Cancer Epidemiology 44S (2016) S23–S42

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Cancer Epidemiology
The International Journal of Cancer Epidemiology, Detection, and Prevention

journal homepage: www.cancerepidemiology.net

Cancer patterns and trends in Central and South America$

Mónica S. Sierraa,* , Isabelle Soerjomatarama , Sébastien Antonia , Mathieu Laversannea ,
Marion Piñerosa , Esther de Vriesb , David Formana
a
International Agency for Research on Cancer, Section of Cancer Surveillance, France
b
Department of Clinical Epidemiology and Biostatistics, Pontificia Universidad Javeriana, Bogota, Colombia

A R T I C L E I N F O A B S T R A C T

Article history: Rationale and objective: Cancer burden is increasing in Central and South America (CSA). We describe the
Received 22 March 2016 current burden of cancer in CSA.
Received in revised form 15 July 2016 Methods: We obtained regional and national-level cancer incidence data from 48 population-based
Accepted 21 July 2016
registries (13 countries) and nation-wide cancer mortality data from the WHO (18 countries). We
estimated world population age-standardized incidence and mortality rates per 100,000 person-years.
Results: The leading cancers diagnosed were prostate, lung, breast, cervix, colorectal, and stomach, which
were also the primary causes of cancer mortality. Countries of high/very high human development index
(HDI) in the region experienced a high burden of prostate and breast cancer while medium HDI countries
had a high burden of stomach and cervical cancers. Between countries, incidence and mortality from all
cancers combined varied by 2–3-fold. French Guyana, Brazil, Uruguay, and Argentina had the highest
incidence of all cancers while Uruguay, Cuba, Argentina, and Chile had the highest mortality. Incidence of
colorectum, prostate and thyroid cancers increased in Argentina, Brazil, Chile and Costa Rica from 1997 to
2008, while lung, stomach and cervical cancers decreased.
Conclusion: CSA carries a double-burden of cancer, with elevated rates of infection- and lifestyle-related
cancers. Encountered variation in cancer rates between countries may reflect differences in registration
practices, healthcare access, and public awareness. Resource-dependent interventions to prevent, early
diagnose, and treat cancer remain an urgent priority. There is an overwhelming need to improve the
quality and coverage of cancer registration to guide and evaluate future cancer control policies and
programs.
ã 2015 International Agency for Research on Cancer; Licensee Elsevier Ltd. This is an open access article
under the CC BY-NC-ND IGO 3.0 license (https://creativecommons.org/licenses/by-nc-nd/3.0/igo/).

1. Introduction non-communicable diseases, including cancer [1]. GLOBOCAN

estimates of 2012 indicated that annually 1 million new cancer
Countries in Central and South America (CSA) have undergone cases and 500,000 cancer deaths occurred in CSA; these figures are
significant economic and social changes during the last few expected to nearly double by the year 2030 (1.7 million new cases
decades [1,2]. Declines in reproductive patterns, urbanization and and 1 million cancer deaths) because of ageing and population
increases in life expectancy are leading to major changes in the growth. The cancer profile is changing and cancers such as prostate
population structure and associated increases in the burden of and breast cancer are increasingly common in CSA [3,4] probably
reflecting changes in reproductive and lifestyle factors related to
economic development (i.e. increasing age at first childbirth, lower
$
parity, tobacco smoking, alcohol use, diets low in fruits and
This is an Open Access article published under the CC BY NC ND 3.0 IGO license
which permits users to download and share the article for non-commercial
vegetables, obesity, and physical inactivity) [4–10]. As a result, the
purposes, so long as the article is reproduced in the whole without changes, and region is facing a double cancer burden with high rates of
provided the original source is properly cited. This article shall not be used or infection-related cancers (i.e. cervix, stomach and liver) and an
reproduced in association with the promotion of commercial products, services or increase in (Western) lifestyle related cancers (i.e. prostate, breast,
any entity. There should be no suggestion that IARC endorses any specific
and colorectum) [2–4,11].
organisation, products or services. The use of the IARC logo is not permitted. This
notice should be preserved along with the article’s original URL. Epidemiologic data on the cancer burden from CSA derives
* Corresponding author. mainly from mortality data; information regarding the incidence
E-mail addresses: [email protected], [email protected] of cancer, though improving, remains variable in its availability.
(M.S. Sierra).

http://dx.doi.org/10.1016/j.canep.2016.07.013
1877-7821/ã 2015 International Agency for Research on Cancer; Licensee Elsevier Ltd. This is an open access article under the CC BY-NC-ND IGO 3.0 license (https://
creativecommons.org/licenses/by-nc-nd/3.0/igo/).
S24 M.S. Sierra et al. / Cancer Epidemiology 44S (2016) S23–S42

While the number of population-based cancer registries (PBCR) in 9 oldest cancer registries included in the US National Cancer
CSA has increased in recent years, only a small number have met Institute’s Surveillance, Epidemiology, and End Results (SEER)
the data quality standards to be included in the last edition of Program, which covers approximately 10% of the US population
Cancer Incidence in Five Continents (CI5), covering 8% of the [23]. Similar to the countries in this report, we took mortality rates
population [12]. Statistics on population cancer incidence and for the US from the WHO mortality database [13].
mortality are essential to identify disparities in cancer burden, to Data on human development index (HDI) for the year 2010 were
develop and evaluate cancer control programs, and to guide future obtained from the United Nations Development Programme and
research [8]. In this paper, we provide an overview of cancer the Institut national de la statistique et des études économiques
patterns in CSA, including previously unpublished incidence data. [24,25,27].
The CSA region was sub-classified according to geographic
2. Methods location (Central America, including Cuba, and South America) and
the Global Burden of Disease study [26] (Andean, Central,
The data sources and methods are described in detail in an Southern, Tropical, and Caribbean) (Annex 1 Table A2).
earlier paper in this supplement issue. In brief, we obtained
regional and national-level incidence data from 48 population- 3. Results
based cancer registries in 13 countries; and national mortality data
from the World Health Organization (WHO) mortality database for This study incorporates data from nearly 546,000 new cancer
18 countries [13]. To allow data comparisons across countries, we cases (47% males and 53% females) and more than 2 million cancer
used standard methods to check the incidence data consistency deaths (52% males and 48% females) from CSA between 2003 and
and quality [14]. All incidence data were converted to the latest 2007. Figs. 1–4 show the rankings across all cancer sites between
version of ICD-O (ICD-O-3) [15]; the data were subsequently CSA countries by human development (HDI) for males and females
translated to the 10th edition of the International Classification of in 2003–2007, unless otherwise specified. Prostate, female breast,
Diseases (ICD-10) [16]. Nationwide mortality data from WHO cervix, lung, colorectum, and stomach cancers accounted for 63% of
systematically undergo data verification, and the data are coded in all the incident cases and 49% of all cancer deaths in CSA in both
ICD-10 to avoid misclassification of cancer mortality over time [13]. sexes combined.
Incidence and mortality data were available from most CSA The leading male cancers diagnosed in CSA were prostate, lung,
countries except in Honduras and Guyana where neither incidence colorectal, stomach, and non-Hodgkin lymphoma (NHL); and the
nor mortality data were available; French Guyana and Bolivia leading female cancers were breast, cervix, colorectal, stomach,
where only incidence data were available; and Belize, Guatemala, thyroid, and lung (Figs. 1 and 3). The most frequent cancer deaths
Nicaragua, Panama, Paraguay, Suriname, and Venezuela where were from stomach, prostate, lung, colorectal, and liver cancer
only mortality data were available. We estimated age-standardized among males and breast, cervix, stomach, lung, colorectal, and
incidence (ASR) and mortality (ASMR) rates per 100,000 person- liver cancer among females (Figs. 2 and 4).
years for 30 cancer sites (Annex 1 Table A1) using the direct
method and the world standard population [17,18]. We estimated 3.1. Overall cancer burden
national ASR by aggregating the data from the available cancer
registries using a weighted average of local rates. Our trend The incidence of all cancers combined (excluding non-
analysis was limited to four countries with 10 or more years of data melanoma skin cancer) varied by about 2-fold between CSA
available (Table 1). We chose to present incidence and mortality countries. Males had up to 60% higher incidence of all cancers than
trends only for the countries that had both incidence and mortality females, except in Ecuador, Peru and Mexico (male-to-female
data available in order to distinguish possible determinants of ratios, M:F = 1:1) as well as Bolivia (M:F = 0.5:1) and El Salvador (M:
observable change over time e.g. early detection, risk factor or poor F = 0.4:1). French Guyana, Brazil, and Uruguay had the highest
treatment, despite that the WHO mortality database makes data incidence of all cancers among males (ASR: 297.2–307.1) and
available for several countries in the region. To describe incidence Brazil, Uruguay and Argentina had the highest incidence among
data and mortality time trends, we calculated the estimated annual females (210.8–236.1) whereas for most CSA countries, male
percent change (EAPC) for the 4 countries that provided incidence rates were below 229 and female rates below 200.
permission to use individual year of diagnosis for at least 10- Mortality rates varied by 2–3-fold between countries, and the rates
years (Table 1) using the method proposed by Esteve et al. [19]. All in males were about 2-fold higher than in females, except in
EAPCs were tested for equality to zero by using the corresponding Guatemala, Ecuador, Peru, El Salvador, and Nicaragua (M:F = 1:1).
standard errors, and considered to be statistically significant if the Uruguay, Cuba, and Argentina had the highest mortality of all
p-value
0.05. We used reallocation methods to separate cervix cancers among males (ASMR: 137.3–181.7) and Uruguay, Cuba and
and corpus uteri from imprecisely coded uterine cancer deaths Chile had the highest mortality among females (91.8–98.2),
[20]. We conducted all analyses in Stata version 12.1 (StataCorp) whereas for most CSA countries, mortality rates were below
[21]. 125 among males and below 90 among females (Fig. 5). The
We also present cancer rates for the United States (US) for incidence of all cancers combined remained stable in the
2003–2007 for comparison. While incidence datasets in the CSA 4 countries evaluated (Argentina, Brazil, Chile, and Costa Rica)
region were obtained directly from the registries, we extracted from 1997 to 2008. Mortality declined by about 1.5% per year in
incidence data from CI5 Volume X [22], using data from the both sexes in Chile and by 2% per year in Costa Rican females.

