Distribution and Genomic Characterization of Third-Generation Cephalosporin-Resistant Escherichia coli Isolated from a Single Family and Home Environment: A 2-Year Longitudinal Study
Abstract
:1. Introduction
2. Results
2.1. Participant Characteristic
2.2. Antimicrobial Susceptibility Profiles
2.3. Genome Sequences, Sequence Types, Serotypes, and Phylogenetic Groups
2.4. ARGs
2.4.1. β-Lactamase-Encoding Genes and Household Transmission
2.4.2. ARGs Other Than β-Lactamase Genes
2.5. Virulence Factors (VF)-Encoding Genes
3. Discussion
4. Materials and Methods
4.1. Participants and Sample Collection
4.2. Questionnaire Design
4.3. Microbiological Analysis and Antimicrobial Susceptibility Testing
4.4. Nanopore Sequencing and De Novo Assembly
4.5. Pathogenic Types of E. coli
4.6. Bioinformatics and Statistical Analysis
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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Variables | Index Patient | Mother | Father | Aunt | Uncle | Cousin 1 | Cousin 2 |
---|---|---|---|---|---|---|---|
Demographic data | |||||||
Age (years) | 0.3 | 35 | 37 | 46 | 42 | 8 | 6 |
Male/Female | M | F | M | F | M | F | F |
Travel abroad in the past 12 months | - | - | - | Japan | Japan China | Japan | Japan |
Postal code | 81146, Nanzi District, live in the same house but different floors | ||||||
Daily animal contact | Dog | ||||||
Diet habit | |||||||
Feed water source | RO water | RO water | RO water | RO water | RO water | RO water | RO water |
Boiled water use | + | + | + | + | + | + | + |
Vegetarian | Breastmilk or formula milk | - | - | - | - | - | - |
Consumption of meats, consumption days per week | |||||||
Pork | 0 | 6 | 7 | 5 | 6 | 6 | 5 |
Beef | 0 | 1 | 1 | 1 | 1 | 1 | 1 |
Sheep | 0 | 0 | 1 | 0 | 0 | 0 | 0 |
Chicken | 0 | 4 | 2 | 4 | 4 | 4 | 4 |
Duck | 0 | 1 | 2 | 1 | 1 | 1 | 1 |
Goose | 0 | 0 | 1 | 0 | 0 | 0 | 0 |
Fish | 0 | 4 | 7 | 4 | 4 | 4 | 4 |
Family cleaning habits | |||||||
Clean toilet bowl every month | + | + | + | + | + | + | + |
Clean bathroom sink every month | + | + | + | + | + | + | + |
Clean bathroom floor every month | + | + | + | + | + | + | + |
Clean children’s bedrooms every month | + | + | + | + | + | + | + |
Clean kitchen floor every month | + | + | + | + | + | + | + |
Clean living room floor every month | + | + | + | + | + | + | + |
Clean master bedroom every month | + | + | + | + | + | + | + |
Clean toys every year | + | + | + | + | + | + | + |
Medical history | |||||||
Previous hospitalization in the past 12 months | 2019/12 UTI 2020/04 UTI | 2019/12 Labor | - | - | - | 2019/5 UTI | 2019/07 Pneumonia |
Previous antimicrobial treatment in the past 12 months | + | + | - | - | - | + | + |
Previous probiotics use in the past 12 months, consumption days per week | 0 | 0 | 0 | 1 | 0 | 7 | 7 |
