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- Material and methods
Background: The risk of allergic disease may be influenced by the degree of “westernization”. A survey was conducted to ascertain whether the prevalence of allergy was lower in Albania than elsewhere in Europe, as it has been the most isolated European country.
Methods: The subjects were residents of Tirana aged 20–44 years. A screening questionnaire was completed by 2653 subjects. A more detailed questionnaire was administered to a random sample of 564 respondents, together with skin prick tests and serum IgE assay.
Results: The prevalence of wheeze in the last year, and of wheeze without a cold, was lower in Albania than in any country that participated in the European Community Respiratory Health Survey. Nasal allergy and atopy (as indicated by serum specific IgE) were also uncommon in Albania, although serum total IgE concentrations were high.
Conclusions: The findings confirmed the hypothesis of a low prevalence of allergy in Albania. Possible reasons include the recent economic isolation of Albania, the infrequency of smoking by women, the lack of domestic pets, and the high incidence of childhood infection and parasitic infestation. The prevalence of allergy and its potential determinants should be monitored in Albania as that country acquires the characteristics of other parts of Europe.
Material and methods
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- Material and methods
The subjects were residents of the administrative district of Tirana (total population 250219 in 1992) who were aged 20–44 years. The sampling frame was the electoral register that was drawn up in 1992, and a random sample of 60 electoral wards was drawn from the 224 wards in Tirana. Within the selected wards, a random sample was chosen of persons who were aged 20–44 years in December 1994. The consent of the local ethics committee was obtained, and the survey was conducted during 1995 and 1996.
The questionnaires were translated from the ECRHS originals into Albanian and independently back-translated into English; the Albanian versions were then corrected accordingly. The design of the study was broadly that of the ECRHS, except that spirometry and methacholine challenge were not performed. A short screening questionnaire was distributed to a random sample of the population of the specified age, enquiring about certain respiratory symptoms in the last 12 months, including wheezing, attacks of breathlessness, and asthma. This questionnaire also asked whether any treatment was currently being taken for asthma, and “Do you have any nasal allergies including ‘hay fever'?” The questionnaires were delivered by hand and completed on the spot, or left to be collected a few days later.
A random subsample of the respondents was asked to participate in a more detailed enquiry, involving administration of a longer questionnaire, skin prick tests for certain allergens, and blood tests for total and specific IgE. Similar investigations were conducted in all other subjects who reported certain symptoms in the screening questionnaire, but their results are not reported here. A further difference from the ECRHS procedure was the use of liquid antigen (supplied by SmithKline Beecham Pharmaceuticals) rather than precoated lancets. The fieldworkers were trained and their skin test results were monitored according to the ECRHS protocol. The allergens for the skin tests were house-dust mite (Dermatophagoides pteronyssinus), cat, grass pollen, Alternaria, Cladosporium, Parietaria, olive, ragweed, Artemisia, and Betula. A wheal of 1 mm or more was regarded as a positive reaction, in accordance with ECRHS recommendations ( 5). The blood samples were transported frozen to a laboratory in Cardiff, where the IgE assays were performed with the Pharmacia CAP System; specific IgE was tested for mite, timothy grass, cat, Parietaria, and olive.
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- Material and methods
There were 3670 subjects aged 20–44 years, randomly selected from 60 electoral wards, who appeared to be eligible for the survey. Of these, 2653 (72.3%) completed the screening questionnaire; this is an underestimate of the response rate, since many subjects had emigrated since the electoral register was compiled, and some addresses could not be located, so that the true denominator is not known. Table 1 shows the prevalence of various symptoms derived from the screening questionnaire. Being woken by breathlessness was the commonest symptom suggestive of asthma; only a quarter of these subjects reported an attack of asthma, and even less were receiving treatment for asthma. Nasal allergy was reported more often than wheezing or waking with breathlessness. All these symptoms had a higher prevalence in women than in men.
