Acessibilidade / Reportar erro

IMPULSE OSCILLOMETRY AND SPIROMETRY IN SCHOOLERS SUBMITTED TO THE SIX-MINUTE WALK TEST

ABSTRACT

Objective:

To verify repercussions of submaximal exercise testing on respiratory mechanics and pulmonary function in schoolchildren.

Methods:

Cross-sectional study, with children aged 7 to 14 years, who had their respiratory mechanics assessed by impulse oscillometry (IOS), and pulmonary function by spirometry. They performed the six-minute walk test (6MWT), as per the standards by the American Thoracic Society. The 6MWT was performed twice with a 30-minute interval. IOS and spirometry were performed before the first 6MWT (Pre-6MWT) and immediately after the first (Post-6MWT1) and second walking tests (Post-6MWT2). The results in these three phases were compared by analysis of variance for repeated measures (post-hoc Bonferroni test) or by the Friedman’s test, with p≤0.05 considered significant.

Results:

Twenty-one subjects participated in the study: 53% were males and mean age was 10.9±2.3 years. There were differences between total resistance (R5) and central airway resistance (R20) at the three phases of assessment (p=0.025 and p=0.041, respectively). Post-hoc analysis indicated increase in R5 when Pre-6MWT and Post-6MWT1 were compared (R5=0.540±0.100 versus 0.590±0.150 kPa/L/s, p=0.013; and R20=0.440±0.800 versus 0.470±0.100 kPa/L/s, p=0.038). Forced expiratory flow 25-75% (FEF25-75%) changed over time (p=0.003).

Conclusions:

Repercussions were: increase in central and total airway resistance and reduction of FEF25-75% after 6MWT in schoolchildren, suggesting that greater attention should be given to submaximal tests in children with predisposition to airways alterations.

Keywords:
Child; Oscillometry; Respiratory function tests; Effort test

RESUMO

Objetivo:

Verificar as repercussões do teste de esforço submáximo na mecânica respiratória e na função pulmonar de escolares.

Métodos:

Estudo transversal com escolares de 7 a 14 anos submetidos à avaliação da mecânica respiratória por sistema de oscilometria de impulso (IOS) e da função pulmonar pela espirometria. Realizou-se também o teste de caminhada de seis minutos (TC6), todos segundo os padrões da Sociedade Torácica Americana. O TC6 foi executado duas vezes com intervalo de 30 minutos entre cada teste. O IOS e a espirometria foram feitos antes do primeiro TC6 (pré-TC6) e repetidos imediatamente após o primeiro TC6 (pós-TC61) e após o segundo TC6 (pós-TC62). A comparação dos resultados nos três tempos do estudo se deu por análise de variância para medidas repetidas (teste post-hoc de Bonferroni) ou teste de Friedman, sendo significante p≤0,05.

Resultados:

Participaram 21 sujeitos; 53% masculinos e idade média de 10,9±2,3 anos. Encontraram-se diferenças entre resistência total (R5) e resistência central das vias aéreas (R20) nos 3 tempos do estudo (p=0,025 e p=0,041, respectivamente). A análise post-hoc indicou aumento de resistência R5 entre pré-TC6 e pós-TC61 (R5=0,540±0,100 versus 0,590±0,150 kPa/L/s, p=0,013; e R20=0,440±0,800 versus 0,470±0,100 kPa/L/s, p=0,038). A única variável espirométrica com alteração no decorrer do tempo foi o fluxo expiratório forçado 25-75% (FEF25-75%) (p=0,003).

Conclusões:

As repercussões encontradas foram: aumento da resistência total e da resistência central das vias aéreas e redução do FEF25-75% após o TC6 em escolares, sugerindo a necessidade de mais atenção na realização de testes submáximos em crianças com alguma predisposição a alterações das vias aéreas.

Palavras-chave:
Criança; Oscilometria; Teste de função respiratória; Teste de esforço

