Environmental Health Perspectives 103, Supplement 2, March 1995
Cancer Risks from Exposure to Radon in Homes
Olav Axelson
Department of Occupational and Environmental Medicine, University Hospital, Linköping, Sweden
Abstract
Exposure to radon and its decay products in mines is a well recognised risk of lung cancer in miners. A large number of epidemiologic studies from various countries are quite consistent in this respect even it the magnitude of the risk differs according to exposure levels. Indoor radon became a concern in the 1970s and about a dozen of studies have been conducted since 1979, mainly of the case-control design. From first being of a simple pilot character, the designs have become increasingly sophisticated, especially with regard to exposure assessment. Crude exposure estimates based on type of house, building material and geological features have been supplemented or replaced by quite extensive measurements. Still, exposure assessment remains a difficult and uncertain issue in these studies, most of which indicate a lung cancer risk from indoor radon, usually with an about doubled risk. Also a recent large scale study has confirmed a lung cancer risk from indoor radon. More recently there are also some studies, mainly of the correlation type, suggesting other cancers than lung cancer to be related to indoor radon, especially leukaemia, kidney cancer and malignant melanoma and some other cancer forms as well. The data are less consistent and much more uncertain than for indoor radon and lung cancer, however and there is no clear support from studies of miners in this respect. --
Environ Health Perspect 103(Suppl 2):37-43 (1995)
Key words: building material, kidney cancer, leukaemia, lung cancer, melanoma, radiation, smoking, stomach cancer
This article was presented at the Fifth International Conference of the International Society for Environmental Epidemiology
Address Correspondence to Olav Axelson, Department of Occupational Medicine, University Hospital, 58 185 Linköping, Sweden. Telehone: 46 13 221440. Fax: 46 13 145831.
Introduction
In the sixteenth century, both Paracelsus and Agricola described a high mortality from pulmonary disorders among miners. In the retrospect, these observations have been taken to suggest a lung cancer risk from exposure to radon in mines. Other lung diseases might have been involved as well, however. In 1879, lung cancer was specifically reported to occur in excess among miners at Schneeberg in southeastern Germany (1). A few decades later a similar observation was made also at Joachimsthal in Czechoslovakia (2). Since radioactive minerals were found in the mines, radioactivity was suggested to be responsible for the excess of lung cancer among these miners (3). More generally, however, the etiological role of radon and its decay products for lung cancer was not well understood and agreed upon until the 1960s, when lung cancer cases appeared in U.S. uranium miners. Over the past one and a half decade, exposure to radon has become a public health concern as discovered to commonly occur also in dwellings, sometimes at fairly high concentrations.
Radon and its decay products
The decay of uranium through radium is the source of radon (or more precisely, radon-222). Radon itself decays further into a series of radioactive isotopes of polonium, bismuth and lead. The first four of these isotopes are referred to as short-lived radon progeny (or radon daughters) with half-lives from less than a millisecond up to almost 27 minutes. Like radon-222 itself, also the decay products polonium-218 and polonium-214 emit alpha-particles. Another isotope, radon-220, or thoron, originate from the thorium decay chain, but the short-lived decay products are thought to be of less hygienic interest.
The decay products of radon get electrically charged when created, and tend to attach to surfaces and dust particles in the air. Some also remain unattached. When the air is dusty, the unattached fraction tends to decrease. The unattached progeny is usually considered to be responsible for most of the alpha-irradiation delivered to the bronchial epithelium, at least in work situations with mouth-breathing, when this fraction is effectively deposited in the bronchia. Radon is not deposited so that the contribution of alpha-irradiation to the bronchial epithelium from the gas itself is relatively marginal. Some absoption of radon as well as the decay products takes place, however. An increasing interest is therefore also directed to the possibility of extra-pulmonary cancer risks.
The alpha-particles travel less than 100 micrometers into the tissue, but their high energy causes an intense local ionization, damaging the tissue with a subsequent risk for cancer development. Beta- and gamma-radiation is also present from some of the decay products but the much lower energy content compared to alpha-radiation makes the effect relatively marginal.
Units for measuring radon and decay products
Traditionally, and since the 1950s, the concentration of radon decay products, that is, radon daughters, or radon progeny, has been measured in working levels (WL) (4). One working level is defined as any combination of short-lived radon progeny in one litre of air that will ultimately release 1.3
105 MeV of alpha energy by decay through polonium-214. In more recently introduced units, this amount of radon progeny may be taken as equivalent to 3700 Bq/m3 EER (Equilibrium Equivalent Radon) (5) or 2.08 x 10-5 J/m3. The accumulated exposure to radiation is expressed in terms of working level months (WLM). In this context, one month refers to 170 hours of exposure. The corresponding SI-unit is the joule-hour per cubic meter, and 1 WLM is equal to 3.6 x 10-3 Jh/m3 and may also be taken as 72 Bq-years/m3.
