Cancer Research and Treatment

Original Articles

Comparison of Long-term Oncological Outcome of Sentinel Lymph Node Mapping Methods (Dye-Only versus Dye and Radioisotope) in Breast Cancer Patients Following Neoadjuvant Chemotherapy: Jinyoung Byeon, Changjin Lim, Eunhye Kang, Ji-Jung Jung, Hong-Kyu Kim, Han-Byoel Lee, Hyeong-Gon Moon, Wonshik Han; Received December 30, 2024 Accepted April 13, 2025 Published online April 15, 2025; DOI: https://doi.org/10.4143/crt.2024.1253 [Accepted]

Abstract PDF: Purpose
Sentinel lymph node biopsy (SLNB) using dye and isotope (DUAL) is recommended over the dye-only (DYE) method after neoadjuvant chemotherapy (NCT) due to potentially lower false-negative rates. However, the long-term outcome of either method is unclear. We aimed to compare the long-term oncological outcomes of DYE versus DUAL SLNB methods in patients who received NCT.
Materials and Methods
In this retrospective cohort study, 893 patients who underwent SLNB following NCT and had pathologically negative lymph nodes were included. After propensity score matching for cT, cN, and pT stages, 280 patients were in the DYE group and 560 in the DUAL group. Indigo carmine was used for dye and Tc-99m antimony trisulfate for isotope mapping.
Results
Median follow-up was 75.6 months in the DYE group and 83.0 months in the DUAL group. Mean (±SD) number of harvested sentinel nodes was 6.7 (±3.4) and 6.7 (±3.8) in the DYE and DUAL groups (p=0.51). Five-year distant metastasis-free survival was 95.2% in DYE group and 93.3% in DUAL group (HR=1.45; 95% CI, 0.82–2.57; p=0.19). Disease-free survival (HR=0.97; 95% CI, 0.69–1.50; p=0.91) and overall survival (HR=0.98; 95% CI, 0.56–1.69; p=0.95) were not significantly different. Axillary recurrence rate was 1.8% and 2.5% in DYE and DUAL groups(p=0.64).
Conclusion
Long-term oncological outcomes did not significantly differ between DYE and DUAL SLNB methods. The dye-only method can be safely recommended for breast cancer patients who received NCT.

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Breast cancer

Retrospective Cohort Study on the Long-term Oncologic Outcomes of Sentinel Lymph Node Mapping Methods (Dye-Only versus Dye and Radioisotope Mapping) in Early Breast Cancer: A Propensity Score-Matched Analysis: Changjin Lim, Eunhye Kang, Ji Gwang Jung, Jong-Ho Cheun, Hong-Kyu Kim, Han-Byoel Lee, Hyeong-Gon Moon, Wonshik Han; Cancer Res Treat. 2023;55(2):562-569. Published online September 26, 2022; DOI: https://doi.org/10.4143/crt.2022.871

Abstract PDF PubReader ePub: Purpose
In sentinel lymph node (SLN) biopsy (SLNB) during breast cancer surgery, SLN mapping using dye and isotope (DUAL) may have lower false-negative rates than the dye-only (DYE) method. However, the long-term outcomes of either method are unclear. We aimed to compare long-term oncological outcomes of DYE and DUAL for SLNB in early breast cancer.
Materials and Methods
This retrospective single-institution cohort study included 5,795 patients (DYE, 2,323; DUAL, 3,472) with clinically node-negative breast cancer who underwent SLNB and no neoadjuvant therapy. Indigo carmine was used for the dye method and Tc99m-antimony trisulfate for the isotope. To compare long-term outcomes, pathologic N0 patients were selected from both groups, and propensity score matching (PSM), considering age, pT category, breast surgery, and adjuvant treatment, was performed (1,441 patients in each group).
Results
The median follow-up duration was 8.7 years. The median number of harvested sentinel nodes was 3.21 and 3.12 in the DYE and DUAL groups, respectively (p=0.112). The lymph node–positive rate was not significantly different between the two groups in subgroups of similar tumor sizes (p > 0.05). Multivariate logistic regression revealed that the mapping method was not significantly associated with the lymph node–positive rate (p=0.758). After PSM, the 5-year axillary recurrence rate (DYE 0.8% vs. DUAL 0.6%, p=0.096), and 5-year disease-free survival (DYE 93.9% vs. DUAL 93.7%, p=0.402) were similar between the two groups.
Conclusion
Dye alone for SLNB was not inferior to dual mapping regarding long-term oncological outcomes in early breast cancer.

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Diagnostic Assessment of Deep Learning Algorithms for Frozen Tissue Section Analysis in Women with Breast Cancer: Young-Gon Kim, In Hye Song, Seung Yeon Cho, Sungchul Kim, Milim Kim, Soomin Ahn, Hyunna Lee, Dong Hyun Yang, Namkug Kim, Sungwan Kim, Taewoo Kim, Daeyoung Kim, Jonghyeon Choi, Ki-Sun Lee, Minuk Ma, Minki Jo, So Yeon Park, Gyungyub Gong; Cancer Res Treat. 2023;55(2):513-522. Published online September 6, 2022; DOI: https://doi.org/10.4143/crt.2022.055

Abstract PDF Supplementary Material PubReader ePub

Purpose
Assessing the metastasis status of the sentinel lymph nodes (SLNs) for hematoxylin and eosin–stained frozen tissue sections by pathologists is an essential but tedious and time-consuming task that contributes to accurate breast cancer staging. This study aimed to review a challenge competition (HeLP 2019) for the development of automated solutions for classifying the metastasis status of breast cancer patients.
Materials and Methods
A total of 524 digital slides were obtained from frozen SLN sections: 297 (56.7%) from Asan Medical Center (AMC) and 227 (43.4%) from Seoul National University Bundang Hospital (SNUBH), South Korea. The slides were divided into training, development, and validation sets, where the development set comprised slides from both institutions and training and validation set included slides from only AMC and SNUBH, respectively. The algorithms were assessed for area under the receiver operating characteristic curve (AUC) and measurement of the longest metastatic tumor diameter. The final total scores were calculated as the mean of the two metrics, and the three teams with AUC values greater than 0.500 were selected for review and analysis in this study.
Results
The top three teams showed AUC values of 0.891, 0.809, and 0.736 and major axis prediction scores of 0.525, 0.459, and 0.387 for the validation set. The major factor that lowered the diagnostic accuracy was micro-metastasis.
Conclusion
In this challenge competition, accurate deep learning algorithms were developed that can be helpful for making a diagnosis on intraoperative SLN biopsy. The clinical utility of this approach was evaluated by including an external validation set from SNUBH.

