From POEM to POET: Applications and perspectives for submucosal tunnel endoscopy

• Background and concept of submucosal endoscopy
• Clinical evidence for POEM: what is still lacking?
• Submucosal tunneling beyond POEM
• Submucosal transgastric endoscopic peritoneoscopy (STEP)
• Gastric peroral endoscopic pyloromyotomy (G-POEM)
• Peroral endoscopic resection of submucosal tumors
• Tunneling for endoscopic submucosal dissection (ESD)
• Submucosal endoscopy – what can we do in the future?
• Summary
• References

Recent advances in submucosal endoscopy have unlocked a new horizon for potential development in diagnostic and therapeutic endoscopy. Increasing evidence has demonstrated that peroral endoscopic myotomy (POEM) is not only clinically feasible and safe, but also has excellent results in symptomatic relief of achalasia. The success of submucosal endoscopy in performance of tumor resection has confirmed the potential of this new area in diagnostic and therapeutic endoscopy. This article reviews the current applications and evidence, from POEM to peroral endoscopic tunnel resection (POET), while exploring the possible future clinical applications in this field.

Background and concept of submucosal endoscopy

Over the past decades, endoscopy has emerged from being a diagnostic tool into a therapeutic platform. Endoscopic resection for early gastrointestinal (GI) neoplasia began with the development of the first polypectomy snare in 1969 by Dr. Shinya [1], progressing subsequently to endoscopic mucosal resection (EMR) [2] using a variety of techniques [3], and finally to endoscopic submucosal dissection (ESD) to achieve en bloc resection for larger lesions. A new set of devices and enhanced electrosurgical units allowed endoscopists to perform ESD with secure hemostasis as well as closure of perforations [4]. Advances in endoluminal resection unleash the potential of advanced endoscopic surgical procedures, suturing, and device development [5] [6] [7] [8].

In addition, technical advances in endoscopy were inspired by the concept of natural orifice transluminal endoscopic surgery (NOTES), first proposed for transgastric peritoneoscopy in 2004 [9]. One of the important barriers to NOTES was the safety of the access to the peritoneal cavity and, even more so, the closure of that access [10]. In an animal model Sumiyama et al. explored the performance of a stepwise submucosal tunnel as a safe access to the peritoneal cavity [11] avoiding full-thickness incision and closure at a single site. Pasricha et al. took this idea further to carry out the first successful submucosal endoscopic myotomy in pigs [12]. Inoue et al. performed the world’s first clinical peroral endoscopic myotomy (POEM) for treatment of achalasia, and reported the first case series of 17 patients [13]: all patients had significant improvement in dysphagia score and lower esophageal sphincter pressure after POEM.

Following this initial description, there was an explosion of reports of small case series with short-term follow-up and encouraging clinical outcomes. In this early phase of a new technique, meta-analyses have already been conducted, even without randomized trials. The six systematic reviews and meta-analyses, which should rather be considered to be reviews, are shown in [Table 1] and [Table 2] [14] [15] [16] [17] [18] [19]. Three of them compared data between POEM and laparoscopic myotomy ([Table 2]) and, interestingly, two reviews on the same topic from two different groups of authors were published in two consecutive issues of the same journal [17] [18]. A seventh review deals with the few studies in children [20]. Despite similar search periods, the abovementioned reviews covered different papers/abstracts from different sources and generally reported a very high clinical efficacy with mostly short-term follow-up (6 – 8 months). The complication rates are highly variable since a uniform definition of complications, especially for minor complications, is still lacking. Another difficulty in interpretation of the clinical results is that some groups have reported results with increasing case numbers in several subsequent publications, so the overlap between the results is not always clear. A similar phenomenon can be observed for retrospective analyses and meta-analyses comparing POEM versus laparoscopic Heller myotomy (LHM) [18] [19] [21] [22] [23] [24] [25] [26]. The results of those studies suggested equivalent results for POEM and LHM, and are certainly interesting, but should mostly be considered as hypothesis-generating for better planning of randomized trials.

Clinical evidence for POEM: what is still lacking?

Mostly small cohort studies, on more than 4000 patients in total worldwide, confirmed the short-term clinical efficacy and relative safety of POEM for treatment of achalasia and other esophageal motility disorders. The incidence of severe adverse events during or after POEM remained uncommon, and POEM has been increasingly accepted as a noninvasive treatment for achalasia. Nevertheless, uniform definitions of minor or serious adverse events relating to POEM are urgently needed and should be used in further studies; for example, cutaneous emphysema and free abdominal air as sequelae or complications need to be defined.

