Association of COVID-19 Pandemic with Colorectal Cancer Screening: Impact of Race/Ethnicity and Social Vulnerability

Background The COVID-19 pandemic disrupted health care delivery, including cancer screening practices. This study sought to determine the impact of the COVID-19 pandemic lockdown on colorectal cancer (CRC) screening relative to social vulnerability. Methods Using the Medicare Standard Analytic File, individuals 65 years old or older who were eligible for guideline-concordant CRC screening between 2019 and 2021 were identified. These data were merged with the Center for Disease Control Social Vulnerability Index (SVI) dataset. Changes in county-level monthly screening volumes relative to the start of the COVID-19 pandemic (March 2020) and easing of restrictions (March 2021) were assessed relative to SVI. Results Among 10,503,180 individuals continuously enrolled in Medicare with no prior diagnosis of CRC, 1,362,457 (12.97%) underwent CRC screening between 2019 and 2021. With the COVID-19 pandemic, CRC screening decreased markedly across the United States (median monthly screening: pre-pandemic [n = 76,444] vs pandemic era [n = 60,826]; median Δn = 15,618; p < 0.001). The 1-year post-pandemic overall CRC screening utilization generally rebounded to pre-COVID-19 levels (monthly median screening volumes: pandemic era [n = 60,826] vs post-pandemic [n = 74,170]; median Δn = 13,344; p < 0.001). Individuals residing in counties with the highest SVI experienced a larger decline in CRC screening odds than individuals residing in low-SVI counties (reference, low SVI: pre-pandemic high SVI [OR, 0.85] vs pandemic high SVI [OR, 0.81] vs post-pandemic high SVI [OR, 0.85]; all p < 0.001). Conclusions The COVID-19 pandemic was associated with a decrease in CRC screening volumes. Patients who resided in high social vulnerability areas experienced the greatest pandemic-related decline. Supplementary Information The online version contains supplementary material available at 10.1245/s10434-024-15029-x.

Association of COVID-19 Pandemic with … such as conversion of routine office visits into telehealth appointments and cancellation of non-urgent interventions such as screening and vaccination. 7These policies affected primary health care by redirecting resources to help with the management of the pandemic. 8,9Notably, cancer screening recommendations also were altered.The American Society for Gastrointestinal Endoscopy (ASGE) recommended the delay of routine screening colonoscopies and follow-up procedures after positive stool tests. 10espite removal of COVID-19 restrictions, the decline in rates of screening for cancers such as breast and lung tumors have not fully recovered to date. 10,11The rate of recovery in screening deficits was notably delayed among the Medicaid or Medicare-Medicaid dual-eligible populations compared with privately insured patients. 12otential changes in the diagnosis and management of CRC after the COVID-19 pandemic have not been welldefined.4][15] Previous studies have demonstrated inequalities in cancer screening among certain racial/ethnic groups and socioeconomically vulnerable populations. 16,17Moreover, the risk of CRC increases by age. 18Siegel et al. 2 estimated that more than 56% of CRCs in 2023 would be diagnosed for individuals age 65 years or older. 2 As such, delays in cancer screening due to the COVID-19 pandemic among older patients and a return to pre-pandemic levels after lockdown restrictions are eased may have important implications. 11,19Therefore, the current study aimed to characterize how the COVID-19 pandemic influenced CRC screening.In addition, the study sought to determine the impact of the COVID-19 pandemic lockdown on CRC screening relative to social vulnerability among a nationally representative cohort of older individuals.