Citations

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Detection of metastatic breast carcinoma in sentinel lymph node frozen sections using an artificial intelligence-assisted system
Chia-Ping Chang, Chih-Yi Hsu, Hsiang Sheng Wang, Peng-Chuna Feng, Wen-Yih Liang
Pathology - Research and Practice.2025; 267: 155836. CrossRef
Value of frozen section to tailor surgical staging in apparent early-stage epithelial ovarian cancer
Stefano Di Berardino, Nicolò Bizzarri, Marianna Ciancia, Francesca Moro, Belen Padial Urtueta, Claudia Marchetti, Gian Franco Zannoni, Giovanni Scambia, Anna Fagotti
International Journal of Gynecological Cancer.2025; : 101746. CrossRef
Comparing the diagnostic efficacy of optical coherence tomography and frozen section for margin assessment in breast-conserving surgery: a meta-analysis
Shishun Fan, Huirui Zhang, Zhenyu Meng, Ang Li, Yuqing Luo, Yueping Liu
Journal of Clinical Pathology.2024; 77(8): 517. CrossRef
Intraoperative Margin Assessment in Breast Conservation Surgery: A Necessity or a Luxury?
Srijan Shukla, Nisha Hariharan
Annals of Surgical Oncology.2023; 30(9): 5314. CrossRef

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Challenge for Diagnostic Assessment of Deep Learning Algorithm for Metastases Classification in Sentinel Lymph Nodes on Frozen Tissue Section Digital Slides in Women with Breast Cancer: Young-Gon Kim, In Hye Song, Hyunna Lee, Sungchul Kim, Dong Hyun Yang, Namkug Kim, Dongho Shin, Yeonsoo Yoo, Kyowoon Lee, Dahye Kim, Hwejin Jung, Hyunbin Cho, Hyungyu Lee, Taeu Kim, Jong Hyun Choi, Changwon Seo, Seong il Han, Young Je Lee, Young Seo Lee, Hyung-Ryun Yoo, Yongju Lee, Jeong Hwan Park, Sohee Oh, Gyungyub Gong; Cancer Res Treat. 2020;52(4):1103-1111. Published online June 30, 2020; DOI: https://doi.org/10.4143/crt.2020.337

Abstract PDF PubReader ePub

Purpose
Assessing the status of metastasis in sentinel lymph nodes (SLNs) by pathologists is an essential task for the accurate staging of breast cancer. However, histopathological evaluation of sentinel lymph nodes by a pathologist is not easy and is a tedious and time-consuming task. The purpose of this study is to review a challenge competition (HeLP 2018) to develop automated solutions for the classification of metastases in hematoxylin and eosin–stained frozen tissue sections of SLNs in breast cancer patients.
Materials and Methods
A total of 297 digital slides were obtained from frozen SLN sections, which include post–neoadjuvant cases (n = 144, 48.5%) in Asan Medical Center, South Korea. The slides were divided into training, development, and validation sets. All of the imaging datasets have been manually segmented by expert pathologists. A total of 10 participants were allowed to use the Kakao challenge platform for six weeks with two P40 GPUs. The algorithms were assessed in terms of the AUC (area under receiver operating characteristic curve).
Results
The top three teams showed 0.986, 0.985, and 0.945 AUCs for the development set and 0.805, 0.776, and 0.765 AUCs for the validation set. Micrometastatic tumors, neoadjuvant systemic therapy, invasive lobular carcinoma, and histologic grade 3 were associated with lower diagnostic accuracy.
Conclusion
In a challenge competition, accurate deep learning algorithms have been developed, which can be helpful in making frozen diagnosis of intraoperative sentinel lymph node biopsy. Whether this approach has clinical utility will require evaluation in a clinical setting

Citations

Citations to this article as recorded by

Detection of metastatic breast carcinoma in sentinel lymph node frozen sections using an artificial intelligence-assisted system
Chia-Ping Chang, Chih-Yi Hsu, Hsiang Sheng Wang, Peng-Chuna Feng, Wen-Yih Liang
Pathology - Research and Practice.2025; 267: 155836. CrossRef
Diagnostic Assessment of Deep Learning Algorithms for Frozen Tissue Section Analysis in Women with Breast Cancer
Young-Gon Kim, In Hye Song, Seung Yeon Cho, Sungchul Kim, Milim Kim, Soomin Ahn, Hyunna Lee, Dong Hyun Yang, Namkug Kim, Sungwan Kim, Taewoo Kim, Daeyoung Kim, Jonghyeon Choi, Ki-Sun Lee, Minuk Ma, Minki Jo, So Yeon Park, Gyungyub Gong
Cancer Research and Treatment.2023; 55(2): 513. CrossRef
Artificial intelligence and frozen section histopathology: A systematic review
Benjamin G. Gorman, Mark A. Lifson, Nahid Y. Vidal
Journal of Cutaneous Pathology.2023; 50(9): 852. CrossRef
Effectiveness of transfer learning for enhancing tumor classification with a convolutional neural network on frozen sections
Young-Gon Kim, Sungchul Kim, Cristina Eunbee Cho, In Hye Song, Hee Jin Lee, Soomin Ahn, So Yeon Park, Gyungyub Gong, Namkug Kim
Scientific Reports.2020;[Epub] CrossRef

