Chest Email Content Delivery
HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
QUICK SEARCH:   [advanced]


     

Guest Access | Sign In via User Name/Password
This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF) Free
Right arrow Submit a response
Right arrow Alert me when this article is cited
Right arrow Alert me when eLetters are posted
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in ISI Web of Science
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Add to My Personal Article Archive
Right arrow Download to citation manager
Right arrow reprints & permissions
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via ISI Web of Science (6)
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Michelet, P.
Right arrow Articles by Auffray, J.-P.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Michelet, P.
Right arrow Articles by Auffray, J.-P.
(Chest. 2005;128:3461-3466.)
© 2005 American College of Chest Physicians

Perioperative Risk Factors for Anastomotic Leakage After Esophagectomy*

Influence of Thoracic Epidural Analgesia

Pierre Michelet, MD; Xavier-Benoit D’Journo, MD; Antoine Roch, MD, PhD; Laurent Papazian, MD, PhD; Jacques Ragni, MD; Pascal Thomas, MD, PhD and Jean-Pierre Auffray, MD

* From the Département d’Anesthésie Réanimation (Drs. Michelet, Roch, Ragni, and Auffray), Service de Chirurgie Thoracique (Drs. D’Journo and Thomas), and Service de Réanimation Médicale (Dr. Papazian), Hôpitaux Sud, Marseille, France.

Correspondence to: Pierre Michelet, MD, Département d’Anesthésie Réanimation, Hôpital Sainte-Marguerite, 13274 Marseille Cedex 9, France; e-mail: pierre.michelet{at}mail.ap-hm.fr


   Abstract
TOP
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Study objectives: Anastomotic leakage after esophagectomy is associated with high postoperative morbidity and mortality. The most important predisposing factors for anastomotic leaks are ischemia of the gastric conduit and low blood oxygen content. The aim of this study was to evaluate the influence of thoracic epidural analgesia (TEA) on the incidence of anastomotic leakage after esophagectomy.

Design: Retrospective study.

Setting: A thoracic surgery and anesthesia department in a teaching hospital.

Patients: Two hundred seven patients who underwent one-stage esophagectomy between 1998 and 2003.

Interventions: The effects of perioperative factors and postoperative complications on the incidence of anastomotic leakage were analyzed. Leakage was defined as an anastomotic disruption detected by an ionic x-ray contrast study and confirmed by upper endoscopy in the postoperative period. Analyzed factors included effective TEA placed before the surgical procedure.

Measurements and results: Anastomotic leakage occurred in 23 patients (11%). This complication was associated with a significant increase in length of stay in the ICU and in the hospital (mean, 19 ± 16 days vs 9 ± 7 days [± SD], p = 0.008; and 43 ± 27 days vs 23 ± 11 days, respectively; p < 0.001). Mortality in patients presenting anastomotic leakage was 26%, compared with 5.4% in the remainder (p = 0.002). Factors independently associated with the incidence of leakage included estimated blood loss per milliliter during the surgical procedure (odds ratio [OR], 1.004; 95% confidence interval [CI], 1.001 to 1.007), the cervical location for anastomosis (OR, 5.4; 95% CI, 1.3 to 22.9), and the development of an ARDS in the postoperative period (OR, 4.1; 95% CI, 2.6 to 176.5). Ninety-three patients benefited from an effective TEA for 4.4 ± 0.8 days. The use of TEA was independently associated with a decrease in the incidence of anastomotic leakage (OR, 0.13; 95% CI, 0.02 to 0.71).

Conclusions: The results of this retrospective study suggest that TEA is associated with a decrease in occurrence of anastomotic leakage.

Key Words: anastomotic leakage • esophagectomy • surgical complication • thoracic epidural analgesia


   Introduction
TOP
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
Carcinoma of the esophagus continues to carry a perioperative mortality rate ranging from 3 to 10%.12 The most frequent postoperative complications are respiratory failure and anastomotic leakage. Both are associated with a high postoperative mortality.345 Besides technical features, the most important predisposing factors for anastomotic leaks are ischemia of the gastric conduit6 and impairment in oxygen delivery.7 Thus, the maintenance of an adequate oxygenation in the postoperative period is of major concern especially when pulmonary failure occurs.3

Thoracic epidural analgesia (TEA) has been shown to provide the most satisfactory analgesia and to reduce the incidence of both fatal and nonfatal respiratory complications.8910 Moreover, its use has been reported to improve the bowel microcirculation and to prevent anastomosis insufficiency after operations on the upper GI tract.1112 However, the influence of this technique on the occurrence of anastomotic leakage after esophagectomy remains unknown. The purpose of this retrospective study was to evaluate the influence of various perioperative factors including the use of TEA on the occurrence of anastomotic leakage after esophagectomy.


