Exploring the Role of the Environment as a Reservoir of Antimicrobial-Resistant Campylobacter: Insights from Wild Birds and Surface Waters
Abstract
:1. Introduction
2. Materials and Methods
2.1. Campylobacter Isolates Collection
2.2. Disk Diffusion Method
2.3. Genomic DNA Extraction and Whole-Genome Sequencing
2.4. Genomic Assembly and Characterisation
2.5. Result Interpretation and Statistical Analyses
3. Results
3.1. AMR Phenotypes and Genotypes of Isolates
3.2. Association between AMR, ST, and Heavy Metals
3.3. Virulence Genes of Isolates
4. Discussion
Supplementary Materials
Author Contributions
Funding
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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C. coli | C. jejuni | |||
---|---|---|---|---|
AMR Profiles | Bird (n = 2) | Water (n = 142) | Bird (n = 110) | Water (n = 9) |
Susceptible | 2 (100%) | 138 (97.2%, CI95: 93.0–98.9%) | 97 (88.2%, CI95: 80.8–93.0%) | 7 (78%) |
AMP | 4 (2.8%, CI95: 1.1–7.0%) | 3 (2.7%, CI95: 0.9–7.7%) | ||
NAL-CIP | 9 (8.2%, CI95: 4.4–14.8%) | |||
NAL-CIP-TET | 1 (0.9%, CI95: 0.2–5.0%) | |||
AMP-NAL-CIP-TET | 2 (22%) |
C. coli | C. jejuni | |||
---|---|---|---|---|
AMR Profiles | Bird (n = 2) | Water (n = 142) | Bird (n = 110) | Water (n = 9) |
Susceptible | 2 (100%) | 74 (52.1%, CI95: 43.9–60.2%) | 10 (9.1%, CI95: 5.0–15.9%) | 1 (11.1%) |
Aminoglycoside | 48 (33.8%, CI95: 26.5–41.9%) | |||
Beta-lactam | 16 (11.3%, CI95: 7.1–17.5%) | 87 (79.1%, CI95: 70.6–85.6%) | 6 (66.7%) | |
Aminoglycoside–Macrolide | 1 (0.9%, CI95:0.2–3.9%) | |||
Aminoglycoside–Beta-lactam | 2 (1.2%, CI95: 0.4–5%) | 1 (0.9%, CI95: 0.2–5%) | ||
Beta-lactam–Quinolone | 9 (8.2%, CI95: 4.4–14.8%) | |||
Beta-lactam–Tetracycline | 1 (0.9%, CI95: 0.2–5%) | |||
Aminoglycoside–Beta-lactam–Quinolone | 1 (0.9%, CI95: 0.2–3.9%) | |||
Beta-lactam–Macrolide–Tetracycline | 1 (0.9%, CI95: 0.2–5%) | |||
Beta-lactam–Quinolone–Tetracycline | 2 (22%) | |||
Macrolide–Quinolone–Tetracycline | 1 (0.9%, CI95: 0.2–5%) |
C. coli | C. jejuni | ||||
---|---|---|---|---|---|
Bird (n = 2) | Water (n = 142) | Bird (n = 110) | Water (n = 9) | ||
Aminoglycoside | No. of isolates with R phenotype | 0 | 0 | 0 | 0 |
No. of isolates with R genotype | 0 | 52 | 1 | 0 | |
Concordance (%) | 100 | 63 | 99 | 100 | |
Beta-lactam | No. of isolates with R phenotype | 0 | 4 | 3 | 2 |
No. of isolates with R genotype | 0 | 19 | 99 | 8 | |
Concordance (%) | 100 | 89 | 13 | 33 | |
Quinolone | No. of isolates with R phenotype | 0 | 0 | 10 | 2 |
No. of isolates with R genotype | 0 | 1 | 10 | 2 | |
Concordance (%) | 100 | 99 | 100 | 100 | |
Macrolide | No. of isolates with R phenotype | 0 | 0 | 0 | 0 |
No. of isolates with R genotype | 0 | 1 | 2 | 0 | |
Concordance (%) | 100 | 99 | 98 | 100 | |
Tetracycline | No. of isolates with R phenotype | 0 | 0 | 1 | 2 |
No. of isolates with R genotype | 0 | 0 | 3 | 2 | |
Concordance (%) | 100 | 100 | 98 | 100 |
Phenotype: Susceptible | Phenotype: Resistant | |||||||
---|---|---|---|---|---|---|---|---|
Antimicrobial | Genotype: Susceptible | Genotype: Resistant | Genotype: Resistant | Genotype: Susceptible | Cohen’s Kappa Coefficient | 95% CI | Interpretation | |
