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Health Risks of Radon and Other Internally Deposited Alpha-Emitters: BEIR IV (1988)
Commission on Life Sciences (CLS)

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APPENDIX VT Lung-Cancer Histopathology Correlations between radon-daughter exposures and specific histopa- thological cell types of lung cancer in humans have been a subject of con- troversy for many years. Primary cancer of the lung comprises diverse and generally distinct histopathological cell types. The most common are squamou~cell carcinoma, small-cell carcinoma, adenocarcinoma, and large-cell carcinoma, representing, respectively, about 35, 17, 25, and 9% of lung cancers in the male population of the United States. In nonsmokers, adenocarcinoma ~ the most common cell type and small-cell carcinoma is infrequent, accounting for less than 5%0.24 Clinically, these four cell types of lung cancers differ in their manner of clinical presentation, natural history, and response to therapy. At present, lung cancers are generally classi- fied histologically by conventional light microscopy. Figure VI-1 shows examples of some of the common histological types of lung cancers. Nu- merous classification schemes have been published, with the most widely used being that developed by the World Health Organization and recently modified.25 The accuracy of histopathological diagnoses is influenced by the quantity and quality of the tissue available for examination. Observer variability in the classification of lung-cancer histopathology has been well documented and may be of substantial magnitude.~4 Reliance on clinical reports may introduce substantial misclassification. Because of observer variability, classification of lung-cancer cell types for research purposes should incorporate a standardized review of original histological material by a panel of pathologists. However, use of review panels does not ensure comparability between studies. 497

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498 HEALTH RISKS OF RADON AND OTHER ALPHA-EMITT13RS The distribution of lung-cancer cell types has been examined in ura- nium and other miners exposed to radon daughters. The principal pop- ulations are listed in Table VI-1. Most are from from mining groups in which cigarette smoking was prevalent. Exceptions include early miners in Schneeberg and Joachimsthal, reported to have smoked little, and Navajo miners in the United States.~5 In the 1879 report by Harting and Hess, the malignant disease in Schneeberg miners was identified as lymphosarcoma, a designation that may have reflected the similarity of cells in small-cell cancers and in some lymphomas when examined with a light microscope. Autopsy specimens from miners in nearby Joachunsthal showed a preponderance of small-cell carcinomas.~7~23 A later investigation of uranium miners in this same area showed that small-cell cancer remained the most common histological type. Horacek et al.~3 compared the histological distribution of 115 cases of lung cancer in Czechoslovakian uranium miners with that in 326 control cases. Diagnoses were made by one pathologist who was not informed about the exposure status of the cases under review. Only a small percentage of the lung-cancer cases in each group were nonsmokers. The percentages of squamous-cell carcinomas were similar in the miners and in the controls, but about 12% more small-cell cancers were observed in miners. The mortality rate of all major cell types was increased beyond that which would have been expected. In the late 1950s and early 1960s a number of reports from Fiance, which included crude proportionate mortality studies, were published de- scribing the lung-cancer excess among iron miners in Lorraine. Roussel et al., in a histological review of a series of 225 lung-cancer cases among these miners, found that 44% were anaplastic versus an expected value of 28% for nonminers. Both groups included approximately 1% nonsmokers. The studies by Saccomanno and colleagues of the Colorado Plateau uranium miners provide the most extensive data concerning lung-cancer cell types and radon-daughter exposure. Findings have been reported pe- riodically since 1964.39- The case material was derived from miners in the U.S. Public Health Service study and others who lived in the Col- orado Plateau area. Review methods varied; most reports were based on a panel's consensus, but some reviews apparently involved only one patholo- gist. Most of the miners smoked cigarettes, and the total series has included only 14 nonsmokers.20 Initially, the majority of cases reviewed were small- cell carcinomas. The proportion of this cell type declined from 76% in 1964 to 22% in the late 1970s, while squamous cell carcinomas increased concomitantly. In nonsmokers, eight cases were small-cell carcinomas and the remaining six were of other cell types. The strong predominance of squamous-cell carcinomas in Newfound- land fluorspar miners appears anomalous (Table VI-1. However, the histological diagnoses were made by sputum cytology, which results in

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4gg Smog CeD Age Cell Adenocarcinoma Mucous CeD FIGURE VI-1 "~tob~c~ typee of lung cancer SOURCE: Jonstban Saw, unit verity of New Delco, persona com~nic~lon, 1987.

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Boo BARTH RISKS OF RADON AND OTHER ALPHA-EMIlUTERS TABLE VI-1 Lung-Cancer Histopathology in Mining Groups Exposed to Radon Daughters Population Joachimsthal miners '7 23 Findingsa Comment Colorado Plateau uranium miners ~,4,~9,20,2~ Newfoundland fluorspar miners26 British iron ore minersS Swedish iron ore miners Swedish iron ore miners9 Czechoslovakian uranium miners Canadian uranium miners Navajo uranium miners Navajo uranium miners7 28 cases: 16 SCC, 12 squamous SCC predominance, increasing with WLM 29 cases: 26 squamous, 2 SCC, 1 adenocarcinoma 69 cases; 27 SCC 36 cases: 26 SCC, 10 squamous 25 cases: 11 SCC, 11 squamous, 3 adenocarcinoma 115 cases: 62 SCC, 40 squamous, 4 adenocarcinoma, 9 other types 91 cases; 47 SCC 16 cases: 10 SCC, 3 squamous, 3 other types 21 cases: 7 SCC, 8 squamous, 4 adenocarcinoma, 2 LCC Autopsies 1929-1930 and 1933-1938; one pathologist Cases seen at specific hospitals; panel review All cases diagnosed by sputum cytology Histologic type from pathology report Histologic type from Swedish cancer registry Methods not given One pathologist Selected from 134 cases; histologic type from pathology report Methods not given; histologic type from pathology report Panel review New Mexico uranium 45 cases: 28 SCC, Panel review miners6 15 squamous, 1 adenocarcinoma, 1 LCC Abbreviations: SCC, small-cell carcinoma; LCC, large-cell carcinoma; Squamous, squamous cell carcinoma.

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LUNG-CANCER HIS TOPATHOLOGY 501 the over-representation of centrally located tumors. Both squamous- and small-cell carcinomas tend to be located in the larger airways, but at the time of this investigation the former may have been more readily diagnosed by cytology alone. Navajo miners who worked in the Colorado Plateau are of interest be- cause only a small proportion smoked cigarettes, with average consumption by the smokers of only a few cigarettes each day.4~22 Gottlieb and Husenit described 16 Navajo miners diagnosed with lung cancer at the Shiprock Indian Health Service Hospital from 1965 through 1979. Based on record review, they reported that 10 of the cases were small-cell carcinomas. Butler et al.7 reviewed histopathological material for 26 of 32 lung-cancer canes diagnosed among all Navajo males between 1969 and 1982. A panel of three pathologists examined all slides. In contrast with the earlier study of Gottlieb and Husen,~i small-cell carcinomas did not predominate in the 21 cases of lung cancer occurring in Navajo uranium miners. Seven of these cancers were small-cell carcinoma, eight were squa~nous-cell car- cinoma, four were adenocarcinoma, and two were large-cell carcinoma. While small-cell carcinoma was not the predominant cell type in this se- ries, the proportion with this cell type (33%) is far greater than expected from the distribution of lung-cancer his.topathology in nonsmokers. The discrepant findings of these two reports may reflect the use of medical records by Gottlieb and Husenii to determine the diagnoses. Recent reports from Canada and New Mexico document a contin- ued excess incidence of small-cell carcinomas in contemporary uranium miners. In iron-ore miners in Great Britain and Sweden, also exposed to radon daughters, small-cell carcinoma has occulted in excess.5~9~0 The pat- tern has been consistently observed in populations of miners who smoked cigarettes. Data for nonsmokers are sparse and conflicting. Saccomanno et al. 2i reported that most cases of lung cancer ~ nonsmokers from the Colorado Plateau region were small-cell carcinomas. Butler et al.7 found a cell type distribution in Navajo miners comparable to the observed dis- tribution in the general population. Thus, available information does not strongly support the association between uranium mining and small-cell cancers in nonsmokers, although this association in smokers ~ supported by the available data. This pattern appears to change as miners who smoke are and the interval since cessation of uranium mining exposure lengthens. REFERENCES 1. Archer, V. E., H. P. Brinton, and J. K. Wagoner. 1964. Pulmonary function of uranium miners. Health Phys. 10:1183-1194. Archer, V. E., J. K. Wagoner, and F. E. Lundin, Jr. 1973. Uranium mining and cigarette smoking effects on man. J. Occup. Med. 15:204-211. Archer, V. E., G. Saccomanno, and J. H. Jones. 1974. Frequency of different histologic types of bronchogenic carcinoma as related to radiation exposure. Cancer 34:2056-2060. 2. 3.

