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Esophagectomy with or without thoracotomy
General Thoracic Surgery
Esophagectomy with or without thoracotomy Is there any difference? Two operative approaches for esophageal carcinoma were compared with respect to operative morbidity and mortality by means of multivariable analysis. From 1980 to 1986, 152 patients underwent resection by laparotomy and right-sided anterolateral thoracotomy with an intrathoracic anastomosis. From 1986 to 1989, 141 patients underwent resection by transhiatal blunt dissection with a cervical anastomosis. The stomach was the preferred organ for reconstruction. Paresis of the recurrent laryngeal nerve and leakage of the cervical anastomosis occurred significantly more often in the transhiatal group. Pulmonary complications occurred less frequently in the transhiatal group. In-hospital mortality (9 % in the thoracotomy group and 5 % in the transhiatal group) increased significantly with advanced age of the patients. Furthermore, it was significantly higher in case of colonic interposition as compared with reconstruction with the stomach. Long-term survival did not differ between the two groups. Especially for carcinomas in the distal part of the esophagus, transhiatal esophageal resection without thoracotomy seems to be an oncologically justifiable operation with a reduced morbidity and mortality. (J THORAC CARDIOVASC SURG 1993;105:898-903)
Hugo W. Tilanus, MD, Willem C. J. Hop, MSc,a Bernhard L. A. M. Langenhorst, MD, and J. Jan B. van Lanschot, MD, Rotterdam, The Netherlands*
Carcinoma of the esophagus has a dismal prognosis once the diagnosis is clear. Because the disease is usually detected late in its course, metastatic spread is common. About half ofthe patients present with a resectable tumor, but mortality after the operation used to be as high as 25% in different series.l' This mortality was mainly due to pulmonary insufficiency, dehiscence of the intrathoracic anastomosis, or a combination of these two factors.t" To diminish the postoperative mortality, we changed
our therapeutic approach in 1986 from a laparotomy and a right-sided anterolateral thoracotomy with an intrathoracic anastomosis to transhiatal esophagectomy with blunt dissection and cervical anastomosis. The last 152 patients from the first group and the first 141 patients from the last group are compared with regard to operative morbidity, in-hospital mortality, and survival after resection.
From the Departments of Surgery and Epidemiology & Biostatistics; Erasmus University Hospital, Rotterdam, The Netherlands.
From January 1, 1980, until November 1, 1986, 152 patients with carcinoma of the esophagus or gastroesophageal junction underwent esophageal resection and reconstruction by rightsided anterolateral thoracotomy and laparotomy with a mostly intrathoracic anastomosis (group T). From November I, 1986, until January I, 1990, 141 patients underwent esophagectomy for carcinoma by laparotomy and right-sided neck incision with a blunt disection of the esophagus and cervical anastomosis (group B). No regular lymph node dissection was performed in either group. Patients who underwent an exploratory laparotomy without resection were excluded from this study. Also
Received for publication Oct. 28,1991. Accepted for publication July 27,1992. Address for reprints: H.W. Tilanus, MD, Department of Surgery, Dijkzigt Ziekenhuis, Dr. Molewaterplein 40:3015 GO Rotterdam, The Netherlands. *The Rotterdam Esophageal Tumor Study Group. Copyright © 1993 by Mosby-Year Book, Inc.
0022-5223/93 $1.00+ .10 12/1/41630
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Patients and methods
The Journal of Thoracic and Cardiovascular Surgery Volume 105, Number 5
Table I. Characteristics ofpatients operated on for esophageal carcinoma with (group T, n = 152) or without (group E, n = 141) thoracotomy Thoracotomy
Men Women Location * Upper third Middle third Lower third Differentiation Squamous cell carcinoma Adenocarcinoma Other Reconstruction Stomach Colon
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Tilanus et al.
Table II. Number ofpatients with complications after esophageal resection with (group T, n = 152) or without (group E, n = 141) thoracotomy Thoracotomy Blunt dissection
Blunt dissection
%
Complication
No.
%
No.
%
p Value
102 39
72 28
9 20 III
6 14 79
50
77
7 12 3 22* I I 36 24 37
5 9 2 16 I I 26 17 28
14
35 55 10
9 7 5 6 5 4 II 34 9
13
62 29 9
13 10 8 9* 7 6 16 51 12
NS NS NS
14 26 60
In-hospital mortality Hemorrhage Chylothorax Paresis Wound infection Delayed emptying Anastomotic leak Pulmonary complication Late stenosis
115 37
76 24
128 13
91 9
No.
%
No.
107 45
70 30
21 40 91 95 44
The mean age in groupTwas 60 years (range 30 to 83) and in group B, 61 years (range 35 to 82). "Missingdata in one patient in group B.
excludedwere patients with a carcinoma of the cervical esophagus because in a substantial number of these patients a simultaneous laryngopharyngectomy was performed. Patient and tumor characteristics are summarized in Table I. Gender and age distribution did not differ significantly between the groups. In group T there were more tumors localizedin the upper and middle thirds of the esophagus(40%) than in group B (20%). This difference is significant and reflects the difference in histologic differentiation. During this study the stomach increasingly became the preferred organ for reconstruction. In later years the colon was used only in patients with a previousstomach resection or gross tumor involvementof the stomach. Statistics. Percentages werecompared by Fisher's exact test. Multivariate analysisof percentages of various types of complications,exceptparesisofthe recurrent laryngeal nerve,wasdone by logistic regression7 in case the complication occurred in at least 10 patients. Survival curves were constructed by the Kaplan-Meier method and compared with the log rank test. No patients were lostto follow-up. Statistical significancewas set at p < 0.05 (two-sided).
