© 2004 by Oxford University Press
2004 © Oxford University Press
Article |
Outcomes Research in Lung Cancer
Correspondence to: Craig C. Earle, M.D., M.Sc., F.R.C.P.C., Center for Outcomes and Policy Research, Dana-Farber Cancer Institute, 44 Binney St., 454-STE 21-24, Boston, MA 02115 (e-mail: craig_earle{at}dfci.harvard.edu).
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ABSTRACT |
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 TopNotes Abstract IntroductionMethodsResultsDiscussionReferences |
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Background: Lung cancer is the leading cause of cancer death in the United States. Most therapeutic interventions for this disease achieve modest benefits, but at the expense of nontrivial toxicity and cost, making it an important area for outcomes analysis. Objective: The goal of the study was to audit the literature of outcomes pertaining to lung cancer. Data sources: The English language outcomes literature published during the period from 1990 through 2000 was systematically reviewed and analyzed. Study selection: Papers had to contain original research in one of the following areas: quality of life, health economics, communication, decision making, quality of care, or patient satisfaction. Data extraction: The literature was reviewed and analyzed by the author. Data synthesis: The lung cancer outcomes literature is growing rapidly. Of the 199 studies examined, 106 (53%) dealt primarily with quality-of-life measurement, 69 (35%) examined costs, 11 (6%) dealt with communication and decision making, 11 (6%) assessed the quality of care, and two (1%) evaluated patient satisfaction. Most studies focused on the palliative phase of care. Women, the elderly, and minorities were generally well represented in these studies. The European Organization for Research and Treatment of Cancer QLQ-C30 with its LC13 module is emerging as the most commonly employed quality-of-life instrument in lung cancer studies. Economic studies vary widely in their quality. The literature is relatively sparse with respect to quality of care, communication, and decision making, however. Conclusions: A substantial body of outcomes research has been published since 1990. Further work is needed in the area of methods development, in the assessment of the impact of new technologies, and in the monitoring of the quality of lung cancer care in vulnerable populations.
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INTRODUCTION |
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Lung cancer is the leading cause of cancer death in the United States (1). Small-cell lung cancer (SCLC) accounts for approximately 20% of cases, and the balance of cases are referred to as non-small-cell lung cancer (NSCLC), composed mostly of squamous, adenocarcinoma, and large-cell histologies. Most patients present with incurable disease at the time of diagnosis and, because of early hematogenous spread, even those presenting with "early"-stage disease will often eventually develop incurable metastases (2). The 5-year survival rate for all lung cancer patients is only 15% and has not improved greatly during the past 30 years despite much effort in prevention and therapeutics (3).
Surgery is the only treatment modality that can consistently cure a small number of patients with early NSCLC, although radiation therapy can be curative in some limited circumstances. Chemotherapy may contribute in an adjuvant or neoadjuvant role, but it is used mostly as a palliative therapy for advanced disease. SCLC, on the other hand, is more chemosensitive and can be cured in a minority of patients with chemotherapy and radiation therapy. Nevertheless, most patients relapse and die within 1 year of diagnosis (2).
Treatments for all stages and histologies of lung cancer are difficult and expensive and come with nontrivial toxicity. Physicians have traditionally evaluated interventions by looking at their effects on tumor shrinkage, time to disease progression, and survival. However, the unsatisfactory results of most lung cancer therapies have led to increasing interest in other end points that affect decision making by patients, payers, and regulators.
In this study, I focused on the following broad categories: 1) quality of life, 2) health economics, 3) quality of care, and 4) communication and decision making, as they pertain to lung cancer. This study examines the use of these end points in methodological, descriptive, and intervention studies, as well as economic and decision analyses in order to understand the impact of lung cancer on patients, families, providers, and payers.
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METHODS |
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Literature Search
A computerized literature search was done centrally at the National Library of Medicine. It was designed to look for Medical Subject Headings (MeSH) relevant to outcomes research in lung cancer, restricted to English-language articles with on-line abstracts using the following strategy: (quality of life [mh] OR survival analysis [majr] OR health status [mh:noexp] OR health status indicators [mh] OR activities of daily living [mh] OR decision support techniques [majr:noexp] OR decision theory [majr] OR decision making [majr:noexp] OR choice behavior [majr] OR medical futility [majr] OR economics [majr:noexp] OR "costs and cost analysis" [majr] OR cost-benefit analysis [majr] OR economic value of life [majr] OR economics, hospital [majr] OR economics, medical [majr] OR economics, nursing [majr] OR economics, pharmaceutical [majr] OR health services research [mh:noexp] OR delivery of health care [majr:noexp] OR attitude to death [majr] OR attitude to health [majr] OR "health services needs and demand" [majr] OR needs assessment [majr] OR professional-patient relations [majr] OR patient satisfaction [majr] OR physician-patient relations [majr] OR quality of health care [majr:noexp] OR medical audit [majr] OR nursing audit [majr] OR "outcome and process assessment (health care)" [majr] OR peer review, health care [majr] OR professional review organizations [majr] OR program evaluation [majr] OR quality assurance, health care [majr:noexp] OR guidelines [majr] OR total quality management [majr] OR quality indicators, health care [majr]) AND lung neoplasms [majr] AND english [la] AND journal article [pt] AND 1990: 2000[pdat] AND has abstract.
Personal reprints and reference lists were also reviewed.
Data Abstraction
The study was carried out in two steps. First, for a report to the Outcomes Branch of the National Cancer Institute, National Institutes of Health, Department of Health and Human Services, Bethesda, MD, the literature was searched in August 1999 for all articles published during the period from January 1990 through August 1999. In January 2001, this literature search was updated to include all studies published through the end of December 2000. All abstracts were examined, and relevant articles were retrieved. Papers were subsequently excluded if they were found to be reviews, editorials, or opinion pieces or if they were judged not to be outcomes research. Studies that claimed to measure quality of life but did so without an instrument (i.e., relying on the general impressions of the physicians) or that only measured performance status were excluded. Predetermined data elements were abstracted and entered immediately into an electronic database. These included the intervention studied, the type of outcome assessed, measurement instruments used, the study design and perspective, years of data collection, sample size, stages and histology of lung cancer in the study population, percentage of female subjects, percentage of nonwhite subjects, average age of the patients, and a short description of the study findings. For the updated review (August 1999 through December 2000), additional data elements were abstracted, such as the phase of care being addressed by the study, whether the sample size was based on an a priori power calculation, and whether confidence limits were presented around measured estimates. Database manipulation and analyses were carried out by using the Statistical Analysis Software, version 8.01 (SAS Institute, Cary, NC, 1999).
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RESULTS |
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Literature Search
The literature search yielded 860 articles, of which 210 were deemed appropriate for retrieval and review on the basis of the abstract. Of these, 11 were excluded: Six were reviews (4-9), one was an opinion piece (10), and four did not have any true outcomes component (11-14). The remaining 199 studies are described in the Appendix. One hundred six studies (53%) dealt primarily with quality-of-life measurement, followed in number by the 69 (35%) papers that examined costs (Table 1). There were 11 (6%) studies dealing with communication and decision making, 11 (6%) assessing the quality of care, and two (1%) evaluating patient satisfaction. There has been a rise in the number of studies published each year over the course of the decade, most noticeable in the quality-of-life literature (Fig. 1).
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Most studies focused on NSCLC (108 studies, 54%), although many examined both histologies (63 studies, 32%). More than half of the studies (51%) examined patients with all stages of disease, and more than 30% were restricted to the study of advanced, incurable cancer. A prospective cohort study design was most common, being used in 61 (31%) of the studies, followed by quality-of-life or economic companions alongside randomized controlled trials (43 studies, 22%). Sixteen studies (8%) were carried out prospectively alongside phase I or II trials. Thirty-one decision analyses (16% of studies), all but one an economic evaluation, were reported. Retrospective cohorts were assembled in 26 (13%) studies, and 16 studies (8%) carried out cross-sectional surveys.
