Originally published as JCO Early Release 10.1200/JCO.2006.09.9572 on June 4 2007

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Mammography Surveillance and Mortality in Older Breast Cancer Survivors

Timothy L. Lash, Matthew P. Fox, Diana S.M. Buist, Feifei Wei, Terry S. Field, Floyd J. Frost, Ann M. Geiger, Virginia P. Quinn, Marianne Ulcickas Yood, Rebecca A. Silliman

From the Departments of Epidemiology and International Health, Boston University School of Public Health; Geriatrics Section, Department of Medicine, Boston University School of Medicine, Boston; University of Massachusetts Medical School, Worcester; Fallon Community Health Plan, Worcester, MA; Group Health Center for Health Studies, Seattle, WA; HealthPartners Research Foundation, Minneapolis, MN; Lovelace Health Systems, Albuquerque, NM; Wake Forest University School of Medicine, Winston-Salem, NC; Kaiser Permanente Southern California, Pasadena, CA; Henry Ford Health System, Detroit, MI; and the Yale University School of Medicine, New Haven, CT

Address reprint requests to Timothy L. Lash, DSc, Department of Epidemiology, Boston University School of Public Health, 715 Albany St, TE3, Boston, MA 02118; e-mail: tlash{at}bu.edu

	ABSTRACT

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Purpose There are more than 2,000,000 breast cancer survivors in the United States today. While surveillance for asymptomatic recurrence and second primary is included in consensus recommendations, the effectiveness of this surveillance has not been well characterized. Our purpose is to estimate the effectiveness of surveillance mammography in a cohort of breast cancer survivors with complete ascertainment of surveillance mammograms and negligible losses to follow-up.

Patients and Methods We enrolled 1,846 stage I and II breast cancer patients who were at least 65 years old at six integrated health care delivery systems. We used medical record review and existing databases to ascertain patient, tumor, and therapy characteristics, as well as receipt of surveillance mammograms. We linked personal identifiers to the National Death Index to ascertain date and cause of death. We matched four controls to each breast cancer decedent to estimate the association between receipt of surveillance mammogram and breast cancer mortality.

Results One hundred seventy-eight women died of breast cancer during 5 years of follow-up. Each additional surveillance mammogram was associated with a 0.69-fold decrease in the odds of breast cancer mortality (95% CI, 0.52 to 0.92). The protective association was strongest among women with stage I disease, those who received mastectomy, and those in the oldest age group.

Conclusion Given existing recommendations for post-therapy surveillance, trials to compare surveillance with no surveillance are unlikely. This large observational study provides support for the recommendations, suggesting that receipt of surveillance mammograms reduces the rate of breast cancer mortality in older patients diagnosed with early-stage disease.

	INTRODUCTION

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More than 2,000,000 living women in the United States have survived breast cancer,¹ more than half of whom are older than 65.² Guidelines for the care of breast cancer survivors after they complete primary therapy recommend annual history, physical examination, and surveillance mammogram.^3,4 A primary objective of postbreast cancer therapy surveillance is to detect potentially curable conditions, such as local recurrence of cancer in the breast after breast-conserving surgery and new cancers in the contralateral breast.⁵

No clinical trial evidence supports the guideline recommendations for receipt of an annual surveillance mammogram,^4-7 yet in the presence of these guidelines, it would be unethical to randomly assign women to receive less than guideline surveillance. Trials of screening mammography have seldom included older women,⁸ and healthy older women receive screening mammography less often than recommended.⁹ Observational studies must therefore provide estimates of the effectiveness in older women of guideline surveillance or its components, such as annual surveillance mammogram.

In earlier cohort studies, we reported protective associations between receipt of guideline surveillance and breast cancer mortality¹⁰ and all-cause mortality.¹¹ However, these studies were limited by small sample size, incomplete assessment of receipt of surveillance mammograms, and potentially differential losses to follow-up. The objective of this investigation was to estimate the effect of surveillance mammograms on the rate of breast cancer mortality in a large cohort of older breast cancer survivors without selection bias and with complete ascertainment of post-therapy surveillance mammograms.

	PATIENTS AND METHODS

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We have previously described the study design and data collection methods,¹² which were approved by institutional review boards at the coordinating center and enrollment sites and were conducted in accord with an assurance filed with and approved by the Department of Health and Human Services.

