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Global cancer transitions according to the Human
Development Index (2008–2030): a population-based study
Freddie Bray, Ahmedin Jemal, Nathan Grey, Jacques Ferlay, David Forman
Summary
Background Cancer is set to become a major cause of morbidity and mortality in the coming decades in every region
of the world. We aimed to assess the changing patterns of cancer according to varying levels of human development.
Methods We used four levels (low, medium, high, and very high) of the Human Development Index (HDI), a
composite indicator of life expectancy, education, and gross domestic product per head, to highlight cancer-specific
patterns in 2008 (on the basis of GLOBOCAN estimates) and trends 1988–2002 (on the basis of the series in Cancer
Incidence in Five Continents), and to produce future burden scenario for 2030 according to projected demographic
changes alone and trends-based changes for selected cancer sites.
Findings In the highest HDI regions in 2008, cancers of the female breast, lung, colorectum, and prostate accounted
for half the overall cancer burden, whereas in medium HDI regions, cancers of the oesophagus, stomach, and liver
were also common, and together these seven cancers comprised 62% of the total cancer burden in medium to very
high HDI areas. In low HDI regions, cervical cancer was more common than both breast cancer and liver cancer.
Nine different cancers were the most commonly diagnosed in men across 184 countries, with cancers of the prostate,
lung, and liver being the most common. Breast and cervical cancers were the most common in women. In medium
HDI and high HDI settings, decreases in cervical and stomach cancer incidence seem to be offset by increases in the
incidence of cancers of the female breast, prostate, and colorectum. If the cancer-specific and sex-specific trends
estimated in this study continue, we predict an increase in the incidence of all-cancer cases from 12·7 million new
cases in 2008 to 22·2 million by 2030.
Published Online
June 1, 2012
DOI:10.1016/S14702045(12)70211-5
Section of Cancer Information,
International Agency for
Research on Cancer, Lyon,
France (F Bray PhD, J Ferlay ME,
D Forman PhD); and
Department of Surveillance
and Health Policy Research,
American Cancer Society,
Atlanta, GA, USA (A Jemal PhD,
N Grey PhD)
Correspondence to:
Dr Freddie Bray, Section of
Cancer Information,
International Agency for
Research on Cancer, 150 cours
Albert Thomas, 69372,
Lyon Cedex 08, France
[email protected]
Interpretation Our findings suggest that rapid societal and economic transition in many countries means that any
reductions in infection-related cancers are offset by an increasing number of new cases that are more associated with
reproductive, dietary, and hormonal factors. Targeted interventions can lead to a decrease in the projected increases in
cancer burden through effective primary prevention strategies, alongside the implementation of vaccination, early
detection, and effective treatment programmes.
Funding None.
Introduction
Global action is needed to stem the increasing burden of
non-communicable diseases, especially in low-income
and middle-income countries1–9 which now bear 80% of
the worldwide burden of such diseases.10 Cancer, already
the leading cause of death in many high-income
countries, is set to become a major cause of morbidity
and mortality in the next few decades in every region of
the world, irrespective of level of resource.10–12
The UN has forecast that the global population will
reach 7 billion by 2012 and 8·3 billion by 2030.13 The
effect of population ageing and growth will be greatest
in low-income and middle-income countries. These
changes translate to a predicted global burden of
20·3 million new cancer cases by 2030 compared with
an estimated 12·7 million cases in 2008, and a predicted
13·2 million cancer-related deaths worldwide by 2030,
up from 7·6 million in 2008.11 Such a demographic
transition and the resulting upsurge in cancer incidence
and mortality are contingent on population projections
that assume decreases in human fertility and population
growth as a result of continuous social and economic
development,14 and on incidence and mortality rates of
all cancer types combined remaining unaltered over the
next few decades.
The static trends in the risk of cancer in future decades
seems the less robust of these two assumptions,
especially in view of the cancer-specific incidence and
mortality trends seen over the past half century. Rather
than describing constant rates over time, many reports
have documented lagged changes in lung and other
tobacco-related cancers according to the country-specific
and sex-specific phases of the tobacco epidemic,
uniform decreases in stomach cancer as a result of
primary prevention efforts, and a rising incidence of
breast, colorectal, and prostate cancers, initially in
affluent populations and, within the last couple of
decades, in historically less-affluent populations at
lower cancer risk. The changes are likely to be
attributable to a combination of unfavourable changes
in several ill defined reproductive, dietary, metabolic,
hormonal, and other behavioural determinants that
increase the risk of these cancers. The so-called cancer
transition—an analogy to Omran’s epidemiological
www.thelancet.com/neurology Published online June 1, 2012 DOI:10.1016/S1470-2045(12)70211-5
1
Articles
See Online for appendix
transition15—thus fits well with the occurrence of
socioeconomic transition in several historically lowresource to medium-resource populations. The result
has been a reduction in the prevalence of predominantly
infection-based diseases, and a concomitant rise in
those with apparently little or no established associations
with infection.16
By linking geographical and temporal patterns of
cancer to corresponding levels of social and economic
progress, we provide an overview of the key characteristics
of the global cancer transition. We used the Human
Development Index (HDI)17 as an indicator of socioeconomic development, and rates of cancer incidence
and mortality as markers of the extent of the cancer
transition globally. We aimed to draw attention to
geographical variations and trends in cancer-specific
rates in each of the HDI areas and in different world
regions, and to offer a global, trends-based profile of the
possible cancer burden in 2030.
