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10.1245/ASO.2006.04.040
Annals of Surgical Oncology 13:557-564 (2006)
© 2006 Society of Surgical Oncology
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Original Article

The Influence of Technical Complications on Postoperative Outcome and Survival After Esophagectomy

Lorenzo E. Ferri, MD, FRCS (C), Simon Law, MS, MA (Cantab), MBBChir, FRCS (Edin), FACS, Kam-Ho Wong, MBBS, FRCS (Edin), Ka-Fai Kwok, MBBS, FRCS (Edin) and John Wong, MD, PhD, FRACS, FACS (Hon)

Department of Surgery, Division of Esophageal Surgery, University of Hong Kong Medical Centre, Queen Mary Hospital, 102 Pokfulam Road, Hong Kong, China

Correspondence: Address correspondence and reprint requests to: Simon Law, MS, MA (Cantab), MBBChir, FRCS (Edin), FACS; E-mail: slaw{at}hku.hk.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: The dismal survival associated with esophagectomy for cancer has led to the search for potentially correctable factors responsible for this poor prognosis. Although it is intuitive that technical complications could increase postoperative mortality, the effect on long-term survival is controversial.

Methods: From 1990 to 2002, 434 patients underwent resection for squamous cell carcinoma of the intrathoracic esophagus. Prospectively collected data were reviewed for the presence of technical complications. Patient, tumor, and operative variables, postoperative outcome, and survival were compared between patients with technical complications and those without. Prognostic factors were assessed by multivariate analysis.

Results: Technical complications occurred in 98 (22.6%) patients. Patients with technical complications had a higher prevalence of cardiac disease, more proximal tumors, and more cervical anastomoses. Technical complications were associated with an increased rate of pulmonary complications (37.8% vs. 10.7%; P < .001) and increased hospital mortality (9.2% vs. 3.3%; P = .025), but no difference in 30-day mortality (2% vs. 1.2%; P = .6). Poor-prognostic factors for survival included male sex, stage III/IV disease, cirrhosis, proximal tumors, and R1/R2 resection, but not technical complications.

Conclusions: Although immediate postoperative outcome and hospital mortality rates were increased, no effect on long-term survival was seen in patients with complications related to errors in surgical technique.

Key Words: Esophageal cancer • Survival • Complications • Mortality


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Despite advances in cancer care, malignancy of the esophagus continues to portend a poor prognosis, with 5-year survival rates of 15% to 40%.1–6 Surgical resection remains the cornerstone of any potential cure. However, esophagectomy is a complex oncological procedure, and except in specialized centers, mortality and morbidity rates approximate 10% and 35%, respectively.7 These poor outcomes have motivated surgeons to identify potentially preventable causes. Although improved patient selection plays a role in reducing mortality,5,8,9 the persistent high morbidity rate leaves room for further improvement. Technical complications represent potentially correctable factors in the treatment of patients with esophageal malignancy. Furthermore, several reports suggest that postoperative morbidity may also negatively affect long-term survival, thus implying that the presence of surgical complications in itself increases the risk of recurrent malignancy and death.10,11 A definitive link between technical complications and long-term survival has yet to be clearly defined. To address this issue, we sought to determine the effects of complications that arise from potentially correctable errors in surgical technique on both postoperative outcome and long-term survival after esophagectomy.


   METHODS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Data of 1312 patients with esophageal cancer treated at the Department of Surgery, University of Hong Kong Medical Center at Queen Mary Hospital, from 1990 to 2002 were prospectively collected. Tumor resection was performed in 714 patients. Patients who underwent pharyngolaryngoesophagectomy and those with gastric cardia cancer were excluded from this study. Because tumor histological characteristics may affect prognosis in esophageal cancer,12,13 only patients with intrathoracic squamous cell carcinoma were evaluated; thus, 434 patients were included for final analysis in this study.

