RESEARCH ARTICLE

Hospitalization for Community-Acquired

Pneumonia in Children: Effect of an Asthma
Codiagnosis
Karen M. Wilson, MD, MPH,a Michelle R. Torok, PhD,b,c Russell Localio, PhD,d Lisa McLeod, MD, MSCE,a Rajendu Srivastava, MD, FRCP(C), MPH,e
Xianqun Luan, MS,f Zeinab Mohamad, DrPH,f Samir S. Shah, MD, MSCE,g for the Pediatric Research in Inpatient Settings (PRIS) Network

ABSTRACT

BACKGROUND AND OBJECTIVE: Community-acquired pneumonia (CAP) is a common and

expensive cause of hospitalization among US children, many of whom receive a codiagnosis of acute
asthma. The objective of this study was to describe demographic characteristics, cost, length of stay
(LOS), and adherence to clinical guidelines among these groups and to compare health care
utilization and guideline adherence between them.

METHODS: This was a multicenter retrospective cohort study using data from the Pediatric Health
aSection

of Pediatric
Hospital Medicine,
Childrens Hospital
Colorado and the
University of Colorado
School of Medicine,
Aurora, Colorado;
bSection of Pediatric
Hospital Medicine,
Childrens Hospital
Colorado, Aurora,
Colorado; cChildrens
Outcomes Research,
University of Colorado
School of Medicine,
Aurora, Colorado;
dDepartment of
Biostatistics and
Epidemiology, Perelman
School of Medicine,
University of
Pennsylvania,
Philadelphia,
Pennsylvania; eDivision of
Pediatric Inpatient
Medicine, Department of
Pediatrics, Primary
Childrens Hospital and
Institute for Healthcare
Delivery Research,
Intermountain
Healthcare, Salt Lake City,
Utah; fHealthcare
Analytics Unit, PolicyLab,
Childrens Hospital of
Philadelphia,
Philadelphia,
Pennsylvania; and
gDivisions of Hospital
Medicine and Infectious
Diseases, Cincinnati
Childrens Hospital
Medical Center,
Cincinnati, Ohio

Information System. Children aged 2 to 18 who were hospitalized with uncomplicated CAP from July
1, 2007, to June 30, 2012 were included. Demographics, LOS, total standardized cost, and clinical
guideline adherence were compared between patients with CAP only and CAP plus acute asthma.

RESULTS: Among the 25 124 admissions, 57% were diagnosed with CAP only; 43% had
a codiagnosis of acute asthma. The geometric mean for standardized cost was $4830; for LOS, it was
2.01 days. Eighty-four percent of patients had chest radiographs; CAP1acute asthma patients were
less likely to have a blood culture performed (36% vs 62%, respectively) and more likely not to have
a complete blood count performed (49% vs 27%, respectively). Greater guideline adherence was
associated with higher cost at the patient-level but lower average cost per hospitalization at the
hospital level. CAP1acute asthma patients had higher relative costs (11.8%) and LOS (5.6%) within
hospitals and had more cost variation across hospitals, compared with patients with CAP only.
CONCLUSIONS: A codiagnosis of acute asthma is common for children with CAP. This could be
from misdiagnosis or co-occurrence. Diagnostic and/or management variability appears to be greater in
patients with CAP1asthma, which may increase resource utilization and LOS for these patients.

www.hospitalpediatrics.org
DOI:10.1542/hpeds.2015-0007
Copyright 2015 by the American Academy of Pediatrics
Address correspondence to Karen M. Wilson, MD, MPH, Section of Pediatric Hospital Medicine, Childrens Hospital Colorado, University of
Colorado School of Medicine, 13123 E. 16th Ave, B302, Aurora, CO 80045. E-mail: Karen.wilson@childrenscolorado.org
HOSPITAL PEDIATRICS (ISSN Numbers: Print, 2154-1663; Online, 2154-1671).
FINANCIAL DISCLOSURE: Drs Wilson, Srivastava, and Shah were supported by the Childrens Hospital Association. The other authors have
indicated that they have no nancial relationships relevant to this article to disclose.
FUNDING: A grant from the Childrens Hospital Association to the Pediatric Research in Inpatient Settings Network
POTENTIAL CONFLICT OF INTEREST: The authors have indicated they have no potential conicts of interest to disclose.
Dr Wilson conceptualized the design and led the study and drafted the initial manuscript; Dr Torok helped with analytic planning and methods,
completed statistical analyses, and helped draft the manuscript; Dr Localio led the analytic plan and advised on statistical procedures and study
design, performed statistical analyses, drafted parts of the manuscript, and helped edit the manuscript; Mr Luan and Dr Mohamad completed
statistical analyses, assisted with study design, and helped edit the manuscript; Drs McLeod, Srivastava, and Shah participated in the study
design, analytic planning, and data quality review and edited the manuscript; and all authors approved the nal manuscript as submitted.

