Abstract
Background
The purpose of this study was to evaluate the impact of infectious diseases consultation (IDC) and a real-time antimicrobial stewardship (AMS) review on the management of Staphylococcus aureus bacteremia (SAB).
Methods
This retrospective study included adult inpatients with SAB from January 2016 to December 2018 at 7 hospitals. Outcomes were compared between 3 time periods: before mandatory IDC and AMS review (period 1), after mandatory IDC and before AMS review (period 2), and after mandatory IDC and AMS review (period 3). The primary outcome was bundle adherence, defined as appropriate intravenous antimicrobial therapy, appropriate duration of therapy, appropriate surveillance cultures, echocardiography, and removal of indwelling intravenous catheters, if applicable. Secondary end points included individual bundle components, source control, length of stay (LOS), 30-day bacteremia-related readmission, and in-hospital all-cause mortality.
Results
A total of 579 patients met inclusion criteria for analysis. Complete bundle adherence was 65% in period 1 (n = 241/371), 54% in period 2 (n = 47/87), and 76% in period 3 (n = 92/121). Relative to period 3, bundle adherence was significantly lower in period 1 (odds ratio [OR], 0.58; 95% confidence interval [CI], 0.37–0.93; P = .02) and period 2 (OR, 0.37; 95% CI, 0.20–0.67; P = .0009). No difference in bundle adherence was noted between periods 1 and 2. Significant differences were seen in obtaining echocardiography (91% vs 83% vs 100%; P < .001), source control (34% vs 45% vs 45%; P = .04), and hospital LOS (10.5 vs 8.9 vs 12.0 days; P = .01). No differences were noted for readmission or mortality.
Conclusions
The addition of AMS pharmacist review to mandatory IDC was associated with significantly improved quality care bundle adherence.
Keywords: antimicrobial stewardship, bacteremia, bundle adherence, Staphylococcus aureus
Staphylococcus aureus is a leading cause of nosocomial and community-acquired bloodstream infections [1]. S. aureus bacteremia (SAB) is frequently complicated by metastatic infections such as osteomyelitis and endocarditis, and mortality estimates range from 13.3% to 26.0% in the United States [2]. Various strategies have been implemented to improve outcomes for SAB patients. Previous studies have demonstrated that infectious diseases consultation (IDC) improves mortality for patients with SAB [3–14]. Mandating IDC for all patients with SAB has been shown to improve rates of guideline-recommended care, including echocardiography, source control, appropriate antimicrobial therapy, and follow-up cultures [4, 5, 15, 16].
Antimicrobial stewardship (AMS) interventions have also been investigated as a strategy to enhance SAB quality of care. AMS review has been shown to improve optimal therapy for methicillin-sensitive S. aureus (MSSA) bacteremia, decrease hospital length of stay, and increase adherence to quality care bundles [17–19]. A pharmacist-driven real-time AMS review with quality care bundle recommendations has also been associated with improved bundle adherence and decreased 30-day SAB-related readmission [20].
Evidence of the combined effect of IDC and AMS is limited. Smith and colleagues [21] implemented a pharmacist-driven AMS review and quality care bundle that resulted in increasing the rate of IDC from 74% to 100% and was associated with decreased readmission for SAB. However, the impact of the increased rate of IDC and AMS intervention cannot be independently evaluated. Buehrle and colleagues [22] examined the benefit of IDC on the management of SAB at an institution with a comprehensive AMS program already in place and found that IDC patients were more likely to receive guideline-recommended management and had reduced mortality.
The influence of real-time AMS review on SAB outcomes in the setting of preexisting mandatory IDC for SAB has not been evaluated. The objective of this study was to assess adherence to a bundle of quality care indicators for SAB before and after implementation of mandatory IDC as well as before and after subsequent implementation of real-time pharmacist-driven AMS review.
METHODS
Study Design
This was a retrospective study of all inpatients ≥18 years of age with at least 1 blood culture positive for S. aureus from January 2016 to December 2018 at 7 Advocate Aurora Health hospitals located in the Chicago, Illinois, area. Patients were excluded if they had a polymicrobial bacteremia, preexisting SAB before admission, were transferred to another institution within 72 hours of their first positive blood culture being drawn, transitioned to hospice care before completion of antimicrobial therapy, or died within 48 hours of their first positive blood culture being drawn. The study received a non–human subject research determination from the organization’s institutional review board.
