Abstract
Purpose
Colorectal cancer (CRC) is the second most common cause of cancer death in developed countries among men (after lung cancer) and the third most common among women. This study thus examines the long-term trends of CRC mortality in Taiwan.
Methods
CRC cases were collective between patients aged 30 years or older and younger than 85 years from the Taiwan death registries during 1971–2010. Standard descriptive techniques such as age-standardized mortality rates (ASMR), aural percent change, and age–period–cohort analyses were used.
Results
The increase of percentage change by each age group in men was higher than in women. The ASMR of CRC increased 2-fold for men and almost 1.5-fold for women during the periods 1971–1975 and 2006–2010. For age–period–cohort analysis, the estimated mortality rate increased steadily with age in both sexes, and plateaued at 175.29 per 100,000 people for men and 128.14 per 100,000 for women in the 80- to 84-year-old group. Period effects were weak in both sexes. Cohort effects were strong. Between 30 and 59 years of age, the sex ratio showed that the female CRC mortality rate was higher than that of their male counterparts. Conversely, the mortality risk of CRC in men was higher than that in women when they were between 60 and 84 years old.
Conclusions
The current findings showed a consistent increase in mortality from CRC over the years. Changes in the patient sex ratio indicated an important etiological role of sex hormones, especially in women aged 60 years or younger.
This is a preview of subscription content, access via your institution.



Reference
Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D (2011) Global cancer statistics. CA Cancer J Clin 61(2):69–90. doi:10.3322/caac.20107
Center MM, Jemal A, Smith RA, Ward E (2009) Worldwide variations in colorectal cancer. CA Cancer J Clin 59(6):366–378. doi:10.3322/caac.20038
Giovannucci EWK (2006) Cancers of the colon and rectum. In: Schottenfeld D, Fraumeni J (eds) Cancer epidemiology and prevention, 3rd edn. Oxford University Press, New York, pp 809–829
Botteri E, Iodice S, Bagnardi V, Raimondi S, Lowenfels AB, Maisonneuve P (2008) Smoking and colorectal cancer: a meta-analysis. JAMA J Am Med Assoc 300(23):2765–2778. doi:10.1001/jama.2008.839
Giovannucci E (2002) Modifiable risk factors for colon cancer. Gastroenterol Clin N Am 31(4):925–943
Ferrari P, Jenab M, Norat T, Moskal A, Slimani N, Olsen A, Tjonneland A, Overvad K, Jensen MK, Boutron-Ruault MC, Clavel-Chapelon F, Morois S, Rohrmann S, Linseisen J, Boeing H, Bergmann M, Kontopoulou D, Trichopoulou A, Kassapa C, Masala G, Krogh V, Vineis P, Panico S, Tumino R, van Gils CH, Peeters P, Bueno-de-Mesquita HB, Ocke MC, Skeie G, Lund E, Agudo A, Ardanaz E, Lopez DC, Sanchez MJ, Quiros JR, Amiano P, Berglund G, Manjer J, Palmqvist R, Van Guelpen B, Allen N, Key T, Bingham S, Mazuir M, Boffetta P, Kaaks R, Riboli E (2007) Lifetime and baseline alcohol intake and risk of colon and rectal cancers in the European prospective investigation into cancer and nutrition (EPIC). Int J Cancer J Int Cancer 121(9):2065–2072. doi:10.1002/ijc.22966
