Occurrence and Antimicrobial Resistance Traits of Escherichia coli from Wild Birds and Rodents in Singapore
Abstract
:1. Introduction
2. Materials and Methods
2.1. Sample Collection, Isolation and Identification
2.2. Antimicrobial Susceptibility Testing of E. coli Isolates
2.3. Extended Spectrum Beta-Lactamases (ESBL) Testing for E. coli Isolates
2.4. Genotypic Characterisation by Whole Genome Sequencing
2.5. Statistical Analysis
3. Results
3.1. Occurrence of E. coli in Wild Birds and Rodents
3.2. Antimicrobial Resistance in E. coli Isolated from Wild Birds and Rodents
3.3. Distribution of Resistance Genes in Eight MDR E. coli Isolates from Wild Birds and Rodents
3.4. Comparison between Phenotypic and Genotypic Characteristics of MDR E. coli Isolates
4. Discussion
5. Conclusions
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
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Sample ID | Sample Type | Source | AK30 | AMC30 | AMP10 | CRO30 | C30 | CIP5 | CN10 | MEM10 | NA30 | NOR10 | SXT25 | TE30 |
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
C1776# | Wild Bird | Crow | S | S | R | S | R | R | S | S | R | R | R | R |
C1775 | Wild Bird | Myna | S | S | R | S | S | S | S | S | S | S | S | S |
8657-0407-0411-1 | Rodent | Rodent | S | S | S | S | S | S | S | S | S | S | S | S |
8657-0948-0411 | Rodent | Rodent | S | S | I | S | S | S | S | S | S | S | S | S |
8645-0135# | Rodent | Rodent | S | S | R | S | R | S | S | S | S | S | R | R |
C1797# | Wild Bird | Crested Goshawk | S | S | I | S | R | R | S | S | R | R | S | R |
C1809-1 | Wild Bird | Hooded Pitta | S | S | I | S | S | S | S | S | S | S | S | S |
C1789 | Wild Bird | Crow | S | S | I | S | S | S | S | S | S | S | S | S |
C1798 | Wild Bird | Black-naped oriole | S | S | I | S | S | S | S | S | S | S | S | S |
HHK-M04-060417-1 | Rodent | Rodent | S | S | S | S | S | S | S | S | S | S | S | S |
HHK-M04-060417-3 | Rodent | Rodent | S | S | I | S | S | S | S | S | S | S | S | S |
8642-0159-0410-1 | Rodent | Rodent | S | S | S | S | S | S | S | S | S | S | S | S |
C1742# | Wild Bird | Yellow Bittern | S | I | R | S | R | S | S | S | S | S | S | R |
C1779 | Wild Bird | Crow | S | S | S | S | S | S | S | S | S | S | S | S |
C1805-1# | Wild Bird | Crow | S | I | R | S | R | S | S | S | S | S | S | R |
8657-0146-0224 | Rodent | Rodent | S | S | S | S | S | S | S | S | S | S | S | S |
NHA-M02-230117 | Rodent | Rodent | S | S | S | S | S | S | S | S | S | S | S | S |
8657-0258-0411-1 | Rodent | Rodent | S | S | S | S | S | S | S | S | S | S | S | S |
7574-0224-0224 | Rodent | Rodent | S | S | I | S | S | S | S | S | S | S | S | S |
C1802-1 | Wild Bird | Crow | S | S | S | S | S | S | R | S | S | S | S | R |
8646-0251-0301 | Rodent | Rodent | S | S | I | S | S | S | S | S | S | S | S | S |
HHK-M05-160317 | Rodent | Rodent | S | S | S | S | S | S | S | S | S | S | S | S |
C1743E | Wild Bird | Black Bittern | S | S | S | S | S | S | S | S | S | S | S | S |
C1781 | Wild Bird | Black Bittern | S | S | I | S | S | S | S | S | S | S | S | S |
HHK-M07-060417-1 | Rodent | Rodent | S | I | R | S | S | S | S | S | S | S | S | R |
C1806-1 | Wild Bird | Pied Fantail | S | S | S | S | S | S | S | S | S | S | S | S |
C1736 | Wild Bird | Brahmin Kite | S | S | S | S | S | S | S | S | S | S | S | S |
8645-0205-0411-1 | Rodent | Rodent | S | S | S | S | S | S | S | S | S | S | S | S |
C1795 | Wild Bird | Sparrow Hawk | S | S | I | S | S | S | S | S | R | S | S | S |
