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Treatment Patterns Among Women Diagnosed With Stage I-III Triple-negative Breast Cancer

Sineshaw, Helmneh M., MD, MPH*; Freedman, Rachel A., MD, MPH; DeSantis, Carol E., MPH*; Jemal, Ahmedin, DVM, PhD*

American Journal of Clinical Oncology: October 2018 - Volume 41 - Issue 10 - p 997–1007
doi: 10.1097/COC.0000000000000418
Original Articles: Breast

Objective: To examine contemporary treatment patterns for women diagnosed with stage I-III triple-negative breast cancer (TNBC) in the United States.

Methods: We identified 48,961 patients diagnosed with stage I-III TNBC from 2010 to 2013 in the National Cancer Data Base and created 3 treatment subcohorts (definitive locoregional therapy [appropriate local therapy, including surgery/radiation], adjuvant chemotherapy [stage II-III disease or stage I tumors with tumor size ≥1 cm], and adjuvant chemotherapy for small tumors [stage I tumors with tumor size <1 cm and node negative]). We performed descriptive analyses, calculated percentages for treatment receipt, and used multivariable modified Poisson regression models to estimate risk ratios (RRs) with 95% confidence intervals (CIs) predicting receipt of treatments.

Results: Older age, larger tumor size, positive nodal status, and Southern/Pacific US regions, but not race/ethnicity, were strongly associated with a lower probability of receiving definitive locoregional therapy. Older age was also strongly associated with lower likelihood of adjuvant chemotherapy receipt, as were grade, negative nodal status, and higher comorbidity. For example, compared with women aged 18 to 39 years, those aged 75 to 90 years were 17% less likely to receive definitive locoregional therapy (RR, 0.83; 95% CI, 0.73-0.88), and 62% less likely to receive adjuvant chemotherapy (RR, 0.38; 95% CI, 0.35-0.41). Age, tumor grade, tumor size, and comorbidity score were also independently associated with receipt of chemotherapy for women with small TNBC.

Conclusions: Advancing age but not race/ethnicity was associated with lower likelihood of recommended treatment receipt among women with TNBC. Although omission of therapy among older patients with breast cancer may be appropriate in the case of smaller and lower risk TNBC, some were likely undertreated.

*American Cancer Society, Atlanta, GA

Harvard Medical School, Dana-Farber Cancer Institute, Boston, MA

Supported by American Cancer Society (grant number: 125912-MRSG-14-240-01-CPPB) and Susan G. Komen for the Cure (grant number: CCR14298143).

R.A.F. declares receiving institutional funding from Genentech, Puma, and Eisai. The remaining authors declare no conflicts of interest.

Reprints: Helmneh M. Sineshaw, MD, MPH, American Cancer Society, 250 Williams Street NW, Atlanta, GA 30303. E-mail: helmneh.sineshaw@cancer.org.

Triple-negative breast cancer (TNBC) is a heterogenous breast cancer subtype defined by lack of expression for estrogen receptor, progesterone receptor, and human epidermal growth factor receptor 2 (HER2).1–3 TNBC, which is an aggressive disease often associated with a worse prognosis than other subtypes, accounts for about 10% to 15% of incident breast cancers in the United States.2,4,5 TNBC is more common in younger patients and black patients compared with their counterparts.2,4–6 Currently, conventional chemotherapy is the mainstay of systemic therapy for patients with TNBC.7,8 National Comprehensive Cancer Network (NCCN) guidelines (2016) have recommended strong consideration of adjuvant chemotherapy for TNBC that are ≥6 mm in size and radiation therapy in the setting of breast conservation or after mastectomy in the setting of substantial node-positive disease or tumors >5 cm.7 Adjuvant chemotherapy for tumors ≤0.5 cm that are node negative is not routinely recommended,7 although there is variation in practice and rates of administration.9

Although several previous studies reported disparities in treatment and survival for women with breast cancer by race/ethnicity, socioeconomic status, age, and other factors,10–15 few studies have examined such patterns for TNBC specifically.16–20 Further, most of the studies that examined TNBC were single rather than multi-institution based because cancer registries did not begin systematically collecting information on HER2 status until the 2010 diagnosis year. Some of the previous studies were also limited by restriction of cohorts to women aged below 70 years with lower risk disease16 or by examination of patterns of locoregional therapy only,16 or did not account for differences in sociodemographic, clinical, and institutional factors that affect receipt of treatment.17–19 In this analysis, we examine contemporary treatment patterns and sociodemographic disparities in receipt of recommended local therapy and chemotherapy for women with stage I-III TNBC using the National Cancer Data Base (NCDB), taking advantage of recently available information on HER2 status and inclusion of women with older ages.

