Letters: Pneumonia in Children Presenting To The Emergency Department With An Asthma Exacerbation

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RESEARCH LETTER nose pneumonia in children with asthma, although less than
5% of children have pneumonia that can be radiographically
Pneumonia in Children Presenting to the Emergency confirmed (hereafter referred to as radiographic pneumonia).2
Department With an Asthma Exacerbation The consequences of the overuse of radiography include in-
Asthma and pneumonia are 2 of the most common reasons creased time in the hospital, unnecessary radiation expo-
children visit the emergency department.1 These conditions sure, increased costs, and inappropriate antibiotic use due to
have overlapping features and can occur concomitantly. Sub- equivocal imaging findings.3 Given the high rate of normal
sequently, physicians often obtain chest radiographs to diag- chest radiographs and the consequences of unnecessary

Table 1. Factors Associated With Radiographic Pneumonia Among Children Presenting


to the Emergency Department With Asthma Exacerbation

Children, Children, No. (%)a


Total No. (%) No Pneumonia Pneumonia
Factor (N = 4708) (n = 4428) (n = 280) P Valuea OR (95% CI)b
Female sex 1965 (41.7) 1830 (41.3) 135 (48.2) .02 1.29 (1.01-1.64)
Age ≥5 y 2573 (54.7) 2385 (53.9) 188 (67.1) <.001 1.91 (1.47-2.48)
Racec
White 2058 (43.8) 1931 (43.7) 127 (45.4)
African American 2051 (43.7) 1927 (43.6) 124 (44.3) .53
Other 587 (12.5) 558 (12.6) 29 (10.4)
Hispanic ethnicity 270 (5.7) 258 (5.8) 12 (4.3) .28
Insurance
Private 1607 (34.1) 1512 (34.1) 95 (33.9)
Government 2982 (63.3) 2804 (63.3) 178 (63.6) >.99
Self-pay 119 (2.5) 112 (2.5) 7 (2.5)
Medical history 488 (10.4) 449 (10.1) 39 (13.9) .04 1.32 (0.92-1.89)
of pneumonia
Taking antibiotics 233 (4.9) 215 (4.9) 18 (6.4) .24
prior to ED visit
Tachycardiad
At triage 2993 (63.6) 2798 (63.2) 195 (69.6) .03 1.16 (0.87-1.54)
During ED visitd 3888 (82.6) 3646 (82.3) 242 (86.4) .08
Tachypnead
At triage 3169 (67.3) 2964 (66.9) 205 (73.2) .03 1.18 (0.88-1.59)
During ED visit 3838 (81.5) 3603 (81.4) 235 (83.9) .30
Oxygen saturation at triagee
Abbreviations: ED, emergency
Normal (≥94%) 3804 (80.8) 3595 (81.2) 209 (74.6) department; OR, odds ratio.
Mild hypoxia (92%-94%) 508 (10.8) 471 (10.6) 37 (13.2) a
Univariable analyses (children with
Moderate hypoxia 212 (4.5) 195 (4.4) 17 (6.1) .06 radiographic pneumonia are those
(90%-92%) with pneumonia that can be
Severe hypoxia (<90%) 165 (3.5) 150 (3.4) 15 (5.4) radiographically confirmed).
b
Lowest oxygen saturation Multivariable analyses.
during ED stay c
A total of 4696 children (4416
Normal (≥94%) 3078 (65.4) 2920 (65.9) 158 (56.4) 1 [Reference] without pneumonia and 280 with
Mild hypoxia (92%-94%) 815 (17.3) 761 (17.2) 54 (19.3) 1.28 (0.93-1.78) pneumonia).
d
Moderate hypoxia 388 (8.2) 361 (8.2) 27 (9.6) <.001 1.27 (0.82-1.95) Tachycardia and tachypnea for age
(90%-92%) were defined as having a heart rate
Severe hypoxia (<90%) 408 (8.7) 369 (8.3) 39 (13.9) 1.88 (1.28-2.74) or respiratory rate in the 99th
percentile or greater for age.5
Fever e
To avoid collinearity, we only
During ED stay 1240 (26.3) 1139 (25.7) 101 (36.1) <.001 1.65 (1.27-2.15) included 1 variable for tachycardia,
(temperature ≥38°C)
oxygen saturation, and fever in the
At triage (temperature 974 (20.7.1) 893 (20.2) 81 (28.9) .001 multivariable model based on the
≥38°C)e best model fit.

