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Colorectal cancer incidence in 5 Asian countries by subsite: An analysis of Cancer Incidence in Five Continents (1998–2007)
Cancer Epidemiology 45 (2016) 65–70
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Cancer Epidemiology The International Journal of Cancer Epidemiology, Detection, and Prevention journal homepage: www.cancerepidemiology.net
Colorectal cancer incidence in 5 Asian countries by subsite: An analysis of Cancer Incidence in Five Continents (1998–2007) Hye-Min Parka , Hyeongtaek Woob , Sun Jae Jungb,c, Kyu-Won Jungd , Hai-Rim Shine , Aesun Shin, MD, PhDb,f,* a
Department of Applied Biology and Chemistry, College of Agriculture and Life Science, Seoul National University, Seoul, Republic of Korea Department of Preventive Medicine, Seoul National University College of Medicine, Seoul, Republic of Korea Department of Biomedical Science, Seoul National University, Seoul, Republic of Korea d Cancer Registration Branch, National Cancer Control Institute, National Cancer Center, Goyang, Republic of Korea e Noncommunicable Diseases and Health Promotion, Division of NCD and Health through the Life-Course, World Health Organization, Regional Office for the Western Pacific, Manila, Philippines f Cancer Research Institute, Seoul National University, Seoul, Republic of Korea b c
A R T I C L E I N F O
Article history: Received 21 June 2016 Received in revised form 12 September 2016 Accepted 25 September 2016 Available online xxx Keywords: Cancer Incidence Proximal colon Distal colon Rectum
A B S T R A C T
Colorectal cancer is the fourth most common cancer in Asia. However, the trends in colorectal cancer incidence by subsite have not been analyzed across Asian countries. We used the most recent, high quality data from 6 cancer registries for two 5-year periods, 1998–2002 and 2003–2007, from Cancer Incidence in Five Continents to estimate colorectal cancer incidence by subsite in 5 Asian countries. Cases with overlapping lesions or otherwise unspecified colon cancer were re-distributed as proximal or distal colon cancer. Age-standardized incidence rates (ASRs) per 100,000 population and incidence rate ratios from 1998 to 2002 to 2003–2007 were calculated for each subsite. For 2003–2007, men in Miyagi, Japan, had the highest ASR for cancer in the proximal colon, distal colon and rectum. Men of Jewish ancestry in Israel had a high ASR for proximal and distal colon cancer, but the lowest ASR for rectal cancer. The proportion of rectal cancer was highest among Korean men (51.39%) and lowest among Israeli women (26.6%). From 1998–2002 to 2003–2007, rectal cancer incidence did not significantly change in most registries, except for men in Miyagi, Japan, and both sexes in Korea. However, during the same period cancer incidence in the proximal and distal colon increased in most registries. In conclusion, there was substantial variation in subsite distributions of colorectal cancer in Asian registries and increases in overall incidence of colorectal cancer could be attributed to increases in colon cancer. ã 2016 Elsevier Ltd. All rights reserved.
1. Introduction Colorectal cancer is one of the most common cancers in the world, and the fourth most common cancer among both men and women in Asia [1]. Although colorectal cancer incidence has been lower in Asia compared with Western countries, many Asian countries are undergoing a rapid increase in colorectal cancer incidence due to the economic development and westernization
* Corresponding author at: Department of Preventive Medicine, Seoul National University College of Medicine, 103 Daehakno, Jongno-Gu, Seoul, 110-799, Republic of Korea. E-mail addresses: [email protected], http://[email protected] (A. Shin). http://dx.doi.org/10.1016/j.canep.2016.09.012 1877-7821/ã 2016 Elsevier Ltd. All rights reserved.
[2]. In addition, it has been suggested that proximal and distal colon have differential functions, as well as different embryologic and etiological characteristics [3], suggesting differences in epidemiological patterns. Proximal shift, or the increase in the number of cases of proximal colon cancer as a proportion of all colorectal cancer cases over time, has been reported in Western countries [4–6]. In Asia, detailed analyses of colorectal cancer incidence by subsite have been reported for Japan [7,8], Korea [9,10], Singapore [11], and China [12]. However, to our knowledge there have been no analyses of comparing distribution of colorectal cancer incidence by subsite across Asian countries. In this study, we estimated cancer incidence patterns for cancer of the proximal colon, distal colon and rectum and their trends
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Table 1 Estimated age-standardized incidence rates for colorectal cancer subsites among men in 6 Asian registries, 1998–2007 (Cancer Incidence in Five Continents). Country/Registry
Proximal Colon 1998–2002
China Israel Japan Japan Koreab Singapore
Shanghai Jewish ancestry Miyagi Nagasaki National Chinese ancestry
7.84 14.47 16.66 11.37 6.16 10.93
2003–07 8.33 15.19 17.78 12.50 8.60 10.25
Distal Colon IRR
a
(95% CI)
c
1.06 1.05c 1.07c 1.10c 1.40c 0.94c
(1.04–1.08) (1.02–1.08) (1.03–1.11) (1.04–1.16) (1.39–1.40) (0.88–0.99)
1998–2002 7.94 14.76 19.30 15.83 8.06 15.56
Rectum 2003–07 7.66 14.00 20.12 17.26 12.58 15.37
IRR
a c
0.96 0.95c 1.04c 1.09c 1.56c 0.99
(95% CI)
1998–2002
2003–07
IRRa
(95% CI)
(0.95–0.98) (0.92–0.97) (1.00–1.08) (1.03–1.16) (1.55–1.57) (0.93–1.05)
11.24 11.13 22.44 19.50 14.87 17.61
11.56 11.20 24.14 20.45 19.47 18.37
1.03 1.01 1.08c 1.05 1.31c 1.04
(0.97–1.08) (0.94–1.08) (1.02–1.14) (0.97–1.13) (1.28–1.34) (0.96–1.13)
Abbreviations: CI refers to Confidence Internal. IRR refers to Incidence Rate Ratio of the incidence rates in 2003–2007 compared to that in 1998–2002. a Incidence rates are per 100,000 persons and were age-adjusted to the 1960 Segi’s world standard population. b National data for Korea for the first time interval were based on incidence data from 1999 to 2002. c Statistically significant rate ratios are given with the asterisk mark.
