Encapsulated papillary carcinoma of the breast: A single institution experience
- Authors:
- Published online on: September 7, 2023 https://doi.org/10.3892/ol.2023.14046
- Article Number: 459
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Copyright: © Xu et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
Abstract
Introduction
Encapsulated papillary carcinoma (EPC) of the breast, which is observed in only 0.5–1% of all malignant cases worldwide (1), is regarded as a transition between ductal carcinoma in situ (DCIS) and invasive carcinoma (2). According to the histological features, EPC can be divided into three subtypes: Pure EPC, EPC associated with DCIS and EPC associated with invasive carcinoma (3).
Microscopically, similar to other types of papillary intraductal carcinoma, EPCs arise in a cystically dilated duct and lack myoepithelial cells (MECs), both in the fibrovascular cores and at the periphery (4). The absence of MECs and reported cases of metastatic tumors indicate that these tumors represent low-grade invasive carcinomas with an expansile growth pattern (5). However, the presence of continuous and intense collagen IV expression at the periphery is considered highly suggestive of a non-invasive carcinoma that is confined within an intact basement membrane (6). EPC without an adjacent DCIS or any invasive component has a very favorable prognosis with adequate local therapy; however, the presence of associated DCIS or invasive components confers a higher risk of local recurrence (7).
Notably, the outcomes of EPC cases associated with invasive carcinoma remain unclear. Several retrospective clinicopathological studies have demonstrated that EPC has a favorable prognosis with suitable local therapy alone, regardless of whether they are in situ or not (8,9). However, evidence from other studies has indicated that EPC associated with invasive carcinoma behaves aggressively, and these tumors should be staged and treated as invasive breast cancer, especially in cases with an invasive component outside the tumor capsule (7,10). To the best of our knowledge, no clearly defined guidelines on treatments for EPC have been established thus far, due to its low incidence rate.
To better understand the pathology of EPC of the breast and to investigate the therapeutic role of treatment modalities, including surgery, chemotherapy, radiotherapy and hormonal therapy, the present study aimed to compare the clinicopathological features and survival of patients with non-invasive EPC and invasive EPC admitted to The Third Hospital of Nanchang City (Nanchang, China), and to provide preliminary guidelines for standard treatment recommendations of this rare clinical entity.
Materials and methods
Patient cohort
From the institutional database, all patients that were diagnosed with EPC and admitted to the Prevention and Cure Center of Breast Disease, The Third Hospital of Nanchang City between January 2015 and December 2021 were included in this retrospective clinicopathological study. All microscopy slides of these cases were confirmed as EPC by two pathologists independently. Cases with/without an adjacent DCIS or any invasive components were included. Data such as age, sex, menopausal status, primary complaint and treatments were also collected.
Pathological examination
All available hematoxylin and eosin (H&E)-stained EPC slides were reviewed by two independent pathologists. Tumor morphologies, including nuclear grade, mitotic rate, and presence and extent of associated in situ and invasive carcinoma were assessed using recently described criteria (11). Immunohistochemical analyses were performed on 4-µm paraffin-embedded tissue slides, which were initially fixed with 10% formalin at room temperature for 6 h, as previously described (12). First, the slides were incubated at 65°C for 2 h and then deparaffinized twice, 5 min each time. Antigen retrieval was performed in antigen retrieval solution (10 mmol/l Tris; 1 mmol/l EDTA; pH 9.0) at 100°C for 5 min and 2% sheep serum (Beyotime Institute of Biotechnology) was added for blocking at room temperature for 30 min. The slides were then incubated with primary antibody at 4°C overnight, and with the horseradish peroxidase-labeled secondary antibody and DAB for 1 h at 37°C. Tumor immunoreactivity was evaluated by two pathologists independently. Moreover, immunohistochemistry (IHC), as well as fluorescence in situ hybridization (FISH), was used to determine the status of human epidermal growth factor receptor-2 (HER2) according to the updated 2018 American Society of Clinical Oncology-College of American Pathologists recommendations for HER2 testing in breast cancer (13). FISH analyses were performed as previously reported (14).
Follow-up
All patients were followed-up in the Prevention and Cure Center of Breast Disease, The Third Hospital of Nanchang City. During the follow-up period, routine physical and radiological examinations were performed to monitor recurrence. All of the patients were followed up by telephone communication and the date of the last follow-up was October 1, 2022. In total, in the present study, 46 patients with EPC were included; one of which was diagnosed with bilateral primary EPC. Follow-up information was available from 42 patients.
