Guidelines for Laparoscopic Resection of Curable Colon and Rectal Cancer

PREAMBLE

This is one of a series of clinical practice guidelines issued by the Society of American Gastrointestinal and Endoscopic Surgeons (SAGES), and has been developed in collaboration with the American Society of Colon and Rectal Surgeons (ASCRS).  There has been considerable controversy regarding the safety of utilizing a laparoscopic approach for malignant colorectal disease, as well as many lessons learned from clinical trials and experience.  The following recommendations are for surgeons regarding the safe performance of laparoscopic resection for curable colon and rectal cancer.    This guideline also provides suggestions for the overall clinical management of patients with curable colon and rectal cancer who are being treated by properly trained and experienced minimally invasive surgeons.  This document will not address the endoscopic screening or surveillance for colorectal cancer.  SAGES and the ASCRS have previously published a joint statement regarding the credentialing process. 1    SAGES also has guidelines that specifically address privileging for laparoscopic procedures in general.2  The current recommendations are graded and linked to the evidence utilizing the definitions in the appendix A and B.

DISCLAIMER

Clinical practice guidelines are intended to indicate the best available approach to medical conditions as established by systematic review of available data, clinical practice and expert opinion.  The approach suggested may not necessarily be the only acceptable approach given the complexity of the health care environment.  These guidelines are intended to be flexible, as the surgeon must always choose the approach best suited to the individual patient and variables in existence at the moment of decision.  These guidelines are applicable only to those physicians who are appropriately credentialed and address the clinical situation in question, regardless of specialty.

Guidelines are developed under the auspices of the Society of Gastrointestinal and Endoscopic Surgeons and its various committees, and approved by the Board of Governors.  Each guideline is developed with a systematic approach, and includes review of the available literature and expert opinion when published data alone are insufficient to make recommendations. All guidelines undergo appropriate multidisciplinary review prior to publication, and recommendations are considered valid at the time of publication.  Because new developments in medical research and practice can change recommendations, all guidelines undergo scheduled, periodic review to reflect any changes.  The systematic development process of clinical practice guidelines began in 2005, and will be applied to all revisions as they come up for scheduled review, as well as all new guidelines.

I.  DIAGNOSTIC EVALUATION

Standard screening guidelines should be followed.3,4  Published guidelines on preoperative assessment for open resection of curable colon or rectal cancer should be followed.5 A laparoscopic approach requires additional considerations.

A.  Recommendation: The segment of colon or rectum containing the tumor should be localized accurately preoperatively. (Level III evidence, Grade C recommendation)

Once a colon or rectal cancer has been detected, preoperative staging, assessment of resectability, and assessment of the patient’s operative risks are indicated. The entire colon and rectum should be evaluated, usually with colonoscopy. Consideration of a minimally invasive surgical approach requires accurate localization of the tumor, as a known cancer may not be apparent during laparoscopic visualization from the serosal aspect of the bowel. Without accurate localization, the wrong segment of colon may be removed.6 Colonoscopy is accurate for localization of a tumor in the rectum and cecum only, and may otherwise be inaccurate.7 Other methods for identifying the segment of colon involved include tattooing at the time of colonoscopy8, barium enema, and CT colonography. CT scan may be helpful in the setting of a large tumor, but does not reliably localize smaller tumors. If the tumor is not localized preoperatively, intraoperative colonoscopy may be helpful.

B.  Recommendation: The liver should be evaluated with preoperative CT scan or ultrasound (US), or intraoperative US (Level II evidence, Grade B recommendation)

The liver is not routinely evaluated preoperatively when open resection of colon cancer is performed.5 Liver metastases of >1cm diameter are detected by CT scan with sensitivities and specificities of 90 and 95%.9  However, this rarely results in a change in the operative strategy in many institutions. Routine use is noted in centers where synchronous resection of the primary and metastatic tumors is performed. Instead, the liver is palpated intraoperatively or intraoperative US may be performed. A laparoscopic approach precludes the ability to palpate the liver, although the visualization provided may reveal surface lesions not detected by CT scan. Given the inability to palpate the liver intraoperatively, preoperative assessment of the liver by CT or US10 or intraoperative US should be performed.

