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Causes of Death for Patients With Community-Acquired Pneumonia
Results From the Pneumonia Patient Outcomes Research Team Cohort Study
Eric M. Mortensen, MD, MSc;
Christopher M. Coley, MD;
Daniel E. Singer, MD;
Thomas J. Marrie, MD;
D. Scott Obrosky, MSc;
Wishwa N. Kapoor, MD, MPH;
Michael J. Fine, MD, MSc
Arch Intern Med. 2002;162:1059-1064.
ABSTRACT
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Background To our knowledge, no previous study has systematically examined pneumonia-related
and pneumonia-unrelated mortality. This study was performed to identify the
cause(s) of death and to compare the timing and risk factors associated with
pneumonia-related and pneumonia-unrelated mortality.
Methods For all deaths within 90 days of presentation, a synopsis of all events
preceding death was independently reviewed by 2 members of a 5-member review
panel (C.M.C., D.E.S., T.J.M., W.N.K., and M.J.F.). The underlying and immediate
causes of death and whether pneumonia had a major, a minor, or no apparent
role in the death were determined using consensus. Death was defined as pneumonia
related if pneumonia was the underlying or immediate cause of death or played
a major role in the cause of death. Competing-risk Cox proportional hazards
regression models were used to identify baseline characteristics associated
with mortality.
Results Patients (944 outpatients and 1343 inpatients) with clinical and radiographic
evidence of pneumonia were enrolled, and 208 (9%) died by 90 days. The most
frequent immediate causes of death were respiratory failure (38%), cardiac
conditions (13%), and infectious conditions (11%); the most frequent underlying
causes of death were neurological conditions (29%), malignancies (24%), and
cardiac conditions (14%). Mortality was pneumonia related in 110 (53%) of
the 208 deaths. Pneumonia-related deaths were 7.7 times more likely to occur
within 30 days of presentation compared with pneumonia-unrelated deaths. Factors
independently associated with pneumonia-related mortality were hypothermia,
altered mental status, elevated serum urea nitrogen level, chronic liver disease,
leukopenia, and hypoxemia. Factors independently associated with pneumonia-unrelated
mortality were dementia, immunosuppression, active cancer, systolic hypotension,
male sex, and multilobar pulmonary infiltrates. Increasing age and evidence
of aspiration were independent predictors of both types of mortality.
Conclusions For patients with community-acquired pneumonia, only half of all deaths
are attributable to their acute illness. Differences in the timing of death
and risk factors for mortality suggest that future studies of community-acquired
pneumonia should differentiate all-cause and pneumonia-related mortality.
INTRODUCTION
PNEUMONIA COMBINED with influenza is the sixth leading cause of death
in the United States.1 Although the mortality
rate from pneumonia decreased sharply with the introduction of antibiotic
therapy in the 1940s, since 1950, the overall mortality rate for this illness
has either remained stable or increased.2 In
a meta-analysis3 of studies of prognosis, the
short-term mortality of patients hospitalized with community-acquired pneumonia
ranged from 5.1% for patients treated in an ambulatory or hospital setting
to 36.5% for patients treated in an intensive care unit.
Prior studies4-6
of pneumonia prognosis focused almost exclusively on short-term mortality
and assessed risk factors for all-cause mortality. To our knowledge, no previous
studies have examined the causes of death of patients with community-acquired
pneumonia or the role that pneumonia played in the cause of death. The goals
of this study were as follows: (1) to identify the underlying and immediate
causes of death for patients with community-acquired pneumonia, (2) to determine
the role that community-acquired pneumonia played in the cause of death, and
(3) to compare the risk factors associated with pneumonia-related and pneumonia-unrelated
mortality in patients with this illness.
