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      Development of a Rare Earth Nanoprobe Enables In Vivo Real-Time Detection of Sentinel Lymph Node Metastasis of Breast Cancer Using NIR-IIb Imaging

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          Abstract

          NIR-IIb imaging of a rare-earth nanoprobe that is specifically taken up by breast cancer cells can accurately detect breast cancer macrometastases and micrometastases in sentinel lymph nodes.

          Abstract

          Sentinel lymph node (SLN) biopsy plays a critical role in axillary staging of breast cancer. However, traditional SLN mapping does not accurately discern the presence or absence of metastatic disease. Detection of SLN metastasis largely hinges on examination of frozen sections or paraffin-embedded tissues post-SLN biopsy. To improve detection of SLN metastasis, we developed a second near-infrared (NIR-II) in vivo fluorescence imaging system, pairing erbium-based rare-earth nanoparticles (ErNP) with bright down-conversion fluorescence at 1,556 nm. To visualize SLNs bearing breast cancer, ErNPs were modified by balixafortide (ErNPs@POL6326), a peptide antagonist of the chemokine receptor CXCR4. The ErNPs@POL6326 probes readily drained into SLNs when delivered subcutaneously, entering metastatic breast tumor cells specifically via CXCR4-mediated endocytosis. NIR fluorescence signals increased significantly in tumor-positive versus tumor-negative SLNs, enabling accurate determination of SLN breast cancer metastasis. In a syngeneic mouse mammary tumor model and a human breast cancer xenograft model, sensitivity for SLN metastasis detection was 92.86% and 93.33%, respectively, and specificity was 96.15% and 96.08%, respectively. Of note, the probes accurately detected both macrometastases and micrometastases in SLNs. These results overall underscore the potential of ErNPs@POL6326 for real-time visualization of SLNs and in vivo screening for SLN metastasis.

          Significance:

          NIR-IIb imaging of a rare-earth nanoprobe that is specifically taken up by breast cancer cells can accurately detect breast cancer macrometastases and micrometastases in sentinel lymph nodes.

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          Most cited references57

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          A randomized comparison of sentinel-node biopsy with routine axillary dissection in breast cancer.

          Although numerous studies have shown that the status of the sentinel node is an accurate predictor of the status of the axillary nodes in breast cancer, the efficacy and safety of sentinel-node biopsy require validation. From March 1998 to December 1999, we randomly assigned 516 patients with primary breast cancer in whom the tumor was less than or equal to 2 cm in diameter either to sentinel-node biopsy and total axillary dissection (the axillary-dissection group) or to sentinel-node biopsy followed by axillary dissection only if the sentinel node contained metastases (the sentinel-node group). The number of sentinel nodes found was the same in the two groups. A sentinel node was positive in 83 of the 257 patients in the axillary-dissection group (32.3 percent), and in 92 of the 259 patients in the sentinel-node group (35.5 percent). In the axillary-dissection group, the overall accuracy of the sentinel-node status was 96.9 percent, the sensitivity 91.2 percent, and the specificity 100 percent. There was less pain and better arm mobility in the patients who underwent sentinel-node biopsy only than in those who also underwent axillary dissection. There were 15 events associated with breast cancer in the axillary-dissection group and 10 such events in the sentinel-node group. Among the 167 patients who did not undergo axillary dissection, there were no cases of overt axillary metastasis during follow-up. Sentinel-node biopsy is a safe and accurate method of screening the axillary nodes for metastasis in women with a small breast cancer. Copyright 2003 Massachusetts Medical Society
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            Involvement of chemokine receptors in breast cancer metastasis.

            Breast cancer is characterized by a distinct metastatic pattern involving the regional lymph nodes, bone marrow, lung and liver. Tumour cell migration and metastasis share many similarities with leukocyte trafficking, which is critically regulated by chemokines and their receptors. Here we report that the chemokine receptors CXCR4 and CCR7 are highly expressed in human breast cancer cells, malignant breast tumours and metastases. Their respective ligands CXCL12/SDF-1alpha and CCL21/6Ckine exhibit peak levels of expression in organs representing the first destinations of breast cancer metastasis. In breast cancer cells, signalling through CXCR4 or CCR7 mediates actin polymerization and pseudopodia formation, and subsequently induces chemotactic and invasive responses. In vivo, neutralizing the interactions of CXCL12/CXCR4 significantly impairs metastasis of breast cancer cells to regional lymph nodes and lung. Malignant melanoma, which has a similar metastatic pattern as breast cancer but also a high incidence of skin metastases, shows high expression levels of CCR10 in addition to CXCR4 and CCR7. Our findings indicate that chemokines and their receptors have a critical role in determining the metastatic destination of tumour cells.
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              Randomized multicenter trial of sentinel node biopsy versus standard axillary treatment in operable breast cancer: the ALMANAC Trial.

