Abstract
OBJECTIVE:
To compare and evaluate diagnostic capabilities of preoperative ultrasonography (US) and magnetic resonance imaging (MRI) in the cervical lymph nodes of patients with papillary thyroid cancer.
METHODS:
A retrospective dataset involving 156 patients who had undergone thyroidectomy and preoperative US and MRI was assembled. Among these, 69 had cervical lymph node metastasis and 87 did not. At least four radiologists unilaterally and spontaneously investigated the US and MRI attributes of the cervical lymph nodes. The efficiency of diagnostic imaging for cervical lymph nodes, including their true-positive rate or sensitivity, true-negative rate or specificity, positive predictive value, negative predictive value, and predictive accuracy were analysed and assessed.
RESULTS:
In the assessment of cervical lymph node metastases of papillary thyroid cancer, the diagnostic sensitivity, specificity, positive predictive value, negative predictive value, and accuracy of diagnostic US vs. MRI were 58.0% vs. 79.7%, 69.0% vs. 83.9%, 59.7% vs. 79.7%, 67.4% vs. 83.9%, and 64.1% vs. 82.1%, respectively. The accuracy consistency of the two imaging modalities was 83.5%.
CONCLUSIONS:
MRI is more effective than US in diagnosing and assessing cervical lymph node metastases of papillary thyroid cancer.
Keywords
Introduction
Thyroid cancer is the most prevalent endocrine neoplasm and the twelfth most frequently occurring form of cancer [1]. The most common subtype is papillary thyroid carcinoma (PTC), which contributes to approximately 80% of confirmed cases [2–6] and accounts for at least 85% of all well-differentiated follicular thyroid cancers. It is classified as an indolent tumor with a 10-year mortality rate of nearly 93% [7]. Currently, patients with PTC are treated surgically and with radioactive iodine, which has an impressive medical prognosis [8, 9]. Since PTC accounts for approximately 85% of all thyroid cancers, it is the predisposing factor for the recurrence of cervical lymph node metastasis (CLNM) among patients with PTC [10–12].
The most difficult aspect of thyroid cancer imaging is its identification from benign thyroid disease. However, thyroid cancer is generally an endocrine malignant tumor in adolescents [13]. Radiological tests are critical for identifying CLNM in patients with thyroid cancer preoperatively and postoperatively, as their identification is vital for minimizing tumor recurrence and survival [14–17]. CLNM arises in 35% –80% of PTC cases.
Metastatic propagation of PTC to the neck does not appear to influence mortality or disease specificity; however, the probability of regional and local tumor reappearance and the need to proceed with surgery becomes increased. Nevertheless, the predictive value and optimum lymph node dissection of CLNM remain controversial. PTCs can potentially metastasize in the central compartment (level 6) and the horizontal plane of the lateral compartment (level 2–4). Therefore, preoperative evaluation of a cervical lymph node malignant growth is essential in choosing the surgical approach [18–21].
The current imaging technique used to measure lymph node metastases is ultrasound (US). In US, hyperechogenicity, calcification, cystic medial necrosis, circular form, poorly expressed peripheral edges, or mixed vascularity, and the exclusion of an echogenic hilum have been reported in PTC metastatic lymph nodes [22–29]. Additionally, the American Thyroid Association’s 2015 recommendations suggest that in cases where there is a clinical presumption of advanced disease, cross-sectional imaging or aerodigestive tract invasion should be performed when neck US visualization is ineffective. Consequently, cross-sectional imaging based on risk stratification can be used as a model method for “aggressive monitoring”, which the American Thyroid Association recommends for patients with a high probability of recurrence [30–32]. According to a previous study, US is a highly sensitive metastatic lymph node detection tool in the head and neck. Its sensitivity, precision, and accuracy have been confirmed when used in conjunction with fine-needle aspiration [33].
