Lung Function Increases With Increasing Level of Physical Activity in School Children

(1)

402

Lung Function Increases With Increasing

Level of Physical Activity in School

Children

Sveinung Berntsen, Torbjørn Wisløff, Per Nafstad, and Wenche Nystad

Little is known about the association between physical activity and lung function in childhood. We conducted a survey including parental reports of the child’s participa-tion in physical activity and measurements of lung funcparticipa-tion. The associaparticipa-tions between physical activity and lung function were estimated by linear regression analysis adjusting for potential confounders in 2,537 children (9 to 10 years). Using the linear model in exploring the effect of physical activity on lung function with those who were physical active less than once a week as the reference category, showed that forced expiratory volume in 1 s (FEV1) was highest among those who were physical

active ≥ 4 times a week also when adjusting for potential confounders (p = .02). FEV1

increased with 70 ml. A similar pattern was present for forced vital capacity (FVC;

p = .002). The present study suggested that lung function was highest in highly phys-ical active children age 9 to 10 years. The implications are that exercise may influence lung function, but these findings need to be confirmed using a longitudinal study design.

Several Western societies including the Scandinavian child population is during the last decades characterized by a decreasing level of physical activity and an increasing body weight (2,5). Inactivity and obesity is associated with a variety of adverse health outcomes of great global concern (24). Information concerning the association between a sedentary lifestyle and health outcomes such as respira-tory related diseases in children are, however, sparse (15). Some prospective stud-ies have shown that the development of asthma was associated with decreased physical activity or aerobic fitness in children (15) and adult twins (7). It is also suggested that bronchial hyper responsiveness is associated with decreased physi-cal activity in adults and children with asthma (12,17). However, little is known about the association between lung function and habitual physical activity during childhood (18,20). Exercise is known to induce a cascade of physiological responses, which may vary dependent upon the type, intensity and duration of exercise (10,12,22), and it is suggested that the pathophysiology behind the ben-efits of exercise on asthma is related to deep inspiration and smooth muscle acti-vation (9). Linking exercise to lung function is thus plausible.

Berntsen, Wisløff, Nafstad, and Nystad are with the Division of Epidemiology, Norwegian Institute of Public Health, Oslo, Norway.

(2)

The aim of the current study was therefore to assess the association between physical activity and lung function among Norwegian school children.

Material and Methods

Study Population

A follow-up of the Oslo Birth Cohort was carried out in 2001–2002 (11). A cross-sectional study of all children born in 1992 and living in Oslo was carried out simultaneously. A total of 6,327 children were invited and 4,219 (67%) families accepted and returned a self-administered questionnaire that was mailed them together with the invitation. The participants were also offered a clinical examina-tion including measurement of lung funcexamina-tion. The examinaexamina-tion was performed during school hours by a trained staff of research nurses. Results of lung function tests were available for 3,224 children, collected in the period between November 2001 and December 2002. The present analyses include participating children with two parents from Western societies with lung function measurements (n = 2,537). The participants in the current study were representative of the 4,219 fam-ilies who accepted and returned the self-administered questionnaire as they did not differ significantly with respect to physical activity level, socioeconomic fac-tors, parental smoking, and prevalence of asthma.

The study was approved by the Data Inspectorate of Norway and the Medical Research Ethics Committee. Written informed consent to take part was obtained from the parents of the participating children.

Baseline Lung Function

Lung function was measured by maximal forced expiratory flow-volume curves (MasterScope, Erich Jaeger GmbH, Germany), according to the guidelines rec-ommended by the European Respiratory Society (ERS; 14). Age of the child was calculated by subtracting the child’s date of birth from the date of the testing day. Children with major signs of upper respiratory tract infections were excluded. The measurements were conducted with the participant sitting wearing a nose clip. Calibration, taking into consideration ambient conditions, was conducted at least twice a day according to the guidelines of the manufacturer. All maneuvers com-plied with the general acceptability criteria of ERS (14). If the child were unable to do three acceptable and reproducible maneuvers, up to eight maneuvers were performed. However, children with at least two acceptable maneuvers were also included in the analysis (14). All individual flow-volume curves were reviewed for technical acceptability. Lung function parameters were: forced expiratory volume in one second (FEV1) and forced vital capacity (FVC). Reproducibility of

FVC and FEV1 was considered acceptable when the highest FVC and FEV1 value

did not exceed the second highest value by more than 5% (14). The reproducibil-ity criterion was not used to exclude children with a complete test set. Tests that did not meet this criterion were marked, to be able to analyze these data sepa-rately. The largest reading is reported using the envelope method of reading flows, which means that the highest flow at a given lung volume is chosen, irrespective of the curve. Due to the lack of relevant or good reference populations, the vari-ables are presented in absolute values and not in percent of predicted.

