Review
1Office of Community Health and Research, University of Arkansas for Medical Sciences Northwest, Fayetteville, AR, United States
2College of Medicine, University of Arkansas for Medical Sciences Northwest, Fayetteville, AR, United States
Corresponding Author:
Pearl A McElfish, MBA, PhD
College of Medicine
University of Arkansas for Medical Sciences Northwest
1125 N College Avenue
Fayetteville, AR, 72703
United States
Phone: 1 (479) 713 8680
Email: pamcelfish@uams.edu
Abstract
Background: Cancer screening tests are recommended to prevent cancer-associated mortality by detecting precancerous and cancerous lesions in early stages. The COVID-19 pandemic disrupted the use of preventive health care services. Although there was an increase in the number of cancer screening tests beginning in late 2020, screenings remained 29% to 36% lower than in the prepandemic era.
Objective: The aim of this review is to assist health care providers in identifying approaches for prioritizing patients and increasing breast, cervical, and colorectal cancer screening during the uncertainty of the COVID-19 pandemic.
Methods: We used the scoping review framework to identify articles on PubMed and EBSCO databases. A total of 403 articles were identified, and 23 articles were selected for this review. The literature review ranged from January 1, 2020, to September 30, 2021.
Results: The articles included two primary categories of recommendations: (1) risk stratification and triage to prioritize screenings and (2) alternative methods to conduct cancer screenings. Risk stratification and triage recommendations focused on prioritizing high-risk patients with an abnormal or suspicious result on the previous screening test, patients in certain age groups and sex, patients with a personal medical or family cancer history, patients that are currently symptomatic, and patients that are predisposed to hereditary cancers and cancer-causing mutations. Other recommended strategies included identifying areas facing the most disparities, creating algorithms and using artificial intelligence to create cancer risk scores, leveraging in-person visits to assess cancer risk, and providing the option of open access screenings where patients can schedule screenings and can be assigned a priority category by health care staff. Some recommended using telemedicine to categorize patients and determine screening eligibility for patients with new complaints. Several articles noted the importance of implementing preventive measures such as COVID-19 screening prior to the procedures, maintaining hygiene measures, and social distancing in waiting rooms. Alternative screening methods that do not require an in-person clinic visit and can effectively screen patients for cancers included mailing self-collection sampling kits for cervical and colorectal cancers, and implementing or expanding mobile screening units.
Conclusions: Although the COVID-19 pandemic had devastating effects on population health globally, it could be an opportunity to adapt and evolve cancer screening methods. Disruption often creates innovation, and focus on alternative methods for cancer screenings may help reach rural and underresourced areas after the pandemic has ended.
doi:10.2196/34392
Keywords
Introduction
Cancer-associated mortality is the second leading cause of death in the United States [Anderson RN. Deaths: leading causes for 2000. Natl Vital Stat Rep 2002 Sep 16;50(16):1-85 [FREE Full text] [Medline]1,Ahmad FB, Anderson RN. The leading causes of death in the US for 2020. JAMA 2021 May 11;325(18):1829-1830. [CrossRef] [Medline]2]. Cancer screening tests are recommended to prevent cancer-associated mortality by detecting precancerous and cancerous lesions in early stages [Maida M, Macaluso FS, Ianiro G, Mangiola F, Sinagra E, Hold G, et al. Screening of colorectal cancer: present and future. Expert Rev Anticancer Ther 2017 Dec;17(12):1131-1146. [CrossRef] [Medline]3]. The most common routine cancer screenings include breast, colorectal, and cervical [Cancer. Centers for Disease Control and Prevention. 2021. URL: https://www.cdc.gov/chronicdisease/pdf/factsheets/cancer-h.pdf [accessed 2021-10-14] 4].
The COVID-19 pandemic disrupted the use of preventive health care services [Carethers JM, Sengupta R, Blakey R, Ribas A, D'Souza G. Disparities in cancer prevention in the COVID-19 era. Cancer Prev Res (Phila) 2020 Nov;13(11):893-896 [FREE Full text] [CrossRef] [Medline]5]; there was an abrupt decline in cancer screening services throughout 2020 [Croswell JM, Corley DA, Lafata JE, Haas JS, Inadomi JM, Kamineni A, National Cancer Institute Population-based Research to Optimize the Screening Process (PROSPR) II Consortium. Cancer screening in the U.S. through the COVID-19 pandemic, recovery, and beyond. Prev Med 2021 Oct;151:106595. [CrossRef] [Medline]6]. A report from May 2020 suggested there was a 94% drop in cancer screening tests across the United States, primarily due to disruptions in access to screening tests [Mast C, Munoz del Rio A. Delayed cancer screenings—a second look. Epic Research. 2020. URL: https://ehrn.org/articles/delayed-cancer-screenings-a-second-look [accessed 2021-08-03] 7]. Although there was an increase in the number of cancer screening tests beginning in late 2020, screenings remained 29% to 36% lower than in the prepandemic era [Mast C, Munoz del Rio A, Heist T. Cancer screenings are still lagging. Epic Research. 2021. URL: https://ehrn.org/articles/cancer-screenings-are-still-lagging [accessed 2021-08-03] 8].
