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Journal of Thoracic Oncology:
doi: 10.1097/JTO.0b013e31822ada77
Original Articles

Comparison of Demographic Characteristics, Surgical Resection Patterns, and Survival Outcomes for Veterans and Nonveterans with Non-small Cell Lung Cancer in the Pacific Northwest

Zeliadt, Steven B. PhD*†; Sekaran, Nishant K. MD‡; Hu, Elaine Y. MS*; Slatore, Christopher C. MD, MS§; Au, David H. MD*‡∥; Backhus, Leah MD∥¶; Wu, Daniel Y. MD, PhD∥; Crawford, Jeffrey MD#; Lyman, Gary H. MD, MPH#; Dale, David C. MD‡

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Author Information

*VA Health Services Research & Development Service, Department of Veterans Affairs Medical Center; †Health Services Department, University of Washington; ‡Department of Medicine, University of Washington, Seattle, Washington; §Department of Veterans Affairs Medical Center, Portland, Oregon; ∥Department of Veterans Affairs Medical Center, Seattle, Washington; ¶Division of Cardiothoracic Surgery, Department of Surgery, University of Washington, Seattle, Washington; and #Department of Medicine, Duke University and the Duke Comprehensive Cancer Center, Durham, North Carolina.

Disclosure: The authors declare no conflicts of interest.

Address for correspondence: Steven B. Zeliadt, PhD, VA Puget Sound HSR&D Northwest Center of Excellence, 1100 Olive Way, Suite 1400, Seattle, WA 98101. E-mail:

Portions of this work were presented at the American Society of Clinical Oncology 2010 Annual Meeting in Chicago, Illinois June 4–8, 2010.

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Introduction: Lung cancer is a leading cause of death in the United States and among veterans. This study compares patterns of diagnosis, treatment, and survival for veterans diagnosed with non-small cell lung cancer (NSCLC) using a recently established cancer registry for the Veterans Affairs Pacific Northwest Network with the Puget Sound Surveillance, Epidemiology, and End Results cancer registry.

Methods: A cohort of 1715 veterans with NSCLC were diagnosed between 2000 and 2006, and 7864 men were diagnosed in Washington State during the same period. Demographics, tumor characteristics, initial surgical patterns, and survival across the two registries were evaluated.

Results: Veterans were more likely to be diagnosed with stage I or II disease (32.8%) compared with the surrounding community (21.5%, p = 0.001). Surgical resection rates were similar for veterans (70.2%) and nonveterans (71.2%) older than 65 years with early-stage disease (p = 0.298). However, veterans younger than 65 years with early-stage disease were less likely to undergo surgical resection (83.3% versus 91.5%, p = 0.003). Because there were fewer late-stage patients among veterans, overall survival was better, although within each stage group veterans experienced worse survival compared with community patients. The largest differences were among early-stage patients with 44.6% 5-year survival for veterans compared with 57.4% for nonveterans (p = 0.004).

Conclusions: The use of surgical resection among younger veterans with NSCLC may be lower compared with the surrounding community and may be contributing to poorer survival. Cancer quality of care studies have primarily focused on patients older than 65 years using Medicare claims; however, efforts to examine care for younger patients within and outside the Department of Veterans Affairs are needed.

Lung cancer is the leading cause of cancer-related death in the United States and the leading cause of cancer deaths for veterans cared for by the U.S. Veterans Health Administration (VHA).1 The burden of lung cancer among veterans is nearly double compared with the general population because of the high prevalence of smoking among military service members.2–4 There is relatively little information on quality and patterns of care for patients treated within the Veterans Affairs (VA) for non-small cell lung cancer (NSCLC).5 A historical study observed that lung cancer resection rates for early-stage disease were lower among VA patients compared with national rates, potentially because of difficulty accessing specialty care.6 In 2006, the VA conducted a chart review at 132 facilities randomly selecting 20 patients with lung cancer from each site,7 observing that only 46% of patients who underwent surgery were treated within the recommended timeframe of 8 weeks.8 Disparity in initial treatment, particularly surgery for early-stage disease, is a key priority both within and outside of the VA as black race, lower education, and lower socioeconomic status have been observed to be associated with low rates of surgical resection for early-stage lung cancer.9–11

In 1995, as part of the VHA's transformation from a highly centralized hospital system to a multifaceted primary and specialty care-based delivery system,12 the VHA developed a comprehensive oncology program that included a mandate for a national cancer registry program to evaluate and improve the quality of oncology care delivered to veterans.13 In 2010, there were 132 cancer registry programs in the VHA that comprise the VA Central Cancer Registry of which eight comprise the Northwest Veterans Affairs Oncology Registry (VAOR) which provided data for this study.

