Background If discovered at an early stage, non–small-celllung cancer is potentially curable by surgical resection. However,two disparities have been noted between black patients and whitepatients with this disease. Blacks are less likely to receivesurgical treatment than whites, and they are likely to die soonerthan whites. We undertook a population-based study to estimatethe disparity in the rates of surgical treatment and to evaluatethe extent to which this disparity is associated with differencesin overall survival.
Methods We studied all black patients and white patients 65years of age or older who were given a diagnosis of resectablenon–small-cell lung cancer (stage I or II) between 1985and 1993 and who resided in 1 of the 10 study areas of the Surveillance,Epidemiology, and End Results (SEER) program (10,984 patients).Data on the diagnosis, stage of disease, treatment, and demographiccharacteristics of the patients were obtained from the SEERdata base. Information on coexisting illnesses, type of Medicarecoverage, and survival was obtained from linked Medicare inpatient-dischargerecords.
Results The rate of surgery was 12.7 percentage points lowerfor black patients than for white patients (64.0 percent vs.76.7 percent, P<0.001), and the five-year survival rate wasalso lower for blacks (26.4 percent vs. 34.1 percent, P<0.001).However, among the patients undergoing surgery, survival wassimilar for the two racial groups, as it was among those whodid not undergo surgery. Furthermore, analyses in which adjustmentswere made for factors that are predictive of either candidacyfor surgery or survival did not alter the influence of raceon these outcomes.
Conclusions Our analyses suggest that the lower survival rateamong black patients with early-stage, non–small-celllung cancer, as compared with white patients, is largely explainedby the lower rate of surgical treatment among blacks. Effortsto increase the rate of surgical treatment for black patientsappear to be a promising way of improving survival in this group.
In the United States, lung cancer is the leading cause of deathattributed to cancer among both men and women, claiming thelives of more than 150,000 people each year. About one thirdof patients with the most common histologic type of lung cancer,non–small-cell cancer, are first given the diagnosis atan early, potentially curable stage. If treated by surgicalresection, these patients have a 40 percent likelihood of survivingfor five years or longer. In contrast, patients who presentwith advanced disease or who do not undergo surgical resectionhave a median survival of less than one year.1 In the lightof this information, it is important to determine whether patientswho have potentially curable disease actually receive surgicaltreatment.
Several studies have uncovered an association between race andthe likelihood of receiving surgical treatment for resectablenon–small-cell lung cancer. Greenwald et al. found thatpatients with stage I disease in Seattle, San Francisco, andDetroit were less likely to undergo surgical resection if theywere black or of lower socioeconomic status than if they werewhite or of higher socioeconomic status.2 Smith et al. foundsimilar disparities in the treatment of black patients and whitepatients in a cohort in Virginia.3 Samet et al. found that olderage and Hispanic ancestry were associated with lower rates ofsurgical treatment in a cohort in New Mexico.4
We undertook a study to answer two questions about the treatmentof early-stage, non–small-cell lung cancer. First, isthere a difference in the rate of surgical treatment betweenwhite patients and black patients with this type of lung cancer,and if so, is the discrepancy still apparent once we accountfor the effects of coexisting illness, socioeconomic status,insurance coverage, and availability of care? Second, does thisdiscrepancy in part explain the differences in survival betweenblack patients and white patients with lung cancer? To answerthese questions, we chose a setting and design that mitigatedthe effect of the confounding factors. We proposed two hypotheses:that black patients would receive surgical treatment less frequentlythan white patients and that differences in survival betweenblack patients and white patients would be substantially explainedby the difference in the rates of surgical treatment.
Methods
Sources of Data
We tested our hypotheses with the use of data from the Surveillance,Epidemiology, and End Results (SEER) cancer registries thathave been linked with data on Medicare hospitalizations. TheSEER–Medicare data base has been used extensively to assesspatterns of care for persons with new diagnoses of cancer.5,6The SEER registries, sponsored by the National Cancer Institute,list all incident cases of cancer in five metropolitan areas(San Francisco–Oakland–San Jose, Detroit, Atlanta,Seattle, and Los Angeles County) and five states (Connecticut,Utah, New Mexico, Iowa, and Hawaii) and cover approximately14 percent of the population of the United States.7 These datacontain information on each newly diagnosed case of cancer,including the month and year of the diagnosis; the location,histologic type, nodal involvement, and spread of the tumor;and the type of treatment provided within four months afterdiagnosis (e.g., surgery or radiation). The site of cancer iscoded in the SEER data according to the International Classificationof Diseases for Oncology, 2nd edition (ICD-O-2).8
The Medicare program, which provides health care coverage for97 percent of persons 65 years of age or older, collects claimsfor all services covered by the program. Information about hospitalizationsis included in the Medicare Provider Analysis and Review (MEDPAR)files, which contain information on all hospital admissionssince 1984. Medicare also maintains files that document thedates of death of beneficiaries and whether they were coveredby a traditional indemnity program or by a health maintenanceorganization (HMO).
