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Epidemiology and Outcomes of Health-care–Associated Pneumonia^*

Results From a Large US Database of Culture-Positive Pneumonia

^* From the Pulmonary and Critical Care Division (Dr. Kollef), Washington University School of Medicine, St. Louis, MO; Pulmonary and Critical Care Medicine Service (Dr. Shorr), Walter Reed Army Medical Center, Washington, DC; Cardinal Health Clinical Knowledge Services Research Group (Drs. Tabak, Gupta, and Johannes), Marlborough, MA; and Pfizer Inc. (Dr. Liu), New York, NY.

Correspondence to: Marin H. Kollef, MD, FCCP, Campus Box 8052, Washington University School of Medicine, 660 South Euclid Ave, St. Louis, MO 63110; e-mail: mkollef{at}im.wustl.edu

	Abstract

TOP Abstract Introduction Materials and Methods Results Comment References

 
Context: Traditionally, pneumonia developing in patients outside the hospital is categorized as community acquired, even if these patients have been receiving health care in an outpatient facility. Accumulating evidence suggests that health-care–associated infections are distinct from those that are truly community acquired.

Objective: To characterize the microbiology and outcomes among patients with culture-positive community-acquired pneumonia (CAP), health-care–associated pneumonia (HCAP), hospital-acquired pneumonia (HAP), and ventilator-associated pneumonia (VAP).

Design and setting: A retrospective cohort study based on a large US inpatient database.

Patients: A total of 4,543 patients with culture-positive pneumonia admitted into 59 US hospitals between January 1, 2002, and December 31, 2003, and recorded in a large, multi-institutional database of US acute-care hospitals (Cardinal Health-Atlas Research Database; Cardinal Health Clinical Knowledge Services; Marlborough, MA).

Main measures: Culture data (respiratory and blood), in-hospital mortality, length of hospital stay (LOS), and billed hospital charges.

Results: Approximately one half of hospitalized patients with pneumonia had CAP, and > 20% had HCAP. Staphylococcus aureus was a major pathogen in all pneumonia types, with its occurrence markedly higher in the non-CAP groups than in the CAP group. Mortality rates associated with HCAP (19.8%) and HAP (18.8%) were comparable (p > 0.05), and both were significantly higher than that for CAP (10%, all p < 0.0001) and lower than that for VAP (29.3%, all p < 0.0001). Mean LOS varied significantly with pneumonia category (in order of ascending values: CAP, HCAP, HAP, and VAP; all p < 0.0001). Similarly, mean hospital charge varied significantly with pneumonia category (in order of ascending value: CAP, HCAP, HAP, and VAP; all p < 0.0001).

Conclusions: The present analysis justified HCAP as a new category of pneumonia. S aureus was a major pathogen of all pneumonias with higher rates in non-CAP pneumonias. Compared with CAP, non-CAP was associated with more severe disease, higher mortality rate, greater LOS, and increased cost.

Key Words: community acquired • epidemiology • health care • mechanical ventilation • mortality • nosocomial • outcomes • pneumonia • resource use

	Introduction

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Pneumonia is often classified as either community acquired or nosocomial, depending on whether the infection developed while the patient was in an outpatient setting or in an inpatient setting.¹ Nosocomial pneumonia (NP) is further differentiated into ventilator-associated pneumonia (VAP) if the process arose after the patient had been receiving at least 24 h of mechanical ventilation.²³ This classification scheme reflects differences in the pathogens responsible for these infections and forms the basis for treatment decisions and antibiotic selections. For example, Streptococcus pneumoniae is a common cause of community-acquired pneumonia (CAP)⁴⁵ but is infrequently implicated in VAP.³⁶ Similarly, many empiric regimens for VAP include antimicrobials active against Pseudomonas aeruginosa, as this is regularly recovered from patients with VAP⁷ but is rarely seen in outpatients with CAP.