Statistical analysis
Data were analyzed using SPSS version 21.0 (IBM Corp.). All continuous data, such as tumor size and age were compared using unpaired Student's two-sided t-test. In addition, a Pearson's χ2 test or Fisher's exact test was used to evaluate the categorical variables, including clinicopathological features, such as sex, axillary nodal invasion and hormone receptor (HR) status. P<0.05 was considered to indicate a statistically significant difference.
Results
Clinical and pathological findings
Descriptive characteristics and clinical findings of the patients included in the present study are listed in Table I. Between January 2015 and December 2021, 46 patients with EPC were admitted to the Third Hospital of Nanchang City. Consistent with previous studies (15,16), the majority of patients with EPC were female, with only one 70-year-old male patient diagnosed in 2017 in the present case series. The age of onset ranged from 41–88 years, with a median age of 62.1 years. As shown in Table I, a total of 22 cases (46.8%) were pure EPC, 6 cases (12.8%) were EPC associated with DCIS and 19 cases (40.4%) were EPC associated with invasive carcinoma.
In the present study, the most common clinical manifestation of EPC was a painless and palpable lump in the breast (82.9%). Nipple discharge was present in 5 cases (10.8%). Of the cases, 24 tumors (52.2%) were located in the left breast and 21 tumors (45.7%) were located in the right breast. Notably, one 61-year-old woman (2.2%) presented with synchronous bilateral EPC tumors. Upon palpation, the tumor size ranged from 0.8–6.1 cm (median, 2.5 cm). Ultrasonography revealed that most of the EPC lesions presented with a solid or mixed cystic nodule, which displayed a heterogeneous echo structure and the border was often obscured or irregular in shape. In 7 cases (14.9%), ipsilateral axillary node enlargement with no abnormal blood flow signal was also observed. Screening mammograms also depicted a well-circumscribed, round-to-oval and lobulated mass in 31 cases (66.0%). Clustered microcalcifications were also found in 6 cases (12.8%).
Histopathological examination of EPC showed a well-defined lesion of papillary carcinoma within a dilated duct comprised of fibrovascular cores covered by single or multiple layers of neoplastic cells, surrounded by a fibrous capsule. The surrounding fibrous capsule was thick and may have been accompanied by inflammatory cell infiltration (Fig. 1). According to the Nottingham Grading System in primary breast cancer, 5 EPC cases were high nuclear grade (10.6%), and they were all EPC associated with invasive carcinoma. Subsequent immunohistochemical analyses demonstrated that the EPC cases were primarily estrogen receptor (ER)- and progesterone receptor (PR)-positive (ER, 91.5%; PR, 80.9%). Notably, all 4 ER-negative cases were diagnosed with EPC associated with invasive carcinoma. As for the 9 PR-negative cases, 2 were pure EPC, 2 were EPC associated with DCIS and 5 were EPC associated with invasive carcinoma. According to the American Society of Clinical Oncology-College of American Pathologists Guideline for HER2 testing in breast cancer (17), cancer with HER2 overexpression refers to those patients who are HER2 IHC (3+), or HER2 IHC (2+) and FISH (+). Therefore, the majority of lesions were HER2-negative breast cancer (97.9%) in the present study, except for only one HER2 (2+) patient who had invasive EPC and was positive in the subsequent FISH analysis (Table II). Myoepithelial markers, such as p63, α smooth muscle antigen (α-SMA) and cytokeratin (CK)5/6, were negative in the majority of lesions (p63, 85.1% negative; α-SMA, 76.6% negative; CK5/6, 87.2% negative), which indicated that myoepithelial cells were often absent both in the fibrovascular cores and at the periphery of the tumor nodules of EPC (Fig. 2). A summary of the immunohistochemical analysis of the cohort is shown in Table II.
