|Year : 2019 | Volume
| Issue : 2 | Page : 74-81
Role of Bethesda system for reporting thyroid lesion and its correlation with histopathological diagnosis
Deepika Agrawal, Arvind S Bhake, Naincy Rastogi, Sheronica Laishram, Akanksha Wankhade, A Agarwal
Department of Pathology, Jawaharlal Nehru Medical College, Datta Meghe Institute of Medical Sciences (DU), Wardha, Maharashtra, India
|Date of Submission||01-Nov-2018|
|Date of Decision||08-Dec-2018|
|Date of Acceptance||20-Feb-2019|
|Date of Web Publication||25-Nov-2019|
Dr. Deepika Agrawal
Department of Pathology, Jawaharlal Nehru Medical College, Datta Meghe Institute of Medical Sciences (DU), Sawangi (Meghe), Wardha, Maharashtra
Source of Support: None, Conflict of Interest: None
Introduction: Interestingly enough, while TBS is forging ahead to bring about uniformity a thyroid FNA cytology reporting, a similar milestone has also been reported with an application of United Kingdom (UK-RC path system or BTA/RC Path) for reporting thyroid FNA cytology. It achieved practicing activism in 2003 and later got modified in the year 2009 & 2016. The TBS and RC path system being contemporary system of reporting thyroid cytopathology, uniform system of reporting cytopathology of nodular thyroid lesion still is not achieved but activated. Aim: To study the nodular thyroid lesions on FNAC by reporting system of TBSRTC and UK RC Path. Objectives: To compare the categories of the Bethesda system with contemporary categories of UK Royal college of pathologist for cytomorphological diagnosis and overlaps as well as with conventional reporting system and to compare with tissue diagnosis of surgically resected specimen of nodular thyroid lesions for its malignancy risk. Material and Methods: This study is hospital-based observational prospective and analytic study including 255 patients with nodular thyroid lesion. FNAC were carried out with or without under the guidance of sonography. The staining performed were conventional for smears of the aspirate. The smears were classified and categorized by two systems, TBSRTC and UK-RC path system of reporting thyroid lesion. The tissue diagnosis was done for the surgically resected specimens of nodular thyroid lesion in case of patient who underwent surgery. The values of comparative statistics were bought out. Observations: Females predominated over males. The distribution of cases for into the categories of TBSRTC and UK RC Path were as follow: category I/Thy1- 23, category II/Thy2-156, category III/Thy 3a-21/19, category IV/Thy3f-22/24, category V/Thy4-21, category VI/Thy5-16. There were 57 patients underwent surgical intervention in form of total or partial thyroidectomy or lobectomy and had available histopathological examination reports for cyto-histopathology co-relation. Values of comparative analysis show high NPV, PPV and high values of specificity, as compared to conventional. Conclusion: TBSRTC and UK RC path for reporting thyroid cytology are suitable for reporting thyroid nodular lesions on FNAC because of uniformity of nomenclature categories and implication at management with high correlation percentile with subsequent surgically resected specimen of thyroid.