The advantage of POEM is the achievement of myotomy similarly to that of a surgical approach but without incision; however long-term results are available from only very few studies. The clinical efficacy of POEM has remained excellent in studies from Asia [27] [28] [29], but a Western multicenter series suggested some loss of efficacy over time [30]. There is a need for more focus on reporting mid- to long-term results of 2 years and longer.

Gastroesophageal reflux disease (GERD) is another concern, currently overshadowed by optimistic assumptions that POEM might have reflux rates similar to those of laparoscopic myotomy. Again, reflux rates in East Asia are much lower than those reported from Western centers. In one of the reviews cited above, the overall rate of GERD and/or reflux esophagitis was 10.9 %, while studies from Western societies reported much higher rates of GERD ranging from 33 % to 72.2 % [15]. Most of the patients could obviously be managed by proton pump inhibitors (PPIs) in the short term. In another review, the rate of GERD was 8.5 %, and 13 % of patients had esophagitis while 47 % had abnormal acid exposure found in 24-hour pH studies [16]. Again, reports from Asia demonstrated a low rate of esophagitis while the rate apparently increased with increasing myotomy length and duration of the procedure. Another comparative study in 66 patients with achalasia demonstrated that POEM achieved similar GERD-related quality of life outcomes compared to LHM with fundoplication [21].

The next important issue concerns technical refinements of POEM for safe practice and long-term outcomes especially with respect to the development of GERD. Inoue et al. began performance of POEM using an anterior approach and a long myotomy at the 1-o’clock position [13]. The aim of using the anterior approach is to avoid damage to the angle of His and the sling muscle fibres located over the fundus at the greater curvature, which are important natural antireflux mechanisms. Zhou et al. reported the techniques of posterior myotomy, where the mucosal incision and the development of the submucosal tunnel is begun at the 5 – to 6-o’clock position [7]. The posterior approach allowed better alignment of the knife for performing myotomy, as the working channel for most endoscopes is located over the 5 – or 7-o’clock position. However, the angle of His is located at around the 8-o’clock position and posterior POEM may theoretically risk damage to the angle of His and disruption of the natural antireflux mechanism. Randomized trials comparing anterior versus posterior POEM will be necessary to assess their technical advantages and the incidence of GERD. Given that differences are expected to be minor, these studies will probably need large sample sizes.

Finally, the clinical efficacy of POEM versus its alternatives, mainly endoscopic pneumatic dilation and LHM should be compared in well-designed prospective randomized trials. The latter two therapies remain as well-established conventional treatments for achalasia [18] [31]. A search in clinicaltrial.gov using keywords “peroral endoscopic myotomy” or “achalasia” generated a list of 69 registered clinical trials. Eight of these study protocols focused on comparisons between POEM and other treatment modalities, including endoscopic botox injection, endoscopic pneumatic dilatation, and LHM; an overview is shown in [Table 3]. In addition, a multicenter prospective randomized trial comparing pneumatic dilation POEM was identified in the Netherlands trial registry (NTR3593); this is targeted to close by 2017.

Submucosal tunneling beyond POEM

Submucosal transgastric endoscopic peritoneoscopy (STEP)

The submucosal tunneling technique was first conceptualized as a means of gaining safe access to the peritoneal cavity using flexible endoscopy [11]. Liu et al. reviewed publications on clinical applications of NOTES and found a total of 11 clinical studies reporting transgastric peritoneoscopy in 103 patients [32]. The indications included staging peritoneoscopy for carcinoma of pancreas or stomach and for those undergoing surgery for morbid obesity. After peritoneoscopy, most of the gastrotomies were either included in the surgical procedure or used for performance of gastrojejunostomy to avoid leakage. Lee et al. performed transgastric peritoneoscopy in five patients through submucosal tunneling [33]. All the submucosal transgastric endoscopic peritoneoscopies (STEPs) were technically successful with a mean hospital stay of 3.8 days.

It has to be said however, that, in contrast to POEM, this technique has not gained widespread acceptance. Furthermore, the indications for STEP are limited as advances in preoperative imaging allow accurate staging for intra-abdominal cancers.

