BioMed Research International

BioMed Research International / 2015 / Article
Special Issue

Optimal Use of Biomarkers in Oncology

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Review Article | Open Access

Volume 2015 |Article ID 103515 | 10 pages | https://doi.org/10.1155/2015/103515

Reproductive Factors but Not Hormonal Factors Associated with Thyroid Cancer Risk: A Systematic Review and Meta-Analysis

Academic Editor: Ondrej Topolcan
Received04 Oct 2014
Accepted16 Mar 2015
Published03 Aug 2015

Abstract

Many studies have investigated the association between hormonal and reproductive factors and thyroid cancer risk but provided contradictory and inconclusive findings. This review was aimed at precisely estimating this association by pooling all available epidemiological studies. 25 independent studies were retrieved after a comprehensive literature search in databases of PubMed and Embase. Overall, common hormonal factors including oral contraceptive and hormone replacement therapy did not alter the risk of thyroid cancer. Older age at menopause was associated with weakly increased risk of thyroid cancer in overall analysis (RR = 1.24, 95% CI 1.00–1.53, ); however, longer duration of breast feeding was related to moderately reduced risk of thyroid cancer, suggested by pooled analysis in all cohort studies (RR = 0.7, 95% CI 0.51–0.95, ). The pooled RR in hospital-based case-control studies implicated that parous women were more susceptible to thyroid cancer than nulliparous women (RR = 2.30, 95% CI 1.31–4.04, ). The present meta-analysis suggests that older age at menopause and parity are risk factors for thyroid cancer, while longer duration of breast feeding plays a protective role against this cancer. Nevertheless, more relevant epidemiological studies are warranted to investigate roles of hormonal and reproductive factors in thyroid carcinogenesis.

1. Introduction

Thyroid cancer is the most common type of endocrine malignancy, which accounts for nearly 3% of all malignancies [1]. Despite low mortality rate, rates of local recurrence and distant metastases are high in thyroid cancer patients. The incidence of thyroid cancer has been increasing worldwide for the last five years, while the etiology remains largely unknown. Ionizing radiation is a well documented risk factor for thyroid cancer [2]. However, not all individuals exposed to radiation develop this disease, implicating some other unknown factors involved in thyroid carcinogenesis, such as hormone-related factors.

Gender discrepancy is well known in thyroid malignancies. Thyroid cancer occurs three times more frequently in women than in men, and the incidence decreases among postmenopausal women. It has been well established that female sex hormones, particularly estrogens, can influence the proliferation and invasion of thyroid cancer cells by recognizing corresponding hormonal receptors expressed in those cells, such as estrogen receptor alpha and beta [35]. It has been demonstrated that the secretion of thyroid stimulating hormone (TSH) increased during puberty, pregnancy, and oral contraceptive use [6]. Elevated TSH production can promote thyroid growth, while estrogens increase levels of TSH in human body [7]. Therefore, regulation between TSH and estrogens may play a critical role in the development of thyroid disease, thyroid malignancies in particular. Taken together, it can be hypothesized that some hormonal and reproductive factors may confer modifying effects on thyroid carcinogenesis by influencing the signaling of sex hormones and their receptors in thyroid gland. Many epidemiological studies have investigated roles of hormonal and reproductive factors in the development of thyroid cancer, for instance, oral contraceptive use, hormone replacement therapy, menstrual factors, and fertility status [832]. Nevertheless, the precise association has not yet been fully elucidated due to conflicting and inconclusive findings in previous studies. We performed this meta-analysis by pooling all currently published studies to obtain a better estimation and provide important insights into the etiology of thyroid cancer.

2. Materials and Methods

2.1. Search Strategy

We searched studies on the association between hormonal and reproductive factors and thyroid cancer risk in PubMed and Embase databases from their inception up to September 10, 2014, using the following items: thyroid cancer, or thyroid carcinoma; and oral contraceptive, hormone replacement therapy, reproductive factors, menstrual factors, age at menarche, age at first birth, menopausal status, age at menopause, parity, pregnancy, reproductive history, or breast feeding; and incidence, or risk factor. References of relevant studies were also screened for additional papers. If studies were duplicated, only the most complete study was included.

