{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,12,11]],"date-time":"2025-12-11T03:04:12Z","timestamp":1765422252518,"version":"build-2065373602"},"reference-count":46,"publisher":"MDPI AG","issue":"16","license":[{"start":{"date-parts":[[2021,8,14]],"date-time":"2021-08-14T00:00:00Z","timestamp":1628899200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Cancers"],"abstract":"<jats:p>Sentinel lymph node (SLN) biopsy (SLNB) usually need not be simultaneously performed with breast-conserving surgery (BCS) for patients diagnosed with ductal carcinoma in situ (DCIS) by preoperative core needle biopsy (CNB), but must be performed once there is invasive carcinoma (IC) found postoperatively. This study aimed to investigate the factors contributing to SLN metastasis in underestimated IC patients with an initial diagnosis of DCIS by CNB. We retrospectively reviewed 1240 consecutive cases of DCIS by image-guided CNB from January 2010 to December 2017 and identified 316 underestimated IC cases with SLNB. Data on clinical characteristics, radiologic features, and final pathological findings were examined. Twenty-three patients (7.3%) had SLN metastasis. Multivariate analysis indicated that an IC tumor size &gt; 0.5 cm (odds ratio: 3.11, p = 0.033) and the presence of lymphovascular invasion (odds ratio: 32.85, p &lt; 0.0001) were independent risk predictors of SLN metastasis. In the absence of any predictors, the incidence of positive SLNs was very low (2.6%) in the total population and extremely low (1.3%) in the BCS subgroup. Therefore, omitting SLNB may be an acceptable option for patients who initially underwent BCS without risk predictors on final pathological assessment. Further prospective studies are necessary before clinical application.<\/jats:p>","DOI":"10.3390\/cancers13164099","type":"journal-article","created":{"date-parts":[[2021,8,15]],"date-time":"2021-08-15T21:43:55Z","timestamp":1629063835000},"page":"4099","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":8,"title":["Predictors of Sentinel Lymph Node Metastasis in Postoperatively Upgraded Invasive Breast Carcinoma Patients"],"prefix":"10.3390","volume":"13","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-2565-4305","authenticated-orcid":false,"given":"Chi-Chang","family":"Yu","sequence":"first","affiliation":[{"name":"Department of General Surgery, Chang Gung Memorial Hospital at Linkou, Chang Gung University, Taoyuan 333, Taiwan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6870-3429","authenticated-orcid":false,"given":"Yun-Chung","family":"Cheung","sequence":"additional","affiliation":[{"name":"Department of Diagnostic Radiology, Chang Gung Memorial Hospital at Linkou, Chang Gung University, Taoyuan 333, Taiwan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Chuen","family":"Hsueh","sequence":"additional","affiliation":[{"name":"Department of Pathology, Chang Gung Memorial Hospital at Linkou, Chang Gung University, Taoyuan 333, Taiwan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0177-0045","authenticated-orcid":false,"given":"Shin-Cheh","family":"Chen","sequence":"additional","affiliation":[{"name":"Department of General Surgery, Chang Gung Memorial Hospital at Linkou, Chang Gung University, Taoyuan 333, Taiwan"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2021,8,14]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"127","DOI":"10.1016\/j.amjsurg.2010.09.005","article-title":"Utilization of minimally invasive breast biopsy for the evaluation of suspicious breast lesions","volume":"202","author":"Gutwein","year":"2011","journal-title":"Am. J. Surg."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"462","DOI":"10.5858\/arpa.2012-0078-RA","article-title":"Ductal carcinoma in situ of the breast: Current concepts and future directions","volume":"137","author":"Siziopikou","year":"2013","journal-title":"Arch. Pathol. Lab. Med."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"119","DOI":"10.1148\/radiol.11102368","article-title":"Ductal carcinoma in situ at core-needle biopsy: Meta-analysis of underestimation and predictors of invasive breast cancer","volume":"260","author":"Brennan","year":"2011","journal-title":"Radiology"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"561","DOI":"10.1200\/JCO.2016.71.0947","article-title":"Sentinel Lymph Node Biopsy for Patients With Early-Stage Breast Cancer: American Society of Clinical Oncology Clinical Practice Guideline Update","volume":"35","author":"Lyman","year":"2017","journal-title":"J. Clin. Oncol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"546","DOI":"10.1056\/NEJMoa012782","article-title":"A randomized comparison of sentinel-node biopsy with routine axillary dissection in breast cancer","volume":"349","author":"Veronesi","year":"2003","journal-title":"N. Engl. J. Med."