Gastric peroral endoscopic pyloromyotomy (G-POEM)

Gastroparesis can cause debilitating symptoms of delayed gastric emptying including repeated nausea and vomiting [34]. Common causes of gastroparesis include diabetes mellitus, surgical or iatrogenic vagotomy, and an idiopathic pathogenesis. One of the hypothesized mechanisms for development of gastroparesis is the incoordination of peristalsis and relaxation of the pyloric antrum due to degeneration of myenteric plexus and loss of interstitial cells of Cajal [35]. The endoscopic injection of botulinum toxin was aimed at reducing the release of acetylcholine from cholinergic nerves and relaxing the pyloric sphincter [36]. Although prospective cohort studies demonstrated symptomatic improvements after endoscopic botox injection, two randomized controlled studies showed no improvement in symptoms and gastric emptying when endoscopic botox injection was compared with placebo [37] [38]. Laparoscopic pyloroplasty represented another approach to disrupting the pyloric constriction and relieving the obstruction, a concept similar to botox injection and pyloric stenting [39], but no evidence is available that compares this to other therapies.

Recently, the idea of POEM has been extended to performance of myotomy at the pylorus, with development of the gastric peroral endoscopic pyloromyotomy (G-POEM) [40] [41] [42]. Technically, the principles of G-POEM are similar to those of POEM, including creation of a submucosal tunnel, endoscopic myotomy, and closure of the mucosal entrance. The myotomy focused on inner circular and oblique muscle layers with sparing of the outer longitudinal layer, thus avoiding outer important structures including major vessels.

Early results from case reports and series demonstrated the technical success of G-POEM. Among the seven cases reported by Shlomovitz et al., one patient had difficulty in swallowing after peroral endoscopic pyloromyotomy and another patient had upper GI bleeding. Six of the seven patients had significant symptomatic improvement, while normal gastric emptying was observed in 80 % of cases [42]. Further clinical studies and long-term reports are necessary to confirm the efficacy and safety of G-POEM for treatment of gastroparesis.

Peroral endoscopic resection of submucosal tumors

Submucosal tunnel endoscopic resection (STER) or peroral endoscopic tunnel resection (POET) represents a novel approach to treatment of subepithelial tumors of the GI tract ([Fig. 1]). Subepithelial tumors of the GI tract comprise various pathologies arising from subepithelial tissues; the commonest types include gastrointestinal stromal tumors (GISTs), leiomyomas, schwannomas, lipomas, and ectopic pancreas. However, the real incidence of the various pathologies in esophagus, stomach, and duodenum is not fully known, especially for smaller lesions (< 2 or 3 cm), since surgical series include some referral bias towards more serious pathology and follow-up studies often lack tissue confirmation.

Many studies have covered endoscopic resection of subepithelial tumors of the upper GI tract using a variety of techniques; the issue of ESD for resection of subepithelial tumors [43] [44] [45] [46] [47] [48] will not be covered in detail here, since it represents a different principle and the risk of perforation amounted to 15 %. Technically, the risk of perforation during ESD will be determined by the extent of involvement in the muscular layer by the subepithelial tumor. By creation of a submucosal tunnel while maintaining the integrity of the overlying mucosa, endoscopic resection of submucosal tumors is possible without full-thickness perforation. Nine prospective studies have reported the performance of STER or POET for treatment of subepithelial tumors located in the esophagus or gastroesophageal junction, or, in some studies, also in the stomach [49] [50] [51] [52] [53] [54] [55] [56] [57] ([Table 4]). In most cases the pathology was leiomyoma or GIST of the upper gastrointestinal tract, and the most commonly reported complications included gas-related emphysema, pneumoperitoneum, and bleeding. The technique of STER/POET is still evolving, while the indications for applying such procedures for treatment of subepithelial tumors remain controversial [58] [59]. As there is a size limitation for tumors that can be removed perorally, tumors larger than 40 mm are generally not indicated for submucosal tunnel resection. Meanwhile, the risk of malignancy for submucosal tumors less than 20 mm in size is small and probably endoscopic/EUS surveillance should be recommended. Refinement in POET techniques and larger prospective cohort studies with longer-term follow-up should be conducted to confirm safety and oncological outcomes as well as the overall requirement for invasive treatment of these submucosal tumors.

Tunneling for endoscopic submucosal dissection (ESD)

The principle of tunneling has also been advocated for ESD especially of larger lesions in the esophagus [60] [61] [62] [63]. The technical advances in tunneling could be adopted, and make ESD resection easier, quicker, and perhaps safer. The impact of submucosal tunneling with regard to clinical outcomes and learning curve of ESD should be investigated in prospective randomized studies.

