AMERICAN JOURNAL OF INDUSTRIAL MEDICINE 55:793–798 (2012) Small Pneumoconiotic Opacities on U.S. Coal Worker Surveillance Chest Radiographs Are not Predominantly in the Upper Lung Zones A. Scott Laney, PhD Ã and Edward L. Petsonk, MD Background Radiographic shadows of coal workers’ pneumoconiosis (CWP) are commonly described as predominantly in the upper lung zones. Methods We evaluated the lung distribution of small opacities on surveillance chest radiographs (CXRs) taken between 1981 and 2010 among 2,467 underground US coal miners. All had evidence of pneumoconiosis (category !1/0), based on the contemporary International Labour Office Classification of Radiographs of Pneumoconioses. Results Small opacity involvement was approximately equal over all lung zones, with 30.7% of the total involvement reported in the upper zones, 37.1% in the middle zones, and 32.1% in the lower zones. Primarily rounded opacities were seen in 62.1% of miners and primarily irregular opacities were seen in 37.9%. Miners with primarily rounded opacities had a distribution with moderate upper zone predominance (upper ¼ 36.8%, middle ¼ 36.5%, and lower ¼ 27.2%). In contrast, miners with primarily irregular opacities showed a lower zone preponderance (upper ¼ 20.5%, middle ¼ 38.4%, and lower ¼ 41.1%). Conclusion The distribution of small pneumoconiotic opacities on surveillance CXRs of working US coal miners is not consistent with the conventional expectations of upper lung zone predominance. Am. J. Ind. Med. 55:793–798, 2012. ß 2012 Wiley Periodicals, Inc. KEY WORDS: coal workers’ pneumoconiosis; radiography INTRODUCTION Surveillance Branch, Division of Respiratory Disease Studies, National Institute for Occupational Safety and Health, Centers for Disease Control and Prevention, Morgantown, West Virginia The findings and conclusions in this report are those of the authors and do not necessarily represent the views of the National Institute for Occupational Safety and Health. Disclosure Statement: The authors report no conflicts of interests. Ethics approval: This study was conducted with the approval of the National Institute for Occupational Safety and Health. *Correspondence to: Dr. A. Scott Laney, PhD, Surveillance Branch, Division of Respiratory Disease Studies, National Institute for Occupational Safety and Health, Centers for Disease Control and Prevention, 1095 Willowdale Rd., Mail Stop HG900.2, Morgantown, 26505^ 2888,WV. E-mail: alaney@cdc.gov Accepted10 March 2012 DOI10.1002/ajim.22049. Published online19 April 2012 in Wiley Online Library (wileyonlinelibrary.com). ß 2012 Wiley Periodicals,Inc. Starting in 1973, regulations in the United States required operators of underground coal mines to maintain respirable dust below 2 mg/m3. By 2000, coal miner surveillance radiographs had shown an 89% decline in the prevalence of pneumoconiosis [National Institute for Occupational Safety and Health, 2008]. However, over the last decade, reports have documented increases in pneumoconiosis prevalence, as well as clusters of rapidly progressive disease and advanced and fatal disease in relatively young miners [Centers for Disease Control and Prevention, 1983; Centers for Disease Control and Prevention, 2004; Centers for Disease Control and Prevention, 2006; Centers for Disease Control and Prevention, 2007; Centers for Disease Control and Prevention, 2009; Laney and Attfield, 2010; Laney et al., 2010; Wade et al., 2011]. 794 Laney and Petsonk These recent trends have resulted in renewed attention to the clinical presentations and management of coal mine dust-related lung disease. Review articles and textbooks describe the location of the radiographic shadows of coal workers’ pneumoconiosis (CWP) as predominantly in the upper lung zones [Castranova and Vallyathan, 2000; Cohen and Velho, 2002; Cecil et al., 2008; Cohen et al., 2008]. For example, one U.S. textbook states ‘‘These lesions start in the upper lobes but can involve all lobes in more advanced CWP’’ [Schwartz, 2011] and similar statements are found in several British texts [Parkes, 1994; Brichet et al., 2002]. Although, the zonal distribution of pneumoconiotic opacities is not an accepted diagnostic criterion for CWP, many physicians appear to reiterate the view that simple CWP is predominantly identified in the upper lung fields, and this does likely influence both radiographic classifications and CWP diagnoses. Importantly, physicians may exclude a diagnosis of CWP or silicosis if a miner’s small opacities are not predominantly in the upper lung zones, or when parenchymal nodules are found only in the lower lung zones [Zhong and Li, 1995; U.S. Department of Labor Office of Administrative Law Judges, 2007]. At least two published studies have assessed zonal patterns of small opacities and did not confirm the traditional