Breast Cancer Subtype is Associated With Axillary Lymph Node Metastasis
Identifieur interne : 000378 ( Pmc/Corpus ); précédent : 000377; suivant : 000379Breast Cancer Subtype is Associated With Axillary Lymph Node Metastasis
Auteurs : Zhen-Yu He ; San-Gang Wu ; Qi Yang ; Jia-Yuan Sun ; Feng-Yan Li ; Qin Lin ; Huan-Xin LinSource :
- Medicine [ 0025-7974 ] ; 2015.
Abstract
The purpose of this study was to assess whether breast cancer subtype (BCS) as determined by estrogen receptor, progesterone receptor, and human epidermal growth factor receptor 2 can predict the axillary lymph node metastasis in breast cancer.
Patients who received breast conserving surgery or mastectomy and axillary lymph node dissection were identified from 2 cancer centers. The associations between clinicopathological variables and axillary lymph node involvement were evaluated in univariate and multivariate regression analyses.
A total of 3471 patients met the inclusion criteria, and 53.0% had axillary lymph node metastases at diagnosis. Patients with hormone receptor (HR)−/human epidermal growth factor receptor 2 (HER2)− subtype had a higher grade disease and the lowest rate of lymphovascular invasion. Univariate and multivariable logistic regression analyses showed that BCS was significantly associated with lymph node involvement. Patients with the HR−/HER2− subtype had the lowest odds of having nodal positivity than those with other BCSs. HR+/HER2− (odds ratio [OR] 1.651, 95% confidence interval [CI]: 1.349–2.021,
Breast cancer subtype can predict the presence of axillary lymph node metastasis in breast cancer. HR−/HER2− is associated with a reduced risk of axillary lymph node metastasis compared to other BCSs. Our findings may play an important role in guiding axillary treatment considerations if further confirmed in larger sample size studies.
Url:
DOI: 10.1097/MD.0000000000002213
PubMed: 26632910
PubMed Central: 4674213
Links to Exploration step
PMC:4674213Le document en format XML
<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Breast Cancer Subtype is Associated With Axillary Lymph Node Metastasis</title><author><name sortKey="He, Zhen Yu" sort="He, Zhen Yu" uniqKey="He Z" first="Zhen-Yu" last="He">Zhen-Yu He</name></author><author><name sortKey="Wu, San Gang" sort="Wu, San Gang" uniqKey="Wu S" first="San-Gang" last="Wu">San-Gang Wu</name></author><author><name sortKey="Yang, Qi" sort="Yang, Qi" uniqKey="Yang Q" first="Qi" last="Yang">Qi Yang</name></author><author><name sortKey="Sun, Jia Yuan" sort="Sun, Jia Yuan" uniqKey="Sun J" first="Jia-Yuan" last="Sun">Jia-Yuan Sun</name></author><author><name sortKey="Li, Feng Yan" sort="Li, Feng Yan" uniqKey="Li F" first="Feng-Yan" last="Li">Feng-Yan Li</name></author><author><name sortKey="Lin, Qin" sort="Lin, Qin" uniqKey="Lin Q" first="Qin" last="Lin">Qin Lin</name></author><author><name sortKey="Lin, Huan Xin" sort="Lin, Huan Xin" uniqKey="Lin H" first="Huan-Xin" last="Lin">Huan-Xin Lin</name></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">26632910</idno><idno type="pmc">4674213</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4674213</idno><idno type="RBID">PMC:4674213</idno><idno type="doi">10.1097/MD.0000000000002213</idno><date when="2015">2015</date><idno type="wicri:Area/Pmc/Corpus">000378</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000378</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Breast Cancer Subtype is Associated With Axillary Lymph Node Metastasis</title><author><name sortKey="He, Zhen Yu" sort="He, Zhen Yu" uniqKey="He Z" first="Zhen-Yu" last="He">Zhen-Yu He</name></author><author><name sortKey="Wu, San Gang" sort="Wu, San Gang" uniqKey="Wu S" first="San-Gang" last="Wu">San-Gang Wu</name></author><author><name sortKey="Yang, Qi" sort="Yang, Qi" uniqKey="Yang Q" first="Qi" last="Yang">Qi Yang</name></author><author><name sortKey="Sun, Jia Yuan" sort="Sun, Jia Yuan" uniqKey="Sun J" first="Jia-Yuan" last="Sun">Jia-Yuan Sun</name></author><author><name sortKey="Li, Feng Yan" sort="Li, Feng Yan" uniqKey="Li F" first="Feng-Yan" last="Li">Feng-Yan Li</name></author><author><name sortKey="Lin, Qin" sort="Lin, Qin" uniqKey="Lin Q" first="Qin" last="Lin">Qin Lin</name></author><author><name sortKey="Lin, Huan Xin" sort="Lin, Huan Xin" uniqKey="Lin H" first="Huan-Xin" last="Lin">Huan-Xin Lin</name></author></analytic><series><title level="j">Medicine</title><idno type="ISSN">0025-7974</idno><idno type="eISSN">1536-5964</idno><imprint><date when="2015">2015</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><title>Abstract</title><p>The purpose of this study was to assess whether breast cancer subtype (BCS) as determined by estrogen receptor, progesterone receptor, and human epidermal growth factor receptor 2 can predict the axillary lymph node metastasis in breast cancer.</p><p>Patients who received breast conserving surgery or mastectomy and axillary lymph node dissection were identified from 2 cancer centers. The associations between clinicopathological variables and axillary lymph node involvement were evaluated in univariate and multivariate regression analyses.</p><p>A total of 3471 patients met the inclusion criteria, and 53.0% had axillary lymph node metastases at diagnosis. Patients with hormone receptor (HR)−/human epidermal growth factor receptor 2 (HER2)− subtype had a higher grade disease and the lowest rate of lymphovascular invasion. Univariate and multivariable logistic regression analyses showed that BCS was significantly associated with lymph node involvement. Patients with the HR−/HER2− subtype had the lowest odds of having nodal positivity than those with other BCSs. HR+/HER2− (odds ratio [OR] 1.651, 95% confidence interval [CI]: 1.349–2.021, <italic>P</italic> < 0.001), HR+/HER2+ (OR 1.958, 95%CI 1.542–2.486, <italic>P</italic> < 0.001), and HR−/HER2+ (OR 1.525, 95%CI 1.181–1.970, <italic>P</italic> < 0.001) tumors had higher risk of nodal positivity than the HR−/HER2− subtype. The other independent predictors of nodal metastases included tumor size, tumor grade, and lymphovascular invasion.</p><p>Breast cancer subtype can predict the presence of axillary lymph node metastasis in breast cancer. HR−/HER2− is associated with a reduced risk of axillary lymph node metastasis compared to other BCSs. Our findings may play an important role in guiding axillary treatment considerations if further confirmed in larger sample size studies.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Layeequr Rahman, R" uniqKey="Layeequr Rahman R">R Layeequr Rahman</name></author><author><name sortKey="Crawford, Sl" uniqKey="Crawford S">SL Crawford</name></author><author><name sortKey="Siwawa, P" uniqKey="Siwawa P">P Siwawa</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Giuliano, Ae" uniqKey="Giuliano A">AE Giuliano</name></author><author><name sortKey="Mccall, L" uniqKey="Mccall L">L McCall</name></author><author><name sortKey="Beitsch, P" uniqKey="Beitsch P">P Beitsch</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Giuliano, Ae" uniqKey="Giuliano A">AE Giuliano</name></author><author><name sortKey="Hunt, Kk" uniqKey="Hunt K">KK Hunt</name></author><author><name sortKey="Ballman, Kv" uniqKey="Ballman K">KV Ballman</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Bevilacqua, Jl" uniqKey="Bevilacqua J">JL Bevilacqua</name></author><author><name sortKey="Kattan, Mw" uniqKey="Kattan M">MW Kattan</name></author><author><name sortKey="Fey, Jv" uniqKey="Fey J">JV Fey</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Yoshihara, E" uniqKey="Yoshihara E">E Yoshihara</name></author><author><name sortKey="Smeets, A" uniqKey="Smeets A">A Smeets</name></author><author><name sortKey="Laenen, A" uniqKey="Laenen A">A