ORIGINAL ARTICLE


https://doi.org/10.5005/jp-journals-10002-1435
World Journal of Endocrine Surgery
Volume 14 | Issue 2 | Year 2022

Assessment of Ultrasound Features in Thyroid Nodules of Northeast Indian Population and its Correlation with Histopathology


Suvamoy Chakraborty1https://orcid.org/0000-0002-4988-7568, Manu Coimbatore Balakrishnan2https://orcid.org/0000-0002-4745-2210, Pranjal Phukan3, Vandana Raphael4https://orcid.org/0000-0002-1422-2240, Ratan Medhi5, Barishisha Kharkongor6

1,2,5,6Department of Otorhinolaryngology (ENT), North Eastern Indira Gandhi Regional Institute of Health & Medical Sciences (NEIGRIHMS), Shillong, Meghalaya, India

3Department of Radiology, North Eastern Indira Gandhi Regional Institute of Health & Medical Sciences (NEIGRIHMS), Shillong, Meghalaya, India

4Department of Pathology, North Eastern Indira Gandhi Regional Institute of Health & Medical Sciences (NEIGRIHMS), Shillong, Meghalaya, India

Corresponding Author: Manu Coimbatore Balakrishnan, Department of Otorhinolaryngology (ENT), North Eastern Indira Gandhi Regional Institute of Health & Medical Sciences (NEIGRIHMS), Shillong, Meghalaya, India, Phone: +91 9786032010, e-mail: cbalakrishnanmanu@gmail.com

Received on: 29 October 2022; Accepted on: 10 February 2023; Published on: 15 April 2023

ABSTRACT

A thyroid nodule can be radiologically detected in up to 60% of the population. No single ultrasound feature is sensitive or specific for malignancy.

Aims: To assess the ultrasound features in thyroid nodules of the Northeast Indian population in a tertiary care hospital.

Objective: To correlate ultrasonography (USG) with the histopathological examination (HPE) findings after surgery using the American College of Radiology Thyroid Imaging Reporting and Data System (ACR TI-RADS).

Materials and methods: This retrospective cohort study involved the records of 40 patients with thyroid nodules who had visited the Department of ENT in the year 2019–2020. Case records were retrieved and out of which only 28 patients had both USG findings and HPE reports.

Results: Ultrasonography (USG) findings of 28 patients were analyzed and correlated with HPE reports. ACR TI-RADS had sensitivity, specificity, positive predictive value (PPV), and negative predictive value (NPV) of 70, 87, 82, and 77%, respectively, in diagnosing thyroid malignancy. The risk of malignancy (ROM) for ACR TI-RADS, 1, 2, 3, 4, and 5 groups in our study was 0, 0, 25, 71, and 100%, respectively.

Conclusion: A specificity of 87% and PPV of 82% of ACR TI-RADS USG is good for diagnosing thyroid malignancy and planning further management in our population. We recommend the routine use of ACR TI-RADS USG classification systems.

Clinical significance: Routine use of any widely accepted USG classification system should be employed. We recommend institutional studies of large sample sizes or audits to study the ROM for each target population to plan for population-specific treatment protocols.

How to cite this article: Chakraborty S, Balakrishnan MC, Phukan P, et al. Assessment of Ultrasound Features in Thyroid Nodules of Northeast Indian Population and its Correlation with Histopathology. World J Endoc Surg 2022;14(2):46-50.

Source of support: Nil

Conflict of interest: None

Keywords: Diagnostic imaging, Diagnostic value, Retrospective study, Thyroid malignancy, Thyroid nodule, Ultrasonography.

INTRODUCTION

A nodule in a thyroid gland that is clinically palpable can be seen in 4% of the population. However, on imaging, it can be detected in up to 60% of the population.1 Assessment of the thyroid gland involves clinical examination, imaging, biochemical, and cytological tests. The idea of all these tests is to detect malignancy at the earliest and to offer conservative management to those patients who have benign conditions. Ultrasound imaging is the primary imaging modality utilized in the evaluation of thyroid nodules. It is a noninvasive technique and is used to characterize the thyroid nodule. It is used as a screening tool and to aid in guiding fine-needle aspiration cytology (FNAC) and for follow-up of patients.1 It has been found that no single feature is sensitive or specific to identify thyroid malignancy; however, when multiple features are combined, it provides an idea if the lesion is malignant or not.1,2 Several guidelines have been formulated for studying thyroid USG features. As of now, it has been suggested that there are not enough studies to decide on the best system for routine application in clinical practice.3,4 ACR TI-RADS score was modified in 2017 and not many studies have evaluated its efficacy in identifying malignancy in regional populations.5 Few studies which are present usually compare the USG findings with FNAC results.6,7 This study assessed the ultrasound features of thyroid nodules using the TI-RADS scoring system and compared them with HPE in the Northeast Indian population in a tertiary care hospital. We believe this study can add to the population-based findings of the routine use of ACR TI-RADS in clinical practice.

