Surgical Oncology 25 (2016) 252e262

Contents lists available at ScienceDirect

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

Review

Complete mesocolic excision and central vascular ligation for colon

cancer: Principle, anatomy, surgical technique, and outcomes
Nam Kyu Kim b, *, Young Wan Kim a, Yoon Dae Han b, Min Soo Cho b, Hyuk Hur b,
Byung Soh Min b, Kang Young Lee b
a
Department of Surgery, Division of Colorectal Surgery, Yonsei University Wonju College of Medicine, Wonju, South Korea
b
Department of Surgery, Division of Colorectal Surgery, Yonsei University College of Medicine, Seoul, South Korea

a r t i c l e i n f o a b s t r a c t

Article history: Classic colon cancer surgery refers to a wide resection of the tumor-bearing segment and the lymphatics
Received 11 April 2016 draining along the named artery. The concept of TME has been applied to colon cancer and complete
Accepted 19 May 2016 mesocolic excision (CME) in conjuction with central vascular ligation (CVL) has been introduced as the
surgical treatment for colon cancer. Here, we discuss appropriate CME procedure with regard to the
Keywords: oncologic backgrounds, essential components, applied anatomy, laparoscopic technique, short-term, and
Colonic neoplasms
oncologic outcomes. The introduction of CME has improved oncologic outcomes greatly in patients with
Mesocolic excision
colon cancer. The improved outcomes with CME can be attributed to underlying sound oncologic
Morbidity
Survival rate
principles such as dissection through the proper plane of mesocolic excision, central vascular ligation,
and sufficient length of proximal and distal margins. Thereby, CME technique can achieve en bloc
removal of the diseased lesion with the increased amount of the colonic mesentery even though the
length of for both bowel and mesentery resection remains a matter of debate. CME is a technically
demanding operation thus, comprehensive understanding of the applied vascular anatomy is essential
for successful CME. Favorable outcomes of open CME have been replicated with a laparoscopic approach.
In future perspective, incorporating a structured education program on minimally invasive (laparoscopy
or robot) CME would be beneficial.
© 2016 Elsevier Ltd. All rights reserved.

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 253
2. Surgical principle of colon cancer . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 253
2.1. Oncologic background of CME . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 253
2.2. Essential components of CME . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 254
2.2.1. The plane of mesocolic excision . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 254
2.2.2. Central vascular ligation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 254
2.2.3. Length of proximal and distal margins . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 254
2.3. Special circumstances . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 255
2.3.1. Metastasis to infrapyloric lymph node and the gastroepiploic arcade . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 255
3. Vascular anatomy and lymphatic system . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 255
3.1. Artery . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 255
3.2. Vein . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 255
3.3. Lymphatics . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 256

Abbreviations: CME, complete mesocolic excision; CVL, central vascular ligation;

SMA, superior mesenteric artery; SMV, superior mesenteric vein; IMA, inferior
mesenteric artery; IMV, inferior mesenteric vein.
* Corresponding author. Department of Surgery, Yonsei University College of
Medicine, 250 Seongsan-ro, Seodaemun-gu, Seoul 120-527, South Korea
E-mail address: namkyuk@yuhs.ac (N.K. Kim).

http://dx.doi.org/10.1016/j.suronc.2016.05.009
0960-7404/© 2016 Elsevier Ltd. All rights reserved.
 N.K. Kim et al. / Surgical Oncology 25 (2016) 252e262 253

4. Preoperative consideration . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 256

4.1. Preoperative staging . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 256
4.2. Indication . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 256
4.3. Preoperative preparation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 256
5. Surgical techniques . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 256
5.1. CME with CVL for right-sided colon cancer . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 256
5.2. CME with CVL for left-sided colon cancer . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 257
5.3. Adjuvant chemotherapy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 258
6. Short-term outcomes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 258
7. Oncologic outcomes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 259
8. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 259
Funding source . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 261
Conflict of interest . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 261
Contributions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 261
Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 261
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 261

