Abstract
Healthcare-associated infections (HCAIs) are a major source of morbidity and mortality and are the second most prevalent cause of death. Furthermore, it has been reported that for every one-hundred patients admitted to hospital, seven patients in high-income economies and ten in emerging and low-income economies acquire at least one type of HCAI. Currently, almost all pathogenic microorganisms have developed antimicrobial resistance, and few new antimicrobials are being developed and brought to market. The literature search for this narrative review was performed by searching bibliographic databases (including Google Scholar and PubMed) using the search terms: “Strategies,” “Prevention,” and “Healthcare-Associated Infections,” followed by snowballing references cited by critical articles. We found that although hand hygiene is a centuries-old concept, it is still the primary strategy used around the world to prevent HCAIs. It forms one of a bundle of approaches used to clean and maintain a safe hospital environment and to stop the transmission of contagious and infectious microorganisms, including multidrug-resistant microbes. Finally, antibiotic stewardship also has a crucial role in reducing the impact of HCAIs through conserving currently available antimicrobials.
Keywords: prevention, hand hygiene, environmental hygiene, surveillance, antibiotic stewardship
Introduction
Infectious and contagious diseases are of global concern and are the second most common cause of death in flora and fauna.1 Communicable infectious diseases have threatened and challenged humans throughout history, where observers have recorded the advent of epidemics from epizootic diseases. Before communicable diseases were identified, infections were often attributed to various conditions: asters, environmental changes, acts of God, or spiritual reasons.2–4 The notions of transmissible and spreadable diseases emerged first, and those of contagious and infectious diseases emerged much later.5 In Europe between the 5th and the 15th centuries, contagious diseases had a substantial negative impact on public health.5 From 1346–1353, plagues alone killed about 75 to 200 million of the European population, including the Bubonic plague known as the “Black Death.”6–9 Many European cities and towns were deserted as most of their communities died from the plague and other infectious diseases, with, for example, 300–400,000 people in Britain dying from the plague in one single outbreak in 1471.10–13 Regular, but less severe, plague epidemics continued until 1650.6 Before the discovery of antibiotics, average life expectancy was below 50 even for the people in high-income nations because of infectious diseases.14 The dramatic rise in life expectancy in the 20th Century is primarily because of public health measures such as sanitation and the control of these diseases by antibiotics.14 Although it was once thought that infectious diseases could be totally controlled, they are still a substantial public health problem around the world and, because they remain the primary cause of death and infirmity, the costs of treating them are both high and increasing.15–21 At least 30 novel contagious and communicable diseases have appeared in the last 35 years, the majority of which are of zoonotic origin.22 Over recent years, the socioeconomic, environmental, and ecological impact of infectious diseases has increasingly affected the huge mobile global population, which is encountering both new infections (such as COVID-19) and battling the worldwide epidemic of multidrug-resistant existing infectious diseases.23–33 Currently, almost all pathogenic microorganisms have developed some antimicrobial resistance, and few new antimicrobials are being developed and brought to market.
Healthcare-associated infections (HCAIs) are a major source of morbidity and mortality and are the second most prevalent cause of death globally.34–40 The World Health Organization (WHO) and other researchers report that 7% of patients in high-income economies and 10% in emerging and developing economies acquire at least one type of HCAIs, and of these patients, 10% die.34–38 For example, in the US, approximately 1.7 million individuals develop HCAIs annually (a prevalence rate of 4.5%), causing the death of 90,000–99,000 people.37,38 Another study found that 2,609,911 new cases of HCAIs were identified every year in the European Economic Area, causing 2,506,091 DALYs (Disability-Adjusted Life Years) per annum, corresponding to 501 DALYs per 100,000 of the population.36–38 The prevalence rate of HCAIs in Lower- and Middle-Income Counties (LMICs) has been reported as between 5.7–19.1%.38 However, data on HCAIs is patchy, particularly from LMICs because of more inadequate infrastructures (such as data record-keeping) and lack of resources.38,41,42 The WHO conducted a multicenter study estimating HCAIs in Intensive Care Units (ICU), finding that 51% of patients admitted to ICUs developed HCAIs, which prolonged their hospital stay and increased the risk of further infections and other morbidities.43 Infectious diseases cause 15 million deaths per year, of which 95% occur in the emerging economic nations, and these deaths are principally because of acute respiratory infections, diarrheal diseases, measles, AIDS, malaria, and tuberculosis.1 Furthermore, it has been estimated that globally more than 1.4 million patients have HCAIs at any one time in both advanced and emergent countries, causing a substantial financial burden at an individual, community, and public levels.44 A considerable proportion of HCAIs are, however, preventable through proper infection prevention and control (IPC) policy and planning.38 This review presents current updates regarding global strategies to prevent healthcare-associated infections.
Materials and Methods
The literature search for this narrative review was performed by searching bibliographic databases (including Google Scholar, and PubMed) (using free downloads as the research did not have financial support) provided by the Universiti Pertahanan Nasional Malaysia [(UPNM) the National Defence University of Malaysia], Kuala Lumpur, Malaysia and the University of the West Indies, St. Augustine, Trinidad, and Tobago. The search terms used were: “Strategies,” “Prevention,” “Hand Hygiene,” “Environmental Hygiene,” “Surveillance,” “Antibiotic Stewardship,” “Hospital Infections,” and “Healthcare-Associated Infections” followed by snowballing references cited by critical articles. All types of peer-reviewed articles published in English were included. Articles for which the full text was not available and those not written in English were excluded. From the articles retrieved in the first round of search, additional references were identified by a manual search among the cited references. As this is a narrative (not a systematic) review, whilst we have included principally recent papers, those with historical relevance (which are older papers) to the narrative have also been included.
Strategies to Prevent Healthcare-Associated Infections
HCAIs (their prevention and control) are a significant global public health burden about which concerns have been raised from all healthcare stakeholders, including health professionals, patients, and the public.45–48 Their impact has dramatically increased because of the advent of multidrug-resistant pathogenic microorganisms.49–51 Currently, almost all available antimicrobials are resistant52,53 and very few antimicrobials are in the process of being developed for widespread use.54–56 Amongst these pathogens, Klebsiella pneumoniae, which is the most common resistant pathogen, especially in ICU settings, is a significant concern.57,58 The prevention and control of HCAIs is therefore very complicated, and a multi-dimensional approach and strategies are required to address this significant public health concern.36,50,59–63
In the following sections, we discuss the primary ways of addressing the impact of HCAIs as determined in the papers identified in the search and published in well-regarded journals36,45–200 These are the main issues identified in these papers, noting that (depending on the focus of the research and findings) some articles report on a single issue, whereas others report on a number.
Hand hygiene
Maintaining a safe, clean, hygienic hospital environment
Screening and categorizing patients into cohorts
Public health surveillance
Antibiotic stewardship
Following patient safety guidelines
Hand Hygiene
In the mid-19th Century, several researchers in Europe and the US, including Labarraque, Semmelweis, and Wendell Holmes, were working to prevent hospital-acquired, nosocomial HCAIs.60,64–68 Although investigating independently, their observations led them to develop a similar hypothesis, ie, that health care workers (HCWs) carried pathogenic microorganisms from one patient to another on their hands, transmitting pathogens to vulnerable patients who consequently developed infections.69 Over the next hundred years, much evidence accrued that pathogenic microorganisms were often transmitted through the hands of HCWs.65,70–76 Semmelweis is regarded as the first doctor to identify the importance of hand hygiene (HH) in combating contagious infectious diseases.77–80 Florence Nightingale, considered the founder of modern nursing practice,81 wrote that “every nurse ought to be careful to wash her hands very frequently during the day … with soap and soft water”82 subsequent to introducing handwashing and other hygiene practices in the war hospitals during the Crimean War (1853–1856).83–85 HH practices were slow to become widespread; however, until much later, for example, it was only during the foodborne diseases outburst in the US in the 1980s that the Center for Disease Control and Prevention (CDC) recognized HH as a vital technique to stop the widespread infection.74,86–88 Subsequently, the CDC produced and promoted guidelines regarding handwashing practices in hospitals, principally encouraging handwashing with non-antimicrobial soaps both before and after carrying out procedures with the possibility to spread pathogens, especially among high-risk patients, where they could rapidly cause a fatal outcome.86–90 Alcohol-based solutions were suggested only in circumstances where a wash-hand basin was not accessible.86,87 Another study in 1995 encouraged the use of antimicrobial soap or a waterless antiseptic agent for cleaning hands upon leaving the rooms of patients infected with multidrug-resistant microorganisms.90
Ensuring patient safety whilst in hospital and other healthcare facilities is a substantial international public health problem with HCAIs being the most common adverse events in any healthcare system in high- and low-income countries.35,50,91 Each year, hundreds of millions of hospitalized patients are affected with HCAIs, causing substantial morbidity, mortality, and financial losses for individuals, communities, and the public healthcare budget.92,93 HH has been identified as the most important single behavior change that healthcare workers can make for infection control, especially in relation to HCAIs.59,94 For example, the strict practice of HH has been reported to reduce nosocomial infections by between 40% to 70%.95,96 Despite this, rigorous hand washing strategies in hospitals have been observed to be weak, with multiple research studies reporting that globally, in many hospital wards, regular HH by healthcare workers often does not reach over 40%.97–102 Non-compliance with the guiding principles of HH is thus a global public health issue which requires more standardized policies, regular monitoring and surveillance, and additional research.102
The Joint Commission Journal on Quality and Patient Safety reports 24 reasons HCWs cited for their non-compliance with effective HH.103 Many reasons cited stem from a lack of education or training about the need for strict HH, leading to poor practice around ensuring and promoting HH as a key priority and a lack of understanding of how to maintain personal and patient safety. For example, some HCWs thought that wearing sterile gloves meant that HH was unnecessary or that their hospital management’s requirements for HH were too extreme. This view was compounded by many hospitals lacking data and evidence about the impact of HH on infection rates. The high workload was cited as a key factor, with HCWs feeling overworked and burnt out and reporting a perceived lack of time to wash their hands properly or change their gloves between rooms/patients. HCWs also felt that in some clinical situations, such as emergency situations, HH could not be carried out properly, and specific issues were reported relating to gloving and gowning in isolation areas. Logistics and room design were reported as impacting non-compliance, for example, an inappropriate or troublesome location of a hand rub slot machine or basin; broken hand washing facilities, including lack of hand rub or cleanser or that the supplied cleansing agent caused irritation or allergy. The movement of colleagues and relatives between rooms, sharing of equipment, and lack of places to work or put equipment and paperwork were also cited as logistical problems leading to non-compliance with routine hand washing to stop the spread of cross-infection.103
Stemming from this study, the Joint Commission proposed five essential plans for improving HH, using the acronym ‘HANDS’: H = “Habit,” A = “Active feedback,” N = “No One Excused,” D = “Data-driven,” S = “Systems.”104 This plan aims to engender good HH habits in HCWs so that they wash their hands and maintain HH as an automatic behavior “upon entering or leaving a patient care area, as well as before and after patient care.” Active feedback requires health professional leaders to continually remind their staff about HH importance and adherence. Health managers and administrative staff should provide an appraisal of and feedback on HCWs’ HH practice with real-time performance data. Hospital authorities should regularly arrange necessary training programs and must acknowledge and reward hospital staff for achieving the targets. No one excused means that from the most senior to the most junior of all hospital staff, all are similarly accountable and responsible for appropriate HH hygiene. Hospital authorities should recognize HH as of paramount importance in maintaining patient care and safety, and every staff member must follow HH guidelines. Data-driven HH policy requires strict and routine monitoring and recording of compliance, with the data, gathered being analyzed to identify and prioritize areas for development and enhancement. Additionally, research should be continued to develop new ideas to resolve issues in implementing the best HH practice. Systems mean that HH responsiveness is a system-wide effort with rules and regulations regarding HH being applied throughout the health system. Authorities must provide all necessary logistic support to enable all workers to utilize, adhere to, and promote appropriate HH practice. This includes ensuring staff have easy access to HH facilities and using technologies to remind all workers to practice proper HH, emphasizing the benefits not only for patients but also for HCWs themselves.104
