Background
Minimally invasive esophagectomy (MIE) is a well-accepted approach to the treatment of benign esophageal diseases. It has not been as widely employed for the treatment of esophageal cancer, largely because it is highly technical and complex, but a number of studies have supported its feasibility in this context, and interest in this application has grown. [1, 2]
The incidence of esophageal cancer has increased over the last several decades, and adenocarcinoma now surpasses the incidence of squamous cell carcinoma. Treatment of esophageal carcinoma has become more aggressive and effective, and the overall morbidity and mortality in those who are surgically treated have declined, approaching 8-11% and 40-50%, respectively. [3, 4]
In the 17th century, the first cervical esophagotomy was reported; in the latter part of the 19th century, the first cervical esophagectomy was performed by Johann Nepomuk Czerny. [5] In 1913, Franz Torek performed the first thoracic esophagectomy for cancer in the German (now Lenox Hill) Hospital in New York City. [6] Over the next several decades, open surgical esophagectomy developed as an acceptable treatment for benign disease as well as esophageal cancer.
In 1989, interest in laparoscopic surgical techniques was sparked, as the first laparoscopic cholecystectomy was performed. [7] This technique was first adapted into the field of esophageal disease in 1991 with laparoscopic fundoplication, performed by Dallemagne et al. [8] With this, the shift toward minimally invasive esophageal surgery began.
Traditional approaches via open transhiatal or transthoracic (Ivor Lewis) resections were first "hybridized" with minimally invasive techniques, where parts of the procedure were performed in a minimally invasive fashion and other parts via standard incisions. [9]
Dallemagne et al performed the first mini-invasive subtotal esophagectomy in 1992, using both thoracoscopy (for dissecting the esophagus) and laparoscopy (for the gastroplasty). [10] The first esophagectomy performed completely via laparoscopy through a transhiatal approach was in 1995 by DePaul et al. [11] In 1999, Watson et al described a completely minimally invasive Ivor Lewis technique. [12] Since then, robotic-assisted approaches have described [13, 14, 15, 16, 17] (see the video below). Single-port approaches have been developed as well. [18]
Indications
Traditionally, esophagectomy has been performed via open transthoracic or transhiatal approaches, with randomized trials showing no significant difference in overall survival or disease-free survival. Outcomes after MIE have compared favorably to the reported series of open esophagectomy. [19]
Minimally invasive approaches to treatment of benign esophageal diseases have been met with widespread acceptance. This includes diseases such as achalasia, paraesophageal hernia, and other complex esophageal disorders. [20, 21, 22, 23]
This has not been the case with malignant disease of the esophagus. Currently, criteria for determining when a minimally invasive procedure should be performed in preference to an open procedure remain to be defined. [24] However, support for the feasibility of employing MIE in esophageal cancer has grown. [25] A multicenter retrospective matched-cohort study by Capovilla et al found that in 160 elderly patients (> 75 y) with esophageal cancer, thoracoscopic/laparoscopic MIE and robot-assisted MIE (RAMIE; n = 58) yielded a better postoperative course than open esophagectomy (n = 102), an improvement comparable to that seen in younger patients. [26]
Many high-volume institutions have increasingly elected to use MIE in the treatment of Barrett disease with high-grade dysplasia and in patients with small resectable lesions that have limited nodal involvement (N0-1). This includes T1 (invasion of the lamina propria or submucosa), T2 (invasion of the muscularis propria), and some instances of T3 lesions (invasion of the adventitia). Neoadjuvant chemoradiation is not a contraindication for MIE. [27, 28] For more information, see Esophageal Cancer Guidelines.
Contraindications
Currently, no standardized contraindications exist for the use of MIE. However, T4 lesions (invasion of surrounding tissues) are generally not amenable to any form of surgical resection. Extensive nodal disease and metastatic disease are also advanced stages that may necessitate an open surgical approach or even endoscopic stenting for palliation instead of an attempt at MIE. [28] Furthermore, any patient with a lesion that bridges the esophagogastric junction (EGJ) may not be considered a candidate for this approach unless the gastric margin can be cleared and an esophagogastrectomy can be done via either an open or a minimally invasive approach.
