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\begin{document}

\title{Anatomical and Functional Assessment of Upper Airway Performance Using
Innovative NasoOroSpirometer and Cone Beam Computed Tomographic
Diagnostic Devices in Children with Adenoid Hypertrophy -- Observational
Study}



\author[1]{Edyta Zomkowska}%
\author[2]{Sylwia Grzybowska-Detka}%
\author[3]{Magdalena Zakrzewska}%
\author[4]{Jerzy Romaszko}%
\author[5]{Robert Barański}%
\author[6]{Andrzej Zając}%
\author[7]{Hanna Zajączkiewicz}%
\author[7]{Szymon Nitkiewicz}%
\author[7]{Andrzej Kukwa}%
\affil[1]{Clinical University Hospital in Olsztyn}%
\affil[2]{CMKP}%
\affil[3]{ Independent Public Centre for Tuberculosis and Lung Diseases Treatment}%
\affil[4]{University of Warmia and Mazury in Olsztyn School of Medicine}%
\affil[5]{AGH University of Science and Technology}%
\affil[6]{Military University of Technology}%
\affil[7]{University of Warmia and Mazury in Olsztyn}%


\vspace{-1em}



  
  \date{May 27, 2024}


\begingroup
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\selectlanguage{english}
\begin{abstract}
Introduction. Adenoid hypertrophy leading to upper airway blockage is
the most common cause of sleep apnoea syndrome in children. Moreover,
the following disturbances can occur: normal speech resonance
impairment, middle ear ventilation difficulties, and the development of
an abnormal oral breathing pattern. Abnormal craniofacial growth and
occlusal abnormalities can be observed as well. Objectives.The aim of
the study was to confirm the relationship between respiratory disorders
with the impaired upper airway patency resulting from reduced
nasopharyngeal space. Moreover, an attempt was made to validate a new
medical device, a NasoOroSpirometer, for diagnosing respiratory
disorders resulting from adenoid hypertrophy. Design and Setting The
NasoOroSpirometer is made up of three anemometric sensors (two nasal and
one additional oral sensor) and is used to measure the airflow through
the upper airways (UA). A measurement of the flow of air simultaneously
through both nasal orifices was carried out in 105 children aged 4-8
years. The values obtained included the number of inhalations per
minute, the inspiratory time and the inhalation volume. Results and
discussion. The study demonstrated that children with adenoid
hypertrophy had a statistically significantly lower number of
inhalations through the nose than children from the control group. The
current results demonstrated no statistically significant difference
between the volume and the number of inhalations in both a combined
analysis and in one analysis conducted separately for each nasal
passage. The demonstrated statistically significant difference is most
probably due to the oral compensation for the inefficient nasal
respiratory pattern. A~NasoOroSpirometric examination can be a screening
tool in the assessment of UA patency disorders and an indicator for the
eligibility for instrumental or imaging examinations.%
\end{abstract}%



\sloppy


Key points:

- Description of application of innovative devices and methods in the
diagnostic process of impairments arising in upper respiratory tract in
children

- NasoOroSpirometry indicates presence of anatomic anomalies in UA based
on functional examination

- CBCT confirms anatomic and functional impairments observed in nasal
spirometry

- Resection of hypertrophied adenoid in children increases quality of
life

- Both previously mentioned methods are easy to perform, completely
safe, quick and non-invasive. Abstract

Introduction. Adenoid hypertrophy leading to upper airway blockage is
the most common cause of sleep apnoea syndrome in children. Moreover,
the following disturbances can occur: normal speech resonance
impairment, middle ear ventilation difficulties, and the development of
an abnormal oral breathing pattern. Abnormal craniofacial growth and
occlusal abnormalities can be observed as well. Objectives.The aim of
the study was to confirm the relationship between respiratory disorders
with the impaired upper airway patency resulting from reduced
nasopharyngeal space. Moreover, an attempt was made to validate a new
medical device, a NasoOroSpirometer, for diagnosing respiratory
disorders resulting from adenoid hypertrophy.

Design and Setting. The NasoOroSpirometer is made up of three
anemometric sensors (two nasal and one additional oral sensor) and is
used to measure the airflow through the upper airways (UA). A
measurement of the flow of air simultaneously through both nasal
orifices was carried out in 105 children aged 4-8 years. The values
obtained included the number of inhalations per minute, the inspiratory
time and the inhalation volume.