   Materials and Methods
TOP
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
The study included all patients who underwent en bloc esophagectomy with two-field lymphadenectomy for malignancy between January 1998 and December 2003 at our institution.

Data Collection
Data were abstracted from our prospective esophagectomy database and from the medical chart of each patient. Missing values were recorded as such. Data were classified as preoperative, perioperative, and postoperative data, and postoperative complications.

The preoperative data registered included age, gender, American Society of Anesthesiologists (ASA) score13 and New York Heart Association (NYHA) status, body mass index (BMI), smoking history, history of ischemic heart disease, diabetes, arterial blood gases on air with PaO2 as percentage of predicted, simple spirometry (FEV1 and FVC as percentage of predicted and FEV1/FVC ratio), prior chemotherapy and/or radiotherapy, type of malignancy, and tumor stage recorded from the postoperative histology findings.

Perioperative data studied were the duration of surgical procedure (from skin incision to closure), the duration of one-lung ventilation (OLV), and the duration of mechanical ventilation, perioperative estimated blood loss, and the occurrence of an hemodynamic instability defined as a systolic arterial pressure < 80 mm Hg over 5 min. The experience of the surgeon and the anesthetist were not recorded since all surgical procedures were performed by the same surgical (P.T., R.G.) and anesthetic team (J.R., P.M.) with an experience in the management of esophagectomies > 10 years.1415

Postoperative data gathered included the need for postoperative blood transfusion, inotropic use, the lowest value of the PaO2/fraction of inspired oxygen (FIO2) ratio within the first 24-h postoperative period, and the need for reintubation with mechanical ventilation for acute respiratory failure. Postoperative complications included the occurrence of postoperative pneumonia, ARDS,16 sepsis17 and anastomotic leak within the 30 days after surgical procedure. Postoperative pneumonia was defined as new and persistent lung infiltrates on chest radiographs, a temperature > 38.5°C, a PaO2/FIO2 ratio < 200 mm Hg, and macroscopically proven purulent tracheal secretions. When patients were receiving mechanical ventilation, the diagnosis of pneumonia was confirmed by a BAL culture findings > 104 cfu/mL.18 Postoperative death was defined as occurring within 30 days after esophagectomy. To exclude a confounding relationship between the development of ARDS and the occurrence of an anastomotic leakage, all patients who required mechanical ventilation for ARDS were not recorded as such but only as leakage in case of concomitant or prior diagnosis of leakage.

Anastomotic leakage was defined as an esophagogastrostomy anastomotic dehiscence diagnosed during the postoperative period. For critically ill patients requiring mechanical ventilation, a routine upper endoscopy was performed to confirm or rule out an anastomotic leakage as the possible cause of the respiratory failure. In patients with a short stay in the ICU, anastomotic leakage was assessed by a water-soluble, monomeric, ionic x-ray contrast medium (Gastrografin; Schering AG; Berlin, Germany) study on postoperative days 8 to 10 and, in case of suspicion, confirmed by an endoscopy.

Surgical and Anesthetic Techniques
Anesthesia was established with midazolam, sufentanyl, and a muscular relaxant. A left-sided, double-lumen endobronchial tube was used for ventilation (BronchoPart; Rüsch; Betschdorf, France). Tidal volume was 8 to 10 mL/kg in double-lung ventilation and 5 to 6 mL/kg in OLV with a positive end-expiratory pressure of 5 cm H2O.

The surgical procedure was a one-stage en bloc esophagectomy with two-field lymphadenectomy. A right transthoracic approach was used in all cases with an esophagogastric anastomosis in the upper thorax for lower third and gastroesophageal tumors (Ivor-Lewis technique) or in the neck for higher lesions. The gastric tubulization was achieved by transecting the stomach proximally along the gastric fundus while preserving its vascularization from the right gastric and right gastroepiploic arteries and placing in the posterior mediastinum. All patients underwent a Heineke-Mikulicz pyloroplasty to ensure an efficient gastric drainage.

