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An Intervention To Improve Antibiotic Delivery and Sputum Procurement in Patients Hospitalized With Community-Acquired Pneumonia^*

^* From the Division of Infectious Diseases (Drs. Lawrence and Mundy) and Division of Emergency Medicine (Dr. Hall), Washington University School of Medicine; and Saint Louis University School of Public Health (Dr. Leet) and Center for the Study of Bioterrorism and Emerging Infections (Dr. Shadel), St. Louis, MO.

Correspondence to: Steven J. Lawrence, MD, Washington University School of Medicine, Division of Infectious Diseases, 660 South Euclid Ave, Campus Box 8051, St. Louis, MO 63110; e-mail: slawrenc{at}im.wustl.edu

	Abstract

TOP Abstract Introduction Materials and Methods Results Discussion References

 
Study objectives: To determine if an educational intervention targeting emergency department (ED) and medicine staff could successfully decrease the time to antibiotic delivery (door-to-drug delivery time [DDD]) for patients admitted through the ED with community-acquired pneumonia (CAP).

Design: Prospective, multidisciplinary team-based educational project. Demographics, outcomes, and processes of care including DDD and sputum procurement for patients with CAP were determined during a baseline period and compared to the same parameters for patients with CAP presenting after the educational intervention was administered to ED and medicine staff.

Setting: Barnes-Jewish Hospital, a large Midwest teaching institution affiliated with the Washington University School of Medicine.

Patients: Consecutive adult patients admitted through the ED with CAP.

Intervention: Multidisciplinary in-service education administered to ED physicians and nurses, and medicine housestaff, which emphasized the importance of rapid antibiotic delivery and procurement of preantibiotic expectorated sputum.

Results: Mean DDD improved from 413 to 291 min (p = 0.02), with more patients receiving antibiotics in the ED (46% vs 69%; adjusted odds ratio [OR], 2.3; 95% confidence interval [CI], 1.0 to 4.9). Sputum procurement improved from 11.5 to 25.4% (adjusted OR, 3.3; 95% CI, 1.1 to 9.9). There were no observed differences for inpatient mortality or length of stay.

Conclusion: This multidisciplinary team intervention significantly improved the time to initiation of antibiotics and procurement of sputum for patients with CAP.

Key Words: antibiotic • community-acquired pneumonia • drug delivery • quality improvement • sputum

	Introduction

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Community-acquired pneumonia (CAP) affects 2 to 3 million people annually, causing approximately 45,000 deaths, making it the leading infectious cause of mortality in the United States.^{1 2 3} Larger studies have estimated mortality for hospitalized patients with CAP at 7 to 14%,^{4 5 6} and median length of stay (LOS) from 5 to 8 days, with a high degree of interhospital variability.^{4 7 8} Many efforts have been made in recent years to identify and improve processes of care for patients with CAP. Those that have been most frequently identified include the time elapsed prior to initiation of antibiotic therapy (the door-to-drug delivery time [DDD]) and performance of preantibiotic blood cultures and expectorated sputum Gram stain and culture.^{9 10 11 12}

Meehan and colleagues⁹ demonstrated an important link between a DDD of < 8 h and 30-day mortality in an elderly CAP population. Subsequently, there have been few reported quality improvement projects describing interventions to improve the DDD. Metersky and colleagues¹⁰ reported a statistically significant aggregate DDD reduction from 5.5 to 4.7 h in four of six participating hospitals that implemented separate, nonstandardized interventions. The improvement was attributed to an increase in the receipt of first dose of antibiotic within 4 h and in the emergency department (ED).¹⁰ McGarvey and Harper¹² initiated a clinical pathway that led to a higher proportion of patients receiving antibiotics within 4 h (from 42 to 87%); however, statistical significance was not reported. Other groups have also recognized the importance of antibiotic receipt within 4 h.¹³

