Minimally invasive surgery for adult oesophageal duplication cysts: Clinical profile and outcomes of treatment from a tertiary care centre and a review of literature.

BACKGROUND: Oesophageal duplication cysts (ODC) are rare in adults. Complete surgical excision is the ideal treatment. Conventionally, it is performed through a thoracotomy. We aimed to study the feasibility and safety of minimally invasive surgery (MIS) in the management of ODC and briefly reviewed the available literature.
MATERIALS AND METHODS: A retrospective study of all adult patients with ODC diagnosed and treated at our tertiary care centre, from 2015 to 2019, was done. All patients were operated on by MIS. Their demographic, clinicopathological, radiological and surgical details and outcomes were analysed.
RESULTS: A total of six patients (four females and two males) were diagnosed to have ODC by contrast-enhanced computed tomography. The mean age was 38 ± 4.4 years. The most common presenting complaint was chest pain (50%). Upper gastrointestinal endoscopy was normal in four patients. Endoscopic ultrasound was performed in five patients. In four patients, the cyst was located in the distal third of the oesophagus. The mean size of the cysts was 5.7 ± 2.02 cm. All the patients were operated upon by video-assisted thoracoscopic surgery (VATS). There was no conversion to open surgery. The resection was complete in all but one patient. The mean duration of surgery was 143.3 ± 35 min, and the average blood loss was 58.33 ± 20.4 mL. One patient had an oesophageal staple line leak on the 9th post-operative day. There was no mortality. The median duration of hospital stay was 7.5 days (range: 3-25 days).
CONCLUSION: MIS is feasible and safe in the management of adult ODC.

INTRODUCTION

Oesophageal duplication cysts (ODC) are developmental anomalies which usually present in childhood and hence are rare in adults.[12] Adults with ODC are mostly symptomatic, presenting with chest pain, dysphagia or symptoms of a complication.[234] A contrast-enhanced computed tomography (CECT) scan is usually diagnostic. Complete surgical excision is the gold standard of treatment, conventionally done by a thoracotomy. With increasing expertise in minimally invasive surgical (MIS) techniques, it has become possible to manage this benign condition by video-assisted thoracoscopic surgery (VATS), avoiding the morbidity of a thoracotomy. Only a few case reports of VATS for ODC are available in the literature.[5678910] In this paper, we have analysed the clinical profile, details of investigations, surgical technique and outcomes in six consecutive patients with ODC, treated by VATS in our institution.

MATERIALS AND METHODS

After obtaining the necessary clearance from the institutional review board (IRB Min. No. 12998 [Retro] dated 24 June 2020), a retrospective study of all adult patients with ODC, managed in our institute between January 2015 and December 2019, was done. The demographic and clinical data were obtained from electronic medical records. The images and the reports of the pre-operative radiological studies and the upper gastrointestinal (UGI) endoscopy were retrieved for the study. The operative details were obtained from the operation records. All post-operative complications were classified according to the Clavien–Dindo grading.[11] All continuous variables were expressed as mean ± standard deviation or median with range.

RESULTS

There were six patients (four females and two males) with ODC diagnosed and operated upon in our institution during the study period, with a mean age of 38 ± 4.4 years. All the patients were symptomatic at presentation. Chest pain was the predominant symptom in this group (n = 3). Two patients had Grade-2 dysphagia and one presented with the complaints of recurrent cough. Clinical examination was unremarkable in all patients. As per the American Society of Anesthesiologists grading, four patients belonged to Grade 1, and the remaining two patients belonged to Grades 2 and 3.

The chest radiography showed a left posterior mediastinal mass in two patients and was unremarkable in the remaining four patients. All patients had a CECT scan of the thorax for diagnosis and planning of the surgery. All the patients underwent a UGI endoscopy. It was normal in four patients, and in the other two, it revealed a sub-mucosal bulge. The two patients with dysphagia had a barium swallow study, which was normal. Five patients had endoscopic ultrasound (EUS) performed as part of the initial evaluation. EUS-guided fine-needle aspiration cytology (FNAC) was performed by the referring physician in two patients before they were seen in the surgical department. The cyst was located in the distal third of the oesophagus in four patients and the mid-oesophagus in the other two. The mean size of the cyst was 5.7 ± 2.02 cm. The radiological findings of the six cases are summarised in Table 1.

