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American Journal of Epidemiology Advance Access originally published online on September 12, 2007
American Journal of Epidemiology 2007 166(10):1140-1149; doi:10.1093/aje/kwm204
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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

Alcohol Drinking, Tobacco Smoking, and Anthropometric Characteristics as Risk Factors for Thyroid Cancer: A Countrywide Case-Control Study in New Caledonia

Romain Guignard1,2, Thérèse Truong1,2, Yannick Rougier3, Dominique Baron-Dubourdieu4 and Pascal Guénel1,2

1 Unité 754, INSERM, Villejuif, France
2 University Paris-Sud, Villejuif, France
3 Institut Pasteur de Nouvelle-Calédonie, Nouméa, New Caledonia
4 Laboratory of Anatomy and Cytopathology, Nouméa, New Caledonia

Correspondence to Dr. Pascal Guénel, Unité 754, INSERM, 16 avenue Paul Vaillant-Couturier, 94807 Villejuif Cedex, France (e-mail: guenel{at}vjf.inserm.fr).

Received for publication February 14, 2007. Accepted for publication June 8, 2007.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
Exceptionally high incidence rates of thyroid cancer are observed in New Caledonia, particularly in Melanesian women. To investigate further the etiology of thyroid cancer and to clarify the reasons of this elevated incidence, the authors conducted a countrywide population-based case-control study in this multiethnic population. The study included 332 cases with histologically verified papillary or follicular carcinoma (293 women and 39 men) diagnosed in 1993–1999 and 412 population controls (354 women and 58 men) frequency matched by gender and 5-year age group. Thyroid cancer was negatively associated with tobacco smoking and alcohol drinking, but no inverse dose-response relation was observed. Height was positively associated with thyroid cancer, particularly in men. Strong positive associations with weight and body mass index were observed in Melanesian women aged 50 years or more, with an odds ratio of 5.5 (95% confidence interval: 1.5, 20.3) for a body mass index of 35 kg/m2 or greater compared with normal-weight women, and there was a clear dose-response trend. This study clarifies the role of overweight for thyroid cancer in postmenopausal women. Because of the high prevalence of obesity among Melanesian women of New Caledonia, this finding may explain in part the exceptionally elevated incidence of thyroid cancer in this group.

alcohol drinking; body height; body mass index; body weight; case-control studies; New Caledonia; smoking; thyroid neoplasms

Abbreviations: BMI, body mass index; CI, confidence interval; OR, odds ratio; TSH, thyroid-stimulating hormone


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
Thyroid cancer represents about 1 percent of all cancers worldwide, but it is the most frequent endocrine malignancy (1). In 1993–1997, the age-standardized incidence rate per 100,000 ranged from three to eight in women and from one to three in men in most countries (2). Incidence rates of about 20 in women have also been reported in Iceland, for Filipinos in Hawaii, or in French Polynesia (2, 3). In recent years, the incidence of thyroid cancer has increased sharply in many geographic areas, particularly for papillary carcinomas (4–9). With the exception of thyroid cancer in children in areas with high radioactive fallout from the Chernobyl accident (10), most of this increase is attributed to improved screening of thyroid tumors, as can be assessed from the growing proportion of microcarcinomas (11). We have recently reported elevated incidence rates for thyroid cancer in New Caledonia, a French overseas territory in the South Pacific. This country has approximately 200,000 inhabitants of whom 45 percent are native Melanesians, 35 percent are of European origin, and 20 percent are of various ethnic groups, mainly Polynesian or Asian. In 1995–1999, incidence rates as high as 120 per 100,000 were observed among women of Melanesian origin (9). Enhanced detection of thyroid nodules starting in 1995 probably accounts for the increase in incidence of thyroid cancer, but the rates for this cancer have been outstandingly elevated in this population since at least 1985 (9, 12). The reasons for the elevated incidence are currently unknown. In particular, radioactive fallout from atmospheric nuclear tests carried out in French Polynesia in the 1960s and 1970s is not known to have affected New Caledonia located 4,500 km away.

