You are here

Article Text

Article menu
Original articles
Changing trends in asthma in 9–12 year olds between 1964 and 2009
  1. G Malik1,
  2. N Tagiyeva1,
  3. L Aucott2,
  4. G McNeill3,
  5. S W Turner1
  1. 1Department of Child Health, University of Aberdeen, Aberdeen, UK
  2. 2Department of Public Health, University of Aberdeen, Aberdeen, UK
  3. 3Public Health Nutrition Research Group, University of Aberdeen, Aberdeen, UK
  1. Correspondence to Dr S W Turner, Department of Child Health, School of Medicine, Royal Aberdeen Children's Hospital, Foresterhill, Aberdeen AB25 2ZG, UK; s.w.turner{at}abdn.ac.uk

Abstract

Introduction Childhood asthma is a common condition and the prevalence has increased in many countries during the late 20th century. The Aberdeen schools asthma surveys reported rising lifetime prevalence of asthma between 1964 and 2004 in children aged 9–12 years, but a fall in wheeze in the last 3 years between 1999 and 2004. The present study tested the hypothesis that lifetime childhood asthma prevalence has fallen since 2004.

Methods Children aged 9–12 years who attended the same schools surveyed since 1964 were invited to participate. A lifetime history of asthma or eczema and also wheeze in the past 3 years and 12 months was ascertained from a questionnaire. Trends over 1999, 2004 and 2009 were analysed with adjustment for age, gender and an index of deprivation.

Results There were 2253 eligible children and 1196 (53%) questionnaires were returned. The lifetime prevalence of asthma rose from 24.3% in 1999 to 28.4% in 2004 but fell to 22.1% in 2009 (p<0.001), while wheeze in the last 3 years fell from 27.9% in 1999 to 25.2% in 2004 and fell further to 22.2% in 2009 (p<0.001). The lifetime prevalence of eczema among 9–12 year olds was 21.4% in 1999, 34.1% in 2004 and 30.7% in 2009 (p<0.001). Reductions in symptom prevalences between 2004 and 2009 were significant for girls but not boys.

Conclusion The prevalence of lifetime asthma and wheeze appear to have fallen in school children, especially girls, although the low response rate means some caution is required when interpreting the results. Asthma prevalence remains high and the underlying mechanisms remain incompletely understood.

https://doi.org/10.1136/adc.2010.189175

Statistics from Altmetric.com

    Request Permissions

    If you wish to reuse any or all of this article please use the link below which will take you to the Copyright Clearance Center’s RightsLink service. You will be able to get a quick price and instant permission to reuse the content in many different ways.

    Introduction

    Childhood asthma is a very common chronic condition. In the UK, there are approximately one million children with asthma,1 5% of children are prescribed inhaled corticosteroids to control persistent asthma symptoms2 and approximately three children per million die of asthma each year.3 In many countries, including the UK, the prevalence of childhood asthma rose during the 1980s and 1990s.4,–,7 Although globally there was no obvious pattern to changes in childhood asthma prevalence in the early 2000s,8 recent evidence from some European countries point to a slowing or even a halt in the rise of asthma prevalence among children and adolescents.9,–,11

    The first Aberdeen Schools Asthma Survey was completed in 196412 and subsequently repeated in 198913, 199414, 199915 and 2004.5 We have recently reported that although the lifetime prevalence of asthma in 9–12 year old children rose between 1999 and 2004, wheeze in the last 3 years fell in this period.5 Based on our observations in 1999 and 2004, we speculated that the prevalence of asthma might fall after 20045 and in the present report we test this hypothesis using the data from the 2009 survey.

    What is already known on this topic

    • ▶ Asthma prevalence has increased in the UK between 1964 and 2004.

    • ▶ Evidence of a slowing or reversal of rising asthma prevalence has been seen in countries other than the UK.

    What this study adds

    • ▶ There is evidence that asthma prevalence is now falling in the UK.

    • ▶ The fall in asthma prevalence seems to be greater in girls.