Table 1

Endoscopic ultrasound and contrast-enhanced computed tomography scan of thorax findings

Case number	EUS			CECT thorax
	Echogenicity	Atypical findings	FNAC	Location of the cyst in the oesophagus	Size (cm3)	Complications of the cyst
Case 1	Hypoechoic	Nil	Mucoid material	Left lateral wall of the distal 3rd	4.3×3.8×4.2	Probably infected
Case 2	Hypoechoic with internal septa	Nil	N/P	Left posterolateral wall of the mid 3rd	3.9×3.8×3.9	Probable fistulation into the lumen
Case 3	Hypoechoic	Nil	N/P	Left lateral wall of the distal 3rd	9.2×4.5×6.6	Nil
Case 4	Hypoechoic	Nil	N/P	Right lateral wall of the mid 3rd	4.8×3.6×4.4	Nil
Case 5	Hypoechoic	Nil	Mucoid material	Left lateral wall of the distal 3rd	7.0×6.5×3.9	Nil
Case 6	N/P	N/P	N/P	Right lateral wall of the distal 3rd	5×5×3	Nil

EUS: Endoscopic ultrasound, CECT: Contrast-enhanced computed tomography, FNAC: Fine-needle aspiration cytology, N/P: Not performed

VATS technique was used in all patients in this case series. Under general anaesthesia, the patients were positioned in a semi-prone position. A single-lumen endotracheal tube was used in two patients and a double-lumen tube in the remaining four patients. Optical trocar entry was used to create a pneumothorax in five patients and a Veress needle in one patient. In addition to the 10-mm camera port, two 5-mm ports were used.

The cysts were dissected off the surrounding structures in the mediastinum, and its base was delineated by splitting the oesophageal muscle fibres vertically. In two patients, the cysts ruptured during dissection and hence mobilisation continued after its contents were evacuated. Enucleation of the cyst was performed in two patients. In one patient, only a partial excision was feasible, wherein a small portion of the cyst wall was left behind after thoroughly cauterising its mucosa. In three patients, where the cyst was fused with the oesophageal wall, the resection was completed using an endoscopic linear cutter stapler. Two patients developed focal perforation of the oesophageal mucosa during the dissection of the cyst, both of which were identified intraoperatively and suture repaired with 3/0 polyglactin. In five cases, the split muscle fibres of the oesophagus were approximated using interrupted or continuous 3/0 polydioxanone sutures (PDS). In all cases, an intercostal drainage tube was placed in the chest, before the ports were closed. A brief description of the stapled resection technique for a cyst which had fused with the oesophageal wall is given in Figure 1. The intraoperative details are summarised in Table 2.

Figure 1

(a) The oesophagus being mobilised along with the cyst, off the mediastinum (yellow arrowhead). (b) The base of the cyst is being delineated by separating the adventitia and muscle fibres (yellow arrowhead) (c) demonstrating the isolated cyst, and its fused wall with the oesophagus. (d) Application of endostapler. (e) The cyst being transected off the oesophagus along its fused part. (f) A defect in the muscular layer of the oesophagus being suture repaired

Table 2

Operative details

Variable	n=6
Approach
Left VATS	3
Right VATS	3
Intraoperative rupture of the cyst	2
Mucosal perforation	2
Technique of resection
Enucleation	2
Partial excision and cauterisation of the residual wall mucosa	1
Endoscopic linear cutter stapler	3
Closure of defect
Mucosal	3/0 polyglactin - 2
Muscle	3/0 PDS - 5
Intraoperative endoscopy	2
Specimen extraction
Mini-thoracotomy	2
Endo bag	3
Piecemeal	1
Drains	6
Feeding procedure	1 (FJ)
Completeness of resection	Complete - 5
	Incomplete - 1

VATS: Video-assisted thoracoscopic surgery, PDS: Polydioxanone suture, FJ: Feeding jejunostomy

