|Year : 2013 | Volume
| Issue : 4 | Page : 564-570
Encapsulated papillary carcinoma of the breast: An overview
Kyrgias George1, Zygogianni Anna1, Kostopoulou Evanthia2, Kouloulias Vassilios3
1 Department of Radiotherapy; Department of Radiation Oncology, University Hospital of Larissa, Thessaly, Greece
2 Department of Pathology, School of Health Sciences; Department of Pathology, University Hospital of Larissa, Thessaly, Greece
3 Department of Radiology, Radiotherapy Unit, Kapodistrian University of Athens, Greece
|Date of Web Publication||11-Feb-2014|
University of Thessaly, School of Health Sciences, Faculty of Medicine, Department of Radiotherapy, Biopolis, Larissa 41110
Source of Support: None, Conflict of Interest: None
Any papillary growth of the breast presents both a diagnostic and a therapeutic challenge: For each one of them a diagnosis of whether they are malignant or benign in nature is required as well as appropriate staging and suitable treatment. In the international literature, we find a considerable amount of different terms being used for papillary breast growths. As a result, pathological and clinical evaluation is somewhat problematic. Encapsulated papillary carcinoma (EPC) is an interesting subgroup of breast papillary tumours. Because of its rarity, there have been only a limited number of large clinical studies that safely assess its appropriate treatment and expected outcome. However, more safe data exist in terms of prognosis - which seems to be excellent, as almost all published studies regarding these tumours have confirmed so far. We present a systematic overview of breast EPC and of the most important studies published on this topic in order to make diagnosis and treatment more straightforward for cancer clinicians. The information for this review was compiled by searching the Pubmed, Medline, Scopus, Embase, and ISI Web of Science databases for articles published from 1980 through December 2012. Electronic early-release publications were also included.
Keywords: Breast, encapsulated papillary carcinoma, intracystic papillary carcinoma, rare tumours
|How to cite this article:|
George K, Anna Z, Evanthia K, Vassilios K. Encapsulated papillary carcinoma of the breast: An overview. J Can Res Ther 2013;9:564-70
| > Introduction|| |
The terminology used in reports of papillary growths of the breast varies confusingly in the international literature, making their pathological and clinical evaluation more difficult.
The most recent studies which connect nomenclature and classification to clinical evaluation and biological behaviour have somewhat clarified the uncertainties regarding papillary lesions of the breast. Moreover, the latest edition of the "WHO Classification of the Tumors of the Breast" (4 th Edition, Lyon 2012) has clarified the issue further.
Encapsulated papillary carcinomas (EPCs) of the breast, also referred to in the past as intracystic papillary carcinomas, are a subgroup of intraductal papillary lesions of the breast characterised by non-aggressive biological behaviour and excellent prognosis. Only a few clinical studies have been published on this issue, most of them case reports.
We performed a systematic overview of this malignancy of the breast and of the most important studies published on this topic in order to make diagnosis and treatment more straightforward for cancer clinicians.
| > Materials and Methods|| |
The information for this review was compiled by searching the Pubmed, Medline, Scopus, Embase, and ISI Web of Science databases for articles published from 1980 through December 2012. Electronic early-release publications were also included.
The search terms used included the key words "breast cancer", "encapsulated papillary carcinoma", "intracystic papillary carcinoma" and "rare tumours".
Articles published in any language other than english were excluded. When possible, primary sources have been quoted.
A senior author analyzed the search results, decided which studies could be potentially included and requested the full texts of these.
References were chosen on the basis of the best clinical or technical evidence and selected on the basis of the following inclusion criteria: In terms of study design, selection was restricted to systematic reviews, meta-analyses, clinical trials, cohort studies, case -control studies and case series; in terms of sample size, there was a restriction of five in number of patients who have been studied.
| > Epidemiology and Clinical Presentation|| |
Encapsulated Papillary Carcinoma of the breast (EPC) is a rare malignancy accounting for 0.5-1% of all breast cancers,  and up to 3% in certain areas (e.g. Nigeria). 
