Extended-Spectrum Beta-Lactamase- and Plasmidic AmpC-Producing Enterobacterales among the Faecal Samples in the Bulgarian Community
Abstract
:1. Introduction
2. Materials and Methods
2.1. Bacterial Isolates
2.2. Phenotypic Methods for ESBL/Carbapenemase Detection: Antimicrobial Susceptibility Testing
2.3. Molecular–Genetic Methods for Beta-Lactamase Identification
2.4. Molecular Typing
2.5. Statistical Analysis
3. Results
3.1. Bacterial Isolates
3.2. Phenotypic Methods for ESBL/Carbapenemase Detection: Antimicrobial Susceptibility Testing
3.3. Molecular–Genetic Methods for Beta-Lactamase Identification
3.4. Molecular Typing
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Mojica, M.F.; De La Cadena, E.; Hernández-Gómez, C.; Correa, A.; Appel, T.M.; Pallares, C.J.; Villegas, M.V. Performance of disk diffusion and broth microdilution for fosfomycin susceptibility testing of multi-drug resistant clinical isolates of Enterobacterales and Pseudomonas aeruginosa. J. Glob. Antimicrob. Resist. 2020, 21, 391–395. [Google Scholar] [CrossRef] [PubMed]
- Jacoby, G.A. AmpC β-lactamases. Clin. Microbiol. Rev. 2009, 22, 161–182. [Google Scholar] [CrossRef]
- Rossolini, G.M.; D’Andrea, M.M.; Mugnaioli, C. The spread of CTX-M-type extended-spectrum beta-lactamases. Clin. Microbiol. Infect. 2008, 14 (Suppl. S5), 21–24. [Google Scholar] [CrossRef]
- Shurina, B.A.; Page, R.C. Structural Comparisons of Cefotaximase (CTX-M-ase) Sub Family 1. Front. Microbiol. 2021, 12, 688509. [Google Scholar] [CrossRef]
- 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]
- Ma, J.; Song, X.; Li, M.; Yu, Z.; Cheng, W.; Yu, Z.; Zhang, W.; Zhang, Y.; Shen, A.; Sun, H.; et al. Global spread of carbapenem-resistant Enterobacteriaceae: Epidemiological features, resistance mechanisms, detection and therapy. Microbiol. Res. 2023, 266, 127249. [Google Scholar] [CrossRef] [PubMed]
- Willems, R.P.J.; van Dijk, K.; Dierikx, C.M.; Twisk, J.W.R.; van der Klis, F.R.M.; de Greeff, S.C.; Vandenbroucke-Grauls, C.M.J.E. Gastric acid suppression, lifestyle factors and intestinal carriage of ESBL and carbapenemase-producing Enterobacterales: A nationwide population-based study. J. Antimicrob. Chemother. 2021, 77, 237–245. [Google Scholar] [CrossRef]
- Bezabih, Y.M.; Sabiiti, W.; Alamneh, E.; Bezabih, A.; Peterson, G.M.; Bezabhe, W.M.; Roujeinikova, A. The global prevalence and trend of human intestinal carriage of ESBL-producing Escherichia coli in the community. J. Antimicrob. Chemother. 2021, 76, 22–29. [Google Scholar] [CrossRef] [PubMed]
- Dwiyanto, J.; Hor, J.W.; Reidpath, D.; Su, T.T.; Lee, S.W.H.; Ayub, Q.; Mustapha, F.B.; Lee, S.M.; Foo, S.C.; Chong, C.W.; et al. Pan-genome and resistome analysis of extended-spectrum ß-lactamase-producing Escherichia coli: A multi-setting epidemiological surveillance study from Malaysia. PLoS ONE 2022, 17, e0265142. [Google Scholar] [CrossRef]
- Markovska, R.; Stankova, P.; Stoeva, T.; Ivanova, D.; Pencheva, D.; Kaneva, R.; Boyanova, L. Fecal Carriage and Epidemiology of Extended-Spectrum Beta-Lactamase/Carbapenemases Producing Enterobacterales Isolates in Bulgarian Hospitals. Antibiotics 2021, 10, 747. [Google Scholar] [CrossRef]
- Markovska, R.; Stankova, P.; Stoeva, T.; Murdjeva, M.; Marteva-Proevska, Y.; Ivanova, D.; Sredkova, M.; Petrova, A.; Mihova, K.; Boyanova, L. Dissemination of High-Risk Clones Enterobacterales among Bulgarian Fecal Carriage Isolates. Microorganisms 2022, 10, 2144. [Google Scholar] [CrossRef]
- Wieser, A.; Schneider, L.; Jung, J.; Schubert, S. MALDI-TOF MS in microbiological diagnostics-identification of microrganisms and beyond. Appl. Microbiol. Biotechnol. 2012, 93, 965–974. [Google Scholar] [CrossRef]
- EUCAST Resistance Mechanisms. Available online: https://www.eucast.org/resistance_mechanisms/ (accessed on 25 May 2024).