Diagnosis, treatments and survival
To establish a diagnosis, an ultrasound-guided core needle biopsy was performed in 26 cases prior to surgery. Of the 26 cases, 6 cases were diagnosed as pure EPC, 2 cases were diagnosed as EPC with DCIS, 2 cases were diagnosed as EPC with invasive carcinoma, 3 cases were diagnosed as invasive carcinoma, 10 cases were diagnosed as papilloma neoplasm, 2 cases were diagnosed as EPC suspicious for invasion and 1 case was diagnosed as atypical ductal hyperplasia. Subsequently, surgical excision was advised in all of these cases. Breast-conserving surgery/lumpectomy was performed in 16 cases (34.0%) and mastectomy was performed in 31 cases (66.0%). Sentinel lymph node biopsy (SLNB) was performed in all 47 cases to evaluate the axillary lymph node status and 4 (8.5%) of the cases were found to exhibit axillary lymph node involvement. Notably, all of the patients who had positive sentinel lymph nodes were diagnosed with EPC associated with invasive carcinoma. Additionally, all of these patients underwent subsequent axillary lymph node dissection (ALND) (Table III). Due to the observation that a substantial proportion of invasive EPC cases were axillary lymph node-positive (21.1%), SLNB should be considered in this unique subgroup.
Concerning the postoperative treatments, tumor size, histological grade and the molecular subtyping of the invasive tumor cells should be considered when frankly invasive carcinoma is present in association with an EPC. In the present study, radiotherapy, chemotherapy, as well as endocrine therapy, were administered. Among all of the patients, 18 of them (39.1%) received adjuvant radiotherapy. Additionally, 4 patients (8.7%) who were originally diagnosed with axillary lymph node metastasis received systemic chemotherapy. Notably, these 4 patients all had invasive EPC and their invasive components were all HR-negative or HER2-positive. Moreover, one 41-year-old woman diagnosed with EPC associated with invasive carcinoma received adjuvant HER2-targeted therapy for 1 year as the invasive tumor cells were HER2-positive. Furthermore, adjuvant endocrine therapy was administered in 42 patients (91.3%). In the present study, all of the postmenopausal patients with EPC were given aromatase inhibitors (AIs), and all the premenopausal patients with EPC were given selective estrogen receptor modulators (SERMs), such as tamoxifen. Detailed treatments of this case series are listed in Table III.
Due to of the aggressive biological features and metastatic potential of invasive EPC, the clinicopathological characteristics of non-invasive EPC were compared with invasive EPC (Table IV). The results indicated that invasive EPC was positively associated with a larger tumor size, ER-negative status and axillary lymph node metastasis when compared with non-invasive EPC. Although not statistically significant, it should be noted that a PR-negative status was more often observed in EPC associated with invasive carcinoma.
Follow-up information was available for 42 patients, with a mean follow-up of 31.5 months (range, 11.0–67.0 months). Routine physical and radiological examinations at the follow-up were performed to monitor recurrence. Until October 1, 2022, 40 cases were free of any recurrence on clinical examination and radiological imaging, while 2 patients experienced local recurrence or distant metastasis. One of these patients developed ipsilateral breast recurrence ~28 months after breast-conserving surgery, and they received a subsequent mastectomy in combination with ALND; the pathological examination showed a pure EPC with high nuclear grade and no regional lymph node metastasis. The immunohistochemical results demonstrated the recurrent EPC tumor was positive for HR and negative for HER2. However, the patient refused post-operative radiotherapy after primary breast-conserving surgery. In the other case, the patient was diagnosed with invasive EPC, and received mastectomy together with SLNB and adjuvant endocrine therapy. A total of 41 months after the primary surgery, routine ultrasonography found an enlarged ipsilateral supraclavicular fossa lymph node and metastatic adenocarcinoma was found in the ultrasound-guided core needle biopsy. Notably, the immunohistochemical staining revealed the metastatic lesion in the supraclavicular fossa was HR-negative and HER2-negative, although the corresponding primary tumor was classified as luminal A subtype. The computed tomography scan also suggested multiple pulmonary metastases and therefore chemotherapy was administered. In the follow-up, the 2 patients were still alive. The other patients (95.2%) were still in good health with no evidence of relapse or metastasis.
