Advertisement

Antimicrobial Stewardship: Considerations for a Transplant Center

  • Susan K. SeoEmail author
  • Graeme N. Forrest
Chapter

Abstract

Caring for immunocompromised patients is challenging. Despite significant advances, infection remains a major cause of morbidity and mortality, and as such, these patients are frequently exposed to antimicrobial agents. Antimicrobial stewardship programs (ASPs) can assist transplant centers in optimizing antibiotic usage, particularly in this age of growing microbial resistance and the scarcity of new anti-infective agents in development. The collaborative approach of antimicrobial stewardship serves well in the transplant center where multidisciplinary teamwork is the norm. The purpose of this chapter is to explore both the basic and unique aspects of coordinating an ASP at a transplant center.

Keywords

Antimicrobial stewardship Cost savings Guidelines Infectious diseases Microbiology Multidisciplinary Rapid molecular testing Pharmacy Prescribing strategies 

References

  1. 1.
    Spellberg B, Powers JH, Brass EP, Miller LG, Edwards JE Jr. Trends in antimicrobial drug development: implications for the future. Clin Infect Dis. 2004;38(9):1279–86.PubMedCrossRefPubMedCentralGoogle Scholar
  2. 2.
    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. 2009;48(1):1–12.CrossRefGoogle Scholar
  3. 3.
    Society for Healthcare Epidemiology of America, Infectious Diseases Society of America, Pediatric Infectious Diseases Society. Policy statement on antimicrobial stewardship by the Society for Healthcare Epidemiology of America (SHEA), the Infectious Diseases Society of America (IDSA), and the Pediatric Infectious Diseases Society (PIDS). Infect Control Hosp Epidemiol. 2012;33(4):322–7.CrossRefGoogle Scholar
  4. 4.
    National action plan for combating antibiotic-resistant bacteria. The White House website. https://www.whitehouse.gov/the-press-office/2015/03/27/fact-sheet-obama-administration-releases-national-action-plan-combat-ant. Published 2015. Accessed 6 June 2016.
  5. 5.
    Abbo LM, Ariza-Heredia EJ. Antimicrobial stewardship in immunocompromised hosts. Infect Dis Clin N Am. 2014;28(2):263–79.CrossRefGoogle Scholar
  6. 6.
    Aitken SL, Palmer HR, Topal JE, Gabardi S, Tichy E. Call for antimicrobial stewardship in solid organ transplantation. Am J Transplant. 2013;13(9):2499.PubMedCrossRefPubMedCentralGoogle Scholar
  7. 7.
    Barlam TF, Cosgrove SE, Abbo LM, et al. Implementing an antibiotic stewardship program: guidelines by the Infectious Diseases Society of America and the Society for Healthcare Epidemiology of America. Clin Infect Dis. 2016;62(10):e51–77.PubMedPubMedCentralCrossRefGoogle Scholar
  8. 8.
    Dellit TH, Owens RC, JE MG Jr, et al. 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. 2007;44(2):159–77.PubMedPubMedCentralCrossRefGoogle Scholar
  9. 9.
    Seo SK, Lo K, Abbo LM. Current state of antimicrobial stewardship at solid organ and hematopoietic cell transplant centers in the United States. Infect Control Hosp Epidemiol. 2016;37(10):1195–200.PubMedPubMedCentralCrossRefGoogle Scholar
  10. 10.
    Gross R, Morgan AS, Kinky DE, Weiner M, Gibson GA, Fishman NO. Impact of a hospital-based antimicrobial management program on clinical and economic outcomes. Clin Infect Dis. 2001;33(3):289–95.PubMedCrossRefPubMedCentralGoogle Scholar
  11. 11.
    Core elements of hospital antibiotic stewardship programs. The Centers for Disease Control and Prevention website. http://www.cdc.gov/getsmart/healthcare/implementation/core-elements.html. Updated 2016. Accessed 6 June 2016.
  12. 12.
    Kahan BD. Forty years of publication of Transplantation Proceedings--the fourth decade: globalization of the enterprise. Transplant Proc. 2011;43(1):3–29.PubMedCrossRefPubMedCentralGoogle Scholar
  13. 13.
    Appelbaum FR. Hematopoietic-cell transplantation at 50. N Engl J Med. 2007;357(15):1472–5.PubMedCrossRefPubMedCentralGoogle Scholar
  14. 14.
    Polk RE, Hohmann SF, Medvedev S, Ibrahim O. Benchmarking risk-adjusted adult antibacterial drug use in 70 US academic medical center hospitals. Clin Infect Dis. 2011;53(11):1100–10.PubMedCrossRefPubMedCentralGoogle Scholar
  15. 15.
    Meyer E, Schwab F, Gastmeier P, Ruden H, Heininger A. Antifungal use in intensive care units. J Antimicrob Chemother. 2007;60(3):619–24.PubMedCrossRefPubMedCentralGoogle Scholar
  16. 16.
    Bonadio M, Morelli G, Mori S, Riccioni R, Papineschi F, Petrini M. Fluoroquinolone resistance in hematopoietic stem cell transplant recipients with infectious complications. Biomed Pharmacother. 2005;59(9):511–6.PubMedPubMedCentralCrossRefGoogle Scholar
  17. 17.
    Mikulska M, Del Bono V, Raiola AM, et al. Blood stream infections in allogeneic hematopoietic stem cell transplant recipients: reemergence of Gram-negative rods and increasing antibiotic resistance. Biol Blood Marrow Transplant. 2009;15(1):47–53.PubMedPubMedCentralCrossRefGoogle Scholar
  18. 18.
