Assessment of Colorectal Cancer Screening Disparities in U.S. Men and Women Using a Demographically Representative Sample

Timely receipt of colorectal cancer screening can reduce morbidity and mortality. This is the first known study to adopt Andersen's model of health services use to identify factors associated with colorectal cancer screening among U.S. adults. The data from National Health Interview Survey from 2019 was utilized to conduct the analyses. Multivariable logistic regression was used to separately analyze data from 7,503 age-eligible women and 6,486 age-eligible men. We found similar colorectal cancer screening levels among men (57.7%) and women (57.6%). Factors associated with higher screening odds in women were older age, married/cohabitating with a partner, Black race, >bachelor's degree, having a usual source of care, and personal cancer history. Factors associated with lower odds for women were American Indian/Alaska Native race, living in the United States for ≤10 years, ≤138% federal poverty level (FPL), uninsured or having Medicare, and in fair/poor health. For men, factors associated with higher screening odds were older age, homosexuality, married/cohabitating with a partner, Black race, >high school/general educational development education, having military insurance, having a usual source of care, and personal cancer history. Factors associated with lower odds for men were being a foreign-born U.S. resident, living in the South or Midwest, ≤138% FPL, and being uninsured or having other insurance. Despite lower screening rates in the past, Black adults show a significantly higher likelihood of colorectal cancer screening than White adults; yet, screening disparities remain in certain other groups. Colorectal cancer screening efforts should continue to target groups with lower screening rates to eliminate screening disparities. Significance: Timely receipt of colorectal cancer screening can reduce morbidity and mortality. Identification of populations and domains of factors associated with colorectal cancer screening receipt among men and women can help future interventions to alleviate impeding factors and target screening promotion efforts in populations not adherent with screening guidelines.


Introduction
Cancer screenings help identify cancers early and mitigate cancer-associated morbidity and mortality and the growing financial burden of cancer treatment (1). Colorectal cancer is the second most common cancer in men and women in the United States (2). Screening for colorectal cancer can detect precancerous polyps and cancerous lesions in early stages which can be treated comprehensive Andersen's model of health services (Andersen's model) use using a national representative sample. This study was undertaken to fill these gaps in the literature and to contribute to scientific knowledge of colorectal cancer screening by examining variations in screening receipt using a nationally representative dataset, the NHIS (10).
The Andersen's model categorizes factors affecting service use into three domains: "predisposing," "enabling," and "need" factors (11). Predisposing factors are sociodemographic characteristics (e.g., age, sex, race/ethnicity, education level, country of birth) related to service use. Enabling factors are resources that facilitate service use if they are available (e.g., health insurance, transportation). Need factors are real and perceived health conditions that may warrant service use (e.g., medical history, health status; refs. 11,12). Identification of individual and domains of factors associated with colorectal cancer screening among men and women can inform interventions to target those who are not adherent with screening guidelines.

Data Source
The study used data from the 2019 NHIS. The NHIS is conducted annually by the National Center for Health Statistics to monitor the health of the U.S. population on a broad range of health topics by surveying a representative random sample of the U.S. civilian noninstitutionalized population. Data are collected through personally interviewing one adult from each household randomly selected to answer detailed questions about their demographic information and health. More information about the NHIS can be found elsewhere (13).

Study Population
There were 15,989 respondents to the 2019 NHIS who were age-eligible (50-75 years) for USPSTF colorectal cancer screening. As the focus of the study was on routine colorectal cancer screening, respondents who reported colorectal cancer screening for reasons other than a routine examination were excluded from the study population (n = 1,876), resulting in a final analytic sample of 13,989 (women = 7,503, men = 6,486).

