UPPER GI SURGERY

▲
Minimally invasive Ivor–Lewis oesophagectomy is a feasible and safe
approach for patients with oesophageal cancer

Xinyu Mei,*† Meiqing Xu,† Mingfa Guo,† Mingran Xie,† Changqing Liu† and Zhou Wang*
*Department of Thoracic Surgery, Shandong Provincial Hospital affiliated to Shandong University, Jinan, China and
ANZJSurg.com

†Department of Thoracic Surgery, Anhui Provincial Hospital, Hefei, China

Key words Abstract

minimally invasive surgery, oesophageal cancer,
oesophagectomy.
Correspondence
Professor Zhou Wang, Department of Thoracic Surgery,
Shandong Provincial Hospital affiliated to Shandong
University, No. 324, Jinwu Weiqi Road, Jinan 250021,
China. Email: zwsdslyy@163.com
X. Mei MBBS; M. Xu MBBS; M. Guo MBBS; M. Xie
PhD; C. Liu MBBS; Z. Wang PhD.
Accepted for publication 14 March 2015.
doi: 10.1111/ans.13161
Background: Minimally invasive approaches are increasingly being used in
oesophagectomy. The aim of this study was to compare the short-term clinical out-
comes of the minimally invasive Ivor–Lewis oesophagectomy (MIILE) technique with
those of the open Ivor–Lewis oesophagectomy (OILE) technique.
Methods: We identified 131 patients who underwent MIILE combined with
thoracoscopy and laparoscopy. These patients were compared with 248 patients who
underwent OILE between January 2012 and December 2013.
Results: MIILE and OILE produced similar post-operative hospital mortality (MIILE
2.3 versus OILE 2%; P = 1.000). The MIILE approach was associated with a signifi-
cant decrease in the time until chest drain removal (MIILE 9.07 ± 5.075 days versus
OILE 11.26 ± 6.989 days; P = 0.002) and post-operative length of stay (MIILE 10.89
± 4.976 days versus OILE 12.83 ± 6.921 days; P = 0.002). Pneumonia was the most
common complication in both groups. MIILE patients exhibited a lower incidence of
post-operative pneumonia (MIILE 17.6% versus OILE 28.2%; P = 0.024) compared
with OILE. The survival rate did not significantly differ between the MIILE and OILE
groups (1-year survival rates: MIILE 86 versus OILE 88.2%; P = 0.537).
Conclusions: In this study, we demonstrate that MIILE is a feasible and safe
approach for patients with middle or lower oesophageal cancer.

Introduction present report is the initial analysis of our experience with

Oesophageal cancer is the eighth most common cancer worldwide,
causing more than 400 000 deaths in 2008.1 In cases with resectable
disease, surgery is the gold standard for treatment. Minimally
invasive oesophagectomy (MIE) was first reported by Cuschieri
and colleagues in 1992.2 The minimally invasive approach for
oesophagectomy includes three main approaches:3 (i) laparoscopic
transhiatal oesophagectomy with anastomosis in the neck; (ii)
laparoscopic and thoracoscopic minimally invasive Ivor–Lewis
oesophagectomy (MIILE); and (iii) laparoscopic and thoracoscopic
oesophagectomy with anastomosis in the neck (minimally invasive
McKeown oesophagogastrectomy).
The majority of published series report the outcomes of McKeown
oesophagogastrectomy.4,5 There are few reports on minimally inva-
sive Ivor–Lewis.6–8 Minimally invasive intrathoracic anastomosis
includes two main approaches: (i) circular-stapled anastomosis with
the transoral anvil technique (Orvil)9,10 and (ii) circular-stapled anas-
tomosis with the Premium Plus CEEA anvil technique.11
We began using MIILE with the Premium Plus CEEA (Covidien,
Minneapolis, MN, USA) anvil technique in October 2011. The
oesophagectomy based on a comparative study of MIILE and open
Ivor–Lewis oesophagectomy (OILE), with particular focus on the
perioperative outcomes and post-operative complications.
Methods
General information
From January 2012 to December 2013, 743 patients with oesophageal
cancer underwent oesophagectomy. Based on the database, we veri-
fied and updated the clinical data in the patient records through April
2014. Patients were selected based on the following eligibility crite-
ria: (i) histopathologically proven oesophageal cancer; (ii) tumours
located in the middle or lower third of the oesophagus; (iii) clinical
T1-3N0-1M0 disease prior to operation; and (iv) no known distant
metastasis. Patients were excluded if they met one of the following
criteria: (i) received palliative resection; (ii) incomplete medical
records; or (iii) received neoadjuvant chemoradiation. Finally, 379
patients were enrolled in this retrospective study; 131 patients under-
went the MIILE approach and 248 patients underwent the OILE

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J Surg 86Australasian College of Surgeons
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2Minimally invasive Ivor–Lewis oesophagectomy
743 patients received
oesophagectomy
Eligibility and exclusion criteria
364 patients received McKeown oesophagectomy
and left transthoracic oesophagectomy
379 patients received Ivor–Lewis oesophagectomy
(Divided the patients into two groups according
to the operation approach)
MIILE group (131) OILE group (248)
Compared the patient Compared the surgical,
demographics between pathologic and survival
the two groups data between the two groups
approach. Other patients who underwent McKeown oesophago-
gastrectomy, left transthoracic approach oesophagogastrectomy or
patients whose tumour staging was higher than cT1-3N0-1 M0 were
not enrolled in this study (Fig. 1).
Patients who underwent Ivor–Lewis oesophagectomy were staged
according to the TNM staging system of the American Joint Committee
on Cancer (AJCC Staging Manual, 7th edition). The criterion for patient
selection for OILE was the same as for MIILE. MIILE was recom-
mended for all patients with preoperative cT1-3N0-1M0 staging. Some
patients underwent OILE due to fear regarding the risk of the new
technology or concerns about the high cost of the operation. The study
was approved by the Ethics Committee of Anhui Provincial Hospital.
The collected data included clinical characteristics, surgical and
pathologic data and post-operative complications.
An R0 resection was defined as tumour >1 mm from the resection
margin. Pathologic tumour clearance was determined according to
the Royal College of Pathologists system. An involved circumferen-
tial resection margin (R1) was defined in any case in which tumour
was found within 1 mm of the resection margin.8
Surgical technique for MIILE
Laparoscopy
Each patient was placed in a supine position after general anaesthesia.
Five abdominal ports (5–12 mm) were used (Fig. 2a). Using these ports,
the lesser omental bursa was opened, and then the gastro-hepatic liga-
ment and lymph nodes of the left gastric pedicle were dissected. The
stomach was elevated from the lesser curvature, and the left gastric
pedicle was exposed. The left gastric artery was ligated at its origin
using a Hem-o-lok clip (Teleflex Incorporated, Wayne, PA, USA) and
© 2015 Royal Australasian College of Surgeons
Mei et275
al.
Fig. 1. Flow diagram of the study.
MIILE, minimally invasive Ivor–Lewis
oesophagectomy; OILE, open Ivor–
Lewis oesophagectomy.
Compared the
post-operative data between
the two groups
then dissected with an ultrasound scalpel. The lymph nodes of the celiac
axis, common hepatic artery and lesser curvature were dissected during
the mobilization of the lesser curvature of the stomach. The greater
curvature of the stomach was mobilized by dividing the short gastric
vessels and then preserving the right gastroepiploic vessels. The lymph
nodes of the greater curvature along the short gastric arteries and splenic
artery were dissected. After gastric mobilization, the subxiphoid port
was extended to 5 cm. The oesophagogastric junction was dissected
circumferentially at the level of the hiatus, and the distal gastric tissue
was removed through the subxiphoid incision (Fig. 2b). A 4- to 5-cm
wide gastric conduit was created along the lesser curvature of the
stomach in the direction of the gastric angle using a GIA linear stapler
(Covidien). The gastric conduit was then attached to the oesophagus
with interrupted sutures. The four ports were closed, and the subxiphoid
incision was temporarily closed.
Thoracoscopy
Each patient was repositioned in the left lateral decubitus position with
the right lung deflated using double-lumen tube intubation during the
thoracic procedure. Thoracoscopic mobilization of the oesophagus was
performed using a three-port technique (Fig. 2c). A sponge holding
forceps was used to provide downward traction on the lung and to
facilitate the exploration of the mediastinum from the posterior port.
The mediastinal pleura overlying the oesophagus was divided, and the
azygous vein was then ligated at its two sides using Hem-o-lok clips and
dissected using the ultrasound scalpel. The thoracic oesophagus with
the perioesophageal tissue was circumferentially mobilized from the
diaphragm to the roof of the pleural cavity. The paraoesophageal lymph
nodes and the right recurrent laryngeal nerve nodes were dissected
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(a) (b) (c)

