Abstract
Acinetobacter baumannii was reported as a frequent pathogen leading to outbreaks of multidrug-resistant organisms both in the intensive care unit (ICU) and in non-ICU units during the coronavirus disease in 2019 (COVID-19). In this study we aimed to examine the phenotypic and molecular characteristics of clinical isolates of carbapenem-resistant A. baumannii (CrAb) obtained from Siirt Training Hospital in Siirt, Türkiye, during the Covid-19 pandemic. In our study, 31.6% of the patients whose culture was taken were Covid-19 positive. Of the 57 CrAb strains tested for antibiotic resistance, 52 (91.2%) showed extensive-drug resistance (XDR), 4 (7%) multi-drug resistance (MDR), and 1 (1.8%) pan-drug resistance (PDR). According to 16 S rRNA analysis, the sequences of the CrAb strains used in our study were 99–100% similar to the 16 S rRNA genes of the A. baumannii strains registered in GenBank. The most frequently detected carbapenem resistance gene in the species in our study was the OXA51 gene (85.7%). It’s interesting to note that the blaNDM gene, which has a direct connection to the Indian Subcontinent and has recently been observed in the Middle East but has been rarely detected in Türkiye, was discovered in our study at a high rate. We think that this situation is caused by migration from the Middle East due to war in recent years. Additionally, we believe that horizontal gene transfer between bacteria is the cause of the high frequency of the blaVIM gene, whose source is primarily Pseudomonas species, in A. baumannii species in our study.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The corresponding author will provide the datasets used and/or analyzed during the current work upon reasonable request.
Abbreviations
- CrAb:
-
Carbapenem-resistant A. baumannii
- XDR:
-
Extensive-drug resistance
- MDR:
-
Multi-drug resistance
- PDR:
-
Pan-drug resistance
- IMP:
-
Imipenemase Seoul
- SIM:
-
Imipenemase
- VIM:
-
Verona integron-encoded metallo-?-lactamase
- NDM:
-
New Delhi Metallo-?-lactamase
- MBLs:
-
Metallo-?-lactamases
- OXAs:
-
Oxacillinases
- CHDLs:
-
Carbapenem-hydrolyzing class D?-lactamases
- COVID-19:
-
Coronavirus disease 2019
- ICU:
-
Intensive care unit
- PCR:
-
polymerase chain reaction
- NCBI:
-
National Center for Biotechnology Information
- BLAST:
-
Basic Local Alignment Search Tool
- MIC:
-
Minimal inhibitory concentration
- blaKPC:
-
Klebsiella pneumoniae carbapenemase
References
Abbo A, Navon-Venezia S, Hammer-Muntz O, Krichali T, Siegman-Igra Y, Carmeli Y (2005) Multidrug-resistant Acinetobacter baumannii. Emerg Infect Dis 11:22–29. https://doi.org/10.3201/eid1101.040001
Abouelfetouh A, Torky AS, Aboulmagd E (2019) Phenotypic and genotypic characterization of carbapenem-resistant Acinetobacter baumannii isolates from Egypt. Antimicrob Resist Infect Control 8:1–9. https://doi.org/10.1016/j.matpr.2021.07.347
Acer Ö, Genc Bahce Y, Özüdoğru O (2022) Association of viral load with age, gender, disease severity, and death in severe acute respiratory syndrome coronavirus 2 variants. J Med Virol 94:3063–3069. https://doi.org/10.1002/jmv.27677
Asgin N, Otlu B, Cakmakliogullari EK, Celik B (2019) High prevalence of TEM, VIM, and OXA-2 beta-lactamases and clonal diversity among Acinetobacter baumannii isolates in Turkey. J Infect Dev Countr 13:794–801. https://doi.org/10.3855/jidc.11684
Avila-Novoa M-G, Solís-Velázquez O-A, Rangel-Lopez D-E, González-Gómez J-P, Guerrero-Medina P-J, Gutiérrez-Lomelí M (2019) Biofilm formation and detection of fluoroquinolone-and carbapenem-resistant genes in multidrug-resistant Acinetobacter baumannii. Can J Infect Dis Med Microbiol 2019(2019). https://doi.org/10.1155/2019/3454907
