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Abstract
Background
In Korea, a sudden increase in vancomycin-resistant enterococci (VRE) infection has been noted since the late 1990s. This study was conducted to describe the antimicrobial resistances of enterococcal blood isolates and to identify risk factors associated with VRE bacteremia in a tertiary care university hospital over a recent five-year period.
Methods
This study was conducted to analyze the antimicrobial susceptibilities of enterococcal blood isolates by year from January 2003 to December 2007. Multivariate logistic regression analysis was used to investigate factors associated with VRE bacteremia.
Results
A total of 225 enterococcal strains (44.7% Enterococcus faecalis, 42.4% Enterococcus facium, 5.9% Enterococcus casseliflavus, and 4.7% Enterococcus gallinarum) were detected in blood, 55 of which (21.6%) were resistant to vancomycin. In 2004 and 2005, the resistance rates for vancomycin and teicoplanin (33.3% and 27.3%; 34.4% and 23.0%, respectively) increased. In 2003, 2006, and 2007, the resistance rates for vancomycin and teicoplanin (8.7% and 8.7%; 19.0% and 14.3%; 13.5% and 11.5%, respectively) decreased relative to those of the previous years. When 55 patients with VRE bacteremia were compared with 55 patients with vancomycin-susceptible enterococcal bacteremia using multivariate analysis, E. faecium bacteremia (OR 12.624, P＜0.001) and enterococcal bacteremia caused by species other than E. faecium and E. faecalis (OR 21.473, P=0.011) were found to be statistical risk factors. Among several infection control activities, the restricted uses of vancomycin and quinupristin-dalfopristin decreased the vancomycin resistance rate from 27.78% to 15.50% (P=0.0257).
REFERENCES
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Table 1.
Distribution of enterococcal species in blood culture according to years
| Year | No. (%) of Enterococcus species recovered | ||||
|---|---|---|---|---|---|
| E. faecalis | E. faecium | E. casseliflavus | E. gallinarum | Other species∗ | |
| 2003 (N=46) | 25 (54.3) | 19 (41.3) | 0 (0.0) | 2 (4.3) | 0 (0.0) |
| 2004 (N=33) | 13 (39.4) | 18 (54.5) | 0 (0.0) | 0 (0.0) | 2 (6.1) |
| 2005 (N=61) | 20 (32.8) | 34 (55.7) | 3 (4.9) | 4 (6.6) | 0 (0.0) |
| 2006 (N=63) | 27 (42.9) | 24 (38.1) | 5 (7.9) | 6 (9.5) | 1 (1.6) |
| 2007 (N=52) | 29 (55.8) | 13 (25.0) | 7 (13.5) | 0 (0.0) | 3 (5.8) |
| Total (N=255) | 114 (44.7) | 108 (42.4) | 15 (5.9) | 12 (4.7) | 6 (2.4) |
Table 2.
Antimicrobial resistance rates of enterococcal isolates
| Antimicrobial agent | E. faecalis (N=114) % (N) | E. faecium (N=108) % (N) | E. casseliflavus (N=15) % (N) | E. gallinarum (N=12) % (N) | Other species∗ (N=6) % (N) | Total (N=255) % (N) |
|---|---|---|---|---|---|---|
| Ampicillin | 3.5 (4/114) | 79.6 (86/108) | 80.0 (12/15) | 100.0 (12/12) | 33.3 (2/6) | 45.5 (116/255) |
| Penicillin G | 23.1 (15/65) | 86.2 (50/58) | 86.7 (13/15) | 100.0 (10/10) | 50.0 (2/4) | 59.2 (90/152) |
| Vancomycin | 7.9 (9/114) | 37.0 (40/108) | 13.3 (2/15) | 33.3 (4/12) | 0.0 (0/6) | 21.6 (55/255) |
| Teicoplanin | 7.9 (9/114) | 26.9 (29/108) | 13.3 (2/15) | 16.7 (2/12) | 0.0 (0/6) | 16.5 (42/255) |
| Erythromycin | 77.9 (74/95) | 94.7 (72/76) | 85.7 (12/14) | 100.0 (5/5) | 50.0 (1/6) | 83.7 (164/196) |
| Ciprofloxacin | 53.5 (61/114) | 90.7 (98/108) | 80.0 (12/15) | 100.0 (12/12) | 16.7 (0/6) | 71.8 (783/255) |
| Quinupristin-dalfopri | stin NT | 8.6 (5/58) | 20.0 (3/15) | 0.0 (0/10) | 50.0 (2/4) | 11.5 (10/87) |
| Linezolid | 0.0 (0/21) | 0.0 (0/32) | 33.3 (1/3) | 0.0 (0/8) | NT | 1.6 (1/64) |
| Tetracycline | 76.6 (59/77) | 23.0 (17/74) | 6.7 (1/15) | 30.0 (3/10) | 33.3 (2/6) | 45.1 (82/182) |
Table 3.