Population
We identified potentially eligible women age 65 years or older with histologically confirmed American Joint Committee on Cancer (AJCC)¹³ stage I, IIA, or IIB breast cancer diagnosed from 1990 through 1994. Eligible women were enrolled at one of six geographically dispersed integrated health care delivery systems (networks of care providers and organizations that offer coordinated health care services to a defined population and assume clinical and fiscal accountability for clinical outcomes¹⁴) participating in the National Cancer Institute–funded Cancer Research Network (CRN; Group Health, Washington; Kaiser Permanente-Southern California; Lovelace Health Systems, New Mexico; Henry Ford Health System, Michigan; HealthPartners, Minnesota; and the Meyers Primary Care Institute of Fallon Community Health Plan/Fallon Foundation/University of Massachusetts Medical School, Massachusetts), for at least 1 year before and after diagnosis, unless they died within the first year after diagnosis. At the time of this study, the CRN included the research programs, enrollee populations, and data systems of these six and five other integrated health care systems. The six sites were selected from 11 to optimize the geographic and ethnic diversity of the study population. The goal of the CRN is to conduct research that improves the prevention, management, and outcomes of cancer.

We excluded women with bilateral breast cancer or other malignancies, except nonmelanoma skin cancer, diagnosed within 5 years before or 30 days after the incident breast cancer diagnosis.

Data Collection
Whenever possible, we initially populated the study's database with electronically available data (date of birth, race/ethnicity, date of diagnosis, eligibility criteria, and cancer characteristics). We verified preloaded data by medical record review, except elements reported to the sites by the National Cancer Institute's Surveillance, Epidemiology and End Results registry¹⁵ (stage characteristics, histology, and estrogen receptor expression). We verified, or completed, all other data elements (demographic, tumor, treatment, comorbidity, and follow-up data) by medical record review. One person trained all medical record reviewers at all sites using a standardized training procedure. Medical record reviews were conducted on site by the trained abstractors, and the data were entered directly into a computer-based data collection system.¹⁶

We ascertained vital status by matching participants' identifying information to the records of the National Death Index through December 31, 2004. We cross-checked the National Death Index matches against vital status information available at the enrollment sites.

Analytic Variables
Follow-up time. We defined the start of follow-up as beginning 90 days after finishing the last portion of initial treatment for breast cancer (surgery, radiation therapy, or chemotherapy, but not including hormone therapy), and follow-up continued until the first end of follow-up event (death, disenrollment from the health care system, or the completion of 5 years of follow-up).

Breast cancer mortality: nested cases and controls. Patients were women identified with breast cancer as the cause of death with International Classification Diagnosis (ICD)-9 code 174 or ICD-10 code C50 in the underlying cause of death field or any line of part I of the death certificate. For each case, we defined a risk set as those subjects observed at least as long as the case and matched to the case on enrollment site, age category, AJCC stage,¹⁰ primary surgery type (mastectomy, breast-conserving surgery, or other), and baseline Charlson comorbidity index.¹⁷ We selected four unique controls at random from each case's risk set when the risk set contained more than four subjects, and selected the whole risk set to be the case's controls when the risk set contained four or fewer subjects.

Surveillance mammograms. We instructed medical record reviewers to distinguish surveillance mammograms separately from mammograms ordered for evaluation of a clinical finding (with or without clinical findings), work-up of abnormal mammogram, and evaluation of breast after biopsy or surgery. Of 163 mammogram records re-reviewed by experienced reviewers at each site, 145 (89%) agreed with respect to the reason the mammogram had been ordered.

We counted the number of surveillance mammograms received from the first day of surveillance until 6 months before the date of death for cases or, for controls, before the follow-up time accrued to 6 months before the date of death of the matched case. We excluded mammograms fewer than 9 months from the preceding mammogram¹⁸ because repeated mammograms ordered to follow suspicious initial findings would tend to increase the number of mammograms counted among women with recurrences or second primary breast cancer, inducing a bias toward the null. We did not count surveillance mammograms after the date of a patient's local, regional, or distant recurrence or second primary breast cancer. For controls, we did not count mammograms after the follow-up time accrued by the date of the local, regional, or distant recurrence or second primary breast cancer of the matched patient.

Candidate confounders. We classified women by year of diagnosis, age at diagnosis (65 to 69, 70 to 79, and 80 or older years), and by race/ethnicity (white non-Hispanic, Asian, African American, white Hispanic, and other/unknown). We collected information on comorbid conditions and calculated the Charlson comorbidity index¹³ in the year preceding breast cancer diagnosis (baseline), 1 year after diagnosis, and 3 years after diagnosis. We matched controls to cases on baseline Charlson comorbidity category (0, 1, or 2/3), as originally defined,¹³ and we adjusted for change in Charlson comorbidity category between baseline and the last Charlson measurement before the index date (death for cases and the matched cases' date of death for controls). We collected information on tumor stage¹⁰ (stage I, IIA, or IIB) and estrogen receptor status (positive, negative, or other) at diagnosis. Finally, we gathered information on primary surgery type (breast-conserving surgery, mastectomy, or other), receipt of radiation therapy (completed or not), and systemic therapies (any tamoxifen, any chemotherapy, or both, v none).

