Antimicrobial Resistance, Virulence Factors, and Genotypes of Enterococcus faecalis and Enterococcus faecium Clinical Isolates in Northern Japan: Identification of optrA in ST480 E. faecalis
Abstract
:1. Introduction
2. Results
2.1. Bacterial Isolates
2.2. Prevalence of Virulence Factors
2.3. Prevalence and Profile of Antimicrobial Resistance and Resistance Determinants
2.4. Characterization of optrA Gene and Its Cluster
2.5. Genotypes of Isolates with Different Characteristics
3. Discussion
4. Materials and Methods
4.1. Clinical Isolates and Species Identification
4.2. Antibiotic Susceptibility Testing
4.3. Detection of Virulence Factors Genes
4.4. Detection of Drug Resistance Genes
4.5. Genetic Determinants of Oxazolidinone Resistance Isolate
4.6. Multilocus Sequence Typing (MLST), Phylogenetic Analysis
4.7. GenBank Accession Number
4.8. Statistical Analysis
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
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Virulence Factor Genes | E. faecalis n = 426 (%) | E. faecium n = 54 (%) |
---|---|---|
asa1 (Aggregation substance) | 252 (59.2) * | 0 (0) |
efaA (endocarditis antigen) | 209 (49.1) * | 1 (1.9) |
cylA (Cytolysin) | 147 (34.5) * | 0 (0) |
gelE (Gelatinase) | 248 (58.2) * | 0 (0) |
esp (Enterococcal surface protein) | 188 (44.1) | 26 (48.1) |
ace (Collagen-binding protein) | 197 (46.2) * | 0 (0) |
hyl (Hyaluronidase) | 0 (0) | 6 (11.1) * |
Tested Antibiotics/Resistance Genes | E. faecalis n = 426 (%) | E. faecium n = 54 (%) |
---|---|---|
Penicillin (PEN) | 0 (0) | 50 (92.6) *1 |
Ampicillin (AMP) | 0 (0) | 50 (92.6) *1 |
Ampicillin-Sulbactam (SAM) | 0 (0) | 50 (92.6) *1 |
Imipenem (IPM) | 0 (0) | 50 (92.6) *1 |
Minocycline (MIN) | 27 (6.3) | 2 (3.7) |
Erythromycin (ERY) | 212 (49.8) | 48 (88.9) *1 |
Levofloxacin (LVX) | 29 (6.8) | 52 (96.3) *1 |
High-level resistance to Gentamicin (GEN-HLR) | 54 (12.7) | 10 (18.5) |
Linezolid (LZD) | 1 *2 (0.2) | 0 (0) |
Rifampicin (RIF) | 54 (12.7) | 24 (44.4) *1 |
erm(B) | 184 (43.2) | 21 (38.9) |
msrC | 0 (0) | 30 (55.6) *1 |
aac(6′)-Ie-aph(2″)-Ia | 98 (23.0) | 9 (16.7) |
aph(3′)-IIIa | 93 (21.8) *1 | 2 (3.7) |
ant(6)-Ia | 6 (1.4) | 0 (0) |
ant(9)-Ia | 1 (0.2) | 0 (0) |
optrA | 1 (0.2) | 0 (0) |
fexA | 1 (0.2) | 0 (0) |
erm(A), erm(C), erm(F), erm(G), erm(Q), erm(T), erm(X), erm(Y), lunA, lnuB, lsaA, mefA/E, msrA, msrB, vanA, vanB, vanD, vanM, poxtA, cfr | 0 (0) | 0 (0) |
Drug Resistance Determinants *1 | E. faecalis | E. faecium |
---|---|---|
Macrolide resistance gene | n = 212 (%) | n = 48 (%) |
erm(B) only | 184 (86.8) *2 | 18 (37.5) |
