Content uploaded by Muhammed Rafay Siddiqui
Author content
All content in this area was uploaded by Muhammed Rafay Siddiqui on Dec 09, 2015
Content may be subject to copyright.
REVIEW
A systematic review and meta-analysis evaluating the role
of laparoscopic surgical resection of transverse colon tumours
M. Chand •M. R. S. Siddiqui •S. Rasheed •
G. Brown •P. Tekkis •A. Parvaiz •T. Qureshi
Received: 9 November 2013 / Accepted: 23 April 2014 / Published online: 25 June 2014
ÓSpringer Science+Business Media New York 2014
Abstract
Objectives A meta-analysis of published literature com-
paring outcomes after laparoscopic resection (LR) with
open resection (OR) for transverse colon tumours.
Methods Medline, PubMed, CINAHL, EMBASE and
Cochrane were searched from inception to October 2013.
The text words ‘‘minimally invasive’’, ‘‘keyhole surgery’’
and ‘‘transverse colon’’ were used in combination with the
medical subject headings ‘‘laparoscopy’’ and ‘‘colon can-
cer’’. Outcome variables were chosen based upon whether
the included articles reported results. A meta-analysis was
performed to obtain a summative outcome.
Results Six comparatives involving 444 patients were
analysed. Of them 245 patients were in the LR group and 199
in the OR group. There was a significant increase in operative
time in the LR group compared with the OR group [random
effects model: SMD =-0.65, 95 % CI (-1.01, -0.30),
z=-3.60, p\0.001] but there was significant heteroge-
neity amongst trials (Q=15.51, df =5, p=0.008,
I
2
=68). There was less blood loss in the LR group [fixed
effects model: SMD =0.70, 95 % CI (0.47, 0.93), z=6.01,
p\0.001] and patients returned to oral diet earlier [random
effects model: SMD =0.78, 95 % CI (0.40, 1.16), z=4.01,
p\0.001] and had a reduced time to functioning bowel
[fixed effects model: SMD =0.86, 95 % CI (0.60, 1.11),
z=6.63, p\0.001]. No difference was seen for overall
morbidity (p=0.76) or mortality (p=0.58).
Conclusions LR of transverse colon tumours is a safe and
effective technique. Although there is an increase in operating
time, operative and clinical outcomes of intraoperative blood
loss and faster recovery are seen with laparoscopic procedures.
Keywords Laparoscopy Transverse colon tumours
Colorectal cancer Surgery Outcomes
Laparoscopic resection (LR) has become well established
in the surgical management of colon cancer in recent years.
Whilst there remains some debate about the merits of
laparoscopy in rectal cancer particularly surrounding
oncological compromise [1], the benefits of shorter hospital
stay, faster recovery and reduced morbidity in uncompli-
cated colon cancer are well documented [2,3].
Several large scale trials have attempted to evaluate the
role of laparoscopy in colorectal cancer, but noticeably
many have not included transverse colon tumours in the
study group [4–9]. The surgical management of tumours of
the transverse colon is not standardized and may depend on
several factors including exact location of tumour, stage
and anatomical factors. For example, the position of the
tumour will determine whether or not the middle colic
artery (MCA) needs to be included in the resection
M. Chand (&)M. R. S. Siddiqui S. Rasheed G. Brown
P. Tekkis
Royal Marsden Hospital, Downs Road, Sutton, Surrey,
London SM2 5PT, UK
e-mail: mans001@aol.com; manish.chand@rmh.nhs.uk
M. Chand G. Brown P. Tekkis
Imperial College, London, UK
M. Chand T. Qureshi
Poole Hospital, Poole, UK
M. R. S. Siddiqui
Croydon Hospital, Surrey, UK
S. Rasheed
Royal Marsden Hospital, London, UK
A. Parvaiz
Queen Alexandra Hospital, Portsmouth, UK
123
Surg Endosc (2014) 28:3263–3272
DOI 10.1007/s00464-014-3634-3
and Other Interventional Techniques
specimen. This issue becomes more pronounced in lapa-
roscopic surgery which relies on standardization of tech-
nique and approach for success. The apparent difficulty is
associated with laparoscopic dissection and control of the
MCA, and extended lymphadenectomy has meant that only
experienced surgeons have attempted such procedures.
