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Effects of environmental disinfection on the isolation of vancomycin-resistant Enterococcus after a hospital-associated outbreak of Middle East respiratory syndrome

Identifieur interne : 000657 ( Pmc/Corpus ); précédent : 000656; suivant : 000658

Effects of environmental disinfection on the isolation of vancomycin-resistant Enterococcus after a hospital-associated outbreak of Middle East respiratory syndrome

Auteurs : Jae-Hoon Ko ; Si-Ho Kim ; Nam Yong Lee ; Yae-Jin Kim ; Sun Young Cho ; Cheol-In Kang ; Doo Ryeon Chung ; Kyong Ran Peck

Source :

RBID : PMC:7115339

Abstract

Highlights

Rooms of patients with Middle East respiratory syndrome (MERS) were disinfected.

Environmental disinfection was performed after the 2015 Korean MERS outbreak.

Sodium hypochlorite and hydrogen peroxide vapor were used.

Vancomycin-resistant Enterococcus significantly decreased for 2 months.

Other multidrug-resistant organisms did not decrease.


Url:
DOI: 10.1016/j.ajic.2019.05.032
PubMed: 31307795
PubMed Central: 7115339

Links to Exploration step

PMC:7115339

Le document en format XML

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<p id="para0005">Environmental disinfection was performed after the 2015 Korean MERS outbreak.</p>
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<p id="para0006">Sodium hypochlorite and hydrogen peroxide vapor were used.</p>
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<p id="para0007">Vancomycin-resistant
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<p id="para0008">Other multidrug-resistant organisms did not decrease.</p>
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<front>
<journal-meta>
<journal-id journal-id-type="nlm-ta">Am J Infect Control</journal-id>
<journal-id journal-id-type="iso-abbrev">Am J Infect Control</journal-id>
<journal-title-group>
<journal-title>American Journal of Infection Control</journal-title>
</journal-title-group>
<issn pub-type="ppub">0196-6553</issn>
<issn pub-type="epub">1527-3296</issn>
<publisher>
<publisher-name>Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc.</publisher-name>
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<article-id pub-id-type="pmid">31307795</article-id>
<article-id pub-id-type="pmc">7115339</article-id>
<article-id pub-id-type="publisher-id">S0196-6553(19)30614-5</article-id>
<article-id pub-id-type="doi">10.1016/j.ajic.2019.05.032</article-id>
<article-categories>
<subj-group subj-group-type="heading">
<subject>Article</subject>
</subj-group>
</article-categories>
<title-group>
<article-title>Effects of environmental disinfection on the isolation of vancomycin-resistant
<italic>Enterococcus</italic>
after a hospital-associated outbreak of Middle East respiratory syndrome</article-title>
</title-group>
<contrib-group>
<contrib contrib-type="author" id="au0001">
<name>
<surname>Ko</surname>
<given-names>Jae-Hoon</given-names>
</name>
<degrees>MD</degrees>
<xref rid="aff0001" ref-type="aff">a</xref>
</contrib>
<contrib contrib-type="author" id="au0002">
<name>
<surname>Kim</surname>
<given-names>Si-Ho</given-names>
</name>
<degrees>MD</degrees>
<xref rid="aff0001" ref-type="aff">a</xref>
</contrib>
<contrib contrib-type="author" id="au0003">
<name>
<surname>Lee</surname>
<given-names>Nam Yong</given-names>
</name>
<degrees>MD</degrees>
<xref rid="aff0002" ref-type="aff">b</xref>
</contrib>
<contrib contrib-type="author" id="au0004">
<name>
<surname>Kim</surname>
<given-names>Yae-jin</given-names>
</name>
<degrees>MD</degrees>
<xref rid="aff0003" ref-type="aff">c</xref>
</contrib>
<contrib contrib-type="author" id="au0005">
<name>
<surname>Cho</surname>
<given-names>Sun Young</given-names>
</name>
<degrees>MD</degrees>
<xref rid="aff0001" ref-type="aff">a</xref>
</contrib>
<contrib contrib-type="author" id="au0006">
<name>
<surname>Kang</surname>
<given-names>Cheol-In</given-names>
</name>
<degrees>MD</degrees>
<xref rid="aff0001" ref-type="aff">a</xref>
</contrib>
