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Original Articles: Gastroenterology

Endoscopic resection of early squamous neoplasia of the oesophagus: long-term follow-up in a UK population from a tertiary hospital

Kuan, Jen Yeea; Baskind, Sameulb; Kim, Yesona; McGrath, Stephenc; Chaparala, Ramakrishnad; Assadsangabi, Arashb; Prasad, Neerajb; Regi, Georgee; Ang, Yengb,,f

Author Information
European Journal of Gastroenterology & Hepatology: July 2020 - Volume 32 - Issue 7 - p 789-796
doi: 10.1097/MEG.0000000000001692
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Abstract

Introduction

Endoscopic resection is a minimally invasive technique that has been steadily gaining acceptance worldwide as a promising treatment for early-stage oesophageal squamous cell carcinoma (OSCC) [1–6]. Endoscopic resection can be classified into piecemeal [endoscopic piecemeal mucosal resection (EpMR)] and en-bloc resections. En-bloc resections can be further subdivided into endoscopic mucosal resection (EMR), endoscopic submucosal dissection (ESD) and hybrid ESD. According to the European Society of Gastrointestinal Endoscopy (ESGE) guideline, the main criterion for endoscopic resection selection is the size of the tumour [7]. Additionally, it is recommended to be the primary treatment option for patients who are deemed to have increased risk for surgery [8]. The management of early-stage OSCC is highly dependent on two factors: the risk of lymph node metastases (>10% when lesion involves deeper than T1M2) versus the significant risks of morbidity and mortality associated with oesophagectomy [1,3,7–9]. Endoscopic resection shows a similar oncologic success rate as oesophagectomy with the additional benefits of being less invasive, less costly and has shorter operation times and hospital stays [2,6,9,10,11]. Endoscopic resection has the potential to be a better treatment for early-stage OSCC due to its safety profile and comparable curative outcomes to surgery [9].

Endoscopic resection has been reported to be superior to endoscopic ultrasound (EUS) and endoscopic biopsy at detecting the presence of submucosal invasion and the metastatic potential of oesophageal squamous neoplasia [7,12,13]. Previous studies have reported that endoscopic resection specimens changed the diagnostic grade in 20–40% of lesions [7,13–15]. This can help guide subsequent management decisions and therapeutic strategies by avoiding under or over treatment [13,14].

Research evidence for the efficacy of endoscopic resection is predominantly sourced from Japan where it is well established for the treatment of early-stage OSCC [7]. However, the epidemiology of oesophageal cancer in Japan is different from the UK, and the undertaking of robust endoscopic resection studies is lacking in the West [16]. One of the latest studies from Germany by Probst et al. [17] demonstrated results with relatively high en-bloc and curative resection rates of 100% and 45.8%, respectively, with no endoluminal recurrence and disease-specific survival rate of 95.8% for over a mean follow-up period of 38 months. In the UK, the Japanese Esophageal Society and ESGE guidelines are used to select lesions for endoscopic resection [7,18,19]. The National Institute of Health and Care Excellence (NICE) only uses research evidence that is carefully audited in high-volume tertiary referral centres in the UK when formulating clinical guidelines [16]. No studies have focussed on the diagnostic and therapeutic potential of endoscopic resection for early-stage OSCC in the UK and as a result it is only recommended by NICE in the context of research.

As part of our clinical audit and service development, this retrospective study aims to investigate the long-term therapeutic efficacy and diagnostic potential of endoscopic resection in treating oesophageal squamous dysplasia or early neoplasia in the UK in a tertiary referral centre.

Materials and methods

Data collection

Detailed patient information was retrieved from multidisciplinary team meeting letters, endoscopy and histopathological reports via electronic patient records. Microsoft Excel was used for data processing and statistical analysis.

Inclusion and exclusion criteria

Only patients who were initially diagnosed with superficial oesophageal squamous neoplasms were included in the study. This means oesophageal lesions with low-grade dysplasia, high-grade dysplasia, and squamous cell carcinoma limited to the submucosal layer (Vienna 5; T1b sm1 and T1a m1-3) [20]. Patients with oesophageal adenocarcinoma and suspected squamous cell carcinoma beyond submucosal invasion (T1b sm2 and deeper invasion) with lymph node micrometastasis, or distant metastasis based on the results from EUS, computed tomography and PET scans were excluded.

Endoscopic resection procedure

Preoperative assessment and mapping with oesophagogastroduodenoscopy (OGD) was used to evaluate patient’s suitability for endoscopic resection. With the aid of white light, narrow-band imaging and Lugol’s iodine, lesion features were assessed by using Paris classification. The lifting ability of lesions is graded based on the Kato classification [6,21]. Intrapapillary capillary loops were not routinely assessed due to the nonavailability of zoom endoscopy. Lugol’s iodine was used to delineate the extent of lesion from the normal squamous epithelium. The resection border was established by placing marking dots approximately 5 mm from the tumour margin via argon plasma coagulation (APC) on the normal mucosa to provide safety margins. The lesions were lifted by injecting EMR solution (containing indigo carmine and 0.1% lidocaine) into the submucosal layer. Supplementary hyaluronic acid solution was used to achieve better lift in lesions of poor mucosal elevation caused by extensive fibrosis of the submucosal layer or ulceration of the lesion. Excision of the lesion was made outside the APC marking dots. Complete excision of lesion is determined by the endoscopists on the basis of the removal of all the APC marks.

Endoscopic resection procedures are mainly subdivided into piecemeal and en-bloc resections. Piecemeal resections were only completed by EpMR. En-bloc resections were achieved by EMR, ESD or Hybrid ESD. Both EMR and EpMR procedures involved the use of band-assisted endoscopic snare – the Duette Multi-Band Mucosectomy (COOK Medical; DT-6-5F) for lesion size <15 mm. Lesion size of >20 mm was completed by ESD. Lesion size between 15 and 20 mm can either be completed by ESD, Hybrid ESD or EpMR depending on the patient’s physical fitness for the procedure. Hybrid ESD was classified as ESD as the lesion was initially approached by a circumferential mucosal incision and submucosal dissection. The lesion was later removed completely in en-bloc with a snare. The rationale of using Hybrid ESD or EpMR was due to the time constraints and potential complications of putting a patient with multiple comorbidities and the American Society of Anaesthesiologists (ASA) grade 2–4 under general anaesthesia [22].

Details of the ESD procedure, endoscopic equipment and imaging enhancement techniques, as well as postendoscopic resection follow-up procedures involved in this study have been described previously by Sooltangos et al. [6] in 2017.

Histopathological evaluation

The resected specimens were gently stretched out, pinned onto polystyrene foam board, placed in 4% formalin and submitted for histopathological assessment. The fixed specimens were cut into parallel slices (each slice measuring approximately 3 mm in width) and processed into paraffin wax blocks. At least one histology section (3 µm in thickness) was produced from each paraffin block. All sections were mounted onto glass slides and stained with haematoxylin and eosin. Histopathologic evaluation was performed to assess lesional grade of differentiation, depth of invasion, resection margin involvement and lymphovascular space invasion status using standard histopathologic criteria and in accordance with the Vienna classification [7,18–20].

Defining outcomes

The primary outcome of this study was curative resection. A resection is considered curative (curative resection) when at least 1 mm of deep/vertical margin of a specimen are cleared from dysplastic or neoplastic cells [18,19]. Endoscopic resection was deemed to be noncurative (noncurative resection) when histology deep/vertical margin clearance from neoplasia was <1 mm. The changes in staging from endoscopic resection histology before and after endoscopic resection procedures were also investigated. This was recorded as the worst histological grade reported for each lesion. All of these outcomes were interpreted based on the number of lesion.

The secondary end-points were the complete reversal of dysplasia at 12 months or at the latest follow-up from the ‘curative resection’ patient group. These findings were then further analysed based on the most recent type of endoscopic resection received by patient (either by a piecemeal or en-bloc resection). Each patient is considered as a single entity regardless of the number of resections received.

Safety outcomes were evaluated and complications categorized as immediate (occurred during endoscopic resection or <48 h postendoscopic resection) or late (>48 h postendoscopic resection). A 5-year overall survival rate of patients with attempted and completed endoscopic resection was also reported.

Results

Patient demographics

Twenty-one patients who met the inclusion criteria were considered for endoscopic resection. The demographics of patients involved in the study are shown in Table 1. Out of the 21 patients, 18 were deemed suitable for endoscopic resection after mapping OGD. Endoscopic resection was attempted on 22 lesions. However, two lesions from one patient were aborted during the procedure. Twenty lesions from 17 patients were successfully completed (Fig. 1).

