0
We're unable to sign you in at this time. Please try again in a few minutes.
Retry
We were able to sign you in, but your subscription(s) could not be found. Please try again in a few minutes.
Retry
There may be a problem with your account. Please contact the AMA Service Center to resolve this issue.
Contact the AMA Service Center:
Telephone: 1 (800) 262-2350 or 1 (312) 670-7827  *   Email: subscriptions@jamanetwork.com
Error Message ......
Paper |

Third-Generation Cephalosporins and Vancomycin as Risk Factors for Postoperative Vancomycin-Resistant Enterococcus Infection FREE

Rachel A. Dahms, BS; Eric M. Johnson, MD; Catherine L. Statz, RN, MPH; James T. Lee, MD, PhD; David L. Dunn, MD, PhD; Gregory J. Beilman, MD
[+] Author Affiliations

From the Department of Surgery, University of Minnesota Medical School (Mss Dahms and Statz and Drs Johnson, Lee, Dunn, and Beilman), and Surgical Service, Veterans Administration Medical Center (Dr Lee), Minneapolis.


Arch Surg. 1998;133(12):1343-1346. doi:10.1001/archsurg.133.12.1343.
Text Size: A A A
Published online

Objective  To examine use of third-generation cephalosporins (3GCs) alone and in association with vancomycin hydrochloride as a risk factor for vancomycin-resistant enterococcus (VRE) infection in surgical patients.

Design  Case-control retrospective study analyzing antibiotic use in the 30 days preceding culture of VRE or vancomycin-sensitive enterococcus from an infected site.

Setting  A large tertiary care teaching hospital.

Patients  Surgical inpatients with VRE infections between September 3, 1993, and January 29, 1997, were matched with patients with vancomycin-sensitive enterococcus infections. Matches were based on surgical procedure, initial infection site, and immunosuppression. Matches were found for 32 of 50 surgical patients with VRE. Twenty matched pairs of patients were recipients of solid organ transplants.

Main Outcome Measures  Multivariate logistic regression analysis was done to examine 3GCs and vancomycin as risk factors for VRE infection. Univariate analysis of use of other antibiotic agents and demographic data was also performed.

Results  Multivariate analysis showed significant differences in the use of 3GCs both alone and concurrently with vancomycin. Univariate analysis also showed higher use of metronidazole, concurrent vancomycin and metronidazole, concurrent vancomycin and ceftazidime, and all antibiotics combined in patients with VRE infections.

Conclusions  This matched control study showed that use of 3GCs, alone (P=.05) or concurrently with vancomycin (P=.05), was a risk factor for VRE infection in surgical patients. Judicious administration of third-generation antibiotics is warranted in surgical patients with other risk factors for VRE.

Figures in this Article

SINCE THE late 1980s, group D enterococcus (GDEN), including Enterococcus faecalis and Enterococcus faecium, has emerged as an important nosocomial pathogen.1,2 Once thought to be a nonpathogen or a copathogen, GDEN has been shown to have the virulence factors necessary to cause infections in varied patient populations.3,4 Strains of GDEN resistant to multiple antibiotics have been studied as clinically problematic pathogens in surgical patients.57 Increased incidence of vancomycin-resistant enterococcus (VRE) has been identified as a serious complication in recipients of solid organ transplants.8,9

Throughout the emergence of GDEN as a recognized pathogen, antibiotic use has been cited consistently as a significant risk factor for infection.1012 As antibiotic resistance among enterococci developed and VRE became endemic in many institutions, vancomycin hydrochloride and third-generation cephalosporins (3CGs) have been associated repeatedly with acquisition of VRE.1315 The most commonly held theory on the mechanism by which broad-spectrum antibiotics such as 3GCs select for VRE is a disruption of the patient's endogenous intestinal microbial flora.16,17 This disruption allows for accelerated growth of opportunistic pathogens, such as enterococci.18

Fairview-University Medical Center, in Minneapolis, Minn, is a large (>300-bed) tertiary care teaching hospital. A marked increase in the number of surgical patients with VRE beginning on September 3, 1993, prompted the design of a 1:1 matched case-control study to investigate 3GC use as a risk factor for infection with VRE. By matching patients with VRE infections and those with vancomycin-sensitive enterococcus (VSE) infections, we sought to identify the risk factors specific for infection with VRE as opposed to infection with enterococci in general.

