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Asbestos: Selected Cancers (2006)

Chapter: 9 Esophageal Cancer and Asbestos

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Suggested Citation:"9 Esophageal Cancer and Asbestos." Institute of Medicine. 2006. Asbestos: Selected Cancers. Washington, DC: The National Academies Press. doi: 10.17226/11665.
×

9
Esophageal Cancer and Asbestos

NATURE OF THIS CANCER TYPE

The esophagus is a muscular tube that carries food and liquid from the mouth to the stomach (Figures 7.1 and 9.1).

The American Cancer Society (Jemal et al. 2006) has estimated that 14,550 new cases of and 13,770 deaths from esophageal cancer (ICD-9 150; ICD-O-3 C15.0-15.9) will occur in the United States in 2006. Esophageal cancer ranks 19th in numbers of cases of cancer in the United States and sixth in developing countries (Kleihues and Stewart 2003).

The incidence is nearly 4 times higher in men than in women in the United States and slightly higher among blacks than among whites. The incidence has increased among men by an average of 1.7% per year since 1975, although the predominant histologic type and location of cancers in the esophagus have changed since the 1970s in most economically developed countries. Historically, the most common form of esophageal cancer worldwide was squamous-cell carcinoma, which occurred largely in the upper two-thirds of the esophagus (Blot 1994). Since the 1970s, the incidence of adenocarcinoma of the lower one-third of the esophagus and the junction with the stomach has increased by a factor of more than 5 among white and black men in the United States, whereas the incidence of squamous-cell carcinoma has decreased moderately. Rates of adenocarcinoma are also rising in women but are much lower than in men. Adenocarcinoma now makes up more than half of the esophageal cancers in white males, whereas squamous-cell carcinoma remains the predominant histologic type among black people and in high-incidence populations worldwide (Blot and McLaughlin 1999).

Suggested Citation:"9 Esophageal Cancer and Asbestos." Institute of Medicine. 2006. Asbestos: Selected Cancers. Washington, DC: The National Academies Press. doi: 10.17226/11665.
×

FIGURE 9.1 Anatomy of the esophagus, colon, rectum, and other digestive organs.

SOURCE: Copyright 2005 American Cancer Society, Inc. Reprinted with permission from www.cancer.org.

The incidence of carcinoma of the esophagus varies widely among countries. In regions extending from Iran through the steppes of Central Asia, Mongolia, and the northern portion of China, cancer frequencies are 10-100 times higher than in the countries at lowest risk. Squamous-cell carcinoma still predominates in the areas of high endemic risk, whereas adenocarcinoma now makes up about 50% of all cases in the low-risk areas of the United States, Europe, South Africa, Southeast Asia, and Japan.

The known risk factors differ somewhat for the two major histologic types of esophageal cancer. Known risk factors for squamous-cell carcinoma include all forms of tobacco-smoking (cigarettes, cigars, pipes, and bidis), use of chewing tobacco or snuff, and excessive consumption of alcohol. The combination of tobacco use and alcohol consumption potentiates the risk of either factor alone. Factors known to increase the risk of adenocarcinoma include chronic esophageal reflux (regurgitation of stomach acid and bile through the lower esophageal sphincter into the lower esophagus), obesity (which contributes to reflux), smoking, and achalasia (a type of esophageal dysfunction).

Adenocarcinoma of the esophagus develops from Barrett’s esophagus, a premalignant condition in which normal squamous epithelium of the lower esophagus is replaced with metaplastic columnar epithelium. The main cause of Barrett’s esophagus is thought to be chronic gastroesoph-

Suggested Citation:"9 Esophageal Cancer and Asbestos." Institute of Medicine. 2006. Asbestos: Selected Cancers. Washington, DC: The National Academies Press. doi: 10.17226/11665.
×

ageal reflux. People with Barrett’s esophagus are at increased risk for developing cancer of the esophagus and should be followed closely by their doctors. Even though they are at greater than average risk, most people with Barrett’s esophagus do not develop cancer of the esophagus.