<contrib contrib-type="author" id="au0007">
<name>
<surname>Chung</surname>
<given-names>Doo Ryeon</given-names>
</name>
<degrees>MD</degrees>
<xref rid="aff0001" ref-type="aff">a</xref>
</contrib>
<contrib contrib-type="author" id="au0008">
<name>
<surname>Peck</surname>
<given-names>Kyong Ran</given-names>
</name>
<degrees>MD</degrees>
<email>krpeck@skku.edu</email>
<xref rid="aff0001" ref-type="aff">a</xref>
<xref rid="cor0001" ref-type="corresp"></xref>
</contrib>
</contrib-group>
<aff id="aff0001">
<label>a</label>
Division of Infectious Diseases, Department of Medicine, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Republic of Korea</aff>
<aff id="aff0002">
<label>b</label>
Department of Laboratory Medicine and Genetics, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Republic of Korea</aff>
<aff id="aff0003">
<label>c</label>
Division of Infectious Diseases, Department of Pediatrics, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Republic of Korea</aff>
<author-notes>
<corresp id="cor0001">
<label></label>
Address correspondence to Kyong Ran Peck, MD, PhD, Division of Infectious Diseases, Department of Medicine, Samsung Medical Center, Sungkyunkwan University School of Medicine, 81 Irwon-ro, Gangnam-gu, Seoul 06531, Korea.
<email>krpeck@skku.edu</email>
</corresp>
</author-notes>
<pub-date pub-type="pmc-release">
<day>12</day>
<month>7</month>
<year>2019</year>
</pub-date>
<pmc-comment> PMC Release delay is 0 months and 0 days and was based on .</pmc-comment>
<pub-date pub-type="ppub">
<month>12</month>
<year>2019</year>
</pub-date>
<pub-date pub-type="epub">
<day>12</day>
<month>7</month>
<year>2019</year>
</pub-date>
<volume>47</volume>
<issue>12</issue>
<fpage>1516</fpage>
<lpage>1518</lpage>
<permissions>
<copyright-statement>© 2019 Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved.</copyright-statement>
<copyright-year>2019</copyright-year>
<copyright-holder>Association for Professionals in Infection Control and Epidemiology, Inc.</copyright-holder>
<license>
<license-p>Since January 2020 Elsevier has created a COVID-19 resource centre with free information in English and Mandarin on the novel coronavirus COVID-19. The COVID-19 resource centre is hosted on Elsevier Connect, the company's public news and information website. Elsevier hereby grants permission to make all its COVID-19-related research that is available on the COVID-19 resource centre - including this research content - immediately available in PubMed Central and other publicly funded repositories, such as the WHO COVID database with rights for unrestricted research re-use and analyses in any form or by any means with acknowledgement of the original source. These permissions are granted for free by Elsevier for as long as the COVID-19 resource centre remains active.</license-p>
</license>
</permissions>
<abstract abstract-type="author-highlights" id="abs0001">
<title>Highlights</title>
<p>
<list list-type="simple" id="celist0001">
<list-item id="celistitem0001">
<label></label>
<p id="para0004">Rooms of patients with Middle East respiratory syndrome (MERS) were disinfected.</p>
</list-item>
<list-item id="celistitem0002">
<label></label>
<p id="para0005">Environmental disinfection was performed after the 2015 Korean MERS outbreak.</p>
</list-item>
<list-item id="celistitem0003">
<label></label>
<p id="para0006">Sodium hypochlorite and hydrogen peroxide vapor were used.</p>
</list-item>
<list-item id="celistitem0004">
<label></label>
<p id="para0007">Vancomycin-resistant
<italic>Enterococcus</italic>
significantly decreased for 2 months.</p>
</list-item>
<list-item id="celistitem0005">
<label></label>
<p id="para0008">Other multidrug-resistant organisms did not decrease.</p>
</list-item>
</list>
</p>
</abstract>
<abstract id="abs0001a">
<p>Environmental disinfection with sodium hypochlorite and hydrogen peroxide vapor was performed after a hospital-associated outbreak of Middle East respiratory syndrome. Although only 11% of total beds were disinfected, the isolation and vancomycin-resistance rates of
