Colorectal cancer

Optimal approach to elective resection for colon cancers (COL1-2a)

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Guideline contents > COL1-2a-b: What is the optimal approach to resection of colorectal cancers? (a: colon)

  Cite this page

Luck, A, Victoria Freeman, Dr Carina Chow, Dr Chip Farmer, Dr Henry Hicks, Cancer Council Australia Colorectal Cancer Guidelines Working Party. Clinical question:Surgical resection colon cancer . In: Clinical practice guidelines for the prevention, early detection and management of colorectal cancer. Sydney: Cancer Council Australia. [Version URL: https://wiki.cancer.org.au/australiawiki/index.php?oldid=173082, cited 2023 Jun 1]. Available from: https://wiki.cancer.org.au/australia/Guidelines:Colorectal_cancer.


Last modified:
7 November 2017 23:37:51

Background[edit source]

The surgical management of adenocarcinoma of the colon is achieved by resection of the primary tumour and anastomosis of the bowel. Until recent decades, this procedure required a laparotomy, usually entailing a long midline abdominal incision. With the advent of laparoscopic surgery in the late 1980s, techniques have been developed that allow a minimally invasive approach to the surgical management of colon cancer. In the last 15 years there have been several large multicentre randomised controlled trials (RCTs), as well as many smaller RCTs and meta-analyses, comparing open and laparoscopic approaches to the elective resection of colon cancer.

Systematic review evidence[edit source]

In patients diagnosed with colon cancer, what is the optimal resection strategy to achieve the best outcomes in terms of length and quality of life? (COL1-2a)

A systematic review was undertaken to ascertain the optimal surgical approach for resection of adenocarcinoma of the colon. The review focused on RCTs comparing open and laparoscopic colon resection, with particular reference to the outcomes of colon cancer mortality, disease free survival, colorectal cancer recurrence, lymph node harvest and perioperative mortality and morbidity, as well as surgery-related outcomes including postoperative pain levels, length of hospital stay, return of postoperative bowel function and operative time.

One systematic review and meta-analysis[1] and 17 RCTs reported across 40 articles[2][3][4][5][6][7][8][9][10][11][12][13][14][15][16][17][18][19][20][21][22][23][24][25][26][27][28][29][30][31][32][33][34][35][36][37][38][39][40][41][42] were identified that compared open and laparoscopic approaches to the resection of colon cancer. The systematic review and meta-analysis had a low risk of bias.[1] All the RCTs were considered to be at unclear or high risk of bias.[2][3][4][5][6][7][8][9][10][11][12][13][14][15][16][19][17][18][20][21][22][23][24][25][26][27][28][29][30][31][32][33][34][35][36][37][38][39][40][41][42]

The search strategy, inclusion and exclusion criteria, and quality assessment are described in detail in the Technical report.

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Oncological outcomes[edit source]

Colorectal cancer-specific mortality[edit source]

Thirteen RCTs reported colorectal cancer mortality rates.[7][10][11][15][21][25][29][31][33][38][39][41][42] The RCT with the longest follow-up reported a nonsignificant difference in cancer-specific mortality between the laparoscopic and open surgery groups at 95 months’ follow-up (16% versus 27%; p = 0.07).[21] However, there was an overall cancer-specific survival benefit in favour of the laparoscopic group at 10-year follow up (83% versus 65%; p = 0.02).[21]

Disease-free survival[edit source]

Six RCTs[7][8][10][17][18][25] reported 3-year, 5-year and/or 10-year disease-free survival outcomes for patients who underwent laparoscopic or open surgery. All trials were consistent in reporting no difference in disease-free survival between the different surgical approaches at any of these follow up intervals.

Colorectal cancer recurrence[edit source]

Eleven RCTs[5][7][8][10][12][17][21][25][26][31][42] reported either overall, local and/or distant colorectal cancer recurrence outcomes for laparoscopic versus open surgery, with follow up periods ranging from 2 to 10 years. One RCT[21] reported a statistically significant difference in colorectal cancer recurrence favouring the laparoscopic group at 10-year follow up (78% versus 64%; p = 0.05). All other RCTs and one meta-analysis[1] reported no difference in rates of colorectal cancer recurrence between groups who underwent open and laparoscopic colon cancer resection.

Lymph node harvest[edit source]

The number of lymph nodes removed at colon cancer surgery is considered to be a surrogate marker of the quality of the resection.[43][44] Some authors have reported that removal of fewer than 12 lymph nodes is associated with poor prognosis.

Ten RCTs reported the mean or median number of lymph nodes retrieved.[6][7][8][10][15][25][26][31][41][42] There was no evidence of a significant difference between the two techniques in the number of lymph nodes retrieved.

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Perioperative mortality and morbidity[edit source]

Perioperative mortality[edit source]

Thirteen RCTs reported either operative mortality, perioperative mortality or postoperative mortality.[7][10][11][15][21][25][29][31][33][38][39][41][42] No differences between open and laparoscopic techniques were reported for these outcomes.

