Virulence and Antibiotic Resistance Genes in Enterococcus from Wastewater for Reuse and Their Health Impact
Abstract
:1. Introduction
2. Materials and Methods
2.1. Collecting and Processing of Samples
2.2. Detection of Van A, B, C1, and C2/3 Genes Specific to Each Species
2.3. Detection of Other Resistance Genes Tet, gyrA, parC, and emeA Genes
2.4. Detection of Virulence Genes
2.5. Validation of Virulence Gene by Sequencing Gelatinase Gene, gelE Amplicon
2.6. Statistical Examination
3. Results
3.1. Antibiotic Resistance Across the Sampling Points and Species
3.2. Vancomycin Resistance Genes Based on Species Diversity
3.3. Detection of Other Resistance Genes
3.4. Detection of gelE and Gelatinase Activity
3.5. Detection of cylA and Haemolytic Activity
3.6. Detection of Ace, efaA, asa1, hyl, Esp Genes and Biofilm Formation
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Tendulkar, S.R.; Baghdayan, A.S.; Shankar, N. Putative surface proteins encoded within a novel transferable locus confer a high-biofilm phenotype to Enterococcus faecalis. J. Bacteriol. 2006, 185, 2063–2072. [Google Scholar] [CrossRef] [PubMed]
- Adegoke, A.A.; Stenstrom, T.A. Septic Systems. In Global Water Pathogen Project; Rose, J.B., Jiménez-Cisneros, B., Mihelcic, J.R., Verbyla, M.E., Eds.; Michigan State University: East Lansing, MI, USA; UNESCO: London, UK, 2019. [Google Scholar] [CrossRef]
- Giridhara Upadhyaya, P.M.; Ravikumar, K.L.; Umapathy, B.L. Review of virulence factors of Enterococcus: An emerging nosocomial pathogen. Indian J. Med. Microbiol. 2009, 27, 301–305. [Google Scholar] [CrossRef] [PubMed]
- Al-Ahdal, M.N.; Abozaid, S.M.; Al-Shammary, H.F.; Bohol, M.F.; Al-Thawadi, S.I.; Al-Jaberi, A.A.; Senok, A.C.; Shibl, A.M.; Al-Qahtani, A.A. Characterization of Enterococcus faecium isolates and first report of vanB phenotype–vanA genotype incongruence in the Middle East. Eur. J. Clin. Microbiol. Infect. Dis. 2012, 31, 3223–3229. [Google Scholar] [CrossRef]
- Comerlato, C.B.; de Resende, M.C.C.; Caierão, J.; Alves d’Azevedo, P. Presence of virulence factors in Enterococcus faecalis and Enterococcus faecium susceptible and resistant to vancomycin. Mem. Inst. Oswaldo Cruz 2013, 108, 590–595. [Google Scholar] [CrossRef] [PubMed]
- Billington, E.O.; Phang, S.H.; Gregson, D.B.; Pitout, J.D.D.; Ross, T.; Church, D.L.; Laupland, K.B.; Parkins, M.D. Incidence, risk factors, and outcomes for Enterococcus spp. bloodstream infections: A population-based study. Int. J. Infect. Dis. 2014, 26, 76–82. [Google Scholar] [CrossRef]
- Fisher, K.; Phillips, C. The ecology, epidemiology, and virulence of Enterococcus. Microbiology 2009, 155, 1749–1757. [Google Scholar] [CrossRef]
- Diazgranados, C.A.; Zimmer, S.M.; Klein, M.; Jernigan, J.A. Comparison of mortality associated with vancomycin-resistant and vancomycin-susceptible enterococcal bloodstream infections: A meta-analysis. Clin. Infect. Dis. 2005, 41, 327–333. [Google Scholar] [CrossRef] [PubMed]
- Iweriebor, B.C.; Obi, L.C.; Okoh, A.I. Virulence and antimicrobial resistance factors of Enterococcus spp. isolated from faecal samples from piggery farms in Eastern Cape, South Africa. BMC Microbiol. 2015, 15, 136. [Google Scholar] [CrossRef] [PubMed]
