Occurrence of Plasmid-Mediated Quinolone Resistance and Carbapenemase-Encoding Genes in Pseudomonas aeruginosa Isolates from Nosocomial Patients in Aguascalientes, Mexico
Abstract
1. Introduction
2. Materials and Methods
2.1. Sampling and Bacterial Isolation
2.2. Ethics Statement
2.3. Data Collection
2.4. Antibiotic Susceptibility Testing
2.5. Screening and Identification of PMQR and Carbapenemase-Encoding Genes
2.6. Statistical Analysis
3. Results
3.1. Identification of the Isolates and Clinical Characteristics
3.2. Antimicrobial Susceptibility
3.3. Occurrence of Carbapenemase Encoding-Genes
3.4. Screening for Plasmid-Mediated Colistin-Resistant mcr-1 Gene
3.5. Presence of PMQR Determinants
3.6. Co-Occurrence of Carbapenemase-Encoding Genes and PMQR Determinants
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Reynolds, D.; Kollef, M. The Epidemiology and Pathogenesis and Treatment of Pseudomonas aeruginosa Infections: An Update. Drugs 2021, 81, 2117–2131. [Google Scholar] [CrossRef]
- Bonomo, R.A.; Szabo, D. Mechanisms of multidrug resistance in Acinetobacter species and Pseudomonas aeruginosa. Clin. Infect. Dis. 2006, 43, S49–S56. [Google Scholar] [CrossRef]
- Ramanathan, S.; Fitzpatrick, M.A.; Suda, K.J.; Burns, S.P.; Jones, M.M.; LaVela, S.L.; Evans, C.T. Multidrug-resistant Gram-negative organisms and association with 1-year mortality, readmission, and length of stay in Veterans with spinal cord injuries and disorders. Spinal Cord 2020, 58, 596–608. [Google Scholar] [CrossRef]
- Antimicrobial Resistance Collaborators. Global burden of bacterial antimicrobial resistance in 2019: A systematic analysis. Lancet 2022, 399, 629–655. [Google Scholar] [CrossRef]
- Avakh, A.; Grant, G.D.; Cheesman, M.J.; Kalkundri, T.; Hall, S. The Art of War with Pseudomonas aeruginosa: Targeting Mex Efflux Pumps Directly to Strategically Enhance Antipseudomonal Drug Efficacy. Antibiotics 2023, 12, 1304. [Google Scholar] [CrossRef]
- Liu, Y.Y.; Wang, Y.; Walsh, T.; Yi, L.-X.; Zhang, R.; Spencer, J.; Doi, Y.; Tian, G.; Dong, B.; Huan, X.; et al. Emergence of plasmid-mediated colistin resistance mechanism MCR-1 in animals and human beings in China: A microbiological and molecular biological study. Lancet Infct. Dis. 2016, 16, 161–168. [Google Scholar] [CrossRef]
- Wieland, K.; Chhatwal, P.; Vonberg, R.P. Nosocomial outbreaks caused by Acinetobacter baumannii and Pseudomonas aeruginosa: Results of a systematic review. Am. J. Infect. Control. 2018, 46, 643–648. [Google Scholar] [CrossRef]
- Huang, W.; Wei, X.; Xu, G.; Zhang, X.; Wang, X. Carbapenem-resistant Pseudomonas aeruginosa infections in critically ill children: Prevalence, risk factors, and impact on outcome in a large tertiary pediatric hospital of China. Front. Public Heal. 2023, 11, 1088262. [Google Scholar] [CrossRef]
- Pai, H.; Kim, J.; Kim, J.; Lee, J.H.; Choe, K.W.; Gotoh, N. Carbapenem resistance mechanisms in Pseudomonas aeruginosa clinical isolates. Antimicrob. Agents Chemother. 2001, 45, 480–484. [Google Scholar] [CrossRef]
- Cornaglia, G.; Giamarellou, H.; Rossolini, G.M. Metallo-β-lactamases: A last frontier for β-lactams? Lancet Infect. Dis. 2011, 11, 381–393. [Google Scholar] [CrossRef]
- Garza-Ramos, U.; Silva-Sánchez, J.; López-Jácome, L.E.; Hernández-Durán, M.; Colín-Castro, C.A.; Sánchez-Pérez, A.; Rodríguez-Santiago, J.; Morfín-Otero, R.; Rodríguez-Noriega, E.; Velázquez-Acosta, M.D.; et al. Carbapenemase-Encoding Genes and Colistin Resistance in Gram-Negative Bacteria During the COVID-19 Pandemic in Mexico: Results from the Invifar Network. Microb. Drug. Resist. 2023, 29, 239–248. [Google Scholar] [CrossRef] [PubMed]
