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\begin{document}

\title{Factors associated with length to recover adequate nutrition and length
of stay in children hospitalized for bronchiolitis: a retrospective
study.}



\author[1]{Arnaud Maugendre}%
\author[2]{Clément Médrinal}%
\author[3]{Tristan Bonnevie}%
\author[2]{Pascal Le Roux}%
\author[2]{Guillaume Prieur}%
\author[2]{Yann Combret}%
\affil[1]{Cabinet COTTEAU et Assistant.e.s}%
\affil[2]{Groupe Hospitalier du Havre}%
\affil[3]{University Hospital Centre Rouen}%


\vspace{-1em}



  
  \date{May 19, 2024}


\begingroup
\let\center\flushleft
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\selectlanguage{english}
\begin{abstract}
Context: Inadequate feeding is a frequent reason for hospital referring
in children with bronchiolitis and leads to prolonged hospitalization in
26\% of the cases. The main objective was to identify the factors
associated with the time to recover adequate nutrition in infants
hospitalized for bronchiolitis. Method: We conducted a single-center
retrospective study including infants less than 12 months hospitalized
for bronchiolitis at Le Havre Hospital (France) between September 2018
and February 2021. A multivariate logistic regression model was computed
to investigate the factors associated with (1) the time to recover
adequate feeding (LOFR), and (2) the hospital length of stay (LOS).
Results: 268 infants were included to assess the LOFR and 478 infants to
assess the LOS. The median age was 3.2 months (1.6-5.4) and the sex
ratio M/F was 11/20. The use of accessory muscles, nutritional support,
and RR [?] 70/min or \textless{} 30/min or apnea are associated (OR=1.5),
from virtually no association (OR=1.0) to a significant positive
association (OR=2.6) with the LOFR. Intense use of accessory muscles
(OR=3.9; 95\%CI 1.6-10.4) and ``severe'' clinical condition (OR=2.8;
95\%CI 1.7-4. 8) at admission, O2 supplementation (OR=2.0; 95\%CI
1.3-3.1) were significantly related to prolonged LOS in the multivariate
analysis. Conclusion: The clinical severity on admission may be related
to the LOFR, ranging from none to significant. Other known factors and
the new clinical severity scale proposed by the latest French guidelines
appeared to be related to the LOS in this work. Further studies are
needed to highlight these factors.%
\end{abstract}%



\sloppy


\section*{Introduction}

{\label{introduction}}

Bronchiolitis affects 30\% of infants under 24 months of age
(\textasciitilde{}480000 children) every winter in France, with a low
mortality rate (2.4-2.6 / 100000 births) \textsuperscript{1,2,3}.
However, bronchiolitis leads to a high burden that importantly impacts
the healthcare system every winter. Bronchiolitis is mostly mild and
resolves spontaneously within a few days, but in France, 2 to 3\% of the
infants will have a severe form of the disease that require
hospitalization. The average cost of hospitalization for the first
episode of bronchiolitis is 5671\textbackslash{}euro (\selectlanguage{ngerman}± 3354) and the
average length of stay (LOS) is 3 days (±3) \textsuperscript{4}. The
latest international guidelines for in-hospital management of children
with bronchiolitis recommend the use of sole supportive treatments:
feeding and/or oxygen supplementation for infants who require it. The
referral for airway clearance techniques (ACT) application is no longer
recommended worldwide since no clear benefit have been
reported\textsuperscript{3,5,6,7}.

Several features have been linked with a higher LOS including a
premature birth \textless{}36 weeks of gestational age (GA), and the
presence of comorbidities \textsuperscript{5}. Beyond these criteria,
the nutrition is a determining factor in managing the LOS of these
infants \textsuperscript{8,9}. On the other hand, the factors associated
with the time to recover adequate feeding (LOFR) are poorly known.
Nonetheless, the latest French health authority guidelines
(HAS)\textsuperscript{5} proposed a new algorithm for hospital referring
including feeding assessment further reinforcing the need to investigate
the factors related with feeding in this population.

The main objective of this study was to investigate the factors
associated with (1) the LOFR, and (2) the LOS. Among these factors, we
aimed to investigate the indications for bronchiolitis ACT referring in
our center.

