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14 Upper Airway Evaluatıon: Dıagnostıc Clues fromUpper Respıratory Tract
25. Yellon RF, Goldberg H.Update on gastroesophageal reux disease in pediatric airway disorders. Am J Med. 2001;111(suppl 8A):78S–84S.
26. Hoa M, Kingsley EL, Coticchia JM. Correlating the clinical course of recurrent croup
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2008;117:464–9.
197
Preschool Lung Functıon Testıng
andtheUpper Respıratory Tract
SedaTunca, ÖzgeYilmaz, andEnricoLombardi
Abbreviations
GLI Global Lung Function Initiative
FOT Forced Oscillation Technique
FRC Functional residual capacity
Raw Resistance airway
RV Residual volüme
TLC Total lung capacity
15.1 Introduction
15
The essential anatomical and functional differences between the pediatric and adult
airways contribute to understanding the various respiratory symptoms and the differences during disease. Knowing the essential features of pediatric airways is helpful in the prevention, management, and treatment of acute and chronic diseases of
the respiratory tract. The developmental changes in the structure of respiratory
tracts during childhood should also be paid attention to. The age-related variations
should be taken into consideration in the evaluation of airway function in the light
of united airway theory, and a combined evaluation should be performed considering anatomical, physiological, and chemical differences.
S. Tunca · Ö. Yilmaz (*)
Department of Pediatric Allergy, School of Medicine, Manisa Celal Bayar University,
Manisa, Türkiye
E. Lombardi
Pediatric Pulmonary Unit, Meyer Children’s Hospital, Florence, Italy
e-mail: e.lombardi@meyer.it
© The Author(s), under exclusive license to Springer Nature
Switzerland AG 2024
H. Yüksel et al. (eds.), Pediatric Airway Diseases, Comprehensive ENT,
https://doi.org/10.1007/978-3-031-74853-0_15
199
200
S. Tunca et al.
Upper airways have a changing and developing structure with age, particularly in
the preschool period and in younger children. Children have a relatively smaller oral
cavity and larger tongue in the upper airway in comparisonto adults. This condition
should be emphasized as an indicator of the fact that obstruction risk is higher and
nasal obstruction may lead to more serious consequences in children. Epiglottis is
longer and weaker, it may easily cause obstruction if it is edematous. Tonsil and adenoid tissues rapidly grow in childhood and may cause serious obstructions in case of
infections resulting in edema. Since the larynx and glottis are located in the upper
aspect of the neck in children, aspiration risk in children is higher than in adults.
Similar differences between children and adults also apply to lower airways. Therefore,
it is of utmost importance to take all these differences into consideration when measuring airway function in children and prefer the most appropriate airway measurement technique for the selected age group with respect to diagnosis and treatment.
The lower respiratory tract in children has many differences compared to adults.
Since the wall thickness of the bronchi is thinner, it may cause easy collapse of the
lumen during inspiration. On the other hand, the length of the trachea is shorter in
children than in adults, which facilitates the access of inammation to the lower
airways. Abdominal breathing is predominant in children, especially in the newborn
and early childhood, due to the weak intercostal muscles and the fact that the cartilaginous part of the thorax is more than the bony part. In addition, a signicant
increase in the number of alveoli is observed from newborn to adulthood until the
age of eight to ten. Especially in newborns and early childhood, abdominal breathing is at the forefront in children due to the weak intercostal muscles and the fact
that the cartilage part of the thorax is more than the bone part. There is also a
marked increase in the number of alveoli from the newborn to adulthood, up to
8–10years of age. After this age, a decrease in number is observed, while structural
development comes to the fore. Lung surface area also increases from childhood to
adulthood. All these differences show that the tests related to the lower airway in
children should be evaluated by considering the appropriate percentile range and
anatomical and physiological differences in the evaluation stages.
15.2 Airway Measurements
Since respiratory system diseases may progress with a high-risk clinical course for
mortality and morbidity, respiratory function tests have an important role in diagnosis and follow-up. The evaluation of lung function is more difcult in infants and
preschoolers compared with older children. Because of the lack of cooperation during measurements, several conditions such as lying during natural sleep or under
sedation can be used in infants, while this is not feasible in preschool children.
In children aged over 5years and adults, spirometry is the gold standard technique in the measurement of lung function [1]. However, spirometry cannot be
performed very often by the younger age group, because of collaboration issues.
On the other side, body plethysmography is the gold standard method in the determination of airway resistance and lung volumes [2]. Airway resistance is
15 Preschool Lung Functıon Testıng andtheUpper Respıratory Tract
201
determined by lung volume and is expected to decrease as lung volume increases
[3, 4]. Body plethysmography is performed by closing the patient into a cabin and
asking the patient to perform respiratory maneuvers. Young children may experience difculties in performing these maneuvers. Therefore, body plethysmography
is preferably performed in older age groups for accurate diagnosis and treatment
approach. Other techniques, like respiratory oscillometry and the interrupter technique, that only require tidal breathing and minimal collaboration from the subject,
have proved to be more suitable for measuring airway resistance in preschool children [5]. Differently from the interrupter technique, oscillometry can also differentiate the upper airway component of respiratory impedance and give information
about reactance, which can be interpreted as compliance (or distensibility) of the
respiratory system (Table15.1).
Table 15.1 Tests used in the evaluation of the lower airway
Test applied
Spırometry
Pletısmography
Aırway
occlusıon
technıques
Multıple breath
helıum dılutıon
Multıple breath
wash test
Forced
oscıllatıon
technıque
Impulse
oscıllometry
Area of use
Used to measure lung function in
children over 6years of age and
adults
Used to determine airway
resistance (raw) and lung volumes
In cases such as occlusion of the
airways at the end of inspiration or
expiration, it is used in the
evaluation of passive respiratory
system mechanics (respiratory
system compliance, resistance)
It is an easily applicable method
used for the determination of lung
volumes, mostly FRC, during tidal
breathing
Detection of ventilation disorders
in small peripheral airways and
early detection of lung disease in
children with or without minimal
clinical symptoms
The forced oscillation technique
(FOT) is a simple and noninvasive
method that utilizes external sound/
pressure waves generated by a
loudspeaker
It is a type of forced oscillation
technique. More detailed analyses
of respiratory function are provided
with square pressure waves
generated regularly ve times per
second
Measurements
The relationship between volume
and time and the relationship
between ow and volume are shown
Residual volume (RV), total lung
capacity (TLC), and functional
residual capacity (FRC) allow the
measurement of all static and
dynamic lung volumes
The airow interrupter technique
(Rint) is a simple method of
measuring airway resistance
Used for the determination of FRC
(functional residual capacity)
Residual volume (RV), total lung
capacity (TLC), and functional
residual capacity (FRC) are
determined
It enables the evaluation of the
mechanical properties of the lung by
measuring the change in pressure
and ow
Impedance (Z), resistance (R),
reactance (X), resonance frequency
(Fres), and reactance area (AX) can
be measured with IOS.These values
are measured and named at specic
frequencies (5–35Hz)
202
S. Tunca et al.
15.3 The Most Appropriate Lung Function Technique
inPreschoolers
The answer to this question always depends on the clinical/research issue we are
facing [6]. Oscillometry, also called Forced Oscillation Technique (FOT), is evaluated as one of the most suitable techniques regarding applicability in preschool
children [5]. This technique requires no challenging expiration maneuvers and is
diagnostically very precious when the difculty in the clinical evaluation of lower
airways increases as age decreases [7]. In the application of oscillometry, sound
waves produced using a loudspeaker and transmitted to the lung cause changes in
pressure and these changes result in differences in airow. The measurement of
these changes in pressure and airow allows the determination of the mechanical
properties of the lung by giving an estimate of respiratory impedance (Zrs), which
includes resistance (Rrs, frictional losses of the respiratory system) and reactance
(Xrs, elastic properties of the respiratory system at low frequencies and inertial
forces of the air columns at higher frequencies) [8, 9].
Sinusoidal waves or impulses (impulse oscillometry, IOS) have been used, both
as single-frequency or multiple-frequency signals, with frequencies 5–10Hz being
considered to reect the mechanical properties of the total airways and higher frequencies giving an estimate of more proximal airways [8–10]. This is because highfrequency sound waves return from the large airways, while low-frequency sound
waves progress through the peripheral system and also provide information about
distal airways. Rrs increases at all frequencies in case of central airway obstruction,
whereas low-frequency Rrs increases with no change in high-frequency Rrs in case
of small airway obstruction.
