|Ahead of print publication
Laparoscopic-assisted surgery versus open surgery for transverse colon cancer: A multicenter retrospective study
Hiroshi Tamagawa1, Masakatsu Numata1, Toru Aoyama1, Keisuke Kazama1, Yukio Maezawa1, Yosuke Atsumi1, Kentaro Hara1, Kazuki Kano1, Keisuke Komori1, Shinnosuke Kawahara1, Norio Yukawa1, Sho Sawazaki2, Hiroyuki Saeki2, Teni Godai3, Yasushi Rino1, Munetaka Masuda1
1 Department of Surgery, Yokohama City University, Yokohama, Japan
2 Department of Surgery, Yokohama Minami Kyosai Hospital, Yokohama, Japan
3 Department of Surgery, Fujisawa Shonandai Hospital, Takakura, Fujisawa, Japan
|Date of Submission||18-Jul-2020|
|Date of Decision||20-Dec-2020|
|Date of Acceptance||03-Jan-2021|
|Date of Web Publication||17-Jul-2021|
Department of Surgery, Yokohama City University, 3-9 Fukuura, Kanazawa, Yokohama 236-0004
Source of Support: None, Conflict of Interest: None
Introduction: Previous randomized controlled trials demonstrated similar oncological outcomes between laparoscopic-assisted (LA) and open (OP) colectomy; however, patients with transverse colon cancer were not analyzed. The aim of this study was to confirm the oncological safety and the advantages of the short- and long-term results of LA surgery for transverse colon cancer in comparison to OP surgery.
Materials and Methods: The study data were retrospectively collected from the databases of four hospitals. Patients with transverse colon cancer who underwent LA or OP R0 or R1 resection were registered.
Results: Among the 204 patients, 149 underwent OP colectomy and 55 underwent LA colectomy. The median follow-up period was 43 months. The rate of conversion to OP resection was 7.3%. The 5-year overall survival rate of the LA group was higher than that of the OP surgery group for all-stage patients (97.5% vs. 91.1%, P = 0.108), and it was similar in Stage II and Stage III patients (94.1% vs. 94.2%, P = 0.510). The LA group had significantly lower blood loss and a significantly longer operative time in comparison to the OP surgery group. Furthermore, the postoperative hospital stay was significantly shorter (9 vs. 13 days, P = 0.001) and the incidence of Grade ≥III complications was lower in the LA group (3.7% vs. 14.8%, P = 0.031).
Conclusion: We concluded that LA surgery for transverse colon cancer is oncologically safe and yields better short-term results in comparison to OP surgery.
Keywords: Laparoscopic colectomy, outcomes, transverse colon cancer
|How to cite this URL:|
Tamagawa H, Numata M, Aoyama T, Kazama K, Maezawa Y, Atsumi Y, Hara K, Kano K, Komori K, Kawahara S, Yukawa N, Sawazaki S, Saeki H, Godai T, Rino Y, Masuda M. Laparoscopic-assisted surgery versus open surgery for transverse colon cancer: A multicenter retrospective study. J Can Res Ther [Epub ahead of print] [cited 2021 Jul 29]. Available from: https://www.cancerjournal.net/preprintarticle.asp?id=321716
| > Introduction|| |
Colorectal cancer (CRC) remains the third frequent cause of mortality and cancer-specific cause of death worldwide. Laparoscopic-assisted (LA) colectomy is an established minimally invasive procedure since first reported in 1991. Since the surgical approach was widely introduced, many technical advancements to this procedure were reported, and several randomized controlled trials have demonstrated its safety, short-term benefits, and oncological efficacy in comparison to conventional open (OP) surgery, which include better cosmetic results, less blood loss, and less pain.,, Because of the technical difficulty of operation of the middle colic vessels and the dissection of lymph node around the middle colic artery by laparoscopy., In addition, many of these trials have excluded patients with transverse colon cancer due to the low incidence of the disease.
