Evolution in the Treatment of Esophageal Disease at a Single Academic Institution: 2004

Abstract

Introduction:

Management of benign and malignant esophageal disease has changed rapidly over the past decade. The aim of this study was to analyze evolution in surgical management of esophageal disease at a single academic medical center during this period.

Materials and Methods:

We reviewed a retrospective cohort of patients who underwent esophagectomy between 2004 and 2013. Patient, institutional, treatment, and outcomes variables were reviewed.

Results:

317 patients were analyzed. Median age was 63.5 years; 80% were male. Average inhospital mortality rate was 3.8%. Operative indications changed significantly from 2004 to 2013, with more operations performed for invasive malignancy (77% vs. 95%) and fewer for high-grade dysplasia (12% vs. 3%, P = .008). In 2004, Ivor Lewis esophagectomy was the most common surgical technique, but the three-field technique was the operation of choice in 2013. A minimally invasive approach was used in 19% of cases in 2004 and 100% of cases in 2013 (P < .001). Anastomotic leak ranged from 0% to 21% with no significant difference over the study period (P = .18). Median lymph node harvest increased from seven to 18 nodes from 2004 to 2013 (P = .001). Hospital length of stay decreased from 15 to 8 days (P = .001). In 2013, 79% of patients were discharged to home, compared to 73% in 2004 (P = .04).

Discussion:

Over the last decade, our treatment of esophageal disease has evolved from a predominantly open Ivor Lewis to a minimally invasive three-field approach. Operations for malignancy have also increased dramatically. Postoperative complications and mortality were not significantly changed, but were consistently low during the latter years of the study.

Introduction

In the United States, the incidence of esophageal adenocarcinoma has increased dramatically and is now the seventh leading cause of cancer death in men.^1,2 As a result, many treatment centers are experiencing an increase in patient referrals for comprehensive treatment. Historically, mortality and morbidity associated with surgical treatment have been high. As recently as the mid-1990s, some experienced groups reported an inhospital mortality as high as 18%.³ Consequently, significant improvement in preoperative selection, staging, and surgical techniques has been proposed to decrease the adverse outcomes related to treating esophageal disease.⁴

A small number of reports have raised the issue of process improvement that might lead to better outcomes after esophagectomy.^5,6 Most other studies have relied on procedure volume,⁷ multidisciplinary treatment paradigms,⁸ or quality of life indices⁹ as prime indicators of success after treatment of esophageal cancer. Treatment has recently experienced major changes with respect to surgical technique and approach, but a paucity of contemporary data on how this may contribute to improved outcomes after esophagectomy remains. Consequently, the aim of this study was to analyze the evolution in the surgical management and associated outcomes following esophagectomy at a single, National Cancer Institute (NCI)-designated, academic medical center over a decade.

Materials and Methods

We performed a retrospective review of a prospectively maintained single-center esophageal cancer registry after Institutional Review Board approval (IRB 1759). Patients who underwent esophagectomy with reconstruction at Oregon Health and Science University (OHSU) between January 2004 and December 2013 were included for analysis. Individual patient, institutional, and postoperative variables were abstracted and reviewed. Outcome measurements included indications for surgery, surgical technique, surgical approach, number of lymph nodes harvested, postoperative complications, length of stay (LOS), discharge disposition, inhospital mortality, and overall survival (OS).

Neoadjuvant therapy

Beginning in 2005, all esophageal disease patients under consideration for esophagectomy were presented at an institutional multidisciplinary Esophageal Care Conference. Patients with resectable tumors were offered either esophagectomy alone for early disease or neoadjuvant chemoradiotherapy (CRT) followed by esophagectomy for regionally advanced disease. In the latter half of the study, we adopted a more liberal use of neoadjuvant CRT to include stage II esophageal cancers, given the emerging evidence of the benefit of neoadjuvant CRT in stage III patients.¹⁰ In the early years of the study, patients received standard chemotherapy regimen of a platin-based therapy (cisplatin, carboplatin, or oxaliplatin) and 5-fluorouracil (5-FU) administered over 5–6 weeks. In the latter half of the study, capecitabine or a taxane derivative (paclitaxel or docetaxel) was used instead of 5-FU, in line with a large prospective trial reporting survival benefit from this regimen when combined with surgery.¹⁰ For most patients, External Beam Radiotherapy (EBRT) was delivered to the tumor and regional nodes for a total treatment dose of 50.4–54 Gy.