The SEER and Medicare data bases have been linked in order topermit population-based studies of health outcomes. The dataon 94 percent of the persons included in the SEER files whoare 65 years of age or older have been successfully linked toMedicare records.7 Focusing on this group of people who wereeligible for Medicare led to the exclusion of the 44 percentof patients in the SEER data base who received diagnoses oflung cancer before the age of 65 years, but this allowed usto adjust for coexisting conditions, eliminated the confoundingeffects of insurance coverage, and provided sufficient geographicspecificity to allow us to control for the availability of healthcare.
Study Participants
The subjects were persons with a form of lung cancer for whichsurgical resection has been shown to confer a definitive benefit— stage I or stage II non–small-cell lung cancer.9We included all patients classified as non-Hispanic white orblack who were 65 years of age or older, who resided in 1 ofthe 10 SEER areas, and who were given a diagnosis between 1985and 1993 of primary cancer of the lung, non–small-cellhistologic type (SEER codes 34.0 to 34.9 and ICD-O-2 morphologycodes 8010 to 8040, 8050 to 8076, 8140, 8250 to 8260, 8310,8320, 8323, 8430, 8470 to 8490, 8550 to 8573, 8980, and 8981);there were a total of 59,365 patients.
From this group we excluded patients who had not undergone acomplete evaluation to determine the stage of disease —that is, those for whom there was either no documentation orincomplete documentation with regard to tumor size, spread,or nodal involvement in the SEER data base (21,006 patients[35.4 percent]). We then identified patients with stage I orstage II disease (12,900 patients) according to the stagingsystem of the American Joint Committee on Cancer,10,11 usingthe information in the SEER data base on size, spread, and nodalinvolvement of the tumor. The definitions of these stages wereconstant throughout the study period. We then excluded patientsfor whom diagnoses were obtained from death certificates orat autopsy (127 patients [1.0 percent]) and those in whom asecond cancer was diagnosed within two months of the primarylung cancer (1789 patients [13.9 percent]), leaving a cohortof 10,984.
Surgical Treatment and Survival after Diagnosis
Patients were considered to have undergone surgical resectionif the variable for site-specific surgery in the SEER data baseindicated that a procedure that was curative in intent had beenperformed. Such procedures included local resection, wedge resection,segmentectomy, lobectomy, sleeve resection, partial pneumonectomy,and radical pneumonectomy (SEER codes 10 to 70). The month andyear of diagnosis were documented in the SEER data base; foranalytic purposes, we assumed that the diagnosis was made onthe first day of the month. Dates of death were obtained fromMedicare, which receives this information from the Social SecurityAdministration. All records of death are complete through December31, 1994, which was therefore chosen as the date of data censoringfor patients who were last known to be alive.
Characteristics of the Participants
Demographic Characteristics and Coexisting Illnesses
Information on the sex of the patients was obtained from Medicarerecords, and information on race and age at diagnosis was obtainedfrom the SEER data base. The socioeconomic status of each patientwas estimated on the basis of Medicare data on the median incomefor the ZIP Code of the patient's residence. This variable wasnecessarily an aggregate measurement of income, as opposed toa factor that reflected socioeconomic status on an individualbasis. We constructed two strata: one containing the patientswho resided in areas in the lowest quartile of median income,and the other containing the remaining patients.
The burden of coexisting illness was determined with the useof MEDPAR inpatient records through an examination of all hospitaladmissions occurring within the 12-month period before the monthof diagnosis. We calculated two indexes of coexisting illnessfor each patient: one according to the method suggested by Romanoet al.,12 in which the maximal Charlson comorbidity index13was calculated on the basis of inpatient records during thisperiod and the other according to the total number of hospitaladmissions during this period. In order to calculate these twoindexes, we needed one year of recorded Medicare data beforediagnosis. We therefore calculated the comorbidity indexes andconducted the adjusted analyses only for patients who at thetime of diagnosis were 66 years of age or older and were coveredby traditional indemnity insurance, since Medicare does notcollect data on hospitalization for persons in HMOs (84 percentof the total sample of 10,984). The Romano–Charlson indexcould not be determined for patients without a hospitalizationduring this period.
