Temporal trends in colorectal cancer inci dence among Asian American populations in the United States, 1994–2013

Haijun Wang, Maria C. Mejia de Grubb, Sandra J. Gonzalez, Mohamad Sidani, Jianping Ma, Roger J. Zoorob

Temporal trends in colorectal cancer inci dence among Asian American populations in the United States, 1994–2013

Haijun Wang1, Maria C. Mejia de Grubb1, Sandra J. Gonzalez1, Mohamad Sidani1, Jianping Ma2, Roger J. Zoorob1

Objective:To investigate the incidence and trends in colorectal cancer (CRC) among Asian American populations in the United States.

Methods:CRC incidence data from 1994 through 2013 were obtained from 13 Surveillance,Epidemiology, and End Results registries. SEER*Stat and IBM SPSS Statistics were used.

Results:The age-adjusted incidence of CRC among Asian Americans decreased from 45.6 per 100,000 in 1994 to 33.0 per 100,000 in 2013, with the annual percent change being ?1.8%(P＜0.05). The incidences were higher for men, the elderly (aged 60 years or older), and several geographic areas. For those younger than 70 years, the rectal site was more affected compared with those aged 70 years or older, in whom the proximal site were more affected. Most patients presented with localized and regional stages. Men, 80 years or older, in situ stage, and some geographic areas such as Connecticut and California experienced significant incidence decreases in the 20-year observation period.

Conclusion:Although CRC incidence has declined among Asian American populations in the United States in the past 2 decades, there are persistent differences by age and geographic areas.Further research is needed to guide the design and implementation of tailored strategies to reduce CRC outcome differences across Asian American populations.

Colorectal cancer; proximal colon; distal colon; rectal cancer; incidence; trend

Introduction

Colorectal cancer (CRC) is the third most commonly diagnosed cancer and the second most common cause of cancer-related death among men and women in the United States [1]. The American Cancer Society (ACS) estimates that in 2014, 136,830 people received a diagnosis of CRC and 50,310 people died of the disease [2].Diagnosis, treatment, and management of CRC are associated with significant health care costs in the United States, with national expenditure for CRC exceeding $14 billion annually [3].

Data show that CRC incidence and mortality rates have declined since 1998 for non-Hispanic whites in the United States, which is widely attributed to improved adherence to CRC screening guidelines and effective cancer therapy [4—7]. Murphy et al. [8] reported the decrease in incidence of CRC among individuals 50 years or older following recommendations for population based screening.In contrast, increases in the incidence of CRC among Asian American have been reported[9]. Studies have shown that at least some Asian American subgroups are less likely to undergo screening[10]. However, CRC incidence rates for the Asian population in the United States have not been reported in detail so far.

In this study, we used data from the population-based US Surveillance, Epidemiology, and End Results (SEER) cancer registry to investigate the incidence rate of and temporal trends in CRC among Asian American populations and differences for sex, age group, stage, and anatomic site. This study aimed to examine the patterns of CRC in Asian American populations in the United States.

Materials and methods

Study population

Asian Americans represent any of the original peoples of the Far East, Southeast Asia, or the Indian subcontinent [11]. Data were obtained from 13 SEER registries, which were released in April 2016. Data were based on the November 2015 submission results [12].

The SEER Program is an authoritative source ofinformation on cancer incidence and mortality in the United States.The SEER Program collects and publishes cancer data from a set of 17 population-based regional cancer registries located throughout the country. Data include patient demographics,primary tumor site, morphology, stage at diagnosis, fi rst course of treatment, and follow-up for vital status. We selected a subset of the current SEER data that includes data from 13 population-based cancer registries in 10 states; thus our analysis covers 14% of the US population: New Mexico, Iowa, Detroit(metropolitan), Atlanta (metropolitan), Connecticut, Utah,San Jose—Monterey, Seattle (Puget Sound), San Francisco-Oakland SMSA, Los Angeles, Hawaii, Alaska Natives, and rural Georgia. In this data set, cases were diagnosed from 1994 to 2013. The population we choose to analyze is Asian/Pacific Islander. We used the SEER Historic Stage A variable for extent of disease at diagnosis. The stage includes in situ,regional, localized, distant, and unstaged. The SEER Historic Stage A variable is the only stage variable in SEER that has been recorded consistently from 1975 to 2013.