<italic>Enterococcus</italic>
spp significantly decreased for 2 months, whereas other multidrug-resistant organisms did not.</p>
</abstract>
<kwd-group id="keys0001">
<title>Key Words</title>
<kwd>Sodium hypochlorite</kwd>
<kwd>Hydrogen peroxide</kwd>
<kwd>VRE</kwd>
</kwd-group>
</article-meta>
</front>
<body>
<p id="para0009">Environmental disinfection using sodium hypochlorite or hydrogen peroxide vapor has demonstrated its effect on reducing multidrug-resistant organisms (MDROs) in several studies, especially for high-risk wards or outbreak control.
<xref rid="bib0001" ref-type="bibr">1</xref>
,
<xref rid="bib0002" ref-type="bibr">2</xref>
,
<xref rid="bib0003" ref-type="bibr">3</xref>
,
<xref rid="bib0004" ref-type="bibr">4</xref>
However, because such disinfection processes require evacuation of patient rooms, the effects of environmental disinfection not targeted for MDRO-contaminated spaces have not yet been evaluated. After a hospital-associated outbreak of Middle East respiratory syndrome (MERS), we conducted environmental disinfection of patient rooms where confirmed patients with MERS stayed.
<xref rid="bib0005" ref-type="bibr">
<sup>5</sup>
</xref>
Although a small proportion of rooms were cleaned regardless of MDRO risks, we observed a decrease in the number of MDROs detected after the MERS outbreak. For a precise analysis, we evaluated disinfection records and microbiologic data together with inpatient numbers.</p>
<sec id="sec0001">
<title>Methods</title>
<p id="para0010">There was a large hospital-associated MERS outbreak in South Korea from May to July 2015, and environmental disinfection was emphasized after the end of the outbreak.
<xref rid="bib0005" ref-type="bibr">
<sup>5</sup>
</xref>
Patient rooms where confirmed patients with MERS stayed were cleaned with sodium hypochlorite (500 ppm) 6 times after discharge. Low-level disinfectants including sodium hypochlorite, alcohol, and quaternary ammonium compounds are effective for MERS coronavirus.
<xref rid="bib0006" ref-type="bibr">
<sup>6</sup>
</xref>
After the cleaning process, rooms were disinfected by hydrogen peroxide vapor as previously described.
<xref rid="bib0003" ref-type="bibr">3</xref>
,
<xref rid="bib0006" ref-type="bibr">6</xref>
,
<xref rid="bib0007" ref-type="bibr">7</xref>
As 45 patients with MERS changed rooms and used 2- or 6-bed rooms as private,
<xref rid="bib0005" ref-type="bibr">5</xref>
,
<xref rid="bib0008" ref-type="bibr">8</xref>
a total of 86 rooms with 214 beds were disinfected, which represented 11.0% of the total 1,941 beds.</p>
<p id="para0011">We retrospectively collected disinfection records, the number of inpatients in person-days (PD), the use of antibiotics as daily defined dose per 10
<sup>3</sup>
PD,
<xref rid="bib0009" ref-type="bibr">
<sup>9</sup>
</xref>
and microbiologic data from January to December 2015. Considering that the decrease of MDROs was observed for only 2 months after the MERS outbreak, this period (August to September 2015) was defined as the “post-outbreak period.” The MERS outbreak period (June to July 2015) and the post-outbreak period were compared with the non-outbreak period (the rest of 2015). MRDOs included methicillin-resistant
<italic>Staphylococcus aureus</italic>
(MRSA), vancomycin-resistant
<italic>Enterococcus</italic>
(VRE), third-generation cephalosporin-resistant Enterobacteriaceae, carbapenem-resistant Enterobacteriaceae (CRE), carbapenem-resistant
<italic>Pseudomonas</italic>
(CRP), and carbapenem-resistant
<italic>Acinetobacter. Clostridium difficile</italic>
was not included because of limited cases in our center. The Student t test was used for statistical comparison using IBM SPSS Statistics version 20.0 (IBM, Armonk, NY). All
<italic>P</italic>
values were 2-tailed and
<italic>P</italic>
<.05 was considered statistically significant.</p>
</sec>
<sec id="sec0002">
<title>Results</title>
