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Impact of Routine Infectious Diseases Service Consultation on the Evaluation, Management, and Outcomes of Staphylococcus aureus Bacteremia

  1. Timothy C. Jenkins1,3,
  2. Connie S. Price1,3,
  3. Allison L. Sabel2,4,
  4. Philip S. Mehler2, and
  5. William J. Burman1,3
  1. 1Division of Infectious Diseases, Denver, Colorado
  2. 2Department of Patient Safety and Quality, Denver Health and Hospital Authority, Denver, Colorado
  3. 3Department of Medicine, Division of Infectious Diseases, Denver, Colorado
  4. 4Department of Preventive Medicine and Biometry, University of Colorado Health Sciences Center, Denver, Colorado
  1. Reprints or correspondence: Dr. Timothy C. Jenkins, Denver Public Health, 605 Bannock St., Denver, Colorado 80204 (timothy.jenkins{at}dhha.org).
 
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Abstract

Background. Staphylococcus aureus bacteremia causes considerable morbidity and mortality, and strategies to improve management and outcomes of this disease are needed.

Methods. Routine consultation with an infectious diseases specialist for cases of S. aureus bacteremia was mandated at our institution in May 2005. We compared the evaluation, management, and outcomes of cases before and after this policy change. All comparisons are by period (i.e., before or after initiation of the policy of routine consultation).

Results. In the year before and the year after after the implementation of routine consultation, 134 and 100 cases of S. aureus bacteremia, respectively, were evaluated. Consultation rates increased from 53% of cases before to 90% of cases after the policy change (Pt;.001). Echocardiography (57% vs. 73%; P=.01) and radiographic studies (81% vs. 91%; P=.04) were used more frequently during the period of routine consultation, and infective endocarditis or metastatic infections were diagnosed more frequently (33% vs. 46%; P=.04). All 4 standards of care (removal of intravascular foci of infection, obtaining follow-up blood culture samples, use of parenteral β-lactam therapy when possible, and administration of es;28 days of therapy for complicated infections) were adhered to more frequently with routine consultation (40% vs. 74%; Pt;.001). Treatment failure (microbiological failure, recurrent bacteremia, late metastatic infection, or death) occurred less often during the intervention year (17% vs. 12%), but this difference was not statistically significant (P=.27).

Conclusions. A policy of routine consultation with an infectious diseases specialist for patients with S. aureus bacteremia resulted in more-detailed evaluation, more-frequent detection of endocarditis and metastatic infection, and improved adherence to standards of care.

Staphylococcus aureus bacteremia is a common illness associated with significant morbidity and mortality. Distinguishing uncomplicated episodes of S. aureus bacteremia from bacteremia associated with deep-tissue infection can be challenging [1, 2]; however, the provision of appropriate therapy relies on such accurate distinction. Furthermore, considerable uncertainty exists regarding the optimal evaluation and management of S. aureus bacteremia [3]. Consultation with an infectious diseases (ID) specialist has been suggested as a method to address these clinical challenges [4–7].

Adherence to recommendations from ID consultation was associated with improved clinical outcomes among patients with S. aureus bacteremia in 1 prior study [4]. However, in that study, ID consultation was not requested for all cases. Whether a system of consultation in all cases of S. aureus bacteremia (i.e., routine ID consultation) would improve outcomes is not known. In 2005, Denver Health (Denver, CO) implemented such a policy. The purpose of this study was to assess whether this intervention resulted in improvements in the evaluation, treatment, and outcomes of affected patients.

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Methods

Study Setting and Population

Denver Health is a comprehensive, urban health care system that comprises a 400-bed teaching hospital, emergency department with a level 1 trauma center, urgent care center, community health centers, subspecialty clinics, and a public health department [8]. All of these sites are vertically integrated by a computerized health-information system. Furthermore, a large proportion of patients who access Denver Health use this system as their sole source of care. S. aureus is the most common cause of clinical bloodstream infection at Denver Health and Hospital Authority, with 100–150 cases per year. All inpatients with S. aureus bacteremia during the 1-year period before implementation of routine ID consultation (1 May 2004–30 April 2005) and during the 1-year period after implementation of the policy (1 July 2005–30 June 2006) were eligible for study inclusion. Data from the initial 2 months of the program were not collected, because the intervention was just getting under way. Because the study was designed to evaluate the effects of inpatient ID consultation for adults, exclusion criteria included age < 18 years, outpatient status, contaminated blood culture specimen, refusal of treatment, or any of the following within 4 days of collection of the initial positive blood culture sample: death, initiation of hospice care, or transfer to another facility. The study was approved by the Colorado Multiple Institutional Review Board.

