Annals of Oncology Advance Access originally published online on February 24, 2006
Annals of Oncology 2006 17(5):785-793; doi:10.1093/annonc/mdl023
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© 2006 European Society for Medical Oncology
Computed tomography screening for lung cancer in Hodgkin's lymphoma survivors: decision analysis and cost-effectiveness analysis
1 Department of Radiation Oncology, U.T. M.D. Anderson Cancer Center, Houston, TX; Departments of 2 Radiation Oncology and 3 Medical Oncology, Dana Farber Cancer Institute and Brigham and Women's Hospital, Harvard Medical School; 4 Department of Health Policy and Management, Harvard School of Public Health, Boston, MA, USA
* Correspondence to: P. Das, Department of Radiation Oncology, U.T. M.D. Anderson Cancer Center, 1515 Holcombe Boulevard, Unit 97, Houston, TX 77030, USA. Tel: +1-713-563-2300; Fax: +1-713-563-2366; E-mail: PrajDas{at}mdanderson.org
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Abstract |
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Background: Hodgkin's lymphoma patients have an elevated risk of developing lung cancer and may be targeted for lung cancer screening. We used a decision-analytic model to estimate the potential clinical benefits and cost-effectiveness of computed tomography (CT) screening for lung cancer in Hodgkin's lymphoma survivors.
Materials and methods: We developed a Markov decision-analytic model to compare annual low-dose CT screening versus no screening in a hypothetical cohort of patients diagnosed with stage IA–IIB Hodgkin's lymphoma at age 25, with screening starting 5 years after initial diagnosis. We derived model parameters from published studies and the Surveillance, Epidemiology and End Results (SEER) Program, and assumed that stage-shift produces a survival benefit.
Results: Annual CT screening increased survival by 0.64 years for smokers and 0.16 years for non-smokers. The corresponding benefits in quality-adjusted survival were 0.58 quality-adjusted life-years (QALYs) for smokers and 0.14 QALYs for non-smokers. The incremental cost-effectiveness ratios for annual CT screening compared with no screening were $34 100/QALY for smokers and $125 400/QALY for non-smokers.
Conclusions: Our analysis suggests that if early promising results for lung cancer screening hold, CT screening for lung cancer may increase survival and quality-adjusted survival among Hodgkin's lymphoma survivors, with a benefit and incremental cost-effectiveness ratio for smokers comparable to that of other recommended cancer screening strategies.
Key words: cost-effectiveness, decision analysis, Hodgkin's lymphoma, lung cancer, second malignancies
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introduction |
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Second malignancies represent an important clinical problem in Hodgkin's lymphoma survivors. Although patients treated for early-stage Hodgkin's lymphoma have high cure rates, they face excess mortality from other causes [1
–6]. Among patients with early-stage Hodgkin's lymphoma, excess mortality from other causes starts to exceed the mortality from Hodgkin's lymphoma, 12–15 years after initial diagnosis. Second malignancies represent the leading component of excess mortality from other causes in these patients, and the long-term mortality from second malignancies has been reported to be nearly 10% [1–7]. Hence there exists a great need for devising cost-effective, evidence-based strategies for early detection of second malignancies in these patients.
Lung cancer is one of the most common second malignancies in Hodgkin's lymphoma survivors. The relative risk of developing lung cancer is between 2.9 and 7.0 compared with the general population [7–12]. The risk of developing lung cancer after Hodgkin's lymphoma is greater in those with prior radiation therapy, prior alkylating chemotherapy or a history of smoking [13–17]. Hodgkin's lymphoma survivors who develop lung cancer have a median survival of less than a year [18, 19]. Hodgkin's lymphoma survivors may have a particularly poor survival from lung cancer because of co-morbid conditions or because these patients may not be candidates for further radiation therapy to the thorax. Thus, Hodgkin's lymphoma survivors represent a population that could be targeted for lung cancer screening.
