–822

    PubMed  CAS  Google Scholar 

  15. Zervos MJ, Kaufman CA, Therasse PM, Bergmann AG, Mikesell TS, Schaberg DR (1987) Nosocomial infection by gentamicin-resistant Streptococcus faecalis: an epidemiologic study. Ann Intern Med 106:687–691

    PubMed  CAS  Google Scholar 

  16. Rice LB, Bellais S, Carias LL, Hutton-Thomas R, Bonomo RA, Caspers P, Page MG, Gutmann L (2004) Impact of specific pbp5 mutations on expression of beta-lactam resistance in Enterococcus faecium. Antimicrob Agents Chemother 48:3028–3032

    Article  PubMed  CAS  Google Scholar 

  17. (2004) National Nosocomial Infections Surveillance (NNIS) System Report, data summary from January 1992 through June 2004, issued October 2004. Am J Infect Control 32:470–485

  18. Sahm DF, Marsilio MK, Piazza G (1999) Antimicrobial resistance in key bloodstream bacterial isolates: electronic surveillance with the Surveillance Network Database—USA. Clin Infect Dis 29:259–263

    Article  PubMed  CAS  Google Scholar 

  19. Marshall SH, Donskey CJ, Hutton-Thomas R, Salata RA, Rice LB (2002) Gene dosage and linezolid resistance in Enterococcus faecium and Enterococcus faecalis. Antimicrob Agents Chemother 46:3334–3336

    Article  PubMed  CAS  Google Scholar 

  20. Vergis EN, Hayden MK, Chow JW, Snydman DR, Zervos MJ, Linden PK, Wagener MM, Schmitt B, Muder RR (2001) Determinants of vancomycin resistance and mortality rates in enterococcal bacteremia: a prospective multicenter study. Ann Intern Med 135:484–492

    PubMed  CAS  Google Scholar 

  21. Tomich PK, An FY, Clewell DB (1980) Properties of erythromycin-inducible transposon Tn917 in Streptococcus faecalis. J Bacteriol 141:1366–1374

    PubMed  CAS  Google Scholar 

  22. Arthur M, Molinas C, Depardieu F, Courvalin P (1993) Characterization of Tn1546, a Tn3-related transposon conferring glycopeptide resistance by synthesis of depsipeptide peptidoglycan precursors in Enterococcus faecium BM4147. J Bacteriol 175:117–127

    PubMed  CAS  Google Scholar 

  23. Rice LB (1998) Tn916-family conjugative transposons and dissemination of antimicrobial resistance determinants. Antimicrob Agents Chemother 42:1871–1877

    PubMed  CAS  Google Scholar 

  24. Carias LL, Rudin SD, Donskey CJ, Rice LB (1998) Genetic linkage and cotransfer of a novel, vanB-containing transposon (Tn5382) and a low-affinity penicillin-binding protein 5 gene in a clinical vancomycin-resistant Enterococcus faecium isolate. J Bacteriol 180:4426–4434

    PubMed  CAS  Google Scholar 

  25. Hodel-Christian SL, Murray BE (1991) Characterization of the gentamicin resistance transposon Tn5281 from Enterococcus faecalis and comparison to staphylococcal transposons Tn4001 and Tn4031. Antimicrob Agents Chemother 35:1147–1152

    PubMed  CAS  Google Scholar 

  26. Rice LB, Carias LL (1998) Transfer of Tn5385, a composite, multiresistance element from Enterococcus faecalis. J Bacteriol 180:714–721

    PubMed  CAS  Google Scholar 

  27. Clewell DB, Tomich PK, Gawron-Burke MC, Franke AE, Yagi Y, An FY (1982) Mapping of Streptococcus faecalis plasmids pAD1 and pAD2 and studies relating to transposition of Tn917. J Bacteriol 152:1220–1230

    PubMed  CAS  Google Scholar 

  28. Swinfield T-J, Janniere L, Ehrlich SD, Minton NP (1991) Characterization of a region of Enterococcus faecalis plasmid pAMß1 which enhances the segregational stability of pAMß1-derived cloning vectors in Bacillus subtilis. Plasmid 26:209–221

