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Carbapenem-Resistant Pseudomonas aeruginosa in Chronic Lung Infection: Current Resistance Profile and Hypermutability in Patients with Cystic Fibrosis

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Abstract

Pseudomonas aeruginosa is associated with chronic and progressive lung disease and is closely related to increased morbidity and mortality in cystic fibrosis (CF) patients. Hypermutable (HPM) P. aeruginosa isolates have been described in these patients and are usually associated with antibiotic resistance. This study aimed to investigate the occurrence of carbapenem resistance and hypermutable phenotype in 179 P. aeruginosa isolates from 8 chronically CF patients assisted at two reference centers in Rio de Janeiro, Brazil. Using disk diffusion test, non-susceptible (NS) rates higher than 40% were observed for imipenem, amikacin, and gentamicin. A total of 79 isolates (44.1%), 71 (39.6%), and 8 (4.4%) were classified as carbapenem-resistant (CR resistance to at least one carbapenem), multidrug-resistant (MDR), and extensively drug-resistant (XDR), respectively. Minimal inhibitory concentration was determined for 79 CR P. aeruginosa and showed the following variations: 4 and 128 μg/mL to imipenem, 4 and 64 µg/mL to meropenem, and 4 and ≥ 32 µg/mL to doripenem. We have found only four (2.23%) HPM isolates from 4 patients. Analyzing the genetic relationship among the HPM isolates, 3 pulsed-field gel electrophoresis/pulsotypes (D, M, and J) were observed. Only M pulsotype was recovered from two patients in different years. Polymerase chain reaction screening for blaGES, blaIMP, blaKPC, blaNDM, blaOXA-48, blaSPM, and blaVIM genes was performed for all CR isolates and none of them were positive. Our results demonstrate a high occurrence of CR and MDR P. aeruginosa of CF patients follow-up in both centers studied, while the presence of HPM is still unusual.

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References

  1. Bhagirath AY, Li Y, Somayajula D, Dadashi M, Badr S, Duan K (2016) Cystic fibrosis lung environment and Pseudomonas aeruginosa infection. BMC Pulm Med 16:1–22. https://doi.org/10.1186/s12890-016-0339-5

    Article  CAS  Google Scholar 

  2. Finnan S, Morrissey JP, Gara FO, Boyd EF (2004) Genome diversity of Pseudomonas aeruginosa isolates from cystic fibrosis patients and the hospital environment. J Clin Microbiol 42:5783–5792. https://doi.org/10.1128/JCM.42.12.5783-5792.2004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Mustafa M, Chalhoub H, Denis O, Deplano A, Vergison A, Rodriguez-villalobos H, Tunney MM, Elborn JS, Kahl BC, Traore H, Vanderbist F, Tulkens PM (2016) Antimicrobial susceptibility of Pseudomonas aeruginosa isolated from cystic fibrosis patients in Northern Europe. Antimicrob Agents Chemother 60:6735–6741. https://doi.org/10.1128/AAC.01046-16

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Maciá MD, Blanquer D, Togores B, Sauleda J, Perez JL, Oliver A (2005) Hypermutation is a key factor in development of multiple-antimicrobial resistance in Pseudomonas aeruginosa strains causing chronic lung infections. Antimicrob Agents Chemother 49:3382–3386. https://doi.org/10.1128/AAC.49.8.3382-3386.2005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Feliziani S, Luján AM, Moyano AJ, Sola C, Bocco JL, Montanaro P, Canigia LF, Argaraña CE, Smania AM (2010) Mucoidy, quorum sensing, mismatch repair and antibiotic resistance in Pseudomonas aeruginosa from cystic fibrosis chronic airways infections. PLoS ONE 5:1–12. https://doi.org/10.1371/journal.pone.0012669

    Article  CAS  Google Scholar 

  6. Lutz L, Leão RS, Ferreira AG, Pereira DC, Raupp C, Pitt T, Marques EA, Barth AL (2013) Hypermutable Pseudomonas aeruginosa in cystic fibrosis patients from two Brazilian cities. J Clin Microbiol 51:927–930. https://doi.org/10.1128/JCM.02638-12

