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Long-term survival outcomes of laparoscopyassisted gastrectomy with D2 lymph node dissection for gastric cancer at 103 Military Hospital

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Although laparoscopy-assisted gastrectomy for gastric cancer has been applied in the world since 1991, it was not until 2007 that this technique was used widely at large medical centers in Vietnam. However, there have been no studies to evaluate the long-term survival of method so far. Subjects and methods: To study 165 gastric cancer patients undergoing laparoscopy-assisted gastrectomy with D2 lymph node dissection at 103 Military Hospital from April 2009 to August 2013. Surgical procedures according to instructions of Ministry of Health. Lymph node dissection and postoperative stage according to 3rd JGCA were diagnosed. Patients were followed at least 5 years after surgery, intra-and-postoperative complications, recurrence and metastases were recorded and managed.

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LONG-TERM SURVIVAL OUTCOMES OF LAPAROSCOPY-

ASSISTED GASTRECTOMY WITH D2 LYMPH NODE

DISSECTION FOR GASTRIC CANCER AT 103 MILITARY HOSPITAL

Ho Chi Thanh 1 ; Hoang Manh An 1 ; Dang Viet Dung 1 ; Nguyen Van Xuyen 1

Nguyen Trong Hoe 1 ; Le Thanh Son 1 ; Phan Hung Phuc 2 ; Nguyen Van Tiep 1

SUMMARY

Background: Although laparoscopy-assisted gastrectomy for gastric cancer has been applied

in the world since 1991, it was not until 2007 that this technique was used widely at large

medical centers in Vietnam However, there have been no studies to evaluate the long-term

survival of method so far Subjects and methods: To study 165 gastric cancer patients

undergoing laparoscopy-assisted gastrectomy with D2 lymph node dissection at 103 Military

Hospital from April 2009 to August 2013 Surgical procedures according to instructions of

Ministry of Health Lymph node dissection and postoperative stage according to 3 rd JGCA were

diagnosed Patients were followed at least 5 years after surgery, intra-and-postoperative

complications, recurrence and metastases were recorded and managed Analysis and

processing of data were performed by using SPSS software version 15.0 Results: Mean

operative time was 205.7 ± 51.8 minutes, mean number of lymph nodes dissection per one

patient was 21.5 ± 6.09 The incident in surgery was 1.81%, complications after surgery was

4.2%, postoperative mortality rate was 0.6%, cancer recurrence and metastasis was 44.8%

Survival outcomes of postoperative five-year follow-up were 50.3%; with 93.3% in the stage Ia,

89.7% in the stage Ib; 61.7% in the stage IIa; 70.0% in the stage IIb; 25% in the stage IIIa; 7.7% in the stage IIIb and 0% in the stage IIIc Conclusions: Our study found that the long-term

outcome of laparoscopy-assisted gastrectomy with D2 lymph node dissection for gastric cancer

was promising and acceptable Survival outcomes after surgery depends on the stage and

lymph node metastasis status

* Keywords: Gastric cancer; Laparoscopy-assisted gastrectomy; D2 lymph node dissection;

Long-term survival outcomes

INTRODUCTION

Gastric cancer is the most malignant

disease in gastrointestinal cancer,

according to Global Cancer Statistics

in 2018, with mortality rate of 8.2%, which

comes the second, just after lung cancer, common in both men and women [1]

Radical gastrectomy with lymphadenectomy

is the most effective treatment, increasing the survival rate

1 103 Military Hospital

2 Vietnam Military Medical University

Corresponding author: Ho Chi Thanh (hochithanh103@gmail.com)

Date received: 20/11/2018

Date accepted: 14/01/2019

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Laparoscopic gastrectomy for early gastric

cancer was first performed by Kitano in

1991, so far many surgeons in the world

have done this technique For advanced

gastric cancer, gastrectomy with D2 lymph

node dissection is considered standard

surgery, however, with laparoscopy assisted,

surgeons suspect the radicalization of the

method [2, 3] In Vietnam,

laparoscopy-assisted gastrectomy (LAG) with D2

lymph node dissection for gastric cancer

has been performed in big hospitals, but

short follow-up time and there have been

no studies of evaluating the long-term

survival outcome Therefore, we studied

this study: To evaluate long-term survival

outcome of LAG with D2 lymph node

dissection for gastric cancer

SUBJECTS AND METHODS

1 Research subjects

165 patients were diagnosed with gastric

adenocarcinoma, who was LAG with D2

lymphadenectomy from April 2009 to

October 2013, at Abdominal Surgery

Department, 103 Military Hospital

- The procedure of LAG was uniform

under the treatment guidelines of Ministry

of Health issued in 2013 for laparoscopic

gastrectomy with D2 lymphadenectomy [4]

- The patients were the first people to

undergo laparoscopic gastrectomy, afterwards,

they conversed to open surgery

2 Methods

- Descriptive study, tracking down

uncontrolled

- Patient was followed up after surgery with 3rd JGCA, follow-up time at least

60 months All cases of recurrence, metastases and causes of death were recorded and confirmed [5]

* Handling of the resected specimen and description of histological findings:

- The specimens are opened along the greater curvature, cleaned, fixed and examination of macroscopic type, location, size, invasion of tumor Measurement

of tumor size along the margin of mucosal lesion, and the length of the proximal and distal resection margins were measured

- After dissection of lymph nodes from the specimen, station to number according

to 3rd JGCA, examples of macroscopic type, number of lymph nodes, and fixed

in 15 - 20% formalin solution, sent to histopathology department

- The results of postoperation stage according to 3rd JGCA [5]

* Statistical analysis:

- Data were processed by the Kaplan-Meier method using SPSS software, version 15.0

RESULTS

1 Characteristics of patients

- Mean age: 56.1 ± 11.38 (range,

26 - 81 years)

- Male: 113 patients (68.5%); female:

52 patients (31.5%)

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2 Pathological characteristics

Table 2:

Tumor location

Macroscopic type

T stage

Histological type

Poorly

differentiated

Lymph node stage

TNM stage

3 Surgical outcomes

Mean operative time: 205.7 ± 51.8 mins

Average lymph node dissection:

21.5 ± 6.09

Table 3:

Type of gastrectomy

Complications

Mortality (because of

* Recurrence and metastasis (n = 74; 44.8%):

Peritoneum: 50 patients (30.3%); liver:

7 patients (4.2 %); hepatic lymph node:

6 patients (3.6%); colon: 3 patients (1.8%);

lung: 2 patients (1.2%); brain: 1 patient

(0.6%); rectum: 1 patient (0.6%); troiser:

2 patients (1.2%); ovary: 1 patient (0.6%); spine: 1 patient (0.6%)

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Table 4: Results of follow-up survival

Figure 1: Follow-up overall survival

Overall 5-year survival rate was 50.3%

Figure 2: Follow-up overall survival of sex

Overall 5-year survival rates of male

and female were 54.9% and 50.0%, test

Log Rank χ2 =0.389, p = 0.533

Figure 3: Follow-up overall survival

of macroscopy

Overall 5-year survival rates of polypoid, ulcerated, infiltrative ulcerated and infiltrative were 68.8%, 74.7%, 25.4% and 28.6%, test Log Rank χ2 =49.220, p = 0.000

Figure 4: Follow up overall survival

of T stage

Overall 5-year survival rates of T1, T2, T3 and T4a were 90.5%, 70.1%, 33.3% and 7.1%, test Log Rank; χ2 =56.538, p = 0.000