Table 1. Prevalence of symptoms in last 12 months according to screening questionnaire
|Symptom*||Men (n=1260) ||Women (n=1393) ||All subjects (n=2653) |
|Wheeze || 76|| 6.0||102|| 7.3||178|| 6.7|
|Wheeze with breathlessness [1.1]|| 58|| 4.6|| 88|| 6.3||146|| 5.5|
|Wheeze without cold [1.2]|| 30|| 2.4|| 49|| 3.5|| 79|| 3.0|
|Woken by breathlessness || 85|| 6.7||139||10.0||224|| 8.4|
|Attack of asthma || 16|| 1.3|| 40|| 2.9|| 56|| 2.1|
|Current treatment for asthma || 8|| 0.6|| 32|| 2.3|| 40|| 1.5|
|Nasal allergy ||132||10.5||198||14.2||330||12.4|
The prevalence of some of these symptoms was compared with that in countries that participated in the ECRHS ( 2). Fig. 1 shows the prevalence of wheeze in the last 12 months in Albania and the European ECRHS countries (some of which conducted the survey in more than one place); centres in southern Europe are shown separately, and the Algerian centre (Algiers) is also shown, as it has a Mediterranean location. The prevalence of wheeze was lower in Albania than in any other European centre, but slightly higher than that in Algeria; the next lowest prevalence rates were in the three Italian centres, all in northern Italy. The prevalence of nasal allergy in Albania was among the lowest in Europe, although it was lower still in Algeria ( Fig. 2).
The random subsample selected for further investigation comprised 598 subjects, of whom 564 (94.3%) were actually seen. Table 2 shows the prevalence of current tobacco smoking among these subjects classified by age. At all ages, smoking was far more common in men than in women. There was no obvious trend with age among the men, but in women the prevalence was highest in the oldest group. Smoking status was not recorded for one woman.
Table 2. Prevalence of current smoking by age group
|Age group (years) ||Men||Women||All subjects|
| ||no.||no. (%)||no.||no. (%)||no.||no. (%)|
|20–24|| 35|| 14 (40) || 44|| 0 (0) || 79|| 14 (18) |
|25–29|| 37|| 24 (65) || 65|| 1 (2) ||102|| 25 (25) |
|30–34|| 68|| 30 (44) || 69|| 5 (7) ||137|| 35 (26) |
|35–39|| 62|| 27 (44) || 75|| 4 (5) ||137|| 31 (23) |
|40–44|| 46|| 15 (33) || 62||10 (16) ||108|| 25 (23) |
|All ages||248||110 (44.4)||315||20 (6.3)||563||130 (23.1)|
Table 3 shows the prevalence of certain symptoms that were addressed in the detailed questionnaire. Subjects with “chronic cough” are those who answered “Yes” to both the following questions:
Table 3. Prevalence of certain symptoms in random subsample
|Symptom||Men (n=248) ||Women (n=316) ||All subjects (n=564) |
|Chronic cough||36||14.5||23|| 7.3||59||10.5|
|Chronic phlegm||55||22.2||23|| 7.3||78||13.8|
|Constant breathing trouble|| 5|| 2.0|| 5|| 1.6||10|| 1.8|
|Asthma ever||10|| 4.0||14|| 4.4||24|| 4.3|
“Do you usually cough during the day, or at night, in the winter?”
“Do you cough like this on most days for as much as 3 months each year?”
Similar questions defined “chronic phlegm”. These two symptoms were much more commonly reported by men than by women, whereas continuous breathing trouble, asthma ever, and eczema ever were reported to a similar extent by men and women.
The results of the skin tests are shown in Table 4. The house-dust mite was by far the allergen to which most people were sensitized, followed by grass pollen. Reactions to other allergens occurred in less than 5% of subjects. Among the 564 people seen, 58 (10.3%) owned a cat, 44 (7.8%) owned a dog, and 14 (2.5%) owned a bird.
Table 4. Prevalence of positive skin prick tests to individual allergens
| ||Subjects with positive skin tests (n=564) |
|Cat|| 16|| 2.8|
|Grass pollen|| 30|| 5.3|
|Alternaria|| 17|| 3.0|
|Cladosporium|| 16|| 2.8|
|Parietaria|| 14|| 2.5|
|Olive|| 19|| 3.4|
|Ragweed|| 17|| 3.0|
|Artemisia|| 22|| 3.9|
|Betula|| 15|| 2.7|
|Any of these||169||30.0|
Serum total IgE was measured in 229 men and 284 women. The geometric mean concentrations were 93 and 72 kU/l, respectively (81 kU/l overall). Tests for specific IgE for five allergens were performed on 502 serum samples, and the results are shown in Table 5. Mite was the allergen to which specific IgE antibodies most frequently occurred, followed by timothy grass.
