Research progress of carbon tattoo in targeted lymph node dissection after neoadjuvant therapy for breast cancer_CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Authors：

XU Jiawei , GONG Junge ,  LI Hongyuan

Department of Breast and Thyroid Surgery, The First Affiliated Hospital of Chongqing Medical University, Chongqing 400042, P. R. China;

Corresponding author：

LI Hongyuan, Email: hongy_li@hotmail.com

Keywords：

breast cancer; carbon tattoo; lymph node labeling

DOI：

10.7507/1007-9424.202312080

Video：

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Objective To summarize the progress of the researches about nano-carbon tattoo in targeted lymph node dissection of breast cancer. Method The relevant studies on the application of nano-carbon tattoo to target lymph nodes in the breast cancer at home and abroad were searched and the feasibility and shortcomings of this method were summarized. Result From the studies reported, the nano-carbon tattoo method had a high detection rate (64.0%–100%) and coincidence rate (55.0%–100%), as well as a lower false negative rate (0.0%–9.1%) in the labeling of breast cancer targeted lymph nodes. Conclusions The nano-carbon tattoo method is a useful, simple, and safe in the labeling of targeted lymph nodes in breast cancer. But the specific implementation scheme of this method, such as the optimal labeling dosage, the number of labeled lymph nodes, and the improvement of patients’ quality of life are still unclear, which still needs more large-scale prospective research to verify.

Citation： XU Jiawei, GONG Junge, LI Hongyuan. Research progress of carbon tattoo in targeted lymph node dissection after neoadjuvant therapy for breast cancer. CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY, 2024, 31(7): 892-896. doi: 10.7507/1007-9424.202312080 Copy