Anatomic subsites

Anatomic subsites were defi ned with the third edition of the International Classification of Diseases for Oncology [13].

The incidence of CRC was stratifi ed into the following anatomic subsites: proximal part of the colon, distal part of the colon, and rectum. The proximal part of the colon included the cecum (C18.0), ascending colon (C18.2), hepatic fl exure(C18.3), transverse colon (C18.4), and splenic fl exure (C18.5).The distal part of the colon included the descending colon(C18.6) and sigmoid colon (C18.7). The rectum included the rectum (C19.9) and rectosigmoid junction (C20.9).

Statistical methods

All analyses were performed with SEER*Stat 8.3.2 and IBM SPSS Statistics version 23.0. Rates were expressed per 100,000 person-years, and were age-adjusted to the 2000 US standard population (19 age groups — US Census P25-1130).The annual percent change (APC), which is the average annual rate of change over the time series selected, was used to measure trends or changes in rates over time. Ninety-fi ve percent confi dence intervals (CI) for age-adjusted rates and ratios were calculated with the modification of Tiwari et al.[14]. Graphs showing the incidence rates were plotted by year of diagnosis for age groups (＜50 years, 50—59 years, 60—69 years, 70—79 years, and ≥80 years), sexes, races, subsites, and stages. Only data points based on at least 25 cases by sex were used in plotting the rates. SEER Historic Stage A was used for CRC staging — in situ, localized, regional, distant, and unstaged. Incidence rates were analyzed by year of diagnosis —1994—1998, 1999—2003, 2004—2008, and 2009—2013. The incidences were compared by CIs and APC statistics to assess incidence patterns over time with a two-sided P-value that was calculated by weighted least squares methods. The percent change in a statistic over a given time interval is defi ned as(fi nal value?initial value)/initial value×100. A positive percent change corresponds to an increasing trend, and a negative percent change corresponds to a decreasing trend. The APC is used to measure the trend or change in rate over a single year,indicating the ‘a(chǎn)verage’ annual rate of change within the time series selected. A P-value less than 0.05 was considered statistically significant.

Results

Of 34,887 CRC cases diagnosed between 1994 and 2013 in the 13 SEER registries, 18,473 (52.9%) corresponded to male patients and 16,414 corresponded to female patients (47.1%).The median age was 68 years, and 97.7% cases were confirmed by positive histologic fi ndings. The overall annual ageadjusted incidence of CRC for Asian Americans in the United States was 41.0 per 100,000 per year (Table 1), which is much lower than that for non-Hispanic whites (45.1 per 100,000),blacks (55.2 per 100,000), and other races (59.9 per 100,000).The age-specific rate was the lowest among those younger than 50 years (6.0 per 100,000 per year), but it increased to 119.7 per 100,000 (20-fold) among those aged 60—69 years,and 276.4 per 100,000 (46-fold) for those aged 80 years or older. The incidence rate declined from 46.0 per 100,000 for 1994—1998 to 35.7 per 100,000 for 2009—2013. There were substantial geographic variations in incidence rates across different geographic areas. The incidence rates were lowest in New Mexico (20.0 per 100,000), and the highest in Hawaii(49.3 per 100,), with corresponding relative risks between 1.96 and 3.16. The CRC incidence rates among various registries can be roughly divided into three levels: low (＜30 per 100,000 for New Mexico, Iowa, Detroit, Atlanta, and Connecticut),medium (30—40 per 100,000 for Utah, San Jose, and Seattle),and high (＞40 per 100,000 for Los Angeles and Hawaii). Most CRCs were in localized or regional stages, and they accounted for about 40% and 35% of the total respectively. The proportions ofin situ and distant stages were relatively small: 3%and 16% respectively. Further subdivision of the time periods included in the analysis (1994—1998, 1999—2003, 2004—2008,and 2009—2013) did not result in any appreciable differences in cancer incidence by sex or anatomic subsite.

The incidence rates between anatomic subsites were compared against sex, race, age group, years of diagnosis, registries, and stage (Table 2). For males, the proximal subsite had lowest incidence rate, but for women the rectum had the lowest incidence rate. For Asian Americans the incidence rates at different anatomic sites were almost the same, but for blacks the incidence for the proximal site was twice as great as that for the distal site or for the rectal sites (27 per 100,000 vs. 13.6 per 100,000 and 13.5 per 100,000 respectively) (data not shown).Among Asian Americans the incidence rate of proximal-site CRC was higher than that at other sites but the difference was less than two-fold. Among the younger group aged less than 50 years, the incidence rate for the rectal site was the highest,the difference from the rate for the proximal site being more than two-fold (2.7 per 100,000 vs. 1.3 per 100,000). In contrast, among those aged 80 years or older, the incidence for the proximal site was almost twice that for the rectal site (125.4 per 100,000 vs. 70.2 per 100,000). The incidence differences between anatomic sites were smaller between different years and different geographic locations. The highest incidence at the in situ stage occurred for the distal site, and was four times higher than that for proximal site (2.0 per 100,000 vs. 0.6 per 100,000). The incidence rate for the rectal site at the same stage was 3.3 times greater than that for the proximal site.

Asian Americans in the United States experienced a statistically significant (1.8%, 95% CI ?2.2% to 1.4%) annual decrease in CRC incidence from 1994 to 2013 (Fig. 1). The highest incidence was in 2002 (48.3 per 100,000), and the lowest incidence was in 2013 (33.0 per 100,000). Non-Hispanic whites experienced the highest decline, 2.2% (95% CI ?2.6%to 1.9%), from 53.4 per 100,000 in 1998 to 34.1 per 100,000 in 2013. In contrast, for Asian Americans, there was a 5-year gap in the continuous incidence decrease compared with non-Hispanic whites (2003 vs. 1999). Figure 2 shows the CRC incidence trends by age group from 1994 to 2013. For those younger than 50 years and those aged 50—59 years, the incidence rates did not increase significantly (APC 0.5%, 95%CI 0.1—1.2%, and APC 0.3%, 95% CI ?0.3% to 0.9%, respectively). Significant incidence decreases were observed for age groups older than 60 years. The APCs for those aged 60—69 years, 70—79 years, and 80 years or older were ?1.8% (95% CI?2.2% to 1.4%), ?2.6% (95% CI ?1.9% to 3.4% ), and ?3.3%(95% CI ?2.6% to 3.9%) respectively. The incidence rate decreased for both sexes, with an APC of ?1.7% for women and ?1.9% for men (Fig. 3). A significant decrease of CRC incidence was not observed in New Mexico, Iowa, Detroit,Utah, and Atlanta, but significant decrease of CRC incidence occurred in Connecticut, San Jose, Seattle, San Francisco,and Los Angeles. Connecticut had the biggest CRC incidence decrease (2.9%). The age-adjusted incidence trends at all the different stages had significant decreases ranging from ?0.9%(localized) to ?4.5% (in situ) annually (Fig. 4). Among the anatomic sites, the distal anatomic site had the biggest decrease,with an APC of ?2.5% (Fig. 5). The APCs for the proximal and rectal sites were ?1.3% and ?1.8% respectively. Figure 6shows the incidence trend by stage and by subsite. Except for distant stage and unstaged cancer of the rectal site and distant stage of the distal site, significant incidence decreases were observed from 1994 to 2013. The in situ stage had biggest decrease, with an APC ?5.8% for the distal site, ?5.2% for the rectal site, and ?4.5% for proximal site.

Table 1. Demographic and disease features of Asian American with colorectal cancer by sex, 1994—2013

Table 2. Demographic and disease features of Asian American with colorectal cancer by anatomic subsites, 1994—2013

Fig. 1. Age-adjusted incidence rates of colorectal cancer by race(1994—2013).

Fig. 2. Age-adjusted incidence rates of colorectal cancer by age group (1994—2013).

Fig. 3. Age-adjusted incidence rates of colorectal cancer by sex(1994—2013).

Fig. 4. Age-adjusted incidence rates of colorectal cancer by stage(1994—2013).