Submucosal endoscopy – what can we do in the future?

Based on prior NOTES experience, submucosal tunneling allowed endoscopists to access a completely new area of the GI tract beyond the mucosa. The tissues within reach of the submucosal tunnel include muscularis propria, submucosal (Meissner) nerve plexus, myenteric (Auerbach) nerve plexus, and other mesenchymal tissues. Diagnosis of submucosal diseases – if clinically indicated – can be greatly enhanced by endoscopic examination through the tunnel, as direct inspection of the disease pathology is possible ([Table 5]). Sumiyama et al. reported the observation of myenteric plexus using confocal endomicroscopy in colonic submucosa after ESD with application of acriflavine over the resected area [64], which is an interesting experimental approach. The direct examination of neurons and nerve plexus can be done through endomicroscopy for diagnosis of functional GI disorders especially when targeted probes are employed to enhance endoscopic molecular imaging [65] [66]. Sato et al. recently reported the diagnosis of eosinophilic esophageal myositis which caused the development of nutcracker and jackhammer esophagus [67]. Upon POEM, a biopsy of esophageal muscularis propria demonstrated eosinophilic infiltration. The observation of the eosinophilic infiltration was possible through the application of endomicroscopy in submucosal endoscopy. However, clinical utility has to be weighed against this approach which is rather aggressive compared to endoscopic biopsy and EUS-FNA.

Submucosal tunneling allows direct endoscopic examination of mediastinum and the peritoneal cavity, similarly to mediastinoscopy and diagnostic laparoscopy, as shown mostly in animals [68] [69]. However, appropriate clinical application will not be commensurate with the technological feasibility. The indications for mediastinoscopy are declining with advances in endobronchial ultrasound and transbronchial needle aspiration for nodal sampling [70]. Pulmonary biopsy would be another potential application through a transesophageal submucosal tunneling endoscopy [71]. Staging laparoscopy is regarded as one of the essential procedures for detection of peritoneal metastasis for carcinoma of stomach and pancreas, by some, but not all groups [72]. Kikuchi et al. reported that the diagnostic accuracy for peritoneal metastasis was significantly higher (83.8 % vs. 62.2 %) with laparoscopic narrow band imaging (NBI) compared with conventional laparoscopic white-light imaging [72], which implied that endoscopic NBI could achieve similar results without surgical incision.

Laparoscopic adjustable gastric banding for treatment of morbid obesity can sometimes lead to development of esophageal outflow obstruction mimicking achalasia, especially when band slippage occurs [73]. POEM has served as an alternative approach to relieve the high pressure at the lower esophageal sphincter without need for re-operation. Myotomy is one of the treatments for spastic disorders of the GI tract. Extension of this innovative submucosal approach can be considered beyond the upper GI tract. Bapaye et al. reported the first successful performance of per-rectal endoscopic myotomy (PREM) for treatment of a 24-year-old patient with Hirschsprung’s disease [74]. Future larger-scale clinical studies should evaluate this technique for treatment of Hirschsprung’s disease as well as for hypertensive anal sphincter and sphincter dyssynergia leading to chronic constipation and anal fissure [75] ([Table 5]). If myotomy can be performed for muscularis propria through submucosal endoscopy, treatment for damaged muscularis propria through submucosal endoscopy will be another future possibility. The extent to which submucosal endoscopy can be involved in antireflux treatment is yet to be defined. Submucosal injection of collagen at the lower esophageal sphincter has been described previously for treatment of GERD in 10 patients [76]. With regard to electrical stimulation of the lower esophageal sphincter [77], following miniaturization of the device and electrodes, endoscopic implantation may become possible through the submucosal tunneling approach.

Summary

Submucosal endoscopy represents a new horizon for innovative development in endoscopic diagnosis and treatment. This has led to a paradigm shift and offers a new working space for endoscopists to perform diagnostic and therapeutic procedures, for diseases within and outside the GI tract. However, the quality of clinical research is still limited, and we must await the results of ongoing randomized trials. Future research will focus on comparing the short- and long-term efficacy of POEM with that of other standard treatments for achalasia, on refining the techniques of POEM, and finally on extending the horizon of submucosal endoscopy to tumor resection and beyond.

Competing interests: None

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Corresponding author

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