1.	Belmonte R, Messaggi-Sartor M, Ferrer M, et al. Prospective study of shoulder strength, shoulder range of motion, and lymphedema in breast cancer patients from pre-surgery to 5 years after ALND or SLNB. Support Care Cancer, 2018, 26(9): 3277-3287.
2.	Diego EJ, McAuliffe PF, Soran A, et al. Axillary staging after neoadjuvant chemotherapy for breast cancer: A pilot study combining sentinel lymph node biopsy with radioactive seed localization of pre-treatment positive axillary lymph nodes. Ann Surg Oncol, 2016, 23(5): 1549-1553.
3.	Dominici LS, Negron Gonzalez VM, Buzdar AU, et al. Cytologically proven axillary lymph node metastases are eradicated in patients receiving preoperative chemotherapy with concurrent trastuzumab for HER2-positive breast cancer. Cancer, 2010, 116(12): 2884-2889.
4.	Woods RW, Camp MS, Durr NJ, et al. A review of options for localization of axillary lymph nodes in the treatment of invasive breast cancer. Acad Radiol, 2019, 26(6): 805-819.
5.	Lim GH, Teo SY, Gudi M, et al. Initial results of a novel technique of clipped node localization in breast cancer patients postneoadjuvant chemotherapy: Skin Mark clipped Axillary nodes Removal Technique (SMART trial). Cancer Med, 2020, 9(6): 1978-1985.
6.	Caudle AS, Yang WT, Krishnamurthy S, et al. Improved axillary evaluation following neoadjuvant therapy for patients with node-positive breast cancer using selective evaluation of clipped nodes: implementation of targeted axillary dissection. J Clin Oncol, 2016, 34(10): 1072-1078.
7.	Nizam R, Siddiqi N, Landas SK, et al. Colonic tattooing with India ink: benefits, risks, and alternatives. Am J Gastroenterol, 1996, 91(9): 1804-1808.
8.	Mullen DJ, Eisen RN, Newman RD, et al. The use of carbon marking after stereotactic large-core-needle breast biopsy. Radiology, 2001, 218(1): 255-260.
9.	Kim WH, Kim HJ, Kim SH, et al. Ultrasound-guided dual-localization for axillary nodes before and after neoadjuvant chemotherapy with clip and activated charcoal in breast cancer patients: a feasibility study. BMC Cancer, 2019, 19(1): 859. doi: 10.1186/s12885-019-6095-1.
10.	Khallaf E, Wessam R, Abdoon M. Targeted axillary dissection of carbon-tattooed metastatic lymph nodes in combination with post-neo-adjuvant sentinel lymph node biopsy using 1% methylene blue in breast cancer patients. Breast J, 2020, 26(5): 1061-1063.
11.	Park S, Koo JS, Kim GM, et al. 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. Cancer Res Treat, 2018, 50(3): 801-812.
12.	Banys-Paluchowski M, Gruber IV, Hartkopf A, et al. Axillary ultrasound for prediction of response to neoadjuvant therapy in the context of surgical strategies to axillary dissection in primary breast cancer: a systematic review of the current literature. Arch Gynecol Obstet, 2020, 301(2): 341-353.
13.	Wazir U, Mokbel K. De-escalation of axillary surgery in the neoadjuvant chemotherapy (NACT) setting for breast cancer: Is it oncologically safe?. Anticancer Res, 2020, 40(10): 5351-5354.
14.	Boughey JC, Ballman KV, Le-Petross HT, et al. Identification and resection of clipped node decreases the false-negative rate of sentinel lymph node surgery in patients presenting with node-positive breast cancer (T0–T4, N1–N2) who receive neoadjuvant chemotherapy: results from ACOSOG Z1071 (Alliance). Ann Surg, 2016, 263(4): 802-807.
15.	Boughey JC, Suman VJ, Mittendorf EA, et al. Sentinel lymph node surgery after neoadjuvant chemotherapy in patients with node-positive breast cancer: the ACOSOG Z1071 (Alliance) clinical trial. JAMA, 2013, 310(14): 1455-1461.
16.	Youn I, Choi SH, Kook SH, et al. Ultrasonography-guided surgical clip placement for tumor localization in patients undergoing neoadjuvant chemotherapy for breast cancer. J Breast Cancer, 2015, 18(1): 44-49.
17.	Wong SM, Almana N, Choi J, et al. Prognostic significance of residual axillary nodal micrometastases and isolated tumor cells after neoadjuvant chemotherapy for breast cancer. Ann Surg Oncol, 2019, 26(11): 3502-3509.
18.	Siso C, de Torres J, Esgueva-Colmenarejo A, et al. Intraoperative ultrasound-guided excision of axillary clip in patients with node-positive breast cancer treated with neoadjuvant therapy (ILINA Trial): A new tool to guide the excision of the clipped node after neoadjuvant treatment. Ann Surg Oncol, 2018, 25(3): 784-791.
