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* From the Pediatric Pulmonary Unit (Drs. Vilozni, Barak, Efrati, Augarten, and Yahav), Edmond and Lily Safra Childrens Hospital, Chaim Sheba Medical Center, Tel-HaShomer, and the Sackler Medical School, Tel-Aviv University, Tel Aviv; Institute of Pulmonology (Dr. Springer), Hadassah Medical Center, Jerusalem; and Pediatric Pulmonary Unit (Dr. Bentur), Meyer Childrens Hospital, Rambam Medical Center and the Faculty of Medicine, Technion, Haifa, Israel.
Correspondence to: Daphna Vilozni, PhD, Pediatric Pulmonary Unit, The Edmond and Lily Safra Childrens Hospital, Chaim Sheba Medical Center, Tel HaShomer, Ramat-Gan 52625, Israel; e-mail: avi_vil{at}bezeqint.net
| Abstract |
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Design: Feasibility study.
Settings: Community kindergartens around Israel and a tertiary pediatric pulmonary clinic.
Participants: Healthy and asthmatic preschool children (age range, 2.0 to 6.5 years).
Intervention: Multitarget interactive spirometry games including three targets: full inspiration before expiration, instant forced expiration, and long expiration to residual volume.
Measurements and results: One hundred nine healthy and 157 asthmatic children succeeded in performing adequate spirometry using a multitarget interactive spirometry game. American Thoracic Society (ATS)/European Respiratory Society spirometry criteria for adults for the start of the test, and repeatability were met. Expiration time increased with age (1.3 ± 0.3 s at 3 years to 1.9 ± 0.3 s at 6 years [± SD], p < 0.05). FVC and flow rates increased with age, while FEV1/FVC decreased. Healthy children had FVC and FEV1 values similar to those of previous preschool studies, but flows were significantly higher (> 1.5 SD for forced expiratory flow at 50% of vital capacity [FEF50] and forced expiratory flow at 75% of vital capacity [FEF75], p < 0.005). The descending part of the flow/volume curve was convex in 2.5- to 3.5-year-old patients, resembling that of infants, while in 5- to 6-year-old patients, there was linear decay. Asthma severity by Global Initiative for Asthma guidelines correlated with longer expiration time (1.7 ± 0.4 s; p < 0.03) and lower FEF50 (32 to 63%; p < 0.001) compared to healthy children. Bronchodilators improved FEV1 by 10 to 13% and FEF50 by 38 to 56% of baseline.
Conclusions: Interactive respiratory games can facilitate spirometry in very young children, yielding results that conform to most of the ATS criteria established for adults and published data for healthy preschool children. Spirometric indexes correlated with degree of asthma severity.
Key Words: asthma preschool children respiratory interactive computer games spirometry
| Introduction |
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Spirometry is generally taught to adults and children by verbal coaching. Since games play an important role in the learning processes of the preschool child, several manufacturers have integrated computer games into their commercially available spirometry software. These games teach the child to blow out forcefully using a visual incentive such as blowing out candles, moving clouds, or popping balloons with arrows. These incentives are based on a single target, usually peak expiratory flow rate (PEFR). Taking a deep breath to total lung capacity (TLC) may be "instinct dependent," but expiration to residual volume (RV) is not.
The effectiveness of these games as an aid for teaching spirometry is controversial.10111213 Studies51011 showed that children cooperated with single-target games and achieved acceptable reproducibility criteria, but FVC and FEV1 were underestimated. It was concluded that teaching spirometry using games did not yield superior results to verbal coaching. Other studies1213 examined teaching spirometry via several games and targets, one being PEFR and the other FVC, and found this to be helpful in the learning process of spirometry in young children. We developed and assessed an animated program for teaching spirometry to young children.5 This program teaches a full FVC maneuver using multiple targets in a step-by-step manner. These steps include complete initial inspiration to TLC, maximal effort on expiration, and complete expiration without a break before reaching RV.
