Infection Prevention and the Physical Environment

Curtis J. Donskey

The physical environment in healthcare facilities frequently becomes contaminated with healthcare-associated pathogens.¹ The importance of such contamination in pathogen transmission and the value of environmental disinfection interventions have been long been a topic of debate. In a 2004 systematic review of environmental surface disinfection interventions, it was concluded that the quality of the studies was poor with no convincing evidence of reduced infections.² However, during the past 15 years, a growing body of evidence has accumulated, suggesting that environmental contamination may contribute to transmission of a wide range of pathogens.³^,⁴^,⁵^,⁶^,⁷^,⁸^,⁹^,¹⁰ Although the quality of the studies remains suboptimal, there is also evidence that environmental disinfection interventions may prevent pathogen transmission and reduce healthcareassociated infections.¹¹^,¹²^,¹³^,¹⁴^,¹⁵^,¹⁶ Therefore, current guidelines for pathogens such as Clostridioides difficile, methicillin-resistant Staphylococcus aureus (MRSA), norovirus, and Candida auris emphasize the importance of environmental cleaning and disinfection as a control measure.¹⁷^,¹⁸^,¹⁹^,²⁰^,²¹

This chapter reviews basic concepts related to environmental contamination and pathogen transmission and summarizes recent evidence on the impact of cleaning and disinfection interventions. Practical approaches to improve manual cleaning and disinfection are emphasized. Several areas of uncertainty are also discussed. These include the role of no-touch technologies, optimal methods to monitor cleaning and disinfection, and the importance of contamination of sites such as portable equipment and wastewater drainage systems.

ENVIRONMENTAL CONTAMINATION AS A SOURCE OF PATHOGEN TRANSMISSION

Overview of Transmission Routes and Potential Interventions

Figure 42-1 provides an overview of common routes of transmission of healthcare-associated pathogens.¹ Patients colonized or infected with healthcare-associated pathogens shed organisms onto their skin, clothing, bedding, and nearby environmental surfaces.¹ In addition to surfaces in rooms, portable equipment and other fomites often become contaminated after contact with patients or contaminated surfaces.⁶^,²² Susceptible patients may acquire pathogens through direct contact with contaminated surfaces or equipment or via the hands of healthcare personnel (HCP) that have become contaminated after contact with patients or environmental surfaces.¹^,⁵ Wastewater drainage systems (eg, sinks, toilets) in patient rooms may become colonized with resistant Gram-negative bacilli and Candida species that can be dispersed to the environment, medical supplies, or personnel.²³^,²⁴^,²⁵ For many pathogens, most patients acquiring colonization do not develop clinically apparent infections. These asymptomatic carriers may shed pathogens into the environment and contribute to transmission.²⁶

Based on these routes of transmission, Figure 42-1 highlights four potential environmental disinfection strategies to reduce transmission. First, improving cleaning and disinfection of rooms of patients known to carry healthcareassociated pathogens after discharge (ie, postdischarge cleaning) will reduce the risk that patients subsequently admitted to the same room will acquire those pathogens from contaminated surfaces.⁵ Second, daily disinfection of high-touch surfaces in isolation rooms may be useful to reduce the risk of contamination of the hands of HCP contacting those surfaces.²⁷ This strategy is analogous to daily disinfection of the skin of colonized patients as a means of source control to reduce infections with pathogens such as MRSA and vancomycin-resistant enterococci (VRE).²⁸ Third, disinfection of portable equipment between patients or use of disposable equipment in isolation rooms may reduce the risk for transmission.⁵^,¹⁸ Finally, rather than focusing only on isolation rooms, efforts to improve cleaning and disinfection of all rooms may be beneficial if there is a concern that many carriers are not identified or are identified only after long delays.²⁶

Although environmental interventions are the focus of this chapter, it should be noted that other components of infection prevention bundles may also reduce the risk for environmental dissemination of pathogens. Hand hygiene after contact with contaminated surfaces and equipment will reduce the risk for dissemination of pathogens. Chlorhexidine treatment has been shown to reduce patient skin contamination with VRE with subsequent reduction in
environmental contamination, presumably through reduced shedding of VRE from skin.²⁸ Patient hand hygiene and ensuring cleanliness of patient clothing could also potentially reduce the risk that colonized patients will disperse pathogens to the environment.²⁹

FIGURE 42-1 Overview of common routes of transmission of healthcare-associated pathogens and potential environmental disinfection strategies. Patients colonized or infected with healthcare-associated pathogens shed organisms onto their skin, clothing, and nearby environmental surfaces. Susceptible patients may acquire pathogens through direct contact with surfaces or equipment or via the hands of HCP. Four sources of transmission and potential environmental disinfection strategies to interrupt transmission are shown: (1) contamination of surfaces after terminal cleaning of isolation rooms resulting in risk of acquisition by patients subsequently admitted to the same room (intervention: improve terminal room cleaning and disinfection); (2) contamination of surfaces in isolation rooms resulting in risk for contamination of HCP hands (intervention: daily disinfection of high-touch surfaces); (3) contamination of portable equipment (intervention: disinfection of portable equipment between patients or use of disposable equipment in isolation rooms); and (4) contamination of surfaces in rooms of unidentified carriers of healthcare-associated pathogens (intervention: improve cleaning and disinfection of all rooms on high-risk wards or throughout a facility). (Reprinted from Donskey CJ. Does improving surface cleaning and disinfection reduce healthcare-associated infections? Am J Infect Control. 2013;41:S12-S19.)