Keywords: Nodular thyroid lesion, TBSRTC, United Kingdom RC path
|How to cite this article:|
Agrawal D, Bhake AS, Rastogi N, Laishram S, Wankhade A, Agarwal A. Role of Bethesda system for reporting thyroid lesion and its correlation with histopathological diagnosis. J Datta Meghe Inst Med Sci Univ 2019;14:74-81
|How to cite this URL:|
Agrawal D, Bhake AS, Rastogi N, Laishram S, Wankhade A, Agarwal A. Role of Bethesda system for reporting thyroid lesion and its correlation with histopathological diagnosis. J Datta Meghe Inst Med Sci Univ [serial online] 2019 [cited 2020 Feb 20];14:74-81. Available from: http://www.journaldmims.com/text.asp?2019/14/2/74/271556
| Introduction|| |
Ambiguity for the diagnosis in the reports of fine-needle aspiration cytology (FNAC) of thyroid nodular lesions have been a treating dilemma for surgeons and clinicians over a past few decades. In recognition of role, the thyroid FNA has an impact in the clinical management of a patient with thyroid pathology; the last few years saw the deliberation for unifying the system for reporting thyroid FNA. One such attempt to relook the reporting of cytopathology of thyroid nodular lesions assessed on FNAC was a decade earlier under aguis of the National Cancer Institute (NCI) that hosted “NCI thyroid FNA state of science conference” in 2007 in Bethesda by Andria Abati., The objective of it was to address terminology and other usage related to thyroid FNA that would have served at treatment and follow-up. In context to pros and cons of TBSRTC, the experiences have recently published as commentary for proposed modifications and updates for the 2nd edition from an international panel in 2016. These proposed modification and updates offered their comments for all the classes, hopefully, to be included in the 2nd edition of TBSRTC in 2018. Interestingly enough, while TBS is forging ahead to bring about uniformity a thyroid FNA cytology reporting, a similar milestone has also been reported with an application of the United Kingdom (UK)-RC path system (BTA/RC Path) for reporting thyroid FNA cytology.,, It achieved practicing activism in 2003 and later got modified in the year 2009 and 2016. The TBS and RC path system being contemporary system of reporting thyroid cytopathology, uniform system of reporting cytopathology of nodular thyroid lesion still is not achieved but activated. The present work over the reporting of thyroid cytopathology of thyroid nodular lesion on FNAC in Indian literature is still debated. With this background, the present work aims to study the nodular thyroid lesions on FNAC by reporting system of TBSRTC and UK-RC Path.
| Materials and Methods|| |
The study was carried out for 2 years from August 2016 to July 2018 in the Department of Pathology, JNMC, Sawangi (Meghe), Wardha, Maharashtra, India, with referral from the Department of Surgery, ENT followed by Medicine. The present study was cleared by Institutional Ethics Committee. This study is hospital-based observational prospective and analytic study, comprised of 255 patients. The study included patients presenting with nodular thyroid lesion on clinical examination or on ultrasonography and who are not on treatment for thyroid nodule. The patients who were previously operated for thyroid nodular lesion or undergone FNAC of thyroid nodules or have contradiction for the procedure of FNAC of nodular thyroid lesion were excluded for the patients. These patients were recorded for their preliminary clinical and personal data. A complete blood count of all the patients was recorded. The laboratory values of T3,T4, and thyroid stimulating hormone (TSH) in available cases were also recorded. FNAC was carried out with or without under the guidance of sonography under aseptic condition. The staining performed was conventional for smears of the aspirate. The smears were classified and categorized by two systems, TBSRTC and UK-RC path system of reporting thyroid lesion. The operating surgeons decided on surgery of nodular thyroid lesion categorization as entertained in cytopathology report by conventional reporting, TBSRTC, UK-RC path. The tissue diagnosis was done for the surgically resected specimens of nodular thyroid lesion in case of the patient who underwent surgery. The sensitivity, specificity, positive predictive value (PPV), and negative predictive value (NPV) of reporting system of TBSRTC, UK-RC Path, and conventional in comparison to surgical specimen diagnosis of nodular thyroid lesion were carried out. The calculation of surgical rate, malignancy rate, and implied risk of malignancy by TBSRTC was done.
| Results|| |
The age of the patients ranged from 7 to 81 years. The majority of patient recruited belonged to the age group of 31–50 years. The female predominated over the male in proportion of 5.2:1. The laboratory values of T3, T4, and TSH were available in 57 (22.35%) patients included in the study. The frequency of patients included in the present study observed 37 (64.91%) patients of euthyroid state followed by 14 (24.56%) hyperthyroid state and 6 (10.52%) patients with hypothyroid state. The patients of nodular thyroid lesion with ultrasonography done in 78 (30.58%) patients were also assessed for features such as margin, shape, size, composition, echogenicity, and/or calcification if made available. The findings of ultrasonography of nodular thyroid lesion showed 72 (92.3%) patients who were reported as nonneoplastic nodule one patient was reported as benign, neoplastic nodule, and 6 (7.7%) patients were reported as malignant. The distribution of cytological diagnosis of nodular thyroid lesion by conventional reporting system is depicted in [Table 1]. The distribution of cytological diagnosis of nodular thyroid lesion by TBSRTC by reference  laid out criteria is depicted in [Table 2]. The distribution of cytological diagnosis of nodular thyroid lesion by the UK-RC Path by reference  laid out criteria depicted in [Table 3]. The observation of categories by UK-RC Path was simulating with categories of TBSRTC in all patients except in two patients who were grouped under category III by TBSRTC while according to the UK-RC Path system were grouped as Thy3f, for whom no follow-up data were available. The other categories show parallel results, i.e., in Category I/Thy1, II/Thy2, V/Thy4, and VI/Thy5 for the comparison of cytodiagnosis by TBSRTC and UK-RC Path. However, when compared with conventional system, the smears of Category II/Thy2, Category III/Thy3a, and Category V/Thy 4 of TBSRTC/UK-RC Path were classified as nonneoplastic lesion. The cases of Category IV/Thy 3f were classed as benign neoplastic.
