The Feasibility and Accuracy of Sentinel Lymph Node Biopsy in Initially Clinically Node-Negative Breast Cancer after Neoadjuvant Chemotherapy: A Systematic Review and Meta-Analysis
Identifieur interne : 004406 ( Pmc/Corpus ); précédent : 004405; suivant : 004407The Feasibility and Accuracy of Sentinel Lymph Node Biopsy in Initially Clinically Node-Negative Breast Cancer after Neoadjuvant Chemotherapy: A Systematic Review and Meta-Analysis
Auteurs : Chong Geng ; Xiao Chen ; Xiaohua Pan ; Jiyu LiSource :
- PLoS ONE [ 1932-6203 ] ; 2016.
Abstract
With the increased use of neoadjuvant chemotherapy (NAC) in breast cancer, the timing of sentinel lymph node biopsy (SLNB) has become increasingly important. In this study, we aimed to evaluate the feasibility and accuracy of SLNB for initially clinically node-negative breast cancer after NAC by conducting a systematic review and meta-analysis.
We searched PubMed, Embase, and the Cochrane Library from January 1, 1993 to November 30, 2015 for studies on initially clinically node-negative breast cancer patients who underwent SLNB after NAC followed by axillary lymph node dissection (ALND).
A total of 1,456 patients from 16 studies were included in this review. The pooled identification rate (IR) for SLNB was 96% [95% confidence interval (CI): 95%-97%], and the false negative rate (FNR) was 6% (95% CI: 3%-8%). The pooled sensitivity, negative predictive value (NPV) and accuracy rate (AR) were 94% (95% CI: 92%-97%, I2 = 27.5%), 98% (95% CI: 98%-99%, I2 = 42.7%) and 99% (95% CI: 99%-100%, I2 = 32.6%), respectively. In the subgroup analysis, no significant differences were found in either the IR of an SLNB when different mapping methods were used (P = 0.180) or in the FNR between studies with and without immunohistochemistry (IHC) staining (P = 0.241).
Based on current evidence, SLNB is technically feasible and accurate enough for axillary staging in initially clinically node-negative breast cancer patients after NAC.
Url:
DOI: 10.1371/journal.pone.0162605
PubMed: 27606623
PubMed Central: 5015960
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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">The Feasibility and Accuracy of Sentinel Lymph Node Biopsy in Initially Clinically Node-Negative Breast Cancer after Neoadjuvant Chemotherapy: A Systematic Review and Meta-Analysis</title><author><name sortKey="Geng, Chong" sort="Geng, Chong" uniqKey="Geng C" first="Chong" last="Geng">Chong Geng</name><affiliation><nlm:aff id="aff001"></nlm:aff></affiliation></author><author><name sortKey="Chen, Xiao" sort="Chen, Xiao" uniqKey="Chen X" first="Xiao" last="Chen">Xiao Chen</name><affiliation><nlm:aff id="aff001"></nlm:aff></affiliation></author><author><name sortKey="Pan, Xiaohua" sort="Pan, Xiaohua" uniqKey="Pan X" first="Xiaohua" last="Pan">Xiaohua Pan</name><affiliation><nlm:aff id="aff001"></nlm:aff></affiliation></author><author><name sortKey="Li, Jiyu" sort="Li, Jiyu" uniqKey="Li J" first="Jiyu" last="Li">Jiyu Li</name><affiliation><nlm:aff id="aff001"></nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">27606623</idno><idno type="pmc">5015960</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5015960</idno><idno type="RBID">PMC:5015960</idno><idno type="doi">10.1371/journal.pone.0162605</idno><date when="2016">2016</date><idno type="wicri:Area/Pmc/Corpus">004406</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">004406</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">The Feasibility and Accuracy of Sentinel Lymph Node Biopsy in Initially Clinically Node-Negative Breast Cancer after Neoadjuvant Chemotherapy: A Systematic Review and Meta-Analysis</title><author><name sortKey="Geng, Chong" sort="Geng, Chong" uniqKey="Geng C" first="Chong" last="Geng">Chong Geng</name><affiliation><nlm:aff id="aff001"></nlm:aff></affiliation></author><author><name sortKey="Chen, Xiao" sort="Chen, Xiao" uniqKey="Chen X" first="Xiao" last="Chen">Xiao Chen</name><affiliation><nlm:aff id="aff001"></nlm:aff></affiliation></author><author><name sortKey="Pan, Xiaohua" sort="Pan, Xiaohua" uniqKey="Pan X" first="Xiaohua" last="Pan">Xiaohua Pan</name><affiliation><nlm:aff id="aff001"></nlm:aff></affiliation></author><author><name sortKey="Li, Jiyu" sort="Li, Jiyu" uniqKey="Li J" first="Jiyu" last="Li">Jiyu Li</name><affiliation><nlm:aff id="aff001"></nlm:aff></affiliation></author></analytic><series><title level="j">PLoS ONE</title><idno type="eISSN">1932-6203</idno><imprint><date when="2016">2016</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><sec id="sec001"><title>Background</title><p>With the increased use of neoadjuvant chemotherapy (NAC) in breast cancer, the timing of sentinel lymph node biopsy (SLNB) has become increasingly important. In this study, we aimed to evaluate the feasibility and accuracy of SLNB for initially clinically node-negative breast cancer after NAC by conducting a systematic review and meta-analysis.</p></sec><sec id="sec002"><title>Methods</title><p>We searched PubMed, Embase, and the Cochrane Library from January 1, 1993 to November 30, 2015 for studies on initially clinically node-negative breast cancer patients who underwent SLNB after NAC followed by axillary lymph node dissection (ALND).</p></sec><sec id="sec003"><title>Results</title><p>A total of 1,456 patients from 16 studies were included in this review. The pooled identification rate (IR) for SLNB was 96% [95% confidence interval (CI): 95%-97%], and the false negative rate (FNR) was 6% (95% CI: 3%-8%). The pooled sensitivity, negative predictive value (NPV) and accuracy rate (AR) were 94% (95% CI: 92%-97%, I<sup>2</sup> = 27.5%), 98% (95% CI: 98%-99%, I<sup>2</sup> = 42.7%) and 99% (95% CI: 99%-100%, I<sup>2</sup> = 32.6%), respectively. In the subgroup analysis, no significant differences were found in either the IR of an SLNB when different mapping methods were used (P = 0.180) or in the FNR between studies with and without immunohistochemistry (IHC) staining (P = 0.241).</p></sec><sec id="sec004"><title>Conclusion</title><p>Based on current evidence, SLNB is technically feasible and accurate enough for axillary staging in initially clinically node-negative breast cancer patients after NAC.</p></sec></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Samphao, S" uniqKey="Samphao S">S Samphao</name></author><author><name sortKey="Eremin, Jm" uniqKey="Eremin J">JM Eremin</name></author><author><name sortKey="El Sheemy, M" uniqKey="El Sheemy M">M El-Sheemy</name></author><author><name sortKey="Eremin, O" uniqKey="Eremin O">O Eremin</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Botteri, E" uniqKey="Botteri E">E 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<front><journal-meta><journal-id journal-id-type="nlm-ta">PLoS One</journal-id><journal-id journal-id-type="iso-abbrev">PLoS ONE</journal-id><journal-id journal-id-type="publisher-id">plos</journal-id><journal-id journal-id-type="pmc">plosone</journal-id><journal-title-group><journal-title>PLoS ONE</journal-title></journal-title-group><issn pub-type="epub">1932-6203</issn><publisher><publisher-name>Public Library of Science</publisher-name><publisher-loc>San Francisco, CA USA</publisher-loc></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">27606623</article-id><article-id pub-id-type="pmc">5015960</article-id><article-id pub-id-type="doi">10.1371/journal.pone.0162605</article-id><article-id pub-id-type="publisher-id">PONE-D-16-04285</article-id><article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Medicine and Health Sciences</subject><subj-group><subject>Oncology</subject><subj-group><subject>Cancers and Neoplasms</subject><subj-group><subject>Breast Tumors</subject><subj-group><subject>Breast Cancer</subject></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Research and Analysis Methods</subject><subj-group><subject>Mathematical and Statistical Techniques</subject><subj-group><subject>Statistical Methods</subject><subj-group><subject>Meta-Analysis</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Physical Sciences</subject><subj-group><subject>Mathematics</subject><subj-group><subject>Statistics (Mathematics)</subject><subj-group><subject>Statistical Methods</subject><subj-group><subject>Meta-Analysis</subject></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Anatomy</subject><subj-group><subject>Lymphatic System</subject><subj-group><subject>Lymph Nodes</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Medicine and Health Sciences</subject><subj-group><subject>Anatomy</subject><subj-group><subject>Lymphatic System</subject><subj-group><subject>Lymph Nodes</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Medicine and Health Sciences</subject><subj-group><subject>Diagnostic Medicine</subject><subj-group><subject>Cancer Detection and Diagnosis</subject><subj-group><subject>Lymphatic Mapping</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Medicine and Health Sciences</subject><subj-group><subject>Oncology</subject><subj-group><subject>Cancer Detection and Diagnosis</subject><subj-group><subject>Lymphatic Mapping</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Medicine and Health Sciences</subject><subj-group><subject>Oncology</subject><subj-group><subject>Cancer Treatment</subject><subj-group><subject>Chemotherapy</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Medicine and Health Sciences</subject><subj-group><subject>Clinical Medicine</subject><subj-group><subject>Clinical Oncology</subject><subj-group><subject>Chemotherapy</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Medicine and Health Sciences</subject><subj-group><subject>Oncology</subject><subj-group><subject>Clinical Oncology</subject><subj-group><subject>Chemotherapy</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Medicine and Health Sciences</subject><subj-group><subject>Pharmaceutics</subject><subj-group><subject>Drug Therapy</subject><subj-group><subject>Chemotherapy</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Anatomy</subject><subj-group><subject>Histology</subject></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Medicine and Health Sciences</subject><subj-group><subject>Anatomy</subject><subj-group><subject>Histology</subject></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Research and Analysis Methods</subject><subj-group><subject>Specimen Preparation and Treatment</subject><subj-group><subject>Staining</subject><subj-group><subject>Negative Staining</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Research