Infection Control & Hospital Epidemiology The clusters in our study were most closely related to USA100
(WGS groups 2 and 3) and to USA300 (WGS group 1). The USA100 strain is a common healthcare-associated strain that is typically multidrug resistant,14 and the USA300 strain is considered a community-associated strain that is generally susceptible to most antibiotics,14 consistent with our findings. However, surveillance stu- dies have demonstrated that USA300 is now as common as or more common than USA100 as a cause of nosocomial infection.19,20 Indeed, USA300 has been the cause of other reported outbreaks within NICUs, 8,21 and several authors have described the concomitant presence of USA100 and USA300 in their units,22,23 which highlights the increasingly blurred distinction between hospital and community strains. In addition to the 2 major clusters, we found 8 unique isolates, which is commonly observed as well.10,22,23 These findings demon- strate that multiple sources of transmission exist within as well as outside the unit. Our report underscores the complexity of the transmission dynamics and the difficulty in identifying effective pre- vention and control strategies. Previous studies indicate thatMRSA surveillance with cohorting
of colonized infants and the use of contact precautions may reduce the transmission of MRSA to other infants.23,24 This is important because colonized infants have a higher risk of developing infection with MRSA than those who are not colonized,3,4,24 and decoloni- zation is often unsuccessful in this population.22 In our study a quarter of colonized infants developed confirmed or suspected infection with MRSA during their hospitalization, a rate similar to other reports.4,22 In our study, as in others,22,25 infection control practices alone with or without infant decolonization were insuf- ficient to stop transmission. Environmental screening did not identify an environmental source, and deep cleaning of infant rooms was not successful in preventing ongoing transmission. As WGS data suggested horizontal transmission, HCWs were screened. Those who were positive were colonized primarily with WGS group 1 isolates (n=3), with 1 HCW harboring a WGS group 2 isolate. The disappearance of WGS group 1 after March 2017 suggests that screening and treatment of colonized HCWs may have assisted in control efforts. Other investigators have reported success with this strategy.26 However, WGS group 2 reappeared in the fall of 2017, which suggests persistent reservoirs in our unit that have not been identified. This reappearance could also represent recolonization of a previously colonized HCW, as described by others studies in which 80% of previously treated HCWs were positive again several months later.22 The HCWs in our study were rescreened after decolonization and were negative, but no further screening was performed to assess the long-term success of decolonization. With the use of WGS, a database of NICU MRSA isolates was established. This allowed analysis of isolates in real time as new cases were identified, and it will continue to be used for long- itudinal comparison of new isolates to tailor replace with IPAC strategies. For example, the recurrence of previous outbreak strains could lead to repeated screening and decolonization of HCWs, whereas the ongoing introduction of unique strains could focus interventions on education and reinforcement of hand hygiene in visitors and family members, or potentially family member screening and decolonization. Although this approach could be accomplished with sophisticated PFGE analysis software and databases, it would be technically more challenging than using WGS. Furthermore, the WGS data are portable and can be used for comparison with other isolates within our institution or can potentially be shared with other institutions without the difficulty of interlaboratory comparison and standardization
1417
expected with PFGE data. Researchers in Europe have already applied MRSA WGS technology on a larger scale,13,27–29 demonstrating the power of this technology for investigating outbreaks as well as the potential for pathogen surveillance on regional, national, and international levels. This study has several limitations. Universal weekly screening
of infants was not implemented until April 2016; therefore, some cases of MRSA colonization before that time may have gone undetected. The HCWs were selected for screening based on contact with MRSA colonized or infected infants documented in the EMR. This selection strategy was expected to capture most providers, but it may have missed HCWs whose care activities were not documented in the EMR. In addition, a few HCWs were not available for screening, and visitors and family members of infants were not screened. Finally, only 1 isolate from each infant and HCW was sequenced; therefore, colonization with >1 strain of MRSA would not have been detected. In summary, WGS is a powerful tool for MRSA outbreak
investigation that provides more detailed information on isolate relatedness than other conventional typing techniques, such as PFGE. This approach may be helpful in dissecting complex transmission pathways. In addition, WGS data allows for easy and near-real-time longitudinal comparison of isolates by establishing a database of sequenced isolates. Thus,WGS characterization of strains is expected to become the preferred method for molecular typing with the potential for data sharing and application on a wide scale.
Supplementary material. To view supplementary material for this article, please visit
https://doi.org/10.1017/ice.2018.239
Acknowledgments. We thank the physicians, nurses, and other staff in the NICU for their excellent patient care and help with this investigation. We also thank the staff in the clinical microbiology laboratory for their help with isolate acquisition, storage, processing, and analysis. Finally, we thank the Mayo Clinic Center for Individualized Medicine for their assistance with development of the WGS platform.
Financial support. This research was graciously supported by the Mayo Clinic Center for Individualized Medicine.
Conflicts of interest. Dr Patel reports grants from CD Diagnostics, BioFire, Curetis, Merck, Hutchison Biofilm Medical Solutions, Accelerate Diagnostics, Allergan, and The Medicines Company. Dr Patel is or has been a consultant to Curetis, Qvella, St. Jude, Beckman Coulter, Morgan Stanley, Heraeus Medical GmbH, CORMATRIX, Specific Technologies, Diaxonit, Selux Dx, GenMark Diagnostics, LBT Innovations Ltd, PathoQuest and Genentech; monies are paid to Mayo Clinic. In addition, Dr. Patel has a patent on Bordetella pertussis/ parapertussis PCR, a patent on a device/method for sonication with royalties paid by Samsung to Mayo Clinic, and a patent on an antibiofilm substance. Dr Patel receives travel reimbursement from ASM and IDSA and an editor’s stipend from ASM and IDSA, as well as honoraria from the NBME, Up-to- Date, and the Infectious Diseases Board Review Course. Dr Sampathkumar served as a consultant as a member of an advisory board on an experimental Zika vaccine. All other authors declare no conflicts of interest.
References
1. Song X, Perencevich E, Campos J, Short BL, Singh N. Clinical and economic impact of methicillin-resistant Staphylococcus aureus coloniza- tion or infection on neonates in intensive care units. Infect Control Hosp Epidemiol 2010;31:177–182.
2. Schultz ED, Tanaka DT, Goldberg RN, Benjamin DK Jr, Smith PB. Effect of methicillin-resistant Staphylococcus aureus colonization in the neonatal intensive care unit on total hospital cost. Infect Control Hosp Epidemiol 2009;30:383–385.
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