Multidrug resistance profiles of isolated Staphylococcus strains
| Species of bird | Number of Staphylococcus (% strains of all isolated strains) | Phenotypic resistance combination pattern (number of classes of antimicrobial agents) | Number of strains |
|---|---|---|---|
| no resistance | 10 | ||
| β-lactams (1) | 6 | ||
| macrolides (1) | 7 | ||
| fusidic acid (1) | 6 | ||
| fluoroquinolones (1) | 1 | ||
| fusidic acid, fluoroquinolones (2) | 5 | ||
| phenicols, tetracyclines (2) | 1 | ||
| fluoroquinolones, β-lactams (2) | 1 | ||
| fluoroquinolones, fusidic acid, β-lactams (3) | 2 | ||
| fluoroquinolones, macrolides, β-lactams (3) | 2 | ||
| macrolides, β-lactams, tetracyclines (3) | 2 | ||
| fluoroquinolones, fusidic acid, tetracyclines (3) | 1 | ||
| Capercaillie | fluoroquinolones, fusidic acid, β-lactams, sulfonamide + dihydrofolate reductase inhibitor (4) | 1 | |
| (Tetrao urogallus) | 57 (44.2) | fluoroquinolones, tetracyclines, β-lactams, sulfonamide + dihydrofolate reductase inhibitor (4) | 1 |
| fluoroquinolones, fusidic acid, β-lactams, tetracyclines (4) | 1 | ||
| fluoroquinolones, fusidic acid, β-lactams, macrolides (4) | 1 | ||
| fluoroquinolones, tetracyclines, macrolides, sulfonamide + dihydrofolate reductase inhibitor (4) | 1 | ||
| fluoroquinolones, macrolides, β-lactams, sulfonamide + dihydrofolate reductase inhibitor (4) | 1 | ||
| fluoroquinolones, aminoglycosides, β-lactams, sulfonamide + dihydrofolate reductase inhibitor (4) | 1 | ||
| fluoroquinolones, macrolides, β-lactams, tetracyclines, phenicols (5) | 1 | ||
| fluoroquinolones, macrolides, β-lactams, tetracyclines, sulfonamide + dihydrofolate reductase inhibitor (5) | 2 | ||
| fluoroquinolones, macrolides, β-lactams, Fusidic acid, aminoglycosides, sulfonamide + dihydrofolate reductase inhibitor (6) | 1 | ||
| fluoroquinolones, macrolides, β-lactams, Fusidic acid, aminoglycosides, tetracyclines, phenicols, sulfonamide + dihydrofolate reductase inhibitor (8) | 2 | ||
| no resistance | 7 | ||
| β-lactams (1) | 1 | ||
| macrolides (1) | 1 | ||
| tetracyclines (1) | 2 | ||
| sulfonamide + dihydrofolate reductase inhibitor (1) | 1 | ||
| macrolides, tetracyclines (2) | 2 | ||
| Fusidic acid, tetracyclines (2) | 3 | ||
| Fusidic acid, fluoroquinolones (2) | 1 | ||
| macrolides, β-lactams (2) | 1 | ||
| White stork (Ciconia ciconia) | 27 (20.9) | fusidic acid, fluoroquinolones, tetracyclines (3) fusidic acid, fluoroquinolones, β-lactams (3) | 1 1 |
| fusidic acid, fluoroquinolones, β-lactams, macrolides (4) | 1 | ||
| fusidic acid, fluoroquinolones, macrolides, sulfonamide + dihydrofolate reductase inhibitor (4) | 1 | ||
| fusidic acid, fluoroquinolones, macrolides, β-lactams, tetracyclines (5) | 1 | ||
