Abstract
Background:
Literature on colorectal cancer (CRC) outcomes in individuals of Middle Eastern and North African (MENA) descent is limited. To address this gap, we estimated five-year CRC-specific survival by race and ethnicity, including MENA individuals, in a diverse, population-based sample in California.
Methods:
We identified adults (ages 18–79 years) diagnosed with a first or only CRC in 2004 – 2017 using the California Cancer Registry, including non-Hispanic White, non-Hispanic Black, non-Hispanic Asian, Hispanic, and MENA individuals. For each racial/ethnic group, we calculated five-year CRC-specific survival and used Cox proportional hazards regression models to examine the association of race/ethnicity and survival, adjusting for clinical and sociodemographic factors.
Results:
Of 110,192 persons diagnosed with CRC, five-year CRC-specific survival was lowest in Black (61.0%) and highest in MENA (73.2%) individuals. Asian (72.2%) individuals had higher survival than White (70.0%) and Hispanic (68.2%) individuals. In adjusted analysis, MENA (aHR 0.82, 95% CI 0.76, 0.89), Asian (aHR 0.86, 95% CI 0.83, 0.90), and Hispanic (aHR 0.94, 95% CI 0.91, 0.97) race/ethnicity were associated with higher, and Black (aHR 1.13, 95% CI 1.09, 1.18) race/ethnicity was associated with lower, survival compared to non-Hispanic White race/ethnicity.
Conclusion:
To our knowledge, this is the first study to report CRC survival in MENA individuals in the U.S. We observed higher survival of MENA individuals compared to other racial/ethnic groups, adjusting for sociodemographic and clinical factors.
Impact:
Future studies are needed to identify factors contributing to cancer outcomes in this unique population.
Keywords: colorectal cancer, survival, Middle Eastern, race/ethnicity, population-based
Introduction
Colorectal cancer (CRC) is the second leading cause of cancer-related mortality among men and women in the United States (U.S.).(1) Incidence rates have decreased steadily over the past two decades (from 55.1 per 100,000 persons in 2000 to 37.2 per 100,000 persons in 2019), but five-year relative survival has improved little during the same time period (from 62.1% in 2000 to 63.8% in 2014) (Surveillance Epidemiology and End Results; RRID:SCR_006902).
Current literature on CRC risk and outcomes in individuals of Middle Eastern and North African (MENA) descent is limited. MENA individuals comprise a diverse population group and are generally defined as having heritage from one of 22 member states of the Arab League and some non-Arabic speaking countries, including Iran, Turkey, and Israel. In the U.S., the MENA population exceeds 4 million and accounts for roughly 3% of all immigrants,(2) with the highest concentration in Michigan and California.(3) The U.S. Census and many national surveys (e.g., National Health Interview Survey) classify MENA individuals as White, guided by a 1997 Office of Management and Budget standard that defines White individuals as having origins in Europe, the Middle East, or North Africa. The National Institutes of Health similarly excludes the MENA population from its list of health disparity populations. As a consequence, MENA individuals are often invisible in studies of cancer epidemiology,(4, 5) masking differences in risk and outcomes.
We previously reported characteristics of MENA women diagnosed with breast cancer in in California, observing higher survival in first-generation MENA women compared to White women, despite having higher odds of being diagnosed with non-localized disease at diagnosis.(6) To our knowledge, no study to date has investigated CRC survival in MENA individuals using a population-based sample. In the present study, we extend the findings of our prior work by estimating five-year CRC-specific survival by race and ethnicity, including MENA individuals, in a diverse, population-based sample of adults diagnosed with CRC.
