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(Chest. 2001;119:1420-1426.)
© 2001 American College of Chest Physicians

Empiric Antibiotic Therapy and Mortality Among Medicare Pneumonia Inpatients in 10 Western States*

1993, 1995, and 1997

Peter M. Houck, MD; Richard F. MacLehose, MS; Michael S. Niederman, MD, FCCP and Joseph K. Lowery, PhD

* From the Health Care Financing Administration (Drs. Houck and Lowery, and Mr. MacLehose), Region 10, Seattle, WA; and Winthrop University Hospital (Dr. Niederman), Mineola, NY.

Correspondence to: Peter Houck, MD, HCFA, MS RX-40, 2201 Sixth Ave, Seattle, WA 98121; e-mail: phouck{at}hcfa.gov


   Abstract
TOP
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 Conclusion
 References
 
Study objectives: To examine the association of empiric inpatient antibiotic treatment of community-acquired pneumonia (CAP) with mortality, and whether this association varies from year to year.

Design: Population-based, retrospective study adjusting for demographics, comorbidities, and clinical characteristics.

Setting: Acute-care hospitals in 10 western states.

Patients: A group of 10,069 Medicare beneficiaries aged >= 65 years who were hospitalized with CAP during fiscal years 1993, 1995, and 1997.

Measurements and results: We examined the risk for mortality during the 30 days after admission to the hospital. The impact of specific antibiotic regimens varied greatly from year to year. In 1993, therapy with a macrolide plus a ß-lactam was associated with significantly lower mortality than therapy with either a ß-lactam alone (adjusted odds ratio [AOR], 0.42; 95% confidence interval [CI], 0.25 to 0.69) or other regimens that did not include a macrolide, ß-lactam, or fluoroquinolone (AOR, 0.35; 95% CI, 0.20 to 0.62). Those associations were not observed in 1995 or 1997. Lower mortality was associated with fluoroquinolone monotherapy compared with ß-lactam monotherapy in 1997 (AOR, 0.27; 95% CI, 0.07 to 0.96) and with macrolide monotherapy compared with other regimens in 1995 (AOR, 0.24; 95% CI, 0.06 to 0.93), but the number of patients who received these regimens was small.

Conclusions: The inclusion of a macrolide or a fluoroquinolone in initial empiric CAP treatment was associated with improved survival, but this association varied from year to year, perhaps as a result of a temporal variation in the incidence of atypical pathogen pneumonia. Improved testing and surveillance for atypical pathogen pneumonia are needed to guide empiric therapy.

Key Words: atypical pathogen • community-acquired • macrolide • mortality • pneumonia


   Introduction
TOP
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 Conclusion
 References
 
Pneumonia ranks second among reasons for the short-term hospitalization of Medicare beneficiaries, accounting for > 600,000 discharges from hospitals.1 With influenza, pneumonia ranked fifth among causes of death of persons aged >= 65 years in the United States during 1998.2 Previous reports have described clinical outcomes,3 4 5 6 but few have dealt with the impact of initial antibiotic therapy on mortality. Several reports have addressed antibiotic therapy and length of stay7 or mortality8 among patients at individual institutions.

Gleason et al9 have reported results of a population-based national study of Medicare patients who had been hospitalized with community-acquired pneumonia (CAP) in 1995. They observed that fluoroquinolone monotherapy or therapy with a macrolide combined with selected second-generation or third-generation cephalosporins was associated with lower mortality rates compared with therapy with third-generation cephalosporins alone. Such associations would be expected if there were a substantial incidence of pneumonia caused by atypical pathogens such as Legionella spp, Chlamydia pneumoniae, and Mycoplasma pneumoniae. There is increasing evidence that the incidence of infection and coinfection with these organisms is much higher than previously believed.10 11 12 13 14 15 16 Although some studies have demonstrated a benefit for adding a macrolide agent to a ß-lactam in CAP therapy, there are no population-based assessments of atypical organism coverage over several years. A multiyear assessment is needed because the frequency of atypical infection could vary over time.

