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Gut Online First, published on January 27, 2016 as 10.1136/gutjnl-2015-310912
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ORIGINAL ARTICLE

Global patterns and trends in colorectal cancer

incidence and mortality
Melina Arnold,1 Mónica S Sierra,1 Mathieu Laversanne,1 Isabelle Soerjomataram,1
Ahmedin Jemal,2 Freddie Bray1

▸ Additional material is ABSTRACT

published online only. To view, Objective The global burden of colorectal cancer Significance of this study
please visit the journal online
(http://dx.doi.org/10.1136/
(CRC) is expected to increase by 60% to more than
gutjnl-2015-310912). 2.2 million new cases and 1.1 million deaths by 2030.
In this study, we aim to describe the recent CRC What is already known on this subject?
1
Section of Cancer incidence and mortality patterns and trends linking the ▸ Colorectal cancer (CRC) is the third most
Surveillance, International findings to the prospects of reducing the burden through commonly diagnosed malignancy and the
Agency for Research on cancer prevention and care. fourth leading cause of cancer-related deaths in
Cancer, Lyon, France Design Estimates of sex-specific CRC incidence and
2
Surveillance Research
the world, and its burden is expected to
Program, American Cancer
mortality rates in 2012 were extracted from the increase by 60% to more than 2.2 million new
Society, Atlanta, Georgia, USA GLOBOCAN database. Temporal patterns were assessed cases and 1.1 million cancer deaths by 2030.
for 37 countries using data from Cancer Incidence in ▸ CRC is considered one of the clearest markers
Correspondence to Five Continents (CI5) volumes I–X and the WHO of the cancer transition, whereby countries
Dr Melina Arnold, Section of
mortality database. Trends were assessed via the annual undergoing rapid societal and economic
Cancer Surveillance,
International Agency for percentage change using joinpoint regression and changes show rapid increases in cancers
Research on Cancer, 150 discussed in relation to human development levels. already more frequent in high-income
Cours Albert Thomas, Results CRC incidence and mortality rates vary up to countries.
Lyon 69008, France;
[email protected]
10-fold worldwide, with distinct gradients across human ▸ Understanding the current patterns of CRC and
development levels, pointing towards widening its evolution from an international perspective
Received 16 October 2015 disparities and an increasing burden in countries in is imperative in order to direct future prospects
Revised 12 November 2015 transition. Generally, CRC incidence and mortality rates of reducing the burden through cancer
Accepted 13 November 2015 are still rising rapidly in many low-income and middle- prevention and cancer care.
income countries; stabilising or decreasing trends tend to
be seen in highly developed countries where rates What are the new findings?
remain among the highest in the world. ▸ CRC incidence and mortality rates vary widely
Conclusions Patterns and trends in CRC incidence and worldwide, with distinct gradients across
mortality correlate with present human development human development levels and trends point
levels and their incremental changes might reflect the towards widening disparities and an increasing
adoption of more western lifestyles. Targeted resource- burden in countries in transition.
dependent interventions, including primary prevention in ▸ We identified three patterns of CRC incidence
low-income, supplemented with early detection in high- and mortality trends and ascertained that CRC
income settings, are needed to reduce the number of incidence and mortality rates are still rising
patients with CRC in future decades. rapidly in many low-income and middle-income
countries, linked to ongoing societal and
economic development; stabilising or
decreasing trends tend to be seen only in
INTRODUCTION highly developed countries where rates remain
Colorectal cancer (CRC) is the third most com- among the highest in the world.
monly diagnosed malignancy and the fourth How might it impact on clinical practice in
leading cause of cancer death in the world, the foreseeable future?
accounting for about 1.4 million new cases and ▸ Without targeted resource-dependent actions
almost 700 000 deaths in 2012.1 The distribution based on this evidence, the number of patients
of CRC burden varies widely, with more than with CRC will continue to increase in future
two-thirds of all cases and about 60% of all deaths decades.
occurring in countries with a high or very high ▸ Improvements in treatment options and
human development index (HDI).1 CRC is consid- accessibility are vital, particularly in low-income
ered one of the clearest markers of the cancer tran- and middle-income countries that face an
To cite: Arnold M,
Sierra MS, Laversanne M,
sition, replacing infection-related cancers in increasing burden of CRC.
et al. Gut Published Online countries undergoing rapid societal and economic ▸ Prioritisation of primary prevention and early
First: [ please include Day changes together with other cancers predominantly detection are necessary, alongside their
Month Year] doi:10.1136/ linked to western lifestyles, which are already fre-
gutjnl-2015-310912
integration into existing healthcare plans.
quently found in high-income countries.2–4

