Abstract
Impulse oscillometry is a lung function test that has become more widely used over the past 30 years. It is particularly useful in patients who have difficulty performing forced respiratory maneuvers, such as preschool children, who have shorter expiration times, less strength to inhale, less coordination and shorter attention spans than older children or adults. At preschool age, oscillometry has a higher success rate than spirometry and is more sensitive in detecting changes in lung function in the diagnosis and monitoring of asthma. This review summarizes the available scientific evidence supporting its use in the diagnosis, measurement of control, severity, monitoring and follow-up of preschool asthma.
Keywords
Asthma, Preschool, Impulse oscillometry
Introduction
Impulse oscillometry (IOS) is a lung function test derived from the forced oscillation technique (FOT) described in 1956 by Dubois [1]. In 1994, Voegel and Smith presented it to the international scientific community, which allowed the German laboratory Jaeger® to begin its development and commercialization for both children and adults worldwide [2]. In the last 30 years its use has expanded globally, having a particular utility in the diagnosis and monitoring of respiratory diseases in children and adults [3]. In simple terms, IOS uses a loudspeaker to transmit square-shaped sound waves in constant pulses of at least 5 times per second that travel in an oscillating manner superimposed on the normal respiratory flow at different frequencies, allowing pressure and flow to be determined by transducers and transmitting this information to software to calculate Impedance (Zrs), Resistance (Rrs) and Reactance (Xrs) and other parameters of the respiratory system (Table 1). These parameters are useful for diagnosis and monitoring of different diseases affecting the respiratory system [4]. Technical and interpretation recommendations for IOS for children and adults have recently been published [5,6]. The parameters measured in the IOS may vary due to different factors, among which the most important are age, height and ethnicity; which may contribute to the underrepresentation of some populations [7]. Recently, predictive equations for healthy people from 2.7 to 90 years of age were published, which will allow more accurate measurements of lung function throughout life in the future [8]. IOS is a noninvasive technique, easy to perform, without complex maneuvers, which makes it ideal for young children. It has been shown that only 80% of children are able to perform the forced spirometric maneuver, unlike 100% who can perform IOS [9]. In addition, it is a fast, reliable and sensitive technique for small changes in lung function, which allows diagnosis of small airway obstruction, a site of the respiratory system that in recent years has been recognized as the target for the treatment of asthma in the first years of life [10,11]. Recent evidence highlights preschool IOS as one of the best techniques to identify children at highest risk of future lung function decline [12].
|
Parameter |
Definition |
|
Respiratory Impedance (Zrs) |
Respiratory Resistance plus Respiratory Reactance. |
|
Respiratory Resistance (Rrs) |
Energy to propagate a pressure wave through the airways. |
|
Resistance at 5 Hertz (R5) |
Reflects the total resistance of the airway. |
|
Resistance at 20 Hertz (R20) |
Reflects proximal airway resistance. |
|
Difference between 5 and 20 Hertz Resistance (R5-R20) |
Reflects the resistance of the distal airway. |
|
Respiratory Reactance (Xrs) |
Energy generated by the recoil of the lungs after distension by a pressure wave, composed of inertance and elastance. |
|
Reactance at 5 Herz (X5) |
Reactance at low frequency where the elastance effect predominates. |
|
Reactance Area (AX) |
Area under the curve between values of X5 and Fres, also called the Goldman triangle. |
|
Resonance frequency (Fres) |
Point where reactance is equal to zero, where elastic forces are equivalent to inertial forces. |
Furthermore, IOS has been shown to be a cost-effective technique for the diagnosis of asthma when compared with spirometry in preschool children [13]. The objective of the present study was to describe the scientific evidence available regarding the usefulness of IOS in preschool asthma.
Method
A review of the scientific evidence on the use of IOS in asthmatic preschoolers was conducted. The search for articles was carried out between September 2024 in the Medline (PubMed), Web of Science (WOS), EBSCO Host, Science Direct and SCOPUS databases. MeSH terms and free terms in their English version were used. The terms were grouped into two dimensions: i) Impulse oscillometry ii) preschool asthma. The Boolean operator “and” was used to integrate the two dimensions. In addition, abstracts of publications published at the congresses of the American Thoracic Society (ATS) and the European Respiratory Society (ERS) were reviewed. The articles found were grouped into three categories: oscillometry in the diagnosis of preschool asthma, oscillometry in control and severity of preschool asthma, and oscillometry for monitoring and follow-up of preschool asthma.
