Sage Journals: Discover world-class research

Abstract

Musculoskeletal ultrasound is a powerful tool not only for evaluating joint and related structures but also for assessing disease activity. Ultrasound in rheumatology has rapidly evolved and been incorporated into routine clinical practice over the past decade. Moreover, technological development of equipment has made it more accessible for rheumatologists. We present a review of advances in ultrasound in rheumatology, focusing on major chronological developments.

Keywords

evolution musculoskeletal ultrasound rheumatology ultrasonography

Introduction

Musculoskeletal ultrasound has been considered a diagnostic tool for a variety of rheumatologic diseases for more than 30 years. However, its use has increased dramatically over the past decade, largely as a result of technological developments and falling costs. The former has allowed the production of high-quality and more easily interpretable images and the latter has made machines more affordable and accessible to the clinician. These improvements have been influential in driving the interests of the rheumatologist, particularly with respect to inflammatory arthritis and the early identification of inflammation and structural damage. In this review, we explore the major chronological advances of musculoskeletal ultrasound and highlight potential future directions in rheumatology.

Brief history: from the discovery of ultrasound to recent high-end machines

In the history of the development of ultrasonography, one of the most important contributions is certainly from Lazzaro Spallanzani, an Italian biologist, who observed, in the eighteenth century, that blindfolded bats were able to avoid thin wires stretched across a dark room. This ability was prevented when wax was placed in the bats’ ears, and not when they were blindfolded, so that he concluded that their capacity to ‘see’ was strictly dependent on their ears. However, he was unaware that the bats used ultrasound to avoid the wires.

In 1843, the Austrian astronomer, physicist and mathematician Christian Doppler described the apparent change in frequency and wavelength of a mechanical wave perceived by an observer when the source of sound moved in relation to the object. This effect, later coined the ‘Doppler effect’, is the principle of the technique for estimating synovial blood flow in rheumatology ultrasound assessment. However, it was not until 1880, through the discovery of the piezo-electric effect of crystals by the French physicist Curie brothers, that the first relevant step to the development of modern ultrasound probes was made. The first realization of the use of ultrasound began in the military sector with the development of sound navigation and ranging (SONAR) systems for submarines during the First World War. Subsequently, its first development as a medical diagnostic tool is attributed to the Austrian neurologist Karl Dussik who in 1942 described his attempt to identify the cerebral ventricles and brain tumours using ultrasound beams directed through the skull [Dussik, 1942]. Shortly afterwards, Scottish obstetrician Ian Donald and Glasgow engineer Tom Brown developed the first A-mode a unidimensional ultrasound scanner and investigated abdominal masses [Donald et al. 1958].

The first clinically relevant musculoskeletal ultrasound study was published in 1972, in the British Journal of Radiology, by American radiologists Daniel McDonald and George Leopold [McDonald and Leopold, 1972]. They described the use of a contact B-mode, real-time scanner to differentiate Baker’s cysts from thrombophlebitis. Six years later, in 1978, using greyscale ultrasound, a Canadian radiologist Peter Cooperberg published the first demonstration of synovitis in patients with rheumatoid arthritis [Cooperberg et al. 1978]. Since then, ultrasound has gained an increasing interest from musculoskeletal practitioners as it allowed the potential to directly visualize the primary site of pathology and a better understanding of joint pathophysiology. In recent years, increasing and changing demands made by the clinicians have influenced the direction of ultrasound development by manufacturers.

Nowadays, the cost of ultrasound equipment is quite variable. Equipment providing the highest image quality and the larger range of software add-ons is more expensive. However, the less expensive and less sophisticated units have facilitated the diffusion and accessibility of ultrasound training to a larger number of rheumatologists. Touch and flat screens of the latest-generation machines mean the traditional keyboard is no longer required which is relevant to the miniaturization of the machine; these screens also allow an easier and quicker transition between different aspects of the ultrasound examination. The feasibility to transfer small ultrasound equipment easily between different rooms of the same institution is also an advance. In addition, smaller and higher frequency transducers have facilitated the improved visualization of superficial and tiny anatomical structures such as ligaments, tendons and smaller joints. Despite the availability of different types of transducers, linear probes are best able to assess all indications in musculoskeletal ultrasound. The development of the ‘hockey stick’ probes, so called because of their shape, has surely facilitated the evaluation of joints that are difficult to reach due to their anatomy and size. Moreover, the use of small and handy probes has enabled the operator to obtain better angulation and control, thus reducing the risk of creating image artefacts.

From the first demonstration of synovial thickening to the end of the twentieth century

After the first greyscale demonstration of synovial thickening pre and post treatment with yttrium-90 injection in rheumatoid arthritis of the knee using 5 MHz of ultrasound frequency in 1978 [Cooperberg et al. 1978], interest in imaging smaller joints and periarticular structures has grown amongst clinicians. Three years later, in 1981, the first report on the utility of ultrasound to successfully guide a joint aspiration in a patient with advanced rheumatoid arthritis with bilateral shoulder dislocation due to septic arthritis was published [Gompels and Darlington, 1981]. In 1988, the first ultrasound description of rheumatoid nodule and tenosynovitis in patients with rheumatoid arthritis was detailed [De Flaviis et al. 1988].

On the basis of these publications, in the late 1980s, a small group of enthusiastic European rheumatologists started to practice musculoskeletal ultrasound and published pioneering articles on the use of the technique in rheumatology clinics [Koski, 1989; Koski et al. 1989; Iagnocco et al. 1992]. Koski and colleagues demonstrated intra-articular effusion or synovitis in clinically and radiologically apparently normal hip joints of patients with active rheumatoid arthritis [Koski, 1989] and lagnocco and colleagues found that cartilage thickness measured with a 5 MHz linear probe was diminished both in rheumatoid arthritis and in osteoarthritis knees compared with normal joints [Iagnocco et al. 1992]. In these studies, only greyscale ultrasonography in which images are produced in a black and white format was used.

In 1994, the first paper demonstrating the ability of power Doppler to visualize abnormal joint vascularity was published and this subsequently led the way for modern rheumatology ultrasound practice [Newman et al. 1994]. In the following year, the first use of colour Doppler ultrasound to diagnose temporal arteritis was published by pioneering rheumatologists in this field [Schmidt et al. 1995]. Since then, ultrasound for vasculitis of both small and large vessels started to attract rheumatologists’ interest [Hau et al. 1999].

Towards the end of 2000, the recognition of the potential of ultrasound as a method to confirm the primary diagnosis and to assess therapeutic response in many rheumatologic diseases spurred the interest of rheumatologists to learn the technique themselves in order to improve their clinical practice. To support the learning needs of rheumatologists a ‘EULAR [European League Against Rheumatism] Working Group for Musculoskeletal Ultrasound’ was formed by rheumatology experts in 1998. Thus, the first EULAR ultrasound training course entitled ‘An introduction to musculoskeletal ultrasound’ was held in the Netherlands in 1998 [Wakefield et al. 1999].

