Transcutaneous contrast-enhanced sonography for diagnosis of sentinel lymph nodes in early breast cancer
https://doi.org/10.17650/2782-3202-2024-4-4-111-118
Abstract
Disease stage and especially condition of the sentinel lymph node (SLN) assessed in patients with breast cancer prior to treatment are among the most important prognostic factors. SLN is the first lymph node in the regional lymph node system receiving lymph outflow from the primary tumor. SLN biopsy with blue dye gradually replaced traditional axillary lymph node dissection as the standard of treatment of early breast cancer. In the recent years, technique of contrast-enhanced sonography with microbubble contrast agents for examination of the lymph system has been studied both in animal and human trials.
Aim of the review is to investigate the effectiveness of transcutaneous contrast-enhanced sonography of the SLN for biopsy and for diagnosis of metastatic SLNs using methylene blue as the standard in patients with early breast cancer.
About the Authors
G. G. KhakimovaUzbekistan
Gulnoz Golibovna Khakimova
1 Bogiston St., Tashkent, 100070
223 Bogishamol St., Tashkent, 100140
I. V. Reshetov
Russian Federation
Bld. 2, 8 Trubetskaya St., Moscow, 119991
Bld. 2, 11 Rossolimo St., Moscow, 119021
A. D. Zikiryakhodzhaev
Russian Federation
3 2ndBotkinskiy Proezd, Moscow, 125284
Bld. 2, 8 Trubetskaya St., Moscow, 119991
6 Miklukho-Maklaya St., Moscow, 117198
M. V. Starkova
Russian Federation
3 2ndBotkinskiy Proezd, Moscow 125284
Sh. G. Khakimova
Russian Federation
Bld. 2, 11 Rossolimo St., Moscow 119021
3 2ndBotkinskiy Proezd, Moscow 125284
V. O. Timoshkin
Russian Federation
3 2ndBotkinskiy Proezd, Moscow 125284
References
1. The state of cancer care for the population of Russia in 2022. Ed. by A.D. Kaprin, V.V. Starinsky, A.O. Shakhzadova. Moscow: MNIOI im. P.A. Gertsena - filial FGBU “NMITS radiologii” Minzdrava Rossii, 2022. (In Russ.).
2. Sung H., Ferlay J., Siegel R.L. et al. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 2021;71(3):209-49. DOI: 10.3322/caac.21660
3. The state of cancer care for the population of Russia in 2021. Ed. by A.D. Kaprin, V.V. Starinsky, A.O. Shakhzadova. Moscow: MNIOI im. P.A. Gertsena - filial FGBU “NMITS radiologii” Minzdrava Rossii, 2022. (In Russ.).
4. Bosieva A.R., Ermoshchenkova M.V., Volchenko N.N., Zikiryahodjaev A.D. Breast-conserving surgery after neoadjuvant chemotherapy in breast cancer patients. Sibirskiy onkologicheskiy zhurnal = Siberian Journal of Oncology 2021;20(4):116-21. (In Russ.). DOI: 10.21294/1814-4861-2021-20-4-116-121
5. Rasskazova E.A., Zikiryakhodzhaev A.D. Organ-sparing and oncoplastic resections for breast cancer. Modern tendencies. Onkologiya. Zhurnal im. P.A. Hertsena = P.A. Herzen Journal of Oncology 2022;11(5):65-9. (In Russ.). DOI: 10.17116/onkolog20221105165
