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<?covid-19-tdm?>
<article xmlns:xlink="http://www.w3.org/1999/xlink" article-type="research-article" dtd-version="2.0">
  <front>
    <journal-meta>
      <journal-id journal-id-type="publisher-id">JC</journal-id>
      <journal-id journal-id-type="nlm-ta">JMIR Cancer</journal-id>
      <journal-title>JMIR Cancer</journal-title>
      <issn pub-type="epub">2369-1999</issn>
      <publisher>
        <publisher-name>JMIR Publications</publisher-name>
        <publisher-loc>Toronto, Canada</publisher-loc>
      </publisher>
    </journal-meta>
    <article-meta>
      <article-id pub-id-type="publisher-id">v8i1e34392</article-id>
      <article-id pub-id-type="pmid">35142621</article-id>
      <article-id pub-id-type="doi">10.2196/34392</article-id>
      <article-categories>
        <subj-group subj-group-type="heading">
          <subject>Review</subject>
        </subj-group>
        <subj-group subj-group-type="article-type">
          <subject>Review</subject>
        </subj-group>
      </article-categories>
      <title-group>
        <article-title>Cancer Screening Recommendations During the COVID-19 Pandemic: Scoping Review</article-title>
      </title-group>
      <contrib-group>
        <contrib contrib-type="editor">
          <name>
            <surname>Mavragani</surname>
            <given-names>Amaryllis</given-names>
          </name>
        </contrib>
      </contrib-group>
      <contrib-group>
        <contrib contrib-type="reviewer">
          <name>
            <surname>Hardikar</surname>
            <given-names>Navneetha</given-names>
          </name>
        </contrib>
        <contrib contrib-type="reviewer">
          <name>
            <surname>McGuinness</surname>
            <given-names>Julia</given-names>
          </name>
        </contrib>
      </contrib-group>
      <contrib-group>
        <contrib id="contrib1" contrib-type="author">
          <name name-style="western">
            <surname>Shah</surname>
            <given-names>Sumit K</given-names>
          </name>
          <degrees>MPH, MD</degrees>
          <xref rid="aff1" ref-type="aff">1</xref>
          <ext-link ext-link-type="orcid">https://orcid.org/0000-0003-2916-8045</ext-link>
        </contrib>
        <contrib id="contrib2" contrib-type="author" corresp="yes">
          <name name-style="western">
            <surname>McElfish</surname>
            <given-names>Pearl A</given-names>
          </name>
          <degrees>MBA, PhD</degrees>
          <xref rid="aff2" ref-type="aff">2</xref>
          <address>
            <institution>College of Medicine</institution>
            <institution>University of Arkansas for Medical Sciences Northwest</institution>
            <addr-line>1125 N College Avenue</addr-line>
            <addr-line>Fayetteville, AR, 72703</addr-line>
            <country>United States</country>
            <phone>1 (479) 713 8680</phone>
            <email>pamcelfish@uams.edu</email>
          </address>
          <ext-link ext-link-type="orcid">https://orcid.org/0000-0002-4033-6241</ext-link>
        </contrib>
      </contrib-group>
      <aff id="aff1">
        <label>1</label>
        <institution>Office of Community Health and Research</institution>
        <institution>University of Arkansas for Medical Sciences Northwest</institution>
        <addr-line>Fayetteville, AR</addr-line>
        <country>United States</country>
      </aff>
      <aff id="aff2">
        <label>2</label>
        <institution>College of Medicine</institution>
        <institution>University of Arkansas for Medical Sciences Northwest</institution>
        <addr-line>Fayetteville, AR</addr-line>
        <country>United States</country>
      </aff>
      <author-notes>
        <corresp>Corresponding Author: Pearl A McElfish <email>pamcelfish@uams.edu</email></corresp>
      </author-notes>
      <pub-date pub-type="collection">
        <season>Jan-Mar</season>
        <year>2022</year>
      </pub-date>
      <pub-date pub-type="epub">
        <day>24</day>
        <month>2</month>
        <year>2022</year>
      </pub-date>
      <volume>8</volume>
      <issue>1</issue>
      <elocation-id>e34392</elocation-id>
      <history>
        <date date-type="received">