In the present study, we investigated whether a "multiple-target" game in healthy preschool children can yield spirometry results that are compatible with American Thoracic Society (ATS)/European Respiratory Society (ERS) recommendations34 and with published data for preschool children.6131013 We also evaluated the validity of this spirometry game in a group of children with respiratory symptoms as compared with healthy children.
| Materials and Methods |
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Healthy Group: Children were recruited to the study from a number of public kindergartens. An initial screening questionnaire addressing the childs birth, past and present health status, parental smoking habits, and asthma or allergies within the immediate family was completed by the parents. The questionnaire was based on the ATS-DLD-78-A questionnaire for adults, adapted for children6 and translated into Hebrew. Each patient underwent a physical examination on the day of test.
Exclusion criteria included previous symptoms or treatment for asthma of the child, his or her parents, or siblings; any respiratory symptoms (cough, postnasal drip, pneumonia, allergic rhinitis) within the preceding 4 weeks; history of respiratory syncytial virus bronchiolitis, prematurity, oxygen administration or mechanical ventilation; any chronic respiratory illness (ie, cystic fibrosis, bronchopulmonary dysplasia, or chest deformation). Children with allergic rhinitis, atopic dermatitis, gastroesophageal reflux, and extensive passive tobacco exposure were also excluded.
Asthmatic Group: This group included children with asthma diagnosed by pediatric pulmonary physicians prior to the study. Children in the asthmatic group were considered to have asthma if they exhibited the following symptoms: repeated episodes of shortness of breath, wheezing and/or nocturnal cough with clinical response to inhaled bronchodilators (Global Initiative for Asthma [GINA]).2 These children had all been referred to the Pediatric Pulmonary Unit. A detailed history (including comorbidity factors such as passive smoking, allergic rhinitis, allergic conjunctivitis, and atopic dermatitis) was obtained, and a physical examination was performed. Asthma severity was classified clinically according to GINA guidelines,2 as mild intermittent, mild persistent, moderate persistent, and severe persistent. Exclusion criteria were current acute respiratory illness (common cold, pneumonia), use of bronchodilators within the past 12 h, any other chronic respiratory illnesses (cystic fibrosis, bronchopulmonary dysplasia, or chest deformation), history of prematurity, oxygen administration or mechanical ventilation, gastroesophageal reflux disease, and other nonrespiratory chronic illnesses.
Written informed consent was obtained from each parent or legal guardian. The Helsinki Board at the Sheba Medical Center approved the study.
Spirometry
Spirometry was performed with a commercial spirometer (ZAN100; ZAN Messgeraete GmbH; Oberthulba, Germany). Calibration was performed before each testing session. The spirometer software includes on-line analysis of the FEFV curves. The curves were monitored on the computer screen to ensure best effort. Results were corrected to body temperature and barometric pressure, saturated. The software also included SpiroGame (patented by Dr. Vilzone, 2003), an interactive animated computer game set by targets of the FEFV maneuver, combining maximal inhalation before forced expiration, PEFR, and FVC, with emphasis on prolonged expiration. The targets were the extrapolated values derived from comparative data from older children, corrected for height.14 Target values were increased by 10% if the flows exceeded the target or decreased by 10% if despite an optimal effort the child could not reach the target. The SpiroGame is comprehensively described in a previous publication5 and briefly in the Appendix.
Procedure
Healthy Children:
Tests were performed in a designated room in the kindergarten. One parent or teacher was present during the test. We allowed up to two additional children in the room for learning purposes.
Asthmatic Group: Tests were performed in the Pediatric Pulmonary Function Laboratory. As with the healthy children, parents were present during the test. Children were asked to refrain from using bronchodilators 12 h before the test.
Spirometry Measurements: Tests were performed in a standing position without a nose clip. An experienced pulmonary technician instructed each child how to operate the game. Emphasis was placed on full inspiration before expiration, without breath holding, and on forced expiration to RV according to the game targets. Maneuvers were repeated to obtain best possible efforts on at least three technically acceptable FEFV curves. Sessions lasted on average 15 min per child, but were shorter if three repetitive, technically acceptable curves were achieved. These curves were stored, and the three curves with the maximal FVC + FEV1 (or FVC + forced expiratory flow at 0.5 s [FEV0.5]) were analyzed for the study.