Operative technique and approach

Both open and minimally invasive approaches were used during the study period, and three different techniques were performed, including transhiatal, transthoracic (Ivor Lewis), and three field. The open transhiatal technique required a laparotomy and a left cervical incision. An open Ivor Lewis esophagectomy was performed through a laparotomy and a right thoracotomy, as originally described,¹¹ with only minor modifications. For the open three-field technique, the chest was accessed by means of a right anterior thoracotomy, and the abdomen was opened through a laparotomy, with the anastomosis performed through a left cervical incision. For the minimally invasive approach to each of these techniques, both chest and abdominal incisions were replaced by functionally positioned laparoscopic or thoracoscopic ports. The left neck incision was identical for both the open and minimally invasive approaches. Since 2010, a pyloroplasty has been performed on all patients, due to a high incidence of delayed conduit emptying prior.

When the transhiatal technique was indicated, the stomach was mobilized on the right gastric and right gastroepiploic arteries. The left gastric artery was divided at its origin. Lymph nodes extending from the right gastric vessel through the base of the celiac axis, nodes superior to the proximal portion of the splenic artery, and those along the lesser curvature and upper greater curve of the stomach were also included in the resection.¹² The thoracic mobilization was performed through the hiatus of the diaphragm and also through the thoracic inlet from the cervical incision. The esophagus was inverted at the time of extraction, and a neck anastomosis was performed in a modified Orringer manner.¹³

For the Ivor Lewis technique, the abdominal portion was performed as previously described.¹¹ The patient was repositioned to allow access to the right chest. The thoracic esophagus was mobilized, all paraesophageal lymph nodes were removed, and the specimen was resected. An esophagogastric anastomosis was constructed in the right chest. Most often, a hand-sewn two-layer anastomosis was used for the open approach. When done thoracoscopically the anastomosis was completed using a linear or circular stapler.

Finally, the three-field technique started with the patient positioned in a left lateral decubitus position. Esophageal mobilization with en bloc lymphadenectomy was performed through the right chest. In addition, superior mediastinal nodes were removed in the dissection. The patient was repositioned in the supine split leg position, then the abdominal portion of the operation consisted of conduit preparation, with an en bloc upper abdominal central lymphadenectomy.^12,14 A left cervical esophagus exposure was performed, and the conduit was brought up into the neck, where an end-to-side stapled modified Orringer esophagogastric anastomosis was created.

Statistical analysis

Comparisons for differences across time were performed using a Kruskal–Wallis test for continuous variables and Pearson chi-squared test for discrete variables. Kaplan–Meier analysis was used to evaluate OS. Comparisons of survival between groups were made using the log-rank test. Statistical analysis was performed using R (version 2.13.1, R Development Core Team, Vienna, Austria), and significance was set at a P value of .05.

Results

Demographic data are shown in Table 1. Three hundred seventeen patients were analyzed. Median age was 63.5 years; 80% were male. Adenocarcinoma was the most common operative indication, accounting for 74% of cases overall. Invasive malignancy accounted for 77% of esophagectomy patients in 2004 and increased to 95% in 2013. Operations for high-grade dysplasia (HGD) decreased from 12% to 3% during the same period. Operations for benign disease also decreased from 12% in 2004 to 3% in 2013 (P = .008). The evolution of operative approach and technique is depicted in Figure 1. Open operations accounted for 73% of cases in 2004. In contrast, the laparoscopic approach was used in only 19% of cases in 2004, but 100% of cases in 2013 (P < .001). An Ivor Lewis technique was the most common surgery in the early portion of the study, accounting for 54% of cases in 2004, but decreasing to only 3% in 2013 (P < .001). The three-field technique was the most common in 2013, accounting for 71% of cases. Perioperative outcome data are shown in Table 2. Atrial fibrillation was the most common complication, averaging 24% across the study period. Anastomotic leaks ranged between 0% and 21% and occurred in 3% of patients in 2013. Median lymph node harvest increased from 7 to 18 nodes (P < .001), and hospital stay decreased from 15 to 8 days (P < .001). In 2013, 79% of patients were discharged to home, compared to 73% in 2004 (P = .04). The average inhospital mortality rate for our cohort was 3.8%. OS comparing minimally invasive esophagectomy (MIE) versus Open approach for the entire cohort is shown in Figure 2. OS based on early stage (stage 0 and I) and locoregional (stage II and III) disease is shown in Figure 3.

