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Background: Protection against thrips, a common pest in bell pepper horticulture is effectively possible without pesticides by using the commercially available predatory mite Amblyzeius cucumeris (Ac). The prevalence of sensitization to Ac among exposed greenhouse employees and its clinical relevance was studied.
Methods: Four hundred and seventytwo employees were asked to fill in a questionnaire and were tested on location. Next to RAST, skin prick tests (SPTs) were performed with common inhalant allergens, the storage mite Tyrophagus putrescentiae (Tp) which serves as a temporary food source during the cultivation process and Ac. Furthermore, nasal challenge tests with Ac were carried out in 23 sensitized employees.
Results: SPTs positive to Ac were found in 109 employees (23%). Work-related symptoms were reported by 76.1%. Sensitization to Tp was found in 62 employees of whom 48 were also sensitized to Ac. Immunoglobulin (Ig)E-mediated allergy to inhalant allergens appeared to be an important risk factor for sensitization to Ac. Employees with rhinitis symptoms showed a significantly higher response to all Ac doses during the nasal challenge test compared with employees without rhinitis symptoms.
Conclusions: The predatory mite Ac is a new occupational allergen in horticulture which can cause an IgE-mediated allergy in exposed employees. It is biologically active on the mucous membranes of the nose and therefore clinically relevant for the development of work-related symptoms.
The Netherlands count approximately 1150 hectares of sweet bell pepper horticulture. One of the major pests of this greenhouse crop is thrips. The most common thrips species are Frankliniella occidentalis and Echinothrips americanus (1). Especially the Frankliniella can cause tremendous damage to the plants, by feeding and as a consequence of transmission of viruses. Chemical control proved to be undesirable for environmental reasons and because of its interference with the biological control of other pests. Hence, an effective biological control agent of this thrips species was needed. From the various groups of natural enemies that can be used, the predatory mite Amblyseius cucumeris (Ac) appeared to be very successful (2, 3). This predatory mite was introduced in bell pepper greenhouses in 1985 and their use for year-round biological control has been stimulated ever since. In the past few years, an increasing number of allergic complaints seem to have appeared among employees of bell pepper greenhouses. A comprehensive study among 472 employees revealed that work-related symptoms in bell pepper horticulturists are highly prevalent (53.8%) and strongly associated with exposure to the bell pepper pollen (MS in preparation). However, not all symptoms could be explained by an IgE-mediated response to this occupational allergen and the question remains what may have caused the work-related symptoms in nonsensitized employees. Very few reports on sensitization to Ac or an antigenic relation between the common house dust mite Dermatophagoides pteronyssinus and the predatory mite Ac are found in scientific literature. However, it can be hypothesized that an elevated exposure to Ac as currently observed in bell pepper greenhouses might lead to sensitization as well as subsequently to work-related symptoms in sensitized employees.
Ac belongs to the order of mites (Acari), the suborder Mesostigmata, the family of the Phytoseidae, and the genus of Neoseiulus. It represents its own species. Taxonomically, the Ac mite is very different from the house dust mites or storage mites (Table 1). Four generation stages, from eggs to the adult animals pass through during the cultivation process which takes place together with the Tyrophagus putrescentiae (Tp). This storage mite, belonging to the Acaridae family, serves as a food source for nymphs and adult animals until the first weeks after their introduction into the crop. This usually happens a few weeks after planting. When the Tyrophagus mites are no longer available, Ac starts actively to search for thrips. The predator population can be maintained throughout the year without reintroductions. This persistence, which occurs even in absence of thrips, may be attributed to the presence of bell pepper pollen as an alternative food source. The microclimate of the leaf surface of the bell pepper plant is mostly of such quality that low air humidity during frost periods and on bright summer days does not affect their predation rate. The species used nowadays shows a total absence of diapause, so that year-round effective biological control is now provided.
Table 1. Classification of Amblyseius cucumeris and its relation to the storage mite Tyrophagus putrescentiae and the house dust mite Dermatophagoides pteronyssinus
The aim of this study was to estimate the prevalence of sensitization to Ac and the clinical relevance of sensitization.
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- Material and methods
The predatory mite Ac appears to be an important occupational allergen in bell pepper horticulture next to the bell pepper pollen. As many as 23% of the greenhouse employees in this study showed a positive SPT result to this mite. In these sensitized employees work-related symptoms were highly prevalent (76.1%), the main symptoms being rhinitis and conjunctivitis in 71.6% and 48.6%, respectively. Local dermatitis and asthma, the most serious manifestation of an occupational allergy, were reported to a lesser extent, in 26.6% and 25.7%, respectively. As in the case of high-molecular-weight agents, rhinoconjunctivitis is often more pronounced and may precede the onset of symptoms of the lower airways in exposed subjects (11). The prevalence rate of sensitization to Ac in this study was in accordance with previous recent studies on occupational allergies caused by mites: the citrus red mite (Panonychus citri), a common pest in citrus trees, was found positive in 16.5% of 181 citrus farmers (12) while the European red mite (Panonychus ulmi) and the two-spotted spider mite (Tetranychus urticae), common pests in apple orchards, were positive in 23.2% and 16.6%, respectively, of 725 apple-cultivating farmers (13). To our knowledge, this is the second study in which work-related symptoms are related to mites that are deliberately introduced into the working environment. A recent preliminary report by van Hage-Hamsten et al. revealed that cucumber-cultivating greenhouse workers, who use predatory mites for biological crop protection, may be at risk for occupational allergy to these mite species (14).
Sensitization to high-molecular-weight allergens is known to occur at a higher rate among atopic individuals (15–18). In this study 81 (74.3%) of the 109 employees sensitized to the Ac mite were also sensitized to one or more common inhalant allergens. The sensitization rate to Ac was significantly higher in atopic employees than in nonatopic employees, illustrating a clear association between sensitization to Ac- and IgE-mediated allergy to inhalant allergens (PRR 4.82; 95% confidence interval (CI) 3.27–7.10). Of all common inhalant allergens sensitization to the house dust mite and grass pollen were most prevalent in our study population as well as in our subgroup of Ac-sensitized employees. The association between sensitization to house dust mite and sensitization to Ac (PRR 4.08; CI 2.96–5.62) was stronger than the association between grass pollen and Ac (PRR 2.56; CI 1.87–3.50). Although sensitization to the house dust mite was most prevalent and more marked with sensitization to Ac than the other inhalant allergens, the positive skin reactions do not necessarily reflect cross-sensitization to Ac. The house dust mite is known to be one of the most common sensitizing allergens in the Netherlands. Moreover, there is no close taxonomic relationship between the two mites, which also reduces the probability of cross-allergy. Sensitization to Tp was in most cases associated with sensitization to Ac (77.4%, PRR 5.20). This storage mite only serves as a temporary food source for Ac, is normally not common in greenhouses and also has no close taxonomic relation with Ac. It can be supposed that the positive SPT results to Tp found in this study might be owing to the presence of Tp in commercially available Ac mites. Furthermore, sensitization to Tp was also strongly associated with sensitization to house dust mite (PRR 8.20). Cross-reactivity between these two mites has been described in a previous study (19). Of the 64 employees sensitized to Ac and house dust mite, 38 (59.4%) showed a concomitant sensitization to Tp. Because of the fact that all three mites are closely associated to each other, it is not possible to draw any further conclusions. Although from our investigations an independent sensitization to Ac might be suspected, crossreactivity between Ac and Tp and between Ac and D. pteronyssinus, respectively, cannot be excluded. Further investigation by means of RAST inhibition tests and immunoblot analyzes is necessary and under way.
The biological activity of Ac on human mucous membranes, in particular those of the nose, and the consequent clinical-allergological relevance of sensitization could be confirmed by nasal challenge tests. When comparing the clinical response in employees with and without rhinitis complaints, the former showed a significantly higher clinical response at all Ac concentrations. Furthermore, there was a significant difference in the nasal reactivity between the rhinitis+ and the rhinitis– group, with a higher response in the rhinitis+ group. This difference was not revealed by the skin reactivity to Ac in the SPT, which implies that a nasal challenge test with Ac is a better and more sensitive test for discrimination between sensitized employees with and without rhinitis.
It is difficult to single out the specific effect of Ac in an occupational population with a high exposure and consequent sensitization to bell pepper pollen and/or plant. Hence, it is also difficult to predict whether intervention strategies focused on the contribution of bell pepper pollen and plant will be more beneficial than those aimed at reduction or elimination of the use of Ac. This is, however, important to know when possible solutions for exposure intervention are considered and should therefore be a subject for further research. The described results of this study may have consequences for the extensive use of biological control in horticulture nowadays. In the knowledge that indoor as well as outdoor mites are a frequent cause of allergic diseases, the use of predatory mites as biological control agents should be critically evaluated. Furthermore, the benefits of biological control should be weighed carefully against the increased risk of employees developing an occupational allergy.
In conclusion, the predatory mite Ac is a new occupational allergen in horticulture which cause an IgE-mediated allergy in exposed employees. It is biologically active on the mucous membranes of the nose and therefore clinically relevant for the development of work-related symptoms.