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415

Community-acquired pneumonia (CAP)

ranks among the most common and costly
reasons for hospitalization of children.1
Children hospitalized with CAP often receive
a diagnosis of asthma, a condition
colloquially referred to as asthmonia.
Distinguishing CAP occurring alone from
CAP occurring with an asthma exacerbation
can be challenging because viral
respiratory tract infections predispose to
bacterial pneumonia and also trigger
asthma exacerbations. In addition, although
CAP is typically diagnosed by chest
radiograph or focal lung ndings, there is
evidence that atelectasis can mimic
inltrates,2 which could lead to
misdiagnosis of pneumonia in a patient with
asthma. Children with asthma are at
increased risk for invasive pneumococcal
infections,3 including pneumonia. An
important challenge in the management of
CAP occurring with an asthma exacerbation
is that national guidelines focus treatment
on a single diagnosis (CAP alone or asthma
alone), and in some cases, the guidelines
conict on ideal management.4,5
The guidelines for treatment of
uncomplicated CAP include obtaining
bacterial cultures, viral testing,
inammatory markers, chest radiography,
and the use of an aminopenicillin.
Corticosteroids, a mainstay of asthma
therapy, have not been proven effective for
the treatment of CAP in randomized trials
involving adults6 and are not recommended.
There is no role for bronchodilators in the
treatment of CAP. In contrast, management
of an acute asthma exacerbation includes
administration of oral corticosteroids and
bronchodilators. Routine chest radiographs
and viral testing are not recommended, and
in fact, chest radiographs in pediatric
asthma were chosen as one of the Choosing
Wisely campaigns procedures not to order.7
Previous studies of hospital-level adherence
to CAP guidelines have shown variability; the
average percent of patients receiving
a chest radiograph for CAP across 29
childrens hospitals ranged from 54% to
90%, whereas the average percent of
patients with a documented blood culture
ranged from 0% to 92%.8 Conversely,
adherence to the asthma care guidelines of

using systemic corticosteroids and

bronchodilators was high and consistent
across hospitals.9 Although the
recommendations for management of
uncomplicated pneumonia alone or asthma
alone are well dened, they do not provide
direction for a common clinical occurrence:
treating patients who are diagnosed with
both. We hypothesized that this might lead
to more diagnostic uncertainty, and
therefore decreased adherence to clinical
care guidelines, increased health care
utilization, and variation in the clinical
management and treatment of these
patients. Understanding how patients who
have pneumonia and asthma codiagnoses
inuence utilization might help to clarify
more appropriate patient selection for
guidelines use, and allow systems of
carebased interventions to more
accurately measure patient and cost
outcomes.
We used data from a national multihospital
cohort of children to determine the
variation in resource utilization and
adherence to the pneumonia guidelines in
children with CAP with and without
a concomitant diagnosis of asthma.

METHODS
Data Source and Study Design
We conducted a retrospective, multicenter
cohort study using data from the Pediatric
Health Information System (PHIS), an
administrative database that contains
inpatient data from .40 pediatric hospitals
in the United States. Detailed hospitalization
and resource utilization data, such as
demographic, diagnostic, procedural,
outcome, and charge information, are
contained in PHIS. Data are deidentied;
however, encrypted medical record
numbers permit tracking of patients within
hospitals across hospitalizations. The
Childrens Hospital Association and
participating hospitals jointly ensure data
quality as previously described.10 This study,
using deidentied data, was considered
exempt according to the policies of the
Cincinnati Childrens Hospital Medical
Center Institutional Review Board.

Study Cohort
We created a cohort of patients with
uncomplicated CAP and CAP1asthma for