Edwards BK, Ward E, Kohler BA, Eheman C, Zauber AG, Anderson RN, Jemal A, Schymura MJ, Lansdorp-Vogelaar I, Seeff LC, van Ballegooijen M, Goede SL, Ries LA (2010) Annual report to the nation on the status of cancer, 1975–2006, featuring colorectal cancer trends and impact of interventions (risk factors, screening, and treatment) to reduce future rates. Cancer 116(3):544–573. doi:10.1002/cncr.24760
Chu KC, Tarone RE, Chow WH, Hankey BF, Ries LA (1994) Temporal patterns in colorectal cancer incidence, survival, and mortality from 1950 through 1990. J Natl Cancer Inst 86(13):997–1006
Sant M, Capocaccia R, Coleman MP, Berrino F, Gatta G, Micheli A, Verdecchia A, Faivre J, Hakulinen T, Coebergh JW, Martinez-Garcia C, Forman D, Zappone A (2001) Cancer survival increases in Europe, but international differences remain wide. Eur J Cancer 37(13):1659–1667
Mitry E, Bouvier AM, Esteve J, Faivre J (2002) Benefit of operative mortality reduction on colorectal cancer survival. Br J Surg 89(12):1557–1562. doi:10.1046/j.1365-2168.2002.02276.x
Sung JJ, Lau JY, Young GP, Sano Y, Chiu HM, Byeon JS, Yeoh KG, Goh KL, Sollano J, Rerknimitr R, Matsuda T, Wu KC, Ng S, Leung SY, Makharia G, Chong VH, Ho KY, Brooks D, Lieberman DA, Chan FK (2008) Asia Pacific consensus recommendations for colorectal cancer screening. Gut 57(8):1166–1176. doi:10.1136/gut.2007.146316
Cause of death statistics in Taiwan. (2010)
Carstensen B (2007) Age–period–cohort models for the Lexis diagram. Stat Med 26(15):3018–3045. doi:10.1002/sim.2764
Russo A, Autelitano M, Bisanti L (2008) Metabolic syndrome and cancer risk. Eur J Cancer 44(2):293–297. doi:10.1016/j.ejca.2007.11.005
Pollak M (2008) Insulin, insulin-like growth factors and neoplasia. Best Pract Res Clin Endocrinol Metab 22(4):625–638. doi:10.1016/j.beem.2008.08.004
Chiou WK, Wang MH, Huang DH, Chiu HT, Lee YJ, Lin JD (2010) The relationship between serum uric acid level and metabolic syndrome: differences by sex and age in Taiwanese. J Epidemiol / Jpn Epidemiol Assoc 20(3):219–224
Hu NC, Chen JD, Lin YM, Chang JY, Chen YH (2011) Stepwise relationship between components of metabolic syndrome and risk of colorectal adenoma in a Taiwanese population receiving screening colonoscopy. Journal of the Formosan Medical Association =. Taiwan yi zhi 110(2):100–108. doi:10.1016/S0929-6646(11)60016-8
Wang CCTTC, Hsiehb T, Hsua CS, Wanga PC, Lina HH, Kao JH (2012) Severity of fatty liver on ultrasound correlates with metabolic and cardiovascular risk. Kaohsiung J Med Sci:1-10
Lin YC, Chou SC, Huang PT, Chiou HY (2011) Risk factors and predictors of non-alcoholic fatty liver disease in Taiwan. Ann Hepato Off J Mex Assoc Hepatol 10(2):125–132
Center MM, Jemal A, Ward E (2009) International trends in colorectal cancer incidence rates. Cancer Epidemiol, Biomark Prev: Publ Am Assoc Cancer Res, cosponsored Am Soc Prev Oncol 18(6):1688–1694. doi:10.1158/1055-9965.EPI-09-0090
Chen LT, Whang-Peng J (2004) Current status of clinical studies for colorectal cancer in Taiwan. Clin Colorectal Cancer 4(3):196–203
Yeh CC, Hsieh LL, Tang R, Chang-Chieh CR, Sung FC (2003) Risk factors for colorectal cancer in Taiwan: a hospital-based case-control study. J Formos Med Assoc = Taiwan yi zhi 102(5):305–312
Wang TS (2001) Legal reform in Taiwan under Japanese colonial rule, 1895–1945: the reception of western law. J Asian Stud 60(1):157–159
Jemal A, Siegel R, Xu J, Ward E (2010) Cancer statistics, 2010. CA Cancer J Clin 60(5):277–300. doi:10.3322/caac.20073
