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American Journal of Epidemiology Advance Access originally published online on October 26, 2007
American Journal of Epidemiology 2008 167(2):219-229; doi:10.1093/aje/kwm288
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American Journal of Epidemiology © The Author 2007. Published by the Johns Hopkins Bloomberg School of Public Health. All rights reserved. For permissions, please e-mail: journals.permissions@oxfordjournals.org.

ORIGINAL CONTRIBUTIONS

Menstrual and Reproductive Factors in the Risk of Differentiated Thyroid Carcinoma in Native Women in French Polynesia: A Population-based Case-Control Study

Pauline Brindel1,2,3, Françoise Doyon1,2,3, Frédérique Rachédi4, Jean-Louis Boissin5, Joseph Sebbag6, Larrys Shan5, Vaiana Chungue1,2,3, Laure Yen Kai Sun7, Frédérique Bost-Bezeaud4,8, Patrice Petitdidier8,9, John Paoaafaite9,10, Joseph Teuri9,10 and Florent de Vathaire1,2,3

1 Unit 605, INSERM, Villejuif, France
2 Department of Biostatistics and Epidemiology, Institut Gustave Roussy, Villejuif, France
3 University Paris XI, Villejuif, France
4 Department of Diabetology and Endocrinology, Territorial Hospital Mamao, Papeete, French Polynesia
5 Endocrinologists, Papeete, French Polynesia
6 Endocrinologist, Clinique Paofai, Papeete, French Polynesia
7 Cancer Registry of French Polynesia, Direction de la santé, Papeete, French Polynesia
8 Department of Biology, Territorial Hospital Mamao, Papeete, French Polynesia
9 Laboratory of Anatomy and Cytopathology Boz and Petitdidier, Papeete, French Polynesia
10 Institut de Recherche pour le Développement, Papeete, French Polynesia

Correspondence to Dr. Florent de Vathaire, INSERM Unit 605, Institut Gustave Roussy, 39 rue Camille Desmoulins, 94805 Villejuif Cedex, France (e-mail: fdv{at}igr.fr).

Received for publication May 31, 2006. Accepted for publication September 7, 2007.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
French Polynesia has one of the world's highest incidence rates of thyroid cancer. A case-control study among native residents of French Polynesia included 201 women diagnosed with differentiated thyroid cancer before the age of 56 years, between 1981 and 2004, matched to 324 population controls on date of birth. Face-to-face interviews were conducted from 2002 to 2004. Odds ratios were calculated by using conditional logistic regression and were reported in the total group and by ethnic group ("Polynesian" vs. "mixed"). The risk of thyroid cancer increased with natural (odds ratio = 1.9) or artificial (odds ratio = 4.5) menopause compared with that associated with a premenopausal status and with number of births (p for trend = 0.03): odds ratios for one, two, three, four or five, six or seven, and eight or more births were, respectively, 0.90, 1.6, 2.3, 2.2, 2.7, and 1.7 compared with a nulliparous status. Similar results were observed for Polynesian women. No association was observed with irregular menstrual cycles, age at menopause, history of miscarriage or induced abortion, time since last birth, age at and outcome of first pregnancy, or breastfeeding. This study confirms the role of menstrual and reproductive factors in the risk of differentiated thyroid cancer in Pacific island populations.

case-control studies; menopause; menstruation; Polynesia; pregnancy; thyroid neoplasms; women

Abbreviations: CI, confidence interval; OR, odds ratio


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
French Polynesia is in the South Pacific and is composed of five archipelagos: the Windward and Leeward Islands (which make up the Society Islands), the Marquesas and Austral Islands, and the Tuamotu Gambier archipelago. It comprises about 121 atolls or islands, scattered over a surface of 4 million km2 of the Pacific Ocean, with only 4,000 km2 of solid, dry land. According to the 2002 census, more than 87 percent of the 246,000 inhabitants of French Polynesia were living on the Society Islands. About 93 percent of the population born in French Polynesia defined themselves as Maori or of mixed Maori origin in the 1988 census, the last census to record ethnic information.

The highest thyroid cancer incidence rates are observed in the South Pacific. The highest incidence of 35/100,000 (world standardized) was observed among Melanesian women in New Caledonia in 1985–1992 (1). In 1985–1995, thyroid cancer incidence in French Polynesia was 17/100,000 among native French Polynesian women, 1.8-fold higher than among the native Maori population in Hawaii and 2.6-fold higher than among Maoris in New Zealand (2).

Substantial variations in thyroid cancer incidence in the world population strongly suggest that environmental factors play a role in the etiology of this cancer. Ionizing radiation has been identified as the main risk factor for differentiated papillary thyroid carcinoma (3–7). Menstrual and reproductive factors are suspected because of a much higher incidence among females and the probable implication of hormonal factors, be they endogenous hormones such as estrogens and thyroid-stimulating hormones, as suggested in observational studies (8–12), or exogenous hormones such as oral contraceptives, which were shown to increase the risk in a pooled analysis of case-control studies (13). Several menstrual and reproductive factors seem to play a role, although the results of studies are contradictory (14–36). A high number of births has been shown to be related to a higher risk of thyroid cancer (15, 22, 34, 36), whereas miscarriage at first pregnancy has been alternately suspected to increase (28, 29, 34) or lower (36) the risk of thyroid cancer, suggesting that the potential relation between pregnancy and thyroid cancer should be further explored. In addition, an older age at menarche and at menopause was found to be related to thyroid cancer in a pooled analysis (28).

To explain the high incidence of thyroid cancer in French Polynesia, we performed a case-control study to investigate the potential role of French atmospheric nuclear testing between 1966 and 1974 on Mururoa and to study other risk factors, notably the role of hormonal factors in thyroid cancer risk among native women in this Pacific population.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 References
 
The study was approved by the French Polynesian Ethics Committee. Consent forms were written in the French and Polynesian languages, and written informed consent was obtained from all participants so that we could contact their physicians.

Case selection
All patients diagnosed with thyroid cancer before the age of 56 years and born and living in French Polynesia were eligible for the study. Prevalent cases were identified from the cancer registry of French Polynesia, medical insurance files, and the four endocrinologists in Tahiti. The pathologic characteristics of tumors were obtained from the two histopathology laboratories (one public and one private) in Tahiti and from the medical files of endocrinologists. Mixed papillary follicular cancers were considered papillary lesions. The histologic slides of 68 patients who had received 131I treatment at the Institute of Oncology Gustave Roussy were reviewed in the institute's pathology department, and the diagnoses were in agreement with those established in French Polynesia for 64 patients (94 percent). Of the 221 eligible female thyroid cancer cases, 20 (9 percent) were not interviewed because they refused to participate (n = 2), had died (n = 13), could not be contacted (n = 4), or were too ill to be interviewed (n = 1). The study population thus consisted of 201 female cases.

Matching process
For each eligible case, two potential controls, matched on date of birth (±6 months) and sex, were selected at random from the French Polynesia registry of births, which records all inhabitants born in French Polynesia. To do so, an SAS random number generator was used (SAS Institute, Inc., Cary, North Carolina). At the end of the interviews, a few cases could not be matched to interviewed controls. Each of these cases was matched to a control initially selected for another case of the same gender and with the same date of birth. Matching on date of birth was then extended if necessary. Finally, of the 201 interviewed cases, 78 were matched to one control (39 percent) and 123 to two controls (61 percent), and the difference in date of birth ranged from 6 to 17 months for 23 controls.

Contacting controls and conducting interviews
Of the 404 randomly selected controls, 80 (20 percent) were not interviewed because the subjects had died (n = 8), could not be contacted (n = 28), were too ill to be interviewed (n = 2), had moved away from French Polynesia (n = 16), or refused to participate (n = 26). A total of 324 female controls were thus included.