INTRODUCTION

The six-minute walk test (6MWT) is among the main functional capacity assessment tests used in pediatrics that are considered low-cost, easy to use, reliable and reproducible.11. Aquino ES, Mourão FA, Souza RK, Glicério BM, Coelho CC. Comparative analysis of the six-minute walk test in healthy children and adolescentes. Rev Bras Fisioter. 2010;14:75-80. It is a submaximal test capable of reflecting the limitations of individuals with chronic respiratory diseases22. Lammers AE, Hislop AA, Flynn Y, Haworth SG. The 6-minute walk test: normal values for childrenof 4-11 years of age. Arch Dis Child. 2008;93:464-8.,33. Boyce D, Pullins E, McCormack MC, Mathai SC, Khair R. Safety of the six-minute walk test in chronic lung disease. Abstract of the American Thoracic Society 2016 International Conference; 2016 May 13-18; San Francisco, USA. p. A5722. which is commonly used to evaluate children11. Aquino ES, Mourão FA, Souza RK, Glicério BM, Coelho CC. Comparative analysis of the six-minute walk test in healthy children and adolescentes. Rev Bras Fisioter. 2010;14:75-80.,44. Geiger R, Strasak A, Treml B, Gasser K, Kleinsasser A, Fischer V, et al. Six-minute walk test in children and adolescents. J Pediatr. 2007;150:395-9. with the purpose of establishing reference values/equations55. Saad HB, Prefaut C, Missaoui R, Mohamed IH, Tabka Z, Hayot M. Reference equation for 6-min walk distance in healthy North African children 6-16 years old. Pediatr Pulmonol. 2009;44:316-24.,66. Klepper SE, Muir N. Reference values on the 6-minute walk test for children living in the United States. Pediatr Phys Ther. 2011;23:32-40. and investigating respiratory, neuromuscular and skeletal diseases.77. Bartels B, Groot JF, Terwee CB. The six-minute walk test in chronic pediatric conditions: a systematic review of measurement properties. Phys Ther. 2013;93:529-41. Well established in the literature, it follows guidelines and recommendations by the American Thoracic Society (ATS) and the European Respiratory Society (ERS).88. ATS Committee on Proficiency Standards for Clinical Pulmonary Function Laboratories. ATS statement: guidelines for the six-minute walk test. Am J Respir Crit Care Med. 2002;166:111-7.,99. Holland AE, Spruit MA, Troosters T, Puhan MA, Pepin V, Saey D, et al. An official European Respiratory Society/American Thoracic Society technical standard: field walking tests in chronic respiratory disease. Eur Respir J. 2014;44:1428-46.

Although this is a physical exercise testing and the literature reports possible changes in airways’ caliber as an important determinant of airflow and respiratory efforts during physical activities,1010. Gotshall RW. Airway response during exercise and hyperpnoea in non-asthmatic and asthmatic individuals. Sports Med. 2006;36:513-27.,1111. Wanrooij VH, Willeboordse M, Dompeling E, Kant KD. Exercise training in children with asthma: a systematic review. Br J Sports Med. 2014;48:1024-31. little is known about the dynamic relationship between airway resistance and its execution. According to the ATS,1212. Parsons JP, Hallstrand TS, Mastronarde JG, Kaminsky DA, Rundell KW, Hull JH, et al. An official American Thoracic Society clinical practice guideline: exercise-induced bronchoconstriction. Am J Respir Crit Care Med. 2013;187:1016-27. exercise-induced bronchospasm is the acute airway narrowing in response to exercise that happens even in patients without asthma diagnosis. Research in this field has focused on the relationship between bronchial narrowing, pulmonary function and cardiorespiratory and physiological parameters in individuals with asthma.1010. Gotshall RW. Airway response during exercise and hyperpnoea in non-asthmatic and asthmatic individuals. Sports Med. 2006;36:513-27.,1111. Wanrooij VH, Willeboordse M, Dompeling E, Kant KD. Exercise training in children with asthma: a systematic review. Br J Sports Med. 2014;48:1024-31.

In asthma and other respiratory diseases, spirometry has been routinely indicated for monitoring and intervention control. It is an exam conducted within well-defined guidelines and considered the gold standard to identify airway obstruction and restriction in pulmonary diseases.1313. Miller MR, Hankinson J, Brusasco V, Burgos F, Casaburi R, Coates A, et al. Standardisation of spirometry. Eur Respir J. 2005;26:319-38. Due to its difficult execution in the pediatric age group, impulse oscillometry system (IOS) is an important tool to analyze pulmonary mechanics parameters, as it is less complex to execute1414. Komarow HD, Myles IA, Uzzaman A, Metcalfe DD. Impulse oscillometry in the evaluation of diseases of the airways in children. Ann Allergy Asthma Immunol. 2011;106:191-9. and complements spirometric results.1515. Shirai T, Kurosawa H. Clinical application of the forced oscillation technique. Intern Med. 2016;55:559-66. IOS evaluates impedance (Z), resistance (R) and reactance (X5) parameters in multiple frequencies, from 5 to 35 Hertz, based on breaths at tidal volume. Described as a practical exam for being fast-paces and not requiring expiratory effort by individuals, it allows the identification of obstructive changes in the respiratory system.1616. Assumpção MS, Gonçalves RM, Ferreira LG, Schivinski CI. Impulse oscillometry system in pediatrics: review. Medicina (Ribeirão Preto). 2014;47:131-42.,1717. Bickel S, Popler J, Lesnick B, Eid N. Impulse oscillometry: interpretation and practical applications. Chest. 2014;146:841-7.