Most studies came from the United States (68 studies, 34%), followed by Canada (33 studies, 17%), and the United Kingdom (25 studies, 13%). The distribution was similar for all outcomes. Eight studies (4%) were international. For studies that included patients, the average sample size was 523; however, this varied widely. Studies of quality of care (mean = 3560 patients) and cost (mean = 624 patients) tended to be the largest. Quality-of-life studies averaged 206 patients, and studies of decision making and communication had 254 patients on average; satisfaction was evaluated in an average of 37 patients. The mean age of patients in lung cancer outcomes studies was 63 years, and 30% of patients were women. There were three studies, all from the same author, that examined quality-of-life issues in cohorts made up exclusively of women (15-17). Only 24 articles (12%) commented on the racial makeup of their study population. All but one, a communication study from the United Kingdom, were U.S. quality-of-life papers. Of those studies that did report a racial distribution, an average of 15% of patients were nonwhite (range, 1%-38%). The age, sex, and racial demographics of patients studied did not differ greatly across the different types of outcomes studies. Levels of comorbidity were generally not reported.
Eighty-four percent of the studies dealt with treatment, and 13% evaluated staging work-up. The rest were evenly split between studies of diagnosis and prevention. A priori power calculations for the outcomes end point were made in 13% of prospective randomized studies and in 40% of cross-sectional surveys. A power calculation was never reported as being a consideration in other study designs, such as phase II studies or prospective cohort analyses.
Quality of Life
Quality-of-life studies were most likely to examine patients with "lung cancer" not restricted to homogeneous stage (46% of the time) and often were not restricted to a common histologic group either (30% of the time). Of note, more than one-quarter of the studies were primarily methodological in nature. As expected, the majority of quality-of-life studies were prospective, and 27% involved quality-of-life assessment alongside a randomized trial. Another 16% were carried out alongside phase I and II trials. Fifty-seven percent of the studies presented quality-of-life estimates with some indication of variability (e.g., confidence intervals and standard deviation), whereas 43% did not.
Instruments More than one-half of the studies used more than one instrument. Forty-one percent used two, and 13% used three or more, for an average of 1.7 instruments per study. When two or more instruments were used in the same study, they were usually used as complementary instruments in a clinical trial. Although generally not paired for methodological reasons, the different instruments tended to show convergent results. The European Organization for Research and Treatment of Cancer Quality of Life Cancer Questionnaire (EORTC QLQ-C30), either alone or with its lung cancer subscale, the LC13, clearly dominates the literature, being used in 39 (37%) studies (Table 2), especially in more recent studies. The next most commonly used scales were the Rotterdam Symptom Checklist (RSC) and the Hospital Anxiety and Depression Scale (HADS), which were often used together in British studies in the early 1990s, along with the British Medical Research Council (MRC) daily diary card. U.S. studies tended to use the domestically developed Lung Cancer Symptom Scale (LCSS) or Functional Assessment of Cancer Therapy with its lung cancer subscale (FACT-L). In six studies, the investigators developed unique, unvalidated instruments to measure quality of life.
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Findings To date, the results of many of the quality-of-life studies seem predictable. In observational studies, patients starting out with poor quality of life were less likely to receive aggressive treatment. However, health care professionals can underestimate quality of life compared with patient self-reports (18). Furthermore, quality of life can change rapidly and, therefore, should be measured frequently (at least every 3-4 weeks) to get an accurate picture of the disease course (19). A common finding in randomized studies was that the toxicity of treatment was counterbalanced by decreased tumor-related symptoms (4,20-22). Quality of life can improve even with stable disease (23). Quality-of-life studies rarely changed the outcome of an analysis, but there were some examples where both treatment arms yielded similar survival results, and the quality-of-life effects determined the preferred strategy (24,25). The ability of quality-of-life measures to predict response and survival has been shown many times (26-34). Missing data as a result of patient deterioration were frequently cited as a technical problem, however, often resulting in compliance of around 50% or less (22,24,33, 35-43). Simple daily diary cards have been reported to have better completion rates (25,44).
Costs
Cost studies have tended to focus on NSCLC. There was a flurry of publications on NSCLC in the middle of the decade, which seems to have leveled out somewhat recently. The plurality of papers (43%) reported decision analytic disease and economic models, although a total of 22% collected prospective or retrospective data alongside randomized clinical trials. It is interesting that only eight (12%) of the 69 economic studies reported a clearly negative result for the intervention being assessed (45-52).
Fifty-five percent of studies looked only at the resources consumed by lung cancer care or at cost-minimization between two management options, without consideration of treatment effects. Thirty-eight percent were cost-effectiveness studies with some measure of the consequences of intervention in the denominator. Methodologies differed widely between studies. Only two (3%) attempted to incorporate patient preferences in a cost-utility analysis (50,53). These did not use validated utility instruments like the EQ-5D (EuroQol) or the Health Utilities Index (HUI). A non-economic methodological study using data from a lung cancer trial tried to map the RSC and HADS to the EQ-5D and HUI, however (54).
Most studies (93%) took the payer's perspective. Only four studies (6%) took a societal perspective, including costs such as patient time and transportation expenses in the numerator (55-58). The rest of the studies either looked at patient's out-of-pocket costs, or the perspective could not be inferred. Still, the types of costs included in these analyses were inconsistent, with some studies, for example, reporting results that excluded the costs of the study drug (59-61). Subjectively, the quality of studies including an economic component varied widely, with several simply stating cost estimates without any methods discussed (62-64).
Because of the short survival time of most patients, lung cancer was commonly found to be a relatively inexpensive disease to manage on a cost-per-case basis. However, because of its prevalence, it constitutes an important proportion of total health care expenditures (61). Hospitalization consistently emerged as the main driver of cost. Interventions such as palliative chemotherapy can lead to patients spending fewer days in hospital and requiring less palliative radiotherapy, thus offsetting the cost of the intervention (65).
Quality of Care and Satisfaction
There were 11 studies dealing with quality-of-care issues and two studies concerned with patient satisfaction. The most consistent theme to emerge from these studies was that there is variation in practice patterns based on both valid medical considerations like age (66-68) and nonmedical factors like race (69), geographic location (70,71), socioeconomic status (72), and the type of physician being consulted (73). Patient satisfaction was found to be enhanced by using quality-of-life surveys taken during visits to the clinic (74) and by identifying how involved patients wanted to be in the decision-making processes (75).
Communication and Decision Making
The 11 articles pertaining to decision making and doctor—patient communication focused on areas where the treatment decision is controversial, such as multimodality treatment for locally advanced NSCLC and palliative chemotherapy for advanced disease. These studies were generally carried out by using structured interviews, and they reinforced the notion that patients want information about their disease and want to participate in decision making, although there is important individual variation in how involved they want to be.
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DISCUSSION |
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This systematic review has found that there is a substantial body of work in outcomes research pertaining to lung cancer. Some areas, such as quality-of-life assessment and cost analyses, have received much attention and prominence. Quality-of-care studies, including patient satisfaction, decision making, and doctor-patient communication, appear in publications less often. Unlike other diseases where there are technologies suitable for assessment in several distinct phases of care (screening, primary and adjuvant therapy, follow-up, and survivorship), outcomes research in lung cancer, by virtue of the disease's poor prognosis, is largely focused on palliative care. It is comforting to see that the age, sex, and racial makeup of most studies are similar to those reported for lung cancer in the Surveillance, Epidemiology, and End Results (SEER) Program1 (3). It is interesting that race is really only an issue in U.S. studies and is not even noted in studies from other countries. Nevertheless, there remain several areas where further research is needed and where certain vulnerable populations require ongoing vigilance to ensure representation.
Quality-of-Life Studies
Quality-of-life research in particular has undergone substantial methodological development over the past decade. However, the result is a body of work that has largely included a mixture of tumor stage and histologic types assessed with a wide variety of instruments. Useful clinical information appears to be lacking on the experiences of homogeneous groups of patients receiving specific treatments. The situation is starting to improve, however, as researchers recognize the importance of an intervention's effects on quality of life and move its assessment into the earlier phases of testing. Still, quality-of-life end points rarely figured into the power calculation when designing these trials. This may be appropriate, however, given the relatively low completion rates of quality-of-life surveys discussed below.
