Assessment of the Microbial Constituents of the Home Environment of Individuals with Cystic Fibrosis (CF) and Their Association with Lower Airways Infections

Heirali, Alya; McKeon, Suzanne; Purighalla, Swathi; Storey, Douglas G.; Rossi, Laura; Costilhes, Geoffrey; Drews, Steven J.; Rabin, Harvey; Surette, Michael G.; Parkins, Michael D.

doi:10.1371/journal.pone.0148534

Cited by 25 publications

(19 citation statements)

References 60 publications

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“…The introduction of ST395 during the construction of a hospital was already suspected in the United Kingdom (3). This is consistent with the frequent isolation of the ST395 clone in water (19,20) and the probable role of drinking water as a source of P. aeruginosa infection (21,22). Overall, the ST395 clone has presumably contaminated the water network of the hospital before its opening but the pathogen further spread among patients by other routes of transmission (e.g.…”

Section: Bessupporting

confidence: 74%

The rise and the fall of aPseudomonas aeruginosaepidemic lineage in a hospital

Petitjean

Juarez

Meunier³

et al. 2020

Preprint

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The biological features that allow a pathogen to survive in the hospital environment are mostly unknown. The extinction of bacterial epidemics in hospitals is mostly attributed to changes in medical practice, including infection control, but the role of bacterial adaptation has never been documented. We analyzed a collection of Pseudomonas aeruginosa isolates belonging to the Besançon Epidemic Strain (BES), responsible for a 12-year nosocomial outbreak, using a genotype-to-phenotype approach. Bayesian analysis estimated the emergence of the clone in the hospital five years before its opening, during the creation of its water distribution network made of copper. BES survived better than the reference strains PAO1 and PA14 in a copper solution due to a genomic island containing 13 metal-resistance genes and was specifically able to proliferate in the ubiquitous amoeba Vermamoeba vermiformis. Mutations affecting amino-acid metabolism, antibiotic resistance, lipopolysaccharide biosynthesis, and regulation were enriched during the spread of BES. Seven distinct regulatory mutations attenuated the overexpression of the genes encoding the efflux pump MexAB-OprM over time. The fitness of BES decreased over time in correlation with its genome size. Overall, the resistance to inhibitors and predators presumably aided the proliferation and propagation of BES in the plumbing system of the hospital. The pathogen further spread among patients via multiple routes of contamination. The decreased prevalence of patients infected by BES mirrored the parallel and convergent genomic evolution and reduction that affected bacterial fitness. Along with infection control measures, this may have participated in the extinction of BES in the hospital setting.ImportanceBacterial pathogens are responsible for nosocomial outbreaks, but the sources of contamination of the hospitals are mostly unclear and the role of bacterial evolution in the extinction of outbreaks has never been considered. Here, we found that an epidemic strain of the pathogen Pseudomonas aeruginosa contaminated the drinking water network of a hospital due to its tolerance to copper and predatory amoeba, both present in the water pipes. The extinction of the outbreak occurred concomitantly with parallel and convergent genome evolution and a reduction in the size of the bacterial genome that correlated with the fitness of the pathogen. Our data suggest that pathogen evolution participated in the extinction of an outbreak in a hospital setting.

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Section: Bessupporting

confidence: 74%

The rise and the fall of aPseudomonas aeruginosaepidemic lineage in a hospital

Petitjean

Juarez

Meunier³

et al. 2020

Preprint

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“…Given the ubiquity of P. aeruginosa in the natural environment and abundant data from more recent works [ 34 ] showing shared clonal but unrelated connected strains, we believe that the four patient-pairs with shared strains observed in our study are not due to cross-infection. We demonstrated through WGS that isolates differed much more between patients than within patients, suggesting independent environmental acquisition [ 17 , 34 , 35 ]. Our findings agree with recent evidence positing the likelihood of independent acquisition of isolates from the environment [ 14 , 15 ].…”