Perioperative morbidity[edit source]

Five RCTs reported intraoperative complication rates.[11][13][15][29][37] Only one RCT, the Australasian Randomized Clinical Study Comparing Laparoscopic and Conventional Open Surgical Treatments for Colon Cancer (ALCCaS trial),[15] reported that the proportion of patients with one or more intraoperative complication was significantly lower among the open surgery group than the laparoscopic surgery group (3.7% versus 10.5%; p = 0.001). All other RCTs found no statistically significant difference in intraoperative complication rates between the operative techniques.[11][13][29][37]

Ten RCTs reported overall postoperative complication rates.[3][11][13][15][26][29][32][35][37][38] Most found no difference between open and laparoscopic surgery, although two RCTs[11][32] reported that laparoscopic surgery was associated with significantly lower rates of complications in the first 30 days postoperatively, compared with open surgery (15–21.1% versus 30–39.4%; p = 0.01–0.02). In addition, the ALCCaS trial[15] reported that, among patients aged over 70 years, there was a lower rate of postoperative complications (first 59 days) in the laparoscopic group, compared with the open surgery group (37.8% versus 50.7%; p = 0.02).

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Intraoperative blood loss[edit source]

Of the 10 RCTs that reported median or mean intraoperative blood loss,[11][15][25][26][31][37][38][39][41][42] six reported significantly reduced blood loss in the laparoscopic surgery group, compared with the open surgery group, with a weighted mean difference of 108.39 mL (98.02 mL versus 206.42 mL) for those that reported mean.[11][26][37][38][41] Each of the two trials that reported median blood loss also observed significantly less blood loss in the laparoscopic group, with differences in medians of 75 mL[38] and 55 mL.[41]

The clinical significance of these differences is unclear. Seven RCTs compared intraoperative, perioperative or postoperative blood transfusion rates between open and laparoscopic colon cancer surgery.[15][25][29][31][39][41][42] No differences were found between the groups in any of these trials.

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Injury to other organs[edit source]

In introducing new techniques to surgery, there is appropriate concern that hitherto-unreported complications may occur. Damage to organs out of the view of the laparoscope during laparoscopic colon cancer surgery is an example of this concern. Four RCTs[13][15][29][41] reported the incidence of intraoperative injury to small bowel, colon, splenic, ureteric, blood vessel and/or bladder in colon cancer surgery. None observed a difference between laparoscopic and open surgery in any of these parameters, with one exception: the ALCCaS trial[15] reported a higher rate of colonic serosal tear in the laparoscopic group, compared with the open surgery group (2.7% versus 0.3%; p = 0.02). This finding is of questionable clinical significance.

Reoperation[edit source]

Four RCTs[15][25][38][41] reported reoperation rates in the postoperative period. All of the trials reported trends, with one trial[41] favouring the laparoscopic group and the other three trials favouring the open group. However, none of these differences reached statistical significance (p values ranged from 0.13 to 0.54).

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Anastomotic complications[edit source]

Eleven RCTs[11][13][16][25][26][29][31][32][33][38][39] reported the rate or the cumulative incidence of anastomotic complication rates. None of the studies observed a difference in anastomotic complication rate between laparoscopic and open colon cancer surgery.

Postoperative small bowel obstruction[edit source]

Three RCTs reported reoperation rates for bowel obstruction in the early postoperative period.[25][29][34] Two of these trials[25][34] reported no significant difference between open and laparoscopic surgery, whereas one[29] found reported a higher obstruction rate in the laparoscopic group than the open surgery group (2.8% versus 0%; p = 0.02).

Six trials reported rate or cumulative incidence of bowel obstruction up to 5 years after surgery.[29][32][34][36][38][41] None observed a difference in the rate of bowel obstruction between open and laparoscopic surgery, although the CLASSIC trial[36] found a marginally lower rate of bowel obstruction in the 3 years following randomisation in the laparoscopic group than the open surgery group (1.3% versus 4.0%; p value not reported).

Wound complications[edit source]

Eight RCTs reported rates of postoperative wound infection[11][13][15][25][26][31][38][41] for laparoscopic versus open surgery. There was no statistically significant difference between the groups in any of these trials.

Several studies reported either postoperative incisional hernia rates or non-infectious wound complication rates. All observed numerical differences favouring the laparoscopic group, but in only one RCT[41] did this difference reach statistical significance (2.1% versus 7.4%; p < 0.001).