Materials and Methods
We identified persons newly diagnosed with a first or only incident, invasive CRC at ages 18 – 79 years using population-based data from the California Cancer Registry (CCR) during the period 2004 – 2017. CRC was defined using International Classification of Diseases for Oncology, 3rd Edition (ICD-O-3) codes for “colon” (C180–189, C260) and “rectum” (C199, C209) (more information at: https://seer.cancer.gov/siterecode/). CCR is California’s statewide, population-based cancer surveillance system and routinely collects data on demographics (e.g., health insurance, socioeconomic status [SES], marital status), cancer characteristics (e.g., primary tumor site, stage at diagnosis, tumor grade or differentiation), and treatment (e.g., surgery, chemotherapy). Insurance was categorized as managed care, Medicare, Medicaid, other insurance (inclusive of fee-for-Service, TRICARE, Veterans Affairs, or not otherwise specified), and not insured or unknown. The Yost and Yang indices were used to categorize census tract-level SES into quintiles for persons diagnosed before and after 2006, respectively; these are composite indices of SES contained within the CCR and based on principal component analysis of block group level census variables such as education, income, and occupation.(7, 8) We used the American Joint Committee on Cancer staging system, 6th (diagnosis years 2004 – 2009) and 7th (diagnosis years 2010+) editions, to categorize cancer stage (I, II, III, and IV) using a combination of clinical and pathologic information. Tumor grade or differentiation was categorized as: grade I or well differentiated, grade II or moderately differentiated, grade III or poorly differentiated, grade IV or undifferentiated/anaplastic, and grade/differentiation unknown. Treatment quality was measured as receipt of National Comprehensive Cancer Network (NCCN)-concordant treatment,(9, 10) which has been associated with improved survival in patients with colon cancer;(11) see Supplementary Table 1 for details.
We identified 127,127 persons diagnosed with incident, invasive CRC, subsequently excluding those diagnosed on autopsy or death certificate only (n=521), those with missing or unknown stage (n=9,869) or treatment (n=6,517) information, and those with a missing surname (n=28). A total of 110,192 persons were included in final analytic sample.
We included individuals who were non-Hispanic White (“White”), non-Hispanic Black (“Black”), non-Hispanic Asian (“Asian”), Hispanic (any race), MENA, and other/unknown (inclusive of Pacific Islander and American Indian or Alaska Native). Specifically, we identified MENA individuals using a validated list of common Middle Eastern surnames linked to the CCR, with a sensitivity of 91% for men and 86% for women in detecting MENA place of birth.(12) Using cause of death recorded in the CCR, we defined CRC-specific mortality as death caused by CRC; persons who died of other causes or who were alive at the end of follow-up on November 30, 2018 were censored. Similarly, we defined overall mortality as death from all causes; persons who were alive at the end of follow-up were censored.
For each racial and ethnic (hereafter “racial/ethnic” or “race/ethnicity”) group, we estimated five-year CRC-specific survival (overall and by stage I-III versus IV) using Kaplan-Meier methods and compared survival by race/ethnicity with a log-rank test. We reported survival percentages and corresponding standard errors (SEs). We then used Cox proportional hazards regression models to examine the association of race/ethnicity and survival (CRC-specific and overall), adjusting for age at diagnosis, year of diagnosis, sex, insurance, census tract-level SES, marital status, tumor site (colon versus rectum), stage at diagnosis, tumor grade or differentiation, and receipt of NCCN-concordant treatment. To assess the proportional hazards assumption, we used Kaplan-Meier curves to compare the survival function with respect to survival time; because our covariates were time-fixed and categorical, the presence of parallel curves in our graphs indicated that the assumption was not violated. We reported adjusted hazard ratios (aHR) and 95% confidence intervals (CIs).
Analyses were conducted using SAS version 9.4 (SAS Institute, Cary, NC). Statistical significance was set at p<0.05 using two-tailed tests.
