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Wastewater drains: epidemiology and interventions in 23 carbapenem-resistant organism outbreaks

Published online by Cambridge University Press:  28 June 2018

Philip C. Carling
Philip C. Carling*
Affiliation:
Infectious Diseases Section, Steward Carney Hospital, Boston, MassachusettsBoston University School of Medicine, Boston, Massachusetts
*
Author for correspondence: Philip C. Carling, MD, Infectious Diseases Section, Steward Carney Hospital, 2100 Dorchester Avenue, Boston, MA 02124. E-mail: pcarling@comcast.net
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Abstract

For many years, patient-area wastewater drains (ie, sink and shower drains) have been considered a potential source of bacterial pathogens that can be transmitted to patients. Recently, evolving genomic epidemiology tools combined with new insights into the ecology of wastewater drain (WWD) biofilm have provided new perspectives on the clinical relevance and hospital-associated infection (HAI) transmission risks related to these fixtures. To further clarify the clinical relevance of WWD-associated pathogen transmission, reports of outbreaks attributed to WWDs were selected for review that (1) investigated the outbreak epidemiology of WWD-associated transmission of bacterial pathogens, (2) utilized advanced microbiologic methods to establish clonality of outbreak pathogens and/or resistance genes, or (3) described interventions implemented to mitigate transmission of the outbreak pathogens from WWDs. These reports were collated, compared, and analyzed, and the results are presented here.

Information

Type
Review
Information
Infection Control & Hospital Epidemiology , Volume 39 , Issue 8 , August 2018, pp. 972 - 979
Copyright
© 2018 by The Society for Healthcare Epidemiology of America. All rights reserved. 

Background

While the basic elements of healthcare-associated pathogen epidemiology and acquisition are well recognized, new insights into the complexity of transmission events, particularly with respect to carbapenem-resistant organisms (CROs), have begun to evolve dramatically. The first recognition of and validation of transmission clusters of gram-negative pathogens occurred as a result of the recognition of new resistance patterns in Klebsiella pneumoniae and Acinetobacter baumannii. Reference Decker and Palmore 1 Improved species-specific typing technologies and, recently, the rapidly escalating use of sequencing have greatly facilitated what is now recognized as genomic epidemiology. Although water tap and/or aerator Pseudomonas outbreaks were recognized and remediated in the 1990s,Reference Decker and Palmore 1 only when Berrouane et alReference Berrouane, McNutt and Buschelman 2 identified and corrected a whirlpool drain–associated Pseudomonas outbreak in 2000 did wastewater drain (WWD) systems begin to be evaluated as a potential source of environmental CRO transmission to patients. In 2003, Yomoda et alReference Yomoda, Okubo, Takahashi, Murakami and Lyobe 3 described the first reported outbreak associated with the transferrable bla(IMP) carbapenamase genes among Pseudomonas spp cultured from WWDs.Reference Yomoda, Okubo, Takahashi, Murakami and Lyobe 3 Subsequently, 20 additional reports describing both the epidemiology and the mitigation initiatives were published; they serve as the basis for this review. All of these outbreaks were caused by CROs: Pseudomonas spp (n=9), K. pneumoniae (n=3), K. oxytoca (n=3), Escherichia coli (n=3), multiple CROs (n=3), Acinetobacter (n=1), and Serratia (n=1).

Methods

The PubMed database (1990–2018) was searched using multiple text terms: “healthcare drains” and “wastewater drains” as well as “sink drains” and “shower drains” individually and combined with the terms “biofilm” and “outbreaks.” All studies that met the following inclusion criteria were analyzed and compared: (1) investigated the clinical outbreak epidemiology of WWD-associated transmission of CROs, (2) utilized advanced microbiologic methods to establish clonality of outbreak pathogens and/or resistance genes, or (3) described interventions implemented to mitigate transmission of the outbreak pathogens from WWDs.