    Article  PubMed  CAS  Google Scholar 

  29. Paulsen IT, Banerjei L, Myers GS, Nelson KE, Seshadri R, Read TD, Fouts DE, Eisen JA, Gill SR, Heidelberg JF, Tettelin H, Dodson RJ, Umayam L, Brinkac L, Beanan M, Daugherty S, DeBoy RT, Durkin S, Kolonay J, Madupu R, Nelson W, Vamathevan J, Tran B, Upton J, Hansen T, Shetty J, Khouri H, Utterback T, Radune D, Ketchum KA, Dougherty BA, Fraser CM (2003) Role of mobile DNA in the evolution of vancomycin-resistant Enterococcus faecalis. Science 299:2071–2074

    Article  PubMed  CAS  Google Scholar 

  30. Rosdahl VT, Knudsen AM (1991) The decline of methicillin resistance among Danish Staphylococcus aureus strains. Infect Control Hosp Epidemiol 12:83–88

    Article  PubMed  CAS  Google Scholar 

  31. Garnier F, Taourit S, Glaser P, Courvalin P, Galimand M (2000) Characterization of transposon Tn1549, conferring VanB-type resistance in Enterococcus spp. Microbiology 146:1481–1489

    PubMed  CAS  Google Scholar 

  32. van der Auwera P, Pensart N, Korten V, Murray BE, Leclercq R (1996) Influence of oral glycopeptides on the fecal flora of human volunteers: selection of highly glycopeptide-resistant enterococci. J Infect Dis 173:1129–1136

    PubMed  Google Scholar 

  33. Klare I, Badstubner D, Konstabel C, Bohme G, Claus H, Witte W (1999) Decreased incidence of VanA-type vancomycin-resistant enterococci isolated from poultry meat and from fecal samples of humans in the community after discontinuation of avoparcin usage in animal husbandry. Microbial Drug Resist 5:45–51

    CAS  Google Scholar 

  34. Manson JM, Smith JM, Cook GM (2004) Persistence of vancomycin-resistant enterococci in New Zealand broilers after discontinuation of avoparcin use. Appl Environ Microbiol 70:5764–5768

    Article  PubMed  CAS  Google Scholar 

  35. Descheemaeker PRM, Chapelle S, Devriese LA, Butaye P, Vandamme P, Goossens H (1999) Comparison of glycopeptide-resistant Enterococcus faecium isolates and glycopeptide resistance genes of human and animal origin. Antimicrob Agents Chemother 43:2032–2037

    PubMed  CAS  Google Scholar 

  36. Hershberger E, Oprea SF, Donabedian SM, Perri M, Bozigar P, Bartlett P, Zervos MJ (2005) Epidemiology of antimicrobial resistance in enterococci of animal origin. J Antimicrob Chemother 55:127–130

    Article  PubMed  CAS  Google Scholar 

  37. Bartlett JG, Chang TW, Gurwith M, Gorbach SL, Onderdonk AB (1978) Antibiotic-associated pseudomembranous colitis due to toxin-producing clostridia. N Engl J Med 298:531–534

    Article  PubMed  CAS  Google Scholar 

  38. Chirurgi VA, Oster SE, Goldberg AA, McCabe RE (1992) Nosocomial acquisition of β-lactamase-negative, ampicillin-resistant enterococcus. Arch Intern Med 152:1457–1461

    Article  PubMed  CAS  Google Scholar 

  39. Impallomeni M, Galletly NP, Wort SJ, Starr JM, Rogers TR (1995) Increased risk of diarrhoea caused by Clostridium difficile in elderly patients receiving cefotaxime. BMJ 311:1345–1346

    PubMed  CAS  Google Scholar 

  40. Willems RJ, Homan W, Top J, van Santen-Verheuvel M, Tribe D, Manzioros X, Gaillard C, Vandenbroucke-Grauls CM, Mascini EM, van Kregten E, van Embden JD, Bonten MJ (2001) Variant esp gene as a marker of a distinct genetic lineage of vancomycin-resistant Enterococcus faecium spreading in hospitals. Lancet 357:853–855

    Article  PubMed  CAS  Google Scholar 

  41. Rice LB, Carias L, Rudin S, Vael C, Goossens H, Konstabel C, Klare I, Nallapareddy SR, Huang W, Murray BE (2003) A potential virulence gene, hylEfm, predominates in Enterococcus faecium of clinical origin. J Infect Dis 187:508–512

