Laparoscopy-assisted distal gastrectomy (LADG) for gastric cancer has been widely accepted since it was first introduced in 1994.1 LADG has some advantages, including good cosmetic results and less invasiveness because of the small incisions required and the reduced time of extracorporeal manipulation.2,3 In recent years, several studies have also demonstrated good short-term and long-term outcomes of LADG with D2 lymphadenectomy for advanced gastric cancer, and other studies have shown satisfactory results of intracorporeal anastomosis as a method of postgastrectomy reconstruction.4,5 However, unlike other laparoscopy-assisted surgeries such as colorectal surgery and cholecystectomy, LADG is not commonly performed in general hospitals. This is because advanced skills are required during lymph node dissection and reconstruction, which cause extended operative times and an increased risk of operative complications.
Hand-assisted laparoscopic surgery (HALS) is a hybrid procedure that allows surgeons to perform laparoscopic surgery using their hand. The tactile sensation of the surgeon’s hand allows the gentle manipulation of organs and an easy extension of the surgical field. Furthermore, having a hand in the abdominal cavity can be useful for securing vessels and for the rapid control of bleeding, contributing to operative safety. However, limited information is available regarding the features and role of hand-assisted laparoscopic distal gastrectomy (HALDG), which is a HALS technique, compared with those of LADG in the treatment of gastric cancer. In addition, the usefulness of HALS for gastric cancer remains unclear. Therefore, the purpose of this study was to clarify the clinical features of HALDG compared with LADG and to evaluate the role of HALDG in the treatment of gastric cancer.
MATERIALS AND METHODS
Patients who consecutively underwent HALDG or LADG for pathological stage I gastric cancer at Nihon University Hospital between April 2005 and November 2016 were eligible for the study. Diagnoses of all patients were preoperatively confirmed by a pathological examination of gastroscopic biopsy samples. Before surgery, abdominal computed tomography and ultrasonography were conducted to rule out possible distant metastasis. Patients who had remnant gastric cancer were excluded. The operative procedure was selected by several experienced surgeons during a preoperative conference. All patients received either D1+, D1+β, or D2 lymph node dissection according to the Japanese Gastric Cancer Treatment Guidelines.6,7 Pathological stages were classified according to the Japanese Classification of Gastric Carcinoma.8 The same postoperative treatment protocols were applied to all patients. Appropriate timing for starting a soft diet and for the discharge of patients was finally decided by the attending surgeon in accordance with the patients’ conditions.
Patients were placed on the operating table in the supine position under general and epidural anesthesia in each procedure.
Incisions of 7 cm were made below the xiphoid at the beginning of the operation; a hand-port device (Gelport; Applied Medical, Rancho Santa Margarita, CA) was then placed. Omentectomy and isolation from the transverse colon were directly performed through the incision. A 12 mm trocar (FineSEAL disposable trocar; Lagis Enterprise Co. Ltd, Taiwan) was inserted at the umbilicus. Subsequently, pneumoperitoneum was induced. An additional 12 mm and two 5 mm trocars were placed under the pneumoperitoneum. The surgeon stood at the right side of the patient and performed the procedure using the right-sided trocar. Stomach mobilization, vessel transection, and lymph node dissection were performed laparoscopically (Figs. 1A, C). Finally, stomach transection and reconstruction were directly performed through the incision. After reconstruction, the intra-abdominal cavity was rechecked for bleeding. Finally, after the placement of a drainage tube, the operation was completed.
The conventional 5-trocar method was applied in LADG. A 12 mm trocar was initially inserted at the umbilicus using an open technique. Following the induction of pneumoperitoneum, 2 additional 12 mm and two 5 mm trocars were placed. Exclusion of the liver was performed as gently as possible using a liver retractor with Silicone Disc (Hakko Co. Ltd, Tokyo, Japan) that was placed below the xiphoid. The surgeon mainly stood at the right side of the patient and performed the procedure using 2 right-sided trocars. However, the surgeon performed No. 6 lymph node dissection on the left side of the patient, unlike in HALDG. Stomach mobilization, vessel transection, and lymph node dissection were performed laparoscopically in the same manner as in HALDG (Figs. 1B, D).
