First report of SPM metallo-β-lactamases producing Acinetobacter baumannii isolates in Morocco
-
Abdelhamid Massik
,
Lahbib Hibaoui
,
Benboubker Moussa
,
Ghita Yahyaoui
,
Bouchra Oumokhtar
,
Mustapha Mahmoud
Abstract
Background and Objectives: Carbapenem-resistant Acinetobacter baumannii has recently been identified by the World Health Organization as a critical pathogen. We propose to characterize the molecular characteristics of clinical isolates of A. baumannii resistant to carbapenems collected in a Moroccan hospital.
Materials and Methods: Seventy carbapenem-resistant A. baumannii isolates from various samples were received at the microbiology laboratory of the Hospital Center. Antibiotic susceptibility was tested by the diffusion disc method and molecular characterization of antimicrobial resistance was performed by PCR and sequencing.
Results: Carbapenemase genes were detected in our isolates: the OXA-51 gene and the ISbA1 sequence were detected in all isolates (100%), the OXA-23 and OXA-58 genes were detected in 82.85% and 10% of isolates respectively, MBL genes were dominated by VIM 39 isolates (55.7%), followed by GIM 26 isolates (37%), SIM 20 isolates (28.5%), IMP 8 isolates (11, 4%), NDM 3 isolates (4%) and for the first time in Morocco SPM with 4 isolates (5.7%).
Conclusion: The emergence of resistance of A. baumannii to carbapenems is a serious problem in our hospital which requires the establishment of a prevention strategy and strict respect for hygiene to minimize their dissemination.
1. Howard A, O’Donoghue M, Feeney A, Sleator RD. Acinetobacter baumannii: an emerging opportunistic pathogen. Virulence 2012; 3: 243-250.
2. Bergogne-Berezin E, Towner KJ. Acinetobacter spp. as nosocomial pathogens: microbiological, clinical, and epidemiological features. Clin Microbiol Rev 1996; 9: 148-165.
3. Chang WN, Lu CH, Huang CR, Chuang YC. Community-acquired Acinetobacter meningitis in adults. Infection 2000; 28: 395-397.
4. Falagas ME, Karveli EA, Kelesidis I, Kelesidis T. Community-acquired Acinetobacter infections. Eur J Clin Microbiol Infect Dis 2007; 26: 857-868.
5. Heritier C, Poirel L, Nordmann P. Cephalosporinase over-expression resulting from insertion of ISAba1 in Acinetobacter baumannii. Clin Microbiol Infect 2006; 12: 123-130.
6. El Hafa H, Nayme K, El Hamzaoui N, Maroui I, Sbiti M, Zerouali K, et al. Dissemination of carbapenem-resistant Acinetobacter baumannii strains carrying the blaGES, blaNDM and blaOXA23 in Morocco. Germs 2019; 9: 133-141.
7. Grall N, Andremont A, Armand-Lefèvre L. Résistance aux carbapénèmes: vers une nouvelle impasse? Carbapenem resistance: Towards a new dead end? J Anti-Infect 2011; 13: 87-102.
8. Pollini S, Maradei S, Pecile P, Olivo G, Luzzaro F, Docquier J-D, et al. FIM-1, a New Acquired Metallo-β-Lactamase from a Pseudomonas aeruginosa clinical isolate from Italy. Antimicrob Agents Chemother 2013; 57: 410-416.
9. Lee K, Chong Y, Shin HB, Kim YA, Yong D, Yum JH. Modified Hodge and EDTA-disk synergy tests to screen metallo-beta-lactamase-producing strains of Pseudomonas and Acinetobactet species. Clin Microbiol Infect 2001; 7: 88-91.
10. 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.
11. Ellington MJ, Kistler J, Livermore DM, Woodford N. Multiplex PCR for rapid detection of genes encoding acquired metallo-beta-lactamases. J Antimicrob Chemother 2007; 59: 321-322.
12. Poirel L, Nordmann P. Carbapenem resistance in Acinetobacter baumannii: mechanisms and epidemiology. Clin Microbiol Infect 2006; 12: 826-836.
13. Poirel L, Nordmann P. Résistance aux β-lactamines chez Acinetobacter baumannii: évolution et émergence de nouveaux mécanismes. Antibiotiques 2006; 8: 100-107.
14. Uwingabiye J, Frikh M, Lemnouer A, Bssaibis F, Belefquih B, Maleb A, et al. Acinetobacter infections prevalence and frequency of the antibiotics resistance: comparative study of intensive care units versus other hospital units. Pan Afr Med J 2016; 23: 191.