          <day>20</day>
          <month>10</month>
          <year>2021</year>
        </date>
        <date date-type="rev-request">
          <day>6</day>
          <month>1</month>
          <year>2022</year>
        </date>
        <date date-type="rev-recd">
          <day>25</day>
          <month>1</month>
          <year>2022</year>
        </date>
        <date date-type="accepted">
          <day>3</day>
          <month>2</month>
          <year>2022</year>
        </date>
      </history>
      <copyright-statement>©Sumit K Shah, Pearl A McElfish. Originally published in JMIR Cancer (https://cancer.jmir.org), 24.02.2022.</copyright-statement>
      <copyright-year>2022</copyright-year>
      <license license-type="open-access" xlink:href="https://creativecommons.org/licenses/by/4.0/">
        <p>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.</p>
      </license>
      <self-uri xlink:href="https://cancer.jmir.org/2022/1/e34392" xlink:type="simple"/>
      <abstract>
        <sec sec-type="background">
          <title>Background</title>
          <p>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.</p>
        </sec>
        <sec sec-type="objective">
          <title>Objective</title>
          <p>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.</p>
        </sec>
        <sec sec-type="methods">
          <title>Methods</title>
          <p>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.</p>
        </sec>
        <sec sec-type="results">
          <title>Results</title>
          <p>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.</p>
        </sec>
        <sec sec-type="conclusions">
          <title>Conclusions</title>
          <p>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.</p>
        </sec>
      </abstract>
      <kwd-group>
        <kwd>COVID-19</kwd>
        <kwd>cancer prevention and early detection</kwd>
        <kwd>cancer screenings</kwd>
        <kwd>breast cancer screening</kwd>
        <kwd>cervical cancer screening</kwd>
        <kwd>colorectal cancer screening</kwd>
      </kwd-group>
    </article-meta>
  </front>
  <body>
    <sec sec-type="introduction">
      <title>Introduction</title>
      <p>Cancer-associated mortality is the second leading cause of death in the United States [<xref ref-type="bibr" rid="ref1">1</xref>,<xref ref-type="bibr" rid="ref2">2</xref>]. Cancer screening tests are recommended to prevent cancer-associated mortality by detecting precancerous and cancerous lesions in early stages [<xref ref-type="bibr" rid="ref3">3</xref>]. The most common routine cancer screenings include breast, colorectal, and cervical [<xref ref-type="bibr" rid="ref4">4</xref>].</p>
      <p>The COVID-19 pandemic disrupted the use of preventive health care services [<xref ref-type="bibr" rid="ref5">5</xref>]; there was an abrupt decline in cancer screening services throughout 2020 [<xref ref-type="bibr" rid="ref6">6</xref>]. 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 [<xref ref-type="bibr" rid="ref7">7</xref>]. 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 [<xref ref-type="bibr" rid="ref8">8</xref>].</p>
      <p>The reduction in cancer screenings and other preventative and diagnostic care have been attributed to both health care provider and patient constraints [<xref ref-type="bibr" rid="ref9">9</xref>-<xref ref-type="bibr" rid="ref12">12</xref>]. Health care provider constraints included restrictions on elective procedures [<xref ref-type="bibr" rid="ref9">9</xref>] and a shortage of health care staff due to redeployment to help with pandemic-related care [<xref ref-type="bibr" rid="ref9">9</xref>,<xref ref-type="bibr" rid="ref10">10</xref>]. 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 [<xref ref-type="bibr" rid="ref11">11</xref>] and fear of contracting COVID-19 during in-person health care visits [<xref ref-type="bibr" rid="ref12">12</xref>].</p>
      <p>The decline in cancer screening resulted in fewer cancer diagnoses in 2020 [<xref ref-type="bibr" rid="ref13">13</xref>,<xref ref-type="bibr" rid="ref14">14</xref>] and raises concerns that missed screenings and delayed cancer diagnoses will likely lead to late stage diagnosis and higher cancer-related mortality [<xref ref-type="bibr" rid="ref7">7</xref>,<xref ref-type="bibr" rid="ref14">14</xref>]. For example, a study (n=5167) reported a 13.5% (<italic>P</italic>=.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% (<italic>P</italic>&#60;.001) [<xref ref-type="bibr" rid="ref15">15</xref>].</p>