The EORTC QLQ-C30 is emerging as the most commonly used quality-of-life instrument. This is partly driven by the decision of the MRC to switch from the RSC and HADS to the EORTC scale as a required component of all of its sponsored trials. The EORTC QLQ-C30 has undergone relatively extensive field testing for reliability and validity. Because its first disease-specific module was the lung cancer module, the LC13, much of the early psychometric validation was done in lung cancer patients (44,76-79). Other lung cancer-specific instruments are the FACT-L and the LCSS. All three have undergone fairly extensive reliability and validity testing and appear to have acceptable psychometric properties (5,80). They have never been compared head-to-head, however. All instruments are meant to be self-administered, although the LCSS has an optional observer component. In different studies they were administered in a variety of ways (81), including being sent to physicians to fill out (82), administered by computer (74), or being only partially administered (21,83-86) or scored (38,43). Partial administration was sometimes done in order to focus on the global quality-of-life questions (e.g., questions 29 and 30 of the EORTC QLQ-C30). The use of ad hoc instruments to measure quality of life is decreasing and should continue to be discouraged. The measures described above have undergone extensive field testing, and there is little reason to create new instruments, the results of which are difficult to interpret across studies.
The EORTC QLQ-C30 consists of 30 questions in yes/no, Likert, and numerical analogue scale (NAS) formats (87). The yes/no questions have been removed in the most recent version, however. The LC13 adds 13 more questions (88-90). It is estimated to take about 11 minutes to complete (91) and, at the time of this writing, has been translated into 35 languages. The questions are mostly about disease-related symptoms and treatment-related toxicity experienced in the week before the survey. The LC13 is thought to be especially good in situations where patients are relatively ill, but it is lengthy and complicated compared with other instruments. It is unique in including a question about the perceived financial impact of the disease.
The FACT-G (92) consists of 34 questions, 28 of which are scored, whereas the FACT-L (93) currently adds seven questions. Questions about hair loss and regret for smoking were taken out in 1995. The FACT-G uses Likert and NAS formats to ask questions about quality of life in the week leading up to its administration. The FACT focuses more on psychosocial dimensions than the EORTC instrument. Consequently, it may be best in situations where patients are not as sick. It has been assessed at a grade 6-7 reading level, and it has been translated into at least 30 languages. Taking up to 10 minutes to administer, it is also a fairly burdensome scale to complete. As a result, the Physical and Functional scales have been combined with the lung cancer module to form the shorter 21 item "Trial Outcome Index" (94,95).
The LCSS is only a disease-specific instrument, with no general health component (96-100). It focuses exclusively on the symptoms of lung cancer and does not attempt to assess the toxicity of treatment. Its advantage is its simplicity. It is rated at a grade 2 level of comprehension; consists of only nine visual analogue scales (VAS) (and six optional ones for an observer to fill out), asking about quality of life in the previous 24 hours; and takes only 5-8 minutes to complete (101). However, the lack of a general component makes it difficult to compare across disease sites, and some respondents have difficulty using the VAS. It is recommended that it be given initially as a face-to-face interview to demonstrate the VAS. It has been translated into at least 26 languages (102).
Additional Observations
Missing data continue to be a big problem in quality-of-life research. This is especially true in lung cancer, because patients are often too sick to complete surveys and usually experience a rapid downhill course (19). The effects of aggressive treatment can contribute to this phenomenon as well. Consequently, censoring is informative, resulting in misleading analyses in which the average quality of life can appear to increase over time as only healthier patients remain. Several studies in this review (22,24,33,35-43) found that only about one-half of the patients had more than a baseline evaluation, making repeated measures analyses and even comparisons of the proportion of patients who improved versus worsened impossible. Some analysts have tried to impute missing data (19), but this is difficult when there is only one measurement from a patient and the specific trajectory of quality of life is uncertain. Others have tried to limit the analysis to those with complete data (36); however, this may not be valid because it assumes uninformative censoring. As a result, some have turned to looking at other measures such as performance status (90) to estimate missing quality-of-life data. Methodological studies developing less burdensome instruments or validating the use of proxy respondents in various situations would be welcome in order to ameliorate the problem of missing data as a result of patient deterioration in lung cancer quality-of-life studies.
