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doi:10.1378/chest.06-2323
(Chest. 2007; 131:1197-1204)
© 2007 American College of Chest Physicians
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Excess Respiratory Symptoms in Full-time Male and Female Workers in Large-Scale Swine Operations*

Ambikaipakan Senthilselvan, PhD; Liliane Chénard, MSc, PEng; Kendra Ulmer, BSN; Natasha Gibson-Burlinguette, LPN; Cheryl Leuschen, RN and James A. Dosman, MD, FCCP

* From the Canadian Centre for Health and Safety in Agriculture (Ms. Chénard, Ms. Ulmer, Ms. Gibson-Burlinguette, and Ms. Leuschen), and Department of Medicine (Dr. Dosman), University of Saskatchewan, Saskatoon, SK; and the Department of Public Health Sciences (Dr. Senthilselvan), School of Public Health, University of Alberta, Edmonton, AB, Canada.

Correspondence to: Ambikaipakan Senthilselvan, PhD, Department of Public Health Sciences, School of Public Health, 13–106B Clinical Sciences Building, University of Alberta, Edmonton, AB, T6G 2G3, Canada

Abstract

Background: The respiratory health effects of working in swine operations have been previously investigated mainly in male owner/operators with intermittent exposure to indoor air contaminants.

Objectives: To examine the respiratory health of male and female workers employed full time in large-scale intensive swine operations in Saskatchewan.

Design: A cross-sectional study of male and female swine workers employed full time and nonfarming control subjects.

Results: In total, 374 swine farmers (240 men and 134 women) and 411 nonfarming rural control subjects (184 men and 227 women) participated in the study. After controlling for age and smoking, male and female workers were significantly more likely to have chronic and usual cough, and chronic and usual phlegm in comparison to male and female nonfarming control subjects, respectively. The risks of these symptoms were greater in female workers (chronic cough: odds ratio [OR], 5.14; 95% confidence interval, 2.67 to 9.89; chronic phlegm: OR, 4.26; 95% confidence interval, 1.86 to 9.73) than in male workers (chronic cough: OR, 3.47; 95% confidence interval, 1.77 to 6.81; chronic phlegm: OR, 3.22; 95% confidence interval, 1.76 to 5.89). These increased risks were not observed for asthma and asthma-like symptoms in female workers. Male workers had an increased risk of shortness of breath in comparison to their nonfarming counter parts.

Conclusions: Swine workers had increased risk of chronic and usual bronchitis-like symptoms. Female workers in swine operations appear to have greater risk of these symptoms. Future surveillance programs should include both male and female workers.

Key Words: females • males • respiratory symptoms • smoking • swine workers

Recent years have seen the successive evolution of swine production in Canada through mainly three stages, from small, largely outdoor production with minimal respiratory exposures to the farmer, to larger, intensive indoor operations on individual farms managed by the farmer owner/operator experiencing intermittent exposures, to the current, large commercial facilities operated by workers employed full time experiencing ≥ 8 h/d of respiratory exposures. Almost all of our current understanding of the respiratory health effects of ambient exposures in intensive swine production facilities has come from studies on individual male farmers during the 1980s and 1990s who experienced intermittent "2 to 3 h/d" exposures that have demonstrated increases in respiratory symptoms, reductions in expiratory flow rates, and increases in bronchial responsiveness.12345678 Across-shift studies have demonstrated acute reductions in pulmonary function test variables,9101112 increases in bronchial responsiveness,1011121314 and increases in inflammatory mediators.10111213 Longitudinal studies have demonstrated increases in bronchial responsiveness,15 excess decline in pulmonary function test variables,16 with acute across-shift changes predicting longitudinal decline in measures of lung function.17 The relationship of respiratory effects to indoor occupational air contaminants including dust, endotoxin, ammonia, and hydrogen sulfide have been described.6791011181920212223242526 The study that we herein describe is to our knowledge the first report on the respiratory health effects incurred by workers employed full time in the recently developed, indoor, large-scale, corporate intensive swine production facilities that also includes robust numbers of both women and men.

Materials and Methods

Sampling Frame
The study was conducted in rural Saskatchewan, Canada. Swine workers were recruited with the collaboration of SaskPork, the pork producers’ association in Saskatchewan, and large swine production companies in Saskatchewan. A description of the study was posted in the SaskPork periodic newsletter, and visits encouraging participation were made to executives of the swine production companies. The large swine production companies cooperated by encouraging all workers to attend the evaluation clinics that were held in nearby towns and villages. The companies cooperated by scheduling the workers into prearranged time slots. All workers were given the opportunity to participate. To participate in the study, swine workers had to be ≥ 17 years old and had to work in the confinement building for at least 4 d/wk with a total work duration of ≥ 20 h/wk.

