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Thyroid cancer is a relatively rare form of cancer, causing less than one per cent of cancer deaths, but with higher incidence in younger women, and, together with gallbladder cancer, it is one of the non sex-related site cancers whose rates are higher for females than for males.1–3

An established risk factor for thyroid cancer is a history of benign thyroid disease, mostly goitre, adenomas and hyper- thyroidism.4–9Other recognized risk factors include exposure to radiotherapy2 and radioactive iodine,10–12 mainly during

childhood,13–15 and long-term residence in regions with iodine imbalances, including high endemic goitre areas,9such as iodine-deficient regions in the Alps, or areas with high iodine levels, like Iceland and Hawaii.16–19Furthermore, a diet poor in vegetables and fruit20–23and rich in starchy food,24which are indicators of a poor diet in several populations, has been associated with an increased risk of thyroid cancer.6,7,25

Between 1986 and 1992 we conducted a case-control study of thyroid cancer in Italy, whose results confirmed the strong association with history of benign thyroid disease.9Other deter- minants for thyroid cancer risk were a history of radiotherapy, long-term residence in endemic goitre areas9and selected aspects of diet.24The role of each of these factors, or their combination, depends not only on the strength of the association, but also on the prevalence of each factor in the population. To address these issues, we estimated the population attributable risk (PAR) of thyroid cancer, i.e. the proportion of thyroid cancer cases in

Case-control study of thyroid cancer in Northern Italy: attributable risk

Francesca Fioretti,

a

Alessandra Tavani,

a

Silvano Gallus,

a

Silvia Franceschi,

b

Eva Negri

a

and Carlo La Vecchia

a,c

Background The percentage of thyroid cancer cases attributable to specific risk factors can be calculated to focus preventive strategies. The per cent population attributable risks (PAR) for thyroid cancer were estimated in relation to history of benign thyroid diseases, history of radiotherapy, residence in endemic goitre areas and selected indicators of a poor diet, using data from a case-control study conducted between 1986 and 1992 in Northern Italy.

Methods Cases were 399 histologically confirmed incident thyroid cancers and controls were 617 patients, admitted to hospital for a wide range of acute, non-neoplastic, non-hormone-related diseases. The PAR were computed on the basis of multi- variate odds ratios (OR) and on the distribution of risk exposure among cases, assuming they are representative of the general population of cases.

Results A history of benign thyroid disease accounted for 18.9% of cases, radiotherapy for 1.2%, residence for >20 years in endemic goitre areas for 2.4% of cases, and their combination for 21.7% of thyroid cancer cases; selected indicators of a poor diet accounted for 40.9% of thyroid cancer cases in this population. The com- bination of all factors considered explained over 57% of thyroid cancer cases in both sexes. The estimates for thyroid-related conditions were higher in women than men, whereas the opposite was true for dietary indicators. The overall PAR were somewhat higher in people aged >45 years (63.8%) than in younger subjects, and for follicular (69.1%) rather than papillary (53.7%) cancers.

Conclusions Exposure to a few simply identified and potentially modifiable risk factors or indicators (benign thyroid disease, residence in endemic goitre area and a poor diet) explained about 60% of thyroid cancer cases in this Italian population, indicating the theoretical scope for prevention.

Keywords Attributable risk, diet, radiotherapy, risk factors, thyroid cancer, benign thyroid diseases

Accepted 3 February 1999

aIstituto di Ricerche Farmacologiche ‘Mario Negri’, Via Eritrea 62, 20157 Milan, Italy.

bCentro di Riferimento Oncologico, Via Pedemontana Occidentale, 33081, Aviano (PN), Italy.

cIstituto di Statistica Medica e Biometria, Università degli Studi di Milano, Via Venezian 1, 20133 Milan, Italy.

Reprint requests to: Francesca Fioretti, Istituto di Ricerche Farmacologiche

‘Mario Negri’, Via Eritrea 62, 20157 Milano, Italy. E-mail: tavani@irfmn.mnegri.it

626

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Northern Italy attributable to selected benign thyroid diseases, radiotherapy, long-term residence in endemic goitre areas and selected indicators of a poor diet.