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Letters

radiographs, more accurate criteria are needed to identify chil-


Table 2. Odds of Radiographic Pneumonia for Combinations of
dren with asthma who are at increased risk for pneumonia. This Significant Factors From Multivariable Analysis
study aims to identify risk factors for pneumonia in children
Significant Factors Odds Ratio (95% CI)a
with asthma exacerbations.
Female sex and fever 2.12 (1.47-3.07)
Female sex and severe hypoxia (<90%) 2.39 (1.51-3.79)
Methods | This is a retrospective cohort study of children 2 to
Age ≥5 y and female sex 2.47 (1.72-3.54)
18 years of age who presented to the emergency department
Severe hypoxia (<90%) and fever 3.08 (1.92-4.34)
of the Cincinnati Children’s Hospital Medical Center between
January 1, 2010, and December 31, 2013, with an asthma ex- Age ≥5 y and fever 3.17 (2.14-4.69)

acerbation. Children were identified using a validated algo- Age ≥5 y and severe hypoxia (<90%) 3.57 (2.23-5.72)

rithm of an International Classification of Diseases, Ninth Female sex, severe hypoxia (<90%), and fever 3.96 (2.31-6.78)
Revision, Clinical Modification diagnosis code for asthma (code Age ≥5 y, female sex, and fever 4.07 (2.55-6.50)
493.X) in the first 3 diagnosis positions and receipt of 1 or more Age ≥5 y, female sex, and severe hypoxia (<90%) 4.59 (2.69-7.84)
doses of albuterol sulfate in the emergency department.4 We Age ≥5 y, severe hypoxia (<90%), and fever 5.90 (3.37-10.30)
excluded children who were younger than 2 years of age to Severe hypoxia (<90%), female sex, age ≥5 y, 7.59 (4.09-14.10)
and fever
minimize including infants with bronchiolitis. The Cincin-
a
nati Children’s Hospital Medical Center institutional review Interpreted as the odds of having radiographic pneumonia (ie, pneumonia that
can be radiographically confirmed) with all factors listed compared with
board approved this study. Informed consent was not
having none of those factors.
required because the data were deidentified.
Data were abstracted from the electronic health record
Our study is limited by its retrospective nature; however,
(Epic Systems Corporation). Potential factors associated with
prior studies found that many of the variables that we did not
pneumonia included demographics, medical history, medi-
include (eg, auscultatory findings) were not associated with
cations, and vital signs (Table 1). The primary outcome was
pneumonia in wheezing children.2 The validated algorithm that
radiographic pneumonia as determined by 2 investigators
we used to identify children may lead to misclassification be-
who manually reviewed the final radiologist reports using a
cause we are excluding children with asthma but no active
coding manual. Meetings to clarify disagreements occurred
wheezing by requiring albuterol use.4 This will bias our re-
weekly. Abnormal radiographs were classified as definite
sults toward the null because we are underestimating the total
atelectasis, favoring atelectasis, atelectasis vs pneumonia,
burden of asthma, thus likely underestimating the magni-
favoring pneumonia, and definite pneumonia. Radiographic
tude of effect. In the final models, we only included children
pneumonia was present if the radiologist favored or defini-
who underwent radiography of the chest, which may result in
tively diagnosed pneumonia.2 Less than 1.9% of data were
an overestimation of pneumonia. The use of radiographic read-
missing from any variable, so a complete case analysis was
ings from clinical care may introduce variability and bias, but
performed.
knowledge of clinical history represents real-world applica-
The t test and the χ2 test were performed to examine the
tion and does not influence a radiologist’s interpretation.6 Our
relationship between each potential risk factor and radio-
results suggest that routine use of radiography for younger chil-
graphic pneumonia. Variables with P ≤ .20 in the univariable
dren with asthma who are not febrile or hypoxic should be
analysis were included in a multivariable logistic regression
discouraged.
model to determine the association of risk factors with radio-
graphic pneumonia.
Todd A. Florin, MD, MSCE
Hannah Carron, BS
Results | There were 14 007 emergency department visits for
Guixia Huang, MS
asthma exacerbation; chest radiography was performed dur-
Samir S. Shah, MD, MSCE
ing 4708 of 14 007 emergency department visits (33.6%).
Richard Ruddy, MD
Radiographic pneumonia was present in 280 of the 4708 chil-
Lilliam Ambroggio, PhD, MPH
dren who underwent chest radiography (5.9%). Factors inde-
pendently associated with pneumonia included an age of 5 Author Affiliations: Division of Emergency Medicine, Cincinnati Children’s
years or older, female sex, fever, and an oxygen saturation of Hospital Medical Center, Cincinnati, Ohio (Florin, Ruddy); Department of
less than 90% (Table 1 and Table 2). Pediatrics, University of Cincinnati College of Medicine, Cincinnati, Ohio (Florin,
Carron, Shah, Ruddy, Ambroggio); Division of Biostatistics and Epidemiology,
Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio (Huang,
Discussion | Less than 2% of patients with an asthma exacerba- Ambroggio); Division of Hospital Medicine, Cincinnati Children’s Hospital
tion had radiographic pneumonia, yet one-third underwent Medical Center, Cincinnati, Ohio (Shah, Ambroggio); Division of Infectious
chest radiography. Being 5 years of age or older, female, fe- Diseases, Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio (Shah).