Evidence That Environmental Contamination Contributes to Transmission

Table 42-1 provides a summary of the evidence supporting environmental contamination as a source of pathogen transmission. Although much of the evidence is indirect, several recent reports provide substantial evidence of transmission linked to environmental contamination. The evidence is most convincing for pathogens that have a propensity to survive for prolonged periods on dry surfaces, including C difficile, VRE, MRSA, Acinetobacter species, norovirus, and C auris.¹

Contamination of Patient Rooms and Portable Equipment Surfaces in rooms of colonized or infected patients frequently become contaminated.¹ The ability to survive on dry surfaces varies for different pathogens. Organisms such as VRE, MRSA, Acinetobacter species, norovirus, and C auris can survive for days to weeks on dry surfaces, and C difficile spores can persist for months.³⁰ Many studies have demonstrated widespread contamination of surfaces with these pathogens in rooms of colonized patients, although the burden of contamination is generally low.⁸ In contrast, organisms such as carbapenem-resistant Enterobacteriaceae survive relatively poorly on dry surfaces and may be recovered less frequently from surfaces in rooms of colonized patients.³¹

TABLE 42-1 Evidence Supporting Environmental Contamination as a Source of Transmission of Healthcare-Associated Pathogens

Surfaces in rooms of colonized or infected patients and portable equipment frequently become contaminated with healthcare-associated pathogens

Many healthcare-associated pathogens survive for prolonged periods on dry surfaces

Pathogens on surfaces may be acquired on the hands of personnel or patients

Admission to a room previously occupied by a colonized or infected patient increases risk for acquisition by subsequent occupants

Contaminated shared medical equipment has been implicated as a source for transmission of healthcareassociated pathogens

Studies using benign surrogate markers have demonstrated the potential for contaminated surfaces to serve as a source of pathogen dissemination

Transfer of multidrug-resistant bacteria to gloves and gowns of healthcare personnel during patient care increases with environmental contamination

Cleaning and disinfection interventions have been associated with reductions in colonization or infection with healthcare-associated pathogens

Adapted from Weber DJ, Rutala WA, Miller MB, et al. Role of hospital surfaces in the transmission of emerging health care-associated pathogens: norovirus, Clostridium difficile, and Acinetobacter species. Am J Infect Control. 2010;38:S25-S33.

Portable equipment and other shared items also frequently become contaminated with healthcare-associated pathogens, including C difficile, MRSA, VRE, multidrugresistant Gram-negative bacilli, and C auris.³² Much of the contamination may occur when equipment is used during medical procedures and patient care activities. In an evaluation of shedding of MRSA by colonized patients during procedures, contamination was detected on 32% of surfaces touched by personnel and on 25% of portable equipment used for the procedures or care activities.²²

Transfer From the Environment to Hands of Personnel The hands of HCP are generally considered the primary source of transmission of pathogens in healthcare settings. Several recent studies have demonstrated that contaminated environmental surfaces may be an important source of hand contamination. Hand or glove acquisition of C difficile spores or MRSA occurred as frequently after contact with commonly touched environmental surfaces in patient rooms as after contact with commonly examined skin sites.³³^,³⁴ Figure 42-2 provides an illustration of contamination of gloved hands with C difficile spores after contact with a C difficile infection (CDI) patient and with surfaces in the patient’s room. Similarly, hand acquisition of VRE occurred nearly as often after touching the environment in VRE isolation room as after touching the colonized patient and the environment (52% vs 70%, respectively).³⁵ Several other studies have also demonstrated frequent acquisition of pathogens on hands after contacting contaminated surfaces.³⁶^,³⁷^,³⁸ In one study, a positive correlation has been demonstrated between isolation of C difficile from the hands of personnel caring for CDI patients and the percentage of positive environmental cultures in the CDI patient rooms.³⁷ Finally, it has been demonstrated that transfer of multidrugresistant bacteria to gloves and gowns of HCP during patient contact increases with environmental contamination.³⁸

Admission to a Room Previously Occupied by a Colonized Patient Increases the Risk for Subsequent Occupants Environmental surfaces in rooms of patients in contact precautions often remain contaminated after completion of postdischarge cleaning and disinfection.¹ Such contamination is a potential source for pathogen acquisition by subsequent room occupants. Several recent studies have demonstrated that admission to a room previously occupied by a colonized or infected patient increases the risk for subsequent room occupants to acquire the same organism.⁶ Organisms associated with increased risk have included C difficile, MRSA, VRE, and multidrug-resistant Gram-negative bacilli (Acinetobacter baumannii, extendedspectrum beta-lactamase [ESBL]-producing Gram-negative bacilli, and Pseudomonas aeruginosa). One prior study found that admission to a room previously occupied by a patient with an ESBL-producing Gram-negative bacillus was not associated with an increased risk for subsequent room occupants after adjusting for colonization pressure and antibiotic exposure in the intensive care unit.³⁹

FIGURE 42-2 Pictures showing contamination of gloved hands with Clostridioides difficile spores after examining the abdomen of a patient with C difficile infection (A) and after touching the patient’s bed rail (B).