Arnold M, et al. Gut 2016;0:1–9. doi:10.1136/gutjnl-2015-310912 1

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Rapid increases in both CRC incidence and mortality are evolution from an international perspective is therefore
now observed in many medium-to-high HDI countries particu- imperative, and in this study, we describe the geographical var-
larly in Eastern Europe, Asia and South America.2 In contrast, iations in CRC incidence and mortality in 184 countries and
CRC incidence and mortality rates have been stabilising or time trends in 37 countries, linking the findings to the future
declining in a number of the highest indexed HDI countries: prospects of reducing the burden through cancer prevention
the USA, Australia, New Zealand and several Western and care.
European countries.2 The reasons for the recent declining
trends in incidence in these countries are ill-defined and likely METHODS
numerous but may partially reflect increased early detection Incidence and mortality estimates of malignant neoplasms of the
and prevention through polypectomy (at least in the USA). colon and rectum (ICD-10 C18-21) by country for 184 coun-
Together with the factors that have brought about declines in tries in 2012 were extracted from the GLOBOCAN database.1
incidence, improvements in perioperative care, as well as Data on HDI for the same year were obtained from the United
chemotherapy and radiotherapy, will have contributed to the Nations Development Programme.7
uniformly decreasing trends in CRC mortality in many high- To assess time trends in CRC incidence and mortality, we
income settings.5 6 used data from two different sources with the requirement of at
Given the temporal profiles and demographic projections, least 15 consecutive years of data, and the availability of both
the global burden of CRC is expected to increase by 60% to incidence and mortality data for each country included. For
more than 2.2 million new cases and 1.1 million cancer deaths CRC incidence, data series from high-quality regional and
by 2030.1 Understanding the current patterns of CRC and its national population-based cancer registries were extracted from

Figure 1 Worldwide colorectal cancer incidence and mortality rates (age adjusted according to the world standard population, per 100 000) in
males in 2012 (GLOBOCAN 20121).
2 Arnold M, et al. Gut 2016;0:1–9. doi:10.1136/gutjnl-2015-310912
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the Cancer Incidence in Five Continents (CI5) series Volumes observed with increasing levels of HDI: incidence rates in coun-
I–X,8 complemented with publically available data from tries with a very high HDI were six times greater than countries
European countries,9 10 11 Australia,12 New Zealand,13 and the with a low HDI (figure 2A). Geographical patterns of CRC
USA14 for more recent years. Of the 37 countries studied, mortality rates generally followed those of incidence, although
national incidence data were available for 25 countries. For the the highest rates observed tended to be in countries with high
remaining countries, data from regional registries were pooled rather than very high HDI in Central and Eastern Europe and
to obtain a proxy of the national incidence (see online supple- Latin America (figure 1). As with incidence, mortality showed a
mentary annex table S1). National mortality data series were distinct gradient across HDI levels (figure 2B), while compari-
extracted from the WHO mortality database, with the minimal sons of incidence-to-mortality revealed higher case fatalities
inclusion criteria set at the WHO-defined medium data quality among countries indexed with lower levels of HDI.
level, ensuring a reasonable degree of population coverage, com-
pleteness and accuracy.15 Rates were age-standardised (ASR) to Trends in incidence and mortality from CRC
the world standard population.16 Based on temporal characteristics of incidence and mortality
To analyse incidence and mortality trends, we used joinpoint (in males), three different groups of countries were identified
regression,17 which involves fitting a series of joined straight (table 1): those with increasing or stable incidence and mortal-
lines to ASR trends. A logarithmic transformation of the rates, ity (group 1, n=14 countries), those with increasing incidence
calculation of SEs using the binomial approximation, and a and decreasing mortality (group 2, n=14 countries) and those
maximum number of three joinpoints were specified as options with decreasing incidence and mortality (group 3, n=9 coun-
in the analysis. To estimate the magnitude and direction of tries). The results are presented according to these three
recent trends, we calculated the average annual percentage categories.
change (AAPC) and the corresponding 95% CI for the last avail-
able 10 years. The AAPC is a geometrically weighted average of Group 1: increasing incidence and mortality
the different annual percentage changes from the joinpoint Increases in both incidence and mortality over the most recent
trend analysis, for which weights are equal to the length of each 10-year period were seen in this group, comprising several
segment during the specified time interval. Eastern European countries, and also in populations in Latin
America and Asia (see figures 3A and 4A/B; online supplemen-
RESULTS tary annex tables S2 and S3). In males, the largest increases in
Incidence and mortality patterns of CRC in 2012 incidence were seen in Brazil (AAPC 7.2, 95% CI −7.5 to 24.2),
In 2012, the estimated incidence rates in males varied from <5 Costa Rica (3.6, 95% CI 3.1 to 4.2) and Bulgaria (3.6, 95% CI
( per 100 000) in several African countries to over 40 in certain 3.1 to 4.2), while mortality rates rose most rapidly in the
countries in Europe, Northern America and Oceania (figure 1). Philippines (5.7, 95% CI 4.7 to 6.7) and Belarus (3.4, 95% CI
The highest rates in males were observed in Slovakia (61.6), 2.5 to 4.3). Incidence uniformly rose in all countries within this
Hungary (58.9) and the Republic of Korea (58.7), while the group, while mortality rates appeared to level off in Bulgaria,
lowest were seen in sub-Saharan Africa, in The Gambia and Russia, Croatia, Spain, Latvia and Estonia. Trends in females
Mozambique (both 1.5 per 100 000). Geographical patterns were similar to those in males, although both incidence and
were very similar between the sexes, although rates in females mortality were generally lower except in Latin American coun-
tended to be lower (25% less) than their male counterparts tries (Brazil, Costa Rica and Colombia), where rates in males
(data not shown, see ref. 1). Gradients in incidence were and females were quite similar.