Oscillometry in the diagnosis of preschool asthma
Preschoolers with early or late wheezing have been shown to have significantly higher baseline values of the reactance area (AX), the difference between the resistance at 5 Hertz (R5) and the resistance at 20 Hertz (R20) measured in Kilopascals (R5-R20) or percentage (R5-R20%) compared to healthy preschoolers [14]. Prebronchodilator R5 and R5-R20 values have been found to be significantly higher in preschoolers whose mothers reported more respiratory symptoms suggestive of asthma than those with fewer symptoms [15]. The IOS has also been shown to be useful for confirming abnormalities in preschoolers at high risk of asthma. One study showed that preschoolers with a history of maternal asthma and moderate to severe rhinovirus bronchiolitis had significantly higher baseline R5 and 5 Hertz reactance (X5) values on the IOS than preschoolers without this history [16]. Bronchodilator response (BDR) in IOS has also been studied in the diagnosis of preschool asthma. The first study that measured the utility of BDR in IOS demonstrated that post-bronchodilator decrease of R5 ≥ -40% could be a good parameter to differentiate between preschoolers with asthma and healthy children [17]. It was subsequently reported that decreases ≥ -27% or -29% in R5 could be good cut-off points to differentiate between preschool asthma and healthy controls [18]. A controlled study compared preschoolers with or without asthma at age 4 years, showing that the post-bronchodilator fall in R5 and 10 Hertz Resistance (R10) were the best parameters to discriminate between preschoolers with asthma and healthy ones. In this study, it was proposed that a decrease in post-bronchodilator resistance of -20 to -25% in R5 and/or -10 to -15% in R10 would be the best cut-off points to diagnose asthma among atopic preschoolers [19]. Another study found significantly higher baseline values of R10 in asthmatic preschoolers compared to healthy controls, as well as greater post-bronchodilator decreases in R5, R10, R20 and resistance at 35 Hertz (R35), differences that were not found in spirometry. Furthermore, this study reported that these differences were found in both atopic and non-atopic asthmatics compared to healthy controls [20]. The addition of the IOS BDR to the spirometry BDR has been shown to increase the accuracy in diagnosing preschool asthma, with this combination being superior to each parameter alone [21]. A recent retrospective evaluation of the BDR measured by IOS and spirometry in preschoolers diagnosed with asthma was performed. This evaluation found that the decrease in R5 and the increase in X5 after the bronchodilator would be the best parameters to identify the BDR in spirometry [22]. The IOS has also been used to measure bronchial hyperresponsiveness (BHR) with methacholine in the diagnosis of asthma, with the percentage change in X5 with respect to the predicted value being the parameter with the highest sensitivity and specificity [23]. A study showed that for the diagnosis of BHR with methacholine and IOS, the combination of an increase in R5 with the decrease in X5 was the one that had the best sensitivity to detect the 20% drop in the expiratory volume of the first second in spirometry [24]. It has been shown that the increase in R5 during the methacholine test can differentiate preschoolers with current asthma symptoms from healthy controls, a parameter that has been termed PD40R5, i.e. the dose of methacholine with which the 40% increase in R5 is caused [25]. BHR measured with methacholine and IOS has been found in up to 97% of patients studied with R5 and X5, the latter parameter being the most reproducible [26]. In asthma diagnosis, the utility of the IOS combined with clinical predictive algorithms or biomarkers in respiratory diseases has been measured. It has been shown that baseline values of R5-R20% are increased in recurrent wheezers with a positive modified asthma predictive index (mAPI) compared to those with a negative algorithm, which may help to identify recurrent wheezers at high risk of asthma [27]. Other investigations have combined parameters of the IOS with the fraction of exhaled nitric oxide (FeNO). One study found that the best combination of markers for the diagnosis of cough-variant asthma was X5 less than -4.15 cmH2O/L/s plus FeNO over 18 ppb [28]. A 1-year follow-up study was recently published that was able to create a predictive model for preschool asthma, showing that the combination of R5, X5, and FeNO is able to differentiate with a high degree of accuracy preschoolers with or without asthma, with the combined model being superior to each parameter individually [29].