Discussion

The Asian American group is the fastest-growing minority group in the United States [15, 16]. According to the 2010 US Census, Asian Americans constitute about 4.8% of the US total population. The overall incidence of CRC in the United States has steadily decreased, but the incidence rates and trends have not been addressed for Asian American populations.

The CRC incidence rates for Asian Americans were lower than those for non-Hispanic whites, but the incidence difference between both groups has been becoming smaller since 2008 (incidence rate ratio 1.1 vs. 1.08 P＜0.05). The incidence trends analysis shows that the decline in CRC incidence has been slower in Asian Americans than in non-Hispanic whites.Although CRC screening has been shown to effectively decrease mortality, it remains the least used screening tool in the United States, and is particularly underused by Asian Americans [17]. Previous studies found lower CRC screening use among Asian Americans compared with non-Hispanic whites, where 46—51% of Asian Americans were up-to-date with CRC screening compared with 56—59% of their non-Hispanic white counterparts [18—21].

Fig. 5. Age-adjusted incidence rates of colorectal cancer by anatomic site (1994—2013).

CRC is now the third most common malignant disease in both men and women in Asia, and the incidence and mortality have been rising rapidly in Asia [22—27]. This has been attributed to dietary habits including an increase in the consumption of meat, animal fat, and preserved food, as well as lifestyle factors such as cigarette smoking, alcohol drinking, and physical inactivity [22]. The opposite direction ofincidence change for Asian Americans in the United States might be related to the access to CRC screening. In the United States, overall 59.6%reported being up-to-date on CRC screening in 2010. In East Asia and Southeast Asia, the participation rate in CRC screening programs is low, and colonoscopy has not been adopted as a primary population-based screening tool because of staffi ng constraints in relation to large population size, increased costs,and potential adverse events [28].

Fig. 6. Age-adjusted incidence rates of colorectal cancer by stage and anatomic site (1994—2013).

The fi rst guidelines for CRC screening were issued in 1989 by the US Preventive Services Task Force [29], but the decrease in the incidence of CRC for the Asian American population in our study occurred in 2003, 5 years later than in the non-Hispanic white population. According to the Behavioral Risk Factor Surveillance System data from 2010, the self-reported CRC screening rate was highest in white (62.0%), followed by blacks (59.0%), Hispanics (52.5%), and Asians (47.2%) [30].Therefore the lower CRC incidence decrease might be related to lower awareness of screening tests among immigrants [31]and the lower CRC screening participation rate in the Asian American group.

Even though incidence declines occurred in all the geographic areas, there was a significant incidence decrease only in Connecticut, San Jose, Seattle, San Francisco, and Los Angeles. There were only no significant decreases in New Mexico, Iowa, Detroit, Utah and Atlanta. This may also be related to the CRC screening rates in these areas; further study is needed.

Our analysis supports the inference of a relationship between the anatomic site and patients’ age: more cancers were in the rectal site at younger ages (＜50 years) and in proximal site at later ages. This pattern is similar to that in the study of Meyer et al. [32] but the reasons remain unknown. We also found that younger age increases the risk of lymph node positivity in early-stage rectal cancer [33].

Our results show that the largest decrease in incidence overall occurred for the in situ stage. This may be related to the new CRC screening guideline (implemented in 1998) that promoted a higher CRC screening rate to detect precancerous polyps so they could be removed before progressing to CRC.Kubisch et al. [34] found that screening for CRC using fecal occult blood tests and colonoscopy is associated with reduced CRC incidence and mortality [34].

There are several limitations in interpreting these results.First, each SEER registry is responsible for fi nding cancer cases in its defi ning registry area. Misdiagnosis and underregistration in SEER registries are potential issues [35]. Second, the data were from only 13 of 18 available registries, representing 14% of the US population, so they may not be representative of the general US population. Last, changes in diagnostic capabilities, including screening and pathology, may also inf l uence the accuracy ofincidence data collected over time [6].

In spite of these potential limitations, our populationbased study provides trends in the incidence of CRC for Asian Americans in the United States and describes patterns that have not been reported previously. The diverse incidence patterns by age group, sex, stage, and anatomic site, along with geographic area, may be indicative of a specific cause. These data may be useful in planning public health strategies, identifying risks, and understanding the causes of CRC for future prevention.