Exposure to radon and radon progeny
Very high levels of radon have occurred in uranium mines but quite often also in metal mines. For example, cumulated occupational exposures of as much as 3720 WLM were in the past obtained in uranium mines (6). Radon progeny concentrations in many nonuranium mines have also been relatively high, often about 1 WL or more, e.g. in haematite mines in West Cumberland, Great Britain (7). A cumulated annual exposure of 2.5 - 4.3 WLM was obtained by French miners during the late 1950s and 1960s but decreased to 1.6 - 3.2 WLM during the following decade (8).
Both the use of stony building materials and ground conditions influence indoor concentrations of radon and its decay products. The leakage of radon from the ground shows great variations, and very high indoor concentrations can occur in one house but not in another even if located quite nearby. In general, the leakage of radon from the ground is usually more important than its emanation from stony building materials (9). Temperature, wind conditions, and air pressure, as well as behavioral factors influence ventilation and therefore the concentrations of radon and its decay products that may build up in a room. Efforts to improve insulation and preserve energy, may have impaired the situation (10-12). Radon dissolves to some extent in water, which may serve as a carrier. Wet mines therefore tend to be high in radon, and to some extent, radon in tap water may contribute to the indoor concentrations.
The first measurements on indoor radon were made in Swedish dwellings in the 1950s (13). The levels found were in the range of 20 - 69 Bq/m3. These observations seem not to have caused any concern from the hygienic point of view, however. Recent measurements of indoor radon in Swedish homes have revealed higher levels. On an average, 122 Bq/m3 were found in detached houses and 85 Bq/m3 in apartments. Great variations occurred, however, that is, from 11 to 3,300 Bq/m3 (14). The differences found between the earlier and the more recently measured concentrations may suggest a general increase in the levels over time.
Indoor radon with concentrations in the range of 40 - 100 Bq/m3 have been reported as an average from many countries, e.g. USA (15), Norway (16), Finland (17), Federal Republic of Germany (18), etc. Considerably higher levels like two or three thousand Bq/m3, may occur in many houses, and this is about double the level tolerated in mines in most countries (about 1100 Bq/m3 or 0.3 WL).
Lung cancer in miners
Many mining populations with exposure to radon and its decay products have been investigated, both by cohort and case-control studies. Some of the main results of these studies are summarized in tables 1 and 2. There is a remarkable consistency between the results as always indicating an increased risk of lung cancer among the miners, even if the overall risk ratios range from about 1.5 to 15. It may be noted in this context also, that other malignant disorders than lung cancer have not yet been clearly demonstrated to depend on radon progeny exposure in mines. A few studies of miners have shown a tendency towards an excess of stomach cancer, however (41).
Other agents than radon and its decay products are present in the mine atmosphere and might be thought of as also responsible for the lung cancer risk among miners, for example, carcinogenic trace metals in the dust. Arsenic might have been present at low concentrations in some mines and clearly influenced the risk in one study (33). Asbestiform fibres have occurred in some Swedish mines at least, but are considered less likely to have played any substantial role for miners' lung cancer (42). Silica dust exposure is a probable cause of lung cancer, especially among silicotics (43). Such exposure does not seem to explain the lung cancer risk of miners, however, at least not to any greater extent (44). Furthermore, where the exposure to radon and progeny has been very low as in coal (45), potash (46), and iron mining (47), little or no excess of lung cancer has been observed. Hence, taking these various studies together, the etiologic role of radon as a cause of lung cancer appears as well supported both through positive and negative epidemiologic observations.
Assessing exposure to indoor radon
Epidemiologic studies of indoor radon and lung cancer are demanding, especially regarding assessment of exposure. This aspect includes also the problem of obtaining proper contrasts in exposure. The main difficulties derive from the fact that some people spend most of their time at home, whereas others are more often out in the open air or have indoor activities elsewhere with subsequent exposure to different radon concentrations. Furthermore, almost everybody has lived in several houses with varying exposure levels. Only the exposure relating to the home environment would be possible to estimate reasonably accurate in the retrospect, whereas exposure obtained in other houses can hardly be accounted for. No support in exposure assessment can be obtained from the individual since there is no perception of exposure to radon and its decay products. This could be a benefit from the validity point of view, however, since there remains little room for discussing recall bias in case-control studies of the health effects of indoor radon.
To assess exposure to indoor radon, current measurements in a number of subsequently used homes of an individual are useful and even necessary. Still, such measurements do not provide any particularly good estimate of an individual's accumulated exposure over many decades. A combination of measurements and judgements with regard to pertinent characteristics of a house might nevertheless be assumed to give a usable estimate of radon progeny exposure. Contrasts in exposure tend to level out, however, so that studies on indoor radon are inherently insensitive and likely to underestimate an effect.