EPC is more frequent in the elderly (median age of 69.5 years, range 22 to 99) and much more frequent in women (up to 96.5%) than in men (up to 3.5%). In a large study using data from the database of the National Cancer Institute, Surveillance, Epidemiology and End Results 1973-1998, Giordano et al.,  reported 385,683 cases of breast cancer of which 2,537 (0,65%) involved men. Of these men, only 63 (2.6%) had papillary histology. Despite the small number of reports concerning male EPC in the international literature, ,,,,,,,, the evidence is that, as with woman's EPC, male EPC involves the elderly and seems to have an excellent prognosis. 
Caucasians are the most common sufferers of EPC (63%), followed by Hispanics (12-30%), Asian/Pacific Islanders (10-13%) and African-Americans (7-10.5%). 
EPC can be presented either as a palpable mass in an otherwise normal breast or as a swollen breast due to the presence of a huge cystic mass within it.  In some cases, nipple retraction may be present with or without nipple bleeding, requiring further examination using imaging and biopsy. EPC may also be a simple mammographic finding without any clinical evidence. Almost 50% of the EPCs arise in the retro-areolar region. 
The terminology used in reports of papillary growths of the breast varies confusingly in the international literature, making their pathological and clinical evaluation more difficult. The most recent studies classify EPC as an independent histological entity. ,,
Grabowski et al., report that about 50% of all EPCs are in situ lesions, whereas in the case of invasive EPCs <10% are regionally extended and <1% are metastatic.
Mulligan and O'Malley  classified papillary carcinomas into solid, intracystic without invasion, intracystic with a focus of invasion (usually ductal carcinoma) and invasive papillary carcinomas.
The separation of papillary lesions into categories by Collins and Schnitt  modified in the base of the WHO classification of tumors the breast (2012) as reported in [Table 1], seems appropriate and clinically meaningfull. They clearly differentiate benign from malignant papillary lesions, and encapsulated from solid papillary carcinomas of the breast. The presence or absence of myoepithelial cells represents an important criterion for differential diagnosis, as presented in [Table 1].The current WHO classification divides "intraductal" papillary lesions of the breast into four groups: Intraductal papilloma, intraductal papillary carcinoma, encapsulated papillary carcinoma and solid-papillary carcinoma.  Despite any existing drawbacks, this constitutes an important change in the classification in comparison to the previous WHO edition. Encapsulated papillary carcinoma is described as a lesion surrounded by a thick fibrous capsule and composed of delicate fibrovascular stalks, covered by a monomorphic population of neoplastic epithelial cells. These can be arranged in solid or cribriform patterns and exhibit low- or intermediate-grade nuclei.  Myoepithelial cells are not present, neither at the periphery of the lesion nor within the fibrovascular cores and their absence can be verified by immunohistochemical stains.
Immunohistochemical stains, such as p63, actin, calponin, can facilitate the recognition of myoepithelial cells; thus, they are useful in differentiating EPC from other breast papillary lesions. 
|Table 1: Distribution of myoepithelial cells in papillary lesions of the breast|
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When neoplastic epithelial elements infiltrate beyond the surrounding fibrous capsule, frank invasive carcinoma is diagnosed and this should be differentiated both from entrapment of neoplastic cells in the fibrous capsule and from their displacement into a previous biopsy tract.
The absence of myoepithelial cells at the lesion periphery has been interpreted as revealing a minimally invasive form of carcinoma, , or according to other investigators, a form of carcinoma "in transition" between in situ and invasive carcinoma.  Interestingly, the expression pattern of invasion-associated markers appears intermediate in nature between ductal carcinoma in situ (DCIS) and invasive cancer. 
As a consequence, staging of pure EPC is controversial. However, according to the WHO Working Group, these lesions, in the absence of conventional invasive carcinoma, should be considered and treated as Tis disease. 
