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Print version ISSN 0034-8910
Rev. Saúde Pública vol.40 n.5 São Paulo Oct. 2006 Epub Sep 01, 2006
Neice Müller Xavier FariaI; Luiz Augusto FacchiniII; Anaclaudia Gastal FassaII; Elaine TomasiIII
de Pós-Graduação em Epidemiologia. Departamento de Medicina
Social. Universidade Federal de Pelotas (UFPel). Pelotas, RS, Brasil
IIDepartamento de Medicina Social. UFPel. Pelotas, RS, Brasil
IIIPrograma de Pós-Graduação em Saúde Pública. Universidade Católica de Pelotas. Pelotas, RS, Brasil
Environmental working conditions in rural areas, notably exposure to organic
and mineral dusts, have been associated with increases in respiratory diseases.
The objective of this study was to evaluate the prevalence of respiratory symptoms
among farmers and the associations of these with occupational risk factors.
METHODS: This cross-sectional study was undertaken in 1996 with 1,379 farmers from Southern Brazil. Sociodemographic and farming-production parameters were collected, as were levels of exposure to organic and mineral dusts. Respiratory symptoms were assessed by a modified version of American Thoracic Society-Division of Lung Disease questionnaire. Multiple logistic regression analysis was used in analyses, controlling for confounding factors.
RESULTS: The majority (52%) of interviewees worked in activities with intense exposure to dust. Workers on farms with better economic indicators had a lower prevalence of respiratory symptoms. Poultry workers showed more symptoms of chronic respiratory disease (OR=1.60; 95% CI: 1.05-2.42). Farmers exposed to high concentrations of dust had more than 70% higher risk of asthma symptoms (OR=1.71; 95% CI: 1.10-2.67) and chronic respiratory disease symptoms (OR=1.77; 95% CI: 1.25-2.50).
CONCLUSIONS: The rural workers studied herein were exposed to high levels of organic and mineral dusts. Those exposed to higher dust concentrations, such as poultry workers, showed an increased risk of work-related respiratory symptoms. The implementation of respiratory protection programs is recommended, emphasizing workers involved with poultry production.
Keywords: Rural workers. Air pollutants, occupational, adverse effects. Occupational risks. Respiratory tract diseases. Cross-sectional studies. Dust.
Certain environmental conditions in the rural workplace, principally animal and plant dusts, have been associated with increases in respiratory illnesses including asthma,11,13,16,20 chronic bronchitis2,17,20 and hypersensitivity pneumonitis.1,16 Several agricultural activities involve high levels of exposure to dusts3,19 and substances such as toxic gasses,1,4 endotoxins1,3,4,11 and agrotoxins.1,10 Fungal spores, which generally occur in organic dusts, further increase the risks from exposure.1,19
Agriculture can lead to higher risks of respiratory problems.1,14 A broad multicentric study among European farmers found that 22% had respiratory symptoms related to rural work (wheezing, shortness of breath/or cough with expectorant).20 Those working in swine production comprised the group of highest risk, based on dose-response in relation to the number of hours in the workplace.18 In New Zealand, 18% of farmers showed work-related respiratory problems associated with contact with birds, swine, equines and grains (during harvest and storage).14 In Switzerland, farmers showed twice the level of chronic bronchitis and 4.5 times chronic expectoration relative to the overall population.2 In Norway, non-atopic farmers who worked with two or more types of livestock showed nearly twice the rate of asthma than those that did not work with animals.4
High levels of respiratory symptoms in farmers and rural workers1,20 have been found in specific workplaces, such as swine14,18,20 and poultry11,14,18 enclosures and areas of grain production.14 Reduction in pulmonary function among those working with animals within enclosed spaces, such as aviaries3 and swine barns,17,22 has also been observed.
The present study is part of a broader project evaluating the health of rural workers in the context of family farming.5 The objective of the project was to undertake a population epidemiological study of respiratory problems among agricultural workers. In a previous article,6 the prevalence of various respiratory symptoms was shown to be associated with the use of pesticides. The present work aimed to analyze rural production particularly agricultural and livestock activities in relation to exposure to agricultural dusts (organic and mineral) and to examine the associations between occupational factors and respiratory symptoms of asthma and of chronic respiratory disease.
