Supraclavicular lymph node metastasis should not be defined as regional lymph node metastasis in cervical and upper thoracic esophageal squamous cell carcinoma

Zeng,Hai; Zhu,Min; Sun,Yujiao; Deng,Li; Fu,Weiyang; Li,Shuang; Xiang,Ying; Zhang,Weijia

doi:10.3892/ol.2024.14595

Supraclavicular lymph node metastasis should not be defined as regional lymph node metastasis in cervical and upper thoracic esophageal squamous cell carcinoma

Authors:
- Hai Zeng
- Min Zhu
- Yujiao Sun
- Li Deng
- Weiyang Fu
- Shuang Li
- Ying Xiang
- Weijia Zhang
View Affiliations

Affiliations: Department of Oncology, First Affiliated Hospital of Yangtze University, Jingzhou, Hubei 434000, P.R. China, Second Clinical College, Medical School of Yangtze University, Jingzhou, Hubei 434000, P.R. China, Department of Medicine, First Affiliated Hospital of Yangtze University, Jingzhou, Hubei 434000, P.R. China
Published online on: July 26, 2024 https://doi.org/10.3892/ol.2024.14595
Article Number: 462
Copyright: © Zeng et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )

Metrics: Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )

Cited By (CrossRef): 0 citations Loading Articles...

Abstract

The importance of supraclavicular lymph node (SCLN) metastasis in cervical and upper thoracic esophageal squamous cell carcinoma (ESCC) has not been determined. The aim of the present study was to provide a detailed definition of the range of SCLN regions and to explore whether SCLNs should be considered as a regional lymph nodes for patients with cervical and upper thoracic ESCC. A retrospective analysis was performed on 230 patients with locally advanced cervical or upper thoracic ESCC who underwent radical radiotherapy and chemotherapy. The range of SCLN regions was defined in detail on contrast enhanced computed tomography images of the neck. According to whether the patient had lymph node metastasis in the supraclavicular region, the included patients were divided into two groups, and the survival differences and reasons for treatment failure between the two groups were analyzed. Of the 230 patients with ESCC, 71 (30.87%) exhibited lymph node metastases in the supraclavicular region. The median overall survival time of ESCC patients with and without SCLN metastasis was 17 and 30 months, respectively (P<0.001). After propensity score matching (PSM), the median overall survival time of ESCC patients with and without SCLN metastasis was 17 and 28 months, respectively (P<0.001). During the follow‑up period, there were a total of 101 cases of failure of treatment in the irradiation field, 6 cases had esophageal metastasis in the non‑irradiated field and 27 cases had regional lymph node metastasis in the non‑irradiated field. In addition, there were 33 cases of metastasis to the distant lymph nodes or organs. There was no significant difference in the local treatment failure rate between the groups with or without SCLN metastasis in both the irradiation field and the non‑irradiation field, but the probability of distant metastasis in the SCLN metastasis group was significantly higher than that in the group without SCLN metastasis (P=0.025). In conclusion, patients with cervical and upper thoracic ESCC with SCLN metastasis have a poor prognosis and the median overall survival time is closer to that of metastatic ESCC than ESCC with regional lymph node metastasis; therefore, SCLNs should not be defined as regional lymph nodes in patients with cervical and upper thoracic ESCC.

