Current situation of lymphatic chemotherapy in esophageal cancer_Chinese Journal of Clinical Thoracic and Cardiovascular Surgery

Authors：

CAI Jie , NI Pengzhi , WANG Wenping , ZHENG Xi ,  CHEN Longqi

Department of Thoracic Surgery, West China Hospital, Sichuan University, Chengdu, 610041, P.R.China;

Corresponding?author：

CHEN Longqi, Email: drchenlq@scu.edu.cn

Keywords：

Lymphatic chemotherapy; esophageal cancer; nano carbon

DOI：

10.7507/1007-4848.201605002

Video：

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Lymphatic metastasis of esophageal cancer is one of the main ways of esophageal cancer metastasis and it is as well one of the most important factors influencing the prognosis of esophageal cancer patients. Compared to intravenous administration of chemotherapy, local chemotherapy has the less toxicity and less systemic side effects. Nano carbon is a safe and effective carrier for intraoperative lymphatic chemotherapy. It plays an important role in tracing and targeting lymph node during the lymphatic chemotherapy. Lymphatic chemotherapy can induce tumor into necrosis and apoptosis. For esophageal cancer, lymphatic chemotherapy is also to be proved to improve the rate of lymph node dissection and the number of metastatic lymph nodes, decrease tumor size, improve the quality of life and survival rate. In conclusion, lymphatic chemotherapy can be considered an assistant therapy to eliminate the tumor cell in lymph nodes and micrometastatic foci. In this review, the metastatic characteristic of esophageal cancer, the significance, mechanism and application of lymphatic chemotherapy carried by nano carbon are summarized.

Citation： CAI Jie, NI Pengzhi, WANG Wenping, ZHENG Xi, CHEN Longqi. Current situation of lymphatic chemotherapy in esophageal cancer. Chinese Journal of Clinical Thoracic and Cardiovascular Surgery, 2017, 24(8): 635-639. doi: 10.7507/1007-4848.201605002 Copy

