Advertisement

Endocrine

, Volume 53, Issue 2, pp 471–479 | Cite as

Increased thyroid cancer incidence in a basaltic volcanic area is associated with non-anthropogenic pollution and biocontamination

  • Pasqualino MalandrinoEmail author
  • Marco Russo
  • Anna Ronchi
  • Claudio Minoia
  • Daniela Cataldo
  • Concetto Regalbuto
  • Carla Giordano
  • Marco Attard
  • Sebastiano Squatrito
  • Francesco Trimarchi
  • Riccardo Vigneri
Original Article

Abstract

The increased thyroid cancer incidence in volcanic areas suggests an environmental effect of volcanic-originated carcinogens. To address this problem, we evaluated environmental pollution and biocontamination in a volcanic area of Sicily with increased thyroid cancer incidence. Thyroid cancer epidemiology was obtained from the Sicilian Regional Registry for Thyroid Cancer. Twenty-seven trace elements were measured by quadrupole mass spectrometry in the drinking water and lichens (to characterize environmental pollution) and in the urine of residents (to identify biocontamination) in the Mt. Etna volcanic area and in adjacent control areas. Thyroid cancer incidence was 18.5 and 9.6/105 inhabitants in the volcanic and the control areas, respectively. The increase was exclusively due to the papillary histotype. Compared with control areas, in the volcanic area many trace elements were increased in both drinking water and lichens, indicating both water and atmospheric pollution. Differences were greater for water. Additionally, in the urine of the residents of the volcanic area, the average levels of many trace elements were significantly increased, with values higher two-fold or more than in residents of the control area: cadmium (×2.1), mercury (×2.6), manganese (×3.0), palladium (×9.0), thallium (×2.0), uranium (×2.0), vanadium (×8.0), and tungsten (×2.4). Urine concentrations were significantly correlated with values in water but not in lichens. Our findings reveal a complex non-anthropogenic biocontamination with many trace elements in residents of an active volcanic area where thyroid cancer incidence is increased. The possible carcinogenic effect of these chemicals on the thyroid and other tissues cannot be excluded and should be investigated.