|
Author |
Type of study |
Population |
Age |
Result |
|
|
Kinitiä et al. [14] |
Cross-sectional |
Early wheezing, late wheezing, bronchopulmonary dysplasia vs healthy |
Average 5 to 6 years |
In early and late wheezing preschoolers, the z-scores of R5-20, R5-20% and AX were significantly higher than in healthy subjects (p<0.001 for all comparisons). |
|
|
Medeiros et al. [15] |
Cross-sectional |
Preschoolers with or without respiratory symptoms |
3 to 6 years |
R5 baseline (symptoms 1.03 vs. no symptoms 0.92, p=0.018); R5-R20 baseline (symptoms 0.37 vs. no symptoms 0.29, p=0.009) |
|
|
Da Silva Sena et al. [16] |
Prospective |
Preschoolers with a history of hospitalization for moderate to severe bronchiolitis |
3 to 6 years |
R5>1.65 Adjusted RR=3.11 and X5<-1.65 Adjusted RR=2.11 in preschoolers with maternal asthma and rhinovirus bronchiolitis |
|
|
Hellinckx et al. [17] |
Cross-sectional |
Asthmatic vs. healthy preschoolers |
2.7 to 6.6 years |
Average post-bronchodilator decrease in R5 was -12% in healthy preschoolers with an upper range up to 40% |
|
|
Nielsen et al. [18]
|
Cross-sectional |
Asthmatic vs. healthy preschoolers |
2 to 5 years |
Post-bronchodilator decrease in R5 (S=76%, E= 65%, PPV=76%, NPV=65%) |
|
|
Marotta et al. [ 19]
|
Cross-sectional |
Asthmatic vs. healthy preschoolers |
4 years |
Δ R5 (asthma -27% vs no asthma 17%; P=0.02) y Δ10 asthma (24% vs no asthma 16%; P=0.03) |
|
|
Song et al. [20] |
Cross-sectional |
Asthmatic vs. healthy preschoolers |
3 to 6 years |
R10 (asthma 0.8 kPa/L/s vs healthy controls 0.7 kPa/L/s, p=0.035). Bronchodilator response to detect clinical asthma (AUC ?R5=0.663, AUC ? R10=0.609) |
|
|
Shin et al. [21]
|
Cross-sectional |
Preschoolers with stable asthma vs healthy controls |
Average 4.6 years |
Δ FEV1 ≥ 9% + ΔR5 ≥ -29% (S=63%, E=93%, LR+ 9.14) |
|
|
Meoli et al. [22] |
Retrospective |
Preschoolers with asthma |
3 to 6 years |
Δ R5 -25.7% (AUC 0.77, p = .03) and Δ X5 25.7% (AUC 0.75, p = 0.04) achieve the best sensitivity and specificity for FEV1 ≥ 12% and/or ≥200 ml |
|
|
Jee et al. [23]
|
Cross-sectional |
Preschoolers with asthma and controls with chronic cough |
2 to 6 years |
PC80X5 was the best cut-off point to differentiate asthma from controls (S= 80%, E= 82.9%). |
|
|
Schulze et al. [24] |
Cross-sectional |
Preschoolers with suspected asthma |
3 to 6 years |
Increase in R5 by 45% and/or reduction in X5 by 0.69 kPa/L/s detect a drop in FEV1 by 20% (S= 72% and E =73%; S=80% and E=76%, respectively) |
|
|
Kalliola et al. [25] |
Cross-sectional |
Preschoolers with early-onset wheezing, late-onset wheezing, bronchopulmonary dysplasia, and healthy controls |
3 to 8 years |
40% increase in R5 with methacholine (late wheezing 77% vs healthy controls 21%, p < 0.001) |
|
|
Choi et al. [26]
|
Prospective |
Preschoolers with asthma |
3 to 6 years |
Reproducibility coefficient (C80X5=2.56, C30R5=1.54) |
|
|
Arikoglu et al. [27] |
Cross-sectional |
Recurrent wheezing with or without positive mAPI |
3 to 6 years |
R5-R20% in predicting recurrent wheezing positive mAPI (OR=1.4, p=0.02, AUC=0.655, p=0.003, S=75%, E=53%)) |
|
|
Hu et al. [28] |
Cross-sectional |
Preschoolers with or without cough as a variant of asthma |
3 to 6 years |
AUC for the diagnosis of cough as a variant of asthma (X5 = 0.657, FeNO = 0.779, X5 + FeNO = 0.809) |
|
|
Chen et al. [29] |
Prospective |
Preschoolers with or without asthma |
3 to 6 years |
R5 + X5 + FeNO in the prediction of asthma (AUC=0.94, S=0.89, E=0.88, PPV=0.88 NPV=0.9) |
|
|
Δ: Variation in Bronchodilator Response; AUC: Area Under the Curve; S: Sensitivity; E: Specificity; PPV: Positive Predictive Value; NPV: Negative Predictive Value; LR+: Positive Likelihood Ratio; OR: Odds Ratio; RR: Relative Risk, mAPI: Modified Asthma Predicted Index; FeNO: Exhaled Fraction of Nitric Oxide |
|||||
Oscillometry in control and severity of preschool asthma