LADG comprises 2 reconstruction procedures. At the beginning of this series, we performed extracorporeal reconstruction in LADG. An incision of 5 cm length was made under the xiphoid, and a wound sealing device was placed. Stomach transection and reconstruction were directly performed through this incision. We applied intracorporeal reconstruction to LADG throughout these procedures. After transecting the stomach, the initial umbilical incision was extended to 5 cm, and a wound sealing device was placed. Subsequently, the transected specimen was extracted through this incision, and the tumor location was confirmed in the transected specimen. Pneumoperitoneum was induced again, and reconstruction was subsequently performed intracorporeally. The operation was concluded after the placement of a drainage tube.
In this study, the reconstruction procedure comprised 2 methods: Billroth-I (B-I) reconstruction was routinely performed in each procedure, and Roux-en-Y (R-Y) reconstruction was selected if B-I reconstruction was contraindicated, such as when the remnant stomach was too small. In HALDG, B-I reconstruction was performed using hand sutures. R-Y reconstruction was performed using linear staplers (Endo GIA with Tri-Staple Technology; Medtronic, Dublin, Ireland) in gastrojejunostomy and using hand sutures in jejunojejunostomy. In LADG, extracorporeal B-I reconstruction was performed using hand sutures, and intracorporeal B-I reconstruction was performed with delta-shaped anastomosis using linear staplers.9 R-Y reconstruction was performed using linear staplers in gastrojejunostomy and using hand sutures in jejunojejunostomy.
An ultrasonic incision or vessel-sealing system was used during surgery in each procedure. Two experts certified for the Japan Society for Endoscopic Surgery (JSES) Endoscopic Surgical Skill Qualification System for laparoscopic surgery performed HALDG or LADG in all cases. Informed consent was obtained preoperatively from all patients after a comprehensive explanation of the surgical risks. This study was approved by the institutional review board of our hospital (No. 20190203).
Patient indices [age, sex, body mass index (BMI), American Society of Anesthesiologists Physical Status (ASA-PS), comorbidity, pathological stage, and history of laparotomy], operative indices (operative time, blood loss, number of harvested lymph nodes, extent of lymph node dissection, reconstruction procedure, rate of combined surgery and conversion to laparotomy), and postoperative recovery indices (time to first flatus, time to soft diet and walk, body temperature ≥38°C, number of analgesics used, serum C-reactive protein (CRP) levels on postoperative days (POD) 1, 3 or 4, and 7, alanine aminotransferase (ALT) level on POD 1, aspartate aminotransferase (AST) level on POD 1, postoperative complications (Clavien-Dindo, CD, Classification≥grade 3),10 length of postoperative hospital stay, readmission rate within 30 POD, and mortality rate] were investigated. Variables are presented as the median with range or as the number of patients with percentages. The 3-year relapse-free survival (3Y-RFS) and 3-year overall survival (3Y-OS) rates were calculated for each group and the results were compared. In addition, the total cost of operative devices in each procedure was compared.
Data analysis was performed using JMP, version 14.0.0 (SAS Institute Inc., Cary, NC). Statistical analysis was performed using the χ2 test and Wilcoxon signed-rank test. The cutoff value of operative time in each group was decided using the receiver operating characteristic curve. Factors affecting prolonged operative time were analyzed using logistic regression analysis. The Kaplan-Meier method was used to estimate 3Y-RFS and 3Y-OS rates, while the log-rank test and hazard ratio (HR) [95% confidence interval (CI)] by Cox regression models were used for comparison between the 2 groups. Statistical significance was defined as P-value <0.05.
Among the 148 eligible patients, HALDG and LADG were performed for 58 and 90 patients, respectively. The characteristics of patients who underwent each procedure are shown in Table 1. There were no significant differences between the 2 groups in terms of patient background.
Operative outcomes are summarized in Table 2. Operative time was significantly shorter in the HALDG group than in the LADG group. In contrast, blood loss was significantly higher in the HALDG group than in the LADG group. There were no significant differences in the number of harvested lymph nodes, reconstruction procedures, and combined surgery between these groups. Both groups had no conversion to laparotomy and reoperation.