VRE CASE PATIENTS

Cases of VRE were defined as adult surgical inpatients (aged >18 years) who had undergone a surgical procedure within 2 to 60 days preceding VRE isolation. Only patients with clinically significant VRE cultures were included. Clinical significance was defined as GDEN isolation from a normally sterile site or from a diagnosed locus of infection. Significant culture sites included abdominal fluid or abscess, urine, blood, extremity tissue, bile, and sputum. In patients with multiple sites of VRE isolation, only the first clinically significant isolate of VRE was included for analysis. Patients who had been transferred from another inpatient facility were excluded.

VSE CONTROL PATIENTS

The VSE controls were defined as adult inpatients in the surgical service with VSE isolates from clinically significant sites. The VSE controls were matched with VRE cases by culture site, immunosuppression, and primary surgery type. Surgical procedures were grouped as involving solid organ transplant, bowel, abdominal cavity (nonbowel), thoracic cavity, or extremity. When more than 1 match possibility was available, random-number generation was used to pair VSE controls and VRE cases.

MEDICAL RECORD REVIEW

Clinical and demographic information was retrospectively collected for the 60-day period preceding positive results of VRE or VSE culture. The use of all antibiotic agents within 30 days of culture was recorded, focusing on vancomycin, 3GCs, and concurrent use of the 2 agents. Other demographic and clinical characteristics analyzed included potential nonantibiotic risk factors for VRE infection. These included age, sex, days in the hospital or intensive care unit (ICU), primary surgical procedures, number of visits to the operating room, primary disease, and Acute Physiology and Chronic Health Evaluation (APACHE) II19 score at the time of culture. For patients with positive urine cultures, the number of days with an indwelling urinary catheter was noted. Information about patients undergoing peritoneal dialysis or hemodialysis was also collected. Death and the presence of an initial monomicrobial GDEN culture were tracked as outcomes rather than risk factors for infection.

STATISTICAL METHODS

Multivariate conditional logistic regression analysis of clinical and demographic data was performed to compare 3GC use and patient characteristics of the VRE case patients and VSE controls. Infection with VRE was defined as the outcome measure. Univariate analysis of all other numerical data was carried out by means of a paired Wilcoxon signed rank test. In addition, the paired Wilcoxon univariate analysis was used to compare the groups of patients included in this study with those excluded because of a lack of matches. The McNemar test was used to analyze all factors with yes or no answers. In all instances, P<.05 was considered significant.

VRE CASES AND VSE CONTROLS

Between September 3, 1993, and January 29, 1997, 116 cases of VRE were identified by the hospital laboratory. Patients admitted to services accounted for 88 cases of VRE. Clinically significant VRE was isolated from 50 of those patients. Complete medical records were available for 44 of these VRE patients, and 36 fit the criteria for inclusion. Matched controls were found for 32 patients.

The remaining 4 VRE cases, excluded because of a lack of matches, were comparable with the study group with respect to age, use of vancomycin and 3GCs, APACHE II score, and days in the hospital and ICU (P=.58, .54, .09, .06, and .35, respectively). The 25 excluded VSE controls were comparable with the VRE group with respect to age, APACHE II score, and days in the hospital (P=.08, .37, and .79, respectively). There was a significant difference only in the concurrent use of vancomycin and 3GCs and in the number of days in the ICU (P=.03 and .006, respectively).