Outcome
Being up-to-date with colorectal cancer screening was defined as receiving a recommended screening test at specified intervals as per the USPSTF guidelines (see Table 1). The tests recommended are: High-sensitivity guaiac fecal occult blood test (gFOBT), fecal immunochemical test (FIT), stool DNA test with FIT (sDNA-FIT), CT/virtual colonography, flexible sigmoidoscopy, flexible sigmoidoscopy with FIT, and colonoscopy. The NHIS questionnaire asked respondents to indicate whether they had received any of those tests, the time since they last received the test, and whether the screening was part of a routine examination. Respondents were coded as having had a recommended colorectal cancer screening if they had had one of those recommended screening tests within the recommended frequency for the test as part of a routine examination. Respondents were coded as not having a recommended colorectal cancer screening if they had not had one of the tests or had had one test but outside the USPSTF recommended frequency. Response options "Refused," "Not ascertained," and "Don't know" were coded as missing. Factors representing the Andersen's model three domains were selected for the analysis based on previous research (14,15). The operational definitions of the variables are shown in Supplementary Table S1.

Predisposing Factors
Age, sexual orientation, race/ethnicity, education, marital status, nativity, urban-rural residence classification, and region of residence.

Enabling Factors
Employment status in past 12 months, income level, health insurance coverage, problems paying medical bills in past 12 months, worry about paying medical bills if sick/in an accident, usual source of medical care, and number of children in household.

Needs Factors
Perceived health status, personal history of cancer, and body mass index (BMI) categories.

Statistical Analysis
We computed weighted percentages and weighted 95% confidence intervals (CI) for categorical variables and weighted means and SEs for continuous variables to describe age-eligible adults by sex who were up-to-date with USPSTF colorectal cancer screening.
In separate multivariable logistic regression models for men and women, we estimated the association between colorectal cancer screening and the selected predisposing, enabling, and need factors. The magnitude and direction of the associations were captured by odds ratios (ORs), and the uncertainty around the estimates were captured by 95% CIs.
Multicollinearity among independent variables was assessed by computing the variance inflation factor. Statistical significance was determined at an a priori α = 0.05. The complex design of the survey was accounted for with sampling adult weights and other design variables. All descriptive and regression analyses were conducted with STATA/SE 16 (16).

Data Availability
The data analyzed in this study were obtained from the National Center for Health Statistics NHIS at https://www.cdc.gov/nchs/nhis/2019nhis.htm.

Colorectal Cancer Screening
Within the study population, 57.6% of women and 57.7% of men received routine colorectal cancer screening as recommended by USPSTF guidelines.

Characteristics of Age-Eligible Women and Men Who Received a Colorectal Cancer Screening
Results of the analyses to profile women and men up-to-date with colorectal cancer screening based on the predisposing, enabling, and need factors are described below and also in Supplementary

Adjusted Associations Between Predisposing, Enabling, and Need Factors and Colorectal Cancer Screening Among Age-Eligible Women and Men
Adjusted associations between predisposing, enabling, and need factors and colorectal cancer screening from sex-specific multivariable logistic regression analyses are reported below, in Table 2, and in Figures 1 and 2    Enabling Factors: The odds of having colorectal cancer screening for men at ≤138% FPL, at >138%-250% FPL, and at >250%-400% FPL were lesser (ORs:0.59, 0.71, 0.79, respectively; P < 0.001, <0.01, <0.05, respectively) than the odds for men at >400% FPL. The odds of having colorectal cancer screen-ing for uninsured men and men with other types of health insurance were lesser than the odds for men with private insurance (OR:0.45, P < 0.005; and 0.76, P = 0.020). In contrast, the odds of having colorectal cancer screening for men with military insurance was 1.74 times the odds for men with private insurance (P = 0.010). The odds of having colorectal cancer screening for men who had a usual source of care at a doctor's office were 4.67 times the odds for men without a usual source of care (P < 0.001). For those who had a usual source of care at other medical facilities, their odds of receiving colorectal cancer were 3.48 times the odds of those without a usual source of care (P < 0.001).

Need Factors:
The odds of having colorectal cancer screening for men with a history of cancer diagnosis were 1.30 times the odds for men without a history of cancer diagnosis (P = 0.014). See Table 2 and Figures 1 and 2.

