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Surveillance Testing Among Survivors of Early-Stage Breast Cancer

Nancy L. Keating, Mary Beth Landrum, Edward Guadagnoli, Eric P. Winer, John Z. Ayanian

From the Division of General Internal Medicine, Department of Medicine, Brigham and Women's Hospital; Department of Health Care Policy, Harvard Medical School; and the Department of Adult Oncology, Dana-Farber Cancer Institute, Boston, MA

Address reprint requests to Nancy L. Keating, MD, MPH, Department of Health Care Policy, Harvard Medical School, 180 Longwood Ave, Boston, MA 02115; e-mail: keating{at}hcp.med.harvard.edu

	ABSTRACT

TOP ABSTRACT INTRODUCTION METHODS RESULTS DISCUSSION AUTHORS' DISCLOSURES OF... AUTHOR CONTRIBUTIONS Appendix REFERENCES

 
Purpose: Guidelines recommend against routine surveillance testing for women who have had breast cancer. We described follow-up care for breast cancer survivors, examined how surveillance testing varies by the types of physicians seen, and assessed changes in testing rates over time.

Methods: Using Surveillance, Epidemiology, and End Results–Medicare data, we studied a population-based cohort of 44,511 women age 65 years diagnosed with stage I/II breast cancer during 1992 to 1999 and observed through 2001. We measured bone scans, tumor antigen tests, chest x-rays, and other chest/abdominal imaging during 3 consecutive surveillance years. We described physicians seen in follow-up and used repeated-measures logistic regression to assess the relationship with testing and to assess testing trends over time.

Results: Nearly half of breast cancer survivors saw a medical oncologist in surveillance year 1, but only 27% saw a medical oncologist annually for 3 years. In adjusted analyses, women seeing medical oncologists had more bone scans, tumor antigen testing, chest x-rays, and chest/abdominal imaging than other women (all P < .001). Nevertheless, rates of testing decreased over time (all P < .001). Rates of tumor antigen testing and chest x-rays decreased faster and chest/abdominal imaging increased slower among women seeing medical oncologists than among other women (all P < .05).

Conclusion: Nonrecommended testing for early-stage breast cancer patients has decreased over time. Although most breast cancer survivors did not see oncologists annually, those who did had substantially higher rates of testing than others; whether such testing in this low-risk population was due to more symptoms or excessive surveillance is an important question for additional study.

	INTRODUCTION

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With more than 200,000 women diagnosed with invasive breast cancer yearly,¹ more than 2 million breast cancer survivors are currently alive in the United States.² National guidelines recommend that women with a history of breast cancer undergo annual mammography but advise against other routine surveillance testing (at regular predefined intervals), including complete blood counts, chemistry studies, chest x-rays, bone scans, liver ultrasounds, abdominal computed tomography scans, and tumor markers.^3-5 These recommendations are based on randomized studies demonstrating that routine testing for distant metastatic disease provides no benefit in survival or health-related quality of life.^6-8 Moreover, intensive surveillance costs from $260 million to $630 million more annually than an approach that includes only history, physical examination, mammography, and additional testing when indicated.^9-11

Despite the lack of evidence supporting routine surveillance testing other than mammography for breast cancer survivors and the recommendations against its use, such testing is performed by many physicians,^12-16 under the assumption that detecting and treating recurrences early results in better outcomes. Because many physicians, particularly medical oncologists,¹⁷ may favor intensive surveillance, the types of physicians seen by patients after breast cancer diagnosis and treatment may influence the surveillance care received. Moreover, recent reports emphasize the importance of coordination of care for cancer survivors,^5,18 and better coordination may limit unnecessary testing. Few data are available about the mix of physicians caring for breast cancer survivors or the associated patterns of surveillance testing. In a prior study, we identified underuse of surveillance mammography among breast cancer survivors, with higher rates of mammography among women who visited cancer specialists in the years after diagnosis.¹⁹