One recent systematic review comprising 14 articles concluded that a range of strategic methods is needed to raise HCWs’ compliance regarding HH to an adequate level, but implementing all these might not be possible.105 The interventions suggested included educational programs, monitoring, and feedback, ensuring logistics support, improving access to HH agents, and administrative support.105 Another systematic review concluded that electronic and video monitoring systems could be very effective in enhancing HH practice and preventing or controlling HCAIs.106 However, such methods are costly and may not be affordable for many hospitals, especially in low- and middle-income countries (LMICs). Besides, health professionals might not welcome such round the clock monitoring of their practice, and this could lead to strained professional relationships.106
In 2005, the WHO and World Alliance for Patient Safety started a movement, the First Global Patient Safety Challenge – “Clean Care is Safer Care” – aimed at improving HH in the healthcare system.107 This campaign, known as WHO-5, encourages a multimodal plan comprising five different elements: “system change, training and education, observation and feedback, reminders in the hospital, and a hospital safety climate.”108 Currently, further strategies have been added based on behavioral sciences.108 A systematic review and meta-analysis found that using the WHO-5 approach improved adherence to HH guidance among HCWs.108 This study also suggests that hospital authorities should clearly set out their desired targets, those HCWs who meet the targets should be rewarded with financial incentives, and all HCWs, whatever their position, must be accountable. Such strategies lead to further improvements in HH practice. The study found that the resources and infrastructure required to report on the impact of intervention programs were often insufficient.108 Another systematic review found that interventions to improve HH practice based on “knowledge, awareness, action control, and facilitation are not enough to change” HH practices.109 This research additionally concluded that interventions should be combining diverse, innovative, creative strategies such as “social influence, attitude, self-efficacy, or intention” led to improvements. At present, most policy and planning aimed to ensure better compliance with HH guidance is targeted primarily at the individual and the institutional level, and “group- or team-directed” strategies are hardly ever used.109 This research suggests that the inclusion of team-directed methods to improve HH would be more effective. This review concluded that more comprehensively designed planning is required that acknowledges the many challenges and barriers involved in changing HH practice and that this should address all levels: individual professional, team, and organization.109
Nurses are among the healthcare professionals who spend the most time on patient care and contact.110 A systematic review and meta-analysis evaluating HH practice among nurses comprised six studies: three randomized controlled trials, one controlled before and after study, and two interrupted times series.110 This report reflects the findings from other studies (e.g.,),107 concluding that, whilst individual and collective intervention strategies could improve HH behavior among nurses, more impact was achieved when multimodal plans and policies were implemented.110 This study also suggests setting targets, providing rewards such as bonuses, benefits or financial incentives, and supporting HCWs’ individual accountability regardless of their administrative position.108,110 Another systematic review comprising nineteen articles regarding HH knowledge and compliance among student nurses found a low level of knowledge and practice, with personal and administrative issues often influencing their HH knowledge and practice.111 In summary, noncompliance with HH practice is a global public health issue that promotes more HCAIs, requiring more standardized multi-modal policies and the implementation of more research and monitoring.102
COVID-19 and Hand Hygiene
Handwashing has regained substantial importance in the current global COVID‐19 pandemic.112,113 Whilst a very simple procedure, it is one of the most important protections against the transmission of disease-producing pathogens.95,97,114,115 The CDC advises the public and health professionals to regularly wash their hands with ordinary soap and water for at least 20 seconds as it is considered the first-line preventive strategy of COVID-19 contamination. Alcohol‐based hand sanitizers are recommended when soap and water are not accessible.116,117 Multiple current research studies report that simple handwashing has prevented countless people and healthcare workers around the globe from acquiring COVID-19.118–124
Environmental Hygiene
Maintaining strict environmental hygiene is an essential component of preventing and controlling infections, especially in HCAIs.125,126 Infected and polluted hospital surfaces act as a key reservoir and source of transmission of life-threatening microorganisms, which include Clostridium difficile, antibiotic-resistant organisms such as methicillin-resistant Staphylococcus aureus (MRSA), and vancomycin-resistant enterococci (VRE).127–129 Hospital surfaces, including both porous surfaces, eg, beds, mattresses and linen, and nonporous surfaces, eg, bed rails, door handles, call bells, and light switches are incredibly prone to microbial contamination with high-risk microbes.126,130,131 Maintaining strict hygiene throughout hospitals is, therefore, essential in reducing HCAIs.126,132,133 The aim of such environmental hygiene is to minimize the number of contagious microorganisms that commonly exist on surfaces, as the reduction of pathogens reduces the possibility of the transfer of infectious germs from object to person, thus reducing cross-infection.134,135 Hospital cleaning is a complex and multi-layered process which involves the physical removal (utilizing detergents, chemical disinfectants, and water) of contagious and infectious material from all types of surface, including sputum, urine, blood, secretions, excretions, microorganisms and dust, that can nourish the growth of microorganisms.136–141
The US Center for Disease Control and Prevention (CDC) and the Healthcare Infection Control Practices Advisory Committee endorses that infection prevention and control is the most urgent and vital issue wherever medical care is provided to individuals or communities, irrespective of the type or size of the organization and the healthcare provided.142,143 Appropriate safety measures should include a routine, deep cleaning of all areas of the hospital, both in-patient and out-patient, to minimize communicable transmission infectious diseases.142,143 Antimicrobials used for hospital cleaning comprise both single or multiple components aimed to extinguish or arrest the growth of infectious disease-producing microorganisms, including bacteria, viruses, or fungi. Hospital cleansing products may contain about 275 different constituents and are available in various formulations such as sprays, liquids, concentrated powders, and gases.144 It is crucial for users to understand the level and type of cleaning, its purpose, and limitations, including the various terms, definitions, and classification used (eg, sterilization, disinfection, cleaning) and the categorization of devices and surfaces that require specific measures.145,146 Ethylene oxide gas is used for sterilization, which aims to kill all microorganisms.146–148 Disinfection can eliminate nearly all metabolically active microorganisms except for all microbial spores149 Hydrogen peroxide (7.5%) is a common agent utilized for high-level disinfection.86,87,146 Isopropyl alcohols with a concentration of 70–90% can provide intermediate-level disinfection by the eradication of all vegetative microorganisms with a small number of bacterial spores.146 A quaternary ammonium microbial detergent solution can achieve low-level disinfection by eradicating most metabolically active bacteria, some fungi, and viruses but not metabolically inactive spores.86,146 Cleaning is described as the removal of soil, dust, earth, or biological pollution from an instrument or hospital physical surface through brushing, scrubbing or scraping, using detergent, the surfactant or emulsifying agents that reduce surface tension, and water. Cleaning eliminates many contagious microbes from hospital surfaces, thereby reducing the bacterial load on surfaces. Cleaning is, therefore, the first stage of maintaining hospital hygiene, particularly for surfaces having evident pollution, and helps to safeguard the success of subsequent disinfection procedures.145
Screening and Cohorting Patients
There is increasing political and community concern because multiple approaches have failed or struggled to control the spread of HCAIs, resulting in high morbidity and mortality due to AMR infections developed during hospital stays.150–155 Strategies aimed at minimizing and controlling HCAIs comprise active surveillance cultures (ASCs), contact isolation of patients colonized with epidemiologically significant pathogens, and pre-emptive isolation of high-risk patients.156
It has been suggested that ASCs of all or certain high-risk patients and placing them under contact precautions will help to curb or eliminate the multidrug-resistant organisms (MDROs) that can trigger HCAIs.157 Implementing ASCs is not straightforward, however, raising ethical issues around conflict of interests and confidentiality, practical issues around logistics and bed management, which may lead to isolating or segregating patients when they did not need to be, reallocation of budgets to manage the potentially infected patients, and reduction of healthcare output. ASCs can particularly affect workload in emergency rooms and the ambulance service. Considering these issues, some researchers concluded that implementing ASCs needs to be based on accurate assessments of the impact on public health, and the costs and benefits in relation to existing prevention and control measures.158 A systematic review comprising twenty articles found that although ASCs have been recommended for different hospitals to control the increasing numbers of infections due to multidrug-resistant organisms, their effectiveness and cost-effectiveness are not proven.159 Another prospective study identified that ASCs conducted on patients admitted to ICU did not find the microbes causing bacteriological diseases with the most severe consequences and that bloodstream infections might not, therefore, be associated with ASCs.160 Again, in the ICU setting, a study carried out for four years found that management of MRSA in the ICU does not require ASCs.161
Several countries have successfully reduced the intensities of MRSA infections by executing countrywide controlling strategies such as “search and destroy” (S&D).162 Measures of S&D include the segregation of MRSA-positive patients; anticipatory separation and assessment and evaluation of high-risk cases; screening of patients and staff after an unexpected case of MRSA; assessment of HCWs who are on leave as potential carriers; total decontamination where required and stopping new admissions in areas where more than one carrier found amongst hospitalized patients.163 MDR pathogens such as MRSA, VRE, and multidrug-resistant Gram-negative bacilli (MDR-GNB) are often found in many hospitals and healthcare settings and act as a potential source of MDR outbreaks.164–166 One earlier study reported that approaches to the transmission of HCAIs “include contact isolation, cohorting care, maintaining appropriate staffing ratios, use of active microbiologic surveillance, and decreasing hospital stays.”163 Multiple studies suggested that patient isolation, ASCs, and staff screening can decrease the transmission of MDR pathogens.164,167 And finally, another study found that the anticipatory use of sterile “gloves, with or without a gown,” especially among patients with a high risk of carrying contagious diseases, were very effective in the management of an outbreak of MDRs.168
Surveillance
Public health surveillance is defined as the ongoing systematic collection, analysis, interpretation, and dissemination of data regarding a health-related event for use in public health action to reduce morbidity and mortality and to improve health.169 Surveillance data regarding HCAIs can be used to assess the extent, escalation, and status of infections, to examine, scan and monitor trends of infection rates, inform alert programs, and improve performances, strategy and competence development.170,171 One Scottish study suggested that because the surveillance system in Scotland was not so well-organized, the time taken to first recognize HCAIs was longer than the gold standard.172 This study also found that the time at which HCAIs are recognized can be reduced either by “increasing the number of hospitals participating in surveillance or by optimally selecting which hospitals to include in a surveillance system.”172 Two other Scottish studies echoed this, reporting that a better surveillance system could have prevented a considerable number of Staphylococcus aureus bacteremia (SAB) episodes.173,174 One recent Indian observational prospective study noted a low incidence of HCAIs due to the strict practice of active surveillance in a neurosurgery unit.175 In Germany, the Krankenhaus Infections Surveillance System (KISS) was found to decrease HCAIs more efficiently in comparison to other protocols.176 This system is like that described by the CDC and is structured like the National Nosocomial Surveillance system of the USA.177,178 However, another German study reported that the KISS surveillance system tended to miscalculate the rates of HCAIs.179 Later, yet another German study reported that around 35% of ICUs in Germany have never isolated patients with MRSA as individuals or cohorts.180 Isolation of MDRs infected patients is one of the top priority issues in preventing or controlling an HCAIs epidemic.140,181,182 The timely recognition of the unique variants of HCAIs, especially of MDRs pathogenic microorganisms, is vital, although surveillance strategies are frequently restricted because of financial and practical limitations. Therefore, although surveillance is extensively acknowledged as playing an active part in preventing and controlling HCAIs, there is not enough evidence on how well-organized individual healthcare centered surveillance structures work and how lessons can be applied in low resource settings.183