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"1996","DOI":"10.1245\/s10434-008-9909-y","article-title":"Long-term morbidity of sentinel node biopsy versus complete axillary dissection for unilateral breast cancer","volume":"15","author":"Wascher","year":"2008","journal-title":"Ann. Surg. Oncol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"223","DOI":"10.1111\/j.1524-4741.2011.01069.x","article-title":"Predictors of invasion and axillary lymph node metastasis in patients with a core biopsy diagnosis of ductal carcinoma in situ: An analysis of 255 cases","volume":"17","author":"Han","year":"2011","journal-title":"Breast J."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"197","DOI":"10.1016\/j.breast.2015.01.004","article-title":"Sentinel lymph node biopsy is not warranted following a core needle biopsy diagnosis of ductal carcinoma in situ (DCIS) of the breast","volume":"24","author":"Prendeville","year":"2015","journal-title":"Breast"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"4270","DOI":"10.1245\/s10434-015-4547-7","article-title":"Is Sentinel Lymph Node Dissection Warranted for Patients with a Diagnosis of Ductal Carcinoma In Situ?","volume":"22","author":"Francis","year":"2015","journal-title":"Ann. Surg. Oncol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"517","DOI":"10.1007\/s10549-016-3783-2","article-title":"Sentinel lymph node biopsy can be omitted in DCIS patients treated with breast conserving therapy","volume":"156","author":"Goorts","year":"2016","journal-title":"Breast Cancer Res. Treat."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"e87","DOI":"10.1016\/j.clbc.2016.10.002","article-title":"Sentinel Node Procedure Obsolete in Lumpectomy for Ductal Carcinoma In Situ","volume":"17","author":"Heymans","year":"2017","journal-title":"Clin. Breast Cancer"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"325","DOI":"10.1111\/tbj.12928","article-title":"Sentinel node biopsy in ductal carcinoma in situ of the breast: Never justified?","volume":"24","author":"Sorrentino","year":"2018","journal-title":"Breast J."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"663","DOI":"10.1007\/s12282-018-0871-7","article-title":"Upstaging to invasive ductal carcinoma after mastectomy for ductal carcinoma in situ: Predictive factors and role of sentinel lymph node biopsy","volume":"25","author":"Watanabe","year":"2018","journal-title":"Breast Cancer."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"590686","DOI":"10.3389\/fonc.2020.590686","article-title":"Prediction of Sentinel Lymph Node Metastasis in Breast Ductal Carcinoma In Situ Diagnosed by Preoperative Core Needle Biopsy","volume":"10","author":"Zhang","year":"2020","journal-title":"Front. Oncol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"426","DOI":"10.1097\/SLA.0b013e3181f08f32","article-title":"Locoregional recurrence after sentinel lymph node dissection with or without axillary dissection in patients with sentinel lymph node metastases: The American College of Surgeons Oncology Group Z0011 randomized trial","volume":"252","author":"Giuliano","year":"2010","journal-title":"Ann. Surg."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"297","DOI":"10.1016\/S1470-2045(13)70035-4","article-title":"Axillary dissection versus no axillary dissection in patients with sentinel-node micrometastases (IBCSG 23-01): A phase 3 randomised controlled trial","volume":"14","author":"Galimberti","year":"2013","journal-title":"Lancet Oncol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"678","DOI":"10.1016\/j.breast.2012.06.013","article-title":"Abandoning sentinel lymph node biopsy in early breast cancer? A new trial in progress at the European Institute of Oncology of Milan (SOUND: Sentinel node vs Observation after axillary UltraSouND)","volume":"21","author":"Gentilini","year":"2012","journal-title":"Breast"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"87","DOI":"10.1159\/000360411","article-title":"Local treatment of the axilla in early breast cancer: Concepts from the national surgical adjuvant breast and bowel project B-04 to the planned intergroup sentinel mamma trial","volume":"9","author":"Reimer","year":"2014","journal-title":"Breast Care"},{"key":"ref_19","doi-asserted-by":"crossref","unstructured":"Van Roozendaal, L.M., Vane, M.L.G., van Dalen, T., van der Hage, J.A., Strobbe, L.J.A., Boersma, L.J., Linn, S.C., Lobbes, M.B.I., Poortmans, P.M.P., and Tjan-Heijnen, V.C.G. (2017). Clinically node negative breast cancer patients undergoing breast conserving therapy, sentinel lymph node procedure versus follow-up: A Dutch randomized controlled multicentre trial (BOOG 2013-08). BMC Cancer, 17.","DOI":"10.1186\/s12885-017-3443-x"},{"key":"ref_20","unstructured":"American College of Radiology (2013). Breast Imaging Reporting and Data System, American College of Radiology. [5th ed.]