Healthcare Infection Healthcare Infection Society
Official Journal of the Australasian College for Infection Prevention and Control
RESEARCH ARTICLE

Acute vancomycin-resistant enterococcal bacteraemia outbreak analysis in haematology patients: a case-control study

Ian Gassiep A B F , Mark Armstrong A B , Zoe Van Havre E , Sanmarie Schlebusch B C , Joseph McCormack A B C and Paul Griffin A B C D
+ Author Affiliations
- Author Affiliations

A Department of Infectious Diseases, Mater Health Services and Mater Medical Research Institute, South Brisbane, Qld 4101, Australia.

B School of Medicine, University of Queensland, Mater Hospital Campus, South Brisbane, Qld 4101, Australia.

C Department of Microbiology Mater Health Services and Mater Medical Research Institute, South Brisbane, Qld 4101, Australia.

D The QIMR Berghofer Medical Research Institute, Royal Brisbane and Women’s Hospital, Brisbane, Qld 4006, Australia.

E Queensland University of Technology, Brisbane, Qld 4000, Australia.

F Corresponding author. Email: ian.gassiep@gmail.com

Healthcare Infection 20(4) 115-123 https://doi.org/10.1071/HI15013
Submitted: 27 June 2015  Accepted: 17 August 2015   Published: 7 September 2015

Abstract

Introduction: We report a retrospective case-control series of a vancomycin-resistant Enterococcus faecium (VRE) bacteraemia outbreak at a tertiary metropolitan hospital in Queensland, Australia. The outbreak occurred on a haematology ward between 8 and 14 February 2014, 6 weeks after a ward relocation. The aim was to determine risk factors related to progression from colonisation with VRE to bacteraemia.

Methods: The cases were patients with haematological malignancy and proven catheter-related VRE bacteraemia. Matched controls were selected from the same ward with similar underlying haematological diagnoses and proven gastrointestinal VRE colonisation without invasive infection.

Results: This study suggests that female sex, recent administration of total parenteral nutrition, right-sided catheter placement with odds ratios (OR) 1.99, gastrointestinal disruption (OR: 1.91), and dexamethasone administration (OR: 2.37) are potential risk factors for progression from colonisation to infection. Notably, given the small sample size, the 95% confidence intervals are wide ranging from 0.02 to 222.

Conclusion: While progression from colonisation with VRE to invasive disease is likely to be a complex multifactorial process, the results of this study suggest certain clinical variables that warrant enhanced vigilance to reduce this occurrence. Interestingly, recent relocation of the haematology ward may play a significant role in this outbreak. This study highlights the importance of good infection control practice and the need for additional studies to further delineate risk factors for invasive VRE infection.


References

[1]  Kamarulzaman A, Tosolini F, Boquest AL, Geddes JE, Richards MJ. Vancomycin-resistant Enterococcus faecium in a liver transplant recipient. Australian and New Zealand Journal of Medicine 1995; 25 560

[2]  Whitby M, Jennings A, Allen A, Sherlock K, Paterson D. Isolation of vancomycin-resistant enterococci in Queensland, case 1. Communicable Diseases Intelligence 1996; 20 400–1.

[3]  Bell J, Turnbridge J, Coombs G, O’Brien F. Emergence and epidemiology of vancomycin-resistant enterococci in Australia. Communicable Diseases Intelligence 1998; 22 249–52.
| 1:STN:280:DyaK1M%2FktFShsw%3D%3D&md5=3cc0a1a5a66267a9ba68fc8690c579e8CAS | 9823687PubMed |

[4]  Coombs GW, Pearson JC, Daley DA, Le T, Robinson JO, Gottlieb T. Australian Group on Antimicrobial Resistance (AGAR) Australian Enterococcal Sepsis Outcome Program (AESOP) Annual Report 2013. AGAR; 2013. Available from: http://www.agargroup.org/publications [Verified January 2015]

[5]  Bearman GML, Wenzel RP. Bacteremias: a leading cause of death. Archives of Medical Research 2005; 36 646–59.
Bacteremias: a leading cause of death.CrossRef |

[6]  Deshpande LM, Fritsche TR, Moet GJ, Biedenbach DJ, Jones RN. Antimicrobial resistance and molecular epidemiology of vancomycin-resistant enterococci from North America and Europe: a report from the SENTRY antimicrobial surveillance program. Diagnostic Microbiology and Infectious Disease 2007; 58 163–70.
Antimicrobial resistance and molecular epidemiology of vancomycin-resistant enterococci from North America and Europe: a report from the SENTRY antimicrobial surveillance program.CrossRef | 1:CAS:528:DC%2BD2sXmtlansL4%3D&md5=90a0158f04b3fd38c57c32e2a88b8582CAS | 17368801PubMed |

[7]  Coombs GW, Pearson JC, Daley DA, Le T, Robinson OJ, Gottlieb T, Howden BP, Johnson PDR, Bennett CM, Stinear TP, Turnidge JD. Molecular epidemiology of enterococcal bacteremia in Australia. Journal of Clinical Microbiology 2014; 52 897–905.
Molecular epidemiology of enterococcal bacteremia in Australia.CrossRef | 24391201PubMed |

[8]  Willems RJL, Top J, van Santen M, Robinson DA, Coque TM, Baquero F, Grundmann H, Bonten MJM. Global spread of vancomycin resistant Enterococcus faecium from distinct nosocomial genetic complex. Emerging Infectious Diseases 2005; 11 821–8.
Global spread of vancomycin resistant Enterococcus faecium from distinct nosocomial genetic complex.CrossRef | 1:CAS:528:DC%2BD2MXlsFSit7s%3D&md5=1fefb31413473f46173f8009cfaaa8daCAS |

[9]  Huycke MM, Sahme DF, Gilmore MS. Multiple-drug resistant enterococci: the nature of the problem and an agenda for the future. Emerging Infectious Diseases 1998; 4 239–49.
Multiple-drug resistant enterococci: the nature of the problem and an agenda for the future.CrossRef | 1:STN:280:DyaK1c3osVaitg%3D%3D&md5=b3b98ac26343e4a3ba43b957ff236f47CAS | 9621194PubMed |

[10]  Cetinkaya Y, Falk P, Mayhall CG. Vancomycin-resistant enterococci. Clinical Microbiology Reviews 2000; 13 686–707.
Vancomycin-resistant enterococci.CrossRef | 1:CAS:528:DC%2BD3cXnslCgtbg%3D&md5=4567b4b92498b3a84f4de911f4e65de0CAS | 11023964PubMed |

[11]  Pinholt M, Ostergaard C, Arpi M, Bruun NE, Schonheyder HC, Gradel KO, Sogaard M, Knudsen JD. Incidence, clinical characteristics and 30-day mortality of enterococcal bacteraemia in Denmark 2006–2009: a population-based cohort study. Clinical Microbiology and Infection 2014; 20 145–51.
Incidence, clinical characteristics and 30-day mortality of enterococcal bacteraemia in Denmark 2006–2009: a population-based cohort study.CrossRef | 1:CAS:528:DC%2BC2cXpsF2msg%3D%3D&md5=3144c683306822e1be87419957626323CAS | 23647880PubMed |

[12]  Camins BC, Farley MM, Jernigan JJ, Ray SM, Steinburg JP, Blumberg HM. A population-based investigation of invasive vancomycin-resistant enterococcus infection in metropolitan Atlanta, Georgia, and predictors of mortality. Infection Control and Hospital Epidemiology 2007; 28 983–91.
A population-based investigation of invasive vancomycin-resistant enterococcus infection in metropolitan Atlanta, Georgia, and predictors of mortality.CrossRef | 17620248PubMed |

[13]  Griffin PM, Price GR, Schooneveldt JM, Schebusch S, Tilse MH, Urbanski T, Hamilton B, Venter D. Use of matrix-assisted laser desorption ionization-time of flight mass spectrometry to identify vancomycin-resistent enterococci and investigate the epidemiology of an outbreak. Journal of Clinical Microbiology 2012; 50 2918–31.
Use of matrix-assisted laser desorption ionization-time of flight mass spectrometry to identify vancomycin-resistent enterococci and investigate the epidemiology of an outbreak.CrossRef | 1:CAS:528:DC%2BC38XhsVarsb3E&md5=860e1ce8d691daad031dbbd95f858e66CAS | 22740710PubMed |

[14]  Montecalvo MA, Horowitz H, Gedris C, Carbonaro C, Tenover FC, Issah A, Cook P, Wormser GP. Outbreak of vancomycin, ampicillin, and aminoglycoside-resistant Enterococcus faecium bacteremia in an adult oncology unit. Antimicrobial Agents and Chemotherapy 1994; 38 1363–7.
Outbreak of vancomycin, ampicillin, and aminoglycoside-resistant Enterococcus faecium bacteremia in an adult oncology unit.CrossRef | 1:STN:280:DyaK2cznvFOqsA%3D%3D&md5=9b2c8138174fa47c05b77fb6384c3c8cCAS | 8092838PubMed |

[15]  Timmers GJ, van der Zwet W, Simoons-Smit IM, Savelkoul PHM, Meester HHM, Vandenbroucke-Grauls CMJE. Outbreak of vancomycin-resistant Enterococcus faecium in a haematology unit: risk factor assessment and successful control of the epidemic. British Journal of Haematology 2002; 116 826–33.
Outbreak of vancomycin-resistant Enterococcus faecium in a haematology unit: risk factor assessment and successful control of the epidemic.CrossRef | 11886387PubMed |

[16]  Bhavnani SM, Drake JA, Forrest A, Deinhart JA, Jones RN, Biedenbach DJ, Ballow CH. A nationwide, multicenter, case-control study comparing risk factors, treatment, and outcome for vancomycin-resistant and -susceptible enterococcal bacteremia. Diagnostic Microbiology and Infectious Disease 2000; 36 145–58.
A nationwide, multicenter, case-control study comparing risk factors, treatment, and outcome for vancomycin-resistant and -susceptible enterococcal bacteremia.CrossRef | 1:STN:280:DC%2BD3c7psFGrsQ%3D%3D&md5=fb134a0efb3a826955ee958c1837f4ffCAS | 10729656PubMed |

[17]  Lautenbach E, Bilker WB, Brennan PJ. Enterococcal bacteremia: risk factors for vancomycin resistance and predictors of mortality. Infection Control and Hospital Epidemiology 1999; 20 318–23.
Enterococcal bacteremia: risk factors for vancomycin resistance and predictors of mortality.CrossRef | 1:STN:280:DyaK1M3nslCmsg%3D%3D&md5=17b00cac67de598c3901bb081a62a5e1CAS | 10349947PubMed |

[18]  Song X, Srinivasan A, Plaut D, Perl TM. Effect of nosocomial vancomycin-resistant enterococcal bacteremia on mortality, length of stay, and costs. Infection Control and Hospital Epidemiology 2003; 24 251–6.
Effect of nosocomial vancomycin-resistant enterococcal bacteremia on mortality, length of stay, and costs.CrossRef | 12725353PubMed |

[19]  Cheah AL, Spleman T, Liew D, Peel T, Howden BP, Spelman D, Grayson ML, Nation RL, Kong DCM. Enterococcal bacteraemia: factors influencing mortality, length of stay and costs of hospitalization. Clinical Microbiology and Infection 2013; 19 E181–9.
Enterococcal bacteraemia: factors influencing mortality, length of stay and costs of hospitalization.CrossRef | 1:STN:280:DC%2BC3sznt1KltQ%3D%3D&md5=6e3e5267d683232f545c25b9f2eadc84CAS | 23398607PubMed |

