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How do etiological factors can explain the different clinical features of patients with differentiated thyroid cancer and their histopathological findings?

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Abstract

The aim was to retrospectively analyse the clinical–histopathological characteristics of patients with newly diagnosis of differentiated thyroid cancer (DTC) referred to two Italian centres, one in Northern and the other in Southern Italy, between 2000 and 2013. 1081 patients were included and subdivided into two groups: group A (474 patients from Novara) and group B (607 patients from Naples). The group A came from the industrial area of Novara, while the Group B came from the areas around Vesuvius and Campi Flegrei. The two groups were comparable for iodine levels, body mass index, diagnostic timing and clinical procedures. For all patients, demographic and clinical data were collected. No difference was found in gender, whereas the age at diagnosis was later in the group A (group A 53.1 ± 15.16 years, group B 41.9 ± 14.25 years, p < 0.001). In both groups, the most frequent histotype was papillary thyroid cancer (PTC) with prevalence of follicular variant in group A (p < 0.0001) and classical variant in group B (p < 0.0001). Aggressive histological features were mainly seen in group A (bilaterality p < 0.0001, multifocality p < 0.0001 and thyroid capsular invasion p < 0.0001). Microcarcinomas were more frequent in group A (p < 0.0001) but mostly characterized by bilaterality (p < 0.001) and multifocality (p < 0.04). In both groups, tumour-associated thyroiditis showed a significant increase over the years (group A p < 0.05, group B p < 0.04). Environmental factors could justify the differences found in our study. These preliminary data should stimulate the need for an Italian Cancer Registry of DTC in order to allow an epidemiological characterization, allowing the identification of specific etiological factors and an improvement in the management of the disease.

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References

  1. N. Howlader, A.M. Noone , M. Krapcho, J. Garshell, N. Neyman, S.F. Altekruse, C.L. Kosary, M Yu, J. Ruhl, Z. Tatalovich, H. Cho, A. Mariotto, D.R. Lewis, H.S. Chen, E.J. Feuer, K.A. Cronin (eds). SEER Cancer Statistics Review, 1975-2011, National Cancer Institute. Bethesda. http://seer.cancer.gov/csr/1975_2011/, based on November 2013 SEER data submission, posted to the SEER web site, April 2014

  2. L. Davies, H.G. Welch, Current thyroid cancer trends in the United States. JAMA Otolaryngol.–Head Neck Surg. 140(4), 317–322 (2014)

    Article  PubMed  Google Scholar 

  3. W.D. Kent, S.F. Hall, P.A. Isotalo, R.L. Houlden, R.L. George, P.A. Groome, Increased incidence of differentiated thyroid carcinoma and detection of subclinical disease. CMAJ: Canadian Medical Association journal = journal de l’Association medicale canadienne 177(11), 1357–1361 (2007)

    Article  PubMed  Google Scholar 

  4. E.P. Simard, E.M. Ward, R. Siegel, A. Jemal, Cancers with increasing incidence trends in the United States: 1999 through 2008. CA Cancer J. Clin. 62(2), 118–128 (2012)

    Article  PubMed  Google Scholar 

  5. L. Enewold, K. Zhu, E. Ron, A.J. Marrogi, A. Stojadinovic, G.E. Peoples, S.S. Devesa, Rising thyroid cancer incidence in the United States by demographic and tumor characteristics, 1980-2005. Cancer Epidemiol. Biomark. Prev 18(3), 784–791 (2009)

    Article  Google Scholar 

  6. B. Aschebrook-Kilfoy, M.H. Ward, M.M. Sabra, S.S. Devesa, Thyroid cancer incidence patterns in the United States by histologic type, 1992-2006. Thyroid 21(2), 125–134 (2011)

    Article  PubMed  PubMed Central  Google Scholar 

  7. M. Colonna, A.V. Guizard, C. Schvartz, M. Velten, N. Raverdy, F. Molinie, P. Delafosse, B. Franc, P. Grosclaude, A time trend analysis of papillary and follicular cancers as a function of tumour size: a study of data from six cancer registries in France (1983-2000). Eur. J. Cancer 43(5), 891–900 (2007)

    Article  CAS  PubMed  Google Scholar 

  8. R.M. Reynolds, J. Weir, D.L. Stockton, D.H. Brewster, T.C. Sandeep, M.W. Strachan, Changing trends in incidence and mortality of thyroid cancer in Scotland. Clin. Endocrinol. 62(2), 156–162 (2005)