Data Source and Study Population
Data were extracted from 100% Medicare Standard Analytic Files claims data obtained by the Centers for Medicare and Medicaid Services (CMS) between 2019 through 2021 to identify individuals who did and did not undergo screening for CRC. 20The CMS maintains the Medicare Standard Analytic Files (SAF), an administrative billing database that provides patient-level data on demographics, diagnoses, procedures, and expenditures. 21To be included in the analytic cohort, individuals had to have Medicare coverage and consecutive enrollment in Medicare Parts A and B for the study duration.
Only individuals age 65 years or older were included in the study cohort.The International Classification of Diseases, tenth revision (ICD-10) diagnostic and procedure codes, Current Procedural Terminology (CPT) codes, and Healthcare Common Procedure Coding System (HCPCS) codes were used to identify beneficiaries who had undergone screening for CRC. 22,23These codes included various methods for CRC screening including colonoscopies, barium enema, and fecal-occult blood test (Appendix Table S1). 24ndividuals with a prior diagnosis of CRC, as identified by ICD codes, were excluded from the study cohort.This study was approved by The Ohio State University Institutional Review Board, and the need for informed patient consent was waived because the data were de-identified.

Study and Outcome Measures
Information on age, sex, race/ethnicity, geographic region, Social Vulnerability Index (SVI), and Charlson Comorbidity Index (CCI) were collected. 20,25According to the U.S. census, regions were defined as Northeast (New England, Middle Atlantic), South (South Atlantic, East South Central, and West South Central), Midwest (East North Central, West North Central), and West (Mountain, Pacific). 26he SVI, developed and maintained by the Center for Disease Control and Agency for Toxic Substances and Disease Registry, is a validated measure used to assess community vulnerability to external pressures. 27The SVI was linked with the Medicare Standard Analytical Files using county-level Federal Information Processing System (FIPS) codes and categorized into tertiles. 27he participants were categorized into three equal groups based on tertile values for SVI.The CCI was assessed using ICD-9-CM and ICD-10-CM codes and dichotomized as ≤2 versus >2. 20,25Race/ethnicity was recorded based on self-reported social constructs, which are not a reflection of genetic ancestry, and categorized as non-Hispanic White, non-Hispanic Black, Hispanic, and non-Hispanic other race/ ethnicity. 28The non-Hispanic other race/ethnicity group was categorized as American Indians, Alaskan Natives, Native Hawaiians, Asians, Pacific Islanders, and self-reported "other" race/ethnicity groups due to small sample sizes. 28he primary outcome of interest was monthly median screening volumes for each time period.Monthly volumes of CRC screening were recorded for the entire study duration.The study duration was divided into three periods.The pre-COVID-19 pandemic period was defined as January 2019 to February 2020, whereas the COVID-19 pandemic period was defined as March 2020 to March 2021, and the postpandemic period was defined as April 2021 to December 2021. 29ockdown restrictions were eased throughout the country at different times and in a stepwise fashion.However, the majority of states had eased COVID-related restrictions by March 2021, so this was defined as the cutoff for the post-COVID-19 era 30,31 Statistical Analyses Continuous variables were analyzed via the Wilcoxon rank-sum test and reported as median and interquartile range (IQR).Categorical variables were compared via the chi-square test and represented as frequencies.Multivariable logistic regression models were used to assess the odds of a patient undergoing screening for CRC.Models for screening were adjusted for sex, race, age, CCI, SVI, genetic susceptibility, region, index year, and rurality (non-metropolitan vs metropolitan).The ICD codes were used to identify individuals with genetic susceptibility for malignancy (Appendix Table S2). 22Statistical analyses were performed using STATA version 18, and a two-sided significance level of α equal to 0.05 was used.

Association of the COVID-19 Pandemic CRC Screening Volumes with SVI
The monthly median volumes of CRC screening decreased markedly after the start of the pandemic (n = 60,826) versus before the pandemic (n = 76,444) (p < 0.001; Fig. 1).Compared with the pre-pandemic period, the monthly median CRC screening volumes during the In the post-pandemic period, after March 2021, the monthly median CRC screening volumes generally rebounded to pre-pandemic levels (n = 74,170) and were much higher than during the COVID pandemic in 2020 (n = 60,826) (p < 0.001).Notably, during the post-pandemic period versus during the pandemic in 2020, the monthly median CRC screening volumes rose among all SVI categories as follows: low SVI individuals (all p < 0.001) (Table 2).

DISCUSSION
According to the American Cancer Society, there would be 106,970 new cases of colon cancer and 46,050 new cases of rectal cancer in the United States in 2023. 32Prior studies have demonstrated that earlier diagnosis of CRC is associated with a significantly higher 5-year survival (> 90%). 32Screening for CRC may serve as a highly effective and efficient tool to identify pre-cancerous or early CRC. 337][38][39][40] Although previous research has assessed the impact of the COVID-19 pandemic on screening for other cancers, the effect of lockdown restrictions on CRC screening volumes, especially among vulnerable populations, remains ill-defined. 13,36The current study was important because we specifically characterized the decline in CRC screening during the pandemic, as well as the subsequent recovery in screening volumes relative to county-level SVI and race/ethnicity in a nationally representative cohort.Notably, median monthly CRC screening volumes declined drastically in 2020 after the implementation of lockdown restrictions, with socially vulnerable populations affected the most.Patients living in counties with high social vulnerability experienced the greatest pandemic-related decline.
The COVID-19 pandemic began in early 2020 and caused a substantial lockdown in the United States during March of that year. 29The pandemic placed an enormous burden on the health care system, leading to challenges that had a great impact on the ability to deliver health care services effectively. 41In particular, the pandemic had a significant impact on screening, causing a sharp decline in global screening rates for all cancers. 13,37,42The dramatic decrease in screening was undoubtedly due to cancellations of elective and planned procedures, as well as a decrease in public transport, loss of income to pay for services, and a shift in the health workforce toward COVID-19 services. 43,44To this point, Chen et al. 36 reported that CRC screening rates were 13.1% lower in July 2020 than in July 2019.Similarly, Tinmouth et al. 45 reported a 60% reduction in colonoscopies performed during 2020 versus 2019 in Canada.7][48][49] Furthermore, patients with a high SVI were more likely to be affected by COVID-19-related illnesses, which disproportionately affected their odds of being screened during the pandemic. 50n line with these studies, the current study noted a substantial decrease in median CRC screening volumes during 2020 after implementation of lockdown restrictions due to the COVID-19 pandemic.Interestingly, the post-pandemic screening rate did not rebound to pre-pandemic levels or surpass them.This may have been due to patient reluctance to seek medical care in the post-pandemic setting, as well as difficulty accessing cancer screening due to additional financial burdens related to the pandemic.Elderly patients and patients with comorbidities, who were at higher risk for serious complications from COVID-19, may have been specifically affected by these factors.Another reason for the smaller rebound in post-pandemic screening may have been the expansion of screening guidelines to include individuals 45 years old at a time when the physician workforce was constrained by pandemic-related challenges.Of particular note, individuals with moderate or high SVI had lower odds of screening before, during, and after the pandemic, with the worst odds reported for individuals residing in high-SVI areas during the pandemic.These findings highlight that socially vulnerable populations were most affected by pandemic-related policy changes.
2][53] To this point, SVI may serve as a composite tool to assess key social determinants of health and provide insight into barriers for health care access and utilization.Bauer et al. 16   by high SVI were associated with reduced screening rates.Moreover, individuals from high-SVI counties may not have access to effective transportation for travel to cancer screening facilities. 54,55Despite efforts to improve access to health care, patients who reside in moderate-and high-SVI areas still experience disparities in access to cancer prevention services. 16,56Building on previous work, the current study demonstrated that individuals in the high socially vulnerable areas experienced the lowest odds of CRC screening during the pandemic.2][63] Additionally, efforts were made to ensure that individuals who missed their cancer screenings during to the pandemic were given priority and screened first. 62,63Resumption of these programs, complemented by the relaxation in pandemic lockdowns and increase in tele-medicine services, improved access to health care services globally. 64,65Interestingly, data from the current study demonstrated disparate access to CRC screening among various racial/ethnic groups.For example, Hispanic and other non-White racial/ethnic groups experienced a decline in the odds of CRC screening during the pandemic that did not recover to pre-pandemic levels.Barriers such as language difficulties, insurance status, limited health literacy, reduced awareness of preventive health care, and cultural differences may preclude certain racial/ethnic groups from accessing health services, which may worsen disparities in cancer prevention. 66Recently, health care organizations and policymakers have sought to improve access to care through initiation of the Affordable Care Act, as well as through outreach programs, mobile screening vans, and community-based awareness initiatives. 67,68In turn, these efforts may mitigate race/ethnicity-based disparities in cancer screening among non-Hispanic White and non-Hispanic Black individuals. 69,70In fact, non-Hispanic Black individuals may be more likely than non-Hispanic White individuals to be up to date relative to cancer screening. 71he current study may have important implications for health care institutions, payers, policymakers, and professional organizations.For example, the data offer evidence to support implementation of community policies and related initiatives focused on investment and promotion of structural equity within cancer prevention systems.Socially vulnerable patients from disadvantaged communities face additional barriers that preclude access to cancer care prevention.on providing screening and follow-up services to individuals with low income and limited or no insurance coverage.The National Colorectal Cancer Roundtable (NCCRT) is a coalition of various organizations from the public, private, and voluntary sectors, that is also working to increase CRC screening rates across the country. 73Similar to CRCCP, their efforts primarily target low-income and underrepresented communities through initiatives such as public education campaigns, provider training, and policy advocacy.Health care providers and organizations must work together to improve screening of CRC patients, especially among vulnerable populations, to improve the quality of cancer prevention services.
The current study should be interpreted with consideration of several limitations.Because only Medicare beneficiaries were examined, the findings may not be generalizable to younger individuals. 74Although most screening methods are covered under Medicare, home testing kits using fecal occult blood tests may not fall under the coverage.Moreover, use of administrative data may be associated with data miscoding and misclassification errors.To address this, we used ICD-10-CM diagnosis codes previously demonstrated to have high fidelity for administrative data use. 75The Medicare data were available only until December 2021.As a result, the period after COVID-19 was not fully captured, leading to the utilization of monthly median screening volumes instead of overall screening rates.Moreover, the impact of the COVID-19 pandemic on different screening methods, including colonoscopy, fecal occult blood testing, and CT colonography, could not be assessed due to database limitations.The current study examined only CRC screening.Future studies need to assess the impact of the decrease in screening on the incidence of late-stage CRC and CRC mortality.The current study could not assess the percentage of individuals recommended for screening who were up to date with their screening according to USPSTF screening guidelines due to the limited study duration.In conclusion, the COVID-19 pandemic caused a sharp decline in CRC screening after March 2020 that was followed by a recovery to near pre-pandemic levels after easing of restrictions in 2021.Individuals with high SVI and certain racial/ethnic groups experienced the greatest decline in screening volumes during the COVID pandemic.These data highlight the need to address social determinants of health to alleviate disparities in cancer care prevention.

