Abstract
The role of minimally invasive surgery in the treatment of transverse colon cancer is still controversial. The aim of this study is to investigate the advantages of a totally laparoscopic technique comparing open versus laparoscopic/robotic approach. Three hundred and eighty-eight patients with transverse colon cancer, treated with a segmental colon resection, were retrospectively analyzed. Demographic data, tumor stage, operative time, intraoperative complications, number of harvested lymph nodes and recovery outcomes were recorded. Recurrences and death were also evaluated during the follow-up. No differences were found between conventional and minimally invasive surgery, both for oncological long-term outcomes (recurrence rate p = 0.28; mortality p = 0.62) and postoperative complications (overall rate p = 0.43; anemia p = 0.78; nausea p = 0.68; infections p = 0.91; bleeding p = 0.62; anastomotic leak p = 0.55; ileus p = 0.75). Nevertheless, recovery outcomes showed statistically significant differences in favor of minimally invasive surgery in terms of time to first flatus (p = 0.001), tolerance to solid diet (p = 0.017), time to first mobilization (p = 0.001) and hospital stay (p = 0.004). Compared with laparoscopic approach, robotic surgery showed significantly better results for time to first flatus (p = 0.001), to first mobilization (p = 0.005) and tolerance to solid diet (p = 0.001). Finally, anastomosis evaluation confirmed the superiority of intracorporeal approach which showed significantly better results for time to first flatus (p = 0.001), to first mobilization (p = 0.003) and tolerance to solid diet (p = 0.001); moreover, we recorded a statistical difference in favor of intracorporeal approach for infection rate (p = 0.04), bleeding (p = 0.001) and anastomotic leak (p = 0.03). Minimally invasive approach is safe and effective as the conventional open surgery, with comparable oncological results but not negligible advantages in terms of recovery outcomes. Moreover, we demonstrated that robotic approach may be considered a valid option and an intracorporeal anastomosis should always be preferred.
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Introduction
Laparoscopic resection for colorectal cancer has already demonstrated long- and short-term benefits both for recovery outcomes and oncological safety [1]. However, the role of minimally invasive surgery in the treatment of transverse colon cancer is still controversial: the majority of previous randomized trials have excluded transverse colon cancer because the completeness of resection requires a technically difficult lymph node dissection around the middle colic artery and a hard reconstruction of intestinal continuity [2]. Over the last years, the increasing experience in laparoscopic and robotic colonic resections among surgeons has led to the cumulative publication of several studies comparing the oncological outcomes of the open to the minimally invasive approach for transverse colon cancer, but the real “gold standard” is still far to be defined [3, 4].
The aim of the study is to investigate the short- and long-term outcomes of transverse colon cancer surgery comparing open versus laparoscopic/robotic approach and a subgroup analysis will be performed to compare laparoscopic vs robotic resection and intracorporeal vs extracorporeal anastomosis.
Materials and methods
Study population and design
Three hundred and eighty-eight consecutive patients with mid transverse colon cancer, treated with a segmental colon resection between 2006 and 2016 in 28 Italian high-volume (more than 70 procedures/year) centers were retrospectively analyzed for this study. The protocol for research was approved by the institutional review board of all participating centers.
Mid transverse colon cancer was defined, after surgical exploration, as a tumor located in the mid part of the transverse colon excluding the 10 cm distal third in the left colonic angle (splenic flexure) and the 10 cm proximal part in the right colonic angle (hepatic flexure) of the transverse colon cancer [5].
All patients were operated by expert surgeons (more than 50 procedures/year) with open or minimally invasive (laparoscopic and robotic) approach.
To minimize the bias related to the different surgical techniques, only procedures performed according to the standardized criteria were included in the study: transverse colectomy is defined as the resection of a variable length of bowel included between the hepatic and the splenic flexure, with its lymph vascular supply along the middle colic pedicle, whose ligation is done at its origin. Both flexures are mobilized and the continuity of the bowel restored by fashioning an end-to-end or side-to-side anastomosis. In case of minimally invasive approach, the anastomosis was performed with intra- or extracorporeal technique depending on the advice of the surgeon. The period between surgery and discharge in all enrolled patients followed ERAS perioperative care protocol [6].
