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Jiang KY, Huang H, Chen WY, Yan HJ, Wei ZT, Wang XW, Li HX, Zheng XY, Tian D. Risk factors for lymph node metastasis in T1 esophageal squamous cell carcinoma: A systematic review and meta-analysis. World J Gastroenterol 2021; 27:737-750. [PMID: 33716451 PMCID: PMC7934003 DOI: 10.3748/wjg.v27.i8.737] [Citation(s) in RCA: 26] [Impact Index Per Article: 6.5] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 11/28/2020] [Revised: 01/20/2021] [Accepted: 02/01/2021] [Indexed: 02/06/2023] Open
Abstract
BACKGROUND Lymph node metastasis (LNM) affects the application and outcomes of endoscopic resection in T1 esophageal squamous cell carcinoma (ESCC). However, reports of the risk factors for LNM have been controversial.
AIM To evaluate risk factors for LNM in T1 ESCC.
METHODS We searched Embase, PubMed and Cochrane Library to select studies related to LNM in patients with T1 ESCC. Included studies were divided into LNM and non-LNM groups. We performed a meta-analysis to examine the relationship between LNM and clinicopathologic features. Odds ratio (OR), mean differences and 95% confidence interval (CI) were assessed using a fixed-effects or random-effects model.
RESULTS Seventeen studies involving a total of 3775 patients with T1 ESCC met the inclusion criteria. After excluding studies with heterogeneity based on influence analysis, tumor size (OR = 1.93, 95%CI = 1.49-2.50, P < 0.001), tumor location (OR = 1.46, 95%CI = 1.17-1.82, P < 0.001), macroscopic type (OR = 3.17, 95%CI = 2.33-4.31, P < 0.001), T1 substage (OR = 6.28, 95%CI = 4.93-8.00, P < 0.001), differentiation (OR = 2.11, 95%CI = 1.64-2.72, P < 0.001) and lymphovascular invasion (OR = 5.86, 95%CI = 4.60-7.48, P < 0.001) were found to be significantly associated with LNM. Conversely, sex, age and infiltrative growth pattern were not identified as risk factors for LNM.
CONCLUSION A tumor size > 2 cm, lower location, nonflat macroscopic type, T1b stage, poor differentiation and lymphovascular invasion were associated with LNM in patients with T1 ESCC.
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Affiliation(s)
- Kai-Yuan Jiang
- College of Clinical Medicine, North Sichuan Medical College, Nanchong 637000, Sichuan Province, China
- Department of Thoracic Surgery, Affiliated Hospital of North Sichuan Medical College, Nanchong 637000, Sichuan Province, China
| | - Heng Huang
- College of Clinical Medicine, North Sichuan Medical College, Nanchong 637000, Sichuan Province, China
| | - Wei-Yang Chen
- College of Clinical Medicine, North Sichuan Medical College, Nanchong 637000, Sichuan Province, China
| | - Hao-Ji Yan
- College of Clinical Medicine, North Sichuan Medical College, Nanchong 637000, Sichuan Province, China
| | - Zhen-Ting Wei
- College of Clinical Medicine, North Sichuan Medical College, Nanchong 637000, Sichuan Province, China
| | - Xiao-Wen Wang
- College of Clinical Medicine, North Sichuan Medical College, Nanchong 637000, Sichuan Province, China
| | - Hao-Xuan Li
- College of Clinical Medicine, North Sichuan Medical College, Nanchong 637000, Sichuan Province, China
| | - Xiang-Yun Zheng
- College of Clinical Medicine, North Sichuan Medical College, Nanchong 637000, Sichuan Province, China
| | - Dong Tian
- Department of Thoracic Surgery, Affiliated Hospital of North Sichuan Medical College, Nanchong 637000, Sichuan Province, China
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Long-term outcomes of endoscopic versus surgical resection for MM-SM1 esophageal squamous cell carcinoma using propensity score analysis. Esophagus 2021; 18:72-80. [PMID: 32876825 DOI: 10.1007/s10388-020-00775-0] [Citation(s) in RCA: 3] [Impact Index Per Article: 0.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 03/09/2020] [Accepted: 08/24/2020] [Indexed: 02/08/2023]
Abstract
BACKGROUND Esophageal squamous cell carcinoma (ESCC) confined to the muscularis mucosae (MM) or up to 200 µm of the submucosa (SM1) confers the risk for lymph node metastasis, and is defined as relative indication for endoscopic submucosal dissection (ESD) by the Japan Esophageal Society guidelines. Although additional surgical treatment after ESD is recommended, long-term outcomes of ESD compared with those of surgery have not been clarified. This study aimed to evaluate the long-term outcomes of ESD and surgery for cN0M0 relative indication lesions of ESCC. METHODS Between 2006 and 2016, patients with relative indication lesions of ESCC who underwent ESD or surgery at nine participating hospitals were examined retrospectively. Using propensity score matching, we evaluated survival curves for and hazard ratios associated with endoscopic submucosal dissection and surgery. RESULTS In total, 155 lesions in the ESD group and 106 lesions in the surgery group met the pathological criteria of relative indication for endoscopic resection. After matching, 50 matched pairs of patients who underwent ESD or surgery were selected. The 5-year overall survival rates were 84.5% [95% confidence interval (CI) 68-93] in the ESD group and 79% [95% CI 60-90] in the surgery group. The hazard ratio of mortality for ESD compared with that for surgery estimated by Cox regression analysis was 0.79 (95% CI 0.3-2.06, p = 0.63). CONCLUSIONS Compared with surgery, ESD does not compromise long-term outcomes. ESD alone or ESD with chemotherapy and/or radiotherapy may be an option for the treatment of MM and SM1 ESCC.