1. Introduction and earlier recovery when compared with conventional laparot-

omy [9]. The oncologic safety of laparoscopic surgery has been also
Colorectal cancer is the third most commonly diagnosed cancer confirmed in large randomized clinical trials [10e12]. However,
in men (10.0% of the total cases) and the second in women (9.2% of applying laparoscopy to CME for colon cancer is difficult, mainly
the total cases) with 1,360,000 newly diagnosed patients, world- due to vascular dissection and splenic flexure mobilization [13].
wide [1]. In the United States, it is estimated that 96,830 new cases Accordingly, there is skepticism as to whether favorable outcomes
of colon cancer and 40,000 new cases of rectal cancer in 2014 and of open CME can be reproduced with laparoscopic CME [14e17]. In
proportion of colon cancer comprised over 70% when compared a recent randomized trial, laparoscopic D3 lymphadenectomy for
with rectal cancer [2]. Treatment for colon cancer varies by tumor colon cancer showed short-term surgical safety and clinical bene-
location and stage at diagnosis and, surgery in combination with fits when compared to open surgery [18] and growing number of
selective use of adjuvant chemotherapy are main modalities for papers encourage the use of laparoscopic CME for colon cancer
localized colon cancer. [16,19e21]. Here, we discuss appropriate CME procedure with re-
Rectal cancer surgery has been revolutionized after introduction gard to the oncologic backgrounds, essential components, applied
of total mesorectal excision (TME) by Heald et al. [3] TME removes anatomy, laparoscopic technique, short-term, and oncologic
the rectum and mesorectum as one intact unit by sharp dissection outcomes.
along the mesorectal fascia and the concept of TME has been
applied to colon cancer surgery. Hohenberger et al. [4] firstly
2. Surgical principle of colon cancer
described complete mesocolic excision (CME) in conjuction with
central vascular ligation (CVL) and emphasized the sharp dissection
2.1. Oncologic background of CME
along the mesocolic plane with true central ligation of the main
arteries and veins at their roots. The authors analyzed data of 1329
Metastasis refers to is the secondary tumor growths at a dis-
patients undergoing R0 resection for colon cancer. After the
application of the concept of CME, local recurrence rate decreased tance site from a primary tumor site. The routes of metastases
include lymphatic, hematogenous, disseminated metastasis, and
from 6.5% to 3.6% and 5year cancer related survival rate increased
from 82.1% to 89.1% [4]. The concept of CME was further supported direct invasion to adjacent organs. To date, there are two hypothesis
when metastasis develops [22]. One hypothesis is that metastasis is
by pathologic study. West et al. [5] compared CME specimens with
specimens of standard surgery and observed that CME surgery mainly driven by primary tumor cancer progression thus cancer
metastases occur stepwise pattern. Thus, CME improves outcomes
removed greater area of mesentery and achieved higher resection
rates through the mesocolic plane when compared with standard by removing the mesocolon as one package and high ligation of the
tumor-feeding vessels. The other hypothesis is that metastasis de-
surgeries. The Danish Colorectal Cancer Group showed that CME
surgery yielded better 4year disease-free survival rates when velops independently and progresses simultaneously [23]. Thus,
lymph node metastasis reflects the advanced tumor nature and
compared to conventional non-CME surgery for patients with stage
IeIII colon cancer [6]. extended lymphadenectomy will not improve outcomes. Based on
this, some authors are skeptic over the use of CME for colon cancer
Japanese D3 lymphadenectomy has been performed in many
Asian countries which is based on similar principles to CME with [24]. However, current principle of colon cancer surgery is en bloc
CVL. According to the Japanese Society for Cancer of the Colon and resection of the primary tumor with regional lymph nodes and all
Rectum, D2 lymphadenectomy is defined as removal of D1 lymph grossly suspected or involved lesions should be removed during
nodes (epicolic, paracolic) and D2 nodes (intermediate), and D3 operation.
lymphadenectomy as removal of D3 nodes (main) at the root in The number of lymph nodes retrieved reflects the extent of
addition to D1and D2 nodes [7]. When comparing D3 specimens lymphadenectomy and the increased number of nodes is related to
with CME specimens, both specimens showed higher rates of the favorable survival [25]. CME surgery increased the number of nodes
mesocolic plane surgery and long distances from the high vascular retrieved compared with non-CME surgery [5,26,27]. Improved
tie to the bowel wall [8]. outcomes after CME can be explained partly by the concept of stage
Laparoscopic surgery for colon cancer has clear short-term ad- migration [28]. A sufficient lymph node examination enables ac-
vantages such as less postoperative pain, lower wound infection, curate nodal staging and prognostication. However, the numbers of
nodes are affected by diverse clinicopathological factors such as
254 N.K. Kim et al. / Surgical Oncology 25 (2016) 252e262
gender, tumor location, histologic grade, specimen length, or his-
tologic immune response [29]. Ogino et al. [30] demonstrated
enhanced tumor immune reaction was associated with favorable
survival independent of lymph node count. Thus, it would be
overstating that increased nodal count, itself, after CME surgery
improves survival. We believe that increased lymph node count
may be a byproduct during CME and ultimately, improved out-
comes can be achieved by en bloc resection of a primary tumor and
mesocolon as one package while preserving visceral and retroper-
itoneal mesocolon fascia.
CME surgery removes more mesocolon tissues compared with
non-CME surgery [5,27]. Theoretically, more lymph nodes
harboring isolated tumor cell or micrometastasis (tumor deposits
<2 mm) can be cleared by CME surgery. The presence of occult
metastasis in regional lymph nodes is associated with an increased
risk of recurrence and poor survival in node-negative colorectal
cancer [31]. Baskaranathan et al. [32] observed that 9.25% of pa-
tients had free cancer cells on the peritoneal surface and the
presence of free cancer cells correlated poor cancer-specific sur-
vival in colorectal cancer. CME removes greater area of mesentery
while preserving mesocolon integrity [5,27]. Thus, CME may
remove more free tumor cells on peritoneal surface and reduce
potential sources of disease recurrence.
2.2. Essential components of CME
To date, the detailed surgical treatment for colon cancer is still
different among the nations and surgeons [4,8,27,33,34]. In Japan,
lymph nodes in the mesocolon are grouped based on their locations
and D3 lymphadenectomy, which removes principal lymph nodes
along the major artery, is recommended for clinically node-positive
disease [7]. D3 lymphadenectomy for colon cancer is a widely
accepted surgical procedure in Asian countries, including Korea and
China as well as Japan [35] and systematic regional lymphade-
nectomy has been performed for therapeutic purpose rather than
staging. Although there is some differences of the extent of surgery
between CME and D3 lymphadenectomy, we believe that these two
surgical techniques share common characteristics with regard to
excellent oncologic outcomes [4,5,8,21,36].
The original CME technique emphasized meticulous dissection
between the mesocolon and retroperitoneum along the Toldt’s
fascia and retrieval of the specimen as one unbreached mesocolon
package. The CME surgery should be performed with techniques of
central vascular ligation (CVL) to clear all locoregional lymph nodes.
In addition, adequate proximal and distal margins should be ob-
tained (Table 1).
2.2.1. The plane of mesocolic excision
The plane of mesocolic excision is classified into: (1) a muscu-
laris propria plane means a poor plane of surgery; (2) an intra-
mesocolic plane means a moderate plane of surgery; and (3) a
mesocolic plane means a good plane of surgery [26]. The rate of
mesocolic surgery was higher after CME surgery (89%) compared
with non-CME surgery (47%) [27]. West et al. [37] demonstrated
that a mesocolic plane of surgery improved survival in stage III
colon cancer. A mesocolic plane surgery produces a good-quality
specimen which shows a good bulk of mesocolon with a smooth
surface with no or only minor visceral fascia defects. Thus, the
primary tumor with its vasculatures and lymphatics is removed
uninjured. Poor quality surgery such as a muscularis propria plane
surgery inevitably produces defective specimen and it is likely to
result in tumor cell spillage through major or multiple defects of
the specimen or leave a remnant disease.
Recently, a number of investigators studied the anatomy and
multi-layered fascial structures of mesocolon and raised issues of
standardization of nomenclature [38e47]. Mike and Kano [43]
proposed that the concept of a fusion fascia which is formed by
fusion of the peritoneum and the mesentery after intestinal rota-
tion during the fetal period. Accordingly, the authors suggested that
current nomenclatures of fascial structures such as the visceral
peritoneum (fascia) and the parietal peritoneum (fascia) need to be
replaced with the fusion fascia of the colon and the deep sub-
peritoneal fascia, respectively. In addition, appropriate dissection
plane should be between the fusion fascia of the colon (Toldt’s
fascia) and the deep subperitoneal fascia. Culligan et al. [41]
investigated histologic and electron microscopic structures of the
mesocolon. In the ascending, descending, and apposed sigmoid
mesocolons, the mesocolonic layered structures were surface
mesothelium, mesocolon, deep mesothelium, Toldt’s fascia, retro-
peritoneal mesothelium, and retroperitoneum (from dorsal to
ventral side). Thus, Culligan et al. [39] described that i.e. during left
colectomy, surgical dissection plane can be either between the
mesocolon and Toldt’s fascia (mesofascial separation) or between
the Toldt’s fascia and retroperitoneum (retrofascial separation).
These nomenclatures are not familiar to most surgeons however, to
be popularized the CME principle, the surgical anatomy of the
mesocolon and proper dissection plane need to be re-scrutized in
future studies.
2.2.2. Central vascular ligation
Apical (central or D3) lymph node metastasis has been reported
0e11.1% in patients with right-sided colon cancer (the cecum,
ascending colon, and hepatic flexure) [48,49]. The incidence of
metastatic lymph nodes at the origin of the inferior mesenteric
artery has been reported to 0.3e8.6% in patients with left-sided
colon and rectal cancer [50]. Skip metastasis from epicolic node
(pericolic or D1) to main node (apical or D3) has been reported
0.8%e2% [51e54].CME surgery increased the distance between
tumor to high tie and bowel to high tie [5,26,27]. Central ligation of
main supplying vessels reduces a risk of residual metastatic lymph
nodes and enables accurate staging and prognostication. Kotake
et al. [55] observed that and D3 lymphadenectomy for T3 and T4
colon cancer was superior to D2 lymphadenectomy in terms of
overall survival. Survival benefit was also seen in patients without
lymph node metastasis. They postulated that removal of micro-
metastasis in the main nodes may improve survival.
2.2.3. Length of proximal and distal margins
Unlike mesocolic plane and central ligation, there is no objective
boundaries for proxiaml and distal resection margins. Mesocolic fat
is more prominent around major vessels and that creates a bulky
vascular pedicle [38]. Although there is some difference, CME
technique favors the 10 cm-rule for proximal and distal margins
[54]. Epicolic and paracolic nodes metastases occur along the
marginal artery and thereafter tumor spreads to the intermediate
and apical lymph nodes along the main supplying artery [49]. Thus,
sufficient proximal and distal margins are needed to remove the
mesocolon containing lymph nodes and thereby improve oncologic
outcomes.
Interestingly, the bowel lengths appear to be sufficient even in
non-CME surgery in the actual reported data. West et al. [5] re-
ported that mean length of large bowel for right-sided colon cancer
was 26.5 cm after CME and 18.3 cm after non-CME surgery. For left-
sided colon cancer, mean length was 39.2 cm after CME and 26 cm
after non-CME surgery. The length of bowel resected and the
amount of mesocolon containing lymph nodes are closely interre-
lated, thus it is difficult to assess direct impact of bowel length on
outcomes. However, it may be valuable to rescrutinize the tradi-
tional 10 cm-rule for proximal and distal margins and investigate
optimal small bowel and colonic lengths for colon cancer in this
 N.K. Kim et al. / Surgical Oncology 25 (2016) 252e262 255

Table 1
Specimen quality after complete mesocolic excision (CME) surgery for colon cancer.

Author, year N Mesocolic Specimen length (cm) Tumor to high tie (mm) Area of mesentery (mm2) Lymph nodes (number)
planea (%)

West [5], 2010 CME:49 NR Rt colon ¼ CME:34.8b Rt colon ¼ CME:129b Rt colon ¼ CME:16,770b CME:30b
Non- Non-CME:24.4 Non-CME:81 Non-CME:8881 Non-CME:18
CME:40 Lt colon ¼ CME:39.2b Lt colon ¼ CME:145b Lt colon ¼ CME:24,128b
Non-CME:26.0 Non-CME:97 Non-CME:13,166
Bertelsen [26], CME:93 CME:82 NR CME:96b NR CME:26.7b
2011 Non- Non-CME:80 Non-CME:71 Non-CME:24.5
CME:105
West [8], 2012 CME:136 CME:88 Rt colon ¼ CME:33.4, D3:21.3 Rt colon ¼ CME:118b, Rt colon ¼ CME:15,533b,D3:7620 Rt colon ¼ CME:32b, D3:24
D3:118 D3:73 Transverse colon ¼ CME:41.1, D3:100 Transverse colon ¼ CME:22,367b, Transverse
D3:25.2 Transverse D3:12,548 colon ¼ CME:36b, D3:20
Lt colon ¼ CME:38.2b, colon ¼ CME:107, D3:110 Lt colon ¼ CME:18,551b, D3:8413 Lt colon ¼ CME:25b, D3:16
D3:15.4 Lt colon ¼ CME:126, D3:122
Kobayashi [27], Non- Non-CME:47 Rt colon ¼ Non-CME:19.5 Rt colon ¼ Non-CME:81 Rt colon ¼ Non-CME:11,902 Non-CME:16
2014 CME:19 CME:89 CME:30.5b CME:115b CME:17,641b CME:31b
CME:26 D3:72 D3:18.4 D3:103 D3:8705 D3:21
D3:60 Lt colon ¼ Non-CME:22 Lt colon ¼ Non-CME:100 Lt colon ¼ Non-CME:13,775
CME:35.5b CME:128b CME:17,762b
D3:14.6 D3:120 D3:7807

NR, not reported.

a
The plane of surgery is classified into: (1) a muscularis propria plane means a poor plane of surgery; (2) an intramesocolic plane means a moderate plane of surgery; and (3)
a mesocolic plane means a good plane of surgery.
b
Statistically significant.