FIG. 1.

(a) Percentage of esophagectomies performed by Transthoracic, Transhiatal, and Three-Field techniques, 2004 to 2013. (b) Percentage of esophagectomies performed by open or minimally invasive approaches, 2004 to 2013.

FIG. 2.

Overall survival for our cohort categorized by approach.

FIG. 3.

(a) Overall survival for subgroup of patients with stage 0 and I disease, categorized by approach. (b) Overall survival for patients with stage II and III disease, categorized by approach.

Table 1.

Demographic, Diagnosis, and Treatment Variables for All 317 Study Patients, 2004–2013

Year	2004	2005	2006	2007	2008	2009	2010	2011	2012	2013	P value
Number (N)	26	28	32	29	28	38	33	29	36	38
Age^a	62.5 (56.5–69.2)	68 (57.8–75.2)	65.5 (58–72.2)	62 (56–71)	60.5 (54–68.2)	63.5 (57–73.5)	64 (55–71)	62 (59–70)	64.5 (58.5–73.5)	68 (64–71)	.389¹
Gender, M (%)	21 (81)	20 (71)	24 (75)	25 (86)	23 (82)	29 (76)	24 (73)	26 (90)	30 (83)	31 (82)	.746²
BMI^a	28 (24–32)									29 (24–36)	.246¹
Preoperative Diagnosis (%)											.008¹
Adenocarcinoma	16 (62)	20 (71)	22 (69)	23 (79)	17 (61)	27 (71)	28 (85)	20 (69)	31 (86)	32 (84)
Squamous cell Ca	4 (15)	3 (11)	3 (9)	2 (7)	0 (0)	7 (18)	1 (3)	6 (21)	3 (8)	4 (11)
High-grade dysplasia	3 (12)	2 (7)	3 (9)	3 (10)	5 (18)	0 (0)	1 (3)	2 (7)	1 (3)	1 (3)
Stricture	2 (8)	1 (4)	3 (9)	1 (3)	5 (18)	3 (8)	3 (9)	1 (3)	1 (3)	1 (3)
Perforation	1 (4)	2 (7)	1 (3)	0 (0)	1 (4)	1 (3)	0 (0)	0 (0)	0 (0)	0 (0)
Approach (%)											<.001²
Open	19 (73)	16 (57)	19 (59)	15 (52)	12 (43)	8 (21)	3 (9)	0 (0)	0 (0)	0 (0)
MIE	5 (19)	10 (36)	12 (38)	12 (41)	12 (43)	28 (74)	29 (88)	28 (97)	35 (97)	38 (100)
Conversion	2 (8)	2 (7)	1 (3)	2 (7)	4 (14)	2 (5)	1 (3)	1 (3)	1 (3)	0 (0)
Operative technique (%)											<.001²
Ivor Lewis	14 (54)	7 (25)	12 (38)	12 (41)	7 (25)	5 (13)	5 (15)	3 (10)	3 (9)	1 (3)
Transhiatal	9 (35)	11 (39)	10 (31)	5 (17)	12 (43)	7 (18)	5(15)	3 (10)	1 (3)	8 (21)
Three Field	0 (0)	4 (14)	7 (22)	12 (41)	7 (25)	21 (55)	23 (70)	21 (72)	26 (81)	27 (71)
Other^b	3 (12)	6 (21)	3 (9)	0 (0)	2 (7)	5 (13)	0 (0)	2 (7)	2 (6)	2 (5)

Values are median and interquartile range.

Other category includes partial esophagectomy, esophagogastrectomy, and esophagectomy not otherwise specified.

Kruskal–Wallis test.

Pearson chi-squared test.

MIE, minimally invasive esophagectomy.

Table 2.

