Introduction

Colorectal cancer is the third most common cancer in men and women in the United States and the second leading cause of cancer death1. American Indian Alaska Native (AI/AN) individuals and Non-Hispanic Black individuals, herein referred to as Black, have the highest colorectal cancer incidence and mortality rates among men and women combined1. For every 100 colorectal cancer deaths in Non-Hispanic White individuals, herein referred to as White, there are 132 colorectal cancer deaths among Black individuals2,3. Disparities in colorectal cancer mortality have also been noted in US-born Hispanic men, compared to non-Hispanic White men4.

Screening is a crucial tool to reduce colorectal cancer incidence and mortality1,5,6. Federally qualified community health centers (CHCs) serve a large proportion of racial and ethnic minority patients, which places them in a prime position to address disparities in colorectal cancer screening. However, lower screening rates are seen at CHCs compared to the general population, with screening rates at 41.9% compared to 69.7% for the general population7. Lower colorectal cancer screening rates at CHCs result from multilevel barriers including limited funding, resource limitations, staffing constraints, competing priorities of CHCs and their patients, and others5,8,9,10.

Epidemiologic studies have shown an increasing incidence of colorectal cancer in those age 45 to 54 in the past decade and a declining incidence for those over 5511. In response to the increase in incidence of colorectal cancer in younger individuals, the United States Preventive Task Force (USPSTF) revised the colorectal cancer screening guidelines in 2021 with a grade B recommendation for screening initiation at age 4512. With regular colorectal cancer screening, the years of potential life lost from colorectal cancer are lowest when screening is initiated by ages 45 to 5013. In addition, targeting screening in younger individuals may promote increased uptake of this key preventive behavior and lifelong screening habits14,15.

Colorectal cancer screening is lifesaving and of critical importance to mitigate colorectal cancer incidence and mortality, and thus the revised USPSTF screening recommendations are key to colorectal cancer prevention and early detection in younger individuals. However, it must be recognized that the revision in screening recommendations expanded the population eligible for colorectal cancer screening, which presents a challenge to public health and health care organizations alike to develop strategies to rapidly integrate this population into the colorectal cancer screening landscape. CHCs may be especially impacted by the expansion of the screening-eligible population as they already underfunded and face a multitude of barriers to colorectal cancer screening. The primary objective of our study is to estimate the percentage increase in overall colorectal cancer screenings needed to screen individuals 45 to 49 after the revision in the USPSTF screening guidelines and assess colorectal cancer screening rates one year after the revision across 10 federally-qualified CHCs in Massachusetts that were part of a cancer equity-focused implementation science network. The median baseline colorectal cancer screening rate across our 10 partner CHCs was 50.4% (31.1 − 73.8%) in 2019. A secondary objective of the work was to assess the additional screenings needed to reach the Uniformed Data Systems (UDS) benchmark of 68.3% by different demographic factors. Our sample of CHCs are located across Massachusetts and are distinct in size, demographics of their patient population, and internal characteristics (staffing, resources). The variability amongst the participating CHCs allows for generalizability of findings to health centers that serve a variety of patient populations with diverse needs to better understand and address screening needs of CHCs more broadly.

Methods

Study population

Data was collected from 08/01/2020 to 07/31/2022 to account for a baseline estimate and screening one year following guideline announcement. Patients were included if they were eligible for screening at any point in the time period. Adults who were patients at the CHCs, who were age 45 to 75, and had a UDS qualifying primary care visit in the last 2 years were included in our study. Exclusion criteria included a personal history of colorectal cancer or adenomatous polyps, history of inflammatory bowel disease, and family history of colorectal cancer.

Measures

Colorectal cancer screening was defined as being up to date vs. not up to date based on any of the approved screening modalities. A patient was considered up to date if they had a colonoscopy within the last 10 years, sigmoidoscopy within the last 5 years, or a fecal test in the recommended time-window for the specific test (e.g. 1 year for fecal immunochemical test [FIT], 3 years for FIT-DNA). Patients were coded as not up to date if they had not completed a colorectal cancer screening in the recommended timeframe by one of the modalities listed above. Patient demographic characteristics include age, race/ethnicity, and preferred language. Age was categorized into 45–49, 50–54, and 55 and over; race/ethnicity was classified as non-Hispanic White, non-Hispanic Black/African American, Latino or Hispanic (of any race), non-Hispanic Asian, and non-Hispanic Other. Language was coded as English, Spanish, Portuguese, and Other.

Data source and extraction.

All data were extracted from electronic health records. Nine CHC’s EHRs were connected to Azara Healthcare’s Data Reporting and Visualization System (DRVS), a population health management and quality improvement platform. DRVS is a vendor neutral platform that is connected to EHR systems and extracts patient demographic and clinical data for analysis and reporting purposes. One CHC was not linked to DRVS, their data was extracted directly from the EHR and harmonized to the DRVS data prior to analysis. After data extraction, summary data for screening and demographic characteristics were reviewed by the investigator team and a clinician at the respective CHCs to identify and, if necessary, correct any suspect or out of range values.

Statistical analysis.

Patient characteristics were summarized with absolute and relative frequencies. Colorectal cancer screening rates were characterized by calculating the proportion screened overall across and within CHCs, and by patient demographic characteristics. We used generalized linear models to estimate the marginal screening rates by demographic subgroups controlling for CHC. Statistical significance was tested with a likelihood ratio Chi-square statistic with α = 0.05 as the threshold. Lastly, we calculated the total number screened and the number of additional screenings needed to meet the Uniformed Data Systems (UDS) benchmark for colorectal cancer screening (68.3%) overall and by age group. All data processing and analyses were implemented in R statistical programming software.

Ethics & inclusion.

All methods were carried out in accordance with relevant guidelines and regulations.

All experimental protocols were approved by the Dana Farber Cancer Center IRB (22–167). Informed consent was obtained from all subjects and/or their legal guardian(s).

Results

There were 70,808 patients across 10 health centers in 2022 that were included in the analysis. Approximately 18.6% (n = 13,192) were age 45 to 49, 19.2% (n = 13,595) were 50 to 54, and 62.2% (n = 44,021) were 55 to 75. The median age was 58 years old. The study population was predominantly non-White (Black 29.6%, n = 19,528; Hispanic 19.1%, n = 12,575; Asian 13.7%, n = 9023, non-Hispanic White 35.9%, n = 23,715). Approximately 42% of patients spoke a language other than English (n = 29,763) [Table 1].

Table 1 Demographics of the Study Population.
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There were 13,192 additional individuals who became eligible for screening under the new guideline (range across CHCs: 260 to 2283), or a 22.9% increase in colorectal cancer screenings needed across the 10 health centers. The overall colorectal cancer screening rate across all 10 health centers and all age groups was 35.9% (range: 26.4–46.4%) in 2022 after the USPSTF guideline revision. The lowest marginal screening rate across the 10 health centers was among 45 to 49 year olds (9.6%, 95% CI: 9.1 − 10.1%), and the second lowest among 50 to 54 year olds (24.2%, 95% CI: 23.4 − 24.9%). Those age 55 to 75 had higher marginal screening rates compared to the other two younger age groups at 47.0% (95% CI: 46.6 − 47.5%) [Table 2] (X2(df=2) = 7924.6, P < 0.001).

Table 2 Colorectal cancer screening across 10 health centers by age group, race/ethnicity, and language.
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Figure 1
figure 1

(panel A through D).

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Screening rates overall were highest among those who were Black (38.5%) and Asian (39.2%), and significantly lower among those who were White (35.1%), Hispanic (34.8%), or reporting another race (27.8%) (X2(df=5) = 109.68, P = < 0.001) [Table 2]. Screening rates were similar among those speaking English (35.7%), Spanish (35.9%) and other languages (36.1%), and significantly lower among those speaking Portuguese (31.5%) (X2(df=3) = 30.235, P = < 0.001). Males had significantly lower screening rates than females (Males 34.8%, Females 36.2%)(X2(df=1) = 14.591, P = < 0.001) [Table 2].

We also assessed the additional number of screenings needed by age and other demographic factors to reach the UDS quality benchmark for colorectal cancer screening of 68.3%1. There were an estimated 7706 additional screenings needed to reach UDS quality benchmarks for those 45 to 49 years of age, 5922 for those age 50 to 54, and 9312 needed for those 55 and older [Fig. 1]. Across race and ethnicity, we estimated an additional 5688 screenings would be needed for those who are Black, 7791 for White, 4244 for Hispanic or Latino, and 2588 and Asian to reach the UDS quality benchmark [Fig. 1]. Similarly, by language, we estimated an additional 2565 screenings would be needed to reach that quality benchmark for Spanish speaking patients, 13,006 for English speaking patients, 1785 for Portuguese speaking patients, and 5584 for patients speaking other languages. [Figure 1].

