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Chinese Medical Journal 2014;127 (4) 747

Original article
Comparative study of minimally invasive versus open esophagectomy
for esophageal cancer in a single cancer center
Mu Juwei, Yuan Zuyang, Zhang Baihua, Li Ning, Lyu Fang, Mao Yousheng, Xue Qi, Gao Shugeng, Zhao Jun,
Wang Dali, Li Zhishan, Gao Yushun, Zhang Liangze, Huang Jinfeng, Shao Kang, Feng Feiyue, Zhao Liang,
Li Jian, Cheng Guiyu, Sun Kelin and He Jie

Keywords: surgical procedures; minimally invasive; esophagectomy; comparative study

Background In order to minimize the injury reaction during the surgery and reduce the morbidity rate, hence reducing the
mortality rate of esophagectomy, minimally invasive esophagectomy (MIE) was introduced. The aim of this study was to
compare the postoperative outcomes in patients with esophageal squamous cell carcinoma undergoing minimally invasive
or open esophagectomy (OE).
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Methods The medical records of 176 consecutive patients, who underwent minimally invasive esophagectomy (MIE)
between January 2009 and August 2013 in Cancer Institute & Hospital, Chinese Academy of Medical Sciences, were
retrospectively reviewed. In the same period, 142 patients who underwent OE, either Ivor Lewis or McKeown approach,
were selected randomly as controls. The clinical variables of paired groups were compared, including age, sex, Charlson
score, tumor location, duration of surgery, number of harvested lymph nodes, morbidity rate, the rate of leak, pulmonary
morbidity rate, mortality rate, and hospital length of stay (LOS).
Results The number of harvested lymph nodes was not significantly different between MIE group and OE group (median
20 vs. 16, P=0.740). However, patients who underwent MIE had longer operation time than the OE group (375 vs. 300
minutes, P <0.001). Overall morbidity, pulmonary morbidity, the rate of leak, in-hospital death, and hospital LOS were not
significantly different between MIE and OE groups. Morbidities including anastomotic leak and pulmonary morbidity, in-
hospital death, hospital LOS, and hospital expenses were not significantly different between MIE and OE groups as well.
Conclusions MIE and OE appear equivalent with regard to early oncological outcomes. There is a trend that hospital
LOS and hospital expenses are reduced in the MIE group than the OE group.
Chin Med J 2014;127 (5): 747-752

E sophageal cancer is becoming a growing concern. It is


the eighth most common cause of cancer worldwide.1
The death rate of esophageal cancer in China ranks first in
open esophagectomy (OE).

METHODS
the world, with an incidence of 16.7 per 100 000 person-
years and a death rate of 13.4 per 100 000 person-years.2 General information
For resectable disease, surgery is the gold standard for the This study was approved by the Institutional Review
treatment. Five-year survival rate of esophageal cancer after Board of Cancer Institute & Hospital, Chinese Academy of
esophagectomy is about 30%. However, esophagectomy Medical Sciences. The medical records of 176 consecutive
is a complex procedure and carries a risk of morbidity patients, who underwent MIE between January 2009 and
rate from 23% to 50% and mortality rate from 2% to August 2013 in Cancer Institute & Hospital, Chinese
8%, respectively, in Western countries,3,4 and a morbidity Academy of Medical Sciences, were retrospectively
rate from 9% to 29% and mortality rate from 2% to 4%, reviewed. In the same period, 142 esophagectomies
respectively, in China.5,6 via open approach were selected randomly as controls.
The clinical variables of paired groups were compared,
In order to minimize the injury reaction during the surgery including age, sex, Charlson score, tumor location, duration
and reduce the morbidity rate, hence reducing the mortality of surgery, number of harvested lymph nodes, morbidity
rate of esophagectomy, minimally invasive esophagectomy
(MIE) was introduced into clinical practice in 1992 for the DOI: 10.3760/cma.j.issn.0366-6999.20132224
Department of Thoracic Surgical Oncology, Cancer Institute &
first time.7 Since then, surgeons have witnessed morbidity Hospital, Chinese Academy of Medical Sciences and Peking Union
rate from 11% to 25% and mortality rate from 1% to 3%, Medical College, Beijing 100021, China (Mu JW, Yuan ZY, Zhang
which are lower than previous reports of esophagectomy BH, Li N, Lyu F, Mao YS, Xue Q, Gao SG, Zhao J, Wang DL, Li ZS,
with traditional open approach.8-13 Gao YS, Zhang LZ, Huang JF, Shao K, Feng FY, Zhao L, Li J, Cheng
GY, Sun KL and He J)
Correspondence to: Dr. He Jie, Department of Thoracic Surgical
We started MIE in 2009.14 The aim of the present study was Oncology, Cancer Institute & Hospital, Chinese Academy of Medical
to compare the postoperative outcomes in patients with Sciences and Peking Union Medical College, Beijing 100021, China
esophageal squamous cell carcinoma undergoing MIE or (Email: prof. hejie@263. net)
748 Chin Med J 2014;127 (4)

