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Evolving Treatment Strategies for Inflammatory Breast Cancer: A Population-Based Survival Analysis

From the Breast Cancer Outcomes Unit, Radiation, and Systemic Therapy Programs of the BC Cancer Agency, University of British Columbia, and University of Victoria, Victoria, British Columbia, Canada

Address reprint requests to I.A. Olivotto, MD, Breast Cancer Outcomes Unit, BC Cancer Agency—Vancouver Island Centre, 2410 Lee Avenue, Victoria, BC, Canada V8R 6V5; e-mail: iolivott{at}bccancer.bc.ca

	ABSTRACT

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PURPOSE: To determine if mastectomy (Mx) use, chemotherapy (CT) intensity, or treatment sequence of CT, radiation therapy (RT), and Mx have improved outcome for inflammatory breast cancer (IBC).

PATIENTS AND METHODS: A retrospective analysis of 485 patients with IBC diagnosed in British Columbia between 1980 and 2000 analyzed locoregional relapse-free survival (LRFS) and breast cancer–specific survival (BCSS) by treatment intent and treatment received. Curative intent was defined as delivery of more than four cycles of anthracycline-based CT plus locoregional RT in patients without distant metastases.

RESULTS: Median follow-up among survivors was 6.5 years. Median BCSS was 1.0 and 3.2 years for patients with distant metastases at diagnosis or those who were curatively treated, respectively. Among patients treated curatively (n = 308), there were no significant differences in LRFS or BCSS with timing of Mx before or after CT/RT, time between diagnosis and RT, or the sequence of RT and CT. Patients receiving more intensive CT had improved 10-year BCSS compared with standard CT (43.7% v 26.3%; P = .04). Ten-year LRFS for patients having Mx after CT, Mx before CT, and without Mx was 62.8%, 58.6%, and 34.4%, respectively (P = .0001); the corresponding 10-year BCSS was 36.9%, 19.9%, and 22.5%, respectively (P = .005). On multivariate analysis, Mx was associated with improved LRFS (P = .04). Independent prognostic factors for BCSS were menopausal status (P = .02), estrogen receptor status (P = .02), and CT type (P = .05).

CONCLUSION: This retrospective analysis suggested that mastectomy, in conjunction with CT and RT, seemed to enhance locoregional control, whereas modern CT regimens seemed to improve BCSS.

	INTRODUCTION

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Inflammatory breast cancer (IBC) is an uncommon, rapidly progressive variant of breast cancer characterized by high rates of locoregional recurrence, distant metastases, and mortality.^1-8 In the past, IBC was almost universally fatal and mastectomy (Mx) was not recommended.¹ Attempts to improve outcome have included the use of various chemotherapy (CT) regimens combined in various sequences with radiation therapy (RT) with or without Mx. Evidence-defining management has been based largely on institutional series or extrapolation from experience with non-IBC, and has been limited by small sample sizes, heterogeneous treatment, and variable response criteria. Only one randomized trial included a significant number of patients with IBC.⁸ That study found that CT dose intensification did not improve outcome.

Acknowledging the limitations of existing data, current consensus is that anthracycline-based CT, RT, Mx, and hormone therapy (HT) all have a role in the potentially curative management of selected patients.^2-10 The optimal strategy to integrate the different modalities is controversial. In particular, the sequence of RT relative to CT, the use and timing of Mx, and the intensity of CT have evolved during the last two decades. The effect of evolving therapeutic practices on patient outcome is unclear. This analysis of a large, population-based cohort of women with IBC treated curatively between 1980 and 2000 was designed to determine if changes in the use of CT, RT, and Mx improved locoregional control or survival for women with IBC.

	PATIENTS AND METHODS

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Using the Breast Cancer Outcomes Unit database of the British Columbia Cancer Agency (BCCA), patients with IBC diagnosed between January 1, 1980, and December 31, 2000, and referred to the BCCA were identified. Patients were considered to have been treated with curative intent if they did not have metastases beyond the ipsilateral supraclavicular fossa and the initial treatment intent was to deliver combined CT/RT with more than four cycles of anthracycline-containing CT ( Table 1).

