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Respiratory Symptoms and Farming Practices in Farmers Associated With an Acute Febrile Illness After Organic Dust Exposure
occupational and environmental lung disease Respiratory Symptoms and Farming Practices in Farmers Associated With an Acute Febrile Illness After Organic Dust Exposure* Susanna Von Essen, MD, FCCP; Jon Fryzek, PhD; Bogdan Nowakowski, MD; and Mary Wampler, MD
Study objective: To conduct a preliminary study of occupational respiratory complaints in farmers who have experienced organic dust toxic syndrome (ODTS) symptoms. Design: Cross-sectional. Setting: An agricultural trade show. Intervention: None. Measurement and results: Two hundred ninety-seven people (204 men, 93 women) completed a questionnaire about agricultural practices, respiratory health (including history of febrile episodes while handling grain), and use of respirators. Spirometry was also performed. ODTS symptoms were described by 107 of the people (36%). A strong significant association was found between ODTS and cough or chest tightness after handling grain (odds ratio [OR], 7.5; 95% confidence ratio [CI], 4.2 to 13.5). People who experienced cough or chest tightness after handling grain were more likely to report handling grain sorghum than people who had not experienced cough or chest tightening after handling grain (OR, 2.1; 95% CI, 1.3 to 3.5). The strong association seen between ODTS and frequent use of a respirator while working in grain bins (OR, 3.9; 95% CI, 1.6 to 9.4) may indicate that farmers began using respirators after respiratory symptoms developed. Conclusions: Having a history consistent with ODTS exposure was very common in the farmers surveyed. Farmers who had a history consistent with ODTS were more likely to report cough or chest tightness with handling grain. Exposure to grain sorghum was more likely to be associated with respiratory symptoms than was exposure to other types of grain. There is a need for additional studies to further examine the relationship between ODTS and respiratory symptoms with grain dust exposure in farmers. (CHEST 1999; 116:1452–1458) Key words: bronchitis; farming; grain dust; organic dust toxic syndrome; swine confinement Abbreviations: CI 5 confidence interval; FEF25–75 5 expiratory flow in the mid portion of the forced exhalation; ODTS 5 organic dust toxic syndrome; OR 5 odds ratio
association between work in production agriT heculture and chronic respiratory symptoms has been recognized medically since the early 1700s.1 *From the Department of Preventive and Societal Medicine (Dr. Fryzek), and the Department of Internal Medicine (Drs. Von Essen, Wampler, and Nowakowski), College of Medicine, University of Nebraska Medical Center, Omaha, NE. Supported by the W.K. Kellogg Foundation. Manuscript received August 18, 1998; revision accepted May 7, 1999. Correspondence to: Susanna Von Essen, MD, FCCP, Pulmonary and Critical Care Medicine Section, Department of Internal Medicine, University of Nebraska Medical Center, Box 985300, Omaha, NE 68198-5300; e-mail: [email protected] 1452
Chronic or recurrent respiratory symptoms are particularly common in farmers who grow different types of grain and soy beans2,3 and in farmers who raise livestock.4 The dusts from grains that appear to For editorial comment see page 1157 cause acute lung inflammation after workplace exposures have also been shown to cause similar responses in controlled laboratory challenges.5,6 When the exposure is large, such as the exposure one may get when cleaning a grain storage bin, an acute Occupational and Environmental Lung Disease
febrile illness often results.7–9 A similar acute febrile illness can be seen after work in swine confinement buildings.10 Approximately 20 years ago, influenza-like febrile reactions to organic dust exposure on the farm were first described in the United States.7 These symptoms are associated with an increase in peripheral blood neutrophils. Unlike acute farmers’ lung, spirometry is normal, as is the diffusing capacity for carbon monoxide and the chest radiograph. While it was once assumed that all of these episodes of illness represented farmer’s lung (a form of hypersensitivity pneumonitis), it is clear that there is a disorder distinct from farmer’s lung and that this disorder is much more common than farmer’s lung.11 There is evidence that true farmer’s lung has become relatively uncommon in much of the United States, including Nebraska.12 The type of febrile reaction is now most often known as organic dust toxic syndrome (ODTS). A variety of other terms have been used to describe it, including grain fever, pulmonary mycotoxicosis, and toxic alveolitis.13 According to a previous study, farmers with bronchial hyperreactivity attributed the onset of their airway disease symptoms to an ODTS-like episode occurring after an abnormally severe dust exposure.14 Malmberg and colleagues15 described ODTS as a common occupational illness in Swedish farmers in which the incidence is 30 to 50 times higher than that of farmer’s lung. Despite the fact that ODTS is an important disease, little cross-sectional or population-based data are available on the prevalence of this disease among farmers in the United States. Furthermore, few epidemiologic studies have examined potential agents that may be involved in the etiology of ODTS. We have recently completed a study of acute febrile illnesses among farmers $ 21 years old in the Midwest. An agricultural trade show, Husker Harvest Days, presented itself as a unique opportunity to gather health information on a large number of farmers. We conducted a survey during a health fair at this trade show to determine the frequency of and risk factors for ODTS illness among a Midwestern farming group.
