Bloodstream Infection Due to Vancomycin-resistant Enterococcus Is Associated with Increased Mortality after Hematopoietic Cell Transplantation for Acute Leukemia and Myelodysplastic Syndrome: A Multicenter, Retrospective Cohort Study

Genovefa A. Papanicolaou; Celalettin Ustun; Jo Anne H. Young; Min Chen; Soyoung Kim; Kwang Woo Ahn; Krishna Komanduri; Caroline Lindemans; Jeffery J. Auletta; Marcie L. Riches; Hisham Abdel-Azim; Ibrahim A. Ahmed; Mahmoud Aljurf; Joseph Antin; Karen Kuhn Ballen; Amer Beitinjaneh; Valerie I. Brown; Jan Cerny; Richard Champlin; Nelson Chao; Saurabh Chhabra; Parastoo B. Dahi; Andrew Daly; Christopher Dandoy; Christopher C. Dvorak; Stephen Forman; Siddhartha Ganguly; Shahrukh K. Hashmi; Mohamed A. Kharfan-Dabaja; Hillard Lazarus; Per Ljungman; Adriana K. Malone; Guru Murthy; Taiga Nishihori; Kristin Page; Ravi Sai Ravi Pingali; Vijay Reddy; Ayman Saad; Bipin N. Savani; Matthew Seftel; Jeffrey Szer; Ravi Vij; Daniel Weisdorf; Basem M. William; Kirsten Williams; Baldeep Wirk; Jean Yared

doi:10.1093/cid/ciz031

Bloodstream Infection Due to Vancomycin-resistant Enterococcus Is Associated with Increased Mortality after Hematopoietic Cell Transplantation for Acute Leukemia and Myelodysplastic Syndrome: A Multicenter, Retrospective Cohort Study

Genovefa A. Papanicolaou, Celalettin Ustun, Jo Anne H. Young, Min Chen, Soyoung Kim, Kwang Woo Ahn, Krishna Komanduri, Caroline Lindemans, Jeffery J. Auletta, Marcie L. Riches, Hisham Abdel-Azim, Ibrahim A. Ahmed, Mahmoud Aljurf, Joseph Antin, Karen Kuhn Ballen, Amer Beitinjaneh, Valerie I. Brown, Jan Cerny, Richard Champlin, Nelson ChaoSaurabh Chhabra, Parastoo B. Dahi, Andrew Daly, Christopher Dandoy, Christopher C. Dvorak, Stephen Forman, Siddhartha Ganguly, Shahrukh K. Hashmi, Mohamed A. Kharfan-Dabaja, Hillard Lazarus, Per Ljungman, Adriana K. Malone, Guru Murthy, Taiga Nishihori, Kristin Page, Ravi Sai Ravi Pingali, Vijay Reddy, Ayman Saad, Bipin N. Savani, Matthew Seftel, Jeffrey Szer, Ravi Vij, Daniel Weisdorf, Basem M. William, Kirsten Williams, Baldeep Wirk, Jean Yared

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Abstract

Background: We examined the impact of vancomycin-resistant Enterococcus (VRE) bloodstream infection (BSI) on outcomes of allogeneic hematopoietic cell transplantation (HCT) utilizing the Center for International Blood and Marrow Transplant Research database. Methods: Adult and pediatric patients (N = 7128) who underwent first HCT for acute leukemia or myelodysplastic syndrome from 2008 through 2012 were analyzed as 3 groups - VRE BSI, non-VRE BSI, without BSI - according to BSI status at 100 days (D100) after allogeneic HCT. Multivariable models examined the effect of VRE BSI for overall survival (OS) and nonrelapse mortality (NRM) at 1 year. Results: Of 7128 patients, 258 (3.2%) had VRE BSI, 2398 (33.6%) had non-VRE BSI, and 4472 (63%) had no BSI. The median time to VRE BSI and non-VRE BSI were D11 and D15, respectively. Compared with non-VRE BSI patients, VRE BSI patients were older, had advanced-stage acute leukemia, and received umbilical cord blood (UCB) allografts. In multivariable models, VRE BSI was associated with lower OS (relative risk [RR], 2.9;(99% confidence interval [CI], 2.2-3.7) and increased NRM (RR, 4.7; 99% CI, 3.6-6.2) (P <. 0001) for both. Other predictors for worse OS and increased NRM were non-VRE BSI, older age, advanced disease stage, UCB allograft, - mismatch, comorbidity index ≥3, and cytomegalovirus seropositivity (P <. 001 for all variables). Conclusions: VRE BSI is associated with lowest OS and highest NRM compared with patients without BSI or non-VRE BSI. Novel interventions that address the pathophysiology of VRE BSI have the potential of improving survival after HCT.