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Axillary Lymph Node Dissection Does Not Improve Post-mastectomy Overall or Disease-Free Survival among Breast Cancer Patients with 1-3 Positive Nodes: Ji Hyeon Joo, Su Ssan Kim, Byung Ho Son, Seung Do Ahn, Jin Hong Jung, Eun Kyung Choi, Sei Hyun Ahn, Jong Won Lee, Hee Jeong Kim, Beom Seok Ko; Cancer Res Treat. 2019;51(3):1011-1021. Published online October 16, 2018; DOI: https://doi.org/10.4143/crt.2018.438

Abstract PDF Supplementary Material PubReader ePub

Purpose
Axillary lymph node dissection (ALND) may be avoidable for breast cancer patients with 1-2 positive lymph nodes (LN) after breast-conserving therapy. However, the effects of ALND after mastectomy remain unclear because radiation is not routinely used. Herein, we compared the benefits of post-mastectomy ALND versus sentinel node biopsy (SNB) alone for breast cancer patients with 1-3 metastatic LNs.
Materials and Methods
A total of 1,697 patients with pN1 disease who underwent mastectomy during 2000-2015 were identified from an institutional database. Outcomes were compared using the inverse probability of treatment weighted method.
Results
Patients who underwent SNB tended to have smaller tumors, a lower histology grade, a lower number of positive LNs, and better immunohistochemical findings. After correcting all confounding factors regarding patient, tumor, and adjuvant treatment, the SNB and ALND groups did not differ in terms of overall survival (OS) and disease-free survival (DFS), distant metastasis and locoregional recurrence. The 10-year DFS and OS rates were 83% and 84%, respectively, during a median follow-up period of 93 months.
Conclusion
ALND did not improve post-mastectomy survival outcomes among patients with N1 breast cancer, even after adjusting for all histopathologic and treatment-related factors.

Citations

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Lymphangiogenesis in Breast Cancer: From Molecular Mechanisms to Clinical Implications
Brusi Kola, Sooraj Kakkat, Prabhat Suman, Emily Crouch, Debanjan Chakroborty, Chandrani Sarkar
The FASEB Journal.2025;[Epub] CrossRef
The Impact of Sentinel Lymph Node Biopsy on Female Patients With T3-4c Breast Cancer and 1-2 Positive Lymph Nodes: A Population-Based Cohort Study
Hanzhao Yang, Yadong Sun, Peili Wang, Jianghua Qiao, Chengzheng Wang, Zhenzhen Liu
Clinical Breast Cancer.2024; 24(3): e126. CrossRef
Axillary management in patients with clinical node-negative early breast cancer and positive sentinel lymph node: a systematic review and meta-analysis
Changzai Li, Pan Zhang, Jie Lv, Wei Dong, Baoshan Hu, Jinji Zhang, Hongcheng Zhu
Frontiers in Oncology.2024;[Epub] CrossRef
Reevaluating Axillary Lymph Node Dissection in Total Mastectomy for Low Axillary Burden Breast Cancer: Insights from a Meta-Analysis including the SINODAR-ONE Trial
Munaser Alamoodi, Neill Patani, Kinan Mokbel, Umar Wazir, Kefah Mokbel
Cancers.2024; 16(4): 742. CrossRef
RecurIndex-Guided postoperative radiotherapy with or without Avoidance of Irradiation of regional Nodes in 1–3 node-positive breast cancer (RIGAIN): a study protocol for a multicentre, open-label, randomised controlled prospective, phase III trial
Jing Liu, Yuting Tan, Zhuofei Bi, Suning Huang, Na Zhang, An-du Zhang, Lina Zhao, Yu Wang, Zibin Liang, Yu Hou, Xiangying Xu, Jianying Chen, Fei Wang, Xiaowen Lan, Xiao Lin, Xiaoxue Zhang, Wenyi Zhou, Xuting Ye, Jian-gui Guo, Xiaohong Wang, Ran Ding, Jiay
BMJ Open.2024; 14(7): e078049. CrossRef
The prognostic analysis of further axillary dissection in breast cancer with 1-2 positive sentinel lymph nodes undergoing mastectomy
Xueyi Zhao, Liu Yang, Congbo Cao, Zhenchuan Song
Frontiers in Oncology.2024;[Epub] CrossRef
Sentinel lymph node biopsy versus axillary lymph node dissection in breast cancer patients undergoing mastectomy
Damiano GENTILE, Corrado TINTERRI
Minerva Surgery.2024;[Epub] CrossRef
Can Axillary Lymph Node Dissection be Omitted in Breast Cancer Patients with Metastatic Sentinel Lymph Nodes Undergoing Mastectomy? A Systematic Review and Meta‐Analysis of Real‐World Evidence
Fulong Chen, Xiaowen Li, Xianjun Lin, Lijia Chen, Zhaoling Lin, Hao Wu, Jishang Chen
World Journal of Surgery.2023; 47(10): 2446. CrossRef
De-implementation of Axillary Dissection in Women Undergoing Mastectomy for Breast Cancer
Laura D. Leonard, Thiago B. de Araujo, Christopher Quinn, Madeline B. Thomas, Laurel Beaty, Nicole M. Mott, Kathryn Colborn, Alicia A. Heelan, Sarah E. A. Tevis, Nicole Christian, Gretchen Arhendt, Ana L. Gleisner
Annals of Surgical Oncology.2023; 30(9): 5692. CrossRef
A multi-dimensional nomogram to predict non-sentinel lymph node metastases in T1–2HR+ breast cancer
Ke Xiang, Jialin Chen, Yu Min, Hang Chen, Jiaxin Yang, Daixing Hu, Yuling Han, Guobing Yin, Yang Feng
Frontiers in Endocrinology.2023;[Epub] CrossRef
Sentinel lymph node biopsy versus axillary lymph node dissection in breast cancer patients undergoing mastectomy with one to two metastatic sentinel lymph nodes: sub-analysis of the SINODAR-ONE multicentre randomized clinical trial and reopening of enrolm
Corrado Tinterri, Giuseppe Canavese, Wolfgang Gatzemeier, Erika Barbieri, Alberto Bottini, Andrea Sagona, Giulia Caraceni, Alberto Testori, Simone Di Maria Grimaldi, Carla Dani, Luca Boni, Paolo Bruzzi, Bethania Fernandes, Marta Scorsetti, Alberto Zambell
British Journal of Surgery.2023; 110(9): 1143. CrossRef
Efficacy and safety comparison between axillary lymph node dissection with no axillary surgery in patients with sentinel node-positive breast cancer: a systematic review and meta-analysis
Yu-Jia Fan, Jin-Cheng Li, De-Miao Zhu, Hai-Long Zhu, Yi Zhao, Xin-Bing Zhu, Gang Wu, Ting-ting Bai
BMC Surgery.2023;[Epub] CrossRef
Factores predictivos de metástasis en ganglios no centinela en el cáncer de mama con ganglio centinela positivo
Mariana Peyroteo, Rita Canotilho, Ana Margarida Correia, Catarina Baía, Cátia Ribeiro, Paulo Reis, Abreu de Sousa
Cirugía Española.2022; 100(2): 81. CrossRef
Optimizing Axillary Management in Clinical T1-2N0 Mastectomy Patients with Positive Sentinel Lymph Nodes
Olga Kantor, Jessica Means, Samantha Grossmith, Tanujit Dey, Jennifer R. Bellon, Elizabeth A. Mittendorf, Tari A. King
Annals of Surgical Oncology.2022; 29(2): 972. CrossRef
Predictive factors of non-sentinel lymph node disease in breast cancer patients with positive sentinel lymph node
Mariana Peyroteo, Rita Canotilho, Ana Margarida Correia, Catarina Baía, Cátia Ribeiro, Paulo Reis, Abreu de Sousa
Cirugía Española (English Edition).2022; 100(2): 81. CrossRef
Axilla lymph node dissection can be safely omitted in patients with 1–2 positive sentinel nodes receiving mastectomy: a large multi-institutional study and a systemic meta-analysis
Weiqi Gao, Shuangshuang Lu, Yufei Zeng, Xiaosong Chen, Kunwei Shen
Breast Cancer Research and Treatment.2022; 196(1): 129. CrossRef
Comparison of survival outcomes between axillary conservation and axillary lymph node dissections in N1 early breast cancer: a propensity-matched SEER analysis
Nisha Wu, Xiaohan Su, Qiao Tan, Jing Luo, Yewei Yuan, Lingmi Hou, Junyan Li
Clinical and Translational Oncology.2022; 25(4): 1091. CrossRef
Surgeon Bias in the Management of Positive Sentinel Lymph Nodes
Brittany J. Mathias, James Sun, Weihong Sun, Jun-Min Zhou, William J. Fulp, Christine Laronga, M. Catherine Lee, John V. Kiluk
Clinical Breast Cancer.2021; 21(1): 74. CrossRef
Impact of Axillary Dissection Among Patients With Sentinel Node–Positive Breast Cancer Undergoing Mastectomy
James Sun, Brittany J. Mathias, Christine Laronga, Weihong Sun, Jun-Min Zhou, William J. Fulp, John V. Kiluk, M. Catherine Lee
Journal of the National Comprehensive Cancer Network.2021; 19(1): 40. CrossRef
Evolution of the Use of Completion Axillary Lymph Node Dissection in Patients with T1/2N0M0 Breast Cancer and Tumour-Involved Sentinel Lymph Nodes Undergoing Mastectomy: A Cohort Study
André Hennigs, Fabian Riedel, Manuel Feißt, Melitta Köpke, Mahdi Rezai, Ulrike Nitz, Mareike Moderow, Michael Golatta, Christof Sohn, Jörg Heil
Annals of Surgical Oncology.2019; 26(8): 2435. CrossRef