Despite the popularity of this dichotomous classification scheme for pneumonia, recent evidence⁸⁹¹⁰ indicates that this system may have significant limitations. Specifically, health care now reflects a continuum of care with many traditional inpatient services provided in outpatient settings. Invasive medical therapies are now routinely administered in nursing homes and rehabilitation hospitals, and many surgeries are performed in outpatient-based surgical centers. Additionally, some patients regularly utilize significant medical resources and transition from the hospital to a subacute care facility but are then soon thereafter return to the hospital, never truly residing in the "community." In each of these instances and despite the close link to traditional inpatient care, physicians often categorize new infections in such subjects as "community acquired."¹¹ Data indicate, however, that these health-care–associated infections have a unique epidemiology and that the pathogens causing and the outcomes related to these infections more closely resemble those seen with nosocomial processes.^8111213 Some experts⁸¹¹¹⁴ advocate creating a new class of "health-care–associated" infection. Clarifying the epidemiology of these health-care–associated infections generally, and of health-care–associated pneumonia (HCAP) specifically, is crucial to efforts to design appropriate empiric antimicrobial treatment guidelines.

Accumulating evidence pointing to the potentially significant impact of HCAP results in the very recent recognition of HCAP by the American Thoracic Society and the Infectious Diseases Society of America.¹⁵¹⁶ However, to date, no multi-institutional data exist describing the epidemiology and microbiology of HCAP. Additionally, prior work on this topic has been limited to observations coming from mainly large, academic teaching hospitals. Therefore, to better characterize HCAP and to compare it with CAP, hospital-acquired pneumonia (HAP), and VAP, we retrospectively analyzed the records of patients with culture-positive pneumonia registered in a large US database between January 1, 2002, and December 31, 2003. We hypothesized that HCAP would represent a distinct clinical entity, with the pathogens recovered more closely resembling those seen in HAP and VAP. We also sought to determine if HCAP was clinically distinct from these other types of pneumonia and to assess the economic impact of HCAP.

	Materials and Methods

TOP Abstract Introduction Materials and Methods Results Comment References

 
Study Design
A retrospective cohort analysis was performed to characterize the epidemiology, microbiology, and clinical/economic outcomes of patients with culture-positive CAP, HCAP, HAP, and VAP in the first 5 days of hospital admission. Data were obtained for all patients with pneumonia admitted to 59 US hospitals between January 1, 2002, and December 31, 2003.

Data Source
Data for the present analysis were obtained from a large, multi-institutional database of US acute-care hospitals, the Atlas database (Cardinal Health-Atlas Research Database; Cardinal Health Clinical Knowledge Services; formerly MedisGroup; Marlborough, MA).² Details of this database were published previously.^2171819 Briefly, Cardinal Health Clinical Knowledge Services develops the Atlas software and distributes it to acute-care hospitals in the United States for the collection and analysis of detailed clinical and administrative data. As the largest database of its kind, the Atlas database collects information on approximately 950,000 inpatient admissions to > 200 US acute-care hospitals annually. Hospitals included in the database are similar in bed size to American Hospital Association-member hospitals.

The Atlas database registers patient demographics, admission source, type of ICU, all documented procedure and diagnosis codes (International Classification of Diseases, Ninth Revision, Clinical Modification [ICD-9-CM]), admission and discharge dates for each stay in the ICU, total length of hospital stay (LOS) in hospital, billed total and ancillary hospital charges, discharge disposition, specific interventions received, and information on > 400 key clinical findings,²²⁰ including clinical history and pathophysiologic findings, such as vital signs, laboratory test results, culture findings, and physician assessments. During the study period from January 1, 2002, to December 31, 2003, a total of 162 hospitals in the Atlas database met the data quality criteria for inclusion, of which 59 hospitals (16 teaching hospitals and 43 nonteaching hospitals) collected clinical and culture data for the first 5 days of patient hospitalization and were included for the present study.

