Geographic influences in the global rise of thyroid cancer

Abstract

The incidence of thyroid cancer is on the rise, and this disease is projected to become the fourth leading type of cancer across the globe. From 1990 to 2013, the global age-standardized incidence rate of thyroid cancer increased by 20%. This global rise in incidence has been attributed to several factors, including increased detection of early tumours, the elevated prevalence of modifiable individual risk factors (for example, obesity) and increased exposure to environmental risk factors (for example, iodine levels). In this Review, we explore proven and novel hypotheses for how modifiable risk factors and environmental exposures might be driving the worldwide increase in the incidence of thyroid cancer. Although overscreening and the increased diagnosis of possibly clinically insignificant disease might have a role in certain parts of the world, other areas could be experiencing a true increase in incidence due to elevated exposure risks. In the current era of personalized medicine, national and international registry data should be applied to identify populations who are at increased risk for the development of thyroid cancer.

Key points

  • The incidence of thyroid cancer in higher-income countries has been rising; the causes appear to be complex and multifactorial.

  • Several upper middle-income countries have regional cancer registries that help to better understand cancer incidence in the context of environmental influences, such as iodine supplementation.

  • In lower middle-income and low-income countries, understanding thyroid cancer incidence has been predominantly limited to single-centre studies.

  • Proposed influences in the development of thyroid cancer include dietary changes and environmental exposures, which vary based on region.

  • The development of regional or national cancer registries in low-income countries would provide a rich repository to study thyroid cancer in regions with varying environmental and social exposures.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Fig. 1: Global estimated age-standardized incidence rates of thyroid cancer in 2018.
Fig. 2: Global estimated age-standardized mortality of thyroid cancer in 2018.

References

  1. 1.

    Fitzmaurice, C. et al. The global burden of cancer 2013. JAMA Oncol. 1, 505–527 (2015).

    Google Scholar 

  2. 2.

    Ferlay, J. et al. Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int. J. Cancer 136, E359–E386 (2015).

    CAS  PubMed  Google Scholar 

  3. 3.

    La Vecchia, C. et al. Thyroid cancer mortality and incidence: a global overview. Int. J. Cancer 136, 2187–2195 (2014). This study uses data from the WHO and Cancer Incidence in Five Continents to describe recent worldwide trends in thyroid cancer.

    PubMed  Google Scholar 

  4. 4.

    Lim, H., Devesa, S. S., Sosa, J. A., Check, D. & Kitahara, C. M. Trends in thyroid cancer incidence and mortality in the United States, 1974–2013. JAMA 317, 1338–1348 (2017). This study of the Surveillance, Epidemiology, and End Results-9 cancer registry in the USA finds that the incidence of thyroid cancer has increased from 1974 to 2013.

    PubMed  Google Scholar 

  5. 5.

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

    PubMed  PubMed Central  Google Scholar 

  6. 6.

    Liu, Y., Su, L. & Xiao, H. Review of factors related to the thyroid cancer epidemic. Int. J. Endocrinol. 2017, 5308635 (2017).

    PubMed  PubMed Central  Google Scholar 

  7. 7.

    World Bank Country and Lending Groups – World Bank Data Help Desk. Available at: https://datahelpdesk.worldbank.org/knowledgebase/articles/906519-world-bank-country-and-lending-groups. (Accessed: February 2019).

  8. 8.

    Vaccarella, S. et al. The impact of diagnostic changes on the rise in thyroid cancer incidence: a population-based study in selected high-resource countries. Thyroid 25, 1127–1136 (2015).

    PubMed  Google Scholar 

  9. 9.

    Enewold, L. et al. Rising thyroid cancer incidence in the United States by demographic and tumor characteristics, 1980–2005. Cancer Epidemiol. Biomark. Prev. 18, 784–791 (2009).

    Google Scholar 

  10. 10.

    Ogden, C. L., Carroll, M. D., Kit, B. K. & Flegal, K. M. Prevalence of childhood and adult obesity in the United States, 2011–2012. JAMA 311, 806–814 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  11. 11.

    Kitahara, C. M. et al. Obesity and thyroid cancer risk among US men and women: a pooled analysis of five prospective studies. Cancer Epidemiol. Biomark. Prev. 20, 464–472 (2011).

    Google Scholar 

  12. 12.

    Malik, V. S., Willett, W. C. & Hu, F. B. Global obesity: trends, risk factors and policy implications. Nat. Rev. Endocrinol. 9, 13–27 (2013).

    PubMed  Google Scholar 

  13. 13.

    Colonna, M. et al. Incidence of thyroid cancer in adults recorded by French cancer registries (1978–1997). Eur. J. Cancer 38, 1762–1768 (2002).

    CAS  PubMed  Google Scholar 

  14. 14.

    Forside - DTU Fødevareinstituttet. http://www.food.dtu.dk Available at: http://www.food.dtu.dk/. (Accessed: February 2019).

  15. 15.

    Laurberg, P. et al. Implementation and monitoring of iodine supplementation in Denmark: the Danthyr program. IDD Newsletter 19(4), (2003).

  16. 16.

    Rasmussen, L. B. et al. Iodine intake before and after mandatory iodization in Denmark: results from the Danish investigation of iodine intake and thyroid diseases (DanThyr) study. Br. J. Nutr. 100, 166–173 (2008).

    CAS  PubMed  Google Scholar 

  17. 17.

    Blomberg, M., Feldt-Rasmussen, U., Andersen, K. K. & Kjaer, S. K. Thyroid cancer in Denmark 1943–2008, before and after iodine supplementation. Int. J. Cancer 131, 2360–2366 (2012).

    CAS  PubMed  Google Scholar 

  18. 18.

    Bülow Pedersen, I. et al. An increased incidence of overt hypothyroidism after iodine fortification of salt in Denmark: a prospective population study. J. Clin. Endocrinol. Metab. 92, 3122–3127 (2007).

    Google Scholar 

  19. 19.

    Carle, A. et al. Epidemiology of subtypes of hypothyroidism in Denmark. Eur. J. Endocrinol. 154, 21–28 (2006).

    CAS  PubMed  Google Scholar 

  20. 20.

    Møllehave, L. T. et al. Trends in treatments of thyroid disease following iodine fortification in Denmark: a nationwide register-based study. Clin. Epidemiol. 10, 763–770 (2018).

    PubMed  PubMed Central  Google Scholar 

  21. 21.

    Hori, M. et al. Cancer incidence and incidence rates in Japan in 2009: a study of 32 population-based cancer registries for the monitoring of cancer incidence in Japan (MCIJ) project. Jpn. J. Clin. Oncol. 45, 884–891 (2015).

    PubMed  Google Scholar 

  22. 22.

    Jung, K.-W. et al. Cancer statistics in Korea: incidence, mortality, survival, and prevalence in 2012. Cancer Res. Treat. 47, 127–141 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  23. 23.

    Lee, J. W. et al. Cancer screening using 18F-FDG PET/CT in Korean asymptomatic volunteers: a preliminary report. Ann. Nucl. Med. 23, 685–691 (2009).

    PubMed  Google Scholar 

  24. 24.

    Tsuda, T., Tokinobu, A., Yamamoto, E. & Suzuki, E. Thyroid cancer detection by ultrasound among residents ages 18 years and younger in Fukushima, Japan: 2011 to 2014. Epidemiology 27, 316–322 (2016).

    PubMed  PubMed Central  Google Scholar 

  25. 25.

    Hiranuma, Y. Misrepresented risk of thyroid cancer in Fukushima. Lancet Diabetes Endocrinol. 4, 970 (2016).

    PubMed  Google Scholar 

  26. 26.

    Sadkowsky, K. et al. Epidemiology research using the national cancer statistics clearing house and the national death index databases. Australas. Epidemiol. 8, 29 (2001).

    Google Scholar 

  27. 27.

    Burgess, J. R., Dwyer, T., McArdle, K., Tucker, P. & Shugg, D. The changing incidence and spectrum of thyroid carcinoma in Tasmania (1978–1998) during a transition from iodine sufficiency to iodine deficiency. J. Clin. Endocrinol. Metab. 85, 1513–1517 (2000).

    CAS  PubMed  Google Scholar 

  28. 28.

    Richards, P. A. Iodine nutrition in two Tasmanian cultures. Med. J. Aust. 163, 628–630 (1995).

    CAS  PubMed  Google Scholar 

  29. 29.

    Melick R. & Van Middlesworth L. Radio-iodine fallout in Australian sheep. Med. J. Aust. 2, 930–932 (1966).

  30. 30.

    Burgess, J. R. Temporal trends for thyroid carcinoma in Australia: an increasing incidence of papillary thyroid carcinoma (1982–1997). Thyroid 12, 141–149 (2002).

    PubMed  Google Scholar 

  31. 31.

    Wang, Y. & Wang, W. Increasing incidence of thyroid cancer in Shanghai, China, 1983–2007. Asia Pac. J. Public Health 27, NP223–NP229 (2015).

    PubMed  Google Scholar 

  32. 32.

    Liu, Y. et al. The prevalence of thyroid nodules in northwest China and its correlation with metabolic parameters and uric acid. Oncotarget 8, 41555–41562 (2017).

    PubMed  PubMed Central  Google Scholar 

  33. 33.

    Yao, Y. et al. Thyroid nodules in centenarians: prevalence and relationship to lifestyle characteristics and dietary habits. Clin. Interv. Aging 13, 515–522 (2018).

    PubMed  PubMed Central  Google Scholar 

  34. 34.

    Tazi, M. A., Er-Raki, A. & Benjaafar, N. Cancer incidence in Rabat, Morocco: 2006–2008. Ecancermedicalscience 7, (338 (2013).

    Google Scholar 

  35. 35.

    Jagathnath Krishna, K. M. & Sebastian, P. Cancer incidence and mortality: district cancer registry, Trivandrum, South India. Asian Pac. J. Cancer Prev. 18, 1485–1491 (2017).

    Google Scholar 

  36. 36.

    Lo, T. E., Uy, A. & Maningat, P. D. Well-differentiated thyroid cancer: the Philippine general hospital experience. Endocrine Abstracts 37, EP838, https://doi.org/10.1530/endoabs.37.EP838 (2015).

    Article  Google Scholar 

  37. 37.

    Ukekwe, F. I., Olusina, D. B. & Okere, P. C. N. Patterns of thyroid cancers in Southeastern Nigeria: a 15 year histopathologic review (2000–2014). J. Clin. Diagn. Res. 11, EC16–EC19 (2017).

    PubMed  PubMed Central  Google Scholar 

  38. 38.

    Bukhari, U., Sadiq, S., Memon, J. & Baig, F. Thyroid carcinoma in Pakistan: a retrospective review of 998 cases from an academic referral center. Hematol. Oncol. Stem Cell Ther. 2, 345–348 (2009).

    PubMed  Google Scholar 

  39. 39.

    Lortet-Tieulent, J. & Vaccarella, S. International and subnational variation thyroid cancer incidence and mortality over 2008–2012. Rev. d’Épidémiologie et de Santé Publique 66, S254 (2018).

    Google Scholar 

  40. 40.

    James, B. C. et al. An update in international trends in incidence rates of thyroid cancer, 1973–2007. Cancer Causes Control 29, 465–473 (2018).

    PubMed  Google Scholar 

  41. 41.

    Ahn, H. S., Kim, H. J. & Welch, H. G. Korea’s thyroid-cancer ‘epidemic’ — screening and overdiagnosis. N. Engl. J. Med. 371, 1765–1767 (2014). This perspective piece reviews trends in thyroid cancer incidence in South Korea following the initiation of a government-led national cancer screening program.

    PubMed  Google Scholar 

  42. 42.

    Vaccarella, S. et al. Worldwide thyroid-cancer epidemic? The increasing impact of overdiagnosis. N. Engl. J. Med. 375, 614–617 (2016).

    PubMed  Google Scholar 

  43. 43.

    D’Avanzo, B., La Vecchia, C., Franceschi, S., Negri, E. & Talamini, R. History of thyroid diseases and subsequent thyroid cancer risk. Cancer Epidemiol. Biomark. Prev. 4, 193–199 (1995).

    Google Scholar 

  44. 44.

    Balasubramaniam, S., Ron, E., Gridley, G., Schneider, A. B. & Brenner, A. V. Association between benign thyroid and endocrine disorders and subsequent risk of thyroid cancer among 4.5 million U.S. male veterans. J. Clin. Endocrinol. Metab. 97, 2661–2669 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  45. 45.

    Nosé, V. Familial thyroid cancer: a review. Mod. Pathol. 24, S19–S33 (2011).

    PubMed  Google Scholar 

  46. 46.

    Xu, L., Li, G., Wei, Q., El-Naggar, A. K. & Sturgis, E. M. Family history of cancer and risk of sporadic differentiated thyroid carcinoma. Cancer 118, 1228–1235 (2012).

    PubMed  Google Scholar 

  47. 47.

    Azar, F. K., Lee, S. L. & Rosen, J. E. Medullary thyroid cancer: an update for surgeons. Am. Surg. 81, 1–8 (2015).

    PubMed  Google Scholar 

  48. 48.

    Kouvaraki, M. A. et al. RET proto-oncogene: a review and update of genotype–phenotype correlations in hereditary medullary thyroid cancer and associated endocrine tumors. Thyroid 15, 531–544 (2005).

    CAS  PubMed  Google Scholar 

  49. 49.

    Moses, W., Weng, J. & Kebebew, E. Prevalence, clinicopathologic features, and somatic genetic mutation profile in familial versus sporadic nonmedullary thyroid cancer. Thyroid 21, 367–371 (2011).

    PubMed  PubMed Central  Google Scholar 

  50. 50.

    Xing, M. The T1799A BRAF mutation is not a germline mutation in familial nonmedullary thyroid cancer. Clin. Endocrinol. 63, 263–266 (2005).

    CAS  Google Scholar 

  51. 51.

    Cavaco, B. M. et al. Familial non-medullary thyroid carcinoma (FNMTC): analysis of fPTC/PRN, NMTC1, MNG1 and TCO susceptibility loci and identification of somatic BRAF and RAS mutations. Endocr. Relat. Cancer 15, 207–215 (2008).

    PubMed  Google Scholar 

  52. 52.

    Nosé, V. Familial non-medullary thyroid carcinoma: an update. Endocr. Pathol. 19, 226–240 (2008).

    PubMed  Google Scholar 

  53. 53.

    El Lakis, M. et al. Do patients with familial nonmedullary thyroid cancer present with more aggressive disease? Implications for initial surgical treatment. Surgery 165, 50–57 (2019).

    PubMed  Google Scholar 

  54. 54.

    Peiling Yang, S. & Ngeow, J. Familial non-medullary thyroid cancer: unraveling the genetic maze. Endocr. Relat. Cancer 23, R577–R595 (2016).

    PubMed  Google Scholar 

  55. 55.

    Robinson, D. W. & Orr, T. G. Carcinoma of the thyroid and other diseases of the thyroid in identical twins. AMA Arch. Surg. 70, 923–928 (1955).

    CAS  PubMed  Google Scholar 

  56. 56.

    McKay, J. D. et al. At least three genes account for familial papillary thyroid carcinoma: TCO and MNG1 excluded as susceptibility loci from a large Tasmanian family. Eur. J. Endocrinol. 141, 122–125 (1999).

    CAS  PubMed  Google Scholar 

  57. 57.

    Tsilchorozidou, T. et al. A Greek family with a follicular variant of familial papillary thyroid carcinoma: TCO, MNG1, fPTC/PRN, and NMTC1 excluded as susceptibility loci. Thyroid 15, 1349–1354 (2005).

    CAS  PubMed  Google Scholar 

  58. 58.

    Loh, K. C. Familial nonmedullary thyroid carcinoma: a meta-review of case series. Thyroid 7, 107–113 (1997).

    CAS  PubMed  Google Scholar 

  59. 59.

    Fallah, M. et al. Risk of thyroid cancer in first-degree relatives of patients with non-medullary thyroid cancer by histology type and age at diagnosis: a joint study from five Nordic countries. J. Med. Genet. 50, 373–382 (2013).

    CAS  PubMed  Google Scholar 

  60. 60.

    Roti, E., degli Uberti, E. C., Bondanelli, M. & Braverman, L. E. Thyroid papillary microcarcinoma: a descriptive and meta-analysis study. Eur. J. Endocrinol. 159, 659–673 (2008).

    CAS  PubMed  Google Scholar 

  61. 61.

    Fukunaga, F. H. & Yatani, R. Geographic pathology of occult thyroid carcinomas. Cancer 36, 1095–1099 (1975).

    CAS  PubMed  Google Scholar 

  62. 62.

    Sampson, R. J., Woolner, L. B., Bahn, R. C. & Kurland, L. T. Occult thyroid carcinoma in Olmsted county, Minnesota: prevalence at autopsy compared with that in Hiroshima and Nagasaki, Japan. Cancer 34, 2072–2076 (1974).

    Google Scholar 

  63. 63.

    Harach, H. R., Franssila, K. O. & Wasenius, V.-M. Occult papillary carcinoma of the thyroid. A ‘normal’ finding in Finland. A systematic autopsy study. Cancer 56, 531–538 (1985).

    CAS  PubMed  Google Scholar 

  64. 64.

    Lim, D.-J. et al. Clinical, histopathological, and molecular characteristics of papillary thyroid microcarcinoma. Thyroid 17, 883–888 (2007).

    CAS  PubMed  Google Scholar 

  65. 65.

    Yamashita, H. et al. Extracapsular invasion of lymph node metastasis. A good indicator of disease recurrence and poor prognosis in patients with thyroid microcarcinoma. Cancer 86, 842–849 (1999).

    CAS  PubMed  Google Scholar 

  66. 66.

    Pelizzo, M. R. et al. High prevalence of occult papillary thyroid carcinoma in a surgical series for benign thyroid disease. Tumori 76, 255–257 (1990).

    CAS  PubMed  Google Scholar 

  67. 67.

    Pelizzo, M. R. et al. Papillary thyroid microcarcinoma. Long-term outcome in 587 cases compared with published data. Minerva Chir. 62, 315–325 (2007).

    CAS  PubMed  Google Scholar 

  68. 68.

    Shin, H.-R. et al. Nationwide cancer incidence in Korea, 1999–2001: first result using the national cancer incidence database. Cancer Res. Treat. 37, 325–331 (2005).

    PubMed  PubMed Central  Google Scholar 

  69. 69.

    Leenhardt, L., Grosclaude, P. & Chérié-Challine, L. Increased incidence of thyroid carcinoma in France: a true epidemic or thyroid nodule management effects? report from the French thyroid cancer committee. Thyroid 14, 1056–1060 (2004).

    PubMed  Google Scholar 

  70. 70.

    Leenhardt, L., Grosclaude, P., Chérié-Challine, L. & Others. Guidelines for a national epidemiological surveillance system of thyroid cancer in France. Paris: Public Health Agency 1–211 (2003).

  71. 71.

    US Preventive Services Task Force. et al. Screening for thyroid cancer: US preventive services task force recommendation statement. JAMA 317, 1882–1887 (2017).

    Google Scholar 

  72. 72.

    Harris, R. Don’t screen for thyroid cancer, task force says. NPR https://www.npr.org/sections/health-shots/2017/05/09/527569291/dont-screen-for-thyroid-cancer-task-force-says?t=1568120751891 (2017).

  73. 73.

    Kitahara, C. M. et al. Anthropometric factors and thyroid cancer risk by histological subtype: pooled analysis of 22 prospective studies. Thyroid 26, 306–318 (2016). This pooled analysis of 22 prospective studies including over 2 million patients finds that adulthood obesity is associated with higher incidence of papillary, follicular, and anaplastic thyroid cancer.

    PubMed  PubMed Central  Google Scholar 

  74. 74.

    Kitahara, C. M. & Sosa, J. A. The changing incidence of thyroid cancer. Nat. Rev. Endocrinol. 12, 646–653 (2016).

    PubMed  Google Scholar 

  75. 75.

    Ng, M. et al. Global, regional, and national prevalence of overweight and obesity in children and adults during 1980–2013: a systematic analysis for the global burden of disease study 2013. Lancet 384, 766–781 (2014).

    PubMed  PubMed Central  Google Scholar 

  76. 76.

    Bianchini, F., Kaaks, R. & Vainio, H. Overweight, obesity, and cancer risk. Lancet Oncol. 3, 565–574 (2002).

    PubMed  Google Scholar 

  77. 77.

    Han, J. M. et al. Obesity is a risk factor for thyroid cancer in a large, ultrasonographically screened population. Eur. J. Endocrinol. 168, 879–886 (2013).

    CAS  PubMed  Google Scholar 

  78. 78.

    Rinaldi, S. et al. Body size and risk of differentiated thyroid carcinomas: findings from the EPIC study. Int. J. Cancer 131, E1004–E1014 (2012).

    CAS  PubMed  Google Scholar 

  79. 79.

    Engeland, A., Tretli, S., Akslen, L. A. & Bjørge, T. Body size and thyroid cancer in two million Norwegian men and women. Br. J. Cancer 95, 366–370 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  80. 80.

    Trésallet, C. et al. The incidence of papillary thyroid carcinoma and outcomes in operative patients according to their body mass indices. Surgery 156, 1145–1152 (2014).

    PubMed  Google Scholar 

  81. 81.

    Meinhold, C. L. et al. Nonradiation risk factors for thyroid cancer in the US Radiologic Technologists Study. Am. J. Epidemiol. 171, 242–252 (2010).

    PubMed  Google Scholar 

  82. 82.

    Rossing, M. A., Cushing, K. L., Voigt, L. F., Wicklund, K. G. & Daling, J. R. Risk of papillary thyroid cancer in women in relation to smoking and alcohol consumption. Epidemiology 11, 49–54 (2000).

    CAS  PubMed  Google Scholar 

  83. 83.

    Kitahara, C. M. et al. Cigarette smoking, alcohol intake, and thyroid cancer risk: a pooled analysis of five prospective studies in the United States. Cancer Causes Control 23, 1615–1624 (2012). A pooled analysis of five prospective studies conducted in the USA shows that active smoking and alcohol use are associated with a reduced risk of thyroid cancer.

    PubMed  PubMed Central  Google Scholar 

  84. 84.

    Mack, W. J. et al. A pooled analysis of case–control studies of thyroid cancer: cigarette smoking and consumption of alcohol, coffee, and tea. Cancer Causes Control 14, 773–785 (2003).

    PubMed  Google Scholar 

  85. 85.

    Henderson, B. E., Ross, R. K., Pike, M. C. & Casagrande, J. T. Endogenous hormones as a major factor in human cancer. Cancer Res. 42, 3232–3239 (1982).

    CAS  PubMed  Google Scholar 

  86. 86.

    Williams, E. D. TSH and thyroid cancer. Horm. Metab. Res. Suppl. 23, 72–75 (1990).

    CAS  PubMed  Google Scholar 

  87. 87.

    Soldin, O. P., Goughenour, B. E., Gilbert, S. Z., Landy, H. J. & Soldin, S. J. Thyroid hormone levels associated with active and passive cigarette smoking. Thyroid 19, 817–823 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  88. 88.

    Belin, R. M., Astor, B. C., Powe, N. R. & Ladenson, P. W. Smoke exposure is associated with a lower prevalence of serum thyroid autoantibodies and thyrotropin concentration elevation and a higher prevalence of mild thyrotropin concentration suppression in the third National Health and Nutrition Examination Survey (NHANES III). J. Clin. Endocrinol. Metab. 89, 6077–6086 (2004).

    CAS  PubMed  Google Scholar 

  89. 89.

    Piirtola, M. et al. Association of current and former smoking with body mass index: a study of smoking discordant twin pairs from 21 twin cohorts. PLOS One 13, e0200140 (2018).

    PubMed  PubMed Central  Google Scholar 

  90. 90.

    Rasmussen, F., Tynelius, P. & Kark, M. Importance of smoking habits for longitudinal and age-matched changes in body mass index: a cohort study of Swedish men and women. Prev. Med. 37, 1–9 (2003).

    PubMed  Google Scholar 

  91. 91.

    IARC Working Group on the Evaluation of Carcinogenic Risks to Humans & International Agency for Research on Cancer. Betel-quid and Areca-nut Chewing and Some Areca-nut-derived Nitrosamines. (IARC, 2004).

  92. 92.

    Dasgupta, R. et al. Ultrastructural and hormonal modulations of the thyroid gland following arecoline treatment in albino mice. Mol. Cell. Endocrinol. 319, 1–7 (2010).

    CAS  PubMed  Google Scholar 

  93. 93.

    Bouvard, V. et al. Carcinogenicity of consumption of red and processed meat. Lancet Oncol. 16, 1599–1600 (2015).

    PubMed  Google Scholar 

  94. 94.

    Wie, G.-A. et al. Red meat consumption is associated with an increased overall cancer risk: a prospective cohort study in Korea. Br. J. Nutr. 112, 238–247 (2014).

    CAS  PubMed  Google Scholar 

  95. 95.

    Refetoff, S. et al. Continuing occurrence of thyroid carcinoma after irradiation to the neck in infancy and childhood. N. Engl. J. Med. 292, 171–175 (1975).

    CAS  PubMed  Google Scholar 

  96. 96.

    Heidenreich, W. F. et al. Time trends of thyroid cancer incidence in Belarus after the Chernobyl accident. Radiat. Res. 151, 617–625 (1999).

    CAS  PubMed  Google Scholar 

  97. 97.

    Mathews, J. D. et al. Cancer risk in 680,000 people exposed to computed tomography scans in childhood or adolescence: data linkage study of 11 million Australians. BMJ 346, f2360 (2013).

    PubMed  PubMed Central  Google Scholar 

  98. 98.

    Schonfeld, S. J., Lee, C. & Berrington de González, A. Medical exposure to radiation and thyroid cancer. Clin. Oncol. 23, 244–250 (2011).

    CAS  Google Scholar 

  99. 99.

    Lubin, J. H. et al. Thyroid cancer following childhood low-dose radiation exposure: a pooled analysis of nine cohorts. J. Clin. Endocrinol. Metab. 102, 2575–2583 (2017).

    PubMed  PubMed Central  Google Scholar 

  100. 100.

    Brenner, D. J. & Hall, E. J. Computed tomography — an increasing source of radiation exposure. N. Engl. J. Med. 357, 2277–2284 (2007).

    CAS  PubMed  Google Scholar 

  101. 101.

    United Nations Scientific Committee on the Effects of Atomic Radiation. Sources and Effects of Ionizing Radiation. (United Nations Publications, 2000).

  102. 102.

    Konoplya, E. F. & Rolevich, I. V. The Chernobyl catastrophe consequences in the Republic of Belarus. Natl. Rep. https://inis.iaea.org/search/search.aspx?orig_q=RN:27042492 (1996).

  103. 103.

    Mahoney, M. C. et al. Thyroid cancer incidence trends in Belarus: examining the impact of Chernobyl. Int. J. Epidemiol. 33, 1025–1033 (2004).

    PubMed  Google Scholar 

  104. 104.

    Goldman, M. The Russian radiation legacy: its integrated impact and lessons. Environ. Health Perspect. 105, 1385–1391 (1997).

    PubMed  PubMed Central  Google Scholar 

  105. 105.

    Stsjazhko, V. A., Tsyb, A. F., Tronko, N. D., Souchkevitch, G. & Baverstock, K. F. Childhood thyroid cancer since accident at Chernobyl. BMJ 310, 801–801 (1995).

    CAS  PubMed  PubMed Central  Google Scholar 

  106. 106.

    Buglova, E. E., Kenigsberg, J. E. & Sergeeva, N. V. Cancer risk estimation in Belarussian children due to thyroid irradiation as a consequence of the Chernobyl nuclear accident. Health Phys. 71, 45–49 (1996).

    CAS  PubMed  Google Scholar 

  107. 107.

    Furukawa, K. et al. Long-term trend of thyroid cancer risk among Japanese atomic-bomb survivors: 60 years after exposure. Int. J. Cancer 132, 1222–1226 (2013). In this analysis of the Life Span Study cohort of Japanese atomic bomb survivors, childhood exposure to radiation continues to be associated with higher thyroid cancer risk, even decades after exposure.

    CAS  PubMed  Google Scholar 

  108. 108.

    Mughal, B. B. & Demeneix, B. A. Endocrine disruptors: flame retardants and increased risk of thyroid cancer. Nat. Rev. Endocrinol. 13, 627–628 (2017).

    CAS  PubMed  Google Scholar 

  109. 109.

    Hoffman, K., Sosa, J. A. & Stapleton, H. M. Do flame retardant chemicals increase the risk for thyroid dysregulation and cancer? Curr. Opin. Oncol. 29, 7–13 (2017).

    CAS  PubMed  Google Scholar 

  110. 110.

    Meeker, J. D., Johnson, P. I., Camann, D. & Hauser, R. Polybrominated diphenyl ether (PBDE) concentrations in house dust are related to hormone levels in men. Sci. Total Environ. 407, 3425–3429 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  111. 111.

    Slagle, M. Greater exposure to flame retardants might be associated with thyroid cancer — DCRI. Available at: https://dcri.org/flame-retardants-thyroid-cancer/ (2017). (Accessed: August 2019).

  112. 112.

    Betts, K. S. Unwelcome guest: PBDEs in indoor dust. Environ. Health Perspect. 116, A202–A208 (2008).

    PubMed  PubMed Central  Google Scholar 

  113. 113.

    National Toxicology Program. NTP toxicology and carcinogenesis studies of decabromodiphenyl oxide (CAS No. 1163-19-5) in F344/N rats and B6C3F1 mice (feed studies). Natl Toxicol. Program Tech. Rep. Ser. 309, 1–242 (1986).

    Google Scholar 

  114. 114.

    Turyk, M. E. et al. Hormone disruption by PBDEs in adult male sport fish consumers. Environ. Health Perspect. 116, 1635–1641 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  115. 115.

    Johnson, P. I., Stapleton, H. M., Mukherjee, B., Hauser, R. & Meeker, J. D. Associations between brominated flame retardants in house dust and hormone levels in men. Sci. Total Environ. 445–446, 177–184 (2013).

    PubMed  PubMed Central  Google Scholar 

  116. 116.

    Chevrier, J. et al. Polybrominated diphenyl ether (PBDE) flame retardants and thyroid hormone during pregnancy. Environ. Health Perspect. 118, 1444–1449 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  117. 117.

    Stapleton, H. M., Eagle, S., Anthopolos, R., Wolkin, A. & Miranda, M. L. Associations between polybrominated diphenyl ether (PBDE) flame retardants, phenolic metabolites, and thyroid hormones during pregnancy. Environ. Health Perspect. 119, 1454–1459 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  118. 118.

    Aschebrook-Kilfoy, B. et al. Polybrominated diphenyl ethers and thyroid cancer risk in the prostate, colorectal, lung, and ovarian cancer screening trial cohort. Am. J. Epidemiol. 181, 883–888 (2015). This nested, case-control study in the Prostate, Lung, Colorectal, and Ovarian Cancer screening trial examines serum levels of PBDEs and finds no association between PBDEs and thyroid cancer.

    PubMed  PubMed Central  Google Scholar 

  119. 119.

    Hoffman, K. et al. Exposure to flame retardant chemicals and occurrence and severity of papillary thyroid cancer: a case–control study. Environ. Int. 107, 235–242 (2017).

    CAS  PubMed  Google Scholar 

  120. 120.

    Woodruff, S. L., Arowolo, O. A., Akute, O. O., Afolabi, A. O. & Nwariaku, F. Global variation in the pattern of differentiated thyroid cancer. Am. J. Surg. 200, 462–466 (2010).

    PubMed  Google Scholar 

  121. 121.

    Wiltshire, J. J., Drake, T. M., Uttley, L. & Balasubramanian, S. P. Systematic review of trends in the incidence rates of thyroid cancer. Thyroid 26, 1541–1552 (2016).

    PubMed  Google Scholar 

  122. 122.

    Regional Committee for Africa. Iodine deficiency disorders in the WHO African region: situation analysis and way forward. https://apps.who.int/iris/handle/10665/19986 (2008).

  123. 123.

    Kalk, W. J., Sitas, F. & Patterson, A. C. Thyroid cancer in South Africa — an indicator of regional iodine deficiency. S. Afr. Med. J. 87, 735–738 (1997).

    CAS  PubMed  Google Scholar 

  124. 124.

    Kung, T. M., Ng, W. L. & Gibson, J. B. Volcanoes and carcinoma of the thyroid: a possible association. Arch. Environ. Health 36, 265–267 (1981).

    CAS  PubMed  Google Scholar 

  125. 125.

    Paksoy, N., Montaville, B. & McCarthy, S. W. Cancer occurrence in Vanuatu in the South Pacific, 1980–86. Asia Pac. J. Public Health 3, 231–236 (1989).

    CAS  PubMed  Google Scholar 

  126. 126.

    Truong, T. et al. Time trends and geographic variations for thyroid cancer in New Caledonia, a very high incidence area (1985–1999). Eur. J. Cancer Prev. 16, 62 (2007).

    PubMed  Google Scholar 

  127. 127.

    Pellegriti, G. et al. Papillary thyroid cancer incidence in the volcanic area of Sicily. J. Natl Cancer Inst. 101, 1575–1583 (2009).

    CAS  PubMed  Google Scholar 

  128. 128.

    Malandrino, P. et al. Descriptive epidemiology of human thyroid cancer: experience from a regional registry and the ‘volcanic factor’. Front. Endocrinol. 4, 65 (2013).

    Google Scholar 

  129. 129.

    Vigneri, R., Malandrino, P., Gianì, F., Russo, M. & Vigneri, P. Heavy metals in the volcanic environment and thyroid cancer. Mol. Cell. Endocrinol. 457, 73–80 (2017).

    CAS  PubMed  Google Scholar 

  130. 130.

    Tchounwou, P. B., Yedjou, C. G., Patlolla, A. K. & Sutton, D. J. Heavy metal toxicity and the environment. Experientia Suppl. 101, 133–164 (2012).

    Google Scholar 

  131. 131.

    Ferlay J., et al Global cancer observatory: cancer today. Available at: https://gco.iarc.fr/. (Accessed: August 2019).

Download references

Author information

Affiliations

Authors

Contributions

The authors contributed equally to all aspects of the article.

Corresponding author

Correspondence to Sanziana A. Roman.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Peer review information

Nature Reviews Endocrinology thanks J. Brito, D. Carneiro-Pla and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Glossary

Papillary thyroid cancer

(PTC). The most common type of thyroid cancer, which tends to grow slowly and can spread to lymph nodes in the neck.

Thyroid nodules

Abnormal growths of thyroid cells that can form a mass within the thyroid.

Betel quid

A mix of betel nut, tobacco and spices, which is used like chewing tobacco.

Fine-needle aspiration

A biopsy procedure in which a thin needle is used collect a sample of tissue for evaluation.

Occult thyroid cancers

Thyroid cancers that are not detectable by contemporary clinical methods.

Microcarcinomas

Tumours less than or equal to 1 cm in size.

Anaplastic thyroid cancer

A rare but aggressive type of thyroid cancer.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Kim, J., Gosnell, J.E. & Roman, S.A. Geographic influences in the global rise of thyroid cancer. Nat Rev Endocrinol 16, 17–29 (2020). https://doi.org/10.1038/s41574-019-0263-x

Download citation

Further reading

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing