Electrical lymph node scanning (ELS) system for real-time intra-operative detection of involved axillary lymph nodes in adjuvant breast cancer patients.
Breast cancer surgery
Electrical impedance spectroscopy (EIS)
Impedance phase slope (IPS)
Nodal staging
Pathology
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
05 06 2024
05 06 2024
Historique:
received:
18
09
2023
accepted:
07
05
2024
medline:
6
6
2024
pubmed:
6
6
2024
entrez:
5
6
2024
Statut:
epublish
Résumé
Lymph node (LN) status is an essential prognostic factor in breast cancer (BC) patients, with an important role in the surgical and therapeutic plan. Recently, we have been developed a novel system for real-time intra-operative electrical LN scanning in BC patients. The ELS scores were calibrated by pathological evaluation of the LNs. Herein, we evaluated the efficacy of ELS in a prospective study for non-chemo-treated breast cancer patients. This is a prospective study in which ELS scores are blind for pathologists who declare the clearance or involvement of LNs based on permanent pathology as the gold standard. ELS and frozen-section (FS) pathology results were achieved intra-operatively, and samples were sent for the permanent pathology. The score of ELS did not affect the surgeons' decision, and the treatment approach was carried out based on FS pathology and pre-surgical data, such as imaging and probable biopsies. Patients were recruited from October 2021 through November 2022, and 381 lymph nodes of 97 patients were included in the study. In this study we recruited 38 patients (39.2%) with sentinel lymph node biopsy (SLNB) and 59 patients (60.8%) with ALND. Of the 381 LNs scored by ELS, 329 sentinel LNs underwent routine pathology, while others (n = 52) underwent both FS and permanent pathology. ELS showed a sensitivity of 91.4% for node-positive patients, decreasing to 84.8% when considering all LNs. Using ROC analysis, ELS diagnosis showed a significant AUC of 0.878 in relation to the permanent pathology gold standard. Comparison of ELS diagnosis for different tumor types and LN sizes demonstrated no significant differences, while increasing LN size correlated with enhanced ELS sensitivity. This study confirmed ELS's efficacy in real-time lymph node detection among non-chemo-treated breast cancer patients. The use of ELS's pathological scoring for intra-operative LN diagnosis, especially in the absence of FS pathology or for non-sentinel LN involvement, could improve prognosis and reduce complications by minimizing unnecessary dissection.
Identifiants
pubmed: 38839807
doi: 10.1038/s41598-024-61600-7
pii: 10.1038/s41598-024-61600-7
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
12900Informations de copyright
© 2024. The Author(s).
Références
Li, N. et al. Global burden of breast cancer and attributable risk factors in 195 countries and territories, from 1990 to 2017: Results from the Global Burden of Disease Study 2017. J. Hematol. Oncol. 12(1), 1–12 (2019).
doi: 10.1186/s13045-019-0828-0
Miripour, Z. S. et al. Electrochemical therapy (EChT) of cancer tumor with an external anode, a way to achieve pathological complete response. Med. Oncol. 40(4), 117 (2023).
pubmed: 36928512
doi: 10.1007/s12032-023-01979-x
Abdolahad, M. & Kaviani, A. Real-time detection of cellular metabolism: A new trend for intra-operative diagnosis of cavity margins: Intraoperative CDP. Arch. Breast Cancer 10(1), 1–3 (2023).
doi: 10.32768/abc.20231011-3
Saadati, F. et al. Cold physical plasma toxicity in breast and oral squamous carcinoma in vitro and in patient-derived cancer tissue ex vivo. Appl. Sci. 13(11), 6472 (2023).
doi: 10.3390/app13116472
Dubsky, P. et al. Breast conservation and axillary management after primary systemic therapy in patients with early-stage breast cancer: The Lucerne toolbox. Lancet Oncol. 22(1), e18–e28 (2021).
pubmed: 33387500
doi: 10.1016/S1470-2045(20)30580-5
Hotton, J. et al. Pre-operative axillary ultrasound with fine-needle aspiration cytology performance and predictive factors of false negatives in axillary lymph node involvement in early breast cancer. Breast Cancer Res. Treat. 183, 639–647 (2020).
pubmed: 32737710
doi: 10.1007/s10549-020-05830-z
Fujii, T. et al. Significance of lymphatic invasion combined with size of primary tumor for predicting sentinel lymph node metastasis in patients with breast cancer. Anticancer Res. 35(6), 3581–3584 (2015).
pubmed: 26026130
Sandoughdaran, S., Malekzadeh, M. & Akbari, M. E. Frequency and predictors of axillary lymph node metastases in Iranian women with early breast cancer. Asian Pac. J. Cancer Prev. APJCP 19(6), 1617 (2018).
pubmed: 29936787
Ayana, G., Dese, K. & Choe, S.-W. Transfer learning in breast cancer diagnoses via ultrasound imaging. Cancers 13(4), 738 (2021).
pubmed: 33578891
pmcid: 7916666
doi: 10.3390/cancers13040738
Moschetta, M. et al. Comparison between fine needle aspiration cytology (FNAC) and core needle biopsy (CNB) in the diagnosis of breast lesions. Il Giornale Chir. 35(7–8), 171 (2014).
