Magnetic-Guided Axillary UltraSound (MagUS) Sentinel Lymph Node Biopsy and Mapping in Patients with Early Breast Cancer. A Phase 2, Single-Arm Prospective Clinical Trial

Allan Jazrawi, Eirini Pantiora, Shahin Abdsaleh, Daniel Vasiliu Bacovia, Staffan Eriksson, Henrik Leonhardt, Fredrik Wärnberg, Andreas Karakatsanis, Allan Jazrawi, Eirini Pantiora, Shahin Abdsaleh, Daniel Vasiliu Bacovia, Staffan Eriksson, Henrik Leonhardt, Fredrik Wärnberg, Andreas Karakatsanis

Abstract

Lymph Node Dissection (SLND) is standard of care for diagnosing sentinel lymph node (SLN) status in patients with early breast cancer. Study aim was to determine whether the combination of Superparamagnetic iron oxide nanoparticles (SPIO) MRI-lymphography (MRI-LG) and a Magnetic-guided Axillary UltraSound (MagUS) with biopsy can allow for minimally invasive, axillary evaluation to de-escalate surgery. Patients were injected with 2 mL of SPIO and underwent MRI-LG for SN mapping. Thereafter MagUS and core needle biopsy (CNB) were performed. Patients planned for neoadjuvant treatment, the SLN was clipped and SLND was performed after neoadjuvant with the addition of isotope. During surgery, SLNs were controlled for signs of previous biopsy or clip. The primary endpoint was MagUS SLN detection rate, defined as successful SLN detection of at least one SLN of those retrieved in SLND. In 79 patients, 48 underwent upfront surgery, 12 received neoadjuvant and 19 had recurrent cancer. MagUS traced the SLN in all upfront and neoadjuvant cases, detecting all patients with macrometastases (n = 10). MagUS missed only one micrometastasis, outperforming baseline axillary ultrasound AUS (AUC: 0.950 vs. 0.508, p < 0.001) and showing no discordance to SLND (p = 1.000). MagUS provides the niche for minimally invasive axillary mapping that can reduce diagnostic surgery.

Keywords: breast cancer; magnetic tracer; sentinel lymph node; sentinel lymph node biopsy; superparamagnetic iron oxide.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
(a,b). Visualization of SLN with MRI before and after SPIO. In an enhancement of the SLN is visualized after injection of SPIO. The red circle visualizes the enhanced SLN after the injection of SPIO.
Figure 2
Figure 2
(a,b). MagUS with the SLN visualized in the red circle (left). Magnetic probe localizes the magnetic “hotspot” and after that CNB is performed (right). Monitor width 3.9 cm.
Figure 3
Figure 3
MagUS SLN-biopsy specimen (size 1 cm).
Figure 4
Figure 4
Flowchart showing the MagUS process.
Figure 5
Figure 5
STARD flow diagram. * MRI_LG: Magnetic resonance imaging Lymphography. SLND: Sentinel Lymph Node Dissection.