We sought to confirm the results of the study by Gleason et al9 and to determine whether the associations they observed in 1995 varied from year to year. We used population-based data collected by the Seattle Regional Office of the Health Care Financing Administration on the care provided to Medicare inpatients who had CAP in the western United States during fiscal years 1993, 1995, and 1997. In this report, we describe associations between mortality during the 30 days after hospital admission and selected empiric antibiotic regimens.


   Materials and Methods
TOP
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 Conclusion
 References
 
Patients
The study populations included those Medicare beneficiaries with pneumonia who were admitted to hospitals in Arizona, California, Colorado, Hawaii, Montana, Nevada, New Mexico, Oregon, Utah, and Wyoming from October 1, 1992, through September 31, 1993 (ie, fiscal year 1993), from October 1, 1994, through September 31, 1995 (ie, fiscal year 1995), and from October 1, 1996, through September 31, 1997 (ie, fiscal year 1997). We included patients who lived independently or in nursing facilities.

Sample Plan
Sampling for each state and year was conducted independently. Medicare claims data were used to identify CAP hospitalizations. State-specific samples were drawn from among claims for beneficiaries who were aged >= 65 years and had an admitting or principal diagnosis with International Classification of Diseases, ninth Revision, Clinical Modification (ICD-9-CM)17 codes of 480.0 to 483.99, 485 to 486.99, or 487.0. There were > 85,000 such hospitalizations in each of the 3 years. Sample sizes allowed state-specific and year-specific estimations of prevalence with a precision of ± 5% at a 95% confidence level, conservatively assuming a true prevalence of 50%.18

Data Collection
Trained reviewers used standard protocols and software to abstract data from photocopies of medical records. The Medicare peer review organization in each state abstracted data for 1993. An outside organization (FMAS Corporation; Rockville, MD) abstracted data for the other years. Mortality data were obtained from the Medicare Enrollment Database.

Analysis
Analysis was limited to the following types of hospitalizations: the principal diagnosis ICD-9-CM code was 48X.XX; pneumonia was a physician’s clinical impression at the time of admission to the hospital; a chest radiograph taken within 48 h of hospital admission showed an acute infiltrate; the patient had not been transferred from another acute-care hospital; there had been no hospitalization during the previous 10 days; and the patient was not known to have HIV infection, acute lymphoma or leukemia, or to have undergone organ transplantation. The inclusion of hospitalizations for "comfort measures only" or for palliative care was minimized by excluding patients to whom antibiotics were not administered within 24 h of arrival at the hospital.

We used a statistical software package (STATA, version 6.0; STATA Corp; College Station, TX) for all analyses, including the development of logistic regression models that estimate adjusted odds ratios (AORs), {chi}2 tests, and 95% confidence intervals (CIs) for death within 30 days after admission to the hospital. The following six mutually exclusive antibiotic regimens that were initiated during the first 24 h after arrival at the hospital were evaluated: monotherapy with a ß-lactam (ie, second-generation, third-generation, or fourth-generation cephalosporins and ß-lactam/ß-lactamase inhibitor combinations); macrolide monotherapy; therapy with a ß-lactam plus a macrolide; fluoroquinolone monotherapy; therapy with a ß-lactam plus a fluoroquinolone; and any other antibiotics (ie, antibiotics other than ß-lactams, macrolides, or fluoroquinolones). We also examined separately therapy with ß-lactam/ß-lactamase inhibitor combinations and a macrolide. Population weights were used to account for sampling design.

