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Environmental approaches to controlling Clostridioides difficile infection in healthcare settings

Environmental approaches to controlling Clostridioides difficile infection in healthcare settings As today’s most prevalent and costly healthcare-associated infection, hospital-onset Clostridioides difficile infec- tion (HO-CDI) represents a major threat to patient safety world-wide. This review will discuss how new insights into the epidemiology of CDI have quantified the prevalence of C. difficile (CD) spore contamination of the patient- zone as well as the role of asymptomatically colonized patients who unavoidable contaminate their near and dis- tant environments with resilient spores. Clarification of the epidemiology of CD in parallel with the development of a new generation of sporicidal agents which can be used on a daily basis without damaging surfaces, equipment, or the environment, led to the research discussed in this review. These advances underscore the potential for sig- nificantly mitigating HO-CDI when combined with ongoing programs for optimizing the thoroughness of clean- ing as well as disinfection. The consequence of this paradigm-shift in environmental hygiene practice, particularly when combined with advances in hand hygiene practice, has the potential for significantly improving patient safety in hospitals globally by mitigating the acquisition of CD spores and, quite plausibly, other environmentally transmitted healthcare-associated pathogens. Keywords Clostridioides difficile, Hospital onset Clostridioides difficile infection prevention, Disinfection cleaning, Optimized cleaning performance, Sporicidal disinfectant, Healthcare-associated infections Introduction surface cleaning interventions and concomitant hand As noted by Peters in 2022, healthcare-associated infec- hygiene practice can be quantified to develop clinically tions (HAI) are one of the greatest threats to patient sound implementation science has yet to achieved [2, 3]. safety worldwide [1]. As a result of epidemiologic and Despite such ongoing challenges it is important to rec- microbiologic studies over the past decade, it has become ognize that environmental hygiene represents a critical increasingly evident that interventions to mitigate envi- element of what Wenzel and Edmonds defined as “hori - ronmental surface pathogen contamination constitute zontal interventions” that are central to mitigating a wide an important component of (HAI) prevention. Unfor- range of HAIs (Fig.  1) [4, 5]. These approaches aim to tunately, precisely defining how the impact of various reduce the risk of infections caused by a broad range of pathogens by the implementation of standard practices that are effective regardless of patient specific conditions *Correspondence: [6]. In contrast to the horizontal interventions, “vertical Philip C. Carling interventions” are pathogen and/or condition specific. Pcarling@comcast.net While vertical and horizontal approaches are often com- Carney Hospital, Boston, MA, USA Stamford Medical Center, Stamford, CT, USA plementary, there is evolving evidence that horizontal Trinity Health, Lavonia, MI, USA interventions in endemic situations may represent a best © The Author(s) 2023. 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The Creative Commons Public Domain Dedication waiver (http://creativecom- mons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Carling et al. Antimicrobial Resistance & Infection Control (2023) 12:94 Page 2 of 14 ribotype 027 fell by half between 2007 and 2010, likely due to a concurrent reduction in fluroquinolone use [2]. While the overall trend toward decreasing CDI in Europe is of note, between 23 and 66% of cases in a range of European countries [2] and 50–60% of cases in Australia were found to be under diagnosed due to a lack of clinical suspicion and suboptimal laboratory methods [16]. In the United States, CDI rates had been showing a gradual decrease during the decade prior to the COVID pandemic, primarily due to decreases in HO-CDI [17]. Several factors would appear to have contributed to the Fig. 1 The elements of Horizontal Healthcare Hygienic Practices. The declining incidence including antimicrobial stewardship blue arrows represent the interdependence between the elements [18], better diagnostic stewardship [19] and reimburse- ment negative incentive programs [20]. While some facilities experienced increases in HO-CDI early in the use of HAI prevention resources [6, 7]. As noted in Fig. 1, COVID pandemic, recent more extensive studies have Healthcare Hygienic Practice consists of interventions failed to document a significant trend in CDI rates [21, which have traditionally been addressed separately, but 22]. as will be discussed below, their effectiveness in clinical settings is highly interrelated and interdependent. Evolving insights into healthcare environmental The burden of healthcare associated Clostridiodes dif - Clostridioides difficile epidemiology ficile Infection (CDI), coupled with the expectation that Given the extremely low inoculum necessary to cause improved environmental cleaning could prevent these infection [23] and the fact that CD spores on environ- infections, has led to extensive efforts to mitigate trans - mental surfaces have a basically indefinite ability to mission risk within healthcare settings since 1981 when remain viable decreasing only 0.5 log in 14  months [24] Fekety et al. [8] documented widespread healthcare envi- it is not surprising that surfaces contaminated with CD ronmental contamination of surfaces, both near and spores have a role in CD transmission. Recent studies more distant from patients with CDI. Although numer- have clarified and quantified many aspects of the envi - ous quasi-experimental studies substituting dilute bleach ronmental epidemiology of CD in hospitals (Table 1). for non-sporicidal disinfectants have reported a reduc- As noted in Elements 1 and 2, recent studies have tion in healthcare-associated CDI (HO-CDI) during shown that a substantial proportion of all acute care outbreaks, efforts to effectively mitigate environmen - patients are colonized with CD either at the time of tal transmission of Clostridiodes difficile (CD) spores admission (average incidence density 10.6%, range in endemic settings has been ineffective [9–12]. New 2.8–21% [25–35] or during their hospitalization (aver- insights into the healthcare epidemiology of HO-CDI age prevalence density 12.5%, range 2.9–21%) [25, and new approaches to mitigating environmental trans- 36–41]. As a result, approximately 11% of hospital- mission will be discussed in detail in this review. ized acute care patients present an ongoing risk of CD transmission to the environment and susceptible Global and healthcare epidemiology patients. Genomic epidemiology has now confirmed of Clostridioides difficile infections the environmental transmission of spores from these Global epidemiology patients to other patients [37, 42–45]. As noted in Ele- Although accurate assessments of global trends in CDI ment 3, patients recovering from acute CD infection prevalence are challenged by variations in diagnostic are associated with significant transmission of spores methods as well as resource limitations impeding sur- to their environment [46–48]. This issue was care- veillance activities [2, 13], the world wide epidemiol- fully analyzed in a multi-site study by Davies et  al. in ogy of CDI has been characterized by rapidly evolving 2020 which evaluated the impact of treatment for CD shifts in prevalence of disease [14]. A recent review of infection on patient-zone environmental contamina- regional differences in (CDI) noted that global infections tion [49]. Treatment of CD infection with metronida- have been slowly decreasing between 2 and 4% per year zole, vancomycin or fidaxomicin similarly decreased through 2015 in most European countries while Asia has the proportion of patients with positive stool cultures shown increasing trends through 2014 primarily due to from 100 to 35% immediately after treatment. Fol- increases in western Asia countries including Turkey and lowing treatment, the rate rebounded to 80–90% by Israel [15]. In England declining rates of infection with 2–4 weeks later. And although there was a decrease in C arling et al. Antimicrobial Resistance & Infection Control (2023) 12:94 Page 3 of 14 Table 1 The elements of Clostridioides difficile healthcare epidemiology Elements of Clostridioides difficile Environmental Epidemiology 1. At the time of hospitalization 10.6% of patients (range 2.8–21%) are CD carriers Ref: [25–35] 2. During hospitalization 12.5% of patients (range 2.9–21%) are CD carriers Ref: [25, 36–41] 3. Transmission of CD spores to environmental surfaces is associated with: Ref: [46–48] Patients with acute infection Patients recovering from acute infection Asymptomatic CD colonized patients 4. Treatment does not decrease ongoing environmental spore contamination for more than a month Ref: [49] 5. Wide spread surface contamination far from known CD infected patients Ref: [35, 36] 6. Increased Cleaning and disinfection result in: Ref: [99] Decreased surface and hand contamination Decreased CD acquisition 7. Genomic confirmation of the role of asymptomatic CD carriers in transmission Ref: [37, 42–45] 8. Acquisition of CD from a prior room occupant is significantly dependent on the prior room occupant receiving antibiotics Ref: [52, 53] the proportion of environmental sites contaminated Mitigating Clostridiodes difficile spore transfer with CD spores from 36% before treatment to 20% from environmental surfaces immediately following treatment, environmental con- Chemical disinfection tamination by these patients was still at 27% four weeks Chlorine-based disinfectants, particularly diluted com- after