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Xu W, Liu XB, Li SB, Yang ZH, Tong Q. Prediction of lymph node metastasis in superficial esophageal squamous cell carcinoma in Asia: a systematic review and meta-analysis. Dis Esophagus 2020; 33:5836484. [PMID: 32399558 DOI: 10.1093/dote/doaa032] [Citation(s) in RCA: 9] [Impact Index Per Article: 1.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 09/18/2019] [Revised: 12/15/2019] [Accepted: 01/17/2020] [Indexed: 12/11/2022]
Abstract
A less invasive endoscopic therapy has been used as a routine treatment for superficial esophageal squamous cell carcinoma (SESCC). However, lymph node metastasis (LNM) in SESCC limits the effectiveness of this medical procedure. This meta-analysis aimed to screen the risk factors for LNM in SESCC in Asia to provide evidence for clinicians in selecting treatment. We searched the main reference databases for research involving patients who received esophagectomy (open or minimally invasive) with lymph node dissection for SESCC. Meta-analysis was performed using RevMan 5.3 software. Twenty studies including 3983 patients were obtained in this analysis. The meta-analysis showed that tumor size, macroscopic type of tumor, degree of differentiation, depth of tumor invasion, and lymphovascular involvement are risk factors of LNM in SESCC, whereas age, sex, and tumor location showed no association with LNM. Five variables were screened as predictive factors for LNM in SESCC. The incidence of LNM in SESCC is not rare, and the physicians must be careful when making clinical decisions.
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Affiliation(s)
- Wen Xu
- Department of Gastroenterology, Taihe Hospital, Hubei University of Medicine, Shiyan, 442000, Hubei, China
| | - Xiao-Bo Liu
- Department of Gastroenterology, Taihe Hospital, Hubei University of Medicine, Shiyan, 442000, Hubei, China
| | - Sheng-Bao Li
- Department of Gastroenterology, Taihe Hospital, Hubei University of Medicine, Shiyan, 442000, Hubei, China
| | - Zhi-Hao Yang
- Department of Gastroenterology, Taihe Hospital, Hubei University of Medicine, Shiyan, 442000, Hubei, China
| | - Qiang Tong
- Department of Gastroenterology, Taihe Hospital, Hubei University of Medicine, Shiyan, 442000, Hubei, China
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Nishibuchi I, Murakami Y, Adachi Y, Imano N, Takeuchi Y, Tkahashi I, Kimura T, Urabe Y, Oka S, Tanaka S, Nagata Y. Effectiveness of salvage radiotherapy for superficial esophageal Cancer after non-curative endoscopic resection. Radiat Oncol 2020; 15:133. [PMID: 32487186 PMCID: PMC7268314 DOI: 10.1186/s13014-020-01582-8] [Citation(s) in RCA: 4] [Impact Index Per Article: 0.8] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/28/2019] [Accepted: 05/25/2020] [Indexed: 01/02/2023] Open
Abstract
BACKGROUND Endoscopic resection is widely used as an effective treatment for superficial esophageal cancer. However, the risk of lymph node metastasis increases in cases of muscularis mucosae or deeper invasion, for which additional treatment such as radiotherapy or surgery is required. Accordingly, the current study investigated the efficacy and toxicity of salvage radiotherapy after non-curative endoscopic resection as an organ preservation strategy. METHODS We retrospectively reviewed 37 esophageal cancer patients who received salvage radiotherapy after non-curative endoscopic resection. The pathological invasion depths were the muscularis mucosae, submucosal layer, and muscularis propria in 14, 22, and one patient, respectively. All patients received external beam radiotherapy. Among them, eight received intraluminal brachytherapy following external beam radiotherapy. Elective nodal irradiation was administered to all patients. Twenty-five patients received concurrent platinum and fluorouracil-based chemotherapy. RESULTS The median follow-up time was 74 months (range: 3-212). The 5-year progression-free survival and overall survival rates were 64 and 78%, respectively. No local or regional lymph node recurrence was observed. The causes of death included esophageal cancer in one patient, metachronous esophageal cancer in one patient, other malignancies in eight patients, and other causes in six patients. Late cardiac toxicities ≥ grade 3 were observed in six patients, one of whom died of arrhythmia. CONCLUSIONS Salvage radiotherapy after non-curative esophageal endoscopic resection is an effective treatment as an organ preservation strategy. Although muscularis mucosae and submucosal cancer have a high risk of lymph node metastasis, our results suggest that elective nodal irradiation contributes to reduced regional node metastases.
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Affiliation(s)
- Ikuno Nishibuchi
- Department of Radiation Oncology, Graduate School of Biomedical and Health Sciences, Hiroshima University, 1-2-3 Kasumi, Minami-ku, Hiroshima, 734-8551 Japan
| | - Yuji Murakami
- Department of Radiation Oncology, Graduate School of Biomedical and Health Sciences, Hiroshima University, 1-2-3 Kasumi, Minami-ku, Hiroshima, 734-8551 Japan
| | - Yoshinori Adachi
- Department of Radiation Oncology, Graduate School of Biomedical and Health Sciences, Hiroshima University, 1-2-3 Kasumi, Minami-ku, Hiroshima, 734-8551 Japan
| | - Nobuki Imano
- Department of Radiation Oncology, Graduate School of Biomedical and Health Sciences, Hiroshima University, 1-2-3 Kasumi, Minami-ku, Hiroshima, 734-8551 Japan
| | - Yuki Takeuchi
- Department of Radiation Oncology, Graduate School of Biomedical and Health Sciences, Hiroshima University, 1-2-3 Kasumi, Minami-ku, Hiroshima, 734-8551 Japan
| | - Ippei Tkahashi
- Department of Radiation Oncology, Graduate School of Biomedical and Health Sciences, Hiroshima University, 1-2-3 Kasumi, Minami-ku, Hiroshima, 734-8551 Japan
| | - Tomoki Kimura
- Department of Radiation Oncology, Graduate School of Biomedical and Health Sciences, Hiroshima University, 1-2-3 Kasumi, Minami-ku, Hiroshima, 734-8551 Japan
| | - Yuji Urabe
- Department of Regeneration and Medicine Medical Center for Translation and Clinical Research, Hiroshima University Hospital, 1-2-3 Kasumi, Minami-ku, Hiroshima, 734-8551 Japan
| | - Shiro Oka
- Department of Regeneration and Medicine Medical Center for Translation and Clinical Research, Hiroshima University Hospital, 1-2-3 Kasumi, Minami-ku, Hiroshima, 734-8551 Japan