Discussion
EPC is used to define papillary carcinomas, which are well-defined lesions surrounded by a fibrous capsule, that lack myoepithelial cells in the periphery and the papillae (4). Previous studies have demonstrated that EPC tends to affect elderly women and always presents as a subareolar mass and/or with nipple discharge (18,19). Consistent with these reports, the age of the patients in the present study ranged from 41–88 years, with a median age of 62.1 years. The mean age at initial diagnosis of non-invasive EPC and EPC associated with invasive carcinoma was 61.4 and 62.7 years, respectively. These observations may seem inconsistent with previous studies, which typically had a mean age at initial diagnosis of invasive EPC that was lower when compared with the non-invasive counterparts (7,15). However, it should be acknowledged that a larger sample size is required to further obtain a meaningful result and it should be noted that the sample size in the present study was larger than that of the two aforementioned studies. Previous studies have demonstrated that male patients comprise 2–7% of EPC cases (2,3). This is inconsistent with the present report where a 70-year-old male patient was diagnosed with EPC associated with invasive breast cancer. Unlike several previous case reports (20,21), the male patient in the present case series did not have a significant family history of breast cancer.
The clinical manifestation of EPC mimics a benign breast tumor, as the most common symptom is a palpable breast mass (22,23). As for the tumor size, cases of EPC associated with invasive carcinoma were larger when compared with the non-invasive counterparts. Of note, it was not unusual for patients with EPC to complain of nipple discharge in the present case series (10.6%), and 4 out of 5 patients that presented with nipple discharge had EPC associated with invasion.
Microscopically, although the majority of EPC cases were of a low or intermediate grade according to the Nottingham Grading System in primary breast cancer (24), a substantial amount of tumors showed histological features associated with aggressive behavior, such as high-grade features with a high mitotic count (25,26) or HR negativity. In the present study, 5 EPC cases with high nuclear grade (10.6%) were all invasive EPC and 3 of these exhibited regional lymph node metastases. Therefore, taken together, these findings further indicated that high-grade features may allow EPC to metastasize easily, and these tumors should be staged and treated as non-specific invasive carcinoma.
In the immunohistochemical staining of myoepithelial markers performed in the present study, p63, α-SMA and CK5/6 were negative in the majority of cases, which suggested that myoepithelial cells were often absent in EPC. Although EPC was initially perceived as a rare subtype of in situ carcinoma, the observations of the present study further supported the notion that EPC may be a minimally invasive form of carcinoma with an expansile growth pattern and indolent behavior, or part of a wide spectrum of lesions, ranging from in situ to invasive carcinoma. Due to the lack of myoepithelial cells (27), it has been described that a subset of EPC cases have invasive potential and are able to develop local and/or distant metastases (5,28). The results of the present study also indicated that EPC associated with invasive carcinoma may behave aggressively and should be managed with caution. As for HR and HER2 status, only 4 cases were HR-negative (8.5%), while the majority of EPC cases were HER2-negative (97.9%). Only one of the 15 HER2 (2+) cases was positive in the subsequent FISH analysis. Notably, those patients who were HR-negative or HER2-positive all had EPC associated with invasive carcinoma. The majority of EPC cases in the present study had a luminal A or luminal B phenotype, except for 3 patients with triple-negative breast cancer and 1 patient with HER2-positive cancer. Subsequently, the clinicopathological characteristics of patients with non-invasive EPC were compared with those with invasive EPC. Markedly, invasive EPC was positively associated with tumor size and axillary nodal metastasis. Additionally, a HR-negative status was more often observed in cases of invasive EPC. Therefore, when frankly invasive carcinoma is present in association with EPC, it is recommended to stage and manage invasive EPC based on the characteristics of the invasive component.
To the best of our knowledge, no evidence-based guidelines have yet been established for EPC management given its low incidence rate. Once the tumor is diagnosed with EPC post-biopsy, the primary treatment is based on complete surgical excision, including breast-conserving surgery or mastectomy (3,15). However, differentiating EPC from other papillary breast lesions is difficult when using preoperative core needle biopsies and having to rely on surgical excision to obtain accurate pathological diagnoses (10). Moreover, it has been suggested that pathologists are often confused regarding the displaced fragments of tumor tissue outside the fibrous capsule and true invasion (29). Additionally, a newly proposed variant of invasive lobular carcinoma may sometimes morphologically mimic EPC growth patterns (30,31). In the present study, an ultrasound-guided core needle biopsy was performed in 26 cases before surgery and most of the cases were diagnosed as papillary neoplasm on core needle biopsy and surgical excision was suggested to obtain a clear diagnosis. In the present study, only 1 case of EPC associated with invasion was clearly diagnosed based on core needle biopsy.
