Dhanapal B, Risha M, Saikumar C. Emerging Drug Resistance in Acinetobacter species: A Study on Isolation, Speciation, and Antimicrobial Susceptibility Patterns in a Tertiary Care Hospital. Biomed Pharmacol J 2025;18(2).

---

Manuscript received on :14-10-2024
Manuscript accepted on :28-04-2025
Published online on: 21-05-2025

---

Plagiarism Check: Yes
Reviewed by: Dr. Satnam Singh
Second Review by: Dr. Baby Mittal
Final Approval by: Dr. Patorn Piromchai

---

How to Citeclose    |   Publication History close

 Views: 

Visited 682 times, 1 visit(s) today

 

 PDF Downloads: 

381

Bindu Dhanapal^*, Mymoonah Risha and Chitralekha Saikumar

Department of Microbiology, Sree Balaji Medical College and Hospital, Chrompet, Chennai, Tamilnadu, india.

Corresponding Author E-mail: mail2bindhu@rediffmail.com

DOI : https://dx.doi.org/10.13005/bpj/3194

Abstract

Acinetobacter species are emerging pathogens in healthcare settings, responsible for many infections, including bacteremia, pneumonia, meningitis, peritonitis, and wound infections. Their ability to develop multidrug resistance through various resistance determinants poses significant challenges for treatment. This study aimed to isolate and speciate Acinetobacter using simple phenotypic tests, determine their antibiotic susceptibility profiles, and conduct molecular characterization of resistance genes. This prospective cross-sectional study was conducted from January 2023 to December 2023 to isolate and identify Acinetobacter isolates from confirmed infections using phenotypic methods, followed by antibiotic susceptibility testing. Among 108 confirmed cases of Acinetobacter infection, 73 were male patients, 49 were over 50 years old, and 49 were from the Intensive Care Unit (ICU). The most common specimens were endotracheal aspirates (36.1%) and sputum (34.2%). Levofloxacin and meropenem were the most effective antibiotics, with 81.5% sensitivity each, while ceftriaxone (81.4%), gentamicin (71.3%), cefepime (77%), and ceftazidime (70.3%) exhibited high resistance rates.All the isolates were sensitive to colistin and tigecycline.  In terms of speciation, Acinetobacterbaumannii was predominant, accounting for 97.2% of isolates. Notably, Acinetobacter species were more frequently isolated from ICU patients (38%) than other wards. These findings underscore the critical need for vigilant infection control practices and tailored antibiotic stewardship programs in healthcare settings.

Keywords

Acinetobacterbaumannii; Acinetobacter infections; Antibiotic susceptibility test; Colistin; Ceftazidime-avibactam+aztreonam; ICU; MDR; Synergistic effect

Introduction

Acinetobacter species, particularly Acinetobacter baumannii(A .baumannii), have emerged as significant pathogens in both community and healthcare settings. These bacteria are highly adaptable and able to survive on both dry and moist surfaces, which allows them to persist in hospital environments and cause a variety of opportunistic infections. These infections range from pneumonia, often associated with endotracheal tubes, to bacteremia, meningitis, urinary tract infections, endocarditis, and wound and soft tissue infections.¹ Various risk factors contribute to these infections, including climatic conditions, diabetes mellitus, smoking, alcohol use, and chronic obstructive pulmonary disease (COPD).²

Globally, the prevalence of A. baumannii infections is increasing, particularly in hospital settings.³ The World Health Organization (WHO) has classified carbapenem-resistant A. baumannii as one of the most critical antibiotic-resistant pathogens.⁴ The prevalence rates of multidrug-resistant (MDR) A. baumannii are particularly concerning, with studies indicating that resistance rates are 65% to 80% in many countries worldwide.⁵

In India, the situation is particularly dire, with studies showing a significant rise in A. baumannii infections.  According to Systemic review studies, the prevalence rate of MDR species ranges from 8.9 % to 73.2 % in different healthcare settings.^6,7

This rise in resistance is largely due to factors such as the overuse and misuse of antibiotics, inadequate infection control practices, and the absence of stringent antibiotic stewardship programs.  Even more concerning is the growing resistance to colistin, an antibiotic often used as a last resort. Studies indicate that the global resistance to colistin is around 4%, and similar trends are being observed in India, further limiting the treatment options for these infections. In response to the high level of antibiotic resistance and the variability in resistance profiles across different geographical areas, this study aims to achieve objectives such as (1) to isolate and identify the various Acinetobacter species  2)  to determine the antibiotic susceptibility profiles of Acinetobacter species, focusing on understanding the resistance patterns to critical antibiotics such as carbapenem, colistin, and other commonly used antibiotics 3) to investigate the synergistic effects of ceftazidime-avibactam and aztreonam combination therapy using the E-strip method.