In the case of rectal cancer, staging CT scan or transanal rectal US is routine and not impacted by the laparoscopic approach.11 Preoperative abdominal CT or hepatic US is required in planning surgical treatment for rectal cancer, as the findings may change the operative approach significantly.

II.  PREPARATION FOR OPERATION

Standard guidelines are published regarding the safety of outpatient bowel preparation, use of prophylactic antibiotics, blood cross matching and thromboembolism prophylaxis.5

Recommendation: Preoperative mechanical bowel preparation to facilitate manipulation of the bowel during a laparoscopic approach (Level III evidence, Grade C recommendation)

Preoperative mechanical bowel preparation is the common practice in North America, despite lack of clear evidence of benefit from meta-analysis12 and randomized controlled trials to support its use.13-17  Although some authors have recommended no preparation, an empty colon is generally considered to facilitate manipulation of the bowel during laparoscopic colon and rectal surgery.  When considering a completely laparoscopic approach with intracorporeal anastomosis, a longer period of preparation is used by some authors.18 

III.  OPERATIVE ISSUES

Operative Techniques – Colon

Recommendation: Laparoscopic resection should follow standard oncologic principles: proximal ligation of the primary arterial supply, adequate proximal and distal margins, and appropriate lymphadenectomy (Level I evidence, Grade A recommendation)

Existing guidelines for colon and rectal cancer surgery have established levels of evidence and grades of recommendation for the following: proximal and distal colonic resection margins (determined by the area supplied by the primary feeding arterial vessel(s)); lymphadenectomy with a minimum of 12 lymph nodes harvested; and ligation of the named feeding vessel at its origin.19 The two adequately powered randomized trials of laparoscopic colectomy for curable colon cancer followed these oncologic principles 10,20 and showed no significant difference in proximal and distal bowel margins, number of lymph nodes retrieved, and, in the Clinical Outcomes of Surgical Therapy Study Group (COST) trial, perpendicular length of the primary vascular pedicle.21

These recommendations determine which portions of the procedure may be performed intracorporeally or extracorporeally. In a patient with a normal body mass index (BMI) undergoing right colectomy it is often feasible to ligate the base of the ileocolic pedicle via a periumbilical incision. In a heavier patient, this might best be performed intracorporeally. For all other vessels, the origin of the vessel will generally need to be ligated intracorporeally unless a larger incision such as used for hand-assisted procedures permits safe access to the base of the vessels.  Inability to comply with oncologic principles should prompt conversion to an open operation.

Operative Techniques – Rectum

Recommendation: Laparoscopic resection for rectal cancer should follow standard oncologic principles: adequate distal margin, ligation of the base of the superior rectal/inferior mesenteric artery, and mesorectal excision (Level II evidence, Grade B recommendation)

Operative guidelines for open rectal surgery have been established with levels of evidence and grades of recommendation for techniques relevant only to the rectum.19,22 These include a distal margin of 1-2cm, removal of the blood supply and lymphatics up to the origin of the superior rectal artery (or inferior mesenteric artery if indicated), and appropriate mesorectal excision with radial clearance.

Laparoscopic resection of rectal cancer has not been evaluated in a randomized trial. Prospective23,24 and retrospective25,26 case series have suggested that the procedure is feasible in carefully selected patients. The confines of the pelvis confer additional challenges on the laparoscopic approach, particularly for distal rectal tumors. The ability to perform an oncologically adequate laparoscopic resection for rectal cancer will depend on tumor factors such as size, proximal or distal location, and patient factors including anatomy of the pelvis (narrow or wide), obesity, bulky uterus, and effect of prior radiation on tissue planes. Inability to comply with oncologic principles should prompt conversion to an open operation.

Contiguous Organ Attachment

Recommendation: Open approach is required if a laparoscopic en-bloc resection for a T4 lesion cannot be safely performed. (Level II evidence, Grade B recommendation)

Current guidelines for open colon and rectal cancer surgery recommend en bloc resection to manage locally advanced adherent colorectal tumors.19 Histologically negative margins achieved with en bloc resection are considered curative. Preoperative studies such as CT scan may suggest a bulky tumor invasive into an adjacent organ and guide the decision to perform an open resection. A known T4 colonic cancer may prompt an open approach.27 The ability to perform en bloc resection laparoscopically is dependent on the structure to which the tumor is adherent, in addition to surgeon skill and experience. When the goal is curative resection, intraoperative discovery of a T4 lesion requires conversion, unless the surgeon is capable of properly resecting the lesion en bloc.

