Impact of the COVID-19 Pandemic on Cancer Screening Delays

PURPOSE

To examine delays in cancer screenings during the COVID-19 pandemic.

METHODS

Participants from previous studies (N = 32,989) with permissions to be recontacted were invited to complete a survey between June and November 2020. Participants (n = 7,115) who met the age range for cancer screenings were included. Participants were asked if they planned to have and then if they postponed a scheduled mammogram, Pap test, stool blood test, colonoscopy, or human papillomavirus (HPV) test. Logistic regression was used to determine the factors associated with cancer screening delays for each planned test.

RESULTS

The average age was 57.3 years, 75% were female, 89% were non-Hispanic White, 14% had public insurance, and 34% lived in rural counties. Those who planned cancer screenings (n = 4,266, 60%) were younger, more likely to be female, with higher education, had private insurance, and lived in rural counties. Specifically, 24% delayed a mammogram (n = 732/2,986), 27% delayed a Pap test (n = 448/1,651), 27% delayed an HPV test (n = 59/220), 11% delayed a stool blood test (n = 44/388), and 36% delayed a colonoscopy (n = 304/840). Age, race/ethnicity, education, and health insurance were associated with delays in cancer screenings (all P < .05). Compared with non-Hispanic White women, non-Hispanic Black women had lower odds of delaying a mammogram (odds ratio [OR], 0.60; 95% CI, 0.39 to 0.94), Hispanic women had higher odds of delaying Pap test (OR, 2.46; 95% CI, 1.34 to 4.55), and women with other race/ethnicity had higher odds of delaying both Pap test (OR, 2.38; 95% CI, 1.41 to 4.02) and HPV test (OR, 5.37; 95% CI, 1.44 to 19.97).

CONCLUSION

Our findings highlighted the urgency for health care providers to address the significant delays in cancer screenings in those most likely to delay. Strategies and resources are needed to help those with barriers to receiving guideline-appropriate cancer screening.

INTRODUCTION

The novel COVID-19 caused by the pathogen severe acute respiratory syndrome coronavirus 2 has resulted in 86 million individuals infected and more than one million deaths in the United States.¹ Most US states announced stay-at-home orders on March 22, 2020, to reduce the spread of COVID-19, resulting in decreases in routine health care, including screening, diagnosis, and treatment for non–COVID-19 diseases such as cancer.² As most US hospitals paused elective surgeries and other nonurgent care in the initial phase of the pandemic, the volume of cancer screening dramatically decreased by 86%-94% in March 2020 compared with prior years.³ Between March 15 and June 16, 2020, 285,000 breast, 95,000 colorectal, and 40,000 cervical examinations were missed.³ Across the US population, the total deficit in cancer screening due to the COVID-19 pandemic was estimated to be 3.9 million in breast cancer, 3.8 million in colorectal cancer, and 1.6 million in prostate cancer.⁴

CONTEXT

• Key Objective

• We examined the impact of the COVID-19 pandemic on delays in breast, colorectal, and cervical cancer screenings.

• Knowledge Generated

• Among individuals within the sex and age range of cancer screenings, 60% had a planned cancer screening test between March and December 2020. Among individuals who planned any cancer screenings, 11%-36% delayed the planned test due to the COVID-19 pandemic. Age, race/ethnicity, education, and health insurance were associated with delays in cancer screenings.

• Relevance (I. Cheng)

• The delays observed in planned cancer screenings due to the COVID-19 pandemic and associations with demographic and socioeconomic factors point to the importance of directed health care initiatives to reduce the gaps in cancer screening.*

• *Relevance section written by JCO Associate Editor Iona Cheng, PhD, MPH.