- European Committee on Antimicrobial Susceptibility Testing EUCAST. 2020. Available online: https://www.eucast.org/ast_of_bacteria (accessed on 16 August 2024).
- European Committee on Antimicrobial Susceptibility Testing EUCAST 2020. Available online: https://www.eucast.org/fileadmin/src/media/PDFs/EUCAST_files/Breakpoint_tables/v_10.0_Breakpoint_Tables.pdf (accessed on 15 June 2024).
- Markovska, R.; Schneider, I.; Keuleyan, E.; Sredkova, M.; Ivanova, D.; Markova, B.; Lazarova, G.; Dragijeva, E.; Savov, E.; Haydouchka, I.; et al. Extended-spectrum beta-lactamase-producing Enterobacteriaceae in Bulgarian hospitals. Microb. Drug Resist. 2008, 14, 119–128. [Google Scholar] [CrossRef]
- Pérez-Pérez, F.J.; Hanson, N.D. Detection of plasmid-mediated AmpC beta-lactamase genes in clinical isolates by using multiplex PCR. J. Clin. Microbiol. 2002, 40, 2153–2162. [Google Scholar] [CrossRef]
- Dimitrova, D.; Markovska, R.; Stoeva, T.; Stankova, P.; Boyanova, L.; Mihova, K.; Kaneva, R.; Mitov, I. First report of DHA-1 producing Enterobacter cloacae isolate in Bulgaria. Folia Medica 2019, 61, 458–461. [Google Scholar] [CrossRef]
- Versalovic, J.; Koeuth, T.; Lupski, J. Distribution of repetitive DNA sequences in eubacteria and application to fingerprinting of bacterial genomes. Nucleic Acids Res. 1991, 19, 6823–6831. [Google Scholar] [CrossRef]
- PubMLST. Available online: https://pubmlst.org/bigsdb?db=pubmlst_escherichia_seqdef (accessed on 17 August 2024).
- Wirth, T.; Falush, D.; Lan, R.; Colles, F.; Mensa, P.; Wieler, L.H.; Karch, H.; Reeves, P.R.; Maiden, M.C.; Ochman, H.; et al. Sex and virulence in Escherichia coli: An evolutionary perspective. Mol. Microbiol. 2006, 60, 1136–1151. [Google Scholar] [CrossRef]
- Institute Pasteur. Klebsiella Pneumoniae. Available online: https://bigsdb.pasteur.fr/klebsiella/ (accessed on 16 August 2024).
- Diancourt, L.; Passet, V.; Verhoef, J.; Grimont, P.A.; Brisse, S. Multilocus sequence typing of Klebsiella pneumoniae nosocomial isolates. J. Clin. Microbiol. 2005, 43, 4178–4182. [Google Scholar] [CrossRef] [PubMed]
- PhYLOViZ Online. Available online: http://www.phyloviz.net/ (accessed on 16 August 2024).
- Clermont, O.; Dhanji, H.; Upton, M.; Gibreel, T.; Fox, A.; Boyd, D.; Mulvey, M.R.; Nordmann, P.; Ruppé, E.; Sarthou, J.L.; et al. Rapid detection of the O25b-ST131 clone of Escherichia coli encompassing the CTX-M-15-producing strains. J. Antimicrob. Chemother. 2009, 64, 274–277. [Google Scholar] [CrossRef]
- Clermont, O.; Bonacorsi, S.; Bingen, E. Rapid and simple detection of the Escherichia coli phylogenetic group. Appl. Environ. Microbiol. 2000, 66, 4555–4558. [Google Scholar] [CrossRef]
- GraphPad. Available online: https://www.graphpad.com/quickcalcs/contingency1/ (accessed on 18 August 2024).
