Resistance Profiling and Molecular Characterization of Extended-Spectrum/Plasmid-Mediated AmpC β-Lactamase-Producing Escherichia coli Isolated from Healthy Broiler Chickens in South Korea
Abstract
:1. Introduction
2. Materials and Methods
2.1. Collection of Samples and Isolation of E. coli
2.2. Antimicrobial Susceptibility Testing
2.3. Detection of Resistance Genes
2.4. Conjugation Experiment
2.5. Molecular Characterization of ESBL/pAmpC-Producing E. coli
3. Results
3.1. Antimicrobial Resistance of Indicator E. coli
3.2. Distribution of ESBL/pAmpC-Producing E. coli
3.3. Molecular Characteristics of ESBL/pAmpC-Producing E. coli
4. Discussion
Supplementary Materials
Author Contributions
Funding
Conflicts of Interest
References
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Antimicrobials | Distribution (%) of MICs (µg/mL) | MIC50 | MIC90 | MIC | Resistance | ||||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
≤0.12 | 0.25 | 0.5 | 1 | 2 | 4 | 8 | 16 | 32 | 64 | 128 | 256 | ≥512 | Range | (%) | |||
Amoxicillin/clavulanic acid | 3.6 | 10.8 | 69.9 | 12.3 | 3.3 | 8 | 16 | 2–32 | 3.3 | ||||||||
Ampicillin | 4.8 | 8.1 | 0.6 | 86.4 | 64 | 64 | 2–64 | 86.4 | |||||||||
Cefepime | 87.3 | 1.8 | 2.4 | 0.6 | 3 | 3.6 | 1.2 | 0.25 | 1 | 0.25–16 | 1.2 | ||||||
Cefoxitin | 7.2 | 48.2 | 35.2 | 5.7 | 3.6 | 1 | 4 | 1–32 | 3.6 | ||||||||
Ceftazidime | 89.5 | 1.5 | 2.4 | 3 | 3.6 | 1 | 2 | 1–32 | 3.6 | ||||||||
Ceftiofur | 75 | 10.5 | 0.3 | 14.2 | 0.5 | 8 | 0.5–8 | 13.9 | |||||||||
Chloramphenicol | 0.3 | 12.7 | 18.4 | 1.5 | 2.1 | 65.1 | 64 | 64 | 2–64 | 67.2 | |||||||
Ciprofloxacin | 1.8 | 11.7 | 4.8 | 1.5 | 1.8 | 2.7 | 43.7 | 31.9 | 8 | 16 | 0.12–16 | 78.3 | |||||
Colistin | 99.4 | 0.6 | 2 | 2 | 2–8 | 0.6 | |||||||||||
Gentamicin | 70.2 | 3.9 | 0.3 | 2.4 | 3 | 20.2 | 1 | 64 | 1–64 | 25.6 | |||||||
Meropenem | 100 | 0.25 | 0.25 | 0.25–0.25 | 0 | ||||||||||||
Nalidixic Acid | 2.1 | 1.8 | 2.1 | 1.5 | 0.6 | 1.5 | 90.4 | 128 | 128 | 2–128 | 92.5 | ||||||
Streptomycin | 38.3 | 5.4 | 7.5 | 48.8 | 64 | 128 | 16–128 | 61.7 | |||||||||
Sulfisoxazole | 29.8 | 2.1 | 68.1 | 512 | 512 | 16–512 | 68.1 | ||||||||||
Tetracycline | 28.3 | 14.8 | 22.6 | 34.3 | 64 | 128 | 2–128 | 71.7 | |||||||||
Trimethoprim/ | 33.4 | 9.3 | 4.8 | 2.4 | 0.3 | 49.7 | 1 | 4 | 0.12–4 | 49.7 | |||||||