rate, the rate of leak, pulmonary morbidity rate, mortality intercostal space, and this was used to pass a fan-shaped
rate, and hospital length of stay. retractor to retract the lung anteriorly and allow exposure
of the esophagus. A 5-mm port was placed just below the
Charlson score was carried out according to the definition subscapular tip to place the instruments for retraction and
of Charlson et al.15 Esophageal cancer staging was based counter traction. The inferior pulmonary ligament was
on the American Joint Committee on Cancer (AJCC) 2009 divided. The mediastinal pleura overlying the esophagus
cancer staging.16 was divided and opened to the level of the azygous vein to
expose the thoracic esophagus. The azygous vein was then
Surgical technique dissected and divided with an endoscopic vascular stapler.
MIE includes total MIE and hybrid MIE. 8 The former The thoracic esophagus, along with the periesophageal
consists of thoracoscopic esophagectomy, laparoscopic tissue and mediastinal lymph nodes, was circumferentially
gastric preparation, and gastroesophageal anastomosis, mobilized from the diaphragm to the level of about
while there is only thoracoscopic surgery in hybrid MIE. 2 cm above the carina. After full mobilization of the
In 2009, only hybrid MIE was used in our center. Since its thoracic esophagus, the esophagus was transected 5 cm
introduction in 2010, total MIE was in use. MIE includes above the upper margin of the tumor with an endoscopic
minimally invasive Ivor Lewis or minimally invasive linear stapler. The specimen was then removed. We then
McKeown approach. performed a stapled intrathoracic anastomosis. The first
step of the stapled anastomosis was the placement of a
Minimally invasive Ivor Lewis approach 28-mm EEA anvil in the proximal esophagus. The anvil
Laparoscopic phase was secured with a pursestring suture. We have found
The operation began with the laparoscopic exploration that it was difficult to place this first suture perfectly, as
in patients in whom an Ivor Lewis anastomosis is the anvil tended to move and migrate out of the open
planned. The patient was placed in a supine position. A esophagus. Therefore, we added a second pursestring
pneumoperitoneum (12–14 cmH2O) was established by suture to secure the anvil. Because the fundus of the
CO2 injection through an umbilical port. A total of five stomach is the most ischemic portion of the conduit, we
abdominal ports (three 5 mm and two 10–12 mm) were planned the anastomosis so as to discard the fundal tip.
used. After placement of the ports, the first step of the The tip of the fundus was then opened, and the EEA
laparoscopic phase was an exploration of the abdomen to stapler was advanced into the gastrostomy just created in
rule out advanced disease. The mobilization of the stomach the tip of the fundus. A stapled anastomosis between the
was started with the division of the greater curvature using gastric conduit and the esophagus, high above the azygos
a Harmonic scalpel (Ethicon Endo-Surgery, OH, USA). vein, was then performed. The redundant portion of the
The short gastric vessels were divided with ultrasonic fundus was excised with a reticulating endo-GIA stapler. A
coagulating shears. The gastrocolic omentum was then nasogastric tube was placed across the anastomosis, under
divided, with care taken to preserve the right gastroepiploic direct visualization, and secured. The anastomosis was
artery. The posterior attachments of the stomach were then checked for any leaks. The chest was inspected closely, and
divided after retraction of the stomach anteriorly. The left hemostasis was verified.
gastric vessel was divided at its origin from the celiac trunk
with an endoscopic gastrointestinal anastomosis (GIA) Minimally invasive McKeown approach
stapler. Lymphatic tissues around vessels were included in After laparoscopic phase and thoracoscopic phase, next, a
the resection. Subsequently, the right crus was visualized 4 to 6-cm horizontal neck incision was made. The cervical
and dissected, followed by dissection and defining of the esophagus was exposed. Careful dissection was performed
left crura of the diaphragm. The abdominal esophagus down until the thoracic dissection plane was encountered,
was dissected as far as possible toward the distal end. generally quite easily since the VATS dissection was
Pyloroplasty was not routinely performed. The abdomen is continued well into the thoracic inlet. The esophagogastric
inspected to make sure that hemostasis is adequate and the specimen was pulled out of the neck incision and the
incisions are closed. cervical esophagus divided high. The specimen was
removed from the field. An anastomosis was performed
Thoracoscopic phase between the cervical esophagus and gastric tube using
The patient’s posture was then changed to the left lateral standard techniques. The specimen was removed from the
decubitus position. The position of the double-lumen field.
tube was verified, and single-lung ventilation was used.
Four thoracoscopic ports were established. A 10-mm port OE includes open Ivor Lewis and McKeown approach,
was placed at the seventh intercostal space, just along which was selected according to the location of the tumor
the midaxillary line, for the camera. Another 4-cm port of esophagus.
was placed at the eighth intercostal space, posterior to
the posterior axillary line, for the dissection instrument Statistical analysis
(ultrasonic coagulating shears) and passage of the end- The SPSS software package 16.0 for Windows (SPSS
to-end circular stapler (EEA; Covidien). A 10-mm port Inc., IL ,USA) was used for statistical analysis. Data
was placed in the anterior axillary line, at the fourth were presented as median value (interquartile range) for
Chinese Medical Journal 2014;127 (4) 749

