Mechanisms of Resistance in Gram-Negative Urinary Pathogens: From Country-Specific Molecular Insights to Global Clinical Relevance
Abstract
:1. Urinary Tract Infections: Introduction, Epidemiology, Pathophysiology, and Pathogen Profile
2. The Evolving Story of Resistance Determinants
3. Escherichia coli
4. Klebsiella pneumoniae
5. Pseudomonas aeruginosa
6. Acinetobacter baumannii
7. Resistance “Snapshot” in Other Notable Gram-Negative Urinary Tract Pathogens
8. Laboratory Identification of Resistance Mechanisms as a Prerequisite for Targeted Treatment
9. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Öztürk, R.; Murt, A. Epidemiology of urological infections: A global burden. World J. Urol. 2020, 38, 2669–2679. [Google Scholar] [CrossRef]
- Kaur, R.; Kaur, R. Symptoms, risk factors, diagnosis and treatment of urinary tract infections. Postgrad. Med. J. 2020. [Google Scholar] [CrossRef]
- McLellan, L.K.; Hunstad, D.A. Urinary Tract Infection: Pathogenesis and Outlook. Trends Mol. Med. 2016, 22, 946–957. [Google Scholar] [CrossRef] [Green Version]
- Meštrović, T.; Matijašić, M.; Perić, M.; Čipčić Paljetak, H.; Barešić, A.; Verbanac, D. The Role of Gut, Vaginal, and Urinary Microbiome in Urinary Tract Infections: From Bench to Bedside. Diagnostics 2020, 11, 7. [Google Scholar] [CrossRef]
- Cavallo, J.D.; Tenke, P. Urinary tract infections. In European Manual of Clinical Microbiology, 1st ed.; Cornaglia, G., Courcol, R., Herrmann, J.L., Kahlmeter, G., Peigue-Lafeuille, H., Vila, J., Eds.; SFM–ESCMID: Paris, France; Basel, Switzerland, 2012; pp. 133–143. [Google Scholar]
- Guglietta, A. Recurrent urinary tract infections in women: Risk factors, etiology, pathogenesis and prophylaxis. Future Microbiol. 2017, 12, 239–246. [Google Scholar] [CrossRef]
- Zhao, F.; Yang, H.; Bi, D.; Khaledi, A.; Qiao, M. A systematic review and meta-analysis of antibiotic resistance patterns, and the correlation between biofilm formation with virulence factors in uropathogenic E. coli isolated from urinary tract infections. Microb. Pathog. 2020, 144, 104196. [Google Scholar] [CrossRef]
- Gupta, K.; Grigoryan, L.; Trautner, B. Urinary Tract Infection. Ann. Intern. Med. 2017, 167, ITC49–ITC64. [Google Scholar] [CrossRef]
- Škerk, V.; Andrašević, A.T.; Andrašević, S.; Sušić, E.; Džepina, A.M.; Mađarić, V.; Milutinović, S.; Krhen, I.; Perić, L.; Bagatin, J.; et al. ISKRA guidelines on antimicrobial treatment and prophylaxis of urinary tract infections–Croatian national guidelines. Lijec. Vjesn. 2009, 131, 105–118. [Google Scholar]
- Leung, A.K.C.; Wong, A.H.C.; Leung, A.A.M.; Hon, K.L. Urinary Tract Infection in Children. Recent. Pat. Inflamm. Allergy Drug. Discov. 2019, 13, 2–18. [Google Scholar] [CrossRef]
- Schmiemann, G.; Kniehl, E.; Gebhardt, K.; Matejczyk, M.M.; Hummers-Pradier, E. The diagnosis of urinary tract infection: A systematic review. Dtsch. Arztebl. Int. 2010, 107, 361–367. [Google Scholar] [CrossRef]
- Ternes, B.; Wagenlehner, F.M.E. Guideline-based treatment of urinary tract infections. Urologe A 2020, 59, 550–558. [Google Scholar] [CrossRef]
- Flores-Mireles, A.L.; Walker, J.N.; Caparon, M.; Hultgren, S.J. Urinary tract infections: Epidemiology, mechanisms of infection and treatment options. Nat. Rev. Microbiol. 2015, 13, 269–284. [Google Scholar] [CrossRef]
- Khoshnood, S.; Heidary, M.; Mirnejad, R.; Bahramian, A.; Sedighi, M.; Mirzaei, H. Drug-resistant gram-negative uropathogens: A review. Biomed. Pharmacother. 2017, 94, 982–994. [Google Scholar] [CrossRef]
- Kline, K.A.; Lewis, A.L. Gram-Positive Uropathogens, Polymicrobial Urinary Tract Infection, and the Emerging Microbiota of the Urinary Tract. Microbiol. Spectr. 2016, 4. [Google Scholar] [CrossRef] [Green Version]
- Kranz, J.; Wagenlehner, F.M.E.; Schneidewind, L. Complicated urinary tract infections. Urologe A 2020, 59, 1480–1485. [Google Scholar] [CrossRef]
- Kliebe, C.; Nies, B.; Meyer, J.; Tolxdorf-Neutzling, R.; Wiedemann, B. Evolution of plasmid encoded resistance to broad-spectrum cephalosporins. Antimicrob. Agents Chemother. 1985, 28, 302–327. [Google Scholar] [CrossRef] [Green Version]
- Bradford, P.A. Extended-spectrum beta-lactamases in the 21st Century: Characterization, Epidemiology, and Detection of This Important Resistance Threat. Clin. Microbiol. Rev. 2001, 14, 933–951. [Google Scholar] [CrossRef] [Green Version]
- Jacoby, G.A.; Munoz-Price, L.S. The new β-lactamases. N. Engl. J. Med. 2005, 352, 380–391. [Google Scholar] [CrossRef]
