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Original Article Antibiotic Resistance of Acinetobacter baumannii in Iran: A Systemic Review of the Published Literature
Jale Moradi, Farhad B. Hashemi, Abbas Bahador
Osong Public Health and Research Perspectives 2015;6(2):79-86.
DOI: https://doi.org/10.1016/j.phrp.2014.12.006
Published online: February 19, 2015
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Department of Microbiology, School of Medicine, Tehran University of Medical Sciences, Tehran, Iran

∗Corresponding author. abahador@tums.ac.irab.bahador@gmail.com
• Received: October 16, 2014   • Revised: November 20, 2014   • Accepted: December 22, 2014

© 2015 Published by Elsevier B.V. on behalf of Korea Centers for Disease Control and Prevention.

This is an Open Access article distributed under the terms of the CC-BY-NC License (http://creativecommons.org/licenses/by-nc/3.0).

  • Objectives
    Acinetobacter baumannii is a bacterium responsible for health care-associated infections, and it frequently develops multiple drug resistance (MDR). The prevalence of antibiotic-resistant A. baumannii in Iran has increased, and this may cause significant clinical problems. Therefore, in order to elucidate the development of antibiotic resistance, we performed a systematic review of the literature published on antibiotic-resistant A. baumannii reported in Iran.
  • Methods
    Thirty-six publications that met the criteria for inclusion were reviewed from an initial 87 papers. Selected papers published between 2008 and September 2014, were categorized on the basis of the sample collecting year been between 2001 and 2013.
  • Results
    Analysis of data revealed that, in general, there was an increase in antimicrobial resistance. During the initial time point of these studies (2001–2007) there was a high rate of resistance to all antibiotics, with the exception of carbapenems, lipopeptides, and aminoglycosides that had a low resistance rate in comparison with the others. Also, the resistance rate was increased in one group of these three antimicrobial groups from 2010 to 2013. In particular, there was an increase in resistance to carbapenems (imipenem and meropenem) from 2010–2011 and 2012–2013, whereas no significant change in the resistance rate of the other two antimicrobial groups (lipopeptides and aminoglycosides) during the study time was observed, although we did observe certain trends in amikacin (aminoglycoside group antibiotic) between 2011–2012 and 2012–2013.
  • Conclusion
    These findings indicate that antimicrobial resistance of A. baumannii in Iran has increased, which may very well affect the antimicrobial resistance of this organism worldwide. Based on these results, novel prevention and treatment strategies against A. baumannii infections are warranted. Furthermore, these data may assist in revising treatment guidelines and regional policies in care units to slow the emergence of antimicrobial resistance.
Acinetobacter baumannii is a gram-negative, strictly aerobic, nonfermenting coccobacillus belonging to the Moraxellaceae family [1]. Species belonging to this genus are opportunistic pathogens with increasing relevance in both community-acquired and nosocomial infections, particularly among patients in intensive care units (ICUs) and high-dependency units (HDUs) [2–5]. These organisms have been implicated in various infections, including ventilator-associated pneumonia, endocarditis, meningitis, and infections of the skin, soft tissues, urinary tract, and those originating from prosthetic devices [4,6]. A. baumannii has been isolated from numerous sources such as soil, water, animals, and humans, while its presence in health care institutions and on environmental surfaces has been extremely difficult to control [6].
Three decades ago, A. baumannii infections were effectively treated with traditional antibiotics [7,8]. By contrast, it currently exerts resistance to nearly all major classes of antibiotics, including broad-spectrum penicillins, cephalosporins, carbapenems, most aminoglycosides, fluoroquinolones, chloramphenicol, and tetracyclines. In the past decade, multidrug resistant (MDR) clinical isolates have shown global distribution [3]. Therefore, this pathogen has become a “red-alert” for the following reasons: rapid emergence of resistance, increased incidence, and the worldwide spread of MDR isolates [7]. The rapid spread of MDR strains in nosocomial infections that exhibit resistance to most or all common antibiotics is a troubling evolution [3]. Thus, a study of the antibiotic resistance patterns both in individual hospitals and on countrywide levels may help to clarify the mode of A. baumannii antibiotic resistance spread and epidemiology worldwide [9]. The current review was performed to elucidate the mode of antibiotic resistance of A. baumannii in Iran.
