Published ahead of print on March 17, 2004, doi:10.1164/rccm.200310-1453OC
© 2004 American Thoracic Society
Quality Control for Spirometry in Preschool Children with and without Lung DiseasePortex Respiratory Unit, Institute of Child Health; Cardiorespiratory and Critical Care Division, Great Ormond Street Hospital for Children; and Department of Paediatric Respiratory Medicine, Royal Brompton Hospital, London, United Kingdom Correspondence and requests for reprints should be addressed to Paul Aurora, M.R.C.P., Portex Respiratory Unit, Institute of Child Health, 30 Guilford Street, London WC1N 1EH, UK. E-mail: p.aurora{at}ich.ucl.ac.uk
The reliability of spirometry is dependent on strict quality control. We examined whether quality control criteria recommended for adults could be applied to children aged 2–5 years. Forty-two children with cystic fibrosis and 37 healthy children attempted spirometry during their first visit to our laboratory. Whereas 59 children (75%) were able to produce a technically satisfactory forced expiration lasting 0.5 second, only 46 (58%) could produce an expiration lasting 1 second, with the youngest children having the most difficulty. Start of test criteria for adults were inappropriate for this age group, with only 16 of 59 children producing a volume of back extrapolation as a proportion of forced vital capacity of less than 5%, whereas all but 4 could produce a volume of back extrapolation of 80 ml or less. More than 90% of children were able to produce a second forced vital capacity and a second forced expired volume in 0.75 second within 10% of their highest. Errors in the spirometry software resulted in inaccurate reporting of expiratory duration and inappropriate timed expired volumes in some children. We describe recommendations for modified start of test and repeatability criteria for this age group, and for improvements in software to facilitate better quality control.
Key Words: children • children, preschool • quality control • spirometry Spirometry is the most frequently used method for measuring lung function. The reliability of spirometry depends on standardized methodology, particularly regarding how quickly the subject increases flow at the beginning of the expiration; sustained effort throughout the expiration; duration of the expiratory maneuver; and repeatability. Detailed criteria for data collection and interpretation have been published by the American Thoracic Society (ATS) and by the European Respiratory Society (ERS) (1, 2). Application of these criteria when collecting and interpreting spirometry data is considered mandatory in adult pulmonary function laboratories. Spirometry is not only employed in adults; it is also commonly performed in pediatric pulmonary function laboratories. Spirometry was previously limited to school-age children (those aged 6 to 16 years), but reports have confirmed that preschool children (those aged 2 to 5 years) are also able to attempt these maneuvers (3–10). Both the ATS and ERS guidelines were written for adult patients, and Arets and colleagues have already demonstrated that many school-age children have difficulty meeting some of the quality control criteria (11). Reports of spirometry in preschool children have focused on feasibility (3–5), use of incentive devices (5), and recording of reference values in healthy populations (3, 4) rather than on the issue of quality control. We hypothesized that children aged 2 to 5 years would find it impossible to meet some of the quality control criteria for spirometry, but that alternative criteria may be feasible. The primary aims of this study were to analyze results from spirometry performed by preschool children against quality control criteria recommended for such measures in adults, to identify which of these criteria are easily achieved by preschool children and which are not, to determine whether success in meeting these criteria is affected by the presence of lung disease or by subject age, and to identify possible modifications that could be applicable in preschool children. The secondary aim of this study was to compare results obtained from healthy children in our laboratory with those previously reported from other centers, and to assess whether reference ranges published by those centers apply to our population.
A detailed description of the study population and methods, including examples of unacceptable recordings, is presented in the online supplement. All children were at least 2, and less than 6, years of age at the time of testing. Children with cystic fibrosis (CF) were recruited from centers participating in the London Cystic Fibrosis Collaboration, a longitudinal study of airway function in CF (12). Healthy control children were recruited from the community. All tests were performed between September 2000 and March 2003, at the Institute of Child Health (London, UK). All children were participating in a study comparing different methods of measuring airway function, and performed multiple-breath inert gas washout, specific resistance measurement by plethysmography, and spirometry, in that order. Data reported in this article are limited to spirometric measurements obtained at the child's first laboratory visit. The study was approved by the Research Ethics Committee of the Institute of Child Health and Great Ormond Street Hospital for Children (London, UK). Written informed consent was obtained from the parents of all children entering the study. Spirometry was performed with a Jaeger MasterScope spirometer (VIASYS Healthcare, Höchberg, Germany). The first expirations were encouraged by means of the Jaeger "Candle" incentive program, which promotes a rapid expiration. When the child had mastered rapid expiration the program was changed to display an incentive that encourages prolongation of that rapid expiration. All volume–time and flow–volume curves were visually inspected by at least two of the authors. Recordings were passed if they met the following criteria on visual inspection: the flow–volume trace showed a rapid rise to peak flow, and a smooth descending limb, with no evidence of cough or glottic closure; and the volume–time trace was approaching a horizontal plateau (Figure 1) . Duration of expiration was recorded and the tracing was accepted if it was 0.5 second or more. Results were reported only if two or more technically acceptable curves were obtained.
The Jaeger MasterScope program allows only five maneuvers to be recorded per test file. Additional test files were therefore created as necessary, and a maximum of 25 maneuvers was recorded. Recording was stopped earlier than this if the investigator assessed that maximal results had been obtained, or if the child was showing signs of fatigue or restlessness. Spirometry parameters were obtained by first transferring all data from the Jaeger MasterScope system to a separate PC workstation, and then exporting satisfactory results into an Access relational database (Microsoft, Redmond, WA), using a custom-written export program. This procedure was necessary because standard Jaeger software does not allow (1) reporting of all necessary parameters, or (2) data to be excluded but saved for future reanalysis. The following parameters were reported from each maneuver: FVC, FEV1, FEV0.75, FEV0.5, FEF25–75, duration of maneuver producing the best FVC (forced expiratory time [FET]), back-extrapolated volume (VBE), and VBE/FVC. It was discovered that the Jaeger MasterScope software occasionally reported timed expired volumes inappropriately, so that some children appeared to have an FEV1 equal to FEV0.75 or an FEV0.75 equal to FEV0.5. The reason for this fault is that the Jaeger system continues recording until an inspired volume of 40 ml has been recorded. The software then identifies the point at which inspiratory flow began, and defines this point as the end of expiration (J. Reinstaedtler, personal communication). When children kept their mouth on the mouthpiece at the end of the expiration, the FET recording was correctly terminated at the beginning of the next inspiration. Some children, particularly the younger ones, removed their mouth from the mouthpiece as soon as they had completed their expiration. In this case, the program continued measuring FET until the investigator manually terminated the recording. On visual inspection of the traces we discovered that some of the FET results were overestimated. Therefore, verification of the data was undertaken. First, all reports in which FET was less than 1 second, and/or in which FEV0.75 or FEV1 was equal to FVC, were identified. These curves were then visually inspected and timed volumes that had been inappropriately reported were excluded. By this method six children who had produced satisfactory FEV0.5, but from whom FEV0.75 should not have been reported, and seven children who had produced satisfactory FEV0.5 and FEV0.75, but from whom FEV1 should not have been reported, were identified.
Statistical Analysis
Summary statistics are presented as mean and standard deviation (SD) if normally distributed, and as median and interquartile range (IQR) if nonnormally distributed. Proportions were compared by
Forty-two children with CF and 37 healthy children were recruited. Mean (SD) age of the children with CF was 4.14 (0.90) years. Mean age of the control children was 4.14 (0.85) years. Although matched for age, the children with CF were significantly lighter and shorter than the control children (Table 1) .
Success Rates Seven children were unwilling to attempt spirometry. The median number of spirometry maneuvers attempted by the remaining 72 children was 12 (range, 6–22). Success in producing a reportable FVC, FEV0.5, FEV0.75, FEV1, and FEF25–75 is presented in Table 2 . Fifty-nine children were able to produce acceptable spirometry loops (Figure 1). Nine of these children could produce only 2 acceptable curves, and the remaining 50 children produced between 3 and 9 acceptable loops each (median, 4).
There was no significant difference between the CF and control groups in success rate for any of the parameters. Children aged 2 to less than 4 years were significantly less likely to produce FEV0.75 or FEV1 than children aged 4 to less than 5 years or children aged 5 to less than 6 years. No other differences in success rates by age group were seen. Ability to meet quality control criteria was assessed for the 59 children who produced acceptable results.
Start of Test Criteria
Duration of Maneuver FET, summarized by age group and diagnosis, is presented in Table 3. Twelve of the 59 children produced a FET less than 1 second. These results must be interpreted with caution. For the majority of children FEV1/FVC was greater than 90%, irrespective of age group or diagnosis. By contrast, for the majority of children FEV0.5/FVC was less than 90%. In healthy children there was a significant negative relationship between FEV0.5/FVC and height (r2 = 0.22, p = 0.009) and between FEV0.75/FVC and height (r2 = 0.27, p = 0.008), but no relationship between FEV1/FVC and height. There was no relationship between FEV/FVC parameters and height in the CF population.
Within-Occasion Repeatability
Comparison with Published Reference Data
Additional results are presented in the online supplement. The online supplement includes traces that were excluded on visual inspection, traces from maneuvers that had high VBE or VBE/FVC, data on ethnic background, analysis of timed expired volumes as proportions of FVC by age and diagnosis, plots of  FEV0.75 and FVC against age, and plots of z scores for our healthy population (3, 4).