Outcomes
Primary outcomes: analyses comparing open versus minimally invasive approach in segmental transverse colectomy were performed. Moreover, between patients who underwent minimally invasive techniques, we compared outcomes from laparoscopic versus robotic approach.
Secondary outcomes: an intra- and extracorporeal anastomosis technique in the minimal invasive surgery was compared in the study population.
Data assessment
Demographic data (gender, age, body mass index (BMI), ASA), tumor stage (TNM), operative time, intraoperative complications, number of lymph nodes harvested, time to first flatus, mobilization, tolerance to solid diet and hospital discharge, were recorded.
We also collected data about postoperative surgical complications according to Clavien–Dindo classification [7]: surgical wound infections, anastomotic leakage, prolonged ileus and abdominal or bowel bleeding. The anastomotic leakage was defined as a condition of clinical or radiological anastomotic dehiscence that needed or did not need surgical revision. All centers performed a complete blood examination panel daily including C-reactive protein evaluation for subclinical leaks until patient discharge. We considered as bleeding the cases that required blood transfusion; on the other hand, we considered as anemia cases in which patients had a decrease in hemoglobin that did not need blood transfusions.
Pathological outcomes included the specimen length, the distance of the tumor from the proximal and the distal margin all measured in centimeters. We also reported the number of lymph nodes harvested and how many of these contained metastasis. Recurrences and death were also evaluated during the follow-up.
Statistical analysis
The analysis was performed with SPSS version 20.0 (IBM, Armonk, NY).
Continuous variables are described as median and interquartile range and compared by the Mann–Whitney U test. Categorical variables are reported as percentages and compared by the Fisher’s exact test. A p value of less than 0.05 was defined as statistically significant.
Propensity scores were obtained by a logistic regression model. The surgical technique (laparoscopic vs robotic) and the anastomosis technique (intra vs extracorporeal) were entered into the regression model as the dependent variable, and baseline patient and tumor characteristics (age, sex, BMI, ASA score and TNM stage) were the independent variables. Matching of the propensity scores was obtained with the “1:1 nearest neighbor” matching method, with a conservative caliper width of 20% of the standard deviation of the log of propensity score.
Results
A total of 388 patients with mid transverse colon cancer who underwent segmental resection were included in the study. Of these, 224 (57.7%) patients underwent open surgery and 164 (42.3%) underwent a minimally invasive approach; particularly, 146 (89%) had a laparoscopic segmental colon resection and 18 (11%) had a robotic colon resection. In terms of post-resection anastomosis, 33 (22.6%) patients received an intracorporeal anastomosis and 131 (77.4%) patients had an extracorporeal approach.
Primary outcomes
Open vs minimally invasive surgery
Firstly, we compared the characteristics of patients who underwent open surgery versus patients who underwent a minimally invasive approach. The two treatment groups were entirely matched for the analyzed characteristics; thus, no propensity matching was needed for further analysis. (Table 1).
There were no differences in demographic characteristics such as sex (53.57% vs 43.9% males; p = 0.2), age (72 median, 22.5 IQR vs 72 median, 21.5 IQR; p = 0.1), BMI (19 median, 21 IQR vs 19 median, 19 IQR; p = 0.1) and ASA score (2 median, 1 IQR vs 2 median, 1 IQR; p = 0.5). The two groups were also homogeneous for tumor stage characteristics: T (3 median, 0 IQR vs 3 median, 1 IQR; p = 0.1)—N (0 median, 1 IQR vs 0 median, 1 IQR; p = 0.8)—M (0 median, 0 IQR vs 0 median, 0 IQR p = 0.3).
Median operative time was 157 (80 IQR) min for open resections and 140 (75 IQR) min for minimally invasive approach (p = 0.102).
Recovery outcomes showed statistically significant differences in favor of minimally invasive surgery in terms of time to first flatus (4 median, 2 IQR vs 3 median, 2 IQR days; p = 0.001), tolerance to solid diet (4 median, 3 IQR vs 4 median, 2 IQR days; p = 0.017), time to first mobilization (2 median, 1 IQR vs 1 median, 1 IQR days; p = 0.001) and hospital stay (9 median, 5 IQR vs 7.5 median, 4 IQR days; p = 0.004).