- Adegoke, A.A.; Madu, C.E.; Reddy, P.; Stenström, T.A.; Okoh, A.I. Prevalence of vancomycin-resistant Enterococcus in wastewater treatment plants and their recipients for reuse using PCR and MALDI-ToF MS. Front. Environ. Sci. 2022, 9, 797992. [Google Scholar] [CrossRef]
- Molale, L.G.; Bezuidenhout, C.C. Antibiotic resistance, efflux pump genes and virulence determinants in Enterococcus spp. from surface water systems. Environ. Sci. Pollut. Res. Int. 2016, 23, 21501–21510. [Google Scholar] [CrossRef]
- Klare, I.; Konstabel, C.; Badstübner, D.; Werner, G.; Witte, W. Occurrence and spread of antibiotic resistances in Enterococcus faecium. Int. J. Food Microbiol. 2003, 88, 269–290. [Google Scholar] [CrossRef]
- Miller, W.R.; Munita, J.M.; Arias, C.A. Mechanisms of antibiotic resistance in enterococci. Expert Rev. Anti-Infect. Ther. 2014, 12, 1221–1236. [Google Scholar] [CrossRef] [PubMed]
- Jia, W.; Li, G.; Wang, W. Prevalence and antimicrobial resistance of Enterococcus species: A hospital-based study in China. Int. J. Environ. Res. Public Health 2014, 11, 3424–3442. [Google Scholar] [CrossRef] [PubMed]
- Davis, D.R.; McAlpine, J.B.; Pazole, C.J.; Talbot, M.K.; Alder, E.A.; White, C.; Jonas, B.M.; Murray, B.E.; Weinstock, G.M.; Rogers, B. Enterococcus faecalis multi-drug resistance transporters: Applications for antibiotic discovery. J. Microbiol. Biotechnol. 2001, 3, 179–184. [Google Scholar]
- Jonas, B.M.; Murray, B.E.; Weinstock, G.M. Characterization of emeA, a NorA homolog and multidrug resistance efflux pump, in Enterococcus faecalis. Antimicrob. Agents Chemother. 2001, 45, 3574–3579. [Google Scholar] [CrossRef]
- Nowroozi, J.; Akhavan Sepahi, A.; Sabokbar, A. Comparison of gyrA and parC mutations in ciprofloxacin-resistant and -susceptible Enterococcus faecalis isolates. J. Med. Microbiol. 2014, 63, 68–74. [Google Scholar]
- Mahapatra, A.; Raj Kumar Patro, A.; Khajuria, A.; Dhal, S.; Praharaj, A.K. Ciprofloxacin-resistant Gram-negative isolates from a tertiary care hospital in Eastern India with novel gyrA and parC gene mutations. Med. J. Armed Forces India 2022, 78, 24–31. [Google Scholar] [CrossRef]
- Luna, V.A.; Roberts, M.C. The presence of the tet(O) gene in both tetracycline-resistant and -susceptible strains of Streptococcus pneumoniae. J. Antimicrob. Chemother. 1998, 42, 613–619. [Google Scholar] [CrossRef]
- Koike, S.; Krapac, I.G.; Oliver, H.D.; Yannarell, A.C.; Chee-Sanford, J.C.; Aminov, R.I.; Mackie, R.I. Monitoring and source tracking of tetracycline resistance genes in lagoons and groundwater adjacent to swine production facilities over a 3-year period. Appl. Environ. Microbiol. 2007, 73, 4813–4823. [Google Scholar] [CrossRef]
- Macauley, J.J.; Qiang, Z.; Adams, C.D.; Surampalli, R.; Mormile, M.R. Disinfection of swine wastewater using chlorine, ultraviolet light and ozone. Water Res. 2007, 41, 855–863. [Google Scholar] [CrossRef]