EPIDEMIOLOGIC EVIDENCE CONSIDERED

Cohort Studies

The cohorts that presented usable information on the risk of esophageal cancer were indicated in Table 6.1. Their histories and design properties are described in Table B.1, and the details of their results concerning cancer at this site are abstracted in Table D.3. The results of both the cohort and case-control studies are summarized in Table 9.1, and Figures 9.2 and 9.3 are plots of relative risks (RRs) for overall exposure and for exposure-response gradients from the cohort studies reviewed.

TABLE 9.1 Summary of Epidemiologic Findings Regarding Cancer of Esophagus

Study Type

Figure

Comparison

Study Populations Included

No. Study Populations

Summary RR (95% CI)

Between-Study SD

Cohort

9.2

Any vs none

All

25

0.99

(0.79-1.27)

 

 

9.3

High vs nonea

Lower boundb

7

1.35

(0.81-2.27)

 

 

 

 

Upper boundb

7

1.43

(0.79-2.58)

Case- control

Any vs none

All

2

1.47

(0.87-2.47)

0.00

 

Any vs none

EAM = 1

1

 

 

 

 

 

EAM = 2

1

 

 

 

High vs nonea

EAM = 1

2

1.04

(0.50-1.80)

0.00

NOTE: CI = Confidence interval; EAM = exposure-assessment method; high quality, EAM = 1; lower quality, EAM = 2; RR = relative risk; SD = standard deviation.

aUsed studies that reported dose-response relationship (RR on an exposure gradient).

bFor studies that reported dose-response relationship on multiple gradient metrics, smallest “high vs none” RR was used to compute lower bound, and largest “high vs none” RR was used in computing the upper bound.

Suggested Citation:"9 Esophageal Cancer and Asbestos." Institute of Medicine. 2006. Asbestos: Selected Cancers. Washington, DC: The National Academies Press. doi: 10.17226/11665.
×

FIGURE 9.2 Cohort studies: RR of esophageal cancer in people with “any” exposure to asbestos compared with people who report no exposure.

Few studies presented data explicitly on esophageal cancer, because of its rarity. Therefore, observed numbers, and hence statistical precision, were low. Only UK asbestos-factory workers (Berry et al. 2000) and North American insulation workers (Selikoff and Seidman 1991) showed strong evidence of increased risk with any asbestos exposure. A suggestion that risk might be dose-dependent was seen among Finnish anthophyllite miners (Meurman et al. 1994) and UK textile workers (Peto et al. 1985). The

Suggested Citation:"9 Esophageal Cancer and Asbestos." Institute of Medicine. 2006. Asbestos: Selected Cancers. Washington, DC: The National Academies Press. doi: 10.17226/11665.
×

FIGURE 9.3 Cohort studies: RRs of esophageal cancer among people in extreme exposure category compared with those with none (◆ = more than one exposure gradient reported in citation, so the plot contains both highest and lowest estimates of risk for extreme category over all gradients).

aggregate estimated risk for all 25 cohort populations with information on esophageal cancer risk following any exposure to asbestos was neutral (RR = 0.99, 95% CI 0.79-1.27).

Case-Control Studies

The three case-control studies retained for thorough evaluation after excluding studies that did not assess exposure to asbestos or did not meet other exclusion criteria are listed Table 6.5 according to quality of their exposure assessment. The details of the design aspects of these studies are presented in Table C.1 and their detailed results are abstracted in Table E.3.

Suggested Citation:"9 Esophageal Cancer and Asbestos." Institute of Medicine. 2006. Asbestos: Selected Cancers. Washington, DC: The National Academies Press. doi: 10.17226/11665.
×

The findings of the studies are summarized in Table 9.1; data were inadequate to perform a meta-analysis.

There were two large, well-designed studies with asbestos exposure well assessed and analyses that adjusted for smoking, alcohol consumption, and other risk factors. Parent et al. (2000) assessed the relationship between esophageal cancer and occupational exposures as part of a large, population-based case-control study of men 35-70 years old in the Montreal area. A small excess was observed in esophageal cancers of all types, which decreased slightly when only substantial exposure was considered. A larger excess was observed for squamous-cell cancers specifically, which disappeared when only substantial exposure was considered. Although 21 cases were assessed as having some association with exposure to chrysotile asbestos, there were very few cases with substantial exposure (two overall, including one squamous-cell). Gustavsson et al. (1998) conducted a case-control study of occupational exposure and squamous-cell esophageal cancer among Swedish men 40-79 years old. No association was found with either low or high exposure.

The remaining study had an unusual design. Hillerdal (1980) conducted a case-control study of gastrointestinal cancer among participants in a general health survey conducted in Uppsala County, Sweden, in 1968-1972. Overall, 65-75% of the general population of the region and 80% of people with gastrointestinal cancer participated in the survey, which required a chest x-ray. Cases were identified through the Swedish Cancer Registry, and three controls, matched on age, were chosen for each case. Participants with bilateral pleural plaques were considered exposed. Results were presented as a ratio of observed exposed cases to expected, based on the rate in controls. One of the 21 people with esophageal cancer cases had pleural plaques vs 0.35 expected.

EVIDENCE INTEGRATION AND CONCLUSION

Evidence Considered

Both case-control and cohort studies of esophageal cancer were reviewed. Only three case-control studies met the criteria for inclusion, and so there were too few for a useful quantitative meta-analysis. There were relevant results from 25 cohort populations, although the number of cases was often small. The mortality studies did not distinguish between histologic subtypes, so associations could have been obscured. In assessing biologic plausibility, the cell type, potential dose at the target tissues, results, and possible mechanisms were considered. Findings related to the response to asbestos by esophageal tissues were evaluated from several well con-

Suggested Citation:"9 Esophageal Cancer and Asbestos." Institute of Medicine. 2006. Asbestos: Selected Cancers. Washington, DC: The National Academies Press. doi: 10.17226/11665.
×

ducted chronic rodent studies, four with inhalation exposure and six with dietary administration.

Consistency

The three case-control studies did not have consistent results, and the number of exposed cases was generally small. Two incorporated adjustment for tobacco and alcohol consumption; one of these observed an excess risk of squamous-cell cancer without evidence of a dose-response relationship, and the other found no evidence of an excess. A third, older study found an excess based on a single case, which was difficult to interpret.

Because of the relative rarity of esophageal cancer, few cohort studies presented data explicitly on this endpoint; and when they did, the statistical precision was routinely low. The results of the 20 citations that presented information on esophageal cancer in 25 cohort populations were mixed. Berry et al. (2000) and Selikoff and Seidman (1991) saw strong evidence of increased risk with any exposure, while Meurman et al. (1994) and Peto et al. (1985) found some evidence of a dose-response relationship. Findings from the remaining studies either were close to null, presented mixed or inconsistent results, or indicated lower than expected risks.

Strength of Association

There were too few case-control studies for a meaningful combined analysis. Several cohort studies did observe a dose-response relationship based on relatively small numbers; but when all 25 cohort populations were considered in the meta-analysis, no increase in RR was observed. Some studies did observe excess risks, but overall there was little consistency in the epidemiologic data.

Coherence

The most common histologic type of cancer arising in the upper two-thirds of the esophagus is squamous-cell carcinoma. That is probably the most common histologic type encountered in the epidemiologic studies of workers in the 1970s and earlier. The major risk factors are tobacco-smoking and tobacco-chewing, snuff use, and alcohol consumption. Since the 1970s, the major histologic type of esophageal cancer has been adenocarcinoma arising in the lower one-third of this anatomic region. Major risk factors for this type of esophageal cancer are reflux, obesity, achalasia, and tobacco-smoking. Although the combination of asbestos exposure and tobacco-smoking is an established risk factor for lung cancer, there is no

Suggested Citation:"9 Esophageal Cancer and Asbestos." Institute of Medicine. 2006. Asbestos: Selected Cancers. Washington, DC: The National Academies Press. doi: 10.17226/11665.
×

epidemiologic or experimental evidence addressing whether asbestos is a cofactor with tobacco use or alcohol consumption in the development of esophageal cancer.

Asbestos bodies have been identified in the esophagus (Kobayashi et al. 1987), but contamination during collection or processing of tissue samples is a possibility, as discussed in Chapter 4.

No increase in esophageal tumors has been observed in animals exposed chronically to asbestos either by inhalation (Hesterberg et al. 1993, 1994; McConnell 2005; McConnell et al. 1994a,b, 1999) or by oral feeding (HHS 1983, 1985, 1988, 1990a,b,c). There is no other experimental evidence that asbestos fibers act as a direct or indirect carcinogen specifically in the esophagus.

Conclusion

Some studies have found an association between asbestos exposure and esophageal cancer, but the overall results of epidemiologic studies are mixed. In addition, what little evidence there is from animal experiments about asbestos’s carcinogenic potential specifically on esophageal tissues does not support biological activity at this site. On the basis of those observations, the committee concluded that the evidence is inadequate to infer the presence or absence of a causal relationship between asbestos exposure and esophageal cancer.

REFERENCES

Acheson ED, Gardner MJ, Winter PD, Bennett C. 1984. Cancer in a factory using amosite asbestos. International Journal of Epidemiology 13(1): 3-10.

Armstrong BK, de Klerk NH, Musk AW, Hobbs MS. 1988. Mortality in miners and millers of crocidolite in Western Australia. British Journal of Industrial Medicine 45(1): 5-13.

Berry G, Newhouse ML, Wagner JC. 2000. Mortality from all cancers of asbestos factory workers in east London 1933-1980. Occupational and Environmental Medicine 57(11): 782-785.

Blot WJ. 1994. Esophageal cancer trends and risk factors. Seminars in Oncology 21(4): 403-410.

Blot WJ, McLaughlin JK. 1999. The changing epidemiology of esophageal cancer. Seminars in Oncology 26 (5 Supplement 15): 2-8.

Enterline PE, Hartley J, Henderson V. 1987. Asbestos and cancer: A cohort followed up to death. British Journal of Industrial Medicine 44(6): 396-401.

Finkelstein MM, Verma DK. 2004. A cohort study of mortality among Ontario pipe trades workers. Occupational and Environmental Medicine 61(9): 736-742.

Gardner MJ, Winter PD, Pannett B, Powell CA. 1986. Follow up study of workers manufacturing chrysotile asbestos cement products. British Journal of Industrial Medicine 43(11): 726-732.

Suggested Citation:"9 Esophageal Cancer and Asbestos." Institute of Medicine. 2006. Asbestos: Selected Cancers. Washington, DC: The National Academies Press. doi: 10.17226/11665.
×

Gustavsson P, Jakobsson R, Johansson H, Lewin F, Norell S, Rutkvist LE. 1998. Occupational exposures and squamous cell carcinoma of the oral cavity, pharynx, larynx, and oesophagus: A case-control study in Sweden. Occupational and Environmental Medicine 55(6): 393-400.

Hesterberg TW, Miller WC, McConnell EE, Chevalier J, Hadley JG, Bernstein DM, Thevenaz P, Anderson R. 1993. Chronic inhalation toxicity of size-separated glass fibers in Fischer 344 rats. Fundamental and Applied Toxicology 20(4): 464-476.

Hesterberg TW, Miller WC, Mast R, McConnell EE, Bernstein DM, Anderson R. 1994. Relationship between lung biopersistence and biological effects of man-made vitreous fibers after chronic inhalation in rats. Environmental Health Perspectives 102 (Supplement 5): 133-137.

HHS (US Department of Health and Human Services). 1983. Lifetime Carcinogenesis Studies of Amosite Asbestos (CAS NO. 12172-73-5) in Syrian Golden Hamsters (Feed Studies). NTP TR 249. Research Triangle Park, NC: National Toxicology Program.

HHS. 1985. Toxicology and Carcinogenesis Studies of Chrysotile Asbestos (CAS No. 12001-29-5) in F344/N Rats (Feed Studies). NTP TR 295. Research Triangle Park, NC: National Toxicology Program.

HHS. 1988. Toxicology and Carcinogenesis Studies of Crocidolite Asbestos (CAS No. 12001-28-4) in F344/N Rats (Feed Studies). NTP TR 280. Research Triangle Park, NC: National Toxicology Program.

HHS. 1990a. Lifetime Carcinogenesis Studies of Chrysotile Asbestos (CAS No. 12001-29-5) in Syrian Golden Hamsters (Feed Studies). NTP TR 246. Research Triangle Park, North Carolina: National Toxicology Program.

HHS. 1990b. Toxicology and Carcinogenesis Studies of Amosite Asbestos (CAS No. 12172-73-5) in F344/N Rats (Feed Studies). NTP TR 279. Research Triangle Park, NC: National Toxicology Program.