PATIENTS AND METHODS
PATIENT RECRUITMENT
The Pneumonia Patient Outcomes Research Team cohort study was conducted
at 5 medical institutions in 3 geographic locations between October 12, 1991,
and March 31, 1994. These were the University of Pittsburgh Medical Center,
a 942-bed university teaching hospital, and St Francis Medical Center, a 427-bed
community teaching hospital, in Pittsburgh, Pa; Massachusetts General Hospital,
an 899-bed university teaching hospital, and Harvard Community Health Plan–Kenmore
Center, a staff-model health maintenance organization, in Boston, Mass; and
Victoria General Hospital, a 637-bed university teaching hospital, in Halifax,
Nova Scotia. Outpatients (defined as those initially treated in an outpatient
setting) and inpatients were enrolled from each of the 4 hospital-based sites
(University of Pittsburgh Medical Center, St Francis Medical Center, Massachusetts
General Hospital, and Victoria General Hospital); only outpatients were enrolled
from the Harvard Community Health Plan–Kenmore Center.
Potential study subjects were identified by research assistants through
daily reviews of admitting and radiology department logs and records of patients
presenting to the emergency departments and clinics affiliated with the participating
sites. Inclusion criteria were as follows: 18 years of age or older, 1 or
more symptoms suggestive of community-acquired pneumonia, radiographic evidence
of community-acquired pneumonia not known to be chronic, and informed consent
for baseline and follow-up interviews. Exclusion criteria were as follows:
discharge from an acute-care facility within 10 days of presentation, known
seropositivity for the human immunodeficiency virus, or pulmonary symptoms
secondary to another diagnosis (eg, lung cancer). Patients were only enrolled
once during the study; those who presented with community-acquired pneumonia
on more than 1 occasion were not subsequently enrolled.
BASELINE ASSESSMENT
For all study patients, baseline sociodemographic information and clinical
data were assessed at presentation by direct interview by a study nurse and
medical record review. If unable to obtain information directly from the patient
because of mental status changes or language or communication barriers, a
proxy respondent was used. Clinical data examined included medical history,
physical examination results, laboratory values, chest radiographic findings,
and microbiologic results. Historical information obtained included 5 common
respiratory symptoms (cough, dyspnea, sputum production, pleuritic chest pain,
and hemoptysis) and 14 common nonrespiratory symptoms (fatigue, fever, anorexia,
chills, sweats, headache, myalgias, nausea, sore throat, confusion, inability
to eat, vomiting, diarrhea, and abdominal pain). Physical examination data
collected included vital signs and an evaluation of mental status. Laboratory
data collected, when available, included white blood cell count; hematocrit;
levels of serum urea nitrogen, serum sodium, liver enzymes, and arterial blood
gases; and pulse oximetry readings. Radiographic data included location of
the infiltrate, pattern of the infiltrate (predominantly alveolar, predominantly
interstitial, miliary, or mixed alveolar and interstitial), and presence of
pleural effusion.
When ordered by the physicians caring for these patients, the following
microbiologic tests were abstracted: sputum gram stains and bacterial cultures
obtained within 2 days of presentation, blood cultures drawn before initiating
antimicrobial therapy, pleural fluid cultures, and short-term ( 1 week
of presentation) and convalescent (1-8 weeks after presentation) serologic
tests. Results of these tests were reviewed and a microbiologic cause was
assigned, as previously described.7
Copies of the initial chest radiographs used for the diagnosis of pneumonia
at each study site were independently reviewed by a 3-member panel of attending
radiologists who had no patient-specific clinical information. Pleural effusion
was quantified by the maximum present in either lung as follows: none, minimal
(costophrenic angle blunting only), moderate (less than one third of the pleural
space), and large (one third or more of the pleural space).8
Aspiration pneumonia was diagnosed by the clinical committee based on radiographic
data and synopses of clinical data. Aspiration pneumonia was diagnosed in
patients with a disorder known to alter consciousness, the normal gag reflex,
or the swallowing mechanism in whom the chest radiograph revealed an infiltrate
involving the superior or basilar segments of the lower lobes or the posterior
segments of the upper lobes.9
The severity of illness at presentation was quantified using the validated
Pneumonia Patient Outcomes Research Team prediction rule for 30-day mortality
and medical complications in patients with community-acquired pneumonia.10 This rule is based on 3 demographic characteristics,
5 comorbid illnesses, 5 physical examination findings, and 7 laboratory and
radiographic findings available at presentation. This rule classifies patients
into 5 risk classes, with the 30-day mortality ranging from 0.1% for those
in class I to 31.1% for those in class V.
