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Breast Cancer Treatment of Older Women in Integrated Health Care Settings

Shelley M. Enger, Soe Soe Thwin, Diana S.M. Buist, Terry Field, Floyd Frost, Ann M. Geiger, Timothy L. Lash, Marianne Prout, Marianne Ulcickas Yood, Feifei Wei, Rebecca A. Silliman

From the Department of Research and Evaluation, Kaiser Permanente Medical Care Program, Pasadena, CA; Boston University Medical Center; Department of Epidemiology, Boston University School of Public Health, Boston; Meyers Primary Care Institute of Fallon Community Health Plan/Fallon Foundation/University of Massachusetts Medical School, Worcester, MA; Center for Health Studies, Group Health Cooperative, Seattle, WA; Lovelace Respiratory Research Institute, Albuquerque, NM; Division of Public Health Sciences, Wake Forest University School of Medicine, Winston-Salem, NC; Yale University School of Medicine, New Haven, CT; and the HealthPartners Research Foundation, Minneapolis, MN

Address reprint requests to Rebecca A. Silliman, MD, PhD, Boston University Medical Center, 88 E Newton St, Robinson 2, Boston, MA 02118; e-mail: rsillima{at}bu.edu

	ABSTRACT

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION Authors' Disclosures of... Author Contributions REFERENCES

 
PURPOSE: A substantial literature describes age-dependent variations in breast cancer treatment, showing that older women are less likely to receive standard treatment than younger women. We sought to identify patient and tumor characteristics associated with the nonreceipt of standard primary tumor and systemic adjuvant therapies.

PATIENTS AND METHODS: We studied 1,859 women age 65 years or older with stage I and II breast cancer diagnosed between 1990 and 1994 who were cared for in six geographically dispersed community-based health care systems. We collected demographic, tumor, treatment, and comorbidity data from electronic data sources, including cancer registry, administrative, and clinical databases, and from subjects' medical records.

RESULTS: Women 75 years of age or older and women with higher comorbidity indices were more likely to receive nonstandard primary tumor therapy, to not receive axillary lymph node dissection, and to not receive radiation therapy after breast-conserving surgery (BCS). Asian women were less likely to receive BCS, and African American women were less likely to be prescribed tamoxifen. Although nonreceipt of most therapies was associated with a lower baseline risk of recurrence, an important minority of high-risk women (16% to 30%) did not receive guideline therapies.

CONCLUSION: Age is an independent risk factor for nonreceipt of effective cancer therapies, even when comorbidity and risk of recurrence are taken into account. Information regarding treatment effectiveness in this age group and tools that allow physicians and patients to estimate the benefits versus the risks of therapies, taking into account age and comorbidity burden, are critically needed.

	INTRODUCTION

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION Authors' Disclosures of... Author Contributions REFERENCES

 
A substantial literature describes age-dependent variations in breast cancer treatment, consistently showing that older women are less likely to receive standard treatments than younger women. Past investigations have examined factors that might explain these age-dependent treatment variations, including patients' health and functional status,^1-5 patient-physician communication,^1,3,6-8 and patients' and their families' treatment preferences and support.^3,5,9,10 Race- and socioeconomic status–dependent variations in breast cancer treatment have also been reported.^11,12 In integrated health care settings (networks of care providers and organizations that offer coordinated health care services to a defined population and assume clinical and fiscal accountability for clinical outcomes¹³), where cost and access barriers to care are reduced, a small number of studies indicate that older women and minority women are more likely to receive breast-conserving surgery (BCS) and to receive radiation therapy after BCS than are their counterparts treated in fee-for-service settings.^14-17

We studied 1,859 women aged 65 years or older with early-stage breast cancer who received care in six geographically dispersed community-based integrated health care systems whose care is not accessible for study using Medicare data. We sought to identify patient and tumor characteristics associated with the nonreceipt of standard primary tumor and systemic adjuvant therapies. We extend previous investigations by the inclusion of a substantial number of the oldest women and by focusing on both primary and adjuvant therapies in integrated health care settings.

