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. 2024 Jan 26;9(5):101448. doi: 10.1016/j.adro.2024.101448

Management of Concurrent Malignant Phyllodes Tumor and Invasive Breast Carcinoma

Jie Jane Chen a, Iowis Zhu a, Akshat Patel b, Gregor Krings c, Yunn-Yi Chen c, Florence Yuen a, Rita A Mukhtar d, Michelle Melisko e, Lisa Singer a, Catherine C Park a, Nicolas D Prionas a,⁎
PMCID: PMC10965428  PMID: 38550370

Introduction

Phyllodes tumors (PTs) are rare primary biphasic neoplasms of the breast that account for up to 1% of breast tumors.1 PTs can be classified as benign, borderline, or malignant. Malignant PTs, which comprise less than 25% of all cases, exhibit high-grade histologic features, including marked stromal atypia, hypercellularity, high mitotic activity, stromal overgrowth, and infiltrative borders.1,2 The concept of “giant PT” (>10 cm) is associated with an increased propensity for the development of local recurrence (LR) and distant metastases.3 Given the unpredictable clinical course of PTs, including rapid growth after an indolent period, some suggest considering all PTs as having malignant potential.4 The mainstay of treatment for malignant PT is surgical resection, often followed by adjuvant radiation therapy (RT) to decrease LR rates, especially for large PTs and for positive or close margins.5, 6, 7

Whereas PT originates from stromal tissue, breast carcinomas (BC) develop from the epithelial cells of terminal duct lobular units and represent the vast majority of breast tumors. Early stage invasive BC is typically treated with lumpectomy plus adjuvant RT or mastectomy, with systemic therapy tailored to tumor biology.8 Rarely, case reports have documented the coexistence of borderline or malignant PT and invasive BC within the same mass (Table 1).9, 10, 11, 12, 13, 14, 15, 16, 17, 18, 19, 20, 21, 22, 23, 24, 25, 26, 27, 28, 29, 30, 31, 32, 33 These tumors presented as a single mass and were managed surgically, with the diagnosis of malignancy in both stromal and epithelial components discovered after resection in most cases. There are no uniform guidelines for the management of concurrent PT with invasive carcinoma, with reports using surgery alone9,11,13,15,17, 18, 19, 20, 21, 22, 23, 24,28,31, 32, 33 or surgery followed by adjuvant RT,12,14,17,26,27,30,32 chemotherapy,10,14,25,26,29,32 and/or hormonal therapy.10,13,16,26,30,32

Table 1.

Summary of treatments and outcomes for concurrent borderline or malignant phyllodes tumors and breast carcinoma

