British Journal of Radiology 74 (2001),891-900 © 2001 The British Institute of Radiology
The role of oesophageal stenting in the non-surgical management of oesophageal strictures
S H Lee, MBBS, FRCS(Ed), FRCR
Department of Radiology, Manchester Royal Infirmary, Oxford Road, Manchester M13 9WL, UK
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Abstract
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The role of oesophageal stenting continues to evolve, with several new stents currently on the market. These stents possess anti-reflux valves, internal plastic coatings and retrievable threads. In patients with malignant dysphagia, management should ideally take place within multi-disciplinary teams such that accurate tumour staging occurs prior to treatment. Multi-modality therapy can not only improve dysphagia and response rates but may also improve survival. Several non-surgical palliative techniques are available to recanalize malignant obstruction, including oesophageal stenting. Other therapeutic modalities include the use of endoluminal laser therapy, photodynamic therapy, argon beam and bipolar electrocoagulation, ethanol injection and intracavity brachytherapy. Their use often depends on local availability and expertise. Although the initial costs of metal stents are high, the overall costs compare favourably with other forms of palliative therapy that often require multiple procedures with repeated inpatient hospitalization. Treatment of refractory benign strictures with oesophageal stents remains uncommon and several recent reports using retrievable stents appear to improve outcome, although more work is required in this area.
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Introduction
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Oesophageal intubation for the palliation of dysphagia from malignant oesophageal obstruction has been practised for over a hundred years. In 1959, Celestin [1] described the palliation of oesophageal malignancy with a plastic endoprosthesis introduced at laparotomy. In the 1970s, Atkinson [2] introduced an endoscopically inserted plastic prosthesis, with a much reduced complication rate. The internal diameter of these stents was small (10–12 mm), resulting in many patients having difficulty in resuming a normal diet. They had a relatively high complication rate (up to 36%), mainly due to oesophageal perforation, with a procedure-related mortality rate of between 2% and 16% [3]. Plastic stents have been superseded by the newer range of metallic self-expanding stents that are safer and easier to place [4–10]. Nevertheless, some series report little difference in the degree of palliation from dysphagia between plastic and metal stents [4, 11], although the complication rates with metallic stents are significantly lower.
The first description of the endoscopic placement of an expanding metallic spiral stent was made by Frimberger in 1983 [12]. There are currently at least eight different types of metallic stent on the market, both covered and uncovered, some of which have anti-reflux valves [13, 14]. These newer self-expanding metallic stents are inserted using small calibre delivery systems and often do not require pre-dilatation. They are primarily used to palliate symptoms of dysphagia in patients with inoperable oesophageal cancer. Other indications include anastomotic recurrence following surgery and secondary tumours within the mediastinum causing extrinsic oesophageal compression [4, 15–37]. Most large series use covered stents to treat tracheo-oesophageal fistulae and oesophageal perforation [16, 17, 21, 28, 33, 37, 38], with success rates of 80–100%. Stent insertion to treat fistula and/or perforation may not preclude further treatment with either chemoradiotherapy or more definitive surgery at a later date. Placement of large bore diameter stents (20–25 mm) may be necessary to adequately cover fistulae or perforation in patients following attempted recanalization of malignant strictures. To ensure adequate anchorage of the stent in these circumstances, a temporary plastic balloon-expandable oesophageal stent (Wilson–Cook) placed endoscopically may be preferable to a metallic stent.
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Patient selection
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Stents are used primarily in patients with malignant oesophageal obstruction. Other indications are:- Anastamotic tumour recurrence following surgery (Figure 1
).
- Primary or secondary tumours within the mediastinum causing extrinsic oesophageal compression (Figure 2) [30].
- Tracheo-oesophageal fistulae.
- Oesophageal perforation, which is usually iatrogenic, from direct endoscopic trauma or following stricture dilatation.
- Treatment of symptomatic malignant gastro-oesophageal anastomotic leaks [32].
- Benign oesophageal strictures (see below) [39, 40].
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Figure 1. Covered Gianturco-Z stent placed across an anastomotic recurrence following previous gastrectomy.
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Figure 2. Covered Gianturco-Z stent in a patient with carcinoma of the lung causing extrinsic oesophageal compression.
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Management of all such patients should take place within multi-disciplinary teams to determine the best form of treatment in individual cases. Conventional treatment for advanced oesophageal malignancy includes surgery, radiotherapy and/or chemotherapy together with oesophageal stent placement. Several other techniques are also available to recanalize malignant oesophageal strictures, the most widely used being laser therapy. Oesophageal stent placement in biopsy-proven malignant disease should only be performed following accurate radiological staging of the primary tumour and when other potentially curative therapies have been deemed inappropriate or have failed.
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Oesophageal carcinoma
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Oesophageal carcinoma is the seventh most common malignancy worldwide, with approximately 6000 new cases per annum in England and Wales, and a 6% overall 5-year survival (1994 Office for National Statistics). The incidence is increasing rapidly in the Western world mainly due to adenocarcinoma of the lower third of the oesophagus and gastro-oesophageal junction, which usually arises from areas of Barrett's metaplasia. Unfortunately most patients are no longer curable at the time of presentation with dysphagia as the oesophageal lumen has often reduced by at least 50–75% of its normal calibre. Patient's symptoms can be assessed using a 4 or 5 point dysphagia scoring system:- 0=normal diet/no dysphagia
- 1=ability to swallow semi-solids and liquids
- 2=ability to swallow liquids only
- 3=difficulty in swallowing liquids and saliva
- 4=total dysphagia (some series do not include this score)
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Staging
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Accurate pathological staging using the TNM classification is essential prior to treatment of oesophageal carcinoma (Table 1). Stage 0, I and II tumours are considered potentially curable by resection, whereas stage III tumours are rarely resectable for curative intent and stage IV tumours are usually incurable and inoperable (Table 2).
Imaging
The key prognostic features in oesophageal carcinoma are the depth of tumour infiltration through the oesophageal wall and the presence of nodal metastases. The two primary staging modalities are CT and endoscopic ultrasound (EUS). CT is limited in its ability to differentiate T1 and T2 tumours and tends to underestimate the tumour stage in approximately 40% of patients. CT also has difficulty in determining the presence of nodal metastases, with an accuracy of between 55% and 63% [41]. Lymph nodes greater than 1 cm in the short axis diameter are usually said to be positive for tumour, whereas lymph nodes beneath the diaphragm are deemed positive if greater than 8 mm in size [42].
EUS has an 80–85% accuracy in T staging and a 70–75% accuracy in N staging [41]. EUS can identify small lymph nodes measuring 4–5 mm in size, and nodal biopsy is possible with some probes, enabling a reasonably accurate assessment of tumour resectability in stage I and II disease. Unfortunately, EUS has difficulty distinguishing fibrosis and inflammation following neoadjuvant therapy from the presence of residual tumour. Tight tumour stenosis may prevent passage of the endoscope, although mini-probes are now available. Other diagnostic modalities used in staging oesophageal cancer include MRI, positron emission tomography (PET), thoracoscopy and laparoscopy. MRI is not superior to CT in predicting tumour resectability [43]. PET scanning using 18F-fluorodeoxyglucose is highly sensitive in the detection of oesophageal cancer, including T1 lesions, but is poor in identifying local node involvement [44].
Multi-modality treatment
Surgical resection is the primary treatment for operable oesophageal cancer and is attempted in 10–30% of cases, with a 5-year survival of between 10% and 20%. In early stage I and II disease that is node negative, surgical resection may increase 5-year survival to around 40% [45]. However, most patients have incurable stage III or IV disease at presentation. An attempt to improve survival following surgery is being made using neoadjuvant combination chemoradiotherapy. There appears to be a survival benefit from such combination treatment at the expense of increased morbidity from acute drug toxicity and a slightly increased surgical mortality. For non-surgical or non-curable patients and those with local tumour recurrence there are a number of other therapeutic options. The aims of palliative treatment are two-fold: (a) to relieve dysphagia and (b) to attempt to improve survival. This includes the use of radiotherapy alone or combination chemoradiotherapy together with local treatment for relief of dysphagia [46, 47]. Each treatment plan is tailored to the individual patient according to (a) tumour stage, (b) symptomatology, (c) age and overall health of the patient and (d) the patient's needs and wishes.
Non-surgical palliative techniques include the following.
Thermal ablation
Endoluminal laser therapy
This therapy uses neodymium yttrium–aluminium–garnet (Nd:YAG) and is probably the most widely available first-line tool used to ablate obstructing tumours, especially in patients with short strictures or where there is a large endoluminal tumour bulk. Palliation can be achieved in up to 80% of patients. Multiple treatment sessions, every 4–8 weeks, are often required. However, palliation in one randomized study was not as good as that achieved with metal stents [20]. There was no difference in dysphagia scores between laser therapy, plastic stents and metal stents in a study by Gevers et al [11]. A third comparative study by Konigsrainer et al [36] showed little difference in palliation and outcome between metal stents and laser combined with radiotherapy. Approximately 20% of patients require oesophageal dilatation to enable passage of the endoscope through the tumour, which can result in perforation. This usually responds to conservative management but may require more invasive treatment using a covered oesophageal stent. Significant haemorrhage may also occur. The overall morbidity and mortality rates are reported to be between 5% and 9% [3]. The combination of external beam radiotherapy with laser treatment appears to cut down the number of repeated laser treatment sessions required to maintain palliation [48]. It has also been suggested that laser therapy should be the first choice in patients with a short life expectancy [11].
Photodynamic therapy (PDT)
An intravenously injected porphyrin photo-sensitising agent (sodium porfiler/photofrin) selectively concentrates in malignant tissue, which can then be destroyed by the application of laser light. Dysphagia palliation is similar to or better than that achieved with laser treatment in up to 90% of patients [49–51]. There is also a lower perforation rate, as pre-dilatation is not necessary. Limitations of PDT include the high cost of equipment and the shallow depth of light penetration into the tumour, often requiring repeated treatment. Side effects from the injected photosensitising agent are common and patients have to avoid direct sunlight.
Argon beam or bipolar electrocoagulation therapy
This involves direct tumour coagulation under endoscopic vision. The oesophageal stricture requires pre-dilatation so that the coagulation probe can be passed distally into the tumour. Effective palliation can be achieved in over 80% of patients [52]. Complication rates are similar to those with laser treatment, mainly due to perforation in up to 8% of cases. The equipment is relatively cheap but multiple treatment sessions have been needed in 26% of patients.
Ethanol injection
Absolute alcohol is injected into the tumour under direct endoscopic visualization and causes tumour necrosis. Pre-dilatation is often required and in one series the stricture could not be traversed in 18% of patients. Complication rates are lower than those with other thermal ablative modalities, yet despite good early response to treatment there is a high relapse rate. Experience using this technique remains limited [53–55].
All these ablative techniques can also be used to treat tumour ingrowth and epithelial hyperplasia in patients with recurrent dysphagia following stent placement.
Intracavity brachytherapy
This can be used either alone or in combination with external beam radiotherapy. Palliation of dysphagia can be achieved in 75–95% of patients [56]. There is a high incidence of oesophagitis and stricture formation, but there is a recent report of prolonged median survival of up to 35% at 12 months in patients receiving high dose brachytherapy, which is greater than other forms of local palliative treatment.
External beam radiotherapy
This can be used either as palliation or as definitive treatment for oesophageal carcinoma [57]. Squamous cell carcinoma is usually more sensitive than adenocarcinoma to external beam radiotherapy treatment but dysphagia often deteriorates in the first week following treatment. Adjuvant treatment with chemotherapeutic agents can also be administered, which often gives better control of local disease as well as treatment of distant metastases.
Combination chemoradiation
This not only palliates dysphagia in up to 90% of patients but also gives a 50% response rate in patients with advanced malignancy [58].
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Oesophageal stents in benign disease
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The majority of benign strictures treated in the Western world are due to acid reflux. Most can be treated successfully by endoscopic dilatation using balloon catheters or bougies. Radiologically guided balloon dilatation is an alternative. Other less common causes of benign oesophageal stricture formation are surgical anastomosis, radiation fibrosis, following injection sclerotherapy and corrosive strictures. Oesophageal stent placement is often a last resort if strictures are refractory to conventional treatment and surgery is contraindicated. Corrosive strictures are notoriously difficult to treat as they are often long and multiple. The literature shows mixed results from the use of metallic stents in a limited number of patients [35, 39, 59–61].
Song et al [40] have the widest published experience and describe the use of a Nitinol covered retrievable stent in 25 patients, 22 of whom had corrosive strictures. They aim to leave stents in situ for up to 8 weeks only and then remove the stent. This is to ensure enough time for the strictures to heal and hopefully prevent late stricture recurrence. They claim a 48% improvement of dysphagia with no further treatment during a follow-up period of 2–25 months, with a mean of 13 months. Fan et al [62] used a retrievable, coated Nitinol stent in 24 cases of benign stricture disease, most of which were the result of previous surgery. Stents were left in situ for between 1 month and 2 months only, and dysphagia was effectively palliated in all patients. One potential problem is stent migration, which occurred in 3 out of 10 patients in the series by Fiorini et al [63].
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Currently available metallic stents
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Stents are made either from Nitinol, which is a titanium–nickel alloy, or stainless steel; they are compressed into a small calibre introducer system (10–16 F). Nitinol has thermal shape memory characteristics that allow the stent to expand at body temperature. Most stents have a proximal flared end to help prevent distal migration.
Stents are available in an uncovered bare form or with a plastic coating on the inside and/or the outside of the stent. The advantage of uncovered stents is that they are less liable to migration, especially across the cardia. However, uncovered stents have a higher incidence of tumour in-growth and most stents now placed are of the covered type. Stents are usually inserted under fluoroscopic guidance, which allows for accurate positioning, but endoscopy can also be used. Endoscopy alone may not accurately define the distal aspect of the tumour margin. Commercially available stents are:
- Gianturco-Z stent (Cook UK Ltd) (Figures 1 and 2
). This is made from stainless steel and apolyethylene covering with barbs on the outside or uncoated flared ends to prevent migration. This stent is also available with ananti-reflux distal valve for positioning across the cardia (Figures 3 and 6c) [6, 10, 17, 21, 26].
- Ultraflex (Boston Scientific Ltd). This stent is made from a knitted Nitinol mesh and is available in both uncovered (Figure 4a) and covered (Figure 4b) forms [18–20, 22, 33]. It has the weakest radial force but greater flexibility. These stents may be best for tortuous and upper third strictures.
- Flamingo Wallstent (Boston Scientific Ltd) (Figure 4c). This is a tapered stent made from a braided stainless-steel alloy and is covered on the inside only [35]. It is designed for use across the cardia only, as its conical shape may prevent distal migration.
- Wallstent (Boston Scientific Ltd) (Figure 4d). This stent has an internal silicon-based covering with flared ends and is made from a stainless-steel alloy woven into a tubular mesh [16, 20, 22, 28].
- Esophacoil (Kimal plc) (Figure 5). This stent is uncovered and made from a single Nitinol filament [27, 31]. It demonstrates significant shortening on release but may be retrievable in some patients.
- FerX-Ella stent (Radiologic Ltd) (Figure 6a). This stent is made from stainless steel and is covered with polyethylene internally and externally, which also projects distally to act as an anti-reflux valve [14].
- Choo Stent (Diagmed) (Figure 6b). This is a polyurethane-covered stent made from Nitinol and has a retrievable attached thread [40]. These stents also come with an internal distal anti-reflux valve.
- Memotherm (C.R. Bard) (Figure 6d). This is a flared Nitinol stent with an internal and external PTFE covering [28].
- Song stent, which is a modified Gianturco Z-stent made from stainless steel with a polyurethane covering [34]. This stent has also been made in a retrievable form with a single thread attached to the tubular wire configuration [39].
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Figure 3. Anti-reflux Gianturco-Z stent placed across distal oesophageal adenocarcinoma (arrow). Contrast medium is seen passing through the "windsock" anti-reflux valve (arrowheads).
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Figure 4. (a) Uncovered Ultraflex stent, (b) externally covered Ultraflex stent, (c) Flamingo stent and (d) internally covered Wallstent.
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Figure 6. (a) Covered FerX Ella anti-reflux stent, (b) covered retrievable Choo stent, (c) covered Gianturco anti-reflux stent and (d) covered Memotherm stent.
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Chan et al [64] demonstrated that the Esophacoil stent was the strongest stent in withstanding compressive and angulation forces when compared with the Wallstent, Ultraflex, Song and Gianturco stents. The Ultraflex stent demonstrated the weakest expansile force but withstood angulation forces better than the Song and Gianturco stents. Whether or not this knowledge will affect the selection of an appropriate stent for each particular patient has yet to be demonstrated.
The cost of these stents varies from £750.00 to £1000.00, depending on length and manufacturer. The internal diameter of most stents is 18–22 mm when fully expanded and they have flared ends to prevent slippage. Pre-dilatation of the oesophageal stricture is not always necessary owing to the small size of the stent introducer systems, but may allow more accurate stent positioning, especially if endoscopy is used. More than one stent may be necessary to cover long strictures and at least 1 cm of stent should be placed above and below the stricture to avoid early tumour overgrowth. Post-stent balloon dilatation is not always necessary and may be reserved for patients with persistent dysphagia where the stent has not fully expanded. If proximal or distal stent migration occurs, then a second overlapping stent can be inserted, usually of the uncovered type. Otherwise, an attempt at endoscopic extraction may be possible.
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Stent selection
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It is advisable to use an uncovered stent, e.g. a Flamingo or a Gianturco stent, at the cardia to reduce the risks of distal migration. Gastro-oesophageal reflux occurs in most patients when the cardia has been crossed [19]. This may lead to aspiration, and anti-reflux medication should be given prophylactically in all such cases. However, there are three new anti-reflux stents (Gianturco, FerX-Ella and Choo stents) on the market that are currently being evaluated and these may become the stent of choice across the cardia.
Stents positioned in the upper third of the oesophagus may result in a persistent foreign body sensation, especially if the cricopharyngeus is crossed. Endoscopy during stent placement is useful to identify the level of cricopharyngeus. These symptoms may be difficult to treat. However, some groups have achieved good results [65–67] and the more flexible Ultraflex stent may be best for such high strictures.
The retrievable covered stents (Choo and Song stents) may become the stent of choice in the management of refractory benign strictures [39, 40].
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Early complications
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Early chest pain occurs in up to 100% of patients [19] but prolonged chest pain occurs in less than 13% of patients. Chest pain may be more severe in patients with high strictures and when using large diameter stents [15]. Major complications such as bleeding, perforation, aspiration, fever and fistula occur in 10–20% of patients [11, 15, 17, 19]. Procedure-related mortality is uncommon although one study reported a 7% mortality due to haemorrhage and aspiration [20]. 30-day mortality is reported to be as high as 26% [34]. The incidence of stent migration for uncovered stents is low (0–3%), rising to 6% for stents placed at the cardia [20, 24]. A higher rate of stent migration, between 25% and 32%, is reported for placement of covered stents, especially when positioned across the cardia [13, 19, 24]. This may require multiple stent insertion [17, 18]. Covered stents should be used to cover tracheo-oesophageal fistulae and perforations. Tracheal compression, although uncommon, has been reported when treating upper third strictures [68]. Complication rates following stent insertion were significantly increased owing to oesophageal rupture in a small series of 11 patients who had adjuvant treatment with either dilatation and thermal ablation or PDT with brachytherapy within 1 week of stent placement [69]. Radiotherapy pre- and/or post stent placement also increases the risk of stent migration [70].
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Late complications
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Re-intervention following stent placement is common. This is predominantly due to tumour in-growth with uncovered stents (8–35% of cases). However, tumour in-growth is rare with covered stents [18, 20, 24]. Recurrent dysphagia as a result of stent overgrowth has been reported in up to 60% of patients when followed up for long enough [71], although many of the stents used were uncovered in this retrospective study. Overgrowth may not always be due to spread of tumour but may result from benign epithelial hyperplasia, granulation tissue and fibrosis in up to half of these patients [71]. Treatment of recurrent stenosis may be satisfactorily carried out with either laser therapy, PDT, argon beam therapy, alcohol injection or re-stenting. Other late complications include haemorrhage (3–10%), oesophageal ulceration (7%), perforation or fistula (5%), stent torsion (5%), stent migration (5%) and stent fracture (2%).
Wang et al [72] found that life-threatening complications (massive haemorrhage, fistula, perforation and tracheal compression) were more common in patients with stent placement in the proximal third of the oesophagus, with the Ultraflex stent having fewer overall complications compared with the Gianturco stent or Wallstent.
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Survival
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Mean time to death following stent placement is reported to be between 77 days and 168 days [5, 36]. One series reported a prolonged survival time (median 318 days) following stent placement in patients receiving concurrent radiation and chemotherapy [69].
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Conclusion
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Stenting of malignant oesophageal obstruction and refractory benign strictures continues to evolve with the introduction of newer anti-reflux [13, 14], anti-migration stents with an internal plastic coating [73] and with retrievable stents [39]. Most patients (75–90%) resume a near normal diet after stent placement, with a mean reduction in dysphagia score of around 1.8. It was originally hoped that stenting malignant strictures would be a one-stop procedure but it is now apparent that recurrent stricturing occurs in up to 60% of patients [71] and often requires further intervention. Survival may be increased by the use of adjuvant chemoradiotherapy or endoluminal brachytherapy either before or after stent placement, although this may result in more stent-related complications. Further studies are needed in this area.
The initial cost of an expandable metal stent is high, but overall costs are favourable when compared with other forms of palliative therapy that often require repeated procedures resulting in a prolonged in-patient hospital stay [4, 21, 74]. The determining factor as to which method is used to palliate patients with advanced oesophageal malignancy often depends on local expertise and availability of equipment. Larger comparative studies between the different metal stents may demonstrate which stent has the lowest complication rates. It must be stressed that placement of these stents should only take place following accurate tumour staging and patient evaluation within multi-disciplinary teams.
Received for publication January 9, 2001.
Accepted for publication July 30, 2001.
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Abstract
Introduction