Results In group T the stomach was the preferred organ for reconstruction in 76% of the patients and in group B, for more than 90% of the patients. Operations without a thoracotomy lasted on the average 1 hour less than resection with a thoracotomy (3l/2 hours versus 2Y2 hours). Pyloromyotomy or pyloroplasty was highly favored in group T, but in group B the pylorus was left untouched. No late pyloric procedures had to be performed. Postoperative ventilation time did not significantly differ between the two groups. The majority of patients were extubated within 12 hours after the operation.
p
p
NS, Not significant. "[ncluding one case of bilateral paresis in group T and two in group B.
Table III. Multivariate analysis of the probability of postoperative death according to resection method, type of reconstruction, location of tumor, presence of concomitant disease (cardiac or pulmonary), gender, and age Factor Resection Group T Group B Reconstruction Stomach Colon Location Lower esophagus Upper/middle Concomitant disease No
Odds ratio I 0.7 I 5.0
Significance
p=0.51
p
= 0.002
I 0.8
p= 0.74
Yes
I 1.5
p
Sex Male Female Age (yr)
I 1.6 1.7*
= 0.49
p= 0.38 p= 0.04
Data given are ratios of the odds of death against survival. Odds ratios greater (smaller) than I indicate an increased (decreased)operative mortality. "Relative to 10 years younger.
Postoperative complications are summarized in Table II. The in-hospital mortality for group Twas 9% and for group B, 5%. This difference is not significant (p = 0.25). Multivariate analysis of the factors concomitant diseases (cardiac, pulmonary), age, gender, type of reconstruction, localization of tumor, and type of resection (T, B) showed that the only significant factors regarding in-hospital mortality were age and type of reconstruction (TableIII). With increasing age, in-hospital mortality gradually
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survival
survival Squamous (n=95) .... Adeno (n=44)
100%
40%
.......
100%
40%
......
'
.. ..
". ..
20%
20% 0%
Squamous (n=50) .... Adeno (n=77)
l..-_ _----'-
J -_ _---'
o
24
12
36
- L -_ _- - - '
48
60
month
0%
0
12
36
24
48
60
month
Fig. 1. Survival after operation according to histologic type for patientswith squamous cellcarcinoma or adenocarcinoma for groupsT and B.
Table IV. Multivariate analysis of various complications Factor Resection Group T Group B Age <65 yr >65 yr Location Lower esophagus Upper/middle Reconstruction Stomach Colon COPD No Yes
Hemorrhage
Chylothorax
Leakage of anastomosis
Pulmonary complications
Late stenosis
1
1
1
1
1
1.5 (0.41)
0.4 (0.23)
3.4 (0.001)
0.5 (0.03)
4.1 «0.001)
I 0.6 (0.20)
1
1
1
1
0.6 (0.30)
1.0 (0.98)
1.3 (0.48)
1.0 (0.97)
I 1.7 (0.27)
1
I 1.5 (0.29)
1
1.6 (0.45)
1.4 (0.30)
I 1.5 (0.28)
I 0.8 (0.78)
I 0.9 (0.89)
I 1.9 (0.13)
I 1.2 (0.67)
I 0.3 (0.08)
Not tested
Not tested
Not tested
1
Not tested
1.2 (0.65)
For each type of complication, data given are the ratios of the odds of its occurrence against its absence according to various variables; p values are given in parentheses. COPD, Chronic obstructive pulmonary disease.
increased. Colonic interposition was associated with a significantly higher mortality than stomach tube reconstruction. For patients aged at most 65 years, in-hospital mortality was 14% (5/36) in case of colonic interposition and 3% (4/160) in case of stomach tube reconstruction. These figures for the patients aged above 65 years were, respectively, 29% (4/14) and 8% (7/83). Adjusted for the factors age and type of reconstruction, no significant difference was found between group T and group B. Postoperative hemorrhage necessitating reoperation occurred equally in both resection groups, 7% (group T) versus 9% (group B), including four patients in group B who needed an emergency thoracotomy during blunt dissection for control of intrathoracic bleeding. All four of these cases involved a carcinoma ofthe middle third ofthe intrathoracic esophagus. Table IV, which also summa-
rizes other complications, gives results of the multivariate analysis of the occurrence of hemorrhage in relation to the resection group, age, location of tumor, and type of reconstruction. None of these variables was significantly related to hemorrhage. No significant differences were seen between groups T and B with respect to the occurrence of chylothorax. Multivariate analysis (Table IV) of the factors resection method, age, reconstruction type, and location of the tumor showed that none of them significantly correlated with chylothorax. Paresis of the recurrent laryngeal nerve was significantly more frequent in group B (p < 0.01). The paresis was reversible except in six patients. The percentage of patients with wound infection did not differ significantly between the two resection groups. Age and type of reconstruction were also not significantly related to the occur-
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Cardiovascular Surgery Volume 105, Number 5
survival
survival 100%
100%
Stage I (n=30) Stage II (n=76) .... Stage III/IV (n=29)
80%
60%
60%
40%
40%
20%
20%
0%
90 I
L -_ _----'-
-'--_ _---'
--'-_ _- - l
o
24
48
12
36
60
month
Stage I (n=19) Stage II (n=65) ..... Stage III/IV (n=49)
0% '--------'-----'---_---' o 12 24 36 month
--'-_ _- - J 48 60
Fig. 2. Survivalafter operation according to stage for patients with squamous cell carcinoma or adenocarcinoma for groups T and B (stage missing: each group, four patients).
