|Year : 2019 | Volume
| Issue : 2 | Page : 40-46
Does adding computed tomography on top of ultrasonography for evaluating thyroid diseases provide a better outcome?
Haneen Hussain Sebeih1, Khalid Alqahtani2, Jabir Alharbi3, Nasser Alwehaibi4, Ahmad A Aldereihim5, Taherah Islam6
1 Department of Otolaryngology-Head and Neck Surgery, Ohoud Hospital, Madinah, Saudi Arabia
2 Department of Otolaryngology-Head and Neck Surgery, King Abdul Aziz University Hospital, King Saud University, Riyadh, Saudi Arabia
3 Department of Otolaryngology-Head and Neck Surgery, College of Medicine, Majmaah University, Majmaah City, Riyadh, Saudi Arabia
4 Department of Otolaryngology-Head and Neck Surgery, King Fahad Medical City, Riyadh, Saudi Arabia
5 Department of Medical Imaging, King Fahad Medical City, Riyadh, Saudi Arabia
6 College of Medicine and Research Center, King Saud University, Riyadh, Saudi Arabia
|Date of Submission||22-Jan-2019|
|Date of Decision||20-Mar-2019|
|Date of Acceptance||19-Apr-2019|
|Date of Web Publication||22-Oct-2019|
Dr. Haneen Hussain Sebeih
Department of Otolaryngology-Head and Neck Surgery, Ohoud Hospital, Madinah
Source of Support: None, Conflict of Interest: None
Introduction: Thyroid disease is a common medical disorder. And thyroid cancer considered the second-most common cancer among the young Saudi females. Ultrasonography (US) and computed tomography (CT) are used in the diagnosis of thyroid nodules. However, US has its limitations, and CT scan is superior in detecting important details that would affect patient care and prevents possible complications. Objective: The study evaluates the benefits of CT scans implementation together with the US as a preoperative evaluation of any thyroid diseases which can improve thyroid patient care. Methodology: The retrospective study was conducted on a total of 207 patients, in a tertiary center, Riyadh, Saudi Arabia. Results: A total of 207 patients with thyroid diseases who had both US and CT scan done despite thyroid surgery done or not (164 females and 43 males; mean age, 44.6 ± 14.5 years) were included in our study, and any patient with improper imaging protocol or poor US or CT image quality was excluded. From there, 207 patients, we had 88 patients with benign and 85 with malignant pathology (+34 patients no surgery done for them). The present study showed that US had better specificity and accuracy in the prediction of thyroid malignancy comparing to the CT scan. Furthermore, CT had a significant P < 0.05 in detecting extension to retrosternal or surrounding structures, major vessels involvement, tracheal compression, and pathological lymph node. Conclusions: CT scan of the neck is a useful technique in detecting additional details about the thyroid and surrounded tissues. This study suggests that preoperative CT scan implementations on top of US are positively associated with a good strategy of surgery, postoperative complication prevention, and to success the thyroid surgery in the Saudi population.
Keywords: Evaluation of thyroid nodule, preoperative evaluation, thyroid, ultrasound/computed tomography
|How to cite this article:|
Sebeih HH, Alqahtani K, Alharbi J, Alwehaibi N, Aldereihim AA, Islam T. Does adding computed tomography on top of ultrasonography for evaluating thyroid diseases provide a better outcome?. Saudi J Otorhinolaryngol Head Neck Surg 2019;21:40-6
|How to cite this URL:|
Sebeih HH, Alqahtani K, Alharbi J, Alwehaibi N, Aldereihim AA, Islam T. Does adding computed tomography on top of ultrasonography for evaluating thyroid diseases provide a better outcome?. Saudi J Otorhinolaryngol Head Neck Surg [serial online] 2019 [cited 2019 Dec 12];21:40-6. Available from: http://www.sjohns.org/text.asp?2019/21/2/40/269714
| Introduction|| |
Thyroid disease is a common medical disorder. And thyroid cancer is considered the second-most common cancer among the young Saudi females. Thyroid nodules are very common medical problems account for 5% in women and 1% in men. The importance of detecting thyroid nodules is malignancies, which account for 7%–15% of patients.