2.2. Inclusion Criteria

The included studies must conform to the following inclusion criteria: (1) studies on the association of hormonal and reproductive factors with thyroid cancer risk; (2) cohort or case-control studies; (3) publications presenting odds ratios (ORs), relative risks (RRs), or hazard ratios (HRs) with 95% confidence intervals (95% CIs). Studies not associated with hormonal and reproductive factors and thyroid cancer risk, case-only, animal research, case reports, and duplicated studies were all excluded.

2.3. Data Extraction

Two investigators independently extracted data from each study by use of the following terms: name of first author, year of publication, study design, country of origins, sample size, study period, matching or adjusted factors, and RRs or HRs or ORs with 95% CIs for the estimation of thyroid cancer risk related to hormonal and reproductive factors. Disagreements were solved by discussion.

2.4. Statistical Analysis

Roles of hormonal and reproductive factors in thyroid cancer risk were assessed by calculating pooled RRs with 95% CIs by use of STATA 12.0 software (StataCorp, College Station, TX, USA). was suggested to be statistically significant. The between-study heterogeneity was estimated by Cochran’s and tests, and and implicated obvious between-study heterogeneity [33, 34]. The random-effects model was used when the between-study heterogeneity was significant [35]; otherwise, the fixed-effects model was adopted [36]. Stratified analysis by study design (cohort studies, population-based case-control studies, and hospital-based case-control studies) was also performed. Sensitivity analysis by omission of each study was conducted for further analysis. Publication bias risk was evaluated by both Begg’s funnel plots and Egger’s test [37, 38].

3. Results

3.1. Identification and Characteristics of Studies Included into the Meta-Analysis

112 studies were retrieved after a comprehensive literature in databases of PubMed and Embase. However, 87 studies were excluded due to irrelevance, reviews, animal research, and case reports. 25 independent studies on the association between hormonal and reproductive factors and thyroid cancer risk were finally included into our study [832]. Among the 25 studies, 13 were cohort studies, 10 were population-based case-control studies, and the other 2 were hospital-based case-control studies. Characteristics of all included studies were summarized in Table 1.


First authorYearOriginTimeStudy Hormonal or reproductive factorsAdjusted or matching criteria

Högnäs [13]2014Finland1974–2010Cohort studyParitySex

Zamora-Ros [31] 2015Europe1992–2009Cohort studyOral contraceptive, hormone replacement therapy, age at menarche, parity, age at first birth, menopausal status, age at menopause, breastfeeding status, and duration of breastfeedingSex, center, and age at recruitment

Braganza [8]2014USA1993–2009Cohort studyOral contraceptive, hormone replacement therapy, age at menarche, parity, age at first birth, and age at menopauseSex, education, race, marital status, family history of thyroid cancer, baseline body mass index, and smoking

Islami [15]2013Iran2003–2007PCCParityAge, sex, and neighborhood of residence

Kabat [16]2012USA1993–2011Cohort studyOral contraceptive, hormone replacement therapy, age at menarche, parity, age at first birth, age at menopause, and duration of breastfeedingSex, age, education, height, history of goiter/nodules, pack-years, and alcohol intake

Schonfeld [27]2011USA1995–2006Cohort studyOral contraceptive, hormone replacement therapy, age at menarche, parity, age at first birth, and age at menopauseSex, smoking status, baseline body mass index, race, alcohol consumption, and education

Horn-Ross [14]2011USA1995–2008Cohort studyOral contraceptive, hormone replacement therapy, age at menarche, parity, age at first birth, and menopausal statusSex, ethnicity, family history of thyroid cancer, time since last pregnancy, smoking, alcohol consumption, physical inactivity, height, adolescent cycle length, time to regular menstruation, and age at menarche

Meinhold [18]2010USA1983–2006Cohort studyOral contraceptive, hormone replacement therapy, age at menarche, parity, and menopausal statusSex, birth year, smoking status, body mass index, number of personal radiographs to the head or neck, and cumulative occupational radiation dose

Pham [23]2009Japan1988–1997Cohort studyHormone replacement therapy, age at menarche, parity, age at first birth, and age at menopauseSex, age at baseline, body mass index, tobacco smoking status, education level, history of diabetes, and study area

Dorjgochoo [10]2009China1996–2006Cohort studyOral contraceptiveSex, education, age at menarche, number of live births, cumulative breast feeding months, body mass index, exercised regularly in past 5 years, smoking, menopausal status, first-degree family history of cancer, and other contraceptive methods

Hannibal [12]2008Denmark1963–2000Cohort studyParity and age at first birthSex, parity, age at cohort entry and calendar year of cohort entry, and age at first live birth

Brindel [9] 2008France1981–2004PCCAge at menarche, parity, age at first birth, menopausal status, age at menopause, breastfeeding status, and duration of breastfeedingSex, educational level, height, body mass index, and interviewer

Wong [30]2006China1989–1998Cohort studyOral contraceptive, age at menarche, parity, age at first birth, age at menopause, breastfeeding status, and duration of breastfeedingSex, age, number of live births, and age at first live delivery

Truong [29]2005New Caledonia1993–1999PCCOral contraceptive, hormone replacement therapy, age at menarche, and paritySex, frequency, age, and residential area

Neale [21]2005Sweden1961–1996Cohort study Age at first birthSex, date of birth of the mother, parity, and age at first birth

Navarro Silvera [20]2005Canada1980–2000Cohort studyOral contraceptive, hormone replacement therapy, age at menarche, parity, age at first birth, and menopausal statusSex, age at first live birth, study center and randomization group, parity, and HRT use

Zivaljevic [32]2003Serbia1996–2000HCCParitySex, age, place of residence, and time of hospitalization

Negri [22]2002Mixed1974–1992PCCAge at menarche, parity, age at first birth, and menopausal statusSex, age, ethnicity, and study center

Memon [19]2002Middle East1981–1999PCCOral contraceptive, hormone replacement therapy, age at menarche, parity, age at first birth, and age at menopauseSex, year of birth, nationality, and district of residence.

Sakoda [26]2002USA1992–1998PCCAge at menarche, menopausal status, and age at menopauseSex, frequency, age, ethnicity, education level, history of goiter or nodules, history of radiation to the head or neck, and family history of proliferative thyroid disease

Rossing [24]2000USA1988–1994PCCAge at menarche, parity, age at first birth, and duration of breastfeedingSex, age, county of residence, race, and relative weight at age 10

Mack [17]1999USA1980–1983PCCAge at menarche, parity, age at first birth, menopausal status, breastfeeding status, and duration of breastfeedingSex, age, prior thyroid disease, and number of births

Takezaki [28] 1996Japan1988–1993HCCAge at menarche, parity, and age at first birthSex, age, and year of visit

Rossing [25]1998USA1988–1994PCCOral contraceptive and hormone replacement therapySex, age, county of residence, race, and relative weight at age 10

Galanti [11]1996Sweden and Norway1985–1993PCCOral contraceptive, hormone replacement therapy, parity, age at first birth, and age at menopauseSex, frequency, year and month of birth, type of menopause, and parity

PCC: population-based case-control studies; HCC: hospital-based case-control studies.
3.2. Association between Hormonal Factors and Thyroid Cancer Risk

The common hormonal factors including oral contraceptive and hormone replacement therapy did not modify the risk of thyroid cancer (for oral contraceptive: RR = 0.94, 95% CI 0.85–1.04, ; for hormone replacement therapy: RR = 1.04, 95% CI 0.91–1.19, ) (Table 2). Sensitivity analysis by sequential omission of each study confirmed the findings (data not shown).


ComparisonsaRRb95% CI value Tests for heterogeneity
(%)

All
 Oral contraceptive0.940.85–1.040.21536.00.095
 Hormone replacement therapy1.040.91–1.190.52700.520
 Age at menarche 1.080.97–1.190.14200.486
 Parity 1.100.94–1.280.23461.2<0.001
 Age at first birth 1.070.95–2.200.25514.80.281
 Menopausal status 0.960.79–1.180.7274.90.394
 Age at menopause1.241.00–1.530.04926.40.201
 Duration of breast feeding0.840.65–1.080.17838.30.150
 Breast feeding 0.840.69–1.020.0804.90.368
Cohort studies
 Oral contraceptive0.960.86–1.070.44839.50.104
 Hormone replacement therapy1.050.91–1.200.51300.439
 Age at menarche 1.010.90–1.140.80816.10.299
 Parity 1.000.78–1.280.99370.6<0.001
 Age at first birth 1.040.92–1.180.53000.571
 Menopausal status 0.900.71–1.150.41826.60.252
 Age at menopause 1.31.04–1.630.0222.50.400
 Duration of breast feeding 0.700.51–0.950.02100.661
 Breast feeding 0.820.66–1.020.07800.442
PCC
 Oral contraceptive 0.890.73–1.080.24041.00.166
 Hormone replacement therapy 1.010.68–1.500.9626.00.363
 Age at menarche 1.281.04–1.570.96000.937
 Parity 1.000.93–1.070.96021.60.258
 Age at first birth 1.350.97–1.880.07242.30.123
 Menopausal status 1.100.78–1.570.57700.481
 Age at menopause 0.820.43–1.560.55444.00.147
 Duration of breast feeding 1.240.80–1.930.33228.20.248
 Breast feeding 0.920.60–1.410.69957.60.125
HCC
 Parity 2.301.31–4.040.00400.787

aRR: relative risk; b95% CI: 95% confidence interval; cP: the value of for pooled analysis; dP: the value of for heterogeneity analysis.

Stratified analysis by study design showed that no significant relationship was observed between hormonal factors and thyroid cancer risk in cohort studies and studies in population-based case-control design (Table 2). We failed to perform stratified analysis in hospital-based case-control studies because of insufficient published studies.

3.3. Association between Reproductive Factors and Thyroid Cancer Risk

The pooled RRs revealed that older age at menopause was associated with weakly increased risk of thyroid cancer in overall analysis (RR = 1.24, 95% CI 1.00–1.53, ) (Table 2; Figure 1), whereas longer duration of breast feeding was related to moderately reduced risk of thyroid cancer in cohort studies (RR = 0.7, 95% CI 0.51–0.95, ) (Table 2; Figure 2). Stratified analysis in hospital-based case-control studies showed that more parity could increase the risk of thyroid cancer (RR = 2.30, 95% CI 1.31–4.04, ) (Table 2; Figure 3). No significant relationship was observed between thyroid cancer risk and other common reproductive factors (Table 2). Sensitivity analysis did not materially alter the pooled results (data not shown).

3.4. Heterogeneity Analysis and Publication Bias Risk

No significant between-study heterogeneity was found in most comparisons of overall and stratified analyses, except for the estimation of parity’s effect on thyroid cancer risk (, ). Stratified analysis by study design suggested that the main source of between-study heterogeneity resulted from studies in cohort design (, ).

As suggested by Begg’s funnel plots and Egger’s test, there was no significant publication bias under all comparisons in the present meta-analysis (data not shown).

4. Discussion

Hormonal and reproductive factors have been implicated in the development of thyroid cancer, but the precise association and underlying molecular mechanisms have not yet been fully understood. A previous pooled analysis has investigated the association between female reproductive factors and thyroid cancer risk [39]. Unfortunately, only 17 epidemiological studies are included into the meta-analysis, which shows weak and equivocal association between some hormonal and menstrual cycle factors and thyroid cancer risk [39]. The present meta-analysis was based on 25 epidemiological studies on the association between hormonal and reproductive factors and thyroid cancer risk. No significant association was observed between thyroid cancer risk and common hormonal factors including oral contraceptive and hormone replacement therapy. Interestingly, older age at menopause might increase the risk of thyroid cancer, as suggested by the pooled RR in overall analysis (RR = 1.24, 95% CI 1.00–1.53, ). Besides, longer duration of breast feeding was associated with moderately decreased risk of thyroid cancer, which had been suggested by the pooled analysis in cohort studies (RR = 0.7, 95% CI 0.51–0.95, ). Moreover, the pooled result in hospital-based case-control studies revealed that parous women were more susceptible to thyroid cancer than nulliparous women (RR = 2.30, 95% CI 1.31–4.04, ). Additionally, other reproductive factors including age at menarche, age at first birth, menopausal status, age at menopause, and breast feeding status did not modify the risk of thyroid cancer.

