ABSTRACT
Objective
The Milan System for Reporting Salivary Gland Cytopathology (MSRSGC) provides a standardized framework for interpreting salivary gland fine‐needle aspiration cytology (FNAC) samples and estimating the associated risk of malignancy (ROM). This study aimed to retrospectively reclassify parotid gland fine‐needle aspiration (FNA) samples from our institution according to the MSRSGC, evaluate the correlation between preoperative cytological and postoperative histopathological findings, and determine the ROM for each diagnostic category.
Materials and Methods
A total of 277 parotid gland FNAC cases with subsequent surgical excision between 2010 and 2024 were included. Cytological smears were independently reviewed and reclassified according to MSRSGC by two blinded pathologists. Cytology–histology concordance was assessed, and diagnostic performance metrics, including sensitivity, specificity, positive predictive value (PPV), negative predictive value (NPV), and overall accuracy, were calculated. ROM for each Milan category was derived from the final histopathology.
Results
Of the 612 patients who underwent FNAC, 277 (45.3%) had available histopathological follow‐up. The mean age was 49.6 ± 15.67 years, with a male‐to‐female ratio of 1.2:1. Benign neoplasm (Category IVa) was the most frequent cytological diagnosis (71.1%). Histopathology revealed 235 benign and 42 malignant lesions. FNAC demonstrated a sensitivity of 85.2%, specificity of 99%, PPV of 92%, NPV of 98%, and an overall diagnostic accuracy of 97.4%. ROM values were 16% for nondiagnostic, 20% for nonneoplastic, 11% for atypia of undetermined significance (AUS), 1.5% for benign neoplasm, 47% for salivary gland neoplasm of uncertain malignant potential (SUMP), 100% for suspicious for malignancy (SFM), and 90% for malignant cases. False‐negative results were primarily associated with lymphoma, acinic cell carcinoma, and secretory carcinoma. The combined ROM for indeterminate categories (AUS, SUMP, and SFM) was 46%.
Conclusion
FNAC is a highly accurate and minimally invasive diagnostic method for parotid gland lesions. The Milan System offers valuable guidance for risk stratification and clinical management, although indeterminate categories continue to pose diagnostic difficulties. Multidisciplinary assessment and larger multicenter studies are needed to improve diagnostic precision.
1. Introduction
Salivary gland lesions encompass a wide clinical and histopathological spectrum, and distinguishing between benign and malignant tumors often poses diagnostic challenges. Fine‐needle aspiration cytology (FNAC), which is widely used in the preliminary evaluation of these lesions, is favored in clinical practice because it is minimally invasive, cost‐effective, and has a high diagnostic accuracy [1, 2]. However, the broad morphological spectrum of salivary gland lesions, cytomorphologic overlaps between benign and malignant entities, and the rarity of certain tumor types may limit the diagnostic efficacy of FNAC [3, 4].
To overcome these limitations and to standardize cytologic interpretation, the Milan System for Reporting Salivary Gland Cytopathology (MSRSGC) was proposed in 2018 by the American Society of Cytopathology (ASC) and the International Academy of Cytology (IAC) [5]. The second edition of the system was published in 2023 [6]. MSRSGC classifies cytological diagnoses into six main diagnostic categories, defining the estimated risk of malignancy (ROM) and recommended clinical management strategies for each category. This system facilitates more effective communication among pathologists, surgeons, and clinicians, thereby enhancing the reliability of patient management [7].
Recent retrospective studies have demonstrated that the MSRSGC provides reliable diagnostic sensitivity, specificity, and predictive values [3, 8, 9]. However, considerable inter‐institutional variability has been reported in the ROM rates of the so‐called “indeterminate” categories, including atypia of undetermined significance (AUS), salivary gland neoplasm of uncertain malignant potential (SUMP), and suspicious for malignancy (SFM) [3, 10]. This variability highlights that diagnostic interpretation and clinical decision‐making within these categories remain controversial.
The aim of the present study was to reclassify salivary gland FNAC specimens obtained at our institution according to the Milan System, to evaluate the correlation between cytopathological and histopathological diagnoses, and to determine the ROM for each diagnostic category in order to assess the diagnostic performance of the MSRSGC.
