Abstract

Objective. Small series and individual cases of penile soft tissue tumours are reported in the literature: these are rare tumours that represent less than 5% of all penile tumours.
Methods. Penile soft tissue tumours were collected from the archive of the Department of Pathology at the Istituto Nazionale dei Tumori of Milan between January 1990 and October 2021. All available medical records were retrieved and reviewed to obtain clinical information.
Results. Our series refers to the 30-year experience of highlighting the heterogeneity in the presentation and microscopic features of these rare sarcomas. 18 penile soft tissue tumours are described, 4 benign and 14 malignant. The mean age at diagnosis was 58.2 years (range 24-96 years) and 53.6 years among malignancies (range 24-89). The most frequent histotype was Kaposi’s sarcoma (nr = 4) and very unusual histotypes were observed, namely low-grade fibromyxoid sarcoma, synovial sarcoma, proximal type epithelioid sarcoma and the first reported case of dedifferentiated liposarcoma of the penis.
Conclusions. Among sarcomas of the genitourinary tract, tumours of the soft tissues of the penis are the rarest. Penile sarcomas can present at a young age. Kaposi’s sarcoma in HIV-negative patients has a favorable outcome, while deep sarcomas have an aggressive behavior and poor prognosis.

Introduction

Neoplasms of the penis constitute approximately 0.5% of all malignant neoplasms in the United States and Europe. Mesenchymal malignancies are rare, comprising less than 5% of all penile tumours ¹. Few case reports and small case series over a long time span addressed this issue. Changing classification criteria and evolving therapies are reasons of even greater difficulties in interpretation of data., The 4^th Edition of WHO Classification reported the Armed Forces Institute of Pathology (AFIP) data collected between 1970 and 1999 ², on 116 soft tissue tumours of the penis, with Kaposi sarcoma (KS) being the most common ³.

In this study we report 18 soft tissue tumours of the penis (4 benign, 14 malignant) collected between 1990 and 2021 at Istituto Nazionale Tumori of Milan (INT) in adult males, focusing on their clinicopathologic features and outcomes.

Materials and methods

Penile soft tissue tumours were collected from the archive of the department of Pathology at INT between January 1990 and October 2021, which included hospitalized cases from the Urology Unit at INT, and and outpatient men sent for second opinion. Histological reports and tissue slides were reviewed by a senior author (MC). Ethical approval for the study was obtained and informed consensus was gathered in all cases for patients admitted to INT. All available medical records (discharge letters, outpatient visits and radiological reports) were retrieved and reviewed to obtain age at diagnosis, clinical presentation, prior history of neoplastic diseases, serological HIV status in KS, treatment, local relapses, presence of lymph nodal or distant metastases at time of diagnosis or during follow-up, overall and disease-free survival. Follow-up was censored in December 2022. Penile localisation of metastatic sarcomas with extra-penile primary sites was excluded. Particular attention was paid to re-evaluate the original diagnoses, in order to check that they were all uptodated according to the latest WHO classification ⁴. Clinical and pathological reports and available slides were reviewed in order to collect the following informations: type of surgery, gross description, tumour size, tumour location (root/shaft/foreskin/glans), results of immunohistochemical and molecular studies (when available), and resection margin status of surgical specimens. Neoplasms were classified as either superficial or deep infiltrating. Deep infiltration was defined as neoplastic infiltration of either the corpora spongiosum and/or cavernosum.

Statistical analysis was performed with IBM SPSS Statistics Data Editor v. 23 to calculate a Kaplan-Meier curve that compares the survival between patients with either superficial or deep neoplastic infiltration, respectively.

Results

Among 1,150 penile neoplasms diagnosed and recorded between January 1990 and October 2021 at the Pathology Department of the INT, we selected 18 (1.5%) primary penile soft tissue tumours, after the exclusion of two metastatic sarcomas (one GIST and one spindle cell sarcoma, NOS). Clinical available data are summarised in Table I. Mean age at diagnosis was 58.2 years (range 24-96 years), and 53.6 years among malignant tumours (range 24-89), while for the 4 benign tumours (hemangiomas) age range at diagnosis was 60-96 years (mean 74.5). Follow-up was highly variable in the 10 malignant cases followed at the INT: from 7 to 217 months (mean 83.4 months). Four patients had a history of a previous malignancy. Serological HIV status was available in two KS and it was negative. The mean size of the lesions was 3.95 cm (range 0.8 cm-10 cm). The location of the penile sarcomas was known in 16 cases: glans was affected in 8 cases (in 2 with involvement of the foreskin and in one with the shaft), root of penis in 5, shaft only in 2 cases, foreskin in one case, while two cases had unknown primitive site. The therapeutic procedure varied greatly and depended on the location, histotypes, and age of the patient. In those who underwent surgery with radical intent, the resection margins were free of neoplasms in all cases except one. The latter was initially treated with local excision, and subsequently radicalised with partial penectomy. Only two cases were treated with total penectomy (one including nodal dissection), one with partial penectomy, 12 with biopsies, either incisional (3) or excisional (9). As many as 4 cases had pathological review only and clinical data were lacking. After a median follow-up of 9 months, 7 patients relapsed after 2 to 68 months.