Study Intervention

Beginning in May 2005, all positive blood culture results were reviewed daily by a member of the ID consultation service. A formal consultation was performed for each patient with S. aureus bacteremia, typically within 48 h of collection of the initial positive culture specimen. Although consultation was mandatory, the primary service was not required to follow the recommendations of the ID specialist. A specific algorithm for the evaluation and management of S. aureus bacteremia was not in use during the study period.

Study design and definitions. We performed a retrospective cohort study of patients with S. aureus bacteremia during the specified time period. Medical record review was performed using an abstraction form to document relevant laboratory data, diagnostic studies, and clinical encounters during a 12-week period after the collection of the initial positive blood culture specimen. All definitions were formulated before the study began (table 1). The reviewer (T.C.J.) could not be blind to the date of each case during medical record review.

Standards for the management of S. aureus bacteremia. Using national guidelines and results of prior studies, we developed 4 key standards of care for the evaluation and management of S. aureus bacteremia: (1) removal of an intravascular focus of infection, if present, within 4 days [3, 12], (2) obtaining blood for follow-up culture 2–4 days after collection of the initial positive culture specimen [3, 14], (3) use of parenteral β-lactam therapy for methicillin-susceptible infection [3, 4, 16], and (4) administration of at least 28 total days of therapy for treatment of complicated S. aureus bacteremia [12, 17]. An appropriate duration of antimicrobial therapy was considered to be at least 14 total days for uncomplicated infections [3, 18]. Use of vancomycin was considered to be inappropriate when used for es;7 days for a methicillin-susceptible infection in the absence of a β-lactam allergy or intolerance. Oral therapy was considered to be inappropriate, with the exception of linezolid or a fluoroquinolone plus rifampin in cases in which parenteral therapy was deemed not possible [19, 20].

Outcomes of S. aureus bacteremia. Treatment failure included any of the following: (1) microbiological failure, defined as a blood culture growing S. aureus obtained es;10 days after the collection of the initial positive culture specimen and before the completion of antimicrobial therapy; (2) recurrent bacteremia, defined as a blood culture positive for S. aureus obtained after completion of antimicrobial therapy and during the 12-week follow-up period; (3) late metastatic infection, defined as new evidence of S. aureus infection caused by hematogenous seeding es;10 days after the collection of the initial positive blood culture specimen; or (4) death due to any cause. Possible complications of treatment for S. aureus bacteremia included laboratory toxicities associated with antimicrobial therapy (grade 3 or 4 abnormalities in serum creatinine level, platelet count, absolute neutrophil count, alanine aminotransferase level, or aspartate aminotransferase level [21]), catheter-related thrombotic events, or catheter-related bacteremia (with a species other than S. aureus).

Data Analysis

All comparisons are by time period (i.e., before vs. after the implementation of routine consultation), not by whether consultation actually occurred or whether recommendations were followed. Some patients had episodes of S. aureus bacteremia separated by >12 weeks. We considered these to be distinct episodes of bacteremia, and the evaluation, management, and outcomes of distinct episodes were included in the analysis. Results were similar when we repeated key analyses using only the initial episode of bacteremia. Only the initial episode of bacteremia was included in analysis of demographic factors and the logistic regression model.

Comparisons were performed between the pre- and postintervention time periods with use of Pearson's hi;2 test, Fisher's exact test, or Wilcoxon rank-sum test, where appropriate. A multivariate logistic regression model assessing predictors of treatment failure was performed, including demographic and clinical characteristics associated with adverse outcomes in univariate analysis (Pt;.20). Evaluation- and management-related variables were not included in this model, because the implementation of routine ID consultation affected these variables. A P value of t;.05 was considered to be significant. We used SAS software, version 9.1 (SAS Institute), for data analysis.

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Results

A total of 269 initial positive blood culture results from 252 patients were reviewed (figure 1). Thirty-five patients were excluded for the following reasons: 16 were classified as having contaminated cultures, 5 refused therapy, 3 were t;18 years of age, and 11 had no follow-up beyond 4 days (4 died, 5 entered hospice care, and 2 transferred to another facility). A total of 134 cases (in 127 patients) during the year before routine ID consultation and 100 cases (in 98 patients) after the initiation of routine consultation were included for analysis. Six patients had an episode of bacteremia during each time period and were included only in the preintervention period for analysis of demographic factors and the logistic regression model.

Figure 1
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Figure 1

Summary of 269 eligible cases of Staphylococcus aureus bacteremia. ID, infectious diseases.

Patient demographic characteristics and comorbidities were similar in the pre- and postintervention periods (table 2). There were no significant differences in baseline clinical characteristics in each time period (table 3). Although the proportions of catheter-related infections were similar in each time period, catheter-related infections were more likely to meet “definite” criteria (32% vs. 56%; P=.04) during the intervention year.

Table 1
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Table 1

Definitions used in a study of the impact of infectious diseases consultation on Staphylococcus aureus bacteremia.

Table 2
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Table 2

Patient demographic characteristics.

Table 3
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Table 3

Clinical characteristics at presentation for 234 patients with Staphylococcus aureus bacteremia.

The policy of routine consultation resulted in an increase in the frequency of ID consultation from 53% of cases to 90% of cases (Pt;.001) (table 4). Furthermore, consultations occurred earlier in the course of infection (median time to consultation, 3 days vs. 2 days; P=.005). Echocardiography was used more frequently (57% vs. 73%; P=.01), which led to the discovery of more valvular vegetations (1 case vs. 7 cases; P=.02) during the period of routine consultation. At least 1 radiographic study (excluding plain films) was obtained in a higher percentage of cases during the intervention year (81% vs. 91%; P=.04).

Table 4
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Table 4

Evaluation and classification of Staphylococcus aureus bacteremia by time period.

Infective endocarditis or early metastatic infection was identified more commonly during the year of routine ID consultation (33% vs. 46%; P=.04) (table 4). Of note, the proportion of cases of infective endocarditis or early metastatic infection caused by methicillin-resistant S. aureus in each of the 2 time periods was similar (34% vs. 35%; P=.95).

All 4 standards of care for the management of S. aureus bacteremia were more frequently adhered to during the intervention year (40% vs. 74%; Pt;.001) (table 5). A higher percentage of intravascular catheters were removed (73% vs. 89%; P=.05), follow-up blood culture samples were obtained with more regularity (71% vs. 87%; P=.003), parenteral β-lactam antibiotics were used more consistently (67% vs. 92%; Pt;.001), and therapy was more frequently administered for at least 28 days for complicated infections (42% vs. 74%; Pt;.001) during the routine consultation time period. The median total duration of therapy (16 days vs. 29 days; Pt;.001) and the median duration of parenteral therapy (15 days vs. 29 days; Pt;.001) were significantly longer with routine ID consultation. Before consultation became routine, 26% of patients were treated with t;10 days of parenteral therapy. Inappropriate use of vancomycin (9% vs. 2%; P=.03) and inappropriate use of an oral antimicrobial agent (18% vs. 4%; P=.001) occurred less frequently during the intervention year. Overall, there were somewhat fewer possible complications of therapy for S. aureus bacteremia during the routine consultation period (22% vs. 13%; P=.09), and grade 4 laboratory toxicities were significantly less likely to occur (5% vs. 0%; P=.04) (table 5).

Table 5
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Table 5

Aspects of management and potential complications of therapy by time period.

