Abstract
Purpose
Thyroid cancer has a higher incidence in women than in men, and it has been hypothesized that hormonal factors may explain such disparity. We performed a meta-analysis of observational prospective studies to investigate the association between menstrual and reproductive variables and exogenous hormone use and the risk of thyroid cancer among women.
Methods
We calculated summary relative risks and 95 % confidence intervals (95 % CI) using random effect models.
Results
Overall, 5,434 thyroid cancer cases from twenty-four papers were included. Increasing age at first pregnancy/birth (SRR 1.56, 95 % CI 1.01–2.42) and hysterectomy (SRR 1.43, 95 % CI 1.15–1.78) were associated with thyroid cancer risk. Women that were in menopause at enrolment had a reduced thyroid cancer risk (SRR 0.79, 95 % CI 0.62–1.01). No other menstrual, reproductive, and hormonal variable was associated with thyroid cancer risk.
Conclusions
Menstrual and reproductive factors may play a role in the etiology of thyroid cancer, possibly through the mediation of estrogen receptors.
Similar content being viewed by others
Abbreviations
- 95 % CI:
-
95 % confidence intervals
- ER:
-
Estrogen receptors
- SRR:
-
Summary relative risk
- OC:
-
Oral contraceptives
- HRT:
-
Hormone replacement therapy
References
Kilfoy BA, Zheng T, Holford TR, Han X, Ward MH, Sjodin A, Zhang Y, Bai Y, Zhu C, Guo GL, Rothman N, Zhang Y (2009) International patterns and trends in thyroid cancer incidence, 1973–2002. Cancer Causes Control 20(5):525–531
Davies L, Welch HG (2014) Current thyroid cancer trends in the United States. JAMA Otolaryngol Head Neck Surg 140(4):317–322
Li N, Du XL, Reitzel LR, Xu L, Sturgis EM (2013) 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
Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D (2011) Global cancer statistics. CA Cancer J Clin 61(2):69–90
Rahbari R, Zhang L, Kebebew E (2010) Thyroid cancer gender disparity. Future Oncol 6(11):1771–1779
Zhao ZG, Guo XG, Ba CX, Wang W, Yang YY, Wang J, Cao HY (2012) Overweight, obesity and thyroid cancer risk: a meta-analysis of cohort studies. J Int Med Res 40(6):2041–2050
Bjoro T, Holmen J, Krüger O, Midthjell K, Hunstad K, Schreiner T, Sandnes L, Brochmann H (2000) Prevalence of thyroid disease, thyroid dysfunction and thyroid peroxidase antibodies in a large, unselected population. The Health Study of Nord-Trondelag (HUNT). Eur J Endocrinol 143(5):639–647
Vanderpump MP (2011) The epidemiology of thyroid disease. Br Med Bull 99:39–51
Balasubramaniam S, Ron E, Gridley G, Schneider AB, Brenner AV (2012) 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(8):2661–2669
Fioretti F, Tavani A, Gallus S, Franceschi S, Negri E, La Vecchia C (1999) Case–control study of thyroid cancer in Northern Italy: attributable risk. Int J Epidemiol 28(4):626–630
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
McTiernan AM, Weiss NS, Daling JR (1984) Incidence of thyroid cancer in women in relation to reproductive and hormonal factors. Am J Epidemiol 120(3):423–435
Manole D, Schildknecht B, Gosnell B, Adams E, Derwahl M (2001) Estrogen promotes growth of human thyroid tumor cells by different molecular mechanisms. J Clin Endocrinol Metab 86(3):1072–1077
Kumar A, Klinge CM, Goldstein RE (2010) Estradiol-induced proliferation of papillary and follicular thyroid cancer cells is mediated by estrogen receptors alpha and beta. Int J Oncol 36(5):1067–1080
Negri E, Dal Maso L, Ron E, La Vecchia C, Mark SD, Preston-Martin S, McTiernan A, Kolonel L, Yoshimoto Y, Jin F, Wingren G, Rosaria Galanti M et al (1999) A pooled analysis of case–control studies of thyroid cancer. II. Menstrual and reproductive factors. Cancer Causes Control 10(2):143–155
La Vecchia C, Ron E, Franceschi S, Dal Maso L, Mark SD, Chatenoud L, Braga C, Preston-Martin S, McTiernan A, Kolonel L, Mabuchi K, Jin F et al (1999) A pooled analysis of case–control studies of thyroid cancer. III. Oral contraceptives, menopausal replacement therapy and other female hormones. Cancer Causes Control 10(2):157–166