The delays and avoidance of cancer screenings resulted in a significant decline in the number of newly diagnosed cancer cases during the COVID-19 pandemic. According to a study from Massachusetts General Brigham, between March 2020 and June 2020, the decreases in cancer diagnoses were 19%-78% due to lack of cancer screenings.⁵ Delays in cancer screening due to the COVID-19 pandemic put patients at higher risk for later stages of cancer, potentially facing different therapeutic interventions and other serious complications.^2,6 As the timing of diagnosis substantially influences cancer prognoses and outcomes, delays in cancer screenings and diagnoses can result in excess death.² It was estimated that due to the COVID-19 pandemic, almost 10,000 excess deaths from breast cancer and colorectal cancer would be reported over the next decade in the United States.²

Persistent low screening volumes were observed among people with lower education and Asian, Hispanic, and Black individuals.^7-10 Delays in cancer screenings among these diverse and underserved populations may worsen preexisting disparities in cancer care and outcomes. Identifying populations that are most likely to delay cancer screenings can provide valuable guidance to enhance cancer screening and diagnosis strategies (such as at home cancer screening-fecal immunochemical test [FIT], mobile screening units) for different populations. Understanding the extent of cancer screening delays due to the COVID-19 pandemic can help researchers, health care providers, and policymakers optimize resources to promote cancer screenings and create systems for health promotion to catch up. Therefore, this study was conducted to examine the impact of the the COVID-19 pandemic on delays in the most common cancer screenings, including breast, colorectal, and cervical cancers.

METHODS

Overview

This study was part of a National Cancer Institute–funded initiative conducted in conjunction with 16 other National Cancer Institute–designated Cancer Centers, the IC-4 (Impact of COVID-19 on the Cancer Continuum Consortium). The initiative was funded to collectively develop core survey items and implement population surveys in the respective catchment areas. The overall goal of the IC-4 was to assess how differences in demographics (rural/urban, age, sex, race, and educational attainment) affect engagement in cancer preventive behaviors (eg, tobacco cessation, screening, and diet) and cancer management/survivorship behaviors (eg, adherence to treatment, adherence to surveillance, and access to health services) in the context of COVID-19 environmental constraints (eg, social distancing, employment, and mental health). Each site had its theoretical framework and survey methods. Our site used the IC-4 core set of common data elements, augmented with questions of interest to the local team, with remote data collection methods to include many unique and diverse populations. The survey elements (see Appendix Table A1, online only) were finalized in conjunction with other members of the IC-4.¹¹ The Ohio State University (OSU) Institutional Review Board approved this study.

Sample Selection

Participants who agreed to be recontacted from previous studies were asked to participate in this study with a wide variety of populations, including healthy residents and patients with cancer. Eligible participants were adults age 18 years or older who consented to take part in the study. To ensure the inclusion of the most vulnerable, underserved, and minority populations, we sought to recruit healthy adult volunteers, patients with cancer, cancer survivors, and cancer patients' and survivors' caregivers, mainly from Ohio, with some from Indiana. This was achieved by using two recruitment strategies. First, we identified and contacted individuals who previously participated in studies conducted at OSU and consented to be contacted for future research projects. In addition, we invited patients with cancer and survivors to nominate their primary caregivers to participate in the study. The list of previous research projects conducted at OSU included the Rural Interventions for Screening Effectiveness study (R01 CA196243), the Community Initiative Towards Improving Equity and Health Status cohort (Supplement to P30CA016058), the OSU Center of Excellence in Regulatory Tobacco Science cohort (P50CA180908), and members of the Total Cancer Care cohort (P30CA016058). Second, to further enhance the representative of our study sample and ensure the inclusion of minority and underserved communities, we used our community partners and listservs to send tailored e-mail invitations.