renee of wound infection. Similar findings applied to delayed emptying of the reconstructed esophagus. Leakage of the anastomosis, defined as radiologic leak or clinical fistula, was seen in 16 patients (11%) in group T and 36 patients (26%) in group B (p < 0.01). This difference remains significant after adjustment for other factors investigated (Table IV). The same applied when only the occurrence of clinical fistula (5% in group T, 13% in group B) was analyzed. Pulmonary complications including respiratory distress syndrome differed (p < 0.0 I) between the resection groups in favor of group B. This difference remains significant (Table IV) after adjustment for chronic aspecific respiratory ailment, age, tumor location and reconstruction type. The latter factors themselves, though, were not significantly related to pulmonary complications. In analyzing late stenotic complications of the anastomosis, we excluded patients who died after the operation. The difference between the two resection groups was also significant in favor of group T (p < 0.01) when adjusted for the type of reconstruction (Table IV). The multivariate analysis further revealed that a trend (p = 0.08) existed toward more late stenotic complications after reconstruction with the stomach as compared with colonic interposition. In group T II % of patients with stomach reconstruction had late stenotic complications, whereas this percentage was 0% in those with colonic interposition. These percentages for group B were, respectively, 29% and 18%. No significant correlation was found between anastomotic leakage and late stenotic complications (p = 0.3). Survival of the patients of both groups is analyzed according to histologic type in Fig. I. The difference in survival between the two histologic types within each group is not significant. Survival according to stage for
both treatment groups is seen in Fig. 2. In each group survival decreased significantly with increasing stage. There are no significant differences between the two treatment groups (adjusted for stage, p = 0.34). Discussion Carcinoma of the esophagus is a disseminated disease in the majority of patients at the moment of the diagnosis. About half of the patients have a resectable tumor at first presentation, and even this group has a 5-year survival of less than 20% after resection.v" Adjuvant radiotherapeutic or chemotherapeutic regimens did not substantially improve these disappointing results.P!" Extension of the operative procedure with an en bloc lymphadenectomy did not significantly influence the long-term survival and may increase postoperative pulmonary complications.P: 16 Most authors believe that the goal of surgical treatment of esophageal carcinoma is locoregional control of "at presentation" metastatic disease. This should be attained with the lowest possible morbidity and mortality. Unfortunately, in the past resection was accompanied by a high postoperative mortality of 25% or more. 17-20 Major causes of this mortality and morbidity were pulmonary complications and dehiscence of the intrathoracic anastomosis.v 21, 22 In 1979, esophageal resection by laparotomy and a separate right anterolateral thoracotomy was introduced in our hospital. With this method the patient lies in the supine position during the operation and the right lung is desuffiated during the intrathoracic phase of the 'operation, After esophageal resection the continuity of the digestive tract was restored by gastric tube reconstruction with a mostly intrathoracic anastomosis.P One hundred fifty-two consecutive patients were operated on in this manner until the operative approach was changed to the transhiatal esoph-
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Tilanus et al.
agectomy without thoracotomy in November 1986. This method is extensively described elsewhere.i" Throughout the entire period, the stomach was the preferred organ for esophageal reconstruction. In the early years of the study only a small part of the cardia was resected in continuity with the esophagus, and pyloromyotomy was performed. Complications such as delayed gastric emptying and aspiration pneumonia prompted us to change the operative technique to a narrow stomach tube, 3 em in diameter, created along the greater curvature and vascularized by the right gastroepiploic artery and vein only.25, 26 Pyloromyotomy or pyloroplasty has been advocated after all reconstructions with the stomach. After stomach interposition in this series, however, pyloromyotomy or pyloroplasty did not prevent emptying problems and, encouraged by other authors.F: 28 we completely abandoned the procedure. The narrow gastric tube without pyloromyotomy or pyloroplasty empties rapidly and the nasogastric tube is removed on the first operative day. Pulmonary complications after esophagectomy with or without thoracotomy is a matter of controversy.i" 30 In this series of patients operated on by the same team of surgeons with a similar preoperative and postoperative approach and care, the pulmonary complications did differ significantly in favor of the group operated on without thoracotomy. Bleeding complications were equally divided between the two groups, including four patients in group B who had an urgent thoracotomy during blunt dissection for control of bleeding. In all three cases the patient had a squamous cell carcinoma of the middle third