Preschoolers with recurrent wheezing and a positive Asthma Predictive Index (API) who use inhaled corticosteroids have been reported to have a higher R20 than API-positive preschoolers who do not use inhaled corticosteroids. This would reflect the increased central airway resistance and indicate that they probably have greater asthma severity [30]. The X5 z-score has been reported as a parameter capable of differentiating between preschool asthma of different degrees of severity, defined by the risk of exacerbations with systemic corticosteroid use or the need for controller treatment [31]. The increase in R5-R20 measured during the methacholine test has been reported as a marker of the severity of exercise-induced bronchoconstriction (EIB) in preschoolers with suspected asthma [32]. A prospective one-year study in preschoolers with asthma demonstrated that R5, R5-R20, and X5 were the IOS parameters that best predicted asthma exacerbations [33]. The preschooler subgroup in a study spanning up to adolescence showed that X5 is better than FEF 25-75% as a parameter for predicting uncontrolled asthma [34]. Other studies in preschoolers with asthma demonstrated that the combination of R5, R5-R20, Fres or X5 in IOS with FeNO was the most accurate in discriminating between controlled and uncontrolled asthma [35,36]. AX, R5-R20 and R5 have also been reported to be the best parameters for predicting loss of asthma control in preschoolers after 8 to 12 weeks [37]. Reactance inversion (RI) is a recently described phenomenon in the IOS of asthmatic patients. RI can be identified with the corrected R5 (X5c) and has been found more frequently in preschoolers with decreased lung function on spirometry and peripheral airway obstruction with other IOS parameters such as AX and R5-R20 [38].
|
Author |
Type of study
|
Population |
Age |
Result |
|
Lezana et al. [30]
|
Cross-sectional |
Preschoolers with API positive or negative asthma |
24 to 72 months |
API preschoolers (with CI R20 89% without corticosteroids 81%, p=0.047) |
|
Shin et al. [31] |
Cross-sectional |
Preschoolers with intermittent, mild persistent, moderate-severe persistent asthma |
2 to 5 years |
Z-score X5 below the normal limit have highest need for medication (p=0.008) and highest combined severity (p=0.019) |
|
Kalliola et al. [32] |
Cross-sectional |
Preschoolers with respiratory symptoms of suspected asthma |
3 to 8 years |
Increase R5-R20 in methacholine test (severe EIB vs no EIB p=0.036) |
|
Schulze et al. [33] |
Prospective |
Asthmatic preschoolers |
4 to 7 years |
Prediction of exacerbations in one year (AUC R5= 0.80, p<0.001, AUC R5-R20=0.77, p<0.001, AUC X5=0.70, p=0.01) |
|
Tirakitsoontorn et al. [34]
|
Retrospective |
Subgroup of preschoolers with controlled and uncontrolled asthma |
4 to 7 years |
X5<3.8 cmH2O predicts uncontrolled asthma (AUC>0.7, S=68.8%, E= 77.8%, PPV=64.7%, NPV=80.8%) |
|
Zeng et al. [35] |
Cross-sectional |
Preschoolers with asthma (controlled and uncontrolled) and healthy controls |
3 to 6 years |
AUC of X5<-3.6 cm H2O, FeNO>27ppb and combination of both (0.75, 0.78 and 0.86, respectively) |
|
Xiao et al. [36] |
Prospective |
Preschoolers with asthma (controlled and uncontrolled) and healthy controls |
3 to 6 years |
AUC for predicting uncontrolled asthma (R5-R20+FeNO=0.92, R5 + FeNO=0.91, X5 + FeNO=0.91, Fres + FeNO=0.91) |
|
Zheng et al. [37] |
Prospective |
Preschoolers with asthma and healthy controls |
3 to 6 years |
Prediction of uncontrolled asthma with AUC (AX, R5-R20 and R5 = 0.88, 0.84 and 0.82, respectively) |
|
González et al. [38] |
Cross-sectional |
Subgroup of persistent asthmatic preschoolers with and without reactance inversion |
3 to 6 years |
X5 vs X5c (FEV1 1.28 vs 1.17, p<0.05, FEV0.75 1.16 vs 1.06, p<0.05, FEV0.5 0.97 vs 0.88, p<0.05, (AX 2.7 vs 4.4, p<0.01, R5-R20 0.24 vs 0.42, p<0.01) |
|
API: Asthma Predicted Index; AUC: Area Under the Curve; S: Sensitivity; E: Specificity; PPV: Positive Predictive Value; NPV: Negative Predictive Value; EIB: Exercise-Induced Bronchodilator Restriction; FeNO: Exhaled fraction of nitric oxide |
