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Table of Contents
ORIGINAL ARTICLE
Year : 2022  |  Volume : 10  |  Issue : 2  |  Page : 118-123

Fine-needle aspiration cytopathology correlation study of thyroid nodule with the postoperative histopathological reporting in a rural medical setup


1 Department of Pathology, Al-Azhar Super Specialty Hospital and Medical College, Thodupuzha, Kerala, India
2 Consultant Pathologist, Medilab Diagnostics, Chikmagalur, Karnataka, India
3 Department of Biochemistry, Mount Zion Medical College, Adoor, India
4 Department of Biochemistry, Muthoot Health Care Ltd, Kozhencherry, Pathanamthitta, Kerala, India

Date of Submission15-Jul-2021
Date of Decision22-Jul-2021
Date of Acceptance11-Aug-2021
Date of Web Publication02-Mar-2022

Correspondence Address:
Dr. Rufus K Sam Vargis
Department of Pathology, Al-Azhar Super Specialty Hospital and Medical College, Thodupuzha, Kerala
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/ajim.ajim_73_21

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  Abstract 


Background: Fine-needle aspiration cytology (FNAC) is the examination of cells that are obtained through a fine needle under vacuum. Due to the superior diagnostic reliability and cost-effectiveness of FNAC, American thyroid association had setup some guidelines stating that FNAC must be used as a diagnostic test initially before the ultrasonography and thyroid scintigraphy. This present study was undertaken to categorize and correlate all the thyroid FNAC samples according to the Bethesda system and for assessing the efficacy of the Bethesda reporting system in the preoperative evaluation of thyroid lesions. The major aim of study is to identify the nodules which require surgery and those benign nodules that can be observed clinically, thereby reducing the overall rate of thyroidectomy among patients with benign disorders. Materials and Methods: The present prospective study was conducted among 428 patients with thyroid lesions at a tertiary care rural medical set up. All the specimens were fixed in 10% formalin, and detailed gross examination was done. 3–10 tissue bits were selected from representative areas and all the bits were processed and stained with H and E stain. Cytological diagnoses were correlated with histopathology and the efficacy of The Bethesda System for Reporting Thyroid Cytopathology for reporting FNAC was estimated. Discussion: Out of 428 patients with thyroid lesions, 96 cases of histopathological specimens were collected. The histopathology lesions were divided into benign nonneoplastic, benign neoplastic, and malignant to study the gender, age group affected with these lesions and to calculate the association of malignancy with gender and age. The result showed that diagnostic tests are not significantly different with respect to sensitivity. Hence, FNAC is a reliable test for histopathology in diagnosis of thyroid lesions. In the present study, although the malignancy rate was higher among males, no association of gender and malignancy was not significant (P > 0.05). Conclusion: The Bethesda standardized system for reporting cytopathology improved the communication between pathologists and clinician promoting an interlaboratory agreement.

Keywords: Cytopathology and Bethesda system, fine needle aspiration cytology, histopathology


How to cite this article:
Vargis RK, Peechatt TJ, Raghuveer C R, Sharada M S, Chacko AM, Vijayan A. Fine-needle aspiration cytopathology correlation study of thyroid nodule with the postoperative histopathological reporting in a rural medical setup. APIK J Int Med 2022;10:118-23

How to cite this URL:
Vargis RK, Peechatt TJ, Raghuveer C R, Sharada M S, Chacko AM, Vijayan A. Fine-needle aspiration cytopathology correlation study of thyroid nodule with the postoperative histopathological reporting in a rural medical setup. APIK J Int Med [serial online] 2022 [cited 2022 May 26];10:118-23. Available from: https://www.ajim.in/text.asp?2022/10/2/118/338904