2.1 Database searches
Biomedical databases (Scopus, Medline, Web of Science, EBSCO, IranMedex) were searched in order to retrieve all related manuscripts published in English and Persian. The search identified publications of epidemiological studies in order to compile adequate information on A. baumannii antimicrobial resistance in Iran. The following key words were used: “Acinetobacter baumannii and Iran”, “antimicrobial resistance and Acinetobacter baumannii and Iran”, “antimicrobial resistance and either gram negative bacilli and Iran or Iran”, “nosocomial or hospital acquired and Iran” . Study publications were obtained through PubMed, MEDLINE, and IranMedex database searches. Also, references cited within these articles were used to find additional relevant articles. In this review, A. baumannii susceptibility breakpoints based on Clinical Laboratory Standards Institute (CLSI)-relevant antibiotics were primarily those listed by the World Health Organization Recommended Surveillance Standards.
2.2 Study settings
From the first 87 papers, we identified a total of 36 that were written in English and considered to be eligible for inclusion in this review. The selected papers were published between 2008 and September 2014. We categorized studies on the basis of sample collection year, between 2001 and 2013; some papers collect samples during different years (Table 1). Two studies were performed in three regions of Iran, including central, north, and south. Twenty-two studies were performed north of Iran, with 18 in Tehran (capital of Iran). Two studies occurred in the south of Iran, three in the west, and three in the east. Although the studies used various methods, they were all approved by the CLSI and the National Committee for Clinical Laboratory Standards (NCCLS) and, therefore, suitable for trend analysis.
2.3 Microbiological methods
Clinical specimens in studies were collected from hospitalized patients with different disease and various sampling. Twenty of the studies obtained data from various clinical specimens, including blood, cerebrospinal fluid, urine, sputum, and respiratory tract samples. Data from eight studies were obtained from patients with burn wounds and seven from hospitalized patients in ICUs. Antibiotic susceptibility testing methodologies were declared in all studies, all of which were performed according to the CLSI breakpoints. Twenty-six studies used the Kirby-Bauer disk diffusion method, nine used the E-test, and two used broth microdilution. To identify resistance genes, 25 of the studies used one or more polymerase chain reaction-based molecular methods.
3.1 Phenotypic resistance rates for different antibiotics
The susceptibility data for 3049 A. baumannii isolates are shown in Table 2. These data reflect the 12-year period from 2001 to 2013 of sampling time in the studies identified. The data demonstrate that, with the exception of carbapenems, lipopeptides, and aminoglycosides, there was a high rate of resistance to antimicrobial groups during the initial time point of this study (2001–2007). Also, the resistance rate was increased in one group of these three antimicrobial groups from 2010 to 2013. In particular, there was an increase in resistance to carbapenems (imipenem and meropenem) from 2010–2011 and 2012–2013, whereas no significant change in the resistance rate to other two antimicrobial groups (lipopeptides and aminoglycosides) during the study time was observed, although we did observe certain trends in amikacin (aminoglycoside group antibiotic) between 2011–2012 and 2012–2013.
There are data regarding resistance to penicillins from 2001 to 2011. There was a remarkable increase in piperacillin resistance (from 63.9% in 2001–2007 to 93.4% in 2010–2011). The resistance rate to the β-lactam/β-lactamase combination group was high early in the study, with no substantial change to the study endpoint. The highest level of antimicrobial resistance throughout the study was noted among the cephems group (>90%), including ceftazidime, cefepime, cefotaxime, and ceftriaxone. Resistance to carbapenems was low at the study start point (51.1% imipenem, 64.3% meropenem) and increased by the end of the study (76.5% imipenem, 81.5% meropenem), thus demonstrating the most drastic increase in resistance rate. A low level of resistance at the starting point was also observed for lipopeptides (polymyxin B and colistin), with no significant trends as the study progressed. The resistance rate to aminoglycosides was low, with the exception of amikacin (from 58.4% in 2001–2007 to 95% in 2012–2013). At the beginning of the study, there were no data for tetracyclines, whereas there was a high level of resistance to this group at the study endpoint. Resistance to fluoroquinolones was high during the study period with no remarkable pattern change. Finally, an increased resistance rate to folate pathway inhibitors, including trimethoprim sulfamethoxazole, was observed (from 76.6% in 2001–2007 to 99% in 2012–September 2014). In summary, these data demonstrate a high resistance rate to all antimicrobial agents except lipopeptides.
