Application of real-time indocyanine green fluorescence imaging navigation technology in rectal cancer surgery_CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Authors：

YANG Yong , LI Shanshan , ZHANG Zhengguo , HUANG Luqiao , XIE Guangwei ,  MENG Qingliang

1. Department of Anorectal Surgery, Xuzhou Central Hospital, Xuzhou, Jiangsu 221009, P. R. China;

Corresponding author：

MENG Qingliang, Email: erxing1986@126.com

Keywords：

rectal cancer; indocyanine green; fluorescence navigation; lymphadenectomy; anastomotic blood supply

DOI：

10.7507/1007-9424.202309049

Video：

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Objective To evaluate the value of real-time indocyanine green fluorescence imaging navigation (ICG-FIN) in laparoscopic rectal cancer surgery. Methods The patients who adopted ICG-FIN during laparoscopic rectal cancer surgery in the Department of Anorectal Surgery of Xuzhou Central Hospital from April 2022 to June 2023 according to the inclusion and exclusion criteria (ICG-FIN group) were collected, meanwhile matching (1∶1) of patients who did not adopt ICG-FIN during laparoscopic surgery from January 2021 to May 2022 (control group). The general data, surgical conditions, intraoperative and postoperative outcomes between the two groups were compared. Results There were 62 patients in the ICG-FIN group and 62 patients in the control group. There were no statistical differences in the gender, age, body mass index, comorbidities, and so on between the two groups (P>0.05). The tumor localization, lymph node tracing, fluorescence imaging of the intended resection of intestinal tract and anastomotic site were observed in the ICG-FIN group. Seven patients (11.3%) had changed in the intended resection of intestinal anastomotic line during surgery, while there were no changes of the surgical plan in the control group. There were no statistical differences (P>0.05) in terms of surgical method, operative time, intraoperative bleeding, proportion of ileostomy, time of the first postoperative exhaust, postoperative hospital stay, and incidence of short-term complications between the two groups. Compared with the control group, the incidence of anastomotic leakage was lower (P=0.012), and the number of lymph nodes cleaned was more (P=0.016) in the ICG-FIN group. However, there was no statistical difference in the number of positive lymph nodes detected between the two groups (P=0.343). Conclusions According to the results of this study, ICG-FIN is a reliable and effective method during laparoscopic rectal cancer surgery, which can accurately localize tumor, trace and guide lymph node dissection. Real-time evaluation of intestinal blood flow perfusion is of great practical value in reducing anastomotic leakage.

Citation： YANG Yong, LI Shanshan, ZHANG Zhengguo, HUANG Luqiao, XIE Guangwei, MENG Qingliang. Application of real-time indocyanine green fluorescence imaging navigation technology in rectal cancer surgery. CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY, 2024, 31(1): 45-49. doi: 10.7507/1007-9424.202309049 Copy

1.	Peltrini R, Podda M, Castiglioni S, et al. Intraoperative use of indocyanine green fluorescence imaging in rectal cancer surgery: the state of the art. World J Gastroenterol, 2021, 27(38): 6374-6386.
2.	Ueda K, Ushijima H, Kawamura J. Lymphatic flow mapping during colon cancer surgery using indocyanine green fluorescence imaging. Minim Invasive Ther Allied Technol, 2023, 32(5): 233-239.
3.	Kinoshita H, Kawada K, Itatani Y, et al. Timing of real-time indocyanine green fluorescence visualization for lymph node dissection during laparoscopic colon cancer surgery. Langenbecks Arch Surg, 2023, 408(1): 38.
4.	Rahbari NN, Weitz J, Hohenberger W, et al. Definition and grading of anastomotic leakage following anterior resection of the rectum: a proposal by the International Study Group of Rectal Cancer. Surgery, 2010, 147(3): 339-351.
5.	中华医学会外科学分会结直肠外科学组. 吲哚菁绿近红外光成像在腹腔镜结直肠癌手术中应用中国专家共识(2021版). 中国实用外科杂志, 2021, 41(10): 1098-1103, 1110.
6.	Handgraaf HJ, Boogerd LS, Verbeek FP, et al. Intraoperative fluorescence imaging to localize tumors and sentinel lymph nodes in rectal cancer. Minim Invasive Ther Allied Technol, 2016, 25(1): 48-53.
7.	Magdassi S, Bar-David S, Friedman-Levi Y, et al. Intraoperative localization of rectal tumors using liposomal indocyanine green. Surg Innov, 2017, 24(2): 139-144.
8.	van der Pas MH, Meijer S, Hoekstra OS, et al. Sentinel-lymph-node procedure in colon and rectal cancer: a systematic review and meta-analysis. Lancet Oncol, 2011, 12(6): 540-550.
9.	Protyniak B, Dinallo AM, Boyan WJ, et al. Intraoperative indocyanine green fluorescence angiography—an objective evaluation of anastomotic perfusion in colorectal surgery. Am Surg, 2015, 81(6): 580-584.
10.	Nagata K, Endo S, Hidaka E, et al. Laparoscopic sentinel node mapping for colorectal cancer using infrared ray laparoscopy. Anticancer Res, 2006, 26(3B): 2307-2311.
11.	Noura S, Ohue M, Seki Y, et al. Feasibility of a lateral region sentinel node biopsy of lower rectal cancer guided by indocyanine green using a near-infrared camera system. Ann Surg Oncol, 2010, 17(1): 144-151.
12.	Hirche C, Mohr Z, Kneif S, et al. Ultrastaging of colon cancer by sentinel node biopsy using fluorescence navigation with indocyanine green. Int J Colorectal Dis, 2012, 27(3): 319-324.
13.	Currie AC, Brigic A, Thomas-Gibson S, et al. A pilot study to assess near infrared laparoscopy with indocyanine green (ICG) for intraoperative sentinel lymph node mapping in early colon cancer. Eur J Surg Oncol, 2017, 43(11): 2044-2051.
14.	Ushijima H, Kawamura J, Ueda K, et al. Visualization of lymphatic flow in laparoscopic colon cancer surgery using indocyanine green fluorescence imaging. Sci Rep, 2020, 10(1): 14274.
15.	Ribero D, Mento F, Sega V, et al. ICG-guided lymphadenectomy during surgery for colon and rectal cancer—Interim analysis of the GREENLIGHT trial. Biomedicines, 2022, 10(3): 541.
16.	Liberale G, Bohlok A, Bormans A, et al. Indocyanine green fluorescence imaging for sentinel lymph node detection in colorectal cancer: a systematic review. Eur J Surg Oncol, 2018, 44(9): 1301-1306.
17.	Lucas K, Melling N, Giannou AD, et al. Lymphatic mapping in colon cancer depending on injection time and tracing agent: a systematic review and meta-analysis of prospective designed studies. Cancers (Basel), 2023, 15(12): 3196.
18.	Villegas-Tovar E, Jimenez-Lillo J, Jimenez-Valerio V, et al. Performance of indocyanine green for sentinel lymph node mapping and lymph node metastasis in colorectal cancer: a diagnostic test accuracy meta-analysis. Surg Endosc, 2020, 34(3): 1035-1047.
19.	Lago V, Fotopoulou C, Chiantera V, et al. Risk factors for anastomotic leakage after colorectal resection in ovarian cancer surgery: a multi-centre study. Gynecol Oncol, 2019, 153(3): 549-554.
20.	Arezzo A, Filippini C, Morino M. The REAL (REctal Anastomotic Leak) score for prediction of anastomotic leak after rectal cancer surgery. Tech Coloproctol, 2021, 25(2): 247-248.
21.	Degiuli M, Elmore U, De Luca R, et al. Risk factors for anastomotic leakage after anterior resection for rectal cancer (RALAR study): a nationwide retrospective study of the Italian Society of Surgical Oncology Colorectal Cancer Network Collaborative Group. Colorectal Dis, 2022, 24(3): 264-276.
22.	Vignali A, Gianotti L, Braga M, et al. Altered microperfusion at the rectal stump is predictive for rectal anastomotic leak. Dis Colon Rectum, 2000, 43(1): 76-82.
23.	Karliczek A, Harlaar NJ, Zeebregts CJ, et al. Surgeons lack predictive accuracy for anastomotic leakage in gastrointestinal surgery. Int J Colorectal Dis, 2009, 24(5): 569-576.
24.	Kudszus S, Roesel C, Schachtrupp A, et al. Intraoperative laser fluorescence angiography in colorectal surgery: a noninvasive analysis to reduce the rate of anastomotic leakage. Langenbecks Arch Surg, 2010, 395(8): 1025-1030.
25.	Jafari MD, Lee KH, Halabi WJ, et al. The use of indocyanine green fluorescence to assess anastomotic perfusion during robotic assisted laparoscopic rectal surgery. Surg Endosc, 2013, 27(8): 3003-3008.
26.	Jafari MD, Wexner SD, Martz JE, et al. Perfusion assessment in laparoscopic left-sided/anterior resection (PILLAR Ⅱ): a multi-institutional study. J Am Coll Surg, 2015, 220(1): 82-92.
27.	Sherwinter DA, Gallagher J, Donkar T. Intra-operative transanal near infrared imaging of colorectal anastomotic perfusion: a feasibility study. Colorectal Dis, 2013, 15(1): 91-96.
28.	Boni L, David G, Dionigi G, et al. Indocyanine green-enhanced fluorescence to assess bowel perfusion during laparoscopic colorectal resection. Surg Endosc, 2016, 30(7): 2736-2742.
29.	Trastulli S, Munzi G, Desiderio J, et al. Indocyanine green fluorescence angiography versus standard intraoperative methods for prevention of anastomotic leak in colorectal surgery: meta-analysis. Br J Surg, 2021, 108(4): 359-372.
30.	Emile SH, Khan SM, Wexner SD. Impact of change in the surgical plan based on indocyanine green fluorescence angiography on the rates of colorectal anastomotic leak: a systematic review and meta-analysis. Surg Endosc, 2022, 36(4): 2245-2257.