      <p>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.</p>
    </sec>
    <sec sec-type="methods">
      <title>Methods</title>
      <p>We used the scoping review framework outlined by Arksey and O’Malley [<xref ref-type="bibr" rid="ref16">16</xref>] 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 [<xref ref-type="bibr" rid="ref16">16</xref>]. 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?</p>
      <sec>
        <title>Stage 1: Identification of Relevant Literature</title>
        <p>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.</p>
      </sec>
      <sec>
        <title>Stage 2: Screening of Identified Literature and Selection of Relevant Studies</title>
        <p>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 <xref rid="figure1" ref-type="fig">Figure 1</xref>.</p>
        <fig id="figure1" position="float">
          <label>Figure 1</label>
          <caption>
            <p>PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses) flow diagram for new systematic reviews, which includes searches of databases only.</p>
          </caption>
          <graphic xlink:href="cancer_v8i1e34392_fig1.png" alt-version="no" mimetype="image" position="float" xlink:type="simple"/>
        </fig>
      </sec>
      <sec>
        <title>Stage 3: Extraction of Data</title>
        <p>The data points recorded were the article citations, type of article, type of cancer screening discussed, and key recommendations.</p>
      </sec>
      <sec>
        <title>Stage 4: Summarization and Reporting of the Findings</title>
        <p>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.</p>
      </sec>
    </sec>
    <sec sec-type="results">
      <title>Results</title>
      <p>The articles included two primary categories of recommendations: (1) risk stratification and triage to prioritize screenings and (2) alternative methods to conduct cancer screenings (<xref ref-type="table" rid="table1">Table 1</xref>).</p>
      <table-wrap position="float" id="table1">
        <label>Table 1</label>
        <caption>
          <p>Summary of safely resuming cancer screening services.</p>
        </caption>
        <table width="1000" cellpadding="5" cellspacing="0" border="1" rules="groups" frame="hsides">
          <col width="300"/>
          <col width="300"/>
          <col width="400"/>
          <thead>
            <tr valign="top">
              <td>Approach</td>
              <td>References</td>
              <td>Strategies</td>
            </tr>
          </thead>
          <tbody>
            <tr valign="top">
              <td>Risk stratification and triage</td>
              <td>
                <list list-type="bullet">
                  <list-item>
                    <p>Basu et al 2021 [<xref ref-type="bibr" rid="ref9">9</xref>]</p>
                  </list-item>
                  <list-item>
                    <p>Castanon et al 2021 [<xref ref-type="bibr" rid="ref17">17</xref>]</p>
                  </list-item>
                  <list-item>
                    <p>Cohen et al 2020 [<xref ref-type="bibr" rid="ref18">18</xref>]</p>
                  </list-item>
                  <list-item>
                    <p>Corley et al 2021 [<xref ref-type="bibr" rid="ref19">19</xref>]</p>
                  </list-item>
                  <list-item>
                    <p>Croswell et al 2021 [<xref ref-type="bibr" rid="ref6">6</xref>]</p>
                  </list-item>
                  <list-item>
                    <p>Fagundes et al 2021 [<xref ref-type="bibr" rid="ref20">20</xref>]</p>
                  </list-item>
                  <list-item>
                    <p>Gralnek et al 2020 [<xref ref-type="bibr" rid="ref21">21</xref>]</p>
                  </list-item>
                  <list-item>
                    <p>Helsper et al 2020 [<xref ref-type="bibr" rid="ref22">22</xref>]</p>
                  </list-item>
                  <list-item>
                    <p>Houlihan 2020 [<xref ref-type="bibr" rid="ref23">23</xref>]</p>
                  </list-item>
                  <list-item>
                    <p>Isaacs and Leininger 2021 [<xref ref-type="bibr" rid="ref24">24</xref>]</p>
                  </list-item>
                  <list-item>
                    <p>Issaka and Somsouk 2020 [<xref ref-type="bibr" rid="ref25">25</xref>]</p>
                  </list-item>
                  <list-item>
                    <p>Kadakuntla et al 2021 [<xref ref-type="bibr" rid="ref26">26</xref>]</p>
                  </list-item>
                  <list-item>
                    <p>Miller 2021 [<xref ref-type="bibr" rid="ref27">27</xref>]</p>
                  </list-item>
                  <list-item>
                    <p>Orenstein 2020 [<xref ref-type="bibr" rid="ref28">28</xref>]</p>
                  </list-item>
                  <list-item>
                    <p>Pediconi et al 2020 [<xref ref-type="bibr" rid="ref29">29</xref>]</p>
                  </list-item>
                  <list-item>
                    <p>Puricelli Perin et al 2021 [<xref ref-type="bibr" rid="ref30">30</xref>]</p>
                  </list-item>
                  <list-item>
                    <p>Riley 2020 [<xref ref-type="bibr" rid="ref31">31</xref>]</p>
                  </list-item>
                  <list-item>
                    <p>Seguin 2020 [<xref ref-type="bibr" rid="ref32">32</xref>]</p>
                  </list-item>
                </list>
              </td>
              <td>
                <list list-type="bullet">
                  <list-item>
                    <p>Stratify patients into high-risk, average-risk, and low-risk categories based on age, sex, past medical history, past personal history, or region/area of residence</p>
                  </list-item>
                  <list-item>
                    <p>Triage patients based on risk category, prioritizing patients at high risk of cancer, followed by average-risk and low-risk patients</p>
                  </list-item>
                </list>
              </td>
            </tr>
            <tr valign="top">
              <td>Alternative screening methods</td>
              <td>
                <list list-type="bullet">
                  <list-item>
                    <p>Balzora et al 2020 [<xref ref-type="bibr" rid="ref33">33</xref>]</p>
                  </list-item>
                  <list-item>
                    <p>Castanon et al 2021 [<xref ref-type="bibr" rid="ref17">17</xref>]</p>
                  </list-item>
                  <list-item>
                    <p>Corley et al 2021 [<xref ref-type="bibr" rid="ref19">19</xref>]</p>
                  </list-item>
                  <list-item>
                    <p>Croswell et al 2021 [<xref ref-type="bibr" rid="ref6">6</xref>]</p>
                  </list-item>
                  <list-item>
                    <p>Fagundes et al 2021 [<xref ref-type="bibr" rid="ref20">20</xref>]</p>
                  </list-item>
                  <list-item>
                    <p>Gorin et al 2021 [<xref ref-type="bibr" rid="ref34">34</xref>]</p>
                  </list-item>
                  <list-item>
                    <p>Issaka and Somsouk 2020 [<xref ref-type="bibr" rid="ref25">25</xref>]</p>
                  </list-item>
                  <list-item>
                    <p>Kadakuntla et al 2021 [<xref ref-type="bibr" rid="ref26">26</xref>]</p>
                  </list-item>
                  <list-item>
                    <p>Miller 2021 [<xref ref-type="bibr" rid="ref27">27</xref>]</p>
                  </list-item>
                  <list-item>
                    <p>Miller et al 2021 [<xref ref-type="bibr" rid="ref35">35</xref>]</p>
                  </list-item>
                  <list-item>
                    <p>Orenstein 2020 [<xref ref-type="bibr" rid="ref28">28</xref>]</p>
                  </list-item>
                  <list-item>
                    <p>Ricciardiello et al 2021 [<xref ref-type="bibr" rid="ref36">36</xref>]</p>
                  </list-item>
                </list>
              </td>
              <td>
                <list list-type="bullet">
                  <list-item>
                    <p>Self-collecting of vaginal or urine samples for cervical cancer screening</p>
                  </list-item>
                  <list-item>
                    <p>Self-collection of stool sample for colorectal cancer screening</p>
                  </list-item>
                  <list-item>
                    <p>Mobile units outside primary health care facilities for breast cancer screening</p>
                  </list-item>
                </list>
              </td>
            </tr>
          </tbody>
        </table>
      </table-wrap>
      <sec>
        <title>Risk Stratification and Triage</title>
        <p>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 [<xref ref-type="bibr" rid="ref6">6</xref>,<xref ref-type="bibr" rid="ref9">9</xref>,<xref ref-type="bibr" rid="ref17">17</xref>-<xref ref-type="bibr" rid="ref32">32</xref>]. Potential criteria considered for categorizing patients into high risk included patients with an abnormal or suspicious result on the previous screening test [<xref ref-type="bibr" rid="ref27">27</xref>], age group [<xref ref-type="bibr" rid="ref17">17</xref>,<xref ref-type="bibr" rid="ref26">26</xref>,<xref ref-type="bibr" rid="ref32">32</xref>], sex [<xref ref-type="bibr" rid="ref26">26</xref>], personal medical or family history [<xref ref-type="bibr" rid="ref18">18</xref>,<xref ref-type="bibr" rid="ref24">24</xref>,<xref ref-type="bibr" rid="ref26">26</xref>,<xref ref-type="bibr" rid="ref27">27</xref>], currently symptomatic or asymptomatic, predisposition to hereditary cancers, and inheritance of cancer-causing mutations [<xref ref-type="bibr" rid="ref18">18</xref>,<xref ref-type="bibr" rid="ref26">26</xref>].</p>
        <p>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 [<xref ref-type="bibr" rid="ref17">17</xref>,<xref ref-type="bibr" rid="ref20">20</xref>]; patients who do not have any cancer-related symptoms [<xref ref-type="bibr" rid="ref18">18</xref>,<xref ref-type="bibr" rid="ref22">22</xref>]; patients who have taken prophylactic measures such as the human papillomavirus (HPV) prophylactic vaccine [<xref ref-type="bibr" rid="ref17">17</xref>,<xref ref-type="bibr" rid="ref20">20</xref>,<xref ref-type="bibr" rid="ref24">24</xref>]; and patients who do not have medical, personal, or family-related indication for immediate screening [<xref ref-type="bibr" rid="ref18">18</xref>,<xref ref-type="bibr" rid="ref19">19</xref>,<xref ref-type="bibr" rid="ref23">23</xref>,<xref ref-type="bibr" rid="ref31">31</xref>].</p>
        <p>Other recommended strategies included identifying areas facing most disparities [<xref ref-type="bibr" rid="ref19">19</xref>,<xref ref-type="bibr" rid="ref34">34</xref>], creating algorithms [<xref ref-type="bibr" rid="ref24">24</xref>] and using artificial intelligence [<xref ref-type="bibr" rid="ref28">28</xref>] to create cancer risk scores, leveraging in-person visits to assess cancer risk [<xref ref-type="bibr" rid="ref6">6</xref>], and providing the option of open access screenings where patients can schedule screenings and can be assigned a priority category by health care staff [<xref ref-type="bibr" rid="ref26">26</xref>]. Some recommended screening high-risk patients through telemedicine prior to having them come into health care providers [<xref ref-type="bibr" rid="ref23">23</xref>,<xref ref-type="bibr" rid="ref29">29</xref>].</p>
        <p>In addition to risk stratification and triage, telemedicine was recommended to determine screening for patients with new complaints [<xref ref-type="bibr" rid="ref18">18</xref>,<xref ref-type="bibr" rid="ref19">19</xref>,<xref ref-type="bibr" rid="ref22">22</xref>]. Several articles noted the importance of implementing preventive measures such as COVID-19 screening prior to the procedures [<xref ref-type="bibr" rid="ref6">6</xref>,<xref ref-type="bibr" rid="ref9">9</xref>,<xref ref-type="bibr" rid="ref26">26</xref>], maintaining hygiene measures [<xref ref-type="bibr" rid="ref19">19</xref>,<xref ref-type="bibr" rid="ref32">32</xref>], and social distancing in waiting rooms [<xref ref-type="bibr" rid="ref32">32</xref>].</p>
      </sec>
      <sec>
        <title>Alternative Screening Methods</title>