The comparison of postoperative recovery between the HALDG and LADG groups is summarized in Table 3. There were no significant differences in the number of postoperative analgesics used, time to first walk, time to first flatus, number of patients with body temperature ≥38°C, and postoperative CRP levels. Serum AST and ALT levels on POD 1 were significantly lower in the HALDG group than in the LADG group. However, the time to soft diet and length of postoperative hospital stay were significantly shorter in the LADG group than in the HALDG group. Postoperative complications (CD ≥grade 3) were observed in 4 patients in the HALDG group and in 6 patients in the LADG group. All complications in these groups resolved without additional surgery.
Figure 2 shows 3Y-RFS and 3Y-OS rates in both groups, respectively. The 3Y-RFS rate was 98.2% with HALDG versus 98.9% with LADG [P=0.73; HR, 0.617 (95% CI: 0.024-15.58)], while the 3Y-OS rate was 98.2% with HALDG versus 98.9% with LADG [P=0.73; HR, 0.618 (95% CI: 0.024-15.61)]. There was no significant difference in 3Y-RFS and 3Y-OS rates between these groups.
The total costs of laparoscopic devices (trocars, staplers, a hand-port device, wound sealing devices, and liver retractors) in both groups are shown in Table 4. In B-I reconstruction, the cost amounted to 1621.38 USD in the HALDG group and 2352.36 USD in the LADG group. The costs were reduced by 31% when performing HALDG. In R-Y reconstruction, the cost amounted to 2572.46 USD in the HALDG group and 2678.44 USD in the LADG group. The costs were reduced by 4% when performing HALDG.
We also analyzed the extent to which HALS affected operative time. In accordance with the results of receiver operating characteristic curve analysis, operative time of ≥220 minutes was defined as the prolonged operative time (area under the curve, 0.73; 95% CI: 0.64-0.80) (Fig. 3). Univariate analysis demonstrated that sex (male), operative procedure (LADG), reconstruction procedure (R-Y), and extent of lymph node dissection (D2) were significantly associated with prolonged operative times (Table 5). These 4 factors, and others which are likely to affect operative time, such as the presence of combined surgery, BMI (>25 kg/m2), and history of laparotomy, were included in the multivariate analysis. In the multivariate analysis, operative procedure, reconstruction procedure, BMI, sex, and extent of lymph node dissection showed a significant relationship with prolonged operative time (Table 6). In particular, the operative procedure (LADG/HALDG) strongly affected operative time (odds ratio, 9.65; P<0.001; 95% CI: 3.86-24.10).
In the present study, we analyzed the short-term outcomes, recovery status, and prognosis of patients who underwent HALDG and LADG for stage I gastric cancer. This study demonstrated that operative time was significantly shorter in the HALDG group than in the LADG group, and comparable invasiveness, 3Y-RFS, and 3Y-OS rates were noted in both groups. In contrast, our findings also revealed that blood loss was significantly higher, and the time to first soft diet and length of postoperative hospital stay were slightly longer in the HALDG group than in the LADG group.
LADG is beneficial in terms of lesser pain, faster recovery, and reduced respiratory complications compared with open surgery.2,3 Previous prospective studies provided evidence regarding postoperative complications such as anastomosis leakage and pancreatic fistula in LADG for stage I gastric cancer.11 Moreover, several studies have demonstrated good short-term outcomes of LADG for advanced gastric cancer compared with open surgery.4,5 However, LADG is yet to be widely accepted in clinical practice despite its benefits. This is due to the requirement for advanced skills for lymph node dissection and reconstruction in LADG. Moreover, a prolonged operative time and learning curve are associated with LADG.