Statistical Analysis
We calculated the frequency and proportion of the cohort observed for at least 6 months, and the frequency of the cases and controls within strata of the candidate confounders. We calculated the crude odds ratios and 95% CIs associating covariates with breast cancer mortality. Given the control sampling strategy, the odds ratio estimates the hazard ratio. We fit a conditional logistic regression model to calculate the odds ratios and 95% CIs, conditioned on the matched factors. We examined the association between the number of surveillance mammograms received and breast cancer mortality, and then also adjusted for a subset of the candidate confounders. We selected this subset by the forward model-building strategy suggested by Greenland,¹⁹ based on a 10% change in the estimate of effect for the main exposure. If no adjustment variables changed the estimate of effect by 10% or more, we adjusted only for change in Charlson comorbidity index from baseline. We examined modification of the association between receipt of each additional surveillance mammogram and breast cancer mortality within strata of age at diagnosis, stage at diagnosis, baseline Charlson comorbidity index, and type of initial surgery. To further understand the role of surveillance in preventing death from breast cancer, we compared the pattern of receipt of surveillance mammograms in women with recurrences who died of breast cancer in the first 5 years of follow-up with the pattern in women with recurrences who did not die of breast cancer in that time period.

Finally, we repeated the methods and analysis—with cases defined as those who died from causes other than breast cancer and controls matched to these decedents—to examine whether the association was specific to deaths from breast cancer.

	RESULTS

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We enrolled 1,846 breast cancer patients to contribute to this analysis. We identified 178 breast cancer decedents during the first 5 years of follow-up and matched 634 controls to these patients. Most women were 70 to 79 years old at diagnosis (46%) and white non-Hispanic (82%; Table 1). The majority of the controls had no (40%) or only one (32%) surveillance mammogram during a mean of 31.8 months of follow-up (interquartile range, 20.2 to 43.9 months). Only 13 (2.0%) of 634 controls had four or more surveillance mammograms. As presented in Table 1, the first surveillance mammogram was associated with a protective effect against breast cancer mortality, and the protective effect grew stronger with receipt of each additional surveillance mammogram.

	DISCUSSION

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The estimate of a nearly one-third reduction in mortality rate associated with each additional surveillance mammogram supports one of the objectives of the published guidelines for follow-up care of breast cancer survivors.^3,4 The reduced mortality rate likely results from the effect of detecting local recurrences or second primary breast cancer at an earlier stage with better prognosis, combined with the effect of better medical care in general, as evinced by the lower mortality rate from causes other than breast cancer. Indeed, breast cancer survivors who have guideline surveillance are more likely to receive other preventive care than matched controls.²¹

The potential for regular surveillance to reduce the breast cancer mortality rate may be met with some skepticism, particularly since the difference in the proportions of survivors and decedents who received surveillance mammograms was limited to women with local recurrences. While this finding is exactly as expected, given that mammograms can only detect tumors in the breast, the vast majority of recurrences even among survivors were regional (19%) or distant (56%), so would not have been detected by mammograms. It is possible, however, for a surveillance mammography program to confer benefits beyond the test result itself. For example, women who regularly receive surveillance mammograms may be more likely than women who do not regularly receive surveillance mammograms to seek medical attention at the first sign or symptom of a recurrence, which may be associated with earlier detection of the recurrence and improved prognosis. We also note that asymptomatic surveillance aimed at detecting second primary cancers in the contralateral breast of breast cancer survivors is equivalent to screening a high-risk population,²² and our estimate of protective effect is about the same size as has been observed in trials of screening mammography.²³

Nonetheless, it is often held that surveillance testing confers no survival benefit,^24-28 which likely derives from incomplete understanding of three topics. These are the misperception that clinical trials of surveillance testing have had null results; the notion that recurrent breast cancer is incurable; and the observation that comparisons of survival among women with local, regional, or distant metastases detected asymptomatically versus symptomatically have failed to demonstrate a difference. None of these three suppositions directly refutes the potential protective effect of guideline surveillance on breast cancer mortality.