The mean duration of operation was 143.3 ± 35 min and the average blood loss was 58.33 ± 20.4 mL. There was no conversion to thoracotomy. All patients were extubated on the table and returned to the ward. One patient who had multiple medical comorbidities was observed overnight in the intensive care unit. One patient developed a sudden rise in the intercostal drainage output on the 9th post-operative day, after the initiation of an oral diet. A CECT scan of the thorax with oral contrast showed an oesophageal staple line leak (Clavien–Dindo Grade 4a) with a left-sided empyema [Figure 2]. This was managed by thoracoscopic decortication, washout and re-inforcement of staple line with 3/0 PDS suture over a Bougie positioned in the oesophagus. A feeding jejunostomy was also performed. Although she had a stormy post-operative period, she recovered completely. There was no mortality in this series. The patients were started on oral solids after a median period of 5.5 days (range: 2–31 days). The median duration of hospital stay was 7.5 days (range: 3–25 days). All patients had histopathological confirmation of the diagnosis. There was no evidence of dysplasia or malignancy in any of the resected specimens. Two patients contacted by telephone, 38 months and 46 months, post-operatively, were asymptomatic, while the rest were lost to follow-up.

Figure 2

Computed tomography scan of the thorax with oral contrast showing active leak of the contrast from the oesophagus (yellow arrow) and a left-sided intrapleural collection (black arrow)

DISCUSSION

Duplication cysts of the gut are congenital developmental anomalies that may occur in the foregut, midgut or hindgut. The common sites of duplication cysts are the ileum (35%–45%), oesophagus (10%–15%), jejunum (10%), colon (7%–13%) and stomach (2%–9%).[212] At around the 4th week of gestation, the lumen of the primitive oesophagus becomes solid due to the rapid proliferation of its epithelium. Later, multiple vacuoles form within this solid lumen and later coalesce to form the lumen of the oesophagus. Failure of some of these vacuoles to coalesce by the 5th–8th weeks of gestation results in a cyst that later gets enveloped by the muscle layers of the gut, thus forming the duplication cysts.[21213] This condition was first described in 1711 by Blasius.[2]

The overall estimated prevalence of ODC is 0.0122%.[114] Majority of them present as masses along with or in continuity with the native oesophagus.[12] About 75% of them arise in the lower third of the oesophagus and commonly present in the right posterior mediastinum.[1312] Though termed ‘cysts’, they may present as tubular masses or as a diverticulum in 20% of the patients.[312] In our series, all patients had the cystic subtype of duplication and 66.7% of them were located in the lower third of the oesophagus. Four cysts were located in the left lateral wall of the oesophagus and two in its right lateral wall.

These cysts are more common in the paediatric population.[215] Delayed presentation in adults is infrequent.[23451416] The most common age at presentation is in the second and third decades and is more common in males.[13] Our series had comparatively more females (n = 4) and older patients with a mean age of 38 ± 4.4 years. The majority of adults with ODC are usually symptomatic, though some may be diagnosed incidentally.[3] Most symptoms are mild and non-specific and are related to the location of the cyst.[117] Chest pain, epigastric discomfort, dysphagia to solids, vomiting, cough, dyspnoea and backache are the frequent initial symptoms.[12] The symptoms could also arise as a result of its complications such as rupture, infection, fistulation and atrial fibrillation.[121819] Ulceration and bleeding from ectopic gastric or pancreatic cells within the cyst and a rare malignant transformation have also been reported.[920] The most common presenting symptom in our series was chest pain and dysphagia to solids. None of the patients had presented with a complication of the cyst.

Radiologically, the ODC may be cystic, tubular or diverticular type. Chest X-ray findings will be non-specific. ODC may be seen as well-circumscribed or tubular, smooth, mediastinal opacity on a chest X-ray. A barium swallow study may reveal varying degrees of compression on the oesophagus and a rare luminal communication, as in the diverticular type. CECT scan of the thorax with oral contrast is the gold standard investigation of choice.[12] ODC usually presents as a homogenous lesion with low attenuation and a smooth border [Figure 3a and b].[1221] The oral contrast could demonstrate any luminal communication, if present, in tubular or diverticular subtypes. All patients in our series had a CECT scan of thorax with oral contrast done, which helped in the diagnosis and planning of surgery.

