Persistence of respiratory symptoms in ex-underground iron ore miners

Occupational Medicine 2006;56:380 385 Published online 9 June 2006 doi:10.1093/occmed/kql035 Persistence of respiratory symptoms in ex-underground iron ore miners Ulf Hedlund 1,2,B.Järvholm 1 and B. Lundbäck 2,3 Aims To assess the persistence of respiratory symptoms in ex-miners after cessation of mining exposure. Methods Population-based cross-sectional study using a postal questionnaire comparing prevalence of symptoms between ex-miners who had stopped mining at least 1 year before the study and referents not occupationally exposed to irritants or dust. Age, smoking and a family history of asthma were considered as possible confounders in the analysis. Results A total of 206 ex-miners and 4560 referents participated. Ex-miners had on average been working as miners for 13 years and had stopped mining 16 years before the study. Chronic productive cough and physician-diagnosed chronic bronchitis were significantly more common among ex-miners (P, 0.05 and,0.01, respectively). Furthermore, there was a trend that other respiratory symptoms were more common in ex-miners. Conclusion Ex-miners had an increased risk of chronic productive cough and physician-diagnosed chronic bronchitis many years after they had stopped working as a miner. Key words Asthma; chronic bronchitis; epidemiology; ex-miners; respiratory symptoms; smoking cessation. Introduction Occupational exposure to air pollutants is a major cause of respiratory symptoms and diseases in workers [1 6], e.g. in coal mining [7,8] and metal mining [9,10]. Common symptoms are chronic cough and increased sputum production, i.e. symptoms common in chronic bronchitis. Population attributable risks of 15% have been reported for chronic obstructive pulmonary disease (COPD) and physician-diagnosed chronic bronchitis [2,11,12], 10 15% for asthma or asthma-like symptoms [6,11,13] and 15% for breathlessness and wheeze in one study [11], and somewhat lower figures in another, 9% for breathlessness and 6% for wheeze [6]. Respiratory symptoms are common in smokers. One study found an increased risk only in smoking iron miners [9] while a few studies of iron miners have found no increased risk attributable to air pollutants in the mines [14,15]. 1 Occupational Medicine, Department of Public Health and Clinical Medicine, Umeå University, SE-901 85 Umeå, Sweden. 2 The Obstructive Lung Disease in Northern Sweden Studies, Department of Medicine, Sunderby Central Hospital of Norrbotten, Luleå, Sweden. 3 Lung and Allergy Research, National Institute of Environmental Medicine, Karolinska Institutet, Stockholm, Sweden. Correspondence to: Ulf Hedlund, Occupational Medicine, Department of Public Health and Clinical Medicine, Umeå University, SE-901 85 Umeå, Sweden. Tel: 146 (0)90 785 2242; fax: 146 (0)90 785 2456; e-mail: ulf.hedlund@envmed.umu.se Respiratory symptoms seem to decrease when smokers quit smoking, but little is known about the persistence of respiratory symptoms in ex-miners after the exposure to occupational air pollutants has ceased. The aim of this population-based cross-sectional study was to assess the persistence of respiratory symptoms in ex-miners. Methods The Swedish iron ore mines are situated in the county of Norrbotten in the northernmost part of Sweden. Since the 1920s, all mining has been underground in the town of Malmberget, where this study was performed. This is a population-based cross-sectional study. The prevalence of respiratory symptoms was compared between ex-miners and a sample from the general population in the county. The study base included men born between 1919 and 1972 living in eight townships in Norrbotten in 1992. The Obstructive Lung Disease in Northern Sweden (OLIN) studies are epidemiological studies of obstructive airway diseases and respiratory symptoms in progress since 1985 [16]. This study base comprised all men and women born in 1919 20, 1925 26, 1934 35, 1940 41, 1949 50 and 1955 56 and all born in 1923 56 on the 15th day of each month living in eight areas of the province of Norrbotten in 1992 [17]. This year, a questionnaire was sent to all who could be traced, 20 489 subjects. Ó The Author 2006. Published by Oxford University Press on behalf of the Society of Occupational Medicine. All rights reserved. For Permissions, please email: journals.permissions@oxfordjournals.org

