A narrative review of the role of cross-sectional imaging in the management of thyroid carcinoma: Imaging guidelines and T-CIRADS : Cancer Research, Statistics, and Treatment

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Review Article

A narrative review of the role of cross-sectional imaging in the management of thyroid carcinoma: Imaging guidelines and T-CIRADS

Mahajan, Abhishek; Agarwal, Ujjwal; Padashetty, Shubham; Shukla, Shreya; Smriti, Vasundhara; Rastogi, Shivam; Vaish, Richa; Kumar, Suman; D’Cruz, Anil

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Cancer Research, Statistics, and Treatment: Jul–Sep 2022 - Volume 5 - Issue 3 - p 490-498
doi: 10.4103/crst.crst_300_21
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Abstract

INTRODUCTION

With the increasing prevalence of thyroid malignancies, they now dominate the cohort of endocrine malignancies.[12] Though ultrasonography is the primary imaging test of choice for the evaluation of thyroid nodules, early evaluation of head-and-neck pathologies by cross-sectional imaging can lead to timely and more frequent detection of occult thyroid nodules which can be correlated with ultrasonography. Most of the thyroid nodules may show benign histomorphology, but the incidentally detected malignancies also usually carry a good prognosis. However, many thyroid carcinomas including follicular, anaplastic, poorly differentiated, medullary, and few variants of papillary thyroid carcinomas can carry a poor prognosis, mandating early detection for optimal patient management for which cross-sectional studies are essential.[34]

T-CIRADS, a novel synoptic reporting system that has been developed by our group serves as a fundamental tool for the multidisciplinary teams guiding the medical and surgical management of patients with thyroid malignancies. Cross-sectional imaging has become one of the key imaging tools to guide surgical management. Familiarizing the radiologists with synoptic reporting of computed tomography (CT) and magnetic resonance imaging (MRI) will help streamline the reports resulting in standardized reporting, which will improve patient outcomes. Pre-surgical planning and disease mapping can also be performed to aid the planning of the surgical margins and planes across the viscera. T-CIRADS which consists of synoptic reporting is depicted in Supplementary Table 1.

Since the introduction and easy availability of cross-sectional imaging, the burgeoning number of incidentally detected thyroid nodules has become a matter of concern. The work-up and management of these nodules are not well defined due to the low rate of malignancy and excellent prognosis of the detected carcinomas to which the patients rarely succumb.[56] Ultrasonography, though the primary modality used for the characterization of thyroid nodules may not be very helpful in the assessment of locoregional spread on the posterior aspect of the thyroid, and thus, there is a need for other imaging options like CT and MRI.[7] Similarly, tumors that appear large on clinical examination and are suggestive of local invasion require further cross-sectional evaluation for adequate pre-surgical planning.

Cross-sectional imaging allows for the optimal evaluation of the locoregional spread of the tumor with respect to the surrounding critical neck structures like the trachea, esophagus, larynx, and major vessels. Further comment on the involvement of the trachea or cricoid cartilage as well as the extra-thyroidal extension is important for the planning of surgery; cross-sectional imaging plays a pivotal role in this aspect. It also has excellent resolution for imaging the lymph nodes in the central and lateral compartments. A short delay in radioactive iodine (RAI) therapy can be expected after the use of contrast CT which uses iodinated intravenous contrast media. In such cases, MRI can serve as an excellent alternative as it has no effect on RAI therapy.

This review article focuses on the major changes and key pre-surgical cross-sectional imaging findings mentioned in the American Joint Committee on Cancer (AJCC) 8th edition and describes how these changes are to be incorporated in radiology reports thus influencing the surgical staging and management of thyroid carcinoma.

METHODS

We performed a comprehensive search of abstracts of pre-operative markers in thyroid carcinoma and their key implications on the AJCC 8th edition. We included studies reporting data on the role of pre-surgical imaging and markers in thyroid carcinoma. We selected studies that were published in English. The keywords for medical subject headings included the following: cross-sectional imaging, thyroid carcinoma, AJCC 8th edition, extra-thyroidal extension, strap muscle involvement, recurrent laryngeal nerve involvement, tracheal invasion, esophageal invasion, laryngeal invasion, vascular invasion, and nodal and distant metastasis. The following filters were applied: Full text, English, humans, cancer, and article type: guideline, meta-analysis, systematic review, and randomized controlled trial. We searched in PubMed, Cochrane CENTRAL, MEDLINE, Embase, and Google Scholar. We excluded articles for which the full text was not available, and those that described non-human studies. The search strategy is outlined in Figure 1.