Access to Care
All patients were insured by Medicare. We assigned each patientthe coverage (HMO or indemnity) that he or she had during themonth in which the diagnosis was made. To assess the local availabilityof care, we used the health care service areas defined by theHealth Resources and Services Administration. These areas representregions with certain characteristics of health care availability,and they have been used in other studies of the availabilityof health care.14,15 The areas range in size from parts of acity to substantial portions of less populous states. The healthcare service area corresponding to each patient's area of residencewas documented in the SEER data base — our 10,984 studyparticipants resided in 80 health care service areas. To determinewhether some of our findings could be related to variationsin the local availability of health care services, we lookedfor heterogeneity in our findings with respect to the healthcare service areas and SEER areas.
Statistical Analysis
We assessed the association between the race of the patientsand the receipt of surgical treatment by comparing the overallrates of resection (among black patients as compared with whitepatients) for the entire cohort; by comparing the resectionrates between black patients and white patients within relevantsubgroups, such as those defined by age, comorbidity index,and area of residence; by determining the effect of race onthe receipt of surgical treatment while controlling for otherimportant factors, such as sex, median income in the ZIP Codeof residence, age, stage of disease, and comorbidity (one ofthe two measures); and by determining whether the disparitiesin resection rates were consistent with respect to the SEERarea (with use of the Breslow–Day test for heterogeneity),health care service area (with use of the Mantel–Haenszeltest for heterogeneity), and study year (with use of the Mantel–Haenszeltest).16
Survival curves were constructed with the Kaplan–Meiermethod and compared with use of the log-rank statistic.17 Foranalyses involving adjustments for potential confounding factors,we used the Cox proportional-hazards method.17 All P valuesare two-sided. All analyses were performed with SAS software(version 6.12, SAS Institute, Cary, N.C.). The estimated survivalbenefit under a scenario in which black patients received surgicaltreatment at a rate identical to that of white patients is basedon the estimated survival probabilities derived from the observedpopulation.
Results
Characteristics of the Study Participants
There were 10,984 patients in this study; 860 (8 percent) wereblack, and 10,124 (92 percent) were non-Hispanic white (Table 1).There were no substantial differences between the two groupswith respect to the stage of disease, type of insurance, numberof hospitalizations in the 12 months before the diagnosis, orthe Romano–Charlson comorbidity index. Black patientswere slightly younger and somewhat more likely to be men. Themost important disparity between the two groups was that blackpatients were substantially more likely to reside in a ZIP Codearea with a low median income. Also, the distribution of patientsamong the SEER areas differed between the two groups.
Table 1. Characteristics of Black and White Medicare Beneficiaries 65 Years of Age or Older with Stage I or II Non–Small-Cell Lung Cancer, 1985 to 1993.
Resection Rates and Association with Survival
Black patients and white patients who underwent surgery hadroughly similar rates of survival at five years — 39.1percent among black patients and 42.9 percent among whites (P=0.10)(Figure 1). Those who did not undergo surgery also had similarfive-year survival rates (4 percent among blacks and 5 percentamong whites, P=0.25) (Figure 1). However, 76.7 percent of thewhite patients underwent surgery, whereas only 64.0 percentof the black patients received this treatment (P<0.001) (Table 2).The combination of discrepant resection rates and similarsurvival rates after treatment contributed to a substantialdifference in the overall survival rates, as shown in Figure 2.
Figure 1. Survival of Medicare Beneficiaries 65 Years of Age or Older Who Were Given a Diagnosis of Stage I or II Non–Small-Cell Lung Cancer between 1985 and 1993, According to Treatment and Race.
Figure 2. Survival of Medicare Beneficiaries 65 Years of Age or Older Who Were Given a Diagnosis of Stage I or II Non–Small-Cell Lung Cancer between 1985 and 1993, According to Race.