Interventions
Patients were divided into 3 different time periods: before mandatory IDC and AMS review (period 1), after mandatory IDC and before AMS review (period 2), and after mandatory IDC and AMS review (period 3) (Figure 1). Before the implementation of mandatory IDC and AMS review, 1 of the 7 hospitals already had a dedicated infectious diseases (ID) pharmacist, and an evidence-based practice guideline for the empiric treatment of bacteremia was available for clinicians. However, no system-wide initiatives were implemented to actively promote adherence to quality-of-care measures for SAB. On September 1, 2017, IDCs were mandated for all patients with SAB throughout the health system. A comment was added in the electronic medical record to all blood culture results positive for S. aureus, stating that IDC was required per system policy. In the spring and summer of 2018, an ID pharmacist–driven AMS review program was implemented at all hospitals included in the study. When an organism from a blood culture was identified using matrix-assisted laser desorption time-of-flight mass spectrometry (MALDI-TOF MS), microbiology sent a page in real time to the ID pharmacist providing coverage for that hospital 24 hours a day, 7 days a week. In addition to MALDI-TOF, our laboratory had the capability of testing mecA to differentiate between methicillin-resistant Staphylococcus aureus (MRSA) and methicillin-susceptible S. aureus (MSSA). However, this test may not have been consistently utilized to inform clinical decisions. ID pharmacists made recommendations to the care team regarding optimal empiric therapy while susceptibilities are pending and, when applicable, made recommendations regarding optimization of definitive therapy once additional information was available. ID pharmacists were also responsible for enforcing the mandatory IDC policy and recommended additional interventions such as echocardiography when needed.
Figure 1.
Timeline of study. aExact date of AMS review implementation varied by hospital. Abbreviations: AMS, antimicrobial stewardship; ID, infectious disease.
Outcomes
The primary outcome was complete adherence to a quality care bundle consisting of the following: appropriate intravenous antimicrobial therapy, appropriate duration of therapy, surveillance cultures obtained within 24–48 hours, echocardiography, and removal of indwelling intravenous catheters, if applicable. Antimicrobial therapy was considered appropriate if the empiric therapy selected provided coverage for MRSA and the patient was maintained on intravenous therapy for the entire duration of treatment. For patients with MSSA, therapy was considered appropriate if an antistaphylococcal beta-lactam was used for definitive therapy, unless contraindicated. Vancomycin was considered appropriate for patients with documented allergies to both penicillins and cephalosporins. Appropriate duration of therapy was defined as at least 14 days for uncomplicated SAB and at least 28 days for complicated SAB, as defined by the Infectious Diseases Society of America MRSA clinical practice guideline [23]. Either transthoracic echocardiography or transesophageal echocardiography was considered acceptable. Secondary end points were the individual bundle components, source control, time to IDC, time to definitive antimicrobial therapy, time to blood culture clearance, hospital LOS, intensive care unit LOS, 30-day bacteremia-related readmission, and in-hospital all-cause mortality. Source control was defined as abscess drainage or surgical removal of an infection source such as indwelling prosthetic devices or pacemakers.
Statistical Analysis
Descriptive statistics were performed for all continuous and categorical data. The chi-square or Fisher exact test was used to evaluate categorical data, as appropriate. A 3-way analysis of variance was used to evaluate continuous data. If a statistically significant difference was detected between the 3 groups, the post hoc Tukey, chi-square, or Fisher exact test was used to compare groups 1 and 2, groups 2 and 3, and groups 1 and 3 to determine which pair of groups was driving the difference. A chi-square test with odds ratio (OR) or a Fisher exact test was used for categorical data, and t tests were used for continuous data. Analyses were performed with SAS, version 9.4 (SAS Institute, Cary, NC, USA), and a 2-tailed P value of <.05 was considered statistically significant.