Patients with squamous cell carcinoma of the esophagus were treated in an individualized manner determined by both patient (performance status and comorbidities) and tumor (stage and location) characteristics. The various approaches used in our institution have previously been described in detail.14,15 Briefly, tumors of the middle and lower third were managed by a Lewis-Tanner esophagectomy via an abdominal and right thoracic approach. For patients with tumors above the carina (proximal third), a three-phase esophagectomy was performed. Transhiatal esophagectomy was used in selected patients with diminished cardiopulmonary reserve and in a randomized controlled trial from 1990 to 1994 that compared this approach with transthoracic esophagectomy, the results of which were previously published.15 Thoracoscopic mobilization of the esophagus was introduced in 1994 and has largely supplanted transhiatal resection for patients with limited performance status.16,17

Most resections included a two-field lymphadenectomy comprising complete dissection of the celiac trifurcation and infracarinal mediastinal lymph nodes. Lymph nodes in the superior mediastinum were sampled or resected when present. Cervical lymphadenectomy was performed only when involved cervical nodes were demonstrated because our previous study of recurrence patterns suggested a limited value of routine neck dissection,18 and no survival advantage was conferred by this additional procedure.14,19

Intestinal continuity was restored in the vast majority of cases with a gastric conduit placed in the right thoracic cavity or via the orthotopic route when the anastomosis was performed in the neck. In palliative operations with residual mediastinal tumor, the retrosternal route was preferred after three-phase esophagectomy. The colonic conduit was used sparingly and was indicated only when the stomach was unavailable, such as in a patient with prior gastrectomy. Both the circular stapler and a continuous single-layer, hand-sewn technique with a monofilament absorbable suture were used to construct the esophageal anastomosis after resection in the early part of the study period. A prospective randomized trial comparing the two methods for intrathoracic anastomosis demonstrated no difference in leak rate but a 4-fold increase in the anastomotic stricture rate for stapled anastomoses.20 Since then, all anastomoses have been performed by using the hand-sewn technique, regardless of the anastomotic site.

Patients with resectable tumors were generally not given neoadjuvant or adjuvant chemotherapy/radiotherapy except in the context of a clinical trial. A randomized trial comparing preoperative chemotherapy with immediate resection was performed from 1989 to 1995, the results of which have been published.21 Since mid 1995, patients with potentially resectable tumors on preoperative investigation have been entered onto a recently closed trial that compared induction chemoradiation with surgical resection alone. Patients with locally advanced tumors (T4) or nonregional metastatic spread received palliative treatment with primary chemoradiotherapy. Surgical resection was offered to patients who showed a significant clinical response and had a reasonable performance status.

Patient information prospectively entered into an institutional database was reviewed. Index cases were defined as patients who developed postoperative technical complications. Complications attributed to errors in surgical technique were defined as anastomotic leak (as determined by contrast esophagram, endoscopy, or both), recurrent laryngeal nerve palsy (confirmed by routine postoperative bronchoscopy), chylothorax (confirmed biochemically on chest tube effluent with or without imaging by lymphangiogram), ischemic necrosis of the conduit, postoperative hemorrhage requiring reexploration, wound dehiscence, and delayed gastric emptying (evidenced by a dilated intrathoracic stomach with delayed passage of contrast passage on esophagram, as well as on clinical grounds). This group of patients was compared with the remaining patients who did not have technical complications.

Major pulmonary complications comprised pneumonia (based on radiographical changes associated with fever, an increased leukocyte count, and/or positive sputum cultures), respiratory failure (based on blood gas criteria with or without the need for mechanical ventilation), and acute respiratory distress syndrome (based on blood gas criteria and radiological features). Cardiovascular morbidity included ventricular and supraventricular arrhythmia (mostly in the form of atrial fibrillation), myocardial infarction, heart failure, and pulmonary embolism. Thirty-day mortality was defined as death within the first 30 days after esophagectomy; any death in the hospital after surgery was recorded as hospital mortality.

Data are expressed as mean ± SD for parametric variables and median (range) for nonparametric variables. Fisher’s exact test or the Mann-Whitney U-test was used to assess the significance of differences between groups. A P value of <.05 was regarded as significant. Survival curves were formulated by using the Kaplan-Meier method, and comparisons between groups were assessed by the log-rank test. Predictors for long-term survival were identified by multiple stepwise Cox regression. All statistical analyses were performed by using the SPSS statistical package 9.0 (SPSS Inc., Chicago, IL).


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Of 434 patients who underwent resection, 125 complications attributable to errors in surgical technique were identified in 98 patients (22.6%). These are listed in Table 1Go. Recurrent laryngeal nerve palsy confirmed by direct laryngoscopy was the most common, in 46 patients (10.6%). Patients with a strong cough and who were able to clear their sputum were treated expectantly, and those without this feature underwent early tracheostomy for pulmonary sputum clearance, usually on postoperative day 2 to 3. This was placed in 101 (23%) patients and was significantly more common in patients with technical complications (42.9% vs. 17.6%; P < .001). Anastomotic leak was a rare occurrence, at 3%; most were identified by water-soluble contrast esophagram. All anastomotic leaks were confirmed by endoscopy, and the size of the leak was estimated. Most cases were managed nonoperatively with nil per os; drainage either by opening the neck wound for cervical anastomosis or by using radiological means for intrathoracic anastomosis; intravenous antibiotics; and nutritional support. In most cases, enteral feeding was possible by placement of a fine-bore feeding tube distally at the time of endoscopic confirmation of the leak. Rarely, persistent sepsis necessitated operative repair and drainage. This especially applied to leaks secondary to the ischemic conduit, when early reexploration and takedown of the conduit were indicated. Reexploration was required in 27 patients. Bleeding was the most common reason for reexploration (five patients), and anastomotic leaks, chylothorax, and conduit gangrene accounted for four patients each. Reoperation for gastric outlet obstruction was required in two, and one patient required revision of an obstructed Roux jejunal limb.


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  		TABLE 1. Technical complications in 434 consecutive esophagectomies
 
Patient, tumor, and treatment characteristics for cases with (n = 98) and without (n = 336) technical complications are listed in Table 2Go. Patient characteristics between the two groups differed only in that patients with technical complications were more likely to have a preexisting cardiac condition (23.5% to 13.7%; P = .027). Technical complications were also more likely in those who had proximal third tumors and cervical anastomosis. This may be largely accounted for by a higher incidence of recurrent laryngeal nerve injury, which was 24.6% and 8.5% in the upper third and mid to lower third tumors, respectively (P = .01). The incidences of chylothorax (3.9% in upper vs. 2.5% in mid/lower third) or anastomotic leak (3.5% in upper vs. 2.9% in mid/lower third) were not significantly higher in patients with more proximally located tumors. Neoadjuvant therapies also did not lead to more technical complications.


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  		TABLE 2. Characteristics for patients with and without technical complications
 
Major cardiopulmonary complications are listed in Table 3Go. Major medical complications were more prevalent in patients with technical complications and were accounted for by an increased risk of pulmonary and cardiac morbidities, because other adverse events were uncommon. The 30-day mortality rate was 2% for those who had technical complications and 1.2% for those who did not (P = .6). However, there was a 3-fold increase in the hospital mortality rate in patients with technical complications (9.2% vs. 3.3%; P = .025). A total of 20 patients (4.6%) died in the hospital. The primary causes of death were pulmonary in 13 cases (mostly pneumonia), myocardial infarction in 3, malignant cachexia in 2, cerebrovascular accident in 1, sepsis with multiple organ failure of uncertain etiology in 1, and uncontrolled anastomotic leak in 1.


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  		TABLE 3. Effect of technical complications on postoperative outcomes
 
The median survival for patients who had technical complications was 13.2 months, compared to 17.5 months in those without (P = .13). When hospital deaths were excluded, the median survivals were 14.4 and 18.8 months, respectively (P = .35; Figs. 1Go and 2Go). Male sex, proximal tumor location, presence of cirrhosis, advanced tumor stage (III/IV), and R1/2 resections were identified by multivariate analysis as adverse predictors of survival (Table 4Go). The presence of technical complications did not correlate with survival.


Figure 1
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  		FIG. 1. Kaplan-Meier survival curves for patients undergoing esophagectomy, comparing those with and without technical complications.

 

Figure 2
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  		FIG. 2. Kaplan-Meier survival curve for patients undergoing esophagectomy, excluding hospital deaths.

 

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  		TABLE 4. Independent predictors of survival after esophagectomy
 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
We demonstrated in this study that technical complications were adversely associated with a higher hospital mortality rate but that long-term survival was not significantly affected. Unlike other studies that have investigated the influence of technical complications on outcomes after esophagectomy, this study is unique in that it comprises a uniform cohort of patients with the same tumor histological diagnosis (squamous cell) and site (intrathoracic esophagus) from our center. Both of these are thought to affect survival.