Papillary carcinomas of the breast (EPCs included) present some architectural histological similarities to papillary thyroid carcinoma, but without any evidence of rearranged during transfection (RET) oncogene rearrangements. 
Imaging and diagnosis
In mammography, the presence of a growth which is round, oval or lobulated in shape, with usually well-defined margins, raises suspicions of a papillary carcinoma. This suspicion is reinforced by the presence of pleomorphic microcalcifications appearing within the tumour. The tumour may be surrounded by a, usually minimal, fibrotic reaction. 
Ultrasonography is the imaging modality of choice to distinguish the cystic from the solid variety of papillary carcinoma.  On an ultrasound the EPCs may have a hypoechoic, anechoic or mixed appearance with respect to the prevalence of their solid or cystic component. An irregular shape and/or discontinuous circumference are features of the invasive forms of EPC.  Possible internal vascularity can be seen with Doppler imaging.
An MRI image of a breast papillary carcinoma offers limited potential for diagnosis because of the overlapping of the morphologic features of a papillary carcinoma with those of a benign papilloma. In contrast, an optimal MRI imaging can be very useful in ensuring optimal surgical procedures are applied. 
Diagnosis of an EPC of the breast is confirmed by needle biopsy in most cases. Mammary Ductoscopy (MD) is one of the most appropriate methods to obtain an accurate overview and a biopsy is recommended for any papillary growth of the breast according to some authors,  although others state that MD currently remains experimental as there is little benefit to gain from the added invasiveness.
A mammotome biopsy is another useful option. The Mammotome Biopsy System (MBS) is an image-guided and vacuum-assisted biopsy device for breast lesions which are clinically non-palpable but detectable with mammography.  The MBS is equally effective but less invasive and with fewer comorbidities than needle aspiration biopsy. The MBS has also become established in recent years as a safe, cost-effective alternative to open surgery for the removal of certain benign breast lesions, especially breast intraductal papillomas. However, whenever a histopathologic examination leads to diagnosis of a papilloma with atypical hyperplasia or imaging examinations reveal a suspected malignant lesion despite negative biopsy results, surgical excision is always indicated. 
Treatment and outcome
Due to the rarity of breast papillary tumours, well-designed outcome studies that propose an evidence-based treatment have not been carried out so far.
Surgical excision with negative surgical margins (mainly lumpectomy) appears to be sufficient for pure EPCs. Axillary lymph node dissection seems to make sense only for patients who have a breast EPC associated with conventional DCIS or (micro) invasive carcinoma, but sentinel node biopsy could be equally effective and with fewer comorbidities. 
In almost all relevant studies, EPC appears as an oestrogen receptor (ER) positive malignancy for which hormone therapy could be very useful, whereas the role of post-lumpectomy radiotherapy remains unclear.  According to Fayanju et al.,  the role of both adjuvant radiotherapy and hormonal therapy remains controversial.
In conclusion, the main therapeutic procedure so far remains surgical excision (lumpectomy) followed by adjuvant radiotherapy and, after careful considerations of the risks and benefits, hormonal therapy for invasive subtypes. There is currently no role for cytotoxic chemotherapy.
The non-aggressive biological behaviour of EPCs means that the prognosis is excellent, the median survival ranging 60 to 95% for histologically invasive or in situ EPCs respectively. EPCs which have invasive elements or DCIS can recur locally (10%) or metastasise (2.5%). 
| > Discussion|| |
Only a few clinical studies have been published on EPC, most of them case reports. We reviewed the most important of these [Table 2] and [Table 3], i.e., those which included a large enough number of cases to help us reach the most reliable conclusions possible. The reported studies refer only to Encapsulated Papillary Carcinomas, not solid ones.
