Re: Dutheil et al. Prostate Cancer and Asbestos: A Systematic Review and Meta-Analysis



 

Paolo Boffetta, MD, MPH1,2; Nicolò Franco, MD3; Attilia Gullino, MD, PHD4; Enrico Pira, MD5

Perm J 2020;25:20.215 [Full Citation]

https://doi.org/10.7812/TPP/20.215
E-pub: 12/30/2020

The letter has not been published or simultaneously submitted for publication in whole or in part elsewhere.

Sir,

We read with interest the systematic review and meta-analysis by Dutheil et al.1 on occupational and residential exposure to asbestos and prostate cancer risk. We believe this study suffers from several methodological errors.

First, the search of the literature appears to be deficient. We conducted a quick search, which we do not pretend was systematic, and identified 10 studies that reported results on risk of prostate cancer among asbestos exposed workers and were not included in the review by Dutheil et al.1 (Table 1; outdated results were included for 4 studies). Notably, the 2 studies that included the largest number of prostate cancer deaths (Lin et al., 2015 and Ferrante et al., 2017) were not included in the meta-analysis by Dutheil et al.1

Table 1. Selected studies reporting results on risk of prostate cancer among asbestos exposed workers that were not included in the review by Dutheil et al.1

Study Industry Asbestos type Country Outcome Sex N Obs SMR 95% CI
Acheson et al., 1984a,6 Insulation product mft Am UK Mo M 4820 2 0.94 0.11-3.40
Selikoff and Seidman, 1991a,7 Insulation workers Mix US, Canada Mo M 17800 59 1.12 0.85-1.45
Sanden et al., 19928 Shipyard workers P Ch Sweden Mo M 3893 22 0.80 0.50-1.21
Ulvestad et al., 20029 Cement workers P Ch Norway In M 541 8 0.6 0.3-1.1
Lin et al., 201510 Mixed Mix Taiwan In M 121883 307 0.67 0.59-0.75
Levin et al., 201611 Insulation product mft Am USA Mo PM 1130 6 0.78 0.29-1.70
Pira et al., 2016a,b,12 Textile product mft Mix Italy Mo M 894 7 0.74 0.38-1.94
Ferrante et al., 201713 Mixed Mix Italy Mo M 46060 352 0.97 0.87-1.08
Pira et al., 2017a,b,14 Miners Ch Italy Mo M 1056 9 0.91 0.42-1.74
Rusiecki et al., 2018a,b,15 Shipyard workers NA USA Mo PM 4702 281 0.85 0.57-1.23

Results in italics are derived from raw data reported in the original publications.

a An earlier report of this cohort was included in the review by Dutheil et al.1

b Workers at high asbestos exposure.

Am = amosite; Ch = chrysotile; CI = confidence interval; In = incidence; M = male; mft = manufacture; Mix = mixed fibers; Mo = mortality; N = number of workers; NA = not available; Obs = observed cases or deaths; P Ch = predominantly chrysotile; PM = predominantly (> 90%) male; SMR = standardized mortality ratio (standardized incidence ratio for studies on prostate cancer incidence).

Second, Dutheil et al.1 double-counted some observations. In particular, the papers by Reid et al.2 and Armstrong et al.3 refer to the same cohort of Australian crocidolite workers.

Third, it is debatable whether cohorts of oil refinery workers, such as that studied by Tsai et al.,4 should be included in reviews on asbestos, since these workers are exposed to other potential carcinogens. In any case, if one particular cohort of oil refinery workers is included, it is not clear why the many other cohorts from the same industry are excluded.

Fourth, we think that it is a mistake to combine results of prostate cancer incidence and mortality. On the one hand, prostate cancer incidence is highly sensitive to the implementation of screening with prostate specific antigen.5 On the other hand, mortality from prostate cancer depends on access to effective treatment. These 2 factors might vary between asbestos-exposed workers and the national or regional populations that are used as reference in the studies. These sources of bias require careful consideration, and combining the 2 measures of occurrence, whose biases might act in opposite directions, generates confusion in the results.

