Surgery for cancer of the oesophagus

Acknowledgement

This chapter in the sixth edition was written with Professor Mike Griffin and I am grateful to him for those parts of the chapter which I have kept in this edition.

Introduction

Despite advances in surgical technique and perioperative care, oesophageal cancer remains one of the most challenging conditions confronting the surgeon. The principles of surgery are to achieve complete resection of the tumour and surrounding lymph nodes, and to perform a reconstruction with the optimal functional outcome and the minimum morbidity and mortality. This chapter discusses these principles, focusing on primary tumour resection, the rationale for lymphadenectomy, technical aspects of different surgical approaches including minimally invasive surgery, methods of reconstruction and anastomosis, management of postoperative complications, and outcomes of treatment.

In the UK, 70% of patients with oesophageal cancer have adenocarcinoma of the lower oesophagus or oesophagogastric junction. This chapter includes the surgical management of adenocarcinoma of the lower oesophagus and the cardia (Siewert type 1 and 2), which is frequently staged and treated as oesophageal cancer as well as squamous carcinoma. Subcardial adenocarcinoma (Siewert type 3) is covered elsewhere ( Chapter 6 ).

Unfortunately, as a result of poor fitness and/or advanced disease, only 25–40% of patients with oesophageal cancer are suitable for potentially curative treatment. While radical treatment for adenocarcinoma of the oesophagus is multidisciplinary, surgery remains the primary mode of therapy. Outcome is strongly stage dependent; early tumours have excellent results with surgery alone ( Chapter 7 ), but the majority who have transmural and/or node-positive tumours benefit from multimodality therapy, combining surgery with neoadjuvant chemotherapy, or chemoradiotherapy ( Chapter 8 ). Surgery continues to have a key role in the primary treatment of squamous carcinoma, with outcomes similar to definitive chemoradiotherapy, and as a salvage procedure following failed oncological treatment. The multidisciplinary team must exercise judgement for each individual patient based on the site, histology, and stage of the tumour, and patient fitness and wishes.

Surgical pathology

Tumour site and histology are both crucial factors; squamous cell carcinoma arising in the cervical and thoracic oesophagus and adenocarcinoma arising in the thoracic oesophagus and cardia differ in their mode of spread and response to therapeutic modalities. There is also variation in the pattern of lymph node spread and proximity to vital structures according to the precise tumour site.

Surgical anatomy

It is important that the anatomical divisions of the oesophagus are described to understand the surgical procedures adopted for tumours at each site ( Fig. 5.1 ).

Figure 5.1, Anatomical regions of the hypopharynx, oesophagus, and gastric cardia.

Patient selection

A detailed preoperative assessment to accurately evaluate tumour stage and surgical risk is vital to a successful outcome (see Chapter 3, Chapter 4 ). It is now established that enhanced recovery programmes and perioperative care pathways result in improved clinical outcomes and reduced length of stay, and are cost effective. Elements of such programmes include: preoperative assessment, planning and preparation before admission (prehabilitation), reducing the physical stress of the operation, using a structured, goal-oriented approach to recovery, and, above all, early mobilisation.

Patients and their families should be counselled in detail about treatment options, paying particular attention to the expectations, results, and limitations of surgery. It is crucial that a trained clinical nurse specialist in oesophagogastric cancer oversees the patient pathway. When UK surgeons and patients were questioned about the most important information to be included in such discussions there were notable differences, with surgeons rating short-term clinical outcomes (technical complications) most highly, while patients prioritised information related to long-term benefits of surgery. A consensus meeting developed the final core information set for surgery for oesophageal cancer ( Box 5.1 ).

Box 5.1

Core information set for surgery for oesophageal cancer

In-hospital milestones to recovery
Rates of open-and-close surgery
In-hospital mortality
Major complications (including re-operation)
Milestones in recovery after discharge
Longer term eating and drinking and overall quality of life
Chances of survival

Principles of oesophagectomy

Surgical objectives

Oesophagectomy should be undertaken only when a potentially curative R0 resection (complete removal of all macroscopic and microscopic cancer) is expected. Unlike some gastrointestinal tumours, including colorectal carcinoma, there is little evidence for resection in the presence of proven distant metastases.