Tumor Perforation and the “No-Touch Technique”

Recommendation: Perforation of the tumor should be avoided. (Level III evidence, Grade C recommendation)

Excessive force or use of instruments not suited to handling of the bowel may cause inadvertent perforation.6  Inadvertent perforation results in increased local recurrence rates and a significant reduction in 5-year survival.28  Thus, although the “no-touch technique” (with early ligation of vessels) is not specifically recommended, avoidance of perforating the tumor with handling is advocated.

For open resection of curable colorectal carcinoma, the value of the no-touch technique, with early ligation of the vascular supply, has not been proven.29, 30 In laparoscopic resection, some surgeons employ a medial-to-lateral approach with early ligation of the mesenteric vessels. No oncologic benefit of this approach has been shown.

Prevention of Wound Implants

Recommendation: The extraction incision should be mechanically protected during specimen retrieval. (Level II evidence, Grade C recommendation)

Wound implants, or recurrence of cancer, have been reported at both the extraction site incision and the port sites.31,32,33 The phenomenon has prompted extensive research.34-43

Most measures suggested to prevent wound implants have been generated by in vitro and in vivo animal models, not clinical practice. The results of gasless laparoscopy are inconsistent, as some studies have shown a decrease in port site metastases, 44,45 yet others have been unable to confirm this.46,47 Low insufflation pressures may result in reduced tumor growth.48 Carbon dioxide may enhance tumor implantation and growth49 but is the safest gas to work with in the clinical arena. Helium may reduce the rate of wound implants but is not used clinically.50-52 Wound excision has been shown to both decrease53 and to increase54 the rate of wound recurrence.

Certain experimental findings have resulted in simple modifications of the laparoscopic approach. Aerosolization of tumor implants occurs in experimental models employing large numbers of tumor cells, 55 although others doubt its role in tumor implants.56 As it is easy to desufflate the pneumoperitoneum via the trocars rather than via the incision, some experts advocate this practice.27 Related to this is the description of gas leakage along loosely fixed trocars (the “chimney effect”) which was related to increased tumor growth in one study.57 Thus fixation of trocars or use of trocars with modifications preventing slippage is widely used. Reductions in port site metastases have been shown in animal models following irrigation of the peritoneal cavity and/or port site incisions with solutions such as povidone-iodine, heparin, methotrexate, cyclophosphamide, taurolidine and 5-fluoro-uracil.47,51,58-63 Although these models employ supra-normal numbers of cancer cells, a consensus panel of the European Association of Endoscopic Surgery reported that half the expert panel irrigated the port sites with either povidone-iodine, distilled water or tauroline and all the panel protected the extraction site and/or placed the specimen in a plastic bag prior to extraction.27

The most significant impact on the incidence of port site metastasis has been that of experience and the development of laparoscopic techniques that permit an oncologic resection, identical to the open one, to be performed. Initial reports of port sites metastases ranging from 2-21%32 have dropped to less than 1% in large case series and randomized trials.10,21,64 This is similar to the rate for open colorectal cancer resection.65 In the COST study and Lacy’s study the rates were 0.5% and 0.9% respectively.10,21 Surgical experience is considered the most important factor in the prevention of incisional implants.

In summary, experimental animal models have shown a reduction in wound implants if the wound is protected or treated with a tumoricidal substance. There is no consensus on the nature of the irrigant, but diluted povidone-iodine and distilled water were the most commonly used among experts.  In the operating room, in addition to wound protection, other commonly used techniques are fixation of trocars, evacuation of the pneumoperitoneum via the ports, and wound irrigation. Wound implants should be kept at a rate less than 1% by correct oncologic technique and experience.

IV.  TRAINING AND EXPERIENCE

Recommendation: Adequate training and experience are necessary to perform an appropriate oncologic resection. (Level II, Grade B)

Laparoscopic colorectal resections are considered amongst the most complex of laparoscopic cases. Resection requires mobilization of a bulky structure, working in more than one quadrant of the abdomen, obtaining control of multiple large blood vessels, extraction of a large specimen, and creation of a safe anastomosis. For cancer, oncologic principles must be applied with the additional requirements of adequate distal and proximal margins, appropriate lymphadenectomy, proximal ligation of the vascular pedicle(s) and avoidance of handling and perforating of the tumor.

