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\title{Pediatric Pulmonology Year in Review 2020: Physiology}



\author[1]{Angela Delecaris}%
\author[1]{Samantha Averill, }%
\author[1]{Jonathan Krasinkiewicz}%
\author[1]{Jessica Saunders}%
\author[2]{Clement Ren}%
\affil[1]{Indiana University School of Medicine}%
\affil[2]{Indiana University System}%


\vspace{-1em}



  
  \date{May 25, 2024}


\begingroup
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\selectlanguage{english}
\begin{abstract}
Pulmonary physiology is a core element of pediatric pulmonology care and
research. This article reviews some of the notable publications in
physiology that were published in Pediatric Pulmonology in 2020.%
\end{abstract}%



\sloppy


\textbf{Pediatric Pulmonology Year in Review 2020: Physiology}

Angela O. Delecaris MD

Samantha H. Averill MD

Jonathan Krasinkiewicz MB BCh BAO

Jessica L Saunders MD

Clement L. Ren MD MBA

\textsuperscript{1} Division of Pediatric Pulmonology, Allergy, and
Sleep Medicine, Riley Hospital for Children, Indianapolis, IN. USA

\textsuperscript{2} Department of Pediatrics, Indiana University School
of Medicine, Indianapolis, IN USA

Corresponding author:

Clement L. Ren, MD, MBA Riley Hospital for Children ROC 4270 705 Riley
Hospital Drive Indianapolis, IN 46202 Phone: 317-948-7180 FAX:
317-944-7247 Email: clren@iu.edu

Conflicts of Interests:

AOD has no conflicts of interest to disclose. SA has no conflicts of
interest to disclose. JK has no conflicts of interest to disclose. JBS
has no conflicts of interest to disclose. CLR has no conflicts of
interest to disclose.

Running Title:

Pediatric Pulmonology Year in Review 2020: Physiology

Keywords:

Multiple breath washout, Tidal breathing, Pulmonary function testing,
Forced oscillometry, Bronchopulmonary dysplasia

\emph{}

\emph{Abstract}

Pulmonary physiology is a core element of pediatric pulmonology care and
research. This article reviews some of the notable publications in
physiology that were published in Pediatric Pulmonology in 2020.

\emph{}

\emph{Introduction}

Physiology is one of the foundations of pediatric pulmonology, and in
2020 there were several important articles focused on pediatric
pulmonary physiology published in \emph{Pediatric Pulmonology} .

\emph{Forced Oscillometry}

Forced oscillometry (FO) uses measurement of pressure and flow in
response to an oscillatory pressure wave introduced at the airway
opening to measure respiratory system impedance (Z) {[}1{]}. Z is a
generalized concept of resistance that incorporates the in phase and out
of phase relationships between pressure and flow. The in phase element
of Z is resistance (R), while the out of phase element is represented by
reactance (X). R is composed of the forces associated with frictional
losses in the airways and the lung parenchyma. X is composed of an
inertive element (Xi), which represents the inertive forces of the
respiratory system, and a capacitant element (Xc), which reflects the
visco-elastic properties of the lung. At low frequencies, Xc
predominates over Xi. Because FO does not require a maximal forced
expiratory maneuver, it is easier to obtain measurements from young
children compared to spirometry. X and R at low frequency may also
reflect small airways function better than spirometric measures such as
the forced expiratory volume in 1 second (FEV1).

There is increasing evidence that the lungs are affected by diabetic
microangiopathy. Anik, et al performed FO and spirometry on children
with type 1 diabetes mellitus (T1DM) and compared the results to data
from age matched healthy controls {[}2{]}. R at 5, 10, and 20 Hz (R5,
R10, and R20 respectively) was significantly higher in children with
T1DM compared to controls, and the forced expiratory flow at 75\% of
forced vital capacity (FEF\textsubscript{75}) and between 25-75\% of
forced vital capacity (FEF\textsubscript{25-75}) were both significantly
lower. Lung function was worse in children with poorly controlled T1DM
compared to well-controlled T1DM. These results demonstrate subclinical
impairment of lung function in children with T1DM and suggest that
monitoring of lung function in T1DM should be a part of T1DM care.