The twenty-first century has opened a new era for ultrasound in rheumatology

As more rheumatologists have begun to learn ultrasound, structured training programmes have needed to be developed and researches have progressed towards more specific focuses in the twenty-first century.

Developments in education and training

To accommodate increasing numbers of learners and their requirements, in 2006, EULAR started to divide the EULAR ultrasound course into different levels by launching the first advanced ultrasound course in Denmark for experienced rheumatologists. In the following year, the members who organized the 14th EULAR ultrasound courses in 2007 developed the educational guidelines for the contents and conduct of future EULAR ultrasound courses, which proposed an educational model with three levels of basic, intermediate and advanced [Naredo et al. 2008]. The educational model has been successfully applied to the EULAR ultrasound course. As education progresses towards more structured outcomes, the need for competency assessment reflecting practical skills, knowledge and personal qualities has increased. Currently, an assessment and quality assurance process for trainees has been suggested for development by the EULAR Standing Committee for Education and Training; however, there is still a lack of consensus regarding how to determine whether trainees have enough theoretical knowledge and practical skills.

As in Europe, the use of musculoskeletal ultrasound by rheumatologists has also grown steadily in America. An ultrasound workshop has run at the American College of Rheumatology (ACR) since 1999, but it was not until 2005 when a focus group known as USSONAR (Ultrasound Society of North American Rheumatologists) was formed to foster training and research in ultrasound by rheumatologists [Samuels et al. 2010]. The ACR first started to hold two standalone training conferences in 2010 [Kaeley, 2010].

Developments in standardization

As ultrasound started to increase in popularity, it became apparent that there was a lack of standardization for the use of ultrasound in rheumatology. Consequently, in 2001, the first guidelines for musculoskeletal ultrasound in rheumatology were published by the EULAR Working Group for Musculoskeletal Ultrasound [Backhaus et al. 2001]. However, there remained a lack of consensus regarding standardized ultrasound definitions of pathology as well as scanning methodology. This prompted a group of interested international rheumatology ultrasonographers to form Outcome Measures in Rheumatology (OMERACT), an ultrasound task force. This group developed the first consensus set of definitions for ultrasound pathologies based on the OMERACT filter [Boers et al. 1998] in the inflammatory joint diseases in 2005 [Wakefield et al. 2005], which has provided an initial framework for subsequent studies. This task force has been working towards the development of a standardized ultrasound scoring system for synovitis and an ultrasound joint count according to the OMERACT filter [D’Agostino et al. 2009]. Currently, this group is moving towards spondyloarthropathies, osteoarthritis, pediatrics and crystal arthropathies.

Advances in rheumatologic diseases and their assessment

Rheumatoid arthritis

Rheumatoid arthritis has been focused primarily in rheumatology ultrasound in terms of early detection, grading and treatment of synovitis. Since the first greyscale ultrasound demonstration synovitis of the knee joint, many studies have confirmed the superiority of ultrasound over clinical examination in the detection of synovitis, synovial hypertrophy, effusion and related pathologies [Grassi et al. 1993; Kane et al. 2003; Backhaus, 2009]. This is largely due to the fact that ultrasound can visualize minimally thickened synovium which is not yet perceivable by clinical palpation [Grassi, 2003; Kane et al. 2003; Karim et al. 2004]. Naturally, the next focus moved to how to assess synovitis using power or colour Doppler.

Doppler ultrasound is a technique that has been used widely in other medical ultrasonography areas such as cardiology, obstetrics and gastroenterology to evaluate blood flow of vessels. In rheumatology, especially in arthritis evaluation, the power Doppler technique is unique in terms of measurement of blood flow at a level of microvascularity (Figure 1). Power Doppler has been preferred to colour Doppler for the assessment of disease activity due to its technical advantages, including lack of aliasing, less angle dependency and greater sensitivity for low velocity blood flow. Thus, interest in whether power Doppler ultrasound is able to represent real inflammation within joints started in the early 2000s. Initial work has shown good correlation between Doppler hyperemia and histologically detected pannus [Schmidt et al. 2000] and rate of early synovial enhancement in magnetic resonance imaging (MRI) [Szkudlarek et al. 2001]. These results have been supported by other investigators who evaluated the relationship between Doppler hyperemia and histopatholgic vascularity or MRI later on, confirming good correlation [Szkudlarek et al. 2001; Walther et al. 2001, 2002; Terslev et al. 2003b; Wiell et al. 2007; Bruyn et al. 2009, 2010].

Figure 1.

Greyscale ultrasound can be used to demonstrate synovitis. In this image of a metacarpophalangeal joint of a patient with rheumatoid arthritis, the joint capsule is markedly distended outwards (arrows) due to underlying synovial effusion and hypertrophy. The presence of power Doppler demonstrates the increased microvascular flow of the joint, which is suggestive of active inflammation. M, metacarpal bone; P, proximal phalanx.

With new definitions of primary pathologies, scoring systems were the next to be developed for both greyscale and colour Doppler. Different systems for both greyscale synovial hypertrophy and Doppler hyperemia have been proposed by different groups [Stone et al. 2001; Szkudlarek et al. 2003b]. The majority of these are semiquantitative using a 0–3 scale of mild, moderate and severe [Szkudlarek et al. 2003a]. These semiquantitative scorings are relatively easy to apply in clinical practice but the amount of difference between grades is not equal. Alternatively, scoring region of interest with continuous variables to quantify the degree of inflammation has been suggested. With Doppler in particular, more quantitative measures have been tested, such as the calculation of the resistive index or pixel counting in the region of interest [Terslev et al. 2003a, 2008; Fukae et al. 2010]. The downside of these measures, however, is their feasibility and they are probably only applicable to clinical trials.

A number of studies have started to investigate the role of ultrasound in patients with inflammatory arthritis with particular focus on bone erosion in rheumatoid arthritis. An example of this is a study by Wakefield, which reported the superior sensitivity of ultrasound over radiography for the detection of bone erosions (Figure 2) in patients with rheumatoid arthritis [Wakefield et al. 2000]. In this study ultrasound detected 6.5- and 3.4-fold more erosions in 7.5- and 2.7-fold more patients than radiography in patients with early and late rheumatoid arthritis respectively. Following this study, several other reports have confirmed that ultrasound erosions show good concordance with MRI and computed tomography (CT) [Lopez-Ben et al. 2004; Dohn et al. 2006]. Although the OMERACT ultrasound group established an ultrasound definition of bone erosion, it does not include a size limit. As machine resolution continues to improve, distinguishing between small erosions and physiological bone abnormalities becomes even more important [Finzel et al. 2011]. Moreover, although scoring systems based on size [Wakefield et al. 2000] and semiquantitative scores [Reynolds et al. 2009] have been suggested, no consensus has been made on a standardized scoring system.