|Table 2: Studies on the encapsulated papillary carcinomas of the breast: Patients' characteristics|
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|Table 3: Studies on the encapsulated papillary carcinomas of the breast: Treatment and outcome|
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Carter et al., (1983)  with a cohort of 41 patients with EPC of the breast from three different centres (Yale- New Haven Hospital, Charlotte Memorial Hospital, and Johns Hopkins Hospital) studied the clinical behaviour of papillary carcinomas of the breast. For this purpose, they assorted the breast carcinomas with papillary morphological elements into three categories: Intracystic Papillary Carcinoma, Ductal Carcinoma in situ (DCIS) with papillary elements and Invasive Papillary Carcinoma. After a follow-up of at least seven years, they concluded that the Invasive Papillary Carcinomas had displayed the most aggressive behaviour, because they demonstrated a considerable likelihood of regional and distant metastases. Nowadays, the terminology and anatomic pathological classification of the above three categories have changed considerably: "Intracystic Papillary Carcinoma" has been named EPC. Ductal Carcinoma In Situ (DCIS) with papillary elements is classified with intraductal proliferative lesions of the breast. Invasive Papillary Carcinoma is not classified with Intraductal Papillary Lesions of the breast, but instead is included with special subtypes of the invasive carcinomas of the breast. Whatever the terminology, however, the work of Carter et al., demonstrated the benign biological behaviour of Intracystic Papillary Carcinomas, i.e., EPC using current terminology.
Lefkowitz et al., (1994)  reported a clinicopathological study of 77 cases of EPC of the breast which had had a favourable outcome, as can be seen in [Table 3]. Nevertheless, the authors concluded that EPC of the breast has a less favourable prognosis than other non-comedo breast carcinomas and that the favourable outcome of their patients could be the result of the small size of the tumours and of the aggressiveness of the treatment applied. They added that, although mastectomy provides the longest disease-free survival, it probably represents an overtreatment for most cases.
Leal et al., (1998),  based on their clinicopathological and immunohistochemical study of 29 cases of EPC, concluded that EPC is a carcinoma of elderly women, with low to intermediate malignancy, high ER positivity and c-Erb-B2 negativity.
In a clinical study of 23 patients suffering from EPC, Harris et al., (1999)  confirmed the excellent prognosis of this tumour and recommended wide local excision without axillary lymph node dissection as the treatment of choice for these cases in order to avoid other excessive therapeutic procedures.
In addition, Solorzano et al., (2002)  from the University of Texas - M.D. Anderson Cancer Center confirmed the excellent prognosis of pure EPC. They also claimed that axillary lymph node dissection (ALND) is of no benefit for pure EPC, whereas sentinel node biopsy is a good alternative to ALND for EPCs with an invasive component. Finally, the authors considered that the benefits of adjuvant radiotherapy are uncertain and that any possible adjuvant therapy should be tailored to the patient's histological findings.
In their study on forty-five patients from the Washington University/Barnes Jewish Hospital, Fayanju et al., (2007)  investigated the role of radiation and hormonal therapy in the therapeutic management of EPC. In this paper, the authors advanced the hypothesis that hormone replacement therapy in postmenopausal women could increase the risk of EPC, as is the case for all ER-positive breast cancers. They also supported the claim of Solorzano et al.,  that axillary node dissection seems to be of no benefit for women suffering from EPC and that any adjuvant treatment should be tailored to the patient's histology in order to ensure the excellent outcome expected for these neoplasms. Hence, adjuvant radiotherapy and/or hormone therapy should be considered both for patients with EPC associated with DCIS or microinvasion and for the patients less than 50 years of age with pure EPC.
The study by Grabowski et al., (2008)  is the one with the largest number of cases of EPC based on 917 patients identified on the California Cancer Registry. There were 427 (47%) cases of EPC in situ and 490 (53%) cases of invasive EPC. According to the authors, the prognosis and the long-term survival are substantially the same in the two subgroups but the evaluation of axillary status could be useful for both treatment and prognosis. For all these reasons, they recommend that EPCs be treated in the same way as DCIS with the option for sentinel lymph node biopsy.
