Background Women without private health insurance are less likelythan privately insured women to be screened for breast cancer,and their treatment may differ after cancer is diagnosed. Inthis study we addressed two related questions: Do uninsuredpatients and those covered by Medicaid have more advanced breastcancer than privately insured patients when the disease is initiallydiagnosed? And, for each stage of disease, do uninsured patientsand patients covered by Medicaid die sooner after breast canceris diagnosed than privately insured patients?
Methods we studied 4675 women, 35 to 64 years of age, in whominvasive breast cancer was diagnosed from 1985 through 1987,by linking New Jersey State Cancer Registry records to hospital-dischargedata. We compared the stage of disease and stage-specific survivalamong women with private insurance, no insurance, and Medicaidcoverage through June 1992. We also estimated the adjusted riskof death for these groups, using proportional-hazards regressionanalysis to control for age, race, marital status, householdincome, coexisting diagnoses, and disease stage.
Results Uninsured patients and those covered by Medicaid presentedwith more advanced disease than did privately insured patients(P<0.001 and P = 0.01, respectively). Survival was worsefor uninsured patients and those with Medicaid coverage thanfor privately insured patients with local disease (P<0.001for both comparisons) and regional disease (P<0.001 for bothcomparisons), but not distant metastases. The adjusted riskof death was 49 percent higher (95 percent confidence interval,20 to 84 percent) for uninsured patients and 40 percent higher(95 percent confidence interval, 4 to 89 percent) for Medicaidpatients than for privately insured patients during the 54 to89 months after diagnosis.
Conclusions The more frequent adverse outcomes of breast canceramong women without private health insurance suggest that suchwomen would benefit from improved access to screening and optimaltherapy.
Access to health care is currently a subject of considerableconcern in the United States. Approximately 34 million Americanslack health insurance,1 and many of them may delay or forgonecessary medical care because of its cost2. People withouthealth insurance receive fewer inpatient and outpatient medicalservices than those with insurance,3,4,5,6,7 and the qualityof hospital care may also be lower for uninsured patients8.The Medicaid program has improved access for poor people whoqualify,9 but Medicaid enrollees are less likely than privatelyinsured patients to have a personal physician10 and less likelyto undergo certain major procedures4,6. Medicaid enrollees oftenhave limited access to office-based physicians, in part becauseMedicaid's payment rates are lower than those of other insuranceprograms11,12.
Although there is substantial evidence that the receipt of healthservices varies according to insurance coverage, only a fewstudies have demonstrated a link between insurance coverageand health outcomes13,14,15,16,17. If insurance coverage isassociated with differences in outcome, the relation is mostlikely to be evident for potentially severe illnesses that canbe diagnosed and treated effectively early in their course.A plausible example is breast cancer. This disease causes theloss of more years of potential life among women under 65 yearsof age than any other nontraumatic condition in the United States,18yet it is curable if detected early. Screening with breast examinationsand mammography improves survival for women 50 years of ageand older, and possibly for women 40 to 49 years old as well19,20.
National surveys have demonstrated that women without privateinsurance are less likely than privately insured women to receivecancer-screening services21,22,23. Hospitals that care for largenumbers of uninsured patients and Medicaid enrollees may undertakeless thorough staging of breast cancer,24 and patients withoutprivate health insurance may be treated less vigorously aftercancer is diagnosed25. In this study we posed two questionsarising from these differences in care: Do uninsured patientsand those covered by Medicaid have more advanced breast cancerthan privately insured patients when the disease is first diagnosed?And do these patients die sooner, on average, than privatelyinsured patients during the 7.5 years after breast cancer isdiagnosed?
Methods
Data Sources
The New Jersey State Cancer Registry was established withinthe New Jersey Department of Health as a population-based incidenceregistry for all new cases of cancer among New Jersey residents,beginning in October 197826. State regulations require thathospitals, physicians, dentists, and clinical laboratories reportcases of cancer within six months of diagnosis. Residents whosecancer is diagnosed in hospitals outside the state are identifiedthrough agreements with neighboring states. Survival data areobtained by registry staff through regular contact with reportinghospitals and physicians and by reviews of state death, motor-vehicle,and income-tax records. In addition, data on patients with cancerare regularly matched to the National Death Index, as was donemost recently in July 1990 for deaths during 1987 and 1988.New Jersey also requires that hospital-discharge abstracts bereported for all hospitalizations for acute care in the state.Therefore, by linking registry records to discharge abstracts,we were able to analyze clinical outcomes for individual patientsaccording to their insurance coverage.
