Enterobacteriaceae in Transplantation

  • Kathryn Whitaker
  • Valerie Cluzet
  • Emily A. BlumbergEmail author


Enterobacteriaceae comprise important pathogens for recipients of solid organ and hematopoietic stem cell transplants. Especially common in the early posttransplant period when transplant recipients are still hospitalized, they can occur at any time following the procedure. Increasing frequency of colonization and invasive disease due to antimicrobial-resistant pathogens has been described in recipients of solid organ and hematopoietic stem cell transplants. In solid organ transplant recipients, surgical considerations may affect the development of these infections, and transplant organ-specific infections are frequently seen. In stem cell recipients, blood stream infections are among the most common manifestations. In cases of respiratory tract, superficial wound, and urinary tract isolation of Enterobacteriaceae, it is important to differentiate colonization from true infection. The choice of appropriate antimicrobials should include consideration of the risk for antimicrobial resistance. Source control may be critical to cure infection, especially when the patient has either line-related bloodstream infection or surgical site/wound involvement. Transplant recipients may also be at risk for infection with Enterobacteriaceae that are not typically considered pathogenic in the normal host; consequently, all cultures should be carefully interpreted with respect to clinical presentation and the source of the culture.


Solid organ transplantation Hematopoietic stem cell transplantation Escherichia coli Klebsiella spp. Enterobacter spp. Serratia spp. Citrobacter spp. Proteus spp. Salmonella spp. Shigella spp. Yersinia spp. 


  1. 1.
    Meatherall BL, Gregson D, Ross T, et al. Incidence, risk factors, and outcomes of Klebsiella pneumoniae bacteremia. Am J Med. 2009;122:866.PubMedCrossRefPubMedCentralGoogle Scholar
  2. 2.
    Centers for Disease Control and Prevention. Surveillance for Emerging Antimicrobial Resistance Connected to Healthcare (S.E.A.R.C.H.) Accessed 4/12/2017.
  3. 3.
  4. 4.
    Kawecki D, Kwiatkowski A, Sawicka-Grzelak A, et al. Urinary tract infections in the early posttransplant period after kidney transplantation: etiologic agents and their susceptibility. Transplant Proc. 2011;43:2991–3.PubMedCrossRefPubMedCentralGoogle Scholar
  5. 5.
    Dantas SR, Kuboyama RH, Mazzali M, et al. Nosocomial infections in renal transplant patients: risk factors and treatment implications associated with urinary tract and surgical site infections. J Hosp Infect. 2006;63(2):117–23.PubMedCrossRefPubMedCentralGoogle Scholar
  6. 6.
    Giral M, Pascuariello G, Karam G, et al. Acute graft pyelonephritis and long-term kidney allograft outcome. Kidney Int. 2002;61:1880–6.PubMedCrossRefPubMedCentralGoogle Scholar
  7. 7.
    Vidal E, Torre-Cisneros J, Blanes M, et al. Bacterial urinary tract infection after solid organ transplantation in the RESITRA cohort. Transpl Infect Dis. 2012;14:595–603.PubMedCrossRefPubMedCentralGoogle Scholar
  8. 8.
    Herrero-Martínez JM, Lumbreras C, Manrique A, et al. Epidemiology, risk factors and impact on long-term pancreatic function of infection following pancreas-kidney transplantation. Clin Microbiol Infect. 2013;19:1132–9.PubMedCrossRefPubMedCentralGoogle Scholar
  9. 9.
    Brooks RG, Hofflin JM, Jamieson SW, et al. Infectious complications in heart-lung transplant recipients. Am J Med. 1985;79:412–22.PubMedCrossRefPubMedCentralGoogle Scholar
  10. 10.
    Gullestad L, Eisjkauer H, Gustafsson F, et al. Long-term outcomes of thoracic transplant recipients following conversion to everolimus with reduced calcineurin inhibitor in a multicenter, open-label, randomized trial. Transpl Int. 2016;29:819–29.PubMedCrossRefPubMedCentralGoogle Scholar
  11. 11.
    Yun JH, Kee S-O, Jo K-W, et al. Infections after lung transplantation: time of occurrence, sites, and microbiologic etiologies. Korean J Intern Med. 2015;30:506– Scholar
  12. 12.
    Paya CV, Wiesner RH, Herman PE, et al. Risk factors for cytomegalovirus and severe bacterial infections following liver transplantation: a prospective multivariate time-dependent analysis. J Hepatol. 1993;18:185–95.PubMedCrossRefPubMedCentralGoogle Scholar
  13. 13.
    Lumbreras C, Lizasoin M, Moreno E, et al. Major bacterial infections following liver transplantation: a prospective study. Hepatogastroenterol. 1992;39:362–5.Google Scholar
  14. 14.
    Linares L, García GJ, Cervera C, et al. Early bacteremia after solid organ transplantation. Transplant Proc. 2009;41:2262–4.PubMedCrossRefPubMedCentralGoogle Scholar
  15. 15.
    Wingard JR, Hsu J, Hiemenz JW. Hematopoietic stem cell transplantation: an overview of infection risks and epidemiology. Infect Dis Clin North Am. 2010;24:257–72.PubMedCrossRefPubMedCentralGoogle Scholar
  16. 16.
    Mikulska M, Del Bono V, Viscoli C. Bacterial infections in hematopoietic stem cell transplantation recipients. Curr Opin Hematol. 2014;21:451–8.PubMedCrossRefPubMedCentralGoogle Scholar
  17. 17.
    Balletto E, Mikulska M. Bacterial infections in hematopoietic stem cell transplant recipients. Mediterr J Hematol Infect Dis. 2015;7:e2015045.PubMedPubMedCentralCrossRefGoogle Scholar
  18. 18.