Figure 2.

Transverse view through a second metacarpal head of a patient with rheumatoid arthritis. A well defined erosion can be seen which was confirmed in a longitudinal plane. M, metacarpal bone.

A relatively new area of discussion in rheumatoid arthritis has been which joints to assess by ultrasound in clinical practice and this has led to the concept of an ultrasound joint count. The ACR 66/68 clinical joint count for swelling and tenderness and the reduced 28-joint count have been widely used in rheumatology daily practice and clinical trials. However, these measures are not without limitations. Whether ultrasound can offer a more accurate and comprehensive method of evaluating joint inflammation and a more sensitive method of assessing response to therapies has been questioned. Thus, investigators have started to assess the value of assessing a number of different joint combinations. In 2005, the first ultrasound 28-joint count and index for effusion, synovitis and power Doppler signal showed good correlation with clinical variables [Naredo et al. 2005]. Subsequently, other ultrasound joint scoring systems using a 12-joint [Naredo et al. 2008], 7-joint [Backhaus et al. 2009], 44-joint [Scire et al. 2009], 38-joint [Filer et al. 2011] and 78-joint score [Hammer and Kvien, 2011] have been proposed and all demonstrated sensitivity to change. They differ from each other in terms of joints, tendons and bursae included. Acknowledging the need to reach agreement between the different scoring systems, the OMERACT/EULAR group has been working towards a common consensus on scoring systems for synovitis which are currently being tested in longitudinal studies. Ultimately however, the added value of using ultrasound in standard clinical care needs to be determined.

Until recently, compared with rheumatoid arthritis, less attention has been directed towards the role of ultrasound in the assessment and evaluation of other types of arthritis, including spondyloarthropathies, crystal-associated arthritis and osteoarthritis.

Spondyloarthropathies

The main use of ultrasound in spondyloarthropathies has been for the detection of enthesitis of the Achilles tendon and plantar fascia. In the first large study of 164 patients with spondyloarthropathy and 64 controls, a high prevalence of peripheral entheseal involvement was revealed by greyscale ultrasound combined with power Doppler in patients with spondyloarthropathy. In this study, ultrasound clearly demonstrated its ability to be used to assess spondyloarthropathy activity [D’Agostino et al. 2003]. Other studies have focused on the ability of ultrasound to differentiate between subtypes of spondyloarthropathy [D’Agostino et al. 2003] and to distinguish spondyloarthropathies from rheumatoid arthritis [Falsetti et al. 2003]. As ultrasound demonstrated its usefulness in the evaluation of enthesial pathology, attempts have also been made to quantify enthesial abnormalities with ultrasound using different scoring systems such as the Sonographic Enthesitis Index [Alcalde et al. 2007] and the Madrid Sonographic Enthesis Index [De Miguel et al. 2009]. However, well reported methodology is lacking and consensus on elementary lesions and standardization of ultrasound examination is needed for future application in the evaluation of enthesitis [Gandjbakhch et al. 2011].

Osteoarthritis

The first ultrasonographic report on cartilage evaluation in rheumatology was published in 1992, in which a decrease of cartilage thickness in patients with osteoarthritis was reported. Ultrasound for osteoarthritis has gained less attention compared with rheumatoid arthritis, particularly because there are fewer treatment options for osteoarthritis. Recently the role of ultrasound to assess articular hyaline cartilage in osteoarthritis research has increased. Early and late changes of osteoarthritic cartilage, including loss of transparency and sharpness, which cannot be determined using conventional radiography, and decrease in thickness have been demonstrated since the mid 2000s [Borman et al. 2006; Meenagh et al. 2007; Filippucci et al. 2009; Kunkel, 2010; De Miguel et al. 2011; Ruta et al. 2011]. Moreover, a study reported that reduced cartilage shown by ultrasound may differentiate between early symptomatic osteoarthritis and early rheumatoid arthritis, suggesting measuring joint cartilage by ultrasound may be a promising alternative to conventional imaging [Moller et al. 2009]. In osteoarthritic joints, evidence suggests that synovitis is likely to occur, similar to rheumatoid arthritis, with an episodic aggravation that contributes to cartilage deterioration [Attur et al. 2010]. The use of ultrasound has allowed inflammatory changes to be examined, leading to new research about whether synovitis determined using ultrasound may play an active role in perpetuation of the disease. In the first attempt to examine the relationship between ultrasound detectable changes and symptoms in hand osteoarthritis, painful joints were more likely to have ultrasound-detected greyscale and power Doppler synovitis [Keen et al. 2008]. Furthermore, a recent study demonstrated that joints with power Doppler signal had higher radiographic scores and lower cartilage thickness [Mancarella et al. 2010].

Crystal arthropathies: gout and pseudogout

Ultrasound studies began focusing on gout and pseudogout in the mid 2000s and showed different crystal deposit patterns within cartilage [Grassi et al. 2006; Thiele and Schlesinger, 2007]. At present, demonstrating the presence of monosodium urate (MSU) and calcium pyrophosphate dehydrate (CPPD) crystals in aspirated joint fluid or tophus is considered the gold standard for diagnosis [McCarty and Hollander, 1961]. However, this may change with the pictorial ability of high-resolution ultrasound. MSU and CPPD crystals can be detected with ultrasound when a conventional radiograph is normal [Frediani et al. 2005]. Once MSU or CPPD crystals are deposited in the articular cartilage, the sparkling nature of the deposited crystals makes them easier to be visualized, even for very small aggregates. The existence of a hyperechoic band over the anechoic hyaline cartilage surface, described as a double contour sign in gout, is a differentiating feature of the intracartilage deposit pattern of CPPD crystals and shows good sensitivity for the diagnosis of gout and CPPD disease [Grassi et al. 2006; Thiele and Schlesinger, 2007, 2010; De Miguel et al. 2011]. Currently, as a readily available tool, ultrasound may be helpful for the diagnosis of gout and pseudogout. More comprehensive data are needed to confirm its use for the early diagnosis and prevention of structural damage in patients with gout and pseudogout.

Vasculitis

The first major paper demonstrating the value of ultrasound in large vessel vasculitis was in 1995 [Schmidt et al. 1995]. This study reported a hypoechoic halo in temporal arteritis which disappeared 10–14 days after steroid treatment and suggested that ultrasound had the potential of replacing a temporal artery biopsy [Schmidt et al. 1997]. This work has subsequently been supported by another study [Nesher et al. 2002], although large-scale multicenter studies have not been undertaken. To this end, larger-scale studies are underway to establish the true added value of ultrasound to the diagnosis of temporal arteritis and whether it can reliably replace the need for a biopsy. The scope of vasculitic ultrasound research has expanded to small vessels and other large-vessel arteritis. Vascular ultrasound has shown superiority over MRI and angiography in the visualization of carotid arterial wall affected by Wegener’s granulomatosis [Schmidt et al. 2001] and is able to discriminate between different patterns of finger artery involvement in Wegener’s granulomatosis, rheumatoid vasculitis and systemic sclerosis [Schmidt et al. 2006, 2008].

