Surg Endosc (2013) 27:1–10 and Other Interventional Techniques

DOI 10.1007/s00464-012-2592-x

GUIDELINES

SAGES evidence-based guidelines for the laparoscopic resection

of curable colon and rectal cancer
Marc Zerey • Lisa Martin Hawver • Ziad Awad •
Dimitrios Stefanidis • William Richardson • Robert D. Fanelli •

Members of the SAGES Guidelines Committee

Received: 3 May 2012 / Accepted: 11 June 2012 / Published online: 13 December 2012
Ó Springer Science+Business Media New York 2012

Preamble Endoscopic Surgeons (SAGES) and the American Society of

Colon and Rectal Surgeons (ASCRS) previously published a
The following recommendations regarding the safe perfor- joint statement regarding the credentialing process [1].
mance of laparoscopic resection for curable colon and rectal SAGES also has published guidelines that specifically
cancer are intended for surgeons experienced in both mini- address credentialing surgeons for laparoscopic procedures
mally invasive surgery and the surgical treatment of patients in general [2].
with colon and rectal cancer. This document does not address
the endoscopic screening or surveillance for colorectal
cancer. The Society of American Gastrointestinal and Disclaimer

Guidelines for clinical practice are intended to indicate

preferable approaches to medical problems as established
by experts in the field. These recommendations are based
M. Zerey (&)
Department of Surgery, Sansum Clinic, Santa Barbara, CA, USA on existing data or on a consensus of expert opinion when
e-mail: mzerey@sansumclinic.org little or no data are available.
Guidelines are applicable to all physicians who address
L. M. Hawver
the clinical problem(s) without regard to specialty training
Department of Surgery, University of Cincinnati College of
Medicine, Cincinnati, OH, USA or interests and are intended to indicate the preferred but
e-mail: martinhawver@gmail.com not necessarily the only acceptable approaches due to the
complexity of the health-care environment. Guidelines are
Z. Awad
intended to be flexible. Given the wide range of specifics in
Department of Surgery, University of Florida, Jacksonville, FL,
USA any health-care problem, the surgeon must always choose
e-mail: ziad.awad@jax.ufl.edu the course best suited to the individual patient and the
variables in existence at the moment of decision.
D. Stefanidis
Guidelines are developed under the auspices of the
Department of Surgery, Carolinas Medical Center, Charlotte,
NC, USA Society of American Gastrointestinal and Endoscopic
e-mail: dimitrios.stefanidis@carolinashealthcare.org Surgeons and its various committees and approved by the
Board of Governors. Each clinical practice guideline has
W. Richardson
been systematically researched, reviewed, and revised by
Department of Surgery, Ochsner Clinic Foundation,
1514 Jefferson Highway, New Orleans, LA 70121, USA the guidelines committee, and reviewed by an appropriate
e-mail: wrichardson@ochsner.org multidisciplinary team. The recommendations are therefore
considered valid at the time of their publication based on
R. D. Fanelli
the data available. Each guideline is scheduled for periodic
Department of Surgery, University of Massachusetts School of
Medicine, Pittsfield, MA, USA review to allow incorporation of pertinent new develop-
e-mail: rfanelli@berkshire.rr.com ments in medical research knowledge and practice.

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2 Surg Endosc (2013) 27:1–10

This guideline, written by SAGES, was reviewed and Table 1 GRADE system for rating the quality of evidence for
approved for endorsement by the Executive Council of the SAGES guidelines
ASCRS on 23 February 2012. Quality of Definition Symbol used
Colorectal cancer is the fourth most common malignancy evidence
in the United States and the second most common cause of
High Further research is
death from cancer in this country. In 2006, a total of 139,127 quality very unlikely to
people were diagnosed with colorectal cancer and 53,196 alter confidence
people died from it [3]. One of the most controversial issues in the estimate
in minimally invasive surgery has been the implementation of impact
of laparoscopic techniques for resection of curable colorectal Moderate Further research is
quality likely to alter
malignancies. Initial concerns included the potential viola- confidence in the
tion of oncologic principles, the effects of carbon dioxide estimate of
insufflation, and the phenomenon of port site tumor recur- impact and may
rence [4, 5]. Basic science research and large randomized change the
estimate
controlled trials are now demonstrating that these fears are
Low Further research is
unjustified. The laparoscopic approach, however, involves a quality very likely to
steep learning curve and requires the surgeon and ancillary alter confidence
operating room staff to have advanced skills in laparoscopy. in the estimate
of impact and is
likely to change
the estimate
Definitions Very low Any estimate of
quality impact is
uncertain
Both the quality of the evidence and the strength of the
recommendation for each of the recommendations below GRADE recommendations based on the quality of evidence for
were assessed according to the GRADE system [6] (see SAGES guidelines
Table 1). There is a four-tier system for judging quality of Strong It is very certain that benefit exceeds risk for the option
considered
evidence [very low (), low (), moderate (), or
Weak Risk and benefit well balanced, patients and providers
high ()] and a two-tier system for determining the faced with differing clinical situations likely would
strength of a recommendation (weak or strong). Additional make different choices, or benefits available but not
definitions are provided by SAGES in ‘‘The Definitions certain regarding the option considered
Document: A Reference for Use of SAGES Guidelines.’’ Adapted from Guyatt et al. [6]

assessment of the patient’s operative risks should be per-

Diagnostic evaluation
formed. The entire colon and rectum should be evaluated,
usually with colonoscopy. Consideration of a minimally
Standard guidelines for colorectal cancer screening should
invasive approach requires accurate localization of the
be followed [7, 8]. Published guidelines on preoperative
tumor, as a known cancer may not be visually apparent or
assessment for open resection of curable colon or rectal
palpable laparoscopically [10]. Without accurate localiza-
cancer should be followed [9]. A laparoscopic approach
tion, it is possible that an unaffected segment of colon may
requires additional considerations.
be removed [11, 12]. While colonoscopy is accurate for
localization of tumors in the rectum and cecum, it is
Tumor localization
inaccurate in other areas [13, 14]. Other methods for
identifying the segment of colon involved include tattooing
Recommendation: When approaching colon resection
at the time of colonoscopy [15–17], barium enema, and CT
laparoscopically, every effort should be made to localize
colonography [18]. A CT scan may be helpful when there
the tumor preoperatively. Small lesions should be marked
is a large tumor, but it does not reliably localize smaller
endoscopically with permanent tattoos before surgery to
tumors. Tattooing is extremely important for intraoperative
maximize the surgeon’s ability to identify the lesion. Sur-
localization, especially for small tumors or polyps, and it
geons should be prepared to use colonoscopy intraopera-
should be done at the time of preoperative colonoscopy.
tively if lesion localization is uncertain. ( , strong).
Tattooing should be accomplished using suspended carbon
Once colon or rectal cancer has been detected, preop- black, commercially prepared for this purpose. Multiple,
erative staging, assessment for resectability, and carefully placed, intramural injections should be made

