ORIGINAL ARTICLES

Metastases to the Kidney: Eleven Cases Diagnosed by Aspiration Biopsy With Histological Correlation Shah Giashuddin, M.D., Joan Cangiarella, and Pascale Hummel Levine, M.D.*

M.D.,

Paul Elgert,

Metastases to the kidney from extrarenal primary tumors are uncommon and may mimic renal-cell carcinoma clinically when presenting as a single mass with hematuria. Fine-needle aspiration biopsy (FNAB) is a useful diagnostic method for the evaluation of primary renal tumors. Only a few studies have investigated the value of cytological evaluation of secondary renal tumors. We report our experience with these tumors. Eleven cases of extrarenal primary tumors metastatic to the kidney, diagnosed by aspiration biopsy with histological correlation, are discussed. The diagnosis of metastatic disease to the kidney was accurately made by aspiration biopsy. Knowledge of the patients’ history, histological correlation with the primary tumor, and the radiological characteristics of the renal masses were helpful in achieving a correct diagnosis. FNA cytology (FNAC) is an accurate method for the diagnosis of tumors metastatic to the kidney. Distinction between primary and secondary tumors of the kidney is crucial to guide management and prevent unnecessary surgery. Diagn. Cytopathol. 2005;32:325–329. '

2005 Wiley-Liss, Inc.

Key Words:

FNAC; kidney; secondary tumor; metastasis

The initial study of metastases to the kidney from extrarenal tumors included bronchogenic carcinomas and lymphomas as the most common primary malignancies.1 Subsequently, autopsy studies have shown that the kidney is the fifth most-common site of metastasis occurring in up to 20% of patients dying of disseminated disease with lung, breast, and gastrointestinal tract comprising the common primary sites.2–4 In contrast, clinicopathological studies of tumors metastatic to the kidney during life are rare because renal metastases often are clinically occult.5

New York University and Bellevue Hospital Center, New York, New York *Correspondence to: Pascale Hummel-Levine, M.D., New York University Medical Center, 530 First Ave., Skirball, Suite 10U, W. Tower, New York, NY 10016. E-mail: [email protected] Received 21 June 2004; Accepted 29 November 2004 DOI 10.1002/dc.20243 Published online in Wiley InterScience (www.interscience.wiley.com). '

2005 WILEY-LISS, INC.

C.T. (A.S.C.P.),

Thus, although the role of fine-needle aspiration (FNA) biopsy in the evaluation of newly appearing renal masses is essential in the management of patients with a previous history of malignancy, there are only a few reports describing tumors metastatic to the kidney in the cytological literature.6–12 We report the clinical and pathological features of eleven secondary tumors of the kidney accurately diagnosed by fine-needle aspiration biopsy (FNAB). We also review the literature on aspiration biopsy of renal metastases and compare it with our results.

Materials and Methods The Cytopathology files at New York University-Bellevue Hospital Centers were searched for cases of secondary tumors metastatic to the kidney diagnosed by FNAB. Eleven patients were identified, excluding primary renal tumors and cases without prior or subsequent histological material available for review (five patients). All FNABs were performed by a radiologist under CT or ultrasound guidance using 22-gauge 3-inch spinal needles. Aspirated material was smeared, air-dried, and stained with a modified Giemsa stain (Diff-Quik [DQ]; Baxter Scientific Products, McGaw Park, IL), Ultrafast Papanicolaou, or hematoxylin and eosin stain. A cytotechnologist was present at all procedures for the assessment of adequacy. Additional material, when present, was processed for a cell block. Immunohistochemistry (IHC) was performed in three of five cases using the cell block material and an automated immunostainer, NexES (Ventana Medical Systems, Tucson, AZ), by a modified avidin-biotin peroxidase technique. Monoclonal antibodies included L26, CD3, CD15, CD30, epithelial membrane antigen (EMA), thyroid transcription factor (TTF) 1, synaptophysin, and chromogranin (Ventana Medical Systems). Immunoglobulin gene rearrangement analysis was obtained from formalin-fixed paraffin-embedded tissue in one case. For Diagnostic Cytopathology, Vol 32, No 6

325

GIASHUDDIN ET AL. Table I.