Data collection
The addresses of cases and controls were obtained from the territorial medical insurance plan, which covers all inhabitants, whatever their professional status. Interviewers repeated attempts to reach cases and controls until they succeeded and, when needed, corrected missing or erroneous addresses by questioning municipal registries and the participants' last neighbors. All participants were contacted by mail or phone. Interviews were conducted face-to-face by trained Polynesian interviewers and medical staff using a structured questionnaire. Most interviews were conducted in French; very few were conducted in the Polynesian language, mainly for the oldest participants. Some cases were interviewed at the hospital on the day of their usual follow-up consultation. Data collection included their ethnic group, lifetime weight changes, personal and family history of thyroid disease and cancer, places of residence, education and occupation, gynecologic and reproductive factors, medical x-ray exposure, and diet at both the time of the interview and during childhood. This paper focuses on menstrual and reproductive factors.

Analyzed parameters
Ethnic group of subjects was classified into four categories according to participants' parents' ethnicities: 1) Polynesian (both father and mother Polynesian), 2) Poly-Asian (at least one parent of Asian or of mixed Polynesian-Asian origin but none of European origin), 3) Poly-European (at least one parent of European or of mixed Polynesian-European origin but none of Asian origin), and 4) mixed Polynesian-Asian-European origin. Ethnic group, reclassified as "Polynesian" versus "mixed," was used for the stratified analysis. Educational level, height, and body mass index were considered as continuous variables. Women were considered naturally menopausal if their menstruation ended more than 1 year before the reference age.

Therapeutic abortions, ectopic pregnancies, and voluntary abortions were considered "induced abortions" for the analysis. Women for whom total duration of lactation was 2 months or less were considered to have never breastfed.

Statistical analysis
Data were analyzed by using conditional logistic regression (37) with SAS software, version 9.1 (SAS Institute, Inc.). The PHREG procedure was used, which allows for analysis of a matched 1:m design. A control was allocated a reference age equal to the case's age at the time of diagnosis. Only events or exposures that occurred before the reference age were considered for the analysis. Odds ratios were adjusted for ethnic group, educational level, height, body mass index, and interviewer. Because each interviewer did not always interview cases and controls belonging to the same strata, we adjusted on "interviewer" because some answers may have been influenced by variability in confidence between women and interviewers concerning intimate questions. Analyses were also conducted by ethnic group ("Polynesian"/"mixed") and by age group (<45, ≥45 years) corresponding to reproductive and postreproductive age. All statistical tests were two sided. To test the linear trends for continuous variables, these variables were treated as ordered categorical variables.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 References
 
Characteristics of cases and controls
The characteristics of the 201 cases are described in table 1. Forty-three carcinomas (21 percent) were follicular, of which three were Hurtle cell carcinomas. Follicular carcinomas were larger than papillary carcinomas. One patient had both a papillary and a medullary carcinoma. Information on associated thyroid disorders was collected, but we did not document the circumstances of the diagnosis and were thus unable to separate incidental findings from symptomatic thyroid carcinomas. The mean difference in the date of birth between each case and her control(s) was 41.6 days (standard deviation, 80.6).


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  		TABLE 1. Description of thyroid cancer cases, French Polynesia, 1981–2004

 
No difference in ethnic group or history of head and neck radiographic examinations before age 15 years was evidenced between cases and controls, but cases had a lower educational level and were heavier, were taller, and had a greater body mass index than controls (table 2).


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  		TABLE 2. General characteristics of cases and controls, French Polynesia, 1981–2004

 
Menstrual factors
Age at menarche.
A nonsignificant increased risk of thyroid cancer was evidenced at an older age at menarche (p for trend = 0.12 (table 3)). This result was not significantly dependent on age (table 3) or on ethnic group (table 4).


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  		TABLE 3. Odds ratios* of thyroid cancer associated with menstrual factors, by age at diagnosis, French Polynesia, 1981–2004

 

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  		TABLE 4. Odds ratios* of thyroid cancer associated with menstrual factors, by ethnic group, French Polynesia, 1981–2004

 
Menstrual cycle.
Irregular menstrual cycles were not related to a higher risk of thyroid cancer (table 3); this result was not dependent on age (table 3) or on ethnic origin (table 4).

