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\begin{document}

\title{A Single-Institution Experience in the Use of Chest Radiographs for
Hospitalized Children Labelled as Asthma Exacerbation}



\author[1]{Ela Beyyumi}%
\author[2]{Mohamed Tawil}%
\author[1]{Huda  AlDhanhani}%
\author[1]{Sara  Jameel}%
\author[1]{Manal  Mouhssine}%
\author[1]{Hasa AlNuaimi}%
\author[1]{Osama  Hamdoun}%
\author[1]{Amnah Alabdouli}%
\author[1]{Mohammed Alsamri}%
\author[1]{Ghassan  Ghatasheh}%
\author[3]{Taoufik  Zoubeidi}%
\author[3]{Abdul-Kader  Souid}%
\affil[1]{Tawam Hospital}%
\affil[2]{Shaikh Khalifa Medical City}%
\affil[3]{United Arab Emirates University}%


\vspace{-1em}



  
  \date{May 25, 2024}


\begingroup
\let\center\flushleft
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\selectlanguage{english}
\begin{abstract}
Background: Risks of cancer have become more notable lately, especially
for young children with a chronic condition such as atopy. This study
reports on cumulative radiation from chest radiographs in children with
asthma. Its main aims were to consider our current practice, and suggest
minimizing chest radiograph use in this vulnerable people. Methods: The
study was retrospective and conducted at tertiary center. Eligibility
criteria included children 2-15 y who were admitted between January-2017
and December-2018 for asthma management. Results: Of 643 children who
were admitted as `asthma exacerbation', 243 (40\% females; age
{[}mean\selectlanguage{ngerman}±SD{]} 5.4±3.3 y) met the study criteria for inclusion.
Ninety-two (38\%) children had temperature 38.8±0.7oC on the day of
admission. Antibiotics were prescribed for 148 (61\%) children, mainly
for presumed pneumonia. Chest radiographs were requested for 214 (88\%)
children, mainly on the day of admission. Only 38 (18\%) chest
radiographs showed focal/multifocal pneumonia justifying antibiotic use.
Significant predictors for requesting chest radiographs were antibiotic
use for presumed pneumonia, lower oxygen saturation at presentation, and
requesting blood culture. Rate of chest radiographs per year was
negatively related to child's age; the younger the child the higher the
rate (model coefficient -0.259, P\textless{}0.001). For children
\textless{}5 y, rate of chest radiographs was 1.39±1.21/y and radiation
dose 0.028±0.025 mSV/y. The corresponding rates for children \selectlanguage{english}[?]5 y were
0.78+-0.72/y and 0.008+-0.007 mSV/y, respectively (P\textless{}0.001).
Conclusion: Chest radiographs were commonly requested for children with
asthma, especially the young ones. Prospective studies are necessary to
measure the impact of this practice on their health.%
\end{abstract}\selectlanguage{ngerman}%



\sloppy


\textbf{INTRODUCTION}

Compared to adults, young children are more sensitive to the damaging
effects of low-level ionizing radiation, such as that produced by the
medical imaging {[}1{]}. Although the negative impact of such repeated
exposures is yet to be measured systematically {[}2{]}, the consensus
has been that diagnostic radiographs should be kept at the minimum,
especially for young children with a chronic condition such as asthma
{[}3{]}. As pointed out recently, childhood asthma is a leading cause of
hospitalization, and disparities in its management are substantial
{[}4{]}.

The American Academy of Pediatrics (AAP), the National Heart, Lung and
Blood Institute (NHLBI), and the Global Initiative for Asthma (GINA)
have issued statements addressing the hospital-based care for children
with asthma {[}5-7{]}. The consensus is that requesting a radiographic
imaging requires thoughtful considerations. As wisely stated, there is
an urgent need to improve the awareness of radiation dosing, and
communicating its risk with children's families {[}8-9{]}.

Respiratory disorders are especially common in our community {[}10{]}.
In one study, the estimated prevalence of childhood asthma was about
13\% {[}11{]}. Many of these children, however, have joint causes, such
as atopy, infection, and inherited entities such as primary ciliary
dyskinesia {[}12{]}. Nevertheless, as expected {[}13{]}, the presumptive
diagnosis of `asthma exacerbation' remains a primary cause of our
pediatric admissions. This study aims to determine the prevalence of
requesting chest radiographs for these children. Its main objectives are
to explore our current practice, and suggest rules for improvement.

