Minimally invasive surgery for esophageal cancer

Authors


Correspondence
John G Hunter, Department of Surgery, Oregon Health & Science University, 3181 SW Sam Jackson Park Rd, L-223A, Portland, OR 97239-3098, USA. Tel: +1 503 494 7758
Fax: +1 503 494 8884
Email: hunterj@ohsu.edu

Abstract

Background: Esophageal cancer is among the most deadly cancers worldwide, and esophagectomy remains the standard of care in trying to cure this. Efforts to decrease the incidence of complications in esophagectomy without compromising the efficacy of the procedure have stimulated interest in minimally invasive esophagectomy (MIE), and a wide variety of MIE techniques have been refined by surgeons at specialized centers worldwide.

Data sources: Systematic PubMed searches identified articles related to MIE technique, complications, and outcomes.

Conclusions: Several techniques have been developed for MIE, none of which has been deemed superior, but as a whole, they represent a safe alternative to open surgery. Available results from case series and comparative studies suggest trends towards improved short-term outcomes with equivalent efficacy but without definitive advantages.

Introduction

With a continued rise in incidence and mortality over the last decade, esophageal cancer is among the most deadly cancers worldwide (1–7). Esophagectomy remains one of the most complex and technically challenging surgical procedures, and historically, it has been associated with morbidity and mortality rates of approximately 40% and 10%, respectively (8). Five-year survival rates following curative resection range from 20% to 40% (9–12). However, surgical resection remains the standard of care, and improvements in technique and care have resulted in better surgical outcomes (13).

Minimally invasive techniques for gastrointestinal surgery have evolved since the early 1990s. Well-known advantages of the laparoscopic approach include decreased morbidity, postoperative pain, and hospital stay, as well as a faster return to normal activity. Efforts to decrease the incidence of complications in esophagectomy without compromising the efficacy of the procedure have stimulated interest in minimally invasive esophagectomy (MIE) (14,15). While the first thoracoscopic esophageal mobilizations were reported in the 1990s (16–19), and the first endoscopic esophagectomy reported in 1995 (20), MIE has been slow to gain widespread acceptance in part due to its technically challenging nature and a lack of strong evidence for improved morbidity and mortality. Large comparative studies between MIE and open esophagectomy are scarce, and there are no randomized studies comparing the two approaches. Nevertheless, a wide variety of MIE techniques have been refined by surgeons at specialized centers worldwide, and the minimally invasive surgical approach has been adapted to the entire spectrum of open esophagectomy techniques.

The optimal approach to esophageal resection for high-grade dysplasia and invasive cancer remains controversial, so it is not surprising that the optimal MIE approach or technique remains under debate. For open esophagectomy, some surgeons favor the transthoracic approach, citing the increased lymph node yield, whereas others prefer the transhiatal approach, which decreases early postoperative morbidity and mortality (12,21–24). Since there is no consensus on the optimal technique, it may be best to tailor the surgical approach based on the patient's disease, operative risk, and expectations. In this review, the various major MIE techniques will be presented, along with the relevant data on efficacy, morbidity and mortality. While there are many different ways to perform the various procedures, each key step will be identified and the differences described.

Types of MIE procedures

Three-field MIE

For patients with invasive cancer of the esophagus, we often employ the three-field technique as it allows for greater clearance of the local disease. This procedure begins with thoracoscopic esophageal mobilization performed with the patient in the left lateral decubitus position. The mediastinal pleura overlying the esophagus is opened, and circumferential dissection of the esophagus and its surrounding lymphatic tissue is performed en bloc from the azygos vein to the level of the diaphragmatic hiatus. Near the thoracic inlet, the dissection proceeds near the esophageal wall to avoid injury to the membranous trachea and recurrent laryngeal nerves. The upper mediastinal and paratracheal lymph nodes are removed. Then, the thoracic duct is indentified, secured with clips, and divided at the level of the diaphragm (Figure 1a). After the thoracic dissection is completed, chest tubes are inserted and the patient is placed in the supine split-legged position.

Figure 1.

 (a) Thorascopic esophageal dissection and mobilization. (b) Laparoscopic gastric conduit creation.

At this point the laparoscopic dissection begins. Briefly, hiatal dissection is performed, the short gastric vessels are divided, the posterior stomach is mobilized, and a Kocher maneuver is performed. The right gastroepiploic arcade is preserved, and the left gastric artery is transected at its base, with care taken to maintain all periesophageal lymphatic tissue en bloc with the operative specimen. Following complete gastric mobilization, a 3–5 cm wide stapled greater curvature gastric tube is created at the beginning of the lesser curve approximately 6 cm proximal to the pylorus (Figure 1b). The cervical esophagus is exposed and divided, and the esophageal specimen is removed through the cervical incision. Finally, a hand-sewn or linear-stapled end-to-side esophagogastrostomy is created between the cervical esophagus and gastric fundus (25).