	PATIENTS AND METHODS

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION Authors' Disclosures of... Author Contributions REFERENCES

 
Setting
The Cancer Research Network (CRN) consists of the research programs and enrollee populations of 12 integrated health systems, including Group Health Cooperative, Harvard Pilgrim Health Care, Henry Ford Health System/Health Alliance Plan, HealthPartners Research Foundation, Lovelace Health Plan, the Meyers Primary Care Institute of Fallon Community Health Plan/Fallon Foundation/University of Massachusetts Medical School, and Kaiser Permanente in the following six regions: Colorado, Georgia, Hawaii, Northwest (Oregon and Washington), Northern California, and Southern California. The overall goal of the CRN is to increase the effectiveness of preventive, curative, and supportive interventions that span the natural history of major cancers among diverse populations and health systems through a program of collaborative research.¹⁸

Study Sample Eligibility
We identified potentially eligible patients at the following six CRN members: Group Health Cooperative, Western Washington; Kaiser Permanente, Southern California; Lovelace, New Mexico; Henry Ford Health System, Detroit, Michigan; HealthPartners, Minnesota; and Fallon Community Health Plan, Massachusetts. These six were chosen to achieve diversity in geography, system size, and patient populations while maintaining study feasibility. We used population-based cancer registry databases at four participating sites (Group Health Cooperative, Kaiser Permanente, Lovelace, and Henry Ford Health System) and administrative databases at two participating sites (HealthPartners and Fallon Community Health Plan) to identify potentially eligible patients. Eligible patients were all women aged 65 years or older who were diagnosed for the first time with histologically confirmed, early-stage breast cancer (American Joint Commission on Cancer TNM stage¹⁹ I, IIA, or IIB) between January 1, 1990 and December 31, 1994. Women were ineligible if they had another clinically active malignancy, except nonmelanoma skin cancer, diagnosed within 5 years before or 30 days after their breast cancer diagnosis. We also excluded women with simultaneously diagnosed bilateral breast cancer.

At sites with Surveillance, Epidemiology, and End Results (SEER) cancer registries, we identified women with International Classification of Diseases (ICD) –Oncology codes indicating a breast cancer diagnosis (C50.0 to C50.9). At sites without cancer registries, we reviewed claims and other administrative databases for ICD-9 or ICD-10 codes 174 to 174.9 and ICD-9 and Current Procedural Terminology (CPT) codes for excisional biopsy, breast biopsy, mastectomy, partial mastectomy with lymphadenectomy, partial mastectomy with breast cancer diagnosis, and partial mastectomy with radiotherapy or chemotherapy. Medical record abstractors verified (at sites with cancer registries) or determined (at sites without cancer registries) each patient's primary cancer site and stage at diagnosis, breast cancer diagnosis date, age at diagnosis, and absence of other clinically active malignancies.

Sampling
We included all eligible patients from all sites except Kaiser Permanente, Southern California, the largest site, where we sampled 10% of the subgroup of non-Hispanic white patients younger than 80 years old with stage I breast cancer because including the complete sample of these patients would only marginally increase the statistical power of the study but would substantially decrease its cost efficiency.

Protection of Patients
The protocol for this study was approved by the institutional review boards at each participating institution.

Data Collection
We collected demographic, tumor, treatment, and comorbidity data from electronic data sources, including cancer registry, administrative, and clinical databases, and from patients' medical records. An automated Data Collection System was preloaded with electronically available data from each site. We verified all preloaded data against medical records, except cancer registry data elements for sites with SEER registries. The SEER data items for demographic information, tumor characteristics, and primary tumor therapy were considered the gold standard.²⁰

Standardized medical record reviews were conducted at each site, and the data were entered directly into the Data Collection System. We assessed intrarater and inter-rater reliability twice during the 1.5-year data collection period. The intrarater reliability rates were 93% for both time periods, and the inter-rater reliability rates were 91% for time period 1 and 88% for time period 2.

Demographic information. We ascertained each woman's date of birth, race, and ethnicity.

Comorbidity. Comorbid conditions present during the 1 year before breast cancer diagnosis, as reflected in the medical records, were used to calculate the Charlson comorbidity index.²¹

Tumor characteristics. We collected date of diagnosis and stage at diagnosis, laterality, tumor size, lymph node evaluation, estrogen receptor protein and progesterone receptor protein status, and histology type and grade.

Breast cancer treatment. We collected the specific type of surgery performed and, if done, the results of axillary lymph node dissection (ALND) or sentinel node biopsy (SNB). The number of courses and doses for radiation, hormonal therapy, and chemotherapy and the specific hormonal and chemotherapeutic agents prescribed were ascertained from the medical record.