and Analysis Methods</subject><subj-group><subject>Research Assessment</subject><subj-group><subject>Systematic Reviews</subject></subj-group></subj-group></subj-group></article-categories><title-group><article-title>The Feasibility and Accuracy of Sentinel Lymph Node Biopsy in Initially Clinically Node-Negative Breast Cancer after Neoadjuvant Chemotherapy: A Systematic Review and Meta-Analysis</article-title><alt-title alt-title-type="running-head">Sentinel Lymph Node Biopsy after Neoadjuvant Chemotherapy</alt-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Geng</surname><given-names>Chong</given-names></name><xref ref-type="aff" rid="aff001"></xref></contrib><contrib contrib-type="author"><name><surname>Chen</surname><given-names>Xiao</given-names></name><xref ref-type="aff" rid="aff001"></xref></contrib><contrib contrib-type="author"><name><surname>Pan</surname><given-names>Xiaohua</given-names></name><xref ref-type="aff" rid="aff001"></xref></contrib><contrib contrib-type="author"><name><surname>Li</surname><given-names>Jiyu</given-names></name><xref ref-type="corresp" rid="cor001">*</xref><xref ref-type="aff" rid="aff001"></xref></contrib></contrib-group><aff id="aff001"><addr-line>Department of Breast and Thyroid Surgery, Shandong Provincial Hospital Affiliated to Shandong University, Jinan, Shandong Province, China</addr-line></aff><contrib-group><contrib contrib-type="editor"><name><surname>Dolcetti</surname><given-names>Riccardo</given-names></name><role>Editor</role><xref ref-type="aff" rid="edit1"></xref></contrib></contrib-group><aff id="edit1"><addr-line>Fondazione IRCCS Istituto Nazionale dei Tumori, ITALY</addr-line></aff><author-notes><fn fn-type="COI-statement" id="coi001"><p><bold>Competing Interests: </bold>The authors have declared that no competing interests exist.</p></fn><fn fn-type="con"><p><list list-type="simple"><list-item><p><bold>Conceived and designed the experiments:</bold> JL XP.</p></list-item><list-item><p><bold>Performed the experiments:</bold> CG XC JL.</p></list-item><list-item><p><bold>Analyzed the data:</bold> CG XC XP JL.</p></list-item><list-item><p><bold>Contributed reagents/materials/analysis tools:</bold> CG XC.</p></list-item><list-item><p><bold>Wrote the paper:</bold> CG JL.</p></list-item></list></p></fn><corresp id="cor001">* E-mail: <email>bigli2004@163.com</email></corresp></author-notes><pub-date pub-type="epub"><day>8</day><month>9</month><year>2016</year></pub-date><pub-date pub-type="collection"><year>2016</year></pub-date><volume>11</volume><issue>9</issue><elocation-id>e0162605</elocation-id><history><date date-type="received"><day>3</day><month>2</month><year>2016</year></date><date date-type="accepted"><day>25</day><month>8</month><year>2016</year></date></history><permissions><copyright-statement>© 2016 Geng et al</copyright-statement><copyright-year>2016</copyright-year><copyright-holder>Geng et al</copyright-holder><license xlink:href="http://creativecommons.org/licenses/by/4.0/"><license-p>This is an open access article distributed under the terms of the <ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">Creative Commons Attribution License</ext-link>, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.</license-p></license></permissions><self-uri content-type="pdf" xlink:href="pone.0162605.pdf"></self-uri><abstract><sec id="sec001"><title>Background</title><p>With the increased use of neoadjuvant chemotherapy (NAC) in breast cancer, the timing of sentinel lymph node biopsy (SLNB) has become increasingly important. In this study, we aimed to evaluate the feasibility and accuracy of SLNB for initially clinically node-negative breast cancer after NAC by conducting a systematic review and meta-analysis.</p></sec><sec id="sec002"><title>Methods</title><p>We searched PubMed, Embase, and the Cochrane Library from January 1, 1993 to November 30, 2015 for studies on initially clinically node-negative breast cancer patients who underwent SLNB after NAC followed by axillary lymph node dissection (ALND).</p></sec><sec id="sec003"><title>Results</title><p>A total of 1,456 patients from 16 studies were included in this review. The pooled identification rate (IR) for SLNB was 96% [95% confidence interval (CI): 95%-97%], and the false negative rate (FNR) was 6% (95% CI: 3%-8%). The pooled sensitivity, negative predictive value (NPV) and accuracy rate (AR) were 94% (95% CI: 92%-97%, I<sup>2</sup> = 27.5%), 98% (95% CI: 98%-99%, I<sup>2</sup> = 42.7%) and 99% (95% CI: 99%-100%, I<sup>2</sup> = 32.6%), respectively. In the subgroup analysis, no significant differences were found in either the IR of an SLNB when different mapping methods were used (P = 0.180) or in the FNR between studies with and without immunohistochemistry (IHC) staining (P = 0.241).</p></sec><sec id="sec004"><title>Conclusion</title><p>Based on current evidence, SLNB is technically feasible and accurate enough for axillary staging in initially clinically node-negative breast cancer patients after NAC.</p></sec></abstract><funding-group><award-group id="award001"><funding-source><institution>Key Research and Development Program of Shandong Province</institution></funding-source><award-id>2015GSF118023</award-id><principal-award-recipient><name><surname>Li</surname><given-names>Jiyu</given-names></name></principal-award-recipient></award-group><award-group id="award002"><funding-source><institution>Projects of Medical and Health Technology Development Program in Shandong Province</institution></funding-source><award-id>2014WS0349</award-id><principal-award-recipient><name><surname>Li</surname><given-names>Jiyu</given-names></name></principal-award-recipient></award-group><funding-statement>This work was supported by the Key Research and Development Program of Shandong Province (no. 2015GSF118023, recipient: JL) and the Projects of Medical and Health Technology Development Program in Shandong Province (no. 2014WS0349, recipient: JL). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.</funding-statement></funding-group><counts><fig-count count="5"></fig-count><table-count count="6"></table-count><page-count count="16"></page-count></counts><custom-meta-group><custom-meta id="data-availability"><meta-name>Data Availability</meta-name><meta-value>All relevant data are within the paper and its Supporting Information files.</meta-value></custom-meta></custom-meta-group></article-meta><notes><title>Data Availability</title><p>All relevant data are within the paper and its Supporting Information files.</p></notes></front><body><sec sec-type="intro" id="sec005"><title>Introduction</title><p>Although molecular mechanisms increasingly contribute to our understanding of breast cancer, the status of the axilla remains the most important prognostic factor for breast cancer patients [<xref rid="pone.0162605.ref001" ref-type="bibr">1</xref>–<xref rid="pone.0162605.ref003" ref-type="bibr">3</xref>]. Evaluating the status of the axilla in invasive breast cancer is important for both the prognosis and adjuvant treatment recommendations. Axillary lymph node dissection (ALND) has been a standard technique for axillary staging of breast cancer for over 100 years; however, the complications of ALND, which include lymphedema, axillary web syndrome, numbness, pain, and restriction of shoulder range of motion, decrease patients' quality of life greatly [<xref rid="pone.0162605.ref004" ref-type="bibr">4</xref>–<xref rid="pone.0162605.ref006" ref-type="bibr">6</xref>]. Sentinel lymph node biopsy (SLNB), a minimally invasive procedure, was introduced in the early 1990s [<xref rid="pone.0162605.ref007" ref-type="bibr">7</xref>]. SLNB showed high accuracy in determining the status of the axilla and led to less morbidity compared with ALND [<xref rid="pone.0162605.ref008" ref-type="bibr">8</xref>, <xref rid="pone.0162605.ref009" ref-type="bibr">9</xref>]. SLNB has been studied extensively and recommended as an alternative to traditional ALND for axillary status staging in patients with early breast cancer [<xref rid="pone.0162605.ref009" ref-type="bibr">9</xref>–<xref rid="pone.0162605.ref011" ref-type="bibr">11</xref>].</p><p>Neoadjuvant chemotherapy (NAC) was initially introduced in the 1970s for the treatment of patients with locally advanced breast cancer [<xref rid="pone.0162605.ref012" ref-type="bibr">12</xref>]. Although compared with adjuvant chemotherapy, NAC cannot improve patients’ disease-free and overall survival [<xref rid="pone.0162605.ref013" ref-type="bibr">13</xref>, <xref rid="pone.0162605.ref014" ref-type="bibr">14</xref>], it offers some potential advantages: It provides an additional opportunity for breast-conserving therapy [<xref rid="pone.0162605.ref015" ref-type="bibr">15</xref>, <xref rid="pone.0162605.ref016" ref-type="bibr">16</xref>]; it enables the <italic>in vivo</italic> assessment of sensitivity to chemotherapy [<xref rid="pone.0162605.ref017" ref-type="bibr">17</xref>]; and it presents an opportunity to evaluate the effects of newly developed agents [<xref rid="pone.0162605.ref018" ref-type="bibr">18</xref>]. The role of NAC has changed considerably in recent decades. As a result, the indications for NAC have been extended to select patients with early breast cancer [<xref rid="pone.0162605.ref015" ref-type="bibr">15</xref>, <xref rid="pone.0162605.ref016" ref-type="bibr">16</xref>, <xref rid="pone.0162605.ref019" ref-type="bibr">19</xref>].</p><p>Despite the increasing use of both NAC and SLNB, the feasibility of SLNB after NAC remains controversial. It is possible that tumor eradication after NAC could alter lymphatic drainage via the fibrosis of lymphatic channels and lead to a decreased identification rate and an increased false negative rate in SLNB [<xref rid="pone.0162605.ref020" ref-type="bibr">20</xref>, <xref rid="pone.0162605.ref021" ref-type="bibr">21</xref>]. At present, ALND is the standard treatment for the axilla following NAC.</p><p>For patients with clinically node-negative breast cancer before NAC, the timing of SLNB is controversial. According to guidelines of the American Society of Clinical Oncology (ASCO), breast cancer patients with clinically negative axillary nodes are candidates for SLNB for axillary staging [<xref rid="pone.0162605.ref022" ref-type="bibr">22</xref>]. To avoid the potential influence of NAC, SLNB is usually performed before NAC in this population of patients; however, there are also obvious advantages to implementing SLNB after NAC. If SLNB after NAC in initially clinically node-negative patients can achieve outcomes comparable to those of patients who did not undergo NAC, patients may only need a single surgery for both the breast and axilla instead of two separate operative procedures.