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Introduction
In Korea and Japan, the implementation of a nationwide surveillance program for the early detection of gastric carcinoma has resulted in a widespread acceptance of laparoscopic gastrectomy (LG) as a valid alternative to open surgery, for the treatment of early gastric cancer (EGC).1 Clinical advantages of LG over open surgery, including better cosmesis, less pain, faster bowel recovery, reduced hospital stay, lower morbidity, and improved short-term quality of life, have been reported in several studies.2,3,4 Furthermore, the long term outcomes of LG for EGC are comparable to those of open surgery, with a 5-year survival rate exceeding 98%.5
Obesity is regarded as a major technical limiting factor for LG, because of the substantial operative difficulties caused by the abundant visceral fat and a narrow operating field. However, increasingly advanced surgeon skills and laparoscopic instrument development have facilitated the conduction of studies designed to address the technical feasibility of LG in obese patients.6,7,8,9,10,11 Although the majority of these studies have concluded that LG is technically feasible and safe in obese patients with lower body mass indexs (BMIs) of ≥23 to ≥25 kg/m2, little information exist on the technical feasibility and safety of LG in morbidly obese patients (BMI of ≥30 kg/m2).12,13 In the present study, we aimed to evaluate the shortterm surgical outcomes of laparoscopic distal gastrectomy (LDG) in morbidly obese patients (BMI of ≥30 kg/m2) with gastric carcinoma.
Materials and Methods
1. Patients
Between January 2006 and September 2012, 1,532 patients underwent LDG for gastric carcinoma at our institute. Twenty patients who underwent combined surgery because of a concomitant malignancy were excluded, and the remaining 1,512 patients were retrospectively enrolled in the present study. The indication for LDG at our institution was a mucosal or submucosal cancer without lymph node metastasis (cT1N0) which was unsuitable for endoscopic resection. Some patients with advanced gastric cancer (cT2-3N0 or cN1-2) were subjected to laparoscopic surgery only for clinical trial purposes (ClinicalTrials.gov, NCT01088204). Preoperative work-up included esophagogastroduodenoscopy with biopsy and abdominopelvic computed tomography (CT). Electrocardiography, chest radiography, spirometry, and blood analysis were routinely performed for all patients. Endoscopic ultrasonography, magnetic resonance imaging, or chest CT was performed in selected patients for tumor staging. Patients were divided into three obesity groups: a normal group (BMI<25 kg/m2), an obese group (BMI 25~30 kg/m2), and a morbidly obese group (BMI≥30 kg/m2) according to the World Health Organization definition of obesity in the Asia-Pacific region.
Using the hospital prospective patient data registry, the following parameters were retrospectively collected: age, sex, abdominal surgery history, comorbidities, American Society of Anesthesiologists (ASA) physical status, pathology results, surgical procedures, operating time, intraoperative blood loss, intraoperative complications, postoperative course (time to flatus, time to diet initiation, and length of hospital stay), and postoperative complications. The amount of intraoperative blood loss was estimated by measuring the weight of blood-soaked surgical gauzes used during the operation. A postoperative complication was defined as any event that resulted in a deviation of the normal recovery phase necessitating medical or surgical intervention. A complication associated with the operating field was considered a local complication, and others were regarded as systemic. Complication severity was recorded as described by the Accordion Severity Grading System of Surgical Complications.14 Pathological tumor staging was based on the tumor-node-metastasis (TNM) classification system as described in the seventh edition of the Union for International Cancer Control.15
2. Operative technique
All operations were performed by three experienced surgeons. Briefly, with the patient in the reverse Trendelenburg position, two operator ports were placed on the patient's right side, two assistant ports on the left, and one umbilical port placed for laparoscope insertion. The liver was retracted upward through an additional 5-mm port placed at the epigastrium or by using a simple suturing technique. Under pneumoperitoneum at an insufflation pressure of 12 to 14 mmHg, the procedure began with the division of the greater omentum, 3 cm from the gastroepiploic vessels, and then moved toward the left gastroepiploic area. Lymph node dissection (LND) was performed as described in the Japanese Classification of Gastric Carcinoma (3rd English edition).16 In the present study, D1+LND refers to excision of perigastric lymph nodes and number 7, 8a, and 9 lymph nodes, and D2 LND refers to excision of perigastric lymph nodes and number 7, 8a, 9, 11p, and 12a lymph nodes. All gastric and LNDs were performed using LigaSureTM (LF5544; Valley Labs, Boulder, CO, USA) or a harmonic scalpel (ACE 36E; Ethicon Endo-Surgery, Cincinnati, OH, USA) as appropriate. After completing the gastric dissection, either intra- or extracorporeal anastomosis was performed at the surgeon's discretion. For extracorporeal anastomosis, a 4 to 5 cm upper midline abdominal incision was made, and the Billroth I reconstruction performed by externalization of the stomach through the incision. For intracorporeal anastomosis, the Billroth II method, performed using an endoscopic linear stapler, was the primary choice for reconstruction.