Figure 3

Contrast-enhanced computed tomography scan of the thorax (a) axial and (b) coronal images, showing a well-defined cystic lesion in the posterior mediastinum (yellow arrow), arising from the right lateral wall of the distal third of the oesophagus. (c) Upper gastrointestinal endoscopy showing a submucosal bulge in the lateral wall of the oesophagus with normal overlying mucosa (yellow arrows). (d) Endoscopic ultrasound showing a well-defined, hypoechoic, cystic lesion arising from the oesophagus (yellow arrow)

UGI endoscopy often shows a normal mucosa, like in 75% of our patients.[1] Abnormal findings noted may be in the form of a sub-mucosal bulge [Figure 3c], extrinsic compression or rarely a fistulous opening.[1417] Endoscopic differential diagnoses include a gastrointestinal stromal tumour, leiomyoma or extrinsic compression due to a variety of mediastinal pathologies such as cysts, lymph nodes or tumours.[1] Endoscopy can also rule out an oesophageal malignancy and assess the degree of luminal narrowing due to compression by the cyst and the cyst’s relationship to the oesophagogastric junction (OGJ).[22]

EUS also plays a vital role in the initial assessment.[117] Five patients in our series had EUS. All the cysts were hypoechoic with the classical two-layer muscle pattern [Figure 3d]. One of the cysts was multiseptate, and none had a demonstrable cartilaginous component. There were no solid areas within any cyst. Features such as the proximity of the cyst to the oesophagus, presence of dual muscle layer and absence of cartilage, help in differentiating an ODC from a bronchogenic cyst.[23] The muscular layer of the cyst can often be seen in continuity with the muscularis propria of the oesophagus. The cyst may be anechoic if the content is mucoid, or heteroechoic with anechoic areas if blood or pus is present.[117] EUS-guided FNAC of the cyst fluid is not required to plan the treatment, and it may lead to complications such as rupture or infection.[11016] The rate of infection following EUS-guided FNAC can be as high as 14%.[1] However, it may be performed in lesions where the imaging is atypical or suspicious of malignancy.[1417] FNAC, if mandatory, is best performed with an appropriate antibiotic cover.[14] Although two patients in our series had EUS-guided FNAC before being referred to our surgical unit, the cytology did not provide any specific diagnosis. Thus, EUS-guided FNAC could have been avoided in these patients in the absence of atypical features or suspicion of malignancy in the EUS.

With time, all the cysts grow in size and may develop complications.[51822] Hence, surgical resection is advocated for all adult ODC cases.[612] Complete excision carries the least rates of recurrence.[18] The various factors to be considered in pre-operative planning are the age of the patient, comorbidities, presence of complications, size and location of the cyst, its relationship to the adjacent structures, type of the cyst, the presence of its communications with the oesophageal lumen and its distance from the OGJ.[5615222425]

Traditionally, majority of the thoracic ODC were operated on through a posterolateral thoracotomy.[612] However, they could be managed safely and effectively with minimally invasive approaches such as VATS and robot-assisted thoracoscopic surgery.[567891018222426] There are reports of ODC in the lower oesophagus managed by transhiatal laparoscopic or robotic approach.[1622272829] Intra-abdominally located cysts may be managed by a laparoscopic approach.[132530] The cysts located in the cervical oesophagus are removed by a transcervical approach, with care to preserve the recurrent laryngeal nerve.[12] Compared to open procedures, the VATS approach is associated with shorter periods of chest tube drainage, hospital stay and lower rates of perioperative complications.[561315]

