Genotypic Diversity within a Single Pseudomonas aeruginosa Strain Commonly Shared by Australian Patients with Cystic Fibrosis
In cystic fibrosis (CF), Pseudomonas aeruginosa undergoes intra-strain genotypic and phenotypic diversification while establishing and maintaining chronic lung infections. As the clinical significance of these changes is uncertain, we investigated intra-strain diversity in commonly shared strains fr...
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| Veröffentlicht in: | PloS one 2015-12, Vol.10 (12), p.e0144022-e0144022 |
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| creator | Tai, Anna Sze Bell, Scott Cameron Kidd, Timothy James Trembizki, Ella Buckley, Cameron Ramsay, Kay Annette David, Michael Wainwright, Claire Elizabeth Grimwood, Keith Whiley, David Mark |
| description | In cystic fibrosis (CF), Pseudomonas aeruginosa undergoes intra-strain genotypic and phenotypic diversification while establishing and maintaining chronic lung infections. As the clinical significance of these changes is uncertain, we investigated intra-strain diversity in commonly shared strains from CF patients to determine if specific gene mutations were associated with increased antibiotic resistance and worse clinical outcomes. Two-hundred-and-one P. aeruginosa isolates (163 represented a dominant Australian shared strain, AUST-02) from two Queensland CF centres over two distinct time-periods (2001-2002 and 2007-2009) underwent mexZ and lasR sequencing. Broth microdilution antibiotic susceptibility testing in a subset of isolates was also performed. We identified a novel AUST-02 subtype (M3L7) in adults attending a single Queensland CF centre. This M3L7 subtype was multi-drug resistant and had significantly higher antibiotic minimum inhibitory concentrations than other AUST-02 subtypes. Prospective molecular surveillance using polymerase chain reaction assays determined the prevalence of the 'M3L7' subtype at this centre during 2007-2009 (170 patients) and 2011 (173 patients). Three-year clinical outcomes of patients harbouring different strains and subtypes were compared. MexZ and LasR sequences from AUST-02 isolates were more likely in 2007-2009 than 2001-2002 to exhibit mutations (mexZ: odds ratio (OR) = 3.8; 95% confidence interval (CI): 1.1-13.5 and LasR: OR = 2.5; 95%CI: 1.3-5.0). Surveillance at the adult centre in 2007-2009 identified M3L7 in 28/509 (5.5%) P. aeruginosa isolates from 13/170 (7.6%) patients. A repeat survey in 2011 identified M3L7 in 21/519 (4.0%) P. aeruginosa isolates from 11/173 (6.4%) patients. The M3L7 subtype was associated with greater intravenous antibiotic and hospitalisation requirements, and a higher 3-year risk of death/lung transplantation, than other AUST-02 subtypes (adjusted hazard ratio [HR] = 9.4; 95%CI: 2.2-39.2) and non-AUST-02 strains (adjusted HR = 4.8; 95%CI: 1.4-16.2). This suggests ongoing microevolution of the shared CF strain, AUST-02, was associated with an emerging multi-drug resistant subtype and possibly poorer clinical outcomes. |
| doi_str_mv | 10.1371/journal.pone.0144022 |
| format | Article |
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As the clinical significance of these changes is uncertain, we investigated intra-strain diversity in commonly shared strains from CF patients to determine if specific gene mutations were associated with increased antibiotic resistance and worse clinical outcomes. Two-hundred-and-one P. aeruginosa isolates (163 represented a dominant Australian shared strain, AUST-02) from two Queensland CF centres over two distinct time-periods (2001-2002 and 2007-2009) underwent mexZ and lasR sequencing. Broth microdilution antibiotic susceptibility testing in a subset of isolates was also performed. We identified a novel AUST-02 subtype (M3L7) in adults attending a single Queensland CF centre. This M3L7 subtype was multi-drug resistant and had significantly higher antibiotic minimum inhibitory concentrations than other AUST-02 