Surveillance of Multidrug-Resistant Genes in Clinically Significant Gram-Negative Bacteria Isolated from Hospital Wastewater
Abstract
1. Introduction
2. Results
2.1. Distribution of Gram-Negative Bacteria Across Hospital Wastewater Sites
2.2. Antibiotic Susceptibility Patterns of Gram-Negative Bacteria from Hospital Wastewater
2.3. MAR Indexing Pattern in Hospital Wastewater
2.4. Screening for ARGs in WWTPs
3. Discussion
4. Materials and Methods
4.1. Sampling Sites and Collection of HWW
4.2. Bacterial Isolation and Identification
4.3. Antibiotic Susceptibility Test
4.4. Determination of Antibiotic Resistance Pattern
4.5. Bacterial DNA Extraction
4.6. Detection of ARGs
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
Abbreviations
AMR | Antimicrobial resistance |
AR | Antibiotic resistance |
ARB | antibiotic-resistant bacteria |
AR-GNB | Antibiotic-resistant Gram-negative bacteria |
ARGs | antibiotic resistance genes |
ARI | Antibacterial resistance index |
EMB | Eosin Methylene Blue |
HWW | Hospital wastewater |
JPIAMR | The Joint Programme Initiative on Antimicrobial Resistance |
MAR | Multiple antibiotic resistance |
MDR | Multidrug resistance |
PDR | Pan-drug-resistant |
QRDRs | Quinolone resistance-determining regions |
TCBS | Thiosulfate Citrate Bile sucrose |
TSA | Trypticase Soya Agar |
WHO | World Health Organization |
XDR | extensive drug resistance |
WWTPs | Wastewater Treatment Plants |
References
- Numberger, D.; Ganzert, L.; Zoccarato, L.; Mühldorfer, K.; Sauer, S.; Grossart, H.P.; Greenwood, A.D. Characterization of Bacterial Communities in Wastewater with Enhanced Taxonomic Resolution by Full-Length 16S RRNA Sequencing. Sci. Rep. 2019, 9, 9673. [Google Scholar] [CrossRef] [PubMed]
- Surleac, M.; Barbu, I.C.; Paraschiv, S.; Popa, L.I.; Gheorghe, I.; Marutescu, L.; Popa, M.; Sarbu, I.; Talapan, D.; Nita, M.; et al. Whole Genome Sequencing Snapshot of Multidrug Resistant Klebsiella pneumoniae Strains from Hospitals and Receiving Wastewater Treatment Plants in Southern Romania. PLoS ONE 2020, 15, e0228079. [Google Scholar] [CrossRef]
- Rodríguez, E.A.; Garzón, L.M.; Gómez, I.D.; Jiménez, J.N. Multidrug Resistance and Diversity of Resistance Profiles in Carbapenem-Resistant Gram-Negative Bacilli Throughout a Wastewater Treatment Plant in Colombia. J. Glob. Antimicrob. Resist. 2020, 22, 358–366. [Google Scholar] [CrossRef]
- Talat, A.; Blake, K.S.; Dantas, G.; Khan, A.U. Metagenomic Insight into Microbiome and Antibiotic Resistance Genes of High Clinical Concern in Urban and Rural Hospital Wastewater of Northern India Origin: A Major Reservoir of Antimicrobial Resistance. Microbiol. Spectr. 2023, 11, e04102-22. [Google Scholar] [CrossRef]