- Mirelis, B.; Navarro, F.; Miró, E.; Mesa, R.J.; Coll, P.; Prats, G. Community transmission of extended-spectrum beta-lactamase. Emerg. Infect. Dis. 2003, 9, 1024–1025. [Google Scholar] [CrossRef]
- Ebrahimi, F.; Mózes, J.; Mészáros, J.; Juhász, Á.; Majoros, L.; Szarka, K.; Kardos, G. Asymptomatic faecal carriage of ESBL producing Enterobacteriaceae in Hungarian healthy individuals and in long-term care applicants: A shift towards CTX-M producers in the community. Infect. Dis. 2016, 48, 557–559. [Google Scholar] [CrossRef]
- Wickramasinghe, N.H.; Xu, L.; Eustace, A.; Shabir, S.; Saluja, T.; Hawkey, P.M. High community faecal carriage rates of CTX-M ESBL-producing Escherichia coli in a specific population group in Birmingham, UK. J. Antimicrob. Chemother. 2012, 67, 1108–1113. [Google Scholar] [CrossRef]
- Geser, N.; Stephan, R.; Korczak, B.M.; Beutin, L.; Hächler, H. Molecular identification of extended-spectrum-β-lactamase genes from Enterobacteriaceae isolated from healthy human carriers in Switzerland. Antimicrob. Agents Chemother. 2012, 56, 1609–1612. [Google Scholar] [CrossRef] [PubMed]
- Nicolas-Chanoine, M.H.; Gruson, C.; Bialek-Davenet, S.; Bertrand, X.; Thomas-Jean, F.; Bert, F.; Moyat, M.; Meiller, E.; Marcon, E.; Danchin, N.; et al. 10-Fold increase (2006–11) in the rate of healthy subjects with extended-spectrum β-lactamase-producing Escherichia coli faecal carriage in a Parisian check-up centre. J. Antimicrob. Chemother. 2013, 68, 562–568. [Google Scholar] [CrossRef] [PubMed]
- Sasaki, T.; Hirai, I.; Niki, M.; Nakamura, T.; Komalamisra, C.; Maipanich, W.; Kusolsuk, T.; Sa-Nguankiat, S.; Pubampen, S.; Yamamoto, Y. High prevalence of CTX-M beta-lactamase-producing Enterobacteriaceae in stool specimens obtained from healthy individuals in Thailand. J. Antimicrob. Chemother. 2010, 65, 666–668. [Google Scholar] [CrossRef] [PubMed]
- Luvsansharav, U.O.; Hirai, I.; Nakata, A.; Imura, K.; Yamauchi, K.; Niki, M.; Komalamisra, C.; Kusolsuk, T.; Yamamoto, Y. Prevalence of and risk factors associated with faecal carriage of CTX-M β-lactamase-producing Enterobacteriaceae in rural Thai communities. J. Antimicrob. Chemother. 2012, 67, 1769–1774. [Google Scholar] [CrossRef]
- Luvsansharav, U.O.; Hirai, I.; Niki, M.; Nakata, A.; Yoshinaga, A.; Moriyama, T.; Yamamoto, Y. Prevalence of fecal carriage of extended-spectrum β-lactamase-producing Enterobacteriaceae among healthy adult people in Japan. J. Infect. Chemother. 2011, 17, 722–725. [Google Scholar] [CrossRef]
- Li, B.; Sun, J.-Y.; Liu, Q.-Z.; Han, L.-Z.; Huang, X.-H.; Ni, Y.-X. High prevalence of CTXM β-lactamases in faecal Escherichia coli strains from healthy humans in Fuzhou, China. Scand. J. Infect. Dis. 2011, 43, 170–174. [Google Scholar] [CrossRef]
- Tian, S.F.; Chen, B.Y.; Chu, Y.Z.; Wang, S. Prevalence of rectal carriage of extended-spectrum beta-lactamase-producing Escherichia coli among elderly people in community settings in China. Can. J. Microbiol. 2008, 54, 781–785. [Google Scholar] [CrossRef]
- European Centre for Disease Prevention and Control (ECDC). Antimicrobial Consumption in the EU/EEA. Annual Epidemiologic Report for 2019. Available online: https://www.ecdc.europa.eu/sites/default/files/documents/Antimicrobial-consumption-in-the-EU-Annual-Epidemiological-Report-2019.pdf (accessed on 15 June 2024).
- European Centre for Disease Prevention and Control (ECDC). Antimicrobial Consumption in the EU/EEA. Annual Epidemiologic Report for 2022. Available online: https://www.ecdc.europa.eu/sites/default/files/documents/AER-antimicrobial-consumption.pdf (accessed on 15 June 2024).
- Karanika, S.; Karantanos, T.; Arvanitis, M.; Grigoras, C.; Mylonakis, E. Fecal Colonization With Extended-spectrum Beta-lactamase-Producing Enterobacteriaceae and Risk Factors Among Healthy Individuals: A Systematic Review and Metaanalysis. Clin. Infect. Dis. 2016, 63, 851. [Google Scholar] [CrossRef]
- Jørgensen, S.B.; Søraas, A.; Sundsfjord, A.; Liestøl, K.; Leegaard, T.M.; Jenum, P.A. Fecal carriage of extended spectrum β-lactamase producing Escherichia coli and Klebsiella pneumoniae after urinary tract infection-A three year prospective cohort study. PLoS ONE 2017, 12, e0173510. [Google Scholar] [CrossRef] [PubMed]
- Farrell, M.L.; Chueiri, A.; Maguire, M.; Kovářová, A.; Miliotis, G.; O’Connor, L.; McDonagh, F.; Duane, S.; Cormican, M.; Devane, G.; et al. Longitudinal carriage of antimicrobial resistant Enterobacterales in healthy individuals in Ireland-Assessing the impact of recreational water use on duration of carriage. Sci. Total Environ. 2023, 905, 167100. [Google Scholar] [CrossRef]
- Rodrigues, C.; Machado, E.; Fernandes, S.; Peixe, L.; Novais, Â. An update on faecal carriage of ESBL-producing Enterobacteriaceae by Portuguese healthy humans: Detection of the H30 subclone of B2-ST131 Escherichia coli producing CTX-M-27. J. Antimicrob. Chemother. 2016, 71, 1120–1122. [Google Scholar] [CrossRef]
- Aires-de-Sousa, M.; Lopes, E.; Gonçalves, M.L.; Pereira, A.L.; Machado, E.; Costa, A.; de Lencastre, H.; Poirel, L. Intestinal carriage of extended-spectrum beta-lactamase-producing Enterobacteriaceae at admission in a Portuguese hospital. Eur. J. Clin. Microbiol. Infect. Dis. 2020, 39, 783–790. [Google Scholar] [CrossRef] [PubMed]
- Otter, J.A.; Natale, A.; Batra, R.; Tosas Auguet, O.; Dyakova, E.; Goldenberg, S.D.; Edgeworth, J.D. Individual- and community-level risk factors for ESBL Enterobacteriaceae colonization identified by universal admission screening in London. Clin. Microbiol. Infect. 2019, 25, 1259–1265. [Google Scholar] [CrossRef]
- Sharma, B.; Yadav, S.; Khanal, A.; Shakya, B.; Shrestha, K.; Aryal, S.; Kattel, H.; Parajuli, K.; Mishra, S.K. Fecal Carriage of Extended-Spectrum beta-Lactamase Producing Escherichia coli among Health Science Students. J. Nepal. Health Res. Counc. 2022, 20, 160–165. [Google Scholar]
- Pérez-López, A.; Sundararaju, S.; Tsui, K.M.; Al-Mana, H.; Hasan, M.R.; Suleiman, M.; Al Maslamani, E.; Imam, O.; Roscoe, D.; Tang, P. Fecal Carriage and Molecular Characterization of Carbapenemase-Producing Enterobacterales in the Pediatric Population in Qatar. Microbiol. Spectr. 2021, 9, e0112221. [Google Scholar] [CrossRef] [PubMed]
- Obeng-Nkrumah, N.; Hansen, D.S.; Awuah-Mensah, G.; Blankson, N.K.; Frimodt-Møller, N.; Newman, M.J.; Opintan, J.A.; Krogfelt, K.A. High level of colonization with third-generation cephalosporin-resistant Enterobacterales in African community settings, Ghana. Diagn. Microbiol. Infect. Dis. 2023, 106, 115918. [Google Scholar] [CrossRef]
- Moghnia, O.H.; Rotimi, V.O.; Al-Sweih, N.A. Monitoring antibiotic resistance profiles of faecal isolates of Enterobacteriaceae and the prevalence of carbapenem-resistant isolates among food handlers in Kuwait. J. Glob. Antimicrob. Resist. 2021, 25, 370–376. [Google Scholar] [CrossRef]
- de Pinho Rodrigues, K.M.; de Rezende, D.F.; Pinto, M.P.; Dos Santos Tufic-Garutti, S.; Ramalho, J.V.A.; de Araújo Longo, L.G.; de Carvalho Girão, V.B.; de Oliveira, G.C.; Vilar, L.C.; Moreira, B.M. High levels of gut carriage of antimicrobial-resistant Escherichia coli in community settings in Rio de Janeiro, Brazil. Braz. J. Microbiol. 2022, 53, 205–212. [Google Scholar] [CrossRef] [PubMed]
