Optimal indocyanine green dosage for lymphatic collector mapping during fluorescence-guided laparoscopic D3 lymph node dissection in patients with right colon cancertients with right colon cancer
https://doi.org/10.21294/1814-4861-2025-24-4-5-19
Abstract
Introduction. The standard approach to treating patients with right colon cancer (RCC) is complete mesocolic excision (CME), the main criteria of which include consequent surgical separation by sharp dissection of the visceral fascia layer from the parietal one and high ligation of blood vessels. However, the extent of lymph node dissection is currently not standardized. In European countries, D2 lymph node dissection is more often performed, while in many Asian countries, D3 lymph node dissection, based on the removal of the apical lymph nodes, is widely used. The lack of precise landmarks and insuffcient visualization of the lymphatic system do not allow the surgeon to reliably judge the radicality of the resection of the lymphatic drainage zone without specialized dyes.
The aim of the study was to evaluate the immediate results of regional lymphatic collector mapping in patients with RCC using individual dose calculation of indocyanine green (ICG).
Material and Methods. The study included 63 patients with RCC who underwent laparoscopic right hemicolectomy (LRH) with CME and D3 lymph node dissection between January 2023 and October 2024. All patients underwent colonoscopy with submucosal administration of ICG 1 cm proximal and distal to the tumor on the day before surgery or on the day of surgery at least 3 hours before. In 27 patients (group 1), the ICG dose was determined empirically (0.5–7.5 mg, median 2.0 mg). In 36 patients (group 2), the dose was calculated individually based on the visceral fat area (VFA) determined by abdominal computed tomography (CT). The total ICG dose was 1 mg per 100 cm2 of VFA. All cases were evaluated according to a fve-level scale, with levels 1 and 5 considered as failed mapping and levels 2–4 as a positive result (successful mapping).
Results. Successful mapping was recorded in 22 (81.5 %) of 27 patients in group 1 and in all 36 (100 %) patients in group 2. Moreover, optimal mapping (good visualization of the regional lymph collector in the NIR mode) was obtained in 11 (40.7 %) of 27 and 31 (86.1 %) of 36 patients, respectively (p<0.001). The complication rates were 37.0 % and 19.4 %, respectively (p=0.156), with complications of grade ≥3 according to Clavien–Dindo classifcation in 7.2 % and 2.8 % of patients (p=0.156). During the pathomorphological evaluation of the removed specimen, the median number of examined lymph nodes (LN) was 46 (12–119) and 53 (33–139) (p=0.054), and the median of metastatic LNs was 3 and 4 nodes, respectively (p=0.992).
Conclusion. When mapping the regional lymphatic collector using ICG in RCC, it is advisable to use an individual calculation of the ICG dose based on VFA, which allows achieving the maximum frequency of successful mapping (100 %) and optimal mapping in 86.1 % of cases.
About the Authors
A. A. NevolskikhRussian Federation
Aleksey A. Nevolskikh, MD, DSc, Deputy Director for Medical Work
10, Marshal Zhukov St., Obninsk, 249031
V. A. Avdeenko
Russian Federation
Violetta A. Avdeenko, MD, Clinical Resident
10, Marshal Zhukov St., Obninsk, 249031
I. P. Reznik
Russian Federation
Ivan P. Reznik, MD, Pathologist, Pathology Department
10, Marshal Zhukov St., Obninsk, 249031
V. A. Kukarskaya
Russian Federation
Valeria A. Kukarskaya, MD, Radiologist
29, Soboleva St., Ekaterinburg, 620000
T. A. Agababyan
Russian Federation
Tatev A. Agababyan, MD, PhD, Head of the Department of Radiation Diagnostics
10, Marshal Zhukov St., Obninsk, 249031
T. P. Pochuev
Russian Federation
Taras P. Pochuev, MD, PhD, Senior Researcher, Department of Radiation and Surgical Treatment of Abdominal Diseases