Magnetic resonance imaging (MRI) provides superior contrast for soft tissues and allows for evaluation in multiple planes. Additionally, MRI can provide more information about the lymph nodes and surrounding tissues, has been gradually applied to the diagnosis of tumor lymph node metastasis, and has good diagnostic efficacy. When PTC invades the trachea, larynx, large blood vessels, and cervical lymph nodes, US cannot make an accurate diagnosis, and MRI can more clearly assess the length and range of the trachea and the large blood vessels violated. Unlike computed tomography (CT), MRI involves no radiation; hence, it is increasingly used in clinical practice. Diffusion-weighted imaging (DWI) is an excellent method for thyroid disease diagnosis, and the apparent diffusion coefficient value is a non-invasive imaging procedure used to differentiate malignant from benign solitary thyroid nodules [34]. Exceptional anatomical details of tumors can be seen through MRI, particularly in the head and neck regions. However, it does not adequately determine tumor biology. Nevertheless, the recent development of functional MRI techniques offers a good understanding of both anatomical and functional knowledge on tumor vascularization and inner microarchitecture [35].
In the current knowledge, the cervical lymph node metastasis of papillary thyroid carcinoma is closely related to the survival rate, recurrence rate and mortality rate of patients. Therefore, the correct assessment of cervical lymph node metastasis of PTC before surgery is essential to formulate an appropriate treatment plan and prevent the recurrence of PTC. The aim of this study was to investigate the diagnostic accuracy of preoperative neck US and MRI in detecting CLNM of PTC, as well as its clinical characteristics.
Methods
Demographic study
Our institution’s ethics review committee approved the study and waived the requirement for written explicit authorization. From January 2017 to January 2021, the institutional database investigation identified 156 consecutive patients with PTC who underwent surgery and had undergone preoperative US and MRI of the thyroid at our hospital for PTC evaluation. The patients underwent both thyroid US and MRI within 2 weeks of their thyroidectomy. The complete US and MRI image data are stored in Dicom format in the PACS system. Additionally, all patients underwent a total or near-total thyroidectomy.
Ultrasonographic examination
Three radiologists with over 25 years of expertise in the neck and thyroid gland used a US system with a linear array ultrasonic transducer at a frequency range of 6–12 MHz (Philips iU22; Philips Healthcare, Eindhoven, the Netherlands). The patients were instructed to remain calm and lay on their back in a supine position. The size of the thyroid gland, nodules, echoes, lymph nodes, and microcalcifications were examined. The lymph node variance was explained in detail, and lymph node metastases were labeled.
Magnetic resonance imaging inspection
Each scan was performed using a Siemens MRI scanner (GE Signa HD 1.5 T; GE Health Maintenance System, Madison, WI, USA) equipped with an 8th channel receiver synergy of full-resolution head and neck phased-array coils. Contrast enhancement was performed using MRI, DWI, T1-weighted imaging (T1WI), and T2-weighted imaging (T2WI). For imaging acquisitions, the spin-echo based on the T1WI sequence (repetition time/time to echo = 500/14 ms) in transverse view and the swift spin-echo based on the T2WI sequence (repetition time/time to echo = 4000/90 ms) in frontal and axial views with and without fat suppression were used.
DWI was obtained in three orthogonal directions (X, Y, and Z) using short-TI inversion recovery-based fat-inhibited single-shot echo-planar imaging spin-echo sequences at three different b values (0, 50, and 500 s/mm2). Prior to image acquisition, the thyroid region was properly shimmed, allowing the delicate region of the neck to be viewed under a suitable standard of image quality. All of the participants underwent contrast enhancement T1WI (repetition time/time to echo = 500/14 ms) both with or without fat suppression, directly following an IV dose of 0.1 mmol/kg gadolinium diethylenetriamine pentaacetic acid-labeled dextran at a ratio of 1.5 ml/s (Pharma Schering AG, Magnevist, Germany). The following MRI parameters were used: 3 mm segment diameter, 1 mm intersection width, 40×28 cm2 field of view, 256×256 matrix, and number of excitations 1×4. The examination took 30 min to complete.