erm(B) + msrC | 0 (0) | 3 (6.2) *2 |
msrC only | 0 (0) | 27 (56.3) *2 |
Aminoglycoside modifying enzyme gene | n = 170 *3 (%) | n = 10 (%) |
aac(6′)-Ie-aph(2″)-Ia | 26 (15.3) | 8 (80.0) *2 |
aph(3′)-IIIa | 19 (11.2) | 1 (10.0) |
aph(3′)-IIIa, ant(6)-Ia | 2 (1.2) | 0 (0) |
aac(6′)-Ie-aph(2″)-Ia+aph(3′)-IIIa | 67 (39.4) | 1 (10.0) |
aac(6′)-Ie-aph(2″)-Ia+aph(3′)-IIIa+ant(6)-Ia | 4 (2.4) | 0 (0) |
aac(6′)-Ie-aph(2″)-Ia+aph(3′)-IIIa+ant(9)-Ia | 1 (0.6) | 0 (0) |
Mutation in QRDR (GyrA/ParC) | n = 29 (%) | n = 52 (%) |
S84I/S82I | 18 (62.1) *2 | 9 (17.3) |
S84Y/S82I | 7 (24.1) | 17 (32.7) |
S84I/S82R | 0 (0) | 21 (40.4) *2 |
S84Y/S82R | 0 (0) | 2 (3.8) |
S84F/S82R | 0 (0) | 1 (1.9) |
E88G/S82I | 1 (3.4) | 0 (0) |
S84Y, E88G/S82I | 0 (0) | 1 (1.9) |
NM/S82I | 2 (6.9) | 1 (1.9) |
NM/E86K | 1 (3.4) | 0 (0) |
Isolate ID | Specimen | Age/Sex | Patient Type | Virulence Factors | Antimicrobial Resistance Profile *1 | Antimicrobial Resistance Genes | QRDR Mutation *2 | ST (CC) | Allelic Profile | |
---|---|---|---|---|---|---|---|---|---|---|
GyrA | ParC | |||||||||
ES 9 | sputum | 79/M | Inpatient | asa1, efaA, cylA, gelE, esp, ace | ERY | erm(B) | NM | NM | ST179 (CC16) | 5-1-1-3-7-1-6 |
ES 10 | urine | 52/F | Outpatient | asa1, efaA, cylA, esp, ace | ERY, GEN-HLR | erm(B), aac(6′)-Ie-aph(2″)-Ia, aph(3′)-IIIa | NM | NM | ST179 (CC16) | 5-1-1-3-7-1-6 |
ES 12 | urine | 82/F | Outpatient | efaA, cylA, gelE | LVX | NM | S82I | ST741 | 15-2-3-88-17-15-11 | |
ES 14 | urine | 28/F | Inpatient | asa1, efaA, cylA, gelE, ace | ERY, MIN, GEN-HLR | erm(B), aac(6′)-Ie-aph(2″)-Ia, aph(3′)-IIIa | NM | NM | ST16 (CC16) | 5-1-1-3-7-7-6 |
ES 16 | urine | 96/M | Inpatient | asa1, efaA, cylA, gelE, ace | All susceptible | NM | NM | ST179 (CC16) | 5-1-1-3-7-1-6 | |
ES 27 | urine | 69/M | Outpatient | ERY, LVX | erm(B) | S84Y | S82I | ST895 (ST480 SLV *1) | 5-1-22-22-7-17-6 | |
ES 36 | urine | 83/F | Outpatient | asa1, cylA, gelE | ERY, GEN-HLR | erm(B), aac(6′)-Ie-aph(2″)-Ia, aph(3′)-IIIa | NM | NM | ST179 (CC16) | 5-1-1-3-7-1-6 |
ES 86 | urine | 95/M | Inpatient | asa1, efaA, cylA, esp, ace | ERY | erm(B) | E88G | S82I | ST16 (CC16) | 5-1-1-3-7-7-6 |
ES 94 | urine | 86/F | Outpatient | asa1, efaA, gelE, esp, ace | ERY, LVX, MIN, GEN-HLR | erm(B), aac(6′)-Ie-aph(2″)-Ia, aph(3′)-IIIa, ant(6)-Ia | S84I | S82I | ST1296 *3 | 5-2-3-6-17-1-11 |
ES 101 | urine | 83/M | Outpatient | asa1, efaA, gelE, ace | ERY, LVX | aph(3′)-IIIa | NM | E86K | ST179 (CC16) | 5-1-1-3-7-1-6 |
ES 103 | pus | 82/F | Inpatient | ERY, LVX, GEN-HLR | erm(B), aac(6′)-Ie-aph(2″)-Ia, aph(3′)-IIIa, ant(6)-Ia | S84I | S82I | ST4 (CC4) | 8-7-7-5-4-4-1 | |
ES 116 | venous blood | 73/M | Inpatient | ERY, LVX, GEN-HLR | erm(B), aac(6′)-Ie-aph(2″)-Ia, aph(3′)-IIIa | S84Y | S82I | ST16 (CC16) | 5-1-1-3-7-7-6 | |
ES 120 | urine | 48/F | Outpatient | All susceptible | NM | NM | ST16 (CC16) | 5-1-1-3-7-7-6 | ||
ES 135 | Vaginal discharge | 32/F | Outpatient | asa1, efaA, cylA, gelE, esp, ace | ERY | erm(B), aac(6′)-Ie-aph(2″)-Ia, aph(3′)-IIIa | NM | NM | ST179 (CC16) | 5-1-1-3-7-1-6 |
ES 141 | urine | 54/M | Outpatient | asa1, efaA, cylA, gelE, esp, ace | ERY, LVX | erm(B) | S84I | S84I | ST1296 *3 | 5-2-3-6-17-1-11 |
ES 151 | urine | 39/F | Inpatient | efaA, gelE, ace | ERY | erm(B) | NM | NM | ST40 (CC40) | 3-6-23-12-9-10-7 |
ES 153 | urine | 96/F | Outpatient | asa1, efaA, cylA, gelE, esp, ace | ERY, GEN-HLR | erm(B), aac(6′)-Ie-aph(2″)-Ia, aph(3′)-IIIa | NM | NM | ST179 (CC16) | 5-1-1-3-7-1-6 |
ES 172 | urine | 80/F | Inpatient | asa1, gelE, esp, ace | All susceptible | NM | NM | ST40 (CC40) | 3-6-23-12-9-10-7 | |
ES 174 | urine | 11/M | Outpatient | gelE, esp, ace | ERY, GEN-HLR | erm(B), aac(6′)-Ie-aph(2″)-Ia, aph(3′)-IIIa | NM | NM | ST179 (CC16) | 5-1-1-3-7-1-6 |
ES 179 | urine | 80/F | Outpatient | gelE, esp | LVX | S84I | S82I | ST1296 *3 | 5-2-3-6-17-1-11 | |
ES 180 | urine | 87/F | Inpatient | ERY, LVX, GEN-HLR | erm(B), aac(6′)-Ie-aph(2″)-Ia, aph(3′)-IIIa | S84I | S82I | ST1296 *3 | 5-2-3-6-17-1-11 | |
ES 203 | urine | 94/F | Inpatient | asa1, efaA, gelE, esp, ace | LVX | S84I | S82I | ST28 (CC28) | 4-4-8-3-8-1-3 | |
ES 218 | urine | 82/F | Inpatient | asa1, efaA, cylA, gelE, esp | ERY, LVX | erm(B) | S84I | S82I | ST1296 *3 | 5-2-3-6-17-1-11 |
ES 223 | catheter tip | 72/M | Inpatient | asa1, efaA, cylA, gelE, esp, ace | ERY | erm(B) | NM | NM | ST179 (CC16) | 5-1-1-3-7-1-6 |
ES 236 | urine | 80/M | Inpatient | asa1, efaA, cylA, gelE, esp, ace | LVX | S84I | S82I | ST28 (CC28) | 4-4-8-3-8-1-3 | |
ES 239 | urine | 68/M | Outpatient | asa1, efaA, cylA | ERY, GEN-HLR | aac(6′)-Ie-aph(2″)-Ia | NM | NM | ST6 (CC6) | 12-7-3-7-6-1-5 |
ES 290 | urine | 94/F | Inpatient | efaA | All susceptible | NM | NM | ST1305 *3 | 9-6-11-72-78-1-22 | |
ES 297 | Vaginal discharge | 44/F | Outpatient | asa1, efaA, cylA, gelE, esp, ace | ERY | NM | NM | ST179 (CC16) | 5-1-1-3-7-1-6 | |
ES 334 | Vaginal discharge | 15/F | Outpatient | asa1, efaA, cylA, gelE, esp | ERY | NM | NM | ST179 (CC16) | 5-1-1-3-7-1-6 | |
ES 360 | pus | 25/F | Outpatient | efaA, gelE, esp | RIF | NM | NM | ST191 | 27-1-11-1-21-1-2 | |