RESULTS
A total of 810 patients were screened, with 579 patients meeting inclusion criteria (period 1: n = 137; period 2: n = 82; period 3: n = 121). The most common reason for exclusion was transition to hospice care before completion of antimicrobial therapy (Figure 2). Demographics and baseline characteristics were similar between the 3 groups (Table 1), though significant statistical differences were observed between groups 1, 2, and 3 with regard to MRSA vs MSSA infection (40% vs 45% vs 27%, respectively; P = .01) and in patients with IDC (95% vs 98% vs 99%, respectively; P = .05). A majority of patients were male (n = 353, 61%) and had community-acquired bacteremia (n = 523, 90%), which we defined as first positive culture drawn within 48 hours of hospital admission. The most common source of SAB was acute bacterial skin and skin structure infection (n = 168, 29%), followed by intravenous catheter (n = 112, 19%). Although not statistically significant, a lower rate of uncomplicated bacteremia was seen in period 3 (32%) compared with periods 1 (43%) and 2 (44%; P = .09). A lower proportion of patients in period 1 (29%) had metastatic sites of infection compared with period 3 (39%; OR, 0.63; 95% confidence interval [CI], 0.41–0.97; P = .03), although the rate of metastatic infection was not statistically significant when comparing periods 1, 2, and 3 (29% vs 26% vs 39%, respectively; P = .07). Empiric and definitive therapy for all patients is described in Table 2. All patients in period 3 were given an intravenous agent for empiric and definitive treatment.
Figure 2.
Development of study cohort. Abbreviations: AMS, antimicrobial stewardship; IDC; infectious diseases consult.
Table 1.
Demographics and Baseline Characteristics
| Characteristic | Period 1 (n = 371) | Period 2 (n = 87) | Period 3 (n = 121) | P Value |
|---|---|---|---|---|
| Age, mean ± SD, y | 64.5 ± 16.5 | 67.4 ± 16.8 | 62.9 ± 16.0 | .1 |
| Male sex, No. (%) | 233 (62.8) | 51 (58.6) | 69 (57.0) | .5 |
| Charlson comorbidity index, mean ± SD | 5.3 ± 3.0 | 5.1 ± 2.8 | 4.9 ± 2.7 | .5 |
| Pitt bacteremia score, mean ± SD | 1.3 ± 1.8 | 1.1 ± 1.5 | 1.5 ± 2.3 | .2 |
| History of IV drug abuse, No. (%) | 17 (4.6) | 3 (3.4) | 4 (3.3) | .9 |
| History of SAB, No. (%) | 48 (12.9) | 7 (8.0) | 15 (12.4) | .4 |
| Hardware or prosthetic material, No. (%) | 138 (37.2) | 27 (31.0) | 38 (31.4) | .2 |
| Community-acquired, No. (%) | 334 (90.0) | 80 (92.0) | 109 (90.0) | .9 |
| MRSA, No. (%) | 149 (40.2) | 39 (44.8) | 33 (27.3) | .02 |
| ID consult, No. (%) | 351 (94.6) | 85 (97.7) | 120 (99.2) | .05 |
| Uncomplicated bacteremia, No. (%) | 160 (43.1) | 38 (43.7) | 39 (32.2) | .09 |
| Metastatic site of infection, No. (%) | 106 (28.6) | 23 (26.4) | 47 (38.8) | .07 |
| Source of bacteremia, No. (%) | ||||
| Bone and joint | 48 (12.9) | 15 (17.2) | 26 (21.5) | .1 |
| ABSSSI | 102 (27.5) | 34 (39.1) | 32 (26.4) | |
| Respiratory | 20 (5.4) | 8 (9.2) | 6 (5.0) | |
| Endocarditis | 20 (5.4) | 1 (1.1) | 6 (5.0) | |
| Urinary | 15 (4.0) | 1 (1.1) | 3 (2.5) | |
| Intravenous catheter | 79 (21.3) | 12 (13.8) | 21 (17.4) | |
| Unknown | 53 (14.3) | 8 (9.2) | 19 (15.7) | |
| Other | 34 (9.2) | 8 (9.2) | 8 (6.6) | |
| ICU admission, No. (%) | 140 (37.7) | 25 (28.7) | 45 (37.2) | .3 |
Abbreviations: ABSSSI, acute bacterial skin and skin structure infection; ICU, intensive care unit; ID, infectious disease; IV, intravenous; MRSA, methicillin-resistant Staphylococcus aureus; SAB, Staphylococcus aureus bacteremia.