view of upper zone predominance, although, these have been largely overlooked [Amandus et al., 1974; Young et al., 1992]. Additionally, these older studies used the UICC/Cincinnati (U/C) classification system which was an extension of the International Labour Office (ILO) 1958 classification [UICC, 1970]. The earlier U/C classification required two-independent assessments of the zonal distribution of small opacities; one classification for rounded opacities and one for irregularly shaped opacities. The more recent 1980 and 2000 revisions of the ILO classification system use a similar approach to profusion classification, but require only one combined determination of zonal involvement of small opacities irrespective of opacity shape [International Labour Office, 2002]. In light of the small number of published observational studies addressing this issue, we examined the pneumoconiosis classifications for coal worker surveillance radiographs taken between 1981 and 2010. The objective of the study was to describe the observed zonal distribution of small radiographic opacities in a large number of coal miners whose radiographs were interpreted by experienced readers using the contemporary approach to pneumoconiosis classification. METHODS Data were derived from the NIOSH-administered Coal Workers’ Health Surveillance Program (CWHSP) which includes the enhanced CWHSP (ECWHSP) [National Institute for Occupational Safety and Health, 2009]. This study was conducted with the approval of the National Institute for Occupational Safety and Health. As part of the program, every 5 years, all US coal miners working underground are offered chest radiographs (CXRs). CWHSP radiographs are classified by NIOSH B Readers for the presence, profusion, type, and distribution of lung parenchymal abnormalities consistent with pneumoconiosis, according to the ILO Classification of Radiographs of Pneumoconioses [International Labour Office, 2002]. Results are recorded in a standardized format, communicated to the participants, and assembled in an electronic database [National Institute for Occupational Safety and Health, 2000]. Data for the present analysis included radiographs of underground coal miners acquired from January 1, 1981 to April 15, 2010. Inclusion into the analytic dataset required an ILO Classification complying with NIOSH program procedures, as well as opacity involvement recorded in at least one lung zone and complete information regarding date of the radiograph, and shape/size indication. Study participants were overwhelmingly male (99.6%); eight females and three individuals with unrecorded gender were excluded from analysis. Because the CWHSP is an ongoing health surveillance program, many miners had multiple radiographic readings recorded over time. For the present analysis, data were restricted to the most recent classification by a B Reader of the most recent radiograph available for each individual. The data included only radiographs with a small opacity profusion final determination of !1/0. The final determination was derived by at least two readers according to CWHSP procedures [Centers for Disease Control and Prevention, 2003]. Smoking status was available from participants of the ECWHSP who comprised 10.4% of the sample (n ¼ 258) and was classified as current, never, or former smokers. RESULTS Among 101,407 U.S. underground coal miners who participated in radiographic surveillance from January 1, 1981 to April 15, 2010, 2,642 (2.6%) showed a small opacity profusion !1/0 consistent with pneumoconiosis. Complete information was available for 2,467 who comprised the study population for our analysis. The presence of pneumoconiotic small opacities was indicated in a total of 11,680 lung zones. Overall, small opacities were noted approximately equally over the affected zones, with 30.7% of the total involvement noted in the upper zones, 37.1% in the middle zones, and 32.1% in the lower zones. The primary shape was recorded as rounded for 1,532 (62.1%) miners and irregular for 935 (37.9%) (Table I). Although, 63 possible zonal combinations exist, 86% of Zonal Distribution of Small Pneumoconiotic Opacities on U.S. Miner Radiographs TABLE I. Primary Shape and Size of Small Lung Opacities in 2,467 United States Coal Miners Shape/Size No.