IJC

International Journal of Cancer

Thyroid cancer mortality and incidence: A global overview

Carlo La Vecchia1, Matteo Malvezzi2, Cristina Bosetti2, Werner Garavello3, Paola Bertuccio2, Fabio Levi4 and Eva Negri2
1
Department of Clinical Sciences and Community Health, Universita degli Studi di Milano, Milan, Italy
2
Department of Epidemiology, IRCCS-Istituto di Ricerche Farmacologiche “Mario Negri”, Milan, Italy
3
Clinica Otorinolaringoiatrica, Department of Surgery and Translational Medicine, Universit
a degli Studi di Milano Bicocca, Milan, Italy
4
Institute of Social and Preventive Medicine (IUMSP), Lausanne University Hospital, Lausanne, Switzerland

In most areas of the world, thyroid cancer incidence has been appreciably increasing over the last few decades, whereas mortal-
ity has steadily declined. We updated global trends in thyroid cancer mortality and incidence using official mortality data from
the World Health Organization (1970–2012) and incidence data from the Cancer Incidence in Five Continents (1960–2007). Male
mortality declined in all the major countries considered, with annual percent changes around 22/23% over the last decades.
Only in the United States mortality declined up to the mid 1980s and increased thereafter. Similarly, in women mortality declined
in most countries considered, with APCs around 22/25% over the last decades, with the exception of the UK, the United States
and Australia, where mortality has been declining up to the late 1980s/late 1990s to level off (or increase) thereafter. In 2008–
2012, most countries had mortality rates (age-standardized, world population) between 0.20 and 0.40/100,000 men and 0.20
and 0.60/100,000 women, the highest rates being in Latvia, Hungary, the Republic of Moldova and Israel (over 0.40/100,000)
for men and in Ecuador, Colombia and Israel (over 0.60/100,000) for women. In most countries, a steady increase in the inci-
dence of thyroid cancer (mainly papillary carcinomas) was observed in both sexes. The declines in thyroid cancer mortality reflect
both variations in risk factor exposure and changes in the diagnosis and treatment of the disease, while the increases in the inci-
dence are likely due to the increase in the detection of this neoplasm over the last few decades.

About 230,000 new cases of thyroid cancer were estimated in but relatively smaller in men.1 Incidence rates are more than
2012 among women and 70,000 among men, with an age- twofold higher in high-income countries as compared to low/
standardized (world population) rate of 6.10/100,000 women middle-income ones both in women (11.10/100,000 and 4.70/
and 1.90/100,000 men.1 International comparisons are com- 100,000, respectively) and in men (3.60/100,000 and 1.40/
plex due to differences in diagnosis and ascertainment of the 100,000, respectively). Globally in 2012, estimated numbers
disease. In any case, there is an over tenfold difference in of deaths from thyroid cancer were 27,000 in women and
incidence across different parts of the world in women, high- 13,000 in men, corresponding to mortality rates of approxi-
incidence areas (over 10/100,000 women) including selected mately 0.6/100,000 women and 0.3/100,000 men.
countries of South and North America, Italy in Europe, Japan In most countries, incidence rates have been appreciably
increasing over the last few decades,2,3 and if recent trends

