Abstract
Acinetobacter baumannii, a bacterial strain which demonstrates an elevated wide range multidrug resistance to commonly prescribed antibiotics, has been linked to recent major global outbreaks, raising a major clinical concern. Its reduced antibiotic susceptibility is closely related to the acquisition of a potent carbapenemase and/or intrinsic gene “over expression” through insertion sequences. Hence, this study aimed at investigating the antimicrobial susceptibility and molecular mechanisms underlying β-lactam resistance in A. baumannii, isolated at an academic medical centre. To understand the basis of resistance, 103 multidrug-resistant (MDR) A. baumannii isolates were collected, their antibiotic susceptibility was tested phenotypically, and then molecular analyses were performed, by testing a range of commonly encountered carbapenemases—OXA-51, OXA-23, NDM, VIM, and KPC. All strains demonstrated pan-resistance to most of the advanced antibiotics tested, including piperacillin/tazobactam, ceftazidime, cefepime, and ciprofloxacin. Moreover, majority of isolates exhibited resistance to imipenem (98.1%) and trimethoprim (90.3%). Approximately 50% of the strains showed meropenem, amikacin, and gentamycin resistance; however, lower resistance rate to tigecycline (4.9%) was noted. Moreover, isolates contained potent carbapenemases such as the intrinsic OXA-51 (89.3%), as well as the acquired resistant genes OXA-23 (68.9%), NDM (84.5%), and VIM (88.3%). The insertion sequence element ISAba1 was only detected in 35.9% of the strains. Potent resistant genes known to be carried on mobile genetic elements that aid the spread of highly resistant phenotypes were observed in a majority of isolates. These findings enforce the need for vigilant infection control measures and continuous surveillance.
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References
Villar M, Cano ME, Gato E et al (2014) Epidemiologic and clinical impact of Acinetobacter baumannii colonization and infection. Medicine (Baltimore). https://doi.org/10.1097/MD.0000000000000036
Qureshi ZA, Hittle LE, O’Hara JA et al (2015) Colistin-resistant Acinetobacter baumannii: beyond carbapenem resistance. Clin Infect Dis 60:1295–1303. https://doi.org/10.1093/cid/civ048
Cheon S, Kim M-J, Yun S-J et al (2016) Controlling endemic multidrug-resistant Acinetobacter baumannii in intensive care units using antimicrobial stewardship and infection control. Korean J Intern Med 31:367–374. https://doi.org/10.3904/kjim.2015.178
Chang Y, Luan G, Xu Y et al (2015) Characterization of carbapenem-resistant Acinetobacter baumannii isolates in a Chinese teaching hospital. Front Microbiol. https://doi.org/10.3389/fmicb.2015.00910
Gordon NC, Wareham DW (2010) Multidrug-resistant Acinetobacter baumannii: mechanisms of virulence and resistance. Int J Antimicrob Agents 35:219–226. https://doi.org/10.1016/j.ijantimicag.2009.10.024
Memish ZA, Assiri A, Almasri M et al (2015) Molecular characterization of carbapenemase production among gram-negative bacteria in Saudi Arabia. Microb Drug Resist 21:307–314. https://doi.org/10.1089/mdr.2014.0121
Ghazawi A, Sonnevend A, Bonnin RA et al (2012) NDM-2 carbapenemase-producing Acinetobacter baumannii in the United Arab Emirates. Clin Microbiol Infect 18:E34–E36. https://doi.org/10.1111/j.1469-0691.2011.03726.x
Ibrahim ME (2019) Prevalence of Acinetobacter baumannii in Saudi Arabia: risk factors, antimicrobial resistance patterns and mechanisms of carbapenem resistance. Ann Clin Microbiol Antimicrob. https://doi.org/10.1186/s12941-018-0301-x
Abdalhamid B, Hassan H, Itbaileh A, Shorman M (2014) Characterization of carbapenem-resistant Acinetobacter baumannii clinical isolates in a tertiary care hospital in Saudi Arabia. New Microbiol 37:65–73
Turton JF, Ward ME, Woodford N et al (2006) The role of ISAba1 in expression of OXA carbapenemase genes in Acinetobacter baumannii. FEMS Microbiol Lett 258:72–77. https://doi.org/10.1111/j.1574-6968.2006.00195.x
Bahador A, Raoofian R, Pourakbari B et al (2015) Genotypic and antimicrobial susceptibility of carbapenem-resistant Acinetobacter baumannii: analysis of ISAba elements and blaOXA-23-like genes including a new variant. Front Microbiol. https://doi.org/10.3389/fmicb.2015.01249
Magiorakos A-P, Srinivasan A, Carey RB et al (2012) Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect 18:268–281. https://doi.org/10.1111/j.1469-0691.2011.03570.x
Coelho J, Woodford N, Afzal-Shah M, Livermore D (2006) Occurrence of OXA-58-Like carbapenemases in Acinetobacter spp. collected over 10 years in three continents. Antimicrob Agents Chemother 50:756–758. https://doi.org/10.1128/AAC.50.2.756-758.2006
Afzal-Shah M, Woodford N, Livermore DM (2001) Characterization of OXA-25, OXA-26, and OXA-27, molecular class D β-lactamases associated with carbapenem resistance in clinical isolates of Acinetobacter baumannii. Antimicrob Agents Chemother 45:583–588. https://doi.org/10.1128/AAC.45.2.583-588.2001
Ellington MJ, Kistler J, Livermore DM, Woodford N (2007) Multiplex PCR for rapid detection of genes encoding acquired metallo-β-lactamases. J Antimicrob Chemother 59:321–322. https://doi.org/10.1093/jac/dkl481
Zowawi HM, Sartor AL, Sidjabat HE et al (2015) Molecular epidemiology of carbapenem-resistant Acinetobacter baumannii isolates in the Gulf Cooperation Council States: dominance of OXA-23-type producers. J Clin Microbiol 53:896–903. https://doi.org/10.1128/JCM.02784-14
Ni W, Han Y, Zhao J et al (2016) Tigecycline treatment experience against multidrug-resistant Acinetobacter baumannii infections: a systematic review and meta-analysis. Int J Antimicrob Agents 47:107–116. https://doi.org/10.1016/j.ijantimicag.2015.11.011
Wang J, Pan Y, Shen J, Xu Y (2017) The efficacy and safety of tigecycline for the treatment of bloodstream infections: a systematic review and meta-analysis. Ann Clin Microbiol Antimicrob 16:24. https://doi.org/10.1186/s12941-017-0199-8
Al Johani SM, Akhter J, Balkhy H et al (2010) Prevalence of antimicrobial resistance among gram-negative isolates in an adult intensive care unit at a tertiary care center in Saudi Arabia. Ann Saudi Med 30:364–369. https://doi.org/10.4103/0256-4947.67073
Al-Sweih NA, Al-Hubail M, Rotimi VO (2012) Three distinct clones of carbapenem-resistant Acinetobacter baumannii with high diversity of carbapenemases isolated from patients in two hospitals in Kuwait. J Infect Public Health 5:102–108. https://doi.org/10.1016/j.jiph.2011.11.004
Al-Agamy MH, Jeannot K, El-Mahdy TS et al (2017) First detection of GES-5 carbapenemase-producing Acinetobacter baumannii isolate. Microb Drug Resist 23:556–562. https://doi.org/10.1089/mdr.2016.0152
Al-Agamy MH, Shibl AM, Ali MS et al (2014) Distribution of β-lactamases in carbapenem-non-susceptible Acinetobacter baumannii in Riyadh, Saudi Arabia. J Glob Antimicrob Resist 2:17–21. https://doi.org/10.1016/j.jgar.2013.08.004
El-Mahdy TS, Al-Agamy MH, Al-Qahtani AA, Shibl AM (2017) Detection of blaOXA-23-like and blaNDM-1 in Acinetobacter baumannii from the Eastern Region, Saudi Arabia. Microb Drug Resist 23:115–121. https://doi.org/10.1089/mdr.2015.0304
Al-Sweih NA, Al-Hubail MA, Rotimi VO (2011) Emergence of tigecycline and colistin resistance in acinetobacter species isolated from patients in Kuwait hospitals. J Chemother 23:13–16. https://doi.org/10.1179/joc.2011.23.1.13
Abdulzahra AT, Khalil MAF, Elkhatib WF (2018) First report of colistin resistance among carbapenem-resistant Acinetobacter baumannii isolates recovered from hospitalized patients in Egypt. New Microb New Infect 26:53–58. https://doi.org/10.1016/j.nmni.2018.08.007