Results
We identified 110,192 persons diagnosed with CRC, of whom 58,375 (53.0%) were White, 8,383 (7.6%) were Black, 15,448 (14.0%) were Asian, 23,539 (21.4%) were Hispanic, 2,656 (2.4%) were MENA, and 1,791 (1.6%) were other/unknown. Table 1 summarizes characteristics of the study population by race/ethnicity. Census tract-level SES was highest among MENA individuals (32.9% in Quintile 5) and lowest among Hispanic and Black individuals (7.9% and 9.6% in Quintile 5, respectively). MENA and Asian individuals had fewer stage IV diagnoses (21.5 % and 21.7%, respectively) compared to Hispanic and Black individuals (24.0% and 27.8%, respectively).
Table 1.
Characteristics of 110,192 persons (age 18–79 years) diagnosed with colorectal cancer by race/ethnicity, California Cancer Registry, 2004 – 2017a
Total (n=110,192) | MENA (n=2,656, 2.4% of total) | White (n=58,375, 53.0% of total) | Black (n=8,383, 7.6% of total) | Hispanic (n=23,539, 21.4% of total) | Asian (n=15,448, 14.0% of total) | Other/unknownb (n=1,791, 1.6% of total) |
||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
n | Col % | n | Col % | n | Col % | n | Col % | n | Col % | n | Col % | n | Col % | |
Tumor site | ||||||||||||||
Colon | 80083 | 72.7% | 1975 | 74.4% | 42600 | 73.0% | 6670 | 79.6% | 16776 | 71.3% | 10847 | 70.2% | 1215 | 67.8% |
Rectum | 30109 | 27.3% | 681 | 25.6% | 15775 | 27.0% | 1713 | 20.4% | 6763 | 28.7% | 4601 | 29.8% | 576 | 32.2% |
Age at diagnosis | ||||||||||||||
18–44 | 8838 | 8.0% | 200 | 7.5% | 3601 | 6.2% | 615 | 7.3% | 2993 | 12.7% | 1260 | 8.2% | 169 | 9.4% |
45–54 | 21131 | 19.2% | 508 | 19.1% | 10038 | 17.2% | 1774 | 21.2% | 5313 | 22.6% | 3069 | 19.9% | 429 | 24.0% |
55–64 | 30141 | 27.4% | 733 | 27.6% | 15661 | 26.8% | 2554 | 30.5% | 6471 | 27.5% | 4217 | 27.3% | 505 | 28.2% |
65+ | 50082 | 45.4% | 1215 | 45.7% | 29075 | 49.8% | 3440 | 41.0% | 8762 | 37.2% | 6902 | 44.7% | 688 | 38.4% |
Year of diagnosis | ||||||||||||||
2004–2009 | 46269 | 42.0% | 1095 | 41.2% | 26320 | 45.1% | 3692 | 44.0% | 8407 | 35.7% | 6155 | 39.8% | 600 | 33.5% |
2010+ | 63923 | 58.0% | 1561 | 58.8% | 32055 | 54.9% | 4691 | 56.0% | 15132 | 64.3% | 9293 | 60.2% | 1191 | 66.5% |
Sex | ||||||||||||||
Male | 58885 | 53.4% | 1538 | 57.9% | 31450 | 53.9% | 4091 | 48.8% | 12808 | 54.4% | 8065 | 52.2% | 933 | 52.1% |
Female | 51307 | 46.6% | 1118 | 42.1% | 26925 | 46.1% | 4292 | 51.2% | 10731 | 45.6% | 7383 | 47.8% | 858 | 47.9% |
Insurance | ||||||||||||||
Managed carec | 52081 | 47.3% | 972 | 36.6% | 28062 | 48.1% | 4257 | 50.8% | 10959 | 46.6% | 7077 | 45.8% | 754 | 42.1% |