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The Lymphatic Drainage Pattern of Internal Mammary Sentinel Lymph Node Identified by Small Particle Radiotracer (^99mTc-Dextran 40) in Breast: Xiao-Shan Cao, Guo-Ren Yang, Bin-Bin Cong, Peng-Fei Qiu, Yong-Sheng Wang; Cancer Res Treat. 2019;51(2):483-492. Published online June 11, 2018; DOI: https://doi.org/10.4143/crt.2018.062

Abstract PDF PubReader ePub

Purpose
The purpose of this study was to detect the lymphatic drainage pattern of internal mammary area and verify the concept of internal mammary sentinel lymph node (IM-SLN) in breast.
Materials and Methods
A small particle radiotracer (^99mTc-Dextran 40) was prepared and tested. ^99mTc-Dextran 40 was injected into intraparenchyma at the sound breast by a modified radiotracer injection technique. Subsequently, dynamic single-photon emission computed tomography (SPECT), computed tomography (CT), and SPECT/CT combination images were performed to identify the radioactive lymph vessels and internal mammary lymph nodes (IMLNs). The direction of lymph drainage and the location of the IMLNs were identified in the SPECT/CT imaging.
Results
The radiochemical purity of ^99mTc-Dextran 40 was > 95%. ^99mTc-Dextran 40 could drainage into first, second, and third lymph node and the radioactive lymph node could be detected by the γ detector in the animal experiment. After ^99mTc-Dextran 40 injecting into intraparenchyma, 50.0% cases (15/30) were identified the drainage lymphatic vessels and radioactive IMLNs by SPECT. The drainage lymphatic vessel was found from injection point to the first IMLN (IM-SLN) after 10.5±0.35 minutes radiotracer injection, and then ^99mTc-Dextran 40 was accumulated into the IM-SLN. The combination imaging of SPECT/CT showed the second IMLN received the lymph drainage from the IM-SLN. The lymphatic drainage was step by step in the internal mammary area.
Conclusion
The lymph was identified to drain from different regions of the breast to IM-SLN, and then outward from IM-SLN to other IMLN consecutively. It demonstrated the concept of the IM-SLN and provided more evidences for the application of internal mammary sentinel lymph node biopsy.

