Prevalence of work-related respiratory symptoms in Iranian farmers

1International Institute of Health Studies, Ottawa, Ontario; 2Department of Pulmonary Medicine, Islamic Azad University of Mashhad; 3Department of Medical Statistics; 4Immunology Research Center, Mashhad University of Medical Sciences, Mashhad, Iran Correspondence: Dr Nastaran Hashemi, 12531 26th Avenue Northeast, Seattle, Washington 98125-4301, USA. Telephone 206-364-1601, fax 905-763-9771, e-mail hashemi_nastaran@yahoo.com or hashemi@iihs.ca N Hashemi, M Mirsadraee, MT Shakeri, AR Varasteh. Prevalence of work-related respiratory symptoms in Iranian farmers. Can Respir J 2006;13(4):198-202.

F arming has been known as a high-risk occupation for the development of work-related symptoms since 1555, when Olaus Magnus recognized farming health hazards with respect to grain dust (1).Farmers involved in animal production have a higher prevalence of respiratory symptoms than other farmers and other rural residents.An increase in respiratory symptoms has been noted among animal farmers in North America, Europe and New Zealand (2,3).Although the prevalence of smoking is lower in farming than in other occupations (4), farmers have a greater risk of respiratory disorders than people in nonfarming occupations (5).While at work, animal farmers are exposed to inorganic dust, and organic dust containing microorganisms, mycotoxins, endotoxins, animal feed particles, allergens and chemical agents (6).Organic dust exposure is known to cause allergic and nonallergic rhinitis (7), or organic dust toxic syndrome (8), and can induce chronic bronchitis, asthma or an asthma-like syndrome (9).
Repeated exposure may provoke respiratory symptoms in sheep farmers.Keeping sheep outdoors can cause proliferation of bacteria in the sheep skin-fleece microenvironment.Likewise, exposure to high levels of organic dust during the lambing season (during which farmers stay inside the sheep barn most of the day) could increase exposure to Gram-negative ©2006 Pulsus Group Inc.All rights reserved bacteria (Pseudomonas species) and bacterial endotoxin found in sheep fleece (10).Americans first described the flu-like illness as a febrile reaction to organic dust exposure (11).Farmers with bronchial hyper-reactivity attributed the onset of their airway disease to the flu-like episode occurring after an abnormally severe dust exposure incident (12).
Farming is commonly a lifelong occupation (13).Because farmers often live at their farms, they can continuously be exposed to hazardous agents, and due to animal and plant cycles, exposure patterns at farms may vary over the course of a year.Climatic differences among agricultural areas lead to a variety of farmer exposure patterns across different countries (14).
The present study focuses on the prevalence of work-related symptoms in sheep breeders compared with that of agricultural farmers.The aim of the study was to determine which occupational symptoms are predominant among farmers and to explore potential risk factors for sheep breeders.

Study area and population
The study area included the mountainous rural areas of Rokh and Kadkan, located in northeast Iran.The area has a population of 30,000, many of whom are farmers.

Protocol
We used a Farsi questionnaire (see Appendix) derived from the European Community Respiratory Health Survey questionnaire and the European animal farmers' survey (11,13,14).The first part of questionnaire included questions on work-related respiratory symptoms (WRS), nasal irritation, eye irritation and flu-like illness within the preceding year (11,14).WRS was defined as wheezing, breathlessness, cough or phlegm while at work.A sudden onset of fever, chills, muscle ache, weakness, headache, cough, chest tightness or breathlessness 2 h to 6 h after organic dust exposure was referred to as a 'flu-like illness'.The second part of the questionnaire contained items on details of sheep farming (see Appendix).Some of these items were taken from a previous study (14) on farming in other countries.
Likewise, questions on age, sex, smoking habits (current and past) and the history of the participants' present job were included in this questionnaire.Exclusion criteria included subjects who moved out of the area and subjects who were no longer keeping sheep or were keeping fewer than 10 sheep (for sheep breeders).
In total, 173 farmers comprising 127 sheep breeders and 46 agricultural farmers were interviewed face-to-face by a family doctor on the research team.Subjects were defined as 'sheep breeders' if they kept at least 10 sheep.Among the sheep breeders, only 50 were full-time farmers who worked outdoors among sheep each day.This group was defined as full-time sheep breeders because they had the highest frequency of animal contact.The remainder of the study population worked less than 8 h a day inside sheep barns and, thus, were defined as part-time sheep breeders.Agricultural farmers were defined as farmers who did not keep sheep within the year preceding the interview.Because of the low number of volunteers, all farmers in these areas were included in the present study.
The Ethical Committee of the Mashhad University of Medical Sciences (Mashhad, Iran) approved the study.

Analysis
The design of the study was a cohort survey.Differences in the prevalence of work-related symptoms and syndromes between sheep breeders and agricultural farmers were tested by χ 2 analysis on two-by-two contingency tables.The 95% CI of the RR was also calculated.A two-sided P value of 0.05 was the criterion for statistical significance.Risk factors for work-related symptoms were evaluated among sheep breeders using multiple logistic regressions adjusted for age, sex and smoking habit.All analyses were performed with SPSS software (version 11.5, SPSS Inc, USA).

Subjects
The mean ± SD age of the farmers was 34.9±16.3years and 10% were current smokers (Table 1).Only 50 sheep breeders considered farming as their full-time job.

Prevalence of work-related symptoms
Ten of 46 agricultural farmers suffered from WRS (Table 2).Sheep farmers had a high prevalence of WRS (48%) and nasal irritation (37.8%).Forty-eight of 127 sheep breeders (37.8%) reported the presence of a flu-like illness compared with none of the agricultural farmers.

Farming characteristics and work-related symptoms in sheep breeders
Associations between farming characteristics and work-related symptoms (adjusted for age, sex and smoking habit) are shown in Table 3.In this analysis, working full-time as a sheep breeder, keeping a large number of sheep and sheep shearing were the major risk factors for WRS, asthma and flulike illness.The use of pesticide was a significant predictor for WRS (OR=2.3[95% CI 1.0 to 5.3]).The incidence of asthma was almost 12.6-fold higher among sheep breeders keeping more than 500 sheep than among those who kept fewer than 50 sheep.A higher number of working years as a sheep breeder was only a risk factor for flu-like illness (OR=1.1 [95% CI 1.01 to 1.14]).

Distribution of WRS and farming characteristics in sheep farmers
Table 4 shows the distribution of WRS according to farming characteristics after adjusting for age, sex and smoking habit.The risk of developing work-related wheezing increased significantly with full-time farming (OR=7.Sheep shearing and keeping a large number of sheep were shown to be associated with nearly a fourfold increase in the risk of incidence of phlegm (OR=4.4[95% CI 1.5 to 13.5], OR=4.3 [95% CI 1.1 to 16.3], respectively).A similar association was found for incidence of cough.
The present analysis could not confirm a positive relationship between keeping animals other than sheep and WRS.

DISCUSSION
Animal production has been associated with WRS among farmers (1,3,9,15,16); working in direct contact with animals in animal confinement areas results in exposure to a wide array of hazardous airborne agents (1).Farmers are exposed to a vast array of potential respiratory hazards despite generally being healthier than the rest of the population and having a tendency to smoke less (2).The selection of an appropriate comparison population is a common concern for researchers studying work-related symptoms among farmers.Most studies on animal farming have used nonfarming rural or workingclass populations as their referents and few studies of respiratory symptoms in farmers have been able to make comparisons across agricultural practices to explore the impact of animal exposures (1,17).
In the present study, the prevalence of work-related symptoms and potential risk factors were assessed among Iranian farmers within the year preceding the interview.The European Community Respiratory Health Survey (18) contains items validated for the assessment of respiratory symptoms and disease status.Likewise, farming practices remain stable for some time, so questionnaires assessing farming methods are good proxies for exposure (16).
Comparing farmers raising sheep in the year before the survey with those who did not, we observed a higher prevalence of work-related symptoms among those involved with animal handling.The prevalence of respiratory symptoms, especially breathlessness (OR=3.5 [95% CI 1.2 to 9.98]), was significantly higher among sheep farmers.Considering that our selected list of farmers live in rural areas and follow traditional methods of agriculture, our results cannot be generalized to all farmers.In the present study, an increased frequency of animal contact was associated with an increased risk of work-related symptoms.A significant relationship was shown between the number of daily hours working indoors with animals and the development of work-related symptoms.Our study included 50 sheep breeders who stay outside with their animals almost all day.In this group, the incidence of asthma and flu-like illness was almost fivefold more common than in other sheep breeders, and respiratory symptoms were threefold more common.Our study showed an association between full-time farming and a greater risk of wheezing, which is in agreement with the findings of a European animal farming study (OR=7.1 [95% CI 2.1 to 23.4] versus OR=1.57[95% CI 0.77 to 3.2], respectively) (14).Full-time farming was not shown to be a risk factor for breathlessness in the European study (14), as it was in our study (OR=0.44[95% CI 0.16 to 1.25] versus OR=8.7 [95% CI 3.1 to 24.7], respectively).
An increase in the number of animals raised was associated with a higher risk of work-related symptoms.A positive doseresponse pattern of flu-like illness and work-related incidence of phlegm were observed in our study and in a German farmers' study (13).Our results and others' (1) found an increased risk of wheezing with an increased number of animals on the farm, whereas a study of Ohio grain farmers (19) showed an inverse dose-response trend with the number of animals raised.
It is important to understand whether there are multiple hazardous agents creating a synergistic effect.The increased adverse impact of quality and quantity of exposure on workers is important.Radon and Winter (13) discovered an endotoxin content of 58.2 endotoxin units/mg to 193.9 endotoxin units/mg in sheep wool; thus, endotoxin exposure during sheep shearing could be very high.Our results confirmed a great risk of respiratory symptoms, asthma and flu-like illness associated with sheep shearing.
Kimbell-Dunn et al (3) recently described an association between the use of a formaldehyde dip and breathing problems at work.After adjusting for potential confounding variables, the use of pesticides was associated with an increased risk of WRS (OR=2.3[95% CI 1.01 to 5.3]) in our study.
Overall, the incidence of work-related symptoms and WRS found in this population while at work was significantly higher than that found in the studies performed in New Zealand, Spain, Germany and other countries (3,13,20,21).These differences could be due to climate, exposure pattern or the method of agriculture in the different countries.

CONCLUSIONS
Sheep farmers in general have higher rates of work-related symptoms than agricultural farmers.In view of the severity of respiratory symptoms being influenced by the extent of animal contact, our results probably underestimate the impact of this exposure.

TABLE 3
Prevalence odds ratio (POR) of work-related symptoms and farming characteristics in sheep breeders (n=127)

TABLE 2
Prevalence of work-related respiratory symptoms among sheep breeders and agricultural farmers (control group)