||||
Oscillometry for monitoring and follow-up of preschool asthma
A follow-up study demonstrated that inhaled corticosteroid treatment of preschool asthma can be guided by a free-running exercise challenge test. In this study, The EIB measured by increases in R5 was significantly decreasing with treatment over 3 visits in 6 months [39]. Another study showed that in preschoolers, the IOS improves significantly after one year of controller treatment, however, it maintains a high percentage of significant BDR, which could reflect the severity of the disease. This study also showed that atopy, the degree of asthma control and significant improvement of some parameters that reflect peripheral airway obstruction would allow identifying preschool asthma phenotypes [40]. The decrease in R5 and R5-R20 during asthma treatment has also been shown to correlate significantly with improvement in asthma control as measured by questionnaires at 12 months of treatment [41]. Two recent studies have demonstrated the usefulness of preschool IOS in predicting asthma or impaired lung function at school age. The first was conducted in preschoolers with persistent asthma who were on average 4.9 years old at the first assessment and 7.9 years old at the second assessment three years later, showing that AX, R5-R20 and R5 were the best parameters to discriminate between normal and abnormal spirometry at school age [42]. In the second study, lung function was measured with IOS in preschoolers aged 4, 5, 6 years and spirometry at 5, 6, 7 and 8 years. This study demonstrated that the increase in preschool R5 is able to predict which children will continue to have active asthma or impaired lung function at 8 years of age [43]. Other studies have linked alterations in preschool IOS with decreased lung function measured by spirometry in adolescence. One study showed that high R5 values in asthmatic preschoolers were associated with decreased post-bronchodilator FEV1 in adolescence [44]. Another study showed that post-bronchodilator X5 values in preschool IOS have a strong correlation with post-bronchodilator FEV1 and FVC in adolescents [45]. Finally, a prospective study in preschoolers showed that increased preschool R5 was associated with lower FEV1/FVC, higher medication use, and asthma symptoms in adolescence after 10 years of follow-up [46].
|
Author |
Type of study
|
Population |
Age |
Result |
|
Burman et al. [39] |
Prospective |
Preschoolers diagnosed with asthma |
4 to 7 years |
R5 post-exercise 1st, 2nd and 3rd visit (61% vs 18% vs 13.5%, P<0.001)
|
|
González et al. [40] |
Prospective |
Persistent asthmatic preschoolers |
3 to 6 years |
IOS altered at baseline and after 12 months (80.6% vs 64.5%, p=0.04). BDR at baseline and after 12 months (77.4% vs 83.9, p=0.43) |
|
Hu et al. [41] |
Prospective |
Preschoolers with asthma and exacerbations |
2 to 6 years |
C-ACT with R5% y C-ACT with R5-R20 (both r=-0.49, p<0.01), TRACK with R5% (r=-0.31, p=0.04) TRACK with R5-R20 (r=-0.33, p=0.02) |
|
Grell et al. [42] |
Prospective |
Preschoolers with persistent asthma |
3 to 5 years |
LR+ for predicting abnormal spirometry (AX, R5-R20, R5 = 50, 10, and 7.1, respectively). AUC in predicting abnormal spirometry for AX, R5, R5-R20 (0.91, 0.9, and 0.79, respectively) |
|
Kinitiä et al. [43] |
Prospective |
Preschoolers with asthma |
3 to 8 years |
Increased R5 at 4 years and decreased lung function at 8 years (β =-0.3; p<0.001 for FEV1) or active asthma at 8 years (β=2.0; p=0.029) |
|
Kinitiä et al. [44] |
Retrospective |
Asthmatic adolescents aged 12 to 18 with preschool IOS |
2 to 7 years |
Increased preschool R5 (decreased FEV1 in adolescence, OR=5.9)
|
|
Lauhkonen et al. [45] |
Prospective |
Preschoolers with a history of hospitalization for bronchiolitis before 6 months of age |
5 to 7 years |
Post-BD X5 preschool has a strong correlation with post-BD FVC (rho = 0.61) and post-BD FEV1 (rho=0.59) in adolescence. One unit decrease in preschool X5 Z-score predicts 9.6% lower FEV1 and 9.3% lower FVC in adolescence. |
|
Lajunen et al. [46] |
Prospective |
Preschoolers with asthma |
4 to 7 years |
R5 abnormal preschool (in adolescence OR=9.2 for abnormal FEV1/FVC, 9.2 for medication, and 9.9 for asthma symptoms)
|
|
BDR: Bronchodilator Response; C-ACT: Child-Asthma Control Test; r: Pearson Correlation; LR+: Positive Likelihood Ratio; AUC: Area Under the Curve; OR: Odds Ratio, rho: Spearman Correlation |
||||
Conclusion
There is evidence demonstrating the usefulness of baseline IOS and its bronchodilator response in the diagnosis of preschool asthma. Combining some parameters of the IOS with asthma predictive algorithms or biomarkers increases the ability to discriminate between preschoolers with asthma and healthy children. The IOS has also been shown to be useful in identifying uncontrolled preschool asthma, patients at risk of future exacerbations, and those who require more controller treatment or have decreased lung function by other methods such as spirometry, methacholine test, bronchial challenge test with exercise or FeNO. Recent evidence allows us to recommend the use of the IOS in preschool asthma to identify patients who will continue to have active asthma or decreased lung function at school age or adolescence. Despite the significant developments of preschool IOS, there are still some limitations, such as not having universal predictive values applicable to different populations or establishing clinically useful cut-off points for the bronchodilator response with the different IOS parameters.
Conflict of Interest
There is no conflict of interest in this study.
Funding Sources
This research was not funded by any funding sources.
References
2. Vogel J, Smidt U. Impulse oscillometry: analysis of lung mechanics in general practice and the clinic, epidemiology and experimental research. pmi-Verlag-Gruppe; 1994.
3. Galant SP, Komarow HD, Shin HW, Siddiqui S, Lipworth BJ. The case for impulse oscillometry in the management of asthma in children and adults. Ann Allergy Asthma Immunol. 2017 Jun;118(6):664-71.
4. Kaminsky DA, Simpson SJ, Berger KI, Calverley P, de Melo PL, Dandurand R, et al. Clinical significance and applications of oscillometry. Eur Respir Rev. 2022 Feb 9;31(163):210208.
5. King GG, Bates J, Berger KI, Calverley P, de Melo PL, Dellacà RL, et al. Technical standards for respiratory oscillometry. Eur Respir J. 2020 Feb 27;55(2):1900753.
6. Thamrin C, Dellacà RL, Hall GL, Kaczka DW, Maksym GN, Oostveen E, et al. Technical standards for respiratory oscillometry: test loads for calibration and verification. Eur Respir J. 2020 Oct 8;56(4):2003369.
7. De Assumpcao MS, da Silva Goncalves E, Oliveira MS, Ribeiro JD, Dalbo Contrera Toro AA, de Azevedo Barros-Filho A, et al. Impulse Oscillometry System and Anthropometric Variables of Preschoolers, Children and Adolescents Systematic Review. Curr Pediatr Rev. 2017;13(2):126-35.
8. Gochicoa-Rangel L, Martínez-Briseño D, Guerrero-Zúñiga S, Contreras-Morales J, Arias-Jiménez D, Del-Río-Hidalgo R, et al. Reference equations using segmented regressions for impulse oscillometry in healthy subjects aged 2.7-90 years. ERJ Open Res. 2023 Dec 18;9(6):00503-2023.
9. Garg V, Parakh A. Spirometry vs Impulse oscillometry in evaluation of children with asthma. Eur Respir J. 2020;56(suppl 64):2647.
10. McDowell KM. Recent Diagnosis Techniques in Pediatric Asthma: Impulse Oscillometry in Preschool Asthma and Use of Exhaled Nitric Oxide. Immunol Allergy Clin North Am. 2019 May;39(2):205-19.
11. Comberiati P, Cottini M, Landi M, Berti A, Lombardi C, Peroni D. Impulse oscillometry for the evaluation and management of pediatric asthma. Exploration of Asthma & Allergy. 2023;2023:219-29.
12. Galant SP. Impulse oscillometry metrics identified preschool children at risk of future loss of lung function and asthma. J Allergy Clin Immunol Pract. 2024 Sep;12(9):2551-2.