To investigate further the risk factors for thyroid cancer and to clarify the reasons of the exceptionally high incidence in New Caledonia, we conducted a countrywide population-based case-control study. Besides ionizing radiations, the only well-established cause of thyroid cancer, many other risk factors are suspected to play a role in the etiology of the disease (13). We have reported that irregular menstruations, miscarriages, and the number of full-term pregnancies are associated with thyroid cancer (14). In the present paper, we focus on alcohol drinking and tobacco smoking and on anthropometric characteristics.

Previous studies have reported a moderate inverse association of thyroid cancer with tobacco smoking (15–24). In a pooled analysis of 14 case-control studies (25), current cigarette smoking was significantly associated with a moderate reduction in risk of thyroid cancer, and there was some evidence of a decreasing trend of thyroid cancer risk with smoking intensity and duration (20, 25), suggesting a causal relation between tobacco smoking and thyroid cancer. An inverse association of thyroid cancer with alcohol drinking was also suggested in some studies. However, in the pooled analysis including 10 case-control studies with data on wine and beer consumption, the decreasing trend of thyroid cancer with total alcohol intake was not significant after adjustment for current smoking (25).

Because thyroid function is linked to development and growth, height and weight are seen as possible indicators of thyroid cancer risk. In a pooled analysis of 12 case-control studies, both men and women with height in the topmost tertile had moderately increased odds ratios of thyroid cancer compared with men and women in the lowest tertile (26). Similarly, a cohort study from Norway reported a moderate association between height and thyroid cancer (27). Overweight has been inconsistently associated with thyroid cancer in several studies (15, 28–30), with a pooled odds ratio estimate of 1.2 (95 percent confidence interval (CI): 1.0, 1.4) for the women in the topmost tertile of body mass index (BMI) (26). In the Norwegian cohort study (27), a moderately increased relative risk of 1.29 for thyroid cancer was reported for obese women with BMI equal to or greater than 30.0 kg/m2.

Our study permitted the further investigation of these factors in a very high incidence area for thyroid cancer, and hence it provided a unique opportunity to identify new clues to the etiology of this cancer.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 References
 
Case selection
Cases were patients with papillary or follicular thyroid cancer diagnosed between January 1, 1993, and December 31, 1999, who had been living in New Caledonia for at least 5 years at the time of diagnosis. Thyroid cancer patients were identified from the two pathology laboratories of New Caledonia. In order to ensure completeness of case registration, patients were also sought in the New Caledonia cancer registry and in medical records of head and neck practitioners (9). In total, 369 incident cases were eligible for the study. All pathology reports were reviewed to determine the histologic type of the tumor and the number and diameter of the cancerous nodules in the thyroid gland. When information was missing, the original histologic slides were reviewed by the original pathologist.

Although the data collection started in 1998, the good prognosis of the disease permitted us to contact the patients diagnosed in 1993–1997 for inclusion in the study. Cases diagnosed in 1998 and 1999 were recruited prospectively. Of the 369 eligible cases of thyroid cancer, 37 (10 percent) could not be interviewed because the subject was dead (n = 21), refused to participate (n = 10), could not be contacted (n = 5), or was too ill (n = 1).

Control selection
Controls were randomly selected from electoral rolls recently updated in 1998 that included the name, sex, address, and date of birth of all New Caledonia residents aged 18 years or older, and they were frequency matched to the cases by gender and 5-year age group. To achieve density sampling of the source population, seven groups of controls were selected at random among subjects living in New Caledonia during a given year of the study period from 1993 to 1999 (referred to below as the "reference year"), so that they frequency matched the group of cases with the corresponding year of diagnosis. Subjects were not eligible as controls if they had not been living in New Caledonia for at least 5 years as of the reference year or if they had had a thyroid cancer before that date. Only variables determined at or before diagnosis for the cases or reference year for the controls were considered in the analyses.

Of 473 eligible controls, 61 (13 percent) could not be interviewed because they were dead (n = 13), refused to participate (n = 21), could not be contacted (n = 24), were too ill (n = 2), or for another reason (n = 1).

