Journal Information
Vol. 14. Issue 1.
Pages 9-19 (January - February 2018)
Visits
5168
Vol. 14. Issue 1.
Pages 9-19 (January - February 2018)
Original Article
Full text access
Recommendations for the Use of Ultrasound and Magnetic Resonance in Patients With Rheumatoid Arthritis
Recomendaciones para el uso de la ecografía y la resonancia magnética en pacientes con artritis reumatoide
Visits
5168
Ingrid Möllera, Estibaliz Lozab,
Corresponding author
, Jacqueline Usonc, Carlos Acebesd, Jose Luis Andreue, Enrique Batllef, Ángel Buenog, Paz Colladoh, Juan Manuel Fernández-Gallardoi, Carlos Gonzálezj, Mercedes Jiménez Palope, María Pilar Lisbonak,, Pilar Macarrónl, Joan Maymóm, Jose Antonio Narváezn, Victoria Navarro-Compáno, Jesús Sanze, M. Piedad Rosariop, Esther Vicenteq, Esperanza Naredoj
a Servicio de Reumatología, Instituto Poal de Reumatología, Barcelona, Spain
b Instituto de Salud Musculoesquelética, Madrid, Spain
c Servicio de Reumatología, Hospital Universitario de Móstoles, Madrid, Spain
d Servicio de Reumatología, Hospital General de Villalba, Collado Villalba, Madrid, Spain
e Servicio de Reumatología, Hospital Universitario Puerta de Hierro, Majadahonda, Madrid, Spain
f Servicio de Reumatología, Hospital Universitario Sant Joan d’Alacant, Alicante, Spain
g Servicio de Radiología, Hospital Universitario Fundación Alcorcón, Alcorcón, Madrid, Spain
h Servicio de Reumatología, Hospital Universitario Severo Ochoa, Leganés, Madrid, Spain
i Servicio de Radiología, Hospital Universitario Severo Ochoa, Madrid, Spain
j Servicio de Reumatología, Hospital General Universitario Gregorio Marañón, Madrid, Spain
k Hospital del Mar, Barcelona, Spain
l Servicio de Reumatología, Hospital Universitario Clínico San Carlos, Madrid, Spain
m Servicio de Reumatología, Hospital del Mar, Barcelona, Spain
n Servicio de Radiodiagnóstico, Hospital Universitario de Bellvitge, L’Hospitalet de Llobregat, Barcelona, Spain
o Servicio de Reumatología, Hospital Universitario La Paz, idiPaz, Madrid, Spain
p Servicio Andaluz de Salud, Sevilla, Spain
q Servicio de Reumatología, Hospital Universitario de la Princesa, Madrid, Spain
Ver más
This item has received
Article information
Statistics
Tables (1)
Table 1. Definition of the Recommendations Together With the Level of Evidence, Grade of Recommendation and Level of Agreement, for Rheumatoid Arthritis, in Relation to Ultrasound and Magnetic Resonance Imaging.
Abstract
Objective

To develop evidence-based recommendations on the use of ultrasound (US) and magnetic resonance imaging (MRI) in patients with rheumatoid arthritis (RA).

Methods

Recommendations were generated following a nominal group technique. A panel of experts, consisting of 15 rheumatologists and 3 radiologists, was established in the first panel meeting to define the scope and purpose of the consensus document, as well as chapters, potential recommendations and systematic literature reviews (we used and updated those from previous EULAR documents). A first draft of recommendations and text was generated. Then, an electronic Delphi process (2 rounds) was carried out. Recommendations were voted from 1 (total disagreement) to 10 (total agreement). We defined agreement if at least 70% of experts voted ≥7. The level of evidence and grade or recommendation was assessed using the Oxford Centre for Evidence-based Medicine Levels of Evidence. The full text was circulated and reviewed by the panel. The consensus was coordinated by an expert methodologist.

Results

A total of 20 recommendations were proposed. They include the validity of US and MRI regarding inflammation and damage detection, diagnosis, prediction (structural damage progression, flare, treatment response, etc.), monitoring and the use of US guided injections/biopsies.

Conclusions

These recommendations will help clinicians use US and MRI in RA patients.

Keywords:
Rheumatoid arthritis
Ultrasound
Magnetic resonance
Recommendations
Resumen
Objetivo

Establecer recomendaciones, basadas en la evidencia, sobre el uso de la ecografía (US) y la resonancia magnética (RM) en pacientes con artritis reumatoide (AR)

Métodos

Las recomendaciones se consensuaron mediante metodología basada en grupos nominales. Un grupo de expertos (15 reumatólogos y 3 radiólogos) definió el alcance, usuarios, apartados del documento, posibles recomendaciones, revisiones sistemáticas a realizar (se utilizaron y actualizaron las revisiones de documentos de consenso previos de EULAR), y de la asignación de tareas. Los expertos delimitaron los apartados y redactaron las recomendaciones. El nivel de evidencia y grado de recomendación se realizó utilizando el sistema del Center for Evidence Based Medicine de Oxford. El grado de acuerdo se estableció mediante un Delphi a 2 rondas. Las recomendaciones se votaron según una escala de 1 (total desacuerdo) a 10 (total acuerdo), definiéndose el acuerdo como una puntuación ≥ 7 por al menos el 70% de los participantes. El documento completo fue revisado por los expertos y el proyecto coordinado por un metodólogo experto.

Resultados

Se emitieron 20 recomendaciones que cubren: la validez de la US y RM para la detección de actividad y daño estructural, capacidad diagnóstica, predictora (de progresión de daño estructural, de brote de la enfermedad, respuesta al tratamiento, etc.), utilidad en la evaluación y monitorización de estos pacientes que están en tratamiento, y uso de la US como guía (para infiltraciones o biopsias).

Conclusiones

Se presentan recomendaciones útiles para el manejo de la US y RM por los clínicos en pacientes con AR.

Palabras clave:
Artritis reumatoide
Ecografía
Resonancia magnética
Recomendaciones
Full Text
Introduction

Ultrasound (US) and magnetic resonance imaging (MRI) are highly useful in the daily clinical practice of rheumatologists, both in the diagnosing process and in the therapeutic management of inflammatory diseases, among them, rheumatoid arthritis (RA). The development of new drugs and the establishment of criteria for better control of the inflammatory activity in this disease have led to a marked change in the utilization of the two techniques in the routine management of RA patients.1 The reason for this change lies in both their ability to detect inflammation (with the possibility of intensifying the treatment and avoiding or reducing irreversible structural damage) and the increasing incorporation of US and the greater accessibility of MRI studies on the part of rheumatology departments.

Ultrasound has a great advantage in the fact that it can be performed at the point of care. This enables the immediate comparison with clinical data and findings from other studies in cases of diagnostic suspicion or doubts. As a consequence, it is essential to facilitate programmed learning according to a competitive curriculum for US in rheumatology, to gain access to a medium or high-range US machine and to become familiar with the settings. Magnetic resonance imaging may not be as accessible as US in rheumatology departments, but it is a highly useful imaging technique, both for diagnosis and for patient follow-up.

The incorporation of these imaging techniques into clinical practice should be based on valid scientific criteria, judgment and feasibility. Therefore, the main objective of this project was to draw up recommendations on the use of US and MRI in RA, based on the best available evidence, which serves as a reference for all of the professionals involved in caring for patients with rheumatic diseases. Our proposal was to reduce the variability in the use of these imaging techniques and to close the gaps between clinical practice and the best scientific evidence.

Material and Methods

The preparation of this document was an initiative of the Working Group on Ultrasound of the Spanish Society of Rheumatology (ECOSER). The purpose of the present article was to provide recommendations concerning the use of US and MRI in RA patients. The development involved the utilization of the Delphi method and the nominal group technique.2 The entire process of writing the document was performed through the distribution of tasks and comments among those participating, with the additional aid of several consensus documents published by the European League Against Rheumatism (EULAR) and the critical evaluation and the subsequent update of their systematic literature reviews (SLR).3–5 The process and final document were reviewed and validated by the Spanish Society of Rheumatology (SER).

Selection of the Panel and Assignment of Tasks

The first step was the formation of a panel of 18 experts (15 rheumatologists and 3 radiologists), selected through a search in MEDLINE for Spanish professionals with publications in indexed journals on the utilization of US and/or MRI in RA. The panel was constituted on the basis of the results of that search, the demonstrated experience of the professionals and their interest in the subject, also taking into account criteria concerning geographic representativeness. The entire process was coordinated by a methodologist with demonstrated experience in the Delphi method and SLR.

In the first meeting of the nominal group, the clinical questions to be developed were selected and the scope, objectives and sections of the document were decided. The clinical questions were formulated following the PICO format: patient, intervention, comparison and outcome. It was ultimately decided to carry out the SLR on different aspects of US and MRI in RA, and postpone the assignment of tasks to the panelists until the results of the SLR had been obtained. Given that these clinical questions had been previously formulated in the abovementioned EULAR consensus documents, it was decided that they be critically evaluated and updated.

Systematic Literature Reviews

The critical evaluation and updating of the SLR were performed with the help of an expert Spanish documentalist. For this, we contacted those responsible for carrying out the SLR of the consensus documents published by EULAR on RA, to evaluate the questions and search strategies.3 The evidence tables and conclusions were also critically evaluated. In the SLR of that EULAR document, we screened for the following bibliographic databases: MEDLINE (from inception to June 2011), EMBASE (from inception to June 2011) and Cochrane Library (from inception to June 2011). The present document was updated from those dates to December 2014. Subsequently, using clinical queries, the bibliography was updated to May 2015. The search strategies of the EULAR documents were constructed combining terms in MeSH-like subject headings and free text, in order to improve and achieve a balance between the sensitivity and specificity. The expert documentalist evaluated them and considered them suitable, but introduced certain new terms to improve their yield. The inclusion and exclusion criteria were those used for the EULAR document. Regardless of the evidence tables of said document, which were considered suitable, we began with the selection of articles with the search completed (that corresponding to the EULAR document and that of the update). The process of selecting the articles (using a reference manager) was done by 2 independent reviewers (the SLR were distributed by pairs, for a total of 11 for 3 reviewers—EL, GM and FG), who also analyzed in detail the articles retrieved with the search strategies, utilizing a data collection form designed for that purpose. The methodological quality of the studies included was evaluated using the Quality Assessment of Diagnostic Accuracy Studies (QUADAS) tool6 and that of the Centre for Evidence-Based Medicine of Oxford,7 and a series of questions to evaluate the risk of biases and the applicability of the studies. In the end, we analyzed the level of evidence (LE) and the level of agreement (LA) of each of the studies using the Oxford criteria because of the large volume of studies and the heterogeneity of the aspects evaluated (diagnosis, monitoring, etc.). The results of the SLR were also employed to establish the grade of recommendation (GR). All of the information in the studies was extracted from evidence tables. This entire process was supervised by an expert methodologist and 2 rheumatologists who were expert in the use of these imaging techniques.

Delphi Study

The different sections of the document were distributed among the members of the panel who were to draw them up and prepare them for the corresponding recommendation(s). They received a report of the results of the corresponding SLR to provide support for their drafts. Once drawn up and edited, the recommendations underwent the evaluation of the LA by means of a Delphi survey. For this, we sent the panelists an online questionnaire (http://www.surveymonkey.com) with the complete recommendations, together with the necessary instructions for voting by sending their LA for each of them (first Delph round). The LA was assessed by voting using a Likert scale from 1 (totally in disagreement) to 10 (totally in agreement), and agreement was defined by a score ≥7 voted by at least 70% of the participants. The overall results of the Delphi were sent to all of the panelists (modified Delphi). The recommendations with a LA of less than 70% were reedited and voted in a second round, in pertinent cases. In the first round, it was also possible to include new recommendations to eventually be voted in the second round.