Medicare | 28943 | 26.3% | 841 | 31.7% | 16725 | 28.7% | 2063 | 24.6% | 5036 | 21.4% | 3908 | 25.3% | 370 | 20.7% |
Medicaid | 10253 | 9.3% | 381 | 14.3% | 2979 | 5.1% | 1046 | 12.5% | 3797 | 16.1% | 1881 | 12.2% | 169 | 9.4% |
Other (FFS, Tricare, VA, or NOS) | 14543 | 13.2% | 361 | 13.6% | 8902 | 15.2% | 697 | 8.3% | 2353 | 10.0% | 1971 | 12.8% | 259 | 14.5% |
Not insured or unknownd | 4372 | 4.0% | 101 | 3.8% | 1707 | 2.9% | 320 | 3.8% | 1394 | 5.9% | 611 | 4.0% | 239 | 13.3% |
Socioeconomic Status | ||||||||||||||
Lowest SES | 18234 | 16.5% | 194 | 7.3% | 5798 | 9.9% | 2414 | 28.8% | 7710 | 32.8% | 1838 | 11.9% | 280 | 15.6% |
Lower-middle SES | 22167 | 20.1% | 489 | 18.4% | 10250 | 17.6% | 2099 | 25.0% | 6096 | 25.9% | 2849 | 18.4% | 384 | 21.4% |
Middle SES | 23123 | 21.0% | 495 | 18.6% | 12730 | 21.8% | 1661 | 19.8% | 4564 | 19.4% | 3263 | 21.1% | 410 | 22.9% |
Higher-middle SES | 23848 | 21.6% | 605 | 22.8% | 14373 | 24.6% | 1405 | 16.8% | 3314 | 14.1% | 3766 | 24.4% | 385 | 21.5% |
Highest SES | 22820 | 20.7% | 873 | 32.9% | 15224 | 26.1% | 804 | 9.6% | 1855 | 7.9% | 3732 | 24.2% | 332 | 18.5% |
Marital status | ||||||||||||||
Single or other | 47316 | 42.9% | 918 | 34.6% | 25200 | 43.2% | 5134 | 61.2% | 10120 | 43.0% | 4972 | 32.2% | 972 | 54.3% |
Married | 62876 | 57.1% | 1738 | 65.4% | 33175 | 56.8% | 3249 | 38.8% | 13419 | 57.0% | 10476 | 67.8% | 819 | 45.7% |
Tumor stage | ||||||||||||||
I | 28369 | 25.7% | 653 | 24.6% | 15630 | 26.8% | 1934 | 23.1% | 5551 | 23.6% | 3899 | 25.2% | 702 | 39.2% |
II | 26530 | 24.1% | 682 | 25.7% | 14308 | 24.5% | 1864 | 22.2% | 5781 | 24.6% | 3554 | 23.0% | 341 | 19.0% |
III | 29693 | 26.9% | 751 | 28.3% | 15116 | 25.9% | 2251 | 26.9% | 6552 | 27.8% | 4640 | 30.0% | 383 | 21.4% |
IV | 25600 | 23.2% | 570 | 21.5% | 13321 | 22.8% | 2334 | 27.8% | 5655 | 24.0% | 3355 | 21.7% | 365 | 20.4% |
Tumor grade or differentiation | ||||||||||||||
Grade I or well differentiated | 11403 | 10.3% | 234 | 8.8% | 6097 | 10.4% | 813 | 9.7% | 2553 | 10.8% | 1446 | 9.4% | 260 | 14.5% |
Grade II or moderately differentiated | 68342 | 62.0% | 1758 | 66.2% | 35588 | 61.0% | 5259 | 62.7% | 14731 | 62.6% | 9987 | 64.6% | 1019 | 56.9% |
Grade III or poorly differentiated | 16747 | 15.2% | 398 | 15.0% | 9274 | 15.9% | 1128 | 13.5% | 3453 | 14.7% | 2269 | 14.7% | 225 | 12.6% |
Grade IV or undifferentiated/anaplastic | 1897 | 1.7% | 37 | 1.4% | 1093 | 1.9% | 143 | 1.7% | 375 | 1.6% | 230 | 1.5% | 19 | 1.1% |
Grade/differentiation unknown | 11803 | 10.7% | 229 | 8.6% | 6323 | 10.8% | 1040 | 12.4% | 2427 | 10.3% | 1516 | 9.8% | 268 | 15.0% |
NCCN-concordant treatment | ||||||||||||||
