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      Primary breast sarcoma: clinicopathologic series from the Mayo Clinic and review of the literature

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          Abstract

          Primary sarcomas of the breast are rare, malignant tumours arising from the mesenchymal tissue of the mammary gland (Oberman, 1965; Barnes and Pietruszka, 1977; Callery et al, 1985), with an approximate incidence of 17 new cases per million women (Moore and Kinne, 1996). At the Mayo Clinic, 27 881 malignant breast tumours were seen between 1940 and 1999 (C Adem, personal unpublished data) and 18 breast sarcomas were diagnosed accounting for 0.0006% of breast malignancies. Breast sarcomas should be distinguished from metaplastic carcinomas (Adem et al, 2002). When facing a spindle cell neoplasm in an epithelial organ such as the breast one should be careful in rendering the diagnosis of sarcoma. In this setting, immunohistochemistry using the right antibodies is of major input. Berg et al defined stromal sarcomas of the breast in 1962 as a group of mesenchymal malignant tumours with fibrous, myxoid and adipose components, excluding malignant cystosarcoma phyllodes, lymphomas and angiosarcomas (Berg et al, 1962). However, series in the literature have included many different entities under the rubric of sarcomas such as cystosarcoma phyllodes, lymphosarcoma and carcinosarcoma (Botham et al, 1958; Donegan, 1967; Fawcett, 1967; Kennedy and Biggart, 1967; Rissanen and Holsti, 1968; Gogas et al, 1976; Ludgate et al, 1977; Khanna et al, 1981; Christensen et al, 1988; Terrier et al, 1989; Pitts et al, 1991; Ciatto et al, 1992; Luna Vega et al, 1992; McGregor et al, 1994; Moore and Kinne, 1996; McGowan et al, 2000). For this review, we choose to categorise primary breast sarcomas in histogenic terms, similar to other soft-tissue sarcomas, thus including angiosarcomas, and excluding malignant cystosarcomas phyllodes, as reported by others (see Table 1 Table 1 Major breast sarcomas comparable series in the English literature Author N cases/period Median age (years) Median size (cm) Diagnosis Prognostic factors Barnes and Pietruszka (1977) 10/31 years 51 6.3 5F, 1RMS, 1Le, 2OGS, 1 Li Tumour contour, atypia, mitosis Barrow et al (1999) 59/43 years 45 UK 32F, 17A, 1OGS, 7 NOS Size, margins status, type Berg et al (1962) 25/UK 48 6.0 Li and F Positive margins Callery et al (1985) 25/33 years 54 4.0 9F, 5M, 1HPC, 2Le, 2D, 3Desmoid, 1Li, 2 SS UK Gutman et al (1994) 60/51 years 48 6.5 17A, 16SS, 10F, 6M, 3O, 2Li, 2Le, 1R, 3U Size, multifocal lesions, vascular, lymphatic, skin or chest wall invasion Johnstone et al (1993) 10/12 years 28 UK 4A, 2M, 1R, 1Li, 1SS, 1Sc UK Norris and Taylor (1968) 32/UK 49 4.0 5 OGS, 1 Le/R, 3 Li, 1D, 22F Size, contour, atypia, mitotic activity North et al (1998) 25/31 years 55 6.0 10A, 5SS, 3F, 2Li, 2Le, 1M, 1OGS, 1 U Type of surgery Oberman (1965) 13/30 y 56 7.1 7f, 3R, 2D, 1MM Size, type of surgery Pollard et al (1990) 25/81 years 55.4 5.9 11M, 6Li, 4F, 1CC, 1NS, 1Le, 1ASP Type of surgery Smola et al (1993) 8/23 years 56 12.8 2CHS, 1M, 2Li, 2F, 1A UK Stanley et al (1988) 4/UK 61 UK 2M, 2A UK Zelek et al (2003) 83/37 years 47 6.5 58M, 8A, 7L, 2Sc, 2R, 2OGS, 2Le, 2O Grade, size A = angiosarcoma; SS = stromal sarcoma; F = fibrosarcoma; M = malignant fibrous histiocytoma; Li = liposarcoma; D = dermatofibrosarcoma protuberans; Sc = spindle cell sarcoma; Cs = carcinosarcoma; Le = leiomyosarcoma; R = rhabdomyosarcoma; U = unspecified; CC = clear cell sarcoma; ASP = alveolar soft part sarcoma; MM = malignant mesenchymoma; OGS = osteosarcoma; Others = O. ) (Berg et al, 1962; Oberman, 1965; Norris and Taylor, 1968; Barnes and Pietruszka, 1977; Callery et al, 1985; Stanley et al, 1988; Pollard et al, 1990; Johnstone et al, 1993; Smola et al, 1993; Gutman et al, 1994; North et al, 1998; Barrow et al, 1999). MATERIALS AND METHODS All cases diagnosed pathologically at our institution from 1910 to 2000 as breast sarcomas and stromal sarcomas were retrieved from Mayo Clinic Surgical Pathology files. The H&E-stained sections were examined in all cases to confirm the diagnosis. An average