Table 1
Countries and cancer registries included in the analysis of time trends.

Country Name of registries included Period % of the national population covered

Argentina Bahia Blanca 1993–2007 0.8
Brazil Aracaju, Fortaleza, Goiania, Sao Paulo 1997–2006 8.0
Chile Valdivia 1993–2008 2.2
Costa Rica National registry 1985–2007 100.0
 M.S. Sierra et al. / Cancer Epidemiology 44S (2016) S23–S42 S25

Fig. 1. Cancers ranked* by age-standardized incidence rates among males in Central and South America.

Fig. 2. Cancers ranked* by age-standardized mortality rates among males in Central and South America.
S26 M.S. Sierra et al. / Cancer Epidemiology 44S (2016) S23–S42

Fig. 3. Cancers ranked* by age-standardized incidence rates among females in Central and South America.

Fig. 4. Cancers ranked* by age-standardized mortality rates among females in Central and South America.
 M.S. Sierra et al. / Cancer Epidemiology 44S (2016) S23–S42 S27

Stable mortality rates were seen in both sexes in Argentina and increased, again, at different rates for different countries
Brazil and in Costa Rican males (Tables 2 and 3). (Tables 2 and 3).
In males, time trend analysis for Argentina, Brazil, Chile, and Below we briefly describe incidence and mortality patterns for
Costa Rica showed declines in the incidence of lung, oesophageal, several common cancer sites, including those sites with high burden
stomach cancer, and leukaemias (except in Chile) while the and striking regional variations; nearly all cancer sites showed
incidence of prostate, colorectal, and testicular (except in important between-country variations and sex-disparities in cancer
Argentina) cancers increased, at different rates for each country. incidence and mortality (Annex 1 Fig. A1). The accompanying 14
In females, declines in cervical, stomach, and gallbladder cancers cancer site-specific papers in this supplement issue describe in detail
were observed whereas the incidence of breast and thyroid cancers the geographic and temporal patterns for major cancers.

Table 2
Estimated annual percentage change in age-standardized incidence and mortality rates (per 100,000), males.

Argentina (1998–2007) Brazil (1997–2006) Chile (1997–2008) Costa Rica (1997–2007)

Incidencea Mortality Incidencea Mortality Incidencea Mortality Incidencea Mortality

Lip, oral cavity, and pharynx (C00–14) –4.7 –1.9 –0.8 1.1 –3.1 –1.9 –0.4 1.4
Esophagus (C15) –2.3 –2.1 –2.1 0.4 –3.0 –3.8 –1.5 –0.9
Stomach (C16) –0.7 –2.0 –3.9b –1.4 –4.2b –3.3b –4.4b –4.4b
Colorectum (C18–20)c 2.5 0.5 2 2.5 4.1b 1.8 3.1 2.3
Liver (C22) –0.4 –1.2 1.9 2 –1.8 –0.8 0.6 –1.7
Gallbladder (C23–24) –1.1 –0.9 –1.3 0 –2.2 –2.5 –1.5 –1.1
Pancreas (C25) –9.9b 0.2 –2.9 1.4 1.5 0.1 0.3 –0.1
Larynx (C32) –6.0 –2.7 –2.8 –0.3 –4.1 –3.8 –1.9 –2.4
Lung (C33–34) –5.2b –2.1 –3.8b –0.3 –2.0 –1.4 –1.7 –3.6
Melanoma of skin (C43) –0.7 0.5 0.7 0.5 10.2b –2.1 1.5 3.7
Prostate (C61) 4.8b –0.8 2.8b 1.6 3.2b –0.8 3.8b –0.5
Testis (C62) –5.0 0.9 3.8 2.8 4.5b –2.9 4.4 4.6
Kidney (C64) 2.7 1.3 1.4 2.7 7.3b –0.8 1.1 –0.3
Bladder (C67) 2.1 –1.1 –3.3 0.7 –1.4 0.4 –1.4 4.1
Brain, CNS (C70–72) 5.3 0.9 –2.3 1.6 5.1 2 –1.4 –0.6
Thyroid (C73) –2.0 0.9 5.5 –0.04 –1.4 –0.9 4.7 8.9
HL (C81) 1.7 –5.0 –0.5 –2.6 0.4 –7.6 –1.5 –6.1
NHL (C82–85,96) 2.4 –1.0 –0.6 0.4 –2.9 –0.3 1.5 2.8
Leukemia (C91–95) –9.3b –1.4 –3.8 1.2 2.9 –0.9 –3.5 –0.8
Other and unspecified 4.8 –0.9 2.5 –– –3.2 –1.6 –0.1 0.2
All sites but C44 –0.7 –1.0 –0.1 0.7 0.4 –1.5b 0.3 –1.3

HL, Hodgkin lymphoma; NHL, non-Hodgkin lymphoma.

a
Incidence rates were estimated using aggregated data from regional cancer registries.
b
The estimated annual percentage change is statistically different from zero (P
0.05).
c
Mortality data for colorectal cancer also includes the anus (C21).

Table 3
Estimated annual percentage change in age-standardized incidence and mortality rates (per 100,000), females.

Argentina (1998–2007) Brazil (1997–2006) Chile (1997–2008) Costa Rica (1997–2007)

Incidencea Mortality Incidencea Mortality Incidencea Mortality Incidencea Mortality