(%) p q r Rounded s t u Irregular 251 (10.2) 1,052 (42.6) 229 (9.3) 1,532 (62.1) 461 (18.7) 451 (18.3) 23 (0.9) 935 (37.9) Shape/size designations are defined by the ILO classification system. the lung involvement was reported in just five common patterns (Fig. 1). When the readings were stratified by primary shape designation, the zonal distribution of small opacities differed between those with primarily rounded versus irregularly shaped opacities. Upper zone involvement was significantly more common when the primary shape designation was rounded [Prevalence ratio (PR) ¼ 1.8; 95% and confidence interval (CI) ¼ 1.7–1.9]. Conversely, lower zone involvement was significantly more common when the primary shape designation was irregular (PR ¼ 1.5; 95% CI ¼ 1.4–1.6) with P < 0.0001. Miners with primarily rounded opacities (small opacity type p, q, or r on the ILO pneumoconiosis classification) had a distribution of opacities with moderate upper zone predominance (upper ¼ 36.8%, middle ¼ 36.5%, and lower ¼ 27.2%). Of those, a common pattern was involvement of both upper and middle lung zones representing 18.9% of miners with rounded opacities (Fig. 1, 795 second row). Overall, among the 1,532 miners with primarily rounded opacities, a majority showed upper zone predominance; in 122 (8.0%) neither upper zone was affected. For miner radiographs classified as having primarily rounded opacities, age ranged from 22 to 80 years, with a mean and median of 48.9 and 50.0 years. Among miners with a primary designation of irregularly shaped opacities (ILO small opacity type s, t, or u) there was strong lower lung zone predominance, with exclusively middle and lower lung zone involvement in 41.5% of radiographs. Taken with the radiographs showing predominantly irregular opacities in all six lung zones, 80.6% of the zonal distribution observed could be described by three patterns. (Fig. 1, third row) This is in contrast to upper and middle zone involvement, a pattern found in only 2.4% of radiographs with the primary shape designation of irregular. Overall, among miners with primarily irregularly shaped opacities a majority showed lower zone predominance. In fact, when the B Readers indicated the dominant shape as irregular, in only 4.5% of the radiographs was neither lower zone involved. Mean and median ages were 50.0 and 51.0 years, respectively (range 22–76 years) for miners with radiographs classified as having primarily irregular opacities. In addition to the similarity in age, there was no meaningful difference in mean mining tenure between the group of miners with primarily rounded opacities (24.0 years) and those with irregular opacities (22.8 years). Of the 2,467 subjects included in this analysis, smoking data were available for 258 study subjects (10.4%). An analysis of smoking status by opacity shape revealed similar smoking prevalence between those with primarily rounded opacities compared to those with irregular opacities (Table II). For this subgroup, mean and median age did not meaningfully differ between those with irregular FIGURE 1. Common patterns of zonal involvement by opacity shape. Data are (row%). Values in left column indicate the total number of zones involved for all miners (readers could indicate involvement in one or more, up to six zones). 796 Laney and Petsonk TABLE II. Smoking Status by Opacity Shape in 258 Coal Miners Irregular Current Never Former Rounded PR (95% CI) P-value 13 (24.5) 18 (34.0) 22 (41.5) 64 (31.2) 68 (33.2) 73 (35.6) 0.8 (0.5^1.3) 1.0 (0.7^1.6) 1.2 (0.8^1.7) 0.34 0.91 0.43 Data are no.(%). PR, prevalence ratio. P-values are Mantel Haenszel Chi-squared. opacities (mean ¼ 53.8 and median ¼ 54.0) and rounded opacities (mean ¼ 52.0 and median ¼ 52.0). In addition, mining tenure was similar between the groups with mean tenure of 29.5 years for those with primarily irregular opacities compared to 29.0 years among those with primarily rounded opacities. DISCUSSION Textbooks and review articles often convey the view that the small pneumoconiotic opacities in coal miners are predominantly observed in the upper lung fields. However, the scientific foundation for this expectation is unclear, as upper zone predominance has not been observed in previous published studies of coal miners’ radiographs [Amandus et al., 1974; Young et al., 1992]. To help clarify the distribution of small opacities in CWP, we evaluated classifications submitted by NIOSH B readers for coal miner surveillance CXRs taken between 1981 and 2010. The zonal distribution of small opacities was assessed using the contemporary approach to ILO classification in 2,467 U.S. underground coal miners whose radiographs showed a profusion of !1/0 small opacities. For all small opacity shapes together, there was no clear zonal pattern. Among miners with primarily rounded opacities, a majority showed upper zone predominance. In contrast, among miners whose radiographs showed chiefly irregular opacities, a majority showed lower zone predominance. In the present study, 38% of the radiographs were classified as showing primarily irregular small opacities, and the strong lower lung zone predominance of those opacities was the primary reason for the absence of a pattern of zonal involvement when the data were taken as a whole. Therefore, a consideration of irregularly shaped opacities in CWP