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Surg Endosc (2013) 27:1–10 3

circumferentially in the colonic wall adjacent to the lesion from meta-analyses [28, 29] and randomized controlled
to maximize the surgeon’s ability to localize the lesion trials [30–33]. It should be noted that these studies evalu-
intraoperatively. Transmural injections can result in diffuse ated the use of MBP for open colorectal surgery. It is
intra-abdominal staining and may predispose to adhesion unclear if results from these trials can be extrapolated to
formation [17, 19]. If the tumor is not localized preopera- laparoscopic colorectal surgery. Furthermore, the role of
tively or the preoperative marking cannot be reliably MBP for open rectal surgery remains controversial, espe-
identified during surgery, intraoperative colonoscopy cially in low colorectal or coloanal anastomoses since most
should be used [10]. When intraoperative colonoscopy is trials exclude such patients [28]. This continually evolving
utilized, carbon dioxide insufflation may be preferable as body of literature suggests that MBP is optional for
its rapid absorption lessens the risk of a persistently dis- resections of the colon and the upper rectum, but MBP is
tended colon interfering with surgery. advised before resections of the lower rectum or when
proximal diversion is planned after rectal resection and
Diagnostic evaluation for metastases anastomosis. The literature suggests that MBP facilitates
manipulation of the bowel during laparoscopic resection
Recommendation: We recommend that for patients with and readies the colon for intraoperative colonoscopy when
colon or rectal cancer, the chest, abdomen, and pelvis be it is required for lesion localization or to assess anasto-
evaluated preoperatively with a CT scan. In patients with moses [34–36].
rectal cancer, we also recommend preoperative locore-
gional staging with endorectal ultrasound or MRI.
( , strong). Surgical technique and operative considerations
Routine cross-sectional imaging should be used preop-
Surgical technique: colon
eratively for patients with colon or rectal cancer. Metas-
tases of [1-cm diameter are detected by CT scan, with
Recommendation: We recommend that laparoscopic
sensitivities and specificities of 90 and 95 %, respectively
resection follow standard oncologic principles: proximal
[20]. In the case of rectal cancer, thoracic abdominopelvic
ligation of the primary arterial supply to the segment har-
staging evaluation should always be conducted preopera-
boring the cancer, appropriate proximal and distal margins,
tively as the finding of pulmonary, hepatic, or other
and adequate lymphadenectomy. (, strong).
metastases is likely to change the operative approach
employed and impact overall patient care [21]. In patients Guidelines established by the 2000 National Cancer
with rectal cancer, locoregional staging also is vital to Institute (NCI)-sponsored Colon and Rectal Cancer Sur-
preoperative planning; endorectal ultrasound and MRI are gery Consensus Panel state that the margins of resection for
the most commonly used procedures [22]. A discussion of colon cancer are determined by the arterial supply feeding
locoregional staging for rectal cancer is beyond the inten- the affected segment of colon [37]. Proximal ligation of
ded scope of this guideline, but readers are referred to the vessels supplying tumors, or of multiple feeding vessels
Rectal Cancer Guidelines of the American Society of when the tumor falls between arterial distributions, should
Colon and Rectal Surgeons [23]. result in adequate proximal and distal resection margins.
Lesions should be excised en bloc with oncologically
appropriate tumor-free radial margins (R0) to be consid-
Preparation for operation ered curative [38].
The five adequately powered randomized trials of lap-
Standard guidelines have been published regarding the aroscopic colectomy for curable colon cancer [37, 39–42]
safety of outpatient bowel preparation [21, 22], use of followed these oncologic principles and showed no sig-
prophylactic antibiotics [24], blood cross matching [25, nificant difference in proximal and distal margins, number
26], and venous thromboembolism prophylaxis [27]. of lymph nodes retrieved, and, in the Clinical Outcomes of
Surgical Therapy Study Group (COST) trial, perpendicular
Recommendation: We suggest that preoperative
length of the primary vascular pedicle [37]. Four of these
mechanical bowel preparation (MBP) be used to facilitate
trials showed that long-term survival and recurrence were
manipulation of the bowel during the laparoscopic
no different for patients treated with open surgery versus
approach and to facilitate intraoperative colonoscopy when
laparoscopic surgery [37, 39, 41–42]. In subgroup analysis,
needed. ( , weak).
patients enrolled in the Barcelona trial with resectable,
The use of preoperative MBP is common practice in node-positive colon cancer, AJCC stage III, who were
North America, despite a lack of clear evidence of benefit treated using a laparoscopic approach, had improved