3.2 Genotypic resistance rate
Genotyping of a total of 1717 A. baumannii isolates was performed in 17 studies. Table 3 shows the mechanisms of resistance that were studied for the different antibiotic classes from 2001 to 2013. The genotyping methods in all studies were polymerase chain reaction- and sequence-based. Among the 17 studies, 14, three, three, and one of them were focused on β-lactams, tetracyclines, aminoglycosides, and quinolones, respectively. These genotypic studies demonstrated that isolates harboring resistance genes have increased from 2001 to 2013, which is most remarkable for carbapenem.
3.3 Distribution of multidrug resistance
By definition, MDR A. baumannii isolates are resistant to three or more agents of different antibiotic classes. In total, seven studies revealed the presence of MDR isolates. Among these seven studies, this analyzed 584 A. baumannii isolates, MDR rates ranged from 32.7% to 93%. Chronologically, these rates can be broken down as follows: 2001–2007 (1 study, 50%), 2008–2009 (1 study, 66%), 2009–2010 (1 study, 83%), and 2010–2011 (4 studies, 32.7%, 74.9%, 93%, 94.4%, respectively). In general, the prevalence of MDR increased throughout the duration of the study.
A. baumannii infection has become a critical challenge to health care systems. To become an optimally successful pathogen, an organism must develop antimicrobial resistance. Although there is debate regarding the definitions of “multidrug” and “pandrug” resistance [45], an understanding has been reached in that resistance to all common antimicrobial agents is currently a common problem in health care institutions [46,47]. The emergence of MDR isolates has become a serious problem that has made it difficult to select an empirical antimicrobial for the treatment of A. baumannii infections. Therefore, monitoring the antibiotic resistance patterns of this organism over time may provide useful information regarding its treatment policy. This systematic review considered the distribution of antibiotic-resistant A. baumannii in CLSI-approved studies published in Iran between 2001 and September 2014.
According to the results, some level of resistance to all antibiotic classes existed in the beginning of our study. However, we revealed that the distribution of antimicrobial resistance to all agents was high at the endpoint, with the exception of the lipopeptides. Currently, the antibiotics of choice for treatment of A. baumannii infections include the aminoglycosides, fluoroquinolones, and carbapenems [48]. Thus, it is concerning that our data demonstrate that A. baumannii resistance to these agents increased over the time course of this study, with a resistance rate in excess of 90% in 2013. As such, these antibiotics may not be appropriate empirical therapy in many cases. For example, carbapenems are one of the most clinically important classes of antibiotics used against life-threatening A. baumannii infections in Iran [10]. Our results showed that this group of antibiotics had low-level resistance in 2001–2007 (51.1% imipenem, 64.3% meropenem), which increased in 2012–2013 (76.5% imipenem, 81.5% meropenem). The data also showed that the most drastic increase in resistance is associated with this antibiotic class, possibly due to its frequency of use in health care units. This is an alarming finding that strongly suggests the possibility of treatment failures in life-threatening A. baumannii infections due to carbapenem-resistance strains.
As mentioned previously, our data show that resistance to lipopeptides is lower compared with that of other antimicrobial groups. One of the antibiotics of this class is polymyxin B, which, despite previous concerns regarding its toxicity, has been implemented in treatment more frequently [49]. Another lipopeptide antibiotic is colistin, which has proven effective in the treatment of wound, urinary tract, and bloodstream infections [50], although its nephrotoxicity is a disadvantage to its use [51]. Although use of this antibiotic class has limitations due to toxicity, they are often used for the treatment of life-threatening infections.
In addition to an increase in antibiotic-resistant A. baumannii strains from 2001 to 2013, the prevalence of MDR strains also increased (from 50% in 2001–2007 to 74% in 2010–2011), with a mean prevalence of 71.2%. Treatment of MDR strains is usually difficult, thus creating critical challenges for health care consultants [52,53]. The antibiotic choice for the treatment of MDR A. baumannii infections is also limited and includes the lipopeptides, [52,54] which the results of this study suggest is the best class of antibiotics to use for MDR because of the lower prevalence of resistance.
