Carbapenem resistance in Acinetobacter baumannii clinical isolates from northwest Iran: high prevalence of OXA genes in sync
-
Abolfazl Vahhabi
,
Alka Hasani
,
Mohammad Ahangarzadeh Rezaee
,
Behzad Baradaran
,
Akbar Hasani
,
Hossein Samadi Kafil
,
Elgar Soltani
Abstract
Background and Objectives: Carbapenem treatment for Acinetobacter baumannii infections presently faces threats owing to the production of several types of carbapenemase enzymes, prevalence of which varies among different countries. We explored the current trend of antibiotic resistance in A. baumannii clinical isolates from North West Iran, sought the mechanism of carbapenem resistance and addressed the sequence type groups in carbapenem resistant A. baumannii (CRAB).
Materials and Methods: A. baumannii (n=112) isolates were recovered from various clinical specimens of patients admitted in internal, surgery, burn, infectious diseases and various ICUs wards. Genetically confirmed A. baumannii isolates were screened for carbapenem resistance by the Kirby-Bauer and E-test and the presence of blaMBL, blaOXA-like, ISAba1 genes by PCR. Sequence groups were identified by multiplex PCR.
Results: Multidrug-resistance (MDR) was a characteristic feature of all A. baumannii isolates. Frequency of oxacillinase genes in combination including blaOXA-51-like/blaOXA-23-like, blaOXA-51-like/blaOXA-24/40-like and blaOXA-51-like/blaOXA-23-like/blaOXA-24/40-like was 82.1%, 36.6% and 25.8% respectively. Blending of oxacillinase and MBL genes was evident in eight blaOXA-23-like positive and 7 blaOXA-24-like positive isolates thereby depicting synchronous etiology of carbapenem resistance. Amongst CRAB isolates, 97.3% contained ISAba1 element and 50.9% belonged to the European clone II.
Conclusion: Synchronicity among blaOXA-like with blaMBL and ISAba1 gene was a hallmark of this investigation. Though origin or route of transmission was not elucidated in this study but co-existence among OXA and MBL producing genes is a therapeutic concern demanding strict surveillance strategies and control programs to halt the dissemination of these isolates in the hospital setting.
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2. Poirel L, Nordmann P. Carbapenem resistance in Acinetobacter baumannii: mechanisms and epidemiology. Clin Microbiol Infect 2006;12:826-836.
3. Walsh TR, Toleman MA, Poirel L, Nordmann P. Metallo-beta-lactamases: the quiet before the storm? Clin Microbiol Rev 2005;18:306-325.
4. Lee CR, Lee JH, Park M, Park KS, Bae IK, Kim YB, et al. Biology of Acinetobacter baumannii: pathogenesis, antibiotic resistance mechanisms, and prospective treatment options. Front Cell Infect Microbiol 2017;7:55.
5. Poirel L, Naas T, Nordmann P. Diversity, epidemiology, and genetics of class D beta-lactamases. Antimicrob Agents Chemother 2010;54:24-38.
6. Higgins PG, Lehmann M, Seifert H. Inclusion of OXA-143 primers in a multiplex polymerase chain reaction (PCR) for genes encoding prevalent OXA carbapenemases in Acinetobacter spp. Int J Antimicrob Agents 2010;35:305.
7. Higgins PG, Pérez-Llarena FJ, Zander E, Fernández A, Bou G, Seifert H. OXA-235, a novel class D β-lactamase involved in resistance to carbapenems in Acinetobacter baumannii. Antimicrob Agents Chemother 2013;57:2121-2126.
8. Turton JF, Ward ME, Woodford N, Kaufmann ME, Pike R, Livermore DM, et al. The role of ISAba1 in expression of OXA carbapenemase genes in Acinetobacter baumannii. FEMS Microbiol Lett 2006;258:72-77.
