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Keywords:

  • salivary duct carcinoma;
  • cytology;
  • immunohistochemistry;
  • androgen receptor

Abstract

  1. Top of page
  2. Abstract
  3. MATERIALS AND METHODS
  4. RESULTS
  5. DISCUSSION
  6. REFERENCES

BACKGROUND

Although there have been several reports of cytologic features for salivary duct carcinoma (SDC), it still can be difficult to diagnose patients with these tumor accurately at the time of fine-needle aspiration (FNA). Review of the literature indicates that, immunohistochemically, SDC expresses androgen receptor (AR) in the majority of patients. The authors investigated the cytologic characteristics and utility of AR immunostaining on cytologic smears for the diagnosis of patients with SDC.

METHODS

FNA and imprint smears from four patients with SDC were stained with Papanicolaou and periodic acid-Schiff (PAS). Immunostaining for AR on paraffin sections and imprint smears of SDC was performed, including 51 benign and other malignant salivary gland tumors.

RESULTS

The smears were cellular and contained three-dimensional clusters, flat sheets, and scattered epithelial cells with necrotic backgrounds. A cribriform architectural pattern was noted in many of the tumor sheets. The tumor cells were large polygonal, spindle, and round to oval, and had abundant, finely granular, or vacuolated cytoplasm. Intracytoplasmic vacuoles were PAS negative. The nuclei were hyperchromatic, medium to large in size, round to oval in shape, and often had prominent nucleoli. All SDC tumors expressed AR. Two patients with carcinoma in (pleomorphic adenoma) showed a focal, comedo carcinoma pattern in which AR positive nuclei were observed. Other salivary gland tumors were completely negative for AR.

CONCLUSIONS

The cytologic features of high-grade adenocarcinoma with a variety of cell morphologies, flat sheets of tumor cells with a cribriform pattern, and necrotic backgrounds are characteristic findings in patients with SDC. Immunostaining for AR on cytologic smears is useful for the diagnosis of these patients. Cancer (Cancer Cytopathol) 2001;93:344–350. © 2001 American Cancer Society.

Salivary duct carcinoma (SDC), which was described first by Kleinsasser et al.1 in 1968, is an uncommon salivary gland tumor with a histologic resemblance to ductal carcinoma of the breast. Comedo necrosis is a common feature.2–6 SDC occurs in the major salivary glands, particularly the parotid gland.2 Most patients are males and are age > 50 years. SDC frequently has an aggressive clinical behavior, with invasion of the facial nerve, local recurrence, and/or distant metastasis.2 Aggressive clinical management, including radical surgery and postoperative radiation therapy in the early stage of the tumor, appears to be the only hope for long-term survival.2, 7 Therefore, establishing an accurate preoperative diagnosis by fine-needle aspiration (FNA) is important. Although there have been several reports of cytologic features for SDC,8–17 it still may be difficult to diagnose the tumor accurately at the time of FNA. In addition to thorough FNA sampling of different areas of the tumor, clinical findings may be useful in suggesting the correct diagnosis.13 Review of the literature indicates that, immunohistochemically, SDC expresses androgen receptor (AR) in the majority of patients.18, 19 This study was undertaken to evaluate the cytologic features of SDC to define better the diagnostic characteristics of SDC and to investigate the significance of AR immunostaining for the diagnosis of SDC.

MATERIALS AND METHODS

  1. Top of page
  2. Abstract
  3. MATERIALS AND METHODS
  4. RESULTS
  5. DISCUSSION
  6. REFERENCES

Six histologically confirmed patients with SDC were studied. FNA and imprint cytology were performed in four patients (Patients 1–4 in Table 1). The smears were fixed in 95% ethanol and stained by the standard Papanicolaou method and periodic acid-Schiff (PAS). For histopathologic study, the surgical materials from six patients were fixed in 20% neutral buffered formalin, embedded in paraffin, sectioned at 4-μ intervals, and stained with hematoxylin and eosin and PAS. Slides were reviewed critically to ensure adherence to strict diagnostic criteria for SDC.2, 4 The clinicopathologic findings in these patients are summarized in Table 1.