across 5 Asian countries during a 10-year period using high quality data from Cancer Incidence in Five Continents (CI5). 2. Materials and methods We obtained colorectal cancer data from IARC’s CI5 databases, which was compiled and provided by International Agency for Research on Cancer (IARC) [13,14]. The CI5 series contains worldwide cancer incidence data from high quality, national- or regional-based sources. The most recent 10 years of data were included in the analysis; these data were published in volume 9 (1998–2002; 1999–2003 for Korea), and volume 10 (2003–2007). Using the codes from the International Statistical Classification of Diseases and Related Health Problems, 10th Revision (ICD-10) [15], the colon was defined as the ceacum, appendix, ascending colon, hepatic flexure, transverse colon, splenic flexure of the colon, descending colon, sigmoid colon, overlapping lesions of the colon and colon not otherwise specified (C18.0-C18.9). The rectum was defined as the recto-sigmoid colon (C19) and rectum (C20). For our analyses, the colon was also divided into the proximal colon (C18.0-C18.5) and distal colon (C18.6-C18.7). Among all IARC Asian registries, the proportion of overlapping or unspecified colon cancer cases (C18.8-C18.9) from among all colon cancer cases (C18.0-C18.9) ranged from 3.4% to 49.1%. For subsite analysis of colon cancer incidence, we included only high quality data; specifically, datasets were included only if they had more than 3000 colorectal cancer cases among men for 2003– 2007 and if fewer than 30% percent of cases were classified as overlapping or unspecified (C18.8-18.9). In addition, when multiples registries including national data were selected, the national registry was chosen as a representative data for the respective country. Six registries from 5 countries met these criteria: people of Jewish ancestry in Israel; Miyagi and Nagasaki of Japan; Korea
(national); people of Chinese ancestry in Singapore; Shanghai of China. Cases with overlapping or unspecified colon cancer were redistributed into proximal and distal colon cases, using the proportion of proximal and distal colon cancer in each registry. Age-standardized incidence rates (ASRs) for incidence per 100,000 people were calculated by using a direct method with Segi’s 1960 world standard population [16]. Incidence rate ratios (IRR) and their 95% confidence intervals (CI) for 2003–2007 to 1998–2002 were calculated for each subsite for all registries [16]. SAS version 9.4 (SAS Institute, Cary, NC) was used for statistical analysis. 3. Results The total number of 93,333 (50,889 for men and 42,444 for women) cases for 1998–2002, 147,494(83,230 for men and 64,264 for women) cases for 2003–2007 was used in our analysis. Further information of cases were shown in supplement Tables 1 and 2 by sex, by registry and by subsite. Variances in cancer incidence rates between registries were observed for both men (Table 1) and women (Table 2). Overall, populations in Japan and Israel had the highest incidence rates for cancers of the proximal colon and distal colon, whereas populations in Israel and China had relatively lower incidence rates for rectal cancer. The variation was more distinct for cancers of the proximal and distal colon compared with rectal cancer. In 2003–2007, men in Miyagi, Japan recorded the highest cancer incidence rate for the proximal colon among men (17.78/100,000), distal colon (20.12/100,000), as well as the rectum (24.14/100,000). These rates were about twice as high compared with men in lowerrate countries. Men in Shanghai, China had the lowest cancer incidence rates for the proximal colon (8.33/100,000) and distal colon (7.66/100,000), whereas Jewish men in Israel had the lowest
Table 2 Estimated age-standardized incidence rates for colorectal cancer subsites among women in 6 Asian registries, 1998–2007 (Cancer Incidence in Five Continents). Country/Registry
Proximal Colon 1998–2002
China Israel Japan Japan Koreab Singapore
Shanghai Jewish ancestry Miyagi Nagasaki National Chinese ancestry
8.57 12.67 12.30 8.79 4.52 9.66
2003–07 8.35 11.97 13.61 10.17 6.12 8.95
Distal Colon a
IRR
(95% CI) c
0.97 0.94c 1.11* 1.16c 1.35c 0.93c
(0.96–0.99) (0.93–0.96) (1.07–1.14) (1.10–1.21) (1.35–1.36) (0.88–0.97)
1998–2002 6.05 11.96 9.16 8.34 4.29 11.08
Rectum 2003–07 6.41 10.95 10.41 9.50 6.32 11.71
IRR
a c
1.06 0.92c 1.14c 1.14c 1.47c 1.06c
(95% CI)
1998–2002
2003–07
IRRa
(95% CI)
(1.04–1.08) (0.89–0.94) (1.09–1.18) (1.08–1.20) (1.47–1.48) (1.01–1.11)
8.30 8.18 10.92 10.01 8.56 9.54
8.30 7.88 11.31 9.70 10.24 10.39
1.00 0.96 1.04 0.97 1.20c 1.09
(0.94–1.06) (0.89–1.04) (0.95–1.12) (0.87–1.08) (1.17–1.23) (0.99–1.20)
Abbreviations: CI refers to Confidence Internal. IRR refers to Incidence Rate Ratio of the incidence rates in 2003–2007 compared to that in 1998–2002. a Incidence rates are per 100,000 persons and were age-adjusted to the 1960 Segi’s world standard population. b National data for Korea for the first time interval were based on incidence data from1999-2002. c Statistically significant rate ratios are given with the asterisk mark.
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rectal cancer incidence (11.20/100,000) during the same period. Although there was variation between registries, overall women had lower incidence rates than men in most registries, except for Shanghai. From 1998–2002 to 2003–2007, increases in ASRs incidence rates for all subsites were observed in 5 registries for men and 3 registries for women for the proximal colon, and 3 registries for men and 5 registries for women for the distal colon. In particular, Korea had the largest increase for both sexes. Men in Korea had a 40% increase for the proximal colon, a 56% increase for the distal colon, and a 31% increase for rectal cancer between the two 5-year periods (Table 1). Women in Korea also had an increasing pattern for all subsites, ranging from a 20% increase for rectal cancer to a 47% increase for cancer of the distal colon (Table 2). People in Miyagi and Nagasaki Japan also had an increase in colon cancer, ranging from 10% to 16% for the proximal colon and from 9% to 14% for the distal colon. Two Japanese registries recorded an increasing trend for colon cancer, although the increase did not exceed 10%. For rectal cancer, only men in Miyagi had a slight increase, whereas for both sexes in Nagasaki and for women in Miyagi there were no statistically significant changes. Most of other registries showed statistically significant changes in proximal and distal colon cancer incidence from 1998 to 2002 to 2003–2007, but there were no statistically significant changes in rectal cancer incidence rates. In Shanghai, proximal colon cancer incidence rate increased among men and decreased among women. On the contrary, the distal colon cancer incidence rate decreased among men and increased among women. Proximal colon cancer incidence rates increased among Jewish men in Israel, but distal colon cancer rates decreased. For Jewish women in Israel, both proximal and distal colon rates decreased. Among Chinese in Singapore, proximal colon cancer rates decreased among both men and women; distal colon cancer rates increased only among women.