We diagrammed the effect of these results in a hypotheticalcohort of 1000 white patients and 1000 black patients (Figure 3):76.7 percent of the whites underwent surgery, and 42.9 percentof these patients survived for five years, whereas only 5.2percent of the remaining 23.3 percent of patients who did notreceive surgical treatment survived for that long. Thus, overall,341 patients (34.1 percent) were alive at five years. In contrast,of the 1000 black patients, only 264 patients were alive atfive years — 77 (7.7 percent) fewer than in the whitecohort. Two factors are responsible for this difference: thelower rate of resection among blacks (64.0 percent, vs. 76.7percent among whites) and the slightly (though nonsignificantly)lower five-year survival rate after surgery among blacks (39.1percent vs. 42.9 percent). If black patients had undergone surgeryat a rate similar to that for white patients, we estimate that308 black patients would have been alive at five years, a numberonly 3.3 percent lower than that for whites. These figures suggestthat of the 77 more deaths per 1000 black patients, the majority(44) can be attributed to the failure to provide surgical treatmentfor a curable disease.
Figure 3. Relation between the Rate of Surgical Resection for Stage I or II Non–Small-Cell Lung Cancer and Five-Year Survival in Hypothetical Cohorts of 1000 Black and 1000 White Medicare Beneficiaries 65 Years of Age or Older.
If 76.7 percent of the black patients had undergone surgery, 308 of them would be expected to be alive five years after diagnosis.
Stratified and Adjusted Analyses
We performed a number of stratified and adjusted analyses totest the robustness of these results. The pivotal disparityin rates of resection was evaluated in several important subgroups(Table 2). The results show that the lower resection rate amongblack patients was consistent. In addition, we found no evidencethat the disparity in resection rates differed according tothe health care service area (P=0.85) or SEER area (P=0.64)or that the overall resection rate or the disparity in resectionrates varied during the years of the study (P=0.62) (data notshown).
The disparity also persisted in two multivariable logistic-regressionanalyses in which we controlled for age, sex, stage of disease,median income in the ZIP Code of residence, and coexisting illness,as measured by either the Romano–Charlson index or thenumber of hospitalizations in the previous year. On the basisof these analyses, the odds ratios for undergoing surgery amongblack patients, as compared with white patients, were 0.54 whenthe Romano–Charlson index was used as a measure of coexistingillness and 0.53 when the number of hospitalizations was used— findings that were consistent with the unadjusted oddsratio of 0.52. The results of all the analyses support the hypothesisthat race is an important independent factor in determiningthe likelihood that a patient with early-stage, non–small-celllung cancer will receive surgical treatment.
The observed similarities in survival among black patients andwhite patients after either receiving or not receiving surgicaltreatment were also evaluated in analyses adjusted for factorspreviously identified as affecting survival. These analysesshowed a slightly increased risk of death among black patientsafter surgery (relative risk, 1.10; P=0.18) and a slightly decreasedrisk of death for black patients who did not undergo surgery(relative risk, 0.84; P=0.02) (Table 3). The analyses also confirmedthat in this cohort, residence in an area with a lower medianincome, male sex, older age, a higher stage of disease, andmore coexisting illness all conferred an increased risk of death,regardless of treatment.
Table 3. Effect of Race and Other Factors on Survival among Patients Who Underwent Surgery and Those Who Did Not.
Discussion
The optimal treatment for early-stage, non–small-celllung cancer is surgical resection — a treatment with asubstantial cure rate.9,18,19 In this study, we determined whetherthe rate of surgical treatment for stage I or stage II non–small-celllung cancer was lower for black patients 65 years of age orolder than it was for white patients in the same age group.Then we compared the survival rates between black patients andwhite patients who had undergone surgery and between black patientsand white patients who had not undergone surgery. Using severalanalytic techniques to control for the confounding effects ofdisease stage, type of insurance coverage, availability of care,socioeconomic status, age, and coexisting illnesses, we foundthat black patients were less likely than white patients toundergo surgical resection (a difference of 12.7 percentagepoints). Both unadjusted and adjusted analyses showed that blackpatients who underwent surgical resection had a five-year survivalrate similar to that of white patients who underwent resection,and we estimated that of the 77 more deaths per 1000 black patients,the majority (44) could be attributed to the lack of surgicaltreatment.