Cellulose nitrate film strips have been used for measuring radon decay products (or indirectly radon, which nowadays is thought to be preferable to direct measurements of radon progeny). Such measurements have also been found to agree relatively well with the exposure estimates based on various characteristics of the houses and geological features as likely to have determined indoor radon concentrations (48).
Studies of indoor radon and lung cancer
Several epidemiologic studies have been published since 1979 regarding the indoor radon and risk of lung cancer in the general population. With few exceptions, these studies have been of the case-control type. Most of these studies seem to suggest an effect of indoor radon with regard to lung cancer. The overall results of the various studies are summarized in table 3. Two studies of cohort character have also been reported (61,62), both being fairly inconclusive but showing tendencies consistent with an effect of indoor radon.
Some of the case-control studies provide little evidence of an effect, however. Especially a study from China on women has been taken to show no effect, but for small cell lung cancers, the odds ratio formally amounted to 1.7 (58). This study was conducted in an area with an unusually high risk of lung cancer in women. A high background may therefore have masked an effect of radon. It is of interest too, that in some studies, a less clear effect has been obtained for smokers as well as for urbanised people (48,57).
The first large study on indoor radon and lung cancer has now been preliminary reported from Sweden (63). It involves 1360 lung cancer cases and 2847 controls. Similar to earlier studies it showed a moderate but significant effect of indoor radon on lung cancer with an odds ratio of 1.3 for a time weighted exposure at 140-400 Bq/m3 and 1.8 at levels above 400 Bq/m3 of radon gas. Sleeping with an open window slit eliminated the risk totally. It was estimated that some 9 to 16 percent of the annual lung cancer cases in Sweden were attributable to indoor radon.
The histologic types of the lung cancer cases have usually not been considered in the studies referred to. One of the studies considered specifically oat-cell and other anaplastic lung cancers in women, however. This study showed a clear association with indoor radon (54). Another study demonstrated an interesting predominance of squamous and small cell carcinomas among those who had lived in non-wooden houses as likely to have had higher radon levels than wooden houses (53). Also the new large Swedish study showed the stronger effect for small cell carcinomas (63). These findings agree with the relative excess of small cell undifferentiated lung cancers seen in the studies on uranium miners. In course of time, however, the relative frequency of histologic types has become more normal in miners (64,65,66).
Some correlation studies relating to indoor radon have also indicated an association between lung cancer and indirect measures of potential radon emission from the ground. Some of these studies have utilized a contrast in exposure due radon emanation from phosphate deposits, that had been worked (67), or volcanic versus sedimentary structures (68). Another opportunity to find a contrasting exposure was obtained by comparison of lung cancer rates of the populations within and without areas with high radon emanation from granite with increased radioactivity (69). The estimated average of background gamma radiation per county has also been used as a proxy for potential indoor radon, since there tends to be a rather strong correlation between gamma radiation and emanation of radon from the ground (70). Some other of the more or less positive studies have been based on measurements of Ra-226 in water (71) or levels of radon in water and indoor air (72). Some correlation studies have come out negative with regard to lung cancer, for example, studies from Canada (73), China (74), and France (75).
The combined effect of smoking and radon
The effect of smoking and exposure to radon among miners has been more or less multiplicative in most studies with adequate data available (35,66,76,77). In a few studies there has been a merely additive relationship (25,40,41) and sometimes even less than an additive effect (34,78). Observations in the latter direction has also been observed regarding sputum cytology of uranium miners (79).
These rather inconsistent observations may be found puzzling but could simply depend on an influence from smoking on the dose received by the epithelium. Smoking seems to increase mucous secretion in a dusty mine environment, causing productive cough (80,81). When the mucous sheath get thicker, fewer alpha-particles are able to penetrate to the basal cells of the epithelium from which the cancer develops (82). An increase in thickness of the mucous layer of only about ten micrometers would decrease the dose to the epithelium by the order of some 50 percent (83,84). Furthermore, the clearance of deposited particles carrying radon decay products may also be influenced by smoking with consequences for the ultimate radiation dose delivered to the epithelium.
However, a synergism is likely to occur between chemicals in tobacco smoke and the actual dose of radiation to the epithelium, explaining the more or less multiplicative interaction between smoking and radon progeny exposure seen in most of the studies of miners, especially from the more modern and presumably less dusty mines. Similarly, for indoor radon progeny and smoking, a more or less multiplicative effect has been indicated, although the combined effect has sometimes been weak (48,54,56,57). In the new large scale Swedish study the combined effect appeared as clearly multiplicative, however (63).
Experimental data provide some support the complex view given here on the interaction of smoking and radon progeny exposure in miners. When smoking and non-smoking dogs were exposed to uranium ore dust and radon progeny, the smoking dogs were less affected by respiratory cancer than nonsmoking dogs (85). The reason was believed to be the relative protection offered by increased mucous secretion. On the other hand, experiments in rodents indicate that radon progeny exposure followed by exposure to cigarette smoke stimulated tumour development, whereas the reverse combination did not (86). Smoking may therefore play a complex role, exerting a carcinogenic effect but sometimes also reducing the dose to the epithelium by increasing mucous secretion. Such complex interaction might well explain the range of observed overall effect from multiplicative to less than additive.