- Woerther, P.L.; Burdet, C.; Chachaty, E.; Andremont, A. Trends in human fecal carriage of extended-spectrum β-lactamases in the community: Toward the globalization of CTX-M. Clin. Microbiol. Rev. 2013, 26, 744–758. [Google Scholar] [CrossRef] [PubMed]
- Hu, Y.; Rubin, J.; Mussio, K.; Riley, L.W. Risk factors for faecal carriage of multidrug-resistant Escherichia coli in a college community: A penalised regression model. J. Glob. Antimicrob. Resist. 2021, 26, 166–173. [Google Scholar] [CrossRef] [PubMed]
- D’Andrea, M.M.; Arena, F.; Pallecchi, L.; Rossolini, G.M. CTX-M-type β-lactamases: A successful story of antibiotic resistance. Int. J. Med. Microbiol. 2013, 303, 305–317. [Google Scholar] [CrossRef] [PubMed]
- Freeman, J.T.; McBride, S.J.; Heffernan, H.; Bathgate, T.; Pope, C.; Ellis-Pegler, R.B. Community-onset genitourinary tract infection due to CTX-M-15-Producing Escherichia coli among travelers to the Indian subcontinent in New Zealand. Clin. Infect. Dis. 2008, 47, 689–692. [Google Scholar] [CrossRef] [PubMed]
- Xu, Q.; Pan, F.; Sun, Y.; Wang, C.; Shi, Y.; Zhang, T.; Yu, F.; Zhang, H. Fecal Carriage and Molecular Epidemiology of Carbapenem-Resistant Enterobacteriaceae from Inpatient Children in a Pediatric Hospital of Shanghai. Infect. Drug Resist. 2020, 13, 4405–4415. [Google Scholar] [CrossRef]
- Nedelcheva, G. Epidemiological Typing and Mechanisms of Antibiotic Resistance in Clinically Relevant Klebsiella pneumoniae Isolated at St. Marina University Hospital–Varna. Ph.D. Thesis, Medical Academy Repository, Medical University Varna, Varna, Bulgaria, 2019. [Google Scholar]
- Habibzadeh, N.; Doghaheh, H.P.; Far, M.M.; Asl, H.A.; Iranpour, S.; Arzanlou, M. Fecal Carriage of Extended-Spectrum β-Lactamases and pAmpC Producing Enterobacterales in an Iranian Community: Prevalence, Risk Factors, Molecular Epidemiology, and Antibiotic Resistance. Microb. Drug Resist. 2022, 28, 921–934. [Google Scholar] [CrossRef]
- Ruh, E.; Zakka, J.; Hoti, K.; Fekrat, A.; Guler, E.; Gazi, U.; Erdogmus, Z.; Suer, K. Extended-spectrum β-lactamase, plasmid-mediated AmpC β-lactamase, fluoroquinolone resistance, and decreased susceptibility to carbapenems in Enterobacteriaceae: Fecal carriage rates and associated risk factors in the community of Northern Cyprus. Antimicrob. Resist. Infect. Control 2019, 8, 98. [Google Scholar] [CrossRef]
- Zhang, R.; Liu, L.; Zhou, H.; Chan, E.W.; Li, J.; Fang, Y.; Li, Y.; Liao, K.; Chen, S. Nationwide Surveillance of Clinical Carbapenemresistant Enterobacteriaceae (CRE) Strains in China. EBioMedicine 2017, 19, 98–106. [Google Scholar] [CrossRef]
- Ghebremedhin, B.; Ibukun, A.; Odugbemi, T.; König, W. Multidrug-resistant CTX-M-15 carrying K. pneumoniae isolates and their virulence in Nigeria. Int. J. Infect. Dis. 2014, 21, 95. [Google Scholar] [CrossRef]
- Giske, C.G.; Fröding, I.; Hasan, C.M.; Turlej-Rogacka, A.; Toleman, M.; Livermore, D.; Woodford, N.; Walsh, T.R. Diverse sequence types of Klebsiella pneumoniae contribute to the dissemination of blaNDM-1 in India, Sweden, and the United Kingdom. Antimicrob. Agents Chemother. 2012, 56, 2735–2738. [Google Scholar] [CrossRef] [PubMed]
- Jain, A.; Hopkins, K.L.; Turton, J.; Doumith, M.; Hill, R.; Loy, R.; Meunier, D.; Pike, R.; Livermore, D.M.; Woodford, N. NDM carbapenemases in the United Kingdom: An analysis of the first 250 cases. J. Antimicrob. Chemother. 2014, 69, 1777–1784. [Google Scholar] [CrossRef]
- Yoon, E.J.; Yang, J.W.; Kim, J.O.; Lee, H.; Lee, K.J.; Jeong, S.H. Carbapenemase-producing Enterobacteriaceae in South Korea: A report from the national laboratory surveillance system. Future Microbiol. 2018, 13, 771–783. [Google Scholar] [CrossRef] [PubMed]