\textbf{Methods}

This retrospective data collection study was conducted at Tawam
Hospital, a tertiary referral center in Al Ain (Abu Dhabi, UAE) that
covers a population of over 600,000. The study was approved by `Tawam
Human Research Ethics Committee' (AA/AJ/784; `antibiotics and
radiographical investigation misuse in children admitted with acute
asthma exacerbations, Tawam Hospital experience'). Informed consent to
participate in this `Retrospective Chart Review' was exempt.

In our institution, the utilized equipments were expected to result in a
radiation dose of 0.02 mSV per chest radiograph for children
\textless{}5 y, and 0.01 mSV per chest radiograph for children [?]5 y.
Abnormal chest radiographs were independently reviewed by the pediatric
radiologist (M.I.T.); the findings are summarized in Results.

The participants were children 2 to 15 y who were admitted to the
pediatric ward between January 2017 and December 2018, had a primary
diagnostic label of `asthma exacerbation', and received corticosteroids
as a treatment for asthma. Only the last admission was considered for
those who had multiple hospitalizations during the study period.
Children with group A streptococcus pharyngitis (n = 9) or positive
mycoplasma IgM antibody (n = 3) were included, as these pathogens could
trigger asthma. Children who were admitted to the pediatric intensive
care unit (n = 35) or did not receive corticosteroids (n = 155) were
excluded. Other exclusion criteria were children with Down syndrome,
complex heart disease, swallowing dysfunction, sickle cell disease,
primary ciliary dyskinesia, interstitial lung disease, cystic fibrosis,
Stuve-Wiedemann syndrome, chronic lung disease of prematurity,
tracheostomy, bronchiectasis, pulmonary hypertension, malignancy,
tracheoesophageal fistula, and diaphragmatic hernia.

Nasopharyngeal swabs were performed on admission for viral antigen
detection (typically included influenza A and B, respiratory syncytial
virus {[}RSV{]}, parainfluenza, and adenovirus) and/or for pathogen
genome detection by real-time one-step polymerase chain reaction
(RT-PCR). The latter methodology used Allplex Respiratory Panels One
and Two (Seegene Biotechnology Inc., Seoul, Korea). Panel One included
influenza A, influenza B, human RSV A and B, influenza A subtypes H1,
and H1pdm09. Panel Two included adenovirus, metapneumovirus,
enterovirus, and parainfluenza viruses 1, 2, 3, and 4.

\emph{Statistics} . The analysis was performed using SPSS (version 20).
Multiple logistic regression of requesting chest radiographs versus
various predictors was performed using backward selection (likelihood
ratio). Similarly, multiple logistic regression of using antibiotics
versus various predictors was performed using backward selection
(likelihood ratio). Analysis of the rate of chest radiographs per year
was performed using a negative binomial model with log(age) as offset
variable (sample size = 243). The explanatory variables were age and
age\textsuperscript{2}. \emph{P} \textless{}0.05 was considered
significant.

\textbf{RESULTS}

A total of 643 children were admitted with the label `asthma
exacerbation' during the study period. Of those, 243 children met the
study eligibility criteria and their characteristics are summarized in
Table 1. Ninety-two (38\%) children had temperature
[?]38.0\textsuperscript{o}C on the day of admission. Blood culture was
requested for 173 (71\%) children. Three blood cultures were positive;
one for \emph{viridans streptococci} (a 4-year-old child with
temperature 39.2\textsuperscript{o}C), one for micrococcus (a 7-year-old
child who was afebrile), and one for unspecified `gram positive rods' (a
4-year-old child with temperature 38.0\textsuperscript{o}C). Antibiotics
were prescribed for 148 (61\%) children, mainly for presumed pneumonia
(48\%); three of these children had positive mycoplasma IgM antibody.
Five (2\%) children received antibiotics for otitis media, nine (4\%)
for group A streptococcus pharyngitis, and 14 (6\%) as an empiric dose
of ceftriaxone or augmentin in the emergency department. The duration of
antibiotics was 8.4 \selectlanguage{ngerman}± 2.8 days (median, 10 days). The most commonly used
antibiotic was augmentin, followed by ceftriaxone, cefuroxime,
amoxicillin, penicillin V, azithromycin, and clarithromycin.

Pathogen studies were requested for 180 (74\%) children; 40 (16\%)
children had a positive test (Table 1). Temperature
(36\textsuperscript{o}C to 41\textsuperscript{o}C) on the day of
admission did not correlate with either the white blood cell count or
the C-reactive protein (\emph{R} \textsuperscript{2} \textless{}0.03 for
both).

