26 Minimally Invasive Versus Open Esophagectomy for Cancer

218

26

Minimally Invasive Versus Open Esophagectomy for Cancer

Ara Ketchedjian and Hiran Fernando

26.1. Operative Procedure and Feasibility

Minimally invasive esophagectomy techniques require advanced laparoscopic and thoracoscopic skills for optimal outcomes. Due to the inherent limitations in visualization and instrumentation, operative times are often longer and vary widely (3.7–7.5 h; Table 26.1). The earliest descriptions of MIE involved a combination of open surgery with either thoracoscopy or laparoscopy. In 1993, Collard demonstrated that esophageal dissection could be carried out thoracoscopically when combined with laparotomy for gastric mobiliza- tion. ¹ The disadvantage of a hybrid approach such as this is that the patient is still subjected to the morbidity of the open approach in the abdomen. The fi rst report of a completely mini- mally invasive approach was by Depaula, who described a laparoscopic transhiatal esophagec- tomy. ² Swanstrom and colleagues later described the fi rst North American experience using the same approach as Depaula. ³ Luketich and cowork- ers further modifi ed the approach utilizing both laparoscopy and thoracoscopy to achieve esopha- gectomy. ⁴ This modifi cation was added to help with visualization and dissection of the thoracic esophagus, as well as to achieve a more complete lymph node dissection. As with most new tech- nologies and procedures, there is a continuous evolution of technique in an attempt to improve operative outcome and ease of surgery. Other techniques such as robotic esophagectomy have been reported, but currently the experience with this approach is relatively small. ⁵

Despite advances in medical and radiation oncol- ogy, esophagectomy continues to remain the cor- nerstone of therapy for esophageal cancer when cure is the goal. The surgical approaches to esophagectomy, however, vary by institution. In many cases patients with esophageal cancer are older with signifi cant comorbid diseases. Open approaches to esophagectomy can often carry signifi cant morbidity and mortality for these compromised patients. Minimally invasive strat- egies, bolstered by improving techniques and technology, have made minimally invasive esophagectomy (MIE) a feasible operative strat- egy for esophageal cancer surgery. Minimally invasive surgery offers the potential for faster postoperative recovery and fewer pulmonary complications. Much like open surgery, MIE approaches and techniques differ based on insti- tution and surgeon. The goal, however, regardless of the approach, is complete resection of all cancer. Whether MIE can provide added benefi t to morbidity, mortality, or postoperative recov- ery without compromising oncologic resection continues to be a topic of debate.

Minimally invasive esophagectomy remains a

relatively new approach for the treatment of

esophageal cancer with a paucity of level 1 evi-

dence comparing it to standard open esophageal

surgery. A majority of the literature on MIE

refl ects institutional-based observations and

experience. This chapter will review the litera-

ture on both open and minimally invasive esoph-

agectomy, comparing the relevant factors that

may infl uence a surgeon’s approach to esopha-

geal cancer surgery.

Even for open esophagectomy there is some con- troversy as to which operative approach is best.

Prospective, randomized trials comparing tran- shiatal and transthoracic procedures have demon- strated no signifi cant difference in survival. ^6–8 Additionally, there are differences in outcome when comparing low-volume to high-volume esophageal centers. Birkmeyer and colleagues, in reviewing a national database, reported mortality rates ranging from 8% in high-volume centers to as high as 23% in low-volume centers. ⁹ In the absence of a randomized trial, the differences in outcome between centers is an additional source of bias when trying to compare surgical approaches.

With regards to techniques for open esopha- gectomy, surgeons tend to prefer one approach over another. Advocates of transhiatal esopha- gectomy favor this approach because it avoids thoracotomy and all its associated morbidities. In comparison, achieving an R0 resection has been stressed by others as the most important factor for attaining cure, suggesting that a more exten-

sive dissection accomplished by an open thoracotomy approach is superior. ¹⁰ Extended (three-fi eld) lymph node dissection and en bloc resection are being used to optimize the number of harvested lymph nodes in an attempt to ac complish R0 resection. Some groups have also reported en bloc resections using minimally invasive techniques, although they failed to dem- onstrate any improvement in morbidity. ^11,12 Although en bloc resections have been demon- strated to be safe at high-volume centers, they are associated with higher morbidity.

26.2. Studies Comparing Open and Minimally Invasive Esophagectomy

There have been no randomized studies that compare MIE to open esophagectomy (OE). There are two retrospective studies that have compared MIE to OE. ^13,14 In the fi rst study, 18 MIE were compared to 16 OE. The authors found that the T ABLE 26.1. Minimally invasive esophagectomy – surgical outcome.