In this study, we performed a retrospective multicenter cohort analysis to compare the outcomes of LA surgery versus OP surgery for transverse colon cancer and evaluate the short- and long-term outcomes of LA surgery for transverse colon cancer.
| > Materials and Methods|| |
This retrospective multicenter study was performed using data from a prospectively maintained database of patients with transverse colon cancer undergoing radical surgery at the Yokohama City University, Department of Surgery, and its affiliated institutions between July 2000 and March 2020. Transverse colon cancer was defined as a tumor located between the hepatic and splenic flexures of the colon. A tumor located at the hepatic flexure or within 10 cm distal to the hepatic flexure was treated by extended right hemicolectomy; a tumor at the splenic flexure or within 10 cm proximal to the splenic flexure was treated by segmental colon resection or left extended hemicolectomy. Transverse colectomy was performed for tumor located centrally in the transverse colon. The primary endpoint was overall survival (OS) according to pathological stage. The secondary endpoints were recurrence-free survival (RFS) and the short-term results, including intraoperative blood loss, number of dissected lymph nodes, operative time, hospital stay, and postoperative complications.
According to the guidelines of the 2016 Japanese Society for Cancer of the Colon and Rectum, radical colectomy and lymph node resection were performed. In both groups, complete mesocolic excision with central vascular ligation was performed. In the present study, right hemicolectomy was defined as a procedure requiring division of the ileocolic, right colic (when present), and right branch of the middle colic vessels at their origins. Left hemicolectomy was defined as a procedure requiring division of the left colic and the left branch of the middle colic vessels at their origins. Transverse colectomy was defined as a procedure requiring the division of the middle colic vessels at their origins. The procedure was chosen based on the location and extent of the tumor. Conversion to OP surgery was defined as unplanned skin incision (wounds ≥8 cm in length) for the control of intraoperative complication, severe adhesion, or unexpected tumor extension. Hand-sewn functional end-to-end anastomosis was performed according to tumor location.
Definition of postoperative surgical complications
Postoperative surgical complications, graded according to the Clavien–Dindo classification, were determined retrospectively from the patient's records.
Evaluations and statistical analyses
The patients were divided into a LA surgery group and an OP surgery group. Pearson's Chi-square test or Fisher's exact test was used to compare the baseline characteristics between the two groups. The risk factors for morbidity were analyzed by binominal logistic regression. Linear regression models were fitted to a multivariate analysis. OS was defined as the period between surgery and death. OS and RFS curves were calculated using the Kaplan–Meier method and compared by the log-rank test. P < 0.05 was considered to indicate statistical significance. The IBM SPSS software package (version 21.0; SPSS Inc., Chicago, IL, USA) was used for all statistical analyses. This study was approved by the Institutional Review Board (IRB) of each institution.
This study was approved by the IRB Committee of the Yokohama City University and each institution. Informed consent for the use of clinical data without identifying personal data was obtained in all cases.
| > Results|| |
We evaluated 204 patients in the present study. A flow diagram of the selection process is shown in [Figure 1]. [Table 1] shows the clinicopathological characteristics of the present study. There were 149 cases in the OP surgery group and 55 cases in the LA surgery group. The median follow-up period was 43 months. Four cases required conversion to OP resection (7.3%; intraoperative bleeding, n = 1; T4b, n = 1; poor visual field, n = 2). The patients' ages ranged from 42 to 99 years (median: 73 years); 114 patients were male and 89 were female. The body mass index of the two groups did not differ to a statistically significant extent. Regarding the American Society of Anesthesiologists physical status (ASA-PS) and Eastern Cooperative Oncology Group performance status (ECOG-PS), the patients in the LA surgery group had better scores in comparison to the OP surgery group. The patients who underwent OP surgery had more advanced disease and unfavorable clinicopathological factors in comparison to the LA surgery group, as judged by the tumor size and pathological tumor stage. The short-term outcomes are shown in [Table 2]. The operation time of the LA surgery group was significantly longer in comparison to the OP surgery group (195 min vs. 152 min, P < 0.001), but there was significantly less blood loss (15 ml vs. 100 ml, P = 0.003). More lymph nodes were dissected in the LA surgery group; however, the difference was not statistically significant (16 vs. 12, P = 0.438). The rate of Clavien–Dindo grade ≥3 postoperative complications in the LA surgery group was lower than that in the OP surgery group (3.7% vs. 14.8%, P = 0.031). The postoperative hospital stay was significantly shorter in the LA surgery group (9 days vs. 13 days, P = 0.001).
