Abstract
Background
It is occasionally difficult to diagnose cT3 or cT4b using imaging examinations for esophageal cancer. The optimal treatment strategy for borderline resectable esophageal squamous cell carcinoma (BR-ESCC) is unclear.
Methods
We included 131 patients with cT3 ESCC who received neoadjuvant chemoradiotherapy (NCRT) followed by surgery. The patients were classified as having definitive cT3 (D-cT3) or borderline resectable cT3 (BR-cT3), based on presence of undeniable adjacent organ invasion on pretreatment CT. Surgical outcomes and prognoses were compared among patients with D-cT3 and BR-cT3 tumors, and the risk factors for non-R0 resection were assessed.
Results
Ninety and 41 patients were classified as D-cT3 and BR-cT3, respectively. Although BR-cT3 had a significantly higher non-R0 resection rate than D-cT3 (D-cT3 3.7%; BR-cT3 14.6%), BR-cT3 was not correlated with shorter overall survival (OS) (D-cT3 5-year OS, 50.8%; BR-cT3 5-year OS 38.4%; p = 0.234). Conversely, non-R0 resection was significantly associated with poor OS (R0 resection 5-year OS 48.8%; non-R0 resection 5-year OS 22.2%; p = 0.031). Cox regression analysis of OS demonstrated that BR-cT3 was not a prognostic factor. In the analysis of risk factors for non-R0 resection, BR-cT3 (p = 0.027), suspected invasion of the trachea or bronchus (p = 0.046), and high SUVmax of the primary lesion after NCRT (p = 0.002) were risk factors.
Conclusions
NCRT followed by surgery achieved a relatively high R0 resection rate and an almost equal overall survival rate for BR-cT3 compared with D-cT3 ESCC. Thus, NCRT followed by surgery is an effective treatment strategy for patients with BR-cT3 ESCC.
Similar content being viewed by others
References
Agrawal N, Jiao Y, Bettegowda C et al (2012) Comparative genomic analysis of esophageal adenocarcinoma and squamous cell carcinoma. Cancer Discov 2:899–905
Ohashi S, Miyamoto S, Kikuchi O et al (2015) Recent advances from basic and clinical studies of esophageal squamous cell carcinoma. Gastroenterology 149:1700–1715
Sjoquist KM, Burmeister BH, Smithers BM et al (2011) Survival after neoadjuvant chemotherapy or chemoradiotherapy for resectable oesophageal carcinoma: an updated meta-analysis. Lancet Oncol 12:681–692
van Hagen P, Hulshof MC, van Lanschot JJ et al (2012) Preoperative chemoradiotherapy for esophageal or junctional cancer. N Engl J Med 366:2074–2084
Donahue JM, Nichols FC, Li Z, et al (2009) Complete pathologic response after neoadjuvant chemoradiotherapy for esophageal cancer is associated with enhanced survival. Ann Thorac Surg 87:392–398; discussion 398–399.
Tepper J, Krasna MJ, Niedzwiecki D et al (2008) Phase III trial of trimodality therapy with cisplatin, fluorouracil, radiotherapy, and surgery compared with surgery alone for esophageal cancer: CALGB 9781. J Clin Oncol 26:1086–1092
Shapiro J, van Lanschot JJB, Hulshof MCCM et al (2015) Neoadjuvant chemoradiotherapy plus surgery versus surgery alone for oesophageal or junctional cancer (CROSS): long-term results of a randomised controlled trial. Lancet Oncol 16:1090–1098
Ishida K, Ando N, Yamamoto S et al (2004) Phase II study of cisplatin and 5-fluorouracil with concurrent radiotherapy in advanced squamous cell carcinoma of the esophagus: a Japan esophageal oncology group (JEOG)/Japan clinical oncology group trial (JCOG9516). Jpn J Clin Oncol 34:615–619
Ochi M, Murakami Y, Nishibuchi I et al (2021) Long-term results of definitive chemoradiotherapy for unresectable locally advanced esophageal squamous cell carcinoma. J Radiat Res 62:142–148
Murakami Y, Hamai Y, Emi M et al (2018) Long-term results of neoadjuvant chemoradiotherapy using cisplatin and 5-fluorouracil followed by esophagectomy for resectable, locally advanced esophageal squamous cell carcinoma. J Radiat Res 59:616–624
Hamai Y, Emi M, Ibuki Y et al (2021) Distribution of lymph node metastasis in esophageal squamous cell carcinoma after trimodal therapy. Ann Surg Oncol 28:1798–1807
Kurokawa T, Hamai Y, Emi M et al (2020) Risk factors for recurrence in esophageal squamous cell carcinoma without pathological complete response after trimodal therapy. Anticancer Res 40:4387–4394
Hirohata R, Hamai Y, Emi M et al (2021) Prediction of the tumor response and survival based on computed tomography in esophageal squamous cell carcinoma after trimodality therapy. Surg Today 51:1496–1505
Shiraishi O, Yasuda T, Kato H et al (2021) Comparison of aggressive planned salvage surgery versus neoadjuvant chemoradiotherapy plus surgery for borderline resectable T4 squamous cell carcinoma. Ann Surg Oncol 28:6366–6375
Suzuki T, Okamura A, Watanabe M et al (2020) Neoadjuvant chemoradiotherapy with cisplatin plus fluorouracil for borderline resectable esophageal squamous cell carcinoma. Ann Surg Oncol 27:1510–1517
Hamai Y, Hihara J, Emi M et al (2018) Treatment outcomes and prognostic factors after recurrence of esophageal squamous cell carcinoma. World J Surg 42:2190–2198
Rice TW, Patil DT, Blackstone EH (2017), 8th edition AJCC/UICC staging of cancers of the esophagus and esophagogastric junction: application to clinical practice. Ann Cardiothorac Surg, 8th edn. 6: 119–130.