Figure 2 Correlation between age-standardised colorectal cancer incidence (left panel) and mortality rates (right panel) and human development
index (HDI) in both sexes combined (GLOBOCAN 20121).
Arnold M, et al. Gut 2016;0:1–9. doi:10.1136/gutjnl-2015-310912 3
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Northern European countries and in Canada. Although mortal-

Table 1 Trends in colorectal cancer incidence and mortality: three
ity rates decreased most remarkably in Ireland (−2.1, 95% CI
groups of temporal pattern
−2.9 to −1.3) and Denmark (−1.9, 95% CI −2.3 to −1.6), the
Group 1: incidence ↑ Philippines*, China*, Colombia†, Bulgaria†, Costa corresponding incidence rates remained constant during the
mortality ↑ Rica†, Brazil†, Russia†, Belarus†, Estonia, Lithuania, most recent 10-year period. As declining mortality rates were
Croatia, Spain, Latvia, Poland
also observed in the UK (−2.0, 95% CI −2.2 to −1.8), these
Group 2: Canada, Denmark, Switzerland, Ireland, Sweden,
incidence ↑ mortality ↓ Singapore, Finland, Norway, Slovakia, UK, Netherlands,
were, however, paralleled by a significant average increase of
Italy, Malta, Slovenia 1.3% per year in incidence. Trends were similar in both sexes.
Group 3: US (White), US (Black), Austria, New Zealand, Czech
incidence ↓ mortality ↓ Republic, Iceland, France, Japan, Australia, Israel Group 3: decreasing incidence and mortality
*Medium human development index (HDI), refers to 0.534 < HDI ≤ 0.710. Decreases in both CRC incidence and mortality in this group
†High HDI refers to 0.710 < HDI ≤ 0.796. were restricted to the highest HDI countries such as Australia,
Very high HDI (all remaining countries) refers to HDI > 0.796.
Iceland, New Zealand and Japan (see figures 3C and 4A/B;
online supplementary annex tables S2 and S3). While the mag-
nitude of declining incidence in males were marked among US
Group 2: increasing incidence and decreasing mortality Whites (AAPC −3.0, 95% CI −3.3 to −2.7) and Blacks (−2.2,
In this group, incidence rates continued to increase while mor- 95% CI −3.3 to −1.0), mortality declines were greatest (−4.6%
tality rates decline, an observation seen in several European per annum) in the Czech Republic. Again, patterns were similar
countries, and also in Canada and Singapore (see figures 3B and for males and females.
4A/B; online supplementary annex tables S2 and S3). The rate
of increase in incidence in males was marked in Southern DISCUSSION
European countries including Slovenia (2.7, 95% CI 0.5 to 5.0), This paper provides a comprehensive overview of the patterns
Malta (1.7, 95% CI 0.5 to 2.9) and Italy (1.7, 95% CI 1.5 to and trends in the overall CRC incidence and mortality world-
1.9), while stable or slight rises in trends were observed in wide. CRC incidence and mortality rates varied widely, with