Results and discussion. The study demonstrated that children with
adenoid hypertrophy had a statistically significantly lower number of
inhalations through the nose than children from the control group. The
current results demonstrated no statistically significant difference
between the volume and the number of inhalations in both a combined
analysis and in one analysis conducted separately for each nasal
passage. The demonstrated statistically significant difference is most
probably due to the oral compensation for the inefficient nasal
respiratory pattern. A NasoOroSpirometric examination can be a screening
tool in the assessment of UA patency disorders and an indicator for the
eligibility for instrumental or imaging examinations. Introduction

Adenoid hypertrophy in children is the most common cause of impaired
upper airway patency {[}1{]}. Different degrees of airway obstruction
may lead to the development of an abnormal pattern of breathing through
the mouth (oral respiratory pattern). Impaired ventilation and exchange
of air through the nose can increase the risk of secretory otitis media
or chronic rhinitis {[}2{]}. A consequence of the latter is the
obstruction of posterior nares, and the impaired patency of the
Eustachian tube pharyngeal orifice. In this way, a classical ''vicious
disease circle'' is initiated. A change in the breathing pattern can
cause numerous abnormal consequences {[}3{]} -- it is a causative factor
of adenoid hypertrophy, palatine tonsil hypertrophy, and hypertrophy of
the entire pharyngeal lymphatic system {[}4{]}. Consequently, it can
lead to the manifestation of sleep apnoea syndrome (SAS) in children.
Sleep disturbances with nocturnal arousals and sleep shallowing as well
as sleep fragmentation occur {[}5, 6{]}. This results in impaired body
recovery during sleep and excessive daytime sleepiness. Untreated SAS
can lead to serious consequences, such as growth disorders, the
development of hypertension, cardiac arrhythmias and even cognitive
function disorders, e.g. ADHD (attention-deficit hyperactivity disorder)
{[}1, 7, 8{]}. Adenoid hypertrophy is a mechanical obstruction resulting
in the occlusion of the airways, particularly during sleep, and is one
of the risk factors for the syndrome concerned.{[}9{]}

An examination that enables an objective assessment of the UA is
cone-beam computed tomography (CBCT). This technique, currently widely
applied by dentists and maxillofacial surgeons, is characterised by low
radiation exposure when imaging both osseous and soft tissue structures.
CBCT enables an objective 3D visualisation of the UA, the accurate
determination of the absolute size of the adenoid, and the performance
of its measurements in relation to the total nasopharyngeal volume. The
examination also enables the imaging of the nasal sinuses, the volume of
the petrous pyramids, and an assessment of the middle ear and the
mastoid cells. The latter in the presence of adenoid hypertrophy, are
the cause of impaired Eustachian tube patency, which leads to the
abnormal development of petrous pyramid air spaces. In the sagittal
plane of CBCT examination, the nasopharyngeal space and the location of
the soft palate in relation to the posterior pharyngeal wall and the
cervical spine can be assessed by performing M\selectlanguage{ngerman}üller's manoeuvre. This
procedure, the reverse of a Valsalva manoeuvre, involves closing the
nostrils with fingertips during inhalation, which raises the soft palate
and separates the nasal part from the oral part of the throat. In cases
of lymphatic hyperplasia, the airflow through the upper airways within
individual parts of the throat is then obstructed. The examination
reveals the collapse of the posterior pharyngeal wall, which is
diagnostically important in terms of the cause of obstructive apnoea
{[}10, 11{]}. CBCT enables the visualisation of the discussed region and
the avoidance of complications, e.g. an atlantoaxial subluxation during
adenoidectomy, otherwise known as Grisel's syndrome {[}12, 13{]}. CBCT
examination is relevant in the diagnostic process, particularly at the
stage of qualifying for either surgical treatment
(adenoidectomy/adenotonsillectomy) or non-invasive treatment, e.g.
intranasal steroid therapy. Due to the low radiation dose, the
examination is also carried out when assessing the progress of the
proposed treatment {[}14, 15{]}.

Methodology

Study population

This cohort study was conducted during a period of 2 years at {[}blinded
for review{]}. The study participants comprised 105 children aged 4-8
years. In the group of the examined subjects: in 80 children, adenoid
hypertrophy was revealed, while 25 children constituted a potentially
healthy (control) group. In 80 children with symptoms characteristic of
adenoid hypertrophy, a CBCT examination was conducted in order to
visualise the anatomical structures of the upper airways The CBCT
examination results provided eligibility for an adenoidectomy surgery
and allowed the children to be assigned to individual groups according
to the classification proposed by M.P. Major {[}16{]}.

I. children with the adenoid occupying up to 25\% (1/4) of the
nasopharyngeal volume,

II. patients with the adenoid occupying up to 50\% (1/2) of the
nasopharyngeal volume,

III. patients with the adenoid occupying up to 75\% (3/4) of the
nasopharyngeal volume.

All 105 study patients were examined using a NasoOroSpirometer.

NasoOroSpirometry

A diagram of the device is provided in Fig. 1.