Original language	English
Pages (from-to)	1771-1779
Number of pages	9
Journal	Clinical Infectious Diseases
Volume	69
Issue number	10
DOIs	https://doi.org/10.1093/cid/ciz031
State	Published - Nov 15 2019

Keywords

bacteremia
hematopoietic stem cell transplantation
mortality
vancomycin-resistant Enterococcus (VRE)

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Papanicolaou, G. A., Ustun, C., Young, J. A. H., Chen, M., Kim, S., Woo Ahn, K., Komanduri, K., Lindemans, C., Auletta, J. J., Riches, M. L., Abdel-Azim, H., Ahmed, I. A., Aljurf, M., Antin, J., Ballen, K. K., Beitinjaneh, A., Brown, V. I., Cerny, J., Champlin, R., ... Yared, J. (2019). Bloodstream Infection Due to Vancomycin-resistant Enterococcus Is Associated with Increased Mortality after Hematopoietic Cell Transplantation for Acute Leukemia and Myelodysplastic Syndrome: A Multicenter, Retrospective Cohort Study. Clinical Infectious Diseases, 69(10), 1771-1779. https://doi.org/10.1093/cid/ciz031

Papanicolaou, Genovefa A. ; Ustun, Celalettin ; Young, Jo Anne H. et al. / Bloodstream Infection Due to Vancomycin-resistant Enterococcus Is Associated with Increased Mortality after Hematopoietic Cell Transplantation for Acute Leukemia and Myelodysplastic Syndrome : A Multicenter, Retrospective Cohort Study. In: Clinical Infectious Diseases. 2019 ; Vol. 69, No. 10. pp. 1771-1779.

@article{ee9c31b708f346108b6ecebe61b258d1,

title = "Bloodstream Infection Due to Vancomycin-resistant Enterococcus Is Associated with Increased Mortality after Hematopoietic Cell Transplantation for Acute Leukemia and Myelodysplastic Syndrome: A Multicenter, Retrospective Cohort Study",

abstract = "Background: We examined the impact of vancomycin-resistant Enterococcus (VRE) bloodstream infection (BSI) on outcomes of allogeneic hematopoietic cell transplantation (HCT) utilizing the Center for International Blood and Marrow Transplant Research database. Methods: Adult and pediatric patients (N = 7128) who underwent first HCT for acute leukemia or myelodysplastic syndrome from 2008 through 2012 were analyzed as 3 groups - VRE BSI, non-VRE BSI, without BSI - according to BSI status at 100 days (D100) after allogeneic HCT. Multivariable models examined the effect of VRE BSI for overall survival (OS) and nonrelapse mortality (NRM) at 1 year. Results: Of 7128 patients, 258 (3.2%) had VRE BSI, 2398 (33.6%) had non-VRE BSI, and 4472 (63%) had no BSI. The median time to VRE BSI and non-VRE BSI were D11 and D15, respectively. Compared with non-VRE BSI patients, VRE BSI patients were older, had advanced-stage acute leukemia, and received umbilical cord blood (UCB) allografts. In multivariable models, VRE BSI was associated with lower OS (relative risk [RR], 2.9;(99% confidence interval [CI], 2.2-3.7) and increased NRM (RR, 4.7; 99% CI, 3.6-6.2) (P <. 0001) for both. Other predictors for worse OS and increased NRM were non-VRE BSI, older age, advanced disease stage, UCB allograft, - mismatch, comorbidity index ≥3, and cytomegalovirus seropositivity (P <. 001 for all variables). Conclusions: VRE BSI is associated with lowest OS and highest NRM compared with patients without BSI or non-VRE BSI. Novel interventions that address the pathophysiology of VRE BSI have the potential of improving survival after HCT.",