Sample Populations
Pneumonia was defined by the presence of either primary or secondary ICD-9-CM codes indicative of pneumonia and a concomitant positive respiratory bacterial culture. The study samples were then constructed stepwise according to definitions for different pneumonia types defined in Table 1 . First, patients who were receiving mechanical ventilation for at least 24 h with a first positive bacterial respiratory culture result after ventilator start time were classified into the VAP group. Second, patients with a first positive bacterial respiratory culture result > 2 days from hospital admission who did not meet VAP definition were classified into the HAP group. Third, patients with a first positive bacterial respiratory culture result within 2 days of hospital admission and who were transferred from another health-care facility, had been receiving long-term hemodialysis, or had prior hospitalization within 30 days were classified into the HCAP group, which served as the control group. All remaining patients constituted the CAP group.

	Results

TOP Abstract Introduction Materials and Methods Results Comment References

 
Patient Characteristics
A total of 4,543 patients met the inclusion criteria and were analyzed in the present study. Among these patients, there were 2,221 patients with CAP (48.9%), 988 patients with HCAP (21.7%), 835 patients with HAP (18.4%), and 499 patients with VAP (11%) [Table 2 ]. Gender differences were statistically nonsignificant among the four pneumonia types. HCAP patients (78.1%) were more likely to be white than were patients with VAP (71.7%). A significantly lower proportion of patients with HCAP were black (4.6%) compared with patients with HAP (6.8%) and VAP (12.2%). Patients with HCAP (median age, 77 years) were significantly older than those who had CAP (73 years) or VAP (65 years) but were comparable to those with HAP (76 years). A significantly higher percentage of patients with HCAP (71%) were receiving Medicare than were patients with CAP (62.5%), HAP (62.6%), or VAP (50.3%). Nearly one half of patients with HCAP (49.6%) were admitted from skilled nursing facilities, a rate markedly higher than for patients with CAP (0%), HAP (10.3%), or VAP (9.4%). Fewer patients with HCAP were admitted based on lower to moderate ASG scores of 1 to 2 than were patients with CAP or HAP. In contrast, a higher proportion of patients with HCAP were admitted on high ASG scores of 3 to 4 than were patients with CAP or HAP. A significantly lower proportion of patients with HCAP were admitted on ASG score 4 than were patients with VAP. Other clinical characteristics, including comorbidities and disease group description, were also different among the four pneumonia types (Table 2).

View larger version (21K): [in this window] [in a new window] [Download PPT slide]   Figure 1. Mean mortality rates in patients with CAP, HCAP, HAP, and VAP.

	Comment

TOP Abstract Introduction Materials and Methods Results Comment References

 
To our knowledge, this is the first multi-institutional study defining HCAP as a distinct type of pneumonia. The unique microbiology, epidemiology, and outcomes for patients with CAP, HCAP, HAP, and VAP demonstrated in the present study support a new, refined classification scheme categorizing pneumonias into these four subtypes. Compared with CAP, non-CAP, including HCAP, was associated with more severe disease, higher mortality rate, greater LOS, and increased cost. Our study also suggests that S aureus is a major pathogen with high occurrence among all types of pneumonias.

Pneumonia is one of the leading causes for hospitalization and mortality in the United States.²¹ Effective empiric treatment involves selection of an antibiotic with a spectrum of activity that includes the causative pathogen(s).²¹ In the absence of culture data, empiric antimicrobial treatment should be initiated within 4 h of a pneumonia diagnosis to optimize outcomes.²²²³ Therefore, an evidence-based classification scheme that differentiates different types of pneumonia according to their most likely causative organism(s) will help clinicians maximize the likelihood of achieving a favorable patient outcome.