No | 31855 | 28.9% | 751 | 28.3% | 16608 | 28.5% | 2601 | 31.0% | 6876 | 29.2% | 4511 | 29.2% | 508 | 28.4% |
Yes | 78337 | 71.1% | 1905 | 71.7% | 41767 | 71.5% | 5782 | 69.0% | 16663 | 70.8% | 10937 | 70.8% | 1283 | 71.6% |
MENA = Middle Eastern and North African, FFS = fee-for-service, VA = Veterans Affairs, NOS = not otherwise specified, SES = socioeconomic status, NCCN = National Comprehensive Cancer Network
Inclusive of Pacific Islander and American Indian or Alaska Native
Managed care includes private insurance (Managed Care Organization, Health Maintenance Organization [HMO], or Preferred Provider Organization [PPO]), Medicare (administered through a managed care plan), Medicaid (administered through a managed care plan), and HMO
Individuals with missing data were excluded unless otherwise noted in the table
As shown in Figure 1, five-year CRC-specific survival was lowest in Black (61.0% ± SE 0.6%) and highest in highest in MENA (73.2% ± SE 1.0%) individuals. Asian (72.2% ± SE 0.4%) individuals had higher survival compared to White (70.0% ± SE 0.2%) and Hispanic (68.2% ± SE 0.4%) individuals (p<0.01). For stage I – III cancers, survival remained lowest for Black (79.3% ± SE 0.6%) and highest for MENA (87.3% ± SE 0.9%) individuals (p<0.01) (Figure 2A). For stage IV cancers, survival was lowest for Black (10.5% ± SE 0.8%) and highest in Asian (18.3% ± SE 0.9%) individuals (p<0.01) (Figure 2B).
Figure 1.
Five-year colorectal cancer-specific survival (age 18–79 years) using Kaplan-Meier estimates, by race/ethnicity, California Cancer Registry, 2004 – 2017
Figure 2.
Kaplan-Meier curves showing five-year colorectal cancer-specific survival (age 18–79 years) for A) stage I – III, and B) stage IV cancer, by race/ethnicity, California Cancer Registry, 2004 – 2017a
aMENA = Middle Eastern and North African
Table 2 shows adjusted hazard ratios demonstrating the association of race/ethnicity and CRC-specific and overall survival, adjusting for age at diagnosis, year of diagnosis, sex, insurance, census tract-level SES, marital status, tumor site (colon versus rectum), stage at diagnosis, tumor grade or differentiation, and receipt of NCCN-concordant treatment. In adjusted analysis, MENA (aHR 0.82, 95% CI 0.76, 0.89), Asian (aHR 0.86, 95% CI 0.83, 0.90), and Hispanic (aHR 0.94, 95% CI 0.91, 0.97) race/ethnicity were associated with higher CRC-specific survival compared to White race/ethnicity, and Black (aHR 1.13, 95% CI 1.09, 1.18) race/ethnicity was associated with lower CRC-specific survival compared to White race/ethnicity. A similar pattern was observed for overall survival (Table 2).
Table 2.