3. Statistical analysis
All the results are presented as means±standard deviations for continuous variables or as numbers and percentages for categorical variables. The three groups were compared with respect to clinicopathological characteristics, surgical outcomes, course of hospitalization, morbidity, and mortality, using one-way analysis of variance (ANOVA) or the chi-square test. The Student's t test or the chi-square test was used to compare surgical outcomes in the morbidly obese and normal groups. In addition, to determine the risks posed by morbid obesity on the different types of surgical procedure, a logistic regression analysis model was used to calculate the odds ratios of postoperative complications. The analysis was carried out using the SPSS software, version 12.0 for Windows (SPSS Inc., Chicago, IL, USA), and P-values of <0.05 were considered statistically significant throughout.
Results
Baseline characteristics of the three obesity groups are summarized in Table 1. The study subjects consisted of 992 males and 520 females with a mean age of 60.0 years. Among all patients, 996 (68.9%) were in the normal group, 471 (27.6%) in the obese group, and 45 (3.0%) in the morbidly obese group. Mean BMIs in these three groups were 22.2±1.9, 26.8±1.3, and 31.5±1.3 kg/m2, respectively. The patients' distribution across TNM stages was as follows: 1,406 (93.0%) stage I, 78 (5.2%) stage II, and 28 (1.9%) stage III.
Intergroup comparisons showed that the morbidly obese group had a significantly higher underlying comorbidity rate (75.6% vs. 45.8%, P<0.001) and a higher ASA score (ASA≥2, 82.2% vs. 65.0%, P=0.017) than the normal group. However, no significant intergroup differences were found between the three groups, with respect to age, gender, or abdominal surgery history. Pathological examination revealed no significant differences in the extent of tumor invasion or lymph node metastasis between the three groups.
1. Operative results
Intracorporeal or extracorporeal anastomoses were performed in 522 (34.5%) and 990 (65.5%) patients, respectively. The Billroth I, Billroth II, and Roux-en Y reconstructions were performed in 829 (54.8%), 623 (41.2%), and 60 (4.0%) patients, respectively. Among all patients, 831 underwent D1+LND and 681 underwent D2 LND.
Table 2 shows details of the operative results in the three obesity groups. The morbidly obese group underwent intracorporeal anastomosis more frequently (46.7% vs. 32.6%, P=0.041) than the normal group, but no significant differences were found in the extent of LND or omentectomy between the three groups. The morbidly obese group showed a significantly longer operating time than the normal group (240 minutes vs. 204 minutes, P=0.010), but intraoperative blood loss, intraoperative complications, and number of lymph nodes harvested were similar between the three groups.
2. Course of hospitalization and postoperative morbidity
Among all study subjects, the morbidity and mortality rates were 10.8% and 0.2%, respectively, and the mean length of hospital stay was 8.8±8.6 days (Table 3). Morbidity and mortality rates in the morbidly obese group were 13.3% and 0%, respectively, and not significantly different from those in the normal group. There were no significant differences in time to first flatus or time to diet initiation between the three groups. The lengths of hospital stay were also similar between the three groups (9.0 days in the normal group, 8.4 days in the obese group, and 8.2 days in the morbidly obese group, P=0.380).
Table 4 provides details of postoperative complications that occurred in the three obesity groups. Among all study subjects, the most common complication was luminal bleeding (2.1%), followed by abdominal infection (1.3%), gastric stasis (1.1%), abdominal bleeding (0.9%), and wound complications (0.8%). The rates of each complication were not significantly different between the three groups.
Table 5 represents univariate and multivariate analyses of risk factors for postoperative morbidity. In univariate analysis, old age, male gender, comorbidity, operating time, intraoperative bleeding, and Roux-en Y reconstruction were significantly associated with the development of postoperative complications after LDG, while obesity was not. Multivariate analysis revealed that older age, intraoperative bleeding, and Roux-en-Y reconstruction were independent risk factors for postoperative complications after LDG.