Much interest has been focused on the effect of technical complications on outcomes after major cancer surgery. This is understandable, because prevention of these errors in surgical technique is a clear target for improved practice. It is no exception in esophageal cancer. In this study, an overall technical complication rate of 22.5% was documented. This is comparable to several large series that reported technical complication rates ranging from 22% to 36%.10,13,22 Although usually transient, recurrent laryngeal nerve injury accounted for approximately 50% of all technical complications in this study, occurring in 10.6% of patients. This rate is slightly higher than the 4% to 7% reported in several large series,4,10,13 possibly as a result of the higher prevalence of upper/middle third tumors (approximately 80%) in our patient population. We previously showed that tumor location was related to the risk of recurrent laryngeal nerve injury.23 Furthermore, we perform routine bronchoscopy on all patients after surgery, and, therefore, the true incidence was recognized; our data were also prospectively captured. Series in which recurrent laryngeal nerve injury is diagnosed on clinical grounds of hoarseness alone may underestimate the true incidence of this complication because asymptomatic vocal cord palsy has been shown to occur in up to 20% of cases.24

Anastomotic leak was rare in our series, at 3%. This compares favorably with the rate of 3.5% to 21% reported in recent series of >100 patients.4,6,13,22,25,26 A higher leak rate with cervical compared with intrathoracic anastomoses is generally seen.25,27 In our experience, however, the leak rates did not differ regardless of the site of anastomosis—a finding similar to a recently reported randomized trial of intrathoracic versus cervical anastomoses.28

Neoadjuvant chemotherapy and/or radiotherapy has been associated with increased rates of both technical and nontechnical complications,29,30 possibly as a result of postirradiation fibrosis, which makes dissection more difficult. In our experience, such fibrosis is frequently encountered, obscuring tissue planes, but conversely the difficulties encountered with infiltrative locally advanced tumors are also avoided because of significant tumor downstaging. In this study, we found no correlation between the use of neoadjuvant therapy and technical complications.

That patients with technical complications had an increased risk for other medical morbidities seems obvious. The >300% increase in the rate of pulmonary complications is consistent with other reports.10,31 Recurrent laryngeal nerve palsy interferes with the normal mechanics of deglutition and, thus, increases the risk of aspiration. In turn, this may translate to a higher mortality rate. Patients with technical complications had an increased hospital mortality rate compared with those without (9.7% to 3.2%) despite similar 30-day mortality rates (2.2% to 1.2%). Modern perioperative care can support most patients for a considerable length of time even in the face of severe complications; thus, hospital mortality rates should better reflect postoperative outcomes. Although the overall rates were lower in this study, this 3-fold increase in deaths after technical complications mirrors that recently reported by Rizk et al.10 (12% to 4%).

Male sex, cirrhosis, proximal third tumors, advanced disease stage (stage III and IV), and incomplete resection (R1/R2) were identified as independent adverse prognostic factors after esophagectomy. It is well accepted that both advanced tumor stage and incomplete resection (R1/R2) result in diminished survival after esophagectomy; however, the effects of male sex and tumor location are less well established. The location of the tumor within the esophagus has been confirmed as an independent predictor of poor survival by several investigators,32,33 but this has been disputed by others.6,25 Esophagectomy for proximal tumors is less likely to result in R0 resection,33 and incomplete resection, in turn, is associated with reduced survival.6,12,25 We found that male sex was an independent predictor for poor long-term survival. A potential role of sex in long-term survival after cancer surgery has previously been suggested, and benefits have been demonstrated for women in colorectal,34,35 lung,36 and esophageal cancer.6,37 In a large Swedish population-based study, a definite survival advantage was identified for women for all malignancies.38 It has been proposed that female sex hormones may confer a survival benefit by inhibiting the establishment of distant metastases.39 Another, less mechanistic, reason cited includes greater self-awareness in women, leading to earlier diagnosis.37 However, the precise reason for a potential survival benefit for women with cancer remains unclear.