(3)

404 Berntsen et al. Variables

Physical activity: The child’s participation in physical activity was assessed by using a question of physical activity level from WHO cross-national survey of health behavior in school-aged children (1). Here we used the question: “Outside of school hours, how often does the child engage in sport or exercise so much that he or she gets out of breath or sweat?” Physical activity was categorized into four categories (less than once a week, once a week, 2–3 times a week and four times or more).

Body mass index (BMI): Standing height (m) using a stadiometer and weight (kg) were measured in a standardized way in indoor clothes without shoes using the same equipment and procedures in all children. BMI, defined as kg · m−2_{, was}

included as a continuous variable. BMI percentiles per sex per age according to the cut-off values of Cole et al. (4) were used to define overweight and obesity.

Background variables: The questionnaire included also items of the children’s health including a history of asthma, environmental exposures, parental education (years of education), ethnicity and a history of asthma and allergy among the par-ents (yes vs. no) and parental smoking (yes vs. no). Ethnicity was categorized into two categories: children with and without two parents from Western countries. Data from The Medical Birth Registry of Norway was merged our data, and thus the Medical Birth Registry provided information of birth weight (8).

Data Analysis

We performed linear regression analysis controlling for potential confounders to estimate the association between physical activity and lung function. The con-founders were chosen based on the literature and our underlying theoretical model of how physical activity and lung function may be interrelated. The final model included height, birth weight, age, sex, BMI, physical activity, parental education, parental smoking, and the child’s history of asthma. Physical activity was catego-rized into four categories.

To examine how BMI and physical activity influence lung function, we con-structed a linear model. We conducted both unadjusted and adjusted analyses for boys and girls. There was a strong correlation between the child’s history of asthma and the parental history of asthma. Thus only one of these variables was included in the final model. We performed analysis with and without asthma in the model. Fur-thermore, we first excluded obese children, and then overweight children. Analyses were conducted in SPSS (Statistical Package for Social Sciences, Version 11 for Windows. SPSS Inc. Chicago, USA, 1999) and S-plus (Version 3.3 for Windows. Seattle, Washington: Statistical Sciences, a division of MathSoft, Inc, 1996).

Results

Table 1 describes the characteristics of the participating children. Girls had a lower lung function than boys (Table 1). Describing lung function by level of physical activity showed that lung function increased with increasing level of physical activity (Table 2). Furthermore, lung function was associated with BMI.

(4)

405 Boys (n = 1,299) Girls (n = 1,238) Mean SD Mean SD Age (yrs) 9.9 0.43 9.9 0.43 Height (cm) 140.5 6.29 140.0 6.38 FEV1 (l) 2.16 0.31 2.06 0.30 FVC (l) 2.45 0.36 2.26 0.34 Birth weight (kg) 3.59 0.57 3.47 0.53 BMI 17.9 2.32 17.7 2.45

Table 2 Lung Function Measured in FEV1 and FVC by Level of Physical Activity, Parental Education, Parental Smoking, Childhood Asthma and Body Mass Index (BMI)

Boys Girls % FEV1 FVC % FEV1 FVC Physical activity < once a week 2.5 2.05 2.31 6.0 1.98 2.15 Once a week 12.9 2.13 2.42 22.8 2.06 2.24 2–3 times a week 42.8 2.16 2.45 45.6 2.06 2.27 ≥ 4 times a week 39.6 2.17 2.47 20.5 2.09 2.29 Parental education (yr)

Two parents > 9 yr 84.8 2.17 2.45 84.3 2.07 2.26 One parent with > 9 yr 9.5 2.10 2.38 10.2 2.05 2.26 No parents > 9 yr 2.2 2.02 2.32 1.9 1.96 2.15 Parental smoking Yes 15.6 2.14 2.43 16.2 2.06 2.27 No 83.4 2.16 2.45 83.2 2.06 2.26 Childhood asthma Yes 6.2 2.16 2.49 3.2 1.99 2.27 No 93.5 2.16 2.44 96.7 2.06 2.26 BMI

Over- and normal weight 96.5 2.15 2.44 96.2 2.05 2.25

Obese 3.5 2.37 2.75 3.8 2.35 2.60

Normal weight 86.4 2.13 2.41 87.0 2.03 2.23 Overweight and obese 13.6 2.31 2.66 13.0 2.23 2.48

(5)

406 Berntsen et al.

Using the linear model in exploring the effect of physical activity on lung function with those who were physically active less than once a week as the refer-ence category, showed that FEV1 tended to increase with increasing level of

phys-ical activity also when adjusting for potential confounders (p = .02). FEV1

increased with 70 ml in those who were physically active ≥ 4 times a week. A similar pattern was present for FVC (p = .002; Table 3). Furthermore, using the individual physical activity values in the linear regression model with all variables showed that the slope was statistically significant (p = .001; data not shown). In addition, lung function increased with increasing height, birth weight, age, BMI (all, p < .001), and increasing level of parental education (p = .02). Childhood asthma and parental smoking was also included in the model but these were not statistically significant and did not influence the estimates. Separate analysis excluding first obese children, and second overweight children with and without asthma in the model gave similar results (data not shown).

Stratified analysis in boys and girls showed that the association between lung function and physical activity was only present among girls (p = .01). Further analysis using physical activity as the outcome in girls and boys showed that there was a strong association between height and physical activity among boys, which was not present among girls. Thus including height in the analysis reduced the association between physical activity and lung function among boys but not in girls.

Discussion

The results of the current study suggested that lung function was highest among children age 9 to 10 years with a high level of physical activity. In boys, the asso-ciation was influenced by height.

Due to the cross-sectional design of the current study, we cannot conclude that there is any causal relationship between level of physical activity and lung function. This is a major concern of the current study. The results can be attributed to the fact that children taking part in sports are characterized by better lung func-tion than inactive children. However, it is unlikely that minor differences in lung function such as a difference in FEV1 of 2–3% should influence children’s

physi-cal activity level. It is dubious that perceived exertion due to respiratory limitation in this range should result in inactivity in this age group. Our finding is more rel-evant in conceptualizing disease etiology within a life course framework (3,19). Thus it is important to identify factors that may influence lung function. During childhood the postnatal development of the lung is characterized by alveolar enlargement, peripheral airway elongation and both elongation and enlargement of the central airways (16), and it is plausible that these functional changes may be influenced by exercise. We also demonstrated that there tended to be a small dose response relationship between physical activity and lung function, which support that there may be an association between physical activity and lung func-tion in children. Excluding overweight children did also not influence the results. However, these findings need to be investigated further using a longitudinal design.

(6)

407

Body Mass Index (BMI) and Parental Education in Norwegian Schoolchildren Age 9 to 10 Years

FEV1 FVC

B* 95% CI B* 95% CI All (n = 2,537)

Level of physical activity

< than once a week 0 0

Once a week 53 7 100 69 18 120 2–3 times a week 53 8 97 75 27 124 ≥ 4 times a week 70 24 115 95 45 145 p = .02 p = .002 BMI (kg·m-2₎ ₁₇ ₁₃ ₂₁ ₂₈ ₂₃ ₃₂ p = .000 p = .000

Parental education (years)

Two parents with > 9 yr 0 0

One parent with > 9 yr −27 −56 3 −31 −64 1 No parents with > 9 yr −85 −150 20 −79 −151 −8

p = .011 p = .020

Boys (n = 1,299)

Once a week 39 −47 125 56 −39 152 2–3 times a week 37 −44 118 50 −40 140 ≥ 4 times a week 43 −38 124 65 −25 156 p = .769 p = .457 BMI (kg·m-2₎ ₁₃ ₇ ₁₈ ₂₆ ₂₀ ₃₂ p = .000 p = .000

One parent with > 9 yr −26 16 69 −42 −89 5 No parents with > 9 yr −110 20 200 −104 −204 −4

p = .032 p = .033

Girls (n = 1,238)

Once a week 54 −1 109 70 11 129

2–3 times a week 54 1 106 84 28 140

(7)

The strength of the current study is the large study population of children age 9 to 10 years. Lung function, height and weight were measured in a standardized way in all children by the same highly experienced and trained staff. All individ-ual flow-volume curves were also reviewed for technical acceptability and checked for reproducibility according to ERS (14).