Citations

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99mTc-rituximab tracer injection for guiding internal mammary sentinel lymph nodes biopsy in primary breast cancer: A prospective observational study
Wenxin Chen, Yaodong Su, Hui Zhang, Yu Zhang, Lin Zhu, Mengbo Lin, Zhiyi Lin, Mingdian Yu, Shengping Yang, Yanmin Zhang
Frontiers in Oncology.2023;[Epub] CrossRef
Internal mammary lymph node metastasis in breast cancer patients based on anatomical imaging and functional imaging
Wei Wang, Pengfei Qiu, Jianbin Li
Breast Cancer.2022; 29(6): 933. CrossRef
The hypothesis of internal mammary lymph node drainage chain in breast cancer
Zhao Bi, Peng Chen, Xian-Rang Song, Yong-Sheng Wang
Future Oncology.2020; 16(21): 1489. CrossRef
Comparative research on 99mTc-Rituximab and 99mTc-sulfur colloid in sentinel lymph node imaging of breast cancer
Jing-Jie Zhang, Wan-Chun Zhang, Cai-Xia An, Xiao-Min Li, Le Ma
BMC Cancer.2019;[Epub] CrossRef

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Feasibility of Charcoal Tattooing of Cytology-Proven Metastatic Axillary Lymph Node at Diagnosis and Sentinel Lymph Node Biopsy after Neoadjuvant Chemotherapy in Breast Cancer Patients: Seho Park, Ja Seung Koo, Gun Min Kim, Joohyuk Sohn, Seung Il Kim, Young Up Cho, Byeong-Woo Park, Vivian Youngjean Park, Jung Hyun Yoon, Hee Jung Moon, Min Jung Kim, Eun-Kyung Kim; Cancer Res Treat. 2018;50(3):801-812. Published online August 17, 2017; DOI: https://doi.org/10.4143/crt.2017.210

Abstract PDF PubReader ePub

Purpose
Sentinel lymph node biopsy (SLNB) can be performed when node-positive disease is converted to node-negative status after neoadjuvant chemotherapy (NCT). Tattooing nodes might improve accuracy but supportive data are limited. This study aimed to investigate the feasibility of charcoal tattooing metastatic axillary lymph node (ALN) at presentation followed by SLNB after NCT in breast cancers.
Materials and Methods
Twenty patientswith cytology-proven node metastases prospectively underwent charcoal tattooing at diagnosis. SLNB using dual tracers and axillary surgery after NCT were then performed. The detection rate of tattooed node and diagnostic performance of SLNB were analyzed.
Results
All patients underwent charcoal tattooingwithout significant morbidity. Sentinel and tattooed nodes could be detected during surgery after NCT. Nodal pathologic complete response was achieved in 10 patients. Overall sensitivity, false-negative rate (FNR), negative predictive value, and accuracy of hot/blue SLNB were 80.0%, 20.0%, 83.3%, and 90.0%, respectively. Retrieving more nodes and favorable nodal response were associated with improved performance. The best accuracy was observed when excised tattooed node was calculated together (FNR, 0.0%). Cold/non-blue tattooed nodes of five patients were removed during non-sentinel axillary surgery but clinicopathological parameters did not differ compared to patients with hot/blue tattooed node detected during SLNB, suggesting the importance of the tattooing procedure itself to improve performance.
Conclusion
Charcoal tattooing of cytology-confirmed metastatic ALN at presentation is technically feasible and does not limit SLNB after NCT. The tattooing procedure without additional preoperative localization is advantageous for improving the diagnostic performance of SLNB in this setting.