HALS is a hybrid approach that provides surgeons with the benefits of both the reduced invasiveness of laparoscopic surgery and the convenience of open surgery. Previous studies have shown HALS to be a less invasive approach than open surgery in various diseases.12,13 HALS has also been shown to be beneficial compared with laparoscopic surgery in various diseases as it offers reduced operative time and open conversion, in addition to a shorter learning curve while maintaining lower invasiveness.14–19 In addition, several studies have also revealed that it was particularly suitable in cases with severe adhesions, obesity, or other comorbidities, compared with laparoscopic surgery.20–22 To our knowledge, however, very few studies have been conducted to determine the utility of HALDG compared with LADG for gastric cancer.
A previous retrospective study that compared short-term perioperative outcomes of HALDG and LADG in early gastric cancer concluded that HALDG served only as a bridge between open distal gastrectomy and LADG, offering no special advantages for gastric cancer.23 However, the study involved very small sample sizes, prolonged operative time in HALDG, and higher blood loss compared with previous reports. In contrast, a recent prospective study demonstrated that hand-assisted laparoscopic gastrectomy, including HALDG, had a significantly reduced operative time compared with laparoscopy-assisted gastrectomy, with better postoperative outcomes than LADG. Therefore, the study indicated that HALDG was a safe and feasible treatment for gastric cancer.24 However, ∼50% of patients in their study underwent total or proximal gastrectomy, which may have influenced their findings. In our study, we focused on accurately evaluating the clinical features of HALDG, compared with LADG, in addition to discussing the current practical status of HALDG in the treatment of gastric cancer.
In the present study, HALDG demonstrated a considerably reduced operative time compared with LADG. We postulated that a good operative view and the availability of tactile feedback due to the active use of the surgeon’s hand under pneumoperitoneum, in addition to direct manipulation and reconstruction, were factors that contributed to a shorter operative time. Previous studies showed that lymph node dissection around the right gastroepiploic and right gastric vessels had an effect on shorter operative time,24 however, our results suggest that such a dissection is only one of the many factors contributing to the shorter operative time observed in this study. We performed fewer lymph node dissections extracorporeally, all of which were under pneumoperitoneum, while still reducing operative time. In addition, special devices and anastomosis techniques for reconstruction were unnecessary due to the possible use of the same device both for open surgery and HALDG, which seemed to contribute to a reduced learning curve and less surgeon stress. Consequently, they were also considered to result in shorter operative time.
In contrast, blood loss was significantly higher with HALDG than with LADG. The main cause of this could have been direct manipulation through the incision, although the difference of background in both groups may affect the result. The release of pressure during reconstruction may have been associated with the reduction of a hemostatic effect due to pneumoperitoneum, which led to a higher blood loss in HALS. Nevertheless, this difference seemed to have little impact on operative outcomes in clinical practice, as the blood loss in both groups was very low.
Most factors related to clinical invasiveness were comparable in the 2 groups, although the HALDG group required a longer total incision length, in addition to including more patients with complicated combined surgeries. Several studies have shown that HALS has similar invasiveness compared with laparoscopic surgery.15–18 We speculated that the postoperative internal environment in patients who underwent HALDG was similar to that in those who underwent LADG, despite the differences in operative procedure between the 2 groups. There are several possible explanations for the findings. First, the shorter operative time may have offset the influence of said difference. Previous studies have demonstrated that a prolonged operative time affects patients’ overall condition.25 HALS is associated with a shorter operative time, which could have reduced invasiveness. Second, gentle manipulation could have offset the influence of this difference. In particular, this study showed that postoperative ALT and AST levels were significantly lower with HALDG than with LADG. Several authors have investigated possible risk factors for liver damage associated with laparoscopic surgery, including decreased hepatic perfusion from increased abdominal pressure and inadequate positioning of the patient.26,27 In addition, the characteristic cause of liver damage in LADG is considered to be focal hepatic injury caused by liver exclusion, which could lead to a postoperative transient increase in aminotransferases.28 A shorter operative time and gentle exclusion of the liver using the left hand may have been able to prevent such increases in aminotransferases, which probably led to the reduction of operative invasiveness. Third, regarding incision length, the difference between the groups was 15 mm, which was negligible compared with the total invasiveness of distal gastrectomy.
