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Proceedings of the National Academy of Sciences of the United States of America | 2015

Green spaces and cognitive development in primary schoolchildren

Payam Dadvand; Mark J. Nieuwenhuijsen; Mikel Esnaola; Joan Forns; Xavier Basagaña; Mar Alvarez-Pedrerol; Ioar Rivas; Mónica López-Vicente; Montserrat De Castro Pascual; Jason G. Su; Michael Jerrett; Xavier Querol; Jordi Sunyer

Significance Green spaces have a range of health benefits, but little is known in relation to cognitive development in children. This study, based on comprehensive characterization of outdoor surrounding greenness (at home, school, and during commuting) and repeated computerized cognitive tests in schoolchildren, found an improvement in cognitive development associated with surrounding greenness, particularly with greenness at schools. This association was partly mediated by reductions in air pollution. Our findings provide policymakers with evidence for feasible and achievable targeted interventions such as improving green spaces at schools to attain improvements in mental capital at population level. Exposure to green space has been associated with better physical and mental health. Although this exposure could also influence cognitive development in children, available epidemiological evidence on such an impact is scarce. This study aimed to assess the association between exposure to green space and measures of cognitive development in primary schoolchildren. This study was based on 2,593 schoolchildren in the second to fourth grades (7–10 y) of 36 primary schools in Barcelona, Spain (2012–2013). Cognitive development was assessed as 12-mo change in developmental trajectory of working memory, superior working memory, and inattentiveness by using four repeated (every 3 mo) computerized cognitive tests for each outcome. We assessed exposure to green space by characterizing outdoor surrounding greenness at home and school and during commuting by using high-resolution (5 m × 5 m) satellite data on greenness (normalized difference vegetation index). Multilevel modeling was used to estimate the associations between green spaces and cognitive development. We observed an enhanced 12-mo progress in working memory and superior working memory and a greater 12-mo reduction in inattentiveness associated with greenness within and surrounding school boundaries and with total surrounding greenness index (including greenness surrounding home, commuting route, and school). Adding a traffic-related air pollutant (elemental carbon) to models explained 20–65% of our estimated associations between school greenness and 12-mo cognitive development. Our study showed a beneficial association between exposure to green space and cognitive development among schoolchildren that was partly mediated by reduction in exposure to air pollution.


PLOS Medicine | 2015

Association between traffic-related air pollution in schools and cognitive development in primary school children: a prospective cohort study.

Jordi Sunyer; Mikel Esnaola; Mar Alvarez-Pedrerol; Joan Forns; Ioar Rivas; Mónica López-Vicente; Elisabet Suades-González; Maria Foraster; Raquel Garcia-Esteban; Xavier Basagaña; Mar Viana; Marta Cirach; Teresa Moreno; Andrés Alastuey; Núria Sebastián-Gallés; Mark J. Nieuwenhuijsen; Xavier Querol

Background Air pollution is a suspected developmental neurotoxicant. Many schools are located in close proximity to busy roads, and traffic air pollution peaks when children are at school. We aimed to assess whether exposure of children in primary school to traffic-related air pollutants is associated with impaired cognitive development. Methods and Findings We conducted a prospective study of children (n = 2,715, aged 7 to 10 y) from 39 schools in Barcelona (Catalonia, Spain) exposed to high and low traffic-related air pollution, paired by school socioeconomic index; children were tested four times (i.e., to assess the 12-mo developmental trajectories) via computerized tests (n = 10,112). Chronic traffic air pollution (elemental carbon [EC], nitrogen dioxide [NO2], and ultrafine particle number [UFP; 10–700 nm]) was measured twice during 1-wk campaigns both in the courtyard (outdoor) and inside the classroom (indoor) simultaneously in each school pair. Cognitive development was assessed with the n-back and the attentional network tests, in particular, working memory (two-back detectability), superior working memory (three-back detectability), and inattentiveness (hit reaction time standard error). Linear mixed effects models were adjusted for age, sex, maternal education, socioeconomic status, and air pollution exposure at home. Children from highly polluted schools had a smaller growth in cognitive development than children from the paired lowly polluted schools, both in crude and adjusted models (e.g., 7.4% [95% CI 5.6%–8.8%] versus 11.5% [95% CI 8.9%–12.5%] improvement in working memory, p = 0.0024). Cogently, children attending schools with higher levels of EC, NO2, and UFP both indoors and outdoors experienced substantially smaller growth in all the cognitive measurements; for example, a change from the first to the fourth quartile in indoor EC reduced the gain in working memory by 13.0% (95% CI 4.2%–23.1%). Residual confounding for social class could not be discarded completely; however, the associations remained in stratified analyses (e.g., for type of school or high-/low-polluted area) and after additional adjustments (e.g., for commuting, educational quality, or smoking at home), contradicting a potential residual confounding explanation. Conclusions Children attending schools with higher traffic-related air pollution had a smaller improvement in cognitive development.


Environmental Health Perspectives | 2014

Green and blue spaces and behavioral development in Barcelona schoolchildren: the BREATHE project

Elmira Amoly; Payam Dadvand; Joan Forns; Mónica López-Vicente; Xavier Basagaña; Jordi Julvez; Mar Alvarez-Pedrerol; Mark J. Nieuwenhuijsen; Jordi Sunyer

Background: Green spaces have been associated with improved mental health in children; however, available epidemiological evidence on their impact on child behavioral development is scarce. Objectives: We investigated the impact of contact with green spaces and blue spaces (beaches) on indicators of behavioral development and symptoms of attention deficit/hyperactivity disorder (ADHD) in schoolchildren. Methods: This study was based on a sample of 2,111 schoolchildren (7–10 years of age) from 36 schools in Barcelona in 2012. We obtained data on time spent in green spaces and beaches and Strengths and Difficulties Questionnaires (SDQ) from parents, and ADHD/DSM-IV questionnaires from teachers. Surrounding greenness was abstracted as the average Normalized Difference Vegetation Index (NDVI) in buffers of 100 m, 250 m, and 500 m around each home address. Proximity to green spaces was defined as living within 300 m of a major green space (≥ 0.05 km2). We applied quasi-Poisson mixed-effects models (with school random effect) to separately estimate associations between indicators of contact with green spaces and SDQ and ADHD total and subscale scores. Results: We generally estimated beneficial associations between behavioral indicators and longer time spent in green spaces and beaches, and with residential surrounding greenness. Specifically, we found statistically significant inverse associations between green space playing time and SDQ total difficulties, emotional symptoms, and peer relationship problems; between residential surrounding greenness and SDQ total difficulties and hyperactivity/inattention and ADHD/DSM-IV total and inattention scores; and between annual beach attendance and SDQ total difficulties, peer relationship problems, and prosocial behavior. For proximity to major green spaces, the results were not conclusive. Conclusion: Our findings support beneficial impacts of contact with green and blue spaces on behavioral development in schoolchildren. Citation: Amoly E, Dadvand P, Forns J, López-Vicente M, Basagaña X, Julvez J, Alvarez-Pedrerol M, Nieuwenhuijsen MJ, Sunyer J. 2014. Green and blue spaces and behavioral development in Barcelona schoolchildren: the BREATHE Project. Environ Health Perspect 122:1351–1358; http://dx.doi.org/10.1289/ehp.1408215


Environmental Health Perspectives | 2015

Traffic-Related air pollution, noise at school, and behavioral problems in barcelona schoolchildren: A cross-sectional study

Joan Forns; Payam Dadvand; Maria Foraster; Mar Alvarez-Pedrerol; Ioar Rivas; Mónica López-Vicente; Elisabet Suades-González; Raquel Garcia-Esteban; Mikel Esnaola; Marta Cirach; James Grellier; Xavier Basagaña; Xavier Querol; Mònica Guxens; Mark J. Nieuwenhuijsen; Jordi Sunyer

Background: The available evidence of the effects of air pollution and noise on behavioral development is limited, and it overlooks exposure at schools, where children spend a considerable amount of time. Objective: We aimed to investigate the associations of exposure to traffic-related air pollutants (TRAPs) and noise at school on behavioral development of schoolchildren. Methods: We evaluated children 7–11 years of age in Barcelona (Catalonia, Spain) during 2012–2013 within the BREATHE project. Indoor and outdoor concentrations of elemental carbon (EC), black carbon (BC), and nitrogen dioxide (NO2) were measured at schools in two separate 1-week campaigns. In one campaign we also measured noise levels inside classrooms. Parents filled out the strengths and difficulties questionnaire (SDQ) to assess child behavioral development, while teachers completed the attention deficit/hyperactivity disorder criteria of the DSM-IV (ADHD-DSM-IV) list to assess specific ADHD symptomatology. Negative binomial mixed-effects models were used to estimate associations between the exposures and behavioral development scores. Results: Interquartile range (IQR) increases in indoor and outdoor EC, BC, and NO2 concentrations were positively associated with SDQ total difficulties scores (suggesting more frequent behavioral problems) in adjusted multivariate models, whereas noise was significantly associated with ADHD-DSM-IV scores. Conclusion: In our study population of 7- to 11-year-old children residing in Barcelona, exposure to TRAPs at school was associated with increased behavioral problems in schoolchildren. Noise exposure at school was associated with more ADHD symptoms. Citation: Forns J, Dadvand P, Foraster M, Alvarez-Pedrerol M, Rivas I, López-Vicente M, Suades-Gonzalez E, Garcia-Esteban R, Esnaola M, Cirach M, Grellier J, Basagaña X, Querol X, Guxens M, Nieuwenhuijsen MJ, Sunyer J. 2016. Traffic-related air pollution, noise at school, and behavioral problems in Barcelona schoolchildren: a cross-sectional study. Environ Health Perspect 124:529–535; http://dx.doi.org/10.1289/ehp.1409449