U. HEDLUND ET AL.: RESPIRATORY SYMPTOMS IN EX-MINERS 381 The cohort comprised.10% of all adults in Norrbotten. The participation rate was 85%. From the responders, we selected men who had previously worked as underground miners for at least 1 year. They were identified from the mining company s staff register, which is complete since 1923. Women were excluded because there were only a few female ex-miners. Ex-miners had started to work in the mines from 1936 to 1988 and ceased mining between 1938 and 1991. The questionnaire comprised data on occupational title in 1992 and occupational titles for previous jobs lasting for.5 years. The occupations were classified according to the Nordic Classification System of Occupations [18]. Referents were responders to the questionnaire who had not had a job with high exposure to dust, gases and fumes. The exposure was estimated from the occupational titles from the questionnaires. Men with job titles indicating, for example, working in mining, driving, forestry, paper plants, steel and metal plants, workshops, construction and manufacturing industry were excluded. Miners in the underground iron mine of Malmberget are exposed to quartz and other mineral dust, blasting gases and fumes. The use of diesel-powered equipment started in the mid 1960s. In 1970s, high radon levels were discovered. This resulted in an extensive rebuilding of the ventilation system which was finished in 1975. A systematic measurement programme of air pollutants had started in 1965 [19]. The estimated average exposure of respirable dust between 1920 and 1973 was 14 mg/m 3 in loading, 8.4 mg/m 3 in drilling, 7.6 mg/m 3 in chute gate operating, 40 mg/m 3 in shotcreting (applying concrete to rock walls) and 2.4 mg/m 3 in other occupations. The average exposure from 1974 to 1997 was 2.4 mg/m 3 in loading and 0.8 mg/m 3 elsewhere. Exposure of nitrogen dioxide for all occupational groups was estimated to be 2.0 p.p.m. from 1965 to 1969, 1.2 p.p.m. from 1970 to 1984 and 0.5 p.p.m. from 1985 to 1992. In this paper, exposure relates to years of underground work. The questionnaire for the OLIN studies was based on and expanded from the British Medical Research Council questionnaire [20]. It included questions about respiratory symptoms and diseases, use of respiratory medicines, smoking habits and occupations and has been extensively described [21]. The questionnaire has later been used in a number of studies in Nordic and Baltic countries. Definitions used in this paper are shown in Box 1. Symptoms were grouped in a clinically relevant complex as defined by Eagan et al. [6] asthmatic symptom complex: yes to attacks of shortness of breath and recurrent wheeze. Ex-smokers had stopped smoking.12 months prior to the study. Smokers were current smokers or had stopped smoking,12 months prior to the study. Nonsmokers had never been smokers. Box 1: Definitions used in this paper A family history of asthma: have any of your parents, brothers or sisters had asthma? Physician-diagnosed asthma: have you been diagnosed as having asthma by a physician? Physician-diagnosed chronic bronchitis: have you been diagnosed as having chronic bronchitis or emphysema by a physician? Attacks of shortness of breath: have you now or have you had asthma symptoms during the last year (intermittent breathlessness or attacks of shortness of breath, the symptoms may exist simultaneously with or without cough or wheezing)? Recurrent wheeze: do you usually have wheezing or whistling in your chest when breathing? Long-standing cough: have you had long-standing cough during the last years? Sputum production: do you usually have phlegm when coughing or do you have phlegm on your chest, which is difficult to bring up? Chronic productive cough: yes to sputum production and to Do you bring up phlegm on most days during periods of at least three months? If yes, also yes to Have you had such periods during at least two successive years? [22]. Asthma medicines: do you currently use asthma medicines, regularly or as needed? Statistical analyses were performed using the Statistical Package for the Social Sciences (SPSS) for Windows, release 11.0.0 (SPSS for Windows, 2001). Multiple logistic regression analysis was used to estimate the odds ratios (ORs) in ex-miners compared with referents adjusted for age, smoking and a family history of asthma as possible confounders. For a continuous variable, the corresponding OR informs how much the risk is changed when the variable is changed one unit. Pairwise interactions between the studied variable and other variables were examined using P, 0.01 as level of significance in order not to increase the alpha error. Elsewhere, P, 0.05 was considered statistically significant. The Ethics Committee of the University and the University Hospital of Northern Sweden in Umeå approved the study. Results The ex-miners and the referents were similar regarding age, smoking habits and a family history of asthma (Table 1). The duration of exposure in miners was on average 13 years, median 12 years and range 1.1 37 years. The number of years between the first exposure underground and the study was on average 30 years, median