F1
Figure 1:
The strategy for the literature search for the review article on the role of pre-surgical imaging and radiological markers in thyroid carcinoma

MANAGEMENT OF THYROID NODULES

Benign thyroid nodules largely comprise colloid nodules, cysts, follicular adenomas, Hashimoto’s, and Graves’s thyroiditis. Malignant causes include papillary, follicular, anaplastic, and medullary carcinoma, thyroid lymphoma, and metastases. Clinical history and physical examination remain the initial steps in the assessment of clinically palpable or incidentally noted thyroid nodules. Laboratory tests and imaging follow the clinical work-up; the imaging algorithm is discussed in Figure 2.

F2
Figure 2:
Management of thyroid nodules—An algorithmic approach (PET: Positron emission tomography; FNAC: Fine needle Aspiration Cytology; USG: Ultrasonography; ACR-TIRADS:ACR-TIRADS=American College of Radiology Thyroid Imaging Reporting and Data Systems)

IMPORTANT EXCERPTS FROM THE AJCC 8TH EDITION

Lymph nodal involvement irrespective of the anatomical site is staged in a single category (N1).[8-10] Regardless of the site of nodal metastasis, the presence of N1 disease plays a critical role in early-stage tumors, similar to extra-thyroidal extension in advanced-stage malignancies, both of which independently influence survival.[6] In patients in whom the disease presents late, that is, in the fifth or sixth decades of life (45–55 years), the prognosis is also poor.[6] Keeping these points in mind, there are key imaging features that need to be addressed in the radiology report considering their impact on the management and thus the overall prognosis. These findings are discussed in detail in Table 1.

T1
Table 1:
Major changes in the American Joint Committee on Cancer (AJCC) 8th edition of the staging system[4]

INDICATIONS FOR CROSS-SECTIONAL IMAGING

Although ultrasonography is operator dependent, it is extremely sensitive. However, it is difficult to evaluate the deeper anatomic structures on ultrasonography especially those posterior to the trachea. Ultrasonography is helpful in the pre-operative imaging of the bilateral neck nodes and in performing a biopsy of these nodes. On baseline ultrasonography, if nodal metastasis or advanced disease are visualized, plain and contrast CT neck and thorax are recommended for further planning, particularly for surgical management. Pre-contrast CT can be used to detect calcified nodes and ectopic thyroid tissue.[11]

Contrast CT/MRI is helpful in the evaluation of the enhancement pattern and the cystic changes associated with the disease or the metastatic lymph nodes. In the presence of extra-thyroidal extension, the incidence of nodal metastases and lymphovascular invasion is high.[12] The sensitivity of ultrasonography for identifying extra-thyroidal extension is very low; however, capsular abutment can serve as a surrogate marker for the presence of extra-thyroidal extension with a 100% sensitivity; a lack of capsular abutment has a 100% negative predictive value for excluding an extra-thyroidal extension. On ultrasonography, if there is more than 1 mm normal thyroid parenchyma surrounding the nodule, the possibility of extra-thyroidal extension is <10%. Similarly, in case the dimension of a nodule that closely abuts the capsule is more than 1 cm, the possibility of extra-thyroidal extension is over 80%. In any patient presenting with hoarseness, stridor, hemoptysis, positional dyspnea, rapid increase in swelling, or progressive dysphagia with a hard fixed mass on examination, the possibility of extra-thyroidal extension should be actively evaluated. In such cases, cross-sectional imaging, that is, CT and MRI modalities which can provide excellent resolution of cervical and paratracheal lymph nodes are essential to optimally evaluate the extent of disease, the spread to surrounding structures, and any involvement of the tracheal or cricoid cartilage.[13] The posterior extension of the tumor into the tracheoesophageal groove or between the laryngeal cartilage and hypopharyngeal wall can be detected based on the amount of fatty tissue effacement.[14] As compared to ultrasonography, cross-sectional imaging has better accuracy for the detection of extra-thyroidal extension. A study published by the American Head and Neck Society reported that although CT is not very sensitive for the detection of esophageal invasion, it is highly specific.[15]

Additionally, the mediastinal structures including the nodes and vascular features like the presence of an aberrant subclavian artery, or a double aortic arch are not easily delineated on ultrasonography[16]; a cross-sectional study can detect these easily, thus aiding in the surgical planning. Non-recurrent inferior laryngeal nerve, a variant of the inferior laryngeal nerve should be kept in mind while operating when there is an aberrant right subclavian artery.

WHICH IMAGING MODALITY SHOULD BE USED, AND HOW?

CT is ideally performed by covering the head, neck, and upper thorax region. CT images are acquired in a soft tissue window before reconstruction of the raw data by the bone algorithm and multiplanar reformats which are essential for evaluation. Simultaneously, a CT chest covering the upper abdomen is also done to rule out distant metastasis [Table 2].