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Of all colorectal cancer subsites, the highest proportion of rectal cancer was found in Korea (51.4% among men [Fig. 1] and 44.8% among women for 2003–2007 [Fig. 2]), whereas the lowest proportion of rectal cancer was found in Israel (29.4% among men, 26.6% among women). The proportions of proximal colon cancer were higher among women compared with men in all 6 registries. Specifically, the proportion of women in Miyagi and Nagasaki, Japan with proximal colon cancer was more than 10% higher compared with men in those locations in 2003–2007 (women: 44.0% in Miyagi and 40.6% in Nagasaki; men: 30.6% in Miyagi and 27.5% in Nagasaki). 4. Discussion Colorectal cancer incidence rates vary in Asian countries by subsite and by sex. The highest ASRs for cancer in the proximal colon were found among Jewish men in Israel and men in Miyagi, Japan. For cancer in the distal colon and rectum, the highest ASRs were found among men in Miyagi and Nagasaki, Japan. For the 6 registries included in this analysis, 5 registries showed increases in the incidence of proximal colon cancer and 3 registries showed increases in distal colon cancer among men between 1998 and 2002 and 2003–2007. Among women, 3 registries showed increases the incidence of proximal colon cancer and 5 showed increases in distal colon cancer. For rectal cancer, incidence rates were stable in most countries, except for Korea, where statistically significant increases were found for both men and women. The distribution of colorectal cancer cases by subsite also varied across the registries. Of note, the proportion of rectal cancer among Korean men and the proportion of proximal colon cancer among women in Miyagi, Japan were especially high. Variations between registries, along with the overall pattern of increasing colorectal cancer incidence, were found in Asian the countries included in our analyses. Economic development is known to be related to changes in risk factors for colorectal cancer
Fig. 1. Estimated proportion of colorectal cancer subsites among men in 6 Asian registries, 1998–2007 (Cancer Incidence in Five Continents).
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Fig. 2. Estimated proportion of colorectal cancer subsites among women in 6 Asian registries, 1998–2007 (Cancer Incidence in Five Continents).
[17], which correspond to variances in colorectal cancer incidence across European countries [18]. Japanese migrants to the United States have been shown to have higher colorectal cancer incidence than people residing in Japan, suggesting that environmental exposures are a main contributor to colorectal cancer risk [19]. These risk factors include obesity [20], westernized food consumption such as intakes of red meat and processed foods [21] low levels of intake of fruits dietary fiber [22], heavy alcohol consumption [23], and sedentary lifestyle with reduced physical activity [24]. Indeed, a change toward Westernized food consumption has been reported across a number of Asian countries, including Japan, Singapore, Korea, and China [25–28]. Introduction of cancer screening programs is another explanation for the observed changes in cancer incidence rates. In Japan, the immunochemical fecal occult blood test has been recommended starting in 1983 and was incorporated into a national colorectal cancer program in 1992 for people aged 40 years and older [29]. In Miyagi prefecture, the rate of participation in colorectal cancer screenings increased from 20% in 1997, to 33.8% in 2007, and to 47.6% in 2013[30,31]. In Nagasaki prefecture, the screening rate was 20.7% in 2007 and 32.3% in 2013 [30]. Screening rates for Japan overall were 25.8% in 2007 and 37.9% in 2013. Israel began what has become one of the best established colorectal cancer screening programs using the fecal occult blood test from 1993 [32]. For people aged 50–75 years, a home-based test administered by primary care physicians is provided; 44.5% of detected cancers were categorized as Dukes’ A [33]. Korea began a National Cancer Screening Program in 2004, which covers colorectal cancer using the fecal occult blood test. It is provided free of charge as a primary modality for people aged 50 years or older [34]. According to the Korean National Cancer Screening Survey, the colorectal cancer screening rate observing recommended national screening protocol was 19.5% in 2004; the rate
had increased to 55.6% in 2013 [35]. In Singapore, no screening program for colorectal cancer is available at the general population level yet, but participation in colorectal cancer screening is relatively high (77.2%) on account of a strong recommendation by the nation’s Clinical Practice Guidelines [36]. There is a lack of detailed information available on colorectal cancer screening in Shanghai. In China, cancer screening quality has also been improved reporting Dukes’ B has greatly increased and is prevalent among all reported cases [37]. There is substantial variation in trends of colorectal cancer incidence among registries within Japan. Our data of Miyagi and Nagasaki registries had the highest ASR for colorectal cancer among all 6 selected registries, and comparably high IRR rates. However, ASRs for colorectal cancer in Osaka, Japan, have been reported to be almost half of those reported for Miyagi [38]. In addition, colorectal cancer incidence in Osaka has been decreasing since 1997 for both sexes [38]. Though controversial, the proximal shift was first reported in Western population. In Asia, this phenomenon has been well reported in Japan both in reports of newly developed adenoma [39,40] and in cancer incidence rates from the Osaka registry [8]. In Shanghai, this phenomenon was not observed between 1972 and 1994 [41]; however, a significant increase in proximal colon cancer as a proportion of total colorectal cancer was also found during the 20 year period 1980–1999 in data from 25 hospitals in 11 geographic areas of China[37]. In Korea, the proximal shift in colorectal cancer has not been clearly observed [9,10], although the proportion of adenomatous polyps in the proximal colon greatly increased between 1996 and 2005 [42]. In a study in Singapore for the 25-year period 1968–1992, the proximal shift was not observed [11]. Whereas the proportion of rectal cancer was 28% between 2006 and 2010 in the United States [45], the proportion was 28–
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84% in Asian registries and 26–52% in European registries [14]. Differences in lifestyle risk factors could partially explain the large variation in the proportion of rectal cancer incidence that we observed between registries (more than 45% in Korea and less than 30% in Israel). In Japan and China, decreases in the proportion of rectal cancer cases has been reported over a long-term period [7,37]. When considering these decreases in Japan and China and the rapid switch to a Westernized lifestyle in Korea, the proportion of rectal cancer in Korea may continue to decrease. Another possible reason for the observed subsite variation is aging. In Japan, the proximal shift of colorectal cancer has been reported only among people aged 70 years or older [7]. In addition, the percentage of proximal colon adenoma has been observed to be gradually increase among people aged less than 50 years to people aged 80 years and older [39]. Risk factors may have differential effect on subsites of colorectum. In a Korean study, high body mass index (BMI) was related to distal colon cancer among men; however, BMI was more strongly related to proximal colon cancer among women [43]. A Japanese study has shown that Japanesestyle foods, such as rice or pickled vegetables, have a more protective influence on the proximal colon than the distal colon [44]. Meanwhile, the rectum is more susceptible to the negative effects of habitual smoking and binge alcohol drinking than is the colon [43,44]. The strengths of this article include the use of the high quality data from CI5 for several registries in Asia, which enabled a cancer subsite analysis. In addition, we tried to improve the comparability of the incidence rates for subsites by re-distributing unspecified or overlapping lesions to the proximal or distal colon. The limitations of this study include its coverage of a relatively short time period (10 years) for colorectal cancer incidence. Due to the high percentage of overlapping or unspecified lesions in most Asian registries, we could not extend the analysis to other registries or earlier time periods. To properly demonstrate the sophisticated patterns of colorectal cancer incidence by subsite, it is essential to analyze data for longer periods of time, i.e., 20 years or more. However, the varied quality of data available across registries limits comprehensive analysis over long periods of time. For example, in CI5 vol 8 (1992–1996) only three registries showed the percentage of overlapping and unspecified lesions of the colon (C18.8-9) less than 30%. However, 8 of 15 Asian countries had incidence rates of over 40% for overlapping or unspecified lesions among men [13]. Considering the high reported percentage of overlapping or unspecified lesions in earlier volumes of CI5 in Asian countries, the analysis of subsite-based colorectal cancer incidence in Asia remains difficult. Another limitation is that the registries included in our analysis may not represent for the whole country. Especially colorectal cancer incidence in Shanghai in China and Miyagi and Nagasaki in Japan is one of the highest in the respective countries [14]. 5. Conclusion In China, Israel, Japan, Korea, and Singapore, colorectal cancer incidence varied across countries by sex and by subsite. Miyagi prefecture in Japan had the highest ASRs for men regardless of the subsite, whereas Shanghai, China, recorded the lowest ASRs. Between 1998–2002 and 2003–2007, incidence of proximal and distal colon cancer increased in most registries, especially in Korea and Japan, but rectal cancer incidence was stable in most registries. The proportion of rectal cancer also varied between countries; it was highest in Korea and lowest in Israel. The increases in overall incidence of colorectal cancer can be attributed to increases in colon cancer incidence in Asian registries and may be due to the adoption of a Westernized life style and the expansion of cancer screening program.