</p><p>Several studies have assessed the feasibility and accuracy of SLNB in initially clinically node-negative breast cancer patients after NAC. The patient selection criteria, mapping methods and histological examinations vary across individual studies. Hence, we performed the present meta-analysis to collect data for evaluation purposes. To the best of our knowledge, this is the first meta-analysis to address the clinical question mentioned above.</p></sec><sec sec-type="materials|methods" id="sec006"><title>Methods</title><sec id="sec007"><title>Literature search strategy</title><p>We searched PubMed, Embase, and the Cochrane Library database from January 1, 1993, to November 30, 2015, using both Medical Subject Heading (Mesh) terms and free text terms: ("breast cancer" OR "breast neoplasm") AND ("SLNB" OR "sentinel lymph node biopsy" OR "sentinel lymph node dissection") AND ("preoperative therapy" OR "preoperative chemotherapy" OR "neoadjuvant chemotherapy" OR "NAC"). Only articles published in English were selected. The search strategy is presented in <xref ref-type="fig" rid="pone.0162605.g001">Fig 1</xref>.</p><fig id="pone.0162605.g001" orientation="portrait" position="float"><object-id pub-id-type="doi">10.1371/journal.pone.0162605.g001</object-id><label>Fig 1</label><caption><title>Flow diagram of literature search and individual studies identified for this systematic review and meta-analysis.</title></caption><graphic xlink:href="pone.0162605.g001"></graphic></fig></sec><sec id="sec008"><title>Study inclusion criteria</title><p>Studies included in this review had to meet the following criteria: First, the patients had received NAC for invasive breast cancer. Second, the patients were clinically node-negative at the time of diagnosis. Clinically node-negative was defined as the absence of suspicious or abnormal-appearing lymph nodes on physical examination or ultrasound imaging. Third, the patients had undergone an SLNB after NAC, followed by an ALND. Patients receiving neoadjuvant endocrine therapy or preoperative radiotherapy were excluded from this meta-analysis.</p></sec><sec id="sec009"><title>Study quality assessment</title><p>Two reviewers independently evaluated the study quality using QUADAS 2 [<xref rid="pone.0162605.ref023" ref-type="bibr">23</xref>], a standardized tool for the quality assessment of diagnostic accuracy studies. QUADAS 2 comprises four domains: patient selection, index testing, a reference standard, and flow and timing. The risk of bias is deemed "low," "high," or "unclear." If the answers to all signaling questions for a domain are "yes," then the risk of bias can be judged as low. If any question is answered "no," the risk of bias should be considered high. Applicability concerns were judged using similar criteria. The questions adopted in our review are listed in <xref ref-type="supplementary-material" rid="pone.0162605.s001">S1 File</xref>.</p></sec><sec id="sec010"><title>Data extraction and definitions</title><p>The data were independently extracted by 2 reviewers and checked by other reviewers for accuracy. Discrepancies were resolved by consensus after discussion. The identification rate (IR) was defined as the number of women with successfully identified sentinel lymph nodes (SNs) divided by the total number of women for whom SLNB was attempted, using the histological analysis of the axillary lymph node collected with ALND as the "gold standard". The results of each successfully identified SN were further categorized as true positive (TP), true negative (TN), or false negative (FN). Four test performance parameters were evaluated: sensitivity [TP/(TN+FN)], false negative rate (FNR) [FN/ (FN+TP)], negative predictive value (NPV) [TN/ (TN+FN)] and accuracy rate (AR) [(TP+TN)/total number of successful SLNB].</p></sec><sec id="sec011"><title>Statistical analysis</title><p>The meta-analysis in this study was conducted using R, version 3.2.2 for windows (R: A language and environment for statistical computing; R Foundation for Statistical Computing, Vienna, Austria, <ext-link ext-link-type="uri" xlink:href="http://www.R-project.org/">http://www.R-project.org/</ext-link>).</p><p>The meta-analyses of the IR, AR, FNR, NPV and sensitivity of SLNB were conducted using the <italic>metaprop</italic> function in the R-<italic>meta</italic> package. The individual studies were weighted by study size and by the inverse of the variance of the individual point estimates. The heterogeneity of the studies was evaluated using the inconsistency statistic (I<sup>2</sup>) [<xref rid="pone.0162605.ref024" ref-type="bibr">24</xref>]. Publication bias was displayed graphically using forest plots. The effect of lymph node mapping techniques on the IR and the use of immunohistochemistry (IHC) staining on FNR was determined using the chi-squared test. Two sided p-values<0.05 were considered significant.</p></sec></sec><sec sec-type="results" id="sec012"><title>Results</title><sec id="sec013"><title>Description of included studies</title><p>Based on the search strategy, a total of 1,456 patients in 16 studies who met the inclusion criteria were analyzed [<xref rid="pone.0162605.ref025" ref-type="bibr">25</xref>–<xref rid="pone.0162605.ref040" ref-type="bibr">40</xref>]. QUADAS 2 was used to assess the quality of the studies included in our review. The results of the quality assessment are listed in <xref ref-type="table" rid="pone.0162605.t001">Table 1</xref>. In the included studies, only the risk of bias in patient selection was considered high risk; the other aspects were low risk.</p><table-wrap id="pone.0162605.t001" orientation="portrait" position="float"><object-id pub-id-type="doi">10.1371/journal.pone.0162605.t001</object-id><label>Table 1</label><caption><title>Results of quality assessment according to QUADAS 2 for the included studies.</title></caption><alternatives><graphic id="pone.0162605.t001g" xlink:href="pone.0162605.t001"></graphic><table frame="hsides" rules="groups"><colgroup span="1"><col align="left" valign="middle" span="1"></col><col align="left" valign="middle" span="1"></col><col align="left" valign="middle" span="1"></col><col align="left" valign="middle" span="1"></col><col align="left" valign="middle" span="1"></col><col align="left" valign="middle" span="1"></col><col align="left" valign="middle" span="1"></col><col align="left" valign="middle" span="1"></col></colgroup><thead><tr><th align="left" rowspan="1" colspan="1">Study</th><th align="left" colspan="4" rowspan="1">Risk of bias</th><th align="left" colspan="3" rowspan="1">Applicability concerns</th></tr><tr><th align="left" style="background-color:#cdcdcd" rowspan="1" colspan="1"></th><th align="left" style="background-color:#cdcdcd" rowspan="1" colspan="1">Patient selection</th><th align="left" style="background-color:#cdcdcd" rowspan="1" colspan="1">Index test</th><th align="left" style="background-color:#cdcdcd" rowspan="1" colspan="1">Reference standard</th><th align="left" style="background-color:#cdcdcd" rowspan="1" colspan="1">Flow and timing</th><th align="left" style="background-color:#cdcdcd" rowspan="1" colspan="1">Patient selection</th><th align="left" style="background-color:#cdcdcd" rowspan="1" colspan="1">Index test</th><th align="left" style="background-color:#cdcdcd" rowspan="1" colspan="1">Reference Standard</th></tr></thead><tbody><tr><td align="left" rowspan="1" colspan="1">Nason et al.</td><td align="left" rowspan="1" colspan="1">2</td><td align="left" rowspan="1" colspan="1">1</td><td align="left" rowspan="1" colspan="1">1</td><td align="left" rowspan="1" colspan="1">1</td><td align="left" rowspan="1" colspan="1">1</td><td align="left" rowspan="1" colspan="1">1</td><td align="left" rowspan="1" colspan="1">1</td></tr><tr><td align="left" style="background-color:#cdcdcd" rowspan="1" colspan="1">Tafra et al.</td><td align="left" style="background-color:#cdcdcd" rowspan="1" colspan="1">2</td><td align="left" style="background-color:#cdcdcd" rowspan="1" colspan="1">1</td><td align="left" style="background-color:#cdcdcd" rowspan="1" colspan="1">1</td><td align="left" style="background-color:#cdcdcd" rowspan="1" colspan="1">1</td><td align="left" style="background-color:#cdcdcd" rowspan="1" colspan="1">1</td><td align="left" style="background-color:#cdcdcd" rowspan="1" colspan="1">1</td><td align="left" style="background-color:#cdcdcd" rowspan="1" colspan="1">1</td></tr><tr><td align="left" rowspan="1" colspan="1">Piato et al.</td><td align="left" rowspan="1" colspan="1">2</td><td align="left" rowspan="1" colspan="1">1</td><td align="left" rowspan="1" colspan="1">1</td><td align="left" rowspan="1" colspan="1">1</td><td align="left" rowspan="1" colspan="1">1</td><td align="left" rowspan="1" colspan="1">2</td><td align="left" rowspan="1" colspan="1">1</td></tr><tr><td align="left" style="background-color:#cdcdcd" rowspan="1" colspan="1">Tanaka et al.</td><td align="left" style="background-color:#cdcdcd" rowspan="1" colspan="1">2</td><td align="left" style="background-color:#cdcdcd" rowspan="1" colspan="1">1</td><td align="left" style="background-color:#cdcdcd" rowspan="1" colspan="1">1</td><td align="left" style="background-color:#cdcdcd" rowspan="1" colspan="1">1</td><td align="left" style="background-color:#cdcdcd" rowspan="1" colspan="1">1</td><td align="left" style="background-color:#cdcdcd" rowspan="1" colspan="1">2</td><td align="left" style="background-color:#cdcdcd" rowspan="1" colspan="1">1</td></tr><tr><td align="left" rowspan="1" colspan="1">Yu et al.</td><td align="left" rowspan="1" colspan="1">2</td><td align="left" rowspan="1" colspan="1">1</td><td align="left" rowspan="1" colspan="1">1</td><td align="left" rowspan="1" colspan="1">1</td><td align="left" rowspan="1" colspan="1">2</td><td align="left" rowspan="1" colspan="1">1</td><td align="left" rowspan="1" colspan="1">1</td></tr><tr><td align="left" style="background-color:#cdcdcd" rowspan="1" colspan="1">Kinoshita et al.</td><td align="left" style="background-color:#cdcdcd" rowspan="1" colspan="1">2</td><td align="left" style="background-color:#cdcdcd" rowspan="1" colspan="1">1</td><td align="left" style="background-color:#cdcdcd" rowspan="1" colspan="1">1</td><td align="left" style="background-color:#cdcdcd" rowspan="1" colspan="1">1</td><td align="left" style="background-color:#cdcdcd" rowspan="1" colspan="1">1</td><td align="left" style="background-color:#cdcdcd" rowspan="1" colspan="1">2</td><td align="left" style="background-color:#cdcdcd" rowspan="1" colspan="1">1</td></tr><tr><td align="left" rowspan="1" colspan="1">Gimbergues et al.