If black patients were to undergo surgery at a rate equal tothat of white patients, their survival rate would probably besubstantially improved and would approach that of white patients.Given equal rates of resection, we estimate that there wouldbe a 3.3 percent discrepancy in survival at five years (341survivors among 1000 white patients vs. 308 among 1000 blackpatients). The survival curves shown in Figure 2 for black patientsand white patients after surgery suggest a similar conclusion:given equal treatment, black patients will have a survival ratethat is only marginally lower than that for white patients.The small disparity in survival between black patients and whitepatients with equal resection rates is not surprising, evenif surgery confers an equal benefit in each group. The actuarialdata (deaths due to all causes) in the same population showa larger gap: on average, a 73-year-old black person has a 76percent likelihood of survival for five years, as compared with81 percent for a 73-year-old white person.20
These results should be viewed with caution. We focused on Medicarebeneficiaries who were 65 years of age or older, and it is notclear whether there is similar variability in the care providedto younger patients with lung cancer. In addition, in all thepatients in our study, the diagnosis of non–small-celllung cancer and the stage of disease had been established, whichmeant that all the patients had had extensive involvement withthe health care system. Our study did not address the care receivedby patients who present with advanced disease or those in whomthe stage of disease has not been determined. Two other factorsthat we did not investigate also increase mortality due to non–small-celllung cancer in black persons. The annual incidence of non–small-celllung cancer in this population of people who are 65 years ofage or older is higher among black persons (359 per 100,000population) than among white persons (294 per 100,000).21,22Also, among persons 65 years of age or older in whom the stageof disease is determined at the time of diagnosis, the SEERdata show that black patients are less likely than white patientsto have resectable (i.e., stage I or II) disease (27 percentvs. 31 percent) (unpublished data).
In this study, we were also limited in our ability to make adjustmentsfor two factors that might have influenced the interpretationof our results. We used an aggregate measure of income as asurrogate for the socioeconomic status of each patient. Someinvestigators have argued that our aggregate measure is an adequatesurrogate marker for socioeconomic status,23 but others haveargued that the optimal socioeconomic variable is at the levelof the patient, not at the level of the community.24 Therefore,we cannot be sure that we have separated the effects of racefrom those of socioeconomic status.
In addition, we could not ascertain the Romano–Charlsoncomorbidity index for the 76 percent of our patients who werenot hospitalized in the year before the diagnosis. However,it seems unlikely that this lack has led us to make incorrectconclusions, for three reasons. First, in the 24 percent ofpatients in whom we could evaluate coexisting illness in termsof the Romano–Charlson comorbidity index, the disparityin treatment was consistent. Second, most clinicians would agreethat, barring the presence of severe pulmonary disease, a patientwho had not required hospitalization for a year could probablytolerate a thoracotomy and partial lung resection.25 Third,we can predict that the bias we may have introduced by usingthis measure of coexisting illness would, if anything, haveled us to underestimate the disparity in treatment between blackand white patients. Specifically, for chronic diseases thatare responsive to outpatient management, such as chronic obstructivepulmonary disease, blacks are more likely than whites to behospitalized for the same degree of illness, thus increasingour estimate of the burden of coexisting illness among blacks.25,26
Variations in the care of patients with similar diseases havebeen observed since Wennberg and Gittelsohn first called attentionto the phenomenon in 1973.27 Unlike the treatments under scrutinyin many other studies, the optimal strategy for the treatmentof early-stage, non–small-cell lung cancer is unambiguous:surgical resection confers a meaningful probability of cure,whereas other therapies do not. We cannot determine from ourdata why black patients have a lower rate of resection thantheir white counterparts, but we can conclude that the differencein treatment has a substantial effect on survival. Others haveargued that the preferences of black patients may differ fromthose of white patients or that black patients may weigh therisks of surgical therapy differently.28,29 An alternative explanationis that black patients are offered optimal treatment less frequentlythan their white counterparts.30 These are certainly issuesworthy of investigation in future studies.
We are indebted to the Applied Research Branch, Division ofCancer Prevention and Population Science, National Cancer Institute;to the Office of Information Services and the Office of StrategicPlanning, Health Care Financing Administration; to InformationManagement Services; and to the SEER program. The interpretationand reporting of the data from the linked SEER–Medicaredata base are the sole responsibility of the authors.
Source Information
From the Health Outcomes Research Group, Department of Epidemiology and Biostatistics (P.B.B., L.D.C., C.B.B.), and the Department of Medicine, Pulmonary Service (P.B.B.), Memorial Sloan-Kettering Cancer Center, New York; and the Applied Research Branch, National Cancer Institute, Bethesda, Md. (J.L.W.).
Address reprint requests to Dr. Bach at the Health Outcomes Research Group, Department of Epidemiology and Biostatistics, Memorial Sloan-Kettering Cancer Center, 1275 York Ave., Box 221, New York, NY 10021.
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Garner, E. I. O.
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