Interview/Data Collection

We used several data collection methods, including web, phone, and mailed surveys. Respondents with valid e-mails received an initial survey invitation e-mail along with three reminders seven days apart. All participants were initially screened using an eligibility form before conducting the survey. Participants were able to save the web survey and resume it later. Those who partially completed the web survey received an e-mail reminder one week after they last accessed the survey. A trained interviewer contacted participants without an e-mail address and those with invalid e-mails on file by phone. Participants who were initially reached by phone were offered the option to complete the survey over the phone or online. We mailed a cover letter and a paper survey with a self-addressed, stamped return envelope to participants who requested a mailed survey. For non–English-speaking participants, a bilingual staff member administered the survey in the appropriate language. Participants were offered a gift card of $10 in US dollars (USD) upon completion of the survey. All data were collected and managed using the Research Electronic Data Capture secure web-based application hosted at OSU.^12,13

Measurements

Demographic variables collected included age, sex assigned at birth (male or female), race (White, Black/African American, Asian, or multiple/other), and marital status (single or never married, married/living as married, divorced/widowed/separated/other). Individuals were asked to specify their insurance, which was sorted into no insurance, public only, private only, and public and private. Participants' counties of residence were classified into metro and nonmetro on the basis of the 2013 Rural-Urban Continuum Codes (RUCC).¹⁴ Counties with RUCCs of 1-3 were coded as metro, while those with RUCCs of 4-9 were coded as nonmetro.

To assess the impact of the COVID-19 pandemic on cancer screening, we restricted the analysis to individuals in sex and age ranges that are appropriate for each cancer screening test according to the US Preventive Service Task Force recommendations: mammogram (women age 40-74 years), Pap test (women age 21-65 years), human papillomavirus (HPV) test (women age 30-65 years), and colonoscopy and stool blood test (men and women age 50-75 years).^15-17 Eligible participants were asked whether they planned to have a mammogram, Pap test, stool blood test, colonoscopy, HPV test, or HPV vaccine between March and December 2020. Those who planned any of these tests were asked whether they or their doctor postponed the test because of the COVID-19 pandemic.

Statistical Analysis

Overall and stratified characteristics were summarized using descriptive statistics, including means and standard deviations for continuous variables and frequencies and proportions for categorical variables. Differences between participants with versus without planned cancer screenings were compared using T-tests or Kruskal-Wallis tests for continuous variables and chi-square or Fisher's exact test for categorical variables. Adjusted logistic regression models were used to examine significant predictors associated with delays in each cancer screening, including mammograms, Pap smears, stool blood tests, colonoscopy, and HPV tests. In sensitivity analyses, we combined all cervical cancer screenings (Pap smears and HPV tests) and all colorectal cancer screenings (stool blood tests and colonoscopy). We also conducted modified Poisson regression models to assess significant factors of cancer screening delays using the prevalence ratios.¹⁸ All statistical analyses were conducted using SAS v9.4, with a significance level of 0.05.

RESULTS

A total of 7,115 participants were included in the study (Fig 1). The average age was 57.3 years, 75.0% were female, 89.1% were non-Hispanic White, 55.5% had a college or higher degree, and 75.2% were married (Table 1). Most participants were Ohio residents (95.8%), one third of the study sample lived in rural counties, 14.1% had public insurance, 53.7% had private insurance, and 29.9% had public and private insurance. Compared with those who did not plan (n = 2,849; 40%), participants who planned any cancer screenings (n = 4,266; 60%) were younger, more likely to be female, had higher education, with private insurance, and lived in rural areas (all P < .001).

FIG 1.

Flowchart of the impact of COVID-19 survey. ^aNot all individuals in the study sample planned a cancer screening. The numbers for planned test do not add up to the study sample.

TABLE 1.

Characteristics of Participants by Planned Cancer Screening Status

Among individuals who planned to get cancer screenings, 24.5% delayed a mammogram (n = 732/2,986; Table 2), 27.1% delayed a Pap test (n = 448/1,651), 26.8% delayed an HPV test (n = 59/220), 11.3% delayed a stool blood test (n = 44/388), and 36.2% delayed a colonoscopy (n = 304/840).

TABLE 2.

