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Abstract

Intracystic papillary carcinoma (IPC) is a rare tumor with good prognosis that occurs in only 5% to 7.5% of male breast cancer. We report a case of a 46-year-old man who presented a brown nipple discharge a few months ago. He had a bilateral IPC and an invasive ductal carcinoma on the right breast. A double mastectomy was then performed with a bilateral sentinel lymph node biopsy, and he received chemotherapy, radiotherapy, and hormonotherapy. Two years after the diagnosis, the patient recovered and was free of recurrence. Considering the scarcity of this tumor type, we conducted a systematic literature review on the PubMed of all the cases of IPC in men. The clinical presentation, imaging, and treatment of the 43 case reports from the 41 articles selected were described. Furthermore, no clear guidelines for IPC management are available. Conservative surgery should also be preferred, and a sentinel lymph node biopsy should be performed systematically. Moreover, radiotherapy should be proposed in the case of conservative surgery, and hormone therapy could be proposed in the case of invasive IPC or IPC associated with a ductal carcinoma in situ.

Keywords

Intracystic papillary carcinoma encapsulated papillary carcinoma male breast management

1. Background

Male breast cancer is a rare disease that accounts for only 1% of all breast cancers. Sub-Saharan Africa has high rates of male breast cancer, accounting for 7%–14% of all breast cancers. The average age of onset in men is 65 years, and risk factors include family history, genetic predisposition, previous radiation exposure, androgen deficiency, or excess estrogen [1]. Brinton et al. found a significant association between male breast cancer and weight, as well as with obesity, Klinefelter syndrome, gynecomastia, and diabetes [2].

Intracystic papillary carcinoma (IPC), also known as encapsulated papillary carcinoma, is a rare tumor that accounts for between 0.5% and 2% of breast cancers in women and between 5% and 7.5% of breast cancers in men [3]. The majority of cases present a mass, painful or not, with or without nipple discharges. The location is most often retro-areolar, and its size can vary from 1 to 14 cm [4].

2. Case report

A 46-year-old-man from sub-Saharan Africa presented with a bloody right nipple discharge several months ago. His medical history included hypertension, rheumatoid arthritis, and moderate obesity (BMI: 33), and he had never smoked and had never taken any hormones. In addition, he had never had any breast traumas and had no significant family history. The physical examination revealed bilateral gynecomastia and a suspicious painless mass in the lower outer quadrant of the right breast, with spontaneous light brown nipple discharges (Fig. 1).

Fig. 1.

Spontaneous light brown nipple discharge.

The mammogram confirmed a 18-mm spiculated mass in the right lower outer quadrant and exhibited a retroareolar 13-mm well-circumscribed mass on the left breast. Additionally, the ultrasonography also showed that the previously seen mass in the right breast was an irregular lobulated mass of 28 × 21 × 12 mm more than 1 cm from the nipple. The tests also uncovered a 10-mm right axillary lymph node with an irregular cortex thickness of 2.6 mm. On the left, two hypoechoic complex central cysts in the retroareolar region were found, one 13 × 9 × 11 mm and one 9 × 5 × 7 mm, separated by 16 mm (Fig. 2) (ACR5 classified imaging). Unlike the ultrasound, the magnetic resonance distinguished the mass from the right breast as two distinct masses: an irregular, lobulated, and spiculated cyst of 13 mm and a complex cyst of 10 mm (Fig. 3). The chest X-ray, upper abdominal ultrasound, and bone scan did not reveal any distant lesions either.

Fig. 2.

Hypoechoic complex central cyst of 13 × 9 × 11 mm in the left breast.

Fig. 3.

Axial T2-weighted MR image showing two bilateral complex cystic masses. The right mass is characterized by an early and intense enhancement and washout (a). Enhancement of the walls of cystic masses on an axial contrast-enhanced T1-weighted subtraction image (b).

The genetic testing displayed no mutation among a wide panel of 26 genes, including BRCA 1, BRCA 2, PALB2, CHECK2, and TP53.

The core needle biopsies manifested a grade 1 invasive ductal carcinoma (IDC) on the right breast and two IPCs of the left breast associated with the foci of a ductal carcinoma in situ (DCIS). The cytopuncture of the right axillary lymph node showed no atypia.