Thyroid enlargement is a worldwide disease with an estimated prevalence of 15.6%. Large thyroid extending retrosternal or even down in the mediastinum can cause compression symptoms to the trachea, esophagus or major vessels necessitate surgical resection and preoperative planning for possible multiteam approaches.
The management of thyroid disease varies from small, asymptomatic nodules that do not need any surgical intervention, only regular follow-up in the clinic to more complicated life-threatening nodular enlargement needs difficult surgery, or it could be malignant nodules.
Usually, we use the ultrasonography (US) thyroid as the initial diagnostic imaging in evaluating any thyroid or neck mass. It gives us good information about the gland and nodule size, consistency, echogenicity, presence of calcification, character of the borders, and if there are any pathological lymph nodes. On the other hand, US has disadvantages because it is operator dependent.
Regarding the computed tomography (CT) scan, it can illustrate more detailed characters regarding size, provide detailed anatomy of the thyroid masses, thyroid lobe extension (either retrosternal or to surrounding structures) status of the airway, major vasculature involvements, and the presence of pathological looking lymph nodes.
The majority of retrosternal thyroid extension are usually removed by the transcervical approach; nevertheless, median sternotomy is needed for complete removal of the gland and to save the great vessels around it. Careful preoperative workup to identify any patients with suspicion retrosternal extension that requires sternotomy to facilitates optimal use of health care resources to improve patient care. Hence, preoperative evaluation of retrosternal goiter using CT scan of the neck and thorax is helpful to evaluate thyroid extension.
Preoperative CT scan imaging will be useful in the preoperative period for good planning and to prevent postoperative complication. It may also give the surgeon idea about the extension of the disease posteriorly, to prevent leaving any residual thyroid tissue after resection. Moreover, remnant thyroid tissue can significantly affect the prognosis, disease recurrence, and need for radioisotope ablation not only with malignant thyroid tumors but also with some benign diseases such as Graves' disease.
Evaluating the presence of extrathyroidal extension (ETE) is considered as a strong indicator that can play a major role in planning surgical technique (hemi-/total thyroidectomy or central neck dissection), incision type. And the need for postoperative adjuvant therapy is considered critical determinants for postoperative radioactive iodine (RAI).
US still cannot predict accurately all ETE due to the high rate of false-positive and false-negative findings. On the other hand, regarding the usefulness of CT in thyroid diseases, especially papillary thyroid cancer (PTC) which is a common endocrine neoplasm with a high incidence of cervical lymphatic metastasis which occurs in 35%–80% of patients. Metastatic spread of thyroid cancer to the neck significantly increase the risk of local or regional recurrence of the tumor and the need for another surgery, but it does not seem to affect overall or disease-specific survival. CT scan of the neck is preferable radiological imaging for any neck lesions because it gives us a clear and wide field of view.
| Methodology|| |
Study design and population
This is a retrospective chart review study, which was approved by the King Saud University, for patients with thyroid diseases who visit King Abdulaziz University Hospital and King Fahad Medical City, head and neck clinic from July 2014 to March 2018, as a Tertiary Referral Center, in Riyadh, Saudi Arabia.
We included all patients with thyroid diseases who had both US and CT scan done despite thyroid surgery done or not.
We excluded patients with improper imaging protocol or poor US and CT scan image quality.
The ethical approval was obtained from the IRB of KSU (IRB no. E-18-3232).
Imaging technique and analysis
Usually, thyroid US was performed from the submental area to the supraclavicular level, using a high-resolution US instrument.
Neck CT scans were conducted using a 64-channel, multidetector CT scanner, with an injection of intravenous contrast medium (2.0 mL/kg, maximum 100 mL; 3.0 mL/s, automatic venous injection with 20–30 mL saline flushing).
Neck CT scan was performed in the axial planes from the skull base to the upper mediastinum.
All non- and contrast-enhanced (axial, coronal, and sagittal) images were acquired in all cases.
