Current Infectious Disease Reports

, Volume 15, Issue 6, pp 504–513

Multidrug-Resistant Bacteria in Organ Transplantation: An Emerging Threat with Limited Therapeutic Options

Transplant and Oncology (M Ison and N Theodoropoulos, Section Editors)

Abstract

Multidrug-resistant organisms (MDROs) are an emerging threat in solid organ transplantation (SOT). The changing epidemiology of these MDROs is reviewed along with the growing evidence regarding risk factors and outcomes associated with both colonization and infection in SOT. The management of these infections is complicated by the lack of antimicrobial agents available to treat these infections, and only a handful of new agents, especially for the treatment of MDR GNR infections, are being evaluated in clinical trials. Due to the increased prevalence of MDROs and limited treatment options, as well as organ shortages, transplant candidacy and use of organs from donors with evidence of MDRO colonization and/or infection remain controversial. Increasing collaboration between transplant programs, individual practitioners, infection control programs, and researchers in antimicrobial development will be needed to face this challenge.

Keywords

MRSA VRE CRE KPC Acinetobacter baumannii Pseudomonas aeruginosa Burkholderia 

References

Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance

  1. 1.
    •• Boucher HW, Talbot GH, Benjamin DK, et al. 10 × ′20 progress-- development of new drugs active against gram-negative bacilli: an update from the infectious diseases society of America. Clin Infect Dis. 2013;56(12):1685–94. An upate from the Infectious Diseases Society of America on drugs in development for the treatment of multidrug-resistant Gram-negative infections.CrossRefPubMedGoogle Scholar
  2. 2.
    Patel G, Snydman DR. Vancomycin-resistant Enterococcus infections in solid organ transplantation. Am J Transplant. 2013;13(s4):59–67.CrossRefPubMedGoogle Scholar
  3. 3.
    van Duin D, van Delden C. Multidrug-resistant gram-negative bacteria infections in solid organ transplantation. Am J Transplant. 2013;13(S4):31–41.CrossRefPubMedGoogle Scholar
  4. 4.
    Garzoni C, Vergidis P. Methicillin-resistant, vancomycin-intermediate and vancomycin-resistant Staphylococcus aureus infections in solid organ transplantation. Am J Transplant. 2013;13(S4):50–8.CrossRefPubMedGoogle Scholar
  5. 5.
    •• Magiorakos AP, Srinivasan A, Carey RB, et al. 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):268–81. An international consensus statement regarding standardization of defenitions of multidrug resistance.CrossRefPubMedGoogle Scholar
  6. 6.
    Gupta N, Limbago BM, Patel JB, Kallen AJ. Carbapenem-resistant Enterobacteriaceae: epidemiology and prevention. Clin Infect Dis. 2011;53(1):60–7.CrossRefPubMedGoogle Scholar
  7. 7.
    •• Jacob JT, Klein E, Laxminarayan R, Beldavs Z , Lynfield R, Kallen AJ et al. Vital signs: carbapenem-resistant Enterobacteriaceae. MMWR Morb Mortal Wkly Rep. 2013; 62(9):165-70. An update regarding the prevalence of carbapenem-resistant Enterobacteriaceae in health-care institutions in the U.S. Google Scholar
  8. 8.
    • Patel G, Bonomo RA. “Stormy waters ahead”: global emergence of carbapenemases. Front Microbiol. 2013. doi: 10.3389/fmicb.2013.00048. A review of mechanisms of carbapenem resistance among Gram-negative bacilli.
  9. 9.
    •• Mathers AJ, Hazen KC, Carroll J, et al. First clinical cases of OXA-48-producing carbapenem-resistant Klebsiella pneumoniae in the United States: the “menace” arrives in the new world. J Clin Microbiol. 2013;51(2):680–3. The first case report(s) of carbapenem resistance mediated by OXA-48 in a transplant center in the U.S.CrossRefPubMedGoogle Scholar
  10. 10.
    Nguyen M, Eschenauer GA, Bryan M, et al. Carbapenem-resistant Klebsiella pneumoniae bacteremia: factors correlated with clinical and microbiologic outcomes. Diagn Microbiol Infect Dis. 2010;67(2):180–4.CrossRefPubMedGoogle Scholar
  11. 11.