Transhiatal MIE with or without inversion

Our preference has been to employ transhiatal MIE for patients with benign disease, high-grade dysplasia, or early clinically staged invasive distal esophageal cancers in order to balance oncologic surgical results with the morbidity of the procedure. This procedure commences with laparoscopic gastric mobilization and the creation of neoesophagus, and terminates with cervical specimen removal and anastamosis as in three-field MIE. The key difference from three-field MIE involves the mediastinal dissection of periesophageal lymph nodes; in transhiatal MIE, they are accessed in a narrower field through the hiatal opening but assisted by improved lighting and magnification with laparoscopy (26). Options for transhiatal MIE include retrograde inversion for high-grade dysplasia and small intramucosal tumors well above the gastroesophageal junction or antegrade inversion for tumors adjacent to the gastroesophageal junction.

For the retrograde approach, the proximal stomach is divided with a stapler just below the gastroesophageal junction and a vein stripper is passed distally via a cervical esophagotomy. Within the abdomen, the vein stripper is retrieved through a gastrotomy made in the staple line and attached to an anvil extracorporeally. As the vein stripper is pulled back from the cervical esophagus, inversion places the mediastinal attachments on tension, allowing for excellent visualization of the posterior esophageal structures to the level of the inferior pulmonary veins. At the completion of the resection, the proximal stomach and left gastric pedicle are removed through an enlarged port site (Figure 2a) (27).

Figure 2.

 (a): Transhiatal minimally invasive esophagectomy (MIE): retrograde technique using vein stripper. (b) Transhiatal MIE: antegrade technique.

Antegrade inversion requires the division of the esophagus at the level of the thoracic inlet with a cutting stapler and then passage of the vein stripper distally (Figure 2b). When the tip of the vein stripper reaches the end of the lesser curvature extension of the esophagogastric specimen, the tip of the specimen and the vein stripper are pulled through a convenient port site. The specimen is then opened extracorporeally, and the proximal esophagus is inverted and extracted en bloc with the lesser curvature lymph node packet through an enlarged port site. The neoesophagus is passed to the neck and a cervical gastroesophageal anastomosis is created (27).

Ivor Lewis MIE

This approach has been offered to patients with invasive malignancy of the distal and mid esophagus, and is an alternative to the three-field MIE approach. This procedure commences in a fashion identical to the transhiatal MIE with laparoscopic creation of neoesophagus. The patient is then placed in left lateral decubitus position, and the operation proceeds with thoracoscopic esophageal mobilization and dissection of surrounding lymphatic tissue up to the level of the azygos vein where the esophagus is transected. The esophageal specimen is removed through a small thoracic incision and the gastric conduit is pulled into the right thoracic cavity (Figures 2a and 3). The esophagogastric anastomosis is then performed in the chest using a linear stapler, hand-sewn, or circular stapler technique, with the circular stapler technique allowing for a true thoracoscopic approach.

Figure 3.

 End-to-end anastomosis stapling during minimally invasive Ivor Lewis esophagectomy.

Technical considerations: Nasogastric decompression, pyloroplasty, and gastric preconditioning

While a nasogastric tube (NGT) is often used for decompression after esophagectomy for decompression of the gastric conduit, its use has recently come into question. Traditionally, the rationale behind NGT use involves its ability to prevent gastric distension with associated anastamotic dehiscence and aspiration. The major argument against NGT use is that malpositioning can lead to pressure necrosis of the conduit or anastamosis. In general, there has been a movement away from NGT use for many GI procedures including gastrectomy (28–30). One recent large series reported 3% rate of NGT complications versus a 4% gastric distension rate without NGT decompression (31), but NGT decompression is typically employed after MIE for a period of 3–5 d postoperatively.

Pyloroplasty has traditionally been performed during open esophogectomy to minimize the risk of vagotomy related gastric stasis and gastric outlet obstruction (32). Drawbacks of pyloroplasty include potential leaks at the surgical site, an increase in operating time, and bile reflux. With the evolution of the tubular gastric conduit and the movement away from a large gastric reservoir, gastric emptying has markedly improved. One study reported much improved gastric emptying results with a conduit consisting of tubulized stomach instead of whole stomach (3% vs 38%) (33), which was confirmed by another study with a 7% delayed gastric emptying rate in tubularized conduits (34). Metoclopramide should be considered for all esophagectomy patients with delayed gastric emptying. Other successful treatment options include endoscopic balloon dilatation, with or without botulinum toxin injections. Given the balance of risks and benefits, pyloroplasty during MIE is no longer routinely performed.

Preoperative ischemic gastric conditioning is another concept that must be considered prior to performing MIE. This practice arose following a 1998 report that revealed a significant improvement in gastric blood flow within the conduit at the time of esophagectomy after preoperative embolization of the left gastric and short gastric vessels (35). A more recent report of 83 procedures from 2007 indicated the feasibility and safety of laparoscopic ischemic conditioning of the gastric conduit (36). Although there are theoretical advantages to gastric conditioning that have lead many to advocate for its implementation (37), its ability to reduce postoperative morbidity and mortality has yet to be determined.

Outcomes

The goal of MIE is to decrease the morbidity and mortality that has traditionally been associated with the open approach, as has already been demonstrated in many other GI procedures. To date, no randomized controlled trials have been conducted comparing MIE and open esophagectomy. The data that we have for review consists of several case series and case control studies. While much has been written on the potential morbidity advantages of the thoracoscopic approach for the thoracic phase of esophagectomy (18,38–40), the focus of this review is on those reports with a laparoscopic component. Even within this select group, the variety of operative strategies makes definitive statements regarding MIE difficult, but the present data does at least provide some information on short-term morbidity, mortality, and efficacy.

Case series

There are several large case series in the literature that reveal morbidity and mortality values of the MIE approach to be similar to that of open surgery. In terms of efficacy, some limited survival rates have been reported, but a lack of long-term survival data suggests that the lymph node (LN) harvest number may be one of the more useful measures, with at least 15–18 generally considered to be adequate (41,42). One series of 222 three-field MIE patients, for example, had a mortality rate of 1.4% and an 11.7% anastomotic leak rate, with 36% three-year survival and a mean of 16 LN recovered (43). Another large series of 130 patients who also underwent three-field MIE (but with mini-laparotomy for specimen extraction) reported a 1.5% mortality rate with only a 2.3% leak rate with 45% three-year survival and a mean of 18 LN recovered (44). A more recent large series of 104 MIE with a combination of three-field and Ivor Lewis approaches reported a 1.9% mortality rate and leak rate of 9.6% and a mean of 14 LN recovered (34). Please see Table 1 for a more extensive listings of case series with accompanying details.

Table 1.   Summary of outcomes of MIE case series
AuthorYearTechniqueNMortality
(%)
Overall
morbidity
(%)
Anastomotic
leak (%)
Pneumonia
(%)
Arrythymia
(%)
LNs
(#)
Three-year
survival (%)
  1. LN, lymph nodes; MIE, minimally invasive esophagectomy; NR, not recorded.

Luketich et al. (43)2003Three-field2221.4NR11.77.7NR1636
Bizekis et al. (45)2006Ivor Lewis506NR61014NRNR
Palanivelu et al. (44)2006Three-field1301.520.82.31.55.41845
Collins et al. (46)2006Three-field25432121216NRNR
Smithers et al. (47)2007Three-field230NR430261722
Fabian et al. (48)2008Three-field224.5231451916NR
Nguyen et al. (34)2008Three-field & Ivor Lewis1041.9289.62NR14NR
Kitagawa et al. (49)2009Three-field1603866NRNRNR
Parameswaran et al. (50)2009Three-field5024888023NR
Perry et al. (27)2009Three-field & Transhiatal704.3NR17.115.727.1NRNR

Case control studies

Meta-analysis of studies comparing MIE with open esophagectomy for cancer has been performed. Due to the heterogeneity of the data, three comparative groups were created: (1) total MIE versus open transthoracic esophagectomy, (2) thoracoscopy with laparotomy versus open transthoracic esophagectomy, and (3) laparoscopic versus open transhiatal resection. In total, 10 studies consisting of 1,061 patients were included. While there was no difference in LN harvest, there was a trend towards reduced short-term mortality and major morbidity (in particular pulmonary morbidity) as well as decreased length of hospital stay and blood loss. The only significant finding was a reduced rate of anastomotic leakage (OR=0.51[95%CI: 0.28–0.95]) for the MIE patients in group 2 (51).

Conclusions

MIE has been gaining in popularity since the first reports from the early 1990s, and 25% of surgeons routinely apply some form of MIE (52). Similar to open surgery, several techniques have been developed, none of which has been deemed superior, but as a whole, they represent a safe alternative to open surgery. Available results from case series and comparative studies suggest trends towards improved short-term outcomes with equivalent efficacy, but definitive advantages have yet to be established. Prospective, randomized comparisons of the various approaches to MIE are needed to clarify the advantages of each one and assist with technique selection to optimize patient outcomes.

Acknowledgment

The authors do not have a financial relationship with any commercial entities.

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