Clinical, Cytological, and Histopathological Data of 11 Patients with Metastatic Tumors to the Kidney

Case/age/sex 1/83 M 2/69 F 3/48 M 4/41 M 5/54 F 6/82 F 7/62 F 8/30 M 9/65 M 10/44 M 11/55 F

Cytological diagnosis

Ancillary studies

Previous history and histological correlation

ACA ACA Metastatic ACA Small-cell CA Small-cell CA MC Metastatic SCC NHL, large-B-cell, diffuse Lymphoma Large-cell lymphoma Hemangiopericytoma

Cell block None None Cell block SYNþ, CHRþ Cell block TTF-1þ None None Cell block L26þ, CD3 Genomic DNA None None None

Large-cell CA with giant-cell features (lung) ACA (lung) ACA (lung) Small-cell CA (lung) Small-cell CA (lung) SCC (lung) SCC (lung) NHL, large-cell type (lymph node) NHL, large-B-cell, diffuse (lymph node) NHL, large-B-cell (lymph node) Hemangiopericytoma, buttock, breast, thigh, kidney

ACA, adenocarcinoma; CA, carcinoma; SCC, squamous-cell CA; SYN, synaptophysin; CHR, chromogranin; TTF-1, thyroid transcription factor, NHL, non-Hodgkin’s lymphoma; MC, metastatic carcinoma; M, male; F, Female.

each patient, pertinent clinical history, radiological findings, cytological material, and histological material were reviewed and correlated.

Results Clinical Data Clinical findings are summarized in Table I. Six patients were men and five patients were women, with a mean age of 57 yr (age range, 30-83 yr). All patients had a previous history of malignancy with histological material available for review. Five cases involved the right kidney, four cases involved the left kidney, and two cases were bilateral. Two patients had concomitant liver metastases and one patient had bony metastases. One patient had acquired immunodeficiency syndrome (AIDS). Lung carcinoma was the most frequent primary malignancy to metastasize to the kidney comprising seven cases, including three adenocarcinomas (ACAs; two moderately differentiated adenocarcinomas and one large-cell undifferentiated carcinoma with giant-cell features), two squamous-cell carcinomas, and two small-cell carcinomas. The second most frequent malignancy was lymphoma, comprising three cases (all diffuse large B-cell lymphomas). One case was a metastatic mesenchymal neoplasm (hemangiopericytoma). This patient had a history of multiple metastatic hemangiopericytomas and was the only patient to undergo partial nephrectomy subsequent to her diagnosis. The interval of time between the diagnosis of the primary tumor and the onset of renal metastasis ranged from less than a year for the carcinomas to 12 yr for the hemangiopericytoma.

Cytological-Histological findings The cellularity of the smears was adequate and all cases had the characteristic cytological pattern consistent with the primary malignancy. Metastatic ACAs showed three-dimensional sheets or clusters of cohesive malignant epithelial cells distributed in glandular arrangements with abundant cytoplasm and 326