sulfamethoxazole |
No. of Antimicrobials | Total No. of Isolates (%) | Frequent Resistance Pattern (No. of Isolates) |
---|---|---|
0 | 0 (0) | |
1 | 1 (0.3) | NAL (n = 1) |
2 | 18 (5.4) | AMP TET (n = 8) |
3 | 30 (9) | AMP CIP NAL (n = 8) |
4 | 26 (7.8) | AMP CIP NAL TET (n = 9) |
5 | 53 (16) | AMP CHL CIP NAL TET (n = 16) |
6 | 34 (10.2) | AMP CIP GEN NAL STR TET (n = 4) |
7 | 58 (17.5) | AMP CHL CIP NAL STR FIS TET (n = 13) |
8 | 55 (16.6) | AMP CHL CIP NAL STR FIS TET SXT (n = 39) |
9 | 45 (13.6) | AMP CHL CIP GEN NAL STR FIS TET SXT (n = 35) |
10 | 6 (1.8) | AMP XNL CHL CIP GEN NAL STR FIS TET SXT (n = 3) |
11 | 2 (0.6) | AMC AMP FOX CAZ XNL CHL CIP NAL STR FIS TET (n = 1) |
12 | 1 (0.3) | AMC AMP FOX CAZ XNL CHL CIP NAL STR FIS TET SXT (n = 1) |
13 | 3 (0.9) | AMC AMP FOX CAZ XNL CHL CIP COL NAL STR FIS TET SXT (n = 1) |
MDR (≥3 subclass) | 313 (94.3) |
Farm ID | Province | Prevalence (%) (No. of bla-Positive Isolates/ Total No. of Isolates per Farm) | CTX-M-1 | CTX-M-14 | CTX-M-55 | CTX-M-65 | CMY-2 | CTX-M-55+CMY-2 |
---|---|---|---|---|---|---|---|---|
2019-P-A | Chungbuk | 12.5 (1/8) | 1 | |||||
2019-P-C | Gyeongbuk | 25 (2/8) | 1 | 1 | ||||
2019-P-E | Gyeongbuk | 27.3 (3/11) | 1 | 2 | ||||
2019-P-G | Jeonbuk | 10 (1/10) | 1 | |||||
2019-P-I | Jeonbuk | 50 (5/10) | 4 | 1 | ||||
2019-P-K | Jeonbuk | 20 (2/10) | 2 | |||||
2019-P-M | Jeonnam | 10 (1/10) | 1 | |||||
2019-P-N | Chungbuk | 10 (1/10) | 1 | |||||
2019-P-O | Gyeongbuk | 10 (1/10) | 1 | |||||
2019-P-P | Gyeongbuk | 20 (2/10) | 1 | 1 | ||||
2019-P-T | Chungnam | 9.1 (1/11) | 1 | |||||
2019-P-V | Jeonnam | 10 (1/10) | 1 | |||||
2019-P-W | Jeonbuk | 30 (3/10) | 2 | 1 | ||||
2019-P-Y | Jeonbuk | 10 (1/10) | 1 | |||||
2019-P-Z | Chungnam | 20 (2/10) | 1 | 1 | ||||
2019-P-AA | Chungnam | 9.1 (1/11) | 1 | |||||
2019-P-AB | Jeonnam | 10 (1/10) | 1 | |||||
2019-P-AC | Jeonbuk | 40 (4/10) | 1 | 3 | ||||
2019-P-AD | Gyeonggi | 30 (3/10) | 2 | 1 | ||||
2019-P-AE | Jeonnam | 40 (4/10) | 1 | 2 | 1 | |||
2019-P-AF | Jeonbuk | 20 (2/10) | 2 | |||||
2019-P-AG | Jeonbuk | 40 (4/10) | 4 | |||||
Total | 22.4 (46/219) | 4 | 12 | 18 | 2 | 8 | 2 |
Isolates | Farm ID | Provinces | MICs (µg/mL) | bla Gene | PMQR Gene | Non-β Lactam Antibiotic Resistance | Transfer- Ability | Plasmid Type | Phylogenetic Group | Pulsotype | ||