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Indocyanine Green Fluorescence Plus Blue Dye for Sentinel Lymph Node Biopsy in Patients Undergoing Neoadjuvant Chemotherapy for Breast Cancer: A Multicenter, Prospective Cohort Study
Miao Liu, Yang Yang, Bin Hua, Rui Feng, Tianyu Xu, Mengyuan Wang, Xiaowei Qi, Yingming Cao, Bo Zhou, Fuzhong Tong, Peng Liu, Hongjun Liu, Lin Cheng, Houpu Yang, Fei Xie, Siyuan Wang, Chaobin Wang, Yuan Peng, Danhua Shen, Lei Chen, Jun Jiang, Shu Wang
Thoracic Cancer.2025;[Epub] CrossRef
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James Lucocq, Hassan Baig, Esther McNeill, J Michael Dixon
European Journal of Surgical Oncology.2025; 51(7): 109689. CrossRef
Targeted Axillary Dissection for Clinically Node-Positive Breast Cancer Cases that Turn Negative After Neoadjuvant Systemic Therapy Using Charcoal Tattooing
Mohamed Yousri, Ashraf Khater, Waleed Elnahas, Osama Eldamshety, Eman Alnaghy, Mohamed Ezzat
Indian Journal of Surgical Oncology.2025;[Epub] CrossRef
Radiographic identification of a positive clipped axillary lymph node in a mastectomy specimen following neoadjuvant chemotherapy
Andrew Seto, Cynthia Lin, Samantha Norden, Jamie Stratton, Moira O'Riordan, Helen Pass
Radiology Case Reports.2024; 19(1): 435. CrossRef
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Susie Brousse, Clémentine Lafond, Martin Schmitt, Sophie Guillermet, Sébastien Molière, Carole Mathelin
Gynécologie Obstétrique Fertilité & Sénologie .2024; 52(3): 132. CrossRef
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Rexeena V. Bhargavan, Nisha Prasannan, K.M. Jagathnath Krishna, Paul Augustine, Kurian Cherian
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Melanin-Based Nanoparticles for Lymph Node Tattooing: Experimental, Histopathological and Ultrastructural Study
Marta Baselga, Antonio Güemes, Cristina Yus, Teresa Alejo, Víctor Sebastián, Dolores Arribas, Gracia Mendoza, Eva Monleón, Manuel Arruebo
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Yuka Endo, Haruru Kotani, Nobuko Tamura, Kiyo Tanaka, Chiho Kudo, Masataka Sawaki, Masaya Hattori, Akiyo Yoshimura, Ayumi Kataoka, Kazuki Nozawa, Yuri Ozaki, Ayaka Isogai, Rie Komaki, Akira Nakakami, Nari Kureyama, Maho Kusudo, Waki Hosoda, Hidetaka Kawab
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Oncological outcomes of selective axillary dissection with 4% carbon marking
LUCAS ROSKAMP BUDEL, CLEVERTON CÉSAR SPAUTZ, MARIA HELENA LOUVEIRA, TERESA CRISTINA SANTOS CAVALCANTI, ALESSANDRA CORDEIRO FORNAZARI, PLINIO GASPERIN JUNIOR, LEONARDO NISSEN, VINICIUS MILANI BUDEL
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Desfechos oncológicos da dissecção axilar seletiva utilizando carvão a 4% como marcador
LUCAS ROSKAMP BUDEL, CLEVERTON CÉSAR SPAUTZ, MARIA HELENA LOUVEIRA, TERESA CRISTINA SANTOS CAVALCANTI, ALESSANDRA CORDEIRO FORNAZARI, PLINIO GASPERIN JUNIOR, LEONARDO NISSEN, VINICIUS MILANI BUDEL
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Preclinical evaluation of polymer encapsulated carbon-based nano and microparticles for sentinel lymph node tattooing
Marta Baselga, Antonio Güemes, Manuel Arruebo, Cristina Yus, Teresa Alejo, Víctor Sebastián, Gema Martínez, Dolores Arribas, Gracia Mendoza, Concepción Junquera, Eva Monleón
Scientific Reports.2024;[Epub] CrossRef
Biopsia del ganglio centinela y disección axilar dirigida en mujeres con cáncer de mama y axila positiva en el momento del diagnóstico: caminando hacia el futuro
Paula Moral Rubio, Silvia Delgado García, Hortensia Ballester Galiana, Jose Ponce Lorenzo, Tina Martín Bayón, Gloria Peiró
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Risk Factors for a False-Negative Result of Sentinel Node Biopsy in Patients with Clinically Node-Negative Breast Cancer: Seung Ah Lee, Hak Min Lee, Hak Woo Lee, Ban Seok Yang, Jong Tae Park, Sung Gwe Ahn, Joon Jeong, Seung Il Kim; Cancer Res Treat. 2018;50(3):625-633. Published online July 31, 2017; DOI: https://doi.org/10.4143/crt.2017.089

Abstract PDF Supplementary Material PubReader ePub

Purpose
Although sentinel lymph node biopsy (SLNB) can accurately represent the axillary lymph node (ALN) status, the false-negative rate (FNR) of SLNB is the main concern in the patients who receive SLNB alone instead of ALN dissection (ALND).
Materials and Methods
We analyzed 1,886 patientswho underwent ALNDafter negative results of SLNB,retrospectively. A logistic regression analysis was used to identify risk factors associated with a falsenegative (FN) result. Cox regression model was used to estimate the hazard ratio of factors affecting disease-free survival (DFS).
Results
Tumor located in the upper outer portion of the breast, lymphovascular invasion, suspicious node in imaging assessment and less than three sentinel lymph nodes (SLNs) were significant independent risk factors for FN in SLNB conferring an adjusted odds ratio of 2.10 (95% confidence interval [CI], 1.30 to 3.39), 2.69 (95% CI, 1.47 to 4.91), 2.59 (95% CI, 1.62 to 4.14), and 2.39 (95% CI, 1.45 to 3.95), respectively. The prognostic factors affecting DFS were tumor size larger than 2 cm (hazard ratio [HR], 1.86; 95% CI, 1.17 to 2.96) and FN of SLNB (HR, 2.51; 95% CI, 1.42 to 4.42) in SLN-negative group (FN and true-negative), but in ALN-positive group (FN and true-positive), FN of SLNB (HR, 0.64; 95% CI, 0.33 to 1.25) did not affect DFS.
Conclusion
In patients with risk factors for a FN such as suspicious node in imaging assessment, upper outer breast cancer, less than three harvested nodes, we need attention to find another metastatic focus in non-SLNs during the operation. It may contribute to provide an exact prognosis and optimizing adjuvant treatments.