First, no clinical trial has randomly assigned breast cancer patients to receipt of guideline surveillance versus receipt of no surveillance.⁶ Rather, they have compared intensive surveillance (eg, bone scan, liver sonography, chest x-ray, laboratory tests, physical examination, and annual mammogram) with less-intensive surveillance (eg, physical examination and annual mammogram).^29,30 All trial participants therefore received a minimum of annual mammogram and physical examination, so the effect of surveillance mammograms could not be assessed. Second, local recurrences of breast cancer can be effectively treated. The 5-year survival proportion for breast cancer patients after recurrence confined to the breast parenchyma or skin of the ipsilateral breast is approximately 60%, but the survival proportion is only 24% for recurrence involving regional nodes or recurrence in the nonbreast skin of the ipsilateral chest wall.³¹ Last, comparisons of breast cancer patients with local/regional recurrences or distant metastases detected asymptomatically by intensive surveillance, versus those diagnosed symptomatically, have observed no substantial differences in survival.^22,32-37 These comparisons were meant to assess the effect of surveillance procedures such as chest x-ray on metastatic disease, not the effect of surveillance mammography on local recurrence or second primary and subsequent breast cancer mortality.

Because this study was housed in the health care systems of the CRN, its design provides substantial advantages over previous studies that reported a protective effect of post-therapy surveillance.^7,8 To begin, we ascertained surveillance mammograms ordered by any physician or program connected with the patient's health care system, whereas earlier studies were unable to ascertain surveillance mammograms ordered by primary care physicians and/or some cancer specialists. Next, the cohort had sufficient power to examine deaths attributed to breast cancer, rather than all-cause mortality, which resulted from the large sample size available within the CRN. Last, because the investigation relied on existing registries and medical records, all patients could be included with negligible loss to follow-up, reducing the potential impact of selection biases and selective loss to follow-up.

Despite these strengths, the results must be considered with the study's limitations in mind. Most important, patients received surveillance mammograms in the context of conventional patient-physician decision making, not by a random assignment scheme. Factors related to receipt of surveillance mammograms and survival, such as healthy behaviors and physical function not captured by the comorbidity index, may confound the relation. While we controlled for many such factors—including age, stage, comorbidity over the course of follow-up, primary therapy, and adjuvant therapies—unmeasured indications for receipt of surveillance mammograms among healthier women may confound the association. We observed the same size protective association between receipt of surveillance mammogram and mortality from causes other than breast cancer as we did for breast cancer mortality, which emphasizes the potential for confounding by indication to account for at least part of the protective effect.

We ascertained vital status by matching identifying characteristics with the National Death Index, which has high sensitivity and specificity for death ascertainment. The accuracy of ascertaining mortality should be independent of surveillance classification, since those who matched participants to the mortality databases were blinded to the surveillance history of the participants. Misclassification of the fact of death or its cause would bias toward the null.

With extant guidelines that recommend annual surveillance mammograms for breast cancer survivors, it is unlikely that a trial will be undertaken to investigate the efficacy of post-therapy surveillance. This large study with nearly complete follow-up and ascertainment of nearly all mammograms, regardless of how they were ordered, supports the hypothesis that regular post-therapy surveillance reduces the rate of breast cancer mortality. It is likely, though, that the reduction results from the combination of a direct protective effect and better preventive and chronic illness care in general practiced and received by the breast cancer patients who regularly received their surveillance mammograms.

	AUTHORS' DISCLOSURES OF POTENTIAL CONFLICTS OF INTEREST

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The author(s) 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: Timothy L. Lash, Rebecca A. Silliman

Financial support: Rebecca A. Silliman

Provision of study materials or patients: Diana S.M. Buist, Feifei Wei, Terry S. Field, Floyd J. Frost, Ann M. Geiger, Virginia P. Quinn, Marianne Ulcickas Yood

Collection and assembly of data: Diana S.M. Buist, Feifei Wei, Terry S. Field, Floyd J. Frost, Ann M. Geiger, Virginia P. Quinn, Marianne Ulcickas Yood, Rebecca A. Silliman

Data analysis and interpretation: Timothy L. Lash, Matthew P. Fox, Diana S.M. Buist, Feifei Wei, Rebecca A. Silliman

Manuscript writing: Timothy L. Lash, Matthew P. Fox, Diana S.M. Buist, Feifei Wei, Rebecca A. Silliman

Final approval of manuscript: Timothy L. Lash, Matthew P. Fox, Diana S.M. Buist, Feifei Wei, Terry S. Field, Floyd J. Frost, Ann M. Geiger, Virginia P. Quinn, Marianne Ulcickas Yood, Rebecca A. Silliman

	NOTES

 
published online ahead of print at www.jco.org on June 4, 2007.

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

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Submitted November 14, 2006; accepted April 2, 2007.

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