    Patel G, Huprikar S, Factor SH, Jenkins SG, Calfee DP. Outcomes of carbapenem-resistant Klebsiella pneumoniae infection and the impact of antimicrobial and adjunctive therapies. Infect Control Hosp Epidemiol. 2008;29(12):1099–106.CrossRefPubMedGoogle Scholar
  12. 12.
    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. 2010;10(9):597–602.CrossRefPubMedGoogle Scholar
  13. 13.
    Mathers AJ, Cox HL, Kitchel B, et al. Molecular dissection of an outbreak of carbapenem-resistant enterobacteriaceae reveals Intergenus KPC carbapenemase transmission through a promiscuous plasmid. MBio. 2011;2(6):e00204–11.CrossRefPubMedGoogle Scholar
  14. 14.
    Patel G, Perez F, Bonomo RA. Carbapenem-resistant Enterobacteriaceae and Acinetobacter baumannii: assessing their impact on organ transplantation. Curr Opin Organ Transplant. 2010;15:676–82.CrossRefGoogle Scholar
  15. 15.
    Snitkin ES, Zelazny AM, Thomas PJ, et al. Tracking a hospital outbreak of carbapenem-resistant Klebsiella pneumoniae with whole-genome sequencing. Sci Transl Med. 2012;4(148), 148ra116.CrossRefPubMedGoogle Scholar
  16. 16.
    Rana MM, Sturdevant M, Patel G, Huprikar S. Klebsiella necrotizing soft tissue infections in liver transplant recipients: a case series. Transpl Infect Dis. 2013. doi:10.1111/tid.12103.PubMedGoogle Scholar
  17. 17.
    • Kalpoe JS, Sonnenberg E, Factor SH, et al. Mortality associated with carbapenem-resistant Klebsiella pneumoniae infections in liver transplant recipients. Liver Transpl. 2012;18(4):468–74. An evaluation of the effects of carbapenem-resistant K. pneumoniae in liver transplantation.CrossRefPubMedGoogle Scholar
  18. 18.
    Hirsch EB, Ledesma KR, Chang KT, et al. In vitro activity of MK-7655, a novel beta-lactamase inhibitor, in combination with imipenem against carbapenem-resistant Gram-negative bacteria. Antimicrob Agents Chemother. 2012;56(7):3753–7.CrossRefPubMedGoogle Scholar
  19. 19.
    Lee GC, Burgess DS. Treatment of Klebsiella pneumoniae carbapenemase (KPC) infections: a review of published case series and case reports. Ann Clin Microbiol Antimicrob. 2012;11(32):97–100.Google Scholar
  20. 20.
    Livermore DM, Mushtaq S, Warner M, et al. Activities of NXL104 combinations with ceftazidime and aztreonam against carbapenemase-producing enterobacteriaceae. Antimicrob Agents Chemother. 2011;55(1):390–4.CrossRefPubMedGoogle Scholar
  21. 21.
    Mushtaq S, Warner M, Williams G, Critchley I, Livermore DM. Activity of chequerboard combinations of ceftaroline and NXL104 versus β-lactamase-producing Enterobacteriaceae. J Antimicrob Chemother. 2010;65(7):1428–32.CrossRefPubMedGoogle Scholar
  22. 22.
    Aktas Z, Kayacan C, Oncul O. In vitro activity of avibactam (NXL104) in combination with beta-lactams against Gram-negative bacteria, including OXA-48 beta-lactamase-producing Klebsiella pneumoniae. Int J Antimicrob Agents. 2012;39(1):86–9.CrossRefPubMedGoogle Scholar
  23. 23.
    Aggen JB, Armstrong ES, Goldblum AA, et al. Synthesis and Spectrum of the Neoglycoside ACHN-490. Antimicrob Agents Chemother. 2010;54(11):4636–42.CrossRefPubMedGoogle Scholar
  24. 24.
    Endimiani A, Hujer KM, Hujer AM, et al. ACHN-490, a Neoglycoside with Potent In Vitro Activity against Multidrug-Resistant Klebsiella pneumoniae Isolates. Antimicrob Agents Chemother. 2009;53(10):4504–7.PubMedGoogle Scholar
  25. 25.
