Tumour-to-tumour metastases: prostate carcinoma metastasising to a renal oncocytoma

Abstract

This is a case report of prostate carcinoma metastasising to a renal oncocytoma. The report demonstrates the unusual presentation of metastases from a common cancer to a common benign tumour, and reviews the rare phenomenon of tumour-to-tumour metastases.

Background

Tumour-to-tumour metastases are rare but the histopathologist should be aware of this phenomenon in order to correctly identify morphologically divergent areas within a tumour and keep an open mind to the possibility of this phenomenon especially when there is a history of concurrent or previous malignancies.

For both the clinician and the histopathologist this phenomenon highlights the need for comprehensive history taking and good communication of this information between disciplines.

Case presentation

A 74-year-old man was found to have a left upper pole renal mass on ultrasound scan while being investigated for an episode of asymptomatic haematuria. His significant medical history included metastatic prostate carcinoma (bone involvement only) that was under hormonal control with diethlystilboestrol (prostate specific antigen (PSA) 23.99 ng/ml).

Investigations

A contrast-enhanced CT scan confirmed the presence of an exophytic mass with central necrosis arising from the anterior aspect of the mid-portion of the left kidney. Radical nephrectomy was performed.

Examination of the fixed organ showed a mid-zone well-circumscribed tumour measuring 7.2 cm in maximum dimension. The tumour had a brown homogeneous appearance. An area of central scarring was identified but no necrosis was seen (contrary to the CT scan). Three hilar lymph nodes were identified and sampled.

Microscopic examination revealed a well-circumscribed unencapsulated tumour composed of nests, sheets, acini and tubules of uniform round to polygonal cells with central, round regular nuclei, small nucleoli and eosinophilic granular cytoplasm. No nuclear atypia, mitoses or necrosis was seen. The central scar-like area was composed of paucicellular, oedematous stroma. There was no central necrosis. The lesion merged with the adjacent surrounding normal renal parenchyma. There was bulging of the tumour into the surrounding perinephric fat.

Immunohistochemistry showed the lesion to be diffusely positive for E-cadherin and CK8/18 with patchy positivity for epithelial membrane antigen (EMA), CD117, CD15, CK7 and vimentin. The tumour was negative for CK20, PSA, renal cell carcinoma (RCC) Ag and CD10 and the proliferation index, as estimated by Ki67, was low (<2%). The morphological features were consistent with a renal oncocytoma.

In addition, there were multiple microscopic foci admixed with the main lesion that showed acini and fused, cribriform glands composed of markedly atypical cells which appeared morphologically different from the main lesion. Immunohistochemistry showed these foci to be diffusely positive for CK8/18, PSA and E-cadherin, patchy positivity for CD15 and scattered cells positive for EMA and CK7. These tumour cells were negative for CD117, CK20, RCC Ag and CD10. These tumour cells were also found within lymphovascular spaces within the kidney, in two of three hilar lymph nodes (with extracapsular spread) and as a separate nodular deposit in extranodal fat.

Outcome and follow-up

The morphological features and immunohistochemical profile was of foci of metastatic prostate adenocarcinoma within the parenchyma of the renal oncocytoma (figure 1), with further metastatic deposits in renal vasculature and hilar lymph nodes (figure 2).

Figure 1.

Renal oncocytoma with focus on metastatic prostate carcinoma. (A) H&E, (B) PSA, (C) Ki67 proliferation marker (all ×100 magnification). PSA, prostate specific antigen.

Figure 2.

Lymph node containing deposit of metastatic prostate carcinoma. (A) H&E, (B) PSA (all ×100 magnification). PSA, prostate specific antigen.

Discussion

Tumour-to-tumour metastasis is a rare phenomenon and should be separated from collision tumours (which describes where two primary, originally separate and histologically distinct tumours merge).

The definition of tumour-to-tumour metastasis was set out by Campbell et al¹ in 1968 and the criteria are

• More than one primary tumour must exist in the patient.

• The recipient tumour should be a true benign or malignant neoplasm.

• The metastatic neoplasm should be a true metastasis with established growth in the host tumour, not the result of contiguous growth (‘collision tumour’) or embolisation of tumour cells within the vessels.

• Tumours that have metastasised to the lymphatic system, where lymphoreticular malignant tumours already exist are excluded.

From the literature, the most common recipient is renal cell carcinoma and the most common donor tumour is pulmonary carcinoma.² A search of Pubmed revealed 114 case reports or case series of tumour-to-tumour metastases (table 1).

Table 1.