The decision on a single- or double-lumen endotracheal tube depends on the size, location and extent of the cyst. Because majority of the cysts are located in the lower oesophagus, they could be adequately accessed and excised with single-lumen endotracheal tube ventilation, not requiring a complete collapse of the lung on the operating side. Lateral decubitus positioning is preferred in the case of thoracic oesophageal cysts.[12] The side of the approach is determined by the location and extent of the cyst.[15] The right-sided VATS approach is the more common approach [Table 3]. However, cysts located predominantly in the left chest may be easily approached through a left-sided VATS.[510] In our series, three patients had cysts located in the left posterolateral wall of the lower oesophagus and hence, they were successfully excised through a left-sided VATS approach [Table 2]. In the remaining three cases, the cysts were excised through a right-sided approach. Three-port thoracoscopic access is often adequate, as described in various reports.[5618] The ports’ position is adjusted according to the location and extent of the cyst to ensure adequate access and triangulation. Careful dissection of the cyst all around without rupture and preservation of the muscular layer of the oesophagus are the keys to a successful surgery.[1518] In addition to avoiding injury to the mediastinal structures, phrenic and vagal nerves have to be identified and preserved.[591218] Deliberate decompression of the cyst may be done to make the manipulations easier.[5615] Incomplete excision may lead to recurrences.[121524] There is no convincing evidence that rupture and spillage of the cyst’s contents lead to recurrence.[5615] In our series, there were two cases of intraoperative rupture. Both patients were asymptomatic on follow-up.

Table 3

Published literature on minimally invasive surgery for adult oesophageal duplication cyst

Authors (year)	Number of cases	Age/gender	Location of the cyst in the oesophagus	Cyst size (cm)	Approach	Technique of excision	Is resection complete?
Surendran et al. (2020) (current series)	6	38±4.4 years*/female:male - 4:2	Mid-thoracic - 2Lower thoracic - 4	5.7±2.02*	Right VATS - 3Left VATS - 3	Enucleation - 2Partial resection and cauterisation of the mucosa - 1Endostapler - 3	Yes - 5No - 1
Mori et al. (2020)[25]	1	64 years/female	Intra-abdominal part/OGJ	7.0	Laparoscopy	Enucleation	Yes
Darwish et al. (2019)[5]	1	35 years/male	Lower thoracic - right side	3.0×3.5×4.0	Left VATS	Partial excision and stripping	Yes
Jmv et al. (2018)[16]	1	45 years/female	Lower thoracic - left side	4.6×4.3×4.2	Laparoscopic transhiatal	Enucleation	Yes
Huang et al. (2015)[13]	1	20 years/female	OGJ	13.8×9.6×8.5	Laparoscopy	N/M	N/M
Al-Riyami and Al-Sawafi (2015)[7]	1	24 years/male	Lower thoracic - right side	3.7×2.3×1.5	Right VATS	N/M	Yes
Watanobe et al. (2015)[27]	1	50 years/male	Lower thoracic - right side	3.0×3.5×0.6	Laparoscopic transhiatal	N/M	Yes
Castelijns et al. (2014)[30]	1	20 years/male	Intra-abdominal part/OGJ	3.0×3.0×2.5	Laparoscopy	Endostapler	Yes
Kozu et al. (2014)[8]	1	47 years/female	Lower thoracic	2.5	VATS†	N/M	Yes
Lu et al. (2012)[28]	1	22 years/male	Lower thoracic	6.6×6.4×6.0	Laparoscopic transhiatal	Aspiration and enucleation	Yes
Takemura et al (2011)[9]	1	21 years/female	Mid-thoracic - left side	3.5×3.5	Right VATS	Endostapler	Yes
Ruiz-Tovar et al. (2010)[26]	1	25 years/male	Lower thoracic	4.0×5.0	Right VATS	Enucleation	Yes
Kang et al. (2008)[6]	1	53 years/female	Mid-lower thoracic - right side	3.0	Right VATS	Endostapler	Yes
Zdenek et al. (2007)[29]	1	54 years/female	Intra-abdominal part	10×4×4	Laparoscopic transhiatal	Partial resection	No
Herbella et al. (2006)[10]	2	30 years/female35 years/male	Lower thoracic - posteriorLower thoracic - right side	N/M	Left VATSLeft VATS	EnucleationEnucleation	Yes
Ringley et al. (2006)[22]	1	23 years/female	Lower thoracic - right side	2.1×2.2	Robot-assisted transhiatal	Enucleation	Yes