Because of the short survival of lung cancer patients, the handling of death presents another analytic challenge. Quality of life can be assessed at a fixed time point or at the time of median survival, but this will lead to overestimates because the patients who die before that time, and who most likely had a worse quality of life, will not be included. Some have calculated an area under the survival curve, adjusted for quality of life, to come up with an average daily quality-of-life estimate (19). For example, the Q-TWiST approach assigns death a value of 0 (103,104). However, patients have rated some health states pertinent to lung cancer, such as having constant pain, as being worse than death (105).
Cost Studies
The number of economic studies peaked in the middle of the decade with the introduction of several new and exciting, though expensive, interventions like multimodality therapy for stages IIIA or IIIB disease and palliative compounds like gemcitabine and paclitaxel. Because there were fewer changes in the management of SCLC, it received less attention. Recent clinical data on the possible effectiveness of expensive technologies such as spiral computed tomography and positron emission tomography scanning in the early detection and staging of lung cancer will probably result in another run of publications in the next few years.
The finding in most reports that the study intervention is cost-effective is likely the result of a combination of factors, some benign and some more problematic. Most cost-effectiveness studies probably start with a "back of the envelope" calculations that can tell roughly whether the analysis being considered is likely to yield an important result; those interventions that are not cost-effective are not pursued. Furthermore, negative studies are generally less interesting and are less likely to be submitted or accepted for publication ("publication bias"). However, the wide variation in methodologies reported may also have an effect. Reporting, for example, cost-effectiveness without considering the cost of the drug under evaluation (59-61) could present an inaccurate picture. Publication of methodological and reporting standards by the U.S. Panel on Cost-Effectiveness in 1996 and demands for transparency in published economic models should lead to improvement in the general methodological quality and comparability of studies in the future. Another positive effect should be more focus on the societal, patient, and caregiver costs of undergoing treatment, areas that have received little attention to date.
Other Issues
Quality of care is an area receiving increasing attention in other areas of medicine, yet few studies have analyzed the quality of lung cancer care. In addition to studies attempting to shine a light on inequities and variation in practice, more research is needed in the areas of patient satisfaction, decision making, communication, and the appropriate use of palliative interventions. Related to this, there seems to have been little qualitative research done to date in lung cancer, compared with other diseases such as breast cancer. Qualitative methods may be able to bring more insight into patients' actual experience of this terrible disease and its treatment.
Despite good representation in lung cancer outcomes research, at least in U.S. studies, visible minority patients, the elderly, and women remain at risk for being relatively neglected. Lung cancer is a disease of the elderly and is more common in several minority groups, such as African Americans. Furthermore, lung cancer is increasing in women, whereas the incidence in men has leveled off and has begun to decrease. By addressing the effects of socioeconomic status, literacy, and culture among these groups of patients, outcomes researchers have the opportunity to explore issues of equity and justice in these patients' access to care and the quality of care they receive.
Outcomes research, encompassing such elements of health services research as cost-effectiveness analyses and quality-of-life studies, studies looking at nontraditional clinical end points like quality of care and satisfaction, as well as disease modeling and decision analytic studies, is currently represented in all of these facets in the lung cancer literature. There needs to be more agreement on consistent methods, preferred instruments, and consideration of these outcomes early on in the study design, however, in order to increase rigor in the field. For example, including utility estimates in cost-effectiveness analyses is particularly important for most lung cancer interventions, because effects on quality of life must be balanced against what are usually modest benefits from treatment. In the end, the greatest gains will likely come from exploring the relationships among traditional biomedical outcomes like response and survival, symptom measures, functional status scales, and nontraditional outcomes like health-related quality-of-life and satisfaction with care in order to determine in which situations there is sufficient value added to justify expending the resources to gather these additional data.
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NOTES |
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I thank Candace Canto of the National Library of Medicine for assistance with the literature search.
1 Editor's note: SEER is a set of geographically defined,
population-based, central cancer registries in the United States, operated by
local nonprofit organizations under contract to the National Cancer Institute
(NCI). Registry data are submitted electronically without personal identifiers
to the NCI on a biannual basis, and the NCI makes the data available to the
public for scientific research. 
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