Momentum through the airways transmitting the pressure waves and expansion
capacity of the lung tissue constitutes Xrs. At low frequencies, the lung has a passive expansion, high elasticity, and high expansion capacity. As frequency increases,
active stretching is passed, and amount of the distributed energy increases. At the
transition frequency of passive expansion-active stretching, the required pressure
and elastic expansion capacity become equal at a point. This frequency at which
expansion capacity (reactance) becomes 0 is named resonant frequency (fres) and is
associated with the anterior-posterior diameter and tissue structure of the chest. The
fres values increase, because Xrs is more negative, at low frequencies in obstructive
and restrictive cases [11]. The area under the curve of reactance (AX) is the area
under the Xrs curve between the lowest frequency and fres; this index is reported to
be more sensitive than Xrs itself in detecting changes in compliance of the respiratory system [9].
Oscillometry is often used in the acute and chronic stages of asthma or chronic
lung disease of prematurity. In proximal obstruction, Rrs increases independently
from frequency whereas Xrs is affected very little or none. In distal obstruction,
low-frequency Rrs increases and Xrs decreases. Because of this frequency dependence, often evident in respiratory disease, the difference between Rrs measured at
5Hz and Rrs measured at 20Hz (Rrs5–20) is often used to describe the mechanics
of peripheral airways. Rrs5–20 may actually also reect other determinants of
15 Preschool Lung Functıon Testıng andtheUpper Respıratory Tract
203
respiratory mechanics, including upper airway shunt (compliant zones proximal to
the area of increased resistance) [9].
In children with asthma, Rrs5, AX, and fres increase whereas X5 decreases [12].
Shi etal. have compared essential spirometry and IOS indices in a study conducted
on two groups of children with controlled and uncontrolled asthma. R5 and AX
values were signicantly different between the two groups whereas no difference
was found between baseline spirometry values [13]. The other advantage of oscillometry compared with other techniques, besides the applicability in preschool children due to no requirement of extra effort by the patient during breathing, is the
information of reactance and resistance at different frequencies even from nonhomogeneous regional areas in the lung structure. Its capability to detect even the little
changes in the small or central airways seems very precious when it comes to early
diagnosis in comparison with spirometry [14, 15].
Oscillometry is also a very precious technique for the evaluation of the long-term
pulmonary function of children with bronchopulmonary dysplasia and preterm
birth. A study comparing children with late preterm birth to healthy controls born at
term using the IOS technique found that mean Rrs5 and Rrs10 values were higher
in the late preterm group compared to the control group and that mean Rrs5, Rrs10,
and Zrs5 values were higher in the late preterm children hospitalized for pulmonary
infection compared to the control group [16]. Another study using a sinusoidal signal found that 5-year-old children born very preterm (<32weeks of gestational age)
had impaired Xrs8 and AX, but not Rrs8, when compared with their expected values, showing that the respiratory damage in these children is primarily due to
decreased respiratory compliance [17].
Appropriate reference equations are crucial to distinguish the effects of the disease from the effects of growth and development in the preschool period. Information
about repeatability, differential sensitivity, and specicity is also important to reliably interpret lung function results [6]. Several reference equations are available for
oscillometry in adults and children [13]. The Global Lung Function Initiative (GLI,
www.lungfunction.org) is also collecting reference data for oscillometry from
worldwide laboratories to develop global reference equations for adults and children.
As a conclusion, measuring airway function in children should involve a different approach than in adults, taking into consideration both anatomical and
physiological differences. It is very important to select the most appropriate
respiratory function test routinely used in the diagnosis and follow-up of respiratory tract disease. Many pulmonary function techniques are very precious
methods in the evaluation of lung disease, but not all of them are highly feasible
in preschool children. In recent years, the development and implementation of
novel techniques requiring minimum cooperation, such as oscillometry, allowed
us to obtain more reliable and benecial measurements in preschool children.
Also, oscillometry can differentiate resistance from reactance and give information about the upper airway component of respiratory impedance. The selection
of the most accurate technique for the appropriate patient group will, doubtlessly, increase the chance of diagnostic accuracy and, hopefully, treatment
success.
204
S. Tunca et al.
References
1. Miller MR, Hankinson J, Brusasco V, et al. Standardisation of spirometry. Eur Respir
J. 2005;26(2):319–38.
2. Kjaer BB, Jensen JS, Nielsen KG, et al. Lung function and bronchial responsiveness after
mycoplasma pneumoniae infection in early childhood. Pediatr Pulmonol. 2008;43(6):567–75.