Postoperative Analgesia
The use of TEA for postoperative analgesia was systematically proposed and protocolized during the preoperative period whatever the patient health status was. The TEA was placed before induction of anesthesia, at the T6–7 or T7–8 intercostal space using the median approach. Patient-controlled opioid analgesia was planned in case of the patient’s refusal or the failure of TEA insertion. The infusion of TEA was started at the end of thoracic time, after the esogastric anastomosis with an initial flow of 6 mL/h (12 mg/h of ropivacaine and 3 µg/h of sufentanyl). After extubation, the level of anesthesia was confirmed by loss of pinprick sensation. During the first 5 postoperative days, the rate of TEA infusion was adjusted to obtain a visual analog scale ≤ 3 at rest and a nerve blockade between the second and the ninth thoracic metamere. In case of TEA ineffectiveness or accidental withdrawal before the third day, analgesia was provided by opioid patient-controlled opioid analgesia and recorded as such.

Statistical Analysis
Data were analyzed using statistical software (SPSS 12.0 s; SPSS; Chicago, IL). Initial univariate analysis, using the {chi}2 test or Fisher Exact Test, as appropriate, for categorical variables and the Wilcoxon or Kruskal-Wallis test, as appropriate, for continuous variables, were used to compare occurrence of anastomotic leak against individual preoperative, perioperative, and postoperative variables and development of postoperative complications. Multivariate analysis was used to determine the odds ratio (OR), based on multiple logistic regression of variables found to be significant or with a p value < 0.25 in the univariate analysis. Anastomotic leakage was the dependent variable, and all clinical, surgical, anesthetic, and pathologic variables were the independent variables. ORs and their 95% confidence intervals (CIs) were computed. All tests were two sided, and p values of < 0.05 were considered statistically significant.


   Results
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
Study Population
During the 6-year reference period, 207 patients were retrospectively studied (174 men and 33 women; mean age, of 63 ± 8 years [± SD]). The rate of anastomotic leak was 11% (23 of 207 patients), with a 30-day mortality of 26% (6 of 23 patients), compared to 5.4% (10 of 184 patients) without a leak (p = 0.002). Preoperative characteristics are presented in Table 1 . There was no difference between the groups in regard to surgical, mechanical ventilation, or OLV duration.


View this table:
[in this window]
[in a new window]

  		Table 1.. Results of Univariate Analysis for Preoperative Factors*

 
Anastomotic Leakage
Among the 23 patients with anastomotic leakage, 12 patients presented with early symptoms. In five patients with septic shock and respiratory failure (mean, 5 ± 2 days), the diagnosis was made by endoscopy. In the remaining seven patients, the leakage was preceded by postoperative respiratory failure requiring mechanical ventilation (mean, 6 ± 3 days), although repeated endoscopies in the few days following respiratory failure had not shown any leakage. In these seven patients, leakage was diagnosed in the ICU several days after the onset of ARDS (mean, 10 ± 5 days). Surgical reintervention was required in 11 of these 12 cases.

The remaining 11 patients presented clinically occult leaks diagnosed by routine control after ICU discharge (mean, 9 ± 1 postoperative days). Three of these patients presented respiratory failure requiring reintubation and mechanical ventilation during the ICU stay, but repeated endoscopies in the few days following respiratory failure did not show any leakage.

Considering the 23 patients with anastomotic leakage, 15 patients experienced an anastomotic leak that was associated, causally or coincidentally, with a clinically relevant event during the postoperative course, whereas 8 asymptomatic patients had a "on-screening" diagnosis of fistula. The development of anastomotic leakage was associated with a significant increase in the ICU length of stay (mean, 19 ± 16 days vs 9 ± 7 days, p = 0.008) and in the hospital length of stay (mean, 43 ± 27 days vs 23 ± 11 days, p < 0.001). The adjusted OR for postoperative mortality associated with anastomotic leakage occurrence was 8.1 (95% CI, 2.2 to 30.4; p < 0.002).

TEA
TEA was effective for 93 patients. The characteristics of patients in regard to whether or not the TEA was effective are presented in Table 2 . The mean duration of epidural infusion in the postoperative course was 4.4 ± 0.8 days, with four cases of accidental withdrawal before the third day.