Discussion

In our study assessing the impact of the revised USPSTF screening guidelines on screening burden across 10 health centers, we found that the inclusion of the 45 to 49 year old age group resulted in an approximate 22.9% increase in patients eligible for screening at the participating CHCs. Individuals 45 to 54 had the lowest screening rates across all 10 health centers, while those over 55 had the highest screening rates. Similarly, individuals 45 to 49 had the largest proportion of screenings needed, relative to their population size, to reach the UDS quality benchmark for colorectal cancer screening. In addition, Hispanic and White individuals had the lowest screening rates, whereas Asian and Black individuals had the highest rates. No differences in screening were found between English and Spanish speakers, but Portuguese-speaking individuals had significantly lower screening rates.

The revised USPSTF screening guidelines lowered the screening age for colorectal cancer to address the rising incidence in younger individuals, yet as a result, FQHCs are now faced with an increase in the number of individuals to be screened without a corresponding increase in resources (i.e. CHC funding for additional outreach staff to engage younger patients in screening and follow-up of abnormal results). The mismatch between the increased number of individuals to be screened and limited resources could stand to worsen screening rates at CHCs who already face a multitude of barriers to screening. Currently $1 billion dollars of CHC funding comes from patient-related revenues (57.2% from Medicaid, 15.7% from Medicare, 21.3% from private insurers) while $800 million is from other revenue sources (~ 26.8% are federal grants)16. Increased funding through federal grants, higher reimbursement from insurers, or financial incentives from insurers targeted at colorectal cancer screening rates could be beneficial to assist CHCs in Massachusetts to increase colorectal cancer screening rates. Additional funding would allow CHCs to hire additional staff (i.e. patient navigators or community health workers) or purchase additional colorectal cancer screening materials such as FIT kits. Nevertheless, there are also factors that contribute to screening rates at our CHCs in Massachusetts that would not be resolved with additional funding alone, including staff turnover and the need to re-train staff, leaning mainly on colonoscopy for screening and not taking advantage of FIT to broaden uptake, electronic health record conversions, and limited access to GI providers for colonoscopy to name a few. Still, some CHCs have partnered with organizations such as the Centers for Disease Control and Prevention, the National Colorectal Cancer Roundtable, state and local health departments, and advocacy organizations to implement CRC screening programs and partially offset resource constraints. For example, the Massachusetts League of Community Health Centers, with support from the Massachusetts Department of Public Health and funding from the Centers for Disease Control and Prevention, offers a CRC learning collaborative for CHCs. This learning collaborative, and others like it have been developed to spread knowledge about CRC screening, provide a forum for CHCs to learn from each other about strategies that have been successful around CRC screening at their specific CHC, and provide implementation support for strategies to increase colorectal cancer screening at CHCs across the state.

Nationally, Black men and women have the second highest incidence and mortality from colorectal cancer, with mortality rates that are approximately 44% and 31% higher than White men and women respectively11,17. Within Massachusetts, similar trends are also noted3,18. In Massachusetts, racial and ethnic minorities comprise 31.3% of the general population and 68.3% of the CHC population19. In addition, 89% of CHC patients are at or below 200% of the federal poverty level19. Thus, addressing CRC screening rates in CHCs stands to have a large impact on racial, ethnic, and socioeconomic disparities in the state. Interestingly, in our study there were overall small but statistically significant screening differences across race and ethnicity, with the second highest colorectal cancer screening rates in Black individuals and lower screening rates in White individuals. These findings are similar to what has been shown in other studies of CHC patients. A study by Lee and colleagues noted that among approximately 17 million patients at CHCs across the United States, Black and Hispanic patients had higher odds of receiving cervical cancer and breast cancer screening compared to White patients, and Black patients had higher odds of colorectal cancer screening compared to White patients20. These findings may reflect the efforts of CHCs to address inequities in colorectal cancer among their Black patients, particularly given the high colorectal cancer incidence and mortality rates in this group. Further, given their patient population, CHCs practice with health equity at the forefront, which was reflected in higher screening rates for Black patients and Spanish speakers in our study. However, as the volume of those eligible for screening increases it will be important to maintain the focus on equity while also working to close screening gaps across age groups.

