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Erschienen in: European Surgery 3/2022

Open Access 27.04.2022 | main topic

Malignant phyllodes tumor of the breast with axillary lymph node metastasis: case report and review of the literature

verfasst von: Hubert Hauser, Robert Hammer, Helmut Schöllnast, Ursula Humer-Fuchs, Doris Kriegl, Michael Fuchsjäger, Ferdinand Schmidt, Marija Balic, Sigurd F. Lax

Erschienen in: European Surgery | Ausgabe 3/2022

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Introduction

Phyllodes tumors are fibroepithelial tumors with characteristic histological features. The epithelial component is always benign with luminal and myoepithelial cells, and is surrounded by a cellular mesenchymal component. Phyllodes tumors typically show an exaggerated intracanalicular growth pattern, which results in leaf-like structures projecting into cysts [1]. Since not all phyllodes tumors are cystic, the original name “cystosarcoma phylloides” given by the first describer Johannes Müller (1838) was misleading and later changed by the WHO (1981) to “phyllodes tumor” [2, 3]. According to the current WHO classification, phyllodes tumors are classified as benign, borderline, or malignant based on stromal atypia, stromal cellularity, mitotic rate, stromal overgrowth, and tumor margins [4]. The mesenchymal component determines the biological behavior of the phyllodes tumor. At one end of the spectrum are benign phyllodes tumors with a stroma slightly more cellular than in fibroadenoma and lacking a significant degree of atypia and mitosis, on the other end there are malignant phyllodes tumors with highly atypical and polymorphic stroma with brisk mitotic activity and infiltrative growth into the adjacent tissues. Malignant phyllodes tumors often show an overgrowth by the malignant mesenchymal component, which may lead to a reduction of the epithelial component including the leaf-like pattern and the appearance of a spindle cell neoplasm.
The local recurrence rate of all phyllodes tumors is about 20% and the distant metastasis rate is about 3.5% [5]. However, malignant phyllodes tumors often behave aggressively, with a local recurrence rate of 40% and distant metastasis rate of up to 30% [68]. Due to their clinical manifestation, their radiological appearance, and the histology obtained from preoperative biopsy, a definitive preoperative diagnosis is often difficult or impossible [9].
Surgery with wide tumor-free resection margins or mastectomy is the treatment of choice for malignant phyllodes tumors [9, 10]. Axillary lymph node dissection is required if lymph nodes are palpable or suspect on imaging [2].
We report the rare case of a 59-year-old woman with an enlarged axillary lymph node and multiple lung metastases 4 months after radical surgery and adjuvant radiotherapy of a malignant phyllodes tumor. All performed procedures and investigations were in accordance with the ethical standards of the institutional research committee and with the 1964 Helsinki declaration and its later amendments. Informed consent was obtained.

Case report

A 59-year-old female presented with a palpable lump measuring approximately 3 cm and occasional pain in her left breast. Her medical history included removal of the left adnexa due to a teratoma 16 years ago. Family history included her mother’s death from pancreatic cancer, her father’s death from gastric cancer, and her brother’s death from bile duct cancer. An aunt had colon cancer and a cousin breast cancer.
Mammography showed an irregularly shaped high-density mass with microlobulated margins measuring 3.7 × 2.2 × 2.8 cm in the left upper outer quadrant, which appeared hypoechoic with microlobulated and partly indistinct margins, with dorsal shadowing only at its margins in ultrasonography (Fig. 1a–c). In the axillary gland extension, a suspicious lymph node with thickened cortex was seen (Fig. 1d), which was not palpable. Based on mammography and ultrasonography, the mass was classified as BIRADS V (highly suspicious for malignancy). MRI, which was performed after ultrasound-guided core cut biopsy of the mass for further preoperative assessment, showed malignant features such as rim-like mass enhancement, diffusion restriction, and perilesional edema (Fig. 2a–e). Skeletal scintigraphy as well as abdominal and thoracic CT were unremarkable. Core needle biopsy showed a highly malignant spindle cell tumor, which could not be further identified despite comprehensive immunohistochemical examination. Estrogen (ER) and progesterone (PR) receptors, as well as HER2 were negative. Ki-67 labelling index was 50%.
Surgery was performed 6 weeks after initial diagnosis. Preoperative ultrasound-guided wire marking of the suspicious lymph node was performed on the day of surgery (Fig. 3). For preparation of sentinel lymph node biopsy peritumoral application of technetium 99 was performed the day before the operation. Before the start of the operation, 2 ml patent blue was injected into the subareolar dermis. Wide resection of the tumor (Fig. 4) was performed to achieve a resection distance of at least 2 cm on all sides. Dorsally, due to the tumor location, a resection distance of only 1.3 cm was possible but with exact entrainment of the pectoralis fascia. No signal could be derived from the axillary region by means of gamma probe. The sonographically enlarged and preoperatively wire-marked lymph node was selectively removed. This lymph node additionally showed a blue coloration and, thus, corresponded to the sentinel node. No other lymph nodes were stained blue and no other enlarged lymph nodes were palpable. Intraoperative frozen section examination revealed a metastasis measuring 6 mm (Fig. 5a) within the sentinel lymph node, with infiltration of the perinodal tissue. Subsequently, a level I and II axillary dissection was performed.
Grossly, the lesion presented as a circumscribed, greyish-white, firm nodule, 3.5 cm in its largest diameter. Postoperative histology revealed a highly cellular, atypical spindle cell neoplasm with areas of necrosis and entrapped non-neoplastic glands (Fig. 5b). A leaf-like pattern or papillary fronds were not present. The tumor cells showed marked polymorphism, hyperchromasia of the nuclei, and frequent mitosis (Fig. 5c). Numerous areas of necrosis were present. At the periphery, the tumor cells infiltrated the surrounding adipose tissue. The tumor cells lacked immunoreactivity for cytokeratins (AE1/AE3) and p63, as well as for ER and PR. The surrounding breast tissue showed foci of atypical ductal epithelial hyperplasia (ADH) and flat epithelial atypia (FEA). The axillary resection specimen contained 10 additional tumor-free lymph nodes. Using the UICC TNM classification for soft tissue sarcomas (8th edition, 2017), the tumor was classified as pT1, G3, pN1 (1/11).
Adjuvant 3D conformal photon irradiation was performed with a single dose of 2 Gy to a total planned dose of 50 Gy. Additional saturation of the former tumor bed was performed with a daily single dose of 2 Gy to a total planned dose of 60 Gy as well as irradiation of the left suprafield with a daily single dose of 2 Gy to a total planned dose of 50 Gy.
Four months after surgery the patient developed dyspnea. The CT scan of the thorax showed multiple solid pulmonary nodules with a diameter of up to 2 cm in both lungs, which were histologically proven to be pulmonary metastases by CT-targeted biopsy (Fig. 6a–c). Subsequently, palliative doxorubicin chemotherapy (60–75 mg/m2) was started and after three cycles, CT showed stagnation of tumor growth. Since this is a recent case, no further follow-up information is available.