is warranted. Some researchers in the past have excluded a priori consideration of irregular opacities among coal miners [Ruckley et al., 1984; Fernie and Ruckley, 1987; RemyJardin et al., 1990]. However, a substantial body of research exists which highlights the importance of irregular opacities in CWP [Lyons et al., 1972; Lyons et al., 1974; Musk et al., 1981; Cockcroft et al., 1983; Collins et al., 1988]. Both rounded and irregular radiographic opacities have been recognized as a manifestation of CWP based upon studies that linked the profusion of opacities on a miner’s radiograph with prior work tenure and dust exposure [Amandus et al., 1976; Cockcroft et al., 1983; Collins et al., 1988]. Although, the profusion of radiographic shadows correlates with lung dust content [Rossiter, 1972], no clear correspondence has been established between pneumoconiosis pathology and opacity type [CAM, 1979]. Individual coal macules are generally too small to be appreciated on CXRs [Heitzman et al., 1972]. Pathologic studies have shown that the inflammatory lesions of CWP may appear rounded, but often assume more irregular or stellate shapes as they enlarge, due to scarring, contraction, and associated emphysema [CAM, 1979]. These pathologic lesions appear to be reflected on the radiograph as the irregular (s, t, and u) small opacities of the ILO classification [Heitzman et al., 1972]. The shape of pneumoconiotic opacities may have functional consequences. In a follow-up study of 125 male coal workers with radiographic pneumoconiosis, Musk et al. [1981] found p-type opacities were associated with a reduction in DLCO and increased lung compliance, suggestive of emphysema, while the men with r-type predominance had reductions in both compliance and DLCO, more consistent with fibrosis. The miners with irregular opacities demonstrated reductions in diffusing capacity but no change in lung compliance. Another study of 895 British miners demonstrated that the 39 individuals with predominantly irregular opacities had deficits of 190 ml in both FEV and FVC beyond the expected effects of age, body size, smoking habits, and dust exposure [Collins et al., 1988]. Among general populations, increasing age and tobacco smoking have been associated with a small increase in the profusion of radiographic small opacities [Carilli et al., 1973; Amandus et al., 1976; Blanc and Gamsu, 1988; Blanc and Gamsu, 1989; Weiss, 1991; Meyer et al., 1997]. We observed no clinically relevant differences with respect to age and underground mining tenure between miners with rounded versus irregular small opacities. Among miners in our study for whom the information was available, smoking status was similar among those with primarily irregular opacities compared to those with rounded opacities. However, a limitation of the study was that information on smoking status was not available for most participants. Additionally, the analysis was restricted to working miners with a median ILO classification of category 1/0 or greater (NIOSH final determination). It has been shown that radiographic opacities, irrespective of smoking status, are unlikely to be classified at this level in the absence of occupational dust exposure [Castellan et al., 1985; Kilburn et al., 1986; Blanc and Gamsu, 1988]. Our study has a number of additional strengths and limitations. The analysis included a large number of radiographs, taken over nearly 30 years from all U.S. mining Zonal Distribution of Small Pneumoconiotic Opacities on U.S. Miner Radiographs regions. All classifications included in the study were done in an identical manner by experienced NIOSH certified B readers using the contemporary approach to pneumoconiosis classification, and were recorded on a single revision of the interpretation form. Reader bias is unlikely, since the radiographs were interpreted as part of the health surveillance program, and readers were unaware that zonal involvement was being studied. However, there may be an inherent bias in that the recording of lung zone involvement is influenced by the zonal patterns in the ILO standard images used in the classification, which do reflect the expected zonal distributions of rounded and irregular opacities. Additionally, although, readers score an average overall profusion of small opacities for each image, zonal involvement in the ILO classification system is recorded based only upon the presence or absence of opacities in each of the six lung zones. Thus, we were unable to detect whether, on an individual radiograph, the reader perceived that any of the involved zones demonstrated a higher or lower profusion than the overall score [International Labour Office, 2002]. Finally, participation in the CWHSP is voluntary and has varied over time. 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