9. Turton J, Gabriel SN, Valderrey C, Kaufmann ME, Pitt TL. Use of sequence‐based typing and multiplex PCR to identify clonal lineages of outbreak strains of Acinetobacter baumannii. Clin Microbiol Infect 2007;13:807-815.
10. Hall GS (2015). Bailey & Scott’s Diagnostic Microbiology. 13th ed. American Society for Clinical Pathology. Chicago.
11. Higgins PG, Lehmann M, Wisplinghoff H, Seifert H. gyrB multiplex PCR to differentiate between Acinetobacter calcoaceticus and Acinetobacter genomic species 3. J Clin Microbiol 2010;48:4592-4594.
12. Gundi VAKB, Dijkshoorn L, Burignat S, Raoult D, La Scola B. Validation of partial rpoB gene sequence analysis for the identification of clinically important and emerging Acinetobacter species. Microbiology (Reading) 2009;155:2333-2341.
13. Wayne P (2018). Clinical and Laboratory Standards Institute (CLSI). Performance standards for antimicrobial susceptibility testing. 28th ed. CLSI supplement M100s.
14. Magiorakos AP, Srinivasan A, Carey RB, Carmeli Y, Falagas ME, Giske CG, et al. Multidrug‐resistant, extensively drug‐resistant and pandrug‐resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect 2012;18:268-281.
15. Shoja S, Moosavian M, Rostami S, Abbasi F, Tabatabaiefar MA, Peymani A. Characterization of oxacillinase and metallo-β-lactamas genes and molecular typing of clinical isolates of Acinetobacter baumannii in Ahvaz, south-west of Iran. Jundishapur J Microbiol 2016;9(5):e32388.
16. Woodford N, Ellington MJ, Coelho JM, Turton JF, Ward ME, Brown S, et al. Multiplex PCR for genes encoding prevalent OXA carbapenemases in Acinetobacter spp. Int J Antimicrob Agents 2006;27:351-353.
17. Poirel L, Walsh TR, Cuvillier V, Nordmann P. Multiplex PCR for detection of acquired carbapenemase genes. Diagn Microbiol Infect Dis 2011;70:119-123.
18. Nordmann P, Poirel L, Carrër A, Toleman MA, Walsh TR. How to detect NDM-1 producers. J Clin Microbiol 2011;49:718-721.
19. Sohrabi N, Farajnia S, Akhi MT, Nahaei MR, Naghili B, Peymani A, et al. Prevalence of OXA-type β-lactamases among Acinetobacter baumannii isolates from northwest of Iran. Microb Drug Resist 2012;18:385-389.
20. Maspi H, Mahmoodzadeh Hosseini H, Amin M, Imani Fooladi AA. High prevalence of extensively drug-resistant and metallo beta-lactamase-producing clinical Acinetobacter baumannii in Iran. Microb Pathog 2016;98:155-159.
21. Rynga D, Shariff M, Deb M. Phenotypic and molecular characterization of clinical isolates of Acinetobacter baumannii isolated from Delhi, India. Ann Clin Microbiol Antimicrob 2015;14:40.
22. Elabd FM, Al-Ayed MSZ, Asaad AM, Alsareii SA, Qureshi MA, Musa HA. Molecular characterization of oxacillinases among carbapenem-resistant Acinetobacter baumannii nosocomial isolates in a Saudi hospital. J Infect Public Health 2015;8:242-247.
23. Aksoy MD, Çavuşlu Ş, Tuğrul HM. Investigation of metallo beta lactamases and oxacilinases in carbapenem resistant Acinetobacter baumannii strains isolated from inpatients. Balkan Med J 2015;32:79-83.
24. Nowak P, Paluchowska P, Budak A. Distribution of blaOXA genes among carbapenem-resistant Acinetobacter baumannii nosocomial strains in Poland. New Microbiol 2012;35:317-325.