In this study, we assessed bone scans, tumor antigen testing, chest x-rays, and other chest/abdominal imaging over a 3-year period in a population-based cohort of early-stage breast cancer survivors at low risk for recurrence. We described patterns of follow-up care and examined how testing varied by the types of physicians seen after primary treatment. In addition, we examined trends in testing over time to assess whether practice changed after studies and guidelines related to surveillance testing were published.^3,4,6,7

	METHODS

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Data and Patients
The study methods have been described in detail previously.¹⁹ Briefly, we used the Surveillance, Epidemiology, and End Results–Medicare data,²⁰ which combine uniformly reported data from 11 population-based cancer registries covering approximately 14% of the United States population²¹ with Medicare claims data. The study cohort included 44,511 women with a first diagnosis of stage I/II breast cancer during 1992 to 1999, who were 65 years old and enrolled in Parts A and B of fee-for-service Medicare when diagnosed, and who underwent primary surgery.¹⁹ We censored patients at the end of 2001 or sooner (if they died), discontinued enrollment from Parts A and B fee-for-service Medicare, developed a new cancer, or had evidence of a possible recurrence, using a relatively conservative definition of recurrence to ensure we had disease-free cohorts for assessment of surveillance testing.¹⁹

Because mammography peaks in 1-year intervals after diagnosis^19,22 and because we did not want to capture testing associated with primary treatment, we defined 3 surveillance years: months 7 to 18, 19 to 30, and 31 to 42 after diagnosis. For inclusion in analyses of a surveillance year, women had to be alive and not censored through the end of that surveillance year. Of the 44,511 early-stage breast cancer survivors, 37,967 were observed through surveillance year 1, 30,406 were observed through surveillance year 2, and 23,016 were observed through surveillance year 3.¹⁹

Surveillance Testing
We identified bone scans, tumor antigen testing, chest x-rays, and chest/abdominal imaging (computed tomography, magnetic resonance imaging, and ultrasound) based on inpatient, outpatient, and physician supplier files (Appendix Table A1, online only). For each 12-month surveillance period, we assessed whether at least one of each type of test was performed, recognizing that this would underestimate the total extent of testing. We originally examined each subcategory of tumor markers and chest/abdominal imaging separately; however, because the numbers were small for some subcategories and patterns of testing were similar, we combined them into the larger categories (Appendix Table A1). For analyses examining testing over time, we also assessed mammography (recommended annually).

Visits With Physicians
We identified all outpatient visits with physicians (Appendix Table A1) and obtained each physician's specialty after linking with the American Medical Association Physician Masterfile.²³ We categorized each physician's self-reported primary specialty as primary care physician (family practice, internal medicine, general practice, geriatrics), medical oncologist, general surgeon (including a small number of surgical oncologists), radiation oncologist, medical subspecialist (eg, cardiologist, endocrinologist), surgical subspecialist (eg, vascular surgeon, thoracic surgeon), or other specialist (eg, obstetrician/gynecologist [rarely seen by these elderly cancer survivors], dermatologist, ophthalmologist). We also calculated the total number of office visits during each surveillance year.

Control Variables
The Surveillance, Epidemiology, and End Results registries document each patient's age at diagnosis, race, Hispanic ethnicity, marital status, history of other cancer, residence in a metropolitan county, and tumor characteristics. We characterized education and income of the census tract of residence using 1990 Census data, classified into quartiles within the registry before combining across registries to avoid misclassification due to regional variations. We measured comorbid illness using Diagnostic Cost Group (DCG) scores,²⁴ a risk-adjustment tool used by the Centers for Medicare & Medicaid Services to predict disease burden and future costs for Medicare beneficiaries using diagnostic information from inpatient and ambulatory claims. DCGs capture 184 conditions (v 18 for the Charlson score²⁵), predict mortality in cancer patients,²⁶ and may also capture patients’ propensity to seek health care services. We calculated summary DCGs scores (excluding breast cancer codes) based on the 12-month period beginning at the month of diagnosis to characterize illness at a time when decisions about testing would be made. Finally, we used registry data and claims^19,27-30 to classify primary treatment as mastectomy, breast-conserving surgery with radiation, or breast-conserving surgery without radiation. Variables are categorized as in Table 1.

