Abstract

As we begin the 21st century, musculoskeletal ultrasound (MSUS) is routinely used by an increasing number of rheumatologists throughout Europe and there is a growing interest in the application of MSUS in rheumatological practice in the UK. MSUS allows high-resolution, real-time imaging of articular and periarticular structures and has the advantages of being non-radioactive, inexpensive, portable, highly acceptable to patients and repeatable. There are a number of critical issues that need to be addressed in order to develop the role of MSUS within rheumatology. These include issues of equipment costs, training and certification and the relationship of rheumatologists and radiologists in advancing the field of MSUS. Rheumatologists must demonstrate the relevance of MSUS in their clinical practice through high-quality research. Emerging technologies such as power Doppler and 3D imaging will further improve imaging capabilities and the range of clinical applications of MSUS systems. This paper reviews how MSUS in rheumatology has evolved and the controversies and issues that rheumatologists must now address in developing MSUS as an indispensable, everyday clinical tool.

The application of ultrasound (US) imaging in many medical specialties is now widely regarded as an indispensable tool, having been first pioneered in surgery and obstetrics in the late 1950s and early 1960s [13]. Though the use of US to image articular and periarticular tissues was reported as early as 1958 [4], the first clinical application of musculoskeletal ultrasonography (MSUS)—differentiating Baker's cysts from thrombophlebitis—was only reported in 1972 [5].

The development of rheumatological ultrasound

Modern ‘rheumatological ultrasound’ probably began with the demonstration of synovitis of the knee in rheumatoid arthritis (RA) in 1978 [6]. Technical advances in US have led to high-resolution imaging of musculoskeletal structures and MSUS is now widely used as an important tool in imaging the musculoskeletal system. Combined with a better understanding of the rheumatic diseases, multiplanar imaging of articular structures in real time, low running costs, absence of radiation and excellent patient acceptability, MSUS is an ideal tool for rheumatologists [7]. However, whether MSUS should be performed by radiologists, rheumatologists, other musculoskeletal practitioners or all three continues to generate controversy.

That MSUS would become a natural extension of musculoskeletal examination performed by rheumatologists could have been predicted by the rapid incorporation of US as a routine extension of clinical examination in other clinical specialities such as obstetrics, gynaecology and cardiology. In Germany, the introduction of MSUS into clinical practice was pioneered by rheumatologists and MSUS is now a standard part of the rheumatology training curriculum [7]. Indeed the use of MSUS by rheumatologists has made a considerable contribution to the understanding of the natural history of rheumatic diseases and to improved diagnostic and interventional clinical skills [8, 9].

However, there is considerable variability in the uptake of MSUS by rheumatologists internationally [10]. MSUS is a routine part of rheumatology training in Italy [11] and Germany [7] but remains largely the preserve of radiologists in the USA and UK despite a widespread interest among rheumatologists internationally [10]. The reasons for this are complex and involve issues of funding, equipment, standardization, training and the traditional attitudes of rheumatologists themselves to MSUS.

Why rheumatologists should perform ultrasound

Rheumatologists are divided on the issue of incorporating MSUS into their practices. Because of their anatomical and pathological knowledge of the musculoskeletal system they are in an advantageous position to train in MSUS. However, genuine concerns exist regarding the impact of MSUS on current clinical workload, the initial cost of equipment and the lack of clear guidelines for training. The principal benefits of US are in immediate confirmation of the diagnosis for the patient and superior interventional skills. The steady rise in the number of MSUS publications in the rheumatology literature over the last decade and the over-subscription of the recent European League Against Rheumatism (EULAR) and American College of Rheumatology (ACR) MSUS training sessions is testament to the increasing acceptance of MSUS among rheumatologists.

Current practice of MSUS by rheumatologists in Europe

A survey of rheumatologists from 19 European countries who were attending the 1999 EULAR Annual General Meeting confirmed the existence of a wide degree of interest in MSUS by rheumatologists [10]. Forty per cent of respondents were already performing MSUS within their own department and a further 45% were interested in using MSUS in their practice. The indications for and benefits of MSUS for rheumatologists are detailed in Table 1. The majority of rheumatologists surveyed reported that they used MSUS for clinical purposes in 80% of patients and for research purposes in 20% of patients. Clinical indications were predominantly for diagnosis (84%), injection guidance (12%) and disease monitoring.

Table 1.