15. Manikal VM, Landman D, Saurina G, Oydna E, Lal H, Quale J. Endemic carbapenem-resistant Acinetobacter species in Brooklyn, New York: citywide prevalence, interinstitutional spread, and relation to antibiotic usage. Clin Infect Dis 2000; 31: 101-106.
16. Lin M-F, Lan C-Y. Antimicrobial resistance in Acinetobacter baumannii: From bench to bedside. World J Clin Cases 2014; 2: 787-814.
17. Walther-Rasmussen J, Høiby N. Class A carbapenemases. J Antimicrob Chemother 2007; 60: 470-482.
18. Munoz-Price LS, Weinstein RA. Acinetobacter infection. N Engl J Med 2008; 358: 1271-1281.
19. Decré D. Acinetobacter baumannii et résistance aux antibiotiques: un modèle d’adaptation. Acinetobacter baumannii and multiresistance: a successful adaptative model. Rev Francoph Lab 2012; 2012: 43-52.
20. Domingues S, Da Silva GJ, Nielsen KM. Integrons: vehicles and pathways for horizontal dissemination in bacteria. Mob Genet Elements 2012; 2: 211-223.
21. Uwingabiye J, Lemnouer A, Roca I, Alouane T, Frikh M, Belefquih B, et al. Clonal diversity and detection of carbapenem resistance encoding genes among multidrug-resistant Acinetobacter baumannii isolates recovered from patients and environment in two intensive care units in a Moroccan hospital. Antimicrob Resist Infect Control 2017; 6: 99.
22. Olu-Taiwo MA, Opintan JA, Codjoe FS, Obeng Forson A. Metallo-beta-lactamase-producing Acinetobacter spp. from clinical isolates at a tertiary care Hospital in Ghana. Biomed Res Int 2020; 2020: 3852419.
23. Kabbaj H, Seffar M, Belefquih B, Akka D, Handor N, Amor M, et al. Prevalence of Metallo-β-Lactamases producing Acinetobacter baumannii in a Moroccan Hospital. ISRN Infect Dis 2013; 2013: 154921.
24. Sefraoui I, Berrazeg M, Drissi M, Rolain J-M. Molecular epidemiology of carbapenem-resistant Pseudomonas aeruginosa clinical strains isolated from western Algeria between 2009 and 2012. Microb Drug Resist 2014; 20: 156-161.
25. Mansour W, Bouallegue O, Dahmen S, Boujaafar N. Characterization of the resistance mechanism to beta-lactams in Acinetobacter baumannii strains isolated in the university hospital Sahloul in Tunisia (2005). Pathol Biol (Paris) 2008; 56: 116-120.
26. Davoodi S, Boroumand MA, Sepehriseresht S, Pourgholi L. Detection of VIM- and IMP-type metallo-beta-lactamase genes in Acinetobacter baumannii isolates from patients in two hospitals in Tehran. Iran J Biotechnol 2015; 13:63-67.
27. Riccio ML, Franceschini N, Boschi L, Caravelli B, Cornaglia G, Fontana R, et al. Characterization of the metallo-beta-lactamase determinant of Acinetobacter baumannii AC-54/97 reveals the existence of bla (IMP) Allelic variants carried by gene Cassettes of different phylogeny. Antimicrob Agents Chemother 2000; 44: 1229-1235.
28. Figueiredo S, Poirel L, Papa A, Koulourida V, Nordmann P. First identification of VIM-4 metallo-beta-lactamase in Acinetobacter spp. Clin Microbiol Infect 2008; 14: 289-290.
29. Elabd FM, Al-Ayed MSZ, Asaad AM, Alsareii SA, Qureshi MA, Musa HA-A. Molecular characterization of oxacillinases among carbapenem-resistant Acinetobacter baumannii nosocomial isolates in a Saudi hospital. J Infect Public Health 2015; 8: 242-247.
30. Di Popolo A, Giannouli M, Triassi M, Brisse S, Zarrilli R. Molecular epidemiological investigation of multidrug-resistant Acinetobacter baumannii strains in four Mediterranean countries with a multilocus sequence typing scheme. Clin Microbiol Infect 2011; 17: 197-201.
31. Ikonomidis A, Ntokou E, Maniatis AN, Tsakris A, Pournaras S. Hidden VIM-1 metallo-beta-lactamase phenotypes among Acinetobacter baumannii clinical isolates. J Clin Microbiol 2008; 46: 346-349.
