|Ahead of print publication
Evaluation of thyroid lesions by the bethesda system for reporting thyroid cytopathology
Syed Asif Hashmi1, Monika Aggrawal2, Rahul Pandey3, Deepika Gulati2, Inam Danish Khan2
1 Department of Laboratory Sciences, Military Hospital, Jhansi, Uttar Pradesh, India
2 Department of Laboratory Sciences and Molecular Medicine, Base Hospital, New Delhi, India
3 Department of Surgery, Armed Forces Medical College, Pune, Maharashtra, India
|Date of Submission||20-May-2022|
|Date of Decision||21-Jun-2022|
|Date of Acceptance||25-Jun-2022|
|Date of Web Publication||05-Oct-2022|
Department of Laboratory Sciences and Molecular Medicine, Base Hospital, Delhi Cantt, New Delhi - 110 010
Source of Support: None, Conflict of Interest: None
Introduction: Thyroid swellings are one of the most commonly encountered lesions with most of the thyroid swellings being benign. The cancerous lesions of the thyroid also present as nodules or masses and pose a diagnostic challenge. The thyroid cytology reporting system has been inconsistent with the use of various terminologies. The Bethesda System for Reporting Thyroid Cytopathology (TBSRTC) was introduced in 2007 to bring about uniformity in reporting of thyroid lesions. Aim: This study aimed to compare conventional reporting with TBSRTC. Materials and Methods: A retrospective study was done in which 6 years of data were retrieved. Cytology slides were reviewed and categorized as per the TBSRTC and compared with other studies. Results: There were numerous categories in the conventional thyroid fine-needle aspiration cytology reporting system which has been reduced to six categories in TBSRTC. TBSRTC has also streamlined the reporting removing the confusion among cytologists and clinicians. Conclusion: TBSRTC is consistent and reproducible and should be used as a standard method of reporting.
Keywords: Conventional reporting, the Bethesda System for Reporting Thyroid Cytopathology, thyroid fine-needle aspiration cytology
| Introduction|| |
Thyroid swellings are one of the most commonly encountered lesions among neck swellings in the outpatient department of any hospital. Most of the thyroid swellings are benign with goiter being most frequent. Iodine deficiency disorders are the most common cause of goiter resulting in approximately 200 million people at risk in India. In India, 263 out of 325 districts are endemic for goiter. The cancerous lesions of the thyroid also present as nodules or masses and pose a diagnostic challenge. The importance lies in detecting the incidence of cancers in these thyroid nodules. Thyroid malignancies are the most common malignancies of endocrine organs. It is estimated that thyroid cancers are the 7th most common cancer in females and the 14th most common in males. The incidence is approximately 1%–5% in females and 2% in males. In India, the age-adjusted incidence of thyroid cancer is approximately 1 per 100000 in males and 1.8 per 100000 in the female population. As per 3 year reports of the National Cancer Registry Program of the Indian Council of Medical Research based on population-based cancer registries 2012–2014 published by the National Centre for Disease Informatics and Research the incidence is much higher in women of Arunachal Pradesh and Kerala.
Fine-needle aspiration cytology (FNAC) is one of the most convenient, minimally invasive diagnostic procedures with a high degree of accuracy. It is also safe, cost-effective with rapid results, and distinguishes between benign and malignant lesions with reasonable certainty. This has a profound impact on the management of the patients as it categorizes them and considerably reduces the number of unnecessary surgeries. However, it is not always possible to reach a conclusive diagnosis, particularly in cases of follicular neoplasm (FN) which needs to be distinguished from multinodular goiter. The thyroid cytology reporting system has been inconsistent with the use of various terminologies creating confusion among clinicians. It is also marred by inter- and intra-observer variability. To bring uniformity of reporting, the Bethesda System for Reporting Thyroid Cytopathology (TBSRTC) was introduced in 2007. The TBSRTC system divides thyroid cytology reporting into six categories, namely nondiagnostic, benign, atypia of unknown significance, FN including suspicious of FN, suspicious of malignancy, and malignant. There are other reporting methods such as the Royal College of Pathologists guidelines on thyroid cytology which categorizes thyroid cytology reporting into five categories from Thy 1 to Thy 5, i.e., nondiagnostic, nonneoplastic, neoplasm possible, suspicious of malignancy, and malignant.
| Materials and Methods|| |
This retrospective study was conducted with materials taken over a period of 6 years from April 2013 to April 2019 in an apex tertiary care hospital in Northern India. The study was done on the FNAC of thyroid lesions with a total of 620 cases who underwent the FNA procedure. The FNA slides were retrieved from the archives and were evaluated by two experienced pathologists who classified the conventional findings into the categories of TBSRTC.