For these reasons, we think that the results of the meta-analysis by Dutheil et al.1 are not interpretable and their conclusion that asbestos exposure is associated with prostate cancer is not justified. A careful review of this issue should be based on stronger methodology than the one used by Dutheil et al.1

Disclosure Statement

Paolo Boffetta was involved in litigation on asbestos exposure and prostate cancer risk. Enrico Pira has acted as Court-appointed expert witness and as consultant to parties (judge, prosecutor, and defendant attorney) in asbestos litigations.

Author Affiliations

1Stony Brook Cancer Center, Stony Brook University, Stony Brook, NY

2Department of Medical and Surgical Sciences, University of Bologna, Bologna, Italy

3Department of Public Health Sciences and Pediatrics, University of Turin, Turin, Italy

4University Hospital City of Health and Science of Turin, Turin, Italy

5Department of Public Health Sciences and Pediatrics, University of Turin, Turin, Italy

Corresponding Author

Paolo Boffetta, MD, MPH (paolo.boffetta@stonybrookmedicine.com)

Author Contributions

All authors contributed to the design of the study. Paolo Boffetta and Nicolò Franco drafted the manuscript; all authors reviewed and approved the manuscript.

Funding

No funds were obtained for the study.

How to Cite this Article

Boffetta P, Franco N, Gullino A, Pira E. Re: Dutheil et al. Prostate cancer and asbestos: A systematic review and meta-analysis [Letter]. Perm J 2020;25:20.215. DOI: 10.7812/TPP/20.215

References

1. Dutheil F, Zaragoza-Civale L, Pereira B, et al Prostate cancer and asbestos: A systematic review and meta-analysis. Perm J 2020 Feb;24:19.086. DOI: https://doi.org/10.7812/TPP/19.086

2. Reid A, Franklin P, Olsen N, et al All-cause mortality and cancer incidence among adults exposed to blue asbestos during childhood. Am J Ind Med 2013 Feb;56(2):133-45. DOI: https://doi.org/10.1002/ajim.22103, PMID:22886909

3. Armstrong BK, de Klerk NH, Musk AW, Hobbs MS. Mortality in miners and millers of crocidolite in Western Australia. Br J Ind Med 1988 Jan;45(1):5-13. DOI: https://doi.org/10.1136/oem.45.1.5, PMID:2829959

4. Tsai SP, Waddell LC, Gilstrap EL, Ransdell JD, Ross CE. Mortality among maintenance employees potentially exposed to asbestos in a refinery and petrochemical plant. Am J Ind Med 1996 Jan;29(1):89-98. DOI: https://doi.org/10.1002/(sici)1097-0274(199601)29:1<89::aid-ajim11>3.0.co;2-w, PMID:8808046

5. Thompson IM, Ankerst DP. Prostate-specific antigen in the early detection of prostate cancer. Can Med Assoc J 2007 Jun;176(13):1853-8 DOI: https://doi.org/10.1503/cmaj.060955, PMID:17576986

6. Acheson ED, Gardner MJ, Winter PD, Bennett C. Cancer in a factory using amosite asbestos. Int J Epidemiol 1984;13(1):3-10.

7. Selikoff IJ, Seidman H. Asbestos-associated deaths among insulation workers in the United States and Canada, 1967-1987. Ann N Y Acad Sci 1991;643:1-14.

8. Sandén A, Järvholm B, Larsson S, Thiringer G. The risk of lung cancer and mesothelioma after cessation of asbestos exposure: A prospective cohort study of shipyard workers. Eur Respir J 1992;5(3):281-5.

9. Ulvestad B, Kjaerheim K, Martinsen JI, et al Cancer incidence among workers in the asbestos-cement producing industry in Norway. Scand J Work Environ Health 2002;28(6):411-7.

10. Lin CK, Chang YY, Wang JD, Lee LJ. Increased standardised incidence ratio of malignant pleural mesothelioma in Taiwanese asbestos workers: A 29-year retrospective Cohort study. BioMed Res In 2015.

11. Levin JL, Rouk A, Shepherd S, Hurst GA, McLarty JW. Tyler asbestos workers: A mortality update in a cohort exposed to amosite. J Toxicol Environ Health B Crit Rev 2016;19(5-6):190-200.

12. Pira E, Romano C, Violante FS, et al Updated mortality study of a cohort of asbestos textile workers. Cancer Med 2016;5(9):2623-8.

13. Ferrante D, Chellini E, Merler E, et al Italian pool of asbestos workers cohorts: Mortality trends of asbestos-related neoplasms after long time since first exposure. Occup Environ Med 2017;74(12):887-98.

14. Pira E, Romano C, Donato F, Pelucchi C, Vecchia C, Boffetta P. Mortality from cancer and other causes among Italian chrysotile asbestos miners. Occup Environ Med 2017;74(8):558-563.

15. Rusiecki J, Stewart P, Lee D et al Mortality among coast guard shipyard workers: A retrospective cohort study of specific exposures. Arch Environ Occup Health 2018;73:1, 4-18.

To the Editor: We thank Boffetta et al.1 for their relevant comments concerning our recent systematic review and metaanalysis on asbestos exposure and prostate cancer.2

First, Boffetta et al.1 identified putatively 10 missing articles in our meta-analyses (comprising 30 articles). However, we want to acknowledge that all the suggested articles are not retrieved in any databases using our search strategy. Our algorithm was (prostate cancer OR prostatic neoplasm) AND (asbestos* OR crocidolite* OR chrysotile* OR amphibole* OR amosite*). All the 10 suggested articles did not describe prostate cancer within their title or their abstract. They were impossible to detect using our algorithm, as those articles did not focus at all on prostate cancer—prostate cancer is only described as one line in a table in those articles. The only way to systematically retrieve the 10 suggested articles would have been to broaden the keywords by removing the “prostate” keyword. Using our algorithm (ie, derivates from “prostate cancer” and “asbestos”), we had a putative number of 2547 articles to include in our metaanalysis. Broadening our algorithm without “prostate” (ie, derivates from “cancer” and “asbestos”), the number of putative articles to include would rise to more than 25,000 (10 times more), which is clearly nonmanageable. Boffetta et al.1 are experts on asbestos exposure, and we are thankful from their comments. However, articles were probably retrieved from their knowledge without using our algorithm, but this is not the way to compute a metaanalysis using a reproducible search strategy. Lastly, we also want to point out that we included twice more articles than the preceding metaanalysis of Peng et al.3 published quite simultaneously with our metaanalyses.

Second, we did not double-count the same observations. Armstrong et al.4 studied occupational asbestos exposure in miners, whereas Reid et al.5 described environmental exposure in children living around the mine. Moreover, the studies were published in 19884 and 20135 (ie, with a 25-year gap).

Third, concerning the inclusion of several type of workers (eg, miners, shipyard workers, firefighters, textile industry) and particularly oil refinery workers (ie, maintenance workers exposed to asbestos contained in insulation materials), all of these occupations were exposed to several pollutants and toxics (benzenes, metal fumes, petroleum derived, radiations, smokes, and carbon residues), rendering difficult robust conclusions on the specific link between the asbestos exposure and prostate cancer. To avoid exposition bias, we chose to include all workers or residents exposed to asbestos particles. There is a whole section discussing this limitation in the dedicated section of our article.

Fourth, we totally agree that it might be a bias to mix incidence data and mortality. This is why we computed a sensitivity analyses by type of risk (distinguishing mortality and incidence data): “Stratified results by type of risk demonstrated an increased risk of prostate cancer with standardized incidence ratio (effect size = 1.16, 95% CI = 1.04-1.27) and with standardized rate ratio (1.06, 1.04-1.27), whereas there was no evidence of an increased risk with standard mortality ratio and hazard ratio (1.09, 0.98-1.19; and 0.79, 0.45-1.13, respectively).”

In total, we understand the comments from Boffetta et al.,1 even if answers were already within the articles. Metaanalysis follows a very logical methodology and has its own rules that some less-experienced readers might not be accustomed to. Our conclusions seem perfectly salient and careful; that is, “Asbestos exposure “seems to” increase the risk of prostate cancer.”

Disclosure Statement

The author(s) have no conflicts of interest to disclose.

Author Affiliations

In Response. Frédéric Dutheil MD, PhD1,2

1Université Clermont Auvergne, CNRS, LaPSCo, Physiological and Psychosocial Stress, University Hospital of Clermont–Ferrand, CHU Clermont–Ferrand, Occupational and Environmental Medicine, WittyFit, Clermont–Ferrand, France

2Faculty of Health, School of Exercise Science, Australian Catholic University, Melbourne, Victoria, Australia

Laetitia Zaragoza-Civale MD3

3University Hospital of Clermont Ferrand, CHU Clermont–Ferrand, Occupational and Environmental Medicine, Clermont-Ferrand, France

Bruno Pereira PhD4

4University Hospital of Clermont Ferrand, CHU Clermont–Ferrand, Clinical Research and Innovation Direction, Clermont-Ferrand, France

Martial Mermillod PhD5,6

5Univ. Grenoble Alpes, Univ. Savoie Mont Blanc, CNRS, LPNC, Grenoble, France

6Institut Universitaire de France, Paris, France

Julien S Baker PhD7

7University of the West of Scotland, Institute for Clinical Exercise and Health Science, Hamilton, UK

Jeannot Schmidt MD8

8Université Clermont Auvergne, CNRS, LaPSCo, Physiological and Psychosocial Stress, University Hospital of Clermont-Ferrand (CHU), Emergency department, Clermont-Ferrand, France

Fares Moustafa MD, PhD9

9Université Clermont Auvergne, University Hospital of Clermont-Ferrand (CHU), Emergency department, Clermont-Ferrand, France

Valentin Navel MD10

10Université Clermont Auvergne, CNRS, INSERM, GReD, Translational Approach to Epithelial Injury and Repair, CHU Clermont-Ferrand, University Hospital of Clermont-Ferrand, Ophthalmology, Clermont-Ferrand, France

Corresponding Author

Frédéric Dutheil, (fdutheil@chu-clermontferrand.fr)

How to Cite this Article

Boffetta P, Franco N, Gullino A, Pira E. . Perm J 2020;25:20.215. DOI: 10.7812/TPP/20.215

References

1. Boffetta P, Franco N, Gullino A, Pira E. Re: Dutheil et al. Prostate cancer and Asbestos: a systematic review and meta-analysis. Perm J 2020 Jul.

2. Dutheil F, Zaragoza-Civale L, Pereira B, et al Prostate Cancer and asbestos: A systematic review and meta-analysis. Perm J Feb 2020 Feb;24:19.086. DOI: https://doi.org/10.7812/TPP/19.086

3. Peng R, Fang F, Chen Z, et al Does exposure to asbestos cause prostate cancer? A systematic literature review and meta-analysis. Medicine (Baltim) 2019 Jan;98:e14108. DOI: https://doi.org/10.1097/MD.0000000000014108

4. Armstrong BK, de Klerk NH, Musk AW, Hobbs MS. Mortality in miners and millers of crocidolite in Western Australia. Br J Ind Med 1988 Jan;45(1):5-13. DOI: https://doi.org/10.1136/oem.45.1.5

5. Reid A, Franklin P, Olsen N, et al All-cause mortality and cancer incidence among adults exposed to blue asbestos during childhood. Am J Ind Med 2013 Feb;56(2):133-45. DOI: https://doi.org/10.1002/ajim.22103

Keywords: asbestos, bias, epidemiology, prostate cancer

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