- Open Access
Thyroid nodule ultrasound: technical advances and future horizons
© The Author(s) 2015
- Received: 17 December 2014
- Accepted: 4 February 2015
- Published: 5 March 2015
Thyroid nodules are extremely common and the vast majority are non-malignant; therefore the accurate discrimination of a benign lesion from malignancy is challenging. Ultrasound (US) characterisation has become the key component of many thyroid nodule guidelines and is primarily based on the detection of key features by high-resolution US. The thyroid imager should be familiar with the strengths and limitations of this modality and understand the technical factors that create and alter the imaging characteristics. Specific advances in high-resolution US are discussed with reference to individual features of thyroid cancer and benign disease. Potential roles for three-dimensional thyroid ultrasound and computer-aided diagnosis are also considered. The second section provides an overview of current evidence regarding thyroid ultrasound elastography (USE). USE is a novel imaging technique that quantifies tissue elasticity (stiffness) non-invasively and has potential utility because cancers cause tissue stiffening. In recent years, there has been much research into the value of thyroid USE for distinguishing benign and malignant nodules. Preliminary findings from multiple pilot studies and meta-analyses are promising and suggest that USE can augment the anatomical detail provided by high-resolution US. However, a definite role remains controversial and is discussed.
• High-resolution US characterises thyroid nodules by demonstration of specific anatomical features
• Technical advances heavily influence the key US features of thyroid nodules
• Most papillary carcinomas appear stiffer than benign thyroid nodules on US elastography (USE)
• Thyroid USE is controversial because of variation in the reported accuracies for malignancy
• Combined grey-scale US/USE may lower the FNAC rate in benign nodules
- Thyroid nodules
- Thyroid cancer
Ultrasound (US) examination of the neck is a commonly performed investigation and thyroid nodules are a highly prevalent finding. As the vast majority of nodules are non-malignant, the accurate discrimination of a benign from cancerous lesion is an important and challenging feature of thyroid US. Whilst single US features remain of limited accuracy, constellations of findings enable thyroid nodules to be accurately stratified on a ‘risk-of-malignancy’ basis and form the basis of several guidelines [1, 2]. Imaging features that confer a high positive predictive value and specificity for malignancy are valuable as they enable suspicious lesions to be identified and targeted for pathological analysis (typically fine-needle aspiration cytology, FNAC). The ubiquitous nature of thyroid nodules and the limitations of cytology mean that the confident identification of benign nodules is also important. US characteristics that carry a high negative predictive value for malignancy enable an evidence-based decision not to investigate further, allowing unnecessary FNAC and/or surgery to be avoided in a very large population. Many of these key thyroid nodule features are heavily dependent on recent advances in high-resolution ultrasound technology and are therefore altered and influenced by US machine settings. In an era of wider US use by different groups (e.g., endocrinologists, surgeons), the high-resolution features of thyroid disease—and the technical factors, which create and alter these valuable signs—must be familiar to the operator.
US elastography (USE) is a recent technological advance that measures tissue elasticity or stiffness properties objectively and has been available in recent years on many state-of-the-art clinical US machines. USE is classified as diagnostic ultrasound and is safe, non-invasive and requires no costly consumables. Importantly, USE can be performed in real-time alongside conventional sonography, providing objective stiffness data that can be used to influence clinical decisions during US examinations. The clinical potential of USE relies on the same principles as clinical palpation, namely that processes such as malignancy and fibrosis alter elasticity. Numerous clinical applications of USE are under investigation at different body sites. To date, over 100 preliminary studies on USE for thyroid nodules for malignancy have been published, with promising but controversial results, as will be discussed.
This article will focus on two aspects of thyroid ultrasound: first, technical advances in high-resolution US are discussed with relevance to specific features of thyroid cancer, benign disease and emerging developments. The second part of the article provides a concise overview of the current role of elastography and how elasticity imaging may supplement high-resolution ultrasound in the pursuit of accurate thyroid nodule assessment.
Contrast resolution settings are the primary factors that influence the assessment of nodule consistency, reflectivity and the detection of echogenic foci due to calcium or colloid. Whilst broader bandwidths allow improved beam penetration in the neck, the majority of advances in this aspect of thyroid ultrasound relate to how the echoes are received and processed rather than the pulse transmission. Signal processing (also known as speckle reduction) techniques are designed to interrogate lines of echoes obtained on each frame and improve the signal-to-noise ratio by pattern recognition . For example, an anechoic area containing background noise will be recognised as a cystic structure and the abrupt change in echoes around the margins of this target then recognised as the cyst/vessel wall (e.g., Precision ImagingTM, Toshiba). This process of removing unwanted noise leads to images that look sharper because of the improved signal-to-noise ratio and emphasise cystic vs. solid consistency. The dynamic range and grey-scale map are inherently linked but different aspects of high-resolution ultrasound. The dynamic range controls the range of grey (or the preferred colour tint) that is available to display echo intensity, whilst the grey-scale map allocates which parts of this spectrum are used to represent the echo signals received . Tissue harmonic imaging (THI)—an established technique for improving image contrast at other body sites—has recently become more relevant to high-frequency ultrasound. As the basis of this technique is to receive a signal from the second harmonic frequency of the probe’s transmit pulse (i.e., twice the probe transmit frequency), its use in superficial structures has been limited . However, the advent of wider bandwidths and more sophisticated receive technology means that THI is increasingly available to use with high-frequency probes (e.g., Hitachi High definition dynamic THI) resulting in further removal of clutter/noise and improved tissue contrast. Basic ultrasound settings (focal zones, time gain control, etc.) also affect image quality but are not covered in this article.