References

    1. Kim M.K., Park H.S., Kim J.Y., Kim S., Nam S., Park S., Kim S.I. The clinical implication of the number of lymph nodes harvested during sentinel lymph node biopsy and its effects on survival outcome in patients with node-negative breast cancer. Am. J. Surg. 2016;214:726–732. doi: 10.1016/j.amjsurg.2016.10.019.
    1. Stenmark Tullberg A., Lundstedt D., Olofsson Bagge R., Karlsson P. Positive sentinel node in luminal A-like breast cancer patients-implications for adjuvant chemotherapy? Acta Oncol. 2019;58:162–167. doi: 10.1080/0284186X.2018.1533647.
    1. Veronesi U., Paganelli G., Viale G., Luini A., Zurrida S., Galimberti V., Intra M., Veronesi P., Robertson C., Maisonneuve P., et al. A Randomized Comparison of Sentinel-Node Biopsy with Routine Axillary Dissection in Breast Cancer. N. Engl. J. Med. 2003;349:546–553. doi: 10.1056/NEJMoa012782.
    1. Krag D.N., Anderson S., Julian T.B., Brown A.M., Harlow S.P., Costantino J.P., Ashikaga T., Weaver D.L., Mamounas E.P., Jalovec L.M., et al. Sentinel-lymph-node resection compared with conventional axillary-lymph-node dissection in clinically node-negative patients with breast cancer: Overall survival findings from the NSABP B-32 randomised phase 3 trial. Lancet Oncol. 2010;11:927–933. doi: 10.1016/S1470-2045(10)70207-2.
    1. Morrow M., Jagsi R., McLeod M.C., Shumway D., Katz S.J. Surgeon Attitudes Toward the Omission of Axillary Dissection in Early Breast Cancer. JAMA Oncol. 2018;4:1511–1516. doi: 10.1001/jamaoncol.2018.1908.
    1. Donker M., van Tienhoven G., Straver M.E., Meijnen P., van de Velde C.J.H., Mansel R.E., Cataliotti L., Westenberg A.H., Klinkenbijl J.H.G., Orzalesi L., et al. Radiotherapy or surgery of the axilla after a positive sentinel node in breast cancer (EORTC 10981-22023 AMAROS): A randomised, multicentre, open-label, phase 3 non-inferiority trial. Lancet Oncol. 2014;15:1303–1310. doi: 10.1016/S1470-2045(14)70460-7.
    1. Boughey J.C., Suman V.J., Mittendorf E.A., Ahrendt G.M., Wilke L.G., Taback B., Leitch A.M., Kuerer H.M., Bowling M., Flippo-Morton T.S., et al. Sentinel lymph node surgery after neoadjuvant chemotherapy in patients with node-positive breast cancer: The ACOSOG Z1071 (Alliance) clinical trial. JAMA. 2013;310:1455–1461. doi: 10.1001/jama.2013.278932.
    1. Stearns V., Ewing C.A., Slack R., Penannen M.F., Hayes D.F., Tsangaris T.N. Sentinel lymphadenectomy after neoadjuvant chemotherapy for breast cancer may reliably represent the axilla except for inflammatory breast cancer. Ann. Surg Oncol. 2002;9:235–242. doi: 10.1007/BF02573060.
    1. Giuliano A.E., Ballman K.V., McCall L., Beitsch P.D., Brennan M.B., Kelemen P.R., Ollila D.W., Hansen N.M., Whitworth P.W., Blumencranz P.W., et al. Effect of Axillary Dissection vs. No Axillary Dissection on 10-Year Overall Survival Among Women With Invasive Breast Cancer and Sentinel Node Metastasis: The ACOSOG Z0011 (Alliance) Randomized Clinical Trial. JAMA. 2017;318:918–926. doi: 10.1001/jama.2017.11470.
    1. Ahmed M., Jozsa F., Baker R., Rubio I.T., Benson J., Douek M. Meta-analysis of tumour burden in pre-operative axillary ultrasound positive and negative breast cancer patients. Breast Cancer Res. Treat. 2017;166:329–336. doi: 10.1007/s10549-017-4405-3. Erratum in 2017, 166, 337.
    1. Caudle A.S., Yang W.T., Krishnamurthy S., Mittendorf E.A., Black D.M., Gilcrease M.Z., Bedrosian I., Hobbs B.P., DeSnyder S.M., Hwang R.F., 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;34:1072–1078. doi: 10.1200/JCO.2015.64.0094.