For each category of test, we used repeated-measures logistic regression with generalized estimating equations³¹ to assess the odds of testing associated with seeing a certain provider type, adjusting for the patient characteristics described, and visits (categorized in quintiles for each surveillance year). The modeling strategy allowed women to be included in analyses for all surveillance years in which they had complete data and allowed estimates of the effect of seeing certain types of providers in only some surveillance years. For example, if a patient saw a medical oncologist in years 1 and 3, information from both years 1 and 3 is used in estimating the effect of seeing a medical oncologist on testing.

We examined change in mammography rates and other testing over time using indicator variables for year of diagnosis and calculated P values for the overall effect of year of diagnosis on testing. We calculated adjusted predicted rates of testing according to year of diagnosis using regression model coefficients.³² These predicted rates reflect the average rates of testing for the surveillance years for which each patient has complete data. We also tested the interaction of diagnosis year and visits with a medical oncologist. Because analyses suggested linear trends in testing, we modeled year of diagnosis in these models as a continuous effect.

Given that many women saw more than one type of provider in a given year, we repeated the models after categorizing women into four exclusive categories reflecting types of providers seen during each surveillance year: primary care provider but no cancer specialist (medical oncologist, radiation oncologist, surgeon; reference group), cancer specialist but no primary care provider, both cancer specialist and primary care provider, and neither cancer specialist nor primary care provider.

All tests of statistical significance were two sided. We converted adjusted odds ratios to risk ratios to better reflect the true relative risks.³³ We conducted analyses using SAS statistical software, version 8.2 (SAS Institute Inc, Cary, NC). The Harvard Medical School Committee on Human Studies approved the study protocol.

	RESULTS

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The mean age of the 44,511 breast cancer survivors was 75.3 years at diagnosis and 11% were nonwhite (Table 1). Of 37,967 patients observed throughout surveillance year 1, 13.3% had at least one bone scan, 29.2% had a tumor antigen test, 10.9% had chest/abdominal imaging, and 58.8% had a chest x-ray during surveillance year 1. Of 23,016 patients observed through the end of surveillance year 3, 2.1% had yearly bone scans, 16.0% had yearly tumor antigen testing, 1.0% had yearly chest/abdominal imaging, and 29.2% had yearly chest x-rays.

Most breast cancer survivors visited a primary care provider during surveillance year 1 (Table 2), although only 51% did so annually during 3 years. Forty-two percent of patients saw a medical oncologist in year 1, 46% saw a general surgeon, and 24% saw a radiation oncologist, but few patients saw these types of physicians annually. For example, only 27% saw a medical oncologist annually; those who did were younger (73.4 v 75.3 years; P < .001),were more often diagnosed with stage 2 cancers (47.8% v 31.1%; P < .001), and had lower comorbidity scores (0.57 v 0.62; P < .001), but did not differ by race (4.6% v 4.9% were black; P = .27).

View larger version (17K): [in this window] [in a new window] [PowerPoint Slide for Teaching]   Fig 1. Adjusted rates of testing by year of diagnosis reflect testing performed during up to 3 surveillance years after diagnosis; therefore, rates reflect testing performed during 1993 through 2002. Women are included for each surveillance year for which they have complete data. P values reflect the overall effect of diagnosis year on testing from repeated measures models. CT, computed tomography; MRI, magnetic resonance imaging; CXR, chest x-ray; RCT, randomized controlled trial; ASCO, American Society of Clinical Oncology.