US and CT images analysis were performed independently by different radiologists with excellent experience using a picture archiving and communication system.
- The US features were analyzed based on the glandular size. The anteroposterior, transverse, and longitudinal diameters of both lobes of the thyroid were measured in both modalities and classified into six categories: <1, 1–2 cm (normal), >2–4, >4–6, >6–8, and >8 cm
- Regarding the margin, the thyroid nodules were classified as smooth, irregular, or poorly defined. Irregular thyroid margins were defined as disruption of the perithyroidal echogenic line between the site of the thyroid and the thyroid capsule as seen on US or CT
- Nodule echogenicity was classified according to a comparison with the adjacent parenchyma and strap muscle as follows: isoechoic and hypoechoic (defined as the same echogenicity or decreased echogenicity, as compared with the adjacent normal thyroid parenchyma), respectively. Hyperechoic, including complete calcification with marked hyperechogenicity and posterior shadowing and heterogeneous,
- On the basis of a color Doppler US and contrast enhancement CT scan were divided as follows: normal or increased vascularity
- The presence or absence of necrosis within the gland or the nodules
- Based on the degree of calcification, the thyroid nodule was classified as noncalcified and calcified
- Detailed character of the thyroid isthmus also evaluated
- The retrosternal extension was evaluated in both imaging modalities
- ETE on sonography was defined as the presence of a capsular abutment or protrusion. The capsular abutment is defined as lack of separating tissue between the thyroid cancer and the thyroid capsule, which can be evaluated by CT scan as well
- A lymph node also evaluated. A positive lymph node is observed if there is an increased echogenicity, cystic changes, calcification, loss of the fatty hilum, or a poorly defined margin with a peripheral halo and the location of the lymph nodes either central or in the lateral compartment with their numbers
- Evaluation of thyroid extension to surrounding structures either to the muscle, blood vessels, soft-tissue involvement, tracheal or esophageal invasion, major vessels involvement and tracheal compression by CT, which cannot be assessed by the US.
Using the Bethesda classification as recommended in the thyroid American Thyroid Association (ATA) guidelines are as follows:
- Nondiagnostic or unsatisfactory
- Atypia of undetermined significance or follicular lesion of undetermined significance
- Follicular neoplasm or suspicion for a follicular neoplasm
- Suspicious for malignancy
All patients with thyroid nodules who underwent hemi- or total thyroidectomy, done by a single surgeon with excellent experience in his field.
Histopathology of thyroid parenchyma
The histopathological classification was carried out according to the following criteria:
- Benign (benign multinodular goiter and Hashimoto thyroiditis)
- Malignant (papillary, follicular, medullary, anaplastic, and micro-papillary thyroid carcinoma).
Demographic data (patient's age and gender) were collected from each institution's electronic medical records and medical archives.
All statistical analyses were performed with statistical software (SPSS statistics, version 24.0, IBM Corp., Armonk, New York, USA); P < 0.05 was considered as statistically significant throughout this article.
| Results|| |
Study sample characteristics
We had a total of 207 patients (164 women and 43 men; mean age, 44.6 ± 14.5 years; age range, 10–83 years) and 88 patients with benign and 85 with malignant pathology.
From all these data, we had the following final pathology: about 33.8% PTC, 3.9% follicular thyroid cancer, 1.9% medullary thyroid cancer, 0.5 anaplastic thyroid cancer, 42.5% benign pathology, and 1% micro-PTC adding about 16.4% (34 patients) no surgery done for them yet [Figure 1].
US had better specificity and accuracy in the prediction of thyroid malignancy comparing to the CT, as seen in [Table 1].
Different characters detected in both imaging modalities, as seen in [Table 2].
Furthermore, we find some significant P values with CT scan in the detection of nodular necrosis comparing to the US (0.003 vs. 0.68).