    Methods

    Study design

    Children in primary school aged 5–7 years (approximate ages 9–12 years) were invited to participate. Questionnaires were distributed to children by school staff, completed by parents at home, returned to school and collected by the class teachers prior to collection by the research team. The study was approved by the University of Aberdeen College of Life Sciences and Medicine Ethics Review Board and Aberdeen City Council Education Department. Parental consent was inferred from the return of a completed questionnaire.

    Participants

    Children attending the same schools included in all previous surveys were invited to participate. The survey took place during the month of May, as in all previous surveys. The 1964, 1989 and 1994 surveys included only children aged 9–12 years (primary school years 5–7). The 2004 and 2009 surveys also included children aged 7–9 years (primary school years 3–4) and International Study of Allergy and Asthma in Children (ISAAC) respiratory questions16 were added for all children. The focus of the present report is the results from the 9–12 year olds. Results from 7 to 9 year old participants for the 2009 survey are presented in the online supplement.

    Questionnaire

    The same questionnaire used in 2004 was distributed along with a letter explaining the purpose of the survey. The questions included ‘Has your child wheezed or had a whistle in the chest in the past three years?’, ‘Has your child ever had asthma?’, ‘Has your child ever had eczema?’ and ‘Has your child ever had hay fever?’ Full details of the questionnaire are presented in the online supplement. In addition to questions about asthma and related conditions, a history of smoke exposure and parental asthma were included.16 Data were entered manually with a small random sample being checked by a second person.

    Data analysis

    Imputation of missing values

    Our previous experience5 was that approximately 10% of questionnaires would have a response to the wheeze question but not for lifetime experience of asthma, eczema and hay fever questions. For incomplete questionnaires, missing lifetime asthma, eczema and hay fever data were imputed by extrapolating the ratio of wheeze to lifetime asthma, eczema and hay fever from complete questionnaires returned in 2009 while, at the same time, adjusting for school year group and neighbourhood deprivation (using the Scottish Index of Multiple Deprivation, SIMD17). For example, the imputed value (probability) of a child having asthma was 0.55 if they had wheeze and were in the 9–12 year age-group and in the most deprived SIMD and 0.46 if they did not have wheeze and were in the younger age group and in the most deprived SIMD. Appropriate standard errors of the proportions were calculated using the actual number of children with valid observations for each question. Only imputed values for asthma, eczema and hay fever are displayed in the tables and figures. Imputation was not possible for questionnaires which were not returned or returned without a response to the wheeze question. Imputation was not undertaken for the ISAAC questions since responses were generally complete (more than 96%5).

    Change in prevalence

    Generalised linear model (GLM) was used to analyse changes over the last three surveys adjusting for the effects of sex and deprivation category using imputed values for asthma, eczema and hay fever for years 2004 (imputed from 2004 data) and 2009; imputed values are a continuous variable. The resulting F values were adjusted to reflect the actual numbers observations to minimise the effect of imputation. Logistic regression (for the dichotomous outcome responses, eg, wheeze yes/no) was used to determine the significance of trends over 1999, 2004 and 2009 adjusting for sex, school year group and deprivation category. Standard statistical software was used (SPSS v 17) and significance was assumed at p<0.05.

    Results

    Study participants

    There were 2253 eligible children aged 9–12 of whom questionnaires were returned in 1196 (53%). Where the wheeze question was answered there were missing responses for questions on lifetime experience of asthma, eczema and hayfever in 8%, 11% and 12% of individuals. The average age (SD) of children was 10.8 years (0.9) and 588 were male (49%). Twenty six of the 31 eligible schools agreed to participate including four schools, which had not taken part in 2004; five schools which participated in 2004 declined to take part in 2009. There were no differences in SIMD (derived from school postcode) between participating and non-participating schools. In 2004, the prevalence of lifetime asthma for the five schools who did not participate in 2009 was not different to other schools who participated in 2004 and 2009 (online supplement). There were 22 schools (including two schools which had merged between 2004 and 2009) which participated in each of the surveys in 1999, 2004 and 2009. Compared to the whole 2009 study population, the children attending these 22 ‘common’ schools were similar in terms of age, gender, wheeze, lifetime prevalence of asthma, eczema, hay fever and parental asthma but were less likely to be exposed to tobacco smoke at home (32% versus 36%, p<0.001). The symptom outcomes for children attending the 22 ‘common’ schools, and all schools did not differ (table 2 and online supplement).

    Asthma, eczema and hay fever—longitudinal trends

    These data are presented in table 1. The lifetime prevalence of asthma rose from 24.3% (95% CI 22.8% to 25.8%) in 1999 to 28.4% (95% CI 26.2% to 30.6%) in 2004 but fell to 22.1% (95% CI 19.6% to 24.6%) in 2009, p<0.001 (GLM model assessing yearly trends adjusted for sex and SIMD), figure 1. The prevalence of wheeze in the previous 3 years fell from 27.9% (95% CI 26.4% to 29.4%) in 1999 to 25.2% (95% CI 23.2% to 27.2%) in 2004 and fell further to 22.2% (95% CI 19.8% to 24.6%) in 2009 (p<0.001, figure 1). Lifetime prevalence of eczema was 21.4% (95% CI 20.0% to 22.8%) in 1999, 34.1% (95% CI 31.7% to 36.5%) in 2004 and 30.7% (95% CI 27.9% to 33.5%) in 2009 (p<0.001, figure 1). The lifetime prevalence of hay fever was 15.4% (95% CI 14.1% to 16.6%) in 1999, 26.5% (95% CI 24.2 to 28.8) in 2004 and 25.7% (95% CI 23.1% to 28.4%) in 2009 (p<0.001, figure 1). The reduction in wheeze, asthma and eczema between 2004 and 2009 was significant in girls (p=0.021, p<0.001 and p=0.002, respectively), but there was no significant change in prevalence among boys between 2004 and 2009 (table 2). Unadjusted non-imputed results for 9–12 year olds in 2009 were as follows: recent wheeze 22.2% (265/1196), lifetime asthma 22.7% (250/1103), lifetime eczema 30.7% (328/1070) and lifetime hay fever 25.3% (266/1050). The values for wheeze in the past 3 years, lifetime asthma, eczema and hay fever, for 7–9 year olds were similar to the older children (online supplement).

    Figure 1
    Figure 1

    Trends in wheeze in the last 3 years and lifetime prevalence of asthma, eczema and hay fever in 9–12 year olds between 1964 and 2009. Dots indicate mean prevalence (%) and bars indicate 95% confidence intervals.

    View this table:
    Table 1

    Prevalences (%) with 95% CIs for history of wheeze in the past 3 years and lifetime prevalences of asthma, eczema and hay fever and wheeze for children aged 9–12 years attending all schools

    View this table:
    Table 2

    Separate results for boys and girls for prevalences (%) with 95% CIs for history of wheeze in the past 3 years and lifetime prevalences of asthma, eczema and hay fever and wheeze for children aged 9–12 years attending all schools

    ISAAC respiratory module questions

    The ISAAC questions were completed by 1164 respondents aged 9–12 years in 2009. Wheeze in the previous 12 months was reported to be 18.7% in 20045 and 16.2% (189/1164) in 2009, p=0.056. For girls, wheeze in the previous 12 months was reported to be 20.0% in 2004 and 14.5% in 2009 (p=0.014); for boys, the corresponding figures were 19.3% and 18.8% (p>0.05). The remaining ISAAC questions showed no significant change over time.

    Discussion

    This is the first published survey of asthma prevalence in British children since the mid 2000s, a time when the asthma prevalence was falling in some countries but not in the UK. For the first time in the 45-year history of our survey we report a fall in lifetime asthma prevalence in children aged 9–12 years. There were different trends in boys and girls; the reduction in asthma prevalence was more obvious in girls compared to boys, and there was evidence of falling wheeze in the past 1 and 3 years and also of reducing eczema prevalence in girls but not boys. Childhood asthma remains a very common condition in the UK, but after many years of increasing prevalence the number of affected children might finally be falling. These results should be interpreted with some caution since the response rate approached 50% and the findings should be confirmed elsewhere.

