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Published in: Respiratory Research 1/2018

Open Access 01-12-2018 | Research

Microbial dysbiosis and mortality during mechanical ventilation: a prospective observational study

Authors: Daphnée Lamarche, Jennie Johnstone, Nicole Zytaruk, France Clarke, Lori Hand, Dessi Loukov, Jake C. Szamosi, Laura Rossi, Louis P. Schenck, Chris P. Verschoor, Ellen McDonald, Maureen O. Meade, John C. Marshall, Dawn M. E. Bowdish, Tim Karachi, Diane Heels-Ansdell, Deborah J. Cook, Michael G. Surette, for the PROSPECT Investigators, Canadian Critical Care Trials Group, Canadian Critical Care Translational Biology Group

Published in: Respiratory Research | Issue 1/2018

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Abstract

Background

Host-associated microbial communities have important roles in tissue homeostasis and overall health. Severe perturbations can occur within these microbial communities during critical illness due to underlying diseases and clinical interventions, potentially influencing patient outcomes. We sought to profile the microbial composition of critically ill mechanically ventilated patients, and to determine whether microbial diversity is associated with illness severity and mortality.

Methods

We conducted a prospective, observational study of mechanically ventilated critically ill patients with a high incidence of pneumonia in 2 intensive care units (ICUs) in Hamilton, Canada, nested within a randomized trial for the prevention of healthcare-associated infections. The microbial profiles of specimens from 3 anatomical sites (respiratory, and upper and lower gastrointestinal tracts) were characterized using 16S ribosomal RNA gene sequencing.

Results

We collected 65 specimens from 34 ICU patients enrolled in the trial (29 endotracheal aspirates, 26 gastric aspirates and 10 stool specimens). Specimens were collected at a median time of 3 days (lower respiratory tract and gastric aspirates; interquartile range [IQR] 2–4) and 6 days (stool; IQR 4.25–6.75) following ICU admission. We observed a loss of biogeographical distinction between the lower respiratory tract and gastrointestinal tract microbiota during critical illness. Moreover, microbial diversity in the respiratory tract was inversely correlated with APACHE II score (r = − 0.46, p = 0.013) and was associated with hospital mortality (Median Shannon index: Discharged alive; 1.964 vs. Deceased; 1.348, p = 0.045).

Conclusions

The composition of the host-associated microbial communities is severely perturbed during critical illness. Reduced microbial diversity reflects high illness severity and is associated with mortality. Microbial diversity may be a biomarker of prognostic value in mechanically ventilated patients.