Surgeon n Evidence Operative approach (h) Operation time LOS (days) Mortality (%) Total

MIE

DePaula

12 Retrospective Lap THE 4.3 7.6 0 Swanstrom

9 Retrospective Lap THE 6.5 6.4 0

Watson

7 Retrospective MIE 4.4 12 0

Luketich

222 Retrospective MIE – 7 1.4

Nguyen

46 Retrospective MIE 5.8 8 4.3

Avital

22 Retrospective Lap THE 6.3 8 4.5 Hybrid

Liu

20 Retrospective VATS/laparotomy 4.6

19 0 Peracchia

18 Retrospective VATS/laparotomy 5.6 – 5.5 Law

18 Retrospective VATS/laparotomy 4 – 0 Kawahara

23 Retrospective VATS/laparotomy 1.8

26 0 Smithers

153 Retrospective VATS/laparotomy 5.0 12 3.3 Osugi

80 Retrospective VATS/laparotomy 3.7 – 0 Open

Mathisen

104 Retrospective TA (64)/IL (40) – – 2.9 Lerut

198 Retrospective Open (varied) – 18 9.6 Orringer

1085 Retrospective THE – 10 4 Swanson

250 Retrospective Three-hole – 13 3.6 Bailey

1777 Retrospective Open (varied) – – 9.8 Rizk

510 Retrospective Open (varied) – 23

6.1

11

IL, Ivor Lewis; Lap, laparoscopic; MIE, minimally invasive esophagectomy; TA, left thoraco-abdominal; THE, transhiatal esophagectomy; VATS, video-assisted thorascopic surgery.

a

VATS portion only.

b

Patients with complications.

c

Patients without complications.

mean operative time (364 min), blood loss (297 mL), and length of intensive care unit stay (6.1 days) were decreased compared with open transthoracic esophagectomy (437 min, 1046 mL, 9.9 days) and blunt transhiatal esophagectomy (391 min, 1142 mL, 11.1 days). ¹⁴ The incidence of respiratory complications (pneumonia, pulmo- nary embolism, respiratory failure) was similar among the groups. It should be emphasized, however, that there were signifi cant differences between the groups in this retrospective com- parison. The open patients had more advanced cancers whereas the MIE group had more patients with high-grade dysplasia or a benign disorder requiring esophagectomy. Additionally, the open operations were performed by a group of four surgeons with variable experience with esopha- geal surgery, whereas the MIE procedures were performed by a single surgeon with specifi c expertise in minimally invasive esophageal surgery. The open operations were performed several years before the MIE procedures, so there may also have been differences in practice pat- terns accounting for the longer lengths of stay.

The second comparative study included 25 lapa- roscopic transhiatal (with the use of a handport) and 20 open transhiatal esophagectomies. It should be noted that there was a relatively high incidence (36%) of conversions to laparotomy in the MIE group. Not unexpectedly, the authors demonstrated a signifi cantly longer operative

time in the MIE group (300 vs. 257 min). In favor of MIE, however, there was a signifi cantly shorter intensive care unit stay (1 vs. 2 days) and blood loss (600 vs. 900 mL) in these patients compared to the open procedures. Otherwise there was no difference in perioperative outcome.

In the MIE series by Luketich, the median ICU stay was 1 day, time to oral intake was 4 days, and hospital stay was 7 days. This minimally invasive approach which utilizes thoracoscopy compares favorably with outcomes after laparoscopic tran- shiatal and is better than most series of open esophagectomy (Table 26.1). ¹⁵

26.3. Morbidity and Mortality

As discussed above, there are no randomized or published prospective trials involving MIE. In the absence of such data the best option is to compare the best published results with those reported after open operation. Although mortal- ity is usually reported in esophagectomy series, total morbidity is not. Reports of morbidity typi- cally target specifi c outcomes such as anasto- motic leak and pneumonia rates, making comparisons of morbidity challenging. For this reason, rather than comparing overall morbidity, we have compared the reported rates of specifi c complications after MIE, hybrid, and OE from different series in Tables 26.2 and 26.3.

T ABLE 26.2. Minimally invasive esophagectomy – recurrence and survival.