As with other laparoscopic procedures, patients with extensive adhesions and scar tissue over the abdomen or chest wall, particularly in areas where the thoracoscope or laparoscope would be placed, are at higher risk with MIE. Older patients and those with comorbid conditions are not candidates for surgery, because of the high morbidity with either an MIE or a standard procedure, but they may benefit more from nonsurgical therapy. [29]
Outcomes
Minimally invasive techniques for esophageal resection have been reported to have acceptably reduced procedure-related morbidity without compromising disease-free survival rates. [19]
Luketich et al have reported an extensive experience; their initial series of 222 patients had grown to more than 1000 by 2012. [30] In the initial series, mortality was 1.4% versus 5.5% for an open approach. [29, 31, 32] Furthermore, the survival curve at 19-month follow-up was comparable in the two groups. [29] In their 2012 report of 1011 patients who underwent MIE via either a modified McKeown minimally invasive approach or an Ivor Lewis approach, the authors cited a 0.9% mortality for the Ivor Lewis MIE approach. [30]
In another analysis of 41 elderly patients over the age of 75 years who underwent MIE, no operative deaths occurred, with a survival of 81% at 20 month follow-up. [33] These findings suggest that MIE can be safely performed in selected patients and even in those considered high-risk who might not otherwise be considered for an open surgery.
Other outcome improvements seen with MIE include decreased intensive care unit (ICU) and hospital length of stay, reduced blood loss, and shorter operating times. In particular, Luketich et al reported a median ICU stay of 1 day and a total hospital stay of 7 days, compared with the average hospital stay of 16.6 days in the open approach. Operating room times in the same study averaged 306 minutes, whereas the average for an open procedure is 336 minutes. [29, 31] Similar results can be seen in multiple other series as compared with open procedures (see the table below).
Complications and outcomes are significantly influenced by the volume of patients, because a large learning curve exists. High-volume centers tend to have more experience and therefore better outcomes than smaller-volume hospitals.
Wang et al carried out a propensity score-matched comparison of MIE and open esophagectomy with respect to outcomes, quality of life, and survival in patients with squamous cell carcinoma. [34] They found that MIE was associated with a shorter operating time (191 ± 47 vs 211 ± 44 min), reduced blood loss (135 ± 74 vs 163 ± 84 mL), a similar lymph node harvest (24.1 ± 6.2 vs 24.3 ± 6.0), a shorter postoperative hospital stay (11 vs 12 d), a lower rate of major complications (30.4% vs 36.9%), a lower rate of readmission to the ICU (5.6% vs 9.7%), and comparable perioperative mortality.
van der Sluis et al assessed the long-term oncologic results of RAMIE with two-field lymphadenectomy in 108 patients with potentially resectable esophageal cancer. [35] They found RAMIE to be oncologically effective and capable of providing good local control with a low percentage of local recurrence at long-term follow-up.
In a subsequent randomized controlled trial that included 112 patients with resectable intrathoracic esophageal cancer who were treated with either RAMIE or open transthoracic esophagectomy (OTE), van der Sluis et al found RAMIE to be associated with lower rates of overall surgery-related and cardiopulmonary complications, less postoperative pain, better short-term quality of life, and superior short-term postoperative functional recovery compared to OTE. [36] Oncologic outcomes were comparable for the two approaches.
In a prospective phase II study coordinated by the Eastern Cooperative Oncology Group (ECOG), which was aimed at assessing the feasibility of MIE in a multi-institutional setting, Luketich et al reported the following results [37] :
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The 30-day mortality in eligible patients who underwent MIE was 2.1%
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The median ICU stay was 2 days
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The median hospital stay was 9 days
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Adverse events classified as grade 3 or higher included anastomotic leakage (8.6%), acute respiratory distress syndrome (ARDS; 5.7%), pneumonitis (3.8%), and atrial fibrillation (2.9%)
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The estimated 3-year overall survival (median follow-up, 35.8 months) was 58.4%
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Locoregional recurrence occurred in only 7 patients (6.7%)
In a nationwide retrospective analysis from Japan that included 14,880 patients who underwent esophagectomy for clinical stage 0-III esophageal cancer, Sakamoto et al compared in-hospital mortality and morbidity for MIE versus open esophagectomy. [38] MIE was associated with lower incidences of in-hospital mortality, surgical-site infection (SSI), anastomotic leakage, blood transfusion, reoperation, tracheotomy, and unplanned intubation, as well as a shorter postoperative stay. However, MIE was also associated with higher rates of vocal cord dysfunction and prolonged intubation after esophagectomy, as well as a longer duration of anesthesia.
In a meta-analysis of 14 studies (N = 3468), Deng et al evaluated short-term outcomes for minimally invasive McKeown esophagectomy (MIME) vs minimally invasive Ivor Lewis esophagectomy (MILE) in patients with resectable esophageal or junctional tumors. [39] MIME led to more blood loss, longer operating times, and longer hospital stays, as well as higher rates of pulmonary complications, total anastomotic leak, stricture, and vocal cord injury/palsy. No significant differences were found in R0 resection rate; number of lymph modes retrieved; blood transfusion rate; length of ICU stay; incidence of cardiac arrhythmia, chyle leak, or severe anastomotic leak; 30-day/in-hospital mortality; or 90-day mortality.
In a study of 76 patients with resectable esophageal malignancies, Guerra et al assessed the results of robotic esophagectomy via three approaches: Ivor Lewis (n = 45), McKeown (n = 25), and transhiatal (n = 6). [40] No intraoperative complications and no conversions were noted. Postoperative morbidity was 41%, and the incidence of anastomotic leakage was 13%. Reintervention was required in eight of the 76 patients. The authors found all of the procedures to be associated with the expected perioperative morbidity and to yield excellent pathologic outcomes.
The MIRO trial compared the long-term 5-year outcomes (eg, overall survival [OS], disease-free survival [DFS], and pattern of disease recurrence) of hybrid MIE (HMIE) with those of open esophagectomy in 207 patients (age range, 18-75 y; 175 men, 32 women) with resectable cancer of the middle or lower third of the esophagus. [41] No difference in long-term survival was found between the two groups: 5-year OS was 59% with HMIE vs 47% with open esophagectomy, and 5-year DFS was 52% with HMIE vs 44% with open esophagectomy. There were no statistically significant differences in recurrence rate or location between the two groups.
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Minimally invasive esophagectomy. Thoracoscopic port sites for transthoracic approach.
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Minimally invasive esophagectomy. Mobilization of thoracic esophagus using Penrose drain.
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Minimally invasive esophagectomy. Abdominal port sites for laparoscopic portion of transthoracic esophagectomy with cervical anastomosis.
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Minimally invasive esophagectomy. Pyloroplasty during laparoscopy.
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Minimally invasive esophagectomy. Mobilization of stomach.
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Minimally invasive esophagectomy. Completed reconstruction with gastric conduit.
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Minimally invasive esophagectomy. Dissection of esophagus using inversion technique.
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Outcomes based on procedure type.
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Robotic-assisted esophagectomy: part 1. Video courtesy of Memorial Sloan-Kettering Cancer Center, featuring Inderpal S Sarkaria, MD.
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Robotic-assisted esophagectomy: part 2. Video courtesy of Memorial Sloan-Kettering Cancer Center, featuring Inderpal S Sarkaria, MD.
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Robotic-assisted esophagectomy: part 3. Video courtesy of Memorial Sloan-Kettering Cancer Center, featuring Inderpal S Sarkaria, MD.
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Robotic-assisted esophagectomy: part 4. Video courtesy of Memorial Sloan-Kettering Cancer Center, featuring Inderpal S Sarkaria, MD.
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Robotic-assisted esophagectomy: part 5. Video courtesy of Memorial Sloan-Kettering Cancer Center, featuring Inderpal S Sarkaria, MD.
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Robotic-assisted esophagectomy: part 6. Video courtesy of Memorial Sloan-Kettering Cancer Center, featuring Inderpal S Sarkaria, MD.
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Robotic-assisted esophagectomy: part 7. Video courtesy of Memorial Sloan-Kettering Cancer Center, featuring Inderpal S Sarkaria, MD.
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Advantages of robotic-assisted minimally invasive surgery. Video courtesy of Memorial Sloan-Kettering Cancer Center, featuring Inderpal S Sarkaria, MD.
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Minimally invasive esophagectomy. Room setup and port placement. Video courtesy of Memorial Sloan-Kettering Cancer Center, featuring Inderpal S Sarkaria, MD.