- Wu, W.; Feng, Y.; Tang, G.; Qiao, F.; McNally, A.; Zong, Z. NDM Metallo-β-Lactamases and Their Bacterial Producers in Health Care Settings. Clin. Microbiol. Rev. 2019, 32, e00115-18. [Google Scholar] [CrossRef]
- Can, F.; Azap, O.K.; Seref, C.; Ispir, P.; Arslan, H.; Ergonul, O. Emerging Escherichia coli O25b/ST131 clone predicts treatment failure in urinary tract infections. Clin. Infect. Dis. 2015, 60, 523–527. [Google Scholar] [CrossRef] [PubMed]
- Nicolas-Chanoine, M.H.; Petitjean, M.; Mora, A.; Mayer, N.; Lavigne, J.P.; Boulet, O.; Leflon-Guibout, V.; Blanco, J.; Hocquet, D. The ST131 Escherichia coli H22 subclone from human intestinal microbiota: Comparison of genomic and phenotypic traits with those of the globally successful H30 subclone. BMC Microbiol. 2017, 17, 71. [Google Scholar] [CrossRef] [PubMed]
- Park, D.E.; Aziz, M.; Koch, B.J.; Roach, K.; Clabots, C.; Johnson, J.R.; Price, L.B.; Liu, C.M. Gut microbiome predictors of Escherichia coli sequence type 131 colonization and loss. EBioMedicine 2024, 99, 104909. [Google Scholar] [CrossRef]
- Tóth, K.; Damjanova, I.; Laczkó, L.; Buzgó, L.; Lesinszki, V.; Ungvári, E.; Jánvári, L.; Hanczvikkel, A.; Tóth, Á.; Szabó, D. Genomic Epidemiology of C2/H30Rx and C1-M27 Subclades of Escherichia coli ST131 Isolates from Clinical Blood Samples in Hungary. Antibiotics 2024, 13, 363. [Google Scholar] [CrossRef]
- Flament-Simon, S.C.; Nicolas-Chanoine, M.H.; García, V.; Duprilot, M.; Mayer, N.; Alonso, M.P.; García-Meniño, I.; Blanco, J.E.; Blanco, M.; Blanco, J. Clonal Structure, Virulence Factor-encoding Genes and Antibiotic Resistance of Escherichia coli, Causing Urinary Tract Infections and Other Extraintestinal Infections in Humans in Spain and France during 2016. Antibiotics 2020, 9, 161. [Google Scholar] [CrossRef]
- Cheng, M.F.; Ho, P.Y.; Wang, J.L.; Tseng, F.C.; Chang, J.T.; Huang, I.F.; Hung, C.H. Prevalence and household risk factors for fecal carriage of ESBL-producing, sequence type 131, and extraintestinal pathogenic Escherichia coli among children in southern Taiwan. J. Microbiol. Immunol. Infect. 2022, 55, 695–707. [Google Scholar] [CrossRef]
- Matsumura, Y.; Pitout, J.D.; Gomi, R.; Matsuda, T.; Noguchi, T.; Yamamoto, M.; Peirano, G.; DeVinney, R.; Bradford, P.A.; Motyl, M.R.; et al. Global Escherichia coli Sequence Type 131 Clade with blaCTX-M-27 Gene. Emerg. Infect. Dis. 2016, 22, 1900–1907. [Google Scholar] [CrossRef] [PubMed]
- Matsumura, Y.; Pitout, J.D.D.; Peirano, G.; DeVinney, R.; Noguchi, T.; Yamamoto, M.; Gomi, R.; Matsuda, T.; Nakano, S.; Nagao, M.; et al. Rapid Identification of Different Escherichia coli Sequence Type 131 Clades. Antimicrob. Agents Chemother. 2017, 61, e00179-17. [Google Scholar] [CrossRef]
- Bevan, E.R.; Jones, A.M.; Hawkey, P.M. Global epidemiology of CTX-M β-lactamases: Temporal and geographical shifts in genotype. J. Antimicrob. Chemother. 2017, 72, 2145–2155. [Google Scholar] [CrossRef] [PubMed]
- Merino, I.; Hernández-García, M.; Turrientes, M.C.; Pérez-Viso, B.; López-Fresneña, N.; Diaz-Agero, C.; Maechler, F.; Fankhauser-Rodriguez, C.; Kola, A.; Schrenzel, J.; et al. Emergence of ESBL-producing Escherichia coli ST131-C1-M27 clade colonizing patients in Europe. J. Antimicrob. Chemother. 2018, 73, 2973–2980. [Google Scholar] [CrossRef] [PubMed]
- Peirano, G.; Pitout, J. Extended-Spectrum β-Lactamase-Producing Enterobacteriaceae: Update on Molecular Epidemiology and Treatment Options. Drugs 2019, 79, 1529–1541. [Google Scholar] [CrossRef]