In view of the results, we decided to perform a double mastectomy with a bilateral sentinel lymph node biopsy (SLNB).

In the right breast, the final pathological diagnosis turned out to be a bifocal tumor, with a distance of 2 mm and with the foci of a grade 2 DCIS measuring at least 25 mm. This bifocal tumor was composed of a grade 2 IDC of 13 mm, with Ki67 at 10%–15% and a grade 2 pure IPC of 10 mm with Ki67 at 15%–20% (Figs 4 and 5). Both SLNB had tumor emboli within the capsule but no metastatic infiltration of the parenchyma. On the left breast, there was a retroareolar high-grade IPC of 13 mm with Ki67 at 20% and a grade 3 DCIS with a papillary architecture of 9 mm. Further, a grade 2 DCIS measuring at least 5 mm was found, and the two SLNB were negative. No lymphovascular invasion was detected, and the progesterone and estrogen receptors were positive for all tumors without HER2 amplification.

Fig. 4.

Pure IPC in the right breast. This low power view exhibits a well-circumscribed nodule surrounded by a fibrous capsule. The lesion is composed of fibrovascular stalks covered by a multilayered neoplastic population. Immunohistochemical staining P63, highlighting myoepithelial cells, shows their absence in the periphery as well within the papillary stalks.

Fig. 5.

Pure IPC in the right breast. Close up on the thick fibrous capsule (a) lacking a myoepithelial cell layer, positive around the normal ductal (upper right) (b), and a papillary architecture composed of fibrovascular stalks lined by an atypical ductal cell population in solid or cribriform patterns (c). The capsule may contain “entrapped” neoplastic groups (d), possibly in the biopsy site, which should not be considered true invasion, defined as infiltration beyond this capsule.

We decided to administer adjuvant paclitaxel–epirubicin–cyclophosphamide chemotherapy, right axillary radiotherapy, and adjuvant hormonal therapy with tamoxifen after the multidisciplinary consultation. A two-year follow-up revealed no signs of relapse, and the patient tolerated the adjuvant hormonal therapy with tamoxifen well.

3. Discussion and review of literature

Given the uncommonness of this tumor type, we decided to conduct a systematic review of the literature on the reported cases of papillary carcinoma in male breasts. We searched PubMed with the keywords “intracystic papillary carcinoma”, “encapsulated papillary carcinoma”, and “male breast”. We did not filter for the year or type of document, and we selected documents in English, French, and Spanish. Moreover, we identified 72 articles on PubMed, and only 41 were selected. We also eliminated nine articles on the basis of titles and abstracts and 18 on the basis of contents, and four were unavailable. A total of 43 case reports were described from the 41 articles analyzed. Table 1 shows the data collected from these case reports. The mean age of the reported cases was 65 years.

Through this discussion, we describe the radiological and anatomopathological characteristics and the management of IPC.

On mammography, it presents itself as a well-circumscribed mass, which may be round or oval with well-defined or irregular margin. Ultrasonography will show a complex cystic and solid mass, and the cystic portion may show septations with solid papillary projections in the cyst lumen [4]. Doppler may show intra-tumoral blood flow or large feeding vessels [22]. Magnetic resonance may also increase the diagnostic sensitivity by providing additional information on morphology, mass vascularization, and local extension [45].

IPC is histologically a well-defined tumor with a papillary architecture and surrounded by a fibrous capsule [46,47]. Some authors consider pure IPC to be a variant of carcinoma in situ, while others regard it to be an invasive carcinoma. The P63 immunostaining demonstrated the absence of a myoepithelial layer around the periphery of the tumor, thereby confirming the diagnosis of IPC and distinguishing it from carcinoma in situ. Accordingly, recent studies consider it a low-grade invasive carcinoma [47,48]. Nevertheless, one of the theories of Collins et al. is that they should still be considered in situ lesions because the lack of detection of the myoepithelial layer could be due to its compression in the dilated duct [47]. The preferred method is to combine fine needle aspiration cytology and a core needle biopsy to establish a more reliable diagnosis and reduce false negative rates [29].

What distinguishes invasive IPC from pure IPC is having the focal areas of irregular stromal invasion beyond the fibrous capsule [49]. Grabowski et al. validated that, finally, this is of no clinical significance because a similar 10-year survival rate was observed between the two groups in a cohort of 917 cases including 32 men. The prognosis was excellent in both cases [50]. In our review, 27/43 (63%) were pure IPCs, 9/43 (21%) were invasive IPCs, 5/43 (12%) were IPCs associated with a DCIS, and 2/43 (5%) were IPCs associated with an IDC.

