Abstract
Purpose
Exceptionally high incidence rates of thyroid cancer have been observed in New Caledonia, particularly in Melanesian women, but familial aggregation of thyroid diseases in this population is unknown. We study the association between family history of malignant or benign thyroid diseases and non-medullary thyroid cancer in this country.
Methods
We conducted a population-based case–control study including 332 cases with papillary or follicular carcinoma diagnosed in 1993–1999 and 412 controls, matched by sex and 5-year age-group.
Results
Thyroid cancer was associated with a history of thyroid cancer in first-degree relatives (odds ratio (OR), 3.2; 95 % CI, 1.6–6.2) and with a family history of multinodular goiter (OR, 3.6; 95 % CI, 1.9–7.0). The ORs did not change by age at diagnosis and with the number of affected relatives. The study provides evidence that the familial component of thyroid cancer is particularly strong in men. Thyroid cancer was not associated with a family history of thyroid diseases in Melanesians from the Loyalty Islands, the area with the highest incidence rates for thyroid cancer, possibly indicating a high frequency of genetic susceptibility variants and lack of genetic variation in this population subgroup.
Conclusion
Overall our findings confirm an elevated risk of thyroid cancer in individuals with a family history of malignant or benign thyroid diseases, particularly in Melanesians where familial aggregation of thyroid cancer had never been investigated before. The study of genetic variants in candidate susceptibility genes for thyroid cancer may help clarifying the absence of an association in the subgroup of Melanesians from the Loyalty Islands.
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Abbreviations
- CI:
-
Confidence interval
- FRR:
-
Familial relative risk
- OR:
-
Odds ratio
- NMTC:
-
Non-medullary thyroid cancer
- SIR:
-
Standardized incidence ratio
References
Ferlay J, Shin HR, Bray F, Forman D, Mathers C, Parkin DM (2010) Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int J Cancer 127(12):2893–2917
Ferlay J, Parkin DM, Steliarova-Foucher E (2010) Estimates of cancer incidence and mortality in Europe in 2008. Eur J Cancer 46(4):765–781
Cancer incidence in five continents, vol VIII. IARC Science Publication no. 155, pp 1–781 (2002)
Kent WD, Hall SF, Isotalo PA, Houlden RL, George RL, Groome PA (2007) Increased incidence of differentiated thyroid carcinoma and detection of subclinical disease. CMAJ 177(11):1357–1361
Liu S, Semenciw R, Ugnat AM, Mao Y (2001) Increasing thyroid cancer incidence in Canada, 1970–1996: time trends and age-period-cohort effects. Br J Cancer 85(9):1335–1339
Zheng T, Holford TR, Chen Y, Ma JZ, Flannery J, Liu W et al (1996) Time trend and age-period-cohort effect on incidence of thyroid cancer in Connecticut, 1935–1992. Int J Cancer 67(4):504–509
Davies L, Welch HG (2006) Increasing incidence of thyroid cancer in the United States, 1973–2002. JAMA 295(18):2164–2167
Smailyte G, Miseikyte-Kaubriene E, Kurtinaitis J (2006) Increasing thyroid cancer incidence in Lithuania in 1978–2003. BMC Cancer 6:284
Reynolds RM, Weir J, Stockton DL, Brewster DH, Sandeep TC, Strachan MW (2005) Changing trends in incidence and mortality of thyroid cancer in Scotland. Clin Endocrinol (Oxf) 62(2):156–162
Colonna M, Guizard AV, Schvartz C, Velten M, Raverdy N, Molinie F et al (2007) 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
Burgess JR, Tucker P (2006) Incidence trends for papillary thyroid carcinoma and their correlation with thyroid surgery and thyroid fine-needle aspirate cytology. Thyroid 16(1):47–53
Leenhardt L, Grosclaude P, Cherie-Challine L (2004) Increased incidence of thyroid carcinoma in France: a true epidemic or thyroid nodule management effects? Report from the French Thyroid Cancer Committee. Thyroid 14(12):1056–1060
