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Prevalence of fungal sensitization and atopy was lower among farmers than the US population. Fungal sensitization was related to growing specific agricultural commodities.
To the Editor:
Farm work may result in exposure to microbial bioaerosols. In agriculture, average airborne concentrations of fungal conidia are several orders of magnitude higher than in nonagricultural, indoor environments without water damage. 1 We used data from Iowa (IA) and North Carolina (NC) farmers to explore associations between farming activities and fungal sensitization.
We analyzed serum samples from a neurobehavioral sub-study of 677 male private pesticide applicators in the Agricultural Health Study (AHS). 2 Blood was collected from male pesticide applicators in 2006-8 who had completed all AHS interviews. Blood samples were not available for the whole cohort. Individuals were excluded if they had never been a farmer or had neurologic diseases; women were excluded due to their low prevalence in the cohort (<3%). 2 Participants in the sub-study were similar to the cohort as a whole with regard to farm history (Hoppin et al submitted). The study was approved by Institutional Review Boards of the University of Iowa, the National Institutes of Health and its contractors.
Serum samples were analyzed for total immunoglobulin E (tIgE) and screened for fungal positivity to a fungal-mix (mx2) by fluoroenzymeimmunoassay using ImmunoCAP 100 (Phadia AB, Uppsala, Sweden). Sensitization to other allergens was not measured. If sera were fungal- mix positive, they were tested for sIgE to ten fungal species (Aspergillus fumigatus, Penicillium chrysogenum, Alternaria alternata, Curvularia lunata, Epicoccum purpurascens, Phoma betae, Candida albicans, Botrytis cinerea, Fusarium proliferatum, and Cladosporium herbarum). Fungal sensitization was defined sIgE ≥ 0.35 kU/L to at least one fungus; atopy was defined as tIgE ≥ 100kU/L. 3
Pesticide applicators completed three questionnaires about their agricultural and medical history: one at enrollment and two five-year followup interviews. Farming practices included specific crops and animals raised, growing up on a farm, and years worked or lived on a farm. Data from all three questionnaires was used for the analysis. Exact logistic regression models were used to estimate associations with farming characteristics and fungal sensitization or atopy while controlling for state; other factors such as age and smoking did not confound the associations.
The prevalence of fungal sensitization was 4% and the prevalence of atopy was 21%. While the prevalence of atopy was greater for NC than IA farmers (Odds Ratio (OR) =1.5, 95% Confidence Interval (CI) 1.0-2.1), fungal sensitization did not differ. Twenty-five percent of fungal-sensitized participants were not classified as atopic (n=7; Table E1). Fungal-sensitized farmers (N=28) were slightly older than those who were not (63 years vs. 61 years), however, there was no difference in the average age of the two groups (p=0.27).
Specific commodities were related to fungal sensitization (Table 1). After adjusting for state, farmers who grew tobacco, orchard fruit, or raised animals, particularly cattle, were more likely to be fungal sensitized than farmers not performing these activities. Growing soybeans, field corn, or other grains were also positively associated with fungal sensitization, but were not statistically significant. We lacked the ability to assess multiple crops in the same model due to the low prevalence of fungal sensitization and the high degree of correlation among crops. Sensitization to any specific fungal antigen was low, ~2% for all farmers and between 4 to 8% when limited to those classified as atopic (Table 2). Sensitization to specific fungi showed 11 of the 28 individuals (39%) were monosensitized and 17 (61%) were multisensitized.
Fungal sensitization was less common among these farmers compared to white men, 40 years and older from the National Health and Nutrition Examination Survey (NHANES) in 2005-2006. 4 Among farmers, sensitization prevalence to both Alternaria and Aspergillus was 2% (95%CI=1-3%) lower than NHANES with 7% for A. alternata (95%CI=5-9%) and 6% for A. fumigatus (95% CI=4-7%). Atopy prevalence was also lower (21%, 95%CI=17-25) compared to NHANES participants (30%, 95%CI=27-33%).
Other studies of agricultural workers suggest greater fungal sensitization among farmers. 5-8 While no studies appear to have focused on fungal sensitization associated with specific field crops, 18% of greenhouse workers were sensitized to at least one of four fungal species as measured by skin prick test, much higher than we observed even though our panel included the same fungi in addition to six other species. 5
While our study is among the largest to characterize fungal sensitization among farmers, our analysis was limited due to the low prevalence of sensitization and high prevalence of certain types of crop production and high correlation among these crops. Our panel contained ten common fungal species; many, but not all, have been associated with commodity crops. If the panel included a greater diversity of species, the prevalence of sensitization may have been higher; however, given that most farmers were multisensitized to fungi, it is unlikely that the addition of other fungi would greatly alter our results. The participants were older farmers so a healthy worker effect is possible where sensitized farmers have been selected out of agriculture prior to sampling. Our population was not selected based on respiratory disease history, thus our lower estimates may reflect the fact that other studies may have been enriched for individuals with respiratory outcomes. The agricultural exposure history was well characterized by detailed questionnaires; however, no environmental exposure assessments were conducted. Due to the high degree of correlation between some crops, most notably corn and soybeans, and the high prevalence of growing these two crops, we lacked statistical power to fully evaluate whether one or both of these major crops contributed to fungal sensitization.
In conclusion, this study represents one of the largest and most heterogeneous studies of fungal sensitization with regard to agricultural activities. Both fungal sensitization and atopy were low in this sample of U.S. farmers compared to the U.S. population. Individuals working with tobacco, orchard fruit, or animals had a higher prevalence of fungal sensitization; however, the sample size limited our ability to evaluate the influence of specific crops. Because fungal exposures differ around the world and rates of allergen sensitization differ based on farming history, future studies will need to focus not only on commodities produced and specific fungal agents, but also on population characteristics that may impact sensitization.
The authors would like to thank Stuart Long for his assistance with data analysis. Findings and conclusions in this report are those of the authors and do not necessarily represent the views of the Association of Schools of Public Health and/or the Centers for Disease Control and Prevention. Copies of questionnaires are available at www.aghealth.org/questionnaires.html. We used the P1REL201005, P3REL1090100, and AHSREL201004 releases of the AHS dataset.
Funding: This work was supported in part by the Association of Schools of Public Health and the Centers for Disease Control and Prevention fellowship program, the intramural research program of the National Institutes of Health, the National Institute of Environmental Health Sciences (Z01-ES049030) and National Cancer Institute (Z01-CP010119) and an Interagency Agreement (Y1-ES-0001) between the National Institute for Occupational Safety and Health and the National Institute of Environmental Health Sciences.
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