Application of near-infrared fluorescence imaging of thoracic duct in inflatable video-assisted mediastinoscopic transhiatal esophagectomy: A propensity score matching study_Chinese Journal of Clinical Thoracic and Cardiovascular Surgery

Authors：

LIU Changqing , MEI Xinyu , WU Xianning , WU Gao ,  WU Hanran

Department of Thoracic Surgery, The First Affiliated Hospital of University of Science and Technology of China, Division of Life Sciences and Medicine, University of Science and Technology of China, Hefei, 230001, P. R. China;

Corresponding author：

WU Hanran, Email: whrxwk@163.com

Keywords：

Esophageal neoplasms; thoracoscope; esophagectomy; indocyanine green; chylothorax; thoracic duct

DOI：

10.7507/1007-4848.202412080

Video：

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Abstract Full text Figures/Tables Video References Cited by

Objective To investigate the safety and effectiveness of near-infrared fluorescence imaging of the thoracic duct (NFITD) using indocyanine green (ICG) during inflatable video-assisted mediastinoscopic transhiatal esophagectomy (IVMTE) for esophageal cancer. Methods A retrospective analysis was conducted on patients with esophageal cancer who underwent IVMTE at the Department of Thoracic Surgery, the First Affiliated Hospital of University of Science and Technology of China, from January 2024 to October 2024. Patients were divided into two groups based on whether they underwent NFITD: an ICG NFITD group (ITD group) and a non-ICG NFITD group (NITD group). Propensity score matching was used to balance confounding factors, and perioperative data and short-term follow-up results (within 6 months) of the two groups were compared. Results A total of 66 patients were included, of which 51 were males and 15 were females, with an average age of (70.9±7.2) years. In the comparison of general information between the two groups, the proportion of patients in the ITD group with preoperative chronic obstructive pulmonary disease was higher than that in the NITD group (P=0.044), and the proportion of patients with preoperative bronchiectasis was lower than that in the NITD group (P=0.035). After propensity score matching at a 1:1 ratio, a total of 15 pairs of patients were successfully matched. There was no statistically significant difference between the two groups in terms of intraoperative blood loss, postoperative hospital stay, complications, maximum tumor diameter, pT stage, pN stage, and pTNM stage (P>0.05). The 6-month postoperative follow-up results showed no statistically significant difference between the two groups in terms of anastomotic stricture, hoarseness, gastric paralysis, anastomotic leakage, and postoperative adjuvant treatment (P>0.05). Conclusion The application of NFITD in IVMTE is safe and effective, with a thoracic duct visualization rate of 100.0%. Compared with NITD, ITD prolonged the operation time but increased the number and stations of lymph node dissection without increasing perioperative and short-term postoperative complications (within 6 months), making it worthy of further clinical promotion.

