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Surgical Oncology (2008) xx, 1e9

available at www.sciencedirect.com

journal homepage: www.elsevier.com/locate/suronc

REVIEW

Localized resection for colon cancer


R.A. Cahill*, J. Leroy, J. Marescaux

Department of Surgery, IRCAD/EITS, 1 Place de lHopital, Strasbourg 67091, France

Accepted 20 August 2008

KEYWORDS Abstract
Localized resection; Localized resection of early stage colon cancer is increasingly technically feasible by truly
Endoscopic resection; minimally invasive means. Such techniques as endoscopic submucosal dissection (ESD) and
Early stage colon Natural Orifice Transluminal Endoscopic Surgery (N.O.T.E.S.) now raise the prospect of focused
cancer; intraluminal and transmural resection of small primary tumors without abdominal wall trans-
Sentinel node mapping; gression. The potential clinical benefit that patients may accrue from targeted dissection as
Natural Orifice definitive treatment in place of radical operation is not yet definitively proven but may be
Transluminal considerable at least in the short-term. However, oncological propriety and outcomes must
Endoscopic Surgery be maintained. In particular methods by which regional nodal staging can be assured if stan-
(N.O.T.E.S.) dard operation is avoided need still to be established. Sentinel node mapping is one such puta-
tive means of doing so that deserves serious consideration from this perspective as it performs
a similar function for breast cancer and melanoma and because there is already considerable
evidence to suggest the technique in colonic neoplasia may be at its most accurate in germinal
disease. In addition, it may already be employed by laparoscopy while solely transluminal
means of its deployment are advancing. While the confluence of operative technologies and
techniques now coming on-stream has the potential to precipitate a dramatic shift in the para-
digm for the management of early stage colonic neoplasia, considerable confirmatory study is
required to ensure that oncology propriety and treatment efficacy is maintained so that
patient benefit may be maximized.
2008 Elsevier Ltd. All rights reserved.

Contents

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
Rationale for standard operative extent . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
Appeal of localized resection for colon cancer . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
Specific evidence regarding limited colonic operation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00

* Corresponding author.Tel.: +353872886417.


E-mail addresses: cahillra@gmail.com, ronancahill@eisri.com (R.A. Cahill).

0960-7404/$ - see front matter 2008 Elsevier Ltd. All rights reserved.
doi:10.1016/j.suronc.2008.08.004

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Current means of regional staging colonic cancer without complete mesenteric resection . . . . . . . . . . . . . . . . . 00
Sentinel node mapping for minimally invasive staging of early stage disease . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
Concluding discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
Conflict of interest statement . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00

Introduction so that such patients are not sub-optimally treated [13].


This principle is perhaps especially true in those with early
While the benefits of minimized visceral and lymph basin T-stage disease as approximately 10% of even T1 tumors
resection are readily apparent for patients with early have nodal metastases [14].
cancers of the breast, integument, stomach and, even, An accurate way of precisely determining nodal status
rectum, the current paradigm for the elective treatment of without recourse to radical resection is therefore essential
colon cancer depends on anatomic excision of a long for the evolution of true minimally invasive techniques as
segment of colon with en bloc mesenteric resection in a compelling alternative to conventional operation. In
every case. Indeed many experts have already stated their addition to both improving the efficacy (by determining
assumption that limiting operative extent in the context of those with apparently early disease who are in fact unsuit-
conventional surgical approaches for this disease provides able for localized resection because of nodal dissemination)
negligible gain [1]. However the attendant short-term and expanding the application (by identifying those who are
morbidity rates are in order of 15e25% depending on actually node negative despite more advanced mural
whether the operation is performed by an open or laparo- disease) of endoscopic approaches, a capacity to ensure
scopic approach respectively [2]. Furthermore, there is precise nodal staging without mesenteric excision would
increasing awareness of additional iatrogenic complications allow novel procedures such as N.O.T.E.S. techniques to
of long-term impact such as sexual and urinary dysfunction evolve with a pure focus on the primary lesion. Lymphatic
that may be associated with extensive dissection [3]. mapping and sentinel node biopsy, if performed by mini-
Finally, the high arterial-tie necessary to glean the apical or mally invasive means, may provide the opportunity to assure
para-aortic nodes mandates wide intestinal resection to appropriate patient selection as it does for cancers at other
ensure adequate anastomotic vascularization. This predis- sites. However, the evolution of this technique, at least
poses to impaired postoperative bowel function (at least in from this perspective, has been constrained by the use of
the short-term) and may contribute to the risk of anasto- conventional operation to resect the primary disease. The
motic dehiscence. While very understandable in the advance of endoscopic resective techniques means that this
context of advanced disease, such adverse outcomes are may no longer be the case and so the purpose of lymphatic
less forgivable in patients with early, truly node negative mapping in colon cancer needs re-evaluation [15].
disease. These patients could have their disease cured by The aim of this review is, first, to discuss the rationale
localized resection and only gain reassurance from the for the conventional surgical approach for colon cancer
mesenteric component of their surgery rather than any along with its inherent potential for iatrogenic injury. It will
therapeutic advantage. As the number of patients pre- then deliberate the theoretical advantages of limiting
senting with germinal neoplasia is expanding due to operative dissection and analyze the available clinical
increased patient and physician awareness as well as pop- evidence in support of such a strategy. Finally, it will
ulation screening, the clinical advantages and optimum consider the evidence regarding sentinel node mapping as
means of application of truly minimally invasive techniques a means by which oncological providence may be preserved
in their address therefore needs serious consideration. in the absence of en bloc mesenteric dissection. As much as
Innovative procedures such as endoscopic submucosal frame the case for minimized dissection, such a review
dissection (ESD) and laparoscopic-assisted polypectomy should clearly identify the specific research still necessary
now confer the facility to ensure margin-free resection of to be performed before novel strategies should be prof-
small primary lesions without conventional operation [4e fered in clinical practice.
7], Furthermore, Natural Orifice Transluminal Endoscopic
Surgery (N.O.T.E.S.) portends the prospect of performing Rationale for standard operative extent
narrow-margin transmural resection of such lesions without
incurring abdominal wall transgression [8,9], and already The primary purpose for proposing and performing
hybrid techniques based on this approach are entering the conventional radical operation for early stage colon cancer
clinical domain [10,11], As much as technical capacity, is to ensure accurate regional staging. Although radiological
these techniques however also need to provide a means of imaging can out-rule gross adjacent organ invasion and
consistently ensuring their oncological propriety. Despite methods such as endoscopic ultrasound can provide the
advances in gene profiling, biopsy analysis and perioper- capacity to accurately stage the degree of mural penetra-
ative imaging, no surrogate measure has yet proven 100% tion, to date, no means other than direct analysis has
reliable [12]. It therefore remains mandatory at present to proven wholly convincing for the accurate detection of
ensure that all those with nodal dissemination are detected nodal deposits (see Current means of regional staging