Menopause.
Compared with women who were still menstruating, naturally menopausal women had a twofold risk of developing thyroid cancer, whereas an artificial menopause conferred a 4.5-fold higher risk (table 3). Similar results were observed among women of Maori origin and among women of mixed origin (table 4). When artificially induced menopausal women were compared with naturally menopausal women, taking into account age at menopause, the odds ratio was 1.9 (95 percent confidence interval (CI): 0.6, 6.4). Similar results were obtained for women of Maori origin (odds ratio (OR) = 1.5, 95 percent CI: 0.3, 6.7) and for women of mixed origin (OR = 1.6, 95 percent CI: 0.4, 6.7). Age at menopause was not associated with the risk of developing thyroid cancer even after adjusting for menopausal status (table 3). This result was not significantly dependent on ethnic group (table 4).

Reproductive factors
A nonsignificant increased risk of thyroid cancer was observed for parous women compared with nulliparous women. Thyroid cancer risk increased with number of births (p for trend = 0.03), although the risk decreased for eight or more births (table 5).


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  		TABLE 5. Odds ratios* of thyroid cancer associated with reproductive factors, by age at diagnosis, French Polynesia, 1981–2004

 
Results observed for Polynesian women (p for trend = 0.01) and for women of mixed origin (p for trend = 0.90) were slightly different (table 6), but no significant interaction was found between ethnic origin and number of births. A nonsignificant difference was observed according to the age group of the women: the trend was more apparent among women younger than age 45 years (p for trend = 0.03) than among older women (p for trend = 0.42) (table 5).


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  		TABLE 6. Odds ratios* of thyroid cancer associated with number of births, by ethnic group, French Polynesia, 1981–2004

 
No association with time since last birth was observed for ever parous or uniparous women. This finding was confirmed after restricting the analysis to women younger than 45 years of age. Thyroid cancer risk was not found to be linked to age at first birth or to the outcome of the first pregnancy. Ever having a miscarriage or an induced abortion was not associated with a significantly increased risk of thyroid cancer (table 5), even after adjusting on parity and when the analysis was restricted to ever-pregnant women.

No association was found with ever having breastfed or with duration of breastfeeding (table 5).

Multivariate analysis
A multivariate analysis was conducted, including the strongest menstrual and reproductive risk factors related to thyroid cancer identified in the univariate analysis (p < 0.10) and the adjusting factors (ethnic group, educational level, height, body mass index, interviewer, and history of radiation to the head or neck for diagnostic purposes). Table 7 shows only those reproductive factors that remained significantly associated (p < 0.05) with the risk of thyroid cancer in the multivariate analysis, namely, menopausal status and number of births. Naturally menopausal women had a nonsignificant twofold risk of thyroid cancer, whereas artificially induced menopausal women had a fivefold risk compared with women who were still menstruating. The risk of thyroid cancer increased with number of births, with an odds ratio of 1.2 for each additional birth between one and seven, compared with that for nulliparous women, while eight or more births almost doubled the risk. When a parameterization with a single variable for number of births was considered, the odds ratio was 1.1 (95 percent CI: 0.98, 1.1) for each additional birth, and adding a dichotomous variable for eight or more births to this model significantly increased the fit of the data (p = 0.04). Parameterization including three categories—nulliparous, uniparous, and two or more births—produced an odds ratio of 0.9 (95 percent CI: 0.35, 2.3) for uniparous and 1.4 (95 percent CI: 0.97, 2.1) for two or more births compared with that for a nulliparous status. Compared with such parameterization, adding the number of births exceeding two and fewer than eight as a continuous variable did not better fit the data (p = 0.16). No significant interaction was evidenced between these factors.


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  		TABLE 7. Odds ratios* of thyroid cancer associated with selected menstrual and reproductive factors that remained significant in the multivariate analysis, French Polynesia, 1981–2004

 
Similar results concerning menopausal status and number of births were observed for papillary cancers (table 7). The analysis was also stratified according to size of the cancer, and similar results were observed, although the relation with artificial menopause was stronger for women with a cancer measuring 10 mm or less (excluding those with associated metastasis, lymph node, or extravascular invasion, and multifocal cancers) (table 7). Similar results were observed in a sensitivity analysis conducted after excluding 31 cases diagnosed before 1991 and their 53 controls, a period during which fewer cases were collected than in the later periods.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
References
 
We found that a natural or an artificial menopause and an increasing number of births were associated with thyroid cancer risk in women born and living in French Polynesia and aged 55 years or less.