- Department of Gastroenterology and Metabolism, Institute of Biomedical and Health Sciences, Graduate School of Biomedical and Health Sciences, Hiroshima University, 1-2-3 Kasumi, Minami-ku, Hiroshima, 734-8551 Japan
| | - Shinji Tanaka
- Department of Regeneration and Medicine Medical Center for Translation and Clinical Research, Hiroshima University Hospital, 1-2-3 Kasumi, Minami-ku, Hiroshima, 734-8551 Japan
- Department of Endoscopy, Hiroshima University Hospital, 1-2-3 Kasumi, Minami-ku, Hiroshima, 734-8551 Japan
| | - Yasushi Nagata
- Department of Radiation Oncology, Graduate School of Biomedical and Health Sciences, Hiroshima University, 1-2-3 Kasumi, Minami-ku, Hiroshima, 734-8551 Japan
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Zhou Y, Du J, Wang Y, Li H, Ping G, Luo J, Chen L, Zhang S, Wang W. Prediction of lymph node metastatic status in superficial esophageal squamous cell carcinoma using an assessment model combining clinical characteristics and pathologic results: A retrospective cohort study. Int J Surg 2019; 66:53-61. [DOI: 10.1016/j.ijsu.2019.04.014] [Citation(s) in RCA: 8] [Impact Index Per Article: 1.3] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/08/2018] [Revised: 03/13/2019] [Accepted: 04/22/2019] [Indexed: 01/02/2023]
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Zhou Y, Du J, Li H, Luo J, Chen L, Wang W. Clinicopathologic analysis of lymph node status in superficial esophageal squamous carcinoma. World J Surg Oncol 2016; 14:259. [PMID: 27729036 PMCID: PMC5059900 DOI: 10.1186/s12957-016-1016-0] [Citation(s) in RCA: 19] [Impact Index Per Article: 2.1] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/28/2016] [Accepted: 10/04/2016] [Indexed: 12/17/2022] Open
Abstract
BACKGROUND Endoscopic approaches are gradually considered as a reliable treatment of intramucosal esophageal squamous carcinoma. However, endoscopic resection (ER) is limited by the potential lymph node metastasis (LNM) at various depths of mucosal and submucosal invasion. METHODS We conducted a retrospective review of 498 patients with pT1 superficial esophageal squamous carcinoma (SESC) who underwent surgical resection from January 2008 to August 2015. Pathological characteristics of tumors including location, size, appearance, differentiation, invasion depth, and nodal status were reviewed, and risk factors were analyzed. RESULTS LNM was found in 0.0, 2.7, 6.3, 18.2, 15.9, and 34.3 % of the m1, m2, m3, sm1, sm2, and sm3 lesions, respectively. Univariate logistic regression identified the presence of the tumor size > 2 cm (p < 0.05), the presence of the poor tumor differentiation (p < 0.05), and the depth of tumor invasion (p < 0.05) and angiolymphatic invasion (p < 0.05) to be the important risk factors associated with the prevalence of tumor-positive lymph nodes. These findings were confirmed in multivariate logistic regression as independent predictors for LNM. CONCLUSIONS ER is considered as a reliable treatment of m1 to m2 lesions. Radical surgical resection (SR) is the standard and irreplaceable therapy of sm1 to sm3 lesions. Patients with m3 lesions should undergo ER as the initial procedure for diagnosis. And this treatment is supported only by a successful description of the tumor's characteristics, including (1) only muscularis mucosa invasion and without invasion of the resection margins and (2) without any risk predictors for LNM. Otherwise, SR is recommended.
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Affiliation(s)
- Yue Zhou
- Department of Cardiothoracic Surgery, First Affiliated Hospital of Nanjing Medical University, No. 300 Guangzhou Road, Nanjing, 210029 China
| | - Junjie Du
- Department of Cardiothoracic Surgery, First Affiliated Hospital of Nanjing Medical University, No. 300 Guangzhou Road, Nanjing, 210029 China
| | - Hai Li
- Department of Pathology, First Affiliated Hospital of Nanjing Medical University, No. 300 Guangzhou Road, Nanjing, 210029 China
| | - Jinhua Luo
- Department of Cardiothoracic Surgery, First Affiliated Hospital of Nanjing Medical University, No. 300 Guangzhou Road, Nanjing, 210029 China
| | - Liang Chen
- Department of Cardiothoracic Surgery, First Affiliated Hospital of Nanjing Medical University, No. 300 Guangzhou Road, Nanjing, 210029 China
| | - Wei Wang
- Department of Cardiothoracic Surgery, First Affiliated Hospital of Nanjing Medical University, No. 300 Guangzhou Road, Nanjing, 210029 China
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Tanaka M, Kijima H, Shimada H, Makuuchi H, Ozawa S, Inokuchi S. Expression of podoplanin and vimentin is correlated with prognosis in esophageal squamous cell carcinoma. Mol Med Rep 2015; 12:4029-4036. [PMID: 26095281 PMCID: PMC4526028 DOI: 10.3892/mmr.2015.3966] [Citation(s) in RCA: 28] [Impact Index Per Article: 2.8] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/04/2014] [Accepted: 11/12/2014] [Indexed: 12/15/2022] Open
Abstract
Podoplanin is a small membrane mucin, which is involved in cell migration and cancer cell invasion. However, the roles of podoplanin in esophageal squamous cell carcinoma (ESCC) are poorly understood. In the present study, 139 cases of surgically resected ESCC were analyzed and the clinicopathological significance of podoplanin membrane expression in ESCC was demonstrated. Podoplanin expression was positive in 66.2% (92/139) of ESCC samples; with weak expression in 32.4% (45/139), and strong expression in 33.8% (47/139). Membrane expression of podoplanin was significantly associated with tumor status (P=0.001), venous invasion (P=0.035) and Union for International Cancer Control stage (P=0.029). Patients who exhibited strong podoplanin expression, were shown to have a poorer prognosis [hazard ratio (HR), 3.949; 95% confidence interval (CI), 2.001–7.794]. Expression of vimentin, a mesenchymal marker, was detected in 49 cases (35.3%) and was associated with venous invasion (P=0.020). Vimentin-positive cases were also more likely to have a worse prognosis than vimentin-negative cases (HR, 2.161; 95% CI, 1.300–3.592). Podoplanin membrane expression was significantly correlated with vimentin cytoplasmic expression in ESCC (P<0.001). The present study confirmed that podo-planin and vimentin are independent predictors of mortality (HR, 3.084; 95% CI, 1.543–6.164). These results suggest that podoplanin membrane expression results in epithelial-mesenchymal transition and promotes aggressive invasion in human ESCC.