The risk of thyroid cancer in women increases at the time of puberty and declines after menopause [7, 40], supporting the hypothesis that menstrual cycle factors are involved in thyroid carcinogenesis. Elevated risk of thyroid cancer was related to the menopausal status when compared with premenopausal status [9]. Nonetheless, no significant association between the menopausal status, age at first birth, age at menarche, and age at menopause and thyroid cancer risk was observed [16, 18, 23, 27, 31]. It was worthwhile to note that menopausal females due to surgical factors were more susceptible to thyroid cancer compared with natural menopause ones [31], which might reflect enhanced medical surveillance of women who underwent surgical interventions for gynecological diseases symptoms. Similarly, we failed to identify any appreciable relationship of menstrual factors with thyroid cancer susceptibility. The discrepancies and underlying mechanisms need to be further elucidated by more relevant studies in the future.

It has been well established that estrogen receptors are found in thyroid cancer tissue and confer effects on different molecular signaling pathways involved in the growth and function of thyroid [5, 41, 42]. Estrogens and estrogen receptors signals exert promoting effect on the growth of thyroid gland by enhancing levels of TSH [7]. A number of studies have suggested some hormonal related factors, for instance, oral contraceptive and hormone replacement therapy, which played different roles in the thyroid cancer risk [8, 23, 27, 31]. Oral contraceptive seemed to play a protective role against thyroid cancer while an increased risk of thyroid cancer was found with the use of hormone replacement therapy demonstrated by Zamora-Ros et al. [31]. Similar findings were elucidated in a Caucasian cohort study [27]. Conversely, no modifying effects of oral contraceptive and hormone replacement therapy on the development of thyroid cancer were in another independent cohort study [8, 23]. The contradictory findings may be attributed to different study design, use of contraceptive and hormone replacement therapy, ethnicity, and adjusted or matching criteria in individual epidemiological studies. Our study showed no appreciable roles of hormonal factors in thyroid carcinogenesis, as suggested by both overall analysis and stratified analysis according to study design. More future studies are warranted to further estimate the association between hormonal-related factors and thyroid cancer risk.

The effect of breastfeeding on thyroid cancer risk is still not clear. Kabat and colleagues demonstrated that duration of breastfeeding did not alter the susceptibility to thyroid cancer [16]. However, Mack et al. provided the evidence that longer duration of breastfeeding was negatively associated with the risk of thyroid cancer risk, suggesting a protective role of breastfeeding in thyroid carcinogenesis [17]. Similarly, the pooled RRs in all cohort studies implicated that longer duration of breast feeding was associated with moderately reduced risk of thyroid cancer. Nevertheless, there was no significant relationship between breastfeeding status and thyroid carcinogenesis in pooled analyses of total studies and population-based case-control ones. Thus, the moderate association might be a chance resulting from potential bias in the present meta-analysis. To better understand the role of breastfeeding status in the thyroid cancer development, more relevant studies with high quality are warranted.

The status of parity conferred diverse effects on thyroid cancer risk in different populations. A recent study by Braganza et al. showed that parous women were at an elevated risk of thyroid cancer, as suggested by a recent epidemiological study [8]. Interestingly, for any given level of parity, there was about twofold increased risk of thyroid cancer among women with the age at last pregnancy larger than 30 years [19]. Unlike the findings mentioned above, no appreciable association was suggested between parity and the susceptibility to thyroid cancer among a Caucasian population [27]. In the current meta-analysis, significantly positive association was only demonstrated in the pooled analysis of two hospital-based case-control studies. Although age seemed to influence roles of reproductive factors in thyroid carcinogenesis, we failed to find appreciable association for age at first birth, age at menarche, and age at menopause. In addition, the pooled results, particularly in hospital-based case-control studies, must be interpreted with caution due to limited sample size and insufficient statistical power in current research.

Age is a main confounding factor for the association between hormonal and reproductive factors and thyroid cancer risk [19]. We failed to perform stratified analysis by age or other confounding factors, such as dosage and usage of hormonal drugs, the reason of menopause, number of live births, outcome of first pregnancy, and history of miscarriage, because of unavailable information about these items in single studies. Consequently, the association between hormonal and reproductive factors and thyroid cancer risk should be further investigated in view of above-mentioned confounding factors.