Controls were representative of the general population because they were selected from the registry of births. We were probably unable to exhaustively collect all cases of cancer diagnosed between 1984 (date of registry implementation) and 2003. However, given the geographic isolation of French Polynesia and the Polynesian public health system, only a few recent cases may have been missed by the cancer registry, the medical insurance system, and the endocrinologists in Tahiti. A 1996 investigation using all available sources of information added about 10 percent of cases that had not been registered in 1990–1995 (38). Before 1984, completeness of our collection of cases is extremely low. For the other periods of diagnosis (i.e., 1984–1990 and 1996–2000), we were unable to evaluate the completeness of our cases. However, a sensitivity analysis excluding the cases diagnosed during the 1981–1990 period, when fewer cases were included than in the later periods, showed that our findings remained unchanged. Including cases from this period therefore did not introduce any major bias.

Although interviewers went to great lengths to reach cases and controls, 28 (7 percent) controls could not be contacted and 26 (6 percent) refused to participate, representing four and two cases, respectively. When other reasons for failure to participate were included, the participation rate for controls (80 percent) was lower than that for cases (91 percent). Controls may have been less motivated because of the duration of the interview (90 minutes). A selection bias could therefore have occurred among either controls or cases but is unlikely to have strongly affected our results.

An older age at menarche was not significantly associated with a higher risk of thyroid cancer in our study, which is consistent with the results of the pooled analysis (OR = 1.2, 95 percent CI: 1.0, 1.4 for age 15 years or older versus less than age 13 years) (28). In a case-control study conducted in New Caledonia, this relation was restricted to women of European origin (OR = 3.4, 95 percent CI: 1.0, 12.0 for those aged 15 years or older versus less than age 13 years) (34). No relation was observed in a study conducted in Kuwait (36).

We did not find that irregular menstrual cycles conferred a higher risk of thyroid cancer, unlike the finding observed for Melanesian women in New Caledonia (34). This factor was not studied in the pooled analysis or in the Kuwaiti study (28, 36).

We found that an artificial menopausal status conferred a higher risk of thyroid cancer compared with a premenopausal status, as observed in the pooled analysis (OR = 1.8, 95 percent CI: 1.4, 2.4) (28). This relation was particularly strong among women with microcarcinomas, suggesting a surveillance bias resulting from a more thorough examination of the thyroid gland among women undergoing a surgical procedure such as hysterectomy. In New Caledonia, an artificial menopause and a history of oophorectomy or hysterectomy were not associated with a higher risk of thyroid cancer (34). This difference could be due, at least in part, to a younger age at artificial menopause in our study compared with the New Caledonian study, in which a nonsignificant increased risk was evidenced for women less than 43 years of age at artificial menopause (OR = 1.8, 95 percent CI: 0.7, 4.8). In the Kuwaiti study, no relation was observed with menopause, but the proportion of postmenopausal women was very small. Hysterectomy is often indicated secondary to menstrual disturbances (such as menorrhagia) likely to occur under certain hormonal conditions that are also related to thyroid cancer, as suggested by Luoto et al. (39).

Ever-parous, compared with nulliparous, women were not at significantly higher risk of thyroid cancer in our study, which is consistent with the New Caledonian and Kuwaiti studies (34, 36). Only a weak association was observed in the pooled analysis (OR = 1.2) (28). We found that risk of thyroid cancer increases with number of births, and this finding is in agreement with the New Caledonian and Kuwaiti studies, where women had a higher number of births (3.3 and 4.3, respectively), as in our study (3.2). In New Caledonia, this risk was particularly observed among women less than 45 years of age, reaching 2.8 for six or seven births and then decreasing to 1.1 for eight or more births, whereas, in Kuwaiti women, 11 or more births conferred a twofold risk (95 percent CI: 0.7, 5.8). In the pooled analysis, however, women had less than two children on average, and no relation was observed. The role of hormonal factors may explain the relation between number of births and risk of thyroid cancer. It has been suggested that estrogens, which are elevated during pregnancy, induce the proliferation of malignant thyroid cells (10, 11). Other hormonal factors that are elevated during pregnancy may be implicated. Thyroid-stimulating hormone and human chorionic gonadotropin were shown to be associated with thyrotropic activity in pregnant women (8). Although exposure to elevated thyroid-stimulating hormone levels for several years has been shown to lead to the development of benign thyroid tumors, it very rarely leads to thyroid carcinoma (12). The vulnerability of the pregnant woman's thyroid gland throughout repeated pregnancies could be hypothesized. In our study, this relation was not dependent on histology or on the size of the cancer.