subtypes. Prospective molecular surveillance using polymerase chain reaction assays determined the prevalence of the 'M3L7' subtype at this centre during 2007-2009 (170 patients) and 2011 (173 patients). Three-year clinical outcomes of patients harbouring different strains and subtypes were compared. MexZ and LasR sequences from AUST-02 isolates were more likely in 2007-2009 than 2001-2002 to exhibit mutations (mexZ: odds ratio (OR) = 3.8; 95% confidence interval (CI): 1.1-13.5 and LasR: OR = 2.5; 95%CI: 1.3-5.0). Surveillance at the adult centre in 2007-2009 identified M3L7 in 28/509 (5.5%) P. aeruginosa isolates from 13/170 (7.6%) patients. A repeat survey in 2011 identified M3L7 in 21/519 (4.0%) P. aeruginosa isolates from 11/173 (6.4%) patients. The M3L7 subtype was associated with greater intravenous antibiotic and hospitalisation requirements, and a higher 3-year risk of death/lung transplantation, than other AUST-02 subtypes (adjusted hazard ratio [HR] = 9.4; 95%CI: 2.2-39.2) and non-AUST-02 strains (adjusted HR = 4.8; 95%CI: 1.4-16.2). This suggests ongoing microevolution of the shared CF strain, AUST-02, was associated with an emerging multi-drug resistant subtype and possibly poorer clinical outcomes.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0144022</identifier><identifier>PMID: 26633539</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Adult ; Adults ; Anti-Bacterial Agents - pharmacology ; Anti-Bacterial Agents - therapeutic use ; Antibiotic resistance ; Antibiotics ; Australia ; Biodiversity ; Children & youth ; Clinics ; Complications and side effects ; Confidence intervals ; Cystic fibrosis ; Cystic Fibrosis - microbiology ; Distribution ; Drug resistance ; Epidemics ; Female ; Genes, Bacterial ; Genetic Variation ; Health aspects ; Hospitals ; Humans ; Infections ; Intravenous administration ; Laboratories ; Lung transplantation ; Male ; Medical research ; Medicine ; Microbial Sensitivity Tests ; Mortality ; Multidrug resistance ; Mutation ; Pathogens ; Patients ; Physiological aspects ; Polymerase chain reaction ; Pseudomonas aeruginosa ; Pseudomonas aeruginosa - drug effects ; Pseudomonas aeruginosa - genetics ; Strains (organisms) ; Surveillance ; Thorax ; Transplantation ; Treatment Outcome ; Young Adult</subject><ispartof>PloS one, 2015-12, Vol.10 (12), p.e0144022-e0144022</ispartof><rights>COPYRIGHT 2015 Public Library of Science</rights><rights>2015 Tai et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2015 Tai et al 2015 Tai et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c692t-481831ac993d0688e0a7174b89b4f1b66c4fd0727e4983b9d3bdfaba038eea2d3</citedby><cites>FETCH-LOGICAL-c692t-481831ac993d0688e0a7174b89b4f1b66c4fd0727e4983b9d3bdfaba038eea2d3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4669131/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4669131/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,315,728,781,785,865,886,2103,2929,23871,27929,27930,53796,53798</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/26633539$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Chotirmall, Sanjay Haresh</contributor><creatorcontrib>Tai, Anna Sze</creatorcontrib><creatorcontrib>Bell, Scott Cameron</creatorcontrib><creatorcontrib>Kidd, Timothy James</creatorcontrib><creatorcontrib>Trembizki, Ella</creatorcontrib><creatorcontrib>Buckley, Cameron</creatorcontrib><creatorcontrib>Ramsay, Kay Annette</creatorcontrib><creatorcontrib>David, Michael</creatorcontrib><creatorcontrib>Wainwright, Claire Elizabeth</creatorcontrib><creatorcontrib>Grimwood, Keith</creatorcontrib><creatorcontrib>Whiley, David Mark</creatorcontrib><title>Genotypic Diversity within a Single Pseudomonas aeruginosa Strain Commonly Shared by Australian Patients with Cystic Fibrosis</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>In cystic fibrosis (CF), Pseudomonas aeruginosa undergoes intra-strain genotypic and phenotypic diversification while establishing and maintaining chronic lung infections. As