The target population, for this cross-sectional epidemiological study, were family farmers (either owners or tenants) resident in the municipalities of Antônio Prado and Ipê, in the Serra Gaúcha, during 1996. Assuming an estimate of three workers per property, 20% of rural properties were randomly chosen in each municipality based on official lists of rural producers.*
The resulting sample showed a statistical power of 80% and a 95% confidence level to evaluate associations with a relative risk of 1.6 or more, depending on the exposure evaluated.
All data were obtained through interviews, using the American Thoracic Society/Division of Lung Diseases6 (ATS-DLD-78) questionnaire. Those workers selected for the study were aged 15 or over and worked at least 15 hours per week with agriculture and/or livestock. The interviewers were teacher trainees and rural schoolteachers, who initially participated in training sessions (40 hours) and in a pilot study (56 interviews). Field work was undertaken during five weeks of the summer harvest. Further details of sampling, fieldwork logistics and the questionnaire were presented in previous publications.5,6 Two questionnaires were used: one to obtain data relating to the farm and another relating to farmer characteristics.
The data collected relating to properties were:
- agro-economic indicators: area used for agriculture, level of mechanization and gross production the latter two were constructed indicators5 and evaluated in three categories (low, intermediate and high);
- type of agricultural production: primary agricultural production (fruits in general, pumpkin, onion, corn, bean and greens) and primary livestock (poultry, cattle, swine and equines);
- use of industrial animal feeds on the property.
Individual data for farmers included:
- socio-demographic indicators: gender, age, schooling (years completed). Information on smoking was evaluated in categories (never smoked, ex-smoker, smoker) and by the quantity of tobacco consumed (pack/years of smoking, analyzed in three and four groups);
- agricultural dusts: occurrence of dusts in the workplace. Interviewees were asked whether they were exposed to elevated levels of dust and other inhalants. Each type of dust was classified, according to its perceived intensity in the workplace, into three categories: absent (no exposure), low or high. Twelve types of dusts were evaluated: bird feathers, animal hair, manure dust, cereal grains, flower pollen, straw, cotton, soil dust, ashes, fumes (excluding that from tobacco), stone dust and toxic gases. The synthetic indicator of intense exposure was constructed by grouping the various dusts classified as intense (high dust concentration) and analyzed in three categories: little or no exposure to dust, intense exposure to one type of dust, intense exposure to two or more types of dust;
- duration of exposure: amount of agricultural work per day (during and between harvests), years living on the farm;
- exposure to pesticides: intense (indicator grouping two or more types of pesticide exposure, occurring at least three times per month) and history of acute poisoning by pesticides. The exposure to pesticides was evaluated as a confounding factor.
Various respiratory symptoms were evaluated using an adaptation of the ATS-DLD-78 questionnaire.6 Two conditions were analyzed based on these symptoms. Asthma symptoms: having had two or more wheezing episodes with accompanying shortness of breath.12 Symptoms of chronic respiratory disease, with at least one of the following symptoms: chronic cough or expectoration (during most days of the week and during three or more months per year); symptoms of chronic bronchitis (chronic cough and catarrh during at least two years), persistent wheezing (during most days and nights) or two or more wheezing episodes with shortness of breath.21
Approximately 10% of rural properties were revisited to assess the consistency of responses to the principal questions of the questionnaire. The Kappa test was used to evaluate the concordance between answers given during these two interview sessions.
A bivariate analysis was undertaken using Chi-square, Pearson and linear tendency tests. During this phase of analysis, an attempt was made to characterize the types of properties and the activities involving most exposure to dusts. These were used to define the variables to be included in the multiple regression analysis, which was developed using unconditional logistic regression, with a hierarchical model in two levels:
- Level 1 Socio-demographic factors (gender, age, schooling, smoking status), economic indicators (area used for agriculture, level of mechanization, income from gross production) and type of agricultural production.
- Level 2 Exposure to dust (synthetic indicator of intense dust), use of industrial animal feeds (included only in analyses of economic and agricultural indicators), duration of exposure, exposure to pesticides (grouped intense exposure and acute poisoning, both evaluated as binary variables yes/no).