continuous variables and percentages for dichotomous MIE and OE groups via Ivor Lewis approach, which is
variables. Continuous variables were analyzed using t-test shown in Table 3. No significantly different differences
or nonparametric test, and categorical variables were were found between MIE and OE groups with respect to
analyzed using χ2-test. The significant level was set as a age, sex, Charlson scores, and tumor locations. The number
P-value less than 0.05. of harvested lymph nodes was not significantly different
between the two groups. Patients who underwent MIE
RESULTS had longer operation time than the OE group (420 vs. 270
minutes). With respect to postoperative parameters, overall
Demographics morbidity, pulmonary morbidity, and in-hospital death were
From January 2009 to August 2013, 176 MIEs were not significantly different between MIE and OE groups.
conducted and the number of MIE of each year was shown However, the rate of leak is higher in the MIE group than
in Figure 1. There was an increasing trend of MIE. the OE group (7.7% vs. 0%). Although no significant
difference was found, there was a trend that hospital LOS
In this cohort, the median age was 60 years in the MIE in the MIE group is shorter than the OE group (17 vs. 19
group, which is significantly higher than 59 years in the days, P=0.426).
OE group. No significant differences were found for the
ratio of sex, Charlson scores, and the location of tumor The short-term outcomes between MIE and OE groups via
between MIE group and OE group (Table 1). The number McKeown approach were also analyzed and the results are
of harvested lymph nodes was not significantly diffenent shown in Table 4. Patients in the MIE group had a median
between the two groups. However, patients who underwent age of 60 years, which was higher than the median age of
MIE had longer operation time than the OE group (375 56 years in the OE group. No significant differences were
vs. 300 minutes). There was lower ratio of AJCC stage II found between MIE and OE groups with respect to sex and
patients in the MIE group than in the OE group (38.1% vs. Charlson scores. More patients (59.6%) had upper third
60.6%) which may be attributed to selection bias. esophageal cancer in the OE group. Patients in the OE
group had more stage II diseases. Again, the difference of
Surgical outcomes the number of harvested lymph nodes was not significant
Overall morbidity, pulmonary morbidity, the rate of leak, between the two groups. Operation time in both groups was
in-hospital death, and hospital LOS were not significantly not significantly different with a median of 360 minutes in
different between MIE and OE groups as summarized in
Table 2. Table 2. Perioperative outcome
Minimally invasive
Clinical variables Open (n=142) P values
(n=176)
We further compared the short-term outcomes between Overall morbidity (n (%)) 28 (15.9) 22 (15.5) 0.919
Pulmonary morbidity (n (%)) 6 (3.4) 4 (2.8) 0.764
Leak (n (%)) 12 (6.8) 4 (2.8) 0.105
Mortality (n (%)) 1 (0.6) 1 (0.7) 0.879
Hospital LOS (days) 17 (14­–22) 20 (16–28) 0.195
Hospital expense (Yuan) 91 400 96 800 0.051
(82 900–106 000) (81 800–122 000)
LOS: length of stay.