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Author contributions HMP, HW, and SJJ conducted analyses. HMJ conducted literature review and wrote the first draft of the manuscript, and prepared the tables and figures. AS conceived study design and supervise data collection, analysis, and manuscript writing. KWJ and HRS contributed critical revision of data analysis. All authors reviewed and approved the final version of the manuscript. Acknowledgements This research was funded by the National Research Foundation of Korea (2013R1A1A2A10008260). The authors have no conflicts of interest. The manuscript was edited for clarity, consistency, and English-language usage by Bethanie Rammer, a professional medical editor. Appendix A. Supplementary data Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/j. canep.2016.09.012. References [1] J. Ferlay, I. Soerjomataram, M. Ervik, R. Dikshit, S. Eser, C. Mathers, M. Rebelo, D. Parkin, D. Forman, F. Bray, GLOBOCAN 2012 v1.0, Cancer Incidence and Mortality Worldwide: IARC CancerBase No. 11 [Internet], (2013) . (accessed 24.03) http://globocan.iarc.fr/. [2] J.J. Sung, J.Y. Lau, K.L. Goh, W.K.C. Leung, Asia Pacific Working Group on Colorectal, Increasing incidence of colorectal cancer in Asia: implications for screening, Lancet Oncol. 6 (11) (2005) 871–876. [3] P. Gervaz, P. Bucher, P. Morel, Two colons-two cancers: paradigm shift and clinical implications, J. Surg. Oncol. 88 (4) (2004) 261–266. [4] X.C. Wu, V.W. Chen, B. Steele, B. Ruiz, J. Fulton, L. Liu, S.E. Carozza, R. Greenlee, Subsite-specific incidence rate and stage of disease in colorectal cancer by race, gender, and age group in the United States 1992–1997, Cancer 92 (10) (2001) 2547–2554. [5] A. Miller, M. Gorska, M. Bassett, Proximal shift of colorectal cancer in the Australian Capital Territory over 20 years, Aust. N. Z. J. Med. 30 (2) (2000) 221– 225. [6] E. Svensson, T. Grotmol, G. Hoff, F. Langmark, J. Norstein, S. Tretli, Trends in colorectal cancer incidence in Norway by gender and anatomic site: an ageperiod-cohort analysis, Eur. J. Cancer Prev. 11 (5) (2002) 489–495. [7] H. Takada, T. Ohsawa, S. Iwamoto, R. Yoshida, M. Nakano, S. Imada, K. Yoshioka, M. Okuno, Y. Masuya, K. Hasegawa, N. Kamano, K. Hioki, T. Muto, Y. Koyama, Changing site distribution of colorectal cancer in Japan, Dis. Colon Rectum 45 (9) (2002) 1249–1254. [8] Y. Toyoda, T. Nakayama, Y. Ito, A. Ioka, H. Tsukuma, Trends in colorectal cancer incidence by subsite in Osaka, Japan, Jpn. J. Clin. Oncol. 39 (3) (2009) 189–191. [9] A. Shin, K.Z. Kim, K.W. Jung, S. Park, Y.J. Won, J. Kim, D.Y. Kim, J.H. Oh, Increasing trend of colorectal cancer incidence in Korea 1999–2009, Cancer Res. Treat. 44 (4) (2012) 219–226. [10] D.H. Kim, M.H. Shin, Y.O. Ahn, Incidence pattern of colorectal cancer in Korea by subsite of origin, J. Korean Med. Sci. 15 (6) (2000) 675–681. [11] J. Huang, A. Seow, C.Y. Shi, H.P. Lee, Colorectal carcinoma among ethnic Chinese in Singapore: trends in incidence rate by anatomic subsite from 1968 to 1992, Cancer 85 (12) (1999) 2519–2525. [12] B.T. Ji, S.S. Devesa, W.H. Chow, F. Jin, Y.T. Gao, Colorectal cancer incidence trends by subsite in urban Shanghai, 1972–1994, Cancer Epidemiol. Biomarkers Prev. 7 (8) (1998) 661–666. [13] M.P. Curado, B. Edwards, H.R. Shin, H. Storm, J. Ferlay, M. Heanue, P. Boyle (Eds.), Cancer Incidence in Five Continents, Vol. IX, IARC Scientific Publications, Lyon, IARC, 2007 (No. 160). [14] D. Forman, F. Bray, D.H. Brewster, M. Gombe, C.B. Kohler, M. Piñeros, E. Steliarova-Foucher, R. Swaminathan, J. Ferlay (Eds.), Cancer Incidence in Five Continents, Vol. X, IARC Scientific Publication, Lyon: International Agency for Research on Cancer, 2014 (No. 164). [15] World Health Organization, International Statistical Classification of Diseases and Related Health Problems. 10th Rev, (1994) . [16] P. Boyle, D.M. Parkin, Cancer Registration: Principles and Methods. Statistical Methods for Registries, 95, IARC scientific publications, 1991, pp. 126–158. [17] A. Drewnowski, B.M. Popkin, The Nutrition Transition: New Trends in the Global Diet, (1997) . [18] M.M. Center, A. Jemal, E. Ward, International trends in colorectal cancer incidence rates, Cancer Epidemiol. Biomarkers Prev. 18 (6) (2009) 1688–1694.