    Comparison of asthma prevalences between populations is complicated by differences in the age groups studied and the questionnaires used. Although a standard methodology for surveys was introduced in 1998,16 the Aberdeen Schools Asthma Survey began in 1964 and the original methodology has been preserved to allow direct comparison within 9–12 year olds in our population. The falling asthma prevalence reported here supports our hypothesis and is consistent with the fall in prevalence seen in 13–14 year olds in two areas of the UK surveyed in 1994 and 2002.8 The fall in lifetime asthma prevalence is also consistent with our previous report of falling wheeze in the past 3 years between 1999 and 2004; wheeze in the past 3 years is likely to be a more sensitive index of recent change in asthma compared with lifetime asthma prevalence. The most recent UK surveys of childhood asthma were completed in 7–12 year olds between 2002 and 20045,–,7 and all reported increasing prevalence; the present study suggests that this trend may be reversing over time. Our results are consistent with studies demonstrating falling asthma prevalence between 1989 and 2001 among 8–9 year olds in the Netherlands18 and between 2000 and 2005 among Australian 4–6 year olds.19 Despite differences in study designs, results from across the world indicate that childhood asthma remains a common problem but more evidence is accumulating to suggest that asthma prevalence may be falling in some countries, including the UK.

    The reduction in asthma between 2004 and 2009 was greater for girls compared to boys and this might suggest that gender might be relevant to falling symptom prevalence. There was also evidence that lifetime eczema prevalence had fallen between 2004 and 2009 for girls but not for boys (table 2). Although prevalences of asthma and eczema are traditionally understood to differ between sexes with the burden of symptoms being greater for boys,20 we have previously reported how the prevalence of asthma in boys was greater than for girls in 1989 but the sex difference has narrowed by 2004.21 The present results suggest that although in the past girls have ‘caught up’ with boys in terms of asthma prevalence, it is predominantly girls who are responsible for the fall in asthma we report here.

    This study was not designed to explain why asthma prevalence has decreased. The fall in asthma prevalence is likely in part to reflect a genuine fall in asthma and in part changes in diagnostic practice, for example, the revised 2003 British Thoracic Society/Scottish Intercollegiate Guidelines Network guidelines for asthma.22 The 1997 BTS/SIGN guideline for managing asthma23still advocated the diagnosis of ‘infantile asthma’ and contained a relatively brief section on diagnosis in children. By contrast, the 2003 guideline did not mention ‘infantile asthma’ was much more detailed including a flow chart to guide the decision making process and clues to alternative diagnoses; the 2003 document might have caused clinicians to be more cautious in diagnosing childhood asthma. The pathogenesis for asthma is complex and known to involve factors present in early life. The ban on smoking in public places from 2006 might have contributed to a fall in asthma prevalence between 2004 and 2009 since there is evidence that children's exposure to second-hand smoke has reduced in some settings since the smoking ban was introduced in Scotland.24 The 10% fall in lifetime asthma in girls between 2004 and 2009 was accompanied with a 7% fall in lifetime eczema and thus a fall in atopy may explain part of the reduction in asthma.

    There are a number of factors which should be considered when interpreting these data. One strength of our study is the common methodology used over 45 years which provided the opportunity to compare present trends with those from 1964. A second strength is the relatively static population of Aberdeen. A further strength is the use of imputation which allows data to be considered in the 8–12% of individuals where the questionnaire was incomplete. A limitation is that the response rate for the 2009 survey was 53%, in keeping with another community-based study of children in NE Scotland.25 The response rate in surveys up to 1999 exceeded 80%,13,–,15 but with the introduction of Data Protection Act in 2000 we were not able to directly contact parents and this has had implications for recruitment which we are not able to address. Although the participation rate dropped from 84% in 1999 to 57% in 2004, the similar response rate in 2004 and 2009 should permit direct comparison between surveys, although we cannot be certain that reasons for non-participation were constant for both surveys. The 2004 results were comparable with other UK populations in 2002 suggesting that the 2004 results were valid (eg, the proportion with wheeze in the previous 12 months was 17.4% in Aberdeen5 versus 20.9% elsewhere8 and a 10% rise in asthma seen in Aberdeen, South Wales and London between 1990s and early 2000s5,–,7). A second limitation is that not all schools participated in each survey; some schools declined to take part whilst several schools had merged or closed and the demographics of the study population might have changed between surveys. To address this potential bias we have demonstrated that children attending the ‘common’ schools were similar to the wider study population with the single exception of a reduced prevalence of exposure to tobacco smoke at home; importantly, there were no differences in the burden of symptoms (online supplement) between all children and those attending ‘common schools’.

