https://www.ajmc.com/journals/issue/2011/2011-2-vol17-n2/ajmc_11feb_wernli_162to167
Timing of Follow-up After Abnormal Screening and Diagnostic Mammograms

Karen J. Wernli, PhD; Erin J. Aiello Bowles, MPH; Sebastien Haneuse, PhD; Joanne G. Elmore, MD, MPH; and Diana S.M. Buist, PhD, MPH

Approximately 75% of US women report having at least 1 screening mammogram to detect breast cancer.1 Abnormal mammograms, which require additional imaging or surgical follow-up, occur at a rate of almost 10% and 8% of screening and diagnostic exams, respectively.2,3 There are currently no published national data available for mammography facilities and practices benchmarks for the appropriate timing for receipt of follow-up evaluation after an abnormal mammogram.4-6

A delay in follow-up can be attributed to characteristics of the woman (ie, not making an appointment), the provider (ie, not communicating the importance of follow-up), or the healthcare system (ie, insufficient scheduling space for prompt return). Failure of 1 or all of these systems results in delayed follow-up by the patient, which may contribute to a delayed diagnosis of breast cancer, later stage disease,7 and poorer survival.8,9 Woman-level characteristics associated with a delay or lack of follow-up after an abnormal mammogram include being older,6,10 lacking health insurance,5,11-13 being African American or Hispanic,5,14 having a low income,5,11,12 having no breast symptoms,15 and  having no previous mammograms.12

Evaluating the follow-up of breast health within an HMO setting provides opportunities to monitor women after an abnormal mammographic exam when access to appropriate follow-up care should be equitable. Two prior studies have evaluated follow-up after an abnormal mammogram within an HMO setting,6,12 but neither study had an active program for breast health, which would identify and schedule care for women with abnormal mammograms. In our study, we investigated woman-level characteristics associated with  follow-up after an abnormal mammography examination in women enrolled in a health plan with an active breast health program.

MATERIALS AND METHODS
Study Subjects

Women aged 40 to 84 years who received a mammogram between 1996 and 2003 in Group Health, an integrated delivery system in the Puget Sound region of Washington State, and were enrolled for at least 12 months were eligible for this study. All women had access to free mammography through the health plan, including screening and diagnostic exams. This analysis is restricted to women with an abnormal result from mammography defined as a Breast Imaging Reporting and Data System (BI-RADS)16 assessment of 0 (incomplete), 4 (suspicious abnormality), or 5 (highly suspicious of malignancy). We specifically excluded women recommended for 6-month short-interval follow-up (BI-RADS 3) because we were interested in abnormal exams that required immediate attention. Further, we restricted the sample to women who were recommended to receive additional follow-up with 1 of 4 procedures: (1) biopsy, (2) fine needle aspiration, (3) surgical evaluation, or (4) ultrasound. Women had to be continuously enrolled for 12 months after the abnormal mammogram to ensure adequate information on follow-up. We identified 25,272 and 5074 abnormal screening or diagnostic mammograms, respectively.

Breast Cancer Screening Program at Group Health
Since 1985, the Breast Cancer Screening Program at Group Health has sent reminder letters to women to encourage participation in mammography screening.17 To date, the program has mailed more than 500,000 letters. Breast clinic nurses were responsible for much of the follow-up after a mammogram. For screening mammograms, the radiologist interpreted the image the next working day after the mammogram. The breast clinic nurses called the patient within 24 to 48 hours after the report was issued with the patient’s result. If a patient had an abnormal result, the breast clinic nurse attempted to schedule the next available appointment for the patient. For diagnostic mammograms, the radiologist interpreted the image the same day and reported the result of the mammogram to the woman. A patient with an abnormal diagnostic mammogram would have scheduled the next available follow-up appointment recommended by the radiologist with the breast clinic nurse. Among nonresponders for either screening or diagnostic mammograms, the breast clinic nurse would call the patient to schedule the follow-up appointment.

Data Collection
At the time of the mammography visit, women completed a self-administered questionnaire,18 which collected information on age, reproductive risk factors, breast screening, medical history, and concerns regarding women’s breasts at the time of the exam. Women completed the questionnaire before knowing the results of their mammogram. The  uestionnaire served as the data source for woman-level characteristics under evaluation.

Information about follow-up procedures was available through electronic administrative data including pathology, radiology, utilization, and claims databases. Time to follow-up care was calculated from the date of the mammogram until the first date of follow-up care with any of the 4 procedures. Women might have received a procedure that was different from the one recommended, but was still 1 of the 4 procedures of interest. We categorized women according to receipt of follow-up care within <7, 8 to 14, 15 to 21, and 22 to 180 calendar days, based on ability to seek follow-up care within sequential weeks up to 4 weeks.

This study was approved by the institutional review board at Group Health Research Institute.

Statistical Analysis
Woman-level characteristics of interest for this analysis included the following risk factors: age, race, body mass index (kg/m2), education, family history of breast cancer in first- or second-degree relatives, self-reported symptoms at the time of mammography, biopsy history prior to the mammography examination, radiologists’ interpretation of mammographic breast density,16 and use of postmenopausal hormone therapy. Women with missing data for any of the risk factors or without follow-up within 180 days were excluded from the  analysis. The final sample size included 20,060 screening and 3184 diagnostic mammograms. Descriptive summary statistics were calculated for each variable by interval of follow-up time.

