Gastric cancer is the one of the most common malignancies in developing countries [1]. Like other gastrointestinal malignancies, gastric cancer usually presents in elderly patients [2, 3]. The average age of the population and consequently the number of elderly people has been increasing all over the world, particularly in developing countries [4]. In the future, surgeons can expect to operate more frequently on elderly patients with both malignancies and comorbid medical conditions. Preexisting diseases such as cardiovascular disease, diabetes mellitus and other malignancies impair physical function and make their treatment difficult [5, 6]. Age exceeding 70 years is an independent predictor of increased postoperative complications, in-hospital mortality and a longer hospital stay [5, 7, 8].

Since the first report by Kitano in 1994 [9], laparoscopy-assisted distal gastrectomy (LADG) has been rapidly adopted for the treatment of both early and advanced gastric cancers which need lymph node dissection [10–13]. Prospective randomized trials have revealed that laparoscopic surgery for gastric cancer is feasible, oncologically safe and associated with superior perioperative outcomes when compared to traditional open surgery [14–16]. The advantages reported by several reports included decreased morbidity rate, decreased pain, faster recovery and shorter postoperative hospital stay [17–19]. However, it is important to determine whether elderly patients with gastric cancer can benefit from laparoscopic surgery. Elderly patients who have less functional reserve and more comorbid diseases may be harmed by carbon dioxide pneumoperitoneum which is almost harmless to young patients [20]. Since the interactions among age, comorbidity and short-term surgical outcome were unclear, perioperative outcomes in laparoscopic surgery for the elderly patient with gastric cancer remained non-conclusive.

Published data comparing laparoscopic with open gastrectomy surgery for gastric cancer in elderly patient are limited. Although several studies have reported the safety and benefits of laparoscopic surgery for gastric cancer in elderly, most authors preferred to compare the findings after laparoscopy in the elderly with those in younger patients in order to determine whether or not they had the same benefit from the operation [21, 22]. These researches could not illustrate that the laparoscopic surgery for gastric cancer in elder patients were more effective and safety than traditional open surgery. Therefore, our study aimed to compare the surgical and early postoperative outcomes of laparoscopy-assisted distal gastrectomy (LADG) with those of open distal gastrectomy (ODG) for gastric cancer in patients 70 years of age or older.

Materials and methods

Consecutive patients, aged 70 years and older, who underwent laparoscopic or open distal gastrectomy for gastric cancer at the Department of gastrointestinal Surgery, Shanghai Tenth People’s Hospital, Tongji University, from February 2013 to January 2014 were retrospectively selected from a prospectively designed database. The patients were divided into two groups. The first group was considered as the study group and contained the patients who underwent laparoscopy-assisted distal gastrectomy (LADG group). Patients who underwent traditional open distal gastrectomy were included in the control groups (ODG group).

The exclusion criteria ruled out urgent or emergent procedures, operation other than distal gastrectomy such as total gastrectomy, proximal gastrectomy, wedge resection and procedures with combined resection of another organ(s). Preoperative diagnosis of gastric cancer was determined by esophagogastroduodenoscopy with tumor biopsy, endoscopic ultrasound and computed tomography scan.

Before the operation, we fully informed patients the situation of their diseases which they were suffering from, the brief surgical procedures of laparoscopic surgery and open surgery, and the postoperative complications which may occur after operation. And based on the results of past studies in which the treatment of laparoscopic surgery and open surgery was compared in other malignant disease, such as colon cancer and rectum cancer, we explained to the patients the possible benefits they may receive after laparoscopic surgery or open surgery. All of our patients had the personal conversation with their surgeon. Then, the choice between laparoscopy-assisted and open distal gastrectomy was left up to patient. Written informed consents were obtained from all patients before the operation.

The data evaluated included preoperative patient baseline parameters, perioperative variables, postoperative outcomes and pathologic results. The preoperative parameters analyzed were age, gender, body mass index (BMI), American Society of Anesthesiology (ASA) classification, abdominal surgery and comorbidities which were assessed by Charlson comorbidity index (CCI) [23, 24]. Perioperative variables included mode of anastomosis, length of the operation, estimated blood loss, time to first flatus, time to first oral diet, duration of analgesics administered and postoperative length of hospital stay. For the laparoscopic cases, the reason for conversion to laparotomy was obtained. Postoperative outcomes included postoperative complications, 30-day mortality, recurrence and metastases. Pathologic results were analyzed by tumor size, depth of invasion, number of dissected lymph nodes, lymph node metastasis and cancer stage according to TNM classification, 7th edition of the UICC.