Keywords

Thyroid cancer Volcanic area Trace elements Epidemiology Heavy metals 

Notes

Acknowledgments

This work was supported by grants from the Associazione Italiana per la Ricerca sul Cancro (AIRC, Milan, Italy) to R.V. P.M. was supported by a fellowship from the “Giuseppe Alazio” Foundation, Palermo, Italy. Drs. G. Padova and V. D’Urso (Catania), Dr. M.C. Moleti (Messina), Drs. C.A. Maniglia and P. Richiusa (Palermo) contributed to case selection and urine sample collection. Thyroid cancer incidence data were obtained from the Sicilian Regional Registry for Thyroid Cancer co-ordinated by Dr. G. Pellegriti.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. 1.
    G. Pellegriti, F. De Vathaire, C. Scollo et al., Papillary thyroid cancer incidence in the volcanic area of Sicily. J. Natl. Cancer Inst. 101, 1575–1583 (2009)CrossRefPubMedGoogle Scholar
  2. 2.
    E. Arnbjornsson, A. Arnbjornsson, A. Olafsson, Thyroid cancer incidence in relation to volcanic activity. Arch. Environ. Health 41, 36–40 (1986)CrossRefPubMedGoogle Scholar
  3. 3.
    J. Hrafnkelsson, H. Tulinius, J.G. Jonasson et al., Papillary thyroid carcinoma in Iceland: a study of the occurrence in families and the coexistence of other primary tumours. Acta Oncol. 28, 785–788 (1989)CrossRefPubMedGoogle Scholar
  4. 4.
    M.T. Goodman, C.N. Yoshizawa, L.N. Kolonel, Descriptive epidemiology of thyroid cancer in Hawaii. Cancer 61, 1272–1281 (1988)CrossRefPubMedGoogle Scholar
  5. 5.
    L.N. Kolonel, J.H. Hankin, L.R. Wilkens et al., An epidemiologic study of thyroid cancer in Hawaii. Cancer Causes Control 1, 223–234 (1990)CrossRefPubMedGoogle Scholar
  6. 6.
    L.H. Duntas, C. Doumas, The ‘rings of fire’ and thyroid cancer. Hormones (Athens) 8, 249–253 (2009)CrossRefGoogle Scholar
  7. 7.
    P. Malandrino, C. Scollo, I. Marturano et al., Descriptive epidemiology of human thyroid cancer: experience from a regional registry and the “volcanic factor”. Front Endocrinol (Lausanne) 4, 65 (2013)Google Scholar
  8. 8.
    P. Malandrino, G. Pellegriti, M. Attard et al., Papillary thyroid microcarcinomas: a comparative study of the characteristics and risk factors at presentation in two cancer registries. J. Clin. Endocrinol. Metab. 98, 1427–1434 (2013)CrossRefPubMedGoogle Scholar
  9. 9.
    A. Aiuppa, G. Dongarrà, M. Valenza, C. Federico, G. Pecoraino, Degassing of Trace Volatile Metals During the 2001 Eruption of Etna, in Volcanism and the Earth’s Atmosphere, pp. 41–54, ed. by A. Robock, C. Oppenheimer (American Geophysical Union, Washington, D.C., 2003)Google Scholar
  10. 10.
    B. Wolterbeek, Biomonitoring of trace element air pollution: principles, possibilities and perspectives. Environ. Pollut. 120, 11–21 (2002)CrossRefPubMedGoogle Scholar
  11. 11.
    S. Augusto, C. Máguas, C. Branquinho, Guidelines for biomonitoring persistent organic pollutants (POPs), using lichens and aquatic mosses—a review. Environ. Pollut. 180, 330–338 (2013)CrossRefPubMedGoogle Scholar
  12. 12.
    Valori di riferimento degli elementi metallici di interesse biologico e tossicologico-Società Italiana dei Valori di Riferimento (2005). http://www.valoridiriferimento.it/. Accessed 4 Sept 2013
  13. 13.
    A. Alimonti, B. Bocca, D. Mattei, A. Pino, Biomonitoring of the Italian population to metals: reference values 1990–2009. Rap. ISTISAN 10, 22 (2010)Google Scholar
  14. 14.
    WHO (World Health Organization) Geneva: WHO; 2011b. Guidelines for Drinking-Water Quality. Fourth editionGoogle Scholar
  15. 15.
    Y. Ito, Y.E. Nikiforov, M. Schlumberger et al., Increasing incidence of thyroid cancer: controversies explored. Nat. Rev. Endocrinol. 9, 178–184 (2013)CrossRefPubMedGoogle Scholar
  16. 16.
    L. Davies, H.G. Welch, Current thyroid cancer trends in the United States. JAMA Otolaryngol. Head Neck Surg. 140, 317–322 (2014)CrossRefPubMedGoogle Scholar
  17. 17.
    L. Leenhardt, M.O. Bernier, M.H. Boin-Pineau et al., Advances in diagnostic practices affect thyroid cancer incidence in France. Eur. J. Endocrinol. 150, 133–139 (2004)CrossRefPubMedGoogle Scholar
  18. 18.
