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Analysis of risk factors and different treatments for infections caused by carbapenem-resistant Acinetobacter baumannii in Shaanxi, China

BMC Infectious Diseases volume 24, Article number: 1130 (2024) Cite this article

Abstract

Background

The global threat of Carbapenem-resistant Acinetobacter baumannii (CRAB) has intensified as resistance to carbapenems continues to rise in recent decades. We aimed to explore risk factors, molecular epidemiology, and antimicrobial therapy of CRAB infection.

Methods

The clinical data of 110 patients infected with A. baumannii from December 2021 to December 2022 were retrospectively analyzed. Patients were divided into a carbapenem-resistance group (55 patients) and carbapenem-sensitive group (CSAB; 55 patients) based on resistance to carbapenem, and the risk factors of patients infected with CRAB were analyzed. Fifty-five patients with CRAB infection who received antimicrobial therapy were divided into a combination therapy group (45 patients) and a monotherapy group (10 patients), and differences between the two groups were compared. Whole-genome sequencing analysis was performed to assess resistance genes. Phylogenetic analysis was performed to explore the characteristics of CRAB isolates.

Results

Among the total 110 patients, the rate of poor prognosis in the CRAB group was 43.6% (24/55). Mechanical ventilation (odds ratio [OR] = 5.364, 95% confidence interval [CI] 1.462–19.679, P = 0.011) and puncture (OR = 19.935, 95% CI 1.261–315.031, P = 0.012) were independent risk factors for CRAB infection. Of 55 patients in the antimicrobial regimen study, 45 received combination therapy (including dual, triple, or quadruple antibiotic therapy) and 10 received monotherapy. Univariate analysis revealed significant differences between the combination group and monotherapy group for admission to the intensive care unit and wound infection (P < 0.05). The CRAB strains of 26 patients taking carbapenem-based combination therapy were mainly ST208, ST1968, and ST195, among which patients with ST1968 strains had higher 28-day mortality. Furthermore, the blaOXA−23 gene was harbored in ST1968, ST195, and ST208.

Conclusions

Mortality was significantly higher in patients infected with CRAB than with CSAB. Mechanical ventilation and puncture were independent risk factors in predicting CRAB infections. The distribution of CRAB was dominated by ST208, ST1968, and ST195, among which patients with ST1968 had higher 28-day mortality. The blaOXA−23 gene appears to be widely disseminated.

Peer Review reports

Introduction

Acinetobacter baumannii has become an important opportunistic pathogen that is widespread in hospitals and other healthcare settings [1]. The bacterium normally colonizes on the surface of the skin, mucosa, throat, and respiratory tract, causing severe infections including bloodstream infections, respiratory infections, skin and soft tissue infections, urinary tract infections, and meningitis [2, 3]. A. baumannii has spread rapidly worldwide, and 50-70% of all clinical isolates are multidrug resistant (MDR) [4]. Carbapenems have been known as last-resort antibiotics for A. baumannii infection, However, carbapenem-resistant A. baumannii (CRAB) has spread globally, and the positive rate observed during clinical screening has continually increased in recent decades [5]. In 2019, the Centers for Disease Control and Prevention (CDC) recognized carbapenem-resistant Acinetobacter as an “urgent threat” and a top priority because of the limited options for treatment [6]. Clinical selection and dissemination of CRAB constitute a serious threat, as the mortality rates from infections caused by such strains are high, often exceeding 50% [7].

Several studies have demonstrated that inappropriate empirical antibiotic therapy is a factor associated with increased mortality due to infections caused by CRAB [8, 9]. Therefore, early recognition of risk factors for CRAB infection is important to provide adequate antibiotics. Previous studies have identified some risk factors associated with CRAB infection such as history of previous antibiotics use, history of prolonged hospital stay, and use of a central venous catheter or drainage catheter [10,11,12]. Nevertheless, risk factors associated with the clinical characteristics and outcomes of CRAB could be affected by CRAB prevalence, differences in clinical practice, and antibiotic prescribing habits [13]. A study indicated that carbapenems combined with other antibiotics were the main option for treating infections caused by CRAB, which have strong antibacterial activity [14, 15], but clinical studies are still lacking in China.