The relationship between habitual physical activity and lung function in younger age groups is not well documented. One study of children has tested the impact of an enhanced physical education program upon the growth and develop-ment of static and dynamic lung volumes over a six years period (18). They found that a regular physical education program enhanced lung volumes in primary school students. Forced vital capacity increased in average with 3.2%. Physical active boys had an advantage of 7–8% the last 3 years of the study period. The impact of physical activity on FEV1 was less, but greatest (about 6%) among boys

during the last year of the intervention period. These findings support our observa-tions. Twisk et al. found also that physical activity was positively related to FVC and FEV1 in their study of tracking over time of lung function and their

relation-ship to lifestyle from 13 to 16 years of age and 21–27 years of age (20). It has also been suggested that physical activity must commence in childhood or adolescence to produce significant differences in lung function (23).The underlying pathophys-iology or mechanic behind the effect of exercise on lung function is not clear. However, different path ways related to smooth muscle activity are suggested (9).

In addition, we explored an interesting gender difference, which was explained by the finding that tall boys were more likely to be socialized into sports, which was not the case for girls in the same age group. Consequently, height influenced the effect of physical activity on lung function in boys in this age range.

It is previously shown that overweight and obesity may be a risk factor for childhood asthma (6). However, as earlier described in children 8 to 10 years of age we found that lung function increased in heavier children, which may be a result of height and stronger muscles that improves FVC and FEV1 (13).

Consis-tent with others we explored that boys tended to have improved lung function

Table 3 (continued) FEV1 FVC B* 95% CI B* 95% CI ≥ 4 times a week 90 34 146 114 54 175 p = 0.011 p= 0.002 BMI (kg·m–2₎ ₂₁ ₁₅ ₂₆ ₂₉ ₂₄ ₃₅ p = .000 p =.000

One parent with >9 yr −25 −67 16 −18 −63 26 No parents with >9 yr −59 −154 36 −55 −156 47

p = .254 p = .435

(8)

compared with girls (23). FEV1 and FVC growth for both boys and girls are

reported to be linear with age until the adolescence growth spurt. However, annual velocity as a function of age is different because of earlier and smaller growth spurt in girls (20). The mean age at which velocity of FVC and FEV1 seems to

occur is 12.3 years for girls and about 2 years later for boys. Height growth peak occur on average 6 to 9 months earlier than lung function growth peak (21). Our population was 9 to 10 years of age. Only a few had therefore reached the lung function growth peak.

In conclusion, the current study suggested that lung function was highest in highly physical active children age 9 to 10 years. In boys this association was influenced by height, because tall boys were more likely taking part in sports.

The significance of the present finding is that physical activity may influence the development of lung function in children. These results need, however, to be confirmed using a longitudinal study design including standardized objective assessments of level of physical activity.

Acknowledgments

The study was supported with grants from the Norwegian Research Council. The authors will like to thank head physician Per G. Lund-Larsen and his staff at the Norwegian Institute of Public Health for conducting excellent data collection.

References

1. Health Behaviour in School-Aged Children. A WHO Cross-National Survey. 4. Bergen, Norway: Research Center for Health Promotion, Univerisity of Bergen, 1994. 2. Andersen, L.F., I.T. Lillegaard, N. Overby, L. Lytle, K.I. Klepp, and L. Johansson.

Overweight and obesity among Norwegian school children: changes from 1993 to 2000. Scand. J. Public Health. 33:99–106, 2005.

3. Ben-Shlomo, Y., and D. Kuh. A life course approach to chronic disease epidemiol-ogy: concepual models, empirical challenges and interdisciplinary perspectives. Int. J. Epidemiol. 31:285–293, 2002.

4. Cole, T.J., M.C. Bellizzi, K.M. Flegal, and W.H. Dietz. Establishing a standard definition for child overweight and obesity worldwide: international survey. BMJ. 320:1240–1243, 2000.

5. Dollman, J., K. Norton, and L. Norton. Evidence for secular trends in children’s phys-ical activity behaviour. Br. J. Sports Med. 39:892–897, 2005.

