Factors associated with body mass index in children and adolescents: An international cross-sectional study

Abstract

Background

The increasing prevalence of overweight and obesity in childhood has implications for their future health. There are many potential contributors to overweight and obesity in childhood. The aim was to investigate the association between postulated risk factors and body mass index (BMI) in children and adolescents.

Methods

Secondary analysis of data from a multi-centre, multi-country, cross-sectional study (ISAAC Phase Three). Parents/guardians of children aged 6–7 years completed a questionnaire about their child’s current height and weight, and the postulated risk factors. Adolescents aged 13–14 years reported their own height and weight and answered questions about the postulated risk factors. A general linear mixed model was used to determine the association between BMI and the postulated risk factors. Imputation was used if there were missing responses for 3 or fewer explanatory variables.

Results

65,721 children (27 centres, 15 countries) and 189,282 adolescents (70 centres, 35 countries) were included in the final analyses. Many statistically significant associations were identified, although for most variables the effect sizes were small. In children birth weight (for each kg increase in birth weight the BMI increased by +0.43 kg/m², p<0.001), television viewing (5+ hours/day +0.33 kg/m² vs. <1 hour/day, p<0.001), fast food (≥3 times/week +0.16 kg/m² vs. never, p<0.001) vigorous physical activity (3+ hours/week 0.071 kg/m² vs. never, p = 0.023) and maternal smoking in the first year of life (+0.13 kg/m², p<0.001) were associated with a higher BMI in the adjusted model. Nut consumption (≥3 times/week -0.11 kg/m² vs. never, p = 0.002) was associated with a lower BMI. Early life exposures (antibiotics, paracetamol and breast feeding) were also associated with BMI. For adolescents statistically significant associations with BMI and were seen with maternal smoking (+0.25 kg/m², p<0.001), television viewing (5+ hours/day +0.23 kg/m² vs. <1 hour/day, p<0.001), fast food (≥3 times/week -0.19 kg/m² vs. never, p<0.001), vigorous physical activity (3+ hours/week 0.047 kg/m² vs. never, p<0.001) and nuts (≥3 times/week -0.22 kg/m² vs. never, p<0.001).

Conclusions

Although several early life exposures were associated with small differences in BMI, most effect sizes were small. Larger effect sizes were seen with current maternal smoking, television viewing (both with higher BMI) and frequent nut consumption (lower BMI) in both children and adolescents, suggesting that current behaviours are more important than early exposures. Although many variables may influence BMI in childhood, the putative factors studied are not of sufficient magnitude to support major public health interventions.

About the Authors:

Edwin A. Mitchell

Roles Conceptualization, Funding acquisition, Methodology, Writing – original draft

* E-mail: [email protected]

Affiliation: Department of Paediatrics: Child and Youth Health, Faculty of Medicine and Health Sciences, The University of Auckland, Auckland, New Zealand

ORCID http://orcid.org/0000-0001-6187-7648

Alistair W. Stewart

Roles Formal analysis, Methodology, Writing – review & editing

Affiliation: School of Population Health, Faculty of Medicine and Health Sciences, The University of Auckland, Auckland, New Zealand

Irene Braithwaite

Roles Methodology, Writing – review & editing

Affiliation: Medical Research Institute of New Zealand, Wellington, New Zealand

ORCID http://orcid.org/0000-0001-5327-3027

Rinki Murphy

Roles Methodology, Writing – review & editing

Affiliation: Department of Medicine, Faculty of Medicine and Health Sciences, The University of Auckland, Auckland, New Zealand

Robert J. Hancox

Roles Methodology, Writing – review & editing

Affiliation: Department of Preventive & Social Medicine, Dunedin School of Medicine, University of Otago, Dunedin, New Zealand

Clare Wall

Roles Methodology, Writing – review & editing

Affiliation: Discipline of Nutrition and Dietetics, Faculty of Medicine and Health Sciences, The University of Auckland, Auckland, New Zealand

Richard Beasley

Roles Methodology, Writing – review & editing

Affiliation: Medical Research Institute of New Zealand, Wellington, New Zealand

the ISAAC Phase Three Study Group

¶The complete membership of the ISAAC Phase Three Study Group can be found in the Acknowledgements

Introduction

The increasing prevalence of overweight and obesity in childhood has major implications for their current and future health [1]. This is not an issue just for high-income countries, but is also recognised as a problem for low and middle income countries [2]. At the simplest level the cause of childhood overweight and obesity is an energy imbalance between calories consumed and calories expended. A number of factors are underlying this including a dietary shift towards increased intake of energy-dense foods that are high in fat and sugars, and decreased physical activity levels due to increasing sedentary behaviour, such as television viewing, changes in transportation, and increasing urbanization [3].