Respiratory complications[edit source]

Six RCTs reported postoperative pneumonia rates for open versus laparoscopic colon surgery.[15][16][26][29][31][41] Three trials[15][31][26] observed a non-significant trend in favour of the laparoscopic group (0.47–8.5% versus 2.2–10%; p = 0.11–0.41), while the other three trials (LAPKON II 2009, JCOG 2014, COLOR 2007) observed no difference.[16][29][41]

Several studies reported rates of atelectasis or respiratory failure and found there to be no difference between the groups.[11][25][42]

Other surgery-related outcomes[edit source]

Minimally invasive surgery has been developed to improve surgery related outcomes for the patient in the immediate postoperative period. Expected outcomes include less postoperative pain, more rapid return of postoperative bowel function, and a shortened hospital stay.

It should be noted that many of the RCTs used to analyse these outcomes were from the era prior to the widespread use of enhanced recovery after surgery (ERAS) protocols, which aim to improve postoperative outcomes with a combination of multimodal analgesic options (and minimal narcotic analgesia), early feeding with diet on the first postoperative day, minimal preoperative bowel preparation and early mobilisation.[45][46][47][48] It can only be speculated whether the following findings would be replicated if both open and laparoscopic surgery patients were exposed to such protocols in a RCT, or whether differences between open and laparoscopic surgery would be less apparent

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Postoperative pain[edit source]

A decrease in pain levels in the postoperative period is an expected outcome from minimally invasive surgery, including laparoscopic colon cancer surgery. Five RCTs[10][25][38][41][42] reported postoperative analgesic requirement for laparoscopic and open surgery groups and two RCTs[25][26] reported pain on the first postoperative day using a visual analogue pain scale.

Pain after laparoscopic colon surgery was consistently less than after open surgery, whether measured by overall postoperative analgesic requirement, days of postoperative narcotic analgesia use or number of postoperative narcotic injections. For example, in one study the laparoscopic group required fewer median days of narcotic use than open surgery group (3 days versus 4 days; p < 0.001),[10] while another reported a lower rate of postoperative narcotic use in the laparoscopic group than the open surgery group (32.8% versus 46%; p < 0.001).[41] One study[26] reported that mean visual analogue pain scores on the first postoperative day were lower among the laparoscopic surgery group than the open surgery group (3.5 versus 8.6; p < 0.001).

Length of hospital stay[edit source]

Sixteen RCTs[3][10][11][13][15][19][25][26][29][31][33][37][38][39][41][42] reported the postoperative length of hospital stay for patients undergoing laparoscopic or open resection. Fourteen found that patients having laparoscopic colectomy were discharged earlier,[3][10][11][15][19][25][26][31][33][37][38][39][41][42] with a statistically significant difference in 10 of the RCTs.[3][10][11][19][25][26][31][37][38][41] The ALCCaS trial,[15] which reported findings by age, observed a significantly lower length of stay in the laparoscopic group than the open surgery group in both the under-70 years group (median 7 [range 1–30] versus 8 [range 4–49]; p = 0.01) and the over-70 years group (8 [range 2–55] versus 10 [5–59]; p < 0.001). The weighted mean difference across nine studies was 1.9 days in favour of laparoscopic surgery (weighted mean 9.7 days versus 11.6 days).

Return of bowel function[edit source]

Eight RCTs[13][15][19][25][33][38][41][42] reported return of bowel function outcomes for open versus laparoscopic colon resection. Five trials reported time to first flatus[15][19][25][33][41] with three showing a statistically significant shorter period in favour of the laparoscopic group (mean difference 1.8–3.2 days; p values ranged from < 0.001 to 0.03).[15][19][41]

Four trials[13][15][33][38] reported time to first bowel action. All of these trials showed a shorter time to bowel action in the laparoscopic group, with two trials reaching statistical significance (mean 3.6 versus 4.4 days; p < 0.0001–0.01).[15][38]

Several trials reported the time to resuming normal diet, with most showing a shorter time for the laparoscopic group.[13][19][25][42] With most major centres adopting ERAS protocols that include the provision of solid food on the first postoperative day for both open and laparoscopic surgery, the time to resuming diet is no longer a useful outcome in open versus laparoscopic colon resection analysis.

Operative time[edit source]

Thirteen RCTs reported operative time for open versus laparoscopic colon resection.[10][11][15][19][25][26][29][31][33][37][38][41][42] Nine RCTs reported mean operative time, with open colon cancer surgery being faster than laparoscopic colon cancer surgery by a weighted mean difference of 44.51 minutes (weighted mean 146.61 minutes versus 191.16 minutes).[11][19][25][26][29][31][33][37][42] A further four RCTs used median operative times for their analysis, reporting a similar trend.[10][15][38][41]

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Evidence summary and recommendations[edit source]

Evidence Summary Level References
There is no difference in oncological results, as measured by cancer mortality, disease free survival, cancer recurrence and lymph node harvest between open and laparoscopic colon cancer surgery. II [5][6][7][8][10][11][15][17][18][21][25][26][29][31][33][38][39][41][42]
Open and laparoscopic colon cancer surgery can be performed with equivalent safety, with no significant difference in perioperative mortality or morbidity between the two techniques. II [7][10][11][13][15][21][25][29][31][33][37][38][39][41][42]
Laparoscopic colon cancer surgery provides improved short-term postoperative outcomes, compared with open colon cancer surgery, with less postoperative pain, a shortened time to return of bowel function and a shorter hospital stay. II [3][10][11][13][15][19][25][26][31][33][37][38][39][41][42]