    Article  Google Scholar 

  9. R.T. Netea-Maier, K.K. Aben, M.K. Casparie, M. den Heijer, J.M. Grefte, P. Slootweg, A. Hermus, Trends in incidence and mortality of thyroid carcinoma in The Netherlands between 1989 and 2003: correlation with thyroid fine-needle aspiration cytology and thyroid surgery. Int. J. Cancer 123(7), 1681–1684 (2008)

    Article  CAS  PubMed  Google Scholar 

  10. M. Lise, S. Franceschi, C. Buzzoni, P. Zambon, F. Falcini, E. Crocetti, D. Serraino, F. Iachetta, R. Zanetti, M. Vercelli, S. Ferretti, F. La Rosa, A. Donato, V. De Lisi, L. Mangone, S. Busco, G. Tagliabue, M. Budroni, L. Bisanti, M. Fusco, R.M. Limina, R. Tumino, S. Piffer, A. Madeddu, F. Bellù, A. Giacomin, G. Candela, M.L. Anulli, Dal Maso, L.: AIRTUM Working Group. Changes in the incidence of thyroid cancer between 1991 and 2005 in Italy: a geographical analysis. Thyroid 22(1), 27–34 (2012)

    Article  PubMed  Google Scholar 

  11. R. Elisei, E. Molinaro, L. Agate, V. Bottici, L. Masserini, C. Ceccarelli, F. Lippi, L. Grasso, F. Basolo, G. Bevilacqua, P. Miccoli, G. Di Coscio, P. Vitti, F. Pacini, A. Pinchera, Are the clinical and pathological features of differentiated thyroid carcinoma really changed over the last 35 years? Study on 4187 patients from a single Italian institution to answer this question. J. Clin. Endocrinol. Metab. 95(4), 1516–1527 (2010)

    Article  CAS  PubMed  Google Scholar 

  12. Associazione Italiana Registro Tumori (AIRTUM): I numeri del Cancro 2013. http://www.registri-tumori.it/PDF/AIOM2013/I_numeri_del_cancro_2013.pdf Accessed 20 April 2013

  13. J. Ferlay, F. Bray, P. Pisani, D.M. Parkin, GLOBOCAN 2002 v2.0. in cancer incidence, mortality and prevalence worldwide. Lyon: IARC (2004)

  14. J. Ferlay, H.R. Shin, F. Bray, D. Forman, C. Mathers, D.M. Parkin, GLOBOCAN 2008 v1.2. in cancer incidence, mortality and prevalence worldwide. Lyon: IARC (2010)

  15. T.J. Lee, S. Kim, H.J. Cho, J.H. Lee, The incidence of thyroid cancer is affected by the characteristics of a healthcare system. J. Korean Med. Sci. 27(12), 1491–1498 (2012)

    Article  PubMed  PubMed Central  Google Scholar 

  16. S. Grodski, T. Brown, S. Sidhu, A. Gill, B. Robinson, D. Learoyd, M. Sywak, T. Reeve, L. Delbridge, Increasing incidence of thyroid cancer is due to increased pathologic detection. Surgery 144(6):1038–1043; discussion 1043 (2008)

  17. G. Pellegriti, F. Frasca, C. Regalbuto, S. Squatrito, R. Vigneri, Worldwide increasing incidence of thyroid cancer: update on epidemiology and risk factors. J Cancer Epidemiol. 2013, 965212 (2013)

    Article  PubMed  PubMed Central  Google Scholar 

  18. L.G. Morris, D. Myssiorek, Improved detection does not fully explain the rising incidence of well-differentiated thyroid cancer: a population-based analysis. Am. J. Surg. 200(4), 454–461 (2010)

    Article  PubMed  PubMed Central  Google Scholar 

  19. N. Li, X.L. Du, L.R. Reitzel, L. Xu, E.M. Sturgis, Impact of enhanced detection on the increase in thyroid cancer incidence in the United States: review of incidence trends by socioeconomic status within the surveillance, epidemiology, and end results registry, 1980-2008. Thyroid 23(1), 103–110 (2013)

    Article  PubMed  PubMed Central  Google Scholar 

  20. P. Malandrino, C. Scollo, I. Marturano, M. Russo, M. Tavarelli, M. Attard, P. Richiusa, M.A. Violi, G. Dardanoni, R. Vigneri, G. Pellegriti, Descriptive epidemiology of human thyroid cancer: experience from a regional registry and the “volcanic factor”. Front Endocrinol. 4, 65 (2013)