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METHODS

Data Source and Patient Cohorts

The NCDB is a national hospital-based oncologic outcomes database jointly sponsored by the American College of Surgeons and the American Cancer Society, which captures ∼70% of newly diagnosed cancer cases in the United States.21,22 In addition to detailed information about the first course of treatment, the NCDB collects information on sociodemographic, tumor, and treating hospital characteristics. We identified 55,815 women aged 18 years or older who were diagnosed with pathologic stage I-III first primary breast cancer (sequence number 00 or 01) reported from currently accredited facilities, and with breast carcinoma histology codes (International Classification of Diseases for Oncology, third edition [ICD-O-3]) of 8000-8576, 8980-8981, and 9020/3 (excluding inflammatory breast cancer). We included patients who received all or part of their treatment at the reporting facility and who were diagnosed with estrogen receptor-negative, progesterone receptor-negative, and HER2-negative breast tumors during 2010 to 2013. We used pathologic stage as defined by the American Joint Committee on Cancer (seventh edition) staging system23 and clinical stage if pathologic stage was missing. Additional exclusions included those patients who were older than 90 years of age (n=359) and those with missing/unknown values for grade, insurance (also excluded government insurance other than Medicare/Medicaid), tumor size, nodal status, median income, or receipt of surgery (n=6495). We included 48,961 patients in the final cohort. We created 3 treatment subcohorts based on their eligibility for guideline-recommended treatment: definitive locoregional therapy (n=40,179), adjuvant chemotherapy (n=35,493), and adjuvant chemotherapy for small, node-negative tumors (n=4407) (Fig. 1). The 2013 Facility Oncology Registry Data Standards (FORDS) manual was used to code the variables.24

FIGURE 1

FIGURE 1

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Outcomes of Interest

Definitive Locoregional Therapy

This subcohort first included women who received surgical treatment (n=40,330) and then excluded those who received preoperative radiotherapy (n=151). Definitive locoregional therapy was defined as receipt of breast-conserving surgery and radiotherapy, mastectomy with or without radiotherapy for breast tumor ≤5 cm and no lymph node metastasis, or mastectomy and radiotherapy for breast cancer with tumor >5 cm or lymph node metastasis.7 We defined radiotherapy as part of definitive locoregional therapy if it was received within 1 year of diagnosis (because many women will receive chemotherapy prior to radiation therapy). Breast-conserving surgery included receipt of partial mastectomy, including mastectomy with nipple preservation, lumpectomy or excisional biopsy, re-excision of biopsy site, or segmental mastectomy. Women who received subcutaneous mastectomy, total (simple) mastectomy, modified radical mastectomy, radical mastectomy, extended radical mastectomy, or mastectomy (not otherwise specified) were coded as receiving mastectomy, including those receiving bilateral mastectomy, with or without reconstruction.

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Adjuvant Chemotherapy

We assessed receipt of adjuvant chemotherapy for those undergoing cancer-directed surgery in 2 subcohorts: (a) women with stage II-III disease or stage I tumors with tumor size ≥1 cm and (b) women with stage I tumors with tumor size <1 cm and node negative. Receipt of chemotherapy was defined as adjuvant if administered within 6 months of diagnosis (including those receiving neoadjuvant chemotherapy), given that chemotherapy typically precedes any radiation therapy.

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Variables of Interest

Sociodemographic variables included race/ethnicity (non-Hispanic [NH] white, NH black, Hispanic, Other; categorized using race and ethnicity as reported by the patient and captured in the medical record), age (18 to 39, 40 to 49, 50 to 64, 65 to 74, 75 to 90 y), diagnosis year, insurance (uninsured, Medicaid, Medicare, and private), area-level median household income (divided into quartiles using 2000 US Census data), and US region (New England, Middle Atlantic, South Atlantic, East North Central, East South Central, West North Central, West South Central, Mountain, Pacific). Institutional and clinical variables included treatment facility (community cancer center, comprehensive community cancer center, National Cancer Institute/teaching/research center, and other), facility case volume (low, medium, high; ranked using tertiles by counting the number of TNBC cases reported by each facility during the study period by diagnosis year), comorbidity (0, 1, ≥2, based on the sum of weighted Charlson-Deyo Score25), tumor size (≤2, >2 to 5, >5 cm), grade (I, II, III), and node status (positive, negative, not assessed). For the analyses examining chemotherapy receipt for small tumors, tumor size was categorized as ≤0.5 cm and >0.5 to <1 cm.