The reduction in cancer screenings and other preventative and diagnostic care have been attributed to both health care provider and patient constraints [Basu P, Alhomoud S, Taghavi K, Carvalho AL, Lucas E, Baussano I. Cancer screening in the coronavirus pandemic era: adjusting to a new situation. JCO Glob Oncol 2021 Mar;7:416-424 [FREE Full text] [CrossRef] [Medline]9-Moore R, Zielinski MJ, Thompson RG, Willis DE, Purvis RS, McElfish PA. "This Pandemic Is Making Me More Anxious about My Welfare and the Welfare of Others:" COVID-19 stressors and mental health. Int J Environ Res Public Health 2021 May 26;18(11):5680 [FREE Full text] [CrossRef] [Medline]12]. Health care provider constraints included restrictions on elective procedures [Basu P, Alhomoud S, Taghavi K, Carvalho AL, Lucas E, Baussano I. Cancer screening in the coronavirus pandemic era: adjusting to a new situation. JCO Glob Oncol 2021 Mar;7:416-424 [FREE Full text] [CrossRef] [Medline]9] and a shortage of health care staff due to redeployment to help with pandemic-related care [Basu P, Alhomoud S, Taghavi K, Carvalho AL, Lucas E, Baussano I. Cancer screening in the coronavirus pandemic era: adjusting to a new situation. JCO Glob Oncol 2021 Mar;7:416-424 [FREE Full text] [CrossRef] [Medline]9,Kovar CL, Pestaner M, Webb Corbett R, Rose CL. HPV vaccine promotion: snapshot of two health departments during the COVID-19 pandemic. Public Health Nurs 2021 Sep;38(5):715-719 [FREE Full text] [CrossRef] [Medline]10]. Even when health care providers have increased availability of preventive care and cancer screenings, many patients face constraints. Patient constraints include loss of income and employer-based insurance coverage [Cancino RS, Su Z, Mesa R, Tomlinson GE, Wang J. The impact of COVID-19 on cancer screening: challenges and opportunities. JMIR Cancer 2020 Oct 29;6(2):e21697 [FREE Full text] [CrossRef] [Medline]11] and fear of contracting COVID-19 during in-person health care visits [Moore R, Zielinski MJ, Thompson RG, Willis DE, Purvis RS, McElfish PA. "This Pandemic Is Making Me More Anxious about My Welfare and the Welfare of Others:" COVID-19 stressors and mental health. Int J Environ Res Public Health 2021 May 26;18(11):5680 [FREE Full text] [CrossRef] [Medline]12].
The decline in cancer screening resulted in fewer cancer diagnoses in 2020 [Kaufman HW, Chen Z, Niles J, Fesko Y. Changes in the number of US patients with newly identified cancer before and during the coronavirus disease 2019 (COVID-19) pandemic. JAMA Netw Open 2020 Aug 03;3(8):e2017267 [FREE Full text] [CrossRef] [Medline]13,Alkatout I, Biebl M, Momenimovahed Z, Giovannucci E, Hadavandsiri F, Salehiniya H, et al. Has COVID-19 affected cancer screening programs? A systematic review. Front Oncol 2021;11:675038. [CrossRef] [Medline]14] and raises concerns that missed screenings and delayed cancer diagnoses will likely lead to late stage diagnosis and higher cancer-related mortality [Mast C, Munoz del Rio A. Delayed cancer screenings—a second look. Epic Research. 2020. URL: https://ehrn.org/articles/delayed-cancer-screenings-a-second-look [accessed 2021-08-03] 7,Alkatout I, Biebl M, Momenimovahed Z, Giovannucci E, Hadavandsiri F, Salehiniya H, et al. Has COVID-19 affected cancer screening programs? A systematic review. Front Oncol 2021;11:675038. [CrossRef] [Medline]14]. For example, a study (n=5167) reported a 13.5% (P=.03) decrease in colorectal cancer diagnoses during March 2020 to December 2020 compared to the number of patients diagnosed before the pandemic, and the same study showed the average number of stage three colorectal cancer cases (advanced stage cancers) diagnosed per month increased by 68.4% (P<.001) [Kuzuu K, Misawa N, Ashikari K, Kessoku T, Kato S, Hosono K, et al. Gastrointestinal cancer stage at diagnosis before and during the COVID-19 pandemic in Japan. JAMA Netw Open 2021 Sep 01;4(9):e2126334 [FREE Full text] [CrossRef] [Medline]15].
Health care providers must consider ways to increase cancer screening. Therefore, we conducted a scoping literature review to assist health care providers in identifying approaches for prioritizing and increasing cancer screening during the uncertainty of the COVID-19 pandemic. In this review, we focused on the most common cancer screenings: breast, cervical, and colorectal.
Methods
We used the scoping review framework outlined by Arksey and O’Malley [Arksey H, O'Malley L. Scoping studies: towards a methodological framework. Int J Soc Res Methodology 2005 Feb;8(1):19-32. [CrossRef]16] to identify and gather evidence from all sources in the field. The framework is comprised of four stages: (1) identification of relevant literature on multiple databases, (2) screening of identified literature and selection of relevant studies, (3) extraction of data, and (4) summarization and reporting of the findings [Arksey H, O'Malley L. Scoping studies: towards a methodological framework. Int J Soc Res Methodology 2005 Feb;8(1):19-32. [CrossRef]16]. The research questions of this review are what methods are recommended for risk stratification and triage of patients for cancer screenings, and what alternative cancer screening methods are recommended?
Stage 1: Identification of Relevant Literature
The keywords used to identify articles on PubMed and EBSCO databases were “cancer screening and coronavirus,” “cancer screening and COVID-19,” and “cancer screening and SARS-CoV-2.” The articles selected had to include breast, cervical, and colorectal cancer screening. Articles were screened for relevance based on the information provided in the abstract, and those deemed to be relevant by their abstract were fully reviewed. Additional literature was identified from the references of selected articles. A broader search strategy was adopted to include gray literature. These included commentaries and editorials published in peer-reviewed journals, recommendations published by professional organizations or societies, and medical news articles. The literature review ranged from January 1, 2020, to September 30, 2021.
