Abstract
Background
Although breast cancer is most prevalent among older women, the majority are diagnosed at an early stage. When diagnosed at an early stage, women have the option of breast-conserving surgery (BCS) plus radiation therapy (RT) or mastectomy for the treatment of early-stage breast cancer (ESBC). Omission of RT when receiving BCS increases the risk for recurrence and poor survival. Yet, a small subset of older women may omit RT after BCS. This study examines the current patterns of local treatment for ESBC among older women.
Methods
This study conducted a retrospective observational analysis using the Surveillance, Epidemiology, and End Results (SEER)-Medicare linked dataset of women age ≥66 diagnosed with stage I-II breast cancer in 2003–2009. SEER-Medicare data was additionally linked with data from the Area Resource File (ARF) to examine the association between area-level healthcare resources and treatment. Two logistic regression models were used to estimate how study factors were associated with receiving (1) BCS versus BCS+RT and (2) Mastectomy versus BCS+RT. A stratified analysis was also conducted among women aged <70 years.
Results
Among 45,924 patients, 55% received BCS+RT, 23% received mastectomy, and 22% received BCS only. Women of increasing age, comorbidity, primary care provider visits, stage II disease, and nonwhite race were more likely to have mastectomy or BCS only, than BCS+RT. Women diagnosed in 2004–2006, treated by an oncology surgeon, residing in metro areas, areas of greater education and income, were less likely to receive mastectomy or BCS only, than BCS+RT. While women aged <70 years were more likely to receive BCS+RT, socioeconomic and physician specialties were associated with receiving BCS only.
Conclusions
Over half of older women with ESBC initially receive BCS+RT. The likelihood for mastectomy and BCS only increases with age, comorbidity, and vulnerable socio-demographic characteristics. Findings demonstrate continued treatment disparities among certain vulnerable populations.
Keywords: : breast cancer, early-stage, treatment, elderly
Introduction
Breast conserving surgery (BCS) followed by radiation therapy (RT) is an equally effective local treatment for long-term survival of invasive early-stage breast cancer (ESBC), as is mastectomy,1–3 and is the preferred choice of local treatment, with ∼60% or more women receiving BCS plus RT (BCS+RT).4,5 Treatment guidelines allow older women, age ≥70 years, stage I, estrogen receptor (ER) positive, and taking tamoxifen, to omit RT following BCS, and recommend RT for all other women undergoing BCS.6 RT omission is associated with short-term treatment failure, and consequently, mastectomy, in addition to an increased risk of recurrence and breast cancer mortality.7–13 Unfortunately, a substantial number of clinically eligible older women do not receive RT following BCS, and a greater number may initially be treated with mastectomy, than younger women.7,11,14,15
Following publication of the CALGB trial study results,16 rates of BCS+RT have declined among all older women with ESBC, irrespective of clinical indications.12,17,18 The decline in rates may be due to individual patient characteristics. Retrospective studies have shown age and comorbidity to be the strongest predictors for type of local treatment received. As age and comorbidity increase, so do rates of mastectomy or BCS only.9,14,15,18,19 Omission of RT or use of mastectomy, is intended to preserve quality of life and avoid adverse effects in patients with limited life expectancy, frail health, or low functional status. However, RT omission when receiving BCS increases the risk of recurrence, while mastectomy results in loss of breast preservation and greater physical limitations.20
Therefore, the purpose of this study is to determine patterns of local treatment (BCS+RT, mastectomy, or BCS only) among women aged ≥66 years, with stage I and II breast cancer using the U.S. population-based linked SEER-Medicare dataset. Furthermore, this study aims to determine how age, comorbidity, frequency of primary care provider (PCP) visits, clinical prognostic factors, oncology care resources, and socio-demographic characteristics are associated with choice of local treatment.
Materials and Methods
Data source and cohort definition
The SEER-Medicare linked database was created in a collaborative effort by the National Cancer Institute (NCI) and Centers for Medicare and Medicaid Services (CMS). SEER data collected from 17 tumor registries, representing 26% of the United States (US) population, is successfully matched to Medicare enrollment records for 94% of patients aged ≥65 years.21 SEER-Medicare data contains information about date of diagnosis, cancer site, stage, tumor characteristics, treatment, healthcare use, patient enrollment and eligibility, selected demographic characteristics, and vital status information. County and state of diagnosis were used to identify the area-level density of mammography screening and oncology centers from the U.S. Department of Health and Human Resource's 2009 Area Resource File (ARF).22 This study was approved for exemption by the West Virginia University Institutional Review Board.
We identified 69,376 females aged ≥66 years with a first ever and primary diagnosis of stage I or II incident case of breast cancer between January 1, 2003 and December 31, 2009 who were continuously enrolled in Medicare Part A and B fee-for-service programs 1 year before and after diagnosis. Other exclusion criteria were as follows: enrollment in managed care programs at any time during the year before or after diagnosis (n = 20,872), died within the first year of diagnosis (n = 710), if tumor size was missing (n = 64), if surgeon specialty was missing (n = 852), or did not have any definitive surgery (n = 954). After these exclusions, the final analytic sample consisted of 45,924 patients.
Local treatment variable
The local treatment received (BCS+RT, mastectomy, or BCS only) was identified using surgical and Medicare radiation claims where the claim date was within 366 days of the diagnosis. BCS (i.e., lumpectomy, partial mastectomy, segmental mastectomy), mastectomy, and RT were identified using International Classification of Diseases, 9th Revision (ICD-9) diagnosis and procedure codes and Current Procedural Terminology/Healthcare Common Procedure Coding System (CPT/HCPCS) (Appendix 1).
Explanatory variables
Explanatory variables used in this study include individual-level and area-level measures. Individual-level patient characteristics included diagnosis year, age, race, comorbidity, frequency of PCP visits, clinical prognostic factors, and surgeon specialty. Area-level measures include census tract level of education, census tract level of income, metro status, local density of mammography screening facilities, and local density of oncology treatment centers. Comorbidity scores were calculated using the Klabunde adaptation of the Charlson index (score = 0, 1, ≥ 2).23,24 Frequency of PCP visits was determined by counting the number of unique PCP claim dates the year before diagnosis and dividing by lower and upper 50th percent median cutoff. Clinical prognostic factors included stage at diagnosis, ER status, progesterone receptor (PR) status, and tumor grade. Oncology care resources were captured by the area-level density of mammography screening and oncology treatment centers, and specialty of the treating surgeon. Area-level densities were determined by dividing proportions found in the ARF by lower and upper 50th percent median cutoffs. Surgeon specialty (general only, oncology only, or both) was ascertained using provider specialty claims codes. Demographic characteristics were race, metro status, census-tract level, education, and income
Statistical analysis
Patient characteristics were summarized using descriptive statistics. Mantel–Haenszel chi-square tests of location shift, using either modified ridit scores or table scores, and Mantel–Haenszel chi-square tests of general association, depending on whether the independent measure was dichotomous, nominal, or ordinal, were used to compare significant group differences between patients receiving BCS+RT, mastectomy, or BCS only. Two multivariable logistic regression models were used to estimate likelihood for type of local treatment received (mastectomy vs. BCS+RT and BCS only vs. BCS+RT), adjusting for year of diagnosis, age and health characteristics, clinical prognostic factors, oncology care resources, and socio-demographic characteristics. Parameter estimates calculated in the regression models are presented as adjusted odds ratios (AOR) with their corresponding 95% confidence intervals (CI). p values <0.05 were considered statistically significant. Analysis was conducted using SAS version 9.4 software (SAS Institute, Inc., Cary, NC).
Results
Patient characteristics
Of 45,924 female fee-for-service Medicare beneficiaries diagnosed in 2003–2009 and in our analytic sample 54.5% received BCS+RT, 23.4% had mastectomy, and 22.1% had BCS only; 25.5% were aged 70–74 years at diagnosis, and 56.7% had comorbidity score = 0. Most were treated by both general and oncology surgeons (75.7%) (Table 1).
Table 1.
Descriptive Characteristics of Older Women with Early-Stage Breast Cancer SEER -Medicare, 2003–2009
| N | % | |
|---|---|---|
| All | 45924 | 100.0 |
| Treatment | ||
| BCS+RT | 25038 | 54.5 |
| Mastectomy | 10755 | 23.4 |
| BCS only | 10131 | 22.1 |
| Year of diagnosis | ||
| 2003 | 6620 | 14.4 |
| 2004 | 6523 | 14.2 |
| 2005 | 6416 | 14.0 |
| 2006 | 6493 | 14.1 |
| 2007 | 6563 | 14.3 |
| 2008 | 6628 | 14.4 |
| 2009 | 6681 | 14.6 |
| Age & health | ||
| Age at diagnosis | ||
| 66–69 | 10319 | 22.5 |
| 70–74 | 11728 | 25.5 |
| 75–79 | 10718 | 23.3 |
| 80–84 | 7974 | 17.4 |
| 85–89 | 3900 | 8.5 |
| ≥ 90 | 1285 | 2.8 |
| Comorbidity score | ||
| 0 | 26024 | 56.7 |
| 1 | 12422 | 27.1 |
| ≥ 2 | 7478 | 16.3 |
| PCP visits | ||
| Low | 24805 | 54.0 |
| High | 21119 | 46.0 |
| Clinical prognostic factors | ||
| Stage at diagnosis | ||
| I | 28884 | 62.9 |
| II | 17040 | 37.1 |
| ER status | ||
| Positive | 36321 | 79.1 |
| Negative | 6298 | 13.7 |
| Borderline/unknown | 3305 | 7.2 |
| PR status | ||
| Positive | 30470 | 66.4 |
| Negative | 11754 | 25.6 |
| Borderline/unknown | 3700 | 8.1 |
| Tumor size | ||
| 0–1 cm | 14837 | 32.3 |
| <2 cm | 18001 | 39.2 |
| 2–5 cm | 12371 | 26.9 |
| >5 cm | 715 | 1.6 |
| Tumor grade | ||
| Well differentiated | 12096 | 26.3 |
| Moderately differentiated | 20024 | 43.6 |
| Poorly differentiated | 10826 | 23.6 |
| Undifferentiated/unknown | 2978 | 6.5 |
| Oncology care resources | ||
| Mammography screening centers | ||
| Low | 23761 | 51.7 |
| High | 22163 | 48.3 |
| Oncology treatment centers | ||
| Low | 25733 | 56.0 |
| High | 20191 | 44.0 |
| Type of surgeon seen | ||
| General only | 8536 | 18.6 |
| Oncology only | 2640 | 5.8 |
| Both | 34748 | 75.7 |
| Socio-demographic characteristics | ||
| Race | ||
| White | 41034 | 89.4 |
| Other | 4890 | 10.7 |
| Education | ||
| <15% college degree | 13543 | 29.5 |
| ≥15% college degree | 32381 | 70.5 |
| Annual income | ||
| ≤$35,000 | 10839 | 23.6 |
| >$35,000 | 35085 | 76.4 |
| Metro status | ||
| Nonmetro | 7673 | 16.7 |
| Metro | 38251 | 83.3 |
BCS, breast-conserving surgery; RT, radiation therapy; PCP, primary care physician; ER, estrogen receptor; PR, progesterone receptor; SEER, Surveillance, Epidemiology, and End Results.
Univariate analysis
All p-values are significant at the p < 0.001 level. The proportion of patients receiving BCS+RT decreased with increasing age: 65.0% of women 66–69 years to 14.2% of women ≥90 years (Table 2). In contrast, rates of mastectomy and BCS only were highest among those aged ≥90 years versus 66–69 years (30.9% and 54.9% vs. 20.0% and 15.0%). Women with a comorbidity score = 2 versus 0 had the lowest rates of BCS+RT (47.8% vs. 57.5%), while rates of mastectomy (25.6% vs. 22.6%) and BCS only (26.6% vs. 19.9%) were the highest among women with a score = 2 versus 0. Patients with stage I disease, hormone receptor-positive, and well-differentiated tumors had higher rates of BCS+RT, while those with poor prognostic factors had higher rates of mastectomy and BCS only. Women treated by an oncology surgeon only or both an oncology and general surgeon had the highest rates of BCS+RT, compared to those treated by a general surgeon only, while rates of BCS only were the highest among those treated by a general surgeon only.
Table 2.
Univariate Analysis of Local Treatment Among Older Women with Early-Stage Breast Cancer SEER-Medicare, 2003–2009
| BCS+RT | Mastectomy | BCS Only | |||||
|---|---|---|---|---|---|---|---|
| N | % | N | % | N | % | ||
| All | 25067 | 54.5 | 10768 | 23.4 | 10146 | 22.1 | p-value |
| Year of diagnosis | <0.001*** | ||||||
| 2003 | 3498 | 52.8 | 1646 | 24.9 | 1476 | 22.3 | |
| 2004 | 3502 | 53.7 | 1436 | 22.0 | 1585 | 24.3 | |
| 2005 | 3388 | 52.8 | 1462 | 22.8 | 1566 | 24.4 | |
| 2006 | 3572 | 55.0 | 1418 | 21.8 | 1503 | 23.2 | |
| 2007 | 3636 | 55.4 | 1560 | 23.8 | 1367 | 20.8 | |
| 2008 | 3675 | 55.5 | 1610 | 24.3 | 1343 | 20.3 | |
| 2009 | 3767 | 56.4 | 1623 | 24.3 | 1291 | 19.3 | |
| Age & health | |||||||
| Age at diagnosis | <0.001*** | ||||||
| 66–69 | 6708 | 65.0 | 2064 | 20.0 | 1547 | 15.0 | |
| 70–74 | 7259 | 61.9 | 2521 | 21.5 | 1948 | 16.6 | |
| 75–79 | 6025 | 56.2 | 2523 | 23.5 | 2170 | 20.3 | |
| 80–84 | 3713 | 46.6 | 2085 | 26.2 | 2176 | 27.3 | |
| 85–89 | 1151 | 29.5 | 1165 | 29.9 | 1584 | 40.6 | |
| ≥90 | 182 | 14.2 | 397 | 30.9 | 706 | 54.9 | |
| Comorbidity score | <0.001*** | ||||||
| 0 | 14969 | 57.5 | 5882 | 22.6 | 5173 | 19.9 | |
| 1 | 6495 | 52.3 | 2956 | 23.8 | 2971 | 23.9 | |
| ≥2 | 3574 | 47.8 | 1917 | 25.6 | 1987 | 26.6 | |
| PCP visits | <0.001*** | ||||||
| Low | 14142 | 57.0 | 5679 | 22.9 | 4984 | 20.1 | |
| High | 10896 | 51.6 | 5076 | 24.0 | 5147 | 24.4 | |
| Clinical prognostic factors | |||||||
| Stage at diagnosis | <0.001*** | ||||||
| I | 17734 | 61.4 | 4508 | 15.6 | 6642 | 23.0 | |
| II | 7304 | 42.9 | 6247 | 36.7 | 3489 | 20.5 | |
| ER status | <0.001*** | ||||||
| Positive | 20577 | 56.7 | 7855 | 21.6 | 7889 | 21.7 | |
| Negative | 3157 | 50.1 | 1911 | 30.3 | 1230 | 19.5 | |
| Borderline/Unknown | 1304 | 39.5 | 989 | 29.9 | 1012 | 30.6 | |
| PR status | <0.001*** | ||||||
| Positive | 17386 | 57.1 | 6453 | 21.2 | 6631 | 21.8 | |
| Negative | 6144 | 52.3 | 3217 | 27.4 | 2393 | 20.4 | |
| Borderline/unknown | 1508 | 40.8 | 1085 | 29.3 | 1107 | 29.9 | |
| Tumor size | <0.001*** | ||||||
| 0–1 cm | 9495 | 64.0 | 1859 | 12.5 | 3483 | 23.5 | |
| <2 cm | 10509 | 58.4 | 3622 | 20.1 | 3870 | 21.5 | |
| 2–5 cm | 4824 | 39.0 | 4913 | 39.7 | 2634 | 21.3 | |
| >5 cm | 210 | 29.8 | 361 | 50.5 | 144 | 20.1 | |
| Tumor gradea | <0.001*** | ||||||
| Well differentiated | 7115 | 58.8 | 2194 | 18.1 | 2787 | 23.1 | |
| Moderately differentiated | 11119 | 55.5 | 4600 | 23.0 | 4305 | 21.5 | |
| Poorly differentiated | 5410 | 50.0 | 3266 | 30.2 | 2150 | 19.9 | |
| Undifferentiated/unknown | 1394 | 46.8 | 695 | 23.4 | 889 | 29.9 | |
| Oncology care resources | |||||||
| Mammography screening centersa | <0.001*** | ||||||
| Low | 12263 | 51.6 | 6014 | 25.3 | 5484 | 23.1 | |
| High | 12775 | 57.6 | 4741 | 21.4 | 4647 | 21.0 | |
| Oncology treatment centersa | <0.001*** | ||||||
| Low | 13378 | 52.0 | 6488 | 25.2 | 5867 | 22.8 | |
| High | 11660 | 57.8 | 4267 | 21.1 | 4264 | 21.1 | |
| Type of surgeon seena | <0.001*** | ||||||
| General only | 3627 | 42.5 | 2027 | 23.8 | 2882 | 33.8 | |
| Oncology only | 1535 | 58.1 | 605 | 22.9 | 500 | 18.9 | |
| Both | 19876 | 57.2 | 8123 | 23.4 | 6749 | 19.4 | |
| Socio-demographic characteristics | |||||||
| Racea | <0.001*** | ||||||
| White | 22667 | 55.2 | 9377 | 22.9 | 8990 | 21.9 | |
| Other | 2371 | 48.5 | 1378 | 28.2 | 1141 | 23.3 | |
| Educationa | <0.001*** | ||||||
| <15% college degree | 6311 | 46.6 | 3869 | 28.6 | 3363 | 24.8 | |
| ≥15% college degree | 18727 | 57.8 | 6886 | 21.3 | 6768 | 20.9 | |
| Annual incomea | <0.001*** | ||||||
| ≤$35,000 | 4872 | 45.0 | 3137 | 28.9 | 2830 | 26.1 | |
| >$35,000 | 20166 | 57.5 | 7618 | 21.7 | 7301 | 20.8 | |
| Metro statusa | <0.001*** | ||||||
| Nonmetro | 3360 | 43.8 | 2287 | 29.8 | 2026 | 26.4 | |
| Metro | 21678 | 56.7 | 8468 | 22.1 | 8105 | 21.2 | |
p < 0.05.
p < 0.01.
p < 0.001.