T2
Table 2:
CT protocol in the pre-surgical staging of thyroid carcinoma[13]

The MRI protocol includes imaging from the base of the skull to the tracheal carina and comprises a three-plane localizer with turbo spin-echo imaging, done in the following sequence: axial and coronal T1-weighted images, axial T2-weighted images, axial, and coronal fat-saturated T2-weighted images, followed by a series of diffusion-weighted images and lastly, contrast-enhanced axial and coronal T1-weighted images.[17] On MRI, the thyroid gland appears T1 hyperintense and T2 iso to hypointense on non-contrast images and homogeneously enhances on post-gadolinium images. Considering the high soft tissue contrast of MRI, tumor invasion of structures, such as the strap muscle, larynx, and esophagus, and tumor infiltration of the marrow[121819] are optimally evaluated on MRI. Diffusion-weighted imaging aids in the differentiation of benign from malignant nodules as the benign nodules have a higher apparent diffusion coefficient value than the malignant ones. MR spectroscopy using long echo-time is more sensitive for the differentiation of benign follicular lesions from thyroid carcinoma. A choline peak with raised choline/creatinine ratio can be identified ranging from 1.6 as observed in well-differentiated carcinomas to 9.4 in anaplastic thyroid carcinomas, whereas no peak is seen in normal thyroid tissue.

Pre-operative evaluation of advanced thyroid cancer should ideally be supplemented by functional imaging on a hybrid scanner in the same session.[192021] In the case of anaplastic thyroid cancer, a histologically proven diagnosis of the primary tumor along with [18F] fluorodeoxyglucose (FDG) positron emission tomography (PET)/CT, contrast-enhanced computed tomography (CECT), and PET/MR of the neck and mediastinum are essential before surgery to guide the surgeon regarding the exact extent of disease.[22-24] Recommendations for the evaluation of medullary thyroid carcinoma are Gallium DOTATOC and FDG-PET. A comparison between the different imaging modalities is shown in Table 3.

T3
Table 3:
Comparison of different modalities in the pre-surgical disease assessment of thyroid malignancies, including ultrasound, CECT, MRI, FDG-PET-CT, 18 Fluorine-18-l-Dihydroxyphenylalanine (18 F-DOPA), and radionuclide imaging

EXTRA-THYROIDAL EXTENSION

A small proportion (10–15%) of well-differentiated thyroid carcinomas present as locally advanced carcinoma which is defined as involvement and breach of the surrounding thyroid capsule thus infiltrating the nearby structures such as the strap muscles, trachea, larynx, esophagus, and either of the two laryngeal nerves; if the disease is more extensive, then there is further infiltration of the carotids and internal jugular veins and the prevertebral fascia[31-39] [Figures 3 and 4]. The Shin classification describes the tracheal involvement on CT thus preparing the surgeon for either a shave procedure in early involvement or a segmental resection in case of extensive involvement [Figure 5].

F3
Figure 3:
Pictorial representation with axial contrast enhanced computed tomography (CECT) and ultrasonography images representing the extra-thyroidal extension and the grade. (a) Grade 0—Thyroid parenchyma completely envelopes the tumor (b) Grade 1—Percentage of the tumor perimeter in contact with the thyroid capsule is 1–25% (c) Grade 2—Percentage of the tumor perimeter in contact with the thyroid capsule is 25–50% (d) Grade 3—Percentage of the tumor perimeter in contact with the thyroid capsule is >50%
F4
Figure 4:
Axial contrast enhanced computed tomography (CECT) images depicting (a) Strap muscle involvement (arrow) (b) Prevertebral fascia involvement (arrow) (c) Left vocal cord palsy with nodule extension into the left tracheoesophageal groove (arrow) (d) Tumor thrombosis of the left internal jugular vein, and (e) Carotid involvement more than 270°
F5
Figure 5:
Axial contrast enhanced computed tomography (CECT) images which describe the Shin classification (a) Grade 0: >5 mm distance between the tumor and the trachea. (b) Grade 1: Nodule breaches the capsule of the thyroid gland and does not invade the external perichondrium of the trachea but just abuts it (c) Grade 2: Disease breaches the capsule of the thyroid gland and causes cartilage destruction (d) Grade 3: Disease breaches the capsule of the thyroid gland and further involves the lamina propria of the tracheal mucosa with no involvement of the mucosa in the form of elevation or penetration (e) Grade 4: Full thickness invasion of the tracheal mucosa with associated expansion which is bronchoscopically seen as a bulge or an ulcerated mass

Involvement of the nearby anatomical structures dictates both the clinical presentation and therapeutic options, hence necessitating the distinction between varied forms of locally advanced thyroid malignancies.[40-42] It is the radiologist’s role to recognize and characterize the possibility of extra-thyroidal extension[43] before surgery to aid optimal surgical resection. Thus, the radiologist plays an important role in the decision-making process regarding the extent of surgery. Additionally, the decision regarding the use of post-operative RAI treatment is dependent on the amount of extra-thyroidal extension.[4344] Though newer ultrasonography techniques have improved the accuracy of detection of smaller thyroid nodules, the high false positive rate has limited the role of ultrasonography in the prediction of extra-thyroidal extension, making CT the recommended modality.