In this study, we examined the tumor location, size, shape, signal, edge, enhancement, lesion involvement, peripheral lymph node metastasis, and other signs on T1WI and T2WI. All images underwent double-blind evaluation by two radiologists with 25 years’ extensive clinical experience each. When the two physicians disagreed on the diagnosis, they reached consensus through discussion. Their findings were compared with the pathological results in a blinded manner. If the pathology indicated lymph node metastasis in the area, the largest short-path lymph node in the area was regarded as a metastatic lymph node. Conversely, if the pathology indicated no lymph node metastasis in the area, the largest short-path lymph node in this partition was regarded as a non-metastatic lymph node.
Cervical lymph node image analysis
The imaging criteria for US diagnosis of lymph node metastasis were as follows: presence of microcalcification, elongated lymph node with a length diameter greater than 20 mm, round or oval lymph node with a minimum inner diameter greater than 10 mm, no hilum or hilum migration and low echo, positive lymph nodes directly marked with microcalcification.
According to the United States Joint Committee on Cancer standards, the direct signs of PTC neck lymph node metastasis on preoperative US are (1) ratio of length/short diameter under 2; (2) abnormal echo characteristics of lymphoid portal (normal structure of lymphoid portal disappears or cortical eccentric lymphoid portal); (3) incomplete envelope; (4) irregular shape of lymph node; (5) nonuniform characteristics, such as calcified strong echo, and cystic low echo; and (6) rich internal blood flow. The criteria for determining malignant lymph nodes in the neck are: item 1 positive; or item 2 plus at least one of the other items positive.
The MRI lymph node metastasis criteria are (1) lymph nodes demonstrating cystic degeneration, or the minimum horizontal diameter of a single lymph node ≥15 mm; T1 and T2 phases demonstrate high signal and cystic lymph nodes with thin layer of sac wall; or T1WI demonstrated similar signal strength to the surrounding muscle, T2WI signal significantly increased compared to the muscle, and ≥3 clustered lymph nodes.
Statistical analyses
IBM SPSS Statistics for Windows version 26.0 (Armonk, New York, USA) was used to analyze the data. Sex and age were represented as the mean and standard deviation (±SD), mode, and median. For nominal and ordinal results, the numbers and percentages of the cases were used. Categorical variables were analyzed exclusively using the t-test and chi-square test, as appropriate. Multi-factor logistic regression analysis was used to establish a predictive model of cervical lymph node metastasis, and a receiver operating characteristic (ROC) curve was used to evaluate the diagnostic effectiveness of the predictive model. Statistical significance was considered at P < 0.05. Following the surgery, a specific comparison of the pathological findings with the US and MRI results was obtained. The diagnostic efficacy of the imaging modalities was determined, and the specificity, sensitivity, positive predictive value (PPV), and negative predictive value (NPV) were assessed based on the results.
Results
Comparison of papillary thyroid carcinoma clinical features
All the 156 PTC cases in this study underwent surgical resection and pathological confirmation, with 67 lesions on the right, 59 lesions on the left, and 30 lesions in the isthmus. The diameter of the lesions were 0.6–4.0 (2.75±0.86) cm. There were 69 cases with CLNM (Fig. 1) and 87 cases without CLNM. A comparison of clinical features between patients with and without CLNM is shown in Table 1. There were no discernible differences in age, sex, tumor diameter, node location, node position, internal echo pattern, and node border between the two groups (P > 0.05).

A 33-year-old male patient with papillary carcinoma of the left lobe of the thyroid with metastasis to cervical lymph nodes
Comparison of clinical characteristics of papillary thyroid carcinoma patients with and without cervical lymph node metastasis
PTC, papillary thyroid carcinoma.
Metastatic cervical lymph nodes have a higher resistance index, an unclear lymphoid portal display, uneven internal echo, internal microcalcifications, unclear boundaries, and a longitudinal/transverse diameter < 1.5. All differences are statistically significant (P < 0.05) (Table 2).