There has been increasing interest in lung cancer screening with annual low-radiation-dose CT scans in patients at high risk for lung cancer. A number of prospective studies have demonstrated that annual CT screening enables detection of lung cancer at earlier stages [20–29]. Although a randomized trial called the National Lung Screening Trial is currently investigating the role of CT screening for lung cancer in current and former smokers, this trial may not answer whether CT screening increases survival among Hodgkin's lymphoma survivors. The benefit of lung cancer screening in Hodgkin's lymphoma survivors may be much higher than that in other populations since Hodgkin's lymphoma survivors develop lung cancer at a younger age and have a markedly elevated risk for developing lung cancer, especially for smokers. At the same time, randomized screening trials on Hodgkin's lymphoma survivors are not feasible since Hodgkin's lymphoma is a relatively rare disease and a very long follow-up period would be required to detect a benefit of screening for second malignancies. Given these constraints, a decision-analytic model based on available evidence can help to decide whether these patients would benefit from screening.
We developed a decision-analytic model to evaluate the potential clinical benefits and cost-effectiveness of annual low-dose CT screening for lung cancer in Hodgkin's lymphoma survivors. We estimated the cost-effectiveness of annual low-dose CT screening separately for smokers and non-smokers and determined what factors are likely to influence the survival benefit and cost-effectiveness of CT screening.
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materials and methods |
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model structure
We constructed a decision-analytic model to compare annual low-radiation-dose CT screening with no screening in a hypothetical cohort of patients diagnosed with stage IA–IIB Hodgkin's lymphoma at age 25, with screening starting 5 years after initial diagnosis and continuing until either death or diagnosis of lung cancer. Markov state-transition models were used to project the lifetime prognosis of the patients [30
]. Each model consisted of a number of health states for Hodgkin's lymphoma survivors, including no lung cancer, non-small-cell lung carcinoma (NSCLC) at localized, regional and distant stages, small-cell lung carcinoma and death. In each 1-year cycle, patients with no lung cancer were at risk of developing lung cancer. Moreover, in each cycle, depending on their health states, patients were at risk of dying from lung cancer, Hodgkin's lymphoma, other conditions associated with Hodgkin's lymphoma and causes not related to Hodgkin's lymphoma. Separate analyses were performed for smokers and non-smokers. The life expectancies in screened and unscreened patients were calculated by running the models in 1-year cycles until the entire cohort died. We assigned health-related quality-of-life weights, or utilities, to each health state and calculated quality-adjusted life expectancy by multiplying the time spent by patients in the different health states with the corresponding utilities [31]. We also assigned costs to different health states or transitions between health states. The incremental cost-effectiveness of each strategy was determined by dividing the incremental cost by the incremental effectiveness, measured in life-years or quality-adjusted life-years. The analysis was performed from a modified societal perspective and included medical costs and incurred (downstream) costs. Costs and benefits were discounted at an annual rate of 3% in the baseline analysis, in accordance with the recommendations of the Panel on Cost-Effectiveness in Health and Medicine [32]. We used the DATA software package (TreeAge Software, Inc., Williamstown, MA) to construct the model and perform the analyses.
key assumptions
We assumed that the histology and stage distribution of lung cancer in unscreened Hodgkin's lymphoma patients was similar to the histology and stage distribution of lung cancer in the general population. This assumption was based on published studies on lung cancer after Hodgkin's lymphoma [16, 18, 19]. In our baseline analysis, we assumed that CT screening did not affect the incidence of lung cancer but changed the stage distribution at diagnosis for NSCLC. Annual CT screening thereby caused a stage shift towards earlier, more localized stages. We assumed that CT screening did not affect the stage distribution for small-cell lung cancer. We also assumed that capital equipment and resources were in place for conducting a program of CT screening for lung cancer, and all patients adhered completely to the annual screening program.
In our model, patients with a positive low-dose screening CT underwent a follow-up standard-dose diagnostic chest CT, as described in the guidelines for the Early Lung Cancer Action Project, a recent study on CT screening [20, 21]. If the diagnostic chest CT showed benign disease, the patient underwent no further testing that year and continued with annual low-dose screening CT scans. If the diagnostic chest CT showed suspicious findings, the patient underwent either a CT-guided biopsy or a thoracoscopic biopsy. If the biopsy pathology was benign, the patient received no additional treatments that year and continued with annual low-dose screening CT scans. If the biopsy pathology was positive, the patient was diagnosed with and treated for lung cancer.
baseline estimates
Table 1 shows the baseline estimates of each of the model variables, the ranges over which they were tested in sensitivity analyses and their sources.
