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DNA damage in oral epithelial cells of individuals chronically exposed to indoor radon (222Rn) in a hydrothermal area

Abstract

Hydrothermal areas are potentially hazardous to humans as volcanic gases such as radon (222Rn) are continuously released from soil diffuse degassing. Exposure to radon is estimated to be the second leading cause of lung cancer, but little is known about radon health-associated risks in hydrothermal regions. This cross-sectional study was designed to evaluate the DNA damage in the buccal epithelial cells of individuals chronically exposed to indoor radon in a volcanic area (Furnas volcano, Azores, Portugal) with a hydrothermal system. Buccal epithelial cells were collected from 33 individuals inhabiting the hydrothermal area (Ribeira Quente village) and from 49 individuals inhabiting a non-hydrothermal area (Ponta Delgada city). Indoor radon was measured with Ramon 2.2 detectors. Chromosome damage was measured by micronucleus cytome assay, and RAPD-PCR was used as a complementary tool to evaluate DNA damage, using three 10-mer primers (D11, F1 and F12). Indoor radon concentration correlated positively with the frequency of micronucleated cells (r s = 0.325, p = 0.003). Exposure to radon is a risk factor for the occurrence micronucleated cells in the inhabitants of the hydrothermal area (RR = 1.71; 95% CI, 1.2–2.4; p = 0.003). One RAPD-PCR primer (F12) produced differences in the banding pattern, a fact that can indicate its potential for detecting radon-induced specific genomic alterations. The observed association between chronic exposure to indoor radon and the occurrence of chromosome damage in human oral epithelial cells evidences the usefulness of biological surveillance to assess mutations involved in pre-carcinogenesis in hydrothermal areas, reinforcing the need for further studies with human populations living in these areas.

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References

  1. Agarwal, P., Vinuth, D. P., Harana, S., Thippanna, C. K., Naresh, N., & Moger, G. (2015). Genotoxic and cytotoxic effects of X-ray on buccal epithelial cells following panoramic radiography: A pediatric study. Journal of Cytology, 32(2), 102–106.

    Article  Google Scholar 

  2. Ahmad, K. K., Mustafa, S. K., & Karim, J. K. (2015). Prevalence of micronucleated cell in buccal smears among smokers and non-smokers. International Journal of Advanced Research, 3(4), 972–977.

    CAS  Google Scholar 

  3. Al-Zoughool, M., & Krewski, D. (2009). Health effects of radon: A review of the literature. International Journal of Radiation Biology, 85, 57–69.

    CAS  Article  Google Scholar 

  4. Amaral, A., Rodrigues, V., Oliveira, J., Pinto, C., Carneiro, V., Sanbento, R., et al. (2006). Chronic exposure to volcanic environments and cancer incidence in the Azores, Portugal. Science of the Total Environment, 367, 123–128.

    CAS  Article  Google Scholar 

  5. Atienzar, F. A., & Jha, A. N. (2006). The random amplified polymorphic DNA (RAPD) assay and related techniques applied to genotoxicity and carcinogenesis studies: A critical review. Mutation Research, 613(2–3), 76–102.

    CAS  Article  Google Scholar 

  6. Auxier, J. A. (1976). Respiratory exposure in buildings due to radon progeny. Health Physics, 31, 119–125.

    CAS  Article  Google Scholar 

  7. Axelson, O., Edling, C., & Kling, H. (1979). Lung cancer and residency: A case referent study on the possible impact of exposure to radon and its daughters in dwellings. Scandinavian Journal of Work, Environment & Health, 5, 10–15.

    CAS  Article  Google Scholar 

  8. Baxter, P. J., Baubron, J. C., & Coutinho, R. (1999). Health hazards and disaster potential of ground gas emissions at Furnas volcano, Sao Miguel, Azores. Journal of Volcanology and Geothermal Research, 92, 95–106.

    CAS  Article  Google Scholar 

  9. Bloching, M., Hofmann, A., Lautenschalager, C. H., Berghaus, A., & Grummt, T. (2000). Exfoliative cytology of normal buccal mucosa to predict the relative risk of cancer in the upper aerodigestive tract using the MN-assay. Oral Oncology, 36, 550–555.