    Article  Google Scholar 

  21. G. Pellegriti, F. De Vathaire, C. Scollo, M. Attard, C. Giordano, S. Arena, G. Dardanoni, F. Frasca, P. Malandrino, F. Vermiglio, D.M. Previtera, G. D’Azzò, F. Trimarchi, R. Vigneri, Papillary thyroid cancer incidence in the volcanic area of Sicily. J. Natl Cancer Inst. 101(22), 1575–1583 (2009)

    Article  CAS  PubMed  Google Scholar 

  22. B. Biondi, D. Arpaia, P. Montuori, G. Ciancia, S. Ippolito, G. Pettinato, M. Triassi, Under the shadow of vesuvius: a risk for thyroid cancer? Thyroid 22(12), 1296–1297 (2012)

    Article  PubMed  Google Scholar 

  23. M.A. Marcello, P. Malandrino, J.F. Almeida, M.B. Martins, L.L. Cunha, N.E. Bufalo, G. Pellegriti, L.S. Ward, The influence of the environment on the development of thyroid tumors: a new appraisal. Endocr. Relat. Cancer 21(5), T235–T254 (2014)

    Article  CAS  PubMed  Google Scholar 

  24. Dati ARPA (Agenzia Regionale per la Protezione dell’Ambiente) Piemonte. www.arpa.piemonte.it/ Accessed 15 April 2014

  25. Dati ARPA (Agenzia Regionale per la Protezione dell’Ambiente) Campania. www.arpacampania.it/ Accessed 15 April 2014

  26. Istituto Superiore di Sanità. Attività di monitoraggio del programma nazionale per la prevenzione dei disordini da carenza iodica. A cura di Antonella Olivieri e Paolo Vitti. 2014, iii, 113 p. Rapporti ISTISAN 14/6

  27. Thyroid. In: S.B. Edge, D.R. Byrd, C.C. Compton et al., eds.: AJCC Cancer Staging Manual, 7th edn. (Springer, New York, 2010), pp. 87–96; NCCN Clinical Practice Guidelines in Oncology: Thyroid Carcinoma. V.2.2013. http://www.nccn.org/professionals/physician_gls/pdf/thyroid.pdf. Accessed 5 Sept 2013

  28. V.A. LiVolsi, J. Albores-Saavedra, S.L. Asa, et al., Papillary carcinoma, in World Health Organization Classification of Tumours: Pathology and Genetics, Tumours of the Endocrine Organs, vol 8, ed. by R.A. DeLellis, R.V. Lloyd, P.U. Heitz, C. Eng (IARC Press International Agency for Research on Cancer, Lyon, 2004), pp. 57 e 66

  29. F. Liotti, C. Visciano, R.M. Melillo, Inflammation in thyroid oncogenesis. Am. J. Cancer Res. 2(3), 286–297 (2012)

    PubMed  PubMed Central  Google Scholar 

  30. J.A. Sipos, E.L. Mazzaferri, Thyroid cancer epidemiology and prognostic variables. Clin. Oncol. (R. Coll. Radiol.) 22, 395–404 (2010)

    Article  CAS  Google Scholar 

  31. X. Shi, R. Liu, F. Basolo, R. Giannini, X. Shen, D. Teng, H. Guan, Z. Shan, W. Teng, T.J. Musholt, K. Al-Kuraya, L. Fugazzola, C. Colombo, E. Kebebew, B. Jarzab, A. Czarniecka, B. Bendlova, V. Sykorova, M. Sobrinho-Simões, P. Soares, Y.K. Shong, T.Y. Kim, S. Cheng, S.L. Asa, D. Viola, R. Elisei, L. Yip, C. Mian, F. Vianello, Y. Wang, S. Zhao, G. Oler, J.M. Cerutti, E. Puxeddu, S. Qu, Q. Wei, H. Xu, C.J. O’Neill, M.S. Sywak, R. Clifton-Bligh, A.K. Lam, G. Riesco-Eizaguirre, P. Santisteban, H. Yu, G. Tallini, E.H. Holt, V. Vasko, M. Xing, Differential clinicopathological risk and prognosis of major papillary thyroid cancer variants. J. Clin. Endocrinol. Metab. 101(1), 264–274 (2016)

    Article  CAS  PubMed  Google Scholar 

  32. L.H. Duntas, C. Doumas, The “Ring of fire” and thyroid cancer. Hormones 8(4), 249–253 (2009)

    Article  PubMed  Google Scholar 

  33. E. Arnbjornsson, A. Arnbjornsson, A. Olafsson, Thyroid cancer incidence in relation to volcanic activity. Arch. Environ. Health 41(1), 36–40 (1986)