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Affiliation(s)
- Makiko Tanaka
- Department of Critical Care and Emergency Medicine, Tokai University School of Medicine, Isehara, Kanagawa 259‑1193, Japan
| | - Hiroshi Kijima
- Department of Pathology and Bioscience, Hirosaki University Graduate School of Medicine, Hirosaki, Aomori 036‑8562, Japan
| | - Hideo Shimada
- Department of Gastroenterological Surgery, Tokai University School of Medicine, Isehara, Kanagawa 259‑1193, Japan
| | - Hiroyasu Makuuchi
- Department of Gastroenterological Surgery, Tokai University School of Medicine, Isehara, Kanagawa 259‑1193, Japan
| | - Soji Ozawa
- Department of Gastroenterological Surgery, Tokai University School of Medicine, Isehara, Kanagawa 259‑1193, Japan
| | - Sadaki Inokuchi
- Department of Critical Care and Emergency Medicine, Tokai University School of Medicine, Isehara, Kanagawa 259‑1193, Japan
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Long-term results of definitive concurrent chemoradiotherapy for patients with esophageal submucosal cancer (T1bN0M0). Int J Clin Oncol 2015; 20:897-904. [DOI: 10.1007/s10147-015-0819-2] [Citation(s) in RCA: 14] [Impact Index Per Article: 1.4] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/18/2014] [Accepted: 03/12/2015] [Indexed: 01/02/2023]
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Inoue H, Kaga M, Ikeda H, Sato C, Sato H, Minami H, Santi EG, Hayee B, Eleftheriadis N. Magnification endoscopy in esophageal squamous cell carcinoma: a review of the intrapapillary capillary loop classification. Ann Gastroenterol 2015; 28:41-48. [PMID: 25608626 PMCID: PMC4290003] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Download PDF] [Figures] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 07/26/2014] [Accepted: 09/02/2014] [Indexed: 10/29/2022] Open
Abstract
Recent developments in image-enhancement technology have enabled clear visualization of the microvascular structure of the esophageal mucosa. In particular, intrapapillary capillary loops (IPCLs) are observed as brown loops on magnification endoscopy with narrow-band imaging (NBI). IPCLs demonstrate characteristic morphological changes according to the structural irregularity of esophageal epithelium and cancer infiltration, summarized in the IPCL classification. In this review, the process from the first endoscopic description of IPCLs to the eventual development of the IPCL classification is described and discussed, particularly focusing on early stage squamous cell carcinoma of the esophagus.
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Affiliation(s)
- Haruhiro Inoue
- Digestive Disease Center, Showa University Koto-Toyosu Hospital, Tokyo, Japan (Haruhiro Inoue, Makoto Kaga, Haruo Ikeda, Chiaki Sato, Hiroki Sato, Hitomi Minami, Esperanza Grace Santi, Nikolas Eleftheriadis)
| | - Makoto Kaga
- Digestive Disease Center, Showa University Koto-Toyosu Hospital, Tokyo, Japan (Haruhiro Inoue, Makoto Kaga, Haruo Ikeda, Chiaki Sato, Hiroki Sato, Hitomi Minami, Esperanza Grace Santi, Nikolas Eleftheriadis)
| | - Haruo Ikeda
- Digestive Disease Center, Showa University Koto-Toyosu Hospital, Tokyo, Japan (Haruhiro Inoue, Makoto Kaga, Haruo Ikeda, Chiaki Sato, Hiroki Sato, Hitomi Minami, Esperanza Grace Santi, Nikolas Eleftheriadis)
| | - Chiaki Sato
- Digestive Disease Center, Showa University Koto-Toyosu Hospital, Tokyo, Japan (Haruhiro Inoue, Makoto Kaga, Haruo Ikeda, Chiaki Sato, Hiroki Sato, Hitomi Minami, Esperanza Grace Santi, Nikolas Eleftheriadis)
| | - Hiroki Sato
- Digestive Disease Center, Showa University Koto-Toyosu Hospital, Tokyo, Japan (Haruhiro Inoue, Makoto Kaga, Haruo Ikeda, Chiaki Sato, Hiroki Sato, Hitomi Minami, Esperanza Grace Santi, Nikolas Eleftheriadis)
| | - Hitomi Minami
- Digestive Disease Center, Showa University Koto-Toyosu Hospital, Tokyo, Japan (Haruhiro Inoue, Makoto Kaga, Haruo Ikeda, Chiaki Sato, Hiroki Sato, Hitomi Minami, Esperanza Grace Santi, Nikolas Eleftheriadis)
| | - Esperanza Grace Santi
- Digestive Disease Center, Showa University Koto-Toyosu Hospital, Tokyo, Japan (Haruhiro Inoue, Makoto Kaga, Haruo Ikeda, Chiaki Sato, Hiroki Sato, Hitomi Minami, Esperanza Grace Santi, Nikolas Eleftheriadis)
| | - Bu’Hussain Hayee
- Department of Gastroenterology, King’s College Hospital NHS Foundation Trust, London SE5 9RS, UK
| | - Nikolas Eleftheriadis
- Digestive Disease Center, Showa University Koto-Toyosu Hospital, Tokyo, Japan (Haruhiro Inoue, Makoto Kaga, Haruo Ikeda, Chiaki Sato, Hiroki Sato, Hitomi Minami, Esperanza Grace Santi, Nikolas Eleftheriadis)
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Jansen M, Schölvinck DW, Kushima R, Sekine S, Weusten BL, Wang GQ, Fleischer DE, Yoshinaga S, Dawsey SM, Meijer SL, Bergman JJ, Oda I. Is it justified to ablate flat-type esophageal squamous cancer? An analysis of endoscopic submucosal dissection specimens of lesions meeting the selection criteria of radiofrequency studies. Gastrointest Endosc 2014; 80:995-1002. [PMID: 25434658 PMCID: PMC5763499 DOI: 10.1016/j.gie.2014.09.004] [Citation(s) in RCA: 15] [Impact Index Per Article: 1.4] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 05/14/2014] [Accepted: 09/01/2014] [Indexed: 02/08/2023]
Abstract