Zheng, et al studied whether impulse oscillometry (IOS), a form of FO,
and the fraction of exhaled nitric oxide (FeNO) could be used to predict
future asthma exacerbations in preschool children {[}3{]}. They were
able to identify a cutoff value for the area under the reactance curve
(AX), a measure of total low frequency X, that predicted future loss of
asthma control, while FeNO did not have strong predictive value in this
patient population. Their report suggests that IOS could be used to
monitor preschool children for future risk of asthma exacerbation.

Lundberg, et al investigated the feasibility and correlation between
spirometry and IOS in 6 year old children born extremely premature
{[}4{]}. The success rate of IOS was significantly higher in both term
and preterm children compared to spirometry (93\% vs 60\%). There was
moderate correlation between spirometry measurements and IOS
measurement, suggesting that IOS could be considered as an alternative
test in children who cannot perform spirometry.

Veneroni, et al used FO to compare respiratory mechanics in preterm
infants treated with continuous positive airway pressure (CPAP) versus
CPAP with sustained inflations of 25 cmH2O for 15 seconds {[}5{]}.
Infants presented with highly heterogeneous degrees of lung aeration at
birth, limiting their ability to use FO to assess ventilation
strategies. However, this pilot study did demonstrate the feasibility of
obtaining FO measurements at birth in preterm infants.

\emph{Multiple Breath Washout}

The multiple breath washout (MBW) technique can be used to assess
ventilation inhomogeneity, which can be seen in a variety of pediatric
lung diseases, most notably cystic fibrosis (CF) {[}6{]}. MBW can be
performed either by washing in a tracer gas, such as sulfur
hexafluoride, and then washing the tracer gas out with ambient air or
washing out the resident nitrogen (N\textsubscript{2}) in the lungs with
100\% oxygen. The lung clearance index (LCI) is the most commonly used
measure derived from N\textsubscript{2} MBW, and it represents the
number of lung turnovers required to washout resident
N\textsubscript{2}from the lungs down to 2.5\% of the original
concentration; a higher LCI indicates increased ventilation
inhomogeneity. In addition to LCI, other measures derived from MBW
include LCI\textsubscript{5.0}, where N\textsubscript{2} is washed out
to 5\% of the original concentration, slope of phase III indices, and
moment ratio analysis.

Parisi, et al performed MBW and spirometry in a group of childhood
cancer survivors and matched healthy controls {[}7{]}. They found that
LCI was higher in these children compared to healthy controls, but this
difference was not statistically significant; and there was no
difference in spirometry measurements. There was a significant
correlation between years following chemotherapy and increased LCI.
Their results suggest that the chemotherapy used to treat childhood
tumors may have less pulmonary toxicity than previously expected, at
least during childhood. The increase in LCI over time suggests that LCI
could be used to non-invasively assess pulmonary fibrosis but larger
prospective studies are needed.

Gambazza, et al evaluated the association of LCI with exercise capacity
in patients with CF {[}8{]}. LCI was significantly higher in patients
with exercise intolerance, but it was also higher in some patients with
normal exercise tolerance and normal to moderate airflow obstruction. No
association was found between predicted peak work and LCI, but there was
a significant association between peak work and nutritional status,
airflow obstruction, and chronic \emph{Pseudomonas}
\emph{aeruginosa}infection. Based on these findings, providers should
not assume that patients with normal exercise tolerance do not have
early lung disease.

Irving, et al compared MBW results between children with severe
treatment resistant asthma (STRA), difficult asthma (DA) and healthy
controls {[}9{]}. LCI was significantly higher in the patients with STRA
compared to those with DA and controls but there was no difference
between DA and controls. FeNO and LCI showed significant improvement
following parenteral steroids. These results suggest that distal airways
disease is worse in patients with STRA and can sometimes be improved
with parenteral steroids. The improvement in FeNO and LCI suggests these
patients with STRA may have distal airway eosinophilic inflammation that
may not respond to inhaled corticosteroids. These results suggest that
FeNO and LCI may be useful in monitoring treatment response in patients
with STRA.