Data collection
Data were collected during a face-to-face interview by use of a structured questionnaire. An informed consent was signed by all subjects. In this paper, we focus on anthropometric factors, alcohol drinking, and tobacco smoking. Subjects who had quit smoking for at least 1 year at the reference year were classified as former smokers. Pack-years of tobacco smoking were calculated from the total number of years of tobacco smoking and from the number of cigarettes smoked per day. In these calculations, we assumed that one pipe = one cigarillo = two cigarettes (two women and seven men were pipe smokers; one man smoked cigarillos). Alcohol drinking was assessed in the questionnaire as the number of glasses per week separately for each type of beverage (beer, wine, aperitif, and liqueur). Because the ethanol content is approximately the same for an ordinary glass of any alcoholic beverage, the total number of drinks per week was used as an indicator of total alcohol intake.

Height and weight at the reference year were used to calculate body mass index (BMI) (weight (kg)/height (m)2). BMI was categorized according to the definition of the World Health Organization (31): underweight (BMI: <18.50), normal weight (BMI: 18.50–24.99), preobesity (BMI: 25.00–29.99), moderate obesity (BMI: 30–34.99), and severe obesity (BMI: ≥35).

Statistical analysis
The analyses were conducted for men and women separately, because risk factors may differ according to gender. Unconditional logistic regression (32) was performed with SAS, version 9.1, software (SAS Institute, Inc., Cary, North Carolina). All odds ratios were adjusted for age (5-year age groups) and year of diagnosis/reference. Adjustment for ethnic group was also used in tables 1 and 2 with all subjects combined. Tests for trend were conducted by fitting models using a quantitative variable equal to the median value of the exposure classes. Stratification by ethnic group was conducted in women only, because the number of men was too small for a meaningful analysis. Stratification by age group (<50 years; ≥50 years) was used as a proxy for menopausal status in women. Analyses were also carried out for pre- or postmenopausal women separately, after excluding perimenopausal women whose status was undetermined, but the results were similar and are not shown. Nonordinal polytomous logistic regression (33) was carried out by dividing the cases into two groups according to the size of the thyroid carcinoma (≤10 mm, >10 mm). Odds ratios for alcohol drinking and tobacco smoking were calculated from a single multivariate model where each variable was adjusted for the other. Odds ratios for weight and body mass index were adjusted for miscarriage, irregular menstruations, and number of full-term pregnancies, as these variables may act as confounders (14).


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  		TABLE 1. Sociodemographic characteristics of thyroid cancer cases and controls by gender, New Caledonia, 1993–1999

 

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  		TABLE 2. Odds ratios of thyroid cancer for tobacco smoking, alcohol drinking, and anthropometric characteristics, New Caledonia, 1993–1999

 

   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 References
 
Approximately 85 percent of the thyroid cancer cases were of the papillary type, and among those 55 percent had a diameter of less than 10 mm (table 1). Because of the frequency-matched design of the study, the distribution by age group was similar in cases and in controls. Proportionally more cases than controls were of Melanesian origin, reflecting the higher incidence rate in this group. Among Melanesians, more cases than controls were living in the Loyalty Islands, because of the higher incidence in this province (9).

Tobacco smoking and alcohol drinking
Smoking status was not associated with thyroid cancer (table 2). The odds ratios for smokers of 10–20 pack-years were below one and were at the limit of statistical significance in women. No association with age at start of smoking, smoking duration, or daily tobacco usage was observed (results not shown). The odds ratios for alcohol drinking were below one and as low as 0.45 for women declaring 1–5 drinks per week, but the tests for trend were not statistically significant (table 2). Analyses by type of alcoholic beverage or further stratification by ethnic group, province, or size of carcinoma did not alter these findings (not shown).

Anthropometric characteristics
The odds ratios in women taller than 160 cm, compared with those in smaller women, were increased by about 30 percent. Women weighing 90 kg or more had an odds ratio of about 2.5 when compared with women whose weight was less than 60 kg, and a dose-risk relation between thyroid cancer and weight was apparent (p < 0.01). Results for BMI indicated that women with moderate (BMI: 30–34.99) or severe (BMI: ≥ 35) obesity had a twofold increased risk compared with women in the normal range (BMI: 18.5–24.99), and a linear trend with BMI was also seen (table 2).

Odds ratios above five were observed among men in height categories 170–174 cm and 175–179 cm, but the odds ratio decreased to 2.15 in men taller than 180 cm (table 2). No association with weight or body mass index was apparent in men.