We used a multivariate ordinal logistic regression model (ologit) for ordered outcome variables to compare differences in the follow-up timing intervals.19 An ordinal logistic model is a model for multinomial data that generalizes the logistic regression model. The model allows the consideration of differences in “early” versus “later” follow-up at each of the 3 thresholds of the outcome. The interpretation of the odds ratio is the comparison of early versus late defined in our analysis as <7 days versus >8 days. All analyses included all potential risk factors and used robust methods to account for clustering for multiple records per woman. Tests for trends were evaluated by entering the ordinal term representing  the categorical variable into the ordinal model. We evaluated the contribution of each variable using a likelihood ratio test, comparing the full model with the reduced model. All hypothesis tests were 2-sided and assumed a type I error rate of alpha = .05.

All analyses were conducted in Stata/MP 11.0 (Stata-Corp, College Station, TX).

RESULTS
For women who had an abnormal screening mammogram, the median time from receipt of the exam to followup was 13 days. The proportion of women receiving care within <7, 8 to 14, 15 to 21, and 22 to 180 days was 23.3%, 36.3%, 22.0%, and 18.3%, respectively, among women with abnormal screening mammogram (Table 1). For women who had an abnormal diagnostic mammogram, the median time to further follow-up was 5 days. Further, the proportion of women receiving care within 7, 8 to 14, 15 to 21, and >22 days was 69.1%, 10.6%, 7.0%, and 13.2%, respectively (Table 2).

Among women with an abnormal screening mammogram, those more likely to receive follow-up care after 7 days were older (70-79 and >80 years) (P-trend <.001), Asian or Pacific Islander, and college graduates (P-trend = .006). The woman-level factors associated with being more likely to receive follow-up care within 7 days included reporting symptoms at the time of the exam, having a positive family history of breast cancer, and having extremely dense breasts (P-trend = .001) (Table 1).

Among women with an abnormal diagnostic mammogram, few woman-level characteristics were associated with earlier or later follow-up. Older women had later follow-up than younger women, though the results were not statistically significant at all levels. Women with higher body mass index P-trend = .026) and symptoms at the time of the mammogram were more likely to have follow-up care earlier rather than later.

DISCUSSION
This is the largest study to date to investigate the timing of follow-up after an abnormal mammogram. Unique features of this analysis include the available data from an integrated healthcare system and active surveillance by nurses to encourage and assist patients in returning to evaluate the abnormality noted on the mammogram. Further, we had sufficient data to investigate follow-up for both screening and diagnostic mammograms.

We confirmed that women of older age were more likely to seek care later rather than earlier for both screening and diagnostic mammograms.6,10 We also detected that having symptoms at the time of the mammogram was associated with earlier follow-up for both screening and diagnostic exams. Our finding is supported by Caplan and colleagues, who determined that women with breast symptoms were diagnosed with breast cancer 6 days earlier than women without breast symptoms.15

In this study, we found that women of Asian/Pacific Islander descent were more likely than white women to delay follow-up care after an abnormal screening mammogram. Karliner and colleagues reported that Asian women did not fully understand their physicians’ reports of their mammograms, particularly Chinese-speaking women.20 It is unclear whether language barriers were responsible for the longer delay in seeking care among Asian/Pacific Islander women in our study, but language interpreters or written materials might help reduce delay in other programs.

Women with extremely dense breasts were more likely to seek follow-up care quickly compared with women with less dense breasts. Prior studies have not reported on breast density and delay in follow-up care. The sensitivity of mammography in women with extremely dense breasts is only 30% compared with 80% in women with fatty breasts.21 These women are also likely to have an increased risk of interval cancers,21 which likely results in their prompt follow-up.

In our study, fewer than 1% and 4% of women with abnormal screening and diagnostic mammograms, respectively, did not receive any follow-up within 180 days (data not shown). Other studies have reported lack of follow-up in women after abnormal exams at rates between 8% and 28%.5,10 The difference in rates of follow-up is likely due to the ability of women to receive additional medical services within our health system at no financial burden and with the assistance of specially trained nurses working in the breast program. The use of computer monitoring to follow up with women postmammography reduces the delays in seeking care.22,23 Group Health’s Breast Cancer Screening Program implemented active follow-up of women with breast clinic nurses and now uses the electronic medical record to help track women.

This study was conducted in a well-characterized defined population of women who receive healthcare through an integrated delivery system. There was thorough assessment and follow-up of mammography screening because of the Breast Cancer Screening Program at Group Health. We might have missed some clinical care that occurred at outside facilities that was not submitted for a claim. However, this is unlikely for women with their primary insurance at the health plan, because filing a claim would enable payment for outside services and women would be motivated to do so.

Clinical guidelines for promptness in obtaining an evaluation after an abnormality is noted on mammography examination are not well established. An assessment of the National Initiative on Cancer Care Quality in the United States suggests that 90% of patients should be seen within 3 weeks of an abnormal screening mammogram for a diagnostic mammogram, within 14 days from needing an open biopsy to cancer diagnosis, and within 5 working days from breast cancer diagnosis to an appointment with the treating physician.24 While we cannot make a direct comparison to the National Initiative for Cancer Care Quality, we can report that 82% of women received the recommended follow-up care within 3 weeks of their abnormal screening mammogram. Further, 69% of women with abnormal diagnostic mammograms received recommended follow-up care within 7 days. In 2004, the National Quality Measures for Breast Centers identified 2 measures of timely follow-up: imaging timeliness of care (ie, time between screening mammogram, diagnostic mammogram, needle biopsy, surgery) and surgical timeliness (ie, time between diagnostic mammogram, open surgical biopsy/excision, initial breast cancer surgery).25 There are characteristics that influence women’s timeliness to follow-up that future interventions may address to reduce delays in breast cancer diagnosis.
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