1 Department of Public Health, School of Medicine, Universidad de los Andes, Bogotá, Colombia. an-rami2@uniandes.edu.co, osarmien@uniandes.edu.co
2 Department of Internal Medicine, Fundación Santa Fe de Bogotá, Universidad de los Andes. Bogotá, Colombia. john.duperly@ama.com.co
3 School of Public Health and Primary Care. Prince of Wales Hospital. Co-Director Centre for Occupational & Environmental. Health Studies in the Chinese University of Hong Kong. twwong@cuhk.edu.hk
4 Department of Chemical and Environmental Engineering, Universidad Nacional de Colombia, Bogotá, Colombia. nyrojasr@unal.edu.co
5 Department of Physical Culture, Faculty of Education and Human Sciences. Universidad de Córdoba. Montería, Colombia. cmarangop@gmail.com
6 Environmental Engineering Research Center (CIIA), Civil and Environmental Department. Universidad de los Andes. Bogotá, Colombia. and-mald@uniandes.edu
7 Secretaría Distrital de Salud, Department of Pediatrics, Fundación Santa Fe de Bogotá. Colombia. gusarist@hotmail.com
8 Pulmonary Physiology Department, Fundación Santa Fe de Bogotá. Colombia. ltpfisioterapia@yahoo.com
9 Office for Global Health Promotion. National Center for Chronic Disease Prevention and Health Promotion. Director’s office.Centers for Disease Control and Prevention (CDC). Atlanta, EE.UU. hgn0@cdc.gov

ABSTRACT

Key Words: Physical fitness, air pollution, particulate matter, physical exertion, paediatrics (source: MeSH, NML).

RESUMEN

Objetivo Comparar el acondicionamiento cardiorespiratorio medido como VO2máximo en niños escolarizados expuestos a diferentes niveles de PM₁₀ en Bogotá.
Métodos Estudio de corte transversal. Se incluyeron 1045 niños de 7-12 años de 4 colegios públicos con diferentes corredores viales y sistemas de transporte público. Tres colegios tenían alta contaminación (AC) y uno baja contaminación (BC). Se aplicó una encuesta a niños y padres sobre características sociodemográficas, actividad física, antecedentes de enfermedades respiratorias y salud. Se midió objetivamente peso y talla para calcular el índice masa corporal. El VO2 máximo se estimó con la prueba de Leger validada para Bogotá. Se realizaron espirometrìas en 435 niños.
Resultados Después de ajustar por covariables, no se encontraron diferencias significativas en el VO2 máximo de los niños en colegios con BC ò AC. (Niñas BC: 45,8ml/kg/min vs. AC: 44,6ml/kg/min; p=0,11, niños BC: 47,2ml/kg/min vs. AC: 48,2ml/kg/min; p=0,41).
Conclusión No se encontraron diferencias en el VO2 máximo de los niños que asistían a los colegios de AC ó BC. Se recomienda un estudio longitudinal que evalúe los niveles deVO2 máximo en los niños expuestos a áreas altamente contaminadas.

Palabras Clave: Acondicionamiento físico, contaminación del aire; material particulado, ejercicio, pediatría (fuente: DeCS, BIREME).

Research has shown that exposure to high air pollutant concentrations as particulate matter (PM) is associated with respiratory symptoms, decreased pulmonary function and the development of chronic respiratory diseases (1-4). A highly-polluted environment is a threat to children’s health; the highest environmental disease burden and death toll are concentrated among developing nations’ children, according to the World Health Organization (3).

Evidence has shown that children whose houses or schools are close to roads having high traffic density have increased respiratory symptoms and lower pulmonary function (5-8).Increased health risks are associated with exposure to high levels of air pollutants amongst school-aged children. Specific mechanisms include on-going lung growth, an incomplete metabolic system, immature host defense, high rates of respiratory infection and outdoor activity patterns (9-10). Short- and long-term exposure to air pollution represents a risk factor for non-communicable disease (NCD) which are the main cause of disability and mortality in Latin-America (11).

Physical activity (PA) is a major protective factor against NCD, beginning in childhood (12); nonetheless, promoting outdoor PA while protecting children from contact with air pollutants such as PM₁₀ continues to be a dilemma, particularly in highly-polluted urban settings (13-15) and rapidly-growing mega-cities in Latin-America, such as Mexico City, Santiago de Chile and Bogotá (16-17).