Epidemiology
and the Pacific Islands; the absolute variation is substantial,
are maintained, thyroid cancer may become the fourth most
Key words: incidence, joinpoint analysis, mortality, thyroid cancer, common cancer by 2030 in the United States.4 Such an
trends increase is likely due to improved ascertainment, diagnosis
Abbreviations: APC: annual percent change; EU: European and certification, and largely or totally reflects overdiagnosis
Union; ICD: International Classification of Diseases; WHO: World of indolent disease, i.e., small papillary carcinomas.2,3,5 Con-
Health Organization versely, mortality rates have been steadily declining in most
Additional Supporting Information may be found in the online areas of the world,6–8 likely due to improved diagnosis, man-
version of this article. agement and treatment of the disease. Survival, particularly
Grant sponsor: Italian Association for Cancer Research (AIRC); for papillary carcinoma (i.e., the most frequent histotype in
Grant number: 10264; Grant sponsor: Swiss Leagues Against (young) women) is in fact extremely good (over 98% five-
Cancer; Grant sponsor: Swiss Foundation for Research Against year survival rate in Europe or North America), resulting in
Cancer (KFS); Grant number: 2437-08-2009 comparatively low mortality rates.
DOI: 10.1002/ijc.29251 In order to provide an updated overview of trends in
History: Received 1 Aug 2014; Accepted 30 Sep 2014; Online 4 Oct mortality from thyroid cancer in European countries and
2014 selected other areas of the world, we have analyzed death cer-
Correspondence to: Cristina Bosetti, Department of Epidemiology, tification data over the period 1970–2012. For a few larger
IRCCS-Istituto di Ricerche Farmacologiche "Mario Negri", Via Giu- countries with long-term cancer registration data, we have
seppe La Masa 19-20156 Milan, Italy, Tel.: 139-0239014526, Fax: also analyzed trends in incidence by major histotypes over
139–0233200231, E-mail: cristina.bosetti@marionegri.it the period 1960–2007.

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 2188 Thyroid cancer mortality and incidence

What’s new?
Trends in thyroid cancer incidence and mortality vary widely by country, but for most areas of the world, the data indicate an
upward trend in incidence and a downward trend in mortality. Those trends are supported by the present analysis of thyroid
cancer mortality and incidence globally. The analyses are based on data maintained by the World Health Organization (1970–
2012) and Cancer Incidence in Five Continents (1960–2007). The authors attribute the rise in thyroid cancer incidence to
increased detection of the disease and the decline in mortality to changes in diagnosis, treatment, and risk factor exposure.

Material and Methods In order to identify significant changes in mortality trends

Mortality for selected countries worldwide, we performed joinpoint
Official data for thyroid cancer mortality in 28 European regression analysis allowing for up to three joinpoints.16 For
countries and in 20 countries from other areas of the world each of the identified trends, we computed the estimated
were derived from the World Health Organization (WHO) annual percent change (APC) by fitting a regression line to
online database, for the period 1970–2012.9 We did not con- the natural logarithm of the rates using calendar year as a
sider a few former Soviet Union countries (i.e., Armenia, regression variable. We also calculated the average APC,
Azerbaijan, Georgia, Kazakhstan, Kyrgyzstan and Uzbekistan) based on an underlying joinpoint model estimated as the
which had low national death certification coverage and com- geometric weighted average of the APCs, with the weights
pleteness; Albania, Belarus, the Russian Federation and equal to the lengths of each time interval segment.17
Ukraine, which had no recent data; and a few other Euro-
pean countries (i.e., Iceland, Malta and Luxemburg) which Incidence
had a limited number of deaths (<10 per year in the two Incidence data for thyroid cancer overall and by major histo-
sexes combined). In the American continent, 13 countries logical types (i.e., follicular and papillary carcinoma) were
with satisfactory death certification coverage and complete- obtained from the Cancer Incidence in Five Continents data-
ness were included (i.e., Canada, the United States, Argen- base18 over the period 1960–2007. For countries with more
tina, Brazil, Chile, Colombia, Costa Rica, Cuba, Ecuador, than one cancer registry, data were aggregated to ensure the
Mexico, Puerto Rico, Uruguay and Venezuela). Mortality highest geographic coverage, and the analyses were restricted
data from thyroid cancer were also available for five Asian to the longest common calendar period between registries.
countries (i.e., Hong Kong, Israel, Japan, the Republic of The following countries and registries were considered: Den-
Korea and Singapore) and for Australia and New Zealand. mark (1978–2007); France (1988–2007): Bas-Rhin, Calvados,
Since three different Revisions of the International Classi- Doubs, Haut-Rhin, Herault, Isere, Somme, Tam; Germany
fication of Diseases (ICD) were used in the period consid- (1970–2007): Saarland; Italy (1993–2007): Ferrara province,
ered, we extracted, as applicable, those corresponding to the Varese province, Modena, Parma, Ragusa province, Romagna,
codes ICD-8 193,10 ICD-9 19311 and ICD-10 C73.12 Sassari province, Torino; the Netherlands (1989–2007); Spain
Epidemiology