The tendency of radon progeny to attach to environmental tobacco smoke and other particles in the air may imply further complexity of the interaction of smoking and radon progeny exposure. The air borne radioactivity tends to increase in the presence of tobacco smoke, as there is less plating out of radon progeny on walls, furniture and other surfaces in the room (87). The fraction of unattached progeny tends to be reduced, however, while the attached fraction increases proportionally.
The implications for the lung cancer risk in this respect is not very clear. Usually the lung cancer risk has been tied mainly to the unattached fraction as thought to contribute much more than the attached fraction to the radiation dose to the epithelium. However, the unattached radon progeny tends to be deposited in the nose to as much as about 50%, whereas the attached fraction is little affected by nose breathing (88,89). Attached radon progeny may therefore be deposited further down in bronchial regions with a thinner epithelium. Here the alpha-particles may be able to penetrate to the basal cells, from which cancer develops (84). The biological net effect of the increased radioactivity of smoke-polluted indoor air and the subsequent change of the proportion of unattached to attached radon progeny is therefore not clear, nor are there any epidemiologic observations in this respect.
A relation of extra-pulmonary cancers to indoor radon?
A relatively recent report indicate a correlation of the incidence of myeloid leukaemia, melanoma, cancer of the kidney, and certain childhood cancers to average radon exposure in the homes in a number of countries (90). Remarkably, however, lung cancer did not show any significant correlation, as would have been expected rather than the other positive correlations. Inhaled radon, finally reaching the bone marrow, was thought to have induced the myeloid leukaemia through its further decay. The accumulation of air borne radon progeny on the skin, and a filtering of radon progeny through the kidney, was suggested to explain the correlations seen for melanoma and kidney cancer, respectively.
These observations have been criticized (91) but initiated a case-control study of thirteen cancer forms in relation to residence in areas with different radon levels in the Viterbo province, Italy (92). Increased odds ratios between 2 and 3 were seen in the higher exposure categories for kidney cancer as well as for melanoma and myeloid leukaemia. The dose-response trend and the odds ratio was significantly high only for kidney cancer, however. For lung cancer, there was only a slightly increased risk in the intermediate exposure category. Confounding from smoking might have been negative, however, and was not controlled for in contrast to age, farming and degree of urbanisation.
Also two case-referent (case-control) studies on acute myeloid leukaemia (AML) might be of some interest in this context (93,94). Various exposures were assessed by questionnaires, i.e., occupational exposures, leisure time activities, smoking, medical care, particularly the use of drugs, x-ray treatment and x-ray examinations. Residency was considered in terms of estimated gamma radiation from concrete and other stony building materials. An exposure-response relationship was obtained with an index for background gamma radiation. Indoor radon exposure was not thought of as of importance at the time of the study. Since there tends to be a correlation between radon emanation and gamma radiation from building materials, the possibility remains that indoor radon exposure could have played some etiologic role in this context.
In some of the aforementioned correlation studies there was also a relation to radon exposure for other cancers, for example with regard to pancreatic cancer and male leukaemia (70), bladder and breast cancer (71), reproductive cancer in males as well as for all cancers taken together (72). The mortality rate from stomach cancer was found to be increased in an area with uranium deposits in New Mexico (96).
Epilogue
The results available so far from epidemiologic studies of indoor radon and lung cancer seem to agree fairly well with the data from miners. The conclusion might therefore be that indoor radon means a risk of lung cancer for the general population, but the quantitative aspect of this health hazard is not yet possible to assess more definitely. However, considering the lifetime risk of lung cancer in miners, one extra death per 1000 miners has been proposed as possibly acceptable, which would permit only an exposure of about 0.1 WLM per year (97). The magnitude of the indoor radon problem might then be considered in relation to the fact that the average background exposure in the US has been estimated to 0.2 WLM per year (and up to 0.4 WLM per year in the vicinity of radon emitting ore bodies). Furthermore, there are clear indications that the exposure levels may be even considerably higher for large population sectors in many countries.
It is far from clear, however, if the increased cancer risks reported also for other sites than the lung can be attributed to radon and progeny or concommittant gamma radiation. Further interest into the effects of background radiation can be anticipated for the next decade or so and may finally bring clarity to this question.
References
1. Härting FH, Hesse W. Der Lungenkrebs, die Bergkrankheit in den Schneeberger Gruben. Vierteljahrssehr Gerichtl Med Offentl Gesundheitswesen 30:296- 307, 31:102- 132, 31:313- 337(1879).
