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Ann Thorac Surg 2002;74:1026-1032
© 2002 The Society of Thoracic Surgeons

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Original article: general thoracic

An analysis of multiple staging management strategies for carcinoma of the esophagus: computed tomography, endoscopic ultrasound, positron emission tomography, and thoracoscopy/laparoscopy

^a Digestive Diseases Center, Division of Gastroenterology and Hepatology, Medical University of South Carolina, Charleston, South Carolina, USA
^b Center for Health Care Research and Department of Medicine, Medical University of South Carolina, Charleston, South Carolina, USA
^c Dana-Farber Cancer Institute, Boston, Massachusetts, USA
^d Department of Surgery, University of Maryland, Baltimore, Maryland, USA
^e Department of Surgery, Hollings Cancer Center, Medical University of South Carolina, Charleston, South Carolina, USA

Accepted for publication June 7, 2002.

* Address reprint requests to Dr Wallace, Medical University of South Carolina, 96 Jonathan Lucas St, Suite 210-CSB, PO Box 250327, Charleston, SC 29425 USA
e-mail: wallacem{at}musc.edu

	Abstract

Top Abstract Introduction Material and methods Results Comment Acknowledgments References

 
Background. This study compares the health care costs and effectiveness of multiple staging options for patients with esophageal cancer. Techniques studied included computed tomographic (CT) scan, endoscopic ultrasound with fine-needle aspiration biopsy (EUS-FNA), positron emission tomography (PET), thoracoscopy/laparoscopy, and combinations of these.

Methods. A decision-analysis model was constructed to compare different staging strategies. Costs were derived from the Surveillance, Epidemiology, and End Results (SEER)-Medicare linked databases and from other Medicare reimbursement rates. Life expectancies were obtained from the 1973–1996 SEER database and adjusted for quality of life. Cost and effectiveness measures were discounted at 0% and 3% per year. Sensitivity and specificity measures were obtained from the published literature and a parallel prospective clinical trial, and all key variables were subjected to sensitivity analyses.

Results. Under baseline assumptions, CT + EUS-FNA was the most inexpensive strategy and offered more quality-adjusted life-years, on average, than all other strategies with the exception of PET + EUS-FNA. The latter was slightly more effective but also more expensive. The marginal cost-effectiveness ratio for PET + EUS-FNA was $60,544 per quality-adjusted life-year. These findings were robust and changed very little in all of the sensitivity analyses.

Conclusions. The combination of PET + EUS-FNA should be the recommended staging procedure for patients with esophageal cancer, unless resources are scarce or PET is unavailable. In these instances, CT + EUS-FNA can be considered the preferred strategy.

	Introduction

Top Abstract Introduction Material and methods Results Comment Acknowledgments References

 
Esophageal cancer, especially adenocarcinoma, has been increasing in incidence over the past two decades in developed countries [1, 2]. Approximately one third of these patients have metastatic disease at the time of presentation [3, 4]. Although there is controversy regarding the optimal management of esophageal carcinoma, there is consensus that patients with metastatic disease do not benefit from surgical therapy.

The optimal method of detecting metastatic disease in patients with carcinoma of the esophagus is unknown. Several staging modalities are available that vary considerably in effectiveness, cost, and degree of invasiveness. Computed tomography (CT) has been the standard for staging esophageal carcinoma. A CT scan is noninvasive and is the least costly of the available methods, but it has major limitations for detecting locally advanced and metastatic disease [5, 6]. Positron emission tomography (PET) is also noninvasive and provides qualitatively different information from CT because of its reliance on the metabolic function of tumors instead of tumor size alone. Positron emission tomography is costly and has a sensitivity of 46% to 92% and a specificity of 88% to 94% in published trials [7–11]. Endoscopic ultrasound (EUS) is a semiinvasive procedure but is highly accurate for tumor staging and detection of regional metastases to the celiac lymph nodes [12, 13]. The development of thoracoscopy and laparoscopy (TL) has recently allowed highly accurate staging of esophageal tumors and abdominal metastases [14], but this procedure requires a short hospitalization and is substantially more costly than CT scan or EUS. It is currently not known which of these procedures or which combination of these procedures offers the most cost-effective approach for the detection of locally advanced or metastatic disease for patients with carcinoma of the esophagus.

This study compared the costs and effectiveness of six strategies for staging patients with esophageal cancer: CT alone; CT + EUS-fine-needle aspiration biopsy (FNA), CT + TL, CT + EUS-FNA + TL, PET + EUS-FNA, and CT + PET + EUS-FNA. In each case, it was assumed that staging tests were performed sequentially. If distant metastases were found and confirmed, no further staging was performed.

	Material and methods

Top Abstract Introduction Material and methods Results Comment Acknowledgments References

 
To compare the costs and effectiveness of the six strategies, a decision tree was developed using Data 3.5 (TreeAge Software, Inc). The decision analysis including sensitivity analyses, discounting, assessment of test variables, and cost was performed using standard methods of cost-effectiveness analysis [15]. A diagram of the decision model is shown in Figure 1. This model was based on a third-party payer perspective and incorporated the following: the test characteristics for each of the staging techniques; the prevalence of local, regional, and distant disease among patients with esophageal cancer; life expectancies for esophageal cancer patients with local, regional, and distant disease; costs associated with the different staging techniques; costs associated with the treatment and care of patients identified as having local, regional, and distant disease; and probability of death for patients undergoing TL and those undergoing esophageal resection. Using these data within the model, costs and life expectancies were simulated for hypothetical cohorts of patients.

View larger version (31K): [in this window] [in a new window]   Fig 1. Esophageal cancer staging model. (Conf. Bx = confirmatory biopsy; CT = computed tomography; EUS = endoscopic ultrasound; L/R = local or regional disease; PCO = palliative care only; PET = positron emission tomography; R & FU = esophageal resection and follow-up treatment; TL = thoracoscopy and laparoscopy.)

Using the SEER-Medicare databases, a retrospective cohort was created consisting of all Medicare-eligible patients whose invasive esophageal cancer was diagnosed between January 1, 1991, and December 31, 1996. Patients were excluded if they had had any prior cancer or if they were enrolled in a health maintenance organization at some time during the study period and therefore did not have complete treatment information. Patients were also excluded if the dates of diagnosis (or death) differed by more than 2 months in the SEER and Medicare databases, or if the cancer was first identified at the time of death or postmortem examination. The cost of esophageal cancer care was then calculated using Medicare reimbursements as a proxy for costs, adjusted for time and geographic factors into constant 1998 US dollars and then inflated with the consumer price index into 2000 US dollars. In addition to the inflation adjustments, costs estimates were made using both a 0% and a 3% discount rate to take into account the time value of money. Because the Health Care Financing Administration files include cost data only on patients older than 65 years, the costs for younger patients were inferred by adjusting the overall downstream costs for the stage distribution observed for patients of all ages. All costs are reported in 2000 US dollars.

For each of the six strategies, the average cost was determined for hypothetical cohorts of patients. Using these data in conjunction with the life expectancy data obtained from the SEER database, marginal cost-effectiveness ratios were calculated. Each model variable was subjected to sensitivity analysis to determine which variables had the greatest effects on the cost-effectiveness measures for each strategy.

	Results

Top Abstract Introduction Material and methods Results Comment Acknowledgments References

 
Under baseline assumptions, the costs of CT + EUS-FNA are lower than those of CT alone, CT + TL, CT + EUS-FNA + TL, CT + PET + EUS-FNA, and PET + EUS-FNA. The effectiveness of each technique (as measured in quality-adjusted life-years [QALYs]) is greatest using the PET + EUS-FNA strategy compared with the others primarily because of the confirmatory biopsy carried out for patients testing positive for distant disease. This biopsy reduced the false-positive rate and accordingly extended life for those who would have received only palliative care under the other strategies. Predicted outcomes for each of the six staging strategies are summarized in Table 2.

Because of the dominance of CT + EUS-FNA over four other strategies, the cost-effectiveness analysis was reduced to a comparison between CT + EUS-FNA and PET + EUS-FNA FNA. Compared with CT + EUS-FNA, PET + EUS-FNA is slightly more expensive (by $4,158 on average), yet also slightly more effective (by 0.0687 QALY [almost 1 quality adjusted life-month], on average). The marginal cost-effectiveness ratio comparing PET + EUS-FNA with CT + EUS-FNA is $60,544 per QALY, a ratio that is less than that of other accepted medical treatments.

The baseline results were extremely robust with respect to changes in the model variables. When the model variables were subjected to sensitivity analyses, CT + EUS-FNA continued to dominate all strategies with the exception of PET + EUS-FNA. For example, when the cost of EUS-FNA ranged from $500 to $1,000, CT + EUS-FNA remained the least expensive option and the most effective option, again with the exception of PET + EUS-FNA. For either of the strategies that included TL to prove to be the optimal strategy, the cost of TL would have to have been less than $1,100. In those extreme circumstances, CT + TL would provide the most effective outcomes and be the most inexpensive strategy.

A few of the sensitivity analyses demonstrated a somewhat higher marginal cost-effectiveness ratio for PET + EUS-FNA, albeit at the extremes of those analyses. This marginal ratio increased (ie, PET + EUS-FNA became less cost effective) to approximately $100,000 per QALY if the life expectancy for local disease with resection was 2.8 years, if the quality of life utility for unresected local or regional disease was close to 1.0 (equivalent to perfect health), or if the quality of life utility for resected local or regional disease was close to 0 (equivalent to death).

	Comment

Top Abstract Introduction Material and methods Results Comment Acknowledgments References

 
This decision analysis suggests that PET scanning followed by EUS with FNA (of abnormal lymph nodes or metastases) provides the most cost-effective strategy for preoperative staging and management of patients with carcinoma of the esophagus. Computed tomographic scanning followed by EUS-FNA is also cost effective. Both strategies are more effective and less costly than CT alone or combinations of CT with TL. The marginal cost-effectiveness of PET + EUS-FNA (approximately $60,000 per QALY) is in line with other commonly accepted cancer-screening methods such as mammography [17–19]. The use of CT alone would result in a large proportion of esophagectomies being performed on patients with unrecognized (by CT) metastatic disease. The addition of TL to CT and EUS-FNA does detect a small number of patients with locally advanced or metastatic disease missed by CT and EUS-FNA, but adding TL was not cost effective in our model because of the high cost of surgical staging and the small but measurable mortality and morbidity of general anesthesia and TL. Using EUS-FNA, TL, or both to classify a patient’s cancer stage will lead to substantially lower proportions of unnecessary esophagectomies (<1%). However, EUS-FNA and TL are fairly comparable with respect to sensitivity, and the costs of performing TL ($15,329) far exceed those of EUS-FNA ($723). Thus, the strategy of PET + EUS-FNA or CT + EUS-FNA results in relatively few unnecessary esophagectomies and costs substantially less than any staging procedure involving TL.

Multiple studies [6, 12, 20] have previously demonstrated the superiority of EUS over CT scanning for staging carcinoma of the esophagus. The limitations of these studies included comparison with conventional "slice" CT and the inability to pass an endoscope through an obstructing esophageal tumor. More recently, the use of esophageal dilation to complete EUS-FNA staging has been proven to be a safe and effective procedure for detection of celiac lymph node metastases [13]. Comparisons of EUS-FNA with spiral CT have also determined that EUS-FNA is superior to current-generation CT scanners [16]. Although more invasive than CT scanning, EUS-FNA is a safe procedure with an overall procedure-related morbidity of less then 1 per 300 cases [21].

Positron emission tomographic scanning is also noninvasive and provides qualitatively different information from CT because of its reliance on the metabolic function of tumors instead of tumor size alone. A major advantage of PET scanning is the rapid assessment of whole-body imaging for distant metastases. Positron emission tomography has recently been approved for the staging of esophageal carcinoma. The principal disadvantages of PET are the cost, the availability, and the variable sensitivity of 46% to 92% and specificity of 88% to 94% in published trials [7–11].

The feasibility of combined TL for staging patients with carcinoma of the esophagus has recently been evaluated in a multicenter clinical trial (CALGB 9380) [14]. This study reported results in 113 patients, and the strategy was feasible in 73% of them. In comparison to preoperative testing, TL identified involved lymph nodes or metastatic disease previously missed by CT scan in 50% of patients, by magnetic resonance imaging in 40%, and by EUS in 30%. Median operating time was 210 minutes, and median hospital stay was 3 days. No deaths or major complications occurred. This study demonstrates that TL is a highly accurate method of staging patients with carcinoma of the esophagus. The principle disadvantages are the cost and the hospitalization required.

Our study has several limitations. By their nature, decision-analysis studies are limited by the accuracy of their assumptions. For the purposes of these studies, we based the assumptions for the accuracy of PET, CT, EUS-FNA, and TL on conservative estimates from the published literature. We also subjected these assumptions to broad sensitivity analyses of key variables including the accuracy of the test and its cost.

The validity of our study is also based on the accuracy of our cost assumptions for the staging evaluation. We have based the cost estimates for all staging procedures on uniform Medicare reimbursement rates. The cost assumption for TL specifically was based on hospital reimbursement rates for the diagnostically related group of Medicare reimbursement for patients with carcinoma of the esophagus. Last, these costs were subject to broad sensitivity analyses that demonstrated that the cost of TL would have to be lower than $1,100 (the baseline Medicare reimbursement was $15,329).

We minimized the use of assumed data by using actual treatment costs and outcomes from the SEER and Medicare databases for patients with esophageal cancer. The downstream cost of care for esophageal cancer was estimated from actual Medicare costs for the cohort of patients enrolled in the SEER registry. By using the data from the SEER-Medicare databases, we were able to capture all costs and outcomes (mortality) of patients from the time of diagnosis to death. These costs were also subject to broad sensitivity analyses, and the conclusions were robust under all possible assumptions.

Our model assumed that patients with known metastatic disease (M1b) or tumors that had invaded regional organs (T4) did not undergo operation. This clinical algorithm, although widely practiced, does not match precisely the SEER or American Joint Committee on Cancer staging algorithm. Celiac lymph node involvement is staged as metastatic according to the American Joint Committee on Cancer and SEER staging algorithm [22, 23]. The American Joint Committee on Cancer system subclassifies celiac lymph node involvement as M1a if the tumor is in the distal esophagus and M1b if the tumor is in the proximal esophagus. Although there is consensus that patients with distant metastases (and M1b) do not benefit from surgical intervention, there is controversy regarding metastases to celiac lymph nodes with distal tumors (stage M1a) [24]. The cost and outcome (survival) variables in our model are based on patients treated at SEER centers. This likely reflects a variety of practice patterns regarding the management of M1a disease. If patients with M1a disease were treated similarly to patients without metastatic disease, the value of EUS-FNA and of laparoscopy in patients with distal tumors would be slightly diminished, as these methods are partially aimed at detecting celiac lymph node involvement. This would have minimal impact, however, on the results of our model because EUS-FNA and TL identify other distant metastases (and M1b celiac lymph nodes) and locally advanced disease. The detection of M1a disease by either EUS-FNA or TL would still have some value in directing the need of combined modality therapy.

Decision-analysis studies are also subject to the design of the model, which reflects the clinical algorithm for management of patients. In this study, the staging algorithm was specified according to the protocol. However, downstream management including chemotherapy, radiation therapy, and esophagectomy cost were based on actual procedures for all Medicare patients in the SEER-Medicare databases. For the purposes of the model, however, we assumed that patients with metastatic disease (M1b) did not undergo surgical esophagectomy but only palliative therapy including stents or radiotherapy and chemotherapy. The results of this study may not apply to patients who have substantially different therapy or outcomes than those in the SEER-Medicare registries. This includes younger patients who may have less comorbidity than patients enrolled in Medicare who are by definition older than age 65 years.

In conclusion, this study suggests that patients with a diagnosis of carcinoma of the esophagus should undergo initial PET staging and if no metastatic disease is identified, EUS. Computed tomographic scanning followed by EUS-FNA is slightly less expensive and less effective than PET + EUS-FNA but remains a valid alternative and should be used where PET is not available. Although TL would identify some additional patients with advanced disease, this study suggests that it has little additional benefit. The findings of this decision analysis should be further studied and supported by prospective clinical trials that integrate these staging modalities into treatment algorithms.

	Acknowledgments

Top Abstract Introduction Material and methods Results Comment Acknowledgments References

 
This work was funded, in part, by a grant from the American Digestive Health Foundation, TAP Pharmaceuticals Outcomes Research Award.

	References

Top Abstract Introduction Material and methods Results Comment Acknowledgments References

 

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This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to Personal Folders Download to citation manager Author home page(s): Mark J. Krasna Carolyn E. Reed Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Wallace, M. B. Articles by Reed, C. E. Search for Related Content PubMed PubMed Citation Articles by Wallace, M. B. Articles by Reed, C. E.