The time to first soft diet and length of postoperative hospital stay were significantly longer in the HALDG group than in the LADG group. However, this study revealed that the postoperative recovery time of the small intestine and CRP levels and other invasiveness-related factors were similar in both groups. Therefore, these findings should be interpreted with caution. The results seemed to be affected not only by the difference of operative procedure between the groups but also by the changing nature of postoperative management in accordance with enhanced recovery after surgery,29 and the Japanese insurance system.
This study demonstrated a considerably reduced operative time in HALDG, and multivariate analysis revealed that HALDG was one of the strong contributing factors for a reduced operative time. Thus, there is the possibility that the selection of HALS could reduce the operative time more effectively compared with other factors, leading to reduced operation-induced disturbance. Consequently, this finding may result in the increased use of minimally invasive surgery for patients in poor general conditions.
This study has several limitations. It was retrospective, had a small sample size, and was not a multicenter study.
In conclusion, HALDG is a limited procedure in gastric cancer treatment, as it is not always superior to LADG with respect to certain operative factors, although it demonstrated a significantly shorter operative time and similar invasiveness to LADG. However, this study suggests that HALDG is a safe and feasible approach and could become an effective option in the treatment of stage I gastric cancer, particularly in the presence of older age, high-risk comorbidity, infeasible prolonged surgery, and liver dysfunction. Randomized controlled trials are required to accurately evaluate the utility of HALDG in gastric cancer treatment.
The authors are grateful to Dr Motoo Yamagata who provided guidance on minimally invasive techniques and to Mark Richley for his helpful discussions about HALDG.
1. Kitano S, Iso Y, Moriyama M, et al. Laparoscopy-assisted Billroth I gastrectomy. Surg Laparosc Endosc. 1994;4:146–148.
2. Kim YW, Baik YH, Yun YH, et al. Improved quality of life outcomes after laparoscopy-assisted distal gastrectomy
for early gastric cancer
: results of a prospective randomized clinical trial. Ann Surg. 2008;248:721–727.
3. Kim W, Kim HH, Han SU, et al. Korean Laparo-endoscopic Gastrointestinal Surgery Study (KLASS) Group. Decreased morbidity of laparoscopic distal gastrectomy
compared with open distal gastrectomy
for stage I gastric cancer
: short-term outcomes from a multicenter randomized controlled trial (KLASS-01). Ann Surg. 2016;263:28–35.
4. Yu J, Huang C, Sun Y, et al. Chinese Laparoscopic Gastrointestinal Surgery Study (CLASS) Group. Effect of laparoscopic vs open distal gastrectomy
on 3-year disease-free survival in patients with locally advanced gastric cancer
: the CLASS-01 Randomized Clinical Trial. JAMA. 2019;321:1983–1992.
5. Cui M, Li Z, Xing J, et al. A prospective randomized clinical trial comparing D2 dissection in laparoscopic and open gastrectomy for gastric cancer
. Med Oncol. 2015;32:241.
6. The Japanese Gastric Cancer
Society. Guidelines for diagnosis and treatment of carcinoma of the stomach; April 2004 edition. Available at: www.jgca.jp/pdf/Guidelines2004_eng.pdf
. Accessed June 19, 2019.
7. Japanese Gastric Cancer
Association. Japanese gastric cancer
treatment guidelines 2010 (ver. 3). Gastric Cancer
8. Japanese Gastric Cancer
Association. Japanese classification of gastric carcinoma: 3rd English edition. Gastric Cancer
9. Kanaya S, Gomi T, Momoi H, et al. Delta-shaped anastomosis in totally laparoscopic Billroth I gastrectomy: new technique of intraabdominal gastroduodenostomy. J Am Coll Surg. 2002;195:284–287.
10. Dindo D, Demartines N, Clavien PA. Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg. 2004;240:205–213.
11. Katai H, Sasako M, Fukuda H, et al. JCOG Gastric Cancer
Surgical Study Group. Safety and feasibility of laparoscopy-assisted distal gastrectomy
with suprapancreatic nodal dissection for clinical stage I gastric cancer
: a multicenter phase II trial (JCOG 0703). Gastric Cancer
12. Benlice C, Costedio M, Stocchi L, et al. Hand-assisted laparoscopic vs open colectomy: an assessment from the American College of Surgeons National Surgical Quality Improvement Program procedure-targeted cohort. Am J Surg. 2016;212:808–813.