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502 HEALI'H RISKS OF RADON AND OTHER AWNA-EMITTERS 4. Archer, V. E., J. D. Gillam, and J. W. Wagoner. 1976. Respiratory disease mortality among uranium miners. Ann. N.Y. Acad. Sci. 271:280-293. Boyd, J. T., R. Doll, J. S. Faulds, and J. Leiper. 1970. Cancer of the lung in iron ore (haematite) miners. Br. J. Ind. Med. 27:97-195. 6. Butler, C., J. M. Samet, D. M. Kutvirt, C. R. Key, and W. C. Black. 1985. Cigarette smoking and lung cancer cell types in uranium miners. Am. Rev. Respir. Dis. 131(Pt. 23:A176 (abstract). 7. Butler, C., J. M. Samet, W. C. Black, C. R. Key, and D. M. Kutvirt. 1986. Histopathologic findings of lung cancer in Navajo men: Relations to uranium mining. Health Phys. 51:365-368. 8. Chovil, A., and B. Chir. 1981. The epidemiology of primary lung cancer in uranium miners in Ontario. J. Occup. Med. 23:417-421. 9. Damber, L., and L. G. Lareson. 1982. Combined effects of mining and smoking in the causation of lung carcinoma~case-control study in northern Sweden. Acta Rad. Oncol. 21:305-313. 10. Edling, C. 1982. Lung cancer and smoking in a group of iron ore miners. Am. J. Ind. Med. 3:191-199. 11. Gottlieb, L. S., and L. A. Husen. 1982. Lung cancer canons Navajo uranium miners. Chest 81:449-452. 12. Harting, F. H., and W. Hesse. 1879. Der Lungenkrebe, die Bergkrankheit in den Schneeberger Gruben. Vierteljahreachr Gerichtl. Med. Offentl. Gesundheitswesen 30:296-309; 31:102-129, 313-337. 13. Horacek, J., V. Placek, and J. Sevc. 1977. Histologic types of bronchogenic cancer in relation to different conditions of radiation exposure. Cancer 40:832-835. 14. Ives, J. C., P. A. Buffler, and S. D. Greenberg. 1983. Environmental associations and histopathologic patterns of carcinoma of the lung: The challenge and dilemma in epidemiologic studies. Am. Rev. Respir. Dis. 128:19~209. 15. Myers, D. K., C. G. Stewart, and J. R. Johnson. 1981. Review of epidemiological studies on hazards of radon daughters. Pp. 513-524 in Radiation Hazards in Mining: Control, Measurement, and Medical Aspects, M. Comes, ed. New York: Society of Mining Engineers, American Institute of Mining, Metallurgical, and Petroleum Engineers, Inc. 16. Percy, C., J. W. Horm, and T. E. Goffman. 1983. Trends in histologic types of lung cancer, SEER, 1973-1981. Pp. 15~159 in Lung Cancer: Causes and Prevention, M. Mizell, and P. Correa, ede. DeerBeld Beach, Fla.: Verlag Chemie International. 17. Pirchan, A., and H. Sikl. 1932. Cancer of the lung in miners of Jachymov (Joachimsthal). Report of cases observed in 1929-1930. Am. J. Cancer 16:681- 722. 18. Roussel, J., C. Pernot, P. Schoumacher, M. Pernot, and Y. Kessler. 1964. Considerations statistiques sur la cancer bronchique du mineur de fer du bassin de la Lorraine. J. Radial. Electrol. 45:541-546. 19. Saccomanno, G. 1982. The contribution of uranium miners to lung cancer histogenesis. Rec. Results Cancer Res. 82:4~52. 20. Saccomanno, G., V. E. Archer, R. P. Saunders, L. A. James, and P. A. Beckler. 1964. Lung cancer of uranium miners on the Colorado Plateau. Health Phye. 10:1195-1201. 21. Saccomanno, G., V. E. Archer, O. Auerbach, M. Kuschner, R. P. Saunders, and M. G. Klein. 1971. Histologic types of lung cancer among uranium miners. Cancer 27:515-523.

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LUNG-CANC~R HIS TOPATHOLOGY 503 Samet, J. M., D. M. Kut~nrt, R. J. Waxweiler, and C. R. Key. 1984. Uranium mining and lung cancer in Navajo men. N. Engl. J. Med. 310: 1481-1484. Sikl, H. 1950. The present status of knowledge about the Jachymov disease (cancer of the lungs in the miners of the radium mines). Acta Unio Intl. Contra Cancrum 6:136~1375. 24. Stayner, L. T., and D. H. Wegman. 1983. Smoking, occupation and histopathol- ogy of lung cancer: A case-control study with the use of the Third National Cancer Surrey. J. Natl. Cancer Inst. 70:421. World Health Organization. 1982. The World Health Organization Histological Typing of Lung Tumors, 2nd ed. Am. J. Clin. Pathol. 77:123-136. 26. Wright, E. S., and C. M. Couves. 1977. Radiation-induced carcinoma of the lung the St. Lawrence tragedy. J. Thorac. Cardiovasc. Surg. 74:495-498.

Representative terms from entire chapter:

lung cancer