Follow-up Survival (%) Loco-regional Year n Evidence Approach (months) Median (mos) 1 year 3 years 5 years recurrence l MIE

Swanstrom

1997 9 Retrospective Lap THE 13 – – – – 22.2 Nguyen

2003 46 Retrospective MIE (41 IL) 26 – 87 57 – 26.1 Luketich

2003 222 Retrospective MIE 19 26 69% 45% 36 – Hybrid

Peracchia

1997 18 Retrospective VATS/laparotomy 17 – – – – 16.6 Law

1997 18 Retrospective VATS/laparotomy 13.7 – 81 – – 44.4 Kawahara

1999 23 Retrospective VATS/laparotomy – – – – – 30.4 Smithers

2001 153 Retrospective VATS/laparotomy 21 29 70 – 40 – Open

Mathisen

1988 104 Retrospective TA (64)/IL (40) – – – – 15 5.8

Lerut

1992 198 Retrospective Open (varied) >24 – 63 – 30 –

Orringer

1999 1085 Retrospective THE 27 – 67 34 23 –

Swanson

2001 250 Retrospective Three-hole 24 25 44 – – 5.6

Rizk

2004 510 Retrospective Open (varied) – – 44 – – –

IL, Ivor Lewis; Lap, laparoscopic; MIE, minimally invasive esophagectomy; TA, left thoraco-abdominal; THE, transhiatal esophagectomy; VATS,

video-assisted thoracoscopic surgery.

26.3.1. Mortality

Mortality was 1.5% in the Pittsburgh series and 4.5% from the University of California, Davis series, the two largest MIE reported experiences to date. This compares favorably with other open series, where typically mortality is 5% or less when reported from large-volume esophageal centers. Bailey recently reported on a prospective multicenter series of 1777 patients all from the Veterans Administration (VA) system. ¹⁶ This is one of the largest studies of its kind. Mortality in this study was higher at 9.8%. Similarly, the report analyzing outcomes from the Leapfrog database indicated that mortality even in high- volume esophageal centers was around 8%. ⁹ A prospective, nonrandomized phase II study of MIE currently is being conducted by the Eastern Cooperative Oncology Group and the Cancer and Leukemia Group B (E2202). The goal of E2202 is look at the feasibility of MIE in a multicenter setting, with perioperative mortality being the primary end point.

26.3.2. Complications

In the largest series of MIE, major complications occurred in 32% of patients. ¹⁵ The most common major complication was anastomotic leak, which occurred in 11% of patients overall. The leak rate in this series was infl uenced by technique.

Mid-series a narrow gastric tube (4 cm or less) was utilized and resulted in a very high leak rate of 25.9%. Because of these results the authors subsequently reverted back to a wider gastric tube (6 cm or more) and reported a lower leak rate of 6.1%. In the University of Michigan series of 1085 transhiatal esophagectomies, the overall leak rate was 13%. ¹⁷ More recently, the same group has reported a signifi cant reduction in the

leak rate to 2.7% using a side-to-side stapled anastomosis. ¹⁸ Risk and colleagues recently reported the results from Memorial Sloan- Kettering in 510 open esophagectomies. ¹⁹ Anas- tomotic leak rates were higher (21%) in this group of patients.

Pneumonia has been shown to be a signifi cant predictor of mortality and morbidity after esoph- agectomy. ²⁰ Pneumonia was the second most common major complication in the Pittsburgh series of MIE, occurring in 7.7% of patients. ¹⁵ This pneumonia rate is lower than the reported rates after open approaches that include a signifi - cant number of thoracotomies (15%–30%) but is higher than the 2% pneumonia rate reported after the largest series of transhiatal esophagec- tomies. ¹⁷ In the University of California Davis series of MIE, the most frequent complications were anastomotic leaks (11%) and respiratory failure (11%), which are similar to those in other series. The most frequent minor complication in the Pittsburgh MIE series was atrial fi brillation occurring in 12%. ¹⁵ Atrial fi brillation has been reported to occur in between 20% to 25% of patients after OE. ²¹

26.4. Recurrence and Survival

There is scant data on long-term survival and recurrence patterns following minimally inva- sive approaches to esophagectomy. In the single institution MIE series by Luketich and associates, Kaplan–Meier estimates of survival based on stage were similar to those in the open litera- ture. ¹⁵ Although not presented in that original publication, re-analysis of the original dataset of 222 patients with esophageal cancer demon- strated 1-, 3-, and 5-year survivals of 69%, 45%, and 36%, respectively, which are similar if not T ABLE 26.3. Postoperative complications after esophagectomy.