Breast carcinoma Age Borderline/malignant phyllodes tumor Size of phyllodes tumor (cm) Treatment Sentinel lymph node biopsy performed ER/ PR/ HER2 status Follow-up Reference
DCIS, cribriform type 51 Borderline 14 Resection Unknown ?/?/? Unknown 9
IDC 26 Borderline 10 Mastectomy with adjuvant goserelin acetate, tamoxifen, 6 cycles of 5-fluorouracil, epirubicin, and cyclophosphamide Yes, 1/2 nodes positive +/+/– No recurrence at 15-month follow-up 10
IDC, DCIS 52 Borderline 15 Mastectomy Yes, 0 positive nodes –/–/? No recurrence at 38-month follow-up 11
Invasive tubular carcinoma, LCIS 53 Borderline 5.5 Resection with adjuvant RT Yes, 0/3 positive nodes +/+/? No recurrence at follow-up multiple years postoperatively 12
DCIS 45 Borderline 5 Mastectomy Yes ?/?/? No recurrence at average 3.6-year follow-up 13
IDC, DCIS, LCIS 46 Borderline 7 Mastectomy with adjuvant tamoxifen Yes +/+/- No recurrence at average 3.6-year follow-up 13
IDC 52 Borderline 2.5 Mastectomy with 6 cycles of adjuvant chemotherapy (paclitaxel, pirarubicin, and cyclophosphamide) and RT (50 Gy in 25 fractions) Yes, 1/3 sentinel lymph nodes (micrometastasis), 0/18 in remaining axillary nodes –/–/– No recurrence at 23-month follow-up 14
DCIS 54 Borderline 9 Mastectomy No +/?/– No recurrence at time of publication 15
ILC 40 Borderline 5.3 Lumpectomy followed by bilateral mastectomy with adjuvant tamoxifen Yes, 0 positive nodes +/+/– No recurrence at 6-month follow-up 16
IDC 45 Borderline 2.5 Wide local excision No +/+/– No recurrence at 22-month follow-up 17
LCIS, DCIS 69 Borderline 4.5 Wide local excision followed by re-excision No +/+/– Unknown 17
DCIS 42 Borderline 6.5 Mastectomy Yes, 0 positive nodes +/?/? No recurrence at 8-year follow-up 18
LCIS 48 Malignant 5 Wide excision No ?/?/? No recurrence at average 3.6-year follow-up 13
DCIS 52 Malignant 10 Mastectomy No ?/?/? No recurrence at time of publication 15
DCIS 48 Malignant 5 Mastectomy No ?/?/? No recurrence at time of publication 15
DCIS 45 Malignant 4 Mastectomy Yes, 0 positive nodes –/?/– No recurrence at time of publication 15
IDC 45 Malignant 12 Wide local excision followed by re-excision No +/+/– No recurrence at 10-month follow-up 17
IDC 63 Malignant 20 Mastectomy with adjuvant RT Yes, 0 positive nodes +/+/– No recurrence at 9-month follow-up 17
DCIS 27 Malignant 6 Subcutaneous total mastectomy No ?/?/? Recurrence of malignant phyllodes tumor in contralateral breast at unknown time 19
DCIS 47 Malignant 2 Resection Yes ?/?/? Unknown 20
DCIS 80 Malignant 10.5 Mastectomy No –/–/? Metastasis to lung and subcutaneous tissue at 2-month follow-up, deceased at 10-months 21
DCIS 39 Malignant 9 Resection Unknown ?/?/? Recurrence in contralateral breast at 3-month follow-up; negative for BRCA1/2 22
DCIS 45 Malignant 12 Mastectomy No ?/?/? No recurrence at 9-year follow-up 23
DCIS 75 Malignant 3.5 Mastectomy Yes, 0 positive nodes –/–/+ No recurrence at 26-month follow-up 24
IDC 54 Malignant 6 Neoadjuvant chemotherapy (4 cycles of cyclophosphamide/ doxorubicin/ 5-fluorouracil and 2 cycles of paclitaxel), followed by mastectomy Yes, 0 positive nodes –/–/– Metastasis to lung at 32-month follow-up, deceased 40 months postoperatively 25
DCIS 51 Malignant 21 Mastectomy with 4 cycles of adjuvant chemotherapy (doxorubicin/ cyclophosphamide), RT, and tamoxifen Yes, 2/12 positive nodes +/+/? No recurrence at 11-month follow-up 26
DCIS 43 Malignant 3.4 Wide local excision with adjuvant RT (50.4 Gy/ 28 fractions with boost to 63 Gy total) No +/?/– No recurrence at 1-year follow-up 27
IDC, DCIS 70 Malignant 6 Modified radical mastectomy Yes, 0 positive nodes –/–/– Unknown 28
Invasive cribriform carcinoma 62 Malignant 10 Mastectomy with adjuvant 5-FU, doxorubicin, and cyclophosphamide Yes, 0 positive nodes +/+/– No recurrence at 2-year follow-up 29
DCIS 30 Malignant 3.48 Lumpectomy followed by repeat lumpectomy, adjuvant RT, and tamoxifen No +/–/? No recurrence at 3-year follow-up 30
Neuroendocrine carcinoma 26 Malignant 10 Wide local excision No –/–/– Unknown 31
IDC 50 Malignant 11 Mastectomy with adjuvant chemoradiation therapy Yes, 0 positive nodes –/–/? No recurrence at 11-year follow-up 32
IDC 71 Malignant 5 Mastectomy with adjuvant hormonal therapy and RT Yes, 0 positive nodes +/+/– No recurrence at 39-month follow-up 32
DCIS 45 Malignant 6 Mastectomy 27 months after diagnosis Yes, 0 positive nodes +/+/? No recurrence at 1-year follow-up 32
Invasive carcinoma (no special type), DCIS 75 Malignant 4 Mastectomy with adjuvant anastrozole Yes, 0 positive nodes –/–/– Progression to inflammatory cancer at 3-months post-operatively, received palliative RT and exemestane; deceased at 56 months postoperatively 32
IDC 55 Malignant 6 Lumpectomy No –/–/– No recurrence at 1-year follow-up 33
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Abbreviations: ER, estrogen receptor; DCIS, ductal carcinoma in situ; HER2, human epidermal growth factor receptor 2; IDC, invasive ductal carcinoma; LCIS, lobular carcinoma in situ; PR, progesterone receptor; RT, radiation therapy.

To our knowledge, the management of concurrent PT and invasive BC in the context of previously diagnosed contralateral de novo metastatic BC has not been reported. In this case report, we discuss our experience treating one patient with left breast giant malignant PT with a focus of invasive ductal carcinoma (IDC) and a history of previously diagnosed metastatic right breast IDC. We additionally summarize the literature on dual presentation of breast carcinoma and borderline or malignant PT to help inform clinical decision-making for treatment considerations.

Case Presentation

The patient, a 48-year-old woman, presented to the emergency department with right hip pain and decreased mobility and was found to have a pathologic fracture of the right femur. CT scans of the chest, abdomen, and pelvis demonstrated bony metastatic disease, a right breast mass, and right axillary adenopathy. Her left breast contained a large fluid-filled structure thought to be a prosthesis versus a cyst (Figure 1A-B). Open biopsy of the right femoral neck, right hip hemiarthroplasty, and concurrent intraoperative right breast core needle biopsy showed ER-positive, PR-positive, and HER2-negative metastatic IDC with Ki-67 proliferation index of 10%. Fine needle aspiration (FNA) of the left breast cystic lesion showed atypical cells. However, there was insufficient material in the cell block for further characterization of the atypical cells. She received a diagnosis of de novo metastatic right breast IDC with solitary osseous metastasis to the right femur and bulky right axillary lymphadenopathy.

Figure 1.

Figure 1

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Illustration of malignant phyllodes tumor in this patient over time in relation to left palliative mastectomy and adjuvant radiation therapy to the left chest wall at the following time points: (A) 2 years and 4 months before palliative mastectomy. (B) 2 years and 2 months before palliative mastectomy. (C) 1 year and 4 months before palliative mastectomy. (D) 7 months before palliative mastectomy. (E) 4 months before palliative mastectomy. (F) 2 months before palliative mastectomy. (G) 1 month before palliative mastectomy. (H) 2 days before palliative mastectomy. (I) 2 weeks after palliative mastectomy. (J) During radiation therapy to the left chest wall. (K) 1 year and 4 months after radiation therapy to the left chest wall.

One month after right hip hemiarthroplasty, she started fulvestrant and goserelin, which she received in total for 2 years and 4 months. A month later, she received palliative consolidative RT to the right femur to a dose of 20 Gy in 5 fractions using 3D conformal technique, treated concurrently with her right intact breast, which received 26 Gy in 5 fractions using opposed tangential technique with 6 MV photons. She did not receive regional nodal irradiation. By 4 months after hormonal therapy initiation, she experienced decreases in the size of the right breast mass and right axillary lymphadenopathy.

However, her left breast gradually increased in size (Figure 1C) while on fulvestrant and goserelin, and her case was presented at multidisciplinary tumor board to discuss management of the contralateral left breast cystic lesion. Initially, no surgical intervention was recommended given the lack of related symptoms and concurrent diagnosis of metastatic IDC of the right breast. The patient was recommended palliative RT to the left breast if it became symptomatic, which she deferred.

Approximately 1 year later, the patient presented with accelerated growth of the left breast lesion (Figure 1D-F). Ultrasonography showed a complex cystic and solid mass replacing the entire left breast (Breast Imaging Reporting and Data System 5, more commonly referred to as BI-RADS 5). The patient was evaluated in the breast surgical oncology clinic where mastectomy was recommended given the large size and rapid enlargement. The patient declined mastectomy but underwent aspiration of the cystic component which yielded 450 mL of hemorrhagic fluid, from which cytology showed only inflammatory cells. The solid component of the mass was not amenable to core needle biopsy. About 9 months later, she was seen in radiation oncology clinic and experienced spontaneous skin rupture with high pressure pulsatile bleeding at the inferolateral breast, with pressure applied and silver nitrate used to stop the bleeding (Figure 1G). She was recommended palliative mastectomy but again declined. Several days later, she experienced another spontaneous skin rupture with high pressure bleeding that led to hospitalization and the need for blood transfusion. Three days after discharge, she presented to the ED with left breast hemorrhage (Figure 1H). The patient underwent palliative mastectomy of the left breast, inclusive of a 24 cm mass. Figure 1A-I demonstrates growth of the left breast mass over 2 years and 4 months before left palliative mastectomy. Pathology revealed a malignant spindle cell neoplasm with necrosis and skin ulceration, most consistent with malignant PT (Figure 2A-C). Targeted DNA sequencing of the tumor revealed hotspot MED12 (p.G44C), TERT promoter (c.-124C>T), and FGFR1 (p.K656E) mutations, as well as inactivating BCOR (p.C1363fs) and SETD2 (p.K528*) mutations, confirming the diagnosis of malignant PT. There was also a focus of IDC within the malignant PT that was ER-negative, PR-negative, HER2-negative, and androgen receptor positive (Figure 2D-F), suggestive of a different origin than the previous IDC of the right breast and not a metastatic lesion. The margins were negative, and she was discharged 1 week after surgery.

Figure 2.

Figure 2

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Pathology of the tumor in the left palliative mastectomy specimen. (A) Low power view showed a circumscribed cellular spindle cell neoplasm. (B) On higher magnification, the tumor was primarily composed of diffuse sheets of spindled cells with moderate to focally marked nuclear pleomorphism and high mitotic activity. (C) The neoplastic spindle cells were positive for CD34 and negative for multiple cytokeratin markers, including keratin cocktail of AE1/3 and CAM5.2 as shown in the inset. The morphologic features and immunophenotype along with the presence of hotspot MED12 (p.G44C) and TERT promoter (c.-124C>T) mutations as revealed by the next generation sequencing UCSF500 assay supported the diagnosis of malignant phyllodes tumor. (D) Focally within the tumor was a relatively scant population of epithelial cells arranged as small clusters in an infiltrative growth pattern (highlighted by the yellow line) and spanning over 1.7 cm. (E) The epithelial cells were positive for keratin cocktail AE1/3 and CAM5.2, positive for GATA3 (not shown), and negative for myoepithelial markers p63 and SMM (not shown), supporting the diagnosis of a concurrent invasive ductal carcinoma within the malignant phyllodes tumor. (F) The concurrent invasive ductal carcinoma was negative for ER, PR, and HER2 (not shown), and positive for androgen receptor.

Because of a concern for dermal invasion, along with the large tumor size, she was recommended RT to the left chest wall to a dose of 40.05 Gy in 15 fractions using a tangential technique, which she tolerated well (Figure 1J). The decision was made to pursue adjuvant RT to control an aggressive malignant PT to reduce the risk of morbidity from local progression, given the distant disease from right breast IDC was stable at that time. Two months after completion of RT to the left chest wall, she was lost to follow up for 10 months and did not continue fulvestrant or goserelin. When she reengaged with care at 12 months after left chest wall RT completion, she presented to the ED for a kidney stone and worsening back pain. CT followed by PET/CT scans revealed extensive bone metastases and right pleural nodularity. In multidisciplinary discussion, the metastases were thought to be due to right breast IDC given previously known metastatic right breast cancer to the bone, detection of the metastases after stopping hormonal therapy, and no signs of left chest wall recurrence. Figure 1K depicts the left chest wall at 16 months after RT.

Discussion

Concurrent presentation of malignant PT and BC is rare, with data limited to case reports (Table 1). Accurate diagnosis in these co-presentations is challenging, especially as PTs possess overlapping clinical, radiologic, and histologic characteristics with both benign fibroadenomas and malignant soft tissue sarcomas. With regards to sampling techniques, FNA is associated with low diagnostic yield and high false-negative rates, with FNA accuracy estimates ranging from 32% to 63%.34 Intraoperative diagnosis of PT using frozen section also has limited accuracy of approximately 42%.35 Oftentimes, local excision of the breast mass is needed to establish a diagnosis of PT, and further surgery may be indicated to ensure adequate tumor-free margins.

Understanding the biologic mechanisms behind concurrent malignant PT and IDC development may guide therapies for dual presentation. There are no known genetic predispositions to dual presentation of PT and IDC. Genetic analysis reveals that in contrast to IDCs, the polyclonal epithelial component of PTs is nonneoplastic whereas the monoclonal stromal component is susceptible to malignant transformation.36,37 Some benign tumors may transform into higher grade PT at recurrence.35,38, 39, 40 On the other hand, the epithelial component of PT may be primarily or secondarily involved by ductal carcinoma in situ (DCIS).9,11,13,15,17, 18, 19, 20, 21, 22, 23, 24,26, 27, 28,30,32 Some have hypothesized that growth factors from the PT stroma may increase the risk of metaplasia or neoplasia of the ductal epithelium.9 IDC may arise from DCIS involving the epithelial component of the PT, or IDC may secondarily involve PT from adjacent breast tissue.

Management recommendations vary for synchronous PT and invasive carcinoma. One report recommends the addition of sentinel lymph node biopsy and adjuvant chemoradiation due to the IDC component,41 and another suggests that management should not change with upfront surgical resection for all tumors given the radioresistant and chemo-resistant nature of PT.42 The current literature on dual presentations of borderline or malignant PT and BC has mixed treatment decisions, with 5 reports using adjuvant chemotherapy and 7 reports using adjuvant RT (Table 2). Although the data are sparse, among the 36 patients summarized in Table 1, there were no recurrences among ten patients who received adjuvant chemotherapy or RT, whereas 5 of 26 patients (19.2%) who did not receive adjuvant chemotherapy or RT experienced recurrences (P = .29). This finding, although not statistically significant, is clinically relevant and warrants further investigation among larger cohorts of patients with borderline or malignant PT. On the other hand, contralateral malignant PT was found in 2 patients who received mastectomy alone. Lung metastases were found among one patient who received neoadjuvant chemotherapy followed by mastectomy and another patient who received mastectomy alone. One patient later developed inflammatory BC.

Table 2.

Comparison of characteristics and outcomes of borderline and malignant phyllodes tumors (N = 36)

Borderline phyllodes tumor (n = 12) Malignant phyllodes tumor (n = 24) Fisher's exact test
Variable N (%) N (%) P value
Age (years) Median: 48.5 (Range, 26-69) Median: 49 (Range, 26-80) -
Concurrent primary tumor 0.17
 IDC or DCIS 11 (92%) 20 (83%)
 ILC 1 (8%) 0 (0%)
 Other 0 (0%) 4 (17%)
Size of phyllodes tumor (cm) Median: 6 (Range, 2.5-15) Median: 6 (Range, 2-21) -
Estrogen receptor status 0.19
 ER + 8 (67%) 8 (33%)
 ER – 2 (17%) 9 (38%)
 Unknown 2 (17%) 7 (29%)
Extent of surgical resection 1.00
 Mastectomy 8 (67%) 16 (67%)
 Lumpectomy or wide local excision 4 (33%) 8 (33%)
Received adjuvant treatment* 5 (42%) 8 (33%) 0.72
 RT 2/5 (40%) 5/8 (63%)
 Chemotherapy 2/5 (40%) 3/8 (38%)
 Hormonal therapy 3/5 (60%) 4/8 (50%)
Received SLNB 0.36
 Yes 8 (67%) 12 (50%)
 No 3 (25%) 11 (46%)
 Unknown 1 (8%) 1 (4%)
Node positive on SLNB 2/8 (25%) 1/12 (8%) 0.54
Any recurrence 0.29
 Yes 0 (0%) 5 (21%)
 No 10 (83%) 16 (67%)
 Unknown 2 (17%) 3 (13%)
Recurrence after receiving adjuvant chemotherapy or RT 1.00
 Yes 0/5 (0%) 0/8 (0%)
 No 5/5 (100%) 8/8 (100%)
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⁎

Some patients received a combination of adjuvant radiation therapy, chemotherapy, and hormonal therapy.

Abbreviations: DCIS, ductal carcinoma in situ; ER, estrogen receptor; IDC, invasive ductal carcinoma; RT, radiation therapy; SLNB, sentinel lymph node biopsy.

Prior studies have suggested that hormone therapy has limited effectiveness in treating PTs, as hormone receptors are primarily expressed on the nonneoplastic epithelial component of the tumors.43 A prior case series showed that hormone therapy was ineffective even in patients with hormone receptor-positive PT.44 Similarly, we found that over 2 years of hormonal therapy that was administered for this patient's contralateral hormone receptor-positive IDC was ineffective in controlling the growth of her concurrent malignant PT. Given the relative aggressiveness of malignant PT compared with IDC, with recurrence rates of malignant PTs ranging from 20% to 65%,45,46 we recommend multidisciplinary discussion of adjuvant treatment decisions directed at control of malignant PT.

Surgical resection with margins >1 cm is the primary treatment for malignant PT. In one study of 478 patients with malignant PT treated with surgery, LR rates were 15% or higher for patients with tumors >2 cm treated by lumpectomy alone and tumors >10 cm treated by mastectomy alone, with recommendations for considering adjuvant RT based on tumor size and extent of resection.5 The literature supports axillary lymph node staging only in cases where clinically pathologic nodes are found on examination, given only approximately 5% of patients have axillary metastases at lymph node dissection.47 However, in the setting of known concurrent IDC, axillary sampling should be pursued as standard workup, in accordance with clinical risk of regional metastasis. In this case, axillary sampling was not performed during the left mastectomy given the diagnosis of metastatic disease arising from the contralateral breast, combined with clinically negative left axilla and lack of preoperative pathologic diagnosis. However, potential change in systemic management should be considered based on axillary sampling results.

High stromal overgrowth or the presence of more than 10 mitoses per high power field are associated with LR and may be indicators for consideration of adjuvant RT.48 Adjuvant RT following lumpectomy may reduce LR, though most studies show no impact on overall survival.7,49 A large Surveillance, Epidemiology, and End Results analysis found the combination of mastectomy and adjuvant RT was associated with poor prognosis.50 However, this is likely related to inclusion of patients with larger, more advanced tumors or with closer margins in treatment with both modalities. A prospective nonrandomized multi-institutional trial investigating the role of adjuvant RT after breast-conserving surgery with negative margins for borderline or malignant PT found a 0% LR rate at a median follow up of 56 months.6 Although adjuvant RT is not typically indicated for malignant PT or IDC following mastectomy, as in the case presented, the decision toward postmastectomy irradiation must consider other risks for LR including large tumor size and dermal invasion or ulceration. Adjuvant chemotherapy or RT may benefit selected patients with concurrent malignant PT and IDC with these higher risk features, reducing the risk of morbidity from local progression.

Conclusions

To our knowledge, this is the first report of concurrent malignant PT and IDC presenting in the context of metastatic IDC from the contralateral breast. The biologic mechanisms for the development of malignant PT and IDC are distinct, and management must be appropriately tailored for both, including axillary nodal sampling for IDC and adjuvant treatment for malignant PT with adverse pathologic features, which may provide a period of local control for a disease with a high propensity for recurrence. Our experience suggests that neoadjuvant hormonal therapy is not helpful for concurrent malignant PT and IDC. To reduce the risk of morbidity from local progression, adjuvant therapy including RT or chemotherapy following mastectomy may be beneficial for select high-risk patients with dual presentation of malignant PT and IDC with large tumor size and dermal invasion.

Disclosures

None.

Footnotes

Sources of support: This work had no specific funding.

Data sharing statement: Research data are stored in an institutional repository and will be shared upon request to the corresponding author.

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