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Keywords:

  • asthma;
  • epidemiology;
  • hay dust;
  • IgE;
  • Lepidoglyphus destructor;
  • skin test

Abstract

  1. Top of page
  2. Abstract
  3. Material and methods
  4. Results
  5. Discussion
  6. Acknowledgments
  7. References

Background: The aim of this study was to estimate the prevalence of IgE-mediated allergy to Lepidoglyphus destructor and its clinical importance in Reykjavík, Iceland.

Methods: All Icelandic participants in the European Community Respiratory Health Survey in Reykjavík and suburbs were skin prick tested (SPT) for L. destructor. They also participated in a structured interview including questions about exposure to hay and symptoms related to hay exposure. Spirometry and methacholine tests were also performed.

Results: Altogether, 540 individuals underwent SPT with 12 allergens. Among them, 137 (25.4%) had positive skin tests, defined as at least one mean wheal reaction of ≥1 mm. By this definition, 34 (6.3%) were positive to L. destructor. These 34 individuals were significantly (P<0.001) more often allergic to D. pteronyssinus (24/34), grass (14/34), cat (13/34), dog (12/34), Alternaria (11/34), Cladosporium (9/34), horse (8/34), and olive (8/34) than those not allergic to L. destructor. Those SPT positive to L. destructor had a higher total IgE (geometric mean: 40.9 kU/l vs 12.3 kU/l, P<0.001) than those who were negative to L. destructor, but their lung function was comparable to that of the others. Asthma during the preceding 12 months or asthma ever suffered was not overrepresented among those SPT-positive to L. destructor. Individuals with symptoms associated with hay exposure were more often SPT positive to L. destructor than those not having symptoms (P<0.01).

Conclusions: In a random urban population, 6.3% showed IgE-mediated allergy to L. destructor. These were often polysensitized atopics with a high prevalence of clinical symptoms associated with exposure to hay.

Diseases related to exposure to hay dust have been known for centuries in Iceland (1). The first publication on respiratory symptoms related to inhalation of hay dust appeared in 1790. A few years later, another publication described a case of chronic obstructive lung disease as a consequence of long-lasting exposure to hay dust (1). In the second half of the 20th century, hay-related complaints were still common in Iceland, especially among farm workers (2).

In 1979, Cuthbert et al. were the first to report allergy to storage mites in Scottish farm workers exposed to hay and grain used to feed cattle wintered indoors (3). Subsequent studies of farmers in Finland, Sweden, the UK, and Denmark have confirmed the importance of storage mites in causing allergic symptoms among farm workers (4–7). Allergies to storage mites have also been reported to be a problem among grain handlers and bakers (8, 9), but others have not found an increased prevalence of allergy to storage mites in bakery workers (10, 11). Tee et al. concluded that storage mites were probably widespread in the general environment and that allergy to them among bakery workers was not only a consequence of exposure at work (10).

Several authors have reported positive results of skin prick tests (SPT) to Lepidoglyphus destructor in selected urban populations with atopic symptoms such as asthma and rhinitis (12–14). We are not aware of such study on a random sample of an urban population. Our previous experience had shown sensitization to L. destructor to be the most common cause of IgE-mediated allergy among Icelandic farmers (2). The aim of this study was to estimate the prevalence of IgE-mediated allergy to L. destructor in a randomly selected urban population and to assess its clinical importance.

Material and methods

  1. Top of page
  2. Abstract
  3. Material and methods
  4. Results
  5. Discussion
  6. Acknowledgments
  7. References

Study design and methods

This study is partly based on the protocol used in the European Community Respiratory Health Survey (ECRHS) (15). It was performed on the population in Reykjavík, Iceland, and suburbs (160000 inhabitants) in 1991–2. In the first stage of ECRHS, a sample of 1800 men and 1800 women aged 20–44 years, was randomly selected from the national population register to receive a postal questionnaire. In the second stage, another random sample of 800 individuals was selected from the study population of 3600 and invited to participate in further investigation. The present analyses are based on the results of the second stage.