In each level, the criterion for the maintenance of factors in the regression model was a p-value equal to or lower than 0.20. The variable for smoking status (amount/years of smoking) was not included in the model because it was not shown to be associated with any of the principal occupational exposures. The smoking variable, included in this analysis as a confounding factor, was examined as the main exposure factor in a previous article.6
Employees (7% of the sample) worked on properties with higher agricultural production. As the agro-economic indicators were constructed based on data from rural properties, employees characteristically had higher economic indicators than those of owners. As a result, employees were excluded from the analysis.
Interaction models were tested to evaluate if persons who smoked or who were ex-smokers responded differently from those who had never smoked.
A total of 1,479 rural workers were interviewed (selected from 495 rural properties); 1,281 were owners, 98 tenants or partners and 100 employees; with a response rate of 95%. Because of reasons indicated previously, only data from 1,379 farmers (471 properties) were used: 93% owners and 7% tenants or partners.
Of those interviewed, 55% were male, 12% smokers and 12% ex-smokers. The average time of smoking was 19.8 years (SD=15.1) with an average consumption of 12 cigarettes/day (SD=10.1). The mean age was 42 years (SD=15.6), with the highest being 92. Average schooling was of 4.8 years (SD=2.7), with 6% of interviewees without schooling and 6% having completed elementary school or higher.
The average area of properties was 31.5 hectares (SD=38.2), with 7.4 (SD=8.5) of these allotted for agriculture. Farmers had lived on the same property for 25 years (SD=16.0) and worked with pesticides, on average, for 16.7 years (SD=11.8). At least 75% of workers used pesticides and more than 40% had intense exposure: two or more types of occupational exposure during more than two days per month.
In the analysis of respiratory symptoms, women showed more asthma symptoms: the prevalence was of 15% among women and 10% among men (p<0.01) (Table 1). Symptoms of chronic respiratory disease showed a similar pattern, although not significant, with prevalence of 24% in women and 20% in men (p=0.09). Symptoms of both conditions were more prevalent among persons above 40 years of age and those with low levels of schooling (up to four years). Smokers and, mainly, ex-smokers indicated more symptoms of chronic respiratory disease. The group with highest tobacco consumption (above 182 packs year) showed increased respiratory symptoms (Table 1). This association was confirmed in the adjusted analysis both in relation to asthma symptoms (OR=2.16; 95% CI: 1.32-3.54) and chronic respiratory disease (OR=2.01; 95% CI: 1.34-3.01).
More than half of farmers (52%) worked in areas with high concentrations of at least two types of dust. Exposure to dusts was more intense among farmers on properties with lower economic indicators (gross production income, level of mechanization and car ownership) (Table 2). Likewise, farmers on properties with more animals poultry, cattle and swine and who used industrial animal feeds, stated that they worked in environments with higher concentrations of dusts (Table 2). The groups with highest exposure to dusts were those that worked with poultry; approximately 76% of these declared being exposed to two or more types of dust, in high intensity, during activities in bird enclosures. Thus, intense exposure to dusts was higher among poultry workers than farmers that did not produce poultry (PR=1.56; 95% CI: 1.36-1.79).
The evaluation of respiratory symptoms in relation to the characteristics of the rural property showed that the prevalence of asthma symptoms was lower among farmers whose properties produced fruits and onions (Table 3). Likewise, those on farms with higher economic indicators (area, level of mechanization and car ownership) and that produced onions showed fewer symptoms of chronic respiratory disease (Table 3).
Farmers from properties with poultry production declared higher frequencies of symptoms related to chronic respiratory disease. This association was confirmed by specifically evaluating those that worked directly with animals (Table 4). The majority of poultry farmers were aged up to 40, had higher schooling (p=0.02) and worked on properties with high levels of mechanization (linear tendency p<0.001). All poultry farmers were in the higher quartile of gross production income. Poultry workers showed similar levels of smoking status and consumption to other farmers.
Asthma symptoms were more frequent among farmers who worked on properties where industrial animal feeds were used.
Although not statistically significant, equine production also showed a tendency for higher prevalence of respiratory symptoms in both conditions evaluated. There was no relation between swine, bovine or other types of animal production and the respiratory symptoms evaluated (Table 4).