- Garza-Ramos, U.; Morfin-Otero, R.; Sader, H.S.; Jones, R.N.; Hernández, E.; Rodríguez-Noriega, E.; Sánchez, A.; Carrillo, B.; Esparza-Ahumada, S.; Silva-Sánchez, J. Metallo-beta-lactamase gene bla (IMP-15) in a class 1 integron, In95, from Pseudomonas aeruginosa clinical isolates from a hospital in Mexico. Antimicrob. Agents Chemother. 2008, 52, 2943–2946. [Google Scholar] [CrossRef] [PubMed]
- Nieto-Saucedo, J.R.; López-Jacome, L.E.; Franco-Cendejas, R.; Colín-Castro, C.A.; Hernández-Duran, M.; Rivera-Garay, L.R.; Zamarripa-Martinez, K.S.; Mosqueda-Gómez, J.L. Carbapenem-Resistant Gram-Negative Bacilli Characterization in a Tertiary Care Center from El Bajio, Mexico. Antibiotics 2023, 12, 1295. [Google Scholar] [CrossRef] [PubMed]
- Rodríguez-Martínez, J.M.; Machuca, J.; Cano, M.E.; Calvo, J.; Martínez-Martínez, L.; Pascual, A. Plasmid-mediated quinolone resistance: Two decades on. Drug Resist. Updates 2016, 29, 13–29. [Google Scholar] [CrossRef]
- Saki, M.; Farajzadeh Sheikh, A.; Seyed-Mohammadi, S.; Asareh Zadegan Dezfuli, A.; Shanin, M.; Tabasi, M.; Veisi, H.; Keshavarzi, R.; Khani, P. Occurrence of plasmid-mediated quinolone resistance genes in Pseudomonas aeruginosa strains isolated from clinical specimens in southwest Iran: A multicentral study. Sci Rep. 2022, 12, 2296. [Google Scholar] [CrossRef]
- Al-Marjani, M.F. Presence of qnr gene in environmental and clinical Pseudomonas aeruginosa isolates in Baghdad. Int. J. Curr. Microbiol. Appl. Sci. 2014, 3, 853–857. [Google Scholar]
- Yang, X.; Xing, B.; Liang, C.; Ye, Z.; Zhang, Y. Prevalence and fluoroquinolone resistance of Pseudomonas aeruginosa in a hospital of South China. Int. J. Clin. Exp. Med. 2015, 8, 1386–1390. [Google Scholar]
- Liu, J.; Yang, L.; Li, L.; Li, B.; Chen, D.; Xu, Z. Comparative genomic analyses of two novel qnrVC6 carrying multidrug-resistant Pseudomonas. spp strains, Microb. Pathog. 2018, 123, 269–274. [Google Scholar] [CrossRef]
- Venkataramana, G.P.; Lalitha, A.K.V.; Mariappan, S.; Sekar, U. Plasmid-Mediated Fluoroquinolone Resistance in Pseudomonas aeruginosa and Acinetobacter baumannii. J. Lab. Physicians 2022, 14, 271–277. [Google Scholar] [CrossRef]
- Lin, J.; Chen, D.Q.; Hong, J.; Huang, H.; Xu, X. Prevalence of qnrVC Genes in Pseudomonas aeruginosa Clinical Isolates from Guangdong, China. Curr. Microbiol. 2020, 77, 1532–1539. [Google Scholar] [CrossRef]
- Taha, S.A.; Omar, H.H. Characterization of plasmid-mediated qnrA and qnrB genes among Enterobacteriaceae strains: Quinolone resistance and ESBL production in Ismailia, Egypt. Egypt. J. Med. Hum. Genet. 2019, 20, 1–7. [Google Scholar] [CrossRef]
- Elena, A.; Quinteros, M.; Di Conza, J.; Gutkind, G.; Cejas, D.; Radice, M.A. Full characterization of an IncR plasmid harboring qnrS1 recovered from a VIM-11-producing Pseudomonas aeruginosa. Rev. Argent. Microbiol. 2020, 52, 298–304. [Google Scholar] [CrossRef]
- Araujo, B.F.; Ferreira, M.L.; Campos, P.A.; Royer, S.; Batistão, D.W.; Dantas, R.C.; Gonçalves, I.R.; Faria, A.L.; Brito, C.S.; Yokosawa, J.; et al. Clinical and Molecular Epidemiology of Multidrug-Resistant P. aeruginosa Carrying aac (6′)-Ib-cr, qnrS1 and blaSPM Genes in Brazil. PLoS ONE 2016, 11, e0155914. [Google Scholar] [CrossRef]
- Kocsis, B.; Toth, A.; Gulyas, D.; Ligeti, B.; Katona, K.; Rokusz, L.; Szabo, D. Acquired qnrVC1 and blaNDM-1 resistance markers in an international high-risk Pseudomonas aeruginosa ST773 clone. J. Med. Microbiol. 2019, 68, 336–338. [Google Scholar] [CrossRef]
- Domokos, J.; Kristóf, K.; Szabó, D. Plasmid-mediated quinolone resistance among extended spectrum beta lactase producing Enterobacteriaceae from bloodstream infections. Acta Microbiol. Immunol. Hung. 2016, 63, 313–323. [Google Scholar] [CrossRef]
- Oliver, A.; Rojo-Molinero, E.; Arca-Suarez, J.; Beşli, Y.; Bogaerts, P.; Cantón, R.; Cimen, C.; Croughs, P.D.; Denis, O.; Giske, C.G.; et al. Pseudomonas aeruginosa antimicrobial susceptibility profiles, resistance mechanisms and international clonal lineages: Update from ESGARS-ESCMID/ISARPAE Group. Clin. Microbiol. Infect. Off. Publ. Eur. Soc. Clin. Microbiol. Infect. Dis. 2023, 30, 469–480. [Google Scholar] [CrossRef]