13. Park YH, Lee ES, Kim HH, et al. Long-term oncologic outcomes of hand-assisted laparoscopic radical nephrectomy for clinically localized renal cell carcinoma: a multi-institutional comparative study. J Laparoendosc Adv Surg Tech A. 2014;24:556–562.
14. Qian D, He Z, Hua J, et al. Hand-assisted versus conventional laparoscopic splenectomy: a systematic review and meta-analysis. ANZ J Surg. 2014;84:915–920.
15. Marcello PW, Fleshman JW, Milsom JW, et al. Hand-assisted laparoscopic vs laparoscopic colorectal surgery: a multicenter, prospective, randomized trial. Dis Colon Rectum. 2008;51:818–828.
16. Wang G, Zhou J, Sheng W, et al. Hand-assisted laparoscopic surgery
versus laparoscopic right colectomy: a meta-analysis. World J Surg Oncol. 2017;15:215.
17. HALS Study Group. Hand-assisted laparoscopic surgery
vs standard laparoscopic surgery for colorectal disease: a prospective randomized trial. Surg Endosc. 2000;14:896–901.
18. Dols LF, Kok NF, d’Ancona FC, et al. Randomized controlled trial comparing hand-assisted retroperitoneoscopic versus standard laparoscopic donor nephrectomy. Transplantation. 2014;97:161–167.
19. Ozturk E, da Luz Moreira A, Vogel JD. Hand-assisted laparoscopic colectomy: the learning curve is for operative speed, not for quality. Colorectal Dis. 2010;12:304–309.
20. Myers EA, Feingold DL, Arnell TD, et al. The rate for the use of hand-assisted laparoscopic methods is directly proportional to body mass index. Surg Endosc. 2014;28:108–115.
21. Pyo DH, Huh JW, Park YA, et al. A comparison of hand-assisted laparoscopic surgery
and conventional laparoscopic surgery in rectal cancer: a propensity score analysis. Surg Endosc. 2016;30:2449–2456.
22. Heneghan HM, Martin ST, Kiran RP, et al. Laparoscopic colorectal surgery for obese patients: decreased conversions with the hand-assisted technique. J Gastrointest Surg. 2013;17:548–554.
23. Kim YW, Bae JM, Lee JH, et al. The role of hand-assisted laparoscopic distal gastrectomy
for distal gastric cancer
. Surg Endosc. 2005;19:29–33.
24. Gong J, Cao Y, Li Y, et al. Hand-assisted laparoscopic versus laparoscopy-assisted D2 radical gastrectomy: a prospective study. Surg Endosc. 2014;28:2998–3006.
25. Hirvonen EA, Poikolainen EO, Pääkkönen ME, et al. The adverse hemodynamic effects of anesthesia, head-up tilt, and carbon dioxide pneumoperitoneum during laparoscopic cholecystectomy. Surg Endosc. 2000;14:272–277.
26. Andrei VE, Schein M, Margolis M, et al. Liver enzymes are commonly elevated following laparoscopic cholecystectomy: is elevated intra-abdominal pressure the cause? Dig Surg. 1998;15:256–259.
27. Nguyen NT, Braley S, Fleming NW, et al. Comparison of postoperative hepatic function after laparoscopic versus open gastric bypass. Am J Surg. 2003;186:40–44.
28. Shinohara T, Kanaya S, Yoshimura F, et al. A protective technique for retraction of the liver during laparoscopic gastrectomy for gastric adenocarcinoma: using a Penrose drain. J Gastrointest Surg. 2011;15:1043–1048.
29. Varadhan KK, Neal KR, Dejong CH, et al. The enhanced recovery after surgery (ERAS) pathway for patients undergoing major elective open colorectal surgery: a meta-analysis of randomized controlled trials. Clin Nutr. 2010;29:434–440.