In their respective consensus guidelines for the management of CAP, the Infectious Diseases Society of America (IDSA) advocates routine preantibiotic expectorated sputum procurement and analysis by Gram stain and culture,^{14 15} while the American Thoracic Society (ATS) recommends performance of these diagnostic studies only if resistant pathogens are suspected.¹⁶ The controversy over routine sputum analysis is longstanding because of the many factors that limit its diagnostic utility,^{17 18 19 20 21} the wide range of reported sensitivities and specificities (35 to 96% and 12 to 96%, respectively),^{17 22 23 24 25 26 27 28} and the lack of controlled studies to indicate that sputum analysis improves outcomes for patients with CAP. Nonetheless, the rationale for the IDSA recommendation was that sputum analysis is an inexpensive test that, if done correctly, can guide antibiotic selection to better treat resistant organisms, avoid excess cost and adverse effects associated with broader spectrum antibiotics, and reduce the spread of antibiotic resistance.^{14 15} Indeed, a prospective study²⁸ confirmed that although sensitivity is not high, positive sputum analysis findings can help guide therapy. In this setting of conflicting recommendations, routine sputum analysis for CAP patients is not standard practice in some institutions.²⁹ The purpose of this study was to improve time to initiation of antibiotics and procurement of preantibiotic expectorated sputum from patients presenting to the ED with CAP, in accordance with guideline recommendations.

	Materials and Methods

TOP Abstract Introduction Materials and Methods Results Discussion References

 
Patients
Patients were admitted to Barnes-Jewish Hospital in St. Louis, MO, a tertiary care, university-affiliated medical center with 880 licensed medical/surgical/intensive care beds that provides primary care for the city of St. Louis, as well as referral care for the region. Consecutive patients who were admitted to the housestaff-covered medicine service with a putative diagnosis of CAP between July 7, 1996, and March 31, 1997, were eligible. Inclusion criteria were patients at least 18 years old with a new infiltrate on chest radiography, and either one major or two minor clinical criteria. Major criteria consisted of cough, sputum production, or temperature > 37.8°C, while minor criteria were pleuritic chest pain, dyspnea, altered mental status, pulmonary consolidation on examination, or WBC count > 12,000/µL.³⁰ Immunocompromised patients, defined as those infected with HIV type 1, those who had undergone solid-organ or bone marrow transplant, those having a chronic disease requiring active immunosuppressive therapy or high-dose steroids (receiving at least 21 days of 40 mg/d of prednisone equivalent during the prior year), or those who received chemotherapy in the previous month, were identified and included.²¹ The rationale for including immunocompromised patients was that DDD would be perhaps even more important as a quality indicator for this subset of patients. Also, routine sputum analysis would still play a diagnostic role, as typical bacteria remain the most common identified etiology of CAP in HIV-infected patients.^{21 31} Residents of nursing homes and extended care facilities were also included. Patients who had been previously hospitalized within 14 days prior to admission were presumed to have nosocomial pneumonia and therefore excluded. Those patients transferred from another acute care facility, and those admitted to the hospital directly from home or from a physician’s office were excluded because they were not initially evaluated in the ED, where the educational intervention was focused. Patients admitted to a service other than housestaff-covered general medicine wards were excluded because these floors were the points of identification for eligible patients. This study was approved by the Washington University School of Medicine Human Studies Committee.

Study Definitions
Pneumonia severity of illness index (PSI) scores were calculated using the validated formulas by Fine et al.³² For each patient, an estimated mortality risk was calculated based on history and physical examination data, comorbid illnesses, and laboratory and radiographic abnormalities. Patients were stratified into low (< 4%), moderate (4 to 15%), or high (> 15%) risk of death during the first 60 days after hospital admission, and respectively grouped into PSI categories 1, 2, or 3. The breakpoints outlining the escalating classes of risk were based on the more recent mortality prediction work by Fine et al.³³ The low-risk group (category 1) in our study corresponds to Fine PSI classes I, II, or III, while the moderate- and high-risk groups (categories 2 and 3) correspond to PSI classes IV and V, respectively.