Why rheumatologists should perform musculoskeletal ultrasound

Improve immediate diagnosis of joint and soft tissue disease (‘Extension of clinical examination’) 
Improve interventional skills 
Imaging modality of choice for tendon disease 
Early diagnosis of synovitis 
Early diagnosis of bone erosion and cartilage damage 
Objective monitoring of therapeutic response, disease status and outcome 
Improve clinician's understanding of functional anatomy 
Improve clinician's understanding of functional pathology 
Provide new insights into rheumatological disease 
Patient education 
Paediatric rheumatology: high patient acceptability, no need for general anaesthesia as may be required with MRI 
Improve immediate diagnosis of joint and soft tissue disease (‘Extension of clinical examination’) 
Improve interventional skills 
Imaging modality of choice for tendon disease 
Early diagnosis of synovitis 
Early diagnosis of bone erosion and cartilage damage 
Objective monitoring of therapeutic response, disease status and outcome 
Improve clinician's understanding of functional anatomy 
Improve clinician's understanding of functional pathology 
Provide new insights into rheumatological disease 
Patient education 
Paediatric rheumatology: high patient acceptability, no need for general anaesthesia as may be required with MRI 

Should MSUS be performed by rheumatologists or radiologists?

The 60% of rheumatologists who did not perform MSUS in their departments cited the following principal reasons: an adequate service from their radiology department (45%), lack of clinician time to perform MSUS (38%) and prohibitive expense of equipment (38%). These legitimate concerns need to be addressed. Rheumatology units that perform MSUS usually develop a complementary practice to that of radiologists. Radiological practice has principally focused on orthopaedic conditions such as rotator cuff tears and soft tissue injuries. Rheumatologists have developed MSUS to image previously neglected areas such as the detection of synovitis, enthesitis and bony erosion, the guidance of joint and soft tissue aspiration and injection and for monitoring of therapeutic response. It is important that rheumatologists and radiologists engage in the development of the field of MSUS, which will be best served by good cooperation and communication between them. Though the introduction of MSUS may initially impinge on clinician time, it soon takes only a few minutes to perform a scan in the out-patient setting. It is also likely that more accurate diagnosis, aspiration and joint injection will lead to an improved patient outcome and fewer return visits by the patient resulting in a freeing up of clinician time. The costs of MSUS equipment are continuously decreasing and there is a sound economic and medico-legal argument for introducing US guidance of joint and soft tissue injections in the rheumatology department.

The impact of MSUS on routine rheumatology practice

There is accumulating evidence that MSUS impacts on clinical diagnosis [9, 12] and intervention skills [1315]. Most rheumatologists would accept that MSUS has a major role in the accurate diagnosis of shoulder disease, as the shoulder is a complex joint structure [14]. However, even in the evaluation of knee effusions—a basic clinical skill—MSUS has consistently been proven to be superior to clinical examination [16]. MSUS should not replace clinical examination but should complement it. MSUS also has the advantage that it will continuously improve the operator's understanding of regional and functional anatomy and pathological processes leading to improved clinical examination skills. Joint aspiration is more frequently successful when performed with MSUS guidance [13] and initial evidence suggests that the success of joint injection (Fig. 1) is also improved by more accurate delivery by MSUS guidance [14]. While formal evidence to support the cost-effectiveness of MSUS in rheumatology is currently lacking and is required, it is likely that improved diagnostic and interventional skills will lead to improved patient care and clinical outcome.

Fig. 1.

Sonographic-guided injection of steroid in the metacarpophalangeal joint of a patient with rheumatoid arthritis (8–16 MHz linear transducer, Diasus, Dynamic Imaging Ltd, UK). The tip of the needle is clearly visualized (→), as well as the steroid after the injection (*). MSUS improves the accuracy of joint and soft tissue injection and has the potential to produce major improvements in the efficacy of this routine procedure.

Fig. 1.

Sonographic-guided injection of steroid in the metacarpophalangeal joint of a patient with rheumatoid arthritis (8–16 MHz linear transducer, Diasus, Dynamic Imaging Ltd, UK). The tip of the needle is clearly visualized (→), as well as the steroid after the injection (*). MSUS improves the accuracy of joint and soft tissue injection and has the potential to produce major improvements in the efficacy of this routine procedure.

Is MSUS changing our understanding of rheumatic disease?