View larger version (9K): [in this window] [in a new window] [PowerPoint Slide for Teaching]   Fig 2. Adjusted risk ratios and 95% CIs for seeing a provider of each type (v not seeing a provider of that type) during a surveillance year, using repeated-measures logistic regression with generalized estimating equations to adjust for patient and tumor characteristics. Repeated-measures models allowed estimates of the effect of seeing certain types of providers in only some surveillance years. PCP, primary care physician.

When we categorized women based on combinations of physicians seen in any particular year, we found that compared with women who saw a primary care provider but no cancer specialists, women who saw other combinations of providers had higher rates of bone scans, tumor antigen testing, and abdominal/chest imaging (Table 4).

	DISCUSSION

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Despite relatively high rates of testing overall, we observed that rates of nonrecommended testing generally decreased over time, whereas mammography increased over time. These changes were more pronounced for patients seeing medical oncologists, suggesting that medical oncologists were most influenced by results of clinical trials and guidelines related to surveillance testing published during the 1990s.^3,4,6,7

As the proportion of women diagnosed with early-stage breast cancer increases, so too does the population of breast cancer survivors, emphasizing the importance of follow-up care for these women. Randomized controlled trials have found that routine testing for distant metastatic disease provides no benefit in survival or health-related quality of life,^6-8 and an intensive approach to surveillance is costly.^9-11 Moreover, although many physicians¹⁷ and patients³⁴ may favor intensive surveillance, patients overestimate the value of laboratory and imaging studies and may incorrectly perceive the significance of a normal test.³⁴

It is unclear which type of provider is most suitable to care for breast cancer survivors. According to guidelines, physicians should be experienced in the surveillance of cancer patients and in the examination of irradiated and normal contralateral breasts, and care should be coordinated and not duplicated by multiple specialists.^3,5 Data suggest that follow-up care need not be performed by a cancer specialist. British and Canadian trials comparing primary care–centered and specialist-centered follow-up of breast cancer patients found no difference in time to diagnosing recurrence, anxiety, or quality of life^35,36; in addition, patients observed in primary care settings were more satisfied.³⁷

Nevertheless, British and Canadian data suggest that although generalist physicians are comfortable or even prefer taking primary responsibility for routine follow-up of their breast cancer patients,^38,39 most breast cancer specialists prefer to continue observing their patients and do not believe that general practitioners have the necessary skills to provide adequate follow-up care.³⁸ Although data suggest that breast cancer surveillance care is being provided primarily by specialists,^39,40 these and other^14-16 studies of surveillance testing included relatively small samples of patients treated at cancer centers, large hospitals, or large group practices. Given that breast cancer survivors remain at risk of recurrence for 20 years or more,³ it may be impractical for patients to continue to visit cancer specialists for extended periods of time, especially as they age and develop conditions requiring the expertise of other physicians.

Our finding that most older survivors of early-stage breast cancer in the United States do not visit a medical oncologist or other cancer specialist annually heightens the need to ensure that generalist physicians have the skills to care for cancer survivors, are aware of current recommendations, and can communicate with cancer specialists when necessary. This may be especially important because although elderly patients who do not follow up with cancer specialists receive fewer nonrecommended tests than other women, they also receive fewer surveillance mammograms.^19,41 Patients and their physicians would benefit from greater education about surveillance care recommendations.⁵ In addition, a clear plan regarding which doctor is primarily responsible for patients’ routine follow-up care, including a schedule for visits and testing that patients should expect,¹⁸ would likely increase mammography rates and decrease rates of nonrecommended testing, and could also alert patients and physicians about symptoms that might prompt additional testing. Such a plan could be developed by a patient's oncologist after primary treatment is completed.¹⁸ Finally, better communication among providers sharing re-sponsibility for a patient's care, perhaps using innovative electronic applications, could help to decrease duplicate testing and expedite evaluation of symptoms when necessary.