- Płusa, T.; Konieczny, R.; Baranowska, A.; Szymczak, Z. The growing resistance of bacterial strains to antibiotics. Pol. Merkur. Lekarski. 2019, 47, 106–110. [Google Scholar]
- Doi, Y.; Iovleva, A.; Bonomo, R.A. The ecology of extended-spectrum β-lactamases (ESBLs) in the developed world. J. Travel Med. 2017, 24, S44–S51. [Google Scholar] [CrossRef]
- Bonnet, R. Growing group of extended-spectrum β-lactamases: The CTX-M enzymes. Antimicrob. Agents Chemother. 2004, 48, 1–14. [Google Scholar] [CrossRef] [Green Version]
- Rossolini, G.M.; D’Andrea, M.M.; Mugnaioli, C. The spread of CTX-M-type extended-spectrum β-lactamases. Clin. Microbiol. Infect. 2008, 14, 33–41. [Google Scholar] [CrossRef] [Green Version]
- Gniadkowski, M.; Palucha, A.; Grzesiowski, P.; Hryniewicz, W. Outbreak of ceftazidime-resistant Klebsiella pneumoniae in Warsaw, Poland; Clonal spread of the TEM-47 Extended-spectrum β-lactamase (ESBL)-producing strain and transfer of a plasmid carrying the SHV-5 like ESBL-encoding gene. Antimicrob. Agents Chemother. 1998, 42, 3079–3085. [Google Scholar]
- Shannon, K.; Stapleton, P.; Xiang, X.; Johnson, A.; Beattie, H.; El Bakri, F.; Cookson, B.; French, G. Extended-spectrum β-lactamase-producing Klebsiella pneumoniae strains causing nosocomial outbreak of infection in the United Kingdom. J. Clin. Microbiol. 1998, 36, 3105–3110. [Google Scholar]
- Silva, J.; Gatica, R.; Aguilar, C.; Beccera, Z.; Garza-Ramos, U.; Velazquez, M.; Miranda, G.; Leanos, B.; Solorzano, F.; Echaniz, G. Outbreak of infections with extended-spectrum β-lactamase producing Klebsiella pneumoniae in a Mexican Hospital. J. Clin. Microbiol. 2001, 39, 3193–3196. [Google Scholar] [CrossRef] [Green Version]
- Essack, S.Y. Treatment options for extended-spectrum β-lactamase producers. FEMS Microbiol. Lett. 2000, 190, 181–184. [Google Scholar] [CrossRef] [Green Version]
- Jacoby, G.A. AmpC β-lactamases. J. Clin. Microbiol. 2009, 22, 161–182. [Google Scholar] [CrossRef] [Green Version]
- Elshamy, A.A.; Aboshanab, K.M. A review on bacterial resistance to carbapenems: Epidemiology, detection and treatment options. Future Sci. OA 2020, 6, FSO438. [Google Scholar] [CrossRef] [Green Version]
- Queenan, A.M.; Bush, K. Carbapenemases: The versatile β-lactamases. Clin. Microbiol. Rev. 2007, 20, 440–458. [Google Scholar] [CrossRef] [Green Version]
- Canton, R.; Akova, M.; Carmeli, Y.; Giske, C.G.; Glupczynski, Y.; Gniadkowski, M.; Livermore, D.M.; Miriagou, V.; Naas, T.; Rossolini, G.M.; et al. Rapid evolution and spread of carbapenemases among Enterobacteriaceae in Europe. Clin. Microbiol. Infect. 2012, 18, 413–431. [Google Scholar] [CrossRef] [Green Version]
- Peirano, G.; Pitout, J.D.D. Extended-Spectrum β-Lactamase-Producing Enterobacteriaceae: Update on Molecular Epidemiology and Treatment Options. Drugs 2019, 79, 1529–1541. [Google Scholar] [CrossRef]
- Onanuga, A.; Mahindroo, J.; Singh, S.; Taneja, N. Phenotypic and molecular characterization of antimicrobial resistant Escherichia coli from urinary tract infections in Port-Harcourt, Nigeria. Pan Afr. Med. J. 2019, 34, 144. [Google Scholar] [CrossRef]
- Thapa Shrestha, U.; Shrestha, S.; Adhikari, N.; Rijal, K.R.; Shrestha, B.; Adhikari, B.; Banjara, M.R.; Ghimire, P. Plasmid Profiling and Occurrence of β-Lactamase Enzymes in Multidrug-Resistant Uropathogenic Escherichia coli in Kathmandu, Nepal. Infect. Drug Resist. 2020, 13, 1905–1917. [Google Scholar] [CrossRef]
- Chong, Y.; Shimoda, S.; Shimono, N. Current epidemiology, genetic evolution and clinical impact of extended-spectrum β-lactamase-producing Escherichia coli and Klebsiella pneumoniae. Infect. Genet. Evol. 2018, 61, 185–188. [Google Scholar] [CrossRef]
- Millán, Y.; Hernández, E.; Millán, B.; Araque, M. Distribution of phylogenetic groups and virulence factors in CTX-M-15 β-lactamase-producing uropathogenic Escherichia coli strains isolated from patients in the community of Mérida, Venezuela. Rev. Argent. Microbiol. 2014, 46, 175–181. [Google Scholar] [CrossRef] [Green Version]
- Millán, Y.; Araque, M.; Ramírez, A. Distribution of phylogenetic groups, virulence factors and antimicrobial susceptibility in strains of uropathogenic Escherichia coli. Rev. Chilena. Infectol. 2020, 37, 117–123. [Google Scholar] [CrossRef]
- Biset, S.; Moges, F.; Endalamaw, D.; Eshetie, S. Multi-drug resistant and extended-spectrum β-lactamases producing bacterial uropathogens among pregnant women in Northwest Ethiopia. Ann. Clin. Microbiol. Antimicrob. 2020, 19, 25. [Google Scholar] [CrossRef]