."},{"key":"ref_21","unstructured":"Hoda, S.A., Brogi, E., Koerner, F.C., and Rosen, P.P. (2021). Rosen\u2019s Breast Pathology, Wolters Kluwer. [5th ed.]."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"1154","DOI":"10.1016\/S0140-6736(95)90982-6","article-title":"Prognostic classification of breast ductal carcinoma-in-situ","volume":"345","author":"Silverstein","year":"1995","journal-title":"Lancet"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"134","DOI":"10.1093\/jncimonographs\/lgq035","article-title":"Ductal carcinoma in situ: Terminology, classification, and natural history","volume":"41","author":"Allred","year":"2010","journal-title":"J. Natl. Cancer Inst. Monogr."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"1257","DOI":"10.1038\/s41379-019-0262-4","article-title":"Variability in diagnostic threshold for comedo necrosis among breast pathologists: Implications for patient eligibility for active surveillance trials of ductal carcinoma in situ","volume":"32","author":"Harrison","year":"2019","journal-title":"Mod. Pathol."},{"key":"ref_25","first-page":"aqaa276","article-title":"Significance of Removing Comedonecrosis as an Exclusion Criterion in Mammary Low-Risk Ductal Carcinoma In Situ Managed in an Active Surveillance Clinical Trial","volume":"26","author":"Zhan","year":"2021","journal-title":"Am. J. Clin. Pathol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"403","DOI":"10.1111\/j.1365-2559.1991.tb00229.x","article-title":"Pathological prognostic factors in breast cancer. I. The value of histological grade in breast cancer: Experience from a large study with long-term follow-up","volume":"19","author":"Elston","year":"1991","journal-title":"Histopathology"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"e48","DOI":"10.5858\/134.7.e48","article-title":"American Society of Clinical Oncology\/College of American Pathologists guideline recommendations for immunohistochemical testing of estrogen and progesterone receptors in breast cancer (unabridged version)","volume":"134","author":"Hammond","year":"2010","journal-title":"Arch. Pathol. Lab. Med."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"e026797","DOI":"10.1136\/bmjopen-2018-026797","article-title":"The COMET (Comparison of Operative versus Monitoring and Endocrine Therapy) trial: A phase III randomised controlled clinical trial for low-risk ductal carcinoma in situ (DCIS)","volume":"12","author":"Hwang","year":"2019","journal-title":"BMJ Open"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"29","DOI":"10.1001\/archsurg.1989.01410010035007","article-title":"Nonpalpable in situ ductal carcinoma of the breast. Predictors of multicentricity and microinvasion and implications for treatment","volume":"124","author":"Schwartz","year":"1989","journal-title":"Arch. Surg."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"102","DOI":"10.1002\/1097-0142(19900701)66:1<102::AID-CNCR2820660119>3.0.CO;2-5","article-title":"Intraductal carcinoma of the breast (208 cases). Clinical factors influencing treatment choice","volume":"66","author":"Silverstein","year":"1990","journal-title":"Cancer"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"170","DOI":"10.1093\/jnci\/djp482","article-title":"Ductal carcinoma in situ of the breast: A systematic review of incidence, treatment, and outcomes","volume":"102","author":"Virnig","year":"2010","journal-title":"J. Natl. Cancer Inst."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"616","DOI":"10.1002\/(SICI)1097-0142(19990201)85:3<616::AID-CNCR12>3.0.CO;2-7","article-title":"Predictors of local recurrence after treatment of ductal carcinoma in situ: A meta-analysis","volume":"85","author":"Boyages","year":"1999","journal-title":"Cancer"},{"key":"ref_33","first-page":"185","article-title":"Incidence and predictors of axillary metastasis in T1 carcinoma of the breast","volume":"183","author":"Giuliano","year":"1996","journal-title":"J. Am. Coll. Surg."