    Landman D, Kelly P, Bäcker M, et al. Antimicrobial activity of a novel aminoglycoside, ACHN-490, against Acinetobacter baumannii and Pseudomonas aeruginosa from New York City. J Antimicrob Chemother. 2011;66(2):332–4.CrossRefPubMedGoogle Scholar
  26. 26.
    Livermore DM, Mushtaq S, Warner M, Zhang J-C, Maharjan S, Doumith M, et al. Activity of aminoglycosides, including ACHN-490, against carbapenem-resistant Enterobacteriaceae isolates. J Antimicrob Chemother. 2011;66(1):48–53.CrossRefPubMedGoogle Scholar
  27. 27.
    Sutcliffe JA. Antibiotics in development targeting protein synthesis. Ann N Y Acad Sci. 2011;1241(1):122–52.CrossRefPubMedGoogle Scholar
  28. 28.
    Shi SH, Kong HS, Xu J, et al. Multidrug resistant gram-negative bacilli as predominant bacteremic pathogens in liver transplant recipients. Transpl Infect Dis. 2009;11(5):405–12.CrossRefPubMedGoogle Scholar
  29. 29.
    Nunley DR, Bauldoff GS, Mangino JE, Pope-Harman AL. Mortality associated with Acinetobacter baumannii infections experienced by lung transplant recipients. Lung. 2010;188(5):381–5.CrossRefPubMedGoogle Scholar
  30. 30.
    • Shields RK, Clancy CJ, Gillis LM, et al. Epidemiology, clinical characteristics and outcomes of extensively drug-resistant acinetobacter baumannii infections among solid organ transplant recipients. PLoS ONE. 2012;7(12):e52349. doi:10.1371/journal.pone.0052349. A multiyear restrospective review of solid organ transplant recipients with extensively drug-resistant Acinetobacter baumannii infections, with an assessment of outcomes and possible increased survival with the use of carbapenem–colistin combination therapy.CrossRefPubMedGoogle Scholar
  31. 31.
    de Gouvea EF, Martins IS, Halpern M, et al. The influence of carbapenem resistance on mortality in solid organ transplant recipients with Acinetobacter baumannii infection. BMC Infect Dis. 2012. doi: 10.1186/1471-2334-12-351.
  32. 32.
    Kim YJ, Yoon JH, Kim SI, et al. High mortality associated with Acinetobacter species infection in liver transplant patients. Transplant Proc. 2011;43(6):2397–9.CrossRefPubMedGoogle Scholar
  33. 33.
    Hsieh CE, Chen YL, Lin PY, et al. Liver transplantation in patients infected with gram-negative bacteria: non-Acinetobacter baumannii and Acinetobacter baumannii. Transplant Proc. 2013;45(1):225–30.CrossRefPubMedGoogle Scholar
  34. 34.
    Shields RK, Kwak EJ, Potoski BA, et al. High mortality rates among solid organ transplant recipients infected with extensively drug-resistant Acinetobacter baumannii: using in vitro antibiotic combination testing to identify the combination of a carbapenem and colistin as an effective treatment regimen. Diagn Microbiol Infect Dis. 2011;70(2):246–52.CrossRefPubMedGoogle Scholar
  35. 35.
    Perez F, Endimiani A, Bonomo RA. Why are we afraid of Acinetobacter baumannii? Expert Rev Anti-Infect Ther. 2008;6(3):269–71.CrossRefPubMedGoogle Scholar
  36. 36.
    Perez F, Hujer AM, Hujer KM, Decker BK, Rather PN, Bonomo RA. Global challenge of multidrug-resistant Acinetobacter baumannii. Antimicrob Agents Chemother. 2007;51(10):3471–84.CrossRefPubMedGoogle Scholar
  37. 37.
    Mushtaq S, Warner M, Livermore DM. In vitro activity of ceftazidime + NXL104 against Pseudomonas aeruginosa and other non-fermenters. J Antimicrob Chemother. 2010;65(11):2376–81.CrossRefPubMedGoogle Scholar
  38. 38.