The literature has reports on investigation of relationships between respiratory diseases, such as asthma and cystic fibrosis, and oscillometric/spirometric parameters; however, the evaluation along with functional tests has not been done yet. Individuals with respiratory diseases are routinely assessed for their functional capacity; nevertheless, possible changes following exercise testings are not monitored. Both aspects of evaluation - functional capacity, by exercise testings such as the 6MWT, and respiratory integrity, by IOS and spirometry - are part of the handling of chronic diseases. Knowing some of the relationships between them in healthy children favors the understanding of normal cardiorespiratory mechanisms and responses, making comparisons and the control of sick children more feasible. In this line, evaluating the repercussion of a submaximal exercise test like the 6MWT in the airways of healthy children and adolescents seems relevant.

The 6MWT has been indicated for the adult and pediatric populations to evaluate functional capacity, in epidemiological research proposals, monitoring of interventions effectiveness, and especially as a parameter for response to pulmonary rehabilitation programs and follow-up of physiotherapeutic protocols.1818. Priesnitz CV, Rodrigues GH, Stumpf CS, Viapiana G, Cabral CP, Stein RT, et al. Reference values for the 6-min walk test in healthy children aged 6-12 years. Pediatr Pulmonol. 2009;44:1174-9.,1919. Okuro RT, Schivinski CI. Six-minute walk test in pediatrics: the relationship between performance and anthropometric parameters. Fisioter Mov. 2013;26:219-28. Its repercussion in parameters of non-invasive, easy-to-perform, safe and validated methods of evaluation for the pediatric population, such as IOS and spirometry, has been poorly investigated yet. Thus, to date, there are no studies evaluating the repercussion of a submaximal exertion test on IOS and spirometry variables in children and adolescents. That being said, the purpose of this study was to verify the behavior of respiratory mechanics and pulmonary function in schoolchildren submitted to 6MWT.

METHOD

This is a cross-sectional study with schoolchildren and approved by the Research Ethics Committee of Universidade do Estado de Santa Catarina (UDESC), under protocol 99/2011, conducted in Florianópolis (Santa Catarina, Brazil). Data was collected in public and private institutions of primary and secondary education in the Greater Florianópolis region from October 2012 to December 2014. Children’s caregivers/guardians were informed about the study and, upon agreeing to participate, they signed the informed consente form and fulfilled the ISAAC questionnaire’s (International Study of Asthma and Allergies in Childhood) modules on asthma and rhinitis, in the version validated for the Brazilian Portuguese language.2020. Solé D, Vanna AT, Yamada E, Rizzo MC, Naspitz CK. International study of asthma and allergies in childhood (ISAAC) written questionnaire: validation of the asthma component among Brazilian children. J Investig Allergol Clin Immunol. 1997;8:376-82.,2121. Vanna AT, Yamada E, Arruda LK, Naspitz CK, Solé D. International study of asthma and allergies in childhood: validation of the rhinitis symptom questionnaire and prevalence of rhinitis in schoolchildren in São Paulo, Brazil. Pediatr Allergy Immunol. 2001;12:95-101.

The sample was assembled by selection of participants in the study to determine reference equations for IOS among healthy Brazilian children and adolescents.2222. Assumpção MS, Gonçalves RM, Martins R, Bobbio TG, Schivinski CI. Reference equations for impulse oscillometry system parameters in Brazilian healthy children and adolescents. Respir Care. 2016;61:1090-9. This study included schoolchildren of both sexes, aged between 6 and 14 years, no history of prematurity or passive exposure to smoking, no respiratory infection up to two weeks prior to evaluations and no respiratory impairment such as asthma and allergic rhinitis, according to the cut-off scoring proposed by ISAAC:

  • asthma module: ≥5 points for children aged 6 to 9 years; ≥6 points for children aged 10 to 14 years)2020. Solé D, Vanna AT, Yamada E, Rizzo MC, Naspitz CK. International study of asthma and allergies in childhood (ISAAC) written questionnaire: validation of the asthma component among Brazilian children. J Investig Allergol Clin Immunol. 1997;8:376-82.,2323. Behl RK, Kashyap S, Sarkar M. Prevalence of bronchial asthma in school children of 6-13 years of age in Shimla City. Indian J Chest Dis Allied Sci. 2010;52:145-8.;

  • Allergic rhinitis module: ≥4 points for children aged 6 to 9 years; ≥3 points for children aged 10 to 14 years).2020. Solé D, Vanna AT, Yamada E, Rizzo MC, Naspitz CK. International study of asthma and allergies in childhood (ISAAC) written questionnaire: validation of the asthma component among Brazilian children. J Investig Allergol Clin Immunol. 1997;8:376-82.,2121. Vanna AT, Yamada E, Arruda LK, Naspitz CK, Solé D. International study of asthma and allergies in childhood: validation of the rhinitis symptom questionnaire and prevalence of rhinitis in schoolchildren in São Paulo, Brazil. Pediatr Allergy Immunol. 2001;12:95-101.