The DDD was defined as the time elapsed between the time of presentation recorded on the ED triage sheet to the time of antibiotic administration as recorded by the nursing staff. Sputum procurement was calculated by dividing the number of patients from whom preantibiotic expectorated sputum was collected by the total number of included patients within each study period. All sputum specimens were reviewed in the usual manner by trained microbiology laboratory technicians and were subjected to a standard cytologic screening procedure. The specimens were considered cytologically adequate and subsequently processed for culture only if 10 squamous epithelial cells per low-power field were seen or if sheets of polymorphonuclear leukocytes existed with a corresponding predominant organism on Gram stain regardless of squamous epithelial cell abundance. LOS was defined as the number of whole days elapsed between presentation to the ED and discharge to home or another facility, or to death. Mortality was defined as death during the hospitalization period from all causes. No follow-up data were available regarding mortality or health status subsequent to discharge.

Etiology Determination
The etiologies of pneumonia were classified as definitive, presumptive, or unknown.³⁰ Attempts were not made to exclude large-volume aspiration pneumonia. The performance of etiologic diagnostic tests was left to the discretion of the medicine team and reflects the pattern of routine diagnostic workup typically pursued at the study institution. Rates of performance of blood culture and sputum analysis were measured.

Intervention Strategies
Study patients were prospectively followed as part of a multidisciplinary team effort. The team included two physicians (infectious diseases and emergency medicine), an epidemiologist, a pharmacist, two ED nurses, and a group facilitator with expertise in quality improvement. The baseline (preintervention) period was from July 7, 1996, through November 30, 1996. Prior to the intervention period, the study protocol and rationale were presented to ED physicians, ED nurses, and medicine housestaff. For the ED physicians, a review of CAP, the study protocol, and study rationale were presented at the weekly ED grand rounds. For the ED nurses, the nurse supervisors presented the study protocol and rationale to staff on each nursing shift. For the medicine housestaff and interested faculty, a brief review of CAP, the study protocol, and study rationale were presented at medicine firm conferences. A review of appropriate initial antibiotic choices based on the 1993 ATS guidelines was part of the intervention, with the consideration of atypical etiologies such as Pneumocystis carinii in immunocompromised hosts and Mycobacterium tuberculosis in at-risk hosts. During the intervention period from December 1, 1996, through March 31, 1997, monthly in-service education and feedback on DDD and rates of preantibiotic expectorated sputum procurement were given to ED physicians, ED nurses, and medicine housestaff. This intervention was focused on the objectives and rationale for improved DDD and preantibiotic sputum procurement in the ED. Adequate supplies of typical antibiotics used for CAP were stocked in the ED, already prepared for immediate administration. Antibiotics ordered after the patients’ arrival on the medicine floor required preparation and delivery of the drug by the pharmacy.

Data Analysis
Descriptive statistics were reported as frequency distributions, means, and medians as appropriate. Demographic, health status, and outcome data for patients in the preintervention group were compared to the data in the postintervention group using the ² test for categorical variables and the t test for continuous variables. Two-tailed p values were considered significant if 0.05. Logistic regression was used to calculate odds ratios (ORs) for the preintervention and postintervention sputum procurement and DDD (categorized as 4 h or 8 h). DDD results (in minutes) between the preintervention and postintervention groups were compared by analysis of variance. Statistical software (Version 10.0 for Windows; SPSS; Chicago, IL) was used for all statistical analysis.

	Results

TOP Abstract Introduction Materials and Methods Results Discussion References

 
Patient Characteristics
There were 120 patients presenting with a putative diagnosis of CAP during the study period who met inclusion criteria. One patient was excluded because ED data were not available. Of the remaining 119 patients, 1 patient was admitted twice for CAP during the study period. Only the first episode of care for this patient was included. Both groups were demographically similar with the exception of immune status (Table 1 ). Overall, 14.3% of patients were immunocompromised, however a higher percentage was in the preintervention group. The PSI at presentation to the ED was similar in the preintervention and postintervention groups.