Laenen</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Viale, G" uniqKey="Viale G">G Viale</name></author><author><name sortKey="Zurrida, S" uniqKey="Zurrida S">S Zurrida</name></author><author><name sortKey="Maiorano, E" uniqKey="Maiorano E">E Maiorano</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Greer, Lt" uniqKey="Greer L">LT Greer</name></author><author><name sortKey="Rosman, M" uniqKey="Rosman M">M Rosman</name></author><author><name sortKey="Charles Mylander, W" uniqKey="Charles Mylander W">W Charles Mylander</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Crabb, Sj" uniqKey="Crabb S">SJ Crabb</name></author><author><name sortKey="Cheang, Mc" uniqKey="Cheang M">MC Cheang</name></author><author><name sortKey="Leung, S" uniqKey="Leung S">S Leung</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="S Rlie, T" uniqKey="S Rlie T">T Sørlie</name></author><author><name sortKey="Perou, Cm" uniqKey="Perou C">CM Perou</name></author><author><name sortKey="Tibshirani, R" uniqKey="Tibshirani R">R Tibshirani</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Carey, La" uniqKey="Carey L">LA Carey</name></author><author><name sortKey="Perou, Cm" uniqKey="Perou C">CM Perou</name></author><author><name sortKey="Livasy, Ca" uniqKey="Livasy C">CA Livasy</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Hugh, J" uniqKey="Hugh J">J Hugh</name></author><author><name sortKey="Hanson, J" uniqKey="Hanson J">J Hanson</name></author><author><name sortKey="Cheang, Mc" uniqKey="Cheang M">MC Cheang</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Wu, Sg" uniqKey="Wu S">SG Wu</name></author><author><name sortKey="He, Zy" uniqKey="He Z">ZY He</name></author><author><name sortKey="Li, Q" uniqKey="Li Q">Q Li</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Kyndi, M" uniqKey="Kyndi M">M Kyndi</name></author><author><name sortKey="S Rensen, Fb" uniqKey="S Rensen F">FB Sørensen</name></author><author><name sortKey="Knudsen, H" uniqKey="Knudsen H">H Knudsen</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Holm Rasmussen, Ev" uniqKey="Holm Rasmussen E">EV Holm-Rasmussen</name></author><author><name sortKey="Jensen, Mb" uniqKey="Jensen M">MB Jensen</name></author><author><name sortKey="Balslev, E" uniqKey="Balslev E">E Balslev</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Ugras, S" uniqKey="Ugras S">S Ugras</name></author><author><name sortKey="Stempel, M" uniqKey="Stempel M">M Stempel</name></author><author><name sortKey="Patil, S" uniqKey="Patil S">S Patil</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Lee, Jh" uniqKey="Lee J">JH Lee</name></author><author><name sortKey="Kim, Sh" uniqKey="Kim S">SH Kim</name></author><author><name sortKey="Suh, Yj" uniqKey="Suh Y">YJ Suh</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Gangi, A" uniqKey="Gangi A">A Gangi</name></author><author><name sortKey="Mirocha, J" uniqKey="Mirocha J">J Mirocha</name></author><author><name sortKey="Leong, T" uniqKey="Leong T">T Leong</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Wiechmann, L" uniqKey="Wiechmann L">L Wiechmann</name></author><author><name sortKey="Sampson, M" uniqKey="Sampson M">M Sampson</name></author><author><name sortKey="Stempel, M" uniqKey="Stempel M">M Stempel</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Li, Fy" uniqKey="Li F">FY Li</name></author><author><name sortKey="Wu, Sg" uniqKey="Wu S">SG Wu</name></author><author><name sortKey="Zhou, J" uniqKey="Zhou J">J Zhou</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Wildiers, H" uniqKey="Wildiers H">H Wildiers</name></author><author><name sortKey="Van Calster, B" uniqKey="Van Calster B">B Van Calster</name></author><author><name sortKey="Van De Poll Franse, Lv" uniqKey="Van De Poll Franse L">LV van de Poll-Franse</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Fan, L" uniqKey="Fan L">L Fan</name></author><author><name sortKey="Strasser Weippl, K" uniqKey="Strasser Weippl K">K Strasser-Weippl</name></author><author><name sortKey="Li, Jj" uniqKey="Li J">JJ Li</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Mamounas, Ep" uniqKey="Mamounas E">EP Mamounas</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Zhu, X" uniqKey="Zhu X">X Zhu</name></author><author><name sortKey="Ying, J" uniqKey="Ying J">J Ying</name></author><author><name sortKey="Wang, F" uniqKey="Wang F">F Wang</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Mattes, Md" uniqKey="Mattes M">MD Mattes</name></author><author><name sortKey="Bhatia, Jk" uniqKey="Bhatia J">JK Bhatia</name></author><author><name sortKey="Metzger, D" uniqKey="Metzger D">D Metzger</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Schoppmann, Sf" uniqKey="Schoppmann S">SF Schoppmann</name></author><author><name sortKey="Bayer, G" uniqKey="Bayer G">G Bayer</name></author><author><name sortKey="Aumayr, K" uniqKey="Aumayr K">K Aumayr</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Moo, Ta" uniqKey="Moo T">TA Moo</name></author><author><name sortKey="Mcmillan, R" uniqKey="Mcmillan R">R McMillan</name></author><author><name sortKey="Lee, M" uniqKey="Lee M">M Lee</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Nofech Mozes, S" uniqKey="Nofech Mozes S">S Nofech-Mozes</name></author><author><name sortKey="Ackerman, I" uniqKey="Ackerman I">I Ackerman</name></author><author><name sortKey="Ghorab, Z" uniqKey="Ghorab Z">Z Ghorab</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Foulkes, Wd" uniqKey="Foulkes W">WD Foulkes</name></author><author><name sortKey="Smith, Ie" uniqKey="Smith I">IE Smith</name></author><author><name sortKey="Reis Filho, Js" uniqKey="Reis Filho J">JS Reis-Filho</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Sackey, H" uniqKey="Sackey H">H Sackey</name></author><author><name sortKey="Magnuson, A" uniqKey="Magnuson A">A Magnuson</name></author><author><name sortKey="Sandelin, K" uniqKey="Sandelin K">K Sandelin</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Zhou, W" uniqKey="Zhou W">W Zhou</name></author><author><name sortKey="He, Z" uniqKey="He Z">Z He</name></author><author><name sortKey="Xue, J" uniqKey="Xue J">J Xue</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Freedman, Gm" uniqKey="Freedman G">GM Freedman</name></author><author><name sortKey="Fowble, Bl" uniqKey="Fowble B">BL Fowble</name></author><author><name sortKey="Li, T" uniqKey="Li T">T Li</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Goldhirsch, A" uniqKey="Goldhirsch A">A Goldhirsch</name></author><author><name sortKey="Winer, Ep" uniqKey="Winer E">EP Winer</name></author><author><name sortKey="Coates, As" uniqKey="Coates A">AS Coates</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Mojarad, S" uniqKey="Mojarad S">S Mojarad</name></author><author><name sortKey="Venturini, B" uniqKey="Venturini B">B Venturini</name></author><author><name sortKey="Fulgenzi, P" uniqKey="Fulgenzi P">P Fulgenzi</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Terasaki Fukuzawa, Y" uniqKey="Terasaki Fukuzawa Y">Y Terasaki-Fukuzawa</name></author><author><name sortKey="Kijima, H" uniqKey="Kijima H">H Kijima</name></author><author><name sortKey="Suto, A" uniqKey="Suto A">A Suto</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Dabritz, G" uniqKey="Dabritz G">G Dabritz</name></author><author><name sortKey="Miswan, A" uniqKey="Miswan A">A Miswan</name></author><author><name sortKey="Rowe, N" uniqKey="Rowe N">N Rowe</name></author></analytic></biblStruct></listBibl></div1></back></TEI><pmc article-type="research-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">Medicine (Baltimore)</journal-id><journal-id journal-id-type="iso-abbrev">Medicine (Baltimore)</journal-id><journal-id journal-id-type="publisher-id">MEDI</journal-id><journal-title-group><journal-title>Medicine</journal-title></journal-title-group><issn