International Journal of Surgery 19 (2015) 61e66

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International Journal of Surgery

journal homepage: www.journal-surgery.net

Original research

Laparoscopic assisted versus open gastric pull-up following

thoracoscopic esophagectomy: A cohort study
Hiroyuki Daiko*, Takeo Fujita
Department of Surgery, National Cancer Center Hospital East, Chiba, Japan

h i g h l i g h t s
 This study evaluated a feasibility of laparoscopically assisted gastric pull-up (LAG) following thoracoscopic esophagectomy (TE).
 LAG was compared with open laparotomy gastric pull-up (OLG) following TE.
 No signicant difference was found between two groups in the technical and oncological outcomes.
 LAG following TE was feasible in patient with thoracic esophageal cancer.

a r t i c l e i n f o

a b s t r a c t

Article history:
Received 6 November 2013
Received in revised form
23 March 2015
Accepted 9 April 2015
Available online 15 May 2015

Background: Thoracolaparoscopic esophagectomy (TLE) is a type of minimally invasive esophagectomy

(MIE) for esophageal cancer which consists of thoracoscopic resection and laparoscopic reconstruction.
The aim of the present study was to evaluate the technical and oncological feasibility of alimentary tract
reconstruction with laparoscopically assisted gastric pull-up (LAG) following thoracoscopic esophagectomy in the prone position (TSEP) in comparison with reconstruction with open laparotomy gastric
pull-up (OLG) following TSEP, to establish TLE with extended lymph node dissection as a standard
operation for esophageal cancer.
Methods: Sixty-four patients with esophageal cancer underwent TSEP with 3-eld lymphadenectomy
from 2008 through 2010: for reconstruction after TSEP, 31 patients underwent LAG, and 33 patients
underwent OLG. We retrospectively evaluated the technical and oncological feasibility of TLE with 3-eld
lymphadenectomy and compared surgical outcomes after reconstruction with OLG and that with LAG.
Results: TLE with 3-eld lymphadenectomy was successfully completed in 30 of 31 (97%) patients, and
no surgery-related postoperative deaths occurred. No signicant difference was found between LAG and
OLG in the mean number of dissected abdominal lymph nodes, amount of blood loss, incidence of
postoperative complications, mean postoperative hospital stay, restoration rate of respiratory function, or
rate of complete resection or locoregional control, but the mean duration of abdominal procedures was
signicantly longer with LAG than with OLG.
Conclusion: This study demonstrates that the quality and safety of surgery and the oncological effectiveness of LAG for esophageal cancer. TLE consisting of LAG following TSEP with extended lymph-node
dissection is a feasible surgical technique for thoracic esophageal carcinoma.
2015 The Authors. Published by Elsevier Ltd on behalf of IJS Publishing Group Limited. This is an open
access article under the CC BY-NC-SA license (http://creativecommons.org/licenses/by-nc-sa/4.0/).

Keywords:
Thoracoscopic surgery
Laparoscopic surgery
Esophageal cancer

1. Introduction
Surgical resection is the standard treatment for carcinoma of the
thoracic esophagus. However, the procedure is a complex; involves
the cervical, thoracic, and abdominal elds; and includes

* Corresponding author. Department of Surgery, National Cancer Center Hospital

East, 6-5-1 Kashiwanoha, Kashiwa, Chiba 277-8577, Japan.
E-mail address: hdaikou@east.ncc.go.jp (H. Daiko).

thoracotomy or laparotomy or both. Accordingly, resection of carcinomas of the thoracic esophagus can be associated with signicant morbidity and mortality and a delay in return to preoperative
activity levels. Thoracolaparoscopic esophagectomy (TLE) is a type
of minimally invasive esophagectomy (MIE) for esophageal cancer
which comprises both thoracoscopic resection and laparoscopic
reconstruction. Such an MIE can produce less morbidity than open
operations and allows a quicker return to normal function [1]. We
have assessed the technical and oncological feasibility of

http://dx.doi.org/10.1016/j.ijsu.2015.04.040
1743-9191/ 2015 The Authors. Published by Elsevier Ltd on behalf of IJS Publishing Group Limited. This is an open access article under the CC BY-NC-SA license (http://
creativecommons.org/licenses/by-nc-sa/4.0/).

