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The Impact of Bacterial Biofilms on End-Organ Disease and Mortality in Patients with Hematologic Malignancies Developing a Bloodstream Infection

Bacterial bloodstream infection (BSI) represents a significant complication in hematologic patients. However, factors leading to BSI and progression to end-organ disease and death are understood only partially. The study analyzes host and microbial risk factors and assesses their impact on BSI devel...

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Autores principales: Di Domenico, Enea Gino, Marchesi, Francesco, Cavallo, Ilaria, Toma, Luigi, Sivori, Francesca, Papa, Elena, Spadea, Antonio, Cafarella, Giuseppina, Terrenato, Irene, Prignano, Grazia, Pimpinelli, Fulvia, Mastrofrancesco, Arianna, D’Agosto, Giovanna, Trento, Elisabetta, Morrone, Aldo, Mengarelli, Andrea, Ensoli, Fabrizio
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8552682/
https://www.ncbi.nlm.nih.gov/pubmed/34406812
http://dx.doi.org/10.1128/spectrum.00550-21
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author Di Domenico, Enea Gino
Marchesi, Francesco
Cavallo, Ilaria
Toma, Luigi
Sivori, Francesca
Papa, Elena
Spadea, Antonio
Cafarella, Giuseppina
Terrenato, Irene
Prignano, Grazia
Pimpinelli, Fulvia
Mastrofrancesco, Arianna
D’Agosto, Giovanna
Trento, Elisabetta
Morrone, Aldo
Mengarelli, Andrea
Ensoli, Fabrizio
author_facet Di Domenico, Enea Gino
Marchesi, Francesco
Cavallo, Ilaria
Toma, Luigi
Sivori, Francesca
Papa, Elena
Spadea, Antonio
Cafarella, Giuseppina
Terrenato, Irene
Prignano, Grazia
Pimpinelli, Fulvia
Mastrofrancesco, Arianna
D’Agosto, Giovanna
Trento, Elisabetta
Morrone, Aldo
Mengarelli, Andrea
Ensoli, Fabrizio
author_sort Di Domenico, Enea Gino
collection PubMed
description Bacterial bloodstream infection (BSI) represents a significant complication in hematologic patients. However, factors leading to BSI and progression to end-organ disease and death are understood only partially. The study analyzes host and microbial risk factors and assesses their impact on BSI development and mortality. A total of 96 patients with hematological malignancies and BSI were included in the study. Host-associated risk factors and all causes of mortality were analyzed by multivariable logistic regression at 30 days after BSI onset of the first neutropenic episode. The multidrug-resistant profile and biofilm production of bacterial isolates from primary BSI were included in the analysis. Median age was 60 years. The underlying diagnoses were acute leukemia (55%), lymphoma (31%), and myeloma (14%). A total of 96 bacterial isolates were isolated from BSIs. Escherichia coli was the most common isolate (29.2%). Multidrug-resistant bacteria caused 10.4% of bacteremia episodes. Weak biofilm producers (WBPs) were significantly (P < 0.0001) more abundant (72.2%) than strong biofilm producers (SBPs) (27.8%). Specifically, SBPs were 7.1% for E. coli, 93.7% for P. aeruginosa, 50% for K. pneumoniae, and 3.8% for coagulase-negative staphylococci. Mortality at day 30 was 8.3%, and all deaths were attributable to Gram-negative bacteria. About 22% of all BSIs were catheter-related BSIs (CRBSIs) and mostly caused by Gram-positive bacteria (79.0%). However, CRBSIs were not correlated with biofilm production levels (P = 0.75) and did not significantly impact the mortality rate (P = 0.62). Conversely, SBP bacteria were an independent risk factor (P = 0.018) for developing an end-organ disease. In addition, multivariate analysis indicated that SBPs (P = 0.013) and multidrug-resistant bacteria (P = 0.006) were independent risk factors associated with 30-day mortality. SBP and multidrug-resistant (MDR) bacteria caused a limited fraction of BSI in these patients. However, when present, SBPs raise the risk of end-organ disease and, together with an MDR phenotype, can independently and significantly concur at increasing the risk of death. IMPORTANCE Bacterial bloodstream infection (BSI) is a significant complication in hematologic patients and is associated with high mortality rates. Despite improvements in BSI management, factors leading to sepsis are understood only partially. This study analyzes the contribution of bacterial biofilm on BSI development and mortality in patients with hematological malignancies (HMs). In this work, weak biofilm producers (WBPs) were significantly more abundant than strong biofilm producers (SBPs). However, when present, SBP bacteria raised the risk of end-organ disease in HM patients developing a BSI. Besides, SBPs, together with a multidrug-resistant (MDR) phenotype, independently and significantly concur at increasing the risk of death in HM patients. The characterization of microbial biofilms may provide key information for the diagnosis and therapeutic management of BSI and may help develop novel strategies to either eradicate or control harmful microbial biofilms.