For most countries, population figures based on official (1993–2007): Albacete, Cuenca, Girona, Granada, Murcia,
censuses were obtained from the same WHO database9; only Navarra, Tarrangona; the UK (1988–2007): East of England
for a few countries of the Americas, population data were region, Birmingham and West Midlands, Merseyside and
retrieved from the Pan American Health Organization Cheshire, England North Western, Oxford, England South
(PAHO) database.13,14 and Western regions, Yorkshire; United States (1975–2007):
We computed country- and sex-specific mortality rates SEER 9 registries; Hong Kong (1983–2007); Israel (1963–
for each 5-year age group and calendar period and derived 2007): Jews; Japan (1978–2007): Miyagi prefecture, Osaka
age-standardized rates by the direct method, using the world prefecture; Australia (1983–2007): New South Wales, Queens-
standard population, at all ages and truncated at 35–64 land, Tasmania, Victoria, South Australia, West Australia).
years (i.e., a widely adopted definition of middle-age popula- Three-year moving averages were used to represent the his-
tion15). For the European Union (EU) as a whole, rates tology- and sex-specific incidence trends in age-standardized
were computed using the aggregated number of deaths in incidence rates (direct method, world standard population).
its 28 member states as defined in June 2014, and the cor-
responding populations; Cyprus was excluded as mortality Results
data were available for a limited number of (recent) years Table 1 gives the overall age-standardized mortality rates
only. Interpolation of missing data was only made for the from thyroid cancer in men and women in 28 European
construction of the overall EU rates; when data were not countries, the EU as a whole, and other selected areas of
available for a country, the nearest available figures (i.e., the world around 2000 (1998–2002) and 2010 (2008–2012),
generally those of the previous or subsequent year) were with corresponding percent changes. In 2000, most coun-
replicated. tries had mortality rates between 0.20 and 0.40/100,000 in

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Table 1. Age-adjusted (world population) death rates from thyroid cancer at all ages around 2000 (1998–2002) and around 2010 (2008–
2012) in 48 countries worldwide plus the European Union, with corresponding percent changes
Men Women
No. of No. of
deaths % Change deaths % Change
Country 2000 2010 (2010) 2010/2000 2000 2010 (2010) 2010/2000
Europe
Austria 0.52 0.39 29 225.93 0.61 0.32 43 247.33
Belgium 0.32 0.30 33 25.64 0.51 0.32 48 237.43
Bulgaria 0.36 0.32 21 213.13 0.47 0.33 33 229.30
Croatia 0.40 0.35 13 212.77 0.49 0.39 24 220.51
Czech Republic 0.42 0.33 30 220.86 0.61 0.32 47 247.87
Denmark 0.32 0.26 13 218.74 0.38 0.27 21 228.09
Estonia –1 –1 – – 0.66 0.49 13 225.61
Finland 0.41 0.34 19 214.99 0.42 0.35 32 215.55
France 0.31 0.25 144 218.54 0.35 0.25 249 229.64
Germany 0.44 0.33 296 224.64 0.48 0.31 419 236.03
Greece 0.25 0.22 29 211.04 0.25 0.28 48 13.30
Hungary 0.55 0.43 34 221.83 0.57 0.42 57 226.96
Ireland 0.28 0.28 9 21.20 0.40 0.31 12 223.64
Italy 0.40 0.35 224 212.19 0.46 0.36 347 221.88
Latvia 0.40 0.51 8 26.18 0.89 0.59 20 233.67
Lithuania 0.55 0.39 8 229.54 0.69 0.42 21 239.06
Netherlands 0.28 0.23 35 219.06 0.35 0.32 69 28.64
Norway 0.34 0.29 14 214.83 0.45 0.26 19 241.07
Poland 0.33 0.27 77 217.52 0.56 0.38 181 231.35
Portugal 0.28 0.32 32 15.71 0.40 0.37 62 27.47
Republic of Moldova 0.28 0.42 8 49.91 0.53 0.52 13 21.77
Romania 0.33 0.30 52 26.52 0.43 0.43 102 20.11
Slovakia 0.38 0.32 12 215.36 0.50 0.38 22 225.22
Slovenia 0.49 0.38 6 222.20 0.43 0.19 7 256.13