In summary, our results demonstrate the need for effective surveillance of antimicrobial resistance in A. baumannii in Iran and suggest that it is essential to use antibiotics with the most caution to prevent the emergence of drug-resistant strains. Furthermore, these findings indicate that the prevalence of antibiotic-resistant A. baumannii is high in Iran, especially for the antibiotics of choice. This is an emerging concern to public health, particularly in the clinical management of persons with life-threatening A. baumannii infections. We strongly suggest the implementation of a countrywide surveillance system. This would facilitate the active monitoring of resistance frequency and distinguish antibiotic resistance trends and prevalence, all of which would be effective tools in antibiotic treatment programs.
None to declare.

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

  • 1. Chittawatanarat K., Jaipakdee W., Chotirosniramit N.. Microbiology, resistance patterns, and risk factors of mortality in ventilator-associated bacterial pneumonia in a Northern Thai tertiary-care university based general surgical intensive care unit. Infect Drug Resist 7:2014;203−210. PMID: 25152627.ArticlePubMedPMC
  • 2. Eveillard M., Kempf M., Belmonte O.. Reservoirs of Acinetobacter baumannii outside the hospital and potential involvement in emerging human community-acquired infections. Int J Infect Dis 17(10): 2013;802−805.Article
  • 3. Oh Y.J., Song S.H., Baik S.H.. A case of fulminant community-acquired Acinetobacter baumannii pneumonia in Korea. Korean J Intern Med 28(4): 2013;486−490. PMID: 23864808.ArticlePubMedPMC
  • 4. Kim U.J., Kim H.K., An J.H.. Update on the epidemiology, treatment, and outcomes of carbapenem-resistant Acinetobacter infections. Chonnam Med J 50(2): 2014 Aug;37−44. PMID: 25229014.Article
  • 5. Tang S.S., Apisarnthanarak A., Hsu L.Y.. Mechanisms of β-lactam antimicrobial resistance and epidemiology of major community- and healthcare-associated multidrug-resistant bacteria. Adv Drug Deliv Rev 78:2014 Nov;3−13. PMID: 25134490.Article
  • 6. Nhu N.T., Lan N.P., Campbell J.I.. Emergence of carbapenem-resistant Acinetobacter baumannii as the major cause of ventilator-associated pneumonia in intensive care unit patients at an infectious disease hospital in southern Vietnam. J Med Microbiol 63(10): 2014 Oct;1386−1394. PMID: 25038137.Article
  • 7. Liu B., Liu Y., Di X.. Colistin and anti-Gram-positive bacterial agents against Acinetobacter baumannii. Rev Soc Bras Med Trop 47(4): 2014 Jul;451−456. PMID: 25229285.Article
  • 8. García-Quintanilla M., Pulido M.R., López-Rojas R.. Emerging therapies for multidrug resistant Acinetobacter baumannii. Trends Microbiol 21:2013;157−163. PMID: 23317680.ArticlePubMed
  • 9. Antunes L.C., Visca P., Towner K.J.. Acinetobacter baumannii: evolution of a global pathogen. Pathog Dis 71(3): 2014 Aug;292−301. PMID: 24376225.Article
  • 10. Feizabadi M.M., Fathollahzadeh B., Taherikalani M.. Antimicrobial susceptibility patterns and distribution of blaOXA genes among Acinetobacter spp. Isolated from patients at Tehran hospitals. Jpn J Infect Dis 61:2008;274−278. PMID: 18653968.PubMed
  • 11. Soroush S., Haghi-Ashtiani M.T., Taheri-Kalani M.. Antimicrobial resistance of nosocomial strain of Acinetobacter baumannii in Children's Medical Center of Tehran: a 6-year prospective study. Acta Med Iranica 48:2010;178−184.
