Distribution of Antibiotic Resistance in a Mixed-Use Watershed and the Impact of Wastewater Treatment Plants on Antibiotic Resistance in Surface Water
Abstract
:1. Introduction
2. Results
2.1. Prevalence and Distribution of AR Contaminants in Surface Water
2.1.1. Antibiotic-Resistant Salmonella, Escherichia coli, and Enterococcus
2.1.2. ESBL-Producing Enterobacteriaceae and Carbapenem-Resistant Enterobacteriaceae (CRE)
2.1.3. Antibiotic Resistance Gene Markers
2.1.4. Antibiotics
2.2. WWTPs as a Source of AR Contaminants
3. Discussion
3.1. Prevalence and Distribution of AR Contaminants in Surface Water
3.1.1. Antibiotic-Resistant Salmonella, E. coli, and Enterococcus
3.1.2. ESBL-Producing Enterobacteriaceae and CRE
3.1.3. Antibiotic Resistance Gene Markers
3.1.4. Antibiotics
3.2. WWTPs as a Source of AR Contaminants
4. Materials and Methods
4.1. Surface Water and Wastewater Samples
4.2. Antibiotic-Resistant E. coli, Enterococcus, and Salmonella
4.2.1. Isolation and Identification of E. coli, Enterococcus, and Salmonella
4.2.2. Antimicrobial Susceptibility Testing
4.3. ESBL-Producing Enterobacteriaceae and CRE
4.3.1. Isolation and Identification of ESBL-Producing Enterobacteriaceae and CRE
4.3.2. Confirmation of ESBL Producers and CRE and Detection of β-Lactamase Genes
4.4. Antibiotic Resistance Gene Markers
4.5. Antibiotics
4.5.1. Antibiotics
4.5.2. Sample Preparation
4.5.3. LC-MS/MS Analysis
4.6. Statistical Analysis Methods
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Source | Season (No. of Samples) | Salmonella | E. coli | Enterococcus | |||
---|---|---|---|---|---|---|---|
% of Positive Samples (No. of Isolates) | No. of AR Isolates (No. of MDR Isolates) 1 | % of Positive Samples (No. of Isolates) | No. of AR Isolates (No. of MDR Isolates) 1 | % of Positive Samples (No. of Isolates) | No. of AR Isolates (No. of MDR Isolates) 1 | ||
Surface water | 2017 fall (43) | 72.1 (78) | 27 (27) | 100 (43) | 3 (0) | 100 (43) | 43 (2) |
2018 winter (41) | 48.8 (57) | 0 (0) | 100 (41) | 4 (2) | 97.6 (40) | 40 (4) | |
2018 spring (42) | 59.5 (74) | 2 (0) | 100 (42) | 2 (1) | 100 (42) | 42 (1) | |
2018 summer (44) | 93.2 (94) | 0 (0) | 100 (44) | 2 (1) | 100 (44) | 44 (1) | |
Influent | 2017 fall (3) | 100.0 (5) | 2 (0) | 100.0 (3) | 2 (2) | 100 (3) | 3 (0) |
2018 winter (3) | 100.0 (5) | 2 (0) | 100.0 (3) | 0 (0) | 100 (3) | 3 (1) | |
2018 spring (3) | 100.0 (7) | 2 (0) | 100 (3) | 0 (0) | 100 (3) | 3 (1) | |
2018 summer (3) | 100.0 (6) | 0 (0) | 100 (3) | 0 (0) | 100 (3) | 3 (0) | |
Effluent | 2017 fall (3) | 0 (0) | 0 (0) | 66.7 (2) | 0 (0) | 100 (3) | 3 (1) |
2018 winter (2) | 0 (0) | 0 (0) | 100.0 (2) | 1 (1) | 100 (2) | 2 (0) | |
2018 spring (3) | 0 (0) | 0 (0) | 100 (3) | 1 (0) | 100 (3) | 3 (1) | |
2018 summer (3) | 33.3 (2) | 0 (0) | 66.7 (2) | 1 (1) | 66.7 (2) | 2 (1) |
Season | Source (No. of Samples) | Organisms | No. of β-Lactamase-Positive Enterobacteriaceae | No. of ESBL-Producing Enterobacteriaceae 1 | No. of CRE 1 |
---|---|---|---|---|---|
2017 fall | water (42) | Escherichia coli | 3 | 2 | 0 |
influent (3) | Enterobacter spp. | 2 | 0 | 1 | |
effluent (3) | Escherichia coli | 1 | 1 | 0 | |
2018 winter | water (42) | Escherichia coli | 1 | 1 | 0 |
Serratia fonticola | 19 | 19 | 2 | ||
influent (3) | Citrobacter freundii | 1 | 0 | 0 | |
Escherichia coli | 2 | 1 | 0 | ||
effluent (3) | Enterobacter asburiae | 1 | 0 | 1 | |
2018 spring | water (41) | Escherichia coli | 3 | 2 | 0 |
Klebsiella oxytoca | 1 | 0 | 0 | ||
Klebsiella pneumoniae | 3 | 2 | 1 | ||
Serratia fonticola | 40 | 1 | 2 | ||
influent (3) | Escherichia coli | 1 | 1 | 0 | |
Kluyvera ascorbata | 1 | 0 | 0 | ||
Kluyvera cryocrescens | 2 | 2 | 0 | ||
effluent (3) | Citrobacter braakii/freundii | 1 | 0 | 0 | |
Klebsiella pneumoniae | 3 | 2 | 0 | ||
2018 summer | water (43) | Serratia fonticola | 38 | 0 | 2 |
Enterobacter cloacae complex | 7 | 0 | 7 | ||
Escherichia coli | 4 | 3 | 0 | ||
Klebsiella pneumoniae | 1 | 1 | 0 | ||
influent (3) | Enterobacter asburiae | 1 | 0 | 0 | |
Enterobacter cloacae complex | 1 | 0 | 0 | ||
Escherichia coli | 3 | 3 | 0 | ||
Klebsiella pneumoniae | 3 | 1 | 0 | ||
Kluyvera cryocrescens | 1 | 0 | 0 | ||
effluent (3) | Enterobacter cloacae complex | 2 | 0 | 2 | |
Klebsiella pneumoniae | 1 | 0 | 0 |
Season | Source (No. of Samples) | ermB | tetB | blaKPC | ||||||
No. of Positive Samples (%) | Maximum (Copies/mL) | Average (Copies/mL) | No. of Positive Samples (%) | Maximum (Copies/mL) | Average (Copies/mL) | No. of Positive Samples (%) | Maximum (Copies/mL) | Average (Copies/mL) | ||
2017 fall | surface water (38) | 23 (60.5) | 1533.8 | 57.2 | 10 (26.3) | 127.0 | 4.0 | 9 (23.7) | 13.5 | 1.6 |
influent (3) | 3 (100) | 189,008.9 | 125,110.9 | 3 (100) | 4591.6 | 2524.8 | 3 (100) | 299,148.9 | 153,214.4 | |
effluent (3) | 3 (100) | 33,052.9 | 11,394.3 | 3 (100) | 909.1 | 311.7 | 3 (100) | 31,100.5 | 11,630.9 | |
2018 winter | surface water (38) | 8 (21.6) | 355.0 | 11.3 | 2 (5.6) | 0.7 | 0.0 | 5 (13.5) | 49.9 | 2.0 |
influent (3) | 3 (100) | 338,120.7 | 213,492.4 | 3 (100) | 15,694.5 | 8238.5 | 3 (100) | 362,358.8 | 142,942.9 | |
effluent (3) | 3 (100) | 277.9 | 182.7 | 2 (66.7) | 5.3 | 2.1 | 3 (100) | 197.5 | 115.7 | |
2018 spring | surface water (34) | 8 (23.5) | 41.0 | 1.9 | 1 (2.9) | 1.6 | 0.0 | 2 (5.9) | 76.2 | 2.4 |
influent (3) | 3 (100) | 98,933.2 | 46,165.2 | 3 (100) | 3219.8 | 1216.4 | 3 (100) | 73,007.5 | 48,650.3 | |
2018 summer | surface water (40) | 11 (27.5) | 347.5 | 11.9 | 2 (5.0) | 1.0 | 0.1 | 7 (17.5) | 377.5 | 9.8 |
Season | Source (No. of Samples) | blaSHV | qnrS | blaCTX-M | ||||||
No. of positive samples (%) | Maximum (copies/mL) | Average (copies/mL) | No. of positive samples (%) | Maximum (copies/mL) | Average (copies/mL) | No. of positive samples (%) | Maximum (copies/mL) | Average (copies/mL) | ||
2017 fall | surface water (38) | 9 (23.7) | 325.0 | 10.7 | 8 (21.1) | 308.4 | 12.5 | 3 (7.9) | 455.2 | 15.9 |
influent (3) | 3 (100) | 37,087.9 | 24,498.7 | 3 (100) | 624,275.8 | 418,281.0 | 3 (100) | 6,740.0 | 2633.0 | |
effluent (3) | 3 (100) | 7423.3 | 2637.1 | 3 (100) | 138,990.3 | 50,771.0 | 2 (66.7) | 1499.5 | 502.4 | |
2018 winter | surface water (38) | 2 (5.4) | 2.0 | 0.1 | 8 (21.1) | 582.6 | 19.5 | 0 (0.0) | 0.0 | 0.0 |
influent (3) | 3 (100) | 40,126.5 | 26,100.6 | 3 (100) | 605,863.5 | 322,060.7 | 3 (100) | 26,050.7 | 13,449.5 | |
effluent (3) | 3 (100) | 37.1 | 16.6 | 3 (100) | 1784.4 | 942.9 | 1 (33.3) | 51.8 | 17.3 | |
2018 spring | surface water (34) | 1 (2.9) | 2.0 | 0.1 | 3 (9.4) | 122.4 | 4.6 | 0 (0.0) | 0.0 | 0.0 |
influent (3) | 3 (100) | 34,286.7 | 13,942.2 | 3 (100) | 291,963.4 | 137,383.9 | 3 (100) | 26,165.9 | 9461.5 | |
2018 summer | surface water (40) | 2 (5.0) | 7.7 | 0.2 | 8 (20.0) | 703.0 | 21.5 | 0 (0.0) | 0.0 | 0.0 |
Season | Source (No. of Samples) | Antibiotics 1 | |||||||||||||
AMX | AMP | AZI | AXO | TAZ | TIO | CIP | DAP | ERY | GEN | KAN | LIN | LNZ | |||
2017 fall | water (43) | maximum concentrations (ng/L) | 45.2 | 44.6 | 106.6 | 0.0 | 10.9 | 34.9 | 13.5 | 0.0 | 26.1 | 0.0 | 0.0 | 39.9 | 37.7 |
average concentrations (ng/L) | 2.1 | 4.4 | 3.9 | 0.0 | 0.3 | 1.4 | 1.6 | 0.0 | 1.1 | 0.0 | 0.0 | 1.3 | 2.4 | ||
no. of times detected | 14 | 15 | 7 | 0 | 1 | 21 | 28 | 0 | 19 | 0 | 0 | 14 | 9 | ||
wastewater (6) | maximum concentrations (ng/L) | 2.1 | 52.8 | 120.6 | 0.0 | 0.0 | 38.0 | 123.7 | 16.3 | 20.8 | 0.0 | 0.0 | 1.3 | 0.6 | |
average concentrations (ng/L) | 0.4 | 13.9 | 29.2 | 0.0 | 0.0 | 6.7 | 49.8 | 2.7 | 11.2 | 0.0 | 0.0 | 0.6 | 0.2 | ||
no. of times detected | 1 | 5 | 6 | 0 | 0 | 3 | 6 | 1 | 5 | 0 | 0 | 6 | 3 | ||
2018 winter | water (30) | maximum concentrations (ng/L) | 14.6 | 41.0 | 0.4 | 6.6 | 152.3 | 19.9 | 1.8 | 1472.8 | 0.1 | 122.0 | 0.1 | 3.8 | 0.1 |
average concentrations (ng/L) | 1.8 | 4.5 | 0.0 | 1.0 | 11.4 | 3.4 | 0.1 | 51.1 | 0.0 | 16.5 | 0.0 | 0.1 | 0.0 | ||
no. of times detected | 8 | 6 | 2 | 6 | 4 | 11 | 8 | 5 | 4 | 13 | 1 | 3 | 3 | ||
wastewater (6) | maximum concentrations (ng/L) | 91.0 | 18.3 | 22.9 | 21.9 | 686.0 | 37.8 | 4.6 | 1292.6 | 86.3 | 199.6 | 0.0 | 4.6 | 1.5 | |
average concentrations (ng/L) | 15.2 | 3.1 | 6.8 | 3.6 | 162.0 | 15.5 | 0.8 | 237.1 | 23.0 | 48.1 | 0.0 | 1.4 | 0.3 | ||
no. of times detected | 1 | 1 | 3 | 1 | 2 | 3 | 1 | 2 | 3 | 2 | 0 | 3 | 2 | ||
2018 spring | water (39) | maximum concentrations (ng/L) | 67.6 | 293.3 | 31.9 | 750.5 | 524.3 | 19.8 | 14.9 | 167.8 | 21.9 | 37.9 | 12.0 | 259.7 | 13.7 |
average concentrations (ng/L) | 3.8 | 15.4 | 0.9 | 49.1 | 17.3 | 3.4 | 3.1 | 10.8 | 1.4 | 1.0 | 0.3 | 19.4 | 0.9 | ||
no. of times detected | 12 | 14 | 19 | 6 | 3 | 17 | 19 | 7 | 14 | 1 | 1 | 12 | 18 | ||
wastewater (6) | maximum concentrations (ng/L) | 6.9 | 216.9 | 46.7 | 0.0 | 0.0 | 14.7 | 67.1 | 0.0 | 113.2 | 0.0 | 0.0 | 59.0 | 4.5 | |
average concentrations (ng/L) | 1.5 | 74.9 | 18.8 | 0.0 | 0.0 | 2.5 | 30.4 | 0.0 | 36.6 | 0.0 | 0.0 | 9.8 | 2.0 | ||
no. of times detected | 2 | 4 | 5 | 0 | 0 | 1 | 4 | 0 | 3 | 0 | 0 | 1 | 4 | ||
2018 summer | water (39) | maximum concentrations (ng/L) | 39.9 | 4.6 | 26.9 | 8.6 | 23.8 | 12.7 | 13.6 | 2.9 | 66.5 | 23.7 | 24.9 | 0.1 | 27.3 |
average concentrations (ng/L) | 12.6 | 0.6 | 6.3 | 0.5 | 1.8 | 1.0 | 1.9 | 0.3 | 13.2 | 3.0 | 1.9 | 0.0 | 5.8 | ||
no. of times detected | 31 | 8 | 10 | 6 | 3 | 9 | 11 | 7 | 20 | 5 | 3 | 1 | 10 | ||
wastewater (6) | maximum concentrations (ng/L) | 43.6 | 4.3 | 326.5 | 0.0 | 31.0 | 25.7 | 29.7 | 19.1 | 3550.6 | 23.8 | 75.7 | 0.0 | 69.2 | |
average concentrations (ng/L) | 10.9 | 0.7 | 121.6 | 0.0 | 9.4 | 6.5 | 8.9 | 3.2 | 978.7 | 4.0 | 23.1 | 0.0 | 40.0 | ||
no. of times detected | 2 | 1 | 3 | 0 | 2 | 2 | 2 | 1 | 3 | 1 | 3 | 0 | 6 | ||
Season | Source (No. of Samples) | Antibiotics 1 | |||||||||||||
MRP | MET | NAL | OXA | PEN | SMX | FIS | STR | TGC | TMP | TET | TYL | VAN | |||
2017 fall | water (43) | maximum concentrations (ng/L) | 19.6 | 31.5 | 13.6 | 80.9 | 40.9 | 66.7 | 25.4 | 44.9 | 0.0 | 40.9 | 0.0 | 22.1 | 0.0 |
average concentrations (ng/L) | 0.9 | 2.1 | 0.6 | 10.1 | 2.4 | 3.2 | 1.3 | 6.4 | 0.0 | 2.9 | 0.0 | 1.4 | 0.0 | ||
no. of times detected | 10 | 14 | 9 | 12 | 13 | 25 | 16 | 16 | 0 | 42 | 0 | 18 | 0 | ||
wastewater (6) | maximum concentrations (ng/L) | 0.6 | 6.2 | 14.3 | 163.3 | 26.8 | 173.5 | 43.5 | 0.0 | 0.0 | 70.7 | 0.0 | 2.0 | 0.0 | |
average concentrations (ng/L) | 0.1 | 1.6 | 4.1 | 37.0 | 5.4 | 72.6 | 10.0 | 0.0 | 0.0 | 29.2 | 0.0 | 0.6 | 0.0 | ||
no. of times detected | 1 | 2 | 3 | 2 | 3 | 6 | 4 | 0 | 0 | 6 | 0 | 3 | 0 | ||
2018 winter | water (30) | maximum concentrations (ng/L) | 3.9 | 0.6 | 0.6 | 502.6 | 0.4 | 4.0 | 0.1 | 26.5 | 0.0 | 0.7 | 0.3 | 0.8 | 0.2 |
average concentrations (ng/L) | 0.3 | 0.0 | 0.0 | 17.0 | 0.0 | 0.2 | 0.0 | 3.5 | 0.0 | 0.2 | 0.0 | 0.2 | 0.0 | ||
no. of times detected | 6 | 6 | 2 | 2 | 1 | 7 | 10 | 5 | 0 | 20 | 4 | 20 | 1 | ||
wastewater (6) | maximum concentrations (ng/L) | 0.0 | 2.1 | 0.2 | 10.6 | 0.0 | 35.0 | 0.0 | 28.2 | 0.0 | 91.5 | 2.8 | 91.6 | 0.0 | |
average concentrations (ng/L) | 0.0 | 0.4 | 0.0 | 1.8 | 0.0 | 18.5 | 0.0 | 9.2 | 0.0 | 16.1 | 1.1 | 26.1 | 0.0 | ||
no. of times detected | 0 | 1 | 1 | 1 | 0 | 6 | 0 | 2 | 0 | 4 | 4 | 6 | 0 | ||
2018 spring | water (39) | maximum concentrations (ng/L) | 220.7 | 50.0 | 13.7 | 593.2 | 19.7 | 29.0 | 60.5 | 159.3 | 46.5 | 16.6 | 44.8 | 63.6 | 238.0 |
average concentrations (ng/L) | 8.1 | 4.3 | 0.4 | 23.6 | 3.9 | 1.2 | 4.7 | 6.9 | 3.5 | 4.0 | 15.8 | 6.0 | 18.4 | ||
no. of times detected | 13 | 17 | 2 | 5 | 17 | 9 | 12 | 9 | 5 | 36 | 23 | 20 | 8 | ||
wastewater (6) | maximum concentrations (ng/L) | 11.8 | 42.0 | 148.0 | 0.0 | 99.7 | 362.3 | 85.8 | 256.7 | 288.4 | 168.9 | 490.0 | 12.8 | 262.8 | |
average concentrations (ng/L) | 2.7 | 8.2 | 25.8 | 0.0 | 28.3 | 170.1 | 23.0 | 62.9 | 84.9 | 100.1 | 173.5 | 3.3 | 112.1 | ||
no. of times detected | 2 | 2 | 4 | 0 | 4 | 6 | 4 | 2 | 3 | 6 | 5 | 3 | 3 | ||
