There have been trends worldwide of increased prevalence of both obesity and allergic disorders. Experimental models, several prospective cohort studies and meta-analysis have evaluated the association between obesity and allergy, mostly focusing on asthma, asthma-like symptoms and bronchial inflammation(Reference Chen, Rennie and Cormier1–Reference Gregor and Hotamisligil4). However, the association tends to be stronger in non-allergic or non-atopic individuals than in allergic or atopic individuals(Reference Chen, Dales and Jiang5). A similar trend was proven in bronchial hyperresponsiveness and atopic dermatitis(Reference Silverberg, Kleiman and Lev-Tov6–Reference Mitchell, Beasley and Björksten8), but obesity was negatively associated with the prevalence of allergic rhinitis or there was no relationship(Reference Mitchell, Beasley and Björksten8–Reference Kusunoki, Morimoto and Nishikomori10). Gender is also likely to be important when examining the relationship between allergic disease and obesity in children and adults, but the evidence is inconclusive. Some data showed a relationship of obesity and asthma only in females. Among a number of studies that have been conducted among children and adults, some have demonstrated an increased risk of atopy among overweight or obese individuals(Reference Visness, London and Daniels11, Reference Calvert and Burney12), while others have found no association between adiposity and atopy(Reference Van Gysel, Govaere and Verhamme13, Reference Leung, Kong and Chan14).
The objective of the present study, a part of the Epidemiology of Allergic Disorders in Poland study (ECAP), was to analyse the association between the different BMI categories (normal weight, overweight and obesity) and allergic diseases and sensitization in a population of Polish children aged 6–7 years and 13–14 years and adults aged 20–44 years.
Materials and methods
Study population
ECAP used the methodology of the International Study of Asthma and Allergies in Childhood (ISAAC) and the European Community Respiratory Health Survey (ECRHS). The study areas were selected according to the ECRHS guidelines. ECAP involved the populations of the eight largest urban agglomerations in Poland (each with over 150 000 inhabitants) and additionally one rural region, also with a population of over 150 000 inhabitants since the rural population accounts for 39 % of the entire Polish population. The study areas were chosen specifically but the study participants were selected by stratified random sampling based on the national identification number PESEL. In accordance with the ISAAC and ECRHS protocols, the study included three groups of respondents: children aged 6–7 years and 13–14 years, and adults (aged 20–44 years).
The first part of the project (a questionnaire survey) was carried out on a group of 22 703 participants with the response rate of 64·4 % and eventually 18 617 completed questionnaires were accepted. It involved two age groups of children, 6–7-year-olds and 13–14-year-olds, and adults. There were 4510 (24·2 %) 6–7-year-olds, 4721 (25·4 %) 13–14-year-olds and 9386 (50·4 %) adults. Of the respondents, 10 011 (53·8 %) were female and 8606 (46·2 %) were male. In the medical evaluation part of the study, 4783 patients (25·7 % of the respondents) were assessed on an out-patient basis, including 1329 aged 6–7 years, 1321 aged 13–14 years and 2133 adults. The study group design is shown in Table 1.
Table 1 Baseline characteristics of the study population, part of the Epidemiology of Allergic Disorders in Poland study (ECAP)
Questionnaire-based survey
The questionnaire was based on the translated and validated questionnaires used in ECRHS and ISAAC. The diagnosis of allergic diseases was based on the assumptions of these studies described in detail in previous reports(Reference Sybilski, Raciborski and Lipiec15). Details of the definition of the diseases are shown in the Appendix.
Medical evaluation
Allergologists diagnosed asthma according to the GINA (Global Initiative for Asthma) criteria, allergic rhinitis using the ARIA (Allergic Rhinitis and its Impact on Asthma) criteria and atopic dermatitis using the Hanifin and Rajka criteria. Skin prick testing (SPT) was performed for fifteen of the most common air-borne allergens (Allergopharma, Reinbek, Germany) such as: hazel (Corylus spp.); alder (Alnus spp.); birch (Betula spp.); grasses/crop plants; rye (Secale cereal); mugwort (Artemisia spp.); plantain (Plantago spp.); Alternaria, Cladosporium and perennial allergens, including moulds I (Alternaria tenis, Botrylis cinerea, Cladosporium herbarum, Culvularia lanata, Fusarium moniliforme, Helminthosporium) and moulds II (Aspergillus fumigatus, Mucor mucedo, Penicillium notatum, Rhizopus nigricans, Serpula lacrymans, Pullularia pullulans); common species of mites (Dermatophagoides pteronyssinus and Dermatophagoides farinae); and dog and cat dander. The test was considered negative when the wheal size was <3 mm, positive when the wheal size was 3–5 mm and markedly positive when the wheal size was ≥6 mm. Positive SPT for at least one allergen indicated atopy.