</td><td align="left" rowspan="1" colspan="1">2</td><td align="left" rowspan="1" colspan="1">1</td><td align="left" rowspan="1" colspan="1">1</td><td align="left" rowspan="1" colspan="1">1</td><td align="left" rowspan="1" colspan="1">1</td><td align="left" rowspan="1" colspan="1">2</td><td align="left" rowspan="1" colspan="1">1</td></tr><tr><td align="left" style="background-color:#cdcdcd" rowspan="1" colspan="1">Papa et al.</td><td align="left" style="background-color:#cdcdcd" rowspan="1" colspan="1">2</td><td align="left" style="background-color:#cdcdcd" rowspan="1" colspan="1">1</td><td align="left" style="background-color:#cdcdcd" rowspan="1" colspan="1">1</td><td align="left" style="background-color:#cdcdcd" rowspan="1" colspan="1">1</td><td align="left" style="background-color:#cdcdcd" rowspan="1" colspan="1">1</td><td align="left" style="background-color:#cdcdcd" rowspan="1" colspan="1">2</td><td align="left" style="background-color:#cdcdcd" rowspan="1" colspan="1">1</td></tr><tr><td align="left" rowspan="1" colspan="1">Classe et al.</td><td align="left" rowspan="1" colspan="1">2</td><td align="left" rowspan="1" colspan="1">1</td><td align="left" rowspan="1" colspan="1">1</td><td align="left" rowspan="1" colspan="1">1</td><td align="left" rowspan="1" colspan="1">1</td><td align="left" rowspan="1" colspan="1">1</td><td align="left" rowspan="1" colspan="1">1</td></tr><tr><td align="left" style="background-color:#cdcdcd" rowspan="1" colspan="1">Hunt et al.</td><td align="left" style="background-color:#cdcdcd" rowspan="1" colspan="1">2</td><td align="left" style="background-color:#cdcdcd" rowspan="1" colspan="1">1</td><td align="left" style="background-color:#cdcdcd" rowspan="1" colspan="1">1</td><td align="left" style="background-color:#cdcdcd" rowspan="1" colspan="1">1</td><td align="left" style="background-color:#cdcdcd" rowspan="1" colspan="1">1</td><td align="left" style="background-color:#cdcdcd" rowspan="1" colspan="1">2</td><td align="left" style="background-color:#cdcdcd" rowspan="1" colspan="1">1</td></tr><tr><td align="left" rowspan="1" colspan="1">Dalus et al.</td><td align="left" rowspan="1" colspan="1">2</td><td align="left" rowspan="1" colspan="1">1</td><td align="left" rowspan="1" colspan="1">1</td><td align="left" rowspan="1" colspan="1">1</td><td align="left" rowspan="1" colspan="1">1</td><td align="left" rowspan="1" colspan="1">1</td><td align="left" rowspan="1" colspan="1">1</td></tr><tr><td align="left" style="background-color:#cdcdcd" rowspan="1" colspan="1">Pecha et al.</td><td align="left" style="background-color:#cdcdcd" rowspan="1" colspan="1">2</td><td align="left" style="background-color:#cdcdcd" rowspan="1" colspan="1">1</td><td align="left" style="background-color:#cdcdcd" rowspan="1" colspan="1">1</td><td align="left" style="background-color:#cdcdcd" rowspan="1" colspan="1">1</td><td align="left" style="background-color:#cdcdcd" rowspan="1" colspan="1">1</td><td align="left" style="background-color:#cdcdcd" rowspan="1" colspan="1">2</td><td align="left" style="background-color:#cdcdcd" rowspan="1" colspan="1">1</td></tr><tr><td align="left" rowspan="1" colspan="1">Aguirre et al.</td><td align="left" rowspan="1" colspan="1">2</td><td align="left" rowspan="1" colspan="1">1</td><td align="left" rowspan="1" colspan="1">1</td><td align="left" rowspan="1" colspan="1">1</td><td align="left" rowspan="1" colspan="1">1</td><td align="left" rowspan="1" colspan="1">2</td><td align="left" rowspan="1" colspan="1">1</td></tr><tr><td align="left" style="background-color:#cdcdcd" rowspan="1" colspan="1">Takahashi et al.</td><td align="left" style="background-color:#cdcdcd" rowspan="1" colspan="1">2</td><td align="left" style="background-color:#cdcdcd" rowspan="1" colspan="1">1</td><td align="left" style="background-color:#cdcdcd" rowspan="1" colspan="1">1</td><td align="left" style="background-color:#cdcdcd" rowspan="1" colspan="1">1</td><td align="left" style="background-color:#cdcdcd" rowspan="1" colspan="1">1</td><td align="left" style="background-color:#cdcdcd" rowspan="1" colspan="1">1</td><td align="left" style="background-color:#cdcdcd" rowspan="1" colspan="1">1</td></tr><tr><td align="left" rowspan="1" colspan="1">Madrona et al.</td><td align="left" rowspan="1" colspan="1">2</td><td align="left" rowspan="1" colspan="1">1</td><td align="left" rowspan="1" colspan="1">1</td><td align="left" rowspan="1" colspan="1">1</td><td align="left" rowspan="1" colspan="1">1</td><td align="left" rowspan="1" colspan="1">2</td><td align="left" rowspan="1" colspan="1">1</td></tr><tr><td align="left" style="background-color:#cdcdcd" rowspan="1" colspan="1">Kika et al.</td><td align="left" style="background-color:#cdcdcd" rowspan="1" colspan="1">2</td><td align="left" style="background-color:#cdcdcd" rowspan="1" colspan="1">1</td><td align="left" style="background-color:#cdcdcd" rowspan="1" colspan="1">1</td><td align="left" style="background-color:#cdcdcd" rowspan="1" colspan="1">1</td><td align="left" style="background-color:#cdcdcd" rowspan="1" colspan="1">1</td><td align="left" style="background-color:#cdcdcd" rowspan="1" colspan="1">2</td><td align="left" style="background-color:#cdcdcd" rowspan="1" colspan="1">1</td></tr></tbody></table></alternatives><table-wrap-foot><fn id="t001fn001"><p>1: low risk. 2: high risk.?: unclear risk</p></fn></table-wrap-foot></table-wrap><p>The 16 studies were published between 2000 and 2015. Fourteen studies were single-center studies [<xref rid="pone.0162605.ref025" ref-type="bibr">25</xref>, <xref rid="pone.0162605.ref027" ref-type="bibr">27</xref>–<xref rid="pone.0162605.ref032" ref-type="bibr">32</xref>, <xref rid="pone.0162605.ref034" ref-type="bibr">34</xref>–<xref rid="pone.0162605.ref040" ref-type="bibr">40</xref>], and the other two were multi-center studies [<xref rid="pone.0162605.ref026" ref-type="bibr">26</xref>, <xref rid="pone.0162605.ref033" ref-type="bibr">33</xref>]. Four studies were from Japan [<xref rid="pone.0162605.ref028" ref-type="bibr">28</xref>, <xref rid="pone.0162605.ref030" ref-type="bibr">30</xref>, <xref rid="pone.0162605.ref038" ref-type="bibr">38</xref>, <xref rid="pone.0162605.ref040" ref-type="bibr">40</xref>], 3 from the United States [<xref rid="pone.0162605.ref025" ref-type="bibr">25</xref>, <xref rid="pone.0162605.ref026" ref-type="bibr">26</xref>, <xref rid="pone.0162605.ref034" ref-type="bibr">34</xref>], 2 from France [<xref rid="pone.0162605.ref031" ref-type="bibr">31</xref>, <xref rid="pone.0162605.ref033" ref-type="bibr">33</xref>], 2 from Spain [<xref rid="pone.0162605.ref037" ref-type="bibr">37</xref>, <xref rid="pone.0162605.ref039" ref-type="bibr">39</xref>], and 1 each from Austria [<xref rid="pone.0162605.ref035" ref-type="bibr">35</xref>], Brazil [<xref rid="pone.0162605.ref027" ref-type="bibr">27</xref>], the Czech Republic [<xref rid="pone.0162605.ref036" ref-type="bibr">36</xref>], Israel [<xref rid="pone.0162605.ref032" ref-type="bibr">32</xref>], and Chinese Taipei [<xref rid="pone.0162605.ref029" ref-type="bibr">29</xref>]. All of the studies included a group of patients who were clinically node-negative at the time of diagnosis. All of these patients underwent SLNB and followed by ALND. Four studies performed SN mapping using radiocolloid alone [<xref rid="pone.0162605.ref027" ref-type="bibr">27</xref>, <xref rid="pone.0162605.ref031" ref-type="bibr">31</xref>, <xref rid="pone.0162605.ref032" ref-type="bibr">32</xref>, <xref rid="pone.0162605.ref037" ref-type="bibr">37</xref>], three studies used blue dye alone [<xref rid="pone.0162605.ref028" ref-type="bibr">28</xref>, <xref rid="pone.0162605.ref029" ref-type="bibr">29</xref>, <xref rid="pone.0162605.ref040" ref-type="bibr">40</xref>], and 6 studies used both radiocolloid and blue dye [<xref rid="pone.0162605.ref025" ref-type="bibr">25</xref>, <xref rid="pone.0162605.ref026" ref-type="bibr">26</xref>, <xref rid="pone.0162605.ref033" ref-type="bibr">33</xref>–<xref rid="pone.0162605.ref035" ref-type="bibr">35</xref>, <xref rid="pone.0162605.ref038" ref-type="bibr">38</xref>]. Regarding histological technique, 6 studies used hematoxylin and eosin (H&E) staining alone [<xref rid="pone.0162605.ref027" ref-type="bibr">27</xref>, <xref rid="pone.0162605.ref028" ref-type="bibr">28</xref>, <xref rid="pone.0162605.ref030" ref-type="bibr">30</xref>, <xref rid="pone.0162605.ref032" ref-type="bibr">32</xref>, <xref rid="pone.0162605.ref037" ref-type="bibr">37</xref>, <xref rid="pone.0162605.ref040" ref-type="bibr">40</xref>], 3 studies performed additional IHC staining for negative nodes based on H&E staining results [<xref rid="pone.0162605.ref025" ref-type="bibr">25</xref>, <xref rid="pone.0162605.ref031" ref-type="bibr">31</xref>, <xref rid="pone.0162605.ref033" ref-type="bibr">33</xref>], and 3 studies used IHC staining in all cases [<xref rid="pone.0162605.ref029" ref-type="bibr">29</xref>, <xref rid="pone.0162605.ref034" ref-type="bibr">34</xref>, <xref rid="pone.0162605.ref038" ref-type="bibr">38</xref>]. Detailed descriptions of the included studies are summarized in <xref ref-type="table" rid="pone.0162605.t002">Table 2</xref>.</p><table-wrap id="pone.0162605.t002" orientation="portrait" position="float"><object-id pub-id-type="doi">10.1371/journal.pone.0162605.t002</object-id><label>Table 2</label><caption><title>Detailed descriptions of included studies.</title></caption><alternatives><graphic id="pone.0162605.t002g" xlink:href="pone.0162605.t002"></graphic><table frame="hsides" rules="groups"><colgroup span="1"><col align="left" valign="middle" span="1"></col><col align="left" valign="middle" span="1"></col><col align="left" valign="middle" span="1"></col><col align="left" valign="middle" span="1"></col><col align="left" valign="middle" span="1"></col><col align="left" valign="middle" span="1"></col><col align="left" valign="middle" span="1"></col><col align="left" valign="middle" span="1"></col></colgroup><thead><tr><th align="left" rowspan="1" colspan="1">Study</th><th align="left" rowspan="1" colspan="1">Publication year</th><th align="left" rowspan="1" colspan="1">Origin</th><th align="left" rowspan="1" colspan="1">No. of patients SLNB attempts</th><th align="left" rowspan="1" colspan="1">Initial tumor size</th><th align="left" rowspan="1" colspan="1">Chemotherapy</th><th align="left" rowspan="1" colspan="1">SLNB mapping</th><th align="left" rowspan="1" colspan="1">IHC</th></tr></thead><tbody><tr><td align="left" style="background-color:#d7d7d7" rowspan="1" colspan="1">Nason et al.