ES443 | urine | 74/F | Outpatient | asa1, efaA, esp | ERY, LVX, LZD, CHL, FFC | erm(B), aac(6′)-Ie-aph(2″)-Ia, aph(3′)-IIIa,ant(9)-Ia, optrA, fexA | S84Y | S82I | ST480 | 1-1-22-22-7-17-6 |
Isolate ID | Specimen | Age/Sex | Patient Type | Virulence Factors | Antimicrobial Resistance Profile *1 | Antimicrobial Resistance Genes | QRDR Mutation *2 | ST (CC) | Allelic Profile | |
---|---|---|---|---|---|---|---|---|---|---|
GyrA | ParC | |||||||||
ES 11 | bile | 92/M | Inpatient | esp | ERY, LVX | msrC | S84I | S82R | ST17 (CC17) | 1-1-1-1-1-1-1 |
ES 13 | urine | 93/F | Inpatient | esp | ERY, LVX, RIF | msrC | S84I | S82R | ST17 (CC17) | 1-1-1-1-1-1-1 |
ES 17 | urine | 55/F | Outpatient | hyl | ERY, LVX, RIF | msrC | S84Y | S82I | ST389 (CC17) | 1-5-1-1-1-1-3 |
ES 31 | CVC *1 | 77/M | Inpatient | hyl | ERY, LVX, RIF | msrC | S84Y | S82I | ST18 (CC17) | 7-1-1-1-5-1-1 |
ES 32 | urine | 80/F | Inpatient | esp | ERY, LVX, RIF | msrC | S84I | S82R | ST17 (CC17) | 1-1-1-1-1-1-1 |
ES 35 | urine | 88/F | Inpatient | esp | ERY, LVX, RIF | msrC | S84I | S82R | ST17 (CC17) | 1-1-1-1-1-1-1 |
ES 39 | urine | 90/M | Inpatient | esp | ERY, LVX | erm(B) | S84I | S82R | ST17 (CC17) | 1-1-1-1-1-1-1 |
ES 56 | urine | 80/F | Inpatient | esp | ERY, LVX, GEN-HLR, RIF | aac(6′)-Ie-aph(2″)-Ia | S84Y | S82I | ST17 (CC17) | 1-1-1-1-1-1-1 |
ES 61 | urine | 91/F | Inpatient | esp | GEN-HLR, RIF | aac(6′)-Ie-aph(2″)-Ia | S84Y | S82I | ST17 (CC17) | 1-1-1-1-1-1-1 |
ES 64 | urine | 90/F | Inpatient | esp | ERY, LVX | erm(B) | S84I | S82R | ST17 (CC17) | 1-1-1-1-1-1-1 |
ES 66 | urine | 83/M | Inpatient | esp | ERY, LVX | erm(B) | S84I | S82R | ST17 (CC17) | 1-1-1-1-1-1-1 |
ES 98 | venous blood | 77/M | Inpatient | esp | ERY, LVX, RIF | erm(B) | S84I | S82R | ST2263 *3 (CC17) | 1-1-1-1-1-1-4 |
ES 102 | urine | 85/M | Outpatient | esp | ERY, LVX | msrC | S84I | S82I | ST78 (CC17) | 15-1-1-1-1-1-1 |
ES 106 | urine | 82/F | Inpatient | ERY, LVX | msrC | S84I | S82I | ST18 (CC17) | 7-1-1-1-5-1-1 | |
ES 109 | urine | 90/M | Inpatient | ERY, LVX, GEN-HLR, RIF | erm(B), aac(6′)-Ie-aph(2″)-Ia | S84Y | S82I | ST17 (CC17) | 1-1-1-1-1-1-1 | |
ES 117 | bile | 86/F | Inpatient | ERY, LVX | msrC | S84I | S82I | ST17 (CC17) | 1-1-1-1-1-1-1 | |
ES 132 | urine | 81/F | Inpatient | esp | ERY, LVX | erm(B) | S84I | S82I | ST17 (CC17) | 1-1-1-1-1-1-1 |
ES 140 | bile | 77/M | Inpatient | RIF | NM | NM | ST2264 *3 | 25-15-9-33-10-19-6 | ||
ES 144 | urine | 75/F | Inpatient | ERY, LVX, MIN, RIF | erm(B), msrC | S84Y | S82I | ST78 (CC17) | 15-1-1-1-1-1-1 | |