Epidemiology
Spain 0.28 0.26 109 26.68 0.34 0.30 195 210.70
Sweden 0.30 0.31 31 5.23 0.33 0.30 44 27.56
Switzerland 0.36 0.30 23 217.81 0.45 0.27 35 241.28
United Kingdom 0.21 0.22 136 4.80 0.28 0.25 209 210.63
European Union 0.34 0.30 1381 213.69 0.43 0.32 2333 223.82
America
Argentina 0.25 0.23 58 28.46 0.35 0.30 113 213.23
Brazil 0.19 0.20 196 4.42 0.33 0.29 390 212.54
Canada 0.22 0.20 72 28.47 0.21 0.18 102 214.69
Chile 0.33 0.24 26 228.25 0.55 0.52 73 26.39
Colombia 0.34 0.32 65 27.42 0.54 0.64 168 17.77
Costa Rica 0.15 0.24 6 66.89 0.57 0.32 9 243.94
Cuba 0.19 0.20 23 4.73 0.38 0.35 40 26.90
Ecuador 0.27 0.37 29 36.34 0.65 0.77 72 17.77
Mexico 0.32 0.33 161 2.23 0.62 0.59 395 24.42
Puerto Rico –1 –1 – – 0.19 0.15 10 223.87

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 2190 Thyroid cancer mortality and incidence

Table 1. Age-adjusted (world population) death rates from thyroid cancer at all ages around 2000 (1998–2002) and around 2010 (2008–
2012) in 48 countries worldwide plus the European Union, with corresponding percent changes (Continued)
Men Women
No. of No. of
deaths % Change deaths % Change
Country 2000 2010 (2010) 2010/2000 2000 2010 (2010) 2010/2000
United States 0.23 0.25 713 8.09 0.23 0.24 967 6.76
Uruguay 0.24 0.36 8 47.94 0.35 0.24 11 230.77
Venezuela 0.25 0.23 33 25.05 0.41 0.42 67 3.45
Asia
Hong Kong 0.30 0.31 19 4.59 0.43 0.29 23 231.37
Israel 0.46 0.42 20 29.04 0.64 0.62 39 23.30
Japan 0.33 0.31 533 26.08 0.47 0.39 1066 215.97
Republic of Korea 0.38 0.35 107 27.04 0.59 0.54 254 29.46
Singapore 0.38 0.27 6 229.30 0.76 0.56 17 226.80
Oceania
Australia 0.26 0.23 44 211.36 0.27 0.30 72 14.00
New Zealand 0.26 0.30 10 14.54 0.33 0.29 13 213.21
1
Rates were not reported, since there were five or less deaths.
Epidemiology

Figure 1. Age-standardized (world population) death rates from thyroid cancer at all ages per 100,000 men and women in 48 countries
worldwide plus the European Union, 2008–2012.