Table 5. Prevalence of specific serum IgE to certain allergens
| ||Subjects with specific IgE (n=502*) |
|House-dust mite|| 76||15.1|
|Timothy grass|| 51||10.2|
|Cat|| 10|| 2.0|
|Parietaria|| 38|| 7.6|
|Olive|| 38|| 7.6|
|Any of these||114||22.8|
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- Material and methods
This is the first respiratory survey of adults to be conducted in Albania. The results allow comparisons to be made with data obtained in other countries, and they provide a baseline so that changes can be detected in the future as Albanians adapt to new political, economic, and cultural conditions. The survey took place in Tirana so as to be comparable with the ECRHS, which was mostly conducted in towns of at least 150000 inhabitants. Therefore, the findings do not necessarily apply to the population of the rural parts of Albania. Tirana has a Mediterranean climate, humid in spring and autumn, hot and dry in summer, and mild in winter. Since 1992, there has been some air pollution from an influx of diesel-fuelled cars, but little from industrial sources.
The response rate for the first part of the survey cannot be given precisely, owing to uncertainties about the denominator. A substantial movement of population out of Tirana occurred after the 1992 electoral register was compiled, and the apparent response rate of 72.3% was an underestimate of the true figure. The second part of the survey yielded a response of 94.3%, and it seems reasonable to believe that the participants were representative of young adults living in Tirana.
The most striking finding is perhaps the low prevalence of symptoms in comparison with rates in other European countries. Wheeze in the past year (and wheeze without a cold) was less commonly reported in Albania than in any other European country ( 2). Although it is difficult to exclude altogether the possibility of an artefact of translation, this is unlikely to be the whole explanation, since the prevalence of wheeze tended to be low in other southern European countries (Italy, southern France, and Greece), and it was lower still in Algeria. Asthma attacks and currently treated asthma were less frequently reported in Albania than in most other European centres ( 2); moreover, the prevalence of nasal allergy was low in Albania and Algeria, and fairly low in Italy, Spain, Portugal, and Greece, in comparison with the rest of Europe. It seems that allergic symptoms tend to affect a smaller proportion of the population in Mediterranean countries than in other parts of Europe. Similar findings have emerged from the International Study of Asthma and Allergies in Childhood (ISAAC). This showed that, among 56 participating countries, the mean prevalence of asthma symptoms in 13–14-year-old children was lower in Albania than anywhere else except Indonesia; it was lowest in Albania among the countries that used a video questionnaire, so this position was not a linguistic artefact ( 3). Albania also had the lowest prevalence of symptoms of allergic rhinoconjunctivitis and of atopic eczema in that survey.
The question arises as to why allergic diseases are relatively uncommon in Albania, among children and young adults. The explanation may lie in some aspect of Mediterranean life – for example, the high consumption of fresh fruit, since dietary antioxidants have been suggested as possibly conferring protection against allergy ( 6). Paradoxically, despite its poverty and high infant mortality rate, Albania has adult death rates that are comparable with those of its wealthier neighbours, with a life expectancy at age 15 years that is similar to that in other European countries, and the high intake of fruit and olive oil could account for the health of its adult population ( 7). Alternatively, there could be some adverse factor in the “western” lifestyle from which Albanians have hitherto been shielded by the isolation of their country. It is noteworthy that the prevalence of allergic asthma and of specific serum IgE antibodies is low in Estonia, another formerly socialist country, in comparison with Sweden ( 8). Studies in the former East and West Germany suggest that the prevalence of atopy and allergic disease was lower in the east until the reunification of the country but may now be converging with that in the west ( 9, 10). Relevant aspects of the western lifestyle may include housing conditions, pet ownership, diversity of foods, automobile exhaust emissions, and travel ( 11). Clearly, the prevalence of allergic disease (and of other conditions characteristic of western countries) should be monitored in Albania as its inhabitants increasingly acquire western ways.