- Ruiz, J. Transferable mechanisms of Quinolone Resistance from 1998 onward. Clin. Microbiol. Rev. 2019, 32, e00007–19. [Google Scholar] [CrossRef]
- Liao, C.H.; Hsueh, P.R.; Jacoby, G.A.; Hooper, D.C. Risk factors and clinical characteristics of patients with qnr-positive Klebsiella pneumoniae bacteraemia. J. Antimicrob. Chemother. 2013, 68, 2907–2914. [Google Scholar] [CrossRef]
- Hoseinzadeh, M.; Sedighi, M.; Yahyapour, Y.; Javanian, M.; Beiranvand, M.; Mohammadi, M.; Zarei, S.; Pournajaf, A.; Ebrahimzadeh Namvar, A. Prevalence of plasmid-mediated quinolone resistance genes in extended-spectrum beta-lactamase producing Klebsiella pneumoniae isolates in northern Iran. Heliyon 2024, 10, e37534. [Google Scholar] [CrossRef]
- Yuan, F.; Xiao, W.; Wang, X.; Fu, Y.; Wei, X. Clinical characteristics and prognosis of bloodstream infection with carbapenem-resistant pseudomonas aeruginosa in patients with hematologic malignancies. Infect. Drug Resist. 2023, 16, 4943–4952. [Google Scholar] [CrossRef]
- Aslan, A.T.; Akova, M. Recent updates in treating carbapenem-resistant infections in patients with hematological malignancies. Expert Rev. Anti Infect. Ther. 2024, 1–17. [Google Scholar] [CrossRef] [PubMed]
- López-García, A.; Del Carmen Rocha-Gracia, R.; Bello-López, E.; Juárez-Zelucualtecalt, C.; Sáenz, Y.; Castañeda-Lucio, M.; López-Piego, L.; González-Vázquez, M.C.; Torres, C.; Ayala-Nuñez, T.; et al. Characterization of antimicrobial resistance mechanisms in carbapenem-resistant Pseudomonas aeruginosa carrying IMP variants recovered form a Mexican Hospital. Infect. Drug. Resist. 2018, 11, 1523–1536. [Google Scholar] [CrossRef] [PubMed]
- Spilker, T.; Coenye, T.; Vandamme, P.; LiPuma, J.J. PCR-based assay for differentiation of Pseudomonas aeruginosa from other Pseudomonas species recovered from cystic fibrosis patients. J Clin Microbiol. 2004, 42, 2074–2079. [Google Scholar] [CrossRef] [PubMed]
- CLSI. Clinical Laboratory Standard Institute. Performance Standards for Antimicrobial Susceptibility Testing, 30th ed.; CLSI document M100-ED30; Clinical and Laboratory Standards Institute: Wayne, PA, USA, 2020. [Google Scholar]
- Magiorakos, A.P.; Srinivasan, A.; Carey, R.B.; Carmeli, Y.; Falagas, M.E.; Giske, C.G.; Harbarth, S.; Hindler, J.F.; Kahlmeter, G.; Olsson-Liligequist, B.; 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. [Google Scholar] [CrossRef]
- Sambrook, J.; Russell, D.W. Molecular Cloning, A Laboratory Manual, 3rd ed.; Cold Spring Harbor Laboratory: Cold Spring Harbor, NY, USA, 2001. [Google Scholar]
- Maynard, C.; Fairbrother, J.M.; Bekal, S.; Sanschagrin, F.; Levesque, R.C.; Brousseau, R.; Masson, L.; Lariviere, S.; Harel, J. Antimicrobial resistance genes in enterotoxigenic Escherichia coli O149:K91 isolates obtained over a 23-year period from pigs. Antimicrob. Agents Chemother. 2003, 47, 3214–3221. [Google Scholar] [CrossRef]
- Cerezales, M.; Biniossek, L.; Gerson, S.; Xanthopoulou, K.; Wille, J.; Wohlfarth, E.; Kaase, M.; Seifert, H.; Higgins, P.G. Novel multiplex PCRs for detection of the most prevalent carbapenemase genes in Gram-negative bacteria within Germany. J. Med. Microbiol. 2021, 70, 3214–3221. [Google Scholar] [CrossRef]
- Robicsek, A.; Strahilevitz, J.; Sahm, D.F.; Jacoby, G.A.; Hooper, D.C. qnr prevalence in ceftazidime-resistant Enterobacteriaceae isolates from the United States. Antimicrob. Agents Chemother. 2006, 50, 2872–2874. [Google Scholar] [CrossRef]
- Wang, M.; Guo, Q.; Xu, X.; Wang, X.; Ye, X.; Wu, S.; Hooper, D.C.; Wang, M. New plasmid-mediated quinolone resistance gene, qnrC, found in a clinical isolates of Proteus mirabilis. Antimicrob. Agents Chemother. 2009, 53, 1892–1897. [Google Scholar] [CrossRef]
