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Original Research: NEOPLASTIC DISEASE |

Cost and Outcomes of Patients With Solitary Pulmonary Nodules Managed With PET Scans FREE TO VIEW

Paul G. Barnett, PhD; Lakshmi Ananth, MS; Michael K. Gould, MD, MS; for the Veterans Affairs Positron Emission Tomography Imaging in the Management of Patients with Solitary Pulmonary Nodules (VA SNAP) Cooperative Study Group
Author and Funding Information

From the Health Economics Resource Center (Dr Barnett and Ms Ananth), VA Palo Alto Health Care System (Dr Gould), Palo Alto; and the Stanford School of Medicine (Drs Barnett and Gould), Stanford, CA.

Correspondence to: Paul G. Barnett, PhD, Health Economics Resource Center, 795 Willow Rd (152), Menlo Park, CA 94025; e-mail: paul.barnett@va.gov


For editorial comments see page 4

Funding/Support: This study was supported by the US Department of Veterans Affairs Cooperative Studies Program, Office of Research and Development (VA Cooperative Study 027).

Reproduction of this article is prohibited without written permission from the American College of Chest Physicians (www.chestjournal.org/site/misc/reprints.xhtml).


© 2010 American College of Chest Physicians


Chest. 2010;137(1):53-59. doi:10.1378/chest.08-0529
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Background:  No prior study to our knowledge has observed the cost of managing solitary pulmonary nodules of patient groups defined by PET scan results.

Methods:  We combined study and administrative data over 2 years of follow-up.

Results:  Of 375 individuals with a definitive diagnosis, 54.4% had a malignant nodule and 62.1% had positive PET scan results. Mortality risk was 5.0 times higher (CI, 3.1-8.2) and cost was greater ($50,233 vs $22,461, P<.0001) among patients with malignant nodule. Mortality risk was 4.1 times higher (CI, 2.4-7.0) and cost was greater ($47,823 vs $20,744, P<.0001) among patients with a positive PET scan result. Among patients with a malignant nodule, 4.9% had a false-negative PET scan, but cost and survival were not different from true positives. Among patients with a benign nodule, 22.8% had a false-positive PET scan. These patients had greater cost ($33,783 vs $19,115, P<.01), more surgeries and biopsies, and 3.8 times the mortality risk (CI, 1.6-9.2) of true negatives. Just over one-half (54.5%) of individuals with positive PET scans received surgery. Most individuals with negative PET scans (85.2%) were managed by watchful waiting. They incurred fewer costs than patients with negative PET scans who were managed more aggressively ($19,378 vs $28,611, P<.01).

Conclusions:  Management of solitary pulmonary nodules is expensive, especially if the nodule is malignant or if the PET scan result is false positive. Among patients with malignant nodules, 2-year survival is poor. Compared with true-positive PET scan results, false-negative results are not associated with lower costs or better outcomes.

Lung cancer is the leading cause of cancer death in the United States. Most lung cancer is diagnosed at an advanced stage, when 5-year survival is less than 15%.1

Lung cancer that presents as a solitary pulmonary nodule (SPN) is potentially curable, with 5-year survival of 65% to 80%.1-3 An SPN is a single radiographic opacity up to 3 cm in diameter surrounded completely by aerated lung, without associated atelectasis, post obstructive pneumonia, mediastinal widening, or pleural effusion. The increased use and improved sensitivity of CT scanning has dramatically increased the number of SPNs seen by clinicians.4 Older, community-based studies reported rates of one SPN for every 500 chest radiographs.5 Recent studies of healthy volunteers found an SPN on at least 7% of initial radiographs and in 23% to 51% of initial CT scans.4,6

Depending on the population, between 15% and 75% of classic SPNs (those measuring between 7 mm and 30 mm in diameter) are malignant; the prevalence of malignancy is much lower among those with smaller nodules.6,7 The preferred treatment of patients with malignant nodules is prompt surgical resection.8 Although CT scanning is relatively non specific, a PET scan assesses malignancy based on uptake of the glucose analog 18F-fluorodeoxy glucose.