- Tayh, G.; Al Laham, N.; Ben Yahia, H.; Ben Sallem, R.; Elottol, A.E.; Ben Slama, K. Extended-Spectrum β-Lactamases among Enterobacteriaceae Isolated from Urinary Tract Infections in Gaza Strip, Palestine. Biomed. Res. Int. 2019, 2019, 4041801. [Google Scholar] [CrossRef] [Green Version]
- Majeed, H.T.; Aljanabi, A.J. Antibiotic susceptibility patterns and prevalence of some extended-spectrum β-lactamase genes in Gram-negative bacteria isolated from patients infected with urinary tract infections in Al-Najaf City, Iraq. Avicenna J. Med. Biotechnol. 2019, 11, 192–201. [Google Scholar]
- Cristea, V.C.; Gheorghe, I.; Czobor Barbu, I.; Popa, L.I.; Ispas, B.; Grigore, G.A.; Bucatariu, I.; Popa, G.L.; Angelescu, M.C.; Velican, A.; et al. Snapshot of Phylogenetic Groups, Virulence, and Resistance Markers in Escherichia coli Uropathogenic Strains Isolated from Outpatients with Urinary Tract Infections in Bucharest, Romania. Biomed. Res. Int. 2019, 2019, 5712371. [Google Scholar] [CrossRef] [Green Version]
- Tonkić, M.; Bedenić, B.; Goić-Barišić, I.; Katić, S.; Kalenić, S.; Kaufmann, M.E.; Woodford, N.; Punda-Polić, V. First report of CTX-M extended-spectrum beta-lactamase-producing isolates from croatia. J. Chemother. 2007, 19, 97–100. [Google Scholar] [CrossRef]
- Literacka, E.; Bedenić, B.; Baraniak, A.; Fiett, J.; Tonkić, M.; Jajić-Benčić, I.; Gniadkowski, M. BlaCTX-M genes in Escherichia coli from Croatian hospitals are located in new (blaCTX-M-3) and widely spread (blaCTX-M-3a, blaCTX-M-15) genetic structures. Antimicrob. Agents Chemother. 2009, 53, 1630–1635. [Google Scholar] [CrossRef] [Green Version]
- Krilanović, M.; Tomić-Paradžik, M.; Meštrović, T.; Beader, N.; Herljević, Z.; Conzemius, R.; Barišić, I.; Vraneš, J.; Elveđi-Gašparović, V.; Bedenić, B. Extended-spectrum beta-lactamases and plasmid diversity in urinary isolates of Escherichia coli in Croatia: A nation-wide, multicentric, retrospective study. Folia Microbiol. (Praha) 2020, 65, 649–667. [Google Scholar] [CrossRef]
- Bedenić, B.; Vraneš, J.; Hofmann-Thiel, S.; Tonkić, M.; Novak, A.; Bučević-Popović, V.; Hoffmann, H. Characterization of the extended-spectrum beta-lactamases and determination of the virulence factors of uropathogenic Escherichia coli strains isolated from children. Wien. Klin. Wochenschr. 2012, 124, 504–515. [Google Scholar] [CrossRef] [Green Version]
- Shrestha, R.; Khanal, S.; Poudel, P.; Khadayat, K.; Ghaju, S.; Bhandari, A.; Lekhak, S.; Pant, N.D.; Sharma, M.; Marasini, B.P. Extended spectrum β-lactamase producing uropathogenic Escherichia coli and the correlation of biofilm with antibiotics resistance in Nepal. Ann. Clin. Microbiol. Antimicrob. 2019, 18, 42. [Google Scholar] [CrossRef]
- Calbo, E.; Romani, V.; Xercavins, M.; Gomez, L.; Vidal, C.G.; Quintana, S.; Vila, J.; Gara, J. Risk factors for community-onset urinary tract infections due to Escherichia coli harbouring extended-spectrum β-lactamases. J. Antimicrob. Chemother. 2006, 57, 780–783. [Google Scholar] [CrossRef] [Green Version]
- Meier, S.; Weber, R.; Zbinden, R.; Ruef, C.; Hasse, B. Extended-spectrum beta-lactamase producing Gram-negative pathogens in community-acquired urinary tract infections; an increasing challenge for antimicrobial therapy. Infection 2011, 39, 333–340. [Google Scholar] [CrossRef] [Green Version]
- Fagerström, A.; Mölling, P.; Khan, F.A.; Sundqvist, M.; Jass, J.; Söderquist, B. Comparative distribution of extended-spectrum beta-lactamase-producing Escherichia coli from urine infections and environmental waters. PLoS ONE 2019, 14, e0224861. [Google Scholar] [CrossRef] [Green Version]
- Moradi, Y.; Eshrati, B.; Motevalian, S.A.; Majidpour, A.; Baradaran, H.R. A systematic review and meta-analysis on the prevalence of Escherichia coli and extended-spectrum β-lactamase-producing Escherichia coli in pregnant women. Arch. Gynecol. Obstet. 2021, 303, 363–379. [Google Scholar] [CrossRef]
- M’Zali, F.H.; Heritage, J.; Gascoyne-Binzi, D.M.; Denton, M.; Todd, N.J.; Hawkey, P.M. Transcontinental importation into the UK of Escherichia coli expressing a plasmid-mediated AmpC-type beta-lactamase exposed during an outbreak of SHV-5 extended-spectrum beta-lactamase in a Leeds hospital. J. Antimicrob. Chemother. 1997, 40, 823–831. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bradford, P.A.; Jacobus, N.V.; Bhachech, N.; Bush, K. TEM-28 from an Escherichia coli clinical isolate is a member of the His-164 family of TEM-1 extended-spectrum beta-lactamases. Antimicrob. Agents Chemother. 1996, 40, 260–262. [Google Scholar] [CrossRef] [Green Version]