Treatment failure, including microbiological failure, recurrent bacteremia, late metastatic infection, or death occurred less commonly during the intervention period; however, this difference was not statistically significant (17% vs. 12%; P=.27) (table 6). A trend toward fewer late metastatic infections was observed with routine consultation (4% vs. 0%; P=.07). In a sensitivity analysis of treatment failure, we included the 16 cases classified as involving contaminated cultures (0 treatment failures) and the 4 cases involving early death and found no substantial difference in results. The initial management of the 35 cases associated with treatment failure is summarized in table 7, and more-detailed descriptions of these cases are presented in [table 8[table 8 (online only). Notably, before the initiation of routine ID consultation, 5 patients with complicated S. aureus bacteremia received treatment with ⩽12 days of parenteral therapy, with subsequent treatment failure in all 5 cases.

Table 6
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Table 6

Treatment failures by time period.

Table 7
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Table 7

Initial management for 35 cases of Staphylococcus aureus bacteremia associated with treatment failure.

Table 8
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Table 8

Descriptions of cases associated with treatment failure.

Only 4 variables were included in the multivariate logistic regression model, because of the small number of patients with treatment failure. Persistent fever (⩾ 72 h in duration) and severity of illness score were included on the basis of prior literature [14, 22] and clinical judgment, respectively. Malignancy was associated with treatment failure in univariate analysis (Pt;.001) and remained significant in the multivariate model (OR, 7.87; 95% CI, 3.11–19.94). Routine ID consultation was included in the multivariate model and was not significantly associated with adverse outcomes (P=.45).

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Discussion

Implementation of a policy of routine ID consultation in cases of S. aureus bacteremia resulted in an increased frequency of consultation and was associated with earlier involvement of the ID consultation service. Echocardiography and radiographic studies were used more often and infective endocarditis and metastatic infections were identified more frequently during the intervention period. Standards of care for the management of S. aureus bacteremia were adhered to more consistently after the initiation of routine ID consultation. The median duration of therapy was longer and inappropriate use of vancomycin and oral antimicrobial agents occurred less frequently during the intervention year. Despite the increased duration of therapy, there was a trend toward fewer potential complications of therapy. Microbiological failure, recurrent bacteremia, late metastatic infection, or death occurred less frequently, although this difference was not statistically significant.

To our knowledge, this is the first study to evaluate the effects of a policy of routine ID consultation for cases of S. aureus bacteremia. Fowler and colleagues [4] performed a study in which a member of the ID service contacted the primary physicians of patients with S. aureus bacteremia to offer management recommendations. Acceptance of management recommendations was associated with lower rates of relapse. However, formal consultation was declined and verbal advice was not followed in over one-half of all cases. A policy of routine consultation, as our institution implemented, may lead to additional benefit, because one would expect it to result in both increased frequency of ID consultation and improved adherence to recommendations documented in the medical record. Our study differs from that of Fowler et al. [4], because our purpose was to evaluate the effects of routine ID consultation as an intervention. The pre- and postimplementation periods were compared without regard to the proportion of cases in which ID consultation occurred or recommendations were followed.

Before the implementation of this policy at our institution, the ID service was routinely asked to provide consultation in cases of S. aureus bacteremia associated with clinically apparent infective endocarditis or other deep-tissue infections, but consultation was requested much less frequently in apparently uncomplicated cases. It follows that the dramatic increase in the rate of ID consultation after initiation of this policy reflected increased involvement in such uncomplicated cases. Routine consultation resulted in more-detailed evaluation of patients, with increased use of follow-up blood cultures, echocardiography, and radiographic studies, which led to an increase in the recognition of infective endocarditis and metastatic infection. This suggests that, before routine consultation, a number of cases of endocarditis and metastatic infection were inappropriately classified and were treated as uncomplicated infections. Our data support this hypothesis, because we demonstrated that, before routine consultation, only 40% of patients with complicated infections received at least 28 days of therapy. Routine consultation is an example of a systemwide policy change that may prove to have applicability in other areas of hospital medicine.