Liu J-Y, Wang F-D, Ho M-W et al (2016) In vitro activity of aminoglycosides against clinical isolates of Acinetobacter baumannii complex and other nonfermentative Gram-negative bacilli causing healthcare-associated bloodstream infections in Taiwan. J Microbiol Immunol Infect 49:918–923. https://doi.org/10.1016/j.jmii.2015.07.010
Güler G, Eraç B (2016) Investigation of fluoroquinolone resistance mechanisms in clinical Acinetobacter baumannii isolates. Mikrobiyol Bul 50:278–286
Aly MM, Abu Alsoud NM, Elrobh MS et al (2016) High prevalence of the PER-1 gene among carbapenem-resistant Acinetobacter baumannii in Riyadh, Saudi Arabia. Eur J Clin Microbiol Infect Dis 35:1759–1766. https://doi.org/10.1007/s10096-016-2723-8
Alyamani EJ, Khiyami MA, Booq RY et al (2015) Molecular characterization of extended-spectrum beta-lactamases (ESBLs) produced by clinical isolates of Acinetobacter baumannii in Saudi Arabia. Ann Clin Microbiol Antimicrob 14:38. https://doi.org/10.1186/s12941-015-0098-9
Evans BA, Hamouda A, Amyes SGB (2013) The rise of carbapenem-resistant Acinetobacter baumannii. Curr Pharm Des 19:223–238
Alsultan AA, Evans BA, Elsayed EA et al (2013) High frequency of carbapenem-resistant Acinetobacter baumannii in patients with diabetes mellitus in Saudi Arabia. J Med Microbiol 62:885–888. https://doi.org/10.1099/jmm.0.057216-0
Agoba EE, Govinden U, Peer AKC et al (2018) ISAba1 regulated OXA-23 carbapenem resistance in Acinetobacter baumannii strains in Durban, South Africa. Microb Drug Resist 24:1289–1295. https://doi.org/10.1089/mdr.2017.0172
Segal H, Jacobson RK, Garny S et al (2007) Extended −10 promoter in ISAba-1 upstream of blaOXA-23 from Acinetobacter baumannii. Antimicrob Agents Chemother 51:3040–3041. https://doi.org/10.1128/AAC.00594-07
Martínez P, Mattar S (2012) Imipenem-resistant Acinetobacter baumannii carrying the ISAba1-blaOXA-23,51 and ISAba1-blaADC-7 genes in Monteria, Colombia. Braz J Microbiol 43:1274–1280. https://doi.org/10.1590/S1517-83822012000400006
El-Ageery SM, Al-Hazmi SS (2014) Microbiological and molecular detection of VIM-1 metallo beta lactamase-producing Acinetobacter baumannii. Eur Rev Med Pharmacol Sci 18:965–970
Gomaa FAM, Helal ZH, Khan MI (2017) High prevalence of blaNDM-1, blaVIM, qacE, and qacEΔ1 genes and their association with decreased susceptibility to antibiotics and common hospital biocides in clinical isolates of Acinetobacter baumannii. Microorganisms. https://doi.org/10.3390/microorganisms5020018
Pillonetto M, Arend L, Vespero EC et al (2014) First report of NDM-1-producing Acinetobacter baumannii sequence type 25 in Brazil. Antimicrob Agents Chemother 58:7592–7594. https://doi.org/10.1128/AAC.03444-14
Ramirez MS, Nikolaidis N, Tolmasky ME (2013) Rise and dissemination of aminoglycoside resistance: the aac(6′)-Ib paradigm. Front Microbiol. https://doi.org/10.3389/fmicb.2013.00121
Detection of KPC in Acinetobacter spp. in Puerto Rico | Antimicrobial Agents and Chemotherapy. https://aac.asm.org/content/54/3/1354. Accessed 31 Oct 2019
Comparative genome sequence analysis of multidrug-resistant Acinetobacter baumannii. - PubMed - NCBI. https://www.ncbi.nlm.nih.gov/pubmed/18931120. Accessed 31 Oct 2019
Acknowledgements
This work was funded by the deanship of scientific research, Imam Abdulrahman Bin Faisal University, Dammam, Saudi Arabia (IRB-PGS-2018-03-178). We would like to thank the technical staff at the Microbiology Lab of King Fahad University Hospital, especially Mr. Untoy Rashan, for his help with isolate collection.
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AlAmri, A.M., AlQurayan, A.M., Sebastian, T. et al. Molecular Surveillance of Multidrug-Resistant Acinetobacter baumannii. Curr Microbiol 77, 335–342 (2020). https://doi.org/10.1007/s00284-019-01836-z
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DOI: https://doi.org/10.1007/s00284-019-01836-z