J Minim Invasive Surg 2017; 20(3): 101-107  https://doi.org/10.7602/jmis.2017.20.3.101
Comparison Surgical Outcomes between Laparoscopic and Conventional Distal Gastrectomy for Early Gastric Cancer in Obese Patients
Young Sun Choi, Dong Jin Kim, Han Mo Yoo, Kyo Young Song, and Cho Hyun Park
Department of Surgery, College of Medicine, The Catholic University of Korea, Seoul, Korea
Correspondence to: Han Mo Yoo Department of Surgery, Daejeon St. Mary’s Hospital, College of Medicine, The Catholic University of Korea, 64, Daeheung-ro, Jung-gu, Daejeon 34943, Korea Tel: +82-42-220-9520 Fax: +82-2-6442-4975 E-mail: kalpolipse@catholic.ac.kr
Received: June 27, 2017; Revised: August 5, 2017; Accepted: August 8, 2017; Published online: September 15, 2017.
© Journal of Minimally Invasive Surgery. All rights reserved.

cc This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.
Abstract

Purpose:

In this study, we explored the safety of laparoscopic gastrectomy in obese gastric cancer patients compared with conventional open gastrectomy based on early surgical outcomes.

Methods:

A total of 462 patients who underwent curative gastrectomy for early gastric adenocarcinoma from January 2000 to December 2014 were enrolled. Two obesity cohorts were defined according to a body mass index (BMI) of ≥25 kg/m2 versus ≥30 kg/m2. Those cohorts were further divided into the laparoscopic distal gastrectomy (LDG) and open distal gastrectomy (ODG) groups, and clinicopathologic characteristics were compared with early surgical results.

Results:

There were no significant differences in clinicopathologic characteristics between the LDG and ODG groups in the BMI ≥25 or BMI ≥30 cohorts. For the overall complication rate, fewer complications were observed in the LDG than ODG group in both cohorts. Among the overall complications, significant differences were observed in the minor complication rates (Clavien-Dindo I or II), but no significant difference was observed in the rate of Clavien-Dindo III or higher complications. For risk factor analysis of postoperative complications, open distal gastrectomy, age >60 years, and BMI ≥30 were independent risk factors for postoperative morbidity among all obese patients.

Conclusion:

LDG may be a better procedure to improve surgical outcomes in patients with obesity undergoing surgery for early gastric cancer in terms of less excessive blood loss, shorter operation time, and lower complication rates.

Keywords: Stomach neoplasm, Laparoscopy, Complication, Obesity
INTRODUCTION

Obesity is rapidly increasing on a global scale and is defined as excess fat accumulation, which can lead to health problems. The criteria for obesity is a body mass index (BMI) ≥30 kg/m2 in Western countries and ≥25 kg/m2 in Asian countries.1 Globally, 39% and 13% of adults aged ≥18 years were overweight and obese, respectively, in 2014. According to the Korea National Health and Nutrition Examination Survey, the obesity rate in south Korea is increasing, from 25.8% in 1998 to 32.8% in 2012.2 As obesity in the population increases, the proportion of obese patients with gastric cancer is also increasing.

Generally, gastric cancer surgeries in obese patients are technically demanding, showing limited oncologic safety. Large amounts of intra-abdominal fat can obscure vascular structures and normal surgical planes during surgery. Preoperative BMI is a risk factor for postoperative complications.3 Moreover, complete lymph node dissection is challenging during surgery in obese patients. These issues are equally challenging during laparoscopic surgery. In the past, laparoscopic surgery was not attempted in obese patients due to the above-mentioned problems. However, technical advancements have overcome these limitations. At this time, laparoscopic gastrectomy has advantages over open gastrectomy regarding postoperative outcomes and quality of life.4-6 In the recently published KLASS-01 trial morbidity and mortality report, laparoscopic gastrectomy showed advantages in terms of estimated blood loss, length of hospital stay, and overall complication rate, especially for wound complication.7 However, laparoscopic gastrectomy requires a longer operation time than that of open gastrectomy. Recently, the discrepancy in operation time has decreased due to technical improvements.8 However, the advantages of laparoscopic gastrectomy in obese patients remain controversial. In this study, we explored the safety of laparoscopic gastrectomy in terms of early surgical outcomes in obese gastric cancer patients.