The availability of MSUS in the rheumatology clinic has led to new insights into the pathogenesis of rheumatic diseases such as polymyalgia rheumatica. Previously believed to be an extra-articular disease, MSUS examination—confirmed by magnetic resonance imaging (MRI)—has found hip and shoulder synovitis and subdeltoid bursitis in 68–100% of patients with polymyalgia [1720]. The detection of joint effusion and subsequent aspiration of fluid will facilitate novel approaches in basic research of polymyalgia rheumatica and local corticosteroid injection may have a therapeutic role in some cases.

How to train rheumatologists?

In the absence of an agreed international training curriculum and certification, there is considerable variability in the degree and type of training undertaken by rheumatologists who perform MSUS. A survey of European rheumatologists currently performing MSUS confirmed that the majority had learned MSUS during their postgraduate training, usually through a combination of a formal MSUS course and informal training from a colleague, predominantly a rheumatologist or radiologist [10].

Formal training

A useful starting point for rheumatologists wishing to train in MSUS is to attend a formal 2–3 day training course in order to obtain a standardized overview of the technique and to gain initial practical ‘hands on’ experience. An annual EULAR course has been successfully run since 1996 and increasing demand has seen it become a twice-yearly event with the recent addition of an advanced course. In the UK an Oxford/Leeds course has been run by radiologists since 1996 and the second British Society for Rheumatology (BSR) MSUS course took place in Glasgow in November 2003, having been fully subscribed 6 months in advance. It must be emphasized that these courses are only designed to provide a basis for subsequent supervised MSUS training.

Existing guidelines for supervised MSUS training

Some countries have established guidelines for the duration of supervised MSUS training. In the USA the American College of Radiology recommends a minimum of 3 months of sonographic training with involvement in a minimum of 500 scans and the American Institute of Radiology also recommends a minimum of 500 scans for multiple anatomical sites [21]. In Europe, MSUS in rheumatology is most established in Germany and Italy where it is integrated into the training curriculum of rheumatologists. For accreditation in Germany and Italy, a rheumatologist has to be actively involved in 200 joint and soft tissue US examinations—acting as first operator for at least 60 scans—under the surveillance of an experienced teacher. In addition a 2–3 day training course is recommended in Germany, particularly at the early stages of training [7].

No such guidelines exist in the UK, though the Royal College of Radiologists recommends a minimum of 300 h of supervised scanning in an accredited training department and there is ongoing work on the development of appropriate guidelines for rheumatologists [22]. While some of these guidelines may seem prohibitively excessive, the German and Italian models may be the most appropriate for rheumatologists in the UK and other countries as they have already been successfully implemented for a number of years. The requirements of the German and Italian models are also not particularly onerous when placed in the context of a 4–5 yr training programme for rheumatology. A critical issue in the implementation of this model will be the wider availability of access to ultrasound equipment and proper supervision in rheumatology or radiology departments.

Information technology and self-directed learning

The development of information technology and the internet has also provided other valuable sources for MSUS training. A number of excellent websites such as the EULAR working group for musculoskeletal ultrasound (http://www.sameint.it/eular/ultrasound) and the University of Michigan Health System (http://www.med.umich.edu/rad/muscskel/mskus) provide free technical information, guidelines and illustrative ultrasound pictures for training in addition to a wide array of pathological cases. Using the EULAR website as a training reference for obtaining MSUS images a novice was able to obtain MSUS images of an acceptable clinical standard after 24 non-consecutive hours of mostly self-directed learning on five healthy subjects and 14 patients with arthritis [23]. The novice was continuously evaluated by an experienced ultrasonographer who scored the images and provided advice on improving technical skills and image quality. The novice was a rheumatologist with no prior MSUS experience and a basic anatomical knowledge. The total time spent by the tutor on the process was 500 min. This clearly demonstrates how time-efficient basic training can be performed but the authors correctly point out that the development of diagnostic MSUS skills would require a period of further supervised training. This could also be accelerated through interactive teaching resources.

Is MSUS reproducible?

A key concern of rheumatologists wishing to train in MSUS is the high degree of operator dependence of the technique with consequent problems of a prolonged learning curve and poor standardization. As already detailed, an agreed programme of supervised training and the wider availability of MSUS can allow the trainee to more rapidly reach a competent level of MSUS. A high degree of interobserver agreement can be achieved for the detection of finger and toe joint synovitis and erosion [24] and on normal hip and hip effusion [25] by rheumatologists with limited ultrasound training as compared with more experienced ultrasonographers. It will be important to emphasize that the learning curve is almost endless, not just for trainees but also for the authors of this paper! This is true of all fields of clinical medicine and the rheumatologist who performs MSUS needs to be aware of their limitations. Continuous development of MSUS skills can be achieved by assessing the MSUS findings in the context of the whole clinical examination and not just in isolation, by constantly engaging with other practitioners of MSUS and by referring when appropriate to other imaging modalities.