Children who failed to perform all stages of the assessment properly were excluded.

Weight was measured on a digital glass scale Ultra Slim W903 Wiso® (Santa Catarina, Brazil), and height by a portable stadiometer Sanny® (São Paulo, Brazil). Body mass index (BMI) was defined according to the percentile curves proposed by the World Health Organization (WHO) (http://www.telessaudebrasil.org.br/apps/calculadoras/page=7).2424. Brazil - Ministério da Saúde [homepage on the Internet]. Telessaúde Brasil Redes [cited 2015 may 15]. Available from: http://www.telessaudebrasil.org.br/apps/calculadoras/page=7
http://www.telessaudebrasil.org.br/apps/...

All participants underwent forced expiratory maneuvers of spirometry by the JaegerTM MasterScreenTM IOS (Erich Jaeger, Germany) (spirometry module), as recommended by both ATS and ERS.1313. Miller MR, Hankinson J, Brusasco V, Burgos F, Casaburi R, Coates A, et al. Standardisation of spirometry. Eur Respir J. 2005;26:319-38. In order to avoid excessive maneuvers, which could interfere with results interpretation, each participant made three or four forced expiratory maneuvers, respecting the criteria of three acceptable maneuvers and two reproducible maneuvers.

Respiratory mechanics was analyzed in the IOS JaegerTM MasterScreenTM system (Erich Jaeger, Germany) (impulse oscillometry module) coupled to the same equipment, as per ATS/ERS standards.2525. Beydon N, Lombardi E, Allen J, Arets H, Aurora P, Bisgaard H, et al. An official American Thoracic Society/European Respiratory Society statement: pulmonary function testing in preschool children. Am J Respir Crit Care Med. 2007;175:1304-45.,2626. Oostveen E, MacLeod D, Lorino H, Farré R, Hantos Z, Desager K, et al. The forced oscillation technique in clinical practice: methodology, recommendations and future developments. Eur Respir J. 2003;22:1026-41. Children were instructed to spontaneously breathe at tidal volume, with the mouth engaged in a mouthpiece. Recording time for data acquisition was set between 20 and 30 seconds, with three measurements each. The best measure of these three was considered, complying with the criteria of maneuverability and 10% minimum difference between their parameters. The following parameters were taken into account: total (R5) and central (R20) respiratory resistance; respiratory reactance (X5), respiratory impedance (Z5), resonance frequency (Fres), and reactance area (AX).

Functional capacity was assessed with the 6MWT, conducted according to recommendations of ATS88. ATS Committee on Proficiency Standards for Clinical Pulmonary Function Laboratories. ATS statement: guidelines for the six-minute walk test. Am J Respir Crit Care Med. 2002;166:111-7. in a 30-meter flat covered corridor. Polar Fs2c BLK® digital timer (Kempele, Finland) was used, as well as Nonin Onyx 9500® digital oximeter (Minnesota, USA) to measure heart rate (fc) and peripheral oxygen saturation (SpO2), and Prestige Medical® sphygmomanometer (California, United States) to measure blood pressure (BP). Dyspnea sensation was measured by the modified Borg scale. Values proposed for the distance covered were based in the equation of Priesnitz et al.1818. Priesnitz CV, Rodrigues GH, Stumpf CS, Viapiana G, Cabral CP, Stein RT, et al. Reference values for the 6-min walk test in healthy children aged 6-12 years. Pediatr Pulmonol. 2009;44:1174-9. for Brazilian children.

IOS parameters and spirometry were analyzed in resting conditions, that is, before the first 6MWT (pre-6MWT), immediately after the first 6MWT (post-6MWT1) and after the second 6MWT (post-6MWT2), as shown in Figure 1. In addition to hygiene for current research, the final sample was required to hold children and adolescents who had not exceeded the total number of 12 forced expiratory maneuvers in spirometry considering the three stages of evaluation (pre-6MWT, post-6MWT1 and post-6MWT2).

Figure 1
Flowchart of the sequence of procedures taken to evaluate repercussions of the six-minute walk test on respiratory mechanics and lung function in healthy schoolchildren.

To calculate sample size, we considered a pilot study involving healthy children aged 7 to 14 years. Due to its representativeness in total mechanical load of the respiratory system, the variable selected to check for changes in a more specific way was respiratory impedance. Participants had mean pre-6MWT1 of 0.5 kPa/L/h and standard deviation of 0.11 kPa/L/s and post-6MWT2 of 0.6 kPa/L/s, with standard deviation of 0.15 kPa/L/s, with difference detected of 0.1 kPa/L/s. Significance level was set at 5%, with test power of 80%. With these estimates, the adequate sample should allocate 19 individuals.