Due to the different etiologic pathogens underlying CAP and NP, initial empiric therapies differ. Major national^21242526 and international²⁷²⁸ guidelines recommend the combination of a macrolide and doxycycline, ß-lactam, or fluoroquinolone, depending on the severity of illness at initial presentation and the presence of coexisting illness or advanced age, for the initial empiric antimicrobial treatment for CAP. In contrast, advanced-generation cephalosporins, ß-lactam/ß-lactamase inhibitors, fluoroquinolones, clindamycin, certain carbapenems, vancomycin, linezolid, aminoglycosides, and aztreonam, alone or in combination, are recommended for the treatment of NP.²⁹

Health-care services, such as dialysis, chemotherapy, and same-day surgery, are increasingly being provided in the outpatient environment.¹¹ At present, pneumonia related to these health-care–associated interventions may be classified as CAP and is treated as such. However, given the frequent transfer of patients and health-care workers between these facilities and hospitals, an outpatient facility is likely to be distinct from the true community and may more closely resemble the nosocomial setting in terms of the pathogens it might house. For example, MRSA strains isolated from patients with health-care–associated infections are distinct from those that are truly community acquired and have different susceptibility to antibiotics.¹³ In addition to the complexity introduced by evolving health-care practices, the causative pathogens associated with CAP have also changed in prevalence in recent years. Although S pneumoniae remains the most common causative pathogen, other potential pathogens (eg, Chlamydia pneumoniae, Mycoplasma pneumoniae, and Legionella spp) exist, and their prevalence changes over time and varies by geographic location.²¹ Furthermore, the emerging antimicrobial resistance of respiratory pathogens has complicated the management of these infections.³⁰ These changes necessitate an evolving treatment strategy based on the most recent findings regarding microbiology and epidemiology.³¹

The results of this study justify the separation of a new type of pneumonia, HCAP, from the traditionally defined CAP domain. HCAP is distinct from CAP in terms of patient characteristics, pathogen distribution patterns, and outcomes. HCAP is also different from HAP and VAP along the above-mentioned dimensions; however, in general, HCAP differs from HAP or VAP to a lesser degree than from CAP (eg, more comparable S aureus occurrences and mortality rates). Results of this study revealed that one half of hospitalized patients with culture-positive pneumonia had CAP and > 20% had HCAP. Had the patients with HCAP been included in the CAP category according to the traditional classification scheme, they would have accounted for 31% of CAP patients who needed hospitalization. Given that data in this study were derived from a consortium of hospitals typical of acute-care US hospitals, it is reasonable to expect that at the present time, a large proportion of patients hospitalized in acute-care facilities are being treated for CAP but in fact should be treated for HCAP, resulting in potentially poor clinical outcomes.

We also observed that S aureus was a dominant pathogen in all types of pneumonia, including CAP. There is a consensus in the literature⁵²¹ that the most common pathogen for CAP is S pneumoniae. Our results that fewer patients admitted for CAP had S pneumoniae infection than had S aureus infection probably reflected the effects of various forms of bias. Because only approximately one third of CAP patients require hospitalization,³²³³ the CAP group in this analysis was more likely a sample of CAP patients who require hospitalization, rather than a representative sample for all patients with CAP. Additionally, the high prevalence of S aureus in the CAP group might be attributable to the relationship between S aureus and higher severity of illness, a major factor influencing the decision to hospitalize subjects with CAP treatment.²¹ Finally, since information regarding serologic diagnoses was limited and because of our express focus on culture results, we likely underestimated the incidence of certain pathogens, such as Legionella pneumophila.

The occurrence of S aureus in patients with HCAP was markedly higher than that in patients with CAP. Compared with the HAP group, a greater proportion of patients in the HCAP group had Pseudomonas sp and S pneumoniae and a lower proportion had nongroup Streptococcus. Compared with the VAP group, patients with HCAP were more likely to be infected by S pneumoniae and less likely to have Haemophilus sp infection. Thus, HCAP is microbiologically different from CAP, HAP, and VAP.

