INTRODUCTION
The diverticula of the oesophagus represent a rare benign oesophageal disorder, with the exact incidence to be unknown since patients are often asymptomatic. It is estimated to be up to 2% in Europe,[1] with a higher prevalence in elderly men. An oesophageal diverticulum is an out-pouching of the epithelial-lined tissue of the oesophageal wall. It may be either a true diverticulum, involving all layers of the oesophagus, or a false diverticulum, involving only the mucosa and submucosal layers protruding via the circular and longitudinal oesophageal muscle.[2]
Oesophageal diverticula are commonly classified in three types based on their location: upper (pharyngo-oesophageal/Zenker), middle or distal (epiphrenic). Further classification relates to presumed pathogenetic mechanisms, leading to their formation, namely traction versus pulsion. As such, middle oesophageal diverticula are believed to develop from traction as a consequence of long-standing mediastinal inflammation or fibrosis-as in tuberculosis or histoplasmosis.[2,3] On the contrary, pharyngo-oesophageal and epiphrenic diverticula (ED) usually occur from repeated elevated intraluminal pressure in the area of the diverticulum often as a result of an associated underlying oesophageal motility disorder[4] or more infrequently due to an underlying hiatal hernia or an oesophageal stricture.[5]
The ED typically arises within 10 cm above the lower oesophageal sphincter (LOS), have a tendency to project into the right thoracic cavity and often are asymptomatic.[6] When symptoms are present, the predominant one is dysphagia, typically progressive. Regurgitation, halitosis, chest pain and heartburn are also common.[7] It is important to appreciate that these symptoms are often a reflection of an additional underlying oesophageal disorder as motility disturbance, reflux disease or hiatal hernia rather than the diverticulum itself.[8]
Multiple studies have indicated that asymptomatic ED does not require resection.[9,10] In asymptomatic patients with small diverticula, routine clinical and endoscopic follow-up is therefore advised.[11] The indication for surgical treatment should be carefully evaluated based on the patient’s symptoms and general condition[12] due to significant associated perioperative complications. When the indication is present, minimally invasive diverticulectomy with oesophageal myotomy and partial fundoplication, when deemed appropriate, is considered the gold standard of treatment. While there is a gradual agreement on the pre-operative assessment, no consensus is found with respect to the surgical technique as to when an additional myotomy should be executed, the length of the myotomy or the type of antireflux procedure.[13]
The aim of the present study is to report our experience and propose a standardised approach to manage this rare oesophageal disorder with regard to pre-operative assessment, optimisation for surgery and the optimal selection of both the surgical candidates and the surgical technique as well.
MATERIALS AND METHODS
Study design
The present study was designed according to the Strengthening the Reporting of Observational Studies in Epidemiology Statement:[14] guidelines for reporting observational studies. A study protocol was developed and strictly, followed by all participating authors. Institutional Review Board approval was obtained before the start of the study.
Enrolment period was from January 2015 to December 2020. All consecutive adult patients who underwent elective surgery for symptomatic epiphrenic diverticulum at the Department of Upper gastrointestinal (GI) Surgery, St Thomas’ Hospital, Guy’s and St. Thomas’ NHS Foundation Trust, London, UK, were deemed eligible for inclusion. Exclusion criteria were non-adult patients (<18 years old) and those submitted to emergency surgery.
Data extraction
Two independent authors (DZ, FDM) extracted the data from our prospective database. Discrepancies in data extraction were resolved after consensus with a third independent author (EB).
Variables of interest included
- Epidemiological and clinical characteristics encompassing age, gender, body mass index (BMI), pre-operative health of the surgical candidates based on the American Society of Anaesthesiologists’ (ASA) classification of physical health grading system (ASA score I-V), Indication for Surgical Intervention-Main presenting symptom, Pre-operative symptom assessment based on Eckardt score chart, Type and date of the surgical operation
- Pre-operative work-up including Oesophago GastroDuodenoscopy (OGD), barium study (BS) and high-resolution manometry (HRM) for evaluation of oesophageal motility, size/location of epiphrenic diverticulum, co-presence of associating hiatal hernia or other upper GI pathology, pre-operative diet for optimisation for surgery
- Intraoperative outcomes in the form of operative time (minutes), estimated blood loss (EBL, ml), conversion to open approach, type of surgical operation utilised
- Early post-operative outcomes including diverticulum’s size on histology, minor/major complications, in- and out-of-hospital mortality, length of Hospital stay (LOS, days). The severity of complications was categorized according to the Clavien-Dindo classification system. Minor complications were defined as Grade < II and major complications were those of Grade > IIIa
- Long-term outcomes focussed mainly on residual symptoms (post-operative Eckardt score) with or without endoscopic assessment as well as the length of follow-up, recurrence rates, disease-free survival (DFS) and overall survival (OS). DFS was defined as the period from the surgery date and the first time of recurrence or the date of the last follow-up without recurrence. OS was defined as the period between the operation date and death of the patient or the date of the last follow-up if the patient was still alive.
Statistical analysis
Descriptive statistics were used on the characteristics of patients. Continuous variables were described using mean (–standard deviation) or median (range).
RESULTS
Epidemiological and clinical characteristics of the study population
A total of six patients were enrolled and the general characteristics of the surgical group are described in Table 1. The median age of patients at the time of surgery was 65.5 years (range 49–71). Most patients were male (n = 5/6, 83.3%) with a BMI ranging from 26 to 30. Median ASA Class was II (range I–III).
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Table 1: Epidemiological and clinical characteristics of the study population
Among patients who underwent surgical operation with the indication of symptomatic diverticular disease (n = 6), a total of three patients (50%) had dysphagia in solid/semisolid food as their predominant symptom, whereas the remainder three patients presented with chest pain, regurgitation, post-prandial vomiting and one with GI bleeding. The median pre-operative symptom assessment based on the Eckardt scale chart was 5 ranging from 3 to 5.
Among the patients who underwent laparoscopic diverticulectomy (n = 6), a total of three patients underwent additional myotomy and anterior fundoplication (50%), two additional myotomy, anterior fundoplication plus hiatal hernia repair (30%) and one only additional hiatal hernia repair (20%).
Pre-operative work-up of the study population
All cases were discussed at the benign multi-disciplinary meeting (MDM) before surgery. Particular importance was given to pre-operative assessment with OGD, BS and HRM performed to all cases to ensure appropriate patient selection [Table 2]. The OGDs and BSs demonstrated diverticulum’s median distance from teeth at 35 cm ranging from 32 to 42 cm, an associated hiatus hernia in three out of six patients (50%) and an underlying mild oesophagitis in four out of six patients (67%) [Figure 1]. HRMs demonstrated normal motility, absent contractility, fragmented peristalsis and Jackhammer oesophagus in 2/6, 2/6, 1/6 and 1/6 patients, respectively. LOS was normotensive in four, hypertensive in one and hypotensive in the remainder one patient.
Table 2: Pre-operative work-up of the study population
Figure 1: Initial oesophagram of patient Nr 3 demonstrating the diverticulum and hiatal hernia. HRM findings were fragmented peristalsis with normotensive LOS. HRM: High resolution manometry, LOS: Lower oesophageal sphincter
During the surgical operation on Patient Nr 3, at on-table OGD old solid food was stuck in the diverticulum pouch. To obtain an empty, clean diverticulum the lavage took 40 min and left a distended abdomen to deal with during the laparoscopic approach [Figure 2]. In order to avoid food residues inside the diverticular pouch in the future and to be able to simplify the surgical operation and minimise the risk of stapler line leakage, we implemented a specific diet in preparation for surgery. To this end, all subsequent patients of this cohort (Patient Nr 4–6) were asked to blend all their food for 1 week before surgery and to stay on a liquid diet the day before.
Figure 2: (a) Initial intraoperative endoscopic view with old solid food stuck in the diverticulum pouch, (b) Intraoperative endoscopic view after 40 min lavage to ensure clean pouch for safe resection
Surgical technique and technologies
The surgical operations were conducted with the Olympus VISERA ELITE II OTV-S300 three-dimensional (3D)-video system with a 2 dimensional/3D processor, light emitting diode light source and liquid-crystal display monitor providing full HD/3D displays. Intraoperative gastroscopy was performed with the Olympus EVIS LUCERA ELITE Video Flexible Routine Interventional GI Scope with Two Working/Suction Channels, with an outer diameter of 9.9 mm and a working length of 1030 mm.
Each patient was placed in a supine position with legs open and anti-Trendelenburg tilt. Before preparing the surgical field, a gastroscopy was performed to ensure no food residue was in the diverticulum. A washout was conducted if deemed appropriate and, after taking care to remove all the air in the stomach, the scope was left in as a bougie. Pneumoperitoneum was obtained through Veress needle. Five laparoscopic ports were introduced: two 10–12 mm (supraumbilical-slightly left of midline; left upper quadrant) and three 5 mm (right upper quadrant, subxiphoid and left flank). The operating surgeon stood between the patient’s legs, the assistant on the left. A 30° camera was inserted and a diagnostic laparoscopy performed. A liver retractor was then positioned through the subxiphoid port. The diaphragmatic crura was exposed, the oesophagus then isolated in its distal segment and mobilised in the lower mediastinum. We used Harmonic scalpel for dissection (Ethicon-part of Johnson and Johnson Medical Devices). Ideally, the pleural cavity was not breached during preparation. The diverticulum was then identified and its neck isolated circumferentially. The diverticulum was excised using an Echelon (Ethicon-part of Johnson and Johnson Medical Devices) 45 mm endostapler (blue/white cartridge), with care taken to line up the stapler exactly parallel to the longitudinal axis of the oesophagus, and then extracted through the 10–12 mm port. Staple line reinforcement with the approximation of the muscular layer was routinely conducted to all cases, whereas no intraoperative leak-test (apart from endoscopic inspection) was conducted. In 5/6 patients, a long anterior myotomy was performed from 2 cm below the cardia to reach a point above the inferior aspect of the neck of the diverticulum, as well as an anterior/Dor fundoplication as anti-reflux procedure. In 1/6 patients, we did not perform myotomy or fundoplication. In 3/6 patients, we conducted an anterior hiatal repair using Ethibond sutures (Ethicon-part of Johnson and Johnson Medical Devices).
A transabdominal mediastinal drain was finally introduced through the hiatus. The median operative time was 180 min (range 165–241), and the median EBL was <100 ml (range 100–150), with no intraoperative complications and no conversions to the open approach [Table 3].
Table 3: Intraoperative outcomes of the study population
Early post-operative outcomes of the study population
Data related to early post-operative outcomes are reported in Table 4. Post-operative recovery was uneventful in 3/6 patients (50%). The rest of 3/6 patients developed Minor-Class II complications according to Clavien–Dindo classification in the form of hospital-acquired pneumonia (2/3) and urinary retention (1/6). None developed oesophageal leakage.
Table 4: Early post-operative outcomes of the study population
In line with our protocol, all patients were allowed sips of water straight after surgery and clear fluids on the post-operative day (POD)-1. Either a blue dye swallow test or a water-soluble study (WSS) was conducted on POD-2, before progression with oral intake of soft minced food and removal of the drain [Figures 3 and 4]. Patients were usually discharged on POD-4 or POD-5 on a soft diet for 4 weeks. One out of the six patients was discharged on POD-10 due to pneumonia necessitating intravenous antibiotic treatment. Overall, in- and out-of-hospital 30- and 90-day mortality was 0%.
Figure 3: (a) Pre-operative oesophagram of patient Nr 5 demonstrating a large distal oesophageal diverticulum. HRM findings were absent contractility with hypotensive LOS. (b) Oesophagram post-diverticular resection and hiatal hernia repair with no addition of myotomy/fundoplication. HRM: High resolution manometry, LOS: Lower oesophageal sphincter
Figure 4: (a) Pre-operative oesophagram of patient Nr 6 demonstrating the diverticulum, (b) HRM findings were absent contractility with hypertensive LOS, (c) Oesophagram post-diverticular resection with addition of anterior myotomy and Dor fundoplication. HRM: High-resolution manometry, LOS: Lower oesophageal sphincter
Median size of 54 mm × 31 mm × 15 mm pouch was demonstrated by the final histopathological examination of the diverticula specimens.
Long-term outcomes of the study population
Complete overview of the long-term outcomes is shown in Table 5.
Table 5: Long-term outcomes of the study population
Patients were reviewed in the outpatient clinic 6–8 weeks after their discharge. Visit was mainly focussed on oral intake and further progression to free diet, as well as overall post-operative recovery. A clinical examination was also performed to check for wound healing and eventual post-operative complications. The presence of any residual symptoms was checked and documented by asking patients to complete a second Eckardt chart within 6 months of surgery. Further investigations were not routinely performed unless clinically indicated. In line with our follow-up protocol, the patients were thereafter reviewed every year either via either a face-to-face or a telephone consultation in our outpatient clinic. An OGD or a BS test was then carried out if someone became somewhat symptomatic (higher Eckhard scores in comparison to previous ones), aiming to check the healing of the oesophageal mucosa and any recurrences.