Table 1. Clinicopathologic Findings in Six Patients with Salivary Duct Carcinoma
CharacteristicPatient 1Patient 2Patient 3Patient 4Patient 5Patient 6
  • a

    See Hermanek et al., 1987.20

Age (yrs)764960496554
GenderMaleMaleMaleMaleMaleMale
SymptomsRapidly growing, painless massRapidly growing, painless mass; facial nerve palsyRapidly growing, painless massRapidly growing, painless mass; facial nerve palsyRapidly growing, painless massRapidly growing, painless mass
SiteRight parotidRight parotidLeft parotidRight parotidLeft submandibleRight parotid
Tumor size (cm)7.0 × 4.02.5 × 2.05.5 × 5.02.5 × 2.03.0 × 2.010.0 × 9.0
TNM classificationaT4bN2bM0 stage IVT2aN0M0 stage IT3bN0M0 stage IIIT2bN2bM0,Stage IVT2bN2bM0,Stage IVT4bN2bM0, Stage IV
Follow-upLocal recurrence and metastasis in lung and brain; died of disease at 2 yrsAlive with disease at 4.5 yrs; metastasis in lung and brainNo evidence of disease at 6 monthsMetastasis in lung; died of disease at 2 yrs1 yr later, lost to follow-upUncontrollable local disease; died of disease at 6 months

Immunohistochemical staining for AR (1:70 dilution; mouse monoclonal; BioGenex, San Ramon, CA) was carried out with an automated immunostaining system (OptiMax Plus; BioGenex) on 4-μ paraffin sections from each patient and on ethanol fixed imprint smears from three patients employing a biotin-streptavidin amplified method. Diaminobenzidine was used as a chromogen, and sections and/or smears were counterstained lightly with hematoxylin. Positive tissue and/or smear control samples of breast carcinoma as well as negative control slides that were run simultaneously were used to assess the quality of immunostaining. On paraffin sections, microwave pretreatment for antigen retrieval was carried out prior to incubation with primary antibody. Microwave pretreatment was omitted on imprint smears. In addition, we examined AR expression in 21 samples of benign salivary glands and in 30 samples of other malignant salivary gland tumors. Immunohistochemical studies of estrogen receptor (ER; prediluted; mouse monoclonal ER88; BioGenex) and progesterone receptor (PgR; prediluted; mouse monoclonal PR88; BioGenex) also were performed on paraffin sections from the six patients with SDC using the same method.

RESULTS

  1. Top of page
  2. Abstract
  3. MATERIALS AND METHODS
  4. RESULTS
  5. DISCUSSION
  6. REFERENCES

Cytologic Findings

For two patients, the initial FNA cytologic diagnoses of SDC were high-grade adenocarcinomas (Patients 1 and 3). The FNA specimens from two patients and the imprint smears from three patients were cellular and consisted of cohesive, three-dimensional clusters and flat sheets of tumor cells with necrotic backgrounds (Fig. 1). A cribriform architectural pattern was noted in many of the tumor sheets (Fig. 2). At the periphery of these sheets, there were many scattered, individual tumor cells. The tumor cells were large, polygonal, spindle, and round to oval and had abundant, finely granular, or vacuolated cytoplasm. The nuclei were hyperchromatic, medium to large in size, round to oval in shape, and often had prominent nucleoli (Figs. 3, 4). Cytoplasmic vacuoles were stained negatively with PAS. Mitotic figures were observed frequently. The cytologic findings are summarized in Table 2.

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Figure 1. A fine-needle aspiration biopsy specimen from Patient 1 shows a cluster of three-dimensional tumor cells with a necrotic background (Papanicolaou stain; original magnification, × 200).

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Figure 2. A fine-needle aspiration biopsy specimen from Patient 3 shows a sheet of cells with a cribriform pattern (Papanicolaou stain; original magnification, × 200).