pub-type="ppub">0025-7974</issn><issn pub-type="epub">1536-5964</issn><publisher><publisher-name>Wolters Kluwer Health</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">26632910</article-id><article-id pub-id-type="pmc">4674213</article-id><article-id pub-id-type="doi">10.1097/MD.0000000000002213</article-id><article-id pub-id-type="art-access-id">02213</article-id><article-categories><subj-group subj-group-type="heading"><subject>4400</subject></subj-group><subj-group><subject>Research Article</subject><subject>Observational Study</subject></subj-group></article-categories><title-group><article-title>Breast Cancer Subtype is Associated With Axillary Lymph Node Metastasis</article-title><subtitle>A Retrospective Cohort Study</subtitle></title-group><contrib-group><contrib contrib-type="author"><name><surname>He</surname><given-names>Zhen-Yu</given-names></name><degrees>MD</degrees></contrib><contrib contrib-type="author"><name><surname>Wu</surname><given-names>San-Gang</given-names></name><degrees>MD</degrees></contrib><contrib contrib-type="author"><name><surname>Yang</surname><given-names>Qi</given-names></name><degrees>MD</degrees></contrib><contrib contrib-type="author"><name><surname>Sun</surname><given-names>Jia-Yuan</given-names></name><degrees>MD</degrees></contrib><contrib contrib-type="author"><name><surname>Li</surname><given-names>Feng-Yan</given-names></name><degrees>MD</degrees></contrib><contrib contrib-type="author"><name><surname>Lin</surname><given-names>Qin</given-names></name><degrees>MD</degrees></contrib><contrib contrib-type="author"><name><surname>Lin</surname><given-names>Huan-Xin</given-names></name><degrees>MD</degrees></contrib></contrib-group><contrib-group><contrib contrib-type="editor"><name><surname>Banswal.</surname><given-names>Lalit</given-names></name></contrib></contrib-group><aff>From the Department of Radiation Oncology, Sun Yat-sen University Cancer Center, State Key Laboratory of Oncology in South China, Collaborative Innovation Center for Cancer Medicine, Guangzhou (Z-YH, J-YS, F-YL, H-XL); Department of Radiation Oncology, Xiamen Cancer Center, the First Affiliated Hospital of Xiamen University, Xiamen (S-GW, QL); and Department of Nasopharyngeal Carcinoma, Sun Yat-sen University Cancer Center, State Key Laboratory of Oncology in South China, Collaborative Innovation Center of Cancer Medicine, Guangzhou, People's Republic of China (QY).</aff><author-notes><corresp>Correspondence: Qin Lin, Department of Radiation Oncology, Xiamen Cancer Center, the First Affiliated Hospital of Xiamen University, Xiamen, People's Republic of China (e-mail: <email>linqin05@163.com</email>).</corresp><corresp>Huan-Xin Lin, Department of Radiation Oncology, Sun Yat-sen University Cancer Center, State Key Laboratory of Oncology in South China, Collaborative Innovation Center for Cancer Medicine, Guangzhou, People's Republic of China (e-mail: <email>linhx@sysucc.org.cn</email>).</corresp></author-notes><pub-date pub-type="collection"><month>12</month><year>2015</year></pub-date><pub-date pub-type="epub"><day>07</day><month>12</month><year>2015</year></pub-date><volume>94</volume><issue>48</issue><elocation-id>e2213</elocation-id><history><date date-type="received"><day>31</day><month>7</month><year>2015</year></date><date date-type="rev-recd"><day>7</day><month>10</month><year>2015</year></date><date date-type="accepted"><day>9</day><month>11</month><year>2015</year></date></history><permissions><copyright-statement>Copyright © 2015 Wolters Kluwer Health, Inc. All rights reserved.</copyright-statement><copyright-year>2015</copyright-year><license license-type="open-access" xlink:href="http://creativecommons.org/licenses/by/4.0"><license-p>This is an open access article distributed under the Creative Commons Attribution License 4.0, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. <ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0">http://creativecommons.org/licenses/by/4.0</ext-link></license-p></license></permissions><self-uri xlink:type="simple" xlink:href="medi-94-e2213.pdf"></self-uri><abstract><title>Abstract</title><p>The purpose of this study was to assess whether breast cancer subtype (BCS) as determined by estrogen receptor, progesterone receptor, and human epidermal growth factor receptor 2 can predict the axillary lymph node metastasis in breast cancer.</p><p>Patients who received breast conserving surgery or mastectomy and axillary lymph node dissection were identified from 2 cancer centers. The associations between clinicopathological variables and axillary lymph node involvement were evaluated in univariate and multivariate regression analyses.</p><p>A total of 3471 patients met the inclusion criteria, and 53.0% had axillary lymph node metastases at diagnosis. Patients with hormone receptor (HR)−/human epidermal growth factor receptor 2 (HER2)− subtype had a higher grade disease and the lowest rate of lymphovascular invasion. Univariate and multivariable logistic regression analyses showed that BCS was significantly associated with lymph node involvement. Patients with the HR−/HER2− subtype had the lowest odds of having nodal positivity than those with other BCSs. HR+/HER2− (odds ratio [OR] 1.651, 95% confidence interval [CI]: 1.349–2.021, <italic>P</italic> < 0.001), HR+/HER2+ (OR 1.958, 95%CI 1.542–2.486, <italic>P</italic> < 0.001), and HR−/HER2+ (OR 1.525, 95%CI 1.181–1.970, <italic>P</italic> < 0.001) tumors had higher risk of nodal positivity than the HR−/HER2− subtype. The other independent predictors of nodal metastases included tumor size, tumor grade, and lymphovascular invasion.</p><p>Breast cancer subtype can predict the presence of axillary lymph node metastasis in breast cancer. HR−/HER2− is associated with a reduced risk of axillary lymph node metastasis compared to other BCSs. Our findings may play an important role in guiding axillary treatment considerations if further confirmed in larger sample size studies.</p></abstract><custom-meta-group><custom-meta><meta-name>OPEN-ACCESS</meta-name><meta-value>TRUE</meta-value></custom-meta></custom-meta-group></article-meta></front><body><sec sec-type="intro"><title>INTRODUCTION</title><p>Axillary lymph node status is an important factor in determining the staging, prognosis, and treatment of breast cancer patients.<sup><xref rid="R1" ref-type="bibr">1</xref></sup> However, there is still a great deal of controversy exists regarding the management of axillary lymph nodes in breast cancer. Sentinel lymph nodes have been used in the evaluation of axillary lymph node status in early stage breast cancer patients.<sup><xref rid="R2" ref-type="bibr">2</xref>,<xref rid="R3" ref-type="bibr">3</xref></sup> Several predict factors of axillary lymph node metastasis have been described such as age, tumor location, tumor size, histologic grade, and lymphovascular invasion (LVI).<sup><xref rid="R4" ref-type="bibr">4</xref>–<xref rid="R8" ref-type="bibr">8</xref></sup></p><p>Recently, the immunohistochemical analyses of expression of estrogen receptor (ER), progesterone receptor (PR), and human epidermal growth factor receptor 2 (HER2), are widely used to divide into 4 breast cancer subtypes (BCSs). The BCSs are used to guide the system treatment, and predict response to therapy and disease outcome.<sup><xref rid="R9" ref-type="bibr">9</xref>–<xref rid="R13" ref-type="bibr">13</xref></sup> However, the role of BCS on axillary lymph node status has not been well established.