keywords = "bacteremia, hematopoietic stem cell transplantation, mortality, vancomycin-resistant Enterococcus (VRE)",

author = "Papanicolaou, {Genovefa A.} and Celalettin Ustun and Young, {Jo Anne H.} and Min Chen and Soyoung Kim and {Woo Ahn}, Kwang and Krishna Komanduri and Caroline Lindemans and Auletta, {Jeffery J.} and Riches, {Marcie L.} and Hisham Abdel-Azim and Ahmed, {Ibrahim A.} and Mahmoud Aljurf and Joseph Antin and Ballen, {Karen Kuhn} and Amer Beitinjaneh and Brown, {Valerie I.} and Jan Cerny and Richard Champlin and Nelson Chao and Saurabh Chhabra and Dahi, {Parastoo B.} and Andrew Daly and Christopher Dandoy and Dvorak, {Christopher C.} and Stephen Forman and Siddhartha Ganguly and Hashmi, {Shahrukh K.} and Kharfan-Dabaja, {Mohamed A.} and Hillard Lazarus and Per Ljungman and Malone, {Adriana K.} and Guru Murthy and Taiga Nishihori and Kristin Page and Pingali, {Ravi Sai Ravi} and Vijay Reddy and Ayman Saad and Savani, {Bipin N.} and Matthew Seftel and Jeffrey Szer and Ravi Vij and Daniel Weisdorf and William, {Basem M.} and Kirsten Williams and Baldeep Wirk and Jean Yared",

note = "Funding Information: Financial support. This work was supported by the National Institutes of Health (grant numbers P30 CA008748 and P01 CA023766). The CIBMTR{\textregistered} is supported primarily by a Public Health Service grant/cooperative agreement (grant number 5U24CA076518) from the National Cancer Institute (NCI), the National Heart, Lung, and Blood Institute (NHLBI), and the National Institute of Allergy and Infectious Diseases; a grant/co-operative agreement (grant number 1U24HL138660) from NHLBI and NCI; a contract (number HHSH250201700006C) with Health Resources and Services Administration/Department of Health and Human Services; 2 grants (grant numbers N00014-17-1-2388, N00014-17-1-2850, and N00014-18-1-2045) from the Office of Naval Research; and grants from the following: Adaptive Biotechnologies; *Amgen, Inc.; an anonymous donation to the Medical College of Wisconsin; Astellas Pharma US; Atara Biotherapeutics, Inc.; Be the Match Foundation; *bluebird bio, Inc.; *Bristol Myers Squibb Oncology; *Celgene Corporation; *Chimerix, Inc.; *CytoSen Therapeutics, Inc.; Fred Hutchinson Cancer Research Center; Gamida Cell Ltd.; Gilead Sciences, Inc.; HistoGenetics, Inc.; Immucor; *Incyte Corporation; Janssen Scientific Affairs, LLC; *Jazz Pharmaceuticals, Inc.; Karius, Inc.; Karyopharm Therapeutics, Inc.; *Kite Pharma, Inc.; Medac, GmbH; *Mediware; the Medical College of Wisconsin; *Merck & Co, Inc.; *Mesoblast; MesoScale Diagnostics, Inc.; Millennium, the Takeda Oncology Co.; *Miltenyi Biotec, Inc.; Mundipharma EDO; National Marrow Donor Program; Novartis Pharmaceuticals Corporation; PCORI; *Pfizer, Inc; *Pharmacyclics, LLC; PIRCHE AG; *Sanofi Genzyme; *Seattle Genetics; Shire; Spectrum Pharmaceuticals, Inc.; St. Baldrick{\textquoteright}s Foundation; Swedish Orphan Biovitrum, Inc.; *Takeda Oncology; and University of Minnesota. The asterisks indicate corporate membership. G. A. P. was partially funded by the NCI Cancer Center (support grant number P30 CA008748). Publisher Copyright: {\textcopyright} 2019 The Author(s) 2019. Published by Oxford University Press for the Infectious Diseases Society of America. All rights reserved.",