13. Buendía JA, Patiño DG, Salazar AFZ. Assessing the economic implications of impulse oscillometry in preschoolers with asthma in Colombia. Pediatr Pulmonol. 2024 Mar;59(3):813-5.
14. Knihtilä H, Kotaniemi-Syrjänen A, Pelkonen AS, Kalliola S, Mäkelä MJ, Malmberg LP. Sensitivity of newly defined impulse oscillometry indices in preschool children. Pediatr Pulmonol. 2017 May;52(5):598-605.
15. Medeiros D, Castro P, Bianca ACD, Sarinho E, Araújo JF, Correia Junior M, et al. Impulse oscillometry: pulmonary function assessment in preschool children. Expert Rev Respir Med. 2020 Dec;14(12):1261-6.
16. Da Silva Sena CR, Morten M, Meredith J, Kepreotes E, E Murphy V, G Gibson P, et al. Rhinovirus bronchiolitis, maternal asthma, and the development of asthma and lung function impairments. Pediatr Pulmonol. 2021 Feb;56(2):362-70.
17. Hellinckx J, De Boeck K, Bande-Knops J, van der Poel M, Demedts M. Bronchodilator response in 3-6.5 years old healthy and stable asthmatic children. Eur Respir J. 1998 Aug;12(2):438-43.
18. Nielsen KG, Bisgaard H. Discriminative capacity of bronchodilator response measured with three different lung function techniques in asthmatic and healthy children aged 2 to 5 years. Am J Respir Crit Care Med. 2001 Aug 15;164(4):554-9.
19. Marotta A, Klinnert MD, Price MR, Larsen GL, Liu AH. Impulse oscillometry provides an effective measure of lung dysfunction in 4-year-old children at risk for persistent asthma. Journal of Allergy and Clinical Immunology. 2003 Aug 1;112(2):317-22.
20. Song TW, Kim KW, Kim ES, Park JW, Sohn MH, Kim KE. Utility of impulse oscillometry in young children with asthma. Pediatr Allergy Immunol. 2008 Dec;19(8):763-8.
21. Shin YH, Jang SJ, Yoon JW, Jee HM, Choi SH, Yum HY, et al. Oscillometric and spirometric bronchodilator response in preschool children with and without asthma. Can Respir J. 2012 Jul-Aug;19(4):273-7.
22. Meoli A, Trischler J, Hutter M, Dressler M, Esposito S, Blümchen K, et al. Impulse oscillometry bronchodilator response in preschool children. Pediatr Pulmonol. 2024 May;59(5):1321-9.
23. Jee HM, Kwak JH, Jung DW, Han MY. Useful parameters of bronchial hyperresponsiveness measured with an impulse oscillation technique in preschool children. J Asthma. 2010 Apr;47(3):227-32.
24. Schulze J, Smith HJ, Fuchs J, Herrmann E, Dressler M, Rose MA, et al. Methacholine challenge in young children as evaluated by spirometry and impulse oscillometry. Respir Med. 2012 May;106(5):627-34.
25. Kalliola S, Malmberg LP, Kajosaari M, Mattila PS, Pelkonen AS, Mäkelä MJ. Assessing direct and indirect airway hyperresponsiveness in children using impulse oscillometry. Ann Allergy Asthma Immunol. 2014 Aug;113(2):166-72.
26. Choi SH, Sheen YH, Kim MA, Baek JH, Baek HS, Lee SJ, et al. Clinical Implications of Oscillatory Lung Function during Methacholine Bronchoprovocation Testing of Preschool Children. Biomed Res Int. 2017;2017:9460190.
27. Arikoglu T, Batmaz SB, Yildirim DD, Tezol Ö, Bozlu G, Kuyucu S. Asthma predictive index in relation to respiratory mechanics by impulse oscillometry in recurrent wheezers. Allergol Immunopathol (Madr). 2018 Mar-Apr;46(2):190-5.
28. Hu Y, Zheng S, Chen Z, Yu D, Lai T, Chen Y, et al. Validity of fractional exhaled nitric oxide and small airway lung function measured by IOS in the diagnosis of cough variant asthma in preschool children with chronic cough. Allergy Asthma Clin Immunol. 2023 Sep 9;19(1):83.
29. Chen J, Xiao J, Liu L, Ali K, Wu S. Predictive Value of Impulse Oscillometry Combined with Fractional Expiratory Nitric Oxide Test for Asthma in Preschool Children. J Asthma Allergy. 2024 May 8;17:421-30.