which the pneumonia guidelines would

apply.4 We used a previously validated
algorithm for identifying hospitalized
patients with CAP from PHIS.11 Patients aged
.3 months and ,18 years between July 1,
2007, and June 30, 2012, with principal or
secondary diagnosis International
Classication of Diseases, Ninth Revision,
Clinical Modication diagnosis codes of
pneumonia were eligible. We excluded
patients who were unlikely to have
a diagnosis of uncomplicated CAP using the
following criteria: (1) receipt of antibiotics
not typically used for CAP on day 0, 1, or 212;
(2) no charge for antibiotics on the rst
hospital day; (3) an International
Classication of Diseases code for viral
pneumonia; (4) complex chronic condition13;
(5) age ,2 years (to avoid misclassication
with bronchiolitis); (6) a charge for a chest
computed tomography, ultrasound, or
decubitus lms on the rst hospital day (to
exclude complicated pneumonia on
presentation); (7) a charge for
hyperalimentation on the rst hospital day;
or (8) a charge for extracorporeal
membrane oxygenation on the rst hospital
day. Three clinicians reviewed all additional
diagnoses and procedures and excluded
patients with diagnoses or procedures
suggesting a low likelihood of CAP (eg,
motor vehicle trafc accident). To better
ensure patients with a typical presentation
of CAP, we excluded hospitalizations for
which total costs were beyond the lowest
and highest fth percentile within each
hospital.1 For patients with multiple
admissions meeting the inclusion criteria,
we selected the rst hospitalization.

Exposure Measure
The main exposure was meeting inclusion
criteria for CAP and a codiagnosis of acute
asthma (CAP1asthma). Patients were
considered to have CAP1asthma if they had
any diagnosis code of asthma and a charge
for a short-acting bronchodilator use after
hospital day 1. Because 35% of children
admitted with a diagnosis of CAP in 1 large
cohort had received corticosteroids14 and
this was more common in patients in the
ICU, we did not include steroid use as
a specic marker for asthma to avoid
confounding by severity. Patients in the
CAP1asthma exposure group were

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compared with the clinical group who had

CAP without acute asthma.

Covariables
Categorized age (,5, 511, $12 years),
gender, race (white, black, Asian, other);
insurance (government, nongovernment);
geographic region (Midwest, Northeast,
South, West), mean number of hospital
beds, and ICU stay (yes/no) were included in
the analyses.
Outcome Measures
Measured outcomes were length of stay
(LOS), total standardized cost, and
guideline adherence. LOS in days was
measured as a continuous variable. Total
standardized cost in US dollars was
calculated using a Cost Master Index (CMI)
previously developed for research utilizing
data from PHIS hospitals.1 Briey,
standardized costs for an entire patient
hospitalization are calculated by rst
multiplying the billed units of each item by
its standardized per unit cost and then
summing these itemized costs, resulting in
a total standardized hospital bill.15 All
standardized costs were inated to 2012
dollars by using the medical care services

component of the Consumer Price Index. Of

the 42 hospitals contained in the PHIS
database, 2 were excluded from cost and
LOS analyses due to missing data.
Adherence to the Pediatric Infectious
Diseases Society and the Infectious Diseases
Society of America clinical guidelines for the
management of children with pneumonia3
was the nal outcome. The following
guidelines were assessed, based on
availability in the PHIS dataset: receipt of
chest radiograph (recommended), blood
culture (recommended), respiratory viral
panel testing (recommended), Mycoplasma
pneumoniae testing when macrolide was
ordered (recommended), complete blood
count testing (not recommended), and
Chlamydophila pneumoniae testing (not
recommended). We considered all available
recommendations regardless of strength of
evidence. Adherence to guidelines on the
individual level was depicted as a rate
(number of guidelines followed/total
guidelines measured). Adherence to
guidelines at the hospital-level was depicted
as the mean number of guidelines followed
per patient with CAP admitted to that
particular hospital.

Statistical Analysis
We described variation in the total
standardized costs within hospital using the
geometric mean and range. Bivariable
differences between the exposure groups
were tested using x2 and Wilcoxon ranksum tests for individual-level
characteristics. We used Cochran-MantelHaenszel statistics to test differences in
demographic and clinical course
characteristics between the 2 clinical
groups when stratied by hospital, and logrank tests were used for stratied tests to
evaluate differences between clinical
groups for continuous but skewed
characteristics accounting for hospital.
Analysis of variance was used to test
bivariable differences for hospital-level
variables (region and number of beds).
We modeled cost and LOS with a log g
model with patient-level factors as
covariates and accounting for clustering of
patients by hospital. These models
decomposed the effects of the covariates
into within-hospital and between hospital
components to rule out possible
confounding by hospital in these
associations of interest.16,17 This

FIGURE 1 Cohort selection ow diagram. CT, computed tomography; ECMO, extracorporeal membrane oxygenation;