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Figure 3. A fine-needle aspiration biopsy specimen from Patient 3 shows highly pleomorphic tumor cells with abundant, finely granular, and vacuolated cytoplasm. Enlarged, round nuclei with prominent nucleoli and mitotic figures are seen (Papanicolaou stain; original magnification, × 400).

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Figure 4. An imprint smear from Patient 4 shows scattered, large tumor cells with round-to-oval, hyperchromatic nuclei (Papanicolaou stain; original magnification, × 400).

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Table 2. Cytologic Features of Four Patients with Salivary Duct Carcinoma
Sample characteristicPatient 1 (FNAC)Patient 2 (imprint)Patient 3 (FNAC, imprint)Patient 4 (imprint)
  1. FNAC: fine needle aspiration cytology.

BackgroundExtensively necroticNecroticNecroticExtensively necrotic
Cell ArrangementStratification, sheets, cribriformSheets, cribriform, scatteredStratification, sheets, cribriform, scatteredStratification, sheets, cribriform, scattered
Cells
 SizeMediumMedium to largeMedium to largeMedium to large
 VarianceSlightly pleomorphicPleomorphicPleomorphicPleomorphic
 ShapePolygonal, round, ovalPolygonal, round, ovalPolygonal, spindle, round, ovalPolygonal, spindle, round, oval
CytoplasmFinely granularFinely granular, vacuolatedFinely granular, vacuolatedFinely granular, vacuolated
Nucleus
 ShapeRound to ovalRound to ovalRound to ovalRound to oval
 ChromatinFine, granularFine, granularGranular, coarseGranular, coarse
NucleoliOne or two, smallOne or two, largeOne or two, largeOne or two, large

Pathologic Findings

The tumors ranged in size from 2.5 cm to 10.0 cm. The margins were infiltrative macroscopically. The cut surfaces were yellow-gray and contained necrotic and cystic areas. Microscopically, the tumors were comprised of well-defined islands of epithelial cells exhibiting a cribriform pattern and central comedo necrosis, strongly resembling ductal carcinoma of the breast (Fig. 5). The tumor cells had round-to-oval nuclei with prominent nucleoli and abundant, eosinophilic, granular, or vacuolated cytoplasm. Intracytoplasmic vacuoles were negative with PAS. Mitotic figures were observed frequently.

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Figure 5. A histologic section from Patient 3 shows salivary duct carcinoma with a cribriform pattern and central necrosis resembling comedo carcinoma of the breast (hematoxylin and eosin stain; original magnification, × 200).

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Immunohistochemical Study

Immunostainings for AR, ER, and PgR were successful on positive and negative control slides. The results of immunohistochemical study are listed in Table 3. In five of the six SDC samples, strong immunostaining for AR was observed diffusely in the nuclei of neoplastic cells (Fig. 6). Almost 100% of the tumor cells were positive. The single remaining sample (Patient 1) was weakly stained in about 50% of neoplastic cell nuclei. AR was not expressed in the adjacent normal salivary glands. Two of the three patients with carcinoma in pleomorphic adenoma showed a focal, comedo carcinoma pattern in which AR positive nuclei were observed. The remaining single sample of carcinoma (squamous cell carcinoma-like) in pleomorphic adenoma was negative for AR. Other salivary gland carcinoma samples and benign tumor samples were completely negative for AR. On imprint smears from patients with SDC (Patients 2–4), almost 100% of the neoplastic cell nuclei were strongly positive for AR (Fig. 7). There was no expression of ER or PgR in the SDC samples.

Table 3. Immunohistochemical Expression of Androgen Receptor in Salivary Gland Tumors
Tumor typeNo. of AR positive tumors
  • AR: androgen receptor.

  • a

    Focal, AR positive cell nuclei were present in the comedocarcinoma-like lesions.