10, Marshal Zhukov St., Obninsk, 249031
Yu. Yu. Mikhaleva
Russian Federation
Yulia Yu. Mikhaleva, MD, Oncologist, Department of Radiation and Surgical Treatment of Abdominal Diseases
10, Marshal Zhukov St., Obninsk, 249031
R. F. Zibirov
Russian Federation
Ruslan F. Zibirov, MD, Pathologist, Pathology Department
10, Marshal Zhukov St., Obninsk, 249031
V. N. Grinevich
Russian Federation
Vyacheslav N. Grinevich, MD, Head of the Pathomorphology Department
10, Marshal Zhukov St., Obninsk, 249031
I. A. Orekhov
Russian Federation
Ivan A. Orekhov, MD, Oncologist, Department of Radiation and Surgical Treatment of Abdominal Diseases
10, Marshal Zhukov St., Obninsk, 249031
P. V. Sinyaev
Russian Federation
Petr V. Sinyaev, MD, Head of the Endoscopy Department
10, Marshal Zhukov St., Obninsk, 249031
I. A. Evtehov
Russian Federation
Ilya A. Evtehov, MD, Endoscopist, Endoscopy Department
10, Marshal Zhukov St., Obninsk, 249031
A. A. Yudin
Russian Federation
Andrey A. Yudin, MD, Endoscopist, Endoscopy Department
10, Marshal Zhukov St., Obninsk, 249031
L. O. Petrov
Russian Federation
Leonid O. Petrov, MD, PhD, Head of the Department of Radiation and Surgical Treatment of Abdominal Diseases
10, Marshal Zhukov St., Obninsk, 249031
S. A. Ivanov
Russian Federation
Sergey A. Ivanov, MD, DSc, Corresponding Member of the Russian Academy of Sciences, Director; Professor, Department of Oncology and Roentgenology named after V.P. Kharchenko
10, Marshal Zhukov St., Obninsk, 249031;
6, Miklukho-Maklaya St., Moscow, 117198
A. D. Kaprin
Russian Federation
Andrey D. Kaprin, MD, DSc, Professor, Academician of the Russian Academy of Sciences, Academician of the Russian Academy of Education, Director General; Director; Head of the Department of Oncology and Roentgenology named after V.P. Kharchenko, Medical Institute
6, Miklukho-Maklaya St., Moscow, 117198;
4, Koroleva St., Obninsk, 249036;
3, 2nd Botkin passage, Moscow, 125284
References
1. Сolon cancer: clinical guidelines of the Ministry of Health of the Russian Federation. 2022. [Internet]. [cited 01.03.2025]. URL: https://cr.minzdrav.gov.ru/preview-cr/396_3?ysclid=md8at2k2ga152240752.
2. Argilés G., Tabernero J., Labianca R., Hochhauser D., Salazar R., Iveson T., Laurent-Puig P., Quirke P., Yoshino T., Taieb J., Martinelli E., Arnold D.; ESMO Guidelines Committee. Localised colon cancer: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol. 2020; 31(10): 1291–305. doi: 10.1016/j.annonc.2020.06.022.
3. Benson A.B., Venook A.P., Adam M., Chang G., Chen Y.J., Ciombor K.K., Cohen S.A., Cooper H.S., Deming D., Garrido-Laguna I., Grem J.L., Haste P., Hecht J.R., Hoffe S., Hunt S., Hussan H., Johung K.L., Joseph N., Kirilcuk N., Krishnamurthi S., Malla M., Maratt J.K., Messersmith W.A., Meyerhardt J., Miller E.D., Mulcahy M.F., Nurkin S., Overman M.J., Parikh A., Patel H., Pedersen K., Saltz L., Schneider C., Shibata D., Shogan B., Skibber J.M., Sofocleous C.T., Tavakkoli A., Willett C.G., Wu C., Gurski L.A., Snedeker J., Jones F. Colon Cancer, Version 3.2024, NCCN Clinical Practice Guidelines in Oncology. J Natl Compr Canc Netw. 2024; 22(2 D): e240029. doi: 10.6004/jnccn.2024.0029.
4. Hashiguchi Y., Muro K., Saito Y., Ito Y., Ajioka Y., Hamaguchi T., Hasegawa K., Hotta K., Ishida H., Ishiguro M., Ishihara S., Kanemitsu Y., Kinugasa Y., Murofushi K., Nakajima T.E., Oka S., Tanaka T., Taniguchi H., Tsuji A., Uehara K., Ueno H., Yamanaka T., Yamazaki K., Yoshida M., Yoshino T., Itabashi M., Sakamaki K., Sano K., Shimada Y., Tanaka S., Uetake H., Yamaguchi S., Yamaguchi N., Kobayashi H., Matsuda K., Kotake K., Sugihara K.; Japanese Society for Cancer of the Colon and Rectum. Japanese Society for Cancer of the Colon and Rectum (JSCCR) guidelines 2019 for the treatment of colorectal cancer. Int J Clin Oncol. 2020; 25(1): 1–42. doi: 10.1007/s10147-019-01485-z.
5. Sica G.S., Vinci D., Siragusa L., Sensi B., Guida A.M., Bellato V., García-Granero Á., Pellino G. Definition and reporting of lymphadenectomy and complete mesocolic excision for radical right colectomy: a systematic review. Surg Endosc. 2023; 37(2): 846–61. doi: 10.1007/s00464-022-09548-5.
6. Mazzarella G., Muttillo E.M., Picardi B., Rossi S., Muttillo I.A. Complete mesocolic excision and D3 lymphadenectomy with central vascular ligation in right-sided colon cancer: a systematic review of postoperative outcomes, tumor recurrence and overall survival. Surg Endosc. 2021; 35(9): 4945–55. doi: 10.1007/s00464-021-08529-4.
7. Nesgaar J.M., Stimec B.V., Bakka A.O., Edwin B., Bergamaschi R., Ignjatovic D. Right Colectomy with Extended D3 Mesenterectomy: Anterior and Posterior to the Mesenteric Vessels. Surg Technol Int. 2019; 35: 138–42.
8. Son G.M., Yun M.S., Lee I.Y., Im S.B., Kim K.H., Park S.B., Kim T.U., Shin D.H., Nazir A.M., Ha G.W. Clinical Effectiveness of Fluorescence Lymph Node Mapping Using ICG for Laparoscopic Right Hemicolectomy: A Prospective Case-Control Study. Cancers (Basel). 2023; 15(20): 4927. doi: 10.3390/cancers15204927.
9. Shevchenko I., Serban D., Dascalu A.M., Tribus L., Alius C., Cristea B.M., Suceveanu A.I., Voiculescu D., Dumitrescu D., Bobirca F., Suceveanu A.P., Georgescu D.E., Serboiu C.S. Factors Affecting the Efficiency of NearInfrared Indocyanine Green (NIR/ICG) in Lymphatic Mapping for Colorectal Cancer: A Systematic Review. Cureus. 2024; 16(2): e55290. doi: 10.7759/cureus.55290.
10. Nevolskikh A.A., Avdeenko V.A., Mikhaleva Yu., Sinyaev P.V., Yudin A.A., Agababyan T.A., Yevtekhov I.A., Ivanov S.A., Kaprin A.D. Method for mapping lymphatic collector in right colon cancer by paratumoral administration of indocyanine green. RF patent No. 2814766 C2. Declared. 22.12.2023; Publ 04.03.2024. (in Russian). EDN: MOSHCL.
11. West N.P., Morris E.J., Rotimi O., Cairns A., Finan P.J., Quirke P. Pathology grading of colon cancer surgical resection and its association with survival: a retrospective observational study. Lancet Oncol. 2008; 9(9): 857–65. doi: 10.1016/S1470-2045(08)70181-5.
12. Benz S.R., Feder I.S., Vollmer S., Tam Y., Reinacher-Schick A., Denz R., Hohenberger W., Lippert H., Tannapfel A., Stricker I. Complete mesocolic excision for right colonic cancer: prospective multicentre study. Br J Surg. 2022; 110(1): 98–105. doi: 10.1093/bjs/znac379.
13. Nevolskikh A.A., Avdeenko V.A., Reznik I.P., Pochuev T.P., Zibirov R.F., Ivanov S.A., Kaprin A.D. Surgical treatment of right colon cancer. Siberian Journal of Oncology. 2024; 23(3): 133–49. (in Russian). doi: 10.21294/1814-4861-2024-23-3-133-149. EDN: SBBUMV.
14. Tejedor P., Francis N., Jayne D., Hohenberger W., Khan J.; on behalf the CME Project Working Group. Consensus statements on complete mesocolic excision for right-sided colon cancer-technical steps and training implications. Surg Endosc. 2022; 36(8): 5595–601. doi: 10.1007/s00464-021-08395-0.
15. Ahn H.M., Son G.M., Lee I.Y., Shin D.H., Kim T.K., Park S.B., Kim H.W. Optimal ICG dosage of preoperative colonoscopic tattooing for fluorescence-guided laparoscopic colorectal surgery. Surg Endosc. 2022; 36(2): 1152–63. doi: 10.1007/s00464-021-08382-5.
16. Ribero D., Mento F., Sega V., Lo Conte D., Mellano A., Spinoglio G. ICG-Guided Lymphadenectomy during Surgery for Colon and Rectal Cancer-Interim Analysis of the GREENLIGHT Trial. Biomedicines. 2022; 10(3): 541. doi: 10.3390/biomedicines1003054.