In this study, 374 workers were chosen from 38 large swine operations. The number of workers chosen from each swine operation varied from 3 to 37, resulting in varying response rates for each operation. Nonfarming control subjects were chosen from all nonfarming rural dwellers that were residing within an approximate 100-kilometer radius of a swine production site. A form was sent to all persons in the taxation list provided by the rural towns located in proximity of the swine production sites. Nonfarming rural dwellers who were involved in mining, grain handling, metal, and auto-body work were not considered for selection of control subjects.

All interviews and testing were conducted in hospitals and community centers that were located near the swine production sites and the residence of the nonfarming control subjects. A person-to-person interview was conducted by a trained technician who completed the questionnaire by recording participants’ responses to the questions in the questionnaire. The study was approved by the Biomedical Research Ethics Board of the University of Saskatchewan. Prior to the interview, informed written consent was obtained from all subjects.

Study Group
The participation rate from the large swine operations was approximately 70%. Of the 374 swine workers who participated in the study, 240 were men and 134 were women. Of the 411 nonfarming rural dwellers who participated in the study, 184 were men and 227 were women. The age of the swine workers and nonfarming control subjects ranged from 17 to 65 years.

Medical and Occupational History
A respiratory health and occupational history questionnaire was administered by a trained technician to all participants. The questionnaire used in previous studies3161725 was modified to include questions related to current practice in the swine industry. The presence of usual cough was obtained from an affirmative response to the question, "Do you usually have a cough (count a cough with first smoke or first going outside, do not count clearing the throat)?" The presence of chronic cough was obtained from an affirmative response to the second question in a series of two consecutive questions, "Do you usually cough as much as four to six times a day ≥ 4 days out of the week?" and "Do you usually cough like this on most days for ≥ 3 consecutive months during the year?" The presence of usual phlegm was obtained from an affirmative response to the question, "Do you usually bring up phlegm from your chest (count phlegm with first smoke or first going outside)?" The presence of chronic phlegm was obtained from an affirmative response to the question that followed the question on usual phlegm, "Do you usually bring up phlegm like this as much as twice daily ≥ 4 days out of the week?" The presence of wheeze was obtained from an affirmative response to the question, "Does your chest ever sound wheezy or whistling occasionally apart from colds?" The presence of shortness breath was obtained from an affirmative response to the question, "Are you troubled by shortness of breath when hurrying on the level or walking up a slight hill?" The presence of asthma was obtained from an affirmative response to the question, "Has a doctor ever told you that you have asthma?"

The years of employment in any swine operation were obtained from the response to the question, "How long have you worked in a swine confinement unit?" Days per week and hours per day spent in the current workplace were obtained from the question, "How many days a week and hours a day do you spend in the barn?" The work-related activities and time spent in these activities were obtained in different swine production stages: farrowing, nursery, grower/finisher, breeding/gestation, and other activities. Farrowing is the stage during which the sows give birth and piglets are kept with the sow until they are weaned (up to 3 weeks). After weaning, the piglets are kept in nursery until they reach 8 to 12 weeks of age and are moved to grower/finisher units until they reach 100 to 120 kg. They are then shipped to the market or used for reproduction purposes. The pigs are usually approximately 25 weeks of age when they leave for the market. In the breeding/gestation section, sows are bred and kept during the gestation period until they are moved to farrowing rooms. The "other" category included working in office areas, maintenance that cannot be linked consistently to a single production area, indoor washing of the facility, working in feed mill and/or laboratory, and handling boars for semen production. A worker may engage in more than one of these activities on a single working day. The categories in production stages are not mutually exclusive, and the proportion of workers in these categories will not add up to 100%. For the same reason, mean hours spent in these production stages cannot be added to obtain the total hours spent in a day in the swine operation.

Lung Function Measurements
Pulmonary function testing was performed by trained technicians using a volume displacement spirometer (model 1022; SensorMedics; Yorba Linda, CA) and testing techniques that followed American Thoracic Society recommendations.27 The following parameters were recorded: FEV1, FVC, FEV1/FVC ratio, and forced expiratory flow between 25% and 75% of FVC (FEF25–75%). Percentage of predicted values for FEV1, FVC, FEV1/FVC ratio, and FEF25–75% were obtained from equations developed by Crapo et al.28

Smoking Behavior
Smoking habits were defined as current smokers, persons currently smoking cigarettes; ex-smokers, persons who have smoked > 400 cigarettes (or equivalent amount of tobacco) in his/her lifetime but not currently smoking; and nonsmokers, persons who have not smoked > 400 cigarettes (or equivalent amount of tobacco) in his/her lifetime.