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overall survival, cancer-related survival, and decreased margin. In order to ensure a tension-free anastomosis,
recurrence compared with an open approach, although the vascular ligation should occur either at the takeoff of the
trial was not powered to answer this question [40]. inferior mesenteric artery from the aorta or just distal to the
Extended lymphadenectomy and the ‘‘no-touch’’ tech- takeoff of the left colic artery. Despite the use of stan-
nique have not been shown to result in improved survival dardized surgical techniques and pathology-processing
in open resection [43, 44]. Extended margins of resections protocols, the number of lymph nodes resected with rectal
have not been shown to confer additional survival benefit cancers remains variable and may not serve as a useful
[45]. Some surgeons employ a medial-to-lateral approach indicator of surgical quality [53–55].
with early ligation of the mesenteric vessels [46–48]. No The confines of the pelvis confer additional challenges
oncologic benefit of this approach has been shown. when utilizing the laparoscopic approach, particularly for
Excessive force, the use of instruments not suitable for distal rectal tumors. The ability to perform an oncologi-
handling the bowel, and other techniques that predispose to cally adequate resection for rectal cancer laparoscopically
inadvertent perforation [11] should be avoided since per- will depend on tumor size and location and on anatomical
foration at the tumor site results in increased rates of local factors like a narrow pelvis, obesity, bulky uterus, and
recurrence and a significant reduction in 5-year survival the effects of presurgical radiation. Inability to adhere to
[49]. Atraumatic handling of the bowel should be the goal oncologic principles should prompt conversion to an open
of every surgeon and can be achieved by blunt retraction, operation provided that conversion will enhance adherence
grasping of the epiploic appendages, and the use of to established principles. Selection of the anastomotic
atraumatic graspers. method or creation of a temporary or permanent ostomy
Inability to adhere to all accepted oncologic principles, should be made in a manner that is identical to making
including appropriate vascular ligation, should prompt these decisions in patients undergoing laparotomy.
conversion to an open operation if conversion will permit Several prospective [54–56] and retrospective [57, 58]
adherence to established principles. Careful patient selec- case series have demonstrated that laparoscopic total
tion, complete preoperative staging, accurate tumor local- mesorectal excision can be performed safely and ade-
ization, and an experienced surgeon working with an quately. The mid- and long-term oncological outcomes of
experienced operating room staff all contribute to maxi- open and laparoscopic approaches appear to be similar. To
mizing patient benefit and minimizing conversion to open date, only one randomized trial included long-term results
resection [50]. of laparoscopic and open surgical treatments of rectal
The decision to administer adjuvant therapy is inde- cancer. The UK MRC-CLASSIC Trial Group found no
pendent of the technique used for colon resection and difference in overall survival, disease-free survival, local
should mirror recommendations for open resection recurrence, wound recurrence, or quality of life between
[51, 52]. the two approaches [59, 60]. Thirty-four percent of the
patients randomized to the laparoscopic group underwent
conversion to an open procedure and this cohort had
Surgical technique: rectum
a higher incidence of postoperative complications (p =
0.002) and worsened overall survival but equivalent dis-
Recommendation: We recommend that laparoscopic
ease-free survival at 5 years [60]. Furthermore, in patients
resection for rectal cancer follow standard oncologic
who underwent laparoscopic low anterior resection, there
principles: Adequate distal margin, ligation at the origin of
was a higher rate of positive circumferential margins,
the arterial supply for the involved rectal segment, and
although this did not impact local recurrence or survival
mesorectal excision. ( , strong).
[59]. Overall, male sexual and erectile function was worse
Resection of very low rectal cancers, intersphincteric in the laparoscopic group [61].
resection, and other sphincter-sparing techniques are The COREAN trial randomized 340 patients with
beyond the intended scope of this guideline, but readers are T3N0-2 mid or low rectal cancers, \9 cm from the anal
referred to the Rectal Cancer Guidelines of the ASCRSs verge, to undergo laparoscopic or open surgery following
[23]. neoadjuvant chemoradiation treatment [62]. The primary
Operative guidelines for open rectal surgery have been end point was 3-year disease-free survival. Patients were
established, with levels of evidence and grades of recom- treated by seven surgeons experienced in laparoscopic
mendation for techniques relevant only to the rectum [38, colorectal surgery at three institutions. Their short-term
53]. Malignant lesions of the upper rectum should be outcomes demonstrated less blood loss in the laparoscopic
resected with 5-cm minimum distal margins, while lesions group (200 vs. 217.5 ml, p = 0.006), albeit with a longer
of the middle and lower rectum require total mesorectal operating time (244.9 vs. 197 min, p \ 0.0001). Involve-
resection, including an oncologically appropriate distal ment of the circumferential margin, macroscopic quality of