PATIENT DEMOGRAPHICS, CHARACTERISTICS, AND ANTIBIOTIC USE

More than 60% of the patients in this study (20 of 32) were recipients of solid organ transplants (Figure 1). The remainder of our cases and matches had a variety of surgical procedures, including intestinal resection, extremity vascular bypass, and exploratory laparotomy. The most common site for isolation of GDEN was from abdominal fluid (Figure 2). The least common site of isolation was sputum.

Place holder to copy figure label and caption
Figure 1.

Primary surgical procedures in matched pairs of vancomycin-resistant enterococcus cases and vancomycin-sensitive Enterococcus controls (numbers of cases are given).

Graphic Jump Location
Place holder to copy figure label and caption
Figure 2.

Site and frequency of group D Enterococcus isolation in matched pairs of vancomycin-resistant enterococcus cases and vancomycin-sensitive Enterococcus controls (numbers of cases are given).

Graphic Jump Location

On multivariate analysis, VRE cases and VSE controls showed a significant difference in the days of use of 3GCs, both separately and concurrently with vancomycin (Figure 3). Relative risk for VRE infection was 1.8 for vancomycin, 1.6 for 3GCs, and 2.7 for concurrent use of 3GCs and vancomycin. There were no significant differences in age, APACHE II score, days in the hospital or ICU, or days between surgery and culture.

Place holder to copy figure label and caption
Figure 3.

Duration of use of third-generation cephalosporins and vancomycin in vancomycin-resistant Enterococcus (VRE) cases and vancomycin-sensitive Enterococcus (VSE) controls. Within each treatment group, P<.05 in multivariate analysis for VRE vs VSE. Data are shown as mean+SE.

Graphic Jump Location

Univariate analysis of use of all groups of oral and intravenous antibiotics was performed to identify other differences between the VRE cases and VSE controls. Significant differences were demonstrated in the use of several of these agents (Table 1). As expected, there was a significant difference in the use of 3GCs and vancomycin. In addition, metronidazole hydrochloride, concurrent vancomycin and metronidazole, concurrent vancomycin and ceftazidime, and total antibiotic use were significantly higher in patients with VRE infection. Use of second-generation cephalosporins was significantly lower in VRE cases than in VSE controls.

Table Graphic Jump LocationTable 1. Univariate Analysis of Duration of Antibiotic Use in the 30 Days Preceding Positive Results of Culture*

Univariate analysis of other clinical and demographic data indicated other differing factors between the VRE cases and VSE controls (Table 2). Patients with VRE infection were in the hospital and ICU for longer periods than their cohorts. In addition, patients with VRE infection had slightly higher APACHE II scores at the time of positive results of culture. Initial VRE cultures were more likely to be monomicrobial than the matched results of VSE cultures from the same sites. Patients with positive VRE urine cultures had indwelling urinary catheters in place longer than their VSE counterparts.

Table Graphic Jump LocationTable 2. Patient Demographics and Clinical Data*

The results of this study indicate that use of 3GCs is a significant risk factor for infection with VRE, especially when combined with vancomycin (relative risk, 2.7 for vancomycin and 3GCs together). The incidence of use of 3GCs, either independently or concurrently with vancomycin, was higher in surgical patients with VRE than in matched patients with similar VSE infections.

In addition, metronidazole was significantly associated with VRE acquisition in the univariate analysis, whereas second-generation cephalosporins were associated with VSE rather than VRE infection. As in any study involving a small sample and variables that are substantially correlated, univariate analyses serve to point out potentially important factors but lack the ability to identify which ones will be significant when the entire complex system is taken into account.

Previous publications from our institution have examined the course of VRE outbreaks in hospitalized recipients of solid organs. In patients with pancreas transplants, previous use of vancomycin and metronizadole was found to be a risk factor for VRE infection.20 Furthermore, a separate prospective study found that recognized fecal colonization preceded VRE infection in 50% of cases.21 This lends credence to the theory that VRE infections arise from a patient's endogenous microbial flora. At the same time, the 50% figure reminds us that infection control procedures still have a substantial role in suppression of further VRE dissemination.

