IJE Advance Access originally published online on February 14, 2008
International Journal of Epidemiology 2008 37(3):559-569; doi:10.1093/ije/dyn029
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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
1 Murdoch Childrens Research Institute, Royal Children's Hospital, Melbourne, Australia.
2 Menzies Research Institute, University of Tasmania, Hobart, Australia.
3 Australian National University Medical School, Australian National University, Canberra, Australia.
4 Australian Primary Health Care Research Institute, The Australian National University, Canberra, Australia.
* Corresponding author. Murdoch Childrens Research Institute, Royal Childrens Hospital, Flemington Road, Parkville Victoria, Australia 3052. E-mail: anne-louise.ponsonby{at}mcri.edu.au
| Abstract |
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Background Asthma prevalence has declined in some countries over the past 10 years. Most reports have been based on population surveys conducted at two points of time in a given location. Comparisons across countries and time periods can be limited by differences in study methodology or disease diagnostics in different communities. Here, we examined trends in asthma prevalence using serial annual data and further examine the importance of country of birth.
Methods The source population has children aged 4–6 commencing school in the Australian Capital Territory from 2000 to 2005 inclusive. Over 80% of these children and their families completed a health questionnaire on asthma, other atopic disease and respiratory symptoms using some questions from the International Study of Asthma and Allergies in Childhood (n = 22 882). Current asthma has been previously validated against physician assessment in this setting.
Results The prevalence of current asthma declined (P < 0.001) but eczema ever increased (P < 0.001) from 2000 to 2005. The asthma decline was predominantly linear in form, and accompanied by a reduction in night cough and shortness of breath but not recent wheeze. Compared with Australian-born children, children from New Zealand and the United Kingdom had a similar prevalence of asthma, hay fever and eczema history. However, children born in other countries, such as Asia, generally had a lower prevalence of these disorders. The temporal trends for atopic disorders or respiratory symptoms did not differ for overseas-born compared with Australian-born children.
Conclusion The decline in current asthma prevalence from 2000 to 2005 was linear in form and appeared uncoupled from trends in child eczema. Country of birth was associated with marked variation in atopic disorder prevalence. The similar temporal trends for Australian vs overseas-born children indicate that the factors underlying the asthma prevalence decline are unlikely to be only in the pre-natal period.
Keywords Childhood asthma, prevalence, time trend, eczema, country of birth
Accepted 22 January 2008
| Introduction |
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Asthma prevalence has declined in some countries, but not others over the past decade.1 A greater understanding of the marked international and temporal variation in the prevalence of childhood atopic disease is required to improve the understanding of the aetiology of these disorders.
In 2006, the findings of the International Study of Asthma and Allergies in Childhood (ISAAC) were reported with a comparison of two cross-sectional surveys: Phase 3 (a cross-sectional survey conducted 1999– 2004 (mostly 2002–03) and Phase 1; conducted 1992–98 (mostly 1994–95).1 For 6- to 7-year-old children, the prevalence of asthma symptoms increased in only some centres (25/66) but decreased in other centres with the latter being characterized by a higher mean asthma symptom prevalence in Phase 1. In contrast, for both eczema symptoms and allergic rhinoconjunctivitis, prevalence increased in 80% of centres and this was irrespective of mean prevalence in Phase 1. For Australia, the mean change per year (SE) was –0.8% (0.16) for asthma, 0.67% (0.11) for eczema and 0.34% (0.11) for allergic rhinoconjunctivitis.1
The differing temporal trend for asthma compared with eczema and allergic rhinoconjunctivitis is in agreement with individual studies from Belmont and Melbourne, Australia, which have reported a decline in child recent wheeze but increasing eczema and allergic rhinoconjunctivitis rates over time.2,3 However, data have not been available from serial annual surveys to examine these trends beyond assessments at two time points.