| fusidic acid, fluoroquinolones, macrolides, tetracyclines, sulfonamide + dihydrofolate reductase inhibitor (5) | 1 | ||
| fusidic acid, fluoroquinolones, macrolides, β-lactams, tetracyclines, phenicols (6) | 1 | ||
| fusidic acid, fluoroquinolones, aminoglycosides, β-lactams, tetracyclines, phenicols (6) | 1 | ||
| no resistance | 1 | ||
| phenicols (1) | 1 | ||
| β-lactams, tetracyclines (2) | 1 | ||
| fluoroquinolones, macrolides, tetracyclines (3) | 4 | ||
| macrolides, β-lactams, tetracyclines (3) | 1 | ||
| fluoroquinolones, β-lactams, tetracyclines (3) | 1 | ||
| fluoroquinolones, macrolides, fusidic acid, tetracyclines (4) | 2 | ||
| fluoroquinolones, β-lactams, fusidic acid, tetracyclines (4) | 4 | ||
| Common pheasant | fluoroquinolones, β-lactams, tetracyclines, sulfonamide + dihydrofolate reductase inhibitor (4) | 1 | |
| (Phasianus colchicus) | 22 (17.1) | fluoroquinolones, fusidic acid, tetracyclines, sulfonamide + dihydrofolate reductase inhibitor (4) | 1 |
| fluoroquinolones, β-lactams, tetracyclines, macrolides (4) | 1 | ||
| fluoroquinolones, fusidic acid, tetracyclines, macrolides, phenicols (5) | 1 | ||
| fluoroquinolones, fusidic acid, β-lactams, tetracyclines, sulfonamide + dihydrofolate reductase inhibitor (5) | 1 | ||
| fluoroquinolones, fusidic acid, β-lactams, tetracyclines, macrolides, sulfonamide + dihydrofolate reductase inhibitor (6) | 1 | ||
| fluoroquinolones, fusidic acid, β-lactams, tetracyclines, macrolides, phenicols, sulfonamide + dihydrofolate reductase inhibitor (7) | 1 | ||
| Tawny owl | no resistance | 4 | |
| 6 (4.6) | β-lactams (1) | 1 | |
| (Strix aluco) | macrolides, fusidic acid, tetracyclines (3) | 1 | |
| Common kestrel | 5 (3.9) | no resistance | 4 |
| (Falco tinnunculus) | fluoroquinolones, fusidic acid, macrolides (3) | 1 | |
| Common blackbird (Turdus merula) | 4 (3.1) | no resistance | 4 |
| no resistance | 1 | ||
| Mute swan | 3 (2.3) | fluoroquinolones, β-lactams (2) | 1 |
| (Cygnus olor) | fluoroquinolones, β-lactams, fusidic acid (3) | 1 | |
| Song thrush | no resistance | 1 | |
| (Turdus | 3 (2.3) | fluoroquinolones, fusidic acid (2) | 1 |
| philomelos) | β-lactams, macrolides (2) | 1 | |
| Grey heron (Ardea cinerea) | 1 (0.8) | macrolides, aminoglycosides (2) | 1 |
| Great spotted woodpecker (Dendrocopos major) | 1 (0.8) | no resistance | 1 |
Nucleotide sequences and sizes of PCR products of amplified genes
| Gene | Oligonucleotide sequence (5′-3′) | Amplicon size (bp) | PCR conditions | Reference |
|---|---|---|---|---|
| mecA | AAAATCGATGGTAAAGGTTGGC AGTTCTGGCACTACCGGATTTGC | 533 | 94℃, 5 min, 40 cycles of 94℃ for 1 min, 58℃ for 1 min, 72℃ for 2 min, final extension 72℃ for 5 min | (23) |