Salivary glands/Sjögren syndrome

Conventionally, minor salivary gland biopsy and sialography have been considered the cornerstones of the diagnosis of Sjögren syndrome. This concept has changed in the 2000s by an increasing number of studies assessing patients with Sjögren syndrome using ultrasound. Colour Doppler of patients with primary Sjögren syndrome has shown an increase in colour signal within the parenchyma and the resistive index or pulsatility index at the facial artery may reflect the vascular changes occurring in the salivary glands [Martinoli et al. 1994]. The structural changes, especially the parenchymal inhomogeneity demonstrated by ultrasound, were reported to have similar sensitivity to MRI [Makula et al. 2000]. In addition, the semiquantitative ultrasound score of the major salivary glands showed high diagnostic accuracy [Hocevar et al. 2005; Milic et al. 2009]. However, ultrasonographic classification criteria for primary Sjögren syndrome are still lacking and this has resulted in variable ultrasonographic diagnostic sensitivities of 43–93% and specificities of 64–100% for Sjögren syndrome [De Vita et al. 1992; Yonetsu et al. 2002; Milic et al. 2009]. Nevertheless, as ultrasound can visualize features of glandular involvement of primary Sjögren syndrome, it may replace invasive diagnostic procedures in patients suspected of having the syndrome [Salaffi et al. 2008].

Ultrasound-guided interventions

One of the major advantages with ultrasound is the improvements in the diagnostic and therapeutic musculoskeletal interventions in rheumatology clinical practice. By demonstrating structures within and around joints, ultrasound has helped to increase the accuracy of injections. Although some studies could not demonstrate a better clinical outcome between blind and ultrasound-guided injection [Cunnington et al. 2010], real-time visualization of the needle tip and injected steroid crystals has made it possible to accurately inject steroids into the swollen tendon sheath, carpal tunnel and joint cavity, avoiding nearby neurovascular structures. Many studies have demonstrated the superiority of ultrasound-guided injection compared with blind injection guided by external anatomic landmarks in various synovial joints in terms of accuracy, safety and better clinical outcome [Koski, 2000; Sibbitt et al. 2009; Gilliland et al. 2011].

New research areas in the twenty-first century in rheumatology ultrasound

New developments in hardware and software technology have resulted in new applications, including contrast-enhanced ultrasound, three-dimensional (3D) and four-dimensional (4D) ultrasound, elastography and fusion imaging in rheumatology.

Contrast-enhanced ultrasound

The effect of microbubbles in increasing the backscattering of blood in Doppler ultrasound was first described in the aorta during cardiac catheterization [Gramiak and Shah, 1968]. This led to its application in many different disciplines, including liver, spleen and kidneys. Several types of microbubbles have been developed [Quaia, 2007]. In rheumatology, application of contrast-enhanced greyscale ultrasound began in the 2000s to maximize the spatial resolution using microbubbles. The use of ‘first-generation’ microbubble ultrasound contrast agent with power or colour Doppler resulted in improved detection of vascularity in the joints of patients with rheumatoid arthritis [Carotti et al. 2002; Klauser et al. 2002]. The new ‘second-generation’ ultrasound contrast agents have made microbubbles more stable and durable and therefore enabled continuous scanning to be performed over a specific period of time. Contrast-enhanced ultrasound has provided the differentiation of active synovitis from inactive intra-articular thickening, showing an ability to improve assessment of vascularized synovial proliferation in rheumatoid arthritis affected joints [Klauser et al. 2005]. The rate of uptake of microbubbles can be measured by software packages produced by ultrasound manufacturers, which can provide quantitative data about the degree of vascularity. Furthermore, an exciting new potential role of microbubbles is the delivery of labelled microbubbles to specific anatomical sites either for further imaging studies or for the delivery of targeted drugs [Deshpande et al. 2011]. However, its use in rheumatology clinical practice has been limited by invasiveness, additional cost and time spent on the procedure, as well as the potential adverse reactions of microbubbles such as dyspnea, chest pain, hypotension or hypertension, nausea and vomiting. At present, quantification of contrast enhancement and standardization of measurements and interpretation need further investigation. However, the technique seems to have opened up new horizons in the sensitive assessment of synovitis, leading to evolution of contrast ultrasound from vascular imaging to imaging of perfused tissue at the microvascular level.

Three- and four-dimensional ultrasonography

The 3D technology and real-time update of the 3D volume, also known as 4D ultrasound, have been used mainly for fetal assessment and cardiology, but more recently they have been applied to rheumatology. The 3D ultrasound has been considered an interesting prospect for the assessment of musculoskeletal disease in terms of improving operator reliability. It has a unique advantage in that saved images can be viewed in coronal, and axial planes. The first 3D ultrasound study in rheumatology, reported in 2009, showed good to excellent agreement between two-dimensional (2D) and 3D ultrasound modalities relating to both joint inﬂammation and bone erosion [Filippucci et al. 2009]. Another report also demonstrated that interobserver reliability of 3D volumetric ultrasound in the detection of synovitis was higher than 2D ultrasound [Naredo et al. 2010]. One of the promising features of 3D ultrasound is its ability to quantify regions of interest (Figure 3), although no commercial software is available. The metric ability of 3D ultrasound can provide new advances in measuring lesions, but the metric quality according to the OMERACT filter should be established. It is likely that the use of 3D and 4D ultrasound will grow steadily in the future, but their application in musculoskeletal diseases has remained in the research domain in many rheumatology clinics [Ju et al. 2008].

Figure 3.

Long axis two-dimensional ultrasound and corresponding three-dimensional (3D) ultrasound image of a small full thickness tear of the supraspinatus tendon. With appropriate multiplanar reconstruction, 3D ultrasound allows adequate delineation of the tear width and the amount of tendon retraction from the greater tuberosity (GT) (courtesy of Carlo Martinoli, MD and Paolo Nucci, PhD, Philips Healthcare).

Elastography

The principle of strain imaging, which is known as elastography, was first reported in 1991 as a new ultrasound-based technique able to assess tissue elasticity [Ophir et al. 1991]. Later, a fast cross-sectional technique was developed, based on real-time elastography, which analyzes ultrasound echo signals while the probe compresses or relaxes the tissue [Pesavento et al. 1999]. In rheumatology, elastography was first used to evaluate changes in Achilles tendons in 2009 (Figure 4) [De Zordo et al. 2009a, 2009b]. Then, an elastography study of skin involvement in patients with systemic sclerosis showed the reduction of strain in the dermis of the forearm [Iagnocco et al. 2010]. Currently, additional data are needed on scleroderma and more validatory and prospective studies are required to establish the true value of elastography.