ASSESSMENT OF MORTALITY AND THE CAUSE OF DEATH
Mortality was assessed at 90 days after initial enrollment in the study.
For all patients who died during the follow-up period, death summaries were
prepared by study research nurses using salient information obtained from
the medical record, family or caregiver interviews, and autopsy reports (when
available).
Each death summary was independently reviewed by 2 study investigators
who were part of a 5-member clinical review panel (C.M.C., D.E.S., T.J.M.,
W.N.K., and M.J.F.). Four members of the clinical review panel were general
internists (C.M.C., D.E.S., W.N.K., and M.J.F.) and 1 was an infectious disease
specialist (T.J.M.); all reviewers had extensive clinical and research experience
regarding patients with community-acquired pneumonia. The reviewers were asked
to assign the underlying and immediate causes of death based on World Health
Organization criteria,11 and to assess the
role that community-acquired pneumonia played in the patient's death. The
underlying cause of death was defined as the disease or injury that initiated
the cascade of morbid events leading directly to death. The immediate cause
of death was defined as the disease process, injury, or complication immediately
preceding death. If community-acquired pneumonia was not considered to be
the underlying or immediate cause of death, then each reviewer was asked to
determine whether community-acquired pneumonia played a major or a minor role
in the patient's death. Pneumonia was judged as playing a major role if death
would not have occurred if the patient did not have pneumonia but another
condition was present that also contributed. Pneumonia was defined as playing
a minor role if community-acquired pneumonia was not essential to explain
the patient's death but played some role in the patient's death.
After the causes of death and the role of pneumonia in causing death
were independently assigned by 2 reviewers, each case was presented to the
5-member clinical review panel. Final assignments of the underlying and immediate
cause of death and the role of pneumonia in causing death were based on the
full consensus of this panel.
Mortality was classified as pneumonia related if pneumonia was an immediate
or underlying cause of death or if it played a major role in the patient's
death. Mortality was defined as pneumonia unrelated if pneumonia was neither
an immediate nor an underlying cause of death, and played only a minor role,
no role, or an unknown role in the cause of death.
STATISTICAL ANALYSES
Univariate statistics were used to compare differences in sociodemographic
and clinical characteristics in patients with pneumonia-related and pneumonia-unrelated
mortality. Causes of death as a function of pneumonia severity risk class
and timing of death were analyzed using simple descriptive techniques. Categorical
variables were analyzed using the  2 test, and continuous variables
were analyzed using the t test. To analyze time to
death for patients with pneumonia-related and pneumonia-unrelated mortality,
Kaplan-Meier estimated probabilities were computed. Statistical significance
was assessed using the summary log-rank test. Statistical significance was
defined as P.05 (2-tailed) for all univariate
and multivariate analyses.
To evaluate risk factors for pneumonia-related, pneumonia-unrelated,
and all-cause mortality, baseline patient sociodemographic and clinical characteristics
were used as independent variables in 3 Cox proportional hazards regression
models, using the 3 mortality outcomes as the respective dependent measures.
The baseline variables included all factors composing the Pneumonia Patient
Outcomes Research Team severity model, in addition to others that were postulated
to have an association with 90-day mortality.10
Site of care, severity risk class, intensive care unit status, do not resuscitate
status, and symptoms were omitted as potential predictors. All baseline variables
that were statistically significant in any of the 3 Cox proportional hazards
regression models were then used in a competing-risk Cox proportional hazards
regression model with pneumonia-related mortality, pneumonia-unrelated mortality,
and survival as the respective dependent measures.12
The Kolmogorov-Smirnov test was used to test the statistical significance
of the survival curves for pneumonia-related and pneumonia-unrelated mortality
in the competing-risk analysis.13
RESULTS
Of the 2287 patients enrolled in the Pneumonia Patient Outcomes Research
Team cohort study, 208 (9%) died within 90 days. Overall, 194 (14%) of the
1343 inpatients and 14 (1%) of the 944 outpatients died within this follow-up
period.
CAUSES OF DEATH
As shown in Table 1, respiratory
failure (38%), sepsis or bacteremia (7%), and cardiac arrhythmia (7%) were
the 3 most frequent immediate causes of death. Neurological conditions (29%),
lung cancer (13%), and cardiac ischemia (13%) were the 3 most frequent underlying
causes of death.