|Table 1: Distribution of cytological diagnosis of NTL by conventional reporting system|
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|Table 3: Distribution of cytological diagnosis by United Kingdom/RC path (n=255)|
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There were 57 patients underwent surgical intervention in the form of total or partial thyroidectomy or lobectomy and had available histopathological examination reports for cytohistopathology correlation. The further distribution of histopathology diagnosis of nodular thyroid lesion according to categories of TBSRTC and UK-RC Path is depicted in [Table 4]. The highest frequency of surgery was done in Category II/Thy 2 (23, 40.35%) followed by Category III/Thy3a (12, 21.05%), V/Thy4 (n = 8, 14.04%), and Category VI/Thy5 (n = 8, 14.04%). There were 113 patients (no surgery) of which surgery was either awaited, or surgery was not planned and 85 patients (unknown) who were lost to follow-up. Hence, the correlation with histopathology was not possible in these patients.
Values of comparison for categories of TBS/UK-RC Path and conventional were as follows: FP, F. N, TP, TN, specificity, sensitivity, PPV, and NPV which were significant at its implication [Table 5]. The highest implied risk of malignancy is associated with category V and category VI of TBSRTC whereas the lowest implied risk of malignancy is associated with Category I and Category II of TBSRTC, which were in the range of the implied risk stated by TBS [Table 6].
|Table 6: Category-wise surgical rate and malignancy rate (%) (+ Implied risk of malignancy by TBS)|
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| Discussion|| |
The studies on FNAC over nodular thyroid lesion reviewed for the present work, have observed that nodular thyroid pathology was maximally distributed in the age group of 31–40 years.,,,, Similar finding was observed in the present study. The female preponderance at the suffering of nodular thyroid lesion is known.,,,,,,,,,,,, The female to male ratio of 5.2:1 in the present study was similar to studies quoted by Patel et al. (5.53:1), Bhat et al. (6:2), Hajmanoochehri and Rabiee (5.31:1) and Khadatkar et al.(5:1).,,,
The T3, T4, TSH value was available in 57 patients of which maximum were euthyroid and least were hypothyroid. The finding of hormonal assessment is similar to one quoted by Khadatkar et al. and Sawarkar et al. The study of Patel et al. at hormonal assessment of nodular thyroid lesions cited hyperthyroid states more common than others which is contrary to the present study observation.,
The present study by conventional cytodiagnosis otherwise referred as pre-Bethesda reporting system of nodular thyroid lesion has the categories of unsatisfactory, nonneoplastic, benign, and malignant neoplastic categorization. This has enabled the reporting of thyroid cytomorphology to acceptable level but has been criticized for heterogeneity of terminologist, the cytomorphology overlaps for specific diagnosis, and the indication for treatment guidelines.,,,
The conventional reporting system has thrust more on individual cytomorphology character for the specific lesion of thyroid but is criticized and is therefore under scrutiny on to a count: (1) the absence of the category of atypical cytomorphology which is by few authors referred as the category of indeterminate cytomorphology and (2) the follicular neoplasm which were not further segregated. The present study by following three broad categories of conventional cytomorphology reporting had 23 (9.02%) unsatisfactory cytology, 214 (83.92%) nonneoplastic cytology, and 18 (7.06%) neoplastic which included benign and malignant cytodiagnosis. The similar report of devoicing the conventional cytomorphology patterns of nodular thyroid lesion has been reported by Patel et al. which has similar distribution of percentage for the categories as 15 (7.73%) inadequate, 180 (92.78%) non-neoplastic, 10 (5.16%) neoplastic, and 4 (2.06%) others.