    1. Dubsky P., Pinker K., Cardoso F., Montagna G., Ritter M., Denkert C., Rubio I.T., de Azambuja E., Curigliano G., Gentilini O., et al. Breast conservation and axillary management after primary systemic therapy in patients with early-stage breast cancer: The Lucerne toolbox. Lancet Oncol. 2021;22:e18–e28. doi: 10.1016/S1470-2045(20)30580-5.
    1. Lucci A., McCall L.M., Beitsch P.D., Whitworth P.W., Reintgen D.S., Blumencranz P.W., Leitch A.M., Saha S., Hunt K.K., Giuliano A.E. Surgical Complications Associated With Sentinel Lymph Node Dissection (SLND) Plus Axillary Lymph Node Dissection Compared With SLND Alone in the American College of Surgeons Oncology Group Trial Z0011. J. Clin. Oncol. 2007;25:3657–3663. doi: 10.1200/JCO.2006.07.4062.
    1. Mansel R.E., Fallowfield L., Kissin M., Goyal A., Newcombe R.G., Dixon J.M., Yiangou C., Horgan K., Bundred N., Monypenny I., et al. Randomized Multicenter Trial of Sentinel Node Biopsy Versus Standard Axillary Treatment in Operable Breast Cancer: The ALMANAC Trial. J. Natl. Cancer Inst. 2006;98:599–609. doi: 10.1093/jnci/djj158.
    1. Verbelen H., Tjalma W., Meirte J., Gebruers N. Long-term morbidity after a negative sentinel node in breast cancer patients. Eur. J. Cancer Care. 2019;28:e13077. doi: 10.1111/ecc.13077.
    1. Verbelen H., Gebruers N., Eeckhout F.-M., Verlinden K., Tjalma W. Shoulder and arm morbidity in sentinel node-negative breast cancer patients: A systematic review. Breast Cancer Res. Treat. 2014;144:21–31. doi: 10.1007/s10549-014-2846-5.
    1. Navalkissoor S., Wagner T., Gnanasegaran G., Buscombe J. SPECT/CT in imaging sentinel nodes. Clin. Transl. Imaging. 2015;3:203–215. doi: 10.1007/s40336-015-0113-3.
    1. Nakagawa M., Morimoto M., Takechi H., Tadokoro Y., Tangoku A. Preoperative diagnosis of sentinel lymph node (SLN) metastasis using 3D CT lymphography (CTLG) Breast Cancer. 2015;23:519–524. doi: 10.1007/s12282-015-0597-8.
    1. Cox K., Taylor-Phillips S., Sharma N., Weeks J., Mills P., Sever A., Lim A., Haigh I., Hashem M., De Silva T., et al. Enhanced pre-operative axillary staging using intradermal microbubbles and contrast-enhanced ultrasound to detect and biopsy sentinel lymph nodes in breast cancer: A potential replacement for axillary surgery. Br. J. Radiol. 2017;91:20170626. doi: 10.1259/bjr.20170626.
    1. Teshome M., Wei C., Hunt K.K., Thompson A., Rodriguez K., Mittendorf E.A. Use of a Magnetic Tracer for Sentinel Lymph Node Detection in Early-Stage Breast Cancer Patients: A Meta-analysis. Ann. Surg. Oncol. 2016;23:1508–1514. doi: 10.1245/s10434-016-5135-1.
    1. Karakatsanis A., Christiansen P.M., Fischer L., Hedin C., Pistioli L., Sund M., Rasmussen N.R., Jørnsgård H., Tegnelius D., Eriksson S., et al. The Nordic SentiMag trial: A comparison of super paramagnetic iron oxide (SPIO) nanoparticles versus Tc(99) and patent blue in the detection of sentinel node (SN) in patients with breast cancer and a meta-analysis of earlier studies. Breast Cancer Res. Treat. 2016;157:281–294. doi: 10.1007/s10549-016-3809-9.
    1. Motomura K., Izumi T., Tateishi S., Tamaki Y., Ito Y., Horinouchi T., Nakanishi K. Superparamagnetic iron oxide-enhanced MRI at 3 T for accurate axillary staging in breast cancer. Br. J. Surg. 2016;103:60–69. doi: 10.1002/bjs.10040.
    1. Karakatsanis A., Hersi A., Pistiolis L., Bagge R.O., Lykoudis P.M., Eriksson S., Wärnberg F., Nagy G., Mohammed I., Sundqvist M., et al. Effect of preoperative injection of superparamagnetic iron oxide particles on rates of sentinel lymph node dissection in women undergoing surgery for ductal carcinoma in situ (SentiNot study) J. Br. Surg. 2019;106:720–728. doi: 10.1002/bjs.11110.
    1. Ahmed M., Purushotham A.D., Douek M. Novel techniques for sentinel lymph node biopsy in breast cancer: A systematic review. Lancet Oncol. 2014;15:e351–e362. doi: 10.1016/S1470-2045(13)70590-4.