2. Arnstein A. Über den sogenannten "Schneeberger Lungenkrebs". Verh dt Gesellsch Pathol 16:332- 342(1913).
3. Ludewig P, Lorenser E. Untersuchung der Grubenluft in den Schneeberger Gruben auf den Gehalt und Radiumemanation. Strahlenterapie 17:428- 435(1924).
4. Holaday DA. Digest of the proceedings of the 7-state conference on health hazards in uranium mining. Arch Ind Health 12:465- 467(1955).
5. ICRP, International Commission on Radiological Protection. Radiation protection in uranium and other mines. ICRP publication no. 24. Oxford:Pergamon Press, 1976.
6. Lundin Jr FE, Wagoner JK, Archer VE. Radon daughter exposure and respiratory cancer. Quantitative and temporal aspects. NIOSH-NIEHS joint monograph No. 1. Springfield, VA: Public Health Service, 1971.
7. Boyd JP, Doll R, Faulds JS, Leiper J. Cancer of the lung in iron ore (haematite) miners. Br J Ind Med 27:97- 105(1970).
8. Tirmarche M, Brenot J, Piechowski J, Chameaud J, Pradel J. The present state of an epidemiological study of uranium miners in France. In: Proceedings of the International Conference, Occupational Radiation Safety in Mining, vol 1. Toronto:Canadian Nuclear Association, 1985;344- 349.
9. Åkerblom G, Wilson C. Radon - geological aspects of an environmental problem. Rapporter och meddelanden nr 30. Uppsala: Sveriges geologiska undersökning, 1982.
10. Dickson D. Home insulation may increase radiation hazard. Nature 276:431(1978).
11. Stranden E, Berteig L, Ugletveit F. A study on radon in dwellings. Health Phys 36:413- 421(1979).
12. McGregor RG, Vasudev P, Létourneau EG, McCullough RS, Prantl F A, Taniguchi H. Background concentrations of radon and radon daughters in Canadian homes. Health Phys 39:285- 289(1980).
13. Hultqvist B. Studies on naturally occurring ionizing radiations with special reference to radiation dose in Swedish houses of various types. Kungl svenska vetenskapsakademiens handlingar, 4:e serien, band 6, Nr 3. Stockholm: Almqvist och Wiksell Boktryckeri AB, 1956.
14. Swedjemark GA, Buren A, Mjönes L. Radon levels in Swedish homes: A comparison of the 1980s with the 1950s. In: Radon and its decay products - occurence, properties and health effects (Hopke PK, ed). Washington:American Chemical Society, 1987;85- 96
15. Nero AV, Schwehr MB, Nazaroff WW, Revzan KL. Distribution of airborne radon- 222 concentrations in U. S. homes. Science 234:992- 997(1986).
16. Stranden E. Radon-222 in Norwegian dwellings. In: Radon and its decay products - occurrence, properties and health effects (Hopke PK, ed). Washington: American Chemical Society, 1987; 70- 83.
17. Castren O, Mäkeläinen I, Winqvist K, Voutilainen A. Indoor radon measurements in Finland: A status report. In: Radon and its decay products - occurrence, properties and health effects (Hopke PK, ed). Washington:American Chemical Society, 1987;97- 103.
18. Schmier H, Wick A. Results from a survey of indoor radon exposures in the Federal Republic of Germany. Sci Total Environ 45:307- 310(1985).
19. Wagoner JK, Miller RW, Lundin Jr FE, Fraumeni JF, Haij NE. Unusual mortality among a group of underground metal miners. N Engl J Med 269:281- 289(1963).
20. Waxweiler RJ, Roscoe RJ, Archer VE, Thun MJ, Wagoner JK, Lundin E. Mortality follow-up through 1977 of the white underground uranium miners cohort examined by the United States Public Health Service. In: Radiation Hazards in Mining: Control, Measurement and Medical Aspects (Gomez M, ed). New York: Society of Mining Engineers of the American Institute of Mining, Metallurgical, and Petroleum Engineers, Inc, 1981;823- 830.
21. Placek V, Smid A, Sevc J, Tomasek L, Vernerova P. Late effects at high and very low exposure levels of the radon daughters. In: Radiation research - somatic and genetic effects. Proceedings of 70th International Congress of Radiation Research (Broerse JJ, Barendsen GW, Kal HB, Vanderkogel AJ, eds). Amsterdam: Martinus Nijhoff, 1983.
22. Kunz E, Sevc J, Placek V. Lung cancer in uranium miners. Health Phys 35:579- 580(1978).
23. Fox AJ, Goldblatt P and Kinlen LJ. A study of the mortality of Cornish tin miners. Br J Ind Med 38:378- 380(1981).
24. Jörgensen HS. Lung cancer among underground workers in the iron ore mine of Kiruna based on thirty years of observation. Ann Acad Med (Singapore) 13:371- 377(1984).