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Cancer Epidemiology The International Journal of Cancer Epidemiology, Detection, and Prevention journal homepage: www.cancerepidemiology.net
Colorectal cancer incidence in 5 Asian countries by subsite: An analysis of Cancer Incidence in Five Continents (1998–2007) Hye-Min Parka , Hyeongtaek Woob , Sun Jae Jungb,c, Kyu-Won Jungd , Hai-Rim Shine , Aesun Shin, MD, PhDb,f,* a
Department of Applied Biology and Chemistry, College of Agriculture and Life Science, Seoul National University, Seoul, Republic of Korea Department of Preventive Medicine, Seoul National University College of Medicine, Seoul, Republic of Korea Department of Biomedical Science, Seoul National University, Seoul, Republic of Korea d Cancer Registration Branch, National Cancer Control Institute, National Cancer Center, Goyang, Republic of Korea e Noncommunicable Diseases and Health Promotion, Division of NCD and Health through the Life-Course, World Health Organization, Regional Office for the Western Pacific, Manila, Philippines f Cancer Research Institute, Seoul National University, Seoul, Republic of Korea b c
A R T I C L E I N F O
Article history: Received 21 June 2016 Received in revised form 12 September 2016 Accepted 25 September 2016 Available online xxx Keywords: Cancer Incidence Proximal colon Distal colon Rectum
A B S T R A C T
Colorectal cancer is the fourth most common cancer in Asia. However, the trends in colorectal cancer incidence by subsite have not been analyzed across Asian countries. We used the most recent, high quality data from 6 cancer registries for two 5-year periods, 1998–2002 and 2003–2007, from Cancer Incidence in Five Continents to estimate colorectal cancer incidence by subsite in 5 Asian countries. Cases with overlapping lesions or otherwise unspecified colon cancer were re-distributed as proximal or distal colon cancer. Age-standardized incidence rates (ASRs) per 100,000 population and incidence rate ratios from 1998 to 2002 to 2003–2007 were calculated for each subsite. For 2003–2007, men in Miyagi, Japan, had the highest ASR for cancer in the proximal colon, distal colon and rectum. Men of Jewish ancestry in Israel had a high ASR for proximal and distal colon cancer, but the lowest ASR for rectal cancer. The proportion of rectal cancer was highest among Korean men (51.39%) and lowest among Israeli women (26.6%). From 1998–2002 to 2003–2007, rectal cancer incidence did not significantly change in most registries, except for men in Miyagi, Japan, and both sexes in Korea. However, during the same period cancer incidence in the proximal and distal colon increased in most registries. In conclusion, there was substantial variation in subsite distributions of colorectal cancer in Asian registries and increases in overall incidence of colorectal cancer could be attributed to increases in colon cancer. ã 2016 Elsevier Ltd. All rights reserved.
1. Introduction Colorectal cancer is one of the most common cancers in the world, and the fourth most common cancer among both men and women in Asia [1]. Although colorectal cancer incidence has been lower in Asia compared with Western countries, many Asian countries are undergoing a rapid increase in colorectal cancer incidence due to the economic development and westernization
* Corresponding author at: Department of Preventive Medicine, Seoul National University College of Medicine, 103 Daehakno, Jongno-Gu, Seoul, 110-799, Republic of Korea. E-mail addresses: [email protected], http://[email protected] (A. Shin). http://dx.doi.org/10.1016/j.canep.2016.09.012 1877-7821/ã 2016 Elsevier Ltd. All rights reserved.
[2]. In addition, it has been suggested that proximal and distal colon have differential functions, as well as different embryologic and etiological characteristics [3], suggesting differences in epidemiological patterns. Proximal shift, or the increase in the number of cases of proximal colon cancer as a proportion of all colorectal cancer cases over time, has been reported in Western countries [4–6]. In Asia, detailed analyses of colorectal cancer incidence by subsite have been reported for Japan [7,8], Korea [9,10], Singapore [11], and China [12]. However, to our knowledge there have been no analyses of comparing distribution of colorectal cancer incidence by subsite across Asian countries. In this study, we estimated cancer incidence patterns for cancer of the proximal colon, distal colon and rectum and their trends
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Table 1 Estimated age-standardized incidence rates for colorectal cancer subsites among men in 6 Asian registries, 1998–2007 (Cancer Incidence in Five Continents). Country/Registry
Proximal Colon 1998–2002
China Israel Japan Japan Koreab Singapore
Shanghai Jewish ancestry Miyagi Nagasaki National Chinese ancestry
7.84 14.47 16.66 11.37 6.16 10.93
2003–07 8.33 15.19 17.78 12.50 8.60 10.25
Distal Colon IRR
a
(95% CI)
c
1.06 1.05c 1.07c 1.10c 1.40c 0.94c
(1.04–1.08) (1.02–1.08) (1.03–1.11) (1.04–1.16) (1.39–1.40) (0.88–0.99)
1998–2002 7.94 14.76 19.30 15.83 8.06 15.56
Rectum 2003–07 7.66 14.00 20.12 17.26 12.58 15.37
IRR
a c
0.96 0.95c 1.04c 1.09c 1.56c 0.99
(95% CI)
1998–2002
2003–07
IRRa
(95% CI)
(0.95–0.98) (0.92–0.97) (1.00–1.08) (1.03–1.16) (1.55–1.57) (0.93–1.05)
11.24 11.13 22.44 19.50 14.87 17.61
11.56 11.20 24.14 20.45 19.47 18.37
1.03 1.01 1.08c 1.05 1.31c 1.04
(0.97–1.08) (0.94–1.08) (1.02–1.14) (0.97–1.13) (1.28–1.34) (0.96–1.13)
Abbreviations: CI refers to Confidence Internal. IRR refers to Incidence Rate Ratio of the incidence rates in 2003–2007 compared to that in 1998–2002. a Incidence rates are per 100,000 persons and were age-adjusted to the 1960 Segi’s world standard population. b National data for Korea for the first time interval were based on incidence data from 1999 to 2002. c Statistically significant rate ratios are given with the asterisk mark.