Table 1.
Table 1.:
Patient characteristics included in the study, n (%)
Fig. 1.
Fig. 1.:
PRISMA diagram illustrating selection process of patients associated with their outcomes. CR, curative resection; n L, number of lesions; n P, number of patients.

Preendoscopic resection endoscopic assessment

Most lesions were reported as Kato 1 and one lesion as Kato 3 [21]. The mean size of lesions resected was 34.8 mm (SD 19.0 mm; range 5–60 mm). Features of the lesions deemed suitable for endoscopic resection are shown in Table 1. Of the three patients who were unsuitable for endoscopic resection, two patients were eligible for diagnostic purpose only (one was diagnosed with verrucous squamous carcinoma whereas the other patient had extensive lesion with suspected submucosal invasion). The third patient had an extensive lesion involving >75% of the oesophageal circumference and proceeded with radiotherapy.

Index procedure

The median duration of the endoscopic resection procedures was 2 h. The length of time required for endoscopic resection procedures was affected by factors such as the size of the lesion, lesion location and tissue factors.

Two lesions were attempted by endoscopic resection but aborted during the procedure. One of the aborted lesions had poor lifting (Kato 3), while another lesion was identified to have deep submucosal invasion. Of the 20 resections completed successfully, en-bloc resection was achieved in 35% (7/20) of lesions, while piecemeal resection in 65% (13/20) of lesions.

For lesions ≤20 mm, six of them were removed via EpMR or EMR, whereas two of them were removed by ESD. From the 12 lesions size >20 mm, only one lesion was removed by ESD. The remaining 11 lesions were treated with EpMR (9/11) and Hybrid ESD (2/11). Results show that all 11 lesions belonged to patients with ASA grades 2–3 (i.e., moderate-to-severe risk while undergoing general anaesthesia) and thus EpMR or Hybrid ESD was recommended to be the primary treatment [8].

Resection was considered complete at endoscopy based on consensus made between endoscopists in 90% of lesions. Twelve lesions achieved a definite curative resection (60%; 11 patients) and eight lesions were confirmed to be noncurative resection (40%; 6 patients). From the 12 curative resection lesions, eight of them were excised by piecemeal resection (66.7%), whereas four lesions via en-bloc resection (33.3%). From the eight noncurative resection lesions, five of them were removed by piecemeal resection (62.5%), while three lesions by en-bloc resection (37.5%).

All eight resected lesions from six patients were categorized as noncurative resection as there was <1 mm histological clearance of neoplasia from deep/vertical resection margins. The histological diagnoses of these lesions were graded as invasive (Vienna 4.4 to 5) due to the presence of neoplastic cells invading into muscularis mucosae or submucosal layer.

Sixteen patients (94.1%) had no acute complications of the procedure. One patient (5.9%) suffered oesophageal perforation. This was immediately treated with endoclips and managed conservatively without sequelae. No patients were readmitted to hospital at a period of 8 days postendoscopic resection. The rate of late complications was 35% comprising six patients with oesophageal stricture. Five patients were treated with endoscopic balloon dilatation with or without biodegradable stent placement without complications.

Change in staging from endoscopic resection histology

The two patients who underwent oesophageal endoscopic resection for staging alone were included in the data for this outcome. Oesophageal endoscopic resection changed the histological grade in 79.2% of lesions (n = 24) (Fig. 2). Upstaging occurred in 41.7% of lesions and downstaging occurred in 37.5% of lesions. Invasive submucosal carcinoma was identified histologically in five lesions postendoscopic resection compared to only three lesions preendoscopic resection. Of these five lesions, one lesion upstaged from Vienna 4.2 to 5 [OSCC in situ to submucosal carcinoma (SMC)], two resections were upgraded from Vienna 4.3 to 5 (suspicious for invasive carcinoma to SMC) and two resections changed from Vienna 4.4 to 5 [intramucosal carcinoma (IMC) to SMC].

Fig. 2.
Fig. 2.:
Column chart showing the difference between preendoscopic resection and postendoscopic resection stage for all 24 resected lesions. Ca in situ, carcinoma in situ; Clear, no dysplasia or neoplasia; HGD, high-grade dysplasia; IMC, intramucosal carcinoma; LGD, low-grade dysplasia; n L, number of lesions; SMC, submucosal carcinoma.

