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Ann Thorac Surg 2008;85:424-429. doi:10.1016/j.athoracsur.2007.10.007
© 2008 The Society of Thoracic Surgeons
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Right arrow Esophagus - cancer

Original Articles: General Thoracic

Outcomes After Transhiatal and Transthoracic Esophagectomy for Cancer

Andrew C. Chang, MDa,*, Hong Ji, MScb, Nancy J. Birkmeyer, PhDa,b, Mark B. Orringer, MDa, John D. Birkmeyer, MDa,b

a Department of Surgery, University of Michigan Medical Center, Ann Arbor, Michigan
b Michigan Surgical Collaborative for Outcomes Research and Evaluation (M-SCORE), University of Michigan Medical Center, Ann Arbor, Michigan

Accepted for publication October 2, 2007.

* Address correspondence to Dr Chang, Section of Thoracic Surgery, TC2120G/0344, 1500 East Medical Center Dr, Ann Arbor, MI 48109 (Email: andrwchg{at}umich.edu).


   Abstract
Top
 Abstract
Introduction
 Patients and Methods
 Results
 Comment
 Acknowledgments
 References
 
Background: Although single-center series evaluating esophagectomy for cancer have demonstrated that this operation can be performed safely and with excellent outcomes, controversy remains regarding the comparable oncologic efficacy of the transhiatal and transthoracic approaches. This study was performed to determine outcomes after transhiatal and transthoracic esophagectomy for patients undergoing resection nationwide.

Methods: Using the Surveillance, Epidemiology, and End Results–Medicare linked database (1992 to 2002), we identified registered patients undergoing esophagectomy for esophageal cancer. We evaluated operative mortality, late survival, and length of stay while adjusting for patient characteristics, tumor grade, and stage. As a surrogate for postoperative quality of life, we also assessed subsequent need for anastomotic dilation.

Results: Of 868 patients undergoing either approach, for whom distinct Current Procedural Technology codes could be identified, 225 underwent transhiatal and 643 received transthoracic esophagectomy. Lower operative mortality rate was observed after a transhiatal than transthoracic approach (6.7% versus 13.1%, p = 0.009). Observed 5-year survival was higher for patients undergoing transhiatal rather than transthoracic esophagectomy (30.5% versus 22.7%, p = 0.02). After adjusting for differences in tumor stage, patient, and provider factors, this survival advantage was no longer statistically significant (adjusted hazard ratio for mortality, 0.95, 95% confidence interval: 0.75 to 1.20). Patients undergoing transhiatal esophagectomy were more likely to require endoscopic dilatation within 6 months of surgery (43.1% versus 34.5% for transthoracic operations, p = 0.02).

Conclusions: In the largest population-based study to date assessing long-term outcome after esophagectomy for esophageal cancer, transhiatal esophagectomy confers an early survival advantage, but long-term survival does not appear to differ according to surgical approach.


   Introduction
Top
 Abstract
 Introduction
Patients and Methods
 Results
 Comment
 Acknowledgments
 References
 
Despite improvements in surgical technique, perioperative management, and oncologic care, esophageal cancer remains a highly lethal malignancy causing 13,770 deaths estimated for 2006 [1]. Although most patients present with unresectable disease, in approximately 30% to 40% of patients, esophageal resection remains the mainstay of treatment. On a nationwide basis, esophagectomy carries considerable operative risk, with population-based studies demonstrating operative mortality varying from 8% at "high-volume" centers (those performing on average more than 19 esophagectomies annually) to 23% at "low-volume" centers (performing on average less than 2 esophagectomies annually) [2]. The reasons for such differences in early survival are likely numerous, and currently efforts are being directed toward identifying specific processes of care that might provide the basis for observed volume-outcome correlations.

Operative technique might be considered one such process of care. Although reports from single centers demonstrate excellent outcomes for both transthoracic and transhiatal esophagectomy, there remains considerable debate regarding surgical approach in the management of esophageal cancer. In particular, although it is posited that transthoracic approaches to esophagectomy provide improved surgical exposure for mediastinal lymph node clearance, potentially reducing the risk for locoregional recurrence of esophageal cancers, the long-term oncologic benefit for this strategy has not been well demonstrated. In contrast, as reported in single-center series, perioperative morbidity and mortality after transhiatal esophagectomy are both low, with this operation tolerated better in older patients with significant comorbidity [3–6].