AIMS AND OBJECTIVES

Aim

To assess the ultrasound features in thyroid nodules of the Northeast Indian population in a tertiary care hospital.

Objective

To correlate USG with the HPE findings after surgery using TI-RADS.

MATERIALS AND METHODS

After obtaining Institutional Ethics Committee approval, this retrospective cohort study was conducted in the Department of Otorhinolaryngology. It involved the case records of patients belonging to both genders and all age groups who visited the Department of ENT with thyroid nodules in the year 2019–2020. The details of the patients, like age, gender, USG findings, type of surgery done, and HPE report, were collected. Case records of patients without USG or HPE reports were excluded. In our center, the USG was performed using a Samsung RS80EVO machine with a high-frequency linear probe of 7–12 MHz and the USG was done by a single radiologist. In our study, the ultrasound features which were studied were the composition of the nodule, echogenicity, size of the lesion, calcifications, shape of the lesion, vascularity, margins of the lesions, and presence of any abnormal lymph nodes. ACR TI-RADS score was used to classify thyroid nodules based on USG findings.5

The HPE report was considered the gold standard for diagnosing thyroid malignancy. The data was collected in Microsoft Excel 2017 and data analysis was done using IBM PASW statistics v19.0 (Statistical Package for the Social Sciences version 19.0). The USG findings and HPE reports were correlated and the sensitivity, specificity, PPV, and NPV of USG in detecting thyroid malignancy were calculated with a 95% confidence interval. All the statistical tests were considered statistically significant at a p-value of ≤0.05. The ROM in each ACR TI-RADS category was calculated by the formula:

RESULTS

In 2019–2020, 40 patients with thyroid nodules visited the Department of ENT. Case records were retrieved and out of which only 28 patients had USG findings and HPE reports. The USG findings of only 28 patients were analyzed. The minimum age of the patient was 15 years and maximum age was 70 years and the mean ± standard deviation = 40 ± 14 years. Female patients constituted 79% of the sample size, with the rest being male patients. Table 1 depicts the various sonographic features studied. Clinically solitary thyroid nodule was diagnosed in 22 patients (79%) and multinodular goiter (MNG) was diagnosed in six patients (21%). Figure 1 demonstrates USG findings of a patient with thyroid swelling. ACR TI-RADS scoring was analyzed for all the USG reports and TI-RADS 4 constituted the major part amounting to 14 (50%) patients. Other categories seen were TI-RADS 3 in eight (29%), TIRADS 5 in three (11%), TI-RADS 2 in one (3%), and TI-RADS 1 in two (7%) patients. Table 1 depicts the various sonographic features studied and their analysis (Fig. 1 and Table 1).

Table 1: Various sonographic features in the sample studied with analysis
Sonographic features (N = 28) n HPE benign n = 12 (48%) HPE malignant n = 13 (52%) Test p-value
Nodule size
 <2 cm 10 5 (50%) 5 (50%) Fisher’s exact 0.786
 2–4 cm 9 5 (56%) 4 (44%)
 >4 cm 9 3 (33%) 6 (67%)
Composition
 Cystic 2 2 (100%) 0 Fisher’s exact 0.113
 Solid cystic 10 6 (60%) 4 (40%)
 Solid 16 5 (31%) 11 (69%)
Echogenicity
 Anechoic 2 2 (100%) 0 Fisher’s exact 0.023a
 Hypoechoic 19 6 (32%) 13 (68%)
 Isoechoic 3 1 (33%) 2 (67%)
 Hyperechoic 4 4 (100%) 0
Calcification
 No calcification 18 10 (56%) 8 (44%) Fisher’s exact 0.045a
 Microcalcification 7 0 7 (100%)
 Macrocalcification 3 2 (67%) 1 (33 %)
Shape
 Taller than wide 0 13 (46%) 15 (54%) Fisher’s exact 0.464
 Wider than tall 28
Vascularity
 No vascularity 3 3 (100%) 0 Fisher’s exact 0.076
 Normal vascularity 13 6 (46%) 7 (54%)
 Increased vascularity 12 4 (33%) 8 (67%)
Margin
 Smooth 24 13 (54%) 11 (46%) Fisher’s exact 0.480
 Irregular 3 0 3 (100%)
 ETE 1 0 1 (100%)
Abnormal LN
 Yes 2 0 2 (100%) Fisher’s exact 0.480
 No 26 13 (50%) 13 (50%)
TI-RADS 1 2 2 (100%) 0 Fisher’s exact 0.018a
TI-RADS 2 1 1 (100%) 0
TI-RADS 3 8 6 (75%) 2 (25%)
TI-RADS 4 14 4 (29%) 10 (71%)
TI-RADS 5 3 0 3 (100%)
 USG benign 11 9 (82%) 2 (18%) Chi-squared 0.006a
USG malignant 17 4 (23%) 13 (77%)