Table 3. Comparison of short-term outcomes between minimally


invasive and open esophagectomy for esophageal cancer via Ivor
Lewis approach (n=142)
Minimally invasive Open
Figure 1. The number of minimally invasive esophagectomy Clinical variables
(n=52) (n=90)
P values
performed from 2009 to 2013 in our cancer center. Age (years) 59 (54–65) 59 (54–62) 0.296
Sex (male) 31 (59.6) 67 (74.4) 0.066
Table 1. Patients parameters Charlson scores 0 (0–0) 0 (0–0) 0.425
Minimally invasive Open Tumor location (n (%)) 0.215
Clinical variables P values
(n=176) (n=142) Upper 16 (30.8) 19 (21.1)
Age (years) 60 (55–66) 59 (54–62) 0.005 Middle 31 (59.6) 54 (60.0)
Sex (male, n (%)) 116 (65.9) 106 (74.6) 0.110 Lower 5 (9.6) 17 (18.9)
Charlson scores 0 (0–0) 0 (0–0) 0.775 Duration of surgery (min) 420 (300–480) 270 (210–300) <0.001
Tumor location (n (%)) 0.242 Number of harvested lymph nodes 13 (9–23) 16 (15–21) 0.082
Upper 47 (26.7) 50 (35.2) AJCC stage (n (%)) 0.019
Middle 98 (55.7) 72 (50.7) I 13 (25.0) 15 (16.7)
Lower 31 (17.6) 20 (14.1) II 21 (40.4) 58 (64.4)
Duration of surgery (min) 375 (300–450) 300 (240–330) <0.001 III 18 (34.6) 17 (18.9)
No. of harvested lymph nodes 20 (13–28) 16 (14–22) 0.740 Overall morbidity (n (%)) 11 (21.2) 8 (8.9) 0.045
AJCC stage (n (%)) <0.001 Pulmonary morbidity (n (%)) 1 (1.9) 0 (0) 0.366
I 53 (30.1) 23 (16.2) Leak (n (%)) 4 (7.7) 0 (0) 0.017
II 67 (38.1) 86 (60.6) Mortality (n (%)) 1 (1.9) 1 (1.1) 0.692
III 56 (31.8) 33 (23.2) Hospital LOS (days) 17 (15–19) 19 (16–21) 0.426
AJCC: American Joint Committee on Cancer. AJCC: American Joint Committee on Cancer; LOS, length of stay.
750 Chin Med J 2014;127 (4)

