Study of fine needle aspiration cytology of salivary gland according to the Milan system : D Y Patil Journal of Health Sciences

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Original Articles

Study of fine needle aspiration cytology of salivary gland according to the Milan system

Parmar, Riddhi A1,2; Patel, Jaimin M2; Patel, Keval A2,3,

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D Y Patil Journal of Health Sciences 11(1):p 42-48, January-March 2023. | DOI: 10.4103/DYPJ.DYPJ_5_23
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Abstract

Background: 

Fine-needle aspiration cytology (FNAC) of salivary gland lesions is the initial screening test. The Milan System for Reporting Salivary Gland Cytopathology (MSRSGC) classifies FNAC into six categories, which is a simple, convenient and standardized diagnostic method of reporting and also provides management guidelines. The study was encountered in our tertiary care hospital.

Aims and Objectives: 

To study the cytology of salivary gland lesions by Fine Needle Aspiration Cytology and to classify lesions according to The Milan System for Reporting Salivary Gland Cytopathology (MSRSGC).

Materials and Methods: 

This is a prospective study of 100 patients with clinically enlarged salivary gland presented at the G.K. General Hospital, Bhuj, during April 2019 to March 2020.

Results: 

Of 100 cases, 40 cases were nonneoplastic, 52 cases were neoplastic, and 8 cases were unsatisfactory for evaluation. The category II had 40 cases, out of which chronic sialadenitis was the most common cytological diagnosis (20 cases). There were two case in each category IVb and category V. Category IV had 41 cases on cytology. Category VI had eight cases.

Conclusions: 

It is of particular relevance in the head and neck area because of easy accessibility of the target site minimally invasive procedure, excellent patient compliance and thereby help to avoid surgery in nonneoplastic, inflammatory conditions.

Key Messages:

The present study confirms the usefulness of FNAC as a safe and economic procedure. The high sensitivity, specificity and diagnostic accuracy of FNAC confirm its significant role in association with radiological and clinical findings to provide the best initial assessment which in turn guides the management options.

Introduction

Salivary gland lesions constitute 3%–6% of all lesions of head and neck region.[1] The common presentation is an enlarged mass which is usually accessible for fine needle aspiration cytology (FNAC). The use of aspiration cytology was first reported by Kun in 1847. The procedure was reintroduced in 1930 by Martin and Ellis but the use of FNAC in the head and neck area, especially salivary glands, was promoted in 1950 and 1960 by Eneroth et al.[2] Fine needle aspiration (FNA) is utilized as a preoperative diagnostic technique which is safe, simple, cost effective and widely utilized tool for the diagnosis of salivary gland lesions with diagnostic sensitivity that ranges from 81% to 100%, specificity ranges from 94% to 100% and the accuracy ranges from 61% to 80%.[3]

“The Milan System for Reporting Salivary Gland Cytopathology (MSRSGC)” which includes definitions, diagnostic/morphologic criteria, explanatory notes and a brief management plan for each diagnostic category was published.[4] In this study we have analyzed FNACs of salivary gland lesions according to The Milan system for reporting salivary gland cytopathology and to correlate with their histopathological findings.

Materials and Methods

The present study is conducted in the department of pathology, G K General Hospital, Gujarat Adani Institute of Medical Sciences, Bhuj during April 2019 to March 2020. This is a prospective study that includes patients with salivary gland lesions, irrespective of their age and sex, who were referred to the department of pathology, GKGH Hospital Bhuj for cytological study from ENT/Surgery OPD and those admitted to wards were included. In each patient detailed clinical history was obtained and thorough clinical examination was done prior to procuring sample for cytological study.

FNAs were performed using 22G or 23G needle, with or without an airtight syringe. Few slides were air-dried for Giemsa staining while the rest were immediately fixed in Methanol for Hematoxylin and Eosin and Pap stains. FNAs were reported using MSRSCG system and cancer risk with guidelines for further management were communicated to the surgeon. The recommended diagnostic categories by MSRSCG system and implied risk of malignancy and recommended clinical management are seen in Table 1.[4] The subsequent surgically resected specimen for histopathological examination (HPE) was received in 43 cases. First, a careful gross examination was done. After proper processing of the representative sections, slides were stained with Hematoxylin and Eosin stain. Histopathological categorization was done according to the WHO classification after examining the slides under a light microscope. Cytological and histological findings were evaluated by two separate pathologists. Results of cytology and histopathology were compared and the malignancy risk was calculated.