Prevalence of Cancer Screening Delays Among Individuals Who Planned to Get a Test

For mammograms, older age was significantly associated with lower odds of delaying a planned test (odds ratio [OR], 0.81; 95% CI, 0.72 to 0.92; Table 3). Compared with non-Hispanic White women, non-Hispanic Black women had lower odds of mammogram delays (OR, 0.60; 95% CI, 0.39 to 0.94). Compared with those with high school or less education, women with some college/associate degree, college degree, or graduate degree had increased odds of mammogram delays (OR, 1.45; 95% CI, 1.07 to 1.99; OR, 1.40; 95% CI, 1.03 to 1.92; OR, 1.58; 95% CI, 1.16 to 2.17, respectively). Indiana residents had increased odds of mammogram delays compared with Ohio residents (OR, 1.72; 95% CI, 1.21 to 2.45). Marital status, health insurance status, and rural/metro residence were not significantly associated with mammogram delays. After stratifying women by age (40-49 years and 50-74 years), race and ethnicity (non-Hispanic Black) were the only factors that were associated with lower odds of mammogram delays among women age 40-49 years; whereas younger age, higher education, and residents of Indiana were associated with higher odds of mammogram delays among women age 50-74 years (Appendix Table A2, online only).

TABLE 3.

Adjusted Odds Ratios for Factors Associated With Delays in Cancer Screenings During the COVID-19 Pandemic

For Pap smear tests, older age was associated with lower odds of delaying a planned test (OR, 0.89; 95% CI, 0.79 to 1.00). Compared with non-Hispanic White women, Hispanic and those identified as other races had higher odds of Pap test delays (OR, 2.46; 95% CI, 1.34 to 4.55; OR, 2.38; 95% CI, 1.41 to 4.02, respectively). Compared with those with high school or less education, women with some college/associate degree had increased odds of Pap test delays (OR, 1.53; 95% CI, 1.02 to 2.31). In addition, compared with those without health insurance, women with private (OR, 0.37; 95% CI, 0.18 to 0.74) or a combined public and private insurance (OR, 0.44; 95% CI, 0.19 to 1.00) had lower odds of Pap test delays. Marital status and rural/metro residence were not associated with mammogram delays.

For colorectal cancer screening, graduate-level participants had higher odds of delaying a planned colonoscopy (OR, 2.09; 95% CI, 1.23 to 3.56) than those with a high school degree or less. Widowed, separated, or divorced individuals had lower odds of delaying a planned colonoscopy (OR, 0.48; 95% CI, 0.25 to 0.92) than single individuals. Age, sex, race/ethnicity, health insurance, and rural/metro residence were not associated with colonoscopy delays. We also did not observe any factors associated with delays in stool blood tests.

For the HPV test, older age was associated with lower odds of delaying a planned HPV test (OR, 0.65; 95% CI, 0.46 to 0.93). Compared with non-Hispanic White, individuals who identified as other race-ethnicity had higher odds of HPV test delays (OR, 5.37; 95% CI, 1.44 to 19.97).

DISCUSSION

Our study showed that, among individuals within the sex and age range of cancer screenings, 60% had a planned cancer screening test. Compared with those without planned cancer screenings, individuals who planned for a cancer screening were younger, widowed, separated, or divorced, had higher education, higher income, private insurance, and lived in rural counties. We also found that among those who planned for a cancer screening test, 11%-36% delayed the planned test due to the COVID-19 pandemic. Delays in cancer screenings, especially for Pap smears and HPV tests, were concerning among younger individuals, Hispanic, and the other race/ethnicity group.

Unlike other studies that examined the general delays in cancer screening, our study compared the demographic differences between individuals who did and did not plan to obtain any cancer screenings between March and December 2020. Identifying the characteristics of individuals who were within the age range of guideline-recommended screening but did not schedule one is crucial. These populations have historically faced barriers to adherence to guideline-recommended cancer screenings and may experience additional burdens to access health care during the COVID-19 pandemic disruption.^6,19,20 Health care clinics and public health organizations should form partnerships at the community level to address the barriers to care for these populations. For example, health education programs can inform people that cancer screenings are covered under the Affordable Care Act, as well as free or low-cost screening options for the uninsured or those without physician's referrals.²¹ In addition, mobile screening units demonstrated cost-effectiveness in increasing cancer screening rates, especially among underserved populations.^22-25 Collaboration with mobile screening units can expand access to cancer screening in low-resource settings.