Methods
Data sources
For the GLOBOCAN database
see http://globocan.iarc.fr
For Cancer Incidence in Five
Continents see http://ci5.iarc.fr
The International Agency for Research on Cancer has
compiled estimates of the worldwide incidence and
mortality for 27 cancers in 184 countries in 2008 by
age group and sex in the GLOBOCAN 2008 database.11
Details are provided elsewhere.11 The methods used to
estimate cancer-specific incidence and mortality rates
at the national level are dependent on the availability
and accuracy of local data sources. Generally, there is
a paucity of high quality cancer incidence and
mortality data in low-resource and medium-resource
areas—eg, no population-based cancer registries exist
in 34 of the 184 countries examined in this paper,
32 of 34 countries are low-resource or mediumresource countries, and no vital statistics systems
exist in 88 countries, of which 85 are either lowresource or middle-resource countries.
To examine patterns in the incidence of different types
of cancer in 2008 by levels of socioeconomic development,
we linked the country-specific GLOBOCAN estimates to
the corresponding HDI, as estimated for 2007 by the UN
Development Programme (UNDP).17 The HDI is a
summary measure of human development, which (for
the 2007 UNDP estimates) is a composite index of three
basic dimensions of human development, namely a long
and healthy life (based on life expectancy at birth), access
to knowledge (based on a combination of adult literacy
rate and primary education to tertiary education
enrolment rates), and a decent standard of living (based
on GDP per head adjusted for purchasing-power parity
[US$]). We used the predefined categories of the
distribution of HDI by country: low (HDI<0·5), medium
(0·5≤HDI<0·8), high (0·8≤HDI<0·9), and very high
(HDI≥0·9). The global breakdown by country within
each development level is shown in figure 1 and the
specific countries are listed in the appendix. We use
these HDI levels to characterise aspects of the cancer
burden according to level of resource and extent of
societal development. We also combined the high HDI
and very high HDI levels, and low HDI and medium
HDI levels, to create lower HDI and higher HDI areas,
as alternatives to the traditional grouping of more
developed (North America, Europe, Australia, New
Zealand, and Japan) and less developed regions (all other
areas of the world).
To examine incidence trends in common cancers, we
extracted incident cases of the seven most commonly
diagnosed cancers worldwide: cancers of the lung,
female breast, colorectum, stomach, prostate, liver, and
cervix. Together, these cancers constitute more than
58% of the estimated global cancer burden.
Corresponding population datasets were obtained from
CI5 Plus, which contains annual incidence for
population-based cancer registries published in Cancer
Incidence in Five Continents (CI5) for the longest year
Low HDI (0·3–0·499)
Medium HDI (0·5–0·799)
High HDI (0·8–0·899)
Very high HDI (0·9–0·999)
Figure 1: Global Human Development Index (HDI) levels
This map shows only the countries included in the analysis.
2
www.thelancet.com/neurology Published online June 1, 2012 DOI:10.1016/S1470-2045(12)70211-5
Articles
A
World cancer incidence
New cases in 2008 (thousands)
1000 500 0
500 1000
Lung
830
Female breast
832
Colorectum
825
778
551
409
366
Stomach
Prostate
766
622
132
572
B
World cancer incidence
Cumulative risk up to age 75 years
5 4 3 2 1 0 1 2 3 4 5
Lung
3·5
Female breast
3·4
Colorectum
3·1
Prostate
3·4
375
Cervix uteri
215
141
Leukaemia
175
175
Corpus uteri
157
132
245
493
Stomach
0·9
1·4
Liver
163
532
Liver
0·6
1·4
Liver
106
Non-Hodgkin
lymphoma
Stomach
1·5
Oesophagus
127
1·2
1·1
Breast
389
Bladder
Non-Hodgkin
lymphoma
0·7
0·4
0·5
World cancer mortality
Cumulative risk up to age 75 years
5 4 3 2 1 0 1 2 3 4 5
695
Colorectum
141
681
D
Lung
0·4
178
256
2·3
1·4 1·8
Liver
Bladder
World cancer mortality
Deaths in 2008 (thousands)
1000 500
0
500 1000
Stomach
Cervix uteri
Oesophagus
C
368
230
Oesophagus
89
1·1
Cervix uteri
62
Lung
240
Colorectum
228
Breast
317
213
2·7
2·0
1·2
0·6
0·8
0·6
0·4
Oesophagus
Pancreas
0·7
0·9
0·2
0·9
Pancreas
190
77
Cervix uteri
0·2
0·6
0·9
0·4
Prostate
179
79
Prostate
0·4
0·2
0·8
0·3
Leukaemia
113
0·2
91
101
0·3
0·2
80
95
Leukaemia
Brain, nervous
system
Non-Hodgkin
lymphoma
0·3
Non-Hodgkin
lymphoma
Brain, nervous
system
Bladder
0·3
0·2
87
63
Ovary
0·3
0·2
65
Bladder
0·2
0·2
Lip and oral cavity
0·2
0·3
Kidney
0·3
0·1
Corpus uteri
0·7
0·4
Kidney
0·8
0·2
Pancreas
194
84
Pancreas
0·7
0·2
Kidney
201
72
Lip and oral cavity
0·5
0·4
144
Ovary
75
Lip and oral cavity
114
149
Leukaemia
0·6
0·3
Lip and oral cavity
39
89
Brain, nervous
system
Ovary
109
129
Ovary
0·5
0·2
Kidney
79
37
119
106
Melanoma of skin
0·6
0·1
Gallbladder
61
48
Gallbladder
0·2
0·1
Thyroid
140
73
Brain, nervous
system
0· 4
0·3
Other pharynx
30
65
Other pharynx
0·1
0·2
Melanoma of skin
178
22
Thyroid
0·5
0·1
Larynx
35
46
Larynx
0·2
0·1
Larynx
75
76
Larynx
0·3
0·2
Corpus uteri
8
36
Corpus uteri
0·1
0·1
Gallbladder
81
64
Other pharynx
0·3
0·2
Multiple myeloma
50
22
Multiple myeloma
0·2
0·1
Nasopharynx
7 45
Other pharynx
57
79
Gallbladder
0·3
0·2
Multiple myeloma
76
27
Multiple myeloma
0·3
0·1
Melanoma of skin
Nasopharynx
13
71
Nasopharynx
0·1
0·2
Thyroid
Hodgkin lymphoma
35
33
Testis
38
Kaposi sarcoma
Hodgkin lymphoma
0·1 <0·1
Hodgkin lymphoma
14
Testis
0·1 <0·1
Kaposi sarcoma
34
Kaposi sarcoma
<0·1
Testis
Melanoma of skin
0·1 0·0
12
Nasopharynx
<0·1 0·1
14 22
Thyroid
<0·1 0·1
35
9
21
Hodgkin lymphoma
29
Kaposi sarcoma
<0·1
Testis
<0·1 <0·1
4 6
<0·1 <0·1
Higher HDI
Lower HDI
Figure 2: Distribution of cancer types by Human Development Index (HDI) level
(A) Number of new cases. (B) Lifetime cumulative risk of incidence. (C) Number of deaths. (D) Lifetime cumulative risk of death. Kaposi sarcoma not estimated in higher HDI countries.
span available by registry, year of diagnosis (1988–2002),
and 5-year age group. Inclusion in CI5 was chosen as a
general marker of each registry’s data quality over time,
because the CI5 process includes a detailed assessment
of the comparability, completeness, and validity of the
submitted datasets.
We estimated age-standardised incidence and mortality
rates per 100 000 population using the world standard
population,18,19 and estimated the lifetime cumulative risk
for individuals aged 0–74 years, assuming an absence of
competing causes of death.20 To obtain the estimated
annual percentage change in incidence between 1988 and
2002, registry-specific, sex-specific, and cancer-specific
log-linear models were fitted with an identify link, with
the age-standardised incidence rates the response, and
the year of occurrence included as a covariate, with
95% CIs obtained for the annual percentage change.
We present the future burden of cancer in 2030 by sex
for all cancers combined for the four levels of HDI on the
basis of the rates in 2008, assuming population growth
and ageing in 2030 occurs according to the UN World
Population Prospects medium-fertility variant.13 On the
basis of application of the average trends seen for several
common cancers in medium, high, and very high HDI
areas to the rates in 2008, we also provide a trend-based
scenario of the future cancer burden in 2030.
www.thelancet.com/neurology Published online June 1, 2012 DOI:10.1016/S1470-2045(12)70211-5
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Articles
Role of the funding source
There was no funding source for this study. The
corresponding author had full access to all the data in the
study and had final responsibility for the decision to
submit for publication.
Results
Within higher (high and very high) HDI areas, cancers
of the lung, female breast, and colorectum each account
for a very similar number of new cases (about 830 000)
in 2008, with prostate cancer accounting for about
766 000 cases (figure 2). Together, these four cancers
comprised almost half (49%) the total cancer burden in
these areas. In lower (low and medium) HDI areas,
lung cancer was also the most commonly diagnosed
cancer (778 000). However, several types of cancer were
more common in lower HDI areas than they were in
higher HDI areas, including stomach cancer and liver
cancer, which are more common than both female
Population
in 2008
(millions
[% of world
population])
Population
in 2030
(millions
[% of world
population])
Incidence
in 2008
(millions [% of
total global
burden])
Incidence
in 2030*:
demographic
(millions
[absolute %
increase from
2008])
Incidence
in 2030†:
demographic
plus trend
(millions
[absolute %
change from
2008])
Men
Low HDI
196 (5·7%)
332 (7·9%)
0·11 (1·6%)
0·21 (94%)
0·23 (111%)
2266 (66·4%)
2811 (67·2%)
3·0 (44·7%)
5·4 (82%)
5·4 (82%)
High HDI
452 (13·2%)
504 (12·1%)
1·0 (14·4%)
1·6 (68%)
1·8 (90%)
Very high HDI
498 (14·6%)
532 (12·7%)
2·6 (39·3%)
3·8 (46%)
4·5 (75%)
11·0 (66%)
12·0 (81%)
Medium HDI
Worldwide
3412
4179
6·6
Women
Low HDI
Medium HDI§
198 (5·9%)
332 (8·0%)
0·14 (2·3%)
0·27 (92%)
0·27 (92%)
2176 (64·8%)
2722 (66·0%)
2·8 (45·6%)
4·8 (73%)
4·9 (79%)
High HDI
470 (14·0%)
527 (12·8%)
0·9 (15·6%)
1·4 (53%)
1·6 (70%)
Very high HDI
512 (15·3%)
542 (13·2%)
2·2 (36·6%)
2·9 (31%)
3·4 (54%)
6·0
9·4 (55%)
10·2 (69%)
Worldwide
3356
4123
Total
Low HDI
Medium HDI
High HDI
394 (5·8%)
664 (8·0%)
0·25 (2·0%)
4442 (65·6%)
5533 (66·6%)
5·7 (45·1%)
0·48 (93%)
0·49 (100%)
10·1 (78%)
10·3 (81%)
3·4 (80%)
922 (13·6%)
1031 (12·4%)
1·9 (14·9%)
3·0 (60%)
Very high HDI
1010 (14·9%)
1074 (12·9%)
4·8 (38·0%)
6·7 (39%)
7·9 (65%)
Worldwide
6768
8302
20·3 (61%)
22·2 (75%)
12·7
*Based on demographic changes (UN)—the predicted cases worldwide are derived by aggregation of the predicted
cases obtained after the first application of age-specific rates to the demographic forecasts within each Human
Development Index (HDI) level (these numbers will not correspond exactly with those predicted from the single global
figures, because the underlying rates used to derive the predictions from the two sources differ in their age structure
and size). †Based on demographic changes (UN) plus crude assumptions on trends in rates of six cancers on the basis of
changing annual age-adjusted incidence in 101 cancer registries 1988–2002 (figure 5; table 2): annual decreases in
stomach (2·5%, [worldwide in both sexes]), cervical cancer (2% [worldwide]) and lung cancer (1% [high HDI and very
high HDI areas in men only]); increases in colorectal (1% [worldwide both sexes]), lung (1% [high HDI and very high
HDI areas in women only]), female breast (2% [worldwide]), and prostate cancer (3% [worldwide]). See appendix for a
list of countries by HDI region.