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colonic cancer without complete mesenteric resection intraoperative haemorrhage, the potential for inadvertent
below). Because the location of the first order nodes is not adjacent organ injury is clearly greatly reduced if operative
always adjacent to the primary site, adequate oncological extent is curtailed as the likelihood of ureteric, duodenal
staging requires examination of all the regional nodes. Thus and (in the male) spermatic vessel injury is linked to the
the extent of the standard radical operation for colonic necessity for root mesenteric dissection. Equally, the
cancer is determined by the necessity to ensure full lymph hazard of splenic laceration that occurs with mobilization
node basin clearance concomitantly with resection of the of this left colonic flexure would be obviated in many cases
primary in every case (i.e. en bloc or radical mesenteric were a limited resection performed as extensive mobiliza-
resection) [16]. Although marginal clearance of the primary tion to ensure a tension-free anastomosis would no longer
is usually possible with longitudinal margins between 5 cm be necessary. This operative step, rated as considerably
and 10 cm (colonic tumors in fact rarely infiltrate more hazardous by trainees [26], leads to iatrogenic injury to the
then 2 cm beyond the area of gross involvement [17] and spleen in between 1% and 8% of left hemicolectomies and
extended margins do not improve oncological outcome indeed colonic surgery in general accounts for between
[18e20]), the associated radical lymphadenectomy often 34.3% and 59.9% of splenectomies for iatrogenic injury
mandates a larger visceral resection. This is because [27e29]. This results in considerable acute morbidity as
lymphatic drainage follows the arterial regional blood well as prolonged operation time and hospital stay [30], and
supply and so proximal vascular ligation (a high-tie) is the patient engenders both postoperative [31] and life-long
necessary to ensure complete resection of the entire [32] infectious susceptibility and, it seems, impaired
lymphatic delta. This manoeuvre is therefore the primary oncological outcome.[33,34]
determinant of the extent of the segmental bowel resec- Postoperatively, bowel function may also be expected to
tion required so that the risk of ischemia of the residual be better with limited field dissection[35,36] as symptoms
bowel and re-anastomosis is minimized. Although there is noticeably deteriorate with increasing length of left colon
likely to be a therapeutic value in resecting nodes positive resection[37] and seem ameliorated when longer remnants
for metastatic disease in colon cancer, the main value of have been conserved [38]. Furthermore diminished rates of
such clearance for truly lymph node negative patients can anastomotic dehiscence (because of reduced ischemic
only be the gain of reassurance. If node negativity could be potential of the resection margins [39e41]) as well as
assured without recourse to standard en bloc resection, the shortened duration of postoperative ileus (known to be
operative extent could clearly be lessened. related to operative extent [42,43]) are speculatively
Furthermore, it is worth considering that formal lym- additional advantages that may combine to reduce post-
phadenectomy has its limitations even as the gold stan- operative convalescence as well as in-hospital stay and
dard method of for staging. Firstly, there is controversy in expenditure. Finally, flush ligation of the IMA at its origin
pathological reporting as to what actually constitutes from the abdominal aorta risks injury of the para-aortic
a lymph node metastases with some staging classifications nerves. By this mechanism, anorectal function may be
counting the presence of a tumor deposit over a certain size impaired postoperatively (at least up to one year) as may
as being nodal disease whether or not there is histological sexual function [44]. Although urinary dysfunction is more
evidence of a lymphatic tissue present [77]. Current likely related to pre-sacral nerve injury, this too may occur
criteria are in addition based solely on lymph node number when the radical operation for colon cancer involves
without regard for anatomic classification as in other dissection of and below the colorectal junction. The
staging systems [21]. Clearly also the length of bowel potential for these sequelae has received most attention in
resected will dictate how much mesentery accompanies colonic surgery for benign conditions and, in this scenario,
the specimen for evaluation and there is extensive vari- has led many experts to advocate more conservative
ability in what comprises the standard. Furthermore, operations in order to improve patient outcome. In the
despite a standard operation being performed, nodal longer postoperative term, the extent of postoperative
harvests are often inadequate and many groups currently adhesion formation has long been established as being
fall short of the exacting requirements necessary to ensure related to operative extent and limiting the degree of
that the patient is truly node negative [22e24]. Supple- dissection seems likely to at least limit the distribution if
mentary techniques aimed at increasing lymph harvest are not the degree of peritoneal scarring. This in itself could
both time- and expense-consuming especially if sophisti- present considerable advantages for patients, surgeons and
cated measures of micrometastatic disease are utilized. If health care providers [45].
validated, an alternative means of performing precise
regional staging could in fact aid the standardization of the
diagnosis of node negative colon cancer and alleviate much Specific evidence regarding limited
of the variation involved in the analysis of all the nodes colonic operation
present in an entirely resected lymph basin [25].
Although clinical benefit with lesser operation was first
presented decades ago [46], the issue has only infrequently
Appeal of localized resection for colon cancer been addressed since and there are only few publications
directly comparing limited versus radical resection. There
The potential gains of localized intestinal resection obvi- has however been one multicentre randomized trial [47]
ously include shortened operative time but also should that addressed this issue before the concept of non-radical
provide additional benefits arising secondarily from surgery became unfashionable and the focus switched to
reduced dissection. As much as lessened likelihood of ensuring staging adequacy by maximizing lymph node