2. Materials and Methods
This retrospective observational study included parotid gland FNAC and excision specimens evaluated at the Department of Pathology, Umraniye Training and Research Hospital, Istanbul, Turkey, between 2010 and 2024. The study was conducted in accordance with the principles of the Declaration of Helsinki and was approved by the Institutional Ethics Committee (approval number: 98, approval date: April 24, 2023).
Of the 612 cases recorded in the pathology archives that underwent FNAC, 277 cases with subsequent surgical excision were included in the study. Cases with hypocellularity, technical artifacts that precluded evaluation, or missing archival materials were excluded. Patient age, sex, anatomical site of FNA, and histopathological diagnoses were retrieved from hospital medical records.
FNAC procedures were performed by radiologists under ultrasound guidance. Rapid on‐site evaluation (ROSE) was not performed. Smears were prepared by a cytotechnician. Alcohol‐fixed smears were stained with Papanicolaou (PAP) stain. Cell blocks were prepared for cases with sufficient residual material, and ancillary immunohistochemical studies were performed on cell block sections when necessary to aid in diagnosis.
All cytological preparations were independently reviewed in a blinded manner by two experienced pathologists, without knowledge of the histopathological diagnoses, and reclassified according to the Milan System. Excision specimens were examined histopathologically, and the histopathological diagnoses were accepted as the gold standard.
Concordance between cytological and histopathological diagnoses was assessed. Cases were categorized as true positive (cytologically diagnosed as malignant or SFM and confirmed as malignant histopathologically), true negative (cytologically benign or non‐neoplastic and histopathologically benign), false positive (cytologically malignant or SFM but histopathologically benign), and false negative (cytologically benign or non‐neoplastic but histopathologically malignant).
To evaluate the diagnostic performance of FNAC, cases classified as AUS and SUMP were excluded from the binary sensitivity and specificity calculations to avoid statistical bias, as these categories represent indeterminate diagnoses. However, these cases were included in the overall calculation of the ROM. Non‐neoplastic (Category II) and benign neoplasm (Category IVa) cases were grouped as benign. Although MSRSGC Categories II and IVa are generally considered benign in the literature, the categories regarded as malignant for the calculation of the ROM vary among studies. Therefore, two different settings were established in our study, and calculations were performed separately for each setting. In the first setting, MSRSGC Categories V and VI (SFM and malignant) were considered malignant. In the second setting, MSRSGC Categories IVb, V, and VI were accepted as the positive index test.
Statistical analyses were performed using the SPSS Statistics software package (Version 27.0, IBM Corp., Armonk, NY). Descriptive statistical methods were used for the analysis of the study data. Categorical variables were expressed as frequencies and percentages. Sensitivity, specificity, positive predictive value (PPV), negative predictive value (NPV), and overall diagnostic accuracy were calculated. Cases with negative cytological diagnosis and benign histopathological findings were considered true negatives, whereas cases with negative cytology but malignant histopathological findings were regarded as false negatives. Cases with both positive cytological diagnosis and malignant histopathological findings were classified as true positives, while cases with positive cytology but benign histopathology were considered false positives. The ROM for each Milan category was calculated by dividing the number of histopathologically malignant cases within a given category by the total number of cases in that category.
3. Results
Between 2010 and 2024, a total of 612 patients underwent FNAC for parotid gland masses; among these, 277 patients (45.3%) subsequently underwent surgical resection following cytological evaluation.
The mean age of the patients (n = 277) was 49.6 ± 15.67 years, with 126 (45.5%) females and 151 (54.5%) males. The parotid gland masses were located on the right side in 139 cases (50.1%). The mean tumor diameter was 2.71 ± 1.27 cm, measuring 2.59 ± 1.11 cm in benign lesions and 3.37 ± 1.83 cm in malignant lesions. Clinicopathological findings between genders revealed that malignant neoplasms were observed in 21 male and 20 female patients, while benign lesions were more frequent in males (Table 1).
TABLE 1.