Independent Analytic Variables
Demographic characteristics. We categorized age as 65 to 69, 70 to 74, 75 to 79, and 80+ years of age. We grouped race/ethnicity as non-Hispanic white, Hispanic, African American, and Asian/Pacific Islander. We classified the small number of patients with other/unknown race (n = 5) as non-Hispanic white. For the 19% of the sample with missing ethnicity information, we applied a validated adaptation of the Generally Useful Ethnic Search System computer program to assign ethnicity based on a patient's last name.^22,23

Comorbidity. We calculated the weighted Charlson comorbidity index (0, 1 to 2, 3 to 4, or 5+) using the original algorithm.²¹ Because of small numbers, we collapsed scores of 3 or greater into one group.

Tumor characteristics and risk of recurrence. We categorized stage as I or II pathologically when the data were available (80% of the time) and clinically in the remainder of the women. Histologic grade was categorized as well differentiated, intermediate/moderately differentiated, poorly differentiated/undifferentiated/anaplastic, or not determined/stated. Estrogen and progesterone receptor protein status were classified as positive, negative, or indeterminate/other. Together, these data were combined to categorize risk of recurrence as minimal, intermediate, or high using the 1992 St Gallen criteria.²⁴

Dependent Analytic Variables
Other than standard primary tumor therapy. We compared women who received other than standard primary tumor therapy with women who received standard therapy, with standard primary tumor therapy defined as either BCS with axillary lymph node dissection followed by radiation therapy or modified radical mastectomy, in accordance with the 1990 National Institutes of Health Consensus Development Conference recommendations.²⁵ To better understand specific patterns of care, we examined the components of standard primary tumor therapy, comparing (1) women who did not receive an ALND with women who did (only two patients underwent SNB) and (2) women who did not receive radiation therapy after BCS with women who did. We also compared women who received mastectomy with women who received BCS.

Nonreceipt of systemic adjuvant therapy. We compared both women who did not receive a tamoxifen prescription with women who did and women who did not receive chemotherapy with women who did.

Data Analysis
We calculated the frequency and proportions of patient, tumor, and treatment characteristics in the four age groups. To identify factors associated with nonreceipt of treatments, we compared the patient and tumor characteristics of patients who received treatments with those of patients who did not. We used the Pearson ² to test the homogeneity of the proportions of patients receiving treatments in categories of the independent variables.

All factors found to be associated with treatments at the bivariate level (P < .1) were entered into multivariable logistic regression models (one for each dependent variable). These models were adjusted for age, race/ethnicity, comorbidity, and risk of recurrence, regardless of whether these variables met the model entry criterion of P < .1. We used Generalized Estimating Equations in SAS version 9 (SAS Institute, Cary, NC) to account for clustering by surgeon. The odds ratios represent the odds of not receiving indicated treatment if the patient was in the target category, relative to the reference category, adjusted for the other variables. Type 3 Generalized Estimating Equations analysis was performed to compute a score statistic to test for homogeneity of null odds ratios across covariate categories.²⁶

Because of the differences in patient ascertainment at sites with and without cancer registries, we conducted analyses including and not including the non–cancer registry sites. Because the results were comparable, we present the overall results only.

	RESULTS

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION Authors' Disclosures of... Author Contributions REFERENCES

 
We confirmed eligibility for 1,859 women, excluding 257 women whose medical records were not available. The 257 excluded women did not differ systematically from the 1,859 included women. The cohort was predominantly non-Hispanic white, and one fifth of patients were 80 years of age or older (Table 1). Patients were generally healthy, and most had tumors with favorable prognostic characteristics. The majority (80%) received standard primary tumor therapy. Approximately equal numbers of women received either a mastectomy or BCS, and most underwent ALND. Although only 39% of all study patients received radiation therapy, when the denominator was restricted to just those who received BCS, the proportion increased to 77%. Two thirds of patients received a prescription for tamoxifen, whereas only 10% received adjuvant chemotherapy. The oldest women had, in general, tumors with more favorable prognostic characteristics.