Discussion

Phyllodes tumors are fibroepithelial neoplasms with characteristic architectural features composed of an epithelial and a cellular stromal component. One hallmark of phyllodes tumors is a dominant intracanalicular growth pattern with stromal fronds capped by luminal and myoepithelial cell layers [1]. The presence of both components is crucial for diagnosis. The stromal component represents the neoplastic component and determines the biological behavior of the tumor [2, 11, 12]. In contrast, the epithelial component is benign and characterized by a bilayered epithelium covering either tubuli or leaf-like structures [1].
With a frequency of 0.3–0.9% of all breast tumors and 2.3% of all fibroepithelial breast tumors, phyllodes tumors are rare among tumors of the breast [1, 1317]. At the Breast Center Graz II, we diagnosed 16 phyllodes tumors (0.5%) among 3492 breast tumor patients during the period from 2012 to 2020. This corresponds to the frequency described in the literature. A slightly higher incidence is reported in Asian countries [1]. Malignant phyllodes tumors are even rarer [1315, 17]. In our patient collective, there was only one case of a malignant phyllodes tumor.
Phyllodes tumors can manifest at any age from adolescence onwards. In Western countries, they occur most frequently between 35 and 54 years of age [1820]. Compared with Western countries, a younger age of manifestation is reported in Asian countries [1]. The age of occurrence of malignant phyllodes tumors is the same as that of benign phyllodes tumors [21]. In our case, the patient’s age of 59 years was above the average age described in the literature, but correlated with individual cases described in the literature [4, 22].
Clinical examination usually reveals a palpable but painless, circumscribed tumorous induration [2, 23]. In contrast, our patient presented with pain. Malignant phyllodes tumors are usually much larger at the time of initial manifestation compared to benign phyllodes tumor, and are characterized by rapid growth [2].
One important differential diagnosis is fibroadenoma. Phyllodes tumors show neither specific mammographic features nor sonographic features that would allow a clear differentiation from fibroadenomas [2]. Thus, phyllodes tumors are frequently diagnosed preoperatively as fibroadenomas and operated on due to an increase in size. This is reported in the literature to be as high as 70% [24, 25]. Preoperative biopsy may also be inconclusive, since there are morphological overlaps between these two tumor entities (“fibroadenoma phyllodes”). The same applies to intraoperative frozen section diagnosis. Accordingly, the definitive histological diagnosis can often only be made postoperatively. In particular, the diagnosis of malignant phyllodes tumors may be difficult in core biopsies due to the stromal overgrowth. In the presence of a highly cellular and polymorphic spindle cell proliferation, metaplastic carcinoma of the breast should be excluded. Thus, a definitive preoperative diagnosis is often not possible, as in our case. Although exceedingly rare, a malignant phyllodes tumor is within the spectrum of the differential diagnosis of a rapidly growing breast lesion, particularly in women over the age of 35 years [2].
Due to the high local recurrence rate, surgical resection with a wide safety margin or mastectomy is the treatment of choice in the therapy of malignant phyllodes tumors. In the literature, tumor-free resection margins of at least 1 to 2 cm are recommended [2, 6, 21, 24, 26, 27]. In our case, a resection distance of more than 2 cm was achieved except for the dorsal margin with 1.3 cm, but with complete removal of the fascia pectoralis. In non-metastatic phyllodes tumors operated on with sufficiently wide resection margins, 5‑ and 10-year survival rates of 91% and 89%, respectively, have been reported [10].
Like other sarcomas, malignant phyllodes tumors metastasize mostly by hematogenous and very rarely by lymphatic spread. Therefore, axillary lymph node metastases are rare and routine axillary lymph node dissection is not recommended [2, 6, 2830]. However, if axillary lymph nodes are palpable, axillary dissection is also recommended. The data regarding the value of sentinel node biopsy in malignant phyllodes tumors are currently very limited and, therefore, a recommendation cannot be given [2]. A sentinel node biopsy may be considered for clinically suspicious tumors with diameters larger than 3 cm. In case of single imaging-enlarged or suspicious axillary lymph nodes, we recommend selective removal after preoperative marking. In case of tumor involvement, axillary dissection of levels I and II should be done as usual in breast surgery.
While the distant metastasis rate for the total group of phyllodes tumors is 3.5%, it is up to 30% for malignant phyllodes tumors, mainly by hematogenous spread [58]. In a meta-analysis, Tan et al. found a distant metastasis rate for benign phyllodes tumors of 0.1%, for borderline phyllodes tumors of 1.6%, and for malignant phyllodes tumors of 16.7% [31]. The lung is the most commonly affected site, accounting for 60% of the distant metastases, followed by bone with 28% and the brain with 9% [2, 32]. Large tumor size and the presence of heterologous elements seem to favor the occurrence of distant metastases and seem to be associated with poor outcome [33]. The high malignant potential of our case was underlined by the appearance of pulmonary metastases within the fourth postoperative month. In the presence of distant metastases, median survival rates of 5 months on average have been described [34, 35].
The local recurrence rate of all phyllodes tumors is about 20%, but 40% for malignant phyllodes tumors [58]. Staging examinations for malignant phyllodes tumors should be performed according to the staging guidelines for sarcomas [36]. This should include MR mammography, CT of abdomen and thorax, and skeletal scintigraphy.
Radiation and chemotherapy are recommended in cases with a high risk of metastasis, occurrence of tumor recurrence, or the presence or occurrence of metastases [9]. The value of radiotherapy for malignant phyllodes tumors is discussed controversially in the literature [2, 6]. In our case, due to the lymph node involvement, we decided to perform photon imaging of the breast and left suprafield. This might be helpful to prevent local recurrence but did not prevent the dramatic progression of the disease with early hematogenous metastasis. This is consistent with observations in the literature, where the use of radiotherapy has been shown to reduce local recurrence rates, but not to improve disease-free or overall survival [5, 37].
In case of metastasis, doxorubicin-based chemotherapy is the first-line option [2, 38]. Immediately after detection and histologic verification of multiple lung metastases, palliative doxorubicin was started in our patient. After three cycles, pulmonary CT showed stagnation of tumor growth.
In conclusion, the management of malignant phyllodes tumors remains a major challenge for radiologists, pathologists, surgeons, and oncologists even today, in particular, due to limited scientific evidence. Accordingly, treatment of this tumor entity should be performed only in breast centers by an experienced multidisciplinary team. It is essential to include such tumors in the differential diagnostic considerations during the diagnostic procedure. In order to optimize the currently unsatisfactory adjuvant therapy options, multicenter studies are necessary due to the rarity of the tumors.

Acknowledgements

The authors dedicate this article to Professor Hans-Jörg Mischinger on the occasion of his retirement from the chair of the Department of Surgery at the Medical University of Graz.

Conflict of interest

H. Hauser, R. Hammer, H. Schöllnast, U. Humer-Fuchs, D. Kriegl, M. Fuchsjäger, F. Schmidt, M. Balic, and S.F. Lax declare that they have no competing interests.
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Metadaten
Titel
Malignant phyllodes tumor of the breast with axillary lymph node metastasis: case report and review of the literature
verfasst von
Hubert Hauser
Robert Hammer
Helmut Schöllnast
Ursula Humer-Fuchs
Doris Kriegl
Michael Fuchsjäger
Ferdinand Schmidt
Marija Balic
Sigurd F. Lax
Publikationsdatum
27.04.2022
Verlag
Springer Vienna
Erschienen in
European Surgery / Ausgabe 3/2022
Print ISSN: 1682-8631
Elektronische ISSN: 1682-4016
DOI
https://doi.org/10.1007/s10353-022-00760-0