C1794 | Wild Bird | Grey Heron | S | I | R | S | S | S | S | S | I | S | S | R |
NRS-M02-150317 | Rodent | Rodent | S | S | S | S | S | S | S | S | S | S | S | S |
C1783 | Wild Bird | Scops Owl | S | S | S | S | S | S | S | S | S | S | S | S |
C1770 | Wild Bird | Myna | S | S | S | S | S | S | S | S | S | S | S | R |
C1758# | Wild Bird | Black Bittern | S | I | R | S | S | S | S | S | S | S | R | R |
C1757 | Wild Bird | Yellow Bittern | S | S | I | S | S | S | S | S | S | S | S | S |
C1750 | Wild Bird | Sparrow Hawk | S | I | R | S | S | S | S | S | S | S | S | S |
C1737 | Wild Bird | Crow | S | S | I | S | S | S | S | S | S | S | S | S |
C1740 | Wild Bird | Crow | S | R | R | S | S | S | S | S | S | S | S | S |
C1803-2 | Wild Bird | Crow | S | S | I | S | S | S | S | S | S | S | S | S |
8656-0339-0224 | Rodent | Rodent | S | S | S | S | S | S | S | S | S | S | S | S |
TAH-M01-210317 | Rodent | Rodent | S | S | S | S | S | S | S | S | R | S | S | S |
HHK-M04-060417-1A | Rodent | Rodent | S | S | S | S | S | S | S | S | S | S | S | S |
8655-0114# | Rodent | Rodent | S | R | R | S | S | R | S | S | R | R | S | R |
C1738 | Wild Bird | Crow | S | S | I | S | S | S | S | S | S | S | S | S |
C1722# | Wild Bird | Crow | S | R | R | R | R | I | R | S | R | S | R | R |
HHK-M06-060417-1 | Rodent | Rodent | S | S | S | S | S | S | S | S | S | S | S | S |
Types of Samples | Percentage of Samples Positive for E. coli | Sample Name (Scientific Name) | No. of E. coli Isolates |
---|---|---|---|
Wild Birds | 27.1% (26/96) [95% CI: 19.2–36.7%] | Crow (Corvus spp.) | Ten |
Black Bittern (Ixobrychus flavicollis) | Three | ||
Myna (Acridotheres spp.) | Two | ||
Sparrow Hawk (Accipiter spp.) | Two | ||
Yellow Bittern (Ixobrychus sinensis) | Two | ||
Black-naped oriole (Oriolus chinensis) | One | ||
Brahminy Kite (Haliastur indus) | One | ||
Crested Goshawk (Accipiter trivirgatus) | One | ||
Grey Heron (Ardea cinerea) | One | ||
Hooded Pitta (Pitta sordida) | One | ||
Pied Fantail (Rhipidura javanica) | One | ||
Scops Owl (Otus spp.) | One | ||
Rodents | 14.8% (20/135) [95% CI: 9.8–21.8%] | Black Rat/Brown Rat/House Mouse (Rattus rattus/Rattus norvegicus/Mus musculus) | 20 |
Wild Birds | Rodents | Z-Score |
---|---|---|
80.8% (21/26) [95% CI: 62.1–91.5%] | 40.0% (8/20) [95% CI: 21.9–61.3%] | 2.8 (p < 0.05) |
Antimicrobial Class | Antimicrobial Agent Tested in the Study | Percentage of Isolates Showing Resistant Phenotype (n) | |
---|---|---|---|
Wild Birds (26) | Rodents (20) | ||
Penicillins | Ampicillin | 73.1% (19/26) | 35.0% (7/20) |
Tetracyclines | Tetracycline | 34.6% (9/26) | 15.0% (3/20) |
Beta-lactam/beta-lactamase Inhibitor Combinations | Amoxicillin/Clavulanic acid | 26.9% (7/26) | 10.0% (2/20) |
Quinolones | Nalidixic acid (Quinolone) | 19.2% (5/26) | 10.0% (2/20) |
Phenicols | Chloramphenicol | 19.2% (5/26) | 5.0% (1/20) |
Folate Pathway Synthesis | Sulphamethoxazole/Trimethoprim | 11.5% (3/26) | 5.0% (1/20) |
Quinolones | Ciprofloxacin (Fluoroquinolone) | 11.5% (3/26) | 5.0% (1/20) |
Quinolones | Norfloxacin (Fluoroquinolone) | 7.7% (2/26) | 5.0% (1/20) |
Aminoglycosides | Gentamicin | 7.7% (2/26) | 0.0% |
Third Generation Cephalosporins | Ceftriaxone | 3.8% (1/26) | 0.0% |
Aminoglycosides | Amikacin | 0.0% | 0.0% |
Carbapenems | Meropenem | 0.0% | 0.0% |
Isolate ID | Sample Source | Sample Description | Resistance Genes (n) | Aminoglycoside | ESBL | Quinolone | Fosfomycin | MLS a | Phenicol | Sulphonamide | Tetracycline | Trimethoprim | Chromosomal Point Mutations |