Trial registration

ClinicalTrials.​gov ID NCT01782755. Registered February 4 2013.
Appendix
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Literature
1.
go back to reference Lozupone CA, Stombaugh JI, Gordon JI, Jansson JK, Knight R. Diversity, stability and resilience of the human gut microbiota. Nature. 2012;489:220–30.CrossRefPubMedPubMedCentral Lozupone CA, Stombaugh JI, Gordon JI, Jansson JK, Knight R. Diversity, stability and resilience of the human gut microbiota. Nature. 2012;489:220–30.CrossRefPubMedPubMedCentral
2.
go back to reference Sommer F, Bäckhed F. The gut microbiota--masters of host development and physiology. Nat Rev Microbiol. 2013;11:227–38.CrossRefPubMed Sommer F, Bäckhed F. The gut microbiota--masters of host development and physiology. Nat Rev Microbiol. 2013;11:227–38.CrossRefPubMed
3.
go back to reference Levy M, Blacher E, Elinav E. Microbiome, metabolites and host immunity. Curr Opin Microbiol. 2017;35:8–15.CrossRefPubMed Levy M, Blacher E, Elinav E. Microbiome, metabolites and host immunity. Curr Opin Microbiol. 2017;35:8–15.CrossRefPubMed
4.
go back to reference David LA, Materna AC, Friedman J, Campos-Baptista MI, Blackburn MC, Perrotta A, et al. Host lifestyle affects human microbiota on daily timescales. Genome Biol. 2014;15:R89.CrossRefPubMedPubMedCentral David LA, Materna AC, Friedman J, Campos-Baptista MI, Blackburn MC, Perrotta A, et al. Host lifestyle affects human microbiota on daily timescales. Genome Biol. 2014;15:R89.CrossRefPubMedPubMedCentral
5.
go back to reference Prescott HC, Dickson RP, Rogers MAM, Langa KM, Iwashyna TJ. Hospitalization type and subsequent severe Sepsis. Am J Respir Crit Care Med. 2015;192:581–8.CrossRefPubMedPubMedCentral Prescott HC, Dickson RP, Rogers MAM, Langa KM, Iwashyna TJ. Hospitalization type and subsequent severe Sepsis. Am J Respir Crit Care Med. 2015;192:581–8.CrossRefPubMedPubMedCentral
6.
go back to reference Kitsios GD, Morowitz MJ, Dickson RP, Huffnagle GB, McVerry BJ, Morris A. Dysbiosis in the intensive care unit: microbiome science coming to the bedside. J Crit Care. 2017;38:84–91.CrossRefPubMed Kitsios GD, Morowitz MJ, Dickson RP, Huffnagle GB, McVerry BJ, Morris A. Dysbiosis in the intensive care unit: microbiome science coming to the bedside. J Crit Care. 2017;38:84–91.CrossRefPubMed
7.
go back to reference Dickson RP, Singer BH, Newstead MW, Falkowski NR, Erb-Downward JR, Standiford TJ, et al. Enrichment of the lung microbiome with gut bacteria in sepsis and the acute respiratory distress syndrome. Nat Microbiol. 2016;1:16113.CrossRefPubMedPubMedCentral Dickson RP, Singer BH, Newstead MW, Falkowski NR, Erb-Downward JR, Standiford TJ, et al. Enrichment of the lung microbiome with gut bacteria in sepsis and the acute respiratory distress syndrome. Nat Microbiol. 2016;1:16113.CrossRefPubMedPubMedCentral
8.
go back to reference Zakharkina T, Martin-Loeches I, Matamoros S, Povoa P, Torres A, Kastelijn JB, et al. The dynamics of the pulmonary microbiome during mechanical ventilation in the intensive care unit and the association with occurrence of pneumonia. Thorax. 2017;72:803-10. Zakharkina T, Martin-Loeches I, Matamoros S, Povoa P, Torres A, Kastelijn JB, et al. The dynamics of the pulmonary microbiome during mechanical ventilation in the intensive care unit and the association with occurrence of pneumonia. Thorax. 2017;72:803-10.
9.
go back to reference Yamada T, Shimizu K, Ogura H, Asahara T, Nomoto K, Yamakawa K, et al. Rapid and sustained long-term decrease of fecal short-chain fatty acids in critically ill patients with systemic inflammatory response syndrome. JPEN J Parenter Enteral Nutr. 2015;39:569–77.CrossRefPubMed Yamada T, Shimizu K, Ogura H, Asahara T, Nomoto K, Yamakawa K, et al. Rapid and sustained long-term decrease of fecal short-chain fatty acids in critically ill patients with systemic inflammatory response syndrome. JPEN J Parenter Enteral Nutr. 2015;39:569–77.CrossRefPubMed
11.
go back to reference McDonald D, Ackermann G, Khailova L, Baird C, Heyland D, Kozar R, et al. Extreme Dysbiosis of the Microbiome in Critical Illness. mSphere. 2016;1:e00199–16. McDonald D, Ackermann G, Khailova L, Baird C, Heyland D, Kozar R, et al. Extreme Dysbiosis of the Microbiome in Critical Illness. mSphere. 2016;1:e00199–16.