Anthropometric measurements
In all participants included in the study, the anthropometric parameters were obtained by a questionnaire. Parents of 6–7-year-olds, 13–14-year-olds and adults recorded the body weight (to nearest 0·1 kg) and height (to nearest 0·5 cm). In those participating in the out-patient study, we measured weight without shoes or outer clothing (to nearest 0·1 kg) and height (to nearest 0·1 cm). BMI was calculated as weight/height2 (kg/m2). BMI was analysed as a categorical variable divided into three categories (normal weight, overweight and obesity). According to the accepted definition in epidemiological studies, adult obesity was defined as BMI≥30·0 kg/m2, overweight as BMI=25·0–29·9 kg/m2 and normal weight as BMI=18·5–24·9 kg/m2(Reference Konno, Hizawa and Fukutomi9, Reference Han, Lawlor and Kimm16). Children’s BMI referred to the new Polish growth charts (OLAF Study)(Reference Kułaga, Różdżyńska and Palczewska17) and obesity was diagnosed when BMI was >95th percentile, overweight when BMI was >85th and <95th percentile and normal weight when BMI was >3rd and <85th percentile.
Statistical evaluation
A χ 2 test or Fisher’s exact test (for small sample sizes) was used in the statistical analysis. To determine the strength of association and the dependence between variables, χ 2 statistics and odds ratios were calculated. Results were considered to be statistically significant at P<0·05.
Ethics
The study was approved by the institutional Bioethics Committee. It was carried out as part of the project ‘Implementation of the system for prevention and early diagnosis of allergic disorders in Poland’ (No. 6 P05 2005 C/06572) funded by the Minister for Health and the Minister for Science.
Results
The prevalence of obesity and overweight and of allergic diseases and sensitization in the study population is shown in Table 2.
Table 2 Prevalence of obesity, overweight and allergic diseases and sensitization in the study population, part of the Epidemiology of Allergic Disorders in Poland study (ECAP)
SPT, skin prick test.
Data are presented as percentages.
Among adults (based on the questionnaire), a more frequent presence of symptomatic asthma was significantly associated with being overweight (OR=1·34; P<0·0001) and obese (OR=1·80; P<0·0001). In 13–14-year-olds symptomatic asthma was more frequent only in the obese (OR=1·76; P=0·017). Being overweight was significantly associated with an increased prevalence of declared asthma in 6–7-year-olds (OR=2·44; P<0·0001) and 13–14-year-olds (OR=1·66; P=0·016). Obese patients had no increase of declared asthma. Data based on medical evaluation showed that being overweight (OR=1·99; P=0·032) and obese (OR=2·17; P=0·031) were associated with an increased occurrence of asthma just in 6–7-year-old children. An increased prevalence of sensitization was only found in obese children aged 6–7 years (OR=1·84; P=0·017). Detailed data are shown in Table 3.
Table 3 Relationship between overweight and obesity and the prevalence of allergic diseases and sensitization in the study population, part of the Epidemiology of Allergic Disorders in Poland study (ECAP)
SPT, skin prick test.
Reference category is normal weight. Statistically significant values are shown in bold.
When we divided the patients into two groups: sensitized to seasonal (positive SPT just for seasonal aeroallergens) and perennial (positive SPT just for perennial aeroallergens)aeroallergens, we found no effect of being overweight and obese on the prevalence of sensitization. We also found no effect of being overweight and obesity on monovalent v. polyvalent atopy (data not presented).
In adults, there was a significantly higher prevalence of symptomatic asthma in overweight (OR=1·53; P<0·001) and obese (OR=2·01; P<0·001) females (Table 4(a)). Among 13–14-year-olds, the same significance and tendency were also seen only in obese girls (OR=2·25; P=0·026). In adults, overweight (OR=0·81; P=0·015) and obese (OR=0·76; P<0·05) males had a significantly decreased prevalence of allergic rhinitis.