(d) (e) (f )

Fig. 2. (a) The locations of the laparoscopic port sites. A transumbilical approach was used to insert the 12-mm camera port. Two 5-mm ports were placed
in the right and left lateral subcostal positions. A 5-mm port was placed subxiphoid, and a 12-mm port was inserted into the right lateral portion of the rectus
abdominis at the level of the umbilicus. (b) The subxiphoid incision and the gastric conduit. (c) The locations of the thoracoscopic port sites. The observation
port (1 cm) was placed in the seventh intercostal space at the middle axillary line. The anterior operating port (4 cm) was placed in the fourth intercostal
space at the anterior axillary line. The port site was later used for the stapler. The posterior operating port (2 cm) was located in the eighth intercostal space
at the posterior axillary line. (d) The purse-string device. (e) The anvil was placed inside the oesophagus, and the purse-string line was tied. (f) The spike
was removed from the side of the conduit and docked into the anvil.

during the oesophageal mobilization. After full mobilization of the
thoracic oesophagus, a purse-string clamp device (Shanghai Medical
Instruments Ltd, Shanghai, China) was inserted through the anterior
operating port located on the anterior axillary line and secured with a
purse-string suture 5 cm above the upper margin of the tumour. A
Premium Plus CEEA anvil was placed inside the oesophagus, and the
purse-string line was tied using a knot pusher (Fig. 2d,e). The distal
oesophagus was transected and removed through the anterior operating
port. Then, the left recurrent laryngeal nerve nodes, subcarinal nodes
and nearby hilar nodes were explored and completely dissected using an
ultrasound scalpel. At least 15 lymph nodes were removed to achieve
adequate nodal staging. The gastric conduit was then grasped and pulled
into the right thoracic cavity. A gastrotomy was performed at the tip of
the gastric conduit, and the Premium Plus CEEA shaft was placed into
the gastric conduit through the anterior operating port. The spike from
the Premium Plus CEEA was removed from the side of the conduit and
docked into the anvil (Fig. 2f). The Premium Plus CEEA was then fired
and removed. At this point, a linear stapler (Ethicon, Somerville, NJ,
USA) was used to amputate and close the defect at the tip of the gastric
conduit and remove it from the chest through the anterior operating port
after the anastomosis was completed. A 32-French chest tube was
placed for chest drainage through the observation port, and a Jackson
Pratt drain (Suzhou Medical Equipment Ltd, Suzhou, Jiangsu, China),
which offered negative pressure drainage, was placed in the oesopha-
geal bed for mediastinal drainage through the posterior operating port,
which was located on the posterior axillary line. The operating table was
then tilted 45 degrees to the left, the temporary abdominal incision was
reopened and an indwelling duodenal nutrition tube was placed from
the nose. All ports and incisions were then closed.
Surgical technique for OILE
The OILE was performed as described by Lewis.12 Each patient was
placed under general anaesthesia. Laparotomy (10–15 cm) and
thoracotomy (15–30 cm) procedures were performed. The stomach,
oesophagus and all paraoesophageal lymph nodes were mobilized as
for MIILE. The specimen was resected, and an anastomosis was
constructed between the stomach and the oesophagus using
Premium Plus CEEA. Chest tubes, a Jackson Pratt drain and a
duodenal nutrition tube were placed as with the MIILE procedure,
and the thoracic incision was closed.
Post-operative management
All patients received patient-controlled analgesia post-operatively.
The chest drainage data were collected. The criteria for chest drain
removal were thoracic drainage fluid of less than 100 mL and a
post-operative X-ray indicating the absence of pleural effusion. A
post-operative oesophagogram was used to identify the anastomotic
fistula. The post-operative pulmonary complications included post-
operative pneumonia, pulmonary atelectasis, respiratory failure and
acute respiratory distress syndrome (ARDS).13,14 The criterion for a
pneumonia diagnosis was an infiltrative shadow on a chest radio-
graph, white blood count abnormalities and purulent sputum.15