Smaller nodule detection:
Echogenic foci—colloid vs. calcium
The technological progress of B mode US enables the thyroid gland to be assessed in more anatomic detail than ever before, characterising lesions by a matrix of structural features. Building on these advances, the value of three-dimensional US in thyroid nodule assessment has recently been considered [19–21]. Initial studies have focussed on two aspects: the ability to more accurately assess the key B mode features (e.g., nodule margin) and the potential to uncover independent predictors of malignancy from 3D data sets. Whilst 3D US is not widely used in the neck at present, recent developments in this area suggest the potential to address persisting challenges of thyroid imaging.
In a prospective study of 91 thyroid nodules, the interobserver agreement for specific characteristics (e.g., shape, margin) was better for 3D than 2D US. Although intra-observer agreement remained suboptimal, there was significantly stronger agreement between users for suspicion of malignancy after off-line review of the static 3D images . National guidelines are increasingly based on standardised classification of malignant risk [1, 22] (as opposed to subjective assessment by experienced individuals); therefore reducing inter-observer variation is particularly relevant [1, 21, 22].
In a retrospective study of 71 thyroid nodules, 3D ultrasound data were analysed using multiplanar reformatted (MPR) images and a thin-slice volume-rendered technique . The MPR data found that poorly defined 3D nodule margins were associated with malignancy but also described two novel, independent 3D predictors of malignancy: a lobulated nodule shape in the C-plane (coronal) and altered central 3D vascularity. The smooth surface, thin-slice volume-rendering algorithm created images with higher contrast and reduced noise: a new layer of post processing to compare with existing 2D techniques. The shift in emphasis from real-time image interpretation to volume acquisition with subsequent processing and multiplanar viewing also offers potentially more detailed data analysis. A study of 20 thyroid nodules assessed 3D high-resolution ultrasound data with a computer-aided diagnostics (CAD) software programme . The authors found that CAD-detected specific 3D textural features could be identified and combined as an accurate discriminator of benign and malignant nodules, creating automated malignant risk stratification (‘Thyroid Malignancy Index’). Such an approach would represent a paradigm shift in practice for most thyroid imagers but the potential for accurate objective data to support an operator’s skill and experience is attractive.
Regarding contrast-enhanced ultrasound (CEUS), a small number of studies have documented the feasibility and diagnostic accuracy of assessing thyroid nodule enhancement following intravenous microbubble contrast, using low mechanical index (MI) settings [23, 24]. Recognisable quantitative patterns of perfusion have been identified to construct CEUS malignant risk stratification with 76.9 % sensitivity and 84.8 % specificity in a study of 42 patients . These findings suggest a potential role for CEUS as a diagnostic adjunct to B mode US but the technique is more invasive and time-consuming than standard ultrasound and, at present, the specific clinical utility is unclear.
Elasticity refers to the tendency of a tissue to undergo a reversible deformation and is quantified by Young’s modulus (E) in kiloPascals (kPa), which equals the ratio of an applied stress to the induced strain (displacement/original length) [25, 26]. USE technologies either estimate elasticity or a surrogate parameter such as strain from US signals acquired during a mild tissue deformation, which can be displayed two-dimensionally as elastograms. A range of proprietary USE technologies is available commercially, which can be divided into strain elastography (strain USE) and shear wave elastography (SWE) based on their underlying physics.
Accuracy of USE for malignancy
Presently about 80 studies of strain USE and 20 studies of SWE have been published for thyroid malignancy since 2005 [29–35]. Most are single-institutional series with heterogeneous designs, comprising around 100 nodules selected for FNAC or surgery because of suspicious or equivocal sonographic features, suspicious or malignant cytology or nodules within a compressive goitre. Most studies have also variably excluded nodules containing coarse macro-calcifications, substantial cystic areas or those within a diffuse thyroiditis as early evidence suggested that USE is suboptimal in these cases. Due to this selection bias, a much higher proportion of nodules in these studies is malignant (~25 %) than in an unselected population (~5 %) and most are papillary carcinomas (~90 %); thus published discriminatory performance data actually refer to this histological type [29–35].
