The extremely diversified Acinetobacter genus includes more than 50 species of nonpigmented, Gram-negative, oxidase-positive or oxidase-negative coccobacilli, the bulk of which are nonpathogenic, environmental organisms (1). The species Acinetobacter baumannii, Acinetobacter calcoaceticus, and Acinetobacter lwoffii are the most commonly detected, while Acinetobacter haemolyticus, Acinetobacter johnsonii, Acinetobacter nosocomialis, Acinetobacter pittii, and Acinetobacter schindleri are sporadically encountered (2–4). Typically, the four species A. calcoaceticus, A. baumannii, A. pittii, and A. nosocomialis form together the so called A. calcoaceticus–A. baumannii complex, being closely related and difficult to routinely distinguish; and recently, two new species, Acinetobacter seifertii and Acinetobacter dijkshoorniae were also included within that complex (5).

The 1960s and 1970s witnessed the emergence of infections caused by Acinetobacter species, coinciding with the use of sophisticated intensive care (6, 7). Initially thought of as a commensal opportunist with moderate virulence and little clinical significance, Acinetobacter infections increased in incidence and severity over the past few decades, an increase concomitant with rising prevalence of procedures including mechanical ventilation, central venous catheterization, and broad-spectrum antimicrobial therapy (8, 9). Nowadays, infections by Acinetobacter species, especially A. baumannii, are widely disseminated across hospitals, with highest density in intensive care units (ICUs), accounting for at least 20% of hospital-acquired infections in these wards (10), with estimates of resulting overall mortality exceeding 40% (11). In particular, A. baumannii group includes opportunistic pathogens that cause ventilator-associated pneumonia (VAP), central-line catheter-associated bloodstream infections (CLABSI), meningitis, urinary tract infections, surgical-site and wound infections, among others (12, 13). In one study, A. baumannii accounted for at least 9% of all Gram-negative infections and about 22% of infections in the ICU (14). Moreover, it is incriminated in over 7% of hospital-acquired pneumonia in the ICU and about 2% of nosocomial bloodstream infections (15). In a report issued in 2016 by the National Healthcare Safety Network in the US, the most frequent antimicrobial-resistant pathogens associated with health care-associated infections were reviewed. Acinetobacter species accounted for over 12% of VAP, 8.8% of CLABSI, 1.3% of catheter-associated urinary tract infections, and 1.3% of surgical site infections among gram-negative bacteria (16).

Along with the rise of Acinetobacter infections, major classes of antibiotics are threatened to lose their effectiveness against this pathogen, given its complex and varied resistance mechanisms (17). Acinetobacter exhibits exceptional capacity to retain a multidrug-resistant (MDR) phenotype, further complicating therapy, through a wide variety of pathways such as antibiotic-hydrolyzing enzymes, efflux pump alterations, impermeability, and antibiotic target mutations (18). As such, Acinetobacter spp. are capable of hydrolyzing β-lactams through the four different classes (A to D) of Ambler enzymes; produce aminoglycoside-modifying enzymes; expel multiple antibiotics by efflux pumps; alter carbapenem and aztreonam access through porin mutations; and modify key antibiotic targets like penicillin-binding proteins, DNA gyrase, and lipopolysaccharide (19–22). Accordingly, infections caused by Acinetobacter currently present a challenge to clinicians, and the available therapeutic options remain extremely limited (23). Due to accumulated mechanisms of resistance, Acinetobacter has been classified as MDR, extensively drug resistant (XDR) and pan-drug resistant (PDR), according to the published classification by Magiorakos et al. (24) for healthcare-associated, antimicrobial resistant bacteria. These phenotypes pose a real exertion to antimicrobial chemotherapy (25), and are associated with considerable mortality (26, 27).

In the Gulf Cooperation Council (GCC) and Middle East and North Africa (MENA) regions, accumulating data indicate the prevalence of MDR Acinetobacter infections. For example, Aedh and Colleagues (28) recently demonstrated alarming levels of resistance among MDR Acinetobacter in Saudi ICUs, with gentamicin and colistin being the most sensitive antibiotics. The rate of resistance to antibiotics from β-lactam, fluoroquinolone, and aminoglycoside groups was above 50%, while only trimethoprim-sulfamethoxazole was active against 50% of the isolates. Also in Qatar, different lineages of carbapenemase-producing, MDR Acinetobacter were reported (29). In Kuwait, independent research groups have previously documented expansion of MDR Acinetobacter across different hospitals, with polyclonal nature and transferrable resistance determinants (30–32). As far as the United Arab Emirates (UAE) is concerned, the first preliminary analysis of resistant A. baumannii from the Emirate of Dubai in 2021 reported multiple carbapenemase genes that have horizontally spread (33). An earlier study described MDR Acinetobacter with heterogeneous, sporadic types isolated from 5 different hospitals in Abu Dhabi (34). Moreover, in a local follow-up analysis from a single tertiary hospital at Al-Ain Emirate, a drop in imipenem susceptibility in Acinetobacter species from 99% in 2004 to only 32.5% in 2008 was noticed (35). Such evidence did shed a light on specific resistance mechanisms among local Acinetobacter species and created a background underscoring the need for further surveillance and control. However, large-scale, UAE-wide epidemiological studies of this group of bacteria are still lacking, and trends in antimicrobial resistance remain to be investigated. Of note, these trends have been increasing in reports from various regions (36–40), although some studies indicate a decreasing trend, such as that reported by Logan and colleagues (41), where cephalosporin-resistant A. baumannii decreased significantly between 2008 and 2012 in pediatric infections. The decrease was attributed to calls for improvement in infection control practices during that period, as well as to the concomitant release of an expert guidance on implementation of antimicrobial stewardship in critical care.

The UAE is a country in the GGC region well known for its cosmopolitan atmosphere, being a host for several nationalities and cultures, and a growing role as an international travel, tourism, finance, and health industry hub (42). Such blended and diversified population increases the risk for dissemination of resistant pathogens, and Acinetobacter are not an exception. Nevertheless, a consolidated, time-trend analysis of the evolution and changes in Acinetobacter resistance traits over a long period has not been previously realized in the UAE. While challenges in Acinetobacter species persist, given its nosocomial, resilient nature, longitudinal, retrospective, surveillance studies of such pathogen in a specific region remain necessary (17). Such studies highlight patterns and trends of infection and antibiotic resistance which eventually provide direction for strengthening infection control strategies in healthcare settings in this region (43), and should be beneficial to follow up Acinetobacter resistance patterns in the UAE.

The current investigation was realized to describe the longitudinal changes in Acinetobacter species resistance trends, as reported by the national antimicrobial resistance surveillance system that covers all the seven UAE Emirates. The specific objective of this follow-up study was to explore the nationwide status of Acinetobacter species resistance and evolving nosocomial patterns. It lays out the most prevalent Acinetobacter spp. observed at UAE healthcare facilities, along with the prevalence of their MDR, XDR, and PDR phenotypes, and represents the first documentation of a 12-year resistance portfolio in this pathogen across the whole country, from 2010 until 2021.

This is the first comprehensive analysis across the UAE that shows the significance and magnitude of Acinetobacter infections in clinical settings and the fluctuations in their antimicrobial resistance patterns. The present research utilized an extensive dataset collected over a considerable duration, allowing precise observation of subtle variations in antimicrobial resistance among Acinetobacter. This level of inclusive analysis has not been previously replicated in the country. The samples analyzed in this study consisted of non-repetitive Acinetobacter of laboratory confirmed identity and antibiotic resistance profile, indicating authenticity of the microbiological material used and accuracy of the generated data. Perhaps the most thought-provoking finding in this study is the observation of a decrease in antibiotic resistance in Acinetobacter over about 12 years, and this was evident despite an increase in the number of participating sites from 22 to 317, distributed across all the seven Emirates.

The UAE accommodates a diverse community comprising more than 200 nationalities. Emirati nationals make up approximately 10% of the overall population, highlighting the UAE’s status as one of the countries with a significant expatriate presence. Among the expatriate groups, Indians and Pakistanis represent the largest segments, accounting for 27.5 and 12.7% of the total population, respectively. However, our results show that about 23% of Acinetobacter samples were recovered from Emirati nationals, while 6.1 and 4.5% were recovered from Indian and Pakistani expatriates, respectively. These proportions of the total sample pool should be interpreted cautiously, since 40.6% of the samples attributed from patients for whom their nationality was not coded in the data, hence not available. With the expatriate-inclusive and multicultural setting, expected to prevail for the forthcoming years, the UAE may be an interesting niche to compare how trends of resistance in Acinetobacter differ by nationality, shedding a light on cultural and social factors contributing to resistance in a multidisciplinary research perspective, as previously suggested (47, 48). However, given that a massive 40.6% of our samples originated from patients with unknown nationality, this investigation could not be realized with our data, but remains tempting to explore. Moreover, the majority of patients (52%) from whom samples for the study were recovered were residents of the Emirate of Abu Dhabi, which also included the majority of participating centers (44.2%). Obviously, this conforms with the fact that Abu Dhabi has been the first Emirate to start AMR surveillance, and it also is the largest Emirate in terms of area, where is occupies over 80% of the nation’s land. However, Dubai, rather than Abu Dhabi, is the most populated Emirate, and samples from Dubai residents accounted for a much lower 17% only of those analyzed in this study. As such, these results must be cautiously interpreted.

As shown in Table 1, the majority of recovered species belong to A. calcoaceticus-baumannii complex, which alone occupied 86.7% of the total sample size. The remaining proportion was formed collectively from all other species, with A. lwoffii and A. junii accounting for 4.6 and 2.2% of all isolates collected throughout the study period, in addition to other species. Ubiquitous Acinetobacter species were initially thought of as commensals that are non-pathogenic to immunocompetent subjects (49); globally, reports on hospital outbreaks caused by Acinetobacter spp. have been mostly linked to A. baumanni, which is the most virulent species (50). However, several species of these ubiquitous bacteria have emerged as core pathogens in hospitalized patients and fomites, and can cause life-threatening nosocomial infections in compromised hosts (51). The spread of antimicrobial resistance to these species has further increased concerns regarding them and placed them as a special risk (52), especially in the ICU (53–55). With over 15% of different non-baumannii species isolated throughout the duration of the study, this may shed a light on the presence and long-term maintenance of these strains among patients and, accordingly, the need for precise documentation and tight control of different factors responsible for their dissemination in the UAE.

A consistent minimum of about 70% of species were recovered from adult patients, while pediatric samples declined from 2016 till the end of the study to reach about 12%. Reports of resistant Acinetobacter infections in children in different hospital settings have been previously published (56–58), even in children under 1 year with community acquisition of A. baumanni in their upper respiratory tract (59). This indicates possible epidemiological insights into the existence of Acinetobacter not only in critical settings, but also in non-serious community-based infections in the pediatric population. An in-depth analysis of Acinetobacter infections in infants and children in the UAE has not been yet realized. However, the decreasing rates of infection since 2016 are interesting, and warrant a further focused exploration of the epidemiology and resistance patterns of Acinetobacter in this population.

Urinary and respiratory samples contributed to the largest collection of studied samples, with percentages of 33 and 29%, respectively, from the bulk collection of Acinetobacter. Although described as a cause of catheter-associated urinary tract infections (60), most of the literature has focused on Acinetobacter in pneumonia and bloodstream infections; nevertheless, its role as a uropathogen cannot be neglected (61), and its isolation in urine samples in this study warrants attention. The second most common clinical specimen was from the respiratory tract, and this is in parallel to evidence indicating Acinetobacter abundance in respiratory samples with an incidence from 13 to 68% (62). Of note, the proportion of outpatient samples was about 35%, shedding a light on Acinetobacter reservoirs outside hospital settings, where they can be culprits in community-acquired pneumonia, infections in survivors from natural disasters, and infected war wounds (63). The actual presence of this organism in various environmental locations and being transferred to patients in the community is not possible to confer from our findings and needs further attention.

Over the full duration of the study, the rates of resistance of Acinetobacter to all tested antibiotics did not increase beyond 50%. This is in contrast to a recent report from the Gulf region, where in KSA, a neighboring country, the rates of resistance to all antibiotic in A. baumannii was above 50%, except for gentamycin and colistin (28). Also, in Oman, the rates of A. baumannii resistance to different antibiotics ranged from 50 to 83% (64). Previously, some studies detected the molecular epidemiology of A. baumannii resistance in the region, like detection of OXA-23 and OXA-24 from isolates collected from the Gulf Cooperation Council countries (65), detection of OXA-23, NDM-1 and GES-11 in isolates from Dubai (33), and detection of MDR and XDR strains in Abu Dhabi (34). In this study, a follow-up of resistance trends to different antibiotics consistently at a nationwide level showed that the rates of resistance declined from 2011 to 2021. This was true for all tested β-lactam antibiotics, whose resistance declined from a range of 40–50% at the beginning of the study to 20–30% in the last 3 years of follow-up. For other antibiotic classes, the trends of resistance were more heterogeneous in the first few years (due to smaller sample size), but all declined toward the end of the study. Perhaps the statistically significant decline in imipenem, meropenem, and amikacin is one of the most interesting findings of this analysis, and warrants to investigate the positive practices in the UAE that culminated into such a result. Similarly, the proportions of MDR and possible XDR strains were almost reduced by half, indicating that some isolates have regained their sensitivity or at least ceased being nonsusceptible over the course of the follow-up years. The mild increase in the levels of MDR, possible XDR, and possible PDR strains toward the end of the study period may have been affected by the COVID-19, as reported elsewhere (66, 67), and was probably driven by high rates of antimicrobial utilization and disruption of infection control measures occurring as collateral effects of the global pandemic (68). It is worth mentioning that trends in Acinetobacter species resistance were reported to have similar declining portraits in other parts of the world. For instance, a national study from the US showed a decline in carbapenem resistance (from 43 to 36%), MDR prevalence (from 49 to 36%), and XDR prevalence (from 21 to 10%) from 2010 to 2018. Similar epidemiological data of resistance decline in Acinetobacter exist from KSA (69), Germany (70), and Brazil (71). Hence, the decrease in resistance trends in Acinetobacter in the UAE mirrors other resistance trend observations in the region and elsewhere, and emphasize the need for continuing infection control and stewardship efforts and the development of new therapeutic options. While the trends for antimicrobial resistance to some antibiotics showed a slight rise after 2019, probably associated with factors related to the COVID-19 pandemic (72), the tends remained lower than those observed at the beginning of the study.

Looking into some specific antibiotics and the decrease in resistance among the studied isolates, it is noticeable that, for instance, imipenem and meropenem resistance rates in 2021 were less than 30%. This is much lower than rates of resistance reported in nearby countries like Jordan, where carbapenem resistance rate in 2022 was 99% (73). Moghnieh and Colleagues (74), in their narrative review on resistant Gram-negative pathogens in the region also described rates of carbapenem resistance in Acinetobacter above 80% not only in Jordan, but also in Lebanon and Iraq. The rates of carbapenem resistance in other countries including Turkey, Greece, Italy, and Spain, are much higher, with reported incidences of 50–80, 85, 60, and 45%, respectively (75, 76). For antibiotics from the non-β-lactam class, the highest resistance rates in 2021 were for tetracycline and ciprofloxacin, but both showed rates below 30%. This is in contrast to higher rates observed in Iran (tetracycline resistance 86%) (77), Egypt (ciprofloxacin resistance 42%) (78). However, the rates in this study were higher than those observed in Pakistan for ciprofloxacin (2.5%) and close to those for tetracycline (25%) (79). There are positive insights from the decline in resistance observed over the study duration, and comparison to other data from other countries reveals diverse resistance rates. However, the observed decline does not preclude the need for ongoing surveillance of Acinetobacter infections and continued assessment of effective prevention strategies, to build on the observed resistance mitigation for future attainments.

The two antibiotics tigecycline and colistin remained effective throughout the study period. According to previous evidence (80–84), combinations of these two antibiotics or combination of at least one of them with a third antibiotic have been used in treatment of MDR Acinetobacter infections, with variable success. However, both antibiotics remain among the most effective antimicrobial agents against Acinetobacter isolates in vitro (85), and their value needs to be preserved. As such, antimicrobial usage and consumption surveillance should aim at monitoring the use of colistin and tigecycyline, in presence of reports indicating resistance in Acinetobacter mainly mediated by the tet(X) gene against tigecycline (86, 87), and by the loss or modification of lipopolysaccharide or plasmid-encoded mcr genes against colistin (88, 89). The preservation of effectiveness of these two antibiotics in the UAE during this study, albeit with some rise in colistin resistance in 2018 and 2020, should provide an exemplar on maintaining the effect of last-resort antibiotics in clinical settings of high resistance.

Nevertheless, the mortality rate, according to our observations, was about 5.7-fold higher in patients infected with CRAB compared to those infected with non-CRAB Acinetobacter spp. Patients with an infection associated with CRAB were 3.3-fold more likely to be admitted to ICU, and their median length of stay was increased by 13 days, as compared to patients with non-CRAB infections. This is consistent with other findings that indicated high mortality rate and poor outcomes in patients with CRAB (90, 91) and highlights need for surveillance and control for better health outcomes.

This 12-year follow-up of the resistance trends in Acinetobacter species in the UAE indicated a decline in antimicrobial resistance and in proportions of Acinetobacter isolates with MDR and XDR profiles. The useful surveillance techniques, infection control strategies, and stewardship implemented over this span of time should be all reinforced. Further to these findings, continued epidemiological enquiry and genetic evolution analysis of Acinetobacter are required, to sustain the observed decline in resistance and to provide new strategies for prevention and control.

The datasets presented in this article are not readily available because the National AMR Surveillance database managed by the UAE Ministry of Health and Prevention (MOHAP) contains confidential health information. Requests to access the datasets should be directed to https://mohap.gov.ae/.

Ethical approval for this study was provided by the Ministry of Health and Prevention Research Ethics Committee (MOHAP/DXB-REC/ D.D.D/No.131 / 2021; MOHAP/DXB-REC/J.J.J./No. 86/2023), Dubai Scientific Research Ethics Committee (DSREC-GL17-2023), and Abu Dhabi Health Research and Technology Ethics Committee (DOH/ZHCD/2023/1316).

CM, JT, NA, HA, DE, AS, and GM: conceptualization. JT, CM, NA, HA, DE, AS, GM, and The UAE AMR surveillance consortium: data collection. JT and CM: formal analysis. JT, CM, NA, HA, DE, AS, GM: data interpretation. CM and JT: manuscript preparation. CM, JT, NA, HA, DE, AS, and GM: manuscript review and editing. All authors contributed to the article and approved the submitted version.