Environmental Health Perspectives | 2016

Neurodevelopmental deceleration by urban fine particles from different emission sources: A longitudinal observational study

Xavier Basagaña; Mikel Esnaola; Ioar Rivas; Fulvio Amato; Mar Alvarez-Pedrerol; Joan Forns; Mónica López-Vicente; Jesús Pujol; Mark J. Nieuwenhuijsen; Xavier Querol; Jordi Sunyer

Background: A few studies have reported associations between traffic-related air pollution exposure at schools and cognitive development. The role of PM components or sources other than traffic on cognitive development has been little explored. Objectives: We aimed to explore the role of PM sources in school air on cognitive development. Methods: A cohort of 2,618 schoolchildren (average age, 8.5 years) belonging to 39 schools in Barcelona (Spain) was followed up for a year. Children completed computerized tests assessing working memory, superior working memory, and inattentiveness during four visits. Particulate matter ≤ 2.5 μm (PM2.5) was measured during two 1-week campaigns in each school, both outdoors and in the classroom. Source apportionment resulted in nine sources: mineral, organic/textile/chalk, traffic, secondary sulfate and organics, secondary nitrate, road dust, metallurgy, sea spray, and heavy oil combustion. Differences in cognitive growth trajectories were assessed with mixed models with age-by-source interaction terms. Results: An interquartile range increase in indoor traffic-related PM2.5 was associated with reductions in cognitive growth equivalent to 22% (95% CI: 2%, 42%) of the annual change in working memory, 30% (95% CI: 6%, 54%) of the annual change in superior working memory, and 11% (95% CI: 0%, 22%) of the annual change in the inattentiveness scale. None of the other PM2.5 sources was associated with adverse effects on cognitive development. Conclusions: Traffic was the only source of fine particles associated with a reduction in cognitive development. Reducing air pollution from traffic at primary schools may result in beneficial effects on cognition. Citation: Basagaña X, Esnaola M, Rivas I, Amato F, Alvarez-Pedrerol M, Forns J, López-Vicente M, Pujol J, Nieuwenhuijsen M, Querol X, Sunyer J. 2016. Neurodevelopmental deceleration by urban fine particles from different emission sources: a longitudinal observational study. Environ Health Perspect 124:1630–1636; http://dx.doi.org/10.1289/EHP209


Frontiers in Psychology | 2016

Developmental Trajectories in Primary Schoolchildren Using n-Back Task

Mónica López-Vicente; Joan Forns; Elisabet Suades-González; Mikel Esnaola; Raquel Garcia-Esteban; Mar Alvarez-Pedrerol; Jordi Julvez; Miguel Burgaleta; Núria Sebastián-Gallés; Jordi Sunyer

Background: Neuropsychological instruments to assess cognitive trajectories during childhood in epidemiological studies are needed. This would improve neurodevelopment characterization in order to identify its potential determinants. We aimed to study whether repeated measures of n-back, a working memory task, detect developmental trajectories in schoolchildren during a 1-year follow-up. Methods: We administered the n-back task to 2897 healthy children aged 7–11 years old from 39 schools in Barcelona (Spain). The task consisted of 2 levels of complexity or loads (2- and 3-back) and 2 different stimuli (numbers and words). Participants performed the task four times from January 2012 to March 2013. To study the trajectories during the follow-up, we performed linear mixed-effects models including school, individual and age as random effects. Results: We observed improvements related to age in n-back outcomes d′, HRT and accuracy, as well as reduced cognitive growth at older ages in d′ and HRT. Greater improvements in performance were observed at younger ages, in 2-back, in verbal rather than numerical stimuli and in girls compared to boys. Boys responded faster at baseline, while girls showed increased growth in 2-back numbers. Children with ADHD (Attention Deficit and Hyperactivity Disorder) symptoms (15% of boys and 6% of girls) had a lower working memory at baseline, but they showed similar cognitive growth trajectories in numbers variants of the task, as compared to children without ADHD symptoms. However, the age-related improvement in response speed was not observed in children with ADHD symptoms. Conclusions: Changes in n-back outcomes reflected developmental trajectories in 1-year follow-up. The present results suggest that the repeated administration of this task can be used to study the factors that may alter the cognitive development during childhood.