3. Subgroup analysis of operative risk by morbid obesity
Fig. 1 shows the effect of morbid obesity on the risk of postoperative complications (expressed as odds ratios) in different patient subgroups classified according to the types of operative procedure (omentectomy, LND, or reconstruction procedure) and demographic features (age and gender). The results showed that morbid obesity did not increase the risk of postoperative complications in any of the subgroups.
Discussion
Obesity is often regarded as a challenging problem for many surgeons who perform gastric cancer operations.17,18,19 Studies investigating the technical safety and feasibility of LG have been facilitated by an increasingly higher level of LG skills among surgeons. Most of these studies have been conducted in obese patients, but the feasibility of LG in morbidly obese patients with a BMI of ≥30 kg/m2, has been rarely examined. In the present study, we found that morbidly obese patients had short-term surgical outcomes that were comparable to those of normal patients. Except for a longer operating time, the differences observed between morbidly obese patients and the normal BMI patients in terms of postoperative recovery, length of hospital stay, or morbidity and mortality were not significant. The present study suggests that LDG can be safely performed in morbidly obese patients and should be considered as the primary treatment option for this patient group.
An early study by Noshiro and colleagues20 suggested that obesity is an ominous factor for LG, resulting in extended operating times, delayed bowel recovery, and increased rates of conversion to open surgery. However, more recent studies have shown that, with the exception of longer operating times, LDG did not significantly increase postoperative complications or length of hospital stay in obese patients.6,7,8,9,10,11 From a surgeon's perspective, laparoscopic surgery has important advantages over open surgery in obese patients, such as the creation of a sizeable working space in the abdominal cavity after pneumoperitoneum and a magnified view of the operating field. Makino and colleagues7 found that obesity significantly increased the operating time and the risk of intraoperative bleeding in open gastrectomy, but it did not have any effect in LG, concluding that the latter technique is more suitable than open surgery for obese patients.
The extracorporeal anastomosis procedure through a small abdominal incision during LDG can be particularly cumbersome in obese patients, due to their thick abdominal wall. Kim and colleagues13 have reported that obese patients had significantly longer operating times and more frequent postoperative complications after extracorporeal anastomosis compared to those in patients undergoing the procedure intracorporeally. We found that the operating times and postoperative complication rates were very similar between the normal and obese patients who underwent intracorporeal anastomosis during LDG. Our results support the view that intracorporeal anastomosis can be a more effective way of performing LG in obese patients.
The technical feasibility and safety of LDG has been evaluated in numerous studies in obese patients with relatively lower BMIs (≥23 to ≥25 kg/m2), but the feasibility of LDG in morbidly obese patients (BMI ≥30 kg/m2) remains elusive. However, the prevalence of morbid obesity is gradually increasing in Asian countries and, as a result, surgeons will undoubtedly encounter a progressively greater number of morbidly obese gastric cancer patients.21,22 To our knowledge, only one previous study has evaluated the surgical outcomes of LDG in morbidly obese patients. Contrary to our results, the authors reported longer operating times, larger intraoperative blood losses, delay in diet initiation, longer duration of hospital stays, and more postoperative complications in morbidly obese patients undergoing LDG.23 Considering the feasibility of LDG in morbidly obese patients may depend on the surgeon's experience in LG and on the quality of perioperative hospital management, additional studies are necessary to address conclusively the feasibility and safety of LDG in morbidly obese patients with gastric carcinoma.
Some limitations deserve consideration in the present study. First, the study was inherently limited by its retrospective design, and thus, selection bias. Bias may have resulted from a preference of inexperienced surgeons, during their initial phases of training, for patients with a lower BMI for laparoscopic surgery, which followed the selection of more obese patients as they accumulated surgical experience. Thus, this learning curve effect may have minimized the differences in surgical outcomes, such as operating time and morbidity, between groups. LG is technically demanding in morbidly obese patients as reflected in the longer operating times, and the findings of this study may suggest that a substantial laparoscopic surgery experience is necessary for successful operative outcomes in morbidly obese patients. Second, although the present study demonstrates the feasibility of LDG in morbidly obese patients, it would be more appropriate to evaluate the value of LG by comparing the surgical outcomes of open and LG in these patients. However, this type of analysis might be somewhat difficult to undertake using a retrospective study design because of the broad variety of operative indications for open and LG.
In conclusion, the present study demonstrated the technical feasibility and safety of LDG in morbidly obese patients with gastric cancer. Despite a longer operating time, no significant differences were found between the normal and morbidly obese patients in terms of postoperative recovery, length of hospital stay, or morbidity and mortality. LDG can be safely performed in morbidly obese patients by experienced surgeons and should be considered as the primary treatment option for this patient group.
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