</td><td align="left" style="background-color:#d7d7d7" rowspan="1" colspan="1">2000</td><td align="left" style="background-color:#d7d7d7" rowspan="1" colspan="1">USA</td><td align="left" style="background-color:#d7d7d7" rowspan="1" colspan="1">9</td><td align="left" style="background-color:#d7d7d7" rowspan="1" colspan="1">T1-4</td><td align="left" style="background-color:#d7d7d7" rowspan="1" colspan="1">AC</td><td align="left" style="background-color:#d7d7d7" rowspan="1" colspan="1">BD+RC</td><td align="left" style="background-color:#d7d7d7" rowspan="1" colspan="1">Yes</td></tr><tr><td align="left" rowspan="1" colspan="1">Tafra et al.</td><td align="left" rowspan="1" colspan="1">2001</td><td align="left" rowspan="1" colspan="1">USA</td><td align="left" rowspan="1" colspan="1">29</td><td align="left" rowspan="1" colspan="1">T1-2</td><td align="left" rowspan="1" colspan="1">m</td><td align="left" rowspan="1" colspan="1">BD+RC</td><td align="left" rowspan="1" colspan="1">Yes<xref ref-type="table-fn" rid="t002fn002"><sup>a</sup></xref></td></tr><tr><td align="left" style="background-color:#d7d7d7" rowspan="1" colspan="1">Piato et al.</td><td align="left" style="background-color:#d7d7d7" rowspan="1" colspan="1">2003</td><td align="left" style="background-color:#d7d7d7" rowspan="1" colspan="1">Brazil</td><td align="left" style="background-color:#d7d7d7" rowspan="1" colspan="1">42</td><td align="left" style="background-color:#d7d7d7" rowspan="1" colspan="1">T1-2</td><td align="left" style="background-color:#d7d7d7" rowspan="1" colspan="1">AC</td><td align="left" style="background-color:#d7d7d7" rowspan="1" colspan="1">RC only</td><td align="left" style="background-color:#d7d7d7" rowspan="1" colspan="1">No</td></tr><tr><td align="left" rowspan="1" colspan="1">Tanaka et al.</td><td align="left" rowspan="1" colspan="1">2005</td><td align="left" rowspan="1" colspan="1">Japan</td><td align="left" rowspan="1" colspan="1">17</td><td align="left" rowspan="1" colspan="1">T1-4</td><td align="left" rowspan="1" colspan="1">CPF</td><td align="left" rowspan="1" colspan="1">BD only</td><td align="left" rowspan="1" colspan="1">No</td></tr><tr><td align="left" style="background-color:#d7d7d7" rowspan="1" colspan="1">Yu et al.</td><td align="left" style="background-color:#d7d7d7" rowspan="1" colspan="1">2006</td><td align="left" style="background-color:#d7d7d7" rowspan="1" colspan="1">Chinese Taipei</td><td align="left" style="background-color:#d7d7d7" rowspan="1" colspan="1">127</td><td align="left" style="background-color:#d7d7d7" rowspan="1" colspan="1">T3</td><td align="left" style="background-color:#d7d7d7" rowspan="1" colspan="1">Doxorubicin based</td><td align="left" style="background-color:#d7d7d7" rowspan="1" colspan="1">BD only</td><td align="left" style="background-color:#d7d7d7" rowspan="1" colspan="1">Yes</td></tr><tr><td align="left" rowspan="1" colspan="1">Kinoshita et al.</td><td align="left" rowspan="1" colspan="1">2007</td><td align="left" rowspan="1" colspan="1">Japan</td><td align="left" rowspan="1" colspan="1">54</td><td align="left" rowspan="1" colspan="1">T2-4</td><td align="left" rowspan="1" colspan="1">FEC→T or T</td><td align="left" rowspan="1" colspan="1">BD/RC/Both</td><td align="left" rowspan="1" colspan="1">No</td></tr><tr><td align="left" style="background-color:#d7d7d7" rowspan="1" colspan="1">Gimbergues et al.</td><td align="left" style="background-color:#d7d7d7" rowspan="1" colspan="1">2008</td><td align="left" style="background-color:#d7d7d7" rowspan="1" colspan="1">France</td><td align="left" style="background-color:#d7d7d7" rowspan="1" colspan="1">82</td><td align="left" style="background-color:#d7d7d7" rowspan="1" colspan="1">T1-3</td><td align="left" style="background-color:#d7d7d7" rowspan="1" colspan="1">CAF or E→T or T</td><td align="left" style="background-color:#d7d7d7" rowspan="1" colspan="1">RC only</td><td align="left" style="background-color:#d7d7d7" rowspan="1" colspan="1">Yes</td></tr><tr><td align="left" rowspan="1" colspan="1">Papa et al.</td><td align="left" rowspan="1" colspan="1">2008</td><td align="left" rowspan="1" colspan="1">Israel</td><td align="left" rowspan="1" colspan="1">31</td><td align="left" rowspan="1" colspan="1">T2-3</td><td align="left" rowspan="1" colspan="1">AC</td><td align="left" rowspan="1" colspan="1">RC only</td><td align="left" rowspan="1" colspan="1">No</td></tr><tr><td align="left" style="background-color:#d7d7d7" rowspan="1" colspan="1">Classe et al.</td><td align="left" style="background-color:#d7d7d7" rowspan="1" colspan="1">2009</td><td align="left" style="background-color:#d7d7d7" rowspan="1" colspan="1">France</td><td align="left" style="background-color:#d7d7d7" rowspan="1" colspan="1">130</td><td align="left" style="background-color:#d7d7d7" rowspan="1" colspan="1">T0-3</td><td align="left" style="background-color:#d7d7d7" rowspan="1" colspan="1">m</td><td align="left" style="background-color:#d7d7d7" rowspan="1" colspan="1">BD+RC</td><td align="left" style="background-color:#d7d7d7" rowspan="1" colspan="1">Yes</td></tr><tr><td align="left" rowspan="1" colspan="1">Hunt et al.</td><td align="left" rowspan="1" colspan="1">2009</td><td align="left" rowspan="1" colspan="1">USA</td><td align="left" rowspan="1" colspan="1">575</td><td align="left" rowspan="1" colspan="1">T1-3</td><td align="left" rowspan="1" colspan="1">m</td><td align="left" rowspan="1" colspan="1">BD+RC</td><td align="left" rowspan="1" colspan="1">Yes<xref ref-type="table-fn" rid="t002fn003"><sup>b</sup></xref></td></tr><tr><td align="left" style="background-color:#d7d7d7" rowspan="1" colspan="1">Dalus et al.</td><td align="left" style="background-color:#d7d7d7" rowspan="1" colspan="1">2011</td><td align="left" style="background-color:#d7d7d7" rowspan="1" colspan="1">Austria</td><td align="left" style="background-color:#d7d7d7" rowspan="1" colspan="1">13</td><td align="left" style="background-color:#d7d7d7" rowspan="1" colspan="1">T1-4</td><td align="left" style="background-color:#d7d7d7" rowspan="1" colspan="1">Mainly epirubicin based</td><td align="left" style="background-color:#d7d7d7" rowspan="1" colspan="1">BD+RC</td><td align="left" style="background-color:#d7d7d7" rowspan="1" colspan="1">Yes</td></tr><tr><td align="left" rowspan="1" colspan="1">Pecha et al.</td><td align="left" rowspan="1" colspan="1">2011</td><td align="left" rowspan="1" colspan="1">Cezch</td><td align="left" rowspan="1" colspan="1">172</td><td align="left" rowspan="1" colspan="1">T1-4</td><td align="left" rowspan="1" colspan="1">Anthracycline based</td><td align="left" rowspan="1" colspan="1">RC only/BD only</td><td align="left" rowspan="1" colspan="1">Yes<xref ref-type="table-fn" rid="t002fn004"><sup>c</sup></xref></td></tr><tr><td align="left" style="background-color:#d7d7d7" rowspan="1" colspan="1">Aguirre et al.</td><td align="left" style="background-color:#d7d7d7" rowspan="1" colspan="1">2012</td><td align="left" style="background-color:#d7d7d7" rowspan="1" colspan="1">Spain</td><td align="left" style="background-color:#d7d7d7" rowspan="1" colspan="1">51</td><td align="left" style="background-color:#d7d7d7" rowspan="1" colspan="1">T1-3</td><td align="left" style="background-color:#d7d7d7" rowspan="1" colspan="1">AC→T</td><td align="left" style="background-color:#d7d7d7" rowspan="1" colspan="1">RC only</td><td align="left" style="background-color:#d7d7d7" rowspan="1" colspan="1">No</td></tr><tr><td align="left" rowspan="1" colspan="1">Takahashi et al.</td><td align="left" rowspan="1" colspan="1">2012</td><td align="left" rowspan="1" colspan="1">Japan</td><td align="left" rowspan="1" colspan="1">41</td><td align="left" rowspan="1" colspan="1">T1-4</td><td align="left" rowspan="1" colspan="1">Capecitabine +T→FEC/FEC→T/T</td><td align="left" rowspan="1" colspan="1">BD+RC</td><td align="left" rowspan="1" colspan="1">Yes</td></tr><tr><td align="left" style="background-color:#d7d7d7" rowspan="1" colspan="1">Madrona et al.</td><td align="left" style="background-color:#d7d7d7" rowspan="1" colspan="1">2015</td><td align="left" style="background-color:#d7d7d7" rowspan="1" colspan="1">Spain</td><td align="left" style="background-color:#d7d7d7" rowspan="1" colspan="1">49</td><td align="left" style="background-color:#d7d7d7" rowspan="1" colspan="1">T1-4</td><td align="left" style="background-color:#d7d7d7" rowspan="1" colspan="1">Mainly anthracycline and taxane contained</td><td align="left" style="background-color:#d7d7d7" rowspan="1" colspan="1">RC only/Both</td><td align="left" style="background-color:#d7d7d7" rowspan="1" colspan="1">m</td></tr><tr><td align="left" rowspan="1" colspan="1">Kika et al.</td><td align="left" rowspan="1" colspan="1">2015</td><td align="left" rowspan="1" colspan="1">Japan</td><td align="left" rowspan="1" colspan="1">34</td><td align="left" rowspan="1" colspan="1">T1-4</td><td align="left" rowspan="1" colspan="1">Mainly anthracycline and taxane contained</td><td align="left" rowspan="1" colspan="1">BD only</td><td align="left" rowspan="1" colspan="1">No</td></tr></tbody></table></alternatives><table-wrap-foot><fn id="t002fn001"><p>m, missing value; A, adriamycin(doxorubicin); C, cycolophosphamide; P, pirarubicin; F, 5 fluorouracil; E, epirubicin; T, taxol; BD, blue dye; RC, radiocolloid.</p></fn><fn id="t002fn002"><p><sup>a</sup> performed on majority of SN-negative patients for metastasis on H&E staining.</p></fn><fn id="t002fn003"><p><sup>b</sup> only performed on patients enrolled after 2000.</p></fn><fn id="t002fn004"><p><sup>c</sup> only performed on SN patients with suspicious malignant cells.</p></fn></table-wrap-foot></table-wrap></sec><sec id="sec014"><title>Identification rate of SLNB</title><p>In the 16 studies, the IRs of SLNB ranged from 87% to 100%. Moderate between-study heterogeneity (I<sup>2</sup> = 45.6%, P = 0.0245) in the IR was found. Therefore, a fixed-effects model was used to estimate the combined IR with a result of 96% [95% confidence interval (CI): 95%-97%] (<xref ref-type="fig" rid="pone.0162605.g002">Fig 2</xref>). Funnel plots were used to assess the publication bias of all but one of the studies. The studies showed good symmetry and suggested minimal publication bias (<xref ref-type="fig" rid="pone.0162605.g003">Fig 3</xref>). Begg’s test confirmed the above conclusion, with P = 0.3219.