The study protocol was approved by the institutional reviewboard of the New Jersey Department of Health. Data obtainedfrom the registry included age; race (white, black, or other,including American Indian, Asian, and unknown); marital status(married or unmarried, including single, widowed, divorced,and separated); census tract and ZIP Code of residence; datesof diagnosis, last contact, and death, if applicable, throughJune 1992; the reporting facility; and the summary disease stageat diagnosis. The summary stage was defined as "local" if thetumor was confined to the breast; "regional" if disease hadspread to axillary or internal mammary lymph nodes, the chestwall, subcutaneous tissue, or overlying skin; and "distant"if disease had spread beyond these sites27.
From 1984 through 1988, 4 of the 21 counties in New Jersey (Essex,Hudson, Passaic, and Union) were included in the Surveillance,Epidemiology, and End Results (SEER) Program of the NationalCancer Institute. For residents of these counties, more detaileddata were collected about the primary tumor and metastases,allowing more precise classification of disease stage (I, IIA,IIB, IIIA, IIIB, or IV)28. Stage I disease includes tumors 2cm or less in the longest dimension, without metastasis. StageIIA includes tumors 2 cm or less with metastasis to movableaxillary lymph nodes and tumors larger than 2 cm but no morethan 5 cm without metastasis. Stage IIB includes tumors largerthan 2 cm but no more than 5 cm with metastasis to movable axillarynodes and tumors larger than 5 cm without metastasis. StageIIIA includes tumors of any size with metastasis to fixed axillarynodes and tumors greater than 5 cm with metastasis to movableaxillary nodes. Stage IIIB includes all tumors with direct extensionto the chest wall or skin or with metastasis to ipsilateralinternal mammary nodes, but no distant metastasis. Stage IVincludes all tumors with distant metastasis.
Abstracts of hospital discharges are maintained by Medix Managementsystems, a subsidiary of Blue Cross-Blue Shield of New Jersey.These abstracts include up to nine diagnoses from the InternationalClassification of Diseases, 9th Revision, Clinical Modification(ICD-9-CM). We obtained abstracts for all hospital dischargeswith a principal diagnosis of cancer from 1984 through 1988.From these abstracts we identified insurance coverage (privateinsurance, including Blue Cross, commercial plans, and healthmaintenance organizations; no insurance, a category that includedindigent and self-paying patients; or Medicaid) and the numberof coexisting diagnoses, excluding those related to the breasts(ICD-9-CM codes 174.0 through 174.9, 217, 233.0, 238.3, 239.3,610.0 through 611.9, and V10.3), lymph nodes (codes 196.0 through196.9 and 785.6), and metastatic cancer (codes 197.0 through199.1).
Neither registry records nor discharge abstracts included patients'incomes, so we obtained data on median household income accordingto census tract and ZIP Code for New Jersey from the 1980 U.S.Census. These data were provided by the Princeton UniversityComputing Center.
Patient Population
We identified women residing in New Jersey who were 35 to 64years of age, in whom invasive carcinoma of the breast was diagnosedduring 1985 through 1987, whose cases were reported to the NewJersey State Cancer Registry. We chose 35 years of age as alower limit because no major organizations in the United Statesrecommend routine screening with mammography before this age29.We chose the age of 64 as an upper limit because almost allwomen qualify for Medicare coverage at age 65, so relativelyfew older women remain uninsured or covered solely by Medicaid.
A total of 7290 women in this age group were given a diagnosisof invasive breast cancer from 1985 through 1987. Because wewere interested in the outcomes according to disease stage atdiagnosis and in subsequent survival, we excluded 607 womenwhose disease stage was not reported to the registry. We alsoexcluded 657 women reported to the registry by hospitals inother states. These hospitals do not send discharge abstractsto New Jersey, so the type of insurance coverage was unknownfor these patients. Therefore, 6026 women were eligible forthe study. The women who were excluded were slightly youngerthan the eligible women (mean age, 51.8 vs. 52.8 years; P<0.001by t-test), but similar in race (86.9 percent vs. 85.8 percentwhite, P>0.10 by the chi-square test) and marital status(62.7 percent vs. 65.0 percent married, P>0.10). Women whosecases were reported by hospitals in other states were more likelyto have local disease than women whose cases were reported byhospitals in New Jersey (60.6 percent vs. 53.4 percent, P<0.001).
Data Linkage
Registry records were linked to hospital-discharge abstractsat the New Jersey Department of Health, according to the patient'ssurname, first initial, and date of birth. To minimize the effectof spelling variations, surnames were characterized phoneticallywith use of a version of the New York State Identification andIntelligence System previously modified for the SEER Program.Matches were characterized as definite if the names and datesof birth were identical in both records or probable if the nameswere the same and the dates of birth were within two years.The patients' names were deleted from all records before thedata were analyzed.