The odds ratios for anthropometric characteristics in women after stratification by ethnic group are shown in table 3. Height was clearly associated with thyroid cancer in European women. Odds ratios for weight and BMI were increased in all ethnic groups, although the confidence intervals were wide in non-Melanesian women. Table 3 also shows that obesity (BMI: >30 kg/m2) was more prevalent among Melanesian (26 percent) than among European (17 percent) control women.


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  		TABLE 3. Odds ratios of thyroid cancer for height, weight, and body mass index by ethnic group among women, New Caledonia, 1993–1999

 
Results of the stratified analysis by age group (<50 years; ≥50 years) are shown in table 4 for Melanesian women. In women aged less than 50 years, there was no association with body size variables. Conversely, among older women, the odds ratios for weight and body mass index increased sharply, ranging between 4.5 and 5.5 for BMI above 30 kg/m2, and the tests for trend were statistically significant. Similar results were observed in stratified analyses combining women of all ethnic groups (not shown).


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  		TABLE 4. Odds ratios* of thyroid cancer for height, weight, and body mass index by age group in Melanesian women, New Caledonia, 1993–1999

 
We finally analyzed the effects of anthropometric characteristics by size of the carcinomas in Melanesian women aged 50 or more years. Assuming that microcarcinomas (≤10 mm) are most likely detected during systematic screening of thyroid cancer, this analysis was conducted to see if the associations with weight and body mass index might be related to the higher detection rate of thyroid nodules in overweight women than in normal-weight women. This hypothesis is not supported by results in table 5, where the odds ratios for weight and body mass index do not differ according to the size of carcinoma.


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  		TABLE 5. Odds ratios* of thyroid cancer associated with anthropometric variables, by size of carcinoma, in Melanesian women aged 50 or more years, New Caledonia, 1993–1999

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
References
 
We found a strong positive association between thyroid cancer and weight or body mass index in Melanesian women above 50 years of age. No such association was apparent in men or in younger women. There was also some indication of an association with height, particularly in men, but no clear evidence of an association with tobacco smoking or alcohol drinking.

Strengths and limits
This study has important strengths including the population-based design with virtually exhaustive identification of thyroid cancer cases and a high participation rate among cases and population controls. A careful review of all pathologic reports and slides in the study constitutes another important feature. It permitted us to classify thyroid tumors according to the size of carcinoma and to assess the effects of a possible detection bias due to enhanced diagnoses of thyroid cancers. To our knowledge, no previous study on thyroid cancer risk factors has considered the size of the carcinoma, as this information is not systematically recorded in thyroid cancer registers.

This study also has some limitations. Small numbers did not permit detailed analyses to be carried out in subgroups such as men and non-Melanesian women. It is also possible that self-reported measures of tobacco smoking and alcohol consumption were underestimated, and that body size information was imprecise, leading most likely to nondifferential misclassification. In addition, we collected data on body size at different periods of life, but this information was often missing or unreliable and could not be used to study the effects of weight gain or loss.

Tobacco
An inverse association between tobacco smoking and thyroid cancer has been reported in most previous case-control studies (16, 17, 20, 22, 23). In a pooled analysis of 14 case-control studies, the odds ratio for 40 pack-years of tobacco smoking compared with never smoking was 0.6 (25). This result was confirmed in a recent large case-control study where a highly significant inverse dose-response relation was reported (20). Conversely, no association of tobacco smoking with thyroid cancer was found in two prospective cohort studies of men and women in the San Francisco Bay area (18) and of Canadian women (24), but the results were based on relatively small numbers of thyroid cancer patients. If the effect of tobacco smoking is real, the antiestrogenic properties of tobacco smoke and the decrease in thyroid-stimulating hormone (TSH) levels related to tobacco are possible biologic mechanisms (34, 35). In the present study, a U-shaped pattern was observed, with decreased odds ratios in the intermediate category of 10–20 pack-years for men and women. The absence of a clear inverse association in our data may be related to underestimation of tobacco smoking, particularly in heavier smokers who may not be willing to report high numbers of cigarettes per day in the context of a recent antismoking campaign in New Caledonia.