- Manik, R.K.; Mahmud, Z.; Mishu, I.D.; Hossen, M.S.; Howlader, Z.H.; Nabi, A.H.M.N. Multidrug Resistance Profiles and Resistance Mechanisms to β-Lactams and Fluoroquinolones in Bacterial Isolates from Hospital Wastewater in Bangladesh. Curr. Issues Mol. Biol. 2023, 45, 6485–6502. [Google Scholar] [CrossRef]
- Adekanmbi, A.O.; Akinpelu, M.O.; Olaposi, A.V.; Oyelade, A.A. Extended Spectrum Beta-Lactamase Encoding Gene-Fingerprints in Multidrug Resistant Escherichia Coli Isolated from Wastewater and Sludge of a Hospital Treatment Plant in Nigeria. Int. J. Environ. Stud. 2020, 78, 140–150. [Google Scholar] [CrossRef]
- Shekhawat, S.S.; Kulshreshtha, N.M.; Mishra, R.; Arora, S.; Vivekanand, V.; Gupta, A.B. Antibiotic Resistance in a Predominantly Occurring Gram-Negative Bacterial Community from Treated Sewage to Assess the Need for Going beyond Coliform Standards. Water Qual. Res. J. 2021, 56, 143–154. [Google Scholar] [CrossRef]
- Bhaurao, B.C.; Rajendra, A.S.; Sarita, L.S. Isolation and Characterization of Multidrug Resistance Bacteria from Hospital Sewage Samples, Maharashtra, India. African J. Biotechnol. 2022, 21, 16–25. [Google Scholar] [CrossRef]
- Kumar, G.; Balakrishna, K.; Mukhopadhyay, C.; Eshwara, V.K. Characterization and Comparative Analysis of Antimicrobial Resistance in Escherichia Coli from Hospital and Municipal Wastewater Treatment Plants. J. Water Health 2024, 22, 2276–2288. [Google Scholar] [CrossRef]
- Kutilova, I.; Medvecky, M.; Leekitcharoenphon, P.; Munk, P.; Masarikova, M.; Davidova-Gerzova, L.; Jamborova, I.; Bortolaia, V.; Pamp, S.J.; Dolejska, M. Extended-Spectrum Beta-Lactamase-Producing Escherichia Coli and Antimicrobial Resistance in Municipal and Hospital Wastewaters in Czech Republic: Culture-Based and Metagenomic Approaches. Environ. Res. 2021, 193, 110487. [Google Scholar] [CrossRef]
- Addae-Nuku, D.S.; Kotey, F.C.N.; Dayie, N.T.K.D.; Osei, M.M.; Tette, E.M.A.; Debrah, P.; Donkor, E.S. Multidrug-Resistant Bacteria in Hospital Wastewater of the Korle Bu Teaching Hospital in Accra, Ghana. Environ. Health Insights 2022, 16, 11786302221130612. [Google Scholar] [CrossRef] [PubMed]
- Carlsen, L.; Büttner, H.; Christner, M.; Cordts, L.; Franke, G.; Hoffmann, A.; Knobling, B.; Lütgehetmann, M.; Nakel, J.; Werner, T.; et al. Long Time Persistence and Evolution of Carbapenemase-Producing Enterobacterales in the Wastewater of a Tertiary Care Hospital in Germany. J. Infect. Public Health 2023, 16, 1142–1148. [Google Scholar] [CrossRef] [PubMed]
- Adefisoye, M.A.; Okoh, A.I. Ecological and Public Health Implications of the Discharge of Multidrug-Resistant Bacteria and Physicochemical Contaminants from Treated Wastewater Effluents in the Eastern Cape, South Africa. Water 2017, 9, 562. [Google Scholar] [CrossRef]