Other Outcomes:
Two immunocompetent patients (1.7%) died during the study, both in the postintervention group, although no statistically significant difference between groups existed (Table 2) . The DDDs for these two patients were 126 min and 102 min, respectively. However, both were in the highest risk PSI category 3. There was no difference in the LOS between the preintervention and postintervention groups. Blood cultures were obtained from 93 of 110 patients (84.5%) for whom blood culture data were available.

Etiology of Pneumonia
An etiologic diagnosis was determined for 11% of the patients studied (Table 3 ). Of these etiologic agents, Streptococcus pneumoniae was the only organism identified more than once. Of the four pneumococcal cases, three cases were diagnosed by blood culture and one case was diagnosed from routine culture of preantibiotic-expectorated sputum. Sputum culture also supported blood culture results for the case of bacteremic pneumonia from group A Streptococcus. There were four cases of Gram-negative pneumonia, three definitive cases diagnosed by blood culture, and one presumptive case from sputum. In total, routine expectorated sputum analysis provided an etiology for two cases (1.7%).

	Discussion

TOP Abstract Introduction Materials and Methods Results Discussion References

 
Many important processes of care for patients with CAP, including time to initiation of antibiotics and preantibiotic acquisition of blood and sputum for culture, have recently been defined as quality of care indicators. This study assessed the effectiveness of a multidisciplinary intervention administered to ED physicians, ED nurses, and medicine housestaff with the goal of improving these two processes of care. The most important finding from this study showed that this multidisciplinary intervention was successful in improving the DDD to patients with CAP presenting to the ED. A significant reduction of the DDD by > 2 h was achieved with a nearly 50% increase in the proportion of patients receiving drug in the ED prior to transfer to the medicine floor. As a result, more patients in the postintervention group received drug within the 4-h time frame that has been reported in recent literature,^{10 12} but has not been shown to be associated with decreased mortality. Of note, the improvement in DDD demonstrated by this intervention was not associated with the traditional outcomes of mortality or LOS. In brief intervention projects, there is the risk that a demonstrated effect may be temporary and will disappear after a washout period. This diminished effect is particularly a concern in an ED setting where the intervention may be missed by the physicians who were not in the work rotation during the intervention period and by many staff nurses because of the traditionally high personnel turnover. However, follow-up assessment of DDD among 77 hospitalized CAP patients at our institution in the winter of 1998–1999 identified a sustained effect of 68.5% among patients who received first dose of antibiotic in the ED. The mean DDD for patients receiving drug in the ED was 3.1 h, and for those receiving drug on the medicine floors it was 9.6 h (unpublished data).

There was a marginal improvement in the proportion of patients from whom expectorated sputum was collected after adjusting for potential confounding factors including PSI, immune status, and altered mental status. However, the resulting sputum procurement was still low after the intervention, a finding that we believe reflects continued support of the diagnostic approach advocated by the ATS guidelines.¹⁶

Notably, of the 23 patients from our study for whom expectorated sputum was collected, only 12 patients (52.2%) had specimens categorized as adequate by cytologic standards. Based on this, it seems that further emphasis on obtaining a purulent, deep cough specimen must be made. Procurement by nurses or physicians may be necessary, as those with more advanced training may be better able to recognize a nonpurulent sample and encourage further efforts from the patient. It is unlikely that this low yield from routine analysis of expectorated sputum was a result of transport and processing, as all specimens underwent Gram stain preparation within 60 min of procurement. Consistent with prior studies, there was no demonstrable impact of sputum procurement and analysis on mortality or LOS.

The proportion of patients in whom an etiologic diagnosis was determined in this study is similar to a recent survey of nonsevere CAP,³⁴ but somewhat lower than most others have reported for routine etiology analysis.^{4 35} Reasons for the low rate of identified CAP etiologies may include the strict definition used for assignment of an etiology, the lack of adequate sputum procurement, the lack of use of investigational diagnostic tests such as throat swab polymerase chain reaction for atypical agents, and the lack of use of preconvalescent and postconvalescent sera for complement fixation studies as often used in epidemiologic surveys. Sputum analysis did not contribute substantially to the determination of etiology in this study as a result of the overall low number of adequate specimens procured. From the 12 adequate expectorated sputum samples, 2 samples resulted in an etiologic diagnosis (8.7% of all sputa collected, 16.7% of adequate samples), and 1 specimen supported the definitive diagnosis established by blood culture. This study will do little to end the ongoing controversy regarding the usefulness of routine expectorated sputum analysis. Nonetheless, the unimpressive results of sputum analysis in this small study do not undermine the rationale for performing these tests as advocated by the IDSA.^{14 15} Indeed, there were two patients for whom routine analysis of expectorated sputum was the sole positive diagnostic test. One was a pneumococcal case in which antibiotic therapy could potentially be narrowed, and the other was a Gram-negative pneumonia that may have required additional coverage.

An important limitation of this study was the small sample size, which may prevent differences in infrequent outcomes such as mortality from becoming apparent. The other chief limitation was selection bias in identifying the patient population. Although consecutive patients were identified and then prospectively followed up within each study period, the population was restricted to patients admitted to general medicine floors. The interventions were targeted to ED staff and medicine housestaff, and the point of identification was after admission to the floor. The exclusion of patients initially admitted to an ICU certainly biased the study population to be of lesser pneumonia severity of illness than all patients admitted with CAP. However, the 16.8% of the population that were in PSI category 3 on presentation indicate that this high-risk group was represented in this study. In concert with the lesser severity of illness represented by a nonintensive care patient population, mortality was lower and median hospital LOS was shorter than in most other studies.^{4 5 6 7 8} Finally, this study was conducted at a single site and may not be entirely generalizable to other institutions.

There are several reasons for the success of this intervention. First, and perhaps most importantly, was that it received physician buy-in, from both medicine and ED physicians. Another key component was that it was a multidisciplinary effort across the CAP episode of care, involving health-care providers at both presentation and continued care on the floor. Thirdly, the intervention provided monitoring of results and gave feedback to the involved healthcare providers in order to encourage continued application of the intervention principles.

Much of the recent research involving CAP has focused on attempts to identify and improve processes of care. Differences in these quality indicators, however, have infrequently been associated with more traditional outcomes such as mortality and hospital LOS. Future studies with larger patient populations will be necessary to further elucidate the clinical importance of some of the recognized processes of care, such as DDD within 4 h and sputum analysis, for hospitalized patients with CAP. Additionally, more subjective outcomes such as health status after defined periods of time following a CAP episode and quality of life should be investigated, as it is not known how improvements in the currently defined processes of care affect these parameters.

	Acknowledgements

 
We thank Greg Evans for statistical guidance, Joan Hoppe-Bauer for microbiology laboratory support and data acquisition, Cindy Lefton for coordination of training for ED personnel, Jordana Stewart for data entry and secretarial support, and Elaine Suttle for assistance in obtaining medical charts.

	Footnotes

 
Abbreviations: ATS = American Thoracic Society; CAP = community-acquired pneumonia; CI = confidence interval; DDD = door-to-drug delivery time; ED = emergency department; IDSA = Infectious Diseases Society of America; LOS = length of stay; OR = odds ratio; PSI = pneumonia severity of illness index

Work performed at Barnes-Jewish Hospital, St. Louis, MO.

Received for publication November 19, 2001. Accepted for publication March 5, 2002.

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This Article Abstract Full Text (PDF) Free Submit a response Alert me when this article is cited Alert me when eLetters are posted Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in ISI Web of Science Similar articles in PubMed Alert me to new issues of the journal Add to My Personal Article Archive Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via ISI Web of Science (7) Citing Articles via Google Scholar Google Scholar Articles by Lawrence, S. J. Articles by Mundy, L. M. Search for Related Content PubMed PubMed Citation Articles by Lawrence, S. J. Articles by Mundy, L. M.