Bahçe YG, Acer Ö, Özüdoğru O (2022) Evaluation of bacterial agents isolated from endotracheal aspirate cultures of Covid-19 general intensive care patients and their antibiotic resistance profiles compared to pre-pandemic conditions. Microb Pathog 164(2022):105409. https://doi.org/10.1016/j.micpath.2022.105409
Benmahmod AB, Said HS, Ibrahim RH (2019) Prevalence and mechanisms of carbapenem resistance among Acinetobacter baumannii clinical isolates in Egypt. Microb Drug Resist 25:480–488. https://doi.org/10.1089/mdr.2018.0141
Beriş FŞ, Budak EE, Gülek D, Uzun A, Cizmeci Z, Mengeloğlu FZ, Direkel Ş, Cetinkol Y, Altıntop A, Iraz M (2016) Investigation of the frequency and distribution of beta-lactamase genes in the clinical isolates of Acinetobacter baumannii collected from different regions of Turkey: a multicenter study. Mikrobiyol Bul 50:511–521. https://doi.org/10.5578/mb.29176
Bonnin R, Poirel L, Naas T, Pirs M, Seme K, Schrenzel J, Nordmann P (2012) Dissemination of New Delhi metallo-β-lactamase-1-producing Acinetobacter baumannii in Europe. Clin Microbiol Infect 18:E362–E365. https://doi.org/10.1111/j.1469-0691.2012.03928.x
Ceparano M, Baccolini V, Migliara G, Isonne C, Renzi E, Tufi D, De Vito C, De Giusti M, Trancassini M, Alessandri F (2022) Acinetobacter baumannii isolates from COVID-19 patients in a hospital intensive care unit: molecular typing and risk factors. Microorganisms 10:722. https://doi.org/10.3390/microorganisms10040722
Cicek AC, Saral A, Iraz M, Ceylan A, Duzgun A, Peleg AY, Sandalli C (2014) OXA-and GES-type β-lactamases predominate in extensively drug-resistant Acinetobacter baumannii isolates from a Turkish University Hospital. Clin Microbiol Infect 20:410–415. https://doi.org/10.1111/1469-0691.12338
Cornaglia G, Giamarellou H, Rossolini GM (2011) Metallo-β-lactamases: a last frontier for β-lactams? The Lancet Infect Dis 11:381–393. https://doi.org/10.1016/S1473-3099(11)70056-1
Coskun USS, Caliskan E, Cicek AC, Turumtay H, Sandalli C (2019) β-lactamase genes in carbapenem resistance Acinetobacter baumannii isolates from a Turkish university hospital. J Infect Dev Countr 13:50–55. https://doi.org/10.3855/jidc.10556
Daikos GL, Petrikkos P, Psichogiou M, Kosmidis C, Vryonis E, Skoutelis A, Georgousi K, Tzouvelekis LS, Tassios PT, Bamia C (2009) Prospective observational study of the impact of VIM-1 metallo-β-lactamase on the outcome of patients with Klebsiella pneumoniae bloodstream infections. Antimicrob Agents Chemother 53:1868–1873. https://doi.org/10.1128/aac.00782-08
Doughari HJ, Ndakidemi PA, Human IS, Benade S (2011) The ecology, biology and pathogenesis of Acinetobacter spp.: an overview. Microbes Environ 26:101–112. https://doi.org/10.1264/jsme2.ME10179
Durán-Manuel EM, Cruz-Cruz C, Ibáñez-Cervantes G, Bravata-Alcantará JC, Sosa-Hernandez O, Delgado-Balbuena L, León-García G, Cortés-Ortíz IA, Cureño-Díaz MA, Castro-Escarpulli G (2021) Clonal dispersion of Acinetobacter baumannii in an intensive care unit designed to patients COVID-19. J Infect Dev Countr 15:58–68. https://doi.org/10.3855/jidc.13545
El-Shazly S, Dashti A, Vali L, Bolaris M, Ibrahim AS (2015) Molecular epidemiology and characterization of multiple drug-resistant (MDR) clinical isolates of Acinetobacter baumannii. Int J Infect Dis 41:42–49. https://doi.org/10.1016/j.ijid.2015.10.016
Ergin A, Hascelik G, Eser OK (2013) Molecular characterization of oxacillinases and genotyping of invasive Acinetobacter baumannii isolates using repetitive extragenic palindromic sequence-based polymerase chain reaction in Ankara between 2004 and 2010. Scand J Infect Dis 45:26–31. https://doi.org/10.3109/00365548.2012.708782
Fattouh M, El-Din AN (2014) Emergence of carbapenem-resistant Acinetobacter baumannii in the intensive care unit in Sohag university hospital, Egypt. Int J Curr Microbiol Appl Sci 3:732–744
Girija SA, Jayaseelan VP, Arumugam P (2018) Prevalence of VIM-and GIM-producing Acinetobacter baumannii from patients with severe urinary tract infection. Acta Microbiol Immunol Hung 65:539–550. https://doi.org/10.1556/030.65.2018.038