View this table:
[in this window]
[in a new window]

  		Table 2.. TEA Patient Characteristics*

 
Risk Factors
The results of univariate analysis are displayed in Tables 1, 3 . Patients who experienced anastomotic leakage were more likely to have documented surgical difficulties assessed by the perioperative blood loss and the rate of hypotensive events. These patients were also characterized by a lower frequency of epidural analgesia in the postoperative course. Postoperatively, the development of an ARDS was more frequent in the group of patients with anastomotic leakage. Five patients with postleakage ARDS were not recorded as such. Multiple logistic regression analysis revealed that TEA might decrease the risk of anastomotic leakage, whereas the perioperative blood loss, a cervical anastomosis, and the development of an ARDS were associated with a risk increase (Table 4 ).


View this table:
[in this window]
[in a new window]

  		Table 3.. Results of Univariate Analysis for Peroperative and Postoperative Factors*

 

View this table:
[in this window]
[in a new window]

  		Table 4.. Results of Multiple Logistic Regression Analysis on 181 Patients With Complete Data

 

   Discussion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
This retrospective analysis revealed an 11% rate of anastomotic leakage in a series of 207 patients scheduled for esophagectomy. The main result of this study showed that the TEA used during the postoperative course could decrease the risk for anastomotic leakage.

Esophageal anastomotic leak is a potentially life-threatening complication of esophagectomy related to the disastrous consequences of leakage of GI contents with mediastinitis, septic shock, ARDS, and death.419 After esophagectomy and gastric reconstruction, adequate wound perfusion and oxygenation are critical requirements for wound healing. Indeed, realization of a gastroplasty was shown to impair dramatically the microcirculatory blood flow in the proximal end of the gastric tube despite the absence of significant impairment in systemic hemodynamic status.20 Mechanisms involved mainly include a vasoconstriction of the intramural arterioles supplying the mucosa adjacent to the resection line and the ligature of two of four major blood supply arteries when the narrow gastric tube is constructed.2021 In this setting, development of new techniques that would protect against conduit ischemia and prevent anastomotic leak would have a significant impact on the mortality and morbidity of esophagectomy.

The protective effect of TEA suggested in our study could be explained by several factors. It has been reported that the use of TEA promotes intensive physiotherapy that could preserve the postoperative pulmonary function and prevent hypoxemia.910 Another explanation may result from the related improvement of the gastric tube microcirculation. Indeed, its use has been shown to improve microcirculation of the distal part of the gastric tube in an experimental model of esophagectomy.22 Moreover, Kabon et al11 reported an increase in the tissue oxygen tension resulting from TEA use during major abdominal surgery. As a result, a clinical study12 reported a positive influence of TEA on the rate of anastomotic insufficiency after surgery of the upper GI tract.

The higher leak rate reported in our study in cases of cervical anastomosis has been previously suggested.623 The length of the esophageal reconstruction, the compression of the stomach at the narrow thoracic inlet, and the frequent gastric distension may be parts of the explanation.6 We also found that the risk for anastomotic leakage increased with the perioperative blood loss. The assessment of this factor as an indicator of surgical difficulties is supported by a previous study24 that demonstrated a correlation between intraoperative blood loss, surgical difficulty, and postoperative complications.

In the postoperative period, among the factors tested in our analysis, the only factor that significantly increased leak occurrence was the development of an ARDS. The occurrence of pneumonia and more specifically of ARDS has been reported as a major factor of morbidity and mortality in the postoperative course.31924 Moreover, pulmonary complications are associated with postoperative hypoxemia and hypotension, which are thought to stimulate the release of soluble, proinflammatory mediators followed by impairment of wound healing.2526 These consequences could explain the influence of pulmonary complications on the occurrence of anastomotic leakage. Nevertheless, to our knowledge, reports of the relationship between ARDS and anastomotic leakage occurrence are lacking. Indeed, a confounding relationship could exist between the development of ARDS and the prior onset of anastomotic leakage. To avoid such confusion, an upper digestive endoscopy was systematically performed in case of ARDS in our institution. However, we could not exclude the possibility of an endoscopic false-negative result in the early course of the disease.