Figure 5: Overall survival rates of lymph

node stage

Overall 5-year survival rates of pN0, pN1, pN2 and pN3 were 86.4%, 72.4%, 38.9%

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and 4.9%, test Log Rank χ2 = 148.978,

p = 0.000

Figure 6: Overall survival rates of TNM stage

Overall 5-year survival rates of Ia, Ib, IIa,

IIb, IIIa, IIIb and IIIc were 93.3%, 89.7%,

61.53%, 70.0%, 25.0%, 7.7% and 0.00%,

test Log Rank χ2

=148.978, p = 0.000

Figure 7: Overall survival rates of

histological

Overall 5-year survival rates of papillary,

tubular, mucinous, signet-ring cell and poorly

differentiated carcinoma were 87.5%, 63.2%,

53.8%, 47.1% and 38.9%, test Log Rank

χ2 =28.073, p = 0.000

Figure 8: Overall survival rates of

type gastrectomy

Overall 5-year survival rates of distal, subtotal, total and proximal gastrectomy were 54.3%, 36.4%, 44.4% and 80%, test Log Rank χ2 = 5.152, p = 0.161

DISCUSSION

1 Patients’ characteristics

The mean age was 56.1 ± 11.38 years, males occupied 68.5% and females

accounted for 31.5% (table 1) These results

were consistent with domestic and foreign studies, according to Global Cancer Statistics report in 2018, rates were 2-fold higher in men than in women [1, 6, 7]

Tumor location with lower third was 86.7%, middle third was 9.09% and upper

third was 4.24% (table 2) Pathological

classifications were the most of ulcerated carcinomas (47.9%) and infiltrative ulcerated carcinomas were 38.2%, polypoid tumors was 9.7% and diffuse infiltrative carcinoma was 4.24% Depth of tumor invasion with T1, T2, T3 and T4a were 12.7%; 40.6%,

with the characteristics of gastric cancer

in domestic studies: mostly in the lower third, macroscopic type was usually ulcerated and was advanced stages, surgery and prognosis was poor Park et al: T2, T3 and T4 were 25.7%; 58.7% and 15.6%; tumor location with upper, middle and lower third were 16.1%; 11.3% and 69.0%, respectively [6] Kim et al reported: tumor location with upper, middle and lower third were 5.8%; 23.8% and 70.0%; T1a, T1b, T2, T3 and T4 were 47.1%; 30.4%; 10.4%, 6.6% and 4.4%, respectively [7] Histological characteristics: Papillary, tubular, mucinous adenocarcinomas were

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14.5%; 23.0% and 7.87% Signet-ring cell

and poorly differentiated adenocarcinoma

were 10.3% and 43.6% One case of

squamous cell carcinoma was 0.6%

According to Kitano et al, tubular,

signet-ring cell adenocarcinoma and others were

78.7%, 19.7% and 2.4%, respectively [2]

Kim et al reported, signet-ring cell was 7.8%

and poorly differentiated adenocarcinoma

was 33.9% [7]

Characteristics of lympho node

metastasis: pN0, pN1, pN2 and pN3

were 35.7%, 17.6%, 21.8% and 24.8%

Park et al [6]: pN0, pN1, pN2, pN3 were

44.0%, 16.5%, 13.5% and 25.7% Fang

et al: pN0 was 43.7%, pN1 was 24.1%,

pN2 was 19.5% and pN3 was 12.6% [8]

Pathological stages according to 3rd

JGCA: Ia and Ib were 9.09% and 23.6%;

IIa and IIb were 21.8% and 12.1%; IIIa,

IIIb and IIIc were 16.9%, 15.8% and 6.67%

(table 2) This result was also consistent

with our domestic research, the early

gastric cancer was diagnosed in Vietnam

is much lower than that in Japan and

Korea Kitano et al showed that the rate of

stage disease for Ia, Ib and II were

93.7%, 5.8% and 0.5%, respectively [2]

Kim et al indicated the rate of stage I, II

and III were 82.2%, 11.7% and 5.0% [7]

Huscher C et al, the rate of stage Ia was

20.7%; Ib was 20.7%; II was 13.8%, IIIa

was 17.2%; IIIb was 10.4% and IV was

17.2% [3]

2 Operative results

Mean operative time was 205.7 ± 51.8

minutes, average number of dessected

lymph nodes was 21.5 (table 3), which could

be acceptable compared with open surgery and other authors’ findings [2] The operative time in Huscher et al’s study was 196 ±