The level of experience for these procedures is likely variable and related to the specific procedure, the underlying pathology, and the skill and prior experience of the individual surgeon.10, 66-68 Recognizing the need for experience resulted in SAGES co-endorsing the statement developed by ASCRS to accompany the publication of the results of the COST study.1 Surgeons must be prepared to answer patients’ questions regarding their experience.

REFERENCES

1. The American Society of Colon and Rectal Surgeons. Approved statement on laparoscopic colectomy. Dis Colon Rectum 1994;37:8-12.
2. The Society of American Gastrointestinal and Endoscopic Surgeons. Guidelines for Institutions Granting Privileges Utilizing Laparoscopic and/or Thoracoscopic Techniques. Revised March 2003.
3. Simmang CL, Senatore P, Lowry A, et al. Practice parameters for detection of colorectal neoplasms. Dis Colon Rectum 1999; 42:1123-9.
4. Winawer S, Fletcher R, Rex D, Bond J, Burt R, et al. Colorectal cancer screening and surveillance: clinical guidelines and rationale-Update based on new evidence. Gastroenterol 2003; 124:544-560
5. Otchy D, Hyman NH, Simmang C, et al. Practice parameters for colon cancer. Dis Colon Rectum 2004; 47:1268-84.
6. Larach SW, et al. Complications of laparoscopic colorectal surgery: analysis and comparison of early vs latter experience. Dis Colon Rectum 1997; 40:592-6.
7. Piscatelli N,Hyman N,Osler T. Localizing colorectal cancer by colonoscopy:Are we missing the boat? Arch Surg, in press.
8. Feingold DL. Addona T. Forde KA. Arnell TD. Carter JJ. Huang EH. Whelan RL. Safety and reliability of tattooing colorectal neoplasms prior to laparoscopic resection. [Journal Article] Journal of Gastrointestinal Surgery. 8(5):543-6, 2004 Jul-Aug
9. Ward J, Naik KS, Guthrie JA, Wilson D, Robinson PJ. Hepatic lesion detection: comparison of MR imaging after the administration of superparamagnetic iron oxide with dual-phase CT by using alternative-free response receiver operating characteristic analysis. Radiology 1999;210:459-66.
10. Nelson H, and The Clinical Outcomes of Surgical Therapy Study Group. A comparison of laparoscopically assisted and open colectomy for colon cancer. NEJM 2004;350:2050-9.
11. Abel ME, Rosen L, Kodner IJ, et al. Practice parameters for the treatment of rectal carcinoma. Dis Colon Rectum 1993;36:989-1006
12. Platell C, Hall J. What is the role of mechanical bowel preparation in patients undergoing colorectal surgery? Dis Colon Rectum 1998;41:875-82.
13. Brownson P, Jenkins SA, Nott D,  et al. Mechanical bowel preparation before colorectal surgery: results of a prospective, randomized trial. Br J Surg 1992;79:461-2
14. Burke P, Mealy K, Gillen P, Joyce W, Traynor O, Hyland J. Requirement for bowel preparation in colorectal surgery. Br J Surg 1994;81:580-1
15. Santos JC, Jr, Batista J, Sirimarco MT, Guimaraes AS, Levy CE. Prospective randomized trial of mechanical bowel preparation in patients undergoing elective colorectal surgery. Br J Surg 1994;81:1673-6
16. Miettinen RP, Laitinen ST, Makela JT, Paakkonen ME. Bowel preparation with oral polyethylene glycol electrolyte solution vs. no preparation in elective open colorectal surgery: prospective, randomized study. Dis Colon Rectum 2000;43:669-77
17. Zmora O, Mahajn, A, Barak B, et al. Colon and rectal surgery without mechanical bowel preparation: randomized prospective trial. Ann Surg 2003;237:363-7
18. Franklin ME Jr, Rosenthal D, Abrego-Medina D, Dorman JP, Glass JL, Norem R, Diaz A. Prospective comparison of open vs. laparoscopic colon surgery for carcinoma. Five-year results. Dis Colon Rectum1996;39:S35-46.
19. Nelson H, Petrelli N, Carlin A, et al. Guidelines 2000 for Colon and Rectal Cancer Surgery. JNCI 2001;93:583-96.
20. Lacy AM, García-Valdecasas JC, Delgado S, et al. Laparoscopy-assisted colectomy versus open colectomy for treatment of non-metastatic colon cancer: a randomized trial. Lancet 2002;359:2224-2229
21. Stocchi L, Nelson H. Laparoscopic colectomy for colon cancer: trial update. J Surg Oncol 1998;68:255-267
22. Tjandra J,Kilkenny JW, Buie D et al. Practice parameter for the management of rectal cancer. Dis Colon Rectum 48:411-423,2005.
23. Wu WX, Sun YM, Hua YB, Shen LZ Laparoscopic versus conventional open resection of rectal carcinoma: A clinical comparative study. World J Gastroenterol 2004;10:1167-70.