62

H. Daiko, T. Fujita / International Journal of Surgery 19 (2015) 61e66

thoracoscopic resection and thoracoscopic esophagectomy in the

prone position (TSEP) in comparison with open thoracotomy for the
treatment of carcinoma of the esophagus [2].
Regardless of tumor location, nodal metastasis is often widespread in the 3 operative elds. In one series, the rates of abdominal
lymph-node metastasis from tumors in the upper, middle, and
lower thirds of the thorax were 10%, 74%, and 40%, respectively [3].
Both the open and laparoscopic approaches are associated with a
signicant incidence of reconstruction-related complications.
Anastomotic leakage is a leading cause of operative mortality and
remains responsible for approximately one-third of operative
deaths [4]. For these reasons, the method of alimentary tract
reconstruction is of particular importance in determining perioperative outcomes and the oncological completeness of resection.
However, the laparoscopic approach for reconstruction and
abdominal lymph-node dissection has not, to our knowledge, been
reported, and its technical and oncological feasibility has not been
evaluated in comparison with open laparotomy.
The aim of the present study was to evaluate the technical and
oncological feasibility of alimentary tract reconstruction with laparoscopically assisted gastric pull-up (LAG) following TSEP in
comparison with open laparotomy gastric pull-up (OLG) following
TSEP, to establish TLE with extended lymph node dissection as a
standard operation for esophageal cancer.

2. Materials and methods

2.1. Patients population
Since September 2008, previously untreated clinical stage I
esophageal cancer has been treated with TSEP and 3-eld lymphnode dissection at the National Cancer Center Hospital East. We
have previously reported the oncological feasibility of TSEP with
3-eld lymph node dissection for clinical stage I esophageal
cancer [2]. Since April 2010, the indications for TSEP with 3-eld
lymph node dissection have been expanded to include clinical
stages T1 to T3 without metastasis to thoracic lymph nodes, and
reconstruction with LAG after esophagectomy has been performed for patients without metastasis to abdominal lymph
nodes. From September 2008 through June 2011, TSEP with 3eld lymph node dissection was performed for 64 patients: 33
of these patients underwent gastric reconstruction with OLG via
the posterior mediastinal route, and 31 patients without metastasis to abdominal lymph nodes underwent LAG via the retromediastinal route.
All patients were evaluated and underwent disease staging with
preoperative computed tomographic scans of the neck, chest, and
abdomen; barium swallow examination; endoscopy with biopsy;
and ultrasonography of the neck. Endoscopic ultrasonography was
performed to conrm the presence of submucosal cancer, when the
tumor was suspected to not be restricted to the mucosa. Indications
for denitive operation with extended lymph-node dissection were
submucosal cancer and mucosal cancer with circumferential
spread, for which endoscopic mucosal resection is not indicated.
Comprehensive evaluations of cardiac and respiratory functions
showed that all patients could tolerate anesthesia and operation.
Before surgery and just before discharge after surgery, respiratory
function was assessed with spirometry, including determinations
of vital capacity (VC), percent predicted vital capacity (%VC), forced
vital capacity (FVC), forced expiratory volume in 1 s (FEV1.0), and
FEV1.0 as a percentage of FVC (FEV1.0%). Informed consent was
obtained from all patients. Clinical and pathological staging was
based on the 1997 TNM classication of the International Union
Against Cancer.

2.2. Statistical analysis

Survival time was measured from the date of surgery until death
or the most recent follow-up examination. Length of survival was
determined with the KaplaneMeier method, and the log-rank test
was used for comparisons. The x [2] test and Fisher's exact probability test were used for comparing percentages. A p-value of less
than 0.05 was considered to indicate signicance. All analyses were
performed with the IBM SPSS Statistics software package (IBM
Corp., Armonk, NY).
2.3. Surgery
The operation consists of 3 stages, as previously described in
detail [2]. Stage 1 involves the thoracic eld and includes TSEP and
thorascopic mediastinal lymph-node dissection through 4 or 5
ports. Stage 2 involves the abdominal eld and includes gastric
mobilization and abdominal lymph-node dissection with open
laparotomy or the laparoscopic approach. Stage 3 involves the
cervical eld and includes anastomosis and cervical lymph-node
dissection.
2.4. Stage 1: thoracic stage (TSEP)
After intubation, the patient is placed in the prone position upon
operative beanbags with a blocking balloon in the right main
bronchus for single-lung ventilation.
The port positions are as follows (Fig. 1). Port I is 12-mm blunt
port in the 4th intercostal space (ICS) on the posterior axillary line.
Port II, placed under thoracoscopic guidance, is a 12-mm port in the
5th ICS on the anterior axillary line. Port III is a 12-mm port in the
3rd ICS on the midaxillary line. Port IV is a 5-mm port in the 8th or
9th ICS on the midaxillary line to insert a camera for procedures of
the middle-to-lower mediastinum. Port V is a 5-mm port in the 5th
ICS just under the angle of the scapula to insert a camera for procedures of the upper mediastinum. Carbon dioxide is insufated at
a pressure of 8 mm Hg to expand the mediastinum.