    In summary, we report, for the first time in the UK, a fall in prevalence lifetime asthma in children and we look forward with interest to the results of the 2014 Aberdeen Schools Asthma Survey.

    Acknowledgments

    The authors are indebted to the staff at the schools involved, the parents and the children. The authors would also like to thank Valerie Angus and Olwyn Say for their assistance in data entry. They also acknowledge the unrestricted educations grants for awarded by Novartis and Allen and Hanbury's which were used to produce the questionnaires and the financial contribution made by parents at Cults Primary School which facilitated the statistical analysis.

    References

    1. ↵
    2. ↵
      1. Turner S,
      2. Thomas M,
      3. von Ziegenweidt J,
      4. et al
      . Prescribing trends in asthma: a longitudinal observational study. Arch Dis Child 2009;94:16–22.
      OpenUrlAbstract/FREE Full Text
    3. ↵
      1. Panickar JR,
      2. Dodd SR,
      3. Smyth RL,
      4. et al
      . Trends in deaths from respiratory illness in children in England and Wales from 1968 to 2000. Thorax 2005;60:1035–8.
      OpenUrlAbstract/FREE Full Text
    4. ↵
      1. Eder W,
      2. Ege MJ,
      3. von Mutius E
      . The asthma epidemic. N Engl J Med 2006;355:2226–35.
      OpenUrlCrossRefPubMedWeb of Science
    5. ↵
      1. McNeill G,
      2. Tagiyeva N,
      3. Aucott L,
      4. et al
      . Changes in the prevalence of asthma, eczema and hay fever in pre-pubertal children: a 40-year perspective. Paediatr Perinat Epidemiol 2009;23:506–12.
      OpenUrlCrossRefPubMed
    6. ↵
      1. Butland BK,
      2. Strachan DP,
      3. Crawley-Boevey EE,
      4. et al
      . Childhood asthma in South London: trends in prevalence and use of medical services 1991–2002. Thorax 2006;61:383–7.
      OpenUrlAbstract/FREE Full Text
    7. ↵
      1. Burr ML,
      2. Wat D,
      3. Evans C,
      4. et al
      . British Thoracic Society Research Committee. Asthma prevalence in 1973, 1988 and 2003. Thorax 2006;61:296–9.
      OpenUrlAbstract/FREE Full Text
    8. ↵
      1. Asher MI,
      2. Montefort S,
      3. Björkstén B,
      4. et al
      . Worldwide time trends in the prevalence of symptoms of asthma, allergic rhinoconjunctivitis, and eczema in childhood: ISAAC Phases One and Three repeat multicountry cross-sectional surveys. Lancet 2006;368:733–43.
      OpenUrlCrossRefPubMedWeb of Science
    9. ↵
      1. Annesi-Maesano I,
      2. Mourad C,
      3. Daures JP,
      4. et al
      . Time trends in prevalence and severity of childhood asthma and allergies from 1995 to 2002 in France. Allergy 2009;64:798–800.
      OpenUrlCrossRefPubMed
    10. ↵
      1. Ronchetti R,
      2. Villa MP,
      3. Barreto M,
      4. et al
      . Is the increase in childhood asthma coming to an end? Findings from three surveys of schoolchildren in Rome, Italy. Eur Respir J 2001;17:881–6.
      OpenUrlAbstract/FREE Full Text
    11. ↵
      1. Anthracopoulos MB,
      2. Liolios E,
      3. Panagiotakos DB,
      4. et al
      . Prevalence of asthma among schoolchildren in Patras, Greece: four questionnaire surveys during 1978-2003. Arch Dis Child 2007;92:209–12.
      OpenUrlAbstract/FREE Full Text
    12. ↵
      1. Dawson B,
      2. Illsley R,
      3. Horobin G,
      4. et al
      . A survey of childhood asthma in Aberdeen. Lancet 1969;1:827–30.
      OpenUrlPubMedWeb of Science
    13. ↵
      1. Ninan TK,
      2. Russell G