Diagnostic Cytopathology, Vol 32, No 6

prominent nucleoli (Fig. C-1). In comparison, they were morphologically similar to their primary counterparts. One case of undifferentiated lung ACA may have been confused with a primary sarcomatoid renal-cell carcinoma or with a primary high-grade transitional-cell carcinoma (TCC), but a spindle-cell component was missing and the tumor cells lacked the hard glassy cytoplasm of TCC. In addition, the morphological similarity with the lung tumor and the presence of concomitant liver metastases shortly after pneumonectomy favored a metastatic process in the kidney. Small-cell carcinomas showed the classic features of loosely cohesive hyperchromatic cells with a high nuclear/ cytoplasmic (N:C) ratio, scanty cytoplasm, nuclear molding, and crush artifact (Fig. C-2). Although primary smallcell carcinomas of the kidney have been reported,13 the presence of a previous small-cell carcinoma of the lung indicated a metastatic process rather than a new primary small-cell carcinoma. A Wilm’s tumor must be considered, especially in a younger patient, but would show small primitive epithelial cells arranged in rosettes or tubules (blastema) and a fibrous/myxoid stroma, features not seen in our cases.14 IHC staining in two small-cell carcinomas showed positivity for synaptophysin and chromogranin in one and positivity for TTF-1 in another. Squamous-cell carcinomas, which were readily identified by their necrotic background and keratinized squamous cells with dense cytoplasm on ultrafast Papanicolaou stain (Fig. C-3), did not pose any diagnostic difficulty. The three cases of diffuse large-B-cell lymphoma had a monomorphous population of dissociated large lymphoid cells with scattered lymphoglandular bodies (Fig. C-4); all patients had a previous history of lymphoma. One patient had a diffuse large-B-cell lymphoma, which was confirmed by IHC on the cell block (L26þ, CD3, CD15, CD30, EMA), ruling out anaplastic large-cell lymphoma, Hodgkin’s lymphoma, and T-cell lymphoma; kappa-immunoglobulin gene rearrangement product was detected on genomic DNA. Another patient who had diffuse lymphadenopathy had a cervical lymph node excision, which confirmed the cytological diagnosis of large-

METASTASES TO THE KIDNEY

Figs. C-1–C-5. Fig. C-1. Aspiration smears and histological section from a case of metastatic pulmonary ACA. (A) Aspiration smears show large cells with abundant cytoplasm and prominent nucleoli arranged in glandular patterns or singly (DQ stain, 400). (B) This histological specimen from the lung shows a moderately differentiated ACA (hematoxylin and eosin, 200). Fig. C-2. Aspiration smears are markedly cellular with loosely cohesive clusters of cells with a smooth chromatin pattern and marked nuclear molding. (A) Crush artifact is noted (DQ stain, 400). (B) This histological specimen from the lung shows a small-cell carcinoma (hematoxylin and eosin, 400). Fig. C-3. Aspiration smears show clusters and single cells with hyperchromatic nuclei and abundant, hard cytoplasm. (A) Necrosis and keratinization is noted (ultrafast Papanicolaou stain, 400). (B) This histological section from the lung shows a moderately differentiated squamous-cell carcinoma (hematoxylin and eosin, 200). Fig. C-4. Aspiration smears show a monotonous population of large lymphoid cells with prominent nucleoli and scant cytoplasm. (A) Lymphoglandular bodies are noted in the background (ultrafast Papanicolaou stain, 400). (B) Cervical lymph node excision confirmed a large-cell lymphoma (hematoxylin and eosin, 400). Fig. C-5. Aspiration smears consisted of fascicles and fragments of uniform tightly packed small- to medium-sized cells with round to ovoid irregular nuclei and short cytoplasmic processes in close relationship to capillaries (panel A: DQ stain, 400). Subsequent partial nephrectomy confirmed a hemangiopericytoma (panel B: hematoxylin and eosin, 200).

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327

GIASHUDDIN ET AL. Review of the Literature on Secondary Tumors of the Kidney Evaluated by FNAB

Table II.

Tumor type Author

No. of patients

Carcinoma

Lymphoma

Melanoma

Other

Murphy

7

3

1



Pilotti7

4

1 Lung small-cell CA 1 Lung SCC 1 Ovarian CA 1 Lung small-cell CA 1 Lung SCC 2 Lung CA 1 Small-cell undifferentiated CA 5 SCC (4 lung, 1 cervix) 2 Colonic ACA 1 Ampullary ACA 1 CA, unknown 1 Small-cell CA 3 HCC 6 SCC (4 lung, 1 cervix, 1 UN) 10 ACA (6 lung, 1 breast, 1 pancreas, 2 UN) —



1

1 Seminoma

1 NHL 4 NHL

— —

— —

6 Large-cell lymphomas 1 Hodgkin 1 SLL





6 Large-cell lymphomas 2 small cleaved cell lymphomas 2 SLL 3 NHL











1 Hemangiopericytoma

6

8

Leiman Truong9

3 14

Gattuso10

28

Truong11

10

Mignon12

14

Giashuddin

11

11 ACA (lung, upper airways, kidney, breast, gynecologic)a 3 lung ACA 2 lung small cell CA 2 lung SCC

3 large-B-cell lymphomas

CA, carcinoma; SCC, squamous-cell carcinoma; ACA, adenocarcinoma; UN, unknown; NHL, Non-Hodgkin’s lyphoma; SLL, small lymphocytic lymphoma; HCC, hepatocellular carcinoma. a Exact number not specified.

