Current Curriculum Vitae and Bibliography Sang-Uk Han Personal Name: Sang-Uk Han, M.D., Ph.D Professor, Department of Surgery, Ajou University Address: Office: Department of Surgery, School of Medicine, Ajou University San5, Wonchon-Dong, Yeongtong-Gu, Suwon, 443-749, Korea Tel 82-31-219-5195, Fax 82-31-219-5755 e-mail hansu@ajou.ac.kr Education 1. M.D. in College of Medicine, Seoul National University from 1982. 3 to 1988. 2 2. M.S. in College of Medicine, Seoul National University from 1996. 3 to 1998. 2 3. Ph. D. in College of Medicine, Seoul National University from 1998. 3 to 2000, 2 Academic and Professional Positions 1. M.D. Seoul National University 1988 2. Residency in Department of Surgery, Seoul National University Hospital from 1992 to 1996. 5. Instructor in Department of Surgery, Ajou University from 1996 to 1999 6. Assistant Professor in Department of Surgery, Ajou University from 1999 to 2004. 7. Research Fellow, Laboratory of Cell Regulation and Carcinogenesis, NCI/NIH from March, 2001 to February 2003. 8. Associate Professor in Department of Surgery, Ajou University from 2004 to 2009. 9. Professor in Department of Surgery, Ajou University from March 2009 Committee Assignments in Professional Societies Korean Gastric Cancer Association Council member(2009-present), Director, Publication Committee Director, Scientific Committee Korean Society of Gastroenterology Council member(2011-2013), Director, Information Technology Committee Korean Society for Metabolic Bariatric Surgery Council member (2012-present), Director, Public Relation Committee Editorial Board Journal of Gastric Cancer Editor-in-Chief (2009-present)
Kim et al. BMC Cancer 2014, 14:209 http://www.biomedcentral.com/1471-2407/14/209 STUDY PROTOCOL Open Access Standardization of D2 lymphadenectomy and surgical quality control (KLASS-02-QC): a prospective, observational, multicenter study [NCT01283893] Hyoung-Il Kim 1,2, Hoon Hur 3, Youn Nam Kim 4, Hyuk-Joon Lee 5, Min-Chan Kim 6, Sang-Uk Han 3 and Woo Jin Hyung 1,2* Abstract Background: Extended systemic lymphadenectomy (D2) is standard procedure for surgical treatment of advanced gastric cancer (AGC) although less extensive lymphadenectomy (D1) can be applied to early gastric cancer. Complete D2 lymphadenectomy is the mandatory procedure for studies that evaluate surgical treatment results of AGC. However, the actual extent of D2 lymphadenectomy varies among surgeons because of a lacking consensus on the anatomical definition of each lymph node station. This study is aimed to develop a consensus for D2 lymphadenectomy and also to qualify surgeons that can perform both laparoscopic and open D2 gastrectomy. Methods/Design: This (KLASS-02-QC) is a prospective, observational, multicenter study to qualify the surgeons that will participate in the KLASS-02-RCT, which is a prospective, randomized, clinical trial comparing laparoscopic and open gastrectomy for AGC. Surgeons and reviewers participating in the study will be required to complete a questionnaire detailing their professional experience and specific gastrectomy surgical background/training, and the gastrectomy metrics of their primary hospitals. All surgeons must submit three laparoscopic and three open D2 gastrectomy videos, respectively. Each video will be allocated to five peer reviewers; thus each surgeon s operations will be assessed by a total of 30 reviews. Based on blinded assessment of unedited videos by experts review, a separate review evaluation committee will decide whether or not the evaluated surgeon will participate in the KLASS-02-RCT. The primary outcome measure is each surgeon s proficiency, as assessed by the reviewers based on evaluation criteria for completeness of D2 lymphadenectomy. Discussion: We believe that our study for standardization of D2 lymphadenectomy and surgical quality control (KLASS-02-QC) will guarantee successful implementation of the subsequent KLASS-02-RCT study. After making consensus on D2 lymphadenectomy, we developed evaluation criteria for completeness of D2 lymphadenectomy. We also developed a unique surgical standardization and quality control system that consists of recording unedited surgical videos, and expert review according to evaluation criteria for completeness of D2 lymphadenectomy. We hope our systematic approach will set a milestone in surgical standardization that is essential for surgical clinical trials. Additionally, our methods will serve as a novel system for educating surgeons and assessing surgical proficiency. Trial registration: NCT01283893. Keywords: Neoplasms of stomach, D2 lymphadenectomy, Gastrectomy, Laparoscopy, Standardization, Quality control * Correspondence: wjhyung@yuhs.ac 1 Department of Surgery, Yonsei University College of Medicine, 50 Yonsei-ro, Seodaemun-gu, Seoul 120-752, Korea 2 Robot and MIS Center, Severance Hospital, Yonsei University Health System, 50 Yonsei-ro, Seodaemun-gu, Seoul 120-752, Korea Full list of author information is available at the end of the article 2014 Kim et al.; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
Kim et al. BMC Cancer 2014, 14:209 Page 2 of 6 http://www.biomedcentral.com/1471-2407/14/209 Background Laparoscopic gastrectomy is gaining wide acceptance for treating early gastric cancer because of its favorable short-term outcomes compared to open gastrectomy, including reduced blood loss, less pain, and faster recovery [1,2]. In addition, long-term outcomes following laparoscopic gastrectomy are comparable to conventional open gastrectomy for early gastric cancer [3,4]. Consequently, laparoscopic gastrectomy is now also considered for treating advanced gastric cancer, to provide the potential benefits of a minimally invasive surgical solution to this disease [5,6]. For surgical treatment of advanced gastric cancer, gastrectomy with D2 lymphadenectomy is recommended as a standard procedure in major guidelines because D2 lymphadenectomy results in better patient survival than D1 lymphadenectomy [7-11]. Thus, for studies that evaluate the surgical treatment results of advanced gastric cancer, complete D2 lymphadenectomy is a mandatory procedure. However, D2 dissection is known to be a technically challenging surgical procedure and dissection quality and completeness varies among surgeons. The actual extent of D2 lymphadenectomy varies among surgeons because there remains a lack of consensus on the anatomical definition of appropriate lymph node dissection extent reflected in ambiguous definitions with the published documentation [12]. Despite