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decomposition permits 2 comparisons of

interest: (1) the effects of the risk factor on
outcome when applied to otherwise similar
children within a hospital (eg, do 2 similar
patients at the same hospital have different
outcomes depending on guideline

adherence in their management) and (2)

the effects when moving from a hospital
with 1 average level of a risk factor to
a hospital with a different average level of
the same factor (eg, do similar patients
admitted to 2 hospitals with varying average

guideline adherence across their patient

populations have different outcomes).18
Results from this decomposed model of the
within hospital comparison were then
conrmed with models in which hospital
was a xed effect. We also evaluated the

TABLE 1 Bivariable Comparison of Characteristics Between Clinical Groups

Overall (n 5 25 124)

Characteristics
Age, y (median, SD)

Range Among
Hospitals (n 5 42) (%)

5.0 (3.6)

CAP (n 5 14 390)
4.0 (3.7)

CAP1acute
asthma (n 5 10 734)
5.0 (3.4)

Age, y
,5

12 490 (49.7)

39.868.9

511

10 463 (41.7)

$12

2171 (8.6)

Female
Principal payer, governmentc
ICU stay

Pa

Pb

,.0001
,.0001

,.001

7478 (52.0)

5012 (46.7)

25.450.0

5566 (38.9)

4897 (45.6)

5.414.7

1346 (9.4)

825 (7.7)

12 051 (48.0)

40.054.9

7136 (49.6)

4915 (45.8)

,.0001

,.001

10 514 (41.9)

6.567.0

5639 (39.2)

4875 (45.4)

,.0001

,.001

1936 (7.7)

1.427.9

519 (3.6)

1417 (13.2)

,.0001

,.001

,.0001

,.001

,.0001

N/A

,.0001

N/A

Race (n 5 24 231)
White

13 200 (54.5)

9.599.0

8670 (62.5)

4530 (43.7)

Black

6630 (27.4)

1.771.4

2696 (19.5)

3934 (37.9)

Asian

718 (3.0)

0.234.8

498 (3.6)

220 (2.1)

Other

3683 (15.2)

0.970.1

2000 (14.4)

1683 (16.2)

Region
Midwest

7306 (29.1)

4046 (28.1)

3260 (30.4)
1326 (12.4)

Northeast

2683 (10.7)

1357 (9.4)

South

9620 (38.3)

5882 (40.9)

3738 (34.8)

West

5515 (21.9)

3105 (21.6)

2410 (22.5)

Number of beds
#200 beds

3191 (12.7)

1695 (11.9)

1496 (13.9)

201300 beds

8220 (32.7)

4730 (32.9)

3490 (32.5)

301400 beds

6621 (26.4)

4037 (28.1)

2584 (24.1)

.400 beds

7092 (28.2)

3928 (27.3)

3164 (29.5)

Metrics
% with chest radiograph

20 973 (83.5)

50.094.1

11 906 (82.7)

9067 (84.5)

.0003

% with blood culture

12 829 (51.1)

27.383.3

8931 (62.1)

3898 (36.3)

,.0001

,.0001

.002

% without CBC

9170 (36.5)

6.162.6

3957 (27.5)

5213 (48.6)

,.0001

,.0001

% with respiratory viral panel testing

7935 (31.6)

8.687.9

4477 (31.1)

3458 (32.2)

.06

.17

% with macrolide with

mycoplasma testing

1693 (6.7)

0.455.0

992 (6.9)

701 (6.5)

.26

.18

25 087 (99.9)

99.42100.0

.02

.03

% without Chlamydophila
pneumonia testing

14 362 (99.8)

10 725 (99.9)

LOS, d geometric mean (range), dd

2.0

1.32.6

1.9 (1.22.5)

2.1 (1.52.8)

,.0001

,.0001

ICU LOS, geometric mean (range), de

1.6

1.02.3

1.6 (1.02.3)

1.6 (1.02.8)

.28

,.0001

,.0001

,.0001

Total standardized cost,

geometric mean (range), US$d

4830.4

3291.56547.3

4519.3 (3024.96477.4)

5269.7 (3418.27474.5)

CBC, complete blood count.

a
x 2 and Wilcoxon rank-sum test used to test individual-level variables; analysis of variance used to test hospital-level variables (region and number of beds).
b
Controlling for hospital: Cochran-Mantel-Haenszel statistics used for categorical variables; log-rank test used for continuous variables.
c
Dened as Charity, In-State Medicaid (managed care), In-State Medicaid (other), Medicare, Other Government, Out-of-State Medicaid (all), TRICARE.
d
LOS and total cost data missing for 2 hospitals (n 5 1181).
e
Patients with an ICU stay, n 5 1936.
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effect of codiagnosis on cost and LOS

within hospitals by hospital, by comparing
the likelihood ratios from 2 models. The
rst was the same model as described
earlier, with hospital as a xed effect. The
second included an interaction term
between hospital and clinical group (CAP
or CAP1asthma). A likelihood ratio test
was performed to examine cost and LOS by
hospital. Data were analyzed using SAS
v9.3.
Finally, we investigated the relative
contribution to interhospital variance in
standardized costs attributable to CAP and
CAP1asthma using a mixed effects model
with separate hospital-level random
intercepts for the 2 groups. We compared
these 2 variance components with total
variance (including the residual, withinhospital component), using Stata version 13.
Because log g models for this question
would not converge, we opted for identity
link models for this estimation.