5. Conclusions

The current meta-analysis suggests that older age at menopause and parity are associated with increased risk of thyroid cancer, while longer duration of breast feeding plays a protective role against this cancer. In addition, the precise association needs further investigation by more epidemiological studies with sufficient statistical power in the future.

Conflict of Interests

The authors declare no conflict of interests.

References

  1. L. S. Ward, “Thyroid tumors: are we unveiling the puzzle?” Endocrine-Related Cancer, vol. 21, no. 5, pp. E7–E8, 2014. View at: Publisher Site | Google Scholar
  2. E. Ron, “Cancer risks from medical radiation,” Health Physics, vol. 85, no. 1, pp. 47–59, 2003. View at: Publisher Site | Google Scholar
  3. M. Zane, V. Catalano, E. Scavo et al., “Estrogens and stem cells in thyroid cancer,” Frontiers in Endocrinology, vol. 5, article 124, 2014. View at: Publisher Site | Google Scholar
  4. G. G. Chen, A. C. Vlantis, Q. Zeng, and C. A. van Hasselt, “Regulation of cell growth by estrogen signaling and potential targets in thyroid cancer,” Current Cancer Drug Targets, vol. 8, no. 5, pp. 367–377, 2008. View at: Publisher Site | Google Scholar
  5. P. K. Chaudhuri and R. Prinz, “Estrogen receptor in normal and neoplastic human thyroid tissue,” American Journal of Otolaryngology, vol. 10, no. 5, pp. 322–326, 1989. View at: Publisher Site | Google Scholar
  6. E. D. Williams, “TSH and thyroid cancer,” Hormone and Metabolic Research. Supplement, vol. 23, pp. 72–75, 1990. View at: Google Scholar
  7. R. Tahboub and B. M. Arafah, “Sex steroids and the thyroid,” Best Practice and Research: Clinical Endocrinology and Metabolism, vol. 23, no. 6, pp. 769–780, 2009. View at: Publisher Site | Google Scholar
  8. M. Z. Braganza, A. B. de González, S. J. Schonfeld, N. Wentzensen, A. V. Brenner, and C. M. Kitahara, “Benign breast and gynecologic conditions, reproductive and hormonal factors, and risk of thyroid cancer,” Cancer Prevention Research, vol. 7, no. 4, pp. 418–425, 2014. View at: Publisher Site | Google Scholar
  9. P. Brindel, F. Doyon, F. Rachédi et al., “Menstrual and reproductive factors in the risk of differentiated thyroid carcinoma in native women in French Polynesia: a population-based case-control study,” American Journal of Epidemiology, vol. 167, no. 2, pp. 219–229, 2008. View at: Publisher Site | Google Scholar
  10. T. Dorjgochoo, X.-O. Shu, H.-L. Li et al., “Use of oral contraceptives, intrauterine devices and tubal sterilization and cancer risk in a large prospective study, from 1996 to 2006,” International Journal of Cancer, vol. 124, no. 10, pp. 2442–2449, 2009. View at: Publisher Site | Google Scholar
  11. M. R. Galanti, L. Hansson, E. Lund et al., “Reproductive history and cigarette smoking as risk factors for thyroid cancer in women: a population-based case-control study,” Cancer Epidemiology Biomarkers and Prevention, vol. 5, no. 6, pp. 425–431, 1996. View at: Google Scholar
  12. C. G. Hannibal, A. Jensen, H. Sharif, and S. K. Kjaer, “Risk of thyroid cancer after exposure to fertility drugs: results from a large Danish cohort study,” Human Reproduction, vol. 23, no. 2, pp. 451–456, 2008. View at: Publisher Site | Google Scholar
  13. E. Högnäs, A. Kauppila, E. Pukkala, and J. S. Tapanainen, “Cancer risk in women with 10 or more deliveries,” Obstetrics and Gynecology, vol. 123, no. 4, pp. 811–816, 2014. View at: Publisher Site | Google Scholar
  14. P. L. Horn-Ross, A. J. Canchola, H. Ma, P. Reynolds, and L. Bernstein, “Hormonal factors and the risk of papillary thyroid cancer in the California teachers study cohort,” Cancer Epidemiology Biomarkers and Prevention, vol. 20, no. 8, pp. 1751–1759, 2011. View at: Publisher Site | Google Scholar