Table 2.
Empiric and Definitive Intravenous Therapy
| Empiric Therapy | Definitive Therapy | |||||
|---|---|---|---|---|---|---|
| Period 1 (n = 371) | Period 2 (n = 87) | Period 3 (n = 121) | Period 1 (n = 371) | Period 2 (n = 87) | Period 3 (n = 121) | |
| Vancomycin, No. (%) | 331 (89) | 75 (86) | 94 (78) | 143 (39) | 38 (44) | 29 (24) |
| Daptomycin, No. (%) | 16 (4.3) | 1 (1.1) | 10 (8.3) | 19 (5.1) | 4 (4.6) | 8 (6.6) |
| Oxacillin, No. (%) | 2 (0.54) | 0 (0) | 0 (0) | 50 (13) | 4 (4.6) | 26 (21) |
| Cefazolin, No. (%) | 1 (0.27) | 2 (2.3) | 0 (0) | 127 (34) | 34 (39) | 45 (37) |
| Other,a No. (%) | 17 (4.6) | 7 (8.0) | 17 (14) | 23 (6.2) | 5 (5.7) | 13 (11) |
| None, No. (%) | 4 (1.1) | 2 (2.3) | 0 (0) | 9 (2.4) | 2 (2.3) | 0 (0) |
aOther agents included cefepime, ceftriaxone, clindamycin, doxycycline, ertapenem, levofloxacin, linezolid, meropenem, piperacillin/tazobactam, and telavancin.
Complete bundle adherence was statistically significant across periods 1, 2, and 3 (65% vs 54% vs 76%, respectively; P = .004) (Table 3). Relative to period 3, bundle adherence was significantly lower in period 1 (OR, 0.58; 95% CI, 0.37–0.93; P = .02) and period 2 (OR, 0.37; 95% CI, 0.20–0.67; P = .0009). For the individual bundle elements, a significant difference was seen in obtaining echocardiography, with patients in period 3 (100%) being more likely to have an echocardiogram compared with periods 1 (91%) and 2 (83%; P < .001). The highest rate of compliance across all remaining bundle elements was seen in period 3, though no statistically significant differences were noted (Table 3).
Table 3.
Primary and Secondary Outcomes
| Outcome | Period 1 (n = 371) | Period 2 (n = 87) | Period 3 (n = 121) | P Value |
|---|---|---|---|---|
| Complete bundle adherence,a No. (%) | 241 (65) | 47 (54) | 92 (76) | .004 |
| Repeat blood cultures, No. (%) | 291 (78) | 66 (76) | 105 (87) | .09 |
| Echocardiography, No. (%) | 339 (91) | 72 (83) | 121 (100) | <.0001 |
| Removal of indwelling lines or nonapplicable, No. (%) | 357 (96) | 81 (93) | 117 (97) | .4 |
| Appropriate antimicrobial therapy, No. (%) | 354 (95) | 83 (95) | 120 (99) | .1 |
| Appropriate antimicrobial duration, No. (%) | 324 (87) | 76 (87) | 112 (93) | .3 |
| Source control, No. (%) | 126 (34) | 39 (45) | 54 (45) | .04 |
| Time to IDC, mean ± SD, d | 1.06 ± 1.42 | 0.99 ± 0.85 | 0.83 ± 0.69 | .2 |
| Time to definitive therapy if change in therapy required, mean ± SD, d | 2.49 ± 1.58 | 2.41 ± 1.35 | 2.77 ± 5.67 | .7 |
| Time to blood culture clearance, mean ± SD, h | 52.6 ± 44.0 | 54.2 ± 63.3 | 41.9 ± 25.8 | .06 |
| Hospital LOS, mean ± SD, d | 10.5 ± 6.96 | 8.85 ± 6.17 | 12.0 ± 10.7 | .01 |
| ICU LOS, mean ± SD, d | 5.34 ± 6.10 | 5.33 ± 5.72 | 6.34 ± 6.28 | .6 |
| In-hospital all-cause mortality, No. (%) | 16 (4.3) | 2 (2.3) | 6 (5.0) | .6 |
| 30-d SAB-related readmission, No. (%) | 10 (2.7) | 0 (0) | 0 (0) | .07 |
Abbreviations: ICU, intensive care unit; IDC, infectious diseases consult; LOS, length of stay; SAB, Staphylococcus aureus bacteremia.
aPrimary end point.