Comparison of clinicopathological characteristics between male and female patients.
| Characteristic | Female (n = 126) | Male (n = 151) |
|---|---|---|
| Age (years) (mean ± SD) | 47.92 (±15.03) | 51.13 (±8.49) |
| Tumor size (mean ± SD [cm]) | 2371 ± 1.28 | 2998 ± 1.21 |
| Tumor location (n, %) | ||
| Right | 63 (50%) | 76 (50.33%) |
| Left | 63 (50%) | 75 (49.67%) |
| Histopathological diagnosis (n, %) | ||
| Benign | 106 (83.33%) | 130 (86.1%) |
| Malignant | 20 (16.67%) | 21 (13.9%) |
| Milan category (n, %) | ||
| Benign (IVa) | 88 (72.72%) | 109 (72.18%) |
| Malignant (VI) | 5 (4.13%) | 15 (9.93%) |
Abbreviation: SD: standard deviation.
When the FNAC materials were categorized according to the MSRSGC, the most frequent diagnostic category was benign neoplasm (Category IVa), comprising 71.1% (n = 197) of all cases. The malignant (Category VI) and SFM (Category V) categories together accounted for 9.0% (n = 25) of the cases.
Histopathological examination of the excised specimens revealed 235 benign and 42 malignant cases. The distribution of the final histopathological diagnoses of all cases is summarized in Table 2. The detailed cyto‐histological correlation for all six Milan System categories is presented in Table 3. The distribution of final histological diagnoses across the Milan categories demonstrated a high concordance rate, particularly in the benign and malignant categories.
TABLE 2.
Histopathological distribution of benign and malignant parotid gland lesions.
| Benign lesions (n = 235) | n | % | Malignant lesions (n = 42) | n | % |
|---|---|---|---|---|---|
| Pleomorphic adenoma | 124 | 52.8 | Squamous cell carcinoma | 11 | 26.2 |
| Warthin tumor | 80 | 34.0 | Acinic cell carcinoma | 5 | 11.9 |
| Basal cell adenoma | 4 | 1.7 | Carcinoma ex pleomorphic adenoma | 3 | 7.1 |
| Chronic nonspecific inflammation | 3 | 1.3 | Mucoepidermoid carcinoma | 3 | 7.1 |
| Lipoma | 3 | 1.3 | Salivary duct carcinoma | 3 | 7.1 |
| Myoepithelioma | 3 | 1.3 | Extranodal marginal zone lymphoma | 2 | 4.8 |
| Necrotizing granulomatous lymphadenitis | 3 | 1.3 | Lymphoepithelial carcinoma | 2 | 4.8 |
| Salivary gland tissue | 2 | 0.9 | Secretory carcinoma | 2 | 4.8 |
| Ancient schwannoma | 1 | 0.4 | Adenoid cystic carcinoma | 1 | 2.4 |
| Branchial cleft cyst | 1 | 0.4 | Adenocarcinoma | 1 | 2.4 |
| Ductal cyst | 1 | 0.4 | Basal cell adenocarcinoma | 1 | 2.4 |
| Cavernous hemangioma | 1 | 0.4 | Basosquamous carcinoma | 1 | 2.4 |
| Chronic sialadenitis | 1 | 0.4 | MALT lymphoma | 1 | 2.4 |
| Lymphadenoma | 1 | 0.4 | Metastatic Merkel cell carcinoma | 1 | 2.4 |
| Lymphoepithelial lesion | 1 | 0.4 | Metastatic squamous cell carcinoma | 1 | 2.4 |
| Lipomatosis | 1 | 0.4 | T‐cell lymphoma | 1 | 2.4 |
| Oncocytic hyperplasia | 1 | 0.4 | Diffuse large B‐cell lymphoma | 1 | 2.4 |
| Oncocytoma | 1 | 0.4 | Ductal adenocarcinoma | 1 | 2.4 |
| Periductal lymphocytic infiltration | 1 | 0.4 | Epithelial–myoepithelial carcinoma | 1 | 2.4 |
| Pilomatrixoma | 1 | 0.4 | |||
| Sialadenosis | 1 | 0.4 |
TABLE 3.