Fig. 1. Port placement and skin incisions. Filled circle, Filled circle: 5-mm port; lled
square: 12-mm port. Dotted line is additional minilaparotomy 3e4 cm in diameter.

H. Daiko, T. Fujita / International Journal of Surgery 19 (2015) 61e66

2.5. Thoracoscopic mobilization of the middle-to-lower esophagus

The middle-to-lower esophagus is circumferentially mobilized
from the descending aorta, pericardium, and the left mediastinal
pleura from below the arch of the azygos vein to the diaphragmatic
hiatus. Mobilization of the middle-to-lower esophagus was achieved through en-bloc lymph-node dissection including the middle
mediastinal nodes (subcarinal, bilateral main bronchial, and the
middle paraesophageal lymph nodes) and the lower mediastinal
nodes (lower thoracic paraesophageal, posterior mediastinal, and
supradiaphragmatic lymph nodes).
2.6. Thoracoscopic mobilization of the upper esophagus
Mobilization of the upper esophagus was achieved through enbloc lymph-node dissection including the upper mediastinal nodes
(upper thoracic paraesophageal lymph nodes and thoracic paratracheal lymph nodes, including the bilateral recurrent laryngeal
nerve nodes and infra-aortic arch nodes). The most important point
for lymph-node dissection around the recurrent laryngeal nerve is
to keep the nerve under tension. The right recurrent laryngeal
nerve can be kept tense by taping the right vagus nerve with vessel
loops. On the left side, retraction of the upper third of esophagus
creates tension on the left recurrent laryngeal nerve through its
esophageal branch. Moreover, retracting the esophagus leftward
and dorsally by pulling the tape extrathoracically and by retracting
the trachea rightward and ventrally provides better visualization
and clearance of the left recurrent laryngeal nerve and lymph nodes
around the nerve and simplies lymph nodes dissection without
injuring the left recurrent laryngeal nerve.

63

of the peritoneal cavity, and a gastric tube is created with a linear

stapler.
2.8. Open laparotomy
An upper abdominal incision 30 cm in diameter is made from
xiphoid process to above the umbilicus. Gastric mobilization and
lymph node dissection are performed as in LAG.
2.9. Stage 3: cervical stage
The procedures in the cervical eld include anastomosis and
cervical lymph-node dissection. The cervical lymph nodes
comprise the supraclavicular and cervical paraesophageal lymph
nodes. The alimentary tract was restored with reconstruction of the
stomach through a mediastinal route in 64 patients. Anastomoses
in all patients were performed in an end-to-end manner with
Gambee's method and hand-sewing at the neck.
3. Results
3.1. Clinical and pathological characteristics of TSEP with 3-eld
lymph node dissection according to method of gastric pull-up
Of the patients who underwent TSEP with 3-eld lymph node
dissection, those who underwent LAG had more advanced disease,
as indicated by clinical and pathological stages (Table 1), than did
patients who underwent OLG.