Figure 3 (A) Trends in colorectal cancer incidence and mortality in males (M) and females (F) by country (group 1: increasing or stable incidence
and mortality). §Regional data. (B) Trends in colorectal cancer incidence and mortality in males (M) and females (F) by country (group 2: increasing
incidence and decreasing mortality). §Regional data. (C) Trends in colorectal cancer incidence and mortality in males (M) and females (F) by country
(group 3: decreasing incidence and mortality). §Regional data.
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Figure 3 Continued

Figure 3 Continued

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distinct gradients across HDI levels. We identified three patterns from the mid-1950s until the early-1970s to mid-1970s. The
of CRC incidence and mortality trends: (1) increases in both slow increase until the last decade has been met with marked
incidence and mortality in the most recent decade, as observed concomitant increases in both colon cancer incidence and
in rapidly transitioning countries (eg, medium and high HDI mortality during the years 1990–2000.51 The rapid transition
countries including those in the Baltics, as well as Russia, China in income and economic growth in low-income and
and Brazil), (2) increases in incidence, with concomitant middle-income countries has shifted dietary patterns towards an
decreases in mortality, as seen in very high HDI countries increased intake of fat, sugar and animal-source foods.52
including Canada, UK, Denmark and Singapore and (3) Changes in the food environment including access to cheaper
decreases in both incidence and mortality, as observed in a ‘junk’ food were also paralleled by reductions in physical activ-
number of the highest HDI-indexed countries including the ity and increases in sedentary behaviour, fuelled by both
USA, Japan and France. increases in overweight and obesity and changes in the built
The mortality declines observed in latter two groups affect environment.53
both sexes and have been previously reported in North America Increases in mortality have been reported in several countries
(the USA and Canada5 18), Oceania (Australia and New in Latin America, the Caribbean and Asia,54 55 and these may
Zealand), most European countries (other than Croatia, reflect limited health infrastructure and poorer access to early
Romania, Latvia, Estonia and Russia) and Asia ( Japan).2 These detection and treatment.56 Survival from CRC depends heavily
can partly be linked to improving survival through the adoption on the stage at diagnosis,57–59 and the unfavourable distribution
of best practices in cancer treatment and management for of advanced cancers in low-income and middle-income coun-
CRC.19 20 Removal of polyps and early detection efforts,21–24 tries may explain the higher M:I ratios as well as increases in
including the adoption of colonoscopy, flexible sigmoidoscopy, mortality in these countries. For colon cancer, typically the
CT colonography, faecal immunochemistry testing and faecal tumour and corresponding lymph vessels are removed during
occult blood testing, may be responsible for the rest of the surgery and adjuvant chemotherapy is administered to patients
observed trends. The introduction of screening tests may ini- at high risk of relapse.60 As for rectal cancer, complete removal
tially increase CRC incidence rates due to the detection of of the mesorectum is the standard surgical procedure that has
undiagnosed disease but has been shown to reduce incidence been shown to increase survival and substantially decrease the
longer term due to the removal of precancerous polyps during risk of recurrence.60 61 In addition, typically a combination of
colonoscopy.24 This may be particularly pertinent in explaining (neo)adjuvant chemotherapy and radiotherapy is administered,
the uniformly decreasing mortality trends in the USA, Israel and whereby the recommended regimen depends heavily on the
Japan, countries where organised screening and early detection tumour type and stage at diagnosis. Yet, in low-income settings
programmes have been established since the 1990s.25 However, such as sub-Saharan Africa, surgery is often the only available
the extent to which screening interventions are responsible for treatment option and adjunctive therapy often not available.62
the recent reduction in incidence rates in these countries, rela- Among all patients with cancer receiving radiotherapy in low-
tive to a reduction in risk via a changing prevalence and distri- income and middle-income countries only 1.3% and 3.1%
bution of the key risk factors, is difficult to clarify at present. received radiotherapy for cancers of the colon and rectum,
Other high-income countries have introduced organised screen- respectively, while the ‘optimum’ proportion should have been
ing practices very recently; it is however unlikely that screening 14% and 61%, respectively.58 Furthermore, delays in diagnosis,
has materially influenced recent incidence trends in these referral and treatment and also cultural beliefs and financial con-
countries. straints, for example, in rural areas of Latin America, may
The presence of birth cohort effects implies the importance explain part of the higher mortality in this region.62 63
of changing risk in successive generations in contributing to the This study has a number of strengths and limitations. We have
recent plateau or declines in incidence observed in certain very aimed to provide a comprehensive analysis of geographical var-
high HDI countries without long-standing organised screening iations of both CRC incidence and mortality in 2012 by sex and
programmes, most notably Australia, New Zealand and several the corresponding trends in both indicators in 37 countries.
European countries.26 Certainly, changes in the prevalence of Attention should be drawn to lack of availability of recorded
lifestyle-related factors linked to the extent of ‘westernisation’ (registry) incidence and mortality data ( particularly in low-
are likely to be, in part, responsible for the global variation in income and middle-income countries) in deriving national inci-
CRC incidence as well as the observed increasing incidence dence and mortality estimates in 184 countries as part of our
trends in countries in transition in groups (1) and (2). These GLOBOCAN compilation; only one-third and one-fifth of the
modifiable risk factors include alcohol consumption,27–29 poor world’s countries presently report high-quality incidence and
diet (low consumption of fruits and vegetables, and high con- mortality data, respectively. For the trends analyses, we used
sumption of red/processed meats),30–36 obesity,37 38 physical CI5 data of high comparability, completeness and validity to
inactivity39 40 and smoking.41–43 Despite higher relative risks, assess trends in incidence. In using national mortality, we used
family history of CRC44 and IBD45 accounts for only a small only data with at least WHO-defined medium levels of com-
proportion of the observed variation of CRC burden globally pleteness and coverage.
given their lower prevalence. Established protective factors that The intention was to provide a global snapshot of the scale
could partly explain stabilising of incidence rates in high-income and profile of CRC today, using high-quality data wherever
countries include the regular use of aspirin,46 47 the use of oes- possible. This study serves as a pointer to show how the
trogens after menopause48 and possibly vitamin D intake.49 disease burden is likely to develop in low-income countries in
Dietary patterns and the overall composition of diet have the longer term and highlights the pressing need for cancer
shifted dramatically over the past half-century, with distinct dif- control action to halt the rising mortality rates in many low-
ferences within world regions and individual countries. In income and middle-income countries. While the scope of this
Japan, for example, cereal consumption decreased sharply and study necessitates a general approach, the main weakness stems
vegetable consumption remained almost stable since the 1950s from a lack of granularity in the analyses. We have not
until 1990.50 In contrast, meat and fat intake increased sharply included here a separate assessment of colon and rectal cancer,
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Figure 4 (A) Average annual percentage change (AAPC) of colorectal cancer incidence and mortality in the most recent period (10 years), males.
(B) AAPC of colorectal cancer incidence and mortality in the most recent period (10 years), females.

