Brazilian Journal of Pulmonology

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Current Issue: 2011 - Volume 37 - Number 4 (July/August)

ORIGINAL ARTICLE

Early termination of exhalation: effect on spirometric parameters in healthy preschool children

Efeito da terminação precoce da expiração nos parâmetros espirométricos em crianças pré-escolares saudáveis

 

Edjane Figueiredo Burity; Carlos Alberto de Castro Pereira; José Ângelo Rizzo; Emanuel Sávio Cavalcanti Sarinho; Marcus Herbert Jones

 

Abstract

Objective: To evaluate the acceptability and reproducibility of spirometry in preschool children; to estimate the effect size of early termination of exhalation (ETE) on FVC, FEV1 and FEV0.5; and to evaluate the validity of FEV0.5 in curves with ETE. Methods: Spirometric data were obtained from 240 healthy preschool children, who were selected by simple sampling. On the basis of the best curve from each child according to the end of exhalation, three groups were formed: no ETE (nETE); ETE and flow ≤ 10% of the highest PEF (ETE≤10); and ETE and flow > 10% of the highest PEF value (ETE>10). The reproducibility of FVC, FEV1 and FEV0.5 was compared among the three groups. The effect of ETE on FVC, FEV1, and FEV0.5 was assessed. Results: Of the 240 children tested, 112 (46.5%)-82 (34.0%) of those in the nETE group and 30 (12.5%) of those in the ETE≤10 group-had acceptable curves for all the parameters. In 64 (27.0%) of those in the ETE>10 group, the curves were acceptable only for FEV0.5, increasing the proportion of children with valid FEV0.5 to 73.0%. There were no significant differences between the nETE and ETE≤10 groups in terms of the mean values of the parameters assessed. Conclusions: Maneuvers with ETE and flow ≤ 10% of the highest PEF are valid. In individuals with a flow > 10% of the highest PEF value, these maneuvers are only valid for FEV0.5.

 

Resumo

Objetivo: Avaliar a aceitabilidade e a reprodutibilidade da espirometria em pré-escolares; estimar o tamanho do efeito da terminação precoce da expiração (TPE) nos valores de CVF, VEF1 e VEF0,5; e avaliar a validade do VEF0,5 em curvas com TPE. Métodos: Espirometrias foram obtidas em 240 pré-escolares saudáveis, selecionados por amostragem simples. Três grupos foram formados com base na melhor curva de cada criança de acordo com o término da expiração: sem TPE (sTPE); com TPE e fluxo ≤ 10% do maior PFE (TPE≤10); e com TPE e fluxo > 10% do maior PFE (TPE>10). Foram comparadas a reprodutibilidade da CVF, VEF1 e VEF0,5 nos três grupos. Foi avaliado o efeito da TPE em CVF, VEF1 e VEF0,5. Resultados: Das 240 crianças testadas, 112 (46.5%) realizaram curvas aceitáveis para todos os parâmetros - 82 (34,0%) no grupo sTPE e 30 (12,5%) no grupo TPE≤10. Em 64 (27,0%) no grupo TPE>10, as curvas foram aceitáveis apenas para VEF0,5, aumentando para 73,0% a proporção de crianças com VEF0,5 válido. Não houve diferenças significantes nas médias dos parâmetros avaliados entre os grupos sTPE e TPE≤10. Conclusões: Manobras com TPE e fluxo ≤ 10% do maior PFE são válidas. Em indivíduos com fluxo > 10% do maior PFE, essas manobras são válidas somente para VEF0,5.

 

 

Keywords: Spirometry; Child, preschool; Vital capacity; Forced expiratory volume; Reproducibility of results.

 

Palavras-chave: Espirometria; Pré-escolar; Capacidade vital; Volume expiratório forçado; Reprodutibilidade dos testes.

 

 

Introduction

For the last 10 years, spirometry has been used for the functional evaluation of preschool children.(1-9) The publication of reference values and study reports, showing that 40-90% of preschool children can perform spirometry appropriately, has promoted its use in clinical practice.(1-8)

The acceptability criteria for spirometry in adults, standardized by the American Thoracic Society (ATS),(10) cannot be applied to children, especially because of the brevity of the expiratory maneuver, usually lasting less than 2-3 s. The major technical limitation is early termination of exhalation (ETE), characterized by the sudden interruption of exhalation. To allow for ETE, the following criteria for acceptable curves have been proposed(5,8,9): minimum flows ≤ 25% of the highest PEF; minimum flows ≤ 10% of the highest PEF; and minimum flows ≤ 0.3 L/s. Considering the high frequency of ETE in the spirometric tests of preschool children, the ATS has proposed that the acceptability criteria be relaxed, and that curves with minimum flows ≤ 10% of the highest PEF be accepted.(11) Although this relaxation of the criteria allows curves with ETE to be accepted, the clinical usefulness of such curves needs to be confirmed by determining their reproducibility.

In a recent paper focusing on preschool children, it was recommended that, for FVC and FEV1, the reproducibility criterion be a flow ≤ 0.10 L or ≤ 10% of the highest PEF, whichever is greater.(11) Regarding the reproducibility of FEV0.5, only two studies have evaluated it, and they did not reach a consensus regarding the criterion adopted for curve termination.(3,4)

The disagreement among the authors of the various studies cited regarding whether or not curves with ETE are valid is explained by the lack of studies testing this validity. The limit of 10% of the PEF has been adopted arbitrarily and has not been validated experimentally. The objectives of the present study were to evaluate the acceptability and reproducibility of spirometry in preschool children (3-6 years of age); to estimate the effect size of ETE on FVC, FEV1, and FEV0.5; and to evaluate the validity of FEV0.5 in curves with ETE > 10% of the highest PEF, but with forced expiratory time (FET) ≥ 0.5 s.

Methods

This was a prospective cross-sectional study. The target population consisted of healthy preschool children, 3-6 years of age, selected by simple sampling at public schools, private schools, and public day care centers in the city of Recife, Brazil, and evaluated between February of 2005 and December of 2006. Of the 682 schools and day care centers, 17 were selected by random sampling. From those 17 facilities, a total of 315 children were recruited. Because the present study also aimed to generate reference values, only the children considered to be free of respiratory diseases (asthma and other acute and chronic respiratory diseases) underwent testing. For classifying children as normal, we used the ATS questionnaire known as ATS-DLD-78-C, which is recommended by the Epidemiology Standardization Project and has been adapted and validated for use in Brazil(12) The questionnaire was completed by the parents or legal guardians of the children. For calculating the sample size, we considered the value of 70% as the expected frequency for tests with good reproducibility, in accordance with the study conducted by Nystad et al.(4)

Accepting an error of 6%, with a confidence level of 95%, we calculated the minimum sample size to be 225 children. To compensate for losses due to any cause, we increased the sample size by 40%, and we therefore initiated the study with 315 children. After administration of the questionnaire, 240 children were considered to be free of respiratory abnormalities and were consequently included in the study.

Children with a birth weight < 2,500 g were excluded, as were those born at a gestational age < 37 weeks, those who had respiratory distress at birth, those who had previously performed spirometry, and those with previous or current heart disease.

The study was approved by the local research ethics committee. The parents or legal guardians of the children gave written informed consent.
All tests were performed with MultiSPIROT spirometers (WinDX Revelation 1.0.64; Creative Biomedics, San Clemente, CA, USA). At the time of testing, each child was trained individually. With a nose clip in place, the children were instructed to perform the test standing up, in accordance with the standard technique.(13) The test sessions were suspended if the acceptability criteria were not met after an average of twelve attempts or, before that, if the child showed fatigue or disinterest.
All tests were performed by one of the study authors, who is experienced in performing spirometry in children. Only tests with at least two acceptable curves were included in the analysis. The acceptability criteria were independently evaluated by two other study authors.

The parameters evaluated were as follows: PEF; FVC; FEV1; FEV0.5; and FEF25-75%. The FVC and FEV1 values were obtained from the best curves, in accordance with standard recommendations.(13) The FEV0.5 values were obtained from the curves with the highest FEV1 value or the highest FEV0.5 value, when FET was < 1 s.

The acceptability criteria for the expiratory curves were as follows: FET ≥ 0.5 s; no artifacts (no cough and no early glottal closure); no inspiratory pause (hesitation); evidence of maximal effort (PEF showing a clear and reproducible peak); and back-extrapolated volume < 5% of FVC.
Because there is no consensus regarding the criterion for curve
termination in this age group,(5,6,8,9) the acceptable tests were divided into three groups, based on the criterion for curve termination, in order to determine the validity of partial maneuvers-no child was classified as belonging to more than one group. For the analysis, we selected only the tests with at least two acceptable curves and with reproducible FVC and FEV1 values ≤ 10% or ≤ 0.1 L. The best curve from each child was classified according to the end of exhalation as follows:

 No ETE (nETE): a full exhalation was clearly seen in the flow-volume curve, with a plateau of at least 1 s in the volume-time curve
 ETE and flow ≤ 10% of the highest PEF (ETE≤10%): this point was determined by grading the flow axis of the flow-volume curve with the use of a millimeter ruler
 ETE and flow > 10% of the highest PEF (ETE>10), with FET ≥ 0.5 s
Examples of the three types of acceptable flow-volume curves are shown in Figure 1.





The Epi Info software, version 6.04, and the Statistical Package for the Social Sciences, version 11.0 (SPSS Inc., Chicago, IL, USA), were used for the statistical analysis. The values are expressed as means and standard deviation. For the comparison of the three types of curves adopted, we used F-tests (ANOVA), Student's t-test, and Duncan's test. For a better evaluation of the results of these tests, we performed multiple linear regression analysis of the nETE and ETE≤10 groups, using FVC as the dependent variable; the independent variables were weight, age, group, gender, and height. The kappa coefficient was used for evaluating inter-rater reliability in the selection of acceptable curves. The variability of the measurements performed was assessed by calculating the mean and standard deviation of the difference between the highest and second highest values for each parameter analyzed (PEF, FVC, FEV1, and FEV0.5), separated by type of curve, with the Kruskal-Wallis and Mann-Whitney tests.

Results

Of the 315 children initially evaluated, 56 (18%) were excluded because of a diagnosis of asthma and 19 (6%) were excluded for various reasons (e.g., preterm birth, low weight, heart disease, and declining to undergo testing). Therefore, 240 children underwent testing and were distributed by age as follows: 3 years, 39 (16%); 4 years, 81 (34%); 5 years, 107 (45%); and 6 years, 13 (5%). The characteristics of the sample are detailed in Table 1.





Among the 240 children tested, we obtained at least two acceptable curves in 82 (34.0%) of those in the nETE group; in 30 (12.5%) of those in the ETE≤10 group; and in 64 (27%) of those in the ETE>10 group (Table 2). In the last group, only the FEV0.5 and PEF values were considered. Analyzing the first two groups together, we found that 112 children (46.5%) performed acceptable maneuvers, in accordance with the current guidelines of the ATS and of the European Respiratory Society (ERS).




Considering the nETE and ETE≤10 groups collectively and by age (% of those in the sample as a whole), we obtained at least two acceptable curves in 9 children in the 3-year-old group (7.4%); in 36 children in the 4-year-old group (29.5%); and in 65 children in the 5-year-old group (53.3%), demonstrating that acceptability increases with age. Considering the ETE>10 group alone, we obtained at least two acceptable curves in 14 children in the 3-year-old group (22.0%); in 35 children in the 4-year-old group (54.7%); and in 15 children in the 5-year-old group (23.4%).

Therefore, nearly 77% of the children producing at least two acceptable curves were below 5 years of age. The proportion of children producing at least three acceptable curves was 76%, 64%, and 58% in the nETE, ETE≤10, and ETE>10 groups, respectively. The proportion of children producing at least two acceptable curves was higher than 84% in all three groups.

Regarding the reproducibility of FVC and FEV1, the nETE group, as well as the ETE≤10 group (with at least two acceptable curves), had a rate above 90% when the reproducibility criteria were flows ≤ 0.1 L and ≤ 10% of the highest PEF (Table 3). Regarding the reproducibility of FEV0.5 in relation to the criterion of a flow ≤ 10% of the highest PEF in the children who had at least two acceptable curves, the rate was ≥ 95% for the three groups. In the children who had at least three acceptable curves, the rate was ≥ 81% (data not shown).





The mean values of the parameters assessed were compared among the three groups. Between the nETE and ETE≤10 groups, there was a statistically significant difference only for FVC (data not shown). In order to confirm this difference, we performed multiple linear regression analysis. However, the analysis reviewed no significant difference between the nETE and ETE≤10 groups in terms of FVC (p = 0.346). On average, the FVC values were 27 mL lower in the ETE≤10 group curves than in the nETE group curves. Because the mean FVC value of the latter group was 1,082 mL, this error corresponds to less than 3% (Table 4). Therefore, the ETE≤10 group curves can be considered valid, even in relation to the FVC values.




For the independent selection and classification of curves, we found good inter-rater reliability (kappa coefficient = 0.72), in accordance with the various acceptability criteria adopted. In terms of variability, there were no significant differences among the three types of curves (data not shown).

Discussion

In the present study, we observed that, with the use of stricter acceptability criteria, based on the acceptance of full exhalation curves exclusively, only 34% of the preschool children were able to perform acceptable maneuvers. With the use of more flexible criteria, such as those currently recommended by the ATS/ERS (equivalent to those applied to the ETE≤10 group), that rate was 46.5%. With the acceptance of curves that were less complete (equivalent to those of the ETE>10 group), 73% of the children tested were able to perform maneuvers with reliable and reproducible FEV0.5. The ETE£10 group curves were valid, reliable, and reproducible for FVC, FEV1, and FEV0.5. The ETE>10 group curves, with FET ≥ 0.5 s, were only valid for FEV0.5.

The proportion of acceptable curves in the nETE group (34%) was lower than that reported in a previous study (40%),(6) possibly because of the lower mean age of the children in our study (4.7 years vs. 5.1 years). A recent study, in which the 2007 ATS/ERS recommendations were used, found that 56% of preschool children (4-6 years of age) were able to produce acceptable and reproducible spirometry results.(14) In the present study, that rate was only 46.5%, possibly because our sample was younger, with a predominance of children 3-5 years of age (6-year-olds accounted for only 5% of our sample). A recent study evaluating spirometry results in 76 preschool children with asthma found a high percentage of acceptability (82.4%), with a mean age of 4.8 years, similar to that observed in our sample(15); the differences in the criterion adopted for curve termination might be the explanation for the higher percentage of acceptability (the authors reported that there was a plateau only in the final second). In preschool children, we often observe a plateau in the volume-time curve. However, inspection of the flow-volume curve reveals no correspondence of full exhalation. This is due to a fault in the spirometer program, which maintains the record of a plateau even after the end of exhalation. In some studies of preschool children, the criterion adopted for curve termination is unclear, making it difficult to assess that criterion more accurately, as well as to make comparisons across studies.(2-4) Acceptability was found to increase with age, a finding that is in accordance with data in the literature.(4,6)

Although the number of small children who were able to perform maneuvers in accordance with the 2007 ATS/ERS acceptability criteria was small (7.4% of those aged 3 years and 29.5% of those aged 4 years), with the acceptance of the ETE>10 group curves, FEV0.5 could have been assessed in 20% more of the children tested, raising the proportion of preschool children with available FEV0.5 data to 73%, which would justify the use of spirometry in this age group.

The high reproducibility and low variability of FVC, FEV1, and FEV0.5 in the three groups demonstrates that the measurements performed are reliable. The evidence that the ETE≤10 group curves, which were similar to those recommended by the ATS/ERS in 2007, were reliable and reproducible, validates this standard. Although the confirmed reliability of curves with ETE is a recommended criterion for curve termination in preschool children in the ATS/ERS document,(11) there have been no studies testing that reliability.

The observation that the curves of the ETE>10 also showed high reproducibility and low variability demonstrates that the PEF and FEV0.5 values are reliable and can be used in clinical practice. Other studies have demonstrated that FEV0.5 is reproducible and can be used in the assessment of bronchodilator response.(3,4,9) Vilozni et al. assessed the effect of bronchodilators in children with moderate or severe asthma and observed that, in those with moderate asthma (n = 62), there was, in relation to the baseline value, a response in the mean FEV1 and in the mean FEV0.5 of, respectively, 14% ± 10% and 15% ± 11%, suggesting that the latter would be useful in the assessment of bronchodilator response.(9)

The good inter-rater reliability in the analysis and classification of the maneuvers by group indicates the reliability of the tests.

For younger children who cannot make a full exhalation, curves with partial exhalation, with measurements of FEV1 or only of FEV0.5, can be used in the assessment of respiratory symptoms because they have been proven to be reliable, reproducible, and useful in the assessment of bronchodilator response. The sensitivity of this parameter for the detection of functional abnormalities should be tested in future studies. Similarly, there is a need for studies that will specifically assess cut-off points for bronchodilator response measured by FEV0.5.

It was evident in the present study that, in order to calculate the cut-off point for acceptability of curves with ETE more accurately, more appropriate spirometry programs are necessary, with screens with larger flow-volume curves and two axes with a millimeter ruler. These findings show the need for adapting the spirometry programs to the preschool age group.

Acknowledgments

We would like to thank Prof. Ricardo Ximenes for his assistance in calculating the sample size.

References

1. Lesouef PN, Lafortune BC, Landau LI. Spirometric assessment of asthmatic children aged 2-6 years. Aust NZ Med J. 1986;16:625A.

2. Kanengiser S, Dozor AJ. Forced expiratory maneuvers in children aged 3 to 5 years. Pediatr Pulmonol. 1994;18(3):144-9.

