Maintenance tobramycin primarily affects untargeted bacteria in the CF sputum microbiome
RationaleThe most common antibiotic used to treat people with cystic fibrosis (PWCF) is inhaled tobramycin, administered as maintenance therapy for chronic Pseudomonas aeruginosa lung infections. While the effects of inhaled tobramycin on P. aeruginosa abundance and lung function diminish with conti...
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| Published in | Thorax Vol. 75; no. 9; pp. 780 - 790 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
England
BMJ Publishing Group Ltd and British Thoracic Society
01.09.2020
BMJ Publishing Group LTD |
| Subjects | |
| Online Access | Get full text |
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| Abstract | RationaleThe most common antibiotic used to treat people with cystic fibrosis (PWCF) is inhaled tobramycin, administered as maintenance therapy for chronic Pseudomonas aeruginosa lung infections. While the effects of inhaled tobramycin on P. aeruginosa abundance and lung function diminish with continued therapy, this maintenance treatment is known to improve long-term outcomes, underscoring how little is known about why antibiotics work in CF infections, what their effects are on complex CF sputum microbiomes and how to improve these treatments.ObjectivesTo rigorously define the effect of maintenance tobramycin on CF sputum microbiome characteristics.Methods and measurementsWe collected sputum from 30 PWCF at standardised times before, during and after a single month-long course of maintenance inhaled tobramycin. We used traditional culture, quantitative PCR and metagenomic sequencing to define the dynamic effects of this treatment on sputum microbiomes, including abundance changes in both clinically targeted and untargeted bacteria, as well as functional gene categories.Main resultsCF sputum microbiota changed most markedly by 1 week of antibiotic therapy and plateaued thereafter, and this shift was largely driven by changes in non-dominant taxa. The genetically conferred functional capacities (ie, metagenomes) of subjects’ sputum communities changed little with antibiotic perturbation, despite taxonomic shifts, suggesting functional redundancy within the CF sputum microbiome.ConclusionsMaintenance treatment with inhaled tobramycin, an antibiotic with demonstrated long-term mortality benefit, primarily impacted clinically untargeted bacteria in CF sputum, highlighting the importance of monitoring the non-canonical effects of antibiotics and other treatments to accurately define and improve their clinical impact. |
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| AbstractList | RationaleThe most common antibiotic used to treat people with cystic fibrosis (PWCF) is inhaled tobramycin, administered as maintenance therapy for chronic Pseudomonas aeruginosa lung infections. While the effects of inhaled tobramycin on P. aeruginosa abundance and lung function diminish with continued therapy, this maintenance treatment is known to improve long-term outcomes, underscoring how little is known about why antibiotics work in CF infections, what their effects are on complex CF sputum microbiomes and how to improve these treatments.ObjectivesTo rigorously define the effect of maintenance tobramycin on CF sputum microbiome characteristics.Methods and measurementsWe collected sputum from 30 PWCF at standardised times before, during and after a single month-long course of maintenance inhaled tobramycin. We used traditional culture, quantitative PCR and metagenomic sequencing to define the dynamic effects of this treatment on sputum microbiomes, including abundance changes in both clinically targeted and untargeted bacteria, as well as functional gene categories.Main resultsCF sputum microbiota changed most markedly by 1 week of antibiotic therapy and plateaued thereafter, and this shift was largely driven by changes in non-dominant taxa. The genetically conferred functional capacities (ie, metagenomes) of subjects’ sputum communities changed little with antibiotic perturbation, despite taxonomic shifts, suggesting functional redundancy within the CF sputum microbiome.ConclusionsMaintenance treatment with inhaled tobramycin, an antibiotic with demonstrated long-term mortality benefit, primarily impacted clinically untargeted bacteria in CF sputum, highlighting the importance of monitoring the non-canonical effects of antibiotics and other treatments to accurately define and improve