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Variations in the Use of Chemotherapy for Elderly Patients With Advanced Ovarian Cancer: A Population-Based Study

From the Department of Epidemiology, Joseph L. Mailman School of Public Health; the Herbert Irving Comprehensive Cancer Center; and the Department of Medicine, College of Physicians and Surgeons, Columbia University, New York, NY; and the Department of Epidemiology and Preventive Medicine, Monash Medical School, Melbourne, Australia.

Address reprint requests to Alfred I. Neugut, MD, PhD, Department of Epidemiology, Mailman School of Public Health, PH-18-127, 630 W 168th St, New York, NY 10032; email: ain1{at}columbia.edu

	ABSTRACT

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PURPOSE: Since 1986, the recommended therapy for patients with ovarian cancer has included surgery and chemotherapy with a platinum compound (cisplatin or carboplatin). The purpose of this study is to assess the use of chemotherapy in elderly patients with advanced ovarian cancer.

METHODS: The Surveillance, Epidemiology, and End Results–Medicare database represents approximately 14% of the United States population and provides clinical and demographic information on cancer patients covered by Medicare, along with health care–utilization data from Medicare claims files. We analyzed the association of demographic and clinical factors with treatment among patients diagnosed from 1992 to 1996 with stage III or IV ovarian cancer, who survived 120 days beyond diagnosis, and were 65 years of age (N = 1,775).

RESULTS: Approximately 83% of elderly patients received some form of chemotherapy within 4 months of diagnosis. In a multiple logistic regression model with patients aged 65 to 69 years as the reference, the odds ratios of receiving chemotherapy were 0.96 (95% confidence interval [CI], 0.63 to 1.46) for ages 70 to 74, 0.65 (95% CI, 0.43 to 1.00) for 75 to 79, 0.24 (95% CI, 0.15 to 0.37) for 80 to 84, and 0.12 (95% CI, 0.07 to 0.19) for 85+. Hispanic patients were less likely to receive chemotherapy than non-Hispanic white patients. Since 1992, paclitaxel has gradually replaced cyclophosphamide as the drug most commonly used with platinum.

CONCLUSION: Despite its proven efficacy in treating ovarian cancer, chemotherapy seems to be used less among patients over age 65, especially those who are nonwhite and/or in the oldest age groups. Further research is needed to elucidate to what degree this represents appropriate clinical judgment and to what degree other factors, such as patient choice, play a role.

	INTRODUCTION

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CANCER IS A disease of the elderly. In those over the age of 65 years, the age-adjusted incidence rates for colorectal, prostate, breast, ovary, and lung cancers are six to ten times greater than in those below age 65; mortality rates show a similar pattern. The proportion of all cancer cases diagnosed among the elderly will undoubtedly increase as our population ages.¹

Older patients have been less likely to receive the standard treatment for cancer than younger patients, even when such treatments are potentially curative. A study of the use of potentially curative treatment for cancers of several sites found that the proportion of treated patients decreased with age.²

In the United States, women over the age of 65 account for nearly 50% of diagnosed ovarian cancer cases.¹ Age-specific incidence and mortality rates of ovarian cancer increase with age, peaking at 61.8/100,000 women (incidence) and 56/100,000 women (mortality) among women 80 to 84 years of age.³

Since the early 1980s, patients with advanced ovarian cancer (International Federation of Gynecology and Obstetrics stages III and IV) have experienced improved survival because of two treatment innovations: greater use of cytoreductive surgery and platinum-based chemotherapy.^4-6 Randomized trial results published in 1986 showed that patients who received doxorubicin and cyclophosphamide in combination with cisplatinum survived longer than patients who received the same agents without cisplatin.⁷ Subsequent studies found that patients who received carboplatinum with cyclophosphamide, and more recently with paclitaxel, had improved survival and less toxicity.^8,9 A recent meta-analysis reported a hazard ratio of 0.88 for survival with the use of nonplatinum regimens compared with platinum therapy.¹⁰ In 1994, the National Institutes of Health held a consensus conference at which preliminary results of a trial of cisplatin with paclitaxel or with cyclophosphamide were presented and reviewed; some but not all participants interpreted the data as showing better outcomes for the group receiving paclitaxel.¹¹

Treatment rates among elderly women with advanced ovarian cancer are significantly lower than among younger women. Among patients diagnosed with advanced ovarian cancer from 1983 to 1988 and listed in the National Cancer Institute’s Surveillance, Epidemiology, and End Results (SEER) registry, the proportion not treated with any modality increased sharply with age, from less than 4% of patients aged 55 to 64, to 9% of those aged 65 to 74, 22% of those aged 75 to 84, and 45% of those over 85 years of age. Survival was similarly correlated with age.¹² A survey of hospital tumor registries throughout the United States between 1983 and 1988 also found a pattern of undertreatment of elderly patients with ovarian cancer.¹³ During this same period, ovarian cancer mortality declined by 25% in younger American women but increased by 16% in those older than 65 years.¹² In a review of clinical trials at the Mayo Clinic, women older than age 65 enrolled on trials responded as well as those who were younger.¹⁴ However, this may reflect case selection bias and a better physiologic status among the smaller fraction of older women who were selected to receive chemotherapy. No study to date has been performed on a population-based scale.

In the present study, our objective was to evaluate chemotherapy use and the clinical and demographic variables associated with claims for chemotherapy among patients diagnosed with stage III or IV ovarian cancer after the age of 65 who were included in the SEER-Medicare database,¹⁵ a population-based data set, and will thus provide relatively unbiased information regarding use of chemotherapy in this population. Furthermore, the quality of the data is extremely high, so the utilization information is likely to be valid.

	METHODS

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Sample Selection
We identified all individuals in the linked SEER-Medicare database¹⁵ who had a confirmed first primary ovarian cancer (cancer code 50 in SEER) diagnosed in the years 1992 to 1996 inclusive (n = 7,525), who were 65 years of age (n = 5,979), had confirmed stage III or IV ovarian cancer (n = 3,958), and were not diagnosed by death certificate or autopsy (n = 3,945).

We excluded subjects who did not have Medicare A and B coverage; were members of a health maintenance organization (HMO) (the Health Care Finance Administration does not collect claims data from risk-based HMOs) from 1 year before diagnosis to 120 days after diagnosis; or survived less than 120 days after diagnosis (n = 2,170). The remaining sample for analysis consisted of 1,775 women.

Chemotherapy Treatment
Using the Health Care Finance Administration’s national Common Procedure Coding System (HCPCS code), we identified patients who had received a specified chemotherapeutic drug within 120 days of their cancer diagnosis in either their physician claims files or hospital outpatient claims files (cisplatin [Level II HCPCS J9060], carboplatin [J9045], cyclophosphamide [J9070, J9080, and J9090 to J9097] and paclitaxel [J9265]). In addition, we searched by Level II HCPCS codes (J9XXX, 964XX, 965XX, and Q0083 to Q0085), ICD-9-CM diagnostic codes (V581, V662, E9331, and E9307), and procedure codes (9925) from physician claims files or outpatient or admission hospital claims for evidence of other chemotherapy delivery. Among patients who did not have specific J9XXX chemotherapy HCPCS codes, these codes were used to capture any evidence that an unspecified chemotherapeutic drug was given during the 120 days after diagnosis.

Surgical Treatment and Sociodemographic Variables
We included in the surgically treated group all patients who had any cancer-directed procedure listed in the SEER field for cancer-directed surgery. We obtained data From the SEER database on age, race, sex, and area of residence.

Comorbid Disease
To assess the prevalence of comorbid disease in our cohort, we used the Deyo adaptation of the Charlson comorbidity index,^16,17 searching on the relevant codes for conditions resulting in hospitalization in the time interval from 1 year before to 120 days after diagnosis.

Statistical Analysis
Statistical analyses were carried out using SAS version 6.12 (SAS Institute, Cary, NC). Several classes of chemotherapy variables were defined. First, we identified those patients who received any chemotherapy, whether specified by name or not. We conducted separate analyses of claims that specified a platinum-containing chemotherapy (cisplatin or carboplatin) alone or in combination with cyclophosphamide or paclitaxel.

After univariate and bivariate analyses were performed, multiple logistic analysis models were created with chemotherapy treatment status as the dependent variable and age at diagnosis, year of diagnosis, sex, race/ethnicity, residence in urban setting, inpatient comorbid conditions, stage of ovarian cancer, grade of tumor, histology, and cancer-directed surgical intervention as covariates.

	RESULTS

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Baseline Descriptive Statistics
The sample consisted of 1,775 women over the age of 65 with International Federation of Gynecology and Obstetrics stage III (N = 904) or IV (N = 871) ovarian cancer diagnosed between 1992 and 1996 (Table 1). The age at diagnosis ranged from 65 to 100 years; the median age was 74 years. Most of the patients in the sample were non-Hispanic whites (89%), and most resided in central and fringe counties of metropolitan areas with populations greater than 250,000 (86%). Histologic types in the sample included nonspecific carcinomas (SEER code 02), nonspecific adenocarcinomas (SEER code 11), papillary/villous adenocarcinomas (SEER code 05), cystadenocarcinomas (SEER code 25), other specified carcinomas (SEER code 15), and mucinous adenocarcinomas (SEER codes 26 and 22). Almost half the patients in the sample had poorly differentiated tumors. Of the total sample, 17% had one and 8% had two comorbid conditions that had resulted in hospitalization from 1 year before to 120 days after diagnosis.

Predictors of Treatment With Chemotherapy
In bivariate analyses, older age was associated with decreased likelihood of receiving any form of chemotherapy (Table 2). Eighty-eight percent of women aged 65 to 69 years received chemotherapy, but only 43% of women over the age of 85 received chemotherapy. Tumor grade was also associated with receiving chemotherapy. Race, comorbid conditions, and the use of cancer-directed surgery were associated with receiving chemotherapy, but stage (III v IV) was not. In multiple logistic regression analysis, women who were 75 years of age or Hispanic or had two or more comorbid conditions were less likely than younger women, non-Hispanics, and those with one or no comorbid conditions, respectively, to be treated with chemotherapy (Table 2).

View larger version (17K): [in this window] [in a new window]   Fig 1. Time trends in Medicare claims for specific chemotherapeutic agents for treatment of ovarian cancer (1992 to 1996).

	DISCUSSION

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An inverse correlation of treatment with age has been documented for several cancers. In 1986, an analysis of SEER data from New Mexico documented variations in treatment patterns based on age for a variety of cancers.² Lower rates of treatment among the elderly over the age of 70 to 75 years compared with those in the preceding decade have been found in breast, colorectal, and ovarian cancer.^12,13,18,19 One study of patients over 80 years old suggests that that the majority of patients die or suffer major morbidity during the immediate postoperative period and that most patients who are discharged from the hospital are able to receive postoperative chemotherapy.²⁰ Our study included only patients who survived the first 120 days from diagnosis; these patients should have been eligible for chemotherapy. Such treatment has a proven survival benefit in advanced disease.^4,5,9 Without clear evidence that chemotherapy is more toxic or less beneficial to the elderly than to younger patients, failure to treat elderly patients with advanced disease may compromise their prospects for survival.

Race was also associated with treatment in our model; Hispanic patients were less likely to receive chemotherapy than non-Hispanic whites. Race as a factor in undertreatment has been documented for colorectal cancer, prostate cancer, breast cancer, ovarian cancer, and lung cancer.^21-25 In our own study of colon cancer treatment, non-Hispanic black patients were less likely to receive adjuvant chemotherapy than non-Hispanic white patients.¹⁹

As other studies have found,²⁶ comorbid disease status was inversely associated with chemotherapy, and prior surgical treatment was positively associated with receiving chemotherapy. We interpret surgical treatment as a marker for good functional status and the absence of comorbidities that would be contraindications for chemotherapy.

From 1992 to 1996, the proportion of patients treated with chemotherapy (Table 3, Fig 1) increased from 80% to 86%. Although one cannot be certain, this probably does reflect a true increase in oncology treatment practices within the SEER population. The oncology community seems to have responded relatively quickly to research findings that chemotherapy improved survival. In addition, after the 1993 report that paclitaxel, in conjunction with platinum, could improve survival,²⁷ and the 1994 National Institutes of Health Consensus Conference report further supporting this treatment,¹¹ the use of paclitaxel use rose steadily and cyclophosphamide use fell correspondingly (Fig 1).

One of the limitations of our study is that it is based on SEER data. The population of the SEER counties has been found to be more affluent, more educated, and less rural than the population of the United States.²⁸ These counties have the same density of physician resources as non-SEER counties, but there are fewer beds and fewer hospitals with approval from the Joint Commission on the Accreditation of Hospitals. Our study is also based on Medicare data and, therefore, does not provide any information about the use of chemotherapy among patients less than 65 years of age.

Another limitation of our study is that not all claims for chemotherapy administration identified the agents used, and that some patients who received chemotherapy did not have claims for it. We were able to analyze changes over time only in claims that mentioned specific chemotherapeutic drugs. A recent study compared Medicare claims for chemotherapy to data collected from hospital record abstractions or verification with the treating physician. The study found that the overall sensitivity of the Medicare claims to use of chemotherapy among patients with ovarian cancer was 93%. In the subset of those who had no Medicare claims for chemotherapy, 6% to 10% were found to have received chemotherapy according to the hospital record or the physician (Joan Warren, unpublished data). It is possible that older or nonwhite patients were more likely than other patients to receive treatment without claims. In our data, only 305 patients had no claims for chemotherapy. If 31 of those patients (10%) had actually received chemotherapy and all of them were 85+ years of age, the 85+ age group would still have been less likely to be treated than the 65- to 69-years age group. (The same validation study also found that virtually all patients who had any Medicare claim for chemotherapy had received a regimen including platinum.)

The accuracy of our evaluation of comorbid disease status, an important determinant of treatment, similarly depends on the accuracy of the diagnostic coding in the claims data. For the majority of comorbid diseases used in our index, agreement between claims data and abstracts of the medical record has been found to be higher than 85% and improved from 1977 to 1985.²⁹ We believe that by the 1990s, agreement may have improved still further.

Our data do not address the role of patient functional status in decision-making regarding treatment with chemotherapy. Recent reports indicate that comorbid disease may not be associated with functional status, and the latter may therefore account for what seems to be undertreatment of the very elderly and of Hispanic patients.^30,31

We did not include in our analysis patients who were enrolled in HMOs because Medicare does not collect claims on such patients. Consequently, we do not know how this set of patients may differ in their patterns of care from those with claims-based Medicare coverage. Two studies of treatment patterns in HMOs based in the San Francisco/Oakland and Seattle/Puget Sound areas found no clear disparities in the use of radiotherapy among patients with early-stage breast³² or prostate cancer.³³

Previous studies of decision-making in cancer treatment indicate that age influences both the frequency with which chemotherapy is offered as a treatment alternative and the willingness of patients to accept such treatment. In a study by Newcomb and Carbone,³⁴ nearly 50% of those under age 65, but only 35% of those over 65, were offered chemotherapy as a treatment option. Of those offered chemotherapy, nearly twice as many patients over the age of 65 (33%) as under 65 rejected chemotherapy, fearing side effects. However, a secondary analysis of several phase II trials in advanced cancer found no evidence of increased toxicity in those over the age of 65.³⁵

Our results reveal that by 1992 chemotherapy for ovarian cancer patients over age 65 had reached the level that would be maintained for the next 5 years. Adoption of national recommendations has been relatively rapid. Our data indicate that chemotherapy is much more widely used among older patients with ovarian cancer than among older patients with colon cancer. We believe that gynecologic oncologists have been eager to adopt the recommended treatment because its effects on both cancer and day-to-day quality of life are more readily apparent than the effects of colon cancer chemotherapy on similar end points in colon cancer patients. However, more research on the decision-making process that determines the use of chemotherapy is needed to assure the delivery of appropriate cancer care to the elderly and to other underserved groups.

	ACKNOWLEDGMENTS

 
Supported by the Gustavus and Louise Pfeiffer Research Foundation, Denville, NJ. D.H. was the recipient of an National Cancer Institute–funded postdoctoral fellowship (T32-CA09529). V.R.G. is the recipient of an American Cancer Society Award CRTG-98-260-01. A.I.N. is the recipient of a K05 Award (CA89155) from the National Cancer Institute and an American Cancer Society Award (RSGHP-01-024-01-CCE).

	NOTES

 
This study used the linked Surveillance, Epidemiology, and End Results (SEER)-Medicare database. The interpretation and reporting of these data are the sole responsibility of the authors. The authors acknowledge the efforts of the Applied Research Branch, Division of Cancer Prevention and Population Science, National Cancer Institute; the Office of Information Services, and the Office of Strategic Planning, Health Care Finance Administration; Information Management Services, Inc; and the SEER Program tumor registries in the creation of the SEER-Medicare database.

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Submitted February 5, 2001; accepted July 20, 2001.

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