Table 4. Comparison of short-term outcomes between minimally The number of harvested lymph nodes in the MIE group is
invasive and open esophagectomy for esophageal cancer via 20, which is slightly higher than 16 in the OE group. Other
McKeown approach (n=176)
reports showed similar results. Berger et al17 found that
Minimally invasive
Clinical variables
(n=124)
Open (n=52) P values MIE had a significant increase in the number of harvested
Age (years) 60 (55–66) 56 (53–63) 0.027 lymph nodes of 20 than 9 in the OE group. They concluded
Sex (male) 85 (68.5) 39 (75.0) 0.392 that oncologic efficacy is not compromised and may be
Charlson score 0 (0–0) 0 (0–1) 0.606 improved with MIE. The reason lies in two aspects. First,
Tumor location (n (%)) <0.001
Upper 31 (25.0) 31 (59.6)
pathology departments appreciate the increased importance
Middle 67 (54.0) 18 (34.6) of nodal yields. Second, the surgical technique had evolved
Lower 26 (21.0) 3 (5.8) to include more complete clearance of celiac node basin.18
Duration of surgery (min) 360 (300–420) 322 (300–377) 0.012
No. of harvested lymph nodes 22 (15–29) 17 (13–29) 0.829 An Ivor Lewis esophagectomy is commonly employed by
AJCC stage (n (%)) 0.044
I 40 (32.3) 8 (15.4)
surgeons of Western countries, as it allows for improved
II 46 (37.1) 28 (53.8) visualization of mediastinal structures, a comprehensive
III 38 (30.6) 16 (30.8) thoracic lymph node harvest, and the creation of a tension-
Overall morbidity (n (%)) 17 (13.7) 14 (26.9) 0.036 free anastomosis between the remnant esophagus and
Pulmonary morbidity (n (%)) 4 (4.0) 4 (7.7) 0.315
the gastric conduit.10,18,19 Recently, Li et al20 reported the
Leak (n (%)) 8 (6.5) 4 (7.7) 0.766
Mortality (n (%)) 0 (0) 0 (0) 1.000
initial experience of using combined laparoscopic and
Hospital LOS (days) 17 (14–22) 21 (16–24) 0.090 thoracoscopic Ivor Lewis esophagectomy for esophageal
AJCC: American Joint Committee on Cancer; LOS: length of stay. cancer in China. In the present study, we did find that
patients in the MIE group tended to have a greater
the MIE group and 322 minutes in the OE group. Overall proportion of AJCC stage I tumors than the OE group,
morbidity in the MIE group is significantly lower than the which may reflect a selection bias in the MIE group in the
OE group. Major morbidities including anastomotic leak early period of MIE. A significant difference was noted
and pulmonary morbidity were not significantly different in terms of operative times, which may attribute to the
between these two groups. At last, mortality rate and hospital learning curve of MIE. As that is the first 51 MIE patients
LOS were not significantly different between MIE and OE in our medical center. And so is the fact that the leak rate in
groups. the MIE group is higher than in the OE group. Importantly,
there was no difference in the adequacy of oncological
Hospital expense resection with respect to lymph node retrieval and resection.
The median cost of the MIE group is 91 400 YUAN Lymph node resection is important for a complete resection
(RMB), which is lower than 96 800 YUAN in the OE and staging, which leads to an appropriate postoperative
group. treatment and improved long-term survival. Overall
mortality was not significantly different, which is similar to
DISCUSSION other reports.18,19

In this study, we found that early oncological outcomes are McKeown approach is an option of surgical treatment
comparable between MIE and OE groups in the treatment for cancer of the upper-middle thoracic esophagus.
of esophageal cancer. It is associated with high leak rate and high
pulmonary morbidity rate compared with Ivor Lewis
The feasibility of MIE has been well established in our esophagectomy.21,22 In our study, the leak rate is 7.7% via
center in a previous report, although the duration of surgery open McKeown approach, which is higher than zero in
is longer in the MIE group than the OE group.16 In this open Ivor Lewis approach , and pulmonary morbidity rate
study, patients who underwent MIE had a median of 375 is 7.7% via open McKeown approach, which is higher than
minutes, which is significantly longer than 300 minutes than zero in open Ivor Lewis approach. With the introduction
the OE group, which is attributed to the effect of learning of MIE, pulmonary morbidity is reduced significantly, as
curve. However, further analysis found that learning curve found in several recent reports.9,13,17 Berger et al17 reported
effect predominates in the early phase. As in this study, the that the rate of respiratory failure is 7.7% in the MIE group,
duration of surgery is significantly longer in the MIE group which is significantly lower than 21% in the OE group.
than the OE group in patients who underwent minimally Nafteux et al found that the rate of pulmonary infection
invasive or open Ivor Lewis approach, which is mainly is 35.6% in the OE group, which is significantly higher
conducted in our early practice. In 2010, total MIE was than 18.5% in the MIE group.9 Recently, Biere et al13
introduced in our center. The duration of surgery of the also reported a similar result in a multicenter-randomized
MIE group is shortened and is comparable to that of the trial. However, the leakage rate after MIE or OE via
OE group which is reflected in patients who underwent McKeown approach was not significantly different between
minimally invasive or open McKeown approach in Table 4. MIE and OE groups in most medical centers;9,13,17,23 our
Median operation time was 360 minutes in the MIE group study also demonstrated the similar result. Recently,
and 327 minutes in the OE group. The result is comparable Price et al24 reported results of comparisons of four most
to that of other medical centers.10-13 common esophagogastric anastomotic techniques: circular
Chinese Medical Journal 2014;127 (4) 751