BACKGROUND Endoscopic radiofrequency ablation (RFA) appears to be a safe and effective treatment for flat-type noninvasive squamous neoplasia of the esophagus. However, if RFA is applied to lesions containing invasive cancer (esophageal squamous cell carcinoma [ESCC]), histological features associated with lymph node metastases may remain undetected. In addition, extension of neoplasia down the ducts of esophageal submucosal glands (SMGs) may create a sheltered "niche" beyond the reach of ablation. OBJECTIVE To determine the RFA eligibility of flat-type ESCC. DESIGN Retrospective analysis of prospectively collected data of ESCC patients. SETTING National Cancer Center Hospital, Tokyo, Japan. PATIENTS Patients with flat-type ESCC larger than 3 cm removed by endoscopic submucosal dissection (ESD). INTERVENTIONS Three endoscopists involved in RFA studies in China reviewed endoscopic images to select lesions eligible for RFA. Corresponding ESD resection specimens were histologically examined. MAIN OUTCOME MEASUREMENTS The presence of poor histological features (ie, invasion in m3 or deeper, poor tumor differentiation, or lymphovascular invasion) and the number of involved esophageal SMGs and ducts. RESULTS Sixty-five lesions were included, 17 (26%) of which qualified as RFA eligible by RFA endoscopists. Interobserver agreement for this assessment was poor (κ = 0.09). Six of the 17 specimens (35%) showed relevant disease: 4 lesions invaded in the muscularis mucosae, 1 of which also showed lymphovascular invasion; 2 lesions showed extension of neoplasia into SMGs. LIMITATIONS Limited number of cases. RFA eligibility status was based on analysis of still images. CONCLUSIONS One third of flat-type ESCC, deemed eligible for RFA, demonstrated histological features that are considered (relative) contraindications to endoscopic treatment. Because it appears difficult for endoscopists to identify low-risk ESCC, conservative use of RFA for flat-type ESCC is advocated until long-term follow-up data are available.
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Affiliation(s)
- Marnix Jansen
- Department of Pathology, Academic Medical Center, Amsterdam
| | - Dirk W. Schölvinck
- Department of Gastroenterology and Hepatology, Academic Medical Center, Amsterdam,Department of Gastroenterology and Hepatology, St. Antonius Hospital, Nieuwegein, the Netherlands
| | - Ryoji Kushima
- Pathology Division, National Cancer Center Hospital, Tokyo, Japan
| | - Shigeki Sekine
- Pathology Division, National Cancer Center Hospital, Tokyo, Japan
| | - Bas L.A.M. Weusten
- Department of Gastroenterology and Hepatology, St. Antonius Hospital, Nieuwegein, the Netherlands
| | - Guiqi Q. Wang
- Department of Endoscopy, Cancer Institute and Hospital, Chinese Academy of Medical Sciences, Peking Union Medical College, Beijing, China
| | - David E. Fleischer
- Department of Gastroenterology and Hepatology, Mayo Clinic, Scottsdale, Arizona, USA
| | | | - Sanford M. Dawsey
- Division of Cancer Epidemiology and Genetics, National Cancer Institute, National Institutes of Health, Bethesda, Maryland, USA
| | | | | | - Ichiro Oda
- Endoscopy Division, National Cancer Center Hospital, Tokyo, Japan
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11
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Ito E, Ozawa S, Kijima H, Kazuno A, Miyako H, Nishi T, Chino O, Shimada H, Tanaka M, Inoue S, Inokuchi S, Makuuchi H. Clinicopathological significance of laminin-5γ2 chain expression in superficial esophageal cancer. Dis Esophagus 2014; 27:463-9. [PMID: 22978811 DOI: 10.1111/j.1442-2050.2012.01416.x] [Citation(s) in RCA: 7] [Impact Index Per Article: 0.6] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 12/11/2022]
Abstract
The glycoprotein laminin 5γ2 chain (LN-5γ2) has recently become a focus of increased interest and investigation as a marker of invasion in gastrointestinal malignancies. We investigated the significance of LN-5γ2 expression as a prognostic factor in superficial esophageal cancer. The study population consisted of 87 patients who had undergone a transthoracic esophagectomy and three-field lymphadenectomy for the treatment of superficial esophageal cancer at Tokai University Hospital. Formalin-fixed, paraffin-embedded sections of the resected specimens were examined using immunohistochemical staining and hematoxylin and eosin staining to assess the correlations between the LN-5γ2 expression pattern and the clinicopathological factors (age, sex, T-factor, N-factor, ly-factor, v-factor, degree of differentiation, infiltrative growth pattern, tumor node metastasis classification of malignant tumors [TNM] stage, etc.) and the patient outcome. The expression pattern of LN-5γ2 was classified into an extracellular type (E type), characterized by the staining of extracellular matrix such as the basement membrane and the stroma (31 cases, 35.6%), and a cytoplasmic type (C type), characterized by the staining of the cytoplasm in the cancer cells (56 cases, 64.6%). The expression pattern was not correlated with any of the clinicopathological factors that were assessed. However, univariate analyses of the survival analysis data showed that the N-factor (P = 0.011), TNM stage (P = 0.011), and LN-5γ2 C type (P = 0.017) were prognostic factors. A multivariate analysis revealed that the N-factor (P = 0.049) and LN-5γ2 C type (P = 0.048) were prognostic factors. In the survival analysis, a univariate analysis of the 75 T1b cases also showed that the N-factor (P = 0.048), TNM stage (P = 0.048), and LN-5γ2 C type (P = 0.029) were prognostic factors, while a multivariate analysis showed that the LN-5γ2 C type (P = 0.035) was a prognostic factor. The C type expression of LN-5γ2, i.e. confined to the cytoplasm, was correlated with an unfavorable outcome among the patients with superficial esophageal cancer in the present series. Observation of the LN-5γ2 expression pattern may be useful for the diagnosis of highly malignant tumors.