great efforts to enhance quality control in a previous study that compared D1 versus D2 lymph node dissection, inadequate removal of lymph node station(s) for complete D2 lymphadenectomy, i.e., the non-compliance rate, was reported to be 81.0% [13]. Considering the high rate of inadequate D2 lymphadenectomy in open surgery, even worse results would be anticipated in laparoscopic surgery because of its increased technical difficulty. To get accurate results in clinical trials of laparoscopic and open D2 lymphadenectomy for advanced gastric cancer, only surgeons who can perform exact D2 lymphadenectomy should participate, to ensure objective comparisons. As far as we know, there has been no system to objectively evaluate the gastrectomy procedure focused on D2 lymphadenectomy quality. Furthermore, no study has yet attempted to standardize D2 lymphadenectomy during laparoscopic or open gastrectomy for clinical trials. Therefore, a tool that can assess the surgical proficiency and quality of lymphadenectomy is necessary. Herein, we report the development of a new surgical standardization and quality control system for assessing D2 lymphadenectomy. We intend to use this system to optimize our planned randomized prospective clinical trial to compare laparoscopic D2 lymphadenectomy with open D2 lymphadenectomy (KLASS-02-RCT, NCT01456598), to clarify the surgical feasibility and oncological safety of laparoscopic gastrectomy for advanced gastric cancer. Before initiating the prospective RCT, we conducted this quality control study (KLASS-02-QC, NCT01283893) to make a consensus for D2 lymphadenectomy and to qualify surgeons that can perform both laparoscopic and open D2 gastrectomy. Methods Study design This quality control study (KLASS-02-QC) is a prospective, observational, multicenter study to assess surgeon competency in performing laparoscopic and open D2 lymphadenectomy (Figure 1). Assessments are based on expert rating of unedited surgical videos, according to evaluation criteria for completeness of D2 lymphadenectomy (Additional file 1: Table S1). Only qualified surgeons will participate in the planned clinical trial comparing laparoscopic and open gastrectomy for treating advanced gastric cancer (KLASS-02-RCT). This study was reviewed and approved by institute review board of Severance hospital (4-2010-0637). Study objectives Primary aim To qualify the surgeons participating in the clinical trial (KLASS-02-RCT), which will compare laparoscopic versus open gastrectomy, with D2 lymphadenectomy. Secondary aims 1) To determine the feasibility of surgical standardization based on evaluation criteria for completeness of D2 lymphadenectomy; 2) To evaluate potential surgical proficiency improvement due to the review process; and 3) To assess potential relationships among the rated score, surgeon professional background, and the perioperative surgical outcomes of the patients whose operations were recorded. Organization Data center The role of the data center is to recruit participating surgeons and reviewers; to get signed non-disclosure agreements and completed questionnaires of recruited surgeons (Additional file 2: Table S2) and reviewers (Additional file 3: TableS3);tosupportvideorecordingservicesforopen gastrectomy cases; to blind the information regarding the patients, surgeons, and reviewers; to distribute submitted surgical videos; to collect reviewer assessments of surgical videos; and to disseminate committee decisions on the surgeons that are selected for participation in the subsequent RCT. Reviewers Korean and international surgeons will be invited as reviewers of surgical video recordings. To participate as a
Kim et al. BMC Cancer 2014, 14:209 Page 3 of 6 http://www.biomedcentral.com/1471-2407/14/209 Figure 1 Study schema. reviewer, experts will be required to submit a signed non-disclosure agreement and complete a reviewer questionnaire (Additional file 3: Table S3), which includes information such as personal gastrectomy experience and patient volume at their primary working hospital. Review evaluation committee The review evaluation committee consists of experts in laparoscopic and open D2 lymphadenectomy, including invited surgeon members of the Korean Gastric Cancer Association and principal investigators of the KLASS-02- RCT. Members of the committee developed a consensus on the mandatory anatomical extent of lymph node dissection, evaluation criteria for completeness of D2 lymphadenectomy, and sample surgical videos were then devoted based on this consensus. The review evaluation committee is distinct from the reviewer group, and will be the final determiner of a surgeon s technical competency and approval for participation in the KLASS-02-RCT, based on the reviewers assessments and surgical videos in a blinded way. Study process Evaluation criteria for completeness of D2 lymphadenectomy Definition of D1 lymphadenectomy is removal of the perigastric lymph nodes. Definition of D2 lymphadenectomy is additional removal of a second tier of lymph nodes in the extraperigastric areas, which generally fall along branches of the celiac axis including the left gastric, splenic, common hepatic, and proper hepatic arteries. The assessment form consists of 22 elements of D2 lymphadenectomy that together evaluate the success or failure to perform a surgical task (Additional file 1: Table S1). Although the assessment form was made based on the anatomical definition of lymph node stations, [12] parameters for assessing patient safety and surgical quality are also included in the criteria. Sample videos of D2 lymphadenectomy The review evaluation committee made unedited and edited sample videos of laparoscopic and open gastrectomy for surgeons, which satisfy the evaluation criteria for completeness of D2 lymphadenectomy. The sample videos clearly show the D2 lymphadenectomy, a total omentectomy with lymph node dissection of stations including 1, 3, 4, 5, 6, 7, 8a, 9, 11p and 12a, based on Japanese classifications are performed with appropriate annotations [12]. Recruitment of reviewers and surgeons Surgeon recruitment will be continued until 484 patients have been enrolled in KLASS-02-RCT, at which point planned analysis for safety related to morbidity and mortality is planned. Reviewers Thirty reviewers are required to fully assess the surgical videos of participating surgeons in this quality control study. Thus, our target reviewer enrollment number is 50, which provide a sizeable margin to account for potential drop-outs and work overload.