382 OCCUPATIONAL MEDICINE 32 years and range 4 56 years. On average 16 years, median 14 years and range 1.1 54 years had elapsed after the last underground exposure until the time of participating in the study. Ex-miners aged,45, 45 59 and $60 years had worked as miners for on average 8.6, 12 and 18 years, respectively. They had ceased to work as a miner on average 7.1, 16 and 22 years ago, respectively. The prevalence of all studied symptoms or conditions except long-standing cough was higher in ex-miners than in referents. However, only physician-diagnosed chronic bronchitis and chronic productive cough showed significantly higher prevalence in a univariate analysis in ex-miners (Table 2). Physician-diagnosed chronic bronchitis and chronic productive cough were also significantly higher in a multivariate analysis after adjusting for age, smoking habits and family history of asthma (OR 5 2.5 and 1.7, respectively; Table 3, analysis 1). There was also a trend to Table 1. Study population by age, smoking habits and a family history of asthma Table 2. Prevalence (%) of respiratory symptoms and conditions in ex-miners and referents Symptom or condition Ex-miners (n 5 206) Ex-miners (n 5 206) Referents (n 5 4560) Referents (n 5 4560) Age (years) Mean 56 52 Median 57 51 Standard deviation 11 12 Range 35 73 30 73 Smoking habits n % n % Non-smokers 76 38 1805 41 Ex-smokers 66 33 1322 30 Smokers 59 29 1282 29 Unclear a 5 151 A family history of asthma Yes 64 32 1343 30 No 137 68 3111 70 Unclear a 5 106 a Those with unclear smoking habits and family history of asthma were excluded from percent calculation. Difference (P-value) Physician-diagnosed asthma 8.2 7.2 0.6 Attacks of shortness of breath 22 16 0.08 Recurrent wheeze 18 13 0.06 Asthmatic symptom complex 12 8.1 0.08 Asthma medicines 12 7.8 0.06 Physician-diagnosed 12 4.6,0.001 chronic bronchitis Chronic productive cough 12 7.0 0.01 Long-standing cough 11 11 1.0 Sputum production 24 18 0.07 increased use of asthma medicines among the ex-miners. No significant results were found for other respiratory symptoms or conditions. In a similar multivariate analysis comprising only non-smokers, 76 ex-miners and 1805 referents, there was a significantly increased risk of chronic productive cough (OR 5 2.8, 95% confidence interval 5 1.4 5.8), but not for asthma medicines or physician-diagnosed chronic bronchitis. We also studied if symptoms decreased or increased after the miners had stopped working in the mine. This multivariate analysis comprised only the 206 ex-miners and was adjusted for age, smoking habits, family history of asthma and years of exposure in the mine. Years since the last exposure in mining was positively and significantly associated with the use of asthma medicines, i.e. the use of medicines increased with increasing years since cessation of exposure (OR for 10 years 5 2.0; P, 0.01) (Table 3). No statistically significant results were found for other studied symptoms or conditions. No interaction could be detected in any multivariate analysis. Discussion This population-based study of ex-miners indicates that ex-miners have more respiratory symptoms than controls and suggests that respiratory symptoms caused by occupational exposures may not be totally reversible after the exposure has stopped. The selection procedure of this cohort can be regarded as a random sample from the population in certain age groups living in certain areas of the county. Bias may occur by selection into the job. Subjects entering a dusty job may have better respiratory health at start of employment than those entering jobs with no or less such exposure [23]. Effects of occupational exposure may thus be underestimated in our study. We believe that a differential selection according to moving out of the province influencing the results is improbable. Further, it is not probable that miners have chosen to leave mining for other occupations with more airborne exposure to such an extent that it would invalidate this study [24]. Our study has low power to study effects shortly after leaving mining, as there were few ex-miners with a short time elapsing between leaving the mine and participating in the study. In contrast, the long time after the last exposure in the mine (on average 16 years) makes the study suitable for studying persistence of respiratory symptoms. A self-administered questionnaire gives a good estimation of the prevalence of asthma in a population [25,26], but it underestimates the prevalence of bronchitic symptoms especially in older smokers [16]. The primary aim of our study was to study differences between exposed, i.e. the ex-miners, and the non-exposed and if the underestimation is similar, the bias would be low. Bias would be introduced if different diagnostic criteria were

U. HEDLUND ET AL.: RESPIRATORY SYMPTOMS IN EX-MINERS 383 Table 3. Multivariate analyses Dependent variable Analysis 1 Analysis 2 Estimates of prevalence ratios in miners versus referents (categorical) Risk estimates of years after the last exposure (continuous) OR 95% confidence interval OR 95% confidence interval Asthma medicines 1.5 0.95 2.4 1.07 1.02 1.12 Physician-diagnosed chronic bronchitis 2.5 1.5 3.9 1.04 0.99 1.09 Chronic productive cough 1.7 1.1 2.7 1.00 0.96 1.05 Analysis 1 comparing ex-miners (n 5 206) with referents (n 5 4560). Logistic regression adjusting for age (continuous), smoking habits (categorical) and a family history of asthma (categorical). Analysis 2 comprising 206 ex-miners. Logistic regression adjusting for age (continuous), smoking habits (categorical), a family history of asthma (categorical) and exposure years in mining (continuous). used for ex-miners and controls. In this study, all subjects were