Currently, whether SLNB can be omitted when pure EPC was clearly diagnosed before axillary surgery is still contested. However, some researchers have proposed SLNB as a suitable surgical option when invasive EPC is present given its potentially beneficial role in both prognosis and treatments (3,10). Unfortunately, as aforementioned, preoperative diagnosis of whether EPC occurs with invasion or not is a significant challenge. Therefore, all of the patients received SLNB in the present study and only 4 patients with invasive EPC exhibited axillary lymph node metastases (8.7%). Notably, a significant portion of the patients with invasive EPC showed metastasis in the present cohort (21.1%). Thus, to provide additional information for clear diagnosis, risk stratification and appropriate treatment for EPC, diagnostic imaging modalities, such as digital mammography, contrast-enhanced ultrasound and magnetic resonance imaging, are now considered to be of utmost importance (32,33).
Apart from surgical excision, the therapeutic role of adjuvant radiotherapy, chemotherapy, endocrine therapy, as well as HER2-targeted therapy, in EPC remains unclear. In principle, adjuvant treatment of EPC should be based on the malignant potential of the invasive tumor cells rather than the in situ components. Thus, previous publications have recommended adjuvant radiotherapy, chemotherapy and endocrine therapy in patients with EPC associated with invasive carcinoma (7,34). In the present study, 18 patients received adjuvant radiotherapy, 4 patients diagnosed with axillary lymph node metastases received chemotherapy and 1 patient received 1 year of HER2-targeted therapy. Moreover, the majority of patients with EPC received standard hormone therapy. Of note, all the postmenopausal patients with EPC were subsequently given AIs, although whether AIs were associated with superior benefits was unclear when compared with SERMs in postmenopausal patients with non-invasive carcinoma (35). Collectively, the findings further support that lumpectomy/mastectomy in combination with SLNB is a reliable therapeutic choice for patients with EPC. Adjuvant chemotherapy, radiotherapy, as well as endocrine therapy, should be considered in select patients, especially in cases of EPC associated with invasion, which display aggressive histological and biological features.
In conclusion, EPC, which most frequently affects elderly women, has a relatively excellent prognosis. Due to the lack of myoepithelial cells, EPC has metastatic potential although it is considered to be a malignant tumor in situ with indolent behavior. The present study further confirmed that EPC associated with invasive carcinoma has aggressive biological features, especially in lesions associated with unfavorable clinical or pathological characteristics, such as HR-negative and/or high nuclear grade. Local resection, as well as SLNB, should be considered in this population.
Acknowledgements
Not applicable.
Funding
This study was funded by the National Natural Science Foundation of China (grant nos. 81860467 and 82060482) and the Key Science and Technology Support Project of Nanchang (grant no. 2019-258-13).
Availability of data and materials
The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.
Authors' contributions
LX, WQ, NY and YC conceived and designed the study. LX and QM wrote the manuscript. QL contributed to writing and revising the manuscript. YG and CG performed the statistical analysis. CG, QM, QL and LL collected and analyzed the data. WQ performed the pathological examination and provided experimental support. NY and YC drafted the manuscript and revised it critically for important intellectual content. LX and YC confirm the authenticity of all the raw data. All authors read and approved the final manuscript.
Ethics approval and consent to participate
The present study was approved by the Institutional Review Boards of The Third Hospital of Nanchang City (Nanchang, China) (approval no. K-ky2023004). Written informed consent was obtained from the patients at the time of tissue collection according to The Declaration of Helsinki.
Patient consent for publication
Not applicable.
Competing interests
The authors declare that they have no competing interests.