24. Tsang WW, Chung CC, Li MK. Prospective evaluation of laparoscopic total mesorectal excision with colonic J-pouch reconstruction for mid and low rectal cancers. Br J Surg 2003;90:867-71
25. Leroy J, Jamali F, Forbes L, Smith M, Rubino F, Mutter D, Marescaux J. Laparoscopic total mesorectal excision (TME) for rectal cancer surgery: long-term outcomes. Surg Endosc 2004;18:281-9.
26. Anthuber M, Fuerst A, Elser F, Berger R, Jauch KW. Outcome of laparoscopic surgery for rectal cancer in 101 patients. Dis Colon Rectum 2003;46:1047-53.
27. Veldkamp R, Gholghesaei M, Bonjer HJ, et al. Laparoscopic resection of colon cancer. Consensus of the European Association of Endoscopic Surgery. Surg Endosc 2004;18:1163-85.
28. Slanetz CA Jr. The effect of inadvertent perforation on survival and recurrence in colorectal Cancer. Dis Colon Rectum 1984;27:792-7.
29. Turnbull RB Jr, Kyle K, Watson FR, Spratt J. Cancer of the colon: the influence of the no-touch isolation technic on survival rates. Ann Surg 1967;166:420-7.
30. Wiggers T, Jeekel J, Arends JW, et al. No-touch isolation technique in colon cancer: a controlled prospective trial. Br J Surg 1988;75:409-15.
31. Berends FJ, Kazemier G, Bonjer HJ, Lange JF. Subcutaneous metastases after laparoscopic colectomy. Lancet 1994;344:58-58
32. Johnstone PAS, Rohde DC, Swartz SE, Fetter JE, Wexner SD. Port site recurrences after laparoscopic and thoracoscopic procedures in malignancy. J Clin Oncol 1996;14:1950-1956
33.  Cirocco WC. Schwartzman A. Golub RW. Abdominal wall recurrence after laparoscopic colectomy for colon cancer.[see comment]. [Review] [40 refs] [Case Reports. Journal Article. Review. Review of Reported Cases] Surgery. 116(5):842-6, 1994 Nov. BMC 1952-- FMC 1983—
34. Kirman I. Poltaratskaia N. Cekic V. Forde KA. Ansari P. Boulay C.Whelan RL. Depletion of circulating insulin-like growth factor binding protein 3 after open surgery is associated with high interleukin-6 levels. [Journal Article] Diseases of the Colon & Rectum. 47(6):911-7; discussion 917-8, 2004 Jun. BMC 1958
35. Lee SW. Feingold DL. Carter JJ. Zhai C. Stapleton G. Gleason N. Whelan RL. Peritoneal macrophage and blood monocyte functions after open and laparoscopic-assisted cecectomy in rats. [Journal Article] Surgical Endoscopy. 17(12):1996-2002, 2003 Dec
36. Carter JJ. Feingold DL. Kirman I. Oh A. Wildbrett P. Asi Z. Fowler R. Huang E. Whelan RL. Laparoscopic-assisted cecectomy is associated with decreased formation of postoperative pulmonary metastases compared with open cecectomy in a murine model. [Journal Article] Surgery. 134(3):432-6, 2003 Sep. BMC 1952-- FMC 1983
37. Whelan RL. Franklin M. Holubar SD. Donahue J. Fowler R. Munger C. Doorman J. Balli JE. Glass J. Gonzalez JJ. Bessler M. Xie H. Treat M. Postoperative cell mediated immune response is better preserved after laparoscopic vs open colorectal resection in humans. [Journal Article] Surgical Endoscopy. 17(6):972-8, 2003 Jun
38. Lee SW. Gleason N. Blanco I. Asi ZK. Whelan RL. Higher colon cancer tumor proliferative index and lower tumor cell death rate in mice undergoing laparotomy versus insufflation. [Journal Article] Surgical Endoscopy. 16(1):36-9, 2002 Jan
39. Carter JJ. Whelan RL. The immunologic consequences of laparoscopy in oncology. [Review] [105 refs] [Journal Article. Review] Surgical Oncology Clinics of North America. 10(3):655-77, 2001 Jul
40. Whelan RL. Lee SW. Review of investigations regarding the etiology of port site tumor recurrence. [Review] [61 refs] [Journal Article. Review] Journal of Laparoendoscopic & Advanced Surgical Techniques-Part
41. Allendorf JD. Bessler M. Horvath KD. Marvin MR. Laird DA. Whelan RL. Increased tumor establishment and growth after open vs laparoscopic surgery in mice may be related to differences in postoperative T-cell function. [Journal Article] Surgical Endoscopy. 13(3):233-5, 1999 Mar.
42. Whelan RL. Allendorf JD. Gutt CN. Jacobi CA. Mutter D. Dorrance HR. Bessler M. Bonjer HJ. General oncologic effects of the laparoscopic surgical approach. 1997 Frankfurt international meeting of animal     laparoscopic researchers. [Review] [12 refs] [Congresses. Review. Review, Tutorial] Surgical Endoscopy. 12(8):1092-5, 1998 Aug. BMC 1993
43. Southall JC. Lee SW. Allendorf JD. Bessler M. Whelan RL. Colon adenocarcinoma and B-16 melanoma grow larger following laparotomy vs. pneumoperitoneum in a murine model. [Journal Article] Diseases of the Colon & Rectum. 41(5):564-9, 1998 May. BMC 1958