Results

Demographic features

All 23 WWD-associated outbreaks included in this review occurred in acute-care hospitals and involved CROs. Among them, 16 outbreaks (69%) occurred in Europe, 3 outbreaks (13%) occurred in the United States, 3 outbreaks (13%) occurred in Australia, and 1 (4%) occurred in Canada. Also, 22 outbreaks (95%) were associated with high-risk patient settings. Furthermore, 19 outbreaks (87%) were related to a single CRO: P. aeruginosa (n=9),Reference Yomoda, Okubo, Takahashi, Murakami and Lyobe 3 – Reference La Forgia, Franke, Hacek, Thompson, Robicsek and Peterson 5 , Reference Breathnach, Cubbon, Karunaharan and Pope 11 , Reference Wendel, Kolbe-Busch, Ressina, Schulze-Robbecke and Kindgen-Milles 15 , Reference Davis, Jensen and Van Hal 17 , Reference Stjarne Aspelund, Sjostrom, Liljequist, Morgelin, Melander and Pahlman 19 , Reference Amoureux, Riedweg and Chapuis 21 K. pneumonia (n=3),Reference Snitkin, Zelazny and Thomas 6 , Reference Starlander and Melhus 7 , Reference Tofteland, Naseer, Lislevand, Sundsfjord and Samuelsen 12 E. coli (n=3),Reference Chapuis, Amoureux and Bador 18 , Reference Bousquet, Mee-Marquet and Dubost 20 ,22 K. oxytoca (n=3),Reference Lowe, Willey and O’Shaughnessy 8 , Reference Vergara-Lopez, Dominguez, Conejo, Pascual and Rodriguez-Bano 10 , Reference Leitner, Zarfel and Luxner 16 and a Serratia species (n=1)Reference Kotsanas, Cheong and Korman 13 (Table 1). In addition, 4 outbreaks (17%) involved between 2 and 6 species of CROs that shared the same resistance gene or genes.Reference Leung, Gray, YL Cheong, Haertsch and Gottlieb 9 , Reference Wolf, Bergervoet, Sebens, van den Oever, Savelkoul and van der Zwet 14 , Reference DeGeyter, Blommaert and Verbraeken 23 , Reference Gbaguidi-Haore, Varin, Cholley, Thouverez, Hocquet and Bertrand 24 Of the 17 outbreaks reported since 2013, 6 (35%) were associated with metallo-β-lactamase–producing CROs: 5 occurred in Europe and 1 occurred in Australia.Reference Leung, Gray, YL Cheong, Haertsch and Gottlieb 9 , Reference Vergara-Lopez, Dominguez, Conejo, Pascual and Rodriguez-Bano 10 , Reference Wendel, Kolbe-Busch, Ressina, Schulze-Robbecke and Kindgen-Milles 15 , Reference Chapuis, Amoureux and Bador 18 , Reference Amoureux, Riedweg and Chapuis 21 , Reference Mahida, Clarke, White, Vaughan and Bowell 22 In the past 17 years, 8 reports have described WWD-associated outbreaks without evaluating mitigation intervention.Reference Kac, Podglajen, Vaupre, Colardelle, Buu-Hof and Gutmann 25 – Reference Paopradit, Srinitiwarawong, Ingviya, Singkhamanan and Vuddhakul 32 In these studies, 1 or more CROs were identified as the outbreak strain (ObS). These outbreaks occurred in 8 intensive care units (ICUs) and 1 burn treatment unit and were reported in Europe (n=5), Australia (n=1), Thailand (n=1), and Japan (n=1).

Table 1

Epidemiologic Features of 26 Wastewater Drain–Associated Outbreaks

NOTE. CRE, carbapenem-resistant Enterobacteriaceae; Ec, Escherchia coli; ESBL, extended-spectrum β-lactamase; Ko, Klebsiella oxytoca; Kp, Klebsiella pneumoniae; KPC, Klebsiella pneumoniae carbapenemase; MβL, metallo-β-lactamase; MDR, multidrug resistant; Ab, Acinetobacter; N/A, not available; ObS, outbreak strain; Pa, Pseudomonas aeruginosa; WWD, wastewater drains; BIPI, basic infection prevention interventions; CHG, chlorhexidine gluconate; EIPI, enhanced infection prevention interventions; N/A, not available; ObS, outbreak strain; QAC, quaternary ammonium compound.