  • 12. Taherikalani M., Maleki A., Sadeghifard N.. Dissemination of class 1, 2 and 3 integrons among different multidrug resistant isolates of Acinetobacter baumannii in Tehran hospitals, Iran. Pol J Microbiol 60:2011;169−174. PMID: 21905636.ArticlePubMed
  • 13. Bahador A., Raoofian R., Taheri M.. Multidrug resistance among Acinetobacter Baumannii isolates from Iran: Changes in antimicrobial susceptibility patterns and genotypic profile. Microb Drug Resist 20(6): 2014 Dec;632−640. PMID: 25029126.Article
  • 14. Japoni S., Japoni A., Farshad S.. Association between existence of integrons and multi-drug resistance in Acinetobacter isolated from patients in southern Iran. Pol J Microbiol 60(2): 2011;163−168. PMID: 21905635.ArticlePubMed
  • 15. Mohammadi-Mehr M., Feizabadi M.M.. Antimicrobial resistance pattern of Gram-negative bacilli isolated from patients at ICUs of Army hospitals in Iran. Iran J Microbiol 3:2011;26−30. PMID: 22347579.PubMedPMC
  • 16. Moniri R., Farahani R.K., Shajari G.. Molecular epidemiology of aminoglycosides resistance in Acinetobacter spp. With emergence of multidrug-resistant strains. Iran J Public Health 39(2): 2010;63−68. PMID: 23113008.PubMedPMC
  • 17. Sarafzadeh F., Sohrevardi S., Gharehghozli M.. Detection of the most common microorganisms and their resistance against anti-microbials in intubated patients in an ICU in Kerman, Iran. Iran J Pharm Res 9(4): 2010 Fall;437−443. PMID: 24381610.
  • 18. Peymani A., Nahaei M.R., Farajnia S.. High prevalence of metallo-beta-lactamase-producing Acinetobacter baumannii in a teaching hospital in Tabriz. Iran. Jpn J Infect Dis 64:2011;69−71.
  • 19. Peymani A., Farajnia S., Nahaei M.R.. Prevalence of class 1 integron among multidrug-resistant Acinetobacter baumannii in Tabriz, northwest of Iran. Pol J Microbiol 61:2012;57−60. PMID: 22708347.ArticlePubMed
  • 20. Sohrabi N., Farajnia S., Akhi M.T.. Prevalence of OXA-type beta-lactamases among Acinetobacter baumannii isolates from Northwest of Iran. Microb Drug Resist 18(1): 2012;385−389. PMID: 22352411.ArticlePubMed
  • 21. Farajnia S., Azhari F., Alikhani M.Y.. Prevalence of PER and VEB type extended spectrum betalactamases among multidrug resistant Acinetobacter baumannii isolates in North-West of Iran. Iran J Basic Med Sci 16:2013 Jun;751−755. PMID: 23997900.
  • 22. Shahcheraghi F., Abbasalipour M., Feizabadi M.M.. Isolation and genetic characterization of metallo-beta-lactamase and carbapenamase producing strains of Acinetobacter baumannii from patients at Tehran hospitals. Iran J Microbiol 3(2): 2011 June;68−74. PMID: 22347585.
  • 23. Asadollahi P., Akbari M., Soroush S.. Antimicrobial resistance patterns and their encoding genes among Acinetobacter baumannii strains isolated from burned patients. Burns 38(8): 2012 Dec;1198−1203. PMID: 22579564.Article
  • 24. Mirnejad R., Mostofi S., Masjedian F.. Antibiotic resistance and carriage class 1 and 2 integrons in clinical isolates of Acinetobacter baumannii from Tehran, Iran. Asian Pac J Trop Biomed 3(2): 2013 Feb;140−145. PMID: 23593593.Article
  • 25. Owlia P., Azimi L., Gholami A.. ESBL- and MBL-mediated resistance in Acinetobacter baumannii: a global threat to burn patients. Infez Med 20(3): 2012 Sep;182−187. PMID: 22992558.
  • 26. Shakibaie M.R., Adeli S., Salehi M.H.. Antibiotic resistance patterns and extended-spectrum beta-lactamase production among Acinetobacter spp. isolated from an intensive care Unit of a hospital in Kerman, Iran. Antimicrob Resist Infect Control 1(1): 2012 Jan 26;1PMID: 22958725.Article
  • 27. Rezaee M.A., Pajand O., Nahaei M.R.. Prevalence of Ambler class a beta-lactamases and ampC expression in cephalosporin-resistant isolates of Acinetobacter baumannii. Diagn Micr Infec Dis 76(3): 2013 Jul;330−334.Article
  • 28. Pajand O., Rezaee M.A., Nahaei M.R.. Study of the carbapenem resistance mechanisms in clinical isolates of Acinetobacter baumannii: comparison of burn and non-burn strains. Burns 39(7): 2013 Nov;1414−1419. PMID: 23726475.Article
  • 29. Aghazadeh M., Rezaee M.A., Nahaei M.R.. Dissemination of aminoglycoside-modifying enzymes and 16S rRNA methylases among Acinetobacter baumannii and Pseudomonas aeruginosa isolates. Microb Drug Resist 19(4): 2013 Aug;282−288. PMID: 23577624.Article
  • 30. Azimi L., Lari A.R., Talebi M.. Comparison between phenotypic and PCR for detection of OXA-23 type and metallo-beta-lactamases producer Acinetobacter spp. GMS Hyg Infect Control 8(2): 2013 Nov;16.
  • 31. Japoni-Nejad A., Sofian M., Belkum A.. Nosocomial outbreak of extensively and pan drug-resistant Acinetobacter baumannii in tertiary hospital in central part of Iran. Jundishapur J Microbiol 6:2013;92−98.
  • 32. Japoni-Nejad A., Farshad S., van Belkum A.. Novel cassette array in a class 1 integron in clinical isolates of Acinetobacter baumannii from central Iran. Int J Med Microbiol 303(8): 2013 Dec;645−650. PMID: 24161711.Article
  • 33. Karmostaji A., Peerayeh S.N., Salmanian A.H.. Distribution of OXA-type class D β-lactamase genes among nosocomial multi drug resistant Acinetobacter baumannii isolated in Tehran Hospital. Jundishapur J Microbiol 6:2013;12−14.
  • 34. Mohajeri P., Farahani A., Feizabadi M.M.. Antimicrobial susceptibility profiling and genomic diversity of Acinetobacter baumannii isolates: A study in western Iran. Iran J Microbiol 5(3): 2013 Sep;195−202. PMID: 24475323.
  • 35. Hojabri Z., Pajand O., Bonura C.. Molecular epidemiology of Acinetobacter baumannii in Iran: endemic and epidemic spread of multiresistant isolates. J Antimicrob Chemother 69(9): 2014 Sep;2383−2387. PMID: 24562615.Article
  • 36. Maleki M.H., Sekawi Z., Soroush S.. Phenotypic and genotypic characteristics of tetracycline resistant Acinetobacter baumannii isolates from nosocomial infections at Tehran hospitals. Iran J Basic Med Sci 17(1): 2014 Jan;21−26. PMID: 24592303.
  • 37. Nowroozi J., Sepahi A.A., Kamarposhti L.T.. Evaluation of ciprofloxacin (gyrA, parC genes) and tetracycline (tetB gene) resistance in nosocomial Acinetobacter baumannii infections. Jundishapur J Microbiol 7(2): 2014 Feb;e8976PMID: 25147676.
  • 38. Mirnejad R., Vafaei S.. Antibiotic resistance patterns and the prevalence of ESBLs among strains of Acinetobacter baumannii isolated from clinical specimens. JGMI 2:2013;1−8.
  • 39. Safari M., Saidijam M., Bahador A.. High prevalence of multidrug resistance and metallo-beta-lactamase (MbetaL) producing Acinetobacter baumannii isolated from patients in ICU wards, Hamadan. Iran J Res Health Sci 13(2): 2013 Sep;162−167.
  • 40. Vakili B., Fazeli H., Shoaei P.. Detection of colistin sensitivity in clinical isolates of Acinetobacter baumannii in Iran. Iran J Res Med Sci 19(Suppl. 1): 2014 Mar;S67−70.
  • 41. Bahador A., Taheri M., Pourakbari B.. Emergence of rifampicin, tigecycline, and colistin-resistant Acinetobacter baumannii in Iran; spreading of MDR strains of novel International Clone variants. Microb Drug Resist 19(5): 2013 Oct;397−406. PMID: 23768166.Article
  • 42. Kamalbeik S., Talaie H., Mahdavinejad A.. Multidrug-resistant Acinetobacter baumannii infection in intensive care unit patients in a hospital with building construction: is there an association? Korean J Anesthesiol 66(4): 2014 Apr;295−299. PMID: 24851165.Article
  • 43. Pajand O., Hojabri Z., Nahaei M.R.. In vitro activities of tetracyclines against different clones of multidrug-resistant Acinetobacter baumannii isolates from two Iranian hospitals. Int J Antimicrob Agents 43(5): 2014 May;476−478. PMID: 24657045.Article
  • 44. Fallah F., Noori M., Hashemi A.. Prevalence of bla NDM, bla PER, bla VEB, bla IMP, and bla VIM genes among Acinetobacter baumannii isolated from two hospitals of Tehran, Iran. Scientifica (Cairo) 2014:2014;245162PMID: 25133013.PubMedPMC
  • 45. Falagas M.E., Koletsi P.K., Bliziotis I.A.. The diversity of definitions of multidrug-resistant (MDR) and pandrug-resistant (PDR) Acinetobacter baumannii and Pseudomonas aeruginosa. J Med Microbiol 55(Pt 12): 2006 Dec;1619−1629. PMID: 17108263.Article
  • 46. Livermore D.M., Hope R., Brick G.. BSAC Working Parties on Resistance Surveillance. Non-susceptibility trends among Pseudomonas aeruginosa and other non-fermentative Gram-negative bacteria from bacteremias in the UK and Ireland, 2001-06. J Antimicrob Chemother 2(Suppl. 5): 2008 Nov;55−63.
  • 47. Morgan D.J., Weisenberg S.A., Augenbraun M.H.. Multidrug-resistant Acinetobacter baumannii in New York City – 10 years into the epidemic. Infect Control Hosp Epidemiol 30(2): 2009 Feb;196−197. PMID: 19146464.Article
  • 48. Dijkshoorn L., Aucken H., Gerner-Smidt P.. Comparison of outbreak and nonoutbreak Acinetobacter baumannii strains by genotypic and phenotypic methods. J Clin Microbiol 34(6): 1996 Jun;1519−1525. PMID: 8735109.Article
  • 49. Falagas M.E., Kasiakou S.K.. Colistin: the revival of polymyxins for the management of multidrug-resistant gram-negative bacterial infections. Clin Infect Dis 40(9): 2005 May;1333−1341. PMID: 15825037.Article
  • 50. Gounden R., Bamford C., van Zyl-Smit R.. Safety and effectiveness of colistin compared with tobramycin for multi-drug resistant Acinetobacter baumannii infections. BMC Infect Dis 9(9): 2009 Mar;26−28. PMID: 19272139.Article
  • 51. Linden P.K., Paterson D.L.. Parenteral and inhaled colistin for treatment of ventilator-associated pneumonia. Clin Infect Dis 2(Suppl. 2): 2006 Sep;89−94.Article
  • 52. Fishbain J., Peleg A.Y.. Treatment of Acinetobacter infections. Clin Infect Dis 51(1): 2010 Jul;79−84. PMID: 20504234.Article
  • 53. Garnacho-Montero J., Amaya-Villar R.. Multiresistant Acinetobacter baumannii infections: epidemiology and management. Curr Opin Infect Dis 23:2010;332−339. PMID: 20581674.ArticlePubMed
  • 54. Peleg A.Y., Seifert H., Paterson D.L.. Acinetobacter baumannii: emergence of a successful pathogen. Clin Microbiol Rev 21(3): 2008 Jul;538−582. PMID: 18625687.Article
Table 1
Characteristic of Acinetobacter baumannii antimicrobial resistance studies in Iran.
Year of publication (Refs) Year of sample collecting No. of studies Total samples Location of Iran (No. of studies)
2008 [10], 2010 [11], 2011 [12], 2014 [13] 2001–2007 4 383 Capital (4)
2011 [14], 2011 [15] 2007–2008 2 275 Capital (1), South (1)
2010 [16], 2010 [17], 2011 [14], 2011 [18], 2011 [12], 2012 [19], 2012 [20], 2013 [21] 2008–2009 8 680 Capital (1),North (3),West (2),South (1), East (1)
2011 [22], 2012 [23], 2013 [24] 2009–2010 3 276 Capital (3)
2012 [25], 2012 [26], 2013 [27], 2013 [28], 2013 [29], 2013 [30], 2013 [31], 2013 [32], 2013 [33], 2013 [34], 2014 [35], 2014 [36], 2014 [37] 2010–2011 12 970 Capital (6),North (4),East (1),West (1)
2013 [30], 2013 [32], 2013 [38], 2013 [39], 2014 [13], 2014 [40] 2011–2012 6 525 Capital (5), East (1)
2013 [41], 2013 [42], 2014 [43], 2014 [44] 2012–Sep 2014 4 308 Capital (3), North (1)
Table 2
Phenotypic antibiotic resistance rates in Acinetobacter baumannii isolate from Iran.