In this study, the presence of technical complications was not identified on multivariate analysis to be an independent factor for long-term survival. Several investigators have demonstrated reduced survival associated with the development of postoperative complications for esophageal,10,11 hepatic,40 colon,41 and head and neck42 resections. It is implied, although often not explicitly, that postoperative complications, in some unexplained manner, such as being immunosuppressive, could affect long-term survival. However, the decreased survival rates in these studies most likely merely reflect a higher hospital mortality that accompanies technical errors, as we have shown here and others have suggested.8 Studies do not in general attempt to exclude this effect by performing survival analyses after excluding hospital mortality. We did not detect a difference in survival by univariate or multivariate analysis between patients with and without technical complications in this study, whether or not hospital deaths were excluded. Thus, although technical complications were associated with worse immediate postoperative outcomes, long-term survival was not affected in our patients.

Differences in survival after major cancer resections have been demonstrated in high- compared with low-volume medical centers.43,44 Both increased surgeon45 and hospital46,47 volume have been shown to decrease operative mortality after esophagectomy. These findings have led some to recommend that complex oncological surgery be performed only in centers with experience and sufficient volume. Regionalization of cancer services is in progress in many countries to improve results. Certainly continued self-appraisal and refinement of the surgical techniques of esophagectomy should be the aims of every esophageal surgeon.


   FOOTNOTES
 
Presented at the 19th World Congress of the International Society for Digestive Surgery, Yakohama, Japan, December 8–11, 2004.

Received for publication May 2, 2005. Accepted for publication October 12, 2005.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