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2.	Torre LA, Bray F, Siegel RL, et al. Global cancer statistics, 2012. CA, 2015, 65(2): 87-108.
3.	Lee SJ, Lee KS, Yim YJ, et al. Recurrence of squamous cell carcinoma of the oesophagus after curative surgery: rates and patterns on imaging studies correlated with tumour location and pathological stage. Clin Radiol, 2005, 60(5): 547-554.
4.	Altorki N. Skinner D. Should en bloc esophagectomy be the standard of care for esophageal carcinoma? Ann Surg, 2001, 234(5): 581-587.
5.	Liao Z, Cox JD, Komaki R. Radiochemotherapy of esophageal cancer. J Thorac Oncol, 2007, 2(6): 553-568.
6.	Ito K, Kiriyama K, Watanabe T, et al. A newly developed drug delivery system using fine particles of activated charcoal for targeting chemotherapy. ASAIO Trans, 1990, 36(3): M199-M202.
7.	Hagiwara A, Takahashi T. A new drug-delivery-system of anticancer agents: activated carbon particles adsorbing anticancer agentsJ. In vivo (Athens, Greece), 1987, 1(4): 241-252.
8.	沓仁芝, 陳濟民, 姚崇舜. 淋巴靶向制劑——吸附抗癌藥毫微粒活性炭的研究進展. 沈陽藥科大學學報, 2002, 19(1): 66-69.
9.	Stein HJ, Marcus F, Bruecher BLDM, et al. Early esophageal cancer: pattern of lymphatic spread and prognostic factors for long-term survival after surgical resection. Ann Surg, 2005, 242(4): 573-575.
10.	Natsugoe S, Mueller J, Stein HJ, et al. Micrometastasis and tumor cell microinvolvement of lymph nodes from esophageal squamous cell carcinoma: frequency, associated tumor characteristics, and impact on prognosis. Cancer, 1998, 83(5): 858-866.
11.	Li SH, Wang Z, Liu XY, et al. Lymph node micrometastasis: a predictor of early tumor relapse after complete resection of histologically node-negative esophageal cancer. Surg Today, 2007, 37(12): 1047-1052.
12.	Bonavina L, Ferrero S, Midolo V, et al. Lymph node micrometastases in patients with adenocarcinoma of the esophagogastric junction. J Gastrointest Surg, 1999, 3(5): 468-476.
13.	Qubain SW, Natsugoe S, Matsumoto M, et al. Micrometastases in the cervical lymph nodes in esophageal squamous cell carcinoma. Dis Esophagus, 2001, 14(2): 143-148.
14.	Mueller JD, Stein HJ, Oyang T, et al. Frequency and clinical impact of lymph node micrometastasis and tumor cell microinvolvement in patients with adenocarcinoma of the esophagogastric junction. Cancer, 2000, 89(9): 1874-1882.
15.	Wlodarczyk J, Mueller J, Wlodarczyk J. Lymph node micrometastases of adenocarcinoma located in gastroesophagal junction. Polish J Pathol, 2013, 64(3): 170-174.
16.	Glickman JN, Torres C, Wang HH, et al. The prognostic significance of lymph node micrometastasis in patients with esophageal carcinoma. Cancer, 1999, 85(4): 769-778.
17.	Sato F, Shimada Y, Li Z, et al. Lymph node micrometastasis and prognosis in patients with oesophageal squamous cell carcinoma. Br J Surg, 2001, 88(3): 426-432.
18.	Blom RL, Lagarde SM, van Oudenaarde K, et al. Survival after recurrent esophageal carcinoma has not improved over the past 18 years. Ann Surg Oncol, 2013, 20(8): 2693-2698.
19.	Morita M, Kuwano H, Ohno S, et al. Characteristics and sequence of the recurrent patterns after curative esophagectomy for squamous cell carcinoma. Surg, 1994, 116(1): 1-7.
20.	Bhansali MS, Fujita H, Kakegawa T, et al. Pattern of recurrence after extended radical esophagectomy with three-field lymph node dissection for squamous cell carcinoma in the thoracic esophagus. World J Surg, 1997, 21(3): 275-281.