    Article  CAS  PubMed  Google Scholar 

  34. L.N. Kolonel, J.H. Hankin, L.R. Wilkens, F.H. Fukunaga, M.W. Hinds, An epidemiologic study of thyroid cancer in Hawaii. Cancer Causes Control 1(3), 223–234 (1990)

    Article  CAS  PubMed  Google Scholar 

  35. M.P. Curado, B. Edwards, H.R. Shin, J. Ferlay, M. Heanue, P. Boyle, Cancer incidence in five continents, vol IX (IARC; IARC Scientific Publications No 160, Lyon, 2007)

  36. T. Truong, Y. Rougier, D. Dubourdieu, C. Guihenneuc-Jouyaux, L. Orsi, D. Hemon, P. Guénel, Time trends and geographic variations for thyroid cancer in New Caledonia, a very high incidence area (1985-1999). Eur. J. Cancer Prev. 16(1), 62–70 (2007)

    Article  PubMed  Google Scholar 

  37. L. Patrick, Thyroid disruption: mechanisms and clinical implications in human health. Altern. Med. Rev. 14, 326–346 (2009)

    PubMed  Google Scholar 

  38. P. Malandrino, G. Pellegriti, M. Attard, M.A. Violi, C. Giordano, L. Sciacca, C. Regalbuto, S. Squatrito, R. Vigneri, Papillary thyroid microcarcinomas: a comparative study of the characteristics and risk factors at presentation in two cancer registries. J. Clin. Endocrinol. Metab. 98(4), 1427–1434 (2013)

    Article  CAS  PubMed  Google Scholar 

  39. M.M. Fuzik, A.Y. Prysyazhnyuk, Y. Shibata, A.Y. Romanenko, Z.P. Fedorenko, N.A. Gudzenko, L.O. Gulak, N.K. Trotsyuk, Y.L. Goroh, O.M. Khukhrianska, O.V. Sumkina, V.A. Saenko, S. Yamashita, Age and gender patterns of thyroid cancer incidence in Ukraine depending on thyroid radiation doses from radioactive iodine exposure after the Chornobyl NPP accident. Probl. Radiac. Med. Radiobiol. 18, 144–155 (2013)

    Google Scholar 

  40. A.Y. Prysyazhnyuk, D.A. Bazyka, A.Y. Romanenko, N.A. Gudzenko, M.M. Fuzik, N.K. Trotsyuk, Z.P. Fedorenko, L.O. Gulak, K.M. Slipenyuk, N.G. Babkina, O.M. Khukhrianska, Y.L. Goroh, Z.M. Berestyana, Quarter of century since the Chernobyl accident: cancer risks in affected groups of population. Probl. Radiac. Med. Radiobiol. 19, 147–169 (2014)

    PubMed  Google Scholar 

  41. B. Plante, Chernobyl, 22 years later. CBS News, 2008. http://www.cbsnews.com/htdocs/nuclear_disasters/images/map_europe.gif. Accessed 1 Feb 2016

  42. S. De Leo, M. Perrino, S. Badiali, S. Rossi, V. Cirello, C. Colombo, D. Tosi, G. Cantoni, L. Poggi, G. Bulfamante, P. Beck-Peccoz, L. Vicentini, L. Fugazzola, Clinical and molecular analyses of thyroid cancer in patients treated for benign diseases. Endocr. Relat. Cancer 20(4), L7–L10 (2013)

    PubMed  Google Scholar 

  43. J. Liu, B. Singh, G. Tallini, D.L. Carlson, N. Katabi, A. Shaha, R.M. Tuttle, R.A. Ghossein, Follicular variant of papillary thyroid carcinoma: a clinicopathologic study of a problematic entity. Cancer 107(6), 1255–1264 (2006)

    Article  PubMed  Google Scholar 

  44. G. Tzvetov, D. Hirsch, I. Shraga-Slutzky, R. Weinstein, Y. Manistersky, R. Kalmanovich, M. Lapidot, S. Grozinsky-Glasberg, J. Singer, J. Sulkes, I. Shimon, C. Benbassat, Well-differentiated thyroid carcinoma: comparison of microscopic and macroscopic disease. Thyroid 19(5), 487–494 (2009)

    Article  PubMed  Google Scholar 

  45. S.M. Fincham, A.M. Ugnat, G.B. Hill, N. Kreiger, Y. Mao, Canadian Cancer Registries Epidemiology Research Group, Is occupation a risk factor for thyroid cancer? J. Occup. Environ. Med. 42(3), 318–322 (2000)

