Intraoperative lymphography with indocyanine green experience in liver resection planning in patients with biliary cancer
https://doi.org/10.17709/2410-1893-2025-12-4-4
EDN: TIAPIQ
Abstract
Purpose of the study was to evaluate the feasibility of intraoperative lymphography with indocyanine green in cholangiocarcinoma and gallbladder cancer.
Patients and methods. The study included 26 patients with biliary cancer, who underwent intraoperative fluorescent lymphography with indocyanine green (ICG lymphography) during the period from April 2023 to January 2025 while planning lymph node (LN) dissection and liver resection. The lymph drainage from the liver and bile ducts was studied at 1, 3, 5, 10, 15, 30 ± 45 minutes from the ICG introduction with the determination of the first three stained LNs – sentinel lymph nodes (SLNs) – followed by subsequent LN dissection with the removal of regional LNs, as well as all stained LNs outside the areas of regional metastases. When technically possible, the planned volume of liver surgery and biliary tract resection was performed.
Results. In two cases (7.7 %) no SLN was detected, in this group there were no metastases in the LNs. In the remaining cases (92.3 %, n = 24), accumulation of ICG in one or more LNs was noted. LN invasion was noted in 12 patients. In this group, when using the first two stained LNs as SLNs, the sensitivity was 91.7 % (n = 11/12). Studying SLN 3 did not affect the sensitivity, but allowed identifying affected LNs outside the areas of regional metastases in two cases (7,7 %).
Conclusion. ICG lymphography is a promising method for determination of the SLNs and lymphatic drainage pathways in biliary cancer. It is advisable to evaluate the effect of LN dissection performed using fluorescence lymphography on long-term outcomes in patients with resectable biliary cancer.
Keywords
About the Authors
A. V. KorshakRussian Federation
Alina V. Korshak – oncologist of the Department of Abdominal Oncology No. 2 (tumors of the hepatopancreatobiliary zone)
Scopus Author ID: 58681896200
Moscow
Competing Interests:
the authors declare that there are no obvious and potential conflicts of interest associated with the publication of this article
D. V. Podluzhnyi
Russian Federation
Danil V. Podluzhny – Cand. Sci. (Medicine), Leading Researcher of the Department of abdominal oncology No. 2 (tumors of the hepatopancreatobiliary zone)
AuthorID: 583879
Scopus Author ID: 56801896900
Moscow
Competing Interests:
the authors declare that there are no obvious and potential conflicts of interest associated with the publication of this article
A. G. Kotelnikov
Russian Federation
Alexey G. Kotelnikov – Dr. Sci. (Medicine), Professor, Leading Researcher of the Department of abdominal oncology No. 2 (tumors of the hepatopancreatobiliary zone)
AuthorID: 105352
Scopus Author ID: 7005528750
Moscow
Competing Interests:
the authors declare that there are no obvious and potential conflicts of interest associated with the publication of this article
E. O. Gazaryan
Russian Federation
Eduard O. Gazaryan – MD, oncologist, outpatient care
Moscow
Competing Interests:
the authors declare that there are no obvious and potential conflicts of interest associated with the publication of this article
A. Sh. Umirzokov
Russian Federation
Anvarjon Sh. Umirzokov – postgraduate student of the Department of Abdominal Oncology No. 2 (tumors of the hepatopancreatobiliary zone)
Moscow
Competing Interests:
the authors declare that there are no obvious and potential conflicts of interest associated with the publication of this article
I. V. Savchenko
Russian Federation
Ilya V. Savchenko – oncologist of Department of Antitumor Drug Therapy No. 3 (Department of Drug Treatment)
Moscow
Competing Interests:
the authors declare that there are no obvious and potential conflicts of interest associated with the publication of this article
M. V. Batalova
Russian Federation
Maria V. Batalova – Cand. Sci. (Medicine), radiologist of the Diagnostic Radiology Department
Moscow
Competing Interests:
the authors declare that there are no obvious and potential conflicts of interest associated with the publication of this article
A. N. Polyakov
Russian Federation
Alexander N. Polyakov – Cand. Sci. (Medicine), Senior Researcher, Department of Abdominal Oncology No. 2 (tumors of the hepatopancreatobiliary zone)
AuthorID: 764535
Scopus Author ID: 57190413973
WoS ResearcherID: ABB-8912-2021
Moscow
Competing Interests:
the authors declare that there are no obvious and potential conflicts of interest associated with the publication of this article
References
1. van Keulen AM, Olthof PB, Cescon M, et al. Actual 10-Year Survival after Resection of Perihilar Cholangiocarcinoma: What Factors Preclude a Chance for Cure? Cancers (Basel). 2021 Dec 13;13(24):6260. doi: 10.3390/cancers13246260
2. Zhang XF, Xue F, Dong DH, et al. Number and Station of Lymph Node Metastasis After Curative-intent Resection of Intrahepatic Cholangiocarcinoma Impact Prognosis. Ann Surg. 2021 Dec 1;274(6):e1187-e1195. doi: 10.1097/SLA.0000000000003788
3. Zhu J, Liu C, Li H, at al. Adequate lymph node dissection is essential for accurate nodal staging in intrahepatic cholangiocarcinoma: A population-based study. Cancer Med. 2023 Apr;12(7):8184-8198. doi: 10.1002/cam4.5620
4. Zhang XF, Xue F, Weiss M, at al. Lymph Node Examination and Patterns of Nodal Metastasis Among Patients with Left- Versus Right-Sided Intrahepatic Cholangiocarcinoma After Major Curative-Intent Resection. Ann Surg Oncol. 2023 Mar;30(3):1424-1433. doi: 10.1245/s10434-022-12797-2
5. Ruzzenente A, Conci S, Viganò L, at al. Role of Lymph Node Dissection in Small (≤ 3 cm) Intrahepatic Cholangiocarcinoma. J Gastrointest Surg. 2019 Jun;23(6):1122-1129. doi: 10.1007/s11605-019-04108-0
6. Marinelli I, Guido A, Fuccio L, et al. Clinical Target Volume in Biliary Carcinoma: A Systematic Review of Pathological Studies. Anticancer Res. 2017 Mar;37(3):955-961. doi: 10.21873/anticanres.11404
7. Vogel A, Bridgewater J, Edeline J, et al.; ESMO Guidelines Committee. Electronic address: clinicalguidelines@esmo.org. Biliary tract cancer: ESMO Clinical Practice Guideline for diagnosis, treatment and follow-up. Ann Oncol. 2023 Feb;34(2):127-140. doi: 10.1016/j.annonc.2022.10.506
8. Zhang Y, Zhang Y, Zhu J et al. Clinical application of indocyanine green fluorescence imaging in laparoscopic lymph node dissection for intrahepatic cholangiocarcinoma: A pilot study (with video). Surgery. 2022 Jun;171(6):1589-1595. doi: 10.1016/j.surg.2021.09.032
9. He M, Xu X, Feng H, et al. Regional lymphadenectomy vs. extended lymphadenectomy for hilar cholangiocarcinoma (Relay-HC trial): study protocol for a prospective, multicenter, randomized controlled trial. Trials. 2019 Aug 23;20(1):528. doi: 10.1186/s13063-019-3605-z
10. Li J, Zhou MH, Ma WJ, et al. Extended lymphadenectomy in hilar cholangiocarcinoma: What it will bring? World J Gastroenterol. 2020 Jun 28;26(24):3318-3325. doi: 10.3748/wjg.v26.i24.3318
11. Vega EA, Vinuela E, Yamashita S et al. Extended Lymphadenectomy Is Required for Incidental Gallbladder Cancer Independent of Cystic Duct Lymph Node Status. J Gastrointest Surg. 2018 Jan;22(1):43-51. doi: 10.1007/s11605-017-3507-x
12. van Dam MA, Bijlstra OD, Faber RA, et al. Consensus conference statement on fluorescence-guided surgery (FGS) ESSO course on fluorescence-guided surgery. Eur J Surg Oncol. 2024;50(2):107317. doi:10.1016/j.ejso.2023.107317