Statistical Methods
Continuous variables were described with means and SD. Frequencies and percentages were used to describe the categorical variables. Differences in continuous variables were examined by Mann-Whitney U tests to allow for skewness in the distributions and violation of equal variance assumption in the standard two independent-sample t tests. {chi}2 test was used to test the differences in smoking between swine workers and nonfarming control subjects. Multivariate logistic regression analyses were used to determine the association between respiratory symptoms and working in swine operations after controlling for age and smoking. We also conducted independent dose-response analysis between years of employment and symptoms in male and female workers after controlling for smoking using logistic regression analysis. A three-factor analysis of variance was conducted to determine jointly the significant differences in percentage of predicted lung function between mask users and nonusers and the swine operations after controlling for smoking.

Results

In male and female groups, swine workers were somewhat younger than nonfarming control subjects (Table 1 ). Age ranges for swine workers and control subjects were identical in men (17 to 65 years) and were very similar in women (swine workers, 18 to 57 years; control subjects, 18 to 64 years). Mean weights were similar in swine workers and nonfarming control subjects among men and women, respectively. The proportion of current smokers was significantly greater among swine workers than among nonfarming control subjects among men and women. No significant difference was observed in the proportion of ex-smokers between these groups.


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  		Table 1. Characteristics of Swine Workers and Nonfarming Control Subjects by Gender*

 
Mean years of employment in any swine operation were greater for male workers than female workers (Table 1). The distribution of years of employment in any swine operation was skewed in both men and women with the median and third quartile of years worked being 4.0 years and 9.8 years for men and 3.0 years and 6.1 years for women, respectively, indicating that the majority of the male and female workers have worked in swine operations for < 10 years. Mean number of days per week was greater in male workers than in female workers. As seen in Table 1, both male and female workers worked on average 42.6 h/wk and 40.3 h/wk, respectively. In addition, only 3 of the 374 workers worked exactly 20 h/wk, 14 worked from 21 to 29 h/wk, 244 worked from 30 to 40 h/wk, and 113 worked > 40 h/wk.

The proportions of workers engaged in different production stages and mean hours spent by the workers in these production stages are shown in Table 2 . The proportions in Table 2 will not add up to 100% because a worker may engage in more than in one of these activities on a single working day, and the categories in production stages are not mutually exclusive. A significantly greater proportion of women worked in farrowing operations and the mean hours per day worked in farrowing operations were significantly greater in female workers than in male workers (Table 2). A similar proportion of men and women worked in the nursery operations, but the mean hours per day worked in nursery operations were significantly greater in female workers than in male workers (Table 2). A significantly greater proportion of men worked in grower/finisher and breeding/gestation operations, but the mean hours per day worked in these operations were not significantly different between male and female workers. Among the swine workers, use of a mask in the barn was similar in male workers (84.6%) and female workers (87.3%). Of those who used a mask, 30.5% of male workers and 36.2% female workers used a mask occasionally, 45.3% of male workers and 36.2% female workers used a mask most of the time, and 24.1% of males workers and 27.6% female workers used a mask all the time.


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  		Table 2. Proportion of Workers and Duration of Time Spent per Day in Various Swine Production Stages Among Male and Female Workers*

 
The proportions of chronic and usual cough and phlegm are shown in Figure 1 for swine workers and nonfarming control subjects among men and women. In both men and women, the proportions of these symptoms were significantly greater among swine workers than among nonfarming control subjects, with female subjects having greater differences in the proportion of these symptoms between swine workers and nonfarming control subjects. Chronic and usual cough was more prevalent among female workers than male workers, whereas chronic and usual phlegm was more prevalent among male workers.


Figure 1
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  		Figure 1. Proportion of chronic and usual respiratory symptoms in swine workers and nonfarming control subjects among men and women; p values indicate significant differences in the prevalence of symptoms between swine workers and nonfarming control subjects after controlling for age and smoking using logistic regression analysis.