</p><fig id="pone.0162605.g002" orientation="portrait" position="float"><object-id pub-id-type="doi">10.1371/journal.pone.0162605.g002</object-id><label>Fig 2</label><caption><title>Forest plot of the IR.</title><p>A fixed-effects model was used to estimate the combined IR, with a result of 96% (95% CI: 95%-97%); I<sup>2</sup> = 45.6%.</p></caption><graphic xlink:href="pone.0162605.g002"></graphic></fig><fig id="pone.0162605.g003" orientation="portrait" position="float"><object-id pub-id-type="doi">10.1371/journal.pone.0162605.g003</object-id><label>Fig 3</label><caption><title>Funnel plot to assess the publication bias effect on the IR.</title><p>Each dot represents a separate study. The funnel plot revealed no apparent evidence of publication bias.</p></caption><graphic xlink:href="pone.0162605.g003"></graphic></fig><p>The mapping method was assumed to be associated with the IR of SLNB; therefore, we compared the IR rate according to the mapping method used. Three studies were excluded from this analysis because different mapping methods were used within a single study [<xref rid="pone.0162605.ref030" ref-type="bibr">30</xref>, <xref rid="pone.0162605.ref036" ref-type="bibr">36</xref>, <xref rid="pone.0162605.ref039" ref-type="bibr">39</xref>]. The summarized IR of the 3 studies that used only blue dye mapping was 96% (95% CI: 91%-100%). The pooled IR from the 4 studies that used only radiocolloid was 96% (95% CI: 94%-99%). The pooled IR from the 6 studies that used both blue dye and radiocolloid was 97% (95% CI: 96%-98%). There were no significant differences in the IR of SLNB among the different mapping methods (P = 0.180; <xref ref-type="table" rid="pone.0162605.t003">Table 3</xref>).</p><table-wrap id="pone.0162605.t003" orientation="portrait" position="float"><object-id pub-id-type="doi">10.1371/journal.pone.0162605.t003</object-id><label>Table 3</label><caption><title>Identification rate of SLNB according to mapping method.</title></caption><alternatives><graphic id="pone.0162605.t003g" xlink:href="pone.0162605.t003"></graphic><table frame="hsides" rules="groups"><colgroup span="1"><col align="left" valign="middle" span="1"></col><col align="left" valign="middle" span="1"></col><col align="left" valign="middle" span="1"></col><col align="left" valign="middle" span="1"></col><col align="left" valign="middle" span="1"></col></colgroup><thead><tr><th align="center" rowspan="1" colspan="1">Mapping method</th><th align="center" rowspan="1" colspan="1">No. of studies</th><th align="center" rowspan="1" colspan="1">No. of patients SLNB attempts</th><th align="center" rowspan="1" colspan="1">No. of patients SN successfully identified</th><th align="center" rowspan="1" colspan="1">Identification rate (95% CI)</th></tr></thead><tbody><tr><td align="center" style="background-color:#d7d7d7" rowspan="1" colspan="1">Blue dye alone</td><td align="center" style="background-color:#d7d7d7" rowspan="1" colspan="1">3</td><td align="center" style="background-color:#d7d7d7" rowspan="1" colspan="1">178</td><td align="center" style="background-color:#d7d7d7" rowspan="1" colspan="1">166</td><td align="center" style="background-color:#d7d7d7" rowspan="1" colspan="1">96% (91%-100%)</td></tr><tr><td align="center" rowspan="1" colspan="1">Radiocolloid alone</td><td align="center" rowspan="1" colspan="1">4</td><td align="center" rowspan="1" colspan="1">206</td><td align="center" rowspan="1" colspan="1">195</td><td align="center" rowspan="1" colspan="1">96% (94%-99%)</td></tr><tr><td align="center" style="background-color:#d7d7d7" rowspan="1" colspan="1">Blue dye + radiocolloid</td><td align="center" style="background-color:#d7d7d7" rowspan="1" colspan="1">6</td><td align="center" style="background-color:#d7d7d7" rowspan="1" colspan="1">797</td><td align="center" style="background-color:#d7d7d7" rowspan="1" colspan="1">767</td><td align="center" style="background-color:#d7d7d7" rowspan="1" colspan="1">97% (96%-98%)</td></tr></tbody></table></alternatives><table-wrap-foot><fn id="t003fn001"><p>Three studies were excluded from this analysis due to different mapping methods within a single study.</p></fn></table-wrap-foot></table-wrap></sec><sec id="sec015"><title>False negative rate of SLNB</title><p>The individual FNRs of SLNB ranged from 0% to 33% in the 16 studies. Moderate FNR heterogeneity was found among the studies (I<sup>2</sup> = 27.5%, P = 0.1469; <xref ref-type="fig" rid="pone.0162605.g004">Fig 4</xref>). The summarized estimated FNR for the 16 studies was 6% (95% CI: 3%-8%) based on the fixed-effects model. The funnel plot showed minimal publication bias (<xref ref-type="fig" rid="pone.0162605.g005">Fig 5</xref>), and all studies used the funnel plot. This result was confirmed using Begg’s test, with P = 0.08711.</p><fig id="pone.0162605.g004" orientation="portrait" position="float"><object-id pub-id-type="doi">10.1371/journal.pone.0162605.g004</object-id><label>Fig 4</label><caption><title>Forest plot of the FNR.</title><p>A fixed-effects model was used to estimate the combined FNR with a result of 6% (95% CI: 3%-8%) I<sup>2</sup> = 27.5%.</p></caption><graphic xlink:href="pone.0162605.g004"></graphic></fig><fig id="pone.0162605.g005" orientation="portrait" position="float"><object-id pub-id-type="doi">10.1371/journal.pone.0162605.g005</object-id><label>Fig 5</label><caption><title>Funnel plot to assess publication bias effect on the FNR.</title><p>Each dot represents a separate study. The funnel plot revealed no apparent evidence of publication bias.</p></caption><graphic xlink:href="pone.0162605.g005"></graphic></fig><p>It is generally accepted that IHC staining with anti-cytokeratin antibodies is much more sensitive than conventional H&E staining for detecting the micrometastasis of lymph nodes [<xref rid="pone.0162605.ref041" ref-type="bibr">41</xref>, <xref rid="pone.0162605.ref042" ref-type="bibr">42</xref>]. We compared the FNR rates of the different histological techniques that were used. Four studies were omitted because of incomplete information regarding the histological method [<xref rid="pone.0162605.ref026" ref-type="bibr">26</xref>, <xref rid="pone.0162605.ref034" ref-type="bibr">34</xref>, <xref rid="pone.0162605.ref036" ref-type="bibr">36</xref>, <xref rid="pone.0162605.ref039" ref-type="bibr">39</xref>]. The pooled FNR from the 6 studies that only used H&E staining was 11% (95% CI: 4%-18%). The pooled FNR from the 6 studies that used H&E combined with IHC staining was 4% (95% CI: 1%-7%). No significant difference in the FNR of SLNB was detected between the studies that used IHC staining and those that did not (P = 0.241; <xref ref-type="table" rid="pone.0162605.t004">Table 4</xref>).</p><table-wrap id="pone.0162605.t004" orientation="portrait" position="float"><object-id pub-id-type="doi">10.1371/journal.pone.0162605.t004</object-id><label>Table 4</label><caption><title>False negative rate of SLNB according to histological technique.</title></caption><alternatives><graphic id="pone.0162605.t004g" xlink:href="pone.0162605.t004"></graphic><table frame="hsides" rules="groups"><colgroup span="1"><col align="left" valign="middle" span="1"></col><col align="left" valign="middle" span="1"></col><col align="left" valign="middle" span="1"></col><col align="left" valign="middle" span="1"></col><col align="left" valign="middle" span="1"></col></colgroup><thead><tr><th align="center" rowspan="1" colspan="1">Histological technique</th><th align="center" rowspan="1" colspan="1">No. of studies</th><th align="left" rowspan="1" colspan="1">No. of patients with positive axillary lymph nodes</th><th align="center" rowspan="1" colspan="1">No. of patients with false negative SNs</th><th align="center" rowspan="1" colspan="1">False negative rate (95% CI)</th></tr></thead><tbody><tr><td align="center" style="background-color:#d7d7d7" rowspan="1" colspan="1">IHC staining only</td><td align="center" style="background-color:#d7d7d7" rowspan="1" colspan="1">6</td><td align="center" style="background-color:#d7d7d7" rowspan="1" colspan="1">82</td><td align="center" style="background-color:#d7d7d7" rowspan="1" colspan="1">10</td><td align="center" style="background-color:#d7d7d7" rowspan="1" colspan="1">11% (4%-18%)</td></tr><tr><td align="center" rowspan="1" colspan="1">IHC staining combined with H&E staining</td><td align="center" rowspan="1" colspan="1">6</td><td align="center" rowspan="1" colspan="1">158</td><td align="center" rowspan="1" colspan="1">12</td><td align="center" rowspan="1" colspan="1">4% (1%-7%)</td></tr></tbody></table></alternatives><table-wrap-foot><fn id="t004fn001"><p>Four studies were omitted due to incomplete data regarding the histological method.</p></fn></table-wrap-foot></table-wrap></sec><sec id="sec016"><title>Sensitivity, NPV and AR of SLNB</title><p>Three test performance parameters of SLNB were analyzed: sensitivity, NPV, and AR (<xref ref-type="table" rid="pone.0162605.t005">Table 5</xref>). In the 16 studies, the sensitivity, NPV and AR ranged from 67%-100%, 50–100% and 75%-100%, respectively. The pooled sensitivity, NPV and AR were 94% (95% CI: 92%-97%, I<sup>2</sup> = 27.5%), 98% (95% CI: 98%-99%, I<sup>2</sup> = 42.7%) and 99% (95% CI: 99%-100%, I<sup>2</sup> = 32.6%), respectively. The forest plots displayed minimal variation, and a fixed-effects model was used for the analysis.</p><table-wrap id="pone.0162605.t005" orientation="portrait" position="float"><object-id pub-id-type="doi">10.1371/journal.pone.0162605.t005</object-id><label>Table 5</label><caption><title>Sensitivity, NPV and AR in individual studies.</title></caption><alternatives><graphic id="pone.0162605.t005g" xlink:href="pone.0162605.t005"></graphic><table frame="hsides" rules="groups"><colgroup span="1"><col align="left" valign="middle" span="1"></col><col align="left" valign="middle" span="1"></col><col align="left" valign="middle" span="1"></col><col align="left" valign="middle" span="1"></col></colgroup><thead><tr><th align="center" rowspan="1" colspan="1">Study</th><th align="left" rowspan="1" colspan="1">Sensitivity (95% CI)</th><th align="left" rowspan="1" colspan="1">NPV (95% CI)</th><th align="center" rowspan="1" colspan="1">AR (95%)</th></tr></thead><tbody><tr><td align="center" style="background-color:#d7d7d7" rowspan="1" colspan="1">Nason et al.