across 5 Asian countries during a 10-year period using high quality data from Cancer Incidence in Five Continents (CI5). 2. Materials and methods We obtained colorectal cancer data from IARC’s CI5 databases, which was compiled and provided by International Agency for Research on Cancer (IARC) [13,14]. The CI5 series contains worldwide cancer incidence data from high quality, national- or regional-based sources. The most recent 10 years of data were included in the analysis; these data were published in volume 9 (1998–2002; 1999–2003 for Korea), and volume 10 (2003–2007). Using the codes from the International Statistical Classification of Diseases and Related Health Problems, 10th Revision (ICD-10) [15], the colon was defined as the ceacum, appendix, ascending colon, hepatic flexure, transverse colon, splenic flexure of the colon, descending colon, sigmoid colon, overlapping lesions of the colon and colon not otherwise specified (C18.0-C18.9). The rectum was defined as the recto-sigmoid colon (C19) and rectum (C20). For our analyses, the colon was also divided into the proximal colon (C18.0-C18.5) and distal colon (C18.6-C18.7). Among all IARC Asian registries, the proportion of overlapping or unspecified colon cancer cases (C18.8-C18.9) from among all colon cancer cases (C18.0-C18.9) ranged from 3.4% to 49.1%. For subsite analysis of colon cancer incidence, we included only high quality data; specifically, datasets were included only if they had more than 3000 colorectal cancer cases among men for 2003– 2007 and if fewer than 30% percent of cases were classified as overlapping or unspecified (C18.8-18.9). In addition, when multiples registries including national data were selected, the national registry was chosen as a representative data for the respective country. Six registries from 5 countries met these criteria: people of Jewish ancestry in Israel; Miyagi and Nagasaki of Japan; Korea
(national); people of Chinese ancestry in Singapore; Shanghai of China. Cases with overlapping or unspecified colon cancer were redistributed into proximal and distal colon cases, using the proportion of proximal and distal colon cancer in each registry. Age-standardized incidence rates (ASRs) for incidence per 100,000 people were calculated by using a direct method with Segi’s 1960 world standard population [16]. Incidence rate ratios (IRR) and their 95% confidence intervals (CI) for 2003–2007 to 1998–2002 were calculated for each subsite for all registries [16]. SAS version 9.4 (SAS Institute, Cary, NC) was used for statistical analysis. 3. Results The total number of 93,333 (50,889 for men and 42,444 for women) cases for 1998–2002, 147,494(83,230 for men and 64,264 for women) cases for 2003–2007 was used in our analysis. Further information of cases were shown in supplement Tables 1 and 2 by sex, by registry and by subsite. Variances in cancer incidence rates between registries were observed for both men (Table 1) and women (Table 2). Overall, populations in Japan and Israel had the highest incidence rates for cancers of the proximal colon and distal colon, whereas populations in Israel and China had relatively lower incidence rates for rectal cancer. The variation was more distinct for cancers of the proximal and distal colon compared with rectal cancer. In 2003–2007, men in Miyagi, Japan recorded the highest cancer incidence rate for the proximal colon among men (17.78/100,000), distal colon (20.12/100,000), as well as the rectum (24.14/100,000). These rates were about twice as high compared with men in lowerrate countries. Men in Shanghai, China had the lowest cancer incidence rates for the proximal colon (8.33/100,000) and distal colon (7.66/100,000), whereas Jewish men in Israel had the lowest
Table 2 Estimated age-standardized incidence rates for colorectal cancer subsites among women in 6 Asian registries, 1998–2007 (Cancer Incidence in Five Continents). Country/Registry
Proximal Colon 1998–2002
China Israel Japan Japan Koreab Singapore
Shanghai Jewish ancestry Miyagi Nagasaki National Chinese ancestry
8.57 12.67 12.30 8.79 4.52 9.66
2003–07 8.35 11.97 13.61 10.17 6.12 8.95
Distal Colon a
IRR
(95% CI) c
0.97 0.94c 1.11* 1.16c 1.35c 0.93c
(0.96–0.99) (0.93–0.96) (1.07–1.14) (1.10–1.21) (1.35–1.36) (0.88–0.97)
1998–2002 6.05 11.96 9.16 8.34 4.29 11.08
Rectum 2003–07 6.41 10.95 10.41 9.50 6.32 11.71
IRR
a c
1.06 0.92c 1.14c 1.14c 1.47c 1.06c
(95% CI)
1998–2002
2003–07
IRRa
(95% CI)
(1.04–1.08) (0.89–0.94) (1.09–1.18) (1.08–1.20) (1.47–1.48) (1.01–1.11)
8.30 8.18 10.92 10.01 8.56 9.54
8.30 7.88 11.31 9.70 10.24 10.39
1.00 0.96 1.04 0.97 1.20c 1.09
(0.94–1.06) (0.89–1.04) (0.95–1.12) (0.87–1.08) (1.17–1.23) (0.99–1.20)
Abbreviations: CI refers to Confidence Internal. IRR refers to Incidence Rate Ratio of the incidence rates in 2003–2007 compared to that in 1998–2002. a Incidence rates are per 100,000 persons and were age-adjusted to the 1960 Segi’s world standard population. b National data for Korea for the first time interval were based on incidence data from1999-2002. c Statistically significant rate ratios are given with the asterisk mark.
H.-M. Park et al. / Cancer Epidemiology 45 (2016) 65–70
rectal cancer incidence (11.20/100,000) during the same period. Although there was variation between registries, overall women had lower incidence rates than men in most registries, except for Shanghai. From 1998–2002 to 2003–2007, increases in ASRs incidence rates for all subsites were observed in 5 registries for men and 3 registries for women for the proximal colon, and 3 registries for men and 5 registries for women for the distal colon. In particular, Korea had the largest increase for both sexes. Men in Korea had a 40% increase for the proximal colon, a 56% increase for the distal colon, and a 31% increase for rectal cancer between the two 5-year periods (Table 1). Women in Korea also had an increasing pattern for all subsites, ranging from a 20% increase for rectal cancer to a 47% increase for cancer of the distal colon (Table 2). People in Miyagi and Nagasaki Japan also had an increase in colon cancer, ranging from 10% to 16% for the proximal colon and from 9% to 14% for the distal colon. Two Japanese registries recorded an increasing trend for colon cancer, although the increase did not exceed 10%. For rectal cancer, only men in Miyagi had a slight increase, whereas for both sexes in Nagasaki and for women in Miyagi there were no statistically significant changes. Most of other registries showed statistically significant changes in proximal and distal colon cancer incidence from 1998 to 2002 to 2003–2007, but there were no statistically significant changes in rectal cancer incidence rates. In Shanghai, proximal colon cancer incidence rate increased among men and decreased among women. On the contrary, the distal colon cancer incidence rate decreased among men and increased among women. Proximal colon cancer incidence rates increased among Jewish men in Israel, but distal colon cancer rates decreased. For Jewish women in Israel, both proximal and distal colon rates decreased. Among Chinese in Singapore, proximal colon cancer rates decreased among both men and women; distal colon cancer rates increased only among women.