Several studies have previously examined the association between country of birth and atopic disease. In Australia, migrants from Asia have lower rates of asthma, atopy and skin sensitization4–7 with higher disease rates among those with later age of migration. Similarly, Asian-born UK migrants had lower asthma prevalence than those born in the UK and this was particularly marked among those who migrated before age 5.8 In the USA NHANES study, asthma prevalence was lower among Mexican-born than US-born Mexicans9 but the European Community Respiratory Health Survey (ECRHS) reported more asthma symptoms in immigrants [OR 1.21 (95% CI;1.0–1.51)].7
With regard to changes over time, the Melbourne study found that the relative apparent inverse association between non-Australian birth and recent wheeze tended to be less evident in the 2002 survey [OR 0.8 (95% CI; 0.5–1.3)] than the earlier 1993 survey [OR 0.5 (95% CI; 0.3–0.7)].2 This suggests that the temporal decline in asthma may not have occurred to the same extent for overseas-born children.
Comparison across countries and time periods can be limited by differences in study participation rates, questionnaire interpretation and difference in disease diagnostics of health care. Although the ISAAC study had standardized measures across sites,10,11 there is concern that the prevalence of both symptoms and diagnoses of asthma are heavily dependent on an awareness of asthma in the population studied.12
We examined how asthma, eczema, hay fever and respiratory symptoms in the Australian Capital Territory (ACT) school entry survey differed by country of birth. Further, as serial annual surveys 2000–05 were available we examined temporal trends in these conditions and whether these changes over time differed by country of birth.
| Methods |
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School health nurses offer a health assessment to new entrants to kindergarten classes in all primary schools in the ACT. In preparation of the health assessment, a child health screening questionnaire is sent home to the parents of all children commencing primary school for the first time in the ACT. From 1999, this questionnaire has included questions on respiratory history, including parent-reported asthma, respiratory symptoms, eczema and hay fever.11,13 The survey includes some standardized core questions from the International Study for Asthma and Allergy in Childhood,10 including wheeze frequency over the last 12 months and frequency of ever having had asthma. In addition, the question Does your child have asthma? is used to indicate parent-reported asthma. In a previous study, this question has a sensitivity of 55% and a specificity of 94%, providing a likelihood ratio (LR) positive of 9.2 and LR negative of 0.513 for the physician diagnosis among ACT school children. Due to the lack of a single test or gold standard for asthma,14,15 here we report on not only parent-reported asthma but also on four recent respiratory symptoms.
This includes the ISAAC core question on recent wheeze (a positive report of wheezing or whistling in the chest in the last 12 months) as well as wheezing with colds, dry cough at night without colds and shortness of breath with exercise, all over the last 12 months (Appendix 1). Two questions from the ISAAC module were used to document hay fever ever and eczema ever.16 Although the question on hay fever has been found to have a high positive predictive value (71%) for atopy among those with rhinitis, the eczema question ever does not perform as well as related ISAAC questions that also include flexural location of the rash.16 The study sample for this report was child school entrants aged between 4 and 6 years in the ACT from 2000 to 2005 inclusive.
Although the ordering of atopic disease ever questions was the same from 2000 to 2005, and while most respiratory symptoms were similar in order by year, the wheeze with URTI question preceded the recent wheeze question in 2000 but not for 2001 onwards. Information was also collected in a standard manner over time on the use of preventers as regular asthma medication but not all symptomatic asthma medication. The preventers were: Intal (sodium cromoglycate), Tilade (nedocromil sodium), Pulmicort (budesonide), Flixotide (fluticasone), Qvar (beclomethasone dipropionate), Singulair (montelukast), Seretide (salmeterol/fulticasone), Symbicort (eformoterol/budesonide). The use of any of these is termed regular asthma preventer use for the purposes of this report.
Statistical methods
We examined the characteristics of each annual sample and assessed heterogeneity by year of school entry by chi-squared tests for categorical variables and ANOVA for continuous variables (Table 1). The proportion of children having a disease, symptom or preventer use was tabulated by country of birth in Table 2. We classified overseas-born children as migrants from English speaking (ES) or non-English speaking (NES) countries. Child migrants from New Zealand, the United Kingdom and North America were considered to be from ES countries.