- Arpin, C.; Dubois, V.; Coulange, L.; André, C.; Fischer, I.; Noury, P.; Grobost, F.; Brochet, J.P.; Jullin, J.; Dutilh, B.; et al. Extended-spectrum beta-lactamase-producing Enterobacteriaceae in community and private health care centers. Antimicrob. Agents Chemother. 2003, 47, 3506–3514. [Google Scholar] [CrossRef] [Green Version]
- Bou, G.; Cartelle, M.; Tomas, M.; Canle, D.; Molina, F.; Moure, R.; Eiros, J.M.; Guerrero, A. Identification and broad dissemination of the CTX-M-14 beta-lactamase in different Escherichia coli strains in the northwest area of Spain. J. Clin. Microbiol. 2002, 40, 4030–4036. [Google Scholar] [CrossRef] [Green Version]
- Rodríguez-Baño, J.; Navarro, M.D.; Romero, L.; Martínez-Martínez, L.; Muniain, M.A.; Perea, E.J.; Pérez-Cano, R.; Pascual, A. Epidemiology and clinical features of infections caused by extended-spectrum beta-lactamase-producing Escherichia coli in nonhospitalized patients. J. Clin. Microbiol. 2004, 42, 1089–1094. [Google Scholar] [CrossRef] [Green Version]
- Teshager, T.; Domínguez, L.; Moreno, M.A.; Saénz, Y.; Torres, C.; Cardeñosa, S. Isolation of an SHV-12 beta-lactamase-producing Escherichia coli strain from a dog with recurrent urinary tract infections. Antimicrob. Agents Chemother. 2000, 44, 3483–3484. [Google Scholar] [CrossRef] [Green Version]
- Blazquez, J.; Baquero, M.R.; Canton, R.; Alos, I.; Baquero, F. Characterization of a new TEM-type beta-lactamase resistant to clavulanate, sulbactam, and tazobactam in a clinical isolate of Escherichia coli. Antimicrob. Agents Chemother. 1993, 37, 2059–2063. [Google Scholar] [CrossRef] [Green Version]
- Pitout, J.D.D.; Peirano, G.; Kock, M.M.; Strydom, K.A.; Matsumura, Y. The Global Ascendency of OXA-48-Type Carbapenemases. Clin. Microbiol. Rev. 2019, 33, e00102-19. [Google Scholar] [CrossRef]
- Irfan, S.; Azhar, A.; Bashir, A.; Ahmed, S.; Haque, A. High frequency of simultaneous presence of ESBL and carbapenemase producers among nosocomial coliform isolates in Faisalabad, Pakistan. Pak. J. Med. Sci. 2021, 37, 34–39. [Google Scholar] [CrossRef]
- Aladag, M.O.; Uysal, A.; Dundar, N.; Durak, Y.; Gunes, E. Characterization of Klebsiella pneumoniae strains isolated from urinary tract infections: Detection of ESBL characteristics, antibiotic susceptibility and RAPD genotyping. Pol. J. Microbiol. 2013, 62, 401–409. [Google Scholar]
- Marques, C.; Menezes, J.; Belas, A.; Aboim, C.; Cavaco-Silva, P.; Trigueiro, G.; Telo Gama, L.; Pomba, C. Klebsiella pneumoniae causing urinary tract infections in companion animals and humans: Population structure, antimicrobial resistance and virulence genes. J. Antimicrob. Chemother. 2019, 74, 594–602. [Google Scholar] [CrossRef]
- Taraghian, A.; Nasr Esfahani, B.; Moghim, S.; Fazeli, H. Characterization of Hypervirulent Extended-Spectrum β-Lactamase-Producing Klebsiella pneumoniae Among Urinary Tract Infections: The First Report from Iran. Infect. Drug Resist. 2020, 13, 3103–3111. [Google Scholar] [CrossRef]
- Thomson, K.S.; Sanders, C.C.; Washington, J.A., 2nd. High-level resistance to cefotaxime and ceftazidime in Klebsiella pneumoniae isolates from Cleveland, Ohio. Antimicrob. Agents Chemother. 1991, 35, 1001–1003. [Google Scholar] [CrossRef] [Green Version]
- Podbielski, A.; Schönling, J.; Melzer, B.; Warnatz, K.; Leusch, H.G. Molecular characterization of a new plasmid-encoded SHV-type beta-lactamase (SHV-2 variant) conferring high-level cefotaxime resistance upon Klebsiella pneumoniae. J. Gen. Microbiol. 1991, 137, 569–578. [Google Scholar] [CrossRef] [Green Version]
- Gruteke, P.; Goessens, W.; Van Gils, J.; Peerbooms, P.; Lemmens-Den Toom, N.; Van Santen-Verheuvel, M.; Van Belkum, A.; Verbrugh, H. Patterns of resistance associated with integrons, the extended-spectrum beta-lactamase SHV-5 gene, and a multidrug efflux pump of Klebsiella pneumoniae causing a nosocomial outbreak. J. Clin. Microbiol. 2003, 41, 1161–1166. [Google Scholar] [CrossRef] [Green Version]
- Damjanova, I.; Tóth, A.; Pászti, J.; Jakab, M.; Milch, H.; Bauernfeind, A.; Füzi, M. Epidemiology of SHV-type beta-lactamase-producing Klebsiella spp. from outbreaks in five geographically distant Hungarian neonatal intensive care units: Widespread dissemination of epidemic R-plasmids. Int. J. Antimicrob. Agents 2007, 29, 665–671. [Google Scholar] [CrossRef]
- Gniadkowski, M.; Schneider, I.; Jungwirth, R.; Hryniewicz, W.; Bauernfeind, A. Ceftazidime-resistant Enterobacteriaceae isolates from three Polish hospitals: Identification of three novel TEM- and SHV-5-type extended-spectrum beta-lactamases. Antimicrob. Agents Chemother. 1998, 42, 514–520. [Google Scholar] [CrossRef] [Green Version]