32. Tsakris A, Ikonomidis A, Pournaras S, Tzouvelekis LS, Sofianou D, Legakis NJ, et al. VIM-1 Metallo-β-lactamase in Acinetobacter baumannii. Emerg Infect Dis 2006; 12: 981-983.
33. Nasser M, Ogaili M, Palwe S, Kharat AS. Molecular detection of extended spectrum β-lactamases, metallo β-lactamases, and Amp-Cβ-lactamase genes expressed by multiple drug resistant Pseudomonas aeruginosa isolates collected from patients with burn/wound infections. Burns Open 2020; 4: 160-166.
34. Alkasaby NM, El Sayed Zaki M. Molecular study of Acinetobacter baumannii isolates for metallo-β-lactamases and extended-spectrum-β-lactamases genes in intensive care unit, Mansoura University Hospital, Egypt. Int J Microbiol 2017; 2017: 3925868.
35. Bonnin RA, Nordmann P, Potron A, Lecuyer H, Zahar J-R, Poirel L. Carbapenem-hydrolyzing GES-type extended-spectrum beta-lactamase in Acinetobacter baumannii. Antimicrob Agents Chemother 2011; 55: 349-354.
36. Boulanger A, Naas T, Fortineau N, Figueiredo S, Nordmann P. NDM-1-producing Acinetobacter baumannii from Algeria. Antimicrob Agents Chemother 2012; 56: 2214-2215.
37. Mesli E, Berrazeg M, Drissi M, Bekkhoucha SN, Rolain J-M. Prevalence of carbapenemase-encoding genes including New Delhi metallo-β-lactamase in Acinetobacter species, Algeria. Int J Infect Dis 2013; 17(9): e739-743.
38. Hammerum AM, Larsen AR, Hansen F, Justesen US, Friis-Møller A, Lemming LE, et al. Patients transferred from Libya to Denmark carried OXA-48-producing Klebsiella pneumoniae, NDM-1-producing Acinetobacter baumannii and meticillin-resistant Staphylococcus aureus. Int J Antimicrob Agents 2012; 40: 191-192.
39. Barguigua A, Zerouali K, Katfy K, El Otmani F, Timinouni M, Elmdaghri N. Occurrence of OXA-48 and NDM-1 carbapenemase-producing Klebsiella pneumoniae in a Moroccan university hospital in Casablanca, Morocco. Infect Genet Evol 2015; 31: 142-148.
40. Gales AC, Menezes LC, Silbert S, Sader HS. Dissemination in distinct Brazilian regions of an epidemic carbapenem-resistant Pseudomonas aeruginosa producing SPM metallo-beta-lactamase. J Antimicrob Chemother 2003; 52: 699-702.
2. Bergogne-Berezin E, Towner KJ. Acinetobacter spp. as nosocomial pathogens: microbiological, clinical, and epidemiological features. Clin Microbiol Rev 1996; 9: 148-165.
3. Chang WN, Lu CH, Huang CR, Chuang YC. Community-acquired Acinetobacter meningitis in adults. Infection 2000; 28: 395-397.
4. Falagas ME, Karveli EA, Kelesidis I, Kelesidis T. Community-acquired Acinetobacter infections. Eur J Clin Microbiol Infect Dis 2007; 26: 857-868.
5. Heritier C, Poirel L, Nordmann P. Cephalosporinase over-expression resulting from insertion of ISAba1 in Acinetobacter baumannii. Clin Microbiol Infect 2006; 12: 123-130.
6. El Hafa H, Nayme K, El Hamzaoui N, Maroui I, Sbiti M, Zerouali K, et al. Dissemination of carbapenem-resistant Acinetobacter baumannii strains carrying the blaGES, blaNDM and blaOXA23 in Morocco. Germs 2019; 9: 133-141.
7. Grall N, Andremont A, Armand-Lefèvre L. Résistance aux carbapénèmes: vers une nouvelle impasse? Carbapenem resistance: Towards a new dead end? J Anti-Infect 2011; 13: 87-102.
8. Pollini S, Maradei S, Pecile P, Olivo G, Luzzaro F, Docquier J-D, et al. FIM-1, a New Acquired Metallo-β-Lactamase from a Pseudomonas aeruginosa clinical isolate from Italy. Antimicrob Agents Chemother 2013; 57: 410-416.