  15. F. Islami, Y. Cao, F. Kamangar et al., “Reproductive factors and risk of esophageal squamous cell carcinoma in northern Iran: a case-control study in a high-risk area and literature review,” European Journal of Cancer Prevention, vol. 22, no. 5, pp. 461–466, 2013. View at: Publisher Site | Google Scholar
  16. G. C. Kabat, M. Y. Kim, J. Wactawski-Wende, D. Lane, S. Wassertheil-Smoller, and T. E. Rohan, “Menstrual and reproductive factors, exogenous hormone use, and risk of thyroid carcinoma in postmenopausal women,” Cancer Causes and Control, vol. 23, no. 12, pp. 2031–2040, 2012. View at: Publisher Site | Google Scholar
  17. W. J. Mack, S. Preston-Martin, L. Bernstein, D. Qian, and M. Xiang, “Reproductive and hormonal risk factors for thyroid cancer in Los Angeles County females,” Cancer Epidemiology Biomarkers and Prevention, vol. 8, no. 11, pp. 991–997, 1999. View at: Google Scholar
  18. C. L. Meinhold, E. Ron, S. J. Schonfeld et al., “Nonradiation risk factors for thyroid cancer in the US radiologic technologists study,” American Journal of Epidemiology, vol. 171, no. 2, pp. 242–252, 2010. View at: Publisher Site | Google Scholar
  19. A. Memon, M. Darif, K. Al-Saleh, and A. Suresh, “Epidemiology of reproductive and hormonal factors in thyroid cancer: Evidence from a case-control study in the Middle East,” International Journal of Cancer, vol. 97, no. 1, pp. 82–89, 2002. View at: Publisher Site | Google Scholar
  20. S. A. Navarro Silvera, A. B. Miller, and T. E. Rohan, “Risk factors for thyroid cancer: a prospective cohort study,” International Journal of Cancer, vol. 116, no. 3, pp. 433–438, 2005. View at: Publisher Site | Google Scholar
  21. R. E. Neale, S. Darlington, M. F. G. Murphy, P. B. S. Silcocks, D. M. Purdie, and M. Talbäck, “The effects of twins, parity and age at first birth on cancer risk in Swedish women,” Twin Research and Human Genetics, vol. 8, no. 2, pp. 156–162, 2005. View at: Publisher Site | Google Scholar
  22. E. Negri, E. Ron, S. Franceschi et al., “Risk factors for medullary thyroid carcinoma: a pooled analysis,” Cancer Causes and Control, vol. 13, no. 4, pp. 365–372, 2002. View at: Publisher Site | Google Scholar
  23. T.-M. Pham, Y. Fujino, H. Mikami et al., “Reproductive and menstrual factors and thyroid cancer among Japanese women: the Japan collaborative cohort study,” Journal of Women's Health, vol. 18, no. 3, pp. 331–335, 2009. View at: Publisher Site | Google Scholar
  24. M. A. Rossing, L. F. Voigt, K. G. Wicklund, and J. R. Daling, “Reproductive factors and risk of papillary thyroid cancer in women,” The American Journal of Epidemiology, vol. 151, no. 8, pp. 765–772, 2000. View at: Publisher Site | Google Scholar
  25. M. A. Rossing, L. F. Voigt, K. G. Wicklund, M. Williams, and J. R. Daling, “Use of exogenous hormones and risk of papillary thyroid cancer (Washington, United States),” Cancer Causes and Control, vol. 9, no. 3, pp. 341–349, 1998. View at: Publisher Site | Google Scholar
  26. L. C. Sakoda and P. L. Horn-Ross, “Reproductive and menstrual history and papillary thyroid cancer risk: the San Francisco Bay Area thyroid cancer study,” Cancer Epidemiology Biomarkers and Prevention, vol. 11, no. 1, pp. 51–57, 2002. View at: Google Scholar
  27. S. J. Schonfeld, E. Ron, C. M. Kitahara et al., “Hormonal and reproductive factors and risk of postmenopausal thyroid cancer in the NIH-AARP Diet and Health Study,” Cancer Epidemiology, vol. 35, no. 6, pp. e85–e90, 2011. View at: Publisher Site | Google Scholar