Although there have been many studies of risk factors for overweight and obesity, these have been mainly conducted in high-income countries. Furthermore, most studies have categorised body weight (underweight, normal weight, overweight and obese). However, there is evidence that the whole distribution of body mass index (BMI) is increasing, but with a disproportionate increase at higher BMI levels [4].

We have previously examined in detail the association between BMI and television viewing (5), birth weight [6], breastfeeding [7], fast food [8], antibiotics [(9], paracetamol [10], maternal and paternal smoking [11], vigorous physical activity [12] and food [13] in a large international survey of children and adolescents. The aim of this paper was to investigate the association between all these risk factors and BMI in children and adolescents.

Methods

The methods have been described in detail previously [5]. This study is a secondary analysis of the data from the International Study of Asthma and Allergies (ISAAC) Phase Three study. ISAAC is an international multicentre cross-sectional study investigating the prevalence and risk factors for symptoms of asthma, rhinoconjunctivitis and eczema, and the role of risk factors [14]. Data for ISAAC Phase Three was collected between 2000 and 2003 and involved 6–7 year old children and 13–14 year old adolescents chosen from a random sample of schools in a defined geographic area. The questionnaire was in two parts, the core questionnaire on symptoms of asthma, rhinoconjunctivitis and eczema, and an additional questionnaire regarding putative risk factors for asthma. The risk factor questionnaire was optional and many centres chose to administer only the core questionnaire. Questionnaires were translated into the local language and back translated to ensure accuracy [15].

The children’s questionnaires were completed by their parents. Adolescents completed the questionnaires themselves. As adolescents were unlikely to know the answer of the early life exposures, a more limited number of questions were asked of this age group.

Outcome measure

Height and weight were reported by parents of the children and were self-reported by the adolescents. In some centres height and weight were measured objectively (20% of children and 23% of adolescents), although there were no standardised instructions for this. BMI was calculated (weight (kg)/height (m)²).

Explanatory variables

In both age groups the following questions were asked: paracetamol (acetaminophen) use in the last year (yes/no), television viewing (less than 1 hour, 1 hour but less than 3 hours, 3 hours but less than 5 hours and 5 hours or more per day), vigorous exercise (categorised as never or occasionally, once or twice per week, three or more times a week), current maternal smoking (yes/no), current paternal smoking (yes/no) and the following food items in the last year: fast food, vegetables, fruit, pulses and nuts (categorised as never or occasionally, once or twice per week, three or more times a week).

The following questions were asked only of the parents of the children: birth weight as a continuous measure (kg), antibiotics in first year of life (yes/no), paracetamol (acetaminophen) in the first year of life (yes/no), maternal smoking in the first year of life (yes/no) and breastfed (yes/no). The supplementary table (S1 Table) gives the wording of the questions.

Data cleaning

To eliminate likely erroneous BMI data while preserving as much data as possible, we applied the following methods:

* For children in each centre, those in the top and bottom 0.5% of weights and heights (n = 1,391), and those with heights less than 1.0 metre were excluded (n = 346). Children with BMI less than 9 kg/m² or greater than 40 kg/ m² were excluded (n = 215).

* For adolescents in each centre, those in the top and bottom 0.5% of weights and heights (n = 3,712), and those with heights less than 1.25 m were excluded (n = 904). Adolescents with BMI less than 10 kg/ m² or greater than 45 kg/ m² were excluded (n = 360).

Statistical analyses

BMI was assessed separately for each age group using a general linear mixed model with centre as a random effect and gross national income (GNI) for each country, the individual’s age, sex and measurement type (reported/measured) and each of the explanatory variable separately (referred to as univariable analyses). To this model all the explanatory variables were added (referred to as multivariable analysis). SAS (v9.3, SAS Institute, Cary, NC, USA) was used. Imputation was used if there were missing responses for 3 or fewer explanatory variables. Adjustment for multiple testing was not made as each of the variables examined were associated with BMI in the literature or within this dataset when examined individually [5–13].

Results

Following sequential application of the exclusion and data cleaning criteria described above, 65721 children (27 centres/15 countries) and 189282 adolescents (70 centres/35 countries) were included in the final analysis (Fig 1—children and Fig 2—adolescents). In the adolescent age group two variables (current paternal smoking and pulses) were excluded from the analysis due to missing data (14.5% and 8.1% respectively).

[Figure omitted. See PDF.]

Fig 1. Flow of participants through the study.

Children (6–7 years of age).

https://doi.org/10.1371/journal.pone.0196221.g001

[Figure omitted. See PDF.]

Fig 2. Flow of participants through the study.

Adolescents (13–14 years of age).

https://doi.org/10.1371/journal.pone.0196221.g002

The mean height and weight of children was 122.3 cm and 24.1 kg, and for adolescents 159.7 cm and 50.5 kg. The mean BMI was 16.1 kg/m² and 19.8 kg/m² respectively.