44. Bouvy ND, et al.  "Impact of gas(less) laparoscopy and laparotomy on peritoneal tumor growth and abdominal wall metastases. Ann Surg 1996;224:694-700
45. Watson,DI, et al.  Gasless laparoscopy may reduce the risk of port-site metastases following laparoscopic tumor surgery. Arch Surg 1997;132:166-168
46. Gutt CN, et al.  Impact of laparoscopic colonic resection on tumour growth and spread in an experimental model. Br J Surg 1999;86:1180-1184
47. Iwanaka T, Arya G, Ziegler MM. Mechanism and prevention of port-site tumor recurrence after laparoscopy in a murine model. J Pediatr Surg 1998;33:457-461
48. Wittich P, et al. Intraperitoneal tumor growth is influenced by pressure of carbon dioxide pneumoperitoneum. Surg Endosc 2000;14:817-819
49. Jacobi CA, et al.  The impact of conventional and laparoscopic colon resection (CO2 or helium) on intraperitoneal adhesion formation in a rat peritonitis model. Surg Endosc 2001;15:380-386
50. Neuhaus SJ, et al.  Tumor implantation following laparoscopy using different insufflation gases. Surg Endosc 1998;12:1300-1302
51. Jacobi CA, et al. Influence of different gases and intraperitoneal instillation of antiadherent or cytotoxic agents on peritoneal tumor cell growth and implantation with laparoscopic surgery in a rat model. Surg Endosc 1999;13:1021-1025
52. Bouvy ND, et al. Effects of carbon dioxide pneumoperitoneum, air pneumoperitoneum, and gasless laparoscopy on body weight and tumor growth. Arch Surg 1998;133:652-656
53. Wu JS, et al. Excision of trocar sites reduces tumor implantation in an animal model. Dis Colon Rectum 1998;41:1107-1111
54. Watson DI, et al. Excision of laparoscopic port sites increases the likelihood of wound metastases in an experimental model. 8th World Congress of Endoscopic Surgery, New York, NY, USA. BS01(final program): 77, 2002
55. Wittich P, et al. Port-site metastases after CO(2) laparoscopy: is aerosolization of tumor cells a pivotal factor? Surg Endosc 2000;14:189-192
56. Whelan RL, et al. Trocar site recurrence is unlikely to result from aerosolization of tumor cells. Dis Colon Rectum 1996;39:S7-S13
57. Tseng LN, et al. Port-site metastases: impact of local tissue trauma and gas leakage. Surg Endosc 1998;12:1377-1380
58. Neuhaus SJ, et al. Influence of cytotoxic agents on intraperitoneal tumor implantation after laparoscopy. Dis Colon Rectum 1999;42:10-15
59. Lee SW, et al. Peritoneal irrigation with povidone-iodine solution after laparoscopic-assisted splenectomy significantly decreases port-tumor recurrence in a murine model. Dis Colon Rectum 1999;42:319-326
60. Neuhaus SJ, et al. Experimental study of the effect of intraperitoneal heparin on tumour implantation following laparoscopy. Br J Surg 1999;86:400-404
61. Braumann C, et al.  Influence of intraperitoneal and systemic application of taurolidine and taurolidine/heparin during laparoscopy on intraperitoneal and subcutaneous tumour growth in rats. Clin J Exp Metastasis 20018:547-552
62. Jacobi CA, et al. New therapeutic strategies to avoid intra- and extraperitoneal metastases during laparoscopy: results of a tumor model in the rat. Dig Surg 1999;16:393-399
63. Eshraghi N, et al. Topical treatments of laparoscpoic port sites can decrease the incidence of incision metastasis. Surg Endosc 1999;13:1121-1124
64. Fleshman JW, Nelson H, Peters WR, et al. Early results of laparoscopic surgery for colorectal cancer: retrospective analysis of 372 patients treated by Clinical Outcomes of Surgical Therapy (COST) Study Group. Dis Colon Rectum 1996;39:Suppl:S53-S58
65. Reilly WT, Nelson H, Schroeder G, Wieand HS, Bolton J, O'Connell MJ. Wound recurrence following conventional treatment of colorectal cancer: a rare but perhaps underestimated problem. Dis Colon Rectum 1996;39:200-207
66. Nelson H, Weeks JC, Wieand HS. Proposed phase II trial comparing laparoscopic-assisted colectomy versus open colectomy for colon cancer. In: Journal of the National Cancer Institute monographs. No. 19. Bethesda, Md.: National Cancer Institute, 1995:51-6. (NIH publication no. 94-03839.)
67. Wishner JD, Baker JW Jr, Hoffman GC, et al. Laparoscopic-assisted colectomy. The learning curve. Surg Endosc 1995;9:1179-83.
68. Lumley JW, et al. Laparoscopic-assisted colorectal surgery: lessons learned from 240 consecutive patients. Dis Colon Rectum 1996;39:155-9.