Thong T (2011) To Raise the savage to a higher level: the westernization of Nagas and their culture. Mod Asian Stu:1-26
dos Santos SI, Swerdlow AJ (1996) Sex differences in time trends of colorectal cancer in England and Wales: the possible effect of female hormonal factors. Br J Cancer 73(5):692–697
Zervoudakis A, Strickler HD, Park Y, Xue X, Hollenbeck A, Schatzkin A, Gunter MJ (2011) Reproductive history and risk of colorectal cancer in postmenopausal women. J Natl Cancer Inst 103(10):826–834. doi:10.1093/jnci/djr101
Kelsey JL, Gammon MD, John EM (1993) Reproductive factors and breast cancer. Epidemiol Rev 15(1):36–47
Chavez-MacGregor M, Elias SG, Onland-Moret NC, van der Schouw YT, Van Gils CH, Monninkhof E, Grobbee DE, Peeters PH (2005) Postmenopausal breast cancer risk and cumulative number of menstrual cycles. Cancer Epidemiol, Biomark Prev Pub Am Assoc Cancer Res, cosponsored Am Soc Prev Oncol 14(4):799–804. doi:10.1158/1055-9965.EPI-04-0465
Dossus L, Allen N, Kaaks R, Bakken K, Lund E, Tjonneland A, Olsen A, Overvad K, Clavel-Chapelon F, Fournier A, Chabbert-Buffet N, Boeing H, Schutze M, Trichopoulou A, Trichopoulos D, Lagiou P, Palli D, Krogh V, Tumino R, Vineis P, Mattiello A, Bueno-de-Mesquita HB, Onland-Moret NC, Peeters PH, Dumeaux V, Redondo ML, Duell E, Sanchez-Cantalejo E, Arriola L, Chirlaque MD, Ardanaz E, Manjer J, Borgquist S, Lukanova A, Lundin E, Khaw KT, Wareham N, Key T, Chajes V, Rinaldi S, Slimani N, Mouw T, Gallo V, Riboli E (2010) Reproductive risk factors and endometrial cancer: the European prospective investigation into cancer and nutrition. Int J Cancer J Int Cancer 127(2):442–451. doi:10.1002/ijc.25050
Lin J, Zhang SM, Cook NR, Manson JE, Buring JE, Lee IM (2007) Oral contraceptives, reproductive factors, and risk of colorectal cancer among women in a prospective cohort study. Am J Epidemiol 165(7):794–801. doi:10.1093/aje/kwk068
Jacobs EJ, White E, Weiss NS (1994) Exogenous hormones, reproductive history, and colon cancer (Seattle, Washington, USA). Cancer Causes Control CCC 5(4):359–366
Tsilidis KK, Allen NE, Key TJ, Bakken K, Lund E, Berrino F, Fournier A, Olsen A, Tjonneland A, Overvad K, Boutron-Ruault MC, Clavel-Chapelon F, Byrnes G, Chajes V, Rinaldi S, Chang-Claude J, Kaaks R, Bergmann M, Boeing H, Koumantaki Y, Stasinopoulou G, Trichopoulou A, Palli D, Tagliabue G, Panico S, Tumino R, Vineis P, Bueno-de-Mesquita HB, van Duijnhoven FJ, van Gils CH, Peeters PH, Rodriguez L, Gonzalez CA, Sanchez MJ, Chirlaque MD, Barricarte A, Dorronsoro M, Borgquist S, Manjer J, van Guelpen B, Hallmans G, Rodwell SA, Khaw KT, Norat T, Romaguera D, Riboli E (2010) Oral contraceptives, reproductive history and risk of colorectal cancer in the European prospective investigation into cancer and nutrition. Br J Cancer 103(11):1755–1759. doi:10.1038/sj.bjc.6605965
Kabat GC, Miller AB, Rohan TE (2008) Oral contraceptive use, hormone replacement therapy, reproductive history and risk of colorectal cancer in women. Int J Cancer J Int Cancer 122(3):643–646. doi:10.1002/ijc.23079
Nations U (2004) Press release: Majority of world's couples of reproductive age are using contraception (DEV/2469; POP/902). Department of Public Information, New York