Number Type of Myocardial Anastomotic Atrial Author of patients procedure Pneumonia infarction leak Chylothorax fibrillation

Whooley

710 Open 17 8 3.5 1.7 23

Atkins

NA Open 15.8 1.1 14 3 13.7

Ferguson

269 Open 27 2 16 4 36

Luketich

222 MIE 7.7 1.8 11.7 3.2 12

Nguyen

46 MIE 2.1 2.1 8.7 na na

Abbreviation: na, not applicable.

better than for some open series (Table 26.3). In the University of California at Davis MIE series, there were 87% 1-year and 57% 3-year survival rates in 46 patients. ²² Avital and colleagues in the most recently published MIE series reported a 61% survival at 30-month follow-up. ²³ It should be emphasized, however, that this study included a relatively large number of early-stage cancers, with 84% of the patients having either stage I or II tumors. Loco-regional recurrence rates of between 16% and 44% have been documented in minimally invasive series, which is on par with the known natural history of resected esophageal cancer using open techniques. Prospective, con- trolled studies will be required to more accurately delineate the survival and recurrence patterns afforded by MIE compared to open techniques (Table 26.2).

26.5. Pain and Quality of Life

There are no specifi c analyses of postoperative pain in the MIE literature. Studies comparing video-assisted thorascopic surgery (VATS) or thoracotomy for lung resection have demon- strated less pain, better preservation of lung function, and improved shoulder function with VATS. ^24,25 Whether this holds true after MIE needs to be determined.

Quality of life (QOL) is a critical factor in the management of patients with esophageal cancer.

Headrick and associates have found that on long- term follow-up, esophagectomy can be performed with little to no impairment in QOL compared with normal patients based on SF36 scoring. ²⁶ Similarly, Blazeby and co-authors found that QOL initially was diminished in patients under- going resection for esophageal carcinoma, but improved back to baseline in those patients sur- viving for 2 years following esophagectomy. ²⁷ In the Pittsburgh series of 222 MIE patients, the mean postoperative dysphagia score was 1.4 on a scale from 1 (no dysphagia) to 5 (severe dyspha- gia). ¹⁵ The presence of dysphagia after esopha- gectomy, particularly if performed in a relatively asymptomatic patient such as those with high- grade dysplasia, can have a signifi cant effect on QOL. Overall QOL using the SF36 were also mea- sured and were not signifi cantly different com-

pared to age-matched normal values during follow-up after MIE.

26.6. Summary

Currently, experience with MIE is relatively small, and published results are mostly single institution reports. It should be emphasized that there is no level 1 data comparing OE and MIE.

The only trials that have compared MIE to OE were level 3b (single-institution case control) studies. ^13,14 The fi rst study was biased in terms of case mix and surgeon experience favoring the MIE cases, whereas the second study included a relatively large number of conversions in the MIE group, suggesting that this was early in the sur- geons learning curve. Otherwise, the data sup- porting MIE is primarily level 4 (single institution case series). However, this is also the case for OE where the best reported results in terms of mor- bidity and mortality are from single institution high-volume esophageal centers. Comparison of such MIE and OE reports indicates that MIE is associated with at least equivalent results in terms of mortality, morbidity, and survival after esophagectomy (recommendation grade C).

Although pain control and pulmonary function have not been compared after different esopha- gectomy approaches, there is level 3B evidence suggesting that both of these outcomes are better with VATS compared to thoracotomy (recom- mendation grade C). ^24,25 Similarly, QOL has rarely been addressed in esophagectomy studies. The data that exists is primarily level 4 for both OE and MIE and indicate that with longer follow-up that QOL is similar to normal value patients (rec- ommendation grade C). ^15,26,27

Minimally invasive esophagectomy is associ- ated with at least equivalent results in terms of mortality, morbidity, and survival as open esophagectomy (level of evidence 3b to 4; rec- ommendation grade C).

Pain control and pulmonary function may

be better after VATS compared to thoracotomy

for esophagectomy (level of evidence 3b; rec-

ommendation grade C).

The differences in case mix, experiences of the surgeon and centers involved, as well as a number of alternative open approaches make it diffi cult to draw defi nitive conclusions about whether MIE has real advantages over OE. The prospective E2202 trial will answer some questions about the utility of MIE. It should be emphasized that esophagectomy, whether performed by an open or minimally invasive approach, is a complex proce- dure and outcomes are better in high-volume centers. Another issue with MIE is the steep learn- ing curve required to master these minimally invasive techniques, so it is likely that only a few centers with expertise in both minimally invasive techniques and open esophageal surgery will adopt this approach. Nevertheless, the results are encouraging and may broaden the applicability of this technique to higher-risk patient groups such as the elderly. ²⁸ Prospective studies will be required to determine whether postoperative pain, recov- ery time, and cost are improved. As with VATS lobectomy, there will likely be a cadre of surgeons performing MIE and another group performing OE, all with excellent results. A randomized study may not be feasible because of institutional prefer- ences, and so a prospective registry oriented series may be the best option to help elucidate whether the perceived advantages of MIE hold true.