\section*{Methods}

{\label{methods}}

\subsection*{Ethics statement, study design and
population}

{\label{ethics-statement-study-design-and-population}}

We conducted a single-center retrospective study that was approved by
our institutional ethics committee (n° S21031211000) and has been
declared to the Commission Nationale de l'Informatique et des Libertés
(CNIL) (MR-004 n° 2221599). According to the French law, formal consent
was not required for this type of study. We included children aged
\textless{}12 months hospitalized for bronchiolitis in Le Havre Hospital
between September 2018 to February 2021. Non-inclusion criteria were: an
age \textgreater{}12 months, a LOS \textless{}24h and multiple
hospitalizations.

\subsection*{Data collection and
outcomes}

{\label{data-collection-and-outcomes}}

Children's characteristics were collected from our institution medical
records (SILLAGE® Medical and Care Information System software). The
following reports were consulted, in order: the pediatric emergency
report, the hospitalization report and the detailed care provided
report. The data collected were as follows:

\begin{itemize}
\tightlist
\item
  Demographics: gender, age on admission, weight
\item
  Comorbidities: prematurity (\textless{} 36 GA), bronchopulmonary
  dysplasia, neuromuscular disease and congenital heart disease, chronic
  respiratory disease (childhood asthma), passive smoking, and a
  familial history of atopy (asthma, allergies).
\item
  Parameters at the Emergency Department arrival (ED): time from onset
  of symptoms to hospitalization, heart rate and Silverman score (/10),
  altered general condition (yes, no), feeding (\textless{} or
  \textgreater{} 50\% of usual feeding), respiratory rate (RR), pulsed
  oxygen saturation (SpO2\%) in room air (\textgreater{}92\%,
  90\%\textless{}SpO2\% \selectlanguage{english}[?]92\%, \selectlanguage{english}[?] 90\% or cyanosis), and accessory muscle
  use (mild, moderate, or intense).
\item
  Care during hospital stay: administration of bronchodilator and/or
  corticosteroid therapy, food support (nasogastric tube and/or intra
  veinous perfusion), oxygen support, use of ACT (at least every 48 h),
  LOFR and LOS.
\end{itemize}

\subsection*{Statistical analysis}

{\label{statistical-analysis}}

The clinical condition (severe, moderate, mild) as defined in the
HAS\textsuperscript{5} was automatically calculated according to the
extracted data, using an interface created to optimize the data
collection process in Excel - Office 365(r) software (version 2004), and
based on the aforementioned algorithm. For our main objective, adequate
feeding was defined as a percentage of the daily amount of reconstituted
milk (mL) \textgreater{}70\%; on the basis of the Schofield equation and
the latest European nutritional recommendations \textsuperscript{10,11}.
The daily amount of reconstituted milk (mL) given to exclusively
bottle-fed children was calculated on the basis of the modified Appert
standard \textsuperscript{12}. This calculation took the average growth
curve values (weight and height by sex), the caloric values per 100 mL
of reconstituted milk (first and second age) and the caloric adaptations
for infants \textless{}6 months of age (E-Table 1 ). The LOFR was then
defined as the time needed to reach a daily amount of feeding
\textgreater{}70\% of this reference. The LOFR was only calculated for
exclusively bottle-fed children, excluding breastfed (completely or
partially) infants and those who had diversified feeding. However, the
data collected for these infants were analyzable to investigate the
factors associated with the LOS.

The usual procedure for ACT referred in our center is as follows: (1) a
physician assesses the child and (2) refers to a specialist
physiotherapist for ACT evaluation and (3) provide ACT or not regarding
the clinical conditions of the child. The evaluation for ACT is repeated
every day during hospital stay. For the present study, ACT referral
(ACT+) was defined as the realization of an ACT session at least each
48h of hospitalization. A single evaluation was not rated as an ACT
session. To distinguish the characteristics of the children that
received ACT sessions during their hospital stay for bronchiolitis, the
study sample was dichotomized according to whether at least one session
of ACT was provided every 48 hours of hospital stay by a physiotherapist
(ACT+) or not (ACT-).

Patients' characteristics are reported as numbers (and/or percentages)
for categorical data; and as means (+- Standard Deviation (SD)) or median
(InterQuartile Range (IQR)) for continuous data according to the
distribution of the variables. The normality of the distribution for
each variable was assessed using the Shapiro-Wilk test. For our main
objectives, we calculated univariable logistic regressions for the
dependent variables LOFR and LOS, including the patients'
characteristics as independent variables. For this purpose, the LOFR was
transformed into a binary variable between a short length (\textless{}1
day) and a prolonged length (\selectlanguage{english}[?] 1 day) based on the median LOFR of our
population. Similarly, the LOS was also transformed into a binary
variable between a short (\textless{} 3 days) and a prolonged (\selectlanguage{english}[?] 3 days)
length, according to the average LOS for bronchiolitis in
France\textsuperscript{13,14}. A multivariate logistic regression model,
using the dummy variable technique, was then calculated by including all
the variables significantly associated (p\selectlanguage{english}[?]0.05) with each outcome, to
isolate factors independently related to prolonged LOFR and LOS. Odds
ratios (OR) and their Confidence Intervals (95\%CI) were reported.