ES 146 | urine | 82/M | Inpatient | esp | ERY, LVX | erm(B) | S84I | S82I | ST17 (CC17) | 1-1-1-1-1-1-1 |
ES 148 | urine | 85/M | Inpatient | esp | ERY, LVX | erm(B) | S84I | S82R | ST17 (CC17) | 1-1-1-1-1-1-1 |
ES 150 | urine | 91/F | Inpatient | esp | ERY, LVX, GEN-HLR, RIF | erm(B), aac(6′)-Ie-aph(2″)-Ia | S84Y | S82I | ST17 (CC17) | 1-1-1-1-1-1-1 |
ES 166 | urine | 90/F | Inpatient | ERY, LVX, RIF | erm(B) | S84Y | S82I | ST78 (CC17) | 15-1-1-1-1-1-1 | |
ES 170 | venous blood | 77/M | Inpatient | ERY, LVX, RIF | msrC | S84Y | S82I | ST78 (CC17) | 15-1-1-1-1-1-1 | |
ES 171 | oral cavity | 77/F | Inpatient | esp | LVX, GEN-HLR, RIF | aac(6′)-Ie-aph(2″)-Ia | S84Y | S82I | ST17 (CC17) | 1-1-1-1-1-1-1 |
ES 195 | urine | 87/F | Outpatient | ERY, LVX | erm(B) | S84I | S82R | ST17 (CC17) | 1-1-1-1-1-1-1 | |
ES 196 | urine | 78/M | Inpatient | LVX | S84Y | S82I | ST17 (CC17) | 1-1-1-1-1-1-1 | ||
ES 209 | bile | 83/M | Inpatient | ERY, LVX | erm(B) | S84I | S82R | ST17 (CC17) | 1-1-1-1-1-1-1 | |
ES 211 | urine | 92/M | Inpatient | LVX, MIN, GEN-HLR, RIF | aac(6′)-Ie-aph(2″)-Ia | S84Y | S82I | ST17 (CC17) | 1-1-1-1-1-1-1 | |
ES 215 | drain fluid | 76/M | Inpatient | esp | ERY, LVX, RIF | erm(B) | S84I | S82R | ST17 (CC17) | 1-1-1-1-1-1-1 |
ES 217 | urine | 77/M | Inpatient | esp | ERY, LVX, RIF | erm(B) | S84I | S82R | ST17 (CC17) | 1-1-1-1-1-1-1 |
ES 225 | urine | 89/F | Inpatient | ERY, LVX, SXT | erm(B) | S84Y, E88G | S82I | ST17 (CC17) | 1-1-1-1-1-1-1 | |
ES 231 | urine | 90/F | Outpatient | ERY, LVX, GEN-HLR, RIF | msrC, aac(6′)-Ie-aph(2″)-Ia | S84Y | S82I | ST2267 *3 (CC17) | 1-158-1-1-1-1-1 | |
ES 240 | pus | 75/F | Inpatient | ERY, LVX, RIF | erm(B) | S84I | S82R | ST78 (CC17) | 15-1-1-1-1-1-1 | |
ES 246 | urine | 80/F | Inpatient | esp, hyl | ERY, LVX | erm(B), msrC | S84I | S82I | ST78 (CC17) | 15-1-1-1-1-1-1 |
ES 254 | urine | 89/F | Inpatient | ERY, LVX, GEN-HLR, RIF | erm(B), msrC, aph(3′)-IIIa | S84Y | S82I | ST252 (CC17) | 1-5-1-1-1-1-1 | |
ES 264 | urine | 89/F | Inpatient | esp | ERY, LVX | msrC | S84I | S82R | ST203 (CC17) | 15-1-1-1-1-20-1 |
ES 279 | urine | 96/F | Inpatient | ERY, LVX | msrC | S84I | S82R | ST17 (CC17) | 1-1-1-1-1-1-1 | |
ES 280 | urine | 73/M | Inpatient | hyl | ERY, LVX | msrC | S84I | S82I | ST78 (CC17) | 15-1-1-1-1-1-1 |
ES 288 | urine | 82/F | Inpatient | esp | ERY, LVX | msrC | S84Y | S82R | ST17 (CC17) | 1-1-1-1-1-1-1 |
ES 289 | urine | 83/F | Inpatient | ERY, LVX | msrC | S84Y | S82I | ST78 (CC17) | 15-1-1-1-1-1-1 | |
ES 302 | urine | 74/M | Inpatient | esp | ERY, LVX | msrC | S84Y | S82R | ST17 (CC17) | 1-1-1-1-1-1-1 |