View Figures

View References

1	Morgan E, Soerjomataram I, Rumgay H, Coleman HG, Thrift AP, Vignat J, Laversanne M, Ferlay J and Arnold M: The global landscape of esophageal squamous cell carcinoma and esophageal adenocarcinoma incidence and mortality in 2020 and projections to 2040: New estimates from GLOBOCAN 2020. Gastroenterology. 163:649–658.e2. 2022. View Article : Google Scholar : PubMed/NCBI
2	Zheng RS, Chen R, Han BF, Wang SM, Li L, Sun KX, Zeng HM, Wei WW and He J: Cancer incidence and mortality in China, 2022. Zhonghua Zhong Liu Za Zhi. 46:221–231. 2024.(In Chinese). PubMed/NCBI
3	Verstegen MH, Harker M, van de Water C, van Dieren J, Hugen N, Nagtegaal ID, Rosman C and van der Post RS: Metastatic pattern in esophageal and gastric cancer: Influenced by site and histology. World J Gastroenterol. 26:6037–6046. 2020. View Article : Google Scholar : PubMed/NCBI
4	Wang H, Tang H, Fang Y, Tan L, Yin J, Shen Y, Zeng Z, Zhu J, Hou Y, Du M, et al: Morbidity and mortality of patients who underwent minimally invasive esophagectomy after neoadjuvant chemoradiotherapy vs neoadjuvant chemotherapy for locally advanced esophageal squamous cell carcinoma: A randomized clinical trial. JAMA Surg. 156:444–451. 2021. View Article : Google Scholar : PubMed/NCBI
5	Rice TW, Gress DM, Patil DT, Hofstetter WL, Kelsen DP and Blackstone EH: Cancer of the esophagus and esophagogastric junction-major changes in the American joint committee on cancer eighth edition cancer staging manual. CA Cancer J Clin. 67:304–317. 2017. View Article : Google Scholar : PubMed/NCBI
6	Wang F, Ge X, Wang Z, Weng Y, Yin R and You Q: Clinical significance and prognosis of supraclavicular lymph node metastasis in patients with thoracic esophageal cancer. Ann Transl Med. 8:902020. View Article : Google Scholar : PubMed/NCBI
7	Park SY, Lee J, Jeon YJ, Cho JH, Kim HK, Choi YS, Zo JI and Shim YM: Clinical and pathologic supraclavicular lymph node metastases in esophageal squamous cell carcinoma treated by esophagectomy with three-field lymph node dissection. Ann Surg Oncol. 31:3399–3408. 2024. View Article : Google Scholar : PubMed/NCBI
8	Mine S, Tanaka K, Kawachi H, Shirakawa Y, Kitagawa Y, Toh Y, Yasuda T, Watanabe M, Kamei T, Oyama T, et al: Japanese classification of esophageal cancer, 12th edition: Part I. Esophagus. 21:179–215. 2024. View Article : Google Scholar : PubMed/NCBI
9	Numata Y, Abe T, Higaki E, Hosoi T, Fujieda H, Nagao T, Hanai N, Suzuki H, Nishikawa D, Matsuo K, et al: Should the supraclavicular lymph nodes be considered regional lymph nodes in cervical esophageal cancer? Ann Surg Oncol. 29:616–626. 2022. View Article : Google Scholar : PubMed/NCBI
10	Yu Y, Xu L, Chen X, Li H, Liu Q, Zhang R, Xie H, Chen Y, Yuan L, Tan B, et al: Neoadjuvant therapy combined with surgery is superior to chemoradiotherapy in esophageal squamous cell cancer patients with resectable supraclavicular lymph node metastasis: A propensity score-matched analysis. Ann Transl Med. 10:3492022. View Article : Google Scholar : PubMed/NCBI
11	Tachimori Y, Ozawa S, Numasaki H, Matsubara H, Shinoda M, Toh Y and Udagawa H; Registration Committee for Esophageal Cancer of the Japan Esophageal Society, : Supraclavicular node metastasis from thoracic esophageal carcinoma: A surgical series from a Japanese multi-institutional nationwide registry of esophageal cancer. J Thorac Cardiovasc Surg. 148:1224–1229. 2014. View Article : Google Scholar : PubMed/NCBI
12	Patel DC, Yang CJ, Liou DZ and Berry MF: Treatment and outcomes of proximal esophageal squamous cell carcinoma. Ann Surg Oncol. 30:818–827. 2023. View Article : Google Scholar : PubMed/NCBI
13	Li L, Zhang H, Wang L, Xie C, Yu H and Zhong Y: Optimization of supraclavicular lymph node clinical target volume delineation in high-risk breast cancer: A single center experience and recommendation. BMC Cancer. 23:11682023. View Article : Google Scholar : PubMed/NCBI
14	Zhang J, Zhang W, Zhang B, Qian D, Li X, Zhang H, Wang Q, Zhao L, Pang Q and Wang P: Clinical results of intensity-modulated radiotherapy for 250 patients with cervical and upper thoracic esophageal carcinoma. Cancer Manag Res. 11:8285–8294. 2019. View Article : Google Scholar : PubMed/NCBI
15	Higgins MI and Master VA: Who really knows the performance status: The physician or the patient? Cancer. 127:339–341. 2021. View Article : Google Scholar : PubMed/NCBI
16	Doki Y, Tanaka K, Kawachi H, Shirakawa Y, Kitagawa Y, Toh Y, Yasuda T, Watanabe M, Kamei T, Oyama T, et al: Japanese classification of esophageal cancer, 12th edition: Part II. Esophagus. 21:216–269. 2024. View Article : Google Scholar : PubMed/NCBI