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The incidence of lung cancer in the general population was obtained from the SEER public-use database [33
]. All analyses of the SEER database were performed with SEER Stat 4.2 software, using data collected from nine SEER registries for the period 1973–1999. We included only cases with invasive cancers that were actively followed and excluded cases identified by death certificate or autopsy data. The lung cancer incidence in the general population was then adjusted to reflect the incidence among Hodgkin's lymphoma survivors on the basis of three large retrospective studies [8–10].
The relative risk of lung cancer in smokers and non-smokers was obtained from three case-control studies on Hodgkin's lymphoma survivors [14–16]. These studies have used different criteria for smoking history. One study evaluated the risk of lung cancer in those who had any history of smoking, a second study determined the risk in those who smoked at least 10 pack-years after diagnosis of Hodgkin's lymphoma, and a third study reported the risk in those currently smoking at least one pack per day [14–16]. We assumed that the prevalence of smoking was similar to that in the general population and performed sensitivity analysis to assess the impact of this assumption [34]. We then used the relative risk of lung cancer in smokers and non-smokers and the prevalence of smoking to calculate the incidence of lung cancer among smokers and non-smokers.
The histologic distribution of small-cell lung cancer and NSCLC was obtained from the SEER database [33]. The stage distribution of NSCLC in unscreened patients was also obtained from the SEER database [33]. The stage distribution of NSCLC in screened patients was derived from six published prospective studies on CT screening [20–29].
Mortality from lung cancer was stratified by the stage and histology of lung cancer and was obtained from the SEER database [33]. Lung cancer-specific mortality was estimated as a function of time from diagnosis and declined by 70%–80% from the first year to the fifth year after diagnosis. Mortality from Hodgkin's lymphoma was also obtained from the SEER database and represented both mortality directly due to Hodgkin's lymphoma and excess mortality associated with Hodgkin's lymphoma [33]. Mortality from causes not related to Hodgkin's lymphoma was derived from the 1999 United States life tables [35].
Low-dose screening CT scans may yield false-positive findings that necessitate further diagnostic studies and in some cases, invasive testing. The frequency of such false-positives was estimated from published studies on CT screening for lung cancer [20–28]. We assumed that false-positive tests were associated with increased costs and decreased health-related quality of life, but no changes in mortality. Screening can also be associated with certain biases such as lead-time bias, length-time bias and overdiagnosis bias [36–39]. Previous studies have reported estimates of these biases based on serial chest X-rays, tumor growth rates and necropsy studies [38–43]. We did not include lead-time bias in our baseline model, but incorporated it in sensitivity analyses by subtracting 1 year of survival for patients detected at localized stage by screening [38, 39]. We did not include length-time or overdiagnosis biases in our baseline model, but incorporated these in sensitivity analyses using rates previously reported in the literature [39]. We assumed that patients with ‘overdiagnosed’ lung cancer had the same costs as patients with lung cancer, but the same survival and health-related quality of life as patients without lung cancer.
Health-related quality of life adjustments or utilities for Hodgkin's lymphoma, small cell lung cancer and localized, regional and distant stages of NSCLC were obtained from the medical literature [44, 45]. Patients who had false-positive screening CT scans were assigned short-term losses in utility with values derived from the literature [44].
The direct costs of medical care for lung cancer were obtained from Fireman et al.'s study on the costs of cancer care in a health maintenance organization [46]. These costs were stratified by the stage of lung cancer and the phase of care (initial, continuing or terminal care) [46]. As there are no published reports on long-term costs of care for Hodgkin's lymphoma, we used the long-term costs of care reported by Fireman et al. for breast cancer, prostate cancer, colon cancer and non-Hodgkin's lymphoma, and we performed extensive sensitivity analyses to determine whether the costs of care for Hodgkin's lymphoma influenced our results [46]. The costs for diagnostic tests and office visits were obtained from the 2002 National Physician Fee Schedules Relative Value Scale [47]. In the baseline analysis, the cost for a low-dose screening CT was assumed to be the same as that for a standard-dose diagnostic chest CT. We assumed that patients with a positive screening CT had a follow-up office visit and a follow-up chest CT with their associated costs. We also assumed that if the follow-up CT showed suspicious findings, the patient had another follow-up office visit and either a CT-guided or thoracoscopic biopsy with their associated costs. All costs were converted to 2002 US dollars using the medical care component of the Consumer Price Index to adjust for inflation [48].
sensitivity analysis
We performed sensitivity analyses to evaluate the stability of our results by varying the probabilities, utilities and costs in our model. In most cases, we arbitrarily halved and doubled the baseline rates, and increased and decreased the baseline costs by 30% to provide a broad range to test our assumptions and estimates. As described above, we incorporated adjustments for lead-time, length-time and overdiagnosis bias in some of the sensitivity analyses. Finally, we performed threshold analysis to evaluate how much lead-time, length-time or overdiagnosis bias would be necessary to make the incremental cost-effectiveness ratio exceed $100 000/QALY.
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baseline analysis
Our analysis showed that 24.5% of smokers and 5.9% of non-smokers developed lung cancer. Among screened patients, 17.3% of smokers and 4.1% of non-smokers were detected with localized stage NSCLC. Among unscreened patients, only 4.4% of smokers and 1.1% of non-smokers presented with localized stage NSCLC. Screened patients had an average of 1.5 false-positive screening CTs over their lifetime.
Smokers undergoing annual CT screening had a life-expectancy of 29.60 years while those not undergoing screening had a life-expectancy of 28.96 years (Table 2). Non-smokers undergoing CT screening had a life-expectancy of 32.31 years whereas those not undergoing screening had a life-expectancy of 32.15 years. Thus, the expected benefit with CT screening was 0.64 years or 7.7 months for smokers and 0.16 years or 2.0 months for non-smokers. The expected benefit in quality-adjusted life-expectancy was 0.58 QALYs or 7.0 quality-adjusted months for smokers and 0.14 QALYs or 1.6 quality-adjusted months for non-smokers.
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Annual low-dose CT screening increased the discounted lifetime cost of management of Hodgkin's lymphoma survivors from $74 500 to $82 500 for smokers and from $75 500 to $81 700 for non-smokers (Table 3). The incremental cost-effectiveness ratio for annual CT screening versus no screening was $30 800/life-year or $34 100/QALY for smokers and $97 400/life-year or $125 400/QALY for non-smokers.
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Sensitivity analysis
We evaluated the effect of varying the estimates of probabilities, utilities and costs on our results. Tables 4 and 5 show the model parameters that changed the estimated survival benefit or the incremental cost-effectiveness ratio by at least 20%. Our results were sensitive to the rates of lung cancer in Hodgkin's lymphoma survivors. If the rate of developing lung cancer decreased by half, the survival benefit of CT screening decreased from 0.64 years to 0.35 years for smokers and from 0.16 years to 0.08 years for non-smokers. Moreover, if the rate of developing lung cancer decreased by half, the incremental cost-effectiveness ratio increased from $34 100/QALY to $57 200/QALY for smokers and from $125 400/QALY to $299 400/QALY for non-smokers. Conversely, if the rate of developing lung cancer doubled, the survival benefit increased and the incremental cost-effectiveness ratio for CT screening decreased.
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Our results depended on how many lung cancers CT scans could detect at the localized stage. If the proportion of NSCLC detected at a localized stage by CT screening decreased by half, the survival benefit decreased to 0.17 months for smokers and 0.04 months for non-smokers, whereas the incremental cost-effectiveness ratio increased to $106 600/QALY for smokers and $1 050 000/QALY for non-smokers.
The results were sensitive to the mortality rates from lung cancer, Hodgkin's lymphoma and other causes associated with Hodgkin's lymphoma. As shown in Tables 4 and 5, the survival benefit was higher when mortality from these causes was lower and the survival benefit was lower when mortality from these causes has higher.
The incremental cost-effectiveness ratio for CT screening compared with no screening was also sensitive to the cost of the annual low-dose screening CT. If the cost of each screening CT decreased to $150, the incremental cost-effectiveness ratio decreased to $25 200/QALY for smokers and $79 900/QALY for non-smokers. On the other hand, if the cost of each screening CT increased to $400, the incremental cost-effectiveness ratio increased to $43 600/QALY for smokers and $174 000/QALY for non-smokers.
The incremental cost-effectiveness ratio was insensitive to the costs of care for lung cancer patients, the costs of care for Hodgkin's lymphoma patients and the costs of follow-up diagnostic tests and office visits. Furthermore, the incremental cost-effectiveness ratio and estimated benefits in survival and quality-adjusted survival were insensitive to the utilities of the different health states and the rate of false positive results from the screening CT scans.
When the model was adjusted for lead-time bias, the benefit of CT screening decreased from 0.64 years to 0.47 years for smokers and from 0.16 years to 0.12 years for non-smokers. With adjustment for lead-time bias, the incremental cost-effectiveness ratio increased to $47 000/QALY for smokers and $186 900/QALY for non-smokers. With adjustments for overdiagnosis and length-time bias, the estimated survival did not change but the incremental cost-effectiveness ratio increased to $50 100/QALY for smokers and $142 600/QALY for non-smokers. Finally, when adjustments for lead-time, length-time and overdiagnosis bias were simultaneously incorporated into the model, the incremental cost-effectiveness ratio increased to $68 200/QALY for smokers and $211 600/QALY for non-smokers. Threshold analysis showed that the incremental cost-effectiveness ratio for smokers exceeded $100 000/QALY only for a lead-time of 2.4 years or greater. Threshold analysis also showed that the incremental cost-effectiveness ratio for smokers exceeded $100 000/QALY only if overdiagnoses accounted for 90% of the lung cancers detected in the first year of screening.
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discussion |
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Hodgkin's lymphoma survivors have an elevated risk of lung cancer. Since no direct evidence exists about the benefits of screening for lung cancer in these patients, we developed a decision-analytic model that incorporates all available information about lung cancer incidence in Hodgkin's lymphoma survivors, lung cancer mortality, Hodgkin's lymphoma mortality, benefits of CT screening and economic costs. Under our assumptions, annual CT screening in Hodgkin's lymphoma survivors increases expected survival by 7.7 months for smokers and 2.0 months for non-smokers, and increases expected quality-adjusted survival by 7.0 quality-adjusted months for smokers and 1.6 quality-adjusted months for non-smokers. Furthermore, our analysis shows that annual CT screening has an incremental cost-effectiveness ratio of $34 100/QALY for smokers and $125 400/QALY for non-smokers.
The survival benefits in our analysis compare favorably with that of other recommended cancer screening strategies. For example, breast cancer screening with biennial mammography in 50-year-old women results in a life-expectancy gain of 0.8 months, cervical cancer screening with annual Papanicolaou smears in 20-year-old women results in a gain of 3.2 months, and colorectal cancer screening in 50-year-old men results in a gain of 2.5–2.8 months [49]. The expected benefit of 7.7 months in smokers appears large compared with benefits from other cancer screening programs. This large benefit in life expectancy probably arises from the high risk of lung cancer in these patients and the relatively young age at which lung cancer appears. The incremental cost-effectiveness ratio for annual CT screening in Hodgkin's lymphoma survivors compares favorably to that of other recommended cancer screening strategies. Previous studies have reported incremental cost-effectiveness ratios of $99 000/life-year for annual Papanicolaou testing in 20-year-old women, $132 000/life-year for annual mammography in 55–64 year-old women and $37 000/life-year for annual fecal occult blood testing and sigmoidoscopy every 5 years in 50-year-old men (costs in 1998 dollars) [50, 51]. The estimated survival benefits and cost-effectiveness ratios in this study also appear to be in concordance with that reported for CT screening for lung cancer in other high-risk populations [38, 39, 52, 53].
We constructed separate models for smokers and non-smokers. The survival benefits were four-fold higher and the incremental cost-effectiveness ratios about four-fold lower for smokers compared with non-smokers in our baseline analysis. Sensitivity analyses showed that the cost-effectiveness of CT screening for smokers remains comparable to that for other cancer screening strategies, even with unfavorable assumptions and estimates. In contrast, the cost-effectiveness of CT screening for non-smokers may be higher than that for other accepted screening programs under certain assumptions. Our model assumed that smokers and non-smokers were two distinct, homogeneous groups. In reality, the risk associated with smoking probably forms a continuum and some patients, such as former smokers or light smokers, may have benefits and cost-effectiveness ratios intermediate to that for heavy smokers and non-smokers. Epidemiologic studies in the general population have shown that the risk of lung cancer depends on the duration of smoking, the number of cigarettes smoked per day and the length of abstinence from smoking [54]. Such factors should be carefully considered in deciding whether a Hodgkin's lymphoma survivor should be screened. A recent study on CT screening in the general population has used a history of 10 pack-years of smoking as its eligibility criteria and this may serve as a potential threshold for deciding which Hodgkin's lymphoma survivors should be screened [20].
Our model has a number of limitations. We derived the long-term risk of lung cancer from three large retrospective studies on Hodgkin's lymphoma patients treated between 1963 and 1997 [8–10]. Many of these patients, especially from the earlier years, were treated with extended-field radiation therapy or alkylating chemotherapy such as the mechlorethamine, vincristine, procarbazine and prednisone (MOPP) regimen. Alkylating chemotherapy and radiation therapy have been shown to be associated with higher risks of lung cancer in Hodgkin's lymphoma survivors [12–16]. Hodgkin's lymphoma patients treated in the current era with combined modality therapy, involved-field radiation therapy and non-alkylating chemotherapy regimens may have smaller long-term risks of lung cancer, and the estimates in this study are not necessarily applicable for those patients. However, many Hodgkin's lymphoma survivors exist who were treated in the past with alkylating chemotherapy or extended-field radiation therapy, and these survivors are in need of recommendations and guidelines for long-term follow-up care. The results of this study will be relevant in formulating appropriate follow-up for these long-term Hodgkin's lymphoma survivors.
We derived the stage distribution of NSCLC in screened patients from six prospective cohort studies [20–29]. However, such non-randomized, uncontrolled studies with short follow-up may have limited validity and the actual stage-shift from CT screening may be smaller. Furthermore, radiation-induced changes in the lung may make detection of nodules more difficult for Hodgkin's lymphoma patients and the stage-shift for these patients may be smaller than the stage-shift for other individuals. Our analysis also assumed that all patients adhered completely to the annual screening program. This assumption may be optimisitic, even for a group of highly motivated patients. If patients do not adhere completely to annual screening, the stage-shift may be smaller. Our sensitivity analysis indicates that even with a much smaller stage-shift, the cost-effectiveness of CT screening remains favorable for smokers though not for non-smokers.
Our analysis assumed that CT screening results in a survival benefit because of a stage shift in NSCLC. Many authors have questioned whether CT screening for lung cancer will decrease mortality [36, 37, 55, 56]. Randomized controlled studies have shown that screening with chest X-rays produces no differences in mortality compared with unscreened patients [57–59]. No evidence currently exists that CT screening decreases mortality. A randomized trial called the National Lung Screening Trial was launched recently in the US to compare screening CT and screening chest X-rays in current or former smokers [60]. However, this trial will not necessarily be generalizable to Hodgkin's lymphoma survivors. Since a randomized screening trial is not feasible in Hodgkin's lymphoma survivors, we amalgamated all the available evidence and constructed a decision-analytic model that estimates the potential benefit of CT screening in this population.
Since patients treated for early stage Hodgkin's lymphoma have very high cure rates, efforts to improve survival need to focus on reducing treatment-related mortality such as second malignancies and cardiovascular diseases. We have used a decision-analytic model to evaluate a potential intervention for early detection of second malignancies in this population. Under the assumptions and literature-based estimates in our model, CT screening for lung cancer results in survival benefits of 7.7 months for smokers and 2.0 months for non-smokers. Hence, if early promising results for lung cancer screening hold, CT screening for lung cancer may increase survival and quality-adjusted survival among long-term survivors of Hodgkin's lymphoma. Furthermore, CT screening appears to have a favorable cost-effectiveness ratio compared with other widely accepted screening tests, especially for smokers. The results from our decision-analytic model imply that annual low-dose CT screening for lung cancer should be considered in long-term survivors of Hodgkin's lymphoma that have a significant smoking history (such as 10 pack-years). However, these results may not necessarily be applicable to Hodgkin's lymphoma patients treated in the current era.
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Acknowledgements |
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This work was supported by an Agency for Healthcare Research and Quality National Research Service Award for 2002–2003, awarded to Prajnan Das.
Presented in part at the American Society of Clinical Oncology Annual Meeting, Chicago, Illinois, May 2003 and at the American Society for Therapeutic Radiology and Oncology Annual Meeting, Salt Lake City, Utah, October 2003.
Received for publication December 6, 2005. Revision received January 13, 2006. Accepted for publication January 16, 2006.
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