The study of Khadatkar et al. mentioned about neoplastic being divided into two, i.e., benign neoplastic and malignant neoplastic other than follicular one. The same study than reveal FNAC results of 387 (94.16%) nonneoplastic lesion, 15 (3.64%) of follicular neoplasm, 7 (1.70%) neoplastic, and 2 (0.48%) of unsatisfactory/inadequate smears.
In the distribution by TBSRTC categories, two new categories were added to it as compared to the conventional way of reporting cytopathology of nodular thyroid lesion, which included Category III, AUS equalled with the suggested term of FLUS along with Category V which means cytomorphology suspicious for malignancy as a part of reporting the Category IV which equalled with cytomorphology of follicular neoplasm or suspicious for follicular neoplasm which was conventionally put in broad group of neoplastic has been separately indicated. This categorization as reviewed by various studies has commented positively on addition of these categories that have resulted from more discrete and confident inclusion of cytomorphology with little overlaps. This has been elaborated through our observation made in the studies of Yang et al. Jo et al. and Mehra and Verma.,,
The criticism for Category III (AUS/FLUS) is for the inclusion of atypia which may be seen in varied diagnostic entities that include nodular goiter, follicular hyperplasia, and even Hhashimoto's thyroiditis as has been observed in the present study. However, this category of TBS has also been appreciated that nuclear atypia and follicular placement of cells has been taken into consideration as in indication for a long term. This distinct advantage of categorization of cytomorphology in Category III has been quoted studies of Naz et al., Mufti and Molah, Rabaglia et al., Kiernan et al. and Harvey et al.,,,,
The Category IV which includes follicular neoplasm as a separate distinct entity which is removed from another category of TBSRTC is another category with distinct advantages as it has minimized the bias of separation of follicular adenoma and low-grade follicular carcinoma.
When these two Categories (III and IV) are compared with cytomorphology done by conventional reporting system in the present studies, 21 cases (8.24%) were recategorized as Category III and 22 cases (8.63%) were recognized as Category IV. Such as recategorization in category III and IV has also been reported in the studies of Bhat et al. (III-2%, IV-2.5%), Guo et al. (III-3%, IV-5%), Ugurluoglu et al.(III-3%, IV-3%), and Garg et al.(III-4%, IV-5%).,,,
The category V in TBS is equalled with suspicious for malignancy identified with the specific subcategory, i.e., suspicious of papillary carcinoma, suspicious of medullary carcinoma and others. The present study by nuclear and cytoarchitectural patterns taken into consideration reclassified 21 cases of suspicious for papillary carcinoma which otherwise were reported as nodular colloid goiter with nuclear or architectural atypia. The similar observation has been reported in the studies of Al Dawish et al. (suspicious of PCT, 17), Hajmanoochehri and Rabiee (suspicious of PCT,13) and Mehra and Verma (suspicious of PCT,6).,,
The equalization of the UK-RC path with TBS if it was to be done, Thy3a and Thy3f were equalized to Category III and Category IV, respectively. The present study has two cases which were by TBS were classified in Category III, and when their cytomorphology was revisited in the UK-RC Path reporting system, they were recategorize to Thy3f of the UK-RC Path system. The parallax of categorization was observed only in two cases and all other cases could be categorized in equivalent categories of TBSRTC within the UK-RC Path system. These two cases are unavailable for follow-up. The similar observation of recategorization when two systems of TBS or UK-RC Path were utilized in the studies of Lobo et al. and Gupta et al. The studies observed no significant difference between the categories of two systems when it came to distribution of cytodiagnosis and cytomorphology.,
The histopathological diagnosis did match to categories both of TBSRTC and UK-RC Path reporting system but has revealed two false negative cases and no false positive cases. however, in contrast to conventional cytology reporting, the present study has observed 10 false-negative cases, which when recategorize to TBS had a distribution of 1 case in category III, 1 case in Category IV, and 8 cases in Category V and when recategorize to the UK-RC Path had a distribution of 1 case in Thy3a, 1 case in Thy3f, and 8 cases in Thy4, highlighting the superiority of TBSRTC and UK-RC Path at reduction in false negative reporting. In consideration to the above observation of the present study, the comparative statement of TBS and conventional system with that of the present study is tabulated in [Table 7].
