Abstract
Objectives
Nodules of the thyroid gland are common but rarely malignant. Their management can range from simple monitoring to surgery. The use of ultrasound and fine needle aspiration can reduce the rate of unnecessary surgeries. However, there is a risk of false positives and false negatives of malignancy that only pathology can avoid. The objective of this study is to assess the impact of ultrasound classification on the rate of surgical indications.
Material and methods
Between 2013 and 2017, the ultrasound classification was gradually adopted in our daily practice to become now routine. During this period, we conducted a retrospective study of all the patients who presented to our department for one or more thyroid nodules.
Results
A total of 577 patients were included in the study. We compared two groups, a first where the ultrasound classification was used and a second where this classification was not used. In the end, we found that this classification significantly reduced the surgical indication by 19% while increasing the malignancy detection rate in operated patients by 21%.
Conclusions
The use of ultrasound classification reduces the indications for surgery while increasing the rate of malignancy in operated patients. The generalization of the use of the ultrasound classification score is strongly recommended in daily practice.
Keywords: Thyroid nodule, Ultrasound, TIRADS, Surgery, Pathology
Introduction
A thyroid nodule is a localized hypertrophy of the gland, identifiable on physical examination and/or ultrasound. The majority of nodules are benign but 3.9–13% are malignant regardless of their size [1–3]. The detection of a thyroid nodule raises the question of the possibility of cancer. Only the histopathological examination can confirm or rule out the malignancy, but certain clinical or paraclinical signs have significant orientation value. A wait-and-see attitude can lead to the lack of early treatment for cancer, while routine surgery leads to a large number of unnecessary operations with their risks and costs.
Ultrasound has become the gold standard for detecting, diagnosing, looking for signs of malignancy, and monitoring thyroid nodules. There is a consensus on the need to standardize ultrasound examinations. This resulted in the implementation of the Thyroid Imaging Data and Reporting System (TIRADS), initially developed by Horvath in 2009 [4] and modified several times thereafter.
The TIRADS classification was gradually adopted in our hospital from 2013, to become systematic from 2015. However, at the time, we continued to receive some ultrasounds performed outside our hospital which did not yet adopt the TIRADS classification. Throughout this work, our objective was to assess the impact of the TIRADS classification on the rate of indication for surgery by comparing two groups of patients; one using the TIRADS classification (TIRADS group) and the other without classification (No-TIRADS group).
Material and methods
We performed a retrospective study over a period of 5 years from 2013 to 2017. We included in our study all patients who presented on an outpatient basis with at least one thyroid nodule and who had at least one TSH test (Thyroid Stimulating Hormone) and an ultrasound. We excluded Graves' disease cases because the surgical indication is not related to the ultrasound data. We selected for each patient the most suspicious nodule only. We compared two groups of patients; one using the TIRADS classification (TIRADS group) and the other without classification (No-TIRADS group). We adopted the TIRADS 2013 classification according to Russ [5].
In both groups, the indication for fine needle puncture (FNA) was based on clinical and/or ultrasound criteria, and the indication for surgery was based on clinical and/or ultrasound and/or cytological criteria.
We calculated the sensitivity, specificity, positive predictive value and negative predictive value of the TIRADS score by pooling scores 2 and 3 in favor of benignity and scores 4 and 5 in favor of malignancy.
Results
We included 577 patients in our study, including 494 women (85.6%) and 83 men (14.4%). The sex ratio was 0.16. The average age was 46 years (range 15 to 82). The TIRADS classification was used in 41.6% of cases (240 patients) and not in 58.4% cases (337 patients); Table 1 shows the distribution of patients according to the TIRADS score.
Table 1.
Distribution of patients according to the TIRADS score
| TIRADS score | Number of patients | Percentage | Percentage of surgical indication | Percentage of benignity |
|---|---|---|---|---|
| 2 | 15 | 6.3 | 13 | 100 |
| 3 | 114 | 47.5 | 25 | 97 |
| 4A | 74 | 30.8 | 48.6 | 83 |
| 4B | 35 | 14.6 | 100 | 50 |
| 5 | 2 | 0.8 | 100 | 0 |
The surgical indication was retained in 62.3% of cases (210 patients) in the No-TIRADS group, and in 43.3% of cases (104 patients) in the TIRADS group. The difference was significant. Table 1 presents the percentage of surgical indication according to the TIRADS score. In total, surgery was indicated in 314 patients, of whom 10 refused surgery and 304 patients were operated. The nodules were benign in 89.7% of cases in our series: 98% in the No-TIRADS group and 76.9% in the TIRADS group. The difference was significant. Table 1 shows the percentage of benignity in this group.