P value was significant in the following parameters:
- Retrosternal extension (P = 0.019)
- Extension to surrounding structure (P = 0.039)
- With major vessels involvement about 0.014
- In detecting pathologic lymph nodes about 0.002
- Tracheal compression (P = 0.002).
| Discussion|| |
According to ATA thyroid guidelines, thyroid US is used as the first-line diagnostic modality for thyroid nodules.
In addition, US is useful for evaluating thyroid lesions, thyroglossal duct cyst, and pyramidal thyroid lobe. Moreover, the advantages of US over the CT scan that did not require any ionized contrasted medium injection and had no radiation hazard.
US has known limitation of being operator dependent but CT does not have this limitation and is more standardized. Adding on this advantage, the chance of detection incidental thyroid nodules by CT is high, but US evaluation has been applied for further evaluation of the nodular character because of limited information on CT to differentiate malignant from benign thyroid nodules.
We know that the CT scan of the head and neck is a common imaging modality for evaluating different neck lesions and can provide a wide field of view and clearly delineate any bone or air containing organs. Usually, we use CT to assist in clinical diagnosis and used for tumor-node-metastasis staging, but some suggest that routine use of preoperative neck CT not recommended in patients with thyroid cancer because there is a risk of inherent radiation hazard and high cost.
Till this time, nodule size >1 cm better to be evaluated by CT scan, despite there is no guidelines and no evidence to support this cutoff size. However, any thyroid nodules smaller than 1 cm in the largest diameter are common and they can be easily identified by a high-resolution CT scan.
CT scan provides an excellent resolution and the higher image quality of the thyroid in relation to the surrounding soft tissues in the lower neck and any other lesions. Furthermore, CT can demonstrate the whole neck from the skull base to the upper chest, not just the thyroid and can clearly demonstrate if there is any retrosternal extension of the thyroid as well as the presence of aberrant thyroid tissue in the neck or chest on any other lesions.
Furthermore, CT scan done preoperatively is very helpful in detection if there is any tumor invasion to adjacent structures, such as the muscle, vessels, and soft tissue, and to identify any lymph node metastasis to the neck or mediastinum, and it can give us more important detail such as the presence of ectopic thyroid, presence of pyramidal lobe, and accessory thyroid.
Thyroid nodules characteristic reviewed in both modalities, for example, calcification in thyroid nodules are a common finding on imaging and histopathology. Calcifications have been reported in up to 21% of plain X-rays and 42% of US.
Thyroid nodules calcifications may occur in both the benign and malignant thyroid lesion, but the incidence of malignancy in a thyroid nodule containing calcification is increased compared with a noncalcified nodule.
Calcification was noted by US in 76 of 207 patients, 26% (54 of 207) of the malignant thyroid nodules and about 10.6% (22 of 207) of the nodules with benign pathology. However, by the CT scan calcification was noted in 116 patients, 36.7% (76 of 207) of the malignant thyroid nodules, and about 19.3% (40 of 207) of the nodules with benign pathology. The incidence of cancer was greater in calcified nodules than in noncalcified nodules (P< 0.005 by US and 0.012 by the CT scan).
Several authors have attempted to predict malignancy from the character of distribution of calcification within the thyroid nodules. Most of the macrocalcified lesions were associated with benign lesion, and most of the malignant microcalcified lesions were associated with papillary carcinoma.
Previous literature has shown that calcification is more common in malignant thyroid nodules than in benign lesions by US. The reported incidence of calcification is 26%–79% in malignancy and 8%–39% in benign lesions. Yet, in another study, 57% (65 of 114) of the malignant nodules contained intrathyroidal calcifications on CT, whereas only 26% (70 of 269) of benign lesions had calcifications. Moreover, there was no significant difference in cancer risk between male and female calcified nodules in this study.
Hence, keeping in mind that CT scan findings of thyroid calcification should alert the surgeon to the possibility of thyroid carcinoma in these patients, despite fine-needle aspiration is negative for malignancy. We also found no relation between the mean age and incidence of calcification.