| mecC | GAA AAA AAG GCT TAG AAC GCC TC GAA GAT CTT TTC CGT TTT CAG C | 138 | 94℃, 15 min, 30 cycles of 94℃ for 30 s, 59℃ for 1 min, 72℃ for 1 min, final extension for 10 min | (35) |
| blaZ ermA | ACTTCAACACCTGCTGCTTTC TAGGTTCAGATTGGCCCTTAG TCT AAAAAG CATGTAAAAGAA TGA TTATAATTATTT GATAGC TTC | 173 645 | 95℃, 3 min, 30 cycles of 95℃ for 30 s, 54℃ for 30 s, 72℃ for 30 s, final extension 72℃ for 4 min | (7) |
| ermB | TAACGACGAAACTGGCTAAAA ATCTGTGGTATGGCGGGTAAG | 416 | 95℃, 3 min, 30 cycles of 95℃ for 30 s, 55℃ for 30 s, 72℃ for 45 s, final extension 72℃ for 5 min | (36) |
| ermC | TAATCGTGGAATACGGGTTTG AATCGTCAATTCCTGCATGT | 299 | ||
| tetK | GTAGCGACAATAGGTAATAGT GTAGTGACAATAAACCTCCTA | 360 | ||
| tetM | CATATGTCCTGGCGTGTCTA AGTGGAGCGATTACAGAA | 158 | 94℃, 5 min, 30 cycles of 94℃ for 1 min, 57℃ for 1 min, 72℃ for 1 min, | (18) |
| tetL | ATAAATTGTTTCGGGTCGGTAAT AACCAGCCAACTAATGACAATGAT | 1077 | final extension 72℃ for 5 min | |
| tetO | AACTTAGGCATTCTGGCTCAC TCCCACTGTTCCATATCGTCA | 514 | ||
| msrA/B | GCAAATGGTGTAGGTAAGACAACT ATCATGTGATGTAAACAAAAT | 399 | 95℃, 3 min, 35 cycles of 93℃ for 30 s, 55℃ for 2 min, 74℃ for 1 min, final extension 72℃ 90 s | (36) |
| Aac(6′)/aph(2ʺ) | CAGAGCCTTGGGAAGATGAAG CCTCGTGTAATTCATGTTCTGGC | 348 | 94℃, 10 min, 35 cycles of 94℃ for 45 s, 60℃ for 60 s, 72℃ for 60 s, final extension cycle 72℃ for 5 min | (39) |
| norA | TTTGTTTTCAGTGTCAGAATTTATGTTTG GGCTTGGTGAAATATCAGCTATTAAAC | 140 | 94℃, 5 min, 30 cycles of 94℃ for 30 s, 60℃ for 30 s, 72℃ for 60 s, final extension 72℃ for 5 min | (26) |
| cfr | TGA AGT ATA AAG CAG GTT GGG AGT CA ACC ATA TAA TTG ACC ACA AGC AGC | 746 | 94℃, 2 min, 30 cycles of 94℃ for 30 s, 45℃ for 30 s, and 72℃ for 45 s, final extension 72℃ for 1 min | (13) |
| mphC | GAG ACT ACC AAG AAG ACC TGA CG CAT ACG CCG ATT CTC CTG AT | 530 | 95℃, 5 min, 35 cycles of 94℃ for 1 min, 59℃ for 1 min, 72℃ for 2 min, final extension 72℃ for 1 min | (16) |
| sea | TGCATGTTTTCAGAGTTAATC ACGATCAATTTTTACAGC | 544 | ||
| seb | TCTTTGTCGTAAGATAAACTTC GAATGATATTAATTCGCATC | 416 | 94℃, 5 min, 35 cycles of 94℃ for 2 min, 57℃ for 2 min, 72℃ for 1 min, | (22) |
| sec | GACATAAAAGCTAGGAATTT AAATCGGATTAACATTATCCA | 257 | final extension 72℃ for 7 min | |
| sed | TTACTAGTTTGGTAATATCTCCTT CCACCATAACAATTAATGC | 334 | ||
| see | ATAGATAAAGTTAAAACAAGCAA TAACTTACCGTGGACCC | 170 | ||
| tst | ACCCCTGTTCCCTTATCATC TTTTCAGTATTTGTAACGCC | 326 | ||
| pvl | ATCATTAGGTAAAATGTCTGGACATGATCCA GCATCAASTGTATTGGATAGCAAAAGC | 433 | 95℃, 5 min, 30 cycles of 94℃ for 1 min, 55℃ for 30 s, 72℃ for 1 min, | (38) |
| eta | GCAGGTGTTGATTTAGCATT AGATGTCCCTATTTTTGCTG | 93 | final extension at 72℃ for 5 min | |
| etb | ACAAGCAAAAGAATACAGCG GTTTTTGGCTGCTTCTCTTG | 226 |
Total number of birds and number and type of organs from which bacteria of the genus Staphylococcus were isolated
| Number of Staphylococcus strains isolated from individual organs or tissue | |||||||||
|---|---|---|---|---|---|---|---|---|---|
| Bird species | Total examined animals | Heart | Liver | Spleen | Tarsal joint | Conjunctiva | Palatal fissure | Yolk sac | Dead embryo |
| Capercaillie (Tetrao urogallus) | 73 | 5 | 5 | 9 | 4 | 5 | 7 | 9 | 13 |
| White stork (Ciconia ciconia) | 35 | 3 | 3 | 5 | 3 | 7 | 6 | - | - |
| Common pheasant(Phasianus colchicus) | 46 | 1 | 3 | 6 | 1 | 5 | 4 | 2 | - |
| Tawny owl (Strix aluco) | 10 | - | 1 | 2 | - | 1 | 2 | - | - |
| Common kestrel (Falco tinnunculus) | 8 | 1 | - | 2 | - | - | 2 | - | - |
| Common blackbird (Turdus merula) | 7 | - | - | - | 1 | 1 | 2 | - | - |
| Mute swan (Cygnus olor) | 5 | - | 1 | - | - | 1 | 1 | - | - |
| Song thrush (Turdus philomenos) | 5 | - | - | 1 | - | - | 2 | - | - |
| Grey heron (Ardea cinerea) | 2 | - | 1 | - | - | - | - | - | - |
| Great spotted woodpecker (Dendrocopos major) | 4 | - | - | 1 | - | - | - | - | - |
| Common buzzard (Buteo buteo) | 3 | - | - | - | - | - | - | - | - |
| Black grouse (Lyrurus tetrix) | 2 | - | - | - | - | - | - | - | - |
| Common swift (Apus apus) | 4 | - | - | - | - | - | - | - | - |
| Meadow pipit (Anthus pratensis) | 5 | - | - | - | - | - | - | - | - |
| Fieldfare (Turdus pilaris) | 4 | - | - | - | - | - | - | - | - |
| Lesser spotted eagle (Clanga pomarina) | 1 | - | - | - | - | - | - | - | - |
| Total | 214 | 10 | 14 | 26 | 9 | 20 | 26 | 11 | 13 |
Percentage of Staphylococcus strains isolated from individual bird species resistant to specific antibacterial agents
| Bird species | Number of strains | Antibiotic | ||||||||||||
|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
| AML25 | AMC30 | AMP10 | P10 | FOX30 | DA2 | C30 | E15 | CN10 | TE30 | SXT25 | ENR5 | FD5 | ||
| Capercaillie (Tetrao urogallus) | 57 | 12 21% | 7 12.3% | 21 36.8% | 18 31.6% | 9 15.8% | 23 40.4% | 4 7% | 19 33.3% | 4 7% | 14 24.6% | 11 19.3% | 26 45.6% | 20 35.1% |
| White stork (Ciconia ciconia) | 27 | 5 18.5% | 3 11.1% | 6 22.2% | 5 18.5% | 5 18.5% | 3 11.1% | 2 7.4% | 9 33.3% | 1 3.7% | 12 44.4% | 3 11.1% | 9 33.3% | 12 44.4% |
| Common pheasant (Phasianus colchicus) | 22 | 10 45.5% | 8 36.4% | 12 54.5% | 11 50.0% | 7 31.8% | 3 13.6% | 3 13.6% | 11 50.5% | - | 20 90/9% | 5 22.7% | 18 81.8% | 11 50.5% |
| Tawny owl (Strix aluco) | 6 | - | - | 1 16.7% | - | - | - | - | 1 16.7% | - | 1 16.7% | - | - | 1 16.7% |
| Common kestrel (Falco tinnunculus) | 5 | - | - | - | - | - | - | - | 20.01 % | - | - | - | 20.01 % | 20.01 % |