Rana, M. K., Rana, A. P. S., Sharma, U., Barwal, T. S. & Jain, A. Evolution of frozen section in carcinoma breast: Systematic review. Int. J. Breast Cancer 2022, 1–7 (2022).
doi: 10.1155/2022/4958580
Reimer, T. Omission of axillary sentinel lymph node biopsy in early invasive breast cancer. Breast 67, 124–128 (2023).
pubmed: 36658052
pmcid: 9982316
doi: 10.1016/j.breast.2023.01.002
Gatzemeier, W. & Mann, G. B. Which sentinel lymph-node (SLN) positive breast cancer patient needs an axillary lymph-node dissection (ALND)–ACOSOG Z0011 results and beyond. Breast 22(3), 211–216 (2013).
pubmed: 23478200
doi: 10.1016/j.breast.2013.02.001
Javadi, S. et al. Less axillary lymphadenectomy is more beneficial: 27-year Follow-up of patients with breast cancer. Int. J. Cancer Manag. 14(2), 171–176 (2021).
doi: 10.5812/ijcm.108538
Zheng, Q. et al. Long-term survival after sentinel lymph node biopsy or axillary lymph node dissection in pN0 breast cancer patients: a population-based study. Breast Cancer Res. Treat. 196(3), 613–622 (2022).
pubmed: 36207619
doi: 10.1007/s10549-022-06746-6
Houssami, N., Diepstraten, S. C., Cody, H. S., Turner, R. M. & Sever, A. R. Clinical utility of ultrasound-needle biopsy for preoperative staging of the axilla in invasive breast cancer. Anticancer Res. 34(3), 1087–1097 (2014).
pubmed: 24596347
Yoshihara, E. et al. Predictors of axillary lymph node metastases in early breast cancer and their applicability in clinical practice. Breast 22(3), 357–361 (2013).
pubmed: 23022046
doi: 10.1016/j.breast.2012.09.003
McLaughlin, S. A. et al. Prevalence of lymphedema in women with breast cancer 5 years after sentinel lymph node biopsy or axillary dissection: Objective measurements. J. Clin. Oncol. 26(32), 5213 (2008).
pubmed: 18838709
pmcid: 2652091
doi: 10.1200/JCO.2008.16.3725
Žatecký, J. et al. Level I axillary dissection in patients with breast cancer and tumor-involved sentinel lymph node after NAC is not sufficient for adequate nodal staging. Turk. J. Surg. 39(1), 1 (2023).
pubmed: 37275927
pmcid: 10234716
doi: 10.47717/turkjsurg.2023.5984
Panellists, C. Advanced Breast Cancer Sixth International Consensus Conference (ABC6).
Purushotham, A. D. et al. Morbidity after sentinel lymph node biopsy in primary breast cancer: Results from a randomized controlled trial. J. Clin. Oncol. 23(19), 4312–4321 (2005).
pubmed: 15994144
doi: 10.1200/JCO.2005.03.228
Feggi, L. et al. An original approach in the diagnosis of early breast cancer: Use of the same radiopharmaceutical for both non-palpable lesions and sentinel node localisation. Eur. J. Nucl. Med. 28, 1589–1596 (2001).
pubmed: 11702098
doi: 10.1007/s002590100601
Svoboda, R. M., Prado, G., Mirsky, R. S. & Rigel, D. S. Assessment of clinician accuracy for diagnosing melanoma on the basis of electrical impedance spectroscopy score plus morphology versus lesion morphology alone. J. Am. Acad. Dermatol. 80(1), 285–287 (2019).
pubmed: 30227189
doi: 10.1016/j.jaad.2018.08.048
Vasudeva, S. & Thapa, R. Colloseum to estimate the accuracy of detection of cervical intraepithelial neoplasia using electrical impedance spectroscopy with colposcopy-A one year study. Indian J. Obstet. Gynecol. Res. 8(2), 166–171 (2021).
doi: 10.18231/j.ijogr.2021.037
Årsvold, A. T., Zeltner, A. S., Cheng, Z., Schwaner, K. L., Jensen, P. T., & Savarimuthu, T. R. (eds.) Lymph node detection using robot assisted electrical impedance scanning and an artificial neural network. In 2021 International Symposium on Medical Robotics (ISMR) (IEEE, 2021).