Gozalan A, Unaldı O, Guldemir D, Aydogan S, Kuzucu C, Cakirlar FK, Açıkgoz ZC, Durmaz R (2021) Molecular characterization of carbapenem-resistant Acinetobacter baumannii blood culture isolates from three hospitals in Turkey. Jpn J Infect Dis 74:200–208. https://doi.org/10.7883/yoken.JJID.2020.478
Hasan B, Perveen K, Olsen B, Zahra R (2014) Emergence of carbapenem-resistant Acinetobacter baumannii in hospitals in Pakistan. J Med Microbiol 63:50–55. https://doi.org/10.1099/jmm.0.063925-0
Hasani A, Rezaee MA, Baradaran B, Hasani A, Ka HS, Abbaszadeh F (2021) Expression of Efflux Pumps, Porins and Genotypic Insight Into the Carbapenem Resistance in Acinetobacter Baumannii. https://doi.org/10.21203/rs.3.rs-573246/v1
Heydari F, Mammina C, Koksal F (2015) NDM-1-producing Acinetobacter baumannii ST85 now in Turkey, including one isolate from a Syrian refugee. J Med Microbiol 64:1027–1029
Hou C, Yang F (2015) Drug-resistant gene of blaOXA-23, blaOXA-24, blaOXA-51 and blaOXA-58 in Acinetobacter baumannii. Int J Clin Exp Med 8:13859
Jeon JH, Lee JH, Lee JJ, Park KS, Karim AM, Lee C-R, Jeong BC, Lee SH (2015) Structural basis for carbapenem-hydrolyzing mechanisms of carbapenemases conferring antibiotic resistance. Int J Mol Sci 16:9654–9692. https://doi.org/10.3390/ijms16059654
Karampatakis T, Antachopoulos C, Tsakris A, Roilides E (2017) Molecular epidemiology of carbapenem-resistant Acinetobacter baumannii in Greece: an extended review (2000–2015). Future Microbiol 12:801–815. https://doi.org/10.2217/fmb-2016-0200
Karataş M, Yaşar-Duman M, Tünger A, Çilli F, Aydemir Ş, Özenci V (2021) Secondary bacterial infections and antimicrobial resistance in COVID-19: comparative evaluation of pre-pandemic and pandemic-era, a retrospective single center study. Ann Clin Microbiol Antimicrob 20:1–8. https://doi.org/10.1186/s12941-021-00454-7
Keskin H, Tekeli A, Öcal D (2014) Klinik örneklerden Izole Edilen Acinetobacter baumannii suşlarında beta-laktamaz kaynaklı direncin moleküler karakterizasyonu. Mikrobiyol Bul 48:365–376
Kostyanev T, Xavier BB, García-Castillo M, Lammens C, Acosta JB-F, Rodríguez-Baño J, w, Cantón R, Glupczynski Y, Goossens H (2021) Phenotypic and molecular characterizations of carbapenem-resistant Acinetobacter baumannii isolates collected within the EURECA study. Int J Antimicrob Agents.57:106345. https://doi.org/10.1016/j.ijantimicag.2021.106345
Lai C-C, Wang C-Y, Hsueh P-R (2020) Co-infections among patients with COVID-19: the need for combination therapy with non-anti-SARS-CoV-2 agents? J Microbiol Immunol Infect 53:505–512. https://doi.org/10.1016/j.jmii.2020.05.013
Lee K, Yong D, Jeong SH, Chong Y (2011) Multidrug-resistant Acinetobacter spp.: increasingly problematic nosocomial pathogens. Yonsei Med J 52:879–891. https://doi.org/10.3349/ymj.2011.52.6.879
Liu C, Chen K, Wu Y, Huang L, Fang Y, Lu J, Zeng Y, Xie M, Chan EWC, Chen S (2022) Epidemiological and genetic characteristics of clinical carbapenem-resistant Acinetobacter baumannii strains collected countrywide from hospital intensive care units (ICUs) in China. Emerg Microbes Infect 11:1730–1741. https://doi.org/10.1080/22221751.2022.2093134
Mugnier PD, Poirel L, Naas T, Nordmann P (2010) Worldwide dissemination of the blaOXA-23 carbapenemase gene of Acinetobacter baumannii1. Emerg Infect Dis 16:35–40. https://doi.org/10.3201/eid1601.090852
Mulani MS, Kamble EE, Kumkar SN, Tawre MS, Pardesi KR (2019) Emerging strategies to combat ESKAPE pathogens in the era of antimicrobial resistance: a review. Front Microbiol 10:539. https://doi.org/10.3389/fmicb.2019.00539
Nordmann P, Cuzon G, Naas T (2009) The real threat of Klebsiella pneumoniae carbapenemase-producing bacteria. Lancet Infect Dis 9:228–236. https://doi.org/10.1016/S1473-3099(09)70054-4