- Majlander, J.; Anttila, V.J.; Nurmi, W.; Seppälä, A.; Tiedje, J.; Muziasari, W. Routine Wastewater-Based Monitoring of Antibiotic Resistance in Two Finnish Hospitals: Focus on Carbapenem Resistance Genes and Genes Associated with Bacteria Causing Hospital-Acquired Infections. J. Hosp. Infect. 2021, 117, 157–164. [Google Scholar] [CrossRef]
- Irfan, M.; Almotiri, A.; AlZeyadi, Z.A. Antimicrobial Resistance and β-Lactamase Production in Clinically Significant Gram-Negative Bacteria Isolated from Hospital and Municipal Wastewater. Antibiotics 2023, 12, 653. [Google Scholar] [CrossRef]
- Mustafa, S.S.; Batool, R.; Kamran, M.; Javed, H.; Jamil, N. Evaluating the Role of Wastewaters as Reservoirs of Antibiotic-Resistant ESKAPEE Bacteria Using Phenotypic and Molecular Methods. Infect. Drug Resist. 2022, 15, 5715–5728. [Google Scholar] [CrossRef]
- Zhang, S.; Huang, J.; Zhao, Z.; Cao, Y.; Li, B. Hospital Wastewater as a Reservoir for Antibiotic Resistance Genes: A Meta-Analysis. Front. Public Health 2020, 8, 574968. [Google Scholar] [CrossRef]
- Rahman, M.M.; Devnath, P.; Jahan, R.; Talukder, A. Detection of Multiple Antibiotic-Resistant Bacteria from the Hospital and Non-Hospital Wastewater Sources of a Small Town in Noakhali, Bangladesh. J. Appl. Biol. Biotechnol. 2021, 9, 59–65. [Google Scholar] [CrossRef]
- Guruge, K.S.; Tamamura, Y.A.; Goswami, P.; Tanoue, R.; Jinadasa, K.B.S.N.; Nomiyama, K.; Ohura, T.; Kunisue, T.; Tanabe, S.; Akiba, M. The Association between Antimicrobials and the Antimicrobial-Resistant Phenotypes and Resistance Genes of Escherichia Coli Isolated from Hospital Wastewaters and Adjacent Surface Waters in Sri Lanka. Chemosphere 2021, 279, 130591. [Google Scholar] [CrossRef]
- Shibuki, R.; Nishiyama, M.; Mori, M.; Baba, H.; Kanamori, H.; Watanabe, T. Characterization of Extended-Spectrum β-Lactamase-Producing Escherichia Coli Isolated from Municipal and Hospital Wastewater in Japan. J. Glob. Antimicrob. Resist. 2023, 32, 145–151. [Google Scholar] [CrossRef]
- Souleymane, C.; Fernique, K.K.; Baguy, O.M.; Maxime, D.; Ambroise, K.; Marcelle, M.; Felix, N. Prevalence of Resistant Enterobacterales, in Particular ESBL-Producing Escherichia Coli in Hospital Wastewater Discharged into the Environment: Study of the Abidjan District, Côte d’Ivoire. J. Adv. Microbiol. 2025, 25, 37–46. [Google Scholar] [CrossRef]
- Bourles, A.; Kainiu, M.; Objois, T.; Palma, F.; Brisse, S.; Gourinat, A.-C.; Biron, A.; Pot, M.; Veyrier, F.; Goarant, C.; et al. Water-Based Surveillance Detects Silent Circulation of Carbapenem and Third Generation Cephalosporin Resistant Gram-Negative Bacteria in New Caledonian Environment. Lancet 2025, in press. [Google Scholar]