In our institution, we have defined conversion as the need to perform conventional laparotomy to accomplish the procedure for the reasons of patient’s safety, equipment failure, tumor factors such as anatomical uncertainty and invasion to surrounding organs, or the development of complications such as uncontrolled bleeding, injury of adjacent structures and cavity viscera rupture. A postoperative complication was defined as any problem that required additional conservative or surgical treatment. Major postoperative complications were defined as surgical complications requiring management by an endoscopic or interventional procedure or re-operation such as anastomotic leakage, duodenal stump leakage and wound dehiscence [25]. Other postoperative complications were defined as minor events resulting in a delay in discharge from the hospital or readmission to the hospital within 30 days of discharge.

Postoperative follow-up was conducted by means of direct interviews in outpatient clinic or telephone interviews with patients or their family members. Patients follow-up was scheduled to perform abdominopelvic computed tomography scan and laboratory tests (including tumor markers such as carcinoembryonic antigen and CA19-9) every 6 months after surgery. Endoscopy was suggested every 6 months to monitor recurrence for patients with T3b depth or N1 lymph node metastasis or recurrence suspected, and once a year for other patients after surgery.

All statistical analyses were performed using Social Science (SPSS) 14.0 for windows (SPSS Inc. Chicago, IL, USA). Descriptive data were expressed as mean ± standard error of the mean (SEM), as medians and range or as the number of patients and the percentage. Quantitative and qualitative variables were compared with Student’s t test and the Chi-square (Pearson’s or Fischer’s exact) test, respectively. The Mann–Whitney U test was used for variables not distributed normally. Kaplan–Meier analysis was used for survival analysis. A P value <0.05 was considered to indicate statistical significance.

Surgical procedure

Under general anesthesia, each patient was placed in a supine position with legs apart. After creation of carbon dioxide pneumoperitoneum, one initial 10-mm camera port was introduced below the umbilicus and other four trocars were placed in a “U” shape. Among them, a 12-mm trocar was inserted in the left hypochondria region as main operated port and other three 5-mm trocars were placed as assistant ports.

At the beginning, we divided the greater omentum from the midportion of the gastroepiploic arcade to left gastroepiploic vessel with lymph node around dissected. After that, the inferior border of the pancreas neck portion was dissociated with the middle colic vessels identified carefully. Then, the division was continued toward the right gastroepiploic area, and the right gastroepiploic vessels and gastric artery were divided at the root to clear lymph nodes 6 and 5. In some patients, dissection was advanced to lymph node 14 v around the superior mesenteric vein. After overturning up the gastric body and greater omentum, the lymph nodes 8 a around the common hepatic and the lymph nodes 12 a in the area of proper hepatic arteries were dissected. Then, we dissociated the celiac axis. The left gastric vein and artery were exposed and divided individually at the origin with lymph nodes 7 and 9 removed. The lymph node dissection was continued toward the area of lesser curvature of stomach (lymph node 3) and proximal splenic artery (lymph node 11p).

After all the lymph nodes had been cleared, we transected the duodenum about 2 cm distal from the pylorus with endoscopic linear stapler and then a 7-cm laparotomy was made under the xyphoid. The remnant stomach was put out from abdominal cavity and transected by linear stapler under direct vision. After removing the specimen, gastroduodenostomy (Billroth I) or gastrojejunostomy (Billroth II) was performed.

Open operations were performed in a routing protocol as previously reported. Gastrectomy and D2 lymph node dissection were performed basically with an 18- to 20-cm-length incision from subxiphoid to periumbilical area.

All gastrostomies were performed by the same surgeon experienced both in traditional open resection and laparoscopic gastrectomy in our department.

Results

Patient characteristics

There were 50 elderly patients (70 years of age or older) who had distal gastrectomy for gastric cancer at our institution from February 2013 to January 2014. There were 23 patients in LADG group and 27 patients in ODG group with mean ages of 76.6 ± 4.6 and 80.0 ± 5.4 years, respectively. Table 1 presents the clinical background of the 50 patients. The incidence of comorbidity conditions was high in both groups. Only 30.4 % of the patients in LADG group (n = 7) and 25.9 % of the patients in ODG group (n = 7) had no preexisting comorbidity (CCI = 0). The proportion of patients with ASA score 3 or 4 was 52.5 % in the LADG group (n = 12) and 48.1 % in the ODG group (n = 13). The comparisons between the groups revealed statistically similar results regarding age, gender, BMI, ASA class, history of previous surgeries and CCI.