In our study we also found lower screening rates in patients who spoke Portuguese but similar rates between English speakers, Spanish speakers, and those whose language was “other.” Across the participating CHCs, the majority of patients who speak Portuguese are distributed at three of the participating CHCs, one of which has the lowest screening rate overall and another which has the third lowest screening rate across the participating CHCs. The distribution of Portuguese speakers at the centers with lower screening rates could account for the lower screening rate seen in Portuguese speakers. Other studies have noted lower uptake of colorectal cancer screening amongst limited English speakers as well21. Cataneo and colleagues found that Hispanic individuals who did not have limited English proficiency had higher colorectal cancer screening uptake than Hispanic individuals with limited English proficiency21. Interestingly, in our study Hispanic individuals had the second lowest screening rates despite no significant difference in screening between English and Spanish speakers. Spanish is the second most common language spoken at CHCs across Massachusetts, and our findings could again reflect the efforts of CHCs to prioritize equity in colorectal screening.

In our study the screening rate for those 45 to 49 and 50 to 54 was significantly lower than those 55 and older. Lower screening rates in individuals 45 to 49 have been shown in other studies as well and are expected as this population is only recently eligible for screening1,22. Low screening rates within this group may be due to lower awareness of the need for screening, lower engagement in the medical system compared to older individuals, cost, need for time of work and childcare, or other factors specific to this population23. Cost is likely especially an issue for the uninsured and individuals in non-Medicaid expansion states. To screen this younger population and halt the rising incidence of colorectal cancer in this group, targeted and low-burden interventions (i.e. text message reminders, CRC education given to patients prior to seeing their provider) that address the unique and multi-level barriers faced by all age groups, while not placing additional burdens on CHC resources and providers will be needed.

There are a few limitations of our study. First, if patients received colorectal cancer screening tests outside of the participating CHC that were not recorded in the system, this could underestimate screening rates. Nevertheless, colorectal cancer screening is a reportable metric at CHCs, and thus CHCs work hard to update each individual patient record with outside results. Second, our study includes a sample of only 10 CHCs participating in an equity-focused network in Massachusetts. However, the low screening rates and population characteristics in this study are similar to those seen overall at other CHCs across the state. Third, the data from this study come predominantly from the electronic health record which could be inaccurate if data such as race, ethnicity or language are entered incorrectly or presumed, although there have been significant efforts across CHCs in Massachusetts to ensure high quality data on these variables. Fourth, the CHCs included are all located within Massachusetts which has universal health care and is a Medicaid-expansion state. Thus, our findings may not be generalizable to all states. Fifth, the primary objective of our study was to estimate the percentage of additional screenings needed to screen average-risk individuals 45 to 49 across our partner CHCs, and not the overall burden of individuals due for screening across age groups. As a result the total burden of screenings needed could be underestimated. Our goal was to provide information that would assist our CHC partners in reaching this newly eligible group. Lastly, the data were extracted from a population management system by the population management software provider. At the point of extraction, they applied the exclusion criteria in order to provide us with no more than “minimally necessary data”. Thus, we are unable to provide the number of patients who did not meet inclusion criteria for the study. A strength of our study is that it includes a large and diverse patient population. Further, the diversity of the patient population and the diversity in CHC patient demographics and characteristics makes our findings generalizable to other community health centers caring for diverse patient populations.

After the revision in the USPSTF colorectal cancer screening guidelines, there were a significant number of additional individuals eligible for colorectal cancer screening without an increase in resources. Expanded financial resources should be imparted on CHCs through federal grants, and/or increased reimbursement and financial incentives from insurers to assist them in reaching this larger screening eligible population. Future studies should include cost analyses of screening at CHCs after the revision in the USPSTF guidelines as well as research to identify the unique barriers to screening in individuals age 45 to 49 and develop effective and sustainable strategies to engage this population in colorectal cancer screening and halt the rise of colorectal cancer incidence and mortality in this group. While we applaud the opportunity for cancer prevention reflected in the revised CRC screening guidelines, we note the importance of ensuring that all health systems that serve historically disadvantaged populations have the resources needed to address the expanded screening needs.