Abstract
The prevalence of lymph node (LN) metastasis in esophageal cancer (EC) is widely spread to all three fields, namely, to the neck region, the mediastinal region and the abdominal region. Furthermore, the status of LN metastasis has been recognized as a key factor that influences the outcome after EC surgery. Therefore, the latest version of the UICC/AJCC TNM classification (7th edition) applied the number of metastatic LNs as an N factor. However, the precise clinical diagnosis of metastatic LNs is still difficult. This is mainly because there are many micrometastases in EC. Therefore, the Japanese Classification of Esophageal Cancer (10th edition) has not incorporated the number of LN metastases into the N factor for its staging system and the accurate preoperative diagnosis of LN status is currently one of the most important issues to be resolved for EC. Given the frequency and extent of LN metastasis and its significance for the survival, controlling LN metastasis is a rational therapeutic strategy, and an extended LN dissection, such as three-field lymph node dissection may be logical, although appropriate patient selection is necessary. On the other hand, recent arguments have supported a reduction of unnecessary LN dissection in esophagectomy. To curtail unnecessary LN dissection, one of the current topics is sentinel lymph node-guided surgery and is being investigated as part of the next generation surgeries for EC. In this article, recent literatures were reviewed and we discuss the current status of lymph node dissection in EC.
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References
Ozawa S, Tachimori Y, Baba H, et al. Comprehensive Registry of Esophageal Cancer in Japan, 2004. Esophagus. 2012;9(2):75–98.
Jemal A, Siegel R, Xu J, et al. Cancer statistics. CA Cancer J Clin. 2010;60(5):277–300.
Kayani B, Zacharakis E, Ahmed K, et al. Lymph node metastases and prognosis in oesophageal carcinoma—a systematic review. Eur J Surg Oncol. 2011;37(9):747–53.
Akutsu Y, Uesato M, Shuto K, et al. The overall prevalence of metastasis in T1 esophageal squamous cell carcinoma: a retrospective analysis of 295 patients. Ann Surg. 2012. doi:10.1097/SLA.0b013e31827017fc.
Sepesi B, Watson TJ, Zhou D, et al. Are endoscopic therapies appropriate for superficial submucosal esophageal adenocarcinoma? An analysis of esophagectomy specimens. J Am Coll Surg. 2010;210(4):418–27.
Liu L, Hofstetter WL, Rashid A, et al. Significance of the depth of tumor invasion and lymph node metastasis in superficially invasive (T1) esophageal adenocarcinoma. Am J Surg Pathol. 2005;29(8):1079–85.
Lerut T, Nafteux P, Moons J, et al. Three-field lymphadenectomy for carcinoma of the esophagus and gastroesophageal junction in 174 R0 resections: impact on staging, disease-free survival, and outcome: a plea for adaptation of TNM classification in upper-half esophageal carcinoma. Ann Surg. 2004;240(6):962–72. (discussion 972–4).
Hagen JA, DeMeester SR, Peters JH, et al. Curative resection for esophageal adenocarcinoma: analysis of 100 en bloc esophagectomies. Ann Surg. 2001;234(4):520–30 (discussion 530–1).
Takeno S, Yamashita SI, Yamamoto S, et al. Number of metastasis-positive lymph node stations is a simple and reliable prognostic factor following surgery in patients with esophageal cancer. Exp Ther Med. 2012;4(6):1087–91.
Rice TW. Superficial oesophageal carcinoma: is there a need for three-field lymphadenectomy? Lancet. 1999;354(9181):792–4.
Kuge K, Murakami G, Mizobuchi S, et al. Submucosal territory of the direct lymphatic drainage system to the thoracic duct in the human esophagus. J Thorac Cardiovasc Surg. 2003;125(6):1343–9.
Prenzel KL, Bollschweiler E, Schroder W, et al. Prognostic relevance of skip metastases in esophageal cancer. Ann Thorac Surg. 2010;90(5):1662–7.
Hosch SB, Stoecklein NH, Pichlmeier U, et al. Esophageal cancer: the mode of lymphatic tumor cell spread and its prognostic significance. J Clin Oncol. 2001;19(7):1970–5.
Ando N, Ozawa S, Kitagawa Y, et al. Improvement in the results of surgical treatment of advanced squamous esophageal carcinoma during 15 consecutive years. Ann Surg. 2000;232(2):225–32.
Tachimori Y, Nagai Y, Kanamori N, et al. Pattern of lymph node metastases of esophageal squamous cell carcinoma based on the anatomical lymphatic drainage system. Dis Esophagus. 2011;24(1):33–8.
Takubo K, Makuuchi H, Fujita H, et al. Japanese classification of esophageal cancer, tenth edition: part I. Esophagus. 2009;6:1–25.
Japan Esophageal Society. Japanese classification of esophageal cancer, tenth edition: parts II and III. Esophagus. 2009;6:71–94.
Akutsu Y, Matsubara H. The significance of lymph node status as a prognostic factor for esophageal cancer. Surg Today. 2011;41(9):1190–5.
Lin CS, Chang SC, Wei YH, et al. Prognostic variables in thoracic esophageal squamous cell carcinoma. Ann Thorac Surg. 2009;87(4):1056–65.
Natsugoe S, Matsumoto M, Okumura H, et al. Prognostic factors in patients with submucosal esophageal cancer. J Gastrointest Surg. 2004;8(5):631–5.
Shimada H, Okazumi S, Matsubara H, et al. Impact of the number and extent of positive lymph nodes in 200 patients with thoracic esophageal squamous cell carcinoma after three-field lymph node dissection. World J Surg. 2006;30(8):1441–9.
Akutsu Y, Shuto K, Kono T, et al. The number of pathologic lymph nodes involved is still a significant prognostic factor even after neoadjuvant chemoradiotherapy in esophageal squamous cell carcinoma. J Surg Oncol. 2012;105(8):756–60.
Gertler R, Stein HJ, Langer R, et al. Long-term outcome of 2920 patients with cancers of the esophagus and esophagogastric junction: evaluation of the New Union Internationale Contre le Cancer/American Joint Cancer Committee staging system. Ann Surg. 2011;253(4):689–98.
Zhang HL, Chen LQ, Liu RL, et al. The number of lymph node metastases influences survival and International Union against cancer tumor-node-metastasis classification for esophageal squamous cell carcinoma. Dis Esophagus. 2010;23(1):53–8.
Talsma K, van Hagen P, Grotenhuis BA, et al. Comparison of the 6th and 7th editions of the UICC-AJCC TNM classification for esophageal cancer. Ann Surg Oncol. 2012;19(7):2142–8.
Kajiyama Y, Iwanuma Y, Tomita N, et al. Size analysis of lymph node metastasis in esophageal cancer: diameter distribution and assessment of accuracy of preoperative diagnosis. Esophagus. 2006;3(4):189–95.
Chao YK, Liu HP, Hsieh MJ, et al. Impact of the number of lymph nodes sampled on outcome in ypT0N0 esophageal squamous cell carcinoma patients. J Surg Oncol. 2012;106(4):436–40.
Yang HX, Xu Y, Fu JH, et al. An evaluation of the number of lymph nodes examined and survival for node-negative esophageal carcinoma: data from China. Ann Surg Oncol. 2010;17(7):1901–11.
Groth SS, Virnig BA, Whitson BA, et al. Determination of the minimum number of lymph nodes to examine to maximize survival in patients with esophageal carcinoma: data from the Surveillance Epidemiology and End Results database. J Thorac Cardiovasc Surg. 2010;139(3):612–20.
Greenstein AJ, Litle VR, Swanson SJ, et al. Prognostic significance of the number of lymph node metastases in esophageal cancer. J Am Coll Surg. 2008;206(2):239–46.
Fox M, Farmer R, Scoggins CR, et al. Lymph node ratio is a significant predictor of disease-specific mortality in patients undergoing esophagectomy for cancer. Am Surg. 2012;78(5):528–34.
Hsu WH, Hsu PK, Hsieh CC, et al. The metastatic lymph node number and ratio are independent prognostic factors in esophageal cancer. J Gastrointest Surg. 2009;13(11):1913–20.
Korst RJ, Rusch VW, Venkatraman E, et al. Proposed revision of the staging classification for esophageal cancer. J Thorac Cardiovasc Surg. 1998;115(3):660–9 (discussion 669–70).
Hofstetter W, Correa AM, Bekele N, et al. Proposed modification of nodal status in AJCC esophageal cancer staging system. Ann Thorac Surg. 2007;84(2):365–73 (discussion 374–5).
Wilson M, Rosato EL, Chojnacki KA, et al. Prognostic significance of lymph node metastases and ratio in esophageal cancer. J Surg Res. 2008;146(1):11–5.
Bhamidipati CM, Stukenborg GJ, Thomas CJ, et al. Pathologic lymph node ratio is a predictor of survival in esophageal cancer. Ann Thorac Surg. 2012;94(5):1643–51.
Isono K, Sato H, Nakayama K. Results of a nationwide study on the three-field lymph node dissection of esophageal cancer. Oncology. 1991;48(5):411–20.
Akiyama H, Tsurumaru M, Udagawa H, et al. Radical lymph node dissection for cancer of the thoracic esophagus. Ann Surg. 1994;220(3):364–72 (discussion 372–3).
Lerut T, Coosemans W, De Leyn P, et al.Reflections on three field lymphadenectomy in carcinoma of the esophagus and gastroesophageal junction.Hepatogastroenterology.1999;46(26):717–25.
Baba M, Aikou T, Yoshinaka H, et al. Long-term results of subtotal esophagectomy with three-field lymphadenectomy for carcinoma of the thoracic esophagus. Ann Surg.1994;219(3):310–6.