Data were nalyzed in the Statistical Package for the Social Sciences® (SPSS) software 20.0 (IBM, New York, USA). Initially, we verified data distribution by means of the Shapiro Wilk test and then applied the ANOVA (post-hoc Bonferroni) test for repeated measures or the Friedman’s test to compare results in the three phases of assessment. Significance was set at 5% (p≤0.05).

RESULTS

Of total 864 children and adolescents evaluated in the study by Assumpção et al.2222. Assumpção MS, Gonçalves RM, Martins R, Bobbio TG, Schivinski CI. Reference equations for impulse oscillometry system parameters in Brazilian healthy children and adolescents. Respir Care. 2016;61:1090-9., in which 123 individuals participated, 21 schoolchildren (10 boys) were able to perform the spirometric maneuvers according to preestablished inclusion criteria and constituted the final sample.

The students’ age ranged from 7 to 14 years, with mean 10.9 years. There were no participant losses during tests (intercurrences and/or withdrawals), and all students met the criteria determined for the present study.

Descriptive data regarding weight, height, BMI and distance traveled in the 6MWT are shown in Table 1. Complying with WHO classification, the sample consisted of 21 children, 14 being classified as eutrophic (adequate weight) and seven as non-eutrophic (four overweight and three obese). There were no differences between baseline cardiorespiratory parameters of spirometric variables and oscillometric parameters in the study.

Table 1
Mean and standard deviation of anthropometric variables.

Only nine children performed better than expected when considering reference values for Brazilian children. The description of cardiorespiratory parameters for the first and the second 6MWT is found in Table 2.

Table 2
Description of cardiopulmonary parameters of first and second six-minute walk tests.

After the two tests, a difference between parameters of total airway resistance (R5) and central airway resistance (R20) (p=0.041 and p=0.025, respectively) was observed (Table 3). Significant increase in R5 was observed after post-hoc analysis (R5: 0.540±0.110 versus 0.590±0.150 kPa/L/s, p=0.013), as well as R20 (0.440±0.800 versus 0.470±0.100 kPa/L/s, p=0.038). The increase in R20 was also significant when comparing pre-6MWT and post-6MWT2 (0.440±0.800 versus 0.470±0.110 kPa/L/s, p=0.034).

Table 3
Analysis of oscillometric parameters Pre-6MWT, Post-6MWT1 and Post-6MWT2.

The only spirometric variable that showed significant change after tests was forced expiratory flow between 25-75% (FEF25-75%) (p=0.003), identified in Friedman’s test. Multiple analysis was used to detail the timing of this change. This parameter was shown to decrease between pre and post-6MWT1 moments (85,900±19,900% versus 80,800±20,200%, p=0,010), as well as in pre and post-6MWT2. FEF25-75% (Z score) also changed when compared to pre-6MWT and post-6MWT2 (p=0.001). In the present study, only four infants presented baseline FEF25-75% values below 70% (Table 4).

Table 4
Analysis of spirometric parameters Pre-6MWT, Post-6MWT1 and Post-6MWT2.

DISCUSSION

The analysis of respiratory mechanics behavior and lung function in schoolchildren undergoing submaximal exertion tests leads to the understanding of respiratory system changes. In particular, the present study demonstrated that the 6MWT changed the spirometric variable FEF25-75%. Considered an important measure of respiratory flows, it allows evaluation of airway permeability, since it represents the airflow speed exclusively from the bronchi.2727. Costa D, Jamami M. Bases fundamentais da espirometria. Rev Bras Fisioter. 2001;5:95-102. This parameter was decreased after both the first and the second test, demonstrating the effort performed after a submaximal exercise, accompanied by an increase in total (R5) and central (R20) respiratory resistance.

In this sense, this study on pulmonary function assessed by spirometry before and after the 6MWT showed that this test does not cause a decrease in lung volumes or capacities, which affirms its safe applicability in the sample; however, a significant decrease in the spirometric variable FEF25-75% was seen. This variable represents the mean forced expiratory flow of a segment during forced vital capacity maneuver (FVC), which includes the airway flow of medium and small gauges and is considered a sensitive parameter to detect small airway obstruction.2828. Gontijo PL, Lima TP, Costa TR, Reis EP, Cardoso FP, Cavalcanti Neto FF. Correlation of spirometry with the six-minute walk test in eutrophic and obese individuals. Rev Assoc Med Bras. 2011;57:387-93.,2929. Rodrigues JC, Takahashi A, Olmos FM, Souza JB, Bussamra MH, Cardieri JM. Effect of body mass index on asthma severity and exercise-induced bronchial reactivity in overweight and obese asthmatic children. Rev Paul Pediatr. 2007;25:207-13. This response after the 6MWT may be analogous to bronchoconstrictive effect of small airways after exercise.2929. Rodrigues JC, Takahashi A, Olmos FM, Souza JB, Bussamra MH, Cardieri JM. Effect of body mass index on asthma severity and exercise-induced bronchial reactivity in overweight and obese asthmatic children. Rev Paul Pediatr. 2007;25:207-13. Fonseca et al.3030. Fonseca-Guedes CH, Cabral AL, Martins MA. Exercise-induced bronchospasm in children: comparison of FEV1 and FEF25-75% responses. Pediatr Pulmonol. 2003;36:49-54. discussed this effect in a study using spirometry after bronchoprovocation by exercise in children with ashtma of varying levels of severity. They found that this biomarker may be reduced in response to exercise, especially in children with mild asthma, and recommended its use, along with first-second forced expiratory volume (FEV1), as a criterion for bronchoconstricting response to exercise.2929. Rodrigues JC, Takahashi A, Olmos FM, Souza JB, Bussamra MH, Cardieri JM. Effect of body mass index on asthma severity and exercise-induced bronchial reactivity in overweight and obese asthmatic children. Rev Paul Pediatr. 2007;25:207-13.