1. Liles EG, Coronado GD, Perrin N, Harte AH, Nungesser R,Quigley N, et al. Uptake of a colorectal cancer screening blood test is higher than of a fecal test offered in clinic: a randomized trial. Cancer Treat Res Commun 2016;10:27—31.

2. Oliva JT, Lee HD, Spola?r N, Coy CS, Wu FC. Prototype system for feature extraction, classification and study of medical images.Expert Syst Appl 2016;63:267—83.

3. Mariotto AB, Yabroff KR, Shao Y, Feuer EJ, Brown ML. Projections of the cost of cancer care in the United States: 2010—2020.J Natl Cancer Inst 2011;103(2):117—28.

4. Allison JE, Potter MB. New screening guidelines for colorectal cancer: a practical guide for the primary care physician. Prim Care 2009;36(3):575—602.

5. Yoo W, De S, Wilkins T, Smith SA, Blumenthal D. Age, race and regional disparities in colorectal cancer incidence rates in Georgia between 2000 and 2012. Ann Public Health Res 2016;3(2).

6. Cheng L, Eng C, Nieman LZ, Kapadia AS, Du XL. Trends in colorectal cancer incidence by anatomic site and disease stage in the United States from 1976 to 2005. Am J Clin Oncol 2011;34(6):573—80.

7. Weir HK, Lic, Henley SJ, Joseph D. Years of life and productivity lost from potentially avoidable colorectal cancer deaths in US counties with lower educational attainment (2008—2012). Cancer Epidemiol Prev Biomarkers 2016.

8. Murphy CC, Sandler RS, Sanoff HK, Yang YC, Lund JL, Baron JA. Decrease in incidence of colorectal cancer among individuals 50 years or older after recommendations for population-based screening. Clin Gastroenterol Hepatol 2016. doi: 10.1016/j.cgh.2016.08.037.

9. Giddings BH, Kwong SL, Parikh-Patel A, Bates JH, Snipes KP.Going against the tide: increasing incidence of colorectal cancer among Koreans, Filipinos, and South Asians in California,1988—2007. Cancer Causes Control 2012;23(5):691—702.

10. UCLA Center for Health Policy Research. California Health Interview Survey AskCHIS. 2009 data [accessed 2017 Jan 18].Available from: http://chis.ucla.edu.

11. Loue S. Assessing race, ethnicity and gender in health. New York, NY: Springer Science & Business Media; 2006.

12. Surveillance, Epidemiology, and End Results (SEER) Program(www.seer.cancer.gov) SEER*Stat Database: incidence - SEER 13 regs research data, Nov 2015 sub (1992—2013) ＜Katrina/Rita population adjustment＞ - linked to county attributes - total U.S.,1969—2014 counties, National Cancer Institute, DCCPS, Surveillance Research Program, Surveillance Systems Branch, released April 2016, based on the November 2015 submission.

13. SEER. ICD-O-3 coding materials, 2004. Available from: http://seer.cancer.gov/icd-o-3/.

14. Tiwari RC, Ghosh K, Jemal A, Hachey M, Ward E, Thun MJ,et al. A new method of predicting US and state-level cancer mortality counts for the current calendar year. CA Cancer J Clin 2004;54(1):30—40.

15. Esperat MC, Inouye J, Gonzalez EW, Owen DC, Feng D. Health disparities among Asian Americans and Pacific Islanders. Annu Rev Nurs Res 2004;22:135—59.

16. OHare WP, Felt JC. Asian Americans: Americas fastest growing minority group. 1991:1—16.

17. Fedewa SA, Sauer AG, Siegel RL, Smith RA, Torre LA, Jemal A. Temporal trends in colorectal cancer screening among Asian Americans. Cancer Epidemiol Biomarkers Prev 2016;25(6):995—1000.

18. Jerant AF, Fenton JJ, Franks P. Determinants of racial/ ethnic colorectal cancer screening disparities. Arch Intern Med 2008;168(12):1317—24.