nor did we examine variations in distal (left-sided) cancers of Decreases in incidence (also seen in recent birth cohorts) in high
the rectosigmoid junction and proximal (right-sided) cancers of HDI and high-risk countries are likely driven by changes in life-
the descending and sigmoid colon, despite many studies style and dietary patterns over the past decades, which might
reporting a rising proportion of the latter tumours. The inclu- translate into further future rate declines as these cohorts age.
sion of birth cohort analyses would also have led to a more Early detection and screening might have led to short-term
robust assessment of the recent direction of trends enabling increases in incidence, but such interventions will eventually
the generation of hypotheses linked to the changing prevalence contribute to mortality reductions through the increased detec-
of causative factors in successive cohorts and the impact of tion of early-stage tumours.
early-stage factors and early-in-life experiences, and their The fact that CRC has replaced infection-related cancers as
further study will increase our understanding of the aetiology the second most common cancer in several middle-income
of this cancer. countries ( particularly among women) highlights the major chal-
Diverse global CRC patterns and trends point towards widen- lenge of CRC control in countries undergoing significant socio-
ing disparities and an increasing burden in countries in transi- economic transition, and the importance of continued efforts to
tion. Generally, CRC incidence and mortality rates correlate monitor trends in CRC incidence, mortality and survival world-
with the adoption of a western lifestyle; while they are still wide. Without targeted resource-dependent actions based on
rising rapidly in many low-income and middle-income countries this evidence, the number of patients with CRC will continue to
linked to ongoing societal and economic development, in highly increase in future decades beyond those already projected as a
developed countries, rates are stabilising or decreasing. result of population ageing and population growth.
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Figure 4 Continued