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4Minimally invasive Ivor–Lewis oesophagectomy
Statistical analyses
Statistical analysis was performed using SPSS software version 16
(SPSS Inc, Chicago, IL, USA). For these analyses, continuous variables
were analysed using a two-tailed, unpaired t-test or Fisher’s exact tests,
and categorical data were analysed using chi-square testing. Kaplan–
Meier plots were used to determine the survival distribution. A multi-
variate analysis of survival was performed using Cox regression
analysis to identify the independent prognostic variables. Statistical
significance was set at P < 0.05 throughout the study.
Results
There were no differences in terms of age, sex, smoking history,
American Society of Anesthesiologists grade and incidence of
co-morbidities between the two groups (Table 1).
Surgical data
There were three conversions from thoracoscopic surgery to open
surgery. The indications for conversion included superior vena cava
bleeding, tracheal tearing and extensive pleural adhesions. There were
no conversions from laparoscopy to open surgery. There was a differ-
ence between the two groups in the mean estimated blood loss (MIILE
198.60 ± 49.841 mL versus OILE 210.76 ± 65.920 mL; P = 0.045).
The rate of R0 resections was 74.8% in the MIILE group and 73.4%
in the OILE group. There were no involved longitudinal resection
margins. There was no significant difference between the MIILE and
OILE groups in terms of the operation time, total number of lymph
nodes dissected or the stations of the dissected lymph nodes.
The median time until chest drain removal in the MIILE group
was shorter than that in the OILE group (MIILE 9.07 ± 5.075 versus
OILE 11.26 ± 6.989 days; P = 0.002). The MIILE group had a
shorter post-operative length of stay compared with the OILE group
(MIILE 10.89 ± 4.976 versus OILE 12.83 ± 6.921 days; P = 0.002).
The median follow-up was 18 months (range 1–34 months,
MIILE: 19 months versus OILE: 18 months). The survival rate
exhibited a significant correlation with the tumour stage (P < 0.001)
but had no significant correlation with the patient group (P = 0.537)
or histological findings (P = 0.835) (Table 2).
Table 1 Patient demographics
Characteristics MIILE (n = 131)
Age (year, mean ± SD) 62.95 ± 8.051
Sex (male/female) 100 (76.3%)/31 (23.7%)
Preoperative smoker (yes/no) 73 (55.7%)/58 (44.3%)
Co-morbidities 16 (12.2%)
ASA grade
I 46 (35.1%)
II 62 (47.3%)
III 23 (17.6%)
Weight (kg) 63.01 ± 7.543
Preoperative stage
IA 23 (17.6%)
IB 22 (16.8%)
IIA 41 (31.3%)
IIB 34 (25.9%)
IIIA 11 (8.4%)
ASA, American Society of Anesthesiologists; MIILE, minimally invasive Ivor–Lewis oesophagectomy; OILE, open Ivor–Lewis oesophagectomy; SD, standard
deviation.
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Perioperative complications
The hospital mortality rate was 2.3% in the MIILE group and 2.0%
in the OILE group (P = 1.000). In the MIILE group, two patients
died from an anastomotic leak and multiorgan failure, and one
patient developed severe pneumonia and ARDS that eventually
resulted in death. In the open group, two patients with an
anastomotic leak developed alimentary tract haemorrhage that led to
death, two patients died from post-operative ARDS and sudden,
unexplained death occurred in one patient with pneumonia.
Complications, according to the Clavien–Dindo classification,16 were
reported in 129 patients (34.0%). Major complications (Clavien–Dindo
grades 3–5: requiring surgery, life-threatening complication or death as
a result of complications) were observed in 66 (17.4%) of 379 patients
and included reoperation, sudden death, anastomotic leak, ARDS and
more. Minor complications (Clavien–Dindo grades 1–2) were observed
in 63 (16.6%) patients and included post-operative pneumonia, recur-
rent laryngeal nerve damage, arrhythmia, mild air leak, thoracic cavity
infection, wound infection, functional delayed gastric emptying and
more. Regarding overall complications, the incidences of complications
were 32.1% (42/131) and 35.1% (87/248) in the MIILE and OILE
groups, respectively.
There was a significant difference between the two groups in terms of
the pulmonary complications (MIILE 22.1% versus OILE 32.7%; P =
0.032) and post-operative pneumonia (MIILE 17.6% versus OILE
28.2%; P = 0.024). There were no significant differences between the
groups in terms of other minor complications (Table 3).
Discussion
MIE was first described in the early 1990s;2 most surgeons currently
prefer the combined thoracoscopic and laparoscopic approach with
cervical anastomosis.17,18 Compared with cervical anastomosis,
MIILE is thought to reduce the morbidity associated with recurrent
laryngeal nerve dysfunction,19,20 offer a better field of vision for
exposing the vascular and lymphatic vessels, allow for the creation
of a tension-free anastomosis between the remnant oesophagus and
the gastric conduit21 and produce fewer anastomotic strictures. Com-
OILE (n = 248) P-value
62.46 ± 8.230 0.572
190 (76.6%)/58 (23.4%) 0.530
115 (46.4%)/133 (53.6%) 0.083
30 (12.1%) 1.000
77 (31.0%) 0.622
119 (48.0%)
52 (21.0%)
64.04 ± 8.297 0.604
41 (16.5%) 0.322
54 (21.8%)
74 (29.8%)
47 (19.0%)
32 (12.9%)
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Mei et al.