A recent matched, 1:1 control study of 145 patients also supported the theory that 3GCs, alone or with vancomycin, are associated with VRE infection.22 Colonized and infected patients from both medical and surgical services were included. In addition, VRE cases were matched to VSE controls by date of GDEN culture only. While this helps to equalize the risk of VRE acquisition from contaminated health care workers, we believed that a match by surgery type, culture site, and immunosuppression represented the infected surgical patient more accurately.

On the basis of the obvious connection between vancomycin and VRE infection, many institutions have implemented restriction policies for glycopeptide administration. Unfortunately, control of vancomycin use has shown less than ideal efficacy in the suppression of VRE infection development and dissemination.23 Judicious restriction of 3GCs has been shown to reduce significantly the incidence of enterococcal stool carriage in hospitalized patients.24 This, in conjunction with our study and the growing evidence that use of 3GCs commonly precedes VRE infection in surgical patients, suggests that controlled use of specific cephalosporins may be necessary to minimize the growing nosocomial VRE dilemma.

Both the Surgical Infection Society25 and Hospital Infection Control Practices Advisory Committee26 have previously recommended vancomycin restriction to delay the emergence of VRE infection. We suggest that conservative or restricted use of 3GCs be added to these recommendations. On the basis of our study, the restriction of ceftazidime in surgical patients with multiple risk factors for VRE acquisition or infection is warranted. This, in conjunction with continued vigilant environmental precautions and isolation protocols, may help moderate the spread of VRE infection.

Since the initiation of this study, several cases of Staphylococcus aureus infection have emerged in the United States with intermediate resistance to vancomycin.27 In multiple laboratory experiments, VRE has been proved capable of transferring resistance plasmids to S aureus.28 Although this has not been proved to occur in vivo, the mere possibility should serve as another extremely persuasive reason to do all that is possible to control VRE infection development and propagation.

Ms Dahms received honoraria from Merck and Co Inc, Minneapolis, Minn, for the presentation of these data.

Presented as a poster at the 18th Annual Meeting of the Surgical Infection Society, New York, NY, May 1-2, 1998.

We thank Kristen Gillingham, PhD, and Yan Zheng for their help with statistical analysis and Kim Leighton for her assistance with data collection.

Reprints: Gregory J. Beilman, MD, Department of Surgery, Medical School, University of Minnesota, Box 11, 420 Delaware St SE, Minneapolis, MN 55455 (e-mail: beilm001@maroon.tc.umn.edu).