17. Petz W., Bertani E., Borin S., Fiori G., Ribero D., Spinoglio G. Fluorescence-guided D3 lymphadenectomy in robotic right colectomy with complete mesocolic excision. Int J Med Robot. 2021; 17(3): 2217. doi: 10.1002/rcs.2217.
18. Ho M.F., Futaba K., Mak T.W.C., Ng S.S.M. Personalized laparoscopic resection of colon cancer with the use of indocyanine green lymph node mapping: Technical and clinical outcomes. Asian J Endosc Surg. 2022; 15(3): 563–68. doi: 10.1111/ases.13050.
19. Sato Y., Satoyoshi T., Okita K., Kyuno D., Hamabe A., Okuya K., Nishidate T., Akizuki E., Ishii M., Yamano H.O., Sugita S., Nakase H., Hasegawa T., Takemasa I. Snapshots of lymphatic pathways in colorectal cancer surgery using near-infrared fluorescence, in vivo and ex vivo. Eur J Surg Oncol. 2021; 47(12): 3130–36. doi: 10.1016/j.ejso.2021.07.025.
20. Ushijima H., Kawamura J., Ueda K., Yane Y., Yoshioka Y., Daito K., Tokoro T., Hida JI., Okuno K. Visualization of lymphatic flow in laparoscopic colon cancer surgery using indocyanine green fluorescence imaging. Sci Rep. 2020; 10(1): 14274. doi: 10.1038/s41598-020-71215-3.
21. Park J.H., Moon H.S., Kwon I.S., Yun G.Y., Lee S.H., Park D.H., Kim J.S., Kang S.H., Lee E.S., Kim S.H., Sung J.K., Lee B.S., Jeong H.Y. Usefulness of colonic tattooing using indocyanine green in patients with colorectal tumors. World J Clin Cases. 2018; 6(13): 632–40. doi: 10.12998/wjcc.v6.i13.632.
22. Nishigori N., Koyama F., Nakagawa T., Nakamura S., Ueda T., Inoue T., Kawasaki K., Obara S., Nakamoto T., Fujii H., Nakajima Y. Visualization of Lymph/Blood Flow in Laparoscopic Colorectal Cancer Surgery by ICG Fluorescence Imaging (Lap-IGFI). Ann Surg Oncol. 2016; 23 Suppl 2: 266–74. doi: 10.1245/s10434-015-4509-0.
23. Park I.J., Choi G.S., Kang B.M., Lim K.H., Jun S.H. Lymph node metastasis patterns in right-sided colon cancers: is segmental resection of these tumors oncologically safe? Ann Surg Oncol. 2009; 16(6): 1501–6. doi: 10.1245/s10434-009-0368-x.
24. Kelder W., Braat A.E., Karrenbeld A., Grond J.A.K., De Vries J.E., Oosterhuis J.W.A., Baas P.C., Plukker J.T.M. The sentinel node procedure in colon carcinoma: a multi-centre study in The Netherlands. Int J Colorectal Dis. 2007; 22(12): 1509. doi: 10.1007/s00384-007-0351-6.
25. Saha S., Johnston G., Korant A., Shaik M., Kanaan M., Johnston R., Ganatra B., Kaushal S., Desai D., Mannam S.Aberrant drainage of sentinel lymph nodes in colon cancer and its impact on staging and extent of operation. Am J Surg. 2013; 205(3): 302–5; discussion 305–6. doi: 10.1016/j.amjsurg.2012.10.029.
26. Tanaka S., Horimai C., Katsukawa F. Ethnic differences in abdominal visceral fat accumulation between Japanese, African-Americans, and Caucasians: a meta-analysis. Acta Diabetol. 2003; 40 Suppl 1: 302–4. doi: 10.1007/s00592-003-0093-z.
Review
For citations:
Nevolskikh A.A., Avdeenko V.A., Reznik I.P., Kukarskaya V.A., Agababyan T.A., Pochuev T.P., Mikhaleva Yu.Yu., Zibirov R.F., Grinevich V.N., Orekhov I.A., Sinyaev P.V., Evtehov I.A., Yudin A.A., Petrov L.O., Ivanov S.A., Kaprin A.D. Optimal indocyanine green dosage for lymphatic collector mapping during fluorescence-guided laparoscopic D3 lymph node dissection in patients with right colon cancertients with right colon cancer. Siberian journal of oncology. 2025;24(4):5-19. (In Russ.) https://doi.org/10.21294/1814-4861-2025-24-4-5-19