Discussion
Thyroid nodules are common and most often benign. Their prevalence varies from 2 to 6% on palpation [6] and reaches 35% on imaging and 65% on post-mortem autopsy [7]. The frequency of cancer among thyroid nodules varies between 3.9 and 13% [1, 3], with a frequency of 10.3% in our study.
The TIRADS system makes it possible to assess the risk of malignancy of a thyroid nodule according to its ultrasound appearance. In 2009, the TIRADS classification was first proposed by Horvath, based on the BI-RADS concept in breast cancer. Russ extended the system in 2011[8], then improved it in 2013[5]. It is this last classification that we adopted in our study. In 2017, the European Thyroid Association adopted a new European Thyroid Imaging and Reporting Data System (EU-TIRADS) [9]. Several other classifications are adopted around the world, including that of the ATA (American Thyroid Association) [10]
Table 2 presents the risk of malignancy according to the TIRADS score in the literature and in our series [4, 9, 11]. Table 3 summarizes our results in comparison with the literature [8, 12–15]. Many studies have shown a sensitivity greater than 95%, with a negative predictive value close to 99% [8, 12–15], which is consistent with our results.
Table 2.
| TIRADS score | Risk of malignancy% | |||
|---|---|---|---|---|
| Horvath | Russ | Albair Ashamallah | Our series | |
| 2 | 0 | 0 | 0 | 0 |
| 3 | < 5 | 0.25 | 6.4 | 3 |
| 4A | 5–10 | 6 | 27.7 | 17 |
| 4B | 10–80 | 69 | 65.3 | 50 |
| 5 | > 80 | 100 | 98.2 | 100 |
Table 3.
| Series | Year | Country | Sensibility | Specificity | PPV | NPV |
|---|---|---|---|---|---|---|
| G Russ | 2011 | France | 94 | 53 | – | 99.6 |
| Zhang. | 2015 | China | 97.4 | 91 | 39.6 | 99.8 |
| Srinivas | 2016 | India | 96 | 92.6 | 49 | 99.7 |
| Yoon | 2016 | South Korea | 97.4 | 29.3 | 23.3 | 98.1 |
| Sun | 2017 | China | 98.7 | 30.7 | 47.3 | 97.3 |
| Our series | 2018 | Morocco | 97.3 | 37.7 | 47.1 | 95.23 |
In our study, the surgical indication was retained in 62.3% of cases in the No-TIRADS group and in 43.3% of those in the TIRADS group. Consequently, we have a significant decrease in surgical indications even though there may be differences in clinical, ultrasound or cytological situation in the two groups. The nodule was benign in 98% of cases in the No-TIRADS group and in 76.9% of cases in the TIRADS group. The use of the TIRADS score therefore allows better detection of the benignity and malignancy of thyroid nodules.
According to our results and those of the literature, the TIRADS classification is reliable for the detection of cancers with a high negative predictive value (95.23%). On the other hand, the TIRADS score is not very specific, making FNA necessary in certain indications. However, the TIRADS classification helps prevent unnecessary FNAs in a large group of thyroid lesions and significantly reduces the rate of unnecessary surgeries.
Conclusion
The early diagnosis of thyroid cancer is based on a combination of clinical, ultrasound and cytological criteria. Ultrasound is the gold standard for diagnosing, monitoring, and looking for signs of thyroid nodule malignancy. The TIRADS system standardizes ultrasound examinations and stratifies the risk of malignancy to guide management, thereby reducing operator dependency often attributed to ultrasound. According to our results and those of the literature, the combination of ultrasound with classification and FNA (when indicated) is today the best way to reduce the number of unnecessary thyroid surgeries by allowing patient selection. The dissemination of the use of the TIRADS score in our context is strongly recommended in the daily practice.
Acknowledgements
We thank our colleagues in medical imaging and pathology departments for their contribution.
Declarations
Funding
The authors declare that no funds, grants, or other support were received during the preparation of this manuscript.
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
An approval by ethics committee was not applicable.
Consent to participate
Informed consent was obtained from all individual participants included in the study.
Consent to publish
Not applicable.