- Stenström, T.A.; Okoh, A.I.; Adegoke, A.A. Antibiogram of environmental isolates of Acinetobacter calcoaceticus from Nkonkobe Municipality, South Africa. Fresenius Environ. Bull. 2016, 25, 3059–3065. [Google Scholar] [CrossRef]
- Mahmoudpour, A.; Rahimi, S.; Sina, M.; Soroush, M.H.; Shahisa, S.; Asl-Aminabadi, N. Isolation and identification of Enterococcus faecalis from necrotic root canals using multiplex PCR. J. Oral Sci. 2007, 49, 221–227. [Google Scholar] [CrossRef] [PubMed]
- Mundy, L.M.; Sahm, D.F.; Gilmore, M. Relationships between enterococcal virulence and antimicrobial resistance. Clin. Microbiol. Rev. 2000, 13, 513–522. [Google Scholar] [CrossRef] [PubMed]
- Adegoke, A.A.; Okoh, A.I. Species diversity and antibiotic resistance properties of Staphylococcus of farm animal origin in Nkonkobe Municipality, South Africa. Folia Microbiol. 2014, 59, 133–140. [Google Scholar] [CrossRef]
- Depardieu, F.; Perichon, B.; Courvalin, P. Detection of the van alphabet and identification of enterococci and staphylococci at the species level by multiplex PCR. J. Clin. Microbiol. 2004, 42, 5857–5860. [Google Scholar] [CrossRef] [PubMed]
- World Health Organization. WHO Publishes List of Bacteria for Which New Antibiotics Are Urgently Needed. 2017. Available online: https://www.who.int/news/item/27-02-2017-who-publishes-list-of-bacteria-for-which-new-antibiotics-are-urgently-needed (accessed on 13 February 2025).
- Chuang, O.N.; Schlievert, P.M.; Wells, C.L.; Manias, D.A.; Tripp, T.J. Multiple functional domains of Enterococcus faecalis aggregation substance Asc10 contribute to endocarditis virulence. Infect. Immun. 2009, 77, 539–548. [Google Scholar] [CrossRef]
- Lee, M.G.; Kang, M.J.; Kim, S.; Jeong, H.; Kang, D.K.; Paik, H.D.; Park, Y.S. Safety Assessment of Levilactobacillus brevis KU15006: A Comprehensive Analysis of its Phenotypic and Genotypic Properties. Prob. Antimicrob. Prot. 2024, 1–15. [Google Scholar] [CrossRef]
- Biswas, P.P.; Dey, S.; Sen, A.; Adhikan, L. Molecular characterization of virulence genes in vancomycin-resistant and vancomycin-sensitive enterococci. J. Glob. Infect. Dis. 2016, 8, 16–24. [Google Scholar] [CrossRef]
- Kim, S.J.; Shin, S.Y.; Kang, S.J.; Kim, T.H. Biofilm formation and virulence factors in clinical Enterococcus faecalis isolates from patients with urinary tract infections in Korea. J. Med. Microbiol. 2016, 65, 1165–1173. [Google Scholar] [CrossRef]
- Strateva, T.; Atanasova, D.; Savov, E.; Petrova, G.; Mitov, I. Incidence of virulence determinants in clinical Enterococcus faecalis and Enterococcus faecium isolates collected in Bulgaria. Braz. J. Infect. Dis. 2016, 20, 127–133. [Google Scholar] [CrossRef]
- Zhu, Y.G.; Johnson, T.A.; Su, J.Q.; Qiao, M.; Guo, G.X.; Stedtfeld, R.D.; Hashsham, S.A.; Tiedje, J.M. Diverse and abundant antibiotic resistance genes in Chinese swine farms. Proc. Natl. Acad. Sci. USA 2013, 110, 3435–3440. [Google Scholar] [CrossRef] [PubMed]
- Bengtsson-Palme, J.; Kristiansson, E.; Larsson, D.G.J. Environmental factors influencing the development and spread of antibiotic resistance. FEMS Microbiol. Rev. 2018, 42, fux053. [Google Scholar] [CrossRef] [PubMed]
- Larsson, D.G.J. Pollution from drug manufacturing: Review and perspectives. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2014, 369, 20130571. [Google Scholar] [CrossRef]
- Heuer, H.; Schmitt, H.; Smalla, K. Antibiotic resistance gene spread due to manure application on agricultural fields. Curr. Opin. Microbiol. 2011, 14, 236–243. [Google Scholar] [CrossRef] [PubMed]
- Gaze, W.H.; Krone, S.M.; Larsson, D.G.; Li, X.Z.; Robinson, J.A.; Simonet, P.; Tiedje, J.M. Influence of humans on evolution and mobilization of environmental antibiotic resistome. Emerg. Infect. Dis. 2011, 17, 1205. [Google Scholar] [CrossRef]
- Finley, R.L.; Collignon, P.; Larsson, D.G.; McEwen, S.A.; Li, X.Z. The scourge of antibiotic resistance: The important role of the environment. Clin. Infect. Dis. 2013, 57, 704–710. [Google Scholar] [CrossRef]
- Chee-Sanford, J.C.; Mackie, R.I.; Koike, S.; Krapac, I.G.; Lin, Y.F.; Yannarell, A.C.; Fate, G.D. Fate and transport of antibiotic residues and antibiotic resistance genes following land application of manure waste. J. Environ. Qual. 2009, 38, 1086–1108. [Google Scholar] [CrossRef]
- Muziasari, W.I.; Pitkänen, L.K.; Sorum, H.; Stedtfeld, R.D.; Tiedje, J.M.; Virta, M. The resistome of farmed fish feces contributes to the enrichment of antibiotic resistance genes in sediments below marine fish farms. Front. Microbiol. 2014, 5, 465. [Google Scholar] [CrossRef]
- Iweriebor, B.C.; Obi, L.C.; Okoh, A.I. Macrolide, glycopeptide resistance and virulence genes in Enterococcus species isolates from dairy cattle. J. Med. Microbiol. 2016, 65, 641–648. [Google Scholar] [CrossRef]
- Pignata, C.; Fea, E.; Rovere, R.; Degan, R.; Lorenzi, E.; de Ceglia, M.; Schilirò, T.; Gilli, G. Chlorination in a wastewater treatment plant: Acute toxicity effects of the effluent and of the recipient water body. Environ. Monit. Assess. 2012, 184, 2091–2103. [Google Scholar] [CrossRef]
- Osman, K.; Alvarez-Ordóñez, A.; Ruiz, L.; Badr, J.; ElHofy, F.; Al-Maary, K.S.; Moussa, I.M.; Hessain, A.M.; Orabi, A.; Saad, A.; et al. Antimicrobial resistance and virulence characterization of Staphylococcus aureus and coagulase-negative staphylococci from imported beef meat. Ann. Clin. Microbiol. Antimicrob. 2017, 16, 35. [Google Scholar] [CrossRef] [PubMed]
- Kotzamanidis, C.; Zdragas, A.; Kourelis, A.; Moraitou, E.; Papa, A.; Yiantzi, V.; Pantelidou, C.; Yiangou, M. Characterization of vanA-type Enterococcus faecium isolates from urban and hospital wastewater and pigs. J. Appl. Microbiol. 2009, 107, 997–1005. [Google Scholar] [CrossRef]
- Li, S.; Zhou, Y.; He, F.; Raheem, A.; Yang, H.; Pan, Y.; Pan, Z. Highly efficient capture of antibiotic resistance genes in wastewater using novel biochar-based hybrid adsorbents. Sci. Total Environ. 2023, 863, 160738. [Google Scholar] [CrossRef]
- Johnson, A.P.; Warner, M.; Hallas, G.; Livermore, D.M. Susceptibility to quinupristin/dalfopristin and other antibiotics of van-comycin-resistant enterococci from the UK, 1997 to mid-1999. J. Antimicrob. Chemother. 2000, 46, 167–170. [Google Scholar] [CrossRef] [PubMed]