Although renal cell carcinoma is a common recipient neoplasm of a wide variety of metastatic carcinomas, benign renal neoplasms are far less commonly affected with only five cases of metastases to a renal oncocytoma

Recipient neoplasm	Donor neoplasm	Author, year
Renal cell carcinoma and tubular adenoma	Prostate adenocarcinoma	Majmudar, 19763
Renal cell carcinoma	Pulmonary adenocarcinoma	Shuangshoti, 19834
Renal cell carcinoma	Malignant melanoma	Singh et al, 19845
Renal cell carcinoma	3 separate cases	Sella, 19876
Renal cell carcinoma	Prostate adenocarcinoma	Tislavicz, 19917
Renal cell carcinoma	Prostate adenocarcinoma	Inatomi et al, 19968
Renal cell carcinoma	2 cases: Bronchial carcinoma	Sperb et al, 19969
Renal cell carcinoma	Basaloid squamous cell carcinoma of the tonsil	Khurana, 199710
Renal cell carcinoma	Cervical carcinoma	Petraki et al, 200311
Renal cell carcinoma	Pulmonary adenocarcinoma	Granville et al, 200512
Renal Cell Carcinoma	Pulmonary carcinoma	Sawada et al, 200913
Renal cell carcinoma	Neuroendocrine carcinoma	Duprez et al, 200914
Renal cell carcinoma	Gastric signet ring adenocarcinoma	Sakai et al, 201015
Renal cell carcinoma	Malignant melanoma (amelanotic)	Sayk et al, 201016
Chromophobe Renal cell carcinoma	Colorectal adenocarcinoma	Shin et al, 201117
Renal cell carcinoma	Pulmonary adenocarcinoma	Aggarwal et al, 20122
Renal angiomyolipoma	2 cases: Neuroendocrine carcinoma of the pancreas and pulmonary adenocarcinoma	Ricketts et al, 200818
Renal adenoma	Pulmonary squamous cell carcinoma	Popov et al, 200119
Renal oncocytoma	Bronchogenic carcinoma	Olsen et al, 198420
Renal oncocytoma	Pulmonary squamous cell carcinoma	Altinok et al, 199921
Renal oncocytoma	Breast carcinoma	Gassler et al, 200622
Renal oncocytoma	Breast carcinoma	Fox et al, 200923
Renal Oncocytoma	Prostate adenocarcinoma	*Horn et al, 201024
Meningioma	Prostate adenocarcinoma	Bernstein et al, 198325
Pituitary adenoma	Prostate adenocarcinoma	Ramsay et al, 198826
Follicular adenoma	Prostate adenocarcinoma	Ro et al, 199427
Meningioma	Prostate adenocarcinoma	Mitchell et al, 201128

Case reports, renal recipient neoplasm or prostate adenocarcinoma donor.

*Unpublished, poster presentation at College of American Pathologists 2010 Meeting.

Prostate carcinoma typically metastasises to the bone, and, in the setting of tumour-to-tumour metastasis, only seven case reports have been published where prostate adenocarcinoma was the donor tumour.

The mechanism of tumour-to-tumour metastases is not fully understood but it is hypothesised that highly vascular tumours could receive a large proportion of embolishment by another tumour making them likely recipient tumours.² The kidney is a highly vascular organ and many of the renal parenchymal tumours also show prominent vascularisation suggesting that this vascular theory is the probable explanation for the predominance of recipient renal parenchymal tumours in the tumour-to-tumour literature.

The identification of tumour-to-tumour metastases is dependent on the recognition of morphologically divergent areas within a tumour and the selection of appropriate immunohistochemical antibodies for identification of tumour islands of a separate origin. The histopathologist must keep an open mind to the possibility of tumour-to-tumour metastases especially when there is a history of concurrent or previous malignancies.

This case report demonstrates a case of metastatic prostate adenocarcinoma to a renal oncocytoma and highlights this rare phenomenon. Given the propensity for tumour-to-tumour metastases to occur in renal tumours, it is advisable that urological histopathologists and urologists are aware of the phenomenon so that an adequate clinical history of malignancies can be provided that could guide the histopathologist to the diagnosis, should they encounter a renal tumour with atypical morphology.

Learning points.

• Tumour-to-tumour metastases are a rare phenomenon but should be considered when there are morphologically divergent areas within a tumour and there is a history of concurrent or previous malignancies.

• Tumour-to-tumour metastases are not collision tumours and are defined by Campbell's four criteria.

• Current theories of the mechanism of tumour-to-tumour metastases centre on the vascularity of recipient tumours and their ability to receive a significant load of tumour emboli.