Increases in chronic respiratory disease symptoms were associated (in linear tendency) with intense exposure to bird feathers, straw, manure dust, ashes and fumes. Exposure to corn straw also showed a linear association with asthma symptoms (Table 5).
The synthetic indicator of intense exposure to agricultural dusts was shown to be linearly associated with the increase of respiratory symptoms for the two outcomes investigated.
No significant interactions were observed between the various exposures (agro-economic factors and the various types of dusts) and smoking. However, for the association between bird feathers and chronic respiratory disease, the interaction model with smoking was nearly significant (p=0.06). A reevaluation of this association, with stratification of the three smoking categories, showed that the "bird feather" factor remained as an indicator of risk just for the 1,042 farmers that never smoked (p=0.001, with a linear tendency). The adjusted odds ratio (OR) adjusted for the group with low exposure was of OR=1.01 (95% CI: 0.69-1.48) and for intense exposure was of OR=2.22 (95% CI: 1.44 -3.43). Among the 168 smokers and 169 ex-smokers, the association between bird feathers and respiratory diseases was not significant.
The present study suggests an increase in respiratory symptoms associated with intense exposure to organic and mineral dusts during agricultural work. Moreover, it revealed that work in poultry production presents elevated risks of chronic respiratory disease. These findings are significant, as there are no other known population studies of rural farmers/employees in Brazil.
The referred information provided by the farmers allowed estimates about specific types of dust and various chemical products encountered in the workplace. However, the lack of environmental measurements limits the accuracy of exposure estimates. In this study, a lower than desired agreement was found for some exposures, such as some dusts, which showed Kappa tests lower than 0.43. The quality control evaluation found a higher proportion of farmers exposed to intense concentrations of dusts (of several types) and to pesticides. Thus, exposure estimates should be considered as approximations, being potentially higher than reflected in the data.
Other authors have found high concordance between respiratory symptoms and alterations in pulmonary tests,12 including a study that specifically evaluated the ATS questionnaire.9 In relation to the criteria used for asthma symptoms (wheezing episodes with shortness of breath), the information provided was of high specificity (93%) and reasonable sensitivity (45%) for actual asthma in comparison to the clinical interviews associated with spirometry.12
As information on the conditions studied was based on cumulative prevalence (lifetime prevalence), inaccurate recollections by farmers may have led to underestimation of exposure and effects, or reverse causality, thus limiting causality affirmations.
Although the proportion of smokers and ex-smokers was lower than other studies involving agricultural workers,1 the analysis of tobacco consumption confirmed increased respiratory symptoms in the group with higher cigarette consumption.
The odds ratio can be reduced by the healthy worker effect and should be considered as a minimum effect. This sampling effect has previously been observed in other studies11,13,24 and tends to underestimate the differences between groups. In Holland, a longitudinal study among swine workers showed evidence that a selection bias of non-asthmatics (asthmatics changed to other professions), masked the occupational risks for asthma, but not for chronic bronchitis.24 Likewise the majority of exposure risks (poultry confinement and dusts) in the present study showed associations with chronic respiratory disease, but not with asthma.
There was a higher individual exposure to dusts on properties with higher economic indicators. However, the multivariate analysis indicated fewer respiratory symptoms among workers in these properties, even after adjusting for the effects of higher dust concentrations. Likewise, the principal economic crops (fruits and onions) showed a similar protective effect. Indicators of low socio-economic level have been associated with increased prevalence of asthma, although this remains controversial.** Socioeconomic status, as a main determinant of health conditions, may explain these results, overlapping even the risk originating from dust exposure in the work environment.