    1. Karakatsanis A., Daskalakis K., Stålberg P., Olofsson H., Andersson Y., Eriksson S., Bergkvist L., Wärnberg F. Superparamagnetic iron oxide nanoparticles as the sole method for sentinel node biopsy detection in patients with breast cancer. J. Br. Surg. 2017;104:1675–1685. doi: 10.1002/bjs.10606.
    1. Ahmed M., Baker R., Rubio I.T. Meta-analysis of aberrant lymphatic drainage in recurrent breast cancer. BJS. 2016;103:1579–1588. doi: 10.1002/bjs.10289.
    1. Clough K.B., Nasr R., Nos C., Vieira M., Inguenault C., Poulet B. New anatomical classification of the axilla with implications for sentinel node biopsy. Br. J. Surg. 2010;97:1659–1665. doi: 10.1002/bjs.7217.
    1. Neven A., Mauer M., Hasan B., Sylvester R., Collette L. Sample size computation in phase II designs combining the A’Hern design and the Sargent and Goldberg design. J. Biopharm. Stat. 2020;30:305–321. doi: 10.1080/10543406.2019.1641817.
    1. Bossuyt P.M., Reitsma J.B., Bruns D.E., Gatsonis C.A., Glasziou P.P., Irwig L., Lijmer J.G., Moher D., Rennie D., de Vet H.C.W., et al. For the STARD Group. STARD 2015: An Updated List of Essential Items for Reporting Diagnostic Accuracy Studies. BMJ. 2015;351:h5527. doi: 10.1136/bmj.h5527.
    1. Pilger T.L., Francisco D.F., Candido Dos Reis F.J. Effect of sentinel lymph node biopsy on upper limb function in women with early breast cancer: A systematic review of clinical trials. Eur. J. Surg. Oncol. 2021;30:1497–1506. doi: 10.1016/j.ejso.2021.01.024.
    1. Boughey J.C., Moriarty J.P., Degnim A.C., Gregg M.S., Egginton J.S., Long K.H. Cost modeling of preoperative axillary ultrasound and fine-needle aspiration to guide surgery for invasive breast cancer. Ann. Surg. Oncol. 2010;17:953–958. doi: 10.1245/s10434-010-0919-1.
    1. Turaga K.K., Chau A., Eatrides J.M., Kiluk J.V., Khakpour N., Laronga C., Lee M.C. Selective application of routine preoperative axillary ultrasonography reduces costs for invasive breast cancers. Oncologist. 2011;16:942–948. doi: 10.1634/theoncologist.2010-0373.
    1. Chung A., Gangi A., Amersi F., Zhang X., Guiliano A. Not Performing a Sentinel Node Biopsy for Older Patients with Early-Stage Invasive Breast Cancer. JAMA Surg. 2015;150:683–684. doi: 10.1001/jamasurg.2015.0647.
    1. Ingvar C., Ahlgren J., Emdin S., Lofgren L., Nordander M., Nimeus E., Arnesson L.-G. Long-term outcome of pT1a-b, cN0 breast cancer without axillary dissection or staging: A prospective observational study of 1543 women. Br. J. Surg. 2020;107:1299–1306. doi: 10.1002/bjs.11610.
    1. O’Connell R.L., Rusby J.E., Stamp G.F.W., Conway A., Roche N., Barry P., Khabra K., Bonomi R., Rapisarda I.F., Della Rovere G.Q. Long term results of treatment of breast cancer without axillary surgery–predicting a sound approach? Eur. J. Surg. Oncol. 2016;42:942–948. doi: 10.1016/j.ejso.2016.03.027.
    1. Sentinel Node Vs Observation after Axillary Ultra-souND (SOUND) [(accessed on 18 May 2021)]; Available online: .
    1. Hughes K.S., Schnaper L.A., Bellon J.R., Cirrincione C.T., Berry D.A., McCormick B., Muss H.B., Smith B.L., Hudis C.A., Winer E.P., et al. Lumpectomy plus tamoxifen with or without irradiation in women age 70 years or older with early breast cancer: Long-term follow-up of CALGB 9343. J. Clin. Oncol. 2013;31:2382–2387. doi: 10.1200/JCO.2012.45.2615.
    1. Kunkler I.H., Williams L.J., Jack W.J., Cameron D.A., Dixon J.M., PRIME II Investigators Breast-conserving surgery with or without irradiation in women aged 65 years or older with early breast cancer (PRIME II): A randomised controlled trial. Lancet Oncol. 2015;16:266–273. doi: 10.1016/S1470-2045(14)71221-5.