21 minutes, mean number of lymph nodes dissected was 30.0, which were 322.9 ± 116.6 minutes and 28.5 lymh nodes in Park et al’s stduy; 214.0 ± 52.6 minutes and 34.7 lymph nodes in Kim et al’s;

337 minutes and 32 lymph nodes in Fang

et al’s; 240 ± 58.2 minutes and 35 lymph nodes in Honda et al’s [3, 6, 7, 8, 9] There were 5 laparoscopy-assisted proximal gastrectomy (LAPG), 140 laparoscopy-assisted distal gastrectomy (LADG),

11 laparoscopy-assisted subtotal gastrectomy (LASG) and 9 laparoscopy-assisted total gastrectomy (LATG) This result was consistent with Kitano et al’s: LADG was 91.5%, LAPG was 4.2% and LATG was 4.3% [2], Kim et al reported LADG was 90.5%, LAPG was 0.3% and LATG was 9.2% [7]

The incidence in surgery was 5 cases (3.03%), of which two patients suffered from bleeding by injury splenic artery during dissected 11p, to clip splenic artery

to stop bleeding were not performed splenectomy There was one case of spleen injury This patient had to do laparoscopic spelenectomy Two cases of injured transverse colon, we had to make colostomy Kitano et al, complications of intraoperative was 1.7% in LADG group, 7.4% in LAPG group and 1.8% LATG group [2]

Postoperative complications: 8 cases (4.8%), in which there were two cases with duodenal stump leak (1.2%), resurgery

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to drainage duodenum, after that the patient

was rather well and discharged from hospital

There was one patient with anastomotic

leak on 5th postoperative day (0.6%), who

was performed subtotal gastrectomy with

anemia anastomosis This patient had to

undergo reoperation for total gastrectomy

and was connected jejunum to oesophagus

As a result, the patient recovered a little

and discharged from hospital In the case

of patient undergoing subtotal gastrectomy

with lymphadenectomy and resection all

of short gastric vessels, total gastrectomy

should be performed and jejunum has to

be connected to the oesophagus so that

it is better nourished Residual abscess

was found in two cases on 4th and 5th

post-operative day (1.2%), treated

conservatively, drained fluid under

ultrasound, patients were stable and

discharged after 5 days Incision infection

was observed in one case (0.6%), the

patients were taken care and closed

second incision and patient was fine and

discharged Compared to open surgery

and other authors’s findings, our postoperative

complications were acceptable Kitano et

al reported complication was 14.8% [2]

In Huscher’s study, this rate was 23.3%,

including acute pancreatitis, pleural effusion,

bleeding and wound infection and

conservative treatment, without reoperation

[3] Kim et al conducted a study on

753 patients of LG, rate of complication

was 10.2%, including six cases of duodenal

stump leakage, anastomotic leak were 3

cases, bleeding was encountered in one

case and residual abscess was in one

case [7]

Respiratory failure and death after surgery: 1 case (0.6%) The patient was

74 years old, stage IIIb, pyloric stenosis, respiratory failure on day 6th after surgery Kim et al reported mortality after surgery was 0.1%; in Huscher et al’s study, there was one case of mortality after surgery due to respiratory failure (3.3%) [3, 7]

* Recurrence and metastasis:

Recurrence and metastasis after gastrectomy for gastric caner were common causes of mortality and decreasing survival In table 4, recurrence and metastasis occurred in 74 patients (44.8%),

in which recurrent peritoneal was the highest rate of 30.3%, metastatic liver was 4.2%, liver metastatic lymph node to obstruction of the bide duct were 6 cases (3.36%), metastatic colon: 3 cases (1.8%), lung metastasis: 2 cases (1.2%), metastatic troiser: 2 cases (1.2%), metastatic brain: one case, metastatic Krukenber: one case, metastatic rectum: one case and metastatic spine: one case Of the 74 recurrences, there were 5 cases of reoperation,