Figure 4.

Elastography of a degenerate Achilles tendon. The greyscale image shows relative preservation of the posterior tendon fibres but the mid and anterior portion is abnormal as evidenced by hypoechogenicity, loss of fibrillar pattern and thickening. Elastography represents tissue elasticity using a spectrum of colours – at one extreme, hard structures are denoted as blue and at the other, soft structures are seen as red. These images clearly show that elastography has the potential to differentiate between normal and abnormal portions of tendon. AT, Achilles tendon; Cal, calcaneum.

Fusion imaging

The fusion imaging technique is the simultaneous mapping of ultrasound images onto a pre-acquired 3D multiplanar reslice CT or MRI volume dataset. The transducer needs adaptation to allow additional sensors to be positioned by means of a clip-on attachment. Fusion imaging may be useful for the differentiation of anatomical structures and injection of the sacroiliac joint [Klauser et al. 2008]. In 2011, MRI/ultrasound real-time fusion imaging was first reported in patients with osteoarthritis and rheumatoid arthritis. Fusion imaging was able to provide consistent bony landmarks for potential longitudinal evaluation [Iagnocco et al. 2011]. However, its diagnostic and therapeutic role in rheumatic diseases has not yet been fully studied and requires further definition.

Conclusion

From the discovery of ultrasound to the application in rheumatology, musculoskeletal ultrasound has evolved in favour of early detection of joint inflammation, assessing ongoing disease activity and monitoring therapeutic responses. Consequently, musculoskeletal ultrasound is fast becoming an essential tool in routine clinical practice for rheumatologists. We anticipate that all rheumatology departments in the future will use ultrasound or have access to it. Similarly, it is likely that ultrasound techniques will start to be taught at an undergraduate level as it is fast becoming an integral part of other medical specialties as well. The technical advances expected in the future are likely to make musculoskeletal ultrasound more accessible to rheumatologists and allow faster and more accurate imaging of joints and related structures.

Footnotes

Funding

Dr Lanni is grateful to Pfizer ARTICULUM Fellowship for his financial support.

Conflict of interest statement

The authors declare no conflicts of interest in preparing this article.

References

Alcalde

Acebes

Cruz

Gonzalez-Hombrado

Herrero-Beaumont

Sanchez-Pernaute

(2007) A sonographic enthesitic index of lower limbs is a valuable tool in the assessment of ankylosing spondylitis. Ann Rheum Dis 66: 1015–1019.

Attur

Samuels

Krasnokutsky

Abramson

S.B.

(2010) Targeting the synovial tissue for treating osteoarthritis (OA): where is the evidence? Best Pract Res Clin Rheumatol 24: 71–79.

Backhaus

(2009) Ultrasound and structural changes in inflammatory arthritis: synovitis and tenosynovitis. Ann N Y Acad Sci 1154: 139–151.

Backhaus

Burmester

Gerber

Grassi

Machold

Swen

. (2001) Guidelines for musculoskeletal ultrasound in rheumatology. Ann Rheum Dis 60: 641–649.

Backhaus

Ohrndorf

Kellner

Strunk

Backhaus

Hartung

. (2009) Evaluation of a novel 7-joint ultrasound score in daily rheumatologic practice: a pilot project. Arthritis Rheum 61: 1194–1201.

Boers

Brooks

Strand

Tugwell

(1998) The OMERACT filter for outcome measures in rheumatology. J Rheumatol 25: 198–199.

Borman

Koparal

Babaoglu

Bodur

(2006) Ultrasound detection of entheseal insertions in the foot of patients with spondyloarthropathy. Clin Rheumatol 25: 373–377.

Bruyn

Naredo

Moller

Moragues

Garrido

De Bock

. (2009) Reliability of ultrasonography in detecting shoulder disease in patients with rheumatoid arthritis. Ann Rheum Dis 68: 357–361.

Bruyn

Pineda

Hernandez-Diaz

Ventura-Rios

Moya

Garrido

. (2010) Validity of ultrasonography and measures of adult shoulder function and reliability of ultrasonography in detecting shoulder synovitis in patients with rheumatoid arthritis using magnetic resonance imaging as a gold standard. Arthritis Care Res (Hoboken) 62: 1079–1086.

10.

Carotti

Salaffi

Manganelli

Salera

Simonetti

Grassi

(2002) Power Doppler sonography in the assessment of synovial tissue of the knee joint in rheumatoid arthritis: a preliminary experience. Ann Rheum Dis 61: 877–882.

11.

Cooperberg

Tsang

Truelove

Knickerbocker

(1978) Gray scale ultrasound in the evaluation of rheumatoid arthritis of the knee. Radiology 126: 759–763.

12.

Cunnington

Marshall

Hide

Bracewell

Isaacs

Platt

. (2010) A randomized, double-blind, controlled study of ultrasound-guided corticosteroid injection into the joint of patients with inflammatory arthritis. Arthritis Rheum 62: 1862–1869.

13.

D’Agostino

Conaghan

Naredo

Aegerter

Iagnocco

Freeston

. (2009) The OMERACT ultrasound task force – advances and priorities. J Rheumatol 36: 1829–1832.

14.

D’Agostino

Said-Nahal

Hacquard-Bouder

Brasseur

Dougados

Breban

(2003) Assessment of peripheral enthesitis in the spondylarthropathies by ultrasonography combined with power Doppler: a cross-sectional study. Arthritis Rheum 48: 523–533.

15.

De Flaviis

Scaglione

Nessi

Ventura

Calori

(1988) Ultrasonography of the hand in rheumatoid arthritis. Acta Radiol 29: 457–460.

16.

De Miguel

Cobo

Munoz-Fernandez

Naredo

Uson

Acebes

. (2009) Validity of enthesis ultrasound assessment in spondyloarthropathy. Ann Rheum Dis 68: 169–174.

17.

De Miguel

Puig

Castillo

Peiteado

Torres

Martin-Mola

(2011) Diagnosis of gout in patients with asymptomatic hyperuricaemia: a pilot ultrasound study. Ann Rheum Dis 71: 157–158.

18.

De Vita

Lorenzon

Rossi

Sabella

Fossaluzza

(1992) Salivary gland echography in primary and secondary Sjögren’s syndrome. Clin Exp Rheumatol 10: 351–356.

19.

De Zordo

Fink

Feuchtner

Smekal

Reindl

Klauser

(2009a) Real-time sonoelastography findings in healthy Achilles tendons. AJR Am J Roentgenol 193: W134–W138.

20.