Antibiotic Stewardship
The term Antimicrobial Stewardship (AS) was first coined by McGowan and Gerding in 1996.184 They highlighted that physicians and other health professionals must see antimicrobials as a very valuable one-time healthcare resource.183 The Society for Healthcare Epidemiology of America defines Antibiotic Stewardship as a set of coordinated strategies to improve the use of antimicrobial medications with the goal of enhancing patient health outcomes, reducing resistance to antibiotics, and decreasing unnecessary costs.185 AS is also described as the optimal selection, dosage, and duration of antimicrobial treatment that results in the best clinical outcome for the treatment or prevention of infection, with minimal toxicity to the patient and minimal impact on subsequent resistance.186 As promotes the prudent and rational use of antimicrobials and helps avoid excessively or in appropriate use.187
Hey, surgeons! It is time to lead and be a champion in preventing and managing surgical infections!188
The World Society of Emergency Surgery (WSES) states that surgeons should take the lead in infection prevention, policy, planning, and implementation. WSES has developed several guidelines for infection prevention, particularly for surgery-related issues, aimed at improving health outcomes in relation to surgical infection-related management.188–191 Scientists at Tufts Medical Center suggest that whilst AMR is increasing globally, the development of new antibiotics has slowed, and therefore, the conservation of antimicrobials is essential.192 The CDC describes the seven core elements of AS as “leadership commitment, accountability, drug expertise, action, tracking, reporting, and education.”193 The three primary objectives of AS are first, to ensure prudent and rational utilization of antimicrobials with precisely targeted doses of the right antibiotic, the “de-escalation to pathogen-directed therapy,” and to deliver antibiotic therapy to an agreed, precise timeframe.192,194 The second objective is the need to halt overall antimicrobial overuse, misuse, and abuse in both community and in-patient hospital facilities, and the third are to halt or slow the expansion of resistance.192
The two most important methods of approach to AS are described, with the most effective initiatives combining both approaches.192 The first method of stewardship is in restraining “prescriptive authority.” Clinicians should be restricted from prescribing specific antimicrobials, and they should be required to seek prior approval for prescribing such antimicrobials.192 The second method bases treatment on laboratory reports of culture sensitivity tests, not just clinical signs and symptoms, to ensure that the antibiotic prescribed (if any) is appropriate. Only then should these antibiotics be made available to physicians with guidance that antibiotic availability and treatment might be adjusted, or even suspended.192 Multiple research studies report that the combination of these approaches reduced antimicrobial prescribing and led to higher satisfaction about the quality of care in both doctors and patients.195,196 A systematic review and meta-analysis recently reported that AS initiatives have specifically decreased the frequency of infectious diseases and “colonization with antibiotic-resistant bacteria and Clostridium difficile infections in hospital inpatients.”197 These reports provide healthcare professionals and policymakers “with evidence for the implementation of antibiotic stewardship interventions to reduce the burden of infections from antibiotic-resistant bacteria.”197 One prospective appraisal of 176 ASP interventions reported a significantly reduced antimicrobial use of 24.3%. It concluded that this had a very positive impact on overall antimicrobial usage, length of therapy, and length of in-hospital stay.198 One quasi-experimental retrospective analysis found that the introduction of ASP was associated with a decrease in antibiotic use as well as overall healthcare costs, with a significant reduction in the incidence of some microbes.199 Another systematic review showed that the implementation of hospital ASPs made significant improvements in infection rates and clinical outcomes as well as financial savings.200 Furthermore, another systematic review and meta-analysis found that ASPs in hospitalized patients in the Asia Pacific region effectively reduced antimicrobial use, and improved patient’s treatment outcomes.201 One additional study reported that improved ASP is essential to stop or limit the emergence of AMR, lengthen the efficacy of available antimicrobials, provide better healthcare outcomes and reduce the healthcare costs of HCAIs for both individuals and communities.202 Another study described three different strategies to control antimicrobial resistance: infection prevention and control, diagnostic stewardship, and antimicrobial stewardship.203
Following Patient Safety Guidelines
Policies, guidelines, and checklists are an essential part of improving patient safety; however, these are often interpreted and implemented differently by individuals, departments, and organizations, based on local influences and practices and often not taken behavioral science into account.204–206 A study investigating the failure of an HCAIs strategy found low levels of physician engagement and compliance with guidelines and policies.207,208 Even in healthcare facilities where policies, guidelines, and checklists were effectively implemented, doctors and other health professionals’ practices were found to degrade after around one year. The reasons given included: too much information being provided; guidelines being too complicated to implement; that guidelines conflicted with other guidelines, and because little evidence was provided to support the guidance.209,210
All healthcare policies and planning around patient safety must embed the prevention and control of HCAIs as a fundamental principle.36,206,211,212 As mentioned earlier, the control and prevention of HCAIs is best achieved through a broad, integrated approach and cooperation between healthcare facilities, public health authorities, health insurances, quality management, and patient safety organizations, educational facilities, the public, and the veterinarian sector.213 Another study regarding the improvement of patient safety identified that the following measures helped to optimize the impact of a program: ensure that the educational program is introduced well and certified; report the program outcomes publicly; carefully design healthcare settings with patient safety in mind; promote an informed and transparent managerial approach; provide clear guidance and role modeling; facilitate collaboration between the healthcare program and government health institution; reduce hospital overcapacity; ensure accountability, and provide financial support.214
Strategies for the Prevention of COVID-19
In order to combat the COVID-19 crisis, health systems leaders around the world have had to adopt rapid multiple lines of attack to appraise critical requirements and address areas of weakness.215 This includes taking a rigorous approach to reduce the rates of COVID-19 infection, hospitalization, morbidity, and mortality.216,217 The appropriate strategy for preparedness to face COVID-19 or any future pandemic must be based on reputable guidelines, protocols, and direct experiences of those working on the front line during the COVID-19 pandemic.216,218 The foundations of an operational COVID-19 preventive vigilance and action plan include: 1) mitigating local transmission; 2) conserving, supporting, and protecting staff; 3) eliminating non-urgent strains on the system and 4) coordinating communication.216 Because hospitals and clinics are considered as core areas for the transmission of COVID-19,219 three principal measures should be implemented to reduce preventable exposure and transmission of COVID-19: 1) restrict both visitors and other non-COVID-19 patients to the health care facility; 2) specific healthcare workers need to work in the COVID-19 zone; and 3) every person must be screened and tested regularly before and after entering the hospital facility.216,219,220
Limitations of the Study
This is a narrative review and not a systematic review, so it is not all-inclusive. Plus, the topic of strategies to prevent HCAIs is extremely broad, and therefore it has not been possible to include all discussions relating to the prevention and control of HCAIs in a single manuscript; therefore, the authors have focused on identifying the most significant features of the current debate.
Conclusions
HCAIs are an increasingly important and severe public health issue about which concerns have been expressed among all stakeholders involved in healthcare, including doctors, nurses, allied health professionals, patients, and the public.45–48,221 Globally, the prevention and control of HCAIs have become an urgent issue, particularly because of the rise of multidrug-resistant pathogenic microorganisms.49–51 This research study found overwhelmingly that hand and environmental hygiene with antibiotic stewardship are the principal measures that minimize HCAIs and improve treatment outcomes.
Recommendations
Determined actions are required to address the burden of healthcare-associated infections worldwide and improve patient safety. Hand hygiene and the prudent use of antimicrobials are the key strategies in preventing HCAIs. Hand hygiene is the leading measure for preventing the spread of antimicrobial resistance and reducing HCAIs. Hand hygiene can prevent a significant number of HCAIs since healthcare workers’ hands are the most common vehicle for the transmission of healthcare-associated pathogens from patient to patient and within the healthcare environment. Available evidence highlights the fact that multimodal intervention strategies lead to improved hand hygiene and a reduction in HCAIs. The introduction of alcohol-based hand rubs and continuous educational programs are key factors to overcome infrastructure barriers and to build robust knowledge improvement. Antimicrobial stewardship is also vital to optimize the use of antimicrobials to prevent the development of resistance and improve patient outcomes. Coordinated strategies are required between all actors in the system to help prevent antimicrobial resistance.
Key Findings
HCAIs are the leading cause of morbidity and mortality worldwide, and most of them are preventable.
Hand hygiene is the most effective, simplest, and cheapest measure to prevent HCAIs, but compliance with hand hygiene remains low amongst HCWs.
In order to improve hand hygiene compliance among HCWs, intervention strategies should be implemented, and standardized measures for monitoring should be put in place.
Ensuring adequate hospital environmental hygiene is essential for reducing the threat of HCAIs by minimizing the number of contagious microorganisms existing on surfaces and reducing cross-infection.
The cost-effectiveness of active surveillance cultures (ASCs) is not proven. Contact isolation of patients colonized or infected by pathogens can decrease the transmission of drug-resistant organisms.
Active and passive surveillance programs should be implemented to assess and monitor the extent and trends of HCAIs, to develop precautionary programs, and improve performance, strategy, and competence development.
The implementation of Antibiotic Stewardship Programs is vital to enhance patient health outcomes, reduce resistance to antibiotics, and decrease unnecessary costs.
Guidelines are an important tool to improve patient safety, and efforts should be put into action to improve HCWs adherence to them.
Extensive integrated approaches involving cooperation between public health authorities and HCWs are needed to maximize patient safety by preventing HCAIs.
Acknowledgments
The Principal author is very grateful to the library of the Universiti Pertahanan Nasional Malaysia (National Defence University of Malaysia) for its support in providing necessary manuscripts, which are not free download.
Funding Statement
No funding was received to produce this paper.
Author Contributions
All authors made a significant contribution to the work reported, whether that is in the conception, study design, execution, acquisition of data, analysis, and interpretation, or in all these areas; took part in drafting, revising or critically reviewing the article; gave final approval of the version to be published; have agreed on the journal to which the article has been submitted; and agree to be accountable for all aspects of the work.
Disclosure
The authors have no conflict of interests to declare.
References
- 1.Raka L, Mulliqi-Osmani G. Infection control in developing world; 2012. Available from: https://pdfs.semanticscholar.org/8703/b74aa2341cd2278202607367301764387a86.pdf. Accessed February10, 2019.
- 2.Institute of Medicine (US) Committee for the Study of the Future of Public Health. The future of public health. Washington (DC): National Academies Press (US); 1988. 3. A History of the Public Health System Available from: https://www.ncbi.nlm.nih.gov/books/NBK218224/. Accessed August20, 2020. [PubMed] [Google Scholar]
- 3.Lindahl JF, Grace D. The consequences of human actions on risks for infectious diseases: a review. Infect Ecol Epidemiol. 2015;5:30048. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 4.Cheng Y, Wang J, Yang X. On the global stability of a generalized cholera epidemiological model. J Biol Dyn. 2012;6:1088–1104. doi: 10.1080/17513758.2012.728635 [DOI] [PubMed] [Google Scholar]
- 5.Bazin H. A brief history of the prevention of infectious diseases by immunizations. Comp Immunol Microbiol Infect Dis. 2003;26(5–6):293–308. doi: 10.1016/S0147-9571(03)00016-X [DOI] [PubMed] [Google Scholar]
- 6.Smith PW, Watkins K, Hewlett A. Infection control through the ages. Am J Infect Control. 2012;40(1):35–42. doi: 10.1016/j.ajic.2011.02.019 [DOI] [PubMed] [Google Scholar]
- 7.McNeill WH. Plagues and Peoples. Garden City [NY]: Anchor Press; 1976. [Google Scholar]
- 8.US-Wikipedia om pesten. Available from: http://www.b-informatik.dk/pesten/US-Wikipedia_pesten.pdf. Accessed February8, 2019.