In terms of residual disease, adequate resection margins were achieved in 5/6 patients (83.4%). In one out of six patients (Patient Nr 1), a diverticulum pouch remnant was identified early in their post-operative follow-up consultation (10 mm × 5 mm), which may have led to patient’s later recurrence presenting with progressive dysphagia at 59 months and an Eckard score of 5 (initially 0 postoperatively). Investigation tests at that point revealed a recurrent diverticulum with an increased size of 35 mm × 15 mm and the patient was submitted to revision diverticulectomy and fundoplication taken down. At 18 months’ follow-up since the redo-operation, they are asymptomatic with no documented residual disease [Figure 5].
Figure 5: (a) Recurrence of distal oesophageal diverticulum (patient Nr 1) noted just proximal to the GOJ with no hold-up of contrast on semi-solid bolus in the diverticulum. No hiatus hernia, reflux or oesophageal dysmotility is demonstrated, (b) Oesophagram post-revisional surgery. No extraluminal leak at the surgical site or evidence of previous recurrent diverticulum is demonstrated. Previous fundoplication taken down intraoperatively. GOJ: Gastro-Oesophageal junction
Median follow-up was 66 months, (range 19–77), median DFS was 60.5 months (range 19–72) and OS 66 months (range 19–77). All-cause mortality was 16.4%. Patient Nr 4 died on 08.04.22 due to age-related conditions.
DISCUSSION
Oesophageal diverticular surgery has a long history, with the first diverticulectomies to be described in the early 1900s successfully carried out by Mayo-1910,[19] Barrett-1933, De Bakey-1948[20] and by other pioneer surgeons of the previous century. For decades, multiple changes to diverticular surgery were developed, leading to the first minimally invasive approach for ED, involving transhiatal diverticulectomy, oesophageal myotomy and partial fundoplication described by Rosati[12] in 1998, the introduction of which revolutionised the principles of minimally invasive surgery for oesophageal diverticula.
Minimally invasive diverticulectomy associated with subdiverticular myotomy and possibly gastric fundoplication represents the current standard surgical treatment for symptomatic patients.[21] Benefits of the minimally invasive approach include reduced blood loss, decreased perioperative complications and post-operative pain, shorter recovery time and hospital stay, improved cosmesis and probably a more efficient use of health-care expenditure. The technique can be performed either by thoracic approach (thoracoscopy)[22] or by abdominal approach through laparoscopy,[23] as the optimal pathway for the ED still remains a controversy.[24] While each approach has its relative advantages and potential limitations, comparative studies show no significant discrepancies in outcomes related to morbidity and mortality, as well as insufficient excision or recurrence.[11,25]
Herein, we report our experience in 3D laparoscopic transhiatal diverticulectomy ± anterior myotomy ± anterior fundoplication and propose a standardised approach to manage this rare oesophageal disorder. We prospectively analysed data of six consecutive patients who underwent distal oesophageal diverticulum resection between 2015 and 2020 at the Department of Upper GI Surgery, St Thomas’ Hospital, with regard to patient selection and related pre-operative assessment, optimisation for surgery, surgical technique and post-operative outcomes.
Patient selection criteria for surgery were tailored by careful symptom evaluation, supported by thorough pre-operative investigation series, followed by risk stratification of their overall fitness status.
We implemented the pre-operative symptom assessment Eckardt Chart-typically used for achalasia-in an effort to objectify patients’ symptoms. Only symptomatic patients were considered eligible for surgery.[26] Diverticulum’s size did not affect eligibility for surgery.
In line with the literature, our pre-operative investigations series encompassed BS, OGD and HRM.[3] Typically, BS demonstrates the location and size of the diverticulum with great accuracy and sensitivity. Endoscopy provides valuable information on the diameter of the diverticulum’s neck and distance from teeth, rules out malignancy and identifies co-presence of other conditions such as reflux oesophagitis and hiatus hernia, often associated with ED. The operating surgeon performed the OGDs in order to have a better understanding of the anatomy and plan the surgical treatment. HRM reveals potential underlying oesophageal dysmotility disorder that may have contributed to the development of ED, which may also be associated with the pre-operative symptoms. In addition to its role in the pre-operative assessment, HRM, when combined with BS may also guide a tailored myotomy.[27]
Risk stratification of the overall fitness status was carried out based on the ASAs’ classification of physical health grading system (ASA score I-V).
All cases were discussed at the MDM to review the pre-operative investigations and plan the operation. All cases were referred preoperatively to dieticians to review and support their nutritional needs in preparation for surgery.