    CAS  Article  Google Scholar 

  10. Bolognesi, C., Knasmueller, S., Nersesyan, P., Thomas, P., & Fenech, M. (2013). The HUMNxl scoring criteria for different cell types and nuclear anomalies in the buccal micronucleus cytome assay: An update and expanded photogallery. Mutation Research-Reviews in Mutation Research, 753(2), 100–113.

    CAS  Article  Google Scholar 

  11. Bolognesi, C., Roggieri, P., Ropolo, P., Thomas, P., Hor, M., & Fenech, M., et al. (2015). Buccal micronucleus cytome assay: Results of an intra- and inter-laboratory scoring comparison. Mutagenesis, 30(4), 545–555.

    CAS  Article  Google Scholar 

  12. Bonassi, S., Coskun, E., Ceppi, M., Lando, C., Bolognesi, C., Burgaz, S., et al. (2011). The HUman MicroNucleus project on eXfoLiated buccal cells (HUMNXL): The role of life-style, host factors, occupational exposures, health status, and assay protocol. Mutation Research, 728(3), 88–97.

    CAS  Article  Google Scholar 

  13. Bruschweiler, E. D., Hopf, N. B., Wild, P., Huynh, C. K., Fenech, M., Thomas, P., et al. (2014). Workers exposed to wood dust have an increased micronucleus frequency in nasal and buccal cells: Results from a pilot study. Mutagenesis, 29(3), 201–207.

    CAS  Article  Google Scholar 

  14. Bukvic, N., Gentile, M., Susca, F., Fanelli, M., Serio, G., Buonadonna, L., et al. (2001). Sex chromosome loss, micronuclei, sister chromatid exchange and aging: A study including 16 centenarians. Mutation Research, 498, 159–167.

    CAS  Article  Google Scholar 

  15. Burton, M. R., Sawyer, G. M., & Granieri, D. (2013). Deep carbon emissions from volcanoes. Reviews in Mineralogy and Geochemistry, 75(1), 323–354.

    CAS  Article  Google Scholar 

  16. Camarinho, R., Garcia, P. V., & Rodrigues, A. S. (2013). Chronic exposure to volcanogenic air pollution as cause of lung injury. Environmental Pollution, 181C, 24–30.

    Article  Google Scholar 

  17. Çelik, A., Yildirim, S., Ekinci, S. Y., & Taşdelen, B. (2013). Bio-monitoring for the genotoxic assessment in road construction workers as determined by the buccal micronucleus cytome assay. Ecotoxicology and Environment Safety, 92, 265–270.

    Article  Google Scholar 

  18. Committee on Health Risks of Exposure to Radon, National Research Council. (1999). Health effects of exposure to radon. Washington, DC: The National Academies Press.

    Google Scholar 

  19. Darby, S., Hill, D., Auvinen, A., Barros-Dios, J. M., Baysson, H., Bochicchio, F., et al. (2005). Radon in homes and risk of lung cancer: Collaborative analysis of individual data from 13 European case-control studies. British Medical Journal, 330, 223–226.

    CAS  Article  Google Scholar 

  20. De Wolf, H., Blust, R., & Backeljau, T. (2004). The use of RAPD in ecotoxicology. Mutation Research, 566(3), 249–262.

    Article  Google Scholar 

  21. Decreto Legislativo Regional No. 16/2009/A de 13 de Outubro—Diário da República No. 198 1ª série.

  22. Dionis, S. M., Melián, G., Rodríguez, F., Hernández, P. A., Padrón, E., Pérez, N. M., et al. (2015). Diffuse volcanic gas emission and thermal energy release from the summit crater of Pico do Fogo, Cape Verde. Bulletin of Volcanology, 77, 10.

    Article  Google Scholar 

  23. Durand, M., & Scott, B. J. (2005). Geothermal ground gas emissions and indoor air pollution in Rotorua, New Zealand. Science of the Total Environment, 345, 69–80.

    CAS  Article  Google Scholar 

  24. Fenech, M., Holland, N., Zeiger, E., Chang, W. P., Burgaz, S., Thomas, P., et al. (2011). The HUMN and HUMNxL international collaboration projects on human micronucleus assays in lymphocytes and buccal cells—past, present and future. Mutagenesis, 26(1), 239–245.

    CAS  Article  Google Scholar 

  25. Ferreira, T., Gaspar, J. L., Viveiros, F., Marcos, M., Faria, C., & Sousa, F. (2005). Monitoring of fumarole discharge and CO2 soil degassing in the Azores: Contribution to volcanic surveillance and public health risk assessment. Annals of Geophysics, 48, 4–5.

    Google Scholar 

  26. Ferreira, T., & Oskarsson, N. (1999). Chemical and isotopic composition of fumarole discharge of Furnas caldera. Journal of Volcanology and Geothermal Research, 92, 169–179.

    CAS  Article  Google Scholar 

  27. Garcia, P. V., Linhares, D., Amaral, A. F. S., & Rodrigues, A. S. (2012). Exposure of thermoelectric power-plant workers to volatile organic compounds from fuel oil: Genotoxic and cytotoxic effects in buccal epithelial cells. Mutation Research, 747, 197–201.

    CAS  Article  Google Scholar 

  28. Gonsebatt, M. E., Vega, L., Salazar, A. M., Montero, R., Guzmán, P., Blas, J., et al. (1997). Cytogenic effects in human exposure to arsenic. Mutation Research, 386, 219–228.

    CAS  Article  Google Scholar 

  29. Grattan, J. P., Durand, M., & Taylor, S. (2003). Illness and elevated human mortality coincident with volcanic eruptions. In C. Oppenheimer, J. Pyle, & J. Barclay (Eds.), Volcanic degassing (Vol. 213, pp. 401–414). London: Special Publication-Geological Society.

    Google Scholar 

  30. GT-Analytic Keg. (2003). Ramon 2.2 radon monitor manual. GT-Analytic KEG, Austria, 5p.

  31. Guo, X., Heflich, R. H., Dial, S. L., Ritcher, P. A., Moore, M. M., & Mei, N. (2016). Quantitative analysis of the relative mutagenicity of five chemical constituents of tobacco smoke in the mouse lymphoma assay. Mutagenesis, 31(3), 287–296.

    CAS  Article  Google Scholar 

  32. Hallare, A. V., Gervasio, M. K. R., Gervasio, P. L. G., & Accio-Calro, P. J. B. (2009). Monitoring genotoxicity among gasoline station attendants and traffic enforcers in the City of Manila using the micronucleus assay with exfoliated epithelial cells. Environmental and Monitoring Assessment, 156, 331–341.

    CAS  Article  Google Scholar 

  33. Hipólito, A., Madeira, J., Carmo, R., & Gaspar, J. L. (2013). Neotectonics of Graciosa island (Azores): A contribution to seismic hazard assessment of a volcanic area in a complex geodynamic setting. Annals of Geophysics, Special volume: “Earthquake Geology: Science, Society and Critical Facilities”, 56, 6.

    Google Scholar 

  34. Ishikawa, H., Tian, Y., & Yamauchi, T. (2003). Influence of gender, age and lifestyle factors on micronuclei frequency in healthy Japanese populations. Journal of Occupational Health, 45(3), 179–181.

    Article  Google Scholar 

  35. Jin, X., Chen, Q., Tang, S. S., Zou, J. J., Chen, K. P., Zang, T., et al. (2009). Investigation of qinocetone-induced genotoxicity in HepG2 cells using comet assay, cytokinesis-block micronucleus test and RAPD analysis. Toxicology in Vitro, 23, 1209–1214.

    CAS  Article  Google Scholar 

  36. Kristbjornsdottir, A., & Rafnsson, V. (2015). Cancer mortality and other causes of death in users of geothermal hot water. Acta Oncologica, 2015(54), 115–123.

    Article  Google Scholar 

  37. Kumar, N. S., & Gurusubramanian, G. (2011). Random amplified polymorphic DNA (RAPD) markers and its applications. Science Vision, 11(3), 116–124.

    Google Scholar 

  38. Linhares, D., Garcia, P. V., Viveiros, F., Ferreira, T., Rodrigues, A. (2015). Air pollution by hydrothermal volcanism and human pulmonary function. Biomed Research International. doi:10.1155/2015/326794.

    Google Scholar 

  39. Lourenço, N., Luís, J., & Miranda, J. M. (1997). Azores triple junction bathymetry. Map edited by Science Faculty, Lisbon University and Algarve University, 1 Sheet.

  40. Mahimkar, M. B., Saman, T. A., Kannan, S., & Patilet, T. (2010). Influence of genetic polymorphisms on frequency of micronucleated buccal epithelial cells in leukoplakia patients. Oral Oncology, 46, 761–766.

    CAS  Article  Google Scholar 

  41. Nersesyan, A., Muradyan, R., Kundi, M., & Knasmueller, S. (2011). Impact of smoking on the frequencies of micronuclei and other nuclear abnormalities in exfoliated oral cells: A comparative study with different cigarette types. Mutagenesis, 26, 295–301.

    CAS  Article  Google Scholar 

  42. Robertson, A., Allen, J., Laney, R., & Curnow, A. (2013). The cellular and molecular carcinogenic effects of radon exposure: A review. International Journal of Molecular Sciences, 14, 14024–14063.

    Article  Google Scholar 

  43. Rodrigues, A., Arruda, M., & Garcia, P. (2012). Evidence of DNA damage in humans inhabiting a volcanically active environment: A useful tool for biomonitoring. Environment International, 49, 51–56.

    CAS  Article  Google Scholar 

  44. Russo, M., Malandrino, P., Addario, W. P., Dardanoni, G., Vigneri, P., Pellegriti, G., et al. (2015). Several site-specific cancers are increased in the volcanic area in Sicily. Anticancer Research, 35(7), 3995–4001.

    Google Scholar 

  45. Schmidt, A. (2015). Volcanic gas and aerosol hazards from a future Laki-type eruption in Iceland. In J. F. S. Papale (Ed.), Volcanic Hazards, Risks and Disasters (pp. 377–397). Boston: Elsevier.

    Chapter  Google Scholar 

  46. Sethi, T. K., El-Ghamry, M. N., & Kloecker, G. H. (2012). Radon and lung cancer. Clinical Advances in Hematology & Oncology, 10(3), 157–164.

    Google Scholar 

  47. Silva, C. (2013). Estudo da desgaseificação difusa de 222Rn: Implicações e termos de monitorização sismovulcânica, recursos geotérmicos e saúde pública. Departamento de Geociências. Universidade dos Açores.

  48. Silva, C., Ferreira, T., Viveiros, F., & Allard, P. (2014). Monitorização dos teores de radão (222Rn) no ar interior de edifícios das freguesias das Furnas e Ribeira Quente (Vulcão das Furnas, Açores): avaliação do risco para a saúde pública. Comunicações Geológicas, 101, Especial II, pp. 927–931. ISNN: 0873-948X; e-ISSN: 1647-581X.

  49. Silva, C., Ferreira, T., Viveiros, F., & Allard, P. (2015a). Soil radon (222Rn) monitoring at Furnas Volcano (São Miguel, Azores): Applications and challenges. The European Physical Journal-Special Topics, 224, 659–686.

    CAS  Article  Google Scholar 

  50. Silva, C., Viveiros, F., Ferreira, T., Gaspar, J. L., & Allard, P. (2015b). Diffuse soil emanations of radon and hazard implications at Furnas Volcano, São Miguel Island (Azores). In J. L. Gaspar, J. E. Guest, A. M. Duncan, F. J. A. S. Barriga, & D. K. Chester (Eds.), Volcanic geology of S. Miguel Island (Azores archipelago) (Vol. 44, pp. 197–211). London: Geological Society, Memoirs.

    Google Scholar 

  51. Stich, H. F., San, R. H. C., & Rosin, M. P. (1983). Adaptation of the DNA-repair and micronucleus tests to human cell suspensions and exfoliated cells. Annals of the New York Academy of Sciences, 407, 93–105.

    CAS  Article  Google Scholar 

  52. Thomas, P., Holland, N., Bolognesi, C., Volders, M. K., Bonassi, S., Zeiger, E., et al. (2009). Buccal micronucleus cytome assay. Nature Protocols, 4, 825–837.

    CAS  Article  Google Scholar 

  53. Tolbert, P. E., Shy, C. M., & Allen, J. W. (1991). Micronucleus and other nuclear anomalies in buccal smears: A field test in snuff users. American Journal of Epidemiology, 134, 840–850.

    CAS  Article  Google Scholar 

  54. Tolbert, P. E., Shy, C. M., & Allen, J. W. (1992). Micronucleus and other nuclear anomalies in buccal smears: Methods development. Mutation Research, 271, 69–77.

    CAS  Article  Google Scholar 

  55. Turner, M. C., Krewski, D., Chen, Y., Arden Pope, C., III, Susan Gapstur, S., & Thu, M. J. (2011). Radon and lung cancer in the American Cancer Society Cohort. Cancer Epidemiology, Biomarkers and Prevention, 20, 438–448.

    CAS  Article  Google Scholar 

  56. United Nations Scientific Committee on the Effects of Atomic Radiation (UNSCEAR). (2000). Report of the United Nations Scientific Committee on the effects of atomic radiation to the general assembly. New York, NY: United Nations.

    Google Scholar 

  57. United Nations Scientific Committee on the Effects of Atomic Radiation (UNSCEAR). (2012). Biological mechanisms of radiation actions at low doses. A white paper to guide the scientific committee’s future programme of work. New York, NY: United Nations.

    Google Scholar 

  58. Viveiros, F. (2010). Soil C O2 flux variation at Furnas Volcano (S. Miguel Island, Azores). Tese de doutoramento no ramo de Geologia, especialidade de Vulcanologia, Universidade dos Açores.

  59. Viveiros, F., Cardellini, C., Ferreira, T., & Silva, C. (2012). Contribution of CO2 emitted to the atmosphere by diffuse degassing from volcanoes: The Furnas Volcano case study. International Journal of Global Warming, 4(3–4), 287–304.

    Article  Google Scholar 

  60. Viveiros, F., Cardelllini, C., Ferreira, T., Caliro, S., Chiodini, G., & Silva, C. (2010). Soil CO2 emissions at Furnas Volcano, São Miguel Island, Azores archipelago: Volcano monitoring perspectives, geomorphologic studies, and land use planning application. Journal of Geophysical Research, 115(B12208), 1–17.

    Google Scholar 

  61. Viveiros, F., Gaspar, J. L., Ferreira, T., Silva, C., Marcos, M., & Hipólito, A. (2015). Mapping of soil CO2 diffuse degassing at São Miguel Island and its public health implications. Geological Society, London, Memoirs, 44(1), 185–195.

    Article  Google Scholar 

  62. Weinstein, P., Horwell, C. J., & Cook, A. (2013). Volcanic emissions and health. In O. Selinus et al. (Eds.), Essentials of medical geology (pp. 217–238). Springer: Netherlands.

  63. World Health Organization (WHO). (2009). In H. Zeeb & F. Shannoun (Eds.), WHO handbook on indoor radon, a public health perspective (3rd ed., pp. 94). World Health Organization.

  64. World Health Organization (WHO). (2010). WHO guidelines for indoor air quality: Selected pollutants. Geneva: World Health Organization (WHO).

    Google Scholar 

  65. Yu, K. N., Lau, B. M. F., & Nikezic, D. (2006). Assessment of environmental radon hazard using human respiratory tract models. Journal of Hazardous Materials, 132, 98–110.

    CAS  Article  Google Scholar 

  66. Zölzer, F., Havránková, R., Skalická, Z. F., Rössnerová, A., & Šrám, R. J. (2015). Analysis of genetic damage in lymphocytes of former uranium processing workers. Cytogenetic and Genome Research, 147, 17–23.

    Article  Google Scholar 

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Acknowledgements

The authors thank Fátima Viveiros and Paulo Melo for their support in field and laboratory work. Diana Linhares and Nadya Kazachkova were supported, respectively, by Ph.D. and postdoc fellowships from the Fundo Regional da Ciência (Regional Government of the Azores) (PROEMPREGO Programme) (M3.1.2/F/019/2011 and M3.1.7/F/002/2008). The authors also thank the financial support of BioAir-Biomonitoring air pollution: development of an integrated system (M2.1.2/F/00872011) from Fundo Regional da Ciência (Regional Government of the Azores) (PROEMPREGO Programme).

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Correspondence to Diana Paula Silva Linhares.

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Linhares, D.P.S., Garcia, P.V., Silva, C. et al. DNA damage in oral epithelial cells of individuals chronically exposed to indoor radon (222Rn) in a hydrothermal area. Environ Geochem Health 40, 1713–1724 (2018). https://doi.org/10.1007/s10653-016-9893-2

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Keywords

  • Genotoxicity
  • Micronuclei
  • RAPD-PCR
  • Biomonitoring