25. Feizabadi MM, Fathollahzadeh B, Taherikalani M, Rasoolinejad M, Sadeghifard N, Aligholi M, et al. Antimicrobial susceptibility patterns and distribution of blaOXA genes among Acinetobacter spp. isolated from patients at Tehran hospitals. Jpn J Infect Dis 2008;61:274-278.
26. Al-Sweih NA, Al-Hubail M, Rotimi VO. 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 2012;5:102-108.
27. Villalón P, Valdezate S, Medina-Pascual MJ, Carrasco G, Vindel A, Saez-Nieto JA. Epidemiology of the Acinetobacter-derived cephalosporinase, carbapenem-hydrolysing oxacillinase and metallo-β-lactamase genes, and of common insertion sequences, in epidemic clones of Acinetobacter baumannii from Spain. J Antimicrob Chemother 2013;68:550-553.
28. Savari M, Ekrami A, Shoja S, Bahador A. Plasmid borne Carbapenem-Hydrolyzing Class D β-Lactamases (CHDLs) and AdeABC efflux pump conferring carbapenem-tigecycline resistance among Acinetobacter baumannii isolates harboring TnAbaRs. Microb Pathog 2017;104:310-317.
29. Sarhaddi N, Soleimanpour S, Farsiani H, Mosavat A, Dolatabadi S, Salimizand H, et al. Elevated prevalence of multidrug-resistant Acinetobacter baumannii with extensive genetic diversity in the largest burn centre of northeast Iran. J Glob Antimicrob Resist 2017;8:60-66.
30. Farshadzadeh Z, Hashemi FB, Rahimi S, Pourakbari B, Esmaeili D, Haghighi MA, et al. Wide distribution of carbapenem resistant Acinetobacter baumannii in burns patients in Iran. Front Microbiol 2015;6:1146.
31. Khorsi K, Messai Y, Hamidi M, Ammari H, Bakour R. High prevalence of multidrug-resistance in Acinetobacter baumannii and dissemination of carbapenemase-encoding genes blaOXA-23-like, blaOXA-24-like and blaNDM-1 in Algiers hospitals. Asian Pac J Trop Med 2015;8:438-446.
32. Hadjadj L, Bakour S, Rolain JM. Co-occurrence of carbapenemase encoding genes in Acinetobacter baumannii, a dream or reality? BMC Microbiol 2018;18:107.
33. Nemec A, Křížová L, Maixnerova M, Diancourt L, van der Reijden TJ, Brisse S, et al. Emergence of carbapenem resistance in Acinetobacter baumannii in the Czech Republic is associated with the spread of multidrug-resistant strains of European clone II. J Antimicrob Chemother 2008;62:484-489.
34. Higgins PG, Dammhayn C, Hackel M, Seifert H. Global spread of carbapenem-resistant Acinetobacter baumannii. J Antimicrob Chemother 2010;65:233-238.
2. Poirel L, Nordmann P. Carbapenem resistance in Acinetobacter baumannii: mechanisms and epidemiology. Clin Microbiol Infect 2006;12:826-836.
3. Walsh TR, Toleman MA, Poirel L, Nordmann P. Metallo-beta-lactamases: the quiet before the storm? Clin Microbiol Rev 2005;18:306-325.
4. Lee CR, Lee JH, Park M, Park KS, Bae IK, Kim YB, et al. Biology of Acinetobacter baumannii: pathogenesis, antibiotic resistance mechanisms, and prospective treatment options. Front Cell Infect Microbiol 2017;7:55.
5. Poirel L, Naas T, Nordmann P. Diversity, epidemiology, and genetics of class D beta-lactamases. Antimicrob Agents Chemother 2010;54:24-38.
6. Higgins PG, Lehmann M, Seifert H. Inclusion of OXA-143 primers in a multiplex polymerase chain reaction (PCR) for genes encoding prevalent OXA carbapenemases in Acinetobacter spp. Int J Antimicrob Agents 2010;35:305.