Table 1 Patient demographics of LADG and ODG group
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The type of surgical procedure and the early surgical outcomes are summarized in Table 2. Eight patients in LADG group and 9 patients in ODG group underwent distal gastrectomy with anastomosis of Billroth I type, and the remaining patients in the two groups underwent distal gastrectomy with anastomosis of Billroth II type. All the operations were curative. The rate of conversion to laparotomy was 13.0 % (n = 3). The reasons for conversion were dense adhesions from previous surgery (4.3 %, n = 1), bleeding (4.3 %, n = 1) and patient intolerance of pneumoperitoneum with excessively high airway pressures (4.3 %, n = 1).

Table 2 Surgical and oncological outcomes of LADG and ODG group
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Surgical outcomes

Open surgery was 28 min faster than laparoscopic surgery, but the difference between the two groups was not significant (P = 0.054). There was a significant reduction (P < 0.001) in the estimated blood loss in LADG group (100 mL; range 50–600 mL) compared with that in ODG group (250 mL; range 100–650 mL). Patients in LADG group had a faster return of postoperative bowel function. Time to first flatus was significantly shorter (P < 0.001) in the LADG group (51.6 ± 9.84 h) than in the ODG group (67.2 ± 13.2 h). Days to oral intake were also significantly fewer (P = 0.002) in the LADG group (6.1 ± 2.0 days) than in the ODG group (7.9 ± 1.9 days). The use of analgesic drugs was significantly less after LADG (P < 0.001), and the postoperative hospital stay was significantly shorter (P < 0.001) in the LADG group (12 days; range 8–18 days) than in the ODG group (16 days; range 9–21 days) (Table 2).

Postoperative complications

Table 3 gives details of the postoperative complications in the two groups. In our study, major postoperative complications occurred in 2 LADG patients and 3 ODG patients. In laparoscopic group, 1 patient experienced anastomotic leakage and 1 patient experienced duodenal stump leakage. In open surgery group, 1 patient experienced anastomotic leakage, 1 patient experienced intraluminal bleeding, and 1 patient experienced wound dehiscence. The difference in major postoperative complications between the two groups was not statistically significant (P = 0.618). The overall complication rate in the LADG group (21.7 %) was lower than that in the ODG group (25.9 %), but the difference did not reach statistical significance (P = 0.730). There were no incidences of postoperative mortality during the first 30 postoperative days.

Table 3 Postoperative complications of LADG and ODG group
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Pathological results

Table 4 presents the pathology finding for the two groups. The groups did not differ significantly in terms of depth of invasion (P = 0.761), nodal catalog (P = 0.847), tumor stage (P = 0.618), diameter of tumor (P = 0.169), number of retrieved lymph nodes (P = 0.946) and number of positive lymph node metastasis (P = 0.820).

Table 4 Pathological data of LADG and ODG group
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Follow-up

During a median follow-up period of 19 months (range 8–26 months), the overall 2-year survival rate was 60.5 % in the LADG group and 65.7 % in the ODG group. The overall survival analysis shown in Fig. 1 indicated that there was no significant difference in the overall survival rate between the two groups (P = 0.719). Postoperative recurrence was observed in 8 patients (34.7 %) in LADG group compared to 6 patients (22.2 %) in ODG group. Postoperative metastasis occurred in 4 patients (17.4 %) in LADG group compared to 6 patients (22.2 %) in ODG group. No significant differences in the rate of postoperative recurrence or metastasis were observed in the two groups (Table 2).