B-cell lymphoma. The third patient with AIDS was treated accordingly and no surgery was performed. The most challenging case was that of metastatic hemangiopericytoma. This patient had multiple soft-tissue metastases affecting the breast and extremities diagnosed by previous aspiration biopsies at our institution; they all were morphologically identical to the kidney tumor.15 The tumor consisted of fascicles and fragments of uniform tightly packed small- to medium-sized cells with round to ovoid irregular nuclei and short cytoplasmic processes in close relationship to capillaries (Fig. C-5). Subsequent partial nephrectomy was identical to her prior tumors (Fig. C-5B).

Discussion With the exception of angiomyolipoma, most primary or secondary neoplasms of the kidney including carcinomas, lymphomas, sarcomas, and oncocytomas can not be diagnosed with certainty by radiological imaging because they share common features.16 Although secondary tumors of the kidney usually are bilateral multiple solid enhancing lesions, with evidence of metastatic disease elsewhere, most of our cases presented as a single renal mass and radiological findings often failed to distinguish a primary renal tumor from a metastasis, especially if the mass was well circumscribed. Because chemotherapy is the preferred therapeutic option over surgery, metastatic tumors to the kidney can be assessed by FNAB. The previous 328

Diagnostic Cytopathology, Vol 32, No 6

reports of secondary tumors to the kidney are summarized in Table II. The most common tumors are carcinomas originating from the lung, followed by lymphomas, usually of the large-cell type.9,11 Soft-tissue sarcomas exceptionally metastasize to the kidney.12,15 According to the literature, the diagnosis of secondary tumors to the kidney usually is straightforward and these are included within a larger series of renal tumors evaluated by FNAB. Metastatic carcinomas (MCs) are notoriously different from primary renal-cell carcinoma on cytological smears and often the diagnosis is made by the combination of cytomorphological features, radiological appearance, and clinical history. MCs have three-dimensional clusters of tumor cells, similar to primary renal-cell carcinoma, but lack papillary structures; foamy, clear, or granular cells with abundant cytoplasm; metachromatic basement membrane material attached to the tumor cells; and numerous naked nuclei, all of which are classic features of the latter.9 The cells of MCs have scant cytoplasm and only a few dissociated cells. The background more often is cystic and bloody with calcific debris in primary tumors and necrosis in metastases, although overlapping features exist.10 MC can be confused with collecting duct carcinoma (Bellini tumor) because both entities have tumor cells with hyperchromatic large nuclei and scant cytoplasm.7 Cell blocks can be very helpful when the smears are nondiagnostic.10 The cytological diagnosis in secondary

METASTASES TO THE KIDNEY

renal tumors was accurate in most of the reported cases, except for one case of seminoma diagnosed as renal-cell carcinoma7 and one lymphoma diagnosed as TCC.11 For lymphomas published before the era of IHC, a resection was deemed necessary to confirm the cytological diagnosis.6 In more recent publications of lymphomas evaluated by FNA11 immunophenotyping, flow cytometry and gene rearrangement studies were mandatory to reach an accurate diagnosis, which was confirmed by tissue core biopsies, and prevented unnecessary surgery. For carcinomas, the use of ancillary studies may prove necessary if the primary site is unknown, and when dealing with a singlecell pattern or with a spindle-cell lesion. In our experience, the diagnosis of two of three lymphomas and three small-cell carcinomas were confirmed with immunostains, gene rearrangement studies, and excision of a lymph node in one case of lymphoma. Our study clearly shows that FNAB is a particularly useful diagnostic procedure in the evaluation of renal metastasis. One significant limitation, not seen in our series (as a result of a cytotechnologist being present at each procedure) but reported in the literature, is the failure to obtain a satisfactory sample, which varies between 5 and 28%.9–12 Some authors experienced difficulty in obtaining enough material in lymphomas,6 illustrating the fact that this procedure is operator dependent. Precise knowledge of the cytological features of various tumors also is crucial to reach a correct diagnosis, especially when a history of a primary malignancy is lacking. Lack of sufficient expertise can give rise to false positive or false negative results.6 Knowledge of the patients prior malignancy is helpful in making an accurate diagnosis. In summary, the diagnosis of metastatic tumors to the kidney was made accurately in all cases, based on knowledge of a prior malignancy, cytomorphological features, and in some cases associated ancillary studies. Review of