Complete reversal of dysplasia/neoplasia of curative resection lesions

The complete reversal of dysplasia/neoplasia at 12 months and latest endoscopic follow-up was observed in 72.7% (8/11) and 63.6% (7/11) of patients from the curative resection group, respectively. Eight patients from the curative resection group had piecemeal resections, whereas three patients underwent en-bloc resections. The mean endoscopic follow-up period was 24.3 months (median, 19 months; range, 0–58 months) (Table 2).

Table 2.
Table 2.:
Secondary outcome in the cohort of curative resection group (n L = 12, n P = 11)

Piecemeal resected lesions

From the eight curative resection patients who had piecemeal resections, a complete reversal of dysplasia/neoplasia at 12 months was observed in 87.5% (7/8) of patients (Fig. 3a). The remaining one patient from this group was deceased (cause of death was unrelated to his primary oesophageal disease) before his 12-month endoscopic follow-up.

Fig. 3.
Fig. 3.:
(a) Column chart showing complete reversal of dysplasia at 12 months or latest endoscopic follow-up in the group for curative resection postendoscopic resection: piecemeal resection (on the left) and en-bloc resection (on the right). (b) Kaplan–Meier Survival Curve for 17 patients who had endoscopic resection and subsequent follow-up. CR, curative resection; n L, number of lesions.

Five of the eight patients (62.5%) were found to be free of dysplasia/neoplasia at their latest follow-up (Fig. 3a). One of the three patients was identified with metachronous recurrence 4 years postendoscopic resection and was treated with radiotherapy. However, this patient passed away 8 months later due to subarachnoid haemorrhage. The second patient was found to have a recurrence at the resection site at his 15-month follow-up. This patient passed away 4 years postendoscopic resection with cause of death unrelated to his primary oesophageal disease. The third patient was detected with metachronous recurrence 4 years postendoscopic resection and is currently under endoscopic surveillance only as he was unfit for further interventions.

En-bloc resected lesions

From the three curative resection patients who underwent en-bloc resections, only one patient (33.3%) has achieved a complete reversal of dysplasia/neoplasia at 12 months (Fig. 3a). This is because the remaining two patients have not reached their 12-month endoscopic follow-up at the time of study.

Two of the three patients (66.7%) were found to be free of dysplasia/neoplasia at their latest follow-up (Fig. 3a). A recurrence at the resection site was observed in one patient at his 17 months follow-up. This patient passed away 22 months postendoscopic resection due to metastatic prostatic carcinoma.

Surgery

Five patients were considered for surgery postendoscopic resection. From the six patients of the noncurative resection group, three of them proceeded to oesophagectomy. The remaining three patients in the noncurative resection group were unfit for surgery and had either a radiotherapy or under endoscopic surveillance. Another patient with submucosal SCC (Vienna 5) was listed for a three-stage oesophagectomy. One patient who had an aborted endoscopic resection during the procedure due to the oesophageal lesion invading submucosal layer subsequently had an oesophagectomy.

Overall survival rate

Among the 17 who had endoscopic resection, five deaths were identified and two patients were lost to follow-up. Although three out of the five deceased patients were found to have either recurrence at the resection site or metachronous recurrence at their endoscopic follow-up, none of these patients died due to their primary oesophageal disease. One patient died due to subarachnoid haemorrhage and one due to prostate carcinoma. The cause of death for the remaining three patients was deemed to be unrelated to their oesophageal disease. The mean and median age of deceased patients were 83.2 and 84 years, respectively, with a mean survival time of 37.4 months. The overall mean survival time of all 17 patients was 36.8 months. The five-year overall survival rate was 64% (mean follow-up: 24.9 months) (Fig. 3b).

Discussion

The effectiveness of endoscopic resection at achieving curative resection in this selected patient group has been investigated in this study. The main finding (curative resection = 60%) compares favourably with Ciocirlan et al. [23] and Probst et al. [17] who found curative resection rates of 16–21% and 45.8%, respectively. Although our result is worse than several endoscopic resection studies from Japan which had curative resection ranging from 82.9% to 99.1% [4,18,19,24,25], 72.7% (eight out of 11 patients) were clear of dysplasia/neoplasia at their 12-month endoscopic follow-up. In fact, no patient had disease recurrence at their 12-month follow-up. Notably, two patients have not achieved a 12-month follow-up by the time of data collection, and one patient was deceased before reaching his 12-month follow-up with a cause of death unrelated to his primary oesophageal disease.