    Article  PubMed  PubMed Central  Google Scholar 

  7. Logan LK, Gandra S, Mandal S, Klein EY, Levinson J, Weinstein RA, Laxminarayan R (2017) Multidrug- and carbapenem-resistant Pseudomonas aeruginosa in children, United States, 1999–2012. J Pediatr Infect Dis Soc 6:352–359. https://doi.org/10.1093/jpids/piw064

    Article  Google Scholar 

  8. Rutter WC, Burgess DR, Burgess DS (2016) Increasing incidence of multidrug resistance among cystic fibrosis respiratory bacterial isolates. Microb Drug Resist. https://doi.org/10.1089/mdr.2016.0048

    Article  PubMed  Google Scholar 

  9. Pedersen SS, Koch C, Hoibyt N, Roscndalj K (1986) An epidemic spread of multiresistant Pseudomonas aeruginosa in a cystic fibrosis centre. J Antimicrob Chemother 17:505–516. https://doi.org/10.1093/jac/17.4.505

    Article  CAS  PubMed  Google Scholar 

  10. Romling U, Wingender J, Muller H, Tummler B (1994) A major Pseudomonas aeruginosa clone common to patients and aquatic habitats. Appl Environ Microbiol 60:1734–1738

    Article  CAS  Google Scholar 

  11. Cheng K, Smyth RL, Govan JR, Doherty C, Winstanley C, Denning N, Heaf DP, van Saene H, Hart CA (1996) Spread of beta-lactam-resistant Pseudomonas aeruginosa in a cystic fibrosis clinic. Lancet 348:639–642. https://doi.org/10.1016/S0140-6736(96)05169-0

    Article  CAS  PubMed  Google Scholar 

  12. Jones AM, Govan JR, Doherty CJ, Dodd ME, Isalska BJ, Nigel Stanbridge T, Kevin Webb A (2001) Spread of a multiresistant strain of Pseudomonas aeruginosa in an adult cystic fibrosis clinic. Lancet 358:557–558. https://doi.org/10.1016/s0140-6736(01)05714-2

    Article  CAS  PubMed  Google Scholar 

  13. Armstrong D, Bell S, Robinson M, Bye P, Rose B, Harbour C, Lee C, Service H, Nissen M, Syrmis M, Wainwright C (2003) Evidence for spread of a clonal strain of Pseudomonas aeruginosa among cystic fibrosis clinics. J Clin Microbiol 41:2266–2267. https://doi.org/10.1128/jcm.41.5.2266-2267.2003

    Article  PubMed  Google Scholar 

  14. Scott FW, Pitt TL (2004) Identification and characterization of transmissible Pseudomonas aeruginosa strains in cystic fibrosis patients in England and Wales. J Med Microbiol 53:609–615. https://doi.org/10.1099/jmm.0.45620-0

    Article  CAS  PubMed  Google Scholar 

  15. López-Causape C, Rojo-Molinero E, Mulet X, Cabot G, Moya B, Figuerola J, Togores B, Perez JL, Oliver A (2013) Clonal dissemination, emergence of mutator lineages and antibiotic resistance evolution in Pseudomonas aeruginosa cystic fibrosis chronic lung infection. PLoS ONE 8:1–8. https://doi.org/10.1371/journal.pone.0071001

    Article  CAS  Google Scholar 

  16. Somayaji R, Lam JC, Surette MG, Waddell B, Rabin HR, Sibley CD, Purighalla S, Parkins MD (2017) Long-term clinical outcomes of ‘Prairie Epidemic Strain’ Pseudomonas aeruginosa infection in adults with cystic fibrosis. Thorax 72:333–339. https://doi.org/10.1136/thoraxjnl-2015-208083

