Infection Control & Hospital Epidemiology
when possible. Mothers of MRSA-positive infants were encour- aged to use their own breast pumps in a separate area rather than utilizing the lactation room. No further cases were identified during the following 5 months. Between May and October 2015, 5 MRSA-positive cases were
identified by clinical cultures and 12 more were identified by screening cultures (Figure 1A). Basic prevention practices were reinforced. When 17 more cases were identified between January and March of 2016, environmental sampling was performed to rule out ongoing transmission from a common environmental source. High-touch surfaces, such as drawers, counter tops, phones, patient vital-sign monitors, multiple areas in infant incubators, as well as other objects in patient rooms, utility and storage rooms and the lactation room, were sampled. None of the environmental samples grew MRSA, but adenosine triphosphate testing demonstrated an elevated bioburden on some surfaces. In response to these results, 4 patient rooms were closed in succes- sion for deep cleaning, and environmental services staff received additional training on proper cleaning and disinfection proce- dures. Procedures for reprocessing ophthalmologic equipment were improved. Compliance with contact precautions and hand hygiene was assessed through direct observations, and feedback was provided to staff by the IPAC team. Universal weekly screening of all infants in the unit was
implemented in April 2016 and continued throughout the remainder of the study (Fig. 1A). Because of additional cases, screening of HCWs began in July 2016 and was completed in November 2016. In total, 96 HCWs were selected for screening based on documentation of contact with MRSA colonized or infected infants in their electronic medical records (EMRs). These included physicians, advanced practice providers, nurses, physician assistants, sonography technologists, respiratory therapists, occu- pational therapists, child life specialists, and patient care assistants. Overall, 85 HCWs underwent screening, mostly in July 2016; the others were either unavailable for testing or were lost to follow-up. Five HCWs (6%) tested positive for MRSA (Fig. 1A) and under- went decolonization; all had subsequent negative testing in the weeks following decolonization. Screening was not repeated. Additional infant cases were identified from August to
December of 2016 but at a lower frequency than immediately prior to that time (Figure 1A). Environmental remodeling occurred in November 2016, including replacing the flooring, countertops and sinks, as well as minor updates to lighting and the ceiling. In 2017, 6 colonized infants were identified through surveillance screening.
Clinical information
Of the 64MRSA-positive infants identified between November 2014 and November 2017, 53 (83%) were initially identified by screening swabs. The other 11 infants (17%) were identified by cultures obtained due to clinical illness: surgical wound infection (n=1), bloodstream infection (BSI) (n=3), conjunctivitis (n=3), and sus- pected ventilator-associated pneumonia or tracheitis (n=4) (Fig. 1A). Of the 53 infants identified by screening, 15 (28%) developed con- firmed or suspected MRSA infections later in their hospitalization; the remainder (72%) had no clinical MRSA infection.
PFGE of MRSA isolates
In total, 58 MRSA isolates, 54 from infants and 4 from HCWs, were analyzed using molecular typing. Ten isolates from infants
1415
and 1 isolate from a HCW were unavailable for typing. PFGE identified 2 large clusters of related isolates (PFGE groups 1 and 2), with 25 isolates in each cluster: For HCWs, 3 HCW isolates were in PFGE group 1 and 1 HCW isolate was in PFGE group 2. In addition, 7 infant isolates were unrelated to each other and to PFGE groups 1 or 2. A single infant isolate failed PFGE analysis.
WGS of MRSA isolates
Among the 58 MRSA isolates, cgMLST also identified 2 major clusters (WGS group 1 and WGS group 2) and 1 minor cluster (WGS group 3) (Fig. 2). WGS group 1 was most closely related to the USA300 strain, and WGS groups 2 and 3 were most closely related to the USA100 strain (Fig. 2). Another 8 isolates were unique (Fig. 2). Infant cases included in WGS groups 1 and 2 occurred in parallel and were distributed over long periods of time (Fig. 1B).
Comparison of PFGE and WGS T of MRSA isolates
WGS group 1 included the same 25 isolates (22 infants, 3 HCWs) as PFGE group 1. WGS groups 2 and 3 together included the 25 isolates from PFGE group 2. Isolates in WGS group 3 differed from those in WGS group 2 by >30 alleles and were therefore separated from one another by the higher resolution of WGS cgMLST. The 2 isolates in WGS group 3 were from twin infants. The isolate that was not able to be characterized by PFGE was unrelated to all other isolates according to cgMLST.
Antimicrobial susceptibility
Antimicrobial susceptibilities for MRSA isolates by WGS group are shown in the Supplemental Table. The MRSA isolates in WGS group 1 were mostly susceptible to the tested antimicrobials (aside from oxacillin), whereas isolates in WGS groups 2 and 3 were generally resistant to levofloxacin and clindamycin.
Discussion
The existence of 2 contemporaneous outbreaks described herein would not have been recognized without screening of infants com- bined with the use of molecular typing. Importantly, 83% of MRSA- positive infants were detected initially by screening swabs. The implementation of universal weekly screening in April 2016 led to more rapid identification of new cases and implementation of addi- tional control measures. With the use of WGS, we discovered that 2 major clusters of related isolates occurred in parallel over a long period of time. Thus, WGS was a valuable tool for this outbreak investigation, offering benefit over antibiogram analysis and PFGE in determining isolate relatedness in more detail. WGS distinguished 2 isolates (WGS group 3) occurring in twin infants as distinct isolates not transmitted over time; PFGE did not distinguish these isolates from WGS group 2. Other researchers using WGS for MRSA out- break investigation have also shown that WGS can disprove trans- mission pathways suggested by conventional typing methods and thereby improve the understanding of an outbreak.8,17,18 Notably, the WGS bioinformatics and reporting algorithms we used allow easy and near-real-time longitudinal comparison of isolates. We were able to identify the reappearance of 3WGS group 2 isolates in the fall of 2017, a year after the previous WGS group 2 isolate occurred in September 2016, in addition to a unique isolate (Fig. 1B).
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