their clinical impact. The most common antibiotic used to treat people with cystic fibrosis (PWCF) is inhaled tobramycin, administered as maintenance therapy for chronic Pseudomonas aeruginosa lung infections. While the effects of inhaled tobramycin on P. aeruginosa abundance and lung function diminish with continued therapy, this maintenance treatment is known to improve long-term outcomes, underscoring how little is known about why antibiotics work in CF infections, what their effects are on complex CF sputum microbiomes and how to improve these treatments.RATIONALEThe most common antibiotic used to treat people with cystic fibrosis (PWCF) is inhaled tobramycin, administered as maintenance therapy for chronic Pseudomonas aeruginosa lung infections. While the effects of inhaled tobramycin on P. aeruginosa abundance and lung function diminish with continued therapy, this maintenance treatment is known to improve long-term outcomes, underscoring how little is known about why antibiotics work in CF infections, what their effects are on complex CF sputum microbiomes and how to improve these treatments.To rigorously define the effect of maintenance tobramycin on CF sputum microbiome characteristics.OBJECTIVESTo rigorously define the effect of maintenance tobramycin on CF sputum microbiome characteristics.We collected sputum from 30 PWCF at standardised times before, during and after a single month-long course of maintenance inhaled tobramycin. We used traditional culture, quantitative PCR and metagenomic sequencing to define the dynamic effects of this treatment on sputum microbiomes, including abundance changes in both clinically targeted and untargeted bacteria, as well as functional gene categories.METHODS AND MEASUREMENTSWe collected sputum from 30 PWCF at standardised times before, during and after a single month-long course of maintenance inhaled tobramycin. We used traditional culture, quantitative PCR and metagenomic sequencing to define the dynamic effects of this treatment on sputum microbiomes, including abundance changes in both clinically targeted and untargeted bacteria, as well as functional gene categories.CF sputum microbiota changed most markedly by 1 week of antibiotic therapy and plateaued thereafter, and this shift was largely driven by changes in non-dominant taxa. The genetically conferred functional capacities (ie, metagenomes) of subjects' sputum communities changed little with antibiotic perturbation, despite taxonomic shifts, suggesting functional redundancy within the CF sputum microbiome.MAIN RESULTSCF sputum microbiota changed most markedly by 1 week of antibiotic therapy and plateaued thereafter, and this shift was largely driven by changes in non-dominant taxa. The genetically conferred functional capacities (ie, metagenomes) of subjects' sputum communities changed little with antibiotic perturbation, despite taxonomic shifts, suggesting functional redundancy within the CF sputum microbiome.Maintenance treatment with inhaled tobramycin, an antibiotic with demonstrated long-term mortality benefit, primarily impacted clinically untargeted bacteria in CF sputum, highlighting the importance of monitoring the non-canonical effects of antibiotics and other treatments to accurately define and improve their clinical impact.CONCLUSIONSMaintenance treatment with inhaled tobramycin, an antibiotic with demonstrated long-term mortality benefit, primarily impacted clinically untargeted bacteria in CF sputum, highlighting the importance of monitoring the non-canonical effects of antibiotics and other treatments to accurately define and improve their clinical impact. The most common antibiotic used to treat people with cystic fibrosis (PWCF) is inhaled tobramycin, administered as maintenance therapy for chronic lung infections. While the effects of inhaled tobramycin on abundance and lung function diminish with continued therapy, this maintenance treatment is known to improve long-term outcomes, underscoring how little is known about why antibiotics work in CF infections, what their effects are on complex CF sputum microbiomes and how to improve these treatments. To rigorously define the effect of maintenance tobramycin on CF sputum microbiome characteristics. We collected sputum from 30 PWCF at standardised times before, during and after a single month-long course of maintenance inhaled tobramycin. We used traditional culture, quantitative PCR and metagenomic sequencing to define the dynamic effects of this treatment