Aside from the 5 studies in which only 1 sink drain was cultured, 12 studies reported culturing samples from between 1 and 910 WWDs as part of a preintervention outbreak analysis (Table 1).Reference Yomoda, Okubo, Takahashi, Murakami and Lyobe 3 , Reference La Forgia, Franke, Hacek, Thompson, Robicsek and Peterson 5 , Reference Breathnach, Cubbon, Karunaharan and Pope 11 , Reference Mahida, Clarke, White, Vaughan and Bowell 22 The proportion of positive WWDs ranged between 16% and 100% (mean, 60%). As part of evaluations prior to performing WWD cultures, 15 sites performed several hundred environmental cultures of dry patient-zone surfaces, including sink bowls and sink surrounds. The results of these cultures revealed that these sites were rarely positive for ObS organisms (<1%). In each of the 9 studies identifying Pseudomonas as the outbreak CRO, sink water taps were excluded as a source of the outbreak. Various systems for genotypic testing were employed to define clonality in 13 studies (56%), and in 10 studies, pulse-field gel electrophoresis was used (primarily before 2013).

Epidemiologic features

Of the 23 outbreaks reviewed here, 3 (13%) were relatively short (ie, 1, 4, and 6 months in duration), which precluded the evaluation of their timelines. The study durations of the other 20 outbreaks ranged from 7 to 96 months (mean 37 months), with 14 (70%) lasting 2 or more years. A total of 344 patients (range, 1–84; median, 15 per study) were either colonized or infected with outbreak strains. (Patients identified by screening cultures were not included.) In the studies reviewed, the actual number of clinical cases identified per month was typically quite low (n=1–10; median <1). Indeed, no clinical cases were identified during 578 of the 850 months evaluated (68%). The longest interval between cases ranged from 1 to 40 months (mean, 10.2 months) in the 17 studies from which such information could be obtained (Table 1). The attributable mortality rate reported in 9 studies ranged from 0 to 50% (mean, 33%).

Interventions to mitigate outbreaks

The duration of the outbreaks before implementation of initial mitigation activities directed at WWDs was often substantial in the 21 studies that allowed for such a determination (Table 1). While the interval was only 1 month in 3 studies,Reference Breathnach, Cubbon, Karunaharan and Pope 11 , Reference Bousquet, Mee-Marquet and Dubost 20 , Reference Mahida, Clarke, White, Vaughan and Bowell 22 it was between 6 and 12 months in 7 studiesReference Hota, Hirji and Stockton 4 – Reference Lowe, Willey and O’Shaughnessy 8 , Reference Leitner, Zarfel and Luxner 16 , Reference Davis, Jensen and Van Hal 17 (mean, 8.8 months) and between 24 and 84 months in an additional 7 studies (mean, 53 months).Reference Leung, Gray, YL Cheong, Haertsch and Gottlieb 9 – Reference Breathnach, Cubbon, Karunaharan and Pope 11 , Reference Wendel, Kolbe-Busch, Ressina, Schulze-Robbecke and Kindgen-Milles 15 , Reference Stjarne Aspelund, Sjostrom, Liljequist, Morgelin, Melander and Pahlman 19 , Reference Amoureux, Riedweg and Chapuis 21 , Reference Gbaguidi-Haore, Varin, Cholley, Thouverez, Hocquet and Bertrand 24 Once an outbreak was recognized, 19 sites implemented multiple enhanced infection prevention interventions such as increased hand hygiene education, hand hygiene monitoring, reinforced contact precautions, cohorting infected and colonized patients, cohorting staff caring for such patients, and increased emphasis on daily as well as terminal cleaning practices. Also, 10 sites initiated screening protocols and isolation of asymptomatic ObS gastrointestinal carriers. Although some reports may have included cases identified retrospectively, 2 studies were primarily retrospective, implementing interventions only after an ObS was cultured from 1 or more WWDs.Reference Breathnach, Cubbon, Karunaharan and Pope 11 , Reference Amoureux, Riedweg and Chapuis 21