A definite or probable match between the registry record andat least one discharge abstract was obtained for 5120 eligiblewomen (85.0 percent). The women whose registry records werenot matched to discharge abstracts were similar to the womenwith matched records in terms of age (mean, 53.2 vs. 52.7 years;P = 0.08 by t-test), race (85.8 percent vs. 86.2 percent white,P>0.10 by the chi-square test), and marital status (62.8percent vs. 65.4 percent married, P>0.10).
If a woman had more than one discharge abstract matched to herregistry record, we selected the abstract for the admissionoccurring closest (within 90 days) to the date of diagnosislisted in the registry. For 160 women, the nearest matched abstractwas for an admission more than 90 days before or after diagnosis.We did not analyze the data on these women because the primarypayer at the time of the admission may not have reflected theirinsurance status at the time of diagnosis. We also did not analyzedata on 285 women with primary insurance other than the threetypes of interest, such as Medicare or CHAMPUS.
The final cohort was composed of 4675 women, including 4413with a definite match between registry and discharge recordsand 262 with a probable match. The study population included277 uninsured patients (5.9 percent) and 115 patients coveredby Medicaid (2.5 percent), comparable to the overall proportionsof 6.6 percent and 3.6 percent, respectively, among adults 45to 64 years of age in the Northeast1. For these 4675 women,we linked 1980 Census data on median household income to registryrecords for the smallest residential area in which they couldbe categorized; this was the census tract for 76.0 percent ofpatients and the ZIP Code for all but 8 of the remaining patients.The patient group was divided in thirds according to annualhousehold income, defined as low ($4,175 to $18,478), intermediate($18,485 to $24,992), or high ($25,000 to $59,390). Becauseall patients were assigned the median income of their communities,a few Medicaid patients living in wealthier communities appearedto be relatively affluent.
Statistical Analysis
Our analysis had three parts. First, we compared the stage ofdisease at the time of diagnosis among uninsured and Medicaidpatients separately with the stage of disease among privatelyinsured patients, using the Wilcoxon rank-sum test. Second,we constructed stage-specific survival curves according to insurancecoverage, by the Kaplan-Meier method. The length of time fromdiagnosis to death or the last follow-up contact was measuredin months. The duration of potential follow-up for any individualpatient ranged from 54 to 89 months, depending on the date ofdiagnosis, and follow-up was shorter for some patients who werenot known to have died. Mortality from all causes was incorporatedinto the survival estimates. We compared survival curves withthe Mantel-Cox log-rank test. To present the data consistentlyfor each stage, we have displayed survival curves through 72months after the diagnosis in our figures.
In the third part of our analysis, we estimated the adjustedrisk of death among uninsured and Medicaid patients as comparedwith privately insured patients, using Cox proportional-hazardsregression analysis. We used continuous variables for age andmedian household income and dummy variables for insurance coverage,race, marital status, the number of coexisting diagnoses (1,2, 3, 4, 5, or 6), and the stage of disease at diagnosis. Becauseof potential age-related differences in the biology of breastcancer, we also performed stratified analyses of disease stageand adjusted risk of death among women 35 to 49 years old and50 to 64 years old.
To determine whether more precise staging might alter the findingsof the primary analysis, we performed a secondary analysis ofwomen in the four counties covered by the SEER Program (n =1464). Among these women, more detailed data on the extent ofdisease were available for 1086 (74.2 percent). In this groupwe analyzed the stage of disease and the adjusted risk of deathaccording to insurance coverage by the methods described above.Because few patients were categorized as having stage IIIA orIIIB disease at presentation, we combined these two groups inthe analysis (stage III).
All analyses were conducted with SAS statistical software30,31.We report 95 percent confidence intervals for the adjusted relativerisks of death derived from the proportional-hazards regressionanalyses and two-tailed P values for all other tests.
Results
The characteristics of the women in the three insurance categoriesare presented in Table 1. As compared with women with privateinsurance, uninsured women and women covered by Medicaid wereyounger, less likely to be white, less likely to be married,and more likely to be living in poor communities; both groupsalso had more coexisting diagnoses than privately insured womenduring the initial hospitalization.
Table 1. Characteristics of Women in New Jersey, 35 through 64 Years of Age, in Whom Invasive Breast Cancer Was Diagnosed in 1985 through 1987, According to Insurance Coverage.