As no previous studies have used regional or national VA cancer registries to evaluate care for NSCLC, the objective of this study was first to examine the completeness of the demographic and tumor characteristic information in Northwest VAOR, and then compare tumor characteristics, surgical resection patterns, and survival for VA patients with patients in the surrounding community. We used records from the Puget Sound Surveillance, Epidemiology, and End Results (SEER) registry, one of the oldest SEER registries in the nation, to serve as the gold standard for our comparison.14

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We identified subjects in both the VAOR and Puget Sound SEER registries who were diagnosed with NSCLC between January 1, 2000, and December 31, 2006. Using the VAOR SQL database, all patients with an International Classification of Diseases, Ninth Revision diagnosis code of 162 were identified. Patients younger than 18 years or older than 100 years were excluded, as were cases identified as diagnosed only on the death certificate or at the time of autopsy. Women were excluded from both VAOR and SEER databases. Although women comprise 47% of SEER subjects, only approximately 3% of lung cancer cases in the VA are among women, thus because of privacy concerns associated with potential of identifiability in subgroup analyses, they were excluded. Histologies for NSCLC were classified as adenocarcinoma, squamous cell carcinoma, other NSCLC (including bronchioloalveolar carcinoma, large-cell carcinoma, mixed histology, and other histologies), and NSCLC not otherwise specified.15

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Registry Data

SEER collects and publishes cancer incidence and survival data from 17 distinct population-based cancer registries covering approximately 26% of the US population, and the completeness and accuracy of data collection in SEER have been extensively validated.14,16 SEER data include information on patient demographics, tumor morphology and stage at diagnosis, first course of treatment, and follow-up for vital status.17,18 SEER records were obtained for this study based on the November 2008 submission public use file.19 Similar to SEER, registries contributing to the VAOR perform accession, abstraction, and follow-up activities in conformity with American College of Surgeons and Commission on Cancer data collection standards.20 All VA cancer registries are required to have dedicated tumor registrars and use automated registries using uniform software. The recommended registrar staffing ratio is 1 full-time equivalent position per 350 new cancer cases per year. The VA registrar ensures completeness of registry data by contacting non-VA physicians as well as patients and family members, if necessary, to ensure completeness of documentation for patients diagnosed in the VA who may receive a portion of their initial care outside of the VA. The VA is not a closed system, and it is possible that some subjects were diagnosed in both the VA and an outside hospital in the Puget Sound SEER catchment area. Privacy issues precluded direct identification of duplicate subjects, and based on use agreements with SEER, no attempt was made to identify duplicates.21

The staging system used in both SEER and VAOR databases is based on the Revised International System for Staging Lung Cancer 6th edition, as adopted by the American Joint Committee on Cancer.22 This staging system, based on tumor, node, metastasis classification, is a measure of the extent of disease, can determine prognosis, and can guide management. This information is incorporated into the overall disease stage (stages I-IV).22 For both the SEER and VAOR databases, the extent of disease was evaluated based on clinical-diagnostic stage. Both registries include pathologic information when available. However, because practices may differ between providers in the community and VA that would influence availability of pathologic staging information, the main comparison was based on clinical stage. This variable includes information pertaining to medical history, physical examination, laboratory testing, radiology, tissue sampling, and other treatment evaluation undertaken before primary therapy.

Survival estimates were based on time to all-cause mortality. The Puget Sound SEER registry uses a variety of methods to collect vital status follow-up information, primarily linking to death certificate files from the Washington State Department of Health and to records from Washington State Department of Motor Vehicles. In addition, records of subjects not known to be deceased are submitted to the Center for Medicare/Medicaid Services and the Social Security Administration Death Master File to determine if benefits are being collected and searches using the National Death Index and commercial services including Accurint. VA cancer registrars identify deceased veterans through death certificates internal to the VHA and identification of deaths from other VA benefit programs including pension and burial programs. Similar to SEER, VA routinely exchanges information about deceased individuals with the Center for Medicare/Medicaid Services and the Social Security Administration Death Master File.23

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Descriptive statistics were used to compare race (white or non-white), age at initial diagnosis (<55, 55–64, 65–74, 75–84, and 85+), receipt of surgery, tumor stage (I, II, III, IV, or unknown), and histologic subtype. All variables were treated categorically, and χ2 tests were used to compare veterans in VAOR with subjects in SEER. Kaplan-Meier estimates of survival from the date of diagnosis were based on the log-rank test. All subjects not known to be deceased were censored at the time of the last follow-up for each database, which was the end of 2006 for SEER and the end of 2008 for VAOR.19 Analyses were stratified by age, younger than 65 years and 65 years and older. Kaplan-Meier survival curves were plotted for patients younger than 65 years and 65 years and older for all stages and for stage I and II subjects who underwent surgery. To further adjust for age differences in the receipt of surgery, a logistic regression model was used including age as an adjustment variable. The results are presented as age-adjusted p values in the table. Proportional hazards models were used to further adjust survival estimates by age for both the overall and age-stratified analyses. The age-adjusted p values are presented. The proportional hazards assumption was evaluated using log-log plots of survival curves. We note that the racial distribution was similar between the two registries and that other covariates, such as comorbidity and body mass index, are only available through linkage to medical claims. Thus, further adjustment for comorbidity or other health factors was not feasible. All analyses were conducted in Stata 11.1. This study was reviewed and approved by the Institutional Review Board at VA Puget Sound Health Care System.