12.
go back to reference Zaborin A, Smith D, Garfield K, Quensen J, Shakhsheer B, Kade M, et al. Membership and Behavior of Ultra-Low-Diversity Pathogen Communities Present in the Gut of Humans during Prolonged Critical Illness. mBio. 2014;5:e01361–14.CrossRefPubMedPubMedCentral Zaborin A, Smith D, Garfield K, Quensen J, Shakhsheer B, Kade M, et al. Membership and Behavior of Ultra-Low-Diversity Pathogen Communities Present in the Gut of Humans during Prolonged Critical Illness. mBio. 2014;5:e01361–14.CrossRefPubMedPubMedCentral
13.
go back to reference Berdal JE, Bjørnholt J, Blomfeldt A, Smith-Erichsen N, Bukholm G. Patterns and dynamics of airway colonisation in mechanically-ventilated patients. Clin Microbiol Infect. 2007;13:476–80. Berdal JE, Bjørnholt J, Blomfeldt A, Smith-Erichsen N, Bukholm G. Patterns and dynamics of airway colonisation in mechanically-ventilated patients. Clin Microbiol Infect. 2007;13:476–80.
14.
go back to reference Yeh A, Rogers MB, Firek B, Neal MD, Zuckerbraun BS, Morowitz MJ. Dysbiosis across multiple body sites in critically ill adult surgical patients. Shock. 2016;46:649–54.CrossRefPubMed Yeh A, Rogers MB, Firek B, Neal MD, Zuckerbraun BS, Morowitz MJ. Dysbiosis across multiple body sites in critically ill adult surgical patients. Shock. 2016;46:649–54.CrossRefPubMed
15.
go back to reference Kelly BJ, Imai I, Bittinger K, Laughlin A, Fuchs BD, Bushman FD, et al. Composition and dynamics of the respiratory tract microbiome in intubated patients. Microbiome BioMed Central. 2016;4:7. Kelly BJ, Imai I, Bittinger K, Laughlin A, Fuchs BD, Bushman FD, et al. Composition and dynamics of the respiratory tract microbiome in intubated patients. Microbiome BioMed Central. 2016;4:7.
16.
go back to reference Shimizu K, Ogura H, Tomono K, Tasaki O, Asahara T, Nomoto K, et al. Patterns of gram-stained fecal Flora as a quick diagnostic marker in patients with severe SIRS. Dig Dis Sci Springer US. 2010;56:1782–8.CrossRef Shimizu K, Ogura H, Tomono K, Tasaki O, Asahara T, Nomoto K, et al. Patterns of gram-stained fecal Flora as a quick diagnostic marker in patients with severe SIRS. Dig Dis Sci Springer US. 2010;56:1782–8.CrossRef
17.
go back to reference Lankelma JM, van Vught LA, Belzer C, Schultz MJ, van der Poll T, de Vos WM, et al. Critically ill patients demonstrate large interpersonal variation in intestinal microbiota dysregulation: a pilot study. Intensive Care Med. 2017;43:59–68.CrossRefPubMed Lankelma JM, van Vught LA, Belzer C, Schultz MJ, van der Poll T, de Vos WM, et al. Critically ill patients demonstrate large interpersonal variation in intestinal microbiota dysregulation: a pilot study. Intensive Care Med. 2017;43:59–68.CrossRefPubMed
18.
go back to reference Silvestri L, de la Cal MA, van Saene HKF. Selective decontamination of the digestive tract: the mechanism of action is control of gut overgrowth. Intensive Care Med Springer-Verlag. 2012;38:1738–50.CrossRef Silvestri L, de la Cal MA, van Saene HKF. Selective decontamination of the digestive tract: the mechanism of action is control of gut overgrowth. Intensive Care Med Springer-Verlag. 2012;38:1738–50.CrossRef
19.
go back to reference Manzanares W, Lemieux M, Langlois PL, Wischmeyer PE. Probiotic and synbiotic therapy in critical illness: a systematic review and meta-analysis. Crit Care BioMed Central. 2016;19:262.CrossRef Manzanares W, Lemieux M, Langlois PL, Wischmeyer PE. Probiotic and synbiotic therapy in critical illness: a systematic review and meta-analysis. Crit Care BioMed Central. 2016;19:262.CrossRef
20.
go back to reference Li Q, Wang C, Tang C, He Q, Zhao X, Li N, et al. Successful treatment of severe sepsis and diarrhea after vagotomy utilizing fecal microbiota transplantation: a case report. Crit Care BioMed Central. 2015;19:37.CrossRef Li Q, Wang C, Tang C, He Q, Zhao X, Li N, et al. Successful treatment of severe sepsis and diarrhea after vagotomy utilizing fecal microbiota transplantation: a case report. Crit Care BioMed Central. 2015;19:37.CrossRef
21.