Despite US is the major diagnostic imaging as we said above, CT can guide us for proper preoperative evaluation, preparing and intervention, especially in case of huge thyroid or retrosternal extension, the presence of malignant lesions with suspicion of extracapsular extension or cervical lymph nodes metastasis. CT provides us with some advantages over US, for example, CT is excellent in certain cases, such as patients with short and thick neck or in case of retrosternal extension, which may be obscured by the bony structure like the sternum or tracheal air shadow in US.
The locations of the lymph nodes in the neck were divided into two subgroups: the central group (N1a, Level VI) and the lateral group (N1b, Levels I–V) to determine the nodal staging based on the imaging analysis.
When evaluating the thyroid by CT scan we look for any lymph node metastases, which are common in case of thyroid cancer, especially papillary carcinoma, which if present leads to an increased risk of recurrence and reduced survival., We found a greater association between calcified malignant nodules and the presence of lymph node metastasis. Hence, thyroid calcification detected on the preoperative evaluation of the CT could represent an increased risk for thyroid malignancy.
It is challenging and sometimes difficult for the surgeon and radiologist to detect and diagnose the cervical lymph node metastasis preoperatively by US. The criteria for metastatic lymph nodes from normal or nonmetastatic lymph nodes for example, loss of fatty hilum, change of nodal echogenicity, round shape instead of normal oval shape, calcification, cystic change and an abnormal color Doppler pattern.
The disadvantages of US in detecting metastatic lymph nodes are because thyroid gland and the presence of multiple nodules could mask any metastatic node. Furthermore, surrounding structures in the central neck, clavicle and sternum decrease the ability of US to detect central metastatic nodes. All of these making the US had lower sensitivity and limited in detecting metastatic lymph nodes in the central compartment which was important to be detected preoperatively to determine the extent of the surgery and counseling the patient regarding possible complication.
Even with the great improvement in the imaging quality and techniques of using US for evaluating the thyroid gland, especially detecting small nodules, US still cannot predict accurately ETE due to the high rate of false-positive and negative findings.
Therefore, it is imperative to predict the presence of ETE preoperatively to determine the extension of the surgery, and it will affect the prognosis in case of thyroid cancer. We considered that using the US with the CT scan helping to evaluate the possibility of ETE preoperatively.
In this study, the data showed that the combination of two imaging methods increases positive predictive value of ETE, retrosternal extension, airway compression, and major vessels involvement, as seen in [Figure 2].
|Figure 2: (a) US of the thyroid with a smooth surface and patent airways. (b) Computed tomography scan of the neck with intravenous contrast showing enhancement of the left thyroid lobe with right thyroid nodule abutting the thyroid capsule, irregular borders, and posterior extension reaching prevertebral fascia. (c) Computed tomography for thyroid with diffuse enlargement, it warped behind the esophagus and compressing the airway. (d) Computed tomography for thyroid with calcification and poorly defined margin with extrathyroidal extension|
Click here to view
CT scan can override the disadvantages of US, as it is a two-dimensional image. Adding on that, it can illustrate a lot of information regarding the tumor and surrounding tissue. In contrast, the US probe could compress the patient's neck and may alter and significantly distort the normal parenchyma of the thyroid and tumor. The thyroid gland is a compressible organ; hence, external compression, by the probe of the US, can make the thyroid parenchyma thinner. When the thyroid gland distorted and compressed, US can give misleading information regarding the size, extension, and how much the tumor separated from the thyroid capsule.
From this data, the combination of both imaging modalities US and CT showed the highest diagnostic accuracy. US is the first modality that is used to evaluate the thyroid nodules architecture and consistency. However, the CT scan provides greater spatial resolution, affords improved surrounding anatomical pathology.
The results of this article in Saudi people corroborate a recent report that states a successful thyroid surgery can be achieved by careful thyroid evaluation and determine the surgical modality and postoperative care. Worldwide, thyroid surgery is a safe procedure that has a low mortality rate since 1889.
For that, a good surgeon must be fully aware and mentally ready for different and any difficult anatomy of the central compartment of the neck and be aware for the most important anatomic variations and complexes like the thyroid lobe extension to prevent any operative morbidity. Most of our findings help to achieve better interpretation that leads to successful thyroid surgery, which correlated with well-planned intraoperative management as well as improves postoperative care and oncological safety. However, to confirm our findings, additional multicenter studies are required.