Nordmann P, Poirel L, Toleman MA, Walsh TR (2011) Does broad-spectrum β-lactam resistance due to NDM-1 herald the end of the antibiotic era for treatment of infections caused by Gram-negative bacteria? J Antimicrob Chemother 66:689–692. https://doi.org/10.1093/jac/dkq520
Nowak P, Paluchowska PM, Budak A (2014) Co-occurrence of carbapenem and aminoglycoside resistance genes among multidrug-resistant clinical isolates of Acinetobacter baumannii from Cracow. Pol Med Sci Monit Basic Res 20:9–14. https://doi.org/10.12659/MSMBR.889811
Oh K-W, Kim K, Islam MM, Jung H-W, Lim D, Lee JC, Shin M (2020) Transcriptional regulation of the outer membrane protein A. Acinetobacter baumannii Microorganisms 8:706. https://doi.org/10.3390/microorganisms8050706
Peleg AY, Seifert H, Paterson DL (2008) Acinetobacter baumannii: emergence of a successful pathogen. Clin Microbiol Rev 21:538–582. https://doi.org/10.1128/CMR.00058-07
Poirel L, Nordmann P (2006) Carbapenem resistance in Acinetobacter baumannii: mechanisms and epidemiology. Clin Microbiol Infect 12:826–836. https://doi.org/10.1111/j.1469-0691.2006.01456.x
Poirel L, Naas T, Nordmann P (2010) Diversity, epidemiology, and genetics of class D β-lactamases. Antimicrob Agents Chemother 54:24–38. https://doi.org/10.1128/AAC.01512-08
Pustijanac E, Hrenović J, Vranić-Ladavac M, Močenić M, Karčić N, Lazarić Stefanović L, Hrstić I, Lončarić J, Šeruga Musić M, Drčelić M (2023) Dissemination of clinical Acinetobacter baumannii isolate to Hospital Environment during the COVID-19 pandemic. Pathogens 12:410. https://doi.org/10.3390/pathogens12030410
Queenan AM, Bush K (2007) Carbapenemases: the versatile β-lactamases. Clin Microbiol Rev 20:440–458. https://doi.org/10.1128/CMR.00001-07
Rao M, Rashid F, Shukor S, Hashim R, Ahmad N (2020) Detection of Antimicrobial Resistance Genes Associated with Carbapenem Resistance from the whole-genome sequence of Acinetobacter baumannii isolates from Malaysia. Can J Infect Dis Med Microbiol 2020:5021064–5021064. https://doi.org/10.1155/2020/5021064
Rice TW, Rubinson L, Uyeki TM, Vaughn FL, John BB, Miller RR III, Higgs E, Randolph AG, Smoot BE, Thompson BT (2012) Critical illness from 2009 pandemic influenza A (H1N1) virus and bacterial co-infection in the United States. Crit Care Med 40:1487. https://doi.org/10.1097/CCM.0b013e3182416f23
Richet HM, Mohammed J, McDonald LC, Jarvis WR (2001) Building communication networks: international network for the study and prevention of emerging antimicrobial resistance. Emerg Infect Dis 7:319
Shamsizadeh Z, Nikaeen M, Nasr Esfahani B, Mirhoseini SH, Hatamzadeh M, Hassanzadeh A (2017) Detection of antibiotic resistant Acinetobacter baumannii in various hospital environments: potential sources for transmission of Acinetobacter infections. Environ Health Prev Med 22:1–7. https://doi.org/10.1186/s12199-017-0653-4
Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526. https://doi.org/10.1093/oxfordjournals.molbev.a040023
Tamura K, Stecher G, Kumar S (2021) MEGA11: molecular evolutionary genetics analysis version 11. Mol Biol Evol 38:3022–3027. https://doi.org/10.1093/molbev/msab120
Thadtapong N, Chaturongakul S, Soodvilai S, Dubbs P (2021) Colistin and carbapenem-resistant Acinetobacter baumannii Aci46 in Thailand: genome analysis and antibiotic resistance profiling. Antibiotics 10:1054. https://doi.org/10.3390/antibiotics10091054
Thomson KS (2010) Extended-spectrum-β-lactamase, AmpC, and carbapenemase issues. J Clin Microbiol 48:1019–1025. https://doi.org/10.1128/JCM.00219-10
Timothy RW, Mark AT, Laurent P, Patrice N (2005) Metallo-β-Lactamases: the quiet before the storm? Clin Microbiol Rev 18:306–325. https://doi.org/10.1128/CMR.18.2.306-325.2005