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spelling pubmed-85526822021-11-08 The Impact of Bacterial Biofilms on End-Organ Disease and Mortality in Patients with Hematologic Malignancies Developing a Bloodstream Infection Di Domenico, Enea Gino Marchesi, Francesco Cavallo, Ilaria Toma, Luigi Sivori, Francesca Papa, Elena Spadea, Antonio Cafarella, Giuseppina Terrenato, Irene Prignano, Grazia Pimpinelli, Fulvia Mastrofrancesco, Arianna D’Agosto, Giovanna Trento, Elisabetta Morrone, Aldo Mengarelli, Andrea Ensoli, Fabrizio Microbiol Spectr Research Article Bacterial bloodstream infection (BSI) represents a significant complication in hematologic patients. However, factors leading to BSI and progression to end-organ disease and death are understood only partially. The study analyzes host and microbial risk factors and assesses their impact on BSI development and mortality. A total of 96 patients with hematological malignancies and BSI were included in the study. Host-associated risk factors and all causes of mortality were analyzed by multivariable logistic regression at 30 days after BSI onset of the first neutropenic episode. The multidrug-resistant profile and biofilm production of bacterial isolates from primary BSI were included in the analysis. Median age was 60 years. The underlying diagnoses were acute leukemia (55%), lymphoma (31%), and myeloma (14%). A total of 96 bacterial isolates were isolated from BSIs. Escherichia coli was the most common isolate (29.2%). Multidrug-resistant bacteria caused 10.4% of bacteremia episodes. Weak biofilm producers (WBPs) were significantly (P < 0.0001) more abundant (72.2%) than strong biofilm producers (SBPs) (27.8%). Specifically, SBPs were 7.1% for E. coli, 93.7% for P. aeruginosa, 50% for K. pneumoniae, and 3.8% for coagulase-negative staphylococci. Mortality at day 30 was 8.3%, and all deaths were attributable to Gram-negative bacteria. About 22% of all BSIs were catheter-related BSIs (CRBSIs) and mostly caused by Gram-positive bacteria (79.0%). However, CRBSIs were not correlated with biofilm production levels (P = 0.75) and did not significantly impact the mortality rate (P = 0.62). Conversely, SBP bacteria were an independent risk factor (P = 0.018) for developing an end-organ disease. In addition, multivariate analysis indicated that SBPs (P = 0.013) and multidrug-resistant bacteria (P = 0.006) were independent risk factors associated with 30-day mortality. SBP and multidrug-resistant (MDR) bacteria caused a limited fraction of BSI in these patients. However, when present, SBPs raise the risk of end-organ disease and, together with an MDR phenotype, can independently and significantly concur at increasing the risk of death. IMPORTANCE Bacterial bloodstream infection (BSI) is a significant complication in hematologic patients and is associated with high mortality rates. Despite improvements in BSI management, factors leading to sepsis are understood only partially. This study analyzes the contribution of bacterial biofilm on BSI development and mortality in patients with hematological malignancies (HMs). In this work, weak biofilm producers (WBPs) were significantly more abundant than strong biofilm producers (SBPs). However, when present, SBP bacteria raised the risk of end-organ disease in HM patients developing a BSI. Besides, SBPs, together with a multidrug-resistant (MDR) phenotype, independently and significantly concur at increasing the risk of death in HM patients. The characterization of microbial biofilms may provide key information for the diagnosis and therapeutic management of BSI and may help develop novel strategies to either eradicate or control harmful microbial biofilms. American Society for Microbiology 2021-08-18 /pmc/articles/PMC8552682/ /pubmed/34406812 http://dx.doi.org/10.1128/spectrum.00550-21 Text en Copyright © 2021 Di Domenico et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Di Domenico, Enea Gino
Marchesi, Francesco
Cavallo, Ilaria
Toma, Luigi
Sivori, Francesca
Papa, Elena
Spadea, Antonio
Cafarella, Giuseppina
Terrenato, Irene
Prignano, Grazia
Pimpinelli, Fulvia
Mastrofrancesco, Arianna
D’Agosto, Giovanna
Trento, Elisabetta
Morrone, Aldo
Mengarelli, Andrea
Ensoli, Fabrizio
The Impact of Bacterial Biofilms on End-Organ Disease and Mortality in Patients with Hematologic Malignancies Developing a Bloodstream Infection
title The Impact of Bacterial Biofilms on End-Organ Disease and Mortality in Patients with Hematologic Malignancies Developing a Bloodstream Infection
title_full The Impact of Bacterial Biofilms on End-Organ Disease and Mortality in Patients with Hematologic Malignancies Developing a Bloodstream Infection
title_fullStr The Impact of Bacterial Biofilms on End-Organ Disease and Mortality in Patients with Hematologic Malignancies Developing a Bloodstream Infection
title_full_unstemmed The Impact of Bacterial Biofilms on End-Organ Disease and Mortality in Patients with Hematologic Malignancies Developing a Bloodstream Infection
title_short The Impact of Bacterial Biofilms on End-Organ Disease and Mortality in Patients with Hematologic Malignancies Developing a Bloodstream Infection
title_sort impact of bacterial biofilms on end-organ disease and mortality in patients with hematologic malignancies developing a bloodstream infection
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8552682/
https://www.ncbi.nlm.nih.gov/pubmed/34406812
http://dx.doi.org/10.1128/spectrum.00550-21
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