7. Higgins PG, Pérez-Llarena FJ, Zander E, Fernández A, Bou G, Seifert H. OXA-235, a novel class D β-lactamase involved in resistance to carbapenems in Acinetobacter baumannii. Antimicrob Agents Chemother 2013;57:2121-2126.
8. Turton JF, Ward ME, Woodford N, Kaufmann ME, Pike R, Livermore DM, et al. The role of ISAba1 in expression of OXA carbapenemase genes in Acinetobacter baumannii. FEMS Microbiol Lett 2006;258:72-77.
9. Turton J, Gabriel SN, Valderrey C, Kaufmann ME, Pitt TL. Use of sequence‐based typing and multiplex PCR to identify clonal lineages of outbreak strains of Acinetobacter baumannii. Clin Microbiol Infect 2007;13:807-815.
10. Hall GS (2015). Bailey & Scott’s Diagnostic Microbiology. 13th ed. American Society for Clinical Pathology. Chicago.
11. Higgins PG, Lehmann M, Wisplinghoff H, Seifert H. gyrB multiplex PCR to differentiate between Acinetobacter calcoaceticus and Acinetobacter genomic species 3. J Clin Microbiol 2010;48:4592-4594.
12. Gundi VAKB, Dijkshoorn L, Burignat S, Raoult D, La Scola B. Validation of partial rpoB gene sequence analysis for the identification of clinically important and emerging Acinetobacter species. Microbiology (Reading) 2009;155:2333-2341.
13. Wayne P (2018). Clinical and Laboratory Standards Institute (CLSI). Performance standards for antimicrobial susceptibility testing. 28th ed. CLSI supplement M100s.
14. Magiorakos AP, Srinivasan A, Carey RB, Carmeli Y, Falagas ME, Giske CG, et al. Multidrug‐resistant, extensively drug‐resistant and pandrug‐resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect 2012;18:268-281.
15. Shoja S, Moosavian M, Rostami S, Abbasi F, Tabatabaiefar MA, Peymani A. Characterization of oxacillinase and metallo-β-lactamas genes and molecular typing of clinical isolates of Acinetobacter baumannii in Ahvaz, south-west of Iran. Jundishapur J Microbiol 2016;9(5):e32388.
16. Woodford N, Ellington MJ, Coelho JM, Turton JF, Ward ME, Brown S, et al. Multiplex PCR for genes encoding prevalent OXA carbapenemases in Acinetobacter spp. Int J Antimicrob Agents 2006;27:351-353.
17. Poirel L, Walsh TR, Cuvillier V, Nordmann P. Multiplex PCR for detection of acquired carbapenemase genes. Diagn Microbiol Infect Dis 2011;70:119-123.
18. Nordmann P, Poirel L, Carrër A, Toleman MA, Walsh TR. How to detect NDM-1 producers. J Clin Microbiol 2011;49:718-721.
19. Sohrabi N, Farajnia S, Akhi MT, Nahaei MR, Naghili B, Peymani A, et al. Prevalence of OXA-type β-lactamases among Acinetobacter baumannii isolates from northwest of Iran. Microb Drug Resist 2012;18:385-389.
20. Maspi H, Mahmoodzadeh Hosseini H, Amin M, Imani Fooladi AA. High prevalence of extensively drug-resistant and metallo beta-lactamase-producing clinical Acinetobacter baumannii in Iran. Microb Pathog 2016;98:155-159.
21. Rynga D, Shariff M, Deb M. Phenotypic and molecular characterization of clinical isolates of Acinetobacter baumannii isolated from Delhi, India. Ann Clin Microbiol Antimicrob 2015;14:40.
22. Elabd FM, Al-Ayed MSZ, Asaad AM, Alsareii SA, Qureshi MA, Musa HA. Molecular characterization of oxacillinases among carbapenem-resistant Acinetobacter baumannii nosocomial isolates in a Saudi hospital. J Infect Public Health 2015;8:242-247.