71 case were dead and 3 cases were alive with 2 cases of metastatic liver and one case of metastatic colon There were

no port-site and no incision metastases were observed Park et al: recurrence was 50.7% in the open surgery group and 29.4% in the laparoscopic group, there was no differences between two groups

In the recurrence group, metastatic peritonea was the highest (18.7%), metastatic an intra-abdominal organ was 17.3% and metastases liver was 16.0% [6] Honda

et al, 5 years after surgery found that peritoneal metastases was 0.76% and

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metastases liver was 0.87% [9] Chen

et al, the mean follow-up was 39.7 months

and found that 40 patients developed

tumor recurrence, in which peritoneal

recurrence was the highest (45.0%),

27.5% of distant recurrence, 17.5% of

lymphatic recurrence and 10.0% of

locoregional recurrence [10]

4 Follow-up survival results

Follow-up survival of after cancer

surgery was very interesting, in table 5

and figure 1, the shortest was 60 months,

the longest was 111 months, the average

survival rate were 53.9 ± 31.3 months

5 cases were lost to follow-up assessment,

giving a follow-up rate of 96.96% The

5-year overall survival and disease-free

survival was 80 cases (50.3%) and 77 cases

(48.4%) Death was found in 77 cases

(46.7%) and 71 cases of death (43.0%)

was due to recurrence and metastasis,

6 cases of death due to other causes

These results were consistent with

Huscher et al’s study, followed up with 30

patients of LG, an average survival were

52.2 ± 26.5 months, a survival rate of

58.9% for 5 years, recurrence rates were

37.9% and all died from recurrent disease

[3] Kim et al, the average follow-up time

were 56.2 months, after 5 years’ surgery,

overall survival rate was 97.1% and

disease-free survival rate was 96.3%,

the recurrence rate was 3.3% [7]

Analysis of factors related to

post-operation, we used Log Rank test In figure

2, 5-year survival rate in male was 54.9%

and 50.0% in female, but the Log Rank

χ2

= 0.389, p = 0.533, so the gender was

not related to overall survival after surgery

Follow-up survival of the macroscopic tip at figure 3, we found that the 5 year overall survival of mass was 68.8% and that of ulcerative was 74.7%, higher than the infiltrative ulcerative and diffused infiltrative was 25.4% and 28.6%, significantly different with the Log Rank test χ2 = 49.22 and p = 0.000 The relative between invasive stages and survival after surgery, figure 4 shows that 5-year survival rate of invasive stage T1, T2, T3 and T4a was 90.5%, 70.1%; 33.3% and 7.1%, significant difference with the Log Rank test χ2 = 56.538 and p = 0.000 Fang et al, 5 year overall survival of LADG group was 59%, Chen et al, the 5-years overall survival in T1, T2, T3 and T4a was 92.1%, 84.6%, 65.9%, and 40.7%, respectively [8, 10]

Follow-up survival of the lymph node stages at figure 5 The 5-year survival rate of the cases with non-lympho node metastasis (pN0) was 86.4%; the pN1 was 72.4%, the pN2 was 38.9% and pN3 was 4.9%, significant difference with Log Rank test χ2 = 148.978 and p = 0.000 In figure 6, the 5-year overall survival rate of stage Ia, Ib, IIa, IIb, IIIa, IIIb and IIIc was 93.3%; 89.7%, 61.53%, 70.0%, 25%, 7.7% and 0%, significantly different, with test Log Rank χ2 = 56.538 and p = 0.000 Our results were consistent with Kim et al’s: 5 year overall survival of stage I, II and III was 99.5%, 89.5% and 76.1% [7]

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Kitano et al reported the 5-year

disease-free survival rate was 99.8% for stage Ia,

98.7% for stage Ib and 85.7% for stage II

[2] Park et al reported in LG group, 5-year

overall survival rate of stage I, II and III

was 87.5%, 77.3% and 34.8% [6] Honda

studied LG for gastric cancer of stage I,

the 5-year overall survival rate was 97.1%

[9] Chen et al, according to tumor stage,

5-year overall survival was 93.1% for

stage I, 67.6% for stage II and 41.5% for

stage III [10]

Follow-up survival of histopathology at

figure 7, the 5-year overall survival of

papillary, tubular, mucinous, signet-ring cell

and poorly differentiated adenocarcinoma

was 87.5%, 63.2%, 53.8%, 47.1% and 38.9%,

respectively One patient with squamous

cell carcinoma died after 11 months,

significant difference with test Log Rank

χ2 = 28.073 and p = 0.000 According

to Japanese authors, the intestinal type

has a better prognosis; diffused type,

adenosquamous and squamous cell

carcinoma have less prognosis than other

cells, the survival rate of 5 years is less

than 10% [5]

In figure 8, the 5-year survival rate of

distant gastrectomy group was 54.3%, the

rate of proximal gastrectomy was 80.0%,

the rate of total and subtotal group was

44.4% and 36.4% The difference was

not significant with Log Rank χ2 = 5.152

and p = 0.161 Although there was no

difference, with total and subtotal gastrectomy,

their tumor were not detected early, size

of tumor were big, wide invasion so surgery

and postoperative prognosis will be not good

CONCLUSIONS

The study on 165 patients with gastric cancer were LAG with D2 lymph nodes dissection, we found that it was technically feasible, safe and a good long-term outcome The median survival was 53.9 ± 31.3 months, the 5-year overall survival was 50.3% The survival time was dependent on TNM stage, T-stage, lymph node metastatis stage, type of macroscopic and histological type with p < 0.01 Survival time was not dependent on gender and type of gastrectomy with

p > 0.05 However, the limitation of the study was small and compared with open surgery, therefore, we really need a large-scale multicenter randomized trial to confirm the oncological safety and feasibility

of LAG for patients with advanced gastric cancer

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1 Bray F, Ferlay J et al Global Cancer

Statistics 2018: Globocan estimates of incidence and mortality worldwide for 36 cancers in 185 countries CA Cancer J Clin

2018, pp.1-31

2 Kitano S, Shiraishi N, Uyama I et al A

multicenter study on oncologic outcome of laparoscopic gastrectomy for early cancer in Japan Annals of Surgery 2007, 245 (1), pp.68-72

3 Huscher C, Mingoli A, Sgarzini G et al

Laparoscopic versus open subtotal gastrectomy for distal gastric cancer, five-year results of a randomized prospective trial Annals of Surgery 2005, 241 (2), pp.232-237

4 Ministry of Health Laparoscopic distant

gastrectomy with D2 lymphadenectomy for

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gastric cancer List of guiding medical

examination and treatment procedures

specialized in oncology, promulgated together

with Decision No 3338/QĐ-BYT 2013, September,

9, pp.273-276

5 Japanese Gastric Cancer Association

Japanese classification of gastric carcinoma:

3rd English edition Gastric Cancer 2011, 14,

pp.101-112

6 Park J.H, Jeong S.H, Lee Y.J et al

Comparison of long-term oncologic outcomes

of laparoscopic gastrectomy and open

gastrectomy for advanced gastric cancer:

A retrospective cohort study Korean Journal

of Clinical Oncology 2018, 12, pp.21-29

7 Kim K.H, Kim M.C, Jung G.J et al

Long-term outcomes And Feasibility with

laparoscopy-assisted gastrectomy for gastric cancer J Gastric Cancer 2012, 12 (1), pp.18-25

8 Fang C, Hua J, Li J et al Comparison of

laparoscopy-assisted gastrectomy and open gastrectomy with D2 lymphadenectomy for advanced gastric cancer American Journal of Surgery

2014, 208, pp.391-396

9 Honda M, Hiki N, Kinoshita T et al

Long-term outcomes of laparoscopic versus open surgery for clinical stage I gastric cancer: The LOC-1 Study Annals of Surgery

2016, 264 (2), pp.214-222

10 Chen K, Mou Y.P et al Short-term

surgical and long-term survival outcomes after laparoscopic distal gastrectomy with D2

Gastroenterology 2014, 14 (41), pp.1-7

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