19. Maxwell AE, CrespicM. Trends in colorectal cancer screening utilization among ethnic groups in California: are we closing the gap? Cancer Epidemiol Biomarkers Prev 2009;18(3):752—9.

20. Ioannou GN, Chapko MK, Dominitz JA. Predictors of colorectal cancer screening participation in the United States. Am J Gastroenterol 2003;98(9):2082—91.

21. Fedewa SA, Sauer AG, Siegel RL, Jemal A. Prevalence of major risk factors and use of screening tests for cancer in the United States. Cancer Epidemiol Biomarkers Prev 2015;24(4):637—52.

22. Sung JJ, Lau JY, Goh KL, Leung WK. Increasing incidence of colorectal cancer in Asia: implications for screening. Lancet Oncol 2005;6(11):871—6.

23. Ng SC, Wong SH. Colorectal cancer screening in Asia. Br Med Bull 2013;105:29—42.

24. Wong MT, Eu KW. Rise of colorectal cancer in Singapore: an epidemiological review. Aust N Z J Surg 2007;77(6):446—9.

25. Hirabayashi Y, Tanaka S. Comparison of time trends in colorectal cancer incidence (1973—97) in East Asia, Europe and USA, from Cancer Incidence in Five Continents Vol. IV—VIII. Jpn J Clin Oncol 2007;37(4):325—7.

26. Zhu J, Tan Z, Hollis-Hansen K, Zhang Y, Yu C, Li Y. Epidemiological trends in colorectal cancer in China: an ecological study.Dig Dis Sci 2017;62(1):235—43.

27. Zhou Q, Li K, Lin GZ, Shen JC, Dong H, Gu YT, et al. Incidence trends and age distribution of colorectal cancer by subsite in Guangzhou, 2000—2011. Chin J Cancer 2015;34(8):358—64.

28. Sano Y, Byeon JS, Li XB, Wong M, Chiu HM, Rerknimitr R,et al. Colorectal cancer screening of the general population in East Asia. Dig Endosc 2016;28(3):243—9.

29. Atkins D. First new screening recommendations from the third US Preventive Services Task Force. Br Med J 2003;327(7418):E21—4.

30. Liss DT, Baker DW. Understanding current racial/ethnic disparities in colorectal cancer screening in the United States: the contribution of socioeconomic status and access to care. Am J Prev Med 2014;46(3):228—36.

31. Carrasco-Garrido P, Hernandez-Barrera V, de Andres AL,Jimenez-Trujillo I, Pino CG, Jimenez-Garc?a R. Awareness and uptake of colorectal, breast, cervical and prostate cancer screening tests in Spain. Eur J Public Health 2014;24(2):264—70.

32. Chong VH, Telisinghe PU, Bickle I, Abdullah MS, Lim E,Chong CF. Increasing incidence of colorectal cancer, starting at a younger age for rectal compared to colon cancer in Brunei Darussalam. Asian Pac J Cancer Prev 2015;16(12):5063—7.

33. Meyer JE, Cohen SJ, Ruth KJ, Sigurdson ER, Hall MJ. Young age increases risk of lymph node positivity in early-stage rectal cancer. J Natl Cancer Inst 2016;108(1). doi: 10.1093/jnci/djv284.

34. Kubisch CH, Crispin A, Mansmann U, G?ke B, Kolligs FT.Screening for colorectal cancer is associated with lower disease stage: a population-based study. Clin Gastroenterol Hepatol 2016;14(11):1612—8.e3.

35. Wang H, Chen Y, Li F, Delasalle K, Wang J, Alexanian R, et al.Temporal and geographic variations of Waldenstrom macroglobulinemia incidence: a large population-based study. Cancer 2012;118(15):3793—800.

1. Department of Family and Community Medicine, Baylor College of Medicine, Houston,TX, USA

2. Shenzhen Nanshan Center for Chronic Disease Control, Shenzhen, Guangdong, China

Haijun Wang, PhD, MPH

Department of Family and Community Medicine, Baylor College of Medicine, 3701 Kirby Drive, Suite 600, Houston, TX 77098, USA

E-mail: haijun.wang@bcm.edu

31 January 2017;Accepted 14 March 2017