<p id="para0012">The number of inpatients dramatically dropped during the MERS outbreak period and was significantly lower than the non-outbreak period (20,790 vs 51,510 PD per month;
<italic>P</italic>
< .001). The antibiotic use per inpatient increased during the outbreak period. After the outbreak, inpatient numbers recovered rapidly from August 2015, and the number of inpatients and antibiotic prescriptions were not different between the post-outbreak and non-outbreak periods. Overall trends of pathogen isolations and MDRO proportions are presented in
<xref rid="fig0001" ref-type="fig">Figure 1</xref>
, and comparisons between each period are presented in
<xref rid="sec0005">Supplementary Table S1</xref>
.
<fig id="fig0001">
<label>Fig 1</label>
<caption>
<p>Overall trends for MDRO isolations at a tertiary care hospital where a MERS outbreak occurred, presented as isolations per 10
<sup>3</sup>
PD. Among the MDROs, only
<italic>Enterococcus</italic>
spp and VRE decreased significantly during the post-outbreak period (both
<italic>P</italic>
< .05). (A)
<italic>Staphylococcus aureus</italic>
and MRSA. (B)
<italic>Enterococcus</italic>
spp and VRE. (C) Enterobacteriaceae and 3GCRE. (D) Enterobacteriaceae and CRE. (E)
<italic>Pseudomonas</italic>
spp and CRE. (F)
<italic>Acinetobacter</italic>
spp and CRA.
<italic>3GCRE</italic>
, third-generation cephalosporin-resistant Enterobacteriaceae;
<italic>CRA</italic>
, carbapenem-resistant
<italic>Acinetobacter; CRE</italic>
, carbapenem-resistant Enterobacteriaceae;
<italic>CRP</italic>
, carbapenem-resistant
<italic>Pseudomonas; MDRO</italic>
, multidrug-resistant organism;
<italic>MERS</italic>
, Middle East respiratory syndrome;
<italic>MRSA</italic>
, methicillin-resistant
<italic>S aureus; PD</italic>
, person-days;
<italic>VRE</italic>
, vancomycin-resistant
<italic>Enterococcus</italic>
.</p>
</caption>
<alt-text id="alt0001">Fig 1</alt-text>
<graphic xlink:href="gr1_lrg"></graphic>
</fig>
</p>
<p id="para0013">Isolations of
<italic>S aureus</italic>
and MRSA decreased during the post-outbreak period, but it was not statistically significant compared with the non-outbreak period. Isolations of both
<italic>Enterococcus</italic>
spp (179.34 vs 306.26 per 10
<sup>3</sup>
PD;
<italic>P</italic>
 = .045) and VRE (50.09 vs 160.60 per 10
<sup>3</sup>
PD;
<italic>P</italic>
 = .010) significantly decreased during the post-outbreak period. The proportion of VRE among total
<italic>Enterococcus</italic>
spp isolates also significantly decreased (27.52 vs 53.06%;
<italic>P</italic>
 = .028). These significant reductions were associated with disinfected wards/intensive care units (ICUs) (97.80 vs 202.81 per 10
<sup>3</sup>
PD;
<italic>P</italic>
 = .025 for
<italic>Enterococcus</italic>
spp; 30.13 vs 85.24 per 10
<sup>3</sup>
PD;
<italic>P</italic>
 = .047 for VRE). Isolations of Enterobacteriaceae, third-generation cephalosporin-resistant Enterobacteriaceae, and CRE did not decrease during the post-outbreak period. Decreased isolations of
<italic>Pseudomonas</italic>
spp and CRP decreased during the post-outbreak period were observed without statistical significance. Isolations of
<italic>Acinetobacter</italic>
spp and carbapenem-resistant
<italic>Acinetobacter</italic>
did not decrease during the post-outbreak period.</p>
</sec>
<sec id="sec0003">
<title>Discussion</title>
<p id="para0014">After the end of the MERS outbreak, we noticed a numerical reduction in MRSA, VRE, CRE, and CRP. Reduction of these MDROs would be influenced by 2 major factors: a decreased number of inpatients during the outbreak and environmental disinfection at the end of the outbreak. To assess the effects of environmental cleaning, we adjusted MDRO isolations with inpatient numbers and performed subgroup analysis according to the disinfection status. As a result, only
<italic>Enterococcus</italic>