    Aggen JB, Armstrong ES, Goldblum AA, et al. Synthesis and spectrum of the neoglycoside ACHN-490. Antimicrob Agents Chemother. 2010;54(11):4636–42.CrossRefPubMedGoogle Scholar
  39. 39.
    Johnson LE, D'Agata EM, Paterson DL, et al. Pseudomonas aeruginosa bacteremia over a 10-year period: multidrug resistance and outcomes in transplant recipients. Transpl Infect Dis. 2009;11(3):227–34.CrossRefPubMedGoogle Scholar
  40. 40.
    Iida T, Kaido T, Yagi S, et al. Posttransplant bacteremia in adult living donor liver transplant recipients. Liver Transpl. 2010;16(12):1379–85.CrossRefPubMedGoogle Scholar
  41. 41.
    Shi SH, Kong HS, Jia CK, et al. Risk factors for pneumonia caused by multidrug-resistant Gram-negative bacilli among liver recipients. Clin Transplant. 2010;24(6):758–65.CrossRefPubMedGoogle Scholar
  42. 42.
    Linares L, Garcia-Goez JF, Cervera C, et al. Early bacteremia after solid organ transplantation. Transplant Proc. 2009;41(6):2262–4.CrossRefPubMedGoogle Scholar
  43. 43.
    Aris RM, Gilligan PH, Neuringer IP, et al. The effects of panresistant bacteria in cystic fibrosis patients on lung transplant outcome. Am J Respir Crit Care Med. 1997;155(5):1699–704.CrossRefPubMedGoogle Scholar
  44. 44.
    Dobbin C, Maley M, Harkness J, et al. The impact of pan-resistant bacterial pathogens on survival after lung transplantation in cystic fibrosis: results from a single large referral centre. J Hosp Infect. 2004;56(4):277–82.CrossRefPubMedGoogle Scholar
  45. 45.
    Hadjiliadis D, Steele MP, Chaparro C, et al. Survival of lung transplant patients with cystic fibrosis harboring panresistant bacteria other than Burkholderia cepacia, compared with patients harboring sensitive bacteria. J Heart Lung Transplant. 2007;26(8):834–8.CrossRefPubMedGoogle Scholar
  46. 46.
    Hammami S, Boutiba-Ben Boubaker I, Ghozzi R, et al. Nosocomial outbreak of imipenem-resistant Pseudomonas aeruginosa producing VIM-2 metallo-beta-lactamase in a kidney transplantation unit. Diagn Pathol. 2011. doi: 10.1186/1746-1596-6-106.
  47. 47.
    Poole K. Pseudomonas aeruginosa: resistance to the max. Front Microbiol. 2011. doi: 10.3389/fmicb.2011.00065.
  48. 48.
    •• Tamma PD, Cosgrove SE, Maragakis LL. Combination therapy for treatment of infections with gram-negative bacteria. Clin Microbiol Rev. 2012;25(3):450–70. A contemporary evidence-based review on the use of combination therapy in the treatment of Gram-negative infections.CrossRefPubMedGoogle Scholar
  49. 49.
    Sun HY, Shields RK, Cacciarelli TV, Muder RR, Singh N. A novel combination regimen for the treatment of refractory bacteremia due to multidrug-resistant Pseudomonas aeruginosa in a liver transplant recipient. Transpl Infect Dis. 2010;12(6):555–60.CrossRefPubMedGoogle Scholar
  50. 50.
    Bergen PJ, Tsuji BT, Bulitta JB, et al. Synergistic killing of multidrug-resistant Pseudomonas aeruginosa at multiple inocula by colistin combined with doripenem in an in vitro pharmacokinetic/pharmacodynamic model. Antimicrob Agents Chemother. 2011;55(12):5685–95.CrossRefPubMedGoogle Scholar
  51. 51.
    Florescu DF, Grant W, Botha JF, Fey P, Kalil AC. Should multivisceral transplantation be considered in patients colonized with multidrug-resistant Pseudomonas aeruginosa? Microb Drug Resist. 2012;18(1):74–8.CrossRefPubMedGoogle Scholar
  52. 52.
    Levasseur P, Girard AM, Claudon M, et al. In vitro antibacterial activity of the ceftazidime-avibactam (NXL104) combination against Pseudomonas aeruginosa clinical isolates. Antimicrob Agents Chemother. 2012;56(3):1606–8.CrossRefPubMedGoogle Scholar
  53. 53.