Kim et al. BMC Cancer 2014, 14:209 Page 4 of 6 http://www.biomedcentral.com/1471-2407/14/209 Surgeons The data center recruits surgeons who perform open and laparoscopic gastrectomy in clinical practice. After public offering of study participation to the members of the Korean Gastric Cancer Association, candidates will be accepted who satisfy following criteria: Surgeons who have personally performed more than 50 cases of each gastrectomy approach (i.e., laparoscopic and open), and surgeons that work in institutions where more than 80 gastrectomies are performed annually. To participate, the surgeon must obtain approval required by the Institutional Review Board of each institute, and should submit a completed surgeon questionnaire (Additional file 2: Table S2). This questionnaire includes surgeon information such as personal gastrectomy experience, annual case volume at their institute, and whether their institute has a specialized multidisciplinary team for gastric cancer treatment. Recording unedited surgical videos Criteria of patients for video recording: Patients whose operation will be recorded are required to provide written informed consent. Patients with mental incompetency, are illiterate, pregnant, or are <20 years old or >80 years old will not be asked to participate in this study. Patients must have documented biopsy-proven gastric cancer without distant lymph node metastasis or plans for combined operations. While all resectable gastric cancer patients without adjacent organ invasion are candidates for an open gastrectomy procedure, patients who will undergo a laparoscopic surgery must have gastric cancer without evidence of serosal invasion and extra-perigatric lymph node metastasis, as determined by evaluation of preoperative CT-scans, upper endoscopy, or endoscopic ultrasound. Video recording: Recommended surgical procedures are same as those provided in the sample videos. Reconstruction methods, surgical instruments for anastomosis, and drainage insertion are in accordance with the surgeon s preference. Video recording should clearly identify the extent of lymph node dissection and should record the entire procedure, without edition. No identifiable information of the patient or surgeon should be recorded. Video submissions and assessment Unedited videos of three laparoscopic and three open gastrectomies must be submitted by each participating surgeon to the data center. At the same time, case report forms (CRFs) containing perioperative surgical outcomes also will be submitted. The data center will blind the surgeon information and five reviewers will be randomly allocated to evaluate each video. Reviewers will assess each video based on the evaluation criteria for completeness of D2 lymphadenectomy, and will also give general impression and comments regarding surgeon performance. Decision-making on surgeon qualification The review evaluation committee will make a decision on surgeon qualification to participate in the KLASS-02- RCT based on the reviewers assessments. Additional review of surgical video could be necessary for selected cases. All CRFs containing perioperative surgical outcome will be blinded to preclude potential reviewer and committee bias. Evaluation committee decisions will be categorized as: (1) Qualified; the surgeon s operation proficiency is sufficient to accept them as qualified to participate in the KLASS-02-RCT; (2) Resubmission Required; when the surgeon performance in the submitted operation videos of either or both gastrectomy methods are not satisfactory, the evaluation committee will ask for resubmission of a video and CRF for the failed approach(es); and (3) Not-Qualified; surgeons whose operation performance is insufficient, and must be evaluated by submitting another six videos after getting re-approval from their Institutional Review Board. If a surgeon fails to be deemed qualified even after video resubmission, that surgeon will be regarded as Not-Qualified and will not participate in the RCT. Timeline All prospective RCT surgeons must participate in this quality control trial and only qualified surgeons will participate in the subsequent RCT. All surgeons must submit all required surgical videos and CRFs containing perioperative surgical outcome within 6 months after IRB approval. Otherwise, the surgeon will be regarded as a study dropout. The reviewer assessment process will be completed within 1 month after submission of required videos and CRFs. The review evaluation committee will make decisions after completing the review process for every five sequentially evaluated surgeons. Statistical considerations: estimated number of surgeons, video recordings, reviewers, and assessments This study is not a hypothesis-testing trial and therefore does not include an accepted approach for power calculation. Lacking previous reports on the criteria for surgical competency, we estimated the number of surgical videos and reviewers that are sufficient to assess surgeon proficiency, within realistic ranges. An overall target of six videos for each surgeon and five independent reviewers for each video were set. Considering patient variation, three operations for each surgical approach would be an acceptable number for surgeon assessment. Considering the number of expert surgeons at hospitals with appropriate volume, the estimated number of participating surgeons in Korea is approximately 50. Each surgeon must submit the minimum of six videos (three for each procedure), and up to eight videos if required for reevaluation. The estimated total number of videos will
Kim et al. BMC Cancer 2014, 14:209 Page 5 of 6 http://www.biomedcentral.com/1471-2407/14/209 range from 300 to 350. Thus, final estimated target patient enrollment for gastrectomy video recording will number 350. Analysis plan To explore qualified surgeon characteristics, descriptive statistical methods without formal testing will be used. For evaluating the secondary measurements, data will be analyzed using both quantitative and qualitative techniques. For assessing inter-reviewer agreement on video ratings, a generalized Kappa statistic will be determined. The major factor of the qualification decision, i.e., the average reviewer score based on predetermined criteria for submitted operation videos, will be used for the quantitative evaluation of the secondary measurements. Relationships among the surgeon proficiency rating scores, background information of the participating surgeons and reviewers, decision results by the review evaluation committee, and perioperative surgical outcomes will be analyzed. Data will be analyzed using SAS 9.2 software (SAS Institute Inc., Cary, NC, USA). For all statistical purposes, p < 