Multivariate analysis
The two models of factors associated with treatment (Mastectomy vs. BCS+RT and BCS only vs. BCT+RT) of ESBC among elderly women is given in Table 3. Compared to women aged 66–69 years, women of increasing age were more likely to be treated with mastectomy and BCS only versus BCS+RT, with women aged ≥90 years being the most likely to have mastectomy (AOR 6.16, 95% CI, 5.10–7.44) and BCS only (AOR 14.13, 95% CI, 11.80–16.80). Greater comorbidity (score = 2) was associated with an increased likelihood of have mastectomy (AOR 1.14, 95% CI, 1.07–1.22) and BCS only (AOR 1.38, 95% CI, 1.29–1.48). Women diagnosed with stage II breast cancer were more likely to receive mastectomy (AOR 3.15, 95% CI, 3.00–3.31) and BCS only (AOR 1.26, 95% CI, 1.19–1.32) versus BCS+RT. Those with negative and borderline/unknown ER and PR tumors, and moderately, poorly, and undifferentiated/unknown tumors were more likely to have mastectomy or BCS only.
Table 3.
Odds Ratios from the Fully Adjusted Model of Local Treatment Among Older Women with Early-Stage Breast Cancer SEER-Medicare, 2003–2009
| Treatment | ||||||
|---|---|---|---|---|---|---|
| Mastectomy vs. BCS+RT | BCS Only vs. BCS+RT | |||||
| AOR | 95% CI | Sig. | AOR | 95% CI | Sig. | |
| Year of diagnosis | ||||||
| 2003 | 1.00 | — | 1.00 | — | ||
| 2004 | 0.95 | 0.87–1.04 | 1.15 | 1.05–1.26 | ** | |
| 2005 | 1.01 | 0.92–1.10 | 1.22 | 1.11–1.33 | *** | |
| 2006 | 0.95 | 0.87–1.04 | 1.13 | 1.03–1.23 | * | |
| 2007 | 1.03 | 0.95–1.13 | 0.99 | 0.91–1.09 | ||
| 2008 | 1.08 | 0.99–1.18 | 1.00 | 0.91–1.09 | ||
| 2009 | 1.08 | 0.98–1.17 | 0.94 | 0.85–1.03 | ||
| Age & health | ||||||
| Age at diagnosis | ||||||
| 66–69 | 1.00 | — | 1.00 | — | ||
| 70–74 | 1.12 | 1.05–1.20 | ** | 1.12 | 1.04–1.21 | ** |
| 75–79 | 1.40 | 1.30–1.50 | *** | 1.49 | 1.38–1.61 | *** |
| 80–84 | 1.87 | 1.73–2.02 | *** | 2.39 | 2.21–2.59 | *** |
| 85–89 | 3.21 | 2.90–3.55 | *** | 5.39 | 4.89–5.94 | *** |
| ≥90 | 6.16 | 5.10–7.44 | *** | 14.13 | 11.80–16.80 | *** |
| Comorbidity score | ||||||
| 0 | 1.00 | — | 1.00 | — | ||
| 1 | 1.08 | 1.02–1.14 | * | 1.22 | 1.16–1.30 | *** |
| ≥2 | 1.14 | 1.07–1.22 | *** | 1.38 | 1.29–1.48 | *** |
| PCP visits | ||||||
| Low | 1.00 | — | 1.00 | — | ||
| High | 1.05 | 1.00–1.10 | * | 1.10 | 1.05–1.16 | *** |
| Clinical prognostic factors | ||||||
| Stage at diagnosis | ||||||
| I | 1.00 | — | 1.00 | — | ||
| II | 3.15 | 3.00–3.31 | *** | 1.26 | 1.19–1.32 | *** |
| ER status | ||||||
| Positive | 1.00 | — | 1.00 | — | ||
| Negative | 1.19 | 1.09–1.30 | *** | 1.03 | 0.93–1.13 | |
| Borderline/unknown | 1.56 | 1.24–1.96 | *** | 1.47 | 1.16–1.84 | *** |
| PR status | ||||||
| Positive | 1.00 | — | 1.00 | — | ||
| Negative | 1.12 | 1.05–1.20 | *** | 0.99 | 0.92–1.07 | |
| Borderline/unknown | 1.18 | 0.95–1.47 | 1.17 | 0.94–1.46 | ||
| Tumor size | ||||||
| 0–1 cm | 1.00 | — | 1.00 | — | ||
| <2 cm | 1.58 | 1.48–1.69 | *** | 0.96 | 0.91–1.02 | |
| 2–5 cm | 2.92 | 2.65–3.22 | *** | 1.30 | 1.17–1.44 | *** |
| >5 cm | 4.73 | 3.88–5.75 | *** | 1.47 | 1.15–1.87 | ** |
| Tumor grade | ||||||
| Well differentiated | 1.00 | — | 1.00 | — | ||
| Moderately differentiated | 1.06 | 0.99–1.12 | 0.95 | 0.89–1.01 | ||
| Poorly differentiated | 1.12 | 1.04–1.21 | ** | 0.93 | 0.86–1.00 | * |
| Undifferentiated/unknown | 1.15 | 1.03–1.28 | * | 1.40 | 1.27–1.55 | *** |
| Oncology care resources | ||||||
| Mammography screening centers | ||||||
| Low | 1.00 | — | 1.00 | — | ||
| High | 0.99 | 0.90–1.09 | 0.89 | 0.80–0.98 | * | |
| Oncology treatment centers | ||||||
| Low | 1.00 | — | 1.00 | — | ||
| High | 0.85 | 0.77–0.93 | *** | 1.04 | 0.94–1.14 | |
| Type of surgeon seen | ||||||
| General only | 1.00 | — | 1.00 | — | ||
| Oncology only | 0.78 | 0.70–0.88 | *** | 0.56 | 0.50–0.63 | *** |
| Both | 0.79 | 0.74–0.84 | *** | 0.57 | 0.53–0.60 | *** |
| Socio-demographic characteristics | ||||||
| Race | ||||||
| White | 1.00 | — | 1.00 | — | ||
| Other | 1.29 | 1.20–1.40 | *** | 1.25 | 1.15–1.36 | *** |
| Education | ||||||
| <15% college degree | 1.00 | — | 1.00 | — | ||
| ≥15% college degree | 0.75 | 0.70–0.79 | *** | 0.81 | 0.76–0.86 | *** |
| Annual income | ||||||
| ≤$35,000 | 1.00 | — | 1.00 | — | ||
| >$35,000 | 0.88 | 0.82–0.94 | *** | 0.84 | 0.78–0.90 | *** |
| Metro status | ||||||
| Nonmetro | 1.00 | — | 1.00 | — | ||
| Metro | 0.70 | 0.65–0.76 | *** | 0.73 | 0.67–0.78 | *** |
p < 0.05.
p < 0.01.
p < 0.001.