    1. Wickberg Å., Liljegren G., Killander F., Lindman H., Bjöhle J., Carlberg M., Blomqvist C., Ahlgren J., Villman K. Omitting radiotherapy in women ≥ 65 years with low-risk early breast cancer after breast-conserving surgery and adjuvant endocrine therapy is safe. Eur. J. Surg. Oncol. 2018;44:951–956. doi: 10.1016/j.ejso.2018.04.002.
    1. Kalinsky K., Barlow W.E., Meric-Bernstam F., Gralow J.R., Albain K.S., Hayes D., Lin N., Perez E.A., Goldstein L.J., Chia S., et al. First results from a phase III randomized clinical trial of standard adjuvant endocrine therapy (ET) +/- chemotherapy (CT) in patients (pts) with 1-3 positive nodes, hormone receptor-positive (HR+) and HER2-negative (HER2-) breast cancer (BC) with recurrence score (RS) < 25: SWOG S1007 (RxPonder); Proceedings of the 2020 San Antonio Breast Cancer Virtual Symposium; San Antonio, TX, USA. 8–11 December 2020; Abstract nr GS3-00.
    1. Van Wely B.J., de Wilt J.H., Francissen C., Teerenstra S., Strobbe L.J. Meta-analysis of ultrasound-guided biopsy of suspicious axillary lymph nodes in the selection of patients with extensive axillary tumour burden in breast cancer. Br. J. Surg. 2015;102:159–168. doi: 10.1002/bjs.9663.
    1. Houssami N., Ciatto S., Turner R.M., Cody H.S., 3rd, Macaskill P. Preoperative ultrasound-guided needle biopsy of axillary nodes in invasive breast cancer: Meta-analysis of its accuracy and utility in staging the axilla. Ann. Surg. 2011;254:243–251. doi: 10.1097/SLA.0b013e31821f1564.
    1. Caudle A., Hunt K.K., Kuerer H.M., Meric-Berstein F., Lucci A., Bedrosian I., Babiera G.V., Hwang R.F., Ross M.I., Feig B.W., et al. Multidisciplinary considerations in the implementation of the findings from the American College of Surgeons Oncology Group (ACOSOG) Z0011 study: A practice-changing trial. Ann. Surg. Oncol. 2011;18:2407–2412. doi: 10.1245/s10434-011-1593-7.
    1. [(accessed on 18 May 2021)]; Available online: .
    1. Standard or Comprehensive Radiation Therapy in Treating Patients With Early-Stage Breast Cancer Previously Treated with Chemotherapy and Surgery. [(accessed on 18 May 2021)]; Available online: .
    1. Boughey J.C., Ballman K.V., Le-Petross H.T., McCall L.M., Mittendorf E.A., Ahrendt G.M., Wilke L.G., Taback B., Feliberti E.C., Hunt K.K. 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;263:802–807. doi: 10.1097/SLA.0000000000001375.
    1. Haffty B.G., McCall L.M., Ballman K.V., Buchholz T.A., Hunt K.K., Boughey J.C. Impact of Radiation on Locoregional Control in Women with Node-Positive Breast Cancer Treated with Neoadjuvant Chemotherapy and Axillary Lymph Node Dissection: Results from ACOSOG Z1071 Clinical Trial. Int. J. Radiat. Oncol. Biol. Phys. 2019;105:174–182. doi: 10.1016/j.ijrobp.2019.04.038.
    1. Haffty B.G., McCall L.M., Ballman K.V., McLaughlin S., Jagsi R., Ollila D.W., Hunt K.K., Buchholz T.A., Boughey J.C. Patterns of Local-Regional Management Following Neoadjuvant Chemotherapy in Breast Cancer: Results from ACOSOG Z1071 (Alliance) Int. J. Radiat. Oncol. Biol. Phys. 2016;94:493–502. doi: 10.1016/j.ijrobp.2015.11.005.
    1. Kuemmel S., Heil J., Rueland A., Seiberling C., Harrach H., Schindowski D., Lubitz J., Hellerhoff K., Ankel C., Graßhoff S.T., et al. A Prospective, Multicenter Registry Study to Evaluate the Clinical Feasibility of Targeted Axillary Dissection (TAD) in Node-Positive Breast Cancer Patients. Ann. Surg. 2020 doi: 10.1097/SLA.0000000000004572. [Epub ahead of print]