asignificant p-value; HPE, histopathological examination; ETE, Extra-thyroidal extension; LN, Lymph node

Figs 1A to D: (A) Axial (B) sagittal: shows a hypo-isoechoic solid lesion 3.09 x 2.17 x 3.52 cm in the right lobe of the thyroid with irregular margins. Antero-posterior dimensions of the lesion measure lesser than the transverse diameter. Multiple echogenic foci are seen predominantly in the periphery of the lesion. No extrathyroidal extension; TI-RADS-5; (C) Color Doppler evaluation shows areas of minimal color uptake within the lesion; (D) Shows the right lobe of the thyroid with normal measurements

In USG, the diagnosis of benign nodules was made in 11 patients (39%) and malignant nodules in 17 patients (61%). Hemithyroidectomy was performed in 14 patients (50%), total thyroidectomy (TT) in 10 patients (36%), and TT with neck dissection was performed in four patients (14%). TI-RADS 1 patient underwent surgery in view of the size of the goiter and patient preference. In the HPE of the thyroid specimens, there were 13 benign thyroid pathologies (46%) and 15 malignant pathologies (54%). In HPE, the following diagnoses were noted—colloid goiter in three patients (11%), adenomatoid goiter 1 (3%), MNG in seven patients (25%), follicular adenoma in two patients (7%), papillary carcinoma thyroid in 15 patients (54%). Two out of 11 USG benign cases turned out to be HPE malignant. Both the patients were in TI-RADS three category with MNG. Both the patients underwent TT and each had a single focus of papillary carcinoma in the background of MNG of size 1 cm and 2.5 cm, respectively. The use of USG in diagnosing malignancy of the thyroid gland using ACR TI-RADS score in our study had the following findings:

DISCUSSION

The definitive evaluation of the thyroid gland for malignancy involves cytological examination in the form of FNAC or tissue diagnosis in the form of HPE. Even though HPE is the gold standard for diagnosing thyroid malignancy, it is not possible to get HPE done for all thyroid nodules as the incidence of thyroid malignancy is only 6–7% among thyroid nodules.8 Hence the lesser invasive form of cytological examination is preferred to decide on further treatment for thyroid pathologies. However, even this FNAC has its own disadvantages and limitations. It can result in pain at local sites and around 10–20% of the FNACs can turn out to be non-diagnostic.9 USG has the advantage of being non-invasive. Incidentally detected thyroid nodules can add to the mental agony of the patient and have led to an increased number of thyroidectomies.10 Over the past years, the utilization of USG for diagnosing thyroid malignancies has evolved drastically, with many guidelines being formulated. Modified TI-RADS by Kwak et al. in 2011, ACR TI-RADS updated in 2017, European TI-RADS, Korean TI-RADS, American Association of Clinical Endocrinologists, American College of Endocrinology, Associazione Medici Endocrinology classification, American Thyroid Association classification, and British Thyroid Association classification of USG nodules are some of the widely accepted guidelines. However, as of now, it has been suggested that there are not enough studies to decide on the best system for routine application in clinical practice.3,4

These classification systems emerged as no single USG feature can predict malignancy effectively but rather a combination of USG features. The commonly studied USG features in all the above guidelines have overlapping features. The high-risk USG features are solid nodules, hypoechogenicity, irregular margins, microcalcifications, taller than wider shapes, and the presence of abnormal lymph nodes.

In our study, female patients constituted the major part of the sample (79%). This was the usual finding seen in several other studies.11,12 In our study, the nodule size was not significantly associated with the ROM. The classical teaching was that nodule size was associated with an increased ROM; however, recent studies have shown contradictory findings, with some studies showing malignancy rate directly proportional to nodule size and some studies showing an inverse relationship with nodule size.13 Most common composition of thyroid nodules seen in our study was the solid type, especially in the malignant nodules. However, some benign adenomatous nodules also showed solid composition. This relation was not significant, probably owing to the small sample size. Hypoechogenicity and microcalcification were predominantly seen in malignant nodules. This was in concordance with other international studies. Increased vascularity, particularly central vascularity, irregular margins, and abnormal lymph nodes, are specifically seen in malignant nodules similar to our study.14 However, a significant relationship could not be established in our study, probably owing to the relatively small sample size. Our findings confirm that no single USG feature alone can be reliably used to predict malignancy.

On using ACR TI-RADS scoring, we found a significant relationship in determining malignant thyroid nodules by USG. The sensitivity, specificity, PPV, and NPV of using ACR TI-RADS in USG for determining if a nodule was benign or malignant were 70, 87, 82, and 77%, respectively. These findings were again comparable with other studies. In a study by Singaporewalla et al., the sensitivity and specificity of TI-RADS with FNAC were 70.6 and 90.4%, respectively.6

In a study conducted by Chauhan et al., it was concluded that USG is 67% sensitive and 100% specific in diagnosing malignant thyroid disease.12 The relatively low sensitivity may be attributed to the lack of any USG classification system, thus emphasizing our point.

In another study by Xue et al., the TI-RADS classification system was used with elastography and attained higher sensitivity of 88.9% and specificity of 91.8%.15

Nonetheless, USG and FNAC, when combined together in the evaluation of thyroid nodules, are more sensitive and specific than when used alone, as concluded by Gautam et al. in their study.16

The ROM for ACR TI-RADS, 1, 2, 3, 4, and 5 groups in our study was 0, 0, 25, 71, and 100%, respectively. In a study by Singaporewalla et al., the risk of malignant FNAC for TI-RADS 2, 3, 4, and 5 was 0, 9.5, 0, and 60%, respectively.6

Srinivas et al., in their study, found that the ROM for TI-RADS 1, 2, 3, 4, and 5 was 0, 0, 0.64, 36, and 100%, respectively.9 However, in both the above studies, the ROM was based on the Bethesda system of FNAC. In our study, the ROM was calculated from HPE reports. HPE analysis of the thyroid nodules increases the chances of detecting malignancy compared to FNAC. Combined, the small sample size maybe the reason for the higher ROM in our study. Hence, we recommend a large sample-sized study in the Northeast Indian population to estimate and compare the ROM with other regions of the country.

Park et al. reported the following ROM for TI-RADS 1, 2, 3, 4, and 5 as 1.8, 9.6, 31.1, 76.8, and 100%, respectively. These findings are comparable to our study.17

The limitations of the study were the relatively smaller sample size and retrospective design. A large sample-sized prospective study in our population is needed to accurately comment on the predictive values. The strengths of the study were the assessment of all USG features in a thyroid nodule and the implementation of the latest ACR TI-RADS classification for stratifying the thyroid nodules. The use of HPE instead of FNAC for correlation was also a strength of the study.

CONCLUSION

Using ACR TI-RADS in USG for detecting malignant nodule had sensitivity, specificity, PPV, and NPV of 70, 87, 82, and 77%, respectively. This makes USG an effective initial screening tool for our population. However, a large sample-sized study in our population is needed to accurately predict the sensitivity, specificity, PPV, and NPV of ACR TI-RADS in our population. The ROM for ACR TI-RADS, 1, 2, 3, 4, and 5 groups in our study was 0, 0, 25, 71, and 100%, respectively. This relatively increased ROM in our population needs further evaluation.

Clinical Significance

We would like to emphasize the fact that USG forms an important role in deciding further management of thyroid nodules. The decision for tissue diagnosis in the form of FNAC or biopsy should be made after detailed analysis of USG findings. Patients’ anxiety and unwarranted avoidable surgical interventions are to be kept in mind. To aid in this, the authors recommend the routine use of any widely accepted classification systems for USG. However, before recommending one particular system, in our case, the ACR TI-RADS, we propose that further population-based studies with a larger sample size are needed to compare the efficacy of each.

ACKNOWLEDGMENT

Dr Ningombam Joenna Devi, Senior Resident Doctor, Department of Community medicine, North-Eastern Indira Gandhi Regional Institute of Health and Medical Sciences for helping in statistical analysis.

ORCID

Suvamoy Chakraborty https://orcid.org/0000-0002-4988-7568

Manu Coimbatore Balakrishnan https://orcid.org/0000-0002-4745-2210

Vandana Raphael https://orcid.org/0000-0002-1422-2240

REFERENCES

1. Watkinson JC, Clarke RW, editors. Scott-Brown’s Otorhinolaryngology and Head and Neck Surgery: 3 volume set. CRC Press; 2018.