    Therriault BL, Wilson JW, Barreto JN, Estes LL. Characterization of bacterial infections in allogeneic hematopoietic stem cell transplant recipients who received prophylactic levofloxacin with either penicillin or doxycycline. Mayo Clin Proc. 2010;85(8):711–8.PubMedPubMedCentralCrossRefGoogle Scholar
  19. 19.
    Morris PG, Hassan T, McNamara M, et al. Emergence of MRSA in positive blood cultures from patients with febrile neutropenia--a cause for concern. Support Care Cancer. 2008;16(9):1085–8.PubMedCrossRefPubMedCentralGoogle Scholar
  20. 20.
    Weinstock DM, Conlon M, Iovino C, et al. Colonization, bloodstream infection, and mortality caused by vancomycin-resistant enterococcus early after allogeneic hematopoietic stem cell transplant. Biol Blood Marrow Transplant. 2007;13(5):615–21.PubMedCrossRefPubMedCentralGoogle Scholar
  21. 21.
    Irfan S, Idrees F, Mehraj V, Habib F, Adil S, Hasan R. Emergence of Carbapenem resistant Gram negative and vancomycin resistant Gram positive organisms in bacteremic isolates of febrile neutropenic patients: a descriptive study. BMC Infect Dis. 2008;8:80.PubMedPubMedCentralCrossRefGoogle Scholar
  22. 22.
    Oliveira AL, de Souza M, Carvalho-Dias VM, et al. Epidemiology of bacteremia and factors associated with multi-drug-resistant gram-negative bacteremia in hematopoietic stem cell transplant recipients. Bone Marrow Transplant. 2007;39(12):775–81.PubMedPubMedCentralCrossRefGoogle Scholar
  23. 23.
    Gudiol C, Tubau F, Calatayud L, et al. Bacteraemia due to multidrug-resistant Gram-negative bacilli in cancer patients: risk factors, antibiotic therapy and outcomes. J Antimicrob Chemother. 2011;66(3):657–63.PubMedCrossRefPubMedCentralGoogle Scholar
  24. 24.
    Hamandi B, Holbrook AM, Humar A, et al. Delay of adequate empiric antibiotic therapy is associated with increased mortality among solid-organ transplant patients. Am J Transplant. 2009;9(7):1657–65.PubMedCrossRefPubMedCentralGoogle Scholar
  25. 25.
    Patel R, Allen SL, Manahan JM, et al. Natural history of vancomycin-resistant enterococcal colonization in liver and kidney transplant recipients. Liver Transpl. 2001;7(1):27–31.PubMedCrossRefPubMedCentralGoogle Scholar
  26. 26.
    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.CrossRefGoogle Scholar
  27. 27.
    Munoz P. Multiply resistant gram-positive bacteria: vancomycin-resistant enterococcus in solid organ transplant recipients. Am J Transplant. 2009;9(Suppl 4):S50–6.PubMedPubMedCentralGoogle Scholar
  28. 28.
    Green M, Barbadora K. Recovery of ceftazidime-resistant Klebsiella pneumoniae from pediatric liver and intestinal transplant recipients. Pediatr Transplant. 1998;2(3):224–30.PubMedPubMedCentralGoogle Scholar
  29. 29.
    Paterson DL, Singh N, Rihs JD, Squier C, Rihs BL, Muder RR. Control of an outbreak of infection due to extended-spectrum beta-lactamase--producing Escherichia coli in a liver transplantation unit. Clin Infect Dis. 2001;33(1):126–8.PubMedPubMedCentralCrossRefGoogle Scholar
  30. 30.
    Rebuck JA, Olsen KM, Fey PD, Langnas AN, Rupp ME. Characterization of an outbreak due to extended-spectrum beta-lactamase-producing Klebsiella pneumoniae in a pediatric intensive care unit transplant population. Clin Infect Dis. 2000;31(6):1368–72.CrossRefGoogle Scholar
  31. 31.
    Martins IS, Moreira BM, Riley LW, Santoro-Lopes G. Outbreak of extended-spectrum beta-lactamase-producing Klebsiella pneumoniae infection among renal transplant recipients. J Hosp Infect. 2006;64(3):305–8.PubMedPubMedCentralCrossRefGoogle Scholar
  32. 32.
    Zarate MS, Gales AC, Picao RC, Pujol GS, Lanza A, Smayevsky J. Outbreak of OXY-2-Producing Klebsiella oxytoca in a renal transplant unit. J Clin Microbiol. 2008;46(6):2099–101.PubMedPubMedCentralCrossRefGoogle Scholar
  33. 33.
    Linares L, Cervera C, Cofan F, et al. Risk factors for infection with extended-spectrum and AmpC beta-lactamase-producing gram-negative rods in renal transplantation. Am J Transplant. 2008;8(5):1000–5.PubMedCrossRefPubMedCentralGoogle Scholar
  34. 34.
    van Delden C, Blumberg EA. Multidrug resistant gram-negative bacteria in solid organ transplant recipients. Am J Transplant. 2009;9(Suppl 4):S27–34.PubMedCrossRefPubMedCentralGoogle Scholar
  35. 35.
    Botha P, Archer L, Anderson RL, et al. Pseudomonas aeruginosa colonization of the allograft after lung transplantation and the risk of bronchiolitis obliterans syndrome. Transplantation. 2008;85(5):771–4.PubMedCrossRefPubMedCentralGoogle Scholar
  36. 36.