Alcohol
Negative associations between alcohol drinking and thyroid cancer have also been reported in some studies (15, 17, 19, 23), but the results have been inconsistent (16, 36). In the pooled analysis including 10 case-control studies that collected data on wine and beer consumption, there was a significant trend of decreasing thyroid cancer risk with the number of drinks per week, which disappeared after adjustment for current smoking (25). Our study provides some support, although inconclusive, for a negative association between alcohol drinking and thyroid cancer with odds ratios adjusted for tobacco smoking below 0.5 in intermediate categories of alcohol drinking among women. The average alcohol consumption was particularly low and may have been underestimated particularly by heavier drinkers. A decreased risk of thyroid cancer, if any, might be related to a reduction of thyroid cell proliferation due to altered TSH response to TSH-releasing hormone that has been consistently reported among alcoholics (37).

Height
Height was positively associated with thyroid cancer in men and in European but not Melanesian women. In a pooled analysis of anthropometric factors in thyroid cancer (26) including 11 case-control studies from the United States (15, 16, 38, 39), Europe (40–45), and Asia (29), as well as one unpublished case-control study from Japan, height in the topmost tertile was associated with significantly increased odds ratios of 1.5 in men and of 1.2 in women. A large cohort study from Norway reported a moderate but statistically significant association of thyroid cancer with height in both sexes (27). Our data tend to confirm these findings, although not consistently across all ethnic groups. Correlates of adult height such as dietary factors that also influence thyroid function and thyroid cancer development might represent a possible explanation for this association (26).

Weight and body mass index
The association between thyroid cancer and weight or body mass index at the time of diagnosis was apparent in Melanesian women over 50 years of age. Weight was associated with increased risk of thyroid cancer in European and other ethnic group women, but no significant trend was observed. No association with weight or body mass index was detected in men.

In the pooled analysis of case-control studies, the subjects were classified according to study-specific tertiles of the BMI distributions in low, intermediate, or high BMI categories (26). Women in the topmost tertile had a pooled odds ratio of 1.2 only (95 percent CI: 1.0, 1.4) compared with women in the lowest tertile (26). Because the tertiles were based on study-specific distributions, the pooled odds ratio could not be linked to quantitative values of the BMI, making difficult a comparison between studies. The comparatively elevated odds ratios for BMI in our study may be explained by higher BMI values among Melanesian women than in other study populations. The high prevalence of obesity in these women is consistent with the findings of a previous survey on anthropometric characteristics conducted in New Caledonia (46) and permitted definition of a category of severe obesity with BMI greater than 35 kg/m2.

Our finding of an increased risk of thyroid cancer in women older than 50 years was consistent with findings from a study from Hawaii, which reported an association between thyroid cancer and weight or body mass index among postmenopausal women (30). In the pooled analysis, the association with BMI was of similar magnitude in post- and premenopausal women (26), but the detailed numbers were not shown. In a large cohort study carried out in Norway, a moderately increased relative risk of about 1.3 for women with a body mass index of 30 or more kg/m2 was observed for both groups of women below or above the age of 50 years (27). Weight was measured at the time of entry into the cohort, on average 15 years before cancer diagnosis. Thus, this study may have overlooked recent weight as the possible variable of etiologic importance, particularly for older women as weight gain occurring at the time of menopause was not taken into account. Because weight gain increases estrogen production by adipose tissues and estrogens influence thyroid carcinogenesis by promoting thyroid tumor growth (47), there is some biologic support for our finding of an association between thyroid cancer and BMI in older, mainly postmenopausal women.

It has been suspected that the association between weight or body mass index and thyroid cancer may be due to more frequent examination of the thyroid gland in overweight women (26). Because enhanced detection of thyroid cancer leads to more frequent diagnoses of small sized carcinomas, as demonstrated in time trend analyses of thyroid cancer incidence in New Caledonia (9) and France (48), we have analyzed this association according to the size of the cancerous nodule. We have shown that the association between weight or body mass index and thyroid cancer in older Melanesian women is similar whatever the size of the carcinoma, indicating that detection bias is not a likely explanation for our findings.