ES 303 | IVH tube | 92/F | Inpatient | esp | ERY, LVX | msrC | S84I | S82R | ST17 (CC17) | 1-1-1-1-1-1-1 |
ES 319 | urine | 63/M | Inpatient | ERY, LVX | msrC | S84Y | S82I | ST1693 (CC17) | 9-1-1-1-5-7-1 | |
ES 339 | urine | 77/F | Inpatient | esp | ERY, LVX | msrC | S84I | S82R | ST17 (CC17) | 1-1-1-1-1-1-1 |
ES 348 | urine | 92/F | Inpatient | ERY, LVX, RIF | msrC | S84I | S82R | ST17 (CC17) | 1-1-1-1-1-1-1 | |
ES 359 | urine | 50/F | Outpatient | RIF | NM | NM | ST94 (CC94) | 13-8-8-8-6-10-6 | ||
ES 393 | urine | 77/F | Inpatient | ERY, LVX | msrC | S84I | S82I | ST78 (CC17) | 15-1-1-1-1-1-1 | |
ES 407 | urine | 78/M | Inpatient | esp | ERY, LVX | msrC | S84F | S82R | ST187 (CC17) | 31-1-1-1-1-1-1 |
ES 410 | urine | 86/F | Inpatient | esp | ERY, LVX | msrC | S84I | S82R | ST17 (CC17) | 1-1-1-1-1-1-1 |
ES 434 | urine | 91/F | Inpatient | hyl | ERY, LVX | erm(B) | S84I | S82I | ST18 (CC17) | 7-1-1-1-5-1-1 |
ES 421 | urine | 90/M | Inpatient | efaA | ERY, LVX, GEN-HLR | erm(B), aac(6′)-Ie-aph(2″)-Ia | NM | S82I | ST17 (CC17) | 1-1-1-1-1-1-1 |
ES 441 | urine | 75/M | Inpatient | ERY, LVX, RIF | msrC | S84Y | S82I | ST17 (CC17) | 1-1-1-1-1-1-1 | |
ES 450 | urine | 78/M | Outpatient | hyl | ERY, LVX, GEN-HLR | msrC, aac(6′)-Ie-aph(2″)-Ia, aph(3′)-IIIa | S84I | S82I | ST78 (CC17) | 15-1-1-1-1-1-1 |
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Aung, M.S.; Urushibara, N.; Kawaguchiya, M.; Ohashi, N.; Hirose, M.; Kudo, K.; Tsukamoto, N.; Ito, M.; Kobayashi, N. Antimicrobial Resistance, Virulence Factors, and Genotypes of Enterococcus faecalis and Enterococcus faecium Clinical Isolates in Northern Japan: Identification of optrA in ST480 E. faecalis. Antibiotics 2023, 12, 108. https://doi.org/10.3390/antibiotics12010108
Aung MS, Urushibara N, Kawaguchiya M, Ohashi N, Hirose M, Kudo K, Tsukamoto N, Ito M, Kobayashi N. Antimicrobial Resistance, Virulence Factors, and Genotypes of Enterococcus faecalis and Enterococcus faecium Clinical Isolates in Northern Japan: Identification of optrA in ST480 E. faecalis. Antibiotics. 2023; 12(1):108. https://doi.org/10.3390/antibiotics12010108
Chicago/Turabian StyleAung, Meiji Soe, Noriko Urushibara, Mitsuyo Kawaguchiya, Nobuhide Ohashi, Mina Hirose, Kenji Kudo, Naoyuki Tsukamoto, Masahiko Ito, and Nobumichi Kobayashi. 2023. "Antimicrobial Resistance, Virulence Factors, and Genotypes of Enterococcus faecalis and Enterococcus faecium Clinical Isolates in Northern Japan: Identification of optrA in ST480 E. faecalis" Antibiotics 12, no. 1: 108. https://doi.org/10.3390/antibiotics12010108