A rather different opinion has been voiced by Akagi et al., (2009)  regarding the behaviour of EPC. They studied fourteen patients treated for EPC between the years of 2000 and 2006 at the National Cancer Center Hospital of Tokyo - Japan. In the 14 patients in this study there were no local recurrences or metastases after a follow-up period that ranged from 1 to 72 months. Despite this, after consideration of some case-report publications of EPC with concomitant liver metastases,  Akagi et al., proposed that EPC be evaluated with regards to its malignant potential and be treated like DCIS (Ductal Carcinoma In Situ).
Esposito et al., (2009)  in their study of 27 patients suffering from Encapsulated Papillary Carcinoma of the breast, clearly distinguish EPCs from Invasive Ductal Carcinomas (IDC) of the breast based on their immunohistochemical characteristics. The authors found that EPC-cells have a moderate to intense Collagen type-IV expression which is absent in the cells of the IDC. In conclusion, Esposito et al., confirmed that EPCs have an excellent prognosis and so local treatment alone may be sufficient to control the disease thoroughly.
Seal et al., (2009)  in their study of five cases of EPC from British Columbia Cancer Agency, Vancouver, Canada, consider EPC as a tumour of uncertain malignant potential which should not be treated like invasive ductal carcinoma of the breast.
Calderaro et al., (2009)  found twenty cases of EPC between 7,000 patients treated for breast cancer in the St. Louis Hospital in Paris - France from 1996 to 2006. In their study the authors confirm the low malignancy and excellent prognosis of EPCs and they consider the term "encapsulated papillary carcinoma" proposed by Collins et al., as the most appropriate for these tumours.
The retrospective study of Wynveen et al., (2011)  included 39 patients with 40 EPCs treated at MSKCC (Memorial Sloan-Kettering Cancer Center) from January 1990 to June 2008, as reported in our [Table 2] and [Table 3]. The authors' conclusions add to the widespread body of evidence of the favourable prognosis of EPC, but they indicated the existence of a relative risk of local recurrence in the event of breast-conserving surgery being performed. When such surgery is performed, the authors propose that the potentially beneficial role of adjuvant radiotherapy and hormonal therapy be taken into consideration, since EPC is consistently positive for oestrogen receptors (ER) but negative for HER2. They also propose sentinel lymph node biopsy as a surgical option even if axillary lymph node metastases of EPC are extremely rare.
Another retrospective study performed by Rakha et al., (2011)  used the data from the pathology database of the Nottingham University Hospital NHS Trust (NUH). The study included 207 patients with EPC diagnosed between the years 1990 and 2010. The clinical and outcome data of the study are summarised in [Table 3]. Moreover, the authors consider two subtypes of pure EPC (Encapsulated Papillary Carcinoma without invasive elements): The intracystic one (EPC) and the solid one (SPC). With both of these types, there is controversy as regards the behaviour and the optimal treatment. On this point, they disagree with the 2012 WHO Classification ([Table 1] and the section "Pathology" of this article). They also suggest the abolition of the term "Invasive Papillary Carcinoma" for PCs with an invasive component, which should be named according to their non-papillary invasive component. This opinion is in line with the 2012 WHO Classification. Rakha et al., concluded that, for EPC, a carcinoma with such a favourable prognosis, moderate local treatment, backed up in selected cases by hormonal therapy, is sufficient for an optimal outcome.
| > Conclusions|| |
Encapsulated Papillary Carcinoma of the breast is a rare malignancy of the elderly, much more frequent in women and in Caucasians, with an excellent prognosis, especially in the absence of invasive elements.
The mainstay treatment is surgical excision with negative margins (mainly lumpectomy and alternatively mastectomy for oversized tumours). For EPCs with an invasive component, sentinel node biopsy is a good alternative to axillary lymph-node dissection, in order to provide useful input for both adjuvant treatment and prognosis.
Adjuvant therapy with hormones and/or radiotherapy could be useful in the cases which present either invasive elements or coexistent DCIS given their low, but not insignificant, possibility of locoregional relapse and/or metastases.
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[Table 1], [Table 2], [Table 3]