a prior histopathological specimen and comparison with the material obtained by aspiration biopsy can lead to a confident, accurate diagnosis.

References 1. Klinger ME. Secondary tumors of the genito-urinary tract. J Urol 1951;65:144. 2. Abrams HL, Spiro R, Goldstein N. Metastases in carcinoma: analysis of 1000 autopsied cases. Cancer 1950;3:74. 3. Bracken BR, Chica G, Johnson DE, Luna M. Secondary renal neoplasms: an autopsy study. S Med J 1979;72:806–807. 4. Wagle DG, Moore RH, Murphy GP. Secondary carcinomas of the kidney. J Urol 1975;114:30–32. 5. Newsam JE, Tulloch WS. Metastatic tumors in the Kidney. Br J Urol 1966;31:1–6. 6. Murphy WM, Zambroni BR, Emerson LD, Moinuddin S, Lee LH. Aspiration biopsy of the kidney simultaneous collection of cytologic and histologic specimens. Cancer 1985;56:200–205. 7. Pilotti S, Rilke F, Alasio L, Garbagnati F. The role of fine-needle aspiration in the assessment of renal masses. Acta Cytol 1988;32:1–10. 8. Leiman G. Audit of fine needle aspiration cytology of 120 renal lesions. Cytopathology 1990;1:65–72. 9. Truong LD, Todd TD, Dhurandhar B, Ramzy I. Fine-needle aspiration of renal masses in adults: analysis of results and diagnostic problems in 108 cases. Diagn Cytopathol 1999;20:339–349. 10. Gattuso P, Ramzy I, Truong LD, et al. Utilization of fine-needle aspiration in the diagnosis of metastatic tumors to the kidney. Diagn Cytopathol 1999;21:35–38. 11. Truong LD, Caraway N, Ngo T, Laucirica R, Katz R, Ramzy I. Renal lymphoma. The diagnostic and therapeutic roles of fine-needle aspiration. Am J Clin Pathol 2001;115:18–31. 12. Mignon F, Mesurolle B, Ariche-Cohen M, Vanel D. Interet des ponctions biopsies renales sous controle tomodensitometrique: analyse retrospective de 67 cas. J Radiol 2001;82:907–911. 13. Capella C, Eusebi V, Rosai J. Primary oat cell carcinoma of the kidney. Am J Surg Pathol 1984;8:855–861. 14. Quijano G, Drut R. Cytologic characteristics of Wilms’ tumors in fine-needle aspirates. A study of 10 cases. Acta Cytol 1989;33:263–266. 15. Chhieng D, Cohen JM, Waisman J, Fernandez G, Cangiarella J. Fine-needle aspiration cytology of hemangiopericytoma. Cancer 1999;87:190–195. 16. Volpe JP, Choyke PL. The radiologic evaluation of renal metastases. Crit Rev Diagn Imaging 1990;30:219–246.

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Metastases to the kidney - Wiley Online Library

Metastases to the kidney from extrarenal primary tumors are uncommon and may mimic renal-cell carcinoma clinically when presenting as a single mass with hematuria. Fine-needle aspira- tion biopsy (FNAB) is a useful diagnostic method for the evalua- tion of primary renal tumors. Only a few studies have investi-.

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