Neuroepidemiology | 2015

Environment and Brain Development: Challenges in the Global Context

Jordi Julvez; Tomáš Paus; David C. Bellinger; Brenda Eskenazi; Henning Tiemeier; Neil Pearce; Beate Ritz; Tonya White; Paul Ramchandani; Juan Domingo Gispert; Sylvane Desrivières; Rachel M. Brouwer; Olivier Boucher; Silvia Alemany; Mónica López-Vicente; Elisabet Suades-González; Joan Forns; Philippe Grandjean; Jordi Sunyer

a Centre for Research in Environmental Epidemiology, and b Fundació Pasqual Maragall, Plataforma de Neuroimatge, Barcelona, Catalonia , Spain; c The Rotman Research Institute, Departments of Psychology and Psychiatry, University of Toronto, Toronto, Ont. , and d Centre de Recherche en Neuropsychologie et Cognition, Département de Psychologie, Université de Montréal, Montreal, Que. , Canada; e Child Mind Institute, New York, N.Y. , f Department of Psychiatry, Harvard Medical School and Boston Children’s Hospital, g Department of Environmental Health, Harvard School of Public Health, Boston, Mass. , h Center for Environmental Research and Children’s Health (CERCH), School of Public Health, University of California, Berkeley, Calif. , and i Department of Epidemiology, University of California at Los Angeles School of Public Health, Los Angeles, Calif. , USA; j Department of Psychiatry, Erasmus Medical Centre, k Department of Child and Adolescent Psychiatry/Psychology, Erasmus MC-Sophia Children’s Hospital, Rotterdam , and l Department of Psychiatry, Brain Center Rudolf Magnus, University Medical Center Utrecht, Utrecht , The Netherlands; m London School of Hygiene and Tropical Medicine, n Unit of Child and Adolescent Psychiatry, Imperial College London, and o SGDP Centre, Institute of Psychiatry, Psychology and Neuroscience, King’s College London, London , UK


Environmental Research | 2017

Longitudinal association between air pollution exposure at school and cognitive development in school children over a period of 3.5 years.

Joan Forns; Payam Dadvand; Mikel Esnaola; Mar Alvarez-Pedrerol; Mónica López-Vicente; Raquel Garcia-Esteban; Marta Cirach; Xavier Basagaña; Mònica Guxens; Jordi Sunyer

Introduction: Recently, we showed that exposure to traffic‐related air pollutants (TRAPs) at school was negatively associated with cognitive development, specifically working memory and inattentiveness, in primary schoolchildren during a course of 12 months. The persistence of such associations over longer periods remains as an open question. Objective: To study the longitudinal association between TRAPs at school and cognitive development over a period of 3.5 years. Methods: Indoor and outdoor levels of TRAPs (elemental carbon (EC), dioxide nitrogen (NO2), particulate matter (PM2.5) from traffic sources and ultrafine particles (UFP)) were measured at 39 schools across Barcelona during 2012/2013. Working memory, as a measure of cognitive development, was evaluated 4 times in 2012/2013 assessment and was re‐evaluated one more time in 2015 using computerized n‐back test (3‐back d′ as main outcome). Linear mixed effects models were used to test the association between TRAPs and 3‐back d′, adding child and school as random effects to account for the multilevel nature of the data, and school air pollutants levels (one at a time) as predictor. Results: We found detrimental associations between all TRAPs and annual change in 3‐back d′ (working memory) (i.e. slower development of working memory in children attending schools with higher levels of air pollution). The associations (per one interquartile range increase in exposure) were strongest for outdoor NO2 (Coefficient (Coef) = − 4.22, 95% confidence interval (CI), − 6.22, − 2.22) and indoor UFP (Coef = − 4.12, 95%CI, − 5.68, − 1.83). These reductions were equivalent to − 20% (95%CI, − 30.1, − 10.7) and − 19.9% (95%CI, − 31.5, − 8.4) change in annual working memory development associated with one interquartile range increase in outdoor NO2 and indoor UFP, respectively. Conclusion: Our findings suggest the persistence of the negative association between TRAPs exposure at school and cognitive trajectory measured by n‐back test over a period of 3.5 years. HighlightsLong‐term association between TRAPs at school and cognitive development in schoolchildren.TRAPs at school were measured during the 2012/2013 assessment.Cognitive development (working memory) was assessed by a computerized n‐back task.All TRAPs levels at school were negatively associated with cognitive development.A reduction of 10%–20% per year in cognitive growth was observed due to TRAPs exposure.