  Introduction Top


The nodules of thyroid are the usual clinical findings, having a reported prevalence of around 4%-7% of the adult population with a 3–4 times higher prevalence in females.[1] Thyroid nodules are clinically palpable when their size reaches more than 1 cm and those nodules which are clinically impalpable could be detected on ultrasonography or during the surgery.[2] Most of the nodules are nonneoplastic, out of which only 5%–30% are malignant. Fine-needle aspiration cytology (FNAC), which is the examination of cells that are obtained through a fine-needle under vacuum.[3] FNAC is a safer, simpler, faster, cost-effective, and minimally invasive procedure, which is a worthy asset in the preoperative screening to readily diagnose and distinguish thyroid nodules as neoplastic and nonneoplastic lesions. The thyroid gland is enclosed by dense connective tissue capsule, from which fine collagenous septae extend into the gland, dividing it into lobules. Each lobule consists of several follicles. Each follicle measures an average diameter of 200 μ with considerable variation in size. They are lined by single layer of low cuboidal epithelial cells; shape of the follicular cells varies considerably depending on the activity from flattened to cuboidal cells. The cytoplasm has a pale acidophilic or amphophilic staining quality. Nuclei are of uniform morphology. The acini are filled with chromophilic colloid that contains iodinated and noniodinated proteins. The septa convey a rich blood supply together with lymphatics and nerves. As the follicle is sensitive to large number of influences, hypertrophic and hyperplastic changes can occur and the quantity and staining character of the colloid changes correspondingly. Sparsely interspersed among the follicular cells and within the interfollicular spaces are the parafollicular or “C” cells. It is almost impossible to identify these cells under light microscopy, without the use of special stains. Through the practice of FNAC, the proportion of resected malignant nodules exceeds 50%, improving the precision and outcome of the treatment.[4],[5] Due to the superior diagnostic reliability and cost-effectiveness of FNAC, National Comprehensive Cancer Network and American Thyroid association had set up some of the practical guidelines stating that FNAC must be used as a diagnostic test initially before the ultrasonography and thyroid scintigraphy.[6] To conquer the issue of lack of a standardized system of reporting of thyroid nodules, “National Cancer Institute, Bethesda,” Maryland in the year 2007, formulated guidelines and recommendations through publishing Bethesda thyroid monograph for the diagnosis and management of thyroid disease.[7] By the numerous efforts from more than forty eminent international experts and panelists from various disciplines, The Bethesda System for Reporting Thyroid Cytopathology (TBSRTC) was constituted and made functional from January 2010.[8] Bethesda format consists of definitions, morphologic, and diagnostic criteria, malignancy risk and a plan for management of each diagnostic category briefly. Six discrete diagnostic categories (DC I–VI) were created and correlated with a positive-predictive value for diagnosing the malignancy, allowing for a clinical interpretation and subsequent management algorithm for each of these categories[9] [Table 1]. FNAC too has some drawbacks in some aspects such as the accuracy can be lower in the follicular neoplasms and suspicious cytology. The development of the thyroid gland is controlled by the coordinated action of specific transcription factors such as TTF-1, TTF-2, PAX8, and HHEX, and their altered expression likely plays an important role in thyroid dysgenesis. The major aim of a thyroid FNAC is to identify the nodules which require surgery and those benign nodules that can be observed clinically, thereby reducing the overall rate of thyroidectomy among patients with benign disorders. The primary objective is to triage patients, i.e., to determine the need of surgical intervention and to assist in deciding the appropriate surgical procedure when necessary. The Bethesda System for Reporting Thyroid Cytopathology provides standardized reporting and cytomorphological criteria in aspiration smears. It avoids confusion among surgeons in understanding the pathology report, by providing simple categories and also helps in guiding the management plan the thyroid FNAC in the present study were categorized according to TBSRTC system and malignancy risk was calculated and compared with other studies. This present study was undertaken to categorize and correlate all the thyroid FNAC samples according to the Bethesda system and for assessing the efficacy of the Bethesda reporting system in the preoperative evaluation of thyroid lesions.
Table 1: The bethesda system for reporting thyroid cytopathology; recommended diagnostic categories

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  Materials and Methods Top


This is a prospective study conducted among 428 patients with thyroid lesions at a tertiary care rural medical setting during the period of 2 years, i.e. July 2017–2019. All the patients with thyroid lesions, irrespective of age and sex, referred for FNAC were included in the study. The histopathology lesions were divided into benign nonneoplastic, benign neoplastic and malignant to study the gender, age group affected with these lesions and to calculate the association of malignancy with gender and age. Patients with skin infection at the site of aspiration, with hemorrhagic diathesis, critically ill or anxious patients, and non-cooperative patients were excluded from the study. If cystic fluid was obtained, needle aspiration was continued till the cyst got completely evacuated. The residual lesion was re-aspirated for the cellular tissue left behind.

Investigation and method of collection

Detailed clinical history was obtained, and probable clinical diagnosis was noted among all the patients with thyroid lesions who are included in the study. Details of biochemical analysis and ultrasound examination in the available cases were noted. Details of the procedure and its complications were explained to the patient after obtaining the verbal consent.

