The current study was undertaken to investigate the efficacy of the S–O clip for gastric ESD. The results showed that the S–O clip was significantly associated with shorter procedure time and faster dissection speed, while there were no significant differences in en bloc resection rate, complete resection rate, post-ESD bleeding rate or perforation rate.
The traction methods are classified as the external forceps method, double scope method, clip-and-snare method, internal traction method, and clip-with-line method . However, these methods except for the clip-with-line method are not widely used due to limitations. The external forceps method  is difficult to use in cardia and the lesser curvature of upper gastric body. The double scope method  requires two endoscopists. The clip-and-snare method  has relatively strong interference with endoscope and traction direction is limited to the two ways. The internal traction method [21,22,23],SLC-ESD is classified in this category, has a relatively complicated procedure; thus, its use is not standardized in gastric ESD.
The clip-with-line method was reported in 2002 and one of the most popular traction methods in gastric ESD [24,25,26,27]. However, a recent multicenter randomized controlled trial reported that the clip-with-line method using a dental floss clip did not reduce the gastric ESD procedure time compared with conventional gastric ESD . This is probably because traction direction of the clip-with-line method is limited to the oral side via cardia of stomach. Traction toward the oral side cannot provide countertraction when submucosal dissection is performed in the retroflexed endoscopic position, although gastric ESD is frequently performed in the retroflexed endoscopic position. In this situation, traction toward the anal side can provide countertraction. Simultaneously, it is also important that traction direction becomes near-vertical against muscle layer, because it helps to open the cutting edge and provide proper visualization of submucosa.
In contrast, the S–O clip can provide traction in any direction both in the forward and retroflexed endoscopic positions; therefore, the S–O clip may be useful anywhere in the stomach. Indeed, in the subgroup analysis, the procedure time of the SLC-ESD group at the upper- or middle-third of the stomach was significantly shorter than that in the C-ESD group. The reason why the procedure time of the SLC-ESD group at the lower-third of the stomach was not significantly shorter than that in the C-ESD group is that performing the ESD procedure on the lower-third of the stomach is generally easier than performing that on the upper- or middle-third of the stomach; moreover, it was difficult to make a statistical difference. The procedure time of the SLC-ESD group was not significantly shorter in lesions located at the greater curvature, although there is a tendency of shorter procedure time in the SLC-ESD group. This result is considered to be due to the insufficient number of cases.
According to the subgroup analysis between procedure time and lesion size, for lesions ≤ 20 mm in size, the median procedure time was shorter in the SLC-ESD group than in the C-ESD group. In contrast, for lesions > 20 mm, there were no significant differences between the groups. This result suggests that the efficacy of SLC-ESD depends on the size of the lesion. In SLC-ESD, as the submucosal dissection advances, the distance between the S–O clip attachment site and the anchor site decreases, the spring shrinks, and the traction force gradually weakens. If the lesion is small, submucosal dissection will be completed before the traction force becomes insufficient. In contrast, if the size of the lesion is large, the traction force weakens in the second half of the submucosal dissection, resulting in less benefit for SLC-ESD compared with C-ESD. Therefore, if the lesion size is large (e.g., > 20 mm), operators should consider selecting an anchor site that is relatively far from the S–O clip attachment position or adding a second S–O clip on the way to submucosal dissection to strengthen the traction force.
For lesions that develop in anatomically narrow areas, such as those near the esophagogastric junction or pyloric ring, it is sometimes difficult to achieve both the traction toward the ideal direction and the appropriate distance between the S–O clip attachment position and the anchor site. Moreover, it is relatively difficult to guide the loop of S–O clip to the anchor site using the regular clip because of the narrow working space. In such lesions, we preferentially selected the anchor site where a certain distance between the S–O clip attachment position and the anchor site could be obtained, and the loop of S–O clip could be easily guided to the anchor site. With this procedure, the direction of the traction may slightly deviate from the ideal direction, or the strength of the traction may be slightly weakened; however, this is not a serious problem in most cases. Although it is necessary to be familiar with SLC-ESD, at present, we believe that SLC-ESD can be selected and used in all the parts of the stomach.
One SLC-ESD procedure needs one S–O clip and one regular clip as an anchor clip, which costs ¥5000 and ¥750 ($50 and $7.5, if the exchange rate is ¥100 = $1), respectively. In this study, the median procedure time was 40 min in the SLC-ESD group and 69 min in the C-ESD group, demonstrating approximately 40% reduction of median procedure time in SLC-ESD group. The S–O clip may provide an advantage in terms of cost, although the method of calculating medical costs is different in each country. Although SLC-ESD can be effective for lesions irrespective of their size and location, in consideration of cost and the results of subgroup analysis, SLC-ESD is recommended especially for the lesions that are ≤ 20 mm in size and located at the upper- and middle-third of the stomach.