RESULTS
Patient and Hospital Characteristics
Of the 112 441 admissions eligible for study
inclusion, 25 124 with CAP remained after
applying exclusion criteria (Fig 1); of these,
43% had an additional diagnosis of and
treatment of acute asthma.
The median age was 5.0 years (Table 1). The
distribution of age group, insurance, ICU
stay, and race varied widely across
hospitals. When comparing the 2 clinical

groups, patients hospitalized with CAP1

asthma had a greater median age and were
more likely to be male, to be black or
other race/ethnicity, and to have
government insurance than those with CAP
only. Because patient characteristics are
known to differ by hospital, we compared
demographic and clinical course
characteristics between the 2 clinical
groups adjusting for hospital. The difference
in the number of ICU days by clinical group
reached statistical signicance when
accounting for hospital; other results were
similar to the unadjusted results (Table 1).
Patients with CAP1asthma were more likely
to have received a macrolide antibiotic than
those with CAP alone (59% vs 37%; P , .001)
and to have received corticosteroids (87%
vs 12%; P , .001).

Resource Utilization
Standardized cost varied between hospitals,
from $3292 to $6547, with an overall
geometric mean of $4830. Figure 2 displays
the cost distribution by hospital and clinical
group. Thirty-eight of the 40 hospitals had
higher costs for the CAP1asthma patients
compared with CAP alone. CAP1asthma
patients had higher geometric mean cost
compared with CAP alone ($5270 vs $4519)
(Table 1). Multivariable analysis of total
standardized cost within hospitals indicated
that CAP1asthma patients were more
costly compared with CAP alone (Table 2).
We estimated cost variances not explained
by patient-level factors between patients

with CAP compared with those with CAP1

asthma, and found that unexplained
interhospital variation as a percentage of
total variation in costs was 7.6% for CAP
and 12.3% for CAP1asthma. The likelihood
ratio test for within hospital cost was
statistically signicant, suggesting that
there was some variation in total
standardized cost between CAP1asthma
and CAP only patients across hospitals.
However, the data suggest that for the vast
majority of hospitals, cost is higher among
CAP1asthma patients.
The overall geometric mean for LOS was
2.01, with a range of 1.3 to 2.6 between
hospitals. For ICU days, the overall mean
was 1.63 with a range between hospitals
from 1.0 to 2.3 (Table 1). Figure 3 shows the
distribution of LOS by clinical group and
hospital. Although 7 of 40 hospitals had
longer LOS for CAP alone, the majority had
longer LOS for CAP1asthma. Patients with
CAP1asthma had longer LOS (2.1 vs 1.9);
however, ICU LOS was similar (1.6 vs 1.6,
P 5 .28). Multivariable analysis indicated
that patients with CAP1asthma had a 6%
longer LOS compared with CAP patients
without acute asthma (Table 2). The
likelihood ratio test for within hospital LOS
was statistically signicant, suggesting that
there was some variation in LOS between
CAP1asthma and CAP-only patients across
hospitals. For the majority of hospitals, LOS
was longer for CAP1asthma compared with
CAP only patients.

FIGURE 2 Distribution of total standardized cost by clinical group and hospital (n 5 40).
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TABLE 2 Multivariable Regression Results for Total Standardized Cost and LOS
Total Standardized Cost (n 5 22 853)a