year = "2019",

month = nov,

day = "15",

doi = "10.1093/cid/ciz031",

language = "English",

volume = "69",

pages = "1771--1779",

journal = "Clinical Infectious Diseases",

issn = "1058-4838",

number = "10",

}

Papanicolaou, GA, Ustun, C, Young, JAH, Chen, M, Kim, S, Woo Ahn, K, Komanduri, K, Lindemans, C, Auletta, JJ, Riches, ML, Abdel-Azim, H, Ahmed, IA, Aljurf, M, Antin, J, Ballen, KK, Beitinjaneh, A, Brown, VI, Cerny, J, Champlin, R, Chao, N, Chhabra, S, Dahi, PB, Daly, A, Dandoy, C, Dvorak, CC, Forman, S, Ganguly, S, Hashmi, SK, Kharfan-Dabaja, MA, Lazarus, H, Ljungman, P, Malone, AK, Murthy, G, Nishihori, T, Page, K, Pingali, RSR, Reddy, V, Saad, A, Savani, BN, Seftel, M, Szer, J, Vij, R, Weisdorf, D, William, BM, Williams, K, Wirk, B & Yared, J 2019, 'Bloodstream Infection Due to Vancomycin-resistant Enterococcus Is Associated with Increased Mortality after Hematopoietic Cell Transplantation for Acute Leukemia and Myelodysplastic Syndrome: A Multicenter, Retrospective Cohort Study', Clinical Infectious Diseases, vol. 69, no. 10, pp. 1771-1779. https://doi.org/10.1093/cid/ciz031

Bloodstream Infection Due to Vancomycin-resistant Enterococcus Is Associated with Increased Mortality after Hematopoietic Cell Transplantation for Acute Leukemia and Myelodysplastic Syndrome: A Multicenter, Retrospective Cohort Study. / Papanicolaou, Genovefa A.; Ustun, Celalettin; Young, Jo Anne H. et al.
In: Clinical Infectious Diseases, Vol. 69, No. 10, 15.11.2019, p. 1771-1779.

Research output: Contribution to journal › Article › peer-review

TY - JOUR

T1 - Bloodstream Infection Due to Vancomycin-resistant Enterococcus Is Associated with Increased Mortality after Hematopoietic Cell Transplantation for Acute Leukemia and Myelodysplastic Syndrome

T2 - A Multicenter, Retrospective Cohort Study

AU - Papanicolaou, Genovefa A.

AU - Ustun, Celalettin

AU - Young, Jo Anne H.

AU - Chen, Min

AU - Kim, Soyoung

AU - Woo Ahn, Kwang

AU - Komanduri, Krishna

AU - Lindemans, Caroline

AU - Auletta, Jeffery J.

AU - Riches, Marcie L.

AU - Abdel-Azim, Hisham

AU - Ahmed, Ibrahim A.

AU - Aljurf, Mahmoud

AU - Antin, Joseph

AU - Ballen, Karen Kuhn

AU - Beitinjaneh, Amer

AU - Brown, Valerie I.

AU - Cerny, Jan

AU - Champlin, Richard

AU - Chao, Nelson

AU - Chhabra, Saurabh

AU - Dahi, Parastoo B.

AU - Daly, Andrew

AU - Dandoy, Christopher

AU - Dvorak, Christopher C.

AU - Forman, Stephen

AU - Ganguly, Siddhartha

AU - Hashmi, Shahrukh K.

AU - Kharfan-Dabaja, Mohamed A.