Other studies of MBW focused on use of outcome measures other than LCI
and comparison of difference MBW devices. Arigliani, et al compared the
conduction-dependent contribution to ventilation inhomogeneity
(S\textsubscript{cond}), the diffusion-convection interaction-dependent
inhomogeneity (S\textsubscript{acin}), LCI, spirometry, and transfer
capacity of the lung to carbon monoxide (TLCO) in children born at
\textless{}28 weeks gestational age (GA) {[}10{]}.
S\textsubscript{cond}was abnormal in about one third of children while
LCI and FEV1 were only abnormal in 18\% and 14\% respectively. They did
not identify any significant difference in S\textsubscript{comd} between
infants born prematurely with BPD compared to those without BPD. No
significant difference was observed in S\textsubscript{acin} between the
premature infants and the control group and no significant difference
was found when comparing those with BPD to those without BPD. Finally,
extremely preterm children had lower TLCO compared to controls,Although
moment ratios correlated with pulmonary symptoms, high variability
limits its utility in the clinical setting. These results suggest that
LCI\textsubscript{5.0} can be used to track disease progression in young
children with CF. Compartment analysis (CA) allows partitioning of MBW
data into slower and faster ventilating units. Skov, et al applied CA to
MBW testing in children with CF {[}12{]}. Because CA requires an
extremely regular breathing pattern, it could only be successfully
performed in 53\% of children with CF. However, CA did correlate with
other MBW measurements, such as LCI. Further research is needed to
determine the clinical value of CA. Isaac, et al used a lung model to
compare functional residual capacity (FRC) and LCI measured with 2
different MBW devices and body plethysmography {[}13{]}. Not only were
there differences in these measurements using these 3 different methods,
but for one device LCI decreased with age. These results indicate that
MBW data obtained on one device cannot be directly compared to data from
other devices.

\emph{Reference Equations}

Normal reference values are critically important for interpreting the
results of pulmonary function tests (PFTs), but data in non-White
populations are lacking. Several reports in \emph{PediatricPulmonology}
this past year sought to fill this knowledge gap. Al Querem et al.
evaluated the applicability of the 2012 Global Lungs Initiative (GLI)
reference equations in 582 Jordanian children ages 6-13 year-old
{[}14{]}. The GLI equation for Caucasians demonstrated a reasonable fit
to the data collected in this study and was more suitable than the GLI
equation for other ethnic groups, and equations derived from other
studies conducted in Arabic counties. These results differ from
previously reported values in Jordanian adults which showed that the GLI
equations for other ethnicities rather than GLI Caucasian equation were
better correlated, and demonstrate the importance of identifying
age-specific reference equations.

Reference values for infant PFT's have been reported but there is a lack
of information about racial or ethnic differences. The aim of a study by
Kosma et al was to estimate the extent to which previously published
reference equations for infant spirometry could be implemented in a
cohort of Swedish term, healthy infants {[}15{]}. Tidal volume and
raised volume rapid thoracoabdominal compression (RVRTC) maneuvers were
performed on 91 term infants. Height and weight in Swedish infants were
above average compared to other infant PFT reference cohorts, and this
led to an underestimation of lung function measured by infant spirometry
in the youngest age group and an overestimation in the older infants
using previously published infant PFT reference data.

Not only spirometry reference values but also reference equations to
calculate diffusing capacity of carbon monoxide (DLCO) have been tested
for their applicability in different racial groups. A study by Dridi et
al. measured nitric oxide/carbon monoxide transfer in 118 healthy
Tunisian males ages 8-14 {[}16{]}. They confirmed previous observations
that height and body weight are key individual predictors of DLCO and
that alveolar volume (VA) was related with both height and weight. Their
values for DLCO and VA were similar to those found by Kim et al in both
Caucasian and African American populations {[}17{]}.

Normal reference data for maximal voluntary ventilation (MVV) in
children have only been reported for limited ethnic and racial
populations. Silva et al. obtained MVV data from children in S\selectlanguage{ngerman}ão Paolo,
Brazil {[}18{]}. MVV in their cohort differed from results obtained in
other populations, highlighting the need and importance to obtain normal
reference data for multiple different populations.

Although not the focus of studies published in
\emph{PediatricPulmonology} in 2020, the issue of incorporating race
into PFT reference equations has grown in prominence and importance in
the past few years. Although genetic ancestry contributes to differences
in PFT values in different populations, race is a complex construct that
incorporates more than just genetic ancestry, and includes cultural and
social factors {[}19{]}. Furthermore, race serves as a proxy for social
determinants of health that may affect lung function. It is likely that
in the future, we will see studies in \emph{PediatricPulmonology} that
more directly incorporate genetic ancestry into predictive equations
rather than phenotypic race {[}20{]}.

\emph{Tidal Breathing Studies}

Tidal breathing analysis (TBA) is an attractive method of respiratory
function testing because it can be done without the need for sedation or
the requirement of forced expiratory maneuvers {[}21{]}. TBA can be
performed using a face mask and pneumotachometer, but this can be
challenging to apply in infants since it requires the infant to maintain
a seal over the nose and mouth with the mask, which can also potentially
alter infant breathing patterns. Electromagnetic inductance
plethysmography (EIP) measures changes in the electromagnetic field
created by tidal breathing while wearing a metallic vest through which a
low voltage is applied. Sautter, et al used EIP to perform TBA in a
cohort of 36 infants with bronchiolitis {[}22{]}. EIP was successfully
performed in 80\% of the infants, and a significant increase in the
ratio of the total expiratory time over the inspiratory time (Te/Ti) was
observed after inhalation of normal saline. The ratio of the time to
peak expiratory flow over total expiratory time (Tptef/Te) decreased
after administration of nebulized normal saline, but this change was not
statistically significant. This study demonstrates the feasibility of
using EIP for TBA and suggests that further study of the physiologic
effects of inhaled normal saline in bronchiolitis are warranted.
Traditionally TBA has been done manually, which is a time consuming and
laborious process. A study by Gomes et al. compared two computing
systems, AutoCAD and MATLAB, in their ability to obtain automated TBA
data {[}23{]}. Thoracoabdominal area averages calculated with both
systems were comparable, but MATLAB required less time and less user
training to complete. They suggest that it could be used in the clinic
setting to calculate or derive tidal volume measurements.

\emph{Physiologic Outcomes of Prematurity}

Bronchopulmonary dysplasia (BPD) is the most common short-term
complication of premature birth, and infants with BPD can continue to
have impaired lung function into adulthood {[}24{]}. Although there have
been studies comparing lung function between infants with BPD and those
without this diagnosis, there are limited data in preterm infants who
are born small for gestational age (SGA). Kim, et al investigated the
differences in airway obstruction in term, healthy neonates and preterm
neonates with and without BPD using MBW and TBA {[}25{]}. No significant
differences in Tpef/Te were observed between the term infants, preterm
infants with mild/moderate BPD, and preterm infants with severe BPD.
However, Tpef/Te was significantly lower in the severe BPD infants
compared to the mild/moderate BPD infants, consistent with worse airway
obstruction in the former group. LCI was significantly increased in
preterm infants compared to term ones, but it did not vary between the
infants with no BPD, mild BPD, or severe BPD, even when accounting for
SGA status. SGA infants with BPD had a significantly lower Tpef/Te than
average for GA matched infants, showing a negative effect of SGA in BPD.
These results suggest that SGA status is a risk factor for worse airway
obstruction in infants with BPD.

Sex differences in lung function and structure are well known, but
studies of sex differences in lung mechanics of preterm neonates are
lacking. Kim, et al measured airway pressure and flow~in male and female
neonates requiring mechanical ventilation for neonatal respiratory
distress syndrome, and then used these data to generate a single
compartment model to calculate specific elastance (E\textsubscript{S})
{[}26{]}. Male infants had higher~E\textsubscript{S} compared to female
infants of matched gestational age and less breath-to-breath variability
in E\textsubscript{S}.~ This study suggests that ventilator strategies
may need to take sex into account, but further studies with larger
cohorts are needed.