- Cavaco, L.M.; Hasman, H.; Xia, S.; Aarestrup, F.M. qnrD, a novel gene conferring transferable quinolone resistance in Salmonella enterica serovar Kentucky and Bovismorbificans strains of human origin. Antimicrob. Agents Chemother. 2009, 53, 603–608. [Google Scholar] [CrossRef]
- Park, C.H.; Robicsek, A.; Jacoby, G.A.; Sahm, D.; Hooper, D.C. Prevalence in the United States of aac (6′)-Ib-cr encoding a ciprofloxacin-modifying enzyme. Antimicrob. Agents Chemother. 2006, 50, 3953–3955. [Google Scholar] [CrossRef]
- Chen, X.; Zhang, W.; Pan, W.; Yin, J.; Pan, Z.; Gao, S.; Jiao, X. Prevalence of qnr, aac (6′)-Ib-cr, qepA, and oqxAB in Escherichia coli Isolates from Humans, Animals, and the Environment. Antimicrob. Agents Chemother. 2012, 56, 3423–3427. [Google Scholar] [CrossRef] [PubMed]
- Cai, B.; Echols, R.; Magee, G.; Arjona Ferreira, J.C.; Morgan, G.; Ariyasu, M.; Sawada, T.; Nagata, T.D. Prevalence of Carbapenem-Resistant Gram-Negative Infections in the United States Predominated by Acinetobacter baumannii and Pseudomonas aeruginosa. Open Forum Infect. Dis. 2017, 4, ofx176. [Google Scholar] [CrossRef] [PubMed]
- Palavutitotai, N.; Jitmuang, A.; Tongsai, S.; Kiratisin, P.; Angkasekwinai, N. Epidemiology and risk factors of extensively drug-resistant Pseudomonas aeruginosa infections. PLoS ONE 2018, 13, e0193431. [Google Scholar] [CrossRef]
- Kim, Y.J.; Jun, Y.H.; Kim, Y.R.; Park, K.G.; Park, Y.J.; Kang, J.Y.; Kim, S.I. Risk factors for mortality in patients with Pseudomonas aeruginosa bacteremia; retrospective study of impact of combination antimicrobial therapy. BMC Infect. Dis. 2014, 14, 161. [Google Scholar] [CrossRef] [PubMed]
- Frem, J.A.; Doumat, G.; Kazma, J.; Gharamti, A.; Kanj, S.S.; Fayad, A.G.A.; Matar, G.M.; Kanafani, Z.A. Clinical predictors of mortality in patients with Pseudomonas aeruginosa infection. PLoS ONE 2013, 18, e0282276. [Google Scholar] [CrossRef]
- Martínez-Zavaleta, M.G.; Fernández-Rodríguez, D.; Hernández-Durán, M.; Colín-Castro, C.A.; García-Hernández, M.d.L.; Becerra-Lobato, N.; Franco-Cendejas, R.; López-Jácome, L.E. Acquired blaVIM and blaGES Carbapenemase-Encoding Genes in Pseudomonas aeruginosa: A Seven-Year Survey Highlighting an Increasing Epidemiological Threat. Pathogens 2023, 12, 1256. [Google Scholar] [CrossRef]
- Kawa, D.E.; Tickler, I.A.; Tenover, F.C.; Shettima, S.A. Characterization of Beta-Lactamase and Fluoroquinolone Resistance Determinants in Escherichia coli, Klebsiella pneumoniae, and Pseudomonas aeruginosa Isolates from a Tertiary Hospital in Yola, Nigeria. Trop. Med. Infect. Dis. 2023, 8, 500. [Google Scholar] [CrossRef]
- Yano, H.; Hayashi, W.; Kawakami, S.; Aoki, S.; Anzai, E.; Zuo, H.; Kitamura, N.; Hirabayashi, A.; Kajihara, T.; Kayama, S.; et al. Nationwide genome surveillance of carbapenem-resistant Pseudomonas aeruginosa in Japan. Antimicrob. Agents Chemother. 2024, 68, e0166923. [Google Scholar] [CrossRef]
- Galindo-Méndez, M.; Navarrete-Salazar, H.; Pacheco-Vásquez, R.; Quintas-de la Paz, D.; Baltazar-Jiménez, I.; Santiago-Luna, J.D.; Guadarrama-Monroy, L. Detection of Plasmid-Mediated Resistance against Colistin in Multi-Drug-Resistant Gram-Negative Bacilli Isolated from a Tertiary Hospital. Microorganisms 2023, 11, 1996. [Google Scholar] [CrossRef]
- Xiao, S.Z.; Chu, H.Q.; Han, L.Z.; Zhang, Z.M.; Li, B.; Zhao, L.; Xu, L. Resistant mechanisms and molecular epidemiology of imipenem-resistant Acinetobacter baumannii. Mol. Med. Rep. 2016, 14, 2483–2488. [Google Scholar] [CrossRef]
- Uwingabiye, J.; Lemnouer, A.; Roca, I.; Alouane, T.; Frikh, M.; Belefquih, B.; Bssaibis, F.; Maleb, A.; Benlahlou, Y.; Kassouati, J.; 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. [Google Scholar] [CrossRef] [PubMed]