    Juan C, Zamorano L, Perez JL, Ge Y, Oliver A. Activity of a new antipseudomonal cephalosporin, CXA-101 (FR264205), against carbapenem-resistant and multidrug-resistant Pseudomonas aeruginosa clinical strains. Antimicrob Agents Chemother. 2010;54(2):846–51.CrossRefPubMedGoogle Scholar
  54. 54.
    Sader HS, Rhomberg PR, Farrell DJ, Jones RN. Antimicrobial activity of CXA-101, a novel cephalosporin tested in combination with tazobactam against Enterobacteriaceae, Pseudomonas aeruginosa, and Bacteroides fragilis strains having various resistance phenotypes. Antimicrob Agents Chemother. 2011;55(5):2390–4.CrossRefPubMedGoogle Scholar
  55. 55.
    De Soyza A, Corris PA. Lung transplantation and the Burkholderia cepacia complex. J Heart Lung Transplant. 2003;22(9):954–8.CrossRefPubMedGoogle Scholar
  56. 56.
    De Soyza A, Meachery G, Hester KL, et al. Lung transplantation for patients with cystic fibrosis and Burkholderia cepacia complex infection: a single-center experience. J Heart Lung Transplant. 2010;29(12):1395–404.CrossRefPubMedGoogle Scholar
  57. 57.
    Boussaud V, Guillemain R, Grenet D, et al. Clinical outcome following lung transplantation in patients with cystic fibrosis colonised with Burkholderia cepacia complex: results from two French centres. Thorax. 2008;63(8):732–7.CrossRefPubMedGoogle Scholar
  58. 58.
    Alexander BD, Petzold EW, Reller LB, et al. Survival after lung transplantation of cystic fibrosis patients infected with Burkholderia cepacia complex. Am J Transplant. 2008;8(5):1025–30.CrossRefPubMedGoogle Scholar
  59. 59.
    Kennedy MP, Coakley RD, Donaldson SH, et al. Burkholderia gladioli: five year experience in a cystic fibrosis and lung transplantation center. J Cyst Fibros. 2007;6(4):267–73.CrossRefPubMedGoogle Scholar
  60. 60.
    Murray S, Charbeneau J, Marshall BC, LiPuma JJ. Impact of Burkholderia infection on lung transplantation in cystic fibrosis. Am J Respir Crit Care Med. 2008;178(4):363–71.CrossRefPubMedGoogle Scholar
  61. 61.
    Horsley A, Jones AM. Antibiotic treatment for Burkholderia cepacia complex in people with cystic fibrosis experiencing a pulmonary exacerbation. Cochrane Database Syst Rev. 2012. doi: 10.1002/14651858.CD009529.pub2.
  62. 62.
    Sievert DM, Ricks P, Edwards JR, et al. Antimicrobial-resistant pathogens associated with healthcare-associated infections: summary of data reported to the National Healthcare Safety Network at the Centers for Disease Control and Prevention, 2009-2010. Infect Control Hosp Epidemiol. 2013;34(1):1–14.CrossRefPubMedGoogle Scholar
  63. 63.
    Singh N, Paterson DL, Chang FY, Gayowski T, Squier C, Wagener MM, et al. Methicillin-resistant Staphylococcus aureus: the other emerging resistant gram-positive coccus among liver transplant recipients. Clin Infect Dis. 2000;30(2):322–7.CrossRefPubMedGoogle Scholar
  64. 64.
    Florescu DF, McCartney AM, Qiu F, Langnas AN, Botha J, Mercer DF, et al. Staphylococcus aureus infections after liver transplantation. Infection. 2012;40(3):263–9.CrossRefPubMedGoogle Scholar
  65. 65.
    Schneider CR, Buell JF, Gearhart M, Thomas M, Hanaway MJ, Rudich SM, et al. Methicillin-resistant Staphylococcus aureus infection in liver transplantation: a matched controlled study. Transplant Proc. 2005;37(2):1243–4.CrossRefPubMedGoogle Scholar
  66. 66.