  1. Millikan KW, Silverstein J, Hart V, et al. A 15-year review of esophagectomy for carcinoma of the esophagus and cardia. Arch Surg 1995; 130:617–24.[Abstract]
  2. Ellis FH Jr, Heatley GJ, Krasna MJ, Williamson WA, Balogh K. Esophagogastrectomy for carcinoma of the esophagus and cardia: a comparison of findings and results after standard resection in three consecutive eight-year intervals with improved staging criteria. J Thorac Cardiovasc Surg 1997; 113:836–46; discussion 846–8.[Abstract/Free Full Text]
  3. Thomas P, Doddoli C, Lienne P, et al. Changing patterns and surgical results in adenocarcinoma of the oesophagus. Br J Surg 1997; 84:119–25.[CrossRef][Medline]
  4. Hagen JA, DeMeester SR, Peters JH, Chandrasoma P, DeMeester TR. Curative resection for esophageal adenocarcinoma: analysis of 100 en bloc esophagectomies. Ann Surg 2001; 234:520–30; discussion 530–1.[CrossRef][Medline]
  5. Law S, Kwong DL, Kwok KF, et al. Improvement in treatment results and long-term survival of patients with esophageal cancer: impact of chemoradiation and change in treatment strategy. Ann Surg 2003; 238:339–47; discussion 347–8.[Medline]
  6. Ando N, Ozawa S, Kitagawa Y, Shinozawa Y, Kitajima M. Improvement in the results of surgical treatment of advanced squamous esophageal carcinoma during 15 consecutive years. Ann Surg 2000; 232:225–32.[CrossRef][Medline]
  7. Martin RK, Brennan MF, Jaques DP. Quality of complication reporting in the surgical literature. Ann Surg 2002; 235:803–13.[CrossRef][Medline]
  8. Bartels H, Stein HJ, Siewert JR. Preoperative risk analysis and postoperative mortality of oesophagectomy for resectable oesophageal cancer. Br J Surg 1998; 85:840–4.[CrossRef][Medline]
  9. Whooley BP, Law S, Murthy SC, Alexandrou A, Wong J. Analysis of reduced death and complication rates after esophageal resection. Ann Surg 2001; 233:338–44.[CrossRef][Medline]
  10. Rizk NP, Bach PB, Schrag D, et al. The impact of complications on outcomes after resection for esophageal and gastroesophageal junction carcinoma. J Am Coll Surg 2004; 198:42–50.[CrossRef][Medline]
  11. Hirai T, Yamashita Y, Mukaida H, Kuwahara M, Inoue H, Toge T. Poor prognosis in esophageal cancer patients with postoperative complications. Surg Today 1998; 28:576–9.[Medline]
  12. Siewert JR, Stein HJ, Feith M, Bruecher BL, Bartels H, Fink U. Histologic tumor type is an independent prognostic parameter in esophageal cancer: lessons from more than 1,000 consecutive resections at a single center in the Western world. Ann Surg 2001; 234:360–7; discussion 368–9.[CrossRef][Medline]
  13. Orringer MB, Marshall B, Iannettoni MD. Transhiatal esophagectomy: clinical experience and refinements. Ann Surg 1999; 230:392–400; discussion 400–3.[CrossRef][Medline]
  14. Law S, Wong J. Two-field dissection is enough for esophageal cancer. Dis Esophagus 2001; 14:98–103.[Medline]
  15. Chu KM, Law SY, Fok M, Wong J. A prospective randomized comparison of transhiatal and transthoracic resection for lower-third esophageal carcinoma. Am J Surg 1997; 174:320–4.[CrossRef][Medline]
  16. Law S, Fok M, Chu KM, Wong J. Thoracoscopic esophagectomy for esophageal cancer. Surgery 1997; 122:8–14.[CrossRef][Medline]
  17. Law SY, Fok M, Wei WI, et al. Thoracoscopic esophageal mobilization for pharyngolaryngoesophagectomy. Ann Thorac Surg 2000; 70:418–22.[Abstract/Free Full Text]
  18. Law SY, Fok M, Wong J. Pattern of recurrence after oesophageal resection for cancer: clinical implications. Br J Surg 1996; 83:107–11.[Medline]
  19. Law S, Wong J. Does lymphadenectomy add anything to the treatment of esophageal cancer? Adv Surg 1999; 33:311–27.[Medline]
  20. Law S, Fok M, Chu KM, Wong J. Comparison of hand-sewn and stapled esophagogastric anastomosis after esophageal resection for cancer: a prospective randomized controlled trial. Ann Surg 1997; 226:169–73.[CrossRef][Medline]
  21. Law S, Fok M, Chow S, Chu KM, Wong J. Preoperative chemotherapy versus surgical therapy alone for squamous cell carcinoma of the esophagus: a prospective randomized trial. J Thorac Cardiovasc Surg 1997; 114:210–7.[Abstract/Free Full Text]
  22. van Sandick JW, van Lanschot JJ, ten Kate FJ, Tijssen JG, Obertop H. Indicators of prognosis after transhiatal esophageal resection without thoracotomy for cancer. J Am Coll Surg 2002; 194:28–36.[CrossRef][Medline]
  23. Fok M, Law S, Stipa F, Cheng S, Wong J. A comparison of transhiatal and transthoracic resection for oesophageal carcinoma. Endoscopy 1993; 25:660–3.[Medline]
  24. Johnson PR, Kanegoanker GS, Bates T. Indirect laryngoscopic evaluation of vocal cord function in patients undergoing transhiatal esophagectomy. J Am Coll Surg 1994; 178:605–8.[Medline]