In the present study, patients with CRAB infection in a tertiary teaching hospital in China were retrospectively analyzed to investigate the risk factors and molecular epidemiology of CRAB infection as well as the influence of the choice of antibiotic regimen on the patient prognosis.

Materials and methods

Study population and design

This study was conducted at the Hanzhong Central Hospital, a 2200-bed teaching hospital (Hanzhong, China), from December 2021 to December 2022. The inclusion criteria of A. baumannii-induced infection were positive culture for A. baumannii; clinical signs consistent with infection; infection occurred ≥ 48 h after hospital admission. Only the first episode was included if the patient had multiple episodes of A. baumannii infection. Patients who lacked medical records or insufficient data and those who were discharged against medical advice were excluded.

In this study, patients infected with A. baumannii were divided into two groups according to their sensitivity to imipenem: the carbapenem-resistant Acinetobacter baumannii (CRAB) group (55 patients) and carbapenem-sensitive Acinetobacter baumannii (CSAB) group (55 patients). Differences between the two groups were compared, and the risk factors of CRAB infection were analyzed. Fifty-five patients with infection caused by CRAB were divided into two groups according to the types of antimicrobial agent used in treatment: the monotherapy group (10 patients) and the combination therapy group (45 patients); differences between the two groups were compared. Combination therapy was defined as the use of two or more antimicrobial agents active against gram-negative bacilli within 48 h of in vitro susceptibility results. The duration of antibiotics use in all treatments should be at least 48 h.

Strain identification and antimicrobial susceptibility testing

Patient samples were routinely collected from the Hanzhong Central Hospital, and clinical samples were taken as part of normal medical practice. Samples were cultured on blood agar at 37 °C for 24–48 h. Bacterial identification was performed using matrix-assisted laser desorption ionization time-of-flight mass spectrometry (Bruker Corp., Billerica, MA, USA) and verified by genome sequencing. The bacteria isolates were cryopreserved in Luria Bertani (LB) broth (BD Difco, Franklin Lakes, NJ, USA) with 20% (v/v) glycerol at -80 °C. A. baumannii were subjected to antimicrobial susceptibility testing by broth microdilution for the following antimicrobial agents: piperacillin/tazobactam, ampicillin/sulbactam, ceftazidime, cefotaxime, cefepime, meropenem, imipenem, amikacin, gentamicin, ciprofloxacin, levofloxacin, cotrimoxazole, polymyxins, and tigecycline. The results were interpreted according to Clinical and Laboratory Standards Institute (CLSI) 2022 guidelines and the US Food and Drug Administration breakpoints (minimum inhibitory concentration MIC ≤ 2 mg/L for susceptibility and MIC ≥ 8 mg/L for resistance) for tigecycline against A. baumannii [16]. Escherichia coli (ATCC 25922) and Pseudomonas aeruginosa (ATCC 27853) were used as the quality control strains for both species identification and antimicrobial susceptibility testing. MDR A. baumannii was defined as acquired non-susceptible to at least one agent in three or more antimicrobial categories [17]. All these strains were stored at -80 °C for further investigation.

Whole-genome sequencing and analysis

Genomic DNA was extracted using a Qiagen minikit (Qiagen, Hilden, Germany) in accordance with the manufacturer’s instructions. Whole-genome sequencing (WGS) of CRAB was performed using the Illumina HiSeq platform (Illumina, San Diego, CA, USA) and the MinION platform (Nanopore, Oxford, UK). De novo assembly of reads was performed using Unicycler v0.4.8 [18]. The quality of the assembly sequence was checked using QUAST v5.0.2 [19]. Antibiotic resistance genes were queried using the ResFinder database at the Center for Genomic Epidemiology (http://www.genomicepidemiology.org/, accessed 19 December 2023) [20]. Pasteur and Oxford multilocus sequence typing (MLST) schemes were performed via PubMLST (https://pubmlst.org/) [21]. A phylogenetic tree was constructed using core genes identified among 26 CRAB strains. To ensure consistent gene calling in all genomes, all genomes used in the phylogenetic analysis were annotated using Prokka v1.13 [22]. Core genes were identified using Panaroo v1.1.2 with the alignment option set to “core” [23]. The core gene alignment generated by Panaroo was input into FastTree for phylogenetic tree reconstruction, and the resulting tree was visualized using iTOL v6 (https://itol.embl.de/) [24].