Paused nonurgent care in US hospitals and fear of contracting COVID-19 in health care settings resulted in substantial decreases in cancer screening. Previous studies demonstrated a substantial decline in breast, colorectal, cervical, and prostate cancers from March through May 2020 compared with prior years.^{4,7,8,21,26,27} Although cancer screenings have rebounded since June 2020, it still has not reached 100% of expected rates.^4,28,29 However, most of these studies heavily depended on medical claims and records to measure cancer screening disruptions during the COVID-19 pandemic, which may limit to including people who maintained the same health insurance coverage.^{4,5,7,8,26-29} One study used a population-based national survey to compare cancer screenings in 2020 with previous years and found that racial minorities and people with lower educational attainment experienced a more significant decrease in cancer screenings during health care disruptions.¹⁰ Although this study examined the population-wide guideline-recommended cancer screening rates, it did not assess the proportion of the population within the guideline-recommended screening age who planned and then delayed cancer screening during the COVID-19 pandemic.

Our study showed that among individuals who planned cancer screenings, a delayed screening test was greatest in colonoscopy (36.2%), followed by Pap smears (27.1%), HPV test (26.8%), and mammogram (24.4%). This is consistent with findings from previous studies that a larger deficit was observed in cancer screenings that require procedures.^4,10 Some studies observed an increase in stool tests in 2020 compared with previous years and suggested that the rise may counterbalance the decrease in colonoscopy.^10,30-32 In our study, we found that the delays in stool blood tests were the lowest (11.3%) among other screening tests. This highlighted the potential to use at-home testing to improve cancer screening uptake, especially during a major health care disruption. Researchers have recently developed approaches for self-collected HPV sampling and mobile technologies (mHealth) for cervical cancer screening.^33-37 After establishing the efficacy of these tests, using at-home testing can be an effective strategy to boost cancer screening uptake for different populations.

We found that among those who planned a cancer screening, age, race/ethnicity, education, and health insurance were associated with delays in cancer screenings. For example, older individuals were less likely to delay a mammogram, Pap smear, or HPV test. Older individuals may have other health conditions that require them to follow-up with health care providers regularly. It is possible that they could complete cancer screening during the same medical visit. However, individuals with higher education may have greater concerns of catching COVID-19 and in turn were more likely to avoid nonessential hospital visits, which could explain their higher odds of delay for cancer screenings. Moreover, women with higher education may have other life priorities and responsibilities during the pandemic that did not allow them to make time for mammogram and Pap tests. We also observed that individuals with private or private and public insurance were less likely to delay a Pap smear. They may have less fear of catching COVID-19 as they would have access to health care and sufficient insurance coverage for medical expenses. Our sample included individuals from Ohio and Indiana. As both states are Medicaid expansion states, this could explain why there were no differences in cancer screening delays among individuals with public insurance. However, compared with non-Hispanic White women, Hispanic women were more likely to delay a planned Pap smear, and women of other race/ethnicity were more likely to delay a planned Pap smear and HPV test. This is consistent with other research where Hispanic individuals and the other race/ethnicity groups experienced a more significant decrease in cancer screening.^10,26,27 The disproportionate impact of cancer screening delays among different racial groups is concerning as some of these populations (eg, Hispanic, non-Hispanic American Indian/Alaska Native) have a higher risk of cervical cancer.³⁸ Delays in cervical cancer screenings and timely diagnosis may exacerbate health disparities in these populations. As we identified those most likely to delay cancer screenings, health care providers should target strategies direct at these individuals to address delays in cancer screenings. Health care providers can increase cancer screening by reminding patients that it is safe to get screening tests, and it is crucial to continue routine screenings to detect cancer early.