There is a paucity of literature on the outcomes asso-
ciated with LRs of transverse colon tumours. This paper
aims to systematically review the short- and medium-term
outcomes of LR of transverse colon tumours compared
with open procedures to determine whether it is a safe and
effective procedure.
Methods
All comparative studies investigating laparoscopic versus
open resection (OR) of transverse colon tumours in adult
patients up until October 2013 were identified. We searched
the MEDLINE, EMBASE and CINAHL available through
the National Library of Health website, the Cochrane
library, CENTRAL and PubMed databases available online.
The text words ‘‘minimally invasive’’, ‘‘keyhole surgery’’
and ‘‘transverse colon’’ were used in combination with the
medical subject headings ‘‘laparoscopy’’ and ‘‘colon can-
cer’’. Irrelevant articles, reviews and meta-analyses evident
from the titles and abstracts were excluded. Relevant articles
referenced in these publications were obtained and the
‘‘related article’’ function was used to widen the results. No
language restriction was applied. All abstracts, comparative
studies, non-randomized trials and citations were searched
comprehensively. A flow chart of the literature search
according to PRISMA guidelines [10]isshowninFig.1.
A total of 130 articles were screened for relevance. On
further scrutiny only five comparative studies were found to
have useful data for this meta-analysis.
Each article was critically reviewed by two researchers
using a double extraction method for eligibility in our
review (Table 3). This was performed independently and
any conflict resolved prior to final analysis. A third
researcher confirmed the data extraction.
Outcome variables were chosen based upon whether the
included articles reported results. Statistical analyses were
performed using comprehensive meta-analysis [11].
Fig. 1 PRISMA 2009 flow
diagram
3264 Surg Endosc (2014) 28:3263–3272
123
A value of p\0.05 was chosen as the significance level
for outcome measures. For continuous data (e.g. operation
time), the inverse-variance method was used for the com-
bination of standardized mean differences (SMD). Binary
data (e.g. morbidity) were summarized as risk ratios (RR)
and combined using the Mantel–Haenszel method. In each
case, a heterogeneity test was carried out to see whether the
fixed effects model was appropriate. In a sensitivity ana-
lysis, 1 was added to each cell frequency for trials in which
no event occurred, according to the method recommended
by Deeks et al. [12]. Where standard deviations were not
reported, these were estimated either from ranges or
pvalues. Forest plots were used for the graphical display.
Results
Five comparative studies [13–17] comparing open with LR
of transverse colon tumours were retrieved from the elec-
tronic databases and included in our study according to our
inclusion criteria (Table 1). One study separated data into
stage II and stage III cancers and are treated as separate
data in our meta-analysis [14]. Our exclusion criteria are
listed in Table 2. Characteristics of each trial are given in
Table 3. There were 199 patients in the open group and
245 in the laparoscopic group. The outcome measures
extracted are shown in Tables 4and 5. The methodological
quality of included trials is explained comprehensively in
Table 6[18,19].
Characteristics of studies
There were a range of clinical differences between the
studies. Operative techniques varied between right and left
extended hemicolectomies to subtotal and transverse co-
lectomies. Some studies defined the cases as having
operative techniques necessitating division of one or both
the branches of the MCA whilst others defined their cases
as being between both flexures. Most articles were retro-
spective meaning in some the baseline characteristics were
not comparable such as tumour stage, anastomosis tech-
nique and patient demographics. Furthermore, some studies
identified the need for thorough lymphadenectomies whilst
others did not document this in detail. Detailed character-
istics can be found in Table 3.
Operative time
Five studies [13–17] contributed to a summative outcome.
There was significant heterogeneity amongst trials (Q=
15.51, df =5, p=0.008, I
2
=68). There was a significant
difference in operative time with laparoscopic procedures
taking longer [random effects model: SMD =-0.65,
95 % CI (-1.01, -0.30), z=-3.60, p\0.001; Fig. 2].
This translates to an approximate decrease of 46 min in the
open group (CI -75, -17).