30. Lezana V, Gajardo A, Bofill L, Gutierrez M, Mora S, Castro-Rodriguez JA. Airway tone dysfunction among pre-schoolers with positive asthma predictive index: A case-control study. Allergol Immunopathol (Madr). 2017 Mar-Apr;45(2):169-74.
31. Shin YH, Yoon JW, Choi SH, Baek JH, Kim HY, Jee HM, et al. Use of impulse oscillometry system in assessment of asthma severity for preschool children. J Asthma. 2013 Mar;50(2):198-203.
32. Kalliola S, Malmberg LP, Pelkonen AS, Mäkelä MJ. Aberrant small airways function relates to asthma severity in young children. Respir Med. 2016 Feb;111:16-20.
33. Schulze J, Biedebach S, Christmann M, Herrmann E, Voss S, Zielen S. Impulse Oscillometry as a Predictor of Asthma Exacerbations in Young Children. Respiration. 2016;91(2):107-14.
34. Tirakitsoontorn P, Crookes M, Fregeau W, Pabelonio N, Morphew T, Shin HW, et al. Recognition of the peripheral airway impairment phenotype in children with well-controlled asthma. Ann Allergy Asthma Immunol. 2018 Dec;121(6):692-8.
35. Zeng J, Chen Z, Hu Y, Hu Q, Zhong S, Liao W. Asthma control in preschool children with small airway function as measured by IOS and fractional exhaled nitric oxide. Respir Med. 2018 Dec;145:8-13.
36. Xiao J, Liu L, Ali K, Wu S, Chen J. Impulse Oscillometry Combined to FeNO in Relation to Asthma Control Among Preschool Children. J Asthma Allergy. 2024 Oct 15;17:1015-25.
37. Zheng S, Hu Y, Chen Z, Wang M, Liao W. Predicting asthma exacerbation by impulse oscillometry evaluation of small airway function and fractional exhaled nitric oxide in preschool children. Pediatr Pulmonol. 2020 Jul;55(7):1601-7.
38. González Vera R, Vidal Grell A, Yarur AM, Meneses CO, Castro-Rodriguez JA. "Reactance inversion" at low frequencies during lung function measurement by impulse oscillometry in children with persistent asthma. J Asthma. 2022 Aug;59(8):1597-603.
39. Burman J, Malmberg LP, Remes S, Jartti T, Pelkonen AS, Mäkelä MJ. Impulse oscillometry and free-running tests for diagnosing asthma and monitoring lung function in young children. Ann Allergy Asthma Immunol. 2021 Sep;127(3):326-33.
40. González Vera R, Saavedra Bentjerodt M, Vidal Grell A, Mackenney Poblete J. Evolutionary lung function evaluated by impulse oscillometry in preschoolers with asthma. Andes Pediatr. 2021 Feb;92(1):42-9.
41. Wu HF, Chen AC, Wei CC. Correlation between impulse oscillometry parameters and test for respiratory and asthma control in kids (TRACK) in asthma control of preschoolers with asthma. J Formos Med Assoc. 2024 Mar;123(3):366-73.
42. Grell AV, Vera RG, Yarur AM, Castro-Rodriguez JA, Montenegro MAP, Colodro OF, et al. Impulse oscillometry in preschool children with persistent asthma can predict spirometry at school age. Pediatr Pulmonol. 2023 May;58(5):1411-6.
43. Knihtilä HM, Stubbs BJ, Carey VJ, Laranjo N, Zeiger RS, Bacharier LB, et al. Preschool impulse oscillometry predicts active asthma and impaired lung function at school age. J Allergy Clin Immunol. 2024 Jul;154(1):94-100.e13.
44. Knihtilä H, Kotaniemi-Syrjänen A, Mäkelä MJ, Bondestam J, Pelkonen AS, Malmberg LP. Preschool oscillometry and lung function at adolescence in asthmatic children. Pediatr Pulmonol. 2015 Dec;50(12):1205-13.
45. Lauhkonen E, Riikonen R, Törmänen S, Koponen P, Nuolivirta K, Helminen M, et al. Impulse oscillometry at preschool age is a strong predictor of lung function by flow-volume spirometry in adolescence. Pediatr Pulmonol. 2018 May;53(5):552-8.
46. Lajunen K, Kalliola S, Kotaniemi-Syrjänen A, Sarna S, Malmberg LP, Pelkonen AS, et al. Abnormal lung function at preschool age asthma in adolescence? Ann Allergy Asthma Immunol. 2018 May;120(5):520-6.