Chest radiographs were requested for 214 (88\%) children. Eighteen (8\%)
children had two views. Hundred and seventeen (54\%) chest radiographs
were normal. Ninety seven (46\%) chest radiographs were interpreted as
abnormal, and were all reviewed by the pediatric radiologist (M.I.T.).
His evaluations were as follows. `Frontal chest radiographs of 97
children were available for review. Previous chest radiograph(s) were
available for comparison in 95 children. The radiographic findings were
classified into three categories: (1) Normal, when no radiographic
abnormalities were identified; (2) Pneumonia, when either unifocal or
multifocal consolidation was identified; and (3) Small airways disease
related changes, when the chest radiograph showed one or more of the
following radiographic features: (a) Hyperinflation, (b) Perihilar
bronchial wall thickening, or (c) Long standing bands of atelectasis.
The results show seven chest radiographs were interpreted as normal, 52
as small airways disease related changes, and 38 as pneumonia (of which
27 as focal pneumonia and 11 as multifocal pneumonia).'

The adjusted rate of chest radiographs for children \textless{}5 y was
1.39±1.21/y and \selectlanguage{english}\emph{[?]} 5 y was 0.78+-0.72/y (\emph{P} = 0.000). The
corresponding radiation dose was 0.028+-0.025 mSV/y and 0.008+-0.007
mSV/y, respectively (\emph{P} = 0.000). The cumulative radiation was
5-fold higher in children \textless{}5 y than that in children \selectlanguage{english}\emph{[?]}
5 y (\emph{P} = 0.000).

Multiple logistic regression of requesting chest radiograph or using
antibiotics versus selected predictors was performed using backward
selection (likelihood ratio), Tables 2-3. Significant predictors for
requesting chest radiograph were use of antibiotics for presumed
pneumonia (\emph{P} = 0.002), lower oxygen saturation at presentation
(\emph{P} = 0.031), and requesting blood culture (\emph{P} = 0.035),
Table 2. The significant predictor for using antibiotics was abnormal
chest radiograph (\emph{P} = 0.009), Table 3.

The next analysis investigated whether the rate of chest radiographs
(mean number divided by age in years) differed with age. As shown in
Fig. 1, a negative binomial model fit the data well. The
deviance/degrees of freedom (df) was 1.029, indicating the chi-square
test of goodness-of-fit was non-significant (deviance = 246.016, df =
239, \emph{P} = 0.223). Akiake Information Criterion (AIC) and Bayesian
Information Criterion (BIC) for the negative binomial model were smaller
than those for the Poisson model: AIC = 1280.94 versus 1549.00 and BIC =
1294.75 versus 1559.38. Thus, the negative binomial model fit the data
better than the Poisson model.

The rate of chest radiographs per year was significantly different for
children of different ages (likelihood ratio chi-square test = 56.61, df
= 2, \emph{P} = 0.000). This rate was negatively related to the child's
age; that is, the younger the child the higher the rate (model
coefficient of age = -0.259, \emph{P} = 0.000; and model coefficient of
age\textsuperscript{2} = 0.010, \emph{P} = 0.016), Table 4. Gender was
not significant when added to the negative binomial model described
above (\emph{P} = 0.336). Thus, gender was dropped from the model.

\textbf{DISCUSSION}

The GINA Report defines \emph{asthma exacerbation} as `an acute or
subacute deterioration of symptoms and lung function from the baseline
control' {[}7{]}. As shown here, this term was used imprudently, as the
majority (400 of 643, or 62\%) of our admissions with this label had
considerable comorbidities and, thus, were unfairly designated as asthma
exacerbation. Therefore, we have used the following joint criteria for
the study eligibility: (1) Use of systemic corticosteroids for the
management of asthma exacerbation, and (2) Absence of associated
(relevant) clinical conditions that could influence the assessment and
management. A misuse of the diagnostic tag ``asthma exacerbation''
impedes the development and implementation of practical evidence-based
rules for these children. In addition, variations linked to regional
medical resources (e.g., national health coverage versus self-paid) play
an important role in these admissions. In a recent study that involved
several emergency departments, the prevalence of chest radiograph use in
children with asthma was about 30\% {[}18{]}. This practice did not
significantly change after implementing a quality improvement approach
(pathway) {[}18{]}.