- 9.Benedictow OJ. The black death: the greatest catastrophe ever. Hist Today. 2005;55(3):42–49. [Google Scholar]
- 10.Alfani G, Murphy TE. Plague and lethal epidemics in the pre-industrial world. J Econ Hist. 2017;77(1):314–343. doi: 10.1017/S0022050717000092 [DOI] [Google Scholar]
- 11.Alfani G. Plague in seventeenth-century Europe and the decline of Italy: an epidemiological hypothesis. Eur Rev Econ Hist. 2013;17(4):408–430. doi: 10.1093/ereh/het013 [DOI] [Google Scholar]
- 12.Bianucci R, Benedictow OJ, Fornaciari G, Giuffra V. Quinto Tiberio Angelerio and new measures for controlling plague in 16th-century Alghero, Sardinia. Emerg Infect Dis. 2013;19(9):1478–1483. doi: 10.3201/eid1909.120311 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 13.Gottfried RS. The Black Death: Natural and Human Disaster in Medieval Europe. London: Hale: The Free Press, A Division of Simon & Schuster, Inc., 1230 Avenue of the Americas New York, NY 10020; 1985. [Google Scholar]
- 14.Adedeji WA. The treasure called antibiotics. Ann Ib Postgrad Med. 2016;14(2):56‐57. [PMC free article] [PubMed] [Google Scholar]
- 15.Frieden TR. Six components necessary for effective public health program implementation. Am J Public Health. 2014;104(1):17–22. doi: 10.2105/AJPH.2013.301608 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 16.Institute of Medicine (US) Committee on Assuring the Health of the Public in the 21st Century. The future of the public’s health in the 21st century. Washington (DC): National Academies Press (US); 2002. 5, The Health Care Delivery System Available from: https://www.ncbi.nlm.nih.gov/books/NBK221227/. Accessed February8, 2019. [PubMed] [Google Scholar]
- 17.Dieleman JL, Baral R, Birger M, et al. US spending on personal health care and public health, 1996–2013. JAMA. 2016;316(24):2627–2646. doi: 10.1001/jama.2016.16885 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 18.Holmes KK, Bertozzi S, Bloom BR, et al. Major infectious diseases: key messages from disease control priorities, third edition In: Holmes KK, Bertozzi S, Bloom BR, et al. editors. Major Infectious Diseases. 3rd Washington (DC): The International Bank for Reconstruction and Development/The World Bank; 2017:1. [PubMed] [Google Scholar]
- 19.Dye C. After 2015: infectious diseases in a new era of health and development. Philos Trans R Soc Lond B Biol Sci. 2014;369(1645):20130426. doi: 10.1098/rstb.2013.0426 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 20.Miller M, Barrett S, Henderson DA. Control and eradication editors, Jamison DT, Breman JG, Measham AR. Disease Control Priorities in Developing Countries. 2nd Washington (DC): The International Bank for Reconstruction and Development/The World Bank; 2006: 62. [PubMed] [Google Scholar]
- 21.Russell CD. Eradicating infectious disease: can we, and should we? Front Immunol. 2011;2:53. doi: 10.3389/fimmu.2011.00053 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 22.Nii-Trebi NI. Emerging and neglected infectious diseases: insights, advances, and challenges. Biomed Res Int. 2017;2017:5245021. doi: 10.1155/2017/5245021 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 23.Lederberg J. Summary and assessment In: Davis JR, Lederberg J, editors. Institute of Medicine (US) Forum on Emerging Infections. Washington (DC): National Academies Press (US);2000. [PubMed] [Google Scholar]
- 24.Quinn SC, Kumar S. Health inequalities and infectious disease epidemics: a challenge for global health security. Biosecur Bioterror. 2014;12(5):263–273. doi: 10.1089/bsp.2014.0032 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 25.World Health Organization. Combating emerging infectious diseases in the South-East Asia region. SEA-CD-139. Distribution: general. Regional Office for South-East Asia; New Delhi; 2005. Available from: http://www.searo.who.int/entity/emerging_diseases/documents/b0005.pdf. Accessed February10, 2019. [Google Scholar]
- 26.World Health Organization. Managing epidemics: key facts about major deadly diseases. Geneva: World Health Organization; 2018. License: CC BY-NC-SA 3.0 IGO Available from https://www.who.int/emergencies/diseases/managing-epidemics-interactive.pdf. Accessed February10, 2019. [Google Scholar]
- 27.Yi Y, Lagniton PNP, Ye S, Li E, Xu RH. COVID-19: what has been learned and to be learned about the novel coronavirus disease. Int J Biol Sci. 2020;16(10):1753–1766. doi: 10.7150/ijbs.45134 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 28.Ahmad T, Haroon DK, Dhama K, et al. Biosafety and biosecurity approaches to restrain/contain and counter SARS-CoV-2/COVID-19 pandemic: a rapid-review. Turk J Biol. 2020;44(3):132–145. doi: 10.3906/biy-2005-63 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 29.Haque M. The COVID-19 pandemic - a global public health crisis: a brief overview regarding pharmacological interventions. Pesqui Bras Odontopediatria Clín Integr. 2020;20(supp1):e0146. doi: 10.1590/pboci.2020.137 [DOI] [Google Scholar]
- 30.Haque M. Handwashing in averting infectious diseases: relevance to COVID-19. J Popul Ther Clin Pharmacol. 2020;27(SPt 1):e37–e52. [DOI] [PubMed] [Google Scholar]
- 31.Haque M, Islam S, Iqbal S, et al. Availability and price changes of potential medicines and equipment for the prevention and treatment of COVID-19 among pharmacy and drug stores in Bangladesh; findings and implications. Bang J Med Sci. 2020;19(S):S36–S50. [Google Scholar]
- 32.Haque M. Combating COVID-19: a coordinated efforts of healthcare providers and policy makers with global participation are needed to achieve the desired goals. Bang J Med Sci. 2020;19(S):S01–S05. [Google Scholar]
- 33.Habas K, Nganwuchu C, Shahzad F, et al. Resolution of coronavirus disease 2019 (COVID-19). Expert Rev Anti Infect Ther. 2020. doi: 10.1080/14787210.2020.1797487 [DOI] [PubMed] [Google Scholar]
- 34.Danasekaran R, Mani G, Annadurai K. Prevention of healthcare-associated infections: protecting patients, saving lives. Int J Commun Med Public Health. 2014;1(1):67–68. doi: 10.5455/2394-6040.ijcmph20141114 [DOI] [Google Scholar]
- 35.Khan HA, Baig FK, Mehboob R. Nosocomial infections: epidemiology, prevention, control, and surveillance. Asian Pac J Trop Biomed. 2017;7(5):478. doi: 10.1016/j.apjtb.2017.01.019 [DOI] [Google Scholar]
- 36.Haque M, Sartelli M, McKimm J, Abu Bakar M. Healthcare-associated infections - an overview. Infect Drug Resist. 2018;11:2321–2333. doi: 10.2147/IDR.S177247 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 37.Klevens RM, Edwards JR, Richards CL, et al. Estimating healthcare-associated infections in US hospitals, 2002. Public Health Rep. 2007;122:160–166. doi: 10.1177/003335490712200205 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 38.Guidelines on core components of infection prevention and control programs at the national and acute health care facility level. Geneva: World Health Organization; 2016. 6. The burden of healthcare-associated infection Available from: https://www.ncbi.nlm.nih.gov/books/NBK401766/. Accessed February10, 2019. [PubMed] [Google Scholar]
- 39.Ripabelli G, Salzo A, Mariano A, Sammarco ML, Tamburro M; Collaborative Group for HAIs Point Prevalence Surveys in Molise Region. Healthcare-associated infections point prevalence survey and antimicrobials use in acute care hospitals (PPS 2016–2017) and long-term care facilities (HALT-3): a comprehensive report of the first experience in Molise Region, Central Italy, and targeted intervention strategies. J Infect Public Health. 2019;12(4):509–515. [DOI] [PubMed] [Google Scholar]
- 40.Ricchizzi E, Latour K, Kärki T, et al. Antimicrobial use in European long-term care facilities: results from the third point prevalence survey of healthcare-associated infections and antimicrobial use, 2016 to 2017. Euro Surveill. 2018;23(46):1800394. doi: 10.2807/1560-7917.ES.2018.23.46.1800394 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 41.Cassini A, Plachouras D, Eckmanns T, et al. Burden of six healthcare-associated infections on European population health: estimating incidence-based disability-adjusted life years through a population prevalence-based modelling study. PLoS Med. 2016;13(10):e1002150. doi: 10.1371/journal.pmed.1002150 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 42.Haque M, McKimm J, Godman B, Abu Bakar M, Sartelli M. Initiatives to reduce postoperative surgical site infections of the head and neck cancer surgery with a special emphasis on developing countries. Expert Rev Anticancer Ther. 2019;19(1):81–92. doi: 10.1080/14737140.2019.1544497 [DOI] [PubMed] [Google Scholar]
- 43.World Health Organization. The burden of health care-associated infection worldwide. A summary. Patient safety. A world alliance for safer health care. Saves lives. Clean your hands; 2010. Available from: https://www.who.int/gpsc/country_work/summary_20100430_en.pdf. Accessed February10, 2019.
- 44.World Alliance for Patient Safety. The global patient safety challenge, 2005–2006. Clean care is safer care. WHO Press, World Health Organization, 20 Avenue Appia, 1211 Geneva 27, Switzerland, Geneva; 2005. Available from: https://www.who.int/patientsafety/events/05/GPSC_Launch_ENGLISH_FINAL.pdf. Accessed February10, 2019. [Google Scholar]
- 45.Esfandiari A, Salari H, Rashidian A, Masoumi Asl H, Rahimi Foroushani A, Akbari Sari A. Eliminating healthcare-associated infections in Iran: a qualitative study to explore stakeholders’ views. Int J Health Policy Manag. 2017;7(1):27–34. doi: 10.15171/ijhpm.2017.34 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 46.Esfandiari A, Rashidian A, Masoumi Asl H, Rahimi Foroushani A, Salari H, Akbari Sari A. Prevention and control of healthcare-associated infections in Iran: a qualitative study to explore challenges and barriers. Am J Infect Control. 2016;44(10):1149–1153. doi: 10.1016/j.ajic.2016.03.049 [DOI] [PubMed] [Google Scholar]
- 47.Allegranzi B, Bagheri Nejad S, Combescure C, et al. Burden of endemic health-care-associated infection in developing countries: systematic review and meta-analysis. Lancet. 2011;377(9761):228–241. doi: 10.1016/S0140-6736(10)61458-4 [DOI] [PubMed] [Google Scholar]
- 48.Martin M, Zingg W, Hansen S, et al.; PROHIBIT study group. Public reporting of healthcare-associated infection data in Europe. What are the views of infection prevention opinion leaders? J Hosp Infect. 2013;83(2):94–98. doi: 10.1016/j.jhin.2012.10.010 [DOI] [PubMed] [Google Scholar]
- 49.European Centre for Disease Prevention and Control. An agency of the European Union. Antimicrobial resistance and healthcare-associated infections programme. Available from: https://ecdc.europa.eu/en/about-uswho-we-aredisease-programmes/antimicrobial-resistance-and-healthcare-associated-infections. Accessed February12, 2019.
- 50.Revelas A. Healthcare-associated infections: a public health problem. Niger Med J. 2012;53(2):59–64. doi: 10.4103/0300-1652.103543 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 51.Kanerva M, Ollgren J, Hakanen AJ, Lyytikäinen O. Estimating the burden of healthcare-associated infections caused by selected multidrug-resistant bacteria Finland, 2010. Antimicrob Resist Infect Control. 2012;1(1):33. doi: 10.1186/2047-2994-1-33 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 52.Ventola CL. The antibiotic resistance crisis: part 1: causes and threats. Pharm Ther. 2015;40(4):277–283. [PMC free article] [PubMed] [Google Scholar]
- 53.Prestinaci F, Pezzotti P, Pantosti A. Antimicrobial resistance: a global, multifaceted phenomenon. Pathog Glob Health. 2015;109(7):309–318. doi: 10.1179/2047773215Y.0000000030 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 54.United Nations. Not enough new antibiotics in the pipeline, UN report warns. Sustainable Development, GOALS; 2017. Available from: https://www.un.org/sustainabledevelopment/blog/2017/09/not-enough-new-antibiotics-in-the-pipeline-un-report-warns/. Accessed February12, 2019.