  28. T. Takezaki, K. Hirose, M. Inoue et al., “Risk factors of thyroid cancer among women in Tokai, Japan,” Journal of Epidemiology, vol. 6, no. 3, pp. 140–147, 1996. View at: Publisher Site | Google Scholar
  29. T. Truong, L. Orsi, D. Dubourdieu, Y. Rougier, D. Hémon, and P. Guénel, “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,” The American Journal of Epidemiology, vol. 161, no. 11, pp. 1056–1065, 2005. View at: Publisher Site | Google Scholar
  30. E. Y. Wong, R. Ray, D. L. Gao et al., “Reproductive history, occupational exposures, and thyroid cancer risk among women textile workers in Shanghai, China,” International Archives of Occupational and Environmental Health, vol. 79, no. 3, pp. 251–258, 2006. View at: Publisher Site | Google Scholar
  31. R. Zamora-Ros, S. Rinaldi, C. Biessy et al., “Reproductive and menstrual factors and risk of differentiated thyroid carcinoma: the EPIC study,” International Journal of Cancer, vol. 136, no. 5, pp. 1218–1227, 2015. View at: Publisher Site | Google Scholar
  32. V. Zivaljevic, H. Vlajinac, R. Jankovic et al., “Case-control study of female thyroid cancer—menstrual, reproductive and hormonal factors,” European Journal of Cancer Prevention, vol. 12, no. 1, pp. 63–66, 2003. View at: Publisher Site | Google Scholar
  33. W. G. Cochran, “The comparison of percentages in matched samples,” Biometrika, vol. 37, pp. 256–266, 1950. View at: Publisher Site | Google Scholar | MathSciNet
  34. J. P. T. Higgins, S. G. Thompson, J. J. Deeks, and D. G. Altman, “Measuring inconsistency in meta-analyses,” British Medical Journal, vol. 327, no. 7414, pp. 557–560, 2003. View at: Publisher Site | Google Scholar
  35. R. DerSimonian and N. Laird, “Meta-analysis in clinical trials,” Controlled Clinical Trials, vol. 7, no. 3, pp. 177–188, 1986. View at: Publisher Site | Google Scholar
  36. N. Mantel and W. Haenszel, “Statistical aspects of the analysis of data from retrospective studies of disease,” Journal of the National Cancer Institute, vol. 22, no. 4, pp. 719–748, 1959. View at: Google Scholar
  37. M. Egger, G. D. Smith, M. Schneider, and C. Minder, “Bias in meta-analysis detected by a simple, graphical test,” British Medical Journal, vol. 315, no. 7109, pp. 629–634, 1997. View at: Publisher Site | Google Scholar
  38. A. E. Stuck, L. Z. Rubenstein, and D. Wieland, “Bias in meta-analysis detected by a simple, graphical test. Asymmetry detected in funnel plot was probably due to true heterogeneity,” BMJ (Clinical research ed.), vol. 316, no. 7129, pp. 469–471, 1998. View at: Publisher Site | Google Scholar
  39. E. Peterson, P. De, and R. Nuttall, “BMI, diet and female reproductive factors as risks for thyroid cancer: a systematic review,” PLoS ONE, vol. 7, no. 1, Article ID e29177, 2012. View at: Publisher Site | Google Scholar
  40. P. H. Bisschop, A. W. Toorians, E. Edert, W. M. Wiersinga, L. J. Gooren, and E. Fliers, “The effects of sex-steroid administration on the pituitary-thyroid axis in transsexuals,” European Journal of Endocrinology, vol. 155, no. 1, pp. 11–16, 2006. View at: Publisher Site | Google Scholar
  41. N. Takeichi, H. Ito, R. Haruta, T. Matsuyama, K. Dohi, and E. Tahara, “Relation between estrogen receptor and malignancy of thyroid cancer,” Japanese Journal of Cancer Research, vol. 82, no. 1, pp. 19–22, 1991. View at: Publisher Site | Google Scholar
  42. S. Rajoria, R. Suriano, A. L. George et al., “Estrogen activity as a preventive and therapeutic target in thyroid cancer,” Biomedicine and Pharmacotherapy, vol. 66, no. 2, pp. 151–158, 2012. View at: Publisher Site | Google Scholar

Copyright © 2015 Yijuan Cao et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.


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