Stage 2: Screening of Identified Literature and Selection of Relevant Studies
A total of 350 articles were identified from the databases, and an additional 53 articles were identified from references of the relevant articles. After pooling literature from different sources, we found 192 articles were duplicates; duplicates were excluded. Of the remaining 211 articles, 168 were deemed ineligible after screening the abstracts. Of the remaining 43 articles that were fully reviewed, 20 were excluded. Articles not focused on breast, cervical, and colorectal cancer screenings; not suggesting measures to address cancer screening during and after the pandemic; and providing suggestions not substantiated by past literature were excluded. A total of 23 articles were selected for this review. Two authors (SKS and PAM) reviewed the literature and agreed upon the selection of articles. The PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses) flowchart is provided in Figure 1.

Stage 3: Extraction of Data
The data points recorded were the article citations, type of article, type of cancer screening discussed, and key recommendations.
Stage 4: Summarization and Reporting of the Findings
The Results section and tables summarize the data regarding recommendations for risk stratification and triage and alternative cancer screening methods for breast, cervical, and colorectal cancer screenings and report concise information about alternative methods that can be used for cancer screenings.
Results
The articles included two primary categories of recommendations: (1) risk stratification and triage to prioritize screenings and (2) alternative methods to conduct cancer screenings (Table 1).
Approach | References | Strategies |
Risk stratification and triage |
|
|
Alternative screening methods |
|
|
Risk Stratification and Triage
Risk stratification and triage was recommended as an appropriate method for focusing cancer screenings during the COVID-19 pandemic. The recommendation focused on prioritizing those who are most susceptible to developing cancers [Croswell JM, Corley DA, Lafata JE, Haas JS, Inadomi JM, Kamineni A, National Cancer Institute Population-based Research to Optimize the Screening Process (PROSPR) II Consortium. Cancer screening in the U.S. through the COVID-19 pandemic, recovery, and beyond. Prev Med 2021 Oct;151:106595. [CrossRef] [Medline]6,Basu P, Alhomoud S, Taghavi K, Carvalho AL, Lucas E, Baussano I. Cancer screening in the coronavirus pandemic era: adjusting to a new situation. JCO Glob Oncol 2021 Mar;7:416-424 [FREE Full text] [CrossRef] [Medline]9,Castanon A, Rebolj M, Burger EA, de Kok IMCM, Smith MA, Hanley SJB, et al. Cervical screening during the COVID-19 pandemic: optimising recovery strategies. Lancet Public Health 2021 Jul;6(7):e522-e527 [FREE Full text] [CrossRef] [Medline]17-Seguin C. Breast cancer screenings for the older woman during a pandemic. Tar Heel Nurse 2020:12.32]. Potential criteria considered for categorizing patients into high risk included patients with an abnormal or suspicious result on the previous screening test [Miller J. Getting cervical cancer screening right. Home-based testing can increase access, but testing guidelines remain in flux. Clin Lab News 2021:14-17.27], age group [Castanon A, Rebolj M, Burger EA, de Kok IMCM, Smith MA, Hanley SJB, et al. Cervical screening during the COVID-19 pandemic: optimising recovery strategies. Lancet Public Health 2021 Jul;6(7):e522-e527 [FREE Full text] [CrossRef] [Medline]17,Kadakuntla A, Wang T, Medgyesy K, Rrapi E, Litynski J, Adynski G, et al. Colorectal cancer screening in the COVID-19 era. World J Gastrointest Oncol 2021 Apr 15;13(4):238-251 [FREE Full text] [CrossRef] [Medline]26,Seguin C. Breast cancer screenings for the older woman during a pandemic. Tar Heel Nurse 2020:12.32], sex [Kadakuntla A, Wang T, Medgyesy K, Rrapi E, Litynski J, Adynski G, et al. Colorectal cancer screening in the COVID-19 era. World J Gastrointest Oncol 2021 Apr 15;13(4):238-251 [FREE Full text] [CrossRef] [Medline]26], personal medical or family history [Cohen MA, Powell AM, Coleman JS, Keller JM, Livingston A, Anderson JR. Special ambulatory gynecologic considerations in the era of coronavirus disease 2019 (COVID-19) and implications for future practice. Am J Obstet Gynecol 2020 Sep;223(3):372-378 [FREE Full text] [CrossRef] [Medline]18,Isaacs C, Leininger W. Significant updates occurred in women’s health issues while the world was in survival mode. 2021 Presented at: 2021 American College of Obstetricians and Gynecologists Annual Clinical and Scientific Meeting; April 30-May 2, 2021; Virtual.24,Kadakuntla A, Wang T, Medgyesy K, Rrapi E, Litynski J, Adynski G, et al. Colorectal cancer screening in the COVID-19 era. World J Gastrointest Oncol 2021 Apr 15;13(4):238-251 [FREE Full text] [CrossRef] [Medline]26,Miller J. Getting cervical cancer screening right. Home-based testing can increase access, but testing guidelines remain in flux. Clin Lab News 2021:14-17.27], currently symptomatic or asymptomatic, predisposition to hereditary cancers, and inheritance of cancer-causing mutations [Cohen MA, Powell AM, Coleman JS, Keller JM, Livingston A, Anderson JR. Special ambulatory gynecologic considerations in the era of coronavirus disease 2019 (COVID-19) and implications for future practice. Am J Obstet Gynecol 2020 Sep;223(3):372-378 [FREE Full text] [CrossRef] [Medline]18,Kadakuntla A, Wang T, Medgyesy K, Rrapi E, Litynski J, Adynski G, et al. Colorectal cancer screening in the COVID-19 era. World J Gastrointest Oncol 2021 Apr 15;13(4):238-251 [FREE Full text] [CrossRef] [Medline]26].