Centers for Disease Control and Prevention, Nosocomial enterococci resistant to vancomycin—United States, 1989-1993. MMWR Morb Mortal Wkly Rep. 1993;42597- 599
Christou  NVBarie  PSDellinger  EPWaymack  JPStone  HH Surgical Infection Society intra-abdominal infection study. Arch Surg. 1993;128193- 199
Link to Article
Jett  BDHuycke  MMGilmore  MS Virulence of enterococci. Clin Microbiol Rev. 1994;7462- 478
Johnson  AP Pathogenicity of enterococci. J Antimicrob Chemother. 1994;331083- 1089
Link to Article
Barie  PSChristou  NVDellinger  EPRout  WRStone  HHWaymack  JP Pathogenicity of the enterococcus in surgical infections. Ann Surg. 1995;212155- 159
Link to Article
de Vera  MESimmons  RL Antibiotic-resistant enterococci and the changing face of surgical infections. Arch Surg. 1996;131338- 342
Link to Article
Low  DEWilley  BMMcGreer  AJ Multidrug-resistant enterococci: a threat to the surgical patient. Am J Surg. 1995;169(suppl 5A)8S- 12S
Sastry  VBrennan  PJLevy  MM  et al.  Vancomycin-resistant enterococci. Transplant Proc. 1995;27954- 955
Dominguez  EADavis  JCLangnas  ANWinfield  BCavalieri  SJRupp  ME An outbreak of vancomycin-resistant Enterococcus faecium in liver transplant recipients. Liver Transplant Surg. 1997;3586- 590
Link to Article
Magnussen  CRCave  J Nosocomial enterococcus infections. Am J Infect Control. 1988;16241- 245
Link to Article
Uttley  AHCGeorge  RCNaidoo  J  et al.  High-level vancomycin-resistant enterococci causing hospital infections. Epidemiol Infect. 1989;103173- 181
Link to Article
Wells  VDWong  ESMurray  BECoudron  PEWilliams  DSMarkowitz  SM Infection due to beta-lactamase-producing, high-level gentamicin-resistant Enterococcus faecalisAnn Intern Med. 1992;116285- 292
Link to Article
Morris  JGShay  DKHebden  JN  et al.  Enterococci resistant to multiple antimicrobial agents, including vancomycin. Ann Intern Med. 1995;123250- 259
Link to Article
Patterson  JESweeney  AHSimms  M  et al.  An analysis of 110 serious enterococcal infections. Medicine. 1995;74191- 200
Link to Article
Weinstein  JWRoe  MTowne  M  et al.  Resistant enterococci. Infect Control Hosp Epidemiol. 1996;1736- 41
Link to Article
Nathens  ABChu  PTMarshall  JC Nosocomial infections in the surgical intensive care unit. Infect Dis Clin North Am. 1992;6657- 675
Felmingham  DWilson  APRQuintana  AIGruneberg  RN Enterococcus species in urinary tract infection. Clin Infect Dis. 1992;15295- 301
Link to Article
Cavallero  VCatania  VBonaccorso  R  et al.  Effect of a broad-spectrum cephalosporin on the oral and intestinal microflora in patients undergoing surgery. J Chemother. 1992;482- 87
Knaus  WADraper  EAWagner  DPZimmerman  JE APACHE II: a severity of disease classification system. Crit Care Med. 1985;13818- 829
Link to Article
Dahlberg  PSSielaff  TDDunn  DL Emerging resistance in staphylococci and enterococci. Infect Dis Clin Pract. 1996;5(suppl 2)S49- S56
Link to Article
Wells  CLJuni  BACameron  SB  et al.  Stool carriage, clinical isolation, and mortality during an outbreak of vancomycin-resistant enterococci in hospitalized medical and/or surgical patients. Clin Infect Dis. 1995;2145- 50
Link to Article
Tornieporth  NGRoberts  RBJohn  JHafner  ARiley  LW Risk factors associated with vancomycin-resistant Enterococcus faecium infection or colonization in 145 matched case patients and control patients. Clin Infect Dis. 1996;23767- 772
Link to Article
Morgan  ASBrennan  PJFishman  NO Impact of a vancomycin restriction policy on use and cost of vancomycin and incidence of vancomycin-resistant enterococcus. Ann Pharmacother. 1997;31970- 973
Quale  JLandman  DSaurina  GAtwood  EDi'Tore  VPatel  K Manipulation of a hospital antimicrobial formulary to control an outbreak of vancomycin-resistant enterococci. Clin Infect Dis. 1996;231020- 1025
Link to Article
Davis  JMHuycke  MMWells  CL  et al.  Surgical Infection Society position on vancomycin-resistant enterococcus. Arch Surg. 1996;1311061- 1068
Link to Article
Hospital Infection Control Practices Advisory Committee (HICPAC), Recommendations for preventing the spread of vancomycin resistance. MMWR Morb Mortal Wkly Rep. 1994;441- 13
Centers for Disease Control and Prevention, Staphylococcus aureus with reduced susceptibility to vancomycin—United States, 1997. MMWR Morb Mortal Wkly Rep. 1997;46765- 766
Noble  WCVirani  ZCree  RG Co-transfer of vancomycin and other resistance genes from Enterococcus faecalis NCTC 12201 to Staphylococcus aureusFEMS Microbiol Lett. 1992;72195- 198
Link to Article

Figures

Place holder to copy figure label and caption
Figure 1.