Fig. 1. A diagram and an image of the device: 1 -- a mask with separate
parts for the nose and the mouth, 2 -- sensor casings, 3 -- thermal
anemometric sensors of the airflow, 4 -- power supply and signal cables,
5 -- a set of filters to condition the analogue signal, 6 -- a data
acquisition card, 7 -- a PC computer. The device houses three
constant-temperature anemometers connected by cables to a system
conditioning the signal being measured. The voltage obtained in the
measurements is archived in the PC's memory by means of the data
acquisition card. The measuring sensors are made of tungsten wire with a
diameter of 7.5 \selectlanguage{greek}µ\selectlanguage{english}m. The measuring fibres are placed in separate
measurement canals -- for the nasal canals with a diameter of 11 \selectlanguage{greek}µ\selectlanguage{english}m and
the wall thickness of 2 mm in the nasal sensors, and in the ''oral''
canal with a diameter of 24 mm and the wall thickness of 3 mm. In each
sensor, the casing is 30 mm long. The diameter of the measurement canals
was selected so as not to suppress the airflow in the respiratory
passages. The thermal anemometer fibre inside the casing is heated to
200\textsuperscript{o}C. The measuring elements were pre-calibrated
using known values of the airflow through the measuring system {[}17{]}.
Each sensor was selected in consideration of the upper airflow
measurement range at the level of 1,000 cm3/sec. An adult individual
takes approx. 16 breaths per minute, with one (inhalation and
exhalation) lasting for approx. 2 seconds. The tidal volume of an adult
is approx. 500 cm3, i.e. the volume of the air flowing in one second
(inhalation/exhalation) is 250 cm3, i.e. the average volume of a normal
quiet breath. The number of measurements per unit of time at an assumed
time of inhalation/exhalation should enable the reliable reconstruction
of the monitored flow {[}18{]}. The recorded measurements were analysed
using dedicated Breath Analyzer software developed for this purpose. The
first step of the analysis involved the automatic identification of the
onset of every inhalation. Where the automatic identification was
doubtful, it was possible to make manual corrections of the analysed
part of the examination. What was important in the analysis was the
detection of the onset of each inhalation. The areas between the
inhalation and exhalation starting points were counted as consecutive
breaths. The program enables the recording and assessment of the number
of breaths per minute and the average time and volume of the inhalation
and exhalation {[}17{]}.\textbf{Fig. 2.} A record of NasoOroSpirometric
examination showing the flow values, determined by individual orifices
in the Breath Analyzer program (own materials).

The start of recording was preceded by the recording of the child's
personal data, signing the parents' consent for the examination, and the
description of the patient's history and clinical examination. The
examination was conducted in a sitting position with at least one parent
present. During the examination, the respiratory process was recorded in
real-time. The measurements were read using a dedicated NoseSpirometer
program, and the examination was analysed using the Breath Analyzer
program. The NasoOroSpirometric examination measured the flow of air
simultaneously through both nasal orifices. The following values were
obtained: the number of inhalations, the inspiratory time per minute,
and the inhalation volume.

Statistical analysis

A statistical analysis was carried out using the Statistica software
(data analysis software system), version 13.3. Due to the lack of normal
distribution of the study group, the statistical analyses were conducted
using nonparametric Kruskal-Wallis tests. The statistical significance
was assumed at p \textless{} 0.05. STROBE reporting method has been used
to summarize the results of this study.

Ethical statement The study was conducted based on the consent issued by
the {[}blinded for review{]} Resolution No. 16/2017 of 25 April 2017.

Results

The study group of patients (105 subjects) aged 4-8 years was divided
into four groups depending on the CBCT examination result.

Group I comprised 19 (18\%) patients, group II - 21 (20\%) patients,
while group III - 40 (38\%) patients. The control group IV comprised 25
(24\%) patients.

\textbf{Table 1} . Analysis of age in individual study groups. A
statistical comparison between the study group and control group, and an
analysis of the results for the number of inhalations in study groups
(I, II, III) in relation to the control group (IV) The tests on study
subjects divided into the study group (comprising three groups: I, II,
and III) and the control group IV confirmed that the study was conducted
on children for whom the age difference was not statistically
significant. The LN and RN data helped demonstrate a statistically
significant difference between the study group and the control group in
terms of the number of inhalations per minute. For the analysed cases,
the p-value did not exceed 0.004. Children with adenoid hypertrophy had
a statistically significantly lower number of inhalations through the
nose than children from the control group.

\textbf{Table 2.} An analysis of the average inspiratory time per minute
in individual study groups, and an analysis of the average inhalation
volume in the study groups.