Ten-year Kaplan-Meier estimates of locoregional relapse-free survival (LRFS), breast cancer–specific survival (BCSS), and overall survival (OS) were determined. LRFS was defined as time from diagnosis to relapse within the ipsilateral breast, chest wall, axillary, supraclavicular, or internal mammary nodal regions, before and after any distant recurrence. BCSS was defined as time from diagnosis to death as a result of breast cancer as the primary or underlying cause. If the cause of death was unknown but the patient had experienced a breast cancer relapse (local, regional, or distant) or had a subsequent new primary breast cancer, the death was attributed to breast cancer. OS was defined as time from diagnosis to death or the last date the participant was known to be alive.

The following curative-intent CT protocols were used: doxorubicin 50 mg/m², fluorouracil (FU) 500 mg/m², and cyclophosphamide 500 mg/m² (FAC), all intravenously every 3 weeks for six to eight cycles, including nine patients who received a median of eight cycles (range, five to nine cycles) of doxorubicin 60 mg/m² and cyclophosphamide 600 mg/m² (AC) and one who received eight cycles of cyclophosphamide, mitoxantrone, and FU; doxorubicin 40 mg/m² and cyclophosphamide 200 mg/m² week 1 alternating with methotrexate 350 mg/m² and FU 1,000 mg/m² week 3 (AC/MF) every 4 weeks for six cycle pairs¹²; epirubicin 60 mg/m² and FU 500 mg/m² intravenously on days 1 and 8, with cyclophosphamide 75 mg/m² orally (CEF) for 14 days every 4 weeks for six cycles¹³; doxorubicin 60 mg/m² and paclitaxel 175 mg/m² every 3 weeks for four cycles plus cisplatin 60 mg/m² and paclitaxel 90 mg/m² every 2 weeks for four cycles, or cisplatin 60 mg/m² and paclitaxel 90 mg/m² every 2 weeks for four cycles plus doxorubicin 60 mg/m² and paclitaxel 175 mg/m² every 3 weeks for four cycles (AT/PT)¹⁴; and a multiagent CT regimen including doxorubicin, cyclophosphamide, methotrexate, etoposide, FU, and cisplatin (Quartet) as an alternating 15-week outpatient regimen followed by high-dose CT (cyclophosphamide 3,000 to 4,500 mg/m² intravenously, etoposide 900 to 1,500 mg/m², and cisplatin 75 mg/m²) in divided doses over 3 days in the hospital.¹⁵

Clinical responses to CT plus RT were determined 8 to 12 weeks after the last treatment and before Mx, if performed. Complete response (CR) was defined as a complete disappearance of all clinical evidence of disease. Patients rarely had objective measurements of disease recorded. Partial response (PR) was defined as a greater than 50% decrease in the product of cross-sectional measurements (if they existed) or if the physician's notes indicated a significant or dramatic decrease in the clinical evidence of disease but not a CR. Patients were not assessable for response if Mx was performed before the completion of CT or if there were no clinical notes about response before Mx. Pathologic response was assessed for patients with Mx after CT or CT/RT. Pathologic response was complete (pCR) if there was no residual invasive disease in the breast or lymph nodes, or less than complete if there was residual invasive disease in the breast, lymph nodes, or both.

Kaplan-Meier survival times were calculated from the date of diagnosis to the date of locoregional recurrence (LRFS), death as a result of breast cancer (BCSS), death as a result of any cause (OS), or date of last known follow-up. Differences in survival were compared with log-rank statistics. Multivariable analysis of LRFS and BCSS was performed using the Cox proportional hazards model. Cox analyses were conducted using the following variables: study period (1980 to 1985, 1986 to 1990, 1991 to 1995, and 1996 to 2000), age ( 50 v > 50 years), histologic grade (I or II v III), menopausal status (pre- v postmenopausal), ER status (positive v negative), CT (FAC or AC/MF v intense CT), Mx use and timing (no Mx v Mx before CT/RT, no Mx v Mx after CT/RT, and Mx before v Mx after CT/RT), and RT timing (early RT v late RT, based on whether RT was administered within 183 days from diagnosis or if RT was initiated before or after completion of CT). The results were confirmed using the backward selection model. The last follow-up abstraction was in February 2004. All statistical tests were performed using SPSS software, Version 10.1 (SPSS Inc, Chicago, IL).