MATERIALS AND METHODS

From January 2000 to December 2014, 4,272 patients with gastric adenocarcinoma underwent gastrectomy at the Department of Surgery, Seoul, St. Mary’s Hospital. Eligible criteria were curative resection, distal gastrectomy, pathologically confirmed early gastric cancer, and range of lymph node dissection D1+ or greater. Patients who underwent palliative or non-curative resection or combined resection were excluded. The data were collected retrospectively from a prospectively collected database. Obesity and morbid obesity were defined as BMI ≥25 and BMI ≥30, respectively, according to Asian-Pacific guidelines. Among the 4,274 patients, two cohorts were defined: patients with BMI ≥25 and those with BMI ≥30. A total of 462 patients were included in the former cohort and 41 patients in the latter cohort. Those cohorts were further divided into the laparoscopic distal gastrectomy (LDG) and open distal gastrectomy (ODG) groups. Clinicopathologic characteristics and surgical results included the range of lymph node dissection, early surgical results including postoperative complications, and length of hospital stay. Comparisons of continuous variables were performed using Student’s t-test and categorical variables were assessed using Pearson’s χ2 test or a linear-by-linear association χ2 test. Postoperative complications were graded based on the Clavien-Dindo classification.9 In addition, univariate and multivariate analyses were performed to identify risk factors for the development of postoperative complications. This study followed the 7th UICC TNM staging system (according to the American Joint Committee on Cancer [AJCC] 7th edition).10

RESULTS

Clinicopathological characteristics

In the BMI ≥25 cohort, no significant differences in patient characteristics including age, sex, ECOG, number of comorbidities, social history, or previous operation history were observed between the LDG and ODG groups. Tumor location, degree of differentiation, and N stage also showed no significant differences between the two groups. In the BMI ≥30 cohort, similar results were observed between the two groups (excluding mean tumor size). Tumor size in the LDG group was 2.6±1.5 cm, which was smaller than that (3.9±2.4 cm) in the ODG group (Table 1).

Clinicopathologic characteristics of the patients

VariablesBMI ≥25 (kg/m2) (n=426)BMI ≥30 (kg/m2) (n=41)


LDG (%) (n=260)ODG (%) (n=166)p valueLDG (%) (n=24)ODG (%) (n=17)p value
Age (year)58.9±11.2*59.8±9.9*0.42257.8±10.1*61.2±9.9*0.299
Sex0.6621.000
 Male182 (70.0)120 (72.3)16 (66.7)11 (64.7)
 Female78 (30.0)46 (27.7)8 (33.3)6 (35.3)
BMI (kg/m2)27.3±2.2*27.3±1.9*0.91832.7±2.6*31.5±1.6*0.093
ECOG PS0.7360.115
 0184 (70.8)120 (72.3)19 (79.2)9 (52.9)
 168 (26.2)39 (23.5)5 (20.8)7 (41.2)
 27 (2.7)7 (4.2)0 (0)1 (5.9)
 31 (0.4)0 (0)0 (0)0 (0)
Number of comorbidities0.4700.780
 0107 (41.2)64 (38.6)10 (41.7)4 (23.5)
 1111 (42.7)76 (45.8)10 (41.7)9 (52.9)
 230 (11.5)14 (8.4)1 (4.2)1 (5.9)
 ≥312 (4.6)12 (7.2)3 (12.5)3 (17.6)
Smoking history0.7130.233
 Non-smoker150 (57.7)94 (56.6)13 (54.2)8 (47.1)
 Ex-smoker60 (23.1)35 (21.1)6 (25.0)8 (47.1)
 Current smoker50 (19.2)37 (22.3)5 (20.8)1 (5.9)
Alcohol history0.5450.176
 Non-drinker145 (55.8)91 (54.8)13 (54.2)7 (41.2)
 Social drinker92 (35.4)55 (33.1)8 (33.3)10 (58.8)
 Heavy drinker23 (8.8)20 (12.0)3 (12.5)0 (0)
Previous abdominal operation history0.8030.499
 Absent210 (80.8)132 (79.5)15 (62.5)13 (76.5)
 Present50 (19.2)34 (20.5)9 (37.5)4 (23.5)
Tumor location0.1160.285
 Upper5 (2.0)6 (3.6)0 (0)2 (11.8)
 Middle30 (11.5)29 (17.5)3 (12.5)2 (11.8)
 Lower225 (86.5)131 (78.9)21 (87.5)13 (76.5)
Tumor size (mm)2.6±1.5*3.9±2.4*< 0.0012.6±1.7*4.8±3.2*0.005
Differentiation0.0580.760
 Differentiated153 (58.8)82 (49.4)14 (58.3)6 (52.9)
 Undifferentiated107 (41.2)84 (50.6)10 (41.7)8 (47.1)
N stage0.6480.247
 N0229 (88.1)142 (85.5)21 (87.4)12 (70.6)
 N120 (7.7)13 (7.8)1 (4.2)4 (23.5)
 N26 (2.3)8 (4.8)1 (4.2)1 (5.8)
 N35 (1.9)3 (1.8)1 (4.2)0 (0)