Antimicrobial Resistance Phenotype | Ampicillin/ Sulbactam | Piperacillin | Piperacillin/ Tazobactam | Cefazolin | Cefoxitin | Cefixime b | Ceftazidime b | Ceftriaxone b | Cefepime | Ertapenem | Imipenem | Amikacin | Gentamicin | Ciprofloxacin | Minocycline | Tigecycline | Colistin | Trimethoprim/ Sulfamethoxazole | Chloramphenicol | Azithromycin | |||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
Isolate No. a | Source | Date | blaESBL/blaAmpC Genes | ||||||||||||||||||||
I-01-S | Index case | 2019/12 | blaCTX-M-14 | ND c | ND d | ND d | |||||||||||||||||
I-01-U | Index case | 2020/04 | blaCTX-M-14 | ||||||||||||||||||||
I-02-S | Index case | 2020/04 | blaCTX-M-14 | ||||||||||||||||||||
I-03-S | Index case | 2020/05 | blaCTX-M-14 | ||||||||||||||||||||
I-04-S | Index case | 2020/06 | blaCTX-M-14 | ||||||||||||||||||||
I-05-S | Index case | 2020/11 | blaCMY-2 | ||||||||||||||||||||
I-06-S | Index case | 2021/01 | blaCMY-2 | ||||||||||||||||||||
I-07-S | Index case | 2021/03 | blaCMY-2 | ||||||||||||||||||||
I-08-S | Index case | 2021/04 | blaCMY-2 | ||||||||||||||||||||
I-09-S | Index case | 2021/06 | blaCMY-2 | ||||||||||||||||||||
I-10-S | Index case | 2021/08 | blaCMY-2 | ||||||||||||||||||||
I-11-S | Index case | 2021/09 | blaCMY-2 | ||||||||||||||||||||
F-01-S | Father | 2020/10 | blaCTX-M-27 | ||||||||||||||||||||
M-01-S | Mother | 2020/08 | blaCTX-M-15 | ||||||||||||||||||||
M-02-S | Mother | 2020/08 | blaCTX-M-15 | ||||||||||||||||||||
M-03-S | Mother | 2020/10 | blaCTX-M-15 | ||||||||||||||||||||
M-04-S | Mother | 2020/11 | blaCTX-M-14 | ||||||||||||||||||||
A-01-S | Aunt | 2020/11 | blaCMY-2 | ||||||||||||||||||||
A-02-S | Aunt | 2021/06 | blaCMY-2 | ||||||||||||||||||||
A-03-S | Aunt | 2021/06 | blaCMY-2 | ||||||||||||||||||||
A-04-S | Aunt | 2021/08 | blaCTX-M-55 | ||||||||||||||||||||
C1-01-S | Cousin 1 | 2021/04 | blaCMY-2 | ||||||||||||||||||||
C2-01-S | Cousin 2 | 2020/06 | blaCMY-2 | ||||||||||||||||||||
C2-02-S | Cousin 2 | 2020/12 | blaCMY-2 | ||||||||||||||||||||
C2-03-S | Cousin 2 | 2021/06 | blaCTX-M-55 | ||||||||||||||||||||
C2-04-S | Cousin 2 | 2021/08 | blaCMY-2 | ||||||||||||||||||||
E-01 | Bathroom basin | 2021/03 | blaCMY-2 | ||||||||||||||||||||
Percentage of non-susceptibility | 92.6% | 100.0% | 0 | 100.0% | 55.6% | 100.0% | 55.6% | 100.0% | 7.4% | 0.0% | 0.0% | 0.0% | 59.3% | 63.0% | 63.0% | 0.0% | NA | 55.6% | NA | NA |
Antimicrobial Resistance Genes | β-lactam | Aminoglycoside | Quinolone | Tetracycline | Colistin | Trimethoprim/Sulfamethoxazole | Amphenicol | Macrolide | |||||||||||||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
Isolate No. a | Source | Date | blaTEM | blaCTX-Mb | blaAmpC b | dfrA | sul | ||||||||||||||||||||||
TEM-1B | TEM-135 | CTX-M-14 | CTX-M-15 | CTX-M-27 | CTX-M-55 | CMY-2 | aac(3)-IId | aac(3)-VIa | gyrA c | qnrS1 | qnrS13 | tet(A) | tet(B) | tet(M) | mcr-1.1 | dfrA5 | dfrA12 | dfrA14 | dfrA17 | sul1 | sul2 | sul3 | cmlA1 | catA1 | floR | mph(A) | |||
I-01-S | Index case | 2019/12 | |||||||||||||||||||||||||||
I-01-U | Index case | 2020/04 | |||||||||||||||||||||||||||
I-02-S | Index case | 2020/04 | |||||||||||||||||||||||||||
I-03-S | Index case | 2020/05 | |||||||||||||||||||||||||||
I-04-S | Index case | 2020/06 | |||||||||||||||||||||||||||
I-05-S | Index case | 2020/11 | |||||||||||||||||||||||||||
I-06-S | Index case | 2021/01 | |||||||||||||||||||||||||||
I-07-S | Index case | 2021/03 | |||||||||||||||||||||||||||
I-08-S | Index case | 2021/04 | |||||||||||||||||||||||||||
I-09-S | Index case | 2021/06 | |||||||||||||||||||||||||||
I-10-S | Index case | 2021/08 | |||||||||||||||||||||||||||
I-11-S | Index case | 2021/09 | |||||||||||||||||||||||||||
F-01-S | Father | 2020/10 | |||||||||||||||||||||||||||
M-01-S | Mother | 2020/08 | |||||||||||||||||||||||||||
M-02-S | Mother | 2020/08 | |||||||||||||||||||||||||||
M-03-S | Mother | 2020/10 | |||||||||||||||||||||||||||
M-04-S | Mother | 2020/11 | |||||||||||||||||||||||||||
A-01-S | Aunt | 2020/11 | |||||||||||||||||||||||||||
A-02-S | Aunt | 2021/06 | |||||||||||||||||||||||||||
A-03-S | Aunt | 2021/06 | |||||||||||||||||||||||||||
A-04-S | Aunt | 2021/08 | |||||||||||||||||||||||||||
C1-01-S | Cousin 1 | 2021/04 | |||||||||||||||||||||||||||
C2-01-S | Cousin 2 | 2020/06 | |||||||||||||||||||||||||||
C2-02-S | Cousin 2 | 2020/12 | |||||||||||||||||||||||||||
C2-03-S | Cousin 2 | 2021/06 | |||||||||||||||||||||||||||
C2-04-S | Cousin 2 | 2021/08 | |||||||||||||||||||||||||||
E-01 | Bathroom basin | 2021/03 | |||||||||||||||||||||||||||
Percentage of positive by either of one gene | 20 (74.1%) | 12 (44.4%) | 15 (55.6%) | 16 (59.2%) | 19 (70.3%) | 21 (77.8%) | 1 (3.7%) | 15 (55.6%) | 17 (63%) | 16 (59.2%) | 8 (29.6%) |
Virulence Factor (VF)-Encoding Genes | Adherence | Capsule | Iron Uptake | Toxin | Miscellaneous | Definition | ||||||||||||||||||||||||||||||||||||||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
Isolate No. a | Source | Date | afaA | afaB | afaC | afaD | focC | hra | iha | lpfA | papA | papC | sfaD | yfcV | kpsE | kpsM II | kpsM III | chuA | fyuA | iroN | irp2 | iucC | iutA | sitA | air | astA | ccI | cea | cib | cma | cnf1 | hlyF | pic | sat | senB | tsh | vat | cvaC | eilA | etsC | gad | iss | katP | mcbA | mchF | ompT | terC | traT | usp | ExPEC | UPEC | APEC |
I-01-S | Index patient | 2019/12 | ||||||||||||||||||||||||||||||||||||||||||||||||||
I-01-U | Index patient | 2020/04 | ||||||||||||||||||||||||||||||||||||||||||||||||||
I-02-S | Index patient | 2020/04 | ||||||||||||||||||||||||||||||||||||||||||||||||||
I-03-S | Index patient | 2020/05 | ||||||||||||||||||||||||||||||||||||||||||||||||||
I-04-S | Index patient | 2020/06 | ||||||||||||||||||||||||||||||||||||||||||||||||||
I-05-S | Index patient | 2020/11 | ||||||||||||||||||||||||||||||||||||||||||||||||||
I-06-S | Index patient | 2021/01 | ||||||||||||||||||||||||||||||||||||||||||||||||||
I-07-S | Index patient | 2021/03 | ||||||||||||||||||||||||||||||||||||||||||||||||||
I-08-S | Index patient | 2021/04 | ||||||||||||||||||||||||||||||||||||||||||||||||||
I-09-S | Index patient | 2021/06 | ||||||||||||||||||||||||||||||||||||||||||||||||||