23. Aksoy MD, Çavuşlu Ş, Tuğrul HM. Investigation of metallo beta lactamases and oxacilinases in carbapenem resistant Acinetobacter baumannii strains isolated from inpatients. Balkan Med J 2015;32:79-83.
24. Nowak P, Paluchowska P, Budak A. Distribution of blaOXA genes among carbapenem-resistant Acinetobacter baumannii nosocomial strains in Poland. New Microbiol 2012;35:317-325.
25. Feizabadi MM, Fathollahzadeh B, Taherikalani M, Rasoolinejad M, Sadeghifard N, Aligholi M, et al. Antimicrobial susceptibility patterns and distribution of blaOXA genes among Acinetobacter spp. isolated from patients at Tehran hospitals. Jpn J Infect Dis 2008;61:274-278.
26. Al-Sweih NA, Al-Hubail M, Rotimi VO. 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 2012;5:102-108.
27. Villalón P, Valdezate S, Medina-Pascual MJ, Carrasco G, Vindel A, Saez-Nieto JA. Epidemiology of the Acinetobacter-derived cephalosporinase, carbapenem-hydrolysing oxacillinase and metallo-β-lactamase genes, and of common insertion sequences, in epidemic clones of Acinetobacter baumannii from Spain. J Antimicrob Chemother 2013;68:550-553.
28. Savari M, Ekrami A, Shoja S, Bahador A. Plasmid borne Carbapenem-Hydrolyzing Class D β-Lactamases (CHDLs) and AdeABC efflux pump conferring carbapenem-tigecycline resistance among Acinetobacter baumannii isolates harboring TnAbaRs. Microb Pathog 2017;104:310-317.
29. Sarhaddi N, Soleimanpour S, Farsiani H, Mosavat A, Dolatabadi S, Salimizand H, et al. Elevated prevalence of multidrug-resistant Acinetobacter baumannii with extensive genetic diversity in the largest burn centre of northeast Iran. J Glob Antimicrob Resist 2017;8:60-66.
30. Farshadzadeh Z, Hashemi FB, Rahimi S, Pourakbari B, Esmaeili D, Haghighi MA, et al. Wide distribution of carbapenem resistant Acinetobacter baumannii in burns patients in Iran. Front Microbiol 2015;6:1146.
31. Khorsi K, Messai Y, Hamidi M, Ammari H, Bakour R. High prevalence of multidrug-resistance in Acinetobacter baumannii and dissemination of carbapenemase-encoding genes blaOXA-23-like, blaOXA-24-like and blaNDM-1 in Algiers hospitals. Asian Pac J Trop Med 2015;8:438-446.
32. Hadjadj L, Bakour S, Rolain JM. Co-occurrence of carbapenemase encoding genes in Acinetobacter baumannii, a dream or reality? BMC Microbiol 2018;18:107.
33. Nemec A, Křížová L, Maixnerova M, Diancourt L, van der Reijden TJ, Brisse S, et al. Emergence of carbapenem resistance in Acinetobacter baumannii in the Czech Republic is associated with the spread of multidrug-resistant strains of European clone II. J Antimicrob Chemother 2008;62:484-489.
34. Higgins PG, Dammhayn C, Hackel M, Seifert H. Global spread of carbapenem-resistant Acinetobacter baumannii. J Antimicrob Chemother 2010;65:233-238.
| Files | ||
| Issue | Vol 13 No 3 (2021) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v13i3.6388 | |
| Keywords | ||
| Acinetobacter baumannii; Carbapenems; Carbapenemase; Oxacillinase; Beta-lactamase; Drug resistance; Multiplex polymerase chain reaction | ||
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This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
How to Cite
1.
Vahhabi A, Hasani A, Ahangarzadeh Rezaee M, Baradaran B, Hasani A, Samadi Kafil H, Soltani E. Carbapenem resistance in Acinetobacter baumannii clinical isolates from northwest Iran: high prevalence of OXA genes in sync. Iran J Microbiol. 2021;13(3):282-293.