- Nitz, F.; de Melo, B.O.; da Silva, L.C.N.; de Souza Monteiro, A.; Marques, S.G.; Monteiro-Neto, V.; de Jesus Gomes Turri, R.; Junior, A.D.S.; Conceição, P.C.R.; Magalhães, H.J.C.; et al. Molecular Detection of Drug-Resistance Genes of blaOXA-23-blaOXA-51 and mcr-1 in Clinical Isolates of Pseudomonas aeruginosa. Microorganisms 2021, 9, 786. [Google Scholar] [CrossRef] [PubMed]
- Gondal, A.J.; Choudhry, N.; Niaz, A.; Yasmin, N. Molecular Analysis of Carbapenem and Aminoglycoside Resistance Genes in Carbapenem-Resistant Pseudomonas aeruginosa Clinical Strains: A Challenge for Tertiary Care Hospitals. Antibiotics 2024, 13, 191. [Google Scholar] [CrossRef] [PubMed]
- Tarafdar, F.; Jafari, B.; Azimi, T. Evaluating the antimicrobial resistance patterns and molecular frequency of blaOXA-48 and blaGES-2 genes in Pseudomonas aeruginosa and Acinetobacter baumannii strains isolated from burn wound infection in Tehran, Iran. New Microbes New Infect. 2020, 37, 100686. [Google Scholar] [CrossRef] [PubMed]
- Wolter, D.J.; Hanson, N.D.; Lister, P.D. Insertional inactivation of oprD in clinical isolates of Pseudomonas aeruginosa leading to carbapenem resistance. FEMS Microbiol. Lett. 2004, 236, 137–143. [Google Scholar] [CrossRef]
- Karakonstantis, S.; Kritsotakis, E.I.; Gikas, A. Treatment options for K. pneumoniae, P. aeruginosa and A. baumannii co-resistant to carbapenems, aminoglycosides, polymyxins and tigecycline: An approach based on the mechanisms of resistance to carbapenems. Infection 2020, 48, 835–851. [Google Scholar] [CrossRef]
- Galani, I.; Papoutsaki, V.; Karantani, I.; Karaiskos, I.; Galani, L.; Adamou, P.; Deliolais, I.; Kodonaki, A.; Papadogeogarki, E.; Markopoulou, M.; et al. In vitro activity of ceftolozane/tazobactam alone and in combination with amikacin against MDR/XDR Pseudomonas aeruginosa isolates from Greece. J. Antimicrob. Chemother. 2020, 75, 2164–2172. [Google Scholar] [CrossRef]
- Nang, S.C.; Li, J.; Velkov, T. The rise and spread of mcr plasmid-mediated polymyxin resistance. Crit. Rev. Microbiol. 2019, 45, 131–161. [Google Scholar] [CrossRef]
- El-Baky, R.M.A.; Masoud, S.M.; Mohamed, D.S.; Waly, N.G.; Shafik, E.; A Mohareb, D.; Elkady, A.; Elbadr, M.M.; Hetta, H.F. Prevalence and Some Possible Mechanisms of Colistin Resistance among Multidrug-Resistant and Extensively Drug-Resistant Pseudomonas aeruginosa. Infect. Drug Resist. 2020, 13, 323–332. [Google Scholar] [CrossRef]
- Snesrud, E.; Maybank, R.; Kwak, Y.I.; Jones, A.R.; Hinkle, M.K.; McGann, P. Chromosomally Encoded mcr-5 in Colistin-Nonsusceptible Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 2018, 62, e00679-e18. [Google Scholar] [CrossRef]
- Abdelrahim, S.S.; Hassuna, N.A.; Waly, N.G.F.M.; Kotb, D.N.; Abdelhamid, H.; Zaki, S. Coexistence of plasmid-mediated quinolone resistance (PMQR) and extended-spectrum beta-lactamase (ESBL) genes among clinical Pseudomonas aeruginosa isolates in Egypt. BMC Microbiol. 2024, 24, 175. [Google Scholar] [CrossRef] [PubMed]
- Nouri, R.; Ahangarzadeh Rezaee, M.; Hasani, A.; Aghazadeh, M.; Asgharzadeh, M. The role of gyrA and parC mutations in fluoroquinolones-resistant Pseudomonas aeruginosa isolates from Iran. Braz. J. Microbiol. 2016, 47, 925–930. [Google Scholar] [CrossRef] [PubMed]
- Andres, P.; Lucero, C.; Soler-Bistué, A.; Guerriero, L.; Albornoz, E.; Tran, T.; Zorreguieta, A.; PMQR Group; Galas, M.; Corso, A.; et al. Differential distribution of plasmid-mediated quinolone resistance genes in clinical enterobacteria with unusual phenotypes of quinolone susceptibility from Argentina. Antimicrob. Agents Chemother. 2013, 57, 2467–2475. [Google Scholar] [CrossRef] [PubMed]
- Goudarzi, M.; Azad, M.; Seyedjavadi, S.S. Prevalence of plasmid-mediated quinolone resistance determinants and oqxab efflux pumps among extended-spectrum β-lactamase producing Klebsiella pneumoniae isolated from patients with nosocomial urinary tract infection in Tehran, Iran. Scientifica 2015, 2015, 1–7. [Google Scholar] [CrossRef]