0.05 will be considered indicative of statistically significant differences. Discussion We believe that effectiveness and safety of D2 dissection in advanced gastric cancer can be evaluated only when the D2 surgical procedure is standardized and surgical quality is controlled. If the surgery as an intervention in a clinical trial is of variable quality, the results will not be helpful to identify accurate differences in surgical outcomes using different specific treatments. Such variability would undermine the study findings. Despite attempting quality control of lymph node dissection, the results of a previous study comparing D1 versus D2 lymphadenectomy were weakened because of surgeon non-compliance (inadequate removal of lymph node stations) and contamination (lymph nodes were detected outside the intended level of dissection) rates of 81.0% and 27.1%, respectively [13]. Furthermore, the morbidity and mortality of the D2 group were 43% and 10%, respectively [14]. To compare the surgical outcome of laparoscopic and open D2 lymphadenectomy, lymph node dissection should be a homogenous surgical intervention. We designed this study protocol to assess the proficiency of a surgeon who performs both laparoscopic and open D2 lymphadenectomy. To assure that the standardized procedure is performed, we developed a standardization and quality control protocol. For an RCT comparing two surgical approaches for lymphadenectomy suffers from either high inter-surgeon or intra-surgeon performance variability, this will adversely affect the power to identify significant differences in outcomes between the two treatments. Thus, we prepared sample videos for surgeons to demonstrate essential principles of lymphadenectomy that must be maintained during surgery. Sample videos with annotations were made for easier understanding of the anatomical dissection of each lymph node station. Video demonstration is markedly superior to merely reading the written definitions of the appropriate anatomical extent of lymph node station excision during gastrectomy. We believe that distributing these sample videos will help to implement the consensus by the review evaluation committee on the mandatory anatomical extent of lymph node dissection required, and performed by surgeons participating in the study. To control surgical quality, we suggest assessment using unedited surgical video as assessment and learning tools. Unedited videos can clearly show not only the lymphadenectomy extent but also adverse events that may happen during surgery, such as injuries to adjacent organs and accidental bleeding. Any event that can jeopardize patient safety would be identified by reviewing unedited videos. In addition, using video clips can help peer reviewers to assess the proficiency of a surgeon without personally visiting the operating theater. Removing this limitation will increase the efficiency of the review process because we can provide more robust assessment of surgical proficiency by recruiting a larger number of reviewers. To objectively assess the surgeon s proficiency, we prepared an assessment form consisting of 22 evaluation criteria for completeness of D2 lymphadenectomy. By analyzing inter-reviewer agreement based on the background information of the reviewer, we expect to determine the required number of surgical videos and reviewers required for optimal assessment. Furthermore, our system provides feedback to each surgeon in the form of proficiency assessment score and allow for surgeon learning and improvement if they fail to initially qualify, by requesting resubmission of additional unedited videos. We will be able to evaluate whether the resubmission process improves the surgical proficiency of a surgeon. If this is the case, our method of standardization and quality control can be used for educating novice surgeons, as well as experienced surgeons that are learning new surgical techniques. Developing a quality control consensus for D2 lymphadenectomy performance during gastrectomy, recording unedited surgical videos, and assessing surgeon proficiency according to evaluation criteria for completeness of D2 lymphadenectomy may provide important benefits to clinical practice. Laparoscopic D2 lymphadenectomy for advanced gastric cancer itself was criticized for its applicability because of its inherent technical difficulty. If laparoscopic D2 lymphadenectomy benefits patients, it should not be discarded because of technical difficulty; instead, solutions should be sought to improve technique
Kim et al. BMC Cancer 2014, 14:209 Page 6 of 6 http://www.biomedcentral.com/1471-2407/14/209 performance. We conceived this study as one solution, by implementing a system for surgical standardization and quality control during gastrectomy. This method will provide important new information and education to improve patient surgical outcomes when treating gastric cancer with minimally invasive laparoscopic approaches. In conclusion, we believe that our study for standardization of D2 lymphadenectomy and surgical quality control (KLASS-02-QC) will guarantee successful implementation of the subsequent clinical trial comparing laparoscopic and open D2 lymphadenectomy for advanced gastric cancer (KLASS-02-RCT). After making consensus on D2 lymphadenectomy, we developed evaluation criteria for completeness of D2 lymphadenectomy. We also developed a unique surgical standardization and quality control system that consists of recording unedited surgical videos, and expert review according to evaluation criteria for completeness of D2 lymphadenectomy. We hope that our systematic approach will set a milestone in surgical standardization that is essential for surgical clinical trials. Additionally, our methods will serve as a novel system for educating surgeons and for assessing surgical proficiency. Additional files Additional file 1: Table S1. Evaluation criteria for completeness of subtotal D2 lymphadenectomy. Additional file 2: Table S2. Questionnaire for surgeons. Additional file 3: Table S3. Questionnaire for reviewers. Abbreviations AGC: Advanced gastric cancer; KLASS: Korean Laparoscopic Gastrointestinal Surgery Study Group; CRF: Case report form; RCT: Randomized clinical trial; QC: Quality control. Competing interests All authors declare that they have no competing financial interests to declare. Authors contributions KHI drafted the manuscript and is the primary author of this manuscript. HH, LHJ, and KMC designed this study and participated in the developing the D2 lymphadenectomy consensus. KYN helped draft the manuscript, provided statistical counseling in clinical trial design, and will conduct the primary statistical analyses. HSU is the grant holder, and conceived and initiated the study design. HWJ conceived and initiated the study design, and also supervised the manuscript construction. All authors have read and approved the final manuscript for publication. Acknowledgement This study was supported by a grant from the National R & D Program for Cancer Control, Ministry of Health & Welfare, Republic of Korea (1320270). This funding source had no role in the design of this study and will not have any role during its execution, data analyses and interpretation, or decision to submit results for presentation or publication. Author details 1 Department of Surgery, Yonsei University College of Medicine, 50 Yonsei-ro, Seodaemun-gu, Seoul 120-752, Korea. 