- Brun-Buisson, C.; Legrand, P.; Philippon, A.; Montravers, F.; Ansquer, M.; Duval, J. Transferable enzymatic resistance to third-generation cephalosporins during nosocomial outbreak of multiresistant Klebsiella pneumoniae. Lancet 1987, 2, 302–306. [Google Scholar] [CrossRef]
- Girlich, D.; Poirel, L.; Leelaporn, A.; Karim, A.; Tribuddharat, C.; Fennewald, M.; Nordmann, P. Molecular epidemiology of the integron-located VEB-1 extended-spectrum beta-lactamase in nosocomial enterobacterial isolates in Bangkok, Thailand. J. Clin. Microbiol. 2001, 39, 175–182. [Google Scholar] [CrossRef] [Green Version]
- Verdet, C.; Benzerara, Y.; Gautier, V.; Adam, O.; Ould-Hocine, Z.; Arlet, G. Emergence of DHA-1-producing Klebsiella spp. in the Parisian region: Genetic organization of the ampC and ampR genes originating from Morganella morganii. Antimicrob. Agents Chemother. 2006, 50, 607–617. [Google Scholar] [CrossRef] [Green Version]
- Bedenić, B.; Žagar, Ž. Extended-spectrum beta-lactamases in clinical isolates of Klebsiella pneumoniae from Zagreb, Croatia. J. Chemother. 1998, 10, 449–459. [Google Scholar] [CrossRef]
- Bedenić, B.; Randegger, C.; Stobberingh, E.; Haechler, H. Molecular epidemiology of extended-spectrum beta-lactamases from Klebsiella pneumoniae strains isolated in Zagreb, Croatia. Eur. J. Clin. Microbiol. Infect. Dis. 2001, 20, 505–508. [Google Scholar] [CrossRef]
- Vranić-Ladavac, M.; Bošnjak, Z.; Beader, N.; Barišić, N.; Kalenić, S.; Bedenić, B. Clonal spread of CTX-M producing Klebsiella pneumoniae in Croatian hospital. J. Med. Microbiol. 2010, 59, 1069–1078. [Google Scholar] [CrossRef] [Green Version]
- Bedenić, B.; Vraneš, J.; Bošnjak, Z.; Marijan, T.; Mlinarić-Džepina, A.; Kukovec, T.; Anušić, M.; Beader, N.; Barl, P.; Leskovar, V.; et al. Emergence of CTX-M group 1 extended-spectrum β-lactamase-producing Klebsiella pneumoniae strains in the community. Med. Glas. (Zenica) 2010, 7, 32–39. [Google Scholar]
- Zujić-Atalić, V.; Bedenić, B.; Kocsis, E.; Mazzariol, A.; Sardelić, S.; Barišić, M.; Plečko, V.; Bošnjak, Z.; Mijač, M.; Jajić, I.; et al. Diversity of carbapenemases in clinical isolates of Enterobacteriaceae in Croatia—The results of the multicenter study. Clin. Microbiol. Infect. 2014, 20, O894–O903. [Google Scholar] [CrossRef] [Green Version]
- Bedenić, B.; Sardelić, S.; Luxner, J.; Bošnjak, Z.; Varda-Brkić, D.; Lukić-Grlić, A.; Mareković, I.; Frančula-Zaninović, S.; Krilanović, M.; Šijak, D.; et al. Molecular characterization of class B carbapenemases in advanced stage of dissemination and emergence of class D carbapenemases in Enterobacteriaceae from Croatia. Infect. Genetic. Evol. 2016, 43, 74–82. [Google Scholar] [CrossRef] [Green Version]
- Bedenić, B.; Slade, M.; Starčević, L.Ž.; Sardelić, S.; Vranić-Ladavac, M.; Benčić, A.; Zujić Atalić, V.; Bogdan, M.; Bubonja-Šonje, M.; Tomić-Paradžik, M.; et al. Epidemic spread of OXA-48 beta-lactamase in Croatia. J. Med. Microbiol. 2018, 67, 1031–1034. [Google Scholar] [CrossRef]
- Behzadi, P.; Baráth, Z.; Gajdács, M. It’s Not Easy Being Green: A Narrative Review on the Microbiology, Virulence and Therapeutic Prospects of Multidrug-Resistant Pseudomonas aeruginosa. Antibiotics 2021, 10, 42. [Google Scholar] [CrossRef]
- Sardelić, S.; Bedenić, B.; Colinon-Dupuich, C.; Orhanović, S.; Bošnjak, Z.; Plečko, V.; Cournoyer, B.; Rossolini, G.M. Infrequent finding of metallo-β-lactamase VIM-2 in carbapenem-resistant Pseudomonas aeruginosa from Croatia. Antimicrob. Agents Chemother. 2012, 56, 2746–2749. [Google Scholar] [CrossRef] [Green Version]
- Sorour, A.E.; Wali, I.E.; El-Hodaky, K. OXA-type beta-lactamases among extended-spectrum-cephalosporins non-susceptible Pseudomonas aeruginosa isolates collected from a large teaching hospital in Cairo. Egypt. J. Med. Microbiol. 2008, 17, 565–572. [Google Scholar]
- Rahimzadeh, M.; Habibi, M.; Bouzari, S.; Karam, M.R.A. First study of antimicrobial activity of ceftazidime-avibactam and ceftolozone-tazobactam against Pseudomonas aeruginosa isolated from patients with urinary tract infections in Tehran, Iran. Infect. Drug Resist. 2020, 13, 533–541. [Google Scholar] [CrossRef] [Green Version]
- Pagani, L.; Mantengoli, E.; Migliavacca, R.; Nucleo, E.; Pollini, S.; Spalla, M.; Daturi, R.; Romero, E.; Rossolini, G.M. Multifocal detection of multidrug-resistant Pseudomonas aeruginosa producing PER-1 extended-spectrum β-lactamase in Northern Italy. J. Clin. Microbiol. 2004, 42, 2523–2529. [Google Scholar] [CrossRef] [Green Version]