De Zordo

Lill

Fink

Feuchtner

Jaschke

Bellmann-Weiler

. (2009b) Real-time sonoelastography of lateral epicondylitis: comparison of findings between patients and healthy volunteers. AJR Am J Roentgenol 193: 180–185.

21.

Deshpande

Lutz

Ren

Foygel

Tian

Schneider

. (2011) Quantification and monitoring of inflammation in murine inflammatory bowel disease with targeted contrast-enhanced US. Radiology 262: 172–180

22.

Dohn

Ejbjerg

Court-Payen

Hasselquist

Narvestad

Szkudlarek

. (2006) Are bone erosions detected by magnetic resonance imaging and ultrasonography true erosions? A comparison with computed tomography in rheumatoid arthritis metacarpophalangeal joints. Arthritis Res Ther 8: R110.

23.

Donald

Macvicar

Brown

(1958) Investigation of abdominal masses by pulsed ultrasound. Lancet 1: 1188–1195.

24.

Dussik

(1942) On the possibility of using ultrasound waves as a diagnostic aid. Z Neurol Psychiatr 174: 153–168.

25.

Falsetti

Frediani

Fioravanti

Acciai

Baldi

Filippou

. (2003) Sonographic study of calcaneal entheses in erosive osteoarthritis, nodal osteoarthritis, rheumatoid arthritis and psoriatic arthritis. Scand J Rheumatol 32: 229–234.

26.

Filer

De Pablo

Allen

Nightingale

Jordan

Jobanputra

. (2011) Utility of ultrasound joint counts in the prediction of rheumatoid arthritis in patients with very early synovitis. Ann Rheum Dis 70: 500–507.

27.

Filippucci

Meenagh

Delle Sedie

Salaffi

Riente

Iagnocco

. (2009) Ultrasound imaging for the rheumatologist. xx. sonographic assessment of hand and wrist joint involvement in rheumatoid arthritis: comparison between two- and three-dimensional ultrasonography. Clin Exp Rheumatol 27: 197–200.

28.

Filippucci

Riveros

Georgescu

Salaffi

Grassi

(2009) Hyaline cartilage involvement in patients with gout and calcium pyrophosphate deposition disease. An ultrasound study. Osteoarthritis Cartilage 17: 178–181.

29.

Finzel

Ohrndorf

Englbrecht

Stach

Messerschmidt

Schett

. (2011) A detailed comparative study of high-resolution ultrasound and micro-computed tomography for detection of arthritic bone erosions. Arthritis Rheum 63: 1231–1236.

30.

Frediani

Filippou

Falsetti

Lorenzini

Baldi

Acciai

. (2005) Diagnosis of calcium pyrophosphate dihydrate crystal deposition disease: ultrasonographic criteria proposed. Ann Rheum Dis 64: 638–640.

31.

Fukae

Kon

Henmi

Sakamoto

Narita

Shimizu

. (2010) Change of synovial vascularity in single finger joint assessed by power Doppler sonography correlated with radiographic change in rheumatoid arthritis: comparative study of novel quantitative score with semi-quantitative score. Arthritis Care Res (Hoboken) 62: 657–663.

32.

Gandjbakhch

Terslev

Joshua

Wakefield

Naredo

D’Agostino

(2011) Ultrasound in the evaluation of enthesitis: status and perspectives. Arthritis Res Ther 13: R188.

33.

Gilliland

Salazar

Borchers

(2011) Ultrasound versus anatomic guidance for intra-articular and periarticular injection: a systematic review. Phys Sportsmed 39: 121–131.

34.

Gompels

Darlington

(1981) Septic arthritis in rheumatoid disease causing bilateral shoulder dislocation: diagnosis and treatment assisted by grey scale ultrasonography. Ann Rheum Dis 40: 609–611.

35.

Gramiak

Shah

(1968) Echocardiography of the aortic root. Invest Radiol 3: 356–366.

36.

Grassi

(2003) Clinical evaluation versus ultrasonography: who is the winner? J Rheumatol 30: 908–909.

37.

Grassi

Meenagh

Pascual

Filippucci

(2006) ‘Crystal clear’-sonographic assessment of gout and calcium pyrophosphate deposition disease. Semin Arthritis Rheum 36: 197–202.

38.

Grassi

Tittarelli

Pirani

Avaltroni

Cervini

(1993) Ultrasound examination of metacarpophalangeal joints in rheumatoid arthritis. Scand J Rheumatol 22: 243–247.

39.

Hammer

Kvien

(2011) Comparisons of 7- to 78-joint ultrasonography scores: all different joint combinations show equal response to adalimumab treatment in patients with rheumatoid arthritis. Arthritis Res Ther 13: R78.

40.

Hau

Schultz

Tony

Keberle

Jahns

Haerten

. (1999) Evaluation of pannus and vascularization of the metacarpophalangeal and proximal interphalangeal joints in rheumatoid arthritis by high-resolution ultrasound (multidimensional linear array). Arthritis Rheum 42: 2303–2308.

41.

Hocevar

Ambrozic

Rozman

Kveder

Tomsic

(2005) Ultrasonographic changes of major salivary glands in primary Sjögren’s syndrome. diagnostic value of a novel scoring system. Rheumatology (Oxford) 44: 768–772.

42.

Iagnocco

Coari

Zoppini

(1992) Sonographic evaluation of femoral condylar cartilage in osteoarthritis and rheumatoid arthritis. Scand J Rheumatol 21: 201–203.

43.

Iagnocco

Kaloudi

Perella

Bandinelli

Riccieri

Vasile

. (2010) Ultrasound elastography assessment of skin involvement in systemic sclerosis: lights and shadows. J Rheumatol 37: 1688–1691.

44.

Iagnocco

Perella

D’Agostino

Sabatini

Valesini

Conaghan

(2011) Magnetic resonance and ultrasonography real-time fusion imaging of the hand and wrist in osteoarthritis and rheumatoid arthritis. Rheumatology (Oxford) 50: 1409–1413.

45.

Kang

Kim

Yoon

Kim

Park

(2008) Three-dimensional ultrasonographic application for analyzing synovial hypertrophy of the knee in patients with osteoarthritis. J Ultrasound Med 27: 729–736.

46.

Kaeley

(2010) Training and education in rheumatology ultrasound: American experience. In: Wakefield

D’Agostino

(eds), Essential Applications of Musculoskeletal Ultrasound in Rheumatology. Philadelphia: Elsevier, pp.344–345.

47.

Kane

Balint

Sturrock

(2003) Ultrasonography is superior to clinical examination in the detection and localization of knee joint effusion in rheumatoid arthritis. J Rheumatol 30: 966–971.

48.

Karim

Wakefield

Quinn

Conaghan

Brown

Veale

. (2004) Validation and reproducibility of ultrasonography in the detection of synovitis in the knee: a comparison with arthroscopy and clinical examination. Arthritis Rheum 50: 387–394.