|Table 1: Comparison of patient background factors between laparoscopic-assisted surgery group and open surgery group|
Click here to view
|Table 2: Relationship of short-term outcomes between laparoscopic-assisted surgery group and open surgery group|
Click here to view
The long-term outcomes are shown in [Figure 2] and [Figure 3]. The 5-year OS rate of the LA surgery group was better but no significantly different from that in the OP surgery group for all-stage patients (97.5% vs. 91.1%, P = 0.108), and it was similar for Stage II or Stage III patients (94.1% vs. 94.2%, P = 0.510). Regarding the 5-year RFS rate, there was no significant difference between the LA surgery and OP surgery groups in the overall population (all stages) or in the patients with Stage II or III disease.
|Figure 2: The relapse-free survival (a) and overall survival (b) rates in transverse colon carcinoma patients of all stages who underwent laparoscopic surgery or open surgery|
Click here to view
|Figure 3: The relapse-free survival (a) and overall survival (b) rates in Stage II and III transverse colon carcinoma patients who underwent laparoscopic surgery or open surgery|
Click here to view
| > Discussion|| |
The aim of this study was to confirm the oncological safety and short-term results of LA surgery for transverse colon cancer, which have been demonstrated in the treatment of colon cancer at other sites, in a retrospective multicenter cohort analysis. Several prospective randomized controlled trials have demonstrated that laparoscopic surgery for colon cancer achieves better short-term outcomes and equivalent long-term oncological results in comparison to OP surgery.,, However, subgroup analyses of patients with transverse colon cancer were not performed in these trials due to the technical difficulty in performing an oncologically adequate radical resection by laparoscopic surgery, and very few studies have mentioned laparoscopic colectomy for the treatment of transverse colon cancer.
In our study, LA radical surgery was safe and feasible for patients with transverse colon cancer. The severe postoperative complication rate was significantly lower in the LA surgery group. In previous studies, the postoperative complications and mortality rates were similar in the two groups.,,,,,,, Only Nakashima et al. reported a significantly lower rate of postoperative complications in patients undergoing laparoscopic surgery in comparison to those undergoing OP surgery for transverse colon cancer (6% vs. 36%). In addition, the retrospective study using the large data of right hemicolectomy for CRC including transverse colon was performed in Germany and OP right colectomy seems to have a higher risk for complications and mortality as compared to laparoscopic right colectomy. The main concern of laparoscopic surgery for transverse colon cancer is the risk of inadequate tumor resection because of the difficult performance of lymph node dissection around the middle colic artery by laparoscopy. Nordholm-Carstensen et al. reported that laparoscopic surgery for transverse colonic cancers associated with a lower rate of mesocolic resection plane and fewer lymph nodes harvested. However, although the patients who underwent laparoscopic surgery in this study tended to have significantly smaller lesions and a less advanced stage in comparison to those who underwent OP surgery, a larger number of lymph nodes were dissected by laparoscopic surgery in comparison to OP surgery. Moreover, our study also highlighted several short-term benefits of LA surgery in comparison to OP surgery, including less intraoperative blood loss and a shorter hospital stay. These results suggest that laparoscopic surgery for transverse colon cancer is feasible.
In our study, the 5-year OS and RFS rates for all stages were similar in both the groups, despite the stage distribution bias in the operation period. We therefore assessed the survival rate separately in patients with advanced disease (tumor-node-metastasis classification Stage II–III). The OS and RFS curves were similar and the 5-year OS and RFS rates in these stages did not differ to a statistically significant extent. Similar results have been reported in previous studies and recent misanalyses., Yamaguchi et al. analyzed the big data of laparoscopic surgery and OP surgery for transverse colon cancer and reported that the 3-year OS and RFS rates in patients with Stage II and III disease did not differ to a statistically significant extent between the two operative approaches. Zhao et al. also reported that the 5-year OS and 5-year disease-free survival rates did not differ between the two groups to a statistically significant extent. Including the present study, all previous reports have suggested that LA surgery for transverse colon cancer is oncologically tolerable.
Special attention is required when interpreting the current results, as this study is associated with some potential limitations. First, this was a retrospective study. Thus, our findings in this series may have been observed merely by chance. Second, there may be a selection bias and the different backgrounds of patients undergoing LA and OP surgery in the present study. Inexperienced surgeons or institutions may avoid performing LA surgery for certain patients. Moreover, because the tumor diameter was significantly larger in the OA group than in the LA group and the stage was advanced, the simple comparisons and the drawing of definitive conclusions were difficult. Third, there was a time bias in this study, as the data were collected in multiple institutions between 2000 and 2020. Surgical procedures and perioperative care might have changed over this period. Fourth, because we analyzed a multicenter cohort, there were many missing values for some examination items, such as the ASA-PS and ECOG-PS. Considering these limitations, the current results should be validated by another study.
| > Conclusion|| |
Laparoscopic radical surgery was a safe and feasible approach in the treatment of transverse colon cancer. In comparison to the OP approach, the LA procedure was oncologically safe and was associated with less blood loss, a shorter length of hospital stay, and possibly, a lower morbidity rate.
The work is supported, in part, by the nongovernmental organization Yokohama Surgical Research Group, Association of Healthcare Corporation, Yoshiki Dermatology Clinic Ginza, and Social Hearth Corporation Foundation Pond Friends Association (Fukuoka Wajiro Hospital).
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
| > References|| |
Edwards BK, Noone AM, Mariotto AB, Simard EP, Boscoe FP, Henley SJ, et al
. Annual Report to the Nation on the status of cancer, 1975-2010, featuring prevalence of comorbidity and impact on survival among persons with lung, colorectal, breast, or prostate cancer. Cancer 2014;120:1290-314.
Jacobs M1, Verdeja JC, Goldstein HS. Minimally invasive colon resection (laparoscopic colectomy). Arch Surg 2009;144:1127.
Lacy AM, Delgado S, Castells A, Prins HA, Arroyo V, Ibarzabal A, et al
. The long-term results of a randomized clinical trial of laparoscopy-assisted versus open surgery for colon cancer. Ann Surg 2008;248:1-7.
Guillou PJ, Quirke P, Thorpe H, Walker J, Jayne DG, Smith AM, et al
. Short-term endpoints of conventional versus laparoscopic-assisted surgery in patients with colorectal cancer (MRC CLASICC trial): Multicentre, randomised controlled trial. Lancet 2005;365:1718-26.
Colon Cancer Laparoscopic or Open Resection Study Group; Buunen M, Veldkamp R, Hop WC, Kuhry E, Jeekel J, et al
. Survival after laparoscopic surgery versus open surgery for colon cancer: Long-term outcome of a randomised clinical trial. Lancet Oncol 2009;10:44-52.
Kuwabara K, Matsuda S, Fushimi K, Ishikawa KB, Horiguchi H, Fujimori K. Quantitative comparison of the difficulty of performing laparoscopic colectomy at different tumor locations. World J Surg 2010;34:133-9.
Zmora O, Bar-Dayan A, Khaikin M, Lebeydev A, Shabtai M, Ayalon A, et al
. Laparoscopic colectomy for transverse colon carcinoma. Tech Coloproctol 2010;14:25-30.
Watanabe T, Muro K, Ajioka Y, Hashiguchi Y, Ito Y, Saito Y, et al
. Japanese society for cancer of the colon and rectum (JSCCR) guidelines 2016 for the treatment of colorectal cancer. Int J Clin Oncol 2018;23:1-34.
Clavien PA, Barkun J, de Oliveira ML, Vauthey JN, Dindo D, Schulick RD, et al
. The clavien-dindo classification of surgical complications. Ann Surg 2009;250:187-96.
Nordholm-Carstensen A, Jensen KK, Krarup PM. Oncological outcome following laparoscopic versus open surgery for cancer in the transverse colon: A nationwide cohort study. Surg Endosc 2018;32:4148-57.
Feo CF, Feo CV, Fancellu A, Ginesu GC, Cherchi G, Zese M, et al
. Laparoscopic versus open transverse-incision right hemicolectomy: A retrospective comparison study. ANZ J Surg 2019;89:E292-6.
Toritani K, Watanabe J, Nakagawa K, Suwa Y, Suwa H, Ishibe A, et al
. Randomized controlled trial to evaluate laparoscopic versus open surgery in transverse and descending colon cancer patients. Int J Colorectal Dis 2019;34:1211-20.
Bracale U, Merola G, Pignata G, Corcione F, Pirozzi F, Cuccurullo D, et al
. Laparoscopic resection with complete mesocolic excision for splenic flexure cancer: Long-term follow-up data from a multicenter retrospective study. Surg Endosc 2020;34:2954-62.
Kim HJ, Lee IK, Lee YS, Kang WK, Park JK, Oh ST, et al
. A comparative study on the short-term clinicopathologic outcomes of laparoscopic surgery versus conventional open surgery for transverse colon cancer. Surg Endosc 2009;23:1812-7.
Akiyoshi T, Kuroyanagi H, Fujimoto Y, Konishi T, Ueno M, Oya M, et al
. Short-term outcomes of laparoscopic colectomy for transverse colon cancer. J Gastrointest Surg 2010;14:818-23.
Yamamoto M, Okuda J, Tanaka K, Kondo K, Tanigawa N, Uchiyama K. Clinical outcomes of laparoscopic surgery for advanced transverse and descending colon cancer: A single-center experience. Surg Endosc 2012;26:1566-72.
Nakashima M, Akiyoshi T, Ueno M, Fukunaga Y, Nagayama S, Fujimoto Y, et al
. Colon cancer in the splenic flexure: Comparison of short-term outcomes of laparoscopic and open colectomy. Surg Laparosc Endosc Percutan Tech 2011;21:415-8.
Bosker RJI, van't Riet E, de Noo M, Vermaas M, Karsten TM, Pierie JP. Minimally invasive versus open approach for right-sided colectomy: A study in 12,006 patients from the Dutch surgical colorectal audit. Dig Surg 2019;36:27-32.
Chi Z, Li Z, Cheng L, Wang C. Comparison of long-term outcomes after laparoscopic-assisted and open colectomy for splenic flexure cancer. J BUON 2018;23:322-8.
Gavriilidis P, Katsanos K. Laparoscopic versus open transverse colectomy: A systematic review and meta-analysis. World J Surg 2018;42:3008-14.
Baloyiannis I, Perivoliotis K, Ntellas P, Dadouli K, Tzovaras G. Comparing the safety, efficacy, and oncological outcomes of laparoscopic and open colectomy in transverse colon cancer: A meta-analysis. Int J Colorectal Dis 2020;35:373-86.
Yamaguchi S, Tashiro J, Araki R, Okuda J, Hanai T, Otsuka K, et al
. Laparoscopic versus open resection for transverse and descending colon cancer: Short-term and long-term outcomes of a multicenter retrospective study of 1830 patients. Asian J Endosc Surg 2017;10:268-75.
Zhao L, Wang Y, Liu H, Chen H, Deng H, Yu J, et al
. Long-term outcomes of laparoscopic surgery for advanced transverse colon cancer. J Gastrointest Surg 2014;18:1003-9.
[Figure 1], [Figure 2], [Figure 3]
[Table 1], [Table 2]