2.7. Stage 2: abdominal stage; LAG

After the thoracic esophagus is mobilized with dissection of
lymph nodes in the upper-to-lower mediastinum, the patient is
placed in the supine position and receives bilateral-lung ventilation. The port positions are as follows (Fig. 1). A 12-mm camera
blunt port is created below the umbilicus, and carbon dioxide is
insufated at a pressure of 12 mm Hg to expand the abdomen. Four
other ports (two 12-mm ports and two 5-mm ports) are inserted
under laparoscopic guidance. Under laparoscopic guidance, the
gastrocolic ligament is rst divided along the border of the transverse colon using ultrasonic shears (Harmonic Scalpel; Ethicon
Endo-Surgery Inc., Cincinnati, OH, USA). The greater omentum is
completely preserved because of the arcade of right and left gastroepiploic veins and arteries. The entire greater omentum is
mobilized from transverse colon until the inferior portion of the
spleen, and the root of the left gastroepiploic vein and artery are
isolated and sealed with ultrasonic shears. The division of the
greater omentum is continued toward the hilum of the spleen, and
the gastrosplenic ligament, including the short gastric vein and
artery, is divided until the upper pole of the spleen by means of
ultrasonic shears. The adipose tissue, including lymph nodes along
the celiac artery and left gastric artery, is dissected, and the left
gastric vein and artery are exposed and divided with ultrasonic
shears and clips. After the lesser omentum is sealed and resected
along the liver edge up to the esophagogastric junction, the
abdominal esophagus is mobilized, and the thoracic esophagus
including the primary tumor is removed through the thoracic inlet.
We also partially divide the left crus and anterior diaphragm to
allow easy passage of the gastric specimen and tube through the
hiatus and to prevent gastric outlet obstruction. After gastric
mobilization has been achieved, a 3- to 4-cm minilaparotomy is
made by cranially extending the camera port below the umbilicus.
Through this minilaparotomy, the mobilized stomach is pulled out

Table 1
Clinical and pathological characteristics of TSEP with 3-eld lymph node dissection
according to method of gastric pull-up.

Number of Patients
Sex
male/female
Age, years
Median (range)
Location of tumors
Upper thorax
Middle thorax
Lower thorax
Clinical T status
cT1
cT2
cT3
Clinical N status
cN0
cN1
Clinical stage
I
IIA/IIB
III
Pathological T status
pT1
pT2
pT3
Pathological N status
pN0
pN1
Pathological stage
I
IIA/IIB
III
IVA

Total

OLG

LAG

64

33

31

56/8

28/5

28/3

66 (49e78)

65 (49e76)

66 (49e78)

7
23
34

7
14
12

0
9
22

45
6
13

30
1
2

15
5
11

60
4

31
2

29
2

43
16/3
2

29
2/1
1

14
14/2
1

46
7
11

28
4

18
3
10

45
19

27
6

18
13

37
6/12
6
3

24
2/6
0
1

13
4/6
6
2

P Value
0.71
0.45
0.01

0.001

1.0

0.002

0.002

0.035

0.05

OLG: open laparotomy gastric pull-up.

LAG: laparoscopically assisted gastric pull-up.

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H. Daiko, T. Fujita / International Journal of Surgery 19 (2015) 61e66

3.2. Surgical outcomes of TSEP with 3-eld lymph node dissection

according to method of gastric pull-up

3.4. Restoration rate of respiratory function between before and

after operation

Conversion to an open thoracotomy procedure was required in 3

patients (5%); however, conversion to open laparotomy was not
required. Eventually, microscopically complete resection (R0) was
possible in 32 of 33 (97%) patients undergoing TLE with 3-eld
lymph node dissection. The mean number of lymph nodes harvested in the abdomen, the amount of blood loss in the abdomen,
and the rate of complete resection (R0) did not differ signicantly
between patients undergoing OLG and those undergoing LAG.
However, the total duration of all procedures, the duration of the
thoracic phase, and the duration of the abdominal phase were
greater in patients undergoing LGA (Table 2).

The rate of restoration of spirometric variables (VC, %VC, FVC,

FEV1.0 and FEV1.0%) to preoperative levels did not differ signicantly between patients undergoing OLG and those undergoing
LAG (Table 4).

3.3. Postoperative course and complications of TSEP with 3-eld

lymph node dissection according to method of gastric pull-up

3.5. Pattern of rst failure of TSEP with 3-eld lymph node

dissection according to method of gastric pull-up
Disease recurred in 3 of 33 patients who underwent OLG and in
4 of 33 patients who underwent LAG. The rate of recurrence did not
differ signicantly between the patient groups. In particular,
recurrence in the abdominal eld was not detected in any patient
(Table 5).
4. Discussion

The incidence of postoperative morbidity was 36% in patients

undergoing OLG and 32% in patients undergoing LAG. The rate of
complications did not differ signicantly between the patient
groups. No in-hospital deaths occurred in either group (Table 3).