- Delgado-Blas, J.F.; Valenzuela Agüi, C.; Marin Rodriguez, E.; Serna, C.; Montero, N.; Saba, C.K.S.; Gonzalez-Zorn, B. Dissemination Routes of Carbapenem and Pan-Aminoglycoside Resistance Mechanisms in Hospital and Urban Wastewater Canalizations of Ghana. mSystems 2022, 7, e01019-21. [Google Scholar] [CrossRef]
- Puljko, A.; Barišić, I.; Dekić Rozman, S.; Križanović, S.; Babić, I.; Jelić, M.; Maravić, A.; Udiković-Kolić, N. Molecular Epidemiology and Mechanisms of Carbapenem and Colistin Resistance in Klebsiella and Other Enterobacterales from Treated Wastewater in Croatia. Environ. Int. 2024, 185, 108554. [Google Scholar] [CrossRef]
- Girijan, S.K.; Paul, R.; Rejish Kumar, V.J.; Pillai, D. Investigating the Impact of Hospital Antibiotic Usage on Aquatic Environment and Aquaculture Systems: A Molecular Study of Quinolone Resistance in Escherichia Coli. Sci. Total Environ. 2020, 748, 141538. [Google Scholar] [CrossRef]
- Castrignanò, E.; Kannan, A.M.; Proctor, K.; Petrie, B.; Hodgen, S.; Feil, E.J.; Lewis, S.E.; Lopardo, L.; Camacho-Muñoz, D.; Rice, J.; et al. (Fluoro)Quinolones and Quinolone Resistance Genes in the Aquatic Environment: A River Catchment Perspective. Water Res. 2020, 182, 116015. [Google Scholar] [CrossRef]
- Rolbiecki, D.; Harnisz, M.; Korzeniewska, E.; Jałowiecki, Ł.; Płaza, G. Occurrence of Fluoroquinolones and Sulfonamides Resistance Genes in Wastewater and Sludge at Different Stages of Wastewater Treatment: A Preliminary Case Study. Appl. Sci. 2020, 10, 5816. [Google Scholar] [CrossRef]
- Park, J.H.; Kang, J.; Bae, K.S.; Lee, H.; Kim, J.; Park, E.R.; Yoon, J.K.; Lee, S.H. Evaluation and Characterization of Quinolone-Resistant Escherichia Coli in Wastewater Treatment Plant Effluents. Water 2023, 15, 4040. [Google Scholar] [CrossRef]
- Galarde-López, M.; Velazquez-Meza, M.E.; Bobadilla-Del-valle, M.; Cornejo-Juárez, P.; Carrillo-Quiroz, B.A.; Ponce-De-león, A.; Sassoé-González, A.; Saturno-Hernández, P.; Alpuche-Aranda, C.M. Antimicrobial Resistance Patterns and Clonal Distribution of E. Coli, Enterobacter Spp. and Acinetobacter Spp. Strains Isolated from Two Hospital Wastewater Plants. Antibiotics 2022, 11, 601. [Google Scholar] [CrossRef]
- Divyashree, M.; Mani, M.K.; Shama Prakash, K.; Vijaya Kumar, D.; Veena Shetty, A.; Shetty, A.K.; Karunasagar, I. Hospital Wastewater Treatment Reduces NDM-Positive Bacteria Being Discharged into Water Bodies. Water Environ. Res. 2020, 92, 562–568. [Google Scholar] [CrossRef]
- Proia, L.; Anzil, A.; Borrego, C.; Farrè, M.; Llorca, M.; Sanchis, J.; Bogaerts, P.; Balcázar, J.L.; Servais, P. Occurrence and Persistence of Carbapenemases Genes in Hospital and Wastewater Treatment Plants and Propagation in the Receiving River. J. Hazard. Mater. 2018, 358, 33–43. [Google Scholar] [CrossRef] [PubMed]