Potential role of use in clinical practice
Diagnostic performances of conventional US and a combination of conventional US and USE for diagnosing thyroid malignancy
First author, year (citation)
n (% malignant)
Sebag, 2010 
Trimboli, 2012 
Ragazzoni, 2012 
Cappelli, 2012 
Moon, 2012 
Unluturk, 2012 
Veyrieres, 2012 
Shweel, 2013 
Russ, 2013 
Garino, 2014 
Liu, 2014 
Potential limitations of USE
Practical aspects and operator dependence of USE
USE is a dynamic technique with fluctuating elastographic appearances due to its intrinsic sensitivity to miniscule displacements that are continually occurring under physiological conditions. Various components of USE acquisition and interpretation are operator dependent including freehand compression for strain USE, selection of imaging planes through nodules, selection of representative elastograms, qualitative scoring of elastograms and placement of ROIs for (semi-)quantitative measurements . Strain USE using freehand compression is highly dependent on an optimal axial compression technique, which is hampered by competing non-axial motions (e.g., arterial pulsations and respiration) and the different mobilities of tissues bordering the thyroid (e.g., immobile trachea and mobile vessels). Carotid artery strain USE and SWE circumvent this source of operator dependence. Nevertheless, irrespective of the USE technology used, the operator influences the amount of resting pressure applied via a motionless transducer, termed precompression, which in turn can alter tissue stiffness . This phenomenon reflects the fact the Young’s modulus of biological tissues increases as strain is increased, termed strain hardening, although this effect is minimal for very small strains (<10 %). To mitigate this problem, USE should be performed with minimal pressure applied, which may be facilitated by maintaining an ample US gel layer between the transducer and skin.
Reproducibility of USE
Current and future directions of USE
According to recently published guidelines from the European Federation of Societies of Ultrasound in Medicine and Biology (EFSUMB): “elastography is an additional tool for thyroid lesion differentiation” and “based on expert opinion, elastography may be used to guide follow-up of lesions negative for malignancy at FNAC” . This cautious endorsement reflects the current controversies in thyroid USE evidence. Clearly further research is required including large multi-centre prospective trials of nodules with less pre-selection to evaluate different nodule characteristics, uncommon pathologies and reproducibility and ultimately determine how USE can be integrated with conventional US into emerging malignant risk classification systems (e.g., TIRADS). In this respect, clarifying precisely which types of nodule are unsuitable for thyroid USE will be critical to optimising its accuracy.
Although controversial, USE shows promise as an adjunct to conventional US for reliable identification of benignity in a select group of nodules on the initial US examination as well as those with non-diagnostic or indeterminate cytological results following FNAC. Even if these indications are validated in future studies, several issues will still need to be addressed before USE can be accepted widely in routine practice. USE technologies should be robust and simple to apply by the range of health care professionals who perform thyroid US routinely. The specific strengths and limitations of each USE technology including artefacts need to be catalogued systematically. While it is acknowledged that USE technologies are proprietary and their outputs may not be interchangeable, there should be greater standardisation of thyroid USE, for example by unifying nodule-grading systems and elastogram chromatic scales. Fortunately, USE technologies are continually improving including with respect to measurement precision and quality assurance, which should augment their diagnostic accuracies and reliabilities. Ideally, with advances in CAD software, a nodule’s grey scale and elastographic features could be analysed automatically and converted into a single estimate of its malignant risk. There are still some hurdles to overcome although, at the current pace of promising research and technological advances, USE may well become a valuable complementary technique for evaluating thyroid nodules in the near future.
Innovative advances in high-resolution ultrasound now enable detailed anatomical characterisation and accurate differentiation of benign from malignant disease. Ultrasound has become the core component of thyroid nodule guidelines, but it is important that the key technological aspects of the modality are understood and that challenges and limitations remain with the technique. The large evidence base for ultrasound elastography indicates that the assessment of nodule stiffness can improve the imaging evaluation of thyroid lesions and potentially avoids unnecessary FNAC/surgery for benign nodules, particularly if integrated with US classification. The potential for 3D and CEUS in thyroid nodule US has not yet been realised, but the emergence of these novel approaches is an illustration of the huge strides that have been made in the underlying ultrasound technology.
Dr Bhatia’s contribution was supported by a grant from the Research Grants Council of the Hong Kong Special Administrative Region, China (grant Chinese University of Hong Kong; project no. 460412). The authors wish to thank Dr Simon Elliott (Consultant Radiologist, Freeman Hospital, Newcastle, UK) for reviewing the manuscript and providing specific clinical images and Mr Kevin K.W. Leung (Senior Technician, Radiology Department, Prince of Wales Hospital, Hong Kong) for his assistance with illustrations. Both authors contributed equally to this article. During the writing of this article, technological advice and images were provided by ultrasound system specialists representing a number of UK vendors (Philips, Toshiba, Hitachi and Siemens). The selection of vendors was based on the clinical practice at the authors’ institutions only. No financial support was received from any of the manufacturers and the authors have no commercial interest to declare.
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