Fig. 1
figure 1

Kaplan–Meier overall survival curves of the LADG group and the ODG group

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Discussion

Gastric cancer currently is the second most common cause of cancer-related deaths in the world [26]. As life expectancy increases, the number of elderly patients with both malignancies and comorbid medical conditions has significantly increased. The proportion of aged patients with a diagnosis of gastric cancer is expected to increase gradually over the next few decades in Eastern Asia, Eastern Europe and South American [1, 27, 28]. Surgical resection has remained the mainstay treatment for patients with gastric cancer. Because aging is associated with a gradual loss of reserve capacity [29], even in individuals without obvious underlying comorbidities, age exceeding 70 years is an independent risk factor for gastric cancer to increasing occurrence of postoperative mortality, complication and longer hospital stay [5, 7]. For patients aged 70 years and above, the 30-day mortality is about 6 % and at least 20 % develop one complication during hospitalization. In addition, mortality risk increases 10 % for every year after age 70 [8].

Since laparoscopic gastrectomy was reported by Kitano et al. in 1994 [9], it has been possible to treat both early and advanced gastric cancers successfully by surgical resection, which involved laparoscopy-assisted gastrectomy with lymph node dissection [10–13]. By randomized clinical trials compared with conventional open surgery, laparoscopic gastrectomy for gastric cancer has already been accepted in terms of postoperative benefits, such as improved cosmetic effect, reduced pain, earlier recovery, shorter hospital stay, less morbidity, less mortality and better quality of life [17, 30–33]. A recent meta-analysis showed that LADG had significantly lower overall morbidity, surgical site infection and pulmonary complication rates than open gastrectomy [34]. With the increased number of LADG performed, elderly patients might benefit from the less invasive nature of laparoscopic surgery. However, it is important to determine whether these advantages can be applied to elderly patients because carbon dioxide pneumoperitoneum required for laparoscopic procedures may be harmful to elderly patients and more comorbidities and reduced physiological reserves in elderly patients means more postoperative morbidity and mortality [20, 35]. Two recent, multicenter studies performed in Korea indicated contradictory results on the impact of age and comorbidity on surgical outcomes of LADG [36, 37]. Therefore, there are limited data about the efficacy of laparoscopic gastrectomy in the elderly, especially those 70 years of age or older.

We employed the current study designed to compare laparoscopy-assisted distal gastrectomy in elderly patients with gastric cancer to open distal gastrectomy and clarify the feasibility and efficacy of laparoscopic surgery in elderly patients with gastric cancer. We found that the two groups in this study were no significantly different in terms of demographic and pathologic characteristics, postoperative complication and oncology outcomes. Our current study echoes with the findings of other studies [38, 39]. Laparoscopy-assisted distal gastrectomy for gastric cancer is shown to be more feasible for elderly patients than open distal gastrectomy, resulting in better short-term outcomes including reduced blood loss, less narcotic use, faster bowel function recovery and shorter hospital stay.

The laparoscopic progress of gastric cancer was mostly believed to be a time-consuming procedure [31, 38, 40]. Kitano et al. reported a multicenter study of the oncologic outcomes of laparoscopy-assisted total gastrectomy (LATG) for 1294 patients with gastric cancer in Japan, among whom 55 patients underwent LATG. The authors reported a mean operating time of 271 min in LATG group, longer than that in open total gastrectomy (OTG) group [14]. However, in our present study, LADG group showed a mean operative time only 28 min longer than that of ODG group, and this difference was not found to be statistically significant. With increasing laparoscopic surgery carried out, the surgeon whose learning curve of laparoscopic surgery for gastric cancer came into the platform was becoming more and more mature in laparoscopic technique. The use of up-to-date laparoscopic instrumentation such as laparoscopic coagulating shears or Ligasure for dissection, the endoscopic stapler for resection and hemo-lock vascular clip for hemostasis simplified the progress. Because of the subjective and objective reasons above, the operation time was significantly decreased in LADG group.

Our study did not show that the postoperative complication rate of intraluminal bleeding fell when elderly patients were treated with laparoscopic rather than open surgery. But it revealed that when laparoscopy and open surgery are compared; laparoscopy may reduce the amount of bleeding in patients over 70 during distal gastrectomy for gastric cancer. The estimated intraoperative blood loss was significantly decreased by approximately 150 mL in LADG. We presumed that small wound, the use of laparoscopic coagulating shears or Ligasure, the sensitive ability of camera to detect vessels and the concept of blunt dissection along natural anatomical structure may contribute to decreasing blood loss. Less blood loss indicated a smaller potential risk of operation in LADG and may be preferred by both surgeons and patients.

