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Association of an Active Surveillance and Decolonization Program on Incidence of Clinical Cultures Growing Staphylococcus aureus in the Neonatal Intensive Care Unit

Published online by Cambridge University Press:  20 April 2018

Annie Voskertchian ,
Ibukunoluwa C. Akinboyo ,
Elizabeth Colantuoni ,
Julia Johnson  and
Aaron M. Milstone
Annie Voskertchian
Affiliation:
Division of Infectious Disease, Department of Pediatrics, Johns Hopkins University, Baltimore, Maryland
Ibukunoluwa C. Akinboyo
Affiliation:
Division of Infectious Disease, Department of Pediatrics, Johns Hopkins University, Baltimore, Maryland
Elizabeth Colantuoni
Affiliation:
Department of Biostatistics, Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland.
Julia Johnson
Affiliation:
Division of Neonatology, Department of Pediatrics, Johns Hopkins University, Baltimore, Maryland
Aaron M. Milstone*
Affiliation:
Division of Infectious Disease, Department of Pediatrics, Johns Hopkins University, Baltimore, Maryland
*
Address correspondence to Aaron M. Milstone, MD, MHS, 200 N Wolfe St, Baltimore MD 21287 (amilsto1@jhmi.edu).
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Abstract

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Type
Research Brief
Information
Infection Control & Hospital Epidemiology , Volume 39 , Issue 7 , July 2018 , pp. 882 - 884
Copyright
© 2018 by The Society for Healthcare Epidemiology of America. All rights reserved. 

Staphylococcus aureus remains a leading cause of hospital-acquired infections (HAIs) in neonates.Reference Verstraete, Boelens and De Coen 1 Some neonatal intensive care units (NICUs) use active surveillance cultures (ASCs) and decolonization to prevent methicillin-resistant S. aureus (MRSA) transmission and infections.Reference Huang, Lien, Su, Chou and Lin 2 However, methicillin-susceptible S. aureus (MSSA) infections occur more frequently and have similar mortality in neonates.Reference Ericson, Popoola and Smith 3

In The Johns Hopkins NICU, prior to April 2013, neonates were screened for MRSA colonization and carriers were decolonized.Reference Popoola, Colantuoni and Suwantarat 4 In April 2013, the program expanded to include MSSA screening and decolonization. Previously, we showed that after implementation of MSSA ASCs and targeted decolonization, S. aureus clinical cultures and infections decreased.Reference Popoola, Colantuoni and Suwantarat 4 Our objective was to assess whether the reduction was sustained over 3 years.

METHODS

Using The Johns Hopkins Pathology information system, we retrospectively identified neonates admitted to the NICU between April 1, 2011, and June 30, 2016. Clinical cultures positive for Staphylococcus aureus were defined as nonsurveillance cultures growing S. aureus. Cultures from the same patient were considered unique events if they were collected from the same body site at least 30 days apart or from different body sites at least 14 days apart. NICU-attributable was defined as clinical cultures obtained >2 days after unit admission. A neonate was considered to have a bloodstream infection (BSI) if a blood culture grew S. aureus. Incidence rates for NICU-attributable S. aureus clinical cultures and BSIs and 95% confidence intervals (CI) were calculated for the pre- and post-intervention periods and were compared using 2-sample Poisson tests. Interrupted time series models were fit to the log-transformed quarterly incidence rates to quantify the immediate impact of the program, and the relative change in incidence rates per quarter during the pre- and postintervention period.Reference Popoola, Colantuoni and Suwantarat 4 Our institutional review board approved this study.

RESULTS

During the 24 months before implementation of the intervention (29,200 patient days) and 39 months post-implementation (47,135 patient days), 74 and 68 NICU-attributable S. aureus clinical cultures occurred, respectively. There were 116 unique patients with 142 S. aureus cultures, of which 131 (92%) were MSSA and 11 (8%) were MRSA. Sources for the 142 isolates included 84 (59.2 %) respiratory, 20 (14%) blood, 10 (7.0%) conjunctiva, 11 (7.7%) wound, 7 (4.9%) other, 5 urine (3.5%), 3 abscess (2.1%), and 2 cerebral spinal fluid (1.4%). In the post-intervention period, 1,847 neonates were screened for S. aureus colonization as part of the ASC and decolonization program. Of the 333 colonized patients, 243 were treated with mupirocin.

Overall, a 43% reduction in the incidence rate of S. aureus clinical isolates occurred when comparing the post- to the pre-intervention period (IRR, 0.57; 95% CI, 0.40–0.80) (Figure 1a). Prior to the intervention, the incidence rate of S. aureus clinical cultures was estimated to increase at a nonsignificant rate of 14% per quarter (IRR, 1.14; 95% CI, 0.95–1.38). In the quarter following introduction of MSSA to the ASC program, we observed an immediate 65% decrease (IRR, 0.35; 95% CI, 0.15–0.82); thereafter, we observed an estimated 2.0% quarterly decrease in the incidence of NICU-attributable S. aureus clinical cultures (IRR, 0.98; 95% CI, 0.92–1.05). The rate at which the incidence rates changed over time during the pre- and post-intervention periods did not differ statistically (estimated relative quarterly rate of change, 0.86; P = .12).