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harvest [48]. This study randomly allotted 260 patients treated with localized resection. The key issue though in
(after exclusions for protocol violations) with intraperito- order to respect oncological providence is that such N0
neal left colonic carcinoma to either radical left hemi- patients are precisely identified before opting for a non-
colectomy (with ligation of the IMA at its origin) or left radical operative address of the primary lesion (e.g.
segmental colectomy (with preservation of the origin of endoscopic resection of the primary). However, preopera-
the IMA). While overall early postoperative morbidity tive radiological imaging alone for the detection of nodal
was similar (albeit with a non-significant trend towards metastases has remained unsatisfactory for this purpose
increased postoperative mortality in the extended resec- because most tumor-containing nodes lie below the
tion group), bowel function was significantly better in the threshold of these modalitys discriminative capacity
group undergoing the more conservative resection. Since (approximately 70% of nodes containing metastases are less
then however there have only been three retrospective than 5 mm in size[57e61],) despite the use of sophisticated
single centre reports supporting sigmoidectomy in place of techniques and protocols [62]. Their capacity is particularly
more radical operation in carefully selected patients limited when the main tumor deposit is a micrometastasis
[18,49,50]. as may be expected in the initial stages of lymphatic
There have though been some additional studies that dissemination associated with early cancers. However, with
have focused on the specific operative steps that would be modifications modalities such as PETeCT scanning may be
eliminated or at least markedly reduced should a more able to contribute to any patient-selection process by at
limited bowel resection be performed. Each of these least out-ruling the proportion with gross nodal metastases
publications has tended to show advantages for both the [63,64]. Furthermore while endoscopic ultrasound has
operator and patient if dissection extent is minimized. One proven efficacious for T-staging colon cancer, it has been
recent study examining the benefits of selective splenic less sensitive in its capacity to N-stage [65,66]. Finally, and
flexure mobilization during open anterior resection, rather despite considerable recent advances[12,14], analysis of
than its performance de rigor, confirmed the considerable surrogate markers of lymphatic invasion in either biopsy
practical benefit of reduced operative time without incur- specimens or indeed the fully resected specimen, have not
ring increased anastomotic leak rates [51]. In addition, the been 100% predictive of nodal involvement.
lesser dissection that is necessary to perform a medial- The inability of these modalities to truly reflect the
to-lateral vascular approach in the laparoscopic mobiliza- metastatic potential of the primary means that endoscopic
tion of the left colon has been found significantly related to resection for even the earliest cancers [67] risks either the
reduced operative time and lessened postoperative understaging of systemic disease or the rendering of the
recovery for both right [52] and left-sided [53] operations. effort redundant if formal resection becomes indicated by
Finally, the beneficial effects of preservation of the inferior the full pathology of the resected specimen [13]. Such an
marginal artery have also been shown to impart clinical occurrence may either mandate second extirpative opera-
benefit albeit in operation for benign disease [54]. tion if suspicion of lymphatic dissemination is aroused only
Although further evidential proof is required, in short, after pathological analysis of the primary tumor [68] or,
the clinical benefits of localized rather then radical colec- more worryingly, result in suboptimal clinical outcome if
tomy cannot be assumed to be minimal and may in fact be the patient remains understaged. Thus formal nodal anal-
considerable. Any diminution in surgical risk may particu- ysis remains the gold standard for prognosis prediction and
larly present significant advantages in vulnerable patients adjuvant therapy prescription [13]. Therefore, currently,
[55] while ensuring their oncological outcome is not the only tumors suitable for localized resection are those in
compromised [56]. whom the risk of lymphatic spread is absolutely minimal.
This has led to recommendations that ESD resection should
Current means of regional staging colonic only be performed in the colon for malignant lesions well
below its technical capability (i.e. in general T1 submucosal
cancer without complete mesenteric resection layer (sm)-1 lesions <20 mm in diameter with no adverse
prognostic features) [12,69,70].
Although nodal burden increases in association with the
T-stage of the primary (see Table 1), the majority of
patients with T1 or T2 stage disease could potentially be Sentinel node mapping for minimally invasive
staging of early stage disease
Table 1 Table illustrating the proportions of patients with Sentinel node mapping in general presents a means of
lymph node positivity by T-stage of the primary lesion gleaning the same information without recourse to full
Early stage Lymph node involvement lymph basin resection. However despite broad acceptance
T1 overall (%) 7e15 in other cancers (including, in principle, gastric cancer
sm1 (%) 3e4.2 [71e73]), consideration of the technique for colonic
sm2 (%) 8e21.3 neoplasia has been framed by its performance via the same
sm3 (%) 23e38.5 means as the definitive operation (i.e. at either open or
T2 Overall (%) 14.5e43 laparoscopic resection) [74e82]. This means that the
operative approach and access are already determined and
Incidence figures derived from Refs. [13,14,67,110e114]. Sm so concomitant full lymph node dissection is readily
denotes the extent of submucosal invasion within the category
enabled without adding extra procedural effort. However,
of T1 disease.
this perspective is considerably altered if the primary is

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Table 2 Summary table of all published reports regarding sentinel node biopsy in colorectal cancer
First author Year Journal Detection rate Accuracy rate Sensitivity rate False negative rate
Saha 2000 Ann Surg Oncol 99 96 91 9
Wiese 2000 Arch Pathol Lab Med 99 96 91 9
Waters 2000 Am Surg 91 100 100 0
Bilchik 2001 J Clin Oncol 100 100 100 0
Paramo 2001 Am J Surg 71 100 97 3
Wood 2001 Ann Surg Oncol 96 95 88 12
Wood 2001 Surg Endosc 100 100 100 0
Saha 2001 Ann Surg Oncol 98 96 90 10
Esser 2001 Dis Colon Rectum 58 94 67 33
Bendavid 2002 J Surg Oncol 90 94 95 5
Paramo 2002 Ann Surg Oncol 82 98 93 7
Wood 2002 J GastroInt Surg 97 95 92 8
Bilchik 2002 Eur J Cancer 97 95 91 5
Kitagawa 2002 Dis Colon Rectum 91 92 82 18
Feig 2002 Am J Surg 98 79 38 62
Broderick-Villa 2002 Cancer J 92 79 50 50
Tsioulias 2002 Am Surg 100 93 67 33
Nastro 2002 Tumori 75 100 100 0
Bilchik 2003 Cancer Control 100 93 91 9
Cox 2003 Curr Surg 100 100 100 0
Bilchik 2003 J Clin Oncol 96 96 92 8
Turner 2003 Archives Path 82 92 87 13
Trocha 2003 J GastroInt Surg 98 95 84 16
Veihl 2003 W J Surg 87 78 50 22
Levine 2003 J GastroInt Surg 92 ns 50 ns
Saha 2004 Dis Colon Rectum 99 ns 88 12
Dan 2004 Arch Surg 99 96 86 16
Braat 2004 Eur J Surg Oncol 94 97 80 20
Bertoglio 2004 J Surg Oncol 95 92 78 22
Read 2004 Dis Colon Rectum 79 97 25 75
Patten 2004 Cancer 98 89 83 17
Bertagnolli 2004 Ann Surg 92 80 46 54
Saha 2004 Ann Surg Oncol 100 95 84 16
Saha 2004 Semin Oncol 100 96 92 8
Bembenek 2005 W J Surg 85 ns 92 4
Codnignola 2005 J Clin Oncol 100 ns 72 28
Dahl 2005 Eur J Surg Oncol 100 92 83 17
Bilchik 2006 Arch Surg 100 95 88 12
Tuech 2006 Eur J Surg Oncol 97 94 91 9
Saha 2006 Am J Surg 98 96 90 10
Kelder 2006 Scand J Gastroenterol 97 93 86 14
Thomas 2006 Am Surg 93 20 46 54
Covarelli 2006 Am Surg 95 95 86 14
Kelder 2007 Int J Col Dis 97 96 89 11
Bianchi 2007 Surg End 100 95 83 17
Lim 2007 Ann Surg Oncol 99 83 59 41
Murawa 2007 Acta Chir Belg 93 84 83 17
Bembenek 2007 Ann Surg 85 86 54 46
Sandrucci 2007 J Surg Oncol 100 91 92 9
Tiffet 2007 Dis Colon Rectum 92 81 80 20
Faerden 2008 Dis Colon Rectum 93 86 53 47
Quadros CA 2008 J Surg Oncol 91 79.5 65 35
Note: All studies are shown for completeness, however several studies have published experiences more than once and so have likely
overlapped patient cohorts.

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proposed to be resected by an intraluminal or transluminal possibility would be the harness of advanced optical
endoscopic route. This is particularly the case given that imaging techniques such as optical coherence tomography
the sentinel node mapping can be performed by a laparo- [99] with or without spectroscopy [100,101] (among other
scopic route (and perhaps even by a single port access techniques [102]) to perform an in vivo virtual biopsy of
operation) or, more intriguingly although still experimental, the sentinel node in situ. It is clear though that any means
by a N.O.T.E.S. approach [83]. Further, as much as aiding in of performing rapid analysis of the selected nodes in order
ensuring appropriate patient selection by regional staging, to allow the resection to progress by which ever means
the presence of a concomitant intraperitoneal view may found appropriate (i.e. endoscopic or conventional) would
supplement endoscopic resection of small primary lesions have to meet or exceed the use of immunohistochemistry
in a role already been proposed for adjoint laparoscopy in the detection of micrometastases. However there is
[84,85]. Thus in this way sentinel node biopsy could precedent for such analysis for breast cancer in particular
augment the oncological providence of endoscopic resec- [103e106]. Finally, consideration could be given, at least in
tive techniques without undermining their clinical the early stages of any clinical experience, to confining the
appositeness. technique to those patients least likely to harbour
Confidence in intestinal lymphatic mapping has however lymphatic metastases (e.g. screen detected early stage
been undermined by high discrepancies in the reported cancer) or those in whom the sentinel node is most likely to
results (see Table 2). However, to date, the primary focus be detected (e.g. slim patients without previous abdominal
has been on the facility of sophisticated histological scru- operation). Adjunctive radiological staging as discussed
tiny of the sentinel node to upstage disease after conven- above may also contribute by out-ruling patients with
tional operation has taken place and the focus has primarily evident lymphadenopathy.
been on patients with Stage II disease rather than Stage I.
Closer analysis of the literature regarding sentinel node in Concluding discussion
colon cancer reveals that the considerable variability in
results may be explained by the considerable heterogeneity
None of the concepts presented here are particularly new
of study design employed and, in particular, their patient
and similar considerations have previously prompted others
inclusion criteria [86]. Although selective extraction of data
to look for ways to safely reduce dissection extent by
by formal meta-analysis to definitively determine the
careful case selection [107e109]. Inaccuracy of surrogate
adequacy of the technique selectively in early stage colon
markers and concern over non-adjacent or skip metastases
cancer is impossible by reason of lack of homogeneity [87],
remains the main limitation of these proposals however.
every analysis of false negative rates to date points to
What makes their reconsideration compelling now is the
contamination of the study cohort by rectal cancer, inclu-
potential confluence of novel technologies that encourage
sion of advanced colonic disease, operator inexperience
fundamental challenge of our current preconceptions.
and patient obesity as primary confounders of the tech-
Definitive excisional surgery and staging assurance for early
nique. However two large multicentre trials have shown
stage colon cancer without recourse to conventional oper-
that, when these factors are adjusted for, the accuracy of
ation is certainly possible in concept and seems likely to be
the technique can approach similar levels to those that
increasingly advocated by experts and sought by patients.
justify its use as a means of individualization of surgical
In the absence of a compelling disruptive technology
resection extent in breast cancer and melanoma (i.e.
emerging, lymphatic mapping and sentinel node biopsy
sensitivity of 95%) [88,89]. Therefore, as in these diseases,
seems best placed to provide supportive oncological
it may be that the technique is most reliable in those same
propriety in the near future. However, it should be stated
patients who are most suitable for localized resection of
that, in general, technology is best developed following the
their primary (i.e. T1 and perhaps T2 disease of small
clinical indication. Therefore, if localized resection for
diameter) although this has yet to be definitively proven in
early stage cancer becomes an acceptable concept, it is
a prospective manner.
likely that current technologies such as radiological staging
Additionally, the current propensity for performing
will be re-directed towards this application and will likely
sentinel node biopsy as an adjunct to conventional staging
develop to meet its demands.
has led the technique to develop within this conceptual
In conclusion however, while intuitively attractive, it
framework. As the operation proceeds regardless, blue dye
remains to be definitively proven that localized resection of
alone is most often considered sufficient for the mapping.
early stage colon cancer can meet the oncological require-
However, the greater import that would be attached to the
ments of cancer surgery and indeed whether lymphatic
accuracy and reliability of the technique if operative
mapping can determine regional nodal status as accurately
extent was indeed to be determined by the results of this
as en bloc mesenteric resection in early stage colon cancer.
test would encourage the use and development of addi-
Any short-term patient benefits they may supply would be
tional means of improving technical efficacy and efficiency.
markedly outweighed by any compromise of oncological
Already there have been reports regarding the use of iso-
outcome and so progress in this field must be cautiously
type markers (suggested to improve the techniques results
undertaken with a focus on cancer biology and therapy as
for cancers of the colon [90,91] as well as for other sites
much as technological and technical advance.
[92e94]), fluorescent dyes [95,96] and enhanced detection
probes [97] (both likely to help in obese mesenteries e
a considerable confounding issue in sentinel node detection Conflict of interest statement
rates [98]) and further advances would be likely if the
clinical indication shifted to require it. One intriguing such The authors have no conflict of interest.

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References editors. Lippincott Willaims & Wilkins: PA, USA. [chapter 46.
p. 1121].
[21] Roukos DH, Kappas AM. Perspectives in the treatment of
[1] Sticca RP. Is there a clinical value to sentinel lymph node
gastric cancer. Natl Clin Pract Oncol 2005;2:98e107.
sampling in colon cancer? J Clin Oncol 2006;24:1e2.
[22] Chen SL, Bilchik AJ. More extensive nodal dissection
[2] Hinojosa MW, Murrell ZA, Konyalian VR, Mills S, Nguyen NT,
improves survival for stages I to III of colon cancer. Ann Surg
Stamos MJ. Comparison of laparoscopic vs open sigmoid
2006;244:602e10.
colectomy for benign and malignant disease at academic
[23] Steele GJ. Colorectal cancer. In: McKenna RJ, Murphy GP,
medical centers. J Gastrointest Surg 2007;11:1423e9.
editors. Cancer surgery. Philadelphia: Lippincott; 1994. p.
[3] Bader FG, Roblick UJ, Oevermann E, Bruch HP, Schwandner O.
125e84.
Radical surgery for early colorectal cancer-anachronism or
[24] Joseph NE, Sigurdson ER, Hanlon AL, Wang H, Mayer RJ,
oncologic necessity. Int J Colorectal Dis 2008;23:401e7.
MacDonald JS, et al. Accuracy of determining nodal nega-
[4] Tamegai Y, Saito Y, Masaki N, Hinohara C, Oshima T,
tivity in colorectal cancer on the basis of the number of
Kogure E, et al. Endoscopic submucosal dissection: a safe
nodes retrieved on resection. Ann Surg Oncol 2003;10:213e8.
technique for colorectal tumors. Endoscopy 2007;39:418e22.
[25] Kitagawa Y, Watanabe M, Hasegawa H, Yamamoto S, Fujii H,
[5] Hurlstone DP, Atkinson R, Sanders DS, Thomson M, Cross SS,
Yamamoto K, et al. Sentinel node mapping for colorectal
Brown S. Achieving R0 resection in the colorectum using
cancer with radioactive tracer. Dis Colon Rectum 2002;45:
endoscopic submucosal dissection. Br J Surg 2007;94:1536e42.
1476e80.
[6] Adachi Y, Yasuda K, Kakisako K, Sato K, Shiraishi N, Kitano S.
[26] Torrup A. Surveillance of surgical training by detailed elec-
Histopathologic criteria for local excision of colorectal
tronic registration of logical components. Postgrad Med J
cancer: multivariate analysis. Ann Surg Oncol 1999;6:385e8.
2002;78:607e11.
[7] Tanaka S, Oka S, Kaneko I, Hirata M, Mouri R, Kanao H, et al.
[27] Coon WW. Iatrogenic splenic injury. Am J Surg 1990;159:
Endoscopic submucosal dissection for colorectal neoplasia:
585e8.
possibility of standardization. Gastrointest Endosc 2007;66:
[28] Cioffiro W, Schein CJ, Gliedman ML. Splenic injury during
100e7.
abdominal surgery. Arch Surg 1976;111:167e71.
[8] Whiteford MH, Denk PM, Swanstrom LL. Feasibility of radical
[29] Cassar K, Munro A. Iatrogenic splenic injury. J R Coll Surg
sigmoid colectomy performed as natural orifice translumenal
Edinb 2002;47:731e41.
endoscopic surgery (NOTES) using transanal endoscopic
[30] Konstadoulakis MM, Kymionis GD, Leandros E, Ricaniadis N,
microsurgery. Surg Endosc 2007;21:1870e4.
Manouras A, Krespis E, et al. Long term effect of splenec-
[9] Leroy J, Cahill RA, Perretta S, Forgione A, Dallemagne B,
tomy on patients operated on for cancer of the left colon:
Marescaux J. Totally natural orifice transluminal endoscopic
a retrospective study. Eur J Surg 1999;165:583e7.
surgery in a porcine model with survival. Surg Endosc, in press.
[31] Varty PP, Linehan IP, Boulos PB. Does concurrent splenec-
[10] Lacy AM, Delgado S, Rojas OA, Almenara R, Blasi A, Llach J.
tomy at colorectal cancer resection influence survival? Dis
MA-NOS radical sigmoidectomy: report of a transvaginal
Colon Rectum 1993;36:602e6.
resection in the human. Surg Endosc 2008;22:1717e23.
[32] Robinette CD, Fraumeni JF. Splenectomy and subsequent
[11] Bucher P, Pugin F, Morel P. Single port access laparoscopic
mortality in veterans of the 1939e45 war. Lancet 1977;2:
right hemicolectomy. Int J Colorectal Dis 2008 Jul 8 [Epub
127e9.
ahead of print].
[33] Wakeman CJ, Dobbs BR, Frizelle FA, Bissett IP, Dennett ER,
[12] Yasuda K, Inomata M, Shiromizu A, Shiraishi N, Higashi H,
Hill AG, et al. The impact of splenectomy on outcome after
Kitano S. Risk factors for occult lymph node metastasis of
resection for colorectal cancer: a multicenter, nested,
colorectal cancer invading the submucosa and indications for
paired cohort study. Dis Colon Rectum 2008;51:213e7.
endoscopic mucosal resection. Dis Colon Rectum 2007;50:
[34] Davis CJ, Ilstrup DM, Pemberton JH. Influence of splenec-
1370e6.
tomy on survival rate of patients with colorectal cancer. Am
[13] Chok KS, Law WL. Prognostic factors affecting survival and
J Surg 1988;155:173e9.
recurrence of patients with pT1 and pT2 colorectal cancer.
[35] Ho YH, Low D, Goh HS. Bowel function survey after
World J Surg 2007;31:1485e90.
segmental colorectal resections. Dis Colon Rectum 1996;39:
[14] Sakuragi M, Togashi K, Konishi F, Koinuma K, Kawamura Y,
307e10.
Okada M, et al. Predictive factors for lymph node metastasis
[36] Sato K, Inomata M, Kakisako K, Shiraishi N, Adachi Y,
in T1 stage colorectal carcinomas. Dis Colon Rectum 2003;46:
Kitano S. Surgical technique influences bowel function after
1626e32.
low anterior resection and sigmoid colectomy. Hepatogas-
[15] Cahill RA. An alternative perspective on the rationale for
troenterology 2003;50:1381e4.
sentinel node mapping in colon cancer. Ann Surg, in press.
[37] Adachi Y, Kakisako K, Sato K, Shiraishi N, Miyahara M,
[16] Cahill RA. A multicenter trial of sentinel lymph node mapping
Kitano S. Factors influencing bowel function after low ante-
in colorectal cancer: prognostic implications for nodal
rior resection and sigmoid colectomy. Hepatogastroenterol-
staging and recurrence. Am J Surg 2007;194:139e40.
ogy 2000;47:155e8.
[17] Maurer CA. Colon cancer: resection standards. Tech Colo-
[38] Graf W, Ekstrom K, Glimelius B, Pahlman L. A pilot study of
proctol 2004;8(Suppl. 1):S29e32.
factors influencing bowel function after colorectal anasto-
[18] Secco GB, Ravera G, Gasparo A, Percoco P, Zoli S. Segmental
mosis. Dis Colon Rectum 1996;39:744e9.
resection, lymph nodes dissection and survival in patients
[39] Dworkin MJ, Allen-Mersh TG. Effect of inferior mesenteric
with left colon cancer. Hepatogastroenterology 2007;54:
artery ligation on blood flow in the marginal artery-
422e6.
dependent sigmoid colon. J Am Coll Surg 1996;183:357e60.
[19] Nelson H, Petrelli N, Carlin A, Couture J, Fleshman J,
[40] Seike K, Koda K, Saito N, Oda K, Kosugi C, Shimizu K, et al.
Guillem J, et al. National Cancer Institute Expert Panel.
Laser Doppler assessment of the influence of division at the
Guidelines 2000 for colon and rectal cancer surgery. J Natl
root of the inferior mesenteric artery on anastomotic blood
Cancer Inst 2001;93:583e96.
flow in rectosigmoid cancer surgery. Int J Colorectal Dis
[20] Yahanda AM, Chang AE. Colorectal cancer. In Surgery,
2007;22:689e97.
scientific principles and practice. 3rd ed. Greenfield LJ,
[41] Boyle NH, Manifold D, Jordan MH, Mason RC. Intraoperative
Mulholland MW, Oldham KT, Zelenock KT, Lillemore KD,
assessment of colonic perfusion using scanning laser Doppler

Please cite this article in press as: Cahill RA et al., Localized resection for colon cancer, Surgical Oncology (2008), doi:10.1016/
j.suronc.2008.08.004
ARTICLE IN PRESS
+ MODEL
8 R.A. Cahill et al.

flowmetry during colonic resection. J Am Coll Surg 2000;191: cancer: metastases in lymph nodes <5 mm in size. Ann Surg
504e10. Oncol 1996;3:124e30.
[42] Graber JN, Schulte WJ, Condon RE, Cowles VE. Relationship [61] Haboubi NY, Abdalla SA, Amini S, Clark P, Dougal M, Dube A,
of duration of postoperative ileus to extent and site of et al. The novel combination of fat clearance and immuno-
operative dissection. Surgery 1982;92:87e92. histochemistry improves prediction of the outcome of
[43] Luckey A, Livingston E, Tache Y. Mechanisms and treatment patients with colorectal carcinomas: a preliminary study. Int
of postoperative ileus. Arch Surg 2003;138:206e14. J Colorectal Dis 1998;13:99e102.
[44] Sarli L, Pavlidis C, Cinieri FG, Regina G, Sansebastiano G, [62] Low RN, McCue M, Barone R, Saleh F, Song T. MR staging of
Veronesi L, et al. Prospective comparison of laparoscopic left primary colorectal carcinoma: comparison with surgical and
hemicolectomy for colon cancer with laparoscopic left histopathologic findings. Abdom Imaging 2003;28:784e93.
hemicolectomy for benign colorectal disease. World J Surg [63] Tsunoda Y, Ito M, Fujii H, Kuwano H, Saito N. Preoperative
2006;30:446e52. diagnosis of lymph node metastases of colorectal cancer by
[45] Harris DA, Topley N. Peritoneal adhesions. Br J Surg 2008;95: FDG-PET/CT. Jpn J Clin Oncol 2008;38:347e53.
271e2. [64] Inoue K, Sato T, Kitamura H, Ito M, Tsunoda Y, Hirayama A,
[46] Busuttil RW, Foglia RP, Longmire Jr WP. Treatment of carci- et al. Diagnosis supporting algorithm for lymph node metas-
noma of the sigmoid colon and upper rectum. A comparison tases from colorectal carcinoma on 18F-FDG PET/CT. Ann
of local segmental resection and left hemicolectomy. Arch Nucl Med 2008;22:41e8.
Surg 1977;112:920e3. [65] Hunerbein M, Totkas S, Ghadimi BM, Schlag PM. Preoperative
[47] Rouffet F, Hay JM, Vacher B, Fingerhut A, Elhadad A, evaluation of colorectal neoplasms by colonoscopic minip-
Flamant Y, et al. Curative resection for left colonic robe ultrasonography. Ann Surg 2000;232:46e50.
carcinoma: hemicolectomy vs. segmental colectomy. A [66] Stergiou N, Haji-Kermani N, Schneider C, Menke D,
prospective, controlled, multicenter trial. French Associa- Kockerling F, Wehrmann T. Staging of colonic neoplasms by
tion for Surgical Research. Dis Colon Rectum 1994;37: colonoscopic miniprobe ultrasonography. Int J Colorectal Dis
651e9. 2003;18:445e9.
[48] Desch CE, McNiff KK, Schneider EC, Schrag D, McClure J, [67] Fang WL, Chang SC, Lin JK, Wang HS, Yang SH, Jiang JK, et al.
Lepisto E, et al. American society of clinical oncology/ Metastatic potential in T1 and T2 colorectal cancer. Hep-
national comprehensive cancer network quality measures. atogastroenterology 2005;52:1688e91.
J Clin Oncol 2008;26:3631e7. [68] Bergmann U, Beger HG. Endoscopic mucosal resection for
[49] Di Cataldo A, La Greca G, Lanteri R, Rapisarda C, Li Destri G, advanced non-polypoid colorectal adenoma and early stage
Licata A. Cancer of the sigmoid colon: left hemicolectomy or carcinoma. Surg Endosc 2003;17:475e9.
sigmoidectomy? Int Surg 2007;92:10e4. [69] Tanaka S, Haruma K, Teixeira CR, Tatsuta S, Ohtsu N,
[50] Diaconu C, Ghenghe D, Dragomir C. The segmentary colec- Hiraga Y, et al. Endoscopic treatment of submucosal inva-
tomy or the left hemicolectomy for sigmoid cancer. Rev Med sive colorectal carcinoma with special reference to risk
Chir Soc Med Nat Iasi 2002;106:132e6. factors for lymph node metastasis. J Gastroenterol 1995;30:
[51] Brennan DJ, Moynagh M, Brannigan AE, Gleeson F, 710e7.
Rowland M, OConnell PR. Routine mobilization of the splenic [70] Shimomura T, Ishiguro S, Konishi H, Wakabayashi N,
flexure is not necessary during anterior resection for rectal Mitsufuji S, Kasugai T, et al. New indication for endoscopic
cancer. Dis Colon Rectum 2007;50:302e7. treatment of colorectal carcinoma with submucosal invasion.
[52] Liang JT, Lai HS, Lee PH. Laparoscopic medial-to-lateral J Gastroenterol Hepatol 2004;19:48e55.
approach for the curative resection of right-sided colon [71] Kitagawa Y, Kitajima M. Endoscopic treatment combined
cancer. Ann Surg Oncol 2007;14:1878e9. with laparoscopic sentinel node mapping for superficial
[53] Liang JT, Lai HS, Huang KC, Chang KJ, Shieh MJ, Jeng YM, gastrointestinal cancers. Endoscopy 2007;39:471e5.
et al. Comparison of medial-to-lateral versus traditional [72] Saikawa Y, Otani Y, Kitagawa Y, Yoshida M, Wada N, Kubota T,
lateral-to-medial laparoscopic dissection sequences for et al. Interim results of sentinel node biopsy during laparo-
resection of rectosigmoid cancers: randomized controlled scopic gastrectomy: possible role in function-preserving
clinical trial. World J Surg 2003;27:190e6. surgery for early cancer. World J Surg 2006;30:1962e8.
[54] Tocchi A, Mazzoni G, Fornasari V, Miccini M, Daddi G, [73] Kitagawa Y, Fujii H, Kumai K, Kubota T, Otani Y, Saikawa Y,
Tagliacozzo S. Preservation of the inferior mesenteric artery et al. Recent advances in sentinel node navigation for gastric
in colorectal resection for complicated diverticular disease. cancer: a paradigm shift of surgical management. J Surg
Am J Surg 2001;182:162e7. Oncol 2005;90:147e51.
[55] Janssen-Heijnen ML, Maas HA, Houterman S, Lemmens VE, [74] Tuech JJ, Pessaux P, Regenet N, Bergamaschi R, Colson A.
Rutten HJ, Coebergh JW. Comorbidity in older surgical Sentinel lymph node mapping in colon cancer. Surg Endosc
cancer patients: influence on patient care and outcome. Eur 2004;18:1721e9.
J Cancer 2007;43:2179e93. [75] Prabhudesai AG, Kumar D. The sentinel lymph node in
[56] Faivre J, Lemmens VE, Quipourt V, Bouvier AM. Management colorectal cancer e of clinical value? Colorectal Dis 2002;4:
and survival of colorectal cancer in the elderly in population- 162e6.
based studies. Eur J Cancer 2007;43:2279e84. [76] Mulsow J, Winter DC, OKeane JC, OConnell PR. Sentinel
[57] Monig SP, Baldus SE, Zirbes TK, Schroder W, Lindemann DG, lymph node mapping in colorectal cancer. Br J Surg 2003;90:
Dienes HP, et al. Lymph node size and metastatic infiltration 659e67.
in colon cancer. Ann Surg Oncol 1999;6:579e81. [77] Cserni G. Nodal staging of colorectal carcinomas and sentinel
[58] Herrera-Ornelas L, Justiniano J, Castillo N, Petrelli NJ, nodes. J Clin Pathol 2003;56:327e35.
Stulc JP, Mittelman A. Metastases in small lymph nodes from [78] de Haas RJ, Wicherts DA, Hobbelink MG, Borel Rinkes IH,
colon cancer. Arch Surg 1987;122:1253e6. Schipper ME, van der Zee JA, et al. Sentinel lymph node
[59] Herrera L, Villarreal JR. Incidence of metastases from rectal mapping in colon cancer: current status. Ann Surg Oncol
adenocarcinoma in small lymph nodes detected by a clearing 2007;14:1070e80.
technique. Dis Colon Rectum 1992;35:783e8. [79] Braat AE, Oosterhuis JW, Moll FC, de Vries JE. Successful
[60] Rodriguez-Bigas MA, Maamoun S, Weber TK, Penetrante RB, sentinel node identification in colon carcinoma using Patent
Blumenson LE, Petrelli NJ. Clinical significance of colorectal Blue V. Eur J Surg Oncol 2004;30:633e7.

Please cite this article in press as: Cahill RA et al., Localized resection for colon cancer, Surgical Oncology (2008), doi:10.1016/
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Localized resection for colon cancer 9

[80] Doekhie FS, Peeters KC, Kuppen PJ, Mesker WE, Tanke HJ, [98] Bembenek AE, Rosenberg R, Wagler E, Gretschel S,
Morreau H, et al. The feasibility and reliability of sentinel Sendler A, Siewert JR, et al. Sentinel lymph node biopsy in
node mapping in colorectal cancer. Eur J Surg Oncol 2005;31: colon cancer: a prospective multicenter trial. Ann Surg 2007;
854e62. 245:858e63.
[81] Bembenek A, Gretschel S, Schlag PM. Sentinel lymph node [99] Luo W, Nguyen FT, Zysk AM, Ralston TS, Brockenbrough J,
biopsy for gastrointestinal cancers. J Surg Oncol 2007;96: Marks DL, et al. Optical biopsy of lymph node morphology
342e52. using optical coherence tomography. Technol Cancer Res
[82] Iddings D, Bilchik A. The biologic significance of micro- Treat 2005;4:539e48.
metastatic disease and sentinel lymph node technology on [100] Hama Y, Koyama Y, Urano Y, Choyke PL, Kobayashi H.
colorectal cancer. J Surg Oncol 2007;96:671e7. Simultaneous two-color spectral fluorescence lymphangiog-
[83] Cahill RA, Perretta S, Leroy J, Dallemagne B, Marescaux J. raphy with near infrared quantum dots to map two lymphatic
Lymphatic mapping and sentinel node biopsy in the colonic flows from the breast and the upper extremity. Breast
mesentery by Natural Orifice Transluminal Endoscopic Cancer Res Treat 2007;103:23e8.
Surgery (NOTES). Ann Surg Oncol 2008;15(10):2677e83. [101] Johnson KS, Chicken DW, Pickard DC, Lee AC, Briggs G,
[84] Franklin Jr ME, Leyva-Alvizo A, Abrego-Medina D, Glass JL, Falzon M, et al. Elastic scattering spectroscopy for intra-
Trevino J, Arellano PP, et al. Laparoscopically monitored operative determination of sentinel lymph node status in the
colonoscopic polypectomy: an established form of endolu- breast. J Biomed Opt 2004;9:1122e8.
minal therapy for colorectal polyps. Surg Endosc 2007;21: [102] Sharma R, Wendt JA, Rasmussen JC, Adams KE, Marshall MV,
1650e3. Sevick-Muraca EM. New horizons for imaging lymphatic
[85] Hensman C, Luck AJ, Hewett PJ. Laparoscopic-assisted function. Ann N Y Acad Sci 2008;1131:13e36.
colonoscopic polypectomy: technique and preliminary [103] Tew K, Irwig L, Matthews A, Crowe P, Macaskill P. Meta-
experience. Surg Endosc 1999;13:231e2. analysis of sentinel node imprint cytology in breast cancer.
[86] Cahill RA. Whats wrong with sentinel node mapping in colon Br J Surg 2005;92:1068e80.
cancer. World J Gastroenterol 2007;3:6291e4. [104] Ali R, Hanly AM, Naughton P, Castineira CF, Landers R,
[87] Cahill RA, Leroy J, Marescaux J. Could lymphatic mapping Cahill RA, et al. Intraoperative frozen section assessment of
and sentinel node biopsy provide oncological providence for sentinel lymph nodes in the operative management of women
local resectional techniques for colon cancer? A review of the with symptomatic breast cancer. World J Surg Oncol 2008;6:69.
literature. BMC Surgery, in press. [105] Tsujimoto M, Nakabayashi K, Yoshidome K, Kaneko T,
[88] Bilchik AJ, Hoon DS, Saha S, Turner RR, Wiese D, DiNome M, Iwase T, Akiyama F, et al. One-step nucleic acid amplification
et al. Prognostic impact of micrometastases in colon cancer: for intraoperative detection of lymph node metastasis in
interim results of a prospective multicenter trial. Ann Surg breast cancer patients. Clin Cancer Res 2007;13:4807e16.
2007;246:568e75. [106] Hughes SJ, Xi L, Raja S, Gooding W, Cole DJ, Gillanders WE,
[89] Kelder W, Braat AE, Karrenbeld A, Grond JA, De Vries JE, et al. A rapid, fully automated, molecular-based assay
Oosterhuis JW, et al. The sentinel node procedure in colon accurately analyzes sentinel lymph nodes for the presence of
carcinoma: a multi-centre study in The Netherlands. Int metastatic breast cancer. Ann Surg 2006;243:389e98.
J Colorectal Dis 2007;22:1509e14. [107] Kawamura YJ, Sakuragi M, Togashi K, Okada M, Nagai H,
[90] Trocha SD, Nora DT, Saha SS, Morton DL, Wiese D, Bilchik AJ. Konishi F. Distribution of lymph node metastasis in T1 sigmoid
Combination probe and dye-directed lymphatic mapping colon carcinoma: should we ligate the inferior mesenteric
detects micrometastases in early colorectal cancer. J Gas- artery? Scand J Gastroenterol 2005;40:858e61.
trointest Surg 2003;7:340e5. [108] Hida J, Okuno K, Yasutomi M, Yoshifuji T, Uchida T, Tokoro T,
[91] Saha S, Dan AG, Berman B, Wiese D, Schochet E, Barber K, et al. Optimal ligation level of the primary feeding artery and
et al. Lymphazurin 1% versus 99mTc sulfur colloid for bowel resection margin in colon cancer surgery: the influ-
lymphatic mapping in colorectal tumors: a comparative ence of the site of the primary feeding artery. Dis Colon
analysis. Ann Surg Oncol 2004;11:21e6. Rectum 2005;48:2232e7.
[92] Cody 3rd HS, Fey J, Akhurst T, Fazzari M, Mazumdar M, [109] Nakafusa Y, Tanaka T, Kitajima Y, Sato S, Hirohashi Y,
Yeung H, et al. Complementarity of blue dye and isotope in Miyazaki K. Modification of lymph node dissection for colon
sentinel node localization for breast cancer: univariate and cancer by clinical diagnosis. Hepatogastroenterology 2004;
multivariate analysis of 966 procedures. Ann Surg Oncol 51:722e6.
2001;8:13e9. [110] Nascimbeni R, Burgart LJ, Nivatvongs S, Larson DR. Risk of
[93] Gershenwald JE, Tseng CH, Thompson W, Mansfield PF, lymph node metastasis in T1 carcinoma of the colon and
Lee JE, Bouvet M, et al. Improved sentinel lymph node rectum. Dis Colon Rectum 2002;45:200e6.
localization in patients with primary melanoma with the use [111] Wang HS, Liang WY, Lin TC, Chen WS, Jiang JK, Yang SH,
of radiolabeled colloid. Surgery 1998;124:203e10. et al. Curative resection of T1 colorectal carcinoma: risk of
[94] Albertini JJ, Cruse CW, Rapaport D, Wells K, Ross M, lymph node metastasis and long-term prognosis. Dis Colon
DeConti R, et al. Intraoperative radio-lympho-scintigraphy Rectum 2005;48:1182e92.
improves sentinel lymph node identification for patients with [112] Kikuchi R, Takano M, Takagi K, Fujimoto N, Nozaki R,
melanoma. Ann Surg 1996;223:217e24. Fujiyoshi T, et al. Management of early invasive colorectal
[95] Miyashiro I, Miyoshi N, Hiratsuka M, Kishi K, Yamada T, cancer. Risk of recurrence and clinical guidelines. Dis Colon
Ohue M, et al. Detection of sentinel node in gastric cancer Rectum 1995;38:1286e95.
surgery by indocyanine green fluorescence imaging: [113] Tominaga K, Nakanishi Y, Nimura S, Yoshimura K, Sakai Y,
comparison with infrared imaging. Ann Surg Oncol 2008;15: Shimoda T. Predictive histopathologic factors for lymph node
1640e3. metastasis in patients with nonpedunculated submucosal
[96] Dan AG, Saha S, Monson KM, Wiese D, Schochet E, Barber KR, invasive colorectal carcinoma. Dis Colon Rectum 2005;48:
et al. 1% lymphazurin vs 10% fluorescein for sentinel node 92e100.
mapping in colorectal tumors. Arch Surg 2004;139:1180e4. [114] Hida J, Yasutomi M, Maruyama T, Fujimoto K, Uchida T,
[97] Mutter D, Rubino F, Sowinska M, Henri M, Dutson E, Okuno K. The extent of lymph node dissection for colon
Ceulemans R, et al. A new device for sentinel node detection carcinoma: the potential impact on laparoscopic surgery.
in laparoscopic colon resection. JSLS 2004;8:347e51. Cancer 1997;80:188e92.

Please cite this article in press as: Cahill RA et al., Localized resection for colon cancer, Surgical Oncology (2008), doi:10.1016/
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