spp and VRE showed statistically significant reductions and associations with environmental disinfection. Handwashing might temporally increase during the MERS outbreak and contribute to the reduction of VRE, but the significant decrease in cleaned wards and ICUs supports the effect of environmental cleaning. Considering that decreases in other MDROs were not associated with disinfected wards and ICUs, they may be more affected by a decreased admission of patients who may harbor MDROs rather than by the environmental cleaning itself. A decreased number of inpatients is likely to be associated with a reduced risk of MDRO isolation, and rapid recovery of MDRO detections within 2 months from the outbreak might reflect inflow from the outside. The overall use of antibiotics, another major factor that may affect MDRO acquisition,
<xref rid="bib0010" ref-type="bibr">
<sup>10</sup>
</xref>
increased during the outbreak period, suggesting it might offset the reduction of MDROs.</p>
<p id="para0015">Of note, disinfection at the end of the MERS outbreak was performed nonselectively for MDROs, and cleaning merely 11% of the hospital resulted in the reduction of overall VRE. Previous studies evaluating environmental disinfection were designed to decontaminate rooms of patients known to be infected or colonized with MDROs.
<xref rid="bib0002" ref-type="bibr">2</xref>
,
<xref rid="bib0003" ref-type="bibr">3</xref>
,
<xref rid="bib0004" ref-type="bibr">4</xref>
By evaluating a post-MERS outbreak environmental disinfection, we suggest that nontargeted, partial environmental disinfection also results in reduction of overall VRE burden. This finding supports implementation of environmental cleaning measures as a routine practice, especially in hematology or transplant wards where VRE would cause clinical infections.</p>
<p id="para0016">As a retrospective analysis, it was difficult to differentiate the effects of sodium hypochlorite cleaning and hydrogen peroxide vapor. Also, because we evaluated microbiologic data without review of medical records, we could not differentiate in-hospital acquisitions specifically. Assuming MDRO carriage rates of admitting patients did not significantly change during the study period, we supposed in-hospital acquisition of VRE decreased during the post-outbreak period.</p>
</sec>
<sec id="sec0004">
<title>Conclusions</title>
<p id="para0017">Although only 11% of total beds were disinfected after a MERS outbreak, the isolation and vancomycin-resistance rates of
<italic>Enterococcus</italic>
spp significantly decreased but the effects persisted briefly for 2 months.</p>
</sec>
</body>
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<sec id="sec0006" sec-type="supplementary-material">
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<title>Supplementary materials</title>
<p id="para0018a">
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<media xlink:href="mmc1.docx">
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<ack id="ack0001">
<title>Acknowledgements</title>
<p>The authors are extremely grateful for the staff members who voluntarily participated in the environmental cleaning. The authors also greatly appreciate the health care personnel and staff members at Samsung Medical Center, and all other hospitals who worked together to overcome the MERS outbreak.</p>
</ack>
<fn-group>
<fn id="d32e360">
<p id="notep0001">Funding/support: This study was supported by the
<funding-source id="gs0001">Samsung</funding-source>
Biomedical Research Institute (SBRI grant no. SMX1161321).</p>
</fn>
<fn id="d32e366">
<p id="notep0002">Conflicts of interest: None to report.</p>
</fn>
<fn id="d32e369">
<p id="notep0003">Jae-Hoon Ko and Si-Ho Kim contributed equally to this work.</p>
</fn>
<fn id="sec0005" fn-type="supplementary-material">
<p id="para0009a">Supplementary material associated with this article can be found in the online version at
<ext-link ext-link-type="uri" xlink:href="https://doi.org/10.1016/j.ajic.2019.05.032" id="interref0001">https://doi.org/10.1016/j.ajic.2019.05.032</ext-link>
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</record>

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