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Differences in Treatment and Outcome Between African-American and White Women With Endometrial Cancer

Thomas C. Randall, Katrina Armstrong

From the Departments of Obstetrics and Gynecology and Medicine, and the Center for Clinical Epidemiology and Biostatistics, University of Pennsylvania School of Medicine; Abramson Cancer Center and Leonard Davis Institute of Health Economics, University of Pennsylvania; and Center for Health Equity Research and Promotion, Philadelphia, PA.

Address reprint requests to Katrina Armstrong, MD, MSCE, 1204 Blockley Hall, 423 Guardian Dr, Philadelphia, PA 19104-6021; e-mail: karmstro{at}mail.med.upenn.edu.

	ABSTRACT

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Purpose: To investigate disparities in treatment and outcomes between African-American and white women with endometrial cancer.

Patients and Methods: We analyzed 1992 to 1998 Surveillance, Epidemiology, and End Results data for 21,561 women with epithelial cancers of the endometrium. Sequential Cox proportional hazard models were used to determine the association between tumor characteristics (stage, grade, and histologic type), sociodemographic characteristics (age and marital status), and treatment (surgery and radiation therapy) and the racial difference in mortality.

Results: The unadjusted hazard ratio (HR) for death from endometrial cancer for African-American women compared with white women was 2.57. However, African-American women were significantly more likely to present with advanced-stage disease and have poorly differentiated tumors or tumors with an unfavorable histologic type and were significantly less likely to undergo definitive surgery at all stages of disease. Adjusting for tumor and sociodemographic characteristics lowered the HR for African-American women to 1.80. Further adjustment for the use of surgery reduced the HR to 1.51. The association between surgery and survival was stronger among white women (HR, 0.26) than among African-American women (HR, 0.44).

Conclusion: African-American women with endometrial cancer are significantly less likely to undergo primary surgery and have significantly shorter survival than white women with endometrial cancer. Racial differences in treatment are associated with racial differences in survival. The association between use of surgery and survival is weaker among African-American than white women, raising questions about potential racial differences in the effectiveness of surgery.

	INTRODUCTION

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SURVIVAL AFTER endometrial cancer diagnosis varies significantly between African-American and white women. Between 1992 and 1998, five year survival for African-American women with endometrial cancer was 58.9%, compared with 85.8% for white women.¹ Several factors are known to be associated with this racial disparity. Differences in stage, grade, and histology at presentation between African-American and white women have been documented in several studies.^2–8 Lower socioeconomic status and greater clinical comorbidity have also been found to contribute to worse outcomes among African-American women in some studies.^2–7 However, most studies suggest that substantial racial differences in survival persist after accounting for these factors.

Racial differences in treatment may contribute to racial differences in endometrial cancer survival. Many studies have documented substantial racial disparities in the types of treatment received for other cancers, including the use of radical prostatectomy for localized prostate cancer, surgical resection for early-stage lung cancer, and radiation therapy for localized breast cancer.⁹ In many settings, differences in treatment are clearly linked to differences in mortality. Hysterectomy with bilateral salpingo-oophorectomy is the mainstay of treatment for endometrial cancer without known distant metastases at presentation.^10,11 Pelvic and para-aortic lymph node sampling is frequently performed at the time of surgery.¹¹ In addition, adjuvant radiation therapy may be used for patients felt to be at significant risk for recurrence.^10,11 However, the effects of node sampling and adjuvant radiation therapy on survival are controversial.^10–14 Although several prior studies of endometrial cancer have examined differences in therapy between African-American and white women, most were conducted in the 1980s or before, included relatively few patients or centers, and did not specifically examine the relationship between racial differences in treatment and survival.^2,4,6,7 Thus the aim of this study was to investigate the association between differences in treatment and the observed disparity in endometrial cancer mortality among African-American and white women in the United States.

	PATIENTS AND METHODS

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Study Design
We analyzed data from Surveillance, Epidemiology, and End Results (SEER) on the cohort of women with incident cases of endometrial cancer between 1992 and 1998. The primary outcome was overall survival, with a mean follow-up of 35 months (range, 1 to 83 months). Our main exposures of interest were race and type of treatment.

Data Source
SEER is a population-based national cancer registry that encompasses 11 registries, including the states of Utah, Hawaii, Iowa, New Mexico, and Connecticut and the metropolitan areas of Detroit, San Francisco/Oakland, Seattle, Atlanta, San Jose/Monterey, and Los Angeles. The SEER cachement area is estimated to include more than 10% of the United States population. In SEER, cancer cases are primarily identified from hospital records. Tumor characteristics, initial courses of therapy, and sociodemographic information are obtained from medical records. Survival is determined by SEER using death certificates, medical records, voter registration, and other public records.