        <p>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 (<xref ref-type="table" rid="table2">Table 2</xref>). Mailing of self-collection sampling kits was widely suggested as a screening strategy for cervical and colorectal cancers [<xref ref-type="bibr" rid="ref6">6</xref>,<xref ref-type="bibr" rid="ref17">17</xref>,<xref ref-type="bibr" rid="ref19">19</xref>-<xref ref-type="bibr" rid="ref21">21</xref>,<xref ref-type="bibr" rid="ref25">25</xref>-<xref ref-type="bibr" rid="ref28">28</xref>,<xref ref-type="bibr" rid="ref33">33</xref>-<xref ref-type="bibr" rid="ref36">36</xref>]. 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 [<xref ref-type="bibr" rid="ref17">17</xref>,<xref ref-type="bibr" rid="ref27">27</xref>,<xref ref-type="bibr" rid="ref34">34</xref>,<xref ref-type="bibr" rid="ref35">35</xref>]. Stool-based self-collection kits that are performed at home and mailed for screening were recommended for colorectal cancers [<xref ref-type="bibr" rid="ref6">6</xref>,<xref ref-type="bibr" rid="ref19">19</xref>,<xref ref-type="bibr" rid="ref20">20</xref>,<xref ref-type="bibr" rid="ref25">25</xref>,<xref ref-type="bibr" rid="ref26">26</xref>,<xref ref-type="bibr" rid="ref33">33</xref>-<xref ref-type="bibr" rid="ref36">36</xref>]. 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 [<xref ref-type="bibr" rid="ref28">28</xref>,<xref ref-type="bibr" rid="ref30">30</xref>].</p>
        <table-wrap position="float" id="table2">
          <label>Table 2</label>
          <caption>
            <p>Alternative approaches to increase cancer screenings.</p>
          </caption>
          <table width="1000" cellpadding="5" cellspacing="0" border="1" rules="groups" frame="hsides">
            <col width="250"/>
            <col width="350"/>
            <col width="400"/>
            <thead>
              <tr valign="top">
                <td>Cancer type/cancer risk factors</td>
                <td>Conventional recommendation/practices</td>
                <td>Variation in approaches</td>
              </tr>
            </thead>
            <tbody>
              <tr valign="top">
                <td>Breast cancer</td>
                <td>
                  <list list-type="bullet">
                    <list-item>
                      <p>Mammography</p>
                    </list-item>
                  </list>
                </td>
                <td>
                  <list list-type="bullet">
                    <list-item>
                      <p>Screening at mobile units or small satellite units</p>
                    </list-item>
                    <list-item>
                      <p>Follow-up on patients with abnormal results</p>
                    </list-item>
                  </list>
                </td>
              </tr>
              <tr valign="top">
                <td>Cervical cancer</td>
                <td>
                  <list list-type="bullet">
                    <list-item>
                      <p>Pap smear</p>
                    </list-item>
                    <list-item>
                      <p>Pap smear + HPV<sup>a</sup> co-testing</p>
                    </list-item>
                  </list>
                </td>
                <td>
                  <list list-type="bullet">
                    <list-item>
                      <p>Self-collection of vaginal or urine samples at home</p>
                    </list-item>
                    <list-item>
                      <p>Follow-up on patients with abnormal results</p>
                    </list-item>
                  </list>
                </td>
              </tr>
              <tr valign="top">
                <td>Colorectal cancer</td>
                <td>
                  <list list-type="bullet">
                    <list-item>
                      <p>Colonoscopy</p>
                    </list-item>
                    <list-item>
                      <p>Sigmoidoscopy</p>
                    </list-item>
                    <list-item>
                      <p>CT<sup>b</sup> colonography</p>
                    </list-item>
                    <list-item>
                      <p>Stool-based tests</p>
                    </list-item>
                  </list>
                </td>
                <td>
                  <list list-type="bullet">
                    <list-item>
                      <p>Self-collection of stool samples at home</p>
                    </list-item>
                    <list-item>