| Results|| |
These cases were originally classified as per the conventional system by various pathologists as described in [Table 1]. In our study, of 620 cases, 566 (91.28%) cases were benign lesions. Among the benign lesions, maximum cases were diagnosed as colloid goiter which constituted 344 cases (55.49%), followed by lymphocytic thyroiditis –90 cases (14.51%), colloid goiter with cystic change –74 cases (11.94%), Hashimoto's thyroiditis –41 cases (6.61%), and colloid cyst/inadequate –13 cases (2.09%). Four cases (0.64%) were diagnosed as granulomatous thyroiditis. The total number of malignant lesions was 54 (8.72%). Out of these 54 cases, the most common diagnosis was FN including suggestive of FN, i.e., 28 (4.52%) cases. Other cases were of Hurthle cell neoplasm –5 cases (0.81%), papillary carcinoma –8 cases (1.29%), and anaplastic carcinoma –2 cases (0.32%) with 1 case (0.16%) of medullary carcinoma. The diagnosis of suspicious of malignancy was given in a total of 10 cases (1.62%). The diagnosis of atypia of undetermined significance was not given in any case.
|Table 1: Different categories of cases as per the conventional system of reporting thyroid cytology|
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The reclassification of the thyroid lesions in these 620 cases was done using the Bethesda system of thyroid cytology reporting. The lesions diagnosed as suspicious of malignancy (10 cases), on re-evaluation as per the Bethesda guidelines were classified as atypia of undetermined significance in five cases and an equal number of cases were diagnosed as suspicious of malignancy. The different diagnosis offered in the conventional system in 12 categories as shown in [Figure 1] was placed in six different categories as per the TBSRTC system as shown in [Figure 2].
|Figure 1: Percentage of thyroid cytology cases as per the conventional reporting system|
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|Figure 2: Percentage of thyroid cytology cases as per TBSRTC system. TBSRTC: The Bethesda System of Reporting Thyroid Cytopathology|
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After reclassification of the thyroid lesions as per TBSRTC, the most common category as per the Bethesda system of thyroid cytology was benign lesions of the thyroid (Cat 2) 89.19%. This was followed by FN or suspicious of FN/Hurthle cell neoplasm or suspicious of Hurthle cell neoplasm (Cat 4) 5.32%. The number of cases falling under unsatisfactory (Cat 1) was 2.1%. The total number of cases in the malignant category (Cat 6) was 1.78%. The cases in atypia of undetermined significance (Cat 3) and suspicious of malignancy (Cat 5) were 0.81% each.
| Discussion|| |
This study included a total of 620 patients whose thyroid FNAC smears were evaluated. Majority of these patients were female (65%) with an age range from 15 years to 69 years as evident from [Table 2], the maximum number of cases was benign lesions (89.19%), whereas a total number of cases of FN or suspicious of FN/suspicious of malignancy/malignant category constituted just 7.91%. The FNA cytology was inadequate in 2.09% of cases. Our results were compared with other studies done in various other institutes from different regions of India. The comparison of different studies as per the TBSRTC is shown in [Table 3].
|Table 2: Classification as per the Bethesda system of thyroid cytology reporting (n=620)|
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|Table 3: Comparison among various studies done in India as per the Bethesda System for Reporting Thyroid Cytopathology|
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Only 13 cases were diagnosed as nondiagnostic, comprising only 2.09% of cases. Verma et al. had reported a nearly similar incidence of 2.5% in their study. It is low in comparison to other studies of Mehra and Verma, Mahajan et al., and Laishram et al. but higher than studies of Mondal et al. Nondiagnostic aspirates are those which do not fulfill the criteria for adequacy of thyroid FNAC, i.e., the FNA contains fewer than six follicular groups, each of which contains ten or more well-preserved epithelial cells, inevitably limiting definitive cytologic interpretation.,, Nondiagnostic aspirates can be significantly reduced by repeating the procedure under ultrasound guidance. With the use of ultrasound guidance, Carmeci et al. reported a reduction in the inadequate specimen rate from 16% to 7%. Similarly, Danese et al. reported an inadequacy rate of only 3.5% with the use of ultrasonography guidance in thyroid FNAC.
The benign category has a maximum number of cases and our result is comparable with the results of other studies as shown in [Table 3]. The meta-analysis done by Agarwal and Jain also showed that the percentage of benign lesions in the Indian population is highest. Different studies also show similar incidence in this category ranging between 80% and 90%. However, majority of the studies have found the incidence to be around 89%. The increased incidence of benign lesions in India is probably due to large endemic areas of iodine deficiency. The incidence is particularly high in the Himalayan and sub-Himalayan regions.