This Guideline was developed by the Society of American Gastrointestinal and Endoscopic Surgeons (SAGES) Guidelines Committee in collaboration with the American Society of Colon and Rectal Surgeons (ASCRS), and approved by the SAGES Board of Governors July 2005.

Requests for reprints should be sent to:
Society of American Gastrointestinal and
Endoscopic Surgeons
11300 West Olympic Blvd., Suite 600
Los Angeles, CA  90064
PHONE: (310) 437-0544
FAX: (310) 437‑0585
E-MAIL: sagesweb@sages.org
www.sages.org

SAGES Publication #32

APPENDIX A: Levels of Evidence

Level 1	Evidence from properly conducted randomized, controlled trials
Level II	Evidence from controlled trials without randomization Or Cohort or case-control studies Or Multiple time series, dramatic uncontrolled experiments
Level III	Descriptive case series, opinions of expert panels

APPENDIX B: Scale used for Recommendation Grading

Grade A	Based on high-level (level I or II), well-performed studies with uniform interpretation and conclusions by the expert panel
Grade B	Based on high-level, well-performed studies with varying interpretation and conclusions by the expert panel
Grade C	Based on lower level evidence (level II or less) with inconsistent findings and/or varying interpretations or conclusions by the expert panel

 

 

Return To Previous Page