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10.1245/ASO.2004.02.001
Annals of Surgical Oncology 11:1011-1017 (2004)
© 2004 Society of Surgical Oncology
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ORIGINAL ARTICLES

Risk Factors for Recurrence and Death After Primary Surgical Treatment of Malignant Phyllodes Tumors

Oktar Asoglu, MD, Mustafa M. Ugurlu, MD, Kay Blanchard, MD, Clive S. Grant, MD, Carol Reynolds, MD, Steven S. Cha, MS and John H. Donohue, MD

From the Department of Surgery (OA, MMU, KB, CSG, JHD), Department of Laboratory Medicine and Pathology (CR), and Division of Biostatistics (SSC), Mayo Clinic and Mayo Foundation, Rochester, Minnesota.

Correspondence: Address correspondence and reprint requests to: John H. Donohue, MD, Mayo Clinic, 200 First Street SW, Rochester, MN 55905; Fax: 507-284-5196; E-mail: donohue.john{at}mayo.edu


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: Malignant phyllodes tumor (MPT) is a rare but aggressive breast malignancy. The aim of this study was to evaluate parameters that influence outcome in patients with MPT.

Methods: Fifty women were diagnosed with MPT of the breast and treated between August 1971 and July 2000. All medical records were reviewed retrospectively. The Cox regression model was used for multivariate analysis.

Results: Tumors were classified as borderline (6%), low grade (32%), or high grade (62%). The median patient age was 46 years (range, 14–77 years). The median tumor diameter was 3.5 cm (range, 1.5–18 cm). Twenty-two patients had wide local excision (WLE), and 28 patients had mastectomy. The median follow-up was 91 months (range, 12–360 months). Local recurrence (LR) occurred in 16 patients (32%) an average of 26 months after surgery (median, 17 months; range, 3–72 months). Distant metastasis occurred in 13 patients (26%) at an average of 53.4 months (median, 36 months; range, 4–177 months). Sixteen (32%) patients have died of their disease. LR was significantly increased with stromal overgrowth (P < .0001), large tumor size (P = .0177), and surgical margins <1 cm (P = .0120), but not with WLE (P = .5099). Stromal overgrowth was the only independent variable predictive of systemic metastasis (P < .0001) and patient survival (P < .0001).

Conclusions: Stromal overgrowth in MPT carries a grave prognosis. Close surgical margins and large tumor size, but not type of operation, significantly increased LR. Either WLE with adequate margins or mastectomy is an appropriate treatment for patients with MPT.

Key Words: Malignant phyllodes • Surgical treatment • Local recurrence • Breast


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Phyllodes tumors are rare fibroepithelial neoplasms that account for .3% to .9% of all breast tumors in women.1–4 Although most phyllodes tumors occur in women between the ages of 35 and 55 years,2,5–7 adolescent and elderly women are also affected.6,8–10 Between 10% and 40% of phyllodes tumors have a malignant biology (malignant phyllodes tumor; MPT) and a tendency for local recurrence (LR) and general dissemination.11–16 Mastectomy traditionally has been the treatment of choice, but recently, the popularity of breast-conserving therapy in the management of phyllodes tumors has increased. This retrospective study evaluates the causes of LR and distant metastasis (DM) plus prognostic factors affecting survival, to better define appropriate treatment strategies in the management of MPT.


   METHODS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Between August 1971 and July 2000, 50 women were diagnosed with MPT on the basis of histological criteria and were treated surgically at the Mayo Clinic. All medical records were reviewed retrospectively. MPT was pathologically categorized on the basis of the following histological criteria: tumor borders, mitotic activity, stromal atypia, and stromal overgrowth. The criteria for borderline, low-grade, and high-grade MPTs are listed in Table 1. Stromal overgrowth was defined as disproportionate proliferation of the stromal components without glandular elements in a single x40 field. Fifty patients with full details on clinical outcome were included in this study. Patient characteristics, pathologic variables, and surgical procedures were investigated as predictors of LR, DM, and survival. Two types of surgical procedures—WLE (with an attempt for a margin >1 cm) and mastectomy—were performed, depending on tumor size, margin involvement, and patient or surgeon preference. Tumors were subdivided into three groups according to their maximum measured diameter: <5 cm, 5 to 10 cm, and >10 cm. Treatment failures were classified as LR (involving the breast, chest wall/axilla, or surgical bed) or DM.


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  		TABLE 1. Tumor grading criteria
 
Life tables were constituted with the Kaplan-Meier method, and survival curves were compared by using the log-rank test. Cox regression analysis was used to assess the multivariate relationship between the clinical, surgical, and pathologic factors and outcomes of LR, DM, and survival. Hazard ratios were constructed by using Cox regression analysis.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Patient Demographics/Presentation
The median patient age was 46 years (range, 14–77 years). Thirty-four (64%) patients were premenopausal, and 16 (32%) were postmenopausal. In 30 (60%) patients the tumor occurred in the right breast, and in 20 (40%) patients it occurred in the left breast. No patient had bilateral disease. Three (6%) patients reported a history of benign breast masses. No patient had a history of nonbreast malignancy. All patients presented with a breast mass.

Pathologic Features
MPTs were classified as borderline (n = 3; 6%), low grade (n = 16; 32%), or high grade (n = 31; 62%) on the basis of histological findings. The median tumor size was 3.5 cm (range, 1.5–18 cm). Fifty-four percent of patients had tumors <5 cm in their greatest dimension, and 40% had tumors >5 cm in their greatest dimension. Before referral to our institution, three patients had excisional breast biopsy, and the tumor diameter was unknown. Stromal overgrowth was detected in 12 patients (24%). Axillary dissection was performed in five patients (10%), but only one patient (2%) had pathologically proven nodal involvement.

Primary Tumor Treatment
Twenty-two patients (44%; 3 borderline, 9 low-grade, and 10 high-grade MPT) had WLE, and 28 patients (56%; 7 low-grade and 21 high-grade MPT) had mastectomy. Of the mastectomy patients, five had initial local excision but subsequent mastectomy within 1 month because of positive histological margins. Of the 22 WLEs, 3 required re-excision to obtain a negative margin. Transverse rectus abdominis myocutaneous flap reconstruction was performed in six (21%) of the mastectomy patients, five of which were performed immediately after mastectomy. Both adjuvant radiotherapy (5000 cGy) and chemotherapy (5-fluorouracil and doxorubicin) were given to two patients (7%) after mastectomy because of microscopically positive margins.

Clinical Outcome
Local Recurrence
With a median follow-up of 91 months (range, 12–360 months), LR occurred in 16 patients (32%) at an average of 26 months after surgery (median, 17 months; range, 3–72 months). The LR rates after WLE and mastectomy were 36% and 28%, respectively (P = .5). Of the eight women who had an LR after WLE, only two (25%) also developed DM, both after diagnosis of LR. Eight women had an LR after mastectomy for MPT, and six (75%) also had distant disease. The prevalence of LR by tumor characteristics and operative therapy is listed in Table 2. In multivariate analysis, LR was significantly increased by the presence of stromal overgrowth (P < .0001; Fig. 1), surgical margins <1 cm (P = .0120; Fig. 2), and tumor diameter >5 cm (P = .0177; Fig. 3). LR was increased by more than 7-fold with stromal overgrowth, more than 4-fold by close margins, and 4-fold by tumor size (Table 3).


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  		TABLE 2. Prevalence of local recurrence by tumor characteristics and operative therapy
 


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  		FIG. 1. Risk of malignant phyllodes tumor local recurrence according to the presence or absence of stromal overgrowth.

 


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  		FIG. 2. Risk of malignant phyllodes tumor local recurrence according to resection margin <1 cm or ≥1 cm.

 


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  		FIG. 3. Risk of malignant phyllodes tumor local recurrence according to tumor diameter <5 cm, 5 to 10 cm, or >10 cm.

 

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  		TABLE 3. Hazard ratios for local recurrence
 
After WLE, LR occurred in eight patients. The initial recurrence was treated with mastectomy (n = 5) or repeat WLE (n = 3). Four patients—two had WLE and two had mastectomies—did not experience a second disease relapse. Three patients with LR after WLE who underwent mastectomy died of DM (lung metastases), all within 9 months. The final patient had a second LR after repeat WLE and underwent a completion mastectomy. She had a chest wall recurrence 1 month later. This was treated with en-bloc chest wall resection and radiotherapy. Unfortunately, 5 months later, a fourth LR was diagnosed. Despite a second chest wall resection plus doxorubicin and cisplatin chemotherapy, she died of disease 48 months after her original treatment.

LR occurred in eight patients after mastectomy. In one patient, the LR was treated with local excision 48 months after mastectomy. Lung and bone metastases were detected 91 months after her original operation. She died of the DM 4 months later. In four women, en-bloc chest wall resection was performed for LR after mastectomy. The resections included partial pneumonectomies in two patients for metastasis or direct tumor extension. Of these four women, one died within 5 months with DM (abdominal metastases). The second patient underwent en-bloc chest wall resection and partial pneumonectomy 16 months after mastectomy for a second chest wall recurrence. She died of metastatic disease 10 months later. The third patient had three consecutive local excisions and radiotherapy for LR before presenting with a fourth chest wall recurrence 21 months after her mastectomy. En-bloc chest wall resection was performed, but she died of DM (lung metastasis) 48 months after her initial operation. The last woman in this cohort had a chest wall resection and partial pneumonectomy because of a chest wall recurrence and solitary pulmonary metastasis. Brain metastases were detected, and she died of her metastases 5 months later. Another patient with LR after mastectomy had MPT involving the left lung and pleura. A partial pneumonectomy and excision of the parietal pleura was performed, with clear margins. This patient died of metastatic disease 36 months later. Two patients with LR after mastectomy had inoperable disease. One woman had an axillary mass. On computed tomographic scan, the tumor extended into the chest and the retroperitoneum. A complete resection was attempted, but clear margins could not be obtained. The patient died of her disease less than 3 months later. The last patient with LR after mastectomy had radiotherapy after her primary resection because of a positive resection margin. An inoperable chest wall LR with involvement of the lung and major vessels was diagnosed, and she died 5 months later.

Distant Metastasis
DM occurred in 13 (26%) of 50 patients at a mean of 53.4 months after the primary operation (median, 36 months; range, 4–77 months). DM developed in the lung (n = 11; 85%), bone (n = 4; 31%), liver and abdomen (n = 2; 15%), and brain (n = 1; 8%). Five patients had more than one site of DM. The prevalences of DM by tumor characteristics and operative therapy are listed in Table 4. Eight of the 13 patients with DM had an LR on average 24.3 months (range, 0–86 months) before the diagnosis of DM. All 13 patients who developed DM were treated with chemotherapy (doxorubicin, ifosfamide, or both), radiotherapy, or both. Surgical excision of DM was performed in three women (23%), including an intra-abdominal metastasectomy and two partial pneumonectomies. All patients died an average of 7 months (range, 1–19 months) after diagnosis of DM. Stromal overgrowth was the only significant predictor for DM (P < .0001; Fig. 4). Hazard ratios for several variables are listed in Table 5.


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  		TABLE 4. Prevalence of distant metastases by tumor characteristics and operative therapy
 


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  		FIG. 4. Risk of malignant phyllodes tumor distant metastases according to stromal overgrowth.

 

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  		TABLE 5. Hazard ratios for distant metastases
 
Survival
Actuarial overall survival was 75% at 5 years and 57% at 10 years. At last follow-up, 29 patients (58%) were free of disease, 3 patients (6%) were alive with disease, 16 patients (32%) had died of disease, and 2 patients (4%) had died of unknown causes. The hazard ratios for several variables predicting survival with Cox proportional hazard models are listed in Table 6. Stromal overgrowth had the most significant effect on patient survival (P < .0001; Fig. 5), but surgical margins of <1 cm also significantly affected patient outcome (P = .0302).


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  		TABLE 6. Hazard ratios for patient survival
 


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  		FIG. 5. Patient survival according to stromal overgrowth.

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Phyllodes tumor is a rare tumor that behaves unpredictably. Surgical treatment remains the mainstay of therapy for patients with phyllodes tumor. Most studies of phyllodes tumor include those with both benign and more malignant pathologic features, and the criteria to predict LR and DM have been controversial. There are no randomized protocols comparing different surgical procedures, and there have been only a few studies limited to MPT patients.17–19 Our study evaluated the prevalence of LR and DM, plus prognostic factors to better define treatment strategies for patients with MPT whom our pathologists believed to be at greater risk for recurrent disease.

LR is a common occurrence with MPT, with reported rates ranging from 20% to 65%.6,18,20–24 This variability arises partly from small patient numbers and partly because most patients were treated with mastectomy in some publications. Previous studies have not correlated tumor size and LR,2,12,25,26 but most authors have found negative surgical margins to be an important risk factor for LR and have recommended ≥1-cm margins.2,6,18,21,25,27,28 Mangi et al.28 found that all LRs occurred in patients with a margin of <1 cm. In our study, LR was detected in 16 patients (32%), with a mean time to recurrence of 26 months. Stromal overgrowth, larger tumor size, and involved margin were all significantly correlated with LR. Stromal overgrowth increased the probability of LR 7-fold, whereas if the margin was <1 cm, the risk of LR increased 5-fold, and if tumor size was >10 cm, then the prevalence of LR was four times greater than for smaller tumors.

We found no statistical difference in the incidence of LR between patients treated with WLE and mastectomy. Similar results have been reported by Kapiris et al.18 Of their 48 patients with phyllodes tumors, LR occurred in 21 (44%) of 48 patients: 6 (60%) of 10 patients after local excision, 4 (28%) of 14 patients after WLE, and 11 (46%) of 24 patients after mastectomy. A retrospective study by Pandey et al.17 reported 36 patients with MPT, 69% of whom received postoperative radiotherapy. Among the 72% of their patients who had mastectomy, LR occurred in 22%, and the surgical margin was the only independent predictor of LR. A meta-analysis of phyllodes tumors by Barth24 showed an LR of 65% after local excision, whereas only 36% of phyllodes tumors recurred after WLE and 12% after mastectomy. Their data indicate that WLE might not be as good an option to prevent LR; however, there is no evidence that breast-conserving surgery for patients with MPT resulted in reduced patient survival compared with mastectomy.

In most patients, axillary lymph nodes are not palpable at presentation, because metastatic spread of these tumors is primarily hematogenous. Metastasis to axillary lymph nodes occurred in only 2% of our patients, a finding in agreement with most other studies.1,4,14,15,18,19,28,29 Lymphadenectomy is indicated only for suspicious lymph nodes in women with MPT.

DM in patients with phyllodes tumors has ranged from 25% to 40%.1,2,12,18,29,30 The lungs, pleura, and bone have been the most common sites of metastasis.18,29 Tumor size, stromal atypia, mitotic activity,2,5,18,26,29,21,31,32 LR,13,14,18,33 and surgical excision margin18 have been described as predictors for DM. Ward and Evans34 showed that pathologic features such as tumor necrosis, mitotic rate, stromal cellularity, nuclear size, and pleomorphism had no effect on treatment results but that stromal overgrowth was a highly significant prognostic factor. Cox multivariate regression analysis found stromal overgrowth to be the only independent predictor of DM in our study. Other reports have also demonstrated stromal overgrowth as an important predictor of aggressive tumor behavior.4,28,35,36

The role of radiotherapy for MPT remains unclear from published reports because of small patient numbers5,37,38 and a lack of controlled data. Some authors17,39 have reported good results for local control. Pandey et al.17 suggested that adjuvant radiotherapy also improved the disease-free survival. August and Kearney40 recommended that adjuvant radiotherapy be considered for high-risk phyllodes tumors, including those >5 cm, with stromal overgrowth, with >10 mitoses/high-power field, or with infiltrating margins. Adjuvant radiotherapy was administered in only two women because of microscopic positive margins after mastectomy. LR occurred in both.

Many different chemotherapy regimens have been tried in MPT. Turalba et al.12 showed that doxorubicin- and ifosfamide-based chemotherapies have some efficacy in women with metastatic phyllodes tumors, but there is no established role for adjuvant chemotherapy in phyllodes tumors.19,24,28,32,34,37,41,42 In a study of 101 patients with PT, of whom 4 received adjuvant chemotherapy, the authors suggested that adjuvant chemotherapy should be considered in patients with stromal overgrowth.4 No other study has confirmed this finding.

The 5- and 10-year survival rates for MPT range from 54% to 82% and from 23% to 42%, respectively.4,17–19,33 Our patients had a 5-year survival rate of 75% and a 10-year survival rate of 57%; these compare favorably to other experiences. In our analysis, only stromal overgrowth had a significant effect on survival.

According to our findings, a 1-cm clear margin should be achieved in all patients with MPT to minimize the LR rate. If breast-conserving surgery can be accomplished without significant cosmetic deformity and with adequate margins, then this is a reasonable treatment for small MPTs. If the tumor is too large for this operation, a simple mastectomy should be performed. If stromal overgrowth is detected, then there is a significantly higher risk of LR, DM, and death from disease. Any protocol evaluating systemic therapy in MPT patients should focus on the treatment of patients with this high-risk finding.


   FOOTNOTES
 
Malignant phyllodes tumors more often recur locally when they are large (>5 cm) or inadequately excised (<1-cm margin). Stromal overgrowth significantly increases the risk of both tumor recurrence and patient death.

Received for publication February 4, 2004. Accepted for publication July 28, 2004.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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