- Martin, J.F.; Alvarez-Alvarez, R.; Liras, P. Penicillin-binding proteins, β-lactamases, and β-lactamase inhibitors in β-lactam-producing actinobacteria: Self-resistance mechanisms. Int. J. Mol. Sci. 2022, 23, 5662. [Google Scholar] [CrossRef]
- Figueira, V.; Vaz-Moreira, I.; Silva, M.; Manaia, C.M. Diversity and antibiotic resistance of Aeromonas spp. in drinking and wastewater treatment plants. Water Res. 2011, 45, 5599–5611. [Google Scholar] [CrossRef]
- Said, L.B.; Klibi, N.; Lozano, C.; Dziri, R.; Slama, K.B.; Boudabous, A.; Torres, C. Diversity of enterococcal species and characterization of high-level aminoglycoside resistant enterococci of samples of wastewater and surface water in Tunisia. Sci. Total Environ. 2015, 530, 11–17. [Google Scholar] [CrossRef]
- Hashem, Y.A.; Abdelrahman, K.A.; Aziz, R.K. Phenotype–genotype correlations and distribution of key virulence factors in Enterococcus faecalis isolated from patients with urinary tract infections. Infect. Drug Res. 2021, 14, 1713–1723. [Google Scholar] [CrossRef]
- Kajihara, T.; Nakamura, S.; Iwanaga, N.; Oshima, K.; Takazono, T.; Miyazaki, T.; Izumikawa, K.; Yanagihara, K.; Kohno, N.; Kohno, S. Clinical characteristics and risk factors of enterococcal infections in Nagasaki, Japan: A retrospective study. BMC Infect. Dis. 2015, 15, 426. [Google Scholar] [CrossRef]
- Revathy, S.; Sridharan, K.S.; Elumalai, A.S.; Umasekar, U. Phenotypic detection of high-level aminoglycoside resistance (HLAR) in Enterococcus species in a tertiary care centre. J. Clin. Diagn. Res. 2009, 3, 1785–1790. [Google Scholar]
- La-Rosa, S.L.; Montealegre, M.C.; Singh, K.V.; Murray, B.E. Enterococcus faecalis Ebp pili are important for cell-cell aggregation and intraspecies gene transfer. Microbiology 2016, 162, 798–802. [Google Scholar] [CrossRef] [PubMed]
- Barbosa, J.; Gibbs, P.A.; Teixeira, P. Virulence factors among enterococci isolated from traditional fermented meat products produced in the North of Portugal. Food Control 2010, 21, 651–656. [Google Scholar] [CrossRef]
- Rahman, M.M.; Hasan, M.; Ahmed, A. Potential detrimental role of soluble ACE2 in severe COVID-19 comorbid patients. Rev. Med. Virol. 2021, 31, 1–12. [Google Scholar] [CrossRef]
- Maheshwari, M.; Ahmad, I.; Althubiani, A.S. Isolation and molecular characterization of multidrug-resistant Enterococcus faecalis from clinical samples. Trop. J. Pharm. Res. 2016, 15, 1207–1213. [Google Scholar]
- Chajęcka-Wierzchowska, W.; Zadernowska, A.; Łaniewska-Trokenheim, Ł. Virulence factors of Enterococcus spp. presented in food. LWT 2017, 75, 670–676. [Google Scholar] [CrossRef]
- Gonzalez, B.; Pham, P.; Top, J.; Willems, R.J.L.; van Schaik, W.; van Passel, M.W.J.; Smidt, H. Characterization of Enterococcus isolates colonizing the intestinal tract of intensive care unit patients receiving selective digestive decontamination. Front. Microbiol. 2017, 8, 1596. [Google Scholar] [CrossRef]
- Adegoke, A.A.; Faleye, A.C.; Stenstrom, T.A. Residual antibiotics, antibiotic-resistant superbugs, and antibiotic resistance genes in surface water catchments: Public health impact. Phys. Chem. Earth 2018, 105, 177–183. [Google Scholar] [CrossRef]
