The burden of asthma, hay fever and eczema in children in 25 countries: GAN Phase I study

Discussion

Although with considerable variations at centre, country and GNI levels, the overall global burden of asthma, rhinoconjunctivitis and eczema remains substantial, with ∼10% of adolescents and children experiencing asthma ever, 15% of adolescents and 11% of children having hay fever ever, and 11% of adolescents and 13% of children having eczema ever. Even though the degree of asthma control is relatively high regardless of income levels, asthma control seems to be a substantial problem across the globe.

The trend found in ISAAC of English-speaking countries and Latin-American countries having relatively higher prevalence of asthma [5, 17, 22, 23] was difficult to ascertain in this study because the number of centres in English-speaking countries was low. As in ISAAC Phase III [5, 24], there was a clear trend of asthma symptoms and severity running in parallel in both age groups. For the complete picture of time trends of asthma symptoms, see the recently published paper by Asher et al. [7].

Prevalence of asthma indicators was lower in the group of LICs/LMICs in both age groups, although this may have been driven by Indian centres, which tended to have the lowest prevalence, consistent with previous ISAAC surveys [5, 17]. Usually in LICs/LMICs, hygiene conditions are poorer and contact with farm animals more frequent, thus individuals are probably more exposed to higher amounts and a greater diversity of bacteria, which is a protective factor for atopy and asthma [25, 26].

Consistent with asthma prevalence is the lower prevalence of rhinoconjunctivitis and severe rhinoconjunctivitis symptoms in LICs/LMICs in both age groups. This was not the case with hay fever ever and might indicate that this concept is more familiar in temperate climates than in tropical countries, including many of the LIC and LMICs in GAN. In contrast to the asthma patterns, India did not seem to be wholly responsible for the low prevalence because the other two countries in this GNI category show similar disease prevalence. To what extent rhinoconjunctivitis is a marker of the atopic condition, which may be lower in less westernised countries, cannot be said but deserves some consideration [27]. The fact that hay fever does not follow the same pattern across countries and does not correlate well with rhinoconjunctivitis symptoms at the centre level may reflect genuine differences in prevalence, but may also be due to diverse diagnostic criteria [28].

The prevalence of eczema indicators was also variable, but substantially higher in high income countries (HICs). A higher prevalence of atopy in HICs might explain this distribution [27]. Furthermore, the different prevalence of non-atopic skin diseases, such as those caused by fungi [29], in the different GNI groups makes the epidemiological context of the diagnosis of eczema diverse.

Prevalence variability attributable to centre accounted for some proportion of the total variability in all three conditions. Risk or protective factors, or even interpretation of questions at the centre and individual level, are probably shared more by centres in the same countries than by centres in different countries. This could explain why the pattern of variability found for all three conditions was lower within than between countries.

The higher prevalence of asthma and rhinoconjunctivitis in male children was reversed in adolescents, a finding that was previously shown in ISAAC and other studies [17, 23, 30]. The reason for this change is not clear although hormonal influences have been suggested [31, 32]. With respect to eczema symptoms, previous ISAAC surveys [12, 33] showed that they were more prevalent in girls than in boys in both age groups although this was strongest in adolescents. We only found a difference among adolescents. This higher prevalence in female adolescents has also been found in prospective cohorts [34] and might again be related to oestrogen and progesterone interacting with skin allergies [31]. The lack of difference between sexes in children might be due to the different geographical distribution of centres in GAN and ISAAC [35].

The strengths of the present study are the ample world coverage, the large numbers of new centres and participants, and the use of the identical, standardised and easy to use ISAAC methodology, which allows both robust cross-sectional inferences as well as meaningful comparisons.

The limitations include the diagnosis of any of the three conditions that may not be perfectly well addressed by a self-administered questionnaire, the lack of a specific translation of “wheezing” in many languages and the perception of questions being different between parents and adolescents. All these circumstances may potentially lead to classification bias. However, questions have been previously validated and the translation and back-translation method of ISAAC and GAN has yielded good results [15].

Incorrect labelling is of special interest in hay fever and eczema: if the proportion of severe symptoms without a diagnosis indicates real and current conditions, their burden would be even higher. When estimating the burden of those diseases globally it might be more appropriate to use severe symptoms than diagnostic labels.

Although the perception of questions between adolescents and their parents may not be the same, the present study avoids comparing results between different age groups and focuses on the differences at centre, country or GNI levels within a specific age group. The main limitation of GAN as compared to ISAAC is the lack of representation of many countries. We are lacking centres from Northern Europe, North America and Australia, which in previous studies have shown the highest prevalence of asthma and atopic diseases [5, 11, 12, 23]. Additionally, we have no information about non-participants, although high response rates help to overcome participation bias. Finally, we cannot say what the impact of GNI on the results would have been if more countries were included in all income groups.

In conclusion, the present study, an updated and unique study on the prevalence of indicators of asthma, rhinoconjunctivitis and eczema, shows the persistence of a considerable burden of those conditions among children and adolescents worldwide. The prevalence of indicators of all three diseases was consistently lower in LICs and LMICs. The wide differences in prevalence, which were higher between countries than within countries, could probably be explained by environmental risk (such as pollution) or protective factors (such as contact with bacteria) that are more similar within countries.

Acknowledgements

We are grateful to the children, parents and adults who willingly participated with the help of schools and field workers in GAN Phase I. We thank the children and parents who participated in GAN Phase I, the school staff for their assistance and help with coordination, the principal investigators and their colleagues, and the many funding bodies throughout the world that supported the individual GAN centres. The GAN Global Centre in Auckland was funded by The University of Auckland with additional funding from The International Union Against Tuberculosis and Lung Disease, Boehringer Ingelheim NZ, AstraZeneca Educational Grant. The London Data Centre was supported by a PhD studentship to C.E. Rutter from the UK Medical Research Council (grant number MR/N013638/1) and funding from the European Research Council under the European Union's Seventh Framework Programme (FP7/2007-2013, ERC grant agreement number 668954). The Murcia Data Centre was supported by the University of Murcia and by Instituto de Salud Carlos III, fund PI17/0170. We thank the National Institute for Health Research (NIHR) Global Health Research Unit on Lung Health and TB in Africa at the Liverpool School of Tropical Medicine – “IMPALA” for helping to make this work possible. In relation to IMPALA (grant reference 16/136/35) specifically: IMPALA was funded by the NIHR using UK aid from the UK Government to support global health research. The views expressed in this publication are those of the authors and not necessarily those of the NIHR or the UK Department of Health and Social Care. Individual centres involved in GAN Phase I data collection were funded by the following organisations: Costa Rica and Nicaragua partially funded by an unrestricted grant from AstraZeneca for logistic purposes; India (Kottayam, New Delhi, Chandigarh, Bikaner, Jaipur, Lucknow, Pune): GAN Phase I was undertaken by Asthma Bhawan in India which was supported by Cipla Foundation; Mexico: Puerto Vallarta Centro Universitario de la Costa, Universidad de Guadalajara; New Zealand: Auckland Asthma Charitable Trust; Nigeria, Ibadan: funded by NIHR (IMPALA grant reference 16/136/35) using UK aid from the UK Government to support global health research; South Africa: Cape Town, SA Medical Research Council, Allergy Society of South Africa; Syria, Lattakia: The Medical National Syndicate; Spain: Cartagena, Bilbao, Pamplona funded by Instituto de Salud Carlos III (grants PI17/00179, PI17/00694, PI17/00756), Cantabria by Instituto de Investigación Sanitaria Valdecilla (IDIVAL) de Cantabria PRIMVAL 17/01 y 18/01, Salamanca by Gerencia Regional de Salud de la Junta de Castilla y León (grant GRS 1239b/16) and Sociedad Española de Inmunología Clínica, Alergología y Asma Pediátrica, A Coruña by María José Jove foundation.

Global Asthma Network Study Group. Global Asthma Network Steering Group: M.I. Asher, Department of Paediatrics: Child and Youth Health, Faculty of Medical and Health Sciences, University of Auckland, Auckland, New Zealand; K. Bissell, School of Population Health, Faculty of Medical and Health Sciences, University of Auckland, Auckland, New Zealand; C-Y. Chiang, International Union Against Tuberculosis and Lung Disease, Paris, France, and Division of Pulmonary Medicine, Dept of Internal Medicine, Wan Fang Hospital, Taipei Medical University, and Division of Pulmonary Medicine, Dept of Internal Medicine, School of Medicine, College of Medicine, Taipei Medical University, Taipei, Taiwan; A. El Sony, Epidemiological Laboratory for Public Health and Research, Khartoum, Sudan; E. Ellwood, Department of Paediatrics: Child and Youth Health, Faculty of Medical and Health Sciences, University of Auckland, Auckland, New Zealand; P. Ellwood, Department of Paediatrics: Child and Youth Health, Faculty of Medical and Health Sciences, University of Auckland, Auckland, New Zealand; L. García-Marcos, Pediatric Allergy and Pulmonology Units, Virgen de la Arrixaca University Children's Hospital, University of Murcia and IMIB Bioresearch Institute, Murcia, and ARADyAL Allergy Network, Edificio Departamental-LAIB, Murcia, Spain; G.B. Marks, Respiratory and Environmental Epidemiology, University of New South Wales, Sydney, Australia; R. Masekela, Dept of Paediatrics and Child Health, Nelson R. Mandela School of Clinical Medicine, College of Health Sciences, University of KwaZulu Natal, Durban, South Africa; E. Morales, Department of Public Health Sciences, University of Murcia, and IMIB Bio-health Research Institute, Edificio Departamental-LAIB, Murcia, Spain; K. Mortimer, Liverpool School of Tropical Medicine, Liverpool, UK; N. Pearce, Department of Medical Statistics, London School of Hygiene and Tropical Medicine, London, UK; D.P. Strachan, Population Health Research Institute, St George's, University of London, London, UK.