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Figure 2. Trends in age-standardized (world population) death rates from thyroid cancer per 100,000 men (all ages and age 35–64 years)
in selected countries worldwide, 1970–2012. All ages ; truncated at 35–64 years .

men and between 0.20 and 0.60/100,000 in women. Male Geographic patterns and time trends between 2000 and
rates were 0.34/100,000 in the EU, 0.23/100,000 in the 2010 in middle-age population (35–64 years) were consistent

Epidemiology
United States and 0.33/100,000 in Japan; corresponding fig- with all ages ones (Supporting information Table 1 and Sup-
ures in women were 0.43, 0.23 and 0.47/100,000, respec- porting information Fig. 1).
tively. Between 2000 and 2010, mortality declined in several Figure 2 and Supporting information Table 2 show the
countries worldwide, particularly in women. Some increases results for the joinpoint analysis of age-standardized mortal-
were, however, observed in Estonia, Latvia, Portugal, Mol- ity rates from thyroid cancer (at all ages and at age 35–64)
dova, Sweden, the UK, most countries of the Americas in men from 11 countries worldwide and the EU as a
including the United States, Hong Kong and New Zealand whole between 1970 and 2012. Trends in male overall mor-
for men and in Greece, Colombia, Ecuador, the United tality have been declining in most countries considered,
States, Venezuela and Australia for women. In 2010, most with APC around 22/23% over the last decades. Only in
countries still had mortality rates between 0.20 and 0.40/ Spain, mortality has been increasing up to the early 1990s
100,000 men and 0.20 and 0.60/100,000 women (Table 1 to level off thereafter, while in the United States mortality
and Fig. 1). The highest mortality rates were in Latvia, has been declining up to the mid 1980s and has been mod-
Hungary, the Republic of Moldova and Israel (over 0.40/ erately increasing thereafter. Trends were consistent in
100,000) for men and in Ecuador, Colombia and Israel middle-aged men. Similarly, in women overall and trun-
(over 0.60/100,000) for women; the lowest ones were in cated mortality was declining in most countries considered,
Cuba, Canada, Brazil and Puerto Rico (0.20/100,000) for with APCs around 22/25% over the last decades (Fig. 3
men and Slovenia, Canada and Puerto Rico (below 0.20/ and Supporting information Table 2), with the exception
100,000) for women. In the EU, the United States and the UK, the United States and Australia, where mortality
Japan, rates in 2010 were 0.30, 0.25 and 0.31/100,000 men has been declining up to the late 1980s/late 1990s to level
and 0.32, 0.24 and 0.39/100,000 women, respectively. off (or even increase) thereafter.

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 2192 Thyroid cancer mortality and incidence

Figure 3. Trends in age-standardized (world population) death rates from thyroid cancer per 100,000 women (all ages and age 35–64
years) in selected countries worldwide, 1970–2012. All ages ; truncated at 35–64 years .

Trends in incidence rates for thyroid cancer overall and ous rise in the incidence of thyroid cancer over the last few
for papillary and follicular carcinomas over the period 1960– decades in various countries worldwide.
Epidemiology

2007 in selected countries worldwide are given in Figure 4 The patterns and trends in mortality from thyroid cancer
for men and Figure 5 for women. In most countries consid- reflect both variations in risk factor exposure over geographic
ered, a steady increase in the incidence of thyroid cancer was areas and time periods and changes in the diagnosis and
observed in both men and women. Such an increase mainly treatment of the disease. Thus, several high mortality areas
reflected the rise in the incidence of papillary carcinomas include regions with (past) iodine deficiency or excess iodine
(i.e., the most frequent histotype), while incidence for follicu- intake,19–22 where the frequency of benign thyroid diseases—
lar carcinomas was much lower and remained approximately a major recognised risk factor for thyroid cancer23—was
stable over the period considered. high. In a pooled analysis of thyroid cancer studies world-
wide,23 goitre and benign-nodules/adenomas were the strong-
Discussion est risk factors for thyroid cancer on a population level.
There are three main messages in the present updated analy- Excess risks were observed for both men and women and in
sis of thyroid cancer mortality and incidence, including: (i) relation to both papillary and follicular cancers, with relative
the persistent appreciable variability in thyroid cancer death risks around 5. Consequently, the substantial decline in
rates worldwide, most high mortality countries being in Cen- iodine deficiency prevalence in most countries—particularly
tral America and Asia, but also central and eastern Europe, in low and middle-income areas—may explain the favorable
and those with low rates in western Europe and North trends in thyroid cancer mortality.
America; (ii) the persistent fall in death rates for both sexes Other improvements in diet over the last few decades—
in most previous high mortality areas, but a leveling of rates including a diet richer in vegetables, (micro) nutrients, flavo-
over the last two decades in lowest mortality countries of noids and other food components22—may also have contrib-
North America and northern Europe; and (iii) the continu- uted to the widespread thyroid cancer mortality declines.