- Vincent, S.; Minkler, P.; Bincziewski, B.; Etter, L.; Shlaes, D.M. Vancomycin resistance in Enterococcus gallinarum. Antimicrob. Agents Chemother. 1992, 36, 1392–1399. [Google Scholar] [CrossRef]
- Hao, L.; Wang, H. Successful treatment of Enterococcus gallinarum infection in a neonate with vancomycin: A case report. BMC Pediatr. 2024, 24, 527. [Google Scholar] [CrossRef]
- Tharvornvee, W.; Pruksakorn, C.; Lekcharoensuk, P. Inducible vancomycin resistance is common in porcine Enterococcus gallinarum and E. casseliflavus isolates. Thai J. Vet. Med. 2016, 46, 627–635. [Google Scholar] [CrossRef]
- García-Solache, M.; Rice, L.B. The Enterococcus: A model of adaptability to its environment. Clin. Microbiol. Rev. 2019, 32, e00058-18. [Google Scholar] [CrossRef]
- Lioy, P.J. Exposure science: A view of the past and milestones for the future. Environ. Health Perspect. 2010, 118, 1081–1090. [Google Scholar] [CrossRef] [PubMed]
- Keraita, B.; Amoah, P. Wastewater use in urban and peri-urban vegetable farming. In Wastewater Irrigation and Health; Drechsel, P., Scott, C.A., Raschid-Sally, L., Eds.; IWMI: Colombo, Sri Lanka, 2011; pp. 11–25. [Google Scholar]
- Bonetta, S.; Pignata, C.; Gasparro, E.; Richiardi, L.; Bonetta, S.; Carraro, E. Impact of wastewater treatment plants on microbiological contamination for evaluating the risks of wastewater reuse. Environ. Sci. Eur. 2022, 34, 20. [Google Scholar] [CrossRef]
- Torres, C.; Alonso, C.A.; Ruiz-Ripa, L.; León-Sampedro, R.; Del Campo, R.; Coque, T.M. Antimicrobial resistance in Enterococcus spp. of animal origin. In Antimicrobial Resistance in Bacteria from Livestock and Companion Animals; Wiley: Hoboken, NJ, USA, 2018; pp. 185–227. [Google Scholar]
- European Centre for Disease Prevention and Control (ECDC). European Centre for Disease Prevention and Control Publishes Annual Epidemiological Report 2011. Eurosurveillance 2011, 16, 20012. [Google Scholar]
- Ammerlaan, H.S.; Harbarth, S.; Buiting, A.G.; Crook, D.W.; Fitzpatrick, F.; Hanberger, H.; Herwaldt, L.A.; Van Keulen, P.H.; Kluytmans, J.A.; Kola, A.; et al. Secular trends in nosocomial bloodstream infections: Antibiotic-resistant bacteria increase the total burden of infection. Clin. Infect. Dis. 2013, 56, 798–805. [Google Scholar] [CrossRef] [PubMed]
- De Kraker, M.E.; Jarlier, V.; Monen, J.C.; Heuer, O.E.; van de Sande, N.; Grundmann, H. The changing epidemiology of bacteraemias in Europe: Trends from the European Antimicrobial Resistance Surveillance System. Clin. Microbiol. Infect. 2013, 19, 860–868. [Google Scholar] [CrossRef] [PubMed]
- Didem, K.A.R.T.; Kuştimur, A.S. Investigation of gelatinase gene expression and growth of Enterococcus faecalis clinical isolates in biofilm models. Turk. J. Pharm. Sci. 2019, 16, 356. [Google Scholar]
- Holá, V.; Ruzicka, F.; Horka, M. Microbial diversity in biofilm infections of the urinary tract with the use of sonication techniques. FEMS Immunol. Med. Microbiol. 2010, 59, 525–528. [Google Scholar] [CrossRef]