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Of all colorectal cancer subsites, the highest proportion of rectal cancer was found in Korea (51.4% among men [Fig. 1] and 44.8% among women for 2003–2007 [Fig. 2]), whereas the lowest proportion of rectal cancer was found in Israel (29.4% among men, 26.6% among women). The proportions of proximal colon cancer were higher among women compared with men in all 6 registries. Specifically, the proportion of women in Miyagi and Nagasaki, Japan with proximal colon cancer was more than 10% higher compared with men in those locations in 2003–2007 (women: 44.0% in Miyagi and 40.6% in Nagasaki; men: 30.6% in Miyagi and 27.5% in Nagasaki). 4. Discussion Colorectal cancer incidence rates vary in Asian countries by subsite and by sex. The highest ASRs for cancer in the proximal colon were found among Jewish men in Israel and men in Miyagi, Japan. For cancer in the distal colon and rectum, the highest ASRs were found among men in Miyagi and Nagasaki, Japan. For the 6 registries included in this analysis, 5 registries showed increases in the incidence of proximal colon cancer and 3 registries showed increases in distal colon cancer among men between 1998 and 2002 and 2003–2007. Among women, 3 registries showed increases the incidence of proximal colon cancer and 5 showed increases in distal colon cancer. For rectal cancer, incidence rates were stable in most countries, except for Korea, where statistically significant increases were found for both men and women. The distribution of colorectal cancer cases by subsite also varied across the registries. Of note, the proportion of rectal cancer among Korean men and the proportion of proximal colon cancer among women in Miyagi, Japan were especially high. Variations between registries, along with the overall pattern of increasing colorectal cancer incidence, were found in Asian the countries included in our analyses. Economic development is known to be related to changes in risk factors for colorectal cancer
Fig. 1. Estimated proportion of colorectal cancer subsites among men in 6 Asian registries, 1998–2007 (Cancer Incidence in Five Continents).
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Fig. 2. Estimated proportion of colorectal cancer subsites among women in 6 Asian registries, 1998–2007 (Cancer Incidence in Five Continents).
[17], which correspond to variances in colorectal cancer incidence across European countries [18]. Japanese migrants to the United States have been shown to have higher colorectal cancer incidence than people residing in Japan, suggesting that environmental exposures are a main contributor to colorectal cancer risk [19]. These risk factors include obesity [20], westernized food consumption such as intakes of red meat and processed foods [21] low levels of intake of fruits dietary fiber [22], heavy alcohol consumption [23], and sedentary lifestyle with reduced physical activity [24]. Indeed, a change toward Westernized food consumption has been reported across a number of Asian countries, including Japan, Singapore, Korea, and China [25–28]. Introduction of cancer screening programs is another explanation for the observed changes in cancer incidence rates. In Japan, the immunochemical fecal occult blood test has been recommended starting in 1983 and was incorporated into a national colorectal cancer program in 1992 for people aged 40 years and older [29]. In Miyagi prefecture, the rate of participation in colorectal cancer screenings increased from 20% in 1997, to 33.8% in 2007, and to 47.6% in 2013[30,31]. In Nagasaki prefecture, the screening rate was 20.7% in 2007 and 32.3% in 2013 [30]. Screening rates for Japan overall were 25.8% in 2007 and 37.9% in 2013. Israel began what has become one of the best established colorectal cancer screening programs using the fecal occult blood test from 1993 [32]. For people aged 50–75 years, a home-based test administered by primary care physicians is provided; 44.5% of detected cancers were categorized as Dukes’ A [33]. Korea began a National Cancer Screening Program in 2004, which covers colorectal cancer using the fecal occult blood test. It is provided free of charge as a primary modality for people aged 50 years or older [34]. According to the Korean National Cancer Screening Survey, the colorectal cancer screening rate observing recommended national screening protocol was 19.5% in 2004; the rate
had increased to 55.6% in 2013 [35]. In Singapore, no screening program for colorectal cancer is available at the general population level yet, but participation in colorectal cancer screening is relatively high (77.2%) on account of a strong recommendation by the nation’s Clinical Practice Guidelines [36]. There is a lack of detailed information available on colorectal cancer screening in Shanghai. In China, cancer screening quality has also been improved reporting Dukes’ B has greatly increased and is prevalent among all reported cases [37]. There is substantial variation in trends of colorectal cancer incidence among registries within Japan. Our data of Miyagi and Nagasaki registries had the highest ASR for colorectal cancer among all 6 selected registries, and comparably high IRR rates. However, ASRs for colorectal cancer in Osaka, Japan, have been reported to be almost half of those reported for Miyagi [38]. In addition, colorectal cancer incidence in Osaka has been decreasing since 1997 for both sexes [38]. Though controversial, the proximal shift was first reported in Western population. In Asia, this phenomenon has been well reported in Japan both in reports of newly developed adenoma [39,40] and in cancer incidence rates from the Osaka registry [8]. In Shanghai, this phenomenon was not observed between 1972 and 1994 [41]; however, a significant increase in proximal colon cancer as a proportion of total colorectal cancer was also found during the 20 year period 1980–1999 in data from 25 hospitals in 11 geographic areas of China[37]. In Korea, the proximal shift in colorectal cancer has not been clearly observed [9,10], although the proportion of adenomatous polyps in the proximal colon greatly increased between 1996 and 2005 [42]. In a study in Singapore for the 25-year period 1968–1992, the proximal shift was not observed [11]. Whereas the proportion of rectal cancer was 28% between 2006 and 2010 in the United States [45], the proportion was 28–
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84% in Asian registries and 26–52% in European registries [14]. Differences in lifestyle risk factors could partially explain the large variation in the proportion of rectal cancer incidence that we observed between registries (more than 45% in Korea and less than 30% in Israel). In Japan and China, decreases in the proportion of rectal cancer cases has been reported over a long-term period [7,37]. When considering these decreases in Japan and China and the rapid switch to a Westernized lifestyle in Korea, the proportion of rectal cancer in Korea may continue to decrease. Another possible reason for the observed subsite variation is aging. In Japan, the proximal shift of colorectal cancer has been reported only among people aged 70 years or older [7]. In addition, the percentage of proximal colon adenoma has been observed to be gradually increase among people aged less than 50 years to people aged 80 years and older [39]. Risk factors may have differential effect on subsites of colorectum. In a Korean study, high body mass index (BMI) was related to distal colon cancer among men; however, BMI was more strongly related to proximal colon cancer among women [43]. A Japanese study has shown that Japanesestyle foods, such as rice or pickled vegetables, have a more protective influence on the proximal colon than the distal colon [44]. Meanwhile, the rectum is more susceptible to the negative effects of habitual smoking and binge alcohol drinking than is the colon [43,44]. The strengths of this article include the use of the high quality data from CI5 for several registries in Asia, which enabled a cancer subsite analysis. In addition, we tried to improve the comparability of the incidence rates for subsites by re-distributing unspecified or overlapping lesions to the proximal or distal colon. The limitations of this study include its coverage of a relatively short time period (10 years) for colorectal cancer incidence. Due to the high percentage of overlapping or unspecified lesions in most Asian registries, we could not extend the analysis to other registries or earlier time periods. To properly demonstrate the sophisticated patterns of colorectal cancer incidence by subsite, it is essential to analyze data for longer periods of time, i.e., 20 years or more. However, the varied quality of data available across registries limits comprehensive analysis over long periods of time. For example, in CI5 vol 8 (1992–1996) only three registries showed the percentage of overlapping and unspecified lesions of the colon (C18.8-9) less than 30%. However, 8 of 15 Asian countries had incidence rates of over 40% for overlapping or unspecified lesions among men [13]. Considering the high reported percentage of overlapping or unspecified lesions in earlier volumes of CI5 in Asian countries, the analysis of subsite-based colorectal cancer incidence in Asia remains difficult. Another limitation is that the registries included in our analysis may not represent for the whole country. Especially colorectal cancer incidence in Shanghai in China and Miyagi and Nagasaki in Japan is one of the highest in the respective countries [14]. 5. Conclusion In China, Israel, Japan, Korea, and Singapore, colorectal cancer incidence varied across countries by sex and by subsite. Miyagi prefecture in Japan had the highest ASRs for men regardless of the subsite, whereas Shanghai, China, recorded the lowest ASRs. Between 1998–2002 and 2003–2007, incidence of proximal and distal colon cancer increased in most registries, especially in Korea and Japan, but rectal cancer incidence was stable in most registries. The proportion of rectal cancer also varied between countries; it was highest in Korea and lowest in Israel. The increases in overall incidence of colorectal cancer can be attributed to increases in colon cancer incidence in Asian registries and may be due to the adoption of a Westernized life style and the expansion of cancer screening program.