[20]  Cordova SP, Heath CH, McGechie DB, Keil AD, Beers MY, Riley TV. Methicillin-resistant Staphylococcus aureus bacteraemia in Western Australian teaching hospitals, 1997–1999: risk factors, outcomes and implications for management. The Journal of Hospital Infection 2004; 56 22–8.
Methicillin-resistant Staphylococcus aureus bacteraemia in Western Australian teaching hospitals, 1997–1999: risk factors, outcomes and implications for management.CrossRef | 1:STN:280:DC%2BD2c%2FhtVWjtQ%3D%3D&md5=be121a0869a0f83526a1c694644024acCAS | 14706267PubMed |

[21]  Chavers LS, Moser SA, Benjamin WH, Banks SE, Steinhauer JR, Smith AM, Johnson CN, Funkhouser E, Chavers LP, Stamm AM, Waites KB. Vancomycin-resistant enterococci: 15 years and counting. The Journal of Hospital Infection 2003; 53 159–71.
Vancomycin-resistant enterococci: 15 years and counting.CrossRef | 1:STN:280:DC%2BD3s7htVyqtw%3D%3D&md5=d6470f23f546925e192f990c0db2b1e8CAS | 12623315PubMed |

[22]  Zaas AK, Song X, Tucker P, Perl TM. Risk factors for development of vancomycin-resistant enterococcal bloodstream infection in patients with cancer who are colonized with vancomycin-resistant enterococci. Clinical Infectious Diseases 2002; 35 1139–46.
Risk factors for development of vancomycin-resistant enterococcal bloodstream infection in patients with cancer who are colonized with vancomycin-resistant enterococci.CrossRef | 12410472PubMed |

[23]  Kapur D, Dorsky D, Feingold JM, Bona RP, Edwards RL, Aslanzadeh J, Tutschka PJ, Bilgrami S. Incidence and outcome of vancomycin-resistant enterococcal bacteremia following autologous peripheral blood stem cell transplantation. Bone Marrow Transplantation 2000; 25 147–52.
Incidence and outcome of vancomycin-resistant enterococcal bacteremia following autologous peripheral blood stem cell transplantation.CrossRef | 1:STN:280:DC%2BD3c7jvFegsA%3D%3D&md5=2c0e0b34e5aae5e3437a2a37e3f0078cCAS | 10673672PubMed |

[24]  Kuehnert MJ, Jernigan JA, Pullen AL, Rimland D, Jarvis WR. Association between mucositis severity and vancomycin-resistant enterococcal bloodstream infection in hospitalized cancer patients. Infection Control and Hospital Epidemiology 1999; 20 660–3.
Association between mucositis severity and vancomycin-resistant enterococcal bloodstream infection in hospitalized cancer patients.CrossRef | 1:STN:280:DyaK1MvlvVahtw%3D%3D&md5=f50166128f6524e4b5f61729123e9090CAS | 10530642PubMed |

[25]  Roghmann MC, McCarter RJ, Brewrink J, Cross AS, Morris JG. Clostridium difficile infection is a risk factor for bacteremia due to vancomycin- resistant enterococci (VRE) in VRE-colonized patients with acute leukemia. Clinical Infectious Diseases 1997; 25 1056–9.
Clostridium difficile infection is a risk factor for bacteremia due to vancomycin- resistant enterococci (VRE) in VRE-colonized patients with acute leukemia.CrossRef | 1:STN:280:DyaK1c%2Fmtl2nug%3D%3D&md5=a65c251122be5edfcede4e44cf67e69fCAS | 9402356PubMed |