17	Zhong Z, Wang D, Liu Y, Shao S, Chen S, He S, Yang N, Li C, Ren J, Zhao Y, et al: Lymph drainage and cervical fascia anatomy-oriented differential nodal CTV delineation at the supraclavicular region for esophageal cancer and nasopharyngeal cancer. Radiother Oncol. 177:113–120. 2022. View Article : Google Scholar : PubMed/NCBI
18	Jing H, Tang Y, Wang ZZ, Wei R, Jin JY, Li J, Zhao LY, Jin J, Liu YP, Song YW, et al: Individualized clinical target volume for irradiation of the supraclavicular region in breast cancer based on mapping of the involved ipsilateral supraclavicular lymph nodes. Int J Radiat Oncol Biol Phys. 115:922–932. 2023. View Article : Google Scholar : PubMed/NCBI
19	Luo Y, Liu Y, Wang X, Zhang B, Yu J, Wang C, Huang Y and Li M: Mapping patterns of nodal metastases in esophageal carcinoma: Rethinking the clinical target volume for supraclavicular nodal irradiation. J Thorac Dis. 8:3132–3138. 2016. View Article : Google Scholar : PubMed/NCBI
20	Yu J, Ouyang W, Li C, Shen J, Xu Y, Zhang J and Xie C: Mapping patterns of metastatic lymph nodes for postoperative radiotherapy in thoracic esophageal squamous cell carcinoma: A recommendation for clinical target volume definition. BMC Cancer. 19:9272019. View Article : Google Scholar : PubMed/NCBI
21	Zhang W, Zhu M, Xiang Y, Sun Y, Li S, Cai J and Zeng H: Current and future perspectives in unresectable locally advanced esophageal squamous cell cancer (review). Oncol Rep. 51:652024. View Article : Google Scholar : PubMed/NCBI
22	Bassalobre M, Liebano RE, da Silva MP, Castiglioni MLV, Sadala AY, Ferreira LM and Nahas FX: Changes in the pattern of superficial lymphatic drainage of the abdomen after abdominoplasty. Plast Reconstr Surg. 149:1106e–1113e. 2022. View Article : Google Scholar : PubMed/NCBI
23	Sun JM, Shen L, Shah MA, Enzinger P, Adenis A, Doi T, Kojima T, Metges JP, Li Z, Kim SB, et al: Pembrolizumab plus chemotherapy versus chemotherapy alone for first-line treatment of advanced oesophageal cancer (KEYNOTE-590): A randomised, placebo-controlled, phase 3 study. Lancet. 398:759–771. 2021. View Article : Google Scholar : PubMed/NCBI
24	Liu J, Yang Y, Liu Z, Fu X, Cai X, Li H, Zhu L, Shen Y, Zhang H, Sun Y, et al: Multicenter, single-arm, phase II trial of camrelizumab and chemotherapy as neoadjuvant treatment for locally advanced esophageal squamous cell carcinoma. J Immunother Cancer. 10:e0042912022. View Article : Google Scholar : PubMed/NCBI
25	Okamura A, Watanabe M, Kozuki R, Toihata T, Yuda M, Imamura Y and Mine S: Supraclavicular and celiac metastases in squamous cell carcinoma of the middle thoracic esophagus. Langenbecks Arch Surg. 403:977–984. 2018. View Article : Google Scholar : PubMed/NCBI
26	Wen J, Chen D, Zhao T, Chen J, Zhao Y, Liu D, Wang W, Xu X, Fan M, Chen C and Chen Y: Should the clinical significance of supraclavicular and celiac lymph node metastasis in thoracic esophageal cancer be reevaluated? Thorac Cancer. 10:1725–1735. 2019. View Article : Google Scholar : PubMed/NCBI
27	Tsunoda S, Hoshino N, Yoshida S and Obama K: Prophylactic supraclavicular lymph node dissection for esophageal squamous cell carcinoma: A systematic review and meta-analysis. Surg Today. 53:647–654. 2023. View Article : Google Scholar : PubMed/NCBI
28	Xu Y, Dong B, Zhu W, Li J, Huang R, Sun Z, Yang X, Liu L, He H, Liao Z, et al: A phase III multicenter randomized clinical trial of 60 Gy versus 50 Gy radiation dose in concurrent chemoradiotherapy for inoperable esophageal squamous cell carcinoma. Clin Cancer Res. 28:1792–1799. 2022. View Article : Google Scholar : PubMed/NCBI
29	Kumakura Y, Yokobori T, Yoshida T, Hara K, Sakai M, Sohda M, Miyazaki T, Yokoo H, Handa T, Oyama T, et al: Elucidation of the anatomical mechanism of nodal skip metastasis in superficial thoracic esophageal squamous cell carcinoma. Ann Surg Oncol. 25:1221–1228. 2018. View Article : Google Scholar : PubMed/NCBI
30	Lei X, Cao Z, Wu Y, Lin J, Zhang Z, Jin J, Ai Y, Zhang J, Du D, Tian Z, et al: Preoperative prediction of clinical and pathological stages for patients with esophageal cancer using PET/CT radiomics. Insights Imaging. 14:1742023. View Article : Google Scholar : PubMed/NCBI
31	Watanabe A, Taniguchi M, Kimura Y, Kikkawa T and Hosokawa M: Larynx-preserving hybrid surgery with endoscopic laryngopharyngeal surgery and open surgery for cervical esophageal cancer invading pharynx. Dis Esophagus. 33:doaa0202020. View Article : Google Scholar : PubMed/NCBI