Patients
All women in the SEER database who had an incident diagnosis of uterine cancer between January 1992 and December 1998 were identified. Women were excluded if they were younger than 40 or older than 80 years, were neither white nor African-American, had in situ disease (International Federation of Gynecology and Obstetrics stage 0), or were diagnosed with uterine cancer at autopsy.

Variables
Sociodemographic characteristics. Race was coded as white or African-American. Age was analyzed as a continuous variable. Marital status was grouped into married and not married, with the latter category including never married, separated, divorced, and widowed.

Tumor characteristics. Adjusting for tumor stage in analyses of the effect of surgery on survival is challenging. Because surgery generally includes staging procedures, women who undergo surgery are more likely to be found to be at a higher stage than women who do not undergo surgery. Thus if analyses are based on surgical stage, surgery can seem to improve survival simply by moving women with an intermediate extent of disease from a lower to a higher stage group (stage migration), thereby making both the higher and lower stage groups seem to have better survival.^15,16 Thus our primary analyses adjusted for clinical stage, using information available before undergoing surgery. However, because our primary interest was in racial disparities in treatment and survival, not the absolute effect of surgery on survival, we also explored the effect of adjusting for full stage information (including the information from surgery) using the International Federation of Gynecology and Obstetrics tumor stage classification. Histology was grouped into three categories according to aggressiveness: (1) endometrioid and mucinous; (2) adenocarcinoma, squamous, adenosquamous, and neoplasm or carcinoma, not otherwise specified; and (3) papillary serous, papillary, clear-cell, and anaplastic. Endometrial cancer can be categorized into four grades of increasing severity. Grade 3 and 4 were combined for most analyses because of variation in the use of grade 4 across sites.

Treatment characteristics. On the basis of available SEER codes, initial surgical therapy was categorized as no primary surgery, hysterectomy without node dissection, and hysterectomy with node dissection (including radical hysterectomy). SEER coding did not permit the distinction of radical hysterectomy from extra-fascial hysterectomy with pelvic and para-aortic lymph node dissection. Postoperative radiation therapy (XRT) was identified from SEER coding.

Data Analysis
Statistical analyses were conducted using STATA 7.0 software (STATA Corp, College Station, TX). All P values are two-sided. Sociodemographic, tumor, and treatment characteristics were compared between African-American and white women using independent sample t tests for continuous variables and the ordinary ² test for categoric variables. Associations between race and use of surgery or XRT were adjusted for potential confounding by stage, grade, histology, age, or marital status using multiple logistic regression. Variables were retained in the model if they were significantly associated with the outcome or altered the coefficient for another variable by greater than 15%.¹⁷ SEER site was retained in all models. Interaction terms were assessed for all variables specified a priori as potential effect modifiers.

Cox proportional hazards models were used to assess the effects of tumor characteristics, sociodemographic characteristics, and treatment characteristics on the strength of the association between race and survival. Sequential regression models were built, beginning with the model containing race only and finishing with the model including race, tumor characteristics, sociodemographic characteristics, and treatment characteristics. Treatment was analyzed using dummy variables, initially including only the categories of no surgery, hysterectomy without node dissection, and hysterectomy with node dissection. To assess the effect of postoperative XRT, an additional category of hysterectomy with postoperative XRT was included in a subsequent model. As with the analyses of rates of treatment, all models adjusted for SEER site and interaction terms were tested for all variables specified a priori as potential effect modifiers. Primary analyses included patients with stage I, II, III, and IV disease in the same regression. However, to explore potential differences between stages, we repeated these analyses among the subgroups of women with stage I, II, or III disease only and women with stage IV disease only.

	RESULTS

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A total of 21,561 eligible women were identified (Table 1). African-American women had higher stage and grade at presentation, with 13.5% of African-American women presenting with stage IV disease compared with only 4.4% of white women and 39% of African-American women presenting with grade 3 or 4 tumors compared with 20% of white women. Histology also differed between African-American and white women, with 17% of African-American women having a papillary serous or papillary histology compared with only 6% of white women. In addition, African-American women were more likely to be separated, divorced, widowed, or never married and less likely to be married.