- 55.Sukkar E Why are there so few antibiotics in the research and development pipeline? The pharmaceutical journal. A Royal Pharmaceutical Society Publication; 2013. Available from: https://www.pharmaceutical-journal.com/news-and-analysis/features/why-are-there-so-few-antibiotics-in-the-research-and-development-pipeline/11130209.article?firstPass=false. Accessed February12, 2019. [Google Scholar]
- 56.Paton J, Kresge N, GlaxoSmithKline. Big Pharma is leaving the field of antibiotic research in droves; 2018. Available from: https://www.businesslive.co.za/bd/companies/2018-07-13-big-pharma-is-leaving-the-field-of-antibiotic-research-in-droves/. Accessed February12, 2019.
- 57.Ripabelli G, Tamburro M, Guerrizio G, et al. Tracking multidrug-resistant Klebsiella pneumoniae from an Italian hospital: molecular epidemiology and surveillance by PFGE, RAPD, and PCR-based resistance genes prevalence. Curr Microbiol. 2018;75(8):977–987. doi: 10.1007/s00284-018-1475-3 [DOI] [PubMed] [Google Scholar]
- 58.Di Tella D, Tamburro M, Guerrizio G, Fanelli I, Sammarco ML, Ripabelli G. Molecular epidemiological insights into colistin-resistant and carbapenemases-producing clinical Klebsiella pneumoniae isolates. Infect Drug Resist. 2019;12:3783–3795. doi: 10.2147/IDR.S226416 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 59.WHO Guidelines on hand hygiene in health care: first global patient safety challenge clean care is safer care. Geneva: World Health Organization; 2009. The burden of healthcare-associated infection Available from: https://www.ncbi.nlm.nih.gov/books/NBK144030/. Accessed February14, 2019. [PubMed] [Google Scholar]
- 60.McLaws ML. The relationship between hand hygiene and healthcare-associated infection: it’s complicated. Infect Drug Resist. 2015;8:7–18. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 61.Birgand G, Castro-Sánchez E, Hansen S, et al. Comparison of governance approaches for the control of antimicrobial resistance: analysis of three European countries. Antimicrob Resist Infect Control. 2018;7:28. doi: 10.1186/s13756-018-0321-5 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 62.Mathur P. Prevention of healthcare-associated infections in low- and middle-income countries: the ‘bundle approach’. Indian J Med Microbiol. 2018;36(2):155–162. doi: 10.4103/ijmm.IJMM_18_152 [DOI] [PubMed] [Google Scholar]
- 63.Rosenthal VD, Ramachandran B, Villamil-Gómez W, et al. Impact of a multidimensional infection control strategy on central line-associated bloodstream infection rates in pediatric intensive care units of five developing countries: findings of the International Nosocomial Infection Control Consortium (INICC). Infection. 2012;40(4):415–423. doi: 10.1007/s15010-012-0246-5 [DOI] [PubMed] [Google Scholar]
- 64.WHO Guidelines on hand hygiene in health care: first global patient safety challenge clean care is safer care. Geneva: World Health Organization; 2009. 4. Historical perspective on hand hygiene in health care Available from: https://www.ncbi.nlm.nih.gov/books/NBK144018/. Accessed February14, 2019. [PubMed] [Google Scholar]
- 65.Mathur P. Hand hygiene: back to the basics of infection control. Indian J Med Res. 2011;134(5):611–620. doi: 10.4103/0971-5916.90985 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 66.Labarraque AG. Instructions and Observations Regarding the Use of the Chlorides of Soda and Lime. Porter J, Transed [French]. New Haven, CT: Baldwin and Treadway; 1829. [Google Scholar]
- 67.Semmelweis I. Etiology, Concept, and Prophylaxis of Childbed Fever. 1st Carter KC, Madison WI. The University of Wisconsin Press; 1983. [Google Scholar]
- 68.Lane HJ, Blum N, Fee E. Oliver Wendell Holmes (1809–1894) and Ignaz Philipp Semmelweis (1818–1865): preventing the transmission of puerperal fever. Am J Public Health. 2010;100(6):1008–1009. doi: 10.2105/AJPH.2009.185363 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 69.WHO Guidelines on hand hygiene in health care: first global patient safety challenge clean care is safer care. Geneva: World Health Organization; 2009. 7, Transmission of pathogens by hands Available from: https://www.ncbi.nlm.nih.gov/books/NBK144014/. Accessed February14, 2019. [PubMed] [Google Scholar]
- 70.Lowy EJL, Lilly HA, Bull JP. Disinfection of hands: removal of transient organism. Br Med J. 1964;2(5403):230–233. doi: 10.1136/bmj.2.5403.230 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 71.Jumaa PA. Hand hygiene: simple and complex. Int J Infect Dis. 2005;9(1):3–14. doi: 10.1016/j.ijid.2004.05.005 [DOI] [PubMed] [Google Scholar]
- 72.Sanford MD, Widmer AF, Bale MJ, Jones RN, Wenzel RP. Efficient detection and long-term persistence of the carriage of Methicillin-resistant Staphylococcus aureus. Clin Infect Dis. 1994;19:1123–1128. doi: 10.1093/clinids/19.6.1123 [DOI] [PubMed] [Google Scholar]
- 73.Larson EL, Cronquist AB, Whittier S, Lai L, Lyle CT, Della Latta P. Differences in skin flora between inpatients and chronically ill patients. Heart Lung. 2000;29:298–305. doi: 10.1067/mhl.2000.108324 [DOI] [PubMed] [Google Scholar]
- 74.Rosenthal VD, Guzman S, Safdar N. Reduction in nosocomial infection with improved hand hygiene in intensive care units of a tertiary care hospital in Argentina. Am J Infect Control. 2005;33(7):392–397. doi: 10.1016/j.ajic.2004.08.009 [DOI] [PubMed] [Google Scholar]
- 75.Rigby R, Pegram A, Woodward S. Hand decontamination in clinical practice: a review of the evidence. Br J Nurs. 2017;26(8):448–451. doi: 10.12968/bjon.2017.26.8.448 [DOI] [PubMed] [Google Scholar]
- 76.Di Muzio M, Cammilletti V, Petrelli E, Di Simone E. Hand hygiene in preventing nosocomial infections: a nursing research. Ann Ig. 2015;27(2):485–491. [DOI] [PubMed] [Google Scholar]
- 77.Markel H. Wash your hands! Milbank Q. 2015;93(3):447–454. doi: 10.1111/1468-0009.12128 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 78.Weiß J. Ignaz Semmelweis: a great discovery and even greater ignorance. Z Gastroenterol. 2013;51(5):424. [DOI] [PubMed] [Google Scholar]
- 79.Best M, Neuhauser D. Ignaz Semmelweis, and the birth of infection control. Qual Saf Health Care. 2004;13(3):233–234. doi: 10.1136/qshc.2004.010918 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 80.Owen H. Unexpected consequences of simulator use in medical education: a cautionary tale. Simul Healthc. 2014;9(3):149–152. doi: 10.1097/SIH.0000000000000014 [DOI] [PubMed] [Google Scholar]
- 81.Karimi H, Alavi NM. Florence Nightingale: the mother of nursing. Nurs Midwifery Stud. 2015;4(2):e29475. doi: 10.17795/nmsjournal29475 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 82.Nightingale F. Notes on Nursing. Chapter 11. Personal Cleanliness. 1st ed. Germany: Reproduction of the Original, Outlook Verlag, GmBH, Deutschland, Frankfurt am Main; 2018. [Google Scholar]
- 83.Fee E, Garofalo ME. Florence Nightingale and the crimean war. Am J Public Health. 2010;100(9):1591. doi: 10.2105/AJPH.2009.188607 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 84.Sheingold BH, Hahn JA. The history of healthcare quality: the first 100 years 1860–1960. Int J Afr Nurs Sci. 2014;1:18–22. [Google Scholar]
- 85.The Global Handwashing Partnership (GHP). History; 2017. Available from: https://globalhandwashing.org/about-handwashing/history-of-handwashing/. Accessed February21, 2019.
- 86.Garner JS, Favero MS. CDC guidelines for the prevention and control of nosocomial infections. Guideline for handwashing and hospital environmental control, 1985. Supersedes guideline for hospital environmental control published in 1981. Am J Infect Control. 1986;14(3):110–129. doi: 10.1016/0196-6553(86)90019-2 [DOI] [PubMed] [Google Scholar]
- 87.Garner JS, Favero MS. CDC guideline for handwashing and hospital environmental control, 1985. Infect Control. 1986;7:231–243. [DOI] [PubMed] [Google Scholar]
- 88.Hospital Infection Control Practices Advisory Committee (HICPAC). Recommendations for preventing the spread of vancomycin resistance. Infect Control Hosp Epidemiol. 1995;16:105–113. doi: 10.2307/30140952 [DOI] [PubMed] [Google Scholar]
- 89.Toney-Butler TJ, Carver N. Hand Washing (Hand Hygiene) In: StatPearls [Internet]. Treasure Island (FL): StatPearls Publishing; 2018. Available from: https://www.ncbi.nlm.nih.gov/books/NBK470254/ Accessed February 21, 2019. [Google Scholar]
- 90.Boyce JM, Pittet D. Healthcare infection control practices advisory committee; HICPAC/SHEA/APIC/IDSA hand hygiene task force. Guideline for hand hygiene in health-care settings. Recommendations of the healthcare infection control practices advisory committee and the HICPAC/SHEA/APIC/IDSA hand hygiene task force. Society for healthcare epidemiology of America/Association for professionals in infection control/infectious diseases society of America. MMWR Recomm Rep. 2002;51(RR–16):1–45, quiz CE1–4. [PubMed] [Google Scholar]
- 91.Pittet D, Donaldson L. Challenging the world: patient safety and healthcare-associated infection. Int J Qual Health Care. 2006;18(1):4–8. doi: 10.1093/intqhc/mzi093 [DOI] [PubMed] [Google Scholar]
- 92.Stone PW. Economic burden of healthcare-associated infections: an American perspective. Expert Rev Pharmacoecon Outcomes Res. 2009;9(5):417–422. doi: 10.1586/erp.09.53 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 93.Maliwan H. Developing and Evaluating Effective Interventions to Reduce Healthcare-Associated Infection in A Resource-Limited Hospital in Thailand. Ph.D. Thesis Mahidol Oxford Tropical Medicine Research Unit. The Open University; 2018. Available from: https://oro.open.ac.uk/55283/7/Thesis_Maliwan%20Hongsuwan%2C%20B6976542.pdf. Accessed February21, 2019. [Google Scholar]
- 94.Pittet D, Allegranzi B, Sax H, et al.; WHO Global Patient Safety Challenge, World Alliance for Patient Safety. Evidence-based model for hand transmission during patient care and the role of improved practices. Lancet Infect Dis. 2006;6(10):641–652. doi: 10.1016/S1473-3099(06)70600-4 [DOI] [PubMed] [Google Scholar]
- 95.Kampf G, Löffler H, Gastmeier P. Hand hygiene for the prevention of nosocomial infections. Dtsch Arztebl Int. 2009;106(40):649–655. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 96.Gawande A. On Washing Hands. Notes of a surgeon. N Engl J Med. 2004;350(13):1283–1286. doi: 10.1056/NEJMp048025 [DOI] [PubMed] [Google Scholar]
- 97.Trampuz A, Widmer AF. Hand hygiene: a frequently missed lifesaving opportunity during patient care. Mayo Clin Proc. 2004;79(1):109–116. doi: 10.4065/79.1.109 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 98.Geberemariyam BS, Donka GM, Wordofa B. Assessment of knowledge and practices of healthcare workers towards infection prevention and associated factors in healthcare facilities of West Arsi District, Southeast Ethiopia: a facility-based cross-sectional study. Arch Public Health. 2018;76:69. doi: 10.1186/s13690-018-0314-0 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 99.Schiffers H, Zaatreh S, Mittelmeier W, Bader R. Potential infection control risks associated with roaming healthcare industry representatives. J Infect Prev. 2015;17(1):22–28. doi: 10.1177/1757177415605658 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 100.Longembe EB, Kitronza PL. Compliance with hand-hygiene practice in the General Reference Hospitals of the city of Kisangani, Democratic Republic of the Congo [Observance de l’hygiène des mains dans les hôpitaux généraux de référence de la ville de Kisangani en République Démocratique du Congo]. Pan Afr Med J. 2020;35:57. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 101.Bukhari SZ, Hussain WM, Banjar A, Almaimani WH, Karima TM, Fatani MI. Hand hygiene compliance rate among healthcare professionals. Saudi Med J. 2011;32(5):515–519. [PubMed] [Google Scholar]
- 102.Erasmus V, Daha TJ, Brug H, et al. Systematic review of studies on compliance with hand hygiene guidelines in-hospital care. Infect Control Hosp Epidemiol. 2010;31(3):283–294. doi: 10.1086/650451 [DOI] [PubMed] [Google Scholar]
- 103.Chassin MR, Mayer C, Nether K. Improving hand hygiene at eight hospitals in the United States by targeting specific causes of noncompliance. Jt Comm J Qual Patient Saf. 2015;41(1):4–12. [DOI] [PubMed] [Google Scholar]
- 104.Becker’s Clinical Leadership & Infection Control. 5 strategies to improve hand hygiene adherence; 2014. Available from: https://www.beckershospitalreview.com/quality/5-strategies-to-improve-hand-hygiene-adherence.html. Accessed February23, 2019.]