2 Robot and MIS Center, Severance Hospital, Yonsei University Health System, 50 Yonsei-ro, Seodaemun-gu, Seoul 120-752, Korea. 3 Department of Surgery, Ajou University School of Medicine, 206 World Cup-ro, Yeongtong-gu, Suwon 443-749, Korea. 4 Department of Biostatistics, Yonsei University College of Medicine, 50 Yonsei-ro, Seodaemun-gu, Seoul 120-752, Korea. 5 Department of Surgery, Seoul National University College of Medicine, 101 Daehang-ro, Jongno-gu, Seoul 110-744, Korea. 6 Department of Surgery, Minimally Invasive and Robot Center, Dong-A University College of Medicine, 3-1 Dongdaeshin-dong, Seo-gu, Busan 602-715, Korea. Received: 27 December 2013 Accepted: 13 March 2014 Published: 19 March 2014 References 1. Lee JH, Han HS: A prospective randomized study comparing open vs laparoscopy-assisted distal gastrectomy in early gastric cancer: early results. Surg Endosc 2005, 19(2):168 173. 2. Kitano S, Shiraishi N, Fujii K, Yasuda K, Inomata M, Adachi Y: A randomized controlled trial comparing open vs laparoscopy-assisted distal gastrectomy for the treatment of early gastric cancer: an interim report. Surgery 2002, 131(1 Suppl):S306 S311. 3. Huscher CG, Mingoli A, Sgarzini G, Sansonetti A, Di Paola M, Recher A, Ponzano C: Laparoscopic versus open subtotal gastrectomy for distal gastric cancer: five-year results of a randomized prospective trial. Ann Surg 2005, 241(2):232 237. 4. Kim HH, Hyung WJ, Cho GS, Kim MC, Han SU, Kim W, Ryu SW, Lee HJ, Song KY: Morbidity and mortality of laparoscopic gastrectomy versus open gastrectomy for gastric cancer: an interim report a phase III multicenter, prospective, randomized Trial (KLASS Trial). Ann Surg 2010, 251(3):417 420. 5. Song KY, Kim SN, Park CH: Laparoscopy-assisted distal gastrectomy with D2 lymph node dissection for gastric cancer: technical and oncologic aspects. Surg Endosc 2008, 22(3):655 659. 6. Tokunaga M, Hiki N, Fukunaga T, Nohara K, Katayama H, Akashi Y, Ohyama S, Yamaguchi T: Laparoscopy-assisted distal gastrectomy with D2 lymph node dissection following standardization a preliminary study. J Gastrointest Surg 2009, 13(6):1058 1063. 7. Japanese Gastric Cancer Association: Japanese gastric cancer treatment guidelines 2010 (ver. 3). Gastric Cancer 2011, 14(2):113 123. 8. Ajani JA, Bentrem DJ, Besh S, D'Amico TA, Das P, Denlinger C, Fakih MG, Fuchs CS, Gerdes H, Glasgow RE, Hayman JA, Hofstetter WL, Ilson DH, Keswani RN, Kleinberg LR, Korn WM, Lockhart AC, Meredith K, Mulcahy MF, Orringer MB, Posey JA, Sasson AR, Scott WJ, Strong VE, Varghese TK Jr, Warren G, Washington MK, Willett C, Wright CD, McMillian NR, et al: Gastric cancer, version 2.2013: featured updates to the NCCN Guidelines. J Natl Compr Canc Netw 2013, 11(5):531 546. 9. Okines A, Verheij M, Allum W, Cunningham D, Cervantes A, Group EGW: Gastric cancer: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol 2010, 21(Suppl 5):v50 v54. 10. Wu CW, Hsiung CA, Lo SS, Hsieh MC, Chen JH, Li AF, Lui WY, Whang-Peng J: Nodal dissection for patients with gastric cancer: a randomised controlled trial. Lancet Oncol 2006, 7(4):309 315. 11. Hartgrink HH, van de Velde CJ, Putter H, Bonenkamp JJ, Klein Kranenbarg E, Songun I, Welvaart K, van Krieken JH, Meijer S, Plukker JT, van Elk PJ, Obertop H, Gouma DJ, van Lanschot JJ, Taat CW, de Graaf PW, von Meyenfeldt MF, Tilanus H, Sasako M: Extended lymph node dissection for gastric cancer: who may benefit? Final results of the randomized Dutch gastric cancer group trial. J Clin Oncol 2004, 22(11):2069 2077. 12. Japanese Gastric Cancer Association: Japanese classification of gastric carcinoma: 3rd English edition. Gastric Cancer 2011, 14(2):101 112. 13. Bonenkamp JJ, Hermans J, Sasako M, van De Velde CJ: Quality control of lymph node dissection in the Dutch randomized trial of D1 and D2 lymph node dissection for gastric cancer. Gastric Cancer 1998, 1(2):152 159. 14. Bonenkamp JJ, Hermans J, Sasako M, van de Velde CJ, Welvaart K, Songun I, Meyer S, Plukker JT, Van Elk P, Obertop H, Gouma DJ, van Lanschot JJ, Taat CW, de Graaf PW, von Meyenfeldt MF, Tilanus H, Dutch Gastric Cancer Group: Extended lymph-node dissection for gastric cancer. N Engl J Med 1999, 340(12):908 914. doi:10.1186/1471-2407-14-209 Cite this article as: Kim et al.: Standardization of D2 lymphadenectomy and surgical quality control (KLASS-02-QC): a prospective, observational, multicenter study [NCT01283893]. BMC Cancer 2014 14:209.
As first or corresponding author 1. SU Han, HT Kim, DH Seong, YS Kim, YS Park, YJ Bang, HK Yang, SJ Kim, Loss of the Smad3 expression increases susceptibility to tumorigenicity in human gastric cancer. Oncogene 2004, 23(7):1333-1341. 2. SU Han, HY Lee, JH Lee, WH Kim, HJ Nam, H Kim, YK Cho, MW Kim, KU Lee. Modulation of E-cadherin by hepatocyte growth factor induces aggressiveness of gastric carcinoma. Ann Surg 2005, 242(5), 676-683. 3. SH Jin, DY Kim, H Kim, IH Jeong, MW Kim, YK Cho, SU Han. Multidimensional learning curve in laparoscopy-assisted gastrectomy for early gastric cancer. Surg Endosc 2007, 21(1):28-33. 4. JM Park, SY Oh, JW Cha, SY Choi, HW Lee, H Kim, IH Jeong, SH Chin, MW Kim, YK Cho, SU Han. Comparison of laparoscopy-assisted total gastrectomy with conventional open total gastrectomy for treating early proximal gastric cancer. J Korean Surgical Soc 2007;72(4):290-296. 5. SU Han, TH Kwak, KH Her, YH Cho, C Choi, HJ Lee, S Hong, YS Park, YS Kim, TA Kim, SJ Kim. CEACAM5 and CEACAM6 are major target genes for Smad3-mediated TGFb signaling. Oncogene 2008:27(5);675-683 6. JM Park, DY Kim, JM Lee, CS Leem, SH Jin, YK Cho, SU Han. Laparoscopy-assisted total gastrectomy with pancreas-preserving splenectomy for early gastric cancer: A case report. J Korean Gastric Cancer Assoc 2007;7(2):97-101. 68. SR Lee, SU Han. Chemoprevention of gastric cancer. J Korean Clin Oncol 2007;3(1):4-11. 7. Park JM, Jin SH, Lee SR, Kim H, Jung IH, Cho YK, Han SU. Complications with laparoscopically assisted gastrectomy: multivariate analysis of 300 consecutive cases. Surg Endosc. 2008 Oct;22(10):2133-9.