on sputum microbiomes, including abundance changes in both clinically targeted and untargeted bacteria, as well as functional gene categories. CF sputum microbiota changed most markedly by 1 week of antibiotic therapy and plateaued thereafter, and this shift was largely driven by changes in non-dominant taxa. The genetically conferred functional capacities (ie, metagenomes) of subjects' sputum communities changed little with antibiotic perturbation, despite taxonomic shifts, suggesting functional redundancy within the CF sputum microbiome. Maintenance treatment with inhaled tobramycin, an antibiotic with demonstrated long-term mortality benefit, primarily impacted clinically untargeted bacteria in CF sputum, highlighting the importance of monitoring the non-canonical effects of antibiotics and other treatments to accurately define and improve their clinical impact. |
| Author | McNamara, Sharon Bautista, Gilbert Hayden, Hillary S Brittnacher, Mitchell J Ravishankar, Sumedha Ratjen, Anina Miller, Samuel I Majors, Cheryl Borenstein, Elhanan Blackledge, Marcella Wolter, Daniel J Nay, Laura Nelson, Maria T Vo, Anh T Weiss, Eli J Eng, Alexander Hoffman, Luke R Simon, Richard H LiPuma, John J |
| AuthorAffiliation | 6 Microbiology, University of Washington School of Medicine, Seattle, Washington, USA 11 Pediatrics and Communicable Diseases, University of Michigan, Ann Arbor, Michigan, USA 2 Medical Scientist Training Program, University of Washington School of Medicine, Seattle, Washington, United States 9 Blavatnik School of Computer Science, Tel Aviv University, Tel Aviv, Israel 4 Pediatrics, Seattle Children's Hospital, Seattle, Washington, USA 3 Molecular and Cellular Biology, University of Washington School of Medicine, Seattle, Washington, United States 5 Genome Sciences, University of Washington School of Medicine, Seattle, Washington, USA 1 Pediatrics, University of Washington School of Medicine, Seattle, Washington, USA 10 Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv, Israel 7 Internal Medicine, University of Michigan, Ann Arbor, Michigan, USA 8 Department of Medicine, University of Washington School of Medicine, Seattle, Washington, United States |
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| Keywords | bacterial infection cystic fibrosis respiratory infection |
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| Notes | Original research ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 Contributors MTN, JJL, RHS, DJW and LRH performed conceptualisation and design of the study. MTN, DJW, ATV, SR, GB, AR, MB, SN, LN and CM helped in data collection. MTN, AE, EJW, MJB, EB and LRH performed the data analysis and interpretation. Resources were collected by MJB, HSH, SIM, MB, SN, LN and CM. MTN and LRH helped in writing the original draft. All authors helped in writing, review and editing of the article. MTN helped in visualisation, DJW, EB, JJL, RHS and LRH helped in supervision and LRH, JJL and RHS helped in acquisition of funds. |
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| Snippet | RationaleThe most common antibiotic used to treat people with cystic fibrosis (PWCF) is inhaled tobramycin, administered as maintenance therapy for chronic... The most common antibiotic used to treat people with cystic fibrosis (PWCF) is inhaled tobramycin, administered as maintenance therapy for chronic lung... The most common antibiotic used to treat people with cystic fibrosis (PWCF) is inhaled tobramycin, administered as maintenance therapy for chronic Pseudomonas... |
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| SubjectTerms | Administration, Inhalation Adolescent Adult Aged Anti-Bacterial Agents - pharmacology Anti-Bacterial Agents - therapeutic use Antibiotics Bacteria Bacteria - genetics Bacteria - isolation & purification bacterial infection Bacterial Infections - prevention & control Child Clinical outcomes Cystic fibrosis Cystic Fibrosis - microbiology Cystic Fibrosis - physiopathology Forced Expiratory Volume Genes Humans Maintenance Chemotherapy Metagenome - drug effects Microbiota Microbiota - drug effects Middle Aged Pathogens Respiratory infection Severity of Illness Index Spirometry Sputum - microbiology Staphylococcus infections Studies Taxonomy Time Factors Tobramycin - pharmacology Tobramycin - therapeutic use Young Adult |
| Title | Maintenance tobramycin primarily affects untargeted bacteria in the CF sputum microbiome |
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