    Zając-Spychała O, Wachowiak J, Pieczonka A, Siewiera K, Frączkiewicz J, Kałwak K, et al. Bacterial infections in pediatric hematopoietic stem cell transplantation recipients: incidence, epidemiology, and spectrum of pathogens: report of the Polish Pediatric Group for hematopoietic stem cell transplantation. Transpl Infect Dis. 2016;18:690–8.PubMedCrossRefPubMedCentralGoogle Scholar
  19. 19.
    Parasuraman R, Julian K. Urinary tract infections in solid organ transplantation. Am J Transplant. 2013;13:327–36.PubMedCrossRefPubMedCentralGoogle Scholar
  20. 20.
    Green H, Rahamimov R, Gafter U, Leibovitci L, Paul M. Antibiotic prophylaxis for urinary tract infections in renal transplant recipients: systematic review and meta-analysis. Transpl Infect Dis. 2011;13:441–7.PubMedCrossRefPubMedCentralGoogle Scholar
  21. 21.
    Espinar EJ, Miranda IM, Costa-de-Oliveira S, Rocha R, Rodrigues AG, Pina-Vaz C. Urinary tract infections in kidney transplant patients due to Escherichia coli and Klebsiella pneumoniae-producing extended-spectrum β-lactamases: risk factors and molecular epidemiology. PLoS One. 2015;10(8):e0134737.PubMedPubMedCentralCrossRefGoogle Scholar
  22. 22.
    Azap Ö, Togan T, Yesilkaya A, Arslan H, Haberal M. Antimicrobial susceptibilities of uropathogen Escherichia coli in renal transplant recipients: dramatic increase in ciprofloxacin resistance. Transplant Proc. 2013;45:956–7.PubMedCrossRefPubMedCentralGoogle Scholar
  23. 23.
    Gołębiewska J, Tarasewicz A, Dębska-Ślizień A, Rutkowski B. Klebsiella spp urinary tract infections during first year after renal transplantation. Transplant Proc. 2014;46:2748–51.PubMedCrossRefPubMedCentralGoogle Scholar
  24. 24.
    Freire MP, Abdala E, Moura ML, et al. Risk factors and outcome of infections with Klebsiella pneumoniae carbapenemase-producing K. pneumoniae in kidney transplant recipients. Infection. 2015;43:315–23.PubMedCrossRefPubMedCentralGoogle Scholar
  25. 25.
    Brizendine KD, Richter SS, Cober ED, van Duin D. Carbapenem-resistant Klebsiella pneumoniae urinary tract infection following solid organ transplantation. Antimicrob Agents Chemother. 2015;59:553–7.PubMedCrossRefPubMedCentralGoogle Scholar
  26. 26.
    Pelle G, Vimont S, Levy PP, et al. Acute pyelonephritis represents a risk factor impairing long-term kidney graft function. Am J Transplant. 2007;7:899–907.PubMedCrossRefPubMedCentralGoogle Scholar
  27. 27.
    Audard V, Amor M, Desvaux D, et al. Acute graft pyelonephritis: a potential cause of acute rejection in renal transplant. Transplantation. 2005;80:1128–30.PubMedCrossRefPubMedCentralGoogle Scholar
  28. 28.
    Kamath NS, John GT, Neelakantan N, et al. Acute graft pyelonephritis following renal transplantation. Transpl Infect Dis. 2006;8:140–7.PubMedCrossRefPubMedCentralGoogle Scholar
  29. 29.
    Naik AS, Dharnidharka VR, Schnitzler MA, et al. Clinical and economic consequences of first-year urinary tract infections, sepsis, and pneumonia in contemporary kidney transplantation practice. Transpl Int. 2016;29:241–52.PubMedCrossRefPubMedCentralGoogle Scholar
  30. 30.
    Abbott KC, Swanson SJ, Richter ER, et al. Late urinary tract infection after renal transplantation in the United States. Am J Kidney Dis. 2004;44:353–62.CrossRefGoogle Scholar
  31. 31.
    Fiorante S, Fernández-Ruiz M, López-Medrano F, et al. Acute graft pyelonephritis in renal transplant recipients: incidence, risk factors and long-term outcome. Nephrol Dial Transplant. 2011;26:1065–73.PubMedPubMedCentralCrossRefGoogle Scholar
  32. 32.
    Camargo LF, Esteves ABA, Ulisses LRS, Rivelli GG, Mazzali M. Urinary tract infection in renal transplant recipients: incidence, risk factors, and impact on graft function. Transplant Proc. 2014;46:1757–9.PubMedCrossRefPubMedCentralGoogle Scholar
  33. 33.
    Ariza-Heredia EJ, Beam EN, Lesnick TG, Cosio FG, Kremers WK, Razonable RR. Impact of urinary tract infection on allograft function after kidney transplantation. Clin Transpl. 2014;28:683–90.CrossRefGoogle Scholar
  34. 34.
    George DL, Arnow PM, Fox AS, et al. Bacterial infection as a complication of liver transplantation: epidemiology and risk factors. Rev Infect Dis. 1991;3:287–96.Google Scholar
  35. 35.
    Viehman JA, Clancy CJ, Clarke L, et al. Surgical site infections after liver transplantation: emergence of multidrug-resistant bacteria and implications for prophylaxis and treatment strategies. Transplantation. 2016;100:2107–14.CrossRefGoogle Scholar
  36. 36.
    Kornasiewicz O, Hołówko W, Grąt M, et al. Hepatic abscess: a rare complication after liver transplant. Clin Transpl. 2016;30:1230–5.CrossRefGoogle Scholar
  37. 37.
    Wade JJ, Rolando N, Hayllar K, et al. Bacterial and fungal infections after liver transplantation: an analysis of 284 patients. Hepatology. 1995;21:1328–36.PubMedCrossRefPubMedCentralGoogle Scholar
  38. 38.
    Bubak ME, Porayko MK, Krom RAF, et al. Complications of liver biopsy in liver transplant patients: increased sepsis associated with choledochojejunostomy. Hepatology. 1991;14:1063–5.PubMedCrossRefPubMedCentralGoogle Scholar
  39. 39.
    Krom RAF, Kingma LM, Haagsma EB, et al. Choledochocholedochostomy, a relatively safe procedure in orthotopic liver transplantation. Surgery. 1985;97:552–6.PubMedPubMedCentralGoogle Scholar
  40. 40.
    Arnow PM, Zachary KC, Thistlethwaite JR, Thompson KD, Bova JL, Newell KA. Pathogenesis of early operative site infections after orthotopic liver transplantation. Transplantation. 1998;65:1500–3.PubMedCrossRefPubMedCentralGoogle Scholar
  41. 41.
    Yamamoto M, Takakura S, Iinuma Y, et al. Changes in surgical site infections after living donor liver transplantation. PLoS One. 2015;10(8):e0136559.PubMedPubMedCentralCrossRefGoogle Scholar
  42. 42.
    Kotloff RM, Ahya VN, Crawford SW. Pulmonary complications of solid organ and hematopoietic stem cell transplantation. Am J Respir Crit Care Med. 2004;170(1):22–48.PubMedPubMedCentralCrossRefGoogle Scholar
  43. 43.
    Kramer MR, Marshall SE, Starnes VA, et al. Infectious complications in heart-lung transplantation. Analysis of 200 episodes. Arch Intern Med. 1993;153(17):2010–6.PubMedCrossRefPubMedCentralGoogle Scholar
  44. 44.
    Maurer JR, Tullis DE, Grossman RF, et al. Infectious complications following isolated lung transplantation. Chest. 1992;101(4):1056–9.PubMedCrossRefPubMedCentralGoogle Scholar
  45. 45.
    Cisneros JM, Munoz P, Torre-Cisneros J, et al. Pneumonia after heart transplantation: a multi-institutional study. Spanish Transplantation Infection Study Group. Clin Infect Dis. 1998;27(2):324–31.PubMedCrossRefPubMedCentralGoogle Scholar
  46. 46.
    Cervera C, Augusti C, Marcos MA, et al. Microbiologic features and outcome of pneumonia in transplanted patients. Diagn Microbiol Infect Dis. 2006;55:47–54.CrossRefGoogle Scholar
  47. 47.
    Bonatti H, Pruett TL, Brandacher G, et al. Pneumonia in solid organ recipients: Spectrum of pathogens in 217 episodes. Transplant Proc. 2009;41:371–4.PubMedCrossRefPubMedCentralGoogle Scholar
  48. 48.
    Aguilar-Guisado M, Jiménez-Jambrina M, Espigado I, et al. Pneumonia in allogeneic stem cell transplantation recipients: a multicenter prospective study. Clin Transpl. 2011;25:E629–38.CrossRefGoogle Scholar
  49. 49.
    Giannella M, Muñoz P, Alarcón JM, et al. Pneumonia in solid organ transplant recipients: a prospective multicenter study. Transpl Infect Dis. 2014;16:232–41.PubMedCrossRefPubMedCentralGoogle Scholar
  50. 50.
    Bige N, Zafrani L, Lambert J, et al. Severe infections requiring intensive care unit admission in kidney transplant recipients: impact on graft outcome. Transpl Infect Dis. 2014;16:588–96.PubMedCrossRefPubMedCentralGoogle Scholar
  51. 51.
    Mermel LA, Maki DG. Bacterial pneumonia in solid organ transplantation. Semin Respir Infect. 1990;5(1):10–29.PubMedPubMedCentralGoogle Scholar
  52. 52.
    Patel SR, Kirby TJ, McCarthy PM, et al. Lung transplantation: the Cleveland Clinic experience. Cleve Clin J Med. 1993;60:303–19.PubMedCrossRefPubMedCentralGoogle Scholar
  53. 53.
    Deusch E, End A, Grimm M, et al. Early bacterial infections in lung transplant recipients. Chest. 1993;104:1412–6.52.PubMedCrossRefPubMedCentralGoogle Scholar
  54. 54.
    Aguilar-Guisado M, Givalda J, Ussetti P. Pneumonia after lung transplantation in the Resitra Cohort: a multicenter prospective study. Am J Transplant. 2007;7:1989–96.PubMedPubMedCentralCrossRefGoogle Scholar
  55. 55.
    Dudau D, Camous J, Marchand S, et al. Incidence of nosocomial pneumonia and risk of recurrence after antimicrobial therapy in critically ill lung and heart–lung transplant patients. Clin Transpl. 2014;28:27–36.CrossRefGoogle Scholar
  56. 56.
    Lumbreras C, Fernandez I, Velosa J, et al. Infectious complications following pancreatic transplantation: incidence, microbiological and clinical characteristics, and outcome. Clin Infect Dis. 1995;20:514–20.PubMedCrossRefPubMedCentralGoogle Scholar
  57. 57.
    Paya CV, Hermans PE. Bacterial infections after liver transplantation. Eur J Clin Microbiol Infect Dis. 1989;8:499–504.PubMedCrossRefPubMedCentralGoogle Scholar
  58. 58.
    Ramos A, Asensio A, Muñez E, et al. Incisional surgical infection in heart transplantation. Transpl Infect Dis. 2008;10:298–302.PubMedPubMedCentralCrossRefGoogle Scholar
  59. 59.
    Zanfi C, Cescon M, Lauro A, et al. Incidence and management of abdominal closure-related complications in adult intestinal transplantation. Transplantation. 2008;85:1607–9.PubMedCrossRefPubMedCentralGoogle Scholar
  60. 60.
    Loinaz C, Kato T, Nishida S, et al. Bacterial infections after intestine and multivisceral transplantation. The experience of the University of Miami (1994-2001). Hepatogastroenterology. 2006;53:234–42.PubMedPubMedCentralGoogle Scholar
  61. 61.
    Linhares MM, Gonzalez AM, Triviño T. Simultaneous pancreas-kidney transplantation: infectious complications and microbiological aspects. Transplant Proc. 2004;36:980–1.PubMedCrossRefPubMedCentralGoogle Scholar
  62. 62.