| Common blackbird (Turdus merula) | 4 | - | - | - | - | - | - | - | - | - | - | - | - | - |
| Mute swan (Cygnus olor) | 3 | 1 33.3% | 1 33.3% | 2 66.6% | 2 66.6% | 2 66.6% | - | - | - | - | - | - | 2 66.6% | 1 33.3% |
| Song thrush (Turdus philomenos) | 3 | - | 1 33.3% | 1 33.3% | 1 33.3% | - | - | - | 1 33.3% | - | - | - | 1 33.3% | 1 33.3% |
| Grey heron (Ardea cinerea) | 1 | - | - | - | - | - | - | - | 1 100% | 1 100% | - | - | - | - |
| Great spotted woodpecker (Dendrocopus major) | 1 | - | - | - | - | - | - | - | - | - | - | - | - | - |
Presence of genes encoding resistance to antimicrobial agents and staphylococcal toxins in isolated strains
| Staphylococcus species | |||||||||||||||||||||
|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
| Gene | S. sci (n=56) | S. xyl (n=14) | S. equ (n=12) | S. sap (n=8) | S. aur (n=6) | S. epi (n=6) | S. coh (n=6) | S. pse (n=3) | S. hae (n=3) | S. len (n=3) | S. klo (n=2) | S. suc (n=2) | S. vit (n=2) | S. con (n=1) | S. nep (n=1) | S. arl (n=1) | S. pas (n=1) | S. chr (n=1) | S. war (n=1) | Total | % |
| mecA | 7 | 1 | 1 | 9 | 7.0 | ||||||||||||||||
| mecC | |||||||||||||||||||||
| blaZ | 2 | 3 | 2 | 4 | 2 | 1 | 1 | 1 | 16 | 12.4 | |||||||||||
| msrA/B | 3 | 2 | 3 | 3 | 1 | 1 | 2 | 1 | 1 | 17 | 13.2 | ||||||||||
| ermA | 5 | 1 | 6 | 4.7 | |||||||||||||||||
| ermB | 12 | 1 | 2 | 1 | 2 | 2 | 1 | 21 | 16.3 | ||||||||||||
| ermC | 7 | 3 | 5 | 1 | 5 | 3 | 1 | 1 | 1 | 27 | 20.9 | ||||||||||
| tetK | 19 | 5 | 4 | 5 | 2 | 4 | 4 | 2 | 2 | 1 | 1 | 49 | 38.0 | ||||||||
| tetM | 16 | 7 | 5 | 3 | 3 | 1 | 1 | 1 | 1 | 1 | 1 | 40 | 31.0 | ||||||||
| tetL | 5 | 1 | 1 | 7 | 5.4 | ||||||||||||||||
| tetO | 3 | 1 | 1 | 1 | 1 | 7 | 5.4 | ||||||||||||||
| cfr | 1 | 1 | 1 | 1 | 1 | 5 | 3.9 | ||||||||||||||
| norA | 6 | 2 | 1 | 1 | 6 | 2 | 1 | 1 | 20 | 15.5 | |||||||||||
| aac(6′)/ aph(2ʺ) | 3 | 1 | 1 | 1 | 1 | 7 | 5.4 | ||||||||||||||
| mphC | 7 | 5 | 3 | 2 | 2 | 2 | 1 | 1 | 23 | 17.8 | |||||||||||
| sea | 1 | 1 | 1 | 3 | 2.3 | ||||||||||||||||
| seb | |||||||||||||||||||||
| sec | |||||||||||||||||||||
| sed | |||||||||||||||||||||
| see | |||||||||||||||||||||
| pvl | |||||||||||||||||||||
| eta | |||||||||||||||||||||
| etb | |||||||||||||||||||||
| tst | 1 | 1 | 0.8 | ||||||||||||||||||
| 129 | |||||||||||||||||||||
Phenotypic antimicrobial resistance of Staphylococcus strains
| Antibiotic | ||||||||||||||
|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
| Species | AML25 | AMC30 | AMP10 | P10 | FOX30 | DA2 | C30 | E15 | CN10 | TE30 | SXT25 | ENR5 | FD5 | |
| S. sciuri, n = 56 | R | 15 | 8 | 18 | 16 | 14 | 2 | 2 | - | 1 | 15 | 3 | 26 | 28 |
| I | - | - | - | - | - | 12 | - | 5 | 1 | 1 | - | - | - | |
