Fine needle aspiration of salivary gland carcinomas with high-grade transformation: A multi-institutional study of 22 cases and review of the literature

Abstract

Background: High-grade transformation (HGT) is a rare process whereby conventional low- to intermediate-grade salivary gland carcinomas (SGC) transform into high-grade, poorly or undifferentiated malignancies with focal or complete loss of their conventional histomorphologic features. Because tumors with HGT are associated with a worse prognosis than their conventional counterparts, preoperative recognition of HGT may be of benefit for optimal patient management. Using a multi-institutional approach, we describe the largest fine needle aspiration (FNA) cohort of salivary gland carcinomas with HGT.

Methods: The archives of 9 large academic medical centers were searched, and 22 cases of SGC with HGT were identified by surgical excision accompanied by preoperative FNA. Clinical and cytomorphologic features were retrospectively reviewed.

Results: The male-to-female ratio was 14:8, and the mean patient age was 60.2 years. The average tumor size was 3.6 cm, and 19 cases were from the parotid gland. Acinic cell carcinoma with HGT was the most common tumor subtype, comprising 12 cases with HGT, followed by adenoid cystic carcinoma, secretory carcinoma, and other subtypes. Eighteen cases were classified as malignant; however, a specific diagnosis of HGT was not made. Sixteen cases contained a high-grade cytologic component, and 7 cases had a mixture of both conventional and high-grade components retrospectively.

Conclusions: SGC with HGT should be considered in the differential diagnosis of a salivary gland aspirate exhibiting high-grade cytomorphologic features. The presence of distinct tumor populations, conventional and high-grade, should prompt consideration of HGT, especially when the conventional component is acinic cell carcinoma or adenoid cystic carcinoma.

Keywords: acinic cell carcinoma; adenoid cystic carcinoma; fine needle aspiration; high-grade transformation; salivary cytology; salivary gland; salivary gland carcinoma; secretory carcinoma.

Figure 1.

Cytologic features of high-grade transformation (HGT) exhibiting 2-cell patterns. (A) FNA of acinic cell carcinoma with HGT. Tumor cells from a high-grade component (arrow) have larger nuclei and form disorganized cellular clusters compared with the conventional component (arrowhead) (Papanicolaou stain). (B) Histologic features of the same case (hematoxylin and eosin stain). The tumor loses features of acinic cell carcinoma (left panel) and transforms into poorly differentiated carcinoma (right panel). (C,D) Higher magnification of conventional and high-grade components of acinic cell carcinoma with HGT (Papanicolaou stain). Tightly cohesive clusters of uniform basaloid cells with small nuclei suggestive of low-grade carcinoma (C). Large pleomorphic cells with occasional prominent nucleoli form less cohesive clusters or are present as single cells (D). (E) Diff-Quik stain of secretory carcinoma with HGT. Two cell populations with different sizes and chromatin patterns are observed. (F) Cell block specimen of an FNA of acinic cell carcinoma with HGT. A clear contrast between 2 components is demonstrated. Mitosis is noted in the high-grade component (hematoxylin and eosin stain).

Figure 2.

Cytologic features of high-grade transformation (HGT) with 1 component. (A, B) FNA of HGT showing solely the high-grade carcinoma component (Papanicolaou stain). (A) FNA of adenoid cystic carcinoma with HGT. Large pleomorphic are present in clusters with nuclear crowding. Inflammatory cells and necrotic debris are noted. (B) FNA of acinic cell carcinoma with HGT. The original acinic cell differentiation is completely lost and the cytologic features are indistinguishable from those in panel A. (C, D) FNA of adenoid cystic carcinoma with HGT showing only the conventional carcinoma component. (C) Basaloid hyperchromatic cells are present around matrix globules. This case was signed out as adenoid cystic carcinoma (Diff-Quik stain). (D) Cohesive clusters occasionally associated with matrix-like material. Although slight nuclear size variation is noted, no obvious high-grade features are observed (Papanicolaou stain).