Comparison of ultrasound characteristics of metastatic with non-metastatic lymph nodes
Comparison of ultrasound characteristics of metastatic with non-metastatic lymph nodes
The lymph node ADC value, T1WI signal, lipid inhibitory T2WI signal, shape, edge, and intensity distribution is shown in Table 3. Single-factor analysis identified significant differences in the ADC value, T1WI signal, lipid inhibitory T2WI signal, shape, edge, degree of reinforcement, and other influencing factors between metastatic and non-metastatic lymph nodes (P < 0.05).
Comparison of MRI features of metastatic and non-metastatic lymph nodes in the neck
Comparison of MRI features of metastatic and non-metastatic lymph nodes in the neck
MRI, magnetic resonance imaging; T1WI, T1-weighted imaging; T2WI, T2-weighted imaging.
Two ultrasonographers and radiologists predicted the diagnostic effectiveness of PTC neck lymph node metastasis (see Fig. 3). Tables 4 and 5 indicate how the resistance index predicts PTC cervical lymph node metastasis. Youden’s index and the area under the curve are higher in lymph node metastases. Two ultrasonographers and two radiologists consistently confirmed the predictive value for cervical lymph node metastases in PTC.
Diagnostic efficacy of PTC in predicting cervical lymph node metastasis using various parameters
Diagnostic efficacy of PTC in predicting cervical lymph node metastasis using various parameters
ADC, Apparent Diffusion Coefficient; PTC, papillary thyroid carcinoma; RI, resistance index.
Comparison of diagnostic value of US and MRI in cervical lymph node metastasis in patients with PTC (%)
MRI, magnetic resonance imaging; PTC, papillary thyroid carcinoma; US, ultrasound.
The differentiation of the diagnostic value of US and MRI in cervical lymph node metastasis of PTC is shown in Table 5. In comparison to MRI for the evaluation of cervical lymph node metastasis, the US showed high sensitivity (79.7% vs 58.0%), high specificity (83.9% vs 69.0%), and high accuracy (82.1% vs 64.1%), with statistical significance (P < 0.05) (Fig. 1).
Ultrasound and magnetic resonance imaging diagnosis of cervical lymph node metastasis in papillary thyroid carcinoma
The differentiation of the US and MRI diagnostic values in CLNM of PTC is shown in Table 5. Compared to MRI for the evaluation of CLNM, US showed significantly higher sensitivity (79.7% vs. 58.0%), specificity (83.9% vs. 69.0%), and accuracy (82.1% vs. 64.1%) (P < 0.05). Figs. 1, 2

A 25-year-old female with papillary carcinoma of the right lobe of the thyroid gland with metastasis of cervical lymph nodes

ROC curve of PTC neck lymph node metastasis predicted by two ultrasonographers using resistance index and two radiologists using ADC values.
Thirty PTC cases were randomly selected, US and MRI were performed within 1 week, and diagnoses were made by two sonographers and two radiologists to determine the diagnostic differences between different physicians. Kappa consistency test results indicated that the consistency test Kappa coefficient between the two ultrasonographers was 0.619 (P = 0.001). The Kappa coefficient of the consistency test between the two doctors was 0.634 (P = 0.001). The consistency between the two was statistically significant.
Discussion
Metastases of cervical lymph nodes are established prognostic factors in patients with PTC [36]. The role of this study was to assess the diagnostic capabilities of preoperative US and MRI for cervical lymph node detection in patients with PTC. According to our study, when comparing diagnostic values, MRI has a higher sensitivity and NPV than US. Moreover, MRI has a higher specificity, positive predictive value, and accuracy rate in CLNM of PTC.
The identification of cervical lymph nodes before and after surgery is critical. Some studies have shown that earlier detection of lymph node metastases, leads to fewer recurrences and better prognosis in primary-prosecution patients, who have better chances of cancer survival. [14, 16]. In the diagnosis of neck node metastases, it is as effective, if not superior. In the area of low central comparison (Level 7) with anatomical regions (for example, areas deep in the bone and structures that are filled with air) that are poorly visualized by the US, such as the retropharyngeal and mediastinal areas. A computed tomography scan is often performed when patients show clinically apparent massive LNM. Moreover, retropharyngeal or mediastinal lymph node metastases can be detected using this technique. Some series of US estimates have been correlated with a substantial reduction in the ten-year DSS, from 91.2% to 79.8%, with the existence of sonographic malfunctions in the central compartment. Therefore, sonography is currently being suggested as a routine monitoring method in postoperative patients with thyroid cancer [37, 38].