Multivariate analysis further indicated that S aureus was the only pathogen that correlated with mortality. It was possible that S aureus was the underlying reason for the increased mortality, LOS, and treatment costs observed in patients with HCAP, HAP, and VAP. The clinical outcomes in patients with HCAP and HAP were comparable in terms of raw mortality. However, the mean LOS and treatment costs for patients were significantly lower in these groups of patients than in those with HAP. This might reflect a general undertreatment for HCAP among clinicians who do not distinguish HCAP from CAP at present. Moreover, since treatment guidelines often do not recommend coverage for S aureus in CAP, the association between the presence of S aureus and mortality may reflect that subjects with such infections were more likely to have received antibiotics not effective against MSSA or, in particular, MRSA. In other words, recovery of S aureus may be a surrogate marker for the prescription of inappropriate antimicrobial therapy, a known predictor of poor outcomes in pneumonia.

The major strength of the present study was the use of a large, multicenter database that contained information allowing us to examine clinical and economic variables. The availability of patient-specific outcomes data additionally allowed us to assess the clinical and economic burden associated with each type of pneumonia. Due to the way the patient-specific variables were coded in the database, patients with HCAP could also be identified. Furthermore, the continuous, ongoing data collection characteristic of the database enables us to collect similar data in the future in order to identify temporal trends of the epidemiology of these pneumonias for surveillance purposes.

Our study has several significant limitations. First, only hospitalized patients were included in the Atlas database. Data derived from such a database could have introduced bias for the CAP and HCAP groups in the present analysis, as not all patients with CAP or HCAP are necessarily admitted to an acute-care medical center. Second, we only included subjects with early onset (5 days on hospital admission) pneumonia; this approach may have introduced selection bias in the HAP and VAP groups by excluding late-onset HAP and VAP. Third, our definition of pneumonia based on the presence of ICD-9-CM codes indicative of pneumonia and a concomitant positive respiratory bacterial culture could have introduced misclassification biases. However, since diagnostic testing that involves sputum culture cannot always distinguish between colonization and true infection,²¹ it was impossible to causatively relate the isolated pathogen to pneumonia. Furthermore, our method excluded patients with pneumonia despite false-negative culture findings. Similarly, as noted earlier, the use of serologic studies was not uniformly prescribed. Hence, we likely undercounted events due to atypical organisms. Finally, we could not evaluate the appropriateness of initial empiric antimicrobial therapy. Without the therapy data, we were unable to determine the cost components of therapy and compare the cost-effectiveness of the new classification scheme with the traditional one.

Despite the limitations discussed above, the present analysis supports a new pneumonia classification scheme distinguishing CAP, HCAP, HAP, and VAP. It suggests that HCAP, traditionally classified into the CAP category, is clinically more similar to HAP and should be treated as such until culture data become available. In terms of pathogen distribution pattern, HCAP shares more similarity with HAP and VAP than with CAP. The results from the present analysis imply that the next generation of national treatment guidelines and local critical pathways aimed at optimizing and streamlining initial empiric antibiotic treatment for pneumonia would benefit by differentiating HCAP from CAP.

	Acknowledgements

 
We thank the following Cardinal Health Clinical Knowledge Services Research Group members for their dedicated contributions in database management, analysis, and technical support: Rosemary Kirousis, MPH; Alisa Goetz, PharmD; and Linda Hyde, RHIA.

	Footnotes

 
Abbreviations: ASG = admission severity group; CAP = community-acquired pneumonia; CI = confidence interval; HAP = hospital-acquired pneumonia; HCAP = health-care–associated pneumonia; ICD-9-CM = International Classification of Diseases, Ninth Revision, Clinical Modification; LOS = length of hospital stay; MRSA = methicillin-resistant Staphylococcus aureus; MSSA = methicillin-susceptible Staphylococcus aureus; NP = nosocomial pneumonia; OR = odds ratio; VAP = ventilator-assisted pneumonia

This study was supported by a research grant from Pfizer Inc.

Received for publication April 26, 2005. Accepted for publication May 30, 2005.