of the intrathoracic esophagus. Chylothorax caused by damage of the thoracic duct is possibly enhanced by blunt dissection." Conservative treatment leads to loss of fluid, electrolytes, leukocytes, and proteins. Therefore early ligation of the thoracic duct is mandatory.Vv" Paresis of the recurrent laryngeal nerve is a particular drawback of the transhiatal approach. Apart from hoarseness, it is a serious complication because it prevents adequate coughing. This complication is reported to be under 10% in most small series. The paresis occurs during cervical exploration and seems preventable. Radiologic anastomotic leakages were more common in group B and clinical fistula formation differed significantly between the two groups. All cervical fistulas healed spontaneously except four that needed operative treatment. The in-hospital mortality differed insignificantly between the two groups: 9% for group T and 5% for group B. Esophageal resection has drawbacks both with and without thoracotomy. A thoracotomy in this series adds significantly to postoperative pulmonary complications, whereas without thoracotomy the procedure causes
The Journal of Thoracic and Cardiovascular Surgery May 1993
recurrent laryngeal nerve paresis significantly more often, although it is transient in most instances. The higher leakage rate of the cervical anastomosis is widely known, but the leak heals with conservative treatment in most cases. Late stenosis of the esophagogastrostomy necessitating endoscopic dilation seems not related to radiologic or clinical leakage. The long-term survival after resection is comparable for the two groups of patients. There were no statistically significant differences between the groups as a whole or divided or according to stage. Being aware of potential pitfalls in comparing a series of patients with historical controls, as in the present study, we nevertheless believe that esophagectomy without thoracotomy is an oncologically justifiable operation. We thank Mrs. Vollebregt-Uiterwijk for management of the data base and Mrs. Margo Visser for the multiplerevisions of the manuscript. REFERENCES 1. Giuli R, Gignoux M. Treatment of carcinoma of the esophagus: retrospective study of 2400 patients. Ann Surg 1980;192:44-52. 2. Earlam R, Cunha-Melo JR. Oesophageal squamous cell carcinoma: a critical review of surgery. Br J Surg 1980; 67:381-90. 3. Bosch A, Friaz Z, Pellett JR. Carcinomaof the esophagus: 25 years' experience at the University of Wisconsin Hospitals. Wis Med J 1980;79:23-6. 4. SugimachiK, InokuchiK, Ueo H, Matsuura H, Matsuzaki K, Mori M. Surgical treatment for carcinoma of the esophagus in the elderly patient. Surg Gynecol Obstet 1985;160:317-9. 5. Ellis FH, Gibb P. Esophagogastrectomy for carcinoma. Ann Surg 1979;190:699-705. 6. Andel JG, DeesJ, Dijkhuis CM, Fokkens W, Houten van H, Jong PC de, Woerkom-Eykenboom WMH van. Carcinoma of the esophagus. Ann Surg 1979;190:684-9. 7. Cox DR. The analysisof binary data. London. Chapman and Hall, 1970. 8. Hennessy TP, O'Connei R. Carcinoma of the hypopharynx, esophagus and cardia. Surg Gynecol Obstet 1986; 162:243-7. 9. MannellA, BeckerPJ. Evaluation of the resultsof oesophagectomyforoesophageal cancer.BrJ Surg 1991 ;78:36-40. 10. Gignoux M, Roussel A, Paillot B, Gillet M. The valueof preoperative radiotherapy in esophageal cancer: results of a study of the EORTC. World J Surg 1987;11:426-32. II. Launois B, Delarue D, Campion JP, Kerbaol M. Preoperative radiotherapy for carcinoma of the esophagus. Surg GynecolObstet 1981;153:690-2. 12. Franklin R, Steiger Z, Vaishampayan G, Asfaw 1. Combined modalitytherapy for esophageal squamous cell carcinoma. Cancer 1983;51: I062-71.
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13. Poplin E, Flemming T, Leichman L, Seydel G. Combined therapies for squamous cell-carcinoma of the esophagus: the Southwest Oncology Group study. J Clin Oncol 1987; 5:622-8. 14. Belsey R, Hiebert CA. An exclusive right thoracic approach for cancer of the middle third of the esophagus. Ann Thorac Surg 1974;18:1-15. 15. Mori S, Ishida K, Okamoto K, Oktsu T. Extended dissection of lymph nodes in operation for thoracic esophageal carcinoma. Excerpta Med 1986;40:118-21. 16. Bains MS, Kelsen DP, Beattie EJ, Martini N. Treatment of esophageal carcinoma by combined preoperative chemotherapy. Ann Thorac Surg 1982;34:521-8. 17. Berkholf W, Doermer A, Grunwals S, Fabian W. Chirurgische Behandlung des Kardia- und Oesophagus karzinoms. Fortschr Med 1980;98:21-3. 18. Bertselen S, Aasted A, Vejlsted H. Surgical treatment for malignant lesionsof the distal part of the esophagus and the esophagogastric junction. World J Surg 1985;9:633-8. 19. Hambraeus GM, Mercke CE, Willen R, et al. Prognostic factors influencing survival in combined radiotherapy and surgery of squamous cell carcinoma of the esophagus. Cancer 1988;62:895-904. 20. Husemann B. Cardia carcinoma considered as a distinct clinical entity. Br J Surg 1989;76:136-9. 21. Lorentz T, Fok M, Wong J. Anastomotic leakage after resection and bypass for esophageal cancer: lessonslearned from the past. World J Surg 1989;13:472-7. 22. Denim EV, Stolyarov VI, Volkov ON. Primary complications after surgery for cancer in the cardia-oesophageal region. Acta Chir Scand 1982;148:683-6. 23. Eeftinck Schattenkerk M, Obertop H, Mud HJ, Eijkenboom WMH, Andel JG van, Houten H van. Survival after
24. 25. 26.