6. Breast cancer. Ed. by D.A. Ryabchikov, A.V. Petrovsky. Moscow: GEOTAR-Media, 2023. 400 p. (In Russ.).
7. Fisher B., Redmond C., Poisson R. et al. Eight-year results of a randomized clinical trial comparing total mastectomy and lumpectomy with or without irradiation in the treatment of breast cancer. N Engl J Med 1989;320(13):822-8. DOI: 10.1056/NEJM198903303201302
8. Fisher B., Anderson S., Bryant J. et al. Twenty-year follow-up of a randomized trial comparing total mastectomy, lumpectomy, and lumpectomy plus irradiation for the treatment of invasive breast cancer. New Engl J Med 2002;347(16):1233-41. DOI: 10.1056/NEJMoa022152
9. Veronesi U., Saccozzi R., Del Vecchio M. et al. Comparing radical mastectomy with quadrantectomy, axillary dissection, and radiotherapy in patients with small cancers of the breast. N Engl J Med 1981;305(1): 6-11. DOI: 10.1056/NEJM198107023050102
10. Veronesi U., Cascinelli N., Mariani L. et al. Twenty-year follow-up of a randomized study comparing breast-conserving surgery with radical mastectomy for early breast cancer. New Engl J Med 2002;16(347):1227-32. DOI: 10.1056/NEJMoa020989
11. Krishnamurthy S., Sneige N., Bedi D.G. et al. Role of ultrasound-guided fine-needle aspiration of indeterminate and suspicious axillary lymph nodes in the initial staging of breast carcinoma. Cancer 2002;95(5):982-8. DOI: 10.1002/cncr.10786
12. Oruwari J.U., Chung M.A., Koelliker S. et al. Axillary staging using ultrasound-guided fine needle aspiration biopsy in locally advanced breast cancer. Am J Surg 2002;184(4):307-9. DOI: 10.1016/s0002-9610(02)00957-1
13. Zikiryakhodzhaev A.D., Grushina T.I., Starkova M.V. et al. Methods for sentinel lymph node detection in patients with breast cancer. Sibirskiy onkologicheskiy zhurnal = Siberian Journal of Oncology 2020;19(5):88-96. (In Russ.). DOI: 10.21294/1814-4861-2020-19-5-88-96
14. Fisher B., Bauer M., Wickerham D.L. et al. Relation of number of positive axillary nodes to the prognosis of patients with primary breast cancer. An NSABP update. Cancer 1983;52(9):1551-7. DOI: 10.1002/1097-0142(19831101)52:93.0.co;2-3.
15. Manca G., Volterrani D., Mazzarri S. et al. Sentinel lymph node mapping in breast cancer: a critical reappraisal of the internal mammary chain issue. Q J Nucl Med Mol Imaging 2014;58(2):114-26.
16. Krag D., Weaver D., Ashikaga T. et al. The sentinel node in breast cancer-a multicenter validation study. N Engl J Med 1998;339(14):941-6. DOI: 10.1056/NEJM199810013391401
17. Goldberg B.B., Merton D.A., Liu J.B. et al. Sentinel lymph nodes in a swine model with melanoma: contrast-enhanced lymphatic US. Radiology 2004;230(3):727-34. DOI: 10.1148/radiol.2303021440
18. Sever A.R., Mills P., Jones S.E. et al. Sentinel node identification using microbubbles and contrast-enhanced ultrasonography Clin Radiol 2012;67(7):687-94. DOI: 10.1016/j.crad.2011.11.009
19. Ultrasonic scanners. Available by: https://sonoscan.ru (Date of access 06.09.2024). (In Russ.).
20. Wang Y., Zhou W., Li C. et al. Variation of sentinel lymphatic channels (SLCs) and sentinel lymph nodes (SLNs) assessed by contrast-enhanced ultrasound (CEUS) in breast cancer patients. World J Surg Oncol 2017;15(1):127. DOI: 10.1186/s12957-017-1195-3
21. Shimazu K., Miyake T., Tanei T. et al. Real-time visualization of lymphatic flow to sentinel lymph nodes by contrast-enhanced ultrasonography with sonazoid in patients with breast cancer. Ultrasound Med Biol 2019;45(10):2634-40. DOI: 10.1016/j.ultrasmedbio.2019.07.005
22. Xie F., Zhang D., Cheng L. et al. Intradermal microbubbles and contrast-enhanced ultrasound (CEUS) is a feasible approach for sentinel lymph node identification in early-stage breast cancer. World J Surg Oncol 2015;13:319. DOI: 10.1186/s12957-015-0736-x
23. Hong Y.R. et al. Application of contrast-enhanced ultrasonography in differential diagnosis of superficial lymph node disease. Chinese J Ultrasound Imag 2006;15(11);849-52.
24. Nielsen Moody A., Bull J., Culpan A.M. et al. Preoperative sentinel lymph node identification, biopsy and localisation using contrast enhanced ultrasound (CEUS) in patients with breast cancer: a systematic review and meta-analysis Clin Radiol 2017;72(11): 959-71. DOI: 10.1016/j.crad.2017.06.121
25. Chang E.H. An introduction to contrast-enhanced ultrasound for nephrologists. Nephron 2018;138(3):176-85. DOI: 10.1159/000484635
26. Greis C. Technology overview: SonoVue (Bracco, Milan). Eur Radiol 2004;14(Suppl 8):P11-5.
27. Sidhu P.S., Choi B.I., Nielsen M.B. The EFSUMB Guidelines on the Non-Hepatic Clinical Applications of Contrast Enhanced Ultrasound (CEUS): a new dawn for the escalating use of this ubiquitous technique. Ultraschall Med 2012;33(1):5-7. DOI: 10.1055/s-0031-1299141
28. Sun Y., Cui L., Wang S. et al. Comparative study of two contrast agents for intraoperative identification of sentinel lymph nodes in patients with early breast cancer. Gland Surg 2021;10(5):1638-45. DOI: 10.21037/gs-21-87
29. He M., Zhu L., Huang M. et al. Comparison between SonoVue and Sonazoid contrast-enhanced ultrasound in characterization of focal nodular hyperplasia smaller than 3cm. J Ultrasound Med 2021;40(10):2095-104. DOI: 10.1002/jum.15589
30. Yang S., Tang K., Tao J. et al. Diagnostic effect of subcutaneous injection of ultrasound contrast agent on sentinel lymph nodes of breast cancer. Chin J Clin Oncol Rehabil 2017;24:10-13.