    1. Kuehn T., Bauerfeind I., Fehm T., Fleige B., Hausschild M., Helms G., Lebeau A., Liedtke C., von Minckwitz G., Nekljudova V., et al. Sentinel-lymph-node biopsy in patients with breast cancer before and after neoadjuvant chemotherapy (SENTINA): A prospective, multicentre cohort study. Lancet Oncol. 2013;14:609–618. doi: 10.1016/S1470-2045(13)70166-9.
    1. Schwentner L., Helms G., Nekljudova V., Ataseven B., Bauerfeind I., Ditsch N., Fehm T., Fleige B., Hauschild M., Heil J., et al. Using ultrasound and palpation for predicting axillary lymph node status following neoadjuvant chemotherapy-Results from the multi-center SENTINA trial. Breast. 2017;31:202–207. doi: 10.1016/j.breast.2016.11.012.
    1. van der Noordaa M.E.M., van Duijnhoven F.H., Cuijpers F.N.E., van Werkhoven E., Wiersma T.G., Elkhuizen P.H.M., Winter-Warnars G., Dezentje V., Sonke G.S., Groen E.J., et al. Toward omitting sentinel lymph node biopsy after neoadjuvant chemotherapy in patients with clinically node-negative breast cancer. Br. J. Surg. 2020;108:667–674. doi: 10.1002/bjs.12026.
    1. Reimer T., Glass A., Botteri E., Loibl S., DGentilini O. Avoiding Axillary Sentinel Lymph Node Biopsy after Neoadjuvant Systemic Therapy in Breast Cancer: Rationale for the Prospective, Multicentric EUBREAST-01 Trial. Cancers. 2020;12:3698. doi: 10.3390/cancers12123698.
    1. Lee M.C., Gonzalez S.J., Lin H., Zhao X., Kiluk J.V., Laronga C., Mooney B. Prospective trial of breast MRI versus 2D and 3D ultrasound for evaluation of response to neoadjuvant chemotherapy. Ann. Surg. Oncol. 2015;22:2888–2894. doi: 10.1245/s10434-014-4357-3.
    1. Marinovich M.L., Macaskill P., Irwig L., Sardanelli F., von Minckwitz G., Mamounas E., Brennan M., Ciatto S., Houssami N. Meta-analysis of agreement between MRI and pathologic breast tumour size after neoadjuvant chemotherapy. Br. J. Cancer. 2013;109:1528–1536. doi: 10.1038/bjc.2013.473.
    1. Sheikhbahaei S., Trahan T.J., Xiao J., Taghipour M., Mena E., Connolly R.M., Subramaniam R.M. FDG-PET/CT and MRI for Evaluation of Pathologic Response to Neoadjuvant Chemotherapy in Patients With Breast Cancer: A Meta-Analysis of Diagnostic Accuracy Studies. Oncologist. 2016;21:931–939. doi: 10.1634/theoncologist.2015-0353.
    1. Chen L., Yang Q., Bao J., Liu D., Huang X., Wang J. Direct comparison of PET/CT and MRI to predict the pathological response to neoadjuvant chemotherapy in breast cancer: A meta-analysis. Sci. Rep. 2017;7:8479. doi: 10.1038/s41598-017-08852-8.
    1. Ugras S., Matsen C., Eaton A., Stempel M., Morrow M., Cody H.S., 3rd Reoperative Sentinel Lymph Node Biopsy is Feasible for Locally Recurrent Breast Cancer, But is it Worthwhile? Ann. Surg. Oncol. 2016;23:744–748. doi: 10.1245/s10434-015-5003-4.
    1. Vugts G., Maaskant-Braat A.J., Voogd A.C., van Riet Y.E., Luiten E.J., Rutgers E.J., Rutten H.J., Roumen R.M., Nieuwenhuijzen G.A. Repeat sentinel node biopsy should be considered in patients with locally recurrent breast cancer. Breast Cancer Res. Treat. 2015;153:549–556. doi: 10.1007/s10549-015-3571-4.
    1. Kuemmel S., Holtschmidt J., Gerber B., Von der Assen A., Heil J., Thill M., Krug D., Schem C., Denkert C., Lubitz J., et al. Prospective, Multicenter, Randomized Phase III Trial Evaluating the Impact of Lymphoscintigraphy as Part of Sentinel Node Biopsy in Early Breast Cancer: SenSzi (GBG80) Trial. J. Clin. Oncol. 2019;37:1490–1498. doi: 10.1200/JCO.18.02092.
    1. Motomura K., Izumi T., Tateishi S., Sumino H., Noguchi A., Horinouchi T., Nakanishi K. Correlation between the area of high-signal intensity on SPIO-enhanced MR imaging and the pathologic size of sentinel node metastases in breast cancer patients with positive sentinel nodes. BMC Med. Imaging. 2013;13:32. doi: 10.1186/1471-2342-13-32.

Source: PubMed

赞助者和合作者

医疗条件

药物干预

3
订阅