<sup><xref rid="R14" ref-type="bibr">14</xref>–<xref rid="R18" ref-type="bibr">18</xref></sup> In this study, we retrospectively reviewed the clinicopathological data of breast cancer patients from 2 cancer centers aiming to investigate the association between the BCS status and axillary lymph node involvement, and to assess whether the BCS might be used to guide axillary management decisions.</p></sec><sec sec-type="subjects"><title>PATIENTS AND METHODS</title><sec sec-type="subjects"><title>Patients</title><p>Clinicopathological information of patients who were treated at the First Hospital of Xiamen University (Xiamen Cancer Center, XMCC) between January 2008 and March 2012 and Sun Yat-sen University Cancer Center (SYSUCC) between January 1998 and December 2007 were collected. The inclusion criteria were: (1) female patients with unilateral invasive breast cancer without distant metastasis at diagnosis; (2) received mastectomy or breast-conserving surgery and axillary lymph node dissection; (3) without neoadjuvant therapy; (4) had complete clinicopathological information including ER, PR, and HER2 status. The study was approved by the ethics committee of the First Affiliated Hospital of Xiamen University and SYSUCC.</p></sec><sec sec-type="subjects"><title>Classification Criteria for Patients</title><p>BCSs were defined as follows: HR+/HER2− (ER+ and/or PR+, HER2−), HR+/HER2+ (ER+ and/or PR+, HER2+), HR−/HER2+ (ER−, PR−, and HER2+), and HR−/HER2− (ER−, PR−, and HER2−, TNBC). Hormone receptor (HR) positivity was defined as >1% of ER or PR positive cells by immunohistochemistry. HER2 positivity was defined as immunohistochemical grade of 3+ before 2003 and was defined as immunohistochemical grade of 3+, or 2+ was determined by fluorescence <italic>in situ</italic> hybridization (FISH) after 2003. The cutoff point for Ki-67 was 25% according to our previous reports.<sup><xref rid="R19" ref-type="bibr">19</xref></sup></p><p>Nodal metastasis was defined as the presence of any tumor cells in a lymph node. Breast cancer was staged according to the seventh edition American Joint Committee on Cancer (AJCC)/ Union for International Cancer Control (UICC) staging system. Clinicopathological factors that would impact the axillary lymph node status were then analyzed, including age, menstrual status, tumor size, histologic grade, LVI, ER, PR, HER2, Ki-67, and BCS.</p></sec><sec><title>Statistical Analysis</title><p>All data were analyzed using the SPSS statistical software package (version 16.0; IBM Corporation, Armonk, NY). The χ<sup>2</sup> test and Fisher's exact probability tests were used for categorical variables, and analysis of variance for continuous variables, to compare the distribution of clinicopathological characteristics among BCSs. The relationship between patient characteristics and axillary lymph node metastases was examined by univariate and multivariable logistic regression analyses. Factors that were statistically significant in univariate analysis were entered into multivariable logistic regression analysis. A <italic>P</italic> value < 0.05 was considered significant in all analyses.</p></sec></sec><sec sec-type="results"><title>RESULTS</title><p>A total of 3471 patients included in this study, 662 (19.1%) patients were from XMCC and 2809 (80.9%) patients were from SYSUCC. Patient and tumor characteristics are shown in Table <xref ref-type="table" rid="T1">1</xref>. There were 53.0% of patients had nodal positivity, 57.9% of patients were ER+, 63.4% were PR+, and 33.1% were HER2+. Patients’ tumors were categorized as HR+/HER2− in 1763 (50.8%), HR+/HER2+ in 666 (19.2%), HR−/HER2+ in 481 (13.9%), and HR−/HER2− in 561 (16.1%). Patient and tumor characteristics categorized by BCS are shown in Table <xref ref-type="table" rid="T2">2</xref>. Among the BCSs, there were significant differences in age (<italic>P</italic> = 0.021), menopausal status (<italic>P</italic> < 0.001), tumor size (<italic>P</italic> < 0.001), nodal stage (<italic>P</italic> < 0.001), grade (<italic>P</italic> < 0.001), LVI (<italic>P</italic> = 0.005), and Ki-67 (<italic>P</italic> < 0.001). Patients with HR−/HER2− subtype had a higher grade disease and the lowest rate of LVI. Significantly more patients with high Ki-67 expression were HR+/HER2− subtype than did those with other BCSs (<italic>P</italic> < 0.001).</p><table-wrap id="T1" position="float"><label>TABLE 1</label><caption><p>Clinicopathological Characteristics of Patients With Breast Cancer in 2 Cancer Center</p></caption><graphic xlink:href="medi-94-e2213-g001"></graphic></table-wrap><table-wrap id="T2" position="float"><label>TABLE 2</label><caption><p>Patient and Tumor Characteristics by Breast Cancer Subtype</p></caption><graphic xlink:href="medi-94-e2213-g002"></graphic></table-wrap><p>The results of the univariate logistic regression analysis are shown in Table <xref ref-type="table" rid="T3">3</xref>. Larger tumor size, higher grade, LVI, ER+, PR+, and HER2+ were associated with a higher risk of lymph node metastases. Breast cancer subtype was a significant predictor of nodal positivity. The HR+/HER2−, HR+/HER2+, and HR−/HER2+ subtypes had a significantly higher risk of having positive lymph nodes, whereas the HR−/HER− subtype was associated with a reduced risk of lymph node metastasis (Fig. <xref ref-type="fig" rid="F1">1</xref>).</p><table-wrap id="T3" position="float"><label>TABLE 3</label><caption><p>Univariate Logistic Regression of Axillary Lymph Node Metastasis</p></caption><graphic xlink:href="medi-94-e2213-g003"></graphic></table-wrap><fig id="F1" position="float"><label>FIGURE 1</label><caption><p>The frequency (%) of nodal positivity according to the breast cancer subtype.</p></caption><graphic xlink:href="medi-94-e2213-g004"></graphic></fig><p>The results of the multivariable analysis are shown in Table <xref ref-type="table" rid="T4">4</xref>. In model 1, when adjusted for tumor size, grade, LVI, ER, PR, and HER2, larger tumor size, higher grade, LVI, PR+, and HER2+ were risk factors of axillary lymph nodes metastasis. In model 2, after adjusting for tumor size, grade, LVI, and BCS, tumor size, grade, and LVI remained predictors of lymph node metastases. Patients with the HR−/HER2− subtype had the lowest odds of nodal positivity compared to other BCSs. HR+/HER2− (odds ratio [OR] 1.651, 95% confidence interval [CI]: 1.349–2.021, <italic>P</italic> < 0.001), HR+/HER2+ (OR 1.958, 95%CI 1.542–2.486, <italic>P</italic> < 0.001), and HR−/HER2+ (OR 1.525, 95%CI 1.181–1.970, <italic>P</italic> < 0.001) tumors had higher risk of have lymph node metastases than the HR–/HER2– subtype. The HR−/HER2+ subtype had a reduced risk of axillary lymph node metastasis as compared to the HR+/HER2+ subtype, with an OR of 0.779 (95 % CI: 0.609–0.997, <italic>P</italic> = 0.048).</p><table-wrap id="T4" position="float"><label>TABLE 4</label><caption><p>Multivariate Logistic Regression of Axillary Lymph Node Metastasis</p></caption><graphic xlink:href="medi-94-e2213-g005"></graphic></table-wrap></sec><sec sec-type="discussion"><title>DISCUSSION</title><p>In the present study, we assessed the clinical value of BCS for predicting axillary lymph node metastasis in breast cancer patients and the results showed that HR−/HER2− subtype was associated with a lower risk of lymph node metastasis as compared to other BCSs.</p><p>The status of the axillary lymph node is an important prognostic factor in breast cancer patients. Studies from Western countries showed that age, tumor location, tumor stage, grade, and LVI could be used to evaluate the axillary lymph node status.<sup><xref rid="R4" ref-type="bibr">4</xref>–<xref rid="R8" ref-type="bibr">8</xref></sup> Our findings from a Chinese population showed that tumor stage, grade, and LVI were also factors affecting the axillary lymph node status, but no relationship with age. Similar findings were also observed in a study conducted in Korea.