Primary surgical procedures in matched pairs of vancomycin-resistant enterococcus cases and vancomycin-sensitive Enterococcus controls (numbers of cases are given).

Graphic Jump Location
Place holder to copy figure label and caption
Figure 2.

Site and frequency of group D Enterococcus isolation in matched pairs of vancomycin-resistant enterococcus cases and vancomycin-sensitive Enterococcus controls (numbers of cases are given).

Graphic Jump Location
Place holder to copy figure label and caption
Figure 3.

Duration of use of third-generation cephalosporins and vancomycin in vancomycin-resistant Enterococcus (VRE) cases and vancomycin-sensitive Enterococcus (VSE) controls. Within each treatment group, P<.05 in multivariate analysis for VRE vs VSE. Data are shown as mean+SE.

Graphic Jump Location

Tables

Table Graphic Jump LocationTable 1. Univariate Analysis of Duration of Antibiotic Use in the 30 Days Preceding Positive Results of Culture*
Table Graphic Jump LocationTable 2. Patient Demographics and Clinical Data*

References

Centers for Disease Control and Prevention, Nosocomial enterococci resistant to vancomycin—United States, 1989-1993. MMWR Morb Mortal Wkly Rep. 1993;42597- 599
Christou  NVBarie  PSDellinger  EPWaymack  JPStone  HH Surgical Infection Society intra-abdominal infection study. Arch Surg. 1993;128193- 199
Link to Article
Jett  BDHuycke  MMGilmore  MS Virulence of enterococci. Clin Microbiol Rev. 1994;7462- 478
Johnson  AP Pathogenicity of enterococci. J Antimicrob Chemother. 1994;331083- 1089
Link to Article
Barie  PSChristou  NVDellinger  EPRout  WRStone  HHWaymack  JP Pathogenicity of the enterococcus in surgical infections. Ann Surg. 1995;212155- 159
Link to Article
de Vera  MESimmons  RL Antibiotic-resistant enterococci and the changing face of surgical infections. Arch Surg. 1996;131338- 342
Link to Article
Low  DEWilley  BMMcGreer  AJ Multidrug-resistant enterococci: a threat to the surgical patient. Am J Surg. 1995;169(suppl 5A)8S- 12S
Sastry  VBrennan  PJLevy  MM  et al.  Vancomycin-resistant enterococci. Transplant Proc. 1995;27954- 955
Dominguez  EADavis  JCLangnas  ANWinfield  BCavalieri  SJRupp  ME An outbreak of vancomycin-resistant Enterococcus faecium in liver transplant recipients. Liver Transplant Surg. 1997;3586- 590
Link to Article
Magnussen  CRCave  J Nosocomial enterococcus infections. Am J Infect Control. 1988;16241- 245
Link to Article
Uttley  AHCGeorge  RCNaidoo  J  et al.  High-level vancomycin-resistant enterococci causing hospital infections. Epidemiol Infect. 1989;103173- 181
Link to Article
Wells  VDWong  ESMurray  BECoudron  PEWilliams  DSMarkowitz  SM Infection due to beta-lactamase-producing, high-level gentamicin-resistant Enterococcus faecalisAnn Intern Med. 1992;116285- 292
Link to Article
Morris  JGShay  DKHebden  JN  et al.  Enterococci resistant to multiple antimicrobial agents, including vancomycin. Ann Intern Med. 1995;123250- 259
Link to Article
Patterson  JESweeney  AHSimms  M  et al.  An analysis of 110 serious enterococcal infections. Medicine. 1995;74191- 200
Link to Article
Weinstein  JWRoe  MTowne  M  et al.  Resistant enterococci. Infect Control Hosp Epidemiol. 1996;1736- 41
Link to Article
Nathens  ABChu  PTMarshall  JC Nosocomial infections in the surgical intensive care unit. Infect Dis Clin North Am. 1992;6657- 675
Felmingham  DWilson  APRQuintana  AIGruneberg  RN Enterococcus species in urinary tract infection. Clin Infect Dis. 1992;15295- 301
Link to Article
Cavallero  VCatania  VBonaccorso  R  et al.  Effect of a broad-spectrum cephalosporin on the oral and intestinal microflora in patients undergoing surgery. J Chemother. 1992;482- 87
Knaus  WADraper  EAWagner  DPZimmerman  JE APACHE II: a severity of disease classification system. Crit Care Med. 1985;13818- 829
Link to Article
Dahlberg  PSSielaff  TDDunn  DL Emerging resistance in staphylococci and enterococci. Infect Dis Clin Pract. 1996;5(suppl 2)S49- S56
Link to Article
Wells  CLJuni  BACameron  SB  et al.  Stool carriage, clinical isolation, and mortality during an outbreak of vancomycin-resistant enterococci in hospitalized medical and/or surgical patients. Clin Infect Dis. 1995;2145- 50
Link to Article
Tornieporth  NGRoberts  RBJohn  JHafner  ARiley  LW Risk factors associated with vancomycin-resistant Enterococcus faecium infection or colonization in 145 matched case patients and control patients. Clin Infect Dis. 1996;23767- 772
Link to Article
Morgan  ASBrennan  PJFishman  NO Impact of a vancomycin restriction policy on use and cost of vancomycin and incidence of vancomycin-resistant enterococcus. Ann Pharmacother. 1997;31970- 973
Quale  JLandman  DSaurina  GAtwood  EDi'Tore  VPatel  K Manipulation of a hospital antimicrobial formulary to control an outbreak of vancomycin-resistant enterococci. Clin Infect Dis. 1996;231020- 1025
Link to Article
Davis  JMHuycke  MMWells  CL  et al.  Surgical Infection Society position on vancomycin-resistant enterococcus. Arch Surg. 1996;1311061- 1068
Link to Article
Hospital Infection Control Practices Advisory Committee (HICPAC), Recommendations for preventing the spread of vancomycin resistance. MMWR Morb Mortal Wkly Rep. 1994;441- 13
Centers for Disease Control and Prevention, Staphylococcus aureus with reduced susceptibility to vancomycin—United States, 1997. MMWR Morb Mortal Wkly Rep. 1997;46765- 766
Noble  WCVirani  ZCree  RG Co-transfer of vancomycin and other resistance genes from Enterococcus faecalis NCTC 12201 to Staphylococcus aureusFEMS Microbiol Lett. 1992;72195- 198
Link to Article