13. [Tikhonovskaya M.N., Shevchuk A.S. Sentinel lymph node detection in early stage ovarian cancer: the primary experience in N.N. Blokhin National medical Research Center of Oncology. Tazovaya Khirurgiya i Onkologiya = Pelvic Surgery and Oncology 2022;12(3):19–25. (In Russ.).] doi: 10.17650 / 2686-9594-2022-12-3-19-25
14. Yong TL, Houli N, Christophi C. Anatomy of hepatic lymphatics and its implications in hepatic malignancies. ANZ J Surg. 2016 Nov;86(11):868-873. doi: 10.1111/ans.13662
15. Frenkel NC, Poghosyan S, Verheem A, et al. J. Liver lymphatic drainage patterns follow segmental anatomy in a murine model. Sci Rep. 2020 Dec 11;10(1):21808. doi: 10.1038/s41598-020-78727-y
16. Amin MB, Greene FL, Edge SB, et al. The Eighth Edition AJCC Cancer Staging Manual: Continuing to build a bridge from a population-based to a more "personalized" approach to cancer staging. CA Cancer J Clin. 2017 Mar;67(2):93-99. doi: 10.3322/caac.21388
17. Kolck J, Auer TA, Walter-Rittel T, et al. Prediction of regional lymph node metastasis in intrahepatic cholangiocarcinoma: it's not all about size. Abdom Radiol (NY). 2023 Oct;48(10):3063-3071. doi: 10.1007/s00261-023-03991-1
18. Kim YY, Yeom SK, Shin H, et al. Clinical Staging of Mass-Forming Intrahepatic Cholangiocarcinoma: Computed Tomography Versus Magnetic Resonance Imaging. Hepatol Commun. 2021 Dec;5(12):2009-2018. doi: 10.1002/hep4.1774
19. Lamarca A, Barriuso J, Chander A, et al. 18F-fluorodeoxyglucose positron emission tomography (18FDG-PET) for patients with biliary tract cancer: Systematic review and meta-analysis. J Hepatol. 2019 Jul;71(1):115-129. doi: 10.1016/j.jhep.2019.01.038
20. Gyoten K, Kuriyama N, Maeda K, et al. Safety and efficacy of neoadjuvant chemotherapy based on our resectability criteria for locally advanced perihilar cholangiocarcinoma. Langenbecks Arch Surg. 2023 Jul 1;408(1):261. doi: 10.1007/s00423-023-03000-5
21. Yeow M, Fong KY, Zhao JJ, et al. Value of lymph node dissection in intrahepatic cholangiocarcinoma: a systematic review and meta-analysis. HPB (Oxford). 2024;26(2):161-170. doi:10.1016/j.hpb.2023.11.007
22. Atif M, Borakati A, Mavroeidis VK. Role of routine lymph node dissection alongside resection of intrahepatic cholangiocarcinoma: Systematic review and meta-analysis. World J Gastrointest Oncol. 2023 Nov 15;15(11):2017-2032. doi: 10.4251/wjgo.v15.i11.2017
23. Yuza K, Sakata J, Prasoon P, et al. Long-term outcomes of surgical resection for T1b gallbladder cancer: an institutional evaluation. BMC Cancer. 2020 Jan 6;20(1):20. doi: 10.1186/s12885-019-6507-2
24. Knitter S, Raschzok N, Hillebrandt KH, et al. Short-term postoperative outcomes of lymphadenectomy for cholangiocarcinoma, hepatocellular carcinoma and colorectal liver metastases in the modern era of liver surgery: Insights from the StuDoQ|Liver registry. Eur J Surg Oncol. 2024 Apr;50(4):108010. doi: 10.1016/j.ejso.2024.108010
25. Gholami S, Colby S, Horowitz DP et al. Adjuvant Chemoradiation in Patients with Lymph Node-Positive Biliary Tract Cancers: Secondary Analysis of a Single-Arm Clinical Trial (SWOG 0809). Ann Surg Oncol. 2023 Mar;30(3):1354-1363. doi: 10.1245/s10434-022-12863-9
26. Sposito C, Maspero M, Cucchetti A, et al. A snapshot on current approaches to lymphadenectomy in liver resection for intrahepatic cholangiocarcinoma: results from an international survey. Updates Surg. 2024 Sep;76(5):1797-1805. doi: 10.1007/s13304-024-01852-0
Review
For citations:
Korshak A.V., Podluzhnyi D.V., Kotelnikov A.G., Gazaryan E.O., Umirzokov A.Sh., Savchenko I.V., Batalova M.V., Polyakov A.N. Intraoperative lymphography with indocyanine green experience in liver resection planning in patients with biliary cancer. Research and Practical Medicine Journal. 2025;12(4):44-55. https://doi.org/10.17709/2410-1893-2025-12-4-4. EDN: TIAPIQ


