- Dworniczek, E.; Piwowarczyk, J.; Bania, J.; Kowalska-Krochmal, B.; Wałecka, E.; Seniuk, A.; Dolna, I.; Gościniak, G. Enterococcus in wound infections: Virulence and antimicrobial resistance. Acta Microbiol. Immunol. Hung. 2012, 59, 263–269. [Google Scholar] [CrossRef]
- Sava, I.; Heikens, E.; Toma, I.; Kropec, A.; Willems, R.; Hübner, J. Enterococcal surface protein is a virulence factor in bacteremia but is not a target of opsonic antibodies in E. faecium infection. In Proceedings of the American Society for Microbiology 109th General Meeting, Philadelphia, PA, USA, 17–21 May 2009. [Google Scholar]
Group | Van Gene | No of Isolates | Percentage | Species Involved |
---|---|---|---|---|
VRE | vanA | 149 | 73.8 | Enterococcus faecium, Enterococcus faecalis, Enterococcus hirae, Enterococcus durans |
vanB | 3 | 1.5 | E. faecalis | |
vanC1 | 33 | 16.3 | E. gallinarum, E. casseliflavus E. cecorum | |
vanC2/3 | 16 | 7.9 | E. gallinarum, E. casseliflavus E. faecium | |
VSE | vanA | 14 | 20.9 | E. faecium, E. hirae, E. faecalis, E. durans |
vanB | 0 | 0 | no species | |
vanC1 | 1 | 1.5 | E. casseliflavus | |
vanC2/3 | 7 | 10.4 | E. gallinarum, E. casseliflavus E. faecium/faecalis | |
none | 45 | 67.2 | E. faecium, E. hirae, E. faecalis, E. durans |
VRE No (%) | VSE No (%) | |
---|---|---|
tet(K) | 16/202 (7.9) | 2/67 (3) |
tet(L) | 61/202 (30.2) | 7/67 (10.4) |
tet(M) | 40/202 (19.8) | 12/67 (17.9) |
tet(O) | 10/202 (5.0) | 0 (0) |
emeA | 27/202(13.4) | 8/67 (11.9) |
Virulence Gene | E. faecalis (12) | E. faecium (50) | E. hirae (5) | E. casseliflavus (7) | E. gallinarum (14) |
---|---|---|---|---|---|
efaA | 10 (83.3%) | 5 (10%) | 4 (80%) | 2 (28.6%) | 1 (7.1%) |
ace | 8(66.7%) | 2(4%) | 1 (20%) | - | 1 (7.1%) |
asa1 | 7 (58.3%) | 1 (2%) | - | - | 2 (14.3%) |
hyl | - | 8 (16%) | - | - | - |
esp | 4 (33.3%) | - | - | - | - |
gelE | 9 (75%) | 5 (10%) | - | 1 (14.3%) | 1 (7.1%) |
cylA | - | - | - | 1(14.3%) | - |
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Adegoke, A.A.; Madu, C.E.; Reddy, P.; Fatunla, O.K.; Stenström, T.A.; Okoh, A.I. Virulence and Antibiotic Resistance Genes in Enterococcus from Wastewater for Reuse and Their Health Impact. Microorganisms 2025, 13, 1045. https://doi.org/10.3390/microorganisms13051045
Adegoke AA, Madu CE, Reddy P, Fatunla OK, Stenström TA, Okoh AI. Virulence and Antibiotic Resistance Genes in Enterococcus from Wastewater for Reuse and Their Health Impact. Microorganisms. 2025; 13(5):1045. https://doi.org/10.3390/microorganisms13051045
Chicago/Turabian StyleAdegoke, Anthony A., Chibuzor E. Madu, Poovendhree Reddy, Opeyemi K. Fatunla, Thor A. Stenström, and Anthony I. Okoh. 2025. "Virulence and Antibiotic Resistance Genes in Enterococcus from Wastewater for Reuse and Their Health Impact" Microorganisms 13, no. 5: 1045. https://doi.org/10.3390/microorganisms13051045
APA StyleAdegoke, A. A., Madu, C. E., Reddy, P., Fatunla, O. K., Stenström, T. A., & Okoh, A. I. (2025). Virulence and Antibiotic Resistance Genes in Enterococcus from Wastewater for Reuse and Their Health Impact. Microorganisms, 13(5), 1045. https://doi.org/10.3390/microorganisms13051045