19.	Donker M, Straver ME, Wesseling J, et al. Marking axillary lymph nodes with radioactive iodine seeds for axillary staging after neoadjuvant systemic treatment in breast cancer patients: the MARI procedure. Ann Surg, 2015, 261(2): 378-382.
20.	Ersoy YE, Kadioglu H. Review of novel sentinel lymph node biopsy techniques in breast cancer patients treated with neoadjuvant chemotherapy. Clin Breast Cancer, 2018, 18(4): e555-e559. doi: 10.1016/j.clbc.2018.01.004.
21.	Kasem I, Mokbel K. Savi Scout® radar localisation of non-palpable breast lesions: systematic review and pooled analysis of 842 cases. Anticancer Res, 2020, 40(7): 3633-3643.
22.	Mariscal Martínez A, Vives Roselló I, Salazar Gómez A, et al. Advantages of preoperative localization and surgical resection of metastatic axillary lymph nodes using magnetic seeds after neoadjuvant chemotherapy in breast cancer. Surg Oncol, 2021, 36: 28-33.
23.	Greenwood HI, Wong JM, Mukhtar RA, et al. Feasibility of magnetic seeds for preoperative localization of axillary lymph nodes in breast cancer treatment. AJR Am J Roentgenol, 2019, 213(4): 953-957.
24.	Hersi AF, Eriksson S, Ramos J, et al. A combined, totally magnetic technique with a magnetic marker for non-palpable tumour localization and superparamagnetic iron oxide nanoparticles for sentinel lymph node detection in breast cancer surgery. Eur J Surg Oncol, 2019, 45(4): 544-549.
25.	Choy N, Lipson J, Porter C, et al. Initial results with preoperative tattooing of biopsied axillary lymph nodes and correlation to sentinel lymph nodes in breast cancer patients. Ann Surg Oncol, 2015, 22(2): 377-382.
26.	Natsiopoulos I, Intzes S, Liappis T, et al. Axillary lymph node tattooing and targeted axillary dissection in breast cancer patients who presented as cN⁺ before neoadjuvant chemotherapy and became cN0 after treatment. Clin Breast Cancer, 2019, 19(3): 208-215.
27.	Goyal A, Puri S, Marshall A, et al. A multicentre prospective feasibility study of carbon dye tattooing of biopsied axillary node and surgical localisation in breast cancer patients. Breast Cancer Res Treat, 2021, 185(2): 433-440.
28.	Porpiglia M, Borella F, Chieppa P, et al. Carbon tattooing of axillary lymph nodes in breast cancer patients before neoadjuvant chemotherapy: A retrospective analysis. Tumori, 2023, 109(3): 301-306.
29.	Patel R, MacKerricher W, Tsai J, et al. Pretreatment tattoo marking of suspicious axillary lymph nodes: reliability and correlation with sentinel lymph node. Ann Surg Oncol, 2019, 26(8): 2452-2458.
30.	Dostalek L, Cerny A, Saskova P, et al. Selective extirpation of tattooed lymph node in combination with sentinel lymph node biopsy in the management of node-positive breast cancer patients after neoadjuvant systemic therapy. Breast Care (Basel), 2021, 16(6): 623-629.
31.	Pilewskie M, Morrow M. Axillary nodal management following neoadjuvant chemotherapy: a review. JAMA Oncol, 2017, 3(4): 549-555.
32.	de Boniface J, Frisell J, Kühn T, et al. False-negative rate in the extended prospective TATTOO trial evaluating targeted axillary dissection by carbon tattooing in clinically node-positive breast cancer patients receiving neoadjuvant systemic therapy. Breast Cancer Res Treat, 2022, 193(3): 589-595.
33.	Milone M, Vignali A, Manigrasso M, et al. Sterile carbon particle suspension vs India ink for endoscopic tattooing of colonic lesions: a randomized controlled trial. Tech Coloproctol, 2019, 23(11): 1073-1078.
34.	Gante I, Maldonado JP, Figueiredo Dias M. Marking techniques for targeted axillary dissection among patients with node-positive breast cancer treated with neoadjuvant chemotherapy. Breast Cancer (Auckl), 2023, 17: 11782234231176159. doi: 10.1177/11782234231176159.
35.	Hartmann S, Kühn T, de Boniface J, et al. Carbon tattooing for targeted lymph node biopsy after primary systemic therapy in breast cancer: prospective multicentre TATTOO trial. Br J Surg, 2021, 108(3): 302-307.
36.	Weber WP, Matrai Z, Hayoz S, et al. Tailored axillary surgery in patients with clinically node-positive breast cancer: Pre-planned feasibility substudy of TAXIS (OPBC-03, SAKK 23/16, IBCSG 57-18, ABCSG-53, GBG 101). Breast, 2021, 60: 98-110.