2. Domínguez JM, Baudrand R, Cerda J, et al. An ultrasound model to discriminate the risk of thyroid carcinoma. Acad Radiol 2011;18(2):242–245. DOI: 10.1016/j.acra.2010.09.018

3. Floridi C, Buccimazza G, Arrichiello A, et al. Ultrasound imaging classifications of thyroid nodules for malignancy risk stratification and clinical management: state of the art. Gland Surg 2019;8(Suppl 3):S233–S244. DOI: 10.21037/gs.2019.07.01

4. Durante C, Grani G, Lamartina L, et al. The diagnosis and management of thyroid nodules: a review. JAMA 2018;319(9):914–924. DOI: 10.1001/jama.2018.0898

5. Tessler FN, Middleton WD, Grant EG. Thyroid imaging reporting and data system (TI-RADS): a user’s guide. Radiology 2018;287(1):29–36. DOI: 10.1148/radiol.2017171240

6. Singaporewalla RM, Hwee J, Lang TU, et al. Clinico-pathological correlation of thyroid nodule ultrasound and cytology using the TIRADS and Bethesda classifications. World J Surg 2017;41(7):1807–1811. DOI: 10.1007/s00268-017-3919-5

7. Mohebbi M, Dehaki MG, Mozaffari M. Comparison between ultrasonographic findings and fine needle aspiration cytology in differentiating malignant and benign thyroid nodules. Eur J Transl Myol 2019;29(3):8354. DOI: 10.4081/ejtm.2019.8354

8. Pompili GG, Tresoldi S, Ravelli A, et al. Use of the ultrasound-based total malignancy score in the management of thyroid nodules. Ultrasonography 2018;37(4):315–322. DOI: 10.14366/usg.17063

9. Srinivas MN, Amogh VN, Gautam MS, et al. A prospective study to evaluate the reliability of thyroid imaging reporting and data system in differentiation between benign and malignant thyroid lesions. J Clin Imaging Sci 2016;6:5. DOI: 10.4103/2156-7514.177551

10. Nicolaou MA, Jacobs K, Bhana S, et al. A retrospective study correlating sonographic features of thyroid nodules with fine-needle aspiration cytology in a South African setting. SA J Radiol 2019;23(1):1749. DOI: 10.4102/sajr.v23i1.1749

11. Pal R, Kar S, Sengupta A, et al. Clinico-pathological correlates of incidentally revealed thyroid swelling in Bihar, India. J Pharm Bioallied Sci 2012;4(1):51–55. DOI: 10.4103/0975-7406.92730

12. Chauhan HH, Aiyer RG, Shah PC. Clinical, pathological and radiological correlation of thyroid swellings. Int J Otorhinolaryngol Head Neck Surg 2020;6(4):708. DOI: https://doi.org/10.18203/issn.2454-5929.ijohns20201287

13. Dong S, Pan J, Shen YB, et al. Factors associated with malignancy in patients with maximal thyroid nodules ≥2 cm. Cancer Manag Res 2021;13:4473–4482. DOI: 10.2147/cmar.s303715

14. Remonti LR, Kramer CK, Leitão CB, et al. Thyroid ultrasound features and risk of carcinoma: a systematic review and meta-analysis of observational studies. Thyroid 2015;25(5):538–550. DOI: 10.1089/thy.2014.0353

15. Xue J, Shi L, Wang J, et al. The diagnostic value of combination of TI-RADS and ultrasound elastography in the differentiation of benign and malignant thyroid nodules. Clin Imaging 2016;40(5):913–916. DOI: 10.1016/j.clinimag.2016.04.014

16. Gautam HK, Kumar V, Kanaujia SK, et al. Clinico-cytoradiological correlation of thyroid surgery in patients with thyroid nodule. Ann Indian Acad Otorhinolaryngol Head Neck Surg 2017;1(2):17–21. DOI: 10.4103/aiao.aiao_7_17

17. Park JY, Lee HJ, Jang HW, et al. A proposal for a thyroid imaging reporting and data system for ultrasound features of thyroid carcinoma. Thyroid Off J Am Thyroid Assoc 2009;19(11):1257–1264. DOI: 10.1089/thy.2008.0021

________________________
© The Author(s). 2022 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (https://creativecommons.org/licenses/by-nc/4.0/), which permits unrestricted use, distribution, and non-commercial reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.