Endoscopic resection was only introduced to the UK in the last 10 years making it a relatively new procedure [15,26]. In the UK, it is reported that 400 patients had endoscopic resection from 2014 to 2016, whereas 1198 patients in Japan had endoscopic resection in 2011 alone [26,27]. A lower rate of curative resection in our study demonstrates that we have some way to go until we maximize the potential of this treatment in the UK. Operator skills have a direct impact on the short- and long-term outcomes of endoscopic resection. This highlights the need to increase the volume of procedures and training opportunities, which are currently limited in the UK. Additionally, most of the early-stage OSCC was resected with en-bloc in Japan because EpMR was suggested to have higher disease recurrence rate [7]. We suggest that among patients with severe comorbidity or advanced age in whom prolonged procedures under general anaesthetic are best avoided, EpMR is useful for both staging and management of early squamous neoplasia. Although a relatively higher recurrence rate in this small series, most patients died from unrelated disease.

Three patients demonstrated noncurative resection tumour excision (deep/vertical endoscopic resection resection margins histologically clear from tumour by <1 mm) on postendoscopic resection histology. They went on to have surgery. The histological finding in the post-oesophagectomy samples from two of the three patients showed no evidence of recurrence/dysplasia around the endoscopic resection area. This finding suggests that some patients deemed ‘noncurative resection’ histologically do in fact have curative resections from endoscopic resection and that it may be more successful than the data shows.

According to the National Oesophago-gastric Cancer Audit 2017, 36.4% of oesophagectomy patients were reported suffering from systemic or surgical-related complications, and there was a 90-day postoperative mortality rate of 3.3% [26]. Endoscopic resection has lower morbidity rate when compared with oesophagectomy as only one patient (5.9%) in our study experienced serious complication postendoscopic resection. There was no mortality related to endoscopic resection in our study.

The 5-year overall survival rate was 64%, which compares with oesophagectomy survival rates of 46–83% [28]. This finding is also comparable with other studies on EpMR/EMR where 5-year survival rates range from 58% to 67% [23,29,30]. Our result was also on par with an ESD study done by Probst et al. [17], but compares negatively to another ESD study from Park et al. [24] who reported a 5-year overall survival of 89%. Most of the lesions resected in our study were performed by EpMR/EMR with only a minority of lesions done by ESD and hybrid ESD/EpMR. Hence, our finding does not seem to be greatly inferior compared with the previous studies of patients who were treated by EpMR/EMR alone.

Endoscopic resection was found to change the staging in 79.2% of lesions. In the context of upstaging, endoscopic resection effectively identified three lesions with submucosal invasion, where two of these lesions presumed to be IMC and one case with carcinoma in situ only. This is essential as submucosal invasive carcinoma carries a 20–50% chance of lymph node micrometastasis and may require additional radical treatment such as oesophagectomy, radiotherapy with or without chemotherapy [30]. As supported by several studies, endoscopic resection is suggested to be a more definitive staging tool to guide treatment and prognosis [6,23,31].

The main limitation of this study was the small sample size. OSCC is responsible for only one-third of the total oesophageal cancer incidence in Western populations and endoscopic resection is only eligible to treat relatively early forms before it invades deeper than submucosal layer. For the future, we hope to increase the robustness of the conclusions by a larger number of patients with longer follow-up.

In conclusion, this study provides some promising evidence in favour of the use of endoscopic resection at treating oesophageal squamous dysplasia or early neoplasia in the UK. Despite relatively low histological curative resection rates, our results demonstrate promising long-term outcomes.

Acknowledgements

We thank the clinical and pathological staff for their contribution in helping us to obtain the data and laboratory reports.

J.Y.K. and Y.K. coordinated the study, obtained and analysed the data, and wrote the manuscript. S.M. contributed to manuscript revision. G.R. and Y.A. performed the ESD and analysed the data. R.C. performed surgery and analysed the data. S.B., A.A. and N.P. contributed to the data analysis and manuscript revision. Y.A. designed the study, supervised the project, obtained the data and finalized the manuscript. No external grant support foundations provided.

This study is under ‘audit and service improvement’ section of our directorate and as such no research ethical approval is required.

Conflicts of interest

There are no conflicts of interest.

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Keywords:

early oesophageal cancer; endoscopic mucosal resection; endoscopic resection; endoscopic submucosal dissection; oesophageal squamous cell carcinoma

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