- Azuma, T.; Otomo, K.; Kunitou, M.; Shimizu, M.; Hosomaru, K.; Mikata, S.; Ishida, M.; Hisamatsu, K.; Yunoki, A.; Mino, Y.; et al. Environmental Fate of Pharmaceutical Compounds and Antimicrobial-Resistant Bacteria in Hospital Effluents, and Contributions to Pollutant Loads in the Surface Waters in Japan. Sci. Total Environ. 2019, 657, 476–484. [Google Scholar] [CrossRef] [PubMed]
- Takizawa, S.; Soga, E.; Hayashi, W.; Sakaguchi, K.; Koide, S.; Tanabe, M.; Denda, T.; Sugawara, Y.; Yu, L.; Kayama, S.; et al. Genomic Landscape of BlaGES-5- and BlaGES-24-Harboring Gram-Negative Bacteria from Hospital Wastewater: Emergence of Class 3 Integron-Associated BlaGES-24 Genes. J. Glob. Antimicrob. Resist. 2022, 31, 196–206. [Google Scholar] [CrossRef] [PubMed]
- Rocha, J.; Ferreira, C.; Mil-Homens, D.; Busquets, A.; Fialho, A.M.; Henriques, I.; Gomila, M.; Manaia, C.M. Third Generation Cephalosporin-Resistant Klebsiella pneumoniae Thriving in Patients and in Wastewater: What Do They Have in Common? BMC Genom. 2022, 23, 72. [Google Scholar] [CrossRef]
- Seguni, N.Z.; Kimera, Z.I.; Msafiri, F.; Mgaya, F.X.; Joachim, A.; Mwingwa, A.; Matee, M.I. Multidrug-Resistant Escherichia Coli and Klebsiella pneumoniae Isolated from Hospital Sewage Flowing through Community Sewage System and Discharging into the Indian Ocean. Bull. Natl. Res. Cent. 2023, 47, 66. [Google Scholar] [CrossRef]
- Sinclair, C.G. Bergey’s Manual of Determinative Bacteriology, 9th ed.; Lippincott Williams & Wilkins: Philadelphia, PA, USA, 1939; Volume S1–S19, ISBN 978-0-683-00603-2. [Google Scholar]
- CLSI M100; Performance Standards for Antimicrobial Susceptibility. 32nd ed. Clinical and Laboratory Standard Institute: Wayne, PA, USA, 2019; ISBN 9781684400324.
- Krumperman, P.H. Multiple Antibiotic Resistance Indexing of Escherichia Coli to Identify High-Risk Sources of Fecal Contamination of Foods. Appl. Environ. Microbiol. 1983, 46, 165–170. [Google Scholar] [CrossRef]
- Aditya, V.; Kotian, A.; Saikrishnan, S.; Rohit, A.; Mithoor, D.; Karunasagar, I.; Deekshit, V.K. Effect of Ciprofloxacin and in Vitro Gut Conditions on Biofilm of Escherichia Coli Isolated from Clinical and Environmental Sources. J. Appl. Microbiol. 2022, 132, 964–977. [Google Scholar] [CrossRef]
- Monstein, H.J.; Östholm-Balkhed, Å.; Nilsson, M.V.; Nilsson, M.; Dornbusch, K.; Nilsson, L.E. Multiplex PCR Amplification Assay for the Detection of BlaSHV, BlaTEM and BlaCTX-M Genes in Enterobacteriaceae. Apmis 2007, 115, 1400–1408. [Google Scholar] [CrossRef]