BMI = Body Mass Index; ECOG = Eastern Cooperative Oncology Group.

*Standard deviation.

Indicates χ2 test.


Postoperative and surgical results

In terms of surgical outcomes, there were differences in the type of reconstruction and extent of lymph node dissection between the groups in the BMI ≥25 cohort and in the extent of lymph node dissection in the BMI ≥30 cohort. Billroth-II anastomosis was performed more commonly in the LDG than in the ODG group. In addition, more D2 lymph node dissections were performed in the ODG than in the LDG (Table 2).

Postoperative and surgical outcomes

VariablesBMI ≥25 (kg/m2) (n=426)BMI ≥30 (kg/m2) (n=41)


LDG (%) (n=260)ODG (%) (n=166)p valueLDG (%) (n=24)ODG (%) (n=17)p value
Reconstruction type< 0.0010.110
 B-I45 (17.3)15 (9.0)3 (12.5)4 (23.5)
 B-II166 (63.8)147 (88.6)13 (54.2)12 (70.6)
 R-Y49 (18.8)4 (2.4)8 (33.3)1 (5.9)
LND< 0.0010.012
 D1+β173 (66.5)55 (33.1)17 (70.8)5 (29.4)
 ≥D287 (33.5)111 (66.9)7 (29.2)12 (70.6)
Retrieved LNs39.5±15.2*39.8±15.2*0.83441.1±14.5*39.7±15.2*0.754
Combine resection1.0001.000
 Yes4 (1.5)2 (1.2)23 (95.8)17 (100)
 No256 (98.5)164 (98.8)1 (4.2)0 (0)
Operation time (min)190.7±49.7*200.5±41.1*0.033190.0±64.4*206.8±50.1*0.375
EBL (ml)155.2±124.9*192.4±162.1*0.008151.9±100.2*187.9±119.3*0.300
First flatus (day)3.2±1.7*3.1±1.0*0.5493.1±0.6*3.4±0.5*0.212
Postoperative hospital stay (days)8.2±4.7*8.0±2.8*0.6299.6±5.8*7.9±1.4*0.231

LND = Lymph Node Dissection; EBL = Excessive Blood Loss.

*Standard deviation.

Indicates χ2 test.


In the LDG group, 87 patients (33.5%) underwent >D2 lymph node dissection, and 173 patients (66.5%) underwent D1+ lymph node dissection. In the ODG group, 111 patients (66.9%) underwent >D2 lymph node dissection and 55 patients (33.1%) D1+ lymph node dissection. Nevertheless, the number of retrieved lymph nodes showed no significant difference between the two groups (LDG vs. ODG: 39.5±15.2 vs. 39.8±15.2). An extended operation time was required in the ODG group compared with the LDG group in the BMI ≥25 cohort. However, the difference was minimal, and there was no significant difference in the BMI ≥30 cohort. Less blood loss was observed in the LDG group (155.2±124.9 ml) than in the ODG group (192.4±162.1 ml) in the BMI ≥25 cohort. The postoperative clinical course showed no significant differences between the two groups in terms of flatus day or length of hospital stay.