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the total mesorectal excision specimen, number of har- initial laparoscopy, the goals of surgery may shift from
vested lymph nodes, and perioperative morbidity did not curative to palliative. To date, there have been no ran-
differ between the groups. Conversion rate to open resec- domized trials comparing laparoscopic and open approa-
tion was only 1.2 %. Three months following the proc- ches to T4 colonic or rectal cancer.
tectomy, or ileostomy reversal if one was used, the
laparoscopic group had better quality-of-life scores when Obstructing colon cancer
physical function, fatigue, micturition, and gastrointestinal
function were assessed. The COLOR II, Japanese JCOG Recommendation: We recommend that patients with an
0404, and ACOSOG Z6051 trials are other randomized obstructing right or transverse colon cancer undergo a right
controlled trials currently underway that seek to compare or an extended right colectomy. The open approach is
laparoscopic and open surgery for rectal cancer, assessing required if the laparoscopic approach will not result in an
morbidity and long-term oncological outcome [62–65]. oncologically sound resection. ( , strong).
The decision to offer adjuvant or neoadjuvant chemo-
Patients with an obstructing right or transverse colon
radiation should be based on tumor- and patient-specific
cancer should undergo a right or an extended right colec-
factors and not on the surgical approach. The optimal
tomy with primary ileocolic anastomosis in the appropriate
timing of surgery for rectal cancer following neoadjuvant
clinical setting. Performing an anastomosis and/or the
therapy has been examined in several trials, and although it
creation of a diverting stoma is dependent on the patient’s
is still debated, it should not be altered based on the
general condition. Multiple nonrandomized studies have
technique chosen for resection [66–68]. A complete dis-
demonstrated that a primary anastomosis is safe in the
cussion of adjunctive treatment is beyond the intended
absence of MBP [73, 74]. The decision to proceed lapa-
scope of this guideline, but readers are referred to the
roscopically should take into account the patient’s condi-
Rectal Cancer Guidelines of the ASCRSs [23].
tion, including hemodynamic stability, extent of abdominal
distension, the resectability of the carcinoma, and the sur-
Locally advanced adherent colon and rectal tumors
geon’s ability to perform a curative resection in this setting.
Although there have been some retrospective studies
Recommendation: For locally advanced adherent colon
demonstrating feasibility of laparoscopic resection with
and rectal tumors, an en bloc resection is recommended.
benefits in short-term outcomes [75, 76], a prospective
We suggest an open approach if a laparoscopic en bloc
randomized controlled trial has not yet been published.
resection cannot be performed adequately. ( ,
weak). Recommendation: We suggest that for patients with an
obstructing left-sided colon cancer, the procedure be indi-
Up to 15 % of patients with colon cancer and 5–12 % of
vidualized according to clinical factors. Colonic stenting
patients with rectal cancer will have tumors adherent to
may increase the likelihood of completing a one-stage
adjacent organs [69–71]. Current guidelines for open colon
procedure and may decrease the likelihood of an end
and rectal cancer surgery recommend en bloc resection
colostomy. ( , weak).
to manage locally advanced adherent colorectal tumors
[9, 38]. Histologically negative margins achieved with en For patients who present with an obstructing cancer of
bloc resection are considered curative. Preoperative cross- the left colon, a variety of options have been advocated [77,
sectional imaging, including CT scan, MRI, or ultrasound, 78]. The most frequently used are resection with end
might suggest a bulky tumor invading into adjacent struc- colostomy and Hartmann’s pouch, resection with on-table
tures, guiding the decision to perform an open resection lavage and primary anastomosis with or without diverting
[72]. The ability to perform en bloc resection laparoscop- ostomy, and subtotal colectomy with ileorectal anastomo-
ically is dependent on the structure to which the tumor is sis. More recently, colonic stenting in appropriately
adherent and the surgeon’s skill and experience. When the selected patients may obviate obstruction, permitting
goal is curative resection, intraoperative discovery of a T4 colonic decompression and elective resection with primary
lesion often requires conversion, unless the surgeon is able anastomosis, decreasing the rate of colostomy creation in
to effectively resect the lesion en bloc. However, en bloc this setting. One randomized controlled trial compared
resection might not be possible using either technique, and endoluminal stenting followed by laparoscopic resection to
therefore the surgeon must decide if conversion is likely to immediate open surgical resection of obstructing left-sided
afford curative resection. Occasionally, laparoscopy may colon cancers [79]. The authors found that more patients in
become diagnostic, with closure followed by reimaging the stenting and laparoscopic resection group underwent
and multidisciplinary consultation prior to a definitive one-stage operations (66 vs. 37.5 %; p = 0.04) and that no
resection at a later date. In some situations, based on the patients in this group required colostomy, compared with

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25 % of patients in the open surgery group who received spaces, and fixed instrument tips. Moreover, the robotic
end colostomy. system provides excellent ergonomics, tremor stabilization,
enhanced ambidextrous capability, motion scaling, and
instruments capable of moving with multiple degrees of
Prevention of wound complications freedom. Robotic surgery has the drawbacks of diminished
haptic feedback, increased operative times, and increased
Recommendation: The use of a wound protector at the procedural cost. Large-scale prospective randomized trials
extraction site and the irrigation of port sites and extraction will be required to evaluate long-term clinical outcomes of
site incisions may reduce abdominal wall cancer recur- robotic surgery and to identify actual clinical benefit.
rences. ( , strong).
Wound implants, or abdominal wall cancer recurrences, Training and experience
have been reported at both extraction site and port site
incisions [4, 37, 39, 59, 80], prompting extensive research Recommendation: Before surgeons apply the laparo-
[81–90] and initially calling the oncologic safety of the scopic approach for the resection of curable colon and
laparoscopic approach into question [91]. rectal cancer, they must have adequate knowledge, train-
It is now accepted that port-site recurrence is a technical ing, and experience in laparoscopic techniques and onco-
complication of laparoscopic colectomy and not an inevi- logic principles. ( , strong).
table consequence of the laparoscopic approach. Several
Some reviewed studies mandated a minimum of 20 lapa-
large case series and randomized trials comparing laparo-
roscopic colon cancer operations for surgeon inclusion into
scopic versus open colectomy for colon carcinoma have
clinical trials [37, 38], whereas studies examining the learning
confirmed port-site recurrences well below 1 % [37, 39, 59,
curve for laparoscopic colectomy have suggested that at least
92–94]. This is similar to the rate of incisional recurrence
50 cases are required to gain proficiency [116–118].
noted after open colorectal cancer resection [39, 94, 95].
Advanced laparoscopic training during residency or fellow-
In a consensus report from the European Association of
ship and training on simulators may shorten the learning curve
Endoscopic Surgeons, Veldkamp et al. [72] collected all
toward proficiency. Surgeons must carefully observe the
reported cases of port-site recurrences from a total of 28
principles applicable to resection of colon and rectal cancers to
different studies from Europe, Asia, Australia, and North
have long-term outcomes similar to those of open resections.
America. There were 38 overall port-site recurrences on a
Mentoring, proctoring, and working with an experienced
denominator of 5,225 combined patients, corresponding to
assistant have each been shown to be effective in the adoption
an overall incidence of 0.72 %.
of techniques new to a surgeon’s skill set [119].
Most surgeons performing laparoscopic colectomy use
wound protectors to isolate specimens from contact with the
abdominal wall [72]. Irrigation of the port site with a variety Summary of recommendations
of tumoricidal solutions reduces tumor implants in animal
models, but there is no consensus on the ideal irrigant or Tumor localization
whether this laboratory observation holds value in the per-
formance of colon cancer resections in humans [96–101]. Recommendation: When approaching colon resection
laparoscopically, every effort should be made to localize
the tumor preoperatively. Small lesions should be marked
Robotic surgery endoscopically with permanent tattoos before surgery to
maximize the surgeon’s ability to identify the lesion. Sur-
Recommendation: While robotic surgery for colon and geons should be prepared to use colonoscopy intraopera-
rectal cancer appears feasible and safe, in the absence of tively if lesion localization is uncertain. ( , strong).
long-term oncologic outcome studies, no clear recom-
mendation can be made. ( , weak). Diagnostic evaluation for metastases
Case reports suggest that the use of robotics is feasible
and safe in selected patients with colon and rectal cancer Recommendation: We recommend that for patients with
[102–115]. Robotic devices were developed to overcome colon or rectal cancer, the chest, abdomen, and pelvis be
the disadvantages of conventional laparoscopic surgery, evaluated preoperatively with CT scan. In patients with
such as an assistant-dependent unstable camera platform, rectal cancer, we also recommend preoperative locore-
two-dimensional view, limited dexterity associated with gional staging with endorectal ultrasound or MRI.
the use of traditional laparoscopic instruments in confined ( , strong).