Torres A, Niederman MS, Chastre J, Ewig S, Fernandez-Vandellos P, Hanberger H, Kollef M, Bassi GL, Luna CM, Martin-Loeches I (2017) International ERS/ESICM/ESCMID/ALAT guidelines for the management of hospital-acquired pneumonia and ventilator-associated pneumonia: guidelines for the management of hospital-acquired pneumonia (HAP)/ventilator-associated pneumonia (VAP) of the European Respiratory Society (ERS), European Society of Intensive Care Medicine (ESICM), European Society of Clinical Microbiology and Infectious diseases (ESCMID) and Asociación Latinoamericana Del Tórax (ALAT). Eur Respir J 50. https://doi.org/10.1183/13993003.00582-2017
Turton JF, Ward ME, Woodford N, Kaufmann ME, Pike R, Livermore DM, Pitt TL (2006) The role of IS Aba1 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
Vali L, Dashti K, Opazo-Capurro AF, Dashti AA, Al Obaid K, Evans BA (2015) Diversity of multi-drug resistant Acinetobacter baumannii population in a major hospital in Kuwait. Front Microbiol 6:743. https://doi.org/10.3389/fmicb.2015.00743
Whiteway C, Breine A, Philippe C, Van der Henst C (2022) Acinetobacter baumannii. Trends Microbiol 30:199–200
Yap FH, Gomersall CD, Fung KS, Ho P-L, Ho O-M, Lam PK, Lam DT, Lyon DJ, Joynt GM (2004) Increase in methicillin-resistant Staphylococcus aureus acquisition rate and change in pathogen pattern associated with an outbreak of severe acute respiratory syndrome. Clin Infect Dis 39:511–516. https://doi.org/10.1086/422641
Yigit H, Queenan AM, Anderson GJ, Domenech-Sanchez A, Biddle JW, Steward CD, Alberti S, Bush K, Tenover FC (2001) Novel carbapenem-hydrolyzing β-lactamase, KPC-1, from a carbapenem-resistant strain of Klebsiella pneumoniae. Antimicrob Agents Chemother 45:1151–1161. https://doi.org/10.1128/aac.45.4.1151-1161.2001
Yong D, Toleman MA, Giske CG, Cho HS, Sundman K, Lee K, Walsh TR (2009) Characterization of a new metallo-β-lactamase gene, bla NDM-1, and a novel erythromycin esterase gene carried on a unique genetic structure in Klebsiella pneumoniae sequence type 14 from India. Antimicrob Agents Chemother 53:5046–5054. https://doi.org/10.1128/aac.00774-09
Zhang H-z, Zhang J-s, Qiao L (2013) The Acinetobacter baumannii group: a systemic review. World J Emerg Med 4:169. https://doi.org/10.5847/wjem.j.issn.1920-8642.2013.03.002
Zhou F, Yu T, Du R, Fan G, Liu Y, Liu Z, Xiang J, Wang Y, Song B, Gu X (2020) Clinical course and risk factors for mortality of adult inpatients with COVID-19 in Wuhan, China: a retrospective cohort study. Lancet 395:1054–1062. https://doi.org/10.1016/S0140-6736(20)30566-3
Acknowledgements
The study was supported by the Scientific Research Commission of Siirt University (2022-SİÜTIP-013).
Funding
This work was fnancially supported by the Scientific Research Commission of Siirt University (2022-SİÜTIP-013).
Author information
Authors and Affiliations
Contributions
Ö.A.: Investigation, writing, writing-original draft preparation, reviewing, conceptualization methodology, and Bionformatic analysis. Y.G.B.: Investigation, conceptualization, methodology, data curation, and reviewing; O.Ö.: performed investigation, and reviewing.
Corresponding author
Ethics declarations
Ethical approval
This study was approved by the Siirt University Non-Interventional Clinical Research Ethics Committee (Meeting date: 27.01.2022, meeting number: 33833, decision no: 2022/01.01).
Consent to participate
All participants who were enrolled in the study signed the informed consent form.
Consent for publication
Not applicable.
Competing interests
The authors declare no conflicts of interest.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Acer, Ö., Bahçe, Y.G. & Özüdoğru, O. Carbapenem-resistant Acinetobacter baumannii strains in the Covid-19 pandemic: 16 S rRNA analysis, carbapenem resistance genes, and antibiotic resistance profiles. Biologia 79, 1057–1070 (2024). https://doi.org/10.1007/s11756-024-01611-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11756-024-01611-x