Our study has some limitations. First, it was done in a retrospective way and hence, there was an unavoidable selection bias. The retrospective design prevented us from evaluating all patients with a thyroid nodule.
Second, not all patients underwent thyroidectomy.
Third, microcalcifications may not have been identified in some patients when we used 3–5-mm section thickness of the CT images. Furthermore, evaluation of extrathyroidal capsule was not definitely differentiated by anatomic fibrous capsule making ETE varies subjectively.
Fourth, the very tiny nodule cannot be shown clearly in the CT scan.
Fifth, this study was done in the tertiary center with delayed presentation of some patients.
| Conclusions|| |
CT was significantly superior to US for detecting many features in the preoperative period and providing more diagnostic advantages. An expert surgeon must be mentally ready and expect a lot of challenging anatomical variations for appropriate and proper planning to deal with all difficulties. For this reason, preoperative implementing of CT with US is very helpful to identify more detailed information. Therefore, proper and complete preoperative evaluation and mental awareness have a clear positive effect on the prevention of postoperative complications and surgical morbidity in the Saudi population.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
| References|| |
Vanderpump MP. The epidemiology of thyroid disease. Br Med Bull 2011;99:39-51.
Hussain F, Iqbal S, Mehmood A, Bazarbashi S, ElHassan T, Chaudhri N. Incidence of thyroid cancer in the Kingdom of Saudi Arabia, 2000-2010. Hematol Oncol Stem Cell Ther 2013;6:58-64.
American Thyroid Association (ATA) Guidelines Taskforce on Thyroid Nodules and Differentiated Thyroid Cancer, Cooper DS, Doherty GM, Haugen BR, Kloos RT, Lee SL, et al.
Revised American Thyroid Association management guidelines for patients with thyroid nodules and differentiated thyroid cancer. Thyroid 2009;19:1167-214.
Andersson M, Takkouche B, Egli I, Allen HE, de Benoist B. Current global iodine status and progress over the last decade towards the elimination of iodine deficiency. Bull World Health Organ 2005;83:518-25.
Chen AY, Bernet VJ, Carty SE, Davies TF, Ganly I, Inabnet WB 3rd
, et al.
American Thyroid Association statement on optimal surgical management of goiter. Thyroid 2014;24:181-9.
Braun EM, Windisch G, Wolf G, Hausleitner L, Anderhuber F. The pyramidal lobe: Clinical anatomy and its importance in thyroid surgery. Surg Radiol Anat 2007;29:21-7.
Sundram F, Robinson BG, Kung A, Lim-Abrahan MA, Bay NQ, Chuan LK, et al.
Well-differentiated epithelial thyroid cancer management in the Asia Pacific region: A report and clinical practice guideline. Thyroid 2006;16:461-9.
Gilliland FD, Hunt WC, Morris DM, Key CR. Prognostic factors for thyroid carcinoma. A population-based study of 15,698 cases from the surveillance, epidemiology and end results (SEER) program 1973-1991. Cancer 1997;79:564-73.
Noguchi S, Murakami N. The value of lymph-node dissection in patients with differentiated thyroid cancer. Surg Clin North Am 1987;67:251-61.
Nusynowitz ML. Thyroid imaging. Lippincotts Prim Care Pract 1999;3:546-55.
Frates MC, Benson CB, Charboneau JW, Cibas ES, Clark OH, Coleman BG, et al.
Management of thyroid nodules detected at US: Society of radiologists in ultrasound consensus conference statement. Radiology 2005;237:794-800.
Moon WJ, Jung SL, Lee JH, Na DG, Baek JH, Lee YH, et al.
Benign and malignant thyroid nodules: US differentiation – Multicenter retrospective study. Radiology 2008;247:762-70.