Estimated blood loss
Four studies [13–16] discussed estimated blood loss. There
was no significant heterogeneity amongst trials (Q=4.67,
df =4, p=0.32, I
2
=14). There was less blood loss in
the laparoscopic group [fixed effects model: SMD =0.70,
95 % CI (0.47, 0.93), z=6.01, p\0.001; Fig. 3]. This
translates to an approximate increase of 114 ml in the open
group (CI 59, 170).
Lymph node harvest
There was significant heterogeneity (Q=19.65, df =5,
p=0.001, I
2
=75) amongst five studies [13–17]. There
was no difference in lymph node harvest between laparo-
scopic and ORs [random effects model: SMD =0.13,
95 % CI (-0.27, 0.52), z=0.63, p=0.53; Fig. 4].
Time to oral intake
Four trials [13–16] investigated time to oral intake and
significant heterogeneity existed between trials (Q=
12.31, df =4, p=0.02, I
2
=68). The laparoscopic group
returned to oral intake sooner [random effects model:
SMD =0.78, 95 % CI (0.40, 1.16), z=4.01, p\0.001;
Fig. 5]. This translates to an approximate increase of
1.8 days in the open group (CI 0.7, 3.0).
Time to flatus
Three studies [13,15,16] reported on time to flatus. There
was no significant heterogeneity amongst trials (Q=0.65,
Table 1 Inclusion criteria
All studies comparing laparoscopic with open surgery for
transverse colon tumours
All elective cases
Trials on patients of any age and sex
Trials in all languages
Table 2 Exclusion criteria
Non-comparative studies
Studies comparing laparoscopic with hand-assisted resections of
transverse colon tumours
Studies comparing hand-assisted with open surgery
Studies comparing outcomes from resection of transverse colon
tumours with tumours of other sites
Surg Endosc (2014) 28:3263–3272 3265
123
df =2, p=0.72, I
2
=0). Patients passed flatus sooner
compared with the open group [fixed effects model:
SMD =0.86, 95 % CI (0.60, 1.11), z=6.63, p\0.001;
Fig. 6].
Hospital stay
Four studies [13–16] reported hospital stay. There was sig-
nificant heterogeneity amongst trials (Q=12.14, df =4,
p=0.016, I
2
=67). Patients left hospital sooner after LR
[fixed effects model: SMD =0.41, 95 % CI (0.20, 0.62),
z=3.84, p\0.001; Fig. 7]. This translates to an approxi-
mate increase of 3.6 days in the open group (CI 0.3, 6.8).
Local and distant recurrence
Two studies [13,14] gave data on local and distant
recurrence. There was no significant difference in relation
to local recurrence (p=0.19) and distant recurrence
(p=0.93).
Complications
No difference was seen between the two techniques in
relation to anastomotic leak (p=0.42), wound infection
(p=0.81) or medical complications (p=0.57).
Overall morbidity and mortality
Three articles [13,15,16] reported on overall morbidity
and four studies [13–16] reported overall post-operative
mortality. There was no significant difference highlighted
between the two techniques for morbidity (p=0.76) and
mortality (p=0.58).
Discussion
This study found on a limited number of studies which
reported on outcomes on laparoscopic transverse colec-
tomy. Of the studies identified, there was no parameter
which showed worse results in the laparoscopic group
compared to open.
The outcome measures can be broadly divided into
intra-operative, post-operative and histopathological out-
comes. Intra-operative outcomes include operation length
and estimated blood loss. There was a significant difference
in the operative time which is in keeping with the litera-
ture; however, the difference was only 46 min. This may
reflect the level of difficulty in open operating for trans-
verse colon tumours and that laparoscopy may make access
less challenging. It is worth remembering that in laparo-
scopic right sided resections, it is common to perform the
Table 3 Characteristics of trials
Trial Year Type NType Trial protocol
Fernandez-Cebrian et al. 2013 Open lap 52
34
Retrospective Tumours not defined. Extended right, left, subtotal and
transverse colectomies. 62 % patients male in
laparoscopic group; 48 % male in open. Mean age
Lap: 60.3; Open: 62.4. Stage II, Lap: 38 %; Open:
46 %
Yamamoto et al. (a) 2012 Open lap 34
99
Prospective Tumours included descending colon tumours. 55 %
patients male in laparoscopic group; 58 % male in
open. Mean age Lap: 65; Open: 64. TII and III, Lap:
50 %; Open: 76 %
Zmora et al. 2010 Open lap 24
22
Retrospective Tumours defined as those proximal to splenic and distal
to hepatic flexure. Extended right and left colectomy.