To ensure that these findings were not driven by differential use of surgery in local-regional (stage I, II, and III) or metastatic (stage IV) disease only, we repeated these analyses in the subgroup of women with local-regional disease and the subgroup of women with stage IV disease. In both subgroups, African-American women were significantly less likely to undergo surgery after adjusting for tumor and sociodemographic characteristics (OR, 0.28; 95% CI, 0.19 to 0.41 for stage I, II, and III, and OR, 0.54; 95% CI, 0.34 to 0.85 for stage IV) and use of surgery was significantly associated with survival (OR, 0.27; 95% CI, 0.22 to 0.33 for stage I, II, and III, and OR, 0.29; 95% CI, 0.30 to 0.42 for stage IV). Among patients with stage I disease, 7.7% of African-American women did not undergo surgery, whereas only 2.2% of white women did not undergo surgery. Similarly, among patients with stage II disease, 20.8% of African-American women did not undergo surgery compared with only 6.0% of white women. Furthermore, adjusting for differential use of surgery reduced the racial difference in survival for both subgroups, with the HR for the association between African-American race and mortality declining from 1.6 to 1.4 for women with local-regional disease and 1.7 to 1.5 for women with stage IV disease with the addition of surgery to a regression model containing tumor and sociodemographic characteristics. However, the association between surgery and survival differed between African-American and white women with local-regional disease (HR, 0.41; 95% CI, 0.24 to 0.72 for African-American women and HR, 0.24; 95% CI, 0.19 to 0.30 for white women; P value for interaction = .001) but not between African-American and white women with stage IV disease (P value for interaction > .10).

	DISCUSSION

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The results of this study demonstrate that African-American women with endometrial cancer are less likely to undergo primary surgery and are more likely to die from their disease than are white women with endometrial cancer. Although it is widely accepted that African-American women are more likely to present with advanced-stage, poorly differentiated tumors with unfavorable histologic types, it has been less well recognized that, after adjusting for all these characteristics, African-American women are significantly less likely than white women to have surgery performed for their endometrial cancer. Furthermore, in our study, this racial disparity was observed for women with both local-regional (stages I, II, and III) and metastatic (stage IV) disease. Furthermore, because surgery is significantly associated with survival for both these groups, our study demonstrates that racial differences in survival are smaller after adjusting for lower rates of surgery among African-American women.

Because endometrial cancer surgery includes both staging procedures and therapeutic procedures, it is difficult to determine whether an association between surgery and survival is causal. Women who go to surgery are more likely to be found to have advanced disease and more likely to be upstaged. This process can result in two potential biases. If information from surgical staging is included in the adjustment for stage in multivariate models, surgery can seem to improve survival simply because it has reclassified early-stage patients with more extensive disease into the higher stage category. However, if only clinical stage information is used in multivariate models, stage becomes an imperfect measure of true extent of disease and differences in survival among surgically treated and not treated patients may be partly attributable to unmeasured differences in extent of disease. This problem is particularly important if use of surgery depends on information about extent of disease that is not captured by clinical stage. Thus although surgery remained strongly associated with survival in our analyses whether our models included clinical stage information only or clinical and surgical stage information, it is important to recognize that this association may not be causal. Despite these limitations, analyses of observational data remain an important tool for understanding racial disparities in cancer treatment and outcomes as experimental evidence is generally lacking.

These results confirm and extend the findings of prior studies. A prior analysis of the National Cancer database found that African-American women were less likely to undergo surgical therapy at all stages of disease but did not explicitly examine the association between treatment and survival.² Several other studies found that tumor characteristics, prior hormone use, socioeconomic status, and some treatment characteristics contributed to the difference in survival between African-American and white women with endometrial cancer.^3–7 Other analyses of single institutions found no difference in the extent of treatment but persistent racial differences in survival.^3,5,18 The lower rate of surgery among African-American women is supported by similar racial disparities in use of surgery for many other conditions, including coronary artery bypass surgery, lung cancer resection, and renal transplantation.^9,19–21

Why are African-American women less likely to receive surgery for endometrial cancer? Racial disparities in treatment have been shown in other diseases to be multifactorial and complex.^22–24 These reasons include reduced access to care, through social, geographic, or economic factors, as well as potentially discriminatory practices by surgeons or other caregivers. Supporting the role of socioeconomic factors in this discrepancy, Hicks et al,² using the National Cancer Data Base, found that limited income was associated with a lack of treatment for African-American women with stage IV disease. Other reasons include potential differences in extent of disease, medical comorbidity, or patient preferences for surgery between races. Although we adjusted for clinical stage, grade, and histology, it is likely that disease severity varies by race within these classifications, complicating survival data and making surgery a less feasible option for women with more advanced disease. Thus the lower rates of surgery among African-American patients may be partly related to a higher proportion of African-American patients presenting with advanced-stage disease, which is not generally amenable to primary surgical intervention. Greater medical comorbidity among African-Americans was documented for patients with endometrial cancer in the National Cancer Institute’s Black/White Cancer Survival Study and has been shown to contribute to disparities in the use of many other procedures, including coronary artery catheterization.^4,22,23 To our knowledge, no data currently exist about differences in preferences for surgery between African-American and white women with endometrial cancer.