| S. xylosus, n = 14 | R | 3 | 2 | 3 | 3 | 1 | - | 2 | 4 | - | 6 | 2 | 6 | 6 |
| I | - | - | - | - | - | 1 | 1 | 2 | - | - | - | - | - | |
| S. equorum, n = 12 | R | 1 | - | 1 | 1 | 1 | 1 | 2 | 2 | - | 3 | 1 | 1 | 2 |
| I | - | - | - | - | - | - | - | 3 | 1 | - | - | - | - | |
| S. saprophyticus, n = 8 | R | - | 1 | 2 | 1 | - | - | - | 5 | - | 7 | 2 | 5 | 1 |
| I | - | - | - | - | - | - | - | - | - | - | - | - | - | |
| S. aureus, n = 6 | R | 1 | 4 | 4 | 4 | - | - | - | - | - | - | - | 3 | 1 |
| I | - | - | - | - | - | 3 | - | 4 | - | - | - | - | - | |
| S. epidermidis, n = 6 | R | 1 | 1 | 4 | 3 | - | 3 | - | 4 | - | 4 | 5 | 5 | - |
| I | - | - | - | - | - | - | - | - | - | - | - | - | - | |
| S. cohnii, n = 6 | R | 3 | 1 | 3 | 2 | 3 | 2 | - | 3 | - | 3 | 2 | 3 | 2 |
| I | - | - | - | - | - | 1 | - | 2 | 1 | - | - | - | - | |
| S. pseudintermedius, n = 3 | R | 1 | 1 | 1 | 1 | - | 1 | 1 | 1 | - | 1 | - | 1 | - |
| I | - | - | - | - | - | - | - | 1 | - | - | - | - | - | |
| S. haemolyticus, n = 3 | R | 1 | - | 2 | 2 | 1 | 1 | - | 1 | 1 | 1 | 2 | 1 | 1 |
| I | - | - | - | - | - | - | - | - | - | - | - | - | - | |
| S. lentus, n = 3 | R | - | - | - | - | - | - | - | - | - | 1 | - | 1 | 1 |
| I | - | - | - | - | - | - | - | - | - | - | - | - | - | |
| S. kloosii, n = 2 | R | - | - | 1 | - | - | - | - | - | - | 1 | - | - | 1 |
| I | - | - | - | - | - | - | - | 1 | - | - | - | - | - | |
| S. succinus, n = 2 | R | - | - | - | - | - | - | - | 1 | - | - | - | - | - |
| I | - | - | - | - | - | - | - | - | - | - | - | - | - | |
| S. vitulinus, n = 2 | R | - | 1 | 1 | 1 | 1 | - | - | 1 | - | - | - | 1 | 1 |
| I | - | - | - | - | - | - | - | - | - | - | - | - | - | |
| S. condimenti, n =1 | R | 1 | - | 1 | 1 | 1 | 1 | 1 | - | - | - | - | 1 | 1 |
| I | - | - | - | - | - | - | - | 1 | 1 | 1 | 1 | - | - | |
| S. nepalensis, n = 1 | R | - | - | - | - | - | - | - | - | - | 1 | - | 1 | - |
| I | - | - | - | - | - | - | 1 | - | - | - | - | - | - | |
| S. arlettae, n = 1 | R | - | - | - | 1 | - | - | - | 1 | - | 1- | 1 | 1 | |
| I | - | - | - | - | - | - | - | - | - | - | - | - | - | |
| S. pasteuri, n = 1 | R | - | - | 1 | - | - | - | - | - | - | - | - | - | - |
| I | - | - | - | - | - | - | - | - | - | - | - | - | - | |
| S. chromogenes, n = 1 | R | 1 | 1 | 1 | 1 | 1 | 1 | - | 1 | - | 1 | 1 | 1 | 1 |
| I | - | - | - | - | - | - | - | - | - | - | - | - | - | |
| S. warneri, n = 1 | R | - | - | - | - | - | - | - | - | - | - | - | - | - |
| I | - | - | - | - | - | - | - | - | - | - | - | - | - | |
| Total number | 28 | 20 | 43 | 37 | 23 | 29 | 9 | 43 | 6 | 47 | 19 | 57 | 47 | |
| % | 21.7 | 15.5 | 33.3 | 28.7 | 17.8 | 22.5 | 7.0 | 33.3 | 4.7 | 36.4 | 14.7 | 44.2 | 36.4 | |