According to histology, the most frequent were Kaposi sarcoma. The immunohistochemical results of these cases and of the other neoplasms are summarised in Table II. KS was diagnosed in 4 cases (aged 40 to 77), of whom 2 were treated in our institution. The first showed multiple localisations on the prepuce and shaft, all of which were treated only with local exeresis. The second, after suffering from Hodgkin’s lymphoma and prostate adenocarcinoma, had a first KS on the knee; the following years were characterised by multiple and widespread recurrences with penile involvement.

The second most frequent entity in the present series was proximal-type epithelioid sarcoma ⁵. Three cases were diagnosed at ages of 24, 35 and 59 years. The first two were located at the root of the penis with infiltration of the corpora cavernosa, with a maximum diameter of 6 cm and 4.5 cm respectively, whereas the third case was located on the foreskin (dimensions not available). All the lesions showed loss of nuclear INI1/SMARCB1 expression. The tumour involved the visceral structures of the penile root (predominantly the corpora cavernosa) with an intact overlying skin. Deaths occurred at 7 and 88 months in the first and second cases with disseminated disease, while the third case was lost to follow-up. The case of angiosarcoma occurred in a 69-year-old man with a nodule of the balanopreputial sulcus with diagnosis of epithelioid angiosarcoma on biopsy. He presented in INT with two nodules of the shaft, 7 mm and 8 mm, adjacent to the corpora cavernosa, and underwent chemotherapy and a radical penectomy with bilateral inguinal lymphadenectomy. A 9 mm nodule with a hard consistency was observed on the dorsal side of the shaft, showing the features of epithelioid angiosarcoma (Fig. 1). At the last FU he was alive with no evidence of disease (NED). Two cases were classified as sarcomas with myogenic differentiation: a 47 years old male with a history of fibroblastic osteosarcoma of the left tibia, and a 63-years-old man with recurrent glans carcinoma in situ. The histological examination was characterized by solid proliferation of cells with high-grade atypia, spindle and pleomorphic, mitotically active (mitoses between 10 and 20/10HPF), in sclero-hyaline stroma with focal necrosis. None of the cases showed a pattern of recognisable leiomuscular growth and the diagnosis was sarcoma with myogenic differentiation, grade 3 and grade 2, respectively, according to FNCLCC ⁶. The patient with G3 sarcoma died 52 months later after surgery, and the other patient is alive without disease (36 months follow-up). A case of dedifferentiated liposarcoma occurred in an 89-year-old man with a 4-cm lesion at the root of the penis that extended along the shaft with infiltrating characteristics on CT scan (Fig. 2) and hyper-capturing on PET-FDG. On biopsy the lesion showed atypical, pleomorphic and spindle cells, with diffuse growth, rare mitoses, absence of necrosis, with expression of vimentin, actin 1A4, desmin, calponin, and MDM2 amplification confirmed by FISH. A diagnosis of dedifferentiated liposarcoma with myogenic differentiation was made (Fig. 3 a-b). At the last follow-up the patient had metastases to the lung. A patient with a previous epithelioid haemangioendothelioma of the penis was referred to INT for the presence of nodular formations, one on the dorsal surface of the penis (2 cm) and another on the ventral surface (0.5 cm) in close proximity to the corpora cavernosa: CAMTA1 positivity confirmed the diagnosis of epithelioid haemangioendothelioma in the bioptical samples. During follow-up further local recurrences of the disease occurred.

In two consultation cases, a case of synovial sarcoma (SS) and a case of fibromyxoid sarcoma, we had limited access to the clinical history and histological materials consisting in H&E and some immunostains. SS occurred as a painful penile mass in a 27-year-old man on the right side of the penis. Magnetic resonance imaging (MRI) showed a dishomogeneous oval lesion close to the right corpus cavernosous, measuring 2.6 cm in diameter. Complete enucleation of the tumour was performed, and the diagnosis was synovial sarcoma, as reported in the case published in 2002 ⁷. This patient was lost to follow-up. The second case, provided by an external hospital from North-East Italy, occurred in a 44 years-old man in the root of the penis in a periurethral site. Based on a morphological and molecular study that showed the translocation of the FUS gene in 16p11 by FISH, a diagnosis of low-grade fibromyxoid sarcoma was made. Among the 14 malignant neoplasms, eight cases (57.1%) involved the sub-cutaneous tissue of the prepuce and superficial tissue of the shaft below the Dartos fascia, while six cases (42.9%) involved deep tissues of the glans with involvement of the corpus spongiosum or the shaft. Deep neoplastic infiltration was more frequently observed among patients who died of disease, with a trend towards statistical significance of the Kaplan-Meier curve (p = 0.073; Kaplan-Meier curve is shown as supplementary material n. 1).