About complications, we found no statistical differences: overall rate (31.7% vs 28%; p = 0.43), anemia (2.2% vs 1.8%; p = 0.78), nausea (3.1% vs 2.4%; p = 0.68), infections (4.4% vs 4.2%; p = 0.91), bleeding (5.3% vs 4.2%; p = 0.62), anastomotic leak (4.9% vs 3.6%; p = 0.55) and ileus (0.9% vs 0.6%; p = 0.75) were reported to be comparable between groups.
In terms of pathological outcomes, we found no differences in specimen length (20 median, 11.6 IQR vs 20 median, 12 IQR; p = 0.65), proximal margin (7 median, 7 IQR vs 7 median, 5 IQR; p = 0.46) and distal margin (8 median, 7 IQR vs 10 median, 6.5 IQR; p = 0.14), number of total lymph nodes harvested (13 median, 8 IQR vs 15 median, 7 IQR; p = 0.33) and number of lymph nodes positive for metastasis (0 median, 1 IQR vs 0 median, 1 IQR; p = 0.19). Finally, the mean follow-up of 3.4 ± 2.1 years for open approach and 3.3 ± 2.3 years for minimally invasive approach showed no differences between the two groups both in terms of recurrence rate (22.8% vs 18.3%; p = 0.28) and mortality (6.7% vs 5.5%; p = 0.62).
Laparoscopic vs robotic approach
We compared 146 patients who underwent laparoscopic surgery versus 18 patients underwent robotic surgery: the two groups were not homogeneous for baseline characteristics, so propensity score match was applied, resulting in a study population of 36 patients: 18 for each group (Table 2a, b).
Post-matching no differences were found in sex (88.8% vs 83.3,5% males; p = 0.99), age (73.2 median, 5.7 IQR vs 74.2 median, 6.7 IQR; p = 0.82), BMI (26.6 median, 5.6 IQR vs 25 median, 10.5 IQR kg/m2; p = 0.7) and ASA score (2 median, 0 IQR vs 3 median, 1 IQR; p = 0.43). About tumor staging, we recorded no differences between groups [T: 2 (2 IQR) vs 3 (0 IQR) p = 0.78; N: 0 (0 IQR) vs 0.5 (1 IQR) p = 0.48; M: 0 (0 IQR) vs 0 (0 IQR) p = 0.59].
Also, operative time was comparable between the two approaches [148.5 (51.2 IQR) vs 157.5 (60 IQR) min p = 0.82].
In terms of recovery, robotic approach showed significantly better results for time to first flatus (3.5 median, 1.7 IQR vs 2 median, 0.7 IQR days; p = 0.001), to first mobilization (1.5 median, 1 IQR vs 1 median, 0 IQR days; p = 0.005) and tolerance to solid diet (4.5 median, 1.7 IQR vs 2 median, 0 IQR days; p = 0.001); no differences were recorded in hospital stay (8 median, 4 IQR vs 8 median, 2 IQR days; p = 0.33).
About complications, we recorded no statistical differences between the two approaches for all examined outcomes: overall rate (28.8% vs 22.2%; p = 0.47), anemia (11.1% vs 5.5%; p = 0.91), nausea (16.6% vs 5.6%; p = 0.6), infections (27.7% vs 11.1%; p = 0.4), bleeding (27.7% vs 11.1%; p = 0.4), anastomotic leak (22.2% vs 11.1%; p = 0.65) and ileus (5.5% vs 0%; p = 0.98).
Analysis of pathological outcomes showed no differences in the number of lymph nodes harvested (11.5 median, 9.5 IQR vs 14.5 median, 3.7 IQR; p = 0.77), lymph nodes positive for metastasis (0 median, 0.7 IQR vs 0 median, 1 IQR; p = 0.37), proximal margin (7.5 median, 2 IQR vs 8 median, 9 IQR; p = 0.19), distal margin (9.7 median, 5.2 IQR vs 18 median, 8 IQR; p = 0.42) and specimen length (20 median, 6.2 IQR vs 30 median, 3 IQR; p = 0.47).
At the mean follow-up of 3.6 ± 2.4 years for laparoscopic and 3.4 ± 2.2 years for robotic approach, data showed no differences between the two groups both in terms of recurrence rate (33.3% vs 22.2%; p = 0.71) and mortality (38.8% vs 11.1%; p = 0.12).