Considering the advantages and disadvantages of different imaging modalities, it is essential to combine them to improve patient outcomes. The extra-thyroidal extension of the neoplastic nodules is categorized into four groups by evaluating all axial, coronal, and sagittal CT images [Figure 3 and Table 4].

T4
Table 4:
Extra-thyroidal extension groups

NODAL AND DISTANT METASTASIS

The occurrence of metastasis by the lymphatic route is commonly seen in papillary and medullary thyroid carcinomas with nodal involvement, while the hematogenous route forms the main conduit of spread in follicular thyroid carcinomas which only rarely metastasize to the nodes.[1220] The initial presentation of papillary thyroid carcinoma and medullary thyroid carcinoma could be as a nodal mass, thus mandating either a CT or MRI in search of the primary. In papillary thyroid carcinoma, lymph node metastasis serves as an independent prognostic marker for the disease burden and a significant risk factor for possible recurrence.[22] The presence of nodes in anatomic areas such as the posterior tracheal, para esophageal, retro-pharyngeal, and mediastinal regions which are not visualized in entirety on ultrasonography necessitates the use of a cross-sectional study.[23] In cases of nodal metastasis with an unknown primary, the origin of the primary tumor from the thyroid can manifest in various ways like the appearance of cystic components, calcification, and intense enhancement or proteinaceous/hemorrhagic content appearing as hyper-density on the CT and T1 hyperintensity in the node on MRI. Such variable presentations need to be further evaluated [Figure 6].

F6
Figure 6:
Axial CT images showing (a) Metastatic bilateral cervical nodes (arrow) (b) Metastatic pulmonary nodules (arrow) (c) Skeletal metastasis (arrow)

A study by Suh et al. showed that the sensitivity and specificity of CT in the pre-operative evaluation of cervical lymph nodal involvement in patients with papillary thyroid carcinoma were 62 and 87%, respectively.[24] The sensitivity of a combined CT/ultrasonography was significantly higher at 69% than that of ultrasound alone at 51%, as shown by Suh et al.

Usually, the development of distant metastasis outside the neck is rare in well-differentiated thyroid carcinoma and the most commonly involved sites of distant metastases are the bone and lungs and rarely the brain, kidney, and soft tissue. The presence of distant metastasis at presentation indicates aggressive pathology of the primary disease. The treatment approach in such cases is total thyroidectomy and neck dissection, followed by post-operative RAI.

IMPLICATION OF KEY IMAGING FINDINGS ON MANAGEMENT

The radiologist plays an important role in highlighting the key pre-surgical imaging findings and evaluating the extent of invasion. The implication of the radiological report can be more extensive surgery, for example, laryngectomy; involvement of a vascular, thoracic, or plastic surgeon along with the primary head-and-neck surgeon, or a decision of not-to-operate. These scenarios have been highlighted along with the impact on management in Table 5.[47-53] At our institute, synoptic reporting is followed, so that none of the key findings are missed [Supplementary Table 1].

T5
Table 5:
Implication of the key imaging findings of thyroid imaging on management
T6
Supplementary Table 1:
Cross-sectional synoptic reporting followed in the Department of Radiodiagnosis, Tata Memorial Hospital, Mumbai, India

CONCLUSION

Total thyroidectomy with possible removal of the adjacent infiltrated critical structures along with neck dissection and post-operative risk stratification according to the American Thyroid Association criteria are essential for optimal management and prolonged survival. For patients with a poor Eastern Cooperative Oncology Group performance status, extensive locoregional spread, or the presence of multiple distant metastases, conservative shaving of the thyroid, and avoiding a radical approach with the use of post-operative RAI or external beam radiotherapy may be more appropriate. Thus, radiologists play a critical role in making clinicians aware of the possible scenarios in which imaging with cross-sectional studies can help plan the management and the detection of extra-thyroidal extension on baseline imaging. The behavior and appearance of locally invasive thyroid cancer on CT are crucial for pre-operative evaluation, assessing recurrent tumors, and planning RAI or external beam radiotherapy.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

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Keywords:

AJCC; CT; MRI; thyroid carcinoma; thyroid nodule

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