Regression models were adjusted for documented prehospital antibiotic therapy, for antibiotic therapy initiated after 24 h in the hospital, for isolation of a pathogen from blood, for admission to an ICU during the initial 24 h in the hospital, and for severity of illness using a validated pneumonia-specific mortality risk index.6 That index included age, sex, nursing home residence, and five comorbid conditions and 12 physical or laboratory findings. All severity-related data came from the medical record except for a history of cerebrovascular disease and the presence of pleural effusion, for which ICD-9-CM secondary diagnosis codes were the source. The physical and laboratory values used were those first recorded during the patient’s initial 24 h at the hospital. A history of diabetes mellitus, coronary artery disease, splenectomy, or chronic lung disease, and the number of hours from hospital arrival to first antibiotic administration were evaluated but did not affect the odds ratios. Statistical significance for mortality analyses was defined by a 95% CI that excluded 1.00. The AOR point estimates were evaluated for linear trend over the 3 years, and the prevalence of patient characteristics was compared with likelihood ratio {chi}2 tests. Statistical significance was defined by a p value < 0.05.


   Results
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 Conclusion
 References
 
A total of 16,756 records were abstracted, with data from 10,069 records included in the analysis (1993, 3,032 records; 1995, 3,500 records; 1997, 3,537 records). Reasons for exclusion and principal diagnoses are shown in Table 1 .


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  		Table 1. Inclusion/Exclusion Criteria by Year*

 
Patient Characteristics
Patients’ demographic and clinical characteristics are described in Table 2 . The mean age of patients ranged from 79.1 to 79.5 years, and 48.8 to 50.8% of patients were men. Congestive heart failure was the most prevalent comorbid condition (27.5 to 28.7%), while the most common laboratory and physiologic abnormalities were elevated BUN level (25.4 to 27.0%) and elevated respiratory rates of >= 30 breaths/min (22.5 to 26.4%). There were significant annual prevalence differences in nine of the mortality risk index components. Patients in 1993 had the highest mean mortality risk score.


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  		Table 2. Patient Demographic and Clinical Characteristics by Year*

 
Antibiotic Treatment
Prehospital admission antibiotic treatment was documented for 18.3% (1993), 25.9% (1995), and 22.1% (1997) of patients. Prehospital macrolide use increased from 3.9% in 1993 to 6.5% in 1997 (Table 3 ). ß-Lactam monotherapy was the most commonly used antibiotic regimen during the first 24 h at the hospital, becoming less prevalent from 1993 to 1997 (Table 3) . Therapy with the combination of a macrolide and a ß-lactam was the second most commonly ordered regimen; its use more than doubled during the study period. Use of that combination was common among patients in the lower mortality risk strata, but 60% of all patients who received the combination therapy were in high-risk classes IV and V (Table 4 ). Therapy with a ß-lactam/ß-lactamase inhibitor combination with a macrolide accounted for 27 regimens (0.9%) in 1993, 31 regimens (0.9%) in 1995, and 35 regimens (1.0%) in 1997. Use of fluoroquinolones with enhanced activity against Streptococcus pneumoniae was first documented in 1997, when levofloxacin accounted for 6.5% of all fluoroquinolones used.


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  		Table 3. Antibiotic Treatment by Year*

 

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  		Table 4. Use of Initial Macrolide/ß-Lactam Combination by Mortality Risk Stratum and Year*

 
Mortality and Empiric Antibiotic Selection
The unadjusted 30-day mortality rate was 15.1% during 1993, 12.1% during 1995, and 13.0% during 1997. The unadjusted mortality rates and AORs comparing 30-day mortality rates for selected antibiotic regimens administered during the initial 24 h at the hospital are shown in Table 5 . The impact of initial treatment regimens that included macrolides or fluoroquinolones varied greatly from year to year. In 1993, a macrolide/ß-lactam combination therapy was associated with a significantly reduced mortality rate when compared with ß-lactam monotherapy (AOR, 0.42; 95% CI, 0.25 to 0.69) and other antibiotic regimens (AOR, 0.35; 95% CI, 0.20 to 0.62). This apparent macrolide benefit decreased significantly in 1995 and 1997. Macrolide monotherapy (n = 77) was associated with a reduced mortality rate in 1995 when compared with ß-lactam monotherapy (AOR, 0.29; not significant), and therapy with other antibiotics (AOR, 0.24; 95% CI, 0.06 to 0.93). In 1997, fluoroquinolone monotherapy (n = 52) was associated with reduced mortality when compared with ß-lactam monotherapy (AOR, 0.27; 95% CI, 0.07 to 0.96). Therapy with a ß-lactam/ß-lactamase inhibitor combination with a macrolide was associated with higher mortality than was monotherapy with a second-generation, third-generation, or fourth-generation cephalosporin in 1995 (12.9% vs 11.6%; AOR, 2.30), but the association was not significant. The numbers of patients treated with macrolide monotherapy or fluoroquinolones in any regimen (Table 3) or therapy with ß-lactam/ß-lactamase inhibitor combinations with a macrolide were very small.


