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Ann Thorac Surg 2008;86:934-940. doi:10.1016/j.athoracsur.2008.05.002
© 2008 The Society of Thoracic Surgeons
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Original Articles: General Thoracic

Radiotracer-Guided Thoracoscopic Resection is a Cost-Effective Technique for the Evaluation of Subcentimeter Pulmonary Nodules

Eric L. Grogan, MD, MPHa,*, George J. Stukenborg, PhD, MAb, Alykhan S. Nagji, MDa, Winsor Simmons, RNa, Benjamin D. Kozower, MDa, David R. Jones, MDa, Thomas M. Daniel, MDa

a Department of Surgery, Division of Thoracic and Cardiovascular Surgery, University of Virginia School of Medicine, Charlottesville, Virginia
b Department of Public Health Sciences, Biostatistics and Epidemiology, University of Virginia School of Medicine, Charlottesville, Virginia

Accepted for publication May 5, 2008.

* Address correspondence to Dr Grogan, Thoracic and Cardiovascular Surgery, Heart & Vascular Center, PO Box 800679, University Virginia Health System, Charlottesville, VA 22908-0679 (Email: elg9q{at}virginia.edu).

Presented at the Forty-fourth Annual Meeting of The Society of Thoracic Surgeons, Fort Lauderdale, FL, Jan 28–30, 2008.


   Abstract
Top
 Abstract
Introduction
 Material and Methods
 Results
 Comment
 Discussion
 Acknowledgments
 References
 
Background: Excisional biopsy of small subcentimeter pulmonary nodules can be difficult using standard thoracoscopic techniques and may require thoracotomy. Radiotracer-guided thoracoscopic resection (RGTR) was developed to facilitate resection of intraparenchymal subcentimeter pulmonary nodules. Decision analysis, used to model cost and effectiveness, is useful to compare treatment options. We hypothesize that RGTR strategy is more cost-effective compared with thoracotomy for subcentimeter pulmonary nodules.

Methods: The cost-effectiveness of RGTR versus thoracotomy for evaluating highly suspicious subcentimeter pulmonary nodules was examined with a decision analysis model (Fig 1). A 40-patient institutional cohort who underwent RGTR was used to estimate probabilities and costs of the two treatment options within the model. Effectiveness was estimated using 5-year, stage-specific cancer survival and population survival curves. The Society of Thoracic Surgeons General Thoracic Database was queried obtaining mortality estimates for thoracotomy and thoracoscopic wedge resections. These were used to adjust the 5-year survival estimates of patients with benign disease. Sensitivity analyses determined model robustness and the thresholds at which the most cost-effective strategy changed.


Figure 1
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  		Fig 1. Decision analysis model. Decision tree showing the two treatment choices for evaluating a highly suspicious solitary pulmonary nodule (SPN) in which traditional thoracoscopy is not possible because of the location of the nodule. The clinician has two strategies (fltns = decision node); one is to perform a radiotracer-guided thoracoscopic resection (RGTR) or a traditional thoracotomy. The patient may or may not have a successful radiotracer-guided thoracoscopic resection procedure that relates to the probability of success ({circ} = the occurrence of chance events-chance node). Probability of 5-year survival is based on the disease found and the costs of the strategy ((lefttriangle) = terminal node). Estimated probabilities and costs are listed in Table 1.

 
Results: Radiotracer-guided thoracoscopic resection was 95% successful with no mortality. The average cost-to-effectiveness ratio of RGTR strategy was $27,887 versus $32,271 for thoracotomy. Sensitivity analyses demonstrated that the thoracotomy strategy was more cost-effective if the estimated cost of RGTR increased by 33% or the estimated cost-effectiveness of thoracotomy decreased by 14% or more. Radiotracer-guided thoracoscopic resection was more cost-effective as long as the probability of success was greater than 44%.

Conclusions: Decision analysis is a useful tool to evaluate treatment options for thoracic surgeons, and RGTR is a more cost-effective strategy than thoracotomy for subcentimeter pulmonary nodules.


   Introduction
Top
 Abstract
 Introduction
Material and Methods
 Results
 Comment
 Discussion
 Acknowledgments
 References
 
Lung cancer is the number one cause of cancer mortality in the United States [1]. This remains true despite the steady decline in incidence of lung cancer, increased awareness of the general population, and advent of new technologies to detect cancers in early stages. However, patients who have stage IA lung cancer and undergo surgical resection have nearly an 85% to 92% 5-year survival [2, 3].

Trials to determine whether screening reduced mortality conducted in the 1970s using chest radiography and sputum cytology found that nearly 40% of lung cancers detected were found to be stage I when implementing both modalities; however, these studies did not demonstrate a decrease in lung cancer mortality [4]. The introduction of the low-dose computed tomography scan greatly improved the likelihood of the detection of pulmonary nodules. In response, several large trials were conducted to evaluate the usefulness of using this tool as a screening modality. These studies have found that greater than 80% of the nodules detected were stage IA and typically less than 1 cm in size but currently have mixed results with regard to improving survival from lung cancer [5–7]. Randomized controlled trials are being conducted that will hopefully clarify the role of low-dose computed tomography scans in lung cancer screening [8, 9].

Given the increased detection of solitary pulmonary nodules and the high rate of 5-year survival after surgical resection, thoracic surgeons are being asked to diagnose, evaluate, and treat a greater number of subcentimeter pulmonary lesions. In addition, recent changes in the American College of Chest Physician guidelines recommend a tissue diagnosis for nodules greater than 5 mm that have "unequivocal evidence of growth" [10]. We have previously reported our development and success of radiotracer-guided thoracoscopic localization and excision using a technetium 99m-labeled microalbumin aggregate [11–13]. This technique is safe and effective but is more costly because of the computed tomography-guided radiotracer injection procedure and nuclear medicine study. The purpose of this study was to determine whether radiotracer-guided localization and excision of 5- to 10-mm highly suspicious solitary pulmonary nodules not easily removed by traditional thoracoscopic procedures is a cost-effective treatment option compared with thoracotomy.


   Material and Methods
Top
 Abstract
 Introduction
 Material and Methods
Results
 Comment
 Discussion
 Acknowledgments
 References
 
A decision analysis model (Fig 1) was used to assess the cost-effectiveness of radiotracer-guided thoracoscopic biopsy versus thoracotomy for the surgical treatment of highly suspicious solitary pulmonary nodules 5 to 10 mm in size. Nodules were defined as highly suspicious if they were determined by a thoracic surgeon to have a high probability of malignancy based on the increase in size or characteristics of the nodule. The model represents key outcomes after each surgical treatment alternative, along with estimated probabilities for these events, probabilities of 5-year survival associated with alternative outcomes, and total costs. In the radiotracer-guided thoracoscopic resection (RGTR) arm, patients in whom thoracoscopy was unsuccessful required a thoracotomy. Patients without lung cancer (benign or metastatic) who had a successful thoracoscopic biopsy did not require a thoracotomy. Outcomes for the RGTR and thoracotomy arms included lobectomy for patients diagnosed with lung cancer (stage IA or stage non-IA). The study was approved by the University of Virginia Institutional Review Board, and individual consent was waived.

Data Sources
Multiple sources of data were used to estimate event probabilities, probabilities of 5-year survival, and costs included in the decision analysis model. The Society of Thoracic Surgeons Database was used as the source for current estimates of perioperative mortality after thoracoscopy and thoracotomy [14]. Outcomes after RGTR were estimated using the University of Virginia Thoracic Database, reflecting the experience of the thoracoscopy and thoracotomy patients at University of Virginia Health Sciences system. The costs of care were estimated using data from the University of Virginia Clinical Data Repository, which identifies all chargeable events for patients at the University of Virginia Health Sciences system [15]. The National Cancer Institutes SEER Database was the source for life expectancy data for patients with neoplasms other than lung cancer [16]. Life expectancy estimates for patients with benign disease were obtained from the US National Vital Statistics estimates using the average age of patients with this outcome in the cohort [17]. Additional estimates were obtained from prior studies in the medical literature. Table 1 lists the baseline, minimum, and maximum values for each estimate included in the model and the data sources for each estimate.


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  		Table 1 Probabilities and Costs Used in Decision Tree Analysis
 
Event Probabilities
Baseline probability estimates for outcome events in the model reflect the observed history of 40 patients with small pulmonary nodules (5–10 mm) treated at the University of Virginia Health Sciences Center. Patients in the cohort were assigned to radiotracer placement and attempted thoracoscopic localization and resection, followed by thoracotomy and lobectomy for patients with non–small cell lung cancer (NSCLC). Radiotracer placement was successful for 38 of 40 cases (95.0%). Two patients with unsuccessful radiotracer placement from spillage into the thoracic cavity were converted to thoracotomy to obtain a biopsy. The probability of perioperative death after thoracoscopy (1.4%) and thoracotomy (3.2%) was estimated from the overall experience of patients in the Society of Thoracic Surgery Database for years 2003 through 2006. Confidence intervals for these estimates were obtained from the minimum and maximum annual rates reported during this period.

In the University of Virginia cohort, primary NSCLC was found for 13 of 40 (32.5%) resected nodules: 12 of 13 (92.3%) stage IA, 1 of 13 stage IIIB (from a small second intralobar lung cancer). Metastatic cancer from non-lung primary was diagnosed for 4 of 40 (10.0%), and 23 of 40 (57.5%) were determined to be benign. Because only 1 patient among the 13 with primary NSCLC had stage non-IA disease, outcomes for NSCLC patients were dichotomized into stage IA and stage non-IA (stage IB through stage IV). Published case series indicate that between 79% and 93% of resected NSCLC are stage IA [2, 18]. Plausible minimum and maximum values for event probabilities in the model were obtained from previously reported case series [2, 13, 18–22].

Outcomes
Estimated probabilities of survival at 5 years were used to compare the effectiveness of the treatment alternatives. These probabilities were drawn from 5-year survival outcomes reported for a case series of 83 patients with NSCLC nodules of 1 cm or less [2]. For patients with stage IA, 5-year overall survival was 94% (95% confidence interval, 79% to 98%) [23, 24]. For stage non-IA, 5-year survival was 48% (range, 12% to 77%) [2, 23, 24]. The probability of 5-year survival among patients with other cancers was estimated to be 67.4% (95% confidence interval, 51% to 90%). This range was derived from the National Cancer Institutes SEER Database [16] and based on the metastatic cancers excised in the University of Virginia Cohort (breast, colon, melanoma, prostate, cervical, renal, prostate, and pancreas). The probability of 5-year survival for patients with benign disease was estimated to be 0.913, which is the probability of 5-year survival for the total US population at age 65 in 2002, as reported in the US National Vital Statistics reports [17]. The mean age of the 40 patients treated at the University of Virginia Health Sciences Center was 65 years.

Costs
Cost estimates were obtained by calculating total charges among the 40 patients in the study cohort, for all charges occurring during their hospitalization (Table 2). Patients in the University of Virginia cohort were grouped into those who received RGTR only for patients with metastatic or benign disease, those with unsuccessful RGTR with conversion to thoracotomy, and those with RGTR followed by thoracotomy for patients with NSCLC. Patient-specific charge data were abstracted from the University of Virginia Clinical Data Repository [15]. Total charge data were available for 34 of the 40 cases in the Virginia cohort: 31 RGTR only, 2 unsuccessful thoracoscopic cases, and 11 patients who had RGTR followed by thoracotomy. Total charges were summarized by patient, and then by category of patient, to obtain median charges and minimum and maximum charges for patients in each group. Charges for thoracotomy were estimated by subtracting the estimated cost of the radiotracer localization procedure ($4,008, reported by University of Virginia medical center finance office, radiology) from the total charges for patients with unsuccessful RGTR with conversion to thoracotomy.


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  		Table 2 Cost-Effectiveness Analysis Results Summary
 
Baseline and Sensitivity Analysis
The model was formulated and analyzed using Treeage Pro 2006 (Williamstown, MA). Baseline estimates for each model component were used to calculate the cost-effectiveness ratio.

One-way sensitivity analyses were performed to assess the change in the estimated cost-effectiveness ratio within clinically plausible ranges of the estimated components, and to identify whether any thresholds existed at which the best treatment option would change. Two-way sensitivity analyses were performed for estimated components that obtained changes in the relative cost-effectiveness of the treatment alternatives within plausible values of these estimates.


   Results
Top
 Abstract
 Introduction
 Material and Methods
 Results
Comment
 Discussion
 Acknowledgments
 References
 
Radiotracer-guided thoracoscopic resection had both lower cost ($27,887 versus $32,271) and greater effectiveness (0.8785 versus 0.8696) than thoracotomy, using the baseline values for each estimated component in the model. Results from the one-way sensitivity analysis demonstrated that the thoracotomy strategy obtained lower total average cost if the estimated cost of RGTR was increased by 33% (or more) or if the estimated cost of thoracotomy was decreased by 14% (or more). The results were not sensitive to any other plausible changes in the estimated components. Complete results for the one-way sensitivity analyses are summarized in Table 3. Figure 2 presents results from the two-way sensitivity analysis performed for cost of RGTR and cost of thoracotomy treatment options, and displays the threshold at which higher (or lower) cost per unit of effect is obtained for alternative combinations of these two estimates.


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  		Table 3 One-Way Sensitivity Analysis Results a
 

Figure 2
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  		Fig 2. Two-way sensitivity analysis of cost-effectiveness of radiotracer-guided thoracoscopic resection (RGTR) versus thoracotomy. The dark area includes all combinations of the two estimates in which radiotracer-guided thoracoscopic resection is dominant. As the cost of thoracotomy increases, radiotracer-guided thoracoscopic resection becomes the preferred more cost-effective strategy (dark area). As the cost of radiotracer-guided thoracoscopic resection increases, thoracotomy is preferred (light area).

 

   Comment
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
Discussion
 Acknowledgments
 References
 
Radiotracer-guided thoracoscopic resection is a cost effective strategy for evaluating highly suspicious 5- to 10-mm solitary pulmonary nodules. It has a high success rate with low morbidity and mortality [13] and is a useful tool for thoracic surgeons to diagnose and treat early stage lung cancer. When the cost of the RGTR strategy increased by 33%, the thoracotomy strategy became the most cost-effective option. Likewise, when the cost of the thoracotomy strategy decreased by 14%, it became the dominant approach. There were two other variables that had thresholds outside of the plausible range when sensitivity analysis was performed (Table 3). When the diagnostic success rate of thoracoscopy fell below 44%, the thoracotomy strategy became more cost-effective. The published success rate for this technique is 95% to 96% [13, 25]. In addition, when the probability of obtaining a lung cancer diagnosis was greater than 65%, thoracotomy was the preferred strategy. The range obtained from the literature for cancer in small solitary pulmonary nodules is 21% to 35% [11–13, 18–20, 22].

Decision analysis is an analytic tool useful for comparing treatment alternatives, and we believe it is the best method for determining whether RGTR is a cost-effective strategy. It allowed us to model the increased cost of the localization procedure versus the money saved by reducing the number of patients requiring thoracotomy who had a benign diagnosis. In addition, we were able to model effectiveness based on 5-year mortality estimates that were disease- and stage-specific. By using the current estimates from The Society of Thoracic Surgery Database, the current mortality differences during the study period between thoracotomy and thoracoscopy were also modeled.

Our study does have limitations. All decision analysis models are dependent on the quality of the model and the data input into that model. Our model is fairly simple and represents the clinical decision making from a thoracic surgeon's perspective that occurs with small highly suspicious nodules that cannot be easily accessible through a standard video-assisted thoracoscopy procedure. We did not model larger nodules as these can more often be percutaneously biopsied by radiologists or palpated with traditional thoracoscopic approaches. We also modeled costs from an institutional perspective as this was the only data source available for the radiotracer-guided approach. The model compared stage IA versus all other stages, but we believe this is valid because most 5- to 10-mm cancers are early stage. Finally, we did not model thoracoscopic lobectomies as a therapeutic option for patients diagnosed with lung cancer, but this would further bias the model to support our results as these have been shown to be less costly to the institution in previous studies [26]. In addition, the thoracoscopic equipment has already been opened for the RGTR, and minimal additional equipment costs would be incurred.

Because of the difficulty of obtaining a diagnosis for small and deep nodules, multiple localization techniques have been developed: intraoperative imaging (ultrasound or computed tomography), percutaneous injections (dyes, contrast media, radionucleotides, or colored adhesive agents), and percutaneous insertion of hook-wires or coils. Intraoperative imaging techniques require expensive hybrid operating rooms. The use of percutaneous dye injection is limited by diffusion away from the nodule, inability to visualize the dye in deep nodules, and the risk of anaphylaxis with methylene blue [27]. Radiographic contrast media (Lipiodol) can diffuse away from the nodule and enter the pulmonary lymphatics, where, if it gains access to the pulmonary vasculature, it may cause strokes given that these agents are not water-soluble [28]. Percutaneous insertion of hook-wires can cause clinically significant pneumothoraces in patients with marked emphysema [29], massive air embolism [30], and perioperative dislodgement [25, 31]. Given that each of the above techniques has inherent limitations, we chose to explore the use of computed tomography-guided radiotracer injection using a 99mTc microalbumin aggregate solution, followed by intraoperative thoracoscopic localization with a gamma probe. This technique does not require intraoperative fluoroscopy, imaging in the operating room, purchase of expensive new equipment, or a skilled sonographer, and does not dissipate rapidly into the surrounding parenchyma or lymphatics [13]. Gonfiotti and colleagues [25] recently reported a prospective randomized trial comparing radiotracer versus hookwire localization. They found a lower failure rate (4% versus 16%) and complication rate (4% versus 24%) in the radiotracer group.

In summary, RGTR is a cost-effective strategy for evaluating highly suspicious 5- to 10-mm solitary pulmonary nodules. It has a high success rate with low morbidity and mortality [13] and is a useful tool for thoracic surgeons to localize, excise, and treat early stage lung cancer.


   Discussion
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Discussion
Acknowledgments
 References
 
DR ROBERT J. CERFOLIO (Birmingham, AL): Very good paper and very well presented.

My main question is that you're not really sending a message that you want us to go ahead and evaluate all these 5-mm to 10-mm nodules. You changed the slide a little but the key is the highly suspicious one that you went after. So really what we want to compare is what most of us do every day with 5 mm, 6 mm nodules—you just watch them. So how can you tell us who you decided to operate on to get such a high-percent malignancy when we all know that 80% of these are probably benign and we rarely need to take them to the operating room?

DR GROGAN: Thank you for the question.

It's difficult to quantify exactly what each of us sees in the clinic and what we perceive as risk. According to the ACCP guidelines, any patient who has a risk of lung cancer greater than 60% requires excision. The guidelines also indicate that a patient who has a subcentimeter nodule that shows unequivocal growth be evaluated and tissue be obtained. A patient who has a 5-mm nodule or less has a very low risk, and so I don't think anybody would really recommend that, but the current guidelines support evaluating and obtaining tissue for these small high-risk nodules less than 1 cm.

DR ARA A. VAPORCIYAN (Houston, TX): Eric, I liked that presentation a lot.

One thing about the decision-tree model that you chose, one other treatment strategy would be to use the repeat CT (computed tomography) guidelines that were promulgated by the Early Lung Cancer Action Program (ELCAP). When they used those guidelines, their chance of getting a diagnosis of cancer was much, much higher than 33%. Have you worked that guideline or that treatment option into your cost analysis as well?

DR GROGAN: We have not. I think that's sort of the next step to this piece. However, when I go back to some of the original papers, their cutoff is 1 cm, so if nodules grow larger than 1 cm, they always obtain a tissue diagnosis via percutaneous biopsy. The gray zone was that 5-mm to 9-mm nodule where they basically left it up to the clinician's evaluation based on the risk factors. So looking at where this niche is and where I thought that this sort of piece was useful was for that nodule which we talked about, which was the one that had doubled in size, it was high risk, in a patient that none of us felt comfortable watching, but yet we didn't really have the tools and techniques to go after it without potentially giving somebody a big whack.

DR BRYAN F. MEYERS (St. Louis, MO): Eric, with this kind of a model you usually get an end point that is an incremental cost for an incremental benefit, and a lot of times that is described as a cost of dollars per life year gained, and that allows us to compare the expense of a strategy against other similarly measured strategies in other spheres of health care. Often, there is sometimes a quoted threshold of a certain amount of cost per life year gained above which is considered too expensive. What is your denominator of effectiveness? How were you actually measuring it? Was it life year gained? Was there any quality adjustment of life years or anything like that?

DR GROGAN: There was not a breakpoint because the effectiveness was higher. It was the least costly and more effective procedure. So there wasn't an incremental cost-effectiveness because it was always cost-effective for the radiotracer-guided thoracoscopic strategy. So we did not do incremental cost-effectiveness for that. Our effect was based upon 5-year survival based on the cancer stage. So we did not do qualities per life year saved, but that's certainly the next step with this.

DR MEYERS: So, then, in the sensitivity analysis, you looked at how the different parameters or estimates would have to change in order to not make it a dominant therapy. So if it's cheaper and more effective, then that's clearly dominant and your sensitivity analysis was just looking at how much those costs or success rates would have to change in order to alter that.

DR GROGAN: That's correct.

DR MEYERS: Thanks.

DR DAVID A. WALLER (Leicester, UK): Could you comment on the alternative strategy of diagnostic thoracoscopic segmentectomy when you fail to identify the lesion and the implications for cost of a diagnostic thoracoscopic segmentectomy compared to an open thoracotomy and biopsy?

DR GROGAN: In all of our series we were not doing thoracoscopic segmentectomies for these, and we didn't really have that many where we followed up a potential cancer diagnosis with thoracoscopic lobectomy. So I can't speak to that in terms of a model, although I think that if one cannot obtain a tissue diagnosis with a thoracoscopic biopsy, then one has to perform a lobectomy or segmentectomy to get the lesion out.


   Acknowledgments
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Discussion
 Acknowledgments
References
 
This research was supported by the Commonwealth Fund for Cancer Research support to the University of Virginia Cancer Center.


   References
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Discussion
 Acknowledgments
 References
 

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Ann. Thorac. Surg., June 1, 2010; 89(6): 1724 - 1729.
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Eric L. Grogan
Benjamin D. Kozower
David R. Jones
Thomas M. Daniel
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