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La Vecchia et al. 2193

Figure 4. Trends in age-standardized (world population) incidence rates per 100,000 men for thyroid cancer overall and by major histological
types in selected countries worldwide, 1960–2007. All thyroid cancers ; papillary carcinoma and follicular carcinoma .

While it is now clear that vegetables—including cruciferous It is much more complex to define the risk factors for fol-
ones—have a favorable effect on thyroid cancer,24,25 the asso- licular,29 medullary30 and anaplastic thyroid cancers, and
ciations are relatively modest. The role of fish consumption hence to prevent—and avoid deaths from—these thyroid can-

Epidemiology
appears to be favorable in endemic goitre populations,26 cer subtypes. Likewise, the management and prognosis of
thought not in coastal areas with high iodine intake. A recent these histotypes of thyroid cancer are substantially less favor-
review on fish and thyroid cancer,25 however, reported no able than for papillary ones, and this may account for a back-
consistent association. Likewise, findings on single nutrients, ground, though low, stable level of thyroid cancer mortality
macronutrients and vitamins are limited and inconsistent observed in several low mortality areas.
and therefore no conclusion based on dietary patterns can be In contrast to the declines in mortality from thyroid can-
derived to interpret mortality trends in incidence and cer, steady rises have been observed in the incidence of this
mortality.22 neoplasm (particularly of the papillary subtypes) in many
Another major risk factor for thyroid cancer is ionising countries worldwide over the last decades. Known or likely
radiation, particularly in childhood and adolescence, with a risk factors for thyroid cancer have not been increasing in
summary excess RR around 7 per Gray (Gy).27,28 It is likely the last few decades, but, if any, they have been favorably
that reduced utilisation and better control of irradiation for changing, as discussed above. Thus, the rise in thyroid cancer
medical conditions, particularly in childhood, has lead to a incidence does not appear to reflect a real increase in the
subsequent decline of thyroid cancer mortality. occurrence of this neoplasm, but it is more likely due to a
The leveling off for low mortality rates (about 0.20/ substantial increment in the detection of subclinical thyroid
100,000) in the United States, the UK, Australia, and other cancers (such as small papillary carcinomas) over the last
selected European countries indicates that such a favorable decades, particularly in young women.2,4,31 Indeed, diagnostic
pattern in risk factor exposure and disease management is techniques for thyroid cancer have become more sensitive,
approaching an asymptote for most frequent good prognosis particularly through the use of ultrasounds, ultrasound-
papillary cancers. guided fine-needle aspiration and computed tomography

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 2194 Thyroid cancer mortality and incidence

Figure 5. Trends in age-standardized (world population) incidence rates per 100,000 women for thyroid cancer overall and by major histological
types in selected countries worldwide, 1960–2007. All thyroid cancers ; papillary carcinoma and follicular carcinoma .

scan, which can detect thyroid nodules as small as 0.2 cm. Thus, the diverging trends in the incidence of and mortal-
An important role of “overdiagnosis” is also supported by a ity from thyroid cancer, and the possible relevant role of
shift in the stage distribution of this neoplasm toward earlier “overdiagnosis”, indicate the need to better distinguish the
stages reported in a few US studies.2,3 This has led to a mas- (few) high-risk patients who necessitate treatment from those
Epidemiology

sive overtreatment of thyroid lesions with excellent prognosis (probably most) patients who may not need treatment.
(such as small asymptomatic papillary cancers), but probably
also to a fall in mortality due to the treatment of a subgroup Acknowledgement
of lesions with unfavorable prognosis. The authors thank Mrs. I. Garimoldi for editorial assistance.

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