1. Belmonte R, Messaggi-Sartor M, Ferrer M, et al. Prospective study of shoulder strength, shoulder range of motion, and lymphedema in breast cancer patients from pre-surgery to 5 years after ALND or SLNB. Support Care Cancer, 2018, 26(9): 3277-3287.
2. Diego EJ, McAuliffe PF, Soran A, et al. Axillary staging after neoadjuvant chemotherapy for breast cancer: A pilot study combining sentinel lymph node biopsy with radioactive seed localization of pre-treatment positive axillary lymph nodes. Ann Surg Oncol, 2016, 23(5): 1549-1553.
3. Dominici LS, Negron Gonzalez VM, Buzdar AU, et al. Cytologically proven axillary lymph node metastases are eradicated in patients receiving preoperative chemotherapy with concurrent trastuzumab for HER2-positive breast cancer. Cancer, 2010, 116(12): 2884-2889.
4. Woods RW, Camp MS, Durr NJ, et al. A review of options for localization of axillary lymph nodes in the treatment of invasive breast cancer. Acad Radiol, 2019, 26(6): 805-819.
5. Lim GH, Teo SY, Gudi M, et al. Initial results of a novel technique of clipped node localization in breast cancer patients postneoadjuvant chemotherapy: Skin Mark clipped Axillary nodes Removal Technique (SMART trial). Cancer Med, 2020, 9(6): 1978-1985.
6. Caudle AS, Yang WT, Krishnamurthy S, et al. Improved axillary evaluation following neoadjuvant therapy for patients with node-positive breast cancer using selective evaluation of clipped nodes: implementation of targeted axillary dissection. J Clin Oncol, 2016, 34(10): 1072-1078.
7. Nizam R, Siddiqi N, Landas SK, et al. Colonic tattooing with India ink: benefits, risks, and alternatives. Am J Gastroenterol, 1996, 91(9): 1804-1808.
8. Mullen DJ, Eisen RN, Newman RD, et al. The use of carbon marking after stereotactic large-core-needle breast biopsy. Radiology, 2001, 218(1): 255-260.
9. Kim WH, Kim HJ, Kim SH, et al. Ultrasound-guided dual-localization for axillary nodes before and after neoadjuvant chemotherapy with clip and activated charcoal in breast cancer patients: a feasibility study. BMC Cancer, 2019, 19(1): 859. doi: 10.1186/s12885-019-6095-1.
10. Khallaf E, Wessam R, Abdoon M. Targeted axillary dissection of carbon-tattooed metastatic lymph nodes in combination with post-neo-adjuvant sentinel lymph node biopsy using 1% methylene blue in breast cancer patients. Breast J, 2020, 26(5): 1061-1063.
11. Park S, Koo JS, Kim GM, et al. 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. Cancer Res Treat, 2018, 50(3): 801-812.
12. Banys-Paluchowski M, Gruber IV, Hartkopf A, et al. Axillary ultrasound for prediction of response to neoadjuvant therapy in the context of surgical strategies to axillary dissection in primary breast cancer: a systematic review of the current literature. Arch Gynecol Obstet, 2020, 301(2): 341-353.
13. Wazir U, Mokbel K. De-escalation of axillary surgery in the neoadjuvant chemotherapy (NACT) setting for breast cancer: Is it oncologically safe?. Anticancer Res, 2020, 40(10): 5351-5354.
14. Boughey JC, Ballman KV, Le-Petross HT, et al. Identification and resection of clipped node decreases the false-negative rate of sentinel lymph node surgery in patients presenting with node-positive breast cancer (T0–T4, N1–N2) who receive neoadjuvant chemotherapy: results from ACOSOG Z1071 (Alliance). Ann Surg, 2016, 263(4): 802-807.
15. Boughey JC, Suman VJ, Mittendorf EA, et al. Sentinel lymph node surgery after neoadjuvant chemotherapy in patients with node-positive breast cancer: the ACOSOG Z1071 (Alliance) clinical trial. JAMA, 2013, 310(14): 1455-1461.
16. Youn I, Choi SH, Kook SH, et al. Ultrasonography-guided surgical clip placement for tumor localization in patients undergoing neoadjuvant chemotherapy for breast cancer. J Breast Cancer, 2015, 18(1): 44-49.
17. Wong SM, Almana N, Choi J, et al. Prognostic significance of residual axillary nodal micrometastases and isolated tumor cells after neoadjuvant chemotherapy for breast cancer. Ann Surg Oncol, 2019, 26(11): 3502-3509.
18. Siso C, de Torres J, Esgueva-Colmenarejo A, et al. Intraoperative ultrasound-guided excision of axillary clip in patients with node-positive breast cancer treated with neoadjuvant therapy (ILINA Trial): A new tool to guide the excision of the clipped node after neoadjuvant treatment. Ann Surg Oncol, 2018, 25(3): 784-791.
19. Donker M, Straver ME, Wesseling J, et al. Marking axillary lymph nodes with radioactive iodine seeds for axillary staging after neoadjuvant systemic treatment in breast cancer patients: the MARI procedure. Ann Surg, 2015, 261(2): 378-382.
20. Ersoy YE, Kadioglu H. Review of novel sentinel lymph node biopsy techniques in breast cancer patients treated with neoadjuvant chemotherapy. Clin Breast Cancer, 2018, 18(4): e555-e559. doi: 10.1016/j.clbc.2018.01.004.
21. Kasem I, Mokbel K. Savi Scout® radar localisation of non-palpable breast lesions: systematic review and pooled analysis of 842 cases. Anticancer Res, 2020, 40(7): 3633-3643.
22. Mariscal Martínez A, Vives Roselló I, Salazar Gómez A, et al. Advantages of preoperative localization and surgical resection of metastatic axillary lymph nodes using magnetic seeds after neoadjuvant chemotherapy in breast cancer. Surg Oncol, 2021, 36: 28-33.
23. Greenwood HI, Wong JM, Mukhtar RA, et al. Feasibility of magnetic seeds for preoperative localization of axillary lymph nodes in breast cancer treatment. AJR Am J Roentgenol, 2019, 213(4): 953-957.
24. Hersi AF, Eriksson S, Ramos J, et al. A combined, totally magnetic technique with a magnetic marker for non-palpable tumour localization and superparamagnetic iron oxide nanoparticles for sentinel lymph node detection in breast cancer surgery. Eur J Surg Oncol, 2019, 45(4): 544-549.
25. Choy N, Lipson J, Porter C, et al. Initial results with preoperative tattooing of biopsied axillary lymph nodes and correlation to sentinel lymph nodes in breast cancer patients. Ann Surg Oncol, 2015, 22(2): 377-382.
26. Natsiopoulos I, Intzes S, Liappis T, et al. Axillary lymph node tattooing and targeted axillary dissection in breast cancer patients who presented as cN⁺ before neoadjuvant chemotherapy and became cN0 after treatment. Clin Breast Cancer, 2019, 19(3): 208-215.
27. Goyal A, Puri S, Marshall A, et al. A multicentre prospective feasibility study of carbon dye tattooing of biopsied axillary node and surgical localisation in breast cancer patients. Breast Cancer Res Treat, 2021, 185(2): 433-440.
28. Porpiglia M, Borella F, Chieppa P, et al. Carbon tattooing of axillary lymph nodes in breast cancer patients before neoadjuvant chemotherapy: A retrospective analysis. Tumori, 2023, 109(3): 301-306.
29. Patel R, MacKerricher W, Tsai J, et al. Pretreatment tattoo marking of suspicious axillary lymph nodes: reliability and correlation with sentinel lymph node. Ann Surg Oncol, 2019, 26(8): 2452-2458.
30. Dostalek L, Cerny A, Saskova P, et al. Selective extirpation of tattooed lymph node in combination with sentinel lymph node biopsy in the management of node-positive breast cancer patients after neoadjuvant systemic therapy. Breast Care (Basel), 2021, 16(6): 623-629.
31. Pilewskie M, Morrow M. Axillary nodal management following neoadjuvant chemotherapy: a review. JAMA Oncol, 2017, 3(4): 549-555.
32. de Boniface J, Frisell J, Kühn T, et al. False-negative rate in the extended prospective TATTOO trial evaluating targeted axillary dissection by carbon tattooing in clinically node-positive breast cancer patients receiving neoadjuvant systemic therapy. Breast Cancer Res Treat, 2022, 193(3): 589-595.
33. Milone M, Vignali A, Manigrasso M, et al. Sterile carbon particle suspension vs India ink for endoscopic tattooing of colonic lesions: a randomized controlled trial. Tech Coloproctol, 2019, 23(11): 1073-1078.
34. Gante I, Maldonado JP, Figueiredo Dias M. Marking techniques for targeted axillary dissection among patients with node-positive breast cancer treated with neoadjuvant chemotherapy. Breast Cancer (Auckl), 2023, 17: 11782234231176159. doi: 10.1177/11782234231176159.
35. Hartmann S, Kühn T, de Boniface J, et al. Carbon tattooing for targeted lymph node biopsy after primary systemic therapy in breast cancer: prospective multicentre TATTOO trial. Br J Surg, 2021, 108(3): 302-307.
36. Weber WP, Matrai Z, Hayoz S, et al. Tailored axillary surgery in patients with clinically node-positive breast cancer: Pre-planned feasibility substudy of TAXIS (OPBC-03, SAKK 23/16, IBCSG 57-18, ABCSG-53, GBG 101). Breast, 2021, 60: 98-110.

CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Research progress of carbon tattoo in targeted lymph node dissection after neoadjuvant therapy for breast cancer

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