21.	Fujita H, Kakegawa T, Yamana H, et al. Lymph node metastasis and recurrence in patients with a carcinoma of the thoracic esophagus who underwent three-field dissection. World J Surg, 1994, 18(2): 266-272.
22.	Chen G, Wang Z, Liu XY, et al. Recurrence pattern of squamous cell carcinoma in the middle thoracic esophagus after modified Ivor-Lewis esophagectomy. World J Surg, 2007, 31(5): 1107-1114.
23.	de Manzoni G, Pedrazzani C, Pasini F, et al. Pattern of recurrence after surgery in adenocarcinoma of the gastro-oesophageal junction. Euro J Surg Oncol, 2003, 29(6): 506-510.
24.	Nakagawa S, Kanda T, Kosugi S, et al. Recurrence pattern of squamous cell carcinoma of the thoracic esophagus after extended radical esophagectomy with three-field lymphadenectomy. J Am Coll Surg, 2004, 198(2): 205-211.
25.	Li CL, Zhang FL, Wang YD, et al. Characteristics of recurrence after radical esophagectomy with two-field lymph node dissection for thoracic esophageal cancer. Oncol Lett, 2013, 5(1): 355-359.
26.	Su XD, Zhang DK, Zhang X, et al. Prognostic factors in patients with recurrence after complete resection of esophageal squamous cell carcinoma. J Thorac Dis, 2014, 6(7): 949-957.
27.	Mariette C, Balon JM, Piessen G, et al. Pattern of recurrence following complete resection of esophageal carcinoma and factors predictive of recurrent disease. Cancer, 2003, 97(7): 1616-1623.
28.	Guo XF, Mao T, Gu ZT, et al. Clinical study on postoperative recurrence in patients with pN0 esophageal squamous cell carcinoma. J Cardiothorac Surg, 2014, 9: 150.
29.	Hosokawa Y, Kinoshita T, Konishi M, et al. Recurrence patterns of esophagogastric junction adenocarcinoma according to Siewert’s classification after radical resection. Anticancer Res, 2014, 34(8): 4391-4397.
30.	蘇曉暉, 李榮年. 緩釋靶向模式的胃癌藥物. 中國組織工程研究與臨床康復, 2011, 15(25): 4711-4714.
31.	李偉, 徐亮. 納米炭在胃癌淋巴靶向化療中的應用研究進展. 瀘州醫學院學報, 2009, 32(4): 439-441.
32.	董怡民, 沓小容, 姚崇舜, 等. 納米活性炭對氟尿嘧啶的吸附和緩釋作用的實驗研究. 中國醫科大學學報, 2004, 33(3): 205-206, 211.
33.	曲秋蓮, 張英鴿, 楊留中, 等. 納米活性炭吸附絲裂霉素 C 腹腔化療的實驗研究. 中華腫瘤雜志. 2006, 28(4): 257-260.
34.	張李, 王曉娜, 丁學偉, 等. 納米炭吸附絲裂霉素 C 腹腔化療的實驗研究. 中華腫瘤防治雜志, 2008, 15(7): 503-506.
35.	徐松琳, 王東凱, 高斐, 等. 順鉑納米炭混懸劑的制備及體外釋藥性質. 中國醫藥工業雜志, 2005, 36(11): 685-687.
36.	Nakase Y, Hagiwara A, Kin S, et al. Intratumoral administration of methotrexate bound to activated carbon particles: antitumor effectiveness against human colon carcinoma xenografts and acute toxicity in mice. J Pharmacol Experiment Therap, 2004, 311(1): 382-387.
37.	Fujiyama J, Nakase Y, Mochizuki S, et al. Fundamental studies on locally injected methotrexate bound to activated carbon particles (MTX-CH). Gan To Kagaku Ryoho, 2004, 31(11): 1844-1846.
38.	Nakase Y, Kin S, Fukuda K, et al. Intratumoral administration of methotrexate bound to activated carbon particles (MTX-CH) inducing antitumor effect in vivo. Gan To Kagaku Ryoho, 2003, 30(11): 1859-1861.
39.	Hagiwara A, Takahashi T, Sawai K, et al. Lymph nodal vital staining with newer carbon particle suspensions compared with India ink: experimental and clinical observations. Lymphology, 1992, 25(2): 84-89.
40.	Yokota T, Saito T, Narushima Y, et al. Lymph-node staining with activated carbon CH40: a new method for axillary lymph-node dissection in breast cancer. Can J Surg, 2000, 43(3): 191-196.