Patients in periods 2 and 3 were more likely to have a procedure done for source control compared with period 1 (45% vs 45% vs 34%, respectively; P = .04), reflecting a statistically significantly lower rate of source control observed in period 1 relative to period 3 (OR, 0.64; 95% CI, 0.42–0.97; P = .03). Hospital LOS also varied significantly between periods 1, 2, and 3 (10.5 vs 8.85 vs 12.0 days, respectively; P = .01). Although not statistically significant, 30-day bacteremia-related readmission was higher in period 1 (2.7%) compared with periods 2 (0%) and 3 (0%; P = .07). No statistically significant differences were noted for other secondary outcomes (Table 3).
Discussion
Our study uniquely evaluated the combined effect of implementing a system-wide policy mandating IDC for SAB and real-time AMS ID pharmacist review. The integration of these 2 strategies was associated with improvement in optimal care of SAB. Specifically, mandatory IDC and AMS ID pharmacist review was associated with increased adherence to SAB quality care bundle and achievement of source control. These interventions were also associated with a numerically lower rate of 30-day readmission for SAB, and all patients in the combined intervention period received intravenous empiric and definitive therapy. This was not the case for a small number of patients in periods 1 and 2 who were either discharged on no therapy before blood culture results were available or were given oral therapy.
The results of this study suggest that there is additional benefit to AMS review for SAB patients at an institution with mandatory IDC for SAB already in place. This is consistent with findings from Buehrle and colleagues [22], who evaluated the effect of IDC on the management of SAB at an institution with a comprehensive AMS program already in place. These authors demonstrated that patients with IDC were more likely to receive guideline-recommended management and had reduced mortality. However, improvements in antimicrobial choice or dosing were not seen, perhaps due to the preexisting AMS review. Around-the-clock AMS review of patients with positive blood cultures may provide additional benefit, as delayed appropriate SAB treatment is associated with increased mortality [24]. Real-time AMS review has been shown to decrease time to optimal antimicrobial therapy for bacteremia patients [25]. Specific to SAB, Nguyen and colleagues [20] implemented a pharmacist-driven real-time AMS review with quality care bundle recommendations that was associated with improved bundle adherence and decreased 30-day SAB-related readmission even though a majority of patients had IDC. Therefore, a multidisciplinary approach achieved by combining IDC and AMS review may garner additional benefit for patients with SAB.
IDC remains an integral part of this multidisciplinary approach for improving SAB care. ID physician–led bundled interventions for SAB have also been shown to improve adherence to quality care indicators and decrease mortality [4, 16, 26, 27]. Bedside IDC has been shown to be more effective than a telephone consult for SAB [13, 28]. An AMS intervention that recommends IDC for SAB patients may not be as effective as mandating IDC. Previous studies of pharmacist-led AMS bundles for SAB have included recommending IDC as a component of the intervention, with varied success. Smith and colleagues [21] achieved 100% IDC in their postintervention group. However, other similar studies have shown an IDC rate ranging from 60% to 93.4%; all these results were lower than the IDC rate of 95% seen in our cohort before IDC was mandated [18–20].
