Evaluation of Antibiotic Resistance of Salmonella Serotypes and Whole-Genome Sequencing of Multiresistant Strains Isolated from Food Products in Russia
Abstract
:1. Introduction
2. Results
2.1. Prevalence of Salmonella spp. in Food Products
2.2. Serological Identification of Salmonella
2.3. Prevalence of Antimicrobial Resistance
2.4. Sequencing
2.5. General Characterization of the Genomes
2.6. Multilocus Sequence Typing of Strains
2.7. Antibiotic Resistance Genes
2.8. Plasmids
2.9. Pathogenicity Islands
2.10. Prophages
3. Discussion
4. Materials and Methods
4.1. Strains Used in the Work
4.2. Isolation and Confirmation of Salmonella Isolates
4.3. Serotyping of Salmonella Isolates
4.4. Screening of the Isolates for Resistance to Antimicrobial Preparations
4.5. DNA Isolation and Sequencing
4.6. Bioinformatic Techniques
4.7. Nucleotide Sequence Accession Number
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
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Sample Type | Number of Samples Analysed | Number of Positive Samples (%) |
---|---|---|
Poultry | 112 | 12 (10.7) |
Pork | 91 | 3 (3.3) |
Beef | 103 | 7 (6.8) |
Minced meat | 168 | 10 (6) |
Total | 474 | 32 (6.8) |
Antimicrobial Class | Antimicrobial Agent | No. of Strains (%) | ||
---|---|---|---|---|
Resistant (R) | Intermediate (I) | Susceptible (S) | ||
Penicillins | Ampicillin (AMP) | 8 (25.00) | 8 (3.13) | 23 (71.88) |
Monobactams/carbapenems | Imipenem (IPM) | 6 (18.75) | 2 (6.25) | 24 (75.00) |
Aminoglycosides | Amikacin (AMK) | 9 (28.13) | 14 (43.75) | 9 (28.13) |
Streptomycin (STR) | 8 (25.00) | 4 (12.50) | 20 (62.50) | |
Tobramycin | 5 (15.63) | 1 (3.13) | 26 (81.25) | |
Cephems | Cefotaxime (CTX) | 6 (18.75) | 6 (18.75) | 20 (62.50) |
Cefazolin (CFZ) | 15 (46.86) | 8 (25.00) | 9 (28.13) | |
Folate pathway antagonists | Trimethoprim/ sulfamethoxazole (SXT) | 19 (59.38) | 0 (0) | 13 (40.63) |
Chloramphenicol (CHL) | 7 (21.88) | 3 (9.38) | 22 (68.75) | |
Macrolides and azalides | Azithromycin | 12 (37.50) | - | 20 (62.50) |
β-Lactam/β-lactamase inhibitor combinations | Amoxicillin–clavulanic acid (AMC) | 2 (6.25) | 0 (0) | 30 (93.75) |
Nitrofuran | Furadonin | 5 (18.75) | 3 (9.38) | 24 (75.00) |
Tetracyclines | Tetracycline (TET) | 13 (40.63) | 9 (28.13) | 10 (31.25) |
Antimicrobial Agent | No. of Resistance Isolates by Serotype (Resistance Rate, %) | |||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|
Salmonella Typhimurium | Salmonella Enteritidis | Salmonella Infantis | Salmonella Kentucky | Salmonella Rissen | Salmonella Reading | Salmonella Give | Salmonella Derby | Salmonella Idikan | Salmonella Indiana | Salmonella Genovar | Total | |
Ampicillin (AMP) | 25.0 | 16.7 | 33.3 | 0.0 | 50.0 | 0.0 | 100.0 | 0.0 | 0.0 | 100.0 | 0.0 | 25.0 |