Many reports demonstrated that laparoscopic surgery led to a faster return to a full diet and a shorter postoperative hospital stay. Usui et al. [41] reported that LATG has the advantage compared with OTG of a shorter recovery time, in terms of shorter time to first flatus, time to initiate oral intake and postoperative hospital stay. Our results are similar to their report. The length of the hospital stay depends not only on patients’ medical condition such as postoperative pain, return of gastrointestinal function and postoperative complication, but also on their ability of daily life. We had observed that the old patients in ODG group were more likely to require inpatient rehabilitation due to their declined mobility status and longer postoperative wound pain which seriously hampered the recovery of activities of daily life. A shorter postoperative hospital stay in LADG group may reflect that the potentially reduced surgical stimulus of laparoscopic surgery does impact on the systematic functional recovery of the elderly patients.

In our study, the rate of postoperative complications was not significantly different in LADG and ODG groups (21.7 vs. 25.9 %) and was two times higher than that obtained in the studies of overall age band. Hu et al. [42] reported that postoperative complication of 1184 patients with advanced gastric cancer was 10.2 %. The most common major complication of distal gastrectomy for gastric cancer in elder patients was anastomosis-related leakage and duodenal stump leakage. Usually, the occurrence of leakage-related complication might reflect surgical inexperience and be a matter of learning curve [43]. Because in our study we completed the anastomy by extracorporeal hand-sewn and reinforced the duodenal stump by interrupted suture under direct vision after linear stapler closing both in LADG group and ODG group, it may decrease the occurrence rate of major complication in the group of LADG. Acute cardiac failure was the most common minor complication of distal gastrectomy for gastric cancer, and the incidence of acute cardiac failure in our study was similar irrespective of whether the patient underwent laparoscopic or open surgery. A postoperative pulmonary complication, pneumonia, occurred in only 1 patient in each group, and there was no significant difference between LADG and ODG group. In some reports, it was supposed that the adverse cardiopulmonary effect caused by pneumoperitoneum occurred only when the intra-abdominal pressure was more than 15 mmHg, and low intra-abdominal pressure did not influence the output [44–46]. So it may be safe to perform laparoscopic surgery even in high-risk patients, such as very elderly patients.

The oncologic result of LADG in elderly patients has not yet been determined. In the studies of overall age band, Hu et al. [42] reported that the cumulative 3-year overall survival rate of laparoscopy-assisted gastrectomy for advanced gastric cancer was 75.3 % and the postoperative recurrence rate was 16.7 %. Mochiki et al. [47] suggested that LATG could be a curative therapy for EGC in terms of oncological safety through the comparison of 5-year cumulative survival between LATG and OTG. Hamabe et al. [48] reported that laparoscopy-assisted gastrectomy, including the 21 LATG and 35 OTG cases, is acceptable in terms of long-term oncological results for advanced gastric cancer (AGC) treatment. In this study, we also confirmed similar oncologic outcomes of LADG compared with those of ODG in elderly patients, though the survival rate was lower and recurrence rate was higher than that of the study with overall age band.

Our study had the inherent limitations of retrospective and non-randomized studies, so there was a possibility of selection bias and observer bias with regard to the adoption of the operative approach. In perioperative period, the surgeons might encourage the patients in the group of LADG to move earlier and discharge them earlier. Furthermore, our study had the limitations due to its small number of cases. However, the patients in the two groups had similar demographics, such as age, sex, BMI, ASA, TNM and CCI. Several potential confounding factors have not been considered, such as tumor location, postoperative chemotherapy, which may influence surgical and oncological outcomes of our study. In the future, multicenter randomized controlled trials comparing LADG and ODG in elderly patients with gastric cancer should be conducted to confirm the efficacy and safety of laparoscopic resection in elderly patients.

Conclusions

To the best of our knowledge, our study was the first to evaluate the surgical outcomes of laparoscopy-assisted distal gastrectomy for elderly patients with gastric cancer. The results of our study demonstrated that laparoscopy-assisted distal gastrectomy for gastric cancer in patients older than 70 years was associated with less intraoperative blood loss, less narcotic use, faster bowel function recovery and shorter hospital stay than open resection and no difference was observed in the postoperative complication rate, survival rate, postoperative recurrence and metastasis rate between the patients who underwent LADG and ODG. In conclusion, we suggest that laparoscopy-assisted distal gastrectomy for gastric cancer is feasible, efficacious and safe in elderly patients and may be superior to conventional open resection as regards some surgical outcomes.