    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.PubMedPubMedCentralCrossRefGoogle Scholar
  37. 37.
    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.PubMedCrossRefPubMedCentralGoogle Scholar
  38. 38.
    Ananda-Rajah MR, Slavin MA, Thursky KT. The case for antifungal stewardship. Curr Opin Infect Dis. 2012;25(1):107–15.PubMedCrossRefPubMedCentralGoogle Scholar
  39. 39.
    Luong ML, Hosseini-Moghaddam SM, Singer LG, et al. Risk factors for voriconazole hepatotoxicity at 12 weeks in lung transplant recipients. Am J Transplant. 2012;12(7):1929–35.PubMedCrossRefPubMedCentralGoogle Scholar
  40. 40.
    Luong ML, Clancy CJ, Vadnerkar A, et al. Comparison of an Aspergillus real-time polymerase chain reaction assay with galactomannan testing of bronchoalvelolar lavage fluid for the diagnosis of invasive pulmonary aspergillosis in lung transplant recipients. Clin Infect Dis. 2011;52(10):1218–26.PubMedCrossRefPubMedCentralGoogle Scholar
  41. 41.
    Nguyen MH, Leather H, Clancy CJ, et al. Galactomannan testing in bronchoalveolar lavage fluid facilitates the diagnosis of invasive pulmonary aspergillosis in patients with hematologic malignancies and stem cell transplant recipients. Biol Blood Marrow Transplant. 2011;17(7):1043–50.CrossRefGoogle Scholar
  42. 42.
    Seo SK. Antimicrobial stewardship in challenging patient populations. Available at: http://www.medscape.org/viewarticle/767072. Accessed 6 June 2016.
  43. 43.
    Pestotnik SL, Classen DC, Evans RS, Burke JP. Implementing antibiotic practice guidelines through computer-assisted decision support: clinical and financial outcomes. Ann Intern Med. 1996;124(10):884–90.PubMedCrossRefPubMedCentralGoogle Scholar
  44. 44.
    Evans RS, Pestotnik SL, Classen DC, et al. A computer-assisted management program for antibiotics and other antiinfective agents. N Engl J Med. 1998;338(4):232–8.PubMedCrossRefPubMedCentralGoogle Scholar
  45. 45.
    Evans RS, Pestotnik SL, Classen DC, Burke JP. Evaluation of a computer-assisted antibiotic-dose monitor. Ann Pharmacother. 1999;33(10):1026–31.PubMedCrossRefPubMedCentralGoogle Scholar
  46. 46.
    Mullett CJ, Evans RS, Christenson JC, Dean JM. Development and impact of a computerized pediatric antiinfective decision support program. Pediatrics. 2001;108(4):E75.PubMedCrossRefPubMedCentralGoogle Scholar
  47. 47.
    Po JL, Nguyen BQ, Carling PC. The impact of an infectious diseases specialist-directed computerized physician order entry antimicrobial stewardship program targeting linezolid use. Infect Control Hosp Epidemiol. 2012;33(4):434–5.PubMedCrossRefPubMedCentralGoogle Scholar
  48. 48.
    Rodrigues JF, Casado A, Palos C, Santos C, Duarte A, Fernandez-Llimos F. A computer-assisted prescription system to improve antibacterial surgical prophylaxis. Infect Control Hosp Epidemiol. 2012;33(4):435–7.PubMedCrossRefPubMedCentralGoogle Scholar
  49. 49.
    Jaffe D, Jakubowski A, Sepkowitz K, et al. Prevention of peritransplantation viridans streptococcal bacteremia with early vancomycin administration: a single-center observational cohort study. Clin Infect Dis. 2004;39(11):1625–32.PubMedCrossRefPubMedCentralGoogle Scholar
  50. 50.
    Seo SK, Xiao K, Huang YT, et al. Impact of peri-transplant vancomycin and fluoroquinolone administration on rates of bacteremia in allogeneic hematopoietic stem cell transplant (HSCT) recipients: a 12-year single institution study. J Infect. 2014;69(4):341–51.PubMedPubMedCentralCrossRefGoogle Scholar
  51. 51.
    Freifeld AG, Bow EJ, Sepkowitz KA, et al. Clinical practice guideline for the use of antimicrobial agents in neutropenic patients with cancer: 2010 update by the Infectious Diseases Society of America. Clin Infect Dis. 2011;52(4):427–31.PubMedPubMedCentralCrossRefGoogle Scholar
  52. 52.
    Tomblyn M, Chiller T, Einsele H, et al. Guidelines for preventing infectious complications among hematopoietic cell transplantation recipients: a global perspective. Biol Blood Marrow Transplant. 2009;15(10):1143–238.PubMedPubMedCentralCrossRefGoogle Scholar
  53. 53.
    Bratzler DW, Dellinger EP, Olsen KM, et al. Clinical practice guidelines for antimicrobial prophylaxis in surgery. Am J Health Syst Pharm. 2013;70(3):195–283.PubMedPubMedCentralCrossRefGoogle Scholar
  54. 54.
    Zuckermann J, Moreira LB, Stoll P, Moreira LM, Kuchenbecker RS, Polanczyk CA. Compliance with a critical pathway for the management of febrile neutropenia and impact on clinical outcomes. Ann Hematol. 2008;87(2):139–45.PubMedCrossRefPubMedCentralGoogle Scholar
  55. 55.