Table 1 shows the difference in BMI (kg/m²) between children and adolescents not exposed to the postulated risk factor and those exposed to that risk factor. The findings of the univariable and multivariable analyses are similar. Of the 15 explanatory variables in the model for children, for only one variable (nuts) did the p-value change from non-significance (p = 0.077) in the univariable model to significant in the multivariable model (p = 0.002). Of the 8 explanatory variables in the model for adolescents one variable (fruit) changed from significant (p<0.001) in the univariable model to marginal significance in the multivariable model (p = 0.052).

[Figure omitted. See PDF.]

Table 1. Association between BMI (+/- kg/m², (SE) and p = value) and explanatory variables for children (6–7 years) and adolescents (13–14 years).

https://doi.org/10.1371/journal.pone.0196221.t001

This analysis identified many statistically significant associations, although for most the effect sizes were small. In children the major risk factor for greater BMI was birth weight. For each additional kg in birth weight the BMI was 0.43 kg/m² higher (p<0.001). The next major risk factor was television viewing (5+ hours/day vs. <1 hour/day, 0.33 kg/m², p<0.001). Fast food (≥3 times/week + vs. never) and maternal smoking in the first year of life (yes vs. no) increased BMI by 0.16 kg/m² and 0.13 kg/m² respectively. Paracetamol in the last year (> = 1/month vs. never) and eating nuts (≥3 times/week vs. never) were associated with a lower BMI (-0.11 kg/m² and -0.11 kg/m²). Other factors which were significantly associated with BMI but the effect size was <0.1 kg/m² were breastfeeding (-0.08 kg/m²), antibiotics in the first year of life (0.05 kg/m²), paracetamol in the first year of life (0.05 kg/m²), vigorous exercise (0.07 kg/m²), current maternal smoking (0.08 kg/m²) and current paternal smoking (0.09 kg/m²). Eating vegetables, fruit and pulses (≥3 times/week vs. never) were not associated with BMI.

For adolescents statistically significant associations with BMI were seen with television viewing (5+ hours/day vs. <1 hour/day, 0.23 kg/m², p<0.001), maternal smoking (+0.25 kg/m², p<0.001), fast food (≥3 times/week vs. never, -0.19 kg/m², p<0.001), nuts (≥3 times/week vs. never, -0.22 kg/m², p<0.001), paracetamol in the last year (0.06 kg/m²) and vigorous exercise (0.05 kg/m²). Eating vegetables (≥3 times/week vs. never) was not associated with BMI. Eating fruit (≥3 times/week vs. never) was marginally associated with BMI (-0.07 kg/m²; p = 0.052).

In both age groups television viewing (Fig 3A) and frequent consumption of nuts (Fig 3C) showed a dose effect. Paracetamol in the last year (Fig 3B) and vigorous exercise (Fig 3D) showed a dose effect in children but not in adolescents. Fast food (Fig 4) showed a dose effect but in a different direction for the two age groups.

[Figure omitted. See PDF.]

Fig 3. Graphical representation of change in BMI with television viewing (3A), paracetamol in the last year (3B), nuts (3C), and vigorous exercise (3D) in children (6–7 years of age) and adolescents (13–14 years of age).

https://doi.org/10.1371/journal.pone.0196221.g003

[Figure omitted. See PDF.]

Fig 4. Graphical representation of change in BMI with fast food in children (6–7 years of age) and adolescents (13–14 years of age).

https://doi.org/10.1371/journal.pone.0196221.g004

Discussion

In this secondary analysis of a very large dataset (65,721 children and 189,282 adolescents) we examined 15 and 8 putative risk factors for BMI in children and adolescents respectively. Despite finding many statistically significant associations with BMI, the effect sizes were small with many less than 0.1 kg/m², which equates to a change of less than 0.15 kg body weight for children and 0.26 kg for adolescents who are at the mean height and weight in this study population.

In children the major risk factors for a higher BMI were birth weight, television viewing, maternal smoking in the first year of and eating fast food. Eating nuts was associated with a lower BMI. Because the questionnaire was self-completed, fewer questions were asked of adolescents as they were unlikely to know the answers relating to exposures in early life. In adolescents the major risk factors for a higher BMI were current maternal smoking and television viewing. Eating nuts was also associated with a lower BMI. Unexpectedly, eating fast food in this age group was associated with a lower BMI.

Caution needs to be applied when interpreting the results as the cross sectional design of this study does not allow determination of causality. In general there was a consistency in the findings between children and adolescents. In both age groups there was a positive association between television viewing and BMI and there was evidence that the more television was watched the higher the BMI. This provides support for a causal inference, but it remains possible that television viewing is simply a marker for other lifestyle factors, such as diet, lack of physical activity and socioeconomic factors, although we did adjust for vigorous physical activity and to a more limited extent diet. Our findings are consistent with other cross sectional [16] and longitudinal studies [17]. In addition the findings are consistent with a randomised controlled trial where an intervention designed to reduce children’s television viewing resulted in a significant reduction in BMI compared with the control group [18].