Table 1
Reported cases in the literature of intracystic papillary carcinoma in men

Author Year Age Discharge Pain Location Imaging Method of diagnosis Surgery Axillary staging Final pathological diagnosis Grade IPC ER and/or PR HER2 Positive nodes Adjuvant therapy

Agrawal et al. [5] 2017 52 Yes Yes Subareolar US FNAC Lumpectomy No Pure IPC NS Yes Pos NS NS

Akagi et al. [6] 2009 70 NS NS NS US CNB Lumpectomy No Pure IPC 2 Yes Pos NS Tam

Al Salloom et al. [7] 2015 53 NS No NS MG FNAC + CNB Mastectomy ALND Pure IPC 2 + 3 Yes Nég No NS

Anan et al. [8] 2000 75 NS No Subareolar US+ MG FNAC Mastectomy ALND Pure IPC NS NS NS No NS

Andres et al. [9] 2003 74 NS No Retroareolar US+ MG FNAC Lumpectomy No Pure IPC NS NS NS NS No

Arora et al. [10] 2010 81 NS NS Subareolar NS NS Mastectomy No IPC + invasion NS Yes Nég NS NS

Balsa-Marína et al. [11] 2005 66 NS No Lateral US+ MG Lumpectomy Lumpectomy No Pure IPC NS Yes Nég NS Rth + Tam

Brahmi et al. [12] 2009 50 NS NS Retroareolar US+ MG + MRI Lumpectomy Mastectomy ALND IPC + DCIS 2 Yes NS No No

Başara Akın et al. [13] 2019 72 NS No Retroareolar US+ MG CNB Mastectomy No Pure IPC NS Yes Nég NS NS

De rosa et al. [14] 1992 70 NS NS NS US Lumpectomy Lumpectomy ALND IPC + invasion NS NS NS No NS

Downing et al. [15] 2014 74 No NS Subareolar US+ MG CNB Mastectomy SLNB Pure IPC 3 Yes Pos No No

Hariprasad S. et al. [16] 2013 50 NS No Subareolar US FNAC Mastectomy No Pure IPC 2 Yes NS NS No

Hu et al. [17] 2016 59 Yes NS Lateral US+ MG FNAC Mastectomy SLNB Pure IPC 1 Yes Nég No Tam

Hussain et al. [18] 2009 58 No No NS US CNB Mastectomy SLNB IPC + invasion 2 Yes Nég No Tam

Imoto et al. [19] 1998 62 NS NS Subareolar MG FNAC Lumpectomy No Pure IPC 1 NS NS NS No

Inoue et al. [20] 2003 72 Yes NS Retroareolar US Discharge cytology Lumpectomy No Pure IPC NS Yes NS NS No

Jeffrey et al. [21] 1994 81 NS NS Subareolar NS FNAC Mastectomy ALND Pure IPC NS NS NS No NS

Johnson et al. [22] 2008 70 No No Subareolar US+ MG CNB Mastectomy SLNB Pure IPC 2 Yes Nég No NS

Kelessis et al. [23] 2011 61 Yes No central MG Discharge cytology Mastectomy ALND Pure IPC NS Yes NS No Tam

Kihara et al. [24] 2004 68 No No Subareolar US+ MG + MRI FNAC Mastectomy ALND Pure IPC NS Yes NS No Tam

Kinoshita et al. [25] 2005 71 Yes NS Retroareolar US+ MG CNB Mastectomy No Pure IPC 3 Yes Nég NS No

Kinoshita et al. [26] 2018 64 NS NS Subareolar US CNB Mastectomy SLNB IPC + invasion NS Yes Nég No Tam

Kulkarni et al. [27] 2012 70 No NS Subareolar NS FNAC Mastectomy ALND IPC + DCIS NS NS NS No NS

Kumar et al. [28] 2017 53 No No Subareolar NS FNAC Mastectomy ALND IPC + IDC NS Yes Nég No NS