Perioperative Outcomes for All 317 Study Patients, 2004–2013

Year	2004	2005	2006	2007	2008	2009	2010	2011	2012	2013	P value^b
Number (N)	26	28	32	29	28	38	33	29	36	38
Anastomotic leak (%)	2 (8)	4 (14)	5 (16)	4 (14)	6 (21)	5 (13)	0 (0)	2 (7)	4 (11)	1 (3)	.182
Atrial arrhythmia (%)	5 (19)	7 (25)	10 (31)	11 (38)	4 (14)	12 (32)	4 (12)	8 (28)	7 (19)	8 (21)	.323
Chylothorax (%)	0 (0)	0 (0)	1 (3)	0 (0)	1 (4)	0 (0)	1 (3)	1 (3)	0 (0)	1 (3)	.825
RLN injury (%)	0 (0)	0 (0)	1 (3)	0 (0)	0 (0)	5 (13)	1 (3)	0 (0)	0 (0)	0 (0)	.002
Nodes removed^a	7 (4–12.25)	13 (10–19.25)	8.5 (3.75–14)	13 (6–16)	8.5 (2–13.5)	20 (13.25–28)	18 (15–25)	19 (13–24)	19 (15–29.5)	18 (12–24.75)	<.001
Positive nodes	0 (0–0)	0 (0–0)	0 (0–0)	0 (0–1)	0 (0–0)	0 (0–1.75)	0 (0–1)	0 (0–1)	0 (0–1)	0 (0–2)	.070
LOS^a	15 (11.25–26.25)	10.5 (8.75–17.25)	13.5 (10–18)	13 (12–20)	13.5 (8.75–18.75)	13 (9–18.75)	9 (9–12)	9 (9–11.25)	8.5 (8–12)	8 (8–9.75)	<.001
Disposition (%)											.043
Home	19 (73)	19 (68)	23 (72)	21 (72)	23 (82)	29 (76)	29 (88)	24 (86)	25 (69)	30 (79)
SNF	6 (23)	7 (25)	8 (25)	2 (7)	2 (7)	9 (24)	4 (12)	1 (4)	3 (8)	3 (8)
Other	0 (0)	0 (0)	0 (0)	1 (3)	0 (0)	0 (0)	0 (0)	0 (0)	0 (0)	0 (0)
Unknown	0 (0)	2 (7)	0 (0)	2 (7)	1 (4)	0 (0)	0 (0)	2 (7)	5 (14)	4 (11)
Inhospital death (%)	1 (4)	0 (0)	1 (3)	3 (10)	2 (7)	0 (0)	0 (0)	1 (3)	3 (8)	1 (3)	.318

Values are median and interquartile range.

Kruskal–Wallis test.

LOS, length of stay; RLN, recurrent laryngeal nerve.

Discussion

This study provides insight into the evolution of the surgical management of esophageal disease over a decade at a single institution. Currently, treatment of esophageal disease in the United States warrants increased attention and resource allocation across the healthcare system, due to an alarming increase in incidence.^2,15 This emphasizes the need for refined treatment paradigms that increase early detection rates, maximize tumor response to systemic therapy, and minimize surgical morbidity and mortality to increase survival.

Our study demonstrates a number of important trends that occurred at our institution. First, operations for malignant disease increased from 77% in 2004 to 95% in 2013. In contrast, operations for HGD, stricture, and perforation have all decreased during this time. This is largely due to increased referrals to a tertiary center for the treatment of complex malignancy, as well as the emergence of endoscopic treatments for HGD. It is now well established that morbidity and mortality are significantly improved when esophagectomies are performed at high-volume centers,^16,17 and current consensus guidelines recommend that esophageal cancer patients being considered for esophagectomy should be referred to centers that specialize in the treatment of foregut cancers.¹⁸

Consequently, it is hardly surprising that one U.S. study noted the percentage of esophagectomies done at hospitals performing more than 20 cases per year increased from 31% to 48% from 1990 to 2004.¹⁹ Similar regional referral patterns have contributed to the increase in esophagectomies for malignancy noted in this analysis. In addition, current endoscopic treatment modalities have allowed for a less invasive means of treating HGD and intramucosal cancers. Endoscopic resection has recently surpassed esophagectomy as the most common treatment for early esophageal cancers in the United States.²⁰ Based on data from the National Cancer Database, endoscopic resection was used for 19.0% of T1a tumors in 2004, but increased to 53.0% in 2010.²⁰ While long-term data are lacking to directly compare outcomes of endoscopic therapies versus esophagectomy, early experience with endoscopic resection has shown acceptable oncologic outcomes with lower rates of major complications.^21–28 Both increased referrals to specialized centers and increased adoption of endoscopic therapies have the potential to improve overall patient outcomes and also likely explain the trends noted in this study.