A shorter time since the last birth was not related to a higher risk of thyroid cancer in our study, although a weak relation was observed in the pooled analysis (OR = 0.9, 95 percent CI: 0.8, 1.0) among women less than 45 years of age and in Kuwait for women during the second or third year after their last pregnancy. We observed no relation with older age at first birth, as in Kuwait, unlike the finding from the pooled analysis in which women who gave birth to their first child at the age of 30 years or older had a 1.3-fold risk of thyroid cancer (95 percent CI: 1.0, 1.8). This finding could be explained by a lack of power in our study and the Kuwaiti study, where only 14 percent and 18 percent of women, respectively, had their first birth (or, for the Kuwaiti study, experienced a first pregnancy) at the age of 25 years or older compared with 40 percent in the pooled analysis.

No relation with miscarriage at first pregnancy or number of miscarriages was observed in our study. Contradictory results have been observed in previous studies. Although miscarriage at first pregnancy conferred a higher risk of cancer in the pooled analysis (OR = 1.8, 95 percent CI: 1.2, 2.6) and in New Caledonian women (OR = 2.3, 95 percent CI: 1.0, 5.6), Kuwaitis whose first pregnancy ended with a miscarriage were protected (OR = 0.1, 95 percent CI: 0.03, 0.4), and their risk of thyroid cancer decreased significantly with an increasing number of miscarriages (p for trend < 0.05). Finally, induced abortion was not related to the risk of thyroid cancer in our study, which is consistent with the pooled analysis, whereas it conferred a threefold risk for New Caledonians.

Breastfeeding was not related to thyroid cancer in our study, as shown in the pooled analysis.

This study confirms the role of menstrual and reproductive factors in the risk of differentiated thyroid cancer, and especially the major role of menopause, particularly artificial menopause, and number of births for women less than 56 years of age in populations in the Pacific islands.


   ACKNOWLEDGMENTS
 
This study was supported by the Association pour la Recherche sur le Cancer (ARC); Direction Générale de la Santé (DGS), Comité de radioprotection de l'EDF; Agence Française de Sécurité Sanitaire et Environnementale (AFSSE) and the CHILD-THYR EEC programme. One of the authors, Pauline Brindel, is supported by a grant from ARC.

The authors thank P. Morales, J. Iltis, P. Giraud, P. Didiergeorge, M. Brisard, G. Soubiran, B. Caillou, J. M. Bidard, A. Merceron, M. L. Vanizette, P. Dupire, M. Berges, J. Ienfa, G. de Clermont, N. Cerf, B. Oddo, M. Bambridge, C. Baron, A. Mouchard-Rachet, O. Simonet, D. Lamarque, J. Vabret, J. Delacre, M. P. Darquier, J. Leninger, and L. Saint Ange.

Conflict of interest: none declared.