Imipenem (IPM) | 25.0 | 16.7 | 33.3 | 50.0 | 0.0 | 0.0 | 0.0 | 0.0 | 0.0 | 0.0 | 0.0 | 18.8 |
Amikacin (AMK) | 0.0 | 16.7 | 33.3 | 0.0 | 50.0 | 66.7 | 0.0 | 50.0 | 0.0 | 100.0 | 0.0 | 28.1 |
Streptomycin (STR) | 75.0 | 0.0 | 33.3 | 0.0 | 0.0 | 0.0 | 0.0 | 50.0 | 0.0 | 100.0 | 0.0 | 25 |
Tobramycin (TM) | 25.0 | 0.0 | 22.2 | 0.0 | 0.0 | 0.0 | 0.0 | 50.0 | 0.0 | 100.0 | 0.0 | 15.6 |
Cefotaxime (CFX) | 25.0 | 33.3 | 11.1 | 0.0 | 0.0 | 33.3 | 0.0 | 50.0 | 0.0 | 0.0 | 0.0 | 18.8 |
Cefazolin (CFZ) | 50.0 | 50.0 | 44.4 | 50.0 | 50.0 | 66.7 | 100.0 | 50.0 | 0.0 | 0.0 | 0.0 | 50 |
Trimethoprim/sulfamethoxazole (STX) | 75.0 | 50.0 | 66.7 | 50.0 | 50.0 | 33.3 | 100.0 | 50.0 | 0.0 | 100.0 | 100.0 | 59.34 |
Chloramphenicol (CHL) | 25.0 | 16.7 | 44.4 | 0.0 | 50.0 | 0.0 | 0.0 | 0.0 | 0.0 | 0.0 | 0.0 | 21.9 |
Azithromycin (AZM) | 50.0 | 33.3 | 22.2 | 0.0 | 50.0 | 33.3 | 0.0 | 50.0 | 100.0 | 0.0 | 100.0 | 34.4 |
Amoxicillin + clavulanic acid (AMK) | 0.0 | 0.0 | 22.2 | 0.0 | 0.0 | 0.0 | 0.0 | 0.0 | 0.0 | 0.0 | 0.0 | 6.3 |
Nitrofurantoin (NIT) | 0.0 | 0.0 | 44.4 | 0.0 | 0.0 | 33.3 | 0.0 | 0.0 | 0.0 | 0.0 | 0.0 | 15.6 |
Tetracycline (TET) | 75.0 | 33.3 | 55.6 | 0.0 | 0.0 | 33.3 | 0.0 | 50.0 | 0.0 | 100.0 | 0.0 | 40.6 |
Serovar | Isolate | Pattern | No. of Antimicrobial Agents | No. of Classes |
---|---|---|---|---|
Salmonella Give | S1 | AMP-STX-CFZ | 3 | 3 |
Salmonella Typhimurium | S3 | STR-AMP-TM-IPM-CHL | 5 | 4 |
S5 | CTX-STX-AZM-TET-CFZ | 5 | 4 | |
S14 | STR-STX-AZM-TET-CFZ | 5 | 4 | |
S25 | STR-STX-TET | 3 | 3 | |
Salmonella Reading | S23 | CTX-AMK-AZM-CFZ | 4 | 3 |
S4 | AMK-STX-AZM-TET-NIT | 5 | 5 | |
S33 | CFZ | 1 | 1 | |
Salmonella Derby | S6 | STR-AMK-AZM-TET | 4 | 3 |
S11 | CTX-TM-STX-CFZ | 4 | 3 | |
Salmonella Idikan | S9 | AZM | 1 | 1 |
Salmonella Rissen | S10 | CFZ-CHL | 1 | 1 |
S18 | AMP-AMK-STX-AZM | 4 | 4 | |
Salmonella Infantis | S26 | STR-IPM-CFZ-NIT | 4 | 4 |
S15 | AMK-STX-AZM-TET-CFZ | 5 | 5 | |
SZL 30 | STR-AMP-AMK-TM-STX-IPM-TET-CHL | 8 | 6 | |
SZL 31 | STR-AMP-AMK-TM-STX-IPM-TET-CHL | 8 | 6 | |
S34 | AMK-STX-TET-CFZ-NIT | 5 | 5 | |
S35 | STX | 1 | 1 | |
S36 | ND | 0 | 0 | |
S37 | STX-TET-NIT | 3 | 3 | |
S28 | CTX-AZM-CFZ-CHL-NIT | 5 | 4 | |
Salmonella Genovar | S16 | STX-AZM | 2 | 2 |
Salmonella Enteritidis | S7 | AMK-AZM-CFZ | 3 | 3 |
S8 | CTX-AZM | 2 | 2 | |
S17 | AMP-STX-TET-CFZ-CHL | 5 | 5 | |
S20 | STX-IPM-CFZ | 3 | 3 | |
S27 | CTX-TET | 2 | 2 | |
S29 | STX | 1 | 1 | |
Salmonella Kentucky | S32 | ND | 0 | 0 |
S19 | STX-IMP-CFZ | 3 | 3 | |
Salmonella Typhimurium | SZL 38 | STR-AMP-AMK-TM-STX-TET | 6 | 4 |
Strain | Chromosome Size (bp) | Plasmids | |
---|---|---|---|
Name | Size (bp) | ||
SZL 30 | 4,689,375 | pSZL30.1 pSZL30.2 | 276,251 53,986 |
SZL 31 | 4,689,704 | pSZL31.1 pSZL31.2 | 280,239 53,147 |