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  		Table 5. Crude Mortality Rate and AOR of Death Within 30 Days of Hospital Admission for Antibiotic Regimens Used During the Initial 24 h of Hospitalization, by Year*

 

   Discussion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
Conclusion
 References
 
The most important finding of this study is that the addition of a macrolide to the initial empiric ß-lactam treatment of CAP patients was associated with significantly improved survival rates during 1993. This apparent macrolide benefit was greatly reduced and not statistically significant in 1995 and 1997, thus documenting yearly variability in the benefit from such therapy. We also found suggestive, but inconclusive and inconsistent, evidence that monotherapy with a macrolide or a fluoroquinolone is effective compared with therapy with ß-lactam and other antibiotics.

Any survival benefit of therapy with macrolides or fluoroquinolones might result from their activity against the atypical pathogens such as Legionella spp, C pneumoniae, or M pneumoniae, which are susceptible to these antibiotics. There is increasing evidence that these organisms, once described as unusual causes of pneumonia in older adults,19 are common etiologies. In four studies10 11 12 13 that included aggressive laboratory evaluations of adults with CAP, Legionella spp were detected in 10%,10 6%,11 2%,12 and 12%13 of patients. C pneumoniae was implicated in 8%,10 17%,11 2%,12 and 26%13 of patients, while M pneumoniae was detected in 3%,10 4%,11 5%,12 and 9%13 of patients. In a recent multicenter report,14 atypical pathogens accounted for 33% of cases. As many as 20 to 39% of CAPs might involve coinfection of atypical and typical organisms.15 16 20 In addition, the coinfection of patients with C pneumoniae with S pneumoniae may be associated with particularly severe illness.16 Legionella spp can cause severe pneumonia and have been reported to be the second leading cause of pneumonia in persons requiring ICU admission.21 Most treatment for atypical infection is empiric, because testing is not common in clinical practice. Only 4 to 6% of patients in our three assessments were evaluated for Legionella infection (P. M. Houck, unpublished observation), and clinically useful tests for C pneumoniae and M pneumoniae are not generally available. Routine testing has not been recommended by the American Thoracic Society (ATS)22 or the Infectious Diseases Society of America (IDSA),23 although newly revised IDSA guidelines24 recommend tests for Legionella in severely ill patients who have no other identified etiology.

An alternative explanation for the apparent benefit of adding a macrolide agent to a ß-lactam regimen in 1993 is that macrolides were used preferentially for patients in the lower severity strata. However, this hypothesis is not adequate by itself because the distribution of the use of that regimen among severity strata in 1993 was very similar to those in 1995 and 1997, years in which no significant macrolide-associated survival benefit was noted. In addition, in all years, approximately 60% of the patients who received this therapy fell into the two highest mortality risk strata.

The year-to-year variation in survival benefit associated with the inclusion of a macrolide in treatment regimens could result from changes in the incidence of infection or coinfection with the atypical pathogens. Local annual variation in the nonepidemic incidence of Legionella pneumonia has been reported,25 as have epidemics of disease caused by C pneumoniae.26 The current study, reflecting the general lack of testing for atypical pathogens in clinical practice, did not have etiologic data to address this possibility directly. Unfortunately, reliable population-based, multiyear, etiologic surveillance data also are not available to address this hypothesis indirectly. Most published reports of pneumonia etiology are for short periods of time or involve relatively few patients at a small number of hospitals. The incidence of Legionella infection reported passively to the Centers for Disease Control and Prevention did not show significant variation from 1980 through 198927 or 1993 through 1997,28 but these surveillance data are thought to underestimate the true incidence by a factor of >= 10.