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Table 1. Immediate and Underlying Causes of Death for 208 Patients
With Community-Acquired Pneumonia*
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Death was defined as pneumonia related in 110 (53%) of the 208 deaths.
Of the pneumonia-related deaths, pneumonia was the underlying cause of death
in 20 patients, the immediate cause of death in 9, and a major contributor
to death in 81. Of the pneumonia-unrelated deaths, pneumonia played a minor
role in 34 patients, no role in 52, and an unknown role in 12.
There were distinct differences between the immediate and underlying
causes of death for pneumonia-related and pneumonia-unrelated mortality. The
most frequent immediate causes of death for pneumonia-related mortality were
respiratory failure (50%), pneumonia (8%), multisystem organ failure (6%),
and sepsis (6%). In comparison, respiratory failure (26%), sepsis or bacteremia
(9%), cardiac arrhythmia (8%), and congestive heart failure (7%) were the
leading immediate causes of death for pneumonia-unrelated mortality. The most
frequent underlying causes of death for pneumonia-related mortality were neurological
conditions (22%), pneumonia (18%), and cerebrovascular accident (13%), compared
with lung cancer (19%), other malignancies (17%), and cardiac ischemia (17%)
for those with pneumonia-unrelated mortality.
FACTORS ASSOCIATED WITH MORTALITY
The demographic and clinical factors with significant univariate associations
with all-cause 90-day mortality are shown in Table 2. Overall, 85% of all deaths occurred among patients in the
2 highest risk classes; a greater proportion of pneumonia-related deaths also
occurred within risk classes IV and V.
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Table 2. Factors Associated With All-Cause Mortality*
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Survival plots and frequency distributions of death over time of pneumonia-related
and pneumonia-unrelated mortality are shown in Figure 1 and Figure 2.
For the 110 pneumonia-related deaths, 45% occurred within 2 weeks and 76%
occurred within 30 days of presentation, compared with 8% and 30%, respectively,
of the pneumonia-unrelated deaths (P<.001 for
both comparisons). The odds of a pneumonia-related death occurring within
30 days of presentation was 7.7 that of a pneumonia-unrelated death. The Kolmogorov-Smirnov
test confirmed significantly different patterns in the time to death for those
with pneumonia-related and pneumonia-unrelated mortality (P.001).
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Figure 1. Frequency plot of pneumonia-related
and pneumonia-unrelated mortality. Of the pneumonia-related deaths, 78% occurred
within 30 days; of the pneumonia-unrelated deaths, 68% occurred after 30 days.
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Figure 2. Survival plot of pneumonia-related
and pneumonia-unrelated deaths.
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As shown in Table 3, 6 factors
were independently associated with pneumonia-related mortality only: hypothermia,
altered mental status, elevated serum urea nitrogen level, chronic liver disease,
white blood cell count less than 4000/µL, and hypoxemia. In addition,
6 factors were associated with pneumonia-unrelated mortality only: dementia,
immunosuppression, active cancer, systolic hypotension, male sex, and multilobar
infiltrates. Two variables, increasing age and evidence of aspiration, were
independently associated with pneumonia-related and pneumonia-unrelated mortality.
The magnitude of association for the factors independently associated with
pneumonia-related mortality only ranged from a hazard ratio of 1.90 for temperature
lower than 36.0°C to 3.88 for chronic liver disease. The magnitude of
association for the factors independently associated with pneumonia-unrelated
mortality only ranged from 1.59 for male sex to 2.82 for dementia.
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Table 3. Factors Independently Associated With Pneumonia-Related or
Pneumonia-Unrelated Mortality
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COMMENT
This detailed study of mortality in patients with community-acquired
pneumonia demonstrates substantial differences in the causes, timing, and
risk factors for pneumonia-related and pneumonia-unrelated deaths. The causes
of death for patients in this study were similar to the most common causes
of death for adults in the United States: coronary artery disease, malignancies,
stroke, and chronic obstructive pulmonary disease.14
The most frequent immediate causes of death in this study were respiratory
failure and cardiac disease, while malignancies and neurological disorders
were the most frequent underlying causes of death. However, several causes
of death that many would associate with community-acquired pneumonia, including
sepsis, bacteremia, and multisystem organ failure, were infrequent causes
of death in this cohort. In addition, when the cause of death was stratified
by the role of pneumonia, there were distinct differences between the 2 types
of mortality. For patients with pneumonia-related mortality, the most frequent
causes of death were respiratory failure and neurological disease, while for
patients with pneumonia-unrelated mortality, the most frequent causes of death
were malignancy and cardiac disease.