Statistical analyses

Continuous variables that were normally distributed were compared using an independent-sample t test. Categorical variables were analyzed using the chi-squared test or Fisher’s exact test. Univariate analysis was performed for each risk factor to determine the odds ratio (OR) and 95% confidence interval (CI). In univariate analysis, all biological variables with a P value < 0.05 were included in multivariate logistic regression analysis. All biological variables with a two-tailed P value < 0.05 were considered statistically significant. All data were analyzed using IBM SPSS v. 20.0.

Results

Risk factors associated with CRAB infection

According to univariate analysis, the age of patients with CRAB infection (59.9 ± 16.8 years) was significantly different from that of patients in the CSAB (60.0 ± 26.4 years; P < 0.05). Among the total 110 patients, 73 were male, accounting for 66.4%. The number of cases of cerebrovascular accident in the CRAB group (49.1%, 27 cases) was higher than that in the CSAB group (18.2%, 10 cases), and there were fewer chronic heart disease cases (7.3%, 4 cases) in the CRAB group than in the CSAB group (32.7%, 18 cases), with statistical significance (P < 0.05). However, there was no significant difference between the CRAB and CSAB groups in terms of patients with chronic diseases such as hypertension, diabetes, cancer, kidney disease, liver disease, and respiratory system disease. There were more cases of catheter, puncture, mechanical ventilation, central venous catheter, nasogastric tube intubation, and pulmonary artery catheter in the CRAB group than those in the CSAB group, with statistical significance (P < 0.05). However, there was no statistically significant difference in terms of surgical operations between the two groups. The proportion of ICU admissions was higher in the CRAB group (50.9%, 28 cases) than in the CSAB group (29.1%, 16 cases), and the difference was statistically significant (P < 0.05). In terms of patient prognosis, the number of deaths in the CRAB group (29.1%, 16 cases) was higher than that in the CSAB group (3.6%, 2 cases), and there were fewer cured cases (56.4%, 31 cases) than in the CSAB group (78.2%, 43 cases), with statistical significance (P < 0.05) (Table 1).

Table 1 Univariate analysis of risk factors for carbapenem-resistant Acinetobacter baumannii infection
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Independent predictors of CRAB infection

According to multivariate logistic regression analysis, mechanical ventilation and puncture were independent risk factors for CRAB infection (P < 0.05) (Table 2).

Table 2 Multivariate analysis showing risk factors for carbapenem-resistant Acinetobacter baumannii infection
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Antibacterial therapy for patients with CRAB infection

Patients with CRAB were divided into the combination therapy group and the monotherapy group according to the types of antimicrobial agents used in treatment. The 28-day mortality for the two groups in total was 29.1% (16/55), among which 14 patients died in the combination therapy group (31.1%, 14/45) and 2 patients died in the monotherapy group (20.0%, 2/10). Univariate analysis revealed statistically significant differences between the two groups for ICU admission and wound infection (P < 0.05), as shown in Table 3. Among the 45 patients who received a combination therapy of antibiotics, 26 received dual antibiotic therapy, 11 received triple antibiotic therapy, and 8 patients received quadruple antibiotic therapy. Combination therapy based on carbapenems (26 cases) was the most common combination drug regimen in this study, with a 28-day mortality of 24.4% (11/45). The specific drug regimens are shown in Table 4. Ten patients received monotherapy, including two receiving carbapenems, three on piperacillin-tazobactam, two receiving cefoperazone-sulbactam, two taking third-generation cephalosporins, and one patient on fluoroquinolones.