The characteristics of the children that received ACT and those who did
not were compared using the Mann-Whitney U test or Student's t test for
continuous variables and the Fisher's exact test or the Chi2 test for
categorical variables. A p-value \selectlanguage{english}[?]0.05 was considered as significant.
All the statistical analyses were performed using GraphPad Prism
9\textsuperscript{(r)} software, version 9.0.1.

\section*{Results}

{\label{results}}

\subsection*{Study population}

{\label{study-population}}

From September 2018 to February 2021, 652 children were hospitalized
with a diagnosis of bronchiolitis. Of them, 174 were not eligible for
our study (\textbf{Figure 1} ). A total of 268 children's reports were
investigated for the predictive factors of the LOFR; and 478 were
investigated for the LOS.

The median age of our sample was 3.2 months (1.6 - 5.4), 263 children
were boys (55.0 \%) and the median weight was 5.9 kg (4.5 - 7.2).
Briefly, 94 children had a familial history of atopy (19.7\%) and 69
were born premature (14.4\%). The median LOFR was 1.0 days (0.6 - 2.0)
and the median LOS was 2.9 days (2.0 - 4.8). \textbf{Table 1} presents
the demographic and clinical characteristics of the patients, their
comorbidities, the parameters at ED arrival and course of the stay (when
available).

\subsection*{Factors associated with the LoFR and the
LOS}

{\label{factors-associated-with-the-lofr-and-the-los}}

In the univariate logistic regression model for LOFR: time delay between
the first symptoms and the ED arrival (consultation time), RR \selectlanguage{english}[?] 70/min
or \textless{} 30/min or apnea, moderate use of accessory muscles and
nutritional support requirement were significantly associated with the
LOFR (E-Table 2 ). In the multiple logistic regression model, none of
the investigated associations reached statistical significance, but the
estimate comes with uncertainty ranging from virtually no association to
a significant positive association (95\% CI for the OR: 1.0 to 2.6) for
the moderate use of accessory muscles, nutritional support and RR \selectlanguage{english}[?]
70/min or \textless{} 30/min or apnea that could be associated with the
LOFR (\textbf{Table 2} ).

In the univariate logistic regression model for LOS: age, weight,
consultation time, severe clinical condition, RR \selectlanguage{english}[?] 70/min or \textless{}
30/min or apnea, SpO2\% \textless{} 90 \% or cyanosis, intense use of
accessory muscles, nutritional and oxygen support requirement were
significantly associated with the LOS (E-Table 2 ). In the multiple
logistic regression model, the intense use of accessory muscles (OR=3.9,
95\%CI 1.6 - 10.4, p=0.004), the severe clinical condition (OR=2.8,
95\%CI 1.7 - 4.8, p=0.001), and other known variables, such as the O2
supplementation (OR=2.0, 95\%CI 1.3 - 3.1, p=0.003) remained
significantly associated with the LOS and the effect is large enough to
be worthwhile (\textbf{Table 2} ). For the consultation time (OR=1.2,
95\%CI 1.1 - 1.3, p=0.001) and the age (OR=0.8, 95\%CI 0.7 - 0.9,
p\textless{}0.01), even if they remained significantly associated with
the LOS, the effect may or may not be worthwhile.

\subsection*{In-hospital referral for
ACT}

{\label{in-hospital-referral-for-act}}

Of the 478 infants included in our study, 299 (63\%) were referred for
ACT during their hospital stay (ACT+). Children in the ACT+ group were
significantly older (median age 2.6 (1.5-5.0) vs 3.5 (1.8-5.8) years;
p=0.011) and heavier (median weight 5.3 (4.1-6.8) vs. 6.20 (5.0-7.5) kg;
p\textless{}0.01) compared to those in the ACT- group. Similarly,
children in the ACT+ group were less severe at admission and were more
often prescribed bronchodilators but required less nutritional support.
The complete characteristics of both groups are presented in
the\textbf{Table 3} .

\section*{Discussion}

{\label{discussion}}

\subsection*{Synthesis of the results}

{\label{synthesis-of-the-results}}

The present study showed that (1) the moderate use of accessory muscles,
nutritional support and RR \selectlanguage{english}[?] 70/min or \textless{} 30/min or apnea are
associated (OR=1.5), from virtually no association (OR=1.0) to a
significant positive association (OR=2.6) with the LOFR and (2) the new
severity scale proposed the HAS and other known factors such as oxygen
support appeared to be related to LOS in this work and (3) the ACT+
group were older and heavier and had a less severe clinical condition at
admission compared to the ACT- group.

\subsection*{Adequate nutrition}

{\label{adequate-nutrition}}

One major difficulty for this work was to define what constitutes
adequate infant feeding. The current guidelines agree on the importance
of maintaining adequate feeding during an episode of bronchiolitis, but
a clear definition of the nutritional monitoring and management is
lacking \textsuperscript{3,15}. We chose to define adequate feeding
according to the ratio of food intake to basal metabolic rate (BM), with
a ratio \selectlanguage{english}[?]0.7 indicating adequate nutrition based on the latest
Recommended Dietary Allowances (RDAs) of the French population and the
European guidelines on parenteral nutrition \textsuperscript{11}.
Previous studies including children hospitalized for bronchiolitis in
general ward and pediatric intensive care unit (PICU) proposed the use
of different ratios (namely 0.8 and 0.9) to detect undernourished
children based on expert committee \textsuperscript{16,17}. Furthermore,
the WHO recommends exclusive breastfeeding for children up to 6 months
of age, and dietary diversification starts at about 6 months of
age\textsuperscript{18,19,20}. As these two forms of feeding are not
suitable for mL measurement, we did not include 117 breastfed infants
(24.4\%) and 93 who had started diversification (19.5\%), which could
have impacted our results.

The HAS proposes to consider children with bronchiolitis feeding
difficulties from a cut-off of \textless{}50\% of the habitual on three
consecutive intakes \textsuperscript{5}. According to this definition,
almost all children who had feeding difficulties on admission received
feeding support during the hospital stay (namely 31\% and 28\%). This
proportion is much lower than others studies (86\% and
82\%)\textsuperscript{13,21} and could be explained by the higher
objectivity of this cut-off value, compared to the oral parental
reporting of feeding difficulties in these studies.

\subsection*{Characteristics of the study
sample}

{\label{characteristics-of-the-study-sample}}

The comorbidities previously identified as predictors of higher LOS are
congenital heart disease with shunt, chronic pulmonary disease (such as
cystic fibrosis), immune deficiency, neuromuscular disease
(polyhandicap, Down syndrome), preterm birth (\textless{}36 weeks of GA)
and corrected age \textless{}2 months \textsuperscript{5,13,22}. We did
not find any association between them and prolonged LOS, possibly
because they were not highly prevalent (1.4 to 3.5\%), except for
prematurity (14.4\%). Furthermore, compared to Gajdos et
al.\textsuperscript{13}, our lower proportions of infants exposed to
parental smoking (7\% vs. 27\%) or with atopic background (20\% vs.
40\%) could be due to the absence of systematical reporting in the
admission or medical records.

\subsection*{Respiratory distress
assessment}

{\label{respiratory-distress-assessment}}

The median Silverman-Anderson score was 2/10 at admission in the present
study, corresponding to a mild respiratory distress. This could seem
quite surprising for a cohort of hospitalized children and contradictory
compared to the HAS severity scale, who mostly rated our cohort as
moderate to severe bronchiolitis (39.9 and 51.8\% respectively). These
results can be explained by the important variability of symptoms during
the beginning or the bronchiolitis course, called the critical period by
Florin et al \textsuperscript{6}. As most infants are hospitalized
during the critical period, the clinical variability over 24 hours is
important and may lead to inconsistencies in the clinical evaluation
scores. Secondly, inter-observer reliability of the Silverman-Anderson
score has been shown to be questionable between different
caregivers\textsuperscript{23}.