Tachibana M, Kinugasa S, Yoshimura H, et al. Clinical outcomes of extended esophagectomy with three-field lymph node dissection for esophageal squamous cell carcinoma. Am J Surg. 2005;189(1):98–109.
Nishihira T, Hirayama K, Mori S. A prospective randomized trial of extended cervical and superior mediastinal lymphadenectomy for carcinoma of the thoracic esophagus. Am J Surg. 1998;175(1):47–51.
Udagawa H, Ueno M, Shinohara H, et al. The importance of grouping of lymph node stations and rationale of three-field lymphoadenectomy for thoracic esophageal cancer. J Surg Oncol. 2012;106(6):742–7.
Kato H, Tachimori Y, Watanabe H, et al. Recurrent esophageal carcinoma after esophagectomy with three-field lymph node dissection. J Surg Oncol. 1996;61(4):267–72.
Li H, Zhang Y, Cai H, et al. Pattern of lymph node metastases in patients with squamous cell carcinoma of the thoracic esophagus who underwent three-field lymphadenectomy. Eur Surg Res. 2007;39(1):1–6.
Grotenhuis BA, van Heijl M, Zehetner J, et al. Surgical management of submucosal esophageal cancer: extended or regional lymphadenectomy? Ann Surg. 2010;252(5):823–30.
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):355–9.
Fujita H, Kakegawa T, Yamana H, et al. Mortality and morbidity rates, postoperative course, quality of life, and prognosis after extended radical lymphadenectomy for esophageal cancer. Comparison of three-field lymphadenectomy with two-field lymphadenectomy. Ann Surg. 1995;222(5):654–62.
Kosugi SI, Kanda T, Yajima K, et al. Risk factors influencing the pleural drainage volume after transthoracic oesophagectomy. Eur J Cardiothorac Surg. 2012. doi:10.1093/ejcts/ezs556.
Morton DL, Thompson JF, Essner R, et al. Validation of the accuracy of intraoperative lymphatic mapping and sentinel lymphadenectomy for early-stage melanoma: a multicenter trial. Multicenter Selective Lymphadenectomy Trial Group. Ann Surg 1999;230(4):453–63 (discussion 463–5).
Krag D, Weaver D, Ashikaga T, et al. The sentinel node in breast cancer—a multicenter validation study. N Engl J Med. 1998;339(14):941–6.
Ichikura T, Sugasawa H, Sakamoto N, et al. Limited gastrectomy with dissection of sentinel node stations for early gastric cancer with negative sentinel node biopsy. Ann Surg. 2009;249(6):942–7.
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):540–50.
Burian M, Stein HJ, Sendler A, et al. Sentinel node detection in Barrett’s and cardia cancer. Ann Surg Oncol. 2004;11(Suppl 3):255S–8S.
Kim HK, Kim S, Park JJ, et al. Sentinel node identification using technetium-99 m neomannosyl human serum albumin in esophageal cancer. The Annals of thoracic surgery. 2011;91(5):1517–22.
Takeuchi H, Kawakubo H, Takeda F, et al. Sentinel Node Navigation Surgery in Early-Stage Esophageal Cancer. Annals of thoracic and cardiovascular surgery : official journal of the Association of Thoracic and Cardiovascular Surgeons of Asia 2012.
Yuasa Y, Seike J, Yoshida T, et al. Sentinel lymph node biopsy using intraoperative indocyanine green fluorescence imaging navigated with preoperative CT lymphography for superficial esophageal cancer. Ann Surg Oncol. 2012;19(2):486–93.
Tajima Y, Murakami M, Yamazaki K, et al. Sentinel node mapping guided by indocyanine green fluorescence imaging during laparoscopic surgery in gastric cancer. Ann Surg Oncol. 2010;17(7):1787–93.
Miyashiro I, Miyoshi N, Hiratsuka M, et al. Detection of sentinel node in gastric cancer surgery by indocyanine green fluorescence imaging: comparison with infrared imaging. Ann Surg Oncol. 2008;15(6):1640–3.
Yoshida M, Kubota K, Kuroda J, et al. Indocyanine green injection for detecting sentinel nodes using color fluorescence camera in the laparoscopy-assisted gastrectomy. J Gastroenterol Hepatol. 2012;27(Suppl 3):29–33.
Kitai T, Inomoto T, Miwa M, et al. Fluorescence navigation with indocyanine green for detecting sentinel lymph nodes in breast cancer. Breast cancer. 2005;12(3):211–5.
Rossi EC, Ivanova A, Boggess JF. Robotically assisted fluorescence-guided lymph node mapping with ICG for gynecologic malignancies: a feasibility study. Gynecol Oncol. 2012;124(1):78–82.
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The review was submitted at the invitation of the editorial committee.
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Akutsu, Y., Matsubara, H. Lymph node dissection for esophageal cancer. Gen Thorac Cardiovasc Surg 61, 397–401 (2013). https://doi.org/10.1007/s11748-013-0237-1
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DOI: https://doi.org/10.1007/s11748-013-0237-1