<sup><xref rid="R16" ref-type="bibr">16</xref></sup> There is evidence showing that women are more likely to have positive lymph nodes with increasing age, but the age distribution of breast cancer patients in Eastern was different from those of Western countries.<sup><xref rid="R20" ref-type="bibr">20</xref>,<xref rid="R21" ref-type="bibr">21</xref></sup> Thus, the value of age as a predictor of axillary lymph node status is influenced by other factors.<sup><xref rid="R22" ref-type="bibr">22</xref></sup></p><p>In this study, 3471 patients were included from 2 cancer centers and the results showed that TNBC patients had a lower risk of axillary lymph node metastasis as compared to other BCS patients. The finding of this study was similar to the results of previous studies.<sup><xref rid="R14" ref-type="bibr">14</xref>,<xref rid="R15" ref-type="bibr">15</xref>,<xref rid="R23" ref-type="bibr">23</xref>,<xref rid="R24" ref-type="bibr">24</xref></sup> A study of the Danish Breast Cancer Cooperative Group database that included 20,009 patients showed that TNBC patients had a reduced risk of axillary lymph node involvement than other BCSs when adjusted for other risk factors.<sup><xref rid="R14" ref-type="bibr">14</xref></sup> Ugras et al<sup><xref rid="R15" ref-type="bibr">15</xref></sup> investigated 11,596 patients with breast cancer and found that nodal metastases were least frequent in TNBC as compared with other subtypes. A Chinese National Cancer Center study that included 3,198 patients showed that the probability of positive lymph nodes in TNBC patients was significantly lower than that in patients with other subtypes (28.2% vs 43.3–44.8%), although without multivariate analysis.<sup><xref rid="R23" ref-type="bibr">23</xref></sup> In a Surveillance, Epidemiology, and End Results study with 7,274 patients, the HR+/HER2– subtype had a higher rate of lymph node metastasis at diagnosis than the TNBC.<sup><xref rid="R24" ref-type="bibr">24</xref></sup> However, the value of BCS for predicting axillary lymph node status is still controversial. TNBC patients had a higher risk of nodal positivity (OR 2.09) in a Korean study.<sup><xref rid="R16" ref-type="bibr">16</xref></sup> In addition, Gangi et al<sup><xref rid="R17" ref-type="bibr">17</xref></sup> investigated 2,967 patients and multivariate analysis failed to show a significant difference in the lymph node status among patients with 4 BCSs. Furthermore, Wiechmann et al<sup><xref rid="R18" ref-type="bibr">18</xref></sup> reviewed the records of 6,042 patients and reported that TNBC tumors did not have involved lymph nodes more often than non-TNBC. Sample size variation across studies may produce disparate findings in the above studies.</p><p>Lymphovascular invasion has been found to be a risk factor for locoregional and distant recurrence in breast cancer patients.<sup><xref rid="R25" ref-type="bibr">25</xref>,<xref rid="R26" ref-type="bibr">26</xref></sup> Lymphovascular invasion is an obligatory step in tumor metastasis, and therefore may be a surrogate marker for metastatic potential.<sup><xref rid="R27" ref-type="bibr">27</xref></sup> However, therapeutic failure is frequently found at 3 to 5 years in TNBC patients with hematogenous metastasis.<sup><xref rid="R28" ref-type="bibr">28</xref></sup> Our results showed the frequency of LVI in TNBC patients (7.3%) was statistically lower than that in patients with other BCSs (9.4–13.4%). Ugras et al<sup><xref rid="R15" ref-type="bibr">15</xref></sup> also found that the risk for LVI in other BCSs (OR 1.7–2.5) was statistically higher than in TNBC. Based on these findings, we speculate that TNBC patients have a lower risk for axillary lymph node metastasis and might be susceptible to hematogenous metastasis, but not directly associated with lymphatic spread.</p><p>Sentinel lymph node biopsy is an important treatment for early breast cancer and is helpful to improve quality of life.<sup><xref rid="R29" ref-type="bibr">29</xref></sup> However, a method to accurately evaluate axillary lymph node status is an important prerequisite for sentinel lymph node biopsy. In patients with positive sentinel lymph nodes, the risk for positive nonsentinel nodes in TNBC patients is significantly lower than in Luminal A and Luminal B patients, but similar to that in HER2 overexpressing patients.<sup><xref rid="R30" ref-type="bibr">30</xref></sup> Freedman et al<sup><xref rid="R31" ref-type="bibr">31</xref></sup> found that TNBC had the lowest risk of nonsentinel lymph node metastasis in breast cancer patients with positive sentinel lymph nodes as compared to other subtypes. This indicates that BCS may be an important factor determining the need for axillary lymph node dissection in patients with breast cancer, and dissection may not be necessary in some TNBC patients. However, breast cancer was not subtyped in the ACOSOG Z0011 clinical trial,<sup><xref rid="R2" ref-type="bibr">2</xref>,<xref rid="R3" ref-type="bibr">3</xref></sup> and more studies are required to confirm our findings.</p><p>There are limitations in our study. First, it is a retrospective study and hence is subject to inherent biases. However, the patients included in this study were from 2 cancer centers, and the results of this study had potential impact of axillary lymph node management decisions in clinical practice. Second, because of the patients period spanned with >10 years, BCS were not determined according to the criteria developed in the St. Gallen International Breast Cancer Conference because some patients did not have immunohistochemistry for Ki-67.<sup><xref rid="R32" ref-type="bibr">32</xref></sup> We have not found the value of Ki-67 in predicting lymph node metastases; this confirms findings from previous studies.<sup><xref rid="R33" ref-type="bibr">33</xref>–<xref rid="R35" ref-type="bibr">35</xref></sup> In addition, the ER, PR, and HER2 expressions were mainly detected by immunohistochemistry, which may bias the results, but the results of immunohistochemistry have been widely used in the treatment option for patients with breast cancer.</p></sec><sec sec-type="conclusion"><title>CONCLUSIONS</title><p>In conclusion, our results show that BCS as determined by ER, PR, and HER2 status can predict axillary lymph node metastasis in breast cancer. Although TNBC is more aggressive, a lower risk for axillary lymph node metastasis compared to patients with other BCSs. The findings suggest that lymphatic metastasis is not a major pattern of metastasis in HR−/HER2− patients. Our findings may play an important role in guiding axillary treatment considerations if further confirmed in larger sample size studies.</p></sec></body><back><fn-group><fn fn-type="abbr"><p>Abbreviations: AJCC/UICC = American Joint Committee on Cancer/Union for International Cancer Control, BCS = breast cancer subtype, CI = confidence interval, ER = estrogen receptor, FISH = fluorescence in situ hybridization, HER2 = human epidermal growth factor receptor 2, HR = hormone receptor, LVI = lymphovascular invasion, OR = odds ratio, PR = progesterone receptor, SYSUCC = Sun Yat-sen University Cancer Center, TNBC = triple negative breast cancer, XMCC = Xiamen Cancer Center.</p></fn><fn fn-type="equal"><p>Z-YH and S-GW equally contributed to this study.</p></fn><fn fn-type="supported-by"><p>Funding: this work was supported by grants from the National Natural Science Foundation of China (no. 81402527), the Sci-Tech Office of Guangdong Province (no. 2013B021800157), the Youth Foundation of Fujian Provincial Health and Family Planning Commission (no. 2014-2-63), and the Natural Science Foundation of Fujian Province (no. 2015J01550).