Conclusion
We have shown a clear positive association between weight or body mass index and thyroid cancer in women aged 50 years or more. The high prevalence of overweight among older Melanesian women could explain in part the exceptionally high incidence of thyroid cancer, as it was estimated that about one third of the cases in this group were attributable to a BMI above 30 kg/m2. The association between thyroid cancer and BMI was generally weaker in other studied populations. Our finding could be related to interactions between the BMI and as yet unmeasured genetic, environmental, or lifestyle factors specific to Melanesian women of New Caledonia. Further investigations on these factors are presently underway in this population and will permit examination of this hypothesis.


   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 support during data collection. They are particularly grateful to Michèle Reynier who coordinated the interviews of study subjects across New Caledonia.

Conflict of interest: none declared.


   References
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 

  1. Stewart BW, Kleihues P, eds. Thyroid cancer. In: World cancer report (2003) Lyon, France: International Agency for Research on Cancer. 257–60.
  2. Cancer incidence in five continents. Volume VIII. IARC Sci Publ (2002) (155):1–781.
  3. 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]
  4. Reynolds RM, Weir J, Stockton DL, et al. Changing trends in incidence and mortality of thyroid cancer in Scotland. Clin Endocrinol (Oxf) (2005) 62:156–62.[CrossRef][Medline]
  5. Hodgson NC, Button J, Solorzano CC. Thyroid cancer: is the incidence still increasing? Ann Surg Oncol (2004) 11:1093–7.[CrossRef][Web of Science][Medline]
  6. Levi F, Randimbison L, Te VC, et al. Thyroid cancer in Vaud, Switzerland: an update. Thyroid (2002) 12:163–8.[CrossRef][Web of Science][Medline]
  7. Burgess JR. Temporal trends for thyroid carcinoma in Australia: an increasing incidence of papillary thyroid carcinoma (1982 –1997). Thyroid (2002) 12:141–9.[CrossRef][Web of Science][Medline]
  8. Colonna M, Grosclaude P, Remontet L, et al. Incidence of thyroid cancer in adults recorded by French cancer registries (1978 –1997). Eur J Cancer (2002) 38:1762–8.[CrossRef][Web of Science][Medline]
  9. Truong T, Rougier Y, Dubourdieu D, et al. Time trends and geographic variations for thyroid cancer in New Caledonia, a very high incidence area (1985 –1999). Eur J Cancer Prev (2007) 16:62–70.[CrossRef][Web of Science][Medline]
  10. 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]
  11. Leenhardt L, Grosclaude P, Cherie-Challine L. Increased incidence of thyroid carcinoma in France: a true epidemic or thyroid nodule management effects? Report from the French Thyroid Cancer Committee. Thyroid (2004) 14:1056–60.[CrossRef][Web of Science][Medline]
  12. 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]
  13. Hall P, Adami HO. Thyroid cancer. In: Textbook of cancer epidemiology—Adami HO, Hunter D, Trichopoulos D, eds. (2002) New York, NY: Oxford University Press. 504–19.
  14. 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]
  15. Ron E, Kleinerman RA, Boice JDJ, et al. A population-based case-control study of thyroid cancer. J Natl Cancer Inst (1987) 79:1–12.[Web of Science][Medline]
  16. 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]
  17. Rossing MA, Cushing KL, Voigt LF, et al. Risk of papillary thyroid cancer in women in relation to smoking and alcohol consumption. Epidemiology (2000) 11:49–54.[CrossRef][Web of Science][Medline]
  18. Iribarren C, Haselkorn T, Tekawa IS, et al. Cohort study of thyroid cancer in a San Francisco Bay area population. Int J Cancer (2001) 93:745–50.[CrossRef][Web of Science][Medline]
  19. Mack WJ, Preston-Martin S, Bernstein L, et al. Lifestyle and other risk factors for thyroid cancer in Los Angeles County females. Ann Epidemiol (2002) 12:395–401.[CrossRef][Web of Science][Medline]
  20. Kreiger N, Parkes R. Cigarette smoking and the risk of thyroid cancer. Eur J Cancer (2000) 36:1969–73.[CrossRef][Web of Science][Medline]