    Pagano L, Caira M, Offidani M, et al. Adherence to international guidelines for the treatment of invasive aspergillosis in acute myeloid leukaemia: feasibility and utility (SEIFEM-2008B study). J Antimicrob Chemother. 2010;65(9):2013–8.PubMedCrossRefPubMedCentralGoogle Scholar
  56. 56.
    Tyler LS, Cole SW, May JR, et al. ASHP guidelines on the pharmacy and therapeutics committee and the formulary system. Am J Health Syst Pharm. 2008;65(13):1272–83.PubMedCrossRefPubMedCentralGoogle Scholar
  57. 57.
    Griffith MM, Gross AE, Sutton SH, et al. The impact of anti-infective drug shortages on hospitals in the United States: trends and causes. Clin Infect Dis. 2012;54(5):684–91.PubMedCrossRefPubMedCentralGoogle Scholar
  58. 58.
    Paskovaty A, Lucarelli CD, Patel P, et al. Antimicrobial stewardship efforts to manage a pentamidine shortage. Am J Health Syst Pharm. 2014;71(23):2014–8.PubMedCrossRefPubMedCentralGoogle Scholar
  59. 59.
    Lodise TP Jr, Lomaestro B, Drusano GL. Piperacillin-tazobactam for Pseudomonas aeruginosa infection: clinical implications of an extended-infusion dosing strategy. Clin Infect Dis. 2007 Feb;44(3):357–63.PubMedCrossRefPubMedCentralGoogle Scholar
  60. 60.
    Nicolau DP. Pharmacodynamic optimization of beta-lactams in the patient care setting. Crit Care. 2008;12(Suppl 4):S2.PubMedPubMedCentralCrossRefGoogle Scholar
  61. 61.
    Bulik CC, Nicolau DP. In vivo efficacy of simulated human dosing regimens of prolonged-infusion doripenem against carbapenemase- producing Klebsiella pneumoniae. Antimicrob Agents Chemother. 2010;54(10):4112–5.PubMedPubMedCentralCrossRefGoogle Scholar
  62. 62.
    Xamplas RC, Itokazu GS, Glowacki RC, Grasso AE, Caquelin C, Schwartz DN. Implementation of an extended-infusion piperacillin-tazobactam program at an urban teaching hospital. Am J Health Syst Pharm. 2010;67(8):622–8.PubMedCrossRefPubMedCentralGoogle Scholar
  63. 63.
    Yost RJ, Cappelletty DM, RECEIPT Study Group. The Retrospective Cohort of Extended-Infusion Piperacillin-Tazobactam (RECEIPT) study: a multicenter study. Pharmacotherapy. 2011;31(8):767–75.PubMedCrossRefPubMedCentralGoogle Scholar
  64. 64.
    Heinrich LS, Tokumaru S, Clark NM, Garofalo J, Paek JL, Grim SA. Development and implementation of a piperacillin-tazobactam extended infusion guideline. J Pharm Pract. 2011;24(6):571–6.PubMedCrossRefPubMedCentralGoogle Scholar
  65. 65.
    Struelens MJ. Multidisciplinary antimicrobial management teams: the way forward to control antimicrobial resistance in hospitals. Curr Opin Infect Dis. 2003;16(4):305–7.PubMedCrossRefPubMedCentralGoogle Scholar
  66. 66.
    Procop GW, Winn W. Outsourcing microbiology and offsite laboratories. Implications on patient care, cost savings, and graduate medical education. Arch Pathol Lab Med. 2003;127(5):623–4.PubMedPubMedCentralGoogle Scholar
  67. 67.
    Binkley S, Fishman NO, LaRosa LA, et al. Comparison of unit-specific and hospital-wide antibiograms: potential implications for selection of empirical antimicrobial therapy. Infect Control Hosp Epidemiol. 2006;27(7):682–7.PubMedCrossRefPubMedCentralGoogle Scholar
  68. 68.
    Forrest G. Role of antifungal susceptibility testing in patient management. Curr Opin Infect Dis. 2006;19(6):538–43.PubMedCrossRefPubMedCentralGoogle Scholar
  69. 69.
    Shah DN, Yau R, Weston J, et al. Evaluation of antifungal therapy in patients with candidaemia based on susceptibility testing results: implications for antimicrobial stewardship programmes. J Antimicrob Chemother. 2011;66(9):2146–51.PubMedCrossRefPubMedCentralGoogle Scholar
  70. 70.
    Bal AM, Shankland GS, Scott G, Imtiaz T, Macaulay R, McGill M. Antifungal step-down therapy based on hospital intravenous to oral switch policy and susceptibility testing in adult patients with candidaemia: a single centre experience. Int J Clin Pract. 2014;68(1):20–7.PubMedCrossRefPubMedCentralGoogle Scholar
  71. 71.
    Forrest GN. PNA FISH: present and future impact on patient management. Expert Rev Mol Diagn. 2007;7(3):231–6.PubMedCrossRefPubMedCentralGoogle Scholar
  72. 72.
    Faix JD. Using procalcitonin to diagnose sepsis and the potential for improved antibiotic stewardship. MLO Med Lab Obs. 2008;40(11):25–6.PubMedPubMedCentralGoogle Scholar
  73. 73.
    Mancini N, Carletti S, Ghidoli N, Cichero P, Burioni R, Clementi M. The era of molecular and other non-culture-based methods in diagnosis of sepsis. Clin Microbiol Rev. 2010;23(1):235–51.PubMedPubMedCentralCrossRefGoogle Scholar
  74. 74.
    Tsalik EL, Jones D, Nicholson B, et al. Multiplex PCR to diagnose bloodstream infections in patients admitted from the emergency department with sepsis. J Clin Microbiol. 2010;48(1):26–33.PubMedCrossRefPubMedCentralGoogle Scholar
  75. 75.
