Environmental Cleaning and Healthcare Associated Infection in Asia : A Perspective

Introduction

Contaminated environmental surfaces in patient rooms are a critical component in healthcare-associated infection (HAI) transmission¹ and a well-recognised common source of nosocomial outbreaks.^2-3 It has also been well demonstrated that contact with a contaminated environment by healthcare personnel (HCP) is equally as likely as a direct contact with a patient, which leads to the contamination of the healthcare provider's hands or gloves that may result in patient-to-patient transmission of nosocomial pathogens.⁴ Thus, environmental surfaces and shared noncritical medical equipment may become contaminated with infectious agents and contribute to cross-transmission through the acquisition of transient hand carriage by HCP.⁵ Furthermore, evidence suggests that a patient admitted to a room previously occupied by a patient with methicillin-resistant Staphylococcus aureus (MRSA), vancomycin-resistant enterococci (VRE), multidrug-resistant Acinetobacter baumannii, or Clostridioides (Clostridium) difficile is at a substantially increased risk for acquiring these pathogens.^6-10 Therefore, improving cleaning and disinfection of room surfaces will decrease the risk of HAIs in both resource-available and resource-limited settings in Asia.

Environmental cleaning practices and challenges in resource-limited settings

Standard methods to improve the cleaning/disinfection of environmental surfaces in hospital rooms include improving cleaning/disinfection by environmental service workers through education and feedback on cleaning effectiveness (e.g., use of fluorescent dyes), ‘no-touch’ methods (e.g., UV-C irradiation), and, in the future, possible use of self-disinfecting surfaces (e.g., impregnating or coating surfaces with heavy metals, such as silver or copper, or a germicide).^11-13 In resource-limited settings, with the limitation of access to technology, it is important to adhere to basic concepts of environmental cleaning through the use of a risk stratification matrix in order to help determine the needed frequency of environmental cleaning/ disinfection (ECD).^­14 Data on the practice of ECD in resource-limited settings is limited. Notably, a national survey in Thailand¹⁵ revealed that >90% of surveyed hospitals (n=212) reported having implemented an ECD protocol. However, only 55.2% (117/212) had an ECD checklist available, and 43.4% (92/212) had a mechanism to audit ECD practices. Among the hospitals implementing an ECD protocol, a high adherence to implemented ECD protocols and ECD checklists was documented only in 56.8% (109/192) and 57.3% (67/117), respectively.¹⁵ Because routine and terminal environmental cleaning by environmental service workers are frequently inadequate,¹⁶ these data emphasize the need to have mechanisms for monitoring adherence to ECD protocols and RCD checklists. Interestingly, methods used to audit ECD practices include a visual inspection of cleanliness (66%), microbiological monitoring (57%), fluorescence marking (14%), and ATP or bioluminescent testing (10%). It is recognized that barriers and challenges for hospitals to effectively implement ECD protocol include staff concern, inadequate education provided to staff, lack of resources and funding, time constraints, and uncertainty regarding which cleaning and disinfecting products to use. ¹⁵

Simple suggestions to reduce environment-related infections in resource-limited settings, if implementable, include the following: 1) All mattresses should be covered with a plastic liner that completely encloses the mattress, which makes cleaning easier and eliminates the possibility of mattresses becoming contaminated with liquids and harbouring bacteria. 2) All chairs should be cleanable (e.g., made of wood or plastic and not covered in fabric, which can lead to VRE transmission). 3) A combined cleaner/disinfectant solution should be used. 4) All touchable surfaces should be cleaned periodically (ideally daily but may vary depending on the risk), when soiled, and for terminal disinfection (patient discharged). 5) Environmental service workers should be trained at the start of their employment and yearly and should wear personal protective equipment (e.g., disposable gloves), if available. 6) Each nursing unit should have a checklist, which defines the items that should be cleaned/disinfected by environmental services and those that should be cleaned/disinfected by nurses. 

Environmental cleaning/disinfection and HAls 

It is estimated that contaminated environmental surfaces in patient rooms contribute up to approximately 20% of several key HAI pathogens (e.g., MRSA, VRE, MDR Gram-negative bacilli, and C difficile) transmission in intensive care units.^{6-10, 16} All of these pathogens have been demonstrated to persist in the environment from hours to days or, in some cases, up to months.¹⁷ Furthermore, these pathogens have been demonstrated to frequently contaminate the surface environment and medical equipment in the rooms of colonized or infected patients, to transiently colonized hands of HCP, to be associated with person-to-person transmission, and to cause outbreaks in which environmental transmission deems to play a role.^4-17 Throughout several regions of the world, hospital surfaces have also been demonstrated to be contaminated by several key emerging infectious diseases, such as the severe acute respiratory syndrome coronavirus (SARS-CoV), novel influenza, and Middle East respiratory syndrome coronavirus (MERS-CoV),^18-22 and have been linked as a cause of person-to-person transmission of these pathogens.²²