complete the survey on agricultural exposures and respiratory complaints and undergo spirometry. A total of 404 people completed the questionnaire. Fifty-five people were excluded from the analysis because they did not complete spirometry, and 52 people were excluded because they had a spirogram with a forced expiatory time , 6 s.16 The excluded individuals were slightly younger (though not significantly), were significantly more likely to be women, were not currently farming, and were less likely to have ODTS symptoms or chest tightness after handling grain than those included. The remaining 297 subjects are the focus of this analysis. Questionnaire A self-administered structured questionnaire was used to gather information on the respiratory health and agricultural practices of the study subjects. The questions used to ascertain respiratory health were derived from the American Thoracic Society Epidemiology Standardization Project Questionnaire,17 while the questions on grain handling and ODTS symptoms were developed specifically for this project. Subjects were classified as having a chronic cough if they answered “yes” to all of the following questions: “Do you usually have a cough?”; “Do you usually cough as much as 4 to 6 times a day, 4 or more days out of the week?”; and “Do you usually cough like this on most days for 3 months in a row or more during the year?” Subjects were considered to have chronic bronchitis if they answered “yes” to all of the following questions: “Do you usually bring up phlegm from your chest?”; “Do you usually bring up phlegm like this as much as twice a day, 4 or more days per week?”; and “On most days for 3 or more consecutive months during the year?” Subjects were classified as having organic dust toxic-like syndrome if they had a positive response to the single question, “Have you ever had a flu-like illness consisting of fever, aching and tiredness after working on the farm?” The question, “Do you have cough or chest tightness after handling grain?” was used to classify subjects as having cough or chest tightness after handling grain, Subjects were also asked whether they had ever wheezed and whether they had physician-diagnosed asthma. Current and past agricultural practices were also measured. Subjects were questioned about the crops they handled, their work in swine confinement buildings or on dairy farms, and their use of respirators. Information on the type of respirator worn was not ascertained. Specific lifestyle and demographic factors ascertained included age, sex, race, and cigarette smoking. Spirometry Spirometry was done in triplicate by a trained technician using a spirometer, and the best value was reported (Puritan Bennett Renaissance; Puritan Bennett; Wilmington, MA). Subjects who had a test with a forced expiratory time , 6 s were omitted from the analysis (as noted previously). Interpretation of the findings was done using the Knudson equations for reporting spirometry results.18
Materials and Methods Statistical analysis Subjects We conducted a cross-sectional study among Nebraska farmers attending a health fair at an agricultural trade show, Husker Harvest Days, which was held near Grand Island, Nebraska in September 1996. The opportunity to attend the health fair was advertised to all persons purchasing a ticket for the trade show. Approximately 200,000 people attended the trade fair. Anyone $ 21 years old who had ever lived on a farm was invited to
The data were analyzed using software (SAS Version 6.0; SAS Institute; Cary, NC). Descriptive statistics were used to characterize the study populations. Simple tabulations and percentages were calculated. Univariate analyses were performed to describe differences between the group who reported symptoms consistent with ODTS and the group who did not have ODTS, as well as between the group who reported cough or chest tightness after handling grain and the group who did not have cough or chest CHEST / 116 / 5 / NOVEMBER, 1999
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tightness after handling grain. Multivariate logistic regression analyses were performed to obtain adjusted prevalence odds ratios (ORs) and 95% confidence intervals (CIs) for the associations between agricultural practices, respiratory health, and the two main outcomes of interest (ODTS symptoms and cough or chest tightening after handling any type of grain). Factors included in the model were those found to be significantly associated with the outcomes of interest at p , 0.05 in the univariate analyses. Subjects with missing values for any of the covariates included in the model were deleted from the multivariate logistic regression analyses. The following pulmonary function parameters were examined through spirometry: FVC, FEV1, FEV1/FVC, and expiratory flow in the mid portion of the forced exhalation (FEF25–75). The effects of age, sex, and height were controlled in the reported results by calculating the percentage of predicted pulmonary function. The mean values of each pulmonary function parameter were compared to the two main outcomes of interest (ODTS symptoms and cough or chest tightness after handling any type of grain) by using an analysis of covariance model. This model compares the continuous dependent variables (FVC, FEV1, FEV1/FVC, FEF25–75) to the outcomes of interest while controlling for cigarette smoking (those who have ever smoked cigarettes vs those who have never smoked cigarettes).
Table 1—Characteristics of Study Subjects* Characteristics Age Mean (SD) Gender Men Women Race White Other Cigarette Smoking Never Past Current Missing ODTS history Cough or chest tightness after handling grain Chronic cough Chronic wheeze Physician-diagnosed asthma Chronic bronchitis
No. 53 (15) 204 (69) 93 (31) 290 (98) 7 (2) 199 (67) 67 (23) 22 (7) 9 (3) 107 (36) 106 (36) 40 (14) 51 (17) 12 (4) 23 (8)
*Unless indicated otherwise, values are No. (%).
Results More than ninety-seven percent of the study population (n 5 290) were white with a mean age of 53 years old (SD, 15). Twenty-three percent of the subjects (n 5 67) reported past use of cigarettes while only 7% (n 5 22) reported currently smoking cigarettes. Information on the pack-year history of smoking is not available. One hundred and seven people (36%) reported a history of symptoms consistent with ODTS (95% confidence interval (CI), 31 to 42%) and 106 (36%) reported cough or chest tightness after handling grain (95% CI, 30 to 41%). A smaller proportion of people reported having ever had the other respiratory complaints of interest. Fourteen percent (n 5 40) had a chronic cough, 17% (n 5 51) reported chronic wheeze, 4% (n 5 12) had physician-diagnosed asthma, and 8% (n 5 23) had chronic bronchitis (Table 1). Farming Practices People who worked in swine confinement were almost two times more likely to report ODTS symptoms compared to those who did not work in swine confinement (OR, 2.0; 95% CI, 1.1 to 3.4; Table 2). We also observed suggestive associations between reports of ODTS symptoms and reports of currently farming, handling hay, handling grain sorghum, or handling wheat. Grain sorghum is a type of grain that is used widely in animal feed. It is a major crop in parts of the United States and elsewhere in the world. People who handled grain sorghum on their farms were two times more likely to report cough or chest tightness after handling grain compared to 1454
people who did not handle grain sorghum, and this association was significant (OR, 2.1; 95% CI, 1.3 to 3.5). Suggestive associations between reports of cough or chest tightness after handling grain and reports of currently farming, handling corn, handling hay, or working in swine confinement were also found. Respiratory Conditions We observed no statistically significant associations between ODTS history and chronic cough, chronic bronchitis, wheezing, and physician-diagnosed asthma. In contrast, we found significant associations between subject-reported cough or chest tightness after handling grain and both wheezing (OR, 3.6; 95% CI, 1.8 to 7.1) and physiciandiagnosed asthma (OR, 5.5; 95% CI, 1.4 to 20.7). Of particular interest, people who reported having had ODTS symptoms were 7.5 times more likely to report cough or chest tightness after handling grain (95% CI, 4.2 to 13.5) than were people without a history of ODTS symptoms (Table 3). Spirometry The majority of the people had pulmonary function values within the normal range (n 5 223; 75%). Fifty people (17%) had a borderline obstruction, 12 (4%) had a mild obstruction, 4 (1%) had a moderate obstruction, 2 (1%) had a moderate restriction, and 6 (2%) had a mixed obstruction/restriction. The mean values for FVC, FEV1, FEV1/FVC, and FEF25–75 among people with a history of ODTS were not Occupational and Environmental Lung Disease
Table 2—Prevalence ORs and 95% CIs for Farm Exposures and History of ODTS or Cough or Chest Tightness After Handling Grain* ODTS History
CCT
Data
ODTS/None
OR† (95% CI)
CCT/None
OR (95% CI)
Current farmer Handle corn Handle soy beans Handle grain Sorghum Handle wheat Handle oats Handle hay Swine confinement Dairy farm
83/110 98/51 78/115
1.7 (0.9–3.3) 1.1 (0.5–2.7) 1.0 (0.6–1.8)
85/105 97/143 78/108
1.5 (0.8–3.0) 1.2 (0.5–3.0) 1.2 (0.7–2.1)
58/71 60/79 42/62 90/131 39/41 17/33
1.5 (0.9–2.5) 1.4 (0.9–2.4) 1.0 (0.6–1.7) 1.6 (0.8–3.0) 2.0* (1.1–3.4) 0.9 (0.5–1.8)
61/63 61/73 40/60 88/126 33/43 15/34
2.1‡ (1.3–3.5) 1.4 (0.9–2.4) 0.9 (0.6–1.6) 1.3 (0.9–2.6) 1.2 (0.9–2.1) 0.7 (0.4–1.5)
*CCT 5 cough or chest tightness. †Each OR is adjusted for age, gender, and cigarette smoking. ‡p , 0.05.
significantly different (at p , 0.05) from those without a history of ODTS (Table 4). Similarly, no significant differences in pulmonary function were found for those who had reported cough or chest tightness after handling grain compared to those who did not report having cough or chest tightness after handling grain.
tween ODTS history and those who “sometimes” used respirators compared to those who never used respirators (OR, 3.4; 95% CI, 1.5 to 7.7). No association was found between people who always used respirators in swine confinement and reports of ODTS history. Though the point estimates are not as elevated, a similar pattern of associations was seen for cough or chest tightness after handling grain and respirator use. People who had ever used a respirator were more likely to report cough or chest tightness after handling grain (OR, 2.1; 95% CI, 0.1 to 4.4) than were people who never used a respirator. An elevated borderline significant association was revealed for those who had “sometimes” used a respirator when working in grain bins (OR, 1.9; 95% CI, 1.0 to 3.8). No increased significant association was seen for people who “always” used a respirator when working in grain bins and cough or chest tightness after handling grain. Once again, an increased positive association between cough or chest tightness after handling grain and “sometimes” use of respira-
Use of Respirators As shown in Table 5, people who had used a respirator were 2.7 times more likely to report a history of ODTS compared to people who did not use a respirator (OR, 2.7; 95% CI, 1.3 to 5.9). A significant association was detected between ODTS history and people who “sometimes” used respirators when working in grain bins (OR, 3.4; 95% CI, 1.6 to 7.1), or between people who “always” used respirators when working in grain bins (OR, 3.9; 95% CI, 1.6 to 9.4) and people who never used respirators. For people who used respirators in swine confinement, a significant association was discovered be-
Table 3—Prevalence ORs and 95% CIs for Respiratory Conditions and History of ODTS or Cough or Chest Tightness After Handling Grain* ODTS History
Chronic cough Chronic bronchitis Wheeze Physician-diagnosed asthma CCT
CCT After Handling Grain
ODTS/None
OR† (95% CI)
CCT/None
OR (95% CI)
19/20 11/12 23/25 5/6 69/36
1.6 (0.8–3.2) 1.7 (0.7–4.1) 1.9 (1.0–3.6) 1.7 (0.5–5.9) 7.5 (4.2–13.5)
19/17 12/10 29/20 8/4
2.0 (1.0–4.3) 2.6 (1.0–6.7) 3.6 (1.8–7.1) 5.5 (1.4–20.7)
*See Table 2 for abbreviation. †Each odds ratio is adjusted for age, gender, and cigarette smoking. CHEST / 116 / 5 / NOVEMBER, 1999
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Table 4 —Adjusted Means and Corresponding SDs for Pulmonary Function Among Those With a History of ODTS and Those With Cough or Chest Tightness After Handling Grain* ODTS History (Present)
ODTS History (Absent)
CCT (Present)
CCT (Absent)
Pulmonary Function
N
Mean
SD
N
Mean
SD
p Value
N
Mean
SD
N
Mean
SD
p Value
FVC FEV1 FEV1/FVC FEF25–75
106 106 106 106
115.6 108.1 93.2 90.4
3.3 3.5 0.9 4.6
172 172 172 172
116.4 108.7 92.8 92.3
2.6 2.8 0.7 3.6
0.95 0.92 0.30 0.38
105 105 105 105
117.1 109.6 93.4 90.9
3.3 3.5 0.9 4.5
164 164 164 164
116.3 108.8 93.0 93.3
2.7 2.8 0.7 3.6
0.91 0.96 0.53 0.43
*Results are adjusted for cigarette smoking. Those subjects with missing values were deleted from these analyses. Reported values are percent predicted values. See Table 2 for abbreviation.
tors when working in swine confinement was seen, but this association was not significant. Discussion ODTS is a very common clinical problem in Midwestern farmers. In our study, farmers indicated that they were more susceptible to developing cough or chest tightness after handling grain if they had also reported an illness consistent with ODTS. While one cannot be absolutely certain that the febrile illnesses described in this manuscript were ODTS, the low frequency of restrictive findings on spirometry argues against these illnesses having been episodes of acute hypersensitivity pneumonitis. Although restrictive changes on spirometry may resolve following farmer’s lung, one recent study has shown that some abnormalities often remain.19 Furthermore, there was no significant difference between the mean values of the pulmonary function parameters for those with either one of the outcomes of interest (either ODTS history or cough or chest tightness after handling grain) and those without the outcomes of interest. This is one of the first studies to look at the
association between ODTS and cough or chest tightness after handling grain. Investigators conducting a previous study looking at a small number of farmers with an ODTS history failed to find evidence of abnormalities on pulmonary function testing and concluded that ODTS had no sequelae.14 It is important to note that it is possible to have pulmonary complaints without objective evidence of pulmonary function test changes, particularly during a time when exposure is not taking place. It is also known that farm workers exposed to grain dust and animal confinement unit environments can have respiratory complaints without pulmonary function test values falling below the normal range.2,4,20,21 Enhanced airways reactivity with spirometric values in the normal range has been observed in grain handlers.22 Furthermore, persistent symptoms with normal pulmonary function tests have been described after exposure to irritant chemicals, a syndrome known as reactive airway dysfunction syndrome.23 All of these studies suggest that chronic respiratory complaints can be diagnosed in individuals with normal spirometry. People who reported cough or chest tightness after handling grain were more likely to report
Table 5—Prevalence ORs and 95% CIs for Use of Respirators and History of ODTS or after Handling Grain* ODTS History Data
ODTS/None
CCT After Handling Grain OR† (95% CI)
Any use 85/109 2.7‡ (1.3–5.9) Use respirator when working in grain bins Never 13/50 1.0 (reference) Sometimes 58/69 3.4‡ (1.6–7.1) Always 24/24 3.9‡ (1.6–9.4) Use respirator when working in swine confinement buildings Never 21/52 1.0 (reference) Sometimes 23/19 3.4‡ (1.5–7.7) Always 2/4 0.9 (0.1–5.8)
CCT/None
OR (95% CI)
87/101
2.1 (0.1–4.4)
18/44 59/64 21/26
1.0 (reference) 1.9 (1.0–3.8) 1.5 (0.6–3.4)
26/45 19/21 2/4
1.0 (reference) 1.8 (0.8–4.3) 0.3 (0.1–2.2)
*See Table 2 for abbreviation. †Each odds ratio is adjusted for age, gender, and cigarette smoking. ‡p , 0.05. 1456
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handling grain sorghum than were those who did not report cough or chest tightness after handling grain. A similar borderline significant increased risk was seen for the association between ODTS history and grain sorghum. It is of interest that cough or chest tightness after handling grain was reported more commonly after handling grain sorghum than after other types of grain. Laboratory experiments suggest that various types of grain dusts differ in their ability to cause an inflammatory reaction. Grain sorghum dust causes a more pronounced inflammatory response in vitro than do the dusts from corn and soy beans.24,25 Even though a history of ODTS symptoms was very common, significant associations could not be established between handling specific types of grains (corn, oats, grain sorghum or soybeans) or hay and experiencing the ODTS syndrome. Other studies have also shown that grain dusts are an important respiratory hazard.26 However, it has been suggested that the microbial contamination of the organic material and the resultant high endotoxin levels may cause the ODTS symptoms, not the organic material itself.27,28 It is of note that all study subjects had reported handling at least one of the grains mentioned on the survey. Therefore, the unexposed group for a specific grain contained individuals who were exposed to other grains. Potential confounding by exposure to other grains was adjusted for in these analyses. A relatively large percentage of farmers stated that they sometimes wear respirators when handling grain or working in swine confinement buildings. However, the majority of workers did not describe wearing them all of the time. It is interesting that there was a strong association between wearing respirators and having experienced ODTS. It is likely that prior to experiencing ODTS, they were not wearing respirators, and this illness may have convinced them of the value of wearing respiratory protection. A study in South Dakota found a similar result.29 Farmers who wore respirators were more likely to report having cough, phlegm, and wheezing. Our study showed a similar, though not as profound, effect for farmers who used respirators when working in swine confinement buildings. A study in Canada of swine producers demonstrated the value of wearing respirators in swine confinement buildings. The respiratory health of workers who wore respirators for preventive reasons was significantly better than that of workers who wore respirators because of symptoms. This study further demonstrates a need to increase respirator use for preventive reasons because of their documented effectiveness in decreasing the prevalence of respiratory illnesses in agricultural settings.30 –32
This study was cross-sectional in nature, and the subjects were not selected in a random manner. We were concerned that only the least healthy people at the trade show would participate in the health fair. To evaluate this potential bias, we included questions on hypertension and diabetes in our survey (two conditions that are not associated with respiratory illnesses) to see if the individuals at the health fair were more unhealthy than the general population of Nebraska. In our study, only 2.0% of men and 2.2% of women had physician-diagnosed diabetes. In Nebraska, the prevalence of physician-diagnosed diabetes is 5% in men and 6% in women.33 In our survey, 18.1% of men and 25.8% of women said that a physician had indicated that they had hypertension. In Nebraska, the prevalence of physician-diagnosed hypertension is 22% in men and 23% in women.33 These data demonstrate that our study population was probably not less healthy than the general population of Nebraska. Still, the presence of selection bias must be considered in the interpretation of the results. There is a need for future studies in which the subjects are randomly selected. Given the limitations of the cross-sectional study design, we could not determine if the exposures occurred before or after the main outcomes (ODTS or cough or chest tightness after handling grain). Furthermore, establishing a diagnosis of ODTS with certainty in a retrospective fashion is not possible. The strong, significant association between having an ODTS illness and a susceptibility to developing cough or chest tightness after handling grain raises some questions that can be answered only with a prospective, population-based study. It is important to determine in future prospective studies if the febrile, influenza-like illness precedes the onset of the other complaints. If this is so, this makes a strong case for encouraging workers to use respirators designed for use in dusty environments while handling grain or while working in swine confinement buildings. ACKNOWLEDGMENT: The authors wish to thank Nancy Bolin, Molly Smith, and Heather Eberspacher for their capable assistance in data collection during Husker Harvest Days; and David Howe, editor of the Nebraska Farmer Magazine, for giving us access to the trade show. We would also like to express appreciation to Dr. Paul Blanc for his helpful suggestions. We are grateful to Pat Schott for her assistance with manuscript preparation.
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normal maximal expiratory flow-volume curve with growth and aging. Am Rev Respir Dis 1983; 127:725–734 Kokkarinen JI, Tukiainen HO, Terho EO. Recovery of pulmonary function in farmer’s lung. Am Rev Respir Dis 1993; 147:793–796 Dosman JA, Graham BL, Hall D, et al. Respiratory symptoms and alterations in pulmonary function tests in swine producers in Saskatchewan: results of a survey of farmers. J Occup Med 1988; 30:715–720 Carvalheiro MF, Peterson Y, Rylander R. Bronchial reactivity and work-related symptoms in farmers. Am J Ind Med 1995; 27:65–74 Schwartz DA, Thorne PS, Yagla SJ, et al. The role of endotoxin in grain dust-induced lung disease. Am J Respir Crit Care Med 1995; 152:603– 608 Blanc PD, Galbo M, Hiatt P, et al. Symptoms, lung function and airway responsiveness following irritant inhalation. Chest 1993; 103:1699 –1705 Von Essen SG, Robbins RA, Thompson AB. Mechanisms of neutrophil recruitment to the lung by grain dust exposure. Am Rev Respir Dis 1988; 138:2147–2154 Von Essen SG, O’Neill DP, Olenchock S, et al. Grain dusts and grain plant components vary in their ability to recruit neutrophils. J Toxicol Environ Health 1995; 108:1425–1433 Chan-Yeung M, Enarson D, Kennedy S. The impact of grain dust on respiratory health. Am Rev Respir Dis 1992; 145: 476 – 487 Rask-Andersen A, Malmberg P, Lundholm L. Endotoxin levels in farming: absence of symptoms despite high exposure levels. Brit J Ind Med 1989; 46:412– 416 Olenchock SA, May JJ, Pratt DS, et al. Endotoxins in the agricultural environment. Am J Ind Med 1986; 10:323–324 Schlenker EH, Parry RR. Utilization of masks by Hutterite farmers. S D J Med 1990; 43:13–17 Pickrell JA, Heber AJ, Murphy JP, et al. Endotoxin, ammonia and total and respirable dust in swine confinement buildings: the effect of recirculated air and respiratory protective masks. In: Proceedings from The Kansas State University Swine Day. Manhattan, Kansas: Kansas State University, 1992; 167–172 Zejda JE, Hurst TS, Barber EM, et al. Respiratory health status in swine producers using respiratory protective devices. Am J Ind Med 1993; 23:743–750 Mueller-Wening D, Repp H. Investigation on the protective value of breathing masks in farmer’s lung using an inhalation provocation test. Chest 1989; 95:100 –105 Nebraska Behavioral Risk Factor Surveillance System. Lincoln, Nebraska: Nebraska Department of Health, 1993 to 1994
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Study objective: To conduct a preliminary study of occupational respiratory complaints in farmers who have experienced organic dust toxic syndrome (ODTS) symptoms. Design: Cross-sectional. Setting: An agricultural trade show. Intervention: None. Measurement and results: Two hundred ninety-seven people (204 men, 93 women) completed a questionnaire about agricultural practices, respiratory health (including history of febrile episodes while handling grain), and use of respirators. Spirometry was also performed. ODTS symptoms were described by 107 of the people (36%). A strong significant association was found between ODTS and cough or chest tightness after handling grain (odds ratio [OR], 7.5; 95% confidence ratio [CI], 4.2 to 13.5). People who experienced cough or chest tightness after handling grain were more likely to report handling grain sorghum than people who had not experienced cough or chest tightening after handling grain (OR, 2.1; 95% CI, 1.3 to 3.5). The strong association seen between ODTS and frequent use of a respirator while working in grain bins (OR, 3.9; 95% CI, 1.6 to 9.4) may indicate that farmers began using respirators after respiratory symptoms developed. Conclusions: Having a history consistent with ODTS exposure was very common in the farmers surveyed. Farmers who had a history consistent with ODTS were more likely to report cough or chest tightness with handling grain. Exposure to grain sorghum was more likely to be associated with respiratory symptoms than was exposure to other types of grain. There is a need for additional studies to further examine the relationship between ODTS and respiratory symptoms with grain dust exposure in farmers. (CHEST 1999; 116:1452–1458) Key words: bronchitis; farming; grain dust; organic dust toxic syndrome; swine confinement Abbreviations: CI 5 confidence interval; FEF25–75 5 expiratory flow in the mid portion of the forced exhalation; ODTS 5 organic dust toxic syndrome; OR 5 odds ratio
association between work in production agriT heculture and chronic respiratory symptoms has been recognized medically since the early 1700s.1 *From the Department of Preventive and Societal Medicine (Dr. Fryzek), and the Department of Internal Medicine (Drs. Von Essen, Wampler, and Nowakowski), College of Medicine, University of Nebraska Medical Center, Omaha, NE. Supported by the W.K. Kellogg Foundation. Manuscript received August 18, 1998; revision accepted May 7, 1999. Correspondence to: Susanna Von Essen, MD, FCCP, Pulmonary and Critical Care Medicine Section, Department of Internal Medicine, University of Nebraska Medical Center, Box 985300, Omaha, NE 68198-5300; e-mail: [email protected] 1452
Chronic or recurrent respiratory symptoms are particularly common in farmers who grow different types of grain and soy beans2,3 and in farmers who raise livestock.4 The dusts from grains that appear to For editorial comment see page 1157 cause acute lung inflammation after workplace exposures have also been shown to cause similar responses in controlled laboratory challenges.5,6 When the exposure is large, such as the exposure one may get when cleaning a grain storage bin, an acute Occupational and Environmental Lung Disease
febrile illness often results.7–9 A similar acute febrile illness can be seen after work in swine confinement buildings.10 Approximately 20 years ago, influenza-like febrile reactions to organic dust exposure on the farm were first described in the United States.7 These symptoms are associated with an increase in peripheral blood neutrophils. Unlike acute farmers’ lung, spirometry is normal, as is the diffusing capacity for carbon monoxide and the chest radiograph. While it was once assumed that all of these episodes of illness represented farmer’s lung (a form of hypersensitivity pneumonitis), it is clear that there is a disorder distinct from farmer’s lung and that this disorder is much more common than farmer’s lung.11 There is evidence that true farmer’s lung has become relatively uncommon in much of the United States, including Nebraska.12 The type of febrile reaction is now most often known as organic dust toxic syndrome (ODTS). A variety of other terms have been used to describe it, including grain fever, pulmonary mycotoxicosis, and toxic alveolitis.13 According to a previous study, farmers with bronchial hyperreactivity attributed the onset of their airway disease symptoms to an ODTS-like episode occurring after an abnormally severe dust exposure.14 Malmberg and colleagues15 described ODTS as a common occupational illness in Swedish farmers in which the incidence is 30 to 50 times higher than that of farmer’s lung. Despite the fact that ODTS is an important disease, little cross-sectional or population-based data are available on the prevalence of this disease among farmers in the United States. Furthermore, few epidemiologic studies have examined potential agents that may be involved in the etiology of ODTS. We have recently completed a study of acute febrile illnesses among farmers $ 21 years old in the Midwest. An agricultural trade show, Husker Harvest Days, presented itself as a unique opportunity to gather health information on a large number of farmers. We conducted a survey during a health fair at this trade show to determine the frequency of and risk factors for ODTS illness among a Midwestern farming group.
complete the survey on agricultural exposures and respiratory complaints and undergo spirometry. A total of 404 people completed the questionnaire. Fifty-five people were excluded from the analysis because they did not complete spirometry, and 52 people were excluded because they had a spirogram with a forced expiatory time , 6 s.16 The excluded individuals were slightly younger (though not significantly), were significantly more likely to be women, were not currently farming, and were less likely to have ODTS symptoms or chest tightness after handling grain than those included. The remaining 297 subjects are the focus of this analysis. Questionnaire A self-administered structured questionnaire was used to gather information on the respiratory health and agricultural practices of the study subjects. The questions used to ascertain respiratory health were derived from the American Thoracic Society Epidemiology Standardization Project Questionnaire,17 while the questions on grain handling and ODTS symptoms were developed specifically for this project. Subjects were classified as having a chronic cough if they answered “yes” to all of the following questions: “Do you usually have a cough?”; “Do you usually cough as much as 4 to 6 times a day, 4 or more days out of the week?”; and “Do you usually cough like this on most days for 3 months in a row or more during the year?” Subjects were considered to have chronic bronchitis if they answered “yes” to all of the following questions: “Do you usually bring up phlegm from your chest?”; “Do you usually bring up phlegm like this as much as twice a day, 4 or more days per week?”; and “On most days for 3 or more consecutive months during the year?” Subjects were classified as having organic dust toxic-like syndrome if they had a positive response to the single question, “Have you ever had a flu-like illness consisting of fever, aching and tiredness after working on the farm?” The question, “Do you have cough or chest tightness after handling grain?” was used to classify subjects as having cough or chest tightness after handling grain, Subjects were also asked whether they had ever wheezed and whether they had physician-diagnosed asthma. Current and past agricultural practices were also measured. Subjects were questioned about the crops they handled, their work in swine confinement buildings or on dairy farms, and their use of respirators. Information on the type of respirator worn was not ascertained. Specific lifestyle and demographic factors ascertained included age, sex, race, and cigarette smoking. Spirometry Spirometry was done in triplicate by a trained technician using a spirometer, and the best value was reported (Puritan Bennett Renaissance; Puritan Bennett; Wilmington, MA). Subjects who had a test with a forced expiratory time , 6 s were omitted from the analysis (as noted previously). Interpretation of the findings was done using the Knudson equations for reporting spirometry results.18
Materials and Methods Statistical analysis Subjects We conducted a cross-sectional study among Nebraska farmers attending a health fair at an agricultural trade show, Husker Harvest Days, which was held near Grand Island, Nebraska in September 1996. The opportunity to attend the health fair was advertised to all persons purchasing a ticket for the trade show. Approximately 200,000 people attended the trade fair. Anyone $ 21 years old who had ever lived on a farm was invited to
The data were analyzed using software (SAS Version 6.0; SAS Institute; Cary, NC). Descriptive statistics were used to characterize the study populations. Simple tabulations and percentages were calculated. Univariate analyses were performed to describe differences between the group who reported symptoms consistent with ODTS and the group who did not have ODTS, as well as between the group who reported cough or chest tightness after handling grain and the group who did not have cough or chest CHEST / 116 / 5 / NOVEMBER, 1999
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tightness after handling grain. Multivariate logistic regression analyses were performed to obtain adjusted prevalence odds ratios (ORs) and 95% confidence intervals (CIs) for the associations between agricultural practices, respiratory health, and the two main outcomes of interest (ODTS symptoms and cough or chest tightening after handling any type of grain). Factors included in the model were those found to be significantly associated with the outcomes of interest at p , 0.05 in the univariate analyses. Subjects with missing values for any of the covariates included in the model were deleted from the multivariate logistic regression analyses. The following pulmonary function parameters were examined through spirometry: FVC, FEV1, FEV1/FVC, and expiratory flow in the mid portion of the forced exhalation (FEF25–75). The effects of age, sex, and height were controlled in the reported results by calculating the percentage of predicted pulmonary function. The mean values of each pulmonary function parameter were compared to the two main outcomes of interest (ODTS symptoms and cough or chest tightness after handling any type of grain) by using an analysis of covariance model. This model compares the continuous dependent variables (FVC, FEV1, FEV1/FVC, FEF25–75) to the outcomes of interest while controlling for cigarette smoking (those who have ever smoked cigarettes vs those who have never smoked cigarettes).
Table 1—Characteristics of Study Subjects* Characteristics Age Mean (SD) Gender Men Women Race White Other Cigarette Smoking Never Past Current Missing ODTS history Cough or chest tightness after handling grain Chronic cough Chronic wheeze Physician-diagnosed asthma Chronic bronchitis
No. 53 (15) 204 (69) 93 (31) 290 (98) 7 (2) 199 (67) 67 (23) 22 (7) 9 (3) 107 (36) 106 (36) 40 (14) 51 (17) 12 (4) 23 (8)
*Unless indicated otherwise, values are No. (%).
Results More than ninety-seven percent of the study population (n 5 290) were white with a mean age of 53 years old (SD, 15). Twenty-three percent of the subjects (n 5 67) reported past use of cigarettes while only 7% (n 5 22) reported currently smoking cigarettes. Information on the pack-year history of smoking is not available. One hundred and seven people (36%) reported a history of symptoms consistent with ODTS (95% confidence interval (CI), 31 to 42%) and 106 (36%) reported cough or chest tightness after handling grain (95% CI, 30 to 41%). A smaller proportion of people reported having ever had the other respiratory complaints of interest. Fourteen percent (n 5 40) had a chronic cough, 17% (n 5 51) reported chronic wheeze, 4% (n 5 12) had physician-diagnosed asthma, and 8% (n 5 23) had chronic bronchitis (Table 1). Farming Practices People who worked in swine confinement were almost two times more likely to report ODTS symptoms compared to those who did not work in swine confinement (OR, 2.0; 95% CI, 1.1 to 3.4; Table 2). We also observed suggestive associations between reports of ODTS symptoms and reports of currently farming, handling hay, handling grain sorghum, or handling wheat. Grain sorghum is a type of grain that is used widely in animal feed. It is a major crop in parts of the United States and elsewhere in the world. People who handled grain sorghum on their farms were two times more likely to report cough or chest tightness after handling grain compared to 1454
people who did not handle grain sorghum, and this association was significant (OR, 2.1; 95% CI, 1.3 to 3.5). Suggestive associations between reports of cough or chest tightness after handling grain and reports of currently farming, handling corn, handling hay, or working in swine confinement were also found. Respiratory Conditions We observed no statistically significant associations between ODTS history and chronic cough, chronic bronchitis, wheezing, and physician-diagnosed asthma. In contrast, we found significant associations between subject-reported cough or chest tightness after handling grain and both wheezing (OR, 3.6; 95% CI, 1.8 to 7.1) and physiciandiagnosed asthma (OR, 5.5; 95% CI, 1.4 to 20.7). Of particular interest, people who reported having had ODTS symptoms were 7.5 times more likely to report cough or chest tightness after handling grain (95% CI, 4.2 to 13.5) than were people without a history of ODTS symptoms (Table 3). Spirometry The majority of the people had pulmonary function values within the normal range (n 5 223; 75%). Fifty people (17%) had a borderline obstruction, 12 (4%) had a mild obstruction, 4 (1%) had a moderate obstruction, 2 (1%) had a moderate restriction, and 6 (2%) had a mixed obstruction/restriction. The mean values for FVC, FEV1, FEV1/FVC, and FEF25–75 among people with a history of ODTS were not Occupational and Environmental Lung Disease
Table 2—Prevalence ORs and 95% CIs for Farm Exposures and History of ODTS or Cough or Chest Tightness After Handling Grain* ODTS History
CCT
Data
ODTS/None
OR† (95% CI)
CCT/None
OR (95% CI)
Current farmer Handle corn Handle soy beans Handle grain Sorghum Handle wheat Handle oats Handle hay Swine confinement Dairy farm
83/110 98/51 78/115
1.7 (0.9–3.3) 1.1 (0.5–2.7) 1.0 (0.6–1.8)
85/105 97/143 78/108
1.5 (0.8–3.0) 1.2 (0.5–3.0) 1.2 (0.7–2.1)
58/71 60/79 42/62 90/131 39/41 17/33
1.5 (0.9–2.5) 1.4 (0.9–2.4) 1.0 (0.6–1.7) 1.6 (0.8–3.0) 2.0* (1.1–3.4) 0.9 (0.5–1.8)
61/63 61/73 40/60 88/126 33/43 15/34
2.1‡ (1.3–3.5) 1.4 (0.9–2.4) 0.9 (0.6–1.6) 1.3 (0.9–2.6) 1.2 (0.9–2.1) 0.7 (0.4–1.5)
*CCT 5 cough or chest tightness. †Each OR is adjusted for age, gender, and cigarette smoking. ‡p , 0.05.
significantly different (at p , 0.05) from those without a history of ODTS (Table 4). Similarly, no significant differences in pulmonary function were found for those who had reported cough or chest tightness after handling grain compared to those who did not report having cough or chest tightness after handling grain.
tween ODTS history and those who “sometimes” used respirators compared to those who never used respirators (OR, 3.4; 95% CI, 1.5 to 7.7). No association was found between people who always used respirators in swine confinement and reports of ODTS history. Though the point estimates are not as elevated, a similar pattern of associations was seen for cough or chest tightness after handling grain and respirator use. People who had ever used a respirator were more likely to report cough or chest tightness after handling grain (OR, 2.1; 95% CI, 0.1 to 4.4) than were people who never used a respirator. An elevated borderline significant association was revealed for those who had “sometimes” used a respirator when working in grain bins (OR, 1.9; 95% CI, 1.0 to 3.8). No increased significant association was seen for people who “always” used a respirator when working in grain bins and cough or chest tightness after handling grain. Once again, an increased positive association between cough or chest tightness after handling grain and “sometimes” use of respira-
Use of Respirators As shown in Table 5, people who had used a respirator were 2.7 times more likely to report a history of ODTS compared to people who did not use a respirator (OR, 2.7; 95% CI, 1.3 to 5.9). A significant association was detected between ODTS history and people who “sometimes” used respirators when working in grain bins (OR, 3.4; 95% CI, 1.6 to 7.1), or between people who “always” used respirators when working in grain bins (OR, 3.9; 95% CI, 1.6 to 9.4) and people who never used respirators. For people who used respirators in swine confinement, a significant association was discovered be-
Table 3—Prevalence ORs and 95% CIs for Respiratory Conditions and History of ODTS or Cough or Chest Tightness After Handling Grain* ODTS History
Chronic cough Chronic bronchitis Wheeze Physician-diagnosed asthma CCT
CCT After Handling Grain
ODTS/None
OR† (95% CI)
CCT/None
OR (95% CI)
19/20 11/12 23/25 5/6 69/36
1.6 (0.8–3.2) 1.7 (0.7–4.1) 1.9 (1.0–3.6) 1.7 (0.5–5.9) 7.5 (4.2–13.5)
19/17 12/10 29/20 8/4
2.0 (1.0–4.3) 2.6 (1.0–6.7) 3.6 (1.8–7.1) 5.5 (1.4–20.7)
*See Table 2 for abbreviation. †Each odds ratio is adjusted for age, gender, and cigarette smoking. CHEST / 116 / 5 / NOVEMBER, 1999
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Table 4 —Adjusted Means and Corresponding SDs for Pulmonary Function Among Those With a History of ODTS and Those With Cough or Chest Tightness After Handling Grain* ODTS History (Present)
ODTS History (Absent)
CCT (Present)
CCT (Absent)
Pulmonary Function
N
Mean
SD
N
Mean
SD
p Value
N
Mean
SD
N
Mean
SD
p Value
FVC FEV1 FEV1/FVC FEF25–75
106 106 106 106
115.6 108.1 93.2 90.4
3.3 3.5 0.9 4.6
172 172 172 172
116.4 108.7 92.8 92.3
2.6 2.8 0.7 3.6
0.95 0.92 0.30 0.38
105 105 105 105
117.1 109.6 93.4 90.9
3.3 3.5 0.9 4.5
164 164 164 164
116.3 108.8 93.0 93.3
2.7 2.8 0.7 3.6
0.91 0.96 0.53 0.43
*Results are adjusted for cigarette smoking. Those subjects with missing values were deleted from these analyses. Reported values are percent predicted values. See Table 2 for abbreviation.
tors when working in swine confinement was seen, but this association was not significant. Discussion ODTS is a very common clinical problem in Midwestern farmers. In our study, farmers indicated that they were more susceptible to developing cough or chest tightness after handling grain if they had also reported an illness consistent with ODTS. While one cannot be absolutely certain that the febrile illnesses described in this manuscript were ODTS, the low frequency of restrictive findings on spirometry argues against these illnesses having been episodes of acute hypersensitivity pneumonitis. Although restrictive changes on spirometry may resolve following farmer’s lung, one recent study has shown that some abnormalities often remain.19 Furthermore, there was no significant difference between the mean values of the pulmonary function parameters for those with either one of the outcomes of interest (either ODTS history or cough or chest tightness after handling grain) and those without the outcomes of interest. This is one of the first studies to look at the
association between ODTS and cough or chest tightness after handling grain. Investigators conducting a previous study looking at a small number of farmers with an ODTS history failed to find evidence of abnormalities on pulmonary function testing and concluded that ODTS had no sequelae.14 It is important to note that it is possible to have pulmonary complaints without objective evidence of pulmonary function test changes, particularly during a time when exposure is not taking place. It is also known that farm workers exposed to grain dust and animal confinement unit environments can have respiratory complaints without pulmonary function test values falling below the normal range.2,4,20,21 Enhanced airways reactivity with spirometric values in the normal range has been observed in grain handlers.22 Furthermore, persistent symptoms with normal pulmonary function tests have been described after exposure to irritant chemicals, a syndrome known as reactive airway dysfunction syndrome.23 All of these studies suggest that chronic respiratory complaints can be diagnosed in individuals with normal spirometry. People who reported cough or chest tightness after handling grain were more likely to report
Table 5—Prevalence ORs and 95% CIs for Use of Respirators and History of ODTS or after Handling Grain* ODTS History Data
ODTS/None
CCT After Handling Grain OR† (95% CI)
Any use 85/109 2.7‡ (1.3–5.9) Use respirator when working in grain bins Never 13/50 1.0 (reference) Sometimes 58/69 3.4‡ (1.6–7.1) Always 24/24 3.9‡ (1.6–9.4) Use respirator when working in swine confinement buildings Never 21/52 1.0 (reference) Sometimes 23/19 3.4‡ (1.5–7.7) Always 2/4 0.9 (0.1–5.8)
CCT/None
OR (95% CI)
87/101
2.1 (0.1–4.4)
18/44 59/64 21/26
1.0 (reference) 1.9 (1.0–3.8) 1.5 (0.6–3.4)
26/45 19/21 2/4
1.0 (reference) 1.8 (0.8–4.3) 0.3 (0.1–2.2)
*See Table 2 for abbreviation. †Each odds ratio is adjusted for age, gender, and cigarette smoking. ‡p , 0.05. 1456
Occupational and Environmental Lung Disease
handling grain sorghum than were those who did not report cough or chest tightness after handling grain. A similar borderline significant increased risk was seen for the association between ODTS history and grain sorghum. It is of interest that cough or chest tightness after handling grain was reported more commonly after handling grain sorghum than after other types of grain. Laboratory experiments suggest that various types of grain dusts differ in their ability to cause an inflammatory reaction. Grain sorghum dust causes a more pronounced inflammatory response in vitro than do the dusts from corn and soy beans.24,25 Even though a history of ODTS symptoms was very common, significant associations could not be established between handling specific types of grains (corn, oats, grain sorghum or soybeans) or hay and experiencing the ODTS syndrome. Other studies have also shown that grain dusts are an important respiratory hazard.26 However, it has been suggested that the microbial contamination of the organic material and the resultant high endotoxin levels may cause the ODTS symptoms, not the organic material itself.27,28 It is of note that all study subjects had reported handling at least one of the grains mentioned on the survey. Therefore, the unexposed group for a specific grain contained individuals who were exposed to other grains. Potential confounding by exposure to other grains was adjusted for in these analyses. A relatively large percentage of farmers stated that they sometimes wear respirators when handling grain or working in swine confinement buildings. However, the majority of workers did not describe wearing them all of the time. It is interesting that there was a strong association between wearing respirators and having experienced ODTS. It is likely that prior to experiencing ODTS, they were not wearing respirators, and this illness may have convinced them of the value of wearing respiratory protection. A study in South Dakota found a similar result.29 Farmers who wore respirators were more likely to report having cough, phlegm, and wheezing. Our study showed a similar, though not as profound, effect for farmers who used respirators when working in swine confinement buildings. A study in Canada of swine producers demonstrated the value of wearing respirators in swine confinement buildings. The respiratory health of workers who wore respirators for preventive reasons was significantly better than that of workers who wore respirators because of symptoms. This study further demonstrates a need to increase respirator use for preventive reasons because of their documented effectiveness in decreasing the prevalence of respiratory illnesses in agricultural settings.30 –32
This study was cross-sectional in nature, and the subjects were not selected in a random manner. We were concerned that only the least healthy people at the trade show would participate in the health fair. To evaluate this potential bias, we included questions on hypertension and diabetes in our survey (two conditions that are not associated with respiratory illnesses) to see if the individuals at the health fair were more unhealthy than the general population of Nebraska. In our study, only 2.0% of men and 2.2% of women had physician-diagnosed diabetes. In Nebraska, the prevalence of physician-diagnosed diabetes is 5% in men and 6% in women.33 In our survey, 18.1% of men and 25.8% of women said that a physician had indicated that they had hypertension. In Nebraska, the prevalence of physician-diagnosed hypertension is 22% in men and 23% in women.33 These data demonstrate that our study population was probably not less healthy than the general population of Nebraska. Still, the presence of selection bias must be considered in the interpretation of the results. There is a need for future studies in which the subjects are randomly selected. Given the limitations of the cross-sectional study design, we could not determine if the exposures occurred before or after the main outcomes (ODTS or cough or chest tightness after handling grain). Furthermore, establishing a diagnosis of ODTS with certainty in a retrospective fashion is not possible. The strong, significant association between having an ODTS illness and a susceptibility to developing cough or chest tightness after handling grain raises some questions that can be answered only with a prospective, population-based study. It is important to determine in future prospective studies if the febrile, influenza-like illness precedes the onset of the other complaints. If this is so, this makes a strong case for encouraging workers to use respirators designed for use in dusty environments while handling grain or while working in swine confinement buildings. ACKNOWLEDGMENT: The authors wish to thank Nancy Bolin, Molly Smith, and Heather Eberspacher for their capable assistance in data collection during Husker Harvest Days; and David Howe, editor of the Nebraska Farmer Magazine, for giving us access to the trade show. We would also like to express appreciation to Dr. Paul Blanc for his helpful suggestions. We are grateful to Pat Schott for her assistance with manuscript preparation.
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Occupational and Environmental Lung Disease