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We built models with a continuous exposure term for year of survey for each of the outcomes listed in Figure 1. We compared model fit using linear regression with fractional polynomial regression.17 For the wheeze with upper respiratory tract infection (URTI) outcome, the R2 was greater for the fractional polynomial than the linear regression model, indicating non-linearity. The form of the unadjusted relationship between year of entry and atopic disease and respiratory symptom outcomes is shown in Figure 1.
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Multiple logistic regression models were used to examine associations.18 Potential confounders were added as covariates to this model. Routinely, we adjusted for age at school entry, child gender and usual doctor. The rationale for adjustment for the later was that children with a regular primary care doctor may be more likely to be diagnosed with a disorder or provided regular medication and we wanted to remove these effects to any assessment of how disease rates had changed over time or by country of birth. Tests of trend of ordered categorical variables (year of school entry) were undertaken by testing the statistical significance of the coefficient of a linear predictor formed by assigning consecutive integer scores to the categories in ascending or descending order. In these models, the significance (P-value) for the interaction term was assessed by the Wald test applied to the coefficient of the product term (for example, asthma prevalence change per year by country of birth). Because interaction tests often use a different significance than P = 0.05,19 interaction values with P < 0.1 were considered to indicate significance.
| Results |
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From 2000 to 2005, 22 882 children aged between 4 and 6 years began school in the ACT and had parent-completed questionnaire data available. The proportion of children with completed questionnaire by school entry year was: 2000, 81%; 2001, 89%; 2002, 85%; 2003, 86%; 2004, 87% and 2005, 89%.
The characteristics of the samples in the serial cross-sectional surveys are shown in Table 1. From 2000 to 2005, the proportion of children born overseas remained relatively constant (P = 0.55) varying from 5.1% to 6.1%. The mean age of the sample varied from 4.9 to 5.1 years over the time period. Of the children born overseas, the proportion born in Asia or Africa did vary by year of survey and was higher in more recent years (Table 1). Of overseas-born school entrants, 38.4% migrated before the age of 18 months. A higher proportion had migrated at age 18 months or more in recent, compared with earlier years (Table 1).
We examined variation in prevalence by year of survey (Table 2). From 2000 to 2005, there was variation in the prevalence of most atopic disease and respiratory outcomes. Figure 1 shows that these temporal trends were not uniform in direction. While eczema prevalence among school entrants increased (P < 0.001) from 2000 to 2005, the prevalence of asthma ever, hay fever ever and current asthma declined (Figure 1). In addition, the prevalence of night cough or shortness of breath on exercise or playing also declined. The proportion of children reporting recent wheeze tended to decrease over time (P = 0.19). The trends were predominantly linear in form. Fractional polynomial regression did not provide greater R2 than linear regression with the exception of wheeze with URTI outcome.
The adjusted ORs for having these disorders per year from 2000 to 2005 is shown in Table 2. The likelihood of eczema increased (P < 0.001) but of asthma ever or current asthma decreased (P < 0.001) per year. Night cough and shortness of breath were also less common for more recent school entrants (Table 2). Although the unadjusted trend was downward for wheeze with URTI (Figure 1), this was reduced after adjustment for age, sex and whether the child had a usual doctor (Table 2).
Tables 3–5![]()
show the proportion of children with atopic disease or respiratory symptoms by country of birth. Marked heterogeneity was observed. For asthma ever and eczema ever, the highest prevalence was noted for New Zealand born and the lowest for non-UK Europe and other countries born, respectively (Tables 3–5![]()
). Hay fever ever was most common among Australian-born. Among the overseas-born the prevalence of the disorders shown in Tables 3–5![]()
did not vary by age of immigration (<18 months vs 18 months or older) with the exception of hay fever with a prevalence of 12.3% (34/277) vs 7.7% (32/416); P = 0.009 for younger and older immigrants from NES countries, respectively.