3. Klug B, Bisgaard H.Specic airway resistance, interrupter resistance, and respiratory impedance in healthy children aged 2-7 years. Pediatr Pulmonol. 1998;25(5):322–31.
4. Escobar H, Carver TW.Pulmonary function testing in young children. Curr Allergy Asthma
Rep. 2011;11(6):473–81.
5. Rosenfeld M, Allen J, Arets BH, et al. An ofcial American Thoracic Society workshop
report: optimal lung function tests for monitoring cystic brosis, bronchopulmonary dysplasia, and recurrent wheezing in children less than 6 years of age. Ann Am Thorac Soc.
2013;10(2):S1–S11.
6. Beydon N, Davis SD, Lombardi E, etal. An ofcial American Thoracic Society/European
Respiratory Society statement: pulmonary function testing in preschool children.
American journal of respiratory and critical care medicine. Am J Respir Crit Care Med.
2007;175(12):1304–45.
7. Fainardi V, Lombardi E.Lung function tests to monitor respiratory disease in preschool children. Acta Biomed. 2018;89(2):148–56.
8. King GG, Bates J, Berger KI, et al. Technical standards for respiratory Oscillometry. Eur
Respir J. 2020;55(2):1900753.
9. Kaminsky DA, Simpson SJ, Berger KI, etal. Clinical signicance and applications of oscillometry. Eur Respir Rev. 2022;31(163):210208.
10. Starczewska-Dymek L, Bozek A, Dymek T.Application of the forced oscillation technique in
diagnosing and monitoring asthma in preschool children. Adv Respir Med. 2019;87(1):26–35.
11. Desiraju K, Agrawal A.Impulse oscillometry: the state-of-art for lung function testing. Lung
India. 2016;33(4):410–6.
12. Kaminsky DA. What does airway resistance tell us about lung function? Respir Care.
2012;57(1):85–99.
13. Shi Y, Aledia AS, Galant SP, George SC.Peripheral airway impairment measured by oscillometry predicts loss of asthma control in children. J Allergy Clin Immunol. 2013;131(3):718–23.
14. Smith HJ, Reinhold P, Goldman MD. Forced oscillation technique and impulse oscillometry. In: Gosselink R, Stam H, editors. Lung function testing. European Respiratory Society
Publications; 2005.
15. Bickel S, Popler J, Lesnick B, etal. Impulse oscillometry: interpretation and practical applications. Chest. 2014;146(3):841–7.
16. Er I, Gunlemez A, Uyan ZS, etal. Evaluation of lung function on impulse oscillometry in
preschool children born late preterm. Pediatr Int. 2016;58(4):274–8.
17. Lombardi E, Fainardi V, Calogero C, etal. Lung function in a cohort of 5-year-old children
born very preterm. Pediatr Pulmonol. 2018;53(12):1633–9.
Spirometry andUpper Respiratory Tract
16
VáclavKoucký andNazanCobanoglu
16.1 Introduction
Spirometry is a fundamental lung function examination. It informs about lung volumes and inspiratory and expiratory ows, which reect airway patency and stability. Forced vital capacity (FVC), forced expired volume in 1s (FEV1) and Tiffeneau
index (FEV1/FVC) are the most important spirometry parameters. These parameters
are primarily intended to detect lower airway obstruction. Additionally, they may
raise suspicion about restrictive disorder (which needs estimation of total lung
capacity to conrm). Although the sensitivity and specicity of spirometry for
upper airway pathology is limited, there are visual and quantitative criteria, which
may help in detecting upper airway obstruction. Visual criteria are based on the
evaluation of ow-volume loop shape both in inspiration and expiration. The ‘knee’
shape is one of the most typical ndings. The quantitative criteria include the Empey
index (ratio of FEV1 and peak expiratory ow) and others that use parameters characterising inspiratory ows, expiratory ow at different levels of FVC and others.
Nevertheless, spirometry is just supportive method for the rst-line assessment of
upper airway function and requires further conrmation. Spirometry may also
inform on the concomitant lower airway pathology and trigger a more detailed
investigation.