CME era. 3.1. Artery

2.3. Special circumstances
2.3.1. Metastasis to infrapyloric lymph node and the gastroepiploic
arcade
Incidence of infrapyloric nodal metastasis has been reported
1.1e4% in hepatic flexue or proximal transverse colon cancer
[48,56,57]. Proposed mechanism is a presence of aberrant vessels
or embryonic connection between the colonic flexure, the omen-
tum, and the head of pancreas [54,58]. When suspected, central
ligation of the right gastroepiploic artery and vein is necessary to
remove the gastroepiploic and infrapyloric lymph nodes [4].
However, routine application of infrapyloric node removal is
controversial in hepatic flexue or proximal transverse colon cancer.
Metastasis to the gastroepiploic arcade is seen in 4%e5% of trans-
verse and splenic flexure cancer [4,54]. Hohenberger et al. [4]
described the ‘arcade principle’ which consists of removal of
about 10 cm of the corresponding gastroepiploic arcade and of the
infrapancreatic nodes.
We believe that central ligation of the main feeding vessels,
sharp dissection preserving mesocolonic integrity, and sufficient
proximal and distal margins can lead to favorable oncologic out-
comes when compared to traditional colon cancer surgery. In
addition, tumor-specific CME should be pursued for right-sided
colon cancer. Accordingly, it should be differentiated CME for the
cecum or the proximal ascending colon (CME for right hemi-
colectomy) and for the distal ascending colon, the hepatic flexure or
the proximal transverse colon (CME for extended right
hemicolectomy).
3. Vascular anatomy and lymphatic system
It is important to understand vascular anatomy to perform
surgically and oncologically safe CME surgery for colon cancer. In
particular, minimally invasive approaches such as laparoscopy and
robotics have prompted to get a renewed attention on frequent
anatomic variations of the branching vessels from the superior
mesenteric artery (SMA), superior mesenteric vein (SMV), inferior
mesenteric artery (IMA) and inferior mesenteric vein (IMV).
The midgut (the entire small intestine to proximal two-thirds of
transverse colon) is supplied by the SMA and the hindgut (the distal
third of transverse colon to rectum) is supplied by the IMA [59]. The
SMA branches off two or three major colonic arteries to the right.
The ileocolic artery is constantly present and the right colic artery
arising from the SMA is highly variable and present in 0%e63.3% of
cadavers [60e62]. The right colic artery may arise from the ileocolic
or middle colic artery [63]. The middle colic artery is divided into
two branches (right and left). Anatomic variations of the middle
colic artery include complete absence in up to 25% of cases and the
presence of an accessory (up to 10%) or double middle colic artery
[59,64].
Topography of the ileocolic artery and right colic artery toward
the SMA is important for vascular ligation for right-sided colon
cancer. The ileocolic artery runs anterior to the SMV in 17%e83% of
specimens [61e63,65]. The right colic artery, if present, crosses
anteriorly in 63%e100% of specimens [61e63,65].
The IMA originates from the ventral side of the abdominal aorta
about 3 cme6.3 cm above the aortic bifurcation [66]. The IMA gives
off the left colic artery, 2 to 6 sigmoid branches, and the superior
rectal (hemorrhoidal) artery. Sigmoid branches may arise from the
left colic artery or superior rectal artery [67].
3.2. Vein
The venous drainage follows the arterial anatomy. Venous blood
from the cecum to proximal transverse colon drains into the SMV.
Drainage from the distal transverse colon to most part of the
rectum is directed to the IMV. Clinically, the venous anatomy of the
right colic vein, superior right colic vein, gastrocolic trunk, and the
middle colic vein is highly variable and of interest. Understanding
of these anatomic variation may prevent inadvertent vein injury
during CME for right-sided colon cancer.
Gastrocolic trunk of Henle refers to the confluence of the right
gastroepiploic vein, superior right colic vein, and anterior superior
pancreaticoduodenal vein [68]. A gastrocolic trunk is present in
46%e70% of individuals [68e70]. Yamaguchi et al. [69] observed
that the right colic vein drained into the SMV directly in 56% and
256 N.K. Kim et al. / Surgical Oncology 25 (2016) 252e262
into the gastrocolic trunk in 44%. The middle colic vein entered into
the SMV directly in 84.5% of individuals and into the gastrocolic
trunk in 12.1% of specimens. Anomalous drainage of the middle
colic vein was observed in two individuals (drainage into the
splenic vein and the IMV).
3.3. Lymphatics
Lymphatics are drained along the course of the arterial anatomy.
The colonic wall has an abundant network of lymphatic capillaries
that is drained into extramural lymphatics following the arterial
supply [59]. Lymph nodes are classified into epicolic, paracolic,
intermediate, and main nodes depending on their location. Epicolic
nodes are located in the appendices epiploicae. Paracolic nodes are
located along the marginal artery. Intermediate nodes are located
along the major arterial branches supplying the colon. Main nodes
are located at the origin of the SMA or of IMA.
Main nodes are positioned on the ventral side of the SMV and
the lymphatic channels run through anteriorly toward the SMA
[48]. If the ileocolic artery courses behind the SMV, high ligation at
the root of the SMA may increase nodal gain [65]. However, Japa-
nese surgeon suggested that the ligation of the ileocolic artery at
the level of SMV may not jeopardize oncologic principle [54].
4. Preoperative consideration
4.1. Preoperative staging
Preoperative staging modalities include colonoscopy with bi-
opsy, abdominopelvic computed tomography (CT) scan, and/or
positron emission tomography. In suspected cases, chest CT scan is
performed to rule out thoracic organ metastases. There is still space
for improvement in determining T (depth of tumor invasion) and N
(nodal involvement) staging by CT scan. A recent meta-analysis
showed that sensitivity and specificity of CT was 86% and 78%
when differentiating tumor invasion, and 70% and 78% when
identifying nodal metastasis [71].
4.2. Indication
D3 dissection is generally recommended in patients with clin-
ical stage II/III disease [7,72]. To date, there is limited evidence with
regard to D3 dissection for early-stage colon cancer such as cT2N0
stage. According to the Japanese guideline, D2 dissection as well as
D3 are all acceptable in cT2N0 disease. We think that CME with CVL,
which is similar to D3 dissection, may be useful even in cT2N0
disease because preoperative imaging still has limited accuracy and
D3 dissection can provide more accurate pathologic staging.
Laparoscopic CME takes longer operative time and is technically
difficult. Thus, a laparoscopy can be selected as a primary approach
when patients have the following clinical features: sufficient he-
modynamic stability to tolerate CO2 pneumoperitoneum, non-
emergent settings, or lack of adhesion from prior extensive
abdominal surgery. An open approach can be selected when en bloc
resection is difficult based on preoperative CT imaging or when
patients have a large tumor (larger than 6e8 cm) or extensive
infiltrative tumor to the adjacent organs [33].
4.3. Preoperative preparation
Patients with colon cancer do not receive any mechanical bowel
preparation and oral antibiotics. Patients are fasted only from
midnight the night before the surgery and a glycerin enema is
performed once or twice before the surgery. First-generation
cephalosporin is used as a prophylactic antibiotic and was
administered just before the start of surgery. Postoperative anti-
biotic treatment is continued for 24e48 h. Low molecular weight
heparin is administered for venous thromboprophylaxis, if
necessary.
5. Surgical techniques
The concept of CME procedure includes sharp dissection be-
tween the visceral and parietal fascia layers with full mobilization
of the apposed mesocolon, and central ligation of the supplying and
draining vessels at their origin. The CME procedure emphasizes
longitudinal (or horizontal) removal, vertical removal, and
circumferential removal. The extent of the resection varies by tu-
mor location and we discuss CME surgeries for right-sided and left-
sided colon cancers, respectively.
5.1. CME with CVL for right-sided colon cancer
Various laparoscopic and open techniques are introduced in
precious literature for performing CME with CVL for right-sided
colon cancer. Laparoscopic approach is performed under the
same CME principle as for laparotomy. For laparoscopic CME, one
10 mm port is utilized for a camera at the umblicus and three
working ports (the left upper: 5 mm or 12 mm port, left lower:
5 mm port, and right lower quadrants: 5 mm port). Another 5 mm
port at the right upper quadrant is utilized in difficult cases. After
placement of the trocars, the patient is placed in a Trendelenburg
with right side up position.
A medial to lateral dissection is advocated in most cases, but
when the origin of ileocolic pedicles are not clearly identified, the
dissection is alternated with lateral to medial fashion. The detailed
procedures of ‘A medial to lateral dissection’ are as follows: The
terminal ileum and the ascending colon are dissected off through
the embryological plane. Dissection between the mesocolon and
Gerota’s fascia continues to the duodenum and head of the
pancreas. Once the ileocolic vessels are identified, the mesocolon
package containing lymph nodes is cleared along the vessels while
exposing the ventral side of the SMV and SMA. The ileocolic vessels
are ligated at the root of the SMV and SMA, and the dissection
continues cephalad to the right colic vessels, the gastrocolic trunk
of Henle, and the middle colic vessels. The right colic vessels, if
present, are skeletonized and transected at the root. The gastrocolic
trunk has a number of anatomic variations, and careful dissection is
necessary to avoid unwanted vascular injury. Unless infiltrated by
tumor, the anterior superior pancreaticoduodenal vein and right
gastroepipoloic vein are preserved, and only the right colic and/or
superior right colic vein are transected. Then, the middle colic
vessels are identified and skeletonized at the roots of the SMA and
SMV.
Tumor-specific CME is performed according to the tumor loca-
tion. For cecal and proximal ascending colon cancers, right hemi-
colectomy is performed and the right branches of the middle colic
artery and vein are ligated. For hepatic flexure and proximal
transverse colon cancers, extended right hemicolectomy is per-
formed and the roots of the middle colic artery and vein are ligated.
The Kocher maneuver was not performed routinely. Omentectomy
is performed just below the gastroepiploic vessels and, unless
infiltrated by the tumor, right gastroepiploic vessels are preserved.
(Figs. 1 and 2). The mobilized colon is exteriorized through um-
bilical minilaparotomy and transected with adequate resection
margin. Extracorporeal stapled or hand-sewn anastomosis is per-
formed and one closed suction drain is placed.
On the other hand, the basic principle of ‘A lateral to medial
dissection’ is initiated retroperitoneal mobilization between
embryologic planes of parietal and visceral fascia of mesocolon,
 N.K. Kim et al. / Surgical Oncology 25 (2016) 252e262
Fig. 1. Overview of complete mesocolic excision with central vascular ligation in right-sided colon.
followed by dissection vertically along superior mesenteric vessels
ligating ileocolic, right colic and middle colic pedicles. First, the
small bowel is retracted to the left, and a retroperitoneal plane is
identified and continued laterally using adequate retraction. The
embryological avascular plane between the mesocolon and retro-
peritoneal essential structures such as right ureter, right gonadal
vessels and right kidney is developed by sharp dissection. The plane
is then extended superiorly below Gerota’s fascia and medially to
the retroperitoneal adhesions with the third portion of the duo-
denum. Maintaining tension during lateral retraction of the cecum
resulted in better identification of vascular anatomy, and a perito-
neal window was made safely on the mesentery along the flow of
the ileocolic pedicles to the superior mesenteric vessels. After
clearing of lymph nodes bearing areolar tissue on the SMV, the
origin of ileocolic vessels are completely exposed. Ileocolic vessels
are then divided and ligated, and the remaining attachment to
duodenum is released. Careful sharp dissection along the SMV is
continued up to the root of the middle colic vessels. After complete
removing lymph node-bearing tissue around the origin of middle
colic artery, each branch of middle colic artery is clearly skeleton-
ized. The level of arterial ligation should be performed according to
the tumor location. The vein is subsequently ligated in the same
manner. For gastrocolic ligament division, caudal retraction of the
transverse colon is essential. Division of the gastrocolic ligament
along the right gastroepiploic vessels was continued, and a fusion
257
plane of the duodenum and transverse colon was separated by
sharp dissection. Finally, in particular patient, Gerota’s fascia and
perinephric fat should be included in the specimen. This procedure
is important to evaluate the possibility of circumferential resection
margin positivity.
5.2. CME with CVL for left-sided colon cancer
For laparoscopic CME, one 10 mm port is utilized for a camera at
the umblicus and three working ports (the right lower: 5 mm or
12 mm port, right upper: 5 mm port, and left lower quadrants:
5 mm port). Another 5 mm port at the left upper quadrant is uti-
lized in difficult cases. After placement of the trocars, the patient is
placed in a Trendelenburg with left side up position.
CME procedure is initiated by incising the medial side of the
sigmoid mesocolon at the level of the sacral promontory and
medial to lateral mobilization is continued through the avascular
plane. With adequate traction, the IMA is lifted up and skeletonized
with caution not to damage the superior hypogastric plexus around
the aortic bifurcation. After complete clearance of lymph nodes
around the root of the IMA, the IMA or left colic artery is ligated at
the origin depending on the type of procedure planned (left hem-
icolectomy or anterior resection). The ureter and gonadal vessels
are identified with further medial to lateral dissection and pre-
served. The IMV is lifted up and dissected cephalad to the ligament
258 N.K. Kim et al. / Surgical Oncology 25 (2016) 252e262
Fig. 2. Embryological avascular plane, gastrocolic trunk, and ligated ileocolic pedicles at the origin of superior mesenteric vessels were seen under the parietal fascia.
of Treitz, and ligated at the lower border of the pancreas. Retro-
peritoneal space is developed between the mesocolon and Gerota’s
fascia. Root of the transverse mesocolon is freed from the lower
border of the pancreas and entering the lesser sac by dissection
through the ventral side of the pancreas. After completing medial
colonic mobilization, the left lateral paracolic attachments are
lysed. Dissection continues to the lower pole of the spleen and
splenocolic ligament is dissected. Omentectomy is performed just
below the gastroepiploic vessels and, unless infiltrated by the tu-
mor, left gastroepiploic vessels are preserved. The embryologic
adhesion is cleared up between the stomach and the transverse
mesocolon and the lesser sac is identified. Continued dissection to
the dorsal and lateral side joins the previously dissected surgical
planes.
Tumor-specific CME is performed according to the tumor loca-
tion. For proximal descending colon cancers, the root of the IMA is
preserved and the left colic artery and superior rectal artery are
ligated at its origin from the IMA. For mid descending and sigmoid
colon cancers, the root of the IMA is ligated and the root of the IMV
is ligated just below the lower border of the pancreas. The mobi-
lized colon is exteriorized through umbilical minilaparotomy and
transected with adequate resection margin. Extracorporeal stapled
or hand-sewn anastomosis is performed and one closed suction
drain is placed.
5.3. Adjuvant chemotherapy
After recovery from surgery, chemotherapy is recommended for
patients with stage II and III disease according to National
Comprehensive Cancer Network (NCCN) guidelines [73]. Chemo-
therapy regimens include fluoropyrimidine (fluorouracil with
folinic acid, capecitabine) alone, or in combination with oxaliplatin
(FOLFOX). Stage II patients with high-risk pathologic or clinical
features (T4, histologic grade 3 or 4, lymphovascular involvement,
bowel obstruction, T3 lesions with localized perforation, positive
resection margin, or perineural invasion) are candidates for
oxaliplatin-containing regimens.
6. Short-term outcomes
During CME for colon cancer, exposure and dissection along the
major vascular pedicles for CVL is quite difficult, leading to concerns
 N.K. Kim et al. / Surgical Oncology 25 (2016) 252e262 259

over prolonged operative time and increased postoperative
complication rates. Mean operative time ranged from 156 min to
178 min [74e76] and operative time of CME is longer compared
with non-CME surgery [74,76]. Postoperative morbidity rate ranged
from 11% to 28% [4,74e78] but did not differ between CME and non-
CME surgery [76,78] (Table 2).
When comparing laparoscopic and open CME, mean operative
time after laparoscopic CME ranges from 136 min to 269 min
[16,18e21,34,79e83] and most studies reported prolonged opera-
tive time in the laparoscopic CME group [18,80,82]. Bae et al. [19]
and Huang et al. [83] reported similar operative time between
the laparoscopic and open CME groups. Postoperative complication
rate ranged from 8.3% to 30.8% and it did not differ between the
laparoscopic and open CME groups [19,33,82]. Two studies showed
lower morbidity rates in the laparoscopic CME group [18,80]. In
addition, shorter time to soft diet [19,80,82] and reduced length of
stay [18,19,80] have been reported with laparoscopic CME. Rate of
conversion to open CME ranged from 1.9% to 10.4%
[16,18,19,33,80,82] in the literature. Recently, Yamamoto et al. [18]
performed a randomized controlled trial comparing laparoscopic
(n ¼ 533) and open D3 dissection (n ¼ 524) for clinical stages II/III
colon cancer. Conversion to open surgery occurred in 29 (5.4%)
patients. Laparoscopic CME showed longer operative time (211 min
vs. 153 min). However, short-term advantages were observed in
terms of less blood loss, shorter time to flatus, diminished analge-
sics use, shorter length of stay, and lower postoperative complica-
tion rate (14.3% vs. 22.3%) (Table 3).
Based on these results, CME can be safely performed compared
with non-CME surgery. Although laparoscopic CME is a technically
demanding procedure and requires a steep learning curve due to
technical difficulty [14], this approach may confer short-term ad-
vantages such as lower complication rates, shorter time to diet, and
reduced hospital stay.
7. Oncologic outcomes
Hohenberger et al. [4] reported excellent cancer-specific sur-
vival rates after CME surgery (stage I: 99.1%, stage II: 91.4%, and
stage III: 70.2%). Bertelsen et al. [6] performed a retrospective,
population-based study (n ¼ 1395) and demonstrated CME is
oncologically superior to non-CME surgery in terms of 4year
disease-free survival (CME: 85.8% vs. non-CME: 75.9%). Kotake et al.
[55] compared D2 and D3 lymphadenectomy for T3 and T4 colon
cancer and suggested that D3 lymphadenectomy reduced 18% of
relative risk for overall survival. Nagasaki et al. [84] investigated the
prognostic impact of lymph node location in patients undergoing
CME with CVL for stage III colon cancer. The authors demonstrated
that the lymph node location such as pericolic, intermediate, and
main lymph nodes was associated with accurate prognostication. In
the pathologic N1 group, the recurrence-free survival of patients
with pericolic node metastasis (84.4%) was significantly better than
that of patients with intermediate or main node metastases (71.5%).
Similarly, in the pathologic N2 group, the recurrence-free survival
of patients with epicolic node metastasis (72.6%) was significantly
favorable than that of patients with intermediate or main node
metastasis (53.1%).
When comparing laparoscopic and open CME, similar overall
survival (laparoscopy:70.4% vs. open: 67%) [80] and recurrence
rates (laparoscopy: 8.6% vs. open: 9.1%) [82]. Cho et al. [33] reported
simliar overall and disease-free survival rates between the mini-
mally invasive approaches (laparoscopy and robot) and open CME.
Interestingly, Bae et al. [19] reported a better overall survival rate in
the laparoscopic CME group, but numerous multicenter trials have
failed to show better oncologic outcomes after laparoscopic colon
cancer surgery [11,12,85]. Accordingly, a potential favorable impact
of laparoscopic CME on prognosis needs to be further investigated
(Table 4).
8. Conclusions
The introduction of CME has improved oncologic outcomes
greatly in patients with colon cancer. The improved outcomes with
CME can be attributed to underlying sound oncologic principles
such as dissection through the proper plane of mesocolic excision,
central vascular ligation, and sufficient length of proximal and
distal margins. Thereby, CME technique can achieve en bloc
removal of the diseased lesion with the increased amount of the
colonic mesentery. CME is a technically demanding operation thus,

Table 2
Short-term and oncologic outcomes after extended lymphadenectomy including complete mesocolic excision (CME) for colon cancer.

Author, year Study Characteristics N Colon OT (min) Cx (%) LN AC (%) Survival (%)
period cancer

Tagliacozzo 1979 Standard (SL) vs. extended (EL) SL:84 Rt SL:145a SL:10 SL:12a 0 5year-OS ¼ SL:62.8 vs.
[76],1997 e1989 lymphadenectomy EL:60 EL:156 EL:12 EL:22 EL:64.3
Bokey [86], 2003 1971 Non-standardized (NS) vs. standardized NS:210 Rt,Lt NR NR NR 0 5year-CSS ¼ NS:66.4 vs.
e1995 surgery (SS) SS:657 SS:76.6a
Tentes [78], 1993 Conventional (CS) vs. radical lymph CS:62 Lt NR CS:18 NR CS:28 5year-CSS (Stage III) ¼ CS:19
2007 e2002 node resection (LND) LND:62 LND:11 LND:30 vs. LND:70a
Hohenberger 1978 CME 1329 Rt,Lt NR 19.7 32 5.6 5year-CSS¼I:99.1, II:91.4,
[4], 2009 e2002 III:70.2
Pramateftakis 1989 CME 115 Rt NR 14 NR 72 5year-OS ¼ 72.4
[77], 2010 e2008
Kanemitsu [75], 1990 D3 370 Rt 165 28 31 31 5year-OS¼I:100, II:94.5,
2013 e2003 III:85
Galizia [74], 2004 non-CME (NCME) vs. CME NCME:58 Rt NCME:130a NCME:12 NCME:15a NCME:25 5year-CSS ¼ NCME:74 vs.
2014 e2012 CME:45 CME:178 CME:13 CME:20 CME:21 CME:90
Kotake [55], 1985 D2 vs. D3 for pT3 or pT4 cancer D2:3425 Rt,Lt NR NR D2:15 D2:67 D3 ¼ a relative risk
2014 e1994 D3:3425 D3:22 D3:66 reduction (18%)
Bertelsen [6], 2008 non-CME (NCME) vs. CME NCME:1031 Rt,Lt NR NR NCME:21a (Stage III) 4year-DFS ¼ NCME:75.9 vs.
2015 e2011 CME:364 CME:37 NCME:70 CME:85.8a
CME:74

OT, operative time; Cx, postoperative complication; LN, number of lymph node examined; AC, adjuvant chemotherapy; NR, not reported; OS, overall survival; CSS, cancer-
specific survival; DFS, disease-free survival.
a
Statistically significant.
260 N.K. Kim et al. / Surgical Oncology 25 (2016) 252e262

Table 3
Short-term outcomes after laparoscopic complete mesocolic excision (CME) for colon cancer.

Author, year Study period Technique N Colon cancer OT (min) Conv (%) Diet (day) LOS (day) Cx (%) Comments

Adamina [16], 2012 2005e2010 CME L:52 Rt 136 1.9 NR 3 30.8

Feng [79], 2012 2010e2011 D3 L:35 Rt 150 NR 3 12 8.6 Specimen quality
Han [80], 2014 2003e2010 D3 O:147 Rt O:110a 2.8 O:6a O:17a O:22.5a
L:177 L:133 L:3 L:10 L:13
Shin [20], 2014 2006e2009 D3 L:168 Rt,Lt 196 NRb 2 9 17.8
Liang [34], 2014 2003e2008 D3 L:244 Rt 224 NR NR 11 16
Bae [19], 2014 2006e2008 CME O:85 Rt O:194 6.6c O:7a O:13a O:21 Chyle leakage (%); O:14.1a vs. L:3.5
L:85 L:179 L:6 L:7 L:11
Yamamoto [18], 2014 2004e2009 D3 O:524 Rt,Lt O:159a 5.4 NR O:11a O:22.3a Randomized controlled trial
L:533 L:211 L:10 L:14.3
Zhao [82], 2014 2008e2011 D3 O:57 Rt O:171a 10.4 O:5a O:11 O:19.3
L:48 L:244 L:4 L:10 L:12.5
Siani [81], 2014 2008e2013 CME L:115 Rt 179 NR 3 11 22.6 Specimen quality
Mori [21], 2015 2010e2013 CME L:31 Rt 269 NR NR 13 9.7 Specimen quality
Cho [33], 2014 2000e2009 CME O:568 Rt NR 2.0 NR O:15a O:8.8
MIS:205 MIS:10 MIS:8.3
Liang [87], 2015 1994e2004 CME O:879 Rt,Lt NR NR NR 7 13.5
L:134

OT, operative time; Conv, conversion to open surgery; Diet, time to diet; LOS, length of stay; Cx, postoperative complication; L, laparoscopy; O, open surgery; MIS, minimally
invasive surgery; NR, not reported.
a
Statistically significant.
b
Converted cases were excluded before the study.
c
Before propensity score matching.

Table 4
Pathologic and oncologic outcomes after laparoscopic complete mesocolic excision (CME) for colon cancer.

Author, year TNM Plane of surgery PRM (cm) DRM (cm) Specimen length LN AC (%) Survival (%)
(%)a (cm)

Adamina [16], IeIII NR 12 12 NR 22 25 Median OS:38months,

2012 DFS:37months
Feng [79], 2012 IeIII MCP:100 NR NR 18.3 19 NR NR
Han [80], 2014 IeIII NR NR NR NR O:11b O:75c 5year-OS ¼ O:67 vs. L:70.4
L:15 L:83
Shin [20], 2014 II,III NR AsC:13,TC:22,DC/ AsC:16,TC:14,DC/ NR 27.8 FOLFOX4: 5year-CSS:95.5, DFS:88.3
SC:15 SC:7 92.6%c
Liang [34], 2014 Clinical NR NR NR NR 34.4 NR 5year cumulative recurrence rate:
III 16.6%
Bae [19], 2014 IeIII NR NR NR NR O:28 O:75 5year-OS ¼ O:77.8 vs. L:90.3
L:27 L:81 5year-DFS ¼ O: 71.8 vs. L:83.3
Yamamoto [18], 0eIV NR NR NR NR O:22 NR NR
2014 L:21
Zhao [82], 2014 IeIII NR O:17 O:15 NR O:17 NR Recurrence rate ¼ O:9.1 vs. L:8.6
L:17 L:14 L:17
Siani [81], 2014 IeIII MCP:65 NR NR MCP:24 MCP:31 NR 5year-OS ¼ MCP:82.6, IMP:72, MPP:
IMP:22 IMP,MPP:21 IMP:29 60
MPP:13 MPP:25 5year-DFS ¼ MCP:73.8, IMP:59.7,
MPP:46.6
Mori [21], 2015 IeIV MCP:84 NR NR Colon length: 21.8 25 NR NR
IMP:16
Cho [33], 2014 IeIII NR 16 16 NR O:35.4 80 5year-OS ¼ O:82.4 vs. MIS:89.8
MIS:28.9 (oxaliplatin:28) 5year-DFS ¼ O:82.0 vs. MIS:82.9
c
Liang [87], 2015 IeIII NR NR 12 NR 28.3 80 5year-CSS:83.6
5year-LRFS: 94.9

TNM, tumor-node-metastasis; PRM, proximal resection margin; DRM, distal resection margin; LN, number of lymph nodes examined; AC, adjuvant chemotherapy; NR, not
reported; L, laparoscopy; O, open surgery; OS, overall survival; CSS, cancer-specific survival; DFS, disease-free survival; AsC, ascending colon; TC, transverse colon; DC,
descending colon; SC, sigmoid colon; MCP, mesocolic plane; IMP, intramesocolic plane; MPP, muscularis propria plane; MIS, minimally invasive surgery; LRFS, local
recurrence-free survival.
a
The plane of surgery is classified into: (1) a muscularis propria plane means a poor plane of surgery; (2) an intramesocolic plane means a moderate plane of surgery; and (3) a
mesocolic plane means a good plane of surgery.
b
Statistically significant.
c
Stage III disease.

comprehensive understanding of the applied anatomy is essential
for successful CME. Favorable outcomes of open CME have been
replicated with a laparoscopic approach. However, the debate
about the technical feasibility and optimal extent of surgery
regarding CME technique is still ongoing. International prospective
observational cohort study for colon cancer surgery, so called T-REX
study, is currently underway to establish optimal bowel resection
extent and appropriate central lymph node dissection in Japan,
Korea, Germany and United Kingdom. The T-REX study will hope-
fully help to clarify these issues in the future. Finally, incorporating
a structured education program on minimally invasive (laparos-
copy or robot) CME would be beneficial.
 N.K. Kim et al. / Surgical Oncology 25 (2016) 252e262
Funding source
None.
Conflict of interest
None.
Contributions
Study concept and design: NK Kim, YW Kim, YD Yoon, MS Cho.
Acquisition and interpretation of data: NK Kim, YW Kim, MS
Cho, BS Min, KY Lee.
Drafting of the manuscript: NK Kim, YW Kim, YD Yoon, MS Cho,
BS Min, KY Lee.
Critical revision of the manuscript: NK Kim, YW Kim, MS Cho, H
Hur, BS Min.
All authors have approved the final article.
Acknowledgements
The authors are deeply grateful to Dong-Su Jang, MFA, (Medical
Illustrator, Medical Research Support Section,Yonsei University
College of Medicine, Seoul, Korea) for his outstanding medical
illustrations.
References
[1] J. Ferlay, I. Soerjomataram, R. Dikshit, S. Eser, C. Mathers, M. Rebelo, et al.,
Cancer incidence and mortality worldwide: sources, methods and major
patterns in GLOBOCAN 2012, Int. J. Cancer 136 (5) (2015) E359eE386.
[2] American Cancer Society, Cancer facts & Figures, American Cancer Society,
Atlanta, GA, 2014, 2014.
[3] R.J. Heald, E.M. Husband, R.D. Ryall, The mesorectum in rectal cancer sur-
geryethe clue to pelvic recurrence? Br. J. Surg. 69 (10) (1982) 613e616.
[4] W. Hohenberger, K. Weber, K. Matzel, T. Papadopoulos, S. Merkel, Standard-
ized surgery for colonic cancer: complete mesocolic excision and central
ligationetechnical notes and outcome, Colorectal Dis. 11 (4) (2009) 354e364
discussion 64e5.
[5] N.P. West, W. Hohenberger, K. Weber, A. Perrakis, P.J. Finan, P. Quirke, Com-
plete mesocolic excision with central vascular ligation produces an oncolog-
ically superior specimen compared with standard surgery for carcinoma of the
colon, J. Clin. Oncol. 28 (2) (2010) 272e278.
[6] C.A. Bertelsen, A.U. Neuenschwander, J.E. Jansen, M. Wilhelmsen,
A. Kirkegaard-Klitbo, J.R. Tenma, et al., Disease-free survival after complete
mesocolic excision compared with conventional colon cancer surgery: a
retrospective, population-based study, Lancet Oncol. 16 (2) (2015) 161e168.
[7] T. Watanabe, M. Itabashi, Y. Shimada, S. Tanaka, Y. Ito, Y. Ajioka, et al., Japa-
nese society for Cancer of the colon and rectum (JSCCR) guidelines 2010 for
the treatment of colorectal cancer, Int. J. Clin. Oncol. 17 (1) (2012) 1e29.
[8] N.P. West, H. Kobayashi, K. Takahashi, A. Perrakis, K. Weber, W. Hohenberger,
et al., Understanding optimal colonic cancer surgery: comparison of Japanese
D3 resection and European complete mesocolic excision with central vascular
ligation, J. Clin. Oncol. 30 (15) (2012) 1763e1769.
[9] R.P. Kiran, G.H. El-Gazzaz, J.D. Vogel, F.H. Remzi, Laparoscopic approach
significantly reduces surgical site infections after colorectal surgery: data from
national surgical quality improvement program, J. Am. Coll. Surg. 211 (2)
(2010) 232e238.
[10] S.B. Kang, J.W. Park, S.Y. Jeong, B.H. Nam, H.S. Choi, D.W. Kim, et al., Open
versus laparoscopic surgery for mid or low rectal cancer after neoadjuvant
chemoradiotherapy (COREAN trial): short-term outcomes of an open-label
randomised controlled trial, Lancet Oncol. 11 (7) (2010) 637e645.
[11] D.G. Jayne, P.J. Guillou, H. Thorpe, P. Quirke, J. Copeland, A.M. Smith, et al.,
Randomized trial of laparoscopic-assisted resection of colorectal carcinoma:
3-year results of the UK MRC CLASICC Trial Group, J. Clin. Oncol. 25 (21)
(2007) 3061e3068.
[12] Clinical Outcomes of Surgical Therapy Study Group, A comparison of lapa-
roscopically assisted and open colectomy for colon cancer, N. Engl. J. Med. 350
(20) (2004) 2050e2059.
[13] F.R. Jamali, A.M. Soweid, H. Dimassi, C. Bailey, J. Leroy, J. Marescaux, Evaluating
the degree of difficulty of laparoscopic colorectal surgery, Arch. Surg. 143 (8)
(2008) 762e767 discussion 8.
[14] G. Melich, D.H. Jeong, H. Hur, S.H. Baik, J. Faria, N.K. Kim, et al., Laparoscopic
right hemicolectomy with complete mesocolic excision provides acceptable
perioperative outcomes but is lengthyeanalysis of learning curves for a novice
minimally invasive surgeon, Can. J. Surg. 57 (5) (2014) 331e336.
261
[15] J. Kang, I.K. Kim, S.I. Kang, S.K. Sohn, K.Y. Lee, Laparoscopic right hemi-
colectomy with complete mesocolic excision, Surg. Endosc. 28 (9) (2014)
2747e2751.
[16] M. Adamina, M.L. Manwaring, K.J. Park, C.P. Delaney, Laparoscopic complete
mesocolic excision for right colon cancer, Surg. Endosc. 26 (10) (2012)
2976e2980.
[17] W. Willaert, W. Ceelen, Extent of surgery in cancer of the colon: is more
better? World J. Gastroenterol. 21 (1) (2015) 132e138.
[18] S. Yamamoto, M. Inomata, H. Katayama, J. Mizusawa, T. Etoh, F. Konishi, et al.,
Short-term surgical outcomes from a randomized controlled trial to evaluate
laparoscopic and open D3 dissection for stage II/III colon cancer: Japan Clinical
Oncology Group Study JCOG 0404, Ann. Surg. 260 (1) (2014) 23e30.
[19] S.U. Bae, A.P. Saklani, D.R. Lim, D.W. Kim, H. Hur, B.S. Min, et al., Laparoscopic-
assisted versus open complete mesocolic excision and central vascular liga-
tion for right-sided colon cancer, Ann. Surg. Oncol. 21 (7) (2014) 2288e2294.
[20] J.W. Shin, A.H. Amar, S.H. Kim, J.M. Kwak, S.J. Baek, J.S. Cho, et al., Complete
mesocolic excision with D3 lymph node dissection in laparoscopic colectomy
for stages II and III colon cancer: long-term oncologic outcomes in 168 pa-
tients, Tech. Coloproctol. 18 (9) (2014) 795e803.
[21] S. Mori, K. Baba, M. Yanagi, Y. Kita, S. Yanagita, Y. Uchikado, et al., Laparoscopic
complete mesocolic excision with radical lymph node dissection along the
surgical trunk for right colon cancer, Surg. Endosc. 29 (1) (2015) 34e40.
[22] S.J. Buczacki, R.J. Davies, Colon resection: is standard technique adequate?
Surg. Oncol. Clin. N. Am. 23 (1) (2014) 25e34.
[23] C.A. Klein, Parallel progression of primary tumours and metastases, Nat. Rev.
Cancer 9 (4) (2009) 302e312.
[24] W. Willaert, M. Mareel, D. Van De Putte, Y. Van Nieuwenhove, P. Pattyn,
W. Ceelen, Lymphatic spread, nodal count and the extent of lymphadenec-
tomy in cancer of the colon, Cancer Treat. Rev. 40 (3) (2014) 405e413.
[25] T.E. Le Voyer, E.R. Sigurdson, A.L. Hanlon, R.J. Mayer, J.S. Macdonald,
P.J. Catalano, et al., Colon Cancer survival is associated with increasing number
of lymph nodes analyzed: a secondary survey of intergroup trial INT-0089,
J. Clin. Oncol. 21 (15) (2003) 2912e2919.
[26] C.A. Bertelsen, B. Bols, P. Ingeholm, J.E. Jansen, A.U. Neuenschwander,
J. Vilandt, Can the quality of colonic surgery be improved by standardization
of surgical technique with complete mesocolic excision? Colorectal Dis. 13
(10) (2011) 1123e1129.
[27] H. Kobayashi, N.P. West, K. Takahashi, A. Perrakis, K. Weber, W. Hohenberger,
et al., Quality of surgery for stage III colon cancer: comparison between En-
gland, Germany, and Japan, Ann. Surg. Oncol. 21 (3) (2014) S398eS404.
[28] Y.W. Kim, N.K. Kim, B.S. Min, K.Y. Lee, S.K. Sohn, C.H. Cho, The influence of the
number of retrieved lymph nodes on staging and survival in patients with
stage II and III rectal cancer undergoing tumor-specific mesorectal excision,
Ann. Surg. 249 (6) (2009) 965e972.
[29] Y.W. Kim, K.M. Jan, D.H. Jung, M.Y. Cho, N.K. Kim, Histological inflammatory
cell infiltration is associated with the number of lymph nodes retrieved in
colorectal Cancer, Anticancer Res. 33 (11) (2013) 5143e5150.
[30] S. Ogino, K. Nosho, N. Irahara, J.A. Meyerhardt, Y. Baba, K. Shima, et al.,
Lymphocytic reaction to colorectal Cancer is associated with longer survival,
independent of lymph node count, microsatellite instability, and CpG Island
methylator phenotype, Clin. Cancer Res. 15 (20) (2009) 6412e6420.
[31] N.N. Rahbari, U. Bork, E. Motschall, K. Thorlund, M.W. Büchler, M. Koch, et al.,
Molecular detection of tumor cells in regional lymph nodes is associated with
disease recurrence and poor survival in node-negative colorectal Cancer: a
systematic review and meta-analysis, J. Clin. Oncol. 30 (1) (2012) 60e70.
[32] S. Baskaranathan, J. Philips, P. McCredden, M.J. Solomon, Free colorectal
cancer cells on the peritoneal surface: correlation with pathologic variables
and survival, Dis. Colon Rectum 47 (12) (2004) 2076e2079.
[33] M.S. Cho, S.J. Baek, H. Hur, B. Soh Min, S.H. Baik, N. Kyu Kim, Modified com-
plete mesocolic excision with central vascular ligation for the treatment of
right-sided colon cancer: long-term outcomes and prognostic factors, Ann.
Surg. 261 (4) (2015) 708e715.
[34] J.T. Liang, H.S. Lai, J. Huang, C.T. Sun, Long-term oncologic results of laparo-
scopic D3 lymphadenectomy with complete mesocolic excision for right-
sided colon cancer with clinically positive lymph nodes, Surg. Endosc. 29
(8) (2015) 2394e2401.
[35] C.F. Chow, S.H. Kim, Laparoscopic complete mesocolic excision: west meets
East, World J. Gastroenterol. 20 (39) (2014) 14301e14307.
[36] H.J. Kim, G.S. Choi, J.S. Park, K.H. Lim, Y.S. Jang, S.Y. Park, et al., Laparoscopic
right hemicolectomy with D3 lymph node dissection for a patient with situs
inversus totalis: report of a case, Surg. Today 41 (11) (2011) 1538e1542.
[37] N.P. West, E.J.A. Morris, O. Rotimi, A. Cairns, P.J. Finan, P. Quirke, Pathology
grading of colon cancer surgical resection and its association with survival: a
retrospective observational study, Lancet Oncol. 9 (9) (2008) 857e865.
[38] K. Culligan, J.C. Coffey, R.P. Kiran, M. Kalady, I.C. Lavery, F.H. Remzi, The
mesocolon: a prospective observational study, Colorectal Dis. 14 (4) (2012)
421e428 discussion 8e30.
[39] K. Culligan, F.H. Remzi, M. Soop, J.C. Coffey, Review of nomenclature in colonic
surgeryeproposal of a standardised nomenclature based on mesocolic anat-
omy, Surgeon 11 (1) (2013) 1e5.
[40] K. Culligan, R. Sehgal, D. Mulligan, C. Dunne, S. Walsh, F. Quondamatteo, et al.,
A detailed appraisal of mesocolic lymphangiologyean immunohistochemical
and stereological analysis, J. Anat. 225 (4) (2014) 463e472.
[41] K. Culligan, S. Walsh, C. Dunne, M. Walsh, S. Ryan, F. Quondamatteo, et al., The
mesocolon: a histological and electron microscopic characterization of the
262 N.K. Kim et al. / Surgical Oncology 25 (2016) 252e262
mesenteric attachment of the colon prior to and after surgical mobilization,
Ann. Surg. 260 (6) (2014) 1048e1056.
[42] M. Mike, N. Kano, Reappraisal of the vascular anatomy of the colon and
consequences for the definition of surgical resection, Dig. Surg. 30 (4e6)
(2013) 383e392.
[43] M. Mike, N. Kano, Laparoscopic surgery for colon cancer: a review of the
fascial composition of the abdominal cavity, Surg. Today 45 (2) (2015)
129e139.
[44] R. Sehgal, J.C. Coffey, Historical development of mesenteric anatomy provides
a universally applicable anatomic paradigm for complete/total mesocolic
excision, Gastroenterol. Rep. (Oxf) 2 (4) (2014) 245e250.
[45] R. Sehgal, J.C. Coffey, The development of consensus for complete mesocolic
excision (CME) should commence with standardisation of anatomy and
related terminology, Int. J. Colorectal Dis. 29 (6) (2014) 763e764.
[46] R. Sehgal, J.C. Coffey, Standardization of the nomenclature based on
contemporary mesocolic anatomy is paramount prior to performing a com-
plete mesocolic excision, Int. J. Colorectal Dis. 29 (4) (2014) 543e544.
[47] R. Sehgal, J.C. Coffey, Comprehensive standardization of complete mesocolic
surgery is now possible, Tech. Coloproctol. 18 (7) (2014) 675e676.
[48] S. Toyota, H. Ohta, S. Anazawa, Rationale for extent of lymph node dissection
for right colon cancer, Dis. Colon Rectum 38 (7) (1995) 705e711.
[49] I.J. Park, G.S. Choi, B.M. Kang, K.H. Lim, S.H. Jun, Lymph node metastasis
patterns in right-sided colon cancers: is segmental resection of these tumors
oncologically safe? Ann. Surg. Oncol. 16 (6) (2009) 1501e1506.
[50] J. Kang, H. Hur, B.S. Min, N.K. Kim, K.Y. Lee, Prognostic impact of inferior
mesenteric artery lymph node metastasis in colorectal cancer, Ann. Surg.
Oncol. 18 (3) (2011) 704e710.
[51] Y. Hashiguchi, K. Hase, H. Ueno, H. Mochizuki, E. Shinto, J. Yamamoto, Optimal
margins and lymphadenectomy in colonic cancer surgery, Br. J. Surg. 98 (8)
(2011) 1171e1178.
[52] A.E. Merrie, L.V. Phillips, K. Yun, J.L. McCall, Skip metastases in colon cancer:
assessment by lymph node mapping using molecular detection, Surgery 129
(6) (2001) 684e691.
[53] K.Y. Tan, Y.J. Kawamura, K. Mizokami, J. Sasaki, S. Tsujinaka, T. Maeda, et al.,
Distribution of the first metastatic lymph node in colon cancer and its clinical
significance, Colorectal Dis. 12 (1) (2010) 44e47.
[54] K. Sondenaa, P. Quirke, W. Hohenberger, K. Sugihara, H. Kobayashi, H. Kessler,
et al., The rationale behind complete mesocolic excision (CME) and a central
vascular ligation for colon cancer in open and laparoscopic surgery : pro-
ceedings of a consensus conference, Int. J. Colorectal Dis. 29 (4) (2014)
419e428.
[55] K. Kotake, T. Mizuguchi, K. Moritani, O. Wada, H. Ozawa, I. Oki, et al., Impact of
D3 lymph node dissection on survival for patients with T3 and T4 colon
cancer, Int. J. Colorectal Dis. 29 (7) (2014) 847e852.
[56] C.A. Bertelsen, B. Bols, P. Ingeholm, J.E. Jansen, L.V. Jepsen, B. Kristensen, et al.,
Lymph node metastases in the gastrocolic ligament in patients with colon
cancer, Dis. Colon Rectum 57 (7) (2014) 839e845.
[57] S. Stelzner, W. Hohenberger, K. Weber, N.P. West, H. Witzigmann, T. Wedel,
Anatomy of the transverse colon revisited with respect to complete mesocolic
excision and possible pathways of aberrant lymphatic tumor spread, Int. J.
Colorectal Dis. 31 (2) (2016) 377e384.
[58] A. Perrakis, K. Weber, S. Merkel, K. Matzel, A. Agaimy, C. Gebbert, et al., Lymph
node metastasis of carcinomas of transverse colon including flexures.
Consideration of the extramesocolic lymph node stations, Int. J. Colorectal Dis.
29 (10) (2014) 1223e1229.
[59] D.C. Sabiston, C.M. Townsend, Sabiston Textbook of Surgery : the Biological
Basis of Modern Surgical Practice, Elsevier Saunders, Philadelphia, PA, 2012.
[60] A. Garcia-Ruiz, J.W. Milsom, K.A. Ludwig, P. Marchesa, Right colonic arterial
anatomy. Implications for laparoscopic surgery, Dis. Colon Rectum 39 (8)
(1996) 906e911.
[61] T. Shatari, M. Fujita, K. Nozawa, K. Haku, M. Niimi, Y. Ikeda, et al., Vascular
anatomy for right colon lymphadenectomy, Surg. Radiol. Anat. 25 (2) (2003)
86e88.
[62] D. Ignjatovic, S. Sund, B. Stimec, R. Bergamaschi, Vascular relationships in right
colectomy for cancer: clinical implications, Tech. Coloproctol. 11 (3) (2007)
247e250.
[63] H.I. Acar, A. Comert, A. Avsar, S. Celik, M.A. Kuzu, Dynamic article: surgical
anatomical planes for complete mesocolic excision and applied vascular
anatomy of the right colon, Dis. Colon Rectum 57 (10) (2014) 1169e1175.
[64] G.H. Sakorafas, E. Zouros, G. Peros, Applied vascular anatomy of the colon and
rectum: clinical implications for the surgical oncologist, Surg. Oncol. 15 (4)
(2006) 243e255.
[65] M. Spasojevic, B.V. Stimec, A.P. Dyrbekk, Z. Tepavcevic, B. Edwin, A. Bakka, et
al., Lymph node distribution in the d3 area of the right mesocolon: implica-
tions for an anatomically correct cancer resection. A postmortem study, Dis.
Colon Rectum 56 (12) (2013) 1381e1387.
[66] Y.W. Kim, Y.S. Choi, B.H. Choi, Y.J. Kim, D.Y. Kim, S.J. Cho, et al., The assessment
of the vascular anatomy of the inferior mesenteric artery: an autopsy study,
Korean J. Leg. Med. 31 (2) (2007) 147e150.
[67] G.D. Zuidema, C.J. Yeo, R.T. Shackelford, K.D. Lillemoe, Shackelford’s surgery of
the alimentary tract, 4, W.B. Saunders, Philadelphia; London, 2002.
[68] J.F. Lange, S. Koppert, C.H. van Eyck, G. Kazemier, G.J. Kleinrensink,
M. Godschalk, The gastrocolic trunk of Henle in pancreatic surgery: an
anatomo-clinical study, J. Hepatobiliary Pancreat. Surg. 7 (4) (2000) 401e403.
[69] S. Yamaguchi, H. Kuroyanagi, J.W. Milsom, R. Sim, H. Shimada, Venous anat-
omy of the right colon: precise structure of the major veins and gastrocolic
trunk in 58 cadavers, Dis. Colon Rectum 45 (10) (2002) 1337e1340.
[70] E.J. Voiglio, Retail C. Boutillier du, J.P. Neidhardt, J.L. Caillot, F. Barale,
P. Mertens, Gastrocolic vein. Definition and report of two cases of avulsion,
Surg. Radiol. Anat. 20 (3) (1998) 197e201.
[71] S. Dighe, S. Purkayastha, I. Swift, P.P. Tekkis, A. Darzi, R. A’Hern, et al., Diag-
nostic precision of CT in local staging of colon cancers: a meta-analysis, Clin.
Radiol. 65 (9) (2010) 708e719.
[72] Korean Academy of Medical Science, Korean Clinical Practice Guideline for
Colon and Rectal cancer v.1.0, Korean Academy of Medical Science, Seoul,
2012.
[73] National Comprehensive Cancer Network, National comprehensive cancer
network guidelines, Colon cancer (Version 2.2015), 2015. Available from,
http://www.nccn.org/professionals/physician_gls/pdf/colon.pdf.
[74] G. Galizia, E. Lieto, F. De Vita, F. Ferraraccio, A. Zamboli, A. Mabilia, et al., Is
complete mesocolic excision with central vascular ligation safe and effective
in the surgical treatment of right-sided colon cancers? A prospective study,
Int. J. Colorectal Dis. 29 (1) (2014) 89e97.
[75] Y. Kanemitsu, K. Komori, K. Kimura, T. Kato, D3 lymph node dissection in right
hemicolectomy with a No-touch isolation technique in patients with colon
Cancer, Dis. Colon Rectum 56 (7) (2013) 815e824.
[76] S. Tagliacozzo, A. Tocchi, Extended mesenteric excision in right hemi-
colectomy for carcinoma of the colon, Int. J. Colorectal Dis. 12 (5) (1997)
272e275.
[77] M.G. Pramateftakis, Optimizing colonic cancer surgery: high ligation and
complete mesocolic excision during right hemicolectomy, Tech. Coloproctol.
14 (1) (2010) S49eS51.
[78] A.A. Tentes, C. Mirelis, C. Karanikiotis, O. Korakianitis, Radical lymph node
resection of the retroperitoneal area for left-sided colon cancer, Langenbecks
Arch. Surg. 392 (2) (2007) 155e160.
[79] B. Feng, J. Sun, T.L. Ling, A.G. Lu, M.L. Wang, X.Y. Chen, et al., Laparoscopic
complete mesocolic excision (CME) with medial access for right-hemi colon
cancer: feasibility and technical strategies, Surg. Endosc. 26 (12) (2012)
3669e3675.
[80] D.P. Han, A.G. Lu, H. Feng, P.X. Wang, Q.F. Cao, Y.P. Zong, et al., Long-term
outcome of laparoscopic-assisted right-hemicolectomy with D3 lymphade-
nectomy versus open surgery for colon carcinoma, Surg. Today 44 (5) (2014)
868e874.
[81] L.M. Siani, C. Pulica, Laparoscopic Complete Mesocolic Excision with Central
Vascular Ligation in right colon cancer: long-term oncologic outcome be-
tween mesocolic and non-mesocolic planes of surgery, Scand. J. Surg. 104 (4)
(2015) 219e226.
[82] L.Y. Zhao, H. Liu, Y.N. Wang, H.J. Deng, Q. Xue, G.X. Li, Techniques and feasi-
bility of laparoscopic extended right hemicolectomy with D3 lymphadenec-
tomy, World J. Gastroenterol. 20 (30) (2014) 10531e10536.
[83] J.L. Huang, H.B. Wei, J.F. Fang, Z.H. Zheng, T.F. Chen, B. Wei, et al., Comparison
of laparoscopic versus open complete mesocolic excision for right colon
cancer, Int. J. Surg. 23 (Pt A) (2015) 12e17.
[84] T. Nagasaki, T. Akiyoshi, Y. Fujimoto, T. Konishi, S. Nagayama, Y. Fukunaga, et
al., Prognostic impact of distribution of lymph node metastases in stage III
colon Cancer, World J. Surg. 39 (12) (2015) 3008e3015.
[85] J.C. Li, K.L. Leung, S.S. Ng, S.Y. Liu, J.F. Lee, S.S. Hon, Laparoscopic-assisted
versus open resection of right-sided colonic cancerea prospective random-
ized controlled trial, Int. J. Colorectal Dis. 27 (1) (2012) 95e102.
[86] E.L. Bokey, P.H. Chapuis, O.F. Dent, B.J. Mander, I.P. Bissett, R.C. Newland,
Surgical technique and survival in patients having a curative resection for
colon cancer, Dis. Colon Rectum 46 (7) (2003) 860e866.
[87] J. Liang, V. Fazio, I. Lavery, F. Remzi, T. Hull, S. Strong, et al., Primacy of surgery
for colorectal cancer, Br. J. Surg. 102 (7) (2015) 847e852.