	RESULTS

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Among 31,763 patients with breast cancer diagnosed in British Columbia or the Yukon and referred to the BCCA between 1980 and 2000, 485 (1.5%) had IBC. Of these, 308 were treated curatively and were the study participants. Table 1 lists the reasons for exclusion of 177 participants from the curatively treated cohort. If the intent was curative, but treatment was incomplete because of disease progression (n = 13) or adverse effects from the planned treatment (n = 6), participants were retained in the curative-intent analysis.

Median follow-up time for surviving patients was 6.5 years (range, 0.7 to 19.0 years). The median BCSS of curatively treated patients was 3.2 years (95% CI, 2.6 to 3.9 years). The median BCSS for those patients presenting with distant metastases was 1.0 year (95% CI, 0.76 to 1.16 years). Clinical, tumor, and treatment characteristics of all patients (n = 485) and of the curatively treated cohort (n = 308) are listed in Table 2. Among 485 patients, 380 deaths occurred; all but 41 (10.8%) were a result of breast cancer. In the 308 curatively treated patients there were 217 deaths, of which 16 (5.2%) were not as a result of breast cancer. Because OS and BCSS were closely parallel, additional survival analyses focused on BCSS.

View larger version (15K): [in this window] [in a new window]   Fig 1. (A) Locoregional relapse-free survival based on date of diagnosis. (B) Breast cancer–specific survival based on date of diagnosis.

RT Timing
The impact of early versus late RT was examined by the delivered sequence of CT/RT and by the interval between diagnosis and start of RT. Early RT was defined as either (1) RT before CT or sandwich RT (RT after 3 months of a 6-month course of CT), or (2) RT started within 183 days from diagnosis. Using definition 1, 40 patients (13.4%) had early RT and 259 (86.6%) had late RT. Definition 2 included 179 patients (59.9%) who had early RT and 120 patients (40.1%) who had late RT. Nine patients who did not receive RT because of disease progression (n = 6) or complications during CT (n = 3), were excluded. There were no significant differences in LRFS or BCSS associated with RT timing using either definition. Table 3 lists the results of RT timing relative to diagnosis.

View larger version (16K): [in this window] [in a new window]   Fig 2. (A) Locoregional relapse-free survival based on type of initial chemotherapy. (B) Breast cancer–specific survival based on type of initial chemotherapy. CEF, epirubicin, fluorouracil (FU), cyclophosphamide; AT/PT, doxorubicin and paclitaxel plus cisplatin and paclitaxel, or cisplatin and paclitaxel plus doxorubicin and paclitaxel; Quartet, doxorubicin, cyclophosphamide, methotrexate, etoposide, FU, and cisplatin; FAC, doxorubicin, FU, cyclophosphamide; AC/MF, doxorubicin, cyclophosphamide, methotrexate, FU.

View larger version (37K): [in this window] [in a new window]   Fig 3. Use of mastectomy (Mx) for inflammatory breast cancer between 1980 and 2000 in British Columbia. CT/RT, chemotherapy plus radiation therapy.

View larger version (19K): [in this window] [in a new window]   Fig 4. (A) Locoregional relapse-free survival based on mastectomy (Mx) use and timing. (B) Breast cancer–specific survival based on Mx use and timing. CT/RT, chemotherapy plus radiation therapy.

View larger version (14K): [in this window] [in a new window]   Fig 5. Breast cancer–specific survival based on pathologic complete response (pCR) at mastectomy after chemotherapy plus radiation therapy.

View larger version (15K): [in this window] [in a new window]   Fig 6. Breast cancer–specific survival based on estrogen receptor (ER) status.

	DISCUSSION

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During the two decades of this study, anthracycline-based CT was the mainstay of systemic treatment for patients with IBC. The most common CT regimen was FAC. During the 1980s, a treatment combination designed in accordance with the Goldie-Coldman hypothesis²⁰ used AC alternating with MF CT every 2 weeks.¹² The AC/MF combination was associated with identical LRFS and BCSS compared with standard FAC. In the 1990s, patients continued to be treated with FAC, but a subset of patients (n = 56) were treated with investigational protocols or more intensive CT.^13-15 The more intense CT regimens were associated with a pCR rate of 35% and significantly improved 10-year BCSS compared with patients receiving AC/MF or FAC. More intense adjuvant CT has been associated with improved disease-free survival.^21-23 However, escalation of intensity beyond CEF did not improve pCR or survival rates.^8,24,25 Fit patients should receive CT that is more intense than FAC but short of requiring stem-cell support.