</p></fn><fn fn-type="conflict"><p>The authors have no conflicts of interest to disclose.</p></fn></fn-group><ref-list><title>REFERENCES</title><ref id="R1"><label>1.</label><mixed-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Layeequr Rahman</surname><given-names>R</given-names></name><name><surname>Crawford</surname><given-names>SL</given-names></name><name><surname>Siwawa</surname><given-names>P</given-names></name></person-group><article-title>Management of axilla in breast cancer—The saga continues</article-title>. <source><italic>Breast</italic></source><year>2015</year>; <volume>24</volume>:<fpage>343</fpage>–<lpage>353</lpage>.<pub-id pub-id-type="pmid">25937264</pub-id></mixed-citation></ref><ref id="R2"><label>2.</label><mixed-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Giuliano</surname><given-names>AE</given-names></name><name><surname>McCall</surname><given-names>L</given-names></name><name><surname>Beitsch</surname><given-names>P</given-names></name><etal></etal></person-group><article-title>Locoregional recurrence after sentinel lymph node dissection with or without axillary dissection in patients withsentinel lymph node metastases: the American College of Surgeons Oncology Group Z0011 randomized trial</article-title>. <source><italic>Ann Surg</italic></source><year>2010</year>; <volume>252</volume>:<fpage>426</fpage>–<lpage>432</lpage>.<comment>discussion 432–433</comment>.<pub-id pub-id-type="pmid">20739842</pub-id></mixed-citation></ref><ref id="R3"><label>3.</label><mixed-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Giuliano</surname><given-names>AE</given-names></name><name><surname>Hunt</surname><given-names>KK</given-names></name><name><surname>Ballman</surname><given-names>KV</given-names></name><etal></etal></person-group><article-title>Axillary dissection vs no axillary dissection in women with invasive breast cancer and sentinel node metastasis: a randomized clinical trial</article-title>. <source><italic>JAMA</italic></source><year>2011</year>; <volume>305</volume>:<fpage>569</fpage>–<lpage>575</lpage>.<pub-id pub-id-type="pmid">21304082</pub-id></mixed-citation></ref><ref id="R4"><label>4.</label><mixed-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Bevilacqua</surname><given-names>JL</given-names></name><name><surname>Kattan</surname><given-names>MW</given-names></name><name><surname>Fey</surname><given-names>JV</given-names></name><etal></etal></person-group><article-title>Doctor, what are my chances of having a positive sentinel node? A validated nomogram for risk estimation</article-title>. <source><italic>J Clin Oncol</italic></source><year>2007</year>; <volume>25</volume>:<fpage>3670</fpage>–<lpage>3679</lpage>.<pub-id pub-id-type="pmid">17664461</pub-id></mixed-citation></ref><ref id="R5"><label>5.</label><mixed-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Yoshihara</surname><given-names>E</given-names></name><name><surname>Smeets</surname><given-names>A</given-names></name><name><surname>Laenen</surname><given-names>A</given-names></name><etal></etal></person-group><article-title>Predictors of axillary lymph node metastases in early breast cancer and their applicability in clinical practice</article-title>. <source><italic>Breast</italic></source><year>2013</year>; <volume>22</volume>:<fpage>357</fpage>–<lpage>361</lpage>.<pub-id pub-id-type="pmid">23022046</pub-id></mixed-citation></ref><ref id="R6"><label>6.</label><mixed-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Viale</surname><given-names>G</given-names></name><name><surname>Zurrida</surname><given-names>S</given-names></name><name><surname>Maiorano</surname><given-names>E</given-names></name><etal></etal></person-group><article-title>Predicting the status of axillary sentinel lymph nodes in 4351 patients with invasive breast carcinoma treated in a single institution</article-title>. <source><italic>Cancer</italic></source><year>2005</year>; <volume>103</volume>:<fpage>492</fpage>–<lpage>500</lpage>.<pub-id pub-id-type="pmid">15612028</pub-id></mixed-citation></ref><ref id="R7"><label>7.</label><mixed-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Greer</surname><given-names>LT</given-names></name><name><surname>Rosman</surname><given-names>M</given-names></name><name><surname>Charles Mylander</surname><given-names>W</given-names></name><etal></etal></person-group><article-title>A prediction model for the presence of axillary lymph node involvement in women with invasive breast cancer: a focus on older women</article-title>. <source><italic>Breast J</italic></source><year>2014</year>; <volume>20</volume>:<fpage>147</fpage>–<lpage>153</lpage>.<pub-id pub-id-type="pmid">24475876</pub-id></mixed-citation></ref><ref id="R8"><label>8.</label><mixed-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Crabb</surname><given-names>SJ</given-names></name><name><surname>Cheang</surname><given-names>MC</given-names></name><name><surname>Leung</surname><given-names>S</given-names></name><etal></etal></person-group><article-title>Basal breast cancer molecular subtype predicts for lower incidence of axillary lymph node metastases in primary breast cancer</article-title>. <source><italic>Clin Breast Cancer</italic></source><year>2008</year>; <volume>8</volume>:<fpage>249</fpage>–<lpage>256</lpage>.<pub-id pub-id-type="pmid">18650155</pub-id></mixed-citation></ref><ref id="R9"><label>9.</label><mixed-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Sørlie</surname><given-names>T</given-names></name><name><surname>Perou</surname><given-names>CM</given-names></name><name><surname>Tibshirani</surname><given-names>R</given-names></name><etal></etal></person-group><article-title>Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications</article-title>. <source><italic>Proc Natl Acad Sci U S A</italic></source><year>2001</year>; <volume>98</volume>:<fpage>10869</fpage>–<lpage>10874</lpage>.<pub-id pub-id-type="pmid">11553815</pub-id></mixed-citation></ref><ref id="R10"><label>10.</label><mixed-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Carey</surname><given-names>LA</given-names></name><name><surname>Perou</surname><given-names>CM</given-names></name><name><surname>Livasy</surname><given-names>CA</given-names></name><etal></etal></person-group><article-title>Race, breast cancer subtypes, and survival in the Carolina Breast Cancer Study</article-title>. <source><italic>JAMA</italic></source><year>2006</year>; <volume>295</volume>:<fpage>2492</fpage>–<lpage>2502</lpage>.<pub-id pub-id-type="pmid">16757721</pub-id></mixed-citation></ref><ref id="R11"><label>11.</label><mixed-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Hugh</surname><given-names>J</given-names></name><name><surname>Hanson</surname><given-names>J</given-names></name><name><surname>Cheang</surname><given-names>MC</given-names></name><etal></etal></person-group><article-title>Breast cancer subtypes and response to docetaxel in node-positive breast cancer: use of an immunohistochemical definition in the BCIRG 001 trial</article-title>. <source><italic>J Clin Oncol</italic></source><year>2009</year>; <volume>27</volume>:<fpage>1168</fpage>–<lpage>1176</lpage>.<pub-id pub-id-type="pmid">19204205</pub-id></mixed-citation></ref><ref id="R12"><label>12.</label><mixed-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Wu</surname><given-names>SG</given-names></name><name><surname>He</surname><given-names>ZY</given-names></name><name><surname>Li</surname><given-names>Q</given-names></name><etal></etal></person-group><article-title>Predictive value of breast cancer molecular subtypes in Chinese patients with four or more positive nodes after postmastectomy radiotherapy</article-title>. <source><italic>Breast</italic></source><year>2012</year>; <volume>21</volume>:<fpage>657</fpage>–<lpage>661</lpage>.