Glycopeptides, quinupristin-dalfopristin, and linezolid resistance of enterococcal isolates according to years
| Antimicrobial agents | Enterococci species | Resistance rates according to year, % (N) | |||||
|---|---|---|---|---|---|---|---|
| 2003 (N=46) | 2004 (N=33) | 2005 (N=61) | 2006 (N=63) | 2007 (N=52) | Total (N=255) | ||
| Vancomycin | E. faecalis | 4.0 (1/25) | 15.4 (2/13) | 15.0 (3/20) | 3.7 (1/27) | 6.9 (2/29) | 7.9 (9/114) |
| E. faecium | 15.8 (3/19) | 50.0 (9/18) | 44.1 (15/34) | 33.3 (8/24) | 38.5 (5/13) | 37.0 (40/108) | |
| E. casseliflavus | − | − | 33.3 (1/3) | 20.0 (1/5) | 0.0 (0/7) | 13.3 (2/15) | |
| E. gallinarum | 0.0 (0/2) | − | 50.0 (2/4) | 33.3 (2/6) | − | 33.3 (4/12) | |
| Other species∗ | − | 0.0 (0/2) | − | 0.0 (0/1) | 0.0 (0/3) | 0.0 (0/6) | |
| Total | 8.7 (4/46) | 33.3 (11/33) | 34.4 (21/61) | 19.0 (12/63) | 13.5 (7/52) | 21.6 (55/255) | |
| Teicoplanin | E. faecalis | 4.0 (1/25) | 15.4 (2/13) | 15.0 (3/20) | 3.7 (1/27) | 6.9 (2/29) | 7.9 (9/114) |
| E. faecium | 15.8 (3/19) | 38.9 (7/18) | 29.4 (10/34) | 20.8 (5/24) | 30.7 (4/13) | 26.9 (29/108) | |
| E. casseliflavus | − | − | 33.3 (1/3) | 20.0 (1/5) | 0.0 (0/7) | 13.3 (2/15) | |
| E. gallinarum | 0.0 (0/2) | − | 0.0 (0/4) | 33.3 (2/6) | − | 16.7 (2/12) | |
| Other species∗ | − | 0.0 (0/2) | − | 0.0 (0/1) | 0.0 (0/3) | 0.0 (0/6) | |
| Total | 8.7 (4/46) | 27.3 (9/33) | 23.0 (14/61) | 14.3 (9/63) | 11.5 (6/52) | 16.5 (42/255) | |
| Quinupristin-dalfopristin | E. faecalis | NT | NT | NT | NT | NT | NT |
| E. faecium | NT | NT | 4.2 (1/24) | 8.7 (2/23) | 18.2 (2/11) | 8.6 (5/58) | |
| E. casseliflavus | NT | NT | 33.3 (1/3) | 20.0 (1/5) | 14.3 (1/7) | 20.0 (3/15) | |
| E. gallinarum | NT | NT | 0.0 (0/4) | 0.0 (0/6) | − | 0.0 (0/10) | |
| Other species∗ | NT | NT | − | 100.0 (1/1) | 33.3 (1/3) | 50.0 (2/4) | |
| Total | NT | NT | 6.5 (2/31) | 11.4 (4/35) | 19.0 (4/21) | 11.5 (10/87) | |
| Linezolid | E. faecalis | NT | NT | 0.0 (0/13) | 0.0 (0/6) | 0.0 (0/2) | 0.0 (0/21) |
| E. faecium | NT | NT | 0.0 (0/24) | 0.0 (0/7) | 0.0 (0/1) | 0.0 (0/32) | |
| E. casseliflavus | NT | NT | 33.3 (1/3) | NT | NT | 33.3 (1/3) | |
| E. gallinarum | NT | NT | 0.0 (0/4) | 0.0 (0/4) | − | 0.0 (0/8) | |
| Other species∗ | NT | NT | − | NT | NT | NT | |
| Total | NT | NT | 2.3 (1/44) | 0.0 (0/17) | 0.0 (0/3) | 1.6 (1/64) | |
Table 4.
Univariate analysis of demographic and clinical data between patients with vancomycin-resistant enterococcal (VRE bacteremia and those with vancomycin susceptible enterococca (VSE) bacteremia
| Variables | VRE (N=55)∗ | VSE (N=55)∗ | P† |
|---|---|---|---|
| Gender, M: F | 27: 28 | 29: 26 | 0.849 |
| Age in years, mean±SD | 59.69±19.31 | 61.07±18.38 | 0.701 |
| Ward | |||
| ICU | 28 | 32 | 0.792 |
| MICU | 10 | 12 | 0.792 |
| SICU | 6 | 5 | |
| NICU | 12 | 15 | |
| Non-ICU | 27 | 23 | |
| Hemato-onco ward | 3 | 1 | |
| General ward | 24 | 22 | |
| Hospital stay (day), mean±SD | 64.45±66.38 | 63.05±49.93 | 0.889 |
| Invasive procedure | |||
| Urinary catheter | 444 | 49 | 0.291 |
| Central line | 34 | 34 | 1.000 |
| Ventilator | 33 | 21 | 0.035‡ |
| L-tube | 36 | 38 | 0.839 |
| Surgery Underlying disease | 25 | 26 | 1.000 |
| Diabetes mellitus | 12 | 19 | 0.203 |
| Hypertension | 17 | 22 | 0.426 |
| Tuberculosis | 3 | 1 | 0.618 |
| Cancer | 6 | 5 | 1.000 |
| Renal insufficiency | 9 | 8 | 1.000 |
| Polymicrobial infection | 50 | 42 | 0.069 |
| Polymicrobial bacteremia | 6 | 5 | 1.000 |
| Causative organism | |||
| E. faecium | 43 | 23 | ＜0.001‡ |
| E. faecalis | 6 | 30 | |
| Other species | 6 | 2 | |
| Known source of bacteremia | 12 | 4 | 0.056 |
| Urinary tract | 4 | 4 | |
| Gastointesital tract | 5 | 0 | |
| Others | 3 | 0 | |
| MRSA co-infection | 14 | 10 | 0.489 |
| Prior exposure with antibiotics | |||
| Vancomycin | 31 | 12 | ＜0.001‡ |
| Quinolone | 20 | 21 | 1.000 |
| Imipenem | 9 | 1 | 0.016‡ |
| Penicillin | 28 | 15 | 0.019‡ |
| Cephalosporin | 42 | 36 | 0.294 |
| Aminoglycoside | 30 | 26 | 0.567 |
| Clindamycin | 12 | 12 | 1.000 |
∗ We used the Charlson comorbidity index to evaluate the disease severity and comorbidity in VRE group and VSE group. There were not statistically different in disease severity and comorbidity between VRE group and VSE group (Weighted index comorbidity: P=0.7418 t-test; Combined condition and age related score: P=0.5240, t-test)
Table 5.
Univariate analysis of laboratory data between patients with vancomycin-resistant enterococcal (VRE) bacteremia and those with vancomycin susceptible enterococcal (VSE) bacteremia
| Variables | VRE (N=55)∗ mean±SD (range) | VSE (N=55)∗ mean±SD (range) | P† |
|---|---|---|---|
| ALP (IU/L) Total protein (g/dL) | 108.96±80.5 (31.0∼387.0) 5.60±0.85 (3.9∼7.6) | 118.80±124.81 (23.0∼607.0) 5.56±0.95 (3.9∼7.8) | 0.650 0.830 |
| Albumin (g/dL) | 2.69±0.56 (1.6∼4.0) | 2.64±0.56 (1.8∼3.9) | 0.696 |
| AST (IU/L) | 61.15±66.18 (10.0∼342.0) | 44.20±27.44 (14.0∼116.0) | 0.116 |
| ALT (IU/L) | 44.27±53.91 (3.0∼370.0) | 37.82±43.92 (4.0∼292.0) | 0.527 |
| BUN (mg/dL) | 29.38±27.32 (4.0∼153.0) | 37.18±37.13 (1.0∼156.0) | 0.212 |
| Creatinine (mg/dL) | 1.09±0.86 (0.2∼5.0) | 1.59±1.82 (0.3∼10.1) | 0.071 |
| Sodium (mmol/L) | 135.15±5.77 (123.0∼149.0) | 137.45±6.25 (120.0∼152.0) | 0.047‡ |
| Potassium (mmol/L) | 3.87±0.68 (2.5∼5.4) | 3.79±0.79 (1.9∼6.3) | 0.562 |
| Chloride (mmol/L) | 102.11±6.00 (90.0∼118.0) | 103.82±6.91 (91.0∼105.0) | 0.169 |
| Glucose (mg/dL) | 160.14±88.40 (49.0∼545.0) | 178.44±104.22 (70.0∼710.0) | 0.368 |
| WBC (count/μL) | 11,606±11,605 (180.0∼30,840.0) | 12,632±8,985 (300∼43,200.0) | 0.368 0.482 |
| Hemoglobin (g/dL) | 10.13±2.14 (6.1∼19.3) | 10.45±2.12 (6.5∼16.6) | 0.433 |
| Platelet (count/μL) | 232,055±137,822 (15.0∼610.0) | 178,218±113,651 (15.0∼538.0) | 0.027‡ |
| ESR (mm/hr) | 34.37±24.02 (1.0∼85.0) | 31.77±18.84 (2.0∼85.0) | 0.630 |
Table 6.