49.

Keen

Wakefield

Grainger

Hensor

Emery

Conaghan

(2008) An ultrasonographic study of osteoarthritis of the hand: synovitis and its relationship to structural pathology and symptoms. Arthritis Rheum 59: 1756–1763.

50.

Klauser

De Zordo

Feuchtner

Sogner

Schirmer

Gruber

. (2008) Feasibility of ultrasound-guided sacroiliac joint injection considering sonoanatomic landmarks at two different levels in cadavers and patients. Arthritis Rheum 59: 1618–1624.

51.

Klauser

Demharter

De Marchi

Sureda

Barile

Masciocchi

. (2005) Contrast enhanced greyscale sonography in assessment of joint vascularity in rheumatoid arthritis: results from the IACUS study group. Eur Radiol 15: 2404–2410.

52.

Klauser

Frauscher

Schirmer

Halpern

Pallwein

Herold

. (2002) The value of contrast-enhanced color Doppler ultrasound in the detection of vascularization of finger joints in patients with rheumatoid arthritis. Arthritis Rheum 46: 647–653.

53.

Koski

(1989) Ultrasonographic evidence of hip synovitis in patients with rheumatoid arthritis. Scand J Rheumatol 18: 127–131.

54.

Koski

(2000) Ultrasound guided injections in rheumatology. J Rheumatol 27: 2131–2138.

55.

Koski

Anttila

Isomaki

(1989) Ultrasonography of the adult hip joint. Scand J Rheumatol 18: 113–117.

56.

Kunkel

(2010) Tophaceous gout mimicking osteomyelitis: the value of musculoskeletal ultrasound in establishing the diagnosis. J Clin Rheumatol 16: 295–297.

57.

Lopez-Ben

Bernreuter

Moreland

Alarcon

(2004) Ultrasound detection of bone erosions in rheumatoid arthritis: a comparison to routine radiographs of the hands and feet. Skeletal Radiol 33: 80–84.

58.

Makula

Pokorny

Kiss

Voros

Kovacs

. (2000) The place of magnetic resonance and ultrasonographic examinations of the parotid gland in the diagnosis and follow-up of primary Sjögren’s syndrome. Rheumatology (Oxford) 39: 97–104.

59.

Mancarella

Magnani

Addimanda

Pignotti

Galletti

Meliconi

(2010) Ultrasound-detected synovitis with power Doppler signal is associated with severe radiographic damage and reduced cartilage thickness in hand osteoarthritis. Osteoarthritis Cartilage 18: 1263–1268.

60.

Martinoli

Derchi

Solbiati

Rizzatto

Silvestri

Giannoni

(1994) Color Doppler sonography of salivary glands. AJR Am J Roentgenol 163: 933–941.

61.

McCarty

Hollander

(1961) Identification of urate crystals in gouty synovial fluid. Ann Intern Med 54: 452–460.

62.

McDonald

Leopold

(1972) Ultrasound B-scanning in the differentiating of Baker’s cyst and thrombophlebitis. Br J Radiol 45: 729–732.

63.

Meenagh

Filippucci

Iagnocco

Delle Sedie

Riente

Bombardieri

. (2007) Ultrasound imaging for the rheumatologist VIII. Ultrasound imaging in osteoarthritis. Clin Exp Rheumatol 25: 172–175.

64.

Milic

Petrovic

Boricic

Marinkovic-Eric

Radunovic

Jeremic

. (2009) Diagnostic value of salivary gland ultrasonographic scoring system in primary Sjögren’s syndrome: a comparison with scintigraphy and biopsy. J Rheumatol 36: 1495–1500.

65.

Moller

Bonel

Rotzetter

Villiger

Ziswiler

(2009) Measuring finger joint cartilage by ultrasound as a promising alternative to conventional radiograph imaging. Arthritis Rheum 61: 435–441.

66.

Naredo

Bijlsma

Conaghan

Acebes

Balint

Berner-Hammer

. (2008) Recommendations for the content and conduct of European League Against Rheumatism (EULAR) musculoskeletal ultrasound courses. Ann Rheum Dis 67: 1017–1022.

67.

Naredo

Bonilla

Gamero

Uson

Carmona

Laffon

(2005) Assessment of inflammatory activity in rheumatoid arthritis: a comparative study of clinical evaluation with grey scale and power Doppler ultrasonography. Ann Rheum Dis 64: 375–381.

68.

Naredo

Moller

Acebes

Batlle-Gualda

Brito

De Agustin

. (2010) Three-dimensional volumetric ultrasonography. does it improve reliabililty of musculoskeletal ultrasound? Clin Exp Rheumatol 28: 79–82.

69.

Naredo

Rodriguez

Campos

Rodriguez-Heredia

Medina

Giner

. (2008) Validity, reproducibility, and responsiveness of a twelve-joint simplified power doppler ultrasonographic assessment of joint inflammation in rheumatoid arthritis. Arthritis Rheum 59: 515–522.

70.

Nesher

Shemesh

Mates

Sonnenblick

Abramowitz

(2002) The predictive value of the halo sign in color Doppler ultrasonography of the temporal arteries for diagnosing giant cell arteritis. J Rheumatol 29: 1224–1226.

71.

Newman

Adler

Bude

Rubin

(1994) Detection of soft-tissue hyperemia: value of power Doppler sonography. AJR Am J Roentgenol 163: 385–389.

72.

Ophir

Cespedes

Ponnekanti

Yazdi

(1991) Elastography: a quantitative method for imaging the elasticity of biological tissues. Ultrason Imaging 13: 111–134.

73.

Pesavento

Perrey

Krueger

Ermert

(1999) A time-efficient and accurate strain estimation concept for ultrasonic elastography using iterative phase zero estimation. IEEE Trans Ultrason Ferroelectr Freq Control 46: 1057–1067.

74.

Quaia

(2007) Microbubble ultrasound contrast agents: an update. Eur Radiol 17: 1995–2008.

75.

Reynolds

Heron

Pilcher

Kiely

(2009) Prediction of erosion progression using ultrasound in established rheumatoid arthritis: a 2-year follow-up study. Skeletal Radiol 38: 473–478.

76.

Ruta

Gutierrez

Pena

Garcia

Arturi

Filippucci

. (2011) Prevalence of subclinical enthesopathy in patients with spondyloarthropathy: an ultrasound study. J Clin Rheumatol 17: 18–22.

77.

Salaffi

Carotti

Iagnocco

Luccioli

Ramonda

Sabatini

. (2008) Ultrasonography of salivary glands in primary Sjögren’s syndrome: a comparison with contrast sialography and scintigraphy. Rheumatology (Oxford) 47: 1244–1249.

78.