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Ten patients were excluded because their age at diagnosis was less than 18 years or more than 100 years, and 394 subjects were excluded based on the tumor being identified at autopsy or death certificate only. The final sample size included 1715 male veterans in the VAOR and 7864 men diagnosed with lung cancer in the Puget Sound SEER registry.

The mean age was 68.0 years (SD = 9.6) for the 1715 veterans and 69.3 years (SD = 11.0) for the 7864 men identified in the Puget Sound SEER registry. Tumor characteristics are presented in Table 1. The proportion of patients diagnosed with stage IV disease was similar in both registries, 37.0% in VAOR and 39.0% in SEER (p = 0.121). However, the proportion of subjects in SEER with missing stage information was 12.2% compared with 5.4% in VAOR. The VAOR population was younger, with 73% of VA patients younger than 75 years at the time of diagnosis compared with 64% of SEER patients. The majority of patients in both registries were white, reflecting the demographics of this age group in the Pacific Northwest.

Table 1
Table 1
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The frequency of surgery is presented in Table 2. Stage I and II patients in the VAOR younger than 65 years were less likely to undergo surgery (83.3%) compared with stage I and II patients younger than 65 years in SEER (91.5%, age-adjusted p = 0.003). There were no differences in surgery for stage I and II patients aged 65 years and older (age-adjusted p = 0.298). For younger patients with stage III disease, surgery rates were similar for veterans and nonveterans (age-adjusted p = 0.423), whereas there was a trend toward more frequent surgical resection among older veterans with stage III disease (age-adjusted p < 0.001).

Table 2
Table 2
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As presented in Table 2, overall survival was similar for younger patients in VAOR and SEER when all stages were combined (including missing stage), with nearly overlapping survival curves (Figure 1). For patients younger than 65 years, 5-year survival for all stages combined was 16.0% in VAOR and 17.9% in SEER (age-adjusted p = 0.415). Similarly, among patients aged 65 years and older, 5-year survival was similar for veterans and nonveterans (age-adjusted p = 0.142). We note the unadjusted survival proportions of 13.5% for veterans and 10.9% for nonveterans reflect the lower frequency of veterans older than 75 years. Adjusting for age affected the significance of the results for the more than 65 cohorts, whereas age adjustment did not change the findings substantially for the younger cohort.

Figure 1
Figure 1
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Survival for stage I and II patients was considerably lower (44.6%) for VAOR patients younger than 65 years compared with 57.4% for the SEER cohort (age-adjusted p = 0.004). Similarly, survival for stage I and II patients was slightly lower for VAOR patients older than 65 years (age-adjusted p value = 0.035). The combined survival outcomes for stage I and II patients include a mixture of patients who did and did not undergo surgery. The largest differences in survival between VAOR and SEER were observed among patients who did not undergo resection. Among stage I and II patients who underwent surgery, there was a slight trend of worse survival for VAOR patients overall (age-adjusted p value = 0.060; Figure 2). However, the differences in survival between VAOR and SEER were more pronounced among stage I and II patients who did not undergo surgery (age-adjusted p value = 0.015; Figure 3). Notably, survival was considerably lower among stage I and II patients who did not undergo surgery in both VAOR and SEER, with few patients surviving beyond 5 years.

Figure 2
Figure 2
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Figure 3
Figure 3
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This initial examination of the Northwest VAOR demonstrates a high level of completeness in capturing tumor characteristics among veterans newly diagnosed with NSCLC in a VA medical center. The completeness of key tumor characteristics, including tumor stage, was higher in the VAOR than in the Puget Sound SEER registry. The distribution of NSCLC patients with stage IV disease was similar to SEER and to the 300,000 subject National Cancer Database.24 These results suggest that the VAOR is a reliable source of data to examine resource utilization, treatment heterogeneity, comparative effectiveness, and survival of patients treated within the Pacific Northwest for NSCLC. We do note differences in surgical rates for stage I and II patients compared with stage III patients. Although resection rates were lower in VAOR for stage I and II patients compared with SEER, the proportion of veterans with stage III disease were actually more likely to undergo resection. Although the difference in the absolute number of stage III patients undergoing surgery between the VAOR and SEER cohort is relatively small, it is possible a portion of these patients may be understaged at VA Medical Centers compared with non-VA facilities. Future studies should examine differences in staging procedures, including positron emission tomography, between VA and non-VA facilities.