In both age groups parental smoking was associated with higher BMI values, which is consistent with the literature [19, 20]. Maternal smoking in the first year of life and current maternal smoking were both risk factors for higher BMI in children, but is not clear which age of exposure is more important because smoking at one time period is likely to be strongly associated with smoking at other time periods. Furthermore, it is unclear whether in utero tobacco smoke exposure, which was not measured in this study, has a direct effect [21] or whether the association is due to confounding due to differences in diet or other unhealthy lifestyles [22].

Surprisingly we found that vigorous physical activity in both age groups was positively associated with BMI, although the effect size was small and a dose effect was not consistent. Another study of 136,000 youths found that in 29 of 33 participating countries greater physical activity participation was associated with a lower risk of being overweight [23]. Why our study found the opposite association is not clear, however an increase in BMI due to muscle gain from exercise might explain provide an explanation. Alternatively this could be a result of reverse causation, where children and adolescents are exercising more due to their elevated BMI or due to a reporting bias with greater recall of exercise among those with a higher BMI.

In both age groups eating nuts were associated with a lower BMI, and there was a dose effect. Nuts contain high levels of fats and protein and thus are high energy density foods [24] and have sometimes been considered to be unhealthy but recent evidence suggests nut intake has been associated with the reduction of risk factors for chronic diseases [25]. However, our finding is not consistent with a meta-analysis of 33 clinical trials which found that diets enriched with nuts compared with control diets did not increase or decrease BMI or waist circumference [26].

There were two instances when the findings in children and adolescents were in the opposite direction. In children eating fast food was positively associated with BMI, but in adolescents was negatively associated with BMI. The positive association in children was expected and is consistent with other studies [27]. However the adolescent findings were unexpected. As adolescents reported their own eating behaviours they may have under reported fast food intake, particularly if they were overweight. Alternatively those that are overweight or obese may avoid fast food as a strategy for weight management.

Paracetamol use in the last year in children was associated with a reduced BMI but an inconsistent pattern in adolescents. Given that the association of paracetamol use with BMI differs by GNI [10], this is likely to reflect confounding by indication rather than any direct effect of paracetamol on BMI.

We have previously shown that there was a positive linear relationship between birth weight and BMI in children. There was no evidence of a J- or U-shaped association. Although the magnitude of the association of birth weight and BMI was the largest of any variable studied (0.43 mg/kg² change for each kg of birth weight), this does not lead to a public health intervention because lower birth weights have other undesirable consequences. Nevertheless, it is important to understand the influence of in utero growth on the risk for childhood overweight/obesity.

There were a number of other statistically significant associations but the effect sizes were small. Among these was breastfeeding, which was associated with a small trend to lower BMIs. This small and clinically insignificant effect size contrasts with the emphasis that some authorities have given to breastfeeding as one of the key measures to prevent childhood obesity [28]. Our findings support other research that suggests that this emphasis is misplaced [29, 30].

The negative findings are also important. Many dietary guidelines from around the world recommend increased intakes of fruits and non-starchy vegetables as they are associated with a reduced risk of cardiovascular disease and cancer. However the evidence that they reduce obesity is not well established, especially in children and adolescents [31, 32]. Despite this, interventions to prevent or treat obesity often include the recommendation to increase fruit and vegetable intake in the hope that they will replace energy-dense foods. In our study the intake of vegetables, fruit and pulses were not associated with BMI.

It was noticeable that the multivariable results were similar to the univariable findings. This suggests that the risk factors examined were independent of each other.

Strengths of the study include the large number of participants (65,721 children and 189,282 adolescents) and that the participating centres were from countries with differing socioeconomic development, thus enabling the results to be generalised. The weakness of this study is that height and weight were reported by the parents/guardians for children and self-reported for the adolescents. In some centres height and weight were measured, but there was no standard protocol for doing this. Self-reported height and weight might introduce measurement error, and this would decrease the likelihood of finding and association. Ideally body composition would have been measured, but this was not feasible given the size of the study and inclusion of centres from low-middle income countries, many of whom had not undertaken such surveys previously. Lack of measurement precision is recognised and might influence the results towards the null. Furthermore, the exposure questions were not validated. As this was a secondary analysis of data that had already been collected this was not possible. However, it should be noted that the original ISAAC study was designed as a simple questionnaire that could be conducted in centres/countries that were resource poor and had limited research experience. Validation in such a setting would be impractical. A further limitation was that 7% of participants had missing height or weight. These data are may not be missing randomly, for example, overweight adolescents might decline to answer the weight question.

This study has shown that increasing birthweight and early life exposures, such as breastfeeding, antibiotic and paracetamol exposure were associated with higher BMI values. This provides some support for the programming hypothesis in fetal and early life where persisting changes in the body structure and function are caused by environmental stimuli [33]. Associations were also observed with current maternal smoking, television viewing and frequent nut consumption (reduced BMI) in both children and adolescents, suggesting that current behaviours are also important determinants of BMI. While each of these variables may influence BMI, they are not of sufficient magnitude to support major public health interventions. However, we recognise that establishing healthy behaviours in childhood may be important for later life.

Supporting information

[Figure omitted. See PDF.]

S1 Table. Wording of the questions.

https://doi.org/10.1371/journal.pone.0196221.s001

(DOCX)

Acknowledgments

ISAAC Steering Committee: N Aït-Khaled* (International Union Against Tuberculosis and Lung Diseases, Paris, France); HR Anderson (Division of Community Health Sciences, St Georges, University of London, London, UK); MI Asher (Department of Paediatrics: Child and Youth Health, Faculty of Medical and Health Sciences, The University of Auckland, New Zealand); R Beasley* (Medical Research Institute of New Zealand, Wellington, New Zealand); B Björkstén* (Institute of Environmental Medicine, Karolinska Institutet, Stockholm, Sweden); B Brunekreef (Institute of Risk Assessment Science, Universiteit Utrecht, Netherlands); J Crane (Wellington Asthma Research Group, Wellington School of Medicine, New Zealand); P Ellwood (Department of Paediatrics: Child and Youth Health, Faculty of Medical and Health Sciences, The University of Auckland, New Zealand); C Flohr (Department of Paediatric Allergy and Dermatology, St Johns Institute of dermatology, St Thomas’ Hospital, London, UK); S Foliaki* (Centre for Public Health Research, Massey University, Wellington, New Zealand); F Forastiere (Department of Epidemiology, Local Health authority Rome, Italy); L García-Marcos (Respiratory Medicine and Allergy Units, ‘Virgen de la Arrixaca’ University Children’s Hospital, University of Murcia, Spain); U Keil* (Institut für Epidemiologie und Sozialmedizin, Universität Münster, Germany); CKW Lai* (Department of Medicine and Therapeutics, The Chinese University of Hong Kong, SAR China); J Mallol* (Department of Paediatric Respiratory Medicine, University of Santiago de Chile, Chile); EA Mitchell (Department of Paediatrics: Child and Youth Health, Faculty of Medical and Health Sciences, The University of Auckland, New Zealand); S Montefort* (Department of Medicine, University of Malta, Malta), J Odhiambo† (Centre Respiratory Diseases Research Unit, Kenya Medical Research Institute, Nairobi, Kenya); N Pearce (Department of Medical Statistics, Faculty Epidemiology and Public Health, London School of Hygiene and Tropical Medicine, London, UK); CF Robertson (Murdoch Children’s Research Institute, Melbourne, Australia); AW Stewart (Population Health, Faculty of Medical and Health Sciences, The University of Auckland, New Zealand); D Strachan (Division of Community Health Sciences, St Georges, University of London, London, UK); E von Mutius (Dr von Haunerschen Kinderklinik de Universität München, Germany); SK Weiland† (Institute of Epidemiology, University of Ulm, Germany); G Weinmayr (Institute of Epidemiology and Medical Biometry, University of Ulm, Germany); H Williams (Centre for Evidence Based Dermatology, Queen’s Medical Centre, University Hospital, Nottingham, UK); G Wong (Department of Paediatrics, Prince of Wales Hospital, Hong Kong, SAR China).

* Regional Coordinators; †Deceased

ISAAC International Data Centre: MI Asher, TO Clayton†, E Ellwood, P Ellwood, EA Mitchell, Department of Paediatrics: Child and Youth Health, and AW Stewart, School of Population Health, Faculty of Medical and Health Sciences, The University of Auckland, New Zealand.

†Deceased

ISAAC Principal Investigators: Argentina: Dr M Gómez, Ayre Foundation; Hospital San Bernardo (Salta); Belgium: Professor J Weyler, University of Antwerp (Antwerp); Bolivia: Dra R Pinto-Vargas*, Caja Petrolera de Salud (Santa Cruz); Brasil: Professor AJLA Cunha, Federal Universtity of Rio de Janeiro (Nova Iguaçu), Associate Professor L de Freitas Souza, Universidade Federal da Bahia (Vitória da Conquista); Canada: Professor A Ferguson, University of British Columbia (Vancouver); Chile: Dr P Aguilar, Hospital CRS El Pino (South Santiago), Dr L Amarales, Regional Hospital "Lautaro Navarro" (Punta Arenas), Dr LAV Benavides, (Calama), Dra A Contreras, Hospital de Castro (Chiloe); China: Professor Y-Z Chen*, Training Hospital for Peking University (Beijing, Tong Zhou), Assistant Professor O Kunii, University of Tokyo (Tibet), Dr Q Li Pan, Xinjiang Children’s Hospital (Wulumuqi); Professor NS Zhong, Guangzhou Institute of Respiratory Disease (Guangzhou); Colombia: Dr AM Cepeda, Universidad Metropolitana (Barranquilla); Cote d’Ivoire: Dr BN Koffi*, (Urban Cote d Ivoire); Ecuador: Dr C Bustos, Hospital Alcivar (Guayaquil); Estonia: Dr M-A Riikjärv*, Tallinn Children’s Hospital (Tallinn); Fiji: Dr R Sa’aga-Banuve, UNICEF (Suva); Finland: Dr J Pekkanen*, National Public Health Institute (Kuopio County); Former Yugoslav Republic of Macedonia (FYROM): Associate Professor E Vlaski*, University Children’s Clinic (Skopje); Hungary: Dr G Zsigmond*, Senior Consultant (Svábhegy); India: Dr SN Mantri, Jaslok Hospital & Research Centre (Mumbai (29)), Professor SK Sharma, All India Institute of Medical Sciences (New Delhi (7)); Indonesia: Prof Dr CB Kartasasmita, Padjajaran University (Bandung), Professor P Konthen†, Airlangga University (Bali), Dr W Suprihati, Diponegoro University (Semarang); Iran: Dr M-R Masjedi*, National Research Institute of Tuberculosis and Lung Diseases (Rasht, Tehran); Japan: Dr H Odajima, National Hospital Organization Fukuoka Hospital (Fukuoka); Lithuania: Associate Professor J Kudzyte*, Kaunas Medical University (Kaunas); Mexico: Dra M Barragán-Meijueiro, CoMAAIPE (Ciudad de México (3)), Dra BE Del-Río-Navarro, Hospital Infantil de México (Ciudad de México (1)), Dr FJ Linares-Zapién, Centro De Enfermedades Alergicas Y Asma de Toluca (Toluca), Dra N Ramírez-Chanona, COMPEDIA (Ciudad de México (4)), Dr S Romero-Tapia, Hospital de Alta Especialidad del Niño (Villahermosa); Morocco: Professor Z Bouayad*, Service des Maladies Respiratoires (Boulmene, Casablanca, Marrakech); New Zealand: Dr R MacKay, Canterbury Health Laboratories (Nelson), Dr C Moyes, Whakatane Hospital (Bay of Plenty), Associate Professor P Pattemore, University of Otago, Christchurch (Christchurch); Nigeria: Professor BO Onadeko, (Ibadan); Peru: Dr P Chiarella*, Universidad Peruana de Ciencias Aplicadas, UPC (Lima); Poland: Associate Professor A Brêborowicz, University of Medical Sciences (Poznan), Associate Professor G Lis*, Jagiellonian University (Kraków); Portugal: Dra R Câmara, Centro Hospitilar do Funchal (Funchal), Dr JM Lopes dos Santos, Hospital Pedro Hispano (Porto), Dr C Nunes, Center of Allergy and Immunology of Algarve (Portimao), Dr J Rosado Pinto*, Hospital da Luz (Lisbon); Singapore: Associate Professor DY Goh, National University of Singapore (Singapore); South Africa: Professor HJ Zar*, University of Cape Town (Cape Town); South Korea: Professor H-B Lee*, Hanyang University College of Medicine (Provincial Korea, Seoul); Spain: Professor A Blanco-Quirós, Facultad de Medicina (Valladolid), Dr RM Busquets, Universidad Autonoma de Barcelona (Barcelona), Dr I Carvajal-Urueña, Centro de Salud de La Ería (Asturias), Dr G García-Hernández, Hospital Universitario 12 de Octubre (Madrid), Professor L García-Marcos*, University of Murcia and IMIB-Arrxaca Research Institute (Cartagena), Dr C González Díaz, Universidad del País Vasco UPV /EHU (Bilbao), Dr A López-Silvarrey Varela, Fundacion Maria Jose Jove (A Coruña), Professor M Morales-Suárez-Varela, Valencia University-CIBERESP (Valencia), Professor EG Pérez-Yarza, Universidad del Pais Vasco UPV/EHU (San Sebastián); Sultanate Of Oman: Professor O Al-Rawas*, Sultan Qaboos University (Al-Khodh); Syrian Arab Republic: Dr S Mohammad*, Tishreen University (Tartous), Professor Y Mohammad, National Center for Research and Training in Chronic Respiratory Diseases—Tishreen University (Lattakia), Dr K Tabbah, Aleppo University Hospital (Aleppo); Taiwan: Dr J-L Huang*, Chang Gung University (Taipei), Dr C-C Kao, Kao-Chun-Chieh Clinic (Taoyuan); Thailand: Associate Professor M Trakultivakorn, Chiang Mai University (Chiang Mai), Dr P Vichyanond*, Mahidol University (Bangkok); Usa: Dr HH Windom, Asthma and Allergy Research Center (Sarasota); Uruguay: Dra D Holgado*, Hospital Pereira Rossell (Montevideo), Dra MC Lapides, Hospital Paysandú (Paysandú).

* National Coordinator; †Deceased

ISAAC Phase Three National Coordinators not identified above: Brazil: Professor D Solé, Universidade Federal de São Paulo; Canada: Professor MR Sears, McMaster University; Chile: Dra V Aguirre, Hospital CRS El Pino; Fiji: Dr L Waqatakirewa, Children’s Hospital; India: Dr J Shah, Jaslok Hospital & Research Centre; Indonesia: Prof Dr K Baratawidjaja, University of Indonesia; Japan: Professor S Nishima, The National Minami-Fukuoka Chest Hospital; Mexico: Dr M Baeza-Bacab, University Autónoma de Yucatán; New Zealand: Professor MI Asher, University of Auckland; Singapore: Professor B-W Lee, National University of Singapore;

Citation: Mitchell EA, Stewart AW, Braithwaite I, Murphy R, Hancox RJ, Wall C, et al. (2018) Factors associated with body mass index in children and adolescents: An international cross-sectional study. PLoS ONE 13(5): e0196221. https://doi.org/10.1371/journal.pone.0196221

References

1. Franks PW, Hanson RL, Knowler WC, Sievers ML, Bennett PH, Looker HC. Childhood obesity, other cardiovascular risk factors, and premature death. N Engl J Med. 2010;362:485–493. pmid:20147714

2. World Health Organisation. Global status report on noncommunicable diseases 2014. http://apps.who.int/iris/bitstream/10665/148114/1/9789241564854_eng.pdf (accessed 11 July 2017).

3. Popkin BM, Adair LS, Ng SW. Global nutrition transition and the pandemic of obesity in developing countries. Nutr Rev. 2012;70(1): 3–21. pmid:22221213

4. Flegal KM, Troiano RP. Changes in the distribution of body mass index of adults and children in the US population. Int J Obes Relat Metab Disord. 2000;24(7):807–818. pmid:10918526

5. Braithwaite I, Stewart AW, Hancox RJ, Beasley R, Murphy R, Mitchell EA, the ISAAC Phase Three Study Group. The worldwide association between television viewing and obesity in children and adolescents: cross sectional study. PLoS ONE 2013; 8(9): e74263. pmid:24086327

6. Mitchell EA, Stewart AW, Braithwaite I, Hancox RJ, Murphy R, Wall C, et al. Birth weight and subsequent body mass index in children: an international cross-sectional study. Pediatric Obesity 2016; 1–6.

7. Hancox RJ, Stewart AW, Braithwaite I, Beasley R, Murphy R, Mitchell EA, the ISAAC Phase Three Study Group. Association between breastfeeding and childhood Body Mass Index in an international survey. Pediatric Obesity 2015; 10: 283–7. pmid:25291239

8. Braithwaite I, Stewart AW, Hancox RJ, Beasley R, Murphy R, Mitchell EA, the ISAAC Phase Three Study Group. Fast Food consumption and Body Mass Index in children and adolescents: an international cross-sectional study. BMJ Open 2014; 4:e005813. pmid:25488096

9. Murphy R, Stewart A, Braithwaite I, Beasley R, Hancox R, Mitchell E, the ISAAC Phase Three Study Group. Antibiotic treatment during infancy and increased body mass index in boys: an international cross-sectional study. Int J Obesity 2014;38:1115–1119.

10. Murphy R, Stewart AW, Braithwaite I, Beasley R, Hancox RJ, Mitchell EA. Association of paracetamol use in infancy and childhood on body mass index. Obesity 2015;23(5):1030–8 pmid:25864407

11. Braithwaite I, Stewart AW, Hancox RJ, Beasley R, Murphy R, Mitchell EA, the ISAAC Phase Three Study Group. The worldwide association between parental tobacco use and Body Mass Index in children and adolescents. BMC Pediatrics. 2015; 15: 200.

12. Braithwaite I, Stewart AW, Hancox RJ, Murphy R, Wall C, Beasley R, et al. The association between Body Mass Index and reported vigorous physical activity in children and adolescents: an international cross-sectional study. Acta Paediatrica. 2017;106:1323–1330.