Edition of the Final Document

Once the Delphi study was completed, the sections and recommendations were integrated and edited. The complete document was then sent to the group of panelists for the introduction of the corrections and the necessary comments, which resulted in a final report for the preparation of the definitive document. The methodologist participated in the assignment of each of the recommendations, the LE and the GR according to the Centre for Evidence-Based Medicine of Oxford,7 and the LA (from Delphi). Once the process was concluded, everything was sent to 2 external reviewers, a clinical rheumatologist and a medical epidemiologist with extensive experience in the validation of imaging techniques.

Results

The recommendations generated, which appear in Table 1, are described below.

Table 1.

Definition of the Recommendations Together With the Level of Evidence, Grade of Recommendation and Level of Agreement, for Rheumatoid Arthritis, in Relation to Ultrasound and Magnetic Resonance Imaging.

Recommendations  LE; GR; LA 
The use of US should be considered for the detection of synovitis in RA patients in whom the results of physical examination are questionable or negative  LE 2a; GR B; LA 80% 
MRI can be utilized to evaluate inflammatory activity in RA  LE 2a; GR B; LA 80% 
It is recommended that patients with RA and neurological and/or radiological symptoms indicative of cervical instability undergo MRI of the cervical spine  LE 3a; GR B-C; LA 87% 
US can be utilized rather than plain radiography to detect erosions in accessible small joints of hands and feet  LE 2b; GR B; LA 100% 
MRI can be utilized to detect erosions in patients with normal radiological findings, especially in early RA  LE 2a-b; GR B; LA 93% 
MRI can be utilized, if necessary, to detect structural damage of cartilage and tendons in RA patients  LE 2b; GR B-C; LA 93% 
US (presence and grade of synovitis in GS and Doppler mode, like the presence of erosions) is a useful aid in the diagnosis of RA, together with the clinical, analytical and radiological evaluation  LE 2a; GR B; LA 100% 
US examination for diagnostic purposes should include at least the wrists and MCP and MTP joints, especially the 5th (target of early erosions)  LE 2a; GR B; LA 100% 
US can be useful in RA for the differential diagnosis with regard to other inflammatory arthritides, such as psoriatic arthritis or crystal arthropathy  LE 5; GR D; LA 87% 
10  MRI can contribute to the diagnosis of RA in patients with undifferentiated arthritis in whom the differential diagnosis is of special relevance, for example, in cases of negative autoantibodies and possible nonautoimmune/inflammatory arthritis  LE 2b; GR B-C; LA 80% 
11  US data (especially the presence of a synovial Doppler signal, but synovial proliferation as well, in GS images of joints and tendon sheaths, and of erosions) can be more useful for predicting the development and/or progression of radiological damage in RA (early or established) than routine clinical evaluation  LE 2a; GR B; LA 93% 
12  The finding in MRI of inflammation, synovitis and, above all, BME and erosions could have a greater predictive role in the prognosis of joint damage than other parameters of clinical and biological activity  LE 2a; GR B; LA 93% 
13  The US evaluation of subclinical synovitis should be considered in patients in clinical remission (according to the usual indices: [DAS28]; [SDAI]; etc.) due to its predictive role in the development of flares and/or relapses and in the progression of joint damage  LE 2a; GR B; LA 80% 
14  MRI could be utilized in patients with RA in clinical remission to check for the presence and grade of subclinical inflammation  LE 2b; GR B; LA 80% 
15  The utilization of US to monitor the therapeutic response can be performed with the same periodicity as clinical evaluation (depending on the duration of RA, the presence of factors associated with a good or poor prognosis, therapeutic changes)  LE 5; GR D; LA 80% 
16  A specific US count (number and type of joints) cannot be recommended to monitor the therapeutic response in RA; however, US evaluation should include a bilateral assessment of carpi, certain MCP, MTP and a large joint (elbow, knee or ankle)  LE 2a; GR B; LA 93% 
17  It seems reasonable to perform US monitoring in RA patients who begin or change a DMARD (synthetic or biological), in those who require an increase in the DMARD dose, or in those in whom DMARD therapy is to be reduced or discontinued  LE 2a-b; GR B: LA 80% 
18  The applicability of MRI in monitoring patients in clinical practice is very reduced, although it has been found to be sensitive to change, especially for progression of structural damage and, thus, the panel does not recommend its standardized use in the monitoring of patients  LE 5; GR D; LA 93% 
19  The use of MRI (particularly the finding of BME) could be relevant as a prognostic factor associated with severity in RA and, thus, determine the therapeutic approach in early RA  LE 2b; GR B-C; LA 87% 
20  In patients with RA, the use of US is recommended for the guidance of injections into sites in which it is difficult to gain access by means of palpation or external anatomical landmarks  LE 2b; GR B-C; LA 100% 

BME, bone marrow edema; DAS28, Disease Activity Score of 28 joints; DMARD, disease-modifying antirheumatic drugs; GR, grade of recommendation; GS, gray scale; LA, level of agreement; LE, level of evidence; MCP, metacarpophalangeal; MRI, magnetic resonance imaging; MTP, metatarsophalangeal; RA, rheumatoid arthritis; SDAI, Simple Disease Activity Index; US, ultrasound.

Utility of Ultrasound and Magnetic Resonance Imaging in the Evaluation of Inflammatory Activity

Recommendation 1. The use of ultrasound should be considered for the detection of synovitis in RA patients in whom the results of physical examination were questionable or negative (LE 2a; GR B; LA 80%).

Ultrasound provides added value for the detection of synovitis and can be highly useful in patients with questionable findings on joint examination or in cases requiring a more accurate assessment of inflammatory activity in those patients.

Synovitis detected by US (gray-scale [GS] and Doppler mode) has been found to have a good correlation with histological evidence of synovitis.8–16

When compared to MRI (as a reference method), US has been shown to have high sensitivity and specificity for the detection of synovitis in small joints.14,17–34 Sensibility is less marked in the case of tenosynovitis, although specificity is high.17,18,26,34 Magnetic resonance imaging is also more sensitive than US for the detection of synovitis in large joints.17

On the other hand, in general, study results demonstrate greater sensitivity of US for the detections of synovitis (in large and small joints) in comparison with physical examination, regardless of the duration of RA.28,32,35–43 With respect to activity markers, US has been found to have a good correlation with erythrocyte sedimentation rate14,42,44–48 and endothelial growth factor.13

Recommendation 2. Magnetic resonance imaging can be utilized to evaluate inflammatory activity in RA (LE 2a; GR B; LA 80%).

The use of MRI can be evaluated in patients with RA and inconclusive clinical activity (for example, with spinal involvement) or when the results of MRI may implicate a change in the therapeutic approach.

Synovitis detected by MRI has shown a good correlation with evidence of synovitis revealed by a histological study.16,49–56 Moreover, there is an association between the bone marrow edema (BME) observed in MRI and the presence of inflammatory cell infiltrates (osteitis) in medullary bone.51,53,57 Finally, synovitis detected by MRI is also related to clinical and biological markers of inflammatory activity.49–51,58

Like US, MRI has also been seen to be more sensitive than physical examination for the detection of synovitis and tenosynovitis in hands and feet, regardless of the duration of RA.30,58–66 The same trend appears to be observed in large joints, although the results are less conclusive, probably because we have access to a smaller number of studies.67

The authors of some reports have compared the value of high-field and low-field MRI57,66,68–71 for the detection of synovitis and/or BME in carpi and metacarpophalangeal (MCP) joints, obtaining a high LA for synovitis and somewhat less so for BME. Low-field MRI has a high specificity for synovitis and erosions (>90%), but a low-to-moderate sensitivity for BME (39%) compared to high-field scanners (68%).

Recommendation 3. It is recommended that patients with RA and neurological and/or radiological symptoms indicative of cervical instability undergo MRI of the cervical spine (LE 3a; GR B-C; LA 87%).

A number of comparative studies involving different imaging techniques at the level of the cervical spine have been reported in RA patients. However, more than 2 imaging techniques (plain radiography, computed tomography [CT] and MRI) were simultaneously compared in only 1 of them, which showed that the ability of plain radiography and CT for the detection of atlanto-axial and atlanto-occipital lesions is comparable with that of MRI, although the latter is superior because it identifies lesions of the odontoid process, providing good visualization of changes in soft tissue, which makes it possible to assess complications of the spinal cord.72 On the other hand, MRI also appears to be the best imaging approach for detecting erosions73 and is the technique of choice for evaluating the status of neural structures at that level.

Value of Ultrasound and Magnetic Resonance Imaging for the Evaluation of Joint Injury

Recommendation 4. Ultrasound can be utilized rather than plain radiography to detect erosions in accessible small joints of hands and feet (LE 2b; GR B; LA 100%).

It has been observed that US detects a larger number of bone erosions than plain radiography in accessible joints (2nd and 5th MCP, 5th metatarsophalangeal [MTP], proximal interphalangeal and cubital styloid process), both in early and established RA.17,26,28,30,32,74–87 In comparison with CT and MRI, US has been found to be more sensitive than plain radiography for the detection of erosions and its specificity is high.76–78

On the other hand, the authors of one study observed good sensitivity for the detection of erosions with US and a good relationship between their severity when compared with micro-CT of the hands, although the results of that report showed that the specificity of US was lower than that of micro-CT.88 We should point out, however, that its availability is limited both in Europe and America.

All of the evaluated studies demonstrated that US detects a higher number of patients with “erosive disease” than plain radiography, regardless of the duration of the disease.74,77,80,82–84,88–90 Finally, it has been shown that US and MRI are capable of detecting a similar number of patients with “erosive disease”, irrespective of the joints being examined (MCP and MTP).34

Recommendation 5. Magnetic resonance imaging can be utilized to detect erosions in patients with normal radiological findings, especially in early RA (LE 2a-b; GR B; LA 93%).

Magnetic resonance imaging has been found to detect a higher number of bone erosions than plain radiography, both in early and established RA.26,28,30–32,74,76,77,90–94 Moreover, it has been observed that 78% of new erosions can be visualized by MRI between 1 and 5 years earlier than by plain radiography.95

Recommendation 6. Magnetic resonance imaging can be utilized, if necessary, to detect structural damage of cartilage and tendons in RA patients (LE 2b; GR B-C; LA 93%).

It has been established that the volume of cartilage according to MRI corresponds to the histological cartilage volume.94 On the other hand, evidence of the value of MRI for visualizing tendon damage in RA is limited. The authors of one study observed that MRI had a rate of detection of tendon ruptures in the carpus of 69% and US of 75%, in comparison with surgical findings.96 In another article, the LA between MRI and US was 85% for the evaluation of complete tendon rupture in the shoulder.23

Diagnostic Value

Recommendation 7. Ultrasound (presence and grade of synovitis in GS and Doppler mode, like the presence of erosions) is, together with the clinical, analytical and radiological evaluation, a useful aid in the diagnosis of RA (LE 2a; GR B; LA 100%).

Recommendation 8. Ultrasound examination for diagnostic purposes should include at least the wrists and MCP and MTP joints, especially the 5th (target of early erosions) (LE 2a; GR B; LA 100%).

Recommendation 9. Ultrasound can be useful in RA for the differential diagnosis with regard to other inflammatory arthritides, such as psoriatic arthritis or crystal arthropathy (LE 5; GR D; LA 87%).

The presence of synovitis and erosions in US is a valuable finding for the diagnosis of RA (to differentiate healthy individuals), as is tenosynovitis, although, in the latter case, the number of studies is much smaller.97–99 On the other hand, the utility of US for the diagnosis of early undifferentiated arthritis has also been demonstrated.98 However, the results concerning the ability to discriminate between RA and other inflammatory arthritides are insubstantial.89,100,101 Nevertheless, on the basis of their experience, the members of the panel consider that US may be useful in establishing the differential diagnosis with respect to other arthritides.

Examination with US makes it possible to improve the classification of RA according to different clinical criteria (1987 American College of Rheumatology [ACR] and 2010 ACR/EULAR), as it enhances the sensitivity (0.97 vs 0.59) and has a high specificity.83,102

For the moment, there are few data on the minimum number of joints that should be examined for diagnostic purposes, although the best results have be obtained with the MCP joints.103

The sensitivity and specificity of US for the diagnosis of RA vary depending on the US criteria employed: sensitivity is greater for synovitis utilizing GS images, whereas the highest specificity is found with Doppler synovitis.102,104 We should also point out that the specificity of GS examination has been reported to increase when utilizing the criteria of synovitis of a higher grade.105 On the other hand, erosion detected by US has been seen to have a moderate sensitivity (although higher than that of plain radiography), with an excellent specificity for the diagnosis of RA.103,105

The results of multivariate analysis carried out in 2 studies confirmed the role of US (synovitis in the hands) as an independent predictor of the diagnosis of RA.106,107

At the present time, although we have no clear data on the value of US in the differential diagnosis in the different types of arthritides, on the basis of their experience, the members of the panel consider that it could be useful in that respect.

Recommendation 10. Magnetic resonance imaging can contribute to the diagnosis of RA in patients with undifferentiated arthritis in whom the differential diagnosis is of special relevance, for example, in cases of negative autoantibodies and possible nonautoimmune/inflammatory arthritis (LE 2b; GR B-C; LA 80%).

Magnetic resonance imaging has an adequate sensitivity, specificity and ability to discriminate a diagnosis of RA (versus healthy individuals),17,108 but the results were not consistent enough to differentiate RA from other inflammatory arthritides.109–112 However, on the basis of their experience and data reported in the medical literature, the members of the panel considered that the pattern of inflammation detected with MRI may be characteristic and, thus, help to differentiate between RA and other inflammatory arthritides.110–112

Like US, MRI enhances the discriminative ability of the clinical classification criteria for RA (1987 ACR and 2010 ACR/EULAR).104,113

Finally, we wish to point out that symmetrical synovitis of the hands is the most important MRI parameter for the diagnosis of RA, followed by BME and the erosions.109

Prognostic Value

Recommendation 11. Ultrasound data (especially the presence of a synovial Doppler signal, but synovial proliferation as well, in GS images of joints and tendon sheaths, and of erosions) can be more useful for predicting the development and/or progression of radiological damage in RA (early or established) than routine clinical evaluation (LE 2a; GR B; LA 93%).

The value of US synovitis, particularly that detected by Doppler, in predicting the development and/or progression of structural damage (radiographic of up to at least 3 years) is greater than that of clinical synovitis and comparable with that of MRI.114–119

It has specifically been demonstrated that US synovitis (in GS images and Doppler study) predicts structural damage, in both early and established RA, in patients being treated with disease-modifying antirheumatic drugs (DMARD) or biological agents, and in joints in which US activity is maintained or in which subclinical US synovitis is detected. At this moment, we have insufficient data to establish a cutoff point for the grade of US synovitis that would enable us to predict structural damage, although, generically, the presence of baseline erosions detected by US may predict structural damage.114

On the other hand, at the present time, we can offer little evidence related to the ability to predict structural damage in tenosynovitis identified by US in RA patients.120,121

Recommendation 12. The finding in MRI of inflammation, synovitis and, above all, BME and erosions could have a greater predictive role in the prognosis of joint damage than other parameters of clinical and biological activity (LE 2a; GR B; LA 93%).

It has been shown that the finding in MRI of BME predicts the progression of structural damage (radiographic, evaluated by CT or MRI) in RA.122–131

A number of studies have demonstrated that the predictive ability of synovitis and baseline erosions in MRI, in terms of the progression of short-term and long-term structural damage, in early and established RA, is superior to that of other clinical and laboratory parameters.71,116,126,130,132–137

Evidence of tenosynovitis of the hands in MRI as a predictor of structural damage is less conclusive.66,116,125,127,128 Nevertheless, there are findings that suggest a certain predictive role of tendon rupture seen in MRI over the medium term (1 year) (126) and long term (6 years).138

The presence and size of the erosions in MRI predict the development of new erosions and progression of existing erosions, detected by plain radiography or by MRI, in both early and established RA.14,116,117,122–124,131–133

It has also been observed that the lower values corresponding to inflammation scores in MRI (synovitis, BME and tenosynovitis) and the absence of BME, erosions and synovitis in MRI, have a high negative predictive value (>0.90) in terms of the structural damage detected by radiography or by MRI.129,130,137

There are preliminary data139 that indicate that BME and baseline synovitis may predict progression of cartilage damage in MRI observed in carpus at 3 years. Thus, they could be useful in predicting long-term functional status.140,141 Further studies must be carried out to define this point more precisely.

Remission

Recommendation 13. The US evaluation of subclinical synovitis should be considered in patients in clinical remission (according to the usual indices: Disease Activity Score of 28 joints [DAS28]; Simple Disease Activity Index [SDAI]; etc.) due to its predictive role in the development of flares and/or relapses and in the progression of joint damage (LE 2a; GR B; LA 80%).

Ultrasound can provide added value to physical examination in patients with RA in remission. The identification of synovial hypertrophy in the US study (GS [35%–98.4%] and Doppler activity [17%–93.3%]) in RA patients in clinical remission occurs more frequently in established disease than in early disease, even in clinically silent joints.142–152 Subclinical synovitis detected in Doppler mode may predict the development of relapses or new flares over the short-to-medium term,144,148 as well as progression of the structural damage.146,148,153

There is a good correlation between different models of US evaluation, comprehensive and reduced, in patients with RA in clinical remission.142

Recommendation 14. Magnetic resonance imaging could be utilized in patients with RA in clinical remission to check for the presence and grade of subclinical inflammation (LE 2b; GR B; LA 80%).

Magnetic resonance imaging detects subclinical inflammation (synovitis and/or BME) in carpi and MCP in patients with RA in remission (defined according to distinct criteria), in an elevated percentage of evaluated patients and joints (synovitis between 87% and 96.2%, BME between 23% and 53% and tenosynovitis between 20.8% and 46.8%).71,146–148,154–158

Preliminary data indicate that synovitis, possibly BME and tenosynovitis identified by MRI may predict the progression of structural damage (radiographic damage in hands and feet or of the hands) in RA patients in clinical remission.146,148,154 In fact, cutoff points have been established in MRI scoring to differentiate levels of risk of radiographic progression in patients with RA in remission with subclinical inflammation.155 On the other hand, however, there is presently limited evidence on the value of MRI for predicting relapses.148

Evaluation/monitoring of the Therapeutic Response

Recommendation 15. The utilization of US to monitor the therapeutic response can be performed with the same periodicity as clinical evaluation (depending on the duration of RA, the presence of factors associated with a good or poor prognosis, therapeutic changes) (LE 5; GR D; LA 80%).

Recommendation 16. A specific US count (number and type of joints) cannot be recommended to monitor the therapeutic response in RA; however, US evaluation should include a bilateral assessment of carpi, certain MCP, MTP and a large joint (elbow, knee or ankle) (LE 2a; GR B; LA 93%).

Recommendation 17. It seems reasonable to perform US monitoring in RA patients who begin or change a DMARD (synthetic or biological), in those who require an increase in the DMARD dose, or in those in whom DMARD therapy is to be reduced or discontinued (LE 2a-b; GR B; LA 80%).

Ultrasound synovitis (in GS images or Doppler mode) is sensitive to change that is at least similar to that produced by clinical examination and to that induced by other laboratory parameters related to inflammation.37,117,121,159–165 On the other hand, it has been observed that sensitivity to change of US synovitis is the same in RA patients with different treatment modalities (synthetic or biological DMARD, biological therapies, as first-line approach, with treatment switches, etc.), regardless of the disease activity and disease duration.121

At the present time, we have little data on the utility of US for monitoring erosions because of a lack of consistent evidence, although some authors indicate that it could be as sensitive to change as plain radiography, which would mean that it could be a useful tool for patient monitoring.71,166

Different systems have been utilized for US joint evaluation for monitoring RA patients: comprehensive, reduced and composite clinical-laboratory US indices.119,161,167–170 However, to date, there is insufficient evidence to specifically recommend one or another.

Recommendation 18. The applicability of MRI in monitoring patients in clinical practice is very reduced, although it has been found to be sensitive to change, especially for progression of structural damage and, thus, the panel does not recommend its standardized use in the monitoring of patients (LE 5; GR D; LA 93%).

According to some authors, MRI is sensitive to changes in patients with RA and different treatment modalities.162,171,172 The results of another study have shown that low baseline scores and early reduction (at 12 and 24 weeks) of synovitis and BME in MRI of the hand after treatment with a biological DMARD is associated with less marked radiographic progression at 1 and 2 years.131

Recommendation 19. The use of MRI (particularly the finding of BME) could be relevant as a prognostic factor associated with severity in RA and, thus, determine the therapeutic approach in early RA (LE 2b; GR B-C; LA 87%).

In some studies, baseline BME was the only independent predictor of progression of radiographic structural damage after 2 and 5 years of follow-up in multivariate analyses.122,123 Another article also demonstrated that BME (defined as a score >2 in the Rheumatoid Arthritis Magnetic Resonance Imaging Score [RAMRIS]) is an independent predictor of damage progression (radiographic and in MRI),128 a finding also observed in another report in which BME was a predictor of progression of structural damage in MRI.129 In this case, is was also shown that the development of radiological erosions at 1 year was not very probable in the absence of baseline inflammation in MRI (negative predictive value of 0.92).

Prediction of Response to Treatment

There is insufficient data on the predictive role of US and MRI in the response to therapy of RA patients.173

Guided Injection

Recommendation 20. In patients with RA, the use of US is recommended for the guidance of injections into sites in which it is difficult to gain access by means of palpation or external anatomical landmarks (LE 2b; GR B-C; LA 100%).

It has been demonstrated that US-guided injection is more precise for achieving the objective (making it easier to reach the intended site) than that oriented exclusively by palpation or external anatomical landmarks (verified in shoulder, elbow carpus, knee and ankle). However, to date, we have little evidence concerning the efficacy (in terms of outcome variables like pain or inflammation) of US-guided injection in RA patients as compared to the other approach.174–179 In this respect, the members of the panel consider that its use be recommended, as it facilitates the work of the physician and, if it is easier to gain access to the injection site with US guidance, the results should be better, at least, theoretically, than if the injection is performed without guidance.

Discussion

These are the first recommendations with the participation of the SER on the use of US and MRI in RA in clinical practice. Its support is based on the best evidence currently available.

Ultrasound and MRI were introduced into clinical practice and clinical trials as ancillary tests, together with the clinical parameters of RA; this affirmation is especially evident in the case of US, since its performance is mostly in the hands of the clinicians themselves. The most important added value provided by these techniques is their higher sensitivity for the detection of synovitis and structural damage as compared to standard clinical evaluation and plain radiography. On the other hand, although, in recent years, publications on the metric properties of the two techniques (validity, reliability and sensitivity to change) and on their diagnostic and predictive value have proliferated, at the present time, they will need to be defined and a consensus reached on their use in rheumatology clinical practice.