Neuropsychology (journal) | 2014

Continuous Performance Test II Outcomes in 11-Year-Old Children With Early ADHD Symptoms: A Longitudinal Study

Mónica López-Vicente; Jordi Sunyer; Joan Forns; Maties Torrent; Jordi Julvez

OBJECTIVE This study aimed to assess the association between attention-deficit hyperactivity disorder (ADHD) symptoms at preschool age and attention functioning at 11 years old. METHOD Four-year-old children (n = 422) were assessed using the Diagnostic and Statistical Manual of Mental Disorders (4th ed.; American Psychiatric Association, 1994) ADHD form list for inattention and hyperactivity symptoms. Cognitive development and social behavior were also assessed at this age. The Continuous Performance Test II (CPT-II) was used to assess attention function when the children were 11 years old. RESULTS The presence of inattention symptoms predicted more omission errors (incidence rate ratio [IRR] = 1.07, 95% CI [1.02, 1.12]) and slower hit reaction time (HRT; β = 3.27, 95% CI [0.72, 5.81]) in CPT-II. Both inattention and hyperactivity symptoms predicted greater standard error in the HRT (HRT [SE]) (IRR = 1.02, 95% CI [1.01, 1.03]). The inclusion of social competence and cognitive scores in the multivariate regression models diminished the association with omissions, whereas their inclusion did not change associations with the two HRT outcomes. Stronger associations between inattention symptoms and HRT were observed in the last 2 time-duration blocks of the CPT-II. No associations were found with commissions and detectability. CONCLUSIONS The presence of ADHD symptoms in preschool children was longitudinally associated with a lower performance on the CPT-II. Omission errors seemed to be partly explained by early social and cognitive competences. Slower HRTs showed a direct association with inattention symptoms, particularly in the latest CPT-II blocks. HRT (SE) was strongly related to hyperactivity symptoms.


The Journal of Pediatrics | 2017

Are Early Physical Activity and Sedentary Behaviors Related to Working Memory at 7 and 14 Years of Age

Mónica López-Vicente; Judith Garcia-Aymerich; Jaume Torrent-Pallicer; Joan Forns; Jesús Ibarluzea; Nerea Lertxundi; Llúcia González; Desirée Valera-Gran; Maties Torrent; Payam Dadvand; Martine Vrijheid; Jordi Sunyer

Objective To evaluate the role of extracurricular physical activity and sedentary behavior at preschool and primary school age on working memory at primary school age and adolescence, respectively. Study design This prospective study was based on a birth cohort across 4 Spanish regions. In the 3 younger subcohorts (n = 1093), parents reported lifestyle habits of child at age 4 years of age on a questionnaire, and children performed a computerized working memory task at 7 years of age. In the older subcohort (n = 307), the questionnaire was completed at 6 years of age and working memory was tested at 14 years of age. Adjusted regression models were developed to investigate the associations between lifestyle habits and working memory. Results Low extracurricular physical activity levels at 4 years of age were associated with a nonsignificant 0.95% (95% CI −2.81 to 0.92) reduction of correct responses in the working memory task at age 7 years of age. Low extracurricular physical activity levels at 6 years of age were associated with a 4.22% (95% CI −8.05 to −0.39) reduction of correct responses at age 14 years. Television watching was not associated with working memory. Other sedentary behaviors at 6 year of age were associated with a 5.07% (95% CI −9.68 to −0.46) reduction of correct responses in boys at 14 years of age. Conclusion Low extracurricular physical activity levels at preschool and primary school ages were associated with poorer working memory performance at primary school age and adolescence, respectively. High sedentary behavior levels at primary school age were related negatively to working memory in adolescent boys.

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Jordi Sunyer

Autonomous University of Barcelona

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Joan Forns

Pompeu Fabra University

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Ioar Rivas

Spanish National Research Council

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