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Evidence-based recommendationQuestion mark transparent.png Grade
Either an open approach or a laparoscopic approach can be used for the resection of colon cancer. 		D


Evidence-based recommendationQuestion mark transparent.png Grade
Laparoscopic colectomy has post-operative advantages over open colectomy and should be performed when the surgical expertise and hospital infrastructure are available. 		D



Practice pointQuestion mark transparent.png

Laparoscopic colectomy requires significant additional skills. Surgeons should ensure that they have mastered the necessary techniques before performing laparoscopic colectomy as an independent operator.


Practice pointQuestion mark transparent.png

Laparoscopic colorectal surgery is complex minimally invasive surgery that requires high-resolution video imaging and up-to-date equipment, including instrumentation and energy sources. It should only be undertaken in facilities that provide this infrastructure.

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Health system implications[edit source]

Clinical practice[edit source]

Surgeons in tertiary hospitals perform both laparoscopic and open colectomy as is appropriate for an individual patients. Smaller hospitals may not have access to the equipment necessary for safe laparoscopic colectomy.

Resourcing[edit source]

The recommendation to use a laparoscopic approach, where the requisite the surgical expertise and hospital infrastructure are available, is unlikely to have any resource issues for larger hospitals. Smaller hospitals may need resources to properly equip operating theatres for laparoscopic colectomy.

Barriers to implementation[edit source]

No barriers to the implementation of these recommendations are envisaged.

Discussion[edit source]

Unresolved issues[edit source]

There are no significant unresolved issues.

Studies currently underway[edit source]

There are no significant ongoing studies.

Future research priorities[edit source]

There is some evidence emerging of improved oncological results for colon cancer surgery with complete mesocolic excision and central vascular ligation.[49] Long-term data are awaited.

Next section: optimal approach to elective resection for rectal cancers

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References[edit source]

  1. ↑ 1.0 1.1 1.2 Di B, Li Y, Wei K, Xiao X, Shi J, Zhang Y, et al. Laparoscopic versus open surgery for colon cancer: a meta-analysis of 5-year follow-up outcomes. Surg Oncol 2013 Sep;22(3):e39-43 Available from: http://www.ncbi.nlm.nih.gov/pubmed/23643698.
  2. ↑ 2.0 2.1 COLOR Study Group. COLOR: a randomized clinical trial comparing laparoscopic and open resection for colon cancer. Dig Surg 2000;17(6):617-622 Available from: http://www.ncbi.nlm.nih.gov/pubmed/11155008.
  3. ↑ 3.0 3.1 3.2 3.3 3.4 3.5 3.6 Allardyce RA, Bagshaw PF, Frampton CM, Frizelle FA, Hewett PJ, Rieger NA, et al. Australasian Laparoscopic Colon Cancer Study shows that elderly patients may benefit from lower postoperative complication rates following laparoscopic versus open resection. Br J Surg 2010 Jan;97(1):86-91 Available from: http://www.ncbi.nlm.nih.gov/pubmed/19937975.
  4. ↑ 4.0 4.1 Allardyce RA, Bagshaw PF, Frampton CM, Frizelle FA, Hewett PJ, Rieger NA, et al. Australian and New Zealand study comparing laparoscopic and open surgeries for colon cancer in adults: organization and conduct. ANZ J Surg 2008 Oct;78(10):840-7 Available from: http://www.ncbi.nlm.nih.gov/pubmed/18959634.
  5. ↑ 5.0 5.1 5.2 5.3 Bagshaw PF, Allardyce RA, Frampton CM, Frizelle FA, Hewett PJ, McMurrick PJ, et al. Long-term outcomes of the australasian randomized clinical trial comparing laparoscopic and conventional open surgical treatments for colon cancer: the Australasian Laparoscopic Colon Cancer Study trial. Ann Surg 2012 Dec;256(6):915-9 Available from: http://www.ncbi.nlm.nih.gov/pubmed/23154392.
  6. ↑ 6.0 6.1 6.2 6.3 Braga M, Frasson M, Vignali A, Zuliani W, Di Carlo V. Open right colectomy is still effective compared to laparoscopy: results of a randomized trial. Ann Surg 2007 Dec;246(6):1010-4; discussion 1014-5 Available from: http://www.ncbi.nlm.nih.gov/pubmed/18043103.
  7. ↑ 7.0 7.1 7.2 7.3 7.4 7.5 7.6 7.7 7.8 Braga M, Frasson M, Zuliani W, Vignali A, Pecorelli N, Di Carlo V. Randomized clinical trial of laparoscopic versus open left colonic resection. Br J Surg 2010 Aug;97(8):1180-6 Available from: http://www.ncbi.nlm.nih.gov/pubmed/20602506.
  8. ↑ 8.0 8.1 8.2 8.3 8.4 8.5 Buunen M, Veldkamp R, Hop WC, Kuhry E, Jeekel J, Haglind E, et al. Survival after laparoscopic surgery versus open surgery for colon cancer: long-term outcome of a randomised clinical trial. Lancet Oncol 2009 Jan;10(1):44-52 Available from: http://www.ncbi.nlm.nih.gov/pubmed/19071061.
  9. ↑ 9.0 9.1 Delgado S, Lacy AM, García Valdecasas JC, Balagué C, Pera M, Salvador L, et al. Could age be an indication for laparoscopic colectomy in colorectal cancer? Surg Endosc 2000 Jan;14(1):22-6 Available from: http://www.ncbi.nlm.nih.gov/pubmed/10653230.
  10. ↑ 10.00 10.01 10.02 10.03 10.04 10.05 10.06 10.07 10.08 10.09 10.10 10.11 10.12 10.13 10.14 10.15 10.16 Fleshman J, Sargent DJ, Green E, Anvari M, Stryker SJ, Beart RW Jr, et al. Laparoscopic colectomy for cancer is not inferior to open surgery based on 5-year data from the COST Study Group trial. Ann Surg 2007 Oct;246(4):655-62; discussion 662-4 Available from: http://www.ncbi.nlm.nih.gov/pubmed/17893502.
  11. ↑ 11.00 11.01 11.02 11.03 11.04 11.05 11.06 11.07 11.08 11.09 11.10 11.11 11.12 11.13 11.14 11.15 11.16 11.17 11.18 11.19 11.20 Fujii S, Ishibe A, Ota M, Yamagishi S, Watanabe K, Watanabe J, et al. Short-term results of a randomized study between laparoscopic and open surgery in elderly colorectal cancer patients. Surg Endosc 2014 Feb;28(2):466-76 Available from: http://www.ncbi.nlm.nih.gov/pubmed/24122242.
  12. ↑ 12.0 12.1 12.2 Green BL, Marshall HC, Collinson F, Quirke P, Guillou P, Jayne DG, et al. Long-term follow-up of the Medical Research Council CLASICC trial of conventional versus laparoscopically assisted resection in colorectal cancer. Br J Surg 2013 Jan;100(1):75-82 Available from: http://www.ncbi.nlm.nih.gov/pubmed/23132548.
  13. ↑ 13.00 13.01 13.02 13.03 13.04 13.05 13.06 13.07 13.08 13.09 13.10 13.11 13.12 13.13 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 May;365(9472):1718-26 Available from: http://www.ncbi.nlm.nih.gov/pubmed/15894098.
  14. ↑ 14.0 14.1 Hazebroek EJ, Color Study Group. COLOR: a randomized clinical trial comparing laparoscopic and open resection for colon cancer. Surg Endosc 2002 Jun;16(6):949-53 Available from: http://www.ncbi.nlm.nih.gov/pubmed/12163961.
  15. ↑ 15.00 15.01 15.02 15.03 15.04 15.05 15.06 15.07 15.08 15.09 15.10 15.11 15.12 15.13 15.14 15.15 15.16 15.17 15.18 15.19 15.20 15.21 15.22 15.23 15.24 15.25 15.26 15.27 15.28 15.29 Hewett PJ, Allardyce RA, Bagshaw PF, Frampton CM, Frizelle FA, Rieger NA, et al. Short-term outcomes of the Australasian randomized clinical study comparing laparoscopic and conventional open surgical treatments for colon cancer: the ALCCaS trial. Ann Surg 2008 Nov;248(5):728-38 Available from: http://www.ncbi.nlm.nih.gov/pubmed/18948799.
  16. ↑ 16.0 16.1 16.2 16.3 16.4 Janson M, Lindholm E, Anderberg B, Haglind E. Randomized trial of health-related quality of life after open and laparoscopic surgery for colon cancer. Surg Endosc 2007 May;21(5):747-53 Available from: http://www.ncbi.nlm.nih.gov/pubmed/17342556.
  17. ↑ 17.0 17.1 17.2 17.3 17.4 Jayne DG, Guillou PJ, Thorpe H, Quirke P, Copeland J, Smith AM, et al. Randomized trial of laparoscopic-assisted resection of colorectal carcinoma: 3-year results of the UK MRC CLASICC Trial Group. J Clin Oncol 2007 Jul 20;25(21):3061-8 Available from: http://www.ncbi.nlm.nih.gov/pubmed/17634484.
  18. ↑ 18.0 18.1 18.2 18.3 Jayne DG, Thorpe HC, Copeland J, Quirke P, Brown JM, Guillou PJ. Five-year follow-up of the Medical Research Council CLASICC trial of laparoscopically assisted versus open surgery for colorectal cancer. Br J Surg 2010 Nov;97(11):1638-45 Available from: http://www.ncbi.nlm.nih.gov/pubmed/20629110.
  19. ↑ 19.00 19.01 19.02 19.03 19.04 19.05 19.06 19.07 19.08 19.09 19.10 19.11 Kim JS, Hur H, Min BS, Lee KY, Chung HC, Kim NK. Inflammatory and tumor stimulating responses after laparoscopic sigmoidectomy. Yonsei Med J 2011 Jul;52(4):635-42 Available from: http://www.ncbi.nlm.nih.gov/pubmed/21623607.
  20. ↑ 20.0 20.1 Kitano S, Inomata M, Sato A, Yoshimura K, Moriya Y, Japan Clinical Oncology Group Study. Randomized controlled trial to evaluate laparoscopic surgery for colorectal cancer: Japan Clinical Oncology Group Study JCOG 0404. Jpn J Clin Oncol 2005 Aug;35(8):475-7 Available from: http://www.ncbi.nlm.nih.gov/pubmed/16006574.
  21. ↑ 21.0 21.1 21.2 21.3 21.4 21.5 21.6 21.7 21.8 21.9 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 Jul;248(1):1-7 Available from: http://www.ncbi.nlm.nih.gov/pubmed/18580199.
  22. ↑ 22.0 22.1 Lacy AM, Delgado S, García-Valdecasas JC, Castells A, Piqué JM, Grande L, et al. Port site metastases and recurrence after laparoscopic colectomy. A randomized trial. Surg Endosc 1998 Aug;12(8):1039-42 Available from: http://www.ncbi.nlm.nih.gov/pubmed/9685538.
  23. ↑ 23.0 23.1 Lacy AM, García-Valdecasas JC, Delgado S, Castells A, Taurá P, Piqué JM, et al. Laparoscopy-assisted colectomy versus open colectomy for treatment of non-metastatic colon cancer: a randomised trial. Lancet 2002 Jun 29;359(9325):2224-9 Available from: http://www.ncbi.nlm.nih.gov/pubmed/12103285.
  24. ↑ 24.0 24.1 Lacy AM, García-Valdecasas JC, Piqué JM, Delgado S, Campo E, Bordas JM, et al. Short-term outcome analysis of a randomized study comparing laparoscopic vs open colectomy for colon cancer. Surg Endosc 1995 Oct;9(10):1101-5 Available from: http://www.ncbi.nlm.nih.gov/pubmed/8553212.
  25. ↑ 25.00 25.01 25.02 25.03 25.04 25.05 25.06 25.07 25.08 25.09 25.10 25.11 25.12 25.13 25.14 25.15 25.16 25.17 25.18 25.19 25.20 25.21 25.22 25.23 25.24 25.25 25.26 25.27 Li JC, Leung KL, Ng SS, Liu SY, Lee JF, Hon SS. Laparoscopic-assisted versus open resection of right-sided colonic cancer--a prospective randomized controlled trial. Int J Colorectal Dis 2012 Jan;27(1):95-102 Available from: http://www.ncbi.nlm.nih.gov/pubmed/21861071.
  26. ↑ 26.00 26.01 26.02 26.03 26.04 26.05 26.06 26.07 26.08 26.09 26.10 26.11 26.12 26.13 26.14 26.15 26.16 26.17 26.18 26.19 Liang JT, Huang KC, Lai HS, Lee PH, Jeng YM. Oncologic results of laparoscopic versus conventional open surgery for stage II or III left-sided colon cancers: a randomized controlled trial. Ann Surg Oncol 2007 Jan;14(1):109-17 Available from: http://www.ncbi.nlm.nih.gov/pubmed/17066227.
  27. ↑ 27.0 27.1 Clinical Outcomes of Surgical Therapy Study Group. A comparison of laparoscopically assisted and open colectomy for colon cancer. N Engl J Med 2004 May 13;350(20):2050-9 Available from: http://www.ncbi.nlm.nih.gov/pubmed/15141043.
  28. ↑ 28.0 28.1 Nelson H, Weeks JC, Wieand HS. Proposed phase III trial comparing laparoscopic-assisted colectomy versus open colectomy for colon cancer. J Natl Cancer Inst Monogr 1995;(19):51-6 Available from: http://www.ncbi.nlm.nih.gov/pubmed/7577206.
  29. ↑ 29.00 29.01 29.02 29.03 29.04 29.05 29.06 29.07 29.08 29.09 29.10 29.11 29.12 29.13 29.14 29.15 29.16 29.17 29.18 29.19 Neudecker J, Klein F, Bittner R, Carus T, Stroux A, Schwenk W, et al. Short-term outcomes from a prospective randomized trial comparing laparoscopic and open surgery for colorectal cancer. Br J Surg 2009 Dec;96(12):1458-67 Available from: http://www.ncbi.nlm.nih.gov/pubmed/19918852.
  30. ↑ 30.0 30.1 Ohtani H, Tamamori Y, Arimoto Y, Nishiguchi Y, Maeda K, Hirakawa K. A meta-analysis of the short- and long-term results of randomized controlled trials that compared laparoscopy-assisted and open colectomy for colon cancer. J Cancer 2012;3:49-57 Available from: http://www.ncbi.nlm.nih.gov/pubmed/22315650.
  31. ↑ 31.00 31.01 31.02 31.03 31.04 31.05 31.06 31.07 31.08 31.09 31.10 31.11 31.12 31.13 31.14 31.15 31.16 31.17 31.18 31.19 Pascual M, Alonso S, Parés D, Courtier R, Gil MJ, Grande L, et al. Randomized clinical trial comparing inflammatory and angiogenic response after open versus laparoscopic curative resection for colonic cancer. Br J Surg 2011 Jan;98(1):50-9 Available from: http://www.ncbi.nlm.nih.gov/pubmed/20799296.
  32. ↑ 32.0 32.1 32.2 32.3 32.4 32.5 Pecorelli N, Amodeo S, Frasson M, Vignali A, Zuliani W, Braga M. Ten-year outcomes following laparoscopic colorectal resection: results of a randomized controlled trial. Int J Colorectal Dis 2016 Jul;31(7):1283-90 Available from: http://www.ncbi.nlm.nih.gov/pubmed/27090804.
  33. ↑ 33.00 33.01 33.02 33.03 33.04 33.05 33.06 33.07 33.08 33.09 33.10 33.11 33.12 33.13 33.14 Procacciante F, De Luca M, Abilaliaj V, Chiaretti M, Diamantini G. Post-operative ileus in hemicolectomy for cancer: open versus laparoscopic approach. Ann Ital Chir 2013 Sep;84(5):557-62 Available from: http://www.ncbi.nlm.nih.gov/pubmed/24140940.
  34. ↑ 34.0 34.1 34.2 34.3 34.4 Schölin J, Buunen M, Hop W, Bonjer J, Anderberg B, Cuesta M, et al. Bowel obstruction after laparoscopic and open colon resection for cancer: results of 5 years of follow-up in a randomized trial. Surg Endosc 2011 Dec;25(12):3755-60 Available from: http://www.ncbi.nlm.nih.gov/pubmed/21667207.
  35. ↑ 35.0 35.1 35.2 Stucky CC, Pockaj BA, Novotny PJ, Sloan JA, Sargent DJ, O'Connell MJ, et al. Long-term follow-up and individual item analysis of quality of life assessments related to laparoscopic-assisted colectomy in the COST trial 93-46-53 (INT 0146). Ann Surg Oncol 2011 Sep;18(9):2422-31 Available from: http://www.ncbi.nlm.nih.gov/pubmed/21452066.
  36. ↑ 36.0 36.1 36.2 36.3 Taylor GW, Jayne DG, Brown SR, Thorpe H, Brown JM, Dewberry SC, et al. Adhesions and incisional hernias following laparoscopic versus open surgery for colorectal cancer in the CLASICC trial. Br J Surg 2010 Jan;97(1):70-8 Available from: http://www.ncbi.nlm.nih.gov/pubmed/20013936.
  37. ↑ 37.00 37.01 37.02 37.03 37.04 37.05 37.06 37.07 37.08 37.09 37.10 37.11 37.12 37.13 Tsimogiannis KE, Telis K, Tselepis A, Pappas-Gogos GK, Tsimoyiannis EC, Basdanis G. Α-defensin expression of inflammatory response in open and laparoscopic colectomy for colorectal cancer. World J Surg 2011 Aug;35(8):1911-7 Available from: http://www.ncbi.nlm.nih.gov/pubmed/21567262.
  38. ↑ 38.00 38.01 38.02 38.03 38.04 38.05 38.06 38.07 38.08 38.09 38.10 38.11 38.12 38.13 38.14 38.15 38.16 38.17 38.18 38.19 38.20 38.21 38.22 38.23 Veldkamp R, Kuhry E, Hop WC, Jeekel J, Kazemier G, Bonjer HJ, et al. Laparoscopic surgery versus open surgery for colon cancer: short-term outcomes of a randomised trial. Lancet Oncol 2005 Jul;6(7):477-84 Available from: http://www.ncbi.nlm.nih.gov/pubmed/15992696.
  39. ↑ 39.00 39.01 39.02 39.03 39.04 39.05 39.06 39.07 39.08 39.09 39.10 39.11 Vignali A, Di Palo S, Orsenigo E, Ghirardelli L, Radaelli G, Staudacher C. Effect of prednisolone on local and systemic response in laparoscopic vs. open colon surgery: a randomized, double-blind, placebo-controlled trial. Dis Colon Rectum 2009 Jun;52(6):1080-8 Available from: http://www.ncbi.nlm.nih.gov/pubmed/19581850.
  40. ↑ 40.0 40.1 Weeks JC, Nelson H, Gelber S, Sargent D, Schroeder G, Clinical Outcomes of Surgical Therapy (COST) Study Group. Short-term quality-of-life outcomes following laparoscopic-assisted colectomy vs open colectomy for colon cancer: a randomized trial. JAMA 2002 Jan 16;287(3):321-8 Available from: http://www.ncbi.nlm.nih.gov/pubmed/11790211.
  41. ↑ 41.00 41.01 41.02 41.03 41.04 41.05 41.06 41.07 41.08 41.09 41.10 41.11 41.12 41.13 41.14 41.15 41.16 41.17 41.18 41.19 41.20 41.21 41.22 41.23 41.24 41.25 41.26 41.27 41.28 41.29 Yamamoto S, Inomata M, Katayama H, Mizusawa J, Etoh T, Konishi F, et al. Short-term surgical outcomes from a randomized controlled trial to evaluate laparoscopic and open D3 dissection for stage II/III colon cancer: Japan Clinical Oncology Group Study JCOG 0404. Ann Surg 2014 Jul;260(1):23-30 Available from: http://www.ncbi.nlm.nih.gov/pubmed/24509190.
  42. ↑ 42.00 42.01 42.02 42.03 42.04 42.05 42.06 42.07 42.08 42.09 42.10 42.11 42.12 42.13 42.14 42.15 42.16 42.17 42.18 Kaiser AM, Kang JC, Chan LS, Vukasin P, Beart RW Jr. Laparoscopic-assisted vs. open colectomy for colon cancer: a prospective randomized trial. J Laparoendosc Adv Surg Tech A 2004 Dec;14(6):329-34 Available from: http://www.ncbi.nlm.nih.gov/pubmed/15684776.
  43. ↑ Nelson H, Petrelli N, Carlin A, Couture J, Fleshman J, Guillem J, et al. Guidelines 2000 for colon and rectal cancer surgery. J Natl Cancer Inst 2001 Apr 18;93(8):583-96 Available from: http://www.ncbi.nlm.nih.gov/pubmed/11309435.
  44. ↑ Scott KW, Grace RH. Detection of lymph node metastases in colorectal carcinoma before and after fat clearance. Br J Surg 1989 Nov;76(11):1165-7 Available from: http://www.ncbi.nlm.nih.gov/pubmed/2688803.
  45. ↑ Pritts TA, Nussbaum MS, Flesch LV, Fegelman EJ, Parikh AA, Fischer JE. Implementation of a clinical pathway decreases length of stay and cost for bowel resection. Ann Surg 1999 Nov;230(5):728-33 Available from: http://www.ncbi.nlm.nih.gov/pubmed/10561099.
  46. ↑ Zargar-Shoshtari K, Connolly AB, Israel LH, Hill AG. Fast-track surgery may reduce complications following major colonic surgery. Dis Colon Rectum 2008 Nov;51(11):1633-40 Available from: http://www.ncbi.nlm.nih.gov/pubmed/18536962.
  47. ↑ Kahokehr A, Sammour T, Zargar-Shoshtari K, Thompson L, Hill AG. Implementation of ERAS and how to overcome the barriers. Int J Surg 2009 Feb;7(1):16-9 Available from: http://www.ncbi.nlm.nih.gov/pubmed/19110478.
  48. ↑ Fearon KC, Ljungqvist O, Von Meyenfeldt M, Revhaug A, Dejong CH, Lassen K, et al. Enhanced recovery after surgery: a consensus review of clinical care for patients undergoing colonic resection. Clin Nutr 2005 Jun;24(3):466-77 Available from: http://www.ncbi.nlm.nih.gov/pubmed/15896435.
  49. ↑ Bertelsen CA, Neuenschwander AU, Jansen JE, Wilhelmsen M, Kirkegaard-Klitbo A, Tenma JR, et al. Disease-free survival after complete mesocolic excision compared with conventional colon cancer surgery: a retrospective, population-based study. Lancet Oncol 2015 Feb;16(2):161-8 Available from: http://www.ncbi.nlm.nih.gov/pubmed/25555421.

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Referring to the large bowel, comprising the colon and rectum.

A study in which people are allocated at random (by chance alone) to receive one of several clinical interventions. One of these interventions is the standard of comparison or control.

The main part of the large bowel, which absorbs water and electrolytes from undigested food (solid waste). Its four parts are the ascending colon, transverse colon, descending colon and sigmoid colon.

A recommendation formulated after a systematic review of the evidence, indicating supporting references.

A recommendation on a subject that is outside the scope of the search strategy for the systematic review, based on expert opinion and formulated by a consensus process.

The final section of the large bowel, ending at the anus.

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