Section: Discussionmentioning

confidence: 99%

Epidemiology and natural history ofPseudomonas aeruginosaairway infections in non-cystic fibrosis bronchiectasis

et al. 2018

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The natural history and epidemiology of Pseudomonas aeruginosa infections in non-cystic fibrosis (non-CF) bronchiectasis is not well understood.As such it was our intention to determine the evolution of airway infection and the transmission potential of P. aeruginosa in patients with non-CF bronchiectasis.A longitudinal cohort study was conducted from 1986–2011 using a biobank of prospectively collected isolates from patients with non-CF bronchiectasis. Patients included were ≥18 years old and had ≥2 positive P. aeruginosa cultures over a minimum 6-month period. All isolates obtained at first and most recent clinical encounters, as well as during exacerbations, that were morphologically distinct on MacConkey agar were genotyped by pulsed-field gel electrophoresis (PFGE) and multilocus sequence typing (MLST). A total of 203 isolates from 39 patients were analysed. These were compared to a large collection of globally epidemic and local CF strains, as well as non-CF isolates.We identified four patterns of infection in non-CF bronchiectasis including: 1) persistence of a single strain (n=26; 67%); 2) strain displacement (n=8; 20%); 3) temporary disruption (n=3; 8%); and 4) chaotic airway infection (n=2; 5%). Patterns of infection were not significant predictors of rates of lung function decline or progression to end-stage disease and acquisition of new strains did not associate with the occurrence of exacerbations. Rarely, non-CF bronchiectasis strains with similar pulsotypes were observed in CF and non-CF controls, but no CF epidemic strains were observed. While rare shared strains were observed in non-CF bronchiectasis, whole-genome sequencing refuted patient–patient transmission.We observed a higher incidence of strain-displacement in our patient cohort compared to those observed in CF studies, although this did not impact on outcomes.

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“…A recent study assessed microbial constituents at home and found that the home environment (although rarely) can serve as either a source of infection or a persistent reservoir for reinfection. 33 …”

Section: Discussionmentioning

confidence: 99%

Cleaning and infection control of airway clearance devices used by CF patients

et al. 2017

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Respiratory treatment for cystic fibrosis (CF) patients includes use of respiratory devices. Contamination of airway clearance devices has not been adequately explored. We aimed to determine whether airway clearance devices are contaminated after use and whether cleaning guidelines for nebulizers are as effective for airway clearance devices. Patients brought their airway clearance devices to the clinic. Swabs from the devices were taken before and after cleaning and were cultured for bacterial counts. Total colony-forming units (CFU) was determined, and predominant colonies were identified using Matrix-Assisted Laser Desorption Ionization Time-of-Flight Mass Spectrometry technology. Thirty devices were collected from 23 patients. Most of the devices (28/30) were contaminated when brought to the clinic. Complete bacterial eradication was achieved in 15 (50%) samples and partial eradication in 9 (30%). The cleaning was totally ineffective in four samples. Median CFU decreased significantly from 1250 (IQR 25–75% 175–10.000) to 0 (IQR 25–75% 0–700) before and after cleaning (p < 0.0001). The predominant organisms were identified in five samples only, and there was no concordance with sputum culture results. Airway clearance devices are contaminated after use, and appropriate cleaning can reduce contamination. The effect on disease progression in CF patients is unclear. There is a need for infection prevention and control guidelines for the growing number of respiratory devices.

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Assessment of the Microbial Constituents of the Home Environment of Individuals with Cystic Fibrosis (CF) and Their Association with Lower Airways Infections

Cited by 25 publications

References 60 publications

The rise and the fall of aPseudomonas aeruginosaepidemic lineage in a hospital

The rise and the fall of aPseudomonas aeruginosaepidemic lineage in a hospital

Epidemiology and natural history ofPseudomonas aeruginosaairway infections in non-cystic fibrosis bronchiectasis

Cleaning and infection control of airway clearance devices used by CF patients

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