V. Koucký (*)
Department of Paediatrics, 2nd Faculty of Medicine, Charles University and University
Hospital Motol, Prague, Czech Republic
e-mail: Vaclav.koucky@fnmotol.cz
N. Cobanoglu
Division of Paediatric Pulmonology, Department of Paediatrics, Faculty of Medicine, Ankara
University, Ankara, Turkey
© The Author(s), under exclusive license to Springer Nature
Switzerland AG 2024
H. Yüksel et al. (eds.), Pediatric Airway Diseases, Comprehensive ENT,
https://doi.org/10.1007/978-3-031-74853-0_16
205
206
V. Koucký and N. Cobanoglu
16.2 Background
Spirometry is a fundamental lung function examination. It is widely available, quick
to perform and well known among respiratory physicians. On the other hand, it
requires the cooperation of the subject and is sensitive to the quality of manoeuvre
(risk of falsely pathological results). Spirometry may be successfully performed in
children aged 5years and more, with experienced lab personnel even earlier (3-yearold children). For children under 3years of age, there are special methods for lung
function testing such as raised volume rapid thoracoabdominal compression [1].
This is a technically highly demanding method usually performed in chloralhydrate-induced sleep and is available in several centres worldwide. It may yield similar outcome parameters like spirometry in older children, but the clinical value
needs further evaluation.
Forced spirometry is the most common version of spirometry. The manoeuvre
consists of deep inspiration and forced and long expiration. Sufcient effort from
the patient is crucial as it is necessary to reach residual volume (RV) and total lung
capacity (TLC) levels during the manoeuvre. Only this will allow proper estimation
of vital capacity (VC) (Fig.16.1). Moreover, expiration must be forced to reach
maximal ow and ow limitation. Otherwise, the patency of airways may be underestimated, and false-positive nding of airway obstruction is present.
Technical aspects of spirometry are described in several international documents
published by the European Respiratory Society (ERS) and the American Thoracic
Society (ATS) [2–4]. They state details on the technical requirements to the equipment and other considerations, the test procedure itself, within- and betweenmanoeuvre evaluation, describe outcome indices, quality control and many others.
All physicians dealing with spirometry must be familiar with these recommendations. As they are beyond the scope of this text, we refer interested readers to the
respective documents.
Fig. 16.1 Volume time tracing of the spirometry measurement
16 Spirometry andUpper Respiratory Tract
207
Forced spirometry is usually depicted by a ow-volume (FV) loop (Fig.16.2).
While on the x-axis volume (V) is shown, the y-axis represents ow (F). Inspiratory
ow is negative (below the x-axis) and expiratory ow is positive (above the x-axis).
Pathology (airway obstruction) localised outside the thorax (extra-thoracally—i.e.
above the upper thoracic aperture, e.g. upper airway obstruction) will primarily
manifest during inspiration. On the other hand, pathology localised intra-thoracally
(i.e. under upper thoracic aperture—in the thorax, e.g. peripheral airway obstruction) will primarily affect the expiratory part of the FV loop. In case of severe and
xed obstruction of any localisation along the bronchial tree, both breath phases
may be affected. This is a basic rule for the interpretation of spirometry results and
follows from the physiology of the respiratory tract (see changes in the pressure in
the airway during individual breath phases). Based on this fact, characteristic shapes
of ow volume loops are described (see Fig.16.3). Although they do not allow
denitive diagnosis, they are very helpful in rst-line evaluation and may give hints
on the specic pathology—e.g. peripheral or central airway obstruction, large airway instability, premature termination of expiration, etc.
Beside FV loop shapes, different outcome parameters (indices) may be derived
from the forced spirometry. They are summarised in Table 16.1 along with their
denitions. These outcomes are usually expressed in absolute values (litres or litres
per second) and related to the appropriate norm (reference values). Currently, multiethnic reference values derived within the GLI2012 initiative (Global Lung
Initiative) [5] are usually used, although national or other specic reference values
[6–8] may be preferred in some cases (e.g. availability of the reference for more
outcome parameters, better suitability for the respective population, better comparability to the previous measurements in the respective patient, etc.).
The comparison of the measured (absolute) value of the respective outcome to
the norm may be expressed in various ways. Historically, this was done as a
Fig. 16.2 Flow-volume
loop. PEF, peak
exspiratory ow; FVC,
forced vital capacity;
MEF75, maximum
exspiratory ow at 75% of
FVC; MEF50, maximum
exspiraotry ow at 50% of
FVC; MEF25, maximum
exspiratory ow at 25% of
FVC; IRV, inspiratory
reserve volume; Vt, tidal
volume; ERV, exspiratory
reserve volume; MIF50,
maximum inspiratory ow
at 50% of FVC