completing treatment, confirming the significant mercial grade bleach has been used extensively for ongoing risk of transmission of CD to other patients terminal cleaning of CDI patient rooms [54]. Unfortu- and healthcare workers by patients who had completed nately, physical damage associated with the use of these treatment for CDI. These studies confirm substantial disinfectants precludes their daily use for all high-touch levels of environmental contamination, but they may patient-zone surfaces. Fortunately, we now have broad- actually under-estimate the problem. A recent study spectrum sporicidal agents that are at least as effective as using PCR technology confirmed a tenfold increase in bleach, are not associated with significant damage to sur - the frequency of surface contamination in comparison faces, and are not associated with potentially toxic resid- to direct culture [50]. In 2015 Kundrapu, documented uals during either their use or disposal [55, 56]. These that spore shedding and near patient environmen- hydrogen peroxide/peroxyacetic acid formulation chem- tal contamination with CD spores was substantially istries are rapidly sporicidal and are also effective against increased when asymptomatic patients colonized with Candida auris, healthcare-associated pathogens (HAPs), CD were administered antibiotics [51]. The clinical norovirus and other viral pathogens, including corona relevance of this phenomenon was subsequently clari- viruses [57]. While these chemistries have been widely fied by Freedburg et al. [52].They analyzed a cohort of used and their effectiveness well validated, other non- more than 100,000 patients who sequentially occupied chlorine based sporicidal agents are becoming available. a given hospital bed and found that independent of the prior room occupant’s CDI status, administration Surface disinfection technologies of antibiotics to the prior bed occupant was the most Despite in  vitro studies confirming the resistance of CD significant factor associated with an increased risk of spores to UV light, programs incorporating UV technol- the next bed occupant developing CDI. The same phe- ogy have been reported to have impacted HO-CDI rates nomenon was also identified by Dowling Root in 2021 in hyper-endemic settings [58]. In contrast, several more [53]. In this study of 17,285 patient room occupancies recent reports of such programs failed to show an impact the risk of HO-CDI was significantly associated with on endemic HO-CDI rates [12, 59–62] and a multi-year prior room occupant antibiotic usage (Odds Ratio cluster randomized crossover control trial found that 2.37, p < .001). The results of these two large studies, the daily UV supplemented intervention did not reduce can only be explained by recipient acquisition of resid- either HO-CDI rates or VRE transmission [63]. These ual CD spores asymptomatically shed onto patient- results have now been further supported by a cluster-ran- zone surfaces by the preceding room occupant. domized sham-controlled double blinded crossover trial Carling et al. Antimicrobial Resistance & Infection Control (2023) 12:94 Page 4 of 14 of a UV program, by Kaye et al. involving 25,732 patient performance feedback to EVS staff were shown to be room cleanings. It failed to show an impact on HO-CDI highly effective in improving cleaning outcomes [78, rates, which were actually higher in the sham UV treat- 79]. Despite the challenges the EVS staff contend with ment arm (p 0.53) [64]. Furthermore, the prevalence of [80], published reports of these programs have now E. coli and Staph. aureus contamination of high-touch confirmed the effectiveness of such programs with the patient-zone surfaces was unchanged [65, 66]. Uncon- TDC improving from 40–60% to 80–90% or higher trolled studies utilizing hydrogen peroxide vapor tech- for at least 3 years [79, 81]. Most recently Parry (2022) nology as part of terminal cleaning of CDI patient rooms evaluated the sustained impact of a structured ongoing have appeared to be associated with a decrease in HO- monitoring and feedback program to optimize patient- CDI [67–69] but they were lacking confounder assess- zone disinfection cleaning in a 305 bed acute care hos- ment. In addition, logistical challenges in delivering the pital over 10 years [82]. treatment may hinder the use of this technology beyond The cleaning/disinfection performance of the EVS staff CDI isolation room terminal cleaning [58]. was covertly measured by specially-trained infection pre- vention nurse liaisons to minimize bias and telegraphing surface marking sites. As noted in Fig. 2, cleaning perfor- A programmatic approach to optimizing mance improved from a baseline TDC of 60% to greater environmental hygiene to mitigate HO‑CDI than 80% over the first year of the program. Subsequently Evaluating disinfection cleaning most quarterly rates were at or above the 90% minimum The importance of physically removing visible dirt and target during the final six years reported. The process soil from surfaces in hospitals has been recognized for improvement success of programs related to patient zone more than 150  years [70]. Consequently, all acute care disinfection cleaning had also been realized with respect hospitals have policies and procedures to define the to the operating theatre setting [82, 83]. role of environmental services personnel for cleaning “Tools For Evaluating Environmental Cleaning: The patient-zone surfaces. Environmental services (EVS) Guidance Environmental Cleaning Procedures” As a managers and infection preventionists had imple- result of published evidence supporting objective moni- mented joint visual inspection of surfaces in patient toring to evaluate surface cleaning processes, the CDC care areas well before the CDC recommended that developed the guidance “Options for Evaluating Environ- hospitals clean and disinfect “high-touch surfaces” in mental Cleaning” in 2010 and updated it in the Guidance 2003 [71]. The CDC further recommended that hos - “Best Practices for Environmental Cleaning Procedures” pitals “monitor, (i.e., supervise and inspect cleaning in 2020 [77, 84]. which recommends the use of a fluo - performance) to assure consistent cleaning and dis- rescent marker-based performance monitoring program infection of surfaces in close proximity to the patient along with direct observation of cleaning practice. and likely to be touched by the patient and healthcare Studies in the United States and abroad during the past professionals” in 2006 [72]. Unfortunately, the intrinsi- 20  years have used a specially developed fluorescent gel cally subjective nature of such monitoring along with or “test soil” to covertly evaluate environmental clean- its episodic and deficiency-oriented features limit its ing in a wide range of healthcare settings [75, 76, 85– ability to accurately assess the thoroughness of day-to- 89]. These studies have utilized a standardized metered day cleaning activity. Preliminary studies documenting transparent gel specifically formulated for the covert patient zone surface contamination with HAPs raised evaluation of healthcare surface cleaning. While non- concerns that cleaning practice should be improved standardized fluorescent powders and lotions have been [73]. It was not until actual cleaning practice was objec- used in a non-covert manner for education [90], other tively monitored, initially using a covert visual moni- studies [89, 91] demonstrated that these substances vis- toring program [74] and later with covertly applied ibility in ambient light limited their effective use in pro - fluorescent markers, that actual cleaning practice was grams to objectively monitor cleaning practice as a result objectively evaluated [75, 76]. Evaluations were done of their ability to induce a Hawthorne effect. In 2019 a in a standardized manner with a metered fluorescent ™ study from Johns Hopkins compared the clinical use of marking system (DAZO Ecolab, Inc., St. Paul, MN). the metered applicator with a standardized fluorescent The outcome measured was the actual thoroughness gel to a cotton swab applicator with a non-standardized of cleaning expressed as the “thoroughness of disin- fluorescent gel and found that the metered applicator fection cleaning” or”TDC” [77]. Given the accuracy provided a more accurate assessment of cleaning prac- of the metered fluorescent markers to objectively and tice. The authors concluded that, “Infection control reproducibly identify opportunities to improve clean- programs implementing evaluation of environmental ing thoroughness, process improvement interventions cleaning programs should carefully consider the type based on structured educational activities and direct C arling et al. Antimicrobial Resistance & Infection Control (2023) 12:94 Page 5 of 14 Fig. 2 The thoroughness of disinfection cleaning as objectively documented by the standardized florescent marker monitoring program and method of applying fluorescent gel marks to stand - of the actual EVS cleaning programs. Such an approach, ardize and optimize the measurement of fluorescent gel as discussed previously, assures the validity of the infor- removal” [92, p.796]. mation collected” [77 (Appendix B, p.1, 82]. The impor - ATP bioluminescence technology detects the pres- tance of this issue was confirmed in a study which found ence of organic material, including viable and non- that when EVS managers monitored the discharge room viable bioburden, on surfaces. Although their ease of cleaning, they documented an average TDC score of use led to their use to attempt to quantify healthcare 82.5% while a research team covertly evaluating the same surface bioburden, the high sensitivity of the system to two hospitals documented an average score of 52.4% [96]. non-microbiologic and non-viable organic matter and Given the fact that neither the Joint