- Poirel, L.; Lebessi, E.; Castro, M.; Fèvre, C.; Foustoukou, M.; Nordmann, P. Nosocomial outbreak of extended-spectrum beta-lactamase SHV-5-producing isolates of Pseudomonas aeruginosa in Athens, Greece. Antimicrob. Agents Chemother. 2004, 48, 2277–2279. [Google Scholar] [CrossRef] [Green Version]
- Bošnjak, Z.; Bedenić, B.; Mazzariol, A.; Jarža-Davila, N.; Šuto, S.; Kalenić, S. VIM-2 beta-lactamase in Pseudomonas aeruginosa isolates from Zagreb, Croatia. Scand. J. Infect. Dis. 2010, 42, 193–197. [Google Scholar] [CrossRef] [Green Version]
- Bubonja-Šonje, M.; Matovina, M.; Škrobonja, I.; Bedenić, B.; Abram, M. Mechanisms of carbapenem-resistance in multidrug-resistant clinical isolates of Pseudomonas aeruginosa from a Croatian Hospital. Microb. Drug Resist. 2015, 21, 261–269. [Google Scholar] [CrossRef] [Green Version]
- Ramirez, M.S.; Bonomo, R.A.; Tolmasky, M.E. Carbapenemases: Transforming Acinetobacter baumannii into a Yet More Dangerous Menace. Biomolecules 2020, 10, 720. [Google Scholar] [CrossRef]
- Franolić-Kukina, I.; Bedenić, B.; Budimir, A.; Herljević, Z.; Vraneš, J.; Higgins, P. Clonal spread of carbapenem-resistant OXA-72 positive Acinetobacter baumannii in a Croatian university hospital. Int. J. Infect. Dis. 2011, 15, e706–e709. [Google Scholar] [CrossRef] [Green Version]
- Goić-Barišić, I.; Towner, K.J.; Kovačić, A.; Sisko-Kraljević, K.; Tonkić, M.; Novak, A.; Punda-Polić, V. Outbreak in Croatia caused by a new carbapenem-resistant clone of Acinetobacter baumannii producing OXA-72 carbapenemase. J. Hosp. Infect. 2011, 77, 368–369. [Google Scholar] [CrossRef]
- Vranić-Ladavac, M.; Bedenić, B.; Minandri, F.; Ištok, M.; Frančula-Zaninović, S.; Ladavac, R.; Visca, P. Carbapenem-resistance and acquired class D carbapenemases in Acinetobacter baumannii from Croatia 2009-2010. Eur. J. Clin. Microbiol. Infect. Dis. 2014, 33, 471–478. [Google Scholar] [CrossRef]
- Ladavac, R.; Bedenić, B.; Vranić-Ladavac, M.; Barišić, N.; Karčić, N.; Pompe, K.; Ferenčić, A.; Stojanović, A.; Seifert, H.; Katić, S.; et al. Emergence of different Acinetobacter baumannii clones in a Croatian hospital and correlation with antibiotic susceptibility. J. Glob. Antimicrob. Resist. 2017, 10, 213–218. [Google Scholar] [CrossRef] [Green Version]
- Petrović, T.; Uzunović, S.; Barišić, I.; Luxner, J.; Grisold, A.; Zarfel, G.; Ibrahimagić, A.; Jakovac, S.; Slaćanac, D.; Bedenić, B. Arrival of carbapenem-hydrolyzing-oxacillinases in Acinetobacter baumannii in Bosnia and Herzegovina. Infect. Genet. Evol. 2018, 58, 192–198. [Google Scholar] [CrossRef] [Green Version]
- Pournaras, S.; Markogiannakis, A.; Ikonomidis, A.; Kondyli, L.; Bethimouti, K.; Maniatis, A.N.; Legakis, N.J.; Tsakris, A. Outbreak of multiple clones of imipenem-resistant Acinetobacter baumannii isolates expressing OXA-58 carbapenemase in an intensive care unit. J. Antimicrob. Chemother. 2006, 57, 557–561. [Google Scholar] [CrossRef]
- Sardelić, S.; Bedenić, B.; Šijak, D.; Colinon, C.; Kalenić, S. Emergence of Proteus mirabilis isolates producing TEM-52 extended-spectrum β-lactamase in Croatia. Chemotherapy 2010, 56, 208–213. [Google Scholar] [CrossRef]
- Migliavacca, R.; Nucleo, E.; D’Andrea, M.M.; Spalla, M.; Giani, T.; Pagani, L. Acquired AmpC type beta-lactamases: An emerging problem in Italian long-term care and rehabilitation facilities. New Microbiol. 2007, 30, 295–298. [Google Scholar]
- Bedenić, B.; Firis, N.; Elveđi-Gašparović, V.; Krilanović, M.; Matanović, K.; Štimac, I.; Luxner, J.; Vraneš, J.; Meštrović, T.; Zarfel, G.; et al. Emergence of multidrug-resistant Proteus mirabilis in a long-term care facility in Croatia. Wien. Klin. Wochenschr. 2016, 128, 404–413. [Google Scholar] [CrossRef] [Green Version]
- Meštrović, T.; Lukić-Grlić, A.; Bogdan, M.; Bandić-Pavlović, D.; Cavrić, G.; Drenjančević, D.; Sreter, B.K.; Benčić, A.; Sardelić, S.; Bedenić, B. Cephalosporinases in Proteus mirabilis isolates from long-term care facilities and the community. Acta Med. Croat. 2018, 3, 285–294. [Google Scholar]
- Franolić-Kukina, I.; Sardelić, S.; Beader, N.; Varda-Brkić, D.; Firis, N.; Čačić, M.; Šijak, D.; Frančula-Zaninović, S.; Elveđi-Gašparović, V.; Mareković, I.; et al. Evolution of beta-lactam antibiotic resistance in Enterobacter spp. in Croatia. Lijec. Vjesn. 2016, 138, 240–249. [Google Scholar]
- Franolić, I.; Bedenić, B.; Beader, N.; Lukić-Grlić, A.; Mihaljević, S.; Bielen, L.; Zarfel, G.; Meštrović, T. NDM-1-producing Enterobacter aerogenes isolated from a patient with a JJ ureteric stent in situ. CEN Case Rep. 2019, 8, 38–41. [Google Scholar] [CrossRef]
- Apfalter, P.; Assadian, O.; Daxböck, F.; Hirschl, A.M.; Rotter, M.L.; Makristathis, A. Extended double disc synergy testing reveals a low prevalence of extended-spectrum beta-lactamases in Enterobacter spp. in Vienna, Austria. J. Antimicrob. Chemother. 2007, 59, 854–859. [Google Scholar] [CrossRef] [Green Version]
- Sidjabat, H.E.; Hanson, N.D.; Smith-Moland, E.; Bell, J.M.; Gibson, J.S.; Filippich, L.J.; Trott, D.J. Identification of plasmid-mediated extended-spectrum and AmpC beta-lactamases in Enterobacter spp. isolated from dogs. J. Med. Microbiol. 2007, 56, 426–434. [Google Scholar] [CrossRef] [Green Version]
- Barl, P.; Bedenić, B.; Sardelić, S.; Uzunović-Kamberović, S.; Vraneš, J.; Plečko, V. Spread of CTX-M-15 positive Providencia spp. causing urinary tract infections at the University Hospital Split in Croatia. Med. Glas. (Zenica) 2012, 9, 317–324. [Google Scholar]
- Jarlier, V.; Nicolas, M.H.; Fournier, G.; Philippon, A. Extended broad-spectrum beta-lactamases conferring transferable resistance to newer beta-lactam agents in Enterobacteriaceae: Hospital prevalence and susceptibility patterns. Rev. Infect. Dis. 1988, 10, 867–878. [Google Scholar] [CrossRef]
- Clinical and Laboratory Standards Institute (CLSI). Performance Standards for Antimicrobial Susceptibility Testing; CLSI M100 2020 Edition, M100-S; CLSI: Wayne, PA, USA, 2020. [Google Scholar]
- Lee, K.; Lim, Y.S.; Yong, D.; Yum, J.H.; Chong, Y. Evaluation of the Hodge test and the imipenem-EDTA-double-disk synergy test for differentiating metallo-β-lactamase-producing isolates of Pseudomonas spp. and Acinetobacter spp. J. Clin. Microbiol. 2005, 41, 4623–4629. [Google Scholar] [CrossRef] [Green Version]
- van der Zwaluw, K.; de Haan, A.; Pluister, G.N.; Bootsma, H.J.; de Neeling, A.J.; Schouls, L.M. The carbapenem-inacitvation method (CIM) a simple and low-cost alternative for the Carba NP test to assess phenotypic carbapenemase activity in Gram-negative rods. PLoS ONE 2015, 10, e0123690. [Google Scholar] [CrossRef] [Green Version]
- Simon, M.; Richert, K.; Pfennigwerth, N.; Pfeifer, Y.; Reischl, U.; Gatermann, S.; Gessner, A.; Jantsch, J. Carbapenemase detection using the β-CARBA test: Influence of test conditions on performance and comparison with the RAPIDEC CarbaNP assay. J. Microbiol. Methods 2018, 147, 17–19. [Google Scholar] [CrossRef]
- Meštrović, T.; Bedenić, B. eComment. Diagnostic intricacies and fortuitous treatment approaches for carbapenem-resistant Klebsiella pneumoniae. Interact. Cardiovasc. Thorac. Surg. 2016, 23, 768. [Google Scholar] [CrossRef] [Green Version]
- Pasteran, F.; Gonzalez, L.; Albornoz, E.; Bahr, G.; Vila, A.; Corso, A. Triton Hodge Test: Improved Protocol for Modified Hodge Test for Enhanced Detection of NDM and Other Carbapenemase Producers. J. Clin. Microbiol. 2015, 54, 640–649. [Google Scholar] [CrossRef] [Green Version]
- Cointe, A.; Bonacorsi, S.; Truong, J.; Hobson, C.; Doit, C.; Monjault, A.; Bidet, P.; Birgy, A. Detection of Carbapenemase-Producing Enterobacteriaceae in Positive Blood Culture Using an Immunochromatographic RESIST-4 O.K.N.V. Assay. Antimicrob. Agents Chemother. 2018, 62. [Google Scholar] [CrossRef]
- Wilkinson, K.; Winstanley, T.; Lanyon, C.; Cummings, S.; Raza, M.; Perry, J. Comparison of Four Chromogenic Culture Media for Carbapenemase-Producing Enterobacteriaceae. J. Clin. Microbiol. 2012, 50, 3102–3104. [Google Scholar] [CrossRef] [Green Version]
- Arlet, G.; Brami, G.; Decre, D.; Flippo, A.; Gaillot, O.; Lagrange, P.H.; Phillipon, A. Molecular characterization by PCR restriction fragment polymorphism of TEM β-lactamases. FEMS Microbiol. Lett. 1995, 134, 203–208. [Google Scholar] [CrossRef] [Green Version]
- Nüesch-Inderbinen, M.T.; Hächler, H.; Kayser, F.H. Detection of genes coding for extended-spectrum SHV β-lactamases in clinical isolates by a molecular genetic method, and comparison with the E test. Eur. J. Clin. Microbiol. Infect. Dis. 1996, 15, 398–402. [Google Scholar] [CrossRef]
- Woodford, N.; Ward, M.E.; Kaufmann, M.E.; Turton, J.; Fagan, E.J.; James, D.; Johnson, A.P.; Pike, R.; Warner, M.; Cheasty, T.; et al. Community and hospital spread of Escherichia coli producing CTX-M extended-spectrum β-lactamases in the UK. J. Antimicrob. Chemother. 2004, 54, 735–743. [Google Scholar] [CrossRef]