\textsubscript{0.5}. There was no significant difference in any other
forced expiratory flow measurements, FRC, or respiratory system
compliance between the caffeine treated or untreated groups. When
further stratified by BPD diagnosis, differences in lung function were
only seen in infants without BPD who had received caffeine. These
results indicate that caffeine may have beneficial effects on lung
function in addition to its effect on reducing risk of BPD.

\emph{Other Physiologic Studies}

A study by Fabi et al. examined short- and long-term changes in
respiratory mechanics after palliative or corrective surgery in 168
infants and toddlers with congenital heart disease {[}28{]}. They found
that these patients demonstrated normal basal respiratory function but
decreased exercise capacity. This decrease in exercise capacity was more
pronounced in patients who underwent total cavopulmonary connection
(TCPC) procedures. This suggests the need to conduct respiratory
monitoring on patients with TCPC more closely and for longer than those
with non-TCPC procedures. They also found that a higher age at surgery
but prior to 24 months was associated with better respiratory outcomes
which suggests that increased development of the lung parenchyma prior
to intervention will lead to improved respiratory outcomes
post-operatively.

Sivieri, et al used a preterm infant lung model to evaluate the effects
on end tidal CO\textsubscript{2} (ETCO2) when high frequency oscillation
is superimposed on bubble CPAP (BCPAP) {[}29{]}. They found that there
is improved CO\textsubscript{2} clearance when high frequency
oscillation is applied to BCPAP, and that this effect was more
pronounced when the model mimicked lung disease in a preterm infant
compared to normal infant lung mechanics. This improvement was not
dependent on BCPAP pressure, CO2 clearance was significantly improved
for both lung models as a function of increased frequency and lower
respiratory rate. These results support conducting a clinical trial to
assess the effect of superimposed high frequency oscillations in infants
receiving BCPAP.

Extrathoracic high frequency chest compression (HFCC) using an
inflatable vest is frequently used for airway clearance in patients with
mucociliary abnormalities, such as CF. Weiner, et al sought to determine
if HFCC augments ventilation by measuring end-tidal CO2 (ETCO2) after
HFCC was performed at varying frequencies (Hz)in a cohort of 15 people
with CF who were experiencing a pulmonary exacerbation {[}30{]}. ETCO2
values were significantly lower at all Hz compared to no treatment. This
remained the same when adjusting for patient specific factors such as
age, sex, body mass index, baseline FEV1 and respiratory rate.
Increasing Hz produced a small, but significant improvement in ETC02
clearance. These results demonstrate that HFCC increases clearance of
CO2 in a frequency dependent manner. Further research is needed to
determine the clinical importance of this finding.

Formulas used to calculate the appropriate pediatric tracheostomy or
endotracheal tube (ETT) size have incorporated age, weight, and height,
but there are no formulas that incorporate airflow resistance or
cross-sectional area of the inner cannula. Since resistance varies by
the 4\textsuperscript{th} power of the radius, small changes in ETT
lumen diameter can have marked effects on tube resistance (R) {[}31{]}.
Khan and Baker applied the Hagen-Poiseuille equation for R under laminar
flow conditions to calculate the R in different ETT and tracheostomy
tubes based on tube inner diameter and cross-sectional area {[}32{]}. A
large decrease in R was seen when tube diameter was increased by as
little as 0.5mm in ETTs that would likely be used for patients
\textless{}1 year of age. This effect was not as significant in larger
tube sizes. When invasive mechanical ventilation is required, and a
patient can safely tolerate upsizing of ETT or tracheostomy tube, this
should be considered to lower airway resistance and improve airflow
dynamics.

\emph{Summary}

Pulmonary physiology continues to play an important role in pediatric
pulmonology care and research, and we anticipate that future issues
of\emph{Pediatric Pulmonology} will continue to contain reports of
interest and importance on this topic.

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