Conversely, articles recommended the following patients be deferred until high priority patients are offered cancer screenings: patients with a recent cancer screening with normal results [Castanon A, Rebolj M, Burger EA, de Kok IMCM, Smith MA, Hanley SJB, et al. Cervical screening during the COVID-19 pandemic: optimising recovery strategies. Lancet Public Health 2021 Jul;6(7):e522-e527 [FREE Full text] [CrossRef] [Medline]17,Fagundes TP, Albuquerque RM, Miranda DLP, Landeiro LCG, Ayres GSF, Correia CCE, et al. Dealing with cancer screening in the COVID-19 era. Rev Assoc Med Bras (1992) 2021;67Suppl 1(Suppl 1):86-90 [FREE Full text] [CrossRef] [Medline]20]; patients who do not have any cancer-related symptoms [Cohen MA, Powell AM, Coleman JS, Keller JM, Livingston A, Anderson JR. Special ambulatory gynecologic considerations in the era of coronavirus disease 2019 (COVID-19) and implications for future practice. Am J Obstet Gynecol 2020 Sep;223(3):372-378 [FREE Full text] [CrossRef] [Medline]18,Helsper CW, Campbell C, Emery J, Neal RD, Li L, Rubin G, et al. Cancer has not gone away: a primary care perspective to support a balanced approach for timely cancer diagnosis during COVID-19. Eur J Cancer Care (Engl) 2020 Sep;29(5):e13290 [FREE Full text] [CrossRef] [Medline]22]; patients who have taken prophylactic measures such as the human papillomavirus (HPV) prophylactic vaccine [Castanon A, Rebolj M, Burger EA, de Kok IMCM, Smith MA, Hanley SJB, et al. Cervical screening during the COVID-19 pandemic: optimising recovery strategies. Lancet Public Health 2021 Jul;6(7):e522-e527 [FREE Full text] [CrossRef] [Medline]17,Fagundes TP, Albuquerque RM, Miranda DLP, Landeiro LCG, Ayres GSF, Correia CCE, et al. Dealing with cancer screening in the COVID-19 era. Rev Assoc Med Bras (1992) 2021;67Suppl 1(Suppl 1):86-90 [FREE Full text] [CrossRef] [Medline]20,Isaacs C, Leininger W. Significant updates occurred in women’s health issues while the world was in survival mode. 2021 Presented at: 2021 American College of Obstetricians and Gynecologists Annual Clinical and Scientific Meeting; April 30-May 2, 2021; Virtual.24]; and patients who do not have medical, personal, or family-related indication for immediate screening [Cohen MA, Powell AM, Coleman JS, Keller JM, Livingston A, Anderson JR. Special ambulatory gynecologic considerations in the era of coronavirus disease 2019 (COVID-19) and implications for future practice. Am J Obstet Gynecol 2020 Sep;223(3):372-378 [FREE Full text] [CrossRef] [Medline]18,National Cancer Institute’s PROSPR Consortium, Corley DA, Sedki M, Ritzwoller DP, Greenlee RT, Neslund-Dudas C, et al. Cancer screening during the coronavirus disease-2019 pandemic: a perspective from the National Cancer Institute's PROSPR Consortium. Gastroenterology 2021 Mar;160(4):999-1002 [FREE Full text] [CrossRef] [Medline]19,Houlihan N. Nurse can influence patients and the public to return to cancer screening. Oncology Nursing Society 2020:13.23,Riley S. Nursing strategies for optimizing patient care during the COVID-19 pandemic. The Oncology Nurse. 2020. URL: https://www.theoncologynurse.com/issue-archive/2020/october-2020-vol-13-no-5/18372-nursing-strategies-for-optimizing-patient-care-during-the-covid-19-pandemic [accessed 2022-02-18] 31].
Other recommended strategies included identifying areas facing most disparities [National Cancer Institute’s PROSPR Consortium, Corley DA, Sedki M, Ritzwoller DP, Greenlee RT, Neslund-Dudas C, et al. Cancer screening during the coronavirus disease-2019 pandemic: a perspective from the National Cancer Institute's PROSPR Consortium. Gastroenterology 2021 Mar;160(4):999-1002 [FREE Full text] [CrossRef] [Medline]19,Gorin SNS, Jimbo M, Heizelman R, Harmes KM, Harper DM. The future of cancer screening after COVID-19 may be at home. Cancer 2021 Feb 15;127(4):498-503. [CrossRef] [Medline]34], creating algorithms [Isaacs C, Leininger W. Significant updates occurred in women’s health issues while the world was in survival mode. 2021 Presented at: 2021 American College of Obstetricians and Gynecologists Annual Clinical and Scientific Meeting; April 30-May 2, 2021; Virtual.24] and using artificial intelligence [Orenstein BW. How COVID-19 has changed breast screening. Radiology Today. 2020. URL: https://www.radiologytoday.net/archive/rtSO20p10.shtml [accessed 2021-09-30] 28] to create cancer risk scores, leveraging in-person visits to assess cancer risk [Croswell JM, Corley DA, Lafata JE, Haas JS, Inadomi JM, Kamineni A, National Cancer Institute Population-based Research to Optimize the Screening Process (PROSPR) II Consortium. Cancer screening in the U.S. through the COVID-19 pandemic, recovery, and beyond. Prev Med 2021 Oct;151:106595. [CrossRef] [Medline]6], and providing the option of open access screenings where patients can schedule screenings and can be assigned a priority category by health care staff [Kadakuntla A, Wang T, Medgyesy K, Rrapi E, Litynski J, Adynski G, et al. Colorectal cancer screening in the COVID-19 era. World J Gastrointest Oncol 2021 Apr 15;13(4):238-251 [FREE Full text] [CrossRef] [Medline]26]. Some recommended screening high-risk patients through telemedicine prior to having them come into health care providers [Houlihan N. Nurse can influence patients and the public to return to cancer screening. Oncology Nursing Society 2020:13.23,Pediconi F, Galati F, Bernardi D, Belli P, Brancato B, Calabrese M, et al. Breast imaging and cancer diagnosis during the COVID-19 pandemic: recommendations from the Italian College of Breast Radiologists by SIRM. Radiol Med 2020 Oct;125(10):926-930 [FREE Full text] [CrossRef] [Medline]29].