Secondary outcome
Intra- versus extracorporeal anastomosis
Overall, 33 patients who underwent intracorporeal anastomosis were compared with 131 patients who underwent extracorporeal anastomosis: the two groups showed significant differences in demographic characteristics, so these inhomogeneities required propensity score match analysis (Table 3a, b).
Post-matching, the study population was composed of 66 patients (33 for each group) and there were no significant differences between the groups with regard to the baseline demographic variables [sex: 54.5% vs 45.45% males, p = 0.54; age: 74 (12 IQR) vs 69 (13 IQR) years, p = 0.21; BMI: 25.6 (6.4 IQR) vs 22.7 (5.7 IQR) kg/m2, p = 0.47; ASA: 2.5 (1.1 IQR) vs 3 (1 IQR), p = 0.33] as well as the stage of the tumors [T: 3 (1 IQR) vs 3 (1 IQR), p = 0.77; N: 0 (1 IQR) vs 0 (1 IQR), p = 0.12; M: 0 (0 IQR) vs 0 (0 IQR), p = 0.56).
Operative time was significantly shorter for intracorporeal anastomosis (160 median, 105 IQR vs 185 median, 70 IQR mins; p = 0.005).
Recovery outcomes showed that intracorporeal anastomosis had significantly better results for time to first flatus (3 median, 1 IQR vs 4 median, 1 IQR days; p = 0.001), to first mobilization (1 median, 1 IQR vs 2 median, 1 IQR days; p = 0.003) and tolerance to solid diet (4 median, 1 IQR vs 5 median, 1 IQR; p = 0.001); no differences were recorded in hospital stay (7 median, 3 IQR vs 8 median, 4 IQR days; p = 0.56).
In terms of complications, we recorded a statistical difference in favor of intracorporeal approach for overall rate (12.1% vs 48.5%; p = 0.001), infections (6.1% vs 24.2%; p = 0.04), bleeding (6.1% vs 39.4%; p = 0.001) and anastomotic leak (3% vs 18.1%; p = 0.03).
Analysis of pathological outcomes showed no differences in the number of lymph nodes harvested (11 median, 8 IQR vs 11 median, 9 IQR; p = 0.61), lymph nodes positive for metastasis (0 median, 2 IQR vs 0 median, 0 IQR; p = 0.18), proximal margin (8 median, 4 IQR vs 7 median, 4 IQR; p = 0.43), distal margin (10 median, 8 IQR vs 8 median, 5 IQR; p = 0.62) and specimen length (21 median, 9 IQR vs 19 median, 7 IQR; p = 0.13).
Data from a mean follow-up of 3.1 ± 2.2 years for intracorporeal and 3.2 ± 2.3 years for extracorporeal anastomosis again showed the same results for the two groups, both in terms of recurrence rate (18.2% vs 18.2%; p = 0.99) and mortality (0% vs 6.1%; p = 0.15).
Discussion
Recent RCTs and several reviews have demonstrated that minimally invasive surgery is nowadays considered the gold standard approach for colorectal cancers with excellent short-term outcomes and equivalent long-term oncologic outcomes compared to conventional open surgery [8,9,10]. However, less is known about minimally invasive approach to transverse colon cancer, both for its relatively low incidence and for its technical difficulties, which are higher than that for other site colon cancers: the challenging localization of the neoplasm, isolation and ligation of the middle colic vessels, lymphadenectomy, anatomical features of the transverse colon and its relationships with the spleen, pancreas, superior mesenteric vein, duodenum and Treitz ligament make transverse colon mobilization and dissection a challenging procedure.
Cumulating surgeons experience in this kind of surgical approach resulted in several studies which have compared minimally invasive and open surgery for transverse colon cancer [11,12,13]; however, the interpretation of the data is still limited. The major limitation is the complete absence in literature of studies which analyze and compare the open versus laparoscopic approach to transverse colon cancer on a specific type of resection: in fact, we can only find conclusions based on the mixed results from extended and segmental resections.
We have for the first time, in our best knowledge, compared open versus laparoscopic surgery for segmental resection of transverse colon cancer.
Since knowledge is lacking about the real surgical “gold standard” for the treatment of transverse colon cancer, the decision whether to perform an extended colectomy or a segmental transverse colectomy is based on a surgeon’s preference and segmental resection is one of the possibilities to treat this tumor location [14,15,16].
A recent systematic review with meta-analysis by Milone et al. [17] which involved 11,687 patients found that there were no statistical differences between transverse colectomy and extended hemicolectomy in short- and long-term oncological outcomes, concluding that the current literature gives the opportunity to perform either a segmental resection or an extended hemicolectomy to treat transverse colon cancer. In our study, we evaluated the advantages of a totally minimally invasive approach to transverse colon cancer and comparing it to the outcomes of open surgery. Evaluating the differences between conventional and minimally invasive surgery, our findings demonstrated that both approaches have similar oncological long-term outcomes without discrepancies in terms of postoperative complications. Nevertheless, in line with current literature [4, 18], minimally invasive techniques revealed better recovery results: return of bowel function and resumption of solid diet occurred significantly earlier in the minimally invasive group with a significantly shorter length of hospital stay. Thus, on the basis of our results, we can confirm that the minimally invasive approach to transverse colon cancer is feasible and safe, with similar operative time, morbidity and mortality rates when compared to the open approach.
In the area of mini-invasive surgery, we refined our analysis comparing patients who had undergone laparoscopic resection with those undergoing robotic resection. The current literature is very poor about the possibility of performing a transverse colon resection with a robotic approach but, because of high technical demand of this procedure, the advantages of robotic surgery, such as stable three-dimensional magnified view, can be maximized. de Angelis et al. [19] described their first experience on 22 patients who underwent robotic transverse colectomy matched with 22 patients who received a laparoscopic resection. The authors found no group differences in complications, recovery and oncological outcomes except for conversion rate which was higher in the laparoscopic population. Similarly, Jung and colleagues [20] described three robotic transverse colectomies, using a hand-sewn intracorporeal anastomosis; the authors found encouraging oncological outcomes with a low rate of complications and concluded that robotic transverse colectomy seems to be a safe and feasible technique which may minimize the necessity of mobilizing both colonic flexures, with facilitated intracorporeal anastomosis.
In our results, the analysis between patients who underwent laparoscopic or robotic surgery demonstrated equivalence of the two approaches except for the time to first flatus, tolerance to solid diet and patients’ mobilization which were lower in case of robotic procedures.
Finally, anastomosis evaluation confirmed that intracorporeal approach shows some advantages in terms of complications and recovery outcomes. As previously demonstrated [21], this can be easily explained because an intracorporeal end-to-end anastomosis allows to avoid an excessive dissection and colonic flexure takedown to extract the specimen; on the other hand, an extracorporeal anastomosis requires a mobilization of transverse colonic mesentery and of both colonic flexure to reach the mini-laparotomy site [22, 23]. van Oostendorp and colleagues [24] recently furnished a systematic review on 1492 patients who underwent laparoscopic right colectomy: they found a larger decrease in short-term morbidity and a significant decrease in the length of stay in favor of intracorporeal anastomosis. Similarly, Kelly et al.[25] analyzed data from 21 consecutive patients with a right colon cancer who underwent robotic resection with an intracorporeal anastomosis. The authors observed a low complication rate with good oncological and recovery outcomes, concluding that an intracorporeal approach is safe and feasible. Despite these studies, current literature lacks data about differences and advantages of intra- and extracorporeal anastomosis in transverse colon resections; our results, by this point of view, provide support to the effectiveness of intracorporeal anastomotic technique to provide surgeons a clearer perspective on which to perform a conscious choice during this type of colic resection.
Conclusion
Our results confirm that minimally invasive approach, both laparoscopic and robotic, is as safe and effective in transverse colon surgery as the conventional open surgery, with comparable oncological results and not negligible advantages in terms of recovery outcomes. Moreover, our analysis demonstrated that fashioning intracorporeal anastomosis determines an advantage in terms of recovery outcomes and complications rate.
Limitations
The major limitation of our study is its retrospective design and the small sample size which do not allow us to draw final conclusions; moreover, the multicentric enrollment which lasted 10 years does not permit to exclude a patients’ selection bias, particularly since different devices were used. Finally, because of a lack of consensus on the definition and assessment of post-surgical infections, results about this aspect must be read with caution.
Therefore, well-designed prospective multicentric trials and RCTs with homogeneous parameters are needed to set a real “gold standard” surgical procedure.
Availability of data and material
Upon request to the corresponding author.
Code availability
Not applicable.
References
Fleshman J, Sargent DJ, Green E (2007) Clinical outcomes of surgical therapy study group. Laparoscopic colectomy for cancer is not inferior to open surgery based on 5 year data from the COST study group trial. Ann Surg 246:655–662
Hewett PJ, Allardyce RA, Bagshaw PF, Frampton CM, Frizelle FA, Rieger NA, Smith JS, Solomon MJ, Stephens JH, Stevenson AR (2008) Short-term outcomes of the Australasian randomized clinical study comparing laparoscopic and conventional open surgical treatments for colon cancer: the ALCC trial. Ann Surg 248(5):728–738
Gouvas N, Pechlivanides G, Zervakis N, Kafousi M, Xynos E (2012) Complete mesocolic excision in colon cancer surgery: a comparison between open and laparoscopic approach. Colorectal Dis 14(11):1357–1364
Athanasiou CD, Robinson J, Yiasemidou M, Lockwood S, Markides GA (2017) Laparoscopic vs open approach for transverse colon cancer. A systematic review and meta-analysis of short and long term outcomes. Int J Surg 41:78–85
Milone M, Degiuli M, Allaix ME, Ammirati CA, Anania G, Barberis A, Belli A, Bianchi PP, Bianco F, Bombardini C, Burati M, Cavaliere D, Coco C, Coratti A, De Luca R, De Manzoni G, De Nardi P, De Rosa M, Delrio P, Di Cataldo A, Di Leo A, Donini A, Elmore U, Fontana A, Gallo G, Gentilli S, Giannessi S, Giuliani G, Graziosi L, Guerrieri M, Li Destri G, Longhin R, Manigrasso M, Mineccia M, Monni M, Morino M, Ortenzi M, Pecchini F, Pedrazzani C, Piccoli M, Pollesel S, Pucciarelli S, Reddavid R, Rega D, Rigamonti M, Rizzo G, Robustelli V, Rondelli F, Rosati R, Roviello F, Santarelli M, Saraceno F, Scabini S, Sica GS, Sileri P, Simone M, Siragusa L, Sofia S, Solaini L, Tribuzi A, Trompetto M, Turri G, Urso EDL, Vertaldi S, Vignali A, Zuin M, Zuolo M, D’Ugo D, De Palma GD (2020) Mid-transverse colon cancer and extended versus transverse colectomy: results of the Italian society of surgical oncology colorectal cancer network (SICO CCN) multicenter collaborative study. Eur J Surg Oncol 46(9):1683–1688
Vignali A, Elmore U, Cossu A, Lemma M, Calì B, de Nardi P, Rosati R (2016) Enhanced recovery after surgery (ERAS) pathway vs traditional care in laparoscopic rectal resection: a single-center experience. Tech Coloproctol 20(8):559–566
Makuuchi; PCB de OVDS de SPSBGVPC (2009) The Clavien–Dindo classification of surgical complications: five-year experience. Ann Surg 250(2):187–196
Veldkamp R, Kuhry E, Hop WC, Jeekel J, Kazemier G, Bonjer HJ, Haglind E, Påhlman L, Cuesta MA, Msika S, Morino M, Lacy AM (2005) Laparoscopic surgery versus open surgery for colon cancer: short-term outcomes of a randomised trial. Lancet Oncol 6:477–484
Guillou PJ, Quirke P, Thorpe H, Walker J, Jayne DG, Smith AM, Heath RM, Brown JM (2005) Short-term endpoints of conventional versus laparoscopic-assisted surgery in patients with colorectal cancer (MRC CLASICC trial): multicentre, randomised controlled trial. Lancet 365:1718–1726
Schwenk W, Haase O, Neudecker J, Muller JM (2005) Short term benefits for laparoscopic colorectal resection. Cochrane Database Syst Rev CD003145
Mistrangelo M, Allaix ME, Cassoni P, Giraudo G, Arolfo S, Morino M (2015) Laparoscopic versus open resection for transverse colon cancer. Surg Endosc 29:2196–2202
Kim MK, Won DY, Lee JK, Kang WK, Kye BH, Cho HM, Kim HJ, Kim JG (2015) Laparoscopic surgery for transverse colon cancer: short- and long-term outcomes in comparison with conventional open surgery. J Laparoendosc Adv Surg Tech A 25:982–989
Ozben V, de Muijnck C, Esen E, Aytac E, Baca B, Karahasanoglu T, Hamzaoglu I (2018) Is robotic complete mesocolic excision feasible for transverse colon cancer? J Laparoendosc Adv Surg Tech A 28(12):1443–1450
Chong CS, Huh JW, Oh BY, Park YA, Cho YB, Yun SH, Kim HC, Lee WY (2016) Operative method for transverse colon carcinoma: transverse colectomy versus extended colectomy. Dis Colon Rectum 59:630–639
Matsuda T, Sumi Y, Yamashita K, Hasegawa H, Yamamoto M, Matsuda Y, Kanaji S, Oshikiri T, Nakamura T, Suzuki S, Kakeji Y (2018) Optimal surgery for mid-transverse colon cancer: laparoscopic extended right hemicolectomy versus laparoscopic transverse colectomy. World J Surg 42(10):3398–3404
Leijssen LGJ, Dinaux AM, Amri R, Kunitake H, Bordeianou LG, Berger DL (2018) A transverse colectomy is as safe as an extended right or left colectomy for mid-transverse colon cancer. World J Surg. https://doi.org/10.1007/s00268-018-4582-1
Milone M, Manigrasso M, Elmore U, Maione F, Gennarelli N, Rondelli F, Velotti N, De Palma GD (2019) Short- and long-term outcomes after transverse versus extended colectomy for transverse colon cancer. A systematic review and meta-analysis. Int J Colorectal Dis 34(2):201–207
Ceccarelli G, Andolfi E, Biancafarina A, Rocca A, Amato M, Milone M, Scricciolo M, Frezza B, Miranda E, De Prizio M, Fontani A (2017) Robot-assisted surgery in elderly and very elderly population: our experience in oncologic and general surgery with literature review. Aging Clin Exp Res 29(Suppl 1):55–63
de’Angelis N, Alghamdi S, Renda A, Azoulay D, Brunetti F (2015) Initial experience of robotic versus laparoscopic colectomy for transverse colon cancer: a matched case-control study. World J Surg Oncol 13:295
Jung KU, Park Y, Lee KY, Sohn SK (2015) Robotic transverse colectomy for mid-transverse colon cancer: surgical techniques and oncologic outcomes. J Robot Surg 9(2):131–136
Milone M, Elmore U, Allaix ME, Bianchi PP, Biondi A, Boni L, Bracale U, Cassinotti E, Ceccarelli G, Corcione F, Cuccurullo D, Degiuli M, De Manzini N, D’Ugo D, Formisano G, Manigrasso M, Morino M, Palmisano S, Persiani R, Reddavid R, Rondelli F, Velotti N, Rosati R, De Palma GD (2019) Fashioning enterotomy closure after totally laparoscopic ileocolic anastomosis for right colon cancer: a multicenter experience. Surg Endosc. https://doi.org/10.1007/s00464-019-06796-w
Pigazzi A, Garcia-Aguilar J (2010) Robotic colorectal surgery: for whom and for what? Dis Colon Rectum 53:969–970
Stein SA, Bergamaschi R (2013) Extracorporeal versus intracorporeal ileocolic anastomosis. Tech Coloproctol 17(Suppl 1):S35–S39
van Oostendorp S, Elfrink A, Borstlap W, Schoonmade L, Sietses C, Meijerink J, Tuynman J (2017) Intracorporeal versus extracorporeal anastomosis in right hemicolectomy: a systematic review and meta-analysis. Surg Endosc 31(1):64–77
Kelley SR, Duchalais E, Larson DW (2018) Robotic right colectomy with intracorporeal anastomosis for malignancy. J Robot Surg 12(3):461–466
Acknowledgements
The authors acknowledge Dario Bruzzese, Giuseppe Servillo, Giuseppe De Simone, Katia Di Lauro: Department of Clinical Medicine and Surgery, Federico II University of Naples, Naples, Italy; Silvia Sofia: Department of Oncology, Surgical Oncology and Digestive Surgery Unit, San Luigi University Hospital, Orbassano, Turin, Italy; Marco Ettore Allaix, Mario Morino, Rossella Reddavid, Daniela Rega: Department of Surgical Sciences, University of Turin, Turin, Italy; Carlo Alberto Ammirati, Stefano Scabini: Oncologic Surgical Unit, Hospital Policlinic San Martino, Genova, Italy. Gabriele Anania, Cristina Bombardini: Department of Morphology, Experimental Medicine and Surgery, Section of General and Thoracic Surgery, University of Ferrara, Italy; Andrea Barberis, Roberta Longhin: Unit of General and Hepatobiliopancreatic Surgery, Galliera Hospital, Genova, Italy; Andrea Belli, Francesco Bianco: Division of Surgical Oncology, Department of Abdominal Oncology, IRCCS Fondazione “G. Pascale”, Naples, Italy; Giampaolo Formisano, Giuseppe Giuliani, Paolo Pietro Bianchi: Department of General and Minimally Invasive Surgery, Misericordia Hospital, Grosseto, Italy; Davide Cavaliere, Leonardo Solaini: General and Oncologic Surgery, Morgagni-Pierantoni Hospital, Forlì, Italy; Claudio Coco, Gianluca Rizzo: Department of General Surgery, Sacred Heart Catholic University, Rome, Italy;. Andrea Coratti, Angela Tribuzi: Division of Oncological and Robotic General Surgery, Careggi University Hospital, Florence, Italy; Raffaele De Luca, Michele Simone: Department of Surgical Oncology, National Cancer Research Center, Giovanni Paolo II Tumor Institute, Bari, Italy; Alberto Di Leo, Giovanni De Manzoni: Department of Surgery, General and Upper GI, Surgery Division, University of Verona, Verona, Italy; Paola De Nardi, Ugo Elmore, Riccardo Rosati, Andrea Vignali: Division of Gastrointestinal Surgery, San Raffaele Scientific Institut, Milan, Italy; Paolo Delrio, Ugo Pace, Daniela Rega: Colorectal Abdominal Surgery Division, IRCCS Fondazione “G. Pascale”, Naples, Italy; Antonio Di Cataldo, Giovanni Li Destri: Department of General Surgery and Medical-Surgical Specialties, University of Catania, Catania, Italy; Annibale Donini, Luigina Graziosi: Department of General and Emergency Surgery, University of Perugia, Perugia, Italy.; Andrea Fontana, Michela Mineccia: Department of HPB and Digestive Surgery, Ospedale Mauriziano Umberto I, Turin, Italy; Sergio Gentilli, Manuela Monni: Department of General Surgery, Maggiore della Carità Hospital, Novara, Italy. Mario Guerrieri, Monica Ortenzi: Department of General Surgery, Università Politecnica delle Marche, Ancona, Italy; Francesca Pecchini, Micaela Piccoli: Department of General and Emergency Surgery, Azienda Ospedaliera Universitaria Modena, Modena, Italy. Corrado Pedrazzani, Giulia Turri: Division of General and Hepatobiliary Surgery, Department of Surgical Sciences, Dentistry, Gynecology and Pediatrics, Unit of Colorectal Surgery, University of Verona, Verona, Italy; Sara Pollesel, Franco Roviello: Department of General Surgery and Surgical Oncology, University of Siena, Italy; Marco Rigamonti, Michele Zuolo: Operative Unit of General Surgery, Valli del Noce Hospital, Cles, Trento, Italy. Mauro Santarelli: Division of General and Emergency Surgery, Molinette Hospital, Turin, Italy; Federica Saraceno, Pierpaolo Sileri: Department of General Surgery, University of Rome Tor Vergata, Rome, Italy; Giuseppe Sigismondo Sica, Luigi Siragusa: Department of Minimally Invasive and GI Surgery, Policlinico Tor Vergata, Rome, Italy. Salvatore Pucciarelli, Matteo Zuin: Department of Surgical, Oncological and Gastroenterological Sciences, University of Padova, Padova, Italy.
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All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by MM, MD, NV, MM and SV. The first draft of the manuscript was written by MM and NV and all authors commented on previous versions of the manuscript. Final revision was made by DD’U and Giovanni DDP. All authors read and approved the final manuscript.
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Milone, M., Degiuli, M., Velotti, N. et al. Segmental transverse colectomy. Minimally invasive versus open approach: results from a multicenter collaborative study. Updates Surg 74, 127–135 (2022). https://doi.org/10.1007/s13304-021-01159-4
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DOI: https://doi.org/10.1007/s13304-021-01159-4