In Asia, despite the limitations of research that has focused on the impact of environmental cleaning/disinfection on HAIs, a few works, performed during major floods, demonstrated that infection prevention measures featuring an advanced source control and environmental cleaning can significantly limit the transmission of MDR A. baumannii within a single institution and for the surveyed hospitals.^23-24 Furthermore, the role of environmental cleaning has been highlighted in one national survey in Thailand that demonstrated the association of the presence of environmental cleaning service with the reduction of MDR A. baumannii rates.²⁵ In a recent network meta-analysis²⁶ that included works from resource-available and resource-limited settings, the impact of environmental cleaning may have differential effects on different MDR Gram-negative bacilli. Although a combination of infection prevention approaches, inclusive of standard practices (e.g., adherence to hand hygiene and contact precaution recommendations), antibiotic stewardship, environmental cleaning, and source control, is the most effective intervention to prevent MDR Gram-negative bacilli infections, environmental cleaning plays a critical role in the control of MDR A. baumannii.²⁶ Together, these data highlight the need to enhance environmental cleaning to help effectively control MDR Gram-negative pathogens, particularly MDR A. baumannii, in resource-limited settings. 

Prerequisites of establishing an effective environmental cleaning program in Asia 

In a study that evaluated three-phase cleanliness in a surgical room in a Thai tertiary care center (unpublished data), the investigators tested the cleanliness before cleaning, after manual cleaning, and after a hydrogen peroxide system. The investigators performed RODAC plate cultures before cleaning, after manual cleaning, and after a hydrogen peroxide system. Despite the fact that the hydrogen peroxide system produced the best outcome in reducing the bioburden of pathogens, the RODAC plates revealed that the highest pathogen bioburden occurred after the manual cleaning, which emphasizes the need for the education and training of environmental staff in resource-limited settings. In addition, in a two-stage observational study comparing manual bed cleaning in high- and low-resource settings,²⁷ mattresses in the low-resource settings were found to be highly contaminated prior to cleaning. Cleaning significantly reduced the biological contamination of mattresses in the low-resource settings. After a training, the contamination observed after cleaning in the high- and low-resource settings seemed comparable, and cleaning with the appropriate type of cleaning materials adequately reduced the contamination of mattresses. Predictors for contaminated mattresses in a low-resource setting included the type of products used, type of wards, training, and level of contamination prior to cleaning. The authors concluded that routine manual cleaning by trained staff can be as effective in a low-resource setting as in a high-resource setting.²⁷ Thus, a multimodal strategy, inclusive of the training of domestic service staff, availability of adequate time to clean beds between patient admissions, and application of the correct type of cleaning products, is needed. 

As routine and terminal cleaning of patient rooms is frequently inadequate, other key prerequisites to help implement an effective and sustainable environmental cleaning program include having good to excellent administration support, having a hospital epidemiologist available in resource-limited settings, and enhancement of the hospital safety culture. These factors have been evident in a Thai national survey,¹⁵ which reveals a relationship between having good to excellent hospital administration support for the infection control program and association with high adherence to implemented ECD protocols and ECD checklists, and having a hospital epidemiologist was associated with the presence of an ECD checklist and regular BCD auditing. National infection control curriculums should, therefore, be created to provide formal training for postgraduate physicians in infection prevention to become a hospital epidemiologist as a part of strategic infection prevention plans to improve national ECD practices. Lastly, a strong organisational safety culture and participation in a collaborative network to reduce HAI may also play a significant role to help enhance the effort of HAIs and MDKR pathogens control in resource-limited settings, as suggested by national surveys in the United States, Japan, and Thailand ^28-30

Conclusions 

Overwhelming evidence suggests the key role of environmental cleaning to help reduce the transmission of HAIs, MDR pathogens, as well as emerging infectious diseases. Despite several barriers and challenges, several data suggest a successful implementation of an environmental cleaning program in resource-limited settings. With the limited resources, resource-limited settings should adhere to basic recommendations for environmental cleaning and select a non-technology strategy first. Mechanisms to monitor, audit, and feedback should be available. Several prerequisites, inclusive of leadership support, availability of a hospital epidemiologist, appropriate education and training for staff, and implementation of a multimodal strategy, are essential for establishing an effective environmental cleaning program in resource-limited settings.