Inactivity rates and childhood obesity in these cities are growing rapidly. For example, 47.0 % of children in Chile and 44.0 % in Colombia spend 3 or more hours per day engaged in sedentary activities (18). Regarding obesity, it has been estimated that 33 % of children are overweight and 7 % obese in the Americas (19); however, a protective effect of PA while being exposed to air pollution has not been clearly established regardingVO2 max a protetive affect of PA while being exposed to air pollution has not been clearly established (20).

Although VO2 max in children and young people is highly influenced by genetic conditions, PA levels constitute its primary determinant (21). Despite the importance of adequate fitness levels for children and young people’s health and well-being, VO₂max and pulmonary function variation due to exercising in areas having high air pollutant levels have only been documented in a few studies involving small sample sizes (21), by contrast with large bodies of evidence for adults (22-23).

To our knowledge, no studies in Latin-America have dealt with an association between children’sVO₂max and air pollution despite the fact that the region contains three of the most polluted urban center in the world (the aforementioned Santiago de Chile, Sao Paulo and Bogotá), transportation being the leading cause of PM air pollution in all of them (16,17,24).

Bogotá provides a useful setting for evaluating PM₁₀ air pollution and VO₂max in children for the first time in Latin-America because it has several PA-promoting urban programs and also intends to introduce changes in its transport system (17,25). This study was aimed at assessing whether VO₂max values differed amongst children exposed to different levels of PM₁₀ air pollution due to varying levels of traffic density.

Study population and school setting
A cross-sectional study was conducted during 2006-2007 in Colombia’s capital, Bogotá, located about 2,640 meters above sea level. Bogotá has around 7 million inhabitants, 1.8 million of whom are less than 18 years old. This city has no seasons. Bogotá is one of the most polluted cities in Latin-America (26), PM₁₀ being the main pollutant (26).

The study population was formed by 1,045 children aged 7 to 12 years attending four public schools in Bogotá. Twenty-three of the 737 public schools in the city were selected because they were located less than 100 meters from the main motorized transport corridors. All the schools were served by an old public transport system (OPTS) with or without a rapid bus transit system (known as TransMilenio). Only four of these 23 schools met the inclusion criteria, i.e. being located 2 to 5 meters from a busy street (transport corridor), having boys and girls, having elementary and middle school and having agreed to participate in the study for at least five years.

School 1 acted as control as it was located in a semi-rural area next to a transport corridor having an OPTS, had low traffic density, did not have TransMilenio and had the lowest PM air pollution levels in Bogotá. School 2 was served by an OPTS with no plans for conversion to TransMilenio. School 3 was served by an OPTS which had plans for conversion to TransMilenio in the next few years. School 4 had mixed traffic that included both an OPTS and TransMilenio.

Data collection
Data was collected from 7-12 year-old children and their parents using face-to-face questionnaires after written informed consent had been obtained. All protocols and questionnaires were reviewed and approved by the Universidad de los Andes and Fundación Santa Fe de Bogotá ethics committees.

Outcome variables
Predicted maximum oxygen uptake. VO₂max was calculated using the Leger 20m shuttle run test for girls and boys aged 7 to12 years based on the longest distance (m) run by each child, which had been previously validated for Bogotá (27). The test consisted of asking a child to run between 2 lines marked 20 meters apart according to an increasing pace audio record, and to stop because of fatigue. VO₂max was calculated from the Leger equation based on each child’s age and the longest distance (m) they ran (28).

Independent variables
Sociodemographic factors. Individual variables included gender, age, maternal educational attainment, socioeconomic status, health insurance and maternal employment. The children had to have lived for at least one year in the particular area.

Health-related characteristics. The International Study on Asthma and Allergies in Childhood (ISAAC) questionnaire (previously adapted for children in Bogotá) was used to evaluate respiratory- and asthma-related symptoms (29).Health-related factors for each child included past respiratory diseases, wheezing during the last 12 months and during PA, a diagnosis of asthma, current smoking and passive exposure to smoking in their households.

PA was assessed by using an adapted version of the 3-day physical activity recall (3DPAR) questionnaire (30); the Bogotá version measured two days (a weekday and a Sunday). PA variables included meeting PA recommendations (PAR) (at least 1 hour of moderate to vigorous PA per day) for school-aged young people (31). Height and weight, measured by trained personnel using calibrated equipment, were used to calculate the body mass index (BMI) according to World Health Organization growth charts (32); children were classified accordingly.