3. Crenesse D, Berlioz M, Bourrier T, Albertini M. Spirometry in children aged 3 to 5 years: reliability of forced expiratory maneuvers. Pediatr Pulmonol. 2001;32(1):56-61.

4. Nystad W, Samuelsen SO, Nafstad P, Edvardsen E, Stensrud T, Jaakkola JJ. Feasibility of measuring lung function in preschool children. Thorax. 2002;57(12):1021-7.

5. Eigen H, Bieler H, Grant D, Christoph K, Terrill D, Heilman DK, et al. Spirometric pulmonary function in healthy preschool children. Am J Respir Crit Care Med. 2001;163(3 Pt 1):619-23.

6. Zapletal A, Chalupová J. Forced expiratory parameters in healthy preschool children (3-6 years of age). Pediatr Pulmonol. 2003;35(3):200-7.

7. Aurora P, Stocks J, Oliver C, Saunders C, Castle R, Chaziparasidis G, et al. Quality control for spirometry in preschool children with and without lung disease. Am J Respir Crit Care Med. 2004;169(10):1152-9.

8. Marostica PJ, Weist AD, Eigen H, Angelicchio C, Christoph K, Savage J, et al. Spirometry in 3- to 6-year-old children with cystic fibrosis. Am J Respir Crit Care Med. 2002;166(1):67-71.

9. Vilozni D, Barker M, Jellouschek H, Heimann G, Blau H. An interactive computer-animated system (SpiroGame) facilitates spirometry in preschool children. Am J Respir Crit Care Med. 2001;164(12):2200-5.

10. Standardization of Spirometry, 1994 Update. American Thoracic Society. Am J Respir Crit Care Med. 1995;152(3):1107-36.

11. Beydon N, Davis SD, Lombardi E, Allen JL, Arets HG, Aurora P, 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(12):1304-45.

12. Esteves A, Solé D, Ferraz M. Adaptation and validity of the ATS-DLD-78-C questionnaire for asthma diagnosis in children under 13 years of age. Braz Ped News. 1999;1:3-5.

13. Miller MR, Hankinson J, Brusasco V, Burgos F, Casaburi R, Coates A, et al. Standardisation of spirometry. Eur Respir J. 2005;26(2):319-38.

14. Loeb JS, Blower WC, Feldstein JF, Koch BA, Munlin AL, Hardie WD. Acceptability and repeatability of spirometry in children using updated ATS/ERS criteria. Pediatr Pulmonol. 2008;43(10):1020-4.

15. Veras TN, Pinto LA. Feasibility of spirometry in preschool children. J Bras Pneumol. 2011;37(1):69-74.



Study carried out under the auspices of the Graduate Program in Child and Adolescent Health, Universidade Federal de Pernambuco - UFPE, Federal University of Pernambuco - Recife, Brazil.
Correspondence to: Edjane Figueiredo Burity. Rua Dr. Geraldo de Andrade, 75, apto. 501, Espinheiro, CEP 52021-220, Recife, PE, Brasil.
Tel. 055 081 3427-0926 or 055 081 9961-7132. Fax: 055 081 3426-5110. E-mail: edjaneburity@hotmail.com
Financial support: This study received financial support from the Fundação de Amparo à Ciência e Tecnologia do Estado de Pernambuco (FACEPE, Foundation for the Support of Scientific and Technological Development of the state of Pernambuco).
Submitted: 6 October 2010. Accepted, after review: 30 May 2011.



About the authors

Edjane Figueiredo Burity
Volunteer Preceptor. Medical Residency in Pediatrics and Medical Residency in Allergy and Immunology, Universidade Federal de Pernambuco - UFPE, Federal University of Pernambuco - Recife, Brazil.

Carlos Alberto de Castro Pereira
Director. Department of Pulmonary Diseases, São Paulo Hospital for State Civil Servants, São Paulo, Brazil.

José Ângelo Rizzo
Adjunct Professor of Clinical Medicine. Universidade Federal de Pernambuco - UFPE, Federal University of Pernambuco - Recife, Brazil.

Emanuel Sávio Cavalcanti Sarinho
Adjunct Professor. Graduate Program in Child and Adolescent Health and in Health Sciences, Universidade Federal de Pernambuco - UFPE, Federal University of Pernambuco - Recife, Brazil.

Marcus Herbert Jones
Professor. Department of Pediatrics, Pontifical Catholic University of Rio Grande do Sul School of Medicine, Porto Alegre, Brazil.

 

 


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