the clinical significance of these changes is uncertain, we investigated intra-strain diversity in commonly shared strains from CF patients to determine if specific gene mutations were associated with increased antibiotic resistance and worse clinical outcomes. Two-hundred-and-one P. aeruginosa isolates (163 represented a dominant Australian shared strain, AUST-02) from two Queensland CF centres over two distinct time-periods (2001-2002 and 2007-2009) underwent mexZ and lasR sequencing. Broth microdilution antibiotic susceptibility testing in a subset of isolates was also performed. We identified a novel AUST-02 subtype (M3L7) in adults attending a single Queensland CF centre. This M3L7 subtype was multi-drug resistant and had significantly higher antibiotic minimum inhibitory concentrations than other AUST-02 subtypes. Prospective molecular surveillance using polymerase chain reaction assays determined the prevalence of the 'M3L7' subtype at this centre during 2007-2009 (170 patients) and 2011 (173 patients). Three-year clinical outcomes of patients harbouring different strains and subtypes were compared. MexZ and LasR sequences from AUST-02 isolates were more likely in 2007-2009 than 2001-2002 to exhibit mutations (mexZ: odds ratio (OR) = 3.8; 95% confidence interval (CI): 1.1-13.5 and LasR: OR = 2.5; 95%CI: 1.3-5.0). Surveillance at the adult centre in 2007-2009 identified M3L7 in 28/509 (5.5%) P. aeruginosa isolates from 13/170 (7.6%) patients. A repeat survey in 2011 identified M3L7 in 21/519 (4.0%) P. aeruginosa isolates from 11/173 (6.4%) patients. The M3L7 subtype was associated with greater intravenous antibiotic and hospitalisation requirements, and a higher 3-year risk of death/lung transplantation, than other AUST-02 subtypes (adjusted hazard ratio [HR] = 9.4; 95%CI: 2.2-39.2) and non-AUST-02 strains (adjusted HR = 4.8; 95%CI: 1.4-16.2). This suggests ongoing microevolution of the shared CF strain, AUST-02, was associated with an emerging multi-drug resistant subtype and possibly poorer clinical outcomes.</description><subject>Adult</subject><subject>Adults</subject><subject>Anti-Bacterial Agents - pharmacology</subject><subject>Anti-Bacterial Agents - therapeutic use</subject><subject>Antibiotic resistance</subject><subject>Antibiotics</subject><subject>Australia</subject><subject>Biodiversity</subject><subject>Children & youth</subject><subject>Clinics</subject><subject>Complications and side effects</subject><subject>Confidence intervals</subject><subject>Cystic fibrosis</subject><subject>Cystic Fibrosis - microbiology</subject><subject>Distribution</subject><subject>Drug resistance</subject><subject>Epidemics</subject><subject>Female</subject><subject>Genes, Bacterial</subject><subject>Genetic Variation</subject><subject>Health aspects</subject><subject>Hospitals</subject><subject>Humans</subject><subject>Infections</subject><subject>Intravenous administration</subject><subject>Laboratories</subject><subject>Lung transplantation</subject><subject>Male</subject><subject>Medical research</subject><subject>Medicine</subject><subject>Microbial Sensitivity Tests</subject><subject>Mortality</subject><subject>Multidrug resistance</subject><subject>Mutation</subject><subject>Pathogens</subject><subject>Patients</subject><subject>Physiological aspects</subject><subject>Polymerase chain reaction</subject><subject>Pseudomonas aeruginosa</subject><subject>Pseudomonas aeruginosa - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Tai, Anna Sze</au><au>Bell, Scott Cameron</au><au>Kidd, Timothy James</au><au>Trembizki, Ella</au><au>Buckley, Cameron</au><au>Ramsay, Kay Annette</au><au>David, Michael</au><au>Wainwright, Claire Elizabeth</au><au>Grimwood, Keith</au><au>Whiley, David Mark</au><au>Chotirmall, Sanjay Haresh</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Genotypic Diversity within a Single Pseudomonas aeruginosa Strain Commonly Shared by Australian Patients with Cystic