Materials and Methods

The data were derived from a case-control study of cancer of the thyroid, conducted between 1986 and 1992 in Northern Italy (the Greater Milan area, Friuli Venezia Giulia and Veneto regions), whose general design has already been described.26

Cases were patients older than 15 years and under age 75 with incident (diagnosed within 2 years before the interview), histologically confirmed thyroid cancer, admitted to the eight major teaching and general hospitals in the areas under surveil- lance. A total of 399 patients (108 men and 291 women, median age 44 years, range 16–72) were interviewed. Of these, 274 had papillary carcinomas (or mixed papillary/follicular), 69 follicular, and 56 anaplastic or other or undefined histological types.

Controls were patients from the same geographical areas, admitted to the same network of hospitals, during the same calendar period as cases for acute, non-neoplastic, non- hormonal-related diseases, unrelated to known or likely risk factors for thyroid cancer. A total of 617 controls (190 men and 427 women, median age 46 years, range 16–74 years) were interviewed. Of these, 15% were admitted for traumatic con- ditions, 17% for non-traumatic orthopaedic disorders (mainly low back pain and disc diseases), 28% for acute surgical con- ditions (such as acute appendicitis or strangulated hernia), and 40% for other miscellaneous illnesses (such as ear, nose and throat, eye, dental or skin disorders). Over 95% of cases and controls approached for interview participated.

Interviews were conducted by trained interviewers in a hospital setting, using a structured questionnaire to collect data on socio-demographic and anthropometric characteristics, smoking habits, and other lifestyle details, history of radio- therapy (unrelated to the present thyroid disease), and time of residence in endemic goitre areas. Information on medical history included questions on episodes of thyroiditis, benign nodules (adenomas), goitre, hyper- or hypothyroidism and other unspecified thyroid disease, diagnosed more than one year before the index diagnosis, and history of any radiotherapy.

Benign pathologies were combined in a single variable (any benign thyroid disease) for the purpose of the present analysis.

The food frequency questionnaire comprised 29 items, includ- ing questions on intake of refined cereals, such as bread, pasta, rice and polenta; the frequency of their total intake was com- puted by adding single weekly frequencies. Details of the food frequency questionnaire have been given elsewhere.24 The reproducibility of the questionnaire was satisfactory.27 Beta- carotene intake was computed from the frequency of weekly intake of the main vegetables and fruit, using standard Italian food composition tables.28In this population a high intake of refined cereals and low consumption of vegetables and fruit may be considered indicative of a generally poorer diet, i.e. also poor in several other aspects.

Data analysis

Odds ratios (OR) of thyroid cancer, and the corresponding 95% confidence intervals (CI), were derived using unconditional multiple logistic regression.29The model included terms for age

at diagnosis, sex, education, history of benign thyroid disease, radiotherapy, residence in endemic goitre areas, and intake of refined cereals and beta-carotene.

Using the multivariate OR and the distribution of the risk factors in the cases, percentage PAR were computed, i.e. the proportion of thyroid cancers that would be avoided if all sub- jects were unexposed, or exposed to the level associated with the lowest risk. The method described by Bruzzi et al.30implies knowledge of the risk estimates and of the joint distribution of the risk factors in the population of cases only, and thus can be used for hospital-based case-control studies. The PAR were expressed as per cent terms, and their variance calculations and 95% CI were obtained as described by Benichou and Gail31for each separate risk factor and for various combinations of them whenever computationally possible.32

Results

Table 1 gives the distribution of thyroid cancer cases and the comparison group according to age, sex and other risk factors.

Table 2 gives the corresponding multivariate OR according to various risk factors in the overall dataset and in strata of sex, age, and major histological types (papillary and follicular carcinomas). History of any benign thyroid disease was consist- ently associated with cancer risk (OR = 7.6), with an apparently stronger association in men (OR = 37.1) than women (OR = 6.2), Table 1 Distribution by sex of 399 thyroid cancer cases and 617 controls according to age and other risk factors. Italy, 1986–1992

Thyroid cancer

cases Controls

Women Men Women Men

Age at diagnosis (years)

,40 115 37 157 74

40–54 95 39 130 65

>55 81 32 140 51

Education (years)

,7 133 45 228 69

>7 158 63 199 121

Benign thyroid diseases

No 220 92 407 189

Yes 71 16 20 1

Radiotherapy

No 276 105 412 186

Yes 15 3 15 4

Residence in endemic goitre area (years)

Never or ,20 266 101 405 178

>20 25 7 22 12

Refined cereal intake (portions/week)a

,14.5 72 9 162 30

14.5–,22 130 38 158 67

>22 89 61 107 93

Beta-carotene intake (µg/week)a

>36 380 85 32 152 54

24 370–,36 380 93 32 148 58

,24 370 113 44 127 78

aApproximate tertiles of intake.

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while there was no real heterogeneity across strata of age and histological types. History of radiotherapy and residence for

>20 years in endemic goitre areas also increased thyroid cancer risk (OR = 1.4 for both). The association with radiotherapy was apparently stronger at younger age (OR = 2.0 for patients aged ,45 years). The OR was 2.0 for the highest tertile of refined cereal intake compared to the lowest, and 1.4 for the lowest intake of beta-carotene compared to the highest, with no heterogeneity across strata of the selected covariates.

The PAR for selected risk factors and their combinations are shown in Table 3, assuming all subjects could be moved to the lowest exposure levels. History of any benign thyroid disease accounted for 18.9% of thyroid cancer cases, history of radio- therapy for 1.2% and long-term residence in endemic goitre area for 2.4%. The latter two estimates, however, were not significant.

The selected indicator of a poor diet explained 40.9% of cases.

Although the OR for benign thyroid diseases was higher in men than women, the proportion of thyroid cancer cases attributable to any benign thyroid disease was higher among women (PAR 20.5% compared to 14.4% in men), due to the higher fre- quency of the diseases among women; the PAR for any benign thyroid disease were higher among younger subjects (21.0%) and among patients with follicular carcinoma (26.5%). The PAR for the combination of a high intake of refined cereals and low beta-carotene was higher in men (81.1%) than women (33.2%) and at age >45 years (57.7%, compared to 28.4% at age ,45).

The combination of radiotherapy, residence in endemic goitre areas and any benign thyroid diseases accounted for 21.7% of cases. The combination of all variables accounted for 57.5% of thyroid cancer cases and was very similar in women (58.6%) and men (58.3%), and apparently higher at age >45 (63.8%)

than in younger subjects (52.7%). With reference to the main histological types considered, the overall PAR were somewhat higher for follicular (69.1%) than papillary carcinomas (53.7%).

Discussion

This study indicates that in this Italian population, more than half of thyroid cancer cases may be accounted for by a combina- tion of a few identifiable factors or risk factor correlates such as a history of any benign thyroid disease, history of radiotherapy, long-term residence in endemic goitre areas and some basic indicators of a poor diet.

History of residence in endemic goitre areas, although a well recognized factor for the disease,24accounted only for a small proportion of thyroid cancers, and the corresponding estimate was not significant. Such a proportion, however, may have been underestimated by the fact that current residence was com- parable for cases and controls, and current residence in Italy is strongly correlated to past one. Likewise, the PAR for radio- therapy was not significant. A minimum latency of 3 years was considered between radiation and diagnosis of thyroid cancer, but our definition of radiotherapy included not only conditions requiring heavy exposure (angioma of the neck, thyroid nod- ules, enlarged thymus) but also degenerative arthritis (mainly of the neck) which implied relatively low-dose irradiation of the anterior wall.26History of any benign thyroid disease, although strongly associated in terms of OR, accounted for less than 20%

of thyroid cancer cases. Although the OR for the combination of selected indicator foods was only moderately elevated, this explained over 40% of thyroid cancer cases, suggesting the theoretical scope for dietary intervention on thyroid cancer.