8. Lee SR, Lee HW, Park JM, Jin SH, Kim H, Jeong IH, Kim YB, Kim JH, Cho YK, Han SU. Clinicopathologic features of the superficial spreading type of early gastric cancer. J Korean Surg Soc 2008;75(1):15-19 9. Outcomes after combined laparoscopic gastrectomy and laparoscopic choelcystectomy in gastric cancer patients. IH Jung, SU Choi, SR Lee, JH Kim, JM Park, SH Jin, EK Choi, YK Cho, SU Han. Eur Surg Res 2009;42:203-208. 10. Cytosine deaminase-producing human mesenchymal stem cells mediate an anti-tumor effect in a mouse xenograft model. MH You,WJ Kim, WY S,SR Lee, G Lee, S Choi, DY Kim, YM Kim, HS Kim, SU Han. J Gastroenterol Hepatol, 2009:Aug 24(8):1393-1400. IF 2.410 11. Han SU. Laparoscopic surgery for early gastric cancer. J Korean Med Assoc 2010;53(4):311-317. 12. Song HM, Lee SL, Hur H, Cho YK, Han SU. Linear-shaped gastroduodenostomy in totally laparoscopic distal gastrectomy. J Gastric Cancer 2010:10(2):69-74. 13. Hur H, Kim JY, Cho YK, Han SU. Technical feasibility of Robot-sewn anastomosis in robotic surgery for gastric cancer. J Laparoendosc Adv Surg Tech 2010, 20(8); 693-697, IF 1.012, ISSN 1092-6429, 2010 Oct 14. Oh DK, Hur H, Kim JY, Han SU, Cho YK. V-shaped liver retraction during a laparoscopic gastrectomy for gastric cancer. J Gastric Cancer 2010;10(3):133-136. 15. Kim JY, Hur H, Cho YK, Han SU. Gastric cancer associated with gastritis cystica profunda in patients without previous gastric surgery. J Korean Surg Soc 2010;79:S26-30. 16. Hur H, Kim HH, Hyung WJ, Cho GS, Kim W, Ryo SW, Han SU. Efficacy of NiTi Hand CAC 30 for jejunojejunostomy in gastric cancer surgery: results from a multicenter prospective randomized trial. Gastric Cancer 2011 Feb 24 14(2);124-129.
17. Han SU. Surgical treatment of gastroesophageal reflux disease. J Dae-Gyung Society of Gastroenterology 2011 ;14(1):19-21. 18. Park JM, Ahn CW, Yi X, Hur H, Lee KM, Cho YK, Han SU. Efficacy of endoscopic ultrasonography for prediction of tumor depth in gastric cancer. J Gastric Cancer 2011;11(2):109-115. 19. Xuan Y, Kim JY, Hur H, Cho YK, Thu VD, Han SU. Robotic redo fundoplication for incompetent wrapping after antireflux surgery: A case report. Int J Surg Case Rep 2011;2(8): 278-281. 20. Han SU. Minimal treatment for gastric cancer. Kor J Gastroenterol 2011; 58(5): 103-107. 21. Kim JJ, Kim JY, Hur H, Cho YK, Han SU. Clinicopathologic significance of gastric adenocarcinoma with neuroendocrine features. J Gastric Cancer 2011;11(4):1-5. 22. Kim Tae Gyun, Hur Hoon, Ahn Chang Wook, Xuan Yi, Cho Yong Kwan, Han Sang-Uk. Efficacy of Roux-en-Y reconstruction using two circular staplers after subtotal gastrectomy: results from a pilot study comparing with Billroth-I reconstruction. J Gastric Cancer 2011 11(4):219-224. 23. Jeong IH, Kim JH, Lee SR, Kim JH, Hwang JC, Shin SJ, Lee KM, Hur H, Han Sang-Uk. Minimally invasive treatment of gastric gastrointestinal stromal tumors: laparoscopic and endoscopic approach. Surg Laparosc Endosc Percutan Tech. Surg Laparosc Endosc Percutan Tech. 2012 Jun;22(3):244-50. 24. Hur H, Xuan Y, Ahn CW, Cho YK, Han SU. Trend and outcomes of minimally invasive surgery for gastric cancer :750 consecutive cases in seven years at a single center. Am J Surgery 2013. Jan;205(1):45-51. 25. The Effects of Helicobacter pylori on the prognosis of patients with curatively resected gastric cancers in a population with high infection rate. Hur H, Lee SR, Xuan Y, Kim YB, Lim YA, Cho YK, Han SU. J Korean Surg Soc. 2012 Oct;83(4):203-11.