Materials and Methods

Study Design and Sample Collection: This study was a prospective cross-sectional study conducted in a tertiary care center in the Department of Microbiology over a year (January 2023 to December 2023). The study was approved by our Institutional Human Ethics Committee (SBMCH/002/SBMCH/IEHC/1828).

Sample Types and Collection

Clinical samples such as blood, pus, wound swabs, endotracheal (ET) aspirates, bronchoalveolar lavage (BAL), and sputum were collected from different wards within the hospital. Around 108 non-duplicate Acinetobacter isolates were isolated from the clinical samples.

Isolation

The samples collected were processed using standard microbiological techniques. Initially, the samples inoculated onto appropriate culture media, such as MacConkey agar (Hi media), blood agar (Hi media), and Nutrient agar (Hi media).⁸

Identification by Standard Biochemical Test

Once the colonies suspected to be Acinetobacter were isolated, they were identified using Gram Staining and standard biochemical tests. Common biochemical tests for Acinetobacter include oxidase, catalase, motility, carbohydrate utilization test, oxidation of glucose, beta hemolysis at 37°C and 42°C, and arginine hydrolysistests.⁹ These tests help differentiate Acinetobacter from other Gram-negative bacilli.

Confirmation of Species by Vitex-2MALDI-TOF

The isolates were chosen and smeared over the sample locations on the target slide using loops. After that, the sample was covered with 1 μ of VITEK MS-CHCA matrix, and it was allowed to air dry until the matrix and sample co-crystallized. The VITEK MS (BioMérieux) system was then used to load the target slide containing all of the prepared samples to obtain the mass spectra of each sample’s entire bacterial cell protein, primarily ribosomal protein.In the end, the mass spectra obtained for every sample were compared to those already known and recorded in the database. Based on how well the collected spectra matched the mass spectra in the database, a confidence score was assigned.¹⁰

Kirby-Bauer Disk Diffusion Method

The antibiotic susceptibility of the isolated Acinetobacter strains was determined using the Kirby-Bauer disk diffusion method. This method involves placing antibiotic-impregnated paper disks on an agar plate inoculated with the isolated bacteria. The antibiotics used were:Gentamicin (30 μg) (Himedia), Amikacin (30 μg) (Himedia), Ciprofloxacin (5 μg) (Himedia), Levofloxacin (5 μg) (Himedia), ceftazidime (μg) (Himedia), Ceftriaxone (30 μg) (Himedia), Cefepime (30 μg) (Himedia), Piperacillin-tazobactam (100/20 μg) (Himedia), Meropenem (30 μg) (Himedia). After incubation, the zone of inhibition around each disk is measured to determine the susceptibility of the bacteria to each antibiotic.The interpretation was made using CLSI guidelines 2023.¹¹

Minimum Inhibitory Concentration (MIC) Determination

The MIC for colistin and tigecycline was determined using the VITEK-2 system (Biomerieux) using AST Card 406.

Detection of Ceftazidime-Avibactam and Aztreonam synergy using E strip

This method was done for only 5 MDR Acinetobacter strains isolated from ICU patients. Lawn cultures ofMDR Acinetobacter were done on the Mueller Hinton agar plate, and aztreonam-containing E-test strips were placed and diffused. The first E-test strip (Aztreonam) was removed after 10 minutes of incubation. The Ceftazidime-Avibactam E-strip was placed over the impression of the Aztreonam E-strip. The aztreonam strip was again placed over the ceftazidime/avibactam strip by gradient stacking. Then it was incubated for 16–18 hours after which the MIC value was noted.¹²

Results

A total of 108 non-duplicate Acinetobacter isolates were obtained from various clinical samples. Of these, 103 (95.3%) were identified as Acinetobacter baumannii and 5 (4.6%) as Acinetobacter lwoffii (Figure 1). The distribution of isolates across wards showed that ICU patients contributed the highest number of isolates (42.59%, 46/108), followed by the surgical (19.4%, 21/108) and medical (15.7%, 17/108) wards (Table 1). The Acinetobacter infections were more prevalent in male patients (67.6%) compared to females (32.4%), as shown in Table 2.

Figure 1: Species-wise distribution of Acinetobacter spp.,Click here to view Figure

Table 1: Department-wise distribution of the Acinetobacter species isolates

Table 2: Risk factor analysis

Age Distribution

The majority of patients with Acinetobacter infections were over 50 years old (37.9%, 41/108), followed by those aged 41-50 (10.2%, 11/108), and 31-40 (9.25%, 10/108) (Table 3). Only 0.9% of isolates were from patients aged 1-10 years, indicating that older adults were significantly more affected by these infections.

Table 3: Age-wise distribution of Acinetobacter isolates

Gender Distribution by Sample Type

Table 4 highlights the gender-specific distribution of isolates from different sample types. Endotracheal (ET) aspirates yielded the highest number of isolates (36.1%, 39/108), with 30 from male patients and 9 from females. Sputum samples were the second most common source (34.2%, 37/108), with 24 from males and 13 from females. Pus samples accounted for 21.3% (23/108) of isolates, showing a similar gender trend, while blood and bronchoalveolar lavage (BAL) samples contributed to a smaller percentage of the isolates.

Table 4: Gender-wise distribution of the Acinetobacter spp., isolates in different samples

Duration of Hospitalization and Co-morbid Illness

Patients hospitalized for more than 7 days represented 54.6% (59/108) of the total cases, indicating that prolonged hospital stays were associated with a higher incidence of Acinetobacter infections (Table 2). Additionally, 54.6% of the patients had comorbid illnesses, further suggesting that Acinetobacter infections are more prevalent in patients with pre-existing health conditions.

Antibiotic Susceptibility Test

Antibiotic resistance patterns revealed significant resistance to commonly used antibiotics. Resistance rates for cephalosporins (cefepime, cefotaxime, ceftazidime) ranged from 70.3% to 81.4%, while 71.3% of isolates were resistant to gentamicin, and 77% were resistant to cefepime (Figure 2). Ciprofloxacin and amikacin also exhibited high resistance rates at 62% and 68%, respectively. In contrast, levofloxacin and meropenem demonstrated the highest sensitivity, with 81.5% of isolates susceptible to these antibiotics. Notably, all isolates were sensitive to colistin and tigecycline, making them the most reliable options for treating Acinetobacter infections in this study.

Figure 2: Antibiotic sensitivity pattern of Acinetobacter isolatesClick here to view Figure

Synergy Testing

The results of synergy testing with ceftazidime-avibactam and aztreonam (Figure 3) were encouraging, as all tested multidrug-resistant (MDR) isolates showed reduced minimum inhibitory concentrations (MICs), indicating that this combination therapy could be a promising option for treating MDR Acinetobacter infections. This finding is particularly significant given the high resistance to other commonly used antibiotics.

Figure 3: Synergy testing with ceftazidime-avibactam and aztreonam E-strip.Click here to view Figure

Discussion

Acinetobacter infections have emerged as a significant threat in healthcare settings, particularly in intensive care units.¹³ These infections commonly manifest as ventilator-associated pneumonia, bacteremia, and urinary tract infections.¹⁴ The prevalence of Acinetobacter pneumonia is higher in Asian and European hospitals compared to the United States.¹³ Multidrug-resistant strains pose a significant challenge, with resistance rates varying geographically.^13,15 The mortality rate associated with Acinetobacter infections is high, reaching 45% in some studies.¹⁴

In our study,the majority of the isolates were A .baumannii (95.3 %), and 5 were Acinetobacter lwoffii (4.6 %), similar to a study.¹⁶ The high prevalence of A .baumannii has highlighted the prominence of this species in hospital-acquired infections. Infections in our study were more prevalent in males (67.6) than females, similar to many studies.^{6, 17,18} The predominance of male patients may reflect underlying health behaviors or greater exposure to healthcare interventions, such as mechanical ventilation, that predispose to infection.

In the present study, the infections were more common among the age group > 50 years, and patients with Acinetobacter infections tend to have longer hospital stays than those without infections.This demographic distribution is consistent with previous research, which suggests that older adults,⁶ particularly those with underlying comorbidities,¹⁹ are more susceptible to A. baumannii infections.

Acinetobacter infections are growing in intensive care units (ICUs), particularly in Asia and Europe.¹³ The prevalence of Acinetobacter infections in ICUs ranges from 11.7% to 30.8%.^{19- 20}  Out of 108 isolates studied, 41(38 %) were from ICU patients. A. baumannii infection was more pronounced in the ICU than in other wards, this is in concordance with other studies.^6,9 Most of the patients in the ICU have an immunocompromised state, due to this, it’s associated with increased length of stay in ICUs.¹⁹ Acinetobacter species were recovered from respiratory samples (ET aspirate (36.1%) and sputum (34.2%) followed by wound samples, indicating a high prevalence of respiratory infections similar to some studies.²¹  In this study, the isolation rates of Acinetobacter in ET aspirate and sputum are 36.1% and 34.2% similar to another study,²² with isolation rates ranging from 31.3% to 46%. These nosocomial infections primarily affect the respiratory tract of intubated patients, with medical patients being more susceptible to lung infections, especially late-onset ventilator-associated pneumonia.²³ The high prevalence of A. baumannii in ICU patients underscores the need for stringent infection control measures, particularly in respiratory care settings where ventilator-associated pneumonia is a significant concern. Adopting rigorous hand hygiene, equipment sterilization protocols, and antimicrobial stewardship programs is essential to limit the spread of MDR strains​.

Multidrug-resistant strains are common, with high resistance to penicillins, cephalosporins, and even extended-spectrum antibiotics.¹⁹ Previously multidrug resistance was found in 60–80% of isolates, with strong resistance to carbapenems, cephalosporins, and other widely used antibiotics.^6,24 While carbapenems were traditionally the treatment of choice, increasing resistance has led to the reintroduction of polymyxins (colistin and polymyxin B) and the use of tigecycline. The retained sensitivity to levofloxacin (81.5%) and meropenem (81.5%) is a positive finding, but the increasing reports of carbapenem resistance in other regions suggest that continued surveillance is essential. Studies have shown varying susceptibility rates to these antibiotics and reported high susceptibility to colistin (99.2%) and polymyxin B (100%), with 94% susceptibility to tigecycline.²⁵ One of the most significant findings of this study is the complete sensitivity of all isolates to colistin and tigecycline. However, the global rise of colistin-resistant A. baumannii warrants caution, as resistance to this last-resort antibiotic could severely limit treatment options. To combat this threat, strict infection control practices and appropriate antibiotic policies must be implemented in ICUs.^26,27

The ability of ceftazidime-avibactam+aztreonam to reduce the MICs of Acinetobacter baumanii and MBL-producing Pseudomonas aeruginosa is a potentially promising therapeutic option when faced with growing antimicrobial resistance which is evident from  present study. All MDR isolates subjected to the ceftazidime-avibactam+aztreonam synergy test were sensitive. In case of the limited options available for MDR infections, this combination should be further explored in clinical trials to validate its efficacy.

Conclusion

This study confirms the predominance of A. baumannii as a major pathogen in ICU settings, with a significant proportion of isolates exhibiting multidrug resistance. The high resistance to commonly used antibiotics highlights the need for alternative therapeutic strategies. The sensitivity of all isolates to colistin and tigecycline supports their continued use in managing MDR infections, while the potential of combination therapies with ceftazidime-avibactam and aztreonam warrants further investigation. Future research should explore the genetic mechanisms driving resistance in A. baumannii and evaluate the efficacy of novel combination therapies in clinical settings. Such infection and resistance development to antibiotics can be prevented by hospital infection control practices, strengthening of antimicrobial stewardship program, and implementation of antimicrobial surveillance strategies.

Acknowledgment

We thank the management, Department of Microbiology, Sree Balaji Medical College and Hospital, and technicians for their work support.

Funding Sources

The author(s) received no financial support for the research, authorship, and/or publication of this article.

Conflict of Interest

The author(s) do not have any conflict of interest.

Data Availability Statement

This statement does not apply to this article.

Ethics Statement

The study was approved by our Institutional Human Ethics Committee (SBMCH/002/SBMCH/IEHC/1828).

Informed Consent Statement

This study did not involve human participants, and therefore, informed consent was not required.

Clinical Trial Registration

This research does not involve any clinical trials

Permission to reproduce material from other sources

Not Applicable

Authors Contributions

• Bindu: Conceptualised and designed the study, and drafted the article
• Chitralekha Saikumar: reviewed the article
• Risha Mynooah collected and interpreted the data including the pictures

References

1. Wong D, Nielsen TB, Bonomo RA, Pantapalangkoor P, Luna B, Spellberg B. Clinical and pathophysiological overview of Acinetobacterinfections: a century of challenges. Clin Microbiol Rev. 2017;30:409-447.
   CrossRef
2. Dexter C, Murray GL, Paulsen IT, Peleg AY. Community-acquired Acinetobacter baumannii: clinical characteristics, epidemiology and pathogenesis. Expert Rev Anti Infect Ther. 2015;13:567–573.doi: 10.1586/14787210.2015.1025055.
   CrossRef
3. Pattanaik A, GS Banashankari. Characterisation of Acinetobacter with special reference to carbapenem resistance and biofilm formation. Trop J Path Micro. 2019;5(6):386-395. doi:10.17511/jopm.2019.i06.09.
   CrossRef
4. World Health Organization. (2023). Global priority list of antibiotic-resistant bacteria to guide research, discovery, and development of new antibiotics.
5.  Mohd Sazlly Lim S,  Zainal Abidin A, Liew SM,  Roberts JA, Sime FB.The global prevalence of multidrug-resistance among Acinetobacter baumannii causing hospital-acquired and ventilator-associated pneumonia and its associated mortality: A systematic review and meta-analysis. Journal of Infection. 2019;79 (6):593-600,
   CrossRef
6. Madhavi RB, Anitha D, Beena PM. Clinical and Antimicrobial profile of AcinetobacterSpecies at a Tertiary Care Teaching Hospital. J Pure Appl Microbiol. 2022;16(3):2066-2071. doi: 10.22207/JPAM.16.3.61
   CrossRef
7. Kaur R, Kaur S, Oberoi L, Singh K, Nagpal N, Kaur M. Prevalence & antimicrobial profile of Acinetobacter spp. isolated from tertiary care hospitals. International Journal of Contemporary Medical Research. 2021;8(2):B1-B6.
8. Ajao AO, Robinson G, Lee MS, Ranke TD, Venezia RA, Furuno JP, Harris AD, Johnson JK. Comparison of culture media for detection of Acinetobacter baumannii in surveillance cultures of critically-ill patients. Eur J Clin Microbiol Infect Dis. 2011; (11):1425-30. doi: 10.1007/s10096-011-1237-7. Epub 2011 Apr 12. PMID: 21487763; PMCID: PMC3660032.
   CrossRef
9. Kulkarni SS, Madalgi R, Ajantha GS, Kulkarni RD. Identification of genus Acinetobacter: Standardization of in-house PCR and its comparison with conventional phenotypic methods. J Lab Physicians. 2017;9(4):279-282. doi: 10.4103/0974-2727.214263. PMID: 28966491; PMCID: PMC5607758.
   CrossRef
10. Hsieh WS, Sung LL, Tsai KC, Ho HT. Evaluation of the VITEK 2 cards for identification and antimicrobial susceptibility testing of non-glucose-fermenting Gram-negative bacilli. 2009;117(4):241-7. doi: 10.1111/j.1600-0463.2009.02436.x. PMID: 19343822.
    CrossRef
11. Clinical and Laboratory Standards Institute antimicrobial susceptibility testing standards CLSI M100: Performance Standards for Antimicrobial Disk Susceptibility Tests, 33th Edition(2023).
12. Yamuna Devi Bakthavatchalam, Kamini Walia, Balaji Veeraraghavan,. Susceptibility testing for aztreonam plus ceftazidime/avibactam combination: A general guidance for clinical microbiology laboratories in India. Indian Journal of Medical Microbiology. 2022;40(1):3-6.
    CrossRef
13. Falagas ME, Karveli EA, Siempos II, Vardakas KZ. Acinetobacter infections: a growing threat for critically ill patients. Epidemiol Infect. 2008;136(8):1009-19. doi: 10.1017/S0950268807009478. Epub 2007 Sep 25. PMID: 17892629; PMCID: PMC2870905.
    CrossRef
14. Patel RV, Shah JS, Gunturu R, Siika W, Shah R. Acinetobacter infections: a retrospective study to determine in-hospital mortality rate and clinical factors associated with mortality. Infection Prevention in Practice. 2019;1(2):100010-100010.
    CrossRef
15. Jain, Rupali and Larry H. Danziger. Multidrug-Resistant Acinetobacter Infections: An Emerging Challenge to Clinicians. Annals of Pharmacotherapy. 2004;38:1449 -1459.
    CrossRef
16. Musyoki VM, Masika MM, Mutai W, Wilfred G, Kuria A, Muthini F. Antimicrobial susceptibility pattern of Acinetobacterisolates from patients in Kenyatta National Hospital, Nairobi, Kenya. Pan Afr Med J. 2019;26:33:146. doi: 10.11604/pamj.2019.33.146.17220. PMID: 31558943; PMCID: PMC6754852.
    CrossRef
17. Alotaibi T, Abuhaimed A, Alshahrani M, Albdelhady A, Almubarak Y, Almasari O. Prevalence of multidrug-resistant Acinetobacter baumanniiin a critical care setting: A tertiary teaching hospital experience. SAGE Open Med. 2021; 15;9:20503121211001144. doi: 10.1177/20503121211001144. PMID: 33796296; PMCID: PMC7968016.
    CrossRef
18. Mohammed S H, Ahmed M M, Abd Alameer Abd Alredaa N, Haider Abd Alabbas H, Mohammad Ali Z D, Abed Al-Wahab Z Z, Zainab Ali Mohsin, Zahraa Jalil Jasim Mohammed, Zahraa Abd Al Hamza Mohammed, Noor Yahya Abid Zaid. Prevalence of Acinetobacter Species Isolated from Clinical Samples Referred to Al-Kafeel Hospital and Their Antibiotic Susceptibility Patterns from 2017-2021. Iran J Med Microbiol.2022;16 (1):76-82.
    CrossRef
19. Tahseen, Uzma and Muhammad Tahseen Talib. Acinetobacter infections as an emerging threat in intensive care units. Journal of Ayub Medical College Abbottabad.  JAMC.2015;27(1):113-6 .
20. Aedh, Abdullah Ibrahim. Prevalence of Acinetobacter infections among Intensive Care Unit’s patients in Najran. Int. J. Curr. Res. Med. Sci. 2017;3(5):122-128.
    CrossRef
21. Rani C, Sharma S R, Farooq U, Singh S, Sharma V, Ahmad. Isolation of Acinetobacter Spp. and its antimicrobial resistance pattern in all lower respiratory samples from ICU. IP International Journal of Medical Microbiology and Tropical Diseases. 2022; 8(2):118-122.
    CrossRef
22. S S, S P, S U, Easow JM. Antibiotic Susceptibility Pattern of Aerobic Bacterial Pathogen Isolated from Endotracheal Aspirate. The Journal of the Association of Physicians of India. 2022;70(12):11-12 .doi: 10.5005/japi-11001-0143. PMID: 37355964.
    CrossRef
23.  Sannathimmappa MB, Nambiar V, Aravindakshan R. Antibiotic resistance pattern of Acinetobacter baumannii strains: A retrospective study from Oman. Saudi J Med Med Sci. 2021;9:254-60.
    CrossRef
24. Mathai AS, Oberoi A, Madhavan S, Kaur P. Acinetobacter infections in a tertiary level intensive care unit in northern India: epidemiology, clinical profiles and outcomes. J Infect Public Health. 2012;5(2):145-52. doi: 10.1016/j.jiph.2011.12.002. Epub 2012 Feb 16. PMID: 22541261.
    CrossRef
25. Guddeti PK, Shah H, Karicheri R, Singh L. Clinical Profile of Patients and Antibiogram of Acinetobacter baumanniiIsolates in a Tertiary Care Hospital, Central India. J Pure Appl Microbiol. 2023;17(3):1435-1443. doi: 10.22207/JPAM.17.3.03
    CrossRef
26. Dizbay M, Altuncekic A, Sezer BE, Ozdemir K, Arman D. Colistin and tigecycline susceptibility among multidrug-resistant Acinetobacter baumannii isolated from ventilator-associated pneumonia. Int J Antimicrob Agents. 2008;32(1):29-32. doi: 10.1016/j.ijantimicag.2008.02.016. Epub 2008 Jun 6. PMID: 18539006.
    CrossRef
27. Ugochukwu NV,Adetona FS, Adeola F, Ajani, BR, Olusanya O. Nosocomial Acinetobacter Infections in Intensive Care Unit. American Journal of Infectious Diseases. 2013;9(2):40-45. https://doi.org/10.3844/ajidsp.2013.40.45
    CrossRef