	References

TOP Abstract Introduction Materials and Methods Results Comment References

 

1. Garner, JS, Jarvis, WR, Emori, TG, et al (1988) CDC definitions for nosocomial infections, 1988. Am J Infect Control 16,128-140[CrossRef][ISI][Medline]
2. Rello, J, Ollendorf, DA, Oster, G, et al Epidemiology and outcomes of ventilator-associated pneumonia in a large US database. Chest 2002;122,2115-2121[Abstract/Free Full Text]
3. Chastre, J, Fagon, JY Ventilator-associated pneumonia. Am J Respir Crit Care Med 2002;165,867-903[Abstract/Free Full Text]
4. Fine, MJ, Smith, MA, Carson, CA, et al Prognosis and outcomes of patients with community-acquired pneumonia: a meta-analysis. JAMA 1996;275,134-141[Abstract]
5. Wilkinson, M, Woodhead, MA Guidelines for community-acquired pneumonia in the ICU. Curr Opin Crit Care 2004;10,59-64[Medline]
6. Kollef, MH, Rello, J, Cammarata, SK, et al Clinical cure and survival in Gram-positive ventilator-associated pneumonia: retrospective analysis of two double-blind studies comparing linezolid with vancomycin. Intensive Care Med 2004;30,388-394[CrossRef][ISI][Medline]
7. Rello, J, Gallego, M, Mariscal, D, et al The value of routine microbial investigation in ventilator-associated pneumonia. Am J Respir Crit Care Med 1997;156,196-200[Abstract/Free Full Text]
8. Tambyah, PA, Habib, AG, Ng, TM, et al Community-acquired methicillin-resistant Staphylococcus aureus infection in Singapore is usually "healthcare associated." Infect Control Hosp Epidemiol 2003;24,436-438[CrossRef][ISI][Medline]
9. Farr, BM, Jarvis, WR Would active surveillance cultures help control healthcare-related methicillin-resistant Staphylococcus aureus infections? Infect Control Hosp Epidemiol 2002;23,65-68[CrossRef][Medline]
10. Cookson, BD Methicillin-resistant Staphylococcus aureus in the community: new battlefronts, or are the battles lost? Infect Control Hosp Epidemiol 2000;21,398-403[CrossRef][ISI][Medline]
11. Friedman, ND, Kaye, KS, Stout, JE, et al Health care-associated bloodstream infections in adults: a reason to change the accepted definition of community-acquired infections. Ann Intern Med 2002;137,791-797[Abstract/Free Full Text]
12. Tacconelli, E, Venkataraman, L, De Girolami, PC, et al Methicillin-resistant Staphylococcus aureus bacteraemia diagnosed at hospital admission: distinguishing between community-acquired versus healthcare-associated strains. J Antimicrob Chemother 2004;53,474-479[Abstract/Free Full Text]
13. Naimi, TS, LeDell, KH, Como-Sabetti, K, et al Comparison of community- and health care-associated methicillin-resistant Staphylococcus aureus infection. JAMA 2003;290,2976-2984[Abstract/Free Full Text]
14. Morin, CA, Hadler, JL Population-based incidence and characteristics of community-onset Staphylococcus aureus infections with bacteremia in 4 metropolitan Connecticut areas, 1998. J Infect Dis 2001;184,1029-1034[CrossRef][ISI][Medline]
15. Craven, DE, Palladino, R, McQuillen, DP Healthcare-associated pneumonia in adults: management principles to improve outcomes. Infect Dis Clin North Am 2004;18,939-962[Medline]
16. Hospital-Acquired Pneumonia Guideline Committee of the American Thoracic Society & Infectious Diseases Society of America.. Guidelines for the management of adults with hospital-acquired pneumonia, ventilator-associated pneumonia, and healthcare-associated pneumonia. Am J Respir Crit Care Med 2005;171,388-416[Free Full Text]
17. Iezzoni, LI, Ash, AS, Coffman, GA, et al Admission and mid-stay MedisGroups scores as predictors of hospitalization charges. Med Care 1991;29,210-220[Medline]