Discussion

Our series refers to all cases of penile sarcoma evaluated over 31-years, and to our knowledge this is one of the largest single institutional series on penile soft tissue tumours. The frequency of the histotypes of penile sarcomas differs from those occurring in other sites ^1,4,8. Benign neoplasms usually present with painless nodules, while penile sarcomas are frequently deep lesions occurring with urinary obstruction and priapism ⁴. They represent approximately 1/3 of the AFIP registry, which collects cases from 1970 to 1999, where KS is reported as the most frequent penile sarcoma ⁴. In the California Cancer Registry ⁹, the prevalence of KS compared with all penile cancers was reported to be 7.4% in the period 1988-1995 decreasing to 1.7% in the period 1995-2004. HHV8-associated penile primary sarcoma had a peak incidence in the years of maximum HIV diffusion, a trend conditioned both by the degree of immunosuppression and by the patient’s other possible comorbidities, with a 32.8% 5-year survival rate. This contrasts with the series of Dehner and Smith and the present study, where no deaths were documented. Apart from the association between KS and HHV-8 infection, and a post-radiotherapy penile angiosarcoma ¹⁰, knowledge of possible associated external factors is scarce. Differential diagnosis between benign and malignant tumours is sometimes difficult particularly in vascular neoplasms. Epithelioid hemangioendothelioma of the penis was reported in 22 cases, of which 19 were case reports and 3 were reported by Dehner ^3,11-26. The affected sites were the glans, corpora cavernosa, root of the penis, and subcutaneous tissues: three patients developed metastases and two of them died of the disease, while local recurrence was more frequent; in most cases the course was favourable with a documented disease-free interval of up to 5 years. Most authors agree on treatment based on local excision in small cases, followed by follow-up ¹¹. Some tumours are characterised by the presence of the SERPINE1-FOSB fusion gene, demonstrated by PCR but also by immunohistochemical expression of FOSB ²⁷. In our case the lesion was localised to the root of the penis, the patient underwent local excision and he is alive without disease. The only angiosarcoma observed as a recurrence in the shaft of the penis can be easily differentiated from an anastomosing haemangioma, which has the genitourinary tract, in particular the kidney ²⁸, the retroperitoneum and the paraspinal region as its preferential sites. The differential diagnosis is based on morphology, but cellular atypia and infiltrative growth are missing, the vessels are well formed and can be thrombosed, in addition to the possible presence of extramedullary hematopoiesis ^28-30. Another mimicker of benign lesions is the epithelioid sarcoma (ES), which clinically overlaps with Peyronie’ s disease ³¹. This entity was first described in 1970 by Enzinger ³², while one of the cases reported in his series by Dehner ³, a 35-year-old man diagnosed with “fascial sarcoma,” was a true ES as quoted by Rossi ³¹. Clinical history begins more than 5 years before the diagnosis in the majority of ES. The tumour is characterised by slow growth, and when the lesion is located at the root or shaft of the penis, it causes focal induration and deviation associated with pain during erection. In cases subjected to biopsy, the morphological appearance is characterised by large epithelioid elements with granulomatous-like growth, sometimes necrotizing, often overlooked simulating Peyronie’s disease (Fig. 4 a-d) ³³. Unlike the latter, sarcomatous lesions fail to respond or relapses following Peyronie’s therapy, increasing in size by infiltrating and replacing the surrounding tissue, and causes urinary symptoms ³⁴. An alteration described in over 90% of cases of ES ³⁵ of both variants is the loss of expression of the protein INI1/SMARCB1. Epithelioid features of this entity could be misdiagnosed as squamous cell carcinoma ³⁶. Nodular lesions occurring in young males that grow on the root or shaft and affect the corpora cavernosa and/or spongiosa, without involvement of the epithelium, make epithelial origin unlikely. Unfavourable parameters are deeper locations (i.e., corpora cavernosa invasion), larger size, higher tumour stage, and the proximal subtype ⁶. We have reported two cases of sarcoma with myogenic differentiation not attributable to any mature tissue, mainly consisting of spindle-shaped and pleomorphic elements expressing one or more muscular markers: according to the WHO, to make a diagnosis of leiomyosarcoma, areas with leiomuscular morphology must be present, at least focally ⁴. Leiomyosarcoma represents 5-6% of cases in Dehner’s series ³ and the most numerous series is the one already described by Fetsch ³⁷. The neoplasm affects any age, but most cases are in the fourth and fifth decades of life. Prognosis appears to be related to the lesion size. Then we have reported the first occurrence of penile liposarcoma, which is also the most common malignant mesenchymal neoplasms in the genitourinary system, with frequent occurrence in the paratesticular soft tissues ^38-42. However, no cases have yet been described in the penis, and the presence of adipose tissue in the penile fascia (Buck’s fascia) lining the corpora cavernosa and in the tunica albuginea in penectomy samples ⁴³ in correspondence with the glans penis and penile shaft has been documented in a percentage ranging between 19% and 53%. The adipocytic neoplasia in our case led us to consider the presence of adipose tissue in the root of the penis. The differentiated component with myogenic differentiation observed in the biopsy can justify the metastatic onset with localisation to the lung, considering the aggressive biological behaviour of this morphology ⁴⁴. The other rare cases reported were synovial sarcoma and low-grade fibromyxoid sarcoma, but we lack information regarding the outcomes, because they were sent for a second opinion. About the predictive factors of relapse, Dotan reported in an analysis of 131 sarcomas of genitourinary tract, significant differences in disease-specific survival both between the group of patients who underwent or who did not undergo surgery, and among those with resection margins affected or not affected by the tumour ³⁸. By comparing patients’ prognosis to the depth of tumoural infiltration, 6 cases (46.1%) involved deep tissues of the glans and shaft, where tumours involving the corpus cavernosus or corpus spongiosum were considered deep and tumour-related death was significantly associated with deep extension. Some bias affects the selection of the cases: the most important being almost total absence of benign tumours, excluding vascular neoplasms, that are not referred to a center for treatment of soft tissue sarcomas. Another problem common to many other rare tumours is the absence of therapies other than surgery. Need for other cases delucidating the behavior and best practice to treat these patients is a compelling issue for the rarest among rare penile tumours.lude a review of the key literature. If there are relevant controversies or disagreements in the field, they should be mentioned so that a non-expert reader can delve into these issues further. The discussion should consider the major conclusions of the work along with some explanation and/or speculation on their significance. How do the conclusions affect the existing assumptions and models in the field? How can future research build on these observations? What are the key experiments that remain? The discussion should be concise with solid arguments.