    Article  PubMed  CAS  Google Scholar 

  42. Shlaes DM, Gerding DN, John JF Jr, Craig WA, Bornstein DL, Duncan RA, Eckman MR, Farrer WE, Greene WH, Lorian V, Levy S, McGowan JE Jr, Paul SM, Ruskin J, Tenover FC, Watanakunakorn C (1997) Society for Healthcare Epidemiology of America and Infectious Diseases Society of America Joint Committee on the Prevention of Antimicrobial Resistance: guidelines for the prevention of antimicrobial resistance in hospitals. Clin Infect Dis 25:584–599

    Article  PubMed  CAS  Google Scholar 

  43. Currie BP, Lemos-Filho L (2004) Evidence for biliary excretion of vancomycin into stool during intravenous therapy: potential implications for rectal colonization with vancomycin-resistant enterococci. Antimicrob Agents Chemother 48:4427–4429

    Article  PubMed  CAS  Google Scholar 

  44. Chavers LS, Moser SA, Funkhouser E, Benjamin WH Jr, Chavers P, Stamm AM, Waites KB (2003) Association between antecedent intravenous antimicrobial exposure and isolation of vancomycin-resistant enterococci. Microb Drug Resist 9(Suppl 1):S69–S77

    Article  PubMed  CAS  Google Scholar 

  45. Martinez JA, Ruthazer R, Hansjosten K, Barefoot L, Snydman DR (2003) Role of environmental contamination as a risk factor for acquisition of vancomycin-resistant enterococci in patients treated in a medical intensive care unit. Arch Intern Med 163:1905–1912

    Article  PubMed  Google Scholar 

  46. Padiglione AA, Wolfe R, Grabsch EA, Olden D, Pearson S, Franklin C, Spelman D, Mayall B, Johnson PD, Grayson ML (2003) Risk factors for new detection of vancomycin-resistant enterococci in acute-care hospitals that employ strict infection control procedures. Antimicrob Agents Chemother 47:2492–2498

    Article  PubMed  CAS  Google Scholar 

  47. Elizaga ML, Weinstein RA, Hayden MK (2002) Patients in long-term care facilities: a reservoir for vancomycin-resistant enterococci. Clin Infect Dis 34:441–446

    Article  PubMed  Google Scholar 

  48. Fridkin SK, Edwards JR, Courval JM, Hill H, Tenover FC, Lawton R, Gaynes RP, McGowan JE Jr (2001) The effect of vancomycin and third-generation cephalosporins on prevalence of vancomycin-resistant enterococci in 126 U.S. adult intensive care units. Ann Intern Med 135:175–183

    PubMed  CAS  Google Scholar 

  49. Puzniak LA, Mayfield J, Leet T, Kollef M, Mundy LM (2001) Acquisition of vancomycin-resistant enterococci during scheduled antimicrobial rotation in an intensive care unit. Clin Infect Dis 33:151–157

    Article  PubMed  CAS  Google Scholar 

  50. Lautenbach E, LaRosa LA, Marr AM, Nachamkin I, Bilker WB, Fishman NO (2003) Changes in the prevalence of vancomycin-resistant enterococci in response to antimicrobial formulary interventions: impact of progressive restrictions on use of vancomycin and third-generation cephalosporins. Clin Infect Dis 36:440–446

    Article  PubMed  CAS  Google Scholar 

  51. Quale J, Landman D, Atwood E, Kreiswirth B, Willey BM, Ditore V, Zaman M, Patel K, Saurina G, Huang W, Oydna E, Burney S (1996) Experience with a hospital-wide outbreak of vancomycin-resistant enterococci. Am J Infect Control 24:372–379

    Article  PubMed  CAS  Google Scholar 

  52. Bradley SJ, Wilson AL, Allen MC, Sher HA, Goldstone AH, Scott GM (1999) The control of hyperendemic glycopeptide-resistant Enterococcus spp. on a haematology unit by changing antibiotic usage. J Antimicrob Chemother 43:261–266

    Article  PubMed  CAS  Google Scholar 

  53. Winston LG, Charlebois ED, Pang S, Bangsberg DR, Perdreau-Remington F, Chambers HF (2004) Impact of a formulary switch from ticarcillin–clavulanate to piperacillin–tazobactam on colonization with vancomycin-resistant enterococci. Am J Infect Control 32:462–469