MSUS equipment requirements and future developments

What MSUS system is suitable for a rheumatologist?

The correct selection of MSUS equipment is critical in facilitating the introduction of MSUS into rheumatology practice and for ease of training in MSUS. The important considerations in selecting sonographic equipment for MSUS are cost, image resolution and quality, transducer design, equipment size/portability and colour/power Doppler option. The cost of ultrasound equipment directly relates to image resolution and quality. A high-resolution system with superior imaging definition produces high-quality images that are easier to interpret. However, a high-quality, high-resolution system can cost from £30,000 to £130,000. Significant reductions in cost can be obtained by programming the system solely for musculoskeletal imaging. Small portable systems are less expensive (∼£15,000), produce images of sufficient quality and can be easily used at the bedside. But the smaller screen images are more difficult to interpret for the less experienced ultrasonographer. In the authors’ experience the ideal combination is to have access to a larger, high-resolution system for training and research purposes and for ‘difficult cases’ while a smaller portable system is sufficient for the majority of everyday clinical practice undertaken by the experienced ultrasonographer.

Optimizing image resolution for different articular structures

The choice of transducer used depends on the size and location of the musculoskeletal structure to be imaged. High-frequency transducers (7.5–20 MHz) have higher-resolution imaging but poor tissue penetrance, making them ideal for small and superficial structures. Low-frequency transducers (<7.5 MHz) have poorer resolution but excellent tissue penetrance and are preferable for larger and deeper structures. Ideally, MSUS equipment should have both low- and high-frequency transducers to avoid false negative MSUS examinations due to inadequate imaging. Continuous improvements in imaging definition, equipment size and portability and reductions in cost and technological innovations are expected [26] and will facilitate the development of MSUS by rheumatologists. Current MSUS equipment is already capable of a resolution power of less than 0.1 mm—a definition not achievable by computed tomography (CT) or MRI—and has been termed ‘acoustic microscopy’.

Power Doppler

Power and colour flow Doppler modalities are useful in the detection of vascularity. Power Doppler adds substantial advantages to standard MSUS because of its ability to visualize the movement of blood cells within a vessel with a particular application in detecting increased microvascular blood flow in synovial and entheseal inflammation [27, 28]. It has been demonstrated that power Doppler is of practical value in distinguishing inflammatory and infectious musculoskeletal fluid collections from those that are non-inflammatory. It appears realistic to hypothesize that this imaging technique could provide the solution to the still unsolved problem of combining high-quality morphological information with blood flow imaging.

The interpretation of power Doppler findings is highly dependent on the quality of the equipment, on technical conditions of the examination and the experience of the examiner. A careful and reproducible quantitative approach to the power Doppler signal evaluation and standardization of the examining procedure are key targets for future research. To avoid any artefacts, it is necessary to use two different planes to demonstrate increased flow in the region of interest. The lack of a good commercial phantom model for power Doppler standardization prevents direct comparison of the sensitivity and reproducibility of different MSUS systems. Computer-aided assessment of the pixel area of the synovial vessels may allow a quick and reliable quantitative estimation of the power Doppler signal [29]. Power Doppler is an exciting technique for the diagnosis and quantification of inflammatory musculoskeletal disease but requires further validation and research before it should be included as an essential feature of MSUS equipment.

Microbubble contrast agents

Intravenous microbubble echo contrast agents produce further improvements in imaging quality, particularly in the sensitivity of detection of tissue vascularity with power Doppler and in enhancing imaging of tissues that are not easily visualized by current MSUS systems. These agents have already been applied in oncology and cardiology and are currently being evaluated in inflammatory joint disease [30]. Moreover, microbubbles may act as drug delivery vehicles that can release the loaded drug after a local disruption induced by a targeted energetic wave [31].