AOR, adjusted odds ratios; CI, confidence interval.
Women, residing in areas with a high-density of mammography screening centers were less likely to be treated with BCS only versus BCS+RT (AOR 0.89, 95% CI, 0.80–0.98). Similarly, women residing in areas with a high-density of oncology treatment centers (AOR 0.85, 95% CI, 0.77–0.93) were less likely to have mastectomy. Compared to women treated by a general surgeon only, those treated by an oncology surgeon only or treated by both types of surgeons were less likely (AOR 0.78, 95% CI, 0.70–0.88 and AOR 0.79, 95% CI, 0.74–0.84) to receive mastectomy, or BCS only (AOR 0.56, 95% CI, 0.50–0.63 and AOR 0.57, 95% CI, 0.53–0.60). Women of other races were more likely to have mastectomy or BCS only. Women living in areas of greater education, income, or metro status were less likely to receive mastectomy or BCS only.
Stratified analysis
Taking into account the guideline recommendation that BCS only may be an appropriate option for some women aged ≥70 years, we performed a stratified analysis on women aged 66–69 with comorbidity = 0 who would have been recommended to receive BCS+RT, thus eliminating patients who were eligible for BCS only as a treatment option (Table 4). Therefore, a secondary analysis was conducted to explore associations with treatment among these (age 66–69 years at diagnosis and a Charlson comorbidity score = 0) (Table 4). Among this subgroup of women (n = 6,369), 66.7% were treated with BCS+RT, 19.5% mastectomy, and 13.9% BCS only. Women diagnosed at stage II were more likely (AOR 1.91, 95% CI 1.55–2.35) to be treated with mastectomy, than those diagnosed at stage I. Women with ER negative tumors were more likely to be treated with mastectomy, than those with ER positive tumors. Women with undifferentiated/unknown and poorly differentiated tumors were also more likely to be treated with mastectomy or BCS only versus BCS+RT. Compared to those treated by a general surgeon only, women treated by an oncology surgeon (AOR 0.44, 95% CI, 0.29–0.66) or both an oncology and general surgeon (AOR 0.65, 95% CI. 0.53–0.80) were less likely to be treated with BCS only versus BCS+RT.
Table 4.
Characteristics and Adjusted Odds Ratios of Women Aged 66–69 Years and with a Charlson Comorbidity Score = 0 Diagnosed with Early-Stage Breast Cancer in SEER Regions SEER -Medicare, 2003–2009
| Treatment | ||||||||
|---|---|---|---|---|---|---|---|---|
| N | % | Mastectomy vs. BCS + RT | BCS Only vs. BCS + RT | |||||
| All | 6369 | 100.0 | AOR | 95% CI | Sig. | AOR | 95% CI | Sig. |
| Treatment | ||||||||
| BCS+Radiation | 4246 | 66.7 | ||||||
| Mastectomy | 1239 | 19.5 | ||||||
| BCS only | 884 | 13.9 | ||||||
| Year of diagnosis | ||||||||
| 2003 | 875 | 13.7 | 1.00 | — | 1.00 | — | ||
| 2004 | 908 | 14.3 | 0.90 | 0.70–1.17 | 1.11 | 0.85–1.45 | ||
| 2005 | 896 | 14.1 | 0.90 | 0.70–1.16 | 1.07 | 0.82–1.41 | ||
| 2006 | 888 | 13.9 | 0.83 | 0.64–1.08 | 1.06 | 0.81–1.40 | ||
| 2007 | 932 | 14.6 | 0.89 | 0.70–1.15 | 0.89 | 0.67–1.17 | ||
| 2008 | 961 | 15.1 | 1.27 | 1.00–1.62 | 1.02 | 0.77–1.35 | ||
| 2009 | 909 | 14.3 | 1.12 | 0.87–1.44 | 0.80 | 0.60–1.08 | ||
| Age & health | ||||||||
| PCP visits | ||||||||
| Low | 4622 | 72.6 | 1.00 | — | 1.00 | — | ||
| High | 1747 | 27.4 | 0.95 | 0.81–1.10 | 1.05 | 0.89–1.24 | ||
| Clinical prognostic factors | ||||||||
| Stage at diagnosis | ||||||||
| I | 4142 | 65.0 | 1.00 | — | 1.00 | — | ||
| II | 2227 | 35.0 | 1.91 | 1.55–2.35 | *** | 1.17 | 0.91–1.50 | |
| ER status | ||||||||
| Positive | 5055 | 79.4 | 1.00 | — | 1.00 | — | ||
| Negative | 933 | 14.7 | 1.25 | 0.98–1.60 | 1.07 | 0.80–1.42 | ||
| Borderline/unknown | 381 | 6.0 | 1.90 | 0.91–3.96 | 1.07 | 0.56–2.07 | ||
| PR status | ||||||||
| Positive | 4261 | 66.9 | 1.00 | — | 1.00 | — | ||
| Negative | 1682 | 26.4 | 1.19 | 0.98–1.45 | 0.97 | 0.77–1.22 | ||
| Borderline/unknown | 426 | 6.7 | 0.91 | 0.44–1.86 | 1.73 | 0.93–3.24 | ||
| Tumor size | ||||||||
| 0–1 cm | 2220 | 34.9 | 1.00 | — | 1.00 | — | ||
| >2 cm | 2570 | 40.4 | 1.62 | 1.36–1.94 | *** | 0.93 | 0.78–1.12 | |
| 2–5 cm | 1498 | 23.5 | 2.86 | 2.21–3.70 | *** | 1.56 | 1.15–2.10 | ** |
| >5 cm | 81 | 1.3 | 4.31 | 2.52–7.35 | *** | 1.60 | 0.78–3.29 | |
| Tumor grade | ||||||||
| Well differentiated | 1694 | 26.6 | 1.00 | — | 1.00 | — | ||
| Moderately differentiated | 2788 | 43.8 | 1.09 | 0.91–1.30 | 1.00 | 0.83–1.21 | ||
| Poorly differentiated | 1494 | 23.5 | 1.10 | 0.89–1.36 | 1.27 | 1.01–1.60 | * | |
| Undifferentiated/unknown | 393 | 6.2 | 1.37 | 1.01–1.85 | * | 1.61 | 1.18–2.18 | ** |
| Oncology care resources | ||||||||
| Mammography screening centers | ||||||||
| Low | 3386 | 53.2 | 1.00 | — | 1.00 | — | ||
| High | 2983 | 46.8 | 1.20 | 0.93–1.55 | 0.86 | 0.63–1.17 | ||
| Oncology treatment centers | ||||||||
| Low | 3656 | 57.4 | 1.00 | — | 1.00 | — | ||
| High | 2713 | 42.6 | 0.81 | 0.63–1.05 | 1.13 | 0.84–1.54 | ||
| Type of surgeon seen | ||||||||
| General only | 761 | 12.0 | 1.00 | — | 1.00 | — | ||
| Oncology only | 393 | 6.2 | 0.96 | 0.69–1.35 | 0.44 | 0.29–0.66 | *** | |
| Both | 5215 | 81.9 | 0.92 | 0.74–1.14 | 0.65 | 0.53–0.80 | *** | |
| Socio-demographic characteristics | ||||||||
| Race | ||||||||
| White | 5786 | 90.9 | 1.00 | — | 1.00 | — | ||
| Other | 583 | 9.2 | 1.22 | 0.98–1.53 | 1.30 | 1.02–1.67 | * | |
| Education | ||||||||
| <15% college degree | 1699 | 26.7 | 1.00 | — | 1.00 | — | ||
| ≥15% college degree | 4670 | 73.3 | 0.85 | 0.71–1.01 | 0.90 | 0.74–1.09 | ||
| Annual income | ||||||||
| ≤$35,000 | 1295 | 20.3 | 1.00 | — | 1.00 | — | ||
| >$35,000 | 5074 | 79.7 | 0.78 | 0.65–0.95 | * | 0.65 | 0.53–0.80 | *** |
| Metro status | ||||||||
| Nonmetro | 1115 | 17.5 | 1.00 | — | 1.00 | — | ||
| Metro | 5254 | 82.5 | 0.79 | 0.64–0.96 | * | 0.79 | 0.63–0.98 | * |
p < 0.05.
p < 0.01.
p < 0.001.
Discussion
This is the most recent population-based study to examine patterns of local treatment of ESBC among older women. Previous retrospective studies show that older women are more likely to be treated with mastectomy or BCS only, than BCS+RT. We demonstrated that from 2003 to 2009, 22% had BCS without RT, similar to published studies.25 However, the rates of BCS with RT are lower and mastectomy are higher as compared to published literature. Although these differences may in part be due to differences in study inclusion/exclusion criteria, recent studies examining trends in treatment for ESBC have found that women are increasingly opting for more aggressive treatment, such as mastectomy.26,27
Consistent with previous studies,10,28 age was strongly associated with BCS only or mastectomy. Increasing age is commonly cited as the main reason for omission of RT among older women due to greater comorbidity, intolerance to RT toxicity, adverse effects, and shorter life expectancy.14,29,30 In fact, RT is not always recommended for all women over the age of 70 years, as it has not been shown to improve survival among those with shortened life expectancies.31 Similarly, older women may be more likely to receive mastectomy to avoid any adverse effects associated with RT following BCS. However, not all experts agree that RT is more toxic or less tolerable among older women, than younger women. In fact, several studies have found RT to be well-tolerated among older women, and determined that it did not increase the risk of myocardial infarction or cardiovascular disease.32,33 Declining health is a common occurrence among older individuals, and presents additional challenges to undergoing cancer treatments, particularly RT. Although patients with a comorbidity score = 2 were more likely to have mastectomy or BCS only, 43% of women with a score = 0 were treated with mastectomy or BCS only, suggesting that increased comorbidity may not always drive the type of treatment.
Women diagnosed at stage II versus I, were over three times more likely to undergo mastectomy. While the likelihood of mastectomy intuitively increases with increasing stage, it may be that the increasing use of mastectomy among older women can also be partially explained by age. Mastectomy may be increasingly utilized to avoid any adverse effects of RT and the burden of multiple treatments. However, women who had an oncology surgeon involved in their treatment were less likely to be treated with mastectomy or BCS only. Evidence suggest that surgeon specialty is associated with more advanced methods of breast cancer treatment,34 and having both an oncology and general surgeon involved may be an indication of caseload sharing within high volume treatment centers, a factor associated with better treatment practices.35 Moreover, those treated by an oncology surgeon may have shorter travel distances to access specialty care or are more likely to undergo treatments that require repeated visits, such as BCS+RT.36 This may explain why patients who resided in areas with a high density of mammography screening and oncology treatment centers were less likely to have BCS only or mastectomy.
Findings from the stratified analysis of women who were the youngest and healthiest at diagnosis, and thus the most ideal candidates for BCS+RT, barring other unknown factors, showed that considerably more of these women were treated with BCS+RT, than the entire study sample (66.6% vs. 54.5%). It is understandable from a clinical perspective that those diagnosed at stage II versus I and with unfavorable tumor characteristics were more likely to be treated with mastectomy. However, it is troubling that some groups of women in this stratified analysis were also more likely to be treated with BCS only. Not only do women in this subgroup not meet the NCCN guideline requirements for omission of RT because of age, but patients with these cancer characteristics often require more aggressive treatments that include RT when BCS is the surgical treatment choice. It is possible that this finding is explained by the socio-demographic disparities in treatment observed in this subgroup analysis. Women of other race were more likely to be treated with BCS only, while those residing in areas of higher income, and metro areas were less likely to be treated with BCS only. Similarly, women residing in areas of higher education, higher income, and metro areas were less likely to be treated with mastectomy. Therefore, women with vulnerable socio-demographic characteristics with difficulty accessing equitable treatment may also have not been receiving routine mammography screening before diagnosis, leading to a later stage at diagnosis. In the multivariate analyses of the whole study sample, women who had were treated by an oncology surgeon only or both an oncology and general surgeon were less likely to receive mastectomy or BCS only. In the subgroup analysis only a difference in the likelihood for treatment with BCS only was observed. Younger, healthier patients who had an oncology surgeon as part of their care were 35%–56% less likely to have BCS only. This finding reiterates the importance of having an oncology specialist as member of the patient's oncology care team to ensure that all patients have access to specialized oncology care.
Several limitations should be noted when interpreting the results of this study. While this study examined the relationships between type of treatment and a range of covariates, patient preference was not measured. Completion of RT was not assessed, only the initiation of therapy. Another limitation is the lack of information available regarding patients' HER2/neu tumor status and its association with type of treatment. Given that women diagnosed at stage I and II have 99% and 93% 5-year overall survival rates,37 respectively, it is likely that those who die within the first year of diagnosis, die from noncancer related causes. Because this study excluded women who died in the first year following diagnosis, the findings may underrepresent the proportion of women who received less aggressive treatment due to poor health or old age. Finally, the SEER individuals within the SEER database have been found to be of higher income, and higher concentrations of racial and ethnic minorities, compared to the U.S. population.38
Conclusions
A little more than half of older women receive BCS+RT for treatment of ESBC. Women of increasing age, comorbidity, and stage were the most likely to have mastectomy or BCS only. While it may not be appropriate for all elderly women with ESBC to receive RT, some groups of women still do not receive RT with BCS when they are clinically indicated to do so. In particular, this study identified a subgroup of women younger than 70 years, whose omission of RT was associated with access to an oncology specialist and socioeconomic disparities. Current research focusing on individualized and targeted therapies, and immunotherapy may provide more tolerable treatment options for the elderly population. Furthermore, continued efforts are needed to ensure all patients have equitable access to oncology specialty resources and treatment options.
Appendix 1.
Claims Codes Used for Identifying Types of Treatment
| Type of Treatment | ICD-9 Diagnostic | ICD-9 Procedure | HCPCS/CPT | Revenue Center |
|---|---|---|---|---|
| Breast-Conserving Surgery |
85.20–85.29 | 19120, 19125–19126, 19160, 19162, 19301–19302 | ||
| Mastectomy | 85.33–85.36, 85.40–85.48 | 19140, 19180, 19182, 19300, 19303–19307, 19200, 19220, 19240, 19260, 19271–19272 | ||
| Radiation Therapy | V58.0, V66.1, V67.1 | 92.20–92.39 | 77261–77799, G0256, G0261, G0173–G0174, G0243, G0251, G0338–G03340 | 0330, 0333 |
Acknowledgments
This study was funded by the Agency for Healthcare Research and Quality (AHRQ) grant (1 P20 HS15930-02) and partial support from the West Virginia Clinical and Translational Science Institute (WVCTSI), National Institute of General Medical Sciences grant (U54GM104942).
Author Disclosure Statement
No competing financial interests exist.
References
- 1.Fisher B, Anderson S, Bryant J, et al. Twenty-year follow-up trial comparing total mastectomy, lumpectomy, and lumpectomy plus irradiation for the treatment of invasive breast cancer. N Engl J Med 2002;347:1233–1241 [DOI] [PubMed] [Google Scholar]
- 2.Veronesi U, Cascinelli N, Mariani L, et al. Twenty-year follow-up of a randomize study comparing breast-conserving surgery with radical mastectomy for early breast cancer. N Engl J Med 2002;347:1227–1232 [DOI] [PubMed] [Google Scholar]
- 3.Simone NL, Dan T, Shih J, et al. Twenty-five year results of the national cancer institute randomized breast conservation trial. Breast Cancer Res Treat 2012;132:197–203 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 4.American Cancer Society. Cancer Treatment and Survivorship Facts & Figures 2014–2015. Atlanta: American Cancer Society; 2014. Available at: www.cancer.org/acs/groups/content/@research/documents/document/acspc- 042801.pdf Accessed September, 2015 [Google Scholar]
- 5.Mahmood U, Hanlon AL, Koshy M, et al. Increasing national mastectomy rates for the treatment of early-stage breast cancer. Ann Surg Oncol 2013;20:1436–1443 [DOI] [PubMed] [Google Scholar]
- 6.Gradishar WJ, Anderson BO, Blair SJ, et al. Breast cancer version 3.2014. J Natl Compr Canc Netw 2014;12:542–590 [DOI] [PubMed] [Google Scholar]
- 7.Field TS, Bosco JL, Prout MN, et al. Age, comorbidity, and breast cancer severity: Impact on receipt of definitive local therapy and rate of recurrence among older women with early-stage breast cancer. J Am Coll Surg 2011;213:757–765 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 8.Albert JM, Pan IW, Shih YC, et al. Effectiveness of radiation for prevention of mastectomy in older breast cancer patients treated with conservative surgery. Cancer 2012;118:4642–4651 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 9.Dragun AE, Huang B, Tucker TC, Spanos WJ. Disparities in the application of adjuvant radiotherapy after breast-conserving surgery for early-stage breast cancer: Impact on overall survival. Cancer 2011;117:2590–2598 [DOI] [PubMed] [Google Scholar]
- 10.Tuttle TM, Jarosek S, Habermann EB, et al. Omission of radiation therapy after breast- conserving surgery in the United States. Cancer 2012;118:2004–2013 [DOI] [PubMed] [Google Scholar]
- 11.Showalter SL, Grover S, Sharma S, et al. Factors influencing surgical and adjuvant therapy in stage I breast cancer: A SEER 18 database analysis. Ann Surg Oncol 2013;20:1287–1294 [DOI] [PubMed] [Google Scholar]
- 12.Luu C, Goldstein L, Goldner B, et al. Trends in radiotherapy after breast-conserving surgery in older patients with early-stage breast cancer. Ann Surg Oncol 2013;20:3266–3273 [DOI] [PubMed] [Google Scholar]
- 13.Hughes KS, Schnaper LA, Bellon JR, et al. Lumpectomy plus tamoxifen with or without irradiation in women age 70 years or older with early breast cancer: Long-term follow-up of CALGB 9343. J Clin Oncol 2013;31:2382–2387 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 14.Schonberg MA, Marcantonio ER, Li D, et al. Breast cancer among the oldest old: Tumor characteristics, treatment choices, and survival. J Clin Oncol 2010;28:2038–2045 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 15.Anderson RT, Morris CR, Kimmick G, et al. Patterns of locoregional treatment for nonmetastatic breast cancer by patient and health system factors. Cancer 2014;121:790–799 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 16.Hughes KS, Schnaper LA, Berry D, et al. Lumpectomy plus tamoxifen with or without irradiation in women 70 years of age or older with early breast cancer. N Engl J Med 2004;351:971–977 [DOI] [PubMed] [Google Scholar]
- 17.Rhieu BH, Rajagopalan MS, Sukumvanich P, et al. Patterns of care for omission of radiation therapy for older women with early-stage breast cancer receiving hormonal therapy. Pract Radiat Oncol 2015;5:e267–e273 [DOI] [PubMed] [Google Scholar]
- 18.McCormick B, Ottesen RA, Hughes ME, et al. Impact of guideline changes on use or omission of radiation in the older with early breast cancer: Practice patterns at National Comprehensive Cancer Network institutions. J Am Coll Surg 2014;219:796–802 [DOI] [PubMed] [Google Scholar]
- 19.Lautner M, Lin H, Shen Y, et al. Disparities in the use of breast-conserving therapy among patients with early-stage breast cancer. JAMA Surg 2015;150:778–786 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 20.Nesvold IL, Dahl AA, Løkkevik E, et al. Arm and shoulder morbidity in breast cancer patients after breast-conserving therapy versus mastectomy. Acta Oncol 2008;47:835–842 [DOI] [PubMed] [Google Scholar]
- 21.Engels EA, Pfeiffer RM, Ricker W, et al. Use of Surveillance, Epidemiology, and End Results-Medicare data to conduct case-control studies of cancer among the US older. Am J Epidemiol 2011;174:860–870 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 22.U.S. Health Resources and Services Administration. Bureau of Health Professions. Area Resource File, 2009–2010 Release. Rockville, MD: U.S. Department of Health and Human Services; Fairfax, VA: Quality Resource Systems, Inc. 2010; Codebook: HE-001(2010) [Google Scholar]
- 23.Klabunde CN, Potosky AL, Legler JM, Warren JL. Development of a comorbidity index using physician claims data. J Clin Epidemiol 2000;53:1258–1267 [DOI] [PubMed] [Google Scholar]
- 24.Charlson ME, Pompei P, Ales KL, MacKenzie CR. A new method of classifying prognostic comorbidity in longitudinal studies: Development and validation. J Chronic Dis 1987;40:373–383 [DOI] [PubMed] [Google Scholar]
- 25.Kiderlen M, Bastiaannet E, Walsh PM, et al. Surgical treatment of early-stage breast cancer in older: An international comparison. Breast Cancer Res Treat 2012;132:675–682 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 26.Kummerow KL, Du L, Penson DF, Shyr Y, Hooks MA. Nationwide trends in mastectomy for early-stage breast cancer. JAMA Surg 2015;150:9–16 [DOI] [PubMed] [Google Scholar]
- 27.Vaz-Luis I, Hughes ME, Cronin A, et al. Trends in the use of mastectomy in women with small node-negative breast cancer treated at US academic centers. Breast Cancer Res Treat 2016;155:569–578 [DOI] [PubMed] [Google Scholar]
- 28.Soulos PR, Yu JB, Roberts KB, et al. Assessing the impact of a cooperative group trial on breast cancer care in the Medicare population. J Clin Oncol 2012;30:1601–1607 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 29.Harris EE, Correa C, Hwang WT, et al. Late cardiac mortality and morbidity in early-stage breast cancer patients after breast-conservation treatment. J Clin Oncol 2006;24:4100–4106 [DOI] [PubMed] [Google Scholar]
- 30.Landoni V, Giordano C, Marsella A, et al. Evidence from a breast cancer hypofractionated schedule: Late skin toxicity assessed by ultrasound. J Exp Clin Cancer Res 2013;32:80. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 31.Schwartzberg LS, Blair SL. Strategies for the Management of Early-Stage Breast Cancer in Older Women. J Natl Compr Canc Netw 2016;14(5 Suppl):647–650 [DOI] [PubMed] [Google Scholar]
- 32.Haque R, Prout M, Geiger AM, et al. Comorbidities and cardiovascular disease risk in older breast cancer survivors. Am J Manag Care 2014;20:86–92 [PMC free article] [PubMed] [Google Scholar]
- 33.Plataniotis GA, Theofanopoulou MA, Sotiriadou K, Kyrgias G. Hypofractionated radiotherapy for breast cancer patients treated by breast-conserving surgery: Short-term morbidity and preliminary results. Breast Cancer 2010;17:42–47 [DOI] [PubMed] [Google Scholar]
- 34.Yen TW, Laud PW, Sparapani RA, Nattinger AB. Surgeon specialization and use of sentinel lymph node biopsy for breast cancer. JAMA Surg 2014;149:185–192 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 35.Kimmick GG, Camacho F, Mackley HB, et al. Individual, area, and provider characteristics associated with care received for stages I to III breast cancer in a multistate region of Appalachia. J Oncol Pract 2015;11:e9–e18 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 36.Wheeler SB, Kuo TM, Durham D, et al. Effects of distance to care and rural or urban residence on receipt of radiation therapy among North Carolina Medicare enrollees with breast cancer. N C Med J 2014;75:239–246 [DOI] [PubMed] [Google Scholar]
- 37.Howlader N, Noone AM, Krapcho M, Garshell J, Neyman N, Altekruse SF, et al. SEER Cancer Statistics Review, 1975–2010. Bethesda, MD: National Cancer Institute; http://seer.cancer.gov/csr/1975_2010/, based on November 2012. SEER data submission, posted to the SEER web site, April 2013 [Google Scholar]
- 38.Warren JL, Klabunde CN, Schrag D, et al. Overview of the SEER-Medicare data: Content, research applications, and generalizability to the United States older population. Med Care 2002;40(8 Suppl):IV, 3–18 [DOI] [PubMed] [Google Scholar]