AU - Lazarus, Hillard

AU - Ljungman, Per

AU - Malone, Adriana K.

AU - Murthy, Guru

AU - Nishihori, Taiga

AU - Page, Kristin

AU - Pingali, Ravi Sai Ravi

AU - Reddy, Vijay

AU - Saad, Ayman

AU - Savani, Bipin N.

AU - Seftel, Matthew

AU - Szer, Jeffrey

AU - Vij, Ravi

AU - Weisdorf, Daniel

AU - William, Basem M.

AU - Williams, Kirsten

AU - Wirk, Baldeep

AU - Yared, Jean

N1 - Funding Information: Financial support. This work was supported by the National Institutes of Health (grant numbers P30 CA008748 and P01 CA023766). The CIBMTR® is supported primarily by a Public Health Service grant/cooperative agreement (grant number 5U24CA076518) from the National Cancer Institute (NCI), the National Heart, Lung, and Blood Institute (NHLBI), and the National Institute of Allergy and Infectious Diseases; a grant/co-operative agreement (grant number 1U24HL138660) from NHLBI and NCI; a contract (number HHSH250201700006C) with Health Resources and Services Administration/Department of Health and Human Services; 2 grants (grant numbers N00014-17-1-2388, N00014-17-1-2850, and N00014-18-1-2045) from the Office of Naval Research; and grants from the following: Adaptive Biotechnologies; *Amgen, Inc.; an anonymous donation to the Medical College of Wisconsin; Astellas Pharma US; Atara Biotherapeutics, Inc.; Be the Match Foundation; *bluebird bio, Inc.; *Bristol Myers Squibb Oncology; *Celgene Corporation; *Chimerix, Inc.; *CytoSen Therapeutics, Inc.; Fred Hutchinson Cancer Research Center; Gamida Cell Ltd.; Gilead Sciences, Inc.; HistoGenetics, Inc.; Immucor; *Incyte Corporation; Janssen Scientific Affairs, LLC; *Jazz Pharmaceuticals, Inc.; Karius, Inc.; Karyopharm Therapeutics, Inc.; *Kite Pharma, Inc.; Medac, GmbH; *Mediware; the Medical College of Wisconsin; *Merck & Co, Inc.; *Mesoblast; MesoScale Diagnostics, Inc.; Millennium, the Takeda Oncology Co.; *Miltenyi Biotec, Inc.; Mundipharma EDO; National Marrow Donor Program; Novartis Pharmaceuticals Corporation; PCORI; *Pfizer, Inc; *Pharmacyclics, LLC; PIRCHE AG; *Sanofi Genzyme; *Seattle Genetics; Shire; Spectrum Pharmaceuticals, Inc.; St. Baldrick’s Foundation; Swedish Orphan Biovitrum, Inc.; *Takeda Oncology; and University of Minnesota. The asterisks indicate corporate membership. G. A. P. was partially funded by the NCI Cancer Center (support grant number P30 CA008748). Publisher Copyright: © 2019 The Author(s) 2019. Published by Oxford University Press for the Infectious Diseases Society of America. All rights reserved.