All sites utilized a wide range of focused WWD mitigation interventions with or without the enhanced infection prevention interventions following recognition of WWD colonization by ObS organisms (Table 1). Such initial interventions included liquid disinfectant–based protocols using bleach,Reference Leung, Gray, YL Cheong, Haertsch and Gottlieb 9 , Reference Kotsanas, Cheong and Korman 13 , Reference Mahida, Clarke, White, Vaughan and Bowell 22 acetic acid protocols,Reference Leung, Gray, YL Cheong, Haertsch and Gottlieb 9 , Reference Stjarne Aspelund, Sjostrom, Liljequist, Morgelin, Melander and Pahlman 19 “double-strength phenolic disinfection,”Reference Leung, Gray, YL Cheong, Haertsch and Gottlieb 9 a glucoprotamin disinfection protocol,Reference DeGeyter, Blommaert and Verbraeken 23 the use of a “steam plunger tool,”Reference Kotsanas, Cheong and Korman 13 and a hydrogen peroxide vapor protocol.Reference DeGeyter, Blommaert and Verbraeken 23 Furthermore, 5 studies described environmental structural interventions as part of the initial outbreak control activities, including single sink replacementReference La Forgia, Franke, Hacek, Thompson, Robicsek and Peterson 5 , Reference Vergara-Lopez, Dominguez, Conejo, Pascual and Rodriguez-Bano 10 , Reference Tofteland, Naseer, Lislevand, Sundsfjord and Samuelsen 12 and multiple sink system replacements.Reference Stjarne Aspelund, Sjostrom, Liljequist, Morgelin, Melander and Pahlman 19 , Reference Gbaguidi-Haore, Varin, Cholley, Thouverez, Hocquet and Bertrand 24

All 21 sites with outbreaks that were studied for >1 month documented ongoing patient infection or colonization with the ObS organism(s) and/or persistent WWD colonization with the ObS pathogen(s) despite initial remediation activities. In 7 sites, the failure of these interventions led to subsequent interventions including a bleach-based WWD system flooding protocol,Reference La Forgia, Franke, Hacek, Thompson, Robicsek and Peterson 5 , Reference Leung, Gray, YL Cheong, Haertsch and Gottlieb 9 , Reference Chapuis, Amoureux and Bador 18 , Reference Gbaguidi-Haore, Varin, Cholley, Thouverez, Hocquet and Bertrand 24 multiple environmental interventions,Reference Snitkin, Zelazny and Thomas 6 a thrice daily bleach treatment protocol,Reference Chapuis, Amoureux and Bador 18 “biofilm removal,” and a daily bleach treatment protocol (Table 1).Reference Stjarne Aspelund, Sjostrom, Liljequist, Morgelin, Melander and Pahlman 19 While not quantified, 7 studies noted that the design of sinks and sink areas might have had a role in outbreak perpetuation.Reference Leung, Gray, YL Cheong, Haertsch and Gottlieb 9 , Reference Breathnach, Cubbon, Karunaharan and Pope 11 , Reference Kotsanas, Cheong and Korman 13 , Reference Wendel, Kolbe-Busch, Ressina, Schulze-Robbecke and Kindgen-Milles 15 , Reference Leitner, Zarfel and Luxner 16 , Reference Gbaguidi-Haore, Varin, Cholley, Thouverez, Hocquet and Bertrand 24 Also, 14 sites described WWD system replacement, usually of multiple sinks,Reference Yomoda, Okubo, Takahashi, Murakami and Lyobe 3 , Reference Hota, Hirji and Stockton 4 , Reference Snitkin, Zelazny and Thomas 6 – Reference Lowe, Willey and O’Shaughnessy 8 , Reference Kotsanas, Cheong and Korman 13 – Reference Leitner, Zarfel and Luxner 16 , Reference Bousquet, Mee-Marquet and Dubost 20 – Reference Gbaguidi-Haore, Varin, Cholley, Thouverez, Hocquet and Bertrand 24 as part of subsequent interventions. Overall, 16 of 21 reports (76%) did not describe culture-based WWD evaluation of the effectiveness of these apparently final interventions.Reference Yomoda, Okubo, Takahashi, Murakami and Lyobe 3 , Reference Hota, Hirji and Stockton 4 , Reference Snitkin, Zelazny and Thomas 6 – Reference Lowe, Willey and O’Shaughnessy 8 , Reference Vergara-Lopez, Dominguez, Conejo, Pascual and Rodriguez-Bano 10 , Reference Breathnach, Cubbon, Karunaharan and Pope 11 , Reference Kotsanas, Cheong and Korman 13 , Reference Wolf, Bergervoet, Sebens, van den Oever, Savelkoul and van der Zwet 14 , Reference Leitner, Zarfel and Luxner 16 , Reference Davis, Jensen and Van Hal 17 , Reference Bousquet, Mee-Marquet and Dubost 20 – Reference DeGeyter, Blommaert and Verbraeken 23 Although 3 reports described a partial response to interventions,Reference Kotsanas, Cheong and Korman 13 , Reference Chapuis, Amoureux and Bador 18 , Reference Gbaguidi-Haore, Varin, Cholley, Thouverez, Hocquet and Bertrand 24 6 studies described objectively confirmed failure of final mitigation activities.Reference La Forgia, Franke, Hacek, Thompson, Robicsek and Peterson 5 , Reference Leung, Gray, YL Cheong, Haertsch and Gottlieb 9 , Reference Breathnach, Cubbon, Karunaharan and Pope 11 , Reference Wendel, Kolbe-Busch, Ressina, Schulze-Robbecke and Kindgen-Milles 15 , Reference Stjarne Aspelund, Sjostrom, Liljequist, Morgelin, Melander and Pahlman 19 , Reference Gbaguidi-Haore, Varin, Cholley, Thouverez, Hocquet and Bertrand 24 Of the studies evaluating a response to mitigation activities, only 4 sites used culture-based assessment of the effectiveness of sink system replacement, and all 4 confirmed ongoing or recurrent WWD colonization with ObS organisms.Reference La Forgia, Franke, Hacek, Thompson, Robicsek and Peterson 5 , Reference Kotsanas, Cheong and Korman 13 , Reference Wendel, Kolbe-Busch, Ressina, Schulze-Robbecke and Kindgen-Milles 15 , Reference Gbaguidi-Haore, Varin, Cholley, Thouverez, Hocquet and Bertrand 24

Discussion

Wastewater drain–associated CRO outbreaks

All 23 WWD-associated outbreaks were attributed to 1 or more CROs and occurred in acute-care hospitals. While a recent study has documented pathogenic yeast sink drain colonization and contamination of surrounding surfaces,Reference Jencson, Cadnum, Piedrahita and Donskey 33 no WWD-associated outbreaks have been attributed to yeasts, fungi, or gram-positive organisms. Essentially, all outbreaks that fit the inclusion criteria for this report occurred in hospital areas where substantial populations of immunologically compromised patients were cared for, and these outbreaks were attributed to many different species of CRO. Only 1 rapidly contained outbreak, related to a single colonized sink, occurred on a general medical ward.Reference Mahida, Clarke, White, Vaughan and Bowell 22 As would be expected from the known global distribution of CROs, outbreaks associated with pathogens exhibiting metallo-β-lactamase genes were reported in Europe (n=6) and Australia (n=1) but not North America. While the level of sink colonization with ObS organisms ranged widely (16%–100%), the majority of implicated WWDs (61%) were ObS positive, and 5 of the sites that cultured >1 sink found all WWDs colonized with ObS pathogens.Reference Kotsanas, Cheong and Korman 13 , Reference Wolf, Bergervoet, Sebens, van den Oever, Savelkoul and van der Zwet 14 , Reference Davis, Jensen and Van Hal 17 , Reference Stjarne Aspelund, Sjostrom, Liljequist, Morgelin, Melander and Pahlman 19 , Reference DeGeyter, Blommaert and Verbraeken 23 The review analysis revealed a very wide range in the duration of outbreaks (1–91 months), with 61% outbreaks lasting 2 or more years. Generally, the shorter outbreaks reflected a combination of rapid recognition of WWD ObS colonization and a limited period of follow-up after implementing initial mitigation interventions. While it is possible that they were incompletely characterized, some of the longer-duration outbreaks appeared to reflect relatively late identification of a WWD source of the outbreakReference Lowe, Willey and O’Shaughnessy 8 and/or partial use of retrospective data collation.Reference Breathnach, Cubbon, Karunaharan and Pope 11 , Reference Amoureux, Riedweg and Chapuis 21 Although not specifically described, it is likely that the very low incidence density of clinical cases, the typically long interval between cases, and the 68% of months without documented ObS infection or colonization both adversely impacted the recognition of an ongoing outbreak and confounded the assessment of possible responses to initial as well as subsequent mitigation interventions. Attributable mortality ranged widely from 0 to 50%, but it clustered near the mean of 33% in 6 of the 9 studies reporting this outcome.

Initial interventions reflected a wide range of traditional infection prevention activities that were specifically enhanced once an outbreak was suspected and prior to identification of WWDs having an ongoing role in the outbreak. Once WWD ObS colonization was identified, all sites implemented a wide range of liquid disinfection protocols while continuing enhanced infection prevention activities. Daily bleach protocols as part of initial mitigation activities were specifically identified as being ineffective in 9 reports.Reference Hota, Hirji and Stockton 4 , Reference La Forgia, Franke, Hacek, Thompson, Robicsek and Peterson 5 , Reference Lowe, Willey and O’Shaughnessy 8 , Reference Leung, Gray, YL Cheong, Haertsch and Gottlieb 9 , Reference Kotsanas, Cheong and Korman 13 , Reference Mahida, Clarke, White, Vaughan and Bowell 22 While Lowe et al noted that increasing a daily bleach protocol to thrice daily decreased ObS-positive drain cultures from 16.4% of sinks to 4.9%, an interruption in protocol compliance resulted in the sink colonization rate returning to 16.4%.Reference Lowe, Willey and O’Shaughnessy 8 Other WWD disinfection protocols found to be ineffective included a “phenolic disinfectant,”Reference Leung, Gray, YL Cheong, Haertsch and Gottlieb 9 an acetic acid protocol,Reference Stjarne Aspelund, Sjostrom, Liljequist, Morgelin, Melander and Pahlman 19 a glucoprotamin protocol,Reference DeGeyter, Blommaert and Verbraeken 23 and the addition of a vaporized hydrogen peroxide system protocol to other interventions.Reference Paopradit, Srinitiwarawong, Ingviya, Singkhamanan and Vuddhakul 32

Concomitantly or more usually in the setting of the limited effectiveness of enhanced infection prevention interventions and disinfectant-based protocols, many sites initiated WWD replacement 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,Reference La Forgia, Franke, Hacek, Thompson, Robicsek and Peterson 5 and additional sink system replacements at the other site, which was incompletely evaluated.Reference Vergara-Lopez, Dominguez, Conejo, Pascual and Rodriguez-Bano 10 Replacement of multiple sinks was planned but not evaluated in 1 report.Reference Tokatlidou, Tsivitanidou, Pournaras and Ikonomidis 26 Although all sinks were replaced as an initial intervention in the recent report by Gbaguidi-Haore et al,Reference Gbaguidi-Haore, Varin, Cholley, Thouverez, Hocquet and Bertrand 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.Reference Gbaguidi-Haore, Varin, Cholley, Thouverez, Hocquet and Bertrand 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.Reference Starlander and Melhus 7 , Reference Lowe, Willey and O’Shaughnessy 8 , Reference Vergara-Lopez, Dominguez, Conejo, Pascual and Rodriguez-Bano 10 , Reference Tofteland, Naseer, Lislevand, Sundsfjord and Samuelsen 12 , Reference Leitner, Zarfel and Luxner 16 , Reference Amoureux, Riedweg and Chapuis 21 – Reference DeGeyter, Blommaert and Verbraeken 23 An additional report noted that “no new cases were documented following sink system replacement,” but the duration of follow-up was not described.Reference Tofteland, Naseer, Lislevand, Sundsfjord and Samuelsen 12 Five reports specifically noted the ineffectiveness or incomplete effectiveness of WWD system replacement.Reference La Forgia, Franke, Hacek, Thompson, Robicsek and Peterson 5 , Reference Kotsanas, Cheong and Korman 13 , Reference Wendel, Kolbe-Busch, Ressina, Schulze-Robbecke and Kindgen-Milles 15 , Reference Stjarne Aspelund, Sjostrom, Liljequist, Morgelin, Melander and Pahlman 19 , Reference Gbaguidi-Haore, Varin, Cholley, Thouverez, Hocquet and Bertrand 24

The primary limitation of this analysis of WWD-associated outbreaks relates to variations in the degree to which the epidemiology 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.Reference Kac, Podglajen, Vaupre, Colardelle, Buu-Hof and Gutmann 25 – Reference Paopradit, Srinitiwarawong, Ingviya, Singkhamanan and Vuddhakul 32 All of these 9 studies were associated with CROs in ICUs, and 66% 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 limitation, the well-documented failure of multiple interventions, including drain system replacement, is consistent with our evolving understanding of the epidemiology of the WWD-biofilm–associated microbiome.Reference Khariman, Weingarten and Conlan 34 , Reference Kotay, Chai, Guilford, Barry and Mathers 35 Notably, the wastewater system laboratory work described by Kotay et alReference Kotay, Chai, Guilford, Barry and Mathers 35 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 biofilm following mechanical biofilm removal. In this context, in the 9 reports discussed above, sink replacement failed to successfully mitigate ongoing WWD ObS colonization and/or transmission.Reference La Forgia, Franke, Hacek, Thompson, Robicsek and Peterson 5 , Reference Leung, Gray, YL Cheong, Haertsch and Gottlieb 9 , Reference Vergara-Lopez, Dominguez, Conejo, Pascual and Rodriguez-Bano 10 , Reference Tofteland, Naseer, Lislevand, Sundsfjord and Samuelsen 12 – Reference Wendel, Kolbe-Busch, Ressina, Schulze-Robbecke and Kindgen-Milles 15 , Reference Chapuis, Amoureux and Bador 18 , Reference Stjarne Aspelund, Sjostrom, Liljequist, Morgelin, Melander and Pahlman 19

These reports were also limited by an inability to quantify rates of actual patient acquisition because none of the study sites utilized 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,Reference Grabowski, Kang, Wells, Sifri, Mathers and Lobo 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 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 alReference Roux, Aubier, Cochard, Quentin and van der Mee-Marquet 37 documented widespread endemic CRO WWD colonization 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.Reference Roux, Aubier, Cochard, Quentin and van der Mee-Marquet 37 Despite ongoing mitigation activities, colonization with CROs, primarily K. pneumoniae and Enterobacter cloacae, was found in 0 to 81% of sink drains tested (mean, 31%).Reference Roux, Aubier, Cochard, Quentin and van der Mee-Marquet 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 additional 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.Reference Chen, Anderson and Paterson 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.Reference Snitkin, Zelazny and Thomas 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 infections were found to have shared resistance plasmids not explained by patient-to-patient transmission,Reference Moquet, Bouchiat and Kinana 39 which led to further studies of WWD biofilms.Reference Khan, Dancer and Humphreys 40 – Reference Kizny Gordon, Mathers, Cheong, Gottlieb, Kotay and Walker 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.Reference Khan, Dancer and Humphreys 40 – Reference Kizny Gordon, Mathers, Cheong, Gottlieb, Kotay and Walker 44 Research has now confirmed the occurrence of plasmid-based intra- and interspecies carbapenamase exchange between WWD biofilm-associated pathogens. In 2008, Tokatlidou et alReference Tokatlidou, Tsivitanidou, Pournaras and Ikonomidis 26 documented the clonal spread of a novel bla(VIM-12) metallo-β-lactamase gene among K. pneumoniae.Reference Tokatlidou, Tsivitanidou, Pournaras and Ikonomidis 26 In 2013, Tofteland et alReference Tofteland, Naseer, Lislevand, Sundsfjord and Samuelsen 12 confirmed the interspecies spread of a bla KPC-2 plasmid in WWD-outbreak–associated pathogens. More recently, Wendel et alReference Wendel, Ressina, Kolbe-Busch, Pfeffer and MacKenzie 45 found that biofilm-associated Enterobactericiae and nonfermenters shared metallo-β-lactamase GIM-1 plasmids. Subsequently, Michalikova et alReference Michalikova, Brnova, Hnilicova, Streharova, Liskova and Krcmery 46 quantified transferrable antibiotic 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,Reference Khariman, Weingarten and Conlan 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 alReference Stoesser, Sheppard, Eyre, Dudley, Sebra and Peto 47 found that 14 of 15 ICU room WWDs (93%) contained multiple CRO species that showed bla KPCs. Although transmission of CROs from WWDs represents only 1 of several hospital water-system reservoirs from which pathogens are disseminated,Reference Khan, Dancer and Humphreys 40 – Reference Wendel, Ressina, Kolbe-Busch, Pfeffer and MacKenzie 45 studies over the past 8 years have begun to clarify the bioepidemiology of these critically important components of patient-care WWD environments.

