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disinfectant-based protocols, many sites initiated WWD repla- cement activities. Although the removal of a single implicated sink was done in 2 studies, ongoing WWD colonization led to a more complex bleach protocol being implemented at 1 site, which was incompletely effective,5 and additional sink system replace- ments at the other site, which was incompletely evaluated.10 Replacement of multiple sinks was planned but not evaluated in 1 report.26 Although all sinks were replaced as an initial interven- tion in the recent report by Gbaguidi-Haore et al,24 colonization of the P-trap systems persisted. As a result, twice weekly bleach treatments of all sinks and P-trap replacement for sinks were associated with patient stays of >7 days. While no new clinical cases were identified during 36 months of follow-up, ObS WWD colonization continued to be documented.24 Unfortunately, none of the 9 sites that initiated multiple sink system replacements described the direct objective evaluation of the impact of the intervention on WWD colonization over time.7,8,10,12,16,21–23 An additional report noted that “no new cases were documented following sink system replacement,” but the duration of follow-up was not described.12 Five reports specifically noted the ineffec- tiveness or incomplete effectiveness of WWD system replacement.5,13,15,19,24 The primary limitation of this analysis of WWD-associated
outbreaks relates to variations in the degree to which the epide- miology and mitigation interventions were evaluated and/or described. Despite this limitation, the similarities between the reports, particularly related to the finding of high frequencies of WWD ObS colonization (mean, 60%), the very low incidence density of cases (<1 per month), the typically long interval between cases with 68% of months having no identified cases, as well as the documentation of multilevel mitigation failures are notable and highly consistent in these reports. The epidemiology, but not the mitigation interventions, was
described in 9 additional reports since 2000.25–32 All of these 9 studies were associated withCROsin ICUs, and66%of the hospitals were located in Europe. Taken together, these 9 reports support the epidemiologic aspects of the 23 studies reviewed overall. An additional limitation of this analysis is the fact that only 26%
of studies utilized cultures to evaluate subsequent interventions on ObS contamination of the implicated WWDs. Despite this lim- itation, the well-documented failure of multiple interventions, including drain systemreplacement, is consistent with our evolving understanding of the epidemiology of the WWD-biofilm–asso- ciated microbiome.34,35 Notably, the wastewater system laboratory work described by Kotay et al35 defined the resilience of horizontal drain system biofilm colonization and its ability to continuously support CRO-infected sink drain systems as a result of rapid regrowth of drain biofilmfollowingmechanical biofilmremoval. In this context, in the 9 reports discussed above, sink replacement failed to successfully mitigate ongoing WWD ObS colonization and/or transmission.5,9,10,12–15,18,19 These reports were also limited by an inability to quantify rates
of actual patient acquisition because none of the study sites uti- lized or reported CRO screening to define a direct relationship between individual WWD cultures and clinical cultures. While it is likely that many of the colonized WWDs did not continually transmit ObS organisms to patients directly, or more likely, indirectly,36 the consistent and substantial maximal interval between ObS clinical cases (mean, 10.2 months) provides strong support for there being an ongoing causal relationship between contaminated WWDs and ongoing patient acquisition of CROs. In addition, the nature of these reports and their potential for
Philip C. Carling
selection bias limits the direct use of these studies to estimate how frequently WWD-associated outbreaks are occurring in acute- care hospitals. While it is possible that publication bias could overestimate the true incidence of outbreaks, Roux et al37 docu- mented widespread endemic CROWWDcolonization in 2013. In the only multisite evaluation of ICU WWD CRO colonization published to date, they confirmed CRO contamination in 89 sinks in the ICUs of 9 hospitals in France despite the fact that all sites were using various liquid-disinfectant protocols to suppress pathogen colonization.37 Despite ongoing mitigation activities, colonization with CROs, primarily K. pneumoniae and Enter- obacter cloacae, was found in 0 to 81% of sink drains tested (mean, 31%).37 While additional studies of this type are needed, the findings of Roux et al support the possibility that WWD CRO-related outbreaks are more frequent than is currently recognized, particularly in high-risk patient settings. An addi- tional factor that may be leading to the underrecognition of WWD CRO transmission is the high level of clonality of carbapenem-resistant K. pneumonia in North America, where 70% have similar antibiograms belonging to sequence type 258.38 Indeed, in the United States, the only recognized outbreak of environmentally transmitted KPC was initially recognized because of the uncommon finding of clostin resistance, which led to the recognition of additional cases over the ensuing weeks on the same hematology oncology unit.6
Drain-associated biofilm and the genetic transfer of resistance
Almost a decade ago, as genomic epidemiology became widely available, clusters of gram-negative healthcare-associated infec- tions were found to have shared resistance plasmids not explained by patient-to-patient transmission,39 which led to further studies of WWD biofilms.40–44 It is now recognized that both vertical sink and shower drains as well as horizontal drain system pipes contain complex biofilm-associated microbiomes often contain CROs as well as a wide range of environmental commensal organisms.40–44 Research has now confirmed the occurrence of plasmid-based intra- and interspecies carbapenamase exchange between WWD biofilm-associated pathogens. In 2008, Tokatli- dou et al26 documented the clonal spread of a novel bla(VIM-12) metallo-β-lactamase gene among K. pneumoniae.26 In 2013, Tofteland et al12 confirmed the interspecies spread of a blaKPC-2 plasmid in WWD-outbreak–associated pathogens. More recently, Wendel et al45 found that biofilm-associated Enterobactericiae and nonfermenters shared metallo-β-lactamase GIM-1 plasmids. Subsequently, Michalikova et al46 quantified transferrable anti- biotic resistance in 39.4% of 137 randomly selected environmental Pseudomonas spp, Enterobacter spp, and Klebsiella ssp, finding that the most frequent plasma-mediated antibiotic resistance was present in E. coli (89%) followed by Pseudomonas spp (41%). In studies by Khariman et al,34 multiple variables were evaluated that impacted the horizontal transfer of carbapenamase plasmids; plasmid content, temperature, substrate as well as strain variables substantially impacted such transmission. Most recently, Stoesser et al47 found that 14 of 15ICU room WWDs (93%) contained multiple CRO species that showed bla KPCs. Although trans- mission of CROs from WWDs represents only 1 of several hos- pital water-system reservoirs from which pathogens are disseminated,40–45 studies over the past 8 years have begun to clarify the bioepidemiology of these critically important compo- nents of patient-care WWD environments.
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