[26]  Gedik H, Yildirmak T, Simşek F, Kantürk A, Arıca D, Aydın D, Yokuş O, Demirel N, Arabacı Ç. Vancomycin-resistant enterococci colonization and bacteremia in patients with hematological malignancies. Journal of Infection in Developing Countries 2014; 8 1113–8.
Vancomycin-resistant enterococci colonization and bacteremia in patients with hematological malignancies.CrossRef | 25212075PubMed |

[27]  Worth LJ, Thursky KA, Seymour JF, Slavin MA. Vancomycin-resistant Enterococcus faecium infection in patients with hematologic malignancy: patients with acute myeloid leukemia are at high-risk. European Journal of Haematology 2007; 79 226–33.
Vancomycin-resistant Enterococcus faecium infection in patients with hematologic malignancy: patients with acute myeloid leukemia are at high-risk.CrossRef | 17655696PubMed |

[28]  Bonten MJM, Hayden MK, Nathan C, van Voorhis J, Matushek M, Slaughter S, Rice T, Weinstein RA. Epidemiology of colonisation of patients and environment with vancomycin-resistant enterococci. Lancet 1996; 348 1615–9.
Epidemiology of colonisation of patients and environment with vancomycin-resistant enterococci.CrossRef | 1:STN:280:DyaK2s7itFehtw%3D%3D&md5=6b33c5ad6875294af161376de5aa0551CAS |

[29]  Mollee P, Jones M, Stackelroth J, van Kuilenburg R, Joubert W, Faoagali J, Looke D, Harper J, Clements A. Catheter-associated bloodstream infection incidence and risk factors in adults with cancer: a prospective cohort study. The Journal of Hospital Infection 2011; 78 26–30.
Catheter-associated bloodstream infection incidence and risk factors in adults with cancer: a prospective cohort study.CrossRef | 1:STN:280:DC%2BC3MvktFaltg%3D%3D&md5=d74b04ff1e9d41cadac26ff7718d1e69CAS | 21459476PubMed |

[30]  Piñana JL, Montesinos P, Martino R, Vazquez L, Rovira M, Lopez J, Batlle M, Fiquera A, Barba P, Lahuerta JJ, Deben G, Perez-Lopez C, Garcia R, Rosique P, Lavilla E, Gascon A, Martinez-Cuadron P, Sanz MA. Incidence, risk factors, and outcome of bacteraemia following autologous haematopoietic stem cell transplantation in 720 adult patients. Annals of Hematology 2014; 93 299–307.
Incidence, risk factors, and outcome of bacteraemia following autologous haematopoietic stem cell transplantation in 720 adult patients.CrossRef | 23995612PubMed |

[31]  Stuck AE, Minder CE, Frey FJ. Risk of infectious complication in patients taking corticosteroids. Reviews of Infectious Diseases 1989; 11 954–63.
Risk of infectious complication in patients taking corticosteroids.CrossRef | 1:STN:280:DyaK3c7gtValug%3D%3D&md5=a6b22887699c6af1b7ef2c5fe4fb6356CAS | 2690289PubMed |

[32]  Furtado GHC, Mendes RE, Pignatari ACC, Wey SB, Medeiros EAS. Risk factors for vancomycin-resistent Enterococcus faecalis bacteraemia in hospitalized patients: an analysis of two case-control studies. American Journal of Infection Control 2006; 34 447–51.
Risk factors for vancomycin-resistent Enterococcus faecalis bacteraemia in hospitalized patients: an analysis of two case-control studies.CrossRef |

[33]  Fridkin SK, Edwards JR, Courval JM, Hill H, Tenover FC, Lawton R, Gaynes RP, McGowan JE. The effect of vancomycin and third-generation cephalosporins on prevalence of vancomycin-resistant enterococci in 126 U.S. adult intensive care units. Annals of Internal Medicine 2001; 135 175–83.
The effect of vancomycin and third-generation cephalosporins on prevalence of vancomycin-resistant enterococci in 126 U.S. adult intensive care units.CrossRef | 1:CAS:528:DC%2BD3MXmtlWktr0%3D&md5=62f4d8c7320074a6e55e2c3dc69a59c0CAS | 11487484PubMed |