DISCUSSION

95% CI

Relative Cost per Unit

Change in Variable

Across hospital contrast of effect of diagnosis on

costs per 10% increase in the proportion of
CAP1acute asthma patientsb

0.650

0.4390.962

.03

The difference between CAP-only vs CAP1acute

asthma groups within each hospitalc

1.118

1.0831.155

,.0001

LOS (n 5 22 853)d

Relative LOS per Unit

Change in Variable

Across-hospital contrast of effect of diagnosis on

LOS per 10% increase in proportion of CAP1
acute asthma patients

0.953

0.5851.553

.85

The difference between CAP-only vs CAP1acute

asthma groups within each hospitale

1.056

1.0121.101

.01

Total Standardized Costs and Guideline Adherence

(n 5 23 054)f,g

Relative Cost per Unit

Change in Variable

Number of guidelines adhered to

12

Reference

34

1.201

1.1521.252

,.0001

1.407

1.3081.513

,.0001

Mean no. of guidelines to which hospital adhered

for CAP1acute asthma patients

0.823

0.6830.991

.04

Mean no. of guidelines to which hospital adhered

for CAP-only patients

0.844

0.7101.003

.05

Proportion of patients who have CAP1acute

asthma

1.166

0.7331.857

.52

Sample sizes do not add up to 25 124 due to missing data (see Table 1). Estimates are from a log-g model.
Adjusted for gender, insurance, age group, race, ICU stay, mean number of hospitals beds, and mean LOS.
b
A relative cost of 0.650 means that across hospitals, a 10% increase in CAP1acute asthma patients is
associated with a 35% relative decrease in total standardized cost when controlling for the other
variables in the model.
c
A relative cost of 1.118 means that within hospitals there is a 11.8% relative increase in cost among CAP1acute
asthma patients compared with CAP-only patients when controlling for the other variables in the model.
d
Adjusted for gender, insurance, age group, race, proportion of blacks at the hospital, and ICU stay.
e
There is a 5.6% relative increase in LOS among CAP1acute asthma patients compared with CAP only
patients when controlling for the other variables in the model.
f
Adjusted for gender, insurance, age group, race, ICU stay, and mean number of hospital beds.
g
Controlling for other factors in the model, when 34 vs 12 guidelines are adhered to, there is a relative
increase in total standardized cost of 20%. When 5 guidelines vs 12 guidelines are adhered to, there
is a 40% relative increase in cost. As the mean number of guidelines adhered to at a hospital increases,
the relative cost of CAP1acute asthma patients decreases by 18%; for CAP-only patients, the relative
total standardized cost decreases 16%.
a

Guideline Adherence
When comparing the 2 clinical groups at the
patient level, .80% of patients in both
groups received chest radiographs
(Table 1). CAP1asthma patients were less
likely to have a blood culture performed
(36% vs 62%) and more often did not have
a CBC performed (49% vs 27%). Few
patients in either group received
a macrolide with M pneumoniae testing
(close to 7% in each group), and few
patients in either group had C pneumoniae

testing. Approximately 30% in each group

received respiratory viral panel testing.
Across hospitals, the range of the percent of
guideline adherence was wide for all of the
guidelines except testing for M pneumoniae
and C pneumoniae. At the patient-level,
greater guideline adherence was associated
with higher cost. However, contrasting
adherence across hospitals, greater
hospital-level guideline adherence was
associated with lower average cost per
hospitalization (Table 2).

We found a high percentage of cases of

pneumonia that had a codiagnosis of and
treatment for asthma exacerbation;
although we used an algorithm for
identifying CAP that has been validated with
chart review and radiology data, the
presence of an inltrate on a chest x-ray
may not always represent pneumonia but
may in fact be atelectasis in a case of
primary asthma. In addition, we may be
overidentifying cases of asthma in which
albuterol is being used inappropriately.
Regardless of whether these cases are
misdiagnoses or are truly patients with
pneumonia and asthma, this study
demonstrated the challenge of measuring
guideline adherence in the face of
codiagnoses and diagnostic uncertainty,
particularly in the management of common,
acute pulmonary processes in children. In
this cohort of patients admitted to 42
childrens hospitals, codiagnosis resulted in
broader variation in management and
higher cost. These results also highlight the
complexity of implementing guidelines
where there is true codiagnosis or
diagnostic uncertainty in carefully
identifying the appropriate target
population for guideline development and
management so that when comparing
outcomes, hospitals are using the clinical
groups of patients.
Overall, CAP1asthma patients within the
same hospital had higher costs and longer
LOS than those with CAP alone. There was
signicant variability in cost and LOS among
the hospitals for both CAP and CAP1
asthma. Although having a second diagnosis
may inherently increase overall cost,
a secondary diagnosis of asthma also
increased observed variation in costs
across hospitals, suggesting that the
addition of the second diagnosis may
increase uncertainty. This could be
diagnostic uncertainty, management
uncertainty, or both.
Inappropriate diagnosis with a second
disease process could result in overuse or
misuse of nonrecommended care, and
therefore higher costs. Increasing diagnostic
precision and standardizing treatment of
codiagnoses such as CAP1asthma may