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Affiliation(s)
- E Ito
- Department of Gastroenterological Surgery, Tokai University School of Medicine, Isehara, Kanagawa, Japan
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Sgourakis G, Gockel I, Lang H. Endoscopic and surgical resection of T1a/T1b esophageal neoplasms: A systematic review. World J Gastroenterol 2013; 19:1424-37. [PMID: 23539431 PMCID: PMC3602502 DOI: 10.3748/wjg.v19.i9.1424] [Citation(s) in RCA: 100] [Impact Index Per Article: 8.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 06/16/2012] [Revised: 08/22/2012] [Accepted: 08/25/2012] [Indexed: 02/06/2023] Open
Abstract
AIM: To investigate potential therapeutic recommendations for endoscopic and surgical resection of T1a/T1b esophageal neoplasms.
METHODS: A thorough search of electronic databases MEDLINE, Embase, Pubmed and Cochrane Library, from 1997 up to January 2011 was performed. An analysis was carried out, pooling the effects of outcomes of 4241 patients enrolled in 80 retrospective studies. For comparisons across studies, each reporting on only one endoscopic method, we used a random effects meta-regression of the log-odds of the outcome of treatment in each study. “Neural networks” as a data mining technique was employed in order to establish a prediction model of lymph node status in superficial submucosal esophageal carcinoma. Another data mining technique, the “feature selection and root cause analysis”, was used to identify the most important predictors of local recurrence and metachronous cancer development in endoscopically resected patients, and lymph node positivity in squamous carcinoma (SCC) and adenocarcinoma (ADC) separately in surgically resected patients.
RESULTS: Endoscopically resected patients: Low grade dysplasia was observed in 4% of patients, high grade dysplasia in 14.6%, carcinoma in situ in 19%, mucosal cancer in 54%, and submucosal cancer in 16% of patients. There were no significant differences between endoscopic mucosal resection and endoscopic submucosal dissection (ESD) for the following parameters: complications, patients submitted to surgery, positive margins, lymph node positivity, local recurrence and metachronous cancer. With regard to piecemeal resection, ESD performed better since the number of cases was significantly less [coefficient: -7.709438, 95%CI: (-11.03803, -4.380844), P < 0.001]; hence local recurrence rates were significantly lower [coefficient: -4.033528, 95%CI: (-6.151498, -1.915559), P < 0.01]. A higher rate of esophageal stenosis was observed following ESD [coefficient: 7.322266, 95%CI: (3.810146, 10.83439), P < 0.001]. A significantly greater number of SCC patients were submitted to surgery (log-odds, ADC: -2.1206 ± 0.6249 vs SCC: 4.1356 ± 0.4038, P < 0.05). The odds for re-classification of tumor stage after endoscopic resection were 53% and 39% for ADC and SCC, respectively. Local tumor recurrence was best predicted by grade 3 differentiation and piecemeal resection, metachronous cancer development by the carcinoma in situ component, and lymph node positivity by lymphovascular invasion. With regard to surgically resected patients: Significant differences in patients with positive lymph nodes were observed between ADC and SCC [coefficient: 1.889569, 95%CI: (0.3945146, 3.384624), P < 0.01). In contrast, lymphovascular and microvascular invasion and grade 3 patients between histologic types were comparable, the respective rank order of the predictors of lymph node positivity was: Grade 3, lymphovascular invasion (L+), microvascular invasion (V+), submucosal (Sm) 3 invasion, Sm2 invasion and Sm1 invasion. Histologic type (ADC/SCC) was not included in the model. The best predictors for SCC lymph node positivity were Sm3 invasion and (V+). For ADC, the most important predictor was (L+).
CONCLUSION: Local tumor recurrence is predicted by grade 3, metachronous cancer by the carcinoma in-situ component, and lymph node positivity by L+. T1b cancer should be treated with surgical resection.
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New invasive patterns as a prognostic factor for superficial esophageal cancer. J Gastroenterol 2012; 47:1279-89. [PMID: 22576024 DOI: 10.1007/s00535-012-0587-y] [Citation(s) in RCA: 26] [Impact Index Per Article: 2.0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 11/11/2011] [Accepted: 03/23/2012] [Indexed: 02/04/2023]
Abstract
BACKGROUND Prognostic factors for superficial esophageal cancer cannot be limited to such factors as lymph node metastasis (N factor), depth of tumor invasion (T factor), and genetic alterations. The purpose of this study was to examine whether invasive growth patterns of tumors, such as infiltrative growth pattern c (INFc) and budding, represent new useful prognostic factors for superficial esophageal cancer. METHODS We investigated 87 cases of superficial esophageal cancer in patients treated with radical surgery. First, the invasive growth pattern of the tumor was pathologically evaluated based on the traditional infiltrative growth pattern (INF) classification. Next, new INF criteria were proposed, and the invasive pattern was re-evaluated. We also investigated budding (Bud) in the stroma of the invasive frontal lesion. RESULTS When the patients were divided into two groups, with and without an INFc component, the group with an INFc component had a poorer outcome than the group without an INFc component. When the group with an INFc component was defined as "new INFc", new INFc was correlated with the T factor (p = 0.006) and the ly factor (lymphatic invasion) (p = 0.041). Bud was correlated with the T factor (p = 0.001), the N factor (p = 0.030), and new INFc (p < 0.001). An analysis of survival revealed new INFc (p = 0.002) and Bud (p = 0.006) to be prognostic factors. The survival of the group with new INFc(+)/Bud(+) was poorer than that with new INFc(-)/Bud(-) (p = 0.007). CONCLUSIONS New INFc and Bud, which represent new invasive patterns, were prognostic factors for superficial esophageal cancer.