Cyto‐histological correlation and risk of malignancy (ROM) comparison with Milan System 2nd edition.
| MSRSGC category | ND (I) | NN (II) | AUS (III) | Benign neoplasm (IVa) | SUMP (IVb) | SFM (V) | Malignant (VI) | |
|---|---|---|---|---|---|---|---|---|
| Preoperative cytological diagnosis | (Total n = 277) | 18 | 5 | 9 | 197 | 23 | 5 | 20 |
| Postoperative histopathological diagnosis | Benign n = 235 | 15 | 4 | 8 | 194 | 12 | 0 | 2 |
| Malign n = 42 | 3 | 1 | 1 | 3 | 11 | 5 | 18 | |
| Calculated ROM in current study | (%) | 16 | 20 | 11 | 1.5 | 47 | 100 | 90 |
| MSRSGC 2nd edition (2023) estimated ROM | (%) | 15 | 10 | 20 | < 5 | 35 | 83 | > 90 |
Abbreviations: AUS: atypia of undetermined significance; MSRSGC: Milan System for Reporting Salivary Gland Cytopathology; ND: nondiagnostic; NN: nonneoplastic; ROM: risk of malignancy; SFM: suspicious for malignancy; SUMP: salivary gland neoplasm of uncertain malignant potential.
For Setting 1, after excluding cases in the AUS and SUMP categories, non‐neoplastic (Category II) and benign neoplasm (Category IVa) cases were classified as benign, while SFM (Category V) and malignant (Category VI) cases were classified as malignant, and calculations were performed accordingly.
Based on this classification, the statistical analysis revealed that FNAC had a sensitivity of 85.2%, specificity of 99%, PPV of 92%, and NPV of 98%. The overall diagnostic accuracy of FNA in distinguishing benign from malignant neoplasms was 97.4%. Among the patients, 198 were true negatives, 23 were true positives, 2 were false positives, and 4 were false negatives. The four false‐negative cases included two lymphomas, one acinic cell carcinoma, one secretory carcinoma, and two false positive cases included chronic nonspecific inflammation and Warthin tumor. These cases are summarized in Table 4. The cytological and histopathological features of secretory carcinoma of the parotid gland, in which the lesion was cytologically interpreted as pleomorphic adenoma (Milan Category IVa), are shown in Figure 1.
TABLE 4.
Analysis of discordant cases (false negatives and false positives).
| Case | Type of discordance | Side | Size (cm) | Cytological diagnosis | MSRSGC | Histopathological diagnosis |
|---|---|---|---|---|---|---|
| 1 | False negative | Right | 2.5 | Oncocytic neoplasm | IVa | Acinic cell carcinoma |
| 2 | False negative | Right | 3.0 | Warthin tumor | IVa | T‐cell lymphoma |
| 3 | False negative | Right | 3.0 | Cystic lesion | II | Extranodal marginal zone lymphoma |
| 4 | False negative | Left | 1.6 | Pleomorphic adenoma | IVa | Secretory carcinoma |
| 5 | False positive | Right | 1 | Ductal carcinoma | VI | Chronic nonspecific inflammation |
| 6 | False positive | Right | 1.8 | Acinic cell carcinoma | VI | Warthin tumor |
Abbreviation: MSRSGC: Milan System for Reporting Salivary Gland Cytopathology.
FIGURE 1.
Fine‐needle aspiration cytology and corresponding histopathological findings of secretory carcinoma of the parotid gland. (A, B) Fine‐needle aspiration (FNA) smears showing polygonal tumor cells arranged in papillary‐like clusters and scattered single cells with vacuolated cytoplasm (PAP stain; original magnifications ×40 and ×100). (C, D) Histopathological examination of the resection specimen revealed an infiltrative tumor composed of sheets and large nests of neoplastic cells arranged in a predominantly solid growth pattern (H&E stain; original magnification figure × 40 and ×100). [Color figure can be viewed at wileyonlinelibrary.com]
When the MSRSGC Category IVb was included in the malignant group (Setting 2), 198 cases were true negatives, 34 were true positives, 14 were false positives, and 4 were false negatives. The sensitivity, specificity, PPV, and NPV were 89.5%, 93.4%, 70.8%, and 98.0%, respectively. The overall diagnostic accuracy for distinguishing benign from malignant lesions was 92.8%.
When the AUS, SUMP, and SFM categories were analyzed, the overall ROM was found to be 46%.
Histopathological correlation revealed that the AUS group consisted predominantly of benign lesions, most commonly Warthin tumor (n = 3). In the SUMP category, pleomorphic adenoma (n = 6) was the most frequent diagnosis. The SUMP case, finally diagnosed as pleomorphic adenoma, is shown in Figure 2. All cases in the SFM category were confirmed as malignant on histopathological examination, with squamous cell carcinoma (n = 2) being the most common malignant type. Detailed cytological and histopathological findings are presented in Table 5.
FIGURE 2.
Cytological and histopathological findings of a case classified as salivary gland neoplasm of uncertain malignant potential (SUMP) and subsequently diagnosed as pleomorphic adenoma. (A, B) Fine‐needle aspiration cytology showing cohesive groups of ductal and myoepithelial cells with a slightly discohesive pattern and mild nuclear atypia, classified as SUMP (PAP stain; original magnifications ×40 and ×100). (C, D) Histopathological examination of the resection specimen confirming the diagnosis of pleomorphic adenoma. The tumor exhibits well‐defined borders with ductal and myoepithelial cells embedded in a characteristic chondromyxoid stroma (H&E stain; original magnifications ×40 and ×100). [Color figure can be viewed at wileyonlinelibrary.com]
TABLE 5.
Detailed analysis of cytological and histopathological findings in indeterminate categories.
| Cytological diagnosis a | Histopathological diagnosis | ROM % | |||
|---|---|---|---|---|---|
| Benign | Malign | ||||
|
AUS (Category III) (n = 9) |
|
n = 8 |
|
n = 1 | 11 |
|
SUMP (Category IVb) (n = 23) |
|
n = 12 |
|
n = 11 | 48 |
|
SFM (Category V) (n = 5) |
|
n = 5 | 100 | ||
| Total (n = 37) | n = 20 | n = 17 | 46 | ||
Abbreviations: AUS: atypia of undetermined significance; ROM: risk of malignancy; SFM: suspicious for malignancy; SUMP: salivary gland neoplasm of uncertain malignant potential.
Milan System for Reporting Salivary Gland Cytopathology.
4. Discussion
Although FNAC is widely used in the preoperative evaluation of parotid gland tumors, the broad morphological diversity of these lesions can lead to diagnostic challenges [10]. The MSRSGC was developed to standardize diagnoses and facilitate communication between pathologists and clinicians. Additionally, it allows for the estimation of the ROM for each category [11, 12]. In our study, the analysis of 277 cases reclassified according to the MSRSGC demonstrated that FNAC provides high specificity (99%) and diagnostic accuracy (97.4%) in distinguishing benign from malignant lesions. Additionally, the malignancy risks calculated for each category were found to be higher than those reported in some series, particularly within the SUMP and SFM groups. These findings contribute to the limited number of Milan System studies from our region and highlight the diagnostic variability within the gray‐zone categories, thereby addressing a notable gap in the current literature.
The association of parotid gland tumors with age and sex has been extensively studied, though the literature reports variable findings. In our study, parotid tumors were predominantly observed in older patients, which aligns with previous reports indicating that salivary gland tumors most commonly occur in the fifth and sixth decades of life. Nevertheless, parotid tumors can also present in younger age groups. Regarding sex distribution, the tumor incidence in males was slightly higher than in females (54.5% vs. 45.5%), but this difference was not statistically significant. Similarly, the literature does not report a clear gender predominance, and results vary across different series [13].
The relationship between tumor size and malignancy in parotid neoplasms has been investigated in several studies. Both literature data and our findings demonstrate that malignant lesions generally have larger diameters compared with benign masses. In our study, malignant lesions were significantly larger than benign tumors (3.37 vs. 2.59 cm, p = 0.005). Similar observations were reported by Velez‐Torres et al., Rivera Rolon et al., and Wei et al., indicating that while tumor size alone is not a definitive predictor of malignancy, larger parotid masses are more likely to be malignant [14, 15, 16]. However, some long‐standing benign tumors can also attain large sizes, emphasizing that tumor diameter should be interpreted alongside cytological and radiological findings.
The sensitivity and specificity of FNAC for parotid lesions reported in the literature are highly variable. Sensitivity ranges from 79.4% to 97%, and specificity ranges from 84% to 100% [7, 17]. In our study, FNAC demonstrated a sensitivity of 85.2% and specificity of 99%, which are consistent with previously reported ranges.