    Avdic E, Carroll KC. The role of the microbiology laboratory in antimicrobial stewardship programs. Infect Dis Clin N Am. 2014;28(2):215–35.CrossRefGoogle Scholar
  76. 76.
    Gac AC, Parienti JJ, Chantepie S, et al. Dynamics of procalcitonin and bacteremia in neutropenic adults with acute myeloid leukemia. Leuk Res. 2011;35(10):1294–6.PubMedCrossRefPubMedCentralGoogle Scholar
  77. 77.
    Koivula I, Hamalainen S, Jantunen E, et al. Elevated procalcitonin predicts Gram-negative sepsis in haematological patients with febrile neutropenia. Scand J Infect Dis. 2011;43(6–7):471–8.PubMedCrossRefPubMedCentralGoogle Scholar
  78. 78.
    Koivula I, Juutilainen A. Procalcitonin is a useful marker of infection in neutropenia. Leuk Res. 2011;35(10):1288–9.PubMedCrossRefPubMedCentralGoogle Scholar
  79. 79.
    Mylonakis E, Clancy CJ, Ostrosky-Zeichner L, et al. T2 magnetic resonance assay for the rapid diagnosis of candidemia in whole blood: a clinical trial. Clin Infect Dis. 2015;60(6):892–9.PubMedPubMedCentralCrossRefGoogle Scholar
  80. 80.
    von Lilienfeld-Toal M, Lehmann LE, Raadts AD, et al. Utility of a commercially available multiplex real-time PCR assay to detect bacterial and fungal pathogens in febrile neutropenia. J Clin Microbiol. 2009;47(8):2405–10.CrossRefGoogle Scholar
  81. 81.
    Lamoth F, Jaton K, Prod'hom G, et al. Multiplex blood PCR in combination with blood cultures for improvement of microbiological documentation of infection in febrile neutropenia. J Clin Microbiol. 2010;48(10):3510–6.PubMedPubMedCentralCrossRefGoogle Scholar
  82. 82.
    Bauer KA, West JE, Balada-Llasat JM, Pancholi P, Stevenson KB, Goff DA. An antimicrobial stewardship program's impact with rapid polymerase chain reaction methicillin-resistant Staphylococcus aureus/S. aureus blood culture test in patients with S. aureus bacteremia. Clin Infect Dis. 2010;51(9):1074–80.PubMedCrossRefPubMedCentralGoogle Scholar
  83. 83.
    O'Horo JC, Jones A, Sternke M, Harper C, Safdar N. Molecular techniques for diagnosis of Clostridium difficile infection: systematic review and meta-analysis. Mayo Clin Proc. 2012;87(7):643–51.PubMedPubMedCentralCrossRefGoogle Scholar
  84. 84.
    Crobach MJ, Dekkers OM, Wilcox MH, Kuijper EJ. European Society of Clinical Microbiology and Infectious Diseases (ESCMID): data review and recommendations for diagnosing Clostridium difficile-infection (CDI). Clin Microbiol Infect. 2009;15(12):1053–66.PubMedCrossRefPubMedCentralGoogle Scholar
  85. 85.
    Knetsch CW, Bakker D, de Boer RF, et al. Comparison of real-time PCR techniques to cytotoxigenic culture methods for diagnosing Clostridium difficile infection. J Clin Microbiol. 2011;49(1):227–31.PubMedCrossRefPubMedCentralGoogle Scholar
  86. 86.
    Dubberke ER, Wertheimer AI. Review of current literature on the economic burden of Clostridium difficile infection. Infect Control Hosp Epidemiol. 2009;30(1):57–66.PubMedCrossRefPubMedCentralGoogle Scholar
  87. 87.
    Nerandzic MM, Mullane K, Miller MA, Babakhani F, Donskey CJ. Reduced acquisition and overgrowth of vancomycin-resistant enterococci and Candida species in patients treated with fidaxomicin versus vancomycin for Clostridium difficile infection. Clin Infect Dis. 2012;55(Suppl 2):S121–6.PubMedPubMedCentralCrossRefGoogle Scholar
  88. 88.
    Suzuki H, Hitomi S, Yaguchi Y, et al. Prospective intervention study with a microarray-based, multiplexed, automated molecular diagnosis instrument (Verigene system) for the rapid diagnosis of bloodstream infections, and its impact on the clinical outcomes. J Infect Chemother. 2015;21(12):849–56.PubMedCrossRefPubMedCentralGoogle Scholar
  89. 89.
    Banerjee R, Teng CB, Cunningham SA, et al. Randomized trial of rapid multiplex polymerase chain reaction-based blood culture identification and susceptibility testing. Clin Infect Dis. 2015;61(7):1071–80.PubMedPubMedCentralCrossRefGoogle Scholar
  90. 90.
    Perez KK, Olsen RJ, Musick WL, et al. Integrating rapid pathogen identification and antimicrobial stewardship significantly decreases hospital costs. Arch Pathol Lab Med. 2013;137(9):1247–54.PubMedCrossRefPubMedCentralGoogle Scholar
  91. 91.
    Deck MK, Anderson ES. Buckner RJ,et al. Multicenter evaluation of the Staphylococcus QuickFISH method for simultaneous identification of Staphylococcus aureus and coagulase-negative staphylococci directly from blood culture bottles in less than 30 minutes. J Clin Microbiol. 2012;50(6):1994–8.PubMedPubMedCentralCrossRefGoogle Scholar
  92. 92.