FIGURE 1 (A) Quarterly incidence rate of Staphylococcus aureus clinical cultures before (April 1, 2011–March 30, 2013) and after (April 1, 2013–June 30, 2016) implementation of a methicillin-susceptible S. aureus (MSSA) and methicillin-resistant S. aureus (MRSA) active surveillance and decolonization protocol. Dashed horizontal lines show the average incidence rate of S. aureus during the pre- and postintervention periods and the dashed vertical line represents start of intervention (Quarter 9). MRSA and MSSA are depicted in black and gray, respectively. (B) Quarterly incidence rate of S. aureus bloodstream infections (BSIs) before and after implementation of a methicillin-susceptible S. aureus (MSSA) and methicillin-resistant S. aureus (MRSA) active surveillance and decolonization protocol.

Prior to the intervention, there was no change in the incidence rate of BSIs (IRR, 1.00; 95% CI, 0.78–1.29). After implementation, there were statistically nonsignificant reductions (1) in the overall incidence rate of S. aureus BSIs (IRR, 0.50; 95% CI, 0.18–1.34) (Figure 1b), (2) in the immediate change in rate of S. aureus BSIs (IRR, 0.73; 95% CI, 0.20–2.58), and (3) in the quarterly incidence rate of S. aureus BSIs (IRR, 0.97; 95% CI, 0.92–1.03).

With an average of 5.5 BSIs per year in the pre-intervention period, 18 BSIs were expected to occur in the post-intervention period, yet we observed 9. In the setting of ≥70% compliance with the decolonization protocol, 50% fewer infections occurred than expected, suggesting that 27 neonates were treated to prevent 1 BSI.

DISCUSSION

Our data suggest that an active MSSA screening and decolonization program in the NICU can lead to a sustained reduction (43% overall) in the incidence of clinical S. aureus isolates.

Prior studies have found that ASC and decolonization, in conjunction with other infection control measures, can reduce MRSA colonization and infection.Reference Huang, Lien, Su, Chou and Lin 2 , Reference Delaney, Wang and Melish 5 The burden of MSSA infections exceeds that of MRSA infections in the NICU,Reference Ericson, Popoola and Smith 3 yet few studies have examined the impact of MSSA ASC and decolonization. Recently, Wisgrill et alReference Wisgrill, Zizka and Unterasinger 6 reported promising results of an MSSA surveillance and decolonization program that led to a 50% reduction of MSSA-attributable infections in very low-birth-weight infants. Our study reports similar findings, and we included all neonates admitted to the NICU to reflect the impact on overall burden of S. aureus HAIs.

Efficacy, cost-effectiveness, and safety influence the decision to perform ASCs and decolonization. While neonatal data are limited, reports from adult populations suggest that active surveillance, targeted decolonization, and at times, universal decolonization are cost-effective compared to other prevention methods.Reference Whittington, Atherly, Curtis, Lindrooth, Bradley and Campbell 7 Possible unintended consequences of decolonization include replacing S. aureus with more virulent pathogens. However, in a multicenter NICU study examining MRSA decolonization, patients treated with mupirocin did not show increased risk of novel gram-negative and fungal infections.Reference Pierce, Bryant, Elward, Lessler and Milstone 8 Emerging resistance to mupirocin must also be considered with widespread use, but recent S. aureus ASC and decolonization programs have not found an increase in resistance to mupirocin.Reference Popoola, Colantuoni and Suwantarat 4 – Reference Wisgrill, Zizka and Unterasinger 6 , Reference Hayden, Lolans and Haffenreffer 9

Incorporating MSSA screening into a NICU’s infection control protocol may be an important step to reduce S. aureus infections in this vulnerable neonatal population.

ACKNOWLEDGMENTS

The authors would like to thank Qumars Roshanian of The Johns Hopkins Pathology Data Services for his assistance in extracting microbiology culture data as well as Avinash Gadala of The Johns Hopkins Hospital Department of Hospital Epidemiology and Infection Control for his assistance with data management.

Financial support: This study was partially funded by the Agency for Healthcare Research and Quality (AHRQ grant no. 1R01HS022872).

Potential conflicts of interest: A.M. and J.J. report grant support from Sage Products (Cary, IL). All other authors report no conflicts of interest.

Footnotes

PREVIOUS PRESENTATION. These data were presented in part at IDWeek 2017 on October 7, 2017, in San Diego, California, in the following poster (2170): Voskertchian A, Akinboyo I, Johnson J, Colantuoni E, Sick-Samuels A, Aucott SW, Milstone AM. Association of Active Surveillance and Decolonization Program on Incidence of Clinical Cultures Growing Staphylococcus aureus in the Neonatal Intensive Care Unit.

References

REFERENCES

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Figure 0

FIGURE 1 (A) Quarterly incidence rate of Staphylococcus aureus clinical cultures before (April 1, 2011–March 30, 2013) and after (April 1, 2013–June 30, 2016) implementation of a methicillin-susceptible S. aureus (MSSA) and methicillin-resistant S. aureus (MRSA) active surveillance and decolonization protocol. Dashed horizontal lines show the average incidence rate of S. aureus during the pre- and postintervention periods and the dashed vertical line represents start of intervention (Quarter 9). MRSA and MSSA are depicted in black and gray, respectively. (B) Quarterly incidence rate of S. aureus bloodstream infections (BSIs) before and after implementation of a methicillin-susceptible S. aureus (MSSA) and methicillin-resistant S. aureus (MRSA) active surveillance and decolonization protocol.