- Agyepong, N.; Govinden, U.; Owusu-Ofori, A.; Amoako, D.G.; Allam, M.; Janice, J.; Pedersen, T.; Sundsfjord, A.; Essack, S. Genomic characterization of multidrug-resistant ESBL-producing Klebsiella pneumoniae isolated from a Ghanaian teaching hospital. Int. J. Infect. Dis. 2019, 85, 117–123. [Google Scholar] [CrossRef]
- Li, J.; Zhang, H.; Ning, J.; Sajid, A.; Cheng, G.; Yuan, Z.; Hao, H. The nature and epidemiology of OqxAB, a multidrug efflux pump. Antimicrob. Resist. Infect. Control. 2019, 8, 44. [Google Scholar] [CrossRef]
- Amereh, F.; Arabestani, M.R.; Shokoohizadeh, L. Relationship of OqxAB efflux pump to antibiotic resistance, mainly fluoroquinolones in Klebsiella pneumoniae, isolated from hospitalized patients. Iran. J. Basic Med. Sci. 2023, 26, 93–98. [Google Scholar] [CrossRef]
- Nazik, H.; Ongen, B.; Kuvat, N. Investigation of plasmid-mediated quinolone resistance among isolates obtained in a Turkish intensive care unit. Jpn. J. Infect. Dis. 2008, 61, 310–312. [Google Scholar] [CrossRef]
- Nordmann, P.; Poirel, L. Emergence of plasmid-mediated resistance to quinolones in Enterobacteriaceae. J. Antimicrob. Chemother. 2005, 56, 463–469. [Google Scholar] [CrossRef]
- Jiang, X.; Yu, T.; Jiang, X.; Zhang, W.; Zhang, L.; Ma, J. Emergence of plasmid-mediated quinolone resistance genes in clinical isolates of Acinetobacter baumannii and Pseudomonas aeruginosa in Henan, China. Diagn. Micr. Infec. Dis. 2014, 79, 381–383. [Google Scholar] [CrossRef]
- Belotti, P.T.; Thabet, L.; Laffargue, A.; André, C.; Coulange-Mayonnove, L.; Arpin, C.; Messadi, A.; M’ Zali, F.; Quentin, C.; Dubois, V. Description of an original integron encompassing blaVIM-2, qnrVC1 and genes encoding bacterial group II intron proteins in Pseudomonas aeruginosa. J. Antimicrob. Chemother. 2015, 70, 2237–2240. [Google Scholar] [CrossRef] [PubMed]
- Sarjana Safain, K.; Bhuyan, G.S.; Hassan Hasib, S.; Islam, M.S.; Mahmud-Un-Nabi, M.A.; Sultana, R.; Tasnim, S.; Noor, F.A.; Sarker, S.K.; Islam, M.T.; et al. Genotypic and phenotypic profiles of antibiotic-resistant bacteria isolated from hospitalised patients in Bangladesh. Trop. Med. Int. Health 2021, 26, 720–729. [Google Scholar] [CrossRef] [PubMed]
- Pachori, P.; Gothalwal, R.; Gandhi, P. Emergence of antibiotic resistance Pseudomonas aeruginosa in intensive care unit; a critical review. Genes Dis. 2019, 6, 109–119. [Google Scholar] [CrossRef] [PubMed]
Variables | Total n, (%) | Death 30-Day After Culture (%), [n = 13] | Non-Death 30 Days After Culture (%), [n = 39] | a Odds Ratios (95% CI) | b p Value |
---|---|---|---|---|---|
Clinical characteristics | |||||
Female | 24 (46.2) | 5 (38.5) | 19 (48.7) | Reference | |
Male | 28 (53.8) | 8 (61.5) | 20 (51.3) | 0.66 (0.18–2.37) | 0.522 |
Age category | |||||
20–49 | 19 (36.5) | 4 (30.8) | 15 (38.5) | 1.41 (0.37–5.39) | 0.619 |
50–64 | 16 (30.8) | 4 (30.8) | 12 (30.8) | 1 (0.26–3.9) | 1.000 |
≥65 | 17 (32.7) | 5 (38.5) | 12 (30.8) | 1.41 (0.38–5.2) | 0.609 |
Specimen type | |||||
Respiratory | 34 (65.4) | 10 (76.9) | 24 (61.5) | 0.48 (0.11–2.03) | 0.319 |
Urine | 13 (25.0) | 1 (7.7) | 12 (30.8) | 0.19 (0.02–1.61) | 0.127 |
Blood | 2 (3.8) | 1 (7.7) | 1 (2.6) | 0.32 (0.02–5.44) | 0.427 |
Biopsy | 3 (5.8) | 1 (7.7) | 2 (5.1) | 0.65 (0.05–7.8) | 0.733 |
Co-morbidities | |||||
Diabetes mellitus | 27 (51.9) | 8 (61.5) | 19 (48.7) | 0.59 (0.16–2.14) | 0.425 |
Systemic arterial hypertension | 30 (57.7) | 8 (61.5) | 22 (56.4) | 1.24 (0.34–4.47) | 0.746 |
Chronic kidney disease | 3 (5.8) | 0 (0) | 3 (7.7) | - | - |
Congestive heart failure | 4 (7.7) | 2 (15.4) | 2 (5.1) | 0.3 (0.04–2.36) | 0.251 |
Hypothyroidism | 7 (13.5) | 0 (0) | 7 (17.9) | - | - |
Obesity | 33 (63.5) | 8 (61.5) | 25 (64.1) | 1.12 (0.31–4.07) | 0.868 |