Furthermore, minimally invasive surgical techniques have been used to enhance recovery and improve outcomes for a number of complex operations. Accordingly, MIE is now being performed at a number of centers with excellent outcomes.^29,30 Many studies have demonstrated improved short-term outcomes after MIE, compared to comparable open approaches.^29–33 Our group now considers MIE to be the first-line approach in the surgical treatment of esophageal cancer. Accordingly, we have also seen a significant change in our operative technique in the last decade. An open Ivor Lewis esophagectomy with intrathoracic anastomosis was the most common technique performed early on. We have seen a shift toward a minimally-invasive three-field esophagectomy as the most common operation for locoregional disease. The primary advantage of a three-field technique over the Lewis operation is that the esophagogastric anastomosis is in the neck rather than the chest. Other groups have shown that clinically significant leaks occur with equal frequency in both locations.³⁴ The majority of cervical leaks, however, can be managed conservatively, while mortality from a thoracic anastomotic leak can be significant. In a large study of 475 esophagectomies performed with intrathoracic anastomoses, the inhospital mortality following anastomotic leak was 35%.³⁵ Because of the ease of management and acceptably low leak rate, we now perform a cervical anastomosis exclusively.

Finally, the ability to perform an abdominal, mediastinal, and cervical lymphadenectomy through a three-field technique has provided an advantage beyond a transhiatal operation for locoregional disease. In this study, we demonstrated an increase in mean lymph nodes harvested from seven to 18 nodes per case. This represents the result of our transition toward an extensive three-field lymph node dissection. The presence of lymph node metastasis is one of the most important predictors of survival in esophageal cancer.³⁶ In addition to the presence of positive nodes, the number of positive lymph nodes also plays an important role in determining prognosis.³⁷ The benefit of an extensive lymph node dissection has yet to be definitively established, and no current guidelines exist that define the extent of lymphadenectomy required for accurate staging. It seems reasonable to assume that harvesting more nodes provides more accurate staging. The effect on patient outcomes is still uncertain, but a large analysis of the Surveillance, Epidemiology, and End Results database from 1988 through 2005 found that lymphadenectomy of greater than 18 nodes was an independent predictor of survival in patients undergoing esophagectomy for esophageal adenocarcinoma.³⁷

Ultimately, refinements in operative technique, operative approach, and postoperative care have been initiated in an attempt to improve outcomes over what is currently available. In this cohort, our LOS decreased significantly. Other groups have noted similar improvements in short-term outcomes with minimally invasive approaches and likewise have not demonstrated improvements in OS.³⁸ With the exception of recurrent laryngeal nerve injury, our rate of major complications has remained constant over time (Table 2). This is surprising, given our routine initiation of preoperative immunonutrition (2009), a dedicated postoperative care pathway (2007), and a dedicated esophagostomy surgical, anesthesia, and critical care team. By critically examining the trends in our practice we aim to further improve our perioperative care and operative technique and anticipate continued improvement in postoperative outcomes in to the future.

Our study does have limitations. First, the study represents only a single-center retrospective experience. A larger multi-institution examination would provide better insight into the trends taking place nationally and internationally. In addition, lack of standardization of technique and language used in the literature makes it difficult to compare the data in this study to other institutions. Finally, the study only observes trends in practice, not causative relationships between changes in practice and outcomes.

Over the last decade, our treatment of esophageal disease has evolved from a predominantly open Ivor Lewis technique to a minimally invasive three-field approach. In addition, proportions of operations for malignancy have increased dramatically, while those for benign disease have declined. Postoperative complications and mortality were unchanged over the study period, but were consistently low during the latter years of the study.

Footnotes

Acknowledgments

Dr. Dolan's authorship was supported by the Oregon Clinical and Translational Research Institute (OCTRI) and a grant (Grant # UL1TR000128) from the National Center for Advancing Translational Sciences (NCATS) of the National Institutes of Health (NIH). The content is solely the responsibility of the authors and does not necessarily represent the official views of the NIH.

Disclosure Statement

No competing financial interests exist.