---|---|---|---|---|---|---|---|---|---|---|---|---|
XNL | FOX | CAZ | ||||||||||
A-CF-6 | A | Chungbuk | >8 | 4 | 4 | CTX-M-55 | - | CIP NAL | + | FⅡ | A | P22 |
C-CF-6 | C | Gyeongbuk | >8 | 8 | 2 | CTX-M-1 | qnrS1 | CHL GEN STR FIS TET SXT | + | I1α, FIB, FⅡ | A | P9 |
C-CF-8 | C | Gyeongbuk | >8 | 8 | 4 | CTX-M-55 | qnrS1 | CHL FIS | + | I1α, FⅡ | D | P6 |
E-CF-2 | E | Gyeongbuk | >8 | 32 | 16 | CMY-2 | - | AMC STR FIS TET SXT | - | - | D | P31 |
E-CF-M-5 | E | Gyeongbuk | >8 | >32 | 16 | CMY-2 | mcr-1 | CHL CIP COL NAL STR FIS TET SXT | + | I1α, FⅡ | D | P32 |
E-CF-8 | E | Gyeongbuk | 8 | 8 | ≤1 | CTX-M-14 | - | CHL CIP NAL FIS | + | HI2, Iγ, FⅡ | A | P26 |
G-CF-M-6 | G | Jeonbuk | >8 | >32 | >16 | CMY-2 | - | CHL CIP NAL STR FIS TET SXT | + | I1α | A | P34 |
I-CF-1 | I | Jeonbuk | >8 | 2 | 4 | CTX-M-55 | qnrS1 | TET | + | FⅡ | B1 | P7 |
I-CF-M-2 | I | Jeonbuk | >8 | 4 | ≤1 | CTX-M-14 | - | CIP GEN NAL | - | - | A | P2 |
I-CF-5 | I | Jeonbuk | >8 | 4 | ≤1 | CTX-M-14 | - | CIP GEN NAL | - | - | A | P1 |
I-CF-M-7 | I | Jeonbuk | >8 | 4 | ≤1 | CTX-M-14 | - | CIP GEN NAL | - | - | A | P2 |
I-CF-M-8 | I | Jeonbuk | >8 | 2 | ≤1 | CTX-M-14 | - | CIP GEN NAL | - | - | A | P1 |
K-CF-M-1 | K | Jeonbuk | >8 | >32 | >16 | CMY-2 | - | CHL CIP NAL TET | + | I1α, FIB, FⅡ | D | ND |
K-CF-7 | K | Jeonbuk | >8 | 32 | 16 | CMY-2 | - | CIP NAL | - | - | D | ND |
M-CF-M-3 | M | Jeonnam | >8 | 8 | 8 | CTX-M-55 | - | CIP NAL | - | - | B1 | ND |
N-CF-5 | N | Chungbuk | >8 | >32 | 16 | CTX-M-55, CMY-2 | - | CHL CIP NAL STR FIS | + | K, X4 | D | P27 |
O-CF-4 | O | Gyeongbuk | >8 | 4 | 2 | CTX-M-1 | - | NAL FIS TET | + | I1α | A | P10 |
P-CF-M-2 | P | Gyeongbuk | >8 | 8 | 4 | CTX-M-55 | - | CIP NAL | + | FⅡ | A | P20 |
P-CF-9 | P | Gyeongbuk | >8 | 2 | ≤1 | CTX-M-14 | - | CIP GEN NAL TET | - | - | A | P4 |
T-CF-M-3 | T | Chungbuk | >8 | 4 | 2 | CTX-M-1 | - | CHL CIP NAL FIS TET | + | I1α | B1 | P21 |
V-CF-M-2 | V | Jeonnam | >8 | 4 | 8 | CTX-M-55 | - | CHL CIP NAL STR FIS TET | - | B1 | P11 | |
W-CF-M-5 | W | Jeonbuk | >8 | 4 | 8 | CTX-M-55 | - | CIP GEN NAL TET | + | I1-α, FIB, FⅡ | D | P24 |
W-CF-6 | W | Jeonbuk | >8 | 8 | 8 | CTX-M-55 | - | CHL CIP NAL TET | + | FⅡ | B1 | P14 |