Conclusions

Among sarcomas of the genitourinary tract, tumours of the soft tissues of the penis are the rarest. Penile sarcomas can present at a young age. This single-institutional case series does not allow useful conclusions to be drawn for their clinical management due to the heterogeneity of the histotypes. Kaposi’s sarcoma in HIV-negative patients has a favourable outcome, while deep sarcomas have an aggressive behaviour and poor prognosis.

CONFLICT OF INTEREST STATEMENT

The authors declare no conflict of interest.

FUNDING

None

AUTHORS’ CONTRIBUTIONS

Study concept and design: MC and GMP. Acquisition of pathology data: MC and SS. Supply of clinical data: NN and SS. Analysis and interpretation of data: MC, GMP. Drafting of the manuscript: MC, GMP, SS. Statistical analysis: GMP. Administrative, technical and material support: SS. Critical revision of the manuscript for important intellectual content and supervision: MC, GMP, SS, NN, GP.

ETHICAL CONSIDERATION

The research was conducted ethically, with all study procedures being performed in accordance with the requirements of the World Medical Association’s Declaration of Helsinki.

Figures and tables

Figure 1.Epithelioid angiosarcoma: (A) nodule observed on the dorsal side of the shaft in the lamina propria (H&E stain); (B) Vascular proliferation stained by CD31.

Figure 2.Dedifferentiated liposarcoma: CT scan showing a 4-cm lesion at the root of the penis infiltrating the surrounding tissues.

Figure 3.Dedifferentiated liposarcoma: (A) atypical, pleomorphic and spindle cells in bioptical sample (H&E stain); (B) the cells show MDM2 nuclear immunostaining.

Figure 4.Proximal-type epithelioid sarcoma: (A) low magnification image of incisional biopsy of epitheliod sarcoma of the shaft of the penis showing a multinodular growth pattern of epithelioid cells; (B-C-D) higher magnification of epithelioid elements sometimes necrotising, showing pleomorphic tumour cells with deep eosinophilic cytoplasm and enlarged vesicular nuclei with prominent nucleoli (carcinoma-like). These features are typical of proximal-type epithelioid sarcoma.

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