27.
28.
29.
30.
31.
32. 33. 34.
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resection for carcinoma of the oesophagus. Br J Surg 1987;74:165-8. Orringer MB, Sloan H. Esophagectomy without thoracotomy. J THoRAc CARDIOVASC SURG 1978;76:643-54. Antonioli DA, Cady B. Contemporary aspects of gastric carcinoma. N Engl J Med 1984;310:1538. Cady B, Choe DS. Changing patterns of cancer. In: Niebergs HE, ed. International Symposium on Detection and Prevention of Cancer. Part 2, vol 2. New York: Dekker, 1980:2041-9. McKeown KC. Total oesophagectomy-three-staged resection. In: Jamieson GG. Surgery of the oesophagus. Edinburgh: Churchill Livingstone, 1988;75:677-85. Cheung H C, Diu KF, Wong J. Is pyloroplasty necessary in esophageal replacement by stomach? A prospective, randomized controlled trial. Surgery 1987;102:19-24. Garvin PJ, Kaminski DL. Extrathoracic esophagectomy in the treatment of esophageal cancer. Am J Surg 1980; 140:772-8. Steiger Z, Wilson RF. Comparison of the results of esophagectomy with and without a thoracotomy. Surg Gynecol Obstet 1981;153:653-6. Bolger C, Walsh TN, Tanner WA, Keeling P, Hennessy TPJ. Chylothorax after oesophagectomy. Br J Surg 1991; 78:587-8. Robinson CLN. The management of chylothorax. Ann Thorac Surg 1985;39:90-5. Kostiainen S, Meurala H, Mattila S, Appelqvist P. Chylothorax. Scand J Thorac Cardiovasc Surg 1983;17:79-83. Havas TE, Gullane PJ, Kassel RN. The incidence and management of chylous fistulae. Aust NZ J Surg 1987; 57:851-4.
Esophagectomy with or without thoracotomy Is there any difference? Two operative approaches for esophageal carcinoma were compared with respect to operative morbidity and mortality by means of multivariable analysis. From 1980 to 1986, 152 patients underwent resection by laparotomy and right-sided anterolateral thoracotomy with an intrathoracic anastomosis. From 1986 to 1989, 141 patients underwent resection by transhiatal blunt dissection with a cervical anastomosis. The stomach was the preferred organ for reconstruction. Paresis of the recurrent laryngeal nerve and leakage of the cervical anastomosis occurred significantly more often in the transhiatal group. Pulmonary complications occurred less frequently in the transhiatal group. In-hospital mortality (9 % in the thoracotomy group and 5 % in the transhiatal group) increased significantly with advanced age of the patients. Furthermore, it was significantly higher in case of colonic interposition as compared with reconstruction with the stomach. Long-term survival did not differ between the two groups. Especially for carcinomas in the distal part of the esophagus, transhiatal esophageal resection without thoracotomy seems to be an oncologically justifiable operation with a reduced morbidity and mortality. (J THORAC CARDIOVASC SURG 1993;105:898-903)
Hugo W. Tilanus, MD, Willem C. J. Hop, MSc,a Bernhard L. A. M. Langenhorst, MD, and J. Jan B. van Lanschot, MD, Rotterdam, The Netherlands*
Carcinoma of the esophagus has a dismal prognosis once the diagnosis is clear. Because the disease is usually detected late in its course, metastatic spread is common. About half ofthe patients present with a resectable tumor, but mortality after the operation used to be as high as 25% in different series.l' This mortality was mainly due to pulmonary insufficiency, dehiscence of the intrathoracic anastomosis, or a combination of these two factors.t" To diminish the postoperative mortality, we changed
our therapeutic approach in 1986 from a laparotomy and a right-sided anterolateral thoracotomy with an intrathoracic anastomosis to transhiatal esophagectomy with blunt dissection and cervical anastomosis. The last 152 patients from the first group and the first 141 patients from the last group are compared with regard to operative morbidity, in-hospital mortality, and survival after resection.
From the Departments of Surgery and Epidemiology & Biostatistics; Erasmus University Hospital, Rotterdam, The Netherlands.
From January 1, 1980, until November 1, 1986, 152 patients with carcinoma of the esophagus or gastroesophageal junction underwent esophageal resection and reconstruction by rightsided anterolateral thoracotomy and laparotomy with a mostly intrathoracic anastomosis (group T). From November I, 1986, until January I, 1990, 141 patients underwent esophagectomy for carcinoma by laparotomy and right-sided neck incision with a blunt disection of the esophagus and cervical anastomosis (group B). No regular lymph node dissection was performed in either group. Patients who underwent an exploratory laparotomy without resection were excluded from this study. Also
Received for publication Oct. 28,1991. Accepted for publication July 27,1992. Address for reprints: H.W. Tilanus, MD, Department of Surgery, Dijkzigt Ziekenhuis, Dr. Molewaterplein 40:3015 GO Rotterdam, The Netherlands. *The Rotterdam Esophageal Tumor Study Group. Copyright © 1993 by Mosby-Year Book, Inc.