During the course of this study, the timing of RT varied. A minority of patients had sandwich RT within the first 3 months of combined CT/RT, often together with an immediate single 8-Gy fraction to the breast the day before the first CT cycle. Current practice is to deliver RT after the completion of CT, either before or after Mx.^2-10 Even though IBC has a rapid growth potential, delaying RT until after CT completion did not adversely effect LRFS, BCSS, or OS. It is therefore reasonable to place RT at a convenient place in the sequence of combined-modality therapy. Patients who demonstrate a good response to systemic therapy or who participate in translational research protocols that require tissue specimen collection before and after CT may reasonably receive RT after Mx. Patients with little or no response to CT may be better served by earlier institution of RT in the hopes of obtaining a response that would make it feasible to achieve clear margins at the time of Mx.¹⁰

Patients presenting with supraclavicular lymph node metastases were included in the cohort of patients eligible for curative treatment because recent studies had demonstrated that such patients have a prognosis similar to patients with stage IIIB rather than stage IV disease.^26,27 This observation led the American Joint Committee on Cancer to reclassify patients with supraclavicular nodal metastases from M₁ to N₃ in the 2003 revision (sixth edition) of the TNM staging classification.²⁸ In the present study however, supraclavicular lymph node metastases at diagnosis (n = 32) were a significant adverse prognostic factor. Such patients had a median OS of just 1.85 years.

Another adverse prognostic factor was the presence of ER-negative disease (P = .003). Patients with ER-negative breast cancer experienced disease recurrence earlier but their ultimate 10-year BCSS was comparable with that of patients with ER-positive disease. The 10-year BCSS was 26% for patients with ER-negative and 29% for patients with ER-positive disease.

pCR was a favorable prognostic factor for BCSS. The 28% of patients with a pCR at Mx after CT or CT/RT had a 10-year BCSS of 67%, which was significantly higher than in patients with residual invasive disease in the breast, nodes, or both. Other studies of patients with breast cancer have shown that pCR is associated with improved survival outcomes^29,30 but not necessarily for IBC.⁶

This study is subject to the limitations of all retrospective analyses including nonrandom treatment allocation. Mx was associated with improved locoregional control, but patients without Mx may have had more extensive disease at presentation. Progression of disease was not the reason for lack of Mx. In fact, only 21 patients experienced disease progression during initial CT and 10 of them had an Mx. Of those patients who did not have an Mx, 73% achieved at least a partial response to the combined CT/RT. These patients would have been eligible for Mx but it either was not offered or was declined. The lack of Mx was generally due to a treatment policy discouraging Mx use for IBC in the earlier years of this study. Mx use increased over time, thus patients without Mx would have had longer follow-up. This difference was accommodated by using Kaplan-Meier analyses and reporting 10-year outcomes. Patients receiving more intense CT protocols in the 1990s may have been more fit or motivated to accept toxic treatment than patients treated with FAC. We do not have sufficient data to asses this definitively, but comparison of the median ages showed no significant difference between CT groups (54.1 years for patients receiving AC/MF or FAC and 51.3 years for patients receiving more intense CT; P = .10).

In summary, this study has confirmed the poor but not uniformly fatal prognosis of IBC. An aggressive, multimodality approach incorporating anthracycline-based CT, Mx, and locoregional radiation is warranted. This should be followed by a hormonal intervention for those with ER-positive disease. Without evidence that outcome was associated with the timing of either Mx or RT, these modalities may be safely integrated into the management of IBC based on individual characteristics such as response to CT, patient or physician preference, or research protocol requirements.

	Authors' Disclosures of Potential Conflicts of Interest

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The authors indicated no potential conflicts of interest.

	NOTES

 
Supported by a grant from the Canadian Breast Cancer Foundation, British Columbia and Yukon Chapters.

Presented in part at the Canadian Association of Radiation Oncologists Annual Meeting, Halifax, Nova Scotia, September 9–12, 2004, and San Antonio Breast Cancer Symposium, San Antonio, TX, December 8–11, 2004.

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

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Submitted June 30, 2004; accepted December 20, 2004.

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