Radiation is a well-known cause of cancer, especially for
\emph{high}exposures in early life {[}14{]}. We show here that young
children with asthma receive significantly more chest radiographs than
older children do. Therefore, every effort should be taken to alter this
current practice and the habits of unnecessary use of medical radiation
(including computerized tomography scan) for these youngsters
{[}15-16{]}. Suggested recommendations toward this goal include:
(\emph{1} ) Educating healthcare providers about potential adverse
events coupled with diagnostic radiation (e.g., the AAP initiative for
``improving the value of care delivered to children with asthma'')
{[}17-18{]}, (\emph{2} ) Relying on the medical history and physical
examination to attain clinical assessment {[}19-20{]}; (\emph{3} )
Regulating radiation equipments to deliver minimum necessary dosing
{[}14{]}, (\emph{4} ) Establishing evidence-based thresholds for the
allowed radiation dose as function of age {[}21{]}, and (\emph{5} )
Advancing ultrasound and magnetic resonance imaging (MRI) technologies
to replace the diagnostic radiation procedures.

The study here also shows that the significant predictor for using
antibiotics was abnormal chest radiograph. Therefore, a proper
interpretation of chest radiographs is essential to minimize the use of
antibiotics. As shown here, only 38 (18\%) of the 215 chest radiographs
showed focal or multifocal pneumonia justifying antibiotic use.

Study limitations include being retrospective, single institution
experience, limited number of older children (\textgreater{}5 y), not
including infants (\textless{}1 y) and young toddlers (1 to 2 y), and
missing the total radiation dose from all diagnostic procedures. These
issues are subjects of future research.

\emph{Conclusions} : Evidence-based guidelines are needed to minimize
the medical radiation, especially in young children. Parents' education
and counseling are crucial to achieve this goal. The electronic medical
record should alert healthcare providers on the cumulative medical
radiation (green, yellow, or red); only a valid reasoning for the
imaging procedure should be allowed in the `yellow and red' zones.
Evidence-based guidelines are also needed to define the proper
assessment and management of hospitalized children for asthma.

\textbf{DECLARATIONS}

\emph{Competing interests} : The authors declare that they have no
competing interests.

\emph{Funding} : None

\emph{Acknowledgment} : The authors have no conflicts of interest.

\subsection*{\texorpdfstring{\emph{CRediT
Classification}:}{CRediT Classification:}}

{\label{credit-classification}}

\begin{itemize}
\item ~
  \subsection*{\texorpdfstring{\emph{Conceptualization}: Huda Aldhanhani,
  Ela Beyyumi, and Abdul-Kader
  Souid.}{Conceptualization: Huda Aldhanhani, Ela Beyyumi, and Abdul-Kader Souid.}}

  {\label{conceptualization-huda-aldhanhani-ela-beyyumi-and-abdul-kader-souid.}}
\item
  \emph{Data Curation} : Ela Beyyumi, Sara Jameel, Manal Mouhssine, Hasa
  M. AlNuaimi, Osama Hamdoun, Ghassan Ghatasheh, and Amnah Alabdouli.
\item
  \emph{Statistical Analysis} : Taoufik Zoubeidi.
\item
  \emph{Radiographic Analysis} : Mohamed I. Tawil.
\item
  \emph{Clinical Data Analysis} : Huda Aldhanhani, Ela Beyyumi, Mohammed
  T. Alsamri, and Abdul-Kader Souid.
\item
  \emph{Writing -- Original Draft Preparation} : Abdul-Kader Souid, Ela
  Beyyumi, Taoufik Zoubeidi, and Mohamed I. Tawil.
\item
  \emph{Writing -- Review \& Editing} : Abdul-Kader Souid, Ela Beyyumi,
  Taoufik Zoubeidi, Mohamed I. Tawil, and Huda Aldhanhani.
\end{itemize}

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\textbf{Legends}

\textbf{Fig. 1} . Mean observed rates of chest radiographs per year and
the corresponding predicted rates, estimated using the negative binomial
regression model versus age and age\textsuperscript{2}; the model
fitting curve is: Rate of chest radiographs = Exp\{1.124 -- 0.259 Age +
0.010 Age\textsuperscript{2}\}.

\textbf{Hosted file}

\verb`2-Tables.docx`  available at \url{https://authorea.com/users/415541/articles/523399-a-single-institution-experience-in-the-use-of-chest-radiographs-for-hospitalized-children-labelled-as-asthma-exacerbation}\selectlanguage{english}
\begin{figure}[H]
\begin{center}
\includegraphics[width=0.70\columnwidth]{figures/3-Fig/3-Fig}

\end{center}
\end{figure}

\selectlanguage{english}
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