- Perez-Perez, F.J.; Hanson, N.D. Detection of plasmid-mediated AmpC β-lactamase genes in clinical isolates by using multiplex PCR. J. Clin. Microbiol. 2002, 40, 2153–2162. [Google Scholar] [CrossRef] [Green Version]
- Poirel, L.; Walsh, T.R.; Cuveiller, V.; Nordman, P. Multiplex PCR for detection of acquired carbapenemases genes. Diagn. Microbiol. Infect. Dis. 2011, 70, 119–125. [Google Scholar] [CrossRef]
- Robicsek, A.; Jacoby, G.A.; Hooper, D.C. The worldwide emergence of plasmid-mediated quinolone resistance. Lancet Infect. Dis. 2006, 6, 629–640. [Google Scholar] [CrossRef]
- Tal Jasper, R.; Coyle, J.R.; Katz, D.E.; Marchaim, D. The complex epidemiology of extended-spectrum β-lactamase-producing Enterobacteriaceae. Future Microbiol. 2015, 10, 819–839. [Google Scholar] [CrossRef]
- Naas, T.; Cuzon, G.; Truong, H.; Bernabeu, S.; Nordmann, P. Evaluation of a DNA microarray, the check-points ESBL/KPC array, for rapid detection of TEM, SHV, and CTX-M extended-spectrum beta-lactamases and KPC carbapenemases. Antimicrob. Agents Chemother. 2010, 54, 3086–3092. [Google Scholar] [CrossRef] [Green Version]
- Oviaño, M.; Fernández, B.; Fernández, A.; Barba, M.J.; Mouriño, C.; Bou, G. Rapid detection of Enterobacteriaceae producing extended spectrum beta-lactamases directly from positive blood cultures by matrix-assisted laser desorption ionization-time of flight mass spectrometry. Clin. Microbiol. Infect. 2014, 20, 1146–1157. [Google Scholar] [CrossRef] [Green Version]
- Ota, Y.; Furuhashi, K.; Hirai, N.; Ishikawa, J.; Nagura, O.; Yamanaka, K.; Maekawa, M. Evaluation of MBT STAR-Cepha and MBT STAR-Carba kits for the detection of extended-spectrum β-lactamases and carbapenemase producing microorganisms using matrix-assisted laser desorption/ionization time-of-flight mass spectrometry. J. Microbiol. Methods 2021, 183, 106166. [Google Scholar] [CrossRef]
ESBL | AmpC | Carbapenemases | Aminoglycoside Resistance Mechanisms | Fluoroquinolone Resistance Mechanisms | References | |
---|---|---|---|---|---|---|
(Sorted Alphabetically) | ||||||
Escherichia Coli | CTX-M-1 CTX-M-3 CTX-M-14 CTX-M-9 CTX-M-15 CTX-M-27 CTX-M-30 SHV-7 OXA-1 TEM-21 TEM-22 TEM-28 IRT-3 SHV-12 | CMY-2 | KPC VIM IMP OXA-48 Efflux pumps | aacC2 | qnrA, qnrB, qnrS, mutations in gyrA and parC genes | Arpin, 2003 Blazquez, 1993 Bohnert, 2006 Bou, 2002 Bradford, 1996 Kim, 2020 Onanuga, 2019 Rodrigez-Bano, 2004 Teshager, 2000 Yasufuku, 2011 |
Klebsiella Pneumoniae | CTX-M-15 SHV-2 SHV-2a SHV-5 TEM-15 TEM-19 TEM-21 TEM-24 TEM-48 | DHA-1 FOX CMY-2 | KPC VIM IMP OXA-48 | 16S rRNA methylases: rmtA, rmtB, armA aadB aadA2 | qnrA, qnrB, qnrS, mutations in gyrA and parC genes | Arpin, 2003 Bedenić, 1998 Bedenić, 2001 Bedenić, 2010 Damjanova, 2007 Damjanova, 2008 Gniadkowski, 1998 Gruteke, 2003 M’Zali, 1995 Podbielski, 1991 Thomson, 1991 Vedet, 2006 Zujić-Atalić, 2014 |
Enterobacter spp. | CTX-M-15 CTX-M-10 VEB-1 | Derepressed AmpC | VIM-1 | Apfalter, 2002 Franolić-Kukina, 2016 Girlich, 2001 | ||
Proteus spp. | TEM-52 | CMY-16 | Bedenić, 2016 | |||
Sardelić, 2010 | ||||||
Klebsiella Aerogenes | TEM-3 TEM-24 | Arpin, 2003 | ||||
Citrobacter spp. | CTX-M-2 CTX-M-14 CTX-M-15 SHV-12 | qnrB4 qnrS AAc6-Ib-cr | Kanamori, 2011 | |||
Acinetobacter Baumannii | OXA-23 OXA-24 OXA-58 | 16S rRNA methylases: armA, rmtB | mutations in gyrA and parC genes | Franolić-Kukina, 2011 Garneau-Tsodikova, 2016 Ladavac, 2015 Pournaras, 2006 Vranić-Ladavac, 2014 | ||
Pseudomonas Aeruginosa | OXA-10 OXA-17 SHV -5 | VIM-2 | 16S rRN Amethylases: armA, rmtA, rmtB, rmtD1, rmtG aacC6 | mutations in gyrA and parC genes | Bošnjak, 2010 Bubonja-Šonje, 2015 Garneau-Tsodikova, 2016 Poirel, 2004 Sardelić, 2012 Sorour, 2008 |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2021 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
Bedenić, B.; Meštrović, T. Mechanisms of Resistance in Gram-Negative Urinary Pathogens: From Country-Specific Molecular Insights to Global Clinical Relevance. Diagnostics 2021, 11, 800. https://doi.org/10.3390/diagnostics11050800
Bedenić B, Meštrović T. Mechanisms of Resistance in Gram-Negative Urinary Pathogens: From Country-Specific Molecular Insights to Global Clinical Relevance. Diagnostics. 2021; 11(5):800. https://doi.org/10.3390/diagnostics11050800
Chicago/Turabian StyleBedenić, Branka, and Tomislav Meštrović. 2021. "Mechanisms of Resistance in Gram-Negative Urinary Pathogens: From Country-Specific Molecular Insights to Global Clinical Relevance" Diagnostics 11, no. 5: 800. https://doi.org/10.3390/diagnostics11050800