Abstract
The open surgeries and more recently minimal invasive surgeries aided by laparoscopic or robotic approaches are employed for rectal cancer treatment procedures. The open approach is the most commonly opted technique, but recent studies have also shown that laparoscopic total mesorectal excision (TME) has become the standard of care. There are certain shortcomings of laparoscopic surgery such as long learning curve, inadequate counter traction, limited dexterity, lack of tactile feedback and limited two-dimensional visions. Robotic surgery also offers several benefits to overcome the drawbacks of laparoscopic procedures, such as providing better dexterity and a more stable visualization. This study aims to analyse the surgical results in terms of completion of TME, short-term surgical outcomes and hospital stay in after open, laparoscopic- and robotic-assisted rectal resections respectively. A retrospective review of prospectively maintained database of patients operated for carcinoma rectum between January 2013 and August 2018 at Manipal Comprehensive Cancer Centre, Manipal-Vattikuti Institute of Robotic Surgery, Bangalore, was analysed in this study. The surgical parameters like completion of total mesorectal excision; proximal, distal and circumferential resection margins; number of nodes retrieved; and total post operative hospital stay were analysed in the open, laparoscopic-assisted and robotic-assisted groups. A total of 100 patients were included in the study consisting of 25, 25 and 50 patients each in the open, laparoscopic and robotic arms respectively. In case the desired results were not obtained using the advanced technique the procedure was converted and open technique was adopted. The conversion rate to open procedure was 8% (2of 25) in the laparoscopic-assisted group and 2% (1/50) in the robotic-assisted group. The average post operative hospital stay was 7.4, 7.36 and 6 days in the open, laparoscopic- and robotic-assisted group (p = 0.01) respectively. Robotic rectal resections show a trend towards better surgical results in the form of improved circumferential resection margins, completeness of TME and lower conversion rates.
Electronic supplementary material
The online version of this article (10.1007/s13193-020-01137-z) contains supplementary material, which is available to authorized users.
Keywords: Robotic surgery, Laparoscopy, Total mesorectal excision (TME), Rectal resection, Circumferential resection margins
Introduction
Surgical interventions for rectal cancer are performed with curative intentions. These procedures aim to remove the tumour segment with adequately clear margins and en bloc excision of mesentery containing blood vessels along with regional lymphatics. Conventionally open surgeries and more recently minimal invasive surgeries aided by laparoscopic or robotic approaches are employed for rectal cancer treatment procedures. The open approach is the most commonly opted for technique as it helps in overcoming the shortcomings of laparoscopic surgery such as long learning curve, inadequate counter traction, limited dexterity, lack of tactile feedback and limited two-dimensional vision [1, 2].
Robotic surgery however has the potential to overcome many of the drawbacks of laparoscopic procedures, especially by providing better dexterity and a more stable visualization [3]. The primary critical consideration in rectal cancer surgery is a sharp dissection along the embryological planes, which yields a total mesorectal excision (TME). Achieving complete TME in the narrow pelvic space needs technical expertise even with open approach (Fig. 1). Although these challenges are resolved to some extent by the use of laparoscopic technique, it has still not acquired the status of standard practice for complete TME and nerve preservation procedures [4].
Fig. 1.

Total mesorectal excision (TME) specimen of carcinoma rectum
The conversion rates for laparoscopic rectal TMEs to open are higher than that of colonic resections and lie in the range of 17% [5]. Robotic TME has been proposed as an alternative to conventional open and laparoscopic approach, but large-scale studies supporting its efficacy are limited. The key arguments in favour of robotic TME are lower conversion rates to open procedures and higher chances of nerve preservation [6, 7], whereas higher costs and longer operating time being are its drawbacks [8]. Previous studies have compared rectal resections done by either of the two techniques, i.e., robotic–laparoscopic or open–laparoscopic/robotic surgery, but very few studies have compared all the three modalities. This study aims to analyse the surgical results in terms of completion of TME, short-term surgical outcomes, and hospital stay in after open, laparoscopic- and robotic-assisted rectal resections respectively.