- Kaftandzieva, A.; Trajkovska-Dokic, E.; Panovski, N. Prevalence and Molecular Characterization of Extended Spectrum Beta-Lactamases (ESBLs) Producing Escherichia Coli and Klebsiella pneumoniae. Prilozi 2011, 32, 129–141. [Google Scholar]
- Poirel, L.; Walsh, T.R.; Cuvillier, V.; Nordmann, P. Multiplex PCR for Detection of Acquired Carbapenemase Genes. Diagn. Microbiol. Infect. Dis. 2011, 70, 119–123. [Google Scholar] [CrossRef]
- Ma, M.; Wang, H.; Yu, Y.; Zhang, D.; Liu, S. Detection of Antimicrobial Resistance Genes of Pathogenic Salmonella from Swine with DNA Microarray. J. Vet. Diagn. Investig. 2007, 19, 161–167. [Google Scholar] [CrossRef] [PubMed]
- 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] [PubMed]
Organism Identified | MAR Index |
---|---|
Aeromonas (n = 1) | 0.7 |
Citrobacter freundii (n = 4) | 0.33 |
Citrobacter koseri (n = 2) | 0.53 |
E. coli (n = 13) | 0.55 |
Enterobacter aerogenes (n = 1) | 0.3 |
Klebsiella pneumoniae (n = 16) | 0.48 |
Klebsiella oxytoca (n = 4) | 0.56 |
Pseudomonas (n = 4) | 0.5 |
Proteus vulgaris (n = 3) | 0.65 |
Proteus mirabilis (n = 1) | 0.65 |
Sampling Sites (n = Isolate) | MAR Index |
---|---|
SWW (n = 12) | 0.51 |
HWW-01 (n = 12) | 0.54 |
HWW-02 (n = 9) | 0.53 |
HWW-03 (n = 16) | 0.48 |
Organism Identified | Class of Antibiotics | ||||||||
---|---|---|---|---|---|---|---|---|---|
Aminoglycoside | β-Lactam | Cephalosporin | Phenicols | Fluoroquinolones | Sulfonamides | Carbapenem | Quinolone | Tetracycline | |
Citrobacter (n = 6) | 0.02 | 0.11 | 0.09 | 3.33 | 13.33 | 0 | 0.03 | 10 | 10 |
Ecoli (n = 13) | 0.04 | 0.14 | 0.16 | 0.003 | 0.05 | 0.02 | 0.04 | 0.04 | 0.03 |
Pseudomonas aeruginosa (n = 4) | 0 | 0.1 | 0.13 | 0.03 | 0.01 | 0.03 | 0.03 | 0.05 | 0.04 |
Enterobacter aerogens (n = 1) | 0 | 0.05 | 0.05 | 0 | 0.05 | 0 | 0.05 | 0 | 0.05 |
Aeromonas (n = 1) | 0 | 0.2 | 0.2 | 0.05 | 0.05 | 0 | 0 | 0.05 | 0.05 |
Klebsiella spp. (n = 20) | 0.04 | 0.145 | 0.145 | 0 | 0.04 | 0.01 | 0.05 | 0.02 | 0.015 |
Proteus (n = 4) | 0.03 | 0.13 | 0.16 | 0.05 | 0.04 | 0.05 | 0.04 | 0.05 | 0.05 |
Citrobacter (n = 6) | 0.03 | 0.11 | 0.09 | 3.33 | 13.33 | 0 | 0.03 | 10 | 10 |
Site | Class of Antibiotics | ||||||||
---|---|---|---|---|---|---|---|---|---|
Aminoglycoside | β-Lactam | Cephalosporin | Phenicols | Fluoroquinolones | Sulfonamides | Carbapenem | Quinolone | Tetracycline | |
SWW (n = 12) | 0.03 | 0.15 | 0.14 | 0.004 | 0.04 | 0.01 | 0.04 | 0.03 | 0.017 |
HWW-01 (n = 12) | 0.05 | 0.12 | 0.13 | 0.01 | 0.03 | 0.02 | 0.05 | 0.03 | 0.03 |
HWW-02 (n = 9) | 0.03 | 0.12 | 0.15 | 0.01 | 0.03 | 0.02 | 0.04 | 0.02 | 0.03 |
HWW-03 (n = 16) | 0.03 | 0.12 | 0.125 | 0.009 | 0.05 | 0.01 | 0.03 | 0.03 | 0.03 |
Antibiotic | Primer | Primer Sequence (5′-3′) | Size (bp) | Reference |
---|---|---|---|---|
Penicillin and cephalosporins | blaSHV | F-AAAGCGAAAGCCAGCTGTCG | 656 | [40] |