18. Iezzoni, LI, Moskowitz, MA A clinical assessment of MedisGroups. JAMA 1988;260,3159-3163[Abstract]
19. Silber, JH, Rosenbaum, PR, Schwartz, JS, et al Evaluation of the complication rate as a measure of quality of care in coronary artery bypass graft surgery. JAMA 1995;274,317-323[Abstract]
20. Fine, MJ, Auble, TE, Yealy, DM, et al A prediction rule to identify low-risk patients with community-acquired pneumonia. N Engl J Med 1997;336,243-250[Abstract/Free Full Text]
21. Niederman, MS, Mandell, LA, Anzueto, A, et al Guidelines for the management of adults with community-acquired pneumonia: diagnosis, assessment of severity, antimicrobial therapy, and prevention. Am J Respir Crit Care Med 2001;163,1730-1754[Free Full Text]
22. Ziss, DR, Stowers, A, Feild, C Community-acquired pneumonia: compliance with centers for Medicare and Medicaid services, national guidelines, and factors associated with outcome. South Med J 2003;96,949-959[ISI][Medline]
23. Houck, PM, Bratzler, DW, Nsa, W, et al Timing of antibiotic administration and outcomes for Medicare patients hospitalized with community-acquired pneumonia. Arch Intern Med 2004;164,637-644[Abstract/Free Full Text]
24. Bartlett, JG, Breiman, RF, Mandell, LA, et al Community-acquired pneumonia in adults: guidelines for management. The Infectious Diseases Society of America. Clin Infect Dis 1998;26,811-838[ISI][Medline]
25. Bartlett, JG, Dowell, SF, Mandell, LA, et al Practice guidelines for the management of community-acquired pneumonia in adults. Infectious Diseases Society of America. Clin Infect Dis 2000;31,347-382[CrossRef][Medline]
26. Mandell, LA, Bartlett, JG, Dowell, SF, et al Update of practice guidelines for the management of community-acquired pneumonia in immunocompetent adults. Clin Infect Dis 2003;37,1405-1433[CrossRef][ISI][Medline]
27. British Thoracic Society Standards of Care Committee.. BTS guidelines for the management of community acquired pneumonia in adults. Thorax 2001;56(suppl 4),iv1-iv64
28. Mandell, LA, Marrie, TJ, Grossman, RF, et al Canadian guidelines for the initial management of community-acquired pneumonia: an evidence-based update by the Canadian Infectious Diseases Society and the Canadian Thoracic Society. The Canadian Community-Acquired Pneumonia Working Group. Clin Infect Dis 2000;31,383-421[CrossRef][Medline]
29. American Thoracic Society.. Hospital-acquired pneumonia in adults: diagnosis, assessment of severity, initial antimicrobial therapy, and preventive strategies; a consensus statement, American Thoracic Society, November 1995. Am J Respir Crit Care Med 1996;153,1711-1725[ISI][Medline]
30. File, TM The epidemiology of respiratory tract infections. Semin Respir Infect 2000;15,184-194[Medline]
31. Niederman, MS Review of treatment guidelines for community-acquired pneumonia. Am J Med 2004;117(suppl 3A),51S-57S
32. Marrie, TJ Community-acquired pneumonia. Clin Infect Dis 1994;18,501-513[ISI][Medline]
33. Guest, JF, Morris, A Community-acquired pneumonia: the annual cost to the National Health Service in the UK. Eur Respir J 1997;10,1530-1534[Abstract]

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This Article Abstract Full Text (PDF) Free Erratum (v129,p831) 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 (57) Citing Articles via Google Scholar Google Scholar Articles by Kollef, M. H. Articles by Johannes, R. S. Search for Related Content PubMed PubMed Citation Articles by Kollef, M. H. Articles by Johannes, R. S.