Abstract
The preoperative FNA is an important investigation in the workup of a salivary gland pathology. A preoperative diagnosis is important to plan management and counsel patients accordingly. In this study, we aimed to assess the agreement between the preoperative FNA and the final histopathology report when reported by a head and neck and a non-head and neck pathologist. All patients with major salivary gland neoplasm having undergone a preoperative FNA before surgery from January 2012 to December 2019 at our hospital were included in the study. Analysis was done to check for concordance between head and neck and non-head and neck pathologists of the preoperative FNA and final histopathology. Three hundred and twenty-five patients were included in the study. The preoperative FNA could identify the tumour as benign or malignant in the majority (n = 228, 70.1%). The agreement between the preoperative FNA, frozen section diagnosis and the reporting of grade in the frozen section and the final HPR was slightly better with the head and neck pathologist (kappa = 0.429, kappa = 0.698 and kappa = 0.257), respectively, than with the non-head and neck pathologist (kappa = 0.387, kappa = 0.519 and kappa = 0.158), all of which was statistically significant (p < 0.001). The diagnosis made with the preoperative FNA and reporting in the frozen section had a fair agreement with the final histopathology when reported by a head and neck pathologist in comparison to a non-head and neck pathologist.
Keywords: Fine-needle aspiration cytology, Major salivary gland, Neoplasm, Head and neck pathologists, Non-head and neck pathologists
Introduction
Salivary gland neoplasms are relatively rare tumours of the head and neck region. They account for approximately 6% of all head and neck malignancies [1]. The glands themselves are broadly classified as major and minor salivary glands, each with its unique anatomical variations, a diverse range of histopathological types of tumours and different biological behaviours. After a complete clinical examination, any major salivary gland swelling (neoplasm) requires further investigations to arrive at a diagnosis. Fine-needle aspiration cytology (FNAC) has been commonly used for obtaining a histological diagnosis of salivary gland neoplasms. FNAC is an inexpensive investigation, readily available and convenient to perform; apart from this, it has good diagnostic accuracy [2, 3]. The diagnosis thus obtained helps decide the management of these tumours as well as provides valuable information to assist the clinician in counselling the patients better regarding the prognosis and expected outcomes.
FNAC has been used widely to differentiate neoplastic from non-neoplastic lesions with good accuracy. However, the systemic review and meta-analysis by Schmidt et al.[3] have shown it to be less superior when differentiating benign and malignant neoplasms. This can be attributed to various possibilities such as the diversity and overlapping cytology characteristics of these neoplasms and also the relative rarity of these tumours, which makes it more challenging to obtain diagnostic expertise in reporting these tumours.
This diagnostic challenge led various research groups across the world to come up with various classifications that would help the pathologist to categorize these tumours based on their cytological features. One such system is the Milan system introduced in 2018 [4]. The main aim of this group was to make the reporting of salivary gland neoplasms more standardized leading to better communication among pathologists and clinicians and standardization. However, unlike the Bethesda system used for the cytological diagnosis of thyroid neoplasms, this particular system could not achieve the required sensitivity like the Bethesda system [5]. Inter-observer reproducibility and inter-institutional variations led to lesser use of this system initially. In keeping with the diagnostic challenges, this study attempts to ascertain the impact a pathologist who predominantly reports for head and neck cancer (head and neck pathologists) has in the diagnosis of this diverse group of salivary gland neoplasms.
Patients and Methods
This retrospective study was approved by our institutional review board. All patients with major salivary gland neoplasm, aged 18 years and above, who have undergone surgery at our institute between January 1, 2012, and December 31, 2019, with the availability of preoperative FNAC diagnosis and final histopathology report were included in this study. Patients who underwent preoperative FNAC outside the institute and when these slides were unavailable for review by in-house pathologists were excluded from the study. Minor salivary gland neoplasms, non-salivary gland primaries, i.e. metastasis to the salivary gland from known primaries, and infective and inflammatory lesions were also excluded from the study.
The primary objective of this study was to assess the concordance and/or agreement between preoperative FNAC and the final histopathology report for salivary gland neoplasms between head and neck pathologists and non-head and neck pathologists. The secondary objective was to assess the concordance between frozen section reporting of the primary neoplasm diagnosis and the final histopathology report of the same major salivary gland neoplasm by head and neck and non-head and neck pathologists. Also the concordance of the grading when mentioned in the FNA reports and the grading in frozen section report with the grading on final HPE when reported by head and neck and the non-head and neck pathologists.
In our institute, we have disease management groups (DMG) dedicated to the management of different sites and/or types of malignancies in the body. There are 11 disease management groups head and neck oncology, uro-oncology, thoracic oncology, bone and soft tissue tumours, breast oncology, gynae-oncology, neuro-oncology, gastrointestinal oncology, paediatric solid tumours, paediatric haematolymphoid and adult haematolymphoid. Each DMG has dedicated surgeons, radiation oncologists, medical oncologists, radiologists and pathologists mainly apart from other allied services. Pathologists are given the responsibility for a few (2–3) DMGs predominantly. However, certain sites like head and neck oncology which is one of the common sites of malignancy in our region due to the sheer volume (workload) pathologists whose main DMG is non-head and neck also report certain head- and neck-related pathologies on rotation for timely management of the patients. Keeping this in mind, pathologists were grouped as head and neck pathologists whose main focus of work was in the head and neck DMG and the non-head and neck pathologists for those whose focus of work was predominantly in the non-head and neck DMG. Based on this division, there were 5 head and neck pathologists and 21 non-head and neck pathologists. Among the 5 head and neck pathologists, 3 pathologists had > 10 years’ experience in oncopathology, and two of them had 5–10 years’ experience in oncopathology. Among the 21 non-head and neck pathologists, 10 of them had > 10 years’ experience in oncopathology, one had 5–10 years’ experience, and 10 had up to 5 years of oncopathology experience.
The FNA’s were reported as benign, malignant, inconclusive, and non-diagnostic. A FNA was considered as non-diagnostic if no sufficient material was available for cytopathological assessment or if contaminated by blood. The FNA was considered as inconclusive if the cellularity was sufficient for cytopathological evaluation, but neither a final histotype diagnosis nor clear benign or malignant nature be suggested [6].
Statistical Analysis
Analysis was done using SPSS version 24 (IBM, NY). An agreement analysis was performed to assess preoperative FNAC diagnosis of the primary tumour and the final histopathology reporting, including grading of the tumour between head and neck and non-head and neck pathologists. The analysis was also performed to assess intraoperative frozen section reporting with the final histopathology report. A p value of < 0.05 was considered significant, and a Cohen’s kappa value was used to interpret the agreement between the preoperative FNAC and final histopathology report when reported by head and neck and non-head and neck pathologists. Cohen’s kappa (κ) is a robust statistical tool useful for either interrater or intrarater reliability testing [7].
Results
A total of 436 patients were operated on in the above-mentioned period out of which 325 patients satisfied the eligibility criteria and were included in this study (Fig. 1). The median age of the cohort was 49 years (range, 18–85 years), and the majority were males (n = 192, 59.1%). Most of the patients were treatment-naïve (n = 231, 71.1%), whereas 94 patients (28.9%) had received some form of prior treatment, mostly surgery with or without adjuvant therapy. The parotid gland was the most common site, followed by the submandibular gland and the sublingual gland (Table 1).
Fig. 1.
Flow chart showing the inclusion and exclusion (with reasons) of cases in the study
Table 1.
Demographic, clinical, and treatment-related details
| Factors | Numbers (%) |
|---|---|
| Gender | |
| Male | 192 (59.1%) |
| Female | 133 (40.9%) |
| Comorbidities | |
| Yes | 57 (17.5%) |
| No | 268 (82.5%) |
| Previous treatment | |
| Yes | 94 (28.9%) |
| No | 231 (71.1%) |
| Previous treatment details | |
| Surgery (with/without adjuvant) | 90 (93%) |
| Others | 4 (7%) |
| Site | |
| Parotid | 296 (91.1%) |
| Submandibular gland | 28 (8.6%) |
| Sublingual gland | 1 (0.3%) |
| Surgery | |
| Adequate parotidectomy | 23 (7.1%) |
| Superficial parotidectomy | 128 (39.4%) |
| Total conservative parotidectomy | 69 (21.2%) |
| Radical/extended radical parotidectomy | 74 (22.7%) |
| Submandibular gland excision | 28 (8.6%) |
| Sublingual gland excision | 1 (0.3%) |
| Parapharyngeal mass excision | 2 (0.6%) |
| Neck dissection | |
| Level II sampling | 155 (47.7%) |
| SND | 46 (14.1%) |
| MND | 54 (16.6%) |
| None | 70 (21.5%) |
Head and neck pathologists reported the majority of FNAs (n = 175, 53.8%), followed up closely by non-head and neck pathologists (n = 150, 46.2%). The head and neck pathologists reported on an average 35 cases in comparison to 7 cases reported by every non-head and neck pathologists on an average.
The majority of the FNA were reported as malignant (n = 141, 43.4%) followed by benign (n = 87, 26.8%); the rest were inconclusive (n = 79, 24.3%) and non-diagnostic (n = 18, 5.5%). There was no statistically significant difference between the numbers within the above four categories between the head and neck and the non-head and neck pathologists. Subsequently, all the patients received surgical therapy. Superficial parotidectomy (n = 128, 39.4%) was the most common surgery performed. The majority also underwent a level II sampling as an additional therapeutic measure. Neck dissections were also done wherever indicated (n = 100, 30.7%). Most tumours were reported as low grade (n = 66, 20.3%) on the preoperative FNAC. The head and neck pathologists as compared to the non-head and neck pathologists provided histological grading on the preoperative FNACs (41.9% vs. 32.1%) though this was not statistically significant. This is an important aspect as this helps in counselling the patients regarding the extent of surgery and the possible need for neck dissection preoperatively (Table 2).
Table 2.
Preoperative FNA, intraoperative frozen section, and final histopathology details
| Factors | Numbers (%) |
|---|---|
| Outside FNA diagnosis | |
| Present | 79 (24.3%) |
| Absent | 246 (75.7%) |
| Change in diagnosis (after in-house FNA review) | |
| Yes | 16 (5.5%) |
| No | 63 (19.7%) |
| Not applicable | 246 (74.8%) |
| Preoperative FNA reported by (overall) | |
| Head and neck pathologist | 175 (53.8%) |
| Non-head and neck pathologist | 150 (46.2%) |
| Preoperative FNA report (overall) | |
| Benign | 87 (26.8%) |
| Malignant | 141 (43.4%) |
| Inconclusive | 79 (24.3%) |
| Non-diagnostic | 18 (5.5%) |
| Intraoperative frozen section (for primary diagnosis, including grade) | |
| Done | 131 (40.3%) |
| Not done | 194 (59.7%) |
| Intraoperative frozen section report | |
| Benign | 49 (15.1%) |
| Malignant | 56 (17.2%) |
| Inconclusive/no diagnosis given | 26 (8%) |
| Intraoperative frozen section grading | |
| Low | 9 (2.8%) |
| Intermediate | 2 (0.6%) |
| High | 6 (1.8%) |
| Not reported | 65 (20%) |
| Not applicable (benign) | 49 (15.1%) |
| Intraoperative frozen reported by | |
| Head and neck pathologist | 38 (11.7%) |
| Non-head and neck pathologist | 93 (28.6%) |
| Final histopathology report of primary | |
| Pleomorphic adenoma | 83 (25.5%) |
| Warthin’s tumour | 18 (5.5%) |
| Other benign tumours | 17 (5.2%) |
| Mucoepidermoid carcinoma | 68 (20.9%) |
| Adenoid cystic carcinoma | 28 (8.6%) |
| Adenocarcinoma | 6 (1.8%) |
| Acinic cell carcinoma | 14 (4.3%) |
| Carcinoma ex-pleomorphic adenoma | 23 (7.1%) |
| Salivary duct carcinoma | 18 (5.5%) |
| Squamous cell carcinoma | 8 (2.5%) |
| Mammary analogue secretory carcinoma | 9 (2.8%) |
| Myoepithelial carcinoma | 12 (3.7%) |
| Epithelial–myoepithelial carcinoma | 5 (1.5%) |
| Lymphoma | 4 (1.2%) |
| Lymphoepithelial carcinoma | 5 (1.5%) |
| Other carcinoma | 7 (2.1%) |
| Grade in final report | |
| Low | 39 (12%) |
| Intermediate | 47 (14.5%) |
| High | 73 (22.5%) |
| Not reported | 47 (14.5%) |
| Not applicable | 119 (36.6%) |
| Pathologist reporting final histopathology report | |
| Head and neck pathologists | 135 (41.5%) |
| Non-head and neck pathologists | 190 (58.5%) |
A frozen section facility was utilized in 131 patients (40.3%) with 49 benign and 56 being reported as malignant. The head and neck pathologists reported 38 frozen section specimens, whereas the non-head and neck pathologists reported 93 specimens. Pleomorphic adenoma was the most common benign tumour, and mucoepidermoid carcinoma was the most common malignant tumour in the final histopathology reports (Table 2). Also, the head and neck pathologists reported the grade on the frozen section more frequently (p = 0.03).
The histopathology report was finalized by the head and neck pathologists in 135 (41.5%) patients and by non-head and neck pathologists in 190 (58.5%) patients. The grades in the final histopathology were reported by the head and neck pathologists in 56 (66.7%) patients and non-head and neck pathologists in 88 (72.1%) patients (Table 2). The difference was not statistically significant. The mentioning of the grades in the final histopathology is important in prognosticating the patients and adding adjuvant treatment.
To assess the concordance between the preoperative FNAC diagnosis and the final histopathology report between both the groups, Cohen’s kappa test was used. A score of 0.429 was noted for the head and neck pathologists vs. 0.387 for the non-head and neck pathologists suggesting a fair agreement between the head and neck pathologists.
We also found that the head and neck pathologists had a better concordance (kappa = 0.698, p < 0.001) when looking at the frozen section report with the final histopathology report in comparison to non-head and neck pathologists (kappa = 0.519, p < 0.001). Also, the reporting of the grade of the tumour on the frozen section was often given by the head and neck pathologists (kappa = 0.257, p < 0.001) and matched those with the final histopathology reports in comparison to the non-head and neck pathologists (kappa = 0.158, p < 0.001). This information could be useful for surgeons to take certain important intraoperative decisions.
Discussion
FNAC has gained acceptance as a standard diagnostic modality in the diagnosis of salivary gland neoplasms. Various studies have been conducted to assess its sensitivity and specificity as well as diagnostic accuracy. Sensitivity values ranging from 27 to 97% and specificity values ranging from 84 up to 97% have been reported suggesting FNAC is a fairly accurate diagnostic modality [2, 3]. A study conducted by Dhanani et al. has reported diagnostic accuracy of 95.8% with various studies reporting a range of 84% to 97% [8]. However a non-diagnostic material yield has been considered a drawback of FNAC; this can be reduced by improving the yield of the FNA with better localization with the help of ultrasonography (USG). Lin et al. showed that when a preoperative FNA was reported as malignancy, a higher rate of neck dissection (47% vs 13%, p value = 0.036) was performed upfront, and also there was a higher percentage of clear margins (71% vs 31%, p value = 0.027) [9].
In our study, the non-diagnostic yield was found in 18 (5.5%) patients and inconclusive in 79 (24.3%) patients, which is well within normal standards. As mentioned earlier, this yield may be due to poor localization or entering areas of necrosis or inflammation. Despite its limitations, FNAC is still a very useful diagnostic tool, and to improve its reproducibility and clinical relevance, an international group of pathologists proposed the Milan system for reporting salivary gland cytology report (MSRSGC), published in 2018 [4]. This system is not only attempting to standardize the diagnostic criteria for reporting salivary gland neoplasms but also gives a range of “risk of malignancy” scores for each of the diagnostic categories; however, this system also has certain limitations [10].
Various studies have been conducted to augment the cytological diagnosis with the use of ancillary tests such as immunohistochemistry (IHCs) and various molecular markers. In a review by Jo et al.[11], they have described an array of tests available to assist in specific diagnostic categories such as atypia of undetermined significance (AUS) and salivary gland neoplasm of uncertain malignant potential (SUMP) where the diagnosis needs to be refined.
Farahani et al. [12] in their systematic review and meta-analysis found a total of 622 cases reported as “non-diagnostic” out of 44 studies and the rate of non-diagnostic FNACs ranging from < 1 to 44% with the majority of studies having a non-diagnostic range of < 10%. Other studies have also reported similar rates of non-diagnostic FNAC [13, 14, 15, 16]. Our study was well within this reported range.
In the present study, head and neck pathologists reported 175 preoperative FNACs, whereas non-head and neck pathologists reported 150 FNACs. Within the non-diagnostic and inconclusive category, the head and neck pathologists reported 49 FNACs as inconclusive/non-diagnostic, out of which 25 were benign and 24 were malignant on the final histopathology report. Similarly, the non-head and neck pathologists reported 48 FNACs as inconclusive/non-diagnostic, out of which 16 were benign and 32 were malignant on the final histopathology report. The number of malignancies in the final histopathology report among the inconclusive/non-diagnostic category, when reported by head and neck pathologists, was lower (48.9%) in comparison to the non-head and neck pathologists (66.6%).
We also specifically attempted to ascertain the concordance between the preoperative FNAC diagnosis with the final histopathology report using the kappa value test which is considered superior in assessing the agreement instead of the standard percentage-based scoring and found a fair agreement in both the groups suggesting competence, albeit better agreement with the head and neck pathologists.
The reporting of grades in the FNA, though difficult, could be helpful for the surgeons in counselling the patients further. Reporting the grade in FNA probably may not be possible always and may also be dependent on the experience and expertise of the reporting pathologists apart from the quality of the FNA material available. In our study, the grade was reported in the FNA by the head and neck pathologist more often in comparison to the non-head and neck pathologists, though this association was not statistically significant.
The frozen section has been used as a tool to improve intraoperative decision-making [17, 18, 19]. Various authors including Olsen et al. [12] have described its utility, especially in situations where FNAC-proven benign lesions were found to be malignant on frozen Sects. (11 out of 53 FNACs reported as benign) indicating the need to change to a more aggressive line of treatment. Also, Mantsopoulos et al. reported that the head and neck pathologists were able to detect malignancy as well as identification of histologic subtypes better compared to generalized surgical pathologists [20]. In our study, we found that the head and neck pathologists had a better concordance when looking at the frozen section report with the final histopathology report with only 1 case being reported as benign on the frozen section which was found to be malignant on the final histopathology report.
Reporting the histologic grade of the tumour is important in understanding its characteristics and also in tailoring the treatment plans accordingly. It was found that the head and neck pathologists reported the grading more frequently both on the preoperative FNAC and on the frozen section. In a retrospective study conducted by Lima et al. [21], they found that along with the stage, the grade of the tumour has significant importance in predicting the prognosis of the tumours. The grading not only provides vital information regarding the prognosis but also has a direct correlation with the overall survival, with high-grade tumours having the lowest overall survival rate. In the same study, the 5-year disease-specific survival for 59 high-grade tumour patients was 48%, while for low-grade patients, it was 94%, highlighting the importance of reporting the grade of the tumour.
The strength of the study is that it is probably the first of its kind comparing the agreement between preoperative FNA of major salivary glands reported by head and neck and non-head and neck pathologists with its final histopathology. The limitation of the study is the retrospective nature of the study, thus bringing with it the inherent weakness of such a study design. Also, we have not re-reviewed the FNACs reported by the non-head and neck pathologists by the head and neck pathologists to compare the diagnostic accuracies of these two groups.
Conclusion
This unique study attempted to describe the significant role of a dedicated head and neck pathologist in the management of salivary gland neoplasms. We found the agreement between the preoperative FNAC and the final histopathology report to be almost similar, however, slightly better with the head and neck than with the non-head and neck pathologists. Also, the head and neck pathologists were able to report the grade of the tumours more often than the non-head and neck pathologists in the FNA and the frozen section reports. There was also a better agreement with regard to the frozen section reporting with the final histopathology reports among the head and neck pathologists than the non-head and neck pathologists. Dedicated head and neck pathologists may help in the better reporting of such complex and rarer tumours.
Declarations
Ethics Approval
Approval from our institutes’ ethics committee was taken for this study (Project No: 900660)
Conflict of Interest
The authors declare no competing interests.
Footnotes
Level of evidence: 3
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
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