   References
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 

  1. Ballivet S, Salmi LR, Dubourdieu D, et al. Incidence of thyroid cancer in New Caledonia, South Pacific, during 1985 –1992. Am J Epidemiol (1995) 141:741–6.[Abstract/Free Full Text]
  2. Le Vu B, de Vathaire F, de Vathaire CC, et al. Cancer incidence in French Polynesia 1985 –95. Trop Med Int Health (2000) 5:722–31.[CrossRef][Web of Science][Medline]
  3. Cardis E, Kesminiene A, Ivanov V, et al. Risk of thyroid cancer after exposure to 131I in childhood. J Natl Cancer Inst (2005) 97:724–32.[Abstract/Free Full Text]
  4. de Vathaire F, Hardiman C, Shamsaldin A, et al. Thyroid carcinomas after irradiation for a first cancer during childhood. Arch Intern Med (1999) 159:2713–19.[Abstract/Free Full Text]
  5. Lindberg S, Karlsson P, Arvidsson B, et al. Cancer incidence after radiotherapy for skin haemangioma during infancy. Acta Oncol (1995) 34:735–40.[Web of Science][Medline]
  6. Lundell M, Hakulinen T, Holm LE. Thyroid cancer after radiotherapy for skin hemangioma in infancy. Radiat Res (1994) 140:334–9.[CrossRef][Web of Science][Medline]
  7. Ron E, Lubin JH, Shore RE, et al. Thyroid cancer after exposure to external radiation: a pooled analysis of seven studies. Radiat Res (1995) 141:259–77.[Web of Science][Medline]
  8. Glinoer D, de Nayer P, Bourdoux P, et al. Regulation of maternal thyroid during pregnancy. J Clin Endocrinol Metab (1990) 71:276–87.[Abstract/Free Full Text]
  9. Henderson BE, Ross RK, Pike MC, et al. Endogenous hormones as a major factor in human cancer. Cancer Res (1982) 42:3232–9.[Abstract/Free Full Text]
  10. Kawabata W, Suzuki T, Moriya T, et al. Estrogen receptors (alpha and beta) and 17beta-hydroxysteroid dehydrogenase type 1 and 2 in thyroid disorders: possible in situ estrogen synthesis and actions. Mod Pathol (2003) 16:437–44.[CrossRef][Web of Science][Medline]
  11. Manole D, Schildknecht B, Gosnell B, et al. Estrogen promotes growth of human thyroid tumor cells by different molecular mechanisms. J Clin Endocrinol Metab (2001) 86:1072–7.[Abstract/Free Full Text]
  12. Thomas GA, Williams ED. Thyroid stimulating hormone (TSH)-associated follicular hypertrophy and hyperplasia as a mechanism of thyroid carcinogenesis in mice and rats. IARC Sci Publ (1999) 45–59.
  13. La Vecchia C, Ron E, Franceschi S, et al. A pooled analysis of case-control studies of thyroid cancer. III. Oral contraceptives, menopausal replacement therapy and other female hormones. Cancer Causes Control (1999) 10:157–66.[CrossRef][Web of Science][Medline]
  14. Franceschi S, Fassina A, Talamini R, et al. The influence of reproductive and hormonal factors on thyroid cancer in women. Rev Epidemiol Sante Publique (1990) 38:27–34.[Web of Science][Medline]
  15. Galanti MR, Lambe M, Ekbom A, et al. Parity and risk of thyroid cancer: a nested case-control study of a nationwide Swedish cohort. Cancer Causes Control (1995) 6:37–44.[CrossRef][Web of Science][Medline]
  16. Galanti MR, Hansson L, Lund E, et al. Reproductive history and cigarette smoking as risk factors for thyroid cancer in women: a population-based case-control study. Cancer Epidemiol Biomarkers Prev (1996) 5:425–31.[Abstract]
  17. Galanti MR, Hansson L, Bergstrom R, et al. Diet and the risk of papillary and follicular thyroid carcinoma: a population-based case-control study in Sweden and Norway. Cancer Causes Control (1997) 8:205–14.[CrossRef][Web of Science][Medline]
  18. Glattre E, Haldorsen T, Berg JP, et al. Norwegian case-control study testing the hypothesis that seafood increases the risk of thyroid cancer. Cancer Causes Control (1993) 4:11–16.[CrossRef][Web of Science][Medline]
  19. Goodman MT, Kolonel LN, Wilkens LR. The association of body size, reproductive factors and thyroid cancer. Br J Cancer (1992) 66:1180–4.[Web of Science][Medline]