References

1. Collard JM, Lengele B, Otte JB, Kestens PJ. En bloc and standard esophagectomies by thoracoscopy.

Ann Thorac Surg 1993;56:675–679.

2. DePaula AL, Hashiba K, Ferreira EA, de Paula RA, Grecco E. Laparoscopic transhiatal esophagec- tomy with esophagogastroplasty. Surg Laparosc Endosc 1995;5:1–5.

3. Swanstrom LL, Hansen P. Laparoscopic total esophagectomy. Arch Surg 1997;132:943–947; dis- cussion 7–9.

4. Luketich JD, Nguyen NT, Schauer PR. Laparo- scopic transhiatal esophagectomy for Barrett’s esophagus with high grade dysplasia. JSLS 1998;2:

75–77.

5. Elli E, Espat NJ, Berger R, Jacobsen G, Knoblock L, Horgan S. Robotic-assisted thoracoscopic resec- tion of esophageal leiomyoma. Surg Endosc 2004;18:713–716.

6. Goldminc M, Maddern G, Le Prise E, Meunier B, Campion JP, Launois B. Oesophagectomy by a

transhiatal approach or thoracotomy: a prospec- tive randomized trial. Br J Surg 1993;80:367–370.

7. Chu KM, Law SY, Fok M, Wong J. A prospective randomized comparison of transhiatal and trans- thoracic resection for lower-third esophageal car- cinoma. Am J Surg 1997;174:320–324.

8. Hulscher JB, van Sandick JW, de Boer AG, et al.

Extended transthoracic resection compared with limited transhiatal resection for adenocarcinoma of the esophagus. N Engl J Med 2002;347:1662–

1669.

9. Birkmeyer JD, Siewers AE, Finlayson EV, et al.

Hospital volume and surgical mortality in the United States. N Engl J Med 2002;346:1128–1137.

10. Hermanek P. pTNM and residual tumor classifi ca- tions: problems of assessment and prognostic sig- nifi cance. World J Surg 1995;19:184–190.

11. Akaishi T, Kaneda I, Higuchi N, et al. Thoraco- scopic en bloc total esophagectomy with radical mediastinal lymphadenectomy. J Thorac Cardio- vasc Surg 1996;112:1533–1540; discussion 40–41.

12. Osugi H, Takemura M, Higashino M, Takada N, Lee S, Kinoshita H. A comparison of video-assisted thoracoscopic oesophagectomy and radical lymph node dissection for squamous cell cancer of the oesophagus with open operation. Br J Surg 2003;90:108–113.

13. Nguyen NT, Follette DM, Wolfe BM, Schneider PD, Roberts P, Goodnight JE Jr. Comparison of mini- mally invasive esophagectomy with transthoracic and transhiatal esophagectomy. Arch Surg 2000;

135:920–925.

14. Van den Broek WT, Makay O, Berends FJ, et al.

Laparoscopically assisted transhiatal resection for malignancies of the distal esophagus. Surg Endosc 2004;18:812–817.

15. Luketich JD, Alvelo-Rivera M, Buenaventura PO, et al. Minimally invasive esophagectomy: out- comes in 222 patients. Ann Surg 2003;238:486–494;

discussion 94–95.

16. Bailey SH, Bull DA, Harpole DH, et al. Outcomes after esophagectomy: a ten-year prospective cohort. Ann Thorac Surg 2003;75:217–222; discus- sion 222.

17. Orringer MB, Marshall B, Iannettoni MD. Tran- shiatal esophagectomy: clinical experience and refi nements. Ann Surg 1999;230:392–400; discus- sion 403.

18. Orringer MB, Marshall B, Iannettoni MD. Elimi- nating the cervical esophagogastric anastomotic leak with a side-to-side stapled anastomosis. J Thorac Cardiovasc Surg 2000;119:277–288.

19. Rizk NP, Bach PB, Schrag D, et al. The impact of

complications on outcomes after resection for

esophageal and gastroesophageal junction carci- noma. J Am Coll Surg 2004;198:42–50.