Lung function testing. Lung function was tested on a subsample of 434 children by a certified respiratory therapist following American Thoracic Society recommendations. A portable Jaeger Spiro Pro was used for spirometry, based on the Knudson spirometric reference values for Hispanic children (33). The tests for forced expiratory volume (FEV1) and forced vital capacity (FVC) were performed at least three times during the trial and the results were reviewed by a paediatric pneumologist.

Air pollutant concentration. The schools PM₁₀ was measured using gravimetric techniques, namely Air Diagnostics Inc.’s Harvard Impact or (HI) and MS&T area sampler (MS&T area sampler; Air Diagnostics Inc, Harrison, USA) located inside the schools at 3 locations: the Closest point to the nearby road, 2 to 5 meters from the edge of the main road and 1-5 meters from outdoor PA facilities. Samples were taken daily at each school between 7:00 am and 3:00 pm for four weeks (34).

School 1, located in a slightly-polluted area (SP), served as the control group (55.3μg.m^-3PM₁₀ mean value: SE 4.2); because it had a mean 50 μg.m^-3PM₁₀concentration it was considered a less-polluted area (34). Schools 2, 3 and 4 did not differ significantly regardingPM₁₀ concentration (90.5μg.m^-3, 87.8 μg.m^-3 and 90.4 μg.m^-3PM₁₀, respectively) and were put into the highly-polluted category (HP).

Personal exposure to PM₁₀ and traffic density were measured (such data was not included in the statistical analysis). PM₁₀ concentration was not measured during the Leger 20-m shuttle run test.

Statistical analysis
The first step in multilevel analysis described differences between HP and SP schools regarding the students’ socio-demographic and health characteristics as assessed by X2 or t-test (depending on whether they were percentages or means). A hierarchical linear regression analysis was used for estimating unadjusted and adjusted means for VO₂max. Additional analysis stratified the data by gender in the subpopulation of children suffering asthma and the subpopulation of children who had a spirometry reading. The models were fitted using the MIXED procedure in SAS 9.1 (SAS Institute, Cary, NC, USA) to adjust the clustering effect within schools; all models assumed only the random intercept form.

General characteristics
Mean PM₁₀concentration outside school during 2007 was 35.1μg.m^-3in the SP school and 70.1μg.m^-3, 72.3μg.m^-3and 70.1μg.m^-3in the HP schools; there was also higher traffic density outside HP schools than the SP school.

Study response rate was 95.4 % for children eligible for Leger test in HP locations and 64.3 % in the SP area. SP and HP school samples were not even because the SP school had few students and was the only school in Bogotá which met the stated criteria to be the control (Table 1). The children in the sample were evenly distributed by gender (48.8 % girls cf 51.2 % boys), average age being 9.8 years (SD=1.5). 79.6 % of the children’s mothers had reached more than elementary education level, 30.9 % of the mothers/guardians were not currently working and 71.0 % of the population reported living in low- or middle-income neighborhoods. 92.1 % of the children were covered by health insurance. Regarding respiratory symptoms, 6.5 % reported wheezing during the last year, 2.3 % reported wheezing during exercise and 4.0 % had had asthma diagnosed by a doctor.

Less than 1.0 % of the parents reported smoking and 13.6 % reported their children being exposed to second-hand smoking. More than 70.5 % of the children met PA recommendations and 80.5% had normal BMI; however, 18.5 % of children were at risk of being overweight, were overweight or obese.

Severely wasted and wasted categories were collapsed into one due to a lack of data. No differences by type of school emerged for most sociodemographic and health characteristics (Table 1), except for age, SES and vigorous PA, i.e. students from HP schools were older, more likely to live in middle-income neighborhoods but less likely than students from SP locations to meet vigorous PAR.

VO₂max
Overall VO₂max mean was 46.5ml.kg-1.min-1 (SE=0.4). Significant differences between VO₂max were found in unadjusted analysis by age-group and BMI classification in girls and boys.

Significant differences in VO₂max were only found in the subsample of girls with spirometry regarding lung function (specifically, 45.9 ml.kg-1.min-1 for the girls with FEV1/FVC>80.0 % and 44.2 ml.kg-1.min-1 for girls with FEV1/FVC<80.0 %; p=0.03) (Table 2).