Table 2 Surgical, pathologic and survival data

Characteristics MIILE (n = 131) OILE (n = 248) P-value

Surgical and pathologic data

Blood lose (mL) 198.60 ± 49.841 210.76 ± 65.920 0.045

Mean operating time (min) 252.73 ± 43.487 261.57 ± 46.036 0.066
Total lymph nodes dissected 30.15 ± 4.999 29.77 ± 5.397 0.505
Stations of the total lymph nodes dissected 12.80 ± 1.600 13.01 ± 1.670 0.237
Chest drain removal (d) 9.07 ± 5.075 11.26 ± 6.989 0.002
Post-operative length of stay (d) 10.89 ± 4.976 12.83 ± 6.921 0.002
Post-operative stage
IA 21 (16%) 32 (12.9%) 0.933
IB 19 (14.5%) 42 (16.9%)
IIA 37 (28.2%) 69 (27.8%)
IIB 30 (22.9%) 53 (21.4%)
IIIA 23 (17.6%) 50 (20.2%)
IIIB 1 (0.8%) 2 (0.8%)
Resection clearance
R0 98 (74.8%) 182 (73.4%) 0.807
R1 33 (25.2%) 66 (26.6%)
Histologic type
Squamous 121 (92.3%) 233 (94.0%) 0.642
Adenocarcinoma 9 (6.9%) 11 (4.4%)
Small-cell carcinoma 1 (0.8%) 3 (1.2%)
Carcinosarcoma 0 (0) 1 (0.4%)
Mean survival time (month) 28.27 ± 0.92 27.62 ± 0.66 0.537
1-year survival 86.0% 88.2% –

MIILE, minimally invasive Ivor–Lewis oesophagectomy; OILE, open Ivor–Lewis oesophagectomy.

Table 3 Post-operative data

Variable MIILE (n = 131) OILE (n = 248) P-value

Total complications 42 (32.1%) 87 (35.1%) 0.555

Clavien–Dindo grade – – –
Minor complications (class 1–2)
Recurrent laryngeal nerve damage 4 (3.1%) 9 (3.6%) 1.000
Functional delayed gastric emptying 2 (1.6%) 7 (2.8%) 0.724
Arrhythmia 5 (3.8%) 15 (6%) 0.471
Post-operative pneumonia 23 (17.6%) 70 (28.2%) 0.024
Chylothorax (without reoperation) 4 (3.1%) 8 (3.2%) 1.000
Air leakage (without reoperation) 1 (0.8%) 3 (1.2%) 1.000
Thoracic cavity infection 1 (0.8%) 5 (2%) 0.669
Wound infection 3 (2.3%) 13 (5.2%) 0.282
Major complications (class 3–4)
Thoracic haemorrhage 1 (0.8%) 2 (0.8%) 1.000
Anastomotic haemorrhage 2 (1.5%) 2 (0.8%) 0.611
Chylothorax 2 (1.5%) 1 (0.4%) 0.275
Diaphragmatocele 0 (0) 1 (0.4%) 1.000
Continuing air leakage 0 (0) 1 (0.4%) 1.000
Ventral incisional hernia 1 (0.8%) 0 (0) 0.346
Tracheal injury 1 (0.8%) 0 (0) 0.346
Anastomotic leak 4 (3.1%) 8 (3.2%) 1.000
ARDS 5 (4.6%) 9 (4.4%) 1.000
Mortality (in hospital) (class 5) 3 (2.3%) 5 (2.0%) 1.000
Anastomotic leak 2 (1.5%) 2 (0.8%)
ARDS 1 (0.8%) 2 (0.8%)
Sudden death 0 (0) 1 (0.4%)