Surgical therapy has traditionally been considered the optimal

treatment for esophageal cancer in terms of locoregional control
and long-term survival [5]. In the treatment of esophageal cancer,

Table 2
Surgical outcomes of TSEP with 3-eld lymph node dissection according to method of gastric pull-up.

Number of Patients
Conversion to open procedure
to thoracotomy
to laparotomy
Operation time (minutes)
Mean (range)
Total
Thoracic phase
Abdominal phase
Amount of blood loss (ml)
Mean (range)
Total
Thoracic phase
Abdominal phase
Number of dissected lymph nodes
Mean (range)
Total
Thoracic phase
Abdomen
Completeness of resection
R0
R1

Total

OLG

LAG

64

33

31

P Value

3
0

1
0

1.0

409 (297e569)
217 (123e325)
161 (90e248)

390 (297e480)
233 (147e325)
131 (90e235)

429 (308e569)
200 (123e256)
194 (145e248)

0.009
0.006
0.0001

396 (28e4225)
157 (5e4138)
238 (1e1131)

498 (28e4225)
250 (5e4138)
249 (40e618)

286 (50e1183)
59 (8e263)
227 (1e1131)

0.13
0.15
0.71

57 (20e88)
24 (6e44)
15 (5e31)

57 (26e88)
23 (7e39)
15 (5e31)

58 (20e85)
25 (6e44)
15 (5e29)

0.77
0.24
0.56
1.0

63
1

32
1

31
0

OLG: open laparotomy gastric pull-up.

LAG: laparoscopic assisted gastric pull-up.

Table 3
Postoperative course and complications of TSEP with 3-eld lymph node dissection according to method of gastric pull-up.

Number of Patients
Deaths
Morbidity: number of cases (%)
Pneumonia
Recurrent laryngeal nerve palsy
Anastomotic leakage
Surgical site infection
Chylothorax
Postoperative hospital stay, days
Mean (range)
OLG: open laparotomy gastric pull-up.
LAG: laparoscopic assisted gastric pull-up.

Total

OLG

LAG

64
0
22 (34)
0
9 (14)
10 (16)
5 (9)
3 (5)

33
0
12 (36)
0
6 (18)
4 (12)
5 (15)
1 (3)

31
0
10 (32)
0
3 (10)
6 (19)
0
2 (6)

20 (10e76)

19 (13e51)

20 (10e76)

P Value

0.80
0.48
0.50
0.05
0.61
0.76

H. Daiko, T. Fujita / International Journal of Surgery 19 (2015) 61e66

65

Table 4
Restoration rate of respiratory function between before and after operation according to method of gastric pull-up.
Before
VC (L)
%VC
FVC (L)
FEV1.0 (L)
FEV1.0%

3.3
97.5
3.2
2.4
77.0

OLG after
0.7
17.4
0.7
0.6
6.1

2.4
71.0
2.3
1.8
75.0

0.7
15.6
0.6
0.5
15.4

Restoration rate
72.3
73.2
73.1
72.1
97.3

14.0
14.5
14.5
14.2
8.3

Before
3.5
110.9
3.5
2.7
75.3

LAG after
0.6
17.2
0.6
0.4
9.0

2.6
81.3
2.6
2.0
77.0

0.6
16.1
0.6
0.5
13.2

Restoration rate
74.7
73.5
73.3
72.4
131.5

11.0
10.4
10.4
14.0
172.0

P Value
0.51
0.93
0.93
0.94
0.37

OLG: open laparotomy gastric pull-up.

LAG: laparoscopic assisted gastric pull-up.

Table 5
Pattern of rst failure of TSEP with 3-eld lymph node dissection according to
method of gastric pull-up.

Number of Patients
Median follow-up time, days
Pattern of recurrence: n
Locoreginal
Thorax
Abdomen
Distant
Both

Total

OLG

LAG

64
601
7
2
2
0
4
1

33
784
3
2
2
0
0
1

31
412
4
0
0
0
4
0

P Value

0.70

OLG: open laparotomy gastric pull-up.