A significant difference in VO2 max was found in adjusted analysis for BMI regarding gender (girls’ BMI 45.2 ml.kg-1.min-1 for normal BMI and 43.1 ml.kg-1.min-1 for overweight or obese category; p=<0.001). Regarding PAR and VO₂max, children who met the PAR in the SP had slightly higher VO₂max values than those in the HP; however, the results were not statistically significant (Table 3).

High air pollutant concentrations have been related to health problems in children living in urban areas (5-9,35). A low CF in children and adolescents is associated with an increased risk of NCD (36,37). Nonetheless, no significant difference was found in this study regarding the VO₂max of girls or boys attending the SP or HP schools, or for meeting the PA recommendation for children attending the SP or HP schools.

The harmful respiratory effect of PM air pollution on VO₂max has yet to be determined due to the limited information available concerning this topic. For example, a previous study in Hong Kong showed abnormal VO₂max values having 1 ml.kg-1.min-1difference between HP and SP areas (20); also, PA had no beneficial effect on VO₂max values for children living in HP areas.

Although the VO₂max values in our results were considered normal according to FITNESSGRAM cardio respiratory fitness standards for adolescents (a VO₂max value below 35 ml.kg-1.min-1 for girls and 42 ml.kg-1.min-1for boys) in recent studies with American and European populations (37), a longitudinal study should be undertaken to show how VO₂max in children is affected by longer exposure to air pollutants.

Recommended policy change in Bogotá (Law 15/2008) aimed to promote a healthy environment for the population by enhancing diesel quality by 2012 to comply with the 50 parts per million of sulphur international standard. By so reducing PM emission, urban air quality can be improved and air pollution’s negative respiratory health impact reduced. Other examples of air pollution policy can be seen in Chile, Sao Paulo and Mexico where air quality management plans and surveillance systems have been created for controlling air pollution levels. Sustainable transport projects in Chile, Colombia, Mexico, Peru and Brazil have been aimed at decreasing PM concentrations to improve outdoor air quality (1).

This study’s limitations included the uneven SP school sample compared to the HP schools and assessment of exposure to outdoor pollutants only took PM₁₀into account. The cross-sectional study design necessarily limited analysis of any cause and effect relationship between VO₂max and PM₁₀ air pollution. Despite these limitations, this study has provided a baseline for longitudinal assessment of cardiorespiratory fitness in children and took most factors affecting VO₂maxinto account. Changes in Bogotá’s transport system may facilitate a natural experimental study aimed at assessing the effects of PM on children’s cardiorespiratory fitness.

It is thus recommended that physicians and parents who are currently uncertain about proper recommendations for PA in highly-polluted environments should encourage children to engage in PA when daytime concentrations of PM₁₀ are at their lowest in open rural land or indoors if they are engaging in PA close to a road or during peak PM₁₀ hours. Based on real-time PM₁₀ and PM 2.5 measurements, the lowest concentrations outdoors and in PA facilities occur between 10:30 am and noon, which should therefore be the recommended time for physical education classes. Thermal inversion significantly increases PM concentration before 9:00 am, and thereby exposure; students should preferably not be engaging in PA (especially outside and near major highways) at that time (34).

Acknowledgments: We would like to thank the four public schools and students who participated in this study. We would like to acknowledge valuable comments made by Eduardo Behrentz, Juan Felipe Franco, Julian Marshall, Juan Carlos Correa, Jairo Roa, librarian Jenny Milena Machetáand medical students Camilo Andrés Diaz, Jairo Alberto Dussan, Alejandra Isabel de Zubiria, Juan Camilo Diazand Fernando Salguero. Also, we would like to acknowledge the Colombian science, Technology and Innovation Department (COLCIENCIAS) program "Jovenes Investigadores e innovadores" which supported the work of Andrea Ramirez (convocatoria 525-2011).

Funding
The research was mainly carried out at Universidad de los Andes, Bogota.

This study was financed by a grant (#1204-04-18148) awarded by the Colombian Science, Technology and Innovation Department (Colciencias), the Environmental Engineering Research Centre (CIIA), the Schools of Medicine at the Universidad de Los Andes and the Pontificia Universidad Javeriana and the Schools of Engineering at the Universidad de Los Andes and the Universidad Nacional de Colombia. The study also received funding through a grant awarded by the Fundación Santa Fe de Bogotá’s Health Research and Study Centre and the Universidad de Los Andes’ School of Medicine.

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