Curves had to show a rapid rise to peak flow, and gradual, smooth decline of flow to RV. On-line rejection of curves based on visual inspection for "noncooperation" errors included duration of expiration of < 0.5 s, poor effort, incomplete expiration, cough, and glottis closure. The entire examination of a child was rejected if three technically acceptable curves could not be chosen off-line. Off-line, the curves were inspected for acceptability criteria and common spirometric parameters (FVC, FEV1, FEV0.5, PEFR, forced expiratory flow at 25% of vital capacity, forced expiratory flow at 50% of vital capacity [FEF50], and forced expiratory flow at 75% of vital capacity [FEF75]). These were analyzed.
Analysis and Statistics
Acceptability of Curves:
Three authors of this study reviewed the spirometry curves visually for acceptability, blinded as to name, sex, age, and height of the children. Accepted curves were further analyzed in relation to ATS/ERS criteria for adults34 and to preschool measurements as measured using verbal coaching techniques or a single-target game.691013 These included the following: (1) "start-of-test" criteria: time to peak expiratory flow and backward extrapolated volume (Vbe); (2) "end-of-test" criteria: forced expiratory time of 6 s, and the ratio between the "time of no change in expiratory volume" to total expiratory time; and (3) repeatability: the differences between the three best FEFV curves of each parameter (SD/mean x 100) for each child. In all statistical analyses, p < 0.05 was considered significant.
Further Analysis
Healthy Subjects:
Children were grouped by age: 2.5 to 3.5 years old (age 3), 3.6 to 4.5 years old (age 4), 4.6 to 5.5 years old (age 5), and 5.6 to 6.5 years old (age 6). Correlations between each parameter and height (age) were calculated for the healthy children using the Pearson correlation. Parameters between groups were compared using unpaired t tests and
2 analysis. Spirometric values were then compared by paired t test to the extrapolated for height parameters published previously for preschool children.6910
Asthmatic Children: Asthma severity was classified clinically according to GINA guidelines2 as mild intermittent, mild persistent, moderate persistent, and severe persistent. Bronchodilators were administrated only when airway obstruction was evident. Bronchodilator, 200 µg salbutamol, was delivered via an air-holding chamber with a facemask sealed gently to the face around the nose and the mouth. The child was asked to breathe the medication for 40 s. Spirometric values of each child were compared to the extrapolated values for height of our healthy children by paired t test. Postbronchodilator values were compared as percentage change to the baseline values; p < 0.05 was considered significant.
| Results |
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Start of Test: PEFRs were achieved within 92 ± 8 ms, and mean Vbe was 2.2 ± 1.5% of FVC.
Repeatability: The differences between three measurements were 3.54 ± 2.66% for FVC; 2.95 ± 2.01% for FEV0.5; 3.43 ± 2.34% for FEV1; 4.66 ± 3.01% for PEFR; 5.98 ± 4.89% for FEF50 and 8.99 ± 7.93% for FEF75.
End of Test: The time of "no change in expiratory volume" at the end of expiration was similar in healthy and asthmatic children (0.33 ± 0.05 s).
Expiratory Time: In healthy children, expiratory time increased with age. Mean values for healthy 3-year-old children were 1.34 ± 0.45 s, increasing to 1.86 ± 0.62 s in 6-year-old children (p < 0.05), with mean for the total healthy group of 1.56 ± 0.45 s. The correlation between height (age) and expiratory time is presented in Figure 2 . The ratio of no change in expiratory volume to "total expiration time" was 0.19 ± 0.05 for the healthy children. In asthmatic children, the mean expiration time for the mild group was 1.45 ± 0.41 s, as in healthy preschool children. Expiration time was significantly longer in the moderate and severe groups (1.7 ± 0.4 s and 1.7 ± 0.5 s, respectively), compared with healthy children (p < 0.03).