Youserm DM, Huang T, Loevner LA, Langlotz CP. Clinical and economic impact of incidental thyroid lesions found with CT and MR. AJNR Am J Neuroradiol 1997;18:1423-8.
Martinez CR, Gayler BW, Kashima H, Siegelman SS. Computed tomography of the neck. Radiographics 1983;3:9-40.
Kim E, Park JS, Son KR, Kim JH, Jeon SJ, Na DG. Preoperative diagnosis of cervical metastatic lymph nodes in papillary thyroid carcinoma: Comparison of ultrasound, computed tomography, and combined ultrasound with computed tomography. Thyroid 2008;18:411-8.
Nguyen XV, Choudhury KR, Eastwood JD, Lyman GH, Esclamado RM, Werner JD, et al.
Incidental thyroid nodules on CT: Evaluation of 2 risk-categorization methods for work-up of nodules. AJNR Am J Neuroradiol 2013;34:1812-7.
Ahmed S, Johnson PT, Horton KM, Lai H, Zaheer A, Tsai S, et al.
Prevalence of unsuspected thyroid nodules in adults on contrast enhanced 16- and 64-MDCT of the chest. World J Radiol 2012;4:311-7.
Binder RE, Pugatch RD, Faling LJ, Kanter RA, Sawin CT. Diagnosis of posterior mediastinal goiter by computed tomography. J Comput Assist Tomogr 1980;4:550-2.
Kim DW, Jung SL, Baek JH, Kim J, Ryu JH, Na DG, et al.
The prevalence and features of thyroid pyramidal lobe, accessory thyroid, and ectopic thyroid as assessed by computed tomography: A multicenter study. Thyroid 2013;23:84-91.
Seiberling KA, Dutra JC, Grant T, Bajramovic S. Role of intrathyroidal calcifications detected on ultrasound as a marker of malignancy. Laryngoscope 2004;114:1753-7.
Khoo ML, Asa SL, Witterick IJ, Freeman JL. Thyroid calcification and its association with thyroid carcinoma. Head Neck 2002;24:651-5.
Kakkos SK, Scopa CD, Chalmoukis AK, Karachalios DA, Spiliotis JD, Harkoftakis JG, et al.
Relative risk of cancer in sonographically detected thyroid nodules with calcifications. J Clin Ultrasound 2000;28:347-52.
Wu CW, Dionigi G, Lee KW, Hsiao PJ, Paul Shin MC, Tsai KB, et al.
Calcifications in thyroid nodules identified on preoperative computed tomography: Patterns and clinical significance. Surgery 2012;151:464-70.
Ito Y, Higashiyama T, Takamura Y, Miya A, Kobayashi K, Matsuzuka F, et al.
Risk factors for recurrence to the lymph node in papillary thyroid carcinoma patients without preoperatively detectable lateral node metastasis: Validity of prophylactic modified radical neck dissection. World J Surg 2007;31:2085-91.
Scheumann GF, Gimm O, Wegener G, Hundeshagen H, Dralle H. Prognostic significance and surgical management of locoregional lymph node metastases in papillary thyroid cancer. World J Surg 1994;18:559-67.
Rosário PW, de Faria S, Bicalho L, Alves MF, Borges MA, Purisch S, et al.
Ultrasonographic differentiation between metastatic and benign lymph nodes in patients with papillary thyroid carcinoma. J Ultrasound Med 2005;24:1385-9.
Huang CF, Jeng Y, Chen KD, Yu JK, Shih CM, Huang SM, et al.
The preoperative evaluation prevent the postoperative complications of thyroidectomy. Ann Med Surg (Lond) 2015;4:5-10.
Cernea CR, Brandão LG, Hojaij FC, De Carlucci D, Montenegro FL, Plopper C, et al.
How to minimize complications in thyroid surgery? Auris Nasus Larynx 2010;37:1-5.
Mete O, Rotstein L, Asa SL. Controversies in thyroid pathology: Thyroid capsule invasion and extrathyroidal extension. Ann Surg Oncol 2010;17:386-91.
[Figure 1], [Figure 2]
[Table 1], [Table 2]