COVID-19 | 35 (67.3) | 10 (76.9) | 25 (64.1) | 0.54 (0.13–2.28) | 0.398 |
Charlson Comorbidity Index | |||||
<3 | 28 (53.8) | 4 (30.8) | 24 (61.5) | Reference | |
≥3 | 24 (46.2) | 9 (69.2) | 15 (38.5) | 0.8 (0.54–1.18) | 0.1063 |
Complication | |||||
Mechanical ventilation | 43 (82.7) | 12 (92.3) | 31 (79.5) | 0.32 (0.04–2.87) | 0.310 |
Pneumonia associated with mechanical ventilation | 43 (82.7) | 12 (92.3) | 31 (79.5) | 0.32 (0.04–2.87) | 0.310 |
Tracheostomy | 28 (53.8) | 6 (46.2) | 22 (56.4) | 1.51(0.43–5.33) | 0.522 |
Septic shock | 25 (48.1) | 10 (76.9) | 15 (38.5) | 0.19 (0.04–0.79) | 0.023 |
ICU | 21 (40.4) | 6 (46.2) | 15 (38.5) | 0.73 (0.21–2.59) | 0.625 |
Antibiotic exposure in the previous 90 days | |||||
Any antibiotics | |||||
Yes | 40 (76.9) | 10 (76.9) | 30 (76.9) | 1.0 (0.23–4.44) | 1.000 |
No | 12 (23.1) | 3 (23.1) | 9 (23.1) | ||
Adequate treatment | |||||
Yes | 34 (65.4) | 8 (61.5) | 26 (66.7) | 0.8 (0.22–2.94) | 0.737 |
No | 18 (34.6) | 5 (38.5) | 13 (33.3) | ||
Antimicrobial resistance | |||||
b MDR | 15 (28.8) | 1 (7.7) | 14 (35.9) | 0.15 (0.02–1.27) | 0.081 |
XDR | 30 (57.7) | 11 (84.6) | 19 (48.7) | 0.17 (0.03–0.88) | c 0.035 |
PDR | 7 (13.5) | 1 (7.7) | 6 (15.4) | 2.18 (0.24–20.44) | 0.491 |
Antimicrobial Class | Antimicrobial Agent | Susceptibility (%) | ||
---|---|---|---|---|
Susceptible | Intermediate | Resistant | ||
Quinolones | Ciprofloxacin (n = 52) | 6 (11.5) | 0 (0) | 46 (88.5) |
Carbapenems | Imipenem (n = 44) | 0 (0) | 0 (0) | 44 (100) |
Meropenem (n = 51) | 0 (0) | 0 (0) | 51 (100) | |
Doripenem (n = 44) | 0 (0) | 0 (0) | 44 (100) | |
Polymyxin E | Colistin (n = 44) | 36 (81.8) | 5 (11.4) | 3 (6.8) |
Glycylcline | Tigecycline (n = 42) | 0 (0) | 0 (0) | 42 (100) |
Penicillin and beta-lactamase inhibitors | Piperacillin/tazobactam (n = 39) | 3 (7.7) | 8 (20.5) | 28 (71.8) |
Cephalosporins | Cefepime (n = 52) | 7 (13.5) | 5 (9.6) | 40 (76.9) |
Ceftazidime (n = 48) | 4 (8.3) | 4 (8.3) | 40 (83.3) | |
Ceftriaxone (n = 48) | 0 (0) | 0 (0) | 48 (100) | |
Aminoglycosides | Amikacin (n = 52) | 14 (26.9) | 0 (0) | 38 (73.1) |
Gentamicin (n = 52) | 9 (17.3) | 4 (7.7) | 39 (75.0) |
a Antibiotics | Ciprofloxacin-Resistant | Ciprofloxacin-Susceptible | * p-Value | ||||
---|---|---|---|---|---|---|---|
R, n (%) | I, n (%) | S, n (%) | R, n (%) | I, n (%) | S, n (%) | ||
Colistin (n = 44) CIP-R (n = 38), CIP-S (n = 6) | 2 (5.3) | 4 (10.5) | 32 (84.2) | 1 (16.65) | 1 (16.65) | 4 (66.7) | 0.2968 |
Tigecycline (n = 42) CIP-R (n = 36), CIP-S (n = 6) | 36 (100) | 0 (0) | 0 (0) | 6 (100) | 0 (0) | 0 (0) | >0.9999 |
Piperacillin/tazobactam (n = 39) CIP-R (n = 34), CIP-S (n = 5) | 26 (76.5) | 5 (14.7) | 3 (8.8) | 2 (40) | 3 (60) | 0 (0) | 0.0871 |
Cefepime (n = 52) CIP-R (n = 46), CIP-S (n = 6) | 39 (84.8) | 3 (6.5) | 4 (8.7) | 1 (16.7) | 2 (33.3) | 3 (50) | 0.0018 |
Ceftazidime (n = 48) CIP-R (n = 42), CIP-S (n = 6) | 38 (90.4) | 2 (4.8) | 2 (4.8) | 2 (33.33) | 2 (33.33) | 2 (33.33) | 0.0046 |
Ceftriaxone (n = 48) CIP-R (n = 43), CIP-S (n = 5) | 43 (100) | 0 (0) | 0 (0) | 5 (100) | 0 (0) | 0 (0) | >0.9999 |
Amikacin (n = 52) CIP-R (n = 46), CIP-S (n = 6) | 40 (87.0) | 0 (0) | 6 (13.0) | 0 (0) | 0 (0) | 6 (100) | <0.0001 |
Gentamicin (n = 52) CIP-R (n = 46), CIP-S (n = 6) | 39 (84.8) | 4 (8.7) | 3 (6.5) | 0 (0) | 0 (0) | 6 (100) | <0.0001 |
Carbapenemase-Encoding Genes | PMQR Genes | PMCR a | CIP-Susceptibility b | Total Prevalence (N = 52) | |||||
---|---|---|---|---|---|---|---|---|---|
MBL | OXA | SBL | Qnr Variants | Efflux Pumps | Aminoglycoside Variant | mcr-1 | R c n = 46, (%) | S d n = 6, (%) | |
blaIMP | blaOXA-51 | qnrC | oqxA | aac-(6´)-lb | 1 (2.2) | 0 (0.0) | 1 (1.9) | ||
blaIMP | blaOXA-51 | 1 (2.2) | 0 (0.0) | 1 (1.9) | |||||
blaNDM | blaOXA-1 | aac-(6´)-lb | 1 (2.2) | 0 (0.0) | 1 (1.9) | ||||
blaNDM | blaOXA-1 | 1 (2.2) | 0 (0.0) | 1 (1.9) | |||||