Citations

Citations to this article as recorded by

Axillary staging with 18F-FDG PET/CT in early breast cancer: impact of tumor subtypes
Abdullah Gunes, Nuray Colapkulu-Akgul, Caner Akgul, Ibrahim Unlu, Saffet Cinar
Annals of Saudi Medicine.2025; 45(3): 145. CrossRef
Detection of presence or absence of metastasis in WSI patches of breast cancer using the dual-enhanced convolutional ensemble neural network
Ruigang Ge, Guoyue Chen, Kazuki Saruta, Yuki Terata
Machine Learning with Applications.2024; 17: 100579. CrossRef
Ultrasound radiomics based on axillary lymph nodes images for predicting lymph node metastasis in breast cancer
Yu-Long Tang, Bin Wang, Tao Ou-Yang, Wen-Zhi Lv, Shi-Chu Tang, An Wei, Xin-Wu Cui, Jiang-Sheng Huang
Frontiers in Oncology.2023;[Epub] CrossRef
Future Directions in the Assessment of Axillary Lymph Nodes in Patients with Breast Cancer
Filippo Pesapane, Luciano Mariano, Francesca Magnoni, Anna Rotili, Davide Pupo, Luca Nicosia, Anna Carla Bozzini, Silvia Penco, Antuono Latronico, Maria Pizzamiglio, Giovanni Corso, Enrico Cassano
Medicina.2023; 59(9): 1544. CrossRef
Axillary Lymph Node Dissection Can Be Omitted in Breast Cancer Patients With Mastectomy and False-Negative Frozen Section in Sentinel Lymph Node Biopsy
Jing Si, Rong Guo, Huan Pan, Xiang Lu, Zhiqin Guo, Chao Han, Li Xue, Dan Xing, Wanxin Wu, Caiping Chen
Frontiers in Oncology.2022;[Epub] CrossRef
False-negative frozen section of sentinel nodes in early breast cancer (cT1-2N0) patients
Zhu-Jun Loh, Kuo-Ting Lee, Ya-Ping Chen, Yao-Lung Kuo, Wei-Pang Chung, Ya-Ting Hsu, Chien-Chang Huang, Hui-Ping Hsu
World Journal of Surgical Oncology.2021;[Epub] CrossRef
What Is High-risk Breast Cancer With Pathologically Negative Lymph Nodes for Regional Recurrence?
Sang-Won Kim, Won Kyung Cho, Doo Ho Choi, Haeyoung Kim, Oyeon Cho, Won Park, Mison Chun
International Journal of Radiation Oncology*Biology*Physics.2021; 111(4): 992. CrossRef
Validating the ACOSOG Z0011 Trial Result: A Population-Based Study Using the SEER Database
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Cancers.2020; 12(4): 950. CrossRef
Retrospectively validating the results of the ACOSOG Z0011 trial in a large Asian Z0011-eligible cohort
Jiwoong Jung, Wonshik Han, Eun Sook Lee, So-Youn Jung, Jai Hong Han, Dong-Young Noh, Yumi Kim, Hee Jun Choi, Jeong Eon Lee, Seok Jin Nam, Jong Won Lee, Hee Jeong Kim, Eunhae Um, Joo Heung Kim, Seho Park, Young Up Cho
Breast Cancer Research and Treatment.2019; 175(1): 203. CrossRef
Preliminary study of contrast-enhanced ultrasound in combination with blue dye vs. indocyanine green fluorescence, in combination with blue dye for sentinel lymph node biopsy in breast cancer
Yidong Zhou, Yan Li, Feng Mao, Jing Zhang, Qingli Zhu, Songjie Shen, Yan Lin, Xiaohui Zhang, He Liu, Mengsu Xiao, Yuxin Jiang, Qiang Sun
BMC Cancer.2019;[Epub] CrossRef

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Can We Skip Intraoperative Evaluation of Sentinel Lymph Nodes? Nomogram Predicting Involvement of Three or More Axillary Lymph Nodes before Breast Cancer Surgery: Soo Kyung Ahn, Min Kyoon Kim, Jongjin Kim, Eunshin Lee, Tae-Kyung Yoo, Han-Byoel Lee, Young Joon Kang, Jisun Kim, Hyeong-Gon Moon, Jung Min Chang, Nariya Cho, Woo Kyung Moon, In Ae Park, Dong-Young Noh, Wonshik Han; Cancer Res Treat. 2017;49(4):1088-1096. Published online January 25, 2017; DOI: https://doi.org/10.4143/crt.2016.473

Abstract PDF Supplementary Material PubReader ePub

Purpose
The American College of Surgeons Oncology Group Z0011 trial reported that complete dissection of axillary lymph nodes (ALNs) may not be warranted in women with clinical T1-T2 tumors and one or two involved ALNs who were undergoing lumpectomy plus radiation followed by systemic therapy. The present study was conducted to identify preoperative imaging predictors of ≥ 3 ALNs.
Materials and Methods
The training set consisted of 1,917 patients with clinical T1-T2 and node negative invasive breast cancer. Factors associated with ≥ 3 involved ALNs were evaluated by logistic regression analysis. The validation set consisted of 378 independent patients. The nomogram was applied prospectively to 512 patients who met the Z0011 criteria.
Results
Of the 1,917 patients, 204 (10.6%) had ≥ 3 positive nodes. Multivariate analysis showed that involvement of ≥ 3 nodes was significantly associated with ultrasonographic and chest computed tomography findings of suspicious ALNs (p < 0.001 each). These two imaging criteria, plus patient age, were used to develop a nomogram calculating the probability of involvement of ≥ 3 ALNs. The areas under the receiver operating characteristic curve of the nomogram were 0.852 (95% confidence interval [CI], 0.820 to 0.883) for the training set and 0.896 (95% CI, 0.836 to 0.957) for the validation set. Prospective application of the nomogram showed that 60 of 512 patients (11.7%) had scores above the cut-off. Application of the nomogram reduced operation time and cost, with a very low re-operation rate (1.6%).
Conclusion
Patients likely to have ≥ 3 positive ALNs could be identified by preoperative imaging. The nomogram was helpful in selective intraoperative examination of sentinel lymph nodes.

Citations

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Jung Ho Park, Hyun Ryung Kim, Sanghwa Kim, Young Ah Lim, Kyoonsoon Jung, Lee Su Kim
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V. Madekivi, P. Boström, A. Karlsson, R. Aaltonen, E. Salminen
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Antonio Piñero-Madrona, Francisco Ripoll-Orts, José Ignacio Sánchez-Méndez, Asunción Chaves-Benito, Maximiliano Rodrigo Gómez-de la Bárcena, Ana Calatrava-Fons, Salomón Menjón-Beltrán, Vicente Peg-Cámara
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Jung Min Chang, Jessica W. T. Leung, Linda Moy, Su Min Ha, Woo Kyung Moon
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Martijn Leenders, Gaëlle Kramer, Kamar Belghazi, Katya Duvivier, Petrousjka van den Tol, Hermien Schreurs
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Computer-aided prediction model for axillary lymph node metastasis in breast cancer using tumor morphological and textural features on ultrasound
Woo Kyung Moon, I-Ling Chen, Ann Yi, Min Sun Bae, Sung Ui Shin, Ruey-Feng Chang
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Sofia E Triantafillidou
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Han-kyul Shin, Min Kyoon Kim, Sung Jun Park, Ju Won Seok, Hee-Chul Shin
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The Expression of Carbonic Anhydrase (CA) IX/XII and Lymph Node Metastasis in Early Breast Cancer: Keun-Yong Eom, Min Hye Jang, So Yeon Park, Eun Young Kang, Sung Won Kim, Jee Hyun Kim, Jae-Sung Kim, In Ah Kim; Cancer Res Treat. 2016;48(1):125-132. Published online March 3, 2015; DOI: https://doi.org/10.4143/crt.2014.243