Lip, oral cavity, & pharynx (C00–14) –7.5 0.1 –0.7 1.3 4.3 0.4 1.4 –1.1
Esophagus (C15) –10.6 –1.0 –0.4 0.2 –5.8 –3.8 –5.7 –8.8
Stomach (C16) –2.8 –2.3 –2.2 –1.3 –3.4 –3.4 –3.5 –4.5
Colorectum (C18–20)b 3.6 0.02 0.9 1.8 1.4 0.5 1.9 1
Liver (C22) 0.2 –2.4 0.04 0.9 –0.9 –0.3 –2.2 –3.5
Gallbladder (C23–24) –2.8 –1.5 –2.6 –1.3 –2.1 –3.2 –3.8 –4.2
Pancreas (C25) 1.6 0.6 –2.3 1.9 –0.8 1.6 –1.8 –1.2
Larynx (C32) –4.3 –1.4 0.2 –0.4 0.9 –3.2 –3.5 –4.0
Lung (C33–34) –4.6 1.9 0.1 2.4 –1.4 1.4 0.6 –3.4
Melanoma of skin (C43) –6.8 2.6 –1.1 1 1.6 –2.1 1.6 –3.3
Breast (C50) –1.8 –0.9 –0.7 0.4 2.5 –1.0 1.7 0.2
Cervix uteri (C53) –6.7c –0.4 –4.2c –0.2 –6.2c –4.4 –5.1c –8.3c
Corpus uteri (C54) –2.3 –3.9 0.3 1.4 –0.8 0.1 –0.1 –1.0
Ovary (C56) 4.8 0.8 –4.2 0.9 –4.3 –1.1 0.2 –0.9
Kidney (C64) –1.2 0.9 1.2 1 3.8 –0.1 2.4 0.7
Bladder (C67) 2.1 –0.9 0.4 0.8 –2.6 1.8 0.7 –1.5
Brain, CNS (C70–72) 5.8 1.4 –3.0 2.1 –0.3 3.3 –3.0 –2.6
Thyroid (C73) 17.9c –2.9 6.2c –0.6 6.2 –1.0 8.5c –1.8
HL (C81) 1.6 –1.9 –0.5 –1.2 10.7 –2.0 –0.2 –1.3
NHL (C82–85,96) –0.4 –1.3 –0.1 0.6 –0.5 –0.6 2.7 6
Leukemia (C91–95) 0.2 –0.9 –3.6 0.8 2.8 –0.02 –1.4 –0.3
Other and unspecified 13.6c –1.6 3.3 –– –5.0c –2.0 –0.1 –1.8
All sites but C44 –0.6 –0.6 –0.4 0.6 –0.8 –1.4c –0.1 –2.0c

HL, Hodgkin lymphoma; NHL, non-Hodgkin lymphoma.

a
Incidence rates were estimated using aggregated data from regional cancer registries.
b
Mortality data for colorectal cancer also includes the anus (C21).
c
The estimated annual percentage change is statistically different from zero (P
0.05).
S28 M.S. Sierra et al. / Cancer Epidemiology 44S (2016) S23–S42

3.2. Variations based on sub-regions, HDI level, and country CSA. In the last 5-years available, the most common cancer
diagnoses in the region were cancers of the prostate, lung,
Within sub-regions of CSA, different cancer patterns were noted; colorectal, stomach, and NHL among males and cancers of the
for instance, the incidence and mortality rates from breast cancer in breast, cervix, colorectal, stomach, thyroid, and lung among
South America were 2–5-times higher than in Central America while females. With the exclusion of NHL and the inclusion of liver
the incidence and mortality rates of cervical cancer were up to 3- cancer, these sites were also the most important causes of cancer
times higher in Central than in South America. The incidence of deaths. Some improvements were observed such as the declining
colorectal cancer was the highest in some southern and tropical CSA rates of male lung cancer in Brazil and Argentina as well as the
countries, with rates ranging between 25.2–34.2 for males and from decline in cervical and stomach cancer rates, particularly in
16.9–24.7 for females, as compared to other parts of CSA (ASR countries where the burden was high. On the other hand, increased
<16.9 and ASMR around 11 or below). Lung cancer incidence and incidence rates were observed for prostate and female thyroid
mortality were the highest among males in southern CSA and Cuba cancers. Observed patterns and trends seem to reflect variation in
(ASR: 30.5–50.2 and ASMR: 18–44.5) in comparison with males in HDI, exposure to common risk factors (Table 4), detection
other CSA regions (ASR <27 and ASMR <16). The incidence and practices, and disparities in healthcare access [2,3,9,11,28–33].
mortality from stomach cancer was higher among males in Chile and We also observed high incidence and mortality of gallbladder
some countries located in central CSA (ASR: 25.3–29.1 and ASMR: cancer in the region, particularly in Chile with some of the highest
17.4–24.6) and among females in the Andean region and some incidence and mortality rates in the world [13,22]; although the
central CSA countries (ASR: 12.7–15.1 and ASMR: 9.3–11.2) than reasons for the high burden of gallbladder cancer is still unknown,
among males and females in other CSA regions (ASR <22.0 and ASMR the high frequency of gallstones (major determinant for gallblad-
<16.0 for males; and ASR
10.3 and ASMR <9.0 for females) (Fig. 5). der cancer) along with poor access to gallbladder surgery may
Countries with high/very high HDI such as Argentina, Brazil, contribute to the observed patterns [34].
French Guyana and Uruguay, had a high burden of prostate and Overall, incidence and mortality rates from all cancers
breast cancer and a relatively low burden of stomach and cervical combined were comparatively lower in CSA than in the US, except
cancer, whereas in countries of medium HDI such as Bolivia, El for male mortality in Uruguay, Cuba, and Argentina (6–40% higher)
Salvador, Guatemala, Nicaragua, and Suriname, the burden of which could reflect the high mortality rates from specific cancer
stomach and cervical cancers was relatively high (Figs. 1–4). Also in sites, including those sites which usually have poor survival (i.e.
high/very high HDI countries, the incidence of breast cancer was lung and stomach). Although colorectal, lung, breast, cervix, and
high (ASR: 67.7–71.2) while the incidence of cervical cancer was leukaemia have good prognosis in higher income countries, in
low (ASR: 17.1–18.2); and, in contrast, the opposite was true for Uruguay, Cuba, and Argentina and other CSA countries, survival
medium HDI countries like El Salvador and Bolivia (ASR <13 for remains lower which, again, indicates inadequate and delayed
breast vs. 22–28.9 for cervix). However, in Chile (very high HDI) the access to healthcare (diagnosis and optimum treatment) [35].
incidence of both breast and cervical cancers was relatively low Despite the high HDI level of French Guyana, disparities in cancer
(35.4 and 13.9, respectively), and in Peru (high HDI) the incidence care, particularly among those living in remote areas, have been
of breast cancer was low (35.1) but the incidence of cervical cancer shown in women with advanced breast cancer and invasive
was high (22.1) (Fig. 5). cervical cancer where mortality from these diseases could be
Interesting contrasts in cancer patterns were seen also between similar to that of neighbouring countries [36,37].
countries; for example, unlike other countries in CSA, Chilean The incidence and mortality rates of all cancers combined was
males and females had up to 12-times higher incidence and up to twice as high in males than in females, except in Bolivia and El
30-times higher mortality rates of gallbladder cancer. Males and Salvador; the disparity in these two countries probably reflects the
females in Argentina, Brazil, Chile, and Uruguay and males in Cuba high rates of cervical cancer among women [11]. Although the
had 5–10-times higher mortality rates of oesophageal cancer than reasons for sex disparity in cancer risk are not fully understood,
males and females in any other CSA country (Fig. 5). Cuban males sex-specific hormones and genetic susceptibility may play some
and females had 5–13-times higher mortality of lung, larynx and role alongside differential exposure to risk factors [38–40].
oropharyngeal cancers than males and females in any other CSA Declines in the incidence and mortality of all cancers combined
country, except for lung cancer among Uruguayan males, ASMR: observed in Chile and Costa Rica from 1997 to 2008 may partially
44.5 (Fig. 5 and Annex 1 Fig. A1). reflect declines in stomach and cervical cancers. Regional differ-
ences in incidence and mortality patterns of all cancers combined
3.3. Variations by sex reflect the variability of specific cancer sites (i.e. breast, cervix,
prostate, lung, stomach, colorectum, liver, etc.) and perhaps
Apart from breast cancer, only two cancer types had a higher differences across HDI levels as well as differences in the
incidence in females compared with males: thyroid (0.16:1-to- distribution of major determinants of cancer (i.e. H. pylori infection,
0.24:1), and gallbladder (M:F = 0.25:1-to-0.83:1) except in French smoking), detection practices, advanced stage at cancer diagnosis,
Guyana (M:F = 2:1) where gallbladder is twice more common in and disparities in healthcare access [2,3,11,28,30]. Interpretation of
males than in females. For other cancer sites, males had higher data patterns from all cancers combined is challenging given the
rates than females; for example, M:F rate ratios for lung cancer wide variation in the distribution of risk factors between and
ranged from 2:1-to-6:1 for both incidence and mortality. M:F ratios within countries that could contribute to differences in cancer risk;
for stomach cancer were 3:1 for incidence and mortality (Fig. 5 and moreover, under-registration of cancer patients may lead to
Annex 1 Fig. A1). The most drastic M:F ratio was noted for larynx, underestimation of incidence and/or mortality rates. For instance,
with incidence M:F ratio ranging from 5:1-to-14:1, except in medium HDI countries such as Nicaragua, El Salvador, Suriname,
Bolivia (M:F = 2:1), and mortality M:F ratio ranging from 4:1-to- Panama, and Paraguay, and a couple of high HDI countries like
21:1 (Annex 1 Fig. A1). Peru, and Ecuador had some of the lowest mortality from all
cancers combined in the world [13], if these statistics are not due to
4. Discussion substantial under registration, they may result from the high
competing mortality burden due to other causes such as violence,
This paper provides a comprehensive overview of the most ischemic heart disease, road injuries, lower respiratory infections,
recent incidence and mortality patterns and trends of cancer in among others, in these countries [41].
 M.S. Sierra et al. / Cancer Epidemiology 44S (2016) S23–S42 S29

ASR ASR

ASR ASR
Fig. 5. Age-standardized incidence (light) and mortality (dark) rates per 100,000 for selected cancers in Central and South America for the period 2003–2007, unless
otherwise specifiedy.
y
Period of national mortality data matched as close as possible to the incidence period.
1
Incidence rates were estimated using aggregated data from regional cancer registries.
S30 M.S. Sierra et al. / Cancer Epidemiology 44S (2016) S23–S42

ASR ASR

ASR ASR
Fig. 5. (Continued)
 M.S. Sierra et al. / Cancer Epidemiology 44S (2016) S23–S42 S31

ASR ASR
Fig. 5. (Continued)

4.1. Changes in risk factors and overall cancer burden pregnancies and later age at first pregnancy have been associated
with an increased risk of breast cancer [10,33]. In high HDI countries
Tobacco smoking and alcohol consumption remain important in CSA such as Argentina, Brazil and Uruguay the burden of breast
public health problems in CSA [42,43], given their high prevalence in cancer is high and fertility rates with an average of 2 children per
some countries and strong causal association with several common woman (similar to that in the US); in contrast, in medium HDI
cancers (Table 4). The WHO has established a framework for tobacco countries like Guatemala and Nicaragua and some high HDI
control and has developed a global strategy to reduce the harmful use countries like Peru, and Ecuador, the burden of breast cancer is
of alcohol; while all CSA countries have (partially) implemented the low and fertility rates range between 3 to 4 children per women [54].
framework for tobacco control, only a few countries have started to In addition to the growing burden of cancers related to
develop and/or implement the WHO alcohol policies [44,45]. Brazil, economic development, the burden of cancers associated with
Panama, and Uruguay have implemented some of the most stringent chronic infections and poverty remains high. The main infectious
tobacco smoking policies in the region and the prevalence of agents associated with an increased risk of cancer are shown in
smoking has declined there in recent decades [46–48]. These policies Table 4. Estimates for 2008 revealed that 17% of all the incident
are a likely cause of the declining lung cancer trends in males for cancer cases occurring in South America and Mexico were due to
some of the higher HDI countries. infections (150,000/910,000 cases), including H. pylori, HPV, HBV,
Obesity trends across CSA countries revealed a remarkable HCV, and EBV, among others [55]. However, these estimates
change from underweight to overweight over the last few decades underscore the importance of HPV and H. pylori infections which
[49,50]. High intake of energy-rich foods, combined with low levels are highly prevalent in CSA (12.3–20.4% [56], and 50–95% [57–59],
of physical activity are suggested to cause this marked increase in respectively) as compared to the relatively low prevalence of HCV
body weight [49]. Obesity has been associated with twelve cancer (1.4–2.5% [60]) and HBV (<2% in Central and tropical CSA, and 2–4%
sites (Table 4) and recent estimates indicate that around 15% of the in the Caribbean, Andean and Southern CSA [61]).
incident cancers that occurred in CSA and the Caribbean 2012 could Nearly 90% of all the cervical, vulva, vagina, anal, penile, and
be attributed to obesity, assuming a causal relationship [51]. As oropharyngeal cancer cases combined (75,000/84,000) in CSA could
obesity increases in CSA it is possible that the burden of these be attributed to HPV infections, with the vast majority of these cases
cancers will increase in the future, underlining the importance of being cervical cancers (68,000, 91%) [62]. As of 2006, HPV
controlling this problem. vaccination was introduced in the national immunization schedule
We also observed contrasting patterns in breast and cervical among women 9–20 years old in six CSA countries [2] and by mid-
cancer by HDI levels which may reflect changes in risk factors (Table 2014, 18 countries in the region offered the vaccine via public
4) [3,9,29,31–33] as well as disparities in healthcare access immunization programs [63]. An ongoing clinical trial conducted in
(including screening services, early detection, and treatment of Costa Rica suggests that HPV vaccination in women is effective in
precancerous lesions) between and within countries [2,10,33,52,53]. preventing oral-HPV infection which could potentially reduce the
Changes in reproductive patterns such as a reduced number of risk of HPV-associated oropharyngeal cancer [64].
S32 M.S. Sierra et al. / Cancer Epidemiology 44S (2016) S23–S42

Table 4
Potential factors associated with an increased risk of cancer in Central and South America [69,73,74].

Risk Factors Cancer site

Lifestyle

Tobacco Bone marrow (myeloid leukemia), cervix, colorectum; kidney, larynx, liver, lung; nasal cavity and paranasal sinus; esophagus, oral
cavity; ovary; pancreas; pharynx, stomach, uterus, urinary bladder
Alcohol Breast (female), colorectum, larynx; liver (hepatocellular carcinoma), esophagus, oral cavity, pharynx
Obesity Corpus uteri, ovary, postmenopausal breast, gallbladder (females), esophageal adenocarcinoma, colorectum, pancreas, kidney
Adult attained height Breast, colorectum
Dieta

Red meat, processed meat Colorectum

beta-carotene supplements (high Lung (among smokers)
doses)
Infections

Helicobacter pylori Stomach

Human papillomavirus (HPV) Cervix, vulva, vagina, anus, penis, head and neck (oral cavity, and oropharynx and tonsil)
Hepatitis C virus (HCV) Liver (hepatocellular carcinoma), NHL
Hepatitis B virus (HBV) Liver (hepatocellular carcinoma)
Epstein–Barr virus (EBV) Burkitt’s lymphoma, HL, NHL, lymphoma, nasopharynx
Human herpesvirus type 8 (HHV–8) Kaposi’s sarcoma
Human immunodeficiency virus Anus; cervix; eye (conjunctiva); HL, Kaposi sarcoma, NHL
type 1 (HIV–1)
Aflatoxins Liver, bile duct
Schistosoma haematobium Bladder
Opisthorchis viverrini (Liver flukes) Bile duct
a
Several dietary and nutritional factors have been evaluated but convincing evidence for the carcinogenic or protective effects against cancer are limited [74]: i.e. foods
containing beta-carotene probably protect against esophageal cancer while red meat probably increases the risk of pancreatic and prostate cancer [69,74].

Although there is no vaccine against H. pylori, evidence suggests Hospital (Sao Pablo, Brazil) has established an early detection
that eradication of the infection may reduce the progression of early program which offers screening for skin, breast, cervix, and prostate
gastric lesions [65]. Declines in the prevalence of H. pylori infection, using mobile units in 231 municipalities in 6 states since 2004
along with improvements in sanitation, and preservation and [76,95].
storage of foods are thought to be responsible for the worldwide Breast cancer mortality rates in CSA have increased over the last
decline in stomach cancer rates over the past few decades [48,66– few decades while in high income countries mortality has declined
68]. Despite the reported declines, mortality from stomach cancer in mainly due to screening and effective treatment [2,31,96,97]. In
CSA remains among the highest in the world [13] perhaps due to the CSA, most women are diagnosed at advanced stages and only 5–
high prevalence of H. pylori and unhealthy dietary habits such as a 10% are diagnosed in early disease stages (stage I); this proportion
high consumption of processed meat and salt [69,70]. varies between and within countries likely reflecting inequalities
HBV can be prevented via vaccination but, currently, there are in healthcare access and inadequate medical infrastructure [2,75].
no vaccines available for HCV [65]. The introduction of the HBV In response to the high burden of breast cancer, as of 2009, most
vaccine in CSA between the 1980s and 2000 seems to coincide with CSA countries have developed a legislative framework for the early
declines in liver cancer; however, the extent to which HBV and HCV detection, diagnosis, treatment and follow-up of breast cancer
contributed to the observed rates is still unknown [2,71]. [98,99] and as of 2013, most countries have national recommen-
Estimates for 2002 indicate that 5–28% of the global number of dations for breast cancer screening, except for Ecuador, where the
liver cancer (25,200–155,000/550,000–600,000 cases) could be guidelines are currently under development [100].
attributed to aflatoxin exposure; however, only 2% of these Although cytology-based cervical cancer screening has been
occurred in CSA (589–2980 cases). Interestingly, in Mexico, the introduced in all CSA countries in the last few decades, it has had little
estimated number of aflatoxin-related liver cancer (hepatocellular impact on the burden of cervical cancer due to suboptimal coverage
carcinoma) was 11-times higher than the number of HBV-related and follow-up coupled with disparities in screening compliance and
liver cancers (152–924 cases per 100,000 in HBV-negative people poor access to healthcare [33,53,56,101–106]. However, Chile, Costa
vs. 14–83 cases per 100,000 in HBV-positive people) [72], thus, Rica, Mexico, Brazil, Colombia and Uruguay have made some
suggesting that aflatoxin exposure may be an important contribu- improvements in these areas in recent years leading to better control
tor in the burden of liver cancer in this country and should be of cervical cancer [2,53]. Cervical cancer studies to gather informa-
further evaluated. tion on feasibility and effectiveness of screening, and pre-cancer
treatment in limited-resource settings are also ongoing in 5 CSA
4.2. Screening programs and early detection countries [107]. It is possible that improved cervical screening
activities and treatment of pre-invasive lesions as well as improve-
Differences in prostate, breast, cervical, colorectal, and thyroid ments in socioeconomic conditions could reduce the burden of
cancer rates between CSA countries may partially result from cancer cervical cancer in the future, as has already occurred in North
screening programs (increased medical surveillance), unequal America and some European countries [62,66].
healthcare access and treatment services, and public awareness
[2,75–92]. For example, incidence patterns of prostate cancer likely 4.3. Healthcare access, disease management and treatment
reflect differences in the use of prostate specific antigen (PSA) testing
between countries [66,78,81,83,93,94]. Moreover, community- Several CSA countries have included cancer treatment as part of
specific projects on particular cancers could have also led to their national health insurance coverage, focusing particularly for
increased surveillance and may explain some of the strong differ- those living in poverty, resulting in increased access to health
ences between cancer sites. For example, the Barretos Cancer services [1,108] and probably stable or improved survival for some
 M.S. Sierra et al. / Cancer Epidemiology 44S (2016) S23–S42 S33

cancer sites amenable to treatment such as cervical, breast, colon, variation in the quality of the cancer registries included and the
ovarian, and prostate in a few CSA countries where this was quality of mortality data.
introduced [35]. Aside from the data quality evaluations performed for data
In spite of the improvements in healthcare systems in CSA, previously submitted to CI5, evaluations of data quality for most
including the availability of cancer treatments (radiotherapy and PBCR in the region are scarce [117–119]. For instance, in Colombia, a
chemotherapy) in the public sector [100], inequities remain in access recent evaluation indicated that despite good levels of complete-
to optimal cancer services due to a series of factors including ness and data quality from the PBCR of Cali and Pasto, there is under-
availability of and accessibility to adequate medical infrastructure, coverage for some specific cancer sites (i.e. liver, pancreas,
suboptimal healthcare coverage, and lack of funding and unequal gallbladder, kidney, and leukaemia) probably because some sources
distribution of resources for particular populations [2,75]. Health of information were omitted [117,118]; there is also under-coverage
systems in most countries are fragmented or segment-structured by cancer registration in the PBCR of Bucaramanga and Manizales, as
and provide minimum care (focusing on emergency care); hence, death registries were not systematically used as a source of
there are delays in cancer diagnosis and treatment. Such delays are information [118]. While there was no selection based on quality
usually associated with an advanced-disease stage at diagnosis when criteria, all datasets received for this project were passed through
treatments are less effective [1,2,75,100,108]. These factors, along the same standard consistency control and checking procedures as
with low screening rates, could probably explain the disproportion- used in CI5 [22], and the results produced for this study provide a
ate cancer mortality in CSA as compared to several high income general picture of the cancer burden in the region. However, the lack
countries [2]. of adequate epidemiological data in CSA limit the countries'
Cervical, breast and colorectal cancer are potentially curable capacity to create and evaluate optimum cancer control activities,
with early detection and treatment (including surgery, radiother- including prevention and screening programs [2].
apy and chemotherapy), while testicular cancer, lymphoma, Efforts to collect cancer incidence data in CSA have been
sarcoma and acute lymphoblastic leukaemia are also potentially remarkable despite the limited resources allocated to most of these
curable with adequate treatment. Unfortunately screening and/or registries. However, improvements in coverage and quality of
treatments are not readily accessible for numerous people in low cancer registrations in CSA are urgently needed to minimize
and middle income countries [108]. Hence, differences in the missing or incomplete data. Given the anticipated increase in the
adoption of modern therapies and disparities in disease manage- cancer burden in the CSA, there is still an overwhelming need for
ment probably contributed to some of the observed cancer high quality data and increased coverage to provide vital guidance
patterns in CSA as well [67,78,109–111]. for future cancer control activities. The Global Initiative on Cancer
Registry Development (GICR), convened by International Agency
4.4. Strengths and weaknesses of study for Research on Cancer (IARC) in 2011, aims to increase global
capacity to collect high quality population-based cancer registry
This study has several strengths and limitations. This overview data in low and middle income-countries (http://gicr.iarc.fr/). To
aimed to present the current patterns and trends of cancer in CSA address the lack of high-quality cancer data in CSA, the Latin
and included the most readily available incidence data from American Regional Hub was established in 2013 to provide
13 countries (48 cancer registries), including data not published in increased technical and advocacy assistance.
the latest volume of CI5 (8 countries, 22 cancer registries) [22] and
national mortality data from 18 countries. The final population 5. Conclusion
coverage for incidence data was 10%. Although this figure is still
low, it does represent the largest compilation of cancer incidence Over the study period, the leading cancers diagnosed in CSA
data in the region and the most readily accessible data source were prostate, lung, female breast, cervix, colorectal, and stomach.
available to date. In the absence of national incidence data (except These cancers, were also the primary causes of cancer mortality in
for Costa Rica and Uruguay), nationwide incidence rates are the region. The marked difference in the burden of cancer in CSA
represented by aggregated data from regional registries which do differed according to HDI level, between countries and within the
not cover the entire country and may not be representative of the region, and also by sex. These results confirm the double cancer
cancer burden at the national level. PBCR may differ in complete- burden of cancer in several CSA countries with elevated rates of
ness and data quality which, among other factors, depend on the both infection-related cancers and cancers associated with more
maturity of the cancer registry; this could explain why some of the affluent lifestyles.
rates observed in Mexico, Bolivia and El Salvador were low. The cancer patterns and trends across CSA countries also reveal
Approximately 5% of the total number of cancers diagnosed in CSA differences in disease ascertainment and diagnosis, death certifi-
were classified as other and unspecified. A high proportion of cases cation, and healthcare access. The disproportionately high
classified as “other and unspecified” indicates poor diagnostic mortality from cancer in some countries or regions in CSA may
precision or inability to specify the site of the primary cancer (for reflect deficiencies in prevention, early detection and/or disease
cases diagnosed using tissue from a metastasis) [12]. management. There are important opportunities to reduce the
Rates could be influenced by differences in case ascertainment cancer burden in the future through resource-dependent inter-
and reporting of certain cancers across countries and registries ventions such as the implementation and/or strengthening of
within the region; for example, the interpretation of liver cancer tobacco and alcohol control policies and vaccination against HPV.
patterns depends on the accuracy of the ICD-10 coding [112]. The Increasing public awareness of breast, cervix, colorectum, and
quality of national mortality data rely on completeness, coverage of prostate cancer could lead to early detection and treatment and
the registration, and the proportion of deaths classified as “ill probably better outcomes. Finally, this study demonstrates that
defined” causes; in some CSA countries mortality data may be there is an overwhelming need to improve the quality and
considered of medium or low quality [85,113–115]. Because liver coverage of population-based cancer registries to guide future
cancer is a common metastasis location, the underlying cause of cancer control policies and programs.
death can easily be misclassified as the primary site instead of the
metastatic site which can also bias the rate estimations [116]. Conflict of Interest
Therefore, differences in cancer burden between countries in this
paper must be interpreted with caution, considering the large None declared.
S34 M.S. Sierra et al. / Cancer Epidemiology 44S (2016) S23–S42

Funding Acknowledgements

This work was undertaken during the tenure of a Postdoctoral The authors would like to thank sincerely all of the cancer
Fellowship to Dr Mónica S. Sierra from The International Agency registry directors and their staff (listed in the Appendix to the
for Research on Cancer, partially supported by the European Introduction of this Supplement) for their considerable efforts in
Commission FP7 Marie Curie Actions – People – Co-funding of collecting the data presented in this paper, together with members
regional, national and international programmes (COFUND). of the IARC Section of Cancer Surveillance, especially Murielle
Colombet, Melina Arnold, Morten Ervik, Jacques Ferlay, Eric
Contribution of the authors Masuyer and Katiuska Veselinovic, for their valuable collaboration.
The authors would also like to thank G. Nogueras, E. Renteria and D.
Study conception and design: DF, MS. McKay for their important contributions.
Acquisition of data: MS, SA, ML.
Analysis of data: MS. Annex 1.
Interpretation of data: MS, IS, SA, ML, MP, EdV, DF.
Writing the article: MS, IS.
Critical revision of the article: MS, IS, SA, ML, MP, EdV, DF.
Final approval of the article: MS, IS, SA, ML, MP, EdV, DF.

Table A1
Definition of cancer sites.

Site Codesa Description

Oropharynx C00-C14 Lip, oral cavity and pharynx
Oesophagus C15 Oesophagus
Stomach C16 Stomach
Colorectumb C18-C20 Colon and rectum
Liver C22 Liver
Gallbladder C23-C24 Gallbladder and extrahepatic biliary tract
Pancreas C25 Pancreas
Nose, sinuses C30-C31 Nasal cavity and accessory sinuses
Larynx C32 Larynx
Lung C33-C34 Lung, trachea and bronchus
Cutaneous Melanoma C43 Melanoma of skin
Mesothelioma C45 Mesothelioma
Kaposi sarcoma C46 Kaposi sarcoma
Breast C50 Breast
Cervix C53 Cervix uteri
Corpus C54 Corpus uteri
Ovary C56 Ovary
Penis C60 Penis
Prostate C61 Prostate
Testis C62 Testis
Kidney C64 Kidney
Bladder C67 Bladder
Brain, CNS C70-C72 Brain and central nervous system (CNS)
Thyroid C73 Thyroid
Hodgkin lymphoma C81 Hodgkin lymphoma
Non-Hodgkin C82-85, C96 Non-Hodgkin lymphoma
lymphoma
Multiple myeloma C88 + C90 Multiple myeloma
Leukaemia C91-95 Acute lymphatic, chronic lymphatic, other and unspecified lymphatic, acute myeloid, chronic myeloid, other and unspecified
myeloid, and leukaemia, cell unspecified
All cancers combined C00-C96, but All sites but non-melanoma skin cancer
C44
Other and unspecified
cancers
a
International Classification of Diseases, 10th revision (ICD-10).
b
Mortality data also includes anus (C21).

Table A2
Subregional classification.

Geographic location

Central America Belize, Costa Rica, Cuba, El Salvador, Guatemala, Honduras, Mexico, Nicaragua, Panama
South America Argentina, Brazil, Bolivia, Chile, Colombia, Ecuador, French Guyana, Guyana, Paraguay, Peru, Suriname, Uruguay, Venezuela
Global Burden of Disease Regions [23]

Andean CSA Bolivia, Ecuador, Peru

Central CSA Colombia, Costa Rica, El Salvador, Guatemala, Honduras, Mexico, Nicaragua, Panama, Venezuela
Southern CSA Argentina, Chile, Uruguay
Tropical CSA Brazil, Paraguay
Caribbean Belize, Cuba, Guyana, Suriname
 M.S. Sierra et al. / Cancer Epidemiology 44S (2016) S23–S42 S35

Lip, oral cavity, and pharynx (C00-14) Pancreas (C25)

Females Males Females Males
1 5.0 19.7
Brazil 6.5 9.2
1.2 5.9 Uruguay (2005-07) 6.1 8.6
1 4.2 16.9
French Guyana (2003-08) 6.3 8.4
US 5.4 7.4
4.3 11.2 1 5.5 7.2
US 0.9 2.6 Argentina 5.6 7.7
2.5 10.1 1 4.2 5.3
Uruguay (2005-07) 0.9 5.7 Chile 4.7 4.9
1 3.6 10.0 1 4.2 5.2
Cuba (2004-07) 1.7 5.8 Brazil 3.0 3.7
1 2.2 6.4 1 1.2 1.4
Argentina 0.7 3.0 Mexico (2006-10) 4.4 4.7
1 3.0 5.2 1 2.5 4.7
Colombia 1.0 2.0 French Guyana (2003-08)
2.1 5.0 1 4.0 4.5
Costa Rica 0.8 2.4 Cuba (2004-07) 3.8 4.7
1 1.6 3.4 3.7 4.5
Chile 0.5 1.7 Costa Rica 3.9 4.5
1 2.8 3.0 1 3.8 4.0
Peru (2001-05) 0.6 0.7 Peru (2001-05) 2.4 2.4

Paraguay 0.7 2.8 Suriname 1.5 3.6

1 1.3 2.6
Mexico (2006-10) 0.7 1.8 Panama 3.1 3.3
1 3.2 3.3
Belize 0.3 2.5 Colombia 3.1 3.3

Venezuela 1.0 2.3 Venezuela 3.1 3.2

1 3.7 3.1
Panama 1.0 2.2 Ecuador 2.6 2.4

Guatemala 1.2 2.1 Belize 4.8 2.7

Suriname 0.5 1.8 Paraguay 2.4 2.5

1 1.9 1.8
Ecuador 0.6 1.0 Nicaragua 2.2 2.1
1 1.4 1.6
Bolivia (2011) Guatemala 2.1 1.8
1 1 0.3 0.3
0.8 1.4 El Salvador (1999-03)
El Salvador (1999-03) 0.6 1.4 1.6 1.6
1 1.0 0.4
Nicaragua 0.4 1.4
Bolivia (2011)

20 15 10 5 0 5 10 15 20 10 8 6 4 2 0 2 4 6 8 10

ASR ASR

Nose, sinuses (C30-31) Larynx (C32)

Females Males Females Males
1 0.7 0.9 1 1.4 13.0
Cuba (2004-07) Cuba (2004-07) 1.2 7.8
1 0.5 0.7 1 1.3 9.7
Peru (2001-05) Brazil 0.4 3.6
1 0.4 0.7 0.5 7.2
Brazil Uruguay (2005-07) 0.3 5.4
1 0.3 0.7 1 0.6 5.9
Chile Argentina 0.3 3.9
1 0.6 0.7 1 4.4
Colombia French Guyana (2003-08)
0.4 0.6 0.9 4.1
US US 0.3 1.4
1 0.0
0.6 1 0.5 3.8
French Guyana (2003-08) Colombia 0.5 2.2
1 0.4 0.5
Ecuador Venezuela 0.5 3.0
1 0.2 0.5
Argentina Costa Rica 0.3 3.0
0.2 1.6

Uruguay (2005-07) 0.3 0.5 1 0.7 2.6

Chile 0.2 1.4

Costa Rica 0.3 0.4 1 0.3 2.3

Mexico (2006-10) 0.3 2.1
1 0.1 0.2
El Salvador (1999-03) Belize 0.1 1.8
1 0.1 0.2 1
Mexico (2006-10) 0.3 1.7
Peru (2001-05) 0.2 0.6
1 0.6 0.2
Bolivia (2011) Panama 0.1 1.6

Venezuela Paraguay 0.1 1.4

1 0.3 1.2
Suriname Ecuador 0.1 0.7
1 0.2 1.1
Paraguay El Salvador (1999-03) 0.2 0.9
Panama Suriname 0.2 1.0
Nicaragua Nicaragua 0.2 0.9
Guatemala Guatemala 0.2 0.8
1 0.2 0.3
Belize Bolivia (2011)

1 0.5 0 0.5 1 15 10 5 0 5 10 15

ASR ASR
Fig. A1. Age-standardized incidence (light) and mortality (dark) rates per 100,000 for selected cancers in Central and South America for the period 2003–2007, unless
otherwise specifiedy.
y
Period of national mortality data matched as close as possible to the incidence period.
1
Incidence rates were estimated using aggregated data from regional cancer registries.
S36 M.S. Sierra et al. / Cancer Epidemiology 44S (2016) S23–S42

Cutaneous Melanoma (C43) Mesothelioma (C45)

Females Males Females Males
1 1.5
13.2 17.3 French Guyana (2003-08)
US 1.1 2.5
1 3.8 4.9 0.3 1.0
Brazil 0.5 0.8
US 0.2 0.8
3.6 4.6 Belize
Uruguay (2005-07) 0.6 1.2 0.2 0.8
1 1 0.3 0.7
2.3 3.9 Argentina
French Guyana (2003-08)
1 1 0.3 0.5
3.4 3.2 Peru (2001-05)
Ecuador 0.3 0.4 0.1 0.1
1 2.9 3.1 0.1 0.3
Colombia 0.5 0.6
Uruguay (2005-07) 0.1 0.3
1 1 0.1 0.3
2.8 3.1 Colombia
Argentina 0.7 1.2
1 1 0.2 0.2
2.1 2.6 Ecuador
Chile 0.7 1.0 0.04 0.04
1 0.3 0.2
2.2 2.5 Chile
Costa Rica 0.5 0.9
1 1 0.2 0.2
2.1 2.2 Mexico (2006-10)
Peru (2001-05) 0.3 0.5
1 2.0 2.1 0.04 0.2
Mexico (2006-10) 0.5 0.7 Costa Rica
1 1 0.1 0.1
1.8 1.6 Brazil
Cuba (2004-07) 0.3 0.4 0.03 0.1
1 1 0.2 0.1
0.7 0.7 Cuba (2004-07)
Bolivia (2011)
Paraguay 0.3 0.7 Panama 0.1 0.1

Panama 0.3 0.5 Venezuela 0.1 0.1

1 0.01 0.01
Venezuela 0.4 0.5 El Salvador (1999-03) 0.01 0.02

Guatemala 0.3 0.5 Guatemala

1 0.3 0.4
El Salvador (1999-03) 0.03 0.03 Suriname

Belize 0.3 0.4 Paraguay 0.01

Suriname 0.1 0.3 Nicaragua 0.04

1
Nicaragua 0.2 0.2 Bolivia (2011)

20 15 10 5 0 5 10 15 20 1.5 1.0 0.5 0 .5 1.0 1.5

ASR ASR

Kaposi sarcoma (C46) Corpus uteri (C54)

Females Males
18.0
1 0.2 1.6 US 1.2
French Guyana (2003-08)
1 11.0
1 0.2 1.3 French Guyana (2003-08)
Colombia
8.8
1 0.3 1.1 Uruguay (2005-07) 1.1
Peru (2001-05)
1 7.4
0.1 1.0 Brazil 1.1
US
1 7.4
1 0.1 0.7 Argentina 1.6
Ecuador
7.2
1 0.1 0.7 Costa Rica 1.7
Brazil
1 7.1
1 0.1 0.5 Cuba (2004-07)
Argentina 4.5
1 5.6
Costa Rica 0.1 0.5 Colombia 0.9
1 4.5
Uruguay (2005-07) 0.1 0.5 Peru (2001-05) 1.0
1 4.3
1 0.05 0.4 Ecuador
Mexico (2006-10) 1.4
1 1 4.3
0.1 0.1 Mexico (2006-10)
Chile 0.8
1 1 3.8
0.02 0.1 Chile
Cuba (2004-07) 1.2
1 0.01 0.01
El Salvador (1999-03) Belize 3.6
1 2.3
Venezuela Bolivia (2011)
1 1.6
Suriname El Salvador (1999-03) 1.4

Paraguay Panama 1.5

Panama Venezuela 1.5

Nicaragua Paraguay 1.2

Guatemala Suriname 1.0

1
Bolivia (2011) Nicaragua 0.3

Belize Guatemala 0.3

2.0 1.5 1.0 0.5 0 0.5 1.0 1.5 2.0 0 5 10 15 20

ASR ASR

Fig. A1. (Continued)

 M.S. Sierra et al. / Cancer Epidemiology 44S (2016) S23–S42 S37

Ovary (C56) Penis (C62)

9.3 1 2.0
US 5.5 French Guyana (2003-08)
1 9.1 1 1.7
Argentina 4.1 Brazil
8.4 1 1.6
Uruguay (2005-07) 4.4 Cuba (2004-07)
1 8.2 1.5
French Guyana (2003-08) Uruguay (2005-07)
1 8.1 1 1.5
Brazil 2.7 Argentina
1 7.7 1 1.4
Peru (2001-05) 2.0 Colombia
1 7.6 1 1.3
Colombia 3.3 Chile
1 7.2 1.2
Ecuador 2.0 Costa Rica
1 5.7 1 1.0
Chile 3.5 Peru (2001-05)
5.5 1 1.0
Costa Rica 3.0 Mexico (2006-10)
1 5.4 1 0.7
Cuba (2004-07) 2.9 Bolivia (2011)
1 5.2 1 0.5
Mexico (2006-10) 3.7 El Salvador (1999-03)
1 0.5
Suriname 3.6 Ecuador

Venezuela 3.2 US 0.4

Panama 2.6 Venezuela

1 2.6
Bolivia (2011) Suriname

Paraguay 2.0 Paraguay

Nicaragua 1.8 Panama

1 1.0
El Salvador (1999-03) 1.3 Nicaragua

Belize 1.0
Guatemala

Guatemala 0.8
Belize

0 2 4 6 8 10 0 0.5 1.0 1.5 2.0

ASR ASR

Testis (C62) Kidney (C64)

Females Males
1 8.3
Chile 1.1 5.7 13.4
Uruguay (2005-07) 2.0 6.3
1 5.4
Argentina 0.8 6.6 12.3
US 1.6 3.5
5.3
Uruguay (2005-07) 0.7 1 5.6 10.4
Chile 1.7 4.0
5.3
US 0.2 1 4.5 10.4
Argentina 1.6 4.7
1 4.4
Ecuador 0.3 1 3.0 5.8
Brazil 0.8 1.5
3.4
Costa Rica 0.4 1 2.5 5.0
Peru (2001-05) 0.7 1.2
1 3.2
Peru (2001-05) 0.4 2.4 4.1
Costa Rica 0.9 1.6
1 2.9
Mexico (2006-10) 0.7 1 2.7 3.8
Ecuador 0.7 1.1
1 2.8
Colombia 0.4 1 3.2 3.6
Cuba (2004-07) 0.9 1.9
1 2.2
Brazil 0.3 1 2.3 3.5
Colombia 0.8 1.2
1 1.0
French Guyana (2003-08) 1 1.8 3.4
Mexico (2006-10) 1.5 2.8
1 0.6
Bolivia (2011) 1 3.1 3.1
French Guyana (2003-08)
1 0.6
Cuba (2004-07) 0.3 Venezuela 1.1 1.9
Suriname 0.4 Panama 0.9 1.7
Panama 0.4 Paraguay 0.6 1.1
1 0.4
El Salvador (1999-03) 0.1 Bolivia (2011)
1 0.4 1.1

Guatemala 0.4 Nicaragua 0.4 1.1

Paraguay 0.4 Suriname 0.4 1.0
Venezuela 0.3 Belize 1.7 0.9
Nicaragua 0.2
1
El Salvador (1999-03) 0.2 0.3
0.3 0.6
Belize Guatemala 0.5 0.6

0 2 4 6 8 10 15 10 5 0 5 10 15
ASR ASR
Fig. A1. (Continued)
S38 M.S. Sierra et al. / Cancer Epidemiology 44S (2016) S23–S42

Bladder (C67) Brain, CNS (C70-72)

Females Males Females Males
1 4.8 6.4
US 5.4 21.0 Brazil
1.1 3.7 3.2 4.0
3.3 15.8 4.6 6.2
Uruguay (2005-07) 0.8 5.9 US 2.5 3.7
1 3.0 12.8 4.0 6.2
Argentina 0.8 4.3 Uruguay (2005-07) 1.9 3.2
1 1 3.9 5.5
Brazil 3.5 12.1 Colombia
0.8 2.3 2.3 3.1
1 6.1 10.8 1 4.5 5.3
Chile 1.1 2.6 Argentina 1.9 2.9
1 1 3.6 5.1
Cuba (2004-07) 2.5 8.4 Cuba (2004-07)
1.3 3.9 3.0 4.1
1 3.2 8.4 1 2.1 4.8
French Guyana (2003-08) French Guyana (2003-08)
1 1.8 5.5 1 3.5 4.5
Colombia 0.7 1.6 Peru (2001-05) 1.8 2.2
1.5 5.4 1 3.4 4.2
Costa Rica 0.6 2.1 Ecuador 1.9 2.2
1 2.0 4.9 2.6 3.7
Ecuador 0.3 0.7 Costa Rica 2.0 3.0
1 1.6 4.6
Mexico (2006-10) 0.9 1.8 Panama 2.8 3.0
1 1.8 4.6 1 2.5 2.7
Peru (2001-05) 0.4 0.8 Mexico (2006-10) 1.7 2.5
1 2.5 2.7
Suriname 0.3 1.7 Chile 1.4 2.0

Venezuela 0.7 1.6 Suriname 3.4 2.7

Panama 0.6 1.1 Belize 2.2 2.6

Paraguay 0.2 1.0 Guatemala 2.2 2.5

1 0.6 0.8 1 0.5 0.6
Bolivia (2011) El Salvador (1999-03) 1.9 2.4
1 0.5 0.7
El Salvador (1999-03) 0.4 0.3 Venezuela 1.6 2.0

Nicaragua 0.2 0.5 Nicaragua 1.7 1.9

Guatemala 0.2 0.4 Paraguay 1.2 1.4

1 0.6 0.3
Belize 1.2 0.3 Bolivia (2011)

25 20 15 10 5 0 5 10 15 20 25 10 5 0 5 10

ASR ASR

Thyroid (C73) Hodgkin lymphoma (C81)

Females Males Females Males
13.2 4.2 2.4 2.9
US 0.3 0.3 US 0.2 0.4
1 16.0 3.5 1
Ecuador Argentina 1.5 2.1
0.9 0.5 0.3 0.4
1 14.4 3.4 1
Brazil Cuba (2004-07) 1.4 2.1
0.4 0.2 0.7 1.0
1 10.7 2.5 1 1.5 2.0
Colombia 0.8 0.4 Brazil 0.2 0.3
12.6 2.1 1.4 1.9
Costa Rica 0.5 0.4 Costa Rica 0.6 0.7
1 7.5 1.7 1 0.6 1.8
Peru (2001-05) 0.7 0.3 French Guyana (2003-08)
6.8 1.6 1.6 1.8
Uruguay (2005-07) 0.4 0.4 Uruguay (2005-07) 0.2 0.5
1 7.7 1.5 1 1.1 1.7
Cuba (2004-07) 0.4 0.3 Colombia 0.4 0.5
1 6.6 1.4 1 1.0 1.4
French Guyana (2003-08) Mexico (2006-10) 0.4 0.7
1 8.2 1.4 1 0.5 1.3
Chile 0.6 0.4 Ecuador 0.2 0.4
1 5.5 1.4 1 1.1 1.1
Argentina 0.4 0.3 Chile 0.2 0.3
1 4.9 1.2 1 0.7 0.9
Mexico (2006-10) 0.9 0.5 Peru (2001-05) 0.2 0.3
1 2.7 0.6
Bolivia (2011) Venezuela 0.4 0.6
1 0.1 0.6
Panama 0.4 0.4 Bolivia (2011)

Venezuela 0.6 0.3 Suriname 0.5 0.6

1 0.3 0.4
Paraguay 0.6 0.3 El Salvador (1999-03) 0.4 0.5
1 1.9 0.3
El Salvador (1999-03) 0.3 0.2 Nicaragua 0.2 0.4

Nicaragua 0.6 0.2 Guatemala 0.2 0.4

Guatemala 0.4 0.2 Belize 0.3 0.3

Suriname 0.4 Paraguay 0.1 0.3

Belize 0.2 Panama 0.2 0.3

20 15 10 5 0 5 10 15 20 3 2 1 0 1 2 3

ASR ASR

Fig. A1. (Continued)

 M.S. Sierra et al. / Cancer Epidemiology 44S (2016) S23–S42 S39

Non-Hodgkin lymphoma (C82-85, C96) Multiple myeloma (C88+C90)

Females Males Females Males
1 4.1 4.7
11.4 16.3 French Guyana (2003-08)
US 3.1 4.9
6.4 10.9 3.0 4.5
Uruguay (2005-07) 3.0 4.8 US 1.7 2.6
1 1 2.0 3.3
9.2 10.6 Chile
Ecuador 1.8 2.4 1.7 2.4
1 1 2.5 3.2
8.8 10.2 Brazil
Peru (2001-05) 2.0 2.7 1.0 1.2
1 1 1.7 2.7
6.9 10.2 Ecuador
Colombia 1.9 2.8 0.5 0.6
1 7.0 9.5 1.9 2.6
French Guyana (2003-08) Uruguay (2005-07) 1.5 2.4
1 1 1.6 2.6
6.5 9.1 Peru (2001-05)
Brazil 1.6 2.3 0.5 0.9
1 1 1.9 2.1
5.9 8.1 Colombia
Argentina 2.2 3.5 0.9 1.2
1 1 1.4 1.7
5.1 7.8 Cuba (2004-07)
Cuba (2004-07) 2.2 3.4 1.4 2.1
1 1.8 2.0
5.4 6.8 Argentina
Costa Rica 2.7 3.8 1.0 1.3
1 4.4 5.2
Mexico (2006-10) 2.1 3.0 Panama 1.3 1.8
1 4.3 4.3 1.0 1.3
Chile 2.4 3.4 Costa Rica 1.5 1.7
1 1.3 3.4
Bolivia (2011) Suriname 0.5 1.6

Panama 2.0 2.9 Venezuela 1.0 1.2

1 0.6 0.9
Venezuela 2.0 2.8 Mexico (2006-10) 0.9 1.2

Suriname 1.4 2.0 Belize 0.6 0.8

Paraguay 1.2 1.9 Paraguay 0.5 0.6

Belize 1.2 1.7 Nicaragua 0.3 0.4

1 0.2 0.3
Nicaragua 1.0 1.6
El Salvador (1999-03)
1 1 0.2 0.3
1.3 1.4 Bolivia (2011)
El Salvador (1999-03) 0.5 0.5

Guatemala 0.5 0.8

Guatemala 0.2 0.2

20 15 10 5 0 5 10 15 20 5 4 3 2 1 0 1 2 3 4 5

ASR ASR

Leukaemia (C91-95) Other and unspecified cancers

Females Males
Females Males
7.3 11.4
US 3.2 5.5 1 14.0 17.5
1
Brazil
6.1 7.6
Colombia 3.4 4.3
1 5.4 7.3 10.9 17.4
Argentina 3.0 4.4 Uruguay (2005-07)
1 6.7 6.7
Ecuador 3.1 3.8 1 10.2 13.2
1
Argentina 15.2 17.2
5.0 6.7
Brazil 2.6 3.4
5.1 6.7 1 4.5 4.0
Uruguay (2005-07) 2.9 4.7 Mexico (2006-10) 10.1 11.8
1 5.5 6.3
Peru (2001-05) 2.6 2.9 1 7.1 7.5
Chile 9.8 11.8
1 4.6 6.0
French Guyana (2003-08)
1 4.6 5.6 1 8.3 9.8
Chile 2.9 3.8
Colombia 11.1 11.7
4.6 5.5
Costa Rica 3.8 4.6 9.0 10.2
Costa Rica 9.1 11.1
1 3.4 5.0
Cuba (2004-07) 3.3 4.2
1 3.0 3.8
1 7.0 7.1
Mexico (2006-10) 3.4 4.4
Cuba (2004-07) 10.7 10.1

Panama 3.4 3.8

US 5.4 5.9
Venezuela 3.1 3.7
1 6.5 5.7
Guatemala Peru (2001-05)
3.1 3.5

Paraguay 3.0 3.4 1 6.3 5.5

Ecuador
Nicaragua 2.9 3.2
1 4.6 5.0
1
El Salvador (1999-03) 1.9 1.7 French Guyana (2003-08)
2.6 3.2

Suriname 1.9 2.7 1 2.4 2.1

El Salvador (1999-03)
Belize 2.5 2.5
1 1.3 1.3
Bolivia (2011)
1 1.0 0.7 Bolivia (2011)

15 10 5 0 5 10 15 20 15 10 5 0 5 10 15 20

ASR ASR

Fig. A1. (Continued)

S40 M.S. Sierra et al. / Cancer Epidemiology 44S (2016) S23–S42

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