26. Comparison of Surgical Outcomes between Robotic and Laparoscopic Gastrectomy for Gastric Cancer: The Learning Curve of Robotic Surgery. Kang BH, Xuan Y, Hur H, Ahn CW, Cho YK, Han SU. J Gastric Cancer. 2012 Sep;12(3):156-63. doi: 10.5230/jgc.2012.12.3.156. Epub 2012 Sep 30. 27. Hur H, Xuan Y, Kim YB, Lee G, Shim W, Yun J, Ham IH, Han SU. Expression of pyruvate dehydrogenase kinase-1 in gastric cancer as a potential therapeutic target. Int J Oncol. 2013 Jan;42(1):44-54. doi: 10.3892/ijo.2012.1687. 28. Ahn CW, Hur H, Han SU, Cho YK. Comparison of intracorporeal reconstruction after laparoscopic distal gastrectomy with extracorporeal reconstruction in the view of learning curve. J Gastric Cancer. 2013 Mar;13(1):34-43. 29. Hur H, Han SU. Totally laparoscopic surgery for gastric cancer. J Gastric Cancer. 2013 Mar;13(1):1-2. doi: 10.5230/jgc.2013.13.1.1. 30. Kim HH, Han SU, Kim MC, Hyung WJ, Kim W, Lee HJ, Ryu SW, Cho GS, Song KY, Ryu SY. Long-Term Results of Laparoscopic Gastrectomy for Gastric Cancer: A Large-Scale Case-Control and Case-Matched Korean Multicenter Study. J Clin Oncol. 2014 32(7); 627-634 31.Hur H, Paik MJ, Xuan Y, Nguyen DT, Ham IH, Yun J, Cho YK, Lee G, Han SU. Quantitative measurement of organic acids in tissues from gastric cancer patients indicates increased glucose metabolism in gastric cancer. PLoS One. 2014 Jun 9;9(6):e98581. 32. Reply to M. Honda et al. Kim HH, Son SY, Ahn S, Han SU. J Clin Oncol. 2014 Oct 1;32(28):3201-3202
As co-author 1. Ki Taek Nam, Ki-Baik Hahm, Sang-Yeon Oh, Marie Y대, Sang-Uk Han, Byeongwoo Ahn, Young-Bae Kim, Jin Seok Kang, Dong Deuk Jang, Ki-Hwa Yang, Dae-Yong Kim. The selective cyclooxygenase-2 inhibitor nimesulide prevents Helicobacter pylori-associated gastric cancer development in a mice model. Clin Cancer Res 2004;10(23):8105-8113. 2. Yeo M, DK Kim, SU Han, JE Lee, YB Kim, YK Cho, JH Kim, SW Cho, KB Hahm. Novel action of gastric proton pump inhibitor on suppression of Helicobacter pylori induced angiogenesis. Gut 2006 55(1):26-33. 3. JH Choi, BY Kim, YH Lim, JS Park, HC Kim, YK Cho, SU Han, MW Kim, HJ Joo. 5- Fluorouracil, mitomycin-c, and polysaccharide-k adjuvant chemoimmunotherapy for locally advanced gastric cancer: the prognostic significance of frequent perineural invasion. Hepatogastroenterology 2007;54(73):290-297. 4. Song KY, Hyung WJ, Kim HH, Han SU, Cho GS, Ryu SW, Lee HJ, Kim MC, KLASS Group. Is gastrectomy mandatory for all residual or recurrent gastric cancer following endoscopic resection? A large-scale Korean multi-center study. J Surg Oncol 2008; 98(1):6-10. 5. Kim W, Song KY, Lee HJ, Han SU, Hyung WJ, Cho GS. The impact of comorbidity on surgical outcomes in laparoscopy-assisted distal gastrectomy (LADG): a retrospective analysis of multi-center results Ann Surg 2008;248(5):793-799 6. Kim MC, Kim W, Kim HH, Ryu SW, Ryu SY, Song KY, Lee HJ, Cho GS, Han SU, Hyung WJ ; KLASS Group. Risk factors associated with complication following laparoscopy-assisted gastrectomy for gastric carnecr : a large-scale Korean multi-center study Ann Surg Oncol 2008;15(10):2692-2700 7. The impact of a high body mass index on laparoscopically assisted gastrectomy for gastric
cancer. HJ Lee, HH Kim, MC Kim, SY Ryu, W Kim, KY Song, GS Cho, SU Han, WJ Hyung, SW Ryu. 2009 apr 3 Surg Endosc 2009;23(11):2473-2479. 8. Song J, Lee HJ, Cho GS, Han SU, Kim MC, Ryu SW, Kim W, Song KY, Kim HH, Hyung WJ. Recurrence following laparoscopy-assisted gastrectomy for gastric cancer: a multicenter retrospective analysis of 1,417 patients. Ann Surg Oncol 2010, 17(7);1777-1786 9. Kim HH, Hyung WJ, Cho GS, Kim MC, Han SU, Kim W, Ryu SW, Lee HJ, Song KY. Morbidity and mortality of laparoscopic gastrectomy versus open gastrectomy for gastric cancer. An intrim report- A phase III multicenter, prospective, randomized trial (KLASS trial). Ann Surg 2010;251(3): 417-420. 10. Lee KM, Shin SJ, Hwang JC, Yoo BM, Cheong JY, Lim SG, Kim JK, Cho YK, Han SU, Lee SR, Kim JH. Proximal-releasing stent insertion under transnasal endoscopic guidance in patients with postoperative esophageal leakage. Gastrointest Endosc. 2010;72(1):180-185. 11. Jo Y, Han SU, Kim YJ, Kim JH, Kim ST, Kim SJ, Hahm KB. Suppressed Gastric Mucosal TGF-beta1 Increases Susceptibility to H. pylori-induced Gastric Inflammation and Ulceration: A Stupid Host Defense Response. Gut Liver 2010;4(1):43-53 12. Choi SH, Kim TG, Kim JY, Hur H, Han SU, Cho YK, Kim MW. Clinicopathologic analysis of remnant gastric cancer after distal partial gastrectomy: Experience of single center during 15 years. J Gastric Cancer 2010;10(2); 63-68. 13. Jee H, Nam KT, Kwon HJ, Han SU, Kim DY. Altered Expression and Localization of Connexin32 in Human and Murine Gastric Carcinogenesis. Dig Dis Sci. 2011 56(5); 1323-1332. 14. Kang KC, Cho GS, Han SU, Kim W, Kim HH, Kim MC, Hyung WJ, Ryu SY, Ryu SW, Lee HJ, Song KY; Korean Laparoscopic Gastrointestinal Surgery Study (KLASS) Group.Comparison of Billroth I and Billroth II reconstructions after laparoscopy-assisted distal gastrectomy: a retrospective analysis of large-scale multicenter results from Korea. Surg Endosc.
15. Kang SY, Han JH, Ahn MS, Lee HW, Jeong SH, Park JS, Cho YK, Han SU, Kim YB, Kim JH, Sheen SS, Lim HY, Choi JH. Helicobacter pylori infection as an independent prognostic factor for locally advanced gastric cancer patients treated with adjuvant chemotherapy after curative resection. Int J Cancer 2012;130(4):948-958. 16. Ahn HS, Yook JH, Park CH, Park YK, Yu W, Lee MS, Sang-Uk H, Ryu KW, Sohn TS, Kim HH, Choi SH, Noh SH, Hiki N, Sano T, Yang HK. General perioperative management of gastric cancer patients at high-volume centers. Gastric Cancer 2011; 14(2): 178-182 17. Seo SH, Hur H, Ahn CW, Yi X, Kim JY, Han SU, Cho YK. Operative risk factors in gastric cancer surgery for erlderly patients. J Gastric Cancer 2011;11(2): 116-121. 18. Kwon HJ, Won YS, Nam KT, Yoon YD, Jee H, Yoon WK, Nam KH, Kang JS, Han SU, Choi IP, Kim DY, Kim HC. Vitamin D3 upregulated protein 1 deficiency promotes N- methyl-n-nitrosourea and Helicobacter pylori-induced gastric carcinogenesis in mice. Gut. 2012 Jan, 61(1):53-63, 19. Choi BH, Song HS, An YS, Han SU, Kim JH, Yoon JK. Relation Between Fluorodeoxyglucose Uptake and Glucose Transporter-1 Expression in Gastric Signet Ring Cell Carcinoma. Nucl Med Mol Imaging (2011) 45(1):30 35 20. Kang BH, Hur H, Joung YS, Kim DK, Kim YB, An CW, Han SU, Cho YK. Giant mesenteric cystic lymphangioma originating from the lesser omentum in the abdominal cavity. J Gastric Cancer 2011:11(4): 243-247. 21. Vitamin D₃ upregulated protein 1 deficiency promotes N-methyl-N-nitrosourea and Helicobacter pylori-induced gastric carcinogenesis in mice. Kwon HJ, Won YS, Nam KT, Yoon YD, Jee H, Yoon WK, Nam KH, Kang JS, Han SU, Choi IP, Kim DY, Kim HC. Gut. 2012 Jan;61(1):53-63. 22. Park DJ, Han SU, Hyung WJ, Kim MC, Kim W, Ryu SY, Ryu SW, Song KY, Lee HJ,
Cho GS, Kim HH; Korean Laparoscopic Gastrointestinal Surgery Study (KLASS) Group. Long-term outcomes after laparoscopy-assisted gastrectomy for advanced gastric cancer: a large-scale multicenter retrospective study. Surg Endosc. 2012 Jun;26(6):1548-53. 23. Lim SG, Lee KM, Kim SS, Kim JS, Hwang JC, Shin SJ, Han SU, Kim JH, Cho SW. Endoscopic Approach for Postoperative Complications Following Laparoscopic-Assisted Gastrectomy in Early Gastric Cancer: Literature Review. Hepato-gastroenterology. 2012 Jun;59(116):1308-12. 24. Jung HK, Hong SJ, Jo YJ, Jeon SW, Cho YK, Lee KJ, Lee JS, Park HJ, Shin ES, Lee SH, Han SU. Updated Guidelines 2012 for Gastroesophageal Reflux Disease. The Korean Society of Neurogastroenterology and Motility. Korean J Gastroenterol. 2012 Oct 25;60(4):195-218. 25. Kim HH, Han SU, Kim MC, Hyung WJ, Kim W, Lee HJ, Ryu SW, Cho GS, Kim CY, Yang HK, Park do J, Song KY, Lee SI, Ryu SY, Lee JH; Korean Laparoscopic Gastrointestinal Surgery Study (KLASS) Group. Prospective randomized controlled trial (phase III) to comparing laparoscopic distal gastrectomy with open distal gastrectomy for gastric adenocarcinoma (KLASS 01).J Korean Surg Soc. 2013 Feb;84(2):123-30. 26. Keesang Yoo, M.D., Hoon Hur, M.D., Cheul Su Byun, M.D., Yi Xian, M.D., Sang-Uk Han, M.D., Yong Kwan Cho, M.D. Laparoscopic Resection of Gastric Submucosal Tumors: Outcomes of 141 Consecutive Cases in a Single Center THE KOREAN SOCIETY OF ENDOSCOIC & LAPAROSCOPIC SURGEONS 2012 Dec; 15(4): 106-113 27. Choi JW, Xuan Y, Hur H, Byun CS, Han SU, Cho YK. Outcomes of Critical Pathway in Laparoscopic and Open Surgical Treatments for Gastric Cancer Patients: Patients Selection for Fast-Track Program through Retrospective Analysis. J Gastric Cancer. 2013 Jun;13(2):98-105. 28. Xuan Y, Hur H, Byun CS, Han SU, Cho YK. Efficacy of intraoperative gastroscopy for tumor localization in totally laparoscopic distal gastrectomy for cancer in the middle third of the stomach. Surg Endosc. 2013 Nov;27(11):4364-70.
29. Ahn MS, Kang SY, Lee HW, Jeong SH, Park JS, Lee KJ, Cho YK, Han SU, Lee SY, Lim HY, Choi JH. 5-Fluorouracil, Mitomycin-C, and Polysaccharide-K versus Uracil-Ftorafur Polysaccharide-K as adjuvant chemoimmunotherapy for patients with locally advanced gastric cancer with curative resection. Onkologie 2013;36:421 426 30. Xuan Y, Hur H, Ham IH, Yun J, Lee JY, Shim W, Kim YB, Lee G, Han SU, Cho YK. Dichloroacetate attenuates hypoxia-induced resistance to 5-fluorouracil in gastric cancer through the regulation of glucose metabolism. Exp Cell Res. 2014;321:219-230. 31. Kim HI, Hur H, Kim YN, Lee HJ, Kim MC, Han SU, Hyung WJ. Standardization of D2 lymphadenectomy and surgical quality control (KLASS-02-QC): a prospective, observational, multicenter study [NCT01283893]. BMC Cancer. 2014 Mar 19;14:209. 32. Kang KK, Hur H, Byun CS, Kim YB, Han SU, Cho YK. Conventional cytology is not beneficial for predicting peritoneal recurrence after curative surgery for gastric cancer: results of a prospective clinical study. J Gastric Cancer. 2014 Mar;14(1):23-31. 33. Hur H, Lim SG, Byun C, Kang JK, Shin SJ, Lee KM, Kim JH, Cho YK, Han SU. Laparoscopy-Assisted Endoscopic Full-Thickness Resection with Basin Lymphadenectomy Based on Sentinel Lymph Nodes for Early Gastric Cancer. J Am Coll Surg. 2014 Jun 21. S1072-7515(14)00479-7. 34. Lee D, Kim YB, Chung SH, Lee SR, Byun CS, Han SU, Han JH. Primary gastric histiocytic sarcoma reminiscent of inflammatory pseudotumor: a case report with review of the literature. Korean J Pathol. 2014 Jun;48(3):258-62.