Portable Equipment Linked to Pathogen Transmission In several outbreak investigations, contaminated shared medical equipment has been implicated as a potential vector for transmission of healthcare-associated pathogens.⁶ The types of equipment linked to transmission have included thermometers, respiratory care equipment, ultrasound probes, pressure transducers, and electrocardiogram leads. For many of these outbreaks, no definitive evidence has linked contaminated equipment to pathogen transmission. Rather, contamination of equipment has been demonstrated, and correction of deficiencies in cleaning and disinfection of equipment has been associated with reductions in colonization or infection with pathogens.⁶ However, a recent study that included highly discriminatory molecular typing strongly implicated shared equipment as a vector for transmission of VRE, including as a conduit for transmission between different intensive care unit areas.⁴⁰

The devices most convincingly linked to pathogen transmission are shared electronic thermometers. In the 1990s, shared thermometers, including rectal and oral thermometers, were linked to transmission of VRE, C difficile, and Enterobacter cloacae.⁴¹ In these outbreaks, it was demonstrated that thermometer handles were contaminated, and it was suspected that contamination on the handles was transferred to patients via the hands of personnel. Substitution of single-use disposable thermometers for shared electronic thermometers was associated with significant
reductions in CDI or VRE colonization.⁴²^,⁴³ Based on these findings, guidelines for prevention of CDI in acute care hospitals include a recommendation that single-use disposable thermometers be used in care of CDI patients.⁷ In the E cloacae outbreak attributed to contaminated thermometers, inadequate disinfection practices were identified, and correction of these practices led to control of the outbreak.⁴¹

Recently, transmission of the emerging fungal pathogen C auris has been linked to shared temperature probes.⁷ The reusable probes were wiped between patients with quaternary ammonium compound wipes, but it was noted that the probes were difficult to clean and disinfect due to their design with a two-layer rubber sheath protecting the distal end of the wire adjacent to the sensor. The relatively poor activity of quaternary ammonium compounds against Candida species may have also contributed to inadequate disinfection.⁴⁴ Discontinuation of the use of the temperature probes was associated with resolution of an outbreak.⁷

Benign Surrogate Markers Demonstrate Transmission From Environmental Surfaces Benign surrogate markers, such as nonpathogenic viruses and viral DNA, provide a powerful tool to study routes of pathogen transmission.⁴⁵ In several studies, these surrogate markers have demonstrated the potential for contaminated surfaces to serve as a vector for dissemination of microorganisms. In a medical and surgical intensive care unit, it was demonstrated that a viral DNA marker inoculated onto shared portable equipment disseminated widely to surfaces in patient rooms and provider work areas and to other types of portable equipment.⁴⁶ In hospital and nursing home units, similar dissemination of viral DNA surrogate markers has been demonstrated from thermometer handles and television remote controls.⁴⁷^,⁴⁸

One observation from recent studies using highly discriminatory molecular typing methods is that genetically related organisms are often detected in patients with no shared exposure on the same ward.⁴⁹ Benign surrogate markers provide a means to evaluate the potential for personnel and equipment to disseminate pathogens between wards. In an observational study, a viral DNA marker inoculated onto portable equipment on a medical ward disseminated to other wards when equipment was shared.⁵⁰ Figure 42-3 provides an illustration of transfer of the marker from a contaminated bladder scanner on one ward to three patient rooms on another ward when the device was borrowed by a nurse from the other ward. These findings highlight the potential for portable equipment to serve as a vector for dissemination of pathogens between wards.

FIGURE 42-3 Illustration of transfer of a viral DNA surrogate marker inoculated onto a bladder scanner on one ward to three patient rooms on another ward when the device was borrowed by a nurse from the other ward. (Reprinted from Donskey CJ, Sunkesula VCK, Stone ND, et al. Transmission of Clostridium difficile from asymptomatically colonized or infected long-term care facility residents. Infect Control Hosp Epidemiol. 2018;39:909-916.)

Healthcare Linens as a Source of Mucormycosis

Mucormycosis is an invasive fungal infection caused by fungi of the order Mucorales. Recent outbreaks of healthcare-associated mucormycosis in immunocompromised patients have been linked to contaminated healthcare linens or laundry carts.⁵¹^,⁵²^,⁵³ Thus, healthcare facilities should be aware of the regulatory requirements for cleaning, transporting, and storing linen and regularly review the processes used in their facility.⁵¹^,⁵²^,⁵³ In a recent culture survey of 15 transplant and cancer hospitals, Mucorales were recovered from >10% of freshly laundered linens.⁵⁴ In another recent report, it was demonstrated that C difficile spores were not effectively eliminated by laundering in a commercial washer extractor.⁵⁵ Additional studies are needed to clarify the significance of these findings. There is also a need to determine if strategies such as routine microbiologic surveillance of linens may be beneficial in settings where immunocompromised patients receive care.

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