Malignant8 of 36
 Salivary duct carcinoma6 of 6
 Mucoepidermoid carcinoma0 of 6
 Acinic cell carcinoma0 of 5
 Adenoid cystic carcinoma0 of 8
 Epithelial-myoepithelial carcinoma0 of 2
 Squamous cell carcinoma0 of 1
 Basal cell adenocarcinoma0 of 5
 Carcinoma in pleomorphic adenoma2a of 3
Benign0 of 21
 Pleomorphic adenoma0 of 10
 Warthin tumor0 of 10
 Lymphadenoma0 of 1
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Figure 6. Androgen receptor (AR) immunostaining on a histologic section from Patient 2. Almost 100% of the tumor cells show a strong, positive reaction in the nuclei. The adjacent normal parotid gland shows no AR (biotin-streptavidin amplified method; original magnification, × 100).

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Figure 7. Androgen receptor immunostaining is seen on an imprint smear from Patient 2. Many tumor cell nuclei are strongly positive (biotin-streptavidin amplified method; original magnification, × 200).

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DISCUSSION

  1. Top of page
  2. Abstract
  3. MATERIALS AND METHODS
  4. RESULTS
  5. DISCUSSION
  6. REFERENCES

SDC is a high-grade, malignant tumor that demonstrates a propensity for invasive spread with early regional and distant metastases.2 Although, Delgado et al.21 recently described low-grade SDC in contrast to the aggressive, high-grade SDC and reported that low-grade SDC appeared biologically indolent, with bland cytologic and histologic features, the current report discusses high-grade SDC. Patients commonly present with a painless, rapidly growing, parotid mass, often with facial nerve involvement and cervical adenopathy.2, 3, 5, 6 Approximately 80% of reported patients have been males.2, 6, 13, 16 The age range at the time of presentation is 22–91 years, with a peak incidence in the sixth and seventh decades of life.2 Brandwein et al.3 reviewed the literature on SDC and summarized the prognostic findings from SDC in 60 patients with follow-up. Local recurrence was seen in 39% of patients with SDC, lymphatic involvement was seen in 60%, and distant metastases were seen in 57%. The mortality rate was 55%, within a mean of 29 months. In our series, three patients died of recurrent or metastatic disease within 2 years., and one patient is alive with lung and brain metastases.

Histologically, SDC may contain a combination of growth patterns similar to those seen in ductal carcinoma of the breast. Both intraductal and infiltrating components are recognized.2–6 Extensive central comedo necrosis commonly is associated with the intraductal component. Papillary, cribriform, solid, or various combinations of these histologic patterns are observed. The infiltrating carcinoma consists of irregular glands and cords of compressed cells that frequently are associated with a prominent desmoplastic reaction. The individual cells are large and polygonal in shape, and they display a finely granular, vacuolated, eosinophilic cytoplasm, imparting an apocrine appearance to the cells. The cell borders are well defined. The nuclei are round to oval in shape, hyperchromatic, and moderately pleomorphic. Coarse chromatin, prominent nucleoli, and conspicuous mitotic figures are seen. Intracytoplasmic mucin usually is negative. In our patients, cribriform pattern and comedo necrosis frequently were observed, and intracytoplasmic PAS negative vacuoles often were present.

The cytologic findings reflect the histology and also resemble breast carcinoma. The cytologic features of SDC have been reported in detail for several series.8–17 Most of the reported patients show features of high-grade malignancy. The smears are cellular and contain cohesive, three-dimensional clusters and flat sheets of large, polygonal cells with abundant, finely granular cytoplasm. Some of the sheets of cells display an irregular branching or cribriform pattern as well as papillary cluster formations. Single cells with well-defined borders also are seen. The nuclei are enlarged and round to oval, and they show moderate pleomorphism. The chromatin is finely granular or coarse, and prominent nucleoli are present in the nuclei. Mitotic figures also are seen. Necrosis frequently is present in the background. Although the cytologic features of our patients were almost similar to those in previous series, we would like to stress the marked cytomorphologic variety and the flat sheets of tumor cells with a cribriform pattern.