    Forrest GN, Mehta S, Weekes E, Lincalis DP, Johnson JK, Venezia RA. Impact of rapid in situ hybridization testing on coagulase-negative staphylococci positive blood cultures. J Antimicrob Chemother. 2006;58(1):154–8.PubMedCrossRefPubMedCentralGoogle Scholar
  93. 93.
    Forrest GN, Mankes K, Jabra-Rizk MA, et al. Peptide nucleic acid fluorescence in situ hybridization-based identification of Candida albicans and its impact on mortality and antifungal therapy costs. J Clin Microbiol. 2006;44(9):3381–3.PubMedPubMedCentralCrossRefGoogle Scholar
  94. 94.
    Forrest GN, Roghmann MC, Toombs LS, et al. Peptide nucleic acid fluorescent in situ hybridization for hospital-acquired enterococcal bacteremia: delivering earlier effective antimicrobial therapy. Antimicrob Agents Chemother. 2008;52(10):3558–63.PubMedPubMedCentralCrossRefGoogle Scholar
  95. 95.
    Holtzman C, Whitney D, Barlam T, Miller NS. Assessment of impact of peptide nucleic acid fluorescence in situ hybridization for rapid identification of coagulase-negative staphylococci in the absence of antimicrobial stewardship intervention. J Clin Microbiol. 2011;49(4):1581–2.PubMedPubMedCentralCrossRefGoogle Scholar
  96. 96.
    Frobert E, Burrel S, Ducastelle-Lepretre S, et al. Resistance of herpes simplex viruses to acyclovir: an update from a ten-year survey in France. Antivir Res. 2014;111:36–41.PubMedCrossRefPubMedCentralGoogle Scholar
  97. 97.
    Tramontana AR, George B, Hurt AC, et al. Oseltamivir resistance in adult oncology and hematology patients infected with pandemic (H1N1) 2009 virus, Australia. Emerg Infect Dis. 2010;16(7):1068–75.PubMedPubMedCentralCrossRefGoogle Scholar
  98. 98.
    Chou S. Approach to drug-resistant cytomegalovirus in transplant recipients. Curr Opin Infect Dis. 2015;28(4):293–9.PubMedPubMedCentralCrossRefGoogle Scholar
  99. 99.
    Pfaller MA. Antifungal drug resistance: mechanisms, epidemiology, and consequences for treatment. Am J Med. 2012;125(1 Suppl):S3–13.PubMedPubMedCentralCrossRefGoogle Scholar
  100. 100.
    van der Linden JW, Arendrup MC, Melchers WJ, Verweij PE. Azole resistance of Aspergillus fumigatus in immunocompromised patients with invasive aspergillosis. Emerg Infect Dis. 2016;22(1):158–9.PubMedPubMedCentralCrossRefGoogle Scholar
  101. 101.
    Marty FM, Cosimi LA, Baden LR. Breakthrough zygomycosis after voriconazole treatment in recipients of hematopoietic stem-cell transplants. N Engl J Med. 2004;350(9):950–2.PubMedPubMedCentralCrossRefGoogle Scholar
  102. 102.
    Pongas GN, Lewis RE, Samonis G, Kontoyiannis DP. Voriconazole-associated zygomycosis: a significant consequence of evolving antifungal prophylaxis and immunosuppression practices? Clin Microbiol Infect. 2009;15(Suppl 5):93–7.PubMedPubMedCentralCrossRefGoogle Scholar
  103. 103.
    Dervite I, Hober D, Morel P. Acute hepatitis B in a patient with antibodies to hepatitis B surface antigen who was receiving rituximab. N Engl J Med. 2001;344(1):68–9.PubMedCrossRefPubMedCentralGoogle Scholar
  104. 104.
    Tsutsumi Y, Tanaka J, Kawamura T, et al. Possible efficacy of lamivudine treatment to prevent hepatitis B virus reactivation due to rituximab therapy in a patient with non-Hodgkin's lymphoma. Ann Hematol. 2004;83(1):58–60.PubMedCrossRefPubMedCentralGoogle Scholar
  105. 105.
    Martin SI, Marty FM, Fiumara K, Treon SP, Gribben JG, Baden LR. Infectious complications associated with alemtuzumab use for lymphoproliferative disorders. Clin Infect Dis. 2006;43(1):16–24.PubMedCrossRefPubMedCentralGoogle Scholar
  106. 106.
    Iversen M, Burton CM, Vand S, et al. Aspergillus infection in lung transplant patients: incidence and prognosis. Eur J Clin Microbiol Infect Dis. 2007;26(12):879–86.PubMedCrossRefPubMedCentralGoogle Scholar
  107. 107.
    Koo S, Marty FM, Baden LR. Infectious complications associated with immunomodulating biologic agents. Infect Dis Clin N Am. 2010;24(2):285–306.CrossRefGoogle Scholar
  108. 108.
    Woodward RS, Medoff G, Smith MD, Gray JL 3rd. Antibiotic cost savings from formulary restrictions and physician monitoring in a medical-school-affiliated hospital. Am J Med. 1987;83(5):817–23.PubMedCrossRefPubMedCentralGoogle Scholar
  109. 109.
    Coleman RW, Rodondi LC, Kaubisch S, Granzella NB, O'Hanley PD. Cost-effectiveness of prospective and continuous parenteral antibiotic control: experience at the Palo Alto Veterans Affairs Medical Center from 1987 to 1989. Am J Med. 1991;90(4):439–44.PubMedCrossRefPubMedCentralGoogle Scholar
  110. 110.