References
|
Salemis NS and Mourtzoukou D: Encapsulated papillary carcinoma of the breast. Breast J. 27:280–283. 2021. View Article : Google Scholar : PubMed/NCBI | |
|
George K, Anna Z, Evanthia K and Vassilios K: Encapsulated papillary carcinoma of the breast: An overview. J Cancer Res Ther. 9:564–570. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Steponavičienė L, Gudavičienė D, Briedienė R, Petroška D and Garnelytė A: Diagnosis, treatment, and outcomes of encapsulated papillary carcinoma: A single institution experience. Acta Med Litu. 25:66–75. 2018.PubMed/NCBI | |
|
Masood S: The significance of accurate diagnosis of encapsulated papillary carcinoma of the breast by core needle biopsy. Breast J. 27:207–208. 2021. View Article : Google Scholar : PubMed/NCBI | |
|
Kitahara M, Hozumi Y, Takeuchi N, Ichinohe S, Fujiwara S, Machinaga M, Saitoh H and Iijima T: Distant metastasis after surgery for encapsulated papillary carcinoma of the breast: A case report. Case Rep Oncol. 13:1196–1201. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Mulligan AM and O'Malley FP: Metastatic potential of encapsulated (intracystic) papillary carcinoma of the breast: A report of 2 cases with axillary lymph node micrometastases. Int J Surg Pathol. 15:143–147. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Tariq MU, Idress R, Qureshi MB and Kayani N: Encapsulated papillary carcinoma of breast; a clinicopathological study of 25 cases and literature review with emphasis on high grade variant. Ann Diagn Pathol. 49:1516132020. View Article : Google Scholar : PubMed/NCBI | |
|
Jackson CR, Felty CC, Marotti JD, Rosenkranz KM and Muller KE: Encapsulated papillary carcinoma with and without frank invasion: Comparison of clinicopathologic features and role of axillary staging. Breast J. 27:209–215. 2021. View Article : Google Scholar : PubMed/NCBI | |
|
Grabowski J, Salzstein SL, Sadler GR and Blair S: Intracystic papillary carcinoma: A review of 917 cases. Cancer. 113:916–920. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Hashmi AA, Iftikhar SN, Munawar S, Shah A, Irfan M and Ali J: Encapsulated papillary carcinoma of breast: Clinicopathological features and prognostic parameters. Cureus. 12:e112822020.PubMed/NCBI | |
|
Patel A, Hoda RS and Hoda SA: Papillary breast tumors: Continuing controversies and commentary on WHO's 2019 criteria and classification. Int J Surg Pathol. 30:124–137. 2022. View Article : Google Scholar : PubMed/NCBI | |
|
Yamamoto Y, Hayashi Y, Sakaki H and Murakami I: Downregulation of fascin induces collective cell migration in triple-negative breast cancer. Oncol Rep. 50:1502023. View Article : Google Scholar : PubMed/NCBI | |
|
Wolff AC, Hammond MEH, Allison KH, Harvey BE, Mangu PB, Bartlett JMS, Bilous M, Ellis IO, Fitzgibbons P, Hanna W, et al: Human epidermal growth factor receptor 2 testing in breast cancer: American society of clinical oncology/college of American pathologists clinical practice guideline focused update. Arch Pathol Lab Med. 142:1364–1382. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Jacobs TW, Gown AM, Yaziji H, Barnes MJ and Schnitt SJ: Comparison of fluorescence in situ hybridization and immunohistochemistry for the evaluation of HER-2/neu in breast cancer. J Clin Oncol. 17:1974–1982. 1999. View Article : Google Scholar : PubMed/NCBI | |
|
Hassan Z, Boulos F, Abbas J, El Charif MH, Assi H and Sbaity E: Intracystic papillary carcinoma: Clinical presentation, patterns of practice, and oncological outcomes. Breast Cancer Res Treat. 182:317–323. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Li X, Xu Y, Ye H, Qin S, Hou F and Liu W: Encapsulated papillary carcinoma of the breast: A clinicopathological study of 49 cases. Curr Probl Cancer. 42:291–301. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Wolff AC, Hammond MEH, Allison KH, Harvey BE, Mangu PB, Bartlett JMS, Bilous M, Ellis IO, Fitzgibbons P, Hanna W, et al: Human epidermal growth factor receptor 2 testing in breast cancer: American society of clinical oncology/college of American pathologists clinical practice guideline focused update. J Clin Oncol. 36:2105–2122. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Schwartz CJ, Boroujeni AM, Khodadadi-Jamayran A, Heguy A, Snuderl M, Jour G, Cotzia P and Darvishian F: Molecular analysis of encapsulated papillary carcinoma of the breast with and without invasion. Hum Pathol. 111:67–74. 2021. View Article : Google Scholar : PubMed/NCBI | |