Stapled and handsewn anastomoses. 63 % patients
male in laparoscopic group; 50 % male in open. Mean
age Lap: 68; Open: 70.5. Dukes B and C, Lap: 82 %;
Open: 91 %
Akiyoshi et al. 2010 Open lap 39
53
Unclear,
suggestive
of
retrospective
Tumours defined as those proximal to splenic and distal
to hepatic flexure and ligation of at least one branch of
middle colic artery. Extended right and left colectomy
and transverse colectomies performed. 60 % patients
male in laparoscopic group; 54 % male in open. Mean
age Lap: 66; Open: 62. TII and III, Lap: 47 %; Open:
82 %
Kim et al. 2009 Open lap 50
37
Retrospective Tumours defined as those proximal to splenic and distal
to hepatic flexure and requiring ligation of middle
colic artery. Extended right and left colectomy and
transverse colectomies performed. 50 % patients male
in laparoscopic and open groups. Mean age Lap: 63.3;
Open: 64.5.
3266 Surg Endosc (2014) 28:3263–3272
123
Table 4 Peri-operative outcome measures
Trial Year Type NOT (min) EBL (ml) CR
(n)
LN Oral (days) Flatus (days) HS (days) OMb
(n)
OMt
(n)
LRec
(n)
DRec
(n)
ORec
(%)
OS
(%)
DFS
(%)
Fernandez-
Cebrian et al.
2013 Open
lap
52 199.3
sd =32.9
305.7 ±325.3 14.2 sd =8.3 3.4 ±1.5 3.8 ±3.0 7.3
sd =1.6
8024
34 215.4
sd =44.6
105.9 ±140.9 1 16.2
sd =13.9
3.1 ±1.4 2.1 ±0.3
(p=0.043)
7.1
sd =2.2
6014
Yamamoto
et al. (a)
2012 Open
lap
15 165 100 19 (7–27) 7 29 0 0 0 0 84.9 84.9
55 230
p=0.012
10 p=0.001 5 15 (3–33) 5
p=0.026
15
p=0.001
0 1 1 3.6 93.7 90.0
Yamamoto
et al. (b)
2012 Open
lap
19 202 155 14 [1–10] 7 31 1 3 4 37 63.4 54.6
44 245
p=0.038
10 p=0.001 6 16 (5–35) 4
p=0.001
7
p=0.001
1 3 8 25 66.7 56.9
Zmora et al. 2010 Open
lap
24 147 521 16.8
22 265
p=0.0001
237 1 16.2 [10–23]
Akiyoshi et al. 2010 Open
lap
39 157
(89–271)
79 (3–590) 23 (8–40) 5.3 [3–14] 2.5 [1–4]15[9–24]3 0
53 224
(130–416)
40 (0–330) 1 17 (7–35) 2.4 [2–9] 1.7 (0–4) 12 (6–29) 5 0
Kim et al. 2009 Open
lap
50 199.5
sd =44.9
278.8
sd =268.7
22.7
sd =11.8
5.4
sd =1.9
4.4 sd =2.0 11.2
sd =5.6
30
37 202.6
sd =47.6
113.8
sd =128.9
26.1
sd =13.9
3.9
sd =1.7
2.8 sd =0.9 11 sd =4.0 2 0
Nnumber, OT operative time, EBL estimated blood loss, CR conversion rate, LN lymph node harvest, Oral time to oral intake, Flatus time to flatus passage, HS hospital stay, OMb overall
morbidity, OMt overall mortality, LRec local recurrence, DRec distant recurrence, ORec overall recurrence, OS overall survival, DFS disease free survival. (a)-Stage II; (b)-Stage III
Surg Endosc (2014) 28:3263–3272 3267
123
anastomosis extracorporeally which would be same for
both open and laparoscopic cases. It should be noted also
that there was a wide range of operating times for laparo-
scopic surgery (89–416 min) and may reflect the learning
curves of individual surgeons [9–13]. In terms of blood
loss, there was less in the laparoscopic patients ranging
from 0 to 330 ml compared with 3–590 ml in the open
group [9–12]. This has been a finding in most laparoscopic
procedures which reflects the more precise nature of dis-
section in laparoscopy.