Intravenous microbubble contrast enhancement may potentially increase the sensitivity of the standard power Doppler examination, enhancing the thickened, hypervascular and inflamed synovium. It provides a means of quantifying inflammatory disease by estimation of US signal intensity changes after an injection of contrast agent (contrast enhancement curves). The assessment of perfusion of synovial pannus may prove to be an important objective in evaluating synovitis activity and assisting clinicians in distinguishing between inflammatory and non-inflammatory pannus. A preliminary experience has shown that the areas under the time–intensity curves were correlated with the degree of knee inflammation and significantly higher in patients with clinically active synovitis than in those with inactive synovitis [32].

Three- and four-dimensional ultrasonography

Until recently ultrasound has lagged behind both CT and MRI in the area of 3D imaging. Now computing advances have resulted in 3D ultrasound imaging [33, 34] (termed 4D as it has the advantage of being performed in real time). These innovative technologies are all being currently evaluated and have the potential to see MSUS move out of the shadow of MRI in the assessment of musculoskeletal disease. In a matter of seconds, 3D sonographic pictures of a target area can be acquired allowing for an off-line, exciting virtual anatomical tour in longitudinal, transverse and coronal planes and 3D reconstruction, all at the same time. After an appropriate setting of the workstation, an experienced sonographer and a novice will take the same pictures. Moreover, 3D US has the potential to dramatically reduce the duration of MSUS examination and to improve both quality and standardization of the technique.

Three-dimensional pictures provide a spectacular and in-depth view of the small joints, are easier to understand and clearly illustrate several anatomical details that are undetectable with conventional US (Fig. 2). The main clinical indications for 3D MSUS in rheumatology could include early detection of bone erosions in small joints and a more careful assessment of enthesitis and partial tear of tendons [35]. Although the impact of 3D US on final diagnosis or monitoring of therapy has not yet been defined, it seems reasonable to predict that as technical advances continue to improve image quality, the use of 3D sonography in the diagnosis of musculoskeletal disorders will grow quickly.

Fig. 2.

Three-dimensional sonographic image of the second metacarpophalangeal joint in a patient with rheumatoid arthritis (D), compared with the longitudinal (A), transverse (B) and coronal views of the same area. Bone erosion (°) and synovial proliferation are clearly evident. m = metacarpal head; p = proximal phalanx (Voluson 730–Expert’, General Electric Medical Systems, Milwaukee, WI, USA).

Fig. 2.

Three-dimensional sonographic image of the second metacarpophalangeal joint in a patient with rheumatoid arthritis (D), compared with the longitudinal (A), transverse (B) and coronal views of the same area. Bone erosion (°) and synovial proliferation are clearly evident. m = metacarpal head; p = proximal phalanx (Voluson 730–Expert’, General Electric Medical Systems, Milwaukee, WI, USA).

Future challenges and developments

MSUS is already routinely used by a minority of rheumatologists throughout Europe for proven clinical indications in diagnosis, monitoring and intervention. MSUS in rheumatology is gaining increased acceptance, with formal training being offered by the British Society for Rheumatology, the American College of Rheumatology and the European League Against Rheumatism. It is vital that rheumatologists take a leading role in the development of MSUS within their speciality in a number of critical areas. Agreement on training and certification is essential to legitimize the training of new MSUS practitioners. Rheumatologists must produce high-quality research to standardize sonographic scoring of inflammation and damage and to further validate the role of MSUS in rheumatological practice.

Finally, rheumatologists should endeavour to cooperate with radiologists in the development of MSUS. Both have valuable expertise in technology and clinical pathology and can play complementary roles in the development of MSUS, particularly in the introduction of expensive and innovative ultrasound technologies. The challenge for the future is to integrate high-resolution power Doppler and 3D technology into the next generation of US systems. It seems realistic to predict that the range of clinical applications of these MSUS systems will greatly expand over the next few years. The increasing demand for imaging coupled with an increasing prevalence of musculoskeletal disease in an ageing population means that there will be more than enough MSUS work for both rheumatologists and radiologists in the future.

Dr Balint's work was supported by the Hungarian Medical Research Council (grant number XI.281).

The other authors have declared no conflicts of interest.

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Author notes

School of Clinical and Medical Sciences (Rheumatology), University of Newcastle-upon-Tyne, Newcastle-upon-Tyne, UK, 13rd General and Paediatric Rheumatology Department, National Institute of Rheumatology and Physiotherapy, Budapest, Hungary, 2Centre for Rheumatic Diseases, Glasgow Royal Infirmary, Glasgow, UK, 3Department of Rheumatology, University of Ancona, Ancona, Italy.

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