    Desai D, Desai N, Nightingale P, Elliott T, Neuberger J. Carriage of methicillin-resistant Staphylococcus aureus is associated with an increased risk of infection after liver transplantation. Liver Transpl. 2003;9(7):754–9.CrossRefPubMedGoogle Scholar
  67. 67.
    Russell DL, Flood A, Zaroda TE, et al. Outcomes of colonization with MRSA and VRE among liver transplant candidates and recipients. Am J Transplant. 2008;8(8):1737–43.CrossRefPubMedGoogle Scholar
  68. 68.
    Manuel O, Lien D, Weinkauf J, Humar A, Cobos I, Kumar D. Methicillin-resistant Staphylococcus aureus infection after lung transplantation: 5-year review of clinical and molecular epidemiology. J Heart Lung Transplant. 2009;28(11):1231–6.CrossRefPubMedGoogle Scholar
  69. 69.
    Shields RK, Clancy CJ, Minces LR, et al. Staphylococcus aureus infections in the early period after lung transplantation: epidemiology, risk factors, and outcomes. J Heart Lung Transplant. 2012;31(11):1199–206.CrossRefPubMedGoogle Scholar
  70. 70.
    • van Hal SJ, Lodise TP, Paterson DL. The clinical significance of vancomycin minimum inhibitory concentration in Staphylococcus aureus infections: a systematic review and meta-analysis. Clin Infect Dis. 2012;54(6):755–71. A large meta-analysis examining the significance of higher vancomycin minimum inhibitory concentrations and clinical outcomes.CrossRefPubMedGoogle Scholar
  71. 71.
    van Hal SJ, Fowler Jr VG. Is it time to replace vancomycin in the treatment of methicillin-resistant Staphylococcus aureus infections? Clin Infect Dis. 2013;56(12):1779–88.CrossRefPubMedGoogle Scholar
  72. 72.
    Levy DT, Steed ME, Rybak MJ, et al. Successful treatment of a left ventricular assist device infection with daptomycin non-susceptible methicillin-resistant Staphylococcus aureus: case report and review of the literature. Transpl Infect Dis. 2012;14(5):E89–96.CrossRefPubMedGoogle Scholar
  73. 73.
    Swartz T, Huprikar S, LaBombardi V, et al. Heart transplantation in a patient with heteroresistant vancomycin-intermediate Staphylococcus aureus ventricular assist device mediastinitis and bacteremia. Transpl Infect Dis. 2013. doi: 10.1111/tid.12123.
  74. 74.
    • Wunderink RG, Niederman MS, Kollef MH, et al. Linezolid in methicillin-resistant Staphylococcus aureus nosocomial pneumonia: a randomized, controlled study. Clin Infect Dis. 2012;54(5):621–9. A randominzed controlled tiral evaluating linezolid versus vancomycin in the treatment of nosocomial pneumonia, with a specific emphasis on pneumonia due to methicillin-resistant Staphylococcus aureus.CrossRefPubMedGoogle Scholar
  75. 75.
    Bert F, Clarissou J, Durand F, et al. Prevalence, molecular epidemiology, and clinical significance of heterogeneous glycopeptide-intermediate Staphylococcus aureus in liver transplant recipients. J Clin Microbiol. 2003;41(11):5147–52.CrossRefPubMedGoogle Scholar
  76. 76.
    Centers for Disease Control and Prevention. Nosocomial enterococci resistant to vancomycin--United States, 1989-1993. MMWR Morb Mortal Wkly Rep. 1993; 42(30):597-9.Google Scholar
  77. 77.
    Drees M, Snydman DR, Schmid CH, et al. Antibiotic exposure and room contamination among patients colonized with vancomycin-resistant enterococci. Infect Control Hosp Epidemiol. 2008;29(8):709–15.CrossRefPubMedGoogle Scholar
  78. 78.
    Olivier CN, Blake RK, Steed LL, Salgado CD. Risk of vancomycin-resistant Enterococcus (VRE) bloodstream infection among patients colonized with VRE. Infect Control Hosp Epidemiol. 2008;29(5):404–9.CrossRefPubMedGoogle Scholar
  79. 79.