Correspondence

CME
Meets CME requirements for:
Browse CME for all U.S. States
Accreditation Information
The American Medical Association is accredited by the Accreditation Council for Continuing Medical Education to provide continuing medical education for physicians. The AMA designates this journal-based CME activity for a maximum of 1 AMA PRA Category 1 CreditTM per course. Physicians should claim only the credit commensurate with the extent of their participation in the activity. Physicians who complete the CME course and score at least 80% correct on the quiz are eligible for AMA PRA Category 1 CreditTM.
Note: You must get at least of the answers correct to pass this quiz.
You have not filled in all the answers to complete this quiz
The following questions were not answered:
Sorry, you have unsuccessfully completed this CME quiz with a score of
The following questions were not answered correctly:
Commitment to Change (optional):
Indicate what change(s) you will implement in your practice, if any, based on this CME course.
Your quiz results:
The filled radio buttons indicate your responses. The preferred responses are highlighted
For CME Course: A Proposed Model for Initial Assessment and Management of Acute Heart Failure Syndromes
Indicate what changes(s) you will implement in your practice, if any, based on this CME course.
Submit a Comment

Multimedia

Some tools below are only available to our subscribers or users with an online account.

Web of Science® Times Cited: 51

Related Content

Customize your page view by dragging & repositioning the boxes below.

Articles Related By Topic
Related Collections
PubMed Articles