25. Radford EP, Renard KG St C. Lung cancer in Swedish iron miners exposed to low doses of radon daughters. N Engl J Med 310:1485- 1494(1984).
26. Morrison HI, Semenciw RM, Mao Y, Wigle DT. Cancer mortality among a group of fluorspar miners exposed to radon progeny. Am J Epidemiol 128:1266- 1275(1988).
27. Muller J, Wheeler WC, Gentleman JF, Suranvi G, Kusiak R. Study of mortality of Ontario miners. In: Occupational Radiation Safety in Mining. Proceedings of the International Conference (Stocker, ed). Toronto: Canadian Nuclear Association, 1985;335- 343.
28. Howe GR, Nair RC, Newcombe HB, Miller AB, Frost SE, Abbatt JD. Lung cancer mortality (1950- 1980) in relation to radon daughter in a cohort of workers at the Eldorado Beaverlodge uranium mine. J Natl Cancer 77:357- 362(1986).
29. Kinlen LJ, Willows AN. Decline in the lung cancer hazard: a prospective study of the mortality of iron ore miners in Cumbria. Br J Ind Med 45:219- 224(1988).
30. Battista G, Belli S, Garboncini F, Comba P, Giovanni L, Sartorelli P, Strambi F, Valentini F, Axelson O. Mortality among pyrite miners with low-level exposure to radon daughters. Scand J Environ Health 14:280- 285(1988).
31. Roscoe RJ, Steenland K, Halperin WE, Beaumont JJ, Waxweiler RJ. Lung cancer mortality among nonsmoking uranium miners exposed to radon daughters. J Am Med Ass 262:629- 633(1989).
32. Hodgson JT, Jones RD. Mortality of a cohort of tin miners 1941-86. Br J Ind Med 47:665- 676(1990).
33. Xiang-Zhen X, Lubin JH, Jun-Yao L, Li-Fen Y, Quing Sheng L, Lan Y, Jian-Zhang W, Blot WJ. A cohort study in southern China of tin miners exposed to radon and radon decay products. Health Phys 64:120- 131(1993).
34. Axelson O, Sundell L. Mining, lung cancer and smoking. Scand J Work Environ Health 4:46- 52(1978).
35. Damber L, Larsson LG. Combined effects of mining and smoking in the causation of lung cancer. A case-control study. Acta Radiol Oncol 21:305- 315(1982).
36. Edling C, Axelson O. Quantitative aspects of radon daughter exposure and lung cancer in underground miners. Br J Ind Med 40:182- 187(1983).
37. Samet JM, Kutvirt DM Waxweiler RJ, Key CR. Uranium mining and lungcancer in Navajo men. N Engl J Med 310:1481- 1484(1984).
38. Samet JM, Pathak DR, Morgan MV, Marbury MC, Key CR, Valdivia AA. Radon progeny exposure and lung cancer risk in New Mexico U miners. Health Phys 56:415- 421(1989).
39. Qiao Y, Taylor PR, Yao S-X, Schatzkin A, Mao B-L, Lubin J, Rao J-Y, McAdams M, Xuan X-Z, Li J-Y. Relation of radon exposure and tobacco use to lung cancer among tin miners in Yunnan province, China. Am J Ind Med 16:511- 521(1989).
40. Lubin J H, Qiao Y, Taylor P R, Yao S-X, Schatzkin A, Mao B-L, RaoJ-Y, Xuan X-Z, Li J-Y. Quantitative evaluation of the radonand lung cancer association in a case control study of Chinese tin miners. Cancer Res 50:174- 180(1990).
41. BEIR IV. Committee on the Biological Effects of Ionizing Radiations, US National Research Council. Health risk of radon and other internally deposited alpha-emitters. Washington: National Academy Press, 1988.
42. Edling C. Lung cancer and smoking in a group of iron ore miners. Am J Ind Med 3:191- 199(1982).
43. IARC Monographs on the evaluation of carcinogenic risks to humans, Supplement 7. Lyon: International Agency for Research on Cancer, 1987.
44. Archer VE, Roscoe J, Brown D. Is silica or radon daughters the important factor in the excess lung cancer among underground miners? In: Silica, silicosis, and cancer (Goldsmith DF, Winn DM, Shy CM eds). New York etc: Praeger, 1987;375- 384.
45. IARC Monographs on the evaluation of carcinogenic risks to humans. Radon and Man-made mineral fibres. Lyon: International Agency for Research on Cancer, 1988.
46. Waxweiler RJ, Wagoner JK, Archer VE. Mortality of potash workers. J Occup Med 15:486- 489(1973).
47. Lawler AB, Mandel JS, Schuman LM, Lubin JH. A retrospective cohort mortality study of iron ore (hematite) miners in Minnesota. J Occup Med 27:507- 517(1985).