  25. Hofstetter W, Swisher SG, Correa AM, et al. Treatment outcomes of resected esophageal cancer. Ann Surg 2002; 236:376–84; discussion 384–5.[CrossRef][Medline]
  26. Karl RC, Schreiber R, Boulware D, Baker S, Coppola D. Factors affecting morbidity, mortality, and survival in patients undergoing Ivor Lewis esophagogastrectomy. Ann Surg 2000; 231:635–43.[Medline]
  27. Patil PK, Patel SG, Mistry RC, Deshpande RK, Desai PB. Cancer of the esophagus: esophagogastric anastomotic leak—a retrospective study of predisposing factors. J Surg Oncol 1992; 49:163–7.[Medline]
  28. Walther B, Johansson J, Johnsson F, Von Holstein CS, Zilling T. Cervical or thoracic anastomosis after esophageal resection and gastric tube reconstruction: a prospective randomized trial comparing sutured neck anastomosis with stapled intrathoracic anastomosis. Ann Surg 2003; 238:803–12; discussion 812–4.[Medline]
  29. Imdahl A, Schoffel U, Ruf G. Impact of neoadjuvant therapy of perioperative morbidity in patients with esophageal cancer. Am J Surg 2004; 187:64–8.[Medline]
  30. Bosset JF, Gignoux M, Triboulet JP, et al. Chemoradiotherapy followed by surgery compared with surgery alone in squamous-cell cancer of the esophagus. N Engl J Med 1997; 337:161–7.[Abstract/Free Full Text]
  31. Hulscher JB, van Sandick JW, Devriese PP, van Lanschot JJ, Obertop H. Vocal cord paralysis after subtotal oesophagectomy. Br J Surg 1999; 86:1583–7.[CrossRef][Medline]
  32. Vigneswaran WT, Trastek VF, Pairolero PC, Deschamps C, Daly RC, Allen MS. Extended esophagectomy in the management of carcinoma of the upper thoracic esophagus. J Thorac Cardiovasc Surg 1994; 107:901–6; discussion 906–7.[Abstract/Free Full Text]
  33. Kato H, Tachimori Y, Watanabe H, Yamaguchi H, Ishikawa T, Kagami Y. Thoracic esophageal carcinoma above the carina: a more formidable adversary? J Surg Oncol 1997; 65:28–33.[Medline]
  34. Wichmann MW, Muller C, Hornung HM, Lau-Werner U, Schildberg FW. Gender differences in long-term survival of patients with colorectal cancer. Br J Surg 2001; 88:1092–8.[CrossRef][Medline]
  35. McArdle CS, McMillan DC, Hole DJ. Male gender adversely affects survival following surgery for colorectal cancer. Br J Surg 2003; 90:711–5.[Medline]
  36. Alexiou C, Onyeaka CV, Beggs D, et al. Do women live longer following lung resection for carcinoma? Eur J Cardiothorac Surg 2002; 21:319–25.[Abstract/Free Full Text]
  37. Micheli A, Mariotto A, Giorgi Rossi A, Gatta G, Muti P. The prognostic role of gender in survival of adult cancer patients. Eur J Cancer 1998; 34:2271–8.[CrossRef][Medline]
  38. Adami HO, Bergstrom R, Holmberg L, Klareskog L, Persson I, Ponten J. The effect of female sex hormones on cancer survival. A register-based study in patients younger than 20 years at diagnosis. JAMA 1990; 263:2189–93.[Abstract]
  39. Badwe RA, Patil PK, Bhansali MS, Mistry RC, Juvekar RR, Desai PB. Impact of age and sex on survival after curative resection for carcinoma of the esophagus. Cancer 1994; 74:2425–9.[Medline]
  40. Laurent C, Sa Cunha A, Couderc P, Rullier E, Saric J. Influence of postoperative morbidity on long-term survival following liver resection for colorectal metastases. Br J Surg 2003; 90:1131–6.[CrossRef][Medline]
  41. Fujita S, Teramoto T, Watanabe M, Kodaira S, Kitajima M. Anastomotic leakage after colorectal cancer surgery: a risk factor for recurrence and poor prognosis. Jpn J Clin Oncol 1993; 23:299–302.[Abstract/Free Full Text]
  42. de Melo GM, Ribeiro KC, Kowalski LP, Deheinzelin D. Risk factors for postoperative complications in oral cancer and their prognostic implications. Arch Otolaryngol Head Neck Surg 2001; 127:828–33.[Abstract/Free Full Text]
  43. Bach PB, Cramer LD, Schrag D, Downey RJ, Gelfand SE, Begg CB. The influence of hospital volume on survival after resection for lung cancer. N Engl J Med 2001; 345:181–8.[Abstract/Free Full Text]
  44. Birkmeyer JD, Warshaw AL, Finlayson SR, Grove MR, Tosteson AN. Relationship between hospital volume and late survival after pancreaticoduodenectomy. Surgery 1999; 126:178–83.[Medline]
  45. Birkmeyer JD, Stukel TA, Siewers AE, Goodney PP, Wennberg DE, Lucas FL. Surgeon volume and operative mortality in the United States. N Engl J Med 2003; 349:2117–27.[Abstract/Free Full Text]
  46. Begg CB, Cramer LD, Hoskins WJ, Brennan MF. Impact of hospital volume on operative mortality for major cancer surgery. JAMA 1998; 280:1747–51.[Abstract/Free Full Text]
  47. van Lanschot JJ, Hulscher JB, Buskens CJ, Tilanus HW, ten Kate FJ, Obertop H. Hospital volume and hospital mortality for esophagectomy. Cancer 2001; 91:1574–8.[CrossRef][Medline]



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