    Article  PubMed  Google Scholar 

  17. Gniadek TJ, Carroll KC, Simner PJ (2016) Carbapenem-resistant non-glucose-fermenting Gram-negative Bacilli: the missing piece to the puzzle. J Clin Microbiol 54:1700–1710. https://doi.org/10.1128/JCM.03264-15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Poirel L, Pitout JD, Nordmann P (2007) Carbapenemases: molecular diversity and clinical consequences. Future Microbiol 2:501–512. https://doi.org/10.2217/17460913.2.5.501

    Article  CAS  PubMed  Google Scholar 

  19. Dortet L, Poirel L, Nordmann P (2012) Rapid identification of carbapenemase types in Enterobacteriaceae and Pseudomonas spp. by using a biochemical test. Antimicrob Agents Chemother 56:6437–6440. https://doi.org/10.1128/AAC.01395-12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Li Y, Zhang X, Wang C, Hu Y, Niu X, Pei D, He Z, Bi Y (2014) Characterization by phenotypic and genotypic methods of metallo-B-lactamase-producing Pseudomonas aeruginosa isolated from patients with cystic fibrosis. Mol Med Rep 11:494–498. https://doi.org/10.3892/mmr.2014.2685

    Article  CAS  PubMed  Google Scholar 

  21. Gales AC, Menezes LC, Silbert S, Sader HS (2003) Dissemination in distinct Brazilian regions of an epidemic carbapenem-resistant Pseudomonas aeruginosa producing SPM metallo-β-lactamase. J Antimicrob Chemother 52:699–702. https://doi.org/10.1093/jac/dkg416

    Article  CAS  PubMed  Google Scholar 

  22. Zavascki AP, Gaspareto PB, Martins AF, Gonçalves AL, Barth AL (2005) Outbreak of carbapenem-resistant Pseudomonas aeruginosa producing SPM-1 metallo-B-lactamase in a teaching hospital in southern Brazil. J Antimicrob Chemother 56:1148–1151. https://doi.org/10.1093/jac/dki390

    Article  CAS  PubMed  Google Scholar 

  23. Franco MR, Caiaffa-filho HH, Burattini MN, Rossi F (2010) Metallo-beta-lactamases among imipenem-resistant Pseudomonas aeruginosa in a Brazilian university hospital. Clinics 65:825–829. https://doi.org/10.1590/s1807-59322010000900002

    Article  PubMed  PubMed Central  Google Scholar 

  24. Jácome PR, Alves LR, Cabral AB, Lopes AC, Maciel MA (2012) First report of KPC-producing Pseudomonas aeruginosa in Brazil. Antimicrob Agents Chemother 56:4990. https://doi.org/10.1128/AAC.00699-12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. de Oliveira Santos IC, Albano RM, Asensi MD, D’Alincourt Carvalho-Assef AP (2018) Draft genome sequence of KPC-2-producing Pseudomonas aeruginosa recovered from a bloodstream infection sample in Brazil. J Glob Antimicrob Resist 15:99–100. https://doi.org/10.1016/j.jgar.2018.08.021

    Article  PubMed  Google Scholar 

  26. Galetti R, Andrade LN, Varani AM, Darini ALC (2019) SPM-1-producing Pseudomonas aeruginosa ST277 carries a chromosomal pack of acquired resistance genes: an example of high-risk clone associated with intrinsic resistome. J Glob Antimicrob Resist 16:183–186. https://doi.org/10.1016/j.jgar.2018.12.009

    Article  PubMed  Google Scholar 

  27. Ferreira AG, Leão RS, Carvalho-Assef DA, da Silva EA, Firmida MC, Folescu TW, Paixão VA, Santana MA, de Abreu e Silva FA, Barth AL, Marques EA (2015) Low-level resistance and clonal diversity of Pseudomonas aeruginosa among chronically colonized cystic fibrosis patients. APMIS 123:1061–1068. https://doi.org/10.1111/apm.12463

    Article  CAS  Google Scholar 

  28. Lee B, Haagensen JA, Ciofu O, Andersen JB, Høiby N, Molin S (2005) Heterogeneity of biofilms formed by nonmucoid Pseudomonas aeruginosa isolates from patients with cystic fibrosis. J Clin Microbiol 43:5247–5255. https://doi.org/10.1128/JCM.43.10.5247-5255.2005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Clinical and Laboratory Standard Institute (CLSI) (2018) M100 standards, performance testing, antimicrobial susceptibility, 28th edn. Clinical and Laboratory Standard Institute (CLSI), Wayne, PA