    Maswoswe JJ, Okpara AU. Enforcing a policy for restricting antimicrobial drug use. Am J Health Syst Pharm. 1995;52(13):1433–5.PubMedCrossRefPubMedCentralGoogle Scholar
  111. 111.
    White AC Jr, Atmar RL, Wilson J, Cate TR, Stager CE, Greenberg SB. Effects of requiring prior authorization for selected antimicrobials: expenditures, susceptibilities, and clinical outcomes. Clin Infect Dis. 1997;25(2):230–9.PubMedCrossRefPubMedCentralGoogle Scholar
  112. 112.
    Schentag JJ, Ballow CH, Fritz AL, et al. Changes in antimicrobial agent usage resulting from interactions among clinical pharmacy, the infectious disease division, and the microbiology laboratory. Diagn Microbiol Infect Dis. 1993;16(3):255–64.PubMedCrossRefPubMedCentralGoogle Scholar
  113. 113.
    Fraser GL, Stogsdill P, Dickens JD Jr, Wennberg DE, Smith RP Jr, Prato BS. Antibiotic optimization. An evaluation of patient safety and economic outcomes. Arch Intern Med. 1997;157(15):1689–94.PubMedCrossRefPubMedCentralGoogle Scholar
  114. 114.
    Carling P, Fung T, Killion A, Terrin N, Barza M. Favorable impact of a multidisciplinary antibiotic management program conducted during 7 years. Infect Control Hosp Epidemiol. 2003;24(9):699–706.PubMedCrossRefPubMedCentralGoogle Scholar
  115. 115.
    LaRocco A Jr. Concurrent antibiotic review programs--a role for infectious diseases specialists at small community hospitals. Clin Infect Dis. 2003;37(5):742–3.PubMedCrossRefPubMedCentralGoogle Scholar
  116. 116.
    Cosgrove SE, Seo SK, Bolon MK, et al. Evaluation of postprescription review and feedback as a method of promoting rational antimicrobial use: a multicenter intervention. Infect Control Hosp Epidemiol. 2012;33(4):374–80.PubMedPubMedCentralCrossRefGoogle Scholar
  117. 117.
    Paskovaty A, Pflomm JM, Myke N, Seo SK. A multidisciplinary approach to antimicrobial stewardship: evolution into the 21st century. Int J Antimicrob Agents. 2005;25(1):1–10.PubMedPubMedCentralCrossRefGoogle Scholar
  118. 118.
    Bearden DT, Allen GP. Impact of antimicrobial control programs on patient outcomes. Pharmacy perspective. Dis Manag Health Out. 2003;11(11):723–36.CrossRefGoogle Scholar
  119. 119.
    Grimshaw JM, Shirran L, Thomas R, et al. Changing provider behavior: an overview of systematic reviews of interventions. Med Care. 2001;39(8 Suppl 2):II2–45.PubMedPubMedCentralGoogle Scholar
  120. 120.
    Gray J. Changing physician prescribing behaviour. Can J Clin Pharmacol. 2006;13(1):e81–4.PubMedPubMedCentralGoogle Scholar
  121. 121.
    Girotti MJ, Fodoruk S, Irvine-Meek J, Rotstein OD. Antibiotic handbook and pre-printed perioperative order forms for surgical antibiotic prophylaxis: do they work? Can J Surg. 1990;33(5):385–8.PubMedPubMedCentralGoogle Scholar
  122. 122.
    Bantar C, Sartori B, Vesco E, et al. A hospitalwide intervention program to optimize the quality of antibiotic use: impact on prescribing practice, antibiotic consumption, cost savings, and bacterial resistance. Clin Infect Dis. 2003;37(2):180–6.PubMedCrossRefPubMedCentralGoogle Scholar
  123. 123.
    Belongia EA, Knobloch MJ, Kieke BA, Davis JP, Janette C, Besser RE. Impact of statewide program to promote appropriate antimicrobial drug use. Emerg Infect Dis. 2005 Jun;11(6):912–20.PubMedPubMedCentralCrossRefGoogle Scholar
  124. 124.
    Patterson TF, Thompson GR 3rd, Denning DW, et al. Practice guidelines for the diagnosis and management of aspergillosis: 2016 update by the Infectious Diseases Society of America. Clin Infect Dis. 2016;63(4):e1–e60.PubMedPubMedCentralCrossRefGoogle Scholar
  125. 125.
    Pappas PG, Kauffman CA, Andes DR, et al. Clinical practice guideline for the management of candidiasis: 2016 update by the Infectious Diseases Society of America. Clin Infect Dis. 2016;62(4):e1–50.CrossRefGoogle Scholar
  126. 126.
    Chastre J, Wolff M, Fagon JY, et al. Comparison of 8 vs 15 days of antibiotic therapy for ventilator-associated pneumonia in adults: a randomized trial. JAMA. 2003;290(19):2588–98.PubMedCrossRefPubMedCentralGoogle Scholar
  127. 127.
    Singh N, Rogers P, Atwood CW, Wagener MM, Yu VL. Short-course empiric antibiotic therapy for patients with pulmonary infiltrates in the intensive care unit. A proposed solution for indiscriminate antibiotic prescription. Am J Respir Crit Care Med. 2000;162(2. Pt 1):505–11.PubMedCrossRefPubMedCentralGoogle Scholar
  128. 128.