Table 2 Odds ratios with 95% confidence interval (CI) of 399 cases of thyroid cancer and 617 controls according to selected risk factors. Italy, 1986–1992

Odds ratios (95% CI)a

Sex Age (years) Histological type

All Women Men ,45 >45 Papillary Follicular

Any benign thyroid diseases

No 1c 1c 1c 1c 1c 1c 1c

Yes 7.6 (4.6, 12.6) 6.2 (3.6, 10.6) 37.1 (4.7, 291.3) 9.3 (4.4, 19.7) 6.5 (3.2, 12.9) 7.6 (4.5, 13.1) 11.6 (5.6, 23.8) Radiotherapy

No 1c 1c 1c 1c 1c 1c 1c

Yes 1.4 (0.7, 2.8) 1.4 (0.6, 3.0) 1.3 (0.3, 6.2) 2.0 (0.6, 6.8) 1.1 (0.5, 2.6) 1.5 (0.7, 3.3) 2.0 (0.6, 6.4) Residence in endemic goitre areas (years)

No or ,20 1c 1c 1c 1c 1c 1c 1c

>20 1.4 (0.8, 2.5) 1.7 (0.9, 3.2) 1.2 (0.4, 3.5) 2.2 (0.9, 5.7) 1.2 (0.6, 2.4) 1.4 (0.8, 2.7) 2.3 (0.9, 5.7) Refined cereal intake (portions/week)b

,14.5 1c 1c 1c 1c 1c 1c 1c

14.5–,22 1.9 (1.4, 2.7) 2.0 (1.3, 2.9) 2.3 (0.9, 5.7) 1.6 (0.9, 2.6) 2.5 (1.5, 4.1) 1.8 (1.2, 2.7) 2.6 (1.2, 5.4)

>22 2.0 (1.4, 2.9) 2.0 (1.3, 3.1) 2.5 (1.0, 6.0) 2.0 (1.2, 3.6) 2.2 (1.3, 3.7) 2.2 (1.4, 3.3) 2.3 (1.0, 5.0) Beta-carotene intake (µg/week)b

>36 380 1c 1c 1c 1c 1c 1c 1c

24 370–,36 380 1.0 (0.7, 1.4) 1.0 (0.6, 1.4) 1.0 (0.5, 1.9) 1.0 (0.6, 1.5) 1.0 (0.6, 1.7) 0.8 (0.6, 1.2) 0.9 (0.4, 1.8) ,24 370 1.4 (1.0, 1.9) 1.6 (1.1, 2.4) 0.9 (0.5, 1.6) 1.3 (0.8, 2.1) 1.5 (0.9, 2.4) 1.2 (0.8, 1.8) 1.6 (0.8, 3.0)

aEstimates from multiple logistic regression equations, including terms for age, sex, education and all the variables included in the Table.

bApproximate tertiles of intake.

cReference category.

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An inverse relation with vegetable and fruit intake was consistently observed in several studies.6,7,24,26In this Italian population, high starch intake may simply be an indicator of a diet poor in several aspects, possibly also iodine, whose defici- ency is related to both benign and malignant thyroid diseases.2 A diet poor in vegetables and fruit and rich in starches may also be correlated to non-dietary risk factors, although allowing for education—as an indicator of socioeconomic status—did not notably modify the observed association.

Our general definition of benign thyroid disease includes conditions strongly related to cancer risk (goitre and nodules) and others less strongly related (hyperthyroidism and thyroiditis).2,5,6,9The absolute number of cases for each benign disease was too low to allow separate PAR estimations. The overall estimate in any case is a weighted average of the strength of the association and prevalence of various diseases and should therefore provide, at least in first approximation, a measure of the role of all benign thyroid disease at the popu- lation level.

With reference to OR estimates, this study has some limita- tions as well as several strengths typical of hospital-based case- control studies.33This is one of the largest case-control studies of thyroid cancer to date; only acute conditions, unrelated to known or likely risk factors for thyroid cancer, were included in the comparison group; the distribution of cases and controls was comparable in terms of area of current residence, and the participation of cases and controls was almost complete, thus limiting the extent of any potential selection bias. However, the areas under investigation were not covered by cancer registry and total numbers of incident cases are unidentified.