    Article  PubMed  Google Scholar 

  54. Taylor EW, Poxon V, Alexander-Williams J, Jackson D (1983) Biliary excretion of piperacillin. J Int Med Res 11:28–31

    PubMed  CAS  Google Scholar 

  55. Hayton WL, Schandlik R, Stoeckel K (1986) Biliary excretion and pharmacokinetics of ceftriaxone after cholecystectomy. Eur J Clin Pharmacol 30:445–451

    Article  PubMed  CAS  Google Scholar 

  56. Whitman MS, Pitsakis PG, DeJesus E, Osborne AJ, Levison ME, Johnson CC (1996) Gastrointestinal tract colonization with vancomycin-resistant Enterococcus faecium in an animal model. Antimicrob Agents Chemother 40:1526–1530

    PubMed  CAS  Google Scholar 

  57. Donskey CJ, Hanrahan JA, Hutton RA, Rice LB (1999) Effect of parenteral antibiotic administration on persistence of vancomycin-resistant Enterococcus faecium in the mouse gastrointestinal tract. J Infect Dis 180:384–390

    Article  PubMed  CAS  Google Scholar 

  58. Donskey CJ, Chowdhry TK, Hecker MT, Hoyen CK, Hanrahan JA, Hujer AM, Hutton-Thomas RA, Whalen CC, Bonomo RA, Rice LB (2000) Effect of antibiotic therapy on the density of vancomycin-resistant enterococci in the stool of colonized patients. N Engl J Med 343:1925–1932

    Article  PubMed  CAS  Google Scholar 

  59. Donskey CJ, Helfand MS, Pultz NJ, Rice LB (2004) Effect of parenteral fluoroquinolone administration on persistence of vancomycin-resistant Enterococcus faecium in the mouse gastrointestinal tract. Antimicrob Agents Chemother 48:326–328

    Article  PubMed  CAS  Google Scholar 

  60. Donskey CJ, Hanrahan JA, Hutton RA, Rice LB (2000) Effect of parenteral antibiotic administration on establishment of colonization with vancomycin-resistant Enterococcus faecium in the mouse gastrointestinal tract. J Infect Dis 181:1830–1833

    Article  PubMed  CAS  Google Scholar 

  61. Rice LB, Hutton-Thomas R, Lakticova V, Helfand MS, Donskey CJ (2004) Beta-lactam antibiotics and gastrointestinal colonization with vancomycin-resistant enterococci. J Infect Dis 189:1113–1118

    Article  PubMed  CAS  Google Scholar 

  62. van Ogtrop ML, Guiot HF, Mattie H, van Furth R (1991) Modulation of the intestinal flora of mice by parenteral treatment with broad-spectrum cephalosporins. Antimicrob Agents Chemother 35:976–982

    PubMed  Google Scholar 

  63. Rice LB, Carias LL, Hutton-Thomas R, Sifaoui F, Gutmann L, Rudin SD (2001) Penicillin-binding protein 5 and expression of ampicillin resistance in Enterococcus faecium. Antimicrob Agents Chemother 45:1480–1486

    Article  PubMed  CAS  Google Scholar 

  64. Rice LB, Lakticova V, Helfand MS, Hutton-Thomas R (2004) In vitro antienterococcal activity explains associations between exposures to antimicrobial agents and risk of colonization by multiresistant enterococci. J Infect Dis 190:2162–2166

    Article  PubMed  CAS  Google Scholar 

  65. D’Agata EM, Gautam S, Green WK, Tang YW (2002) High rate of false-negative results of the rectal swab culture method in detection of gastrointestinal colonization with vancomycin-resistant enterococci. Clin Infect Dis 34:167–172

    Article  PubMed  Google Scholar 

  66. Ballard SA, Grabsch EA, Johnson PD, Grayson ML (2005) Comparison of three PCR primer sets for identification of vanB gene carriage in feces and correlation with carriage of vancomycin-resistant enterococci: interference by vanB-containing anaerobic bacilli. Antimicrob Agents Chemother 49:77–81

    Article  PubMed  CAS  Google Scholar 

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  1. Medical Service 111(W), Louis Stokes Cleveland VA Medical Center and Case Medical School, 10701 East Boulevard, Cleveland, OH 44106, USA

    L. B. Rice

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Rice, L.B. Antibiotics and gastrointestinal colonization by vancomycin-resistant enterococci. Eur J Clin Microbiol Infect Dis 24, 804–814 (2005). https://doi.org/10.1007/s10096-005-0057-z

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