In FNA materials, differential diagnoses include high-grade mucoepidermoid carcinoma, squamous cell carcinoma, oncocytic carcinoma, adenoid cystic carcinoma, and adenocarcinoma not otherwise specified (NOS).6, 11, 14–16 High-grade mucoepidermoid carcinoma is comprised of squamoid, intermediate, and rare mucous cells. The squamoid cells with marked atypia and frequent mitotic figures may mimic SDC. The presence of intermediate cells and mucous cells, however, argues against SDC.16 Similarly, squamous cell carcinoma is comprised of round, ovoid, or enlarged atypical cells with dense nuclear chromatin and tumor necrosis; bare nuclei and keratin debris commonly may be encountered. Marked keratinization is a feature that excludes the diagnosis of both SDC and mucoepidermoid carcinoma.16, 22 Oncocytic carcinoma may present a differential diagnosis difficulty, because some SDCs may manifest oncocytic (apocrine-like) features. The marked cytonuclear atypia typically present in SDC and the infrequency of oncocytic carcinoma favor the former diagnosis.16, 23, 24 Adenoid cystic carcinoma may contain cribriform structures, but characteristic amorphous mucoid globules also are seen. Its cells are generally small, whereas those in SDC have larger cytoplasm.9, 10, 14 Adenocarcinoma NOS may have diagnostic problems. This is a salivary gland carcinoma that shows glandular or ductal differentiation but lacks prominence of any of the histomorphologic features that characterize the other, more specific carcinoma types. If sufficient FNA materials cannot be obtained and if they show high-grade malignancy without specific cytomorphologic features, then the cytopathologist may elect to render a diagnosis of adenocarcinoma NOS. Although SDC occurs exclusively in males, metastatic adenocarcinoma from the breast may be indistinguishable from SDC on the basis of cytology alone.

A review of the literature indicates that AR, a marker frequently detected in patients with prostatic adenocarcinoma, is expressed in > 90% of patients with SDC,18, 19 whereas two common breast carcinoma markers, ER and PgR, are expressed in only 1.3% and 6% of patients with SDC, respectively, by immunohistochemistry.6, 18, 19, 25, 26 In our six patients with SDC, ER and PgR were not expressed. This hormonal profile suggests that SDC, in contrast to its histologic similarity to breast carcinoma, is related immunophenotypically more closely to prostatic adenocarcinoma.19 Expression of AR in patients with SDC was an incidental discovery. This discovery led to a study by Kapadia and Barnes18 in which 12 SDC samples were stained for AR, and 11 samples were found positive. Fan et al.19 also reported that 12 of 13 patients with SDC were positive for AR. In our study, all six patients with SDC were positive for AR, and cytologic smears also showed strong positive reactions on the tumor cell nuclei. Other salivary gland tumors were negative for AR, except two patients with carcinoma in pleomorphic adenoma. In these patients, AR positive nuclei were confined to the carcinoma areas that resembled comedo carcinoma of the breast. Although there were a few reported patients with SDC associated with pleomorphic adenoma,5 we could not diagnose our samples as SDC because of small, localized lesions. It may be difficult to differentiate pure SDC from SDC in pleomorphic adenoma. However, a long clinical history of the tumor mass and the admixed pleomorphic adenoma features in FNA materials suggest the diagnosis of SDC in pleomorphic adenoma. Salivary gland metastasis from breast carcinoma may have diagnostic difficulties in FNA materials; however, it can be distinguished from SDC by immunostaining for ER, which is expressed commonly in breast carcinoma.27 Clinical information may be the most important for distinguishing between them. A thorough investigation of cytologic smears and immunostaining for ER and AR may help in the differential diagnosis.

In conclusion, the cytologic features of high-grade adenocarcinoma with a variety of cell morphologies—flat sheets of tumor cells with a cribriform pattern and necrotic backgrounds—are characteristic findings in patients with SDC. Immunostaining for AR on cytologic smears is useful for the diagnosis of SDC.

REFERENCES

  1. Top of page
  2. Abstract
  3. MATERIALS AND METHODS
  4. RESULTS
  5. DISCUSSION
  6. REFERENCES
  • 1
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