Questionnaire

The main questionnaire used in the second stage was the ECRHS modified version of the International Union Against Tuberculosis and Lung Disease (IUATLD) questionnaire on symptoms and medical history (16). In our center, there were additional questions about the handling of stored hay or exposure to hay dust ever in life (brought up on a farm, living as farmer, having farm vacations, or keeping a horse). There were also questions about clinical symptoms related to hay exposure.

Allergy tests

The standard list of allergens that were selected for use in all ECRHS study areas included cat, house-dust mite (Dermatophagoides pteronyssinus), timothy grass, birch, Cladosporium herbarum, Alternaria, olive, common ragweed, and Parietaria judaica.

Each study area could select three allergens of local importance. In Iceland, we chose dog, horse, and L. destructor. Skin prick testing (SPT) was carried out according to the ECRHS protocol described previously (15–18), with Phazets (Pharmacia Diagnostics AB, Uppsala, Sweden), which are lancets precoated with standardized lyophilized extracts. Histamine was used as positive control and uncoated lancets as negative controls. We used glycerinated extract for L. destructor (Allergologisk Laboratorium, Denmark).

All SPTs were performed by two experienced nurses. Wheal size was recorded 15 min after application of the antigens by circling the reaction with a pen and transferring it to a test form with adhesive tape. The wheal diameter was calculated as the mean of the widest diameter and the perpendicular diameter measured at its midpoint.

Total IgE

Venous blood samples were drawn and frozen at −20°C for measurement of total serum immunoglobulin E (total IgE), as part of the ECRHS protocol (15). The analyses were performed at Pharmacia Diagnostics AB, Uppsala, Sweden, by the Pharmacia CAP System (19). The cutoff for total IgE was 2 kU/l.

Spirometry

The spirometer used was a computerized Sensor Medics 2450 (Anaheim CA, USA). The examination was delayed for 1 h if participants had smoked during the preceding hour, and at least for 1 week if they had symptoms of respiratory infection. Use of the short-acting β2-agonists/anticholinergic inhaler was not allowed during the preceding 4 h before the test. Long-acting β2-agonists were not in use at the time of the study.

Bronchial hyperresponsiveness (BHR) was measured with methacholine (Provocholine R from Hoffman La Roche). The subjects inhaled methacholine dilutions with a Mefar MB3 inhalation dosimeter (Bresica, Italy). A 20% or more drop in FEV1 was defined as a positive methacholine test. Before the subjects inhaled the methacholine dilutions up to the upper limit of 2 mg/ml, they inhaled a saline solution, and if there was a drop of 20% or more in FEV1, the test was canceled. This protocol has been described in detail elsewhere (20).

Statistics

Mean values and one standard deviation (±SD) were used for continuous variables and the two-sided t-test for comparison. IgE values are presented as geometric means. The chi-square test was used for comparison of groups.

Results

  1. Top of page
  2. Abstract
  3. Material and methods
  4. Results
  5. Discussion
  6. Acknowledgments
  7. References

Study participation

Of the 800 randomly selected subjects, 56 had moved away and one had died. Altogether, 570 (77%) participated, but to different degrees: 545 answered the questions about hay-dust exposure, 540 agreed to SPTs of the test panel of 12 allergens (49% men), and 519 subjects both answered questions about hay dust and underwent the SPTs.

SPT results

In all, 137 (25.4%) had a positive SPT to at least one allergen (wheal reaction of ≥1 mm) (Table 1). Grass, D. pteronyssinus, dog, and cat were the most common offending allergens with positive SPTs of 12.8%, 10.9%, 10.7%, and 10.6%, respectively. Seventeen subjects had a mean diameter of ≥3 mm when tested for L. destructor, 14 had ≥2 to <3 mm, and three had ≥1 to <2 mm; altogether, 34 (6.3%) were positive to L. destructor. These 34 subjects had positive skin tests significantly (P<0.001) more often for D. pteronyssinus (24/34), grass (14/34), cat (13/34), dog (12/34), Alternaria (11/34), Cladosporium (9/34), horse (8/34), and olive (8/34) than those SPT negative to L. destructor. Among the 24 individuals with a positive reaction to both L. destructor and D. pteronyssinus, there was a correlation between the wheal sizes (r=0.404, P=0.05).

Table 1.  Results of 540 skin prick tests (SPTs)
AllergenMean wheal diameter ≥1 mm %Mean wheal diameter mm±1 SD
Timothy grass12.85.0±3.5
D. pteronyssinus10.93.1±1.7
Dog10.73.4±1.8
Cat10.64.4.±2.5
L. destructor6.32.7±0.9
Birch5.63.7±2.9
Horse3.72.6±2.5
Alternaria3.72.3±1.0
Cladosporium3.52.2±0.8
Olive3.42.0±0.9
Ragweed3.41.7±0.6
Parietaria2.61.8±0.9
At least one positive skin reaction25.4 

Exposure to hay dust and symptoms

Altogether, 296 answered yes to the question, “Have you ever handled hay or been exposed to hay dust?” Sixty-nine percent of all men and 41% of all women answered yes to this question (P<0.001).

A positive SPT to L. destructor was found among 22 (7.8%) of those exposed to hay dust compared to 12 (5%) of those never exposed (P<0.02) (Table 2). Those with various causes of hay-dust exposure were also compared to those without exposure for SPT results to L. destructor. Frequent farm vacations, having been brought up on a farm, and feeding horses were associated with a higher prevalence of SPT than nonexposure, but the difference was significant only for those feeding horses (P<0.05). One ex-farmer was found in the cohort. He had a negative SPT to L. destructor. Eighteen individuals cited other causes of hay-dust exposure, of whom two had positive SPT to L. destructor.

Table 2.  Positive SPTs to L. destructor in relation to exposure to hay dust
Kind of exposure (n=number)Prick test ≥1 mm %
  1. *P<0.05, **P<0.02.

Never exposed to hay dust (n=238)5.0
Ever exposed to hay dust (n=279)7.8**
Frequent farm vacations (n=210)7.6
Brought up on farm (n=54)9.3
Feeding horses (n=34)14.7*

Those exposed to hay dust were asked additional questions about symptoms associated with hay-dust exposure (cough, tightness in the chest, nose symptoms, and eye symptoms). These symptoms were all more prevalent among men than women, but the difference was only significant for symptoms of the nose and eyes (P<0.05).

Of 296 individuals who had been exposed to hay dust, 279 answered questions about symptoms and also underwent SPT. Sixty (21.5%) reported one or more clinical symptoms while in a barn (Table 3). The rate of positive SPTs to L. destructor was significantly higher among those with symptoms than those exposed but without symptoms (P<0.01). The mean wheal reaction for L. destructor in those with symptoms compared to those without symptoms was 0.575 mm±1.34 vs 0.122 mm±0.54 (P=0.0001).

Table 3.  Positive SPT to L. destructor (%) in relation to reported symptoms felt in barns
Symptoms (n=number)Prick test ≥1 mm %
  1. *P<0.05, **P<0.01, ***P<0.001.

Answered questions about symptoms (n=279)7.8
Some symptom(s) reported (n=60)16.7**
Symptoms in barns
 Cough (n=27)22.2*
 Tightness in chest (n=19)31.6***
 Nose symptoms (n=42)21.4***
 Eye symptoms (n=25)32.0***

Total IgE

Blood samples for total IgE were taken with permission from 521 individuals. Those with positive SPT to L. destructor had a higher total IgE (geometric mean 40.9 kU/l vs 12.3 kU/l) than those with negative SPT to L. destructor (P<0.001).

Lung function and respiratory symptoms

The lung function (FEV1%predicted) was the same for those with positive SPT to L. destructor as those with negative SPT to L. destructor (104%vs 105%). Wheezing during the preceding 12 months was not significantly more common among those with positive SPT to L. destructor than among those with negative SPT to L. destructor. On the contrary, ever having had asthma was more commonly reported among those with positive SPT to L. destructor (P<0.02) than among others.