1.	Bray F, Laversanne M, Sung H, et al. Global cancer statistics 2022: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin, 2024, 74(3): 229-263.
2.	吴汉然, 柳常青, 孙效辉, 等. 新辅助免疫治疗联合微创McKeown术治疗局部晚期食管癌近期结果的回顾性队列研究. 中国胸心血管外科临床杂志, 2024, 31(12): 1767-1774.Wu HR, Liu CQ, Sun XH, et al. Short-term outcomes of neoadjuvant immunotherapy combined with minimally invasive McKeown esophagectomy for locally advanced thoracic esophageal squamous cell carcinoma: A retrospective cohort study. Chin J Clin Thorac Cardiovasc Surg, 2024, 31(12): 1767-1774.
3.	吴汉然, 柳常青, 解明然. 充气式纵隔镜食管癌切除术中国专家共识. 中国胸心血管外科临床杂志, 2023, 30(10): 1367-1376.Wu HR, Liu CQ, Xie MR, et al. Chinese expert consensus on inflatable video-assisted mediastinoscopic transhiatal esophagectomy. Chin J Clin Thorac Cardiovasc Surg, 2023, 30(10): 1367-1376.
4.	黄志宁, 柳常青, 郭明发, 等. 充气式纵隔镜联合腹腔镜食管癌切除术的临床分析. 中华外科杂志, 2023, 61(1): 48-53.Huang ZN, Liu CQ, Guo MF, et al. Clinical analysis of inflatable video-assisted mediastinoscopic transhiatal esophagectomy combined with laparoscopy. Chin J Surg, 2023, 61(1): 48-53.
5.	Wu M, Wang G, Sun X, et al. Inflatable video-assisted mediastinoscopic transhiatal esophagectomy: A learning curve study. J Gastrointest Surg, 2023, 27(11): 2589-2591.
6.	Brinkmann S, Schroeder W, Junggeburth K, et al. Incidence and management of chylothorax after Ivor Lewis esophagectomy for cancer of esophagus. J Thorac Cardiovasc Surg, 2016, 151(5): 1309-1404.
7.	Lin Y, Li Z, Li G, et al. Selective en masse ligation of the thoracic duct to prevent chyle leak after esophagectomy. Ann Thorac Surg, 2017, 103(6): 1802-1807.
8.	Lubbers M, Det M, Kouwenhoven EA. Intraoperative lipid-rich nutrition in the detection of chylothorax in minimally invasive Ivor Lewis esophagectomy. Surg Innov, 2019, 26(5): 545-550.
9.	刘德宇, 许世广, 徐惟, 等. 达芬奇机器人与电视胸腔镜肺癌根治术后乳糜胸危险因素的倾向性评分匹配研究. 中国胸心血管外科临床杂志, 2022, 29(4): 449-456.Liu DY, Xu SG, Xu W, et al. Risk factors for postoperative chylothorax after robot-assisted versus video-assisted thoracic surgery in radical lung cancer resection: A propensity score matching study. Chin J Clin Thorac Cardiovasc Surg, 2022, 29(4): 449-456.
10.	Johnson OW, Chick JF, Chauhan NR, et al. The thoracic duct: Clinical importance, anatomic variation, imaging, and embolization. Eur Radiol, 2016, 26(8): 2582-2493.
11.	Chen JY, Liu QW, Zhang SS, et al. Prophylactic thoracic duct ligation is associated with poor prognosis and regional lymph node relapse in esophageal squamous cell carcinoma. J Surg Oncol, 2020, 122(2): 336-343.
12.	Bedat B, Scarpa CR, Sadowski SM, et al. Acute pancreatitis after thoracic duct ligation for iatrogenic chylothorax: A case report. BMC Surg, 2017, 17(1): 9.
13.	刘宏, 邢富臣, 周海, 等. 吲哚菁绿荧光成像技术预防微创食管癌术后乳糜胸. 临床肿瘤学杂志, 2022, 27(1): 55-59.Liu H, Xing FC, Zhou H, et al. Prevention of chylothorax after minimally invasive esophagectomy by indocyanine green fluorescence imaging. Chin Clin Oncol, 2022, 27(1): 55-59.
14.	Slooter MD, Eshuis WJ, Cuesta MA, et al. Fluorescent imaging using indocyanine green during esophagectomy to prevent surgical morbidity: A systematic review and meta-analysis. J Thorac Dis, 2019, 11(Suppl 5): S755-S765.
15.	Tokumaru S, Kitazawa M, Nakamura S, et al. Intraoperative visualization of morphological patterns of the thoracic duct by subcutaneous inguinal injection of indocyanine green in esophagectomy for esophageal cancer. Ann Gastroenterol Surg, 2022, 6(6): 873-879.
16.	Vecchiato M, Martino A, Sponza M, et al. Thoracic duct identification with indocyanine green fluorescence during minimally invasive esophagectomy with patient in prone position. Dis Esophagus, 2020, 33(12): 1-6.
17.	Barbato G, Cammelli F, Braccini G, et al. Fluorescence lymphography for thoracic duct identification: Initial experience of a simplified and feasible ICG administration. Int J Med Robot, 2022, 18: e2380.
18.	Takhellambam L, Yadav TD, Kumar H, et al. Prophylactic ligation of the opacified thoracic duct in minimally invasive esophagectomy: Feasibility and safety. Langenbecks Arch Surg, 2021, 406(7): 2515-2520.
19.	Wang XJ, Hu Y, Wu XW, et al. Near-infrared fluorescence imaging-guided lymphatic mapping in thoracic esophageal cancer surgery. Surg Endosc, 2022, 36(6): 3994-4003.
20.	Hachey KJ, Gilmore DM, Armstrong KW, et al. Safety and feasibility of near-infrared image-guided lymphatic mapping of regional lymph nodes in esophageal cancer. J Thorac Cardiovasc Surg, 2016, 152(2): 546-554.
21.	Zhang A, Li Y, Zhang H, et al. Comparison of TNM AJCC/UICC 8th with JES 11th staging systems for prognostic prediction in patients with esophageal squamous cell carcinoma who underwent radical (chemo) radiotherapy in China. J Cancer Res Ther, 2023, 19(6): 1610-1619.
22.	Buess G, Becker HD. Minimally invasive surgery in tumor of the esophagus. Langenbecks Arch Chir Suppl Ⅱ Verh Dtsch Ges Chir, 1990, 118: 1355-1360.
23.	Tokairin Y, Nakajima Y, Kawada K, et al. A feasibility study of mediastinoscopic radical esophagectomy for thoracic esophageal cancer from the viewpoint of the dissected mediastinal lymph nodes validated with thoracoscopic procedure: A prospective clinical trial. Esophagus, 2019, 16(2): 214-219.
24.	Barnes TG, MacGregor T, Sgromo B, et al. Near infra-red fluorescence identification of the thoracic duct to prevent chyle leaks during oesophagectomy. Surg Endosc, 2022, 36: 5319-5325.
25.	Yang F, Gao J, Cheng S, et al. Near-infrared fluorescence imaging of thoracic duct in minimally invasive esophagectomy. Dis Esophagus, 2023, 36(2): doac049.
26.	Yokota N, Go T, Fujiwara A, et al. A new method for the detection of air leaks using aerosolized indocyanine green. Ann Thorac Surg, 2021, 111(2): 436-439.
27.	Kamiya K, Unno N, Konno H. Intraoperative indocyanine green fluorescence lymphography, a novel imaging technique to detect a chyle fistula after an esophagectomy: Report of a case. Surg Today, 2009, 39(5): 421-424.
28.	Yang F, Zhou J, Li H, et al. Near-infrared fluorescence-guided thoracoscopic surgical intervention for postoperative chylothorax. Interact Cardiovasc Thorac Surg, 2018, 26: 171-175.
29.	方云昊, 陈子豪, 韦荣强, 等. 充气纵隔镜与电视胸腔镜联合腹腔镜手术治疗食管癌的短期随访结果比较. 中国胸心血管外科临床杂志, 2021, 28(2): 239-242.Fang YH, Chen ZH, Wei RQ, et al. Short-term follow-up results of inflatable mediastinoscopy with laparoscopy versus video-assisted thoracoscopic surgery combined with laparoscopy for esophageal cancer. Chin J Clin Thorac Cardiovasc Surg, 2021, 28(2): 239-242.
30.	Liu C, Chen Z, Wei R, et al. Intra-operative events and countermeasures during esophagectomy via transcervical incision inflatable single-port mediastinoscope combined with laparoscopy. J Thorac Dis, 2021, 13(1): 133-139.
31.	宋尚岐, 胡杨, 徐昱扬, 等. 充气纵隔镜联合腹腔镜食管癌切除术的临床进展. 中华消化外科杂志, 2023, 22(4): 474-480.Song SQ, Hu Y, Xu YY, et al. Clinical progress of inflatable video-assisted mediastinoscopic transhiatal esophagectomy. Chin J Dig Surg, 2023, 22(4): 474-480.
32.	Ajani JA, D'Amico TA, Bentrem DJ, et al. Esophageal and esophagogastric junction cancers, version 2. 2019, NCCN clinical practice guidelines in oncology. J Natl Compr Canc Netw, 2019, 17(7): 855-883.
33.	冷雪峰, 大幸宏幸, 韩泳涛. 食管鳞状细胞癌NCCN指南及JES指南外科诊疗要点解读. 肿瘤预防与治疗, 2024, 37(4): 286-291.Leng XF, Daiko H, Han YT. Interpretation of NCCN and JES guidelines for the treatment of esophageal squamous cell carcinoma. J Cancer Control Treat, 2024, 37(4): 286-291.
34.	中华人民共和国国家卫生健康委员会医政医管局. 食管癌诊疗指南 (2022年版). 中华消化外科杂志, 2022, 21(10): 1247-1268.Bureau of Medical Administration, National Health Commission of the People's Republic of China. Standardization for diagnosis and treatment of esophageal cancer (2022 edition). Chin J Dig Surg, 2022, 21(10): 1247-1268.
35.	柳常青, 吴汉然, 郭明发, 等. 改良充气式纵隔镜在早期胸段食管癌中的临床应用. 中华胸心血管外科杂志, 2019, 35(2): 80-85.Liu CQ, Wu HR, Guo MF, et al. Clinical application of modified inflatable video-assisted mediastinoscopic transhiatal esophagectomy in patients with early esophageal cancer. Chin J Thorac Cardiovasc Surg, 2019, 35(2): 80-85.
36.	Tokairin Y, Nakajima Y, Kawada K, et al. The usefulness of a bilateral transcervical pneumomediastinal approach for mediastinoscopic radical esophagectomy: A right transcervical approach is an available option. Gen Thorac Cardiovasc Surg, 2019, 67(10): 884-890.

1. Bray F, Laversanne M, Sung H, et al. Global cancer statistics 2022: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin, 2024, 74(3): 229-263.
2. 吴汉然, 柳常青, 孙效辉, 等. 新辅助免疫治疗联合微创McKeown术治疗局部晚期食管癌近期结果的回顾性队列研究. 中国胸心血管外科临床杂志, 2024, 31(12): 1767-1774.Wu HR, Liu CQ, Sun XH, et al. Short-term outcomes of neoadjuvant immunotherapy combined with minimally invasive McKeown esophagectomy for locally advanced thoracic esophageal squamous cell carcinoma: A retrospective cohort study. Chin J Clin Thorac Cardiovasc Surg, 2024, 31(12): 1767-1774.
3. 吴汉然, 柳常青, 解明然. 充气式纵隔镜食管癌切除术中国专家共识. 中国胸心血管外科临床杂志, 2023, 30(10): 1367-1376.Wu HR, Liu CQ, Xie MR, et al. Chinese expert consensus on inflatable video-assisted mediastinoscopic transhiatal esophagectomy. Chin J Clin Thorac Cardiovasc Surg, 2023, 30(10): 1367-1376.
4. 黄志宁, 柳常青, 郭明发, 等. 充气式纵隔镜联合腹腔镜食管癌切除术的临床分析. 中华外科杂志, 2023, 61(1): 48-53.Huang ZN, Liu CQ, Guo MF, et al. Clinical analysis of inflatable video-assisted mediastinoscopic transhiatal esophagectomy combined with laparoscopy. Chin J Surg, 2023, 61(1): 48-53.
5. Wu M, Wang G, Sun X, et al. Inflatable video-assisted mediastinoscopic transhiatal esophagectomy: A learning curve study. J Gastrointest Surg, 2023, 27(11): 2589-2591.
6. Brinkmann S, Schroeder W, Junggeburth K, et al. Incidence and management of chylothorax after Ivor Lewis esophagectomy for cancer of esophagus. J Thorac Cardiovasc Surg, 2016, 151(5): 1309-1404.
7. Lin Y, Li Z, Li G, et al. Selective en masse ligation of the thoracic duct to prevent chyle leak after esophagectomy. Ann Thorac Surg, 2017, 103(6): 1802-1807.
8. Lubbers M, Det M, Kouwenhoven EA. Intraoperative lipid-rich nutrition in the detection of chylothorax in minimally invasive Ivor Lewis esophagectomy. Surg Innov, 2019, 26(5): 545-550.
9. 刘德宇, 许世广, 徐惟, 等. 达芬奇机器人与电视胸腔镜肺癌根治术后乳糜胸危险因素的倾向性评分匹配研究. 中国胸心血管外科临床杂志, 2022, 29(4): 449-456.Liu DY, Xu SG, Xu W, et al. Risk factors for postoperative chylothorax after robot-assisted versus video-assisted thoracic surgery in radical lung cancer resection: A propensity score matching study. Chin J Clin Thorac Cardiovasc Surg, 2022, 29(4): 449-456.
10. Johnson OW, Chick JF, Chauhan NR, et al. The thoracic duct: Clinical importance, anatomic variation, imaging, and embolization. Eur Radiol, 2016, 26(8): 2582-2493.
11. Chen JY, Liu QW, Zhang SS, et al. Prophylactic thoracic duct ligation is associated with poor prognosis and regional lymph node relapse in esophageal squamous cell carcinoma. J Surg Oncol, 2020, 122(2): 336-343.
12. Bedat B, Scarpa CR, Sadowski SM, et al. Acute pancreatitis after thoracic duct ligation for iatrogenic chylothorax: A case report. BMC Surg, 2017, 17(1): 9.
13. 刘宏, 邢富臣, 周海, 等. 吲哚菁绿荧光成像技术预防微创食管癌术后乳糜胸. 临床肿瘤学杂志, 2022, 27(1): 55-59.Liu H, Xing FC, Zhou H, et al. Prevention of chylothorax after minimally invasive esophagectomy by indocyanine green fluorescence imaging. Chin Clin Oncol, 2022, 27(1): 55-59.