This study also analyzed IOS response to 6MWT and identified a significant increase in R5 after the test (p=0.028). IOS has been used to analyze the effects of procedures and therapeutics. In this sense, Lee et al.3131. Lee JY, Seo JH, Kim HY, Jung YH, Kwon JW, Kim BJ, et al. Reference values of impulse oscillometry and its utility in the diagnosis of asthma in young Korean children. J Asthma. 2012;49:811-6. evaluated the characteristics of airway obstruction in 47 asthmatic young patients (mean age 20.7 years) after a bronchoprovocation test with treadmill methacholine, and reported that R5 increased in the group showing hyperresponsive airways at 5 and 10 minutes after the end of the test. The authors concluded that IOS may be useful for objective assessments and to improve understanding of exercise-induced airway obstruction in young asthmatics. This finding places IOS as a useful tool for early diagnosis of asthma. In our research, increase in R5 after 6MWT can also be justified by the instability of small airways during physical effort, although it is a relatively fast stimulus and involves submaximal effort.

In addition to asthma, IOS has been considered relevant for cystic fibrosis. Vendrusculo et al.3232. Vendrusculo FM, Heinzmann-Filho JP, Piva TC, Marostica PJ, Donadio MV. Inspiratory muscle strength and endurance in children and adolescents with cystic fibrosis. Respir Care. 2016;61:184-91. revealed a relationship between respiratory muscle strength and lung mechanics in this population, while Díez et al.3333. Díez JM, Villa Asensi JR, Vecchi AA. Resistance by oscillometry. Comparison of its behavior in patients with asthma and cystic fibrosis. Rev Clin Esp. 2006;206:95-7. found correlations between FEV1 and some oscillometric parameters (Z, R5, X5). Moreau et al.3434. Moreau L, Crenesse D, Berthier F, Albertini M. Relationship between impulse oscillometry and spirometric indices in cystic fibrosis children. Acta Paediatr. 2009;98:1019-23. had already identified an inverse relationship between R5, Z and Fres values and spirometric parameters such as FEV1 in 15 children with cystic fibrosis aged 4 to 19 years.

Complementarily, IOS and spirometry have been recently used to assess lung function of 2,621 Swedish school-age children (149 preterm and 2,472 at term). The authors observed that at 8 years of age FEV1 was lower in preterm versus term females, but not in preterm males. For the preterm group, IOS showed increased resistance adjusted at 5 Hz for males compared to the same term group.3535. Thunqvist P, Gustafsson PM, Schultz ES, Bellander T, Berggren-Broström E, Norman M, et al. Lung function at 8 and 16 years after moderate-to-late preterm birth: a prospective cohort Study. Pediatrics. 2016;137.

Studies using these both instruments and relating them to exercise testings, likewise the present research, as well as evaluating healthy populations are scarce. IOS has been used as a tool to identify and monitor respiratory system changes due to dysfunctions such as asthma and cystic fibrosis, which makes it difficult to compare and establish normality parameters. In this context, studies on the understanding and use of respiratory resistance measurements arre still infrequent and require clarification.

Regarding these findings, the proportion of overweight and obese children was checked and, after detailed statistical analysis, no difference was found between spirometric and oscillometric values between participants. Therefore, we chose not to create groupings associated with body mass. As for ethnicity, all participnts were classified as White. The literature lacks studies that correlate ethnic differences with performance in the 6MWT, even although pulmonary function is known to be influenced by this characteristic.

To ensure internal and research validity, a strict caution in the control of health history and prematurity was taken in sample selection, in addition to the verification of absence of pulmonary diseases and spirometric values according to normality, so that participants of both groups would not interfere with these factors. Also, possible bias regarding the repercussion of forced expiratory maneuvers was avoided, as inclusion criterias was limited to children who did not exceed 12 maneuvers. Although the sample was small, it reached the previous sample calculation and, with the possible biases under control, it seems to have been representative of healthy schoolchildren. The selection of participants and inclusion criteria, such as maximum number of forced expiratory maneuvers, made it possible to control the external validity of the study, as well as the absence of a relationship between 6MWT and students being considered eutrophic or not.