go back to reference Wei Y, Yang J, Wang J, Yang Y, Huang J, Gong H, et al. Successful treatment with fecal microbiota transplantation in patients with multiple organ dysfunction syndrome and diarrhea following severe sepsis. Crit Care BioMed Central. 2016;20:332.CrossRef Wei Y, Yang J, Wang J, Yang Y, Huang J, Gong H, et al. Successful treatment with fecal microbiota transplantation in patients with multiple organ dysfunction syndrome and diarrhea following severe sepsis. Crit Care BioMed Central. 2016;20:332.CrossRef
22.
go back to reference Cook DJ, Johnstone J, Marshall JC, Lauzier F, Thabane L, Mehta S, et al. Probiotics: Prevention of Severe Pneumonia and Endotracheal Colonization Trial—PROSPECT: a pilot trial. Trials BioMed Central. 2016;17:377. Cook DJ, Johnstone J, Marshall JC, Lauzier F, Thabane L, Mehta S, et al. Probiotics: Prevention of Severe Pneumonia and Endotracheal Colonization Trial—PROSPECT: a pilot trial. Trials BioMed Central. 2016;17:377.
23.
go back to reference Stearns JC, Davidson CJ, McKeon S, Whelan FJ, Fontes ME, Schryvers AB, et al. Culture and molecular-based profiles show shifts in bacterial communities of the upper respiratory tract that occur with age. ISME J. 2015;9:1246–59.CrossRefPubMedPubMedCentral Stearns JC, Davidson CJ, McKeon S, Whelan FJ, Fontes ME, Schryvers AB, et al. Culture and molecular-based profiles show shifts in bacterial communities of the upper respiratory tract that occur with age. ISME J. 2015;9:1246–59.CrossRefPubMedPubMedCentral
24.
go back to reference Moayyedi P, Surette MG, Kim PT, Libertucci J, Wolfe M, Onischi C, et al. Fecal microbiota transplantation induces remission in patients with active ulcerative colitis in a randomized controlled trial. Gastroenterology. 2015;149:102–6.CrossRefPubMed Moayyedi P, Surette MG, Kim PT, Libertucci J, Wolfe M, Onischi C, et al. Fecal microbiota transplantation induces remission in patients with active ulcerative colitis in a randomized controlled trial. Gastroenterology. 2015;149:102–6.CrossRefPubMed
25.
go back to reference Potts RHG. Investigating the gut microbiome of patients with generalized anxiety disorder, major depressive disorder and bipolar patients. Master's thesis. McMaster University, Department of Medical Sciences. 2017. Potts RHG. Investigating the gut microbiome of patients with generalized anxiety disorder, major depressive disorder and bipolar patients. Master's thesis. McMaster University, Department of Medical Sciences. 2017.
26.
go back to reference Baatjes AJ, Smith SG, Watson R, Howie K, Murphy D, Larché M, et al. T regulatory cell phenotypes in peripheral blood and bronchoalveolar lavage from non-asthmatic and asthmatic subjects. Clin Exp Allergy. 2015;45:1654–62.CrossRefPubMed Baatjes AJ, Smith SG, Watson R, Howie K, Murphy D, Larché M, et al. T regulatory cell phenotypes in peripheral blood and bronchoalveolar lavage from non-asthmatic and asthmatic subjects. Clin Exp Allergy. 2015;45:1654–62.CrossRefPubMed
27.
go back to reference Whelan FJ, Verschoor CP, Stearns JC, Rossi L, Luinstra K, Loeb M, et al. The loss of topography in the microbial communities of the upper respiratory tract in the elderly. Annals ATS. 2014;11:513–21.CrossRef Whelan FJ, Verschoor CP, Stearns JC, Rossi L, Luinstra K, Loeb M, et al. The loss of topography in the microbial communities of the upper respiratory tract in the elderly. Annals ATS. 2014;11:513–21.CrossRef
28.
go back to reference Whelan FJ, Surette MG. A comprehensive evaluation of the sl1p pipeline for 16S rRNA gene sequencing analysis. Microbiome BioMed Central. 2017;5:100. Whelan FJ, Surette MG. A comprehensive evaluation of the sl1p pipeline for 16S rRNA gene sequencing analysis. Microbiome BioMed Central. 2017;5:100.
30.
go back to reference McMurdie PJ, Holmes S. Phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. Watson M, editor. PLoS One 2013;8:e61217–e61211. McMurdie PJ, Holmes S. Phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. Watson M, editor. PLoS One 2013;8:e61217–e61211.
31.
go back to reference Morgan XC, Huttenhower C. Chapter 12: Human microbiome analysis. Lewitter F, Kann M, editors. PLoS Comput Biol. Public Libr Sci; 2012;8:e1002808. Morgan XC, Huttenhower C. Chapter 12: Human microbiome analysis. Lewitter F, Kann M, editors. PLoS Comput Biol. Public Libr Sci; 2012;8:e1002808.