41.	Okamoto K, Sawai K, Minato H, et al. Number and anatomical extent of lymph node metastases in gastric cancer: analysis using intra-lymph node injection of activated carbon particles (CH40). Jpn J Clin Oncol, 1999, 29(2): 74-77.
42.	Kitamura K, Yamane T, Oyama T, et al. Rapid and accurate method for delineating cancer lesions in laparoscopic colectomy using activated carbon injection. J Surg Oncol, 1995, 58(1): 31-34.
43.	李紅強, 殷德濤, 王勇飛, 等. 納米碳混懸液在甲狀腺乳頭狀癌中央區淋巴結清掃中療效評價. 中華內分泌外科雜志, 2015, 9(5): 398-400.
44.	蒲敏, 黃斌, 任明揚, 等. 納米炭在腹腔鏡下食管胃交界腺癌手術中的應用. 中國普外基礎與臨床雜志, 2013, 20(2): 147-151.
45.	李偉, 曾曉華, 徐發良, 等. 納米炭吸附多西紫杉醇在乳腺癌區域淋巴化療中的臨床研究. 重慶醫學, 2015, (7): 907-909, 912.
46.	Kin S, Nakase Y, Fukuda K, et al. Endoscopic local injection of anticancer drugs bound to carbon particles for treatment of advanced rectal cancer, when surgical treatment was contraindicated. Gan To Kagaku Ryoho, 2002, 29(12): 2413-2415.
47.	Hagiwara A, Togawa T, Yamasaki J, et al. Extensive gastrectomy and carbon-adsorbed mitomycin C for gastric cancer with peritoneal metastases. Case reports of survivors and their implications. Hepatogastroenterology, 1999, 46(27): 1673-1677.
48.	黃斌, 李昂, 張波, 等. 納米炭吸附 5-FU 淋巴靶向化療對胃癌組織及轉移淋巴結 bcl-2、bax 及 caspase-3 表達的影響. 中國普外基礎與臨床雜志, 2009, 16(1): 18-22.
49.	Chen J, Wang L, Yao Q. Drug concentrations in axillary lymph nodes after lymphatic chemotherapy on patients with breast cancer. Breast Cancer Research Bcr, 2004, 6(4): R474-R477.
50.	Hagiwara A, Torii T, Sakakura C, et al. Local injection of anti-cancer drugs bound to carbon particles for early gastric cancer--a pilot study. Hepato-gastroenterology, 2000, 47(32): 575-578.
51.	Guo F, Mao X, Wang J, et al. Gemcitabine adsorbed onto carbon particles increases drug concentrations at the injection site and in the regional lymph nodes in an animal experiment and a clinical study. J Inter Med Res, 2011, 39(6): 2217-2227.
52.	Shimada M, Natsugoe S, Kumanohoso T, et al. Chief Editor. Local Chemotherapy of Esophageal Cancer with Bleomycin Adsorbed to Activated Carbon Particles: Springer Japan, 1993. 905-910.
53.	Hirao E, Saito T, Kobayashi M. Selective delivery of pepleomycin to esophageal lymph nodes by activated carbon particles. Antican Res, 1993, 13(4): 991-994.
54.	Oyama T, Sakakibara T, Ozaki K, et al. Local injection of peplomycin adsorbed on activated carbon particles combined with 60Co radiation against inoperable advanced esophageal cancer--two long-term survivors. Gan to Kagaku Ryoho, 1993, 20(11): 1710-1712.
55.	Natsugoe S, Aikou T, Shimada M, et al. Loco-regional treatment for esophageal cancer with bleomycin adsorbed to activated carbon particles. Antican Res, 1993, 13(5c): 1785-1787.
56.	Hagiwara A, Takahashi T, Kojima O, et al. Endoscopic local injection of a new drug-delivery format of peplomycin for superficial esophageal cancer: a pilot study. Gastroenterol, 1993, 104(4): 1037-1043.
57.	Kitamura K, Hagiwara A, Sasabe T, et al. Significant clinical response of activated carbon adsorbed-peplomycin against esophageal cancer: a pilot study. J Surg Oncol, 1993, 52(1): 56-60.
58.	許天文, 林建清, 郭啟祥, 等. 順鉑納米炭示蹤劑在食管癌手術中的應用. 中華實驗外科雜志, 2015, 32(12): 3209-3210.
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61.	Singh I, Swami R, Khan W, et al. Lymphatic system: a prospective area for advanced targeting of particulate drug carriers. Expert Opin Drug Deliv, 2014, 11(2): 211-229.

1. Faiyaz M. Esophageal cancer. NEJM, 2004, 350(13): 1363-1364.
2. Torre LA, Bray F, Siegel RL, et al. Global cancer statistics, 2012. CA, 2015, 65(2): 87-108.
3. Lee SJ, Lee KS, Yim YJ, et al. Recurrence of squamous cell carcinoma of the oesophagus after curative surgery: rates and patterns on imaging studies correlated with tumour location and pathological stage. Clin Radiol, 2005, 60(5): 547-554.
4. Altorki N. Skinner D. Should en bloc esophagectomy be the standard of care for esophageal carcinoma? Ann Surg, 2001, 234(5): 581-587.
5. Liao Z, Cox JD, Komaki R. Radiochemotherapy of esophageal cancer. J Thorac Oncol, 2007, 2(6): 553-568.
6. Ito K, Kiriyama K, Watanabe T, et al. A newly developed drug delivery system using fine particles of activated charcoal for targeting chemotherapy. ASAIO Trans, 1990, 36(3): M199-M202.
7. Hagiwara A, Takahashi T. A new drug-delivery-system of anticancer agents: activated carbon particles adsorbing anticancer agentsJ. In vivo (Athens, Greece), 1987, 1(4): 241-252.
8. 沓仁芝, 陳濟民, 姚崇舜. 淋巴靶向制劑——吸附抗癌藥毫微粒活性炭的研究進展. 沈陽藥科大學學報, 2002, 19(1): 66-69.
9. Stein HJ, Marcus F, Bruecher BLDM, et al. Early esophageal cancer: pattern of lymphatic spread and prognostic factors for long-term survival after surgical resection. Ann Surg, 2005, 242(4): 573-575.
10. Natsugoe S, Mueller J, Stein HJ, et al. Micrometastasis and tumor cell microinvolvement of lymph nodes from esophageal squamous cell carcinoma: frequency, associated tumor characteristics, and impact on prognosis. Cancer, 1998, 83(5): 858-866.
11. Li SH, Wang Z, Liu XY, et al. Lymph node micrometastasis: a predictor of early tumor relapse after complete resection of histologically node-negative esophageal cancer. Surg Today, 2007, 37(12): 1047-1052.
12. Bonavina L, Ferrero S, Midolo V, et al. Lymph node micrometastases in patients with adenocarcinoma of the esophagogastric junction. J Gastrointest Surg, 1999, 3(5): 468-476.
13. Qubain SW, Natsugoe S, Matsumoto M, et al. Micrometastases in the cervical lymph nodes in esophageal squamous cell carcinoma. Dis Esophagus, 2001, 14(2): 143-148.
14. Mueller JD, Stein HJ, Oyang T, et al. Frequency and clinical impact of lymph node micrometastasis and tumor cell microinvolvement in patients with adenocarcinoma of the esophagogastric junction. Cancer, 2000, 89(9): 1874-1882.
15. Wlodarczyk J, Mueller J, Wlodarczyk J. Lymph node micrometastases of adenocarcinoma located in gastroesophagal junction. Polish J Pathol, 2013, 64(3): 170-174.
16. Glickman JN, Torres C, Wang HH, et al. The prognostic significance of lymph node micrometastasis in patients with esophageal carcinoma. Cancer, 1999, 85(4): 769-778.
17. Sato F, Shimada Y, Li Z, et al. Lymph node micrometastasis and prognosis in patients with oesophageal squamous cell carcinoma. Br J Surg, 2001, 88(3): 426-432.
18. Blom RL, Lagarde SM, van Oudenaarde K, et al. Survival after recurrent esophageal carcinoma has not improved over the past 18 years. Ann Surg Oncol, 2013, 20(8): 2693-2698.
19. Morita M, Kuwano H, Ohno S, et al. Characteristics and sequence of the recurrent patterns after curative esophagectomy for squamous cell carcinoma. Surg, 1994, 116(1): 1-7.
20. Bhansali MS, Fujita H, Kakegawa T, et al. Pattern of recurrence after extended radical esophagectomy with three-field lymph node dissection for squamous cell carcinoma in the thoracic esophagus. World J Surg, 1997, 21(3): 275-281.
21. Fujita H, Kakegawa T, Yamana H, et al. Lymph node metastasis and recurrence in patients with a carcinoma of the thoracic esophagus who underwent three-field dissection. World J Surg, 1994, 18(2): 266-272.
22. Chen G, Wang Z, Liu XY, et al. Recurrence pattern of squamous cell carcinoma in the middle thoracic esophagus after modified Ivor-Lewis esophagectomy. World J Surg, 2007, 31(5): 1107-1114.
23. de Manzoni G, Pedrazzani C, Pasini F, et al. Pattern of recurrence after surgery in adenocarcinoma of the gastro-oesophageal junction. Euro J Surg Oncol, 2003, 29(6): 506-510.
24. Nakagawa S, Kanda T, Kosugi S, et al. Recurrence pattern of squamous cell carcinoma of the thoracic esophagus after extended radical esophagectomy with three-field lymphadenectomy. J Am Coll Surg, 2004, 198(2): 205-211.
25. Li CL, Zhang FL, Wang YD, et al. Characteristics of recurrence after radical esophagectomy with two-field lymph node dissection for thoracic esophageal cancer. Oncol Lett, 2013, 5(1): 355-359.
26. Su XD, Zhang DK, Zhang X, et al. Prognostic factors in patients with recurrence after complete resection of esophageal squamous cell carcinoma. J Thorac Dis, 2014, 6(7): 949-957.
27. Mariette C, Balon JM, Piessen G, et al. Pattern of recurrence following complete resection of esophageal carcinoma and factors predictive of recurrent disease. Cancer, 2003, 97(7): 1616-1623.
28. Guo XF, Mao T, Gu ZT, et al. Clinical study on postoperative recurrence in patients with pN0 esophageal squamous cell carcinoma. J Cardiothorac Surg, 2014, 9: 150.
29. Hosokawa Y, Kinoshita T, Konishi M, et al. Recurrence patterns of esophagogastric junction adenocarcinoma according to Siewert’s classification after radical resection. Anticancer Res, 2014, 34(8): 4391-4397.
30. 蘇曉暉, 李榮年. 緩釋靶向模式的胃癌藥物. 中國組織工程研究與臨床康復, 2011, 15(25): 4711-4714.
31. 李偉, 徐亮. 納米炭在胃癌淋巴靶向化療中的應用研究進展. 瀘州醫學院學報, 2009, 32(4): 439-441.
32. 董怡民, 沓小容, 姚崇舜, 等. 納米活性炭對氟尿嘧啶的吸附和緩釋作用的實驗研究. 中國醫科大學學報, 2004, 33(3): 205-206, 211.
33. 曲秋蓮, 張英鴿, 楊留中, 等. 納米活性炭吸附絲裂霉素 C 腹腔化療的實驗研究. 中華腫瘤雜志. 2006, 28(4): 257-260.
34. 張李, 王曉娜, 丁學偉, 等. 納米炭吸附絲裂霉素 C 腹腔化療的實驗研究. 中華腫瘤防治雜志, 2008, 15(7): 503-506.
35. 徐松琳, 王東凱, 高斐, 等. 順鉑納米炭混懸劑的制備及體外釋藥性質. 中國醫藥工業雜志, 2005, 36(11): 685-687.
36. Nakase Y, Hagiwara A, Kin S, et al. Intratumoral administration of methotrexate bound to activated carbon particles: antitumor effectiveness against human colon carcinoma xenografts and acute toxicity in mice. J Pharmacol Experiment Therap, 2004, 311(1): 382-387.
37. Fujiyama J, Nakase Y, Mochizuki S, et al. Fundamental studies on locally injected methotrexate bound to activated carbon particles (MTX-CH). Gan To Kagaku Ryoho, 2004, 31(11): 1844-1846.
38. Nakase Y, Kin S, Fukuda K, et al. Intratumoral administration of methotrexate bound to activated carbon particles (MTX-CH) inducing antitumor effect in vivo. Gan To Kagaku Ryoho, 2003, 30(11): 1859-1861.
39. Hagiwara A, Takahashi T, Sawai K, et al. Lymph nodal vital staining with newer carbon particle suspensions compared with India ink: experimental and clinical observations. Lymphology, 1992, 25(2): 84-89.
40. Yokota T, Saito T, Narushima Y, et al. Lymph-node staining with activated carbon CH40: a new method for axillary lymph-node dissection in breast cancer. Can J Surg, 2000, 43(3): 191-196.
41. Okamoto K, Sawai K, Minato H, et al. Number and anatomical extent of lymph node metastases in gastric cancer: analysis using intra-lymph node injection of activated carbon particles (CH40). Jpn J Clin Oncol, 1999, 29(2): 74-77.
42. Kitamura K, Yamane T, Oyama T, et al. Rapid and accurate method for delineating cancer lesions in laparoscopic colectomy using activated carbon injection. J Surg Oncol, 1995, 58(1): 31-34.
43. 李紅強, 殷德濤, 王勇飛, 等. 納米碳混懸液在甲狀腺乳頭狀癌中央區淋巴結清掃中療效評價. 中華內分泌外科雜志, 2015, 9(5): 398-400.
44. 蒲敏, 黃斌, 任明揚, 等. 納米炭在腹腔鏡下食管胃交界腺癌手術中的應用. 中國普外基礎與臨床雜志, 2013, 20(2): 147-151.
45. 李偉, 曾曉華, 徐發良, 等. 納米炭吸附多西紫杉醇在乳腺癌區域淋巴化療中的臨床研究. 重慶醫學, 2015, (7): 907-909, 912.
46. Kin S, Nakase Y, Fukuda K, et al. Endoscopic local injection of anticancer drugs bound to carbon particles for treatment of advanced rectal cancer, when surgical treatment was contraindicated. Gan To Kagaku Ryoho, 2002, 29(12): 2413-2415.
47. Hagiwara A, Togawa T, Yamasaki J, et al. Extensive gastrectomy and carbon-adsorbed mitomycin C for gastric cancer with peritoneal metastases. Case reports of survivors and their implications. Hepatogastroenterology, 1999, 46(27): 1673-1677.
48. 黃斌, 李昂, 張波, 等. 納米炭吸附 5-FU 淋巴靶向化療對胃癌組織及轉移淋巴結 bcl-2、bax 及 caspase-3 表達的影響. 中國普外基礎與臨床雜志, 2009, 16(1): 18-22.
49. Chen J, Wang L, Yao Q. Drug concentrations in axillary lymph nodes after lymphatic chemotherapy on patients with breast cancer. Breast Cancer Research Bcr, 2004, 6(4): R474-R477.
50. Hagiwara A, Torii T, Sakakura C, et al. Local injection of anti-cancer drugs bound to carbon particles for early gastric cancer--a pilot study. Hepato-gastroenterology, 2000, 47(32): 575-578.
51. Guo F, Mao X, Wang J, et al. Gemcitabine adsorbed onto carbon particles increases drug concentrations at the injection site and in the regional lymph nodes in an animal experiment and a clinical study. J Inter Med Res, 2011, 39(6): 2217-2227.
52. Shimada M, Natsugoe S, Kumanohoso T, et al. Chief Editor. Local Chemotherapy of Esophageal Cancer with Bleomycin Adsorbed to Activated Carbon Particles: Springer Japan, 1993. 905-910.
53. Hirao E, Saito T, Kobayashi M. Selective delivery of pepleomycin to esophageal lymph nodes by activated carbon particles. Antican Res, 1993, 13(4): 991-994.
54. Oyama T, Sakakibara T, Ozaki K, et al. Local injection of peplomycin adsorbed on activated carbon particles combined with 60Co radiation against inoperable advanced esophageal cancer--two long-term survivors. Gan to Kagaku Ryoho, 1993, 20(11): 1710-1712.
55. Natsugoe S, Aikou T, Shimada M, et al. Loco-regional treatment for esophageal cancer with bleomycin adsorbed to activated carbon particles. Antican Res, 1993, 13(5c): 1785-1787.
56. Hagiwara A, Takahashi T, Kojima O, et al. Endoscopic local injection of a new drug-delivery format of peplomycin for superficial esophageal cancer: a pilot study. Gastroenterol, 1993, 104(4): 1037-1043.
57. Kitamura K, Hagiwara A, Sasabe T, et al. Significant clinical response of activated carbon adsorbed-peplomycin against esophageal cancer: a pilot study. J Surg Oncol, 1993, 52(1): 56-60.
58. 許天文, 林建清, 郭啟祥, 等. 順鉑納米炭示蹤劑在食管癌手術中的應用. 中華實驗外科雜志, 2015, 32(12): 3209-3210.
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Chinese Journal of Clinical Thoracic and Cardiovascular Surgery

Current situation of lymphatic chemotherapy in esophageal cancer

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