Commission or the its relative insensitivity to some healthcare-associated World Health Organization consider self-monitoring of pathogens has now been clarified [93, 94]. As noted by hand hygiene practice to be acceptable, it seems reason- Mulvey, et  al. in a detailed evaluation of the ATP tech- able that a similar expectation should be applied to moni- nology, “Sensitivity and specificity of 57% (with the ATP toring disinfection cleaning activities. tool) means that the margin for error is too high to justify stringent monitoring of the hospital environment (with Implementing the 2020 CDC guidance: core ATP technology) at present” [95, p.29]. As noted in the components of environmental cleaning CDCs Guidance Best Practices for Environmental Clean- and disinfection in hospitals ing in Healthcare facilities (2020): (Section  4. Tables  29 In October 2020 the CDC published a guidance docu- and 30) ATP technology is not recommended for evaluat- ment to provide hospitals with a detailed roadmap for ing cleaning performance [84]. the development of programs to optimize all aspects of An important requirement for monitoring and pro- patient-zone environmental hygiene because “maintain- cess improvement programs relates to the need for them ing a clean hospital environment and minimizing the to have a successful validation component. As noted in presence of hospital pathogens is critical for keeping the 2010 CDC guidance, “It is important that the moni- patients safe” [97, p.e1]. toring be performed by hospital epidemiologists, infec- The six individual “core components” (Fig.  3) and the tion preventionists or their designees who are not part specific recommendations within each of the strategies Carling et al. Antimicrobial Resistance & Infection Control (2023) 12:94 Page 6 of 14 CDC Core Components of Environmental Cleaning and Disinfec on in Hospitals 1. Integrate Environmental Services into the Hospital’s Safety Culture 2. Educate and Train all Healthcare Providers Responsible for Cleaning and Disinfec ng Pa ent Care Areas 3. Select Appropriate Cleaning and Disinfec on Technologies and Products 4. Standardize Se€ng-specific Cleaning and Disinfec on Protocols 5. Monitor Effec veness and Adherence to Cleaning and Disinfec on Protocols 6. Provide Feedback on Adequacy and Effec veness of Cleaning and Disinfec on to All Responsible HCP as well as Relevant Stakeholders (e.g., Infec on Control, Hospital Leadership) Fig. 3 The CDC core elements of environmental cleaning and disinfection in hospitals Fig. 4 The impact of optimizing environmental hygiene to decrease Clostridioides difficile transmission in a single hospital over two and one half years detailed in the document specify what “every healthcare facility should consider to ensure appropriate environ- mental cleaning and disinfection” [98, p.e1]. While not specifically discussed in the document, describing the analysis employing a group of eight acute care hospitals (EVS) staff involved in patient-zone cleaning and disin - [99]. These hospitals had stable endemic Standardized fection as “healthcare personnel” represents an acknowl- Infection Rates (SIRs) (Mean 1.03 for the group) during edgment of the relevance these activities have to safe an 18-month pre-intervention period. The intervention patient care. Taken together, these Core Components hospitals within the healthcare system studied ranged provide a detailed, clearly structured, comprehensive in size from a 532-bed tertiary care hospital to a 44-bed template, based on implementation science studies over regional critical access hospital (mean 257 beds). Nine the past 20 years, to optimize all aspects of environmen- randomly selected hospitals from the same system tal hygiene practice for acute care hospitals which can that had not enrolled in a standardized (EVS) process also be adapted to a wide range of patient care settings improvement program served as controls. (mean 266 [81]. beds). Thoroughness of cleaning was programmatically monitored in accordance with the 2010 CDC guid- ance[77] using a standardized metered fluorescent Assessment of the potential impact of thorough marking system (DAZO Ecolab, Inc., St Paul, MN). daily sporicidal disinfection cleaning in mitigating HO‑CDI Given the fact that general use of sporicidal disinfectants on patient-zone surfaces is now feasible, it is possible to quantitively assess the impact of daily sporicidal disinfec- tion cleaning of all high-touch patient-zone surfaces in mitigating CD transmission. This approach was initially evaluated in a single-site, quasi-experimental study in 2016 [98]. As noted in Fig.  4, during the 33-month intervention period, thoroughness of disinfection cleaning (TDC) rapidly improved from 81 to 92% and remained greater than 88% during the remainder of the study (P = .01). HO-CDI rates fell significantly during the intervention period from an average of 8.9–3.2/10,000 patient-days (p = 0.0001, 95% CI 3.48–7.81). The clinical impact of implementing daily, hospital- wide sporicidal disinfectant cleaning of all patient-zone surfaces was further evaluated using a control group Fig. 5 Toroughness of Cleaning in 8 Intervention Hospitals validated, quasi-experimental, interrupted-time series C arling et al. Antimicrobial Resistance & Infection Control (2023) 12:94 Page 7 of 14 As noted in Fig.  5, TDC following educational activi- ties during the 3-month wash-in period improved rapidly from 59 to 88%. With the use of ongoing quarterly per- formance feedback, cleaning thoroughness continued to improve over the next 5 quarters and at 18  months the TDC was 93.6% for the group (Range 91–96%, 95% CI 45–24%, p < 0.0001). As noted in Fig.  6, mean group HO-CDI SIRs ranged from 0.49 below to 1.42 above a mean of 1.03 during the 18  months prior to project implementation. In quar- ter-1 following wash-in, all sites documented a decrease in HO-CDI to a mean SIR of 0.6 (95% CI 0.13–0.75, p = 0.009). Over the next 5 quarters, the HO-CDI SIR Fig. 7 Evaluation of potential confounding influences. 1. Q3 continued to decrease stabilizing during the last three pre-intervention year “Enhanced contact precautions for CD quarters evaluated to a mean SIR of 0.4 (95% CI 0.13– positive patients was implemented”. During the first 6 to 9 months 0.75, p = 0.009). of the pre-intervention period these sites implemented nursing As outlined in Fig. 7 seven potentially significant con - education to clarify the importance of early stool specimen collection founders were evaluated pre-and post-intervention and in patients with diarrhea were found not to have had an impact on the results. Using the control hospitals in an adjusted difference- in-differences analysis, the intervention was associ - HO-CDI. While a randomized controlled trial could ated with a 0.55 reduction (95% CI − 0.77 to − 0.32) further clarify and quantify the results of this interven- in HO-CDI (p < 0.001; or a 50% relative decrease from tion, such an undertaking would require considerable a baseline SIR of 1.03). The study represents the first resources as well as the need for sites to defer imple- multi-site, quasi-experimental study with control menting potentially effective design elements of the hospitals to evaluate a daily, hospital wide, perfor- intervention. mance optimized, sporicidal, disinfection cleaning on Fig. 6 The trend in HO-CDI SIR pre and post-intervention Carling et al. Antimicrobial Resistance & Infection Control (2023) 12:94 Page 8 of 14 Given the challenges of a randomized trial, it should CD transmission when TDC is lower than those achieved be noted that the open-access published, agent-based by the intervention group of hospitals discussed above modeling study by Barker, et al. evaluating the impact of [7]. Most recently, this agent-based simulation model multiple single and bundled interventions on HO-CDI was used by Scaria, to compare it with primary observed prevention found that the single most clinically effective data from a 426 mid-western, US hospital over 6  years and cost-effective intervention was daily sporicidal clean - in order to compare the predicted HO-CDI rate to the ing of all patient zone surfaces as depicted in Fig. 8 [7] observed rate between 2013 and 2018. Furthermore, quantitative input analysis of the model As noted in Fig.  9.,the trends in both the modeled found only a limited additional incremental benefit from and actual rates were nearly identical following imple- increasing modeling parameters of thoroughness of menting “increased infection control measures” namely, cleaning from an “enhanced level” (80% TDC) to an “ideal daily patient-zone sporicidal disinfection cleaning and level” (94% TDC), suggesting that daily patient zone improvement in the TDC from 56% in 2013 to 79% in sporicidal cleaning could have a substantial impact on 2017 and 2018 [100]. Of note, the decrease of 46% in HO- CDI, both predicted and observed, was similar to the decrease of 50% documented in the eight hospital study previously discussed. Additional benefits of mitigating CD environmental transmission Collateral microbiological benefits Over the past several years there has been increasing documentation of the potential and actual role of sur- faces in the near patient environment being relevant in HAI epidemiology. As noted in Fig.  10, [101–116] patient-zone environ- mental surfaces are frequently contaminated with a wide range of HAPs. While the frequency of contamination is greatest close to patients, genomic epidemiology has confirmed more distance spread [11, 116]. While docu- menting high level CRE contamination (88% of surfaces) Fig. 8 Evaluation of the modeled cost (cost-avoidance) associated with interventions to mitigate HO-CDI associated with colonized patients, the study by Shams Fig. 9 Comparison of the modeled and observed HO-CDI over 6 years C arling et al. Antimicrobial