The frequency of pet ownership was much lower in Albania than in other European countries. For example, surveys of children in the UK and Sweden have reported cat ownership in 28.5% and 22.7%, respectively, compared with 10.3% in this survey, with similar or greater disparities in the proportions keeping dogs and birds ( 12). It seems most unlikely that this is attributable simply to the difference in age group. Cat and dog antigens are important allergens in relation to clinical disease, and are widely dispersed within the community ( 13). The relative infrequency of pet ownership in Albania may contribute to the low prevalence of allergic disease there.
The relative importance of allergy to house-dust mite (as shown by both skin and serum tests) is striking. In most countries, grass-pollen allergy is nearly as important as mite allergy or still more so, but in Albania its frequency was very much lower. Cat allergy was even less common, reflecting the low prevalence of cat ownership and consequent lack of exposure of the population to cat antigen. Apart from grass, the pollens with the highest frequencies of positive reactions were Artemisia and olive, which are known to provoke allergic symptoms in Mediterranean countries ( 14). Serum specific IgE appeared to be a more sensitive indicator than skin tests for allergy to grass, Parietaria, and olive.
Objective evidence confirming the low prevalence of atopy in Albania is provided by the serum tests. The prevalence of atopy, as defined by specific IgE to any of the allergens tested, was 23%, placing Albania in the lowest quarter of atopy prevalence in the ECRHS ( 15). It is noteworthy that this quarter included Greece and some of the Italian and Spanish centres. The selection of allergens was nearly but not quite identical: Cladosporium was included in the ECRHS, but not in the Albanian survey. The skin tests showed that allergy to olive (included in the Albanian, but not the ECRHS, specific IgE tests) was more common than allergy to Cladosporium in Albania; therefore, the substitution is most unlikely to have reduced the relative prevalence artificially. The prevalence of mite-specific IgE was in the second lowest quarter of the ECRHS distribution; grass-specific IgE was in the lowest quarter, while cat-specific IgE was less common than in any ECRHS centre. In contrast, the geometric mean total IgE concentration was higher than that in any country participating in the ECRHS ( 15). The ECRHS country with the highest overall geometric mean IgE was Greece, so that Albania shares with its neighbour Greece a low prevalence of asthma, allergic diseases, and atopy, and a high serum total IgE. This association may reflect exposure to parasitic worms and Giardia. There is evidence to suggest that some protection against allergic diseases is conferred by helminth and other parasitic infections, despite the increase in IgE that they provoke, and also by other childhood infections ( 16). Among Italian military students, the prevalence of atopy (whether defined by skin tests or by specific IgE) was lower in those who had serum antibodies to hepatitis A virus than in those who did not, suggesting that childhood infections consequent on poor hygiene may reduce the risk of atopy ( 17). The high incidence of infections in childhood, reflected in the high infant mortality rate ( 7), may thus be at least a part of the reason for the low prevalence of allergic diseases in Albania.
Among the lifestyle factors that may change with “westernization” is cigarette smoking. The prevalence of smoking was 44% in men, with little variation across the age band in this survey, but only 6% in the women. The virtual absence of smoking in young women is in particular contrast to the pattern found in western Europe, although the prevalence may be underestimated, owing to possible reluctance to admit smoking. The excess prevalence of chronic cough and phlegm in men compared with women reflects the difference in smoking habits. Current symptoms of asthma were more common among women, however, and the lack of a sex difference for “constant breathing trouble” may represent a combination of two opposite tendencies. Maternal smoking has been implicated as a risk factor for asthma in some studies ( 18, 19), so the relative infrequency of cigarette smoking in Albanian women could be a factor in the low prevalence of asthma in that country.
It is clear that the prevalence of allergy in Albania is low compared with that in most other European countries. If the situation is monitored as the country undergoes rapid changes, clues may emerge about the causes of its relative freedom from allergic diseases hitherto and the increases that have occurred elsewhere.