0022-5223/93 $1.00+ .10 12/1/41630
898
Patients and methods
The Journal of Thoracic and Cardiovascular Surgery Volume 105, Number 5
Table I. Characteristics ofpatients operated on for esophageal carcinoma with (group T, n = 152) or without (group E, n = 141) thoracotomy Thoracotomy
Men Women Location * Upper third Middle third Lower third Differentiation Squamous cell carcinoma Adenocarcinoma Other Reconstruction Stomach Colon
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Table II. Number ofpatients with complications after esophageal resection with (group T, n = 152) or without (group E, n = 141) thoracotomy Thoracotomy Blunt dissection
Blunt dissection
%
Complication
No.
%
No.
%
p Value
102 39
72 28
9 20 III
6 14 79
50
77
7 12 3 22* I I 36 24 37
5 9 2 16 I I 26 17 28
14
35 55 10
9 7 5 6 5 4 II 34 9
13
62 29 9
13 10 8 9* 7 6 16 51 12
NS NS NS
14 26 60
In-hospital mortality Hemorrhage Chylothorax Paresis Wound infection Delayed emptying Anastomotic leak Pulmonary complication Late stenosis
115 37
76 24
128 13
91 9
No.
%
No.
107 45
70 30
21 40 91 95 44
The mean age in groupTwas 60 years (range 30 to 83) and in group B, 61 years (range 35 to 82). "Missingdata in one patient in group B.
excludedwere patients with a carcinoma of the cervical esophagus because in a substantial number of these patients a simultaneous laryngopharyngectomy was performed. Patient and tumor characteristics are summarized in Table I. Gender and age distribution did not differ significantly between the groups. In group T there were more tumors localizedin the upper and middle thirds of the esophagus(40%) than in group B (20%). This difference is significant and reflects the difference in histologic differentiation. During this study the stomach increasingly became the preferred organ for reconstruction. In later years the colon was used only in patients with a previousstomach resection or gross tumor involvementof the stomach. Statistics. Percentages werecompared by Fisher's exact test. Multivariate analysisof percentages of various types of complications,exceptparesisofthe recurrent laryngeal nerve,wasdone by logistic regression7 in case the complication occurred in at least 10 patients. Survival curves were constructed by the Kaplan-Meier method and compared with the log rank test. No patients were lostto follow-up. Statistical significancewas set at p < 0.05 (two-sided).
Results In group T the stomach was the preferred organ for reconstruction in 76% of the patients and in group B, for more than 90% of the patients. Operations without a thoracotomy lasted on the average 1 hour less than resection with a thoracotomy (3l/2 hours versus 2Y2 hours). Pyloromyotomy or pyloroplasty was highly favored in group T, but in group B the pylorus was left untouched. No late pyloric procedures had to be performed. Postoperative ventilation time did not significantly differ between the two groups. The majority of patients were extubated within 12 hours after the operation.
p
p
NS, Not significant. "[ncluding one case of bilateral paresis in group T and two in group B.
Table III. Multivariate analysis of the probability of postoperative death according to resection method, type of reconstruction, location of tumor, presence of concomitant disease (cardiac or pulmonary), gender, and age Factor Resection Group T Group B Reconstruction Stomach Colon Location Lower esophagus Upper/middle Concomitant disease No
Odds ratio I 0.7 I 5.0
Significance
p=0.51
p
= 0.002
I 0.8
p= 0.74
Yes
I 1.5
p
Sex Male Female Age (yr)
I 1.6 1.7*
= 0.49
p= 0.38 p= 0.04
Data given are ratios of the odds of death against survival. Odds ratios greater (smaller) than I indicate an increased (decreased)operative mortality. "Relative to 10 years younger.
Postoperative complications are summarized in Table II. The in-hospital mortality for group Twas 9% and for group B, 5%. This difference is not significant (p = 0.25). Multivariate analysis of the factors concomitant diseases (cardiac, pulmonary), age, gender, type of reconstruction, localization of tumor, and type of resection (T, B) showed that the only significant factors regarding in-hospital mortality were age and type of reconstruction (TableIII). With increasing age, in-hospital mortality gradually
The Journal of Thoracic and
9 00
Cardiovascular Surgery
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May 1993
survival
survival Squamous (n=95) .... Adeno (n=44)
100%
40%
.......
100%
40%
......
'
.. ..
". ..
20%
20% 0%
Squamous (n=50) .... Adeno (n=77)
l..-_ _----'-
J -_ _---'
o
24
12
36
- L -_ _- - - '
48
60
month
0%
0
12
36
24
48
60
month
Fig. 1. Survival after operation according to histologic type for patientswith squamous cellcarcinoma or adenocarcinoma for groupsT and B.