---|---|---|---|---|---|---|---|---|---|---|---|---|---|
C1722 | Wild bird | Crow | 17 | aac(3)-IV, aadA2, aph(3′)-Ia, aph(3″)-Ib, aph(4)-Ia, aph(6)-Id, | blaCTX-M-65, blaTEM-1B | - | fosA3 | mdf(A) | cmlA1, floR | sul2, sul3 | tet(A), tet(X) | dfrA12 | gyrA (Ser83Leu) |
C1742 | Wild bird | Yellow Bittern | 7 | aph(3′)-Ia | blaTEM-176 | qnrS1 | - | mdf(A) | floR | - | tet(A) | dfrA14 | - |
C1758 | Wild bird | Black Bittern | 4 | aph(6)-Id | qnrS1 | - | mdf(A) | - | - | tet(A) | - | - | |
C1776 | Wild bird | Crow | 11 | aadA1, aadA2, aph(3″)-Ib, aph(6)-Id | blaTEM-1B | oqxB | - | mdf(A), mph(A) | cmlA1 | sul3 | tet(A) | - | gyrA, (Ser83Leu), gyrA(Asp87Asn) & parC (Ser80Ile). |
C1797 | Wild bird | Crested Goshawk | 3 | - | - | - | - | mdf(A) | catA1 | - | tet(B) | - | gyrA (Ser83Leu), gyrA(Asp87Asn) & parC (Ser80Ile). |
C1805-1 | Wild bird | Crow | 7 | aadA1 | blaTEM-1B | qnrS1 | - | mdf(A) | floR | sul3 | tet(A) | - | - |
8645-0135 | Rodent | Rodent | 11 | aadA1, aadA2 | blaTEM-1B | qnrS1 | - | mdf(A) | cmlA1, floR | sul2, sul3 | tet(A) | dfrA12 | - |
8655-0114 | Rodent | Rodent | 1 | - | - | - | - | mdf(A) | - | - | - | - | - |
Isolate ID | Sample Source | Sample Description | Beta-lactams | Quinolones | Phenicols | Tetracyclines | ||||
---|---|---|---|---|---|---|---|---|---|---|
Phenotype | Genotype | Phenotype | Genotype | Phenotype | Genotype | Phenotype | Genotype | |||
C1722 | Wild bird | Crow | AMC *, AMP, CRO | blaCTX-M-65, blaTEM-1B | CIP, NA | Chromosomal mutations gyrA (Ser83Leu) | C | cmlA1, floR | TE | tet(A), tet(X) |
C1742 | Wild bird | Yellow Bittern | AMC *, AMP | blaTEM-176 | - | qnrS1 | C | floR | TE | tet(A) |
C1758 | Wild bird | Black Bittern | AMC *, AMP | - | - | qnrS1 | - | - | TE | tet(A) |
C1776 | Wild bird | Crow | AMP | blaTEM-1B | CIP, NA, NOR | oqxB, Chromosomal mutations gyrA (Ser83Leu) gyrA (Asp87Asn) & parC (Ser80Ile) | C | cmlA1 | TE | tet(A) |
C1797 | Wild bird | Crested Goshawk | AMP | - | CIP, NA, NOR | Chromosomal mutations gyrA (Ser83Leu) gyrA (Asp87Asn) & parC (Ser80Ile) | C | catA1 | TE | tet(B) |
C1805_1 | Wild bird | Crow | AMP, AMC * | blaTEM-1B | - | qnrS1 | C | floR | TE | tet(A) |
8645_0135 | Rodent | Rodent | AMP | blaTEM-1B | - | qnrS1 | C | cmlA1, floR | TE | tet(A) |
8655_0114 | Rodent | Rodent | AMC *, AMP | - | CIP, NA, NOR | - | - | - | TE | - |
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Ong, K.H.; Khor, W.C.; Quek, J.Y.; Low, Z.X.; Arivalan, S.; Humaidi, M.; Chua, C.; Seow, K.L.G.; Guo, S.; Tay, M.Y.F.; et al. Occurrence and Antimicrobial Resistance Traits of Escherichia coli from Wild Birds and Rodents in Singapore. Int. J. Environ. Res. Public Health 2020, 17, 5606. https://doi.org/10.3390/ijerph17155606
Ong KH, Khor WC, Quek JY, Low ZX, Arivalan S, Humaidi M, Chua C, Seow KLG, Guo S, Tay MYF, et al. Occurrence and Antimicrobial Resistance Traits of Escherichia coli from Wild Birds and Rodents in Singapore. International Journal of Environmental Research and Public Health. 2020; 17(15):5606. https://doi.org/10.3390/ijerph17155606
Chicago/Turabian StyleOng, Kar Hui, Wei Ching Khor, Jing Yi Quek, Zi Xi Low, Sathish Arivalan, Mahathir Humaidi, Cliff Chua, Kelyn L. G. Seow, Siyao Guo, Moon Y. F. Tay, and et al. 2020. "Occurrence and Antimicrobial Resistance Traits of Escherichia coli from Wild Birds and Rodents in Singapore" International Journal of Environmental Research and Public Health 17, no. 15: 5606. https://doi.org/10.3390/ijerph17155606