Our study has several limitations. First, our data do not allow us to ascertain whether tests were ordered for surveillance or evaluation of symptoms. The patterns of use for some tests (eg, more abdominal/chest imaging among patients who did not see a primary care physician or cancer specialist) suggest that not all tests were performed for breast cancer surveillance. Such noncancer specialists may have a low threshold for ruling out cancer recurrence when patients present with nonspecific symptoms or they may be more closely monitoring other conditions. However, the high rates of annual testing for some tests in our low-risk population suggest that they are being ordered routinely. Similarly, our data are not well suited to assess whether more testing led to identification of recurrences; this issue has been addressed more effectively in randomized clinical trials.^6-8

Second, we used a claims-based algorithm for identifying potential recurrences to exclude women whose testing was unlikely to be routine, and may have misclassified some women. However, our conservative algorithm was more likely to exclude women without recurrences than to include women who had experienced recurrence, which would underestimate testing among low-risk patients. Third, our method for identifying provider specialty may have misclassified some physicians, particularly those with more than one specialty or practice site. Even so, the American Medical Association data may be the most reliable source of physician specialty.²³ Finally, we ascertained receipt of at least one test in each surveillance year, not every test, so our study underestimates the total amount of testing.

In conclusion, our findings demonstrate a high rate of nonrecommended testing associated with surveillance after treatment for early-stage breast cancer, suggesting that these tests may be overused. Testing patterns for our low-risk cohort of patients may underestimate the extent of testing among breast cancer survivors as a whole. Although most breast cancer survivors did not see a cancer specialist annually, those who did had substantially more testing. Given the high cost of breast cancer surveillance testing, eliminating unnecessary testing could provide substantial savings.

	AUTHORS’ DISCLOSURES OF POTENTIAL CONFLICTS OF INTEREST

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Although all authors completed the disclosure declaration, the following author or immediate family members indicated a financial interest. No conflict exists for drugs or devices used in a study if they are not being evaluated as part of the investigation. For a detailed description of the disclosure categories, or for more information about ASCO's conflict of interest policy, please refer to the Author Disclosure Declaration and the Disclosures of Potential Conflicts of Interest section in Information for Contributors.

Employment: N/A Leadership: N/A Consultant: John Z. Ayanian, DxCG Inc Stock: N/A Honoraria: N/A Research Funds: N/A Testimony: N/A Other: N/A

	AUTHOR CONTRIBUTIONS

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Conception and design: Nancy L. Keating, Mary Beth Landrum, Edward Guadagnoli, Eric P. Winer, John Z. Ayanian

Financial support: Nancy L. Keating

Collection and assembly of data: Nancy L. Keating

Data analysis and interpretation: Nancy L. Keating, Mary Beth Landrum, Edward Guadagnoli, Eric P. Winer, John Z. Ayanian

Manuscript writing: Nancy L. Keating, Mary Beth Landrum, Eric P. Winer, John Z. Ayanian

Final approval of manuscript: Nancy L. Keating, Mary Beth Landrum, Edward Guadagnoli, Eric P. Winer, John Z. Ayanian

	Appendix

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	ACKNOWLEDGMENTS

 
This study used the linked Surveillance, Epidemiology, and End Result (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 Program, National Cancer Institute; the Office of Research, Development and Information, Centers for Medicare and Medicaid Services, Information Management Services Inc; and the SEER Program tumor registries in the creation of the SEER-Medicare database. We thank Laurie Meneades, MS, for expert programming assistance.

	NOTES

 
Supported by a Clinical Scientist Development Award from the Doris Duke Charitable Foundation (N.L.K.).

The funding organization had no role in design and conduct of the study; collection, management, analysis, and interpretation of the data; or preparation, review, or approval of the manuscript.

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

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Submitted August 10, 2006; accepted December 12, 2006.

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 Citing Articles Citing Articles via Google Scholar Google Scholar Articles by Keating, N. L. Articles by Ayanian, J. Z. Search for Related Content PubMed PubMed Citation Articles by Keating, N. L. Articles by Ayanian, J. Z.