The early post-operative outcome measures included
time to oral intake, time to flatus and hospital stay. For all
three of these outcomes, patients had better outcomes in the
laparoscopic group. These results are similar to findings in
other laparoscopic colorectal procedures. Laparoscopy
allows for less handling of the bowel and subsequently, less
Table 5 Complication outcomes
Trial Year Type N AL WI Med
Fernandez-Cebrian et al. 2013 Open lap 52
34
0
1
4
0
Yamamoto et al. 2012 Open lap 15
55
1
1
2
8
Yamamoto et al. 2012 Open lap 19
44
2
1
2
6
Zmora et al. 2010 Open lap 24
22
1
1
6
8
3
1
Akiyoshi et al. 2010 Open lap 39
53
0
0
1
0
Kim et al. 2009 Open lap 50 0 2 0
37 0 0 1
AL anastomotic leak, WI wound infection, Med medical complications
Table 6 Methodological
qualities of studies included
(0 = No; 1 = Yes)
Adapted from the Scottish
intercollegiate guidelines
network and Rangel et al.
Quality variables Fernandez-
Cebrian
et al.
Yamamoto
et al.
Zmora
et al.
Akiyoshi
et al.
Kim
et al.
Inclusion criteria 1 1 1 1 1
Exclusion criteria 1 1 0 1 1
Demographics comparable? 1 0 1 1 1
Can the number of participating centres be
determined?
11111
Can the number of surgeons who participated be
determined?
00000
Can the reader determine where the authors are
on the learning curve for the reported
procedure?
11000
Are diagnostic criteria clearly stated for clinical
outcomes if required?
10000
Is the surgical technique adequately described? 1 1 1 1 1
Is there any way that they have tried to
standardize the operative technique?
11111
Is there any way that they have tried to
standardize perioperative care?
1 0.5 0 0 0
Is the age and range given for patients in the
laparoscopic group?
11111
Do authors address whether there is any missing
data?
00010
Is the age and range given for patients in the
open group?
11111
Were patients in each group treated along
similar timelines?
11011
Did all the patients asked to enter the study take
part?
01000
Dropout rates stated 0 0 0 0 0
Outcomes clearly defined? 1 0 0 0 0
Blind Assessors 0 0 0 0 0
Standardized assessment tools? 0 0 0 0 0
Analysis by intention to treat 0 0 0 0 0
3268 Surg Endosc (2014) 28:3263–3272
123
episodes of ileus [20]. The consequence of faster recovery
of the gut helps in shortening hospital stay.
Complications and overall morbidity and mortality were
similar in both groups. In previous systematic reviews of
laparoscopic colorectal surgery, reduced complications and
morbidity have been features of laparoscopy. This would
suggest that LR of transverse colon tumours leads to more
complications and morbidity than would be expected in
other locations of the colorectum. Although the rates are
still low, one of the main perceived advantages of lapa-
roscopy is improved morbidity. Identification and dissec-
tion around the MCA is considered to be one of the most
challenging aspects of laparoscopic colorectal surgery.
Suggestions to confidently dissect the root of the MCA
Fig. 2 Operative time
Fig. 3 Estimated blood loss
Fig. 4 Lymph note harvest
Surg Endosc (2014) 28:3263–3272 3269
123
include exposure of the distal superior mesenteric vein to
facilitate identification below the pancreas [21]; creating a
‘‘window’’ for lymphadenectomy and ligation of the MCA
[22]; and rotation of the mesocolon [23].
One of the main concerns over laparoscopy when first
introduced into the surgical management of colorectal cancer
was compromise of oncology and thus worse rates of disease
recurrence. As with any novel surgical approach, there is an
associated learning curve. Transverse colon tumours account
for approximately 10 % of cases of colorectal cancer. This
means that there is less opportunity for surgeons to improve
their experience with such challenging cases. The recurring
concern with LR of transverse colon tumours is that the
oncology may be compromised by an inadequate lymphad-
enectomy. The number of lymph nodes retrieved following
colorectal resection for cancer is positively associated with
survival [24]. Therefore, an early measure of resection quality
is the number of lymph nodes found on the resection
Fig. 5 Time to first flatus oral
in take
Fig. 6 Time to first flatus
Fig. 7 Hospital stay
3270 Surg Endosc (2014) 28:3263–3272
123
specimen—the lymph node yield. Some skeptics have
incorrectly assumed that laparoscopy leads to fewer lymph
nodes in the resection specimen butthis has not been the case
in the review of the literature for colorectal cancer as a whole
[3,25]. The present study also confirms that there was no
difference in lymph node yield between open and laparo-
scopic patients. Despite the relatively short follow-up period,
there was also no difference in disease recurrence or survival
although only two studies reported on this.