Kumbasar B (2002) Carcinoma of esophagus: radiologic diagnosis and staging. Eur J Radiol 42:170–180
Hamai Y, Hihara J, Emi M et al (2013) Treatment outcomes and prognostic factors for thoracic esophageal cancer with clinical evidence of adjacent organ invasion. Anticancer Res 33:3495–3502
Hamai Y, Hihara J, Taomoto J et al (2015) Effects of neoadjuvant chemoradiotherapy on postoperative morbidity and mortality associated with esophageal cancer. Dis Esophagus 28:358–364
Hamai Y, Hihara J, Emi M et al (2016) Ability of fluorine-18 fluorodeoxyglucose positron emission tomography to predict outcomes of neoadjuvant chemoradiotherapy followed by surgical treatment for esophageal squamous cell carcinoma. Ann Thorac Surg 102:1132–1139
Emi M, Hihara J, Hamai Y et al (2012) Neoadjuvant chemoradiotherapy with docetaxel, cisplatin, and 5-fluorouracil for esophageal cancer. Cancer Chemother Pharmacol 69:1499–1505
Eisenhauer EA, Therasse P, Bogaerts J et al (2009) New response evaluation criteria in solid tumours: revised RECIST guideline, 1.1 version. Eur J Cancer 45:228–247
Japanese classification of esophageal cancer (2017) Esophagus 14, part II and III, 11th edn., p 37–65
Yokota T, Hatooka S, Ura T et al (2011) Docetaxel plus 5-fluorouracil and cisplatin (DCF) induction chemotherapy for locally advanced borderline-resectable T4 esophageal cancer. Anticancer Res 31:3535–3541
Terada M, Hara H, Daiko H et al (2019) Phase III study of tri-modality combination therapy with induction docetaxel plus cisplatin and 5-fluorouracil versus definitive chemoradiotherapy for locally advanced unresectable squamous-cell carcinoma of the thoracic esophagus (JCOG1510: TRIANgLE). Jpn J Clin Oncol 49:1055–1060
Cooper JS, Guo MD, Herskovic A et al (1999) Chemoradiotherapy of locally advanced esophageal cancer: long-term follow-up of a prospective randomized trial (RTOG 85–01). Radiat Ther Oncol Group JAMA 281:1623–1627
Kato K, Muro K, Minashi K et al (2011) Phase II study of chemoradiotherapy with 5-fluorouracil and cisplatin for Stage II–III esophageal squamous cell carcinoma: JCOG trial (JCOG 9906). Int J Radiat Oncol Biol Phys 81:684–690
Wang BY, Hung WH, Wu SC et al (2019) Comparison between esophagectomy and definitive chemoradiotherapy in patients with esophageal cancer. Ann Thorac Surg 107:1060–1067
Yano M, Shiozaki H, Tsujinaka T et al (2000) Squamous cell carcinoma of the esophagus infiltrating the respiratory tract is less sensitive to preoperative concurrent radiation and chemotherapy. J Am Coll Surg 191:626–634
Hamamoto Y, Nojima M, Aoki Y et al (2017) Inter-evaluator heterogeneity of clinical diagnosis for locally advanced esophageal squamous cell carcinoma. Esophagus 14:324–332
Yokota T, Yasuda T, Kato H et al (2018) Concordance of clinical diagnosis of T classification among physicians for locally advanced unresectable thoracic esophageal cancer. Int J Clin Oncol 23:73–80
Acknowledgements
We would like to thank all the individuals of the Department of Surgical Oncology, Hiroshima University, for advice on preparing this manuscript.
Funding
This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Informed consent
Informed consent was obtained from all participants included in the study.
Ethical approval
This study was approved by the Institutional Review Board of Hiroshima University (Ethical Committee for Epidemiology of Hiroshima University, E-2225).
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Hirohata, R., Hamai, Y., Hihara, J. et al. Evaluation of Neoadjuvant Chemoradiotherapy Followed by Surgery for Borderline Resectable Esophageal Squamous Cell Carcinoma. World J Surg 46, 1934–1943 (2022). https://doi.org/10.1007/s00268-022-06568-z
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00268-022-06568-z