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Statistical Analysis

We performed descriptive analyses to show distributions of demographic, treatment facility, socioeconomic, and tumor characteristics in women with stage I-III TNBC. We calculated the percentage of patients who received definitive locoregional therapy and adjuvant chemotherapy by patient, hospital, and tumor characteristics. We used χ2 tests to test statistical significance for categorized variables. We used multivariable modified Poisson regression models, as some log-binomial models had convergence issues, to estimate risk ratios (RRs) and 95% confidence intervals (CIs) predicting receipt of each treatment after accounting for socioeconomic status, comorbidity, and tumor characteristics. In a sensitivity analysis, we calculated the percentage of patients who received treatment after excluding those older than 84 years. We also examined percentage of adjuvant chemotherapy receipt for women with stage III TNBC by age as these women are supposed to benefit from adjuvant chemotherapy. Statistical significance was determined when 2-sided P-value was <0.05. This study was considered exempt from review by the Institutional Review Board at Dana-Farber Cancer Institute (Boston, MA) and Morehouse School of Medicine (Atlanta, GA). All statistical analyses were performed using SAS version 9.4 (SAS Institute, Cary, NC).

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RESULTS

Table 1 shows descriptive characteristics for the 48,961 women diagnosed with stage I-III TNBC. Of these, 68.6% (33,576/48,961) were NH whites, 21.6% (10,591/48,916) NH blacks, 6.2% (3033/48,961) Hispanics, and 3.6% (1761/48,961) categorized as other racial/ethnic group. Compared with NH whites, NH blacks and Hispanics were disproportionately represented in stage II or III (64.9% for NH blacks and 65.9% for Hispanics vs. 51.5% for NH whites), in grade 3 (85.5% for NH blacks and 85.8% for Hispanics vs. 79.5% for NH whites), in tumor size >5 cm (14.0% for NH blacks and 14.4% for Hispanics vs. 9.0% for NH whites), and in node-positive status (34.8% for NH blacks and 35.8% for Hispanics vs. 28.9% for NH whites). NH black women were more likely to have ≥2 comorbid conditions compared with NH whites (6.0% vs. 3.7%, P<0.0001). The percentage of uninsured or Medicaid insured patients were substantially higher in minority groups than in NH whites (21.0% for NH blacks, 37.1% for Hispanics, and 18.9% for other racial/ethnic group vs. 8.1% for NH whites). Higher percentages of NH blacks and Hispanics resided in areas with lowest median income (29.1% for NH blacks and 21.1% for Hispanics vs. 8.8% for NH whites).

TABLE 1

TABLE 1

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Treatment Outcomes

Unadjusted percentages in receipt of recommended treatments for eligible women with TNBC by major characteristics are shown in Table 2. Overall, 80.9% (32,518/40,179) of women in the definitive locoregional therapy subcohort, 80.6% (28,598/35,493) of women in the adjuvant chemotherapy subcohort, and 43.8% (1929/4407) of women in the adjuvant chemotherapy for small tumor subcohort received recommended treatment. Receipt of definitive locoregional therapy by race/ethnicity varied significantly from 76.3% in Hispanics to 82.1% in NH whites, and so did receipt of adjuvant chemotherapy from 79.6% in NH whites to 83.3% in Hispanics. In contrast, receipt of chemotherapy for small TNBC did not vary among racial/ethnic groups (P=0.23). Notably, there were large differences in unadjusted percentages of treatment receipt by age in all 3 subcohorts. Receipt of definitive locoregional therapy ranged from 80.0% to 83.8% in patients aged 18 to 74 years to 68.2% in those aged 75 to 90 years. Similarly, receipt of adjuvant chemotherapy ranged from 93.3% in women aged 18 to 39 years to 32.3% in women aged 75 to 90 years. Compared with node-positive TNBC patients, node-negative TNBC patients had 25% higher receipt of locoregional therapy, and 7% lower receipt of adjuvant chemotherapy in absolute terms. Furthermore, unadjusted percentages in receipt of treatment for each treatment group varied significantly across several other characteristics. Excluding patients older than 84 years of age did not significantly change our results in receipt of treatment (Table S1, Supplemental Digital Content 1, http://links.lww.com/FPC/B300). For women with stage III TNBC in the adjuvant chemotherapy subcohort, only 43.7% of patients aged 75 to 90 years received adjuvant chemotherapy compared with 94.5% in those aged 18 to 39 years (data not shown).