20. Atkins BZ, Shah AS, Hutcheson KA, et al. Reduc- ing hospital morbidity and mortality following esophagectomy. Ann Thorac Surg 2004;78:1170–

1176; discussion 1176.

21. Murthy SC, Law S, Whooley BP, Alexandrou A, Chu KM, Wong J. Atrial fi brillation after esopha- gectomy is a marker for postoperative morbidity and mortality. J Thorac Cardiovasc Surg 2003;126:

1162–1167.

22. Nguyen NT, Roberts P, Follette DM, Rivers R, Wolfe BM. Thoracoscopic and laparoscopic esoph- agectomy for benign and malignant disease:

lessons learned from 46 consecutive procedures. J Am Coll Surg 2003;197:902–913.

23. Avital S, Zundel N, Szomstein S, Rosenthal R.

Laparoscopic transhiatal esophagectomy for esophageal cancer. Am J Surg 2005;190:69–74.

24. Ninomiya M, Nakajima J, Tanaka M, et al. Effects of lung metastasectomy on respiratory function.

Jpn J Thorac Cardiovasc Surg 2001;49:17–20.

25. Landreneau RJ, Mack MJ, Hazelrigg SR, et al.

Prevalence of chronic pain after pulmonary resec- tion by thoracotomy or video-assisted thoracic surgery. J Thorac Cardiovasc Surg 1994;107:1079–

1085; discussion 85–86.

26. Headrick JR, Nichols FC 3rd, Miller DL, et al.

High-grade esophageal dysplasia: long-term sur- vival and quality of life after esophagectomy. Ann Thorac Surg 2002;73:1697–1702; discussion 1702–1703.

27. Blazeby JM, Farndon JR, Donovan J, Alderson D.

A prospective longitudinal study examining the quality of life of patients with esophageal carci- noma. Cancer 2000;88:1781–1787.

28. Perry Y, Fernando HC, Buenaventura PO, Christie NA, Luketich JD. Minimally invasive esophagec- tomy in the elderly. Jsls 2002;6:299–304.

29. Watson DI, Jamieson GG, Devitt PG. Endoscopic cervico-thoraco-abdominal esophagectomy. J Am Coll Surg 2000;190:372–378.

30. Nguyen NT, Roberts PF, Follette DM, et al. Evalu- ation of minimally invasive surgical staging for esophageal cancer. Am J Surg 2001;182:702–706.

31. Liu HP, Chang CH, Lin PJ, Chang JP. Video- assisted endoscopic esophagectomy with stapled intrathoracic esophagogastric anastomosis. World J Surg 1995;19:745–747.

32. Peracchia A, Rosati R, Fumagalli U, Bona S, Chella B. Thoracoscopic esophagectomy: are there bene- fi ts? Semin Surg Oncol 1997;13:259–262.

33. Law S, Fok M, Chu KM, Wong J. Thoracoscopic esophagectomy for esophageal cancer. Surgery 1997;122:8–14.

34. Kawahara K, Maekawa T, Okabayashi K, et al.

Video-assisted thoracoscopic esophagectomy for esophageal cancer. Surg Endosc 1999;13:218–223.

35. Smithers BM, Gotley DC, McEwan D, Martin I, Bessell J, Doyle L. Thoracoscopic mobilization of the esophagus. A 6 year experience. Surg Endosc 2001;15:176–182.

36. Mathisen DJ, Grillo HC, Wilkins EW Jr, Moncure AC, Hilgenberg AD. Transthoracic esophagec- tomy: a safe approach to carcinoma of the esopha- gus. Ann Thorac Surg 1988;45:137–143.

37. Lerut T, De Leyn P, Coosemans W, Van Raem- donck D, Scheys I, LeSaffre E. Surgical strategies in esophageal carcinoma with emphasis on radical lymphadenectomy. Ann Surg 1992;216:583–590.

38. Swanson SJ, Batirel HF, Bueno R, et al. Transtho- racic esophagectomy with radical mediastinal and abdominal lymph node dissection and cervical esophagogastrostomy for esophageal carcinoma.

Ann Thorac Surg 2001;72:1918–1924; discussion 1924–1925.

39. Whooley BP, Law S, Murthy SC, Alexandrou A, Wong J. Analysis of reduced death and complica- tion rates after esophageal resection. Ann Surg 2001;233:338–344.

40. Ferguson MK, Martin TR, Reeder LB, Olak J. Mor- tality after esophagectomy: risk factor analysis.

World J Surg 1997;21:599–603; discussion 604.