\subsection*{The new severity scale (latest French
guidelines)}

{\label{the-new-severity-scale-latest-french-guidelines}}

To our knowledge, this study is the first to investigate the
relationship between this new severity scale proposed by the HAS and the
hospitalization course of these children. It appeared that this scale
was associated with the LOS in the present study, but could be
questioning, especially since the median respiratory distress score was
low. It is worth noting that the Silverman-Anderson score only rates the
respiratory distress, whereas the severity scale includes more items,
such as general condition and feeding. Secondly, it is usually advised
to measure the infant's RR over a complete minute because of the
variability of this parameter. However, in the context of a
retrospective study, the RR could have also been rated according to the
ED's monitor, which is usually higher and more variable, than the
one-minute measure. In addition, assessing the general condition of a
children is highly subjective, which could explain the discrepancies
observed in the severity ratings. Finally, RR and HR are lower during
sleep, which may influence the use of accessory
muscles\textsuperscript{24}. Unfortunately, the children state of
arousal was not reported in the medical charts investigated.

\subsection*{ACT}

{\label{act}}

In daily hospital practice, physiotherapists usually perceive the
indication for ACT in the mildest infants with bronchiolitis. Several
expert's opinion has hypothesized that children with mild or too severe
bronchiolitis would not benefit for in-hospital ACT\textsuperscript{25}.
However, ACT referral is largely based on the subjectivity of the
physician's prescription and on the physiotherapist's assessment. In our
cohort, 63\% of the infants received regular ACT during their hospital
stay, without any clinically relevant significant difference between
them, and those who did not. These results are consistent with the
previous evidence on that topic since the studies that observed a
benefit for ACT in children with acute viral bronchiolitis included
children with a moderate profile\textsuperscript{26}. Clear and
objective indications for ACT referral should be identified, as well as
the profiles of the children that would eventually have a positive
response to ACT. These two elements seem unavoidable to get rid of a one
size fits all approach that seem inappropriate, as well as an approach
only based on subjective features.

\section*{Limitations}

{\label{limitations}}

This study has several limitations. Firstly, the retrospective design of
this study may have induced bias. Also, the multivariate logistic
regression model for LOFR almost reached statistical significance for
all the factors that reached statistical significance in the univariate
analyses. This suggests that our results could have been different with
a larger sample size.

Secondly, some variables of interest may be absent or poorly reported in
the medical records, particularly some features related to the infant's
environment (parental smoking, familial history of atopy). Moreover,
other variables of interest could be influenced by the pediatric
services' usual practices, such as the prescriptions of bronchodilators.
Also, socioeconomic factors were not retrieved in our analysis, because
these variables were not reported in the medical records. Still, common
socioeconomic criteria, namely the level of education, the occupation,
the age, and the average parental income, have been shown to be
associated with hospital referral and LOS, and could explain why 9\% of
the children in our cohort were admitted with only a mild
bronchiolitis\textsuperscript{27,28}.

Thirdly, the clinical severity scale proposed by the HAS has not been
validated yet, and this study was the first to compare its results with
LOS. Furthermore, the clinical severity was retrospectively rated, which
is not the initial intended use of this scale and could have led to some
inaccuracies. Nonetheless, some criteria from this scale (namely the
assessment of respiratory distress) could be highly subjective from one
caregiver to another. Since this sole criterion is sufficient to rate
the clinical severity as ''severe'', the complete reliability of this
tool should be investigated in the future. In our study, 52\% of infants
had a ''severe'' clinical severity on admission, mainly because of a RR
''\selectlanguage{english}[?] 70/min or \textless{} 30/min, or presence of apnea'' or an altered
general condition.

Lastly, the cut-off value used in the present study to describe adequate
infant feeding was decided in the absence of a validated standard but
could have influenced our results.

\section*{Conclusion}

{\label{conclusion}}

Maintaining adequate feeding during hospital stay is a key component of
bronchiolitis care, the clinical severity on admission may be related to
the length of recover adequate feeding (LOFR), ranging from none to
significant. Other known factors such as oxygen therapy and the new
clinical severity scale proposed by the latest French guidelines
appeared to be related to the length of stay (LOS) in this work. On the
other hand, bronchiolitis airway clearance technique (ACT) referral was
not associated with neither LOFR nor LOS, suggesting that ACT use did
not modify the course of these children's stay. Further robust work is
needed to elucidate these questions.

\section*{Acknowledgements}

{\label{acknowledgements}}

Authors would like to thank the whole team of Le Havre for their support
in this study.

\section*{Informed Consent}

{\label{informed-consent}}

According to the French law, formal consent was not required for this
type of study.

\section*{Conflicts of Interest}

{\label{conflicts-of-interest}}

The authors declare no conflicts of interest.

\par\null

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