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Ebi M, Shimura T, Murakami K, Yamada T, Hirata Y, Tsukamoto H, Mizoshita T, Tanida S, Kataoka H, Kamiya T, Joh T. Comparison of staging diagnosis by two magnifying endoscopy classification for superficial oesophageal cancer. Dig Liver Dis 2012; 44:940-4. [PMID: 22704894 DOI: 10.1016/j.dld.2012.05.007] [Citation(s) in RCA: 4] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 03/13/2012] [Revised: 05/03/2012] [Accepted: 05/13/2012] [Indexed: 12/11/2022]
Abstract
BACKGROUND Due to the possibility of lymph node metastasis, surgical resection is indicated for superficial oesophageal cancer with invasion to a depth greater than the muscularis mucosa. Although two magnifying endoscopy classifications are currently used to diagnose the depth of invasion, which classification is more suitable remains controversial. AIMS To compare and evaluate the clinical outcomes of two classifications for superficial oesophageal squamous cell carcinoma. METHODS This cross-sectional study consists of 44 superficial oesophageal squamous cell carcinoma lesions with magnification image-enhanced endoscopy images. Only magnifying endoscopic images were displayed to two experienced endoscopists who independently diagnosed the depth of invasion according to both classifications. RESULTS The sensitivity of invasion greater than the muscularis mucosa tended to be higher in Inoue's classification than Arima's classification (78.3±6.2% vs. 50.0±3.0%; P=0.144), whereas the specificity was significantly lower in Inoue's classification than in Arima's classification (61.9±0.0% vs. 97.6±3.4%; P=0.043). For both classifications, rates of concordance were 90.9% and 84.4%, and κ statistics were 0.81 and 0.66, respectively. CONCLUSIONS Our results suggest that Arima's classification is suitable for general screening before treatment to avoid unnecessary surgery. Inoue's classification is appropriate for assessing wide lesion.
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Affiliation(s)
- Masahide Ebi
- Department of Gastroenterology and Metabolism, Nagoya City University Graduate School of Medical Sciences, Mizuho-ku, Nagoya, Japan
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Sgourakis G, Gockel I, Lyros O, Lanitis S, Dedemadi G, Polotzek U, Karaliotas C, Lang H. The Use of Neural Networks in Identifying Risk Factors for Lymph Node Metastasis and Recommending Management of T1b Esophageal Cancer. Am Surg 2012. [DOI: 10.1177/000313481207800238] [Citation(s) in RCA: 7] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/25/2022]
Abstract
The objective of this study was to establish a prediction model of lymph node status in T1b esophageal carcinoma and define the best squamous and adenocarcinoma predictors. The literature lacks a satisfactory level of evidence of T1b esophageal cancer management. We performed an analysis pooling the effects of outcomes of 2098 patients enrolled into 37 retrospective studies using “neural networks” as data mining techniques. The percentages for lymph node, lymphatic (L1), and vascular (V1) invasion in Sm1 esophageal cancers were 24, 46, and 20 per cent, respectively. The same parameters apply to Sm2 with 34, 63, and 38 per cent as opposed to Sm3 with 51, 69, and 47 per cent. The respective number of patients with well, moderate, and poor histologic differentiation totaled 267, 752, and 582. The rank order of the predictors of lymph node positivity was, respectively: Grade III, (L1), (V1), Sm3 invasion, Sm2 invasion, and Sm1 invasion. Histologic-type squamous and adenocarcinoma (ADC/SCC) was not included in the model. The best predictors for SCC lymph node positivity were sm3 invasion and (V1). As concerns ADC, the most important predictor was (L1). Submucosal esophageal cancer should be managed with surgical resection. However, this is subject to the histologic type and presence of specific predictors that could well alter the perspective of multimodality management.
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Affiliation(s)
- George Sgourakis
- Department of General and Abdominal Surgery, Johannes Gutenberg University Hospital, Mainz, Germany, and the, Athens, Greece
- 2nd Surgical Department and Surgical Oncology Unit of “Korgialenio–Benakio,” Red Cross Hospital, Athens, Greece
| | - Ines Gockel
- Department of General and Abdominal Surgery, Johannes Gutenberg University Hospital, Mainz, Germany, and the, Athens, Greece
| | - Orestis Lyros
- Department of General and Abdominal Surgery, Johannes Gutenberg University Hospital, Mainz, Germany, and the, Athens, Greece
| | - Sophocles Lanitis
- 2nd Surgical Department and Surgical Oncology Unit of “Korgialenio–Benakio,” Red Cross Hospital, Athens, Greece
| | - Georgia Dedemadi
- 2nd Surgical Department and Surgical Oncology Unit of “Korgialenio–Benakio,” Red Cross Hospital, Athens, Greece
| | - Ursula Polotzek
- Department of General and Abdominal Surgery, Johannes Gutenberg University Hospital, Mainz, Germany, and the, Athens, Greece
| | - Constantine Karaliotas
- 2nd Surgical Department and Surgical Oncology Unit of “Korgialenio–Benakio,” Red Cross Hospital, Athens, Greece
| | - Hauke Lang
- Department of General and Abdominal Surgery, Johannes Gutenberg University Hospital, Mainz, Germany, and the, Athens, Greece
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Long-term outcomes of intraluminal brachytherapy in combination with external beam radiotherapy for superficial esophageal cancer. Int J Clin Oncol 2011; 17:263-71. [DOI: 10.1007/s10147-011-0285-4] [Citation(s) in RCA: 19] [Impact Index Per Article: 1.4] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/23/2011] [Accepted: 06/24/2011] [Indexed: 01/02/2023]
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Gockel I, Sgourakis G, Lyros O, Polotzek U, Schimanski CC, Lang H, Hoppo T, Jobe BA. Risk of lymph node metastasis in submucosal esophageal cancer: a review of surgically resected patients. Expert Rev Gastroenterol Hepatol 2011; 5:371-84. [PMID: 21651355 DOI: 10.1586/egh.11.33] [Citation(s) in RCA: 66] [Impact Index Per Article: 4.7] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 12/13/2022]