Improvements in treatment options and accessibility, including REFERENCES

tertiary care, are vital in low-income and middle-income coun- 1 Ferlay J, Soerjomataram I, Ervik M, et al. GLOBOCAN 2012 v1.0, Cancer Incidence
tries that face an increasing burden of CRC. In light of the and Mortality Worldwide: IARC Cancer Base No. 11. Lyon, France: International
Agency for Research on Cancer, 2013.
limited capacity for health service provision and associated 2 Center MM, Jemal A, Smith RA, et al. Worldwide variations in colorectal cancer.
costs, however, there remains an overwhelming need to priori- CA Cancer J Clin 2009;59:366–78.
tise and integrate primary prevention and early detection mea- 3 Bosetti C, Rodríguez T, Chatenoud L, et al. Trends in cancer mortality in Mexico,
sures into existing healthcare plans.64 1981–2007. Eur J Cancer Prev 2011;20:355–63.
4 Bray F. Transitions in human development and the global cancer burden. In:
Acknowledgements The authors gratefully acknowledge all cancer registries and Steward BW, Wild CP, eds. World Cancer Report 2014. Lyon: International Agency
their staff who have contributed in sharing their data needed for this study. This for Research on Cancer, 2014, 54–68.
work was undertaken during the tenure of a Postdoctoral Fellowship to Dr Mónica 5 Center MM, Jemal A, Ward E. International trends in colorectal cancer incidence
S. Sierra from The International Agency for Research on Cancer, partially supported rates. Cancer Epidemiol Biomarkers Prev 2009;18:1688–94.
by the European Commission FP7 Marie Curie Actions—People—Co-funding of 6 Murphy CC, Harlan LC, Lund JL, et al. Patterns of colorectal cancer care in the
regional, national and international programmes (COFUND). United States: 1990–2010. J Natl Cancer Inst 2015;107.
7 Human Development Report 2013. The rise of the south: human progress in a
Contributors Study concept and design: MA, ML, MSS and FB. Analysis and diverse world. New York: United Nations Development Programme (UNDP),
interpretation of data: all authors. Drafting the manuscript: MA, MSS and FB. 2013.
Critical revision of the manuscript for important intellectual content: all authors. 8 Forman D, Bray F, Brewster DH, et al. Cancer Incidence in Five Continents, Vol. X
Competing interests None declared. (electronic version). Lyon: IARC, 2013. http://ci5.iarc.fr
9 Steliarova-Foucher E, O’Callaghan M, Ferlay J, et al. European Cancer Observatory:
Provenance and peer review Not commissioned; externally peer reviewed. Cancer Incidence, Mortality, Prevalence and Survival in Europe. Version 1.0

8 Arnold M, et al. Gut 2016;0:1–9. doi:10.1136/gutjnl-2015-310912

 Downloaded from http://gut.bmj.com/ on August 11, 2016 - Published by group.bmj.com