In addition to risk stratification and triage, telemedicine was recommended to determine screening for patients with new complaints [Cohen MA, Powell AM, Coleman JS, Keller JM, Livingston A, Anderson JR. Special ambulatory gynecologic considerations in the era of coronavirus disease 2019 (COVID-19) and implications for future practice. Am J Obstet Gynecol 2020 Sep;223(3):372-378 [FREE Full text] [CrossRef] [Medline]18,National Cancer Institute’s PROSPR Consortium, Corley DA, Sedki M, Ritzwoller DP, Greenlee RT, Neslund-Dudas C, et al. Cancer screening during the coronavirus disease-2019 pandemic: a perspective from the National Cancer Institute's PROSPR Consortium. Gastroenterology 2021 Mar;160(4):999-1002 [FREE Full text] [CrossRef] [Medline]19,Helsper CW, Campbell C, Emery J, Neal RD, Li L, Rubin G, et al. Cancer has not gone away: a primary care perspective to support a balanced approach for timely cancer diagnosis during COVID-19. Eur J Cancer Care (Engl) 2020 Sep;29(5):e13290 [FREE Full text] [CrossRef] [Medline]22]. Several articles noted the importance of implementing preventive measures such as COVID-19 screening prior to the procedures [Croswell JM, Corley DA, Lafata JE, Haas JS, Inadomi JM, Kamineni A, National Cancer Institute Population-based Research to Optimize the Screening Process (PROSPR) II Consortium. Cancer screening in the U.S. through the COVID-19 pandemic, recovery, and beyond. Prev Med 2021 Oct;151:106595. [CrossRef] [Medline]6,Basu P, Alhomoud S, Taghavi K, Carvalho AL, Lucas E, Baussano I. Cancer screening in the coronavirus pandemic era: adjusting to a new situation. JCO Glob Oncol 2021 Mar;7:416-424 [FREE Full text] [CrossRef] [Medline]9,Kadakuntla A, Wang T, Medgyesy K, Rrapi E, Litynski J, Adynski G, et al. Colorectal cancer screening in the COVID-19 era. World J Gastrointest Oncol 2021 Apr 15;13(4):238-251 [FREE Full text] [CrossRef] [Medline]26], maintaining hygiene measures [National Cancer Institute’s PROSPR Consortium, Corley DA, Sedki M, Ritzwoller DP, Greenlee RT, Neslund-Dudas C, et al. Cancer screening during the coronavirus disease-2019 pandemic: a perspective from the National Cancer Institute's PROSPR Consortium. Gastroenterology 2021 Mar;160(4):999-1002 [FREE Full text] [CrossRef] [Medline]19,Seguin C. Breast cancer screenings for the older woman during a pandemic. Tar Heel Nurse 2020:12.32], and social distancing in waiting rooms [Seguin C. Breast cancer screenings for the older woman during a pandemic. Tar Heel Nurse 2020:12.32].
Alternative Screening Methods
Several studies discussed using novel and alternative screening methods that do not require an in-person clinic visit and can effectively screen patients for cancers (Table 2). Mailing of self-collection sampling kits was widely suggested as a screening strategy for cervical and colorectal cancers [Croswell JM, Corley DA, Lafata JE, Haas JS, Inadomi JM, Kamineni A, National Cancer Institute Population-based Research to Optimize the Screening Process (PROSPR) II Consortium. Cancer screening in the U.S. through the COVID-19 pandemic, recovery, and beyond. Prev Med 2021 Oct;151:106595. [CrossRef] [Medline]6,Castanon A, Rebolj M, Burger EA, de Kok IMCM, Smith MA, Hanley SJB, et al. Cervical screening during the COVID-19 pandemic: optimising recovery strategies. Lancet Public Health 2021 Jul;6(7):e522-e527 [FREE Full text] [CrossRef] [Medline]17,National Cancer Institute’s PROSPR Consortium, Corley DA, Sedki M, Ritzwoller DP, Greenlee RT, Neslund-Dudas C, et al. Cancer screening during the coronavirus disease-2019 pandemic: a perspective from the National Cancer Institute's PROSPR Consortium. Gastroenterology 2021 Mar;160(4):999-1002 [FREE Full text] [CrossRef] [Medline]19-Gralnek IM, Hassan C, Beilenhoff U, Antonelli G, Ebigbo A, Pellisé M, et al. ESGE and ESGENA Position Statement on gastrointestinal endoscopy and COVID-19: an update on guidance during the post-lockdown phase and selected results from a membership survey. Endoscopy 2020 Oct;52(10):891-898 [FREE Full text] [CrossRef] [Medline]21,Issaka RB, Somsouk M. Colorectal cancer screening and prevention in the COVID-19 era. JAMA Health Forum 2020 May;1(5):e200588 [FREE Full text] [CrossRef] [Medline]25-Orenstein BW. How COVID-19 has changed breast screening. Radiology Today. 2020.