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Author contributions HMP, HW, and SJJ conducted analyses. HMJ conducted literature review and wrote the first draft of the manuscript, and prepared the tables and figures. AS conceived study design and supervise data collection, analysis, and manuscript writing. KWJ and HRS contributed critical revision of data analysis. All authors reviewed and approved the final version of the manuscript. Acknowledgements This research was funded by the National Research Foundation of Korea (2013R1A1A2A10008260). The authors have no conflicts of interest. The manuscript was edited for clarity, consistency, and English-language usage by Bethanie Rammer, a professional medical editor. Appendix A. Supplementary data Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/j. canep.2016.09.012. References [1] J. Ferlay, I. Soerjomataram, M. Ervik, R. Dikshit, S. Eser, C. Mathers, M. Rebelo, D. Parkin, D. Forman, F. Bray, GLOBOCAN 2012 v1.0, Cancer Incidence and Mortality Worldwide: IARC CancerBase No. 11 [Internet], (2013) . (accessed 24.03) http://globocan.iarc.fr/. [2] J.J. Sung, J.Y. Lau, K.L. Goh, W.K.C. Leung, Asia Pacific Working Group on Colorectal, Increasing incidence of colorectal cancer in Asia: implications for screening, Lancet Oncol. 6 (11) (2005) 871–876. [3] P. Gervaz, P. Bucher, P. Morel, Two colons-two cancers: paradigm shift and clinical implications, J. Surg. Oncol. 88 (4) (2004) 261–266. [4] X.C. Wu, V.W. Chen, B. Steele, B. Ruiz, J. Fulton, L. Liu, S.E. Carozza, R. Greenlee, Subsite-specific incidence rate and stage of disease in colorectal cancer by race, gender, and age group in the United States 1992–1997, Cancer 92 (10) (2001) 2547–2554. [5] A. Miller, M. Gorska, M. Bassett, Proximal shift of colorectal cancer in the Australian Capital Territory over 20 years, Aust. N. Z. J. Med. 30 (2) (2000) 221– 225. [6] E. Svensson, T. Grotmol, G. Hoff, F. Langmark, J. Norstein, S. Tretli, Trends in colorectal cancer incidence in Norway by gender and anatomic site: an ageperiod-cohort analysis, Eur. J. Cancer Prev. 11 (5) (2002) 489–495. [7] H. Takada, T. Ohsawa, S. Iwamoto, R. Yoshida, M. Nakano, S. Imada, K. Yoshioka, M. Okuno, Y. Masuya, K. Hasegawa, N. Kamano, K. Hioki, T. Muto, Y. Koyama, Changing site distribution of colorectal cancer in Japan, Dis. Colon Rectum 45 (9) (2002) 1249–1254. [8] Y. Toyoda, T. Nakayama, Y. Ito, A. Ioka, H. Tsukuma, Trends in colorectal cancer incidence by subsite in Osaka, Japan, Jpn. J. Clin. Oncol. 39 (3) (2009) 189–191. [9] A. Shin, K.Z. Kim, K.W. Jung, S. Park, Y.J. Won, J. Kim, D.Y. Kim, J.H. Oh, Increasing trend of colorectal cancer incidence in Korea 1999–2009, Cancer Res. Treat. 44 (4) (2012) 219–226. [10] D.H. Kim, M.H. Shin, Y.O. Ahn, Incidence pattern of colorectal cancer in Korea by subsite of origin, J. Korean Med. Sci. 15 (6) (2000) 675–681. [11] J. Huang, A. Seow, C.Y. Shi, H.P. Lee, Colorectal carcinoma among ethnic Chinese in Singapore: trends in incidence rate by anatomic subsite from 1968 to 1992, Cancer 85 (12) (1999) 2519–2525. [12] B.T. Ji, S.S. Devesa, W.H. Chow, F. Jin, Y.T. Gao, Colorectal cancer incidence trends by subsite in urban Shanghai, 1972–1994, Cancer Epidemiol. Biomarkers Prev. 7 (8) (1998) 661–666. [13] M.P. Curado, B. Edwards, H.R. Shin, H. Storm, J. Ferlay, M. Heanue, P. Boyle (Eds.), Cancer Incidence in Five Continents, Vol. IX, IARC Scientific Publications, Lyon, IARC, 2007 (No. 160). [14] D. Forman, F. Bray, D.H. Brewster, M. Gombe, C.B. Kohler, M. Piñeros, E. Steliarova-Foucher, R. Swaminathan, J. Ferlay (Eds.), Cancer Incidence in Five Continents, Vol. X, IARC Scientific Publication, Lyon: International Agency for Research on Cancer, 2014 (No. 164). [15] World Health Organization, International Statistical Classification of Diseases and Related Health Problems. 10th Rev, (1994) . [16] P. Boyle, D.M. Parkin, Cancer Registration: Principles and Methods. Statistical Methods for Registries, 95, IARC scientific publications, 1991, pp. 126–158. [17] A. Drewnowski, B.M. Popkin, The Nutrition Transition: New Trends in the Global Diet, (1997) . [18] M.M. Center, A. Jemal, E. Ward, International trends in colorectal cancer incidence rates, Cancer Epidemiol. Biomarkers Prev. 18 (6) (2009) 1688–1694.
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