Comparison of the clinical prognostic and features between the primary breast sarcomas and malignant phyllodes tumor
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1 Japanese Journal of Clinical Oncology Advance Access published November 11, 2014 Japanese Journal of Clinical Oncology, 2014, 1 7 doi: /jjco/hyu177 Original Article Original Article Comparison of the clinical prognostic and features between the primary breast sarcomas and malignant phyllodes tumor Fang Wang 1,2,3, Yan Jia 1,2,3, and Zhongsheng Tong 1,2,3, * 1 Department of Breast Oncology, Tianjin Medical University Cancer Institute and Hospital, National Clinical Research Center for Cancer, 2 Key Laboratory of Cancer Prevention and Therapy, Tianjin, and 3 Key Laboratory of Breast Cancer Prevention and Therapy, Tianjin Medical University Ministry of Education, Tianjin, China *For reprints and all correspondence: Zhongsheng Tong, Department of Breast Oncology, Tianjin Medical University Cancer Institute and Hospital, Huanhuxi Road, Hexi District, Tianjin , China. tonghang@medmail.com.cn Received 4 August 2014; Accepted 13 October 2014 Abstract Objective: Primary breast sarcoma is a kind of extremely rare disease. Malignant phyllodes tumor represents a specific subset of breast soft tissue tumors. So till now, the classification and clinical management of primary breast sarcoma and malignant phyllodes tumor are controversial. The aim of this study is to explore the differences in clinical features, treatment, disease-free survival and overall survival between primary breast sarcoma and malignant phyllodes tumor group. Methods: A retrospective review of 35 cases with primary breast sarcoma and 70 cases with malignant phyllodes tumor registered from 1995 to 2010 was carried out in Tianjin Medical University Cancer Institute and Hospital. Prognosis in terms of disease-free survival and overall survival was evaluated. Results: In primary breast sarcoma group, the result of univariate analysis demonstrated that surgical type, histopathological nodal status and local recurrence were significantly correlated with disease-free survival and overall survival. While, the result of monofactorial analysis showed the tumor size was significant prognostic indicator of disease-free survival and overall survival in malignant phyllodes tumor group. The Kaplan Meier curves for 5-year disease-free survival rates and overall survival rates demonstrated that no significant difference was found between the primary breast sarcoma and malignant phyllodes tumor group (P = and 0.772, respectively). Conclusions: The primary breast sarcoma patients had identical disease-free survival and overall survival compared with the malignant phyllodes tumor patients, which indicated that primary breast sarcoma and malignant phyllodes tumor patients should be treated with the same strategies. Surgical management is important for both the primary breast sarcoma and malignant phyllodes tumor patients. The role of the adjuvant radiotherapy and chemotherapy remains uncertain. Key words: primary breast sarcomas, malignant phyllodes tumor, prognosis, clinical strategy Introduction Primary breast sarcoma is a rare histological type of tumor arising from the mesenchymal tissue of breast, accounting for <1% of all primary breast malignancies and <5% of all sarcomas (1 4). Annual incidence has been estimated at 44.8 new cases per 10 million women, and this rate remained constant over the period (5,6). Phyllodes tumors which represent a specific subset of these breast soft tissue tumors are composed of a connective tissue stroma The Author Published by Oxford University Press. All rights reserved. For Permissions, please journals.permissions@oup.com 1
2 2 Comparison of the clinical prognostic and features and epithelial elements. In 1981, the World Health Organization applied the term phyllodes tumor and subclassified them histologically as benign, borderline, or malignant according to the features such as tumor margins, stromal overgrowth, tumor necrosis, cellular atypia and number of mitosis per high power field. The majority of phyllodes tumors have been described as benign (35 64%), with the remainder divided between the borderline (low-grade malignant) and malignant subtypes. To date, there is no consensus with regard of the exact Table 1. Comparison of clinical characteristics between PBS and MPT patients Characteristics PBS, n = 35 (%) MPT, n = 70 (%) P Age at diagnosis (71.4) 49 (70.0) >55 10 (28.6) 21 (30.0) Gender Female 34 (97.1) 70 (100.0) Male 1 (2.90) 0 (0.0) History of breast disease Yes 3 (8.6) 5 (7.1) No 32 (91.4) 65 (92.9) Family history of cancer Yes 2 (5.7) 1 (1.4) No 33 (94.2) 69 (98.6) Menopausal status Premenopausal 20 (58.8) 45 (64.3) Postmenopausal 14 (41.2) 25 (35.7) Laterality Right 19 (54.3) 35 (50.0) Left 16 (45.7) 35 (50.0) Tumor location Central 9 (25.7) 18 (25.7) Peripheral quadrant 26 (74.3) 52 (74.3) Tumor size <5 20 (57.1) 37 (52.9) (22.9) 24 (34.3) >10 4 (11.4) 7 (10.0) Unknown 3 (8.6) 2 (2.8) Type of surgery Radical mastectomy 23 (65.7) 25 (35.7) 0.038* Simple mastectomy 2 (5.7) 2 (2.9) Quadrantectomy 1 (2.9) 3 (4.3) Wide excision 3 (8.6) 14 (20.0) Local excision 6 (17.1) 26 (37.1) Axillary dissection Yes 26 (74.3) 24 (34.3) 0.000** No 9 (25.7) 46 (65.7) Lymph node status Negative 22 (62.9) 24 (34.3) 0.000** Positive 4 (11.4) 0 (0.0) Not applicable 9 (25.7) 46 (65.7) Adjuvant radiation Yes 2 (5.6) 0 (0.0) 0.043* No 33 (94.4) 70 (100.0) Adjuvant chemotherapy Yes 22 (62.9) 8 (11.4) 0.000** No 13 (37.1) 62 (88.6) Local recurrence Yes 3 (8.6) 9 (12.9) No 32 (91.4) 61 (87.1) PBS, primary breast sarcoma; MPT, malignant phyllodes tumor. *P < **P < definition of breast sarcoma. Some authors excluded cystosarcoma phyllodes from breast sarcoma due to its epithelial components (7 10), but others had an opposite opinion because of the similar survival and clinical features of breast sarcoma and cystosarcoma phyllodes (1,11 13). It appears to be difficult to draw a definitive conclusion in light of the limited size of study. Given that malignant phyllodes tumor consists of malignant mesenchymal cells and a benign epithelial component, and these lesions microscopically appear as epithelial lined cysts with a hypercellular stroma (14,15). We considered that primary breast sarcomas and malignant phyllodes tumor may be treated with the same strategies and rules. For the treatment of PBS and MPT, although simple mastectomy without axillary dissection was widely accepted as a gold standard, there are major variations in the extent of local excision, ranging from wide local excision to radical mastectomy. The effect of adjuvant radiation or chemotherapy on PBS and MPT is still unclear due to the rarity of these tumors (16,17). Even though some studies indicated an identical prognosis for malignant phyllodes and sarcomas (1,11 13), there is no sufficient data to support this. So in this study, we analyzed the clinical and prognostic characteristics of PBS and MPT, and to compare the survival data during the past 15 years. Figure 1. Kaplan Meier estimates for disease-free survival (DFS) and overall survival (OS) of primary breast sarcoma (PBS) and malignant phyllodes tumor (MPT) patients. There were no significant difference in DFS or OS among the two groups.
3 Jpn J Clin Oncol Patients and methods Patients with PBS and MPT were treated in the Cancer Institute and Hospital of Tianjin Medical University of China between 1995 and A total of 35 PBS cases and 70 MPT cases were enrolled in the study. Clinical characteristics, including the age at diagnosis, menopausal status, personal breast disease history, tumor character and treatment strategies (surgery, chemotherapy and/or radiotherapy) were retrospectively analyzed from the medical records. The follow-up information was acquired from the database, the medical records and contact with the patients or their families. Overall survival (OS) was defined as the time from the surgery until death by any cause. Disease-free survival (DFS) was calculated from the date of diagnosis to the date of the first sign of progression. DFS and OS were calculated using the Kaplan Meier method from the time of diagnosis. The log-rank test was used to evaluate survival difference between the groups. The statistical analysis was performed using GraphPad Prism software version 5.0. A P value of <0.05 was considered significant for both tests. Table 2. Univariate analyses of prognosis in PBS patients Characteristics N DFS OS 5-year % P 5-year % P Age at diagnosis > Menopausal status Premenopausal Postmenopausal Laterality Right Left Tumor location Central Peripheral quadrant Tumor size < > Type of surgery Mastectomy Breast conserving Axillary dissection Yes No Histopathological nodal status Negative Positive Adjuvant radiation Yes No Adjuvant chemotherapy Yes No Local recurrence Yes No Results Clinical and pathological data The median age at diagnosis was similar for the two groups: 49 years (range, years) for PBS patients and 49 years (range, years) for MPT patients. The median size of tumor was 5 cm (range, cm) for PBS patients and 5 cm (range, cm) for MPT patients. Twelve cases of carcinosarcoma (34.3%), 6 cases of liposarcoma (17.1%), 5 cases of stromal sarcoma (14.3%), 4 cases of angiosarcoma (11.4%), 4 cases of leomyosarcoma (11.4%), 2 cases of malignant fibrohistiocytoma (5.7%), 1 case of fibrosarcoma (2.9%) and 1 case of rhabdomyosarcoma (2.9%) were include in PBS. MPT was composed of 51 cases (72.9%) of borderline or low-grade malignant phyllodes tumors and and 19 cases (27.1%) of malignant phyllodes tumors. In 35 PBS cases, all cases (100%) underwent surgery, and 13 cases (37.1%) underwent surgery alone. Surgery was comprised of radical mastectomy for 23 cases (65.7%), local excision for 6 cases (17.1%), wide excision for 3 cases (8.6%), simple mastectomy for 2 cases (5.7%) and quadrantectomy for 1 case (2.9%). DFS, disease-free survival; OS, overall survival. *P < **P < Figure 2. Five-year DFS rates and 5-year overall survival (OS) according to surgery (mastectomy versus breast conserving) in primary breast sarcoma (PBS) patients.
4 4 Comparison of the clinical prognostic and features Axillary dissection was performed in 26 (74.3%) patients. Lymph nodal involvement was detected only in 4 cases (11.4%). Clear margins were obtained in the 34 cases (97.1%) of PBS patients after surgery. Twenty-two cases (62.9%) of PBS patients were performed with chemotherapy after initial surgery, 3 of 22 receiving palliative treatment subsequently. The patients received an association regiments of an anthracycline and ifosfamide including platinum or fluorouracil. The patients received the chemotherapy with a median number of 4 cycles (range, 1 6). At the end of first line treatment, the response was evaluated in 3 cases of recurrent patients: 1 case of patient achieved a partial response, 1 had a stable disease and 1 developed lung metastases. Adjuvant radiation was delivered in 2 cases (5.7%) of patients with a total dose of 50 Gy in 25 fractions. The clinicopathological characteristics of both PBS and MPT group are showen in Table 1. Significant differences were found in the type of surgery (P = 0.038), axillary dissection (P < 0.01), lymph node status (P < 0.01), adjuvant radiation (P = 0.043) and adjuvant chemotherapy (P < 0.01) between PBS and MPT patients. Survival analysis Comparison of survival data between PBS and MPT To evaluate whether PBS and MPT patients had a similar outcome, DFS and OS of the two groups were calculated. The Kaplan Meier curves (Figs 1A and B) for DFS and OS demonstrated that no significant difference was found in the PBS and MPT patients. The 5-year DFS and 5-year OS rates were 71.4 and 74.3% for PBS patients, 68.6 and 77.1% for MPT patients, respectively. Univariate analysis of the prognosis in PBS patients The prognostic factors on 5-year DFS and OS rates for PBS were presented in the Table 2. The univariate analysis revealed that the type of surgery, histopathological nodal status and local recurrence were significantly correlated with 5-year DFS and OS rates. Moreover, tumor size and axillary dissection were prognostic factors of PBS. The 5-year DFS and OS rates for patients treated by mastectomy were 83.3 and 45.5%, and rates for patients treated with breast conserving were 87.5 and 45.5%, respectively (P = and 0.003, Figs 2A and B). The 5-year DFS and OS rates for patients with negative nodal status were 81.8 and 25.0%, and rates for patients with positive nodal status were 86.4 and 25.0%, respectively (P =0.012 and 0.003, Figs 3A and B). For patients developing local recurrence or not, the 5-year DFS and OS rates were 0.00 and 78.1%, while 33.3 and 78.1%, respectively (P = and 0.028, Figs 4A and B). However, age, menopausal status, laterality, tumor location, adjuvant radiation and chemotherapy were not shown to be a significant predictor for survival in PBS patients. Figure 3. Five-year DFS rates and 5-year OS according to lymph node status (negative versus positive) in PBS patients. Figure 4. Five-year DFS rates and 5-year OS according to local recurrence (yes versus no) in PBS patients.
5 Jpn J Clin Oncol Table 3. Univariate analyses of prognosis in MPT patients Characteristics N DFS OS Univariate analysis of prognosis in MPT patients The prognostic factors on 5-year DFS and OS rates for MPT patients are given in Table 3. The univariate analysis demonstrated that tumor size was a prognositic indicator of 5-year DFS and OS rates. Age, laterality and local recurrence were related to survival of MPT patients. For the size of tumors <5 cm, 5 10 cm and >10 cm, the 5-year DFS and OS rates were 75.0 and 88.9%, 70.8 and 75.0%, and 37.5 and 37.5%, respectively (P = and 0.000, Figs 5A and B). Discussion 5-year % P 5-year % P Age at diagnosis > Menopausal status Premenopausal Postmenopausal Laterality Right Left Tumor location Central Peripheral quadrant Tumor size < > Type of surgery Mastectomy Breast conserving Axillary dissection Yes No Adjuvant chemotherapy Yes No Local recurrence Yes No *P < **P < Sarcoma of the breast is a very rare disease which represent <1% of breast cancers and <5% of all location sarcomas (4,18,19). Even the large and famous cancer institutions lack of the experience in dealing with these tumors and have troubles in putting forward a specific treatment for these patients. And, the prognosis was reported varying from 14% to >90% at 5 years by a few series (1,7 9,13,20 22). It is of major interest to identify the clinical characters and the prognosis factors for the PBS and MPT. Sarcoma of the breast is mainly present in women, male patients usually representing <5% (9,23). Mean age ranges from 47 to 52 years, and mean size of tumor ranges from cm (1,9,17). The size of tumor, and histological grade (7,9,21), the traditional prognostic factors of common soft tissues sarcomas, were found to impact the recurrence and survival of breast sarcomas. In our study, the size of tumor played an important role in the 5-year DFS rates for PBS patients (P < 0.05), while 5-year DFS and OS rates for MPT patients Figure 5. Five-year DFS rates and 5-year OS according to tumor size (measuring <5 cm, 5 10 cm and >10 cm) in MPT patients. (P < 0.01). The result differed from the other reports that the size of tumor was irrelevant with mortality (8,17). Adem et al. (9) found clinical tumor size was significantly correlated with decreased survival (RR = 1.3 per 1 cm increase). Zelek et al. (21) also showed that the size of tumor was associated with the 10-year DFS. The prognosis was particularly severe for the size of tumors >10 cm. There is widespread acceptance that surgical resection should be the first modality of treatment for breast sarcoma. There has been much discussion over the years regarding the surgical treatment with the best outcome for the patients (24,25). The purpose of surgery is excellent local control and for many years, mastectomy was regarded as the gold standard. In our study, DFS and OS were significantly increased after total mastectomy as compared with conservative surgery in PBS patients. In contrast, recent studies have demonstrated no significant advantage to mastectomy in comparison with wide local excision (1,7,13,20). This is similar to our observation on the treatment of MPT patients. Axillary dissection was not recommended in light of the rareness of lymph node involvement reported by most authors. In our study, lymph node involvement was observed in 4 out of 26 cases in PBS patients (15.4%) who had axillary dissection. In contrast to the surgical ablation, there is general disagreement for the benefits of radiotherapy. Some authors (8,17) did not find any advantage from the adjuvant radiotherapy due to few cases of patients
6 6 Comparison of the clinical prognostic and features receiving adjuvant radiation. But McGowan et al. (1) and Johnstone et al. (26) demonstrated adjuvant radiotherapy was a good choice for patients. Some studies indicated a trend of benefit for irradiated patients and so recommended adjuvant radiotherapy for primary breast sarcomas, especially if the tumor is of larger size or high grade (21). In our study, adjuvant radiotherapy delivering a dose of 50 Gy had no significant impact on either DFS or OS. This may be related to the fact that only 2 of 35 PBS (5.7%) patients and none of MPT (0.0%) patients were performed with adjuvant radiotherapy. A further point that needs to be addressed is whether adjuvant chemotherapy is capable of increasing long-term survival in breast sarcomas. Twenty-two of 35 PBS patients (62.9%) and 8 of 70 MPT patients (11.4%) with follow-up information received adjuvant chemotherapy. But there was no improvement in overall survival or disease-free survival with adjuvant chemotherapy, probably because it was given for patients with unfavorable tumor features. This was consistent with the previous results that most studies showed no benefits in terms of survival. In contrast to our study, increased diseasefree survival and improved overall survival for patients who received adjuvant chemotherapy were found by Gutman et al. (27). However, in most studies the response rates of breast sarcoma to chemotherapy, especially neoadjuvant chemotherapy, were limited (7,8,13,20). Adjuvant chemotherapy was provided for patients with high-grade tumors or with tumors measuring >5 cm (21). The choice of chemotherapeutic drugs to be used in the breast sarcomas must rely on the experience from soft-tissue sarcomas in other locations, given that data for the breast-specific location are limited (28). Classic sarcoma regimens containing doxorubicin, ifosfamide or combinations may be used in the initial treatment of breast sarcomas (29 31). In our study, we found no prognostic significance between the PBS and MPT patients, which is consistent with the generally held belief that histological subtype is of marginal prognostic significance for sarcomas elsewhere. The current opinion is that MPT and PBS excluding angiosarcomas, have the same prognosis and should be considered together (1,11 13,21). In our study, PBS including angiosarcomas made the same conclusion probably due to its retrospective analysis and small number of patients. Conclusion In conclusion, PBS patients had identical 5-year DFS and 5-year OS compared with MPT patients, which indicates that PBS and MPT patients may be considered together. However, the optimal therapeutic management of PBS and MPT is a crucial problem because of their rarity and also of the specific treatment strategy that must be followed. In our study, for PBS, the complete surgical resection of the sarcoma is vital to in improving survival disease-free survival and overall survival. The breast conservation therapy is provided in the selected patients according to favourable prognositic characters such as low histological grade and tumor size measuring <5 cm. An axillary dissection is not recommended unless the lymph nodes are apparent. Adjuvant radiotherapy alone or following conservative surgery may increase local control for large or high-grade tumors. Adjuvant chemotherapy is still a controversial issue. So, chemotherapy may be suggested to patients with the worst prognosis, although there is no definitive consensus. Funding This study was supported by the Tianjin Research Programme of Application Foundation & Advanced Technology (no. 14JCQNJC12400), the Higher Education of Science and Technology Development foundation Planning Projects of Tianjin (no ), the Starting Foundation for Doctors of Tianjin Medical University Cancer Institute and Hospital (No. B1209), and the Anticancer Key Technologies R & D Program of Tianjin (no. 12ZCDZSY16200). Conflict of interest statement None declared. References 1. McGowan TS, Cummings BJ, O Sullivan B, et al. An analysis of 78 breast sarcoma patients without distant metastases at presentation. Int J Radiat Oncol Biol Phys 2000;46: Szajewski M, Kruszewski WJ, Ciesielski M, et al. Primary osteosarcoma of the breast: a case report. Oncol Lett 2014;7: O Donnell ME, McCavert M, Carson J, et al. Non-epithelial malignancies and metastatic tumours of the breast. Ulster Med J 2009;78: Arora TK, Terracina KP, Soong J, et al. 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7 Jpn J Clin Oncol Johnstone PA, Pierce LJ, Merino MJ, et al. Primary soft tissue sarcomas of the breast: local-regional control with post-operative radiotherapy. Int J Radiat Oncol Biol Phys 1993;27: Gutman H, Pollock RE, Ross MI, et al. Sarcoma of the breast: implications for extent of therapy. The M. D. Anderson experience. Surgery 1994;116: Grimer R, Judson I, Peake D, et al. Guidelines for the management of soft tissue sarcomas. Sarcoma 2010;2010: Pervaiz N, Colterjohn N, Farrokhyar F, et al. A systematic meta-analysis of randomized controlled trials of adjuvant chemotherapy for localized resectable soft-tissue sarcoma. Cancer 2008;113: Eilber FC, Brennan MF, Eilber FR, et al. Chemotherapy is associated with improved survival in adult patients with primary extremity synovial sarcoma. Ann Surg 2007;246: Petrioli R, Coratti A, Correale P, et al. Adjuvant epirubicin with or without ifosfamide for adult soft-tissue sarcoma. Am J Clin Oncol 2002;25:
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