	DISCUSSION

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION Authors' Disclosures of... Author Contributions REFERENCES

 
In this study, which was conducted in a demographically and geographically diverse group of women diagnosed with early-stage breast cancer, older age and greater comorbidity burden were independently and inversely related to the receipt of standard primary therapy. Our findings are consistent with other recent studies^3,4,27,28 and extend them to integrated health care delivery system settings.

Baseline risk of recurrence was associated with the receipt of standard primary therapy, with women at lower initial risk being more likely to receive less than standard therapy. Although this may be appropriate, it is concerning that 16% of women at high risk did not receive standard primary tumor therapy. Considering risk of recurrence in older women is important because gains in life expectancy have occurred at the end of life; the average life expectancy of a 75-year-old woman is nearly 12 years (17 years if healthy), and the average life expectancy of an 85-year-old woman is 5.9 years (9.6 years if healthy).²⁹ These gains mean that older women with breast cancer have, on average, longer periods of time when they are at risk for recurrences than breast cancer patients diagnosed in the past.

Age and comorbidity were also associated with nonreceipt of ALND. These patterns are consistent with data from a similar time frame demonstrating that rates of ALND decreased sharply with age, with women 80+ years of age being nearly six times less likely to receive ALND compared with women 55 years of age or younger.³⁰ The arguments for or against ALND in early-stage breast cancer have shifted focus with the advent of SNB. Although the evidence supporting its use is based on only one published clinical trial, the American Society of Clinical Oncology has determined that SNB "is an appropriate initial alternative to routine staging ALND for patients with...clinically negative axillary nodes."³¹ The expert panel also observed that the odds of successful SNB decrease with increasing age.³² It is unclear how the decreasing accuracy of SNB with age will affect older women's treatment patterns and outcomes.

Although increasing age and comorbidity were also associated with the nonreceipt of radiation therapy, it is noteworthy that baseline recurrence risk was not. This difference may stem from the perception that older women, in general, are at lower risk of recurrence than are younger women and, thus, derive less benefit from radiation therapy. Clinical trial evidence supports this perception but only among node-negative women with small estrogen receptor protein–positive tumors.³³

Asian women were more likely to undergo mastectomy compared with white women. Recent studies of BCS in early-stage breast cancer patients^34-37 suggest that both patient and physician factors may account for the differences in mastectomy versus BCS between Asian/Pacific Islanders and non-Hispanic white women. These factors include poor cosmetic outcome, language barriers, physician concern regarding adherence to radiation therapy regimens, and patient preference. Patients at highest risk of recurrence were also more likely to undergo mastectomy, perhaps because of the recognition that BCS, even when followed by radiation therapy, is associated with an increased risk of recurrence relative to mastectomy.

We found that age and comorbidity were not related to receipt of BCS. Comorbidity has not consistently been considered as a covariate in prior studies in integrated health care settings.^15,38 Although previous studies have reported an inverse association of age with BCS among women with early-stage breast cancer,^4,39,40 at least two studies found that women with private insurance were more likely to have received BCS than women without private insurance.^5,39 The study by Riley et al¹⁵ was conducted during a slightly earlier time frame than our study and found that older women cared for in health maintenance organization settings were modestly more likely to undergo BCS and radiation therapy after BCS than women in fee-for-service settings (38.4% v 36.8% for BCS and 69% v 63.7% for radiation therapy, respectively); our figures were 46% and 77%, respectively.

We observed a reduced receipt of chemotherapy among the oldest women compared with the youngest women, which is consistent with available guidelines at the time of our study enrollment.²⁴ Differences in chemotherapy use by age in early-stage breast cancer have been well-documented,^4,27,41,42 and among those who do receive chemotherapy, older women are more likely to receive a lower dose-intensity.⁴³ The absence of sufficient clinical trial data among women greater than 70 years old and worries about toxicity have undoubtedly influenced clinical practice.

In contrast to the findings for chemotherapy, most studies, including ours, have not found an association between age and receipt of hormonal therapy,^4,27,41 suggesting that patients and their physicians agree that the benefits of hormonal therapy outweigh the risks.⁴⁴ In this study, however, 30% of women at high risk of recurrence at baseline did not receive tamoxifen.