48. Axelson O, Andersson K, Desai G, Fagerlund I, Jansson B, Karlsson C, Wingren G. A case-referent study on lung cancer, indoor radon and active and passive smoking. Scand J Work Environ Health 14:286- 292(1988).
49. Axelson O, Edling C, Kling H. Lung cancer and residency - A case referent study on the possible impact of exposure to radon and its daughters in dwellings. Scand J Work Environ Health 5:10- 15(1979).
50. Lanes SF, Talbott E, Radford E. Lung cancer and environmental radon. Am J Epidemiol 116:565(1982).
51. Edling C, Kling H, Axelson O. Radon in homes - A possible cause of lungcancer. Scand J Work Environ Health 10:25- 34(1984).
52. Pershagen G, Damber L, Falk R. Exposure to radon in dwellings and lung cancer: A pilot study. In: Indoor Air. Radon, passive smoking, particulates and housing epidemiology, vol 2 (Berglund B, Lindvall T, Sundell J, eds). Stockholm: Swedish Council for Building Research, 1984; 73- 78.
53. Damber LA, Larsson LG. Lung cancer in males and type of dwelling. An epidemiological pilot study. Acta Oncol 26:211- 215(1987).
54. Svensson C, Eklund G, Pershagen G. Indoor exposure to radon from the ground and bronchial cancer in women. Int Arch Occup Environ Health 59:123- 131(1987).
55. Lees REM, Steele R, Robert JH. A case-control study of lung cancer relative to domestic radon exposure. Int J Epidemiol 16:7- 12(1987).
56. Svensson C, Pershagen G, Klominek J. Lung cancer in women and type of dwelling in relation to radon exposure. Cancer Res 49: 1861- 1865(1989).
57. Schoenberg JB, Klotz JB, Wilcox HB, Gil-del-Real M, Stemhagen A, Nicholls GP. Lung cancer and exposure to radon in women - New Jersey. MMWR 38:715- 718(1989).
58. Blot WJ, Xu Z-Y, Boice Jr J D, Zhao D-Z, Stone B J, Sun J, Jing L-B, Fraumeni Jr JF. Indoor radon and lung cancer in China. J Natl Cancer Inst 82:1025- 1030(1990).
59. Ruosteenoja E: Indoor radon and risk of lung cancer: an epidemiological study in Finland. Dissertation. Helsinki: Finnish centre for radiation and nuclear safety, 1991.
60. Pershagen G, Liang Z-H, Hrubec Z, Svensson C, Boice JD. Residential radon exposure and lung cancer in Swedish women. Health Phys 63:179- 186(1992).
61. Simpson SG, Comstock GW. Lung cancer and housing characteristics. Arch Environ Health 38:248- 251(1983).
62. Klotz JB, Petix JR, Zagraniski RT. Mortality of a residential cohort exposed to radon from industrially contaminated soil. Am J Epidemiol 129:1179- 1186(1989).
63. Pershagen G, Åkerblom G, Axelson O, Clavensjö B, Damber L, Desai G, Enflo A, Lagarde F, Mellander H, Svartengren M, Swedjemark G A. Residential radon exposure and lung cancer in Sweden. N Engl J Med 330:159- 164 (1994).
64. Archer VE, Sacomanno G, Jones JH. Frequency of different histologic types of bronchogenic carcinoma as related to radon exposure. Cancer 34:2056- 2060(1974).
65. Horacek J, Placek V, Sevc J. Histologic types of bronchogenic cancer in relation to different conditions of radiation exposure. Cancer 34:832- 835(1977).
66. Saccomanno G, Huth GC, Auerbach O, Kuschner M. Relationship of radioactive radon daughters and cigarette smoking in the genesis of lung cancer in uranium miners. Cancer 62:1402- 1408(1988).
67. Fleischer RL. A possible association between lung cancer and phosphate mining and processing. Health Phys 41:171- 175(1981).
68. Forastiere F, Valesini S, Arca M, Magliola ME, Michelozzi P, Tasco C. Lung cancer and natural radiation in an Italian province. Sci Total Environ 45:519- 526(1985).
69. Archer VE. Association of Lung Cancer Mortality with Precambrian Granite. Occup Environ Health 42:87- 91(1987).
70. Edling C, Comba P, Axelson O, Flodin U. Effects of low-dose radiation - A correlation study. Scand J Work Environ Health 8: Suppl. 1, 59- 64(1982).
71. Bean JA, Isacson P, Hahne RMA, Kohler J. Drinking water and cancer incidence in Iowa. Am J Epidemiol 116:924- 32(1982).
72. Hess CT, Weiffenbach CV, Norton SA. Environmental radon and cancer correlation in Maine. Health Phys 45:339- 348(1983).
73. Letourneau EG, Mao Y, McGregor RG, Semenciw R, Smith MH, Wigle DT. Lung cancer mortality and indoor radon concentrations in 18 Canadian cities. Proceedings of the sixteenth midyear topical meeting of the Health Physics Society on Epidemiology applied to health physics. Albuquerque, Jan 9-13. Ottawa: Health physics Society, 1983;470- 483.