    Freitas MC, Pacheco-Silva A, Barbosa D, et al. Prevalence of vancomycin-resistant Enterococcus fecal colonization among kidney transplant patients. BMC Infect Dis. 2006;6:133.CrossRefPubMedGoogle Scholar
  80. 80.
    McNeil SA, Malani PN, Chenoweth CE, et al. Vancomycin-resistant enterococcal colonization and infection in liver transplant candidates and recipients: a prospective surveillance study. Clin Infect Dis. 2006;42(2):195–203. Epub 2005 Dec 12.CrossRefPubMedGoogle Scholar
  81. 81.
    Gearhart M, Martin J, Rudich S, et al. Consequences of vancomycin-resistant Enterococcus in liver transplant recipients: a matched control study. Clin Transplant. 2005;19(6):711–6.PubMedGoogle Scholar
  82. 82.
    Linares L, Cervera C, Cofan F, et al. Epidemiology and outcomes of multiple antibiotic-resistant bacterial infection in renal transplantation. Transplant Proc. 2007;39(7):2222–4.CrossRefPubMedGoogle Scholar
  83. 83.
    El-Khoury J, Fishman JA. Linezolid in the treatment of vancomycin-resistant Enterococcus faecium in solid organ transplant recipients: report of a multicenter compassionate-use trial. Transpl Infect Dis. 2003;5(3):121–5.CrossRefPubMedGoogle Scholar
  84. 84.
    Gonzales RD, Schreckenberger PC, Graham MB, et al. Infections due to vancomycin-resistant Enterococcus faecium resistant to linezolid. Lancet. 2001;357(9263):1179.CrossRefPubMedGoogle Scholar
  85. 85.
    Herrero IA, Issa NC, Patel R. Nosocomial spread of linezolid-resistant, vancomycin-resistant Enterococcus faecium. N Engl J Med. 2002;346(11):867–9.CrossRefPubMedGoogle Scholar
  86. 86.
    Pogue JM, Paterson DL, Pasculle AW, Potoski BA. Determination of risk factors associated with isolation of linezolid-resistant strains of vancomycin-resistant Enterococcus. Infect Control Hosp Epidemiol. 2007;28(12):1382–8.CrossRefPubMedGoogle Scholar
  87. 87.
    • Santayana EM, Grim SA, Janda WM, et al. Risk factors and outcomes associated with vancomycin-resistant Enterococcus infections with reduced susceptibilities to linezolid. Diagn Microbiol Infect Dis. 2012;74(1):39–42. A retrospective matched case–control study of patients with vancomycin-resistant Enterococcus (VRE) with reduced susceptibility to linezolid that demonstrated that receipt of linezolid was associated with reduced susceptibitiy and that reduced susceptibility did not impact patient outcomes, as compared with linezolid-susceptible VRE.CrossRefPubMedGoogle Scholar
  88. 88.
    Twilla JD, Finch CK, Usery JB, et al. Vancomycin-resistant Enterococcus bacteremia: an evaluation of treatment with linezolid or daptomycin. J Hosp Med. 2012;7(3):243–8.CrossRefPubMedGoogle Scholar
  89. 89.
    Munoz-Price LS, Lolans K, Quinn JP. Emergence of resistance to daptomycin during treatment of vancomycin-resistant Enterococcus faecalis infection. Clin Infect Dis. 2005;41(4):565–6.CrossRefPubMedGoogle Scholar
  90. 90.
    Kelesidis T, Humphries R, Uslan DZ, Pegues DA. Daptomycin nonsusceptible enterococci: an emerging challenge for clinicians. Clin Infect Dis. 2011;52(2):228–34.CrossRefPubMedGoogle Scholar
  91. 91.
    Mendes RE, Sader HS, Farrell DJ, Jones RN. Telavancin activity tested against a contemporary collection of Gram-positive pathogens from USA Hospitals (2007-2009). Diagn Microbiol Infect Dis. 2012;72(1):113–7.CrossRefPubMedGoogle Scholar
  92. 92.
    Arias CA, Mendes RE, Stilwell MG, Jones RN, Murray BE. Unmet needs and prospects for oritavancin in the management of vancomycin-resistant enterococcal infections. Clin Infect Dis. 2012;54(S3):S233–8.CrossRefPubMedGoogle Scholar
  93. 93.