Adjusted hazard ratios demonstrating association of race/ethnicity and survival (overall and colorectal cancer-specific, n=110,192), California Cancer Registry, 2004 – 2017a
Overall Survival | Colorectal Cancer-specific Survival | |||||||
---|---|---|---|---|---|---|---|---|
Adjusted HR and 95% CI | p-value | Adjusted HR and 95% CI | p-value | |||||
Age at diagnosis | 1.03 | 1.03 | 1.03 | <0.01 | 1.02 | 1.01 | 1.02 | <0.01 |
Year of diagnosis | 1.02 | 1.02 | 1.02 | <0.01 | 1.00 | 1.00 | 1.00 | 0.71 |
Female | 0.84 | 0.82 | 0.86 | <0.01 | 0.90 | 0.88 | 0.92 | <0.01 |
Race/ethnicity | ||||||||
Middle Eastern/North African | 0.80 | 0.74 | 0.85 | <0.01 | 0.82 | 0.76 | 0.89 | <0.01 |
Non-Hispanic White | Ref | Ref | ||||||
Non-Hispanic Black | 1.11 | 1.07 | 1.15 | <0.01 | 1.13 | 1.09 | 1.18 | <0.01 |
Hispanic | 0.92 | 0.90 | 0.95 | <0.01 | 0.94 | 0.91 | 0.97 | <0.01 |
Non-Hispanic Asian | 0.83 | 0.80 | 0.85 | <0.01 | 0.86 | 0.83 | 0.90 | <0.01 |
Insurance | ||||||||
Managed careb | Ref | Ref | ||||||
Medicare | 1.11 | 1.09 | 1.14 | <0.01 | 1.05 | 1.01 | 1.08 | <0.01 |
Medicaid | 1.33 | 1.28 | 1.38 | <0.01 | 1.28 | 1.23 | 1.33 | <0.01 |
Other (FFS, Tricare, VA, or NOS) | 0.90 | 0.87 | 0.93 | <0.01 | 0.92 | 0.89 | 0.96 | <0.01 |
Not insured or unknown | 1.21 | 1.15 | 1.27 | <0.01 | 1.27 | 1.20 | 1.34 | <0.01 |
Socioeconomic Status | ||||||||
Lowest SES | 1.34 | 1.30 | 1.39 | <0.01 | 1.26 | 1.20 | 1.31 | <0.01 |
Lower-middle SES | 1.29 | 1.25 | 1.33 | <0.01 | 1.23 | 1.18 | 1.28 | <0.01 |
Middle SES | 1.19 | 1.15 | 1.23 | <0.01 | 1.17 | 1.12 | 1.21 | <0.01 |
Higher-middle SES | 1.13 | 1.09 | 1.16 | <0.01 | 1.08 | 1.04 | 1.13 | <0.01 |
Highest SES | Ref | Ref | ||||||
Marital status | ||||||||
Single or other | Ref | Ref | ||||||
Married | 0.79 | 0.78 | 0.81 | <0.01 | 0.83 | 0.81 | 0.85 | <0.01 |
Tumor site | ||||||||
Colon | Ref | Ref | ||||||
Rectum | 0.94 | 0.92 | 0.96 | <0.01 | 1.02 | 0.99 | 1.05 | 0.19 |
Tumor stage | ||||||||
I | Ref | Ref | ||||||
II | 1.65 | 1.59 | 1.71 | <.0001 | 2.84 | 2.66 | 3.03 | <.0001 |
III | 2.07 | 2.00 | 2.15 | <.0001 | 4.82 | 4.54 | 5.12 | <.0001 |
IV | 11.42 | 11.05 | 11.80 | <.0001 | 31.09 | 29.35 | 32.93 | <.0001 |
Tumor grade or differentiation | ||||||||
Grade I or well differentiated | Ref | Ref | ||||||
Grade II or moderately differentiated | 1.20 | 1.15 | 1.25 | <.0001 | 1.38 | 1.30 | 1.46 | <.0001 |
Grade III or poorly differentiated | 1.73 | 1.65 | 1.81 | <.0001 | 2.16 | 2.04 | 2.30 | <.0001 |
Grade IV or undifferentiated/anaplastic | 1.88 | 1.74 | 2.03 | <.0001 | 2.31 | 2.10 | 2.55 | <.0001 |
Grade/differentiation unknown | 1.94 | 1.85 | 2.03 | <.0001 | 2.23 | 2.09 | 2.37 | <.0001 |
NCCN-concordant treatment | ||||||||
No | 1.69 | 1.65 | 1.73 | <.0001 | 1.77 | 1.73 | 1.82 | <.0001 |
Yes | Ref | Ref |
FFS = fee-for-service, VA = Veterans Affairs, NOS = not otherwise specified, SES = socioeconomic status, NCCN = National Comprehensive Cancer Network
Managed care includes private insurance (Managed Care Organization, Health Maintenance Organization [HMO], or Preferred Provider Organization [PPO]), Medicare (administered through a managed care plan), Medicaid (administered through a managed care plan), and HMO
Discussion
Our study demonstrates higher CRC-specific and overall survival in MENA individuals newly diagnosed with CRC compared to other racial/ethnic groups, even after adjusting for clinical and sociodemographic factors. Survival was lowest in Black individuals, and Asian individuals had higher survival compared to White and Hispanic individuals. To our knowledge, this study is the first of its kind to use population-based data to estimate survival in MENA individuals diagnosed with CRC in the U.S. and highlights the importance of disaggregating racial and ethnic data in cancer epidemiology.