Resistance & Infection Control (2023) 12:94 Page 9 of 14 Environmental Transmission of HAPs Other Than CD A. Environmental Contaminaon of rounely Cleaned Paent-Zone Surfaces Reference MRSA, VRE, Ab, Kp 34% of random surfaces MRSA,VRE 55%of random surfaces MRSA, VRE, Ab, Ps 40% C. auris 70% KPC-producing CRE 88% of colonized paent surfaces MRSA, VRE 82% of CP room surfaces 12% of non-CP room surfaces MDROs 65% B. Genomic Epidemiologic Evidence of Environmental Transmission MRSA, VRE Transmission between paents and surface environment 109,110 MRSA and MSSA VRE, MDROs C. Decreased Environmental Contaminaon With Improved Disinfecon Cleaning MRSA 113-115 VRE GNB 104,108 MDROs and Ab D. Decreased Acquision of HAPs With Improved Disinfecon Cleaning 104,116 Ab,MRSA, VRE, Fig. 10 Studies which have clarified the potential for optimized patient-zone disinfection cleaning to mitigate the transmission of healthcare -associated organisms from environmental surfaces also found that 80% of all contamination was associated quantified. As part of the agent-based modeling study with 20% of colonized patients which they character- previously described, Barker used a standardized quality- ized as “super shedders” [101, 117] Although many of the of-life years (QALYs) analysis and found that the impact HAI-associated pathogens in Fig. 10 are effectively killed of the daily, performance optimized (80% TDC) spori- by quaternary-ammonium compounds, or accelerated cidal disinfection patient-zone cleaning intervention in hydrogen peroxide the use of hydrogen peroxide-peroxy- the modeled 200 bed hospital with a 1.0 SIR was associ- acetic acid chemistries for CD mitigation would allow for ated with a savings of 36.8 QALY s annually for such a highly effective disinfection of surfaces harboring Can - program [7]. dida auris, norovirus and quaternary-ammonium resist- In addition to QALYs lost as a result of CDI, the ill- ant A. baumannii [118]. ness has a substantial adverse impact on patient reported Finally, it should be noted that recent reports docu- quality of life. This phenomenon was recently quanti - menting widespread intra-system and inter-system trans- fied in a controlled study by Han (2022) using a health- mission of carbapenem-resistant Klebsiella pneumoniae related quality of life 32 element questionnaire [121]. The and the possibility that terminal patient room clean- study found that patients hospitalized with CDI devel- ing enhanced by a UV treatment protocol can impact oped a quantifiable negative impact on multiple physical the occurrence of hospital-onset bacteremia with some and mental health measures. Of note was a particularly strains of gram negative rods suggest that there is yet adverse impact of recurrent CDI (10% of patients) on the much to be clarified regarding the role of patient zone quality-of-life parameters measured. surfaces in the epidemiology of many HAPs [119, 120] Economic benefits Quality of life benefits While the direct impact of CDI in terms of morbid- While the acute morbidity and mortality (approximately ity and mortality has been well documented, several 5%) of CDI have represented significant issues for years, in-depth population based studies published between analysis of more complex effects of CDI are now being 2011 and 2022 have analyzed the economic costs of CDI Carling et al. Antimicrobial Resistance & Infection Control (2023) 12:94 Page 10 of 14 [122–125]. In considering the impact of these costs, it health care costs and health care utilization associated is critically important to note that a substantial propor- with CDI are likely to increase” [125, p.1]. tion of the total costs per case are not reimbursed by commercial insurance, Medicare or Medicaid in U.S. Environmental hygiene and hand hygiene: hospitals. As summarized in Fig.  10, four studies have an integrated approach specifically evaluated the cost of HO-CDI (Table 2 ). Over the past several years it has become increasingly These matched controlled studies evaluated between evident that infection prevention initiatives focused on 6000 and 60,000 HO-CDI cases over 2–7  years. The optimizing hand hygiene have not realized their hoped- three studies which evaluated total cost found almost for impact on healthcare-associated pathogen (HAP) identical results while the two studies which evaluated transmission in well-resourced healthcare settings non-reimbursed costs also found highly similar costs of [129–133]. Accepting our inability to quantify the abso- $14,257 and $13,476 or approximately 50% of the total lute risk of pathogen acquisition directly from healthcare cost. This proportion of non-reimbursed costs is also workers’ hands, there is good circumstantial evidence consistent with an earlier study of 272, 143 hospitaliza- that such transmission accounts for a substantial propor- tions which found that 65% of the cost of HO-CDI was tion of HAP transmission. Indeed, it has become widely not reimbursed by Medicare payments [126]. Although accepted that hand hygiene, as noted by Palamore, is not stratified to identify costs for HO-CDI, Magee in “critically important for the prevention of HAIs” [134] 2015 determined the excess cost for hospitalized CDI (p.8). patients to be $24,408 based on data from 2009 to 2011 Given the fact that patient zone surfaces not con- [127]. In a similar study Zhang in 2019 found excess taminated by HAPs cannot be a source of pathogen total cost per case of $24,205 [128]. transmission even in the absence of hand hygiene, As modeled by Barker [7] using data from published further consideration must be given to viewing both studies, a 200 bed hospital with a HO-CDI rate at the environmental hygiene and hand hygiene as being inter- national average and a non-reimbursed cost per case dependent interventions since these two interventions of $12,313 was projected to have an annualized sav- are intrinsically interdependent, they represent what can ings of $358,268 as a direct result of implementing be termed “hygienic practices” (Fig. 1.). daily hospital-wide patient zone sporicidal disinfection cleaning at a 70% TDC. Based on this modeling and the Conclusions population based studies discussed it is likely that the In discussing the 2022 Clean Hospitals Healthcare Clean- 8 intervention hospitals previously discussed (average ing Forum, Peters noted that “Healthcare environmental size 258 beds, HO-CDI rate at the national average pre- hygiene has become recognized as being increasingly intervention) realized an annualized savings of approxi- important for patient safety and the prevention of HAIs” mately $3.7 million per year during the last 12  months [135, p.1]. of the study. Given the fact that HO-CDI is the most frequent HAI Based on this research, it is feasible for a hospital to today, representing 56% of NHSN-reported HAIs in US project the yearly non-reimbursed cost of HO-CDI. hospitals (ref) and likely so globally, its mitigation is Taken together, these studies support the likely prob- clearly critical [136]. In light of our recent greatly clari- ability that each case of HO-CDI had a non-reimbursable fied understanding of the healthcare epidemiology of cost of approximately $12,000 between 2008 and 2019. HO-CDI; implementation of new antibiotic and test- While the current cost can be estimated based on these ing stewardship programs; the development of new studies Yu and co-authors in 2019 noted that, “As CDI potent sporicides which can be used on a daily basis for management evolves, the already substantial per-patient patient-zone disinfection cleaning; and the extensive Table 2 Population based studies which have evaluated the average attributable and non-reimbursed cost of HO-CDI in US hospitals Population based studies on the cost of HO-CDI Author Study period Publication date date Total attributable cost per case Non-reimbursed (USD) Cost Per case (USD) Shorr [122] 2008–2010 2022 $28,050 Not evaluated Mollard [123] 2012–2016 2019 $27,122 Not evaluated Sahrmann [124] 2011–2017 2022 $14,257 Yu [125] 2012–2019 2022 $28,762 $13,476 C arling et al. Antimicrobial Resistance & Infection Control (2023) 12:94 Page 11 of 14 9. Daneman N, Gutttmann A, Wang X, Ma X, Gibson D, Stukel TA. The documentation that such cleaning can be sustainably association of hospital prevention processes and patient risk factors optimized with ongoing education and objective, quan- with the risk of Clostridium difficile infection: a population-based cohort titative performance monitoring and feed-back, there study. BMJ Qual Saf. 2015;24:435–43. 10. Principi N, Gnocchi M, Gagliardi M, Argentiero A, Neglia C, Esposito S, is reason to believe that great reductions in HO-CDI et al. Prevention of clostridium difficile infection and associated diar - are feasible, particularly when hand hygiene is also rhea: an unsolved problem. Microorganisms. 2020;8:1640. optimized. 11. Doll ME, Zhao J, Kkang L, Rittmann B, Alvarez M, Fleming M, et al. Chasing the rate: an interrupted time series analysis of interventions While studies incorporating genomic epidemiology will targeting reported hospital onset Clostridioides difficile, 2013–2018. Inf be needed to quantify the impact of HO-CDI mitigation Control Hosp Epidemiol. 2020;41:1142–7. on other HAIs, the documented mitigation of MRSA and 12. Deloney VM, Kociolek LK, Gerding DN, Carrico R, Carling PC, Donskey CJ, et al. Stratigies to prevent clostrididioides difficile infections in acute VRE acquisition with moderately improved TDC and the care hospitals 2022. Infect Control Hosp Epidemiol. 2023;44(4):527–49. environmental epidemiology of a wide range of HAPs 13. Petrosillo N. Clostridioides difficile infection: a never-ending challenge. J suggests that there will be collateral benefits of mitigating Clin Med. 2022;11(4115):1–3. 14. Lessa FC, Gould CV, McDonald LC. Current status of clostridium difficile HO-CDI [74, 115]. infection epidemiology. Clin Infect Dis. 2012;55(Suppl 2):S65–70. 15. Ho J, Wong SH, Doddangoudar VC. Regional differences in temporal incidence of clostridium difficile infection: a systematic review and Author contributions meta-analysis. Am J Infect Control. 2020;48:89–94. PC developed the structure of this review and is the corresponding author. PC, 16. Mitchell BG, Shaban RZ, MacBeth D. The burden of healthcare- MP and RO participated in all aspects of the development of the manuscript associated infection in Australian hospitals: a systematic review of the and approved the final draft. literature. Epub. 2017;15:1–2. 17. Turner NA, Grambow SC, Woods C. Epidemiologic trends in Clostridi- Funding oides difficile infections in a regional community hospital network. Not applicable. JAMA Netw Open. 2019;2(10):1–12. 18. Kazakova SV, Baggs J, Yi SH. Associations of facility-level antibiotic use Availability of data and materials and hospital-onset Clostridioides difficile infection in US acute-care The manuscript will be available as open-access and through the correspond- hospitals, 2012–2018. Infect Control Hosp Epidem. 2022;43(8):1067–9. ing author. 19. Rock C, Abosi O, Bleasdale S. 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Environmental approaches to controlling Clostridioides difficile infection in healthcare settings