*Values expressed in mean±SD, †Side of the VATS not mentioned. ODC: Oesophageal duplication cyst, VATS: Video-assisted thoracoscopic surgery, OGJ: Oesophago-gastric junction, N/M: Not mentioned, SD: Standard deviation

Damage to the mucosa of the oesophagus is to be carefully avoided during the dissection, and if breached accidentally, it should be repaired primarily.[12] In our series, there were two cases of a focal mucosal breach during the dissection, and both were suture repaired. Enucleation is the preferred method of excising these cysts [Table 3]. In the cases where the cysts are densely adherent to the oesophageal wall, there is a high risk of inadvertent injury to the oesophageal mucosa during attempts at enucleation.[561027] In such cases, a partial resection may be performed and an attempt may be made to strip the residual mucosa off the contiguous oesophageal wall. If this is also not feasible, the mucosa of the residual wall should be cauterised to prevent recurrences and a rare future malignant transformation.[15] A laparoscopic stapler technology may also be safely used to achieve complete resection of a closely adherent cyst, avoiding oesophageal mucosal injury.[69] The stapler has to be applied in the final steps of the resection. It is applied longitudinally, parallel to the oesophageal wall, away from the cyst wall.[6] This technique was performed in three patients in our series [Figure 1]. We were able to achieve complete excision of the cysts using this technique in these patients. A similar technique has been employed by other authors with favourable outcomes.[6930] Intraoperative endoscopy may help ascertain the integrity of the lumen and the repair.[691218] It was used only in two of our patients who had a mucosal injury during the dissection. A routine post-operative oral contrast study is not required. It was performed only in two of our patients who had mucosal injury repaired intraoperatively. Both studies were normal. In our series, there was one oesophageal staple line leak in a patient who did not have an obvious mucosal breach intraoperatively and hence did not have an intraoperative endoscopy or a post-operative oral contrast study. Whenever possible, the approximation of the defect in the muscular layer of the oesophagus is recommended.[61831] An increased incidence of post-operative complications and pseudo-diverticula was found in children if the oesophageal muscle layer is left unapproximated.[53132] The muscular defect was closed in all our patients except in one where there was a significant loss of muscle fibres, for fear of causing luminal narrowing. Specimens could be extracted via a mini-thoracotomy using an Endo bag. A larger cyst may be decompressed before its extraction.[12]

Gastro-oesophageal reflux disease (GORD) can result following the resection of cysts located close to the OGJ.[3102531] The alteration in the lower oesophageal sphincter anatomy and damage to the vagal nerve may be the possible causes. The addition of fundoplication and crural repair may help reduce the incidence of post-operative GORD in this situation. This is done easily when the cyst excision is performed by a transhiatal approach.[25]

A comparison of our study with that of published literature on MIS for adult ODC is provided in Table 3.

Endoscopic management of ODC has been tried in a few selected cases. Because ODC is rare, guidelines have not been formulated to select the appropriate patient for this technique of management. A cyst localised to the submucosal layer and not involving the deep muscular layers may be an ideal case for this approach. The various techniques described include endoscopic fenestration, endoscopic submucosal dissection with a dual-knife and anhydrous alcohol spray, snare and electrocautery.[333435]

Histopathological confirmation of the diagnosis is mandatory. The presence of a dual smooth muscle layer in the wall and a gastrointestinal mucosal lining is characteristic of ODC. The mucosa may be lined by a variety of epithelium – squamous, columnar, cuboidal, pseudostratified or ciliated. Any evidence of dysplasia or invasive cancer has to be looked for.[36]

Our study is limited by the retrospective nature and its inherent bias. Follow-up data were also limited, despite our attempts to contact the patients post-operatively because most of our patients are from remote places.

CONCLUSION

ODC is an uncommon condition in the adult population. Surgical excision is advocated in all adult ODC cases, for the alleviation of symptoms, and to avoid complications. We assert that MIS by VATS is a safe and effective method for treating this rare benign condition with acceptable morbidity. This should be the preferred approach when expertise is available. Technical details have to be individualised based on the patient and cyst characteristics.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.