The total numbers of cases in category 3, i.e., atypia of undetermined significance were just 0.8% of cases. This category has been reserved for cytology specimens that contain cells with architectural and/or nuclear atypia that is not sufficient to be classified as suspicious for an FN. In our study, we found only five cases in this category. Meta-analysis done by Shipra et al. also shows that Category 3 is the most heterogeneous category in predicting the risk of malignancy. It is recommended that discussion among the pathologist, clinicians, and radiologist should take place on a case-to-case basis to determine the course of follow-up and optimum treatment regime. This will considerably improve the patient outcome.
A total of 33 (5.32%) cases were found showing atypia with follicular pattern and were placed in suspicious for FN. The goal of this category is to identify all potential follicular carcinomas and refer them for surgery. As these cytomorphological features do not permit distinction between follicular adenoma (FA) and follicular carcinoma, they are reportable as FN or suspicious for follicular neoplasm.
The diagnosis of malignancy cannot be made with reasonable certainty if the sample has a sparse follicular cell population or there are only one or two characteristics of malignancy present and they are only focal and not widespread throughout the follicular cell population. In our study, we found five (0.80%) cases in this category. These cases were suspicious to have papillary carcinoma but out of these five cases, only two showed cytological features without architecture predominance. One of the cases showed papillary fragments without definite nuclear features. Two cases were suspicious for malignancy due to sparse cellularity, and a definite diagnosis could not be offered.
The malignant category is used whenever the cytomorphologic features are indicative of malignancy. Approximately 3%–7% of thyroids FNAs have conclusive features of malignancy, and most of these lesions are papillary carcinomas. Malignant lesions are usually treated by total/subtotal thyroidectomy. In our study, 11 (1.78%) cases fell under this category. Cases definitely diagnosed as malignant were papillary carcinoma of the thyroid, medullary carcinoma, and anaplastic carcinoma. Our results in this category are less in comparison to studies done by Verma et al. (6%), Mondal et al. (4.7%), and Mahajan et al.(9.8%).,, Nina et al. reported a similar incidence of 1.78% in the malignant category whereas Laishram et al. and P Mehra et al. reported the incidence of a malignant lesion as 2.2% each in their respective studies.,, Histopathological correlation was possible only in 15 cases that were operated in our institution and hemithyroidectomy/thyroidectomy specimens were sent for histopathology reporting. Out of these 15 cases, three cases were of Papillary carcinoma, one case of papillary microcarcinoma, four cases of follicular variant of papillary carcinoma, six cases of FA, and one case of Hurthle cell variant of follicular carcinoma.
The incidence of benign (89.19%) and malignant (1.78%) cases as per TBSRTC was comparable with other studies done by Verma et al., Mondal et al., Mehra et al., Mahajan et al., Laishram et al., Kasliwal et al. and also by the metanalysis done by Shipra A et al.,,,,, The overall incidence of benign lesions in most of the studies ranged from 80 to 90%. The incidence of malignant lesions varied in the range from 1.7% to 10%. Overall this study has similar findings when compared with various other studies on thyroid cytology as per TSBRTC guidelines.
Meta-analysis done by Agarwal and Jain among the Indian population showed that thyroid FNA reporting uses a range of formats. These include descriptive reporting, the use of histopathology equivalents, and variably tiered classification systems, ranging from just two categories (nonneoplastic and neoplastic) to four or five categories with the use of a range of formats. Gray zone lesions of cytodiagnostic categories such as hypercellular colloid goiter versus FN, hyperplastic thyroid nodules versus FA, papillary hyperplasia versus papillary thyroid carcinoma, or reactive change versus papillary thyroid carcinoma do not provide management guidelines to clinicians. Hence, a universal system of reporting is required. The Bethesda system of thyroid cytology, i.e., TBSRTC is currently the most widely used reporting system with different studies showing very good efficacy and inter-observer concordance.
Similarly, a meta-analysis done by Bongiovanni et al. also showed high sensitivity and high net predictive value using the Bethesda system concluding that TBSRTC has proven to be an effective and robust thyroid FNA classification scheme to guide the clinical management of patients with thyroid nodules. The findings of this analysis also show a growing trend among institutions both nationally and worldwide of adopting this reporting system to provide clinicians with cytopathology reports that are clear and comprehensible and permit comparisons and performance evaluations on a larger scale.
| Conclusion|| |
Thyroid cytopathology reporting requires consistent and reproducible diagnostic terminology. We also found that the classification of the spectrum of lesions in the FNAC of the thyroid should be done as per the Bethesda guidelines to have uniformity of diagnosis. It improves the quality of reporting by decreasing diagnostic discrepancies. The practice of this flexible framework will facilitate communication among cytopathologists, endocrinologists, surgeons, radiologists, and other health-care providers. It will also facilitate cytologic-histologic correlation of different thyroid diseases; facilitate research into the diagnosis of thyroid disorders, and allow easy and reliable sharing of data from different institutions for national and international collaborative studies.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
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[Figure 1], [Figure 2]
[Table 1], [Table 2], [Table 3]