    Google Scholar 

  30. Clinical and Laboratory Standard Institute (CLSI) (2018) M02 performance standards for antimicrobial disk susceptibility tests, 13th edn. Clinical and Laboratory Standard Institute (CLSI), Wayne, PA

    Google Scholar 

  31. Magiorakos AP, Srinivasan A, Carey RB, Carmeli Y, Falagas ME, Giske CG, Harbarth S, Hindler JF, Kahlmeter G, Olsson-Liljequist B, Paterson DL, Rice LB, Stelling J, Struelens MJ, Vatopoulos A, Weber JT, Monnet DL (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

    Article  CAS  PubMed  Google Scholar 

  32. Clinical and Laboratory Standard Institute (CLSI) (2018) M07 methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically, 28th edn. Clinical and Laboratory Standard Institute (CLSI), Wayne, PA

    Google Scholar 

  33. Oliver A, Cantón R, Campo P, Baquero F, Blásquez J (2016) High frequency of hypermutable Pseudomonas aeruginosa in cystic fibrosis lung infection. Am Assoc Adv Sci 288:1251–1253. https://doi.org/10.1126/science.288.5469.1251

    Article  Google Scholar 

  34. Tsakris A, Pournaras S, Woodford N, Palepou MF, Babini GS, Douboyas J, Livermore DM (2000) Outbreak of infections caused by Pseudomonas aeruginosa producing VIM-1 carbapenemase in Greece. J Clin Microbiol 38:1290–1292

    Article  CAS  Google Scholar 

  35. Yigit H, Queenan AM, Anderson GJ, Domenech-Sanchez A, Biddle JW, Steward CD, Alberti S, Bush K, Tenover FC (2001) Novel carbapenem-hydrolysing B-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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Shibata N, Doi Y, Yamane K, Yagi T, Kurokawa H, Shibayama K, Kato H, Kai K, Arakawa Y (2003) PCR typing of genetic determinants for metallo-B-lactamases and integrases carried by Gram-negative bacteria isolated in Japan, with focus on the class 3 integron. J Clin Microbiol 41:5407–5413. https://doi.org/10.1128/jcm.41.12.5407-5413.2003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Lee K, Park AJ, Kim MY, Lee HJ, Cho J, Kang JO, Yong D, Chong Y (2009) Metallo-B-lactamase producing Pseudomonas spp. in Korea: high prevalence of isolates with VIM-2 type and emergence of isolates with IMP-1 type. Yonsei Med J 50:335–339. https://doi.org/10.3349/ymj.2009.50.3.335

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Monteiro J, Widen RH, Pignatari AC, Kubasek C, Silbert S (2012) Rapid detection of carbapenemase genes by multiplex real-time PCR. J Antimicrob Chemother 67:906–909. https://doi.org/10.1093/jac/dkr563

    Article  CAS  PubMed  Google Scholar 

  39. Sader HS, Pignatari AC, Leme IL, Burattini MN, Tancresi R, Hollis RJ, Jones RN (1993) Epidemiologic typing of multiply drug-resistant Pseudomonas aeruginosa isolated from an outbreak in an intensive care unit. Diagn Microbiol Infect Dis 17:13–18. https://doi.org/10.1016/0732-8893(93)90063-d

    Article  CAS  PubMed  Google Scholar 

  40. Loureiro MM, De Moraes BA, Mendonça VL, Quadra MR, Pinheiro GS (2002) Pseudomonas aeruginosa: study of antibiotic resistance and molecular typing in hospital infection cases in a neonatal intensive care unit from Rio de Janeiro City, Brazil. Memórias do Instituto Oswaldo Cruz 97:387–394. https://doi.org/10.1590/s0074-02762002000300020