Postoperative complications

There were more overall complications in the ODG than in the LDG group in both cohorts. Among the complications, significant differences were observed in the rates of Clavien-Dindo I and II complications (Table 3), but not Clavien-Dindo III and IV complications, between the two groups in both cohorts.

Postoperative morbidities within 30 postoperative days

VariablesBMI ≥25 (kg/m2) (n=426)BMI ≥30 (kg/m2) (n=41)


LDG (%) (n=260)ODG (%) (n=166)p valueLDG (%) (n=24)ODG (%) (n=17)p value
Total number of postoperative morbidity49 (18.8)60 (36.1)<0.0015 (20.8)11 (64.7)0.009
Grade I, II39 (15)50 (30.1)4 (16.7)11 (64.7)
Grade III, IV10 (3.8)10 (6.0)1 (4.2)0 (0)
Grade I14 (5.4)21 (12.7)0.0110 (0)4 (23.5)0.024
Grade II25 (9.6)29 (17.5)0.0244 (16.7)7 (41.2)0.151
Grade IIIa8 (3.1)10 (6.0)0.2161 (4.2)0 (0)1.000
Grade IIIb1 (0.4)0 (0)1.0000 (0)0 (0)1.000
Grade IVa1 (0.4)0 (0)1.0000 (0)0 (0)1.000
Medical
 Pulmonary7 (2.7)17 (10.2)0 (0)4 (23.5)
 Cardiovascular0 (0)2 (1.2)0 (0)0 (0)
 Hepatic1 (0.4)2 (1.2)0 (0)1 (5.8)
 Urinary3 (1.2)1 (0.6)0 (0)0 (0)
Intra-abdominal
 Abscess0 (0)1 (0.6)0 (0)0 (0)
 Anastomosis bleeding1 (0.4)0 (0)0 (0)0 (0)
 Anastomosis leakage5 (1.9)3 (1.8)1 (4.2)1 (5.8)
 Anastomosis stenosis3 (1.2)1 (0.6)0 (0)0 (0)
 Bleeding8 (3.1)2 (1.2)0 (0)0 (0)
 Ileus14 (5.4)10 (6.0)2 (8.3)0 (0)
 Pancreatitis1 (0.4)3 (0.8)1 (4.2)0 (0)
Wound complications3 (1.2)18 (10.8)0 (0)5 (29.4)
Others3 (1.2)0 (0)1 (4.2)0 (0)

Indicates χ2 test.


The most common complications observed in the LDG group were ileus and bleeding, pulmonary complications, and anastomosis leakage. Pulmonary and wound complications were more common in the ODG group than in the LDG group and represented the main differences in terms of complications between the two groups. Based on risk factor evaluation, open distal gastrectomy, age >60 years, and BMI ≥30 were independent risk factors for postoperative morbidity among obese patients (Table 4).

Risk factors for postoperative morbidity

VariablesUnivariate analysisMultivariate analysis


Number of patients (n=426)Morbidities (%)p valueOdds ratiop value
Operative approach< 0.001< 0.001
 Open16660 (36.1)1
 Laparoscopy26049 (18.8)0.431 (0.273~0.683)
Age (years)0.0040.004
 <6021341 (19.2)1
 ≥6021368 (31.9)1.987 (1.252~3.153)
Sex0.0380.057
 Male30286 (28.5)1
 Female12412 (18.5)0.592 (0.344~1.020)
BMI0.0410.039
 <3038593 (24.21
 ≥304116 (39.0)2.106 (1.039~4.269)
ECOG PS0.547
 0, 1411104 (25.3)
 2,3155 (33.3)
Comorbidities1.000
 Absent420170 (25.5)
 Present62 (33.3)
History of abdominal surgery0.488
 Absent34285 (24.9)
 Present8424 (28.6)
Reconstruction type0.100
 B-I6018 (30.0)
 B-II31372 (23.0)
 R-Y5319 (35.8)
LND1.000
 D1+β22858 (25.4)
 D219851 (25.8)
Operation time (min)0.0450.158
 <20022849 (21.5)1
 ≥20019860 (30.3)1.396 (0.879~2.216)
EBL (ml)0.094
 <15019542 (21.5)
 ≥15023167 (29.0)
pN stage1.000
 N037195 (25.6)
 N1~35514 (25.5)

Significant values are indicated in bold. BMI = Body Mass Index; ECOG = Eastern Cooperative Oncology Group.