In the present study, we have not found any association between preoperative pulmonary function and other clinical characteristics on the occurrence of postoperative leakage. This lack of a significant association may be partly explained by important epidemiologic modifications during the last few years including the improvement in patient selection, in preoperative preparation27 and the increase in the prevalence of adenocarcinoma in Western countries.28 Furthermore, systematic surgical jejunostomy allowed a rapid enteral feeding from the second postoperative day, which may have limited the influence of nutritional factors. However, the frequent absence of enteral feeding in case of septic complication may have impaired the nutritional support and represent a supplemental factor of wound healing impairment. Nevertheless, a limitation of our study is that no caloric count and no other nutritional markers except the BMI were recorded.

In conclusion, this retrospective analysis emphasizes the influence of factors associated with an impairment of perfusion or oxygenation in the development of anastomotic leakage. Our results also suggest that TEA could prevent the occurrence of anastomotic leakage in the postoperative course of esophagectomy. These findings reinforce the clinical relevance of this technique after esophagectomy. Further prospective studies are necessary to assess the influence of TEA on perfusion of the gastric conduit.


   Acknowledgements
 
We are grateful to Dr. Karine Barrau and Dr. Anderson Loundou for assistance in statistical analysis and intensive reviewing.


   Footnotes
 
Abbreviations: ASA = American Society of Anesthesiologists; BMI = body mass index; CI = confidence interval; FIO2 = fraction of inspired oxygen; NYHA = New York Heart Association; OLV = one-lung ventilation; OR = odds ratio; TEA = thoracic epidural analgesia

This study was conducted in the Department of Anaesthesiology and Intensive Care of Hôpital Sainte-Marguerite, Marseille, France.

Received for publication January 3, 2005. Accepted for publication May 19, 2005.