C. coli | Aminoglycoside | 92 | 52 | 0 | 0 | - | - | |
Beta-lactam | 122 | 18 | 1 | 3 | 0.04 | −0.11–0.2 | Slight | |
Quinolone | 143 | 1 | 0 | 0 | - | - | ||
Macrolide | 143 | 1 | 0 | 0 | - | - | ||
Tetracylcine | 144 | 0 | 0 | 0 | - | - | ||
C. jejuni | Aminoglycoside | 118 | 1 | 0 | 0 | - | - | |
Beta-lactam | 12 | 102 | 5 | 0 | 0.01 | 0–0.02 | Slight | |
Quinolone | 107 | 0 | 12 | 0 | 1 | 1 | Almost perfect | |
Macrolide | 117 | 2 | 0 | 0 | - | - | ||
Tetracylcine | 114 | 2 | 3 | 0 | 0.74 | 0.40–1 | Substantial |
C. coli | C. jejuni | ||||
---|---|---|---|---|---|
Virulence Gene | Bird (n = 2) | Water (n = 142) | Bird (n = 110) | Water (n = 9) | |
Flagellin | flaC | 2 | 142 | 110 | 9 |
Flagellar proteins | flgB, flgC, flgF, flgG, flgI | 2 | 142 | 110 | 9 |
Flagellar biosynthesis protein | flhA | 2 | 142 | 110 | 9 |
Flagellar protein | fliE, fliF, fliG, fliI, fliL, fliM, fliS, fliW | 2 | 142 | 110 | 9 |
Lipooligosaccharide (LOS) synthesis | hldD | 2 | 142 | 110 | 9 |
Pseudaminic acid synthesis (Flagellin) | pseB | 2 | 142 | 110 | 9 |
Chemotaxis protein | cheW | 2 | 141 | 110 | 9 |
Flagellar protein | flgH, flgJ, flgQ | 2 | 141 | 110 | 9 |
Flagellar motor protein | motA | 2 | 141 | 110 | 9 |
Chemotaxis protein | cheV | 2 | 142 | 109 | 9 |
Flagellar biosynthesis protein | fliR | 2 | 142 | 109 | 9 |
Chemotaxis protein | cheY | 2 | 140 | 110 | 9 |
Flagellar protein | flhG | 0 | 142 | 110 | 9 |
Flagellar protein | flgK | 2 | 141 | 109 | 9 |
Lipooligosaccharide (LOS) synthesis | gmhA | 0 | 139 | 109 | 8 |
Pseudaminic acid synthesis (flagellin) | pseC | 0 | 109 | 110 | 9 |
LOS synthesis | hldE | 2 | 96 | 109 | 9 |
RNA polymerase factor sigma-54 (Pse) | rpoN | 2 | 87 | 110 | 9 |
Pseudaminic acid synthesis (flagellin) | pseI | 2 | 65 | 110 | 9 |
Flagellar protein | flgE | 2 | 43 | 110 | 9 |
Flagellar protein | flaD | 2 | 94 | 50 | 6 |
Pseudaminic acid synthesis (flagellin) | pseA | 2 | 40 | 92 | 7 |
Capsular polysaccharide | kpsT | 2 | 15 | 110 | 9 |
Chemotaxis protein | cheA | 0 | 9 | 109 | 8 |
Flagellar motor protein | fliN | 0 | 6 | 110 | 9 |
Flagellar protein | flgM | 0 | 5 | 110 | 9 |
Pseudaminic acid synthesis (flagellin) | pseF | 0 | 3 | 110 | 9 |
Pseudaminic acid synthesis (flagellin) | pseG | 0 | 2 | 110 | 9 |
Flagellar protein | flaG | 0 | 1 | 110 | 9 |
Flagellar protein | flgQ | 0 | 1 | 110 | 9 |
Outer membrane fibronectin-binding protein | cadF | 0 | 0 | 110 | 9 |
Invasion antigen | ciaB, ciaC | 0 | 0 | 110 | 9 |
Adherence | eptC | 0 | 0 | 110 | 9 |
Flagellar protein | flgA, flgP, flgR, flgS | 0 | 0 | 110 | 9 |
Flagellar biosynthesis protein | flhB, flhF | 0 | 0 | 110 | 9 |
Flagellar biosynthesis protein | fliA, fliH, fliP, fliY | 0 | 0 | 110 | 9 |
Lipooligosaccharide (LOS) synthesis | gmhB | 0 | 0 | 110 | 9 |
Adhesin | jlpA | 0 | 0 | 110 | 9 |
Flagella motor protein | motB | 0 | 0 | 110 | 9 |
Adhesin | pebA | 0 | 0 | 110 | 9 |
Flagellar protein | pflA | 0 | 0 | 110 | 9 |
Lipooligosaccharide (LOS) synthesis | waaC | 0 | 0 | 110 | 9 |
Capsular polysaccharide | kpsS | 0 | 0 | 109 | 9 |
Capsular polysaccharide | kpsD, kpsE | 0 | 1 | 109 | 7 |
Capsular polysaccharide | kpsM | 0 | 2 | 108 | 7 |
Capsular synthesis | Cj1419c | 2 | 20 | 84 | 7 |