In this study, slightly more than half of the deaths were classified
as pneumonia related, and more than 75% of the pneumonia-related deaths occurred
within the first 30 days after presentation. After 30 days, the number of
pneumonia-related deaths diminished rapidly, with less than 15% of all pneumonia-related
deaths occurring after 45 days. In contrast, most pneumonia-unrelated deaths
occurred between 30 and 90 days after presentation, with only 10% occurring
within the first 2 weeks of presentation. These findings suggest that community-acquired
pneumonia has a stronger association with mortality within 45 days of presentation
and that prognosis beyond this point is more heavily influenced by the patient's
age, sex, and other significant comorbid conditions.
We also found that the independent predictors of pneumonia-related and
pneumonia-unrelated mortality were quite different. For pneumonia-unrelated
mortality, comorbid conditions such as malignancy, immunosuppression, and
dementia were independently associated with mortality. In contrast, chronic
liver disease, a relatively rare condition, was the only comorbid condition
independently associated with pneumonia-related mortality. In addition, for
pneumonia-related mortality, acute physiologic or laboratory derangements,
such as hypothermia, decreased white blood cell count, elevated serum urea
nitrogen level, and hypoxemia, were independent predictors of mortality. For
pneumonia-unrelated mortality, systolic hypotension was the only acute physiologic
derangement associated with mortality. Increasing age and evidence of aspiration
were the only risk factors associated with pneumonia-related and pneumonia-unrelated
mortality. Increasing age is a significant risk factor for mortality, after
community-acquired pneumonia, according to previous studies3, 15
of pneumonia prognosis. Aspiration events are related to multiple contributing
factors that could affect prognosis, including neurological problems, malnutrition,
and altered mental status.16-18
There are several limitations of this work that should be acknowledged.
First, approximately 130 patients who met study eligibility were not enrolled
because of death before study enrollment. Therefore, this study may not reflect
the full spectrum of patients who died within 90 days of community-acquired
pneumonia. Second, the validity of using a clinical review committee to determine
the cause of death for patients with community-acquired pneumonia has not
been previously established. Although determining the cause of death by autopsy
results represents the reference standard, autopsies were performed on only
22 of the patients who died, which limited our ability to assess the accuracy
of the assignments of cause of death by the clinical committee. Nevertheless,
this method was chosen because it was the most practical in nature and likely
to provide more reliable data than death certificate reports. Similar clinical
consensus methods have been used to classify mortality for many other conditions,
such as cancer- and cardiac-related mortality.19
Third, the accuracy of the case summaries was not independently confirmed
by the physician investigations, which may have affected the assignments of
the cause of death. Fourth, many outpatients had missing data for physical
signs and laboratory values, which may have affected our analyses to determine
factors associated with pneumonia-related and pneumonia-unrelated mortality.
However, our assumption that missing values were normal has been used in our
prior validated models of pneumonia severity. Finally, the moderate number
of deaths in this study may have limited the ability to detect clinical predictors
of mortality and our ability to distinguish differences in the magnitude of
effect for pneumonia-related and pneumonia-unrelated mortality.
In conclusion, this study demonstrates that there are significant differences
between pneumonia-related and pneumonia-unrelated mortality, including the
underlying and immediate causes of death, the timing of death, and the clinical
predictors of death. These findings suggest that researchers, and those interested
in evaluating the quality of pneumonia care, should use a strategy to differentiate
between pneumonia-related and pneumonia-unrelated mortality. Possible strategies
include using a shorter follow-up (30 days) or using a clinical review
committee to assign the role of community-acquired pneumonia in the processes
leading to death.