In this study results of spirometry attempts in seventy-nine 2- to 5-year-old children were analyzed in detail, to determine whether the results met published quality control criteria for adult spirometry. All flow–volume and volume–time traces were first visually inspected and passed or rejected. Forced expiratory volumes and flows obtained in healthy children were similar to those reported by other groups. The criteria tested were start of test, assessed by back extrapolation; duration of expiration, and the timed expired volumes that are influenced by this; and repeatability. For all these parameters modifications to quality control criteria appear necessary for application to preschool children.
Visual Inspection Evaluation of end-of-test by visual inspection is more difficult. In older children and adults the volume–time trace asymptotes to horizontal toward the end of expiration (1). In preschool children, particularly the youngest, this asymptote is frequently not seen, even in children who appear to have produced a complete expiration (Figure 1). The abrupt cessation of expiration in very young children complicates assessment of end-of-test, as curves such as that shown in Figure 1 should not be excluded inappropriately. Eigen and colleagues (from the Indianapolis group) have suggested excluding curves when expiratory flow abruptly ceases from a point greater than 25% of peak flow (3); Marostica and colleagues (also from the Indianapolis group) have proposed excluding curves when expiratory flow abruptly ceases from a point greater than 10% of peak flow (9); while Vilozni and colleagues have suggested excluding curves when cessation occurs abruptly from a flow of 300 ml · second–1 or more (5). All suggestions have merit, particularly if consensus could be reached, but many spirometry software systems do not provide such information automatically. Our current study design, in which all curves are inspected by at least two experienced researchers, and "borderline" curves by at least three, is not possible in daily practice. We therefore suggest that manufacturers should modify software so that information on change in rate of lung emptying toward the end of expiration is easily available, with automatic identification and display of critical cutoff points as suggested above. In those curves where incomplete expiration is identified, timed expired volumes and peak flows may still be reportable (13), even though FVC and forced expiratory flows cannot be reported from such maneuvers.
Quantitative Start of Test Criteria All the curves included in this analysis had been passed visually as showing acceptable rise to peak flow. After reinspection of curves with high VBE or VBE/FVC, we concluded that our initial visual inspection had included and excluded curves correctly. We therefore suggest that expirations with VBE greater than 80 ml or VBE/FVC greater than 12.5% should be visually reinspected to ensure acceptable rise to peak flow, but should not necessarily be excluded.
Quantitative End-of-Test Criteria and Timed Expired Volumes Duration of expiration determines which time-limited volumes are reportable. If FET is less than 1 second, then FEV1 cannot be reported from that expiration. Success in producing FEV1 was dependent on age in this study, with only 41% of children younger than 4 years able to produce a FEV1, compared with 80% of those more than 5 years of age. There was no difference in the success rates between the healthy and CF groups. Previous researchers have reported similar findings. Eigen and coworkers reported results only from children who were able to expire for at least 1 second, but still recorded a creditable success rate of 83% in a slightly older population than ours (mean [SD] age, 5.0 [0.9] years) (3). Crenesse and coworkers reported results in 473 children aged 3 to 5 years. Seventy-five percent (355) were able to produce at least 1 acceptable forced expiratory maneuver. Of these, only 75% of children 3 to less than 4 years old, 73% of children 4 to less than 5 years old, and 87% of children 5 to less than 6 years old were able to produce an FET of greater than 1 second (10). Nystad and colleagues reported results from 630 children aged 3–6 years, and found that 10% were unable to expire for 1 second (4). It is therefore recommended that spirometry software should calculate FEV0.5 and FEV0.75, and that all laboratories should analyze and report both these parameters in addition to FEV1 for children aged under 6 years, to allow comparison with others of similar age. For many 2- to 4-year-old children, only the shorter timed volumes will be reportable. The Jaeger software currently allows timed expiratory volumes to be reported incorrectly. Operators should ensure that their own software does not contain similar errors. Any timed volume that is reported as equal to FVC should be considered potentially erroneous. Even when an FEV1 is attainable, the clinical value of this parameter in this age group is questionable. Compared with older children and adults, infants and preschool children have large airways relative to their lung volume, and therefore empty their lungs more rapidly. As a result, the FEV1/FVC ratio is more than 90% in the majority of preschool children, including those aged 5 to 6 years, and regardless of whether these children have lung disease. Reporting of FEV0.4 or FEV0.5 in infants is now accepted (13), and assessment of FEV0.5 or FEV0.75 may be more clinically relevant than FEV1 in the preschool age group. Further investigation of the discriminative ability of different spirometric parameters is beyond the scope of the present study, but is an important area for future research.
Repeatability
Comparison with Previously Published Data Ethnic group was not specified by the Oslo group, but Oslo has a very small nonwhite population. We therefore calculated summary statistics for our entire healthy population and separately for our healthy white children. z scores for our control population should be zero, with a standard deviation of 1, for all parameters, provided that our equipment and methodology are similar to that used by previous groups, and that our control population is similar to those from whom the reference equations were derived (14). For our white population, this was true for FEV0.5 z scores calculated from Oslo data, for FVC and FEF25–75 z scores calculated from Indianapolis data, and arguably true for FEV1 z scores calculated from Indianapolis data. Our FVC and FEV1 results did not fit the reference equations reported by the Oslo group.
Methodologic Issues and Strengths and Limitations Incentive software can be distracting for older children (16), but in our population we found it helpful. We used the Jaeger incentive program (which is routinely available with Jaeger spirometry software) for all children. Vilozni and colleagues have reported that only 2% of 3- to 6-year-old children are able to produce an FEV1 with the Jaeger incentive software, as compared with 49% of children who could produce an FEV1 with their own SpiroGame incentive software (5). We note that in Vilozni's study only the Jaeger "Candle" incentive (which encourages rapid expiration) was used, and that, unlike in our study, the investigators did not move on to alternative incentives that encourage prolongation of expiration. We believe this methodologic difference explains the marked discrepancy between our results (in a younger population) and those previously reported by Vilozni's group. On a related matter, children in the current study performed a maximum of 22 expiratory maneuvers, rather than the 8 recommended by the ATS (1). The reason for this is that many younger children initially produced incomplete expirations, particularly when using the "Candle" incentive. The Jaeger system does not allow easy recording of repeated maneuvers, and does not allow borderline or excluded traces to be stored for later reanalysis. Overcoming these hurdles required considerable effort on our part, including the use of custom-written software, and we consider this a strength of our study. The most notable weakness of our study is that children were tested toward the end of a 2-hour laboratory visit. It is likely that some children were fatigued by the time they performed spirometry, and success rates may have been adversely affected. It is unlikely that other parameters would have been influenced by this methodologic issue. By contrast, one factor that may have increased our success rate was our use of a specially adapted preschool laboratory, with data collection performed by trained operators. This setup is not always available in the clinical setting.
Conclusions and Suggestions for Future Work
In addition to these recommendations, we caution users that current spirometry software may result in erroneous reporting of FET and timed expired volumes. We have contacted manufacturers with requests to amend software to allow quantitative assessment of end-of-test, and to allow recording and reanalysis of multiple maneuvers, including those initially assessed as inadequate or borderline. These software amendments should allow data to be excluded from reports or summaries, while still being retained on databases to allow future reanalysis. Before incorporating such recommendations into guidelines it will be necessary for other groups to assess these criteria in their own populations. Given the portability of spirometry equipment, these criteria should ideally be tested in both specialized laboratories and in general clinics or health centers. Accurate application and interpretation of spirometric assessment in the preschool age group has considerable potential benefit, both for clinical practice and research. This benefit justifies the effort required for standardization.
The authors thank the children and their families for taking part in this study. The authors also thank Dr. Rod Lane and Mr. Aidan Laverty (Respiratory Function Laboratory, Great Ormond Street Hospital for Children) and Dr. Sooky Lum (Portex Unit, Institute of Child Health) for comments on the final draft. The authors particularly acknowledge the assistance of Ms. Gail Slade, who assisted with some of the measurements, but who sadly passed away before this manuscript was written.
Supported by Dunhill Medical Trust, British Lung Foundation, Cystic Fibrosis Trust, Portex Ltd. Research at the Institute of Child Health, and Great Ormond Street Hospital for Children NHS Trust benefits from R&D funding received from the NHS Executive. This article has an online supplement, which is accessible from this issue's table of contents online at www.atsjournals.org Conflict of Interest Statement: P.A. does not have a financial relationship with a commercial entity that has an interest in the subject of this manuscript; J.S. received an educational grant of £35,000 from Jaeger-Toemo in 2001 for development and training material for infant lung tests; C.O. does not have a financial relationship with a commercial entity that has an interest in the subject of this manuscript; C.S. does not have a financial relationship with a commercial entity that has an interest in the subject of this manuscript; R.C. does not have a financial relationship with a commercial entity that has an interest in the subject of this manuscript; G.C. does not have a financial relationship with a commercial entity that has an interest in the subject of this manuscript; A.B. does not have a financial relationship with a commercial entity that has an interest in the subject of this manuscript. Received in original form October 25, 2003; accepted in final form March 14, 2004
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ABSTRACT
METHODS
2 test. t tests or Mann–Whitney tests were employed for comparison of two groups; Analysis of variance and post hoc analysis by Tukey's honestly significant difference (HSD) were used to compare three or more groups. When interaction between several factors was suspected this was investigated by multiple regression. z scores for FVC, FEV1, and FEF25–75 were calculated from reference equations derived from 184 healthy white preschool children tested in Indianapolis, Indiana (