   References
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

  1. Ferguson, MK, Martin, TR, Reeder, LB, et al (1997) Mortality after esophagectomy: risk factor analysis. World J Surg 21,599-603;discussion 603–594[CrossRef][ISI][Medline]
  2. Jamieson, GG, Mathew, G, Ludemann, R, et al Postoperative mortality following oesophagectomy and problems in reporting its rate. Br J Surg 2004;91,943-947[CrossRef][ISI][Medline]
  3. Avendano, CE, Flume, PA, Silvestri, GA, et al Pulmonary complications after esophagectomy. Ann Thorac Surg 2002;73,922-926[Abstract/Free Full Text]
  4. Alanezi, K, Urschel, JD Mortality secondary to esophageal anastomotic leak. Ann Thorac Cardiovasc Surg 2004;10,71-75[Medline]
  5. Poon, RT, Law, SY, Chu, KM, et al Esophagectomy for carcinoma of the esophagus in the elderly: results of current surgical management. Ann Surg 1998;227,357-364[CrossRef][ISI][Medline]
  6. Urschel, JD Esophagogastrostomy anastomotic leaks complicating esophagectomy: a review. Am J Surg 1995;169,634-640[CrossRef][ISI][Medline]
  7. Kusano, C, Baba, M, Takao, S, et al Oxygen delivery as a factor in the development of fatal postoperative complications after oesophagectomy. Br J Surg 1997;84,252-257[CrossRef][ISI][Medline]
  8. Brodner, G, Pogatzki, E, Van Aken, H, et al A multimodal approach to control postoperative pathophysiology and rehabilitation in patients undergoing abdominothoracic esophagectomy. Anesth Analg 1998;86,228-234[Abstract]
  9. Chandrashekar, MV, Irving, M, Wayman, J, et al Immediate extubation and epidural analgesia allow safe management in a high-dependency unit after two-stage oesophagectomy: results of eight years of experience in a specialized upper gastrointestinal unit in a district general hospital. Br J Anaesth 2003;90,474-479[Abstract/Free Full Text]
  10. Watson, A, Allen, PR Influence of thoracic epidural analgesia on outcome after resection for esophageal cancer. Surgery 1994;115,429-432[ISI][Medline]
  11. Kabon, B, Fleischmann, E, Treschan, T, et al Thoracic epidural anesthesia increases tissue oxygenation during major abdominal surgery. Anesth Analg 2003;97,1812-1817[Abstract/Free Full Text]
  12. Zugel, N, Bruer, C, Breitschaft, K, et al Effect of thoracic epidural analgesia on the early postoperative phase after interventions on the gastrointestinal tract [in German].Chirurg 2002;73,262-268[Medline]
  13. Dripps, RD, Lamont, A, Eckenhoff, JE The role of anesthesia in surgical mortality. JAMA 1961;178,261-266[ISI][Medline]
  14. Sutton, DN, Wayman, J, Griffin, SM Learning curve for oesophageal cancer surgery. Br J Surg 1998;85,1399-1402[CrossRef][ISI][Medline]
  15. Birkmeyer, J, Stukel, T, Siewers, A, et al Surgeon volume and operative mortality in the United States. N Engl J Med 2003;349,2117-2127[Abstract/Free Full Text]
  16. Bernard, GR, Artigas, A, Brigham, KL, et al The American-European Consensus Conference on ARDS: definitions, mechanisms, relevant outcomes, and clinical trial coordination. Am J Respir Crit Care Med 1994;149,818-824[Abstract]
  17. Levy, MM, Fink, MP, Marshall, JC, et al 2001 SCCM/ESICM/ACCP/ATS/SIS International Sepsis Definitions Conference. Intensive Care Med 2003;29,530-538[Medline]
  18. Jourdain, B, Joly-Guillou, ML, Dombret, MC, et al Usefulness of quantitative cultures of BAL fluid for diagnosing nosocomial pneumonia in ventilated patients. Chest 1997;111,411-418[Abstract/Free Full Text]
  19. Zane Atkins, B, Shah, AS, Hutcheson, KA, et al Reducing hospital morbidity and mortality following esophagectomy. Ann Thorac Surg 2004;78,1170-1176[Abstract/Free Full Text]
  20. Schilling, M, Redaelli, C, Maurer, C, et al Gastric microcirculatory changes during gastric tube formation: assessment with laser Doppler flowmetry. J Surg Res 1996;62,125-129[CrossRef][Medline]
  21. Liebermann-Meffert, DM, Meier, R, Siewert, JR Vascular anatomy of the gastric tube used for esophageal reconstruction. Ann Thorac Surg 1992;54,1110-1115[Abstract]
  22. Lazar, G, Kaszaki, J, Abraham, S, et al Thoracic epidural anesthesia improves the gastric microcirculation during experimental gastric tube formation. Surgery 2003;134,799-805[Medline]
  23. Pierie, JP, de Graaf, PW, van Vroonhoven, TJ, et al Healing of the cervical esophagogastrostomy. J Am Coll Surg 1999;188,448-454[Medline]
  24. Tandon, S, Batchelor, A, Bullock, R, et al Peri-operative risk factors for acute lung injury after elective oesophagectomy. Br J Anaesth 2001;86,633-638[Abstract/Free Full Text]
  25. Kooguchi, K, Kobayashi, A, Kitamura, Y, et al Elevated expression of inducible nitric oxide synthase and inflammatory cytokines in the alveolar macrophages after esophagectomy. Crit Care Med 2002;30,71-76[CrossRef][ISI][Medline]
  26. Yamada, T, Hisanaga, M, Nakajima, Y, et al Serum interleukin-6, interleukin-8, hepatocyte growth factor and nitric oxide changes during thoracic surgery. World J Surg 1998;22,783-790[CrossRef][ISI][Medline]
  27. Thomas, P, Doddoli, C, Lienne, P, et al Changing patterns and surgical results in adenocarcinoma of the oesophagus. Br J Surg 1997;84,119-125[CrossRef][ISI][Medline]
  28. Blot, WJ, Devesa, SS, Kneller, RW, et al Rising incidence of adenocarcinoma of the esophagus and gastric cardia. JAMA 1991;265,1287-1289[Abstract]



This article has been cited by other articles:


Home page
 Eur. J. Cardiothorac. Surg.Home page
Y.-G. Goan, H.-C. Chang, H.-K. Hsu, and Y.-P. Chou
An audit of surgical outcomes of esophageal squamous cell carcinoma
Eur. J. Cardiothorac. Surg., March 1, 2007; 31(3): 536 - 544.
[Abstract] [Full Text] [PDF]

This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF) Free
Right arrow Submit a response
Right arrow Alert me when this article is cited
Right arrow Alert me when eLetters are posted
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in ISI Web of Science
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Add to My Personal Article Archive
Right arrow Download to citation manager
Right arrow reprints & permissions
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via ISI Web of Science (6)
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Michelet, P.
Right arrow Articles by Auffray, J.-P.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Michelet, P.
Right arrow Articles by Auffray, J.-P.

HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS