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Trends in Surgery and Chemotherapy for Women Diagnosed With Ovarian Cancer in the United States

From the Applied Research Program, Surveillance Research Program, and Cancer Therapy Evaluation Program, National Cancer Institute, Bethesda, MD.

Address reprint requests to Linda C. Harlan, PhD, National Cancer Institute, 6130 Executive Blvd, MSC 7344, Bethesda, MD 20892-7344; e-mail: lh50w{at}nih.gov.

	ABSTRACT

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Purpose: We examined patterns of care in a population-based sample of 601 ovarian cancer patients diagnosed in 1991, and a sample of 566 women was selected in 1996 to examine trends in care.

Patients and Methods: Patient cases were sampled from within the Surveillance, Epidemiology, and End Results program. Medical records were reabstracted, and treatment data were verified with the treating physician.

Results: Across these two time periods, the percentage of women with presumptive stage I, II, and IV disease who received lymph node dissection increased. However, a significant number still were not precisely staged. More than 65% of women with ovarian cancer were given cyclophosphamide in 1991 compared with about 14% in 1996. Paclitaxel increased from 1% to 62% during that time. After adjusting for age, race or ethnicity, registry, income, insurance status, Charlson score, residency training program, and marital status, women with early-stage disease were significantly more often given National Institutes of Health Consensus Development Conference guideline therapy in 1996 than in 1991. However, for women with stage III and IV disease, the use of guideline therapy did not significantly increase. Older women and minorities consistently received less guideline therapy, and the lack of private insurance was an impediment for both Hispanic and non-Hispanic black women.

Conclusion: Despite guidelines presented by several organizations, significant numbers of women with ovarian cancer are not being provided with appropriate care. This is particularly true for older and minority women, especially those without private insurance. Educational strategies must be devised to increase the number of women receiving guideline therapy and decrease disparities across population groups.

	INTRODUCTION

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IN 2003, approximately 14,300 women will die from ovarian cancer. It is the fifth most common cancer in women and the leading cause of death from genital cancers.¹ The 5-year survival rate for ovarian cancer is approximately 95% for women with localized disease. However, approximately 60% of women have distant stage ovarian cancer at diagnosis, and the 5-year survival rate with distant disease is only 31%. Age and race or ethnicity influence the incidence of ovarian cancer and the survival rate. Women age 65 years and older have a higher incidence of disease (56.3 of 100,000 compared with 11.2 of 100,000 for women younger than 65 years) and a significantly poorer 5-year survival (32.9% compared with 65.8%). Ovarian cancer occurs more frequently in non-Hispanic white women (18.3 of 100,000) than in non-Hispanic black women (11.9 of 100,000) or Hispanic women (13.5 of 100,000).² The lifetime risk of being diagnosed with ovarian cancer is 1.82% for white women and 1.05% for non-Hispanic black women. However, white women have better survival than non-Hispanic black women within comparable local and distant stages of cancer.

We conducted a patterns of care study of ovarian cancer patients diagnosed in 1991 to examine dissemination of state-of-the-art therapy into community practice.³ We conducted a second patterns of care study of ovarian cancer patients diagnosed in 1996 to examine staging and treatment patterns and trends in these patients over time. This analysis examines patterns and trends in staging and therapy, surgery, and chemotherapy in this population-based study of ovarian cancer patients diagnosed in the years 1991 and 1996.

	PATIENTS AND METHODS

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Data from the Surveillance, Epidemiology, and End Results (SEER) program and the patterns of care study were used for this assessment. SEER is a population-based cancer registry program that routinely collects detailed data on the diagnosis, tumor characteristics, demographics, and treatment of all cancers occurring in defined geographic regions. However, the data appear to be generally representative of cancer incidence and mortality in the United States.⁴ SEER includes areas with more foreign-born individuals and areas that are somewhat more urban. The registry data are obtained primarily by abstracting medical records located in hospitals, outpatient surgical centers, and pathology departments. The patterns of care studies are samples of patients selected by cancer site from within the SEER population. Because the majority of adjuvant therapy is provided in an outpatient setting, and the SEER data collection is primarily hospital based, the patterns of care studies are routinely conducted to supplement SEER information on adjuvant therapy.

We first analyzed ovarian cancer patterns of care patients who were newly diagnosed in 1991 to determine the patterns of treatment in the community setting. We subsequently analyzed a sample of women diagnosed in 1996 to examine trends in diagnostic staging and treatment. We refer to stage at diagnosis as presumptive stage. Because a large percentage of women with ovarian cancer did not have lymph node sampling, which frequently results in upstaging of cancer patients, we use the term presumptive stage when discussing disease stage. In both 1991 and 1996, women with presumptive stage I and II disease were oversampled. In 1996 non-Hispanic blacks and Hispanics also were oversampled for the study. Reported patients age 20 years or older were stratified by race or ethnicity and stage. A random sample was selected by stratum within each registry. Women with a previous diagnosis of cancer (other than nonmelanoma skin cancer) and women diagnosed simultaneously with two primary cancers were ineligible because either condition might alter the selection of initial therapy. Women diagnosed during autopsy or on the death certificate only were likewise ineligible. A total of 777 women diagnosed in 1991 and 816 women diagnosed in 1996 were eligible for the study. We excluded 176 and 250 patients diagnosed with nonepithelial ovarian cancer or cancers of low malignant potential in 1991 and 1996, respectively.

The medical records of each sampled patient were abstracted to verify tumor characteristics, treatment provided, and certain demographic information. Abstractors attended a central training session to ensure consistency and comparability of abstracting and coding across registries. Each patient’s treating physician was contacted to verify whether radiation therapy, chemotherapy, or hormonal therapy had been given and which specific agents were administered. Physicians who did not treat the patient were asked to list the names of other physicians who might have treated the patient. Those physicians were then contacted for treatment information.

The clinical factors included in these analyses were stage at diagnosis, nodal status, histologic tumor grade, and comorbidities. Stage, nodal status, and tumor grade were abstracted using SEER rules. All comorbidities listed in the medical record were recorded. These were centrally coded according to International Classification of Diseases (9th revision, clinical modification) by one medical records technician. The comorbidities were analyzed using the Charlson score.⁵

Demographic factors were categorized and included age, race or ethnicity, marital status, and residence at the time of diagnosis (Table 1). SEER does not have patient-level information on income or education, so we used the patient’s residence to determine the census tract.⁶ The median income and proportion of individuals age 25 years and older with less than a high school education in the patient’s census tract were used as surrogate measures for individuals in the current data sets. Insurance information was collected from the patient’s medical record. Number of hospital beds, presence of a residency training program, and hospital ownership was coded by the registry using data from the American Hospital Association Guide to the Health Care Field.⁷

Because of the importance of race or ethnicity, we constructed separate models for each racial or ethnic group. The goal was to determine the specific factors associated with the use of guideline therapy in the different racial or ethnic groups.

All estimates were weighted to reflect the population from which the sample was drawn. The sample weights, calculated as the inverse of the sampling proportion for each sampling stratum (defined by age, race or ethnicity, stage, and registry), were used to obtain estimates that are representative of all eligible ovarian cancer patients in the study areas. Because early stage was oversampled, an overall mean value will be different from the arithmetic average of each stage group. We used SUDAAN statistical software (1997, Research Triangle Institute, Research Triangle Park, NC) for all analyses. This software allows for the use of sample weights and adjusts the SEs appropriately. All tests are two sided. The results of logistic regression models are shown as percentages receiving the guideline therapy adjusted for the independent variables included in the model. These percentages were directly standardized to the distribution of the covariates among the weighted sample used in each model. The probability of receiving the guideline therapy can then be directly compared across levels of the covariates included in the model.¹¹

	RESULTS

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The distribution of patient cases by year of diagnosis is listed in Table 1 with the weighted percentages and the number of patients sampled (unweighted). More women diagnosed with stage I, II, or III in 1996 had their nodes sampled than did women diagnosed in 1991 (Table 1). There was an increase in the percentage of women who had a Charlson score of 1 or greater in 1996 and a decrease in the percentage of women who had private insurance.

The first two columns of Table 2 show the percentage of women in 1991 and 1996 who received guideline therapy; the reason is listed for those who did not receive guideline therapy. The percentage of women with presumptive stage I and II disease who received guideline therapy increased primarily because of the increased number of those who received lymph node dissections in 1996 (Table 2, columns 1 and 2).

We combined the data from 1991 and 1996 to compare women treated in a hospital with an approved residency training program with those treated in hospitals with no approved program (Table 2, columns 3 and 4). Thirty-nine percent of the women with presumptive stage I, grade 1 to 4 disease who were treated in a hospital with a residency training program were classified as not having received guideline therapy because they failed to have a lymph node assessment, compared with 58% of women with similar stage and grade treated in a facility with no residency training program. Lymph node dissection was not a criterion for guideline therapy for women diagnosed with late-stage disease. However, women with late-stage disease treated in facilities with no residency training program received stage-appropriate surgery and chemotherapy less often than did women treated in a facility with a residency training program.

Non-Hispanic white women were more likely to receive guideline therapy than were non-Hispanic black women in both 1991 and 1996 (Table 3). The difference in several demographic factors remained between 1991 and 1996. Women who were married, were living in a census tract with the highest median income, or who had higher percentages of high school diplomas more often received therapy consistent with the guidelines. The difference between facilities with and without an approved residency training program remained, but the degree of difference narrowed.

Income, education, and hospital ownership were not associated with the use of guideline therapy after adjusting for the other variables in either early-stage or late-stage disease. These factors were dropped from the final model. We also included pair-wise interaction terms for all variables in the model and race or ethnic group. Only the interaction term of insurance and race or ethnic group was important. However, when this was included in the model with all the other variables, it was no longer statistically significant.

Because of the importance of determining factors associated with the use of guideline therapy, we modeled the use within each race or ethnic group (Table 6). Stage I or II, a Charlson score of 1 or more, and the lack of private health insurance were associated with significantly less use of guideline therapy in the model for non-Hispanic black women. Stage I or II and the lack of private insurance were also associated with significantly less use of guideline therapy in Hispanic women. Insurance was not associated with guideline therapy in non-Hispanic white women, although the presence of a residency training program remained statistically significant. Non-Hispanic white women who were married more often received guideline therapy. As with non-Hispanic black women, a Charlson score of 1 or more was associated with the decreased use of guideline therapy.

	DISCUSSION

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Women with presumptive stage I and II ovarian cancer did not receive guideline therapy primarily because of a failure to assess lymph nodes or assign a tumor grade. The failure to assess lymph nodes compares with a report by Averette et al¹² that only 11% of the ovarian cancer patients diagnosed in 1983 and 25% of the ovarian cancer patients diagnosed in 1988 underwent the peritoneal and lymph node biopsies necessary for adequate staging. Information on regional lymph node biopsies in this study indicates that in 1991, 38% of presumptive stage I and II ovarian cancer patients had a lymph node biopsy. This was somewhat higher than for the earlier time period Averette et al reported, and in our study lymph node biopsies increased significantly to 59% in 1996. This suggests an increase over time in the percentage of women with early-stage ovarian cancer who receive lymph node sampling.

An important factor associated with use of guideline therapy for non-Hispanic white women was the presence of an approved residency training program. We do not have data on the type of residency program or the subspecialties of the hospitals, but we suspect that the presence of an approved residency training program may function as a proxy for the presence of an oncologist with expertise in the management of ovarian cancer. In a Utah SEER study, the authors reported that women with advanced disease who saw a gynecologic oncologist had a significant survival advantage.¹³ Averette et al¹² reported that gynecologic oncologists more often performed omentectomies and pelvic and para-aortic lymphadenectomies on their ovarian cancer patients than did obstetricians and gynecologists, who performed these surgical procedures on their ovarian cancer patients more often than did general surgeons. They also reported that fewer than 25% of the patients in their 1988 study were treated by gynecologic oncologists. An analysis of data from the Utah SEER registry found that only 39.3% of ovarian cancer patients diagnosed between 1992 and 1998 saw a gynecologic oncologist at some time during their cancer diagnosis or treatment.¹³ However, the proportion of women seeing a gynecologic oncologist did increase over time.

Hispanic women and non-Hispanic black women in this study generally received guideline therapy less often than did non-Hispanic white women. Overall, non-Hispanic black women did not have higher tumor grade than non-Hispanic white women, and in stage I disease were not significantly more likely to have an unknown grade of tumor. Of those with nodes examined, non-Hispanic black women had significantly more positive nodes. In addition, non-Hispanic black women were more often from census tracts with lower median incomes and with more individuals having less than a high school education, and were more likely to have a Charlson score of 1 or higher. Parham et al¹⁴ reported similar demographic findings in a study comparing the treatment of African-American and non-Hispanic white women. In that study, African-American women with stage I and II ovarian cancer were more often treated with surgery alone, whereas non-Hispanic white women were more often treated with a combination of surgery plus radiation. Among stage III and IV ovarian cancer patients in that study, African-American women were more often treated with chemotherapy without surgery.

Age influenced receipt of guideline therapy only for women diagnosed with stage III and IV disease. Less aggressive therapy has been reported for older individuals in a number of cancer sites including breast, prostate, colorectal, and lung, as well as in other chronic diseases.^15–19 Perhaps physicians anticipate that individuals younger than age 65 years with advanced disease would be expected to gain significant benefit from the more aggressive therapy because of a longer life expectancy. In addition, women with a Charlson score of 0 and women who were married were also more likely to receive guideline therapy. These findings are similar to those of many other studies.^15,17 In most cases, younger people have fewer comorbid conditions that might contraindicate more aggressive therapy. Social factors potentially have a role as well. Younger individuals may have more people they can rely on for support, such as friends and siblings, and many will have parents who might still be able to provide assistance. Being married has been associated with more aggressive therapy. This may be related to the availability of additional social support, as well as higher incomes. Our data showed that nearly 50% fewer unmarried women had private health insurance than did married women.

Among women with late-stage disease, nearly 40% did not receive stage-appropriate surgery and/or chemotherapy. This did not change significantly in the 5 years between 1991 and 1996. We compared the percentage of women receiving chemotherapy in our study to an earlier study of patients diagnosed in 1983 and 1988. In that study, the authors reported that 67% and 66%, respectively, received chemotherapy after the initial tumor debulking.¹² In our study, overall, 74% and 77% of women with ovarian cancer diagnosed in 1991 and 1996, respectively, received chemotherapy. These percentages suggest an increase in the use of adjuvant chemotherapy over the 13-year time period. The use of paclitaxel was approved by the US Food and Drug Administration in 1992. If paclitaxel is added to the 1996 guideline therapy requirement for stage III or IV disease, the percentage of women meeting the guidelines decreases from 62% to 56%.

The adjusted percentages of women receiving guideline therapy, among women with private insurance, differ slightly by race or ethnicity (57% non-Hispanic white women, 55% Hispanic women, and 51% non-Hispanic black women). However, among women who had Medicaid, no insurance, or Medicare without supplemental insurance or unknown insurance, non-Hispanic black women (26%) and Hispanic women (34%) received guideline therapy less often than did white women (51%). Insurance might also be a partial measure of income, wealth, or access to aggressive care. Women with private insurance are likely to have a higher income and may have access to cancer specialists and medical care not available to women with no insurance or publicly funded insurance.

We also investigated whether guideline therapy use differed by different combinations of race or ethnic groups, facilities with or without a residency training programs, and insurance using a three-way interaction term in a multivariate model after adjusting for year of diagnosis, stage of disease, age, race or ethnic group, Charlson score, marital status, insurance, geographic region, and three two-way interaction terms between race or ethnic groups, facilities with or without a residency training programs, and insurance. Although the interaction was not statistically significant overall, the findings were suggestive of differences. Guideline therapy was consistently less in facilities with no residency training program. Non-Hispanic white women treated in facilities with residency training programs received guideline therapy similarly whether or not they had private insurance. In contrast, non-Hispanic black women lacking private insurance, whether treated at facilities with or without residency training programs, were given guideline therapy approximately half as often as were non-Hispanic white women. Hispanic women without private insurance were given guideline therapy less often than were non-Hispanic white women, but the differences were not as large. The lack of private insurance was particularly devastating for minority women, especially if they were treated in a facility with no residency training program.