Therefore, for the purpose of improving clinical practice, we must establish explicit recommendations that encompass aspects as important as the diagnosis or monitoring of treatment. Although it is certain that the evidence is insufficient in certain areas, this document provides a series of highly relevant recommendations that can be especially useful for clinicians.

Ethical DisclosuresProtection of human and animal subjects

The authors declare that no experiments were performed on humans or animals for this investigation.

Confidentiality of data

The authors declare that no patient data appears in this article.

Right to privacy and informed consent

The authors declare that no patient data appear in this article.

Funding

Financed by the Extraordinary Professorship accorded by the Universidad Complutense de Madrid and Merck Sharp & Dohme (UCM/MSD): Prof. Luis Carreño in Autoimmune Inflammatory Diseases.

Conflicts of Interest

Esperanza Naredo has received fees for presentations from Abbvie, Roche Farma, Bristol-Myers Squibb, Pfizer, UCB and Novartis.

Estíbaliz Loza has received fees for research projects from Abbvie, Roche Farma, Bristol-Myers Squibb, Pfizer, MSD, UCB, Sanofi-Aventis and Novartis.

Paz Collado has received fees for presentations from Abbvie and Pfizer.

Enrique Batlle has received fees for presentations, courses, projects and/or has worked as a consultant for Abbvie, BMS, Lilly, Menarini, MSD, Pfizer, Roche, UCB, Menarini and the Spanish Foundation of Rheumatology (FER).

Victoria Navarro-Compán has received fees for presentations and for research projects from Abbvie, BMS, MSD, Novartis, Pfizer, Roche, UCB, SER and ASAS group.

Esther Vicente has received fees for presentations from Abbvie, Roche Farma, Bristol-Myers Squibb, Pfizer, UCB, ROVI and MSD.

M. Pilar Macarrón has received fees for presentations from Abbvie, Roche Farma, Bristol-Myers Squibb, Pfizer, MSD and UCB.

Carlos Acebes has received fees for presentations from Tedec-Meiji Farma.

The remaining authors declare they have no conflicts of interest.

Acknowledgments

This report is supported by the SER.

The panel wishes to thank M. Piedad Rosario for her assistance in the critical evaluation of the systematic reviews referred to in this project; Susana García and Jose Miguel Carrasco for helping with the coordination of the initial stages of the project; Teresa Otón and M. Jesús García de Yébenes for their external review; and Petra Díaz del Campo for her enormous assistance in evaluating all of the documentation, as well as for her suggestions and corrections.

References
[1]
J.S. Smolen, F.C. Breedveld, G.R. Burmester, V. Bykerk, M. Dougados, P. Emery, et al.
Treating rheumatoid arthritis to target: 2014 update of the recommendations of an international task force.
Ann Rheum Dis, 75 (2016), pp. 3-15
[2]
N. Black, M. Murphy, D. Lamping, M. McKee, C. Sanderson, J. Askham, et al.
Consensus development methods: a review of best practice in creating clinical guidelines.
J Health Serv Res Policy, 4 (1999), pp. 236-248
[3]
A.N. Colebatch, C.J. Edwards, M. Ostergaard, D. van der Heijde, P.V. Balint, M.A. D’Agostino, et al.
EULAR recommendations for the use of imaging of the joints in the clinical management of rheumatoid arthritis.
Ann Rheum Dis, 72 (2013), pp. 804-814
[4]
P. Mandl, V. Navarro-Compan, L. Terslev, P. Aegerter, D. van der Heijde, M.A. D’Agostino, et al.
EULAR recommendations for the use of imaging in the diagnosis and management of spondyloarthritis in clinical practice.
Ann Rheum Dis, 74 (2015), pp. 1327-1339
[5]
A.N. Colebatch-Bourn, C.J. Edwards, P. Collado, M.A. d’Agostino, R. Hemke, S. Jousse-Joulin, et al.
EULAR-PReS points to consider for the use of imaging in the diagnosis and management of juvenile idiopathic arthritis in clinical practice.
Ann Rheum Dis, 74 (2015), pp. 1946-1957
[6]
P.F. Whiting, A.W. Rutjes, M.E. Westwood, S. Mallett, J.J. Deeks, J.B. Reitsma, et al.
QUADAS-2: a revised tool for the quality assessment of diagnostic accuracy studies.
Ann Intern Med, 155 (2011), pp. 529-536
[7]
CEBM.
Medicine. CfEB. CEBM Levels of Evidence 2011: University of Oxford.
(2011),
[accessed 11.04.13]. Available from: http://www.cebm.net/index.aspx?o=1025
[8]
E. Alasaarela, J. Leppilahti, M. Hakala.
Ultrasound and operative evaluation of arthritic shoulder joints.
Ann Rheum Dis, 57 (1998), pp. 357-360
[9]
Z. Karim, R.J. Wakefield, M. Quinn, P.G. Conaghan, A.K. Brown, D.J. Veale, et al.
Validation and reproducibility of ultrasonography in the detection of synovitis in the knee: a comparison with arthroscopy and clinical examination.
Arthritis Rheum, 50 (2004), pp. 387-394
[10]
U. Fiocco, F. Ferro, L. Cozzi, M. Vezzu, P. Sfriso, C. Checchetto, et al.
Contrast medium in power Doppler ultrasound for assessment of synovial vascularity: comparison with arthroscopy.
J Rheumatol, 30 (2003), pp. 2170-2176
[11]
J.M. Koski, S. Saarakkala, M. Helle, U. Hakulinen, J.O. Heikkinen, H. Hermunen.
Power Doppler ultrasonography and synovitis: correlating ultrasound imaging with histopathological findings and evaluating the performance of ultrasound equipments.
Ann Rheum Dis, 65 (2006), pp. 1590-1595
[12]
M. Walther, H. Harms, V. Krenn, S. Radke, T.P. Faehndrich, F. Gohlke.
Correlation of power Doppler sonography with vascularity of the synovial tissue of the knee joint in patients with osteoarthritis and rheumatoid arthritis.
[13]
F. Vreju, M. Ciurea, A. Rosu, A. Musetescu, D. Grecu, P. Ciurea.
Power Doppler sonography, a non-invasive method of assessment of the synovial inflammation in patients with early rheumatoid arthritis.
Rom J Morphol Embryol, 52 (2011), pp. 637-643
[14]
K. Takase, S. Ohno, M. Takeno, M. Hama, Y. Kirino, A. Ihata, et al.
Simultaneous evaluation of long-lasting knee synovitis in patients undergoing arthroplasty by power Doppler ultrasonography and contrast-enhanced MRI in comparison with histopathology.
Clin Exp Rheumatol, 30 (2012), pp. 85-92
[15]
M. Andersen, K. Ellegaard, J.B. Hebsgaard, R. Christensen, S. Torp-Pedersen, P.H. Kvist, et al.
Ultrasound colour Doppler is associated with synovial pathology in biopsies from hand joints in rheumatoid arthritis patients: a cross-sectional study.
Ann Rheum Dis, 73 (2014), pp. 678-683
[16]
S. Vordenbaumen, P. Sewerin, T. Logters, F. Miese, C. Schleich, E. Bleck, et al.
Inflammation and vascularisation markers of arthroscopically-guided finger joint synovial biospies reflect global disease activity in rheumatoid arthritis.
Clin Exp Rheumatol, 32 (2014), pp. 117-120
[17]
M.F. Amin, F.M. Ismail, R.R. El Shereef.
The role of ultrasonography in early detection and monitoring of shoulder erosions, and disease activity in rheumatoid arthritis patients; comparison with MRI examination.
Acad Radiol, 19 (2012), pp. 693-700
[18]
R.J. Wakefield, P.J. O’Connor, P.G. Conaghan, D. McGonagle, E.M. Hensor, W.W. Gibbon, et al.
Finger tendon disease in untreated early rheumatoid arthritis: a comparison of ultrasound and magnetic resonance imaging.
Arthritis Rheum, 57 (2007), pp. 1158-1164
[19]
J.E. Freeston, P.G. Conaghan, S. Dass, E. Vital, E.M. Hensor, S.P. Stewart, et al.
Does extremity-MRI improve erosion detection in severely damaged joints? A study of long-standing rheumatoid arthritis using three imaging modalities.
Ann Rheum Dis, 66 (2007), pp. 1538-1540
[20]
C. Yucesoy, G. Genc, A. Bal, B. Keyik, E. Ozturk, M. Tuzun, et al.
Ultrasonographic assessment of knee in patients with rheumatoid arthritis: is it an effective imaging method for initial evaluation? [Romatoid artritli hastalarda ultrasonografik diz degerlendirimi: Baslangi{dotless}c icin etkin bir goruntuleme yontemi midir?].
Turk J Rheumatol, 26 (2011), pp. 120-126
[21]
E. Alasaarela, R. Takalo, O. Tervonen, M. Hakala, I. Suramo.
Sonography and MRI in the evaluation of painful arthritic shoulder.
Brit J Rheumatol, 36 (1997), pp. 996-1000
[22]
K.G. Hermann, M. Backhaus, U. Schneider, K. Labs, D. Loreck, S. Zuhlsdorf, et al.
Rheumatoid arthritis of the shoulder joint: comparison of conventional radiography, ultrasound, and dynamic contrast-enhanced magnetic resonance imaging.
Arthritis Rheum, 48 (2003), pp. 3338-3349
[23]
G.A. Bruyn, E. Naredo, I. Moller, C. Moragues, J. Garrido, G.H. de Bock, et al.
Reliability of ultrasonography in detecting shoulder disease in patients with rheumatoid arthritis.
Ann Rheum Dis, 68 (2009), pp. 357-361
[24]
G.A. Bruyn, C. Pineda, C. Hernandez-Diaz, L. Ventura-Rios, C. Moya, J. Garrido, et al.
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 (2010), pp. 1079-1086
[25]
M. Boesen, K. Ellegaard, L. Boesen, M.A. Cimmino, P.S. Jensen, L. Terslev, et al.
Ultrasound Doppler score correlates with OMERACT RAMRIS bone marrow oedema and synovitis score in the wrist joint of patients with rheumatoid arthritis.
Ultraschall Med, 33 (2012), pp. E166-E172
[26]
M. Backhaus, T. Kamradt, D. Sandrock, D. Loreck, J. Fritz, K.J. Wolf, et al.
Arthritis of the finger joints: a comprehensive approach comparing conventional radiography, scintigraphy, ultrasound, and contrast-enhanced magnetic resonance imaging.
[27]
M. Szkudlarek, M. Court-Payen, C. Strandberg, M. Klarlund, T. Klausen, M. Ostergaard.
Power Doppler ultrasonography for assessment of synovitis in the metacarpophalangeal joints of patients with rheumatoid arthritis: a comparison with dynamic magnetic resonance imaging.
[28]
M. Backhaus, G.R. Burmester, D. Sandrock, D. Loreck, D. Hess, A. Scholz, et al.
Prospective two year follow up study comparing novel and conventional imaging procedures in patients with arthritic finger joints.
Ann Rheum Dis, 61 (2002), pp. 895-904
[29]
M. Szkudlarek, M. Court-Payen, C. Strandberg, M. Klarlund, T. Klausen, M. Ostergaard.
Contrast-enhanced power Doppler ultrasonography of the metacarpophalangeal joints in rheumatoid arthritis.
Eur Radiol, 13 (2003), pp. 163-168
[30]
M. Szkudlarek, M. Klarlund, E. Narvestad, M. Court-Payen, C. Strandberg, K.E. Jensen, et al.
Ultrasonography of the metacarpophalangeal and proximal interphalangeal joints in rheumatoid arthritis: a comparison with magnetic resonance imaging, conventional radiography and clinical examination.
Arthritis Res Ther, 8 (2006), pp. R52
[31]
C.H. Lee, W. Srikhum, A.J. Burghardt, W. Virayavanich, J.B. Imboden, T.M. Link, et al.
Correlation of structural abnormalities of the wrist and metacarpophalangeal joints evaluated by high-resolution peripheral quantitative computed tomography, 3 Tesla magnetic resonance imaging and conventional radiographs in rheumatoid arthritis.
Int J Rheum Dis, 18 (2015), pp. 628-639
[32]
A.K. Scheel, K.G. Hermann, S. Ohrndorf, C. Werner, C. Schirmer, J. Detert, et al.
Prospective 7 year follow up imaging study comparing radiography, ultrasonography, and magnetic resonance imaging in rheumatoid arthritis finger joints.
Ann Rheum Dis, 65 (2006), pp. 595-600
[33]
N. Damjanov, G. Radunovic, S. Prodanovic, V. Vukovic, V. Milic, K. Simic Pasalic, et al.
Construct validity and reliability of ultrasound disease activity score in assessing joint inflammation in RA: comparison with DAS-28.
Rheumatology (Oxford), 51 (2012), pp. 120-128
[34]
W.A. Schmidt, B. Schicke, B. Ostendorf, A. Scherer, A. Krause, M. Walther.
Low-field MRI versus ultrasound: which is more sensitive in detecting inflammation and bone damage in MCP and MTP joints in mild or moderate rheumatoid arthritis?.
Clin Exp Rheumatol, 31 (2013), pp. 91-96
[35]
F. Salaffi, E. Filippucci, M. Carotti, E. Naredo, G. Meenagh, A. Ciapetti, et al.
Inter-observer agreement of standard joint counts in early rheumatoid arthritis: a comparison with grey scale ultrasonography—a preliminary study.
Rheumatology (Oxford), 47 (2008), pp. 54-58
[36]
T. Funck-Brentano, F. Etchepare, S.J. Joulin, F. Gandjbakch, V.D. Pensec, C. Cyteval, et al.
Benefits of ultrasonography in the management of early arthritis: a cross-sectional study of baseline data from the ESPOIR cohort.
Rheumatology (Oxford), 48 (2009), pp. 1515-1519
[37]
M. Backhaus, S. Ohrndorf, H. Kellner, J. Strunk, T.M. Backhaus, W. Hartung, et al.
Evaluation of a novel 7-joint ultrasound score in daily rheumatologic practice: a pilot project.
Arthritis Rheum, 61 (2009), pp. 1194-1201
[38]
D. Kane, P.V. Balint, R.D. Sturrock.
Ultrasonography is superior to clinical examination in the detection and localization of knee joint effusion in rheumatoid arthritis.
J Rheumatol, 30 (2003), pp. 966-971
[39]
P.P. Cheung, L. Gossec, A. Ruyssen-Witrand, C. le Bourlout, M. Mezieres, M. Dougados.
The relationship of patient-reported joints with active synovitis detected by power Doppler ultrasonography in rheumatoid arthritis.
Clin Exp Rheumatol, 31 (2013), pp. 490-497
[40]
M. Le Boedec, S. Jousse-Joulin, J.F. Ferlet, T. Marhadour, G. Chales, L. Grange, et al.
Factors influencing concordance between clinical and ultrasound findings in rheumatoid arthritis.
J Rheumatol, 40 (2013), pp. 244-252
[41]
M. Szkudlarek, M. Court-Payen, S. Jacobsen, M. Klarlund, H.S. Thomsen, M. Ostergaard.
Interobserver agreement in ultrasonography of the finger and toe joints in rheumatoid arthritis.
Arthritis Rheum, 48 (2003), pp. 955-962
[42]
C. Ribbens, B. Andre, S. Marcelis, O. Kaye, L. Mathy, V. Bonnet, et al.
Rheumatoid hand joint synovitis: gray-scale and power Doppler US quantifications following anti-tumor necrosis factor-alpha treatment: Pilot study.
Radiology, 229 (2003), pp. 562-569
[43]
G. Murayama, M. Ogasawara, T. Nemoto, Y. Yamada, S. Ando, K. Minowa, et al.
Clinical miscount of involved joints denotes the need for ultrasound complementation in usual practice for patients with rheumatoid arthritis.
Clin Exp Rheumatol, 31 (2013), pp. 506-514
[44]
E. Naredo, G. Bonilla, F. Gamero, J. Uson, L. Carmona, A. Laffon.
Assessment of inflammatory activity in rheumatoid arthritis: a comparative study of clinical evaluation with grey scale and power Doppler ultrasonography.
Ann Rheum Dis, 64 (2005), pp. 375-381
[45]
E. Naredo, F. Gamero, G. Bonilla, J. Uson, L. Carmona, A. Laffon.
Ultrasonographic assessment of inflammatory activity in rheumatoid arthritis: comparison of extended versus reduced joint evaluation.
Clin Exp Rheumatol, 23 (2005), pp. 881-884
[46]
K. Ellegaard, S. Torp-Pedersen, L. Terslev, B. Danneskiold-Samsoe, M. Henriksen, H. Bliddal.
Ultrasound colour Doppler measurements in a single joint as measure of disease activity in patients with rheumatoid arthritis—assessment of concurrent validity.
Rheumatology (Oxford), 48 (2009), pp. 254-257
[47]
S.Y. Kawashiri, A. Kawakami, N. Iwamoto, K. Fujikawa, K. Satoh, M. Tamai, et al.
The power Doppler ultrasonography score from 24 synovial sites or 6 simplified synovial sites, including the metacarpophalangeal joints, reflects the clinical disease activity and level of serum biomarkers in patients with rheumatoid arthritis.
Rheumatology (Oxford), 50 (2011), pp. 962-965
[48]
T. Watanabe, M. Takemura, M. Sato, A. Sekine, D. Fukuoka, M. Seishima, et al.
Quantitative analysis of vascularization in the finger joints in patients with rheumatoid arthritis using three-dimensional volumetric ultrasonography with power Doppler.
Clin Rheumatol, 31 (2012), pp. 299-307
[49]
H. Konig, J. Sieper, K.J. Wolf.
Rheumatoid arthritis: evaluation of hypervascular and fibrous pannus with dynamic MR imaging enhanced with Gd-DTPA.
Radiology, 176 (1990), pp. 473-477
[50]
M. Ostergaard.
Magnetic resonance imaging in rheumatoid arthritis. Quantitative methods for assessment of the inflammatory process in peripheral joints.
Dan Med Bull, 46 (1999), pp. 313-344
[51]
E. Jimenez-Boj, I. Nobauer-Huhmann, B. Hanslik-Schnabel, R. Dorotka, A.H. Wanivenhaus, F. Kainberger, et al.
Bone erosions and bone marrow edema as defined by magnetic resonance imaging reflect true bone marrow inflammation in rheumatoid arthritis.
Arthritis Rheum, 56 (2007), pp. 1118-1124
[52]
K. Gaffney, J. Cookson, S. Blades, A. Coumbe, D. Blake.
Quantitative assessment of the rheumatoid synovial microvascular bed by gadolinium-DTPA enhanced magnetic resonance imaging.
Ann Rheum Dis, 57 (1998), pp. 152-157
[53]
F.M. McQueen, A. Gao, M. Ostergaard, A. King, G. Shalley, E. Robinson, et al.
High-grade MRI bone oedema is common within the surgical field in rheumatoid arthritis patients undergoing joint replacement and is associated with osteitis in subchondral bone.
Ann Rheum Dis, 66 (2007), pp. 1581-1587
[54]
M. Ostergaard, M. Stoltenberg, P. Lovgreen-Nielsen, B. Volck, C.H. Jensen, I. Lorenzen.
Magnetic resonance imaging-determined synovial membrane and joint effusion volumes in rheumatoid arthritis and osteoarthritis: comparison with the macroscopic and microscopic appearance of the synovium.
[55]
M.B. Axelsen, M. Stoltenberg, R.P. Poggenborg, O. Kubassova, M. Boesen, H. Bliddal, et al.
Dynamic gadolinium-enhanced magnetic resonance imaging allows accurate assessment of the synovial inflammatory activity in rheumatoid arthritis knee joints: a comparison with synovial histology.
Scand J Rheumatol, 41 (2012), pp. 89-94
[56]
S. Vordenbaumen, C. Schleich, T. Logters, P. Sewerin, E. Bleck, T. Pauly, et al.
Dynamic contrast-enhanced magnetic resonance imaging of metacarpophalangeal joints reflects histological signs of synovitis in rheumatoid arthritis.
Arthritis Res Ther, 16 (2014), pp. 452
[57]
N. Dalbeth, T. Smith, S. Gray, A. Doyle, P. Antill, M. Lobo, et al.
Cellular characterisation of magnetic resonance imaging bone oedema in rheumatoid arthritis; implications for pathogenesis of erosive disease.
Ann Rheum Dis, 68 (2009), pp. 279-282
[58]
P. Emery, D. van der Heijde, M. Ostergaard, P.G. Conaghan, M.C. Genovese, E.C. Keystone, et al.
Exploratory analyses of the association of MRI with clinical, laboratory and radiographic findings in patients with rheumatoid arthritis.
Ann Rheum Dis, 70 (2011), pp. 2126-2130
[59]
P. Goupille, B. Roulot, S. Akoka, A.M. Avimadje, P. Garaud, L. Naccache, et al.
Magnetic resonance imaging: a valuable method for the detection of synovial inflammation in rheumatoid arthritis.
J Rheumatol, 28 (2001), pp. 35-40
[60]
C. Calisir, A.I. Murat Aynaci, C. Korkmaz.
The accuracy of magnetic resonance imaging of the hands and feet in the diagnosis of early rheumatoid arthritis.
Joint Bone Spine, 74 (2007), pp. 362-367
[61]
L. Roimicher, F.P. Lopes, S.A. de Souza, L.F. Mendes, R.C. Domingues, L.M. da Fonseca, et al.
(99m)Tc-anti-TNF-alpha scintigraphy in RA: a comparison pilot study with MRI and clinical examination.
Rheumatology (Oxford), 50 (2011), pp. 2044-2050
[62]
M. Tamai, A. Kawakami, N. Iwamoto, S.Y. Kawashiri, K. Fujikawa, T. Aramaki, et al.
Comparative study of the detection of joint injury in early-stage rheumatoid arthritis by magnetic resonance imaging of the wrist and finger joints and physical examination.
Arthritis Care Res (Hoboken), 63 (2011), pp. 436-439
[63]
M.B. Axelsen, I. Eshed, A. Duer-Jensen, J.M. Moller, S.J. Pedersen, M. Ostergaard.
Whole-body MRI assessment of disease activity and structural damage in rheumatoid arthritis: first step towards an MRI joint count.
Rheumatology (Oxford), 53 (2014), pp. 845-853
[64]
K. Forslind, A. Johanson, E.M. Larsson, B. Svensson.
Magnetic resonance imaging of the fifth metatarsophalangeal joint compared with conventional radiography in patients with early rheumatoid arthritis.
Scand J Rheumatol, 32 (2003), pp. 131-137
[65]
R.J. Wakefield, J.E. Freeston, P. O’Connor, N. Reay, A. Budgen, E.M. Hensor, et al.
The optimal assessment of the rheumatoid arthritis hindfoot: a comparative study of clinical examination, ultrasound and high field MRI.
Ann Rheum Dis, 67 (2008), pp. 1678-1682
[66]
W.P. Nieuwenhuis, A. Krabben, W. Stomp, T.W. Huizinga, D. van der Heijde, J.L. Bloem, et al.
Evaluating MRI-detected tenosynovitis in the hand and wrist in early arthritis.
Arthritis Rheumatol, (2014),
[67]
K. Forslind, E.M. Larsson, K. Eberhardt, A. Johansson, B. Svensson.
Magnetic resonance imaging of the knee: a tool for prediction of joint damage in early rheumatoid arthritis?.
Scand J Rheumatol, 33 (2004), pp. 154-161
[68]
B.J. Ejbjerg, E. Narvestad, S. Jacobsen, H.S. Thomsen, M. Ostergaard.
Optimised, low cost, low field dedicated extremity MRI is highly specific and sensitive for synovitis and bone erosions in rheumatoid arthritis wrist and finger joints: comparison with conventional high field MRI and radiography.
Ann Rheum Dis, 64 (2005), pp. 1280-1287
[69]
M.F. Reiser, G.P. Bongartz, R. Erlemann, M. Schneider, T. Pauly, H. Sittek, et al.
Gadolinium-DTPA in rheumatoid arthritis and related diseases: first results with dynamic magnetic resonance imaging.
Skeletal Radiol, 18 (1989), pp. 591-597
[70]
M. Ostergaard, M. Stoltenberg, P. Lovgreen-Nielsen, B. Volck, S. Sonne-Holm, I. Lorenzen.
Quantification of synovistis by MRI: correlation between dynamic and static gadolinium-enhanced magnetic resonance imaging and microscopic and macroscopic signs of synovial inflammation.
Magn Reson Imaging, 16 (1998), pp. 743-754
[71]
F. Gandjbakhch, P.G. Conaghan, B. Ejbjerg, E.A. Haavardsholm, V. Foltz, A.K. Brown, et al.
Synovitis and osteitis are very frequent in rheumatoid arthritis clinical remission: results from an MRI study of 294 patients in clinical remission or low disease activity state.
J Rheumatol, 38 (2011), pp. 2039-2044
[72]
I. Fezoulidis, A. Neuhold, L. Wicke, G. Seidl, B. Eydokimidis.
Diagnostic imaging of the occipito-cervical junction in patients with rheumatoid arthritis. Plain films, computed tomography, magnetic resonance imaging.
Eur J Radiol, 9 (1989), pp. 5-11
[73]
M. Younes, S. Belghali, S. Kriaa, S. Zrour, I. Bejia, M. Touzi, et al.
Compared imaging of the rheumatoid cervical spine: prevalence study and associated factors.
Joint Bone Spine, 76 (2009), pp. 361-368
[74]
R.J. Wakefield, W.W. Gibbon, P.G. Conaghan, P. O’Connor, D. McGonagle, C. Pease, et al.
The value of sonography in the detection of bone erosions in patients with rheumatoid arthritis: a comparison with conventional radiography.
[75]
T. Funck-Brentano, F. Etchepare, S.J. Joulin, F. Gandjbakch, V.D. Pensec, C. Cyteval, et al.
Benefits of ultrasonography in the management of early arthritis: a cross-sectional study of baseline data from the ESPOIR cohort.
Rheumatology, 48 (2009), pp. 1515-1519
[76]
E. Alasaarela, O. Tervonen, R. Takalo, S. Lahde, I. Suramo.
Ultrasound evaluation of the acromioclavicular joint.
J Rheumatol, 24 (1997), pp. 1959-1963
[77]
M. Szkudlarek, E. Narvestad, M. Klarlund, M. Court-Payen, H.S. Thomsen, M. Ostergaard.
Ultrasonography of the metatarsophalangeal joints in rheumatoid arthritis: comparison with magnetic resonance imaging, conventional radiography, and clinical examination.
Arthritis Rheum, 50 (2004), pp. 2103-2112
[78]
M. Rahmani, H. Chegini, S.R. Najafizadeh, M. Azimi, P. Habibollahi, M. Shakiba.
Detection of bone erosion in early rheumatoid arthritis: ultrasonography and conventional radiography versus non-contrast magnetic resonance imaging.
Clin Rheumatol, 29 (2010), pp. 883-891
[79]
K. Lerch, N. Borisch, C. Paetzel, J. Grifka, W. Hartung.
Sonographic evaluation of the elbow in rheumatoid arthritis: a classification of joint destruction.
Ultrasound Med Biol, 29 (2003), pp. 1131-1135
[80]
E. Alasaarela, I. Suramo, O. Tervonen, S. Lahde, R. Takalo, M. Hakala.
Evaluation of humeral head erosions in rheumatoid arthritis: a comparison of ultrasonography, magnetic resonance imaging, computed tomography and plain radiography.
Brit J Rheumatol, 37 (1998), pp. 1152-1156
[81]
R. Klocke, D. Glew, N. Cox, D.R. Blake.
Sonographic erosions of the rheumatoid little toe.
Ann Rheum Dis, 60 (2001), pp. 896-897
[82]
C. Weidekamm, M. Koller, M. Weber, F. Kainberger.
Diagnostic value of high-resolution B-mode and doppler sonography for imaging of hand and finger joints in rheumatoid arthritis.
Arthritis Rheum, 48 (2003), pp. 325-333
[83]
R. Lopez-Ben, W.K. Bernreuter, L.W. Moreland, G.S. Alarcon.
Ultrasound detection of bone erosions in rheumatoid arthritis: a comparison to routine radiographs of the hands and feet.
Skeletal Radiol, 33 (2004), pp. 80-84
[84]
S. Bajaj, R. Lopez-Ben, R. Oster, G.S. Alarcon.
Ultrasound detects rapid progression of erosive disease in early rheumatoid arthritis: a prospective longitudinal study.
Skeletal Radiol, 36 (2007), pp. 123-128
[85]
P. Macchioni, M. Magnani, R. Mule, S. Galletti, M. Catanoso, E. Pignotti, et al.
Ultrasonographic predictors for the development of joint damage in rheumatoid arthritis patients: a single joint prospective study.
Clin Exp Rheumatol, 31 (2013), pp. 08-17
[86]
M. Klarlund, M. Ostergaard, K.E. Jensen, J.L. Madsen, H. Skjodt, I. Lorenzen.
Magnetic resonance imaging, radiography, and scintigraphy of the finger joints: one year follow up of patients with early arthritis. The TIRA Group.
Ann Rheum Dis, 59 (2000), pp. 521-528
[87]
K. Lerch, N. Borisch, C. Paetzel, J. Grifka, W. Hartung.
Proposal for a sonographic classification of target joints in rheumatoid arthritis.
Rheumatol Int, 25 (2005), pp. 215-219
[88]
S. Finzel, S. Ohrndorf, M. Englbrecht, C. Stach, J. Messerschmidt, G. Schett, et al.
A detailed comparative study of high-resolution ultrasound and micro-computed tomography for detection of arthritic bone erosions.
Arthritis Rheum, 63 (2011), pp. 1231-1236
[89]
B.J. Sheane, P. Beddy, M. O’Connor, S. Miller, G. Cunnane.
Targeted ultrasound of the fifth metatarsophalangeal joint in an early inflammatory arthritis cohort.
Arthritis Care Res (Hoboken), 61 (2009), pp. 1004-1008
[90]