brile, and/or hypoxic was statistically associated with radio- Corresponding Author: Todd A. Florin, MD, MSCE, Division of Emergency
Medicine, Cincinnati Children’s Hospital Medical Center, 3333 Burnet Ave, ML
graphic pneumonia. A previous study reported that 4.9% of
2008, Cincinnati, OH 45229 (todd.florin@cchmc.org).
children with wheezing (many <2 years of age) had pneumo-
Published Online: June 6, 2016. doi:10.1001/jamapediatrics.2016.0310.
nia; fever and hypoxia were the strongest pneumonia
Author Contributions: Dr Florin had full access to all of the data in the study
predictors.2 Our study specifically examines pneumonia in and takes responsibility for the integrity of the data and the accuracy of the data
older children with an asthma exacerbation. analysis.

804 JAMA Pediatrics August 2016 Volume 170, Number 8 (Reprinted) jamapediatrics.com

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Letters

Study concept and design: Florin, Carron, Ruddy, Ambroggio. The unweighted response rate ranged from 77% to 93%.3
Acquisition, analysis, or interpretation of data: All authors. Written parental consent was obtained for those younger
Drafting of the manuscript: Florin.
Critical revision of the manuscript for important intellectual content: All authors. than 18 years.
Statistical analysis: Florin, Carron, Huang, Ambroggio. We estimated the proportion of infants ever breastfed (ini-
Obtained funding: Ambroggio. tiated) and those reporting any breastfeeding at 1 month, 4
Administrative, technical, or material support: Ambroggio.
months, and 6 months by birth weight categories and birth year
Study supervision: Florin, Shah, Ruddy, Ambroggio.
cohorts. Infants were excluded if they had not attained the age
Conflict of Interest Disclosures: None reported.
at which breastfeeding was being estimated. Significance was
Funding/Support: Dr Florin received support from the National Center for
Research Resources and the National Center for Advancing Translational set at α < .05 for adjusted Wald method and orthogonal con-
Sciences/National Institutes of Health (grant 5KL2TR000078-05). This study trast matrices for linear tests of trends over time. Taylor se-
was also funded in part by National Institutes of Health grant 1T35HL113229-01 ries linearization was used for variance estimation and 95% CIs
(Ms Carron).
were computed by the Wald method. Kaplan-Meier curves and
Role of the Funder/Sponsor: The funding agencies played no role in the design
log-rank tests assessed differences in the duration of breast-
and conduct of the study; collection, management, analysis, or interpretation of
the data; preparation, review, or approval of the manuscript; and decision to feeding by birth weight cohort from 2009 to 2012. LOESS
submit the manuscript for publication. smoothed curves and 95% CIs from Kaplan-Meier curves are
Disclaimer: Dr Shah is the JAMA Pediatrics Clinical Challenge Editor but was not presented. Infants were censored at the time of interview if
involved in the editorial review or decision to accept the manuscript for they were currently receiving breast milk (12% of respon-
publication.
dents, unweighted n = 324). Overall, 8% of infants were LBW
Additional Contributions: We acknowledge John G. Filcik, BS, for assistance in
(unweighted n = 1279).
the review of the radiograph reports and Mona Ho, MS, for statistical assistance.
No compensation from a funding sponsor was received by either. SAS version 9.3 (SAS Institute) and SUDAAN version 11.0
1. Alpern ER, Stanley RM, Gorelick MH, et al; Pediatric Emergency Care Applied (RTI International) were used. Survey design variables and in-
Research Network. Epidemiology of a pediatric emergency medicine research terview sample weights, which account for differential prob-
network: the PECARN Core Data Project. Pediatr Emerg Care. 2006;22(10): abilities of selection, nonresponse, noncoverage, and sample