|Table 7: Comparison of sensitivity, specificity, positive predictive value, negative predictive value of the present study with other studies|
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The studies as specified in [Table 7], had found that TBS reporting reduces the false-negative rate thereby increases the NPV so also the other statistical values which are similar to observations of the present study. The sensitivity and specificity as mentioned for TBS in the studies of Kasliwal et al. and Arul and Masilamani, which is closer to the sensitivity and specificity observed., Except the study Mehra and Verma et al. and Naz et al. who have TBS sensitivity <80% which is dissimilar finding with that of the present study.,
The study of Lobo et al. brought out combined sensitivity, specificity, NPV, and PPV by that of the UK-RC Path and TBS of reporting equalizing the category of both systems of reporting and has found no difference at their values with the present study.
The impact of reporting TBS and UK-RC Path in the present study was judged through the decision of thyroid surgery. The lowest rate of surgery was reported in the present study in category I/Thy1 group followed by 15.13% of cases Category II/Thy 2 but Category III/Thy3a constituted the highest no. of cases 57.4%/63.4% who underwent surgery, which generically mean category of atypia of undetermined significance/follicular lesion of undetermined significance. This sufficiently explains that in these cases atypical morphology elaborated in the reports were considered by the surgeon as a lesion that may harbor probable malignant process implicating surgical removal of such nodular thyroid swelling. To the surgical rate for the categories as observed in the present studies is similar to the surgical rate quoted by studies of Harvey et al., Mondal et al., Rabaglia et al., Kiernan et al. and Lobo et al. for category of TBS/UK-RC Path.,,,,
However, the study of Mehra and Verma et al. has contrary observation to the present study which were maximized to category IV/Thy 3f (80%), category V/Thy 4 (75%), category VI/Thy 5 (80%). This may be due to sensitization of surgeons to practice system of TBSRTC and UK-RC Path system of reporting thyroid lesion and consolidated follow-up programs.
The present study had malignancy rate in category VI/Thy5, category V/Thy 4, and category III/Thy3a. The observation similar and dissimilar to the present study has been tabulated in below [Table 8].
|Table 8: Observation of malignancy rate of the present study and other studies|
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In most of the studies present for reviewed work, the malignancy rate was crowded in category V/Thy 4 and VI/Thy 5 which is similar to the present study. The malignancy rate for each category by TBSRTC/UK-RC path was within the range of implied malignancy rate as specified by TBS. Similar malignancy rate with their implied risk for the categories IV, V, and VI were also observed in the study of Mufti and Molah and Naz et al.,
| Conclusion|| |
TBS of reporting thyroid cytology provides excellent classifiable categories which increases the sensitivity at reporting thyroid cytopathology. TBS and UK-RC Path cytology reporting system runs parallel for its classes, and therefore, the UK-RC Path is equally suitable at the categorization of cytomorphology of nodular thyroid lesion. TBS/UK-RC Path have been concluded to be advantageous over conventional reporting system as former reduces the false-negative rate and gives the clear-cut guidelines for surgical management of follow-up of the patient. TBS as well as UK/RC Path are concluded to be the most suitable reporting system for cytopathology of nodular thyroid lesion over the conventional cytopathology reporting. Therefore, TBS/UK-RC Path is advised to practice at routine reporting of FNAC of nodular thyroid lesion.
TBSRTC/UK/RC Path may be unified as these are all classes and implied interpretation is similar to bring about the uniformity of terminologies and imbibed implication at management of nodular thyroid lesion and to eliminate discrepancies of intercontinental reporting of cytopathology of nodular thyroid lesion. The sensitization of treating surgeons over the TBSRTC should be brought out to intense the understanding of treatment implication within the category of TBSRTC.
(1) TBS in category III/Thy3a becomes a limitation which requires further analysis so that it can be made more useful for practicing pathologist. However, the present study also felt the need for further analysis to Category III of TBS. (2) The response of surgeon to the specific categories as specified in TBSRTC at follow-up was not adequate as a sizable patient were unavailable for follow-up.
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Conflicts of interest
There are no conflicts of interest.
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[Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6], [Table 7], [Table 8]