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Abstract

As today’s most prevalent and costly healthcare-associated infection, hospital-onset Clostridioides difficile infec- tion (HO-CDI) represents a major threat to patient safety world-wide. This review will discuss how new insights into the epidemiology of CDI have quantified the prevalence of C. difficile (CD) spore contamination of the patient- zone as well as the role of asymptomatically colonized patients who unavoidable contaminate their near and dis- tant environments with resilient spores. Clarification of the epidemiology of CD in parallel with the development of a new generation of sporicidal agents which can be used on a daily basis without damaging surfaces, equipment, or the environment, led to the research discussed in this review. These advances underscore the potential for sig- nificantly mitigating HO-CDI when combined with ongoing programs for optimizing the thoroughness of clean- ing as well as disinfection. The consequence of this paradigm-shift in environmental hygiene practice, particularly when combined with advances in hand hygiene practice, has the potential for significantly improving patient safety in hospitals globally by mitigating the acquisition of CD spores and, quite plausibly, other environmentally transmitted healthcare-associated pathogens. Keywords Clostridioides difficile, Hospital onset Clostridioides difficile infection prevention, Disinfection cleaning, Optimized cleaning performance, Sporicidal disinfectant, Healthcare-associated infections Introduction surface cleaning interventions and concomitant hand As noted by Peters in 2022, healthcare-associated infec- hygiene practice can be quantified to develop clinically tions (HAI) are one of the greatest threats to patient sound implementation science has yet to achieved [2, 3]. safety worldwide [1]. As a result of epidemiologic and Despite such ongoing challenges it is important to rec- microbiologic studies over the past decade, it has become ognize that environmental hygiene represents a critical increasingly evident that interventions to mitigate envi- element of what Wenzel and Edmonds defined as “hori - ronmental surface pathogen contamination constitute zontal interventions” that are central to mitigating a wide an important component of (HAI) prevention. Unfor- range of HAIs (Fig.  1) [4, 5]. These approaches aim to tunately, precisely defining how the impact of various reduce the risk of infections caused by a broad range of pathogens by the implementation of standard practices that are effective regardless of patient specific conditions *Correspondence: [6]. In contrast to the horizontal interventions, “vertical Philip C. Carling interventions” are pathogen and/or condition specific. Pcarling@comcast.net While vertical and horizontal approaches are often com- Carney Hospital, Boston, MA, USA Stamford Medical Center, Stamford, CT, USA plementary, there is evolving evidence that horizontal Trinity Health, Lavonia, MI, USA interventions in endemic situations may represent a best © The Author(s) 2023. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecom- mons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Carling et al. Antimicrobial Resistance & Infection Control (2023) 12:94 Page 2 of 14 ribotype 027 fell by half between 2007 and 2010, likely due to a concurrent reduction in fluroquinolone use [2]. While the overall trend toward decreasing CDI in Europe is of note, between 23 and 66% of cases in a range of European countries [2] and 50–60% of cases in Australia were found to be under diagnosed due to a lack of clinical suspicion and suboptimal laboratory methods [16]. In the United States, CDI rates had been showing a gradual decrease during the decade prior to the COVID pandemic, primarily due to decreases in HO-CDI [17]. Several factors would appear to have contributed to the Fig. 1 The elements of Horizontal Healthcare Hygienic Practices. The declining incidence including antimicrobial stewardship blue arrows represent the interdependence between the elements [18], better diagnostic stewardship [19] and reimburse- ment negative incentive programs [20]. While some facilities experienced increases in HO-CDI early in the use of HAI prevention resources [6, 7]. As noted in Fig. 1, COVID pandemic, recent more extensive studies have Healthcare Hygienic Practice consists of interventions failed to document a significant trend in CDI rates [21, which have traditionally been addressed separately, but 22]. as will be discussed below, their effectiveness in clinical settings is highly interrelated and interdependent. Evolving insights into healthcare environmental The burden of healthcare associated Clostridiodes dif - Clostridioides difficile epidemiology ficile Infection (CDI), coupled with the expectation that Given the extremely low inoculum necessary to cause improved environmental cleaning could prevent these infection [23] and the fact that CD spores on environ- infections, has led to extensive efforts to mitigate trans - mental surfaces have a basically indefinite ability to mission risk within healthcare settings since 1981 when remain viable decreasing only 0.5 log in 14  months [24] Fekety et al. [8] documented widespread healthcare envi- it is not surprising that surfaces contaminated with CD ronmental contamination of surfaces, both near and spores have a role in CD transmission. Recent studies more distant from patients with CDI. Although numer- have clarified and quantified many aspects of the envi - ous quasi-experimental studies substituting dilute bleach ronmental epidemiology of CD in hospitals (Table 1). for non-sporicidal disinfectants have reported a reduc- As noted in Elements 1 and 2, recent studies have tion in healthcare-associated CDI (HO-CDI) during shown that a substantial proportion of all acute care outbreaks, efforts to effectively mitigate environmen - patients are colonized with CD either at the time of tal transmission of Clostridiodes difficile (CD) spores admission (average incidence density 10.6%, range in endemic settings has been ineffective [9–12]. New 2.8–21% [25–35] or during their hospitalization (aver- insights into the healthcare epidemiology of HO-CDI age prevalence density 12.5%, range 2.9–21%) [25, and new approaches to mitigating environmental trans- 36–41]. As a result, approximately 11% of hospital- mission will be discussed in detail in this review. ized acute care patients present an ongoing risk of CD transmission to the environment and susceptible Global and healthcare epidemiology patients. Genomic epidemiology has now confirmed of Clostridioides difficile infections the environmental transmission of spores from these Global epidemiology patients to other patients [37, 42–45]. As noted in Ele- Although accurate assessments of global trends in CDI ment 3, patients recovering from acute CD infection prevalence are challenged by variations in diagnostic are associated with significant transmission of spores methods as well as resource limitations impeding sur- to their environment [46–48]. This issue was care- veillance activities [2, 13], the world wide epidemiol- fully analyzed in a multi-site study by Davies et  al. in ogy of CDI has been characterized by rapidly evolving 2020 which evaluated the impact of treatment for CD shifts in prevalence of disease [14]. A recent review of infection on patient-zone environmental contamina- regional differences in (CDI) noted that global infections tion [49]. Treatment of CD infection with metronida- have been slowly decreasing between 2 and 4% per year zole, vancomycin or fidaxomicin similarly decreased through 2015 in most European countries while Asia has the proportion of patients with positive stool cultures shown increasing trends through 2014 primarily due to from 100 to 35% immediately after treatment. Fol- increases in western Asia countries including Turkey and lowing treatment, the rate rebounded to 80–90% by Israel [15]. In England declining rates of infection with 2–4 weeks later. And although there was a decrease in C arling et al. Antimicrobial Resistance & Infection Control (2023) 12:94 Page 3 of 14 Table 1 The elements of Clostridioides difficile healthcare epidemiology Elements of Clostridioides difficile Environmental Epidemiology 1. At the time of hospitalization 10.6% of patients (range 2.8–21%) are CD carriers Ref: [25–35] 2. During hospitalization 12.5% of patients (range 2.9–21%) are CD carriers Ref: [25, 36–41] 3. Transmission