Table 1: Estimated numbers of new cases of cancers (all sites excluding non-melanomas) in 2008 and
predicted new cases by 2030
4
breast cancer and colorectal cancer in such areas;
cancers of the cervix and oesophagus are also major
contributors to the cancer burden in lower HDI areas
(figure 2). In combination, these seven cancers account
for nearly two-thirds (62%) of the estimated total cancer
burden in lower HDI areas.
The lifetime cumulative risk of incidence of cancers of
the lung, female breast, colorectum, and prostate are all
more than 3% in higher HDI areas—for the remaining
cancers, only the risk of stomach cancer exceeds 1%
(figure 2). In lower HDI areas, lifetime risk of lung cancer
is highest at 2·3%, with the lifetime risk of five common
cancers—cancers of the stomach, liver, female breast,
colorectum, and oesophagus—varying from 1% to 2%.
A greater proportion of the mortality burden is seen in
low HDI and medium HDI areas, especially for cancers
of the liver, stomach, and oesophagus (figure 2). The
most common causes of cancer death in higher HDI
areas are those of the lung, colorectum, stomach, and
female breast, which comprise about 45% of the total
cancer mortality burden. The four most common types
of cancer death in lower HDI areas include cancers of
the lung and stomach, but also liver cancer and
oesophageal cancer, which together constitute 49% of
the cancer mortality burden in these areas. The lifetime
risk of lung cancer death ranks highest in both higher
HDI and lower HDI areas. The second highest lifetime
risk of cancer death was for colorectal cancer in higher
HDI areas, with stomach and liver cancer equal second
in lower HDI areas; lifetime risk of stomach cancer
death ranked third in both higher HDI and lower HDI
areas (figure 2).
Very high HDI areas seem to bear a larger proportion
of the cancer burden, with almost 40% of the global
incidence estimated to occur in these countries, despite
having only 15% of the world’s population (table 1).
The same five cancers (cancers of the colorectum, lung,
female breast, prostate, and stomach) are the most
commonly diagnosed cancers in both very high and high
HDI areas (figure 3). With an estimated 635 000 cases,
cancer of the colorectum is the most common cancer in
very high HDI areas; and cancers of the lung, female
breast, and prostate all contribute about 597 000 cases or
more. Lung cancer is the most common neoplasm in
medium HDI areas with an estimated 773 000 new cases,
ahead of stomach, liver, and female breast cancer, each
contributing more than half a million new cases annually.
The cancer profile is quite different in low HDI areas,
where cervical cancer is the most common cancer, with
female breast cancer, liver cancer, Kaposi sarcoma, and
non-Hodgkin lymphoma the four other most common
cancers (figure 3).
In terms of age-adjusted incidence rates in men, nine
different types of cancer are estimated as most often
diagnosed, the most common of which being prostate
cancer (most common in 82 countries, mainly in
countries with high HDI levels, but also in central and
www.thelancet.com/neurology Published online June 1, 2012 DOI:10.1016/S1470-2045(12)70211-5
Articles
southern Africa), lung cancer (most common in
47 countries, mainly in eastern Europe and Asia,
including China, India and Indonesia), and liver cancer
(most common in 22 countries, mainly in eastern Africa
and southeast Asia; figure 4). In women, either breast
cancer or cervical cancer are the most common cancer
diagnoses in almost all countries (breast cancer was the
most common cancer diagnosis in 135 countries and
cervical cancer was the most common cancer diagnosis
in 45 countries; figure 4).
In terms of age-adjusted mortality, eight different
cancer types worldwide are represented as the most
common cause of cancer death by country among men
(figure 4). In terms of age-adjusted cancer mortality in
men, lung cancer is the most common cause of cancer
A
death in 94 countries, prostate cancer is the most
common cause in 31 countries, liver cancer is the most
common cause in 24 countries, and stomach cancer is
the most common cause in 18 countries (figure 4). In
women, cancers of the breast and cervix are the most
common causes of cancer death worldwide, with breast
cancer the most common cause in 99 countries and
cervical cancer the most common cause in 55 countries
(figure 4). Lung cancer is the most common cause of
cancer deaths in women in 17 countries. Other distinct
geographical patterns are also evident—eg, clusters of
high incidences of male oesophageal cancer in five
countries in eastern Africa and Kaposi sarcoma in nine
sub-Saharan countries, and high mortality rates of
stomach cancer in South America (figure 4).
Very high Human Development Index
Men
Colorectum
Women
347
Lung
288
385
224
600
Breast
Prostate 597
149
Stomach
B
80
High Human Development Index
Breast
232
Lung
168
Colorectum
96
168
Prostate
82 55
Stomach
C
53
94
Medium Human Development Index
Lung
238
535
Stomach
403
Liver
208
158
391
Breast
527
Colorectum
D
218
182
Low Human Development Index
33
Cervix uteri
Breast
24
Liver
15 8
Kaposi sarcoma
13 6
Non-Hodgkin
Lymphoma
7 5
600
4
2
0
2
New cases in 2008 (thousands)
4
600
Figure 3: Five most frequently diagnosed cancers in terms of new cases estimated in 2008, by Human Development Index level
Maps shows only the countries included in the analysis.
www.thelancet.com/neurology Published online June 1, 2012 DOI:10.1016/S1470-2045(12)70211-5
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Articles
A
Prostate
Lung
Liver
Stomach
Kaposi sarcoma
Oesophagus
Colorectum
Oral cavity
Bladder
B
Lung
Prostate
Liver
Stomach
Kaposi sarcoma
Oesophagus
Colorectum
Bladder
C
Breast
Cervix uteri
Thyroid
Liver
D
Breast
Cervix uteri
Lung
Stomach
Liver
Thyroid
Non-Hodgkin lymphoma
Gallbladder
Figure 4: Incidence and mortality from the most common forms of cancer, by sex
(A) Incidence in men. (B) Mortality in men. (C) Incidence in women. (D) Mortality in women.
Maps show only the countries included in the analysis.
6
Figure 5 plots the estimated annual percentage change
(with 95% confidence limits) based on the trends in
annual age-adjusted incidence rates of lung, female
breast, colorectal, stomach, prostate, liver, and cervical
cancer 1988–2002 by sex in 101 cancer registries which
reside in countries in medium, high or very high HDI
areas. Table 2 presents the simple overall mean of these
according to HDI area. Although the absence of
registries in low HDI areas, together with the few
registries in medium HDI areas (six registries) and high
HDI areas (11 registries) weaken the interpretation of
trends in estimated annual percentage change, some
patterns in the observed trends emerge. Incidence rates
of female breast cancer and prostate cancer have been
increasing in almost all countries, irrespective of HDI
level, with average increases for breast cancer of about
2%; increases for prostate cancer varied between 3·2%
and 7% (table 2). We also observed recorded increases in
colorectal cancer in many registry populations, although
the increases are more evident in registries in medium
HDI areas and high HDI areas (figure 5 and table 2).
We recorded decreases in the incidence of cervical and
stomach cancers (in both sexes) in most of the
populations examined, with mean annual decreases in
rates between about 1% and 3% in medium HDI, high
HDI, and very high HDI countries. The trends for liver
cancer are more varied and perhaps less generalisable
than are those for cervical and stomach cancers
(figure 5). Lung cancer incidence rates in men tend to
be decreasing in most registries, but are increasing in
women—at least in populations with very high HDI
levels (figure 5 and table 2).
The projected demographic changes will mean the
global incidence of cancer in both men and women will
increase from an estimated 12·7 million in 2008 to
20·3 million by 2030 (table 1), a net increase of about
60%. The increases in cancer incidence are proportionally
greatest in lower HDI settings, a 93% increase in both
sexes (table 1).
Worldwide, we project annual increases in the rates of
colorectal cancer, female breast cancer, and prostate
cancer, and, in high HDI to very high HDI areas, for lung
cancer in women (table 2). We project annual decreases
worldwide in stomach cancer and cervical cancer, and, in
high HDI to very high HDI areas, for lung cancer in men
(table 2).
Assuming rates in 2030 of all other cancers remain as
estimated in 2008 (including liver cancer, in view of the
fact that the recorded trends are diffuse between and
within HDI areas), we would see an increase in the
annual incidence of 75% from 2008 to 22·2 million by
2030 (table 1).
Figure 5: The estimated annual percentage change (EAPC) in trends in annual
age-adjusted incidence rates of the seven most common cancers, by level of
Human Development Index (1988–2002)
Each point estimate (with 95% CIs) is one of 101 cancer registries.
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Stomach (men)
EAPC incidence 1988−2002
−10 −6 −2 2
6 10
Stomach (women)
EAPC incidence 1988–2002
−10 −6 −2 2
6 10
Cervix
EAPC incidence 1988−2002
−10−8−6−4−2 0 2 4 6 8 10
Lung (men)
EAPC incidence 1988−2002
−10 −6 −2 2
6 10
Lung (women)
EAPC incidence 1988−2002
−10 −6 −2 2
6 10
Medium
Medium
Medium
Medium
Medium
High
High
High
High
High
Very high
Very high
Very high
Very high
Very high
Liver (men)
EAPC incidence 1988−2002
−10 −6 −2 2
6 10
Liver (women)
EAPC incidence 1988−2002
−10 −6 −2 2
6 10
Colorectum (men)
EAPC incidence 1988−2002
−10 −6 −2 2
6 10
Colorectum (women)
EAPC incidence 1988−2002
−10 −6 −2 2
6 10
Female breast
EAPC incidence 1988−2002
−10 −6 −2 2
6 10
Prostate
EAPC incidence 1988−2002
−10 −6 −2 2
6 10
Medium
Medium
Medium
Medium
Medium
Medium
High
High
High
High
High
High
Very high
Very high
Very high
Very high
Very high
Very high
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Men
Women
Medium
HDI
High HDI Very high
HDI
–2·7%
–2·6%
··
··
Lung
–1·5%
–1·3%
Liver
0·1%
Colorectum
1·5%
Stomach
Cervix uteri
Breast
Prostate
Scenario-based prediction for 2030*
Medium
HDI
High HDI
Very high
HDI
–2·8%
–1·9%
–2·5%
–2·5%
2·5% annual decrease in all HDI areas per year
··
–1·8%
–1·2%
–2·6%
2% annual decrease in all HDI areas per year
–1·6%
–0·5%
0·5%
1·8%
1% annual decrease in high HDI and very high HDI areas (men)
1% annual increase in high HDI and very high HDI areas (women)
0·2%
2·5%
–0·4%
0·4%
2·1%
Difficult to generalise, assume no change
2·8%
0·6%
1·5%
1·8%
0·3%
1% annual increase in all HDI areas per year
··
··
··
2·1%
2·6%
1·6%
2% annual increase in all HDI areas per year
3·2%
7·0%
4·4%
··
··
··
3% annual increase in all HDI areas per year
Data are estimated annual percentage change. HDI=Human Development Index. *Cancer-specific scenarios for the annual percentage change in incidence rates up to 2030
are derived from unweighted averages of the estimated annual percentage change (EAPC) by sex and HDI level when clear directional trends emerged; for cancers of the lung
(low-to-medium HDI) and liver (all HDI levels), we assumed no change in the incidence rates by 2030, in view of the heterogeneity in the direction and magnitude of the
trends, and the need for country-specific information on the tobacco epidemic (for lung cancer); for prostate cancer, we assumed a conservative 3% increase in the incidence
rates per annum (at least relative to the increases in very high HDI settings) for all HDI levels—future trends in prostate cancer incidence will be strongly associated with the
(unknown) future trends in testing for prostate-specific antigen.
Table 2: Changing trends in cancer-specific age-adjusted incidence
Discussion
Cancers of the breast, lung, colorectum, and prostate
account for about 50% of the cancer burden in high HDI
and very high HDI regions, whereas in medium HDI
regions, cancers of the oesophagus, stomach, and liver
are also common, and together these seven cancers
account for about 62% of the burden in low HDI and
high HDI areas. Within low HDI regions, cervical cancer
is more common than both breast cancer and liver
cancer. We identified the nine most common cancers in
men in the 184 countries studied, with cancers of the
prostate, lung, and liver most prevalent. In women,
either breast cancer or cervical cancer was the most
commonly diagnosed neoplasm in almost all countries.
In medium HDI and high HDI settings, the observed
decreases in cervical and stomach cancer incidence seem
to be offset by an increase in the incidence of female
breast, prostate, and colorectal cancers.
To our knowledge, this study is the first global overview
of cancer to investigate patterns of incidence and
mortality in relation to predefined levels of the HDI
(panel).
There has been a scarcity of research examining how
macroeconomic determinants correlate with cancer
incidence, mortality, and survival, and how the relation
varies by cancer type and country. Assessment of these
burden indicators against the specific components of
HDI (education, health, and living standards) should
enable examination of their relative importance. Other
inequality measures might also be of relevance, such as
inequality-adjusted HDI, which equals the HDI when
there is no inequality across a population, but is less than
the HDI when inequality is present.21
Cancer is a heterogeneous mix of diseases with different
types of cancer more common in some populations than
in others, sometimes substantially so.22 Cancers have very
different causes, some of which are well understood and
8
some of which are poorly understood, and differences in
the regional and temporal distribution of risk factors will
determine the geographical and secular patterns of
cancer. Therefore, many barriers exist to the
understanding of global patterns of cancer—the
availability of information about disease incidence and
mortality, an understanding of the underlying causes and
how these can change, and knowledge of the
demographics of populations in terms of size and age
structure.23 Incidence estimates will probably become
more accurate as the number of high quality populationbased cancer registries expands (especially in low-income
and middle-income countries) and the completeness and
validity of registration improves in areas already covered.
Forecasted population data are themselves predictions
based on forecasts of birth and death rates and levels of
immigration and emigration. Projections—and subsequently cancer predictions—can thus be materially
altered when information from more up-to-date censuses
is obtained.
Forecasts are dependent not only on demographics and
risk factors, but also on the extent and modalities of early
detection and screening for cancer, which vary from
country to country. Increasing levels of screening at the
population level have the potential to independently
increase the future cancer incidence burden in many
settings, especially for those cancers in which a precursor
lesion is not the target of the intervention. This would
include prostate and breast cancers, for which incidence
is already increasing in many populations.
We are aware of some ambiguity in the examination of
these trends in countries transiting socially and
economically with time, because we have categorised
each country according to the HDI index of 2007. The
trend analyses for a given population should, therefore,
be considered in relation to the levels of human
development attained for that country in 2007.
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Despite the substantive deficiencies in these domains,
much can be learned from analyses of global patterns of
cancer, and the contrasting patterns in relation to levels
of human development. In both high HDI and very high
HDI regions, four cancers (cancers of the female breast,
lung, colorectum, and prostate) explain almost half the
overall cancer burden. In medium HDI regions, lung
and female breast cancers remain among the most
common types of cancer along with stomach and liver
cancers, which are both associated with infectious
causes.24,25 In low HDI regions, female breast and liver
cancers are also common but two additional infectionrelated cancers—cervical cancer and Kaposi sarcoma—
are also prevalent.
Some cancers seem to be positively associated with the
level of socioeconomic development and colorectal cancer
is a good example of this, with 40% of the global burden
occurring in very high HDI regions despite such regions
comprising only 15% of the world’s population. The
reasons for this association are not clear, although dietary
and metabolic factors associated with a so-called western
lifestyle might be of particular relevance.26 Prostate cancer
is another example of a cancer that is positively associated
with HDI and for which the high incidence is partly a
function of increased access to testing facilities for
prostate-specific antigen in higher-resource regions.27
However, prostate cancer is also the most common cancer
and cause of cancer death in men in several sub-Saharan
African countries—both inherited susceptibility and
environmental and lifestyle exposures could contribute to
the increased rates in these regions. Cervical cancer,
however, is negatively associated with HDI such that it is
the most common cancer in low HDI regions and the
most common cancer and cause of cancer death in
women in several low HDI and middle HDI countries.
Infection with human papillomavirus (HPV) is well
established as a cause of cervical cancer28 and changing
sexual behaviour leading to increasing persistent
infection with high-risk HPV, together with inadequate
facilities for screening, early detection, and treatment
underpin this association. Other infection-related cancers
are also associated with lower HDI (stomach cancer, liver
cancer, and Kaposi sarcoma); Sylla and Wild29 proposed
that control of relevant infections should become a crucial
component of cancer prevention programmes in subSaharan Africa, where the impact of infection is greatest.
Female breast cancer is the only type of cancer that is
common in all regions, irrespective of level of HDI. It is
the most common form of female cancer in the vast
majority of countries in the world and thus the global
control of breast cancer through both early detection and
primary prevention is a high priority. Lung cancer and
other tobacco-associated cancers, although not placed
among the leading cancers in low HDI regions at
present, will become a serious problem unless tobacco
smoking is effectively controlled. Lung cancer is the most
common form of cancer worldwide, it is the leading
Panel: Research in context
Systematic review
We reviewed available studies for key papers on the
descriptive epidemiology of cancer, as well as the evidence for
resource-dependent primary prevention, early detection, and
screening interventions for cancer. We searched Medline for
studies in English, with no date restrictions.
Interpretation
To our knowledge, this study is the first global overview of
present and future patterns of cancer incidence and mortality
in relation to predefined levels of the Human Development
Index (a marker of socioeconomic development). Public
health clinicians and cancer control specialists should be
alerted to the increasing magnitude of cancer incidence and
mortality worldwide, the differing cancer profiles that emerge
according to level of human development, and the changing
cancer profiles as countries continue to change both socially
and economically. Cancer is already the leading cause of death
in many high-income countries and is set to become a major
cause of morbidity and mortality in the next decades in every
region of the world; this study serves as an important
reference point in drawing attention to the need for global
action to reduce the increasing burden of cancer. It should
also serve as a catalyst for further work on human inequality
and cancer from a global perspective, to better determine
how and why macroeconomic determinants affect cancer
incidence, mortality, and survival.
cause of cancer deaths in men in many countries, and is
the most common form of cancer death in women in
North America, parts of Europe, and China.
In terms of cancer incidence trends over time, analysis
of the high quality cancer registry data draws attention to
some important aspects of the global cancer transition.
A tendency towards increases in breast, colorectal, and
prostate cancers exist in the very high HDI, high HDI,
and medium HDI regions (where data are available).
These effects seem to be stronger in countries with very
high HDI levels relative to those of medium HDI or high
HDI, which might be indicative of an incidence plateau
having being reached, at least in some very high HDI
populations. Colorectal cancer trends, in particular, seem
to be stable or decreasing in several very high HDI
populations. Nevertheless, the trends point to the
westernisation effect in countries with high HDI or
medium HDI levels, and with increasing average levels of
social and economic development, the population
prevalence of several reproductive, dietary, metabolic, and
hormonal risk factors (towards levels more similar to
those commonly seen in high-income countries) could
correspondingly increase the risk of these cancers.
To some extent, these increases in incidence are
countered by another hallmark of cancer transition, a
reduction in infection-based cancers. Decreases in the
incidence of stomach and cervical cancers are uniformly
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seen in populations with very high, high, and medium
HDI levels. The reduction in cervical cancer burden has
been attributed to corresponding decreases in risk in
older generations of women and, within higher-resource
settings, the beneficial effects of mass screening cytology
programmes.30 The uniform decreases of stomach cancer
during the past 50 years are commonly ascribed to both a
reduction in Helicobacter pylori infection in successive
birth cohorts related to changing childhood environment,
and to improved food preservation practices and better
nutrition.30 The onset of refrigeration for food transport
and storage could have been vital in reduction of salt
consumption by largely eradicating the need for salting,
smoking, and pickling of foods.30,31
Liver cancer is the other infection-related cancer
examined here, and for which the incidence trends
show much more heterogeneity across populations
within each of the three HDI categories assessed. The
assumptions that trends will stay unchanged is, however,
perhaps unduly pessimistic in view of the prospects for
prevention of hepatocellular carcinoma through mass
immunisation against hepatitis B virus infection. In
Taiwan, for instance, the preventability of hepatocellular
carcinoma (after vaccination of all newborn babies in
1984) has been shown beyond childhood to early
adulthood in a 20-year follow-up study.32 In China, where
most liver neoplasms are diagnosed (about 0·35 million
incident cases and deaths estimated per year11), neonatal
hepatitis B vaccination programmes have been expanded
as part of the China-GAVI project.33
With a few exceptions, lung cancer rates in men have
been decreasing in the populations with very high, high,
and medium HDI levels examined here, but have been
increasing in women in the same populations. These
contrasting sex-specific trends in very high HDI settings
are in line with the respective population-specific rise and
fall in adult cigarette consumption in the past decades.
Evidently, other tobacco-related cancers—including
cancers of the bladder, oesophagus, and oral cavity, which
are the 8th, 9th, and 14th most frequent neoplasms
worldwide, respectively—will alter patterns of tobacco
consumption in different regions and countries change.
This study attempted to incorporate cancer-specific
time trends on the basis of recorded data to inform on
the future cancer burden, but a more detailed appraisal
would take into account the specific preventative actions
in operation in the respective countries and regions of
the world, and is an important next step. The trend-based
scenario extrapolates recorded rates by use of crude
averages of the estimated annual percentage change that
are heterogeneous across registries in every HDI
category, and thus should be interpreted with caution.
One clear concern is the reliance on extrapolation of
trends in just six population-based cancer registries
(including two each from China and India) to be
representative of all medium-resource settings. Clearly,
more data and greater precision are needed, although we
10
believe that the scenarios selected in table 2 for making
projections to 2030 are sufficiently reasonable to take at
least preliminary account of the rate changes for some of
the major cancers globally.
Forouzanfar and colleagues34 presented trends in breast
and cervical cancer between 1980 and 2010 in
187 countries using a unified modelling framework that,
as well as being comprehensive, potentially provides
greater comparability between countries. However,
comparisons of their modelled cumulative risk estimates
(ages 15–79 years) of breast cancer incidence with data
from four longstanding Nordic population-based cancer
registries showed a systematic overestimation in all four
countries,35 and the uniformly decreasing trends in
cervical cancer incidence in Uganda reported by
Forouzanfar and colleagues were at odds with the rapidly
increasing trends reported in Kampala 1991–2006,36
which were based on registry data that were considered
to be of high quality.37 Our approach to the trend analyses
and future extrapolations centres around use of observed
data, and although more restrictive than Forouzanfar and
colleagues’, adheres to the principle that results obtained
from models should reasonably agree with actual
observations that are thought to be of reasonable
accuracy. The scarcity of historical time-trend data for
any low HDI populations is an important drawback in
view of the different contemporary patterns of cancer in
these populations, mainly in sub-Saharan Africa, and
correction of this deficiency will be crucial to the
development of cancer control plans in this region. The
projected decreases in cervical cancer worldwide might
be rather over-optimistic in low HDI settings where
screening and early treatment have not yet had an effect.
In terms of the global burden predictions, however, the
low HDI populations constitute 5·7% of the world’s
population and 1·6% of the cancer burden, and the
absence of this information will have a minor effect.
However, the potential effect of major changes in the
rates of common cancers in the vast populations of China
and India is enormous. The tobacco epidemic and its
effect on tobacco-related cancers in China, for instance,
will heavily affect the predicted number of global cancer
cases by 2030. The prevalence of smoking in men, for
example, has risen sharply in many medium-HDI
countries, including China and Indonesia. The future
burden of lung cancer and other smoking-related cancers
in men (in low HDI and medium HDI areas) and women
(globally) will largely depend on smoking practices at the
population level, including the duration of smoking, the
extent of cessation, the types of tobacco smoked, and the
patterns of consumption.38
The incidence and mortality estimates from
GLOBOCAN for 2008 are also subject to precision
limitations. In the compilation of country-specific cancer
incidence and mortality, a hierarchy of methods is used in
GLOBOCAN with accuracy dependent on the quality and
availability of the source information at a given time, and
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Articles
as such requires constant review. For example, national
estimates of cancer incidence in India are based on
corresponding rates obtained from the urban and rural
population-based cancer registries, whereas national
mortality is derived from incidence and survival estimates.
In view of the possible concerns with the accuracy of
cancer deaths in India (and in other low-income and
middle-income countries) related to the number of deaths
occurring at home and without medical attention, the
mortality estimates reported by Dikshit and colleagues,39
which were based on a nationally representative sample of
1·5 million households, could complement the
GLOBOCAN estimates, although the methodological
differences need further assessment.40 More generally,
there is a scarcity of high quality population-based cancer
registries in Africa, Asia, and Latin America, with about
1%, 4%, and 6% of the populations of these respective
regions covered, and there are few national vital
registration systems with adequate mortality data in lowresource and medium-resource countries, especially in
Africa and Asia. Although GLOBOCAN is a comprehensive
data source for examination of the cancer burden
worldwide and in the promotion of global cancer control,
population-based cancer registries have been shown to be
a crucial component in national cancer control strategies,
where the registered incidence information provides the
means to plan, monitor, and assess the effect of specific
interventions in targeted populations.10,41
This study underscores the diversity of cancer as a
worldwide occurrence and the extent to which the disease
patterns vary from country to country. Classification of
these populations by broad levels of human development
does, however, draw attention to some of the key
determinants of such variations, especially in countries
rapidly transiting from lower to higher levels of human
development. The reduction in infection-related cancers
seems to be being offset by concomitant increases in
cancers related to a westernisation of lifestyle and
changes in tobacco consumption and the effect on lung
and other cancers.
Although forecasted demographic changes will probably
increase the number of people with cancer to more than
20 million per year by 2030, targeted interventions can
substantially reduce this number through resourcedependent interventions. Such actions include primary
prevention strategies to effectively control the prevalence
of lifestyle factors including tobacco avoidance and
cessation of smoking, a reduction in alcohol consumption
and obesity, and the promotion of increased levels of
physical activity; as well as the implementation of
vaccination programmes (for liver and cervical cancer),
and early detection programmes (for colorectal, breast, and
cervical cancer). Further reductions in mortality could be
brought about by increasing access to curative treatment
for specific cancers (including cervical, breast, and
colorectal cancer), while increasing access to palliative care
for those patients dying of cancer will reduce the inequities.
Contributors
FB contributed to the data collection, study design, analysis, and writing
of the paper. JF contributed to data collection, analysis, and writing of
the paper. AJ and NG contributed to the writing of the paper. DF
contributed to drafting and finalising the paper. All authors read and
approved the final paper.
Conflicts of interest
We declare that we have no conflicts of interest.
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