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Purpose
The aim of study was to test by immunohistochemical (IHC) staining whether carbonic anhydrase (CA) 9 and 12 have an effect on sentinel lymph node (SLN) metastasis in early breast cancer and to find clinicopathologic factors associated with SLN metastasis.
Materials and Methods
Between June 2003 and June 2011, medical records of 470 patients diagnosedwith breast cancer with pT1-2, pN0-2, and M0 were reviewed. Of these 470, 314 patients who underwent SLN biopsy±axillary dissection were subjects of this study. Using tissue microarray, IHC staining for CA9 and CA12 was performed. Clinicopathologic factors such as patient age, tumour size, lymphatic invasion, hormone receptor status, and the Ki-67 labeling index were analysed together.
Results
The mean age of all patients was 51.7 years. The mean number of harvested SLN was 3.62, and 212 patients (67.5%) had negative SLN. Lymphatic invasion, the Ki-67 labelling index of primary tumours, and CA9 staining of stromal cells, were independent risk factors for SLN metastasis in the multivariate analysis. In 33 patients (10.5%) without the three risk factors, no patient had SLN metastasis. In 80 patients without lymphatic invasion of primary tumours or CA9 staining of stromal cells, only four patients (5%) had positive SLN.
Conclusion
CA9 staining of stromal cells is an independent risk factor for SLN metastasis as well as lymphatic invasion and a low Ki-67 labelling index of primary tumours in patients with early breast cancer. IHC staining of primary tumours for CA12was not associatedwith SLN metastasis.

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The Diagnostic Role of TFF1, TFF3, FOXA1, CA XII and TRPS1 in Serous Effusions
Ben Davidson, Arild Holth, Jeremias Wohlschlaeger, Maurizio Pinamonti, Binnur Önal
Cytopathology.2025;[Epub] CrossRef
Impact of CA9 expression in the diagnosis of lymph-node metastases in non-small cell lung cancer based on [18F]FDG PET/CT
Satoshi Suzuki, Masakazu Yashiro, Nobuhiro Izumi, Takuma Tsukioka, Hidetoshi Inoue, Kantaro Hara, Ryuichi Ito, Takuya Tanimura, Noritoshi Nishiyama, Domenico Albano
PLOS ONE.2024; 19(10): e0312846. CrossRef
Carbonic Anhydrase XII Expression Is Modulated during Epithelial Mesenchymal Transition and Regulated through Protein Kinase C Signaling
Daniele Vergara, Sara Ravaioli, Eugenio Fonzi, Loredaria Adamo, Marina Damato, Sara Bravaccini, Francesca Pirini, Antonio Gaballo, Raffaela Barbano, Barbara Pasculli, Julien Franck, Isabelle Fournier, Michel Salzet, Michele Maffia
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Cancers.2020; 12(4): 898. CrossRef
Identification and validation of a combined hypoxia and immune index for triple‐negative breast cancer
Shaoquan Zheng, Yutian Zou, Jie‐ying Liang, Weikai Xiao, Anli Yang, Tiebao Meng, Shilin Lu, Zhongbing Luo, Xiaoming Xie
Molecular Oncology.2020; 14(11): 2814. CrossRef
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Simonas Daunys, Vilma Petrikaitė
Biology of the Cell.2020; 112(12): 383. CrossRef
Overexpression of HIF1α and CAXI predicts poor outcome in early-stage triple negative breast cancer
Min-Sun Jin, Hyebin Lee, In Ae Park, Yul Ri Chung, Seock-Ah Im, Kyung-Hun Lee, Hyeong-Gon Moon, Wonshik Han, Kyubo Kim, Tae-Yong Kim, Dong-Young Noh, Han Suk Ryu
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Prospective Evaluation of the Feasibility of Sentinel Lymph Node Biopsy in Breast Cancer Patients with Negative Axillary Conversion after Neoadjuvant Chemotherapy: Hy-De Lee, Sung Gwe Ahn, Seung Ah Lee, Hak Min Lee, Joon Jeong; Cancer Res Treat. 2015;47(1):26-33. Published online August 29, 2014; DOI: https://doi.org/10.4143/crt.2013.208

Abstract PDF PubReader ePub

Purpose
Tumor response to neoadjuvant chemotherapy (NAC) may adversely affect the identification and accuracy rate of sentinel lymph node biopsy (SLNB). This study was conducted to evaluate the feasibility of SLNB in node-positive breast cancer patients with negative axillary conversion after NAC. Materials and Methods Ninety-six patients with positive nodes at presentation were prospectively enrolled. 18Fluorodeoxyglucose-positron emission tomography (18F-FDG PET) and ultrasonography were performed before and after NAC. A metastatic axillary lymph node was defined as positive if it was positive upon both 18F-FDG PET and ultrasonography, while it was considered negative if it was negative upon both 18F-FDG PET and ultrasonography. Results After NAC, 55 cases (57.3%) became clinically node-negative, while 41 cases (42.7%) remained node-positive. In the entire cohort, the sentinel lymph node (SLN) identification and false-negative rates were 84.3% (81/96) and 18.4% (9/49), respectively. In the negative axillary conversion group, the results of SLNB showed an 85.7% (48/55) identification rate and 16.7% (4/24) false-negative rate. Conclusion For breast cancer patients with clinically positive nodes at presentation, it is difficult to conclude whether the SLN accurately represents the metastatic status of all axillary lymph nodes, even after clinically negative node conversion following NAC.

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