Samuels

Abramson

Kaeley

(2010) The use of musculoskeletal ultrasound by rheumatologists in the United States. Bull NYU Hosp Jt Dis 68: 292–298.

79.

Schmidt

Kraft

Volker

Vorpahl

Gromnica-Ihle

(1995) Colour Doppler sonography to diagnose temporal arteritis. Lancet 345: 866.

80.

Schmidt

Kraft

Vorpahl

Volker

Gromnica-Ihle

(1997) Color duplex ultrasonography in the diagnosis of temporal arteritis. N Engl J Med 337: 1336–1342.

81.

Schmidt

Krause

Schicke

Wernicke

(2008) Color Doppler ultrasonography of hand and finger arteries to differentiate primary from secondary forms of Raynaud’s phenomenon. J Rheumatol 35: 1591–1598.

82.

Schmidt

Seipelt

Molsen

Poehls

Gromnica-Ihle

(2001) Vasculitis of the internal carotid artery in Wegener’s granulomatosis: comparison of ultrasonography, angiography, and MRI. Scand J Rheumatol 30: 48–50.

83.

Schmidt

Volker

Zacher

Schlafke

Ruhnke

Gromnica-Ihle

(2000) Colour Doppler ultrasonography to detect pannus in knee joint synovitis. Clin Exp Rheumatol 18: 439–444.

84.

Schmidt

Wernicke

Kiefer

Gromnica-Ihle

(2006) Colour duplex sonography of finger arteries in vasculitis and in systemic sclerosis. Ann Rheum Dis 65: 265–267.

85.

Scire

Montecucco

Codullo

Epis

Todoerti

Caporali

(2009) Ultrasonographic evaluation of joint involvement in early rheumatoid arthritis in clinical remission: power Doppler signal predicts short-term relapse. Rheumatology (Oxford) 48: 1092–1097.

86.

Sibbitt

Peisajovich

Michael

Park

Sibbitt

Band

. (2009) Does sonographic needle guidance affect the clinical outcome of intraarticular injections? J Rheumatol 36: 1892–1902.

87.

Stone

Bergin

Whelan

Maher

Murray

McCarthy

(2001) Power Doppler ultrasound assessment of rheumatoid hand synovitis. J Rheumatol 28: 1979–1982.

88.

Szkudlarek

Court-Payen

Jacobsen

Klarlund

Thomsen

Ostergaard

(2003a) Interobserver agreement in ultrasonography of the finger and toe joints in rheumatoid arthritis. Arthritis Rheum 48: 955–962.

89.

Szkudlarek

Court-Payen

Strandberg

Klarlund

Klausen

Ostergaard

(2001) Power Doppler ultrasonography for assessment of synovitis in the metacarpophalangeal joints of patients with rheumatoid arthritis: a comparison with dynamic magnetic resonance imaging. Arthritis Rheum 44: 2018–2023.

90.

Szkudlarek

Court-Payen

Strandberg

Klarlund

Klausen

Ostergaard

(2003b) Contrast-enhanced power Doppler ultrasonography of the metacarpophalangeal joints in rheumatoid arthritis. Eur Radiol 13: 163–168.

91.

Terslev

Torp-Pedersen

Qvistgaard

Bliddal

(2003a) Spectral Doppler and resistive index. A promising tool in ultrasonographic evaluation of inflammation in rheumatoid arthritis. Acta Radiol 44: 645–652.

92.

Terslev

Torp-Pedersen

Savnik

Von Der Recke

Qvistgaard

Danneskiold-Samsoe

. (2003b) Doppler ultrasound and magnetic resonance imaging of synovial inflammation of the hand in rheumatoid arthritis: a comparative study. Arthritis Rheum 48: 2434–2441.

93.

Terslev

Von Der Recke

Torp-Pedersen

Koenig

Bliddal

(2008) Diagnostic sensitivity and specificity of Doppler ultrasound in rheumatoid arthritis. J Rheumatol 35: 49–53.

94.

Thiele

Schlesinger

(2007) Diagnosis of gout by ultrasound. Rheumatology (Oxford) 46: 1116–1121.

95.

Thiele

Schlesinger

(2010) Ultrasonography shows disappearance of monosodium urate crystal deposition on hyaline cartilage after sustained normouricemia is achieved. Rheumatol Int 30: 495–503.

96.

Wakefield

Balint

Szkudlarek

Filippucci

Backhaus

D’Agostino

. (2005) Musculoskeletal ultrasound including definitions for ultrasonographic pathology. J Rheumatol 32: 2485–2487.

97.

Wakefield

Gibbon

Conaghan

O’Connor

McGonagle

Pease

. (2000) The value of sonography in the detection of bone erosions in patients with rheumatoid arthritis: a comparison with conventional radiography. Arthritis Rheum 43: 2762–2770.

98.

Wakefield

Gibbon

Emery

(1999) The current status of ultrasonography in rheumatology. Rheumatology (Oxford) 38: 195–198.

99.

Walther

Harms

Krenn

Radke

Faehndrich

Gohlke

(2001) Correlation of power Doppler sonography with vascularity of the synovial tissue of the knee joint in patients with osteoarthritis and rheumatoid arthritis. Arthritis Rheum 44: 331–338.

100.

Walther

Harms

Krenn

Radke

Kirschner

Gohlke

(2002) Synovial tissue of the hip at power Doppler US: correlation between vascularity and power Doppler US signal. Radiology 225: 225–231.

101.

Wiell

Szkudlarek

Hasselquist

Moller

Vestergaard

Norregaard

. (2007) Ultrasonography, magnetic resonance imaging, radiography, and clinical assessment of inflammatory and destructive changes in fingers and toes of patients with psoriatic arthritis. Arthritis Res Ther 9: R119.

102.

Yonetsu

Takagi

Sumi

Nakamura

Eguchi

(2002) Sonography as a replacement for sialography for the diagnosis of salivary glands affected by Sjögren’s syndrome. Ann Rheum Dis 61: 276–277.

The evolution of ultrasound in rheumatology

Abstract

Keywords

Introduction

Brief history: from the discovery of ultrasound to recent high-end machines

From the first demonstration of synovial thickening to the end of the twentieth century

The twenty-first century has opened a new era for ultrasound in rheumatology

Developments in education and training

Developments in standardization

Advances in rheumatologic diseases and their assessment

Rheumatoid arthritis

Spondyloarthropathies

Osteoarthritis

Crystal arthropathies: gout and pseudogout

Vasculitis

Salivary glands/Sjögren syndrome

Ultrasound-guided interventions

New research areas in the twenty-first century in rheumatology ultrasound

Contrast-enhanced ultrasound

Three- and four-dimensional ultrasonography

Elastography

Fusion imaging

Conclusion

Footnotes

Funding

Conflict of interest statement

References