As summarized in Figure 1, our rapidly evolving understanding of the role of patient-zone WWDs in CRO transmission clarifies the urgent need for further research to qualify and quantify the role of wet biofilm in healthcare environments with respect to both the epidemiology of CROs as well as other Enterobacteriaceae, yeasts, and possibly fungi in a range of healthcare settings. Given the finding that multiple, apparently initially successful, WWD mitigation interventions were later found to be substantially or completely unsuccessful (often after a delay of many months), an assessment of the effectiveness of interventions to mitigate drain biofilm-associated pathogen contamination and transmission might initially be best evaluated by mock-up sink laboratory investigations such as those described by Kotay et al.Reference Kotay, Chai, Guilford, Barry and Mathers 35 Additionally, the likely role of healthcare worker hands in the transmission of WWD CROsReference Grabowski, Kang, Wells, Sifri, Mathers and Lobo 36 and the documentation that bla-KPC–carrying K. pneumonia was cultivable on plastic and steel for up to 5–6 days, and thereafter viable but noncultivable,Reference Strich and Palmore 48 support the need for studies to clarify the role of intermediate fomites in CRO outbreaks. However, the potential role of WWD colonization in CRO outbreaks is not widely recognized. A review published in May 2017 providing detailed recommendations for interventions to optimize recognition and control of CRO stated, “Carbapenem-resistant Enterobactericae have been found infrequently in the environment of infected or colonized patients,”Reference Friedman, Carmeli, Walton and Schwaber 49 (p.586) but these researchers failed to consider the possible role of WWDs in CRO acquisition. Although none of the 6 CRO outbreaks reported in 2017 investigated WWDs as a possible source for ongoing patient acquisition,Reference Munier, Biard, Rousseau, Legrand, Lafaurie and Lomomt 50 – Reference Robustillo-Rodela, Perez-Blanco, Ruiz and Ruiz Carrascoso 56 greater awareness of the potential for WWDs to perpetuate CRO dissemination may lead to the routine evaluation of these sites in all CRO outbreak investigations in the future.

Fig. 1

Summary of wastewater drain carbapenem-resistant organism outbreak characteristics.

Clearly, further studies are needed to clarify and quantify the dynamics of WWD biofilm plasmid exchange because it is now clear that, as Wendel noted, “Drains may serve as a melting pot for horizontal gene transfer, for dissemination into new species, and as a reservoir to propagate future hospital outbreaks.”Reference Wendel, Ressina, Kolbe-Busch, Pfeffer and MacKenzie 45 (p.3605) While developing effective interventions to prevent transmission of WWD pathogens to patients is of immediate importance, it will be equally critical to concomitantly evaluate and mitigate WWD biofilm-colonizing plasmid-mediated antimicrobial resistance.

Financial support

No financial support was sought or received for this study.

Potential conflicts of interest

The author reports no conflicts interest relevant to this report.

Acknowledgments

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Figure 0

Table 1Epidemiologic Features of 26 Wastewater Drain–Associated Outbreaks

Figure 1

Fig. 1Summary of wastewater drain carbapenem-resistant organism outbreak characteristics.