Cytolethal distending toxin (CDT) | cdtC | 0 | 0 | 99 | 9 |
Capsular synthesis | Cj1420c | 2 | 21 | 77 | 6 |
Capsule protein | kpsC | 0 | 0 | 87 | 6 |
Capsule biosynthesis and transport | Cj1417c | 0 | 0 | 85 | 7 |
Lipooligosaccharide (LOS) synthesis | gmhA2 | 0 | 4 | 80 | 4 |
Capsule synthesis | hddA | 0 | 5 | 78 | 4 |
Flagella protein | pseH | 0 | 0 | 72 | 7 |
Major outer membrane protein | porA | 0 | 1 | 57 | 1 |
Cytolethal distending toxin (CDT) | cdtA | 0 | 0 | 54 | 3 |
Cytolethal distending toxin (CDT) | cdtB | 0 | 0 | 53 | 3 |
Lipooligosaccharide (LOS) synthesis | waaF | 0 | 1 | 50 | 4 |
Lipooligosaccharide (LOS) synthesis | htrB | 0 | 0 | 45 | 7 |
Capsule protein | cysC | 0 | 0 | 47 | 4 |
Flagella protein | ptmA, ptmB | 0 | 0 | 42 | 8 |
Flagella protein | flgD | 0 | 1 | 42 | 6 |
Lipooligosaccharide (LOS) synthesis | neuC1 | 0 | 35 | 10 | 0 |
Capsule synthesis | Cj1416c | 0 | 0 | 40 | 4 |
Flagella protein | fliD | 0 | 1 | 39 | 4 |
Capsule synthesis | hddC | 0 | 1 | 37 | 1 |
Motility accessory factor PseE | pseE maf5 | 0 | 0 | 32 | 5 |
Lipooligosaccharide (LOS) synthesis | Cj1135 | 0 | 0 | 23 | 7 |
Capsule protein | Cj1427c | 0 | 1 | 24 | 1 |
Lipooligosaccharide (LOS) synthesis | waaV | 0 | 0 | 24 | 1 |
Flagellin | flaA, flaB | 0 | 0 | 15 | 4 |
Motility accessory factor PseD | pseD maf2 | 0 | 0 | 14 | 1 |
Motility accessory factor | maf4 | 0 | 0 | 9 | 2 |
Capsule protein | rfbC | 0 | 1 | 9 | 0 |
Lipooligosaccharide (LOS) synthesis | neuA1, neuB1 | 0 | 0 | 9 | 0 |
Flagellar protein | fliK | 0 | 0 | 8 | 1 |
Lipooligosaccharide (LOS) synthesis | Cj1137c, Cj1138 | 0 | 0 | 7 | 0 |
Lipooligosaccharide (LOS) synthesis | wlaN | 0 | 0 | 6 | 0 |
Lipooligosaccharide (LOS) synthesis | Cj1136 | 0 | 0 | 5 | 0 |
Lipooligosaccharide (LOS) synthesis | cstIII | 0 | 0 | 5 | 0 |
Capsule synthesis | fcl | 0 | 1 | 4 | 0 |
Capsule protein | Cj1432c, Cj1435c, Cj1436c, Cj1440c | 0 | 1 | 1 | 0 |
Capsule protein | glf | 0 | 1 | 1 | 0 |
Capsule protein | kfiD | 0 | 1 | 1 | 0 |
Capsule protein | Cj1426c | 0 | 0 | 1 | 0 |
Type IV secretion system protein | Cjp54, virB11, virB4, virB8, virD4 | 0 | 1 | 0 | 0 |
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© 2024 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
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Hock, L.; Walczak, C.; Mosser, J.; Ragimbeau, C.; Cauchie, H.-M. Exploring the Role of the Environment as a Reservoir of Antimicrobial-Resistant Campylobacter: Insights from Wild Birds and Surface Waters. Microorganisms 2024, 12, 1621. https://doi.org/10.3390/microorganisms12081621
Hock L, Walczak C, Mosser J, Ragimbeau C, Cauchie H-M. Exploring the Role of the Environment as a Reservoir of Antimicrobial-Resistant Campylobacter: Insights from Wild Birds and Surface Waters. Microorganisms. 2024; 12(8):1621. https://doi.org/10.3390/microorganisms12081621
Chicago/Turabian StyleHock, Louise, Cécile Walczak, Juliette Mosser, Catherine Ragimbeau, and Henry-Michel Cauchie. 2024. "Exploring the Role of the Environment as a Reservoir of Antimicrobial-Resistant Campylobacter: Insights from Wild Birds and Surface Waters" Microorganisms 12, no. 8: 1621. https://doi.org/10.3390/microorganisms12081621