9. Lee K, Chong Y, Shin HB, Kim YA, Yong D, Yum JH. Modified Hodge and EDTA-disk synergy tests to screen metallo-beta-lactamase-producing strains of Pseudomonas and Acinetobactet species. Clin Microbiol Infect 2001; 7: 88-91.
10. 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.
11. Ellington MJ, Kistler J, Livermore DM, Woodford N. Multiplex PCR for rapid detection of genes encoding acquired metallo-beta-lactamases. J Antimicrob Chemother 2007; 59: 321-322.
12. Poirel L, Nordmann P. Carbapenem resistance in Acinetobacter baumannii: mechanisms and epidemiology. Clin Microbiol Infect 2006; 12: 826-836.
13. Poirel L, Nordmann P. Résistance aux β-lactamines chez Acinetobacter baumannii: évolution et émergence de nouveaux mécanismes. Antibiotiques 2006; 8: 100-107.
14. Uwingabiye J, Frikh M, Lemnouer A, Bssaibis F, Belefquih B, Maleb A, et al. Acinetobacter infections prevalence and frequency of the antibiotics resistance: comparative study of intensive care units versus other hospital units. Pan Afr Med J 2016; 23: 191.
15. Manikal VM, Landman D, Saurina G, Oydna E, Lal H, Quale J. Endemic carbapenem-resistant Acinetobacter species in Brooklyn, New York: citywide prevalence, interinstitutional spread, and relation to antibiotic usage. Clin Infect Dis 2000; 31: 101-106.
16. Lin M-F, Lan C-Y. Antimicrobial resistance in Acinetobacter baumannii: From bench to bedside. World J Clin Cases 2014; 2: 787-814.
17. Walther-Rasmussen J, Høiby N. Class A carbapenemases. J Antimicrob Chemother 2007; 60: 470-482.
18. Munoz-Price LS, Weinstein RA. Acinetobacter infection. N Engl J Med 2008; 358: 1271-1281.
19. Decré D. Acinetobacter baumannii et résistance aux antibiotiques: un modèle d’adaptation. Acinetobacter baumannii and multiresistance: a successful adaptative model. Rev Francoph Lab 2012; 2012: 43-52.
20. Domingues S, Da Silva GJ, Nielsen KM. Integrons: vehicles and pathways for horizontal dissemination in bacteria. Mob Genet Elements 2012; 2: 211-223.
21. Uwingabiye J, Lemnouer A, Roca I, Alouane T, Frikh M, Belefquih B, et al. Clonal diversity and detection of carbapenem resistance encoding genes among multidrug-resistant Acinetobacter baumannii isolates recovered from patients and environment in two intensive care units in a Moroccan hospital. Antimicrob Resist Infect Control 2017; 6: 99.
22. Olu-Taiwo MA, Opintan JA, Codjoe FS, Obeng Forson A. Metallo-beta-lactamase-producing Acinetobacter spp. from clinical isolates at a tertiary care Hospital in Ghana. Biomed Res Int 2020; 2020: 3852419.
23. Kabbaj H, Seffar M, Belefquih B, Akka D, Handor N, Amor M, et al. Prevalence of Metallo-β-Lactamases producing Acinetobacter baumannii in a Moroccan Hospital. ISRN Infect Dis 2013; 2013: 154921.
24. Sefraoui I, Berrazeg M, Drissi M, Rolain J-M. Molecular epidemiology of carbapenem-resistant Pseudomonas aeruginosa clinical strains isolated from western Algeria between 2009 and 2012. Microb Drug Resist 2014; 20: 156-161.
25. Mansour W, Bouallegue O, Dahmen S, Boujaafar N. Characterization of the resistance mechanism to beta-lactams in Acinetobacter baumannii strains isolated in the university hospital Sahloul in Tunisia (2005). Pathol Biol (Paris) 2008; 56: 116-120.
26. Davoodi S, Boroumand MA, Sepehriseresht S, Pourgholi L. Detection of VIM- and IMP-type metallo-beta-lactamase genes in Acinetobacter baumannii isolates from patients in two hospitals in Tehran. Iran J Biotechnol 2015; 13:63-67.
27. Riccio ML, Franceschini N, Boschi L, Caravelli B, Cornaglia G, Fontana R, et al. Characterization of the metallo-beta-lactamase determinant of Acinetobacter baumannii AC-54/97 reveals the existence of bla (IMP) Allelic variants carried by gene Cassettes of different phylogeny. Antimicrob Agents Chemother 2000; 44: 1229-1235.