References

Bronson

, Luna

, Hunter

. Tailoring esophageal cancer surgery. Semin Thorac Cardiovasc Surg, 2012; 24:275–287.

Abrams

, Sharaiha

, Gonsalves

, Lightdale

, Neugut

. Dating the rise of esophageal adenocarcinoma: Analysis of Connecticut Tumor Registry data, 1940–2007. Cancer Epidemiol Biomarkers Prev, 2011; 20:183–186.

Poon

, Law

, Chu

, Branicki

, Wong

. Esophagectomy for carcinoma of the esophagus in the elderly: Results of current surgical management. Ann Surg, 1998; 227:357–364.

Hoppo

, Jobe

. Personalizing therapy for esophageal cancer patients. Thorac Surg Clin, 2013; 23:471–478.

Markar

, Schmidt

, Kunz

, et al. Evolution of standardized clinical pathways: Refining multidisciplinary care and process to improve outcomes of the surgical treatment of esophageal cancer. J Gastrointest Surg, 2014; 18:1238–1246.

Low

, Kunz

, Schembre

, et al. Esophagectomy—it's not just about mortality anymore: Standardized perioperative clinical pathways improve outcomes in patients with esophageal cancer. J Gastrointest Surg, 2007; 11:1395–1402; discussion 1402.

Varghese

Jr. , Wood

, Farjah

, et al. Variation in esophagectomy outcomes in hospitals meeting Leapfrog volume outcome standards. Ann Thorac Surg, 2011; 91:1003–1009; discussion 1009–1010.

Siddiqui

, Atkins

, Diggs

, et al. Overall survival analysis of neoadjuvant chemoradiotherapy and esophagectomy for esophageal cancer. J Gastrointest Oncol, 2014; 5:86–91.

Sundaram

, Geronimo

, Willer

, et al. Survival and quality of life after minimally invasive esophagectomy: A single-surgeon experience. Surg Endosc, 2012; 26:168–176.

10.

van Hagen

, Hulshof

, van Lanschot

, et al. Preoperative chemoradiotherapy for esophageal or junctional cancer. N Engl J Med, 2012; 366:2074–2084.

11.

Lewis

. The surgical treatment of carcinoma of the oesophagus; with special reference to a new operation for growths of the middle third. Br J Surg, 1946; 34:18–31.

12.

de Steur

, Dikken

, Hartgrink

. Lymph node dissection in resectable advanced gastric cancer. Dig Surg, 2013; 30:96–103.

13.

Jobe

, Kim

, Minjarez

, et al. Simplifying minimally invasive transhiatal esophagectomy with the inversion approach: Lessons learned from the first 20 cases. Arch Surg, 2006; 141:857–865; discussion 865–856.

14.

Hoppo

, Jobe

, Hunter

. Minimally invasive esophagectomy: The evolution and technique of minimally invasive surgery for esophageal cancer. World J Surg, 2011; 35:1454–1463.

15.

Di Pardo

, Bronson

, Diggs

, et al. The Global Burden of Esophageal Cancer: A Disability-Adjusted Life-Year Approach. World J Surg, 2016; 40:395–401.

16.

Birkmeyer

, Stukel

, Siewers

, et al. Surgeon volume and operative mortality in the United States. N Engl J Med, 2003; 349:2117–2127.

17.

Rodgers

, Jobe

, O'Rourke

, et al. Case volume as a predictor of inpatient mortality after esophagectomy. Arch Surg, 2007; 142:829–839.

18.

American Gastroenterological

, Spechler

, Sharma

, et al. American Gastroenterological Association medical position statement on the management of Barrett's esophagus. Gastroenterology, 2011; 140:1084–1091.

19.

Gasper

, Glidden

, Jin

, Way

, Patti

. Has recognition of the relationship between mortality rates and hospital volume for major cancer surgery in California made a difference?: A follow-up analysis of another decade. Ann Surg, 2009; 250:472–483.

20.

Merkow

, Bilimoria

, Keswani

, et al. Treatment trends, risk of lymph node metastasis, and outcomes for localized esophageal cancer. J Natl Cancer Inst, 2014; 106.

21.

Pacifico

, Wang

, Wongkeesong

, Buttar

, Lutzke

. Combined endoscopic mucosal resection and photodynamic therapy versus esophagectomy for management of early adenocarcinoma in Barrett's esophagus. Clin Gastroenterol Hepatol, 2003; 1:252–257.