<pub-id pub-id-type="pmid">22835918</pub-id></mixed-citation></ref><ref id="R13"><label>13.</label><mixed-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Kyndi</surname><given-names>M</given-names></name><name><surname>Sørensen</surname><given-names>FB</given-names></name><name><surname>Knudsen</surname><given-names>H</given-names></name><etal></etal></person-group><article-title>Estrogen receptor, progesterone receptor, HER-2, and response to postmastectomy radiotherapy in high-risk breast cancer: the Danish Breast Cancer Cooperative Group</article-title>. <source><italic>J Clin Oncol</italic></source><year>2008</year>; <volume>26</volume>:<fpage>1419</fpage>–<lpage>1426</lpage>.<pub-id pub-id-type="pmid">18285604</pub-id></mixed-citation></ref><ref id="R14"><label>14.</label><mixed-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Holm-Rasmussen</surname><given-names>EV</given-names></name><name><surname>Jensen</surname><given-names>MB</given-names></name><name><surname>Balslev</surname><given-names>E</given-names></name><etal></etal></person-group><article-title>Reduced risk of axillary lymphatic spread in triple-negative breast cancer</article-title>. <source><italic>Breast Cancer Res Treat</italic></source><year>2015</year>; <volume>149</volume>:<fpage>229</fpage>–<lpage>236</lpage>.<pub-id pub-id-type="pmid">25488719</pub-id></mixed-citation></ref><ref id="R15"><label>15.</label><mixed-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Ugras</surname><given-names>S</given-names></name><name><surname>Stempel</surname><given-names>M</given-names></name><name><surname>Patil</surname><given-names>S</given-names></name><etal></etal></person-group><article-title>Estrogen receptor, progesterone receptor, and HER2 status predict lymphovascular invasion and lymph node involvement</article-title>. <source><italic>Ann Surg Oncol</italic></source><year>2014</year>; <volume>21</volume>:<fpage>3780</fpage>–<lpage>3786</lpage>.<pub-id pub-id-type="pmid">24952028</pub-id></mixed-citation></ref><ref id="R16"><label>16.</label><mixed-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Lee</surname><given-names>JH</given-names></name><name><surname>Kim</surname><given-names>SH</given-names></name><name><surname>Suh</surname><given-names>YJ</given-names></name><etal></etal></person-group><article-title>Predictors of axillary lymph node metastases (ALNM) in a Korean population with T1-2 breast carcinoma: triple negative breast cancer has a high incidence of ALNM irrespective of the tumor size</article-title>. <source><italic>Cancer Res Treat</italic></source><year>2010</year>; <volume>42</volume>:<fpage>30</fpage>–<lpage>36</lpage>.<pub-id pub-id-type="pmid">20369049</pub-id></mixed-citation></ref><ref id="R17"><label>17.</label><mixed-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Gangi</surname><given-names>A</given-names></name><name><surname>Mirocha</surname><given-names>J</given-names></name><name><surname>Leong</surname><given-names>T</given-names></name><etal></etal></person-group><article-title>Triple-negative breast cancer is not associated with increased likelihood of nodal metastases</article-title>. <source><italic>Ann Surg Oncol</italic></source><year>2014</year>; <volume>21</volume>:<fpage>4098</fpage>–<lpage>4103</lpage>.<pub-id pub-id-type="pmid">25155393</pub-id></mixed-citation></ref><ref id="R18"><label>18.</label><mixed-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Wiechmann</surname><given-names>L</given-names></name><name><surname>Sampson</surname><given-names>M</given-names></name><name><surname>Stempel</surname><given-names>M</given-names></name><etal></etal></person-group><article-title>Presenting features of breast cancer differ by molecular subtype</article-title>. <source><italic>Ann Surg Oncol</italic></source><year>2009</year>; <volume>16</volume>:<fpage>2705</fpage>–<lpage>2710</lpage>.<pub-id pub-id-type="pmid">19593632</pub-id></mixed-citation></ref><ref id="R19"><label>19.</label><mixed-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Li</surname><given-names>FY</given-names></name><name><surname>Wu</surname><given-names>SG</given-names></name><name><surname>Zhou</surname><given-names>J</given-names></name><etal></etal></person-group><article-title>Prognostic value of Ki-67 in breast cancer patients with positive axillary lymph nodes: a retrospective cohort study</article-title>. <source><italic>PLoS One</italic></source><year>2014</year>; <volume>9</volume>:<fpage>e87264</fpage>.<pub-id pub-id-type="pmid">24498305</pub-id></mixed-citation></ref><ref id="R20"><label>20.</label><mixed-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Wildiers</surname><given-names>H</given-names></name><name><surname>Van Calster</surname><given-names>B</given-names></name><name><surname>van de Poll-Franse</surname><given-names>LV</given-names></name><etal></etal></person-group><article-title>Relationship between age and axillary lymph node involvement in women with breast cancer</article-title>. <source><italic>J Clin Oncol</italic></source><year>2009</year>; <volume>27</volume>:<fpage>2931</fpage>–<lpage>2937</lpage>.<pub-id pub-id-type="pmid">19451448</pub-id></mixed-citation></ref><ref id="R21"><label>21.</label><mixed-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Fan</surname><given-names>L</given-names></name><name><surname>Strasser-Weippl</surname><given-names>K</given-names></name><name><surname>Li</surname><given-names>JJ</given-names></name><etal></etal></person-group><article-title>Breast cancer in China</article-title>. <source><italic>Lancet Oncol</italic></source><year>2014</year>; <volume>15</volume>:<fpage>e279</fpage>–<lpage>289</lpage>.<pub-id pub-id-type="pmid">24872111</pub-id></mixed-citation></ref><ref id="R22"><label>22.</label><mixed-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Mamounas</surname><given-names>EP</given-names></name></person-group><article-title>Age and lymph node status in breast cancer: not a straight forward relationship</article-title>. <source><italic>J Clin Oncol</italic></source><year>2009</year>; <volume>27</volume>:<fpage>2900</fpage>–<lpage>2901</lpage>.<pub-id pub-id-type="pmid">19451421</pub-id></mixed-citation></ref><ref id="R23"><label>23.</label><mixed-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Zhu</surname><given-names>X</given-names></name><name><surname>Ying</surname><given-names>J</given-names></name><name><surname>Wang</surname><given-names>F</given-names></name><etal></etal></person-group><article-title>Estrogen receptor, progesterone receptor, and human epidermal growth factor receptor 2 status in invasive breast cancer: a 3,198 cases study at National Cancer Center, China</article-title>. <source><italic>Breast Cancer Res Treat</italic></source><year>2014</year>; <volume>147</volume>:<fpage>551</fpage>–<lpage>555</lpage>.<pub-id pub-id-type="pmid">25234844</pub-id></mixed-citation></ref><ref id="R24"><label>24.</label><mixed-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Mattes</surname><given-names>MD</given-names></name><name><surname>Bhatia</surname><given-names>JK</given-names></name><name><surname>Metzger</surname><given-names>D</given-names></name><etal></etal></person-group><article-title>Breast cancer subtype as a predictor of lymph node metastasis according to the SEER registry</article-title>. <source><italic>J Breast Cancer</italic></source><year>2015</year>; <volume>18</volume>:<fpage>143</fpage>–<lpage>148</lpage>.<pub-id pub-id-type="pmid">26155290</pub-id></mixed-citation></ref><ref id="R25"><label>25.