    Article  CAS  PubMed  Google Scholar 

  46. J.M. Carstensen, G. Wingren, T. Hatschek, M. Fredriksson, H. Noorlind-Brage, O. Axelson, Occupational risks of thyroid cancer: data from the Swedish Cancer-Environment Register, 1961-1979. Am. J. Ind. Med. 18(5), 535–540 (1990)

    Article  CAS  PubMed  Google Scholar 

  47. E.Y. Wong, R. Ray, D.L. Gao, K.J. Wernli, W. Li, E.D. Fitzgibbons, Z. Feng, D.B. Thomas, H. Checkoway, Reproductive history, occupational exposures, and thyroid cancer risk among women textile workers in Shanghai,China. Int. Arch. Occup. Environ. Health. 79(3), 251–258 (2006)

    Article  CAS  PubMed  Google Scholar 

  48. I.H. Kuzmickiene, M.K. Stukonis, Risk of malignant disease among female textile workers in Lithuania. Voprosy Onkologii 55(3), 335–340 (2009)

    CAS  PubMed  Google Scholar 

  49. V. Lope, B. Perez-Gomez, N. Aragones, G. Lopez-Abente, P. Gustavsson, N. Plato, A. Silva-Mato, M. Pollán, Occupational exposure to chemicals and risk of thyroid cancer in Sweden. Int. Arch. Occup. Environ. Health 82(2), 267–274 (2009)

    Article  CAS  PubMed  Google Scholar 

  50. C. Mazzarella, D. Terracciano, A. Di Carlo, P.E. Macchia, E. Consiglio, V. Macchia, A. Mariano, Iodine status assessment in Campania (Italy) as determined by urinary iodine excretion. Nutrition 25(9), 926–929 (2009)

    Article  CAS  PubMed  Google Scholar 

  51. A. Carlé, P. Laurberg, I.B. Pedersen, N. Knudsen, H. Perrild, L. Ovesen, L.B. Rasmussen, T. Jorgensen, Epidemiology of subtypes of hypothyroidism in Denmark. Eur. J. Endocrinol. 154(1), 21–28 (2006)

    Article  PubMed  Google Scholar 

  52. F. Aghini-Lombardi, L. Antonangeli, A. Pinchera, F. Leoli, T. Rago, A.M. Bartolomei, P. Vitti, Effect of iodized salt on thyroid volume of children living in an area previously characterized by moderate iodine deficiency. J. Clin. Endocrinol. Metab. 82(4), 1136–1139 (1997)

    CAS  PubMed  Google Scholar 

  53. P. Malandrino, M. Russo, A. Ronchi, C. Minoia, D. Cataldo, C. Regalbuto, C. Giordano, M. Attard, S. Squatrito, F. Trimarchi, R. Vigneri, Increased thyroid cancer incidence in a basaltic volcanic area is associated with non-anthropogenic pollution and biocontamination. Endocrine (2015). doi:10.1007/s12020-015-0761-0

    PubMed  Google Scholar 

  54. A. Latina, D. Gullo, F. Trimarchi, S. Benvenga, Hashimoto’s thyroiditis: similar and dissimilar characteristics in neighboring areas. Possible implications for the epidemiology of thyroid cancer. PLoS One 8(3), e55450 (2013)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. L.L. Cunha, R.C. Ferreira, M.A. Marcello, J. Vassallo, L.S. Ward, Clinical and pathological implications of concurrent autoimmune thyroid disorders and papillary thyroid cancer. J Thyroid Res. 2011, 387062 (2011)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Authors and Affiliations

  1. Department of Translational Medicine, University of Eastern Piedmont, Via Solaroli 17, 28100, Novara, Italy

    Loredana Pagano, Chiara Mele, Maria Teresa Samà, Marina Caputo, Guido Valente & Gianluca Aimaretti

  2. Department of Clinical Medicine and Surgery, University of Naples Federico II, Naples, Italy

    Debora Arpaia, Serena Ippolito, Carmela Peirce & Bernadette Biondi

  3. Department of Health Sciences, University of Eastern Piedmont, Novara, Italy

    Flavia Prodam

  4. Department of Advanced Biomedical Sciences, University of Naples Federico II, Naples, Italy

    Giuseppe Ciancia

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  1. Loredana Pagano
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Pagano, L., Mele, C., Arpaia, D. et al. How do etiological factors can explain the different clinical features of patients with differentiated thyroid cancer and their histopathological findings?. Endocrine 56, 129–137 (2017). https://doi.org/10.1007/s12020-016-0992-8

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