6. Flaherman, V.R.G. A metha-analysis of the effect of high weight on asthma. Arch. Dis. Child. 91:334–339, 2006.

7. Huovinen, E., J. Kaprio, L.A. Laitinen, and M. Koskenvuo. Social predictors of adult asthma: a co-twin case-control study. Thorax. 56:234–236, 2001.

8. Irgens, L. The Medical Birth Registry of Norway. Epidemiological research and sur-veillance throughout 30 years. Acta Obstet. Gynecol. Scand. 79:435–439, 2000. 9. Lucas, S.R., and A.E. Platts-Mills. Physical activity and exercise in asthma: relevance

to etiology and treatment. J. Allergy Clin. Immunol. 115:928–934, 2005.

10. Makker, H.K., and S.T. Holgate. Mechanisms of exercise-induced asthma. Eur. J. Clin. Invest. 24:571–585, 1994.

11. Nafstad, P., J. Jaakkola, J.A. Hagen, G. Botten, and J. Kongerud. Breastfeeding, maternal smoking and lower respiratory tract infections. Eur. Respir. J. 9:2623–2629, 1996.

(9)

12. Nystad, W., H. Stigum, and K.H. Carlsen. Increased level of bronchial responsiveness in inactive children with asthma. Respir. Med. 95:806–810, 2001.

13. Perez-Padilla, R, R. Rojas, V. Torres, V. Borja-Aburto and G. Olaiz G. Obesity among children residing in Mexico City and its impact on lung function: a comparison with Mexican-Americans. Arch. Med. Res. 37:165–171, 2006.

14. Quanjer, P.H., G.J. Tammeling, J.E. Cotes, O.F. Pedersen, R. Peslin, and J.C. Yernault. Standardized lung function testing: lung volumes and forced ventilatory flows. 1993 update. Eur. Respir. J. 16:14–40, 1993.

15. Rasmussen, F., J. Lambrechtsen, H.C. Siersted, H.S. Hansen, and N.C.G. Hansen. Low physical fitness in childhood is associated with the development of asthma in young adulthood: the Odense schoolchild study. Eur. Respir. J. 16:866–870, 2000. 16. Rosenthal, M., and A. Bush. The growing lung: normal development, and the

long-term effects of pre- and postnatal insult. In: Growing up with lung disease: the lung in trasition to adult life, A. Bush, K-H. Carlsen, and M.S. Zach (Eds.). Sheffield, UK: European Respiratory Society Journals Ltd, 2002, pp. 1–25.

17. Shaaban, R., B. Leynaert, D. Soussan, et al. Physical activity and bronchial hyper-responsiveness: European Community Respiratory Health Survey II. Thorax. 62:403–410, 2007.

18. Shepard, R.J., and H. Lavallee. Effects of enhanced physical education on lung vol-umes of primary school children. J Sports Med Phys Fitness. 36:186–194, 1996. 19. Strachan, D.P. Respiratory and allergic diseases. In: A life course approach to chronic

disease epidemiology, D. Kuh and Y. Ben-Shlomo (Eds.). Oxford, UK: Oxford Uni-versity Press, 1997, pp. 101–120.

20. Twisk, J., B. Staal, M. Brinkman, H. Kemper, and W. van Mechelen. Tracking of lung function parameters and the longitudinal relationship with lifestyle. Eur. Respir. J. 12:627–634, 1998.

21. Wang, X., D.W. Dockery, D. Wypij, et al. Pulmonary function growth velocity in children 6 to 18 years of age. Am. Rev. Respir. Dis. 148:1502–1508, 1993.

22. Wilson, N., and M. Silverman. Bronchial responsiveness and its measurement. In: Childhood asthma and other wheezing disorders, M. Silverman (Ed.). London: Chap-man & Hall, 1995, pp. 141–174.

23. Woolcock, A.J., M.H. Colman, and C.R.B. Blackburn. Factors affecting normal values for ventilatory lung function. Am. Rev. Respir. Dis. 106:692–709, 1972.

24. World Health Organization. Obesity: Preventing and managing the global epidemic. Report of a WHO consultation on obesity, Geneva, 3-5 June 1997. 1998. Geneva, Switzerland: World Health Organization.