    Kollef MH, Kollef KE. Antibiotic utilization and outcomes for patients with clinically suspected ventilator-associated pneumonia and negative quantitative BAL culture results. Chest. 2005;128(4):2706–13.PubMedCrossRefPubMedCentralGoogle Scholar
  129. 129.
    Briceland LL, Nightingale CH, Quintiliani R, Cooper BW, Smith KS. Antibiotic streamlining from combination therapy to monotherapy utilizing an interdisciplinary approach. Arch Intern Med. 1988;148(9):2019–22.PubMedCrossRefPubMedCentralGoogle Scholar
  130. 130.
    Glowacki RC, Schwartz DN, Itokazu GS, Wisniewski MF, Kieszkowski P, Weinstein RA. Antibiotic combinations with redundant antimicrobial spectra: clinical epidemiology and pilot intervention of computer-assisted surveillance. Clin Infect Dis. 2003;37(1):59–64.PubMedCrossRefPubMedCentralGoogle Scholar
  131. 131.
    Lelekis M, Gould IM. Sequential antibiotic therapy for cost containment in the hospital setting: why not? J Hosp Infect. 2001;48(4):249–57.PubMedCrossRefPubMedCentralGoogle Scholar
  132. 132.
    Drew RH. Programs promoting timely sequential antimicrobial therapy: an American perspective. J Infect. 1998;37(Suppl 1):3–9.PubMedCrossRefPubMedCentralGoogle Scholar
  133. 133.
    Amodio-Groton M, Madu A, Madu CN, et al. Sequential parenteral and oral ciprofloxacin regimen versus parenteral therapy for bacteremia: a pharmacoeconomic analysis. Ann Pharmacother. 1996;30(6):596–602.PubMedCrossRefPubMedCentralGoogle Scholar
  134. 134.
    Sevinc F, Prins JM, Koopmans RP, et al. Early switch from intravenous to oral antibiotics: guidelines and implementation in a large teaching hospital. J Antimicrob Chemother. 1999;43(4):601–6.PubMedCrossRefPubMedCentralGoogle Scholar
  135. 135.
    Ramirez JA, Bordon J. Early switch from intravenous to oral antibiotics in hospitalized patients with bacteremic community-acquired Streptococcus pneumoniae pneumonia. Arch Intern Med. 2001;161(6):848–50.PubMedCrossRefPubMedCentralGoogle Scholar
  136. 136.
    Wong-Beringer A, Nguyen KH, Razeghi J. Implementing a program for switching from i.v. to oral antimicrobial therapy. Am J Health Syst Pharm. 2001;58(12):1146–9.PubMedCrossRefPubMedCentralGoogle Scholar
  137. 137.
    Jones M, Huttner B, Madaras-Kelly K, et al. Parenteral to oral conversion of fluoroquinolones: low-hanging fruit for antimicrobial stewardship programs? Infect Control Hosp Epidemiol. 2012;33(4):362–7.PubMedCrossRefPubMedCentralGoogle Scholar
  138. 138.
    Lutters M, Harbarth S, Janssens JP, et al. Effect of a comprehensive, multidisciplinary, educational program on the use of antibiotics in a geriatric university hospital. J Am Geriatr Soc. 2004;52(1):112–6.PubMedCrossRefPubMedCentralGoogle Scholar
  139. 139.
    Paskovaty A, Pastores SM, Gedrimaite Z, Kostelecky N, Riedel ER, Seo SK. Antimicrobial de-escalation in septic cancer patients: is it safe to back down? Intensive Care Med. 2015;41(11):2022–3.PubMedPubMedCentralCrossRefGoogle Scholar
  140. 140.
    Standiford HC, Chan S, Tripoli M, Weekes E, Forrest GN. Antimicrobial stewardship at a large tertiary care academic medical center: cost analysis before, during, and after a 7-year program. Infect Control Hosp Epidemiol. 2012;33(4):338–45.PubMedCrossRefPubMedCentralGoogle Scholar
  141. 141.
    Lopez-Medrano F, San Juan R, Lizasoain M, et al. A non-compulsory stewardship programme for the management of antifungals in a university-affiliated hospital. Clin Microbiol Infect. 2013;19(1):56–61.PubMedCrossRefPubMedCentralGoogle Scholar
  142. 142.
    Mondain V, Lieutier F, Hasseine L, et al. A 6-year antifungal stewardship programme in a teaching hospital. Infection. 2013;41(3):621–8.PubMedCrossRefPubMedCentralGoogle Scholar
  143. 143.
    Micallef C, Aliyu SH, Santos R, Brown NM, Rosembert D, Enoch DA. Introduction of an antifungal stewardship programme targeting high-cost antifungals at a tertiary hospital in Cambridge, England. J Antimicrob Chemother. 2015;70(6):1908–11.PubMedPubMedCentralGoogle Scholar
  144. 144.
    Hamdy RF, Zaoutis TE, Seo SK. Antifungal stewardship considerations for adults and pediatrics. Virulence. 2017;8(6):658–72.PubMedCrossRefPubMedCentralGoogle Scholar
  145. 145.
    Wolf J, Sun Y, Tang L, et al. Antimicrobial stewardship barriers and goals in pediatric oncology and bone marrow transplantation: a survey of antimicrobial stewardship practitioners. Infect Control Hosp Epidemiol. 2016;37(3):343–7.PubMedCrossRefPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of MedicineInfectious Disease Service, Memorial Sloan-Kettering Cancer CenterNew YorkUSA
  2. 2.Division of Infectious DiseasesPortland VA Medical Center and Oregon Health and Science UniversityPortlandUSA

Personalised recommendations