100 FIG. 3
FIG. 3Map showing changes in colorectal cancer (CRC) monthly median screening volumes during the pandemic versus pre-pandemic.

100 FIG. 4
FIG. 4 Map showing changes in colorectal cancer (CRC) monthly median screening volumes post-pandemic versus during the pandemic.

TABLE 1
Race is reported as non-Hispanic White, non-Hispanic Black, Hispanic, non-Hispanic other. b

TABLE 2
reported that areas characterized Monthly median screening volumes for low and high SVI categories before, during, and after the COVID-19 pandemic.Association of COVID-19 Pandemic with … Median monthly CRC screening volumes before, during, and after the COVID-19 pandemic CRC, colorectal cancer; SVI, Social Vulnerability Index; Metro, metropolitan area; Non-metro, Non-metropolitan area a Statistically significant: p < 0.05 b Race is reported as non-Hispanic White, non-Hispanic Black, Hispanic, non-Hispanic other.

TABLE 3
Multivariable logistic regression analysis of patients undergoing CRC screening CRC, colorectal cancer; SVI, Social Vulnerability Index; Metro, metropolitan area; Non-metro, non-metropolitan area; CCI, Charlson Comorbidity Index a Statistically significant: p < 0.05 b Race is reported as non-Hispanic White, non-Hispanic Black, Hispanic, non-Hispanic other.