Esophageal SMT is a rare disease with a low incidence in clinical practice. Leiomyoma is the most common pathological type, accounting for 70–80% of benign esophageal tumors. The middle and lower esophagus are the primary sites, which may be related to the muscle composition of these areas of the esophagus [11, 12]. GIST is another type of esophageal SMT, with an incidence of < 5%. GISTs are believed to arise from the interstitial cells of Cajal [13]. Other rare types include granular cell tumors and lipomas. Although most esophageal SMTs are benign, GISTs tend to become malignant, and patients with tumors > 5 cm may develop clinical symptoms such as dysphagia or substernal pain owing to tumor location and size, thus affecting quality of life. Therefore, timely and complete tumor resection is essential.
Surgery has long been considered the standard of care for gastrointestinal SMTs; however, it is invasive and associated with many complications. With the continuous improvement of endoscopic techniques, ESD has gradually been used to treat SMTs of the esophagus and cardia. Studies have confirmed that ESD is minimally traumatic and associated with lower complication rates. ESD also has a shorter operation time, making it a preferable treatment option. However, for SMTs derived from the MP, the complete resection rate of ESD is relatively low. Bialek et al. [5] reported that the complete resection rate of SMTs originating from the MP using ESD was only 68.2%. Lee et al. [6] confirmed that the complete resection rate of ESD was 75%. Chinese professors have proposed ESE, EFTR, and other procedures related to ESD that are widely used to treat upper gastrointestinal SMTs. Studies have shown that the complete resection rate of ESE has significantly improved, exceeding 90%; however, the rates of bleeding and perforation are also relatively high. Liu et al. [14] reported that the complete resection rate of ESE was 96.8%; however, the perforation rate reached 12.9%. Ye et al. [7] demonstrated that the complete resection rate of ESE was 95.6%, whereas the perforation rate was 8.9%. EFTR is safe and effective for the treatment of gastric SMTs, and studies have proven that its complete resection rate can reach up to 87.5–100% [15, 16], making it suitable for gastrointestinal SMTs arising from the deep MP and growing into the lumen. Although the technique has been proven safe and effective for gastric lesions, the esophageal wall is thinner than the stomach wall and has only an outer membrane (i.e. it lacks a serous membrane), which may lead to serious complications such as perforation, secondary intra-abdominal infection, and gastrointestinal fistula formation. Therefore, its application in esophageal SMTs is relatively limited.
Xu et al. first reported the use of STER, which is based on ESD and POEM, for the treatment of upper gastrointestinal SMTs. In 2012, our center also successfully applied this technique to treat upper gastrointestinal SMTs [17]. Subsequently, many researchers in China and other countries have attempted to apply STER for the resection of esophageal SMTs. Ye et al. [18] conducted a prospective study in 85 patients with SMTs originating from the upper gastrointestinal MP treated with STER, confirming its safety and efficacy. Wang et al. [19] reported the successful resection of SMTs originating from the upper gastrointestinal MP in 83 patients with STER, verifying its safety, feasibility, and efficacy. In 2018, we also retrospectively analyzed 128 cases of esophageal SMTs treated with STER at 4 centers and demonstrated the safety and efficacy of STER for esophageal SMTs [20].
Many studies have shown that STER is a safe and effective treatment for the resection of esophageal SMTs; however, we found over the course of the study that for some special esophageal SMTs, such as those located in the upper esophagus or cardia or those > 3.5 cm in size, due to the limited space in the tunnel and the operative difficulty, the operation time would be longer and the complication rates of STER would greatly increase. In 2015, Jun et al. [21] first reported successful opening of the mucosa on the distal end of the tunnel during STER to resect a 40-mm esophageal SMT. In 2017, Zhang et al. [22] reported 10 cases of SMTs near the cardia that were successfully resected using submucosal tunneling endoscopic resection with double opening (DO-STER), which demonstrated that DO-STER is safe and effective for removing SMTs located within the cardia. Therefore, we made technical improvements to STER and named the new technique O-STER. By constructing a second tunnel opening, the pressure inside the tunnel is reduced, the operating space in the tunnel is increased, and the field of view of marginal tumor dissection is improved, making the resection of the aforementioned types of SMTs safer and more convenient.