I-10-S | Index patient | 2021/08 | ||||||||||||||||||||||||||||||||||||||||||||||||||
I-11-S | Index patient | 2021/09 | ||||||||||||||||||||||||||||||||||||||||||||||||||
F-01-S | Father | 2020/10 | ||||||||||||||||||||||||||||||||||||||||||||||||||
M-01-S | Mother | 2020/08 | ||||||||||||||||||||||||||||||||||||||||||||||||||
M-02-S | Mother | 2020/08 | ||||||||||||||||||||||||||||||||||||||||||||||||||
M-03-S | Mother | 2020/10 | ||||||||||||||||||||||||||||||||||||||||||||||||||
M-04-S | Mother | 2020/11 | ||||||||||||||||||||||||||||||||||||||||||||||||||
A-01-S | Aunt | 2020/11 | ||||||||||||||||||||||||||||||||||||||||||||||||||
A-02-S | Aunt | 2021/06 | ||||||||||||||||||||||||||||||||||||||||||||||||||
A-03-S | Aunt | 2021/06 | ||||||||||||||||||||||||||||||||||||||||||||||||||
A-04-S | Aunt | 2021/08 | ||||||||||||||||||||||||||||||||||||||||||||||||||
C1-01-S | Cousin 1 | 2021/04 | ||||||||||||||||||||||||||||||||||||||||||||||||||
C2-01-S | Cousin 2 | 2020/06 | ||||||||||||||||||||||||||||||||||||||||||||||||||
C2-02-S | Cousin 2 | 2020/12 | ||||||||||||||||||||||||||||||||||||||||||||||||||
C2-03-S | Cousin 2 | 2021/06 | ||||||||||||||||||||||||||||||||||||||||||||||||||
C2-04-S | Cousin 2 | 2021/08 | ||||||||||||||||||||||||||||||||||||||||||||||||||
E-01 | Bathroom basin | 2021/03 | ||||||||||||||||||||||||||||||||||||||||||||||||||
ExPEC:≧2 of 5 markers, including papAH and/or papC, sfa/focDE, afa/draBC, kpsM II, and iutA | ||||||||||||||||||||||||||||||||||||||||||||||||||||
UPEC:≧3 of 4 markers, including chuA, fyuA, vat, and yfcV | ||||||||||||||||||||||||||||||||||||||||||||||||||||
APEC:≧4 of 5 markers, including hlyF, iutA, iroN, iss, and ompT | ||||||||||||||||||||||||||||||||||||||||||||||||||||
Presence of predicted VF-encoding genes |
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Feng, Y.-C.; Liou, C.-H.; Ng, W.V.; Chen, F.-J.; Hung, C.-H.; Liu, P.-Y.; Liao, Y.-C.; Wu, H.-C.; Cheng, M.-F. Distribution and Genomic Characterization of Third-Generation Cephalosporin-Resistant Escherichia coli Isolated from a Single Family and Home Environment: A 2-Year Longitudinal Study. Antibiotics 2022, 11, 1152. https://doi.org/10.3390/antibiotics11091152
Feng Y-C, Liou C-H, Ng WV, Chen F-J, Hung C-H, Liu P-Y, Liao Y-C, Wu H-C, Cheng M-F. Distribution and Genomic Characterization of Third-Generation Cephalosporin-Resistant Escherichia coli Isolated from a Single Family and Home Environment: A 2-Year Longitudinal Study. Antibiotics. 2022; 11(9):1152. https://doi.org/10.3390/antibiotics11091152
Chicago/Turabian StyleFeng, Yin-Chih, Ci-Hong Liou, Wailap Victor Ng, Feng-Jui Chen, Chih-Hsin Hung, Po-Yen Liu, Yu-Chieh Liao, Han-Chieh Wu, and Ming-Fang Cheng. 2022. "Distribution and Genomic Characterization of Third-Generation Cephalosporin-Resistant Escherichia coli Isolated from a Single Family and Home Environment: A 2-Year Longitudinal Study" Antibiotics 11, no. 9: 1152. https://doi.org/10.3390/antibiotics11091152