Discussion

The methods of accurate determination of nasal resistance, described in
the literature, can be divided into two groups: methods for measuring
the passive flow (passive rhinomanometry) and methods based on the
measurement of the airflow during active breathing (active
rhinomanometry) {[}19, 20{]}. The measurement involves pumping a
specified volume of air at a pre-determined speed while measuring the
differential pressure. It can be assumed that the differential pressure
value is proportional to the nasal resistance. Currently, passive
rhinomanometry is rarely applied. It is, however, useful in cases where
the patient's cooperation is not possible, e.g. in young children
{[}21{]}. A number of studies performed rhinomanometric measurements in
children and adults in reference to chronic nasal patency disorders and
adenoid hypertrophy {[}22-24{]}. A study by Zicari et al. included 71
children aged 6-12 years with symptoms of upper airway obstruction, who
were diagnosed with ''chronic mouth breathing''. This research project,
using a rhinomanometric examination, found normal nasal airflow in 19
(26.8\%) children, while indicating nasal obstruction in 52 (73.2\%)
children. A follow-up rhinomanometric examination, performed following
intranasal xylometazoline administration, confirmed the presence of
nasal obstruction in 29 (55.7\%) patients {[}24{]}. Researchers
emphasise that rhinomanometry performed in children with adenoid
hypertrophy can contribute to the better qualification of children for
surgery.

The method, however, has serious disadvantages of which one should be
aware of when employing it {[}25{]}:

1. the patient must hold their breath during the measurement,

2. in certain cases, the flow of the air being forced in can cause
unpleasant sensations and involuntary movements of the soft palate,
which leads to the inclusion of the resulting resistance value into the
measurement result,

3. during the measurements using alternating-direction flow, significant
differences are found between the force-in phase and the suction phase,

4. due to the use of nozzles, during each measurement, the air stream
can be forced in at a different angle, which contributes to low
repeatability of the examination,

5. the result of measurement by the passive rhinomanometric method has a
form of a single numerical value that provides no information on the
nasal flow dynamics. Moreover, the insertion of the nozzle into the
vestibule of the nose during the examination prevents the assessment of
the resistance of this upper airway section and the so-called ''nasal
valve'' located between the vestibule and the proper nasal cavity.

An alternative to the rhinomanometric examination is NasoOroSpirometric
examination conducted by the authors. The examination focuses on an
analysis of airflow and the calculation of inspiratory volumes while
departing from the measurement of pressures (which is characteristic of
rhinomanometry).The difference between both procedures also lies in the
elimination of non-physiological behaviours of the examined patient
during the rhinomanometric measurement.

The examination does not absorb the patient's attention, apart from the
mask placement, which is not very inconvenient, and its effect on the
respiratory process is negligible.

The results obtained in the current study show that in patients with
adenoid hypertrophy, the number of inhalations per minute is lower than
in healthy children (Table 1). However, a hypertrophied adenoid has no
statistically significant effect on the inspiratory time or volume
(Table 2). It was demonstrated that in the group of patients with
significant adenoid hypertrophy (40 children in group III), the number
of inhalations was lower than that in the group of 25 potentially
healthy children (group IV). During the examination of the children, no
measurement of the flow through the mouth was recorded. At the time the
examination was recorded, the oral sensor was inactive (switched off).
Young children tolerate the oral measurement poorly and are much less
cooperative with the oral sensor during the examination. Moreover, a
mask with three openings will most likely prove useful for adults, e.g.
patients with suspected obstructive sleep apnoea, where it will serve as
an examination complementary to polysomnography (under study). This
simple difference in the number of nasal breaths in the study group as
compared to the control group results, most probably, from the
compensation of the nasal respiratory pattern with the oral pattern by
children with adenoid hypertrophy. Apart from the elimination of the
airway obstruction symptoms, adenoid removal results in an increase in
the nasopharyngeal space. Furthermore, it contributes to the restoration
of patency of the posterior nare region. By performing adenoidectomy,
the proper respiratory pattern and volume can be restored, and thus the
number of inhalations by the nasal pattern at rest is increased.
{[}18{]}. Imaging confirmation of the results of a screening
NasoOroSpirometric examination can be provided by CBCT, which enables
the precise determination of anatomical obstructions impairing the
airflow through the upper airway {[}15{]}.

Conclusions

The examination using a NasoOroSpirometer is easy to perform, completely
safe, quick and non-invasive, with the initial results being displayed
while the examination is being recorded. It can serve as a screening
tool in assessing UA patency disorders and be helpful when qualifying
patients for instrumental or imaging examinations.

The results indicated that a statistically lower number of inhalations
are a result of compensatory mouth breathing. The obtained values of
inspiratory volumes, analysed using the Breath Analyzer program, can be
compared with a cone-beam computed tomographic examination of the upper
airways. Disclosure Authors have no conflicts of interest.

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