Methodology
A retrospective review of prospectively maintained database of patients operated for carcinoma rectum between January 2013 and August 2018 at Manipal Comprehensive Cancer Centre, Manipal-Vattikuti Institute of Robotic Surgery, Bangalore, was analysed in this study. The open, laparoscopy, and robotic procedures were performed by 3 different experienced colorectal surgeons since there are different unit preferences for the same. Rectal cancer was defined as any tumour within 15 cm of the anal verge. All patients underwent pelvic MRI to assess local infiltration and nodal metastasis as per the institutional protocol. Data of patients with local invasion (T2–3) with or without node involvement (N0–1) without metastases (M0) who underwent neo-adjuvant chemo/chemo-radiotherapy as well as early rectal lesions (T1, T2) who were considered for upfront resections were reviewed by the multidisciplinary team and included in the study. The neo adjuvant protocol included 50.4 Gy dose of external beam radiotherapy given in 28 fractions over 5.5 weeks, along with systemic 5-flurouracil-based chemotherapy followed by surgery 6–8 weeks later [9, 10]. The surgical parameters like completion of total mesorectal excision; proximal, distal and circumferential resection margins; number of nodes retrieved; and total post operative hospital stay were analysed in the open, laparoscopic-assisted and robotic-assisted groups. The only patients excluded were T4 patients at presentation or stage IV patients, medically unfit; there were no other exclusion criteria. Any patient eligible for surgery, either upfront by virtue of T1/T2 after MRI Pelvis and CECT or undergoing neoadjuvant Chemotherapy/Chemo radiation, was included.
Statistical Analysis
Data were presented as mean, standard deviation and range wherever appropriate. Comparisons between groups were made using Fisher’s exact test/chi square test, and p < 0.05 was considered statistically significant. All statistical analyses were conducted using SPSS version 20 software.
Results
A total of 100 patients were included in the study consisting of 25, 25 and 50 patients each in the open, laparoscopic and robotic arms respectively. The male:female ratio of the participants was 18:7, 21:4 and 34:16 respectively in the open, laparoscopic and robotic groups. Based on the location of the lower limit of tumour in relation to the anal verge, these rectal cancers were classified as upper (10–15 cm), mid (5–10 cm) and low rectal tumours (up to 5 cm) and included 47, 12 and 41 patients in each group. Thirteen patients had undergone abdomino-perineal resection (APR), and remaining 87 patients had undergone low anterior resections (LAR). The conversion rate to open was 8% (2of 25) in the laparoscopic-assisted group. When we split, upper alone was 0% and mid was 12% and lower was 12%; the mean of all together is 8% and 2% (1/50) in the robotic-assisted group. The average post operative hospital stay was 7.4, 7.36 and 6 days in the open, laparoscopic- and robotic-assisted group (p = 0.01) respectively.
On analysis of the post operative histopathology all the 100 patients had adenocarcinoma. This included 31 well differentiated, 58 moderately differentiated and 11 poorly differentiated tumours. The total number of lymph nodes harvested, circumferential resection margins obtained and the post operative hospital stay are summarized in Table 1.
Table 1.