Reasons for the higher survival of MENA individuals compared to other racial/ethnic groups are likely complex and related to socioeconomic status and residence in ethnic enclaves; immigration and acculturation; and resultant preventive behaviors, including CRC screening and observance of the Mediterranean diet. First, about one-third of MENA individuals in our study lived in high SES neighborhoods, and a large literature demonstrates neighborhood-level SES contributes to outcomes across the cancer continuum.(13) Nearly two-thirds of MENA individuals in the U.S. live in ethnic enclaves,(14) and in California, these include Little Arabia in Anaheim,(15) El Cajon near San Diego,(16) and parts of the San Francisco Bay Area.(17) Like neighborhood-level SES, ethnic enclaves contribute to cancer outcomes via pathways including cultural norms (e.g., social support,(18–23) religion), communication, information sharing, access to linguistic resources, and fewer experiences of discrimination;(24) these phenomena have been well-described in Hispanic and Asian populations.(23, 25, 26) MENA individuals living in ethnic enclaves in California are also in close proximity to large medical centers and specialized cancer centers in nearby Los Angeles, San Diego, and San Francisco, which may facilitate access to and timeliness of cancer treatment.(27, 28)
Second, the immigrant health paradox – or the notion that first-generation immigrants to the U.S. comprise selected, healthier individuals compared to both their native populations and second- and third-generation immigrants – may also contribute to better survival of MENA individuals diagnosed with CRC.(29) This paradox has been observed among immigrants from Latin America and Asia, but there has been less research on MENA immigrants. About 65% of the MENA population in the U.S. is foreign-born,(30) and limited data from cross-sectional surveys suggest prevalence of chronic conditions (e.g., heart disease, diabetes) is lower among foreign-born Arab American compared to foreign-born European Americans and U.S.-born White persons,(31, 32) consistent with the immigrant health paradox. Others suggest that these health outcomes are similar among first-, second-, and third-generation Arab Americans in California,(33) and longer time in the U.S. does not contribute to declines in outcomes as it does for other immigrant communities. We did not include birthplace in our study because a large proportion of observations were missing these data (52%), and thus we could not examine associations with recency of immigration and acculturation-related factors on CRC-specific survival.
Third, prevalence of preventive behaviors in MENA individuals, including CRC screening and observance of the Mediterranean diet, may explain our findings. Prevalence of CRC screening may be higher in MENA individuals, thereby contributing to improved survival and consistent with our observation that a smaller proportion were diagnosed with stage IV disease. National surveys do not separate MENA from White individuals, and our study underscores the importance of population-based estimates of screening in this population. A recent cross-sectional survey in Michigan reported lower prevalence of CRC and cervical cancer screening in MENA compared to White women,(34) although results were limited by the small number (n=37) of MENA women participating in the survey. Similarly, the Mediterranean diet is the traditional diet of many MENA individuals, and higher observance of this diet has been associated with reductions in chronic conditions and other adverse health outcomes.(35–38) Ten MENA countries (e.g., Algeria, Egypt, Lebanon) border the Mediterranean Sea, although the culinary traditions may vary within and across these countries. Immigration and acculturation, not captured in our study and as described above, may also impact these preventive behaviors in distinct and complementary ways.