Resection of primary tumour

Accurate preoperative staging information is crucial to guide the optimal surgical approach and procedure. The majority of authors favour a subtotal oesophagectomy to take into account longitudinal spread in submucosal lymphatics for both squamous and adenocarcinoma. There is debate about the length of macroscopically normal oesophagus required to ensure a clear resection margin. In squamous carcinoma this relates primarily to the proximal margin, particularly if there is multifocal disease, which is common, or intramural lymphovascular spread, whereas in adenocarcinoma the distal gastric margin is usually the concern. A 10-cm resection margin is a goal to attain in both directions from the palpable edge of the tumour at surgery, if this is possible . In practice, this can often not be achieved but a minimum clearance of 5 cm should be targeted. When only a short proximal resection margin can be obtained through a thoracic exposure, a cervical phase with near total oesophagectomy must be considered. When there is concern at the time of surgery then a frozen section should be performed. Adenocarcinoma of the lower oesophagus commonly infiltrates the gastric cardia, fundus, and lesser curve. Extensive sleeve resection of the lesser curve and fundus with the formation of a tubular conduit is required to minimise the chance of a positive distal resection margin, particularly for Siewert type 2 tumours.

Circumferential resection margin (CRM) is an independent prognostic factor for oesophageal cancer. A meta-analysis reported rates of CRM involvement of 45% according to the Royal College of Pathologists’ (RCP) definition (tumour less than 1 mm from the resection margin) and 18% according to the College of American Pathologists’ (CAP) definition (tumour at the resection margin). A positive CRM was associated with a worse prognosis regardless of histological subtype, T stage, or use of neoadjuvant therapy. Those positive according to CAP criteria had a worse overall survival.

Radical en bloc resection techniques aim to produce a clear CRM. However, CRM can be influenced by a number of factors other than surgical technique, including case selection, type of neoadjuvant therapy, and histopathological assessment. The potential benefits of extended lymphadenectomy, discussed later, only pertain if the primary tumour has been completely excised (R0).

Resection of lymph nodes

There is no doubt that lymph node involvement and the number of lymph nodes involved are important independent prognostic variables for locoregional recurrence and survival. This was recognised by the RCP use the American Joint Committee on Cancer TNM seventh edition (TNM7), which subdivided the N stage according to the number of involved nodes (N1, 1–2; N2, 3–6; N3, ≥ 7). The Worldwide Esophageal Cancer Collaboration (WECC) has used pooled data from centres that have undertaken radical lymphadenectomy to report in detail the relationship between nodal involvement and survival.

Nodal tiers

Lymph node tiers for oesophageal cancer have been described according to lymphatic drainage of the oesophagus ( Fig. 5.2 ). However, there is confusion in the literature, with terms such as ‘radical en bloc lymphadenectomy’, ‘extended lymphadenectomy’, and ‘two-field lymphadenectomy’ used interchangeably to describe a variety of procedures. It has been proposed that the terminology used to describe the extent of lymphadenectomy should be standardised as follows.

Figure 5.2, Extent of resection and fields of lymph node dissection routinely carried out for cancer of the oesophagus.

Radical lymphadenectomy

One-field lymphadenectomy describes an upper abdominal lymphadenectomy including removal of diaphragmatic, right and left paracardial, lesser curvature, left gastric, coeliac, common hepatic, and splenic artery nodes.

Two-field lymphadenectomy describes removal of the first field along with removal of the paraoesophageal nodes, para-aortic nodes (together with the thoracic duct), and right and left pulmonary hilar, subcarinal, and right paratracheal nodes.

Three-field lymphadenectomy describes removal of the first and second fields along with a neck dissection clearing the brachiocephalic, deep lateral, and external cervical nodes, as well as right and left recurrent nerve lymphatic chains (deep anterior cervical nodes).

Non-radical lymphadenectomy

In this procedure only the nodes in direct proximity to the tumour, the oesophagus, and upper stomach are removed.

As for many solid-organ tumours, controversy persists as to the value of lymphadenectomy in oesophageal cancer. Some authors believe that lymph node metastases are simply markers of systemic disease, while others believe that cure can be obtained in many patients with positive nodes by a radical lymphadenectomy with clear resection margins. ^,

The rationale for lymphadenectomy

The arguments for radical lymphadenectomy are: optimal staging, improved locoregional control, and improved cure rates. Radical lymphadenectomy can also improve dissection of the primary tumour and increase R0 resection rates; for example, en bloc resection of the para-aortic nodes and thoracic duct requires a wider plane of dissection.

Optimal staging

Radical lymphadenectomy certainly allows more accurate pathological staging. ^, Current TNM staging relies not only on identifying positive lymph nodes, but also on how many are found. If an inadequate lymphadenectomy is undertaken, the phenomenon of stage migration means survival will tend to be poorer than that predicted by stage.

Locoregional tumour control

While oesophagectomy should not be undertaken without the potential for long-term survival, locoregional tumour control is an important benefit for those who are ultimately not cured. Radical lymphadenectomy has been associated with prolonged tumour-free survival, resulting from a combination of an increased R0 resection rate and the removal of involved nodes. ^, ^, Locoregional recurrence can be further reduced by neoadjuvant therapy, whether chemotherapy or chemoradiotherapy, with an increase in R0 resection, and fewer positive nodes, associated with improved disease-free and overall survival in randomised trials.

Improved cure rate

It is difficult to demonstrate that radical lymphadenectomy improves cure rates in a randomised controlled trial, and there are few in the literature. ^,

There is an indication from a Dutch randomised trial ^, comparing radical transthoracic and less radical transhiatal resection that patients with a limited number of positive nodes (1–8) had significantly better survival following radical transthoracic oesophagectomy. Node-negative patients did well and those with a higher nodal burden did poorly irrespective of the radicality of surgery.

It has been shown by evaluating the sites of nodal involvement in patients who underwent neoadjuvant therapy and two-field oesophagectomy that long-term survival would have been compromised by limiting the extent of abdominal or mediastinal lymphadenectomy. There is also a rationale for radical lymphadenectomy in patients believed to be node negative at staging, as 20% of these patients will ultimately be found to have lymph node metastases. The role of radical lymphadenectomy in early-stage disease depends on the precise depth of invasion of the primary tumour, with the incidence of lymph node involvement rising sharply with submucosal invasion.

Further evidence in support of radical lymphadenectomy comes from the WECC, who reported on their multi-institution international database of over 4 600 resections in patients who had not had induction therapy. ^, Prognosis was highly dependent on the number of lymph nodes involved; patients with more than three nodes involved had a 50% likelihood of systemic disease and those with more than eight nodes involved had an almost 100% likelihood of systemic disease. Importantly, survival depended not only on the number of nodes involved, but also on how many were removed at resection. The number of lymph nodes removed was the third strongest predictor of survival after depth of invasion and number of nodes involved. This finding has been corroborated by the Surveillance, Epidemiology and End Results (SEER) database. These international studies have recommended a respective lymph node yield of 23 ¹⁷ and 30, ¹⁸ rather than the six nodes proposed for adequate staging in TNM7.

The role of a more extensive three-field dissection in oesophageal cancer is less clear. Five-year survival rates showed no significant difference between two-field and three-field dissection for lower third squamous carcinoma and adenocarcinoma of the oesophagus. Selected patients with squamous and adenocarcinoma of the thoracic oesophagus might benefit from a formal three-field nodal dissection. The potential benefit needs to be balanced against increased morbidity, particularly recurrent laryngeal nerve injury and pulmonary complications.

Summary

There is little justification for oesophagectomy to be performed without an attempt to completely resect the primary tumour with an envelope of surrounding tissue. The majority of patients with oesophageal carcinoma have mediastinal lymph node metastases, and around three-quarters of patients with lower oesophageal tumours have involved upper abdominal lymph nodes. To perform a potentially curative resection for carcinoma in the middle and lower oesophagus, a dissection of upper abdominal and mediastinal lymph nodes is therefore logical. In practice, an infracarinal two-field lymphadenectomy is often performed for adenocarcinoma of the lower oesophagus and oesophagogastric junction.

It is the author’s opinion that a subtotal oesophagectomy with two-field lymphadenectomy is the operation of choice for patients with mid- and lower-third oesophageal cancer and type 1 and 2 tumours of the oesophagogastric junction.

Reconstruction of the oesophagus

Route of reconstruction

Posterior mediastinal

After oesophagectomy, the standard route of reconstruction is the posterior mediastinum. This provides the shortest distance between the abdomen and the apex of the thorax or the neck. Gastric or colonic substitutes are easily passed through the posterior mediastinum after completion of the oesophageal dissection in the thorax. The posterior mediastinal route is the preferred route of reconstruction in the primary surgical excision of oesophageal cancers.

Retrosternal (anterior mediastinal)

The potential space between the sternum and the anterior mediastinum is easily dissected by either blunt finger dissection or the use of a laparoscope through the abdominal and cervical incisions. The tip of an instrument is passed up to the neck in direct contact with the back of the sternum, taking care not to deviate from the midline. A laparoscopic sleeve can aid passage of the conduit from the abdomen to the neck in the retrosternal space. This route is most commonly used for reconstruction when there has been previous sepsis in the posterior mediastinum, such as following emergency treatment of gastric conduit necrosis. Its major disadvantage stems from the angulation of the oesophagus at the thoracic inlet, which can result in an unpleasant sensation on swallowing. When used for a colonic interposition, it is often necessary to resect the head of the clavicle and a small portion of manubrium to limit angulation and accommodate the graft.

Presternal

This is about 2 cm longer than the retrosternal route, which in turn is about 2 cm longer than the posterior mediastinal route. The only indication is when multiple previous reconstructions have compromised the other two routes.

Organ of reconstruction

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