Yu GP, Li JC, Branovan D, McCormick S, Schantz SP (2010) Thyroid cancer incidence and survival in the national cancer institute surveillance, epidemiology, and end results race/ethnicity groups. Thyroid 20(5):465–473
Enewold L, Zhu K, Ron E, Marrogi AJ, Stojadinovic A, Peoples GE et al (2009) Rising thyroid cancer incidence in the United States by demographic and tumor characteristics, 1980–2005. Cancer Epidemiol Biomarkers Prev 18(3):784–791
Truong T, Rougier Y, Dubourdieu D, Guihenneuc-Jouyaux C, Orsi L, Hemon D et al (2007) 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
Truong T, Orsi L, Dubourdieu D, Rougier Y, Hemon D, Guenel P (2005) Role of goiter and of menstrual and reproductive factors in thyroid cancer: a population-based case-control study in New Caledonia (South Pacific), a very high incidence area. Am J Epidemiol 161(11):1056–1065
Guignard R, Truong T, Rougier Y, Baron-Dubourdieu D, Guenel P (2007) Alcohol drinking, tobacco smoking, and anthropometric characteristics as risk factors for thyroid cancer: a countrywide case-control study in New Caledonia. Am J Epidemiol 166(10):1140–1149
Goldgar DE, Easton DF, Cannon-Albright LA, Skolnick MH (1994) Systematic population-based assessment of cancer risk in first-degree relatives of cancer probands. J Natl Cancer Inst 86(21):1600–1608
Hemminki K, Vaittinen P (1999) Familial cancers in a nationwide family cancer database: age distribution and prevalence. Eur J Cancer 35(7):1109–1117
Hemminki K, Eng C, Chen B (2005) Familial risks for nonmedullary thyroid cancer. J Clin Endocrinol Metab 90(10):5747–5753
Kerber RA, O’Brien E (2005) A cohort study of cancer risk in relation to family histories of cancer in the Utah population database. Cancer 103(9):1906–1915
Frich L, Glattre E, Akslen LA (2001) Familial occurrence of nonmedullary thyroid cancer: a population-based study of 5673 first-degree relatives of thyroid cancer patients from Norway. Cancer Epidemiol Biomarkers Prev 10(2):113–117
Hrafnkelsson J, Tulinius H, Jonasson JG, Sigvaldason H (2001) Familial non-medullary thyroid cancer in Iceland. J Med Genet 38(3):189–191
Galanti MR, Ekbom A, Grimelius L, Yuen J (1997) Parental cancer and risk of papillary and follicular thyroid carcinoma. Br J Cancer 75(3):451–456
Horn-Ross PL, Morris JS, Lee M, West DW, Whittemore AS, McDougall IR et al (2001) Iodine and thyroid cancer risk among women in a multiethnic population: the Bay Area Thyroid Cancer Study. Cancer Epidemiol Biomarkers Prev 10(9):979–985
Ron E, Kleinerman RA, LiVolsi VA, Fraumeni JF Jr (1991) Familial nonmedullary thyroid cancer. Oncology 48(4):309–311
Mack WJ, Preston-Martin S, Bernstein L, Qian D (2002) Lifestyle and other risk factors for thyroid cancer in Los Angeles County females. Ann Epidemiol 12(6):395–401
Memon A, Berrington De Gonzalez A, Luqmani Y, Suresh A (2004) Family history of benign thyroid disease and cancer and risk of thyroid cancer. Eur J Cancer 40(5):754–760
Brindel P, Doyon F, Bourgain C, Rachedi F, Boissin JL, Sebbag J et al (2010) Family history of thyroid cancer and the risk of differentiated thyroid cancer in French polynesia. Thyroid 20:393–400
Xu L, Li G, Wei Q, El-Naggar AK, Sturgis EM (2011) Family history of cancer and risk of sporadic differentiated thyroid carcinoma. Cancer 118(5):1228–1235
Adjadj E, Schlumberger M, de Vathaire F (2009) Germ-line DNA polymorphisms and susceptibility to differentiated thyroid cancer. Lancet Oncol 10(2):181–190
Gudmundsson J, Sulem P, Gudbjartsson DF, Jonasson JG, Sigurdsson A, Bergthorsson JT et al (2009) Common variants on 9q22.33 and 14q13.3 predispose to thyroid cancer in European populations. Nat Genet 41(4):460–464
R Development Core Team (2011) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN:3-900051-07-0. http://www.R-project.org
Friedlaender JS, Friedlaender FR, Reed FA, Kidd KK, Kidd JR, Chambers GK et al (2008) The genetic structure of Pacific Islanders. PLoS Genet 4(1):e19
Pal T, Vogl FD, Chappuis PO, Tsang R, Brierley J, Renard H et al (2001) Increased risk for nonmedullary thyroid cancer in the first degree relatives of prevalent cases of nonmedullary thyroid cancer: a hospital-based study. J Clin Endocrinol Metab 86(11):5307–5312