- van der Putten, B.C.L.; van Hattem, J.M.; Penders, J.; Consortium, C.; Mende, D.R.; Schultsz, C. Extra-intestinal pathogenic lineages of extended-spectrum β-lactamase (ESBL)-producing Escherichia coli are associated with prolonged ESBL gene carriage. Access Microbiol. 2024, 6, 000541.v4. [Google Scholar] [CrossRef]
- Pietsch, M.; Irrgang, A.; Roschanski, N.; Brenner Michael, G.; Hamprecht, A.; Rieber, H.; Käsbohrer, A.; Schwarz, S.; Rösler, U.; Kreienbrock, L.; et al. Whole genome analyses of CMY-2-producing Escherichia coli isolates from humans, animals and food in Germany. BMC Genom. 2018, 19, 601. [Google Scholar] [CrossRef] [PubMed]
- Zahra, R.; Javeed, S.; Malala, B.; Babenko, D.; Toleman, M.A. Analysis of Escherichia coli STs and resistance mechanisms in sewage from Islamabad, Pakistan indicates a difference in E. coli carriage types between South Asia and Europe. J. Antimicrob. Chemother. 2018, 73, 1781–1785. [Google Scholar] [CrossRef]
- Cunha, M.P.V.; Saidenberg, A.B.; Moreno, A.M.; Ferreira, A.J.P.; Vieira, M.A.M.; Gomes, T.A.T.; Knöbl, T. Pandemic extra-intestinal pathogenic Escherichia coli (ExPEC) clonal group O6-B2-ST73 as a cause of avian colibacillosis in Brazil. PLoS ONE 2017, 12, e0178970. [Google Scholar] [CrossRef]
- Riley, L.W. Pandemic lineages of extraintestinal pathogenic Escherichia coli. Clin. Microbiol. Infect. 2014, 20, 380–390. [Google Scholar] [CrossRef] [PubMed]
- Aung, M.S.; San, N.; Maw, W.W.; San, T.; Urushibara, N.; Kawaguchiya, M.; Sumi, A.; Kobayashi, N. Prevalence of Extended-Spectrum Beta-Lactamase and Carbapenemase Genes in Clinical Isolates of Escherichia coli in Myanmar: Dominance of blaNDM-5 and Emergence of blaOXA-181. Microb. Drug Resist. 2018, 24, 1333–1344. [Google Scholar] [CrossRef] [PubMed]
- Bonnet, M.; Eckert, C.; Tournebize, R. Decolonization of asymptomatic carriage of multi-drug resistant bacteria by bacteriophages? Front. Microbiol. 2023, 14, 1266416. [Google Scholar] [CrossRef] [PubMed]
- Catho, G.; Huttner, B. Strategies for the eradication of extended-spectrum beta-lactamase or carbapenemase-producing Enterobacteriaceae intestinal carriage. Expert Rev. Anti-Infect. Ther. 2019, 17, 557–569. [Google Scholar] [CrossRef] [PubMed]
- Singh, R.; de Groot, P.F.; Geerlings, S.E.; Hodiamont, C.J.; Belzer, C.; Berge, I.J.M.T.; de Vos, W.M.; Bemelman, F.J.; Nieuwdorp, M. Fecal microbiota transplantation against intestinal colonization by extended spectrum beta-lactamase producing Enterobacteriaceae: A proof of principle study. BMC Res. Notes 2018, 11, 190. [Google Scholar] [CrossRef]
Species/Medical Centre (MC) | E. coli | K. pneumoniae | E. cloacae Complex | C. freundii Complex | M. morganii | H. alvei |
---|---|---|---|---|---|---|
MC—Pleven | 14 | 2 | 4 | 1 | 0 | 0 |
MC—Burgas | 31 | 2 | 1 | 2 | 0 | 0 |
MC 1—Sofia | 39 | 5 | 1 | 2 | 2 | 0 |
MC 2—Sofia | 5 | 0 | 0 | 0 | 0 | 1 |
MC 3—Sofia | 20 | 2 | 2 | 1 | 0 | 3 |
Total numbers (percent) | 109 (77.9%) | 11 (7.9%) | 8 (5.7%) | 6 (4.3%) | 2 (1.4%) | 4 (2.9%) |
Bacterial Species Detected Genes | E. coli n = 109 (%) | K. pneumoniae n = 11 (%) | E. cloacae Complex n = 8 (%) | C. freundii Complex n = 6 (%) | M. morganii n = 2 (%) | H. alvei n = 4 (%) | Total Number n = 140 (%) |
---|---|---|---|---|---|---|---|
blaCTX-M-15 | 47 (43.1%) | 3 (27.2%) | - | 2 (33%) | - | - | 52 (37.1%) |
blaCTX-M-1 | 3 (2.8%) | - | - | - | - | - | 3 (2.1%) |
blaCTX-M-3 | 20 (18.3%) | 7 (63.6%) | - | - | - | - | 27 (19.3%) |
blaCTX-M-9 | 1 (0.9%) | - | - | - | - | - | 1 (0.2%) |
blaCTX-M-14 | 13 (11.9%) | - | 1 (12%) | - | - | - | 14 (10%) |
blaCTX-M-27 | 6 (5.5%) | - | - | - | - | - | 6 (4.3%) |
blaSHV-12 | 2 (1.8%) | - | - | - | - | - | 2 (1.4%) |
blaDHA-1 | 15 (13.8%) | 1 (9.0%) | - | - | - | - | 16 (11.4%) |
blaCMY-2 | 2 (1.8%) | - | - | - | - | - | 2 (1.4%) |
AmpC producer | - | - | 7 (88%) | 4 (67%) | 2 (100%) | 4 (100%) | 17 (12.1%) |
Genes Encoded ESBls/Plasmidic AmpC | MLST Type Number | ERIC Type | Total Number |
---|---|---|---|
blaCTX-M-3 | ST3532; ST24491; ND4 | bn = 2; unique n = 5 | 7 |
blaCTX-M-15 | ST341; ST141 | unique n = 2 | 2 |
blaDHA-1 | ST111 | unique n = 1 | 1 |
Genes Encoded ESBls/Plasmidic AmpC | MLST Type Number/CC | Total Number |
---|---|---|
blaCTX-M-15 | ST13111; CC10(ST49815; ST102); ST3944; ST27972; ST733; ST10572; ST92981; ST11961; ST4051; ND15 | 47 |
blaCTX-M-3 | ST1313; CC10(ST49812; ST42383; ST102; ST341); ST1551; ST2951; ST19931; ND6 | 20 |
blaCTX-M-1 | ST27971; CC155(ST561); ND1 | 3 |
blaCTX-M-14 | ST1311; CC10(ST386); CC155(ST561); ST21781; ST26171; ND3 | 13 |
blaCTX-M-9 | CC10(ST49811) | 1 |
blaCTX-M-27 | ST1312; ST382; ND2 | 6 |
blaSHV-12 | ST85781; ST931; | 2 |
blaDHA-1 | ST42381; ST383; ST693; ST76702; ST6481; | 15 |
blaCMY-2 | ST1311; ST92981; | 2 |
ERIC Type | MLST Type | CC | Phylogroup | ESBL/AmpC Plasmid Genes | Total Number |
---|---|---|---|---|---|
A | 131 | 131 | B2 | blaCTX-M-15 (11), blaCTX-M-3 (3), blaCTX-M-27 (2), blaCTX-M-14 (1), blaCMY-2 (1) | 18 |
X | 4981 | 10 | A | blaCTX-M-15 (5), blaCTX-M-3 (2), blaCTX-M-9 (1) | 8 |
Y | 4238 | 10 | A | blaCTX-M-3 (3), blaDHA-1 (1) | 4 |
J | 10 | 10 | A | blaCTX-M-15 (2), blaCTX-M-3 (2) | 4 |
V | 34 | 10 | A | blaCTX-M-3 (1) | 1 |
S | 38 | 38 | D | blaCTX-M-14 (6), blaCTX-M-27 (2), blaDHA-1 (3) | 11 |
M | 394 | 394 | D | blaCTX-M-15 (4) | 4 |
K | 69 | 69 | D | blaDHA-1 (3) | 3 |
E | 2797 | - | D | blaCTX-M-15 (2), blaCTX-M-1 (1) | 3 |
I | 73 | 73 | B2 | blaCTX-M-15 (3) | 3 |
P | 1057 | 14 | B2 | blaCTX-M-15 (2) | 2 |
O | 7670 | - | D | blaDHA-1 (2) | 2 |
D | 9298 | - | B2 | blaCTX-M-15 (1), blaCMY-2 (1) | 2 |
F1 | 56 | 155 | B1 | blaCTX-M-14 (1), blaCTX-M-1 (1), | 2 |
Unique | 155 | 155 | B1 | blaCTX-M-3 (1) | 10 |
2178 | - | B1 | blaCTX-M-14 (1) | ||
2617 | 59 | B1 | blaCTX-M-14 (1) | ||
295 | 23 | B1 | blaCTX-M-3 (1) | ||
648 | 648 | B1 | blaDHA-1 (1) | ||
8578 | 12 | B2 | blaSHV-12 (1) | ||
93 | 168 | A | blaSHV-12 (1) | ||
1196 | - | B1 | blaCTX-M-15 (1) | ||
405 | 405 | D | blaCTX-M-15 (1) | ||
1993 | - | B2 | blaCTX-M-3 (1) | ||
Unique | ND | - | A(14), B1(3) B2(1), D(14) | blaCTX-M-15 (15), blaCTX-M-3 (6), blaDHA-1(5), blaCTX-M-14 (3), blaCTX-M-27 (2), blaCTX-M-1 (1) | 32 |
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Stankova, P.; Boyanova, L.; Atanasova, D.; Mihaylova, S.; Sredkova, M.; Gergova, R.; Mihova, K.; Markovska, R. Extended-Spectrum Beta-Lactamase- and Plasmidic AmpC-Producing Enterobacterales among the Faecal Samples in the Bulgarian Community. Microorganisms 2024, 12, 1777. https://doi.org/10.3390/microorganisms12091777
Stankova P, Boyanova L, Atanasova D, Mihaylova S, Sredkova M, Gergova R, Mihova K, Markovska R. Extended-Spectrum Beta-Lactamase- and Plasmidic AmpC-Producing Enterobacterales among the Faecal Samples in the Bulgarian Community. Microorganisms. 2024; 12(9):1777. https://doi.org/10.3390/microorganisms12091777
Chicago/Turabian StyleStankova, Petya, Lyudmila Boyanova, Daniela Atanasova, Sashka Mihaylova, Mariya Sredkova, Raina Gergova, Kalina Mihova, and Rumyana Markovska. 2024. "Extended-Spectrum Beta-Lactamase- and Plasmidic AmpC-Producing Enterobacterales among the Faecal Samples in the Bulgarian Community" Microorganisms 12, no. 9: 1777. https://doi.org/10.3390/microorganisms12091777