of CD spores to environmental surfaces is associated with: Ref: [46–48] Patients with acute infection Patients recovering from acute infection Asymptomatic CD colonized patients 4. Treatment does not decrease ongoing environmental spore contamination for more than a month Ref: [49] 5. Wide spread surface contamination far from known CD infected patients Ref: [35, 36] 6. Increased Cleaning and disinfection result in: Ref: [99] Decreased surface and hand contamination Decreased CD acquisition 7. Genomic confirmation of the role of asymptomatic CD carriers in transmission Ref: [37, 42–45] 8. Acquisition of CD from a prior room occupant is significantly dependent on the prior room occupant receiving antibiotics Ref: [52, 53] the proportion of environmental sites contaminated Mitigating Clostridiodes difficile spore transfer with CD spores from 36% before treatment to 20% from environmental surfaces immediately following treatment, environmental con- Chemical disinfection tamination by these patients was still at 27% four weeks Chlorine-based disinfectants, particularly diluted com- after completing treatment, confirming the significant mercial grade bleach has been used extensively for ongoing risk of transmission of CD to other patients terminal cleaning of CDI patient rooms [54]. Unfortu- and healthcare workers by patients who had completed nately, physical damage associated with the use of these treatment for CDI. These studies confirm substantial disinfectants precludes their daily use for all high-touch levels of environmental contamination, but they may patient-zone surfaces. Fortunately, we now have broad- actually under-estimate the problem. A recent study spectrum sporicidal agents that are at least as effective as using PCR technology confirmed a tenfold increase in bleach, are not associated with significant damage to sur - the frequency of surface contamination in comparison faces, and are not associated with potentially toxic resid- to direct culture [50]. In 2015 Kundrapu, documented uals during either their use or disposal [55, 56]. These that spore shedding and near patient environmen- hydrogen peroxide/peroxyacetic acid formulation chem- tal contamination with CD spores was substantially istries are rapidly sporicidal and are also effective against increased when asymptomatic patients colonized with Candida auris, healthcare-associated pathogens (HAPs), CD were administered antibiotics [51]. The clinical norovirus and other viral pathogens, including corona relevance of this phenomenon was subsequently clari- viruses [57]. While these chemistries have been widely fied by Freedburg et al. [52].They analyzed a cohort of used and their effectiveness well validated, other non- more than 100,000 patients who sequentially occupied chlorine based sporicidal agents are becoming available. a given hospital bed and found that independent of the prior room occupant’s CDI status, administration Surface disinfection technologies of antibiotics to the prior bed occupant was the most Despite in  vitro studies confirming the resistance of CD significant factor associated with an increased risk of spores to UV light, programs incorporating UV technol- the next bed occupant developing CDI. The same phe- ogy have been reported to have impacted HO-CDI rates nomenon was also identified by Dowling Root in 2021 in hyper-endemic settings [58]. In contrast, several more [53]. In this study of 17,285 patient room occupancies recent reports of such programs failed to show an impact the risk of HO-CDI was significantly associated with on endemic HO-CDI rates [12, 59–62] and a multi-year prior room occupant antibiotic usage (Odds Ratio cluster randomized crossover control trial found that 2.37, p < .001). The results of these two large studies, the daily UV supplemented intervention did not reduce can only be explained by recipient acquisition of resid- either HO-CDI rates or VRE transmission [63]. These ual CD spores asymptomatically shed onto patient- results have now been further supported by a cluster-ran- zone surfaces by the preceding room occupant. domized sham-controlled double blinded crossover trial Carling et al. Antimicrobial Resistance & Infection Control (2023) 12:94 Page 4 of 14 of a UV program, by Kaye et al. involving 25,732 patient performance feedback to EVS staff were shown to be room cleanings. It failed to show an impact on HO-CDI highly effective in improving cleaning outcomes [78, rates, which were actually higher in the sham UV treat- 79]. Despite the challenges the EVS staff contend with ment arm (p 0.53) [64]. Furthermore, the prevalence of [80], published reports of these programs have now E. coli and Staph. aureus contamination of high-touch confirmed the effectiveness of such programs with the patient-zone surfaces was unchanged [65, 66]. Uncon- TDC improving from 40–60% to 80–90% or higher trolled studies utilizing hydrogen peroxide vapor tech- for at least 3 years [79, 81]. Most recently Parry (2022) nology as part of terminal cleaning of CDI patient rooms evaluated the sustained impact of a structured ongoing have appeared to be associated with a decrease in HO- monitoring and feedback program to optimize patient- CDI [67–69] but they were lacking confounder assess- zone disinfection cleaning in a 305 bed acute care hos- ment. In addition, logistical challenges in delivering the pital over 10 years [82]. treatment may hinder the use of this technology beyond The cleaning/disinfection performance of the EVS staff CDI isolation room terminal cleaning [58]. was covertly measured by specially-trained infection pre- vention nurse liaisons to minimize bias and telegraphing surface marking sites. As noted in Fig. 2, cleaning perfor- A programmatic approach to optimizing mance improved from a baseline TDC of 60% to greater environmental hygiene to mitigate HO‑CDI than 80% over the first year of the program. Subsequently Evaluating disinfection cleaning most quarterly rates were at or above the 90% minimum The importance of physically removing visible dirt and target during the final six years reported. The process soil from surfaces in hospitals has been recognized for improvement success of programs related to patient zone more than 150  years [70]. Consequently, all acute care disinfection cleaning had also been realized with respect hospitals have policies and procedures to define the to the operating theatre setting [82, 83]. role of environmental services personnel for cleaning “Tools For Evaluating Environmental Cleaning: The patient-zone surfaces. Environmental services (EVS) Guidance Environmental Cleaning Procedures” As a managers and infection preventionists had imple- result of published evidence supporting objective moni- mented joint visual inspection of surfaces in patient toring to evaluate surface cleaning processes, the CDC care areas well before the CDC recommended that developed the guidance “Options for Evaluating Environ- hospitals clean and disinfect “high-touch surfaces” in mental Cleaning” in 2010 and updated it in the Guidance 2003 [71]. The CDC further recommended that hos - “Best Practices for Environmental Cleaning Procedures” pitals “monitor, (i.e., supervise and inspect cleaning in 2020 [77, 84]. which recommends the use of a fluo - performance) to assure consistent cleaning and dis- rescent marker-based performance monitoring program infection of surfaces in close proximity to the patient along with direct observation of cleaning practice. and likely to be touched by the patient and healthcare Studies in the United States and abroad during the past professionals” in 2006 [72]. Unfortunately, the intrinsi- 20  years have used a specially developed fluorescent gel cally subjective nature of such monitoring along with or “test soil” to covertly evaluate environmental clean- its episodic and deficiency-oriented features limit its ing in a wide range of healthcare settings [75, 76, 85– ability to accurately assess the thoroughness of day-to- 89]. These studies have utilized a standardized metered day cleaning activity. Preliminary studies documenting transparent gel specifically formulated for the covert patient zone surface contamination with HAPs raised evaluation of healthcare surface cleaning. While non- concerns that cleaning practice should be improved standardized fluorescent powders and lotions have been [73]. It was not until actual cleaning practice was objec- used in a non-covert manner for education [90], other tively monitored, initially using a covert visual moni- studies [89, 91] demonstrated that these substances vis- toring program [74] and later with covertly applied ibility in ambient light limited their effective use in pro - fluorescent markers, that actual cleaning practice was grams to objectively monitor cleaning practice as a result objectively evaluated [75, 76]. Evaluations were done of their ability to induce a Hawthorne effect. In 2019 a in a standardized manner with a metered fluorescent ™ study from Johns Hopkins compared the clinical use of marking system (DAZO Ecolab, Inc., St. Paul, MN). the metered applicator with a standardized fluorescent The outcome measured was the actual thoroughness gel to a cotton swab applicator with a non-standardized of cleaning expressed as the “thoroughness of disin- fluorescent gel and found that the metered applicator fection cleaning” or”TDC” [77]. Given the accuracy provided a more accurate assessment of cleaning prac- of the metered fluorescent markers to objectively and tice. The authors concluded that, “Infection control reproducibly identify opportunities to improve clean- programs implementing evaluation of environmental ing thoroughness, process improvement interventions cleaning programs should carefully consider the type based on structured educational activities and direct C arling et al. Antimicrobial Resistance & Infection Control (2023) 12:94 Page 5 of 14 Fig. 2 The thoroughness of disinfection cleaning as objectively documented by the standardized florescent marker monitoring program and method of applying fluorescent gel marks to stand - of the actual EVS cleaning programs. Such an approach, ardize and optimize the measurement of fluorescent gel as discussed previously, assures the validity of the infor- removal” [92, p.796]. mation collected” [77 (Appendix B, p.1, 82]. The impor - ATP bioluminescence technology detects the pres- tance of this issue was confirmed in a study which found ence of organic material, including viable and non- that when EVS managers monitored the discharge room viable bioburden, on surfaces. Although their ease of cleaning, they documented an average TDC score of use led to their use to attempt to quantify healthcare 82.5% while a research team covertly evaluating the same surface bioburden, the high sensitivity of the system to two hospitals documented an average score of 52.4% [96]. non-microbiologic and non-viable organic matter and Given the fact that neither the Joint Commission or the its relative insensitivity to some healthcare-associated World Health Organization consider self-monitoring of pathogens has now been clarified [93, 94]. As noted by hand hygiene practice to be acceptable, it seems reason- Mulvey, et  al. in a detailed evaluation of the ATP tech- able that a similar expectation should be applied to moni- nology, “Sensitivity and specificity of 57% (with the ATP toring disinfection cleaning activities. tool) means that the margin for error is too high to justify stringent monitoring of the hospital environment (with Implementing the 2020 CDC guidance: core ATP technology) at present” [95, p.29]. As noted in the components of environmental cleaning CDCs Guidance Best Practices for Environmental Clean- and disinfection in hospitals ing in Healthcare facilities (2020): (Section  4. Tables  29 In October 2020 the CDC published a guidance docu- and 30) ATP technology is not recommended for evaluat- ment to provide hospitals with a detailed roadmap for ing cleaning performance [84]. the development of programs to optimize all aspects of An important requirement for monitoring and pro- patient-zone environmental hygiene because “maintain- cess improvement programs relates to the need for them ing a clean hospital environment and minimizing the to have a successful validation component. As noted in presence of hospital pathogens is critical for keeping the 2010 CDC guidance, “It is important that the moni- patients safe” [97, p.e1]. toring be performed by hospital epidemiologists, infec- The six individual “core components” (Fig.  3) and the tion preventionists or their designees who are not part specific recommendations within each of the strategies Carling et al. Antimicrobial Resistance & Infection Control (2023) 12:94 Page 6 of 14 CDC Core Components of Environmental Cleaning and Disinfec on in Hospitals 1. Integrate Environmental Services into the Hospital’s Safety Culture 2. Educate and Train all Healthcare Providers Responsible for Cleaning and Disinfec ng Pa ent Care Areas 3. Select Appropriate Cleaning and Disinfec on Technologies and Products 4. Standardize Se€ng-specific Cleaning and Disinfec on Protocols 5. Monitor Effec veness and Adherence to Cleaning and Disinfec on Protocols 6. Provide Feedback on Adequacy and Effec veness of Cleaning and Disinfec on to All Responsible HCP as well as Relevant Stakeholders (e.g., Infec on Control, Hospital Leadership) Fig. 3 The CDC core elements of environmental cleaning and disinfection in hospitals Fig. 4 The impact of optimizing environmental hygiene to decrease Clostridioides difficile transmission in a single hospital over two and one half years detailed in the document specify what “every healthcare facility should consider to ensure appropriate environ- mental cleaning and disinfection” [98, p.e1]. While not specifically discussed in the document, describing the analysis employing a group of eight acute care hospitals (EVS) staff involved in patient-zone cleaning and disin - [99]. These hospitals had stable endemic Standardized fection as “healthcare personnel” represents an acknowl- Infection Rates (SIRs) (Mean 1.03 for the group) during edgment of the relevance these activities have to safe an 18-month pre-intervention period. The intervention patient care. Taken together, these Core Components hospitals within the healthcare system studied ranged provide a detailed, clearly structured, comprehensive in size from a 532-bed tertiary care hospital to a 44-bed template, based on implementation science studies over regional critical access hospital (mean 257 beds). Nine the past 20 years, to optimize all aspects of environmen- randomly selected hospitals from the same system tal hygiene practice for acute care hospitals which can that had not enrolled in a standardized (EVS) process also be adapted to a wide range of patient care settings improvement program served as controls. (mean 266 [81]. beds). Thoroughness of cleaning was programmatically monitored in accordance with the 2010 CDC guid- ance[77] using a standardized metered fluorescent Assessment of the potential impact of thorough marking system (DAZO Ecolab, Inc., St Paul, MN). daily sporicidal disinfection cleaning in mitigating HO‑CDI Given the fact that general use of sporicidal disinfectants on patient-zone surfaces is now feasible, it is possible to quantitively assess the impact of daily sporicidal disinfec- tion cleaning of all high-touch patient-zone surfaces in mitigating CD transmission. This approach was initially evaluated in a single-site, quasi-experimental study in 2016 [98]. As noted in Fig.  4, during the 33-month intervention period, thoroughness of disinfection cleaning (TDC) rapidly improved from 81 to 92% and remained greater than 88% during the remainder of the study (P = .01). HO-CDI rates fell significantly during the intervention period from an average of 8.9–3.2/10,000 patient-days (p = 0.0001, 95% CI 3.48–7.81). The clinical impact of implementing daily, hospital- wide sporicidal disinfectant cleaning of all patient-zone surfaces was further evaluated using a control group Fig. 5 Toroughness of Cleaning in 8 Intervention Hospitals validated, quasi-experimental, interrupted-time series C arling et al. Antimicrobial Resistance & Infection Control (2023) 12:94 Page 7 of 14 As noted in Fig.  5, TDC following educational activi- ties during the 3-month wash-in period improved rapidly from 59 to 88%. With the use of ongoing quarterly per- formance feedback, cleaning thoroughness continued to improve over the next 5 quarters and at 18  months the TDC was 93.6% for the group (Range 91–96%, 95% CI 45–24%, p < 0.0001). As noted in Fig.  6, mean group HO-CDI SIRs ranged from 0.49 below to 1.42 above a mean of 1.03 during the 18  months prior to project implementation. In quar- ter-1 following wash-in, all sites documented a decrease in HO-CDI to a mean SIR of 0.6 (95% CI 0.13–0.75, p = 0.009). Over the next 5 quarters, the HO-CDI SIR Fig. 7 Evaluation of potential confounding influences. 1. Q3 continued to decrease stabilizing during the last three pre-intervention year “Enhanced contact precautions for CD quarters evaluated to a mean SIR of 0.4 (95% CI 0.13– positive patients was implemented”. During the first 6 to 9 months 0.75, p = 0.009). of the pre-intervention period these sites implemented nursing As outlined in Fig. 7 seven potentially significant con - education to clarify the importance of early stool specimen collection founders were evaluated pre-and post-intervention and in patients with diarrhea were found not to have had an impact on the results. Using the control hospitals in an adjusted difference- in-differences analysis, the intervention was associ - HO-CDI. While a randomized controlled trial could ated with a 0.55 reduction (95% CI − 0.77 to − 0.32) further clarify and quantify the results of this interven- in HO-CDI (p < 0.001; or a 50% relative decrease from tion, such an undertaking would require considerable a baseline SIR of 1.03). The study represents the first resources as well as the need for sites to defer imple- multi-site, quasi-experimental study with control menting potentially effective design elements of the hospitals to evaluate a daily, hospital wide, perfor- intervention. mance optimized, sporicidal, disinfection cleaning on Fig. 6 The trend in HO-CDI SIR pre and post-intervention Carling et al. Antimicrobial Resistance & Infection Control (2023) 12:94 Page 8 of 14 Given the challenges of a randomized trial, it should CD transmission when TDC is lower than those achieved be noted that the open-access published, agent-based by the intervention group of hospitals discussed above modeling study by Barker, et al. evaluating the impact of [7]. Most recently, this agent-based simulation model multiple single and bundled interventions on HO-CDI was used by Scaria, to compare it with primary observed prevention found that the single most clinically effective data from a 426 mid-western, US hospital over 6  years and cost-effective intervention was daily sporicidal clean - in order to compare the predicted HO-CDI rate to the ing of all patient zone surfaces as depicted in Fig. 8 [7] observed rate between 2013 and 2018. Furthermore, quantitative input analysis of the model As noted in Fig.  9.,the trends in both the modeled found only a limited additional incremental benefit from and actual rates were nearly identical following imple- increasing modeling parameters of thoroughness of menting “increased infection control measures” namely, cleaning from an “enhanced level” (80% TDC) to an “ideal daily patient-zone sporicidal disinfection cleaning and level” (94% TDC), suggesting that daily patient zone improvement in the TDC from 56% in 2013 to 79% in