    Article  CAS  PubMed  Google Scholar 

  41. Parkins MD, Glezerson BA, Sibley CD, Sibley KA, Duong J, Purighalla S, Mody CH, Workentine ML, Storey DG, Surette MG, Rabin HR (2014) Twenty-five-year outbreak of Pseudomonas aeruginosa infecting individuals with cystic fibrosis: identification of the Prairie epidemic strain. J Clin Microbiol 52:1127–1135. https://doi.org/10.1128/JCM.03218-13

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Waters VJ, Kidd TJ, Canton R, Ekkelenkamp MB, Johansen HK, LiPuma JJ, Bell SC, Elborn JS, Flume PA, VanDevanter DR, Gilligan P (2013) Reconciling antimicrobial susceptibility testing and clinical response in antimicrobial treatment of chronic cystic fibrosis lung infections. Infect Dis Soc Am. https://doi.org/10.1093/cid/ciz364

    Article  Google Scholar 

  43. Salsgiver EL, Fink AK, Knapp EA, Lipuma JJ, Olivier KN, Marshall BC, Saiman L (2016) Changing epidemiology of the respiratory bacteriology of patients with cystic fibrosis. Chest 149:390–400. https://doi.org/10.1378/chest.15-0676

    Article  PubMed  PubMed Central  Google Scholar 

  44. Damas C, Amorim A, Gomes I (2008) Fibrose quística: revisão. Rev Port Pneumol 14:89–112

    Article  CAS  Google Scholar 

  45. Gaspar MC, Couet W, Olivier JC, Pais AA, Sousa JJ (2013) Pseudomonas aeruginosa infection in cystic fibrosis lung disease and new perspectives of treatment: a review. Eur J Clin Microbiol Infect Dis 32:1231–1252. https://doi.org/10.1007/s10096-013-1876-y

    Article  CAS  PubMed  Google Scholar 

  46. Pournajaf A, Razavi S, Irajian G, Ardebili A, Erfani Y, Solgi S, Yaghoubi S, Rasaeian A, Yahyapour Y, Kafshgari R, Shoja S, Rajabnia R (2018) Integron types, antimicrobial resistance genes, virulence gene profile, alginate production and biofilm formation in Iranian cystic fibrosis Pseudomonas aeruginosa isolates. Le Infezione in Medicina 3:226–236

    Google Scholar 

  47. Paixão VA, Barros TF, Mota CMC, Moreira TF, Santana MA, Reis JN (2010) Prevalence and antimicrobial susceptibility of respiratory pathogens in patients with cystic fibrosis. Braz J Infect Dis 14:406–409

    Article  Google Scholar 

  48. Perez R, Limberger MF, Costi R, Dias G, Barth AL (2014) Evaluation of tests to predict metallo-B-lactamase in cystic fibrosis (CF) and non-(CF) Pseudomonas. Braz J Microbiol 45:835–839. https://doi.org/10.1590/s1517-83822014000300011

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Leão RS, Pereira RH, Folescu TW, Albano RM, Santos EA, Junior LG, Marques EA (2011) KPC-2 carbapenemase-producing Klebsiella pneumoniae isolates from patients with cystic fibrosis. J Cyst Fibros 10:140–142. https://doi.org/10.1016/j.jcf.2010.12.003

    Article  CAS  PubMed  Google Scholar 

  50. Alves DP, Carvalho-Assef APD’A, Conceição-Neto OC, Aires CAM, Albano RM, Folescu TW, Ornelas SCS, Leão RS, Marques EA (2018) Enterobacter cloacae harbouring bla KPC-2 and qnrB-1 isolated from a cystic fibrosis patient: a case report. New Microbes New Infect 25:49–51. https://doi.org/10.1016/j.nmni.2018.06.010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Ciofu O, Riis B, Pressler T, Enghusen H, Høiby N, Poulsen HE (2005) Occurrence of hypermutable Pseudomonas aeruginosa in cystic fibrosis patients is associated with the oxidative stress caused by chronic lung inflammation. Antimicrob Agents Chemother 49:2276–2282. https://doi.org/10.1128/AAC.49.6.2276-2282.2005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Oliver A, Baquero F, Blázquez J (2002) The mismatch repair system (mutS, mutL and uvrD genes) in Pseudomonas aeruginosa: molecular characterization of naturally occurring mutants. Mol Microbiol 43:1641–1650. https://doi.org/10.1046/j.1365-2958.2002.02855.x