T1
Table 1::
The milan system for reporting salivary gland cytopathology: implied risk of malignancy and recommended clinical management

Results

A total of 100 cases of fine needle aspirations of salivary gland lesions were collected in the department of pathology, G.K. General Hospital. The age distribution ranged from 15 to 75 years. The mean age of the patient was 43 years. The youngest patient was 15 years old boy while the oldest patient was of 75 years old male. [Table 2] shows age distribution with percentage. Of the 100 patients with thyroid lesions 60 (60%) were males and 40 (40%) were females. The most common site of involvement was the parotid gland (60 cases; 60%), followed by submandibular gland (35 cases; 35%) and minor salivary glands (5 cases; 5%).

T2
Table 2::
Distribution of patients according to age (N= 100)

Of 100 FNACs, eight aspirates (08%) were inadequate for cytological evaluation; hence they were labeled as unsatisfactory smears (Category I). Cases with fluid aspirate from cysts showed cyst macrophages and hemosiderin laden macrophages were reported as cystic degeneration [Figure 1]. Table 3 shows the number of cases and cytopathological diagnosis in each MSRSCG category. The maximum numbers of cases (40 cases [40%]) were seen in the category II. Of 40 cases, 20 cases were chronic sialadenitis showed a ductal cell cluster with chronic inflammatory cells infiltration [Figure 2]. FNA smears showed collections of epithelioid histiocytes in the background of lymphocytes and clusters of benign salivary acini [Figure 3] and hence a differential diagnosis of granulomatous sialadenitis was made. FNAC of reactive lymph node hyperplasia show a mixed population of mostly small and intermediate-size lymphocytes admixed with follicular dendritic cells. [Figure 4] one case (1%) in Category III.

F1
Figure 1::
Case of cystic lesion showed cyst wall lined by hemosiderin laden macrophages (H&E, X100)
T3
Table 3::
Distribution of salivary gland lesions according to MSRSCG system
F2
Figure 2::
Case of chronic sialadenitis showed ductal cells with chronic inflammatory cells infiltration. (H&E, X400)
F3
Figure 3::
Case of granulomatous sialadenitis showed collection of epithelioid histiocytes. (H&E, X400)
F4
Figure 4::
Case of reactive lymph node showed polymorphous population of lymphoid cells comprising of small lymphocytes, centrocytes and centroblasts. (H&E X400)

Out of the 51 salivary gland neoplasms, 39 (39%) cases were in Category Iva and two (2%) cases were in Category IVb. Of 39 cases, 25 cases were of pleomorphic adenoma showing metachromatic fibrillary matrix with a cellular spindled and epithelioid myoepithelial cell [Figure 5A and B]. Eleven cases were diagnosed as Warthin tumor (WT) showing classic cytomorphologic features consisting of background lymphocytes and groups of oncocytic epithelial cells with abundant granular cytoplasm and well-defined borders [Figure 6]. These category-wise results are tabulated in Table 3.

F5
Figure 5::
(A&B): Case of pleomorphic adenoma showed metachromatic fibrillary matrix with a cellular spindled and epithelioid myoepithelial cell. (H&E, X400)
F6
Figure 6::
Case of warthin tumor showed groups of oncocytic epithelial cells with abundant granular cytoplasm along with lymphocytic infiltration. (MGG, X400)

Category V (Suspicious for malignancy) two (2%) cases were diagnosed in this category.

Category VI (Malignant) eight (8%) cases were diagnosed. One case of adenoid cystic carcinoma showing small uniform, basaloid cells with coarse chromatin, round hyperchromatic nuclei with microcystic sieve like spaces [Figure 7A] and shows abundant acellular homogeneous matrix with sharp borders. Basaloid tumor cells form a syncytial smear surrounding the matrix material [Figure 7B]. Two cases of acinic cell carcinoma showing tumor cells with low nuclear–cytoplasmic (N:C) ratio and Uniform, round nuclei with basophilic cytoplasm forming microcystic pattern [Figure 8].

F7
Figure 7::
Case of adenoid cystic carcinoma showing small uniform, basaloid cells with coarse chromatin, round hyperchromatic nuclei with microcystic sieve like spaces (A) (MGG, X100) and shows abundant acellular homogeneous matrix with sharp borders. Basaloid tumor cells form a syncytial smear surrounding the matrix material (B). (MGG, X400)
F8
Figure 8::
Case of acinic cell carcinoma showed groups of tumor cells with uniform, round nuclei with basophilic cytoplasm. (MGG, X100)

Histological follow-up was available in 43 cases and available histopathological comparison according to MSRSGC and is shown in the above [Table 4]. In category 1 (nondiagnostic), of 8, follow-up was available in only two and out of these, one case turned out to be chronic sialadenitis and another one as Acinic cell carcinoma.

T4
Table 4::
The cytology histology correlation and risk of malignancy

In category 2 (nonneoplastic), histopathological follow-up of 15 cases were available; out of total 40 cases, among which four cases of benign tumor and three cases were malignant reported. The remaining eight cases were nonneoplastic lesions, five of which were chronic sialadenitis and three of which were acute suppurative sialadenitis. Risk of malignancy accounted to 7.5% [Table 4].

We lost the follow of one patient diagnosed as Lymphoepithelial cyst/ Warthin tumor in category 3 (atypia of undetermined significance).

In category 4a had histological follow-up of 15 cases of 39 cases. Twenty-five cases of cytologically diagnosed pleomorphic adenoma, among which nine cases had histopathological follow-up, showed similar concordance on histopathology, except in two cases, which turned out to be basal cell adenocarcinoma and acinic cell carcinoma. Risk of malignancy accounted to 5.1% [Table 4].

In category 4b had both cases histological follow-up were one diagnosed as Mucoepidermoid carcinoma. Risk of malignancy accounted to 50% [Table 4].

In category 5 (Suspicious for malignancy), histopathological follow-up was available in only one case of two cases, and diagnosed as Acinic cell carcinoma. Risk of malignancy accounted to 50% [Table 4].

In category 6 had histological follow-up of all eight cases and showed similar concordance on histopathology. Risk of malignancy accounted to 100% [Table 4].

Discussion

FNAC has been in use around the world for over four decades as a screening/diagnostic tool. The use of FNAC is justified owing to the procedure being inexpensive, minimally invasive, with minimal complications, and for giving an early preoperative diagnosis for most of the salivary gland lesions. However, in lesions showing diverse morphology and various forms of metaplasia, cytomorphological interpretation tends to become challenging. Thus, uniform reporting is important for patient’s further management.

In our study, the age of patients ranges from 15 to 75 years with mean age of 43 years. The highest incidence of salivary gland lesion was found in 31–40 age group whereas Karuna et al.[5] reported highest incidence in 31–40 age group, which is in concordance with our study. While Patil et al.[6] reported highest incidence in 41–50 age group. The male-to-female ratio in our study was 1.5:1 similar to that reported by Rohilla et al.[7] which was 1.7:1, whereas in study by Karuna et al.[5] it was reported to be 2.2:1. In our study, parotid gland was the most common salivary gland involved (60%) followed by submandibular gland (35%) and minor salivary gland (5%) similar to that observed by Rohilla et al.[7] (61.3%, 35.7% and 3% respectively) and Karuna et al.[5] (59.05%, 31.43%, and 9.52%, respectively).

In the present study, eight cases (8%) were unsatisfactory for diagnosis (Category I) due to scant cellularity on aspirate. The most common reason for the inadequacy was fluid aspirate from a cystic lesion. The adequacy rate of the current study were in concordance with studies by Patil et al.[6] (10.20%), Singh et al.[8] (12.15%) and Kala et al.[9] (6.1%), while showing discordance with studies by Rohila et al.[7] (2.2%), Pukhrambam et al.[10] (1.4%), and Singh et al.[11] (18.7%) [Table 5].

T5
Table 5::
Comparison of incidence in various study according to MSRSCG system

Nonneoplastic lesions or Category II were the most common salivary gland lesions in the present study (40%). On review of literature, similar distribution of Category II cases were reported by Patil et al.[6] (49.65%), Singh et al.[8] (41.96%) and Kala et al.[9] (38.2%) and Singh G et al.[11] (31.7%), though a higher proportion was reported by Rohilla et al.[7] (55.8%) Pukhrambam et al.[10] (52.9%). Chronic sialadenitis was the most common cytological diagnosis in our study, like the previous reports.

AUS category or Category III in the MSRSGC is defined as a salivary gland FNA that lacks either qualitative or quantitative cytomorphologic features to be diagnosed with confidence as nonneoplastic or neoplastic. A diagnosis of AUS should lead to careful correlation with clinical and radiologic findings. Depending upon the overall risk assessment, it may result in a repeat FNA, core-needle biopsy, open biopsy, or surgical excision. In aspirates with an atypical lymphoid population, flow cytometry, immunochemistry, or tissue biopsy should be considered to rule out a lymphoproliferative disorder.[4] In present study, only one case (1%) was categorized into Category III. On review of literature, similar distribution of Category III cases was reported by Singh et al.[8] (1.56%) and Kala et al.[9] (2.7%), Singh et al.[11] (0.81%) and Karuna et al.[5] (2.85%), though a higher proportion was reported by Pukhrambam et al.[10] (8.6%).

Neoplastic category IVa had 39 cases (39%) among which majority of cases were of Pleomorphic adenoma 25 cases (64.10%) followed by 11 cases (28.20%) of Warthin’s tumor. Similar distribution were reported by Patil et al.[6] (34%), Rohilla et al.[7] (40.4%), Singh et al.[8] (32.94%), Kala et al.[9] (33.4%) and Singh et al.[11] (39.8%), although a higher proportion was reported by Karuna et al.[5] (51.43%). Singh et al.[8] had 84 cases (32.94%) among which majority cases were of pleomorphic adenoma comprising of 69 cases (84.14%) followed by 11 cases (13.41%) of Warthin’s tumor, which shows concordance with our study.

Neoplastic category IVb had two cases. Similar observations were reported by Singh et al.[8] (2.38%), Kala et al.[9] (2%), Pukhrambam et al.[10] (3%) and Singh et al.[11] (1.63%), although a higher incidence was reported by Karuna et al.[5] (5.71%)

In category V (suspicious for malignancy), only two cases were reported. Similar observation was reported by Singh et al.[8] (2.74%), Kala et al.[9] (2%), Pukhrambam et al.[10] (3%), and Singh et al.[11] (1.63%), although a higher incidence was reported by Karuna et al.[5] (4.76%).

In present study, eight cases (8%) were diagnosed as malignant salivary gland lesions in category VI, which is in concordance with study reported by Patil et al.[6] (4.76%), Singh et al.[8] (8.62%), Pukhrambam et al.[10] (7.6%) and Singh et al.[11] (5.69%), while higher incidence were reported by Karuna et al.[5] (16.20%) and Rohilla et al.[7] (23.9%)

The risk of malignancy value for each category was calculated as 12.5%, 7.5%, 5.1%, 50%, 50% and 100%, respectively. The ROM values of similar studies are summarized in Table 6. These findings are in concordance with studies done by Faquin et al.,[4] Rossi et al.,[12] Rohilla et al.,[7] and Kala et al.[9] In the study of Milan group, these rates were found as 25%, 10%, 20%, <5%, 35%, 50%, and 90%, respectively.

T6
Table 6::
The risk of malignancy (ROM) for each diagnostic category in published other studies

Application of Milan system for reporting salivary gland lesions brings uniformity and it eases clinicians in appropriate management.

Conclusion

The present study confirms the usefulness of FNAC as a safe and economic procedure in distinguishing between benign and malignant salivary gland lesions, which are of utmost value in planning the further management of the patient.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

References

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    Keywords:

    Fine needle aspiration cytology; Milan system; salivary gland

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