Abboud et al. [39] have demonstrated the sensitivity (69%), specificity (71%), PPV (84%), and NPV (51%) of US. They have also sequentially demonstrated the sensitivity (85%), specificity (65%), PPV (78%), and NPV (75%) of US in the lateral neck. In a contemporaneous study, the true-positive rate or sensitivity, true-negative rate or specificity, PPV, NPV, and accuracy rates of US in CLNM of PTC were 58.0%, 69.0%, 59.7%, 67.4%, and 64.1%, respectively, whereas those of MRI were 79.7%, 83.9%, 79.7%, 83.9%, and 82.1%, respectively. Our study revealed the greater sensitivity (79.7%) and greater specificity (83.9%) of MRI, which are in contrast with the findings of previous studies. MRI showed higher sensitivity and negative predictive value than US in CLNM predictive value (79.7% vs. 58.0%, P = 0.001 and 83.9% vs. 67.4%, P = 0.008, respectively).
Single-factor analysis demonstrated that CLNM on US had a higher resistance index, unclear lymphatic portal display, uneven internal echo, internal microcalcifications, unclear boundaries, and longitudinal/transverse diameter < 1.5. The differences between the two groups were statistically significant (P < 0.05).
Regarding MRI examination, the differences in ADC value, T1WI signal, lipid inhibition T2WI signal, shape, edge, and intensity between the two groups were statistically significant (P < 0.05). ROC curve analysis demonstrated that the resistance index predicted PTC neck lymph node metastasis, as well as an unclear lymphatic portal display, uneven internal echo, internal microcalcification, unclear boundary, and longitudinal/transverse diameter < 1.5. All these differences were statistically significant (P < 0.05). The diagnostic efficacy of lymph node metastasis was the greatest, with a sensitivity of 73.9% and a specificity of 80.1%, an area of 0.849 under the ROC curve and a Youden’s index of 53.2.
This study had some limitations. First, this was a retrospective study, which introduced a case selection bias that may have influenced the findings. Second, our research was performed in a single center rather than as part of a multicenter experiment. Third, in some cases of PTC with ambiguous borders, the tumor had been difficult to differentiate. These instances have not been included in this report. The majority of these cases were PTC with CLNM, introducing a certain amount of sampling bias into the analysis.
Additionally, contrast-enhanced MRI provides high-resolution findings for soft tissue, involves no exposure to radiation, and permits the simultaneous recording of several imaging parameters. However, there is currently a lack of relevant studies on the results of using MRI on cancer of the lymph nodes to determine whether it is better than US in terms of diagnosing the location.
In conclusion, our research summarized the diagnostic efficiency of US and MRI in preoperative CLNM of patients with PTC. Our research focused on extensive clinical, pathological, and radiological data collected from the Chinese population. Nevertheless, additional studies are needed to gain a better understanding of the use of US and MRI in detecting CLNM in patients with PTC. The current imaging methods for CLMN of PTC include US, CT, MRI, and nuclide imaging. US, as the preferred imaging examination method for PTC diagnosis, can provide higher spatial resolution, but it is greatly influenced by the examiner. MRI is currently the common imaging examination method for CLMN diagnosis of PTC. MRI anatomical images are more intuitive than US. Examiners suggest that it has less impact and is more convenient for accurate positioning before surgery; it can display areas that cannot be reached by US, such as the mediastinum and parapharyngeal; it has good soft tissue resolution, can accurately stage the lesion before surgery, and clarify the surrounding invasion of the tumor. MRI has more advantages than US.
Footnotes
Acknowledgments
We specially thank Xian Wang, Zhang Guoliang, Nida Fatima Moazzam, Ahmad Daniyal Shahid for their important contribution.