An important limitation of this study was our inability to measure important factors in the treatment decision-making process. We were only able to collect information from automated data and medical records, which are typically poor sources of information about treatment decision making. Another limitation of our study is that our patients were diagnosed in the early to mid-1990s. Although care patterns have changed in the intervening years, with increasing use of BCS, radiation therapy after BCS, tamoxifen, and chemotherapy among older women,^27,45 age remains a strong predictor of how older women are treated.^46,47 Thus, our data remain relevant in the following three ways: (1) they provide comprehensive information about all aspects of breast cancer treatment received by older women in community settings not available for study using Medicare data; (2) age-dependent variations in care persist, and we still do not know how much of the variation is warranted; and (3) the variations in care observed have substantial relevance to the surviving women from this cohort and women like them who were diagnosed in the same timeframe, all of whom continue to be at risk for recurrence and breast cancer mortality. A strength of our work is that we were able to study a relatively unselected sample of older women with complete treatment data in integrated health care systems, where barriers to care have been minimized.

Our work demonstrates that age is an independent risk factor for nonreceipt of effective therapies, even when comorbidity and risk of recurrence are considered. To reduce these disparities will require high-quality evidence regarding treatment efficacy in older and sicker populations. Efficacy information and accurate tools that allow physicians and older patients to estimate the benefits versus the risks of therapies are critically needed. Older persons are heterogeneous with respect to functional reserve, comorbidity burden, and preferences, all of which need to be considered in the treatment decision-making process.

	Authors' Disclosures of Potential Conflicts of Interest

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION Authors' Disclosures of... Author Contributions REFERENCES

 
The authors indicated no potential conflicts of interest.

	Author Contributions

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION Authors' Disclosures of... Author Contributions REFERENCES

 

Conception and design: Shelley M. Enger, Diana S.M. Buist, Terry Field, Floyd Frost, Ann M. Geiger, Timothy L. Lash, Marianne Prout, Marianne Ulcickas Yood, Feifei Wei, Rebecca A. Silliman Administrative support: Rebecca A. Silliman Provision of study materials or patients: Shelley M. Enger, Diana S.M. Buist, Terry Field, Floyd Frost, Ann M. Geiger, Marianne Ulcickas Yood, Feifei Wei Collection and assembly of data: Shelley M. Enger, Soe Soe Thwin, Diana S.M. Buist, Terry Field, Floyd Frost, Ann M. Geiger, Marianne Ulcickas Yood, Feifei Wei, Rebecca A. Silliman Data analysis and interpretation: Shelley M. Enger, Soe Soe Thwin, Diana S.M. Buist, Terry Field, Floyd Frost, Ann M. Geiger, Timothy L. Lash, Marianne Prout, Marianne Ulcickas Yood, Feifei Wei, Rebecca A. Silliman Manuscript writing: Shelley M. Enger, Soe Soe Thwin, Diana S.M. Buist, Terry Field, Floyd Frost, Ann M. Geiger, Timothy L. Lash, Marianne Prout, Marianne Ulcickas Yood, Feifei Wei, Rebecca A. Silliman Final approval of manuscript: Shelley M. Enger, Soe Soe Thwin, Diana S.M. Buist, Terry Field, Floyd Frost, Ann M. Geiger, Timothy L. Lash, Marianne Prout, Marianne Ulcickas Yood, Feifei Wei, Rebecca A. Silliman

 

	ACKNOWLEDGMENTS

 
We thank the people who supported this project including the site project managers, programmers, and medical record abstractors: Group Health Cooperative: Linda Shultz, Kristin Delaney, Margaret Farrell-Ross, Mary Sunderland, Millie Magner, and Beth Kirlin; Meyers Primary Care Institute of Fallon Community Health Plan: Kimberly Hill, Jackie Fuller, Doris Hoyer, and Janet Guilbert; Henry Ford Health System: Sharon Hensley Alford, Karen Wells, Patricia Baker, and Rita Montague; HealthPartners: Maribet McCarty and Alex Kravchik; Kaiser Permanente Southern California: Julie Stern, Janis Yao, Michelle McGuire, Erica Hnatek-Mitchell, and Noemi Manlapaz; and Lovelace Health Plan: Judith Hurley, Hans Petersen, and Melissa Roberts.

	NOTES

 
Supported by Public Health Service Grant No. R01 CA093772 from the National Cancer Institute, National Institutes of Heath, Department of Health and Human Services.

Authors' disclosures of potential conflicts of interest and author contributions are found at the end of this article.

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Submitted February 22, 2006; accepted May 11, 2006.

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