Binary logistic regression.


DISCUSSION

Major advancements in laparoscopic surgery for gastric cancer have been achieved since Kitano et al. first introduced laparoscopy-assisted distal gastrectomy in 1994.11 Subsequently, several retrospective and prospective studies have explored the surgical and oncologic safety of this technique. A meta-analysis of seven randomized controlled trials concluded that laparoscopic assisted gastrectomy significantly reduced blood loss and postoperative complications compared with open distal gastrectomy.12

Obese patients undergoing surgery have been examined in several reports. The postoperative complication rate varies among studies. Some studies have suggested that obesity does not affect postoperative morbidity or mortality.13,14 However, a longer operation time has been noted in obese patients.7

This study evaluated the postoperative complication rate after laparoscopic distal gastrectomy and the safety of laparoscopic distal gastrectomy in patients with a high BMI. The overall complication rate was higher in the ODG than in the LDG group in both cohorts. Specifically, the major complication rates did not differ between the two groups. However, minor complications, especially pulmonary and wound complications, were more common in the ODG group. Although more patients underwent lymph node dissection of >D2 in the ODG group compared with the LDG group, the number of retrieved lymph nodes did not differ between the two groups. In the BMI ≥25 cohort, the ODG group required a longer operation time. However, in the BMI ≥30 cohort, no significant difference in operation time was observed between the groups. Estimated blood loss was lower in the LDG group, but the postoperative clinical course showed no significant difference.

Kim W et al. reported that the wound complication rate of the LDG group was significantly lower than that in the ODG group.7 In our study, wound complications were more common in the ODG group. In obese patients, the risk of wound infections is likely to increase due to abundant subcutaneous fat.

In this study, pulmonary complications were significantly less common in the laparoscopic surgery group. Although objective measurements of postoperative pain were not performed, less pain in the LDG group allowed for early ambulation and prevented pulmonary complications.

In general, surgery in obese patients is associated with technical difficulties and a high complication rate. Especially in surgeries for cancer, in which sufficient lymph node dissection is important for curative resection, a large amount of intra-abdominal fat may obscure anatomical structures and hamper lymph node dissection. Laparoscopic gastrectomy for stomach cancer in patients with a high BMI is technically challenging; thus, the safety of this approach should be explored.

Based on our results, laparoscopic surgery can be more difficult during lymph node dissection for obese patients than for non-obese patients. However, laparoscopic surgery is not inferior to open surgery in obese patients.

This study has several limitations. First, it was designed as a single-institutional retrospective study with a focus on early gastric cancer. Further randomized controlled trials conducted in large cohorts are required to confirm the results of this study. Second, we enrolled patients from 2000 to 2014. In early 2000, the majority of surgeons preferred open gastrectomy over laparoscopic gastrectomy. Over time, as laparoscopic instruments became more developed and surgeons’ experiences increased, the preference shifted to laparoscopy. Patients who underwent laparoscopic gastrectomy at an earlier date may have had higher complication rates. In addition, the surgeon’s preference may lead to selection bias. Third, to ensure the safety of laparoscopic gastrectomy in obese patients, a comparison between obese patients and normal- or low-weight patients is required. In addition, future studies should explore the long-term safety, including cancer recurrence and disease-free survival rates, of laparoscopic gastrectomy in obese patients with gastric cancer.

In conclusion, LDG may improve surgical outcomes in obese patients undergoing surgery for early gastric cancer in terms of less excessive blood loss, shorter operation times, and lower complication rates. The conventional open gastrectomy approach, older age, and higher BMI are associated with postoperative morbidity in obese patients with early gastric cancer.

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