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FIGURE 3 Distribution of length of stay by clinical group and hospital (n 5 s40).

help to decrease interhospital variability in

cost. In particular, adhering to the
recommendation not to get a chest
radiograph in children admitted with
clinical asthma exacerbations might
signicantly decrease the overall cost and
variation in care. The mean LOS for CAP1
asthma of 2.1 days was longer than that
reported in another PHIS study for
noncomplex asthma alone (1.8 days),19 also
supporting the idea that the additional
diagnosis adds complexity. Future studies
examining the impact of a pneumonia
diagnosis on variation in care for asthma
exacerbations may provide corollary
information.
Overall, hospitals that had greater
adherence to the CAP guidelines across
their patient population had lower the
overall costs for CAP and CAP1asthma,
suggesting that although some guidelines
may be applied inappropriately, especially
for CAP1asthma, standardization of care
has some association with lower costs of
care. Because adherence to guidelines for
both CAP and asthma are being used as
quality metrics in some institutions, it may
be helpful to use these as metrics for
patients only when a codiagnosis is not
present.
Studies using administrative data are
inherently limited by the quality of the data
provided by the hospitals, and there are

many potential explanatory variables that

are not available to us in PHIS. Although
PHIS has excellent quality control standards,
its data are not routinely validated with
chart review. We used an algorithm for
diagnosing CAP that has been validated with
chart review,11 but it is nonetheless possible
that there was misclassication for both the
CAP and asthma diagnoses. In addition, we
used antibiotic choice to select out cases of
CAP, which meant that we could not include
antibiotic selection in our analysis of
guideline adherence. Our denition of acute
asthma exacerbation may cause us to
underestimate such cases. We did not
include corticosteroid administration in our
denition because corticosteroids,
particularly at some hospitals, may be
administered to children with CAP.14 This
approach would bias the results to the null
hypothesis. We also had a signicant
number of exclusions to create our nal
cohort; some of these may have biased our
data. Although the pneumonia guidelines
have recommendations related to
M pneumoniae and C pneumoniae testing,
the lack of timely availability of results for
these tests at many institutions is likely to
be an important barrier to their use. The
data are retrospective, and thus we cannot
assume causation. Because we limited our
analyses to children .2 years of age, this
may have increased the potential for
asthma codiagnoses. Finally, our data may

not be generalizable outside of freestanding

childrens hospitals.

CONCLUSIONS
A codiagnosis of acute asthma is common
for children with CAP, adding a layer of
treatment complexity that may increase
resource utilization and LOS, regardless of
whether there is diagnostic
misclassication or whether there are truly
2 disease processes. There is still a high
degree of uncertainty surrounding the most
effective and efcient way to treat CAP1
asthma, and the appropriateness of existing
guidelines to address the co-occurrence of
these conditions. Clinicians should be clear
about which diagnosis they are treating,
which guideline should be applied when the
clinician is unsure, or whether 2 diagnoses
are clearly present. Patients with 2
diagnoses deserve to have both diagnoses
treated according to evidence-based
protocols. In the interim, hospitals can
examine their practice patterns for CAP1
asthma and if they are outliers, work to
standardize and streamline care. As we
increasingly rely on guidelines for the care
of children hospitalized with common
diseases, it is important to remember that
they often have .1 diagnosis, and these
guidelines should incorporate evidence
about common co-occurring conditions as
well as provide recommendations on their
treatment.

HOSPITAL PEDIATRICS Volume 5, Issue 8, August 2015

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421

REFERENCES

double-blinded clinical trial. Am J Respir

Crit Care Med. 2010;181(9):975982

1. Keren R, Luan X, Localio R, et al; Pediatric

Research in Inpatient Settings (PRIS)
Network. Prioritization of comparative
effectiveness research topics in hospital
pediatrics. Arch Pediatr Adolesc Med.
2012;166(12):11551164

7. Quinonez RA, Garber MD, Schroeder AR,

et al. Choosing wisely in pediatric
hospital medicine: ve opportunities for
improved healthcare value. J Hosp Med.
2013;8(9):479485

2. Williams GJ, Macaskill P, Kerr M, et al.

Variability and accuracy in
interpretation of consolidation on chest
radiography for diagnosing pneumonia
in children under 5 years of age. Pediatr
Pulmonol. 2013;48(12):11951200

8. Brogan TV, Hall M, Williams DJ, et al.

Variability in processes of care and
outcomes among children hospitalized
with community-acquired pneumonia.
Pediatr Infect Dis J. 2012;31(10):
10361041