Wong EY, Ray R, Gao DL, Wernli KJ, Li W, Fitzgibbons ED, Feng Z, Thomas DB, Checkoway H (2006) Reproductive history, occupational exposures, and thyroid cancer risk among women textile workers in Shanghai, China. Int Arch Occup Environ Health 79(3):251–258
Pham TM, Fujino Y, Mikami H, Okamoto N, Hoshiyama Y, Tamakoshi A, Matsuda S, Yoshimura T (2009) Japan Collaborative Cohort Study group. reproductive and menstrual factors and thyroid cancer among Japanese women: the Japan Collaborative Cohort Study. J Womens Health (Larchmt) 18(3):331–335
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
Kabat GC, Kim MY, Wactawski-Wende J, Lane D, Wassertheil-Smoller S, Rohan TE (2012) Menstrual and reproductive factors, exogenous hormone use, and risk of thyroid carcinoma in postmenopausal women. Cancer Causes Control 23(12):2031–2040
Stroup DF, Berlin JA, Morton SC, Olkin I, Williamson GD, Rennie D et al (2000) Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis of observational studies in epidemiology (MOOSE) group. JAMA 283(15):2008–2012
Meinhold CL, Ron E, Schonfeld SJ, Alexander BH, Freedman DM, Linet MS (2010) Berrington de González A. Nonradiation risk factors for thyroid cancer in the US Radiologic Technologists Study. Am J Epidemiol 171(2):242–252
Greenland S (1987) Quantitative methods in the review of epidemiologic literature. Epidemiol Rev 9:1–30
van Houwelingen HC, Arends LR, Stijnen T (2002) Advanced methods in meta-analysis: multivariate approach and meta-regression. Stat Med 21(4):589–624
Higgins JP, Thompson SG (2002) Quantifying heterogeneity in a meta-analysis. Stat Med 21(11):1539–1558
von Elm E, Altman DG, Egger M, Pocock SJ, Gøtzsche PC (2008) Vandenbroucke JP; STROBE Initiative. The strengthening the reporting of observational studies in epidemiology (STROBE) statement: guidelines for reporting observational studies. J Clin Epidemiol 61(4):344–349
Macaskill P, Walter SD, Irwig L (2001) A comparison of methods to detect publication bias in meta-analysis. Stat Med 20(4):641–654
Yli-Kuha AN, Gissler M, Klemetti R, Luoto R, Hemminki E (2012) Cancer morbidity in a cohort of 9175 Finnish women treated for infertility. Hum Reprod 27(4):1149–1155
Källén B, Finnström O, Lindam A, Nilsson E, Nygren KG, Olausson PO (2011) Malignancies among women who gave birth after in vitro fertilization. Hum Reprod 26(1):253–258
Zamora-Ros R, Rinaldi S, Biessy C, Tjønneland A, Halkjaer J, Fournier A, Boutron-Ruault MC, Mesrine S, Tikk K, Fortner RT, Boeing H, Förster J, et al. (2014) Reproductive and menstrual factors and risk of differentiated thyroid carcinoma: the EPIC study. Int J Cancer (Epub ahead of print)
Braganza MZ, Berrington de González A, Schonfeld SJ, Wentzensen N, Brenner AV, Kitahara CM (2014) Benign breast and gynecologic conditions, reproductive and hormonal factors, and risk of thyroid cancer. Cancer Prev Res (Phila) 7(4):418–425
Sungwalee W, Vatanasapt P, Kamsa-Ard S, Suwanrungruang K, Promthet S (2013) Reproductive risk factors for thyroid cancer: a prospective cohort study in Khon Kaen, Thailand. Asian Pac J Cancer Prev 14(9):5153–5155
Schonfeld SJ, Ron E, Kitahara CM, Brenner A, Park Y, Sigurdson AJ, Schatzkin A, de González AB (2011) Hormonal and reproductive factors and risk of postmenopausal thyroid cancer in the NIH-AARP diet and health study. Cancer Epidemiol 35(6):e85–e90
Dorjgochoo T, Shu XO, Li HL, Qian HZ, Yang G, Cai H, Gao YT, Zheng W (2009) Use of oral contraceptives, intrauterine devices and tubal sterilization and cancer risk in a large prospective study, from 1996 to 2006. Int J Cancer 124(10):2442–2449
Rosenblatt KA, Gao DL, Ray RM, Nelson ZC, Wernli KJ, Li W, Thomas DB (2009) Oral contraceptives and the risk of all cancers combined and site-specific cancers in Shanghai. Cancer Causes Control 20(1):27–34
Hannibal CG, Jensen A, Sharif H, Kjaer SK (2008) Risk of thyroid cancer after exposure to fertility drugs: results from a large Danish cohort study. Hum Reprod 23(2):451–456