Procedure of fine needle aspiration technique

After examination of the thyroid with the patient in upright position, the patient was made to lie comfortably in supine with a pillow behind the neck for hyperextension, making the lesion more prominent. After instructing the patient to refrain from swallowing, under aseptic precautions, the lesion was needled with a fine needle (23 gauge) quickly and gently at different angles and at point of entry. Needling was concluded once the material got collected in the needle hub. Then, the needle hub was attached to an air-filled syringe, and the plunger was pushed down to expel the material onto a clean, labeled glass slide. The same procedure was repeated at different sites depending on the size of the swelling. The same technique was used for USG-guided FNAs, after identification of the thyroid nodule sonologically.

Six clusters of epithelial cells in at least two slides prepared from two needle passes were taken as adequate. All the cases were categorized according to The Bethesda system for reporting thyroid cytology (TBSRTCJ). Out of 428 cases, 96 patients underwent thyroidectomy surgery, and specimens were sent to histopathology. Histopathological examination of these specimens was done. All the specimens were fixed in 10% formalin. Detailed gross examination was done, and 3–10 tissue bits were selected from representative areas, and all the bits were processed and stained with H and E stain. Cytological diagnoses were correlated with histopathology and the efficacy of TBSRTC for reporting FNAC was estimated. The malignancy risk for each category was calculated. The false-negative and false-positive cases were analyzed.

Equipment required for fine-needle cytology of thyroid lesions is 5 ml disposable plastic syringe, 23G disposable sterile needle, Spirit to clean the skin, Glass microscopic slides for smear preparation, 95% ethanol as fixative for smears, Sterile cotton swab and gauge pads, sterile containers with tight cap to collect fluid obtained from cystic lesions and Coplin's jar. Multiple smears were made in each case, fixed in 95% ethyl alcohol, and stained by H and E method and Papanicolaou method, other were air dried and stained with May-Grunwald-Giemsa stain.

Statistical analysis

All statistical calculations were performed using IBM SPSS Statistics International Business Machines Corporation (IBM) Statistical Package for the Social Sciences (SPSS) for Windows, Version 22, SPSS Inc. an IBM Company program and Microsoft Excel 2010 (Microsoft Corporation, Seattle, WA, United States). The descriptive analysis of the epidemiological data presented as frequencies, percentages, and mean ± standard deviation (SD). Chi-square test was performed to examine the relationship between different variables.


  Results Top


The present study deals with the FNAC of thyroid lesion and determination of efficiency of The Bethesda system for reporting thyroid cytology (TBSRTC) with histopathological correlation. The present study was carried out over a period of 2 years, at cytology section, in Department of Pathology at Al Azhar Super specialty hospital and medical college, Thodupuzha, Idukki District, Kerala, over a period of 2 years, i.e. from August 2015 to August 2017. It was a prospective analysis of 380 cases with thyroid lesions. Of these, 85 cases underwent surgery subsequently, and histopathological examination of the excised specimens was done. FNACs reported were categorized according to TBSRTC. The FNAC diagnoses were compared with histopathology reports of the operative specimens, and malignancy risk for each category of TBSRTC was estimated. The important observations of the study have been represented in tabular and graphical forms. It was a prospective analysis of 428 patients with thyroid lesions, of which 96 cases underwent surgery subsequently, and histopathological examination of the excised specimens was done. Age of the patients presenting with thyroid swelling ranged from 8 to 89 years with a mean age of 37.5 years (SD = 13.9). Youngest case in our study was 8 years old with Hashimoto's thyroiditis and the oldest being 89 years with Papillary thyroid carcinoma (PTC). Peak age incidence was at 31–40 years with females comprising 128 cases (29.9%) and males comprising 11 cases (2.6%). Least common age group involved was 0–10 years accounting for 6 cases (1.4%) [Table 2]. Majority of the patients were females comprising 391 cases 91.4% and males were 37 cases 8.6% leaving a female: Male ratio = 10.5:1. Out of 428 cases, the maximum number of patients, 169 (39.5%) presented with <6-month duration of thyroid swelling. A minimum number of patients 12 (2.8%) of them noticed the thyroid swelling incidentally or after coming to hospital.
Table 2: Distribution of the 380 thyroid cases based on age and gender

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On clinical examination, maximum thyroid swellings were diffuse (168 cases) followed by solitary nodules (156 cases) and all moves with deglutition. Size of the swelling in the largest dimension was 5 cm in maximum cases (54%) and the largest was 8 cm × 6.5 cm and was diagnosed as anaplastic carcinoma thyroid. On FNA, 62% of thyroid lesions yielded hemorrhagic aspirate. FNACs were categorized into six categories of Bethesda. Maximum cases, i.e., 288 cases were of Benign category (DC-II) followed by nondiagnostic (ND) category (DC-I), i.e. 40 cases. Repeat aspiration with USG guidance (8 cases) yielded better aspiration. The most common lesion on FNAC in the present study was Colloid nodular goiter (132 cases). Among malignant categories, the most common lesion was PCT. The Atypia of Undetermined Significance (AUS) category was judiciously used and had only 8 cases.

Out of 428 cases of FNAC, 96 cases underwent thyroidectomy, of them maximum cases resected were of benign category (DC-II). In histopathology, the most common benign lesion was multinodular goiter (27 cases) and malignant lesion was PCT (29 cases). Out of these 29 cases of PCT, 11 cases were of FVPCT. The malignancy risk was obtained by correlating cytological diagnosis with histopathological diagnosis. The malignancy for each category was as follows: DC-I (25%), DC-II (8.16%), DC-III (50%), DC-IV (45.45%), DC-V (66.66%), and DC-VI (90.9%). The malignancy risk among categories I, II, III, and IV was higher compared to malignancy risk according to TBSRTC and in comparison to other studies.

The histopathology lesions were divided into benign nonneoplastic, benign neoplastic, and malignant to study the gender, age group affected with these lesions and to calculate the association of malignancy with gender and age. Ten males underwent thyroidectomy, of which six cases turned out to be malignant and 86 females underwent thyroidectomy, of which 27 cases were malignant. Although the malignancy rate among males (60%) was higher compared to females (31.3%), the association of malignancy and gender was insignificant (P > 0.05). The diagnostic test FNAC and histopathology were compared using McNemar's Chi-square test. McNemar's χ2 = 0.076, P = 0.78, df = 1. The result showed that diagnostic tests are not significantly different with respect to sensitivity. Hence, FNAC is a reliable test for histopathology in diagnosis of thyroid lesions.


  Discussion Top


Thyroid nodules are common clinical findings and have a reported prevalence of 4%–7% of adult population. They are 3–4 times more frequent in females than males. The vast majority of them are non-neoplastic and only 5% to 30% are malignant. Thyroid cytology can provide a definite diagnosis of malignancy, often specifying the tumor type, enabling appropriate therapeutic procedure in one stage. The primary objective is to triage patients that is to determine need of surgical intervention and to assist in deciding the appropriate surgical procedure when necessary. With current thyroid FNA practice, the percentage of resected nodules that are malignant surpasses 50%6 (before usage of FNA, it was 14%). TBSRTC (The Bethesda System for Reporting Thyroid Cytology) describes six diagnostic categories of thyroid lesion that have individual implied risks of malignancy that influence management paradigms. The present study is undertaken to evaluate the efficacy of the Bethesda System for reporting thyroid cytology with histopathological correlation of the cases undergoing surgical resection.

In the present study, FNAC of the comparison of age and gender distribution of the 428 patients with thyroid nodules were discussed in [Table 3] and [Table 4]. The diagnostic tests FNAC and histopathology were compared using McNemar's Chi-square test, and results showed that the diagnostic tests were not significantly different with respect to sensitivity implying FNAC is a good diagnostic tool for preoperative diagnosis of thyroid lesions. The sensitivity, specificity, positive predictive value, negative predictive value, and diagnostic accuracy in the present study were calculated considering benign category as negative and category AUS. The ND category was excluded. The major reason for the wide range of sensitivity and specificity ratios is the differences in the categorization of “FN/SFN,” “suspicious for malignancy,” and “AUS/follicular lesion of undetermined significance (FLUS)” diagnoses. In addition, some authors categorize follicular lesions as histopathologically benign, while others categorize these lesions as malignant. The false-negative rate (20.5%) obtained in the present study was higher than recommended by Bethesda (7%). Practical assessment of the false-negative rate can be achieved only from long-term (e.g., 5–10 years) clinical follow-up of cytological benign nodules. There are only a few studies of patients with benign results that were followed long term and they have reported a false-negative rate of <1%. Ideally, institutions should strive to achieve a false-negative rate that is <2%–3%. This high rate resulted as more benign lesions were resected in the present study. The reasons for false-negative cases were wrong sampling, cytomorphological overlap of benign and malignant features, and interobserver variability. The false-positive rate (12.5%) obtained in the present study was higher compared to other studies. Reasons for false-positive cases being poorly fixed smears, hemorrhage causing diagnostic difficulties and degenerative features mimicking malignancy. In 2008, Melanie. L. Richards et al. studies show ND thyroid fine-needle aspiration biopsies are no longer a dilemma. ND-FNAs occurred in 51 (21%) of 241 patients. In 2017, Ozdemir et al. 58 compared thyroid FNAB results before and after implementation of Bethesda classification and found that, among operated nodules, percentages of benign, and suspicious for malignancy cytologies decreased and percentages of ND and uncertain cytologies increased with the implementation of Bethesda. Ultrasound guidance did not reduce the likelihood of a ND biopsy. Patients with nodules >3 cm had more ND-FNAs. Twenty-one of 51 with a ND biopsy underwent a repeat FNAB. Repeat FNAB was ND in 29% of patients. There was a malignant disease in 7 of 51 (14%) with a ND-FNAB. The range of age distribution in the present study was 8–89 years and average age was 37.5 years (SD = 13.9). This range was close to Ranjan et al.[13] and Renuka et al.[12] The mean age of the present study was close to Ranjan et al.[12] In the present study, the aspirate most commonly obtained from thyroid sampling was hemorrhagic (62%), followed by blood mixed colloid (22%), as thyroid is a highly vascular organ. Panchal et al.[16] found maximum aspirates to be hemorrhagic (51.33%) similar to the present study. Jayaram et al.,[17] suggested that the average number of needle passes recommended for adequate sampling of thyroid nodules is two to five. As the thyroid gland is a highly vascular organ, with each impending trauma, the chances of aspirating hemorrhagic fluid rises each time, so they advised to keep the number of aspirates to minimum. Mandal et al.[18] performed repeat aspiration in 5.5% of cases (n = 6) wherever the first thyroid aspirate was inadequate in their study of 120 cases. The comparison of distribution of Bethesda diagnostic categories of the present study with published studies was explained in [Table 5]. The malignancy risk of categories I to IV in the present study was higher than the range of malignancy risk according to TBSRTC. The risk of malignancy for the benign category was 8.16%. This was higher than the range of malignancy risk according to TBSRTC and in comparison to other studies. This higher value in the present study can be attributed to the fact that to a greater number of cases resected in the category compared to the other categories; this led to the detection of more false-negative cases.
Table 3: Age distribution in various studies compared to present study

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Table 4: Gender distribution in various studies compared to the present study

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Table 5: Comparison of distribution of bethesda diagnostic categories of the present study with published studies

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The risk of malignancy for category AUS was 50%. Similar value was obtained by Shagufta Mufti and Molah[20] but was very high compared to the range of TBSRTC and other studies. False-positive rates are the cases interpreted as malignant on FNAC which were proved benign on histopathology. The FPR in present study was 12.5%. This was slightly higher compared to other studies. Muratli et al.[22] had FPR of 15.5%, higher than the present study. Reasons for false-positive diagnosis in the present study could be poorly fixed smears, hemorrhage causing diagnostic difficulties, degenerative features mimicking malignancy. Chi-square test was applied to know the association of malignancy with gender and specific age group. In the present study, although the malignancy rate was higher among males, no association of gender and malignancy was not significant (P > 0.05). The age groups with benign neoplastic and malignant lesions were compared and association of age group and malignancy was not statistically significant (P = 0.98). Similar findings were obtained by Muratli et al.[22]


  Conclusion Top


FNAC is a simple, minimally invasive first-line diagnostic procedure for the evaluation of thyroid lesions. It is a highly sensitive and specific diagnostic test for preoperative detection of thyroid lesions. This study was done to validate the efficiency of the Bethesda system for reporting thyroid cytology, which found the higher malignancy risks obtained among category I, II, and III patients. This warrants a better follow-up for these categories. The Bethesda standardized system for reporting cytopathology improved the communication between pathologists and clinician promoting an interlaboratory agreement. Adoption of the Bethesda system allows a more standard and uniform method of reporting thyroid cytology providing clear and consistent management guidelines for the clinicians.

Future recommendations

The AUS category was judiciously used in the present study, and high malignancy rate was obtained in it, which needs to be better understood and warrant a further work up with ultrasound scan and repeat aspiration on follow-up.

Limitations of the study

The data regarding both biochemical analysis and ultrasound scan were not available for all the patients subjected to FNAC. Even, the follow up of the patients was minimal, with only a few cases have been followed up.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
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