The key to the STER technique is the successful construction of a submucosal tunnel. The operating space within the tunnel greatly affects its successful dissociation and reduces the occurrence of complications. However, the upper esophagus and the cardia are two special locations that are associated with increased STER difficulty. For SMTs located in the upper esophagus, tunnel construction is difficult due to the short distance from the esophageal entrance. An insufficient tunnel length results in insufficient operating space within the tunnel, making SMT dissection more difficult. SMTs in the cardia border the stomach, resulting in insufficient tunnel space. In addition, a limited field of view at the junction increases the occurrence of complications. Therefore, for the dissection of SMTs in such cases, increasing the operating space and expanding the field of view are essential. The O-STER procedure allows for expansion of the operating space and field of view of the tunnel via the distal end opening of the tunnel, making SMT resection easier and reducing the duration of operation and risk of complications. In this study, 2 (9.5%) tumors were in the upper esophagus versus 14 (66.7%) in the cardia. They were all completely resected during uneventful operations without complications. No residual tumor or recurrence was noted during the follow-up period.
The appropriate SMT size for removal by STER is controversial. Most professors believe that STER is suitable for the resection of SMTs ≤ 3.5 cm; however, some studies suggest that STER can also be effective for the resection of SMTs > 3.5 cm. Ye et al. [18] reported that STER is an effective and safe treatment for upper gastrointestinal SMTs ≤ 3 cm; however, they stated that the operation is too challenging for SMTs > 3 cm. Wang et al. [19] believed that STER is safe and effective for SMTs > 3.5 cm. The Chinese consensus on SMT diagnosis and management in 2018 [23] proposed that STER could be used to remove SMTs ≤ 5 cm. In previous studies, we also confirmed that STER is safe and effective for resecting SMTs ≤ 5 cm. We also found that using STER to resect esophageal SMTs ≤ 3.5 cm is easier and requires a short operation time; conversely, for the resection of SMTs > 3.5 cm, insufficient operating space in the tunnel increases the operative difficulty, the operation duration, and complication rates and obviously reduces the complete resection rate.
Li et al. [24] used STER procedures to resect 47 SMTs at the gastroesophageal junction, among which complete resection was achieved in only 35 cases (74.5%) and the complication rate reached 8.6%. They found that tumor diameter ≥ 2 cm and irregular shape were the main factors responsible for STER failure. Du et al. [25] used STER for 89 cases of esophageal SMTs and found that the complete resection rate was only 78.7% and the complication rate reached 21.3%. They confirmed that SMT size is a key factor in the piecemeal resection of STER procedures and that the resection of SMTs > 3.5 cm is very difficult. Song et al. [26] performed STER in 10 cases of SMTs > 3.5 cm and demonstrated a mean operation duration of 156 (range 60–320) minutes and a complete resection rate of only 80% and perforation rate of 10%, thus confirming that STER is difficult for SMTs > 3.5 cm. Chen et al. [27] also confirmed that a transverse diameter > 3.5 cm was a significant risk factor for segmental resection of STER, the occurrence of complications, and technical difficulty. In the present study, 16 (76.2%) of the enrolled patients had SMTs > 3.5 cm; all were successfully resected by O-STER. The operation time was significantly shorter and there were no serious complications, indicating that O-STER may be a safer and more effective treatment for SMTs > 3.5 cm.
In this study, 21 lesions were successfully resected by O-STER. The mean operation duration was 56.7 minutes, which is consistent with that reported for STER (40–78.3 minutes). All SMTs were preoperatively evaluated by endoscopic ultrasonography. Although common endoscopy can provide a preliminary understanding of lesion size and morphology, the diagnostic sensitivity and specificity for SMTs are only 87% and 29%, respectively [28]. Endoscopic ultrasonography is the most accurate endoscopic method for evaluating SMTs in the gastrointestinal tract, which can evaluate SMT size, origin, growth pattern, and internal properties. In the present study, the en bloc and complete resection rates were both 100% and there was only 1 (4.8%) case of subcutaneous emphysema during the operation; no complications occurred postoperatively. According to the literature, the complete resection rate of SMTs by STER can reach 80–100%; however, the perforation rate is 3–10%, and the gas-related complication rate is 2.4–12.1% [25, 26, 29, 30]. The resection and complication rates of O-STER were similar to those of STER. Postoperative pathological findings showed that most SMTs were classified as leiomyomas (85.7%) and only 3 cases were classified as GISTs; however, all were considered low or very low risk. All specimens had negative vertical and horizontal margins. During the mean follow-up period of 26.7 months, no residue, recurrence, metastasis, or other serious complications were observed.
In summary, the O-STER technique has the following advantages: (1) reduces pressure inside the tunnel, increasing the operating space, especially for SMTs > 3.5 cm, and shortening the operation time; (2) allows a good field of view for SMTs located in the upper esophagus and cardia through opening of the distal tunnel and expanding of the tunnel space; (3) increases the space inside the tunnel owing to a second tunnel opening, thereby reducing the operation-related difficulty, rates of bleeding and perforation in the tunnel, operation time, and complication rates.