32.
33.
go back to reference Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods Nature Publishing Group. 2010;7:335–6.CrossRef Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods Nature Publishing Group. 2010;7:335–6.CrossRef
38.
go back to reference Bates D, Mächler M. Ben Bolker, Walker S. Fitting Linear Mixed-Effects Models Using lme4. J Stat Softw. 2015;67:1–48.CrossRef Bates D, Mächler M. Ben Bolker, Walker S. Fitting Linear Mixed-Effects Models Using lme4. J Stat Softw. 2015;67:1–48.CrossRef
39.
go back to reference The Human Microbiome Project Consortium. Structure, function and diversity of the healthy human microbiome. Nature. Nat Publ Group; 2012;486:207–214. The Human Microbiome Project Consortium. Structure, function and diversity of the healthy human microbiome. Nature. Nat Publ Group; 2012;486:207–214.
40.
go back to reference Charlson ES, Bittinger K, Haas AR, Fitzgerald AS, Frank I, Yadav A, et al. Topographical continuity of bacterial populations in the healthy human respiratory tract. Am J Respir Crit Care Med. 2011;184:957–63.CrossRefPubMedPubMedCentral Charlson ES, Bittinger K, Haas AR, Fitzgerald AS, Frank I, Yadav A, et al. Topographical continuity of bacterial populations in the healthy human respiratory tract. Am J Respir Crit Care Med. 2011;184:957–63.CrossRefPubMedPubMedCentral
41.
go back to reference Dickson RP, Erb-Downward JR, Freeman CM, McCloskey L, Falkowski NR, Huffnagle GB, et al. Bacterial Topography of the Healthy Human Lower Respiratory Tract. Clemente JC, editor. mBio American Society for Microbiology; 2017;8:e02287–e02216. Dickson RP, Erb-Downward JR, Freeman CM, McCloskey L, Falkowski NR, Huffnagle GB, et al. Bacterial Topography of the Healthy Human Lower Respiratory Tract. Clemente JC, editor. mBio American Society for Microbiology; 2017;8:e02287–e02216.
42.
go back to reference Knaus WA, Draper EA, Wagner DP, Zimmerman JE. APACHE II: a severity of disease classification system. Crit Care Med. 1985;13:818–29.CrossRefPubMed Knaus WA, Draper EA, Wagner DP, Zimmerman JE. APACHE II: a severity of disease classification system. Crit Care Med. 1985;13:818–29.CrossRefPubMed
43.
go back to reference Rogers MB, Firek B, Shi M, Yeh A, Brower-Sinning R, Aveson V, et al. Disruption of the microbiota across multiple body sites in critically ill children. Microbiome BioMed Central. 2016;4:66. Rogers MB, Firek B, Shi M, Yeh A, Brower-Sinning R, Aveson V, et al. Disruption of the microbiota across multiple body sites in critically ill children. Microbiome BioMed Central. 2016;4:66.
44.
go back to reference Marshall JC, Christou NV, Horn R, Meakins JL. The microbiology of multiple organ failure. The proximal gastrointestinal tract as an occult reservoir of pathogens. Arch Surg. 1988;123:309–15.CrossRefPubMed Marshall JC, Christou NV, Horn R, Meakins JL. The microbiology of multiple organ failure. The proximal gastrointestinal tract as an occult reservoir of pathogens. Arch Surg. 1988;123:309–15.CrossRefPubMed
45.
go back to reference Chastre J, Fagon J-Y. Ventilator-associated pneumonia. Am J Respir Crit Care Med. 2002;165:867–903.CrossRefPubMed Chastre J, Fagon J-Y. Ventilator-associated pneumonia. Am J Respir Crit Care Med. 2002;165:867–903.CrossRefPubMed
46.
go back to reference Ali T, Harty RF. Stress-induced ulcer bleeding in critically ill patients. Gastroenterol Clin N Am. 2009;38:245–65.CrossRef Ali T, Harty RF. Stress-induced ulcer bleeding in critically ill patients. Gastroenterol Clin N Am. 2009;38:245–65.CrossRef
47.
go back to reference Rosen R, Hu L, Amirault J, Khatwa U, Ward DV, Onderdonk A. 16S community profiling identifies proton pump inhibitor related differences in gastric, lung, and oropharyngeal microflora. J Pediatr. 2015;166:917–23.CrossRefPubMedPubMedCentral Rosen R, Hu L, Amirault J, Khatwa U, Ward DV, Onderdonk A. 16S community profiling identifies proton pump inhibitor related differences in gastric, lung, and oropharyngeal microflora. J Pediatr. 2015;166:917–23.CrossRefPubMedPubMedCentral
48.