    B.A. Kilfoy, T. Zheng, T.R. Holford et al., International patterns and trends in thyroid cancer incidence, 1973–2002. Cancer Causes Control 20, 525–531 (2009)CrossRefPubMedGoogle Scholar
  19. 19.
    R. Vigneri, P. Malandrino, P. Vigneri, The changing epidemiology of thyroid cancer: why is incidence increasing? Curr. Opin. Oncol. 27, 1–7 (2015)CrossRefPubMedGoogle Scholar
  20. 20.
    S.M. Rappaport, M.T. Smith, Epidemiology: environment and disease risks. Science 330, 460–461 (2010)CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    S.M. Rappaport, Implications of the exposome for exposure science. J. Expo. Sci. Environ. Epidemiol. 21, 5–9 (2011)CrossRefPubMedGoogle Scholar
  22. 22.
    G. Pellegriti, P. Malandrino, R. Vigneri, Re: Papillary thyroid cancer incidence in the volcanic area of Sicily. J. Natl. Cancer Inst. 102, 915–916 (2010)CrossRefGoogle Scholar
  23. 23.
    D.D. Deheyn, P. Gendreau, R.J. Baldwin et al., Evidence for enhanced bioavailability of trace elements in the marine ecosystem of Deception Island, a volcano in Antarctica. Mar. Environ. Res. 60, 1–33 (2005)CrossRefPubMedGoogle Scholar
  24. 24.
    C.E. Fiorentino, J.D. Paoloni, M.E. Sequeira et al., The presence of vanadium in groundwater of southeastern extreme the pampean region Argentina: relationship with other chemical elements. J. Contam. Hydrol. 93, 122–129 (2007)CrossRefPubMedGoogle Scholar
  25. 25.
    M. Ferrante, M. Fiore, C. Ledda et al., Monitoraggio di metalli pesanti ed oligoelementi in aria, ortofrutta e terreno nella provincia di Catania. Ig. Sanità Pubbl. 69, 47–54 (2013)PubMedGoogle Scholar
  26. 26.
    D. Varrica, E. Tamburo, G. Dongarrà et al., Trace elements in scalp hair of children chronically exposed to volcanic activity (Mt. Etna, Italy). Sci. Total Environ. 470–471, 117–126 (2014)CrossRefPubMedGoogle Scholar
  27. 27.
    A.S. Rodrigues, M.S. Arruda, P.V. Garcia, Evidence of DNA damage in humans inhabiting a volcanically active environment: a useful tool for biomonitoring. Environ. Int. 49, 51–56 (2012)CrossRefPubMedGoogle Scholar
  28. 28.
    A. Amaral, V. Rodrigues, J. Oliveira et al., Chronic exposure to volcanic environments and cancer incidence in the Azores Portugal. Sci Total Environ. 367, 123–128 (2006)CrossRefPubMedGoogle Scholar
  29. 29.
    A. Kristbjornsdottir, V. Rafnsson, Cancer incidence among population utilizing geothermal hot water: a census-based cohort study. Int. J. Cancer 133, 2944–2952 (2013)PubMedGoogle Scholar
  30. 30.
    M. Russo, P. Malandrino, W.A. Pollina et al., Several site-specific cancers are increased in the volcanic area in Sicily. Anticancer Res. 35, 3995–4001 (2015)PubMedGoogle Scholar
  31. 31.
    IARC Monographs on the Evaluation of the Carcinogenic Risk of Chemicals to Humans. Vol 100C. Cadmium and Cadmium Compounds. Lyon, France: International Agency for Research on Cancer (2012)Google Scholar
  32. 32.
    M.F. Hughes, Biomarkers of exposure: a case study with inorganic arsenic. Environ. Health Perspect. 114, 1790–1796 (2006)PubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Pasqualino Malandrino
    • 1
    Email author
  • Marco Russo
    • 1
  • Anna Ronchi
    • 2
  • Claudio Minoia
    • 2
  • Daniela Cataldo
    • 1
  • Concetto Regalbuto
    • 1
  • Carla Giordano
    • 3
  • Marco Attard
    • 4
  • Sebastiano Squatrito
    • 1
  • Francesco Trimarchi
    • 5
  • Riccardo Vigneri
    • 1
    • 6
    • 7
  1. 1.Endocrinology, Department of Clinical and Experimental Medicine, Garibaldi-Nesima Medical CenterUniversity of CataniaCataniaItaly
  2. 2.Laboratory of Experimental and Clinical Toxicology, Toxicology Unit, Pavia Poison Control Center and National Toxicology Information CenterIRCCS Maugeri FoundationPaviaItaly
  3. 3.Endocrinology, Diabetology and Metabolism, Department of Internal and Specialist BiomedicineUniversity of PalermoPalermoItaly
  4. 4.Unit of EndocrinologyOspedali Riuniti Villa Sofia, Cervello HospitalPalermoItaly
  5. 5.Endocrinology, Department of Clinical and Experimental MedicineUniversity of MessinaMessinaItaly
  6. 6.HumanitasCatania Oncoloy CenterCataniaItaly
  7. 7.Institute of Biostructures and Bioimaging, CNR (National Research Council)CataniaItaly

Personalised recommendations