A. baumannii is one of the most threatening nosocomial microorganisms, characterized by its capacity to survive in various environments and to develop antibiotic resistance. Drug-resistant A. baumannii is prevalent in several healthcare facilities in China. The rapid growth of antibiotic resistance poses considerable economic and medical burdens. In 2017, carbapenem resistant-A. baumannii (CRAB) had a prevalence of 56.1% in China and was related to higher costs, longer hospital stays, and increased mortality in hospital . A study conducted in China estimated that there is a 1.5-fold increase in total medical costs as a result of CRAB . Due to increasing occurrence of XDR and pan drug-resistant A. baumannii strains, WHO reported that there is an urgent need of novel antibiotics , emphasizing the importance of preventing and treating drug-resistant A. baumannii.
This study assessed the effect of XDR-AB colonization on prognoses of severely ill patients. We conducted the study in two mixed adult ICUs in China, where XDR-AB is the most common pathogen in nosocomial infections. The findings revealed that XDR-AB colonization had no effect on the short-term (28-day) mortality of ICU patients but contributed to a 1.97-fold increase in mortality risk at six months.
In our study, the overall peripheral colonization rate of XDR-AB was 18%, which is higher than in previous reports. In Korean ICUs without outbreaks, 5.2% of patients were colonized with CRAB at admission . A prevalence of 13.5% CRAB was observed in trauma ICU patients (n = 364) at an American tertiary hospital from 2010 to 2011 . The relatively high prevalence obtained in our study indicated a possible regional epidemic of XDR-AB in our ICUs.
Studies have elucidated several risk factors of XDR-AB colonization, such as previous admission to long-term healthcare facilities, invasive operations, presence of comorbidities, low socioeconomic status, and previous use of carbapenems [24, 26, 27]. In this study, critical patients with more comorbidities and higher intensity of care were more likely to be colonized with XDR-AB. There are possible reasons for this finding. First, in critically ill patients, immune system disorders lead to poor defensive responses, making them more susceptible to opportunistic pathogens. Second, invasive operations, such as vascular and urinary catheters, tracheostomy, and drainage, provide chances for pathogen colonization through wounds and invasive devices due to impairments in skin and mucosal barriers. Finally, decolonization has not been adopted in ICUs in China; therefore, long hospitalizations coupled with poor baseline conditions and more intensive care might increase opportunities for colonization.
There is not much information on the impact of XDR-AB colonization on patient prognosis. It has been wildly accepted that A. baumannii infections can lead to higher death rates. Among critically ill patients, the estimated increase of in-hospital mortality rate due to A. baumannii infection ranges between 7.8% and 23%, and attributable ICU mortality ranges from 10–43% . High mortality rates have been reported in patients infected with drug-resistant A. baumannii [29, 30]. Colonization with multiple drug-resistant A. baumannii (MDR-AB) upon ICU admission is related with a 1.4-fold increase in in-hospital death rate . Several studies have concluded that colonization and infection with A. baumannii is an independent risk factor of mortality [26, 31–33], without distinguishing between colonization and infection. In this study, we identified colonization using nasopharyngeal and perirectal samplings, which are generally used to identify colonization   . As far as we know, this is the first research to assess the effect of XDR-AB colonization on long-term mortality in critical patients. The results revealed that XDR-AB colonization has no impact on the 28-day prognosis based on the multivariate analysis findings but was associated with higher mortality rates at six months. XDR-AB colonization is an independent risk factor of poor long-term prognoses, indicating the necessity of essential surveillance during the early stage and efficient measures of decolonization.
A meta-analysis reported that decolonization reduces infection caused by multidrug-resistant Gram-negative bacteria when combined with standard care, especially in Europe, where decolonization has been widely applied as an infection prevention and control strategy . However, considering there is a lack of effective antibiotics, it is challenging to eliminate XDR-AB. Daily whole-body bathing with chlorhexidine was efficient in removing MDR-AB from the skin  and was helpful in reducing bloodstream infections in patients colonized with XDR Gram-negative bacilli , making it a practicable approach to decolonize XDR-AB. Decontamination of alimentary tract with polymyxin E and tobramycin was effective in patients colonized with MDR-AB [35, 39–41]. However, there is no clinical evidence on systematic antibiotics for the decolonization of XDR-AB. Additionally, standard nosocomial care is of vital importance, e.g., hand hygiene, exposure precautions, conventional screening, and environmental sterilization especially in wards with highly prevalent strains . According to guidelines established by the European Committee on Infection Control (EUCIC), there is not enough information supporting decolonization of CRAB . Our data provided some evidence supporting the need for decolonization, but further interventional studies are required for strategy development and efficacy validation.
Even though our study did not focus on subsequent infections of XDR-AB, it has been acknowledged that in critical patients, colonization with Gram-negative bacteria contributes to more nosocomial infections . The risk of developing subsequent A. baumannii infections is 8.4 times higher in patients colonized with CRAB . In this study, we observed a greater use of colistin or tigecycline after detecting XDR-AB colonization, which indicated a higher incidence of infections. It is possible that subsequent infections might contribute to the increased risk of mortality.
Subgroup analyses of six-month mortality rates were performed in patients with different characteristics, showing consistent results. Patients colonized with XDR-AB had the worse prognosis (with HR > 1) in all groups; however, some of the subgroups did not show statistical significance. Colonization of XDR-AB was recognized as a risk factor of six-month mortality regardless of age, admission season, comorbidity, and APACHE II scores upon admission. In addition, XDR-AB colonization was worse in ICU patients who were hospitalized for more than 14 days (HR 2.022, 95% CI: 1.393–2.936), indicating the harmful effect of XDR-AB colonization on critical patients with prolonged ICU length of stay.
Our study had some limitations. First, there is no information on the effect of colonization with sensitive or MDR-AB on patient prognosis. Approximately 95% of A. baumannii strains isolated were XDR strains, and sensitive and multidrug-resistant strains were rare. Second, we assumed that colonized patients remained colonized with XDR-AB at discharge, because decolonization measures were not performed.