AUTHOR INFORMATION
Accepted for publication October 2, 2001.
This study was supported by grant R01 HS06468 from the Agency for Healthcare
Research and Quality, Rockville, Md; and grant F32 HS00135 from the Agency
for Healthcare Research and Quality National Research Service Award (Dr Mortensen).
We thank Karen Lahive, MD, for coordinating study activities at the
Harvard Community Health Plan–Kenmore Center; Terry Sefcik, MS, for
data management; and the following clinical research assistants for cohort
study patient enrollment and data collection: Mary Walsh, RN, Donna Polenik,
RN, MPH, and Kathryn Fine, RN, in Pittsburgh; Mary Ungaro, RN, Leila Haddad,
AB, and Marian Hendershot, RN, in Boston; and Rhonda Grandy, RN, Jackie Cunning,
RN, Dawn Menon, GN, Linda Kraft, RN, and Maxine Young, RN, in Halifax.
Corresponding author and reprints: Michael J. Fine, MD, MSc, Center
for the Study of Health Disparities, VA Pittsburgh Healthcare Systems (Mail
Stop 130-U), University Drive C, Location 11E127, Pittsburgh, PA 15240-1001
(e-mail: finemj{at}msx.upmc.edu).
From the Division of General Internal Medicine, Department of Medicine,
and the Center for Research on Health Care, University of Pittsburgh (Drs
Mortensen, Kapoor, and Fine and Mr Obrosky), and the Center for the Study
of Health Disparities, VA Pittsburgh Healthcare System (Dr Fine), Pittsburgh,
Pa; the General Medicine Unit, Department of Medicine, Massachusetts General
Hospital and Harvard Medical School, Boston (Drs Coley and Singer); and the
Division of Infectious Disease, Department of Medicine, University of Alberta,
Edmonton (Dr Marrie).
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Eur Respir J 2007;29:969-975.
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Statins and outcomes in patients with pneumonia: Not only healthy user bias
Mortensen et al.
BMJ 2006;333:1123-1124.
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Statin treatment and reduced risk of pneumonia in patients with diabetes
van de Garde et al.
Thorax 2006;61:957-961.
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COPD is associated with increased mortality in patients with community-acquired pneumonia
Restrepo et al.
Eur Respir J 2006;28:346-351.
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Procalcitonin Guidance of Antibiotic Therapy in Community-acquired Pneumonia: A Randomized Trial
Christ-Crain et al.
Am. J. Respir. Crit. Care Med. 2006;174:84-93.
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Angiotensin-converting enzyme inhibitor use and pneumonia risk in a general population
van de Garde et al.
Eur Respir J 2006;27:1217-1222.
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Impact of Alcohol Abuse in the Etiology and Severity of Community-Acquired Pneumonia
de Roux et al.
Chest 2006;129:1219-1225.
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Impact of initial antibiotic choice on mortality from pneumococcal pneumonia
Aspa et al.
Eur Respir J 2006;27:1010-1019.
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Guidelines for the Treatment of Community-acquired Pneumonia: Predictors of Adherence and Outcome
Menendez et al.
Am. J. Respir. Crit. Care Med. 2005;172:757-762.
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Timing of Antibiotic Administration and Outcomes for Medicare Patients Hospitalized With Community-Acquired Pneumonia
Houck et al.
Arch Intern Med 2004;164:637-644.
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Causes and Factors Associated With Early Failure in Hospitalized Patients With Community-Acquired Pneumonia
Roson et al.
Arch Intern Med 2004;164:502-508.
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Deaths in risk classes I-III: a measure of quality of care in patients hospitalised with CAP?
Marrie
Eur Respir J 2004;23:103-105.
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A prediction rule to identify allocation of inpatient care in community-acquired pneumonia
Espana et al.
Eur Respir J 2003;21:695-701.
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Causes of Death for Patients With Community-Acquired Pneumonia
Stralin et al.
Arch Intern Med 2002;162:2491-2493.
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Severe Community-acquired Pneumonia: Use of Intensive Care Services and Evaluation of American and British Thoracic Society Diagnostic Criteria
Angus et al.
Am. J. Respir. Crit. Care Med. 2002;166:717-723.
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