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"1918","DOI":"10.1002\/(SICI)1097-0142(19970515)79:10<1918::AID-CNCR12>3.0.CO;2-Y","article-title":"Predictors of axillary lymph node metastases in patients with T1 breast carcinoma","volume":"79","author":"Barth","year":"1997","journal-title":"Cancer"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"1011","DOI":"10.1177\/000313480006601104","article-title":"Factors affecting axillary lymph node metastases in patients with T1 breast carcinoma","volume":"66","author":"Markopoulos","year":"2000","journal-title":"Am. Surg."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"229","DOI":"10.1016\/j.pathophys.2009.11.003","article-title":"Lymphangiogenesis and lymphatic metastasis in breast cancer","volume":"17","author":"Ran","year":"2010","journal-title":"Pathophysiology"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"2747","DOI":"10.1002\/ijc.24702","article-title":"Tumor metastasis and the lymphatic vasculature","volume":"125","author":"Sleeman","year":"2009","journal-title":"Int. J. Cancer"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"46","DOI":"10.1016\/j.mvr.2014.07.004","article-title":"Role of lymphatic vasculature in regional and distant metastases","volume":"95","author":"Podgrabinska","year":"2014","journal-title":"Microvasc. Res."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"1772","DOI":"10.1002\/1097-0142(19951115)76:10<1772::AID-CNCR2820761014>3.0.CO;2-O","article-title":"The prognostic value of lymphatic and blood vessel invasion in operable breast cancer","volume":"76","author":"Lauria","year":"1995","journal-title":"Cancer"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"11","DOI":"10.1023\/A:1020231300974","article-title":"T1 breast cancer: Identification of patients at low risk of axillary lymph node metastases","volume":"76","author":"Bader","year":"2002","journal-title":"Breast Cancer Res. Treat."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1007\/s10549-005-9007-9","article-title":"Factors predicting the sentinel and non-sentinel lymph node metastases in breast cancer","volume":"95","author":"Ozmen","year":"2006","journal-title":"Breast Cancer Res. Treat."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"692","DOI":"10.1097\/00000658-199911000-00012","article-title":"Lymphatic invasion, tumor size, and age are independent predictors of axillary lymph node metastases in women with T1 breast cancers","volume":"230","author":"Gajdos","year":"1999","journal-title":"Ann. Surg."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"1391","DOI":"10.1038\/sj.bjc.6605655","article-title":"Presence of an in situ component is associated with reduced biological aggressiveness of size-matched invasive breast cancer","volume":"102","author":"Wong","year":"2010","journal-title":"Br. J. Cancer."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"346","DOI":"10.1016\/j.breast.2014.01.015","article-title":"Accompanying DCIS in breast cancer patients with invasive ductal carcinoma is predictive of improved local recurrence-free survival","volume":"23","author":"Dieterich","year":"2014","journal-title":"Breast"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"1877","DOI":"10.1007\/s00432-019-02930-2","article-title":"Invasive ductal carcinoma with coexisting ductal carcinoma in situ (IDC\/DCIS) versus pure invasive ductal carcinoma (IDC): A comparison of clinicopathological characteristics, molecular subtypes, and clinical outcomes","volume":"145","author":"Goh","year":"2019","journal-title":"J. Cancer Res. Clin. Oncol."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"3416","DOI":"10.1245\/s10434-012-2376-5","article-title":"Axillary node staging for microinvasive breast cancer: Is it justified?","volume":"19","author":"Lyons","year":"2012","journal-title":"Ann. Surg. Oncol."}],"container-title":["Cancers"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2072-6694\/13\/16\/4099\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T06:46:13Z","timestamp":1760165173000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2072-6694\/13\/16\/4099"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,8,14]]},"references-count":46,"journal-issue":{"issue":"16","published-online":{"date-parts":[[2021,8]]}},"alternative-id":["cancers13164099"],"URL":"https:\/\/doi.org\/10.3390\/cancers13164099","relation":{},"ISSN":["2072-6694"],"issn-type":[{"type":"electronic","value":"2072-6694"}],"subject":[],"published":{"date-parts":[[2021,8,14]]}}}