Beyond the higher survival we observed among MENA individuals, CRC-specific survival was lowest for Black followed by Hispanic individuals, and although higher proportions lived in lower SES neighborhoods and had more stage IV diagnoses compared to other racial/ethnic groups, differences remained in models adjusted for these factors. Our findings are consistent with prior studies demonstrating lowest survival in Black individuals.(39–45) Studies on Hispanic-White differences report varying results, depending on the age groups, time periods, and populations examined. For example, a recent study reported lower five-year relative survival of Hispanic individuals newly diagnosed with CRC at age 20–49 compared to White individuals.(46) Others have reported no difference between the two groups.(41, 44, 47) We also observed higher CRC-specific survival among Asian compared to White individuals in our study. The literature on CRC survival in Asian populations is limited, with some reporting lower survival in early-onset patients(46) and other studies reporting higher survival in older adults.(41, 44) A host of clinical and sociodemographic factors contribute to disparities in CRC survival, including differences in pre-existing chronic conditions,(48–50) screening participation,(51, 52) stage at diagnosis,(51) treatment,(27, 53) SES,(27) access to healthcare,(54) trust in the healthcare system,(55, 56) language proficiency,(57) and culture.(55, 58, 59) These are described in detail elsewhere.(51, 60)
An important strength of our study is the large and diverse (45% Black, Asian, Hispanic, or MENA) population-based sample derived from the CCR, along with pertinent demographic and clinical information, including insurance, census tract-level SES, cancer stage, tumor grade or differentiation, and receipt of NCCN-concordant treatment. Despite its strengths, there were several limitations. The algorithm used to identify MENA individuals uses a list of common MENA surnames and is less sensitive for women, likely due to differences in maiden versus married names. We note that women had better CRC-specific and overall survival compared to men, and survival of Asian, Black, Hispanic, and White individuals was worse than MENA individuals; therefore, misclassification of MENA women as another race/ethnicity is unlikely to impact overall findings. We used race/ethnicity as a proxy for social constructs, which may not fully encompass the range of social determinants of health. Population-based cancer registries, including the CCR, are often missing information on birthplace, and missingness also differs by vital status.(61–63) For example, in the Greater Bay Area Cancer Registry, 67% of persons have birthplace recorded, but deceased individuals are 10 times more likely to have birthplace recorded than living individuals.(62) Similarly, persons missing information on treatment (5.1%) were not included in our study. Future studies should consider linkage with electronic health records, population-based surveys, and other sources of clinical data to obtain additional information on covariates and improve data completeness. Lastly, our analysis was limited to California, and although California is home to the largest MENA population in the U.S., survival may differ relative to other states.(64)
In summary, our findings add to the literature on racial/ethnic disparities in CRC by demonstrating higher CRC-specific and overall survival of MENA individuals in California newly diagnosed with CRC compared to other racial/ethnic groups. While neighborhood-level SES, residence in ethnic enclaves and corresponding effects of immigration and acculturation, and preventive behaviors of MENA individuals may, in part, confer a survival benefit, future studies are needed to identify factors contributing to cancer outcomes in this unique population.
Supplementary Material
Acknowledgments
The authors declare no acknowledgements for this study.
Grant support:
C. Murphy is supported by the National Cancer Institute at the National Institutes of Health under award number R01CA242558. The sponsor had no role in: design and conduct of the study; collection, management, analysis, and interpretation of the data; preparation, review, or approval of the manuscript; and decision to submit the manuscript for publication.
Footnotes
Disclosures: CCM reports consulting for Freenome. The remainder of authors report no relevant financial disclosures.
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