Uninsured women and women covered by Medicaid had significantlymore advanced disease than privately insured women when theirdisease was initially diagnosed, as indicated by the summarystage of disease for all women in the state (Table 2). Whenwe stratified the population according to age, significantlymore advanced disease was present among uninsured women 50 to64 years of age (P<0.001) and among women covered by Medicaidwho were 35 to 49 years of age (P = 0.02) than among women withprivate insurance in the same age groups. Nonsignificant trendstoward more advanced disease were noted among uninsured women35 to 49 years of age (P = 0.16) and among women covered byMedicaid who were 50 to 64 years of age (P = 0.21). In the secondaryanalysis of the four counties in the SEER Program, in whichmore precise staging was recorded, uninsured women and womencovered by Medicaid also had significantly more advanced diseasethan privately insured women (Table 3).
Table 2. Summary Stage of Breast Cancer at Diagnosis, According to Insurance Coverage, in Women 35 through 64 Years of Age, in All New Jersey Counties, 1985 through 1987.
Table 3. Stage of Breast Cancer at Diagnosis, According to Insurance Coverage, in Women 35 through 64 Years of Age, in Essex, Hudson, Passaic, and Union Counties, 1985 through 1987.
Survival during the 54 to 89 months after diagnosis was significantlyworse for uninsured patients and those covered by Medicaid thanfor privately insured patients with local disease (P<0.001for both comparisons) (Figure 1). Survival was also significantlyworse for uninsured patients and those covered by Medicaid whohad regional disease (P<0.001 for both comparisons) (Figure 2).Survival did not differ significantly according to insurancecoverage in patients with distant metastases at presentation(P>0.10 for all comparisons) (Figure 3). Survival also didnot differ significantly between uninsured and Medicaid patientswith any of the three stages of disease (P 0.10 for all comparisons).
Figure 1. Kaplan-Meier Survival Estimates According to Insurance Coverage for Women 35 through 64 Years of Age in Whom Local-Stage Breast Cancer Was Diagnosed in New Jersey, 1985 through 1987.
Figure 2. Kaplan-Meier Survival Estimates According to Insurance Coverage for Women 35 through 64 Years of Age in Whom Regional-Stage Breast Cancer Was Diagnosed in New Jersey, 1985 through 1987.
Figure 3. Kaplan-Meier Survival Estimates According to Insurance Coverage for Women 35 through 64 Years of Age in Whom Distant-Stage Breast Cancer Was Diagnosed in New Jersey, 1985 through 1987.
In the primary multivariate analysis of all patients, both uninsuredpatients and patients covered by Medicaid had a higher adjustedrisk of death than privately insured patients (Table 4). Whenwe stratified this analysis according to age, using privatelyinsured patients as the reference group, the adjusted risk ofdeath was significantly greater for uninsured patients 35 to49 years of age (relative risk, 1.57; 95 percent confidenceinterval, 1.11 to 2.24), uninsured patients 50 to 64 years ofage (relative risk, 1.43; 95 percent confidence interval, 1.10to 1.86), and patients with Medicaid coverage 35 to 49 yearsof age (relative risk, 1.59; 95 percent confidence interval,1.02 to 2.49), but not for Medicaid enrollees 50 to 64 yearsof age (relative risk, 1.28; 95 percent confidence interval,0.84 to 1.94). When more precise staging was used in the secondaryanalysis of patients in the SEER Program, the adjusted riskof death was significantly greater for both uninsured patientsand patients with Medicaid coverage than for privately insuredpatients (Table 4).
Table 4. Adjusted Relative Risk of Death among Uninsured Women and Women Covered by Medicaid, as Compared with Privately Insured Women.
Discussion
In this study women without health insurance and those coveredby Medicaid had more advanced breast cancer than women withprivate health insurance when the disease was initially diagnosed.The survival of those women was also worse than that of privatelyinsured women with local and regional disease, and the associationof insurance coverage with survival persisted in a multivariateanalysis in which adjustment was made for numerous potentialconfounders.
Reduced access to care may be an important reason for the moreadvanced disease of uninsured patients and patients coveredby Medicaid. Such patients are less likely than privately insuredpatients to have a primary care physician who can ensure thatthey are screened for cancer10. Having a primary care physicianis strongly associated with the use of mammography,32,33 anda physician's recommendation is the most important factor promptingwomen to undergo mammographic screening34,35.
Less complete staging among uninsured and Medicaid patientscould produce the appearance of worse stage-specific survival,even in the absence of true differences. In one study, for example,hospitals that cared for large numbers of uninsured patientsand patients covered by Medicaid were less likely than othersto evaluate hormone receptors in cancerous breast tissue24.However, if uninsured patients and those covered by Medicaidundergo less complete staging, then we have underestimated theirmore advanced disease stage at diagnosis. Incomplete stagingmay also lead to inadequate therapy.