689-699.
design, were used to obtain estimates representative of the
2. Mathews B, Shah S, Cleveland RH, Lee EY, Bachur RG, Neuman MI. Clinical
civilian noninstitutionalized US population.
predictors of pneumonia among children with wheezing. Pediatrics. 2009;124
(1):e29-e36.
3. Schuh S, Lalani A, Allen U, et al. Evaluation of the utility of radiography in Results | Among all infants, breastfeeding initiation rates
acute bronchiolitis. J Pediatr. 2007;150(4):429-433. increased from 65.7% (95% CI, 62.4%-69.1%) in 1997-2000
4. Sharifi M, Krishanswami S, McPheeters ML. A systematic review of validated to 76.7% (95% CI, 73.5%-79.8%) (P < .001) in 2009-2012.
methods to capture acute bronchospasm using administrative or claims data. Over the same period, breastfeeding initiation rates
Vaccine. 2013;31(suppl 10):K12-K20.
increased from 48.8% (95% CI, 39.6%-57.9%) to 65.4% (95%
5. Fleming S, Thompson M, Stevens R, et al. Normal ranges of heart rate and CI, 55.4%-75.3%) (P = .01) for LBW infants and from 67.4%
respiratory rate in children from birth to 18 years of age: a systematic review of
observational studies. Lancet. 2011;377(9770):1011-1018. (95% CI, 64.0%-70.8%) to 77.5% (95% CI, 74.3%-80.8%)
6. Test M, Shah SS, Monuteaux M, et al. Impact of clinical history on chest
(P < .001) for infants weighing 2500 g or more at birth
radiograph interpretation. J Hosp Med. 2013;8(7):359-364. (Table). An increasing secular trend in the percentage of
infants still breastfeeding at 1 month (59.7% [95% CI, 56.2%-
63.2%] to 68.7% [95% CI, 65.0-72.4%]; P < .001), 4 months
Trends in Breastfeeding Initiation and Duration (42.6% [95% CI, 39.3%-46.0%] to 49.6% [95% CI, 45.6%-
by Birth Weight Among US Children, 1999-2012 53.7%]; P = .005), and 6 months (36.2% [95% CI, 33.0%-
In the United States, breastfeeding initiation rates have risen 39.5%] to 43.1% [95% CI, 39.3%-47.0%]; P = .002) was
to 80%.1 We report secular trends of breastfeeding initiation observed for infants weighing 2500 g or more. For LBW
and duration by birth weight using nationally representative infants, the increase in the percentage still breastfeeding
data from the National Health and Nutrition Examination over time was not significant at any time after birth. This is
Survey (NHANES). likely owing to insufficient power arising from the small
sample of LBW infants.
Methods | The NHANES is a complex, stratified, multistage prob- Within each birth cohort, the percentage of infants initi-
ability sample of the US civilian noninstitutionalized popula- ating breastfeeding and breastfeeding at 1, 4, and 6 months was
tion, conducted by the National Center for Health Statistics, significantly smaller for LBW infants compared with their
Centers for Disease Control and Prevention. The NHANES heavier counterparts. For example, in 2009-2012, 43.1% of in-
was approved by the National Center for Health Statistics fants (95% CI, 39.3%-47.0%) weighing 2500 g or more were
Research Ethics Review Board. breastfeeding at 6 months compared with 27.7% of LBW in-
Using data from 13 859 children ages 0 to 6 years who fants (95% CI, 18.2%-37.2%) (P < .001). The only exception was
participated in the NHANES from 1999 to 2014, we con- among those still breastfeeding at 1 month in 2001-2004; this
structed birth year cohorts (1997-2000, 2001-2004, 2005- difference was not statistically significant.
2008, and 2009-2012) and birth weight categories (<2500 g The Figure presents the smoothed Kaplan-Meier curves
[low birth weight (LBW)], ≥2500 g). Birth weight and breast- for the overall duration of breastfeeding in the first year of
feeding history (ever breastfed or received breast milk) were life by birth weight categories. Infants who never breastfed
obtained by proxy interview, most commonly by a parent.2 were censored at time zero. Among infants born in

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