</td><td align="center" style="background-color:#d7d7d7" rowspan="1" colspan="1">67% (22%-96%)</td><td align="center" style="background-color:#d7d7d7" rowspan="1" colspan="1">50% (7%-93%)</td><td align="center" style="background-color:#d7d7d7" rowspan="1" colspan="1">75% (35%-97%)</td></tr><tr><td align="center" rowspan="1" colspan="1">Tafra et al.</td><td align="center" rowspan="1" colspan="1">100% (78%-100%)</td><td align="center" rowspan="1" colspan="1">100% (74%-100%)</td><td align="center" rowspan="1" colspan="1">100% (87%-100%)</td></tr><tr><td align="center" style="background-color:#d7d7d7" rowspan="1" colspan="1">Piato et al.</td><td align="center" style="background-color:#d7d7d7" rowspan="1" colspan="1">83% (59%-96%)</td><td align="center" style="background-color:#d7d7d7" rowspan="1" colspan="1">88% (70%-98%)</td><td align="center" style="background-color:#d7d7d7" rowspan="1" colspan="1">93% (80%-98%)</td></tr><tr><td align="center" rowspan="1" colspan="1">Tanaka et al.</td><td align="center" rowspan="1" colspan="1">100% (40%-100%)</td><td align="center" rowspan="1" colspan="1">100% (75%-100%)</td><td align="center" rowspan="1" colspan="1">100% (80%-100%)</td></tr><tr><td align="center" style="background-color:#d7d7d7" rowspan="1" colspan="1">Yu et al.</td><td align="center" style="background-color:#d7d7d7" rowspan="1" colspan="1">93% (84%-98%)</td><td align="center" style="background-color:#d7d7d7" rowspan="1" colspan="1">91% (81%-97%)</td><td align="center" style="background-color:#d7d7d7" rowspan="1" colspan="1">100% (97%-100%)</td></tr><tr><td align="center" rowspan="1" colspan="1">Kinoshita et al.</td><td align="center" rowspan="1" colspan="1">86% (57%-98%)</td><td align="center" rowspan="1" colspan="1">95% (83%-99%)</td><td align="center" rowspan="1" colspan="1">96% (87%-100%)</td></tr><tr><td align="center" style="background-color:#d7d7d7" rowspan="1" colspan="1">Gimbergues et al.</td><td align="center" style="background-color:#d7d7d7" rowspan="1" colspan="1">100% (88%-100%)</td><td align="center" style="background-color:#d7d7d7" rowspan="1" colspan="1">100% (93%-100%)</td><td align="center" style="background-color:#d7d7d7" rowspan="1" colspan="1">100% (95%-100%)</td></tr><tr><td align="center" rowspan="1" colspan="1">Papa et al.</td><td align="center" rowspan="1" colspan="1">84% (60%-97%)</td><td align="center" rowspan="1" colspan="1">73% (39%-94%)</td><td align="center" rowspan="1" colspan="1">89% (71%-98%)</td></tr><tr><td align="center" style="background-color:#d7d7d7" rowspan="1" colspan="1">Classe et al.</td><td align="center" style="background-color:#d7d7d7" rowspan="1" colspan="1">91% (75%-99%)</td><td align="center" style="background-color:#d7d7d7" rowspan="1" colspan="1">97% (91%-99%)</td><td align="center" style="background-color:#d7d7d7" rowspan="1" colspan="1">98% (93%-99%)</td></tr><tr><td align="center" rowspan="1" colspan="1">Hunt et al.</td><td align="center" rowspan="1" colspan="1">94% (87%-98%)</td><td align="center" rowspan="1" colspan="1">99% (98%-100%)</td><td align="center" rowspan="1" colspan="1">99% (98%-100%)</td></tr><tr><td align="center" style="background-color:#d7d7d7" rowspan="1" colspan="1">Dalus et al.</td><td align="center" style="background-color:#d7d7d7" rowspan="1" colspan="1">75% (19%-99%)</td><td align="center" style="background-color:#d7d7d7" rowspan="1" colspan="1">90% (55%-100%)</td><td align="center" style="background-color:#d7d7d7" rowspan="1" colspan="1">92% (64%-100%)</td></tr><tr><td align="center" rowspan="1" colspan="1">Pecha et al.</td><td align="center" rowspan="1" colspan="1">84% (69%-93%)</td><td align="center" rowspan="1" colspan="1">94% (88%-98%)</td><td align="center" rowspan="1" colspan="1">95% (91%-98%)</td></tr><tr><td align="center" style="background-color:#d7d7d7" rowspan="1" colspan="1">Aguirre et al.</td><td align="center" style="background-color:#d7d7d7" rowspan="1" colspan="1">90% (70%-99%)</td><td align="center" style="background-color:#d7d7d7" rowspan="1" colspan="1">94% (79%-99%)</td><td align="center" style="background-color:#d7d7d7" rowspan="1" colspan="1">96% (86%-100%)</td></tr><tr><td align="center" rowspan="1" colspan="1">Takahashi et al.</td><td align="center" rowspan="1" colspan="1">94% (73%-100%)</td><td align="center" rowspan="1" colspan="1">95% (75%-100%)</td><td align="center" rowspan="1" colspan="1">100% (90%-100%)</td></tr><tr><td align="center" style="background-color:#d7d7d7" rowspan="1" colspan="1">Madrona et al.</td><td align="center" style="background-color:#d7d7d7" rowspan="1" colspan="1">82% (48%-98%)</td><td align="center" style="background-color:#d7d7d7" rowspan="1" colspan="1">94% (81%-99%)</td><td align="center" style="background-color:#d7d7d7" rowspan="1" colspan="1">95% (85%-99%)</td></tr><tr><td align="center" rowspan="1" colspan="1">Kika et al.</td><td align="center" rowspan="1" colspan="1">100% (54%-100%)</td><td align="center" rowspan="1" colspan="1">100% (87%-100%)</td><td align="center" rowspan="1" colspan="1">100% (89%-100%)</td></tr><tr><td align="center" style="background-color:#d7d7d7" rowspan="1" colspan="1">Pooled estimate</td><td align="center" style="background-color:#d7d7d7" rowspan="1" colspan="1">94% (92%-97%)</td><td align="center" style="background-color:#d7d7d7" rowspan="1" colspan="1">98% (98%-99%)</td><td align="center" style="background-color:#d7d7d7" rowspan="1" colspan="1">99% (99%-100%)</td></tr></tbody></table></alternatives></table-wrap></sec></sec><sec sec-type="conclusions" id="sec017"><title>Discussion</title><p>This present systematic review was conducted to provide an overview of the published literature regarding the feasibility and accuracy of SLNB in initially clinically node-negative breast cancer after NAC. We specifically evaluated the IRs and FNRs, which are the most important test performance parameters in SLNB. The pooled IR was 96%, with a 95% credible interval of 95 to 97%. The pooled FNR was 6%, with a 95% credible interval of 3 to 8%. These rates do not differ substantially from those reported in prior studies that accepted the use of SLNB in early breast cancer without NAC [<xref rid="pone.0162605.ref043" ref-type="bibr">43</xref>–<xref rid="pone.0162605.ref045" ref-type="bibr">45</xref>]. SLNB appears to be a reliable technique for staging initially clinically node-negative breast cancer after NAC.</p><p>Seven meta-analyses concerning SLNB after NAC have been performed. Three of them included both clinically node-positive and node-negative patients prior to NAC [<xref rid="pone.0162605.ref046" ref-type="bibr">46</xref>–<xref rid="pone.0162605.ref048" ref-type="bibr">48</xref>]. Although these 3 meta-analyses reviewed studies from different timespans, similar results were obtained, indicating that SLNB is a potentially reliable staging technique for breast cancer after NAC. Tan and his colleagues investigated the feasibility of SLNB in patients who were clinically node-negative after NAC [<xref rid="pone.0162605.ref049" ref-type="bibr">49</xref>]. The pooled IR and pooled FNR were 94% and 7%, respectively, and were comparable to the rates for SLNB without NAC. Two meta-analyses focused on SLNB in initially clinically node-positive patients after NAC [<xref rid="pone.0162605.ref050" ref-type="bibr">50</xref>, <xref rid="pone.0162605.ref051" ref-type="bibr">51</xref>]. Both studies had acceptable IRs; however, the FNRs were poor (14% and 15.1%, respectively). Mocellin and his colleagues reviewed studies about SLNB after NAC in locally advanced breast cancer [<xref rid="pone.0162605.ref052" ref-type="bibr">52</xref>]. Their review included 72 studies and 7,451 patients. The IR was 89.6%, and the FNR was 14.2%. The performance of SLNB was not as good as that observed in early breast cancer. The current study is the first meta-analysis to investigate the feasibility and accuracy of SLNB in patients with clinically node-negative breast cancer after NAC. The IR found in this study was higher than that of previous meta-analyses, and the FNR was lower.</p><p>Currently, the standard treatment of the axilla after NAC is ALND. The reliability of SLNB in patients undergoing NAC remains controversial [<xref rid="pone.0162605.ref018" ref-type="bibr">18</xref>, <xref rid="pone.0162605.ref053" ref-type="bibr">53</xref>]. Theoretically, chemotherapy could induce lymphovascular shrinkage and fibrosis, which may affect lymphatic mapping and lead to a lower IR. In addition, uneven sterilization of the lymph node tumor in NAC could lead to a higher FNR. These factors could explain why the IR and FNR of SLNB are not very good in patients after NAC. However, these possibilities have not yet been confirmed [<xref rid="pone.0162605.ref031" ref-type="bibr">31</xref>]. The situation seems quite different in early breast cancer. In Hunt’s study, which included 575 initially clinically node-negative patients with breast cancer who underwent SLNB after NAC, the IR was 97.4%, and the FNR was 5.9% [<xref rid="pone.0162605.ref034" ref-type="bibr">34</xref>]. Van der Heiden-van der Loo and his colleagues’ retrospective study showed similar IRs for SLNB in initially clinically node-negative patients before and after NAC (98% vs 95%) [<xref rid="pone.0162605.ref054" ref-type="bibr">54</xref>]. Santa-Maria et al. reported that there were no compelling data to support routine SLNB before NAC and recommended performing SLNB after NAC in patients with clinically node-negative axilla at presentation [<xref rid="pone.0162605.ref053" ref-type="bibr">53</xref>]. The latest ASCO guideline states that SLNB may be performed before or after NAC, but there is no convincing evidence supporting SLNB after NAC in patients with breast cancer [<xref rid="pone.0162605.ref008" ref-type="bibr">8</xref>]. In the present meta-analysis, we obtained a high IR, sensitivity, AR, and NPV and a low FNR for SLNB after NAC in initially clinically node-negative patients. These results directly support Santa-Maria’s opinion.</p><p>In initially clinically node-negative patients, avoiding additional surgical procedure before NAC could be the most important advantage of performing SLNB after NAC. To gain this advantage, two conditions are required: one is that SLNB could stage the axilla accurately after NAC, and the other is that SLNB could provide a safe alternative to ALND in SN-negative down-staged axilla. By pooling the results from these 16 studies, we demonstrate that SLNB is an accurate technique for axillary staging in this population. The first condition mentioned above was met. Kim et al.’s study performed SLNB after NAC in patients who had cytology-proven node-positive disease before NAC [<xref rid="pone.0162605.ref055" ref-type="bibr">55</xref>]. They found that in SN-negative patients, there was no significant difference in axillary recurrence between the SLNB-only and ALND groups. This result indicated that even when SLNB was performed after NAC, ALND was not necessary for SN-negative patients. The second condition was also met. Taken together, these findings indicate that performing SLNB and breast surgery in a single procedure after NAC is reasonable.