TABLE 2

TABLE 2

Adjusted RRs for receipt of definitive locoregional therapy did not show statistically significant differences in NH blacks, Hispanics, and those categorized as other racial/ethnic group compared with NH whites (Table 3). Women aged 75 to 90 years were 17% less likely to receive definitive locoregional therapy compared with those aged 18 to 39 years (RR=0.83; 95% CI, 0.78-0.88). Larger tumor size and South or Pacific US region residence were associated with lower likelihood of receipt of definitive locoregional therapy, whereas negative nodal status was associated with higher likelihood of receipt of locoregional therapy (RR=1.40; 95% CI, 1.36-1.45 vs. positive nodal status).

TABLE 3

TABLE 3

There were no statistically significant differences in adjusted RRs predicting the likelihood of receiving adjuvant chemotherapy for women with TNBC among racial/ethnic groups (Table 4). The likelihood of receiving adjuvant chemotherapy was significantly lower in older women, ranging from 24% less likely in women aged 65 to 74 years to 62% less likely in women aged 75 to 90 years compared with women aged 18 to 39 years. Women with negative nodal status had a 6% lower likelihood of receiving adjuvant chemotherapy compared with those who had positive nodal status (RR, 0.94; 95 CI, 0.91-0.96). Women with comorbidity score of ≥2 were 12% less likely to receive adjuvant chemotherapy than those with comorbidity score of 0 (RR, 0.88; 95% CI, 0.82-0.94). Similar to all TNBC patients, receipt of adjuvant chemotherapy in patients with small TNBC was equally likely among racial/ethnic groups (Table 5). Age, tumor grade, tumor size, and comorbidity score were also independently associated with receiving adjuvant chemotherapy for women with small TNBC.

TABLE 4

TABLE 4

TABLE 5

TABLE 5

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DISCUSSION

Using a nationwide oncologic outcomes database to examine patterns in locoregional and systemic management among women with TNBC for the first time, we observed variable receipt, with differences most striking for those of varying age at diagnosis and by tumor characteristics. Although we observed small racial/ethnic differences in unadjusted rates for receipt of definitive locoregional therapy and adjuvant chemotherapy, these racial/ethnic differences disappeared after controlling for sociodemographic, clinical, and hospital characteristics. In addition, we observed geographic variation in receipt of treatment.

There is a substantial body of literature that documents disparity in receipt of treatment, with minorities being less likely to receive recommended treatments in women with breast cancer.10–12,26 Reassuringly, our findings showed very small racial/ethnic differences in receipt of treatment. Although it is possible that previously documented racial disparities in care are improving, we could not include information on dose intensity, dose delays, completion of therapy, or outcomes for these patients, limiting interpretability of our findings to initiation of chemotherapy only. There are past studies that have reported similar findings, with small to no racial/ethnic differences in receipt of treatment for women with TNBC,16–19 although most of these studies were limited to single institution, selected group of women with lower risk disease, examined patterns of locoregional therapy only, or did not consistently include potentially contributing factors, with possibility of selection bias or lack of statistical power. Further, although racial disparities in chemotherapy receipt were not observed in our study, disparities may be more apparent with the advent of new systemic treatments, as observed for receipt of newer, costly, targeted treatments.27–30

Our findings that older women had lower likelihood of receiving locoregional therapy or adjuvant chemotherapy were in agreement with other previous reports for breast cancer in general or TNBC in particular.12,14,15,20,31–34 For instance, using a single institution-based data, Liedtke et al20 reported that older women with TNBC were significantly less likely to receive adjuvant chemotherapy compared with their younger counterparts. In addition, a multicenter retrospective cohort study conducted in Germany showed higher guideline violations for receipt of treatment in older women with TNBC.31 Several studies also suggested that older women were less likely to receive recommended treatments, which may be due to higher comorbidities, lack of evidence from randomized clinical trials as most trials have few older patients, or differences in patient/physician preferences.14,31,32,35,36 However, several other studies reported that older women could tolerate undergoing chemotherapy without major impact of toxicity37 and could benefit from adjuvant chemotherapy similar to younger women.38 Although the omission of adjuvant chemotherapy for older patients with small-risk or low-risk tumors is likely appropriate, the 56.3% of patients aged 75 to 90 years with stage III TNBC not receiving chemotherapy likely represent undertreatment and disparity and that many of these patients would tolerate therapy and benefit as much as younger patients.

We also observed that higher comorbidity score was associated with lower likelihood of receiving adjuvant chemotherapy for women with TNBC who were eligible to receive such treatment, which is consistent with previous studies.15,35,39 Clinicians may prefer not to administer recommended treatment for patients with comorbid conditions because of concerns about poor outcome, higher toxicity, or lack of evidence from clinical trials.40,41 However, some studies suggested that breast cancer patients with comorbid conditions could be enrolled in clinical trials and offered recommended treatments with no significant difference in toxicity compared with patients with comorbid conditions.42 Hence, the negative effect of comorbidity in receipt of treatment and outcomes for women with TNBC could be minimized if treatment decision and clinical trial protocols consider stratifying patients by their comorbidity status.

Not surprisingly and consistent with past reports,15,39,43–45 tumor characteristics such as tumor size and grade were strongly associated with treatment receipt in our analysis. In addition, the effect of negative nodal status on the likelihood of receiving adjuvant chemotherapy for women with breast cancer was also documented previously.15,46 The NCCN guidelines recommend adjuvant chemotherapy for women with node negative and tumor size >1 cm TNBC.7 However, our findings showed women with node-negative TNBC were less likely to receive adjuvant chemotherapy after controlling for tumor size. This could be due to other unmeasured factors such as physicians opting out offering treatment for these women, or patient preferences. Although there was no previous study that documented the effect of nodal status in receipt of recommended treatment for women with TNBC, our finding and reports for breast cancer in general suggest that it has significance in treatment variation.

Treatment decisions for women with small tumor size TNBC is even more complex than the treatment decisions for women with TNBC in general because of the rarity and lack of data to generate evidence. Differences in receipt of treatment by various characteristics for women with small size TNBC were reported previously.19,47,48 These reports were in line with our findings and could in part be due to lack of high-level evidence or consistent recommendation, or physician/patient preferences.14

A major strength of our study is the use of the NCDB, the largest oncologic outcomes database with detailed information on treatment, sociodemographic, clinical, and institutional characteristics, which is suited to examine contemporary treatment patterns for rare cancers such as TNBC. However, our study has some limitations. First, NCDB is a hospital-based database rather than population-based database. However, a number of previous studies showed that demographic and clinical characteristics of patients are remarkably similar to those from the population-based database.49 Second, although data quality in the NCDB is highly standardized, there could be errors in reporting race/ethnicity, stage, receptor status, and receipt of treatment. Third, adjuvant chemotherapy receipt could be under-ascertained in patients who had delays in surgery as we defined adjuvant chemotherapy within 6 months of diagnosis, although delays in chemotherapy beyond 6 months after diagnosis happen infrequently.50 Fourth, there could be underreporting of receipt of chemotherapy from hospitals as most chemotherapy is being administered in outpatient settings and information may be difficult to obtain. However, completeness of chemotherapy information reporting in the NCDB is high.51 Fifth, the NCDB does not collect information about type of chemotherapy, dose administered, and treatment completion. Also, NCDB lacks information about patient/physician preferences and discussions, and comorbidity may not capture a patient’s functional status. Further, there was no sufficient survival follow-up information in the NCDB for our study population at the time of conducting this study.

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CONCLUSIONS

Using a nationwide contemporary oncologic outcomes database, we found large disparities in receipt of definitive locoregional treatment and adjuvant chemotherapy for women diagnosed with stage I-III TNBC by age but not by race/ethnicity. Although omission of therapy among older patients with breast cancer may be appropriate in the case of smaller, lower risk TNBC, there are some cases where treatments are likely being underutilized. Further study will be required to better quantify the toxicity of chemotherapy for breast cancer as well as the efficacy in this population so that treatments can be optimized.

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ACKNOWLEDGMENT

The data used in the study are derived from a limited data set of the National Cancer Data Base (NCDB). The authors acknowledge the efforts of the American College of Surgeons, the Commission on Cancer and the American Cancer Society in the creation of the National Cancer Data Base. The American College of Surgeons and the Commission on Cancer have not verified and are not responsible for the analytic or statistical methodology employed, or the conclusions drawn from these data by the authors.

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Keywords:

breast cancer; triple negative; TNBC; locoregional; adjuvant chemotherapy

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