    Hellinger WC, Crook JE, Heckman MG, et al. Surgical site infection after liver transplantation: risk factors and association with graft loss or death. Transplantation. 2009;87:1387–93.PubMedCrossRefPubMedCentralGoogle Scholar
  63. 63.
    Michalak G, Kwiatkowski A, Bieniasz M, et al. Infectious complications after simultaneous pancreas-kidney transplantation. Transplant Proc. 2005;37:3560–3.PubMedPubMedCentralCrossRefGoogle Scholar
  64. 64.
    Perdiz LB, Furtado GH, Linhares MM, et al. Incidence and risk factors for surgical site infection after simultaneous pancreas-kidney transplantation. J Hosp Infect. 2009;72:326–31.PubMedPubMedCentralCrossRefGoogle Scholar
  65. 65.
    Shields RK, Clancy CJ, Minces L, et al. Epidemiology and outcomes of deep surgical site infections following lung transplantation. Am J Transplant. 2013;13:2137–45.PubMedPubMedCentralCrossRefGoogle Scholar
  66. 66.
    Kawecki D, Chmura A, Pacholczyk M, et al. Surgical site infections in liver recipients in the early posttransplantation period: etiological agents and susceptibility profiles. Transplant Proc. 2007;39:2800–6.PubMedCrossRefPubMedCentralGoogle Scholar
  67. 67.
    Rana MM, Sturdevant M, Patel G, Huprikar S. Klebsiella necrotizing soft tissue infections in liver transplant recipients: a case series. Transpl Infect Dis. 2013;15:157–63.CrossRefGoogle Scholar
  68. 68.
    Menezes FG, Wey SB, Peres CA, et al. Risk factors for surgical site infection in kidney transplant recipients. Infect Control Hosp Epidemiol. 2008;29(8):771–3.PubMedPubMedCentralCrossRefGoogle Scholar
  69. 69.
    Asensio A, Ramos A, Cuervas-Mons V, et al. Effect of antibiotic prophylaxis on the risk of surgical site infection in orthotopic liver transplant. Liver Transpl. 2008;14(6):799–805.PubMedCrossRefPubMedCentralGoogle Scholar
  70. 70.
    Peraira JR, Segovia J, Arroyo R, et al. High incidence of severe infections in heart transplant recipients receiving tacrolimus. Transplant Proc. 2003;35:1999–2000.PubMedCrossRefPubMedCentralGoogle Scholar
  71. 71.
    Freire MP, Antonopoulos IM, Piovesan AC, et al. Amikacin prophylaxis and risk factors for surgical site infection after kidney transplantation. Transplantation. 2015;99:521–7.PubMedCrossRefPubMedCentralGoogle Scholar
  72. 72.
    Freire MP, Soares Oshiro IC, Bonazzi PR, et al. Surgical site infections in liver transplant recipients in the model for end-stage liver disease era: an analysis of the epidemiology, risk factors, and outcomes. Liver Transpl. 2013;19:1011–9.CrossRefGoogle Scholar
  73. 73.
    Zuckermann A, Barten MJ. Surgical wound complications after heart transplantation. Transpl Int. 2011;24:627–36.PubMedCrossRefPubMedCentralGoogle Scholar
  74. 74.
    Kuppahally S, Al-Khaldi A, Weisshaar D, et al. Wound healing complications with de novo sirolimus versus mycophenolate mofetil-based regimen in cardiac transplant recipients. Am J Transplant. 2006;6:986–92.PubMedCrossRefPubMedCentralGoogle Scholar
  75. 75.
    Husain S, Chan KM, Palmer SM, et al. Bacteremia in lung transplant recipients in the current era. Am J Transplant. 2006;6:3000–7.PubMedCrossRefPubMedCentralGoogle Scholar
  76. 76.
    Wagener MM, Yu VL. Bacteremia in transplant recipients: a prospective study of demographics, etiologic agents, risk factors, and outcomes. Am J Infect Control. 1992;20:239–47.PubMedCrossRefPubMedCentralGoogle Scholar
  77. 77.
    Rodriguez C, Munoz P, Rodriguez-Creixems M, et al. Bloodstream infections among heart transplant recipients. Transplantation. 2006;81:384–91.PubMedPubMedCentralCrossRefGoogle Scholar
  78. 78.
    Al-Hasan MN, Razonable RR, Eckel-Passowd JE, et al. Incidence rate and outcome of gram-negative bloodstream infection in solid organ transplant recipients. Am J Transplant. 2009;9:835–43.PubMedCrossRefPubMedCentralGoogle Scholar
  79. 79.
    Singh N, Gayowski T, Wagener MM, et al. Bloodstream infections in liver transplant recipients receiving tacrolimus. Clin Transpl. 1997;11:275–81.Google Scholar
  80. 80.
    Ye QF, Zhao J, Wan QQ, et al. Frequency and clinical outcomes of ESKAPE bacteremia in solid organ transplantation and the risk factors for mortality. Transpl Infect Dis. 2014;16:767–74.CrossRefGoogle Scholar
  81. 81.
    Blennow O, Ljungman P, Sparrelid E, Mattsson J, Remberger M. Incidence, risk factors, and outcome of bloodstream infections during the pre-engraftment phase in 521 allogeneic hematopoietic stem cell transplantations. Transpl Infect Dis. 2014;16:106–14.PubMedPubMedCentralCrossRefGoogle Scholar
  82. 82.
    Wang CH, Chang FY, Chao TY, Kao WY, Ho CL, Chen YC, et al. Characteristics comparisons of bacteremia in allogeneic and autologous hematopoietic stem cell-transplant recipients with levofloxacin prophylaxis and influence on resistant bacteria emergence. J Microbiol Immunol Infect. 2016;pii: S1684–1182(16)30003–30002.Google Scholar
  83. 83.
    Poutsiaka DD, Price LL, Ucuzian A, Chan GW, Miller KB, Snydman DR. Blood stream infection after hematopoietic stem cell transplantation is associated with increased mortality. Bone Marrow Transplant. 2007;40:63–70.PubMedCrossRefPubMedCentralGoogle Scholar
  84. 84.
    Shigematsu A, Yamamoto S, Sugita J, et al. Increased risk of bacterial infection after engraftment in patients treated with allogeneic bone marrow transplantation following reduced-intensity conditioning regimen. Transpl Infect Dis. 2010;12:412–20.PubMedCrossRefPubMedCentralGoogle Scholar
  85. 85.
    Hong J, Moon SM, Ahn HK, et al. Comparison of characteristics of bacterial bloodstream infection between adult patients with allogeneic and autologous hematopoietic stem cell transplantation. Biol Blood Marrow Transplant. 2013;19:988–99.CrossRefGoogle Scholar
  86. 86.
    Qureshi ZA, Paterson DL, Pakstis DL, et al. Risk factors and outcome of extended-spectrum beta-lactamase producing bloodstream infections. Int J Antimicrob Agents. 2011;37(1):26–32.PubMedCrossRefPubMedCentralGoogle Scholar
  87. 87.
    Qureshi ZA, Paterson DL, Peleg AY, et al. Clinical characteristics of bacteremia caused by extended-spectrum beta-lactamase-producing Enterobacteriaceae in the era of CTX-M-type and KPC-type beta-lactamases. Clin Microbiol Infect. 2012;18(9):887–93.PubMedCrossRefPubMedCentralGoogle Scholar
  88. 88.
    Mills JP, Talati NJ, Alby K, Han JH. The epidemiology of Carbapenem-Resistant Klebsiella pneumoniae colonization and infection among long-term acute care hospital residents. Infect Control Hosp Epidemiol. 2016;37:55–60.PubMedCrossRefPubMedCentralGoogle Scholar
  89. 89.
    Linares L, Cervera C, Hoyo I, et al. Klebsiella pneumoniae infection in solid organ transplant recipients: epidemiology and antibiotic resistance. Transplant Proc. 2010;42:2941–3.PubMedPubMedCentralCrossRefGoogle Scholar
  90. 90.
    Patel G, Huprikar S, Factor SH, et al. Outcomes of carbapenem-resistant Klebsiella pneumoniae infection and the impact of antimicrobial and adjunctive therapies. Infect Control Hosp Epidemiol. 2008;29:1099–106.PubMedCrossRefPubMedCentralGoogle Scholar
  91. 91.
    Schwaber MJ, Navon-Venezia S, Kaye KS, et al. Clinical and economic impact of bacteremia with extended-spectrumβ –lactamase- producing Enterobacteriaceae. Antimicrob Agents Chemother. 2006;50:1257–62.PubMedPubMedCentralCrossRefGoogle Scholar
  92. 92.
    Lee SY, Kotapati S, Kuti JL, et al. Impact of extended-spectrum β-lactamase–producing Escherichia coli and Klebsiella species on clinical outcomes and hospital costs: a matched cohort study. Infect Control Hosp Epidemiol. 2006;27:1226–32.PubMedCrossRefPubMedCentralGoogle Scholar
  93. 93.
    Bodro M, Sabé N, Tubau F, et al. Risk factors and outcomes of bacteremia caused by drug-resistant ESKAPE pathogens in solid-organ transplant recipients. Transplantation. 2013;96:843–9.PubMedCrossRefPubMedCentralGoogle Scholar
  94. 94.
    Bergamasco MD, Barroso Barbosa M, de Oliveira GD, et al. Infection with Klebsiella pneumoniae carbapenemase (KPC)-producing K. pneumoniae in solid organ transplantation. Transpl Infect Dis. 2012;14(2):198–205.PubMedPubMedCentralCrossRefGoogle Scholar
  95. 95.
    Paterson DL, Singh N, Rihs JD, et al. Control of an outbreak of infection due to extended-spectrum beta-lactamase-producing Escherichia coli in a liver transplantation unit. Clin Infect Dis. 2001;33:126–8.PubMedCrossRefPubMedCentralGoogle Scholar
  96. 96.
    Rebuck JA, Olsen KM, Fey PD, et al. 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;31:1368–72.CrossRefGoogle Scholar
  97. 97.
    Martins IS, Moreira BM, Riley LW, et al. Outbreak of extended-spectrum beta-lactamase-producing Klebsiella pneumoniae infection among renal transplant recipients. J Hosp Infect. 2006;64:305–8.PubMedCrossRefPubMedCentralGoogle Scholar
  98. 98.
    Zárate MS, Gales AC, Picão RC, et al. Outbreak of OXY-2 producing Klebsiella oxytoca in a renal transplant unit. J Clin Microbiol. 2008;46:2099–101.PubMedPubMedCentralCrossRefGoogle Scholar
  99. 99.
    Mathers AJ, Cox HL, Bonatti H, et al. Fatal cross infection by carbapenem-resistant Klebsiella in two liver transplant recipients. Transpl Infect Dis. 2009;11(3):257–65.PubMedPubMedCentralCrossRefGoogle Scholar
  100. 100.
    Lai CC, Lin TL, Tseng SP, et al. Pelvic abscess caused by New Delhi metallo-beta-lactamase-1-producing Klebsiella oxytoca in Taiwan in a patient who underwent renal transplantation in China. Diagn Microbiol Infect Dis. 2011;71(4):474–5.PubMedCrossRefPubMedCentralGoogle Scholar
  101. 101.
    Mouloudi E, Protonotariou E, Zagorianou A, et al. Bloodstream infections caused by metallo-beta-lactamase/Klebsiella pneumoniae carbapenemase-producing K. pneumoniae among intensive care unit patients in Greece: risk factors for infection and impact of type of resistance on outcomes. Infect Control Hosp Epidemiol. 2010;31(12):1250–6.PubMedCrossRefPubMedCentralGoogle Scholar
  102. 102.
    Pouch SM, Kubin CJ, Satlin MJ, et al. Epidemiology and outcomes of carbapenem-resistant Klebsiella pneumonia bacteriuria in kidney transplant recipients. Transpl Infect Dis. 2015;17:800–9.PubMedPubMedCentralCrossRefGoogle Scholar
  103. 103.
    Pereira MR, Scully BF, Pouch SM, et al. Risk factors and outcomes of carbapenem-resistant Klebsiella pneumonia infections in liver transplant recipients. Liver Transpl. 2015;21:1511–9.PubMedPubMedCentralCrossRefGoogle Scholar
  104. 104.
    Simkins J, Muggia V, Cohen HW, Minamoto GY. Carbapenem-resistant Klebsiella pneumoniae infections in kidney transplant recipients: a case-control study. Transpl Infect Dis. 2014;16:775–82.PubMedCrossRefPubMedCentralGoogle Scholar
  105. 105.
    Balletto E, Mikulska M. Bacterial infections in hematopoietic stem cell transplant recipients. Mediterr J Hematol Infect Dis. 2015;7(1):e2015045.PubMedPubMedCentralCrossRefGoogle Scholar
  106. 106.
    Zając-Spychała O, Wachowiak J, Pieczonka A, Siewiera K, Frączkiewicz J, Kałwak K, et al. Bacterial infections in pediatric hematopoietic stem cell transplantation recipients: incidence, epidemiology, and spectrum of pathogens: report of the Polish Pediatric Group for hematopoietic stem cell transplantation. Transpl Infect Dis. 2016;18(5):690–8.PubMedCrossRefPubMedCentralGoogle Scholar
  107. 107.
    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.PubMedCrossRefPubMedCentralGoogle Scholar
  108. 108.
    Satlin MJ, Jenkins SG, Walsh TJ. The global challenge of carbapenem-resistant Enterobacteriaceae in transplant recipients and patients with hematologic malignancies. Clin Infect Dis. 2014;58:1274–83.PubMedPubMedCentralCrossRefGoogle Scholar
  109. 109.
    Baker TM, Satlin MJ. The growing threat of multidrug-resistant gram-negative infections in patients with hematologic malignancies. Leuk Lymphoma. 2016;57:2245–58.PubMedPubMedCentralCrossRefGoogle Scholar
  110. 110.
    Iredell J, Brown J, Tagg K. Antibiotic resistance in Enterobacteriaceae: mechanisms and clinical implications. BMJ. 2016;352:h6420.PubMedCrossRefPubMedCentralGoogle Scholar
  111. 111.
    Nordmann P, Naas T, Poirel L. Global spread of Carbapenemase-producing Enterobacteriaceae. Emerg Infect Dis. 2011;17:1791–8.PubMedPubMedCentralCrossRefGoogle Scholar
  112. 112.
    Blumberg E, Green M, Covington SG, et al. Donor derived bacterial infections: report from the Disease Transmission Advisory Committee (DTAC). In: 48th Annual meeting of the Infectious Diseases Society of America. Vancouver. 2010. Available at
  113. 113.
    Watkins AC, Vedula GV, Horan J, et al. The deceased organ donor with an “open abdomen”: proceed with caution. Transpl Infect Dis. 2012;14:311–5.PubMedCrossRefPubMedCentralGoogle Scholar
  114. 114.
    Chung W, Pascoe N, Heseltine G, Qazi Y, Bower WA, Kuehnert M, Wise M, Zheteyeva Y. Transmission of multidrug-resistant Escherichia coli through kidney transplantation – California and Texas, 2009. MMWR. 2010;59(50):1642–6.Google Scholar
  115. 115.
    Mularoni A, Bertani A, Vizzini G, et al. Outcome of transplantation using organs from donors infected or colonized with carbapenem-resistant gram-negative bacteria. Am J Transplant. 2015;15:2674–82.PubMedCrossRefPubMedCentralGoogle Scholar
  116. 116.
    Mills JP, Wilck MB, Weikert BC, et al. Successful treatment of a disseminated infection with extensively drug-resistant Klebsiella pneumoniae in a liver transplant recipient with a fosfomycin-based multidrug regimen. Transpl Infect Dis. 2016;18:777–81.PubMedPubMedCentralCrossRefGoogle Scholar
  117. 117.
    Giani T, Conte V, Mandalà S, et al. Cross-infection of solid organ transplant recipients by a multidrug-resistant Klebsiella pneumoniae isolate producing the OXA-48 carbapenemase, likely derived from a multiorgan donor. J Clin Microbiol. 2014;52:2702–5.PubMedPubMedCentralCrossRefGoogle Scholar
  118. 118.
    Goldberg E, Bishara J, Lev S, et al. Transplantation from a donor colonized with a multidrug-resistant organism: a case report. Transpl Infect Dis. 2012;14(3):296–9.CrossRefGoogle Scholar
  119. 119.
    Ariza-Heredia EJ, Patel R, Blumberg EA, et al. Outcomes of transplantation using organs from a donor infected with Klebsiella pneumoniae carbapenemase (KPC)-producing K. pneumoniae. Transpl Infect Dis. 2012;14(3):229–36.CrossRefGoogle Scholar
  120. 120.
    Ison MG, Grossi P. AST Infectious Diseases Community of Practice. Donor-derived infections in solid organ transplantation. Am J Transplant. 2013;13(Suppl 4):22–30.PubMedCrossRefPubMedCentralGoogle Scholar
  121. 121.
    Miller R, Covington S, Taranto S, et al. Communication gaps associated with donor-derived infections. Am J Transplant. 2015;15:259–64.PubMedCrossRefPubMedCentralGoogle Scholar
  122. 122.
  123. 123.
    Craven DE. 2005 IDSA/ATS Hospital-acquired pneumonia guidelines: new principles for improving management. Johns Hopkins Adv Stud Med Proc. 2006;6(6C):S541–8.Google Scholar
  124. 124.
    Chan CC, Abi-Saleh WJ, Arroliga AC, et al. Diagnostic yield and therapeutic impact of flexible bronchoscopy in lung transplant recipients. J Heart Lung Transplant. 1996;15(2):196–205.PubMedPubMedCentralGoogle Scholar
  125. 125.
    Harris B, Geyer AI. Diagnostic evaluation of pulmonary abnormalities in patients with hematologic malignancies and hematopoietic cell transplantation. Clin Chest Med. 2017;38:317–31.PubMedCrossRefPubMedCentralGoogle Scholar
  126. 126.
    Kupeli E, Akcay S, Ulubay G, Ozyurek BA, Ozdemirel TS, Haberal M. Diagnostic utility of flexible bronchoscopy in recipients of solid organ transplants. Transplant Proc. 2011;43:543–6.PubMedCrossRefPubMedCentralGoogle Scholar
  127. 127.
    Fagon JY, Chastre J, Wolff M, et al. Invasive and noninvasive strategies for management of suspected ventilator-associated pneumonia. A randomized trial. Ann Intern Med. 2000;132:621–30.PubMedCrossRefPubMedCentralGoogle Scholar
  128. 128.
    Origüen J, López-Medrano F, Fernández-Ruiz M, et al. Should asymptomatic bacteriuria be systematically treated in kidney transplant recipients? Results from a randomized controlled trial. Am J Transplant. 2016;16:2943–53.PubMedCrossRefPubMedCentralGoogle Scholar
  129. 129.
  130. 130.
    van Duin D, van Delden C. AST Infectious Diseases Community of Practice. Multidrug-resistant gram-negative bacteria infections in solid organ transplantation. Am J Transplant. 2013;13(Suppl 4):31–41.PubMedPubMedCentralCrossRefGoogle Scholar
  131. 131.
    van Duin D, Cober E, Richter SS, et al. Impact of therapy and strain type on outcomes in urinary tract infections caused by carbapenem-resistant Klebsiella pneumoniae. J Antimicrob Chemother. 2015;70:1203–11.PubMedPubMedCentralGoogle Scholar
  132. 132.
    Souli M, Rekatsina PD, Chryssouli Z, et al. Does the activity of the combination of imipenem and colistin in vitro exceed the problem of resistance in metallo-beta-lactamase-producing Klebsiella pneumoniae isolates? Antimicrob Agents Chemother. 2009;53:2133–35.1.PubMedPubMedCentralCrossRefGoogle Scholar
  133. 133.
    Urban C, Mariano N, Rahal JJ. In vitro double and triple bactericidal activities of doripenem, polymyxin B, and rifampin against multidrugresistant Acinetobacter baumannii, Pseudomonas aeruginosa, Klebsiella pneumoniae, and Escherichia coli. Antimicrob Agents Chemother. 2010;54:2732–4.PubMedPubMedCentralCrossRefGoogle Scholar
  134. 134.
    Lin KH, Chuang YC, Lee SH, Yu WL. In vitro synergistic antimicrobial effect of imipenem and colistin against an isolate of multidrugresistant Enterobacter cloacae. J Microbiol Immunol Infect. 2010;43:317–22.PubMedCrossRefPubMedCentralGoogle Scholar
  135. 135.
    Falagas ME, Rafailidis PI, Ioannidou E, et al. Colistin therapy for microbiologically documented multidrug-resistant gram-negative bacterial infections: a retrospective cohort study of 258 patients. Int J Antimicrob Agents. 2010;35:194–9.PubMedCrossRefPubMedCentralGoogle Scholar
  136. 136.
    Kasiakou SK, Michalopoulos A, Soteriades ES, et al. Combination therapy with intravenous colistin for management of infections due to multidrug-resistant gram-negative bacteria in patients without cystic fibrosis. Antimicrob Agents Chemother. 2005;49:3136–46.PubMedPubMedCentralCrossRefGoogle Scholar
  137. 137.
    Michalopoulos AS, Tsiodras S, Rellos K, et al. Colistin treatment in patients with ICU-acquired infections caused by multiresistant gram-negative bacteria: the renaissance of an old antibiotic. Clin Microbiol Infect. 2005;11:115–21.PubMedCrossRefPubMedCentralGoogle Scholar
  138. 138.
    Yacoub R, Akl NK. Urinary tract infections and asymptomatic bacteriuria in renal transplantrecipients. J Glob Infect Dis. 2011;3(4):383–9.PubMedPubMedCentralCrossRefGoogle Scholar
  139. 139.
    Nicolle LE, Bradley S, Colgan R, Rice JC, Schaeffer A, Hooton TM. Infectious Diseases Society of America; American Society of Nephrology; American Geriatric Society. Infectious Diseases Society of America guidelines for the diagnosis and treatment of asymptomatic bacteriuria in adults. Clin Infect Dis. 2005;40:643–54.PubMedPubMedCentralCrossRefGoogle Scholar
  140. 140.
    Freifeld AG, Freifeld AG, Bow EJ, 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:e56–93.PubMedPubMedCentralCrossRefGoogle Scholar
  141. 141.
    Tolkoff-Rubin NE, Cosimi AB, Russell PS, et al. A controlled study of trimethoprim-sulfamethoxazole prophylaxis of urinary tract infection in renal transplant recipients. Rev Infect Dis. 1982;4:614–8.PubMedPubMedCentralCrossRefGoogle Scholar
  142. 142.
    Fox BC, Sollinger HW, Belzer FO, Maki DG. A prospective, randomized, double-blind study of trimethoprimsulfamethoxazole for prophylaxis of infection in renal transplantation: clinical efficacy, absortion of trimethoprimsulfamethoxazole, effects on the microflora, and the cost-benefit of prophylaxis. Am J Med. 1990;89:255–74.CrossRefGoogle Scholar
  143. 143.
    Resino E, San-Juan R, Aguado JM. Selective intestinal decontamination for the prevention of early bacterial infections after liver transplantation. World J Gastroenterol. 2016;22:5950–7.PubMedPubMedCentralCrossRefGoogle Scholar
  144. 144.