Levine et al. [29] 2002 60 NS NS NS US FNAC NS NS Pure IPC 3 NS NS NS NS

Luo et al. [30] 2020 70 NS No Subareolar US+ MG Excision biopsy Mastectomy SLNB Pure IPC NS Yes Nég No Tam

Author	Year	Age	Discharge	Pain	Location	Imaging	Method of diagnosis	Surgery	Axillary staging	Final pathological diagnosis	Grade IPC	ER and/or PR	HER2	Positive nodes	Adjuvant therapy
Agrawal et al. [5]	2017	52	Yes	Yes	Subareolar	US	FNAC	Lumpectomy	No	Pure IPC	NS	Yes	Pos	NS	NS
Akagi et al. [6]	2009	70	NS	NS	NS	US	CNB	Lumpectomy	No	Pure IPC	2	Yes	Pos	NS	Tam
Al Salloom et al. [7]	2015	53	NS	No	NS	MG	FNAC + CNB	Mastectomy	ALND	Pure IPC	2 + 3	Yes	Nég	No	NS
Anan et al. [8]	2000	75	NS	No	Subareolar	US+ MG	FNAC	Mastectomy	ALND	Pure IPC	NS	NS	NS	No	NS
Andres et al. [9]	2003	74	NS	No	Retroareolar	US+ MG	FNAC	Lumpectomy	No	Pure IPC	NS	NS	NS	NS	No
Arora et al. [10]	2010	81	NS	NS	Subareolar	NS	NS	Mastectomy	No	IPC + invasion	NS	Yes	Nég	NS	NS
Balsa-Marína et al. [11]	2005	66	NS	No	Lateral	US+ MG	Lumpectomy	Lumpectomy	No	Pure IPC	NS	Yes	Nég	NS	Rth + Tam
Brahmi et al. [12]	2009	50	NS	NS	Retroareolar	US+ MG + MRI	Lumpectomy	Mastectomy	ALND	IPC + DCIS	2	Yes	NS	No	No
Başara Akın et al. [13]	2019	72	NS	No	Retroareolar	US+ MG	CNB	Mastectomy	No	Pure IPC	NS	Yes	Nég	NS	NS
De rosa et al. [14]	1992	70	NS	NS	NS	US	Lumpectomy	Lumpectomy	ALND	IPC + invasion	NS	NS	NS	No	NS
Downing et al. [15]	2014	74	No	NS	Subareolar	US+ MG	CNB	Mastectomy	SLNB	Pure IPC	3	Yes	Pos	No	No
Hariprasad S. et al. [16]	2013	50	NS	No	Subareolar	US	FNAC	Mastectomy	No	Pure IPC	2	Yes	NS	NS	No
Hu et al. [17]	2016	59	Yes	NS	Lateral	US+ MG	FNAC	Mastectomy	SLNB	Pure IPC	1	Yes	Nég	No	Tam
Hussain et al. [18]	2009	58	No	No	NS	US	CNB	Mastectomy	SLNB	IPC + invasion	2	Yes	Nég	No	Tam
Imoto et al. [19]	1998	62	NS	NS	Subareolar	MG	FNAC	Lumpectomy	No	Pure IPC	1	NS	NS	NS	No
Inoue et al. [20]	2003	72	Yes	NS	Retroareolar	US	Discharge cytology	Lumpectomy	No	Pure IPC	NS	Yes	NS	NS	No
Jeffrey et al. [21]	1994	81	NS	NS	Subareolar	NS	FNAC	Mastectomy	ALND	Pure IPC	NS	NS	NS	No	NS
Johnson et al. [22]	2008	70	No	No	Subareolar	US+ MG	CNB	Mastectomy	SLNB	Pure IPC	2	Yes	Nég	No	NS
Kelessis et al. [23]	2011	61	Yes	No	central	MG	Discharge cytology	Mastectomy	ALND	Pure IPC	NS	Yes	NS	No	Tam
Kihara et al. [24]	2004	68	No	No	Subareolar	US+ MG + MRI	FNAC	Mastectomy	ALND	Pure IPC	NS	Yes	NS	No	Tam
Kinoshita et al. [25]	2005	71	Yes	NS	Retroareolar	US+ MG	CNB	Mastectomy	No	Pure IPC	3	Yes	Nég	NS	No
Kinoshita et al. [26]	2018	64	NS	NS	Subareolar	US	CNB	Mastectomy	SLNB	IPC + invasion	NS	Yes	Nég	No	Tam
Kulkarni et al. [27]	2012	70	No	NS	Subareolar	NS	FNAC	Mastectomy	ALND	IPC + DCIS	NS	NS	NS	No	NS
Kumar et al. [28]	2017	53	No	No	Subareolar	NS	FNAC	Mastectomy	ALND	IPC + IDC	NS	Yes	Nég	No	NS
Levine et al. [29]	2002	60	NS	NS	NS	US	FNAC	NS	NS	Pure IPC	3	NS	NS	NS	NS
Luo et al. [30]	2020	70	NS	No	Subareolar	US+ MG	Excision biopsy	Mastectomy	SLNB	Pure IPC	NS	Yes	Nég	No	Tam