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Surg Endosc (2013) 27:1–10 7

Preparation for operation Robotic surgery

Recommendation: We suggest that preoperative MBP be Recommendation: While robotic surgery for colon and
used to facilitate manipulation of the bowel during the rectal cancer appears feasible and safe, in the absence of
laparoscopic approach and to facilitate intraoperative long-term oncologic outcome studies, no clear recom-
colonoscopy when needed. ( , weak). mendation can be made. ( , weak).

Surgical technique: colon Training and experience

Recommendation: We recommend that laparoscopic Recommendation: Before surgeons apply the laparo-
resection follow standard oncologic principles: proximal scopic approach for resection of curable colon and rectal
ligation of the primary arterial supply to the segment har- cancer, they must have adequate knowledge, training, and
boring the cancer, appropriate proximal and distal margins, experience in laparoscopic techniques and oncologic prin-
and adequate lymphadenectomy. (, strong). ciples. ( , strong).

Surgical technique: rectum Disclosures No disclosures.

Recommendation: We recommend that laparoscopic

resection for rectal cancer follow standard oncologic References
principles: adequate distal margin, ligation at the origin of
the arterial supply for the involved rectal segment, and 1. The American Society of Colon and Rectal Surgeons (1994)
Approved statement on laparoscopic colectomy. Dis Colon
mesorectal excision. ( , strong).
Rectum 37:8–12
2. The Society of American Gastrointestinal and Endoscopic Sur-
Contiguous organ attachment geons (2010) Guidelines for institutions granting privileges
utilizing laparoscopic and/or thoracosopic techniques (revised).
http://www.sages.org/publication/id/14/
Recommendation: For locally advanced adherent colon
3. Centers for Disease Control and Prevention (2006) National
and rectal tumors, an en bloc resection is recommended. We Program of Cancer Registries, United States Cancer Statistics.
suggest an open approach if a laparoscopic en bloc resection http://apps.nccd.cdc.gov/uscs/
cannot be performed adequately. ( , weak). 4. Berends FJ et al (1994) Subcutaneous metastases after laparo-
scopic colectomy. Lancet 344(8914):58
5. Tseng LN et al (1998) Port-site metastases. Impact of local
Obstructing colon cancer (right-sided) tissue trauma and gas leakage. Surg Endosc 12(12):1377–1380
6. Guyatt GH et al (2008) GRADE: an emerging consensus on
Recommendation: We recommend that patients with an rating quality of evidence and strength of recommendations.
BMJ 336(7650):924–926
obstructing right or transverse colon cancer undergo a right
7. Simmang CL et al (1999) Practice parameters for detection of
or an extended right colectomy. The open approach is colorectal neoplasms. The Standards Committee, The American
required if the laparoscopic approach will not result in an Society of Colon and Rectal Surgeons. Dis Colon Rectum
oncologically sound resection. ( , strong). 42(9):1123–1129
8. Winawer S et al (2003) Colorectal cancer screening and sur-
veillance: clinical guidelines and rationale—update based on
Obstructing colon cancer (left-sided) new evidence. Gastroenterology 124(2):544–560
9. Otchy D et al (2004) Practice parameters for colon cancer. Dis
Recommendation: We suggest that for patients with an Colon Rectum 47(8):1269–1284
10. Cho YB et al (2007) Tumor localization for laparoscopic colo-
obstructing left-sided colon cancer, the procedure be indi-
rectal surgery. World J Surg 31(7):1491–1495
vidualized according to clinical factors. Colonic stenting 11. Larach SW et al (1997) Complications of laparoscopic colo-
may increase the likelihood of completing a one-stage rectal surgery. Analysis and comparison of early vs. latter
procedure and may decrease the likelihood of an end experience. Dis Colon Rectum 40(5):592–596
12. Wexner SD et al (1995) Laparoscopic colorectal surgery—are
colostomy. ( , weak).
we being honest with our patients? Dis Colon Rectum
38(7):723–727
Prevention of wound complications 13. Piscatelli N, Hyman N, Osler T (2005) Localizing colorectal
cancer by colonoscopy. Arch Surg 140(10):932–935
14. Vaziri K, Choxi SC, Orkin BA (2010) Accuracy of colonoscopic
Recommendation: The use of a wound protector at the
localization. Surg Endosc 24(10):2502–2505
extraction site and irrigation of port sites and extraction site 15. Feingold DL et al (2004) Safety and reliability of tattooing
incisions may reduce abdominal wall cancer recurrences. colorectal neoplasms prior to laparoscopic resection. J Gastro-
( , strong). intest Surg 8(5):543–546

123
8 Surg Endosc (2013) 27:1–10

16. Arteaga-Gonzalez I et al (2006) The use of preoperative endo- 36. Ishihara S, Watanabe T, Nagawa H (2008) Intraoperative
scopic tattooing in laparoscopic colorectal cancer surgery for colonoscopy for stapled anastomosis in colorectal surgery. Surg
endoscopically advanced tumors: a prospective comparative Today 38(11):1063–1065
clinical study. World J Surg 30(4):605–611 37. Clinical Outcomes of Surgical Therapy Study Group (2004) A
17. Park JW et al (2008) The usefulness of preoperative colono- comparison of laparoscopically assisted and open colectomy for
scopic tattooing using a saline test injection method with pre- colon cancer. N Engl J Med 350(20):2050–2059
packaged sterile India ink for localization in laparoscopic 38. Nelson H et al (2001) Guidelines 2000 for colon and rectal
colorectal surgery. Surg Endosc 22(2):501–505 cancer surgery. J Natl Cancer Inst 93(8):583–596
18. Johnson CD et al (2008) Accuracy of CT colonography for 39. Lacy AM et al (2002) Laparoscopy-assisted colectomy versus
detection of large adenomas and cancers. N Engl J Med open colectomy for treatment of non-metastatic colon cancer: a
359(12):1207–1217 randomised trial. Lancet 359(9325):2224–2229
19. Yeung JM, Maxwell-Armstrong C, Acheson AG (2009) Colonic 40. Hewett PJ et al (2008) Short-term outcomes of the Australasian
tattooing in laparoscopic surgery—making the mark? Colorectal randomized clinical study comparing laparoscopic and conven-
Dis 11(5):527–530 tional open surgical treatments for colon cancer: the ALCCaS
20. Ward J et al (1999) Hepatic lesion detection: comparison of MR trial. Ann Surg 248(5):728–738
imaging after the administration of superparamagnetic iron 41. Guillou PJ et al (2005) Short-term endpoints of conventional
oxide with dual-phase CT by using alternative-free response versus laparoscopic-assisted surgery in patients with colorectal
receiver operating characteristic analysis. Radiology 210(2): cancer (MRC CLASICC trial): multicentre, randomised con-
459–466 trolled trial. Lancet 365(9472):1718–1726
21. Frazee RC et al (1992) Prospective, randomized trial of inpatient 42. Veldkamp R et al (2005) Laparoscopic surgery versus open
vs. outpatient bowel preparation for elective colorectal surgery. surgery for colon cancer: short-term outcomes of a randomised
Dis Colon Rectum 35(3):223–226 trial. Lancet Oncol 6(7):477–484
22. Lee EC et al (1996) Inpatient vs. outpatient bowel preparation 43. Kawamura YJ et al (2000) Effect of high ligation on the long-
for elective colorectal surgery. Dis Colon Rectum 39(4): term result of patients with operable colon cancer, particularly
369–373 those with limited nodal involvement. Eur J Surg
23. Monson JR et al (2012) Practice parameters for the management 166(10):803–807
of rectal cancer. Dis Colon Rectum (in press) 44. Wiggers T et al (1988) No-touch isolation technique in colon
24. Baum ML et al (1981) A survey of clinical trials of antibiotic cancer: a controlled prospective trial. Br J Surg 75(5):409–415
prophylaxis in colon surgery: evidence against further use of 45. Rouffet F et al (1994) Curative resection for left colonic carci-
no-treatment controls. N Engl J Med 305(14):795–799 noma: hemicolectomy vs. segmental colectomy. A prospective,
25. Chung M, Steinmetz OK, Gordon PH (1993) Perioperative controlled, multicenter trial. French Association for Surgical
blood transfusion and outcome after resection for colorectal Research. Dis Colon Rectum 37(7):651–659
carcinoma. Br J Surg 80(4):427–432 46. Poon JT et al (2009) Impact of the standardized medial-to-lateral
26. Busch OR et al (1993) Blood transfusions and prognosis in approach on outcome of laparoscopic colorectal resection.
colorectal cancer. N Engl J Med 328(19):1372–1376 World J Surg 33(10):2177–2182
27. Stahl TJ et al (2006) Practice parameters for the prevention of 47. Liang JT et al (2003) Comparison of medial-to-lateral versus
venous thrombosis. Dis Colon Rectum 49(10):1477–1483 traditional lateral-to-medial laparoscopic dissection sequences
28. Slim K et al (2009) Updated systematic review and meta- for resection of rectosigmoid cancers: randomized controlled
analysis of randomized clinical trials on the role of mechanical clinical trial. World J Surg 27(2):190–196
bowel preparation before colorectal surgery. Ann Surg 249(2): 48. Senagore AJ et al (2003) Results of a standardized technique
203–209 and postoperative care plan for laparoscopic sigmoid colectomy:
29. Zhu QD et al (2010) Efficacy of mechanical bowel preparation a 30-month experience. Dis Colon Rectum 46(4):503–509
with polyethylene glycol in prevention of postoperative com- 49. Slanetz CA Jr (1984) The effect of inadvertent intraoperative
plications in elective colorectal surgery: a meta-analysis. Int J perforation on survival and recurrence in colorectal cancer. Dis
Colorectal Dis 25(2):267–275 Colon Rectum 27(12):792–797
30. Brownson P, Jenkins SA, Nott D et al (1992) Mechanical bowel 50. Kwok SP et al (1996) Prospective evaluation of laparoscopic-
preparation before colorectal surgery: results of a prospective, assisted large bowel excision for cancer. Ann Surg
randomized trial. Br J Surg 79:461–462 223(2):170–176
31. Contant CM et al (2007) Mechanical bowel preparation for 51. Chang GJ et al (2012) Practice parameters for the management
elective colorectal surgery: a multicentre randomised trial. of colon cancer. Dis Colon Rectum 55(8):831–843
Lancet 370(9605):2112–2117 52. Beck DE et al (2011) The ASCRS textbook of colon and rectal
32. Fa-Si-Oen P et al (2005) Mechanical bowel preparation or not? surgery, 2nd edn. Springer, New York
Outcome of a multicenter, randomized trial in elective open 53. Tjandra JJ et al (2005) Practice parameters for the management
colon surgery. Dis Colon Rectum 48(8):1509–1516 of rectal cancer (revised). Dis Colon Rectum 48(3):411–423
33. Miettinen RP et al (2000) Bowel preparation with oral poly- 54. Morino M et al (2003) Laparoscopic total mesorectal excision: a
ethylene glycol electrolyte solution vs. no preparation in elective consecutive series of 100 patients. Ann Surg 237(3):335–342
open colorectal surgery: prospective, randomized study. Dis 55. Cheung HY et al (2009) Laparoscopic rectal cancer surgery with
Colon Rectum 43(5):669–675; discussion 675–677 and without neoadjuvant chemo-irradiation: a comparative
34. Lanthaler M et al (2008) Intraoperative colonoscopy for anas- study. Surg Endosc 23(1):147–152
tomosis assessment in laparoscopically assisted left-sided colon 56. Hasegawa H et al (2007) Short- and midterm outcomes of lap-
resection: is it worthwhile? J Laparoendosc Adv Surg Tech A aroscopic surgery compared for 131 patients with rectal and
18(1):27–31 rectosigmoid cancer. Surg Endosc 21(6):920–924
35. Li VK et al (2009) Use of routine intraoperative endoscopy in 57. Miyajima N et al (2009) Results of a multicenter study of 1,057
elective laparoscopic colorectal surgery: can it further avoid cases of rectal cancer treated by laparoscopic surgery. Surg
anastomotic failure? Surg Endosc 23(11):2459–2465 Endosc 23(1):113–118

123
Surg Endosc (2013) 27:1–10 9

58. Ng KH et al (2009) Laparoscopic resection for rectal cancers: SCOTIA Study Group. Subtotal Colectomy versus On-table
lessons learned from 579 cases. Ann Surg 249(1):82–86 Irrigation and Anastomosis. Br J Surg 82(12):1622–1627
59. Jayne DG et al (2007) Randomized trial of laparoscopic-assisted 79. Cheung HY et al (2009) Endolaparoscopic approach vs con-
resection of colorectal carcinoma: 3-year results of the UK MRC ventional open surgery in the treatment of obstructing left-sided
CLASICC Trial Group. J Clin Oncol 25(21):3061–3068 colon cancer: a randomized controlled trial. Arch Surg 144(12):
60. Jayne DG et al (2010) Five-year follow-up of the Medical 1127–1132
Research Council CLASSIC trial of laparoscopically assisted 80. Johnstone PA et al (1996) Port site recurrences after laparo-
versus open surgery for colorectal cancer. Br J Surg 97(11): scopic and thoracoscopic procedures in malignancy. J Clin
1638–1645 Oncol 14(6):1950–1956
61. Jayne DG et al (2005) Bladder and sexual function following 81. Kirman I et al (2004) Depletion of circulating insulin-like
resection for rectal cancer in a randomized clinical trial of growth factor binding protein 3 after open surgery is associated
laparoscopic versus open technique. Br J Surg 92(9):1124–1132 with high interleukin-6 levels. Dis Colon Rectum 47(6):11–17;
62. Kang SB et al (2010) Open versus laparoscopic surgery for mid discussion 917–918
or low rectal cancer after neoadjuvant chemoradiotherapy 82. Lee SW et al (2003) Peritoneal macrophage and blood monocyte
(COREAN trial): short-term outcomes of an open-label ran- functions after open and laparoscopic-assisted cecectomy in rats.
domised controlled trial. Lancet Oncol 11(7):637–645 Surg Endosc 17(12):1996–2002
63. Buunen M et al (2009) COLOR II. A randomized clinical trial 83. Carter JJ et al (2003) Laparoscopic-assisted cecectomy is
comparing laparoscopic and open surgery for rectal cancer. Dan associated with decreased formation of postoperative pulmonary
Med Bull 56(2):89–91 metastases compared with open cecectomy in a murine model.
64. Kitano S et al (2005) Randomized controlled trial to evaluate Surgery 134(3):432–436
laparoscopic surgery for colorectal cancer: Japan Clinical 84. Whelan RL et al (2003) Postoperative cell mediated immune
Oncology Group Study JCOG 0404. Jpn J Clin Oncol 35(8): response is better preserved after laparoscopic vs open colo-
475–477 rectal resection in humans. Surg Endosc 17(6):972–978
65. Nandakumar G, Fleshman JW (2010) Laparoscopy for rectal 85. Lee SW et al (2002) Higher colon cancer tumor proliferative
cancer. Surg Oncol Clin N Am 19(4):793–802 index and lower tumor cell death rate in mice undergoing lap-
66. Lim SB et al (2008) Optimal surgery time after preoperative arotomy versus insufflation. Surg Endosc 16(1):36–39
chemoradiotherapy for locally advanced rectal cancers. Ann 86. Carter JJ et al (2006) Perioperative immunomodulation with
Surg 248(2):243–251 Flt3 kinase ligand or a whole tumor cell vaccine is associated
67. Francois Y et al (1999) Influence of the interval between pre- with a reduction in lung metastasis formation after laparotomy
operative radiation therapy and surgery on downstaging and on in mice. Surg Innov 13(1):41–47
the rate of sphincter-sparing surgery for rectal cancer: the Lyon 87. Carter JJ et al (2005) Significant reduction of laparotomy-
R90–01 randomized trial. J Clin Oncol 17(8):2396 associated lung metastases and subcutaneous tumors after peri-
68. Horn A, Morild I, Dahl O (1990) Tumour shrinkage and down operative immunomodulation with flt3 ligand in mice. Surg
staging after preoperative radiation of rectal adenocarcinomas. Innov 12(4):319–325
Radiother Oncol 18(1):19–28 88. Kirman I et al (2002) Combined whole tumor cell and mono-
69. Sugarbaker PH, Corlew S (1982) Influence of surgical tech- phosphoryl lipid A vaccine improved by encapsulation in mur-
niques on survival in patients with colorectal cancer. Dis Colon ine colorectal cancer. Surg Endosc 16(4):654–658
Rectum 25(6):545–557 89. Carter JJ, Whelan RL (2001) The immunologic consequences of
70. Bonfanti G et al (1982) Results of extended surgery for cancer laparoscopy in oncology. Surg Oncol Clin N Am 10(3):655–677
of the rectum and sigmoid. Br J Surg 69(6):305–307 90. Allendorf JD et al (1999) Increased tumor establishment and
71. Curley SA et al (1992) Extended resection for locally advanced growth after open vs laparoscopic surgery in mice may be
colorectal carcinoma. Am J Surg 163(6):553–559 related to differences in postoperative T-cell function. Surg
72. Veldkamp R et al (2004) Laparoscopic resection of colon can- Endosc 13(3):233–235
cer: consensus of the European Association of Endoscopic 91. Wittich P et al (2000) Port-site metastases after CO(2) lapa-
Surgery (EAES). Surg Endosc 18(8):1163–1185 roscopy. Is aerosolization of tumor cells a pivotal factor? Surg
73. Smithers BM et al (1986) Emergency right hemicolectomy in Endosc 14(2):189–192
colon carcinoma: a prospective study. Aust N Z J Surg 92. Stocchi L, Nelson H (1998) Laparoscopic colectomy for colon
56(10):749–752 cancer: trial update. J Surg Oncol 68(4):255–267
74. Runkel NS et al (1998) Improved outcome after emergency 93. Fleshman J et al (2007) Laparoscopic colectomy for cancer is
surgery for cancer of the large intestine. Br J Surg 85(9): not inferior to open surgery based on 5-year data from the COST
1260–1265 Study Group trial. Ann Surg 246(4):655–662; discussion
75. Ng SS et al (2008) Emergency laparoscopic-assisted versus open 662–664
right hemicolectomy for obstructing right-sided colonic carci- 94. Lacy AM et al (2008) The long-term results of a randomized
noma: a comparative study of short-term clinical outcomes. clinical trial of laparoscopy-assisted versus open surgery for
World J Surg 32(3):454–458 colon cancer. Ann Surg 248(1):1–7
76. Ng SS et al (2006) Emergency laparoscopically assisted right 95. Reilly WT et al (1996) Wound recurrence following conven-
hemicolectomy for obstructing right-sided colon carcinoma. tional treatment of colorectal cancer. A rare but perhaps
J Laparoendosc Adv Surg Tech A 16(4):350–354 underestimated problem. Dis Colon Rectum 39(2):200–207
77. Lopez-Kostner F, Hool GR, Lavery IC (1997) Management and 96. Braumann C et al (2000) Influence of intraperitoneal and sys-
causes of acute large-bowel obstruction. Surg Clin North Am temic application of taurolidine and taurolidine/heparin during
77(6):1265–1290 laparoscopy on intraperitoneal and subcutaneous tumour growth
78. The SCOTIA Study Group (1995) Single-stage treatment for in rats. Clin Exp Metastasis 18(7):547–552
malignant left-sided colonic obstruction: a prospective ran- 97. Iwanaka T, Arya G, Ziegler MM (1998) Mechanism and pre-
domized clinical trial comparing subtotal colectomy with seg- vention of port-site tumor recurrence after laparoscopy in a
mental resection following intraoperative irrigation. The murine model. J Pediatr Surg 33(3):457–461

123
10 Surg Endosc (2013) 27:1–10

98. Jacobi CA et al (1999) Influence of different gases and intra- 109. Patriti A et al (2009) Laparoscopic and robot-assisted one-stage
peritoneal instillation of antiadherent or cytotoxic agents on resection of colorectal cancer with synchronous liver metastases:
peritoneal tumor cell growth and implantation with laparoscopic a pilot study. J Hepatobiliary Pancreat Surg 16(4):450–457
surgery in a rat model. Surg Endosc 13(10):1021–1025 110. Luca F et al (2009) Full robotic left colon and rectal cancer
99. Neuhaus SJ et al (1999) Influence of cytotoxic agents on intra- resection: technique and early outcome. Ann Surg Oncol
peritoneal tumor implantation after laparoscopy. Dis Colon 16(5):1274–1278
Rectum 42(1):10–15 111. Spinoglio G et al (2008) Robotic colorectal surgery: first 50
100. Neuhaus SJ et al (1999) Experimental study of the effect of cases experience. Dis Colon Rectum 51(11):1627–1632
intraperitoneal heparin on tumour implantation following lapa- 112. Rawlings AL et al (2007) Robotic versus laparoscopic colec-
roscopy. Br J Surg 86(3):400–404 tomy. Surg Endosc 21(10):1701–1708
101. Lee SW et al (1999) Peritoneal irrigation with povidone-iodine 113. Rawlings AL, Woodland JH, Crawford DL (2006) Telerobotic
solution after laparoscopic-assisted splenectomy significantly surgery for right and sigmoid colectomies: 30 consecutive cases.
decreases port-tumor recurrence in a murine model. Dis Colon Surg Endosc 20(11):1713–1718
Rectum 42(3):319–326 114. Kang J et al (2012) Robotic coloanal anastomosis with or
102. Pigazzi A et al (2010) Multicentric study on robotic tumor- without intersphincteric resection for low rectal cancer: starting
specific mesorectal excision for the treatment of rectal cancer. with the perianal approach followed by robotic procedure. Ann
Ann Surg Oncol 17(6):1614–1620 Surg Oncol 19(1):154–155
103. Koh, Tsang CB, Kim SH (2011) A new application of the four- 115. Luca F et al (2011) Surgical and pathological outcomes after
arm standard da Vinci(R) surgical system: totally robotic- right hemicolectomy: case-matched study comparing robotic
assisted left-sided colon or rectal resection. Surg Endosc and open surgery. Int J Med Robot. doi:10.1002/rcs.398
25(6):1945–1952 116. Park IJ et al (2009) Multidimensional analysis of the learning
104. DeNoto G, Rubach, Ravikumar TS (2006) A standardized curve for laparoscopic colorectal surgery: lessons from 1,000
technique for robotically performed sigmoid colectomy. J cases of laparoscopic colorectal surgery. Surg Endosc 23(4):
Laparoendosc Adv Surg Tech A 16(6):551–556 839–846
105. D’Annibale A et al (2010) Robotic right colon resection: eval- 117. Li JC et al (2009) The learning curve for laparoscopic colec-
uation of first 50 consecutive cases for malignant disease. Ann tomy: experience of a surgical fellow in an university colorectal
Surg Oncol 17(11):2856–2862 unit. Surg Endosc 23(7):1603–1608
106. deSouza AL et al (2010) Robotic assistance in right hemicol- 118. Akiyoshi T et al (2011) Learning curve for standardized lapa-
ectomy: is there a role? Dis Colon Rectum 53(7):1000–1006 roscopic surgery for colorectal cancer under supervision: a
107. Zimmern A et al (2010) Robotic colon and rectal surgery: a single-center experience. Surg Endosc 25(5):1409–1414
series of 131 cases. World J Surg 34(8):1954–1958 119. Miskovic D et al (2010) Systematic review on mentoring and
108. Ceccarelli G et al (2010) Laparoscopic resection with intracor- simulation in laparoscopic colorectal surgery. Ann Surg 252(6):
poreal anastomosis for colon carcinoma located in the splenic 943–951
flexure. Surg Endosc 24(7):1784–1788

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