Discussion
Using the Andersen's model as a comprehensive conceptual framework, this study showed receipt of guideline concordant colorectal cancer screenings was associated with several predisposing, enabling, and need factors. While some factors were common for both women and men, other factors were unique to each sex. Interestingly, our analyses reveal Black respondents exhibited significantly higher odds of colorectal cancer screening receipt compared to White respondents. To the best of our knowledge, this is the first study to show significantly higher odds of colorectal cancer screening among Black adults as compared to White adults in a nationally representative sample. Black adults have historically had lower colorectal cancer screening levels than White adults (17), but this disparity has been decreasing in recent years (17,18). Our findings suggest that targeted efforts toward modifying enabling factors to increase access (19,20) and insurance coverage for Black adults (21,22) may have been successful in improving colorectal cancer screening uptake.
Factors associated with significantly higher odds of colorectal cancer screening uptake for both sexes were: age, being married/cohabitating with a partner, educational attainment higher than a bachelor's degree, having a usual source of care, and having a personal history of cancer. These associations are consistent with the past literature (5,6,(23)(24)(25)(26)(27). As the risk of colorectal cancer increases with age, so does colorectal cancer screening knowledge and awareness (5,23,24). Prior research suggests that being married/cohabitating with a partner provides social support and promotes preventive health seeking behaviors (25,28).
Higher educational attainment and engagement in preventive health behaviors have a well-established association (5,6,24). We also find that having an estab-lished source of care and personal history of cancer increases health care visits which can promote cancer screening uptake (6,26,27). Research suggests having insurance coverage leads to having a usual source of care (26,27) which in turn promotes the use of preventive health care services (21,29,30). Conversely, factors correlated with significantly lower odds of colorectal cancer screening uptake in both sexes were: being born outside the United States and living in the United States for ≤10 years, poverty ≤138% FPL, and lack of insurance coverage. These factors are consistent with prior literature, as lack of insurance coverage is often associated with lower cancer screening uptake due to access and financial barriers (6,23 (7).
Men living in the South and Midwest had lower odds of receiving colorectal cancer screening, and it is not clear why men from these two U.S. regions are less likely to be screened. Colorectal cancer mortality rates are higher in these regions compared to other U.S. regions (38). Additional research is needed to identify regional cultures or other factors that may affect the willingness of men from these regions to follow colorectal cancer screening recommendations.
Our findings showed there are differences between women and men in the predicting factors that facilitate or constrain colorectal cancer screening. Efforts to improve colorectal cancer screening can be informed by these results, which could be used to guide sex-specific outreach and education interventions. Creating targeted educational materials for women and for men, separately, may generate gains in overall colorectal cancer screenings in the United States. Future research should develop and test colorectal cancer screening information and education based on factors that specifically facilitate or constrain colorectal cancer screenings for women and for men.

Limitations and Strengths
Survey-based studies are susceptible to some inherent limitations. The data were self-reported and may be subject to recall bias and/or response bias. Moreover, the cross-sectional data did not allow us to examine long-term adherence to colorectal cancer screening and did not report the proportion of participants receiving different screening methods. Nevertheless, this study used a large, nationally representative sample to examine colorectal cancer screening among U.S. women and men. This is the first study to apply Andersen's model to exam-ine how predisposing, enabling, and need domains may affect colorectal cancer screening uptake among women and men separately; in doing so, the study provides a more complete examination of the factors that may influence colorectal cancer screenings by simultaneously examining factors from the model's three domains.

Conclusion
Encouragingly, this study showed higher odds of colorectal cancer screening receipt among the Black population in a nationally representative sample.
However, the overall colorectal cancer screenings among women and men remain lower than national colorectal cancer screening goals, and disparities among certain populations still exist. Continued monitoring of colorectal cancer screenings may help inform and focus efforts toward alleviating colorectal cancer disparities among the most socially and medically vulnerable populations.