Table IV. Multivariate analysis of various complications Factor Resection Group T Group B Age <65 yr >65 yr Location Lower esophagus Upper/middle Reconstruction Stomach Colon COPD No Yes
Hemorrhage
Chylothorax
Leakage of anastomosis
Pulmonary complications
Late stenosis
1
1
1
1
1
1.5 (0.41)
0.4 (0.23)
3.4 (0.001)
0.5 (0.03)
4.1 «0.001)
I 0.6 (0.20)
1
1
1
1
0.6 (0.30)
1.0 (0.98)
1.3 (0.48)
1.0 (0.97)
I 1.7 (0.27)
1
I 1.5 (0.29)
1
1.6 (0.45)
1.4 (0.30)
I 1.5 (0.28)
I 0.8 (0.78)
I 0.9 (0.89)
I 1.9 (0.13)
I 1.2 (0.67)
I 0.3 (0.08)
Not tested
Not tested
Not tested
1
Not tested
1.2 (0.65)
For each type of complication, data given are the ratios of the odds of its occurrence against its absence according to various variables; p values are given in parentheses. COPD, Chronic obstructive pulmonary disease.
increased. Colonic interposition was associated with a significantly higher mortality than stomach tube reconstruction. For patients aged at most 65 years, in-hospital mortality was 14% (5/36) in case of colonic interposition and 3% (4/160) in case of stomach tube reconstruction. These figures for the patients aged above 65 years were, respectively, 29% (4/14) and 8% (7/83). Adjusted for the factors age and type of reconstruction, no significant difference was found between group T and group B. Postoperative hemorrhage necessitating reoperation occurred equally in both resection groups, 7% (group T) versus 9% (group B), including four patients in group B who needed an emergency thoracotomy during blunt dissection for control of intrathoracic bleeding. All four of these cases involved a carcinoma ofthe middle third ofthe intrathoracic esophagus. Table IV, which also summa-
rizes other complications, gives results of the multivariate analysis of the occurrence of hemorrhage in relation to the resection group, age, location of tumor, and type of reconstruction. None of these variables was significantly related to hemorrhage. No significant differences were seen between groups T and B with respect to the occurrence of chylothorax. Multivariate analysis (Table IV) of the factors resection method, age, reconstruction type, and location of the tumor showed that none of them significantly correlated with chylothorax. Paresis of the recurrent laryngeal nerve was significantly more frequent in group B (p < 0.01). The paresis was reversible except in six patients. The percentage of patients with wound infection did not differ significantly between the two resection groups. Age and type of reconstruction were also not significantly related to the occur-
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Cardiovascular Surgery Volume 105, Number 5
survival
survival 100%
100%
Stage I (n=30) Stage II (n=76) .... Stage III/IV (n=29)
80%
60%
60%
40%
40%
20%
20%
0%
90 I
L -_ _----'-
-'--_ _---'
--'-_ _- - l
o
24
48
12
36
60
month
Stage I (n=19) Stage II (n=65) ..... Stage III/IV (n=49)
0% '--------'-----'---_---' o 12 24 36 month
--'-_ _- - J 48 60
Fig. 2. Survivalafter operation according to stage for patients with squamous cell carcinoma or adenocarcinoma for groups T and B (stage missing: each group, four patients).
renee of wound infection. Similar findings applied to delayed emptying of the reconstructed esophagus. Leakage of the anastomosis, defined as radiologic leak or clinical fistula, was seen in 16 patients (11%) in group T and 36 patients (26%) in group B (p < 0.01). This difference remains significant after adjustment for other factors investigated (Table IV). The same applied when only the occurrence of clinical fistula (5% in group T, 13% in group B) was analyzed. Pulmonary complications including respiratory distress syndrome differed (p < 0.0 I) between the resection groups in favor of group B. This difference remains significant (Table IV) after adjustment for chronic aspecific respiratory ailment, age, tumor location and reconstruction type. The latter factors themselves, though, were not significantly related to pulmonary complications. In analyzing late stenotic complications of the anastomosis, we excluded patients who died after the operation. The difference between the two resection groups was also significant in favor of group T (p < 0.01) when adjusted for the type of reconstruction (Table IV). The multivariate analysis further revealed that a trend (p = 0.08) existed toward more late stenotic complications after reconstruction with the stomach as compared with colonic interposition. In group T II % of patients with stomach reconstruction had late stenotic complications, whereas this percentage was 0% in those with colonic interposition. These percentages for group B were, respectively, 29% and 18%. No significant correlation was found between anastomotic leakage and late stenotic complications (p = 0.3). Survival of the patients of both groups is analyzed according to histologic type in Fig. I. The difference in survival between the two histologic types within each group is not significant. Survival according to stage for
both treatment groups is seen in Fig. 2. In each group survival decreased significantly with increasing stage. There are no significant differences between the two treatment groups (adjusted for stage, p = 0.34). Discussion Carcinoma of the esophagus is a disseminated disease in the majority of patients at the moment of the diagnosis. About half of the patients have a resectable tumor at first presentation, and even this group has a 5-year survival of less than 20% after resection.v" Adjuvant radiotherapeutic or chemotherapeutic regimens did not substantially improve these disappointing results.P!" Extension of the operative procedure with an en bloc lymphadenectomy did not significantly influence the long-term survival and may increase postoperative pulmonary complications.P: 16 Most authors believe that the goal of surgical treatment of esophageal carcinoma is locoregional control of "at presentation" metastatic disease. This should be attained with the lowest possible morbidity and mortality. Unfortunately, in the past resection was accompanied by a high postoperative mortality of 25% or more. 17-20 Major causes of this mortality and morbidity were pulmonary complications and dehiscence of the intrathoracic anastomosis.v 21, 22 In 1979, esophageal resection by laparotomy and a separate right anterolateral thoracotomy was introduced in our hospital. With this method the patient lies in the supine position during the operation and the right lung is desuffiated during the intrathoracic phase of the 'operation, After esophageal resection the continuity of the digestive tract was restored by gastric tube reconstruction with a mostly intrathoracic anastomosis.P One hundred fifty-two consecutive patients were operated on in this manner until the operative approach was changed to the transhiatal esoph-
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Tilanus et al.