W-CF-M-10 | W | Jeonbuk | >8 | 32 | >16 | CTX-M-55, CMY-2 | - | CHL CIP NAL STR FIS TET SXT | - | B1 | P25 | |
Y-CF-4 | Y | Jeonbuk | >8 | 4 | 8 | CTX-M-55 | qnrS1 | TET | + | FⅡ | B1 | P5 |
Z-CF-M-1 | Z | Chungnam | 8 | >32 | 8 | CMY-2 | - | CHL CIP NAL STR FIS TET | + | K | B1 | P29 |
Z-CF-7 | Z | Chungnam | >8 | 4 | 2 | CTX-M-1 | - | CIP NAL TET | - | B1 | P28 | |
AA-CF-M-2 | AA | Chungnam | >8 | 4 | 4 | CTX-M-55 | - | CIP NAL | + | FIB, FⅡ | B1 | P23 |
AB-CF-M-1 | AB | Jeonbuk | >8 | >32 | 16 | CMY-2 | - | CHL CIP NALSTR FIS TET | + | I1α | D | P33 |
AC-CF-2 | AC | Jeonbuk | >8 | 32 | >16 | CTX-M-55 | - | CHL CIP NAL FIS TET | - | B1 | P13 | |
AC-CF-M-3 | AC | Jeonbuk | >8 | 4 | 4 | CTX-M-55 | - | CHL CIP NAL STR FIS SXT | + | FⅡ | A | P15 |
AC-CF-M-5 | AC | Jeonbuk | >8 | 8 | 16 | CTX-M-55 | - | CHL CIP NAL FIS TET | - | B1 | P13 | |
AC-CF-10 | AC | Jeonbuk | >8 | 2 | ≤1 | CTX-M-14 | - | CIP GEN NAL | - | A | P3 | |
AD-CF-M-2 | AD | Gyeonggi | 8 | 8 | ≤1 | CTX-M-14 | - | CHL CIP GEN NAL FIS TET SXT | + | HI2, I1α | B1 | P18 |
AD-CF-8 | AD | Gyeonggi | 8 | 16 | ≤1 | CTX-M-14 | - | CHL CIP GEN NAL STR FIS TET | + | HI2 | B1 | P16 |
AD-CF-M-10 | AD | Gyeonggi | >8 | 4 | 8 | CTX-M-55 | - | CHL CIP NAL STR FIS TET SXT | - | A | P8 | |
AE-CF-M-1 | AE | Jeonnam | >8 | >32 | 16 | CMY-2 | - | CHL CIP GEN NAL STR FIS TET SXT | + | I1α | B1 | P30 |
AE-CF-4 | AE | Jeonnam | >8 | 2 | ≤1 | CTX-M-14 | - | CIP GEN NAL | - | A | P3 | |
AE-CF-M-9 | AE | Jeonnam | >8 | 8 | ≤1 | CTX-M-65 | qnrS2, aac(6′)-Ib-cr | CHL CIP GEN NAL STR FIS TET SXT | - | B1 | P12 | |
AE-CF-M-10 | AE | Jeonnam | >8 | 8 | 2 | CTX-M-65 | aac(6′)-Ib-cr | CHL CIP GEN NAL STR FIS TET SXT | - | B1 | P12 | |
AF-CF-M-1 | AF | Jeonbuk | 8 | 4 | ≤1 | CTX-M-14 | - | CHL CIP GEN NAL FIS TET SXT | + | HI2 | B1 | ND |
AF-CF-M-4 | AF | Jeonbuk | >8 | 4 | ≤1 | CTX-M-14 | - | CHL CIP GEN NAL FIS TET | + | HI2 | B1 | ND |
AG-CF-M-4 | AG | Jeonbuk | >8 | 8 | 8 | CTX-M-55 | - | CHL CIP NAL STR FIS TET SXT | + | FⅡ | A | P19 |
AG-CF-6 | AG | Jeonbuk | >8 | 4 | 8 | CTX-M-55 | - | CHL CIP NAL STR FIS TET SXT | + | FⅡ | A | P19 |
AG-CF-M-9 | AG | Jeonbuk | >8 | 8 | 8 | CTX-M-55 | - | CHL CIP NAL STR FIS TET SXT | + | FⅡ | A | P19 |
AG-CF-M-10 | AG | Jeonbuk | >8 | 4 | 4 | CTX-M-55 | - | CHL STR FIS TET | + | I1α, FⅡ | B1 | P17 |
Type of bla Gene | No. of Isolates | Self-Transfer | No. of Replicon Type | Genetic Environment | ||||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
I1α | I1α+ FⅡ | I1α + FⅡ + FIB | FⅡ | FⅡ + FIB | HI2 | HI2 + I1α | HI2 + FⅡ + Iγ | K | B/O +K + X4 | Upstream | Downstream | |||||
ISEcp1 | IS26 | IS903 | orf477 | |||||||||||||
CTX-M-1 | 4 | 3 | 2 | - | 1 | - | - | - | - | - | - | - | 3 | - | - | 3 |
CTX-M-14 | 12 | 5 | - | - | - | - | - | 3 | 1 | 1 | - | - | - | - | 5 | - |
CTX-M-55 a | 11 | 9 | - | 1 | - | 8 | - | - | - | - | - | - | - | - | - | 9 |
CTX-M-55 b | 7 | 4 | - | 1 | 1 | 1 | 1 | - | - | - | - | - | 4 | - | - | 4 |
CTX-M-65 | 2 | 0 | - | - | - | - | - | - | - | - | - | - | - | - | - | - |
CMY-2 | 8 | 6 | 3 | 1 | 1 | - | - | - | - | - | 1 | - | 6 | - | - | - |
CTX-M-55+CMY-2 | 2 | 1 | - | - | - | - | - | - | - | - | - | 1 | 1 | - | - | - |
Total | 46 | 28 | 5 | 3 | 3 | 9 | 1 | 3 | 1 | 1 | 1 | 1 | 14 | 0 | 5 | 16 |
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Song, H.-J.; Moon, D.C.; Mechesso, A.F.; Kang, H.Y.; Kim, M.H.; Choi, J.-H.; Kim, S.-J.; Yoon, S.-S.; Lim, S.-K. Resistance Profiling and Molecular Characterization of Extended-Spectrum/Plasmid-Mediated AmpC β-Lactamase-Producing Escherichia coli Isolated from Healthy Broiler Chickens in South Korea. Microorganisms 2020, 8, 1434. https://doi.org/10.3390/microorganisms8091434
Song H-J, Moon DC, Mechesso AF, Kang HY, Kim MH, Choi J-H, Kim S-J, Yoon S-S, Lim S-K. Resistance Profiling and Molecular Characterization of Extended-Spectrum/Plasmid-Mediated AmpC β-Lactamase-Producing Escherichia coli Isolated from Healthy Broiler Chickens in South Korea. Microorganisms. 2020; 8(9):1434. https://doi.org/10.3390/microorganisms8091434
Chicago/Turabian StyleSong, Hyun-Ju, Dong Chan Moon, Abraham Fikru Mechesso, Hee Young Kang, Mi Hyun Kim, Ji-Hyun Choi, Su-Jeong Kim, Soon-Seek Yoon, and Suk-Kyung Lim. 2020. "Resistance Profiling and Molecular Characterization of Extended-Spectrum/Plasmid-Mediated AmpC β-Lactamase-Producing Escherichia coli Isolated from Healthy Broiler Chickens in South Korea" Microorganisms 8, no. 9: 1434. https://doi.org/10.3390/microorganisms8091434