The upper age limit at 75 years, introduced to increase reliability of information collected, has led to the exclusion of less than 15% of cases in this population.34The potential confounding

effect of several covariates was allowed for in the analysis, although allowance for confounding may have been incom- plete, on account of computational constraints in the size of the matrix for estimation of variance.31,32Any such underadjust- ment, however, should be limited, since the PAR estimates were practically unchanged when different terms were introduced in the models. Furthermore, the PAR for dietary factors are very likely underestimated, since in the absence of an unexposed category, these are influenced by the definition of quantiles of intake or any other arbitrary cut-off, and consequently by the shape of the dose-risk relationship.

Computation of PAR implies that the cases are representative of all cases in the population studied.30Such an assumption is reasonable, since cases were identified in the major teaching and general hospitals of the areas under surveillance, although in the absence of a cancer registry the exact proportion of cases interviewed is not known. To improve the reliability and validity of the information collected,27we included only sub- jects below age 75 years, so the PAR applied to this age group only.

Although the causal relationship for some of the risk factors considered remains open to discussion, since they may re- present indicators of risk, and although their modification is not obvious, intervention on a few identified and potentially modifiable conditions is likely to be relevant on a public health scale. In 1994 in Italy there were about 400 deaths from thyroid cancer in women and 200 in men.35 Surveillance of benign thyroid diseases, supplementing iodine in the diet in endemic goitre areas and some modification in the diet (useful also in the prevention of other more common chronic diseases) are likely to avoid over 300 deaths per year in Italy, mainly in younger women, thus indicating the scope and importance of preventive health measures for this disease.2,3

Table 3 Per cent attributable risksawith 95% confidence interval (CI), according to selected risk factors in strata of selected covariates. Italy, 1986–1992

Per cent attributable risks (95% CI)a

Sex Age (years) Histological type

All cases Women Men ,45 >45 Papillary Follicular

Benign thyroid diseases 18.9 20.5 14.4 21.0 17.0 19.4 26.5

(14.6, 23.3) (15.0, 26.0) (7.6, 21.2) (14.7, 27.3) (10.9, 23.1) (14.1, 24.6) (15.4, 37.6)

Radiotherapy 1.2 1.4 0.7 2.0 0.4 1.7 2.8

(–1.5, 3.9) (–2.0, 4.8) (–3.1, 4.5) (–1.3, 5.4) (–3.8, 4.6) (–1.5, 5.0) (–3.3, 8.9)

Residence in endemic goitre areas 2.4 3.4 1.2 3.5 1.7 2.3 6.6

(–1.2, 6.0) (–0.9, 7.7) (–4.9, 7.4) (–0.6, 7.7) (–4.1, 7.5) (–1.8, 6.4) (–1.9, 15.0)

Indicator of poor dietb 40.9 33.2 81.1 28.4 57.7 24.5 67.2

(14.4, 67.5) (2.6, 63.8) (42.2, 120.0) (–12.1, 68.9) (25.4, 90.1) (–10.7, 59.8) (27.1, 107.2) Benign thyroid diseases

and goitre area 20.7 22.8 15.5 23.3 18.6 21.0 31.9

(15.5, 25.8) (16.6, 29.1) (11.0, 26.2) (15.0, 27.1) (19.3, 44.5)

Radiotherapy, goitre area

and benign thyroid diseases 21.7 24.0 16.2 24.7 18.7 22.3 34.4

Benign thyroid diseases

and indicator of poor dietb 56.0 56.7 57.5 50.4 63.0 51.8 66.1

All the above 57.5 58.6 58.3 52.7 63.8 53.7 69.1

aBased on OR reported in Table 2, after allowance for age, sex and all variables included in the Table.

bPoor diet is defined as a high intake of refined cereals and low intake of beta-carotene.

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Acknowledgements

This work was conducted with the contribution of the Italian Association for Cancer Research, Milan. The authors thank Mrs J Baggott, MP Bonifacino and the GA Pfeiffer Memorial Library staff for editorial assistance.

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