Although a PET scan costs $2,000 per scan,9 it might reduce the cost of unnecessary surgery or biopsy by identifying patients who can be safely followed by watchful waiting. The cost-effectiveness of this trade-off has been evaluated with clinical decision models.10-15 Models could be improved with more accurate information on cost.

The economic literature is largely limited to studies of cost after diagnosis.16-21 Diagnosis and treatment of lung cancer account for 20% of cancer care costs, and 2% of all US health-care costs.22 Initial treatment of lung cancer is more costly than all but colorectal cancer, but lifetime cost of treating lung cancer is less than other cancers because of limited survival.19 No prior study to our knowledge has directly observed the cost of SPN management or of patient groups defined by PET scan results.

Results from the largest study of patients with SPN evaluated with PET scan were recently published.23 We combined information from that prospective study with administrative data with the goal of determining the treatment, cost, and outcomes of patients with SPN. We studied cost incurred by study participants grouped by PET scan result and SPN diagnosis, but we did not attempt to attribute which portion of costs were due to lung cancer, SPN, or other disease.

Our aim was to test how treatment was affected by PET scan result and to determine if there were clinical consequences of false PET scan findings. We examined whether patients with a malignant SPN were more likely to survive if the PET scan result was negative, as suggested by previous studies.24,25 We characterized care and outcomes after a positive PET scan. We studied whether a false-positive PET scan leads to more intensive treatment or different outcomes. We examined whether watchful waiting after a negative PET scan saves costs or delays surgical treatment.

Patients in the Veterans Affairs (VA) health system with an SPN on chest radiograph or CT scan were enrolled in the clinical study, Positron Emission Tomography Imaging in the Management of Patients with Solitary Pulmonary Nodules (SNAP), evaluated with CT and PET scans, and followed until there was a definitive diagnosis by pathology (from surgery or biopsy) or by confirmation that the nodule did not increase in size over 2 years of follow-up.26 Study participants provided informed consent in a protocol approved by human subjects’ committee. Waiver from additional consent was obtained to extract data on participants’ cost and use.

PET scans were regarded as positive if the site-reader interpretation was probably malignant, definitely malignant, or indeterminate. PET scans were regarded as positive outside the target nodule if the reader indicated an adrenal mass, hilar or mediastinal adenopathy, or an extrapulmonary abnormality.

Biopsies were recorded on case-report forms. Surgeries were identified by procedures coded at hospital discharge. Chemotherapy and radiation therapy were identified by procedure codes or type of ambulatory clinic. We defined watchful waiting as the management given to individuals with negative PET scan results who did not have a biopsy within 60 days of their PET scan, or surgery, chemotherapy, or radiation therapy within 90 days of their scan.

Cost of Care

We used hospital and outpatient costs from the VA Health Economics Resource Center27,28 and pharmacy costs from the VA Decision Support System.29 Exclusion of capital financing may understate cost by 5%.30 We did not adjust for inflation; care was provided during 1999 to 2003.

Hospital costs were considered related to cancer or management of SPN if the primary diagnosis was cancer or a benign disease associated with SPN. Outpatient visits were classified as related to lung cancer or SPN if they involved these diagnoses, a relevant clinic (pulmonary, chemotherapy, radiation therapy, or oncology clinic), or procedure code (chest radiograph, chest or thoracic CT scan, PET scan, other nuclear imaging, lung biopsy, chemotherapy, or radiation therapy). We divided remaining care between acute medical-surgical hospitalization and all other (which included rehabilitation, psychiatric, and nursing home stays, other outpatient visits, and outpatient pharmacy). We determined cost per life-month by dividing cost by the number of months the subject was alive. Deaths were identified in the VA Beneficiary Identification and Records Locator Subsystem Death File, which is nearly as complete as the National Death Index.31

Statistical Methods

Because cost data are often skewed, we used the Wilcoxon rank-sum test, or for more than two groups, the Kruskal-Wallis test, followed by Wilcoxon post hoc comparisons. Survival differences were tested with Cox regressions. Group differences in proportions were tested by Χ2 test, Fisher exact test, or logistic regression.

The SNAP study enrolled 532 patients with a newly diagnosed SPN, evaluated 486 with both CT and PET scan, and assigned a definitive diagnosis to 344.23 We included 32 patients not in the earlier report because their diagnosis was established by biopsy from a site other than the study SPN,23 and excluded one individual not found in VA data. Our cohort of 375 individuals was a mean of 65.9 (±10.7) years old; 97.9% were men. Almost all (94.4%) were current or former smokers, with an average of 55 pack-years of smoking history; 47.2% were current smokers. Many participants had a history of previous cancer treatment; 13% had been treated for lung cancer, and 17% had been treated for extrathoracic cancer.

Effect of Malignant Nodules on Cost and Outcomes

We compared 204 of 375 participants (54.4%) with a malignant SPN to those whose nodule was benign (Table 1). Individuals with a malignant SPN had 5.0 times the mortality risk (CI, 3.1-8.2, P<.001). Their care cost was $50,233 compared with $22,461 for those with a benign nodule (P<.001). Monthly costs were more than three times greater in the malignant group ($ 3,223 vs $ 1,070, P<.001).

Table Graphic Jump Location
Table 1 —Study Participants by Cancer Status

SPN = solitary pulmonary nodule.

a 

P<.05.

b 

P<.0001.

c 

P<.001.

Costs were greater because individuals with malignant nodules were much more likely to undergo lung surgery, chemotherapy, and radiation therapy. Even so, 22.1% of those with a malignant nodule did not undergo any of these procedures in the VA health-care system. Some of these patients may have decided not to obtain further care, their health may have deteriorated so that curative treatment was no longer feasible, or they may have received additional treatment from another provider. Of the 204 participants with a malignant nodule, nine (4.4%) were small cell lung cancer and six (2.9%) were metastatic from a different primary site.

Association Between PET Scan Result, Cost, and Outcomes

The PET scan was positive in 62.1% of patients. Nodules were malignant in 83.3% who had a positive PET scan and in 7.0% with a negative PET scan (P<.0001). Patients with a positive PET scan incurred $ 47,823 in cost, compared with $ 20,744 incurred by patients who had a negative PET scan (P<.0001). After controlling for age, those with a positive PET scan had 4.1 times the risk of death (CI, 2.4-7.0).

Individuals With Malignant Nodules by PET Scan Result

Among the 204 participants with a malignant nodule, 194 (95.1%) had a positive PET scan result and 10 were false negative (Table 2). Among those with a malignant SPN, positive PET scan was associated with a larger nodule, more prompt surgery, and greater cost (not statistically significant). PET scan result was not associated with any significant difference in survival, but we had limited power to detect a difference.

Table Graphic Jump Location
Table 2 —Study Participants by Cancer Status and Test Result

See Table 1 for expansion of abbreviation.

a 

False positive significantly different from true negative, P<.01.

b 

False positive significantly different from true negative, P<.05.

Among the 10 patients with false-negative findings, two received surgery within 90 days and three more received surgery by the end of study. All five who received surgery survived the 2-year follow-up period, whereas three of the five who did not receive surgery survived this long.

Individuals Without Cancer by PET Scan Result

Of the 171 participants with a benign nodule, PET scan was negative in 132 and false positive in 39 (Table 2). Cost was greater in the false-positive group ($ 33,783 compared with $ 19,115, P<.001). Patients with false-positive scans were also more likely to have surgery, biopsy, and chemotherapy or radiation therapy. Benign SPNs that were PET scan positive were significantly larger than those that were PET scan negative (P<.01).

Among patients with benign SPN, those with false-positive PET scan had 3.8 times the risk of death (CI, 1.6-9.2, P<.01). We considered if the higher mortality rate was a consequence of more aggressive treatment. Of the six individuals with a false-positive PET scan who died, four had a biopsy of their nodule, and none had surgery. None of the individuals with biopsy died within 30 days of the procedure. Among these six was an individual who received chemotherapy or radiation therapy for a different cancer.

An alternative explanation for the less favorable prognosis after false-positive PET scan is an active infectious or inflammatory process. Among 171 patients with a benign SPN, six had a nodule that was confirmed by biopsy to be due to coccidioidomycosis, histoplasmosis, hamartoma, or tuberculosis. An additional nine were assigned one of these diagnoses by administrative data. Among patients with a benign nodule, 15.4% who were PET scan positive were later diagnosed with an infectious or inflammatory condition, compared with 6.4% among patients who were PET scan negative (not significantly different).

Individuals with a benign SPN of infectious or inflammatory origin had 2.0 times the mortality hazard of those with a benign nodule of a different or unknown cause, but this trend was not statistically significant (CI, 0.6-6.8). Surgical treatment was received by 46.7% of those with an infectious or inflammatory process, compared with 8.3% of other individuals with a benign nodule (P<.001). Those with infectious or inflammatory diagnosis incurred significantly higher costs ($ 26,934 compared with $ 22,031, P<.05).

There were seven individuals whose index SPN was benign who received chemotherapy or radiation therapy. Administrative data indicated that two of them were treated for prostate cancer, one for multiple myeloma, and one for osteoarthritis. The remaining three received treatment of lung cancer that began 57, 147, and 173 days after study enrollment, presumably from a different pulmonary lesion.

Treatment Provided After Positive PET Scan

We evaluated the treatment, cost, and outcomes of the 233 patients with a positive PET scan. We classified them into mutually exclusive groups by their primary treatment. There were 99 who received surgery within 90 days of their PET scan. Of the remainder, 21 received chemotherapy or radiation therapy within 90 days of their PET scan. Among those who did not receive either type of initial care were 28 patients who received later surgery, 23 patients who did not receive surgery but received chemotherapy or radiation therapy, and 62 individuals with no record of any of these treatments. These groups are compared in Table 3. We made five comparisons. We compared initial surgery to initial chemotherapy, to later surgery, and to no treatment. We compared initial chemotherapy to later chemotherapy and to no treatment.

Table Graphic Jump Location
Table 3 —Treatment, Cost, and Outcomes of Patients With Positive PET Scan With SPN

See Table 1 for expansion of abbreviation.

a 

Initial surgery vs initial chemotherapy, P<.05.

b 

Initial surgery vs no cancer treatment, P<.05.

c 

Initial surgery vs initial chemotherapy, P<.01.

d 

Initial surgery vs later surgery, P<.05.

e 

Initial surgery vs no cancer treatment, P<.01.

f 

Initial chemotherapy vs no cancer treatment, P<.05.

g 

Initial chemotherapy vs no cancer treatment, P<.01.

Patients who received initial surgery incurred significantly greater cost and greater monthly cost than the no-treatment group. Compared with the no-treatment group, the initial surgery group was more likely to have a malignant nodule (92.9% vs 61.3%, P<.001) but less likely to have a PET scan that was positive in an area outside the target nodule (32.3% vs 51.6%, P<.05).

We examined the effect of treatment strategy on survival, while controlling for the extranodular PET scan result. A positive PET scan for extranodular cancer was associated with 2.38 times the mortality risk (CI, 1.56-3.63). The initial surgery group had 0.41 times the mortality risk (CI, 0.24-0.68) of the no-treatment group.

The surgery group had a lower mortality hazard than those who received chemotherapy or radiation therapy as their initial treatment. There was no significant difference in costs or survival between surgically treated patients who did and did not receive surgery within 90 days.

Watchful Waiting After Negative PET Scan

Watchful waiting was used to manage 121 of 142 (85.2%) individuals with negative PET scan results. We compared these patients to others with negative PET scan results. CT scan results were either indeterminate, probably, or definitely malignant in 50.5% of watchful waiting patients, compared with 90.5% of the patients with negative PET scans not managed by watchful waiting (P<.001).

Those managed with watchful waiting incurred less cost than other patients who were PET scan negative ($ 19,378 vs $ 28,611, P<.01) and lower monthly cost ($ 829 vs $ 1,266, P<.01). Costs were less because the watchful waiting group had significantly fewer biopsies (0.8% vs 47.6%), surgeries (4.1% vs 42.9%), and less chemotherapy or radiation therapy (2.5% vs 14.3%) than other patients with negative PET scan results.

Watchful waiting saved costs and was associated with less timely surgery. Among those with a malignant nodule, the average time between PET scan and surgery was 14.5 months in the watchful waiting group, significantly longer (P<.001) than the 3.4 months to surgery in patients who were PET scan positive with cancer, and 0.5 months in patients who were PET scan negative with cancer who were managed more aggressively.

We considered whether delay was so great that it precluded surgery. Among patients who had a malignant nodule, surgery was performed in 75% (3/4) of patients managed by watchful waiting, in 33% (2/6) of those with negative PET scan not managed by watchful waiting, and in 60% (116/194) of those with positive PET scan results. These proportions were not significantly different. There were no significant differences in survival between these groups.

Malignant SPN was associated with high costs and poor outcomes, even though it is a relatively indolent presentation of lung cancer. Patients with a malignant SPN had five times the risk of death of patients with a benign nodule; 32.3% died within 2 years.

Care from lung cancer diagnosis until death, provided over a median of 1.7 years, cost the US Medicare program an average of $ 29,184. Mean cost in the US commercially insured population has been reported as $ 42,99021 and $ 47,941.20 Most cost is incurred in the initial diagnosis and treatment19,32 and in the hospital setting.17,19,20

In this study, care of patients with malignant SPN cost $ 50,233. This differs from these earlier studies in Medicare and commercial insurance populations because of inflation (this study is 10 years more current), differences in time frame (we studied patients two years after initial evaluation, not from diagnosis until death), different cancer (we studied malignant SPN, as opposed to more heterogeneous lung cancers), and different scope of care. Our estimate reflects the comprehensive benefits of VA, and includes pharmacy, mental health services, and nursing home care.

Previous studies found that patients with malignant nodules lived longer if the PET scan result was negative.24,25 We identified a nonsignificant trend showing worse survival after false-negative PET scan. Statistical power was limited by the small number of false-negative scans.

We found patients with a benign SPN incurred $ 22,461 cost over 2 years; we found no comparable estimate in the literature. Among individuals with a benign nodule, those with a positive PET scan incurred more cost, were more likely to have surgery and other procedures, and had a higher risk of death. This was not explained by periprocedural mortality or by a higher incidence of infectious or inflammatory nodules. However, our method of detecting benign nodules of this cause may have been imperfect.

Most patients with positive PET scan results received surgery (127 of 233, or 54.5%). Surgery was performed an average of 3.6 months after the PET scan, and 84.2% of these patients survived at least 2 years. Patients who were PET scan positive who did not receive surgery had 2.9 times the mortality hazard (CI, 1.9-4.4). Some of these patients may not have been healthy enough to undergo surgical resection, highlighting the importance of comorbidities in this population. Others may have received care outside of the VA health care system; we did not have information on non-VA health services received by the study cohort.

Patients who were PET scan negative incurred $ 9,233 less cost if they were managed by watchful waiting. Costs were lower with watchful waiting not only because of avoided surgery, but also because this group was less likely to have cancer.

Our previous decision analysis found that a strategy of needle biopsy was slightly more expensive and marginally more effective than watchful waiting in surgical candidates with a non-hypermetabolic nodule.10 Biopsy reduced the delay in resection of malignant nodules that occurs with watchful waiting. In the current study, we also found patients with non-hypermetabolic nodules incurred significantly greater costs when they were not followed by watchful waiting. We did not find a difference in survival, but few patients with non-hypermetabolic nodules were managed without watchful waiting, and selection bias undoubtedly was involved. A much larger percentage of these more aggressively managed patients underwent surgical resection (43%), suggesting that clinical characteristics or CT scan findings raised the suspicion of malignancy despite the lack of 18F-fluorodeoxyglucose uptake.

Our study has limitations. The observational design limits our ability to make inferences about the effect of management strategies. For example, because patients were not randomly assigned to watchful waiting, clinical factors, including clinician assessment of risk, determined who received more aggressive care. We did not control for these factors. The protocol mandated management that started with a CT and PET scan. We did not observe the effect of management strategies that did not use these tests at the outset. Other limitations include the lack of a definitive diagnosis for 111 study participant, and enrollment of very few women.

At many centers, integrated PET/CT scan is replacing the dedicated PET scan technology used in this study. Although there is no evidence that integrated PET/CT scan is more accurate than dedicated PET scan for characterizing lung nodules, PET/CT scan may provide better information about stage in patients with malignant nodules.

Patients who present with SPN are expensive to manage. Those who have a malignant nodule are especially expensive, and their outcomes are quite poor, especially if they are not treated surgically. Watchful waiting appears to be a cost-saving strategy. Patients managed by watchful waiting incurred fewer costs than other patients who had negative PET scan results. Although no detrimental effects from watchful waiting could be detected, the study had limited ability to detect them. Patients with a benign nodule who had a false-positive PET scan result used more resources and had worse outcomes, although the reason for this remains unclear.

Our findings are generalizable to the population of US veterans and to similar populations of older male smokers with a relatively high prevalence of malignant nodules. The overall findings cannot be generalized to groups with a lower prevalence of malignancy, such as asymptomatic persons with small (<1 cm) nodules detected by CT screening, but findings for the subgroup of patients with malignant nodules are likely generalizable to similar patients outside of the VA. However, because of the low prevalence of granulomatous disease in our study, findings for patients with benign nodules are probably not generalizable to settings in which the prevalence of TB or endemic mycoses is high.

Prior studies have determined health-care cost only after the diagnosis of lung cancer. This study identified the cost incurred after nodule detection. This should help health-care planners to anticipate some of the economic consequences of increasing use of CT scan.

It has been previously reported that patients with malignant nodules were more likely to survive if the PET scan was negative. We observed a trend toward better survival in the 10 participants with false-negative PET scan results; this finding was not statistically significant.

Author contributions:Dr Barnett: contributed to conceiving of the analysis, directing data analysis, selecting statistical tests, and writing much of the paper.

Ms Ananth: contributed to conducting data analyses and statistical tests.

Dr Gould: contributed to conceptualization of the analysis, helping define and refine data analyses, and helping write and revise the manuscript.

Financial/nonfinancial disclosures: The authors have reported to CHEST that no potential conflicts of interest exist with any companies/organizations whose products or services may be discussed in this article.

Other contributions: We thank the site investigators, study staff, and patients participating in the Positron Emission Tomography Imaging in the Management of Patients with Solitary Pulmonary Nodules study (VA Cooperative Study 27) for their contributions.

Role of sponsors: The conclusions are those of the authors and do not represent the official views of the US Department of Veterans Affairs.

SNAP

Positron Emission Tomography Imaging in the Management of Patients with Solitary Pulmonary Nodules study (VA Cooperative Study 27)

SPN

solitary pulmonary nodules

VA

US Department of Veterans Affairs

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Figures

Tables

Table Graphic Jump Location
Table 1 —Study Participants by Cancer Status

SPN = solitary pulmonary nodule.

a 

P<.05.

b 

P<.0001.

c 

P<.001.

Table Graphic Jump Location
Table 2 —Study Participants by Cancer Status and Test Result

See Table 1 for expansion of abbreviation.

a 

False positive significantly different from true negative, P<.01.

b 

False positive significantly different from true negative, P<.05.

Table Graphic Jump Location
Table 3 —Treatment, Cost, and Outcomes of Patients With Positive PET Scan With SPN

See Table 1 for expansion of abbreviation.

a 

Initial surgery vs initial chemotherapy, P<.05.

b 

Initial surgery vs no cancer treatment, P<.05.

c 

Initial surgery vs initial chemotherapy, P<.01.

d 

Initial surgery vs later surgery, P<.05.

e 

Initial surgery vs no cancer treatment, P<.01.

f 

Initial chemotherapy vs no cancer treatment, P<.05.

g 

Initial chemotherapy vs no cancer treatment, P<.01.

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