Abstract
This chapter analyzes histopathological characteristics of papillary thyroid carcinoma (PTC) in subjects of Ukraine who were children and adolescents at the time of the Chernobyl accident. Tumor architecture and invasive properties significantly changed with patients’ age at surgery increasing from 4 to 48 years and with the time elapsed after the accident extending to 30 years. Two major linear trends, the age- and time-related, were revealed for most pathological characteristics; some of them were ascending and some descending. “Radiogenic” PTC in subjects aged ≤4 years at the time of exposure who resided in three regions most contaminated by 131I differed from “sporadic” PTC in age-matched groups of patients from the same regions in terms of both tumor histoarchitectonics and invasiveness. “Radiogenic” PTC displayed a higher frequency of invasive features especially pronounced in children and adolescents. Changes in histopathological characteristics suggest that the phenotype of both “radiogenic” and “sporadic” PTCs becomes less invasive at older patients’ ages. The frequency of intermediate pathological diagnoses of thyroid tumors according to the WHO Classification of Tumours of Endocrine Organs, 4th edition, in the Ukrainian cases included in the Chernobyl Tissue Bank appeared to be not more than 3%.
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References
Kazakov VS, Demidchik EP, Astakhova LN. Thyroid cancer after Chernobyl. Nature. 1992;359(6390):21.
Likhtarev IA, Sobolev BG, Kairo IA, Tronko ND, Bogdanova TI, Oleinic VA, et al. Thyroid cancer in the Ukraine. Nature. 1995;375(6530):365.
Jacob P, Goulko G, Heidenreich WF, Likhtarev I, Kairo I, Tronko ND, et al. Thyroid cancer risk to children calculated. Nature. 1998;392(6671):31–2.
Jacob P, Bogdanova TI, Buglova E, Chepurniy M, Demidchik Y, Gavrilin Y, et al. Thyroid cancer among Ukrainians and Belarusians who were children or adolescents at the time of the Chernobyl accident. J Radiol Prot. 2006;26(1):51–67.
Cardis E, Hatch M. The Chernobyl accident—an epidemiological perspective. Clin Oncol (R Coll Radiol). 2011;23(4):251–60.
Saenko V, Ivanov V, Tsyb A, Bogdanova T, Tronko M, Demidchik Y, et al. The Chernobyl accident and its consequences. Clin Oncol (R Coll Radiol). 2011;23(4):234–43.
Tronko M, Bogdanova T, Saenko V, Thomas GA, Likhtaterv I, Yamashita S, editors. Thyroid cancer in Ukraine after Chernobyl: dosimetry, epidemiology, pathology, molecular biology. Nagasaki: IN-TEX; 2014. p. 175.
Tronko M, Bogdanova T, Shpak V, Gulak L. Thyroid cancer in Ukraine during 1986–2014. In: Bazyka DSV, Chumak A, Chumak V, Yanovich L, editors. Health effects of Chornobyl accident thirty years aftermath. Kyiv: DIA; 2016. p. 85–103.
Tronko M, Brenner AV, Bogdanova T, Shpak V, Oliynyk V, Cahoon EK, et al. Thyroid neoplasia risk is increased nearly 30 years after the Chernobyl accident. Int J Cancer. 2017;141(8):1585–8.
Likhtarov I, Thomas G, Kovgan L, Masiuk S, Chepurny M, Ivanova O, et al. Reconstruction of individual thyroid doses to the Ukrainian subjects enrolled in the Chernobyl Tissue Bank. Radiat Prot Dosimetry. 2013;156(4):407–23.
Likhtarov I, Kovgan L, Masiuk S, Talerko M, Chepurny M, Ivanova O, et al. Thyroid cancer study among Ukrainian children exposed to radiation after the Chornobyl accident: improved estimates of the thyroid doses to the cohort members. Health Phys. 2014;106(3):370–96.
Likhtarov I, Kovgan L, Masiuk S, Chepurny M, Ivanova O, Gerasymenko V, Tronko M, Bogdanova T, Thomas GA Different level of thyroid dose individualisation of the Ukrainian donors in Chernobyl tissue bank. In: Tronko MD, Bogdanova T, Saenko V, Thomas G, Likhtarov I, Yamashita S, editors. Thyroid cancer in Ukraine after Chernobyl: dosimetry, epidemiology, pathology, molecular biology. Nagasaki: IN-TEX; 2014. p. 19–38.
Tronko M, Bogdanova T, Voskoboynyk L, Zurnadzhy L, Shpak V, Gulak L. Radiation induced thyroid cancer: fundamental and applied aspects. Exp Oncol. 2010;32(3):200–4.
Thomas GA, Bogdanova T, Tronko M, Yamashita S. Ukrainian contribution to the international Chernobyl Tissue Bank. In: Tronko MD, Bogdanova T, Saenko V, Thomas G, Likhtarov I, Yamashita S, editors. Thyroid cancer in Ukraine after Chernobyl: dosimetry, epidemiology, pathology, molecular biology. Nagasaki: IN-TEX; 2014. p. 135–42.
Thomas G. Somatic genomics of childhood thyroid cancer. In: Yamashita S, Thomas G, editors. Thyroid cancer and Nuclear accidents – long term after effects of Chernobyl and Fukushima. London: Academic Press/Elsevier; 2017. p. 121–32.
Tronko MD, Bogdanova TI, Komissarenko IV, Epstein OV, Oliynyk V, Kovalenko A, et al. Thyroid carcinoma in children and adolescents in Ukraine after the Chernobyl nuclear accident: statistical data and clinicomorphologic characteristics. Cancer. 1999;86(1):149–56.
Williams ED, Abrosimov A, Bogdanova T, Demidchik EP, Ito M, LiVolsi V, et al. Thyroid carcinoma after Chernobyl latent period, morphology and aggressiveness. Br J Cancer. 2004;90(11):2219–24.
Thomas GA, Williams ED, Becker DV, Bogdanova TI, Demidchik EP, Lushnikov E, et al. Chernobyl tumor bank. Thyroid. 2000;10(12):1126–7.
Suzuki S. Childhood and adolescent thyroid cancer in Fukushima after the Fukushima Daiichi nuclear power plant accident: 5 years on. Clin Oncol (R Coll Radiol). 2016;28(4):263–71.
Ezaki H, Ebihara S, Fujimoto Y, Iida F, Ito K, Kuma K, et al. Analysis of thyroid carcinoma based on material registered in Japan during 1977-1986 with special reference to predominance of papillary type. Cancer. 1992;70(4):808–14.
Dobyns BM, Hyrmer BA. The surgical management of benign and malignant thyroid neoplasms in Marshall Islanders exposed to hydrogen bomb fallout. World J Surg. 1992;16(1):126–39. discussion 39–40
Harach HR, Williams ED. Childhood thyroid cancer in England and Wales. Br J Cancer. 1995;72(3):777–83.
LiVolsi VA, Abrosimov AA, Bogdanova T, Fadda G, Hunt JL, Ito M, et al. The Chernobyl thyroid cancer experience: pathology. Clin Oncol (R Coll Radiol). 2011;23(4):261–7.
Bogdanova T, Zurnadzhy L, LiVolsi VA, Williams ED, Ito M, Nakashima M, Thomas GA. Thyroid cancer pathology in Ukraine after Chernobyl. In: Tronko MD, Bogdanova T, Saenko V, Thomas G, Likhtarov I, Yamashita S, editors. Thyroid cancer in Ukraine after Chernobyl: dosimetry, epidemiology, pathology, molecular biology. Nagasaki: IN-TEX; 2014. p. 109–35.
Bogdanova TI, Kozyritsky V, Tronko M, Likhtarov I, Kairo I, Chepurnoy M, Shpak V. Morphological features and analysis of radiation risk of development of post-Chernobyl thyroid carcinoma in children and adolescents of Ukraine. In: Thomas G, Karaoglou A, Williams ED, editors. Radiation and thyroid cancer. Singapore: World Scientific; 1999. p. 151–4.
Nikiforov YE, Erickson LA, Nikiforova MN, Caudill CM, Lloyd RV. Solid variant of papillary thyroid carcinoma: incidence, clinical-pathologic characteristics, molecular analysis, and biologic behavior. Am J Surg Pathol. 2001;25(12):1478–84.
Nikiforov Y, Biddinger PW, Thompson LDR. Diagnostic pathology and molecular genetics of the thyroid. 2nd ed. Philadelphia: Wolters Kluwer; 2012. p. 375.
Zuo H, Tang W, Kakudo K. Prognostic factors of papillary carcinoma of the thyroid. In: Ito Y, Miyauchi A, Amino N, editors. Recent advances in thyroid cancer research. Kerala: Transworld research network; 2006. p. 33–48.
Rosai J. Thyroid gland. In: Rosai J, editor. Rosai and Ackerman’s surgical pathology. 10th ed. Edinburgh: Mosby; 2011. p. 487–564.
DeLellis RA, Lloyd R, Heitz PH, Eng CH, editors. Pathology and genetics of tumours of endocrine organs. 3rd ed. Lyon: IARC Press; 2004. p. 320.
Lloyd RV, Osamura RY, Kloppel G, Rosai J, editors. WHO classification of tumours of endocrine organs. 4th ed. Lyon: IARC Press; 2017. p. 355.
Sobin LH, Gospodarowicz MK. Wittekind C and International Union against Cancer. TNM classification of malignant tumours. Wiley-Blackwell: Chichester; 2010. p. 320.
Brierley JD, Gospodarowich MK, Wittekind C. TNM classification of malignant tumours. 8th ed. Oxford: Wiley-Blackwell; 2017. p. 233.
Ahn HS, Kim HJ, Welch HG. Korea’s thyroid-cancer “epidemic”—screening and overdiagnosis. N Engl J Med. 2014;371(19):1765–7.
Ahn HS, Kim HJ, Kim KH, Lee YS, Han SJ, Kim Y, et al. Thyroid cancer screening in South Korea increases detection of papillary cancers with no impact on other subtypes or thyroid cancer mortality. Thyroid. 2016;26(11):1535–40.
Yamashita S, Radiation Medical Science Center for the Fukushima Health Management S. Comprehensive health risk management after the Fukushima nuclear power plant accident. Clin Oncol (R Coll Radiol). 2016;28(4):255–62.
Yamashita S, Saenko VA. What is the “screening effect” six years after the fukushima nuclear power plant accident? Thyroid. 2017;27(5):595–6.
Yamashita S, Suzuki S, Suzuki S, Shimura H, Saenko V. Lessons from Fukushima: latest findings of thyroid cancer after the fukushima nuclear power plant accident. Thyroid. 2018;28(1):11–22. https://doi.org/10.1089/thy.2017.0283.
Hershman JM. The increased incidence of thyroid cancer is worldwide. Clin Thyroidol. 2017;29:11–2.
Vaccarella S, Franceschi S, Bray F, Wild CP, Plummer M, Dal Maso L. Worldwide thyroid-cancer epidemic? The increasing impact of overdiagnosis. N Engl J Med. 2016;375(7):614–7.
Pearse EN. Thyroid cancer overdiagnosis is a result of screening programs in South Korea. Clin Thyroidol. 2017;29:8–10.
Oda H, Miyauchi A, Ito Y, Yoshioka K, Nakayama A, Sasai H, et al. Incidences of unfavorable events in the management of low-risk papillary microcarcinoma of the thyroid by active surveillance versus immediate surgery. Thyroid. 2016;26(1):150–5.
Leboulleux S, Tuttle RM, Pacini F, Schlumberger M. Papillary thyroid microcarcinoma: time to shift from surgery to active surveillance? Lancet Diabetes Endocrinol. 2016;4(11):933–42.
Leung A. Active surveillance of small, low-risk papillary thyroid cancer can be a safe alternative to surgery in selected patients. Clin Thyroidol. 2017;29:97–9.
Miyauchi A, Ito Y, Oda H. Insights into the management of papillary microcarcinoma of the thyroid. Thyroid. 2018;28(1):23–31. https://doi.org/10.1089/thy.2017.0227.
Bogdanova T, Saenko V, Shpak V, Zurnadzhy L, Voskoboynyk L, Dekhtyarova T, Burko S, Gulii T, Yamashita S, Tronko M. Long-term Analysis of the Incidence and Histopathology of Thyroid Cancer in Ukraine in adult patients who were children and adolescents at the time of the Chernobyl accident. In: Yamashita S, Thomas G, editors. Thyroid cancer and nuclear accidents – long term after effects of Chernobyl and Fukushima. London: Academic Press/Elsevier; 2017. p. 67–76.
Demidchik Y, Fridman M, Schmid KW, Reiners C, Biko J, Mankovskaya S. Papillary thyroid cancer in childhood and adolescence with specific consideration of patients after radiation exposure. In: Fahey TJ, editor. Updates in the understanding and management of thyroid cancer. Rijeka: InTech; 2012. p. 163–88.
Fridman M, Lam AK, Krasko O, Schmid KW, Branovan DI, Demidchik Y. Morphological and clinical presentation of papillary thyroid carcinoma in children and adolescents of Belarus: the influence of radiation exposure and the source of irradiation. Exp Mol Pathol. 2015;98(3):527–31.
Williams D. Radiation carcinogenesis: lessons from Chernobyl. Oncogene. 2008;27(Suppl 2):S9–18.
Williams ED, Abrosimov A, Bogdanova T, Demidchik EP, Ito M, LiVolsi V, et al. Morphologic characteristics of Chernobyl-related childhood papillary thyroid carcinomas are independent of radiation exposure but vary with iodine intake. Thyroid. 2008;18(8):847–52.
Bogdanova T, Saenko V, Zurnadzhy L, Likhtarov I, Kovgan L, Masiuk S, Kashcheev V, LiVolsi VA, Williams ED, Ito M, Mine M, Thomas GA, Tronko M, Yamashita S. Comparative pathological analysis of papillary thyroid carcinoma in age-matched groups of patients born before and after Chernobyl. In: Tronko MD, Bogdanova T, Saenko V, Thomas G, Likhtarov I, Yamashita S, editors. Thyroid cancer in Ukraine after Chernobyl: dosimetry, epidemiology, pathology, molecular biology. Nagasaki: IN-TEX; 2014. p. 65–108.
Nikiforov YE, Seethala RR, Tallini G, Baloch ZW, Basolo F, Thompson LD, et al. Nomenclature revision for encapsulated follicular variant of papillary thyroid carcinoma: a paradigm shift to reduce overtreatment of indolent tumors. JAMA Oncol. 2016;2(8):1023–9.
Fugazzola L, Pilotti S, Pinchera A, Vorontsova TV, Mondellini P, Bongarzone I, et al. Oncogenic rearrangements of the RET proto-oncogene in papillary thyroid carcinomas from children exposed to the Chernobyl nuclear accident. Cancer Res. 1995;55(23):5617–20.
Klugbauer S, Lengfelder E, Demidchik EP, Rabes HM. High prevalence of RET rearrangement in thyroid tumors of children from Belarus after the Chernobyl reactor accident. Oncogene. 1995;11(12):2459–67.
Nikiforov YE, Rowland JM, Bove KE, Monforte-Munoz H, Fagin JA. Distinct pattern of ret oncogene rearrangements in morphological variants of radiation-induced and sporadic thyroid papillary carcinomas in children. Cancer Res. 1997;57(9):1690–4.
Nikiforova MN, Ciampi R, Salvatore G, Santoro M, Gandhi M, Knauf JA, et al. Low prevalence of BRAF mutations in radiation-induced thyroid tumors in contrast to sporadic papillary carcinomas. Cancer Lett. 2004;209(1):1–6.
Lima J, Trovisco V, Soares P, Maximo V, Magalhaes J, Salvatore G, et al. BRAF mutations are not a major event in post-Chernobyl childhood thyroid carcinomas. J Clin Endocrinol Metab. 2004;89(9):4267–71.
Kumagai A, Namba H, Saenko VA, Ashizawa K, Ohtsuru A, Ito M, et al. Low frequency of BRAFT1796A mutations in childhood thyroid carcinomas. J Clin Endocrinol Metab. 2004;89(9):4280–4.
Powell N, Jeremiah S, Morishita M, Dudley E, Bethel J, Bogdanova T, et al. Frequency of BRAF T1796A mutation in papillary thyroid carcinoma relates to age of patient at diagnosis and not to radiation exposure. J Pathol. 2005;205(5):558–64.
Dom G, Tarabichi M, Unger K, Thomas G, Oczko-Wojciechowska M, Bogdanova T, et al. A gene expression signature distinguishes normal tissues of sporadic and radiation-induced papillary thyroid carcinomas. Br J Cancer. 2012;107(6):994–1000.
Ricarte-Filho JC, Li S, Garcia-Rendueles ME, Montero-Conde C, Voza F, Knauf JA, et al. Identification of kinase fusion oncogenes in post-Chernobyl radiation-induced thyroid cancers. J Clin Invest. 2013;123(11):4935–44.
Handkiewicz-Junak D, Swierniak M, Rusinek D, Oczko-Wojciechowska M, Dom G, Maenhaut C, et al. Gene signature of the post-Chernobyl papillary thyroid cancer. Eur J Nucl Med Mol Imaging. 2016;43(7):1267–77.
Leeman-Neill RJ, Brenner AV, Little MP, Bogdanova TI, Hatch M, Zurnadzy LY, et al. RET/PTC and PAX8/PPARgamma chromosomal rearrangements in post-Chernobyl thyroid cancer and their association with iodine-131 radiation dose and other characteristics. Cancer. 2013;119(10):1792–9.
Efanov AA, Brenner AV, Bogdanova TI, Kelly LM, Liu P, Little MP, et al. Investigation of the relationship between radiation dose and gene mutations and fusions in post-Chernobyl thyroid cancer. J Natl Cancer Inst. 2018;110(4):371–8. https://doi.org/10.1093/jnci/djx209.
Bogdanova TI, Zurnadzhy LY, Nikiforov YE, Leeman-Neill RJ, Tronko MD, Chanock S, et al. Histopathological features of papillary thyroid carcinomas detected during four screening examinations of a Ukrainian-American cohort. Br J Cancer. 2015;113(11):1556–64.
Leeman-Neill RJ, Kelly LM, Liu P, Brenner AV, Little MP, Bogdanova TI, et al. ETV6-NTRK3 is a common chromosomal rearrangement in radiation-associated thyroid cancer. Cancer. 2014;120(6):799–807.
Rosai J, Carcangiu ML, DeLellis RA. Tumors of the thyroid gland. Washington, DC: Armed Forces Institute of Pathology; 1992. p. 343.
Williams ED. Guest editorial: two proposals regarding the terminology of thyroid tumors. Int J Surg Pathol. 2000;8(3):181–3.
Haugen BR, Sawka AM, Alexander EK, Bible KC, Caturegli P, Doherty GM, et al. American Thyroid Association Guidelines on the Management of Thyroid Nodules and Differentiated Thyroid Cancer Task Force Review and Recommendation on the Proposed Renaming of Encapsulated Follicular Variant Papillary Thyroid Carcinoma Without Invasion to Noninvasive Follicular Thyroid Neoplasm with Papillary-Like Nuclear Features. Thyroid. 2017;27(4):481–3.
Xu B, Tallini G, Scognamiglio T, Roman BR, Tuttle RM, Ghossein RA. Outcome of large noninvasive follicular thyroid neoplasm with papillary-like nuclear features. Thyroid. 2017;27(4):512–7.
Acknowledgments
We acknowledge the commitment of the staff of the Laboratory of Morphology of Endocrine System who prepared all pathological material and the staff of the Department of Surgery of Endocrine System of IEM who operated these patients. The authors gratefully acknowledge the confirmation of diagnoses by the International Pathology Panel of the Chernobyl Tissue Bank: Professors A. Abrosimov, T. Bogdanova, G. Fadda, J. Hunt, M. Ito, V. Livolsi, J. Rosai, E. D. Williams, and Dr. N. Dvinskyh.
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Bogdanova, T.I. et al. (2019). Pathology of Radiation-Induced Thyroid Cancer: Lessons from Chernobyl Thyroid Cancer Study. In: Kakudo, K. (eds) Thyroid FNA Cytology. Springer, Singapore. https://doi.org/10.1007/978-981-13-1897-9_70
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