agectomy without thoracotomy in November 1986. This method is extensively described elsewhere.i" Throughout the entire period, the stomach was the preferred organ for esophageal reconstruction. In the early years of the study only a small part of the cardia was resected in continuity with the esophagus, and pyloromyotomy was performed. Complications such as delayed gastric emptying and aspiration pneumonia prompted us to change the operative technique to a narrow stomach tube, 3 em in diameter, created along the greater curvature and vascularized by the right gastroepiploic artery and vein only.25, 26 Pyloromyotomy or pyloroplasty has been advocated after all reconstructions with the stomach. After stomach interposition in this series, however, pyloromyotomy or pyloroplasty did not prevent emptying problems and, encouraged by other authors.F: 28 we completely abandoned the procedure. The narrow gastric tube without pyloromyotomy or pyloroplasty empties rapidly and the nasogastric tube is removed on the first operative day. Pulmonary complications after esophagectomy with or without thoracotomy is a matter of controversy.i" 30 In this series of patients operated on by the same team of surgeons with a similar preoperative and postoperative approach and care, the pulmonary complications did differ significantly in favor of the group operated on without thoracotomy. Bleeding complications were equally divided between the two groups, including four patients in group B who had an urgent thoracotomy during blunt dissection for control of bleeding. In all three cases the patient had a squamous cell carcinoma of the middle third of the intrathoracic esophagus. Chylothorax caused by damage of the thoracic duct is possibly enhanced by blunt dissection." Conservative treatment leads to loss of fluid, electrolytes, leukocytes, and proteins. Therefore early ligation of the thoracic duct is mandatory.Vv" Paresis of the recurrent laryngeal nerve is a particular drawback of the transhiatal approach. Apart from hoarseness, it is a serious complication because it prevents adequate coughing. This complication is reported to be under 10% in most small series. The paresis occurs during cervical exploration and seems preventable. Radiologic anastomotic leakages were more common in group B and clinical fistula formation differed significantly between the two groups. All cervical fistulas healed spontaneously except four that needed operative treatment. The in-hospital mortality differed insignificantly between the two groups: 9% for group T and 5% for group B. Esophageal resection has drawbacks both with and without thoracotomy. A thoracotomy in this series adds significantly to postoperative pulmonary complications, whereas without thoracotomy the procedure causes
The Journal of Thoracic and Cardiovascular Surgery May 1993
recurrent laryngeal nerve paresis significantly more often, although it is transient in most instances. The higher leakage rate of the cervical anastomosis is widely known, but the leak heals with conservative treatment in most cases. Late stenosis of the esophagogastrostomy necessitating endoscopic dilation seems not related to radiologic or clinical leakage. The long-term survival after resection is comparable for the two groups of patients. There were no statistically significant differences between the groups as a whole or divided or according to stage. Being aware of potential pitfalls in comparing a series of patients with historical controls, as in the present study, we nevertheless believe that esophagectomy without thoracotomy is an oncologically justifiable operation. We thank Mrs. Vollebregt-Uiterwijk for management of the data base and Mrs. Margo Visser for the multiplerevisions of the manuscript. REFERENCES 1. Giuli R, Gignoux M. Treatment of carcinoma of the esophagus: retrospective study of 2400 patients. Ann Surg 1980;192:44-52. 2. Earlam R, Cunha-Melo JR. Oesophageal squamous cell carcinoma: a critical review of surgery. Br J Surg 1980; 67:381-90. 3. Bosch A, Friaz Z, Pellett JR. Carcinomaof the esophagus: 25 years' experience at the University of Wisconsin Hospitals. Wis Med J 1980;79:23-6. 4. SugimachiK, InokuchiK, Ueo H, Matsuura H, Matsuzaki K, Mori M. Surgical treatment for carcinoma of the esophagus in the elderly patient. Surg Gynecol Obstet 1985;160:317-9. 5. Ellis FH, Gibb P. Esophagogastrectomy for carcinoma. Ann Surg 1979;190:699-705. 6. Andel JG, DeesJ, Dijkhuis CM, Fokkens W, Houten van H, Jong PC de, Woerkom-Eykenboom WMH van. Carcinoma of the esophagus. Ann Surg 1979;190:684-9. 7. Cox DR. The analysisof binary data. London. Chapman and Hall, 1970. 8. Hennessy TP, O'Connei R. Carcinoma of the hypopharynx, esophagus and cardia. Surg Gynecol Obstet 1986; 162:243-7. 9. MannellA, BeckerPJ. Evaluation of the resultsof oesophagectomyforoesophageal cancer.BrJ Surg 1991 ;78:36-40. 10. Gignoux M, Roussel A, Paillot B, Gillet M. The valueof preoperative radiotherapy in esophageal cancer: results of a study of the EORTC. World J Surg 1987;11:426-32. II. Launois B, Delarue D, Campion JP, Kerbaol M. Preoperative radiotherapy for carcinoma of the esophagus. Surg GynecolObstet 1981;153:690-2. 12. Franklin R, Steiger Z, Vaishampayan G, Asfaw 1. Combined modalitytherapy for esophageal squamous cell carcinoma. Cancer 1983;51: I062-71.
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