  20. Hallquist A, Hardell L, Degerman A, et al. Thyroid cancer: reproductive factors, previous diseases, drug intake, family history and diet. A case control study. Eur J Cancer Prev (1994) 3:481–8.[Medline]
  21. Kolonel LN, Hankin JH, Wilkens LR, et al. An epidemiologic study of thyroid cancer in Hawaii. Cancer Causes Control (1990) 1:223–34.[CrossRef][Web of Science][Medline]
  22. Kravdal O, Glattre E, Haldorsen T. Positive correlation between parity and incidence of thyroid cancer: new evidence based on complete Norwegian birth cohorts. Int J Cancer (1991) 49:831–6.[Web of Science][Medline]
  23. Levi F, Franceschi S, Gulie C, et al. Female thyroid cancer: the role of reproductive and hormonal factors in Switzerland. Oncology (1993) 50:309–15.[CrossRef][Web of Science][Medline]
  24. Linos A, Linos DA, Vgotza N, et al. Does coffee consumption protect against thyroid disease? Acta Chir Scand (1989) 155:317–20.[Web of Science][Medline]
  25. Mack WJ, Preston-Martin S, Bernstein L, et al. Reproductive and hormonal risk factors for thyroid cancer in Los Angeles County females. Cancer Epidemiol Biomarkers Prev (1999) 8:991–7.[Abstract/Free Full Text]
  26. McTiernan A, Weiss NS, Daling JR. Incidence of thyroid cancer in women in relation to known or suspected risk factors for breast cancer. Cancer Res (1987) 47:292–5.[Abstract/Free Full Text]
  27. McTiernan AM, Weiss NS, Daling JR. Incidence of thyroid cancer in women in relation to reproductive and hormonal factors. Am J Epidemiol (1984) 120:423–35.[Abstract/Free Full Text]
  28. Negri E, Dal Maso L, Ron E, et al. A pooled analysis of case-control studies of thyroid cancer. II. Menstrual and reproductive factors. Cancer Causes Control (1999) 10:143–55.[CrossRef][Web of Science][Medline]
  29. Preston-Martin S, Bernstein L, Pike MC, et al. Thyroid cancer among young women related to prior thyroid disease and pregnancy history. Br J Cancer (1987) 55:191–5.[Web of Science][Medline]
  30. Preston-Martin S, Jin F, Duda MJ, et al. A case-control study of thyroid cancer in women under age 55 in Shanghai (People's Republic of China). Cancer Causes Control (1993) 4:431–40.[CrossRef][Web of Science][Medline]
  31. Ron E, Kleinerman RA, Boice JD Jr, et al. A population-based case-control study of thyroid cancer. J Natl Cancer Inst (1987) 79:1–12.[Web of Science][Medline]
  32. Rossing MA, Voigt LF, Wicklund KG, et al. Reproductive factors and risk of papillary thyroid cancer in women. Am J Epidemiol (2000) 151:765–72.[Abstract/Free Full Text]
  33. Sakoda LC, Horn-Ross PL. Reproductive and menstrual history and papillary thyroid cancer risk: the San Francisco Bay Area thyroid cancer study. Cancer Epidemiol Biomarkers Prev (2002) 11:51–7.[Abstract/Free Full Text]
  34. Truong T, Orsi L, Dubourdieu D, et al. 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 (2005) 161:1056–65.[Abstract/Free Full Text]
  35. Wingren G, Hatschek T, Axelson O. Determinants of papillary cancer of the thyroid. Am J Epidemiol (1993) 138:482–91.[Abstract/Free Full Text]
  36. Memon A, Darif M, Al Saleh K, et al. Epidemiology of reproductive and hormonal factors in thyroid cancer: evidence from a case-control study in the Middle East. Int J Cancer (2002) 97:82–9.[CrossRef][Web of Science][Medline]
  37. Breslow NE, Day NE, eds. Statistical methods in cancer research. Vol 1. The analysis of case-control studies (1980) Lyon, France: International Agency for Research on Cancer. (IARC scientific publication no. 32).
  38. de Vathaire F, Le Vu B, Vathaire CC. Thyroid cancer in French Polynesia between 1985 and 1995: influence of atmospheric nuclear bomb tests performed at Mururoa and Fangataufa between 1966 and 1974. Cancer Causes Control (2000) 11:59–63.[CrossRef][Web of Science][Medline]
  39. Luoto R, Grenman S, Salonen S, et al. Increased risk of thyroid cancer among women with hysterectomies. Am J Obstet Gynecol (2003) 188:45–8.[CrossRef][Web of Science][Medline]

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