HHS. 1990c. Toxicology and Carcinogenesis Studies of Tremolite (CAS No. 14567-73-8) in F344/N Rats (Feed Studies). NTP TR 277. Research Triangle Park, NC: National Toxicology Program.Hillerdal G. 1980. Gastrointestinal carcinoma and occurrence of pleural plaques on pulmonary X-ray. Journal of Occupational Medicine 22(12): 806-809.

Hodgson JT, Jones RD. 1986. Mortality of asbestos workers in England and Wales 1971-81. British Journal of Industrial Medicine 43(3): 158-164.

Hughes JM, Weill H, Hammad YY. 1987. Mortality of workers employed in two asbestos cement manufacturing plants. British Journal of Industrial Medicine 44(3): 161-174.

Jemal A, Siegel R, Ward E, Murray T, Xu J, Smigal C, Thun M. 2006. Cancer statistics, 2006. CA: A Cancer Journal for Clinicians 56: 106-130.

Karjalainen A, Pukkala E, Kauppinen T, Partanen T. 1999. Incidence of cancer among Finnish patients with asbestos-related pulmonary or pleural fibrosis. Cancer Causes and Control 10(1): 51-57.

Kleihues P, Stewart BW, eds. 2003. World Cancer Report. Lyon, France: International Agency for Research on Cancer.

Kobayashi H, Ming ZW, Watanabe H, Ohnishi Y. 1987. A quantitative study on the distribution of asbestos bodies in extrapulmonary organs. ACTA Pathologica Japonica 37(3): 375-383.

Levin J, McLarty J, Hurst GA, Smith A, Frank AL. 1998. Tyler asbestos workers: Mortality experience in a cohort exposed to amosite. Occupational and Environmental Medicine 55(3): 155-160.

McConnell EE. 2005 (October 27). Personal Communication to Mary Paxton for the Committee on Asbestos: Selected Health Effects. Available in IOM Public Access Files.

McConnell E, Kamstrup O, Musselman R, Hesterberg T, Chevalier J, Miller W, Thevenaz P. 1994a. Chronic inhalation study of size-separated rock and slag wool insulation fibers in Fischer 344/N rats. Inhalation Toxicology 6(6): 571-614.

Suggested Citation:"9 Esophageal Cancer and Asbestos." Institute of Medicine. 2006. Asbestos: Selected Cancers. Washington, DC: The National Academies Press. doi: 10.17226/11665.
×

McConnell E, Mast R, Hesterberg T, Chevalier J, Kotin P, Bernstein D, Thevenaz P, Glass L, Anderson R. 1994b. Chronic inhalation toxicity of a kaolin-based refactory cermaic fiber in Syrian golden hamsters. Inhalation Toxicology 6(6): 503-532.

McConnell EE, Axten C, Hesterberg TW, Chevalier J, Miller WC, Everitt J, Oberdorster G, Chase GR, Thevenaz P, Kotin P. 1999. Studies on the inhalation toxicology of two fiberglasses and amosite asbestos in the Syrian golden hamster: Part II. Results of chronic exposure. Inhalation Toxicology 11(9): 785-835.

McDonald JC, Liddell FD, Dufresne A, McDonald AD. 1993. The 1891-1920 birth cohort of Quebec chrysotile miners and millers: Mortality 1976-88. British Journal of Industrial Medicine 50(12): 1073-1081.

Meurman LO, Pukkala E, Hakama M. 1994. Incidence of cancer among anthophyllite asbestos miners in Finland. Occupational and Environmental Medicine 51(6): 421-425.

Parent ME, Siemiatycki J, Fritschi L. 2000. Workplace exposures and oesophageal cancer. Occupational and Environmental Medicine 57(5): 325-334.

Peto J, Doll R, Hermon C, Binns W, Clayton R, Goffe T. 1985. Relationship of mortality to measures of environmental asbestos pollution in an asbestos textile factory. Annals of Occupational Hygiene 29(3): 305-355.

Puntoni R, Merlo F, Borsa L, Reggiardo G, Garrone E, Ceppi M. 2001. A historical cohort mortality study among shipyard workers in Genoa, Italy. American Journal of Industrial Medicine 40(4): 363-370.