go back to reference Arpaia N, Campbell C, Fan X, Dikiy S, van der Veeken J, deRoos P, et al. Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation. Nature. 2013;504:451–5.CrossRefPubMedPubMedCentral Arpaia N, Campbell C, Fan X, Dikiy S, van der Veeken J, deRoos P, et al. Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation. Nature. 2013;504:451–5.CrossRefPubMedPubMedCentral
49.
go back to reference Sokol H, Pigneur B, Watterlot L, Lakhdari O, Bermúdez-Humarán LG, Gratadoux J-J, et al. Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proc. Natl. Acad. Sci. U.S.a. National Acad Sciences. 2008;105:16731–6.CrossRef Sokol H, Pigneur B, Watterlot L, Lakhdari O, Bermúdez-Humarán LG, Gratadoux J-J, et al. Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proc. Natl. Acad. Sci. U.S.a. National Acad Sciences. 2008;105:16731–6.CrossRef
50.
go back to reference Hayakawa M, Asahara T, Henzan N, Murakami H, Yamamoto H, Mukai N, et al. Dramatic changes of the gut flora immediately after severe and sudden insults. Dig Dis Sci. 2011;56:2361–5.CrossRefPubMed Hayakawa M, Asahara T, Henzan N, Murakami H, Yamamoto H, Mukai N, et al. Dramatic changes of the gut flora immediately after severe and sudden insults. Dig Dis Sci. 2011;56:2361–5.CrossRefPubMed
51.
go back to reference Scales BS, Dickson RP, Huffnagle GB. A tale of two sites: how inflammation can reshape the microbiomes of the gut and lungs. J Leukoc Biol. 2016;100:943–50.CrossRefPubMedPubMedCentral Scales BS, Dickson RP, Huffnagle GB. A tale of two sites: how inflammation can reshape the microbiomes of the gut and lungs. J Leukoc Biol. 2016;100:943–50.CrossRefPubMedPubMedCentral
52.
go back to reference Richards MJ, Edwards JR, Culver DH, Gaynes RP. Nosocomial infections in combined medical-surgical intensive care units in the United States. Infect Control Hosp Epidemiol. 2000;21:510–5.CrossRefPubMed Richards MJ, Edwards JR, Culver DH, Gaynes RP. Nosocomial infections in combined medical-surgical intensive care units in the United States. Infect Control Hosp Epidemiol. 2000;21:510–5.CrossRefPubMed
53.
go back to reference Vincent J-L, Rello J, Marshall J, Silva E, Anzueto A, Martin CD, et al. International study of the prevalence and outcomes of infection in intensive care units. JAMA American Medical Association. 2009;302:2323–9.CrossRef Vincent J-L, Rello J, Marshall J, Silva E, Anzueto A, Martin CD, et al. International study of the prevalence and outcomes of infection in intensive care units. JAMA American Medical Association. 2009;302:2323–9.CrossRef
54.
go back to reference Taur Y, Jenq RR, Perales M-A, Littmann ER, Morjaria S, Ling L, et al. The effects of intestinal tract bacterial diversity on mortality following allogeneic hematopoietic stem cell transplantation. Blood. 2014;124:1174–82.CrossRefPubMedPubMedCentral Taur Y, Jenq RR, Perales M-A, Littmann ER, Morjaria S, Ling L, et al. The effects of intestinal tract bacterial diversity on mortality following allogeneic hematopoietic stem cell transplantation. Blood. 2014;124:1174–82.CrossRefPubMedPubMedCentral
55.
go back to reference Iapichino G, Callegari ML, Marzorati S, Cigada M, Corbella D, Ferrari S, et al. Impact of antibiotics on the gut microbiota of critically ill patients. J Med Microbiol. 2008;57:1007–14. Iapichino G, Callegari ML, Marzorati S, Cigada M, Corbella D, Ferrari S, et al. Impact of antibiotics on the gut microbiota of critically ill patients. J Med Microbiol. 2008;57:1007–14.
Metadata
Title
Microbial dysbiosis and mortality during mechanical ventilation: a prospective observational study
Authors
Daphnée Lamarche
Jennie Johnstone
Nicole Zytaruk
France Clarke
Lori Hand
Dessi Loukov
Jake C. Szamosi
Laura Rossi
Louis P. Schenck
Chris P. Verschoor
Ellen McDonald
Maureen O. Meade
John C. Marshall
Dawn M. E. Bowdish
Tim Karachi
Diane Heels-Ansdell
Deborah J. Cook
Michael G. Surette
for the PROSPECT Investigators
Canadian Critical Care Trials Group
Canadian Critical Care Translational Biology Group
Publication date
01-12-2018
Publisher
BioMed Central
Published in
Respiratory Research / Issue 1/2018
Electronic ISSN: 1465-993X
DOI
https://doi.org/10.1186/s12931-018-0950-5

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