Increasing antibiotic resistance might also affect the benefit of macrolide treatment. Doern et al29 30 reported the prevalence of macrolide resistance among S pneumoniae isolates from selected facilities in the United States to have increased only slightly from 10% in 1994-199529 to 13% in 1997.30 Ten percent of invasive S pneumoniae isolates in Washington state from October 1995 through January 1997 were not susceptible to erythromycin, but no significant temporal differences were detected.31 However, the significant reduction in the benefit of therapy of adding macrolides to ß-lactams that was seen from 1993 to 1997 would not likely be the result of macrolide-resistant S pneumoniae alone, because macrolides were coadministered with highly active antipneumococcal ß-lactams. Such a trend would more likely result from a decreased incidence of atypical infection or increased macrolide resistance among atypical organisms. Again, relevant data are not available to test these hypotheses.

Our findings add information to that presented by Gleason et al,9 who observed a survival benefit associated with macrolide and fluoroquinolone therapy among Medicare CAP patients hospitalized in all 50 states during 1995. In addition to our similar findings about the benefit of macrolides in the treatment of CAP, we observed also that treatment in 1995 with a ß-lactam/ß-lactamase inhibitor and a macrolide was associated, although not significantly, with increased mortality when compared with second-generation, third-generation, or fourth-generation cephalosporins. However, this association was not observed in 1993 and was both weak and nonsignificant in 1997, suggesting that the addition of a macrolide agent to a ß-lactam/ß-lactamase inhibitor does not consistently and adversely affect survival. This finding should be interpreted with caution because of the small number of patients involved. The reason that these two studies did not concur on the effect of adding a macrolide agent to a ß-lactam in 1995 is uncertain. A possible explanation is that our study was limited to the western United States, Gleason et al9 did not stratify their analysis by region, and there might be regional as well as temporal variations in the incidence of atypical pneumonia. Additional exploration of this hypothesis is needed.

Our study has both strengths and potential limitations. The use of random samples from the entire fee-for-service Medicare population avoids potential bias from reliance on volunteer institutions. Our database allowed adjustment for a large number of patient characteristics, including prehospital antibiotic therapy, blood culture results, and antibiotic therapy instituted after the initial 24 h in the hospital. As with any nonrandomized study, these findings must be interpreted with some caution, because we could not adjust for all potential confounders. The mortality risk index that we used, while probably the best tool available, does not account for all variance. Our ability to assess macrolide monotherapy and any regimen containing a fluoroquinolone was limited by the small number of patients who received those agents. Comparisons that include these regimens should be interpreted with particular caution. Our results are limited to the western United States only, and a possible regional variation needs to be explored.

Guidelines for the initial empiric antibiotic treatment of CAP in adult inpatients were published by the ATS in 199322 and by the IDSA in 199823 and 2000.24 All the guidelines focus on broad-spectrum ß-lactam agents. The ATS and 1998 IDSA guidelines make atypical pathogen coverage (ie, macrolides and fluoroquinolones) optional for those patients treated on general medical wards and recommended for all those admitted to ICUs. The 2000 IDSA guidelines recommend atypical organism coverage for all hospitalized CAP patients and offer fluoroquinolone monotherapy as an option for non-ICU patients. The 2000 IDSA guidelines include the caveat that the studies supporting such coverage may reflect temporal or geographic differences. Our findings support not only the empiric inclusion of atypical organism coverage, but also the concern about temporal differences.