[34]  Donskey CJ, Chowdhry TK, Hecker MT, Hoyen CK, Hanrahan JA, Hujer AM, Hutton-Thomas RA, Whalen CC, Bonomo RA, Rice LB. Effect of antibiotic therapy on the density of vancomycin-resistant enterococci in the stool of colonized patients. The New England Journal of Medicine 2000; 343 1925–32.
Effect of antibiotic therapy on the density of vancomycin-resistant enterococci in the stool of colonized patients.CrossRef | 1:CAS:528:DC%2BD3MXktlSltw%3D%3D&md5=cbfc8005c1d5be20a78de8d9c95bddc7CAS | 11136263PubMed |

[35]  Avery R, Kalaycio M, Pohlman B, Sobecks R, Kuczkowski E, Andresen S, Mossad S, Shamp J, Curtis J, Kosar J, Sands K, Serafin M, Bolwell B. Early vancomycin-resistant enterococcus (VRE) bacteremia after allogeneic bone marrow transplantation is associated with a rapidly deteriorating clinical course. Bone Marrow Transplantation 2005; 35 497–9.
Early vancomycin-resistant enterococcus (VRE) bacteremia after allogeneic bone marrow transplantation is associated with a rapidly deteriorating clinical course.CrossRef | 1:CAS:528:DC%2BD2MXhsFWlsL0%3D&md5=2ed62cf958d244eabc5b3225387afe52CAS | 15640812PubMed |

[36]  Tang HJ, Lin HL, Lin YH, Leung PO, Chuang YC, Lai CC. The impact of central line insertion bundle on central line-associated bloodstream infection. BMC Infectious Diseases 2014; 14 356
The impact of central line insertion bundle on central line-associated bloodstream infection.CrossRef | 24985729PubMed |

[37]  Aslam S, Darouiche RO. Prolonged bacterial exposure to minocycline/rifampicin-impregnated vascular catheters does not affect antimicrobial activity of catheters. The Journal of Antimicrobial Chemotherapy 2007; 60 148–51.
Prolonged bacterial exposure to minocycline/rifampicin-impregnated vascular catheters does not affect antimicrobial activity of catheters.CrossRef | 1:CAS:528:DC%2BD2sXot1ertrk%3D&md5=9f5120a0be148128ad635e8df8cc9488CAS | 17525051PubMed |

[38]  Therapeutic Guidelines Limited M. Empirical therapy for febrile neutropaenia. eTG complete. 2014. Available from: https://www.tg.org.au [Verified December 2014]

[39]  D’Antonio D, Staniscia T, Piccolomini R, Fioritoni G, Rotolo S, Parruti G, Di Bonaventura G, Manna A, Savini V, Fiorilli MP, Di Giovanni P, Francione A, Schioppa F, Romano F. Addition of teicoplanin or vancomycin for the treatment of documented bacteremia due to gram-positive cocci in neutropenic patients with hematological malignancies: microbiological, clinical and economic evaluation. Chemotherapy 2004; 50 81–7.
Addition of teicoplanin or vancomycin for the treatment of documented bacteremia due to gram-positive cocci in neutropenic patients with hematological malignancies: microbiological, clinical and economic evaluation.CrossRef | 1:CAS:528:DC%2BD2cXltVWktLk%3D&md5=36ba734bd973aaf5664b38a557d20b83CAS | 15211082PubMed |

[40]  Vázquez L, Encinas MP, Morin LS, Vilches P, Gutierrez N, Garcia-Sanz R, Caballero D, Hurle ADG, San Miguel JF. Randomized prospective study comparing cost-effectiveness of teicoplanin and vancomycin as second-line empiric therapy for infection in neutropenic patients. Haematologica 1999; 8 231–6.


Export Citation