SZL 38 | 5,052,615 | pSZL38.1 | 79,333 |
Parameter | Strain | ||
---|---|---|---|
30 | 31 | 38 | |
Predicted genes | 5184 | 5191 | 5320 |
Protein-coding genes | 5078 | 5085 | 5209 |
Protein-coding genes with predicted function | 3845 (75.7%) | 3785 (74.4%) | 3851 (73.9%) |
tRNA genes | 84 | 84 | 89 |
Resistance Gene | Protein | Antimicrobial Agent | Location | ||
---|---|---|---|---|---|
SZL 30 | SZL 31 | SZL 38 | |||
aadA1 | Aminoglycoside (3″) (9)-adenylyltransferase | STR | pSZL30.2 | - | - |
aadA2b | - | pSZL31.1 | - | ||
aph(3″)-Ib | Aminoglycoside 3′-phosphotransferase | - | - | chromosome | |
aph(6)-Id | Aminoglycoside O-phosphotransferase | - | - | chromosome | |
blaTEM-1B | Class A β-lactamase | AMP | pSZL30.2 | pSZL31.2 | chromosome |
aac(6′)-Iaa | Chromosomal encoded aminoglycoside N (6′)-acetyltransferase | AMK, TM | chromosome | chromosome | chromosome |
sul3 | Dihydropteroate synthase | STX | pSZL30.2 | pSZL31.1 pSZL31.2 | - |
sul2 | - | - | chromosome | ||
tet(A) | Tetracycline efflux MSF transporter | TET | pSZL30.1 | pSZL31.1 | - |
tet(B) | - | - | chromosome | ||
cmlA1 | Drug efflux MSF transporter Bcr/CflA family | CHL | pSZL30.2 | pSZL31.1 pSZL31.2 | - |
mefB | MSF efflux transporter | AZM, ERY | pSZL30.2 | chromosome pSZL31.2 | - |
mdfA/cmr | MSF efflux transporter | RIF, PUR, ERY | chromosome | chromosome | chromosome |
mdtABC-tolC | MSF efflux transporter | NB, NAL, NOR | chromosome | chromosome | chromosome |
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Rakitin, A.L.; Yushina, Y.K.; Zaiko, E.V.; Bataeva, D.S.; Kuznetsova, O.A.; Semenova, A.A.; Ermolaeva, S.A.; Beletskiy, A.V.; Kolganova, T.V.; Mardanov, A.V.; et al. Evaluation of Antibiotic Resistance of Salmonella Serotypes and Whole-Genome Sequencing of Multiresistant Strains Isolated from Food Products in Russia. Antibiotics 2022, 11, 1. https://doi.org/10.3390/antibiotics11010001
Rakitin AL, Yushina YK, Zaiko EV, Bataeva DS, Kuznetsova OA, Semenova AA, Ermolaeva SA, Beletskiy AV, Kolganova TV, Mardanov AV, et al. Evaluation of Antibiotic Resistance of Salmonella Serotypes and Whole-Genome Sequencing of Multiresistant Strains Isolated from Food Products in Russia. Antibiotics. 2022; 11(1):1. https://doi.org/10.3390/antibiotics11010001
Chicago/Turabian StyleRakitin, Andrey L., Yulia K. Yushina, Elena V. Zaiko, Dagmara S. Bataeva, Oksana A. Kuznetsova, Anastasia A. Semenova, Svetlana A. Ermolaeva, Aleksey V. Beletskiy, Tat’yana V. Kolganova, Andrey V. Mardanov, and et al. 2022. "Evaluation of Antibiotic Resistance of Salmonella Serotypes and Whole-Genome Sequencing of Multiresistant Strains Isolated from Food Products in Russia" Antibiotics 11, no. 1: 1. https://doi.org/10.3390/antibiotics11010001