- 105.Alshehari AA, Park S, Rashid H. Strategies to improve hand hygiene compliance among healthcare workers in adult intensive care units: a mini systematic review. J Hosp Infect. 2018;100(2):152–158. doi: 10.1016/j.jhin.2018.03.013 [DOI] [PubMed] [Google Scholar]
- 106.Srigley JA, Lightfoot D, Fernie G, Gardam M, Muller MP. Hand hygiene monitoring technology: protocol for a systematic review. Syst Rev. 2013;2:101. doi: 10.1186/2046-4053-2-101 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 107.World Health Organizations. Patient safety. A world alliance for safer health care. WHO guidelines on hand hygiene in health care (First global patient safety challenge clean care is safer care). WHO Press, World Health Organization, 20 Avenue Appia, 1211 Geneva 27, Switzerland; 2009. Available from: https://apps.who.int/iris/bitstream/handle/10665/44102/9789241597906_eng.pdf;jsessionid=B052A1AA8F486348C9B126B729F534E8?sequence=1. Accessed February24, 2019. [PubMed] [Google Scholar]
- 108.Luangasanatip N, Hongsuwan M, Limmathurotsakul D, et al. Comparative efficacy of interventions to promote hand hygiene in hospital: systematic review and network meta-analysis. BMJ. 2015;351:h3728. doi: 10.1136/bmj.h3728 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 109.Huis A, van Achterberg T, de Bruin M, Grol R, Schoonhoven L, Hulscher M. A systematic review of hand hygiene improvement strategies: a behavioral approach. Implement Sci. 2012;7:92. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 110.Doronina O, Jones D, Martello M, Biron A, Lavoie-Tremblay M, Systematic A. Review on the effectiveness of interventions to improve hand hygiene compliance of nurses in the hospital setting. J Nurs Scholarsh. 2017;49(2):143–152. doi: 10.1111/jnu.12274 [DOI] [PubMed] [Google Scholar]
- 111.Labrague LJ, McEnroe-Petitte DM, van de Mortel T, Nasirudeen AMA. A systematic review on hand hygiene knowledge and compliance in student nurses. Int Nurs Rev. 2018;65(3):336–348. doi: 10.1111/inr.12410 [DOI] [PubMed] [Google Scholar]
- 112.Alzyood M, Jackson D, Aveyard H, Brooke J. COVID-19 reinforces the importance of handwashing. J Clin Nurs. 2020;29(15–16):2760–2761. doi: 10.1111/jocn.15313 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 113.Cavanagh G, Wambier CG. Rational hand hygiene during the coronavirus 2019 (COVID-19) pandemic. J Am Acad Dermatol. 2020;82(6):e211. doi: 10.1016/j.jaad.2020.03.090 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 114.Boyce JM. New insights for improving hand hygiene practices. Infect Control Hosp Epidemiol. 2004;25(3):187–188. doi: 10.1086/502374 [DOI] [PubMed] [Google Scholar]
- 115.Sahud AG, Bhanot N. The art and science of influencing hand hygiene. Infect Control Hosp Epidemiol. 2009;30(8):810–811. doi: 10.1086/599089 [DOI] [PubMed] [Google Scholar]
- 116.Center for Disease Control and Prevention. Cleaning and disinfection for households interim recommendations for U.S. Households with suspected or confirmed Coronavirus disease 2019 (COVID-19); 2020. Available from: https://www.cdc.gov/coronavirus/2019-ncov/prevent-getting-sick/cleaning-disinfection.html. Accessed August21, 2020.
- 117.Center for Disease Control and Prevention. How to protect yourself & others; 2020. Available from: https://www.cdc.gov/coronavirus/2019-ncov/prevent-getting-sick/prevention.html. Accessed August21, 2020.
- 118.Singh PK Promote hand hygiene to save lives and combat COVID-19. WHO Regional Director for South-East Asia, SEARO; 2020. Available from: https://www.who.int/southeastasia/news/detail/04-05-2020-promote-hand-hygiene-to-save-lives-and-combat-covid-19. Accessed August21, 2020. [Google Scholar]
- 119.World Health Organization. Save lives: clean your hands in the context of COVID-19; 2020. Available from: https://www.who.int/infection-prevention/campaigns/clean-hands/WHO_HH-Community-Campaign_finalv3.pdf?ua=1. Accessed August21, 2020.
- 120.Hillier MD. Using effective hand hygiene practice to prevent and control infection. Nurs Stand. 2020;35(5):45–50. doi: 10.7748/ns.2020.e11552 [DOI] [PubMed] [Google Scholar]
- 121.De Vitis R, Passiatore M, Perna A, Proietti L, Taccardo G. COVID-19 contagion and contamination through hands of trauma patients: what risks and what precautions? J Hosp Infect. 2020;105(2):354–355. doi: 10.1016/j.jhin.2020.03.037 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 122.Cawthorne KR, Cooke RPD. Innovative technologies for hand hygiene monitoring are urgently needed in the fight against COVID-19. J Hosp Infect. 2020;105(2):362–363. doi: 10.1016/j.jhin.2020.04.005 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 123.Güner R, Hasanoğlu I, Aktaş F. COVID-19: prevention and control measures in community. Turk J Med Sci. 2020;50(SI–1):571–577. doi: 10.3906/sag-2004-146 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 124.Araghi F, Tabary M, Gheisari M, Abdollahimajd F, Dadkhahfar S. Hand hygiene among health care workers during COVID-19 pandemic: challenges and recommendations. Dermatitis. 2020;31(4):233–237. doi: 10.1097/DER.0000000000000639 [DOI] [PubMed] [Google Scholar]
- 125.Moffa M, Guo W, Li T, Cronk R, Abebe LS, Bartram J. A systematic review of nosocomial waterborne infections in neonates and mothers. Int J Hyg Environ Health. 2017;220(8):1199–1206. doi: 10.1016/j.ijheh.2017.07.011 [DOI] [PubMed] [Google Scholar]
- 126.Brian F, Leas BF, Nancy Sullivan N, et al. Environmental cleaning for the prevention of healthcare-associated infections. (Technical Briefs, No. 22.). Agency for Healthcare Research and Quality. U.S. Department of Health and Human Services; 540 Gaither Road, Rockville, MD 20850, USDA; 2015. Available from: https://www.ncbi.nlm.nih.gov/books/NBK311016/pdf/Bookshelf_NBK311016.pdf. Accessed March3, 2019. [PubMed] [Google Scholar]
- 127.Chemaly RF, Simmons S, Dale C, et al. The role of the healthcare environment in the spread of multidrug-resistant organisms: update on current best practices for containment. Ther Adv Infect Dis. 2014;2(3–4):79–90. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 128.Kenters N, Gottlieb T, Hopman J, et al.;. An international survey of cleaning and disinfection practices in the healthcare environment. J Hosp Infect. 2018;100(2):236–241. doi: 10.1016/j.jhin.2018.05.008 [DOI] [PubMed] [Google Scholar]
- 129.Rupp ME, Fitzgerald T, Hayes K, et al. Effect of cessation of contact isolation for endemic methicillin-resistant Staphylococcus aureus and vancomycin-resistant enterococci. Infect Control Hosp Epidemiol. 2017;38(8):1005–1007. doi: 10.1017/ice.2017.122 [DOI] [PubMed] [Google Scholar]
- 130.Ministry of Health and Family Welfare, Government of India. National guidelines for clean hospitals. Applicable to tertiary care hospitals, hospitals associated with medical colleges & super-specialty hospitals in India; 2015. Available from: https://mohfw.gov.in/sites/default/files/7660257301436254417_0.pdf. Accessed March3, 2019.
- 131.Ling ML, Apisarnthanarak A, Thu le TA, Villanueva V, Pandjaitan C, Yusof MY. APSIC guidelines for environmental cleaning and decontamination. Antimicrob Resist Infect Control. 2015;4:58. doi: 10.1186/s13756-015-0099-7 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 132.Mehta Y, Gupta A, Todi S, et al. Guidelines for prevention of hospital-acquired infections. Indian J Crit Care Med. 2014;18(3):149–163. doi: 10.4103/0972-5229.128705 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 133.National Clinical Guideline Centre (UK). Infection: prevention and control of healthcare-associated infections in primary and community care: partial update of NICE clinical guideline 2. London: Royal College of Physicians (UK); 2012. (NICE Clinical Guidelines, No. 139.) 7, Standard principles for the use of personal protective equipment Available from: https://www.ncbi.nlm.nih.gov/books/NBK115274/. Accessed March3, 2019. [PubMed] [Google Scholar]
- 134.Lupión C, López-Cortés LE, Rodríguez-Baño J. Preventive measures for avoiding transmission of microorganisms between hospitalized patients. Hand hygiene [Medidas de prevención de la transmisión de microorganismos entre pacientes hospitalizados. Higiene de manos]. Enferm Infecc Microbiol Clin. 2014;32(9):603–609. doi: 10.1016/j.eimc.2014.02.003 [DOI] [PubMed] [Google Scholar]
- 135.Yousif SA, Alenazi TH, Arabi Y. Taming the beast: hospital management of a nosocomial middle east respiratory syndrome outbreak. J Infect Public Health. 2016;9(4):386–388. doi: 10.1016/j.jiph.2016.03.002 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 136.Government of South Africa. Environmental hygiene in healthcare. Available from: https://www.sahealth.sa.gov.au/wps/wcm/connect/public+content/sa+health+internet/clinical+resources/clinical+topics/healthcare+associated+infections/prevention+and+management+of+infections+in+healthcare+settings/environmental+hygiene+in+healthcare#main. Accessed March3, 2019.
- 137.Carling PC. Optimizing health care environmental hygiene. Infect Dis Clin North Am. 2016;30(3):639–660. doi: 10.1016/j.idc.2016.04.010 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 138.Adams J, Bartram J, Chartier Y Essential environmental health standards in health care. WHO Press, World Health Organization, 20 Avenue Appia, 1211 Geneva 27, Switzerland; 2008. Available from: https://www.who.int/water_sanitation_health/hygiene/settings/ehs_health_care.pdf.pdf. Accessed March3, 2019. [Google Scholar]
- 139.Allen M, Hall L, Halton K, Graves N. Improving hospital environmental hygiene with the use of a targeted multi-modal bundle strategy. Infect Dis Health. 2018;23(2):107–113. doi: 10.1016/j.idh.2018.01.003 [DOI] [PubMed] [Google Scholar]
- 140.Sydnor ER, Perl TM. Hospital epidemiology and infection control in acute-care settings. Clin Microbiol Rev. 2011;24(1):141–173. doi: 10.1128/CMR.00027-10 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 141.Shillabeer AG. Current Status. In: Shillabeer AG (Eds) The health of Vietnam. 57–90, Singapore: Springer; 2016. doi: 10.1007/978-981-287-709-3_5 [DOI] [Google Scholar]
- 142.Sehulster LM, Chinn RYW, Arduino MJ, et al. Guidelines for environmental infection control in health-care facilities. Recommendations of CDC and the Healthcare Infection Control Practices Advisory Committee (HICPAC). U.S. Department of Health and Human Services, Centers for Disease Control and Prevention (CDC), Atlanta, GA 30329, 2003. Available from: https://www.cdc.gov/infectioncontrol/pdf/guidelines/environmental-guidelines.pdf. Accessed March9, 2019. [PubMed] [Google Scholar]
- 143.Centers for Disease Control and Prevention. Guide to infection prevention for outpatient settings; 2011. Available from: http://www.cdc.gov/HAI/pdfs/guidelines/Outpatient-Care-Guide-withChecklist.pdf. Accessed March9, 2019.
- 144.The United States Environmental Protection Agency. What are antimicrobial pesticides? 2014. Available from: http://www.epa.gov/oppad001/ad_info.htm. Accessed March9, 2019.
- 145.National Institute for Occupational Safety and Health (NIOSH); Quinn MM, Henneberger PK, Braun B, et al. Cleaning and disinfecting environmental surfaces in health care: toward an integrated framework for infection and occupational illness prevention. Am J Infect Control. 2015;43(5):424–434. doi: 10.1016/j.ajic.2015.01.029. [DOI] [PubMed] [Google Scholar]
- 146.Rutala WA, Weber DJ; The Healthcare Infection Control Practices Advisory Committee (HICPAC). Guideline for disinfection and sterilization in healthcare facilities, 2008; 2019. Centers for Disease Control and Prevention, National Center for Emerging and Zoonotic Infectious Diseases (NCEZID), Division of Healthcare Quality Promotion (DHQP), 1600 Clifton Road Atlanta, GA 30329-4027, USA: Available from: https://www.cdc.gov/infectioncontrol/pdf/guidelines/disinfection-guidelines.pdf. Accessed March9, 2019. [Google Scholar]
- 147.Kelsey JC. Sterilization by ethylene oxide. J Clin Pathol. 1961;14(1):59–61. doi: 10.1136/jcp.14.1.59 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 148.Furuhashi M, Miyamae T. Ethylene oxide sterilization of medical devices–with special reference to the sporicidal activity and residual concentration of ethylene oxide and its secondary products. Bull Tokyo Med Dent Univ. 1982;29(2):23–35. [PubMed] [Google Scholar]
- 149.Centers for Disease Control and Prevention, National Center for Emerging and Zoonotic Infectious Diseases (NCEZID), Division of Healthcare Quality Promotion (DHQP). Guideline for disinfection and sterilization in healthcare facilities (2008); 2017. Available from https://www.cdc.gov/infectioncontrol/guidelines/disinfection/introduction.html. Accessed March9, 2019.
- 150.Irek EO, Amupitan AA, Obadare TO, Aboderin AO. A systematic review of healthcare-associated infections in Africa: an antimicrobial resistance perspective. Afr J Lab Med. 2018;7(2):796. doi: 10.4102/ajlm.v7i2.796 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 151.Li B, Webster TJ, Zhao H. Bacteria antibiotic resistance: new challenges and opportunities for implant-associated orthopedic infections. J Orthop Res. 2017;36(1):22–32. doi: 10.1186/s13018-017-0520-4 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 152.Hamdy RF, Hsu AJ, Stockmann C, et al. Epidemiology of methicillin-resistant Staphylococcus aureus bacteremia in children. Pediatrics. 2017;139(6):e20170183. doi: 10.1542/peds.2017-0183 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 153.Morgan DJ, Murthy R, Munoz-Price LS, et al. Reconsidering contact precautions for endemic methicillin-resistant Staphylococcus aureus and vancomycin-resistant Enterococcus. Infect Control Hosp Epidemiol. 2015;36(10):1163–1172. doi: 10.1017/ice.2015.156 [DOI] [PubMed] [Google Scholar]
- 154.De Angelis G, Cataldo MA, De Waure C, et al. Infection control and prevention measures to reduce the spread of vancomycin-resistant enterococci in hospitalized patients: a systematic review and meta-analysis. J Antimicrob Chemother. 2014;69(5):1185–1192. doi: 10.1093/jac/dkt525 [DOI] [PubMed] [Google Scholar]
- 155.Otter JA, Mutters NT, Tacconelli E, Gikas A, Holmes AH. Controversies in guidelines for the control of multidrug-resistant Gram-negative bacteria in EU countries. Clin Microbiol Infect. 2015;21(12):1057–1066. doi: 10.1016/j.cmi.2015.09.021 [DOI] [PubMed] [Google Scholar]
- 156.Tacconelli E. Screening and isolation for infection control. J Hosp Infect. 2009;73(4):371e377. doi: 10.1016/j.jhin.2009.05.002 [DOI] [PubMed] [Google Scholar]
- 157.Infection Control Today. Active Surveillance Cultures: friend or Foe? 2010. Available from: https://www.infectioncontroltoday.com/epidemiology-surveillance/active-surveillance-cultures-friend-or-foe. Accessed March14, 2019.
- 158.Edmond M, Lyckholm L, Diekema D. Ethical implications of active surveillance cultures and contact precautions for controlling multidrug-resistant organisms in the hospital setting. Public Health Ethics. 2008;1(3):235–245. doi: 10.1093/phe/phn014 [DOI] [Google Scholar]
- 159.McGinigle KL, Gourlay ML, Buchanan IB. The use of active surveillance cultures in adult intensive care units to reduce methicillin-resistant Staphylococcus aureus–related morbidity, mortality, and costs: a systematic review. Clin Infect Dis. 2008;46(11):1717–1725. doi: 10.1086/587901 [DOI] [PubMed] [Google Scholar]
- 160.Soroksky A, Nagornov S, Klinowski E, et al. Active surveillance cultures in critically ill patients: pathogens, patterns, and correlation with eventual bloodstream infections. Isr Med Assoc J. 2014;16(7):418–422. [PubMed] [Google Scholar]
- 161.Edmond MB, Ober JF, Bearman G. Active surveillance cultures are not required to control MRSA infections in the critical care setting. Am J Infect Control. 2008;36(6):461–463. doi: 10.1016/j.ajic.2007.09.011 [DOI] [PubMed] [Google Scholar]
- 162.Vos MC, Ott A, Verbrugh HA, Wannet WJB, de Neeling AJ. Successful search-and-destroy policy for methicillin-resistant Staphylococcus aureus in the Netherlands. J Clin Microbiol. 2005;43(4):2034. doi: 10.1128/JCM.43.4.2034-2035.2005 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 163.Bootsma MC, Diekmann O, Bonten MJ. Controlling methicillin-resistant Staphylococcus aureus: quantifying the effects of interventions and rapid diagnostic testing. Proc Natl Acad Sci USA. 2006;103(14):5620–5625. doi: 10.1073/pnas.0510077103 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 164.Henderson DK. Managing methicillin-resistant staphylococci: a paradigm for preventing nosocomial transmission of resistant organisms. Am J Med. 2006;119(Suppl 6):S45–52. doi: 10.1016/j.amjmed.2006.04.002 [DOI] [PubMed] [Google Scholar]
- 165.Chemaly RF, Simmons S, Dale C, et al. The role of the healthcare environment in the spread of multidrug-resistant organisms: update on current best practices for containment. Ther Adv Infect Dis. 2014;2(3–4):79–90. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 166.Duffy J, Sievert D, Rebmann C, et al. Effective state-based surveillance for multidrug-resistant organisms related to healthcare-associated infections. Public Health Rep. 2011;126(2):176–185. doi: 10.1177/003335491112600208 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 167.Goetz MB, Mulligan ME, Kwok R, O’Brien H, Caballes C, Garcia JP. Management and epidemiologic analyses of an outbreak due to methicillin-resistant Staphylococcus aureus. Am J Med. 1992;92(6):607–614. doi: 10.1016/0002-9343(92)90778-A [DOI] [PubMed] [Google Scholar]
- 168.Safdar N, Marx J, Meyer NA, Maki DG. Effectiveness of preemptive barrier precautions in controlling nosocomial colonization and infection by methicillin-resistant Staphylococcus aureus in a burn unit. Am J Infect Control. 2006;34(8):476–483. doi: 10.1016/j.ajic.2006.01.011 [DOI] [PubMed] [Google Scholar]
- 169.Tomar SL. Public health perspectives on surveillance for periodontal diseases. J Periodontol. 2007;78(Suppl 7S):1380–1386. doi: 10.1902/jop.2007.060340 [DOI] [PubMed] [Google Scholar]
- 170.Ridelberg M, Nilsen P. Using surveillance data to reduce healthcare-associated infection: a qualitative study in Sweden. J Infect Prev. 2015;16(5):208–214. doi: 10.1177/1757177415588380 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 171.de Bruin JS, Seeling W, Schuh C. Data use and effectiveness in electronic surveillance of healthcare-associated infections in the 21st Century: a systematic review. J Am Med Inform Assoc. 2014;21(5):942–951. doi: 10.1136/amiajnl-2013-002089 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 172.van Bunnik BA, Ciccolini M, Gibbons CL, et al. Efficient national surveillance for health-care-associated infections. BMC Public Health. 2015;15:832. doi: 10.1186/s12889-015-2172-9 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 173.Morris AK, Russell CD. Enhanced surveillance of Staphylococcus aureus bacteremia to identify targets for infection prevention. J Hosp Infect. 2016;93(2):169–174. doi: 10.1016/j.jhin.2016.03.003 [DOI] [PubMed] [Google Scholar]
- 174.Murdoch F, Danial J, Morris AK, et al. The Scottish enhanced Staphylococcus aureus bacteremia surveillance program: the first 18 months of data in adults. J Hosp Infect. 2017;97(2):133–139. doi: 10.1016/j.jhin.2017.06.008 [DOI] [PubMed] [Google Scholar]
- 175.Agarwal R, Mohapatra S, Rath GP, Kapil A. Active surveillance of health care-associated infections in neurosurgical patients. J Clin Diagn Res. 2017;11(7):DC01–DC04. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 176.Zuschneid I, Rücker G, Schoop R, et al. Representativeness of the surveillance data in the intensive care unit component of the German nosocomial infections surveillance system. Infect Control Hosp Epidemiol. 2010;31(9):934–938. doi: 10.1086/655462 [DOI] [PubMed] [Google Scholar]
- 177.Garner JS, Emori WR, Horan TC, Hughes JM, Hughes JM. CDC definitions for nosocomial infections. Am J Infect Control. 1988;16(3):128–140. doi: 10.1016/0196-6553(88)90053-3 [DOI] [PubMed] [Google Scholar]
- 178.Emori TG, Culver DH, Horan TC, et al. National nosocomial infection surveillance system (NNIS): description of surveillance methods. Am J Infect Control. 1991;19(1):19–35. doi: 10.1016/0196-6553(91)90157-8 [DOI] [PubMed] [Google Scholar]
- 179.Rücker G, Schoop R, Beyersmann J, Schumacher M, Zuschneid I. Are KISS data representative of German intensive care units? Statistical issues. Methods Inf Med. 2006;45(4):424–429. doi: 10.1055/s-0038-1634099 [DOI] [PubMed] [Google Scholar]
- 180.Gastmeier P, Schwab F, Geffers C, Rüden H. To isolate or not to isolate? Analysis of data from the German Nosocomial Infection Surveillance System regarding the placement of patients with methicillin-resistant Staphylococcus aureus in private rooms in intensive care units. Infect Control Hosp Epidemiol. 2004;25(2):109–113. doi: 10.1086/502359 [DOI] [PubMed] [Google Scholar]
- 181.Mehta Y, Gupta A, Todi S, et al. Guidelines for prevention of hospital-acquired infections. Indian J Crit Care Med. 2014;18(3):149–163. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 182.Alp E, Damani N. Healthcare-associated infections in intensive care units: epidemiology and infection control in low-to-middle income countries. J Infect Dev Ctries. 2015;9(10):1040–1045. doi: 10.3855/jidc.6832 [DOI] [PubMed] [Google Scholar]
- 183.Ciccolini M, Donker T, Grundmann H, Bonten MJ, Woolhouse ME. Efficient surveillance for healthcare-associated infections spreading between hospitals. Proc Natl Acad Sci USA. 2014;111(6):2271–2276. doi: 10.1073/pnas.1308062111 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 184.McGowan JE, Gerding DN. Does antibiotic restriction prevent resistance? New Horiz. 1996;4(3):370–376. [PubMed] [Google Scholar]
- 185.The Society for Healthcare Epidemiology of America. Antimicrobial Stewardship; 2019. 1300 Wilson Boulevard, Suite 300, Arlington, VA 22209, USA: Available from https://www.shea-online.org/index.php/practice-resources/priority-topics/antimicrobial-stewardship. Accessed March16, 2019. [Google Scholar]
- 186.Gerding DN. The search for good antimicrobial stewardship. Jt Comm J Qual Improv. 2001;27(8):403–404. [DOI] [PubMed] [Google Scholar]
- 187.Dyar OJ, Huttner B, Schouten J, Pulcini C; ESGAP (ESCMID Study Group for Antimicrobial stewardship). What is antimicrobial stewardship? Clin Microbiol Infect. 2017;23(11):793–798. doi: 10.1016/j.cmi.2017.08.026 [DOI] [PubMed] [Google Scholar]
- 188.Sartelli M, Coccolini F, Abu-Zidan FM, et al. Hey surgeons! It is time to lead and be a champion in preventing and managing surgical infections! World J Emerg Surg. 2020;15(1):28. doi: 10.1186/s13017-020-00308-1 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 189.Sartelli M, Malangoni MA, May AK, et al. World Society of Emergency Surgery (WSES) guidelines for management of skin and soft tissue infections. World J Emerg Surg. 2014;9(1):57. doi: 10.1186/1749-7922-9-57 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 190.Sartelli M, Malangoni MA, Abu-Zidan FM, et al. WSES guidelines for management of Clostridium difficile infection in surgical patients. World J Emerg Surg. 2015;10:38. doi: 10.1186/s13017-015-0033-6 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 191.Sartelli M, Chichom-Mefire A, Labricciosa FM, et al. The management of intra-abdominal infections from a global perspective: 2017 WSES guidelines for management of intra-abdominal infections. World J Emerg Surg. 2017;12:29. doi: 10.1186/s13017-017-0141-6 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 192.Doron S, Davidson LE. Antimicrobial stewardship. Mayo Clin Proc. 2011;86(11):1113–1123. doi: 10.4065/mcp.2011.0358 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 193.Centers for Disease Control and Prevention, National Center for Emerging and Zoonotic Infectious Diseases (NCEZID), Division of Healthcare Quality Promotion (DHQP). Core elements of hospital antibiotic stewardship programs; 2015. Available from: https://www.cdc.gov/antibiotic-use/healthcare/implementation/core-elements.html. Accessed March16, 2019.
- 194.Joseph J, Rodvold KA. The role of carbapenems in the treatment of severe nosocomial respiratory tract infections. Expert Opin Pharmacother. 2008;9(4):561–575. doi: 10.1517/14656566.9.4.561 [DOI] [PubMed] [Google Scholar]
- 195.Solomon DH, Van Houten L, Glynn RJ, et al. Academic detailing to improve use of broad-spectrum antibiotics at an academic medical center. Arch Intern Med. 2001;161(15):1897–1902. doi: 10.1001/archinte.161.15.1897 [DOI] [PubMed] [Google Scholar]
- 196.Fraser GL, Stogsdill P, Dickens JD, Wennberg DE, Smith RP, Prato BS. Antibiotic optimization: an evaluation of patient safety and economic outcomes. Arch Intern Med. 1997;157(15):1689–1694. doi: 10.1001/archinte.1997.00440360105012 [DOI] [PubMed] [Google Scholar]
- 197.Baur D, Gladstone BP, Burkert F, et al. Effect of antibiotic stewardship on the incidence of infection and colonization with antibiotic-resistant bacteria and Clostridium difficile infection: a systematic review and meta-analysis. Lancet Infect Dis. 2017;17(9):990–1001. doi: 10.1016/S1473-3099(17)30325-0 [DOI] [PubMed] [Google Scholar]
- 198.Khdour MR, Hallak HO, Aldeyab MA, et al. Impact of antimicrobial stewardship program on hospitalized patients at the intensive care unit: a prospective audit and feedback study. Br J Clin Pharmacol. 2018;84(4):708–715. doi: 10.1111/bcp.13486 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 199.Timbrook TT, Hurst JM, Bosso JA. Impact of an antimicrobial stewardship program on antimicrobial utilization, bacterial susceptibilities, and financial expenditures at an academic medical center. Hosp Pharm. 2016;51(9):703–711. doi: 10.1310/hpj5109-703 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 200.Nathwani D, Varghese D, Stephens J, Ansari W, Martin S, Charbonneau C. Value of hospital antimicrobial stewardship programs [ASPs]: a systematic review. Antimicrob Resist Infect Control. 2019;8:35. doi: 10.1186/s13756-019-0471-0 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 201.Honda H, Ohmagari N, Tokuda Y, Mattar C, Warren DK. Antimicrobial stewardship in inpatient settings in the asia pacific region: a systematic review and meta-analysis. Clin Infect Dis. 2017;64(Suppl_2):S119–S126. doi: 10.1093/cid/cix017 [DOI] [PubMed] [Google Scholar]
- 202.Goff DA. Antimicrobial stewardship: bridging the gap between quality care and cost. Curr Opin Infect Dis. 2011;24(Suppl 1):S11–20. doi: 10.1097/01.qco.0000393484.17894.05 [DOI] [PubMed] [Google Scholar]
- 203.Dik JW, Poelman R, Friedrich AW, et al. An integrated stewardship model: antimicrobial, infection prevention and diagnostic (AID). Future Microbiol. 2016;11(1):93–102. doi: 10.2217/fmb.15.99 [DOI] [PubMed] [Google Scholar]
- 204.Treadwell JR, Lucas S, Tsou AY. Surgical checklists: a systematic review of impacts and implementation. BMJ Qual Saf. 2013;23(4):299–318. doi: 10.1136/bmjqs-2012-001797 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 205.Carthey J, Walker S, Deelchand V, Vincent C, Griffiths WH. Breaking the rules: understanding non-compliance with policies and guidelines. BMJ. 2011;343:d5283. doi: 10.1136/bmj.d5283 [DOI] [PubMed] [Google Scholar]
- 206.Collins AS. Preventing health care-associated infections In: Hughes RG, editor. Patient Safety and Quality: An Evidence-Based Handbook for Nurses. Rockville (MD): Agency for Healthcare Research and Quality (US); 2008:41. [PubMed] [Google Scholar]
- 207.Dunagan WC, Woodward RS, Medoff G, et al. Antimicrobial misuse in patients with positive blood cultures. Am J Med. 1989;87(3):253e259. doi: 10.1016/S0002-9343(89)80146-9 [DOI] [PubMed] [Google Scholar]
- 208.McInnes E, Phillips R, Middleton S, Gould D. A qualitative study of senior hospital managers’ views on current and innovative strategies to improve hand hygiene. BMC Infect Dis. 2014;14:611. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 209.Gerber JS, Prasad PA, Fiks AG, et al. Durability of benefits of an outpatient antimicrobial stewardship intervention after discontinuation of audit and feedback. JAMA. 2014;312(23):2569–2570. doi: 10.1001/jama.2014.14042 [DOI] [PubMed] [Google Scholar]
- 210.Ament SM, de Groot JJ, Maessen JM, Dirksen CD, van der Weijden T, Kleijnen J. Sustainability of professionals’ adherence to clinical practice guidelines in medical care: a systematic review. BMJ Open. 2015;5(12):e008073. doi: 10.1136/bmjopen-2015-008073 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 211.Pronovost P, Needham D, Berenholtz S, et al. An intervention to decrease catheter-related bloodstream infections in the ICU. N Engl J Med. 2006;355(26):2725–2732. doi: 10.1056/NEJMoa061115 [DOI] [PubMed] [Google Scholar]
- 212.Jeeva RR, Wright D. Healthcare-associated infections: a national patient safety problem and the coordinated response. Med Care. 2014;52(Suppl 2):S4–S8. doi: 10.1097/MLR.0b013e3182a54581 [DOI] [PubMed] [Google Scholar]
- 213.Gastmeier P. Healthcare-associated versus community-acquired infections: a new challenge for science and society. Int J Med Microbiol. 2010;300(6):342–345. doi: 10.1016/j.ijmm.2010.04.007 [DOI] [PubMed] [Google Scholar]
- 214.Gardam MA, Lemieux C, Reason P, van Dijk M, Goel V. Healthcare-associated infections as patient safety indicators. Healthc Pap. 2009;9(3):8–24. doi: 10.12927/hcpap.2009.20922 [DOI] [PubMed] [Google Scholar]
- 215.Bavel JJV, Baicker K, Boggio PS, et al. Using social and behavioral science to support COVID-19 pandemic response. Natl Human Behav. 2020;4(5):460–471. [DOI] [PubMed] [Google Scholar]
- 216.Kuy S, Gupta R, Correa R, Tsai R, Vohra S. Best practices for a Covid-19 preparedness plan for health systems. NEJM Catal Innov Care Deliv. 2020. doi: 10.1056/CAT.20.0108 [DOI] [Google Scholar]
- 217.Triggle CR, Bansal D, Farag EABA, Ding H, Sultan AA, Rosenberg HF. COVID-19: learning from lessons to guide treatment and prevention interventions. mSphere. 2020;5(3):e00317–20. doi: 10.1128/mSphere.00317-20 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 218.Qian X, Ren R, Wang Y, et al. Fighting against the common enemy of COVID-19: a practice of building a community with a shared future for mankind. Infect Dis Poverty. 2020;9(1):34. doi: 10.1186/s40249-020-00650-1 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 219.Lee IK, Wang CC, Lin MC, Kung CT, Lan KC, Lee CT. Effective strategies to prevent coronavirus disease-2019 (COVID-19) outbreak in hospital. J Hosp Infect. 2020;105(1):102–103. doi: 10.1016/j.jhin.2020.02.022 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 220.Wu T, Hu E, Zeng W, Zhang H, Xue X, Ma J. Unprecedented action has been taken to contain the epidemic of coronavirus disease 2019 in China. Zhong Nan Da Xue Xue Bao Yi Xue Ban. 2020;45(3):334–337. [DOI] [PubMed] [Google Scholar]
- 221.Ripabelli G, Tamburro M, Guerrizio G, Fanelli I, Agnusdei CP, Sammarco ML. A single-arm study to evaluate skin tolerance, effectiveness, and adherence to use of an alcohol-based hand rub solution among hospital nurses. J Infect Prev. 2019;20(5):224–230. doi: 10.1177/1757177419846295 [DOI] [Google Scholar]