Table 1 (Continued).

Author	Year	Age	Discharge	Pain	Location	Imaging	Method of diagnosis	Surgery	Axillary staging	Final pathological diagnosis	Grade IPC	ER and/or PR	HER2	Positive nodes	Adjuvant therapy
Luo et al. [30]	2020	67	No	No	Subareolar	US+ MG	Excision biopsy	Mastectomy	SLNB	IPC + invasion	NS	Yes	Nég	No	Tam
Luo et al. [30]	2020	76	NS	No	Retroareolar	US+ MG	Excision biopsy	Mastectomy	No	Pure IPC	NS	Yes	Nég	NS	No
Mok et al. [31]	2018	89	NS	NS	NS	US+ MG	Excision biopsy	Mastectomy	SLNB	Pure IPC	1	NS	NS	No	No
Muallaoglu et al. [32]	2012	48	NS	Yes	Retroareolar	US	Lumpectomy	Lumpectomy	No	Pure IPC	NS	NS	NS	NS	No
Niikura et al. [33]	2010	70	No	No	Retroareolar	US+ MG	Excision biopsy	Lumpectomy	SLNB	IPC + DCIS	NS	Yes	Nég	No	Rth
Paccelli et al. [34]	2002	67	NS	No	Lateral	US+ MG	CNB	Mastectomy	SLNB	Pure IPC	NS	NS	NS	No	No
Pandey et al. [35]	2010	50	Yes	No	Subareolar	US	FNAC	Lumpectomy	No	Pure IPC	NS	NS	NS	NS	No
Romics et al. [36]	2009	44	NS	NS	Subareolar	US+ MG	FNAC + CNB	Mastectomy	SLNB	Pure IPC	NS	Yes	NS	No	Rth
Shukla et al. [37]	2010	65	NS	NS	NS	US	FNAC	Mastectomy	ALND	IPC + IDC grade 2	NS	Yes	Nég	3/7 invaded	NS
Singh et al. [38]	2020	40	Yes	NS	Subareolar	US	FNAC	Mastectomy	ALND	IPC + invasion	NS	Yes	Nég	No	Tam
Sinha et al. [39]	2006	75	NS	No	latéral	US	FNAC	Lumpectomy	No	Pure IPC	1	NS	NS	NS	No
Sonksen et al. [3]	1996	62	NS	No	Retroareolar	US+ MG	FNAC	Mastectomy	ALND	IPC + DCIS	NS	NS	NS	No	No
Stolnicu et al. [40]	2018	75	Yes	NS	NS	NS	CNB	Mastectomy	SLNB	IPC + DCIS	NS	Yes	Nég	subcapsular tumour cells	Rth + Tam
Tochika et al. [41]	2001	66	NS	Yes	Subareolar	US+ MRI	FNAC	Mastectomy	ALND	IPC + invasion	NS	Yes	Nég	NS	Tam
Vagholkar et al. [42]	2013	55	Yes	NS	Subareolar	NS	FNAC + Cytology discharge	Lumpectomy + mastectomy	ALND	IPC + invasion	NS	Yes	NS	No	NS
Yilmaz et al. [43]	2018	63	NS	No	Subareolar	US+ MG + MRI	CNB	Mastectomy	SLNB	Pure IPC	2	Yes	NS	No	NS
Yoshida et al. [44]	2010	64	No	Yes	Subareolar	US+ MG	FNAC	Lumpectomy	ALND	IPC + invasion	NS	Yes	Nég	No	Tam

Abbreviations: NS: not specified; CNB: core needle biopsy; FNAC: fine needle aspiration cytology; US: ultrasonography; MG: mammography; MRI: magnetic resonance imaging; SLNB: sentinel lymph node biopsy; ALND: axillary lymph node dissection; IPC: intracystic papillary carcinoma; DCIS: ductal carcinoma in situ; IDC: invasive ductal carcinoma; Tam: tamoxifen; Rth: radiation therapy.