 
The relationship between respiratory symptoms and working in swine operations was further investigated using odds ratios (ORs) and 95% confidence intervals from multivariate logistic regression analysis (Table 3 ). The ORs of respiratory symptoms for working in swine operations were greater in women than in men for all four symptoms. Female subjects working in a swine operation had fourfold to fivefold increases in the risk of reporting respiratory symptoms, whereas male subjects had threefold to fourfold increases in the risk. As indicated by the ORs in Table 3, the effect of current smoking on respiratory symptoms was greater among women than men. In female subjects, a fivefold increase in the risk of chronic cough was associated with both current smoking and working in swine operations. As shown in Table 3, with age fixed at any value, the OR for chronic phlegm (cough) for nonsmokers who were swine workers was 3.22 (3.24) in men and 4.26 (5.66) in women in comparison to nonfarming control subjects. Similarly, with age fixed at any value, for nonfarming control subjects who were current smokers the OR for chronic phlegm (cough) was 3.13 (2.57) in men and 4.33 (4.66) in women in comparison to nonsmokers.


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  		Table 3. Association Between Chronic and Usual Cough and Working in Swine Operations Among Men and Women From Multivariate Analysis*

 
To eliminate the potential residual confounding of smoking in the association between respiratory symptoms and working in a swine operation, a subgroup analysis was conducted in nonsmokers among swine workers and nonfarming control subjects. Although estimates of the ORs were less stable due to the smaller sample size, significant associations were observed between the four respiratory symptoms and working in swine operations (data not shown). In dose-response analysis, no significant association was between length of employment and any of the symptoms after controlling for smoking.

The prevalence of asthma was very similar in swine workers (11.9%) and control subjects (11.5%) among men and was slightly higher among swine workers (15.5%) in comparison to nonfarming control subjects (14.2%) among women. A significant association was observed between shortness of breath and working in swine operations in males. This significance was not observed in women. Working in swine operations was not significantly associated with asthma or wheeze apart from cold.

Among both men and women, mean lung function values and percentage of predicted values were very similar in swine workers and nonfarming control subjects (Table 4 ), and no significant differences were observed between these means. In male and female workers, we conducted a three-factor analysis of variance to determine jointly the significant differences in percentage of predicted lung function between mask users and nonusers and the swine operations after controlling for smoking. There were no significant differences in any of the lung function parameters between mask users and nonusers or between the swine operations.


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  		Table 4. Mean Values of Lung Function Parameters for Swine Workers and Nonfarming Control Subjects by Gender*

 
Discussion

This is the first study of which we are aware in which the respiratory health of swine workers employed full time has been evaluated, and the first time that a reasonably large population of workers being evaluated has included both women and men, reflecting the changing work force in the industry. The results demonstrate the apparent development of a considerable complex of respiratory symptoms in the workers. On average, the years of exposure were 6.6 years in men and 4.1 years in women. Despite this significant lower number of exposure years in the women, enhanced risk ratios for chronic cough and usual cough were observed among the women. The limited number of exposure years might partially explain the absence of significant differences in lung function between workers and nonfarming control subjects.

To our knowledge, information to date on the respiratory effects of swine barn exposures has been based primarily on male farmer owner operators and their family members with intermittent exposures. These previous reports12345678161718 have demonstrated increased symptoms, reductions in pulmonary function test results, increased airways responsiveness, and increases longitudinal decline that relates to ambient exposure levels.

The development of respiratory manifestations in farmers exposed to the indoor environment in swine confinement operations has been well documented.12345678 In a study26 conducted in Ontario, Canada, no significant differences were found in lung function tests between swine farmers and dairy farmers, but longitudinal observations demonstrated a relationship between respiratory symptoms and exposures among the swine farmers.29 In a study conducted in Iowa,1 no significant differences were observed in lung function between swine farmers who worked in confinement facilities and swine farmers who did not work in confinement facilities. However, both acute and chronic symptoms were significantly more common in those who worked in the confinement facilities. The most convincing evidence of pulmonary function differences was observed in young workers vs older swine workers in a cross-sectional study3 conducted in Saskatchewan, Canada, raising the possibility of a healthy worker effect in swine confinement farmers. The healthy worker effect was subsequently demonstrated in long-term swine farmers in a longitudinal study30 conducted by the same group of researchers. In a longitudinal study, no differences was observed in lung function test results between swine farmers and neighborhood farmers studied longitudinally, but endotoxin concentrations in the swine confinement facilities were related to decline in lung function.18 A longitudinal study16 from Saskatchewan, Canada demonstrated convincing evidence of longitudinal decline over a 5-year period in measures of lung function in swine farmers as compared to rural dwelling nonfarming control subjects, a finding also confirmed in a study31 conducted in Denmark. In this study, we demonstrated an increase in cough and phlegm in both female and male workers in swine confinement operations but not in asthma and wheeze and asthma-like symptoms. Despite working fewer years in the industry, women demonstrated higher risks compared to men for chronic and usual cough and chronic and usual phlegm after controlling for the effect of smoking. Although smoking was associated with these symptoms, there was also increased risk of cough and phlegm in lifetime nonsmoking workers.