Limitations and heterogeneity
Limitations to our meta-analysis include lack of clear
definitions in individual studies relating to measurement of
operative time, how they calculated blood loss or whether
it was a simple estimate and the techniques specifically
used to assess lymph node harvest. Furthermore, the lack of
randomization means the strength of the evidence is lim-
ited. The low number of trials also makes specific con-
clusions challenging to make.
There was significant heterogeneity in operative time,
lymph node harvest, time to oral intake and hospital stay.
These differences may relate to the variation in operation e.g.
extended right hemicolectomy, left hemicolectomy and seg-
mental resections. Local protocols may be a significant
influence in early feeding versus a more conservative
approach especially given that the studies were not random-
ized. There were also large discrepancies between sample
sizes in the laparoscopic versus open groups in individual
studies. These clinical differences need to be borne in mind in
relation to the other outcome measures despite a lack of sta-
tistical heterogeneity (e.g. overall morbidity and mortality).
The potential of these factors along with possible publication
bias means conclusions for clinical practice derived from
these studies need to be determined with caution.
In conclusion, LR of transverse colon tumours is a safe
and effective technique. Although there is an increase in
operating time, operative and clinical outcomes of intra-
operative blood loss and faster recovery are seen with
laparoscopic procedures.
Disclosures Chand M, Siddiqui MRS, Rasheed S, Brown G, Tekkis
P, Parvaiz A, Qureshi T have no conflict of interests.
References
1. Chand M, Heald RJ (2011) Laparoscopic rectal cancer surgery.
Br J Surg 98:166–167
2. Kuhry E, Schwenk W, Gaupset R, Romild U, Bonjer J (2008)
Long-term outcome of laparoscopic surgery for colorectal cancer:
a cochrane systematic review of randomised controlled trials.
Cancer Treat Rev 34:498–504
3. Schwenk W, Haase O, Neudecker J, Muller JM (2005) Short term
benefits for laparoscopic colorectal resection Cochrane Database
Syst Rev 3:CD003145
4. Guillou PJ, Quirke P, Thorpe H, Walker J, Jayne DG, Smith AM,
Heath RM, Brown JM (2005) Short-term endpoints of conven-
tional versus laparoscopic-assisted surgery in patients with
colorectal cancer (MRC CLASICC trial): multicentre, random-
ised controlled trial. Lancet 365:1718–1726
5. COlon cancer Laparoscopic or Open Resection Study Group
(COLOR) (2000) COLOR: a randomized clinical trial comparing
laparoscopic and open resection for colon cancer. Dig Surg
17:617–622
6. Clinical Outcomes of Surgical Therapy Study Group (2004) A
comparison of laparoscopically assisted and open colectomy for
colon cancer. N Engl J Med 350:2050–2059
7. Lacy AM, Garcia-Valdecasas JC, Delgado S, Castells A, Taura P,
Pique JM, Visa J (2002) Laparoscopy-assisted colectomy versus
open colectomy for treatment of non-metastatic colon cancer: a
randomised trial. Lancet 359:2224–2229
8. Braga M, Vignali A, Zuliani W, Frasson M, Di Serio C, Di Carlo
V (2005) Laparoscopic versus open colorectal surgery: cost-
benefit analysis in a single-center randomized trial Ann Surg:
242:890–895 (discussion 5–6)
9. Leung KL, Kwok SP, Lam SC, Lee JF, Yiu RY, Ng SS, Lai PB,
Lau WY (2004) Laparoscopic resection of rectosigmoid carci-
noma: prospective randomised trial. Lancet 363:1187–1192
10. Liberati A, Altman DG, Tetzlaff J, Mulrow C, Gotzsche PC,
Ioannidis JP, Clarke M, Devereaux PJ, Kleijnen J, Moher D
(2009) The PRISMA statement for reporting systematic reviews
and meta-analyses of studies that evaluate healthcare interven-
tions: explanation and elaboration. BMJ 339:b2700
11. Zandvliet ML, Kester MG, van Liempt E, de Ru AH, van Veelen
PA, Griffioen M, Guchelaar HJ, Falkenburg JH, Meij P (2012)
Efficiency and mechanism of antigen-specific CD8?T-cell
activation using synthetic long peptides. J Immunother 35:
142–153
12. Mijailovich SM, Li X, Griffiths RH, Geeves MA (2012) The hill
model for binding myosin S1 to regulated actin is not equivalent
to the Mckillop–Geeves model. J Mol Biol 417:112–128
13. Fernandez-Cebrian JM, GilYonte P, Jimenez-Toscano M, Vega
L, Ochando F (2013) Laparoscopic colectomy for transverse
colon carcinoma: a surgical challenge but oncologically feasible.