One might hypothesize that the differences in the proportions of infective endocarditis and metastatic infection observed in this study were attributable to an increase in the incidence of these complications rather than to an increase in their recognition through routine ID consultation. For example, the incidence of invasive infection due to community-associated methicillin-resistant S. aureus, a more virulent strain of methicillin-resistant S. aureus, has increased dramatically recently [23, 24]. However, the proportion of cases of infective endocarditis or metastatic infection caused by methicillin-resistant S. aureus remained stable over the study period. Moreover, rates of inpatient and outpatient S. aureus infection caused by methicillin-resistant isolates did not increase over the study period in our institution (data not shown). Finally, patients in the 2 time periods had similar comorbidities and severity of illness. Therefore, it is most likely that the increases in the proportions of infective endocarditis and metastatic infection observed during the intervention year were a result of increased recognition of these complications.

Similar to results of a previous study of ID consultation for S. aureus bacteremia [6], initiation of routine ID consultation was associated with a longer duration of therapy. However, in contrast to previous findings [5], we found that the duration of hospitalization was unchanged after initiating this policy. This observation is likely attributable to the use of outpatient parenteral antimicrobial therapy at our institution. Outpatient parenteral antimicrobial therapy is now routine in clinical practice and has been demonstrated to be a successful treatment option for serious staphylococcal infections [25]. In addition, whereas one might have expected an increase in complications associated with more-prolonged parenteral therapy, the incidence of potential complications actually decreased during the period of routine consultation. Patients who are seen by the ID service during hospitalization and who require outpatient parenteral therapy are followed in the outpatient ID clinic on a weekly basis for clinical and laboratory monitoring. This frequent follow-up and monitoring may, in part, explain the observed trend toward fewer complications of therapy during the intervention period.

Limitations inherent to retrospective studies apply to our study. First, because it is a pre- and postintervention analysis, there is the potential for period effect. We are not aware of any changes in hospital practice during the study period that may have confounded the study. Second, the reviewer could not be blind to the time period of each case. Objective measures of evaluation, management, and outcome were chosen to minimize the introduction of reviewer bias. Third, patient follow-up was often incomplete. It is possible that some patients who experienced treatment failure presented to outside institutions, although this would be expected to have occurred with equal frequency during both periods. Fourth, we could not perform DNA fingerprinting of isolates to determine whether episodes of recurrent S. aureus bacteremia or late metastatic infection represented relapse of infection or reinfection with a different strain of S. aureus. Previous studies have shown that 82%–90% of cases of recurrent S. aureus bacteremia are attributable to relapse of infection due to the original strain [4, 26].

We classified cases as being uncomplicated or complicated using readily available clinical criteria; however, considerable uncertainty exists regarding the appropriate classification of S. aureus bacteremia. Furthermore, there continue to be uncertainties regarding the optimal treatment of S. aureus bacteremia, and the treatment courses suggested in published guidelines do not apply to all cases. We chose 14-day and 28-day cutoffs as appropriate durations of therapy for uncomplicated and complicated cases, respectively, on the basis of current guidelines [3, 17] and recent literature [12, 18]. Finally, our study was underpowered to detect a moderate difference in adverse clinical outcomes. For example, with sample sizes of im;100 patients per arm, our study had only 40% power to detect a 50% relative reduction in treatment failure (e.g., 17% vs. 8.5%).

Implementation of a policy of routine ID consultation in cases of S. aureus bacteremia dramatically increased the frequency of ID consultation in these cases. Increases in the use of diagnostic modalities to identify complications of infection likely led to more-frequent diagnoses of infective endocarditis and metastatic infections. In addition, routine ID consultation dramatically improved adherence to standards of care for the management of S. aureus bacteremia. Although treatment failure occurred less commonly during the intervention year, this difference was not statistically significant. A program of routine ID consultation is an effective way to improve the evaluation and management of S. aureus bacteremia that may lead to improved clinical outcomes.

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Acknowledgments

We thank Robert Belknap for his participation on the adjudication committee.

Financial support. The Department of Patient Safety and Quality, Denver Health (Denver, CO).

Potential conflicts of interest. All authors: no conflicts.

  • Received June 27, 2007.
  • Accepted November 13, 2007.
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  1. Clin Infect Dis. (2008) 46 (7): 1000-1008. doi: 10.1086/529190
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