PY - 2019/11/15

Y1 - 2019/11/15

N2 - Background: We examined the impact of vancomycin-resistant Enterococcus (VRE) bloodstream infection (BSI) on outcomes of allogeneic hematopoietic cell transplantation (HCT) utilizing the Center for International Blood and Marrow Transplant Research database. Methods: Adult and pediatric patients (N = 7128) who underwent first HCT for acute leukemia or myelodysplastic syndrome from 2008 through 2012 were analyzed as 3 groups - VRE BSI, non-VRE BSI, without BSI - according to BSI status at 100 days (D100) after allogeneic HCT. Multivariable models examined the effect of VRE BSI for overall survival (OS) and nonrelapse mortality (NRM) at 1 year. Results: Of 7128 patients, 258 (3.2%) had VRE BSI, 2398 (33.6%) had non-VRE BSI, and 4472 (63%) had no BSI. The median time to VRE BSI and non-VRE BSI were D11 and D15, respectively. Compared with non-VRE BSI patients, VRE BSI patients were older, had advanced-stage acute leukemia, and received umbilical cord blood (UCB) allografts. In multivariable models, VRE BSI was associated with lower OS (relative risk [RR], 2.9;(99% confidence interval [CI], 2.2-3.7) and increased NRM (RR, 4.7; 99% CI, 3.6-6.2) (P <. 0001) for both. Other predictors for worse OS and increased NRM were non-VRE BSI, older age, advanced disease stage, UCB allograft, - mismatch, comorbidity index ≥3, and cytomegalovirus seropositivity (P <. 001 for all variables). Conclusions: VRE BSI is associated with lowest OS and highest NRM compared with patients without BSI or non-VRE BSI. Novel interventions that address the pathophysiology of VRE BSI have the potential of improving survival after HCT.

AB - Background: We examined the impact of vancomycin-resistant Enterococcus (VRE) bloodstream infection (BSI) on outcomes of allogeneic hematopoietic cell transplantation (HCT) utilizing the Center for International Blood and Marrow Transplant Research database. Methods: Adult and pediatric patients (N = 7128) who underwent first HCT for acute leukemia or myelodysplastic syndrome from 2008 through 2012 were analyzed as 3 groups - VRE BSI, non-VRE BSI, without BSI - according to BSI status at 100 days (D100) after allogeneic HCT. Multivariable models examined the effect of VRE BSI for overall survival (OS) and nonrelapse mortality (NRM) at 1 year. Results: Of 7128 patients, 258 (3.2%) had VRE BSI, 2398 (33.6%) had non-VRE BSI, and 4472 (63%) had no BSI. The median time to VRE BSI and non-VRE BSI were D11 and D15, respectively. Compared with non-VRE BSI patients, VRE BSI patients were older, had advanced-stage acute leukemia, and received umbilical cord blood (UCB) allografts. In multivariable models, VRE BSI was associated with lower OS (relative risk [RR], 2.9;(99% confidence interval [CI], 2.2-3.7) and increased NRM (RR, 4.7; 99% CI, 3.6-6.2) (P <. 0001) for both. Other predictors for worse OS and increased NRM were non-VRE BSI, older age, advanced disease stage, UCB allograft, - mismatch, comorbidity index ≥3, and cytomegalovirus seropositivity (P <. 001 for all variables). Conclusions: VRE BSI is associated with lowest OS and highest NRM compared with patients without BSI or non-VRE BSI. Novel interventions that address the pathophysiology of VRE BSI have the potential of improving survival after HCT.

KW - bacteremia

KW - hematopoietic stem cell transplantation

KW - mortality

KW - vancomycin-resistant Enterococcus (VRE)

UR - http://www.scopus.com/inward/record.url?scp=85066129430&partnerID=8YFLogxK

U2 - 10.1093/cid/ciz031

DO - 10.1093/cid/ciz031

M3 - Article

C2 - 30649224

AN - SCOPUS:85066129430

SN - 1058-4838

VL - 69

SP - 1771

EP - 1779

JO - Clinical Infectious Diseases

JF - Clinical Infectious Diseases

IS - 10

ER -

Papanicolaou GA, Ustun C, Young JAH, Chen M, Kim S, Woo Ahn K et al. Bloodstream Infection Due to Vancomycin-resistant Enterococcus Is Associated with Increased Mortality after Hematopoietic Cell Transplantation for Acute Leukemia and Myelodysplastic Syndrome: A Multicenter, Retrospective Cohort Study. Clinical Infectious Diseases. 2019 Nov 15;69(10):1771-1779. doi: 10.1093/cid/ciz031

Bloodstream Infection Due to Vancomycin-resistant Enterococcus Is Associated with Increased Mortality after Hematopoietic Cell Transplantation for Acute Leukemia and Myelodysplastic Syndrome: A Multicenter, Retrospective Cohort Study

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