Among rural farmers, those who worked in poultry enclosures were notable because of their high levels of chronic respiratory disease symptoms. This result was confirmed among farmers that, in addition to raising poultry on their farms, dealt directly with these animals during daily work. This effect was seen even on rural properties with higher economic indicators. In addition, the dusts directly linked to poultry confinement such as bird feathers and manure dust were also a risk effect for chronic respiratory symptoms. These results are consistent with other research that found an increase in respiratory symptoms among poultry workers.2,3,11,14 A study16 evaluating 9,027 European and American farmers found higher respiratory symptoms associated with some types of agricultural work, notably workers in poultry farming and other activities with confined animals. A European multicentric study18 with 6,156 farmers found higher levels of wheezing among poultry workers during the year previous to the study, with dose-response related to the amount of time spent within poultry enclosures. In the USA, approximately 20,000 farmers who used pesticides were evaluated and a specific risk of wheezing symptoms was identified as associated with animal production and close contact with grains. Exposure related to poultry farming was the most important predictor of wheezing during the year prior to the study.11
In the region of the present study, animal farming, in the majority of cases, was undertaken on a large spatial scale, particularly for cattle, sheep and equines. Thus, activities involving these types of livestock were carried out in open and expansive areas. The quantity of animals was also relatively small: the majority of farmers owned less than 40 heads. In contrast, the production of confined poultry has expanded in the last decades, following a general Brazilian trend. In poultry confinement houses, approximately 14,000 animals were kept in each lot (a minimum of 2,000 and as many as 28,000 birds/enclosure, or approximately 23 birds per m2) which increases significantly the concentration of dusts and toxic gases, such as ammonia and carbon dioxide.7 In addition to the risks arising from direct contact with birds, the cleaning and maintenance of confinement houses can also be hazardous, primarily that involving the "aviary bed", on which reared birds are kept.7,13 The annual removal and weekly turnover of the "bed" normally result in intense exposure to dusts and micro-organisms such as bacteria, fungi, viruses and endotoxins.3,7,19 Results from the present study confirm other work that document the respiratory risk of raising animals in confined spaces2,22 and, more specifically, the respiratory risks of poultry confinement.3,11,18
Concentrations of burning residues (fumes and ashes) also showed an association with increased chronic respiratory disease, as in previous studies in China,23 Iran8 and Califórnia,15 where exposure to smoke from domestic and agricultural incineration (cereal straw and other production by-products) was associated with an increase in asthma or respiratory symptoms. In the USA, the Environmental Protection Agency defines all of these particles suspended in air as particulate matter, and has developed specific programs to investigate exposure to this type of dust.
Overall, the present study revealed that agricultural work involves substantial exposure to various types of dusts, both organic and mineral. Farmers who work in environments with higher dust concentrations, particularly poultry workers, showed more respiratory symptoms of asthma and of chronic respiratory disease, which is consistent with the international literature.
The shortage of Brazilian studies on rural workers highlights the need for further research on respiratory health of workers in different agricultural contexts. In future studies, it is suggested the use of methodologies able to identify causality between occupational exposure and respiratory problems. Measures of environmental exposure may contribute to more precision and objectivity in estimates of dust concentrations and other environmental hazards. Likewise, tests of pulmonary function might diagnose respiratory illnesses and their severity. In order to reduce recall bias, limits should be set for the evaluation of symptoms from more recent periods, such as, for example, the 12 months prior to interviews.
Results from the present study emphasize the need to invest in respiratory protection of workers on family farms and rural employees, primarily during activities where they are exposed to high levels of agricultural dusts. Considering the risk evidenced for poultry workers and the rapidly expanding poultry industry, the implementation of specific programs that address respiratory protection for all workers involved in poultry farming is recommended.
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Neice M. Xavier Faria
R. República, 80/1401 Cidade Alta
95700-000 Bento Gonçalves, RS, Brasil
Supported by Conselho Nacional de Desenvolvimento Científico e Tecnológico (National Council for Scientific and Technological Development CNPq - Process n. 400569/92-2).
Based on a doctorate
thesis presented to the Postgraduate Program in Epidemiology of the Universidade
Federal de Pelotas, in 2005.
* Lists provided by Instituto Nacional de Colonização e Reforma Agrária (INCRA) (National Institute for Colonization and Agrarian Reform) and Associação Rio-Grandense de Empreendimentos de Assistência Técnica e Extensão Rural (EMATER-RS) (Association for Technical Assistance and Rural Extension of Rio Grande do Sul).
** Global Initiative for Asthma. Global strategy for asthma management and prevention [workshop report]. Bethesda (MD): National Heart, Lung, and Blood Institute; 2002. Available from http://www.ginasthma.com/GuidelineItem.asp?intId=60 [access in 2006 Feb 19]