U.M. Dohn, B.J. Ejbjerg, M. Court-Payen, M. Hasselquist, E. Narvestad, M. Szkudlarek, et al.
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 (2006), pp. R110
[91]
S. Agrawal, S.S. Bhagat, B. Dasgupta.
Improvement in diagnosis and management of musculoskeletal conditions with one-stop clinic-based ultrasonography.
Mod Rheumatol, 19 (2009), pp. 53-56
[92]
A. Corvetta, A. Giovagnoni, S. Baldelli, P. Ercolani, G. Pomponio, M.M. Luchetti, et al.
MR imaging of rheumatoid hand lesions: comparison with conventional radiology in 31 patients.
Clin Exp Rheumatol, 10 (1992), pp. 217-222
[93]
N.B. Gaylis, S.D. Needell, D. Rudensky.
Comparison of in-office magnetic resonance imaging versus conventional radiography in detecting changes in erosions after one year of infliximab therapy in patients with rheumatoid arthritis.
Mod Rheumatol, 17 (2007), pp. 273-278
[94]
C.G. Peterfy, C.F. van Dijke, Y. Lu, A. Nguyen, T.J. Connick, J.B. Kneeland, et al.
Quantification of the volume of articular cartilage in the metacarpophalangeal joints of the hand: accuracy and precision of three-dimensional MR imaging.
AJR Am J Roentgenol, 165 (1995), pp. 371-375
[95]
M. Ostergaard, P. Boyesen, I. Eshed, F. Gandjbakhch, S. Lillegraven, P. Bird, et al.
Development and preliminary validation of a magnetic resonance imaging joint space narrowing score for use in rheumatoid arthritis: potential adjunct to the OMERACT RA MRI scoring system.
J Rheumatol, 38 (2011), pp. 2045-2050
[96]
W.A. Swen, J.W. Jacobs, P.C. Hubach, J.H. Klasens, P.R. Algra, J.W. Bijlsma.
Comparison of sonography and magnetic resonance imaging for the diagnosis of partial tears of finger extensor tendons in rheumatoid arthritis.
Rheumatology (Oxford), 39 (2000), pp. 55-62
[97]
G.A. Kunkel, G.W. Cannon, D.O. Clegg.
Combined structural and synovial assessment for improved ultrasound discrimination of rheumatoid, osteoarthritic, and normal joints: a pilot study.
Open Rheumatol J, 6 (2012), pp. 199-206
[98]
F. Millot, G. Clavel, F. Etchepare, F. Gandjbakhch, F. Grados, A. Saraux, et al.
Musculoskeletal ultrasonography in healthy subjects and ultrasound criteria for early arthritis (the ESPOIR cohort).
J Rheumatol, 38 (2011), pp. 613-620
[99]
S. Ruta, J. Rosa, D.A. Navarta, C. Saucedo, L.J. Catoggio, R.G. Monaco, et al.
Ultrasound assessment of new onset bilateral painful shoulder in patients with polymyalgia rheumatica and rheumatoid arthritis.
Clin Rheumatol, 31 (2012), pp. 1383-1387
[100]
M. Gutierrez, E. Filippucci, S. Ruta, F. Salaffi, P. Blasetti, L. di Geso, et al.
Inter-observer reliability of high-resolution ultrasonography in the assessment of bone erosions in patients with rheumatoid arthritis: experience of an intensive dedicated training programme.
Rheumatology, 50 (2011), pp. 373-380
[101]
C.A. Scire, A. Iagnocco, G. Meenagh, L. Riente, E. Filippucci, A. Delle Sedie, et al.
Ultrasound imaging for the rheumatologist. XXXIII. Sonographic assessment of the foot in early arthritis patients.
Clin Exp Rheumatol, 29 (2011), pp. 465-469
[102]
S.Y. Kawashiri, T. Suzuki, A. Okada, S. Yamasaki, M. Tamai, H. Nakamura, et al.
Musculoskeletal ultrasonography assists the diagnostic performance of the 2010 classification criteria for rheumatoid arthritis.
Mod Rheumatol, 23 (2013), pp. 36-43
[103]
A. Filer, P. de Pablo, G. Allen, P. Nightingale, A. Jordan, P. Jobanputra, et al.
Utility of ultrasound joint counts in the prediction of rheumatoid arthritis in patients with very early synovitis.
Ann Rheum Dis, 70 (2011), pp. 500-507
[104]
M. Broll, K. Albrecht, I. Tarner, U. Muller-Ladner, J. Strunk.
Sensitivity and specificity of ultrasonography and low-field magnetic resonance imaging for diagnosing arthritis.
Clin Exp Rheumatol, 30 (2012), pp. 543-547
[105]
J.E. Freeston, R.J. Wakefield, P.G. Conaghan, E.M. Hensor, S.P. Stewart, P. Emery.
A diagnostic algorithm for persistence of very early inflammatory arthritis: the utility of power Doppler ultrasound when added to conventional assessment tools.
Ann Rheum Dis, 69 (2010), pp. 417-419
[106]
M. Chen, X. Li, P. Akhavan, C. Bombardier.
A longitudinal trivariate model of disease activity score, physical function and radiographic damage: results from sonora study.
Reumatol Clin, 7 (2011),
CM 129–74
[107]
D. Nakagomi, K. Ikeda, A. Okubo, T. Iwamoto, Y. Sanayama, K. Takahashi, et al.
Ultrasound can improve the accuracy of the 2010 American College of Rheumatology/European League against rheumatism classification criteria for rheumatoid arthritis to predict the requirement for methotrexate treatment.
Arthritis Rheum, 65 (2013), pp. 890-898
[108]
M.B. Axelsen, B.J. Ejbjerg, M.L. Hetland, H. Skjodt, O. Majgaard, U.B. Lauridsen, et al.
Differentiation between early rheumatoid arthritis patients and healthy persons by conventional and dynamic contrast-enhanced magnetic resonance imaging.
Scand J Rheumatol, 43 (2014), pp. 109-118
[109]
P.M. Machado, R. Koevoets, C. Bombardier, D.M. van der Heijde.
The value of magnetic resonance imaging and ultrasound in undifferentiated arthritis: a systematic review.
J Rheumatol, 87 (2011), pp. 31-37
[110]
N. Boutry, E. Hachulla, R.M. Flipo, B. Cortet, A. Cotten.
MR imaging findings in hands in early rheumatoid arthritis: comparison with those in systemic lupus erythematosus and primary Sjogren syndrome.
Radiology, 236 (2005), pp. 593-600
[111]
E. Solau-Gervais, J.L. Legrand, B. Cortet, B. Duquesnoy, R.M. Flipo.
Magnetic resonance imaging of the hand for the diagnosis of rheumatoid arthritis in the absence of anti-cyclic citrullinated peptide antibodies: a prospective study.
J Rheumatol, 33 (2006), pp. 1760-1765
[112]
J. Narvaez, J.A. Narvaez, M. de Albert, C. Gomez-Vaquero, J.M. Nolla.
Can magnetic resonance imaging of the hand and wrist differentiate between rheumatoid arthritis and psoriatic arthritis in the early stages of the disease?.
Semin Arthritis Rheum, 42 (2012), pp. 234-245
[113]
W. Stomp, A. Krabben, D. van der Heijde, T.W. Huizinga, J.L. Bloem, A.H. van der Helm-van Mil, et al.
Are rheumatoid arthritis patients discernible from other early arthritis patients using 1.5T extremity magnetic resonance imaging? A large cross-sectional study.
J Rheumatol, 41 (2014), pp. 1630-1637
[114]
T. Funck-Brentano, F. Gandjbakhch, F. Etchepare, S. Jousse-Joulin, A. Miquel, C. Cyteval, et al.
Prediction of radiographic damage in early arthritis by sonographic erosions and power doppler signal: a longitudinal observational study.
Arthritis Care Res (Hoboken), 65 (2013), pp. 896-902
[115]
L. Hooper, C.J. Bowen, L. Gates, D.J. Culliford, C. Ball, C.J. Edwards, et al.
Prognostic indicators of foot-related disability in patients with rheumatoid arthritis: results of a prospective three-year study.
Arthritis Care Res (Hoboken), 64 (2012), pp. 1116-1124
[116]
J.L. Hoving, R. Buchbinder, S. Hall, G. Lawler, P. Coombs, S. McNealy, et al.
A comparison of magnetic resonance imaging, sonography, and radiography of the hand in patients with early rheumatoid arthritis.
J Rheumatol, 31 (2004), pp. 663-675
[117]
T. Kamishima, K. Tanimura, M. Shimizu, M. Matsuhashi, J. Fukae, Y. Kon, et al.
Monitoring anti-interleukin 6 receptor antibody treatment for rheumatoid arthritis by quantitative magnetic resonance imaging of the hand and power Doppler ultrasonography of the finger.
Skeletal Radiol, 40 (2011), pp. 745-755
[118]
P.P. Reynolds, C. Heron, J. Pilcher, P.D. Kiely.
Prediction of erosion progression using ultrasound in established rheumatoid arthritis: a 2-year follow-up study.
Skeletal Radiol, 38 (2009), pp. 473-478
[119]
E. Naredo, P. Collado, A. Cruz, M.J. Palop, F. Cabero, P. Richi, et al.
Longitudinal power Doppler ultrasonographic assessment of joint inflammatory activity in early rheumatoid arthritis: predictive value in disease activity and radiologic progression.
Arthritis Rheum, 57 (2007), pp. 116-124
[120]
S. Lillegraven, P. Boyesen, H.B. Hammer, M. Ostergaard, T. Uhlig, S. Sesseng, et al.
Tenosynovitis of the extensor carpi ulnaris tendon predicts erosive progression in early rheumatoid arthritis.
Ann Rheum Dis, 70 (2011), pp. 2049-2050
[121]
T.M. Backhaus, S. Ohrndorf, H. Kellner, J. Strunk, W. Hartung, H. Sattler, et al.
The US7 score is sensitive to change in a large cohort of patients with rheumatoid arthritis over 12 months of therapy.
Ann Rheum Dis, 72 (2013), pp. 1163-1169
[122]
M.L. Hetland, B. Ejbjerg, K. Horslev-Petersen, S. Jacobsen, A. Vestergaard, A.G. Jurik, et al.
MRI bone oedema is the strongest predictor of subsequent radiographic progression in early rheumatoid arthritis. Results from a 2-year randomised controlled trial (CIMESTRA).
Ann Rheum Dis, 68 (2009), pp. 384-390
[123]
M.L. Hetland, K. Stengaard-Pedersen, P. Junker, M. Ostergaard, B.J. Ejbjerg, S. Jacobsen, et al.
Radiographic progression and remission rates in early rheumatoid arthritis—MRI bone oedema and anti-CCP predicted radiographic progression in the 5-year extension of the double-blind randomised CIMESTRA trial.
Ann Rheum Dis, 69 (2010), pp. 1789-1795
[124]
H.M. Lindegaard, J. Vallo, K. Horslev-Petersen, P. Junker, M. Ostergaard.
Low-cost, low-field dedicated extremity magnetic resonance imaging in early rheumatoid arthritis: a 1-year follow-up study.
Ann Rheum Dis, 65 (2006), pp. 1208-1212
[125]
P. Boyesen, E.A. Haavardsholm, M. Ostergaard, D. van der Heijde, S. Sesseng, T.K. Kvien.
MRI in early rheumatoid arthritis: synovitis and bone marrow oedema are independent predictors of subsequent radiographic progression.
Ann Rheum Dis, 70 (2011), pp. 428-433
[126]
A. Krabben, W. Stomp, J.A. van Nies, T.W. Huizinga, D. van der Heijde, J.L. Bloem, et al.
MRI-detected subclinical joint inflammation is associated with radiographic progression.
Ann Rheum Dis, 73 (2014), pp. 2034-2037
[127]
F.M. McQueen, N. Benton, D. Perry, J. Crabbe, E. Robinson, S. Yeoman, et al.
Bone edema scored on magnetic resonance imaging scans of the dominant carpus at presentation predicts radiographic joint damage of the hands and feet six years later in patients with rheumatoid arthritis.
Arthritis Rheum, 48 (2003), pp. 1814-1827
[128]
E.A. Haavardsholm, P. Boyesen, M. Ostergaard, A. Schildvold, T.K. Kvien.
Magnetic resonance imaging findings in 84 patients with early rheumatoid arthritis: bone marrow oedema predicts erosive progression.
Ann Rheum Dis, 67 (2008), pp. 794-800
[129]
F.M. McQueen, N. Stewart, J. Crabbe, E. Robinson, S. Yeoman, P.L. Tan, et al.
Magnetic resonance imaging of the wrist in early rheumatoid arthritis reveals progression of erosions despite clinical improvement.
Ann Rheum Dis, 58 (1999), pp. 156-163
[130]
M.L. Mundwiler, P. Maranian, D.H. Brown, J.M. Silverman, D. Wallace, D. Khanna, et al.
The utility of MRI in predicting radiographic erosions in the metatarsophalangeal joints of the rheumatoid foot: a prospective longitudinal cohort study.
Arthritis Res Ther, 11 (2009), pp. R94
[131]
J.F. Baker, M. Ostergaard, P. Emery, E.C. Hsia, J. Lu, D.G. Baker, et al.
Early MRI measures independently predict 1-year and 2-year radiographic progression in rheumatoid arthritis: secondary analysis from a large clinical trial.
Ann Rheum Dis, 73 (2014), pp. 1968-1974
[132]
F.M. McQueen, N. Benton, J. Crabbe, E. Robinson, S. Yeoman, L. McLean, et al.
What is the fate of erosions in early rheumatoid arthritis? Tracking individual lesions using x rays and magnetic resonance imaging over the first two years of disease.
Ann Rheum Dis, 60 (2001), pp. 859-868