3. Talbot TR, Hartert TV, Mitchel E, et al.

Asthma as a risk factor for invasive
pneumococcal disease. N Engl J Med.
2005;352(20):20822090

9. Morse RB, Hall M, Fieldston ES, et al.

Hospital-level compliance with asthma
care quality measures at childrens
hospitals and subsequent asthmarelated outcomes. JAMA. 2011;306(13):
14541460

4. Bradley JS, Byington CL, Shah SS, et al;

Pediatric Infectious Diseases Society and
the Infectious Diseases Society of
America. The management of
community-acquired pneumonia in
infants and children older than 3
months of age: clinical practice
guidelines by the Pediatric Infectious
Diseases Society and the Infectious
Diseases Society of America. Clin Infect
Dis. 2011;53(7):e25e76
5. National Asthma Education and
Prevention Program. Expert Panel
Report 3 (EPR-3): Guidelines for the
Diagnosis and Management of AsthmaSummary Report 2007. J Allergy Clin
Immunol. 2007;120(5 Suppl):S94S138
6. Snijders D, Daniels JM, de Graaff CS, van
der Werf TS, Boersma WG. Efcacy of
corticosteroids in community-acquired
pneumonia: a randomized

10. Mongelluzzo J, Mohamad Z, Ten Have TR,

Shah SS. Impact of bacterial meningitisassociated conditions on pediatric
inpatient resource utilization. J Hosp
Med. 2010;5(6):E1E7
11. Williams DJ, Shah SS, Myers A, et al.
Identifying pediatric communityacquired pneumonia hospitalizations:
Accuracy of administrative billing
codes. JAMA Pediatr. 2013;167(9):
851858
12. Ambroggio L, Tabb LP, OMeara T,
Shefer-Collins S, McGowan KL, Shah
SS. Inuence of antibiotic
susceptibility patterns on empiric
antibiotic prescribing for children
hospitalized with community-acquired
pneumonia. Pediatr Infect Dis J. 2012;
31(4):331336

13. Feudtner C, Hays RM, Haynes G, Geyer

JR, Neff JM, Koepsell TD. Deaths
attributed to pediatric complex chronic
conditions: national trends and
implications for supportive care
services. Pediatrics. 2001;107(6).
Available at: www.pediatrics.org/cgi/
content/full/107/6/E99
14. Weiss AK, Hall M, Lee GE, Kronman MP,
Shefer-Collins S, Shah SS. Adjunct
corticosteroids in children hospitalized
with community-acquired pneumonia.
Pediatrics. 2011;127(2):e255e263
15. Drummond MF, Schulpher MJ, Torrance
GW, OBrien BJ, Stoddart GL. Methods for
the Economic Evaluation of Health Care
Programmes. 2nd ed. Oxford, UK: Oxford
University Press; 1997
16. Berlin JA, Kimmel SE, Ten Have TR,
Sammel MD. An empirical comparison of
several clustered data approaches
under confounding due to cluster effects
in the analysis of complications of
coronary angioplasty. Biometrics. 1999;
55(2):470476
17. Neuhaus JM, Kalbeisch JD. Betweenand within-cluster covariate effects in
the analysis of clustered data.
Biometrics. 1998;54(2):638645
18. Begg MD, Parides MK. Separation of
individual-level and cluster-level
covariate effects in regression analysis
of correlated data. Stat Med. 2003;
22(16):25912602
19. Morse RB, Hall M, Fieldston ES, et al.
Childrens hospitals with shorter lengths
of stay do not have higher readmission
rates. J Pediatr. 2013;163(4):1034, e1

422

WILSON et al

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Hospitalization for Community-Acquired Pneumonia in Children: Effect of an

Asthma Codiagnosis
Karen M. Wilson, Michelle R. Torok, Russell Localio, Lisa McLeod, Rajendu
Srivastava, Xianqun Luan, Zeinab Mohamad, Samir S. Shah and for the Pediatric
Research in Inpatient Settings (PRIS) Network
Hospital Pediatrics 2015;5;415
DOI: 10.1542/hpeds.2015-0007

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Hospitalization for Community-Acquired Pneumonia in Children: Effect of an

Asthma Codiagnosis
Karen M. Wilson, Michelle R. Torok, Russell Localio, Lisa McLeod, Rajendu
Srivastava, Xianqun Luan, Zeinab Mohamad, Samir S. Shah and for the Pediatric
Research in Inpatient Settings (PRIS) Network
Hospital Pediatrics 2015;5;415
DOI: 10.1542/hpeds.2015-0007

The online version of this article, along with updated information and services, is
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