Malignant mesothelioma and asbestos exposure in Europe: Evidence of spatial clustering

Submitted: 13 October 2020
Accepted: 25 February 2021
Published: 14 May 2021
Abstract Views: 2966
PDF: 911
Appendix: 140
HTML: 341
Publisher's note
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.


Exposure to asbestos causes a wide range of diseases, such as asbestosis, malignant mesothelioma (MM) and other types of cancer. Many European countries have reduced production and use of asbestos and some have banned it altogether. Based on data derived from the World Health Organisation (WHO) Cancer Mortality Database, we investigated whether some regions in Europe could have a higher relative risk of MM incidence than others. The data were compared, including the number of MM deaths per million inhabitants and aged-standardized mortality rates. Applying Moran's I and Getis-Ord Gi statistic on the agedstandardized mortality rates of MM cases assisted the spatial analysis of the occurrence of health events leading to an assessment of the heterogeneity of distribution and cluster detection of MM. We found a statistically significant positive autocorrelation for the male population and also the general population, while there was no statistically significant positive one for the female population. Hotspots of relative risk of developing MM were found in northwestern Europe. For the general population, Great Britain and the Netherlands stood out with high levels at the 99% and 95% confidence levels, respectively. For the male population, the results were similar, but with addition of risk also in Belgium and Switzerland. However, in many European countries with high asbestos use per capita, the MM incidence was found to still be low. The reasons for this are not yet clear, but part of the problem is certainly due to incomplete data in registers and databases. The latency time can be longer than 40 years and is related to the intensity and time of exposure (occupational, para-occupational and environmental). In Europe, even though peak production occurred in the 1960s and 1970s, a significant decrease in production did not occur until 25 years later, which means that the impact will continue for as late as The mid 2030s.



PlumX Metrics


Download data is not yet available.


Agudo A, Gonzalez CA, Bleda MJ, Ramirez J, Hernandez S, Lopez F, Calleja A, Panades R, Turuguet D, Escoalr A, 2000. Occupation and risks of malignant pleural mesothelioma: a case-control study in Spain. Am J Ind Med 37:159-68. DOI:<159::AID-AJIM1>3.0.CO;2-0
Alies-Patin AM, Valleron AJ, 1985. Mortality of workers in a French asbestos cement factory 1940-82. Br J Ind Med 42:219-25. DOI:
Allen LP, Baez J, Stern MEC, Takahashi K, George F, 2018. Trends and the economic effect of asbestos bans and decline in asbestos consumption and production worldwide. Int J Environ Res Public Health 16:15. DOI:
Anselin L, 1995. Local indicators of spatial association - LISA. Geogr Anal 27:93-115. DOI:
ANSES, 2016. French Agency for Food, Environmental and Occupational Health & Safety. Asbestos. Presentation, health effects, exposure and regulatory framework. Available from: Accessed: 3 January 2020.
Banaei A, Auvert B, Goldberg M, Gueguen A, Luce D, Goldberg S, 2000. Future trends in mortality of French men from mesothelioma. Occup Environ Med 57:488-94. DOI:
Barrett JC, 1994. Cellular and molecular mechanisms of asbestos carcinogenicity: implications for biopersistence. Environ Health Perspect 102:19-23. DOI:
Baur X, 2018. Asbestos-related disorders in Germany: background, politics, incidence, diagnostics and compensation. Int J Environ Res Public Health 15:143. DOI:
Bianchi C, Bianchi T, 2007. Malignant mesothelioma: global incidence and relationship with asbestos. Ind Health 45:379-87. DOI:
Bianchi C, Giarelli L, Grandi G, Brollo A, Ramani L, Zuch C, 1997. Latency periods in asbestos-related mesothelioma of the pleura. Eur J Cancer Prev 6:162-6.
Bowles O, 1955. The asbestos industry. United States Government Printing Office, Washington, pp. 48-49.
Burdorf A, Heederik D, 2011. Applying quality criteria to exposure in asbestos epidemiology increases the estimated risk. Ann Occup Hyg 55:565-8.
Carbone M, Bedrossian CW, 2006. The pathogenesis of mesothelioma. Semin Diagn Pathol 23:56-60. DOI:
Carbone M, Emri S, Dogan AU, Steele I, Tuncer M, Pass HI, Baris YI, 2007. A mesothelioma epidemic in Cappadocia: scientific developments and unexpected social outcomes. Nat Rev Cancer 7:147-54. DOI:
Corfiati M, Scarselli A, Binazzi A, Di Marzio D, Verardo M, 2015. Epidemiological patterns of asbestos exposure and spatial clusters of incident cases of malignant mesothelioma from the Italian national registry. BMC Cancer 15:286. DOI:
Donaldson K, Brown RC, Brown GM, 1993. Respirable industrial fibres: mechanisms of pathogenicity. Thorax 48:390-5. DOI:
Gardner MJ, Winter PD, Bannett B, Powell CA, 1986. Follow-up study of workers manufacturing chrysotile asbestos cement products. Br J Ind Med 43:726-32. DOI:
Getis A, Ord JK, 1992. The analysis of spatial association by use of distance statistics. Geogr Anal 24:189-206. DOI:
Gilham C, Rake C, Hodgson J, Darnton A, Burdett G, Peto Wild J, Newton M, Nicholson AG, Davidson L, Shires M, Treasure T, Peto J, 2018. TIPS Collaboration. Past and current asbestos exposure and future mesothelioma risks in Britain: the Inhaled Particles Study (TIPS). Int J Epidemiol 47:1745-56. DOI:
Harris NL, Goldman E, Gabris C, Nordling J, Minnemeyer S, Ansari S, Lippmann M, Bennett L, Raad M, Hansen M, 2017. Using spatial statistics to identify emerging hot spots of forest loss. Environ Res Lett 12:024012. DOI:
Hendry N, 1965. The geology, occurrences, and major uses of asbestos. Ann N Y Acad Sci 132:12-21. DOI:
Hilliard AK, Lovett JK, McGavin CR, 2003. The rise and fall in incidence of malignant mesothelioma from a British naval dockyard, 1979-1999. Occup Med 53:209-12. DOI:
Hindry M, 2012. Eternit in France. Available from: Accessed: 3 January 2020.
Hodgson JT, McElvenny DM, Darnton AJ, Price MJ, Peto J, 2005. The expected burden of mesothelioma mortality in Great Britain from 2002 to 2050. Br J Cancer 92:587-93. DOI:
HSE, 2019. Mesothelioma statistics for Great Britain. Available from: Accessed: 3 January 2020.
Huncharek M, 1992. Changing risk groups for malignant mesothelioma. Cancer 69:2704-11. DOI:<2704::AID-CNCR2820691113>3.0.CO;2-F
IARC, 2020. International Agency for Research on Cancer World Health Organization. Available from: Accessed: 6 January, 2020.
Jamrozik E, de Klerk N, Musk AW, 2011. Asbestos-related disease. Intern Med J 41:372-80. DOI:
Klebe S, Leigh J, Henderson DW, Nurminen M, 2020. Asbestos, smoking and lung cancer: an update. Int J Environ Res Public Health 17:258. DOI:
Krówczyńska M, Raczko E, Staniszewska N, Wilk E, 2020. Asbestos-cement roofing identification using remote sensing and convolutional neural networks (CNNs). Remote Sens 12:408. DOI:
Krówczyńska M, Wilk E, 2018. Asbestos exposure and the mesothelioma incidence in Poland. Int J Environ Res Public Health 15:1741. DOI:
Krówczyńska M, Wilk E, Zagajewski B, 2014. The electronic spatial information system-tools for the monitoring of asbestos in Poland. Misc Geogr 18:59-64. DOI:
Ledda C, Senia P, Rapisarda V, 2018. Biomarkers for early diagnosis and prognosis of malignant pleural mesothelioma: the quest goes on. Cancers 10:203. DOI:
Lee PN, 2001. Relation between exposure to asbestos and smoking jointly and the risk of lung cancer. Occup Environ Med 58:145-53. DOI:
Li H, Calder CA, Cressie N, 2007. Beyond Moran’s I: testing for spatial dependence based on the spatial autoregressive model. Geogr Anal 39:357-75. DOI:
Lin S, Lu Y, 2009. The spatial patterns of adverse health effects of ozone pollution on childhood respiratory diseases in urban Houston. Ann GIS 15:127-40. DOI:
Mackenbach JP, Martikainen P, Menvielle G, de Gelder R, 2016. The arithmetic of reducing relative and absolute inequalities in health: a theoretical analysis illustrated with European mortality data. J Epidemiol Community Health 70:730-6. DOI:
Magnani C, Dalmasso P, Biggeri A, Ivaldi C, Mirabelli D, 2001. Increased risk of malignant mesothelioma of the pleura after residential or domestic exposure to asbestos: a case control study in Casale Monferrato, Italy. Environ Health Perspect 9:915-8. DOI:
Marinaccio A, Binazzi A, Cauzillo G, Cavone D, Zotti RD, Ferrante P, Gennaro V, Gorini G, Menegozzo M, Mensi C, Merler E, Mirabelli D, Montanaro F, Musti M, Pannelli F, Romanelli A, Scarselli A, Tumino R, 2007. Italian Mesothelioma Register (ReNaM) Working Group. Analysis of latency time and its determinants in asbestos related malignant mesothelioma cases of the Italian register. Eur J Cancer 43:2722-8. DOI:
Marinaccio A, Montanaro F, Mastrantonio M, Uccelli R, Altavista P, Nesti M, Costantini AS, Gorini G, 2005. Predictions of mortality from pleural mesothelioma in Italy: a model based on asbestos consumption figures supports results from age-period-cohort models. Int J Cancer 115:142-7. DOI:
Markowitz SB, Levin SM, Miller A, Morabia A, 2013. Asbestos, asbestosis, smoking, and lung cancer. New findings from the North American insulator cohort. Am. J. Respir. Crit Care Med 188:90-6. DOI:
McDonald AD, Case BW, Churg A, Dufresne A, Gibbs GW, Sébastien P, McDonald JC, 1997. Mesothelioma in Quebec chrysotile miners and millers: epidemiology and aetiology. Ann Occup Hyg 41:707-19. DOI:
McDonald AD, McDonald JC, 1978. Mesothelioma after crocidolite exposure during gas mask manufacture. Environ Res 17:340-6. DOI:
McDonald JC, McDonald AD, 1996. The epidemiology of mesothelioma in historical context. Eur Respir J 9:1932-42. DOI:
McElvenny DM, Darnton AJ, Price MJ, Hodgson JT, 2005. Mesothelioma mortality in Great Britain from 1968 to 2001. Occup Med 55:79-87. DOI:
Moran PAP, 1950. Notes on continuous stochastic phenomena. Biometrika 37:17-23. DOI:
Mowe G, Gylseth B, Hartveit F, Skaug V, 1984. Occupational asbestos exposure, lung-fiber concentration and latency time in malignant mesothelioma. Scand J Work Environ Health 10:293-8. DOI:
Murray R, 1990. Asbestos: a chronology of its origins and health effects. Br J Ind Med 47:361-5. DOI:
Musti M, Pollice A, Cavone D, Dragonieri S, Bilancia M, 2009. The relationship between mesothelioma and an asbestos cement plant environmental risk: a spatial case-control study in the city of Bari (Italy). Int Arch Occup Environ Health 82:489-97. DOI:
Natural Earth, 2019. Natural Earth data. Available from: Accessed: 10 October 2019.
Neyens T, Lawson A, Kirby R, Nuyts V, Watjou K, Aregay M, Carroll R, Nawrot T, Faes CH, 2017. Disease mapping of zero-excessive mesothelioma data in Flanders. Ann Epidemiol 27:59-66. DOI:
NIPH, 2012. National Institute of Public Health - National Institute of Hygiene. Description of the methods and interpretation of results presented in the atlas of mortality of Poland population 2012-2014. Available from: Accessed: 6 January, 2020.
Oddone E, Bollob J, Nava CR, Bugani M, Consonni D, Marinaccio A, Magnani C, Baroneâ€Adesi F, 2020. Predictions of mortality from pleural mesothelioma in Italy after the ban of asbestos use. Int J Environ Res Public Health 17:607. DOI:
Ord JK, Getis A, 1995. Local spatial autocorrelation statistics: distributional issues and an application. Geogr Anal 27:286-306. DOI:
Peto J, Decarli A, La Vecchia C, Levi F, Negri E, 1999. The European mesothelioma epidemic. Br J Cancer 79:666-72. DOI:
Peto J, Hodgson JT, Matthews FE, Jones JR, 1995. Continuing increase in mesothelioma mortality in Britain. Lancet 345:535-9. DOI:
Pott F, Roller M, Ziem U, Reiffer FJ, Bellmann B, Rosenbruch M, Huth F, 1989. Carcinogenicity studies on natural and man-made fibres with the intraperitoneal test in rats. IARC Sci Publ 90:173-9.
Reid A, de Klerk NH, Magnani C, Ferrante D, Musk AW, Merler E, 2014. Mesothelioma risk after 40 years since first exposure to asbestos: a pooled analysis. Thorax 69:843-50. DOI:
Robinson B, Chahinian A, 2002. Mesothelioma, 1st ed. Martin Dunitz; CRC Press, London, UK. DOI:
Robinson BW, Musk AW, Lake RA, 2005. Malignant mesothelioma. Lancet 366:397-408. DOI:
Schlegel H, Kempf E, 1982. Mesotheliome nach beruflichem Asbestkontakt. Soz Präventivmed 27:220-2. DOI:
Schneider F, Sporn TA, Roggli VL, 2008. Crocidolite and mesothelioma. Ultrastruct Pathol 32:171-7. DOI:
Schonfeld SJ, McCormack V, Rutherford MJ, Schutz J, 2014. Regional variations in German mesothelioma mortality rates: 2000-2010. Cancer Causes Control 25:615-24. DOI:
Sulcova M, Krcmery V, Pleko I, Kakoova B, 2001. The Slovakian asbestos experience: use, health effects and preventive measures. Available from: Accessed: 3 January 2020.
SUVA, 2014. Annual Report 2014. Available from: Accessed: 3 January 2020.
Suzuki Y, Kohyama N, 1991. Translocation of inhaled asbestos fibres from the lung to other tissues. Am J Ind Med 19:701-4. DOI:
Tobler W, 1970. Computer movie simulating urban growth in the Detroit Region. Econ Geogr 46:234-40. DOI:
Tompa E, Kalcevich C, McLeod C, Lebeau M, Song C, McLeod K, Kim J, Demers PA, 2017. The economic burden of lung cancer and mesothelioma due to occupational and para-occupational asbestos exposure. Occup Environ Med 74:816-22. DOI:
Tsakane A, 1997. Asbestos, asbestosis and cancer: the Helsinki criteria for diagnosis and attribution. Scand J Work Environ Health 23:311-6.
Van der Borre L, Deboosere P, 2014. Asbestos in Belgium: an underestimated health risk. The evolution of mesothelioma mortality rates (1969-2009). Int J Occup Environ Health 20:134-40. DOI:
van Zandwijk N, Reid G, Frank AL, 2020. Asbestos-related cancers: the ‘Hidden Killer’ remains a global threat. Expert Rev Anticancer Ther 20:271-8. DOI:
Vangelowa K, Dimitrova S, Dimitrova I, 2015. National asbestos profile of Bulgaria. Available from: Accessed: 3 January 2020.
Virta R, 2002. Asbestos: geology, mineralogy, mining, and uses. Open-File Report 02-149. Available from: Accessed: 10 October 2015.
Virta R, 2006. Worldwide asbestos supply and consumption trends from 1900 through 2003. USGS Open-File Report 03-083. Available from: Accessed: 10 October 2019. DOI:
Wagner JC, Sleggs CA, Marchand P, 1960. Diffuse pleural mesothelioma and asbestos exposure in the North Western Cape Province. Br J Ind Med 17:260-71. DOI:
Wakefield J, 2007. Disease mapping and spatial regression with count data. Biostatistics 8:158-83. DOI:
Wang Y, Yang Y, Shi X, Mao S, Shi N, Hui X, 2016. The spatial distribution pattern of human immunodeficiency virus/acquired immune deficiency syndrome in China. Geospat Health 11:414. DOI:
WHO, 2016. International statistical classification of diseases and related health problems - 10th revision. World Health Organization Geneva, Switzerland. Available from: Accessed: 20 October 2019.
WHO, 2018. Asbestos: elimination of asbestos-related disease. World Health Organization Geneva, Switzerland. Available from: Accessed: 10 October 2019.
Wilk E, Krówczyńska M, Zagajewski B, 2019. Modelling the spatial distribution of asbestos-cement products in poland with the use of the random forest algorithm. Sustainability 11:4355. DOI:
Yang H, Testa JR, Carbone M, 2008. Mesothelioma epidemiology, carcinogenesis, and pathogenesis. Curr Treat Options Oncol 9:147-57. DOI:

How to Cite

Wilk, E., & KròwczyÅ„ska, M. (2021). Malignant mesothelioma and asbestos exposure in Europe: Evidence of spatial clustering. Geospatial Health, 16(1).

List of Cited By :

Crossref logo

Similar Articles

You may also start an advanced similarity search for this article.