13. Wall C, Stewart AW, Hancox R, Murphy R, Braithwaite I, Beasley R, et al. Association between frequency of consumption of fruit, vegetables, nuts and pulses and BMI: analyses of the International Study of Asthma and Allergies in Childhood (ISAAC). Nutrients. 2018, 10, 316; pmid:29518923

14. Ellwood P, Asher MI, Beasley R, Clayton TO, Stewart AW, ISAAC Steering Committee. The international study of asthma and allergies in childhood (ISAAC): phase three rationale and methods. Int J Tuberc Lung Dis 2005;9(1): 10–6. pmid:15675544

15. Ellwood P, Williams H, Ait-Khaled N, Bjorksten B, Robertson C, ISAAC Phase III Study Group. The impact of the method of consent on response rates in the ISAAC time trends study. Int J Tuberc Lung Dis. 2010;14(8):1059–65. pmid:20626953

16. Marshall SJ, Biddle SJH, Gorely T, Cameron N, Murdey I. Relationships between media use, body fatness and physical activity in children and youth: a meta-analysis. Int J Obesity. 2004;28:1238–1246. pmid:15314635

17. Hancox RG, Poulton R. Watching television is associated with childhood obesity: but is it clinically important? Int J Obesity. 2006;30:171–175. pmid:16158085

18. Robinson TN. Reducing Children’s Television Viewing to Prevent Obesity: A Randomized Controlled Trial. JAMA. 1999;282(16):1561–1567. pmid:10546696

19. Oken E, Levitan EB, Gillman MW. Maternal smoking during pregnancy and child overweight: systematic review and meta-analysis. Int J Obes (Lond). 2008;32:201–210

20. Ino T. Maternal smoking during pregnancy and offspring obesity: Meta-analysis. Pediatrics International. 2010;52:94–99. pmid:19400912

21. Al Mamun A, Lawlor DA, Alati R, Callaghan JO, Williams GM, Najman JM. Does maternal smoking during pregnancy have direct effect on future offspring obesity? Evidence from a prospective cohort study. Am J Epidemiol. 2006;164:317–325. pmid:16775040

22. Florath I, Kohler M, Weck MN, Brandt S, Rothenbacher D, Schöttker B, et al. Association of pre- and post-natal parental smoking with offspring body mass index: an 8-year follow-up of a birth cohort. Pediatr Obesity. 2014;9:121–134. pmid:23420701

23. Janssen I, Katzmarzyk PT, Boyce WF, Vereecken C, Mulvihill C, Roberts C, et al. Comparison of overweight and obesity prevalence in school-aged youth from 34 countries and their relationships with physical activity and dietary patterns. Obes Rev. 2005;6:123–32 pmid:15836463

24. Ros E, Mataix J. Fatty acid composition of nuts–implications for cardiovascular health. Br J Nutr. 2006;96(suppl 2):S29–35.

25. Ibarrola-Jurado N, Bulló M, Guasch-Ferré M, Ros E, Martínez-González MA, Corella D, et al. Cross-sectional assessment of nut consumption and obesity, metabolic syndrome and other cardiometabolic risk factors: The PREDIMED Study. PLoS One. 2013;8:e57367. pmid:23460844

26. Flores-Mateo G, Rojas-Rueda D, Basora J, Ros E, Salas-Salvadó J. Nut intake and adiposity: meta-analysis of clinical trials. Am J Clin Nutr. 2013;97(6):1346–55. pmid:23595878

27. Bhat VN. Fast Food Consumption and Body Mass Index. J Social Sci. 2016;12:129–135.

28. White House Task Force on Childhood Obesity Report to the President. Solving the problem of childhood obesity within a generation. 2010. https://letsmove.obamawhitehouse.archives.gov/sites/letsmove.gov/files/TaskForce_on_Childhood_Obesity_May2010_FullReport.pdf (accessed 20/07/2017)

29. Casazza K, Fontaine KR, Astrup A, Birch LL, Brown AW, Bohan Brown MM et al. Myths, Presumptions, and Facts about Obesity. N Engl J Med. 2013;368:446–454. pmid:23363498

30. Kramer MS, Matush L, Vanilovich I, Platt RW, Bogdanovich N, Sevkovskaya Z et al. Effects of prolonged and exclusive breastfeeding on child height, weight, adiposity, and blood pressure at age 6.5 y: evidence from a large randomized trial. Am J Clin Nutr. 2007;86:1717–1721. pmid:18065591

31. Sahota P, Rudolf MC, Dixey R, Hill AJ, Barth JH, Cade J. Randomised controlled trial of primary school based intervention to reduce risk factors for obesity. BMJ. 2001;323:1029–1032. pmid:11691759

32. Field AE, Gillman MW, Rosner B, Rockett HR, Colditz GA. Association between fruit and vegetable intake and change in body mass index among a large sample of children and adolescents in the United States. Int J Obes Relat Metab Disord. 2003:27(7):821–6. pmid:12821968

33. Gillman MW. Developmental origins of health and disease. N Engl J Med. 2005;353(17):1848–50. pmid:16251542