Table 4 Association of different BMI categories with the prevalence of allergic diseases and sensitization according to gender (a) and place of residence (b), study population part of the Epidemiology of Allergic Disorders in Poland study (ECAP)
SPT, skin prick test; TSS, too small sample.
Reference category is normal weight. Statistically significant values are shown in bold.
Among participants from urban areas, the prevalence of symptomatic asthma was significantly higher in overweight (OR=1·36; P<0·01) and obese (OR=1·88; P<0·01) adults and obese 13–14-year-olds (OR=2·07; P<0·01). Similar correlations were not observed in inhabitants from rural areas. In rural adult inhabitants, being overweight was associated with a decreased prevalence of allergic rhinitis (OR=0·59; P=0·02; Table 4(b)).
Discussion
To our knowledge, the present study is first and largest one in this part of Europe assessing the relationship between overweight and obesity and the prevalence of allergic diseases and sensitization among children and adults, using data from a large questionnaire-based survey. The data were collected from almost 20 000 participants and additionally from medical evaluation of more than 4500 out-patients. The study was conducted in accordance with the standards of ISAAC and ECRHS and due to the Polish specificity (rural residents constitute 39 % of the Polish population) included one rural area.
In the literature, there are conflicting reports about the influence of BMI on allergic status. At the present state of knowledge, it appears that no study has confirmed objective evidence for the association, and results might be due to increased reporting of symptoms in obese individuals or to diagnostic bias. Similar contradictory results were also found for BMI and atopy. Our study confirmed previous reports of cross-sectional epidemiological studies that being overweight and obese is associated with an increased risk of asthma in adults (especially symptomatic asthma). Additionally, the adverse effect increased with increasing BMI: being obese compared with being overweight substantially increased the risk of asthma. Several investigations have already shown that the relationship between obesity and asthma is more likely to be observed among females, which is consistent with our present finding. It has been speculated that female sex hormones may contribute to the increased risk of asthma in obesity, although the precise mechanisms remain to be elucidated(Reference Weiss and Shore18). Confirmation of the profound impact of environmental factors and lifestyle on the development of asthma was our finding of the relationship between being overweight and obese and the prevalence of asthma only in urban residents. There was no such trend in the rural population. This could be due to the representation of the rural inhabitants, who accounted for approximately 20 % of our study population; this is relatively low compared with the true percentage of the entire Polish population and the proportion of the urban population. The second reason for such a result could be the fact that in addition to a high BMI increasing the prevalence of asthma, other environmental factors could also play a role (e.g. air pollution, smoking and lifestyle). Further detailed study is required to analyse the impact of obesity and overweight in allergic diseases in rural populations.
In 6–7-year-old children, based on a questionnaire survey, we confirmed no correlation between obesity and asthma, but there was a statistically significant increased prevalence of clinically diagnosed asthma. In overweight children, there was an increased occurrence of clinically diagnosed asthma and declared asthma. This finding, as well as a trend towards atopy in this group, is also supported by the significant association with SPT ≥ 6 mm. It seems that this discrepancy may be due to underdiagnosis of asthma in the Polish population, which was recorded in ECAP and presented in previous reports(Reference Samoliński, Sybilski and Raciborski19).
Although the association between obesity and asthma has been gaining more attention, few studies have been conducted concerning the relationship between obesity and other allergic diseases. The results are ambiguous and often contradictory. Most of the published studies suggest that being overweight and obese has a positive association with atopic dermatitis in children and adults(Reference Silverberg, Kleiman and Lev-Tov6–Reference Mitchell, Beasley and Björksten8, Reference Kusunoki, Morimoto and Nishikomori10, Reference Murray, Canoy and Buchan20, Reference Luo, Xiang and Dong21). However, there are also reports of the non-existence of such a relationship(Reference Van Gysel, Govaere and Verhamme13, Reference Tanaka, Miyake and Arakawa22), which is consistent with our results. We found no effect of higher BMI on the prevalence of atopic dermatitis in children and adults, as well as in men and women, and urban and rural inhabitants.