R-GTTATTCGGGCCAAGCAGGG | ||||
Ampicillin | blaTEM | F-CGCCCCGAAGAACGTTTTCC | 329 | |
R-CGTTGGGAACCGGAGCTG | ||||
Cefotaxime | blaCTX-M | F-CGGTGCAACAAAAGCTGGCG | 503 | |
R-GCGGCTGGGTAAAATAGGTC | ||||
CTX-M group I | blaCTM-M15 | F-ATCACTGCGCCAGTTCACGCT | 584 | [41] |
R-GGCTGGGTGAAGTAAGTGACC | ||||
Carbapenem | blaNDM-1 | F-GGTTTGGCGATCTGGTTTTC | 621 | [42] |
R-CGGAATGGCTCATCACGATC | ||||
blaIMP | F-GGAATAGAGTGGCTTAACTCTC | 232 | ||
R-GGTTTAACAAAACAACCACC | ||||
blaVIM | F-GATGGTGTTTGGTCGCATA | 390 | ||
R-CGAATGCGCAGCACCAG | ||||
blaKPC | F-CGTCTAGTTCTGCTGTCTTG | 798 | ||
R-CTTGTCATCCTTGTTAGGCG | ||||
blaOXA-48 | F-GCGTGGTTAAGGATGAACAC | 438 | ||
R-CATCAAGTTCAACCCAACCG | ||||
Tetracycline | tetD | F-GCAAACCATTACGGCATTCT | 546 | [43] |
R-GATAAGCTGCGCGGTAAAAA | ||||
tetE | F-TATTAACGGGCTGGCATTTC | 544 | ||
R-AGCTGTCAGGTGGGTCAAAC | ||||
tetG | F-GCTCGGTGGTATCTCTGCTC | 550 | ||
R-CAAAGCCCCTTGCTTGTTAC | ||||
Chloramphenicol | catA1 | F-AACCAGACCGTTCAGCTGGAT | 549 | |
R-CCTGCCACTCATCGCAGTAC | ||||
catA2 | F-AACGGCATGATGAACCTGAA | 547 | ||
R-ATCCCAATGGCATCGTAAAG | ||||
Sulfonamide | sulIII | F-ATGAGCAAGATTTTTGGAATCGT | 792 | |
R-CTAACCTAGGGCTTTGGATATTT | ||||
Plasmid-mediated quinolone resistance genes Quinolones | qnrA | F-ATTTCTCACGCCAGGATTTG | 516 | [44] |
R-GATCGGCAAAGGTTAGGTCA | ||||
qnrB | F-GATCGTGAAAGCCAGAAAGG | 469 | ||
R-ACGATGCCTGGTAGTTGTCC | ||||
qnrS | F-ACGACATTCGTCAACTGCAA | 417 | ||
R-TAAATTGGCACCCTGTAGGC | ||||
Fluoroquinolone | qepa | F-CGTGTTGCTGGAGTTCTTC | 403 | |
R-CTGCAGGTACTGCGTCATG |
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Shetty, S.C.; Gowda, L.S.; Jacob, A.M.; Shetty, K.; Shetty, A.V. Surveillance of Multidrug-Resistant Genes in Clinically Significant Gram-Negative Bacteria Isolated from Hospital Wastewater. Antibiotics 2025, 14, 607. https://doi.org/10.3390/antibiotics14060607
Shetty SC, Gowda LS, Jacob AM, Shetty K, Shetty AV. Surveillance of Multidrug-Resistant Genes in Clinically Significant Gram-Negative Bacteria Isolated from Hospital Wastewater. Antibiotics. 2025; 14(6):607. https://doi.org/10.3390/antibiotics14060607
Chicago/Turabian StyleShetty, Shriya C., Lakshya S. Gowda, Ankeeta Menona Jacob, Kalidas Shetty, and A. Veena Shetty. 2025. "Surveillance of Multidrug-Resistant Genes in Clinically Significant Gram-Negative Bacteria Isolated from Hospital Wastewater" Antibiotics 14, no. 6: 607. https://doi.org/10.3390/antibiotics14060607
APA StyleShetty, S. C., Gowda, L. S., Jacob, A. M., Shetty, K., & Shetty, A. V. (2025). Surveillance of Multidrug-Resistant Genes in Clinically Significant Gram-Negative Bacteria Isolated from Hospital Wastewater. Antibiotics, 14(6), 607. https://doi.org/10.3390/antibiotics14060607