Colon
(September 2012). European Network of Cancer Registries, International Agency for 36 Matos E, Brandani A. Review on meat consumption and cancer in South America.
Research on Cancer. http://eco.iarc.fr Mutat Res 2002;506–507:243–9.
10 Engholm G, Ferlay J, Christensen N, et al. NORDCAN: Cancer Incidence, Mortality, 37 Renehan AG, Tyson M, Egger M, et al. Body-mass index and incidence of cancer:
Prevalence and Survival in the Nordic Countries, Version 7.1 (09.07.2015). a systematic review and meta-analysis of prospective observational studies. Lancet
Association of the Nordic Cancer Registries. Danish Cancer Society. http://www. 2008;371:569–78.
ancr.nu 38 Food, Nutrition, Physical activity, and the Prevention of Colorectal Cancer.
11 Russian Federation. Moscow Research Oncological Institute. http://www.oncology.ru Continuous Update Project Report. World Cancer Research Fund/American Institute
12 Cancer in Australia. Australian Institute of Health and Welfare. http://www.aihw. for Cancer Research, 2011.
gov.au/ 39 Samad AK, Taylor RS, Marshall T, et al. A meta-analysis of the association of
13 New Zealand National Ministry of Health. http://www.nzhis.govt.nz/ physical activity with reduced risk of colorectal cancer. Colorectal Dis
14 SEER. SEER*Stat Database: Incidence—SEER 9 Regs Research Data, November 2005;7:204–13.
2013 Sub (1992–2011) Surveillance, Epidemiology, and End Results (SEER) 40 Harriss DJ, Atkinson G, Batterham A, et al. Lifestyle factors and colorectal cancer
Program. 2013. http://www.seer.cancer.gov risk (2): a systematic review and meta-analysis of associations with leisure-time
15 Mathers CD, Fat DM, Inoue M, et al. Counting the dead and what they died from: physical activity. Colorectal Dis 2009;11:689–701.
an assessment of the global status of cause of death data. Bull World Health Organ 41 Walter V, Jansen L, Hoffmeister M, et al. Smoking and survival of colorectal cancer
2005;83:171–7. patients: systematic review and meta-analysis. Ann Oncol 2014;25:1517–25.
16 Segi M, Fujisaku S, Kurihara M. Geographical observation on cancer mortality by 42 Botteri E, Iodice S, Bagnardi V, et al. Smoking and colorectal cancer: a meta-analysis.
selected sites on the basis of standardised death rate. Gan 1957;48:219–25. JAMA 2008;300:2765–78.
17 Kim H-J, Fay MP, Feuer EJ, et al. Permutation tests for joinpoint regression with 43 Liang PS, Chen TY, Giovannucci E. Cigarette smoking and colorectal cancer
applications to cancer rates. Stat Med 2000;19:335–51. incidence and mortality: systematic review and meta-analysis. Int J Cancer
18 Jemal A, Thun MJ, Ries LA, et al. Annual report to the nation on the status of 2009;124:2406–15.
cancer, 1975–2005, featuring trends in lung cancer, tobacco use, and tobacco 44 Taylor DP, Burt RW, Williams MS, et al. Population-based family history-specific
control. J Natl Cancer Inst 2008;100:1672–94. risks for colorectal cancer: a constellation approach. Gastroenterology
19 Cammà C, Giunta M, Fiorica F, et al. Preoperative radiotherapy for resectable rectal 2010;138:877–85.
cancer: a meta-analysis. JAMA 2000;284:1008–15. 45 Jess T, Rungoe C, Peyrin-Biroulet L. Risk of colorectal cancer in patients with
20 Renehan AG, Egger M, Saunders MP, et al. Impact on survival of intensive follow ulcerative colitis: a meta-analysis of population-based cohort studies. Clin
up after curative resection for colorectal cancer: systematic review and meta-analysis Gastroenterol Hepatol 2012;10:639–45.
of randomised trials. BMJ 2002;324:813. 46 Bosetti C, Rosato V, Gallus S, et al. Aspirin and cancer risk: a quantitative review to
21 McGregor SE, Hilsden RJ, Li FX, et al. Low uptake of colorectal cancer screening 2011. Ann Oncol 2012;23:1403–15.
3 yr after release of national recommendations for screening. Am J Gastroenterol 47 Rothwell PM, Fowkes FG, Belch JF, et al. Effect of daily aspirin on long-term risk of
2007;102:1727–35. death due to cancer: analysis of individual patient data from randomised trials.
22 Atkin WS, Edwards R, Kralj-Hans I, et al. Once-only flexible sigmoidoscopy Lancet 2011;377:31–41.
screening in prevention of colorectal cancer: a multicentre randomised controlled 48 Lin KJ, Cheung WY, Lai JY, et al. The effect of estrogen vs. combined
trial. Lancet 2010;375:1624–33. estrogen-progestogen therapy on the risk of colorectal cancer. Int J Cancer
23 Kuriki K, Tajima K. The increasing incidence of colorectal cancer and the preventive 2012;130:419–30.