URL: https://www.radiologytoday.net/archive/rtSO20p10.shtml [accessed 2021-09-30]
28,Balzora S, Issaka RB, Anyane-Yeboa A, Gray DM, May FP. Impact of COVID-19 on colorectal cancer disparities and the way forward. Gastrointest Endosc 2020 Oct;92(4):946-950 [FREE Full text] [CrossRef] [Medline]33-Ricciardiello L, Ferrari C, Cameletti M, Gaianill F, Buttitta F, Bazzoli F, et al. Impact of SARS-CoV-2 pandemic on colorectal cancer screening delay: effect on stage shift and increased mortality. Clin Gastroenterol Hepatol 2021 Jul;19(7):1410-1417.e9 [FREE Full text] [CrossRef] [Medline]36]. Cervical cancer screening included mailing or pharmacy pickup of kits for self-sampling of vaginal or urine samples that can be tested for HPV strains most likely to cause cancers [Castanon A, Rebolj M, Burger EA, de Kok IMCM, Smith MA, Hanley SJB, et al. Cervical screening during the COVID-19 pandemic: optimising recovery strategies. Lancet Public Health 2021 Jul;6(7):e522-e527 [FREE Full text] [CrossRef] [Medline]17,Miller J. Getting cervical cancer screening right. Home-based testing can increase access, but testing guidelines remain in flux. Clin Lab News 2021:14-17.27,Gorin SNS, Jimbo M, Heizelman R, Harmes KM, Harper DM. The future of cancer screening after COVID-19 may be at home. Cancer 2021 Feb 15;127(4):498-503. [CrossRef] [Medline]34,Miller MJ, Xu L, Qin J, Hahn EE, Ngo-Metzger Q, Mittman B, et al. Impact of COVID-19 on cervical cancer screening rates among women aged 21-65 years in a large integrated health care system - Southern California, January 1-September 30, 2019, and January 1-September 30, 2020. MMWR Morb Mortal Wkly Rep 2021 Jan 29;70(4):109-113. [CrossRef] [Medline]35]. Stool-based self-collection kits that are performed at home and mailed for screening were recommended for colorectal cancers [Croswell JM, Corley DA, Lafata JE, Haas JS, Inadomi JM, Kamineni A, National Cancer Institute Population-based Research to Optimize the Screening Process (PROSPR) II Consortium. Cancer screening in the U.S. through the COVID-19 pandemic, recovery, and beyond. Prev Med 2021 Oct;151:106595. [CrossRef] [Medline]6,National Cancer Institute’s PROSPR Consortium, Corley DA, Sedki M, Ritzwoller DP, Greenlee RT, Neslund-Dudas C, et al. Cancer screening during the coronavirus disease-2019 pandemic: a perspective from the National Cancer Institute's PROSPR Consortium. Gastroenterology 2021 Mar;160(4):999-1002 [FREE Full text] [CrossRef] [Medline]19,Fagundes TP, Albuquerque RM, Miranda DLP, Landeiro LCG, Ayres GSF, Correia CCE, et al. Dealing with cancer screening in the COVID-19 era. Rev Assoc Med Bras (1992) 2021;67Suppl 1(Suppl 1):86-90 [FREE Full text] [CrossRef] [Medline]20,Issaka RB, Somsouk M. Colorectal cancer screening and prevention in the COVID-19 era. JAMA Health Forum 2020 May;1(5):e200588 [FREE Full text] [CrossRef] [Medline]25,Kadakuntla A, Wang T, Medgyesy K, Rrapi E, Litynski J, Adynski G, et al. Colorectal cancer screening in the COVID-19 era. World J Gastrointest Oncol 2021 Apr 15;13(4):238-251 [FREE Full text] [CrossRef] [Medline]26,Balzora S, Issaka RB, Anyane-Yeboa A, Gray DM, May FP. Impact of COVID-19 on colorectal cancer disparities and the way forward. Gastrointest Endosc 2020 Oct;92(4):946-950 [FREE Full text] [CrossRef] [Medline]33-Ricciardiello L, Ferrari C, Cameletti M, Gaianill F, Buttitta F, Bazzoli F, et al. Impact of SARS-CoV-2 pandemic on colorectal cancer screening delay: effect on stage shift and increased mortality. Clin Gastroenterol Hepatol 2021 Jul;19(7):1410-1417.e9 [FREE Full text] [CrossRef] [Medline]36]. Although self–breast examinations can be done at home, they do not take the place of mammography; therefore, articles recommended implementing and expanding mobile screening units [Orenstein BW. How COVID-19 has changed breast screening. Radiology Today. 2020.
URL: https://www.radiologytoday.net/archive/rtSO20p10.shtml [accessed 2021-09-30]
28,Puricelli Perin DM, Christensen T, Burón A, Haas JS, Kamineni A, Pashayan N, International Cancer Screening Network ICSN. Interruption of cancer screening services due to COVID-19 pandemic: lessons from previous disasters. Prev Med Rep 2021 Sep;23:101399 [FREE Full text] [CrossRef] [Medline]30].
Cancer type/cancer risk factors | Conventional recommendation/practices | Variation in approaches |
Breast cancer |
|
|
Cervical cancer |
|
|
Colorectal cancer |
|
|
aHPV: human papillomavirus.
bCT: computed tomography.
Discussion
The number of cancer screenings missed during the COVID-19 pandemic will likely lead to a sharp increase in the number of late-stage cancer diagnoses and increased cancer mortality [Alkatout I, Biebl M, Momenimovahed Z, Giovannucci E, Hadavandsiri F, Salehiniya H, et al. Has COVID-19 affected cancer screening programs? A systematic review. Front Oncol 2021;11:675038. [CrossRef] [Medline]14]. As health care providers look for ways to focus their cancer screening efforts, this review provides insights into risk stratification and triage approaches and alternative screening approaches that can be adopted to reduce the impact of COVID-19 on cancer mortality.
Risk stratification and triage approaches focused on prioritizing patients based on personal characteristics, medical history, cancer screening history, and communities facing highest cancer disparities [Croswell JM, Corley DA, Lafata JE, Haas JS, Inadomi JM, Kamineni A, National Cancer Institute Population-based Research to Optimize the Screening Process (PROSPR) II Consortium. Cancer screening in the U.S. through the COVID-19 pandemic, recovery, and beyond. Prev Med 2021 Oct;151:106595. [CrossRef] [Medline]6,Basu P, Alhomoud S, Taghavi K, Carvalho AL, Lucas E, Baussano I. Cancer screening in the coronavirus pandemic era: adjusting to a new situation. JCO Glob Oncol 2021 Mar;7:416-424 [FREE Full text] [CrossRef] [Medline]9,Castanon A, Rebolj M, Burger EA, de Kok IMCM, Smith MA, Hanley SJB, et al. Cervical screening during the COVID-19 pandemic: optimising recovery strategies. Lancet Public Health 2021 Jul;6(7):e522-e527 [FREE Full text] [CrossRef] [Medline]17-Seguin C. Breast cancer screenings for the older woman during a pandemic. Tar Heel Nurse 2020:12.32]. The literature suggests that older patients at higher risk should be given priority since the risk of cancer increases with age [Castanon A, Rebolj M, Burger EA, de Kok IMCM, Smith MA, Hanley SJB, et al. Cervical screening during the COVID-19 pandemic: optimising recovery strategies. Lancet Public Health 2021 Jul;6(7):e522-e527 [FREE Full text] [CrossRef] [Medline]17,Kadakuntla A, Wang T, Medgyesy K, Rrapi E, Litynski J, Adynski G, et al. Colorectal cancer screening in the COVID-19 era. World J Gastrointest Oncol 2021 Apr 15;13(4):238-251 [FREE Full text] [CrossRef] [Medline]26].
Prioritizing high-risk patients based on the past screening history could help the health care provider prioritize care based on the probability of patients developing cancerous lesions. Several studies have shown that prioritizing high-risk patients based on past medical history is important [Croswell JM, Corley DA, Lafata JE, Haas JS, Inadomi JM, Kamineni A, National Cancer Institute Population-based Research to Optimize the Screening Process (PROSPR) II Consortium. Cancer screening in the U.S. through the COVID-19 pandemic, recovery, and beyond. Prev Med 2021 Oct;151:106595. [CrossRef] [Medline]6,Basu P, Alhomoud S, Taghavi K, Carvalho AL, Lucas E, Baussano I. Cancer screening in the coronavirus pandemic era: adjusting to a new situation. JCO Glob Oncol 2021 Mar;7:416-424 [FREE Full text] [CrossRef] [Medline]9,Castanon A, Rebolj M, Burger EA, de Kok IMCM, Smith MA, Hanley SJB, et al. Cervical screening during the COVID-19 pandemic: optimising recovery strategies. Lancet Public Health 2021 Jul;6(7):e522-e527 [FREE Full text] [CrossRef] [Medline]17-Seguin C. Breast cancer screenings for the older woman during a pandemic. Tar Heel Nurse 2020:12.32], and studies have reported the effectiveness of the personalized screening approach, demonstrating that the one-size-fits-all approach may not be the best strategy [Sankatsing VDV, van Ravesteyn NT, Heijnsdijk EAM, Broeders MJM, de Koning HJ. Risk stratification in breast cancer screening: cost-effectiveness and harm-benefit ratios for low-risk and high-risk women. Int J Cancer 2020 Dec 01;147(11):3059-3067. [CrossRef] [Medline]37-Thomas C, Mandrik O, Saunders CL, Thompson D, Whyte S, Griffin S, et al. The costs and benefits of risk stratification for colorectal cancer screening based on phenotypic and genetic risk: a health economic analysis. Cancer Prev Res (Phila) 2021 Aug;14(8):811-822 [FREE Full text] [CrossRef] [Medline]40]. In addition, using algorithms and artificial intelligence to categorize and triage high-risk patients will help navigate large data sets and assist physicians in the decision-making process [Isaacs C, Leininger W. Significant updates occurred in women’s health issues while the world was in survival mode. 2021 Presented at: 2021 American College of Obstetricians and Gynecologists Annual Clinical and Scientific Meeting; April 30-May 2, 2021; Virtual.24,Orenstein BW. How COVID-19 has changed breast screening. Radiology Today. 2020. URL: https://www.radiologytoday.net/archive/rtSO20p10.shtml [accessed 2021-09-30] 28].
Alternative cancer screening approaches focused on tests that do not require a clinic or hospital visit can be used to collect samples at home. These alternative methods allow initial screening outside the traditional clinical environment, take fewer clinical resources, and reduce exposure risk to patients. Alternative at-home screening modalities exist for cervical cancer screening [Sabeena S, Kuriakose S, Binesh D, Abdulmajeed J, Dsouza G, Ramachandran A, et al. The utility of urine-based sampling for cervical cancer screening in low-resource settings. Asian Pac J Cancer Prev 2019 Aug 01;20(8):2409-2413 [FREE Full text] [CrossRef] [Medline]41-Ørnskov D, Jochumsen K, Steiner PH, Grunnet IM, Lykkebo AW, Waldstrøm M. Clinical performance and acceptability of self-collected vaginal and urine samples compared with clinician-taken cervical samples for HPV testing among women referred for colposcopy. A cross-sectional study. BMJ Open 2021 Mar 05;11(3):e041512 [FREE Full text] [CrossRef] [Medline]43] and colorectal cancer [Kadakuntla A, Wang T, Medgyesy K, Rrapi E, Litynski J, Adynski G, et al. Colorectal cancer screening in the COVID-19 era. World J Gastrointest Oncol 2021 Apr 15;13(4):238-251 [FREE Full text] [CrossRef] [Medline]26]. Studies have evaluated the efficacy of detecting cervical intraepithelial lesions using self-collected samples with samples collected in the doctor’s office and concluded that self-sampling is a safe and effective alternative to screen for cervical cancers [Tranberg M, Jensen JS, Bech BH, Andersen B. Urine collection in cervical cancer screening - analytical comparison of two HPV DNA assays. BMC Infect Dis 2020 Dec 04;20(1):926 [FREE Full text] [CrossRef] [Medline]42,Ørnskov D, Jochumsen K, Steiner PH, Grunnet IM, Lykkebo AW, Waldstrøm M. Clinical performance and acceptability of self-collected vaginal and urine samples compared with clinician-taken cervical samples for HPV testing among women referred for colposcopy. A cross-sectional study. BMJ Open 2021 Mar 05;11(3):e041512 [FREE Full text] [CrossRef] [Medline]43]. Similar to cervical cancer, colorectal cancer screenings can be effectively conducted using noninvasive stool-based test kits at home [Walsh JM, Salazar R, Nguyen TT, Kaplan C, Nguyen L, Hwang J, et al. Healthy colon, healthy life: a novel colorectal cancer screening intervention. Am J Prev Med 2010 Jul;39(1):1-14 [FREE Full text] [CrossRef] [Medline]44,Christy SM, Davis SN, Williams KR, Zhao X, Govindaraju SK, Quinn GP, et al. A community-based trial of educational interventions with fecal immunochemical tests for colorectal cancer screening uptake among blacks in community settings. Cancer 2016 Nov 15;122(21):3288-3296. [CrossRef] [Medline]45]. Studies have shown that stool-based test kits can help reach underresourced communities and increase colorectal cancer screening uptake [Preston MA, Glover-Collins K, Ross L, Porter A, Bursac Z, Woods D, et al. Colorectal cancer screening in rural and poor-resourced communities. Am J Surg 2018 Aug;216(2):245-250 [FREE Full text] [CrossRef] [Medline]46]. Although the stool-based tests have a high false-positive rate [Malagón M, Ramió-Pujol S, Serrano M, Amoedo J, Oliver L, Bahí A, et al. New fecal bacterial signature for colorectal cancer screening reduces the fecal immunochemical test false-positive rate in a screening population. PLoS One 2020;15(12):e0243158. [CrossRef] [Medline]47], patients testing negative can be assured that they do not have colorectal cancers [Kadakuntla A, Wang T, Medgyesy K, Rrapi E, Litynski J, Adynski G, et al. Colorectal cancer screening in the COVID-19 era. World J Gastrointest Oncol 2021 Apr 15;13(4):238-251 [FREE Full text] [CrossRef] [Medline]26].
Follow-up for abnormal results from at-home tests can be provided and help focus limited clinical resources. Although there are not at-home alternatives for mammography, mobile units can provide a way to reach the community [Orenstein BW. How COVID-19 has changed breast screening. Radiology Today. 2020. URL: https://www.radiologytoday.net/archive/rtSO20p10.shtml [accessed 2021-09-30] 28,Puricelli Perin DM, Christensen T, Burón A, Haas JS, Kamineni A, Pashayan N, International Cancer Screening Network ICSN. Interruption of cancer screening services due to COVID-19 pandemic: lessons from previous disasters. Prev Med Rep 2021 Sep;23:101399 [FREE Full text] [CrossRef] [Medline]30] and reduce exposure risk.
Although the COVID-19 pandemic had devastating effects on population health globally, it could be an opportunity to adapt and evolve our cancer screening recommendations. Disruption often creates innovation, and focus on alternative methods for cancer screenings may help reach rural and underresourced areas after the pandemic has ended.
Acknowledgments
Funding support for this study was provided by a Translational Research Institute grant (#UL1 TR003107) from the National Center for Advancing Translational Sciences of the National Institutes of Health. The content of this paper is solely the responsibility of the authors and does not necessarily represent the official views of the funders.
The authors would also like to thank Erin Gloster for her review and formatting assistance.
Conflicts of Interest
None declared.
Multimedia Appendix 1
PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses) checklist.
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Abbreviations
HPV: human papillomavirus |
PRISMA: Preferred Reporting Items for Systematic Reviews and Meta-Analyses |
Edited by A Mavragani; submitted 20.10.21; peer-reviewed by N Hardikar, J McGuinness; comments to author 06.01.22; revised version received 25.01.22; accepted 03.02.22; published 24.02.22
Copyright©Sumit K Shah, Pearl A McElfish. Originally published in JMIR Cancer (https://cancer.jmir.org), 24.02.2022.
This is an open-access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work, first published in JMIR Cancer, is properly cited. The complete bibliographic information, a link to the original publication on https://cancer.jmir.org/, as well as this copyright and license information must be included.