The ROM for each Milan category in our study showed some differences when compared with literature averages. In the nondiagnostic (Category I) group, we observed a ROM of 16%, similar to the reported average of 15%. In the non‐neoplastic (Category II) group, our ROM was 20%, higher than the reported 11%. The AUS (Category III) group in our study had a ROM of 11%, lower than the reported 30%. In the SUMP (Category IVb) category, the ROM was 47%, compared with 35% in the literature. In the SFM (Category V) group, the ROM was 100%, whereas the literature reports 83%. For malignant (Category VI) cases, our ROM was 90%, slightly lower than the reported 98%. These discrepancies are primarily attributable to limited case numbers in certain categories and potential interobserver and institutional variations in the interpretation of “gray‐zone” categories (AUS, SUMP, and SFM) [18].
In our cohort, four false‐negative and two false‐positive cases were identified. The analysis of these discordant cases provides valuable insights into diagnostic pitfalls. In our analysis, the “gray‐zone” categories (AUS, SUMP, and SFM) were not included in the evaluation of false‐negative and false‐positive cases in Setting 1. Therefore, all false‐result cases represented clinically clear discrepancies, as they were assigned to the opposite diagnostic group. Therefore, the discrepancies observed in our four false‐negative and two false‐positive cases may be classified as major discrepancies. Among the false‐negative cases, the cytological diagnoses were classified as Category IVa—oncocytic neoplasm, Warthin tumor, and pleomorphic adenoma—and Category II—cystic lesion. The corresponding histopathological diagnoses were acinic cell carcinoma, T‐cell lymphoma, secretory carcinoma, and extranodal marginal zone lymphoma, respectively. Secretory carcinoma is a particularly challenging entity due to its rarity and diverse morphology. As highlighted by Wiles et al. in a multi‐institutional study, secretory carcinoma often presents with bland cytological features that can mimic benign neoplasms, leading to misclassification. Key features such as vacuolated cytoplasm and a proteinaceous background may be subtle or overlooked [19, 20]. In our case, the bland morphology likely contributed to the false‐negative interpretation. Additionally, Rivera Rolon et al. reported difficulties in detecting oncocytic neoplasms, low‐grade carcinomas, and lymphomas via FNAC [15]. In the two false‐positive cases, cytological diagnoses of ductal carcinoma and acinic cell carcinoma were ultimately diagnosed histopathologically as chronic nonspecific inflammation and Warthin tumor, respectively. Such false‐positive interpretations are well‐known pitfalls in salivary gland FNAC and may result from reactive epithelial atypia, degenerative changes, inflammatory or proteinaceous background, and cytomorphological overlap between oncocytic benign lesions and malignant tumors. Warthin tumor, in particular, may mimic malignancy because of its oncocytic epithelial component, lymphoid background, cystic degeneration, and metaplastic changes. Wei et al. and other studies have highlighted the need for ancillary immunohistochemical and molecular testing in salivary gland lesions [15, 16, 20, 21]. Therefore, clinical, radiological, and pathological correlation is particularly crucial for gray‐zone categories.
Several limitations should be acknowledged. First, the retrospective design and single‐center dataset may limit the generalizability of our results. Low case numbers in AUS, SUMP, and SFM categories reduce the statistical reliability of ROM calculations for these groups. Moreover, the lack of immunohistochemical or molecular evaluation in some cases may limit diagnostic accuracy. Large‐scale prospective studies are warranted to enhance the reproducibility and reliability of the Milan System.
Strengths of our study include the relatively large sample size (n = 277) and extended study period, as well as the blinded re‐evaluation of cytological specimens by two experienced pathologists independent of histopathological diagnoses. Furthermore, our findings demonstrate that FNAC has high specificity (99%) and accuracy (97.4%) in distinguishing benign from malignant neoplasms, underscoring the clinical reliability of this diagnostic method.
5. Conclusion
FNAC is a reliable and effective diagnostic tool for the management of salivary gland masses. The Milan System provides practical guidance for assessing the ROM; however, diagnostic challenges persist in gray‐zone categories. Therefore, integration of clinical, radiological, and cytological findings is essential for accurate evaluation in these cases. Future multicenter studies with larger case series are warranted to further enhance the diagnostic reliability of the Milan System.
Funding
The authors have nothing to report.
Conflicts of Interest
The authors declare no conflicts of interest.
Data Availability Statement
The data that support the findings of this study are available from the corresponding author upon reasonable request.
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Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Data Availability Statement
The data that support the findings of this study are available from the corresponding author upon reasonable request.