It is important to prevent interference between the endoscope and traction device, because interference causes strong traction, resulting in traction device slip-off, damage to the specimen and elevation of muscle layer. In the clip-with-line method or clip-and-snare method, interference caused by the friction between the endoscope and traction device in the cardia cannot be eliminated. In SLC-ESD, interference rarely occurs in the forward endoscopic position, while interference in the retroflexed endoscopic position can be eliminated by devising an attachment procedure as stated in materials and methods section. Indeed, the S–O clip slip-off rate was 3.9%, occurring in only two cases in the SLC-ESD group. The clip slip-off rate of the clip-with-line method was reported to be 13.2% ; therefore, the S–O clip slip-off rate was relatively lower and permissible. The S–O clip reattachment was required in nine patients in the SLC-ESD group, as mentioned the results section, primarily to add traction force. The frequency of reattachments appears to be relatively high; however, this number may decrease as operators become more familiar with SLC-ESD.
Generally, the forward endoscopic position is non-preferred for the upper- or middle-third of stomach during C-ESD, because it is difficult to turn over the mucosal flap owing to the movement of the lesion caused by the patient’s respiration. However, in subgroup analysis, the forward endoscopic position selected rate for the lesion located at the upper-third of stomach was significantly higher in the SLC-ESD group than in the C-ESD group. The forward endoscopic position selected rate for the lesion at middle-third of stomach also tended to be higher in the SLC-ESD group than in the C-ESD group, although there was no significant difference. These results suggest that the S–O clip makes it easy to perform submucosal dissection for the lesion located at the upper- or middle-third of the stomach even in the forward endoscopic position, while it helps in turning over the mucosal flap. Moreover, interference between the endoscope and the spring rarely occurs in the forward endoscopic position during SLC-ESD. Therefore, the forward endoscopic position should be the first choice in SLC-ESD.
To the best of our knowledge, there is an only one retrospective cohort study about SLC-ESD using the S–O clip for gastric neoplasms . However, the use of S–O clip in the retroflexed endoscopic position that is frequently selected in gastric ESD and the S–O clip attachment method were not standardized. Our study demonstrated that using S–O clip both in the forward and retroflexed endoscopic positions could be standardized, and the mean S–O clip attachment time was as short as 2.08 min. In contrast, a previous study has reported that the mean S–O clip attachment time required was as long as 4.4 min. This was probably because the modified S–O clip attachment method  in which the loop came over the mucosa made it easy to hook the loop by the anchor clip; however, the loop came under the mucosa in the conventional attachment method . There were no significant differences in mean S–O clip attachment time between the first half and the second half of SLC-ESD group. This result suggests that the modified S–O clip attachment method may be used without serious difficulties from the beginning of introduction by endoscopists who are accustomed to using hemoclips.
The management of anchor clip after SLC-ESD in the stomach is not standardized. In a previous report, the loop of the S–O clip was cut to detach the resected specimen from the stomach . However, in this procedure, there is a possibility that the anchor clip permanently remains on the gastric wall. The natural drop of the anchor clip from gastric wall could not be expected because vermiculation of stomach is poor except in the pars pylorica. The clamping ring of the anchor clip can be loosened using forceps to detach the anchor clip; however, it is time-consuming and not always successful. In this study, we attempted to detach the anchor clip from the gastric wall with forceps in all SLC-ESD cases, followed by extraction of the resected specimen with the S–O clip and anchor clip. The successful removal rate of the anchor clip was 92.2%, and there were no adverse events due to removal of anchor clip. In all failed removal cases, detaching the anchor clip was attempted more than one month after ESD. This failure probably resulted from submucosal fibrosis around the remaining anchor clip; therefore, it was considered better to remove the anchor clip immediately after ESD on the same day.
The current study has several limitations. First, this was a retrospective study with a limited number of patients. Second, propensity score matching analysis can decrease bias in causal estimates owing to observed differences between groups but are still subject to biases owing to unobserved differences. A randomized controlled trial is needed to evaluate the efficacy of the S–O clip for gastric ESD.
In conclusion, the S–O clip shortened the gastric ESD procedure time, allowing countertraction both in the forward and retroflexed endoscopic positions. Moreover, devising the usage of S–O clip could eliminate the interference between the endoscope and the spring of S–O clip, simplifying the attachment procedure. Therefore, the S–O clip has the potential to be the best traction device for gastric ESD.