sporicidal cleaning could have a substantial impact on 2017 and 2018 [100]. Of note, the decrease of 46% in HO- CDI, both predicted and observed, was similar to the decrease of 50% documented in the eight hospital study previously discussed. Additional benefits of mitigating CD environmental transmission Collateral microbiological benefits Over the past several years there has been increasing documentation of the potential and actual role of sur- faces in the near patient environment being relevant in HAI epidemiology. As noted in Fig.  10, [101–116] patient-zone environ- mental surfaces are frequently contaminated with a wide range of HAPs. While the frequency of contamination is greatest close to patients, genomic epidemiology has confirmed more distance spread [11, 116]. While docu- menting high level CRE contamination (88% of surfaces) Fig. 8 Evaluation of the modeled cost (cost-avoidance) associated with interventions to mitigate HO-CDI associated with colonized patients, the study by Shams Fig. 9 Comparison of the modeled and observed HO-CDI over 6 years C arling et al. Antimicrobial Resistance & Infection Control (2023) 12:94 Page 9 of 14 Environmental Transmission of HAPs Other Than CD A. Environmental Contaminaon of rounely Cleaned Paent-Zone Surfaces Reference MRSA, VRE, Ab, Kp 34% of random surfaces MRSA,VRE 55%of random surfaces MRSA, VRE, Ab, Ps 40% C. auris 70% KPC-producing CRE 88% of colonized paent surfaces MRSA, VRE 82% of CP room surfaces 12% of non-CP room surfaces MDROs 65% B. Genomic Epidemiologic Evidence of Environmental Transmission MRSA, VRE Transmission between paents and surface environment 109,110 MRSA and MSSA VRE, MDROs C. Decreased Environmental Contaminaon With Improved Disinfecon Cleaning MRSA 113-115 VRE GNB 104,108 MDROs and Ab D. Decreased Acquision of HAPs With Improved Disinfecon Cleaning 104,116 Ab,MRSA, VRE, Fig. 10 Studies which have clarified the potential for optimized patient-zone disinfection cleaning to mitigate the transmission of healthcare -associated organisms from environmental surfaces also found that 80% of all contamination was associated quantified. As part of the agent-based modeling study with 20% of colonized patients which they character- previously described, Barker used a standardized quality- ized as “super shedders” [101, 117] Although many of the of-life years (QALYs) analysis and found that the impact HAI-associated pathogens in Fig. 10 are effectively killed of the daily, performance optimized (80% TDC) spori- by quaternary-ammonium compounds, or accelerated cidal disinfection patient-zone cleaning intervention in hydrogen peroxide the use of hydrogen peroxide-peroxy- the modeled 200 bed hospital with a 1.0 SIR was associ- acetic acid chemistries for CD mitigation would allow for ated with a savings of 36.8 QALY s annually for such a highly effective disinfection of surfaces harboring Can - program [7]. dida auris, norovirus and quaternary-ammonium resist- In addition to QALYs lost as a result of CDI, the ill- ant A. baumannii [118]. ness has a substantial adverse impact on patient reported Finally, it should be noted that recent reports docu- quality of life. This phenomenon was recently quanti - menting widespread intra-system and inter-system trans- fied in a controlled study by Han (2022) using a health- mission of carbapenem-resistant Klebsiella pneumoniae related quality of life 32 element questionnaire [121]. The and the possibility that terminal patient room clean- study found that patients hospitalized with CDI devel- ing enhanced by a UV treatment protocol can impact oped a quantifiable negative impact on multiple physical the occurrence of hospital-onset bacteremia with some and mental health measures. Of note was a particularly strains of gram negative rods suggest that there is yet adverse impact of recurrent CDI (10% of patients) on the much to be clarified regarding the role of patient zone quality-of-life parameters measured. surfaces in the epidemiology of many HAPs [119, 120] Economic benefits Quality of life benefits While the direct impact of CDI in terms of morbid- While the acute morbidity and mortality (approximately ity and mortality has been well documented, several 5%) of CDI have represented significant issues for years, in-depth population based studies published between analysis of more complex effects of CDI are now being 2011 and 2022 have analyzed the economic costs of CDI Carling et al. Antimicrobial Resistance & Infection Control (2023) 12:94 Page 10 of 14 [122–125]. In considering the impact of these costs, it health care costs and health care utilization associated is critically important to note that a substantial propor- with CDI are likely to increase” [125, p.1]. tion of the total costs per case are not reimbursed by commercial insurance, Medicare or Medicaid in U.S. Environmental hygiene and hand hygiene: hospitals. As summarized in Fig.  10, four studies have an integrated approach specifically evaluated the cost of HO-CDI (Table 2 ). Over the past several years it has become increasingly These matched controlled studies evaluated between evident that infection prevention initiatives focused on 6000 and 60,000 HO-CDI cases over 2–7  years. The optimizing hand hygiene have not realized their hoped- three studies which evaluated total cost found almost for impact on healthcare-associated pathogen (HAP) identical results while the two studies which evaluated transmission in well-resourced healthcare settings non-reimbursed costs also found highly similar costs of [129–133]. Accepting our inability to quantify the abso- $14,257 and $13,476 or approximately 50% of the total lute risk of pathogen acquisition directly from healthcare cost. This proportion of non-reimbursed costs is also workers’ hands, there is good circumstantial evidence consistent with an earlier study of 272, 143 hospitaliza- that such transmission accounts for a substantial propor- tions which found that 65% of the cost of HO-CDI was tion of HAP transmission. Indeed, it has become widely not reimbursed by Medicare payments [126]. Although accepted that hand hygiene, as noted by Palamore, is not stratified to identify costs for HO-CDI, Magee in “critically important for the prevention of HAIs” [134] 2015 determined the excess cost for hospitalized CDI (p.8). patients to be $24,408 based on data from 2009 to 2011 Given the fact that patient zone surfaces not con- [127]. In a similar study Zhang in 2019 found excess taminated by HAPs cannot be a source of pathogen total cost per case of $24,205 [128]. transmission even in the absence of hand hygiene, As modeled by Barker [7] using data from published further consideration must be given to viewing both studies, a 200 bed hospital with a HO-CDI rate at the environmental hygiene and hand hygiene as being inter- national average and a non-reimbursed cost per case dependent interventions since these two interventions of $12,313 was projected to have an annualized sav- are intrinsically interdependent, they represent what can ings of $358,268 as a direct result of implementing be termed “hygienic practices” (Fig. 1.). daily hospital-wide patient zone sporicidal disinfection cleaning at a 70% TDC. Based on this modeling and the Conclusions population based studies discussed it is likely that the In discussing the 2022 Clean Hospitals Healthcare Clean- 8 intervention hospitals previously discussed (average ing Forum, Peters noted that “Healthcare environmental size 258 beds, HO-CDI rate at the national average pre- hygiene has become recognized as being increasingly intervention) realized an annualized savings of approxi- important for patient safety and the prevention of HAIs” mately $3.7 million per year during the last 12  months [135, p.1]. of the study. Given the fact that HO-CDI is the most frequent HAI Based on this research, it is feasible for a hospital to today, representing 56% of NHSN-reported HAIs in US project the yearly non-reimbursed cost of HO-CDI. hospitals (ref) and likely so globally, its mitigation is Taken together, these studies support the likely prob- clearly critical [136]. In light of our recent greatly clari- ability that each case of HO-CDI had a non-reimbursable fied understanding of the healthcare epidemiology of cost of approximately $12,000 between 2008 and 2019. HO-CDI; implementation of new antibiotic and test- While the current cost can be estimated based on these ing stewardship programs; the development of new studies Yu and co-authors in 2019 noted that, “As CDI potent sporicides which can be used on a daily basis for management evolves, the already substantial per-patient patient-zone disinfection cleaning; and the extensive Table 2 Population based studies which have evaluated the average attributable and non-reimbursed cost of HO-CDI in US hospitals Population based studies on the cost of HO-CDI Author Study period Publication date date Total attributable cost per case Non-reimbursed (USD) Cost Per case (USD) Shorr [122] 2008–2010 2022 $28,050 Not evaluated Mollard [123] 2012–2016 2019 $27,122 Not evaluated Sahrmann [124] 2011–2017 2022 $14,257 Yu [125] 2012–2019 2022 $28,762 $13,476 C arling et al. Antimicrobial Resistance & Infection Control (2023) 12:94 Page 11 of 14 9. Daneman N, Gutttmann A, Wang X, Ma X, Gibson D, Stukel TA. 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Presented at the interscience conference on antimicrobial agents and Learn more biomedcentral.com/submissions chemotherapy 2015. San Diego

Journal

Antimicrobial Resistance and Infection Control – Springer Journals

Published: Sep 7, 2023

Keywords: Clostridioides difficile; Hospital onset Clostridioides difficile infection prevention; Disinfection cleaning; Optimized cleaning performance; Sporicidal disinfectant; Healthcare-associated infections

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