  21. Memon A, Varghese A, Suresh A. Benign thyroid disease and dietary factors in thyroid cancer: a case-control study in Kuwait. Br J Cancer (2002) 86:1745–50.[CrossRef][Web of Science][Medline]
  22. Hallquist A, Hardell L, Degerman A, et al. Occupational exposures and thyroid cancer: results of a case-control study. Eur J Cancer Prev (1993) 2:345–9.[Medline]
  23. 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]
  24. Navarro Silvera SA, Miller AB, Rohan TE. Risk factors for thyroid cancer: a prospective cohort study. Int J Cancer (2005) 116:433–8.[CrossRef][Web of Science][Medline]
  25. Mack WJ, Preston-Martin S, Dal ML, et al. A pooled analysis of case-control studies of thyroid cancer: cigarette smoking and consumption of alcohol, coffee, and tea. Cancer Causes Control (2003) 14:773–85.[CrossRef][Web of Science][Medline]
  26. Dal Maso L, La Vecchia C, Franceschi S, et al. A pooled analysis of thyroid cancer studies. V. Anthropometric factors. Cancer Causes Control (2000) 11:137–44.[CrossRef][Web of Science][Medline]
  27. Engeland A, Tretli S, Akslen LA, et al. Body size and thyroid cancer in two million Norwegian men and women. Br J Cancer (2006) 95:366–70.[CrossRef][Web of Science][Medline]
  28. 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]
  29. 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]
  30. 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]
  31. World Heath Organization. Report of a WHO consultation on obesity. Obesity: preventing and managing the global epidemic (1998) Geneva, Switzerland: World Health Organization.
  32. Breslow NE, Day NE, eds. Statistical methods in cancer research. Vol I. The analysis of case-control studies (1980) Lyon, France: International Agency for Research on Cancer. (IARC scientific publication no. 32).
  33. Hosmer D, Lemeshow S. Applied logistic regression (1989) New York, NY: John Wiley & Sons, Inc.
  34. Georgiadis E, Papapostolou C, Korakis T, et al. The influence of smoking habits on thyroid gland volume: an ultrasonic approach. J R Soc Health (1997) 117:355–8.[Web of Science][Medline]
  35. Knudsen N, Bulow I, Laurberg P, et al. High occurrence of thyroid multinodularity and low occurrence of subclinical hypothyroidism among tobacco smokers in a large population study. J Endocrinol (2002) 175:571–6.[Abstract]
  36. Franceschi S, Fassina A, Talamini R, et al. Risk factors for thyroid cancer in northern Italy. Int J Epidemiol (1989) 18:578–84.[Abstract/Free Full Text]
  37. Zoeller RT, Fletcher DL, Simonyl A, et al. Chronic ethanol treatment reduces the responsiveness of the hypothalamic-pituitary-thyroid axis to central stimulation. Alcohol Clin Exp Res (1996) 20:954–60.[Web of Science][Medline]
  38. 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]
  39. McTiernan AM, Weiss NS, Daling JR. Incidence of thyroid cancer in women in relation to previous exposure to radiation therapy and history of thyroid disease. J Natl Cancer Inst (1984) 73:575–81.[Web of Science][Medline]
  40. 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]
  41. Wingren G, Hatschek T, Axelson O. Determinants of papillary cancer of the thyroid. Am J Epidemiol (1993) 138:482–91.[Abstract/Free Full Text]
  42. 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]
  43. D'Avanzo B, La Vecchia C, Franceschi S, et al. History of thyroid diseases and subsequent thyroid cancer risk. Cancer Epidemiol Biomarkers Prev (1995) 4:193–9.[Abstract]
  44. Levi F, Franceschi S, La Vecchia C, et al. Previous thyroid disease and risk of thyroid cancer in Switzerland. Eur J Cancer (1991) 27:85–8.[Web of Science][Medline]
  45. 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]
  46. Tassie JM, Papoz L, Barny S, et al. Nutritional status in adults in the pluri-ethnic population of New Caledonia. The CALDIA Study Group. Int J Obes Relat Metab Disord (1997) 21:61–6.[CrossRef][Web of Science][Medline]
  47. 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]
  48. Colonna M, Guizard AV, Schvartz C, et al. 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 (2007) 43:891–900.[CrossRef][Web of Science][Medline]

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