Table 3 Characteristics of patients with carbapenem-resistant Acinetobacter baumannii infection in terms of antimicrobial regimen
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Table 4 Outcomes of 26 patients with carbapenem-resistant Acinetobacter baumannii infection treated with a carbapenem-based regimen
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In this study, the MIC value of imipenem was analyzed for patients taking carbapenem-based combination therapy. The results showed that a total of 26 patients with CRAB infection were treated with carbapenem-based combination treatment. Among them, the imipenem MIC of 20 patients was ≥ 32 mg/L, and the 28-day mortality was 45.0%; the imipenem MIC of five patients was 16 mg/ L, with a 28-day mortality of 40.0%. One patient with imipenem MIC ≤ 8 mg/L had a 28-day survival rate of 100% (Table 5).

Table 5 The 28-day survival of 26 patients with carbapenem-resistant Acinetobacter baumannii infection treated with carbapenem-based combination therapy in terms of imipenem MIC
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Molecular epidemiology

We conducted WGS to assess the sequence type (ST) of 26 CRAB strains. These could be categorized into three ST types according to Oxford MLST schemes, among which ST208 was the most dominant with 14 strains (53.8%), followed by ST1968 with 8 strains (30.8%) and ST195 with 4 strains (15.4%). Based on the high resolution of the genome sequence, cgMLST was used to analyze the phylogenetic relationships of these CRAB strains. Strains with ST208 were divided into two clades, and the 28-day mortality of patients with ST208 strains was 15.4% (4 patients). ST195 contained four CRAB strains, and the 28-day mortality was 7.7% (2 patients). ST1968 contained eight CRAB strains, with a 28-day mortality of 19.2% (5 patients).

Resistome analysis

All A. baumannii isolates harbored intrinsic blaOXA−51−like genes, including blaOXA−66 and blaOXA−80. The blaOXA−23 gene was mainly responsible for carbapenem resistance, and it was present in 19 isolates. Another β-lactamase gene was co-harbored, such as blaTEM−12, blaADC−30, and blaADC−73. Moreover, 17/26 isolates harbored armA, which is responsible for high-level resistance against aminoglycosides. Aminoglycoside-modifying enzymes that commonly mediate low- or medium-level resistance to aminoglycosides, such as ant(3’’)-IIa, aph(3’)-Ia, aph(3’’)-Ib, aph(6)-Id aadA1, aac(3)-Ia and aac(6’)-Ib, were detected in all isolates. Among other antimicrobial resistance genes, we also screened the macrolide resistance genes mph(E) and msr(E), sulphonamide resistance genes sul1 and sul2, tigecycline resistance gene tet(B), and phenicol resistance gene catB8 (Fig. 1).

Fig. 1
figure 1

Phylogenetic tree of 26 carbapenem-resistant Acinetobacter baumannii strains. The characteristics of each strain are shown, including sequence type, carbapenem resistance gene, and prognosis

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Discussion

A. baumannii is a major hospital-acquired pathogen that causes various nosocomial infections [1]. According to the China Antimicrobial Resistance Surveillance Network (CHINET) program, the resistance rate of A. baumannii to imipenem and meropenem increased to 62.8% and 59.4% in 2013 and to 71.2% and 71.9% in 2022, respectively (http://www.chinets.com/). According to the World Health Organization, CRAB has recently become the most critical pathogen for public health, topping the global priority list of antibiotic-resistant bacteria [25].

In this study, the mortality rate in patients infected with A. baumannii was 16.4%, and the rate of poor prognosis was 32.7%. Mortality in the CRAB group was 29.1% and that in the CSAB group was 3.6%, with a statistically significant difference (P < 0.05). The poor prognosis rate was 43.6% in the CRAB group and 21.8% in the CSAB group, with a significant difference (P < 0.05). Similar to other studies [5, 26], we demonstrated that patients with CRAB infection have a worse prognosis than those with CSAB infection.

CRAB infection mostly develops in patients with severe underlying disease, immunodeficiency, and/or repeated long-term use of broad-spectrum antimicrobial agents and is associated with poor clinical outcomes. Several clinical studies have also suggested that the mortality risk factors associated with poor prognosis include older age, severity of the underlying disease, septic shock, previous surgery, mechanical ventilation, and inappropriate antimicrobial treatment [27,28,29]. Previous studies have identified several risk factors related to infections caused by CRAB, revealing that ICU admission, ventilator or central venous catheter use, and the presence of diabetes mellitus are more common in infections caused by CRAB than CSAB [12, 13, 30]. In the present study, the CRAB group was compared with the CSAB group, and the results showed that mechanical ventilation and puncture were independent risk factors for CRAB infection. Invasive procedures can alter the site of bacterial colonization to some extent, such as, invasive operations damage the body’s natural barrier, which increased chance of infection and patient mortality [31]. Regarding of this study; 74.5% of patients in the CRAB group had a history of mechanical ventilation, during mechanical ventilation, might damage airway epithelial cells, compromising the natural defense function of the body and increasing the risk of pathogen adhesion and colonization, hindering the effective penetration of some antibacterial drugs and increasing the risk of CRAB infection [32]. In addition, we found that the age of patients in the CRAB group was younger than that in the CSAB group, and the difference between the two groups was statistically significant (P < 0.05). This result deviates from other research reports, which suggest that the CRAB infection rate increases with age, possibly due to a weakened immune system in elderly people, the common occurrence of more diseases, a long hospitalization course, and the high incidence of nosocomial infection [33]. The results of this study may be attributed to the fact that a higher proportion of patients in the CRAB group had undergone invasive operations, leading to their infection with drug-resistant bacteria that exist in the medical environment. No difference in sex was observed between the CRAB group and the CSAB group. But the incidence of male patients infected with A. baumannii is higher than that of female patients, which is consistent with the results of many studies [10, 27]. The cause of this phenomenon is not yet clear and further research is needed.

CRAB are typically multidrug-resistant strains that are usually sensitive to tigecycline and polymyxins [34]. For infections caused by MDR Acinetobacter strains, efficacious treatment is limited, antimicrobial monotherapy usually does not have satisfactory efficacy. Whereas the combination antimicrobial therapy is used in most cases. Some studies reported that combination antimicrobial therapy should be given as a priority treatment for MDR A. baumannii infection, which can appropriately reduce the dosage of drugs, reduce the probability of adverse drug reactions, and help prevent the rise of bacterial drug resistance [35]. A large retrospective study performed across 27 Turkish hospitals [35] revealed that the in-hospital mortality rate in the group taking combination therapy was significantly lower, and the microbial eradication rate was significantly higher than that of the monotherapy group. However, we found no significant difference between groups receiving combination therapy and monotherapy in terms of 28-day mortality. Some studies have reported that combination therapy does not significantly improve survival compared with monotherapy, and this result supports the same conclusion [10]. The results of this study may be related to the fact that the proportion of patients admitted to the ICU in the combination group was significantly higher than that in the monotherapy group. Most patients admitted to the ICU have serious underlying diseases, compromised immune function as well as, have undergone invasive procedures like mechanical ventilation resulting in more complicated conditions among ICU patients that are more difficult to cure. This could have led to an increase in the 28-day mortality of our patients in the combination group.

Due to the long time needed to culture clinical samples, doctors usually use or change antibacterial drugs according to patients’ symptoms and other auxiliary examinations. Several clinical studies have suggested that carbapenems in combination with other antimicrobial agents are associated with better efficacy against infections with carbapenem-resistant gram-negative bacilli than carbapenem monotherapy or other antimicrobial combinations [34, 36,37,38]. In this study, the most common drug combination regimen involved combinations of carbapenem-based drugs. Therefore, the MIC value of carbapenems was analyzed in 26 patients who received a combination of carbapenem-based drugs. The results indicated that the higher the MIC value of carbapenem antibiotics, the lower the efficacy of carbapenem-based drug combinations, and the higher the 28-day mortality. This is similar to the results of a study by Daikos et al. [36]. In addition, the CRAB strains collected from these 26 patients mainly comprised ST208, ST1968, and ST195, which is similar to the results reported by Gu et al. [5]. Besides, ST208, ST1968 and ST195 belonged to clonal complex (CC) 92, which is the largest and most geographically diverse CC, and is widespread in many countries [39]. The results of this study showed that patients infected with ST1968 CRAB had higher 28-day mortality, which might be attributed to drug-resistance genes and virulence factors carried by this particular strain of CRAB [10].

