Genomic epidemiology of a protracted hospital outbreak caused by multidrug-resistant Acinetobacter baumannii in Birmingham, England

Abstract

Background: Multidrug-resistant Acinetobacter baumannii commonly causes hospital outbreaks. However, within an outbreak, it can be difficult to identify the routes of cross-infection rapidly and accurately enough to inform infection control. Here, we describe a protracted hospital outbreak of multidrug-resistant A. baumannii, in which whole-genome sequencing (WGS) was used to obtain a high-resolution view of the relationships between isolates.

Methods: To delineate and investigate the outbreak, we attempted to genome-sequence 114 isolates that had been assigned to the A. baumannii complex by the Vitek2 system and obtained informative draft genome sequences from 102 of them. Genomes were mapped against an outbreak reference sequence to identify single nucleotide variants (SNVs).

Results: We found that the pulsotype 27 outbreak strain was distinct from all other genome-sequenced strains. Seventy-four isolates from 49 patients could be assigned to the pulsotype 27 outbreak on the basis of genomic similarity, while WGS allowed 18 isolates to be ruled out of the outbreak. Among the pulsotype 27 outbreak isolates, we identified 31 SNVs and seven major genotypic clusters. In two patients, we documented within-host diversity, including mixtures of unrelated strains and within-strain clouds of SNV diversity. By combining WGS and epidemiological data, we reconstructed potential transmission events that linked all but 10 of the patients and confirmed links between clinical and environmental isolates. Identification of a contaminated bed and a burns theatre as sources of transmission led to enhanced environmental decontamination procedures.

Conclusions: WGS is now poised to make an impact on hospital infection prevention and control, delivering cost-effective identification of routes of infection within a clinically relevant timeframe and allowing infection control teams to track, and even prevent, the spread of drug-resistant hospital pathogens.

Figure 1

Chronology of the Acinetobacter baumannii pulsotype 27 outbreak in Birmingham, UK, 2011 to 2013, showing ward occupancy and other events for 52 patients. (a) The first phase of the outbreak, up to week 70. (b) A detailed view of the second phase of the outbreak, after week 70. Vertical bars indicate samples positive for MDR-Aci. The coloured horizontal bars indicate ward occupancy by patients carrying MDR-Aci. Patients are ordered by the SNV genotype of their MDR-Aci isolates, with major genotypes delineated by rectangles. Ward 1 cares mainly for burns and trauma patients; Ward 2 cares mainly for cardiac surgery patients, Ward 3 cares mainly for trauma patients; Ward 4 for plastic, ear-nose-and-throat, maxillofacial, trauma patients. * The first of three isolates obtained from patient 30 was not genome-sequenced. ° Patient 32 visited Ward 1 for 12 hours.

Figure 2

Genotypes obtained from 84 isolates from the Acinetobacter baumannii pulsotype 27 outbreak in Birmingham, UK, 2011 to 2013, including 74 clinical isolates from 49 patients and 10 environmental isolates. Numbers in red represent SNVs; ‘p’ indicates loss of plasmid; isolates in italics are plasmid-negative; dotted lines indicate alternative phylogenetic links (plasmid loss then SNV acquisition versus SNV acquisition then plasmid loss).