The importance of this study is the possibility of clarifying the relationship between IOS and other evaluation instruments, especially those already established in the scientific community, such as spirometry and the 6MWT. Multicentric studies with separate individuals grouped by gender, weight and age, height and ethnicity, are necessary to achieve accuracy of results found by the present study. Thus, understanding physiological and respiratory responses to physical effort should be guided by studies with larger samples.

The present study examined respiratory mechanics and lung function in children and adolescents submitted to the 6MWT and identified an increase in airway resistance (total and central), as well as a significant decrease in FEF25-75% after the test. These findings point to more attention and caution when performing submaximal tests in children presenting with predisposition to airway abnormalities, especially when undergoing exercise testings, as performed with children with asthma and cystic fibrosis.

REFERÊNCIAS

  • 1
    Aquino ES, Mourão FA, Souza RK, Glicério BM, Coelho CC. Comparative analysis of the six-minute walk test in healthy children and adolescentes. Rev Bras Fisioter. 2010;14:75-80.
  • 2
    Lammers AE, Hislop AA, Flynn Y, Haworth SG. The 6-minute walk test: normal values for childrenof 4-11 years of age. Arch Dis Child. 2008;93:464-8.
  • 3
    Boyce D, Pullins E, McCormack MC, Mathai SC, Khair R. Safety of the six-minute walk test in chronic lung disease. Abstract of the American Thoracic Society 2016 International Conference; 2016 May 13-18; San Francisco, USA. p. A5722.
  • 4
    Geiger R, Strasak A, Treml B, Gasser K, Kleinsasser A, Fischer V, et al. Six-minute walk test in children and adolescents. J Pediatr. 2007;150:395-9.
  • 5
    Saad HB, Prefaut C, Missaoui R, Mohamed IH, Tabka Z, Hayot M. Reference equation for 6-min walk distance in healthy North African children 6-16 years old. Pediatr Pulmonol. 2009;44:316-24.
  • 6
    Klepper SE, Muir N. Reference values on the 6-minute walk test for children living in the United States. Pediatr Phys Ther. 2011;23:32-40.
  • 7
    Bartels B, Groot JF, Terwee CB. The six-minute walk test in chronic pediatric conditions: a systematic review of measurement properties. Phys Ther. 2013;93:529-41.
  • 8
    ATS Committee on Proficiency Standards for Clinical Pulmonary Function Laboratories. ATS statement: guidelines for the six-minute walk test. Am J Respir Crit Care Med. 2002;166:111-7.
  • 9
    Holland AE, Spruit MA, Troosters T, Puhan MA, Pepin V, Saey D, et al. An official European Respiratory Society/American Thoracic Society technical standard: field walking tests in chronic respiratory disease. Eur Respir J. 2014;44:1428-46.
  • 10
    Gotshall RW. Airway response during exercise and hyperpnoea in non-asthmatic and asthmatic individuals. Sports Med. 2006;36:513-27.
  • 11
    Wanrooij VH, Willeboordse M, Dompeling E, Kant KD. Exercise training in children with asthma: a systematic review. Br J Sports Med. 2014;48:1024-31.
  • 12
    Parsons JP, Hallstrand TS, Mastronarde JG, Kaminsky DA, Rundell KW, Hull JH, et al. An official American Thoracic Society clinical practice guideline: exercise-induced bronchoconstriction. Am J Respir Crit Care Med. 2013;187:1016-27.
  • 13
    Miller MR, Hankinson J, Brusasco V, Burgos F, Casaburi R, Coates A, et al. Standardisation of spirometry. Eur Respir J. 2005;26:319-38.
  • 14
    Komarow HD, Myles IA, Uzzaman A, Metcalfe DD. Impulse oscillometry in the evaluation of diseases of the airways in children. Ann Allergy Asthma Immunol. 2011;106:191-9.
  • 15
    Shirai T, Kurosawa H. Clinical application of the forced oscillation technique. Intern Med. 2016;55:559-66.
  • 16
    Assumpção MS, Gonçalves RM, Ferreira LG, Schivinski CI. Impulse oscillometry system in pediatrics: review. Medicina (Ribeirão Preto). 2014;47:131-42.
  • 17
    Bickel S, Popler J, Lesnick B, Eid N. Impulse oscillometry: interpretation and practical applications. Chest. 2014;146:841-7.
  • 18