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| Discussion |
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It is interesting to note a small gap between parental perceptions of "healthy" and past respiratory diseases. We found that, for 5 of the 153 children whose parents indicated were healthy on the questionnaire, spirometry was strongly suggestive of obstructive airways disease. These children were not included in the analysis. As healthy children were defined based on the parental questionnaire and physical examination, the possibility that other "asthmatic children" were included cannot be ruled out.
Meeting ATS/ERS Criteria
Overall, most start-of-test, end-of-test, and repeatability criteria were met, and results were similar to those reported previously for adults, school children, and healthy preschool children.341315 Repeatability was also similar to values reported by Nystad et al,10 who taught spirometry using games. Specific differences in acceptability of curves found in our study.
Start-of-Test Criteria:
The volume exhaled during the first 100 ms overlapped 25% of the expiratory volume in some of the younger healthy children. We rejected curves if PEFR was reached after 25% of the expiratory volume (defined as slow starts), but this rejection may have to be reconsidered since the younger children may not be able to reach their peak expiratory flow within 100 ms. Vbe
5% of FVC found in our study is tighter than reported,13 as we have rejected in advance curves with Vbe > 5% of FVC at the expense of success rate. The value of 100 to 150 mL, also cited for differences between curves, is a relatively high percentage of the FVC in young children (> 18% of FVC in healthy 3 year olds and/or 10% of FVC at age 6). Therefore, rejecting curves on this basis may be inappropriate
End-of-Test Criteria: We found that expiratory time was age related. Thus, it is suggested that age-related rather then a fixed expiratory time may be more appropriate to define end-of-test criteria at the preschool ages. A positive correlation between expiratory time and age has been documented in infants16; therefore, our finding may insinuate continuation of lung growth.
In that respect, further findings were related to age in healthy subjects and seem to be a continuation of lung growth; spirometry indexes increased with age as expected. The shape of the curve changed with age as the descending part of the expiratory curve changes from a convex profile in younger ages to an almost linear decay in older children (Fig 5 ). The change in shape was supported by a similarity between PEFR and forced expiratory flow at 25% of vital capacity, thus forming a round-shaped, peak flow-volume curve pattern, particularly in the younger children, and by an increase in expiratory time with age. The convex profile of the expiratory limb of the flow/volume curve in the young children resembled that produced by infants.17 It was shown that the infant lung is not a smaller version of the adult lung and that lung volume is small relative to airway size.1819202122 This causes a quick emptying of the lungs, producing a convex shape of the expiratory FEFV curve. We assume that, as in infants, the change in shape from convex to linear in the preschool age reflects a continuation of the developmental processes of lung maturation. The significant decline of spirometric indexes in relation to FVC found in our study and by Zapletal and Chalupova9 supports our assumption of continued developmental processes of lung volume in preschool age.
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Spirometry in Asthmatic Children as Compared With Healthy Children
The correct spirometry reference values for preschool children are still controversial and are currently being standardized.13 The present study examined spirometry in preschool children who were thought to have asthma, with varying degrees of respiratory symptom severity (Tables 1, 5) in relation to a healthy population. A difficulty related to this study exists in the definition of asthma at this young age, particularly since there are a number of other entities, such as transient wheezing or viral-associated wheezing, that may overlap, and can cause repeated wheezing in young infants. Their exact definition and nomenclature are still the subject of research and debate.
In our study, children with repeated episodes of wheezing and shortness of breath responding to bronchodilators were considered as having asthma. Their diagnosis of asthma and its severity were based on GINA criteria, which do not include pulmonary function at this age. GINA guidelines2 state that there have been no well-conducted clinical trials to provide scientific evidence for the proper treatment of asthma at each step of severity in the preschool age, and no objective lung function measurement in the preschool age. This may increase intergroup SDs. The overlap between the groups may also be due to the inclusion of" silent asthmatic" patients in the healthy group. Spirometry indexes of children with asthma from the "mild groups" did not significantly differ from those of our healthy control children. Our findings did not agree with Zapletal and Chalupova,9 who suggested that both PEFR and FEF50 in mildly asthmatic children should be reduced by 2 to 3 SDs. The inclusion of mild intermittent asthma in the mild group may explain the normal values found in our study in mild asthma.