2018 summer | water (39) | maximum concentrations (ng/L) | 9.9 | 21.6 | 81.8 | 0.0 | 23.8 | 98.4 | 2.8 | 0.0 | 0.0 | 87.5 | 0.2 | 24.5 | 0.0 |
average concentrations (ng/L) | 0.7 | 2.2 | 4.5 | 0.0 | 3.7 | 11.6 | 0.5 | 0.0 | 0.0 | 19.3 | 0.0 | 9.8 | 0.0 | ||
no. of times detected | 4 | 12 | 4 | 0 | 12 | 32 | 11 | 0 | 0 | 37 | 1 | 33 | 0 | ||
wastewater (6) | maximum concentrations (ng/L) | 31.8 | 28.2 | 328.5 | 0.0 | 0.0 | 2193.5 | 19.0 | 0.0 | 0.0 | 5777.0 | 20.9 | 134.0 | 0.0 | |
average concentrations (ng/L) | 5.3 | 4.7 | 113.8 | 0.0 | 0.0 | 909.6 | 3.2 | 0.0 | 0.0 | 1228.0 | 3.7 | 55.2 | 0.0 | ||
no. of times detected | 1 | 1 | 4 | 0 | 0 | 6 | 1 | 0 | 0 | 6 | 2 | 6 | 0 |
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Cho, S.; Hiott, L.M.; Read, Q.D.; Damashek, J.; Westrich, J.; Edwards, M.; Seim, R.F.; Glinski, D.A.; Bateman McDonald, J.M.; Ottesen, E.A.; et al. Distribution of Antibiotic Resistance in a Mixed-Use Watershed and the Impact of Wastewater Treatment Plants on Antibiotic Resistance in Surface Water. Antibiotics 2023, 12, 1586. https://doi.org/10.3390/antibiotics12111586
Cho S, Hiott LM, Read QD, Damashek J, Westrich J, Edwards M, Seim RF, Glinski DA, Bateman McDonald JM, Ottesen EA, et al. Distribution of Antibiotic Resistance in a Mixed-Use Watershed and the Impact of Wastewater Treatment Plants on Antibiotic Resistance in Surface Water. Antibiotics. 2023; 12(11):1586. https://doi.org/10.3390/antibiotics12111586
Chicago/Turabian StyleCho, Sohyun, Lari M. Hiott, Quentin D. Read, Julian Damashek, Jason Westrich, Martinique Edwards, Roland F. Seim, Donna A. Glinski, Jacob M. Bateman McDonald, Elizabeth A. Ottesen, and et al. 2023. "Distribution of Antibiotic Resistance in a Mixed-Use Watershed and the Impact of Wastewater Treatment Plants on Antibiotic Resistance in Surface Water" Antibiotics 12, no. 11: 1586. https://doi.org/10.3390/antibiotics12111586
APA StyleCho, S., Hiott, L. M., Read, Q. D., Damashek, J., Westrich, J., Edwards, M., Seim, R. F., Glinski, D. A., Bateman McDonald, J. M., Ottesen, E. A., Lipp, E. K., Henderson, W. M., Jackson, C. R., & Frye, J. G. (2023). Distribution of Antibiotic Resistance in a Mixed-Use Watershed and the Impact of Wastewater Treatment Plants on Antibiotic Resistance in Surface Water. Antibiotics, 12(11), 1586. https://doi.org/10.3390/antibiotics12111586