Using data from the national Surveillance, Epidemiology, and End Results (SEER)–Medicare linked database we performed a retrospective cohort study to evaluate late outcomes after esophageal resection, comparing results after either transhiatal or transthoracic esophagectomy.


   Patients and Methods
Top
 Abstract
 Introduction
 Patients and Methods
Results
 Comment
 Acknowledgments
 References
 
Patient Sample
A waiver of informed consent for this study was approved by the Institutional Review Boards of the University of Michigan Medical School. Patients aged 65 to 99 years reported with esophageal carcinoma between 1992 and 2002 were identified from the SEER–Medicare linked database (Fig 1). As detailed elsewhere [7], the SEER database is a nationally-representative collection of population-based registries of all incident cancers from diverse geographic populations in the United States. During this study period, there were 11 SEER regions, representing approximately 14% of the US population. For each Medicare patient in SEER, the SEER-Medicare linked files contain all Medicare claims from the inpatient, outpatient, physician, home health, and hospice files.


Figure 1
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  		Fig 1. Patient identification algorithm. (CPT = Current Procedural Technology; ICD-9 = International Classification of Diseases, version 9; SEER = Surveillance, Epidemiology, and End Results database.)

 
All Medicare patients with incident cases of esophageal cancer were identified from the SEER files, and patients undergoing esophagectomy were identified from the Medicare inpatient file using Current Procedural Technology (CPT) codes and codes from the International Classification of Disease, version 9 (ICD-9). Patients with a diagnosis of esophageal cancer were identified by ICD-9 codes 150.0–150.9 and 151.0, and the following ICD-9 procedural codes were used to identify patients undergoing resection: esophagectomy (42.40–42.42), esophagogastrectomy NOS (43.99), intrathoracic esophagogastrostomy (42.52), antesternal esophagogastrostomy (42.62), partial gastrectomy with anastomosis to esophagus (43.5). The CPT codes for transhiatal esophagectomy included 43107 and 43119; and for transthoracic esophagectomy, we included 43112, 43117, 43121, and 43122. We identified patients who subsequently had anastomotic stricture (ICD-9 code, 530.3) or required esophageal dilation (ICD-9 codes 42.2, 42.92).

Excluded from analysis were patients who, based on the following procedural codes, had undergone complex reconstruction including colon or small bowel interposition (CPT: 43108, 43113, 43116, 43118, 43123).

Analysis
Our primary outcome measure was mortality, determined at 5 years from the date of operation or through December 31, 2002, the end of the follow-up period. We used Cox proportional hazards models to examine relationships between operative approach and mortality, adjusting for patient characteristics, censoring at the end of the follow-up period. We used {chi}2 analysis to evaluate differences between groups for categorical variables. We adjusted for age group (65 to 69 years, 70 to 74, 75 to 79, 80 to 84, 85 and over), sex, race (black, nonblack), and their interactions, year of procedure, and acuity of the index admission (elective, urgent, emergent), and patient comorbidities.

Comorbidities were identified using information from the index admission and inpatient encounters from the preceding 6 months [8]. As described elsewhere [9, 10], inpatient, outpatient, and physician claims files were used to identify patients receiving chemotherapy or radiation therapy, defined as treatment occurring within 6 months before or after surgery. We also adjusted for provider characteristics potentially associated with improved late survival after cancer surgery, including hospital teaching status and hospital volume divided into low, medium, and high terciles. Because patients often cross SEER boundaries for their care, relying on SEER-Medicare data alone to assess procedure volumes may misclassify the volume status of some hospitals [11]. For this reason, hospital volume was assessed using 100% Medicare data, as described elsewhere [12].


   Results
Top
 Abstract
 Introduction
 Patients and Methods
 Results
Comment
 Acknowledgments
 References
 
Patient and Provider Characteristics
Patient characteristics, including demographic data, admission acuity, and number of comorbidities were similar between patients undergoing transthoracic and transhiatal esophagectomy. Patients undergoing transthoracic approaches were less likely to have localized disease, as recorded in the SEER registry, but no significant differences were observed in the frequency of patients receiving chemotherapy or radiation treatment. Transhiatal esophagectomy was performed more frequently in the highest volume tercile of centers performing esophagectomy. Medical centers designated as "teaching hospital" performed transhiatal esophagectomy more commonly, although this difference was not statistically significant (Table 1).


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  		Table 1 Characteristics of Patients and Providers, SEER-Medicare Database, 1992 to 2002
 
Survival, Unadjusted and Adjusted
Patients undergoing transhiatal esophagectomy had a lower operative mortality rate (Table 2) than those undergoing transthoracic operations (6.7% versus 13.1%, p = 0.009). Observed 5-year survival (Fig 2) was also higher with transhiatal than with transthoracic esophagectomy (30.5% versus 22.7%, p = 0.02). The benefits conferred by transhiatal esophagectomy were diminished after adjustments for patient and hospital/provider characteristics (Table 3).


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  		Table 2 Outcomes
 

Figure 2
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  		Fig 2. Kaplan-Meier plots describing overall survival for patients undergoing either transthoracic esophagectomy (TTE [solid line]) or transhiatal esophagectomy (THE [dashed line]), based on the SEER-Medicare linked database, 1992 to 2002.

 

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  		Table 3 Association Between Two Esophagectomy Procedures (Transthoracic Versus Transhiatal) and Late Survival, With and Without Adjustment for Patient and Provider Characteristics
 
Esophageal Dilatation
Anastomotic complications can result in considerable impairment of postoperative quality of life, particularly for a procedure designed to restore comfortable swallowing. As a surrogate for anastomotic complication, particularly postoperative dysphagia, we identified patients who required endoscopic esophageal dilatation within the first 6 months of operation. Patients undergoing transhiatal esophagectomy were more likely to require endoscopic dilatation (43.1% versus 34.5% for transthoracic operations, p = 0.02).


   Comment
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
Acknowledgments
 References
 
Our study is the largest nationwide population-based study to date assessing long-term outcome after esophagectomy for esophageal cancer. We identified a cohort of 868 patients undergoing esophagectomy for cancer between 1992 and 2002. The SEER registry accrues data from 11 regions, representing 14% of the US population. By combining cancer-specific data with Medicare administrative claims data, we can evaluate outcomes primarily for patients 65 years of age or greater. Despite this possible limitation, the SEER-Medicare database remains a fair representation of nationwide practices, particularly for operations such as esophagectomy, which tend to be performed in nonrural areas. While we found an early survival advantage for transhiatal esophagectomy, there was no advantage to a transhiatal approach compared with transthoracic operations with regard to long-term survival after adjustment for tumor stage, patient and provider factors. Patients undergoing transhiatal esophagectomy were also more likely to require endoscopic dilatation within 6 months of surgery.

The outcomes of transthoracic and transhiatal approaches for esophagectomy have been assessed previously in a number of single-center studies and were compared among patients undergoing operation at Veterans’ Affairs medical centers nationwide by the National Surgical Quality and Improvement Program (NSQIP). Analysis of early outcomes demonstrated 30-day mortality of approximately 10% for both approaches [13] despite the additional observations that postoperative pneumonia and myocardial infarction occurred more frequently among patients undergoing transthoracic esophagectomy. Long-term outcomes and survival were not reported in this study.

Several hospital characteristics that we examined were associated with improved unadjusted early and late survival conferred by a transhiatal approach, including hospital volume and teaching hospital status. Even after adjusting for these factors, 5-year cancer survival was at least equivalent for both surgical approaches. These two factors might be surrogates for other processes of care such as individual surgeon experience, which also appears to have a significant impact on operative mortality, as has been demonstrated previously at a national level [14] and within single institutions [15]. Other specific processes of care underlying these differences remain undefined [16]. In the SEER-Medicare population studied, most patients underwent operation electively, as expected, but a minority of patients continued to require urgent operation. This might indicate patients undergoing operation because of high-grade obstruction or because of iatrogenic complications such as perforation during evaluation for presenting symptoms such as dysphagia.

In our study, patients undergoing transhiatal esophagectomy were more likely to have earlier stage malignancy. There may be several reasons accounting for this difference. The extent of lymph node dissection may be greater for patients undergoing a transthoracic approach, providing greater opportunity to determine esophageal cancer staging [17]. Such "stage migration" also has been proposed as a reason for differences previously observed in long-term survival between transthoracic or transhiatal esophagectomy [4]. Counter to this assertion, it is also recognized that extensive lymph node dissection can be accomplished through transhiatal esophagectomy [18]. While assessments of lymph node counts are included in population-based analyses of outcomes after procedures such as colorectal operations, such data typically were not recorded for esophageal cancer in the SEER database. As potentially more precise diagnostic modalities, such as combined computed tomography and positron-emitting tomography and esophageal endoscopic ultrasound, become utilized, improved accuracy in clinical staging may provide for increasingly valid comparisons of treatment regimens. The SEER database might be criticized for imprecise staging for patients with esophageal cancer, but it is unlikely that there are systematic variances across hospitals regarding reporting of cancer stage that would bias the findings of our study.

The role of multimodality treatment, including chemotherapy or radiation therapy in addition to resection, administered either preoperatively or in an adjuvant setting, remains controversial [19]. Although preoperative chemoradiation regimens appear to yield improved R0 (complete) resection [20, 21], improvement in overall survival has not been demonstrated convincingly, perhaps owing to increased perioperative complications observed in patients receiving preoperative chemoradiation. In contrast, two recent trials have demonstrated a benefit for adjuvant chemoradiation, but only for patients with adenocarcinoma of the gastroesophageal junction [22, 23]. Regardless of these findings, in our analysis, only 29% and 34% of patients received chemotherapy and radiotherapy, respectively, with no differences in the delivery of these processes of care observed between the two surgical groups. This likely reflects the older age distribution of patients inherent in the SEER-Medicare database.

Overall, nearly 37% of all patients studied required at least one esophageal dilatation, consistent with previous reports evaluating long-term sequelae after transthoracic or transhiatal esophagectomy. We observed that more patients undergoing a transhiatal approach (43.1% versus 34.5%, p = 0.02) required esophageal dilatation. The need for esophageal dilatation has been most commonly associated with development of an anastomotic stricture, but other reasons, particularly incomplete emptying of the esophageal substitute, may necessitate postoperative dilatation. Although this study did not evaluate postoperative quality of life, others have shown that postoperative dysphagia after operation to restore comfortable swallowing may impede patient recovery and affects patients’ assessment of social functioning, although overall self-reported quality of life did not appear to differ in long-term esophageal cancer survivors, when compared to national norms [24, 25].

The SEER-Medicare linked databases provide aggregate information regarding cancer diagnosis, treatment, and outcomes not readily available from either dataset separately, and can generate a snapshot of surgical practice in the treatment of esophageal cancer. Although these linked databases do not include patients covered by health maintenance organizations, these data provide an accurate reflection of the older US population [7]. Although the early survival advantage conferred for patients undergoing transhiatal esophagectomy might indicate a systematic bias, in which this operation is reserved for older patients or for those with significant comorbidity, we would not expect this to result in the equivalent 5-year survival observed. It is also possible that the observed early survival advantage after transhiatal esophagectomy might be a reflection of as yet undefined differences in processes of health care delivery.

There are several limitations in this study that might attenuate the reported findings. Although inaccurate coding of surgical procedure would hinder proper assignment of a given patient to either surgical group, such an error would diminish rather than increase any observed differences between transthoracic and transhiatal approaches. Several factors, including SEER cancer stage and hospital procedural volume, were found to differ significantly between patients treated by transthoracic esophagectomy or transhiatal esophagectomy. This raises the possibility of confounding by other unmeasured variables. For example, in the SEER registry, esophageal cancer histology, namely, squamous cell carcinoma or adenocarcinoma, is not well distinguished. It is recognized, however, that the prevalence of adenocarcinoma is rising in the United States [26], not only in population-based studies but also in several large surgical series [27, 28]. While it is possible that patients with squamous cell carcinoma of the esophagus, which tends to have worse long-term survival, might undergo transthoracic rather than transhiatal esophagectomy, fewer patients with squamous cell carcinoma are likely to undergo operation overall. Moreover, there have been no large reported series indicating such a bias in favor of one surgical approach based on tumor histology.

In conclusion, patients undergoing transhiatal esophagectomy for esophageal cancer demonstrate improved 30-day mortality and equivalent 5-year overall survival when compared with transthoracic approaches. Long-term survival after esophagectomy for esophageal cancer remains poor regardless of current surgical approaches, emphasizing the need for continued improvements in operative technique, perioperative management and especially other treatment modalities, derived from more thorough understanding of esophageal tumor biology.


   Acknowledgments
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Acknowledgments
References
 
This study was supported by the National Cancer Institute: 1 R01 CA098481-01A1 (J.D.B.).


   References
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Acknowledgments
 References
 

  1. http://seer.cancer.gov/csr/1975_2003/Accessed on Jan 8, 2007.
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