observed in the same way and to the same extent, which ought to have reduced diagnostic bias. Nevertheless, in asthma, chronic bronchitis, emphysema and COPD, symptoms often overlap [27]. Physicians may have diagnosed chronic bronchitis rather than asthma and vice versa. Further, asthma medicines may have been prescribed to treat bronchitic symptoms. Bias may also be introduced by non-response. However, the response rate was high, 85%, which reduces a possible selection bias caused by non-response. Thanks to the staff register of the mining company, we could reliably identify ex-miners. Subjects who had been occupationally exposed to dust, gases or fumes were rejected as referents. The reference group was thus considered representative of subjects with a low occupational exposure to dust and irritating gases. In industry-based studies of current miners, referents have often been taken from the mining industry such that underground miners have been compared with surface workers from the same mine [9,14,15]. As surface workers at least to some extent have also been occupationally exposed to dust, gases and fumes, an association between exposure and respiratory health in such studies may be underestimated. A population-based study, as in our study, may reduce this error. Another design has been to compare miners with and without diesel exposure [28]. Possible confounders such as age, smoking habits and a family history of asthma were adjusted for in the analysis. Including a family history of asthma in the analysis controlled for a possible confounding by inherited susceptibility to respiratory diseases. We consider a possible remaining bias to be low and mainly non-differential. ORs of 1.2 2.1 for current respiratory symptoms have been reported from other population-based studies of occupational exposure to dust, gases and fumes [1 3,5,6]. A Norwegian study found an OR of 1.6 for an asthmatic disease pattern in workers exposed to dust and fumes [6]. Some studies show an association between long-term low-dose exposure to dust, gases and fumes and asthma or asthma-like symptoms [3,29 31]. However, there is still no consensus [32]. In a South African cross-sectional study, ex-gold miners [10] for 1 year or longer (how long was not reported) were compared with still working miners. There was a somewhat higher prevalence of chronic bronchitis in the ex-miners. The authors found this to be different to what had been shown after smoking cessation and concluded that the symptoms persisted after cessation of mining exposure. Swedish iron ore miners had increased risk of asthma-like symptoms 1 year after unemployment compared with controls from the general population [33]. In a population-based longitudinal study, subjects exposed to dust, gases and fumes in different occupations were examined [1]. Workers previously exposed, but not during the last 3 years, had after adjustment to confounders significantly higher risks of cough, phlegm, wheeze and breathlessness compared with workers without such exposure. It is interesting to compare our findings in ex-miners with ex-smokers. There is consensus that smoking cessation improves respiratory symptoms. Most changes occur during the first year, but dyspnoea is less likely to improve [34]. However, respiratory symptoms are more common in ex-smokers than in non-smokers, indicating that the symptoms are not totally reversible. A few histopathological studies suggest persistence of airway inflammation, which probably reflects a repairing and not a damaging process [34]. It is unlikely that the increased prevalence in ex-miners could be explained by anything else than occupational exposure to dust, gases and fumes. In the analysis within ex-miners, physician-diagnosed chronic bronchitis was not inversely associated with years after the last mining exposure. Thus, our findings seem not to be quite in accordance with the findings of effects after smoking cessation. Both in ex-smokers and ex-miners, there is persistence of symptoms after cessation of exposure. In ex-smokers, symptoms improve after smoking

384 OCCUPATIONAL MEDICINE cessation, but in ex-miners, there was no such indication after stopping mining. The increased use of asthma medicines and the tendency of increased prevalence of physician-diagnosed chronic bronchitis with time in exminers in our study is probably an effect of ageing [16,20], which also has been demonstrated by others [4,28]. We therefore conclude from our study that physiciandiagnosed chronic bronchitis and chronic productive cough in ex-iron miners persist several years after the exposure had stopped. Acknowledgements The authors thank the staff of the OLIN studies for collecting the data. We also thank industrial hygienist Leif Kågström, Kåre Eriksson, Eva Rönmark and the statistician Elsy Jönsson for valuable support. Grants from the Swedish Heart Lung Foundation, the former Swedish Council for Working Life (RALF) and Norrbotten s Local Health Authority are acknowledged. Conflicts of interest None declared. References 1. 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