Fibrosis</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2015-12-03</date><risdate>2015</risdate><volume>10</volume><issue>12</issue><spage>e0144022</spage><epage>e0144022</epage><pages>e0144022-e0144022</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>In cystic fibrosis (CF), Pseudomonas aeruginosa undergoes intra-strain genotypic and phenotypic diversification while establishing and maintaining chronic lung infections. As the clinical significance of these changes is uncertain, we investigated intra-strain diversity in commonly shared strains from CF patients to determine if specific gene mutations were associated with increased antibiotic resistance and worse clinical outcomes. Two-hundred-and-one P. aeruginosa isolates (163 represented a dominant Australian shared strain, AUST-02) from two Queensland CF centres over two distinct time-periods (2001-2002 and 2007-2009) underwent mexZ and lasR sequencing. Broth microdilution antibiotic susceptibility testing in a subset of isolates was also performed. We identified a novel AUST-02 subtype (M3L7) in adults attending a single Queensland CF centre. This M3L7 subtype was multi-drug resistant and had significantly higher antibiotic minimum inhibitory concentrations than other AUST-02 subtypes. Prospective molecular surveillance using polymerase chain reaction assays determined the prevalence of the 'M3L7' subtype at this centre during 2007-2009 (170 patients) and 2011 (173 patients). Three-year clinical outcomes of patients harbouring different strains and subtypes were compared. MexZ and LasR sequences from AUST-02 isolates were more likely in 2007-2009 than 2001-2002 to exhibit mutations (mexZ: odds ratio (OR) = 3.8; 95% confidence interval (CI): 1.1-13.5 and LasR: OR = 2.5; 95%CI: 1.3-5.0). Surveillance at the adult centre in 2007-2009 identified M3L7 in 28/509 (5.5%) P. aeruginosa isolates from 13/170 (7.6%) patients. A repeat survey in 2011 identified M3L7 in 21/519 (4.0%) P. aeruginosa isolates from 11/173 (6.4%) patients. The M3L7 subtype was associated with greater intravenous antibiotic and hospitalisation requirements, and a higher 3-year risk of death/lung transplantation, than other AUST-02 subtypes (adjusted hazard ratio [HR] = 9.4; 95%CI: 2.2-39.2) and non-AUST-02 strains (adjusted HR = 4.8; 95%CI: 1.4-16.2). This suggests ongoing microevolution of the shared CF strain, AUST-02, was associated with an emerging multi-drug resistant subtype and possibly poorer clinical outcomes.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>26633539</pmid><doi>10.1371/journal.pone.0144022</doi><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 1932-6203 |
| ispartof | PloS one, 2015-12, Vol.10 (12), p.e0144022-e0144022 |
| issn | 1932-6203 1932-6203 |
| language | eng |
| recordid | cdi_plos_journals_1739077386 |
| source | MEDLINE; DOAJ Directory of Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; Public Library of Science (PLoS) Journals Open Access; PubMed Central; Free Full-Text Journals in Chemistry |
| subjects | Adult Adults Anti-Bacterial Agents - pharmacology Anti-Bacterial Agents - therapeutic use Antibiotic resistance Antibiotics Australia Biodiversity Children & youth Clinics Complications and side effects Confidence intervals Cystic fibrosis Cystic Fibrosis - microbiology Distribution Drug resistance Epidemics Female Genes, Bacterial Genetic Variation Health aspects Hospitals Humans Infections Intravenous administration Laboratories Lung transplantation Male Medical research Medicine Microbial Sensitivity Tests Mortality Multidrug resistance Mutation Pathogens Patients Physiological aspects Polymerase chain reaction Pseudomonas aeruginosa Pseudomonas aeruginosa - drug effects Pseudomonas aeruginosa - genetics Strains (organisms) Surveillance Thorax Transplantation Treatment Outcome Young Adult |
| title | Genotypic Diversity within a Single Pseudomonas aeruginosa Strain Commonly Shared by Australian Patients with Cystic Fibrosis |
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