Global Asthma Network International Data Centres. GAN Global Centre: P. Ellwood, E. Ellwood, M.I. Asher, Department of Paediatrics: Child and Youth Health, Faculty of Medical and Health Sciences, University of Auckland, Auckland, New Zealand. Murcia, Spain: L. García-Marcos, Pediatric Allergy and Pulmonology Units, Virgen de la Arrixaca University Children's Hospital, University of Murcia and IMIB Bioresearch Institute, Murcia, and ARADyAL Allergy Network, Edificio Departamental-LAIB, Murcia, Spain; V. Perez-Fernández, Dept of Paediatrics, University of Murcia, and IMIB Bio-health Research Institute, Edificio Departamental-LAIB, Murcia Spain; E. Morales, Dept of Public Health Sciences, University of Murcia, and IMIB Bio-health Research Institute, Edificio Departamental-LAIB, Murcia, Spain; A. Martinez-Torres, Paediatric Allergy and Pulmonology Units and Nurse Research Group, Virgen de la Arrixaca University Children's Hospital, University of Murcia and IMIB Bio-health Research Institute, Edificio Departamental-LAIB, Murcia, Spain. London, UK: D.P. Strachan, Population Health Research Institute, St George's, University of London, London, UK; N. Pearce, S. Robertson and C.E. Rutter, Dept of Medical Statistics, London School of Hygiene and Tropical Medicine, London, UK; R.J. Silverwood, Dept of Medical Statistics, London School of Hygiene and Tropical Medicine, and Centre for Longitudinal Studies, UCL Social Research Institute, University College London, London, UK.