of seven (range, 1–28) H&E slides per case were available. Clinical charts and surgical notes were retrospectively reviewed and the following information was collected: age, gender, size of tumour, clinical presentation, duration of symptom, history of radiation, type of surgery, local recurrences and systemic metastases. Follow-up information was obtained from patient records and death certificates. Patients with other prior primary malignancy in the breast, radiation therapy and metastatic disease to the breast were excluded. Patients with cystosarcoma phyllodes were excluded, as well as patients with metaplastic carcinoma. For this purpose, immunoperoxidase studies were performed using two primary antibodies, vimentin, to determine immunocompetence and wide spectrum screening keratin, to diagnose a metaplastic carcinoma as reported earlier (Adem et al, 2002). In regards of the fact that some cases were diagnosed at the beginning of the century, if immunoperoxidase study with vimentin was negative, another block representative of the tumour was chosen for further immunostaining. If vimentin staining was still negative, search for an internal control such as normal or carcinomatous component was done in each case. Size, diagnosis, infiltrative or nodular pattern, presence of heterologous elements, grade according to Broders' scheme of grading used at the Mayo Clinic, mitotic index (in 10 high-power fields, using a Leitz microscope, field diameter 0.45 mm), and necrosis were assessed. Overall survival (OS) and cause-specific survival (CSS) following diagnosis were estimated based on the Kaplan–Meier method, overall and separately for morphological features. Associations between morphologic features and survival were evaluated univariately based on fitting Cox proportional hazards models. All calculated P-values were two-sided and P-values less than 0.05 were considered statistically significant. RESULTS In all, 42 patients were retrieved between 1910 and 2000. Six were excluded after morphological review for the following reasons: cystosarcoma phyllodes (n=4), fibromatosis (n=1), benign haemangioma (n=1). Totally, 11 cases were also excluded after showing a positive stain with wide spectrum screening keratin, and being considered metaplastic carcinoma. Clinical data Overall, 25 remaining patients constituted the study group and are summarised in Table 2 Table 2 Patients clinical and pathological characteristics in our series   Age (years) Diagnosis Duration Surgery Adjuvant therapy Size Gross Margins Grade Local recurrence Metastases Last follow-up Case 1 38 MXFS 15 m R Mast N UK C N 2 3 y, S N DUK, 45 m Case 2 38 F UK R Mast RT 5 UK UK 2 N N DOC, 5.5 y Case 3 31 PS 2 m Excision N UK UK I 4 1 y, R Mast N DOC, 1 y Case 4 38 A UK Excision N UK UK I 2 5 times, 3 to 6 y, S/RT L, 6 y DOD, 84 m Case 5 72 PS UK R Mast N 3 I I 4 N N Alive, 18 y Case 6 49 F 1 m Mast UK 3 UK I 3 N N DOC, 37 y Case 7 43 A 1 m Mast N 8 C I 1 N B/L, 1 y, S/CT DOD, 16 m Case 8 48 MXFS 96 m Mast RT 5.5 I I 3 4 m, No TTT N AWD, 6 m Case 9 55 F 2 m Mast UK UK UK N 2 Twice, 11 m and 17 m, S N DOD, 76 m Case 10 67 Le UK Excision CT 2 UK UK 4 N Li/B/Skin, at presentation, CT DOD, 7 m Case 11 39 A 2 m Excision N 8 I I 2 20 m, S Li/Jejunum, 9 y, None DOD, 114 m Case 12 32 PS 2 m Excision N UK UK I 4 2 m, S N DOD, 23 m Case 13 52 F 4 m M R Mast N 4.5 C I 3 N N Alive, NED, 23.5 y Case 14 27 A 11 m S Mast N 12 I I 2 11 m, UK L/Li/S, 22 m, UK DOD, 32 m Case 15 63 MXFS 30 y S Mast N 4 C N 2 N N DOC, 21 y Case 16 60 PS 12 m R Mast RT 10 C N 4 N B/Lu, 6 y, RT DOD, 88 m Case 17 55 Le UK Mast N 4 UK N 4 N Multiple sites, 6 y, CT DOD, 77 m Case 18 33 A 12 m R Mast RT 10 C I 2 10 m, UK B, 10 m, RT DOD, 13 m Case 19 33 HPC UK UK UK UK UK N 4 N L/Li/Pelvis, UK, RT DOD, 41 m Case 20 24 PS 12 S Mast N 5 C I 3 N N Alive, NED, 11 y Case 21 32 A 11 m S Mast N UK UK I 3 14 m, RT B/L, 14 m, RT/CT DOD, 26 m Case 22 42 F UK S Mast N 3 UK I 3 8 m, S N DOC, 49 y Case 23 54 F 1 m M R Mast N 5 UK N 2 N N Alive, NED, 13 y Case 24 81 PS UK M R Mast N 0.3 UK I 4 N N Alive, NED, 14 m Case 25 54 OGS UK M R Mast N 10 C I 3 N N Alive, NED, 4 y Abbreviations: MXFS = myxofibrosarcoma; F = fibrosarcoma; PS = pleomorphic sarcoma; AGS = angiosarcoma; Le = leiomyosarcoma; HPC = hemangiopericytoma; OGS = osteosarcoma; UK = unknown; R = radical; Mast = mastectomy; S = simple; M = modified; RT = radiotherapy; CT = chemotherapy; C = circumscribed; I = infiltrative; y = year; m = month; DOC = dead of other causes; DUK = dead of unknown cause; NED = no evidence of disease; DOD = dead of disease; Lu = lung; B = bone; Li = liver; S = spleen; N = nodular or pushing margins; I = infiltrative. . There were 25 women age range 24–81 (mean 45 years). In total, 24 cases presented with lump, two of them associated with pain. In one case, it presented as an incidental mammographic finding. Contralateral breast sarcoma had been diagnosed elsewhere 3 years earlier in one case, renal cell carcinoma 5 years later in one case, colon cancer 4 years earlier in one case, skin melanoma and uterine cancer in one case 16 and 27 years earlier, respectively. No history of prior radiation was found in any case, therefore excluding postradiation sarcoma. The duration of symptoms for 16 patients ranged between 1 month to 40 years (mean 3.2 years). Surgical treatment was excision in five cases, mastectomy in 19 cases (modified, four; simple, five; radical, five; not specified, five), and unknown in one case. Adjuvant therapy was administered in five cases (radiation, four; chemotherapy, one). The right breast was affected in 10 cases, while the left was affected in 15 cases. Pathological data Gross description was available in 12 cases. Eight tumours were described as well-circumscribed, four as infiltrative of which two were angiosarcoma. Tumour size was available on 18 patients, and the mean tumour size was 5.7 cm (range 0.3–12.0). Angiosarcomas tended to be larger in size with a mean of 10 cm (range, 8–12 cm). After present review, histopathological diagnoses were fibrosarcoma (n=6), angiosarcoma (n=6), pleomorphic sarcoma (n=6), leiomyosarcoma (n=2), myxofibrosarcoma (n=3), hemangiopericytoma (n=1) and osteosarcoma (n=1). Tumours were graded as low grade (grade 1, one; grade 2, nine), and high grade (grade 3, seven; grade 4, eight). Necrosis was observed in four cases (three high-grade tumours). In all, 11 (range, 0–43) mitoses were found on average in 10 HPF. Heterologous component was seen in one case of osteosarcoma. Seven had pushing margins while 16 had infiltrative ones. An in situ ductal carcinoma component was observed in one case. In this case of pleomorphic sarcoma, keratin staining was negative in neoplastic cells with adequate internal control (the in situ component as well as benign entrapped ducts). There was no metastasis in the 15 cases where axillary node dissection was performed. Follow-up and survival analysis (Figure 1) Figure 1 Overall survival following surgery, according to tumour size (⩽5 vs >5 cm). The numbers in parentheses indicate the number of patients still at risk at selected time points. Overall mean and median follow-up were, respectively, 10.5 and 6.4 years (range, 7 months–41 years). Local recurrence was observed in 11 patients and ranged from 2 to 36 months (mean 15 months), while distant metastasis was observed in 10 patients, in order of frequency affecting the lungs (n=7), bones (n=6), liver (n=5), spleen (two) and skin (two). In one case, other sites were also kidney, pancreas, adrenal, omentum, epicardium and mediastinum. Of the 25 patients, 12 have died of disease and six of other causes. At the last follow-up, seven patients were still alive with a mean and median follow-up of 10.2 and 10.9 years, respectively. Five-year overall (OS) and cause-specific survival (CSS) were 66 and 70%, respectively. Five-year OS and CSS were both 91% for tumours ⩽5 cm, and 50% for tumours >5 cm. Tumour size was significantly associated with OS (risk ratio=1.3 per 1 cm increase; 95% CI, 1.02–1.7; P=0.036). There was no significant difference between low- and high-grade lesions (OS were 60 and 70%, P=0.14, CSS were 70 and 70%, P=0.5, respectively) or tumours showing infiltrative compared to pushing margins (OS were 65 and 71%, P=0.47, CSS were 65 and 86%, P=0.94, respectively) in terms of OS or CSS. Although there was no statistically significant association between tumour size and metastasis or recurrence, mean tumour size of patients with recurrence or metastasis was 7.7 cm, compared to 4.9 and 4.3 cm, respectively, for patients without recurrence or metastasis. Four out of five patients treated with simple excision had recurrence or metastasis. By the most common histopathologic types, all but one patient with angiosarcoma (4/5), one patient with fibrosarcoma, and two patients with pleomorphic sarcoma, died of disease. DISCUSSION Primary breast sarcomas are extremely rare (Moore and Kinne, 1996). In our institution, they compose 0.0006% of breast malignancies. They constitute a specific clinicopathologic entity and, therefore should be differentiated from the two main entities in differential diagnosis, cystosarcoma phyllodes and metaplastic carcinoma. Specific morphological features (biphasic tumour, with leaf-like architecture and epithelial component) recognise the former, and extensive sampling of the tumour can help when a stromal overgrowth is present. The latter is recognised on H&E sections by the presence of a carcinomatous component, or based on a cytokeratin immunopositivity of the neoplastic spindle cells. Reported series in the English literature had included all three entities as breast sarcomas, and include in their reports angiosarcomas, desmoid tumours, and lymphosarcomas (Botham et al, 1958; Berg et al, 1962; Oberman, 1965; Donegan, 1967; Fawcett, 1967; Kennedy and Biggart, 1967; Norris and Taylor, 1968; Rissanen and Holsti, 1968; Gogas et al, 1976; Barnes and Pietruszka, 1977; Ludgate et al, 1977; Khanna et al, 1981; Callery et al, 1985; Christensen et al, 1988; Stanley et al, 1988; Terrier et al, 1989; Pollard et al, 1990; Pitts et al, 1991; Ciatto et al, 1992; Luna Vega et al, 1992; Johnstone et al, 1993; Smola et al, 1993; Gutman et al, 1994; McGregor et al, 1994; Moore and Kinne, 1996; North et al, 1998; Barrow et al, 1999; McGowan et al, 2000). Therefore, reliable assessments of prognostic factors are difficult to make based on the published literature. Table 1 depicts comparable major series using soft-tissue tumours as basis for classification. Tumour size seems to be the most frequently reliable prognostic factor in many of these series, as in breast carcinomas and soft-tissue sarcomas (Oberman, 1965; Norris and Taylor, 1968; Gutman et al, 1994; Barrow et al, 1999; Zelek et al, 2003) Other reported prognostic factors are the histopathological diagnosis (Barrow et al, 1999), the infiltrative features (Norris and Taylor, 1968; Barnes and Pietruszka, 1977), the histopathologic grading (Norris and Taylor, 1968; Barnes and Pietruszka, 1977; Gutman et al, 1994; Barrow et al, 1999; Zelek et al, 2003), presence of positive margins (Berg et al, 1962; Barrow et al, 1999), and extent of surgery for local recurrence (Pollard et al, 1990; North et al, 1998). Some authors found age to be of prognostic importance (Ludgate et al, 1977). Margins status is a major risk factor for recurrence as it occurs in any neoplastic entity, and some authors advised adjuvant radiotherapy for cases with positive margins (Callery et al, 1985; Smola et al, 1993), or less than 2 cm of clear margins (McGowan et al, 2000). Treatment is generally based on a wide local excision, without axillary dissection (Barrow et al, 1999). Breast sarcomas bear different histogenesis than breast carcinomas as shown by cytogenetic studies (Garcia-Palazzo et al, 1992), and biological behaviour (Berg et al, 1962). We believe that breast sarcomas are comparable to soft-tissue sarcomas seen elsewhere. They present mainly as a lump and size is a prognostic marker with 5 cm serving as a valuable cut point. Tumour grade did not correlate with the outcome in our series but statistical power was limited and this finding could be related to the small size of the series. Lymphatic spread is uncommon as shown by the absence of axillary lymph node metastasis in our cases, and therefore axillary node dissection is not necessary. When lymph node metastasis is present, the diagnosis of a metaplastic carcinoma should be considered even in the presence of a pure spindle cell neoplasm.

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          Most cited references29

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          Prognostic factors in primary breast sarcomas: a series of patients with long-term follow-up.

          To describe the pathologic characteristics and prognostic factors of primary breast sarcomas (PBSs). We reviewed the clinical records and pathologic slides of 83 women with PBS treated in our institution between 1954 and 1991, with a median follow-up of 7.8 years. The majority of patients had undergone surgical treatment. The main histologic type was malignant fibrohistiocytoma (n = 57). For the whole population, the 10-year overall survival (OS) and disease-free survival (DFS) rates were 62% and 50%, respectively. For Fédération Nationale des Centres de Lutte Contre le Cancer grade 1, 2, and 3 tumors, the 10-year OS and DFS rates were 82% and 61%, 62% and 51%, and 36% and 25%, respectively (P =.00007 and.004, respectively). For tumors measuring less than 5 cm, 5 to 10 cm, and more than 10 cm, the 10-year OS and DFS rates were 76% and 66%, 68% and 55%, and 28% and 15%, respectively (P =.002 and.009, respectively). In the multivariate analysis, the tumor size and histologic grade were correlated with the 10-year DFS rate (P =.04 and.01, respectively), but only the histologic grade was correlated with OS (P =.01). Angiosarcoma was the only histologic type significantly associated with a poorer outcome in the multivariate analysis. PBSs have the same clinical history and prognostic factors as sarcomas arising at other sites. Therefore, it is legitimate to use a similar treatment strategy for PBS as for other sarcomas.
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            An analysis of 78 breast sarcoma patients without distant metastases at presentation.

            A retrospective review of a single cancer center experience was undertaken to identify clinical or treatment prognostic factors for these unusual tumors, to allow for a recommendation regarding management. The charts of 76 women and 2 men with breast sarcoma and without distant metastases at presentation registered from 1958 to 1990 were reviewed. Pathology was centrally reviewed in 54 cases. Histology, tumor size, grade, nodal status, age, menopausal status, history of benign breast disease, extent of surgery, resection margins, and radiation dose were each examined as potential prognostic factors by univariate analysis. To allow an analysis of radiation dose, total dose was normalized to a daily fraction size of 2 Gy. The median age at diagnosis was 50.5 years (13-82 years). The pathologic diagnosis was found to be malignant cystosarcoma phyllodes in 32 patients, with the remainder being stromal sarcoma (14), angiosarcoma (8), fibrosarcoma (7), carcinosarcoma (5), liposarcoma (4), other (8). Eighteen patients had grade I or II tumors, 43 had grade III or IV, and 18 were not evaluable. The 5- and 10-year actuarial rates for all 78 patients were 57% and 48% for cause-specific survival (CSS), and 47% and 42% for the relapse-free rates (RFR), respectively. The local relapse-free rate (LRFR) was 75% at both 5 and 10 years. The 5-year CSS for grade I or II tumors was 84% versus 55% for grade III or IV tumors (p = 0.01). Conservative surgery versus mastectomy did not lead to statistically significant different outcomes for CSS, RFR, or LRFR. The comparison of positive versus negative margins showed a 5-year LRFR of 33% versus 80% (p = 0.009). Pairwise comparisons of the 5-year CSS of 91% for > 48 Gy versus either 50% for < or = 48 Gy or 50% for no radiation showed p-values of 0.03 and 0.06, respectively. The authors propose that if negative surgical margins can be achieved, breast sarcoma should be managed by conservative surgery with postoperative irradiation to a microscopic tumoricidal dose (50 Gy) to the whole beast, and at least 60 Gy to the tumor bed. The decision to treat should be preceded by a preoperative multidisciplinary assessment. It is also recommended that an axillary lymph node dissection is not indicated, with the possible exception of patients with carcinosarcoma.
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              Role of radiotherapy in sarcoma of the breast--a retrospective review of the M.D. Anderson experience.

              The role of adjuvant radiotherapy for sarcoma of the breast, based on local extension of disease and patterns of failure, remains undefined because of the rarity of the disease presentation. Fifty-nine cases of soft tissue sarcoma of the breast were retrospectively reviewed. Cystosarcoma phylloides was excluded from analysis. Surgical intervention consisted of segmental resection (n = 16) or mastectomy (n = 38); five patients underwent excisional biopsy. Adjuvant radiotherapy was administered in four patients following segmental resection and in 13 patients after mastectomy. Doses totaled 50 Gy in the majority of patients, and conventional criteria and radiotherapy techniques for adjuvant breast irradiation were used. None of the dissected axillary nodes contained metastatic tumor on pathologic review. Patterns of failure were evaluated. Tumor size (P < 0.03) and surgical margins (P < 0.002) were predictive of local failure (LF). Due to limited patient numbers, no statistical significance was identified with any treatment modality. Following mastectomy alone, LF occurred in 13 patients (34%) versus the 13% rate of LF with mastectomy and radiotherapy (P = NS). Distant metastases developed concurrently with the two local failures in the group that underwent mastectomy and radiation. After segmental mastectomy, LF occurred in 3 cases (25%) concurrent with distant metastases: no LF were noted after segmental mastectomy and radiation (P = 0.27). For all treatment groups, local recurrences were characterized as multiple and involved the chest wall. Local failure occurred in 60% of patients with positive surgical margins who did not receive adjuvant irradiation. Irrespective of surgical margins, over 75% of local recurrences developed among patients treated by surgery alone. The role of radiotherapy for breast sarcoma remains undefined due to the rarity of this disease presentation. This retrospective review failed to demonstrate a statistical benefit for the administration of adjuvant irradiation in sarcoma of the breast, probably because of limited patient numbers. Because large tumor size and positive surgical margins incur a higher risk for LF, radiotherapy is probably indicated in these cases. Axillary dissection obligates the radiotherapist to treat the axilla in order to include all tissues in the surgical bed, and should be avoided to reduce potential treatment related morbidity. Established therapeutic principles and techniques used for both soft tissue sarcoma and breast cancer should continue to be applied.
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                Author and article information

                Journal
                Br J Cancer
                British Journal of Cancer
                Nature Publishing Group
                0007-0920
                1532-1827
                08 June 2004
                13 July 2004
                19 July 2004
                : 91
                : 2
                : 237-241
                Affiliations
                [1 ] 1Department of Anatomic Pathology, Pitie Salpetriere Hospital, Paris, France
                [2 ] 2Department of Laboratory Medicine and Pathology, Mayo Clinic, Rochester, USA
                [3 ] 3Division of Medical Oncology, Mayo Clinic, Rochester, USA
                Author notes
                [* ]Author for correspondence: camilo.adem@ 123456psl.ap-hop-paris.fr
                Article
                6601920
                10.1038/sj.bjc.6601920
                2409972
                15187996
                b178b6ee-bc50-4fb4-9366-e86859607115
                Copyright 2004, Cancer Research UK
                History
                : 28 November 2003
                : 18 March 2004
                : 23 April 2004
                Categories
                Clinical

                Oncology & Radiotherapy
                sarcoma,prognosis,review,tumour,breast,survival
                Oncology & Radiotherapy
                sarcoma, prognosis, review, tumour, breast, survival

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