strategy in Japan. Asian Pac J Cancer Prev 2006;7:495–501. 49 Ma Y, Zhang P, Wang F, et al. Association between vitamin D and risk of colorectal
24 Levin B, Lieberman DA, McFarland B, et al. Screening and surveillance for the early cancer: a systematic review of prospective studies. J Clin Oncol 2011;29:3775–82.
detection of colorectal cancer and adenomatous polyps, 2008: a joint guideline 50 Kono S, Ahn YO. Vegetables, cereals and colon cancer mortality: long-term trend in
from the American Cancer Society, the US Multi-Society Task Force on Colorectal Japan. Eur J Cancer Prev 2000;9:363–5.
Cancer, and the American College of Radiology. CA Cancer J Clin 2008;58:130–60. 51 Kono S. Secular trend of colon cancer incidence and mortality in relation to fat and
25 Schreuders EH, Ruco A, Rabeneck L, et al. Colorectal cancer screening: a global meat intake in Japan. Eur J Cancer Prev 2004;13:127–32.
overview of existing programmes. Gut 2015;64:1637–49. 52 Popkin BM, Adair LS, Ng SW. Global nutrition transition and the pandemic of
26 van Steenbergen LN, Lemmens VE, Louwman MJ, et al. Increasing incidence and obesity in developing countries. Nutr Rev 2012;70:3–21.
decreasing mortality of colorectal cancer due to marked cohort effects in southern 53 Stevens GA, Singh GM, Lu Y, et al. National, regional, and global trends in adult
Netherlands. Eur J Cancer Prev 2009;18:145–52. overweight and obesity prevalences. Popul Health Metr 2012;10:22.
27 Fedirko V, Tramacere I, Bagnardi V, et al. Alcohol drinking and colorectal cancer 54 Chatenoud L, Bertuccio P, Bosetti C, et al. Trends in cancer mortality in Brazil,
risk: an overall and dose-response meta-analysis of published studies. Ann Oncol 1980–2004. Eur J Cancer Prev 2010;19:79–86.
2011;22:1958–72. 55 Malvezzi M, Bosetti C, Chatenoud L, et al. Trends in cancer mortality in Mexico,
28 Bagnardi V, Blangiardo M, La Vecchia C, et al. A meta-analysis of alcohol drinking 1970–1999. Ann Oncol 2004;15:1712–18.
and cancer risk. Br J Cancer 2001;85:1700–5. 56 CanTreat I. Scaling up cancer diagnosis and treatment in developing countries:
29 Moskal A, Norat T, Ferrari P, et al. Alcohol intake and colorectal cancer risk: what can we learn from the HIV/AIDS epidemic? Ann Oncol 2010;21:680–2.
a dose–response meta-analysis of published cohort studies. Int J Cancer 57 Gatta G, Capocaccia R, Sant M, et al. Understanding variations in survival for
2007;120:664–71. colorectal cancer in Europe: a EUROCARE high resolution study. Gut
30 Huncharek M, Muscat J, Kupelnick B. Colorectal cancer risk and dietary intake of 2000;47:533–8.
calcium, vitamin D, and dairy products: a meta-analysis of 26,335 cases from 60 58 Barton MB, Frommer M, Shafiq J. Role of radiotherapy in cancer control in
observational studies. Nutr Cancer 2009;61:47–69. low-income and middle-income countries. Lancet Oncol 2006;7:584–95.
31 Bouvard V, Loomis D, Guyton KZ, et al. Carcinogenicity of consumption of red and 59 Richards MA. The size of the prize for earlier diagnosis of cancer in England.
processed meat. Lancet Oncol Published Online First: 26 Oct 2015. doi:10.1016/ Br J Cancer 2009;101(Suppl 2):S125–9.
S1470-2045(15)00444-1 60 Brenner H, Kloor M, Pox CP. Colorectal cancer. Lancet 2014;383:1490–502.
32 Park Y, Hunter DJ, Spiegelman D, et al. Dietary fiber intake and risk of colorectal 61 Guren MG, Kørner H, Pfeffer F, et al. Nationwide improvement of rectal cancer
cancer: a pooled analysis of prospective cohort studies. JAMA 2005;294:2849–57. treatment outcomes in Norway, 1993–2010. Acta Oncol 2015;54:1714––22.
33 Asano T, McLeod RS. Dietary fibre for the prevention of colorectal adenomas and 62 Kingham TP, Alatise OI, Vanderpuye V, et al. Treatment of cancer in sub-Saharan
carcinomas. Cochrane Database Syst Rev 2002;(2):CD003430. Africa. Lancet Oncol 2013;14:e158–67.
34 Larsson SC, Wolk A. Meat consumption and risk of colorectal cancer: 63 Goss PE, Lee BL, Badovinac-Crnjevic T, et al. Planning cancer control in Latin
a meta-analysis of prospective studies. Int J Cancer 2006;119:2657–64. America and the Caribbean. Lancet Oncol 2013;14:391–436.
35 Norat T, Lukanova A, Ferrari P, et al. Meat consumption and colorectal cancer risk: 64 Bray F, Jemal A, Torre LA, et al. Long-term realism and cost-effectiveness: primary
dose–response meta-analysis of epidemiological studies. Int J Cancer prevention in combating cancer and associated inequalities worldwide. J Natl
2002;98:241–56. Cancer Inst 2015;107:pii:djv273.

Arnold M, et al. Gut 2016;0:1–9. doi:10.1136/gutjnl-2015-310912 9

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