14. Slooter MD, Eshuis WJ, Cuesta MA, et al. Fluorescent imaging using indocyanine green during esophagectomy to prevent surgical morbidity: A systematic review and meta-analysis. J Thorac Dis, 2019, 11(Suppl 5): S755-S765.
15. Tokumaru S, Kitazawa M, Nakamura S, et al. Intraoperative visualization of morphological patterns of the thoracic duct by subcutaneous inguinal injection of indocyanine green in esophagectomy for esophageal cancer. Ann Gastroenterol Surg, 2022, 6(6): 873-879.
16. Vecchiato M, Martino A, Sponza M, et al. Thoracic duct identification with indocyanine green fluorescence during minimally invasive esophagectomy with patient in prone position. Dis Esophagus, 2020, 33(12): 1-6.
17. Barbato G, Cammelli F, Braccini G, et al. Fluorescence lymphography for thoracic duct identification: Initial experience of a simplified and feasible ICG administration. Int J Med Robot, 2022, 18: e2380.
18. Takhellambam L, Yadav TD, Kumar H, et al. Prophylactic ligation of the opacified thoracic duct in minimally invasive esophagectomy: Feasibility and safety. Langenbecks Arch Surg, 2021, 406(7): 2515-2520.
19. Wang XJ, Hu Y, Wu XW, et al. Near-infrared fluorescence imaging-guided lymphatic mapping in thoracic esophageal cancer surgery. Surg Endosc, 2022, 36(6): 3994-4003.
20. Hachey KJ, Gilmore DM, Armstrong KW, et al. Safety and feasibility of near-infrared image-guided lymphatic mapping of regional lymph nodes in esophageal cancer. J Thorac Cardiovasc Surg, 2016, 152(2): 546-554.
21. Zhang A, Li Y, Zhang H, et al. Comparison of TNM AJCC/UICC 8th with JES 11th staging systems for prognostic prediction in patients with esophageal squamous cell carcinoma who underwent radical (chemo) radiotherapy in China. J Cancer Res Ther, 2023, 19(6): 1610-1619.
22. Buess G, Becker HD. Minimally invasive surgery in tumor of the esophagus. Langenbecks Arch Chir Suppl Ⅱ Verh Dtsch Ges Chir, 1990, 118: 1355-1360.
23. Tokairin Y, Nakajima Y, Kawada K, et al. A feasibility study of mediastinoscopic radical esophagectomy for thoracic esophageal cancer from the viewpoint of the dissected mediastinal lymph nodes validated with thoracoscopic procedure: A prospective clinical trial. Esophagus, 2019, 16(2): 214-219.
24. Barnes TG, MacGregor T, Sgromo B, et al. Near infra-red fluorescence identification of the thoracic duct to prevent chyle leaks during oesophagectomy. Surg Endosc, 2022, 36: 5319-5325.
25. Yang F, Gao J, Cheng S, et al. Near-infrared fluorescence imaging of thoracic duct in minimally invasive esophagectomy. Dis Esophagus, 2023, 36(2): doac049.
26. Yokota N, Go T, Fujiwara A, et al. A new method for the detection of air leaks using aerosolized indocyanine green. Ann Thorac Surg, 2021, 111(2): 436-439.
27. Kamiya K, Unno N, Konno H. Intraoperative indocyanine green fluorescence lymphography, a novel imaging technique to detect a chyle fistula after an esophagectomy: Report of a case. Surg Today, 2009, 39(5): 421-424.
28. Yang F, Zhou J, Li H, et al. Near-infrared fluorescence-guided thoracoscopic surgical intervention for postoperative chylothorax. Interact Cardiovasc Thorac Surg, 2018, 26: 171-175.
29. 方云昊, 陈子豪, 韦荣强, 等. 充气纵隔镜与电视胸腔镜联合腹腔镜手术治疗食管癌的短期随访结果比较. 中国胸心血管外科临床杂志, 2021, 28(2): 239-242.Fang YH, Chen ZH, Wei RQ, et al. Short-term follow-up results of inflatable mediastinoscopy with laparoscopy versus video-assisted thoracoscopic surgery combined with laparoscopy for esophageal cancer. Chin J Clin Thorac Cardiovasc Surg, 2021, 28(2): 239-242.
30. Liu C, Chen Z, Wei R, et al. Intra-operative events and countermeasures during esophagectomy via transcervical incision inflatable single-port mediastinoscope combined with laparoscopy. J Thorac Dis, 2021, 13(1): 133-139.
31. 宋尚岐, 胡杨, 徐昱扬, 等. 充气纵隔镜联合腹腔镜食管癌切除术的临床进展. 中华消化外科杂志, 2023, 22(4): 474-480.Song SQ, Hu Y, Xu YY, et al. Clinical progress of inflatable video-assisted mediastinoscopic transhiatal esophagectomy. Chin J Dig Surg, 2023, 22(4): 474-480.
32. Ajani JA, D'Amico TA, Bentrem DJ, et al. Esophageal and esophagogastric junction cancers, version 2. 2019, NCCN clinical practice guidelines in oncology. J Natl Compr Canc Netw, 2019, 17(7): 855-883.
33. 冷雪峰, 大幸宏幸, 韩泳涛. 食管鳞状细胞癌NCCN指南及JES指南外科诊疗要点解读. 肿瘤预防与治疗, 2024, 37(4): 286-291.Leng XF, Daiko H, Han YT. Interpretation of NCCN and JES guidelines for the treatment of esophageal squamous cell carcinoma. J Cancer Control Treat, 2024, 37(4): 286-291.
34. 中华人民共和国国家卫生健康委员会医政医管局. 食管癌诊疗指南 (2022年版). 中华消化外科杂志, 2022, 21(10): 1247-1268.Bureau of Medical Administration, National Health Commission of the People's Republic of China. Standardization for diagnosis and treatment of esophageal cancer (2022 edition). Chin J Dig Surg, 2022, 21(10): 1247-1268.
35. 柳常青, 吴汉然, 郭明发, 等. 改良充气式纵隔镜在早期胸段食管癌中的临床应用. 中华胸心血管外科杂志, 2019, 35(2): 80-85.Liu CQ, Wu HR, Guo MF, et al. Clinical application of modified inflatable video-assisted mediastinoscopic transhiatal esophagectomy in patients with early esophageal cancer. Chin J Thorac Cardiovasc Surg, 2019, 35(2): 80-85.
36. Tokairin Y, Nakajima Y, Kawada K, et al. The usefulness of a bilateral transcervical pneumomediastinal approach for mediastinoscopic radical esophagectomy: A right transcervical approach is an available option. Gen Thorac Cardiovasc Surg, 2019, 67(10): 884-890.

Chinese Journal of Clinical Thoracic and Cardiovascular Surgery

Latest ArticlesApplication of near-infrared fluorescence imaging of thoracic duct in inflatable video-assisted mediastinoscopic transhiatal esophagectomy: A propensity score matching study

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