Mentzel, H.-J. et al. Electrical impedance scanning—Application of this new technique for lymph node evaluation in children. Pediatr. Radiol. 33, 461–466 (2003).
pubmed: 12728287
doi: 10.1007/s00247-003-0930-9
Malich, A. et al. Electrical impedance scanning of lymph nodes: Initial clinical and technical findings. Clin. Radiol. 57(7), 579–586 (2002).
pubmed: 12096855
doi: 10.1053/crad.2001.0927
Kashihara, T., Zablocki, D. & Sadoshima, J. YAP-dependent metabolic remodeling in local lymph node boosts the function of cancer cells. Biotarget 3, 14 (2019).
pubmed: 31511850
pmcid: 6738959
doi: 10.21037/biotarget.2019.08.01
Comen, E. A., Norton, L. & Massagué, J. Breast cancer tumor size, nodal status, and prognosis: Biology trumps anatomy. J. Clin. Oncol. 29(19), 2610–2612 (2011).
pubmed: 21606411
doi: 10.1200/JCO.2011.36.1873
Beheshti Firoozabadi, J. et al. Intraoperative assessment of high-risk thyroid nodules based on electrical impedance measurements: A feasibility study. Diagnostics 12(12), 2950 (2022).
pubmed: 36552958
pmcid: 9776834
doi: 10.3390/diagnostics12122950
Mahdavi, R. et al. Bioelectrical pathology of the breast; Real-time diagnosis of malignancy by clinically calibrated impedance spectroscopy of freshly dissected tissue. Biosens. Bioelectron. 165, 112421 (2020).
pubmed: 32729539
doi: 10.1016/j.bios.2020.112421
Mahdavi, R. et al. Intraradiological pathology-calibrated electrical impedance spectroscopy in the evaluation of excision-required breast lesions. Med. Phys. 49(4), 2746–2760 (2022).
pubmed: 35107181
doi: 10.1002/mp.15481
Mamou, J. et al. Three-dimensional high-frequency characterization of cancerous lymph nodes. Ultrasound Med. Biol. 36(3), 361–375 (2010).
pubmed: 20133046
pmcid: 2826510
doi: 10.1016/j.ultrasmedbio.2009.10.007
Hong, Y. T., Yun, J., Lee, J. H. & Hong, K.-H. Smart needle to diagnose metastatic lymph node using electrical impedance spectroscopy. Auris Nasus Larynx 48(2), 281–287 (2021).
pubmed: 33288360
doi: 10.1016/j.anl.2020.08.011
Zandi, A. et al. The design and fabrication of nanoengineered platinum needles with laser welded carbon nanotubes (CNTs) for the electrochemical biosensing of cancer lymph nodes. Biomater. Sci. 9(18), 6214–6226 (2021).
pubmed: 34357368
doi: 10.1039/D1BM00875G
Uygun, Z. O., Yeniay, L. & Sağın, F. G. CRISPR-dCas9 powered impedimetric biosensor for label-free detection of circulating tumor DNAs. Anal. Chim. Acta 1121, 35–41 (2020).
pubmed: 32493587
doi: 10.1016/j.aca.2020.04.009
Lin, Y.-C. et al. Identifying good prognosis group of breast cancer patients with 1–3 positive axillary nodes for adjuvant cyclophosphamide, methotrexate and 5-fluorouracil (CMF) chemotherapy. Jpn. J. Clin. Oncol. 35(9), 514–519 (2005).
pubmed: 16199422
doi: 10.1093/jjco/hyi143
Mahdavi, R. et al. Intraoperative pathologically-calibrated diagnosis of lymph nodes involved by breast cancer cells based on electrical impedance spectroscopy; A prospective diagnostic human model study. Int. J. Surg. 96, 106166 (2021).
pubmed: 34768024
doi: 10.1016/j.ijsu.2021.106166
Ersoy, E. et al. Intraoperative lymph node assessment (touch preparation only) for metastatic breast carcinoma in neoadjuvant and non-neoadjuvant settings. Arch. Pathol. Lab. Med. 147(2), 149–158 (2023).
pubmed: 35512225
doi: 10.5858/arpa.2021-0520-OA
Bakri, N. A. C. et al. Impact of axillary lymph node dissection and sentinel lymph node biopsy on upper limb morbidity in breast cancer patients: A systematic review and meta-analysis. Ann. Surg. 277(4), 572 (2023).
doi: 10.1097/SLA.0000000000005671
Rahim, M. K. et al. Dynamic CD8+ T cell responses to cancer immunotherapy in human regional lymph nodes are disrupted in metastatic lymph nodes. Cell 186(6), 1127–1143 (2023).
pubmed: 36931243
pmcid: 10348701
doi: 10.1016/j.cell.2023.02.021
Reticker-Flynn, N. E. & Engleman, E. G. Lymph nodes: At the intersection of cancer treatment and progression. Trends Cell Biol. 33, 1021–1034 (2023).
pubmed: 37149414
doi: 10.1016/j.tcb.2023.04.001
Fransen, M. F., van Hall, T. & Ossendorp, F. Immune checkpoint therapy: Tumor draining lymph nodes in the spotlights. Int. J. Mol. Sci. 22(17), 9401 (2021).
pubmed: 34502307
pmcid: 8431673
doi: 10.3390/ijms22179401
Van Pul, K. M., Fransen, M. F., Van de Ven, R. & De Gruijl, T. D. Immunotherapy goes local: The central role of lymph nodes in driving tumor infiltration and efficacy. Front. Immunol. 12, 518 (2021).
Koehler, K. & Ohlinger, R. Sensitivity and specificity of preoperative ultrasonography for diagnosing nodal metastases in patients with breast cancer. Ultraschall Med. Eur. J. Ultrasound 32, 393–399 (2010).
doi: 10.1055/s-0029-1245505
Zhang, H., Sui, X., Zhou, S., Hu, L. & Huang, X. Correlation of conventional ultrasound characteristics of breast tumors with axillary lymph node metastasis and Ki-67 expression in patients with breast cancer. J. Ultrasound Med. 38(7), 1833–1840 (2019).
pubmed: 30480840
doi: 10.1002/jum.14879
Nair, N. S. et al. Accuracy of intraoperative frozen section analysis of lymph nodes in women undergoing axillary sampling for treatment of breast cancer: Single institution audit. Clin. Breast Cancer 23, e420 (2023).
pubmed: 37460382
doi: 10.1016/j.clbc.2023.06.010
Namdar, Z. M. et al. How accurate is frozen section pathology compared to permanent pathology in detecting involved margins and lymph nodes in breast cancer?. World J. Surg. Oncol. 19(1), 1–7 (2021).
doi: 10.1186/s12957-021-02365-5
DiNardo, L. J., Lin, J., Karageorge, L. S. & Powers, C. N. Accuracy, utility, and cost of frozen section margins in head and neck cancer surgery. Laryngoscope 110(10), 1773–1776 (2000).
pubmed: 11037842
doi: 10.1097/00005537-200010000-00039
Yuan, Q. et al. Identification and preservation of arm lymphatic system in axillary dissection for breast cancer to reduce arm lymphedema events: A randomized clinical trial. Ann. Surg. Oncol. 26, 3446–3454 (2019).
pubmed: 31240591
doi: 10.1245/s10434-019-07569-4
Elliott, R. M., Shenk, R. R., Thompson, C. L. & Gilmore, H. L. Touch preparations for the intraoperative evaluation of sentinel lymph nodes after neoadjuvant therapy have high false-negative rates in patients with breast cancer. Arch. Pathol. Lab. Med. 138(6), 814–818 (2014).
pubmed: 24878021
doi: 10.5858/arpa.2013-0281-OA
Guidroz, J. A., Johnson, M. T., Scott-Conner, C. E., De Young, B. R. & Weigel, R. J. The use of touch preparation for the evaluation of sentinel lymph nodes in breast cancer. Am. J. Surg. 199(6), 792–796 (2010).
pubmed: 19954770
doi: 10.1016/j.amjsurg.2009.06.020
Ohashi, R. et al. Diagnostic value of fine needle aspiration and core needle biopsy in special types of breast cancer. Breast Cancer 23, 675–683 (2016).
pubmed: 26134558
doi: 10.1007/s12282-015-0624-9
Cocco, D. et al. Invasive lobular breast cancer: Data to support surgical decision making. Ann. Surg. Oncol. 28, 5723–5729 (2021).
pubmed: 34324111
doi: 10.1245/s10434-021-10455-7
Verheuvel, N., Ooms, H., Tjan-Heijnen, V., Roumen, R. & Voogd, A. Predictors for extensive nodal involvement in breast cancer patients with axillary lymph node metastases. Breast 27, 175–181 (2016).
pubmed: 27123958
doi: 10.1016/j.breast.2016.02.006
Malter, W. et al. Factors predictive of sentinel lymph node involvement in primary breast cancer. Anticancer Res. 38(6), 3657–3662 (2018).
pubmed: 29848724
doi: 10.21873/anticanres.12642
Cornwell, L. B., Mcmasters, K. M. & Chagpar, A. B. The impact of lymphovascular invasion on lymph node status in patients with breast cancer. Am. Surg. 77(7), 874–877 (2011).
pubmed: 21944350
doi: 10.1177/000313481107700722
Wang, W. & Dong, H. A commentary on" Intraoperative pathologically-calibrated diagnosis of lymph nodes involved by breast cancer cells based on electrical impedance spectroscopy; a prospective diagnostic human model study"(Int J Surg 2021; 96: 106166). Int. J. Surg. 104, 106771 (2022).
pubmed: 35863625
doi: 10.1016/j.ijsu.2022.106771