|
Solanki MH, Derylo AF, Visotcky AM and Jorns JM: Encapsulated and solid papillary carcinomas of the breast: Tumors in transition from in situ to invasive? Breast J. 25:539–541. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
Romics L Jr, O'Brien ME, Relihan N, O'Connell F and Redmond HP: Intracystic papillary carcinoma in a male as a rare presentation of breast cancer: A case report and literature review. J Med Case Rep. 3:132009. View Article : Google Scholar : PubMed/NCBI | |
|
Brents M and Hancock J: Ductal carcinoma in situ of the male breast. Breast Care (Basel). 11:288–290. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Rehman B, Mumtaz A, Sajjad B, Urooj N, Khan SM, Zahid MT, Mannan H, Chaudhary MZ, Khan A and Parvaiz MA: Papillary carcinoma of breast: Clinicopathological characteristics, management, and survival. Int J Breast Cancer. 2022:54278372022. View Article : Google Scholar : PubMed/NCBI | |
|
Morgan S, Dodington D, Wu JM and Turashvili G: Solid papillary carcinoma and encapsulated papillary carcinoma of the breast: Clinical-pathologic features and basement membrane studies of 50 cases. Pathobiology. 88:359–373. 2021. View Article : Google Scholar : PubMed/NCBI | |
|
Galea MH, Blamey RW, Elston CE and Ellis IO: The Nottingham prognostic index in primary breast cancer. Breast Cancer Res Treat. 22:207–219. 1992. View Article : Google Scholar : PubMed/NCBI | |
|
Liu X, Wu H, Teng L, Zhang H, Lu J and Liang Z: High-grade encapsulated papillary carcinoma of the breast is clinicopathologically distinct from low/intermediate-grade neoplasms in Chinese patients. Histol Histopathol. 34:137–147. 2019.PubMed/NCBI | |
|
Rakha EA, Varga Z, Elsheik S and Ellis IO: High-grade encapsulated papillary carcinoma of the breast: An under-recognized entity. Histopathology. 66:740–746. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Athanasiou A, Khomsi F, de Joliniere B and Feki A: Encapsulated papillary carcinoma: A case report and review of the literature. Front Surg. 8:7438812022. View Article : Google Scholar : PubMed/NCBI | |
|
Yee C, Drost L, Niglas M, Chow E and Vesprini D: Early local recurrence in a patient with encapsulated papillary carcinoma of the breast. Clin Breast Cancer. 18:e447–e448. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Kang HJ, Kwon SY, Kim A, Kim WG, Kim EK, Kim AR, Kim C, Min SK, Park SY, Sung SH, et al: A multicenter study of interobserver variability in pathologic diagnosis of papillary breast lesions on core needle biopsy with WHO classification. J Pathol Transl Med. 55:380–387. 2021. View Article : Google Scholar : PubMed/NCBI | |
|
Zheng L, Saluja K and Guo T: Invasive lobular carcinoma mimicking encapsulated papillary carcinoma with a literature review: A rare variant detected serendipitously. Int J Surg Pathol. 30:912–920. 2022. View Article : Google Scholar : PubMed/NCBI | |
|
Motanagh SA and Muller KE: Invasive lobular carcinoma with papillary features: A newly described variant that poses a difficult histologic differential diagnosis. Breast J. 26:1231–1233. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Kurtoğlu Özçağlayan Tİ and Öznur M: Digital mammography, ultrasound and magnetic resonance imaging characteristics in differential diagnosis of papillary carcinoma subtypes of the breast and diagnostic challenges. Eur J Breast Health. 18:172–181. 2022. View Article : Google Scholar : PubMed/NCBI | |
|
Tang CY, Guan PS, You QQ, Yuan HX and Wang WP: Contrast-enhanced ultrasound combined with ultrasonic elastography to diagnose encapsulated papillary carcinoma: A case report. Clin Hemorheol Microcirc. 82:391–396. 2022. View Article : Google Scholar : PubMed/NCBI | |
|
Tariq N, Mamoon N, Usman M, Ali Z and Nazir I: Encapsulated papillary carcinoma (EPC) of breast: A clinical, pathological and immunohistochemical analysis of eight cases. J Pak Med Assoc. 66:1490–1493. 2016.PubMed/NCBI | |
|
Lazzeroni M, Dunn BK, Pruneri G, Jereczek-Fossa BA, Orecchia R, Bonanni B and DeCensi A: Adjuvant therapy in patients with ductal carcinoma in situ of the breast: The Pandora's box. Cancer Treat Rev. 55:1–9. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Giuliano AE, Edge SB and Hortobagyi GN: Eighth edition of the AJCC cancer staging manual: Breast cancer. Ann Surg Oncol. 25:1783–1785. 2018. View Article : Google Scholar : PubMed/NCBI |