LAG: laparoscopic assisted gastric pull-up.

the trauma and invasiveness associated with esophagectomy are

greater than those of other surgical interventions. The signicant
trauma associated with thoracotomy or laparotomy or both is a key
disadvantage and induces a pronounced systemic inammatory
response [6]. The conventional open surgical procedure, which
includes thoracotomy, laparotomy, or both, is associated with signicant morbidity and mortality and a delay in return to the preoperative level of activity [7,8]. Recently, a type of MIE for
esophageal cancer including thoracoscopic procedures or laparoscopic procedures or both has been performed and its surgical
benets have been assessed. Several studies of thoracoscopic MIE
have been performed. Several different techniques for thoracoscopic MIE have been described and have been found to be equal to
open thoracotomy in terms of technical and oncological feasibility.
Furthermore, thorascopic surgery has the advantages of shorter
intensive care unit stays and hospital stays after surgery, a weaker
systemic inammatory response, less blood loss, and lower rates of
surgical site infection, blood transfusion, and postoperative complications, especially pulmonary complications [9e20].
Two different surgical positions are used for procedures in the
thoracic stage: the left lateral decubitus position and the prone
position. First described by Cuschieri and colleagues in 1994, TSEP
has attracted attention as a potentially less-invasive procedure [21].
Recent reports on the use of TSEP have stimulated new interest in it
and have described short-term perioperative outcomes
[2,9,14,16,20,22,23]. Because of the effects of gravity with the patient in the prone position, the esophagus is well-visualized,
dissection is simpler because the esophagus falls anteriorly from
its normal position, the lungs and heart require no retraction, and
blood pools outside the operative eld [2,14,22]. Moreover, with the
patient in the prone position, neither a skilled assistant surgeon nor
an endoscopist is required [2]. The technical and oncological
feasibility of TSEP has been conrmed to be equal to that of open
thoracotomy [2,9,14,16,20]. However, these reports demonstrating
the advantages of TSEP did not evaluate its technical and oncological feasibility for abdominal surgical procedures. Surgery for
esophageal cancer consists of thoracic, abdominal, and cervical
phases, and an MIE for esophageal cancer is TLE, which consists of
thoracoscopic resection and laparoscopic reconstruction. Moreover,

the abdominal phase is of particular importance for the perioperative outcome and oncological completeness of resection.
In the present study, we have demonstrated the technical and
oncological feasibility of LAG in comparison with conventional
open abdominal procedures for esophageal cancer. We found no
signicant differences between LAG and OLG in the mean number
of dissected abdominal lymph nodes, volume of blood loss, incidence of postoperative complications, mean postoperative hospital
stay, restoration rate of respiratory function, or rate of complete
resection or locoregional control, but the mean duration of
abdominal procedure was signicantly longer for LAG than for OLG.
Pulmonary function is suppressed after abdominal surgery
because of diaphragmatic dysfunction and postoperative pain.
Several randomized trials have demonstrated that FVC and FEV1.0
value are suppressed less after laparoscopic cholecystectomy than
after open procedures [24e26]. However, Kitano et al. have reported that the suppression of FVC differs signicantly between
laparoscopically assisted distal gastrectomy and open distal gastrectomy but that the suppression of FEV1.0 does not [27]. Moreover, Stage et al. have found no signicant difference in pulmonary
function between a laparoscopic colectomy and open colectomy
[28]. Whether laparoscopic surgery or open surgery causes greater
suppression of pulmonary function remains controversial. Therefore, a study with a large number of cases is necessary to investigate
the effects of laparoscopic surgery and open surgery on pulmonary
function.
A previous study has demonstrated the safety and oncological
feasibility of throacoscopic MIE but did not assess the technical and
oncological feasibility of LAG compared with conventional open
abdominal procedures for esophageal cancer [2]. The present
report is, to our knowledge, the rst to demonstrate the technical
and oncological feasibility of alimentary tract reconstruction with
LAG following TSEP and extended lymph-node dissection for
esophageal cancer. The safety and oncological effectiveness of
reconstruction with LAG following TSEP are comparable to those of
reconstruction with OLG. For these reasons, we believe TLE consisting of TSEP followed by LAG has the potential to become a
standard surgical treatment and the ultimate minimally invasive
surgery for esophageal cancer.
This study demonstrates that the quality and safety of surgery
and the oncological effectiveness of LAG for esophageal cancer. We
conclude that TLE, consisting of TSEP followed by LAG with
extended lymph node dissection, is a feasible surgical technique for
thoracic esophageal carcinoma.
Conict of interest
None.
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