Multivariate logistic regression analysis of risk factors for acquiring bacteremia caused by vancomycin-resistant enterococci (VRE)
| Variables∗ | B | S.E. | Wald | DOF | P | Exp(B) | 95% confide interval | |
|---|---|---|---|---|---|---|---|---|
| Lower | Upper | |||||||
| Ventilatior | 0.832 | 0.585 | 2.024 | 1 | 0.155 | 2.298 | 0.730 | 7.235 |
| Polymicrobial infection | 0.623 | 0.751 | 0.690 | 1 | 0.406 | 1.865 | 0.428 | 8.123 |
| Causative organism | ||||||||
| E. faecalis | 15.226 | 2 | 0.000 | |||||
| E. faecium | 2.536 | 0.670 | 14.341 | 1 | ＜0.001‡ | 12.624 | 3.398 | 46.895 |
| Other species | 3.067 | 1.202 | 6.515 | 1 | 0.011‡ | 21.473 | 2.038 | 226.275 |
| Known source of bacteremia | 1.266 | 1.008 | 1.576 | 1 | 0.209 | 3.547 | 0.491 | 25.600 |
| Previous vancomycin therapy | 1.042 | 0.621 | 2.817 | 1 | 0.093 | 2.836 | 0.840 | 9.579 |
| Previous imipenem therapy | 1.074 | 1.214 | 0.783 | 1 | 0.376 | 2.927 | 0.271 | 31.590 |
| Previous penicillin therapy Creatinine (mg/dL) | 0.885 | 0.579 | 2.336 | 1 | 0.126 | 2.424 | 0.779 | 7.545 |
| 0.6∼1.2 | 1.845 | 2 | 0.398 | |||||
| ＜0.6 | −1.157 | 0.857 | 1.822 | 1 | 0.177 | 0.314 | 0.059 | 1.687 |
| ＜1.2 | −0.097 | 0.654 | 0.022 | 1 | 0.882 | 0.908 | 0.252 | 3.269 |
| Sodium (mmol/L) | ||||||||
| 135∼145 | 2.720 | 2 | 0.257 | |||||
| ＜135 | 0.368 | 0.543 | 0.460 | 1 | 0.497 | 1.445 | 0.499 | 4.190 |
| ＞145 | −1.926 | 1.359 | 2.010 | 1 | 0.156 | 0.146 | 0.010 | 2.088 |
| Platelet (count/μL) 150,000∼350,000 | 7.073 | 2 | 0.029 | |||||
| ＜150,000 | 1.275 | 1.436 | 0.788 | 1 | 0.375 | 3.579 | 0.215 | 59.697 |
| ＞350,000 | 2.793 | 1.452 | 3.698 | 1 | 0.054 | 16.327 | 0.948 | 281.317 |
| Constant† | −5.723 | 1.807 | 10.035 | 1 | 0.002 | 0.003 | ||
Table 7.
Difference of vancomycin resistance rate according to infection control activities
| Infection control activities | Vancomycin resistance rate | P‡ | |
|---|---|---|---|
| Before % (N) | After % (N) | ||
| Application of restricted vancomycin and quinupristin-dalfopristin from October 2005† | 27.78 (35/126) | 15.50 (20/129) | 0.0257∗ |
| Strengthening infection control management because of 2006 | 23.96 (23/96) | 19.23 (5/26) | 0.8060 |
| A. baumannii outbreak in ICU from November | |||
| Ward remodeling | |||
| Ward A (from April 2006 to July 2006) | 60.0 (3/5) | 0.0 (0/6) | 0.06 |
| Ward B (from August 2006 to November 2006) | 29.41 (5/17) | 0.0 (0/1) | 1.0 |
| Ward C (from December 2006 to March 2007) | 25.0 (3/12) | 0.0 (0/2) | 1.0 |
| Ward D (from October 2005 to February 2006) | 25.0 (2/8) | 0.0 (0/0) | NT |
† The vancomycin-resistance rates of E. faecalis and E. faecium were 11.3% (6/53) and 30.8% (20/65) before October 2005. They were 5.0% (3/60) and 30.9% (23/42) after October 2005. However, there were not statistically different (E. faecalis: P=0.3733, E. faecium: P=0.8459). Quinupristin-dalfopristin resistance rate was 37.5% (12/32) before October 2005 and 49.15% (58/118) after October 2005. However, there was no significant difference (P=0.3310);
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