We observed a longer average hospital LOS in period 3, our combined intervention group, compared with periods 1 and 2. Because more patients in period 3 had complicated bacteremia and metastatic sites of infection, they may have required a longer hospital stay in order to obtain source control. Remtulla and colleagues [19] observed a similar increase in LOS and decrease in patients with uncomplicated bacteremia in their study of a successful AMS intervention for SAB. We observed a nonsignificant decrease in 30-day SAB-related readmission from 10 patients in period 1 to 0 patients in periods 2 and 3, which was consistent with findings from previous studies [19, 27, 29]. We did not see a mortality benefit, possibly due to the already low 4.3% mortality in period 1. The high rate of IDC before IDC was mandated for all patients may have also contributed. Previous studies that demonstrated a mortality benefit with IDC had a much lower baseline rate of IDC, ranging from 33% to 67% [8–10]. This likely made differences in mortality easier to detect. The mortality rate seen in our study was similar to the postintervention 3% mortality found in a similar study by Smith and colleagues [21], which also excluded patients who transitioned to hospice care and those who died or transferred to another institution shortly after admission.
Other novel interventions for SAB care have been investigated. Djelic and colleagues [30] implemented a process to notify ID physicians of blood cultures positive for S. aureus in real time, which was similar to our real-time notification of AMS pharmacists. This intervention was associated with decreased time to IDC and improved adherence to quality care indicators. Real-time notification of SAB detection for ID physicians may be an effective method for ensuring prompt IDC, especially for institutions like ours that mandate IDC for SAB patients. Wenzler and colleagues [29] developed an automated scoring tool for SAB within their EMR for use by frontline pharmacists working all shifts. The intervention was associated with improved adherence to quality care indicators and a decrease in mortality. Similarly, Brotherton and colleagues [31] created a best practice advisory alert within their EMR that provided physicians with recommendations for SAB management and was associated with improved bundle adherence. It is unclear how these types of interventions compare to involvement of physicians and pharmacists specially trained in infectious diseases. Utilization of rapid diagnostic testing may also have a role in improving outcomes, particularly by shortening time to definitive therapy [32]. After the completion of data collection for this study, our institution began using a new FDA-approved polymerase chain reaction testing for all blood culture isolates with a gram stain of gram-positive cocci in clusters. This technology can rapidly identify S. aureus and detect MRSA resistance genes, and its impact on patient outcomes may warrant further investigation.
The limitations of our study include its retrospective design and reliance on manual chart review for data collection. There were a limited number of patients eligible to be included in period 2, owing to the timing of the implementation of the 2 interventions examined in this study. This may have hindered our ability to detect statistical differences between our 3 periods. Another important limitation of our analysis is the already high rate of IDC in period 1, which may account for the lack of improvement seen from period 1 to period 2. Additionally, there was an ID pharmacist employed at 1 of the 7 hospitals included in this study before the implementation of the real-time AMS review who provided recommendations for SAB patients, which may have also confounded the results of our study. The strengths of this study include the multisite design and the unique combination of mandatory IDC followed by the implementation of a real-time AMS review.
In conclusion, this study describes an effective real-time, pharmacist-driven AMS review that was associated with improved management of SAB in the setting of preexisting mandatory IDC. Combining mandatory IDC and AMS review was associated with increased adherence to a bundle of quality care indicators and improvement in the rate of source control. Our study is unique in that it demonstrates the benefit of AMS review in addition to IDC for optimizing SAB care.
Acknowledgments
Financial support. This study was carried out as part of our routine work.
Potential conflicts of interest. All authors: no reported conflicts of interest. All authors have submitted the ICMJE Form for Disclosure of Potential Conflicts of Interest. Conflicts that the editors consider relevant to the content of the manuscript have been disclosed.
Prior presentation. This work was previously presented as a poster at IDWeek 2019 in Washington, DC.
References
- 1. Biedenbach DJ, Moet GJ, Jones RN. Occurrence and antimicrobial resistance pattern comparisons among bloodstream infection isolates from the SENTRY Antimicrobial Surveillance Program (1997–2002). Diagn Microbiol Infect Dis 2004; 50:59–69. [DOI] [PubMed] [Google Scholar]
- 2. van Hal SJ, Jensen SO, Vaska VL, et al. Predictors of mortality in Staphylococcus aureus bacteremia. Clin Microbiol Rev 2012; 25:362–86. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 3. Vogel M, Schmitz RP, Hagel S, et al. Infectious disease consultation for Staphylococcus aureus bacteremia - a systematic review and meta-analysis. J Infect 2016; 72:19–28. [DOI] [PubMed] [Google Scholar]
- 4. Borde JP, Batin N, Rieg S, et al. Adherence to an antibiotic stewardship bundle targeting Staphylococcus aureus blood stream infections at a 200-bed community hospital. Infection 2014; 42:713–9. [DOI] [PubMed] [Google Scholar]
- 5. Tissot F, Calandra T, Prod’hom G, et al. Mandatory infectious diseases consultation for MRSA bacteremia is associated with reduced mortality. J Infect 2014; 69:226–34. [DOI] [PubMed] [Google Scholar]
- 6. Fries BL, Licitra C, Crespo A, et al. Infectious diseases consultation and the management of Staphylococcus aureus bacteremia. Clin Infect Dis 2014; 58:598–9. [DOI] [PubMed] [Google Scholar]
- 7. Robinson JO, Pozzi-Langhi S, Phillips M, et al. Formal infectious diseases consultation is associated with decreased mortality in Staphylococcus aureus bacteraemia. Eur J Clin Microbiol Infect Dis 2012; 31:2421–8. [DOI] [PubMed] [Google Scholar]
- 8. Lahey T, Shah R, Gittzus J, et al. Infectious diseases consultation lowers mortality from Staphylococcus aureus bacteremia. Medicine (Baltimore) 2009; 88:263–7. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 9. Honda H, Krauss MJ, Jones JC, et al. The value of infectious diseases consultation in Staphylococcus aureus bacteremia. Am J Med 2010; 123:631–7. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 10. Rieg S, Peyerl-Hoffmann G, de With K, et al. Mortality of S. aureus bacteremia and infectious diseases specialist consultation—a study of 521 patients in Germany. J Infect 2009; 59:232–9. [DOI] [PubMed] [Google Scholar]
- 11. Bai AD, Showler A, Burry L, et al. Impact of infectious disease consultation on quality of care, mortality, and length of stay in Staphylococcus aureus bacteremia: results from a large multicenter cohort study. Clin Infect Dis 2015; 60:1451–61. [DOI] [PubMed] [Google Scholar]
- 12. Pastagia M, Kleinman LC, Lacerda de la Cruz EG, Jenkins SG. Predicting risk for death from MRSA bacteremia. Emerg Infect Dis 2012; 18:1072–80. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 13. Forsblom E, Ruotsalainen E, Ollgren J, Järvinen A. Telephone consultation cannot replace bedside infectious disease consultation in the management of Staphylococcus aureus bacteremia. Clin Infect Dis 2013; 56:527–35. [DOI] [PubMed] [Google Scholar]
- 14. Chesdachai S, Kline S, Helmin D, et al. The effect of infectious diseases consultation on mortality in hospitalized patients with MRSA, Candida, and Pseudomonas bloodstream infections. Open Forum Infect Dis 2020; 7:XXX–XX. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 15. Jenkins TC, Price CS, Sabel AL, et al. Impact of routine infectious diseases service consultation on the evaluation, management, and outcomes of Staphylococcus aureus bacteremia. Clin Infect Dis 2008; 46:1000–8. [DOI] [PubMed] [Google Scholar]
- 16. Nagao M, Yamamoto M, Matsumura Y, et al. Complete adherence to evidence-based quality-of-care indicators for Staphylococcus aureus bacteremia resulted in better prognosis. Infection 2017; 45:83–91. [DOI] [PubMed] [Google Scholar]
- 17. Johannsson B, Johnson SJ, Ernst EJ, et al. Antimicrobial therapy for bloodstream infection due to methicillin-susceptible Staphylococcus aureus in an era of increasing methicillin resistance: opportunities for antimicrobial stewardship. Ann Pharmacother 2012; 46:904–5. [DOI] [PubMed] [Google Scholar]
- 18. Bauer KA, West JE, Balada-Llasat JM, et al. An antimicrobial stewardship program’s impact with rapid polymerase chain reaction methicillin-resistant Staphylococcus aureus/S. aureus blood culture test in patients with S. aureus bacteremia. Clin Infect Dis 2010; 51:1074–80. [DOI] [PubMed] [Google Scholar]
- 19. Remtulla S, Zurek K, Cervera C, et al. Impact of an unsolicited, standardized form-based antimicrobial stewardship intervention to improve guideline adherence in the management of bacteremia. Open Forum Infect Dis 2019; 6:XXX–XX. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 20. Nguyen CT, Gandhi T, Chenoweth C, et al. Impact of an antimicrobial stewardship-led intervention for Staphylococcus aureus bacteraemia: a quasi-experimental study. J Antimicrob Chemother 2015; 70:3390–6. [DOI] [PubMed] [Google Scholar]
- 21. Smith JR, Frens JJ, Snider CB, Claeys KC. Impact of a pharmacist-driven care package on Staphylococcus aureus bacteremia management in a large community healthcare network: a propensity score-matched, quasi-experimental study. Diagn Microbiol Infect Dis 2018; 90:50–4. [DOI] [PubMed] [Google Scholar]
- 22. Buehrle K, Pisano J, Han Z, Pettit NN. Guideline compliance and clinical outcomes among patients with Staphylococcus aureus bacteremia with infectious diseases consultation in addition to antimicrobial stewardship-directed review. Am J Infect Control 2017; 45:713–6. [DOI] [PubMed] [Google Scholar]
- 23. Liu C, Bayer A, Cosgrove SE, et al. ; Infectious Diseases Society of America Clinical practice guidelines by the Infectious Diseases Society of America for the treatment of methicillin-resistant Staphylococcus aureus infections in adults and children. Clin Infect Dis 2011; 52:e18–55. [DOI] [PubMed] [Google Scholar]
- 24. Lodise TP, McKinnon PS, Swiderski L, Rybak MJ. Outcomes analysis of delayed antibiotic treatment for hospital-acquired Staphylococcus aureus bacteremia. Clin Infect Dis 2003; 36:1418–23. [DOI] [PubMed] [Google Scholar]
- 25. Beganovic M, Costello M, Wieczorkiewicz SM. Effect of matrix-assisted laser desorption ionization-time of flight mass spectrometry (MALDI-TOF MS) alone versus MALDI-TOF MS combined with real-time antimicrobial stewardship interventions on time to optimal antimicrobial therapy in patients with positive blood cultures. J Clin Microbiol 2017; 55:1437–45. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 26. López-Cortés LE, Del Toro MD, Gálvez-Acebal J, et al. ; REIPI/SAB group Impact of an evidence-based bundle intervention in the quality-of-care management and outcome of Staphylococcus aureus bacteremia. Clin Infect Dis 2013; 57:1225–33. [DOI] [PubMed] [Google Scholar]
- 27. Townsend J, Pelletier J, Peterson G, et al. Quality improvement of Staphylococcus aureus bacteremia management and predictors of relapse-free survival. Am J Med 2016; 129:195–203. [DOI] [PubMed] [Google Scholar]
- 28. Saunderson RB, Gouliouris T, Nickerson EK, et al. Impact of routine bedside infectious disease consultation on clinical management and outcome of Staphylococcus aureus bacteraemia in adults. Clin Microbiol Infect 2015; 21:779–85. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 29. Wenzler E, Wang F, Goff DA, et al. An automated, pharmacist-driven initiative improves quality of care for Staphylococcus aureus bacteremia. Clin Infect Dis 2017; 65:194–200. [DOI] [PubMed] [Google Scholar]
- 30. Djelic L, Andany N, Craig J, et al. Automatic notification and infectious diseases consultation for patients with Staphylococcus aureus bacteremia. Diagn Microbiol Infect Dis 2018; 91:282–3. [DOI] [PubMed] [Google Scholar]
- 31. Brotherton AL, Rab S, Kandiah S, et al. The impact of an automated antimicrobial stewardship intervention for the management of Staphylococcus aureus bacteraemia utilizing the electronic health record. J Antimicrob Chemother 2020; 75:1054–60. [DOI] [PubMed] [Google Scholar]
- 32. Beganovic M, McCreary EK, Mahoney MV, et al. Interplay between rapid diagnostic tests and antimicrobial stewardship programs among patients with bloodstream and other severe infections. J Appl Lab Med 2019; 3:601–16. [DOI] [PubMed] [Google Scholar]