    Article  CAS  PubMed  Google Scholar 

  53. Maciá MD, Borrell N, Pérez JL, Oliver A (2004) Detection and susceptibility testing of hypermutable Pseudomonas aeruginosa strains with the Etest and disk diffusion detection and susceptibility testing of hypermutable Pseudomonas aeruginosa strains with the Etest and disk diffusion. Antimicrob Agents Chemother 48:2665–2672. https://doi.org/10.1128/AAC.48.7.2665-2672.2004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Mena A, Smith E, Burns JL, Speert DP, Moskowitz SM, Perez JL, Oliver A (2008) Genetic adaptation of Pseudomonas aeruginosa to the airways of cystic fibrosis patients is catalysed by hypermutation. J Bacteriol 190:7910–7917. https://doi.org/10.1128/JB.01147-08

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This work was funded by INPRA—Instituto Nacional de Pesquisa em Resistência Antimicrobiana—Brazil, CNPq 465718/2014-0, FAPERGS 17/2551-0000514-7. This study was also partially supported by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior, Brasil (CAPES), Finance Code 001.

Funding

This work was funded by INPRA—Instituto Nacional de Pesquisa em Resistência Antimicrobiana—Brazil, CNPq 465718/2014–0, FAPERGS 17/2551-0000514-7. This study was also partially supported by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior, Brasil (CAPES), Finance Code 001.

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Authors and Affiliations

  1. Departamento de Microbiologia, Imunologia e Parasitologia, Faculdade de Ciências Médicas, Universidade do Estado do Rio de Janeiro, Rio de Janeiro, Brazil

    Mila M. Almeida, Meyvianne T. Freitas, Elizabeth A. Marques & Robson S. Leão

  2. Instituto Nacional de Saúde da Mulher, Criança e do Adolescente Fernandes Figueira, Centro de Referência para Crianças e Adolescentes com Fibrose Cística - Ministério da Saúde, Fundação Oswaldo Cruz, Rio de Janeiro, Brazil

    Tania W. Folescu

  3. Departamento de Doenças do Tórax, Faculdade de Ciências Médicas, Universidade do Estado do Rio de Janeiro, Rio de Janeiro, Brazil

    Monica C. Firmida

  4. Laboratório de Pesquisa em Infecção Hospitalar, Instituto Oswaldo Cruz, Fundação Oswaldo Cruz, Rio de Janeiro, Brazil

    Ana Paula D’A. Carvalho-Assef

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  1. Mila M. Almeida
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Contributions

All authors contributed to the study conception and design. Study conception and design were performed by EAM and RSL. Most of material preparation, data collection, and phenotypic and molecular analysis were performed by MMA. Material preparation, data collection, and phenotypic analysis were performed by MMA and MTF. Molecular analysis by PFGE was performed by EAM, RSL, MMA, and APD´ACA. Clinical data collection and analysis were performed by TWF and MCF. The first draft of the manuscript was written by MMA, EAM, and RSL and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

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Correspondence to Robson S. Leão.

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All procedures performed in this study were in accordance with the ethical standards of the institutional research committee (CAAE: 79547616.1.0000.5259), and the approval was waived by the local Ethics Committee of Universidade do Estado do Rio de Janeiro, in view of the retrospective nature of the study and all the procedures were performed with samples stored in a bacteriological collection.

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Almeida, M.M., Freitas, M.T., Folescu, T.W. et al. Carbapenem-Resistant Pseudomonas aeruginosa in Chronic Lung Infection: Current Resistance Profile and Hypermutability in Patients with Cystic Fibrosis. Curr Microbiol 78, 696–704 (2021). https://doi.org/10.1007/s00284-020-02337-0

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