Since the NIH Consensus Development Conference in 1994, several guidelines for the management of women with ovarian cancer have been published. These include guidelines by the National Comprehensive Cancer Network,²⁰ the Society of Gynecologic Oncologists,²¹ and the International Workshop on Advanced Ovarian Cancer.²² In addition, the National Cancer Institute’s Physician Desk Query program²³ has continued to update its summary of treatment findings. These additional guideline statements should influence treatment as well. Clearly, publication of guidelines and recommendations may not be enough to change clinical practice. Although paclitaxel therapy did replace cyclophosphamide therapy in women with ovarian cancer between 1991 and 1996, the use of paclitaxel was supported by an extensive and expensive advertising and sales campaign by the sole manufacturer, Bristol-Myers Squibb Oncology (Princeton, NJ). Groups that publish guidelines do not have the funds for similar ad campaigns. The improvement in the compliance with guideline therapy for stage I and II ovarian cancer is explained primarily by an increase use of lymph node sampling as part of a primary staging. Neither the proportion of women with early-stage disease who were assigned histologic grade, nor the proportion of women with stage III and IV disease who underwent recommended surgery and chemotherapy changed.

Potential reasons for this persistence of less than optimal care include disparities in patient access to cancer specialists (such as gynecologic oncologists), resistance to change among practitioners, the presence of comorbidity, or reluctance among patients and their families to undergo aggressive treatment. Especially worrisome is that non-Hispanic black and Hispanic women without private insurance receive guideline therapy less often. The majority of these women do have public insurance, either Medicare or Medicaid. The presence of a residency training program suggests that there may be an issue of access to specialists. To ensure that all women with ovarian cancer receive appropriate care, the barriers to care need to be identified, and the appropriate interventions need to be implemented to remove these barriers.

	AUTHORS’ DISCLOSURES OF POTENTIAL CONFLICTS OF INTEREST

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The authors indicated no potential conflicts of interest.

	ACKNOWLEDGMENTS

 
The authors acknowledge Rachel Ballard-Barbash for her valuable analytic and editorial critique.

	REFERENCES

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION AUTHORS’ DISCLOSURES OF... REFERENCES

 
1. American Cancer Society. Statistics for 2003. www.cancer.org/docroot/STT/stt_0.asp

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7. American Hospital Association: American Hospital Association Guide to the Health Care Field. Chicago, IL, American Hospital Association, 1988.

8. Trimble EL: The NIH consensus conference on ovarian cancer: Screening, treatment, and follow-up. Gynecol Oncol 55:S1–3, 1994[CrossRef][Medline]

9. McGuire WP, Hoskins WJ, Brady MF, et al: Cyclophosphamide and cisplatin compared with paclitaxel and cisplatin in patients with stage III and stage IV ovarian cancer. N Engl J Med 334:1–6, 1996[Abstract/Free Full Text]

10. Piccart MJ, Bertelsen K, James K, et al: Randomized intergroup trial of cisplatin-paclitaxel versus cisplatin-cyclophosphamide in women with advanced epithelial ovarian cancer: Three-year results. J Natl Cancer Inst 92:699–708, 2000[Abstract/Free Full Text]

11. Korn EL, Graubard BI: Analysis of Health Surveys. New York, NY, John Wiley & Sons, Inc, 1999

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15. Muss HB: Factors used to select adjuvant therapy of breast cancer in the United States: An overview of age, race, and socioeconomic status. J Natl Cancer Inst Monogr 30:52–55, 2001

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17. Potosky AL, Harlan LC, Kaplan RS, et al: Age, sex, and racial differences in the use of standard adjuvant therapy for colorectal cancer. J Clin Oncol 20:1192–1202, 2002[Abstract/Free Full Text]

18. Greenberg ER, Chute CG, Stukel T, et al: Social and economic factors in the choice of lung cancer treatment: A population-based study in two rural states. N Engl J Med 318:612–617, 1988[Abstract]

19. Gatsonis CA, Epstein AM, Newhouse JP, et al: Variations in the utilization of coronary angiography for elderly patients with an acute myocardial infarction: An analysis using hierarchical logistic regression. Med Care 33:625–642, 1995[Medline]

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Submitted January 10, 2003; accepted June 27, 2003.

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This Article Abstract Full Text (PDF) Purchase Article View Shopping Cart Alert me when this article is cited Alert me if a correction is posted Services Email this article to a colleague Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Save to my personal folders Download to citation manager Rights & Permissions Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Harlan, L. C. Articles by Trimble, E. L. Search for Related Content PubMed PubMed Citation Articles by Harlan, L. C. Articles by Trimble, E. L. Social Bookmarking                            What's this?