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Whole-genome sequencing for methicillin-resistant Staphylococcus aureus (MRSA) outbreak investigation in a neonatal intensive care unit

Published online by Cambridge University Press:  04 October 2018

Theresa Madigan ,
Scott A. Cunningham ,
Robin Patel ,
Kerryl E. Greenwood-Quaintance ,
Jean E. Barth ,
Priya Sampathkumar ,
Nicolynn C. Cole ,
Peggy C. Kohner ,
Christopher E. Colby  and
Garth F. Asay
...Show all authors
Theresa Madigan
Affiliation:
Division of Pediatric Infectious Diseases, Department of Pediatric and Adolescent Medicine, Mayo Clinic, Rochester, Minnesota
Scott A. Cunningham
Affiliation:
Division of Clinical Microbiology, Department of Laboratory Medicine and Pathology, Mayo Clinic Rochester, Minnesota
Robin Patel*
Affiliation:
Division of Clinical Microbiology, Department of Laboratory Medicine and Pathology, Mayo Clinic Rochester, Minnesota Division of Infectious Diseases, Department of Medicine, Mayo Clinic, Rochester, Minnesota
Kerryl E. Greenwood-Quaintance
Affiliation:
Division of Clinical Microbiology, Department of Laboratory Medicine and Pathology, Mayo Clinic Rochester, Minnesota
Jean E. Barth
Affiliation:
Infection Prevention and Control, Mayo Clinic, Rochester, Minnesota
Priya Sampathkumar
Affiliation:
Division of Infectious Diseases, Department of Medicine, Mayo Clinic, Rochester, Minnesota Infection Prevention and Control, Mayo Clinic, Rochester, Minnesota
Nicolynn C. Cole
Affiliation:
Division of Clinical Microbiology, Department of Laboratory Medicine and Pathology, Mayo Clinic Rochester, Minnesota
Peggy C. Kohner
Affiliation:
Division of Clinical Microbiology, Department of Laboratory Medicine and Pathology, Mayo Clinic Rochester, Minnesota
Christopher E. Colby
Affiliation:
Division of Neonatal Medicine, Department of Pediatric and Adolescent Medicine, Mayo Clinic, Rochester, Minnesota
Garth F. Asay
Affiliation:
Division of Neonatal Medicine, Department of Pediatric and Adolescent Medicine, Mayo Clinic, Rochester, Minnesota
Jennifer L. Fang
Affiliation:
Division of Neonatal Medicine, Department of Pediatric and Adolescent Medicine, Mayo Clinic, Rochester, Minnesota
Christine A. Baker
Affiliation:
Division of Neonatal Medicine, Department of Pediatric and Adolescent Medicine, Mayo Clinic, Rochester, Minnesota Department of Nursing, Mayo Clinic, Rochester, Minnesota
Angela L. Heinrich
Affiliation:
Division of Neonatal Medicine, Department of Pediatric and Adolescent Medicine, Mayo Clinic, Rochester, Minnesota Department of Nursing, Mayo Clinic, Rochester, Minnesota
Kelly A. Fjerstad
Affiliation:
Division of Neonatal Medicine, Department of Pediatric and Adolescent Medicine, Mayo Clinic, Rochester, Minnesota Department of Nursing, Mayo Clinic, Rochester, Minnesota
Maria J. Lujero
Affiliation:
Division of Neonatal Medicine, Department of Pediatric and Adolescent Medicine, Mayo Clinic, Rochester, Minnesota Department of Nursing, Mayo Clinic, Rochester, Minnesota
Nicholas Chia
Affiliation:
Department of Surgery, Mayo Clinic, Rochester, Minnesota Microbiome Program, Center for Individualized Medicine, Mayo Clinic, Rochester, Minnesota
Patricio R. Jeraldo
Affiliation:
Department of Surgery, Mayo Clinic, Rochester, Minnesota Microbiome Program, Center for Individualized Medicine, Mayo Clinic, Rochester, Minnesota
Heidi Nelson
Affiliation:
Department of Surgery, Mayo Clinic, Rochester, Minnesota Microbiome Program, Center for Individualized Medicine, Mayo Clinic, Rochester, Minnesota
W. Charles Huskins
Affiliation:
Division of Pediatric Infectious Diseases, Department of Pediatric and Adolescent Medicine, Mayo Clinic, Rochester, Minnesota Infection Prevention and Control, Mayo Clinic, Rochester, Minnesota
*
Author for correspondence: Robin Patel MD, Division of Clinical Microbiology, Department of Laboratory Medicine and Pathology, Mayo Clinic, Rochester, MN 55905. E-mail: patel.robin@mayo.edu
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Abstract

Objective

To evaluate whole-genome sequencing (WGS) as a molecular typing tool for MRSA outbreak investigation.

Design

Investigation of MRSA colonization/infection in a neonatal intensive care unit (NICU) over 3 years (2014–2017).

Setting

Single-center level IV NICU.

Patients

NICU infants and healthcare workers (HCWs).

Methods

Infants were screened for MRSA using a swab of the anterior nares, axilla, and groin, initially by targeted (ring) screening, and later by universal weekly screening. Clinical cultures were collected as indicated. HCWs were screened once using swabs of the anterior nares. MRSA isolates were typed using WGS with core-genome multilocus sequence typing (cgMLST) analysis and by pulsed-field gel electrophoresis (PFGE). Colonized and infected infants and HCWs were decolonized. Control strategies included reinforcement of hand hygiene, use of contact precautions, cohorting, enhanced environmental cleaning, and remodeling of the NICU.

Results

We identified 64 MRSA-positive infants: 53 (83%) by screening and 11 (17%) by clinical cultures. Of 85 screened HCWs, 5 (6%) were MRSA positive. WGS of MRSA isolates identified 2 large clusters (WGS groups 1 and 2), 1 small cluster (WGS group 3), and 8 unrelated isolates. PFGE failed to distinguish WGS group 2 and 3 isolates. WGS groups 1 and 2 were codistributed over time. HCW MRSA isolates were primarily in WGS group 1. New infant MRSA cases declined after implementation of the control interventions.

Conclusion

We identified 2 contemporaneous MRSA outbreaks alongside sporadic cases in a NICU. WGS was used to determine strain relatedness at a higher resolution than PFGE and was useful in guiding efforts to control MRSA transmission.

Type
Original Article
Information
Infection Control & Hospital Epidemiology , Volume 39 , Issue 12 , December 2018 , pp. 1412 - 1418
Copyright
© 2018 by The Society for Healthcare Epidemiology of America. All rights reserved. 

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Footnotes

PREVIOUS PRESENTATION: The results of this project were presented in part at the ASM Microbe 2017 meeting on June 5, 2017, in New Orleans, Louisiana, and at the Pediatric Academic Societies meeting on May 6, 2018, in Toronto, Canada.

Cite this article: Madigan T, et al. (2018). Whole-genome sequencing for methicillin-resistant Staphylococcus aureus (MRSA) outbreak investigation in a neonatal intensive care unit. Infection Control & Hospital Epidemiology 2018, 39, 1412–1418 doi: 10.1017/ice.2018.239

References

1. Song, X, Perencevich, E, Campos, J, Short, BL, Singh, N. Clinical and economic impact of methicillin-resistant Staphylococcus aureus colonization or infection on neonates in intensive care units. Infect Control Hosp Epidemiol 2010;31:177–182.Google Scholar
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.Google Scholar
3. Zervou, FN, Zacharioudakis, IM, Ziakas, PD, Mylonakis, E. MRSA colonization and risk of infection in the neonatal and pediatric ICU: a meta-analysis. Pediatrics 2014;133:e1015–e1023.Google Scholar
4. Huang, YC, Chou, YH, Su, LH, Lien, RI, Lin, TY. Methicillin-resistant Staphylococcus aureus colonization and its association with infection among infants hospitalized in neonatal intensive care units. Pediatrics 2006;118:469–474.Google Scholar
5. Gerber, SI, Jones, RC, Scott, MV, et al. Management of outbreaks of methicillin-resistant Staphylococcus aureus infection in the neonatal intensive care unit: a consensus statement. Infect Control Hosp Epidemiol 2006;27:139–145.Google Scholar
6. Struelens, MJ, Hawkey, PM, French, GL, Witte, W, Tacconelli, E. Laboratory tools and strategies for methicillin-resistant Staphylococcus aureus screening, surveillance and typing: state of the art and unmet needs. Clin Microbiol Infect 2009;15:112–119.Google Scholar
7. Koser, CU, Holden, MT, Ellington, MJ, et al. Rapid whole-genome sequencing for investigation of a neonatal MRSA outbreak. N Engl J Med 2012;366:2267–2275.Google Scholar
8. Azarian, T, Cook, RL, Johnson, JA, et al. Whole-genome sequencing for outbreak investigations of methicillin-resistant Staphylococcus aureus in the neonatal intensive care unit: Time for routine practice? Infect Control Hosp Epidemiol 2015;36:777–785.Google Scholar
9. Harris, SR, Cartwright, EJ, Torok, ME, et al. Whole-genome sequencing for analysis of an outbreak of meticillin-resistant Staphylococcus aureus: a descriptive study. Lancet Infect Dis 2013;13:130–136.Google Scholar
10. Azarian, T, Maraqa, NF, Cook, RL, et al. Genomic epidemiology of methicillin-resistant Staphylococcus aureus in a neonatal intensive care unit. PLoS One 2016;11(10):e0164397.Google Scholar
11. Ugolotti, E, Larghero, P, Vanni, I, et al. Whole-genome sequencing as standard practice for the analysis of clonality in outbreaks of meticillin-resistant Staphylococcus aureus in a paediatric setting. J Hosp Infect 2016;93:375–381.Google Scholar
12. Nubel, U, Nachtnebel, M, Falkenhorst, G, et al. MRSA transmission on a neonatal intensive care unit: epidemiological and genome-based phylogenetic analyses. PLoS One 2013;8(1):e54898.Google Scholar
13. Earls, MR, Coleman, DC, Brennan, GI, et al. Intra-hospital, inter-hospital and intercontinental spread of ST78 MRSA from two neonatal intensive care unit outbreaks established using whole-genome sequencing. Front Microbiol 2018;9:1485.Google Scholar
14. McDougal, LK, Steward, CD, Killgore, GE, Chaitram, JM, McAllister, SK, Tenover, FC. Pulsed-field gel electrophoresis typing of oxacillin-resistant Staphylococcus aureus isolates from the United States: establishing a national database. J Clin Microbiol 2003;41:5113–5120.Google Scholar
15. Cunningham, SA, Chia, N, Jeraldo, PR, et al. Comparison of whole-genome sequencing methods for analysis of three methicillin-resistant Staphylococcus aureus outbreaks. J Clin Microbiol. 2017;55:1946–1953.Google Scholar
16. Calfee, DP, Salgado, CD, Milstone, AM, et al. Strategies to prevent methicillin-resistant Staphylococcus aureus transmission and infection in acute care hospitals: 2014 update. Infect Control Hosp Epidemiol 2014;35:772–796.Google Scholar
17. Moore, G, Cookson, B, Gordon, NC, et al. Whole-genome sequencing in hierarchy with pulsed-field gel electrophoresis: the utility of this approach to establish possible sources of MRSA cross-transmission. J Hosp Infect 2015;90:38–45.Google Scholar
18. Garvey, MI, Pichon, B, Bradley, CW, Moiemen, NS, Oppenheim, B, Kearns, AM. Improved understanding of an outbreak of meticillin-resistant Staphylococcus aureus in a regional burns centre via whole-genome sequencing. J Hosp Infect 2016;94:401–404.Google Scholar
19. Diekema, DJ, Richter, SS, Heilmann, KP, et al. Continued emergence of USA300 methicillin-resistant Staphylococcus aureus in the United States: Results from a nationwide surveillance study. Infect Control Hosp Epidemiol 2014;35:285–292.Google Scholar
20. Richter, SS, Heilmann, KP, Dohrn, CL, et al. Activity of ceftaroline and epidemiologic trends in Staphylococcus aureus isolates collected from 43 medical centers in the United States in 2009. Antimicrob Agents Chemother 2011;55:4154–4160.Google Scholar
21. McAdams, RM, Ellis, MW, Trevino, S, Rajnik, M. Spread of methicillin-resistant Staphylococcus aureus USA300 in a neonatal intensive care unit. Pediatr Int 2008;50:810–815.Google Scholar
22. Popoola, VO, Budd, A, Wittig, SM, et al. Methicillin-resistant Staphylococcus aureus transmission and infections in a neonatal intensive care unit despite active surveillance cultures and decolonization: challenges for infection prevention. Infect Control Hosp Epidemiol 2014;35:412–418.Google Scholar
23. Nelson, MU, Bizzarro, MJ, Baltimore, RS, Dembry, LM, Gallagher, PG. Clinical and molecular epidemiology of methicillin-resistant Staphylococcus aureus in a neonatal intensive care unit in the decade following implementation of an active detection and isolation program. J Clin Microbiol 2015;53:2492–2501.Google Scholar
24. Kaushik, A, Kest, H, Zauk, A, DeBari, VA, Lamacchia, M. Impact of routine methicillin-resistant Staphylococcus aureus (MRSA) surveillance and cohorting on MRSA-related bloodstream infection in neonatal intensive care unit. Am J Perinatol 2015;32:531–536.Google Scholar
25. Gregory, ML, Eichenwald, EC, Puopolo, KM. Seven-year experience with a surveillance program to reduce methicillin-resistant Staphylococcus aureus colonization in a neonatal intensive care unit. Pediatrics 2009;123:e790–e796.Google Scholar
26. Khoury, J, Jones, M, Grim, A, Dunne, WM, Fraser, V. Eradication of methicillin-resistant Staphylococcus aureus from a neonatal intensive care unit by active surveillance and aggressive infection control measures. Infect Control Hosp Epidemiol 2005;26:616–621.Google Scholar
27. Coll, F, Harrison, EM, Toleman, MS, et al. Longitudinal genomic surveillance of MRSA in the UK reveals transmission patterns in hospitals and the community. Sci Transl Med 2017;9(413). pii: eaak9745.Google Scholar
28. Reuter, S, Torok, ME, Holden, MTG, et al. Building a genomic framework for prospective MRSA surveillance in the United Kingdom and the Republic of Ireland. Genome Res 2016;26:263–270.Google Scholar
29. Aanensen, DM, Feil, EJ, Holden, MT, et al. Whole-genome sequencing for routine pathogen surveillance in public health: a population snapshot of invasive Staphylococcus aureus in Europe. mBio 2016;7(3). doi: 10.1128/mBio.00444-16.Google Scholar
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