Spirometry was sensitive in detecting moderate and severe symptoms. Airway obstruction increased with increasing severity of symptoms according to the groups, but indexes differed in their sensitivity and FEF50 was reduced more than FEV1. We found that FEV1/FVC deteriorated with severity of symptoms in a similar degree to FEF50. This finding may counter the considerable doubt over whether FEV1/FVC is sensitive enough to reveal airway obstruction in preschool age children since some young children are not able to expire for > 1 s. In light of our findings, the decision regarding which of the parameters is best for determining airway obstruction may require additional investigation.
Unexpectedly, we found that both FVC and PEFR decreased with severity of symptoms. This finding may indicate elevation of functional residual capacity as a strategy of breathing or elevation of RV due to air trapping.2324252627
The Effect of Bronchodilators on Spirometry Indexes in the Moderate and Severe Groups
Bronchodilators were administrated only to those children showing airways obstruction, ie, the moderate and severe groups. In the moderate and severe groups, we found that use of bronchodilators improved most spirometry indexes > 15%. The sensitivity of reversibility testing based on spirometry seems to be comparable to that found in asthmatic school children.28
The magnitude of response of flow-related volumes was three times higher than volume-related time values. Interestingly, PEFRs were improved
22%. The ratios of FEV1/FVC (or FEV0.5/FVC) were insensitive indexes for measuring airway responsiveness, as they did not significantly improve in either of the groups, probably due to simultaneous improvement of flow and volume.
The Role of Games in Teaching Spirometry to Young Children
We strongly believe in the value of games for teaching spirometry in preschool-age children, particularly the younger ones. In addition to the elements of fun and pleasure, games engage the children passionately and intensely, offering motivation and ego gratification. But games need rules, structure, goals, and feedback to regulate the learning process. It is only then that a game can have measurable outcomes. Achieving successful goals cannot rely on the instinct of the child to take a deep breath to TLC, nor the voluntary effort to blow out down to RV. Thus, a game with multiple targets to teach all of the steps needed to achieve successful curves seems justified. The use of several games, each teaching a single step of the maneuver to incorporate a full maneuver, may also be appropriate. The relatively small number of healthy children participating in our study may not be sufficient to establish global reference values. Larger study groups evaluating different teaching methods in other institutions may establish solid reference values.
We conclude that many children > 2.5 years of age can perform reliable FEFV curves. The incentive teaching technique with computer games can facilitate spirometry in these very young children, but incentive programs should include all steps of spirometry. Spirometry obtained at the preschool age can detect airway obstruction and correlates with degree of asthma severity. Among the routine indexes used to quantify spirometry, flow-related volumes were better than timed expiratory volume in detecting abnormal airway function. Our results emphasize the need for standardization of suitable teaching techniques, and outcome parameters of spirometry measurements in healthy children, and in revealing airway obstruction in preschool children.
| Appendix |
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The second game teaches the FVC maneuver. A caterpillar is crawling (tidal breathing) in a field with flowers situated at different locations on the screen. A bee is sitting on the first flower that the caterpillar reaches. On reaching the first flower, the bee flies to another one according to the forced expiratory maneuver targets (inspiratory capacity, PEFR, FVC, with emphasis on long expiration). To produce a PEFR, the bee has to fly over a fence; to produce FVC, the last flower is within a visual distance from the others. On completion of the FEFV maneuver, a new picture rewards the child for success. The targets are calculated from extrapolated predicted values for height,14 and the game has several levels of difficulties.
| Footnotes |
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Received for publication September 25, 2004. Accepted for publication January 18, 2005.
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This article has been cited by other articles:
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D. Vilozni, L. Bentur, O. Efrati, A. Barak, A. Szeinberg, D. Shoseyov, Y. Yahav, and A. Augarten Exercise Challenge Test in 3- to 6-Year-Old Asthmatic Children Chest, August 1, 2007; 132(2): 497 - 503. [Abstract] [Full Text] [PDF] |
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