Colorectal Disease 15:e79–e83
14. Yamamoto M, Okuda J, Tanaka K, Kondo K, Tanigawa N,
Uchiyama K (2012) Clinical outcomes of laparoscopic surgery
for advanced transverse and descending colon cancer: a single-
center experience. Surg Endosc 26:1566–1572
15. Kim HJ, Lee IK, Lee YS, Kang WK, Park JK, Oh ST, Kim JG,
Kim YH (2009) A comparative study on the short-term clinico-
pathologic outcomes of laparoscopic surgery versus conventional
open surgery for transverse colon cancer. Surg Endosc 23:
1812–1817
16. Akiyoshi T, Kuroyanagi H, Fujimoto Y, Konishi T, Ueno M, Oya
M, Yamaguchi T (2010) Short-term outcomes of laparoscopic
colectomy for transverse colon cancer. J Gastrointest Surg
14:818–823
17. Zmora O, Bar-Dayan A, Khaikin M, Lebeydev A, Shabtai M,
Ayalon A, Rosin D (2010) Laparoscopic colectomy for transverse
colon carcinoma. Tech Coloproctol 14:25–30
18. Rangel SJ, Kelsey J, Colby CE, Anderson J, Moss RL.(2003)
Development of a quality assessment scale for retrospective
clinical studies in pediatric surgery J Pediatr Surg 38:390–396
(discussion-6)
19. http://www.sign.ac.uk/guidelines/fulltext/50/checklist3.html.SIGN
Guidelines. 2009 [updated March 2009; cited 2013 10th October]
Surg Endosc (2014) 28:3263–3272 3271
123
20. Schwenk W, Bohm B, Haase O, Junghans T, Muller JM (1998)
Laparoscopic versus conventional colorectal resection: a pro-
spective randomised study of postoperative ileus and early
postoperative feeding. Langenbecks Arch Surg 383:49–55
21. Fujita J, Uyama I, Sugioka A, Komori Y, Matsui H, Hasumi A
(2001) Laparoscopic right hemicolectomy with radical lymph
node dissection using the no-touch isolation technique for
advanced colon cancer. Surg Today 31:93–96
22. Baca I, Perko Z, Bokan I, Mimica Z, Petricevic A, Druzijanic N,
Situm M (2005) Technique and survival after laparoscopically
assisted right hemicolectomy. Surg Endosc 19:650–655
23. Ichihara T, Takada M, Fukumoto S, Kuroda Y (2004) Lymphad-
enectomy along the middle colic artery in laparoscopic resection of
transverse colon. Hepatogastroenterology 51:454–456
24. Chang GJ, Rodriguez-Bigas MA, Skibber JM, Moyer VA (2007)
Lymph node evaluation and survival after curative resection of
colon cancer: systematic review. J Natl Cancer Inst 99:433–441
25. Kuhry E, Schwenk WF, Gaupset R, Romild U, Bonjer HJ (2008)
Long-term results of laparoscopic colorectal cancer resection.
Cochrane Database Syst Rev. doi:10.1002/14651858.CD003432.
pub2
3272 Surg Endosc (2014) 28:3263–3272
123