Differences in treatment may contribute to the worse survivalof patients without private health insurance. In a study oflung cancer, patients without private insurance were less likelythan privately insured patients to undergo surgery, chemotherapy,or radiation therapy25. Although the subsequent survival ofthe two groups did not differ, treatment differences could bemore consequential for conditions such as breast cancer thatare more frequently detected at an early stage.
Lead-time bias is a possible explanation for the better survivalof privately insured patients. If their disease is diagnosedsooner (i.e., with a longer lead time) within each stage thanthat of uninsured patients and patients with Medicaid coverage,their subsequent survival could appear to be longer, even ifearlier treatment is not prolonging their lives. Length-timebias is another possible explanation. Higher screening ratesamong privately insured women may lead to the detection of cancersthat spread more slowly (i.e., take longer to become symptomatic)and are less likely to be lethal within a given stage36. Thesepotential biases can be evaluated in randomized trials,19,20,37but we cannot evaluate their effects with our observationaldata.
Health insurance may be a proxy for other socioeconomic factorsthat influence outcomes. Several studies have documented moreadvanced breast cancer and worse survival among patients oflower socioeconomic status, but the causes of these patternsare not well defined38,39,40,41,42,43. Women without privateinsurance may be less aware than privately insured women ofscreening services, including self-examination44. Even whenaccess to medical services is provided, poorer patients mayuse such services less regularly because they may deny the existenceof symptoms or distrust the medical system; the result wouldbe worse survival, as is seen in women who decline screeningin randomized trials19,37. Differences in the availability ofsocial support may have a role45,46,47. Other factors affectingoutcomes, such as obesity and alcohol intake, may also be associatedwith insurance coverage.
The comparable outcomes of uninsured patients and patients coveredby Medicaid suggest that Medicaid coverage alone -- withoutefforts to enhance primary care and screening -- may be insufficientto improve outcomes for poor women with breast cancer. From1985 through 1987, New Jersey did not cover screening mammographyfor Medicaid enrollees, but it has since become 1 of 44 statesto provide this benefit48. Moreover, Medicaid coverage may havebeen discontinuous for some women, leaving them uninsured atkey times before or after cancer was diagnosed.
This study has several limitations. We have documented a clearassociation between insurance coverage and clinical outcomes,but the possibility of lead-time bias, length-time bias, andunmeasured confounding requires further investigation. Informationon income was available only according to census tract and ZIPCode. Some prognostic variables were also unavailable, suchas the number of positive lymph nodes and the presence or absenceof hormone receptors, and we did not analyze treatment, suchas the type of surgical procedure and whether postoperativeadjuvant therapy was used. Another possible limitation is dueto the exclusion of patients whose cases were reported by hospitalsoutside New Jersey. These women had less advanced disease thanthose treated at in-state hospitals, however, and they werelikely to be insured for out-of-state care. Therefore, includingthem would probably have reinforced our findings.
We conclude that women without private health insurance whohave breast cancer receive this diagnosis later and die soonerafter the diagnosis than privately insured women with breastcancer. Future research should evaluate potential reasons forthese disparities, including the factors that lead to delayin diagnosis and the subsequent quality of care. Comprehensiveprograms to improve access to early detection and optimal treatment49,50,51may yield substantial benefits.
Dr. Ayanian is a Medical Foundation-Charles A. King Trust ResearchFellow.
We are indebted to Krishna Bose, Dr.P.H., for initiating thelinkage of cancer-registry records and hospital-discharge abstracts;to Dolores Skolnick for assistance with computer programming;to Judith Rowe and Douglas Mills for providing census data;and to Anthony L. Komaroff, M.D., Barbara J. McNeil, M.D., Ph.D.,Jane C. Weeks, M.D., and Joel S. Weissman, Ph.D., for theirhelpful comments on the manuscript.
Source Information
From the Division of General Medicine, Section on Health Services and Policy Research, Department of Medicine, Brigham and Women's Hospital and Harvard Medical School, Boston (J.Z.A., A.M.E.); the Department of Health Care Policy, Harvard Medical School, Boston (J.Z.A., A.M.E.); and the State Cancer Registry, New Jersey Department of Health, Trenton (B.A.K., T.A.).
Address reprint requests to Dr. Ayanian at the Department of Health Care Policy, Harvard Medical School, 25 Shattuck St., Parcel B, 1st Fl., Boston, MA 02115.
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