Carbapenem-resistant A. baumanni or XDR-AB has been recently recognized by the “World Health Organization (WHO) AMR study group” as a high priority Gram-negative organism for the research and development of new antibiotics, given the limited availability of treatment options, its swiftness in developing AMR, in addition to the elevated rates of mortality due to associated infections . Through current evidence, its resistance to disinfection and its endemicity around the globe has exponentially augmented the problem rendering it the nightmare of Infection Control practitioners when managing sustained outbreaks . Another group of international experts developed the “TOp TEn resistant Microorganisms (TOTEM) in critical care” study group, which aimed to assess the global top priority organisms affecting ICU patients specifically . Carbapenem-resistant A. baumannii was again classified as the top critical organism thus coinciding with the WHO priority list .
Many critical care and burn units of acute care facilities in the Middle East and North Africa region have become endemic with XDR-AB . In the current study, out of 335 patients admitted to our ICU, 13% acquired XDR-AB during their stay and the overall incidence reached 14.6 cases/1000 ICU days. Other studies from Lebanon and the region reported different burdens of XDR-AB in critical care units. A prospective study conducted over 7 years form 2007 to 2014 at a large university hospital in Beirut showed that the a rate of XDR-AB colonization pressure was 315.4 cases/1000 ICU patient-days . Another matched case–control study from a specialist hospital in the Kingdom of Saudi Arabia between January and August 2012, assessing potential risk factors for XDR-AB acquisition, showed that the proportion of ICU patients who harbored XDR-AB during their stay reached 33% (66/198 patients) . These figures indicate in our geographical region that XDR-AB is rampant in critical care units.
Infections caused by A. baumanii in general and especially among critically ill patients are associated with high morbidity and mortality . To be able to reduce this high mortality rate, a multidisciplinary approach is essential, including early detection and surveillance for acquisition, strategies for patient risk factor identification, antimicrobial stewardship interventions, and tight adherence to standardized infection control practices [2, 25,26,27,28].
Risk factor identification and mitigation are critical pillars in decreasing the transmission of XDR-AB . Our study showed that contact pressure of 3 or more days with other patients who harbored XDR-AB was an independent risk factor for acquisition of the same organism, and it significantly increased the odds of horizontal acquisition by almost 10 folds. This can be explained by the fact that the open-bay ICU is one big room and all bed occupants are like “roommates”. It has been also well documented that patients admitted to ICU beds of prior occupants who harbored bacterial pathogens are at an elevated risk of acquiring the same organism, i.e. vertical transmission of the organism . In a multicenter matched case-control study that evaluated the association between having a prior bed occupant or roommate with a positive culture and subsequent infection with the same organism, the risk of infection increased by 6 folds in case of the prior bed occupant (vertical transmission) and 5 times in case of the roommate (horizontal transmission) . With time, transmission of XDR-AB occurring in both directions, vertical and horizontal, will absolutely increase and one will lead to the other in an open-bay ICU. In this setting, ICU evacuation and ETD have been practiced to potentially stem the vertical transmission and break the vicious cycle.
Our results further showed that patients who were administered carbapenems for more than 4 days or piperacillin-tazobactam were more likely to acquire XDR-AB during their hospital stay. Antimicrobial stewardship programs play an important role in sparing the use of carbapenems and other broad-spectrum antibiotics . Their extensive use has been positively correlated with an increasing incidence of XDR-AB , while restricting their consumption has led to an important reduction in its incidence [25, 26, 28]. The proper selection of broad-spectrum antibiotics for the empiric treatment of infections is based on the institutional epidemiology of AMR, along with an appropriate duration and de-escalation of therapy once antibiograms are available.
In general, risk factors for XDR-AB acquisition may vary from one ICU to the other due to differences in applying standard precautions, compliance to hand hygiene, distance between beds, type of ICU whether open-bay or single-room [2, 32]. On the other hand, risk factors including the use of invasive devices, treatment with broad-spectrum antibiotics, length of stay in ICU and contact pressure are commonly reported in several studies [2, 3, 23, 33].
Regarding infection prevention, the presence of robust programs is crucial in order to help curb the spread of XDR-AB throughout healthcare systems. Patient cohorting, improved hand hygiene, regular environmental cleaning and disinfection, in addition to novel non-touch techniques used in ETD have succeeded in reducing nosocomial infection rates and controlling outbreaks of XDR-AB [25, 26]. Contactless automated decontamination technologies include aerosol or vaporized H2O2 and mobile continuous germicidal ultraviolet light (UV-C). Yet, the success of ETD, which is only one part of the puzzle, depends on human factors such as training and compliance of nursing and environmental services staff, as well as accessibility of all inanimate surfaces in the unit. The quality of surface disinfection is highlighted by a study that proved surface contamination with epidemiologically important pathogens owed to a failure to practice thorough cleaning and disinfection rather than a faulty product or procedure .
Based on our findings, XDR-AB acquisition followed an ascending trend as a function of numerical weeks after ETD (P = 0.03). This implied that more patients acquired XDR-AB with time after ETD due to the waning effect of the procedure. The complete evacuation of the ICU and admitting patients who are not infected or colonized with XDR-AB decreased the contact pressure during the early numerical weeks after ETD, which is a very strong factor of XDR-AB acquisition as mentioned previously. The effect of the contactless modality of disinfection using aerosolized H2O2 could be explained as such. First, the physical and biochemical properties of the aerosolized H2O2 particles enable it to reach and potentially decontaminate surfaces that are usually inaccessible by manual techniques [35,36,37]. Second, H2O2 could synergistically improve the effect of other common agents used in manual disinfection, such as quaternary-ammonium containing products (used in our case), when applied to cleaned surfaces with potential residual XDR-AB contamination [35,36,37].
A study from the United Kingdom investigated the efficacy of terminal disinfection using different operating concentrations of vaporized hydrogen peroxide on methicillin-resistant Staphylococcus aureus (MRSA), Klebsiella pneumoniae and Clostridium difficile persistence on single isolation room surfaces after patient discharge . Investigators artificially contaminated high-frequency-touch surfaces with these organisms, where the sites were sampled with contact plates before and after hydrogen peroxide fumigation . After manual disinfection only, more than 90% of the sites were still contaminated with these organisms, with high bacterial count present on floors, bed control panels, and nurse call buttons . Enhanced disinfection with hydrogen peroxide achieved an approximately 5 log10 reduction in C. difficile spores on contact plates and an approximately 6 log10 reduction in MRSA/K. pneumoniae colony forming units on contact plates in all tested areas .
The direct effect of ETD in general was recently elucidated in the Benefits of Enhanced Terminal Room (BETR) Disinfection study, a prospective cluster-randomized crossover trial . This study assessed 3 different enhanced methods of room disinfection (bleach, quaternary ammonium-containing product with disinfecting UV-C, and bleach with UV-C compared to a standard disinfection method with quaternary ammonium-containing product only (control) . Results showed that enhanced methods of disinfection overcame limitations of standard disinfection strategies and thus could be potential strategies to reduce the risk of acquisition of multidrug-resistant organisms and Clostridium difficile . This trial has shown the efficacy of using UV-C as a non-touch strategy for enhanced disinfection, but not H2O2. Limited data are available on the activity of aerosolized H2O2 based on laboratory findings or evaluation of experimentally contaminated surfaces in hospitals . An aerosolized H2O2 system was capable of eradicating methicillin-resistant Staphylococcus aureus and A. baumannii on open hospital room surfaces; however, it was not effective in closed or semiclosed areas like inside a drawer . On the other hand, Blazejewski and colleagues reported results of a prospective crossover study in five medical and surgical ICUs located in a single tertiary care hospital, which examined the impact of ETD using H2O2 on environmental contamination with multidrug-resistant organisms including imipenem-resistant A. baumannii . In this study, target rooms (n = 182) underwent routine terminal cleaning with a quaternary ammonium compound and bleach. Then, they were disinfected by either H2O2 vapor or aerosolized H2O2 combined with peracetic acid during 6 weeks with a switch to the other method for another 6 weeks . Environmental sampling of 8 high-touch surfaces was performed in each room at 3 time points: (1) after patient discharge, (2) after routine terminal cleaning, and (3) after ETD. First after patient discharge, 15/182 (8%) rooms were contaminated with at least one multi-drug resistant organism . Then, routine terminal cleaning reduced environmental contamination with multi-drug resistant organisms from 8 to 6% (11/182 rooms), albeit insignificantly (P = 0.371) . Yet, investigators observed a significant reduction in environmental contamination with multi-drug resistant organisms from 11/182 rooms (6%) (after routine terminal cleaning) to 1/182 rooms (0.6%) after ETD using H2O2 (P = 0.004). Interestingly, both studied techniques (aerosolized and vapor H2O2) showed similar disinfection efficacy . The evidence provided in the aforementioned studies could be used to interpret our results, through highlighting the disinfection efficacy of ETD with H2O2, in addition to the effect of decreasing contact pressure after ICU evacuation as mentioned earlier. More robust studies on room decontamination should be performed with specific H2O2 formulations and related ETD techniques, and these should be compared to other standardized and reliable methods.
As we previously mentioned, ETD necessitated the evacuation and closure of our open-bay ICU for at least 24 h. It was not feasible on a regular basis after the discharge of each infected or colonized patient with XDR-AB from the unit. Such intervention is costly regarding the loss of ICU bed occupancy during the time of unit closure. On the other hand, XDR-AB acquisition exerts an economic burden on the hospital, not to mention the associated morbidity and mortality . Finding the optimal timing for ETD would help prevent sustained transmission on one the hand, and unnecessary evacuation and loss of bed occupancy on the other hand. As per the multivariate regression analysis in our cohort, the first numerical week that considerably increased the odds of XDR-AB acquisition with respect to control was ‘Week 7’ after ETD. The chance that a patient staying in the ICU during ‘Week 7’ to have acquired XDR-AB was 6.5 times significantly higher than not to acquire it. So, we recommend performing ETD with aerosolized H2O2 every 7 calendar weeks in our open-bay ICU as part of an infection control bundle, in order to limit the increasing rate of XDR-AB acquisition with time.
The increasing risk of XDR-AB acquisition with time after ETD in an open-bay ICU makes this design a questionable situation. Separate rooms or cubicles where ETD can be performed after the stay of each colonized or infected patient might be the preferable architecture of an ICU in the era of virulent XDR organism transmission, along with the paucity of effective antimicrobials . Halaby et al. successfully described the implementation of a single room policy in their ICU compared to a previous open-bay design. This shift resulted in a clear and sustained decrease in the prevalence of the multi-drug resistant Gram-negative bacteria, keeping in mind that no significant changes in variables including bed occupancy and numbers of patient admissions was documented during the study period . In 2018, the revised US guidelines of hospital construction provided a new recommendation that critical care units be designed on a single-room basis except for neonatal ICUs . An exception is provided for renovation of patient rooms or cubicles for single-patient use provided they have a minimum clear floor area of 150 square feet .