Gray-Scale Ultrasonography Combined with Elastography Imaging for the Evaluation of Papillary Thyroid Microcarcinoma: As a Prognostic Clinicopathology Factor

Abstract

Ultrasonography (US) is the preferred imaging modality for papillary thyroid microcarcinoma (PTMC). The aim of this study was to evaluate the importance of gray-scale ultrasound combined with elastography to predict extrathyroidal extension and cervical lymph node (LN) metastasis in patients with PTMC. We retrospectively evaluated gray-scale ultrasonic and elastographic results from 119 consecutive cases of PTMC with 138 nodules and correlated the histopathological findings. The results indicated that pathological extrathyroidal extension was significantly associated with T staging on US, extrathyroidal extension on US, bilaterality on US, boundary, strain ratio and hard malignancy as measured with the Rago score. Central LN metastasis on pathology was significantly associated with central LN metastasis on US, lateral LN metastasis on US, multifocality on US and bilaterality on US. Lateral LN metastasis on US was significantly associated with lateral LN metastasis on pathology. On multivariate analysis, T staging on US, extrathyroidal extension on US and hard malignancy as measured with the Rago score were significantly associated with pathological extrathyroidal extension. Lateral LN metastasis on US and bilaterality on US were independent factors in predicting central LN metastasis on pathology. Lateral LN metastasis on US was the predictive factor for lateral LN metastasis on pathology. US should be helpful in the diagnosis of PTMC and in the evaluation of possible PTMC recurrence on US in routine clinical practice.

Introduction

Thyroid microcarcinomas, almost exclusively papillary thyroid cancers, are defined as thyroid cancers measuring ≤1 cm in maximum dimension (Hedinger 1988). Thyroid cancer has become the most common tumor in women, and its global morbidity is increasing by 4% annually (Nix et al. 2005). In particular, the incidence of papillary thyroid microcarcinoma (PTMC) is rapidly increasing (Cramer et al., 2010, Hughes et al., 2011, Jung et al., 2011). This increase in incidence is due largely to improved detection by imaging modalities such as thyroid ultrasound, emission computed tomography, magnetic resonance imaging and ¹⁸F-fluorodeoxyglucose positron emission tomography scanning of small nodules not detected by clinical palpation (Bernet 2010).

Papillary thyroid microcarcinoma was introduced as a subtype of papillary thyroid cancer by the World Health Organization in 2004 and accounts for 30% to 40% of all papillary thyroid cancers (DeLellis et al., 2004, Mazeh and Chen, 2011). Many PTMCs are rarely detected during physical examinations by clinicians because PTMCs usually have no clinical symptoms and follow an indolent course; 76% of the nodules confirmed by pathological examination were missed, even by experienced clinicians, and nodules >2.0 cm could be missed in a short fat neck (Yu et al. 2012). Therefore, the diagnosis of PTMC depends mostly on imaging technologies and cytological examinations.

Ultrasonography-guided fine-needle aspiration biopsy (US-FNA) has been widely accepted as providing the most specific information on the cellular composition of a nodule and is the most crucial step in the pre-operative assessment of thyroid nodules. However, US-FNA is not indicated routinely for thyroid nodules <1 cm according to the guidelines issued by the American Thyroid Association (Cooper et al. 2009). Because of the wide availability of high-frequency ultrasonic transducers and the improvement of spatial resolution, ultrasonography (US) is now the preferred imaging method for the screening of thyroid diseases, especially PTMC. In addition, ultrasonography is one of the most important methodologies for post-operative monitoring of patients with PTMC. Recently, it was reported that treatment of PTMCs should differ with the tumor’s biological behavior and that consecutive follow-up with US every 6 or 12 mo is feasible for the lowest-risk PTMCs (Sugitani et al. 2010). A firm and hard thyroid nodule on palpation is known to be associated with an increased risk for thyroid malignancy (Gharib et al. 2010). Clinical palpation is often the method used to determine the relevant stiffness of lesions, but it is more subjective among clinicians with varied experience, and deep small lesions are not easily accessible. Ultrasound elastography (UE) is a technology that determines tissue stiffness by measuring the degree of distortion under the application of an external force. In comparison with clinical palpation, UE is more objective as a tool to evaluate tissue hardness and is a very promising imaging method in differentiating malignant from benign thyroid nodules (Asteria et al., 2008, Dighe et al., 2008, Friedrich-Rust et al., 2010, Friedrich-Rust et al., 2012, Gu et al., 2012, Hong et al., 2009, Rago et al., 2010). However, there are few studies on the correlation between the combination of gray-scale ultrasound with UE findings and histopathological characteristics. In this study, we reviewed the ultrasonic features of PTMCs along with their histopathological characteristics, as a prognostic factor in patients with PTMC, to survey the pre-operative clinical implications of gray-scale ultrasound combined with UE.