ARDS, acute respiratory distress syndrome; MIILE, minimally invasive Ivor–Lewis oesophagectomy; OILE, open Ivor–Lewis oesophagectomy.

pared with the other reports,7,9 MIILE produced similar outcomes in
terms of the time to discharge and respiratory complication rates.
Minimally invasive intrathoracic anastomosis techniques include
the transoral anvil technique (Orvil)9,10 and circular-stapled anasto-
mosis with the Premium Plus CEEA anvil technique.11 Compared
with the transoral anvil technique (Orvil), circular-stapled anasto-
mosis with the Premium Plus CEEA anvil technique has two theo-
retical advantages. First, it avoids the chest contamination associated
with the trans-oral operation. Second, the use of surgical instruments
and operating costs are reduced. In our procedure, we report a
purse-string clamp device technique that is different from the hand-
sewn purse-string stapled anastomosis.11
A number of single-institution studies have demonstrated accept-
able short-term outcomes of MIE in terms of the operative time,
blood loss and number of lymph nodes harvested. We found that
MIILE was associated with a shorter post-operative hospital stay,

© 2015 Royal Australasian College of Surgeons © 2015 Royal Australasian College of Surgeons
6Minimally invasive Ivor–Lewis oesophagectomy
which is similar to previous reports.22,23 MIILE seems to have better
surgical outcomes than OILE.
In our procedure, there was no difference found in the hospital mor-
tality, which is similar to previous reports.8 Considering the incidence of
major surgery-related complications, MIILE is acceptable and similar to
OILE. The most serious post-operative complications associated with
oesophageal cancer surgery were ARDS and anastomotic leakage.
The most severe pulmonary complications following oesopha-
gectomy are pneumonia, ARDS and acute lung injury.24 Pneumonia is
the most common complication, and it is significantly associated with
the need for re-intubation, prolonged hospital stays and hospital mor-
tality.24 Consistent with other studies, the MIILE group had a lower rate
of post-operative pneumonia, and the difference was statistically sig-
nificant.19,24 The reduced post-operative pneumonia in the MIILE group
was most likely due to the following: (i) minimal lung retraction, which
caused less lung parenchymal injury compared with the OILE proce-
dure; (ii) the reduction in minimally invasive surgery trauma to the chest
wall muscles; and (iii) the reduction in the post-operative pain and easy
drainage of bronchial secretions. The reduced incidence of pneumonia
is beneficial for patients with old age, poor pulmonary function and
chronic obstructive pulmonary disease.
We routinely dissected the lymph nodes of the bilateral laryngeal
recurrent nerve, and there was no significant difference between the
two groups in terms of post-operative recurrent nerve palsy.
Thoracoscopy and laparoscopy provide a better field of view and can
be used to more clearly expose the vascular and lymphatic vessels.
In our procedure, the key aspect of the MIILE procedure is the use
of the purse-string clamp device technique with thoracoscopy. The
purse-string clamp device technique makes it technically less chal-
lenging to perform minimally invasive intrathoracic anastomosis in
the roof of the right pleural cavity.
A limitation of the study is the possibility of selection bias for
patients to undergo the minimally invasive approach, although the
demographic factors tend to exhibit no difference. In addition, there
were incomplete long-term survival data. The long-term oncologic
outcomes still need to be evaluated, and further prospective studies,
such as a large multicentre, randomized, controlled trial, are needed
to confirm these results.
Conclusions
The short-term results indicate that MIILE is a feasible and safe
approach for patients with middle or lower oesophageal cancer. This
approach has advantages in terms of the surgical outcomes and the
limited post-operative pneumonia.
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