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The likelihood of having eczema, hay fever or asthma was substantially lower for children born in non-UK Europe, Asia or other countries than Australian-born children. Children born in North America, Asia or other countries were less likely to be reported to have current asthma. Of note, immigrant children from New Zealand or the United Kingdom did not differ to Australian-born children with regard to the likelihood of these disorders (Tables 3–5
We then stratified school entrants by whether they were Australian-born, overseas-born from ES or NES countries (Table 6). Among the Australian-born, an eczema prevalence increase and asthma ever or current asthma prevalence decrease was observed, accompanied by a decline of borderline significance in asthma preventer use (Table 6). There was no difference in the adjusted odds ratio per year for any outcome in Table 6 between Australian and overseas born except recent wheeze, which declined to a greater extent among Australian born than migrants born in an ES country (Table 6).
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We examined whether the odds ratios per year in Table 6 for the outcome of recent wheeze altered substantially after adjustment for regular asthma preventer use. We found that the Australian-born had an adjusted odds ratio (AOR) of 0.99 (95% CI; 0.96, 1.01). Again, there was no difference in effect for overseas-born to the Australian-born (P = 0.97).
We further examined recent wheeze trends among those who were not on regular asthma preventer use. We found that the Australian-born had an AOR of 0.98 (95% CI; 0.96, 1.01). Again, there was no difference by location of birth (P = 0.92).
We examined whether differences in disease prevalence were likely to reflect differences in diagnosis or treatment by country of birth. Among children with asthma there was no variation in the proportion on regular asthma preventer use by country of birth; however, there was for recent wheeze, (P = 0.18 and P = 0.01, respectively). Among those with asthma ever, the proportion with recent wheeze did not vary by country of birth (P = 0.28). Among those with current asthma, the proportion with recent wheeze did vary by country of birth (P = 0.04).
| Discussion |
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In this series of annual surveys of school entry into primary school in the ACT, temporal trends were observed for the prevalence of these disorders from 2000 to 2005. A marked reduction in history of asthma ever was accompanied by parallel reductions in current asthma, night cough, shortness of breath and hay fever ever but not recent wheeze. In contrast, the prevalence of eczema increased steadily.
Strengths of this study include the availability of annual surveys which, to our knowledge have not previously been assessed in relation to recent changes in asthma and also other atopic disorders. Further, the sample was large and representative. The response rates to the survey were high for all years and age, and sex distribution of the sample did not change markedly over time. We have previously reported that current asthma has very good agreement with physician diagnosis in this setting.13 The clinical diagnosis of asthma, eczema and hay fever would have been generally made in the ACT using a uniform health care system. However, we cannot exclude the possibility that the increase in eczema partly reflects a change in reporting as objective measures are not available.
Overall, the time trends for wheeze should be treated with caution because the questionnaire ordering of these items changed over time. Providing reassurance that at least part of the asthma decline was real, parallel declines in night cough and shortness of breath were reported. The lack of a downward trend for recent wheeze but not asthma raises the possibility that part of the asthma decline is due to a change in diagnostic labelling. This is further supported by the results of a recent medication analysis in our location that found that although only 19% of salbutamol use was for children without asthma in 2000, this had increased to 35% by 2005.20
Children who were born overseas were generally less likely to have eczema, hay fever or asthma history and also less likely to have respiratory symptoms and be on regular preventer medication. An exception to this pattern for overseas-born children was for children born in New Zealand who had similar prevalence to Australian-born children for these disorders. Among children who were born overseas but residing in Australia at the time of school entry, age at migration (under 18 months vs 18 or more months of age) did not appear important except with regard to lower hay fever prevalence in the older age immigrants from NES countries. Previously, we have shown that children in the ACT have a high prevalence of ryegrass sensitization21 and it is possible that children who avoid this setting in the first 18 months of life may be less likely to have a history of hay fever by school entry. Previously, Asian immigrants into Australia have been found to have higher rates of hay fever with increasing Australian residence, indicating that post-migration local factors are important in hay fever initiation.5
Potential limitations in the examination of migrants include small numbers by some individual countries of birth and that recent migrants may not be likely to report to health care and thus not have a label of asthma. However, the proportion of children with recent wheeze among those with asthma ever did not vary by country of birth, suggesting that country of birth differences in asthma ever were also not likely to reflect differences in asthma labelling among children with wheeze. Similarly, among those with asthma, the proportion with preventer use does not differ by country of birth—suggesting medical care is similar and not an explanation for the country of birth differences in symptoms. However, it was shown that for those with current asthma, the proportion with recent wheeze did vary by country of birth. This may reflect differences in severity of current asthma by country of birth. Nevertheless, the problems of variable asthma diagnosis or treatment or questionnaire ascertainment of symptoms by country of birth is likely to be less in this study than international study comparisons. Thus, this study provides important confirmatory findings to support the findings of the ISAAC study that the prevalence of asthma symptoms is lower in many Asian countries than Australia or New Zealand.1
The similarity of prevalence for Australia, New Zealand the United Kingdom for these disorders was evident. Although this could reflect an English-speaking background, children from North America had a much lower prevalence of asthma and atopic disorders suggesting this may not be the case. Previously, rates of sudden infant death syndrome were also high in these three countries prompting people to point out a common cultural heritage with regard to the culture of infant and child care.22 The finding of lower prevalence of these disorders among those migrating to Australia from Asia is consistent with past work in the United Kingdom and Australia.4–6
Although children born overseas in the later time period were still at lower risk of these disorders than Australian-born children, the temporal trends for the atopic disorders did not differ between Australian or overseas born. This suggests that the factors underlying the decline in asthma prevalence in Australia2,3 are likely to operate in early life but not in the pre-natal period alone. The lack of effect of age of migration may be that we were examining only early life before the age of five and that age-related effects occur after this age or may reflect that age at migration does not necessarily reflect change in cultural practices which may persist beyond their physical migration.
The decline in asthma prevalence was uncoupled from an increasing trend for eczema over the same time period. This uncoupling of asthma and other atopic diseases over time has been reported in two other Australian studies (Belmont, Melbourne).2,3 However, those studies also reported an uncoupling of asthma trends from hay fever trends but this was not observed here. We propose that one reason may be that in our setting, asthma is strongly linked to ryegrass sensitization,21 so hay fever and asthma may be more tightly linked in our location.
When considering the asthma prevalence decline over time in our location, one must consider factors that could potentially have changed over time that would impact preferentially on asthma or hay fever rather than eczema. A full discussion of the comparative aetiologies of these three diseases is beyond the scope of this paper, but two issues are now discussed. One such factor is environmental pollen load. In Australia, ryegrass pollen load increases with higher spring rainfall patterns.23 Thus, it is possible that a rainfall decline would impact to reduce hay fever and asthma. However, over 2000 to 2005, no clear trends for declining rainfall24 were evident (total annual rainfall P = 0.88, total spring rainfall, P = 0.87). Another possible factor to consider is infection of the respiratory tract, a site of interest for asthma and hay fever but not eczema. Asthma is thought to be increased by respiratory tract infections in early life,25,26 although studies have been conflicting. In this context, it is interesting to note that child passive smoke exposure, a risk factor for respiratory tract infection,27 has declined in Australia over time. National survey data indicate that in 1995, 31% of children were exposed to tobacco smoke in the home and by 2001, 20% of children.28 Furthermore, passive smoke exposure has been related to a higher asthma risk rather than eczema risk.29–33 Further work is required to evaluate the role of environmental factors in the asthma decline.
In conclusion, this study has demonstrated a marked variation in the prevalence of atopic disorders and respiratory symptoms among ACT children at school entry. Among overseas-born children, age at migration related only to hay fever history by school entry. Marked temporal trends were observed and it was particularly notable that an increase in eczema occurred while asthma prevalence declined from 2000 to 2005. The temporal trends did not differ markedly by country of birth, indicating postnatal factors may be important. Further work is required to identify factors that may underlie these temporal trends and country of birth effects.
| Appendix 1 |
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Respiratory symptoms and disease history in the Part 1 kindergarten survey
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Items I1-I5 are International Study of Asthma and Allergies in Childhood (ISAAC) questions.1
| Acknowledgements |
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We thank all children, families and schools participating in the school entry survey. We thank the maternal and child health nursing service for distributing and collecting the forms and ACT Community Care for conducting this school program. We thank Rachel Yates for developing the collation system.
Conflict of interest: None declared.
KEY MESSAGES
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