We also implemented a specific diet in preparation for surgery. We considered it after the first three cases, which all had food residues in the intraoperative OGD and required time-consuming endoscopic washouts to obtain a clean diverticular pouch so as to perform the resection in a safely manner minimising the potential risk of staple line leak. To this end, we advised the following patients of our cohort to stay on a blended diet for a week, with the past 24 h before surgery consisting of liquids only. This appeared to be helpful in our subsequent cases, where the pouch was found clean at on-table OGD, enabling a safer and faster resection.
With regard to the surgical technique, taking advantage of the vast progress been made in skills, instruments and technology, we employed adjuncts as a 3D-system and a camera holder to improve the laparoscopic vision and optimise the surgical procedure. We found the 3D-vision together with the steadiness of the image when using a camera holder, most helpful during the hiatal and mediastinal dissections.
In 5/6 patients of our study, we performed an additional long anterior myotomy, from 2 cm below the cardia to reach above the inferior aspect of the diverticulum’s neck, as well as an anterior/Dor fundoplication for the anti-reflux barrier.[28] The incidence of gastro-oesophageal reflux after a myotomy can get up to 50% if not followed by a fundoplication. Controversy remains related to the most suitable type of fundoplication, in order to avoid a high-pressure zone that may favour staple line leakage. Based on our local protocol, we routinely perform a partial anterior wrap, which has demonstrated good anti-reflux potential and a low incidence of dysphagia when concomitant disrupted oesophageal motility is in place.[29] In 1/6 patients, we did not perform myotomy with fundoplication since pre-operative HRM findings were absent contractility with hypotensive LOS with complete relaxation on wet-swallows.
3D laparoscopy ensured us easier access to visualise the Gastro-Oesophageal junction and thus facilitate the proximal part of the myotomy, which could then be safely extended high in the mediastinum above the level of the diverticular neck. It also warranted better alignment of the stapler cartridge to the longitudinal axis of the oesophagus, thus avoiding blind remnants at the level of the suture line and the opportunity to perform a combination of myotomy with antireflux and crural repair procedures. Technical difficulties were noted when the time came to dissect the upper part of the diverticular neck, especially for large diverticula, which is known to be demanding via the laparoscopic approach with risks of pneumothorax, intra-thoracic bleeding and oesophageal perforation.
Post-operative recovery was uneventful in 3/6 patients (50%). The rest of 3/6 patients developed Minor-Class II complications and 0/6 developed oesophageal leakage from the staple line. We routinely perform stapler line reinforcement but no intra-operative leak test. Overall, in- and out-of-hospital 30- and 90-day mortality was 0%.
In agreement with our protocol’s pre-defined post-operative nutrition scheme, all patients were allowed sips of water straight after surgery and clear fluids on POD-1. Either a blue dye or a WSS test was conducted on POD-2, before progression with oral intake of soft minced food and drain removal. All patients were discharged on a soft diet for 4 weeks.
All patients were reviewed in the outpatient clinic 6–8 weeks after discharge. The presence of any residual symptoms was checked and documented by a post-operative Eckardt chart. Further investigations were not routinely performed unless clinically indicated. In line with our follow-up protocol, they were thereafter reviewed every year either through a face-to-face or via a telephone consultation in our clinic, with a median follow-up of 66 months.
In terms of recurrent disease, 1/6 patients developed symptomatic recurrence presenting with progressive dysphagia at 59 months’ post-initial surgery, necessitating revision diverticulectomy and taken down of their fundoplication. While a minor diverticular remnant was identified early after the first operation, it is uncertain if this was actually the cause of patient’s recurrence. Interestingly, this particular patient did not have any associating motility disorder, hiatal hernia or stricture-known potential pre-disposing factors to elevated intraluminal pressure, which can generate a diverticulum. This may be another indication that there are still uncharted territories in the pathogenesis route of oesophageal diverticula that once explored, may lead to improvement of treatment outcomes.
CONCLUSIONS
Minimally invasive operations for oesophageal ED are feasible but also challenging. Laparoscopic transhiatal resection, long oesophagomyotomy and an anterior anti-reflux procedure provide reliable long-term functional results with relatively low perioperative morbidity and mortality, as well as minimal recurrence rates.[30]
Optimal patient selection based on thorough pre-operative assessment with HRM as the cornerstone, pre-operative optimisation for surgery with the implementation of a blended liquefied diet for 1 week, multidisciplinary approach, experience alongside innovation in surgical techniques and meticulous follow-up are all fundamental to improve post-operative outcomes before undertaking treatment for this rare benign oesophageal disorder.
Compliance with ethical standards
All procedures were conducted in accordance with the Helsinki declaration of 1964 and later versions.
Financial support and sponsorship
Nil.
Conflicts of interest
There are no conflicts of interest.
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