   Conclusion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Conclusion
References
 
CAP is a common condition that results in great suffering and mortality among Medicare beneficiaries. The results of this study suggest that the empiric addition of macrolide therapy to a ß-lactam agent for inpatients offers the potential for significantly improved survival. However, the final answer might not be a universal "macrolide, yes or no," but could vary both temporally and geographically. Use of rapid urine antigen tests for Legionella pneumophila can help to guide treatment and to accumulate important surveillance data. The additional assessment of year-to-year and geographic variations in the impact of therapy with macrolides and fluoroquinolones is needed. A definitive randomized trial that includes prospective testing for atypical pathogens would be ideal but would need to be large enough to take into account the findings of this study and previous studies. However, in the absence of rapid diagnostic tests and surveillance data on atypical pathogen infections to guide empiric therapy, the inclusion of atypical organism coverage in initial empiric treatment would seem warranted.


   Acknowledgements
 
We thank the staff of FMAS Corporation and the following Medicare peer review organizations: California Medical Review, Inc; Colorado Foundation for Medical Care; Hawaii Medical Service Association; Health Services Advisory Group (Arizona); HealthInsight-Nevada; HealthInsight-Utah; Montana-Wyoming Foundation for Medical Care; New Mexico Medical Review Association; and Oregon Medical Professional Review Organization. We dedicate this report to the memory of our colleague, Dr. Joseph Lowery.


   Footnotes
 
Abbreviations: AOR = adjusted odds ratio; ATS = American Thoracic Society; CAP = community-acquired pneumonia; CI = confidence interval; ICD-9-CM = International Classification of Diseases, ninth revision, Clinical Manual; IDSA = Infectious Diseases Society of America

The opinions expressed are those of the authors and do not necessarily reflect the policy of the US Department of Health and Human Services and the Health Care Financing Administration. The authors have no financial involvement in and received no support from any organization with a direct commercial financial interest in the subject of this manuscript. This work was funded entirely by the Health Care Financing Administration.

Received for publication June 16, 2000. Accepted for publication November 21, 2000.


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 Materials and Methods
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 Discussion
 Conclusion
 References
 

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T. M. File Jr, J. Garau, F. Blasi, C. Chidiac, K. Klugman, H. Lode, J. R. Lonks, L. Mandell, J. Ramirez, and V. Yu
Guidelines for Empiric Antimicrobial Prescribing in Community-Acquired Pneumonia
Chest, May 1, 2004; 125(5): 1888 - 1901.
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J. J. Oosterheert, M. J. M. Bonten, E. Buskens, M. M. E. Schneider, and I. M. Hoepelman
Algorithm To Determine Cost Savings of Targeting Antimicrobial Therapy Based on Results of Rapid Diagnostic Testing
J. Clin. Microbiol., October 1, 2003; 41(10): 4708 - 4713.
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 J Antimicrob ChemotherHome page
J. J. Oosterheert, M. J. M. Bonten, E. Hak, M. M. E. Schneider, and I. M. Hoepelman
How good is the evidence for the recommended empirical antimicrobial treatment of patients hospitalized because of community-acquired pneumonia? A systematic review
J. Antimicrob. Chemother., October 1, 2003; 52(4): 555 - 563.
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O. Leroy, T. d'Escrivan, H. Georges, and S. Alfandari
Impact of Positive Microbiological Diagnosis on Management and Prognosis of Severe Community-Acquired Pneumonia
Chest, September 1, 2003; 124(3): 1179 - 1180.
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E. A. Halm and A. S. Teirstein
Management of Community-Acquired Pneumonia
N. Engl. J. Med., December 19, 2002; 347(25): 2039 - 2045.
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 Eur Respir JHome page
A. Ortqvist
Treatment of community-acquired lower respiratory tract infections in adults
Eur. Respir. J., July 1, 2002; 20(36_suppl): 40S - 53s.
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 Arch Intern MedHome page
P. M. Houck, D. W. Bratzler, M. Niederman, and J. G. Bartlett
Pneumonia Treatment Process and Quality
Arch Intern Med, April 8, 2002; 162(7): 843 - 844.
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