</p><p>Initially clinically node-negative breast cancer patients have a relatively small tumor burden in the lymph nodes. NAC kills tumor cells in the lymph nodes, which can result in the downstaging of macrometastasis in SNs to micrometastasis. In this specific population of patients, macrometastases in SNs have a relatively high likelihood of shrinking to micrometastasis after NAC. Several studies have recommend to omitting an ALND in patients with micrometastasis and isolated tumor cells in SNs [<xref rid="pone.0162605.ref056" ref-type="bibr">56</xref>, <xref rid="pone.0162605.ref057" ref-type="bibr">57</xref>]. If we regard SNs with micrometastasis after NAC as negative node, these patients could avoid an ALND. This could be another advantage of performing SLNB after NAC in initially clinically node-negative breast cancer patients. The SN FNAC study recommends that tumor of any size be considered positive in SLNB after NAC in biopsy-proven node-positive breast cancer [<xref rid="pone.0162605.ref058" ref-type="bibr">58</xref>]. In their study, if an SN with isolated tumor cells after NAC had been considered negative, the FNR would have increased to 13.3%. Whether ALND could be omitted in initially clinically node-negative patients with micrometastasis in SNs after NAC is unclear. More studies are needed to evaluate the clinical significant of micrometastasis in SNs after NAC in this specific patient population.</p><p>In our meta-analysis, the summarized IRs of the blue dye-alone group, the radiocolloid-alone group and the combined group were 96%, 96% and 97%, respectively. No significant difference was detected with the chi-square test. The different mapping methods did not influence the IRs. Boughey and his colleagues evaluated the factors affecting SN identification after NAC [<xref rid="pone.0162605.ref059" ref-type="bibr">59</xref>]. The IRs of SLNB were 78.6% with blue dye alone, 91.4% with radiocolloid and 93.8% with dual mapping agents. The researchers concluded that the IR of SLNB after NAC was higher when mapping was performed using radiocolloid either alone or combined with blue dye than with blue dye alone. The different results that we obtained may be related to the fact that the initial axillary status varied among the patients included in our systematic review.</p><p>Opinions differ on the influence of IHC on the FNR of SLNB after NAC. In Tan’s review, the summary FNRs of SLNB after NAC were 9% and 12% in the groups with and without IHC utility, respectively (P = 0.45) [<xref rid="pone.0162605.ref049" ref-type="bibr">49</xref>]. Meanwhile, a meta-regression conducted by Fu et al. identified IHC as an independent factor underlying the heterogeneity of FNR (P = 0.04) [<xref rid="pone.0162605.ref050" ref-type="bibr">50</xref>]. Further analysis revealed that the FNR in the IHC-plus-H&E group was significant lower than in the H&E-alone group (8.7% vs 16.0%, P = 0.001). In the present meta-analysis, the pooled FNRs were 4% in the IHC-plus-H&E group and 11% in the H&E-alone group. There was no significant difference between the two groups (P = 0.241). Further studies are needed to investigate the benefit of IHC in SLNB after NAC.</p><p>It has been reported that in 40 to 70% of patients, the SN is the only involved axillary node in early breast cancer [<xref rid="pone.0162605.ref060" ref-type="bibr">60</xref>–<xref rid="pone.0162605.ref062" ref-type="bibr">62</xref>]. Predicting the status of non-SN will spare some SN-positive patients from ALND. The situation in initially clinically node-negative breast cancer patients after NAC is unclear. Evaluating the metastatic rate to non-SNs according to SN status in these patients would be of great value. We could only extract these data from 3 articles for analysis. The metastatic rate to non-SNs according to SN status is shown in <xref ref-type="table" rid="pone.0162605.t006">Table 6</xref>. In Yu’s study, the metastatic rate in SN-positive patients is noticeably higher because only T3 tumor patients were included in that study. The information that we could obtain from those three studies was limited, and further study is needed to address this issue.</p><table-wrap id="pone.0162605.t006" orientation="portrait" position="float"><object-id pub-id-type="doi">10.1371/journal.pone.0162605.t006</object-id><label>Table 6</label><caption><title>The metastatic rate to non-SNs according to SN status in initially clinically node-negative breast cancer patients after NAC.</title></caption><alternatives><graphic id="pone.0162605.t006g" xlink:href="pone.0162605.t006"></graphic><table frame="hsides" rules="groups"><colgroup span="1"><col align="left" valign="middle" span="1"></col><col align="left" valign="middle" span="1"></col><col align="left" valign="middle" span="1"></col></colgroup><thead><tr><th align="center" rowspan="1" colspan="1">Study</th><th align="left" rowspan="1" colspan="1">Non SN metastatic rate in SN positive patients</th><th align="left" rowspan="1" colspan="1">Non SN metastatic rate in SN negative patients</th></tr></thead><tbody><tr><td align="left" style="background-color:#d7d7d7" rowspan="1" colspan="1">Tanaka et al</td><td align="left" style="background-color:#d7d7d7" rowspan="1" colspan="1">0%(0/4)</td><td align="left" style="background-color:#d7d7d7" rowspan="1" colspan="1">0%(0/13)</td></tr><tr><td align="left" rowspan="1" colspan="1">Yu et al.</td><td align="left" rowspan="1" colspan="1">62.5%(40/64)</td><td align="left" rowspan="1" colspan="1">9.6%(5/52)</td></tr><tr><td align="left" style="background-color:#d7d7d7" rowspan="1" colspan="1">Kinoshita et al.</td><td align="left" style="background-color:#d7d7d7" rowspan="1" colspan="1">33.3%(4/12)</td><td align="left" style="background-color:#d7d7d7" rowspan="1" colspan="1">5%(2/40)</td></tr></tbody></table></alternatives></table-wrap><p>Only studies published in English were included in our meta-analysis, which may have led to publication bias. In addition, studies favoring the use of SLNB after NAC are more likely to be published, which may cause a bias in favor of SLNB. Funnel plots were used to evaluate the publication bias in the present meta-analysis, and the results indicated there was minimal publication bias. Begg’s test further confirmed these results.</p><p>In conclusion, based on current evidence, SLNB is technically feasible and accurate enough for staging the axilla in initially clinically node-negative breast cancer after NAC.</p></sec><sec sec-type="supplementary-material" id="sec018"><title>Supporting Information</title><supplementary-material content-type="local-data" id="pone.0162605.s001"><label>S1 File</label><caption><title>Questions used to assess the quality of the literature.</title><p>(DOCX)</p></caption><media xlink:href="pone.0162605.s001.docx"><caption><p>Click here for additional data file.</p></caption></media></supplementary-material><supplementary-material content-type="local-data" id="pone.0162605.s002"><label>S1 Table</label><caption><title>PRISMA Checklist.</title><p>(DOC)</p></caption><media xlink:href="pone.0162605.s002.doc"><caption><p>Click here for additional data file.</p></caption></media></supplementary-material></sec></body><back><ref-list><title>References</title><ref id="pone.0162605.ref001"><label>1</label><mixed-citation publication-type="journal"><name><surname>Samphao</surname><given-names>S</given-names></name>, <name><surname>Eremin</surname><given-names>JM</given-names></name>, <name><surname>El-Sheemy</surname><given-names>M</given-names></name>, <name><surname>Eremin</surname><given-names>O</given-names></name>. <article-title>Management of the axilla in women with breast cancer: current clinical practice and a new selective targeted approach</article-title>. <source>Annals of surgical oncology</source>. <year>2008</year>;<volume>15</volume>(<issue>5</issue>):<fpage>1282</fpage>–<lpage>96</lpage>. <comment>doi: <ext-link ext-link-type="uri" xlink:href="http://dx.doi.org/10.1245/s10434-008-9863-8">10.1245/s10434-008-9863-8</ext-link></comment> .<pub-id pub-id-type="pmid">18330650</pub-id></mixed-citation></ref><ref id="pone.0162605.ref002"><label>2</label><mixed-citation publication-type="journal"><name><surname>Botteri</surname><given-names>E</given-names></name>, <name><surname>Bagnardi</surname><given-names>V</given-names></name>, <name><surname>Rotmensz</surname><given-names>N</given-names></name>, <name><surname>Gentilini</surname><given-names>O</given-names></name>, <name><surname>Disalvatore</surname><given-names>D</given-names></name>, <name><surname>Bazolli</surname><given-names>B</given-names></name>, <etal>et al</etal><article-title>Analysis of local and regional recurrences in breast cancer after conservative surgery</article-title>. <source>Annals of oncology: official journal of the European Society for Medical Oncology / ESMO</source>. <year>2010</year>;<volume>21</volume>(<issue>4</issue>):<fpage>723</fpage>–<lpage>8</lpage>. <comment>doi: <ext-link ext-link-type="uri" xlink:href="http://dx.doi.org/10.1093/annonc/mdp386">10.1093/annonc/mdp386</ext-link></comment> .<pub-id pub-id-type="pmid">19833817</pub-id></mixed-citation></ref><ref id="pone.0162605.ref003"><label>3</label><mixed-citation publication-type="journal"><name><surname>Yin</surname><given-names>K</given-names></name>, <name><surname>Zhou</surname><given-names>L</given-names></name>, <name><surname>Shao</surname><given-names>Z</given-names></name>, <name><surname>Yin</surname><given-names>W</given-names></name>, <name><surname>Lu</surname><given-names>J</given-names></name>. <article-title>Clinical significance of locoregional and systemic treatment in operable high-risk breast cancer patients with more than four positive axillary lymph nodes</article-title>. <source>OncoTargets and therapy</source>. <year>2015</year>;<volume>8</volume>:<fpage>2665</fpage>–<lpage>73</lpage>. <comment>doi: <ext-link ext-link-type="uri" xlink:href="http://dx.doi.org/10.2147/OTT.S88216">10.2147/OTT.S88216</ext-link></comment> ; 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