Altogether, 474 were tested with methacholine (others were excluded or refused to participate in the test); of them, 41 had a 20% fall in FEV1 after inhaling 2 mg or less of methacholine, thus showing signs of BHR. There were 28 with positive SPT to L. destructor tested with methacholine, of whom four had signs of BHR (14.3% compared to 8.6% of all tested, P=0.28).

Discussion

  1. Top of page
  2. Abstract
  3. Material and methods
  4. Results
  5. Discussion
  6. Acknowledgments
  7. References

In this study, we used a cutoff limit for a positive SPT of ≥1 mm, which was the smallest positive skin response recorded in the study. In epidemiologic studies, positive SPT results have been expressed as wheal size from >0 to 5 mm or at least half the histamine wheal diameter. In a newly published study, a cutoff of >0 mm for positive results gave a more consistent relation to the corresponding specific IgE value than either a cutoff of ≥3 mm or the use of the mean wheal diameter (21). In our study, an SPT reaction of ≥1 mm to L. destructor had a good correspondence with the symptoms reported from hay dust (P<0.01).

Compared to results from other ECRHS centers, the mean total serum IgE in our study area is the lowest reported (22). The prevalence of positive SPTs in our area was also relatively low (22). Compared to other allergens, L. destructor is of importance even in the urban population of Iceland and should be included in a standard SPT panel.

How far these results reflect the situation in urban populations in other countries is uncertain. A surprisingly large number of participants in the study had been exposed to hay dust at some period in their lives. That is probably unique to the urban population in Iceland. Of those never exposed to hay dust, 5% were SPT positive to L. destructor, a figure higher than for half of the allergens tested in this study.

The hay harvest season is very short in Iceland, only 2 months, and rainy weather makes drying the hay difficult, often leaving wet pockets in the harvested hay.The average relative humidity of air at that season is 78–84%, a level at which the hay tends to equilibrate when stored in the barns (23). Storage mites flourish in such an environment. Nine-teen different species of storage mites have been described in the hay in Iceland, and L. destructor was found in 83% of all hay samples, sometimes in very high numbers (24).

In a previous study of farmers' families in two communities in Iceland, a third of the study population had some hay-related symptoms in the eyes and respiratory tract, and 38% of those with symptoms had positive SPT to L. destructor, with ≥2 mm as the cutoff limit for positive tests (2).

Although this study was carried out on a random urban population, 54% had had some previous history of exposure to hay dust. In Iceland, exposure to hay was very common among the urban population during the middle of this century because of farm vacations among the youngsters, especially boys. In many cases, this exposure was only sporadic and at an early age. Nowadays, horseback riding is increasing in popularity, with the horses mainly tended by men. This fact probably explains the more common exposure and greater prevalence of symptoms among men than women.

Being exposed to hay is a risk factor for sensitization to L. destructor, as seen in Table 2, even though the figures are significant only for those feeding horses, who thereby possibly experience the greatest exposure.

Our study found a relationship between symptoms and skin responses to L. destructor for all symptoms, and this result is in accordance with our earlier experience (2).

There was a strong correlation between skin responses to L. destructor and D. pteronyssinus, a finding which may express a cross-reaction between these allergens (25, 26) or multiple sensitization to different species of mites because of the home environment. No investigation has been carried out on the occurrence of mites in Icelandic homes.

Acknowledgments

  1. Top of page
  2. Abstract
  3. Material and methods
  4. Results
  5. Discussion
  6. Acknowledgments
  7. References

We thank the Ministry of Health of Iceland, the Icelandic Association of Tuberculosis and Chest Patients (SIBS), and the Icelandic Research Council for financial support for this study.

References

  1. Top of page
  2. Abstract
  3. Material and methods
  4. Results
  5. Discussion
  6. Acknowledgments
  7. References