Global Asthma Network Principal Investigators. Argentina: H. Badellino, Clinica Regional Del Este, San Francisco; Brazil: M. Urrutia-Pereira, Federal University of Pampa, UNIPAMPA, Uruguaiana; Cameroon: A.E. Ndikum, The University of Yaounde 1, Yaounde; Chile: J. Mallol, University of Santiago de Chile (USACH), South Santiago; Costa Rica: M.E. Soto-Martínez, Hospital Nacional de Niños “Dr. Carlos Saénz Herrera”, Caja Costarricense Seguro Social – Universidad de Costa Rica, San José, Costa Rica; Ecuador: A. Cabrera Aguilar, Respiraclinic, Quito; Greece: K. Douros, National and Kapodistrian University of Athens, Athens; Honduras: S.M. Sosa Ferrari, Instituto Nacional Cardiopulmonar, Tegucigalpa; India: S. Mohammad, Kothari Medical and Research Institute, Bikaner; M. Singh, Postgraduate Institute of Medical Education and Research, Chandigarh; V. Singh (national coordinator), Asthma Bhawan, Jaipur; A.G. Ghoshal, National Allergy Asthma Bronchitis Institute, Kolkata; T.U. Sukumaran, Pushpagiri Institute of Medical Sciences and Research, Thiruvalla, Kottayam; S. Awasthi, King George's Medical University, Lucknow; P.A. Mahesh, JSS Medical College, JSSAHER, Mysuru; S.K. Kabra, All India Institute of Medical Sciences, New Delhi (7); S. Salvi, Chest Research Foundation, Pune; Iran: M. Tavakol, Alborz University of Medical Sciences, Karaj; N. Behniafard, Shahid Sadoughi University of Medical Sciences, Yazd; Kingdom of Saudi Arabia: S.A. Alomary, Ministry of Health, Kingdom of Saudi Arabia; Kosovo: I. Bucaliu-Ismajli, The Principal Center of Family Care, Ferizaj; L. Pajaziti, University Hospital Clinic, Clinic of Dermatology, Prishtina; V. Gashi, American Hospital in Kosovo, Gjilan; X. Kurhasani, UBT College Kosovo, Peja 13–14; B. Gacaferri-Lumezi, University of Prishtina Hasan Prishtina, Peja 6–7; L.N. Ahmetaj (national coordinator), University Hospital (Prishtina); V. Zhjeqi, University of Prishtina, Prizren; México: M.G. Sanchez Coronel, COMPEDIA (Colegio Mexicano de Pediatras Especialistas en Inmunología y Alergia), Aguascalientes; H.L. Moreno Gardea, Hospital Angeles Chihuahua, Chihuahua; G. Ochoa-Lopez, Department of Pediatric Allergology, Ciudad Juárez; R. García-Almaráz, Hospital Infantil de Tamaulipas, Ciudad Victoria; J.A. Sacre Hazouri, Instituto Privado de Alergia, Córdoba; N. Rodriguez-Perez, Instituto de Ciencias y Estudios Superiores de Tamaulipas, Matamoros; J.V. Mérida-Palacio, Centro de Investigacion de Enfermedades Alergicas y Respiratorias, Mexicali; B.E. Del Río Navarro (national coordinator), Service of Allergy and Clinical Immunology, Hospital Infantil de México, México City; L.O. Hernández-Mondragón, CRIT de Michoacán, Michoacán; S.N. González-Díaz, Universidad Autónoma de Nuevo León, Monterrey; R. Garcia-Muñoz, Universidad Regional del Sureste, Oaxaca; Md. Juan Pineda, Universidad de Guadalajara, Puerto Vallarta; Bd. Ramos García, Instituto Mexicano del Seguro Social, San Luis Potosí; A.J. Escalante-Dominguez, Hospital General Tijuana, Isesalud, Tijuana; F.J. Linares-Zapién, Centro De Enfermedades Alergicas Y Asma de Toluca, Toluca Rural; E.M. Navarrete-Rodriguez, Hospital Infantil de México Federico Gómez, Toluca Urban Area; J. Santos Lozano, Medica san Angel, Xalapa; New Zealand: I. Asher, University of Auckland, Auckland; Nicaragua: J.F. Sánchez, Hospital Infantil Manuel de Jesús Rivera, Managua; Nigeria: A.G. Falade, University of Ibadan and University College Hospital, Ibadan; Poland: G. Brożek, Medical University of Silesia, Katowice; Russia: K. Kyzmicheva, Tyumen State Medical University, Tyumen; South Africa: H.J. Zar, SA MRC Unit on Child and Adolescent Health, Cape Town; R. Masekela, University of Kwazulu Natal, Durban; Spain: A. López-Silvarrey Varela, Fundacion Maria Jose Jove, A Coruña; C. González Díaz, Universidad del País Vasco UPV/EHU, Bilbao; A. Bercedo Sanz, Cantabrian Health Service, Valdecilla Research Institute (IDIVAL), Dobra Health Center, Torrelavega, Cantabria; L. García-Marcos (national coordinator), Pediatric Allergy and Pulmonology Units, Virgen de la Arrixaca University Children's Hospital, University of Murcia and IMIB Bioresearch Institute, Murcia; J. Pellegrini Belinchon, Universidad de Salamanca, Salamanca; Sri Lanka: J.C. Ranasinghe, Teaching Hospital Peradeniya, Anuradhapura; S.T. Kudagammana, University of Peradeniya, Peradeniya; Sudan: H. El Sadig, Ministry of Health, Gadarif; M. Nour, Epi-Lab, Khartoum; Syrian Arab Republic: G. Alkhayer, Syrian Private University, Damascus; G. Dib and Y. Mohammad (national coordinator), National Center for Research and Training for Chronic Respiratory Disease and Co-Morbidities, Tishreen University, Lattakia; Taiwan: J. Huang, Department of Pediatrics, Chang Gung Memorial Hospital, New Taipei Municipal TuChen Hospital, and Chang Gung University, Taipei; Thailand: S. Chinratanapisit, Department of Pediatrics, Bhumibol Adulyadej Hospital, Royal Thai Air Force, Bangkok. Global Asthma Network National Co-ordinators not named above: Brazil: D. Solé, Escola Paulista de Medicina, Federal University of São Paulo, São Paulo; Costa Rica: M.E. Soto-Quirós, University of Costa Rica; Kingdom of Saudi Arabia: W.A. Althagafi, Ministry of Health, Kingdom of Saudi Arabia; Sudan: A. El Sony, Epidemiological Laboratory (Epi-Lab) for Public Health, Research and Development, Khartoum; Thailand: P. Vichyanond, Mahidol University, Phutthamonthon.

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