blaNDM | oqxA | 1 (2.2) | 0 (0.0) | 1 (1.9) | |||||
blaVIM | blaOXA-51 | aac-(6´)-lb | 1 (2.2) | 0 (0.0) | 1 (1.9) | ||||
blaVIM | blaOXA-51 | 1 (2.2) | 0 (0.0) | 1 (1.9) | |||||
blaVIM | blaOXA-51 | oqxA | 0 (0.0) | 1 (16.7) | 1 (1.9) | ||||
blaVIM | blaKPC | qnrB, qnrC, qnrS | oqxA | 1 (2.2) | 0 (0.0) | 1 (1.9) | |||
blaVIM | blaOXA-48 | qnrS | mcr-1 | 1 (2.2) | 0 (0.0) | 1 (1.9) | |||
blaVIM | blaOXA-51, blaOXA-1 | 1 (2.2) | 0 (0.0) | 1 (1.9) | |||||
blaVIM | aac-(6´)-lb | 1 (2.2) | 0 (0.0) | 1 (1.9) | |||||
blaVIM | 0 (0.0) | 1 (16.7) | 1 (1.9) | ||||||
blaOXA-1 | 2 (4.3) | 0 (0.0) | 2 (3.8) | ||||||
blaOXA-1 | qnrS | aac-(6´)-lb | 1 (2.2) | 0 (0.0) | 1 (1.9) | ||||
blaGES | qnrB, qnrS | oqxA | 0 (0.0) | 1 (16.7) | 1 (1.9) | ||||
blaOXA-48 | blaKPC | qnrS | oqxA | 0 (0.0) | 1 (16.7) | 1 (1.9) | |||
blaOXA-48 | qnrS | oqxA | 1 (2.2) | 0 (0.0) | 1 (1.9) | ||||
blaOXA-51 | blaKPC | oqxA | 1 (2.2) | 0 (0.0) | 1 (1.9) | ||||
blaOXA-51, blaOXA-1 | oqxA | 1 (2.2) | 0 (0.0) | 1 (1.9) | |||||
blaOXA-51, blaOXA-1 | oqxA | aac-(6´)-lb | 1 (2.2) | 0 (0.0) | 1 (1.9) | ||||
blaOXA-51, blaOXA-48 | 1 (2.2) | 0 (0.0) | 1 (1.9) | ||||||
blaOXA-51 | aac-(6´)-lb | 2 (4.3) | 0 (0.0) | 2 (3.8) | |||||
blaOXA-51 | oqxA | 4 (8.7) | 0 (0.0) | 4 (7.7) | |||||
blaOXA-51 | 4 (8.7) | 0 (0.0) | 4 (7.7) | ||||||
blaOXA-51 | qnrC | oqxA | 1 (2.2) | 0 (0.0) | 1 (1.9) | ||||
blaOXA-51 | oqxA | aac-(6´)-lb | 1 (2.2) | 0 (0.0) | 1 (1.9) | ||||
qnrC, qnrS | oqxA | 2 (4.3) | 1 (16.7) | 3 (5.8) | |||||
qnrC | 1 (2.2) | 0 (0.0) | 1 (1.9) | ||||||
oqxA | aac-(6´)-lb | 1 (2.2) | 0 (0.0) | 1 (1.9) | |||||
oqxA | 3 (6.5) | 1 (16.7) | 4 (7.7) | ||||||
aac-(6´)-lb | 3 (6.5) | 0 (0.0) | 3 (5.8) | ||||||
- | - | - | - | - | - | 5 (10.9) | 0 (0.0) | 5 (9.6) |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2024 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Tapia-Cornejo, A.S.; Ramírez-Castillo, F.Y.; Guerrero-Barrera, A.L.; Guillen-Padilla, D.E.; Arreola-Guerra, J.M.; González-Gámez, M.; Avelar-González, F.J.; Loera-Muro, A.; Hernández-Cuellar, E.; Ramos-Medellín, C.L.; et al. Occurrence of Plasmid-Mediated Quinolone Resistance and Carbapenemase-Encoding Genes in Pseudomonas aeruginosa Isolates from Nosocomial Patients in Aguascalientes, Mexico. Pathogens 2024, 13, 992. https://doi.org/10.3390/pathogens13110992
Tapia-Cornejo AS, Ramírez-Castillo FY, Guerrero-Barrera AL, Guillen-Padilla DE, Arreola-Guerra JM, González-Gámez M, Avelar-González FJ, Loera-Muro A, Hernández-Cuellar E, Ramos-Medellín CL, et al. Occurrence of Plasmid-Mediated Quinolone Resistance and Carbapenemase-Encoding Genes in Pseudomonas aeruginosa Isolates from Nosocomial Patients in Aguascalientes, Mexico. Pathogens. 2024; 13(11):992. https://doi.org/10.3390/pathogens13110992
Chicago/Turabian StyleTapia-Cornejo, Ana S., Flor Y. Ramírez-Castillo, Alma L. Guerrero-Barrera, Diana E. Guillen-Padilla, José M. Arreola-Guerra, Mario González-Gámez, Francisco J. Avelar-González, Abraham Loera-Muro, Eduardo Hernández-Cuellar, Carmen L. Ramos-Medellín, and et al. 2024. "Occurrence of Plasmid-Mediated Quinolone Resistance and Carbapenemase-Encoding Genes in Pseudomonas aeruginosa Isolates from Nosocomial Patients in Aguascalientes, Mexico" Pathogens 13, no. 11: 992. https://doi.org/10.3390/pathogens13110992
APA StyleTapia-Cornejo, A. S., Ramírez-Castillo, F. Y., Guerrero-Barrera, A. L., Guillen-Padilla, D. E., Arreola-Guerra, J. M., González-Gámez, M., Avelar-González, F. J., Loera-Muro, A., Hernández-Cuellar, E., Ramos-Medellín, C. L., Adame-Álvarez, C., García-Romo, R., Galindo-Guerrero, F., & Moreno-Flores, A. C. (2024). Occurrence of Plasmid-Mediated Quinolone Resistance and Carbapenemase-Encoding Genes in Pseudomonas aeruginosa Isolates from Nosocomial Patients in Aguascalientes, Mexico. Pathogens, 13(11), 992. https://doi.org/10.3390/pathogens13110992