22.

Pech

, Bollschweiler

, Manner

, et al. Comparison between endoscopic and surgical resection of mucosal esophageal adenocarcinoma in Barrett's esophagus at two high-volume centers. Ann Surg, 2011; 254:67–72.

23.

Prasad

, Wang

, Buttar

, et al. Long-term survival following endoscopic and surgical treatment of high-grade dysplasia in Barrett's esophagus. Gastroenterology, 2007; 132:1226–1233.

24.

Prasad

, Wu

, Wigle

, et al. Endoscopic and surgical treatment of mucosal (T1a) esophageal adenocarcinoma in Barrett's esophagus. Gastroenterology, 2009; 137:815–823.

25.

Reed

, Tolis

Jr. , Edil

, et al. Surgical treatment of esophageal high-grade dysplasia. Ann Thorac Surg, 2005; 79:1110–1115; discussion 1110–1115.

26.

Schembre

, Huang

, Lin

, Cantone

, Low

. Treatment of Barrett's esophagus with early neoplasia: A comparison of endoscopic therapy and esophagectomy. Gastrointest Endosc, 2008; 67:595–601.

27.

Zehetner

, DeMeester

, Hagen

, et al. Endoscopic resection and ablation versus esophagectomy for high-grade dysplasia and intramucosal adenocarcinoma. J Thorac Cardiovasc Surg, 2011; 141:39–47.

28.

Huntington

, Walker

, Meara

, et al. Endoscopic mucosal resection for staging and treatment of early esophageal carcinoma: A single institution experience. Surg Endosc, 2015; 29:2121–2125.

29.

Pham

, Perry

, Dolan

, et al. Comparison of perioperative outcomes after combined thoracoscopic-laparoscopic esophagectomy and open Ivor-Lewis esophagectomy. Am J Surg, 2010; 199:594–598.

30.

Biere

, Cuesta

, van der Peet

. Minimally invasive versus open esophagectomy for cancer: A systematic review and meta-analysis. Minerva Chir, 2009; 64:121–133.

31.

Treitl

, Hurtado

, Ben-David

. Minimally Invasive Esophagectomy: A New Era of Surgical Resection. J Laparoendosc Adv Surg Tech A, 2016; 26:276–280.

32.

Perry

, Enestvedt

, Pham

, et al. Comparison of laparoscopic inversion esophagectomy and open transhiatal esophagectomy for high-grade dysplasia and stage I esophageal adenocarcinoma. Arch Surg, 2009; 144:679–684.

33.

Hong

, Zhang

, Yang

, Zhao

. The short-term outcome of three-field minimally invasive esophagectomy for Siewert type I esophagogastric junctional adenocarcinoma. Ann Thorac Surg, 2013; 96:1826–1831.

34.

Price

, Nichols

, Harmsen

, et al. A comprehensive review of anastomotic technique in 432 esophagectomies. Ann Thorac Surg, 2013; 95:1154–1160; discussion 1160–1151.

35.

Whooley

, Law

, Alexandrou

, Murthy

, Wong

. Critical appraisal of the significance of intrathoracic anastomotic leakage after esophagectomy for cancer. Am J Surg, 2001; 181:198–203.

36.

Lagergren

, Mattsson

, Zylstra

, et al. Extent of Lymphadenectomy and Prognosis After Esophageal Cancer Surgery. JAMA Surg, 2016; 151:32–39.

37.

Solomon

, Zhuge

, Cheung

, Franceschi

, Koniaris

. The roles of neoadjuvant radiotherapy and lymphadenectomy in the treatment of esophageal adenocarcinoma. Ann Surg Oncol, 2010; 17:791–803.

38.

Cash

, Zehetner

, Hedayati

, et al. Outcomes following laparoscopic transhiatal esophagectomy for esophageal cancer. Surg Endosc, 2014; 28:492–499.

Evolution in the Treatment of Esophageal Disease at a Single Academic Institution: 2004–2013

Abstract

Abstract

Introduction:

Materials and Methods:

Results:

Discussion:

Introduction

Materials and Methods

Neoadjuvant therapy

Operative technique and approach

Statistical analysis

Results

Discussion

Footnotes

Acknowledgments

Disclosure Statement

References