It has recently been recognized that women employed in exposed circumstances might be at risk of enhanced respiratory effects. In our study, we find that, in comparison to a nonexposed rural dwelling control population of women, women workers were at higher risk of reporting usual cough and usual phlegm and chronic cough and phlegm. We further found that this increased risk was independent of the risk related to smoking. Even when we excluded current and ex-smokers, the lifetime nonsmokers continued to show these trends. A possible reason for this increased risk of symptoms in female workers might be related to the increased levels of air contaminants in the operations where they work. In our study, a greater proportion of women worked in farrowing operations, and they spent longer duration in farrowing and nursery operations during their daily work shift. Workers get closer contact with pigs in these operations and are exposed to increased air contaminant levels. In our study, use of a mask in the barn was very similar in male and female workers. In a study32 conducted in Iowa, although the total dust levels were higher in the finisher operations, the mean respirable dust fraction was higher in the farrowing and nursery operations in comparison to the finisher operations. However, it is not known if endotoxin concentrations were different between these operations.

There is evidence that the respiratory response of women to environmental and occupational exposures may differ somewhat in women as compared to men. We have previously demonstrated that female smokers appeared to have more evidence of airways obstruction with a lower number of smoking pack-years than did male smokers.33 In a review article,34 a number of sources were cited as evidence for a gender specific susceptibility to COPD in women. Female first-degree relatives of current or ex-smokers had greater bronchodilator responsiveness than did first-degree male relatives in a study35 examining the gender differences in severe, early onset COPD. In a review article36 on occupational lung disease in women, the authors suggest that although gender differences in effects of exposure have been identified there did not appear to be a "clear pattern" of susceptibility in women. Our report37 on the apparent development of occupational asthma among four cases of newly employed workers in intensive swine production facilities were all women, although we have recently seen several more apparent cases that were in men.38 Whatever the effect on gender, these findings would appear to indicate more of a bronchitis effect than an asthmatic effect as indicated by the symptoms of cough and phlegm as opposed to wheeze. However, the fact that shortness of breath was significant in men but not in women might also indicate a differential gender effect of swine confinement exposures including dust, endotoxin, and other substances.

Certain limitations apply to the study. Although we do have a robust sample size, this is nevertheless not a cohort study, and the limitations of any cross-sectional study apply. In addition, we do not have environmental measurements, but a study23 from Quebec, Canada has shown that that the contaminants in the new larger facilities are if anything as abundant as those in the smaller facilities that they studied. Absence of dust and endotoxin assessments in different production stages (farrowing, nursery, grower/finisher, breeding/gestation) is a major weakness in our study and did not allow us to determine the effects of these exposures on lung function or reported symptoms. In addition, occupational histories prior to working in the swine operations and exposure in these occupations were not available for our study. The control subjects were not matched with swine workers on age and smoking in our study. However, the potential confounding effect of age was controlled in the multivariate logistic regression. To control for potential residual confounding of smoking, a stratified analysis of nonsmokers was conducted, and the results from this analysis were very similar to that from the whole sample.

These studies demonstrate the need for a cohort study to determine the natural history of respiratory dysfunction in full-time workers in the large animal confinement facilities. In future studies, the effects of exposure on gender will require consideration. These studies add to a growing body of evidence indicating that health surveillance programs should be considered for these workers.

Acknowledgements

The authors acknowledge with gratitude the individual swine workers and rural dwellers who participated in the study and the rural towns in Saskatchewan who provided us with their taxation rolls. We recognize the assistance of Ms. Sandra Halliday, RN, and Ms. Natalie Delmaire, RN, who performed many of the tests. The contribution of E. Barber, PhD, C. Rhodes DVM, SaskPork, and the swine production companies in Saskatchewan to the planning and execution of the project is acknowledged and appreciated. Hospitals and communities in rural Saskatchewan have been helpful in providing facilities for testing, and we thank them for their collaboration.

Footnotes

Abbreviations: FEF25–75% = forced expiratory flow between 25% and 75% of FVC; OR = odds ratio

This study was supported by grant MOP-57907 from the Canadian Institutes of Health Research.

The authors have no financial or other potential conflict of interests to disclose.

Received for publication September 20, 2006. Accepted for publication December 13, 2006.

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