</label><mixed-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Schoppmann</surname><given-names>SF</given-names></name><name><surname>Bayer</surname><given-names>G</given-names></name><name><surname>Aumayr</surname><given-names>K</given-names></name><etal></etal></person-group><article-title>Prognostic value of lymphangiogenesis and lymphovascular invasion in invasive breast cancer</article-title>. <source><italic>Ann Surg</italic></source><year>2004</year>; <volume>240</volume>:<fpage>306</fpage>–<lpage>312</lpage>.<pub-id pub-id-type="pmid">15273556</pub-id></mixed-citation></ref><ref id="R26"><label>26.</label><mixed-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Moo</surname><given-names>TA</given-names></name><name><surname>McMillan</surname><given-names>R</given-names></name><name><surname>Lee</surname><given-names>M</given-names></name><etal></etal></person-group><article-title>Impact of molecular subtype on locoregional recurrence in mastectomy patients with T1–T2 breast cancer and 1-3 positive lymph nodes</article-title>. <source><italic>Ann Surg Oncol</italic></source><year>2014</year>; <volume>21</volume>:<fpage>1569</fpage>–<lpage>1574</lpage>.<pub-id pub-id-type="pmid">24488216</pub-id></mixed-citation></ref><ref id="R27"><label>27.</label><mixed-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Nofech-Mozes</surname><given-names>S</given-names></name><name><surname>Ackerman</surname><given-names>I</given-names></name><name><surname>Ghorab</surname><given-names>Z</given-names></name><etal></etal></person-group><article-title>Lymphovascular invasion is a significant predictor for distant recurrence in patients with early-stage endometrial endometrioid adenocarcinoma</article-title>. <source><italic>Am J Clin Pathol</italic></source><year>2008</year>; <volume>129</volume>:<fpage>912</fpage>–<lpage>917</lpage>.<pub-id pub-id-type="pmid">18480008</pub-id></mixed-citation></ref><ref id="R28"><label>28.</label><mixed-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Foulkes</surname><given-names>WD</given-names></name><name><surname>Smith</surname><given-names>IE</given-names></name><name><surname>Reis-Filho</surname><given-names>JS</given-names></name></person-group><article-title>Triple-negative breast cancer</article-title>. <source><italic>N Engl J Med</italic></source><year>2010</year>; <volume>363</volume>:<fpage>1938</fpage>–<lpage>1948</lpage>.<pub-id pub-id-type="pmid">21067385</pub-id></mixed-citation></ref><ref id="R29"><label>29.</label><mixed-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Sackey</surname><given-names>H</given-names></name><name><surname>Magnuson</surname><given-names>A</given-names></name><name><surname>Sandelin</surname><given-names>K</given-names></name><etal></etal></person-group><article-title>Arm lymphoedema after axillary surgery in women with invasive breast cancer</article-title>. <source><italic>Br J Surg</italic></source><year>2014</year>; <volume>101</volume>:<fpage>390</fpage>–<lpage>397</lpage>.<pub-id pub-id-type="pmid">24536010</pub-id></mixed-citation></ref><ref id="R30"><label>30.</label><mixed-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Zhou</surname><given-names>W</given-names></name><name><surname>He</surname><given-names>Z</given-names></name><name><surname>Xue</surname><given-names>J</given-names></name><etal></etal></person-group><article-title>Molecular subtype classification is a determinant of non-sentinel lymph node metastasis in breast cancer patients with positive sentinel lymph nodes</article-title>. <source><italic>PLoS One</italic></source><year>2012</year>; <volume>7</volume>:<fpage>e35881</fpage>.<pub-id pub-id-type="pmid">22563412</pub-id></mixed-citation></ref><ref id="R31"><label>31.</label><mixed-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Freedman</surname><given-names>GM</given-names></name><name><surname>Fowble</surname><given-names>BL</given-names></name><name><surname>Li</surname><given-names>T</given-names></name><etal></etal></person-group><article-title>Risk of positive nonsentinel nodes in women with 1-2 positive sentinel nodes related to age and molecular subtype approximated by receptor status</article-title>. <source><italic>Breast J</italic></source><year>2014</year>; <volume>20</volume>:<fpage>358</fpage>–<lpage>363</lpage>.<pub-id pub-id-type="pmid">24861613</pub-id></mixed-citation></ref><ref id="R32"><label>32.</label><mixed-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Goldhirsch</surname><given-names>A</given-names></name><name><surname>Winer</surname><given-names>EP</given-names></name><name><surname>Coates</surname><given-names>AS</given-names></name><etal></etal></person-group><article-title>Personalizing the treatment of women with early breast cancer: highlights of the St Gallen International Expert Consensus on the Primary Therapy of Early Breast Cancer 2013</article-title>. <source><italic>Ann Oncol</italic></source><year>2013</year>; <volume>24</volume>:<fpage>2206</fpage>–<lpage>2223</lpage>.<pub-id pub-id-type="pmid">23917950</pub-id></mixed-citation></ref><ref id="R33"><label>33.</label><mixed-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Mojarad</surname><given-names>S</given-names></name><name><surname>Venturini</surname><given-names>B</given-names></name><name><surname>Fulgenzi</surname><given-names>P</given-names></name><etal></etal></person-group><article-title>Prediction of nodal metastasis and prognosis of breast cancer by ANN-based assessment of tumour size and p53, Ki-67 and steroid receptor expression</article-title>. <source><italic>Anticancer Res</italic></source><year>2013</year>; <volume>33</volume>:<fpage>3925</fpage>–<lpage>3933</lpage>.<pub-id pub-id-type="pmid">24023330</pub-id></mixed-citation></ref><ref id="R34"><label>34.</label><mixed-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Terasaki-Fukuzawa</surname><given-names>Y</given-names></name><name><surname>Kijima</surname><given-names>H</given-names></name><name><surname>Suto</surname><given-names>A</given-names></name><etal></etal></person-group><article-title>Decreased nm23 expression, but not Ki-67 labeling index, is significantly correlated with lymph node metastasis of breast invasive ductal carcinoma</article-title>. <source><italic>Int J Mol Med</italic></source><year>2002</year>; <volume>9</volume>:<fpage>25</fpage>–<lpage>29</lpage>.<pub-id pub-id-type="pmid">11744991</pub-id></mixed-citation></ref><ref id="R35"><label>35.</label><mixed-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Dabritz</surname><given-names>G</given-names></name><name><surname>Miswan</surname><given-names>A</given-names></name><name><surname>Rowe</surname><given-names>N</given-names></name><etal></etal></person-group><article-title>KI-67 expression and axillary lymph node metastases (ALN) in invasive breast cancer”</article-title>. <source><italic>International Journal of Surgery</italic></source><year>2011</year>; <volume>9</volume>:<fpage>559</fpage>–<lpage>560</lpage>.</mixed-citation></ref></ref-list></back></pmc></record>Pour manipuler ce document sous Unix (Dilib)
EXPLOR_STEP=$WICRI_ROOT/Wicri/Sante/explor/LymphedemaV1/Data/Pmc/Corpus
HfdSelect -h $EXPLOR_STEP/biblio.hfd -nk 000378 | SxmlIndent | more
Ou
HfdSelect -h $EXPLOR_AREA/Data/Pmc/Corpus/biblio.hfd -nk 000378 | SxmlIndent | more
Pour mettre un lien sur cette page dans le réseau Wicri
{{Explor lien
|wiki= Wicri/Sante
|area= LymphedemaV1
|flux= Pmc
|étape= Corpus
|type= RBID
|clé= PMC:4674213
|texte= Breast Cancer Subtype is Associated With Axillary Lymph Node Metastasis
}}
Pour générer des pages wiki
HfdIndexSelect -h $EXPLOR_AREA/Data/Pmc/Corpus/RBID.i -Sk "pubmed:26632910" \
| HfdSelect -Kh $EXPLOR_AREA/Data/Pmc/Corpus/biblio.hfd \
| NlmPubMed2Wicri -a LymphedemaV1
| This area was generated with Dilib version V0.6.31. |  |