28. Figueiredo S, Poirel L, Papa A, Koulourida V, Nordmann P. First identification of VIM-4 metallo-beta-lactamase in Acinetobacter spp. Clin Microbiol Infect 2008; 14: 289-290.
29. Elabd FM, Al-Ayed MSZ, Asaad AM, Alsareii SA, Qureshi MA, Musa HA-A. Molecular characterization of oxacillinases among carbapenem-resistant Acinetobacter baumannii nosocomial isolates in a Saudi hospital. J Infect Public Health 2015; 8: 242-247.
30. Di Popolo A, Giannouli M, Triassi M, Brisse S, Zarrilli R. Molecular epidemiological investigation of multidrug-resistant Acinetobacter baumannii strains in four Mediterranean countries with a multilocus sequence typing scheme. Clin Microbiol Infect 2011; 17: 197-201.
31. Ikonomidis A, Ntokou E, Maniatis AN, Tsakris A, Pournaras S. Hidden VIM-1 metallo-beta-lactamase phenotypes among Acinetobacter baumannii clinical isolates. J Clin Microbiol 2008; 46: 346-349.
32. Tsakris A, Ikonomidis A, Pournaras S, Tzouvelekis LS, Sofianou D, Legakis NJ, et al. VIM-1 Metallo-β-lactamase in Acinetobacter baumannii. Emerg Infect Dis 2006; 12: 981-983.
33. Nasser M, Ogaili M, Palwe S, Kharat AS. Molecular detection of extended spectrum β-lactamases, metallo β-lactamases, and Amp-Cβ-lactamase genes expressed by multiple drug resistant Pseudomonas aeruginosa isolates collected from patients with burn/wound infections. Burns Open 2020; 4: 160-166.
34. Alkasaby NM, El Sayed Zaki M. Molecular study of Acinetobacter baumannii isolates for metallo-β-lactamases and extended-spectrum-β-lactamases genes in intensive care unit, Mansoura University Hospital, Egypt. Int J Microbiol 2017; 2017: 3925868.
35. Bonnin RA, Nordmann P, Potron A, Lecuyer H, Zahar J-R, Poirel L. Carbapenem-hydrolyzing GES-type extended-spectrum beta-lactamase in Acinetobacter baumannii. Antimicrob Agents Chemother 2011; 55: 349-354.
36. Boulanger A, Naas T, Fortineau N, Figueiredo S, Nordmann P. NDM-1-producing Acinetobacter baumannii from Algeria. Antimicrob Agents Chemother 2012; 56: 2214-2215.
37. Mesli E, Berrazeg M, Drissi M, Bekkhoucha SN, Rolain J-M. Prevalence of carbapenemase-encoding genes including New Delhi metallo-β-lactamase in Acinetobacter species, Algeria. Int J Infect Dis 2013; 17(9): e739-743.
38. Hammerum AM, Larsen AR, Hansen F, Justesen US, Friis-Møller A, Lemming LE, et al. Patients transferred from Libya to Denmark carried OXA-48-producing Klebsiella pneumoniae, NDM-1-producing Acinetobacter baumannii and meticillin-resistant Staphylococcus aureus. Int J Antimicrob Agents 2012; 40: 191-192.
39. Barguigua A, Zerouali K, Katfy K, El Otmani F, Timinouni M, Elmdaghri N. Occurrence of OXA-48 and NDM-1 carbapenemase-producing Klebsiella pneumoniae in a Moroccan university hospital in Casablanca, Morocco. Infect Genet Evol 2015; 31: 142-148.
40. Gales AC, Menezes LC, Silbert S, Sader HS. Dissemination in distinct Brazilian regions of an epidemic carbapenem-resistant Pseudomonas aeruginosa producing SPM metallo-beta-lactamase. J Antimicrob Chemother 2003; 52: 699-702.
| Files | ||
| Issue | Vol 14 No 4 (2022) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v14i4.10229 | |
| Keywords | ||
| Acinetobacter baumannii; Carbapenems; Resistance; Metallo-beta-lactamase | ||
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How to Cite
1.
Massik A, Hibaoui L, Moussa B, Yahyaoui G, Oumokhtar B, Mahmoud M. First report of SPM metallo-β-lactamases producing Acinetobacter baumannii isolates in Morocco. Iran J Microbiol. 2022;14(4):438-444.