    Badger IL, Crosby HA, Kong KL, et al. Is selective bowel decontamination of the digestive tract beneficial in liver transplant patients? Interim results of a prospective, randomized trial. Transplant Proc. 1991;23:1460–1.PubMedPubMedCentralGoogle Scholar
  145. 145.
    Smith SD, Jackson RJ, Hannakan CJ, et al. Selective decontamination in pediatric liver transplants. A randomized prospective study. Transplantation. 1993;55:1306–9.PubMedCrossRefPubMedCentralGoogle Scholar
  146. 146.
    Safdar N, Said A, Lucey MR. The role of selective digestive decontamination for reducing infection in patients undergoing liver transplantation: a systematic review and meta-analysis. Liver Transpl. 2004;10:817–27.PubMedCrossRefPubMedCentralGoogle Scholar
  147. 147.
    Wingard JR, Hsu J, Hiemenz JW. Hematopoietic stem cell transplantation: an overview of infection risks and epidemiology. Infect Dis Clin North Am. 2010;24(2):257–72.PubMedCrossRefPubMedCentralGoogle Scholar
  148. 148.
    Bert F, Larroque B, Paugam-Burtz C, et al. Pretransplant fecal carriage of extended-spectrum β-lactamase-producing Enterobacteriaceae and infection after liver transplant, France. Emerg Infect Dis. 2012;18:908–16.PubMedPubMedCentralCrossRefGoogle Scholar
  149. 149.
    Lübbert C, Becker-Rux D, Rodloff AC, et al. Colonization of liver transplant recipients with KPC-producing Klebsiella pneumoniae is associated with high infection rates and excess mortality: a case-control analysis. Infection. 2014;42:309–16.PubMedCrossRefGoogle Scholar
  150. 150.
    Ullmann AJ, Schmidt-Hieber M, Bertz H, et al. Infectious diseases in allogeneic haematopoietic stem cell transplantation: prevention and prophylaxis strategy guidelines 2016. Ann Hematol. 2016;95(9):1435–55.PubMedPubMedCentralCrossRefGoogle Scholar
  151. 151.
    Facility Guidance for Control of Carbapenem-resistant Enterobacteriaceae (CRE) – November 2015 Update CRE Toolkit.
  152. 152.
    Sellin JH. The pathophysiology of diarrhea. Clin Transplant. 2001;15(Supple 4):29–35.Google Scholar
  153. 153.
    Angarone M, Ison MG. Diarrhea in solid organ transplant recipients. Curr Opin Infect Dis. 2015;28:308–16.PubMedCrossRefPubMedCentralGoogle Scholar
  154. 154.
    Arslan H, Inci EK, Azap OK, et al. Etiologic agents of diarrhea in solid organ recipients. Transpl Infect Dis. 2007;9:270–5.CrossRefGoogle Scholar
  155. 155.
    Dhar JM, Al-Khader AA, Al-Sulaiman M, et al. Non-typhoid Salmonella in renal transplant recipients: a report of twenty cases and review of the literature. Q J Med. 1991;78:235–50.PubMedPubMedCentralGoogle Scholar
  156. 156.
    Lübbert C. Antimicrobial therapy of acute diarrhoea: a clinical review. Expert Rev Anti Infect Ther. 2016;14(2):193–206.PubMedCrossRefPubMedCentralGoogle Scholar
  157. 157.
    Washington JA 2nd, Birk RJ, Ritts RE Jr. Bacteriologic and epidemiologic characteristics of Enterobacter hafniae and Enterobacter liquefaciens. J Infect Dis. 1971;124:379–86.PubMedCrossRefPubMedCentralGoogle Scholar
  158. 158.
    Günthard H, Pennekamp A. Clinical significance of extraintestinal Hafnia alvei isolates from 61 patients and review of the literature. Clin Infect Dis. 1996;22:1040–5.PubMedCrossRefPubMedCentralGoogle Scholar
  159. 159.
    Barry JW, Dominguez EA, Boken DJ, Preheim LC. Hafnia alvei infection after liver transplantation. Clin Infect Dis. 1997;24:1263–4.PubMedCrossRefPubMedCentralGoogle Scholar
  160. 160.
    Benito MH, Hernández RS, Fernàndez-Reyes MJ, Hernando S. Sepsis induced by Hafnia alvei in a kidney transplant patient. Nefrologia. 2008;28:470–1.PubMedPubMedCentralGoogle Scholar
  161. 161.
    Cardile AP, Forbes D, Cirigliano V, et al. Hafnia alvei pyelonephritis in a renal transplant recipient: case report and review of an under-recognized nosocomial pathogen. Transpl Infect Dis. 2011;13:407–10.PubMedCrossRefPubMedCentralGoogle Scholar
  162. 162.
    Shubov A, Jagannathan P, Chin-Hong PV. Pantoea agglomerans pneumonia in a heart-lung transplant recipient: case report and a review of an emerging pathogen in immunocompromised hosts. Transpl Infect Dis. 2011;13(5):536–9.PubMedCrossRefPubMedCentralGoogle Scholar
  163. 163.
    Cheruvattath R, Balan V, Stewart R, et al. Kluyvera co-infection in two solid organ transplant recipients: an emerging pathogen or a colonizer bystander? Transpl Infect Dis. 2007;9(1):83–6.PubMedCrossRefPubMedCentralGoogle Scholar

Copyright information

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

Authors and Affiliations

  • Kathryn Whitaker
    • 1
  • Valerie Cluzet
    • 2
  • Emily A. Blumberg
    • 1
    Email author
  1. 1.Division of Infectious DiseasesHospital of the University of Pennsylvania, Perelman School of Medicine at the University of PennsylvaniaPhiladelphiaUSA
  2. 2.Health Quest Medical Practice, Department of Infectious DiseasesPoughkeepsieUSA

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