Selby JV, Friedman GD, Quesenberry CP Jr, Weiss NS (1992) A case–control study of screening sigmoidoscopy and mortality from colorectal cancer. N Engl J Med 326(10):653–657. doi:10.1056/NEJM199203053261001
Winawer S, Fletcher R, Rex D, Bond J, Burt R, Ferrucci J, Ganiats T, Levin T, Woolf S, Johnson D, Kirk L, Litin S, Simmang C (2003) Colorectal cancer screening and surveillance: clinical guidelines and rationale—update based on new evidence. Gastroenterology 124(2):544–560. doi:10.1053/gast.2003.50044
Yen SJ, Leu SY, Hsu H (1994) Colonoscopic screening for first degree relatives of patients with colorectal cancer. Zhonghua yi xue za zhi = Chin Med J Free China ed 54(3):166–169
Forbes SS, Sutradhar R, Paszat LF, Rabeneck L, Urbach DR, Baxter NN (2010) Long-term survival in young adults with colorectal cancer: a population-based study. Dis Colon Rectum 53(7):973–978. doi:10.1007/DCR.0b013e3181cf8341
Zbuk K, Sidebotham EL, Bleyer A, La Quaglia MP (2009) Colorectal cancer in young adults. Semin Oncol 36(5):439–450. doi:10.1053/j.seminoncol.2009.07.008
Bedikian AY, Kantarjian H, Nelson RS, Stroehlein JR, Bodey GP (1981) Colorectal cancer in young adults. South Med J 74(8):920–924
MacGillivray DC, Swartz SE, Robinson AM, Cruess DF, Smith LE (1991) Adenocarcinoma of the colon and rectum in patients less than 40 years of age. Surg, Gynecol Obstet 172(1):1–7
Turkiewicz D, Miller B, Schache D, Cohen J, Theile D (2001) Young patients with colorectal cancer: how do they fare? ANZ J Surg 71(12):707–710
Minardi AJ Jr, Sittig KM, Zibari GB, McDonald JC (1998) Colorectal cancer in the young patient. Am Surg 64(9):849–853
Tung SY, Wu CS (2000) Risk factors for colorectal adenomas among immediate family members of patients with colorectal cancer in Taiwan: a case–control study. Am J Gastroenterol 95(12):3624–3628. doi:10.1111/j.1572-0241.2000.03380.x
Liou TY, Hsu H, Chen SS, Feng YS, Wang HM (1989) Evaluation of rapid colon preparation by oral intake of dulcolax for colorectal surgery. Zhonghua yi xue za zhi = Chin Med J Free China ed 44(2):103–108
Chen CF, Lin JK, Leu SY, Liang CL (1989) Evaluation of rapid colon preparation with Golytely. Zhonghua yi xue za zhi = Chin Med J Free China ed 44(1):45–56
Chiu HM, Lin JT, Wu MS, Wang HP (2009) Current status and future perspective of endoscopic diagnosis and treatment for colorectal neoplasia—situation in Taiwan. Dig Endosc Off J Japan Gastroenterol Endosc Soc 21(Suppl 1):S17–21. doi:10.1111/j.1443-1661.2009.00853.x
Lopez-Abente G, Ardanaz E, Torrella-Ramos A, Mateos A, Delgado-Sanz C, Chirlaque MD (2010) Changes in colorectal cancer incidence and mortality trends in Spain. Ann Oncol Off J Eur Soc Med Oncol / ESMO 21(Suppl 3):iii76–82. doi:10.1093/annonc/mdq091
Conflict of interest
The authors have no funding or financial relationships to declare.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
ESM 1
(PDF 1539 kb)
Rights and permissions
About this article
Cite this article
Su, SY., Huang, JY., Jian, ZH. et al. Mortality of colorectal cancer in Taiwan, 1971–2010: temporal changes and age–period–cohort analysis. Int J Colorectal Dis 27, 1665–1672 (2012). https://doi.org/10.1007/s00384-012-1521-8
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00384-012-1521-8
Keywords
- Age–period–cohort analysis
- Colorectal cancer
- Sex ratio
- Taiwan