Concerning this study, CRAB isolates harbored multiple resistance determinants, among which oxacillinase genes were common. The blaOXA-type enzymes related to carbapenem resistance include natural blaOXA51-like and three acquired genes: blaOXA-23-like, blaOXA-24-like, and blaOXA-58-like [40]. The enzymes of the blaOXA-51 cluster are naturally occurring enzymes in A. baumannii, given their chromosomal location, and oxacillinase expression does not mediate carbapenem resistance. However, the presence of the insertion sequence IS Aba1 upstream of the blaOXA-51-like gene may act as a promoter leading to overproduction of carbapenemase and resulting in carbapenem resistance [41]. The blaOXA-23 gene has contributed to increasing carbapenem resistance in A. baumannii worldwide and is the most commonly acquired gene associated with carbapenem resistance in China [42]. To our knowledge, the blaOXA-23 gene is mobilized by Tn2006, Tn 2007, Tn2008, and Tn2009, and dissemination of the blaOXA-23 gene is caused by transposons [43,44,45]. In this study, the blaOXA-23 gene was harbored in three different STs (ST1968, ST195, and ST208, respectively). Thus, it seems that the blaOXA-23 gene has been widely disseminated by transposons.

There are some limitations to this study: the patient data was collected from a single center, so the conclusions do not represent the overall situation in this region, and it was a retrospective study, which is prone to bias, and the sample size was relatively small. In the future, our conclusions will be further validated in a larger multicenter study with a larger sample size.

Conclusion

Our data suggest that the patients infected with CRAB have a higher mortality rate. Mechanical ventilation and puncture were found to be independent risk factors for CRAB infection. There were no significant differences in 28-day mortality owing to CRAB infection between the combination group and the monotherapy group under different antimicrobial therapy regimens. There is widespread dispersion of the blaOXA–23 gene, and the common sequence types were ST208, ST1968, and ST195 among CRAB isolates. In patients with CRAB infection bearing ST1968 strains, 28-day mortality was higher.

Data availability

Sequence data that support the findings of this study have been deposited in the National Center for Biotechnology Information with the primary accession code PRJNA1068792.

Abbreviations

CRAB:

Carbapenem-resistant Acinetobacter baumannii

CSAB:

Carbapenem-sensitive Acinetobacter baumannii

OR:

Odds ratio

CI:

Confidence interval

ST:

Sequence type

MDR:

Multidrug resistant

CLSI:

Clinical and Laboratory Standards Institute

MIC:

Minimum inhibitory concentration

WGS:

Whole-genome sequencing

MLST:

Multilocus sequence typing

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Acknowledgements

We thank LetPub (www.letpub.com) for its linguistic assistance during the preparation of this manuscript.

Funding

This study was supported by the Natural Science Basic Research Program of Shaanxi (No. 2022JQ-974).

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Authors and Affiliations

  1. Department of Clinical Laboratory, Hanzhong Central Hospital, 22 Kangfu Road, Hanzhong, Shaanxi, People’s Republic of China

    Xiaoliang He, Jin Tang, Sanjun He & Xiaoxia Huang

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  1. Xiaoliang He
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  2. Jin Tang
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  3. Sanjun He
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  4. Xiaoxia Huang
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Contributions

XXH contributed to the study conception and design. Material preparation, data collection, and analysis were performed by XLH, JT, and SJH. The manuscript was written by XLH. All authors read and approved the final manuscript.

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Correspondence to Xiaoxia Huang.

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Ethics approval and consent to participate

This work was approved by the Ethics Committees of Hanzhong Central Hospital (2023026). The ethics committee waived the need for written informed consent provided by participants due to the retrospective nature of this study. The study followed the principles outlined in the Declaration of Helsinki.

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He, X., Tang, J., He, S. et al. Analysis of risk factors and different treatments for infections caused by carbapenem-resistant Acinetobacter baumannii in Shaanxi, China. BMC Infect Dis 24, 1130 (2024). https://doi.org/10.1186/s12879-024-10036-5

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Keywords

BMC Infectious Diseases

ISSN: 1471-2334

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