31. Guo K., Zhong F., Cai Z. et al. Comparison of the effects of subcutaneous and areola injection of contrast agent to locate sentinel lymph nodes in breast cancer. J Clin Exp Med 2018;17:2450-3.
32. Sever A.R., Mills P., Jones S.E. et al. Preoperative sentinel node identification with ultrasound using microbubbles in patients with breast cancer. AJR Am J Roentgenol 2011;196(2):251-6. DOI: 10.2214/AJR.10.4865
33. Omoto K., Matsunaga H., Take N. et al. Sentinel node detection method using contrast-enhanced ultrasonography with sonazoid in breast cancer: preliminary clinical study. Ultrasound Med Biol 2009;35(8):1249-56. DOI: 10.1016/j.ultrasmedbio.2009.02.004
34. Machado P., Stanczak M., Liu J.B. et al. Subdermal ultrasound contrast agent injection for sentinel lymph node identification: an analysis of safety and contrast agent dose in healthy volunteers. J Ultrasound Med 2018;37(7):1611-20. DOI: 10.1002/jum.14502
35. Wu X., Tang L., Huang W. et al. Contrast-enhanced ultrasonography and blue dye methods in detection of sentinel lymph nodes following neoadjuvant chemotherapy in initially node positive breast cancer. Arch Gynecol Obstet 2020;302(3):685-92. DOI: 10.1007/s00404-020-05646-8
36. Liu J., Liu X., He J. et al. Percutaneous contrast-enhanced ultrasound for localization and diagnosis of sentinel lymph node in early breast cancer. Sci Rep 2019;9(1):13545. DOI: 10.1038/s41598-019-49736-3
37. Iwamoto N., Aruga T., Asami H., Horiguchi S.I. False-negative ultrasound-guided fine-needle aspiration of axillary lymph nodes in breast cancer patients. Cytopathology 2020;31(5):463-7. DOI: 10.1111/cyt.12877
38. Dutta S.W., Volaric A., Morgan J.T. et al. Pathologic evaluation and prognostic implications of nodal micrometastases in breast cancer. Semin Radiat Oncol 2019;29(2):102-10. DOI: 10.1016/j.semradonc.2018.11.001
39. Hetterich M., Gerken M., Ortmann O. et al. Adjuvant chemotherapy for breast cancer patients with axillary lymph node micrometastases. Breast Cancer Res Treat 2021;187(3):715-27. DOI: 10.1007/s10549-021-06162-2
40. Chen X.M., Zhong J.Y., Hu Z.M. et al. Trans-lymphatic contrastenhanced ultrasound in combination with blue dye injection is feasible for detection and biopsy of sentinel lymph nodes in breast cancer. Adv Ultrasound Diagnosis Ther 2018;2:94-100.
41. Shimazu K., Ito T., Uji K. et al. Identification of sentinel lymph nodes by contrast-enhanced ultrasonography with Sonazoid in patients with breast cancer: a feasibility study in three hospitals. Cancer Med 2017;6(8):1915-2. DOI: 10.1002/cam4.1142
42. Aoki T., Moriyasu F., Yamamoto K. et al. Image of tumor metastasis and inflammatory lymph node enlargement by contrast-enhanced ultrasonography. World J Radiol 2011;3(12):298-305. DOI: 10.4329/wjr.v3.i12.298
43. Li P., Sun D. Advanced diagnostic imaging of sentinel lymph node in early stage breast cancer. J Clin Ultrasound 2022;50(3):415-21. DOI: 10.1002/jcu.23151.
Review
For citations:
Khakimova G.G., Reshetov I.V., Zikiryakhodzhaev A.D., Starkova M.V., Khakimova Sh.G., Timoshkin V.O. Transcutaneous contrast-enhanced sonography for diagnosis of sentinel lymph nodes in early breast cancer. MD-Onco. 2024;4(4):111-118. (In Russ.) https://doi.org/10.17650/2782-3202-2024-4-4-111-118