Footnotes
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
References
- 1.Kamran SC, Marqusee E, Kim MI, Frates MC, Ritner J, Peters H, Barletta J. Thyroid nodule size and prediction of cancer. J Clin Endocrinol Metab. 2013;98(2):564–570. doi: 10.1210/jc.2012-2968. [DOI] [PubMed] [Google Scholar]
- 2.Tramalloni J, Wémeau JL. Consensus français sur la prise en charge du nodule thyroïdien: ce que le radiologue doit connaître. EMC Radiol Imag Médicale Cardiovasc Thorac Cervicale. 2012;7(4):1–18. doi: 10.1016/S1879-8535(12)60946-5. [DOI] [Google Scholar]
- 3.Wémeau J-L, Sadoul J-L, d’Herbomez M, Monpeyssen H, Tramalloni J, Leteurtre E, Leenhardt L. Guidelines of the French society of endocrinology for the management of thyroid nodules. Annales d’Endocrinologie. 2011;72(4):251–281. doi: 10.1016/j.ando.2011.05.003. [DOI] [PubMed] [Google Scholar]
- 4.Horvath E, Majlis S, Rossi R, Franco C, Niedmann JP, Castro A, Dominguez M. An ultrasonogram reporting system for thyroid nodules stratifying cancer risk for clinical management. J Clin Endocrinol Metab. 2009;94(5):1748–1751. doi: 10.1210/jc.2008-1724. [DOI] [PubMed] [Google Scholar]
- 5.Russ G, Royer B, Bigorgne C, Rouxel A, Bienvenu-Perrard M, Leenhardt L. Prospective evaluation of thyroid imaging reporting and data system on 4550 nodules with and without elastography. Eur J Endocrinol. 2013;168(5):649–655. doi: 10.1530/EJE-12-0936. [DOI] [PubMed] [Google Scholar]
- 6.Dean DS, Gharib H. Epidemiology of thyroid nodules. Best Pract Res Clin Endocrinol Metab. 2008;22(6):901–911. doi: 10.1016/j.beem.2008.09.019. [DOI] [PubMed] [Google Scholar]
- 7.Granja F, Morari J, Morari EC, Correa LA, Assumpção LV, Ward LS. GST profiling may be useful in the screening for thyroid nodule malignancy. Cancer Lett. 2004;209(2):129–137. doi: 10.1016/j.canlet.2003.12.013. [DOI] [PubMed] [Google Scholar]
- 8.Russ G, Bigorgne C, Royer B, Rouxel A, Bienvenu-Perrard M. Le système TIRADS en échographie thyroïdienne. J Radiol. 2011;92(7–8):701–713. doi: 10.1016/j.jradio.2011.03.022. [DOI] [PubMed] [Google Scholar]
- 9.Russ G, Bonnema SJ, Erdogan MF, Durante C, Ngu R, Leenhardt L. European Thyroid Association guidelines for ultrasound malignancy risk stratification of thyroid nodules in adults: the EU-TIRADS. Eur Thyroid J. 2017;6(5):225–237. doi: 10.1159/000478927. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 10.Haugen BR, Alexander EK, Bible KC, Doherty GM, Mandel SJ, Nikiforov YE, Wartofsky L. 2015 American Thyroid Association management guidelines for adult patients with thyroid nodules and differentiated thyroid cancer: the American Thyroid Association guidelines task force on thyroid nodules and differentiated thyroid cancer. Thyroid. 2015;26(1):1–133. doi: 10.1089/thy.2015.0020. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 11.AlbairAshamallah G, El-Adalany MA. Risk for malignancy of thyroid nodules: comparative study between TIRADS and US based classification system. Egypt J Radiol Nucl Med. 2016;47(4):1373–1384. doi: 10.1016/j.ejrnm.2016.08.021. [DOI] [Google Scholar]
- 12.Srinivas MNS, Amogh VN, Gautam MS, Prathyusha IS, Vikram NR, Retnam MK, Kudva N. 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 doi: 10.4103/2156-7514.177551. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 13.Sun C-Y, Lei K-R, Liu B-J, Bo X-W, Li X-L, He Y-P, Xu H-X. Virtual touch tissue imaging and quantification (VTIQ) in the evaluation of thyroid nodules: the associated factors leading to misdiagnosis. Sci Rep. 2017;7:41958. doi: 10.1038/srep41958. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 14.Yoon JH, Lee HS, Kim E-K, Moon HJ, Kwak JY. Malignancy risk stratification of thyroid nodules: comparison between the thyroid imaging reporting and data system and the 2014 American thyroid association management guidelines. Radiology. 2015;278(3):917–924. doi: 10.1148/radiol.2015150056. [DOI] [PubMed] [Google Scholar]
- 15.Zhang J, Liu B-J, Xu H-X, Xu J-M, Zhang Y-F, Liu C, Qu S. Prospective validation of an ultrasound-based thyroid imaging reporting and data system (TI-RADS) on 3980 thyroid nodules. Int J Clin Exp Med. 2015;8(4):5911–5917. [PMC free article] [PubMed] [Google Scholar]