    Priesnitz CV, Rodrigues GH, Stumpf CS, Viapiana G, Cabral CP, Stein RT, et al. Reference values for the 6-min walk test in healthy children aged 6-12 years. Pediatr Pulmonol. 2009;44:1174-9.
  • 19
    Okuro RT, Schivinski CI. Six-minute walk test in pediatrics: the relationship between performance and anthropometric parameters. Fisioter Mov. 2013;26:219-28.
  • 20
    Solé D, Vanna AT, Yamada E, Rizzo MC, Naspitz CK. International study of asthma and allergies in childhood (ISAAC) written questionnaire: validation of the asthma component among Brazilian children. J Investig Allergol Clin Immunol. 1997;8:376-82.
  • 21
    Vanna AT, Yamada E, Arruda LK, Naspitz CK, Solé D. International study of asthma and allergies in childhood: validation of the rhinitis symptom questionnaire and prevalence of rhinitis in schoolchildren in São Paulo, Brazil. Pediatr Allergy Immunol. 2001;12:95-101.
  • 22
    Assumpção MS, Gonçalves RM, Martins R, Bobbio TG, Schivinski CI. Reference equations for impulse oscillometry system parameters in Brazilian healthy children and adolescents. Respir Care. 2016;61:1090-9.
  • 23
    Behl RK, Kashyap S, Sarkar M. Prevalence of bronchial asthma in school children of 6-13 years of age in Shimla City. Indian J Chest Dis Allied Sci. 2010;52:145-8.
  • 24
    Brazil - Ministério da Saúde [homepage on the Internet]. Telessaúde Brasil Redes [cited 2015 may 15]. Available from: http://www.telessaudebrasil.org.br/apps/calculadoras/page=7
    » http://www.telessaudebrasil.org.br/apps/calculadoras/page=7
  • 25
    Beydon N, Lombardi E, Allen J, Arets H, Aurora P, Bisgaard H, et al. An official American Thoracic Society/European Respiratory Society statement: pulmonary function testing in preschool children. Am J Respir Crit Care Med. 2007;175:1304-45.
  • 26
    Oostveen E, MacLeod D, Lorino H, Farré R, Hantos Z, Desager K, et al. The forced oscillation technique in clinical practice: methodology, recommendations and future developments. Eur Respir J. 2003;22:1026-41.
  • 27
    Costa D, Jamami M. Bases fundamentais da espirometria. Rev Bras Fisioter. 2001;5:95-102.
  • 28
    Gontijo PL, Lima TP, Costa TR, Reis EP, Cardoso FP, Cavalcanti Neto FF. Correlation of spirometry with the six-minute walk test in eutrophic and obese individuals. Rev Assoc Med Bras. 2011;57:387-93.
  • 29
    Rodrigues JC, Takahashi A, Olmos FM, Souza JB, Bussamra MH, Cardieri JM. Effect of body mass index on asthma severity and exercise-induced bronchial reactivity in overweight and obese asthmatic children. Rev Paul Pediatr. 2007;25:207-13.
  • 30
    Fonseca-Guedes CH, Cabral AL, Martins MA. Exercise-induced bronchospasm in children: comparison of FEV1 and FEF25-75% responses. Pediatr Pulmonol. 2003;36:49-54.
  • 31
    Lee JY, Seo JH, Kim HY, Jung YH, Kwon JW, Kim BJ, et al. Reference values of impulse oscillometry and its utility in the diagnosis of asthma in young Korean children. J Asthma. 2012;49:811-6.
  • 32
    Vendrusculo FM, Heinzmann-Filho JP, Piva TC, Marostica PJ, Donadio MV. Inspiratory muscle strength and endurance in children and adolescents with cystic fibrosis. Respir Care. 2016;61:184-91.
  • 33
    Díez JM, Villa Asensi JR, Vecchi AA. Resistance by oscillometry. Comparison of its behavior in patients with asthma and cystic fibrosis. Rev Clin Esp. 2006;206:95-7.
  • 34
    Moreau L, Crenesse D, Berthier F, Albertini M. Relationship between impulse oscillometry and spirometric indices in cystic fibrosis children. Acta Paediatr. 2009;98:1019-23.
  • 35
    Thunqvist P, Gustafsson PM, Schultz ES, Bellander T, Berggren-Broström E, Norman M, et al. Lung function at 8 and 16 years after moderate-to-late preterm birth: a prospective cohort Study. Pediatrics. 2016;137.

Funding

  • Coordination for the Improvement of Higher Level Personnel (CAPES) scholarship.

Publication Dates

  • Publication in this collection
    29 Oct 2018
  • Date of issue
    Oct-Dec 2018

History

  • Received
    04 Apr 2017
  • Accepted
    08 Oct 2017
  • Published
    23 Oct 2018
Sociedade de Pediatria de São Paulo R. Maria Figueiredo, 595 - 10o andar, 04002-003 São Paulo - SP - Brasil, Tel./Fax: (11 55) 3284-0308; 3289-9809; 3284-0051 - São Paulo - SP - Brazil
E-mail: rpp@spsp.org.br