Asthma and allergy in Russian and Norwegian schoolchildren: results from two questionnaire-based studies in the Kola Peninsula, Russia, and northern Norway

Authors


Dr Anders Selnes, Gjøvik Fylkessykehus (Oppland Central Hospital)
Kyrre Grepps gt. 11
N-2819 Gjøvik
Norway

Abstract

Background: Previous studies have shown that the prevalence of asthma and allergy in children is lower in Eastern than Western Europe.

Methods: We have compared the prevalence of asthma, respiratory symptoms, allergic rhinoconjunctivitis, and atopic dermatitis in schoolchildren aged 7–13 years in a questionnaire-based study conducted in the city of Nikel on the Kola Peninsula, Russia, in 1994 (n=1143) and another conducted in northern Norway in 1995 (n=8676).

Results: The prevalence of diagnosed asthma was 5.1% in Russian children and 8.6% in Norwegian children; RR=0.58 (95% CI: 0.44–0.76). The prevalence of all respiratory symptoms was higher in Russian children. The prevalence of allergic rhinoconjunctivitis was 16.9% in Russian children and 22.1% in Norwegian children: RR=0.74 (95% CI: 0.65–0.85). The prevalence of atopic dermatitis was 7.4% in Russian children and 19.7% in Norwegian children; RR=0.38 (95% CI: 0.31–0.46).

Conclusions: We conclude that the prevalence of diagnosed asthma, allergic rhinoconjunctivitis, and atopic dermatitis was higher in Norwegian than Russian schoolchildren. The higher prevalence of respiratory symptoms in Russian children probably reflects a higher prevalence of undiagnosed, nonallergic asthma.

Epidemiologic studies have shown a higher prevalence of asthma in Western than Eastern Europe (1–3). In the phase I report from the International Study of Asthma and Allergies in Childhood (ISAAC), marked variations in the prevalence of both asthma and allergy were found between the countries (4, 5). The authors suggest that the major differences are likely to be due to environmental factors. von Mutius et al. studied the prevalence of asthma, allergic rhinoconjunctivitis (AR), atopy, and bronchial hyperresponsiveness (BHR) in children 9–11 years old in West and East Germany (1). They found a higher prevalence of BHR, current asthma, and AR in the West German children than in the children in East Germany. They concluded that sensitization to aeroallergens was strikingly more frequent in West Germany than in East Germany. The prevalence of atopic sensitization and respiratory symptoms was studied in Estonian schoolchildren (2). The investigators concluded that, as in other former socialist countries of Europe, the prevalence of atopy as defined by positive skin prick tests, asthma, and respiratory symptoms, was low in Estonia.

A questionnaire-based prevalence study of asthma and allergy in schoolchildren was conducted in the city of Nikel, Russia, in 1994, and in northern Norway in 1995. Here, we compare the prevalence of asthma, respiratory symptoms, AR, and atopic dermatitis (AD) in the Russian and Norwegian schoolchildren.

Material and methods

The questionnaire

In 1985, Bolle and Holt formulated a four-page questionnaire to assess the prevalence of asthma and allergy in schoolchildren aged 7–13 years in northern Norway (6, 7). This questionnaire has been employed in many Norwegian studies of atopic diseases in children (8–10). It focuses on asthma, AR, AD, urticaria, and food intolerance and symptoms related to these diseases (symptom-based questionnaire). It also focuses on atopic diseases in parents/siblings, and indoor/outdoor environments. The questionnaire includes an accompanying letter with a broader description of symptoms and signs of the diseases in question.

Norwegian study

In 1995, this questionnaire was distributed to primary schoolchildren in northern Norway (11). The primary schools were randomly selected within the three northernmost counties of Norway, i.e., Nordland, Troms, and Finnmark. The local school nurse provided the schoolchildren with questionnaires, which were filled in at home. In agreement with the respondents, the school nurse ensured that all fields were filled in before the questionnaires were returned to the Institute of Community Medicine, University of Tromsø, Norway. In the Norwegian survey, 9950 schoolchildren aged 7–13 years were included, and 8676 subjects (87.3%) returned a completed questionnaire. The Norwegian questionnaire was answered by the child's mother in 78.5% of cases and by the father in 12.3%, by both mother and father in 5.0%, by the child in 2.9%, and by others in 1.3%.

Russian study

In 1994, a similar study was conducted among all primary school- children aged 7–17 years, in the city of Nikel on the Kola Peninsula, Russia. The questionnaire described above was translated into Russian by a person well acquainted with both written Norwegian and written Russian. In order to evaluate the translation, an independent translator, with medical experience, back-translated the Russian version into Norwegian. The questionnaires were filled in at home by the schoolchildren and their parents. Before delivery, the schoolteacher went through the questionnaire with the respondents to ensure that all fields were completed. There were 1800 subjects in the Russian study, and 1598 (88.8%) returned a completed questionnaire. Among these, 455 were at least 14 years old and were therefore excluded, leaving 1143 children for comparative analysis. The Russian questionnaire was answered by the child's mother in 82.0% of cases, by the father in 6.8%, by the child in 8.0%, and by others in 3.1%.

In both countries, the ratio of boys to girls was 1.0. In the statistical analysis, the children were distributed in six age groups according to school class. Because the children in the first class level (7–8 years) were on vacation by the time of the Russian study, these children represented only 5.0% of the Russian study population. The other five Russian age groups represented 16–22% each. In the Norwegian study population, the six age groups represented 15–18% each. The mean age of the Russian children (10 years) was higher than the Norwegian (9½ years) (P<0.001). The studies were based on informed consent by the parents, and the Norwegian Data Inspectorate gave the approval to file the questionnaires. The surveys were also approved by the ethics committee of northern Norway and the Regional Health Administration of Murmansk County. All statistics, including Cochran-Mantel-Haenszel statistics for 2×2 tables and linear regression, were computed by the SAS software package (12).

Definitions

An affirmative answer to the question, “Has the child ever had asthma?”, will be referred to as diagnosed asthma. With the question, “Does the child suffer from wheeze, periods with cough, or attacks of shortness of breath (asthma) caused by external factors?”, the questionnaire encouraged respondents to indicate what causes were responsible among the following six: animals, grass, infections, changes in weather, food, and other (external factors). AR was defined as episodic rhinorrhea associated with nasal stuffiness and sneezing in response to known or strongly suspected allergens and often accompanied by itching and lacrimation. AD was recorded in the cases of itchy eruption lasting for more than 4 weeks combined with either lesions in the face, elbow, or knee flexures, or a high degree of itching and lesions elsewhere.

Validity of the questionnaire

The questionnaire was used to assess atopic diseases among schoolchildren in Telemark County and Sør-Varanger Community, Norway (9, 13–15). Clinical follow-up studies showed that the sensitivity and the specificity of the questionnaire were high. It was concluded that the questionnaire was a useful epidemiologic tool.

Results

The prevalence of diagnosed asthma was highest in the Norwegian study population, and the relative risk was of the same magnitude for boys and girls (Table 1). On the other hand, the highest prevalence of all respiratory symptoms was found in the Russian study population. The difference between the study populations was greatest in children with symptoms of asthma without the children being recognized as asthmatics. Furthermore, the greatest difference in prevalence of respiratory symptoms was found between Russian and Norwegian girls. The prevalence of AR was highest in Norwegian children although the difference between the study populations was restricted to boys. Moreover, the prevalence of AD was highest in Norwegian children, both boys and girls. In Table 2, the prevalence of diagnosed asthma, AR, and AD in the two study populations is shown by age and presented by sex. The prevalence of diagnosed asthma increased with age in both Russian and Norwegian girls. With the exception of Russian boys, the prevalence of AR increased with age, and the increase was greatest in Russian girls. The prevalence of AD decreased with age in Russian boys, and in both girls and boys of the Norwegian study population. Symptoms caused by exposure to animals and grass were more frequently reported in Norwegian than Russian children with external provoked asthma (Table 3). On the contrary, more Russian than Norwegian children experienced asthma caused by changes in the weather. Among the children with asthma symptoms caused by external factors, 52% of the Russian and 76% of the Norwegian had either AR or AD (P<0.001). Furthermore, among these same children, 32% of the Russian and 58% of the Norwegian had a mother or father with either asthma, AR, or AD (P<0.001).

Table 1.  Prevalence of diagnosed asthma, respiratory symptoms, allergic rhinoconjunctivitis, and atopic dermatitis in Russian and Norwegian schoolchildren; relative risk (RR) and corresponding 95% confidence interval (CI)
 Prevalence (%)Prevalence in boys (%)Prevalence in girls (%)
 CountryRussia/NorwayCountryRussia/NorwayCountryRussia/Norway
 RussiaNorwayRR195% CIRussiaNorwayRR295% CIRussiaNorwayRR295% CI
  1. 1 RR adjusted by age and sex.
    2 RR adjusted by age.

Diagnosed asthma
 5.18.60.58(0.44–0.76)6.010.50.57(0.40–0.81)4.26.80.60(0.39–0.91)
Wheeze, periods with cough or attacks with shortness of breath (asthma) caused by external factors?
 16.310.61.52(1.30–1.79)15.412.01.26(1.00–1.59)17.39.21.86(1.48–2.32)
Periods with shortness of breath and wheezing and/or episodes with dyspnea without this being recognized as asthma?
 35.313.72.58(2.32–2.87)36.915.72.33(2.02–2.70)33.711.82.91(2.49–3.40)
Periods with cough without having cold?
 42.720.72.08(1.90–2.28)42.222.51.89(1.67–2.15)43.118.92.30(2.03–2.62)
Episodes with shortness of breath?
 24.512.41.95(1.71–2.21)26.814.41.85(1.56–2.19)22.110.52.08(1.72–2.52)
Wheeze or more dyspneic compared to children of same age during exercise or in raw, cold air?
 12.78.61.42(1.18–1.70)13.09.51.34(1.04–1.72)12.57.81.52(1.17–1.97)
Allergic rhinoconjunctivitis
 16.922.10.74(0.65–0.85)15.925.50.62(0.51–0.75)17.818.90.91(0.75–1.10)
Atopic dermatitis
 7.419.70.38(0.31–0.46)7.116.60.43(0.32–0.57)7.622.60.34(0.26–0.44)
Table 2.  Prevalence (%) of diagnosed asthma, allergic rhinoconjunctivitis, and atopic dermatitis in Russian and Norwegian schoolchildren according to age, including rate of increase per class level and corresponding 95% confidence interval (CI) and P value
  Age (years)
  7–88–99–1010–1111–1212–13Rate of
change
95% CIP value
Diagnosed asthma
 BoysRussia4.35.06.35.39.05.20.4(−1.1–1.8)0.61
 Norway10.012.510.19.99.910.2−0.2(−0.8–0.3)0.46
 GirlsRussia3.92.01.05.75.87.31.3(0.1–2.5)0.03
 Norway5.16.75.88.46.98.10.5(0.1–1.0)0.02
Allergic rhinoconjunctivitis
 BoysRussia23.813.814.617.322.89.8−0.4(−2.6–1.8)0.73
 Norway23.521.125.426.228.129.91.5(0.7–2.3)<0.001
 GirlsRussia12.012.912.416.227.423.23.3(1.1–5.6)<0.01
 Norway13.919.519.420.320.021.01.1(0.4–1.8)<0.01
Atopic dermatitis
 BoysRussia13.08.37.98.84.92.5−1.5(−3.0–0)0.05
 Norway17.118.817.915.616.113.1−0.8(−1.5 to −0.2)0.01
 GirlsRussia11.17.87.66.52.113.80.2(−1.3–1.7)0.80
 Norway23.524.523.323.521.718.8−0.9(−1.6 to −0.2)0.02
Table 3.  External factors associated with affirmative answer to question, “Does child suffer wheeze, periods with cough, or attacks of shortness of breath (asthma) caused by external factors?”, relative risk (RR), and corresponding 95% confidence interval (CI)
 Prevalence (%)Prevalence in boys (%)Prevalence in girls (%)
 CountryRussia/NorwayCountryRussia/NorwayCountryRussia/Norway
 RussiaNorwayRR195% CIRussiaNorwayRR295% CIRussiaNorwayRR295% CI
  1. 1 RR adjusted by age and sex.
    2 RR adjusted by age.

Animals11.051.50.21(0.15–0.29)12.350.90.24(0.16–0.38)9.852.30.18(0.11–0.29)
Grass7.739.10.20(0.13–0.30)11.041.50.26(0.16–0.45)4.936.10.13(0.06–0.25)
Infections31.029.01.07(0.82–1.38)31.525.81.36(0.92–2.01)30.533.10.98(0.69–1.41)
Changes in weather37.427.61.37(1.08–1.75)39.728.81.38(0.99–1.93)35.426.01.36(0.96–1.93)
Food12.914.00.92(0.60–1.43)17.813.11.33(0.76–2.33)8.515.20.60(0.29–1.24)
Other factors29.028.61.02(0.78–1.33)28.825.21.10(0.74–1.64)29.332.80.89(0.62–1.29)

Discussion

The present comparative prevalence study of asthma, respiratory symptoms, and allergy in Russian and Norwegian schoolchildren revealed higher prevalences of diagnosed asthma, AR, and AD in the Norwegian study population. However, generally, the prevalence of asthma symptoms caused by external factors and respiratory symptoms was higher in the Russian study population.

The method of translation of the Norwegian written questionnaire into Russian was not standardized according to the guidelines adopted for ISAAC (4). However, the translation involved two independent translators both familiar with the terminology of the questionnaire. Some language disagreement is inevitable, particularly in questions concerning wheeze. The public awareness of asthma may well differ in Russia and Norway. In addition, cultural differences in the threshold of reporting symptoms and the opinion of the stigma of disease may have been a source of bias. The studies we compared did not include a clinical examination, respiratory function measurements, skin prick tests, and blood specimen sampling for serum IgE and the radioallergosorbent test (RAST). Consequently, no objective measurements were available with which to label children with BHR or IgE-mediated allergy.

The prevalence of asthma is higher in boys than girls during childhood, but the sex differences in prevalence are reversed in adolescence (16, 17). In our study, this trend seemed to exist for diagnosed asthma in both Russia and Norway. The prevalence of AR is known to increase throughout the school years, as observed in our study, with the exception of Russian boys (18). The peak incidence of AD is in the pre-school age, and cessation of symptoms before adolescence is common (19). The observed decrease in AD prevalence with age in Russian boys and Norwegian children may represent an actual increase in prevalence in the youngest children. However, another explanation is simply that the AD symptoms were left out in many cases of older children who had recovered from a modest eruption many years prior to the study.

Asthma symptoms due to aeroallergens from animals and grass were more often reported in the Norwegian children. On the contrary, changes in weather provoked symptoms in a higher proportion of Russian children. In 1992, the emissions from the nickel smelters in Nikel and the neighboring city of Zapolyarny were about 260 000 t of SO2 (20). The episodes with highest air pollution in the vicinity are due to meteorologic conditions characterized by high atmospheric pressure and slow ground wind during the winter (21). Among the subjects with asthma symptoms caused by external factors, the prevalence of atopic diseases in both children and parents was highest in Norway. Among the Russian children, asthma symptoms caused by external factors predominated in girls. Asthma can be divided into two forms, allergic and nonallergic, and the diagnosis of the latter is primary based upon exclusion criteria, i.e., the absence of demonstrable allergy (22, 23). Nonallergic asthma is more prevalent in girls than in boys (23, 24). Like occupational asthma, nonallergic asthma is characterized by an increased number of CD8+ cells in the airway wall (24). Many epidemiologic studies have described symptom exacerbation in subjects with asthma or chronic obstructive respiratory disease in response to environmental SO2 (25–27). A prevalence study of BHR, as determined by several methods, was conducted among Estonian schoolchildren (28). It was concluded that most children with BHR in Estonia were not atopic, in contrast to studies in Western Europe. In summary, the high prevalence of asthma symptoms caused by external factors in the Russian study population is likely to reflect a high prevalence of nonallergic asthma. Necessarily, estimating asthma prevalence in epidemiology depends on whether nonallergic asthma is labeled asthma. Consequently, we suggest that a nonallergic/allergic asthma prevalence ratio be employed when asthma prevalence in Western and Eastern Europe is compared.

Acknowledgments

We thank the following Russian colleagues for excellent handling of the questionnaires in Nikel: Alexander Duriagin, Irina Zhivakova, and Leonid Zhivakov. The translation of the questionnaire into Russian and the back-translation into Norwegian of the answers were expertly done by Knut Ivedal and Anne Sofie Furberg. Economic support for the Russian part of the project was provided by the University of Tromsø steering groups of medical research in Nordland and Finnmark, together with the Barentssecretariate, Kirkenes, Norway.

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