1. Peltrini R, Podda M, Castiglioni S, et al. Intraoperative use of indocyanine green fluorescence imaging in rectal cancer surgery: the state of the art. World J Gastroenterol, 2021, 27(38): 6374-6386.
2. Ueda K, Ushijima H, Kawamura J. Lymphatic flow mapping during colon cancer surgery using indocyanine green fluorescence imaging. Minim Invasive Ther Allied Technol, 2023, 32(5): 233-239.
3. Kinoshita H, Kawada K, Itatani Y, et al. Timing of real-time indocyanine green fluorescence visualization for lymph node dissection during laparoscopic colon cancer surgery. Langenbecks Arch Surg, 2023, 408(1): 38.
4. Rahbari NN, Weitz J, Hohenberger W, et al. Definition and grading of anastomotic leakage following anterior resection of the rectum: a proposal by the International Study Group of Rectal Cancer. Surgery, 2010, 147(3): 339-351.
5. 中华医学会外科学分会结直肠外科学组. 吲哚菁绿近红外光成像在腹腔镜结直肠癌手术中应用中国专家共识(2021版). 中国实用外科杂志, 2021, 41(10): 1098-1103, 1110.
6. Handgraaf HJ, Boogerd LS, Verbeek FP, et al. Intraoperative fluorescence imaging to localize tumors and sentinel lymph nodes in rectal cancer. Minim Invasive Ther Allied Technol, 2016, 25(1): 48-53.
7. Magdassi S, Bar-David S, Friedman-Levi Y, et al. Intraoperative localization of rectal tumors using liposomal indocyanine green. Surg Innov, 2017, 24(2): 139-144.
8. van der Pas MH, Meijer S, Hoekstra OS, et al. Sentinel-lymph-node procedure in colon and rectal cancer: a systematic review and meta-analysis. Lancet Oncol, 2011, 12(6): 540-550.
9. Protyniak B, Dinallo AM, Boyan WJ, et al. Intraoperative indocyanine green fluorescence angiography—an objective evaluation of anastomotic perfusion in colorectal surgery. Am Surg, 2015, 81(6): 580-584.
10. Nagata K, Endo S, Hidaka E, et al. Laparoscopic sentinel node mapping for colorectal cancer using infrared ray laparoscopy. Anticancer Res, 2006, 26(3B): 2307-2311.
11. Noura S, Ohue M, Seki Y, et al. Feasibility of a lateral region sentinel node biopsy of lower rectal cancer guided by indocyanine green using a near-infrared camera system. Ann Surg Oncol, 2010, 17(1): 144-151.
12. Hirche C, Mohr Z, Kneif S, et al. Ultrastaging of colon cancer by sentinel node biopsy using fluorescence navigation with indocyanine green. Int J Colorectal Dis, 2012, 27(3): 319-324.
13. Currie AC, Brigic A, Thomas-Gibson S, et al. A pilot study to assess near infrared laparoscopy with indocyanine green (ICG) for intraoperative sentinel lymph node mapping in early colon cancer. Eur J Surg Oncol, 2017, 43(11): 2044-2051.
14. Ushijima H, Kawamura J, Ueda K, et al. Visualization of lymphatic flow in laparoscopic colon cancer surgery using indocyanine green fluorescence imaging. Sci Rep, 2020, 10(1): 14274.
15. Ribero D, Mento F, Sega V, et al. ICG-guided lymphadenectomy during surgery for colon and rectal cancer—Interim analysis of the GREENLIGHT trial. Biomedicines, 2022, 10(3): 541.
16. Liberale G, Bohlok A, Bormans A, et al. Indocyanine green fluorescence imaging for sentinel lymph node detection in colorectal cancer: a systematic review. Eur J Surg Oncol, 2018, 44(9): 1301-1306.
17. Lucas K, Melling N, Giannou AD, et al. Lymphatic mapping in colon cancer depending on injection time and tracing agent: a systematic review and meta-analysis of prospective designed studies. Cancers (Basel), 2023, 15(12): 3196.
18. Villegas-Tovar E, Jimenez-Lillo J, Jimenez-Valerio V, et al. Performance of indocyanine green for sentinel lymph node mapping and lymph node metastasis in colorectal cancer: a diagnostic test accuracy meta-analysis. Surg Endosc, 2020, 34(3): 1035-1047.
19. Lago V, Fotopoulou C, Chiantera V, et al. Risk factors for anastomotic leakage after colorectal resection in ovarian cancer surgery: a multi-centre study. Gynecol Oncol, 2019, 153(3): 549-554.
20. Arezzo A, Filippini C, Morino M. The REAL (REctal Anastomotic Leak) score for prediction of anastomotic leak after rectal cancer surgery. Tech Coloproctol, 2021, 25(2): 247-248.
21. Degiuli M, Elmore U, De Luca R, et al. Risk factors for anastomotic leakage after anterior resection for rectal cancer (RALAR study): a nationwide retrospective study of the Italian Society of Surgical Oncology Colorectal Cancer Network Collaborative Group. Colorectal Dis, 2022, 24(3): 264-276.
22. Vignali A, Gianotti L, Braga M, et al. Altered microperfusion at the rectal stump is predictive for rectal anastomotic leak. Dis Colon Rectum, 2000, 43(1): 76-82.
23. Karliczek A, Harlaar NJ, Zeebregts CJ, et al. Surgeons lack predictive accuracy for anastomotic leakage in gastrointestinal surgery. Int J Colorectal Dis, 2009, 24(5): 569-576.
24. Kudszus S, Roesel C, Schachtrupp A, et al. Intraoperative laser fluorescence angiography in colorectal surgery: a noninvasive analysis to reduce the rate of anastomotic leakage. Langenbecks Arch Surg, 2010, 395(8): 1025-1030.
25. Jafari MD, Lee KH, Halabi WJ, et al. The use of indocyanine green fluorescence to assess anastomotic perfusion during robotic assisted laparoscopic rectal surgery. Surg Endosc, 2013, 27(8): 3003-3008.
26. Jafari MD, Wexner SD, Martz JE, et al. Perfusion assessment in laparoscopic left-sided/anterior resection (PILLAR Ⅱ): a multi-institutional study. J Am Coll Surg, 2015, 220(1): 82-92.
27. Sherwinter DA, Gallagher J, Donkar T. Intra-operative transanal near infrared imaging of colorectal anastomotic perfusion: a feasibility study. Colorectal Dis, 2013, 15(1): 91-96.
28. Boni L, David G, Dionigi G, et al. Indocyanine green-enhanced fluorescence to assess bowel perfusion during laparoscopic colorectal resection. Surg Endosc, 2016, 30(7): 2736-2742.
29. Trastulli S, Munzi G, Desiderio J, et al. Indocyanine green fluorescence angiography versus standard intraoperative methods for prevention of anastomotic leak in colorectal surgery: meta-analysis. Br J Surg, 2021, 108(4): 359-372.
30. Emile SH, Khan SM, Wexner SD. Impact of change in the surgical plan based on indocyanine green fluorescence angiography on the rates of colorectal anastomotic leak: a systematic review and meta-analysis. Surg Endosc, 2022, 36(4): 2245-2257.

CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Application of real-time indocyanine green fluorescence imaging navigation technology in rectal cancer surgery

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