Reid A, Ambrosini G, de Klerk N, Fritschi L, Musk B. 2004. Aerodigestive and gastrointestinal tract cancers and exposure to crocidolite (blue asbestos): Incidence and mortality among former crocidolite workers. International Journal of Cancer 111(5): 757-761.

Seidman H, Selikoff IJ, Gelb SK. 1986. Mortality experience of amosite asbestos factory workers: Dose-response relationships 5 to 40 years after onset of short-term work exposure. American Journal of Industrial Medicine 10(5-6): 479-514.

Selikoff IJ, Seidman H. 1991. Asbestos-associated deaths among insulation workers in the United States and Canada, 1967-1987. Annals of the New York Academy of Sciences 643: 1-14.

Selikoff IJ, Hammond EC, Seidman H. 1979. Mortality experience of insulation workers in the United States and Canada, 1943-1976. Annals of the New York Academy of Sciences 330: 91-116.

Szeszenia-Dabrowska N, Urszula W, Szymczak W, Strzelecka A. 2002. Mortality study of workers compensated for asbestosis in Poland, 1970-1997. International Journal of Occupational Medicine and Environmental Health 15(3): 267-278.

Tola S, Kalliomaki PL, Pukkala E, Asp S, Korkala ML. 1988. Incidence of cancer among welders, platers, machinists, and pipe fitters in shipyards and machine shops. British Journal of Industrial Medicine 45(4): 209-218.

Suggested Citation:"9 Esophageal Cancer and Asbestos." Institute of Medicine. 2006. Asbestos: Selected Cancers. Washington, DC: The National Academies Press. doi: 10.17226/11665.
×
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Suggested Citation:"9 Esophageal Cancer and Asbestos." Institute of Medicine. 2006. Asbestos: Selected Cancers. Washington, DC: The National Academies Press. doi: 10.17226/11665.
×
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Suggested Citation:"9 Esophageal Cancer and Asbestos." Institute of Medicine. 2006. Asbestos: Selected Cancers. Washington, DC: The National Academies Press. doi: 10.17226/11665.
×
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Suggested Citation:"9 Esophageal Cancer and Asbestos." Institute of Medicine. 2006. Asbestos: Selected Cancers. Washington, DC: The National Academies Press. doi: 10.17226/11665.
×
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Suggested Citation:"9 Esophageal Cancer and Asbestos." Institute of Medicine. 2006. Asbestos: Selected Cancers. Washington, DC: The National Academies Press. doi: 10.17226/11665.
×
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Suggested Citation:"9 Esophageal Cancer and Asbestos." Institute of Medicine. 2006. Asbestos: Selected Cancers. Washington, DC: The National Academies Press. doi: 10.17226/11665.
×
Page 198
Suggested Citation:"9 Esophageal Cancer and Asbestos." Institute of Medicine. 2006. Asbestos: Selected Cancers. Washington, DC: The National Academies Press. doi: 10.17226/11665.
×
Page 199
Suggested Citation:"9 Esophageal Cancer and Asbestos." Institute of Medicine. 2006. Asbestos: Selected Cancers. Washington, DC: The National Academies Press. doi: 10.17226/11665.
×
Page 200
Suggested Citation:"9 Esophageal Cancer and Asbestos." Institute of Medicine. 2006. Asbestos: Selected Cancers. Washington, DC: The National Academies Press. doi: 10.17226/11665.
×
Page 201
Suggested Citation:"9 Esophageal Cancer and Asbestos." Institute of Medicine. 2006. Asbestos: Selected Cancers. Washington, DC: The National Academies Press. doi: 10.17226/11665.
×
Page 202
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In conjunction with drafting comprehensive legislation concerning compensation for health effects related to asbestos exposure (the Fairness in Asbestos Injury Act), the Senate Committee on the Judiciary directed the Institute of Medicine to assemble the Committee on Asbestos: Selected Health Effects. This committee was charged with addressing whether asbestos exposure is causally related to adverse health consequences in addition to asbestosis, mesothelioma, and lung cancer. Asbestos: Selected Cancers presents the committee's comprehensive distillation of the peer-reviewed scientific and medical literature regarding association between asbestos and colorectal, laryngeal, esophageal, pharyngeal, and stomach cancers.

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