Patient parameters studied and p value (CI = 95%)
| Open | Laparoscopic | Robotic | ||||||||
|---|---|---|---|---|---|---|---|---|---|---|
| N | Mean | SD | N | Mean | SD | N | Mean | SD | P value | |
| Age | 25 | 57.08 | 15.942 | 25 | 54.32 | 14.73 | 50 | 59.88 | 12.02 | .251 |
| Nodes | 25 | 9.96 | 5.420 | 25 | 10.36 | 4.47 | 50 | 14.02 | 5.44 | .002 |
| CRM | 25 | 1.508 | .7187 | 25 | 1.16 | .73 | 50 | 2.244 | .75 | .000 |
| Proximal margin | 25 | 9.180 | 5.6160 | 25 | 12.18 | 6.19 | 50 | 10.420 | 5.27 | .167 |
| Distal margin | 25 | 2.940 | 1.1930 | 25 | 2.64 | 1.94 | 50 | 3.750 | 2.10 | .038 |
| Hospital stay | 25 | 7.44 | 2.364 | 25 | 7.36 | 1.95 | 50 | 6.08 | .96 | .001 |
The final histopathological reports were compared to evaluate TME intactness. It was observed that two patients in the open arm and one patient each in the laparoscopic and robotic arm had an incomplete TME, but this difference was not statistically significant (p = 0.45). The proximal and distal margins were negative in all the 100 patients. On analysis of the sub group of patients with low rectal tumours who underwent LAR (N = 28) the mean distal resection margins were 3.14 + 1.5, 4 + 2.8 and 4.7 + 0.8 in the open, laparoscopic and robotic arms respectively(p = 0.21).
Discussion
Over time robotic-assisted surgery is gaining more acceptances by the surgeons and patients alike. The advantages of minimal invasive surgery in rectal resections include better visualization; illumination, better post operative recovery etc. have been well studied [11, 12]. In cancer surgery the most important factor is the oncological outcome of surgery. In rectal resections certain surgical parameters that can be used to gauge the oncological principles include circumferential resection margin (CRM), intactness of TME, adequacy of lymphadenectomy and proximal and distal marginal clearance [13]. Clear circumferential margin is of great importance because the risk of local recurrence increases three to four times when these margins are invaded with tumour cells [13, 14]. All these surgical parameters have in turn shown to also determine the overall survival and the disease free survival. The present study compared these surgical parameters in the open, laparoscopic-assisted and robotic-assisted rectal resection groups. The CRM obtained in the robotic arm patients was higher than the other two groups (p = 0.005) (ESM graph 1). The mesorectum was reported to be intact in 98% of patients in the robotic arm compared to 96% in laparoscopic and 92% in the open group (p = 0.38). Similar outcomes were noted in a meta-analysis where in robotic rectal resection was found to be associated with a lower conversion rate, lower rate of circumferential margin involvement and lower overall complication rate [15]. The advantages of the robotic surgical system, such as the three-dimensional visualization, reduction of the physiologic tremor and extra degrees of freedom in movement, may explain these beneficial effects.
With the increased use of preoperative radiotherapy in patients of rectal cancers, the prognostic significance of lymph node counts in rectal cancers is less clear. Some reports suggest that a decrease in the number of lymph nodes retrieved following neo-adjuvant therapy [16, 17]. Other parameters determine the number of lymph nodes isolated; these include patient age, tumour location, pathology techniques and surgical technique [17]. Significant difference was noted in the number of lymph nodes harvested among the three groups; the results were in favour of the robotic approach. This is in contrast to previous studies including meta-analysis, which have not demonstrated any significant difference in the number of lymph nodes harvested [18, 19]. The present study had included only patients who underwent neo-adjuvant treatment in all the three arms.
The difference between laparoscopic and robotic rectal resections in terms of hospital stay also favoured robotic approach; previous meta-analysis concurs with these findings [15]. In addition to the minimal invasive approach, lesser tissue trauma, better nerve preservation resulting in early catheter removal all contribute to reduced hospital stay.
Compared to laparoscopic colon cancer surgery, laparoscopic rectal resections have shown to be more challenging and associated with longer learning curve. One of the first randomized control trials to include patients with rectal cancer reported a 29% conversion rate [4]. Robotic system has advantages of high-definition three-dimensional vision and articular instruments with high dexterity, allowing more precise dissection in the deep and narrow pelvic cavity [19, 20]. In our study also there was one conversion in the robotic arm compared to two in the laparoscopic arm during the study period.
Limitation of our study was that it is not a randomized controlled trial. It was a single institution study. It was not a large volume study.
Conclusion
Robotic rectal resections show a trend towards better surgical results in the form of improved circumferential resection margins, completeness of TME and lower conversion rates. Further large-scale randomized studies with follow up results are warranted to confirm these findings.
Electronic supplementary material
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Footnotes
Key Message
Robotic rectal resections show a trend towards better surgical results in the form of improved circumferential resection margins, completeness of TME and lower conversion rates.
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References
- 1.Baik SH, Gincherman M, Mutch MG, Birnbaum EH, Fleshman JW. Laparoscopic vs open resection for patients with rectal cancer: comparison of perioperative outcomes and long-term survival. Dis Colon Rectum. 2011;54(1):6–14. doi: 10.1007/DCR.0b013e3181fd19d0. [DOI] [PubMed] [Google Scholar]
- 2.Avital S, Hermon H, Greenberg R, Karin E, Skornick Y. Learning curve in laparoscopic colorectal surgery: our first 100 patients. Isr Med Assoc J. 2006;8(10):683–686. [PubMed] [Google Scholar]
- 3.Mangano A, Valle V, Fernandes E, Bustos R, Gheza F, Giulianotti PC (2018) Operative technique in robotic rectal resection. Minerva Chir [DOI] [PubMed]
- 4.Guillou PJ, Quirke P, Thorpe H, Walker J, Jayne DG, Smith AMH, Heath RM, Brown JM. Short-term endpoints of conventional versus laparoscopic-assisted surgery in patients with colorectal cancer (MRC CLASICC trial): multicentre, randomised controlled trial. Lancet. 2005;365(9472):1718–1726. doi: 10.1016/S0140-6736(05)66545-2. [DOI] [PubMed] [Google Scholar]
- 5.Bonjer HJ, Deijen CL, Abis GA, Cuesta MA, van der Pas MHGM, de Lange-de Klerk ESM, Lacy AM, Bemelman WA, Andersson J, Angenete E, Rosenberg J, Fuerst A, Haglind E, COLOR II Study Group A randomized trial of laparoscopic versus open surgery for rectal cancer. N Engl J Med. 2015;372(14):1324–1332. doi: 10.1056/NEJMoa1414882. [DOI] [PubMed] [Google Scholar]
- 6.Trastulli S, Farinella E, Cirocchi R, Cavaliere D, Avenia N, Sciannameo F, et al. Robotic resection compared with laparoscopic rectal resection for cancer: systematic review and meta-analysis of short-term outcome. Color Dis. 2012;14(4):e134–e156. doi: 10.1111/j.1463-1318.2011.02907.x. [DOI] [PubMed] [Google Scholar]
- 7.Luca F, Valvo M, Ghezzi TL, Zuccaro M, Cenciarelli S, Trovato C, Sonzogni A, Biffi R. Impact of robotic surgery on sexual and urinary functions after fully robotic nerve-sparing total mesorectal excision for rectal cancer. Ann Surg. 2013;257(4):672–678. doi: 10.1097/SLA.0b013e318269d03b. [DOI] [PubMed] [Google Scholar]
- 8.Baek SK, Carmichael JC, Pigazzi A. Robotic surgery: colon and rectum. Cancer J. 2013;19(2):140–146. doi: 10.1097/PPO.0b013e31828ba0fd. [DOI] [PubMed] [Google Scholar]
- 9.Brown G, Daniels IR. Preoperative staging of rectal cancer: the MERCURY research project. Recent Results Cancer Res. 2005;165:58–74. doi: 10.1007/3-540-27449-9_8. [DOI] [PubMed] [Google Scholar]
- 10.Sauer R, Becker H, Hohenberger W, Rödel C, Wittekind C, Fietkau R, Martus P, Tschmelitsch J, Hager E, Hess CF, Karstens JH, Liersch T, Schmidberger H, Raab R, German Rectal Cancer Study Group Preoperative versus postoperative chemoradiotherapy for rectal cancer. N Engl J Med. 2004;351(17):1731–1740. doi: 10.1056/NEJMoa040694. [DOI] [PubMed] [Google Scholar]
- 11.van der Pas MH, Haglind E, Cuesta MA, Fürst A, Lacy AM, Hop WC, Bonjer HJ, COlorectal cancer Laparoscopic or Open Resection II (COLOR II) Study Group Laparoscopic versus open surgery for rectal cancer (COLOR II): short-term outcomes of a randomised, phase 3 trial. Lancet Oncol. 2013;14(3):210–218. doi: 10.1016/S1470-2045(13)70016-0. [DOI] [PubMed] [Google Scholar]
- 12.Jeong S-Y, Park JW, Nam BH, Kim S, Kang S-B, Lim S-B, Choi HS, Kim DW, Chang HJ, Kim DY, Jung KH, Kim TY, Kang GH, Chie EK, Kim SY, Sohn DK, Kim DH, Kim JS, Lee HS, Kim JH, Oh JH. Open versus laparoscopic surgery for mid-rectal or low-rectal cancer after neoadjuvant chemoradiotherapy (COREAN trial): survival outcomes of an open-label, non-inferiority, randomised controlled trial. Lancet Oncol. 2014;15(7):767–774. doi: 10.1016/S1470-2045(14)70205-0. [DOI] [PubMed] [Google Scholar]
- 13.Nagtegaal ID, Marijnen CAM, Kranenbarg EK, van de Velde CJH, van Krieken JHJM. Pathology Review Committee, et al. Circumferential margin involvement is still an important predictor of local recurrence in rectal carcinoma: not one millimeter but two millimeters is the limit. Am J Surg Pathol. 2002;26(3):350–357. doi: 10.1097/00000478-200203000-00009. [DOI] [PubMed] [Google Scholar]
- 14.Birbeck KF, Macklin CP, Tiffin NJ, Parsons W, Dixon MF, Mapstone NP, Abbott CR, Scott N, Finan PJ, Johnston D, Quirke P. Rates of circumferential resection margin involvement vary between surgeons and predict outcomes in rectal cancer surgery. Ann Surg. 2002;235(4):449–457. doi: 10.1097/00000658-200204000-00001. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 15.Sun Y, Xu H, Li Z, Han J, Song W, Wang J, et al. Robotic versus laparoscopic low anterior resection for rectal cancer: a meta-analysis. World J Surg Oncol. 2016;1:14. doi: 10.1186/s12957-016-0816-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 16.Baxter NN, Morris AM, Rothenberger DA, Tepper JE. Impact of preoperative radiation for rectal cancer on subsequent lymph node evaluation: a population-based analysis. Int J Radiat Oncol Biol Phys. 2005;61(2):426–431. doi: 10.1016/j.ijrobp.2004.06.259. [DOI] [PubMed] [Google Scholar]
- 17.Wong SL. Lymph node counts and survival rates after resection for colon and rectal cancer. Gastrointest Cancer Res GCR. 2009;3(2 Suppl 1):S33–S35. [PMC free article] [PubMed] [Google Scholar]
- 18.Liao G, Li Y-B, Zhao Z, Li X, Deng H, Li G. Robotic-assisted surgery versus open surgery in the treatment of rectal cancer: the current evidence. Sci Rep. 2016;27:6. doi: 10.1038/srep26981. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 19.Somashekhar SP, Ashwin KR, Rajashekhar J, Zaveri S. Prospective randomized study comparing robotic-assisted surgery with traditional laparotomy for rectal cancer—Indian study. Indian J Surg. 2015;77(Suppl 3):788–794. doi: 10.1007/s12262-013-1003-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 20.Pucci MJ, Beekley AC. Use of robotics in colon and rectal surgery. Clin Colon Rectal Surg. 2013;26(1):39–46. doi: 10.1055/s-0033-1333660. [DOI] [PMC free article] [PubMed] [Google Scholar]
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