      . Respiratory symptoms and atopy in Aberdeen schoolchildren: evidence from two surveys 25 years apart. BMJ 1992;304:873–5.
      OpenUrlAbstract/FREE Full Text
    14. ↵
      1. Omran M,
      2. Russell G
      . Continuing increase in respiratory symptoms and atopy in Aberdeen schoolchildren. BMJ 1996;312:34.
      OpenUrlFREE Full Text
    15. ↵
      1. Devenny A,
      2. Wassall H,
      3. Ninan T,
      4. et al
      . Respiratory symptoms and atopy in children in Aberdeen: questionnaire studies of a defined school population repeated over 35 years. BMJ 2004;329:489–90.
      OpenUrlFREE Full Text
    16. ↵
      Anon. Worldwide variations in the prevalence of asthma symptoms: the International Study of Asthma and Allergies in Childhood (ISAAC). Eur Respir J 1998;12:315–35.
      OpenUrlAbstract
    17. ↵
      SIMD. Office of the Chief Statistician, Scottish Executive. Scottish Index of Multiple Deprivation 2006: technical report. http://www.scotland.gov.uk/Publications/2006/10/13142913/0 (Accessed 11 September 2009).
    18. ↵
      1. Mommers M,
      2. Gielkens-Sijstermans C,
      3. Swaen GM,
      4. et al
      . Trends in the prevalence of respiratory symptoms and treatment in Dutch children over a 12 year period: results of the fourth consecutive survey. Thorax 2005;60:97–9.
      OpenUrlAbstract/FREE Full Text
    19. ↵
      1. Ponsonby AL,
      2. Glasgow N,
      3. Pezic A,
      4. et al
      . A temporal decline in asthma but not eczema prevalence from 2000 to 2005 at school entry in the Australian Capital Territory with further consideration of country of birth. Int J Epidemiol 2008;37:559–69.
      OpenUrlAbstract/FREE Full Text
    20. ↵
      1. Anderson HR,
      2. Pottier AC,
      3. Strachan DP
      . Asthma from birth to age 23: incidence and relation to prior and concurrent atopic disease. Thorax 1992;47:537–42.
      OpenUrlAbstract/FREE Full Text
    21. ↵
      1. Osman M,
      2. Tagiyeva N,
      3. Wassall HJ,
      4. et al
      . Changing trends in sex specific prevalence rates for childhood asthma, eczema, and hay fever. Pediatr Pulmonol 2007;42:60–5.
      OpenUrlCrossRefPubMedWeb of Science
    22. ↵
      BTS/SIGN. British guideline on the management of asthma, 2008. http://www.sign.ac.uk/guidelines/fulltext/101/index.html (accessed 17 December 2009).
    23. ↵
      British Thoracic Society. The British Guideline on the Management of Asthma 1997. Thorax 1997;52(Suppl I):S1.
      OpenUrlPubMed
    24. ↵
      1. Akhtar PC,
      2. Currie DB,
      3. Currie CE,
      4. et al
      . Changes in child exposure to environmental tobacco smoke (CHETS) study after implementation of smoke-free legislation in Scotland: national cross sectional survey. BMJ 2007;335:545.
      OpenUrlAbstract/FREE Full Text
    25. ↵
      1. Devereux G,
      2. Turner SW,
      3. Craig LC,
      4. et al
      . Low maternal vitamin E intake during pregnancy is associated with asthma in 5-year-old children. Am J Respir Crit Care Med 2006;174:499–507.
      OpenUrlCrossRefPubMedWeb of Science

    Supplementary materials

    • Web Only Data adc.2010.189175

      Files in this Data Supplement:

    Footnotes

    • Competing interests ST had support from Allen and Hanbury's and Novartis for the submitted work (payment for printing of questionnaires).

    • Ethics approval This study was conducted with the approval of the University of Aberdeen College Review Board.

    • Provenance and peer review Not commissioned; externally peer reviewed.