              Sentinel lymph node biopsy in women with operable breast cancer is routinely used in some countries for staging the axilla despite limited data from randomized trials on morbidity and mortality outcomes. We conducted a multicenter randomized trial to compare quality-of-life outcomes between patients with clinically node-negative invasive breast cancer who received sentinel lymph node biopsy and patients who received standard axillary treatment. The primary outcome measures were arm and shoulder morbidity and quality of life. From November 1999 to October 2003, 1031 patients were randomly assigned to undergo sentinel lymph node biopsy (n = 515) or standard axillary surgery (n = 516). Patients with sentinel lymph node metastases proceeded to delayed axillary clearance or received axillary radiotherapy (depending on the protocol at the treating institution). Intention-to-treat analyses of data at 1, 3, 6, and 12 months after surgery are presented. All statistical tests were two-sided. The relative risks of any lymphedema and sensory loss for the sentinel lymph node biopsy group compared with the standard axillary treatment group at 12 months were 0.37 (95% confidence interval [CI] = 0.23 to 0.60; absolute rates: 5% versus 13%) and 0.37 (95% CI = 0.27 to 0.50; absolute rates: 11% versus 31%), respectively. Drain usage, length of hospital stay, and time to resumption of normal day-to-day activities after surgery were statistically significantly lower in the sentinel lymph node biopsy group (all P .05). Sentinel lymph node biopsy is associated with reduced arm morbidity and better quality of life than standard axillary treatment and should be the treatment of choice for patients who have early-stage breast cancer with clinically negative nodes.
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                Author and article information

                Journal
                Cancer Res
                Cancer Res
                Cancer Research
                American Association for Cancer Research
                0008-5472
                1538-7445
                13 October 2023
                04 August 2023
                : 83
                : 20
                : 3428-3441
                Affiliations
                [1 ]Department of Breast-Thyroid-Surgery and Cancer Center, Xiang'an Hospital of Xiamen University, School of Medicine, Xiamen University, Xiamen, China.
                [2 ]Fujian Key Laboratory of Precision Diagnosis and Treatment in Breast Cancer (Xiang'an Hospital of Xiamen University), Xiamen, China.
                [3 ]Xiamen Key Laboratory for Endocrine Related Cancer Precision Medicine, Xiang'an Hospital of Xiamen University, Xiamen, China.
                [4 ]Xiamen Research Center of Clinical Medicine in Breast & Thyroid Cancers, Xiamen, China.
                [5 ]State Key Laboratory of Structural Chemistry, Fujian Institute of Research on the Structure of Matter, Chinese Academy of Sciences, Fuzhou, China.
                [6 ]Xiamen Key Laboratory of Rare Earth Photoelectric Functional Materials, Xiamen Institute of Rare Earth Materials, Haixi Institute, Chinese Academy of Sciences, Xiamen, China.
                [7 ]University of Chinese Academy of Sciences, Beijing, China.
                [8 ]Cancer Research Center, School of Medicine, Xiamen University, Xiamen, China.
                Author notes
                [#]

                Y-Y. Zhu, L. Song, and Y-Q. Zhang contributed equally to this article.

                [* ] Corresponding Authors: Guo-Jun Zhang, The Cancer Center and the Department of Breast Thyroid Surgery, Xiang'an Hospital of Xiamen University, Xiamen 361100, China. E-mail: gjzhang@ 123456xah.xmu.edu.cn ; and Yun Zhang, Xiamen Institute of Rare Earth Materials, Haixi Institute, Chinese Academy of Sciences, Xiamen 361021, China. E-mail: zhangy@ 123456fjirsm.ac.cn

                Cancer Res 2023;83:3428–41

                Author information
                https://orcid.org/0009-0003-3439-6170
                https://orcid.org/0009-0001-9751-6649
                https://orcid.org/0009-0000-4527-1558
                https://orcid.org/0009-0008-4740-720X
                https://orcid.org/0000-0002-2261-4519
                https://orcid.org/0009-0001-8110-2396
                https://orcid.org/0009-0004-0915-3043
                https://orcid.org/0009-0009-1802-9294
                https://orcid.org/0009-0005-5643-2907
                https://orcid.org/0000-0001-6288-4671
                https://orcid.org/0000-0001-5182-5887
                Article
                CAN-22-3432
                10.1158/0008-5472.CAN-22-3432
                10570679
                37540231
                d2e23d6b-56bf-45ed-9a69-932ca09bb67b
                ©2023 The Authors; Published by the American Association for Cancer Research

                This open access article is distributed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International (CC BY-NC-ND 4.0) license.

                History
                : 31 October 2022
                : 09 May 2023
                : 02 August 2023
                Page count
                Pages: 14
                Funding
                Funded by: National Natural Science Foundation of China (NSFC), https://doi.org/10.13039/501100001809;
                Award ID: 32171363
                Award Recipient :
                Funded by: National Natural Science Foundation of China (NSFC), https://doi.org/10.13039/501100001809;
                Award ID: 62105333
                Award Recipient :
                Categories
                Translational Cancer Biology

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