stapled, hand sewn, linear stapled (longitudinally stapled Edinb 1992; 37: 7-11.
anastomosis), and modified Collard (combined linear and 8. Luketich JD, Alvelo-Rivera M, Buenaventura PO, Christie
transverse stapled anastomosis). They found that hand sewn NA, McCaughan JS, Litle VR,  et al. Minimally invasive
anastomosis had the highest odds of leakage (P=0.01). The esophagectomy: outcomes in 222 patients. Ann Surg 2003; 238:
result of this study needs further investigation in the future. 486-495.
9. Nafteux P, Moons J, Coosemans W, Decaluwé H, Decker G, De
Several meta-analyses demonstrated the similar result that Leyn P, et al. Minimally invasive oesophagectomy: a valuable
MIE is equivalent to OE in achieving similar oncological alternative to open oesophagectomy for the treatment of early
outcomes, perioperative results, and prognosis.25-27 Recently, oesophageal and gastro-oesophageal junction carcinoma. Eur J
a multicenter-randomized trial showed that MIE provides Cardiothorac Surg 2011; 40: 1455-1463.
short-term benefits over OE for patients with resectable 10. Sihag S, Wright CD, Wain JC, Gaissert HA, Lanuti M, Allan
esophageal cancer. Combining literatures and our results, JS, et al. Comparison of perioperative outcomes following open
we agree with the opinion of Pennathur et al28 that MIE versus minimally invasive Ivor Lewis oesophagectomy at a
may be the best operation for resectable esophageal cancer. single, high-volume centre. Eur J Cardiothorac Surg 2012; 42:
Few studies assessed the cost-effectiveness of MIE versus 430-437.
OE for esophageal cancer. Lee et al estimated the expected 11. Chen BF, Zhu CC, Wang CG, Ma DH, Lin J, Zhang B,
costs and outcomes after MIE and OE from a health- et al. Clinical comparative study of minimally invasive
care system using a decision-analysis model and found esophagectomy versus open esophagectomy for esophageal
that MIE is cost-effective compared with OE in patients carcinoma (in Chinese). Chin J Surg 2010; 48: 1206-1209.
with resectable esophageal cancer.29 In our study, hospital 12. Tsujimoto H, Takahata R, Nomura S, Yaguchi Y, Kumano I,
expense in the MIE group was lower than in the OE group. Matsumoto Y, et al. Video-assisted thoracoscopic surgery for
However, the sample of this study is relatively small and esophageal cancer attenuates postoperative systemic responses
further study is needed to draw a concluding view of cost- and pulmonary complications. Surgery 2012; 151: 667-673.
effectiveness of MIE versus OE for esophageal cancer. The 13. Biere SS, van Berge Henegouwen MI, Maas KW, Bonavina
limitation of this study mainly comes from the retrospective L, Rosman C, Garcia JR, et al. Minimally invasive versus
nature, which carries a risk of some selection bias. open oesophagectomy for patients with oesophageal cancer:
Randomized or multicenter trials are needed in the future to a multicentre, open-label, randomised controlled trial. Lancet
overcome the shortcomings of this study. 2012; 379: 1887-1892.
14. Mu JW, Chen GY, Sun KL,Wang DW, Zhang BH, Li N, et al.
In conclusion, MIE and OE appear equivalent with Application of video-assisted thoracic surgery in the standard
regard to early oncological outcomes in the treatment of operation for thoracic tumors. Cancer Biol Med 2013; 10: 28-35.
esophageal cancer. 15. Charlson ME, Pompei P, Ales KL, MacKenzie CR. A new
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