    Paterson DL, Rihs JD, Squier C, et al. Lack of efficacy of mupirocin in the prevention of infections with Staphylococcus aureus in liver transplant recipients and candidates. Transplantation. 2003;75(2):194–8.CrossRefPubMedGoogle Scholar
  94. 94.
    Singh N, Squier C, Wannstedt C, et al. Impact of an aggressive infection control strategy on endemic Staphylococcus aureus infection in liver transplant recipients. Infect Control Hosp Epidemiol. 2006;27(2):122–6.CrossRefPubMedGoogle Scholar
  95. 95.
    •• Huang SS, Septimus E, Kleinman K, et al. Targeted versus universal decolonization to prevent ICU infection. N Engl J Med. 2013;368(24):2255–65. A large, randomized multicenter trial assessing the effect of universal decolonization and rates of methicillin-resistant Staphylococcus aureus and bloodstream infections.CrossRefPubMedGoogle Scholar
  96. 96.
    •• Climo MW, Yokoe DS, Warren DK, et al. Effect of daily chlorhexidine bathing on hospital-acquired infection. N Engl J Med. 2013;368(6):533–42. A large multicenter randomized trial demonstrating reduction in the acquisition of multidrug-resistant organsims and the development of health-care-acquired bloodstream infections with daily chlorhexidine bathing.CrossRefPubMedGoogle Scholar
  97. 97.
    Karki S, Cheng AC. Impact of non-rinse skin cleansing with chlorhexidine gluconate on prevention of healthcare-associated infections and colonization with multi-resistant organisms: a systematic review. J Hosp Infect. 2012;82(2):71–84.CrossRefPubMedGoogle Scholar
  98. 98.
    O'Horo JC, Silva GL, Munoz-Price LS, Safdar N. The efficacy of daily bathing with chlorhexidine for reducing healthcare-associated bloodstream infections: a meta-analysis. Infect Control Hosp Epidemiol. 2012;33(3):257–67.CrossRefPubMedGoogle Scholar
  99. 99.
    •• Sifri CD, Ison MG. Highly resistant bacteria and donor-derived infections: treading in uncharted territory. Transpl Infect Dis. 2012;14(3):223–8. A review of published cases of donor-derived multidrug-resistant infections in organ transplantation.CrossRefPubMedGoogle Scholar
  100. 100.
    • Bishara J, Goldberg E, Lev S, et al. The utilization of solid organs for transplantation in the setting of infection with multidrug-resistant organisms: an expert opinion. Clin Transplant. 2012;26(6):811–5. A guidance document offering an opinion on the utilization of organs from donors colonized or infected with multidrug-resistant organisms from an area endemic for carbapenem-resistant Enterobacteriaceae.CrossRefPubMedGoogle Scholar
  101. 101.
    Marchaim D, Chopra T, Bhargava A, Bogan C, Dhar S, Hayakawa K, et al. Recent exposure to antimicrobials and carbapenem-resistant Enterobacteriaceae: the role of antimicrobial stewardship. Infect Control Hosp Epidemiol. 2012;33(8):817–30.CrossRefPubMedGoogle Scholar
  102. 102.
    • Swaminathan M, Sharma S, Poliansky Blash S, et al. Prevalence and risk factors for acquisition of carbepenem-resistant Enterobacteriaceae in the setting of endemicity. Infect Control Hosp Epidemiol. 2013;34(8):809–17. A multicenter study in New York City demonstrated that in an area of endemicity, colonization pressure, mechanical ventilation, and days of antimicrobial exposure were associated with carbapenem-resistant Enterobacteriaceae acquisition.CrossRefPubMedGoogle Scholar
  103. 103.
    Reddy P, Zembower TR, Ison MG, Baker TA, Stosor V. Carbapenem-resistant Acinetobacter baumannii infections after organ transplantation. Transpl Infect Dis. 2010;12(1):87–93.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  • Gopi Patel
    • 1
  • Meenakshi M. Rana
    • 1
  • Shirish Huprikar
    • 1
  1. 1.Division of Infectious Diseases, Department of MedicineIcahn School of Medicine at Mount SinaiNew YorkUSA

Personalised recommendations