74. Hofmann W, Katz R, Zhang C. Lung cancer incidence in a Chinese high background area - epidemiological results and theoretical interpretation. Sci Total Environ 45:527- 534(1985).
75. Dousset M, Jammet H. Comparison de la mortalitie par cancer dans le Limousin et le Poitou-Charentes. Radioprotection GEDIM 20:61- 67 (1985).
76. Archer VE, Wagoner JK, Lundin FE. Uranium mining and cigarette smoking effects on man. J Occup Med 15:204- 211(1973).
77. Whittemore AS, McMillan A. Lung cancer mortality among U.S. uranium miners: A reappraisal. J Natl Cancer Inst 71:489- 499(1983).
78. Dahlgren E. Lungcancer, hjärt-kärlsjukdom och rökning hos en grupp gruvarbetare (Lung cancer, cardiovascular disease and smoking in a group of miners). Läkartidningen 76:4811- 4814(1979).
79. Band P, Feldstein M, Saccomanno G, Watson L, King G. Potentiation of cigarette smoking and radiation. Evidénce from a sputum cytology survey among uranium miners and controls. Cancer 45:1237- 1277(1980).
80. Sluis-Cremer GK, Walthers LG, Sichel HF. Chronic bronchitis in miners and non-miners: An epidemiological survey of a community in the goldmining area in Transvaal. Br J Ind Med 24:1- 12(1967).
81. Jörgensen H, Swensson A. Undersökning av arbetare i gruva med dieseldrift, särskilt med hänsyn till lungfunktion, luftvägssymtom och rökvanor (Investigation of workers in a mine with diesel drift, especially regarding lung function, respiratory symptoms and smoking habits; English summary). AI rapport No. 16. Stockholm: Arbetarskyddsverket, 1970.
82. Axelson O. Room for a role for radon in lung cancer causation? Medical Hypotheses 13:51- 61(1984).
83. Altschuler B, Nelson N, Kuschner M. Estimation of lung tissue dose from the inhalation of radon and daughters. Health Phys 10:1137- 1161(1964).
84. Walsh PJ. Radiation dose to the respiratory tract of uranium miners - A review of the literature. Environ Res 3:14- 36(1970).
85. Cross FT, Palmer R F, Filipy R E, Dagle G E, Stuart B O. Carcinogenic effects of radon daughters, uranium ore dust and cigarette smoke in beagle dogs. Health Phys 42:33- 52(1982).
86. Chameaud J, Masse R, Morin M, Lafuma J. Lung cancer induction by radon daughters in rats; present state of the data in low dose exposures. In: Proceedings of the International Conference on Occupational Radiation Safety in mining (Stocker H, ed). Toronto: Canadian Nuclear Association, 1985;350- 353.
87. Bergman H, Edling C, Axelson O. Indoor radon daughter concentrations and passive smoking. Environ Internat 12:17- 19(1986).
88. George AC, Breslin AJ. Deposition of radon daughters in human exposed to uranium mine atmospheres. Health Phys 17:115- 124(1969).
89. James AC. A reconsideration of cells at risk and other key factors in radon daughter dosimetry. In: Radon and its decay products - occurrence, properties and health effects (Hopke PH, ed). Washington: American Chemical Society, 1987;400- 418.
90. Henshaw DL, Eatough JP, Richardson RB. Radon as a causative factor of myeloid leukaemia and other cancers. Lancet 335:1008- 1012(1990).
91. Butland BK, Muirhead CR, Draper GJ. Radon and leukaemia. Lancet 335:138- 139(1990).
92. Forastiere F, Quiercia A, Cavariani F, Miceli M, Perucci CA, Axelson O. Cancer risk and radon exposure. Lancet 339:1115(1992).
93. Flodin U, Andersson L, Anjou C-G, Palm U-B, Vikrot O, Axelson O. A case-referent study on acute myeloid leukaemia, background radiation and exposure to solvents and other agents. Scand. J. Work Environ. Health 7:169- 178(1981).
94. Flodin U, Fredriksson M, Persson B, Axelson O. Acute myeloid leukaemia and background radiation in a expanded case-referent study. Arch Environ Health 45:364- 366(1990).
95. Tomasek L, Darby S, Swerdlow AJ, Placek V, Kunz E. Radon exposure and cancers other than lung cancer among uranium miners in West Bohemia. Lancet 341:919- 923(1993).
96. Wilkinson GS. Gastric cancer in New Mexico conties with significant deposits of uranium. Arch Environ Health 40:307- 312(1985).
97. NIOSH, National Institute for Occupational Safety and Health. A recommended standard for occupational exposure to radon progeny in underground mines. Washington:US Department of Health and Human Services, 1987.
Last Update: October 7, 1998