Abstract
OBJECTIVES Endoscopic local procedures are increasingly applied in patients with superficial esophageal cancer as an alternative to radical oncologic resection. The objective of this article is to determine the risk of nodal metastases in submucosal (sm) esophageal cancer, comparing the two predominating histologic tumor types, squamous cell cancer (SCC) and adenocarcinoma (ADC). METHODS A query of PubMed, MEDLINE, Embase and Cochrane Library (1980-2009) using predetermined search terms revealed 675 abstracts, of which 485 full-text articles were reviewed. A total of 105 articles met the selection criteria. A review of article references and consultation with experts revealed additional articles for inclusion. Studies that enrolled patients with submucosal esophageal cancer and provided adequate extractable data were included. RESULTS The pooled outcomes of 7645 patients with esophageal cancer involving the sm level of infiltration were included in the analysis. Overall, the percentage of lymph node metastasis in submucosal cancer was 37%. Lymph node (N), lymphatic (L) and vascular (V) invasion in sm1 esophageal cancers was 27, 46 and 22%, respectively. Within sm2 lesions, N, L and V invasion were involved in 38, 63 and 38% of patients, respectively. Finally, N, L and V involvement in patients with sm3 lesions was 54, 69 and 47%, respectively. The rates of lymph node metastasis for sm1 and sm2 were higher in SCC compared with ADC, whereas the lymph node metastasis for sm3 was comparable, with >50% involvement in both histologic subtypes. SCC revealed an overall more aggressive behavior compared with ADC (N+: 45 vs 26%; L+: 57 vs 37%; V+: 40 vs 18%). DISCUSSION While endoscopic therapy may be adequate in selected patients with 'low-risk' sm1 ADC, submucosal SCC necessitates esophageal resection and systematic lymphadenectomy because of its aggressive nature and tendency for early metastasis.
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Affiliation(s)
- Ines Gockel
- Johannes Gutenberg-University of Mainz, Mainz, Germany.
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HORIUCHI M, MAKUUCHI H, MACHIMURA T, TAMURA Y, SAKAI M. Survival Benefit of Screening for Early Esophageal Carcinoma in Head and Neck Cancer Patients. Dig Endosc 2007. [DOI: 10.1111/j.1443-1661.1998.tb00546.x] [Citation(s) in RCA: 11] [Impact Index Per Article: 0.6] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 02/23/2023]
Affiliation(s)
- Masatoshi HORIUCHI
- Department of Otolaryngology, Tokai University School of Medicine, Kanagaiva, Japan
| | - Hiroyasu MAKUUCHI
- Department of Surgery, Tokai University School of Medicine, Kanagaiva, Japan
| | - Takao MACHIMURA
- Department of Surgery, Tokai University School of Medicine, Kanagaiva, Japan
| | - Yoshiyuki TAMURA
- Department of Otolaryngology, Tokai University School of Medicine, Kanagaiva, Japan
| | - Makoto SAKAI
- Department of Otolaryngology, Tokai University School of Medicine, Kanagaiva, Japan
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Endo M, Yoshino K, Kawano T, Nagai K, Inoue H. Clinicopathologic analysis of lymph node metastasis in surgically resected superficial cancer of the thoracic esophagus. Dis Esophagus 2000; 13:125-9. [PMID: 14601903 DOI: 10.1046/j.1442-2050.2000.00100.x] [Citation(s) in RCA: 132] [Impact Index Per Article: 5.3] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 12/11/2022]
Abstract
We examined lymph node metastasis clinicopathologically in 236 cases of superficial cancer (T1, Tis) of the thoracic esophagus surgically resected at our department without adjuvant treatment. Mucosal cancer was observed in 112 cases (47%) and submucosal cancer in 124 cases (53%). Lymph node metastasis was present in 3% of mucosal cancer cases and 41% of submucosal cancer cases. By the recent pathologic subclassification of the extent of the cancerous invasion in superficial esophageal cancer, mucosal cancer and submucosal cancer were each divided into three subtypes according to the extent of invasion, i.e. m1, m2, m3, sm1, sm2 and sm3 cancers. There was no case of lymph node metastasis in m1 and m2 cases, but it was observed in 8% of m3 cases, in 11% of sm1 cases, in 30% of sm2 cases and in 61% of sm3 cases. The number of involved nodes was three or less in m3 and sm1 cases, however four or more involved nodes were observed in 14% of sm2 cases and in 24% of sm3 cases. Positive lymph nodes were found only in the mediastinum in m3 and sm1 cases. On the contrary, they were found extensively in the mediastinum, the abdomen and the neck and in two or more regions in 27% of sm2 cases and in 38% of sm3 cases. Considering the location of positive nodes, the recurrent nerve lymph nodes were most frequently involved, followed by the cardiac lymph nodes. A similar tendency was observed in cases with single node metastasis. The 5-year survival rate of cases from m1 to sm1 was similar. That of sm3 cases was significantly worse than that of other groups. Based on the clinical results, the therapeutic guidelines for superficial cancer of the thoracic esophagus are considered to be as follows: (i) in m1 and m2 cancer, endoscopic mucosal resection is generally indicated in principle, although transhiatal esophagectomy may be indicated in some cases; (ii) in m3 and sm1 cancer, endoscopic mucosal resection is performed initially, then subsequent treatment is selected if necessary; (iii) in sm2 and sm3 cancer, conventional transthoracic esophagectomy with systematic lymph node dissection is indicated.
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Affiliation(s)
- M Endo
- Department of Surgery, Tokyo Medical and Dental University 1-5-45, Yushima, Bunkyo-ku, Tokyo 113-8519, Japan
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