This study has some limitations. The study used a cross-sectional survey design, and also depended on self-reported data, which may have recall bias. The current study did not assess the actual month of the cancer screening delays, which did not allow us to examine the variations of cancer screening delay over time. In addition, we did not have access to medical records, which prohibited us from truly assessing each participant's cancer screening history. The survey did not ask usual source of care, and we were not able to evaluate how source of health care was associated with delays in cancer screening. In addition, we recruited participants from previous studies. Hence, it is possible that cancer screening behaviors differed among individuals willing to participate in research studies versus those not enrolled in research studies. Finally, the study population was not nationally representative, as most participants were from Ohio and Indiana. Therefore, the findings from our study may not be generalizable to other populations.

Our study has several strengths. First, the large sample size allowed us to assess planned and delayed through various methods of cancer screenings (eg, colonoscopy and stool blood test for colorectal cancer, Pap smears, and HPV tests for cervical cancer). Second, the timing of this study was June to November 2020, which was the midst of the pandemic. This allowed us to understand the impact of COVID-19 on cancer screenings. Third, to our knowledge, we are the first study to examine the characteristics of those who planned versus not planned a cancer screening between March and December 2020. Those who did not plan a screening may need one but did not schedule one because of the COVID-19 pandemic. They are the populations that might need additional resources to overcome barriers to adherent guideline-recommended cancer screenings. The novelty of our study is that we examined individuals who delayed a planned cancer screening test. Identifying the characteristics of the most likely to delay a planned test provides valuable information to health care providers. These individuals may be more likely to return to routine cancer screening after receiving reminders from providers that it is safe to get screened.

In conclusion, among individuals who planned a cancer screening, some delayed the planned test due to the COVID-19 pandemic. Delays were especially concerning in younger individuals, Hispanic, and other race/ethnicity group. Delayed cancer screening may worsen preexisting disparities in cancer care and outcomes. Health care providers need to address delays in cancer screenings in those most likely to delay, such as reminding patients that it is safe to schedule cancer screenings.

APPENDIX 1. Impact of COVID-19 on Behaviors across the Cancer Control Continuum in Ohio group

Guy Brock, Victoria L. Champion, Chasity Washington, Amy K. Ferketich, Heather Hampel, Heather Aker, Xiaochen Zhang, Mohamed I. Elsaid, Cecilia DeGraffinreid, and Electra D. Paskett

TABLE A1.

Survey Elements by Core Constructs

TABLE A2.

Adjusted Odds Ratios for Factors Associated With Breast Cancer Screening Delays During the COVID-19 Pandemic, by Age Groups

TABLE A3.

Adjusted Odds Ratios for Factors Associated With Delays in Cancer Screenings (combined all cervical cancer screenings and all colorectal cancer screenings) During the COVID-19 Pandemic

TABLE A4.

Adjusted Prevalence Ratios for Factors Associated With Delays in Cancer Screenings During the COVID-19 Pandemic

AUTHOR CONTRIBUTIONS

Conception and design: All authors

Financial support: Electra D. Paskett

Administrative support: Cecilia DeGraffinreid, Electra D. Paskett

Provision of study materials or patients: Victoria L. Champion, Electra D. Paskett

Collection and assembly of data: Cecilia DeGraffinreid, Victoria L. Champion, Electra D. Paskett

Data analysis and interpretation: Xiaochen Zhang, Mohamed I. Elsaid, Electra D. Paskett

Manuscript writing: All authors

Final approval of manuscript: All authors

Accountable for all aspects of the work: All authors

AUTHORS' DISCLOSURES OF POTENTIAL CONFLICTS OF INTEREST

Impact of the COVID-19 Pandemic on Cancer Screening Delays

The following represents disclosure information provided by authors of this manuscript. All relationships are considered compensated unless otherwise noted. Relationships are self-held unless noted. I = Immediate Family Member, Inst = My Institution. Relationships may not relate to the subject matter of this manuscript. For more information about ASCO's conflict of interest policy, please refer to www.asco.org/rwc or ascopubs.org/jco/authors/author-center.

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