This evaluation also provides the foundation for ensuring the validity of future studies combining VA cancer registry records with the VA's comprehensive electronic medical record databases, similar to the SEER-Medicare database that combines Medicare claims with SEER records for patients older than 65 years.25 The VA has invested heavily in electronic medical records, with all inpatient and outpatient visits captured since 1986, and databases that now include comprehensive information including pharmacy records, vital measures, and laboratory values. Linkage of cancer registry records with these electronic records provides a unique resource to examine cancer care and allow for inclusion of younger men.26 Although SEER-Medicare has been used extensively to examine cancer care for patients older than 65 years, few large studies have been able to include younger patients. The VAOR represents a unique opportunity to focus examinations on patients seen within a vertically integrated healthcare delivery system.

Our findings suggest that younger veterans with early-stage disease were less likely to undergo surgery and have worse survival compared with men in the surrounding community. Ensuring that all eligible candidates are offered surgery is critical for this devastating disease and a key priority for the VA.27,28 The reason for lower surgery rates in the VA compared with the community cannot be determined based on these data, as no claims or comorbidity records are available for the SEER population. The significantly worse overall survival among younger veterans who did not undergo surgery compared with men in the community who did undergo surgery (Figure 2) suggests that comorbidities may be higher among veterans in this population and may have been a factor in the lower surgery rates. The VA recently conducted a chart review of 20 patients with lung cancer from 132 medical centers across the VA. This study observed that veterans with early-stage disease had longer time in initiating treatment from the time of diagnosis compared with advanced-stage patients.29 One of the potential reasons for the delays was access to appropriate surgeons, which may also be contributing to lower rates of surgery in the VA compared with the community.

This comparison is unique as few studies have compared cancer survival for veterans and nonveterans. Regulations prohibiting the exchange of cancer registry data among VA and non-VA registries in the last decade have made such comparisons difficult. One historical study from Pennsylvania observed that survival was worse for white veterans compared with whites in the community, whereas survival for black veterans was similar to blacks in the community.30 Our results suggest that these comparisons are important to be able to compare healthcare delivery between different systems of care, and facilitation of data sharing between federal and nonfederal agencies should be encouraged.

A key limitation of this study is the lack of covariates to control for potential differences between the VAOR and SEER population among patients younger than 65 years. Although detailed comorbidity, smoking history, body mass index, pulmonary function tests, laboratory tests, and other information are available on the veteran population, similar information was not available for the SEER cohort. We note that the VAOR and SEER populations differed considerably in the distribution of patients older than 75 years. Because of the lack of comorbidity and other key variables, results are presented stratified by age with additional age adjustment to estimate appropriate p-values. Although this did not change the results for patients younger than 65 years, for patients 65 years and older, we observed significant differences in unadjusted and age-adjusted analyses. After age adjustment, survival among older patients was similar in both registries.

Another limitation is the lack of information on treatment other than surgery. One unique future opportunity of the VAOR will be the ability to examine outcomes associated with detailed chemotherapy patterns as VA databases include chemotherapy dose and laboratory measures to evaluate response and toxicities. Similar data were not available in other registry settings, including SEER-Medicare, which only has the date of chemotherapy claim.25 Our findings cannot be generalized to female veterans. Within the next decade, women are expected to comprise 10% of the VA population. However, the population in this study where the mean age was 68 years includes less than 3% women. Although all VA cancer registries use standardized cancer registry software and have access to similar electronic medical record systems, the completeness and validity of data observed in this study may not exist across all VA registries nationally. In addition, some VA patients may have been included in the SEER registry counts. The overall number of subjects is likely to be minimal as VA stopped reporting to SEER in 2005, and SEER typically excludes patients diagnosed at VA hospitals.21 Privacy constraints precluded identification of diagnosing facility for verification, and individual identifiers were not available to examine subjects with overlapping data.

Overall, this initial evaluation demonstrates the validity of VAOR and highlights the importance of this resource for evaluating and improving oncology care for veterans. The gap identified in use of surgical resection for younger, early-stage patients in the VA is a critical area for oncology programs in the VA's Northwest network to further ensure that no true disparity exists.

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Supported, in part, by the U.S. Department of Veterans Affairs, Office of Research and Development Health Services R&D Program. This work was funded by Amgen through a grant to the Duke University Awareness of Neutropenia In Chemotherapy Study Group.

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Lung cancer; Surgical resection; Survival; Veterans Health Administration; Surveillance; Epidemiology, and End results (SEER)

© 2011International Association for the Study of Lung Cancer


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