Our analyses suggest that the association between surgery and survival is weaker among African-American women (HR, 0.44) than white women (HR, 0.26). As noted previously, interpreting the association between surgery and survival is difficult, and it is important not to assume that differences in the strength of the association indicate differences in the effectiveness of surgery. For example, it is possible that these differences are a marker for differences in the selection of patients for surgery. If the differential use of surgery between healthy and less healthy white women is greater than among African-American women, the apparent benefit of surgery among white women could be greater, simply because use of surgery is a better marker of being healthy among white than African-American women. However, it is possible that racial differences in the strength of the association between surgery and survival represent differential effectiveness of surgery. Such a difference in effectiveness might, in turn, have several potential explanations. African-Americans may have more biologically aggressive tumors, as has been observed using molecular markers, and these tumors may be less likely to be cured by surgery.²⁵ Another possible explanation is that the quality of surgical and perioperative care may vary according to race. Several studies have demonstrated that surgical specialty has a substantial effect on survival in ovarian cancer, with women undergoing primary surgery by a gynecologic oncologist or general surgeon having significantly better survival than women whose primary surgeon was a general gynecologist.^26,27 Thus it is possible that racial differences in access to gynecologic oncologists or general surgeons may contribute to differential effectiveness of surgery.²⁸ In addition, case volume has been demonstrated to be closely associated with outcomes in many cancer surgeries, and one recent analysis of Medicare data suggests that high-volume hospitals have lower proportions of African-Americans undergoing high-risk surgeries than do low-volume hospitals.^29–31 Further research is needed to test this hypothesis, as detailed information regarding surgical and preoperative care, including physician specialty, are not available through the SEER database.

Our study confirms the important contribution of differences in stage, grade, and histology to the survival difference between African-American and white women with endometrial cancer. Although we are unable to determine whether these differences reflect differences in prior exposures (such as differential use of postmenopausal hormone replacement therapy), prior medical care and screening, or genotypes, it is clear that worse tumor characteristics at presentation are the single greatest contributor to the difference in survival. Our analyses also show that clinical stage, grade, and, to a lesser extent, histology are significantly associated with use of primary surgical therapy and postoperative XRT. Women seem to be less likely to undergo surgery if they have stage II, III, or IV disease than if they have stage I disease, although they are more likely to undergo postoperative XRT at higher stages.

These data also offer some insight into the effectiveness of lymph node sampling and of postoperative XRT in improving survival from endometrial cancer. In this analysis, adjusting for clinical stage without including results of the node sampling itself, use of lymph node sampling was associated with a small but significant reduction in mortality (approximately 10%). Postoperative XRT was associated with a somewhat larger reduction in mortality (20%). Although the selection of healthier patients for these procedures may contribute to their apparent effect on survival, these results support the argument that postoperative XRT and, to a lesser extent, lymph node sampling may improve survival among women with endometrial cancer.

Our study has several important limitations. The SEER database does not include information about comorbid medical conditions or socioeconomic status, preventing us from determining how these factors contribute to the differential rates of surgery or the residual increase in mortality among African-American women. Also unavailable are details regarding patients’ preferences and access to care, as well as what treatments were recommended to individual patients and how that information was communicated. However, only a minority of the women not receiving surgery would be likely to be considered surgically inoperable based on clinical evidence of unresectable disease, though we did find that African-American women with stage IV endometrial cancer were less likely to undergo surgery. As noted previously, accurately adjusting for stage at diagnosis is difficult because information about extent of disease can be determined through surgery. Thus we are unable to determine whether the observed associations between surgery and survival are causal.

These data demonstrate that endometrial cancer treatment and mortality vary significantly according to race and suggest that differential use and effectiveness of surgery need to be considered as potential explanations for the increased mortality observed in African-American women with endometrial cancer. Further studies are necessary to explore why the association between surgery and survival is weaker among African-American women and to test the hypothesis that this differential effect may reflect differences in the quality of providers or hospitals. Together, these efforts are only beginning steps toward understanding and addressing the dramatic difference in endometrial cancer survival between African-American and white women in the United States.

	AUTHORS’ DISCLOSURES OF POTENTIAL CONFLICTS OF INTEREST

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The authors indicated no potential conflicts of interest.

	NOTES

 
K.A. is supported by a Robert Wood Johnson Generalist Physician Faculty Scholar Award and an American Cancer Society Clinical Research Training Grant.

	REFERENCES

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20. Daumit G, Hermann J, Coresh J, et al: Use of cardiovascular procedures among black persons and white persons: A 7-year nationwide study in patients with renal disease. Ann Intern Med 130:173–182, 1999[Abstract/Free Full Text]

21. Eggers P: Racial differences in access to kidney transplantation. Health Care Financ Rev 17:89–103, 1995[Medline]

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Submitted January 29, 2003; accepted August 25, 2003.

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