Rosenblatt KA, Gao DL, Ray RM, Rowland MR, Nelson ZC, Wernli KJ, Li W, Thomas DB (2006) Induced abortions and the risk of all cancers combined and site-specific cancers in Shanghai. Cancer Causes Control 17(10):1275–1280
Althuis MD, Scoccia B, Lamb EJ, Moghissi KS, Westhoff CL, Mabie JE, Brinton LA (2005) Melanoma, thyroid, cervical, and colon cancer risk after use of fertility drugs. Am J Obstet Gynecol 193(3 Pt 1):668–674
Navarro Silvera SA, Miller AB, Rohan TE (2005) Risk factors for thyroid cancer: a prospective cohort study. Int J Cancer 116(3):433–438
Neale RE, Darlington S, Murphy MF, Silcocks PB, Purdie DM, Talbäck M (2005) The effects of twins, parity and age at first birth on cancer risk in Swedish women. Twin Res Hum Genet 8(2):156–162
Luoto R, Grenman S, Salonen S, Pukkala E (2003) Increased risk of thyroid cancer among women with hysterectomies. Am J Obstet Gynecol 188(1):45–48
Modan B, Ron E, Lerner-Geva L, Blumstein T, Menczer J, Rabinovici J, Oelsner G, Freedman L, Mashiach S, Lunenfeld B (1998) Cancer incidence in a cohort of infertile women. Am J Epidemiol 147(11):1038–1042
Luoto R, Auvinen A, Pukkala E, Hakama M (1997) Hysterectomy and subsequent risk of cancer. Int J Epidemiol 26(3):476–483
Persson I, Yuen J, Bergkvist L, Schairer C (1996) Cancer incidence and mortality in women receiving estrogen and estrogen-progestin replacement therapy–long-term follow-up of a Swedish cohort. Int J Cancer 67(3):327–332
Galanti MR, Lambe M, Ekbom A, Sparén P, Pettersson B (1995) Parity and risk of thyroid cancer: a nested case–control study of a nationwide Swedish cohort. Cancer Causes Control 6(1):37–44
Akslen LA, Nilssen S, Kvåle G (1992) Reproductive factors and risk of thyroid cancer. A prospective study of 63,090 women from Norway. Br J Cancer 65(5):772–774
Brinton LA, Melton LJ 3rd, Malkasian GD Jr, Bond A, Hoover R (1989) Cancer risk after evaluation for infertility. Am J Epidemiol 129(4):712–722
Santin AP, Furlanetto TW (2011) Role of estrogen in thyroid function and growth regulation. J Thyroid Res 2011:875125
Huang Y, Dong W, Li J, Zhang H, Shan Z, Teng W (2014) Differential expression patterns and clinical significance of estrogen receptor-α and β in papillary thyroid carcinoma. BMC Cancer 29(14):383
Fleury Y, Van Melle G, Woringer V, Gaillard RC, Portmann L (2001) Sex-dependent variations and timing of thyroid growth during puberty. J Clin Endocrinol Metab 86(2):750–754
Weber G, Vigone MC, Stroppa L, Chiumello G (2003) Thyroid function and puberty. J Pediatr Endocrinol Metab 16(Suppl 2):253–257
Grün JP, Meuris S, De Nayer P, Glinoer D (1997) The thyrotrophic role of human chorionic gonadotrophin (hCG) in the early stages of twin (versus single) pregnancies. Clin Endocrinol (Oxf) 46(6):719–725
Leux C, Guénel P (2010) Risk factors of thyroid tumors: role of environmental and occupational exposures to chemical pollutants. Rev Epidemiol Sante Publique 58(5):359–367
Kim MH, Park YR, Lim DJ, Yoon KH, Kang MI, Cha BY, Lee KW, Son HY (2010) The relationship between thyroid nodules and uterine fibroids. Endocr J 57(7):615–621
Pellegriti G, Frasca F, Regalbuto C, Squatrito S, Vigneri R (2013) Worldwide increasing incidence of thyroid cancer: update on epidemiology and risk factors. J Cancer Epidemiol 2013:965212
Dieringer P, Klass EM, Caine B, Smith-Gagen J (2015) Associations between body mass and papillary thyroid cancer stage and tumor size: a population-based study. J Cancer Res Clin Oncol 141(1):93–98
Acknowledgments
This research did not receive any specific grant from any funding agency in the public, commercial, or not-for-profit sector.
Conflict of interest
The authors declare they have no conflicts of interest to disclose.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Caini, S., Gibelli, B., Palli, D. et al. Menstrual and reproductive history and use of exogenous sex hormones and risk of thyroid cancer among women: a meta-analysis of prospective studies. Cancer Causes Control 26, 511–518 (2015). https://doi.org/10.1007/s10552-015-0546-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10552-015-0546-z