                      <p>Follow-up on patients with abnormal results</p>
                    </list-item>
                  </list>
                </td>
              </tr>
            </tbody>
          </table>
          <table-wrap-foot>
            <fn id="table2fn1">
              <p><sup>a</sup>HPV: human papillomavirus.</p>
            </fn>
            <fn id="table2fn2">
              <p><sup>b</sup>CT: computed tomography.</p>
            </fn>
          </table-wrap-foot>
        </table-wrap>
      </sec>
    </sec>
    <sec sec-type="discussion">
      <title>Discussion</title>
      <p>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 [<xref ref-type="bibr" rid="ref14">14</xref>]. 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.</p>
      <p>Risk stratification and triage approaches focused on prioritizing patients based on personal characteristics, medical history, cancer screening history, and communities facing highest cancer disparities [<xref ref-type="bibr" rid="ref6">6</xref>,<xref ref-type="bibr" rid="ref9">9</xref>,<xref ref-type="bibr" rid="ref17">17</xref>-<xref ref-type="bibr" rid="ref32">32</xref>]. The literature suggests that older patients at higher risk should be given priority since the risk of cancer increases with age [<xref ref-type="bibr" rid="ref17">17</xref>,<xref ref-type="bibr" rid="ref26">26</xref>].</p>
      <p>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 [<xref ref-type="bibr" rid="ref6">6</xref>,<xref ref-type="bibr" rid="ref9">9</xref>,<xref ref-type="bibr" rid="ref17">17</xref>-<xref ref-type="bibr" rid="ref32">32</xref>], 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 [<xref ref-type="bibr" rid="ref37">37</xref>-<xref ref-type="bibr" rid="ref40">40</xref>]. 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 [<xref ref-type="bibr" rid="ref24">24</xref>,<xref ref-type="bibr" rid="ref28">28</xref>].</p>
      <p>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 [<xref ref-type="bibr" rid="ref41">41</xref>-<xref ref-type="bibr" rid="ref43">43</xref>] and colorectal cancer [<xref ref-type="bibr" rid="ref26">26</xref>]. 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 [<xref ref-type="bibr" rid="ref42">42</xref>,<xref ref-type="bibr" rid="ref43">43</xref>]. Similar to cervical cancer, colorectal cancer screenings can be effectively conducted using noninvasive stool-based test kits at home [<xref ref-type="bibr" rid="ref44">44</xref>,<xref ref-type="bibr" rid="ref45">45</xref>]. Studies have shown that stool-based test kits can help reach underresourced communities and increase colorectal cancer screening uptake [<xref ref-type="bibr" rid="ref46">46</xref>]. Although the stool-based tests have a high false-positive rate [<xref ref-type="bibr" rid="ref47">47</xref>], patients testing negative can be assured that they do not have colorectal cancers [<xref ref-type="bibr" rid="ref26">26</xref>].</p>
      <p>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 [<xref ref-type="bibr" rid="ref28">28</xref>,<xref ref-type="bibr" rid="ref30">30</xref>] and reduce exposure risk.</p>
      <p>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.</p>
    </sec>
  </body>
  <back>
    <app-group>
      <supplementary-material id="app1">
        <label>Multimedia Appendix 1</label>
        <p>PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses) checklist.</p>
        <media xlink:href="cancer_v8i1e34392_app1.docx" xlink:title="DOCX File , 31 KB"/>
      </supplementary-material>
    </app-group>
    <glossary>
      <title>Abbreviations</title>
      <def-list>
        <def-item>
          <term id="abb1">HPV</term>
          <def>
            <p>human papillomavirus</p>
          </def>
        </def-item>
        <def-item>
          <term id="abb2">PRISMA</term>
          <def>
            <p>Preferred Reporting Items for Systematic Reviews and Meta-Analyses</p>
          </def>
        </def-item>
      </def-list>
    </glossary>
    <ack>
      <p>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.</p>
      <p>The authors would also like to thank Erin Gloster for her review and formatting assistance.</p>
    </ack>
    <fn-group>
      <fn fn-type="conflict">
        <p>None declared.</p>
      </fn>
    </fn-group>
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