[133]
M. Ostergaard, A. Duer, H. Nielsen, J.S. Johansen, E. Narvestad, B.J. Ejbjerg, et al.
Magnetic resonance imaging for accelerated assessment of drug effect and prediction of subsequent radiographic progression in rheumatoid arthritis: a study of patients receiving combined anakinra and methotrexate treatment.
Ann Rheum Dis, 64 (2005), pp. 1503-1506
[134]
M. Ostergaard, M. Hansen, M. Stoltenberg, P. Gideon, M. Klarlund, K.E. Jensen, et al.
Magnetic resonance imaging-determined synovial membrane volume as a marker of disease activity and a predictor of progressive joint destruction in the wrists of patients with rheumatoid arthritis.
[135]
A. Savnik, H. Malmskov, H.S. Thomsen, L.B. Graff, H. Nielsen, B. Danneskiold-Samsoe, et al.
MRI of the wrist and finger joints in inflammatory joint diseases at 1-year interval: MRI features to predict bone erosions.
Eur Radiol, 12 (2002), pp. 1203-1210
[136]
N. Tanaka, H. Sakahashi, S. Ishii, E. Sato, K. Hirose, T. Ishima.
Synovial membrane enhancement and bone erosion by magnetic resonance imaging for prediction of radiologic progression in patients with early rheumatoid arthritis.
Rheumatol Int, 25 (2005), pp. 103-107
[137]
P.G. Conaghan, P. O’Connor, D. McGonagle, P. Astin, R.J. Wakefield, W.W. Gibbon, et al.
Elucidation of the relationship between synovitis and bone damage: a randomized magnetic resonance imaging study of individual joints in patients with early rheumatoid arthritis.
Arthritis Rheum, 48 (2003), pp. 64-71
[138]
F. McQueen, V. Beckley, J. Crabbe, E. Robinson, S. Yeoman, N. Stewart.
Magnetic resonance imaging evidence of tendinopathy in early rheumatoid arthritis predicts tendon rupture at six years.
Arthritis Rheum, 52 (2005), pp. 744-751
[139]
F.M. McQueen, A. McHaffie, A. Clarke, A.C. Lee, Q. Reeves, B. Curteis, et al.
MRI osteitis predicts cartilage damage at the wrist in RA: a three-year prospective 3T MRI study examining cartilage damage.
Arthritis Res Ther, 16 (2014), pp. R33
[140]
N. Benton, N. Stewart, J. Crabbe, E. Robinson, S. Yeoman, F.M. McQueen.
MRI of the wrist in early rheumatoid arthritis can be used to predict functional outcome at 6 years.
Ann Rheum Dis, 63 (2004), pp. 555-561
[141]
S. Zheng, E. Robinson, S. Yeoman, N. Stewart, J. Crabbe, J. Rouse, et al.
MRI bone oedema predicts eight year tendon function at the wrist but not the requirement for orthopaedic surgery in rheumatoid arthritis.
Ann Rheum Dis, 65 (2006), pp. 607-611
[142]
E. Naredo, L. Valor, I. de la Torre, J. Martinez-Barrio, M. Hinojosa, F. Aramburu, et al.
Ultrasound joint inflammation in rheumatoid arthritis in clinical remission: how many and which joints should be assessed?.
Arthritis Care Res (Hoboken), 65 (2013), pp. 512-517
[143]
G. Sakellariou, C.A. Scire, S.M. Verstappen, C. Montecucco, R. Caporali.
In patients with early rheumatoid arthritis, the new ACR/EULAR definition of remission identifies patients with persistent absence of functional disability and suppression of ultrasonographic synovitis.
Ann Rheum Dis, 72 (2013), pp. 245-249
[144]
C.A. Scire, C. Montecucco, V. Codullo, O. Epis, M. Todoerti, R. Caporali.
Ultrasonographic evaluation of joint involvement in early rheumatoid arthritis in clinical remission: power Doppler signal predicts short-term relapse.
Rheumatology (Oxford), 48 (2009), pp. 1092-1097
[145]
J. Ramirez, V. Ruiz-Esquide, I. Pomes, R. Celis, A. Cuervo, M.V. Hernandez, et al.
Patients with rheumatoid arthritis in clinical remission and ultrasound-defined active synovitis exhibit higher disease activity and increased serum levels of angiogenic biomarkers.
Arthritis Res Ther, 16 (2014), pp. R5
[146]
A.K. Brown, P.G. Conaghan, Z. Karim, M.A. Quinn, K. Ikeda, C.G. Peterfy, et al.
An explanation for the apparent dissociation between clinical remission and continued structural deterioration in rheumatoid arthritis.
Arthritis Rheum, 58 (2008), pp. 2958-2967
[147]
A.K. Brown, M.A. Quinn, Z. Karim, P.G. Conaghan, C.G. Peterfy, E. Hensor, et al.
Presence of significant synovitis in rheumatoid arthritis patients with disease-modifying antirheumatic drug-induced clinical remission: evidence from an imaging study may explain structural progression.
Arthritis Rheum, 54 (2006), pp. 3761-3773
[148]
V. Foltz, F. Gandjbakhch, F. Etchepare, C. Rosenberg, M.L. Tanguy, S. Rozenberg, et al.
Power Doppler ultrasound, but not low-field magnetic resonance imaging, predicts relapse and radiographic disease progression in rheumatoid arthritis patients with low levels of disease activity.
Arthritis Rheum, 64 (2012), pp. 67-76
[149]
A. Balsa, E. de Miguel, C. Castillo, D. Peiteado, E. Martin-Mola.
Superiority of SDAI over DAS-28 in assessment of remission in rheumatoid arthritis patients using power Doppler ultrasonography as a gold standard.
Rheumatology (Oxford), 49 (2010), pp. 683-690
[150]
M. Gartner, P. Mandl, H. Radner, G. Supp, K.P. Machold, D. Aletaha, et al.
Sonographic joint assessment in rheumatoid arthritis: associations with clinical joint assessment during a state of remission.
Arthritis Rheum, 65 (2013), pp. 2005-2014
[151]
B. Saleem, A.K. Brown, H. Keen, S. Nizam, J. Freeston, R. Wakefield, et al.
Should imaging be a component of rheumatoid arthritis remission criteria? A comparison between traditional and modified composite remission scores and imaging assessments.
Ann Rheum Dis, 70 (2011), pp. 792-798
[152]
G. Peluso, A. Michelutti, S. Bosello, E. Gremese, B. Tolusso, G. Ferraccioli.
Clinical and ultrasonographic remission determines different chances of relapse in early and long standing rheumatoid arthritis.
Ann Rheum Dis, 70 (2011), pp. 172-175
[153]
R. Yoshimi, M. Hama, K. Takase, A. Ihata, D. Kishimoto, K. Terauchi, et al.
Ultrasonography is a potent tool for the prediction of progressive joint destruction during clinical remission of rheumatoid arthritis.
Mod Rheumatol, 23 (2013), pp. 456-465
[154]
F. Gandjbakhch, V. Foltz, A. Mallet, P. Bourgeois, B. Fautrel.
Bone marrow oedema predicts structural progression in a 1-year follow-up of 85 patients with RA in remission or with low disease activity with low-field MRI.
Ann Rheum Dis, 70 (2011), pp. 2159-2162
[155]
F. Gandjbakhch, E.A. Haavardsholm, P.G. Conaghan, B. Ejbjerg, V. Foltz, A.K. Brown, et al.
Determining a magnetic resonance imaging inflammatory activity acceptable state without subsequent radiographic progression in rheumatoid arthritis: results from a followup MRI study of 254 patients in clinical remission or low disease activity.
J Rheumatol, 41 (2014), pp. 398-406
[156]
L.C. Chew, P. Chandra Mohan, L.P. Chan, K.Y. Fong, J. Thumboo.
Use of magnetic resonance imaging in detecting subclinical synovitis in rheumatoid arthritis and correlation of imaging findings with interleukin-18 levels.
Int J Rheum Dis, (2014),
[157]
M.P. Lisbona, A. Pamies, J. Ares, M. Almirall, M. Navallas, A. Solano, et al.
Association of bone edema with the progression of bone erosions quantified by hand magnetic resonance imaging in patients with rheumatoid arthritis in remission.
J Rheumatol, 41 (2014), pp. 1623-1629
[158]
V.K. Ranganath, K. Motamedi, E.A. Haavardsholm, P. Maranian, D. Elashoff, F. McQueen, et al.
Comprehensive appraisal of magnetic resonance imaging findings in sustained rheumatoid arthritis remission: a substudy.
Arthritis Care Res (Hoboken), 67 (2015), pp. 929-939
[159]
C. Beckers, X. Jeukens, C. Ribbens, B. Andre, S. Marcelis, P. Leclercq, et al.
(18)F-FDG PET imaging of rheumatoid knee synovitis correlates with dynamic magnetic resonance and sonographic assessments as well as with the serum level of metalloproteinase-3.
Eur J Nucl Med Mol Imaging, 33 (2006), pp. 275-280
[160]
M. Boesen, L. Boesen, K.E. Jensen, M.A. Cimmino, S. Torp-Pedersen, L. Terslev, et al.
Clinical outcome and imaging changes after intraarticular (IA) application of etanercept or methylprednisolone in rheumatoid arthritis: magnetic resonance imaging and ultrasound-Doppler show no effect of IA injections in the wrist after 4 weeks.
J Rheumatol, 35 (2008), pp. 584-591
[161]
M. Dougados, S. Jousse-Joulin, F. Mistretta, M.A. d’Agostino, M. Backhaus, J. Bentin, et al.
Evaluation of several ultrasonography scoring systems for synovitis and comparison to clinical examination: results from a prospective multicentre study of rheumatoid arthritis.
Ann Rheum Dis, 69 (2010), pp. 828-833
[162]
E.A. Haavardsholm, M. Ostergaard, H.B. Hammer, P. Boyesen, A. Boonen, D. van der Heijde, et al.
Monitoring anti-TNFalpha treatment in rheumatoid arthritis: responsiveness of magnetic resonance imaging and ultrasonography of the dominant wrist joint compared with conventional measures of disease activity and structural damage.
Ann Rheum Dis, 68 (2009), pp. 1572-1579
[163]
M. Hama, T. Uehara, K. Takase, A. Ihata, A. Ueda, M. Takeno, et al.
Power Doppler ultrasonography is useful for assessing disease activity and predicting joint destruction in rheumatoid arthritis patients receiving tocilizumab—preliminary data.
Rheumatol Int, 32 (2012), pp. 1327-1333
[164]
H.B. Hammer, M. Sveinsson, A.K. Kongtorp, T.K. Kvien.
A 78-joints ultrasonographic assessment is associated with clinical assessments and is highly responsive to improvement in a longitudinal study of patients with rheumatoid arthritis starting adalimumab treatment.
Ann Rheum Dis, 69 (2010), pp. 1349-1351
[165]
P. Mandl, P.V. Balint, Y. Brault, M. Backhaus, M.A. D’Agostino, W. Grassi, et al.
Metrologic properties of ultrasound versus clinical evaluation of synovitis in rheumatoid arthritis: results of a multicenter, randomized study.
Arthritis Rheum, 64 (2012), pp. 1272-1282
[166]
E. Naredo, I. Moller, A. Cruz, L. Carmona, J. Garrido.
Power Doppler ultrasonographic monitoring of response to anti-tumor necrosis factor therapy in patients with rheumatoid arthritis.
Arthritis Rheum, 58 (2008), pp. 2248-2256
[167]
H.B. Hammer, T.K. Kvien.
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 (2011), pp. R78
[168]
P. Mandl, P.V. Balint, Y. Brault, M. Backhaus, M.A. D’Agostino, W. Grassi, et al.
Clinical and ultrasound-based composite disease activity indices in rheumatoid arthritis: results from a multicenter, randomized study.
Arthritis Care Res (Hoboken), 65 (2013), pp. 879-887
[169]
E. Naredo, M. Rodriguez, C. Campos, J.M. Rodriguez-Heredia, J.A. Medina, E. Giner, et al.
Validity, reproducibility, and responsiveness of a twelve-joint simplified power doppler ultrasonographic assessment of joint inflammation in rheumatoid arthritis.
Arthritis Rheum, 59 (2008), pp. 515-522
[170]
E. Naredo, C. Acebes, E. Brito, J.J. de Agustin, E. de Miguel, L. Mayordomo, et al.
Three-dimensional volumetric ultrasound: a valid method for blinded assessment of response to therapy in rheumatoid arthritis.
J Rheumatol, 40 (2013), pp. 253-260
[171]
M.B. Axelsen, R.P. Poggenborg, M. Stoltenberg, O. Kubassova, M. Boesen, K. Horslev-Petersen, et al.
Reliability and responsiveness of dynamic contrast-enhanced magnetic resonance imaging in rheumatoid arthritis.
Scand J Rheumatol, 42 (2013), pp. 115-122
[172]
M.P. Lisbona, J. Maymo, J. Perich, M. Almirall, J. Carbonell.
Rapid reduction in tenosynovitis of the wrist and fingers evaluated by MRI in patients with rheumatoid arthritis after treatment with etanercept.
Ann Rheum Dis, 69 (2010), pp. 1117-1122
[173]
K. Ellegaard, R. Christensen, S. Torp-Pedersen, L. Terslev, C.C. Holm, M.J. Konig, et al.
Ultrasound Doppler measurements predict success