Leprat F, Bonichon F, Guyot M, Trouette H, Trojani M, Vergnot V et al (1999) Familial non-medullary thyroid carcinoma: pathology review in 27 affected cases from 13 French families. Clin Endocrinol (Oxf) 50(5):589–594
Loh KC (1997) Familial nonmedullary thyroid carcinoma: a meta-review of case series. Thyroid 7(1):107–113
Grossman RF, Tu SH, Duh QY, Siperstein AE, Novosolov F, Clark OH (1995) Familial nonmedullary thyroid cancer. An emerging entity that warrants aggressive treatment. Arch Surg 130(8):892–897; discussion 8–9
Lupoli G, Vitale G, Caraglia M, Fittipaldi MR, Abbruzzese A, Tagliaferri P et al (1999) Familial papillary thyroid microcarcinoma: a new clinical entity. Lancet 353(9153):637–639
Alsanea O, Wada N, Ain K, Wong M, Taylor K, Ituarte PH, et al. (2000) Is familial non-medullary thyroid carcinoma more aggressive than sporadic thyroid cancer? A multicenter series. Surgery 128(6):1043–1050; discussion 50–51
Uchino S, Noguchi S, Kawamoto H, Yamashita H, Watanabe S, Yamashita H et al (2002) Familial nonmedullary thyroid carcinoma characterized by multifocality and a high recurrence rate in a large study population. World J Surg 26(8):897–902
Sippel RS, Caron NR, Clark OH (2007) An evidence-based approach to familial nonmedullary thyroid cancer: screening, clinical management, and follow-up. World J Surg 31(5):924–933
Triponez F, Wong M, Sturgeon C, Caron N, Ginzinger DG, Segal MR et al (2006) Does familial non-medullary thyroid cancer adversely affect survival? World J Surg 30(5):787–793
Maxwell EL, Hall FT, Freeman JL (2004) Familial non-medullary thyroid cancer: a matched-case control study. Laryngoscope 114(12):2182–2186
Mack WJ, Preston-Martin S, Bernstein L, Qian D, Xiang M (1999) Reproductive and hormonal risk factors for thyroid cancer in Los Angeles County females. Cancer Epidemiol Biomarkers Prev 8(11):991–997
Horn-Ross PL, Canchola AJ, Ma H, Reynolds P, Bernstein L (2011) Hormonal factors and the risk of papillary thyroid cancer in the california teachers study cohort. Cancer Epidemiol Biomarkers Prev 20(8):1751–1759
Fagin JA (1997) Familial nonmedullary thyroid carcinoma—the case for genetic susceptibility. J Clin Endocrinol Metab 82(2):342–344
Burgess JR, Duffield A, Wilkinson SJ, Ware R, Greenaway TM, Percival J et al (1997) Two families with an autosomal dominant inheritance pattern for papillary carcinoma of the thyroid. J Clin Endocrinol Metab 82(2):345–348
Bignell GR, Canzian F, Shayeghi M, Stark M, Shugart YY, Biggs P et al (1997) Familial nontoxic multinodular thyroid goiter locus maps to chromosome 14q but does not account for familial nonmedullary thyroid cancer. Am J Hum Genet 61(5):1123–1130
Canzian F, Amati P, Harach HR, Kraimps JL, Lesueur F, Barbier J et al (1998) A gene predisposing to familial thyroid tumors with cell oxyphilia maps to chromosome 19p13.2. Am J Hum Genet 63(6):1743–1748
Malchoff CD, Sarfarazi M, Tendler B, Forouhar F, Whalen G, Joshi V et al (2000) Papillary thyroid carcinoma associated with papillary renal neoplasia: genetic linkage analysis of a distinct heritable tumor syndrome. J Clin Endocrinol Metab 85(5):1758–1764
McKay JD, Lesueur F, Jonard L, Pastore A, Williamson J, Hoffman L et al (2001) Localization of a susceptibility gene for familial nonmedullary thyroid carcinoma to chromosome 2q21. Am J Hum Genet 69(2):440–446
He H, Nagy R, Liyanarachchi S, Jiao H, Li W, Suster S et al (2009) A susceptibility locus for papillary thyroid carcinoma on chromosome 8q24. Cancer Res 69(2):625–631
Lesueur F, Stark M, Tocco T, Ayadi H, Delisle MJ, Goldgar DE et al (1999) Genetic heterogeneity in familial nonmedullary thyroid carcinoma: exclusion of linkage to RET, MNG1, and TCO in 56 families. NMTC Consortium. J Clin Endocrinol Metab 84(6):2157–2162
Bevan S, Pal T, Greenberg CR, Green H, Wixey J, Bignell G et al (2001) A comprehensive analysis of MNG1, TCO1, fPTC, PTEN, TSHR, and TRKA in familial nonmedullary thyroid cancer: confirmation of linkage to TCO1. J Clin Endocrinol Metab 86(8):3701–3704
Cavaco BM, Batista PF, Martins C, Banito A, do Rosario F, Limbert E, et al. (2008) 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(1):207–215
Truong T, Baron-Dubourdieu D, Rougier Y, Guenel P (2010) Role of dietary iodine and cruciferous vegetables in thyroid cancer: a countrywide case-control study in New Caledonia. Cancer Causes Control 21(8):1183–1192
Hemminki K, Li X (2002) Gender effects in familial cancer. Int J Cancer 102(2):184–187
Wingren G, Hatschek T, Axelson O (1993) Determinants of papillary cancer of the thyroid. Am J Epidemiol 138(7):482–491
Paoff K, Preston-Martin S, Mack WJ, Monroe K (1995) A case-control study of maternal risk factors for thyroid cancer in young women (California, United States). Cancer Causes Control 6(5):389–397
Kolonel LN, Hankin JH, Wilkens LR, Fukunaga FH, Hinds MW (1990) An epidemiologic study of thyroid cancer in Hawaii. Cancer Causes Control 1(3):223–234
Preston-Martin S, Jin F, Duda MJ, Mack WJ (1993) A case-control study of thyroid cancer in women under age 55 in Shanghai (People’s Republic of China). Cancer Causes Control 4(5):431–440
D’Avanzo B, La Vecchia C, Franceschi S, Negri E, Talamini R (1995) History of thyroid diseases and subsequent thyroid cancer risk. Cancer Epidemiol Biomarkers Prev 4(3):193–199
Hallquist A, Hardell L, Degerman A, Boquist L (1994) Thyroid cancer: reproductive factors, previous diseases, drug intake, family history and diet. A case-control study. Eur J Cancer Prev 3(6):481–488
Sokic SI, Adanja BJ, Vlajinac HD, Jankovic RR, Marinkovic JP, Zivaljevic VR (1994) Risk factors for thyroid cancer. Neoplasma 41(6):371–374
Iribarren C, Haselkorn T, Tekawa IS, Friedman GD (2001) Cohort study of thyroid cancer in a San Francisco Bay area population. Int J Cancer 93(5):745–750
Levi F, Franceschi S, La Vecchia C, Negri E, Gulie C, Duruz G et al (1991) Previous thyroid disease and risk of thyroid cancer in Switzerland. Eur J Cancer 27(1):85–88
Franceschi S, Preston-Martin S, Dal Maso L, Negri E, La Vecchia C, Mack WJ, et al. (1999) A pooled analysis of case-control studies of thyroid cancer. IV. Benign thyroid diseases. Cancer Causes Control 10(6):583–595
Kerber RA, Slattery ML (1997) Comparison of self-reported and database-linked family history of cancer data in a case-control study. Am J Epidemiol 146(3):244–248
Soegaard M, Jensen A, Frederiksen K, Hogdall E, Hogdall C, Blaakaer J et al (2008) Accuracy of self-reported family history of cancer in a large case-control study of ovarian cancer. Cancer Causes Control 19(5):469–479
Mitchell RJ, Brewster D, Campbell H, Porteous ME, Wyllie AH, Bird CC et al (2004) Accuracy of reporting of family history of colorectal cancer. Gut 53(2):291–295
Acknowledgments
This study was supported by grants from the “Fondation de France,” the “Association pour la Recherche contre le Cancer,” and the “Agence Française de Sécurité Sanitaire de l’Environnement et du Travail (AFSSET).” The authors wish to thank Dr Jean-Paul Grangeon (Direction des Affaires Sanitaires et Sociales Nouvelle-Calédonie) as well as the Provincial Health Authorities (DPASS Sud, DPASS Nord, DPASS Îles) for their support during data collection. They are particularly grateful to Michèle Reynier who coordinated the interviews of study subjects across New Caledonia.
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The authors declare that they have no conflict of interest.
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Leux, C., Truong, T., Petit, C. et al. Family history of malignant and benign thyroid diseases and risk of thyroid cancer: a population-based case–control study in New Caledonia. Cancer Causes Control 23, 745–755 (2012). https://doi.org/10.1007/s10552-012-9944-7
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DOI: https://doi.org/10.1007/s10552-012-9944-7