Another interesting and unexpected finding of our study was that being overweight and obese had a negative association with rhinitis prevalence in males 20–44 years of age. The odds ratio for occurrence of allergic rhinitis in overweight men was 0·81, but the risk was even lower in obese men (OR=0·76). Of note, similar results were obtained in the Japanese population in adults(Reference Konno, Hizawa and Fukutomi9) and schoolchildren(Reference Kusunoki, Morimoto and Nishikomori10). These results may support our findings of opposing effects of obesity on asthma and rhinitis. The explanation for this phenomenon may be found in the results of the study by Johnston et al.(Reference Johnston, Zhu and Rivera-Sanchez23), who showed enhanced airway responsiveness with attenuation of airway inflammation in obese mice. These observations were confirmed by Yoo et al.(Reference Yoo, Kim and Lee24), who indicated an increased bronchial hyperresponsiveness in obese patients. In addition, at the same time, obesity is associated with increased breathing effort, decreased physical activity and poorer skill performance, which could also cause the development and exacerbation of asthma.
The lack of an association between adiposity and atopic sensitization, which has also been observed in our and other studies(Reference Van Gysel, Govaere and Verhamme13, Reference Leung, Kong and Chan14, Reference Murray, Canoy and Buchan20), suggests that the underlying biological pathway of development of asthma may involve non-immunological mechanisms.
Also, some confirmation of this assumption is the study by Chen et al.(Reference Chen, Dales and Jiang5). Their results demonstrated that the association between increased BMI and asthma was stronger among non-allergic adults compared with allergic adults. If one assumes that those without a history of allergy are less likely to have allergic asthma, Chen’s observations suggest that obesity has a stronger relationship with non-allergic than allergic asthma. On the other hand, we have the results of several research groups that indicate a significant association between obesity and atopic sensitization(Reference Chen, Rennie and Cormier1, Reference Van Gysel, Govaere and Verhamme13, Reference Yoo, Kim and Lee24). It seems that the mechanisms for atopic sensitization associated with obesity need to be explored, and further cross-sectional studies are required.
Conclusion
In conclusion, our cross-sectional study using the ISAAC and ECRHS standards showed that being overweight and obese is associated with an increased prevalence of symptomatic asthma in adults, especially in women. This correlation was only observed in obese 13–14-year-olds. Being overweight in the 6–7-year-old group was associated with an increased prevalence of clinically diagnosed asthma and declared asthma and a trend towards atopy. Higher BMI was negatively associated with the occurrence of allergic rhinitis in overweight and obese men. Being overweight and obese were not significant factors in increased prevalence of atopy for either males or females. Further study of the relationship between obesity and allergic diseases should shed light on the complex aetiologies of the diseases and lead to new management options for allergy.
Acknowledgements
Financial support: This study was carried out as part of the project ‘Implementation of the system for prevention and early diagnosis of allergic disorders in Poland’ (No. 6 P05 2005 C/06572) funded by the Minister for Health and the Minister for Science. The Minister for Health and the Minister for Science had no role in the design, analysis or writing of this article. Conflict of interest: None. Authorship: B.S., F.R., A.T., A.L. and E.F.-K. conceived and carried out the experiments; A.J.S., J.K. and B.S. conceived the experiments and analysed data; A.L. and K.F. carried out the experiments; A.J.S. and B.S. conceived the data interpretation; A.S. conceived the literature search and generation of figures. All authors were involved in writing the paper and had final approval of the submitted and published versions. Ethics of human subject participation: The study was approved by the institutional Bioethics Committee in the Centre of Postgraduate Medical Education.
Appendix
Definition of allergic diseases
Allergic diseases are defined if answers to the questions are ‘yes’.
Declared asthma (DA): ‘Have you ever had asthma?’
Symptomatic asthma (AS): ‘Have you had wheezing or whistling in your chest at any time in the last 12 months?’
Allergic rhinitis (AR): ‘Do you have any nasal allergies, including hay fever?’
Atopic dermatitis (AD) is defined if the answers to questions 1 and 2 and 3 are ‘yes’:
1. ‘Have you ever had an itchy rash that was coming and going for at least 6 months?’
2. ‘Have you had this itchy rash in the last 12 months?’
3. ‘Has this itchy rash at any time affected any of the following places: the folds of the elbows, behind the knees, in front of the ankles under the buttocks or around the neck, ears or eyes?’