Because of its rarity, there are no clear guidelines for its management. Surgery remains the cornerstone of treatment, and mastectomy or lumpectomy may be considered. However, given the low rate of recurrence locally and at a distance, lumpectomy may be the treatment of choice [50]. Moreover, the study by Mogal et al. is one of the largest series on IPCs in women, where an equivalent survival rate for lumpectomy versus mastectomy was noted, independent of radiotherapy [51]. In our review, 30/43 (70%) underwent a mastectomy, and 12/43 (30%) experienced a lumpectomy.

Even in the case of an invasive IPC, the prognosis remains excellent, and IPC is very rarely associated with lymph node invasion. Some authors, such as Wang et al., have recommended not to perform a systematical SLNB [52]. Other authors, such as Mogal et al. and Grabowski et al., have affirmed that patients with lymph node metastases (8% to 14%) have a poorer prognosis and therefore recommend a systematic SLNB [50,51]. Nevertheless, all authors have agreed that systematic axillary lymph node dissection should not be performed. In our review, 15/43 (35%) had axillary lymph node dissection, and 13/43 (30%) had a SLNB.

There are no guidelines for adjuvant treatments, such as radiation or hormone therapy, and the only powerful studies have been done in women. Even in its pure form, an IPC has a potential for metastasis and local recurrence that should not be overlooked [51,53]. The study by Solorzano et al. involved 40 patients, 12 of whom received radiotherapy, and concluded that it did not affect recurrence-free survival or overall survival [54]. In this study and in the study by Fayanju et al., the vast majority of radiotherapy indications were for invasive IPCs and IPCs associated with a DCIS, regardless of the type of surgery [55].

The much larger study by Mogal et al., which involved 2,649 female patients with IPC, 897 of whom had received radiotherapy, verified that survival was significantly improved with radiotherapy. Nonetheless, many patients were offered hormone therapy. Discerning the influence of hormone therapy on radiotherapy was difficult, and unfortunately, this was not supported in the study [51].

The place of hormonal therapy remains less clear. In invasive cancer, the benefit of hormone therapy on survival is clear, whereas in a DCIS, it reduces the risk of bilateral recurrence but does not decrease mortality [56]. Concerning IPC, it will depend whether it is considered an invasive or in situ. Fayanju et al. recommended hormone therapy in women under 50 years old with a pure IPC or an IPC combined with invasion or a DCIS [55]. Wynveen et al. also considered radiotherapy and hormone therapy in all cases [46]. These studies involved only a small number of cases, and chemotherapy is not recommended by any of the studies. In our review, 13/29 (45%) had no adjuvant treatment, 4/29 (14%) had radiation therapy, and 13/29 (45%) had hormone therapy.

The study by Giordano et al. published in the BMJ affirmed the tendency to under-treat breast cancers in men and suggested treating them in the same way as women [57]. The dropout rate from Tamoxifen due to side effects is similar with an order of 20% in men and 21% in women [58,59]. If hormone therapy is considered, then tamoxifen should be preferred, and if contraindicated, a combination of an aromatase inhibitor and a GnRH analogue should be used [57,60].

In our clinical case, we decided to administer chemotherapy, right axillary radiotherapy, and hormonal therapy because of the associated grade 2 IDC and tumor emboli within the capsule of right SLNB.

4. Conclusion

IPC is a rare tumor with a good prognosis despite the ongoing debate on its histological nature, and it should nevertheless be considered an invasive carcinoma. Whether in its pure or invasive form, the survival rate appears to be similar, and there are no clear guidelines for its management. The different treatments proposed in the literature for IPC in men are based on an extrapolation of those proposed for women. Conservative surgery should be preferred, and a SLNB should be performed systematically. Radiotherapy should also be proposed in the case of conservative surgery, and hormone therapy could be proposed in the case of an invasive IPC or an IPC associated with a DCIS.

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