Antibiotic agents Mean resistance rate (%) in different studies
2001–2007 n = 383 (4 studies) [10–13] 2007–2008 n = 275(2 studies) [14,15] 2008–2009 n = 620(7 studies) [12,14,17–21] 2009–2010 n = 276(3 studies) [22–24] 2010–2011 n = 907(12 studies) [25,26,29–37] 2011–2012 n = 280(4 studies) [13,38–40] 2012–Sep 2014 n = 308(4 studies) [41,43]
PIP 69.9 88.2 93.75 98 93.4
MZ 81.7
TIC 100 100 94
SAM 83.3 27.8 63.5 48.39 33.7 77.5
TZP 52.9 35.3 88.6 71.5 97.3 82.5 70
TIM 100 82.6 94 80
CAZ 93.5 90.7 92 93 92.6 97
FEP 94.1 89 96.6 88.6 97
CTX 95 100 94 99 96.1 98 97
CRO 89.1 100 93.6 97.3 95.6 97.5
IPM 51.1 32 57.75 52.4 81.9 80.5 76.5
MEM 64.3 27.8 59.25 72 85.2 81.5 81.5
PB 8.8 16 3 13.5 3 9.5
CST 1.3 19 12 9.3 16
GEN 76.85 81.9 83.75 40.6 82.9 63 78.5
TOB 63.2 39.2 28 60.9 56 70
AMK 58.4 79.4 82.7 69.5 75 89.5 95
NET 80.5 69.6
TET 34.78 83.82 51 56
DOX 25 42.9
MIN 25.6 34
CIP 83.9 67.6 83.75 92 85.2 97 72
LVX 83.3 81.75 81.25 99
GAT 43.3
SXT 76.6 82.4 87.3 94.3 99

AMK = amikacin; CAZ = ceftazidime; CIP = ciprofloxacin; CRO = ceftriaxone; CST = colistin; CTX = cefotaxime; DOX = doxycycline; FEP = cefepime; GAT = gatifloxacin; GEN = gentamicin; IPM = imipenem; LVX = levofloxacin; MEM = meropenem; MIN = minocycline; MZ = mezlocilli; NET = netilmicin; PB = polymyxin B; PIP = piperacillin; SAM = ampicillin/sulbactam; SXT = trimethoprim/sulfamethoxazole; TET = tetracycline; TIC = ticarcillin; TIM = ticarcillin/clavulanic acid; TOB = tobramycin; TZP = piperacillin/tazobactam.

Table 3
Genotypic resistance rate in Acinetobacter baumannii isolate from Iran.
Antimicrobial class Resistance mechanism Genes Mean Resistance rate (%) in different studies
References
2001––2007 n/N = 2/208 2007–2008 n/N = 0/0 2008–2009 n/N = 3/360 2009–2010 n/N = 2/226 2010–2011 n/N = 7/602 2011–2012 n/N = 1/31 2012–Sep 2014 n/N = 2/302
β-lactams β-lactamases PER-1 51 54.3 27.6 78.03 21,27,23,45
PER-2 0 21
VEB-1 10 39.5 21,45
TEM-1 47.2 13.1 27,23
SHV 5.6 23
ISAba1/ampC 46 63.1 27,20
ISAba 25/ampC 7.8 27
Carbapenemases OXA-23 -like 25, 55 24.58,84 30,67,77.9, 80 70.1 28,30,27,23,20,22,12,37,44
OXA-40 -like 17.1,47 35.8 28,27,44
OXA-58 -like 21.2 12
OXA-24 -like 15, 19.2 12,34
OXA-51 -like 96 94 14.4 28,22,10
IMP 19 3.48 18,45
VIM 9 17.44 18,45
Tetracyclines Efflux pump Tet A 11 36
Tet B 99,86.1 19.4 36,37,44
Aminoglycosides Enzymatic degradation aph(3′)-IIb 61.8 29
aac(6′)-Ib 60.5 16.4 29,44
aph(3′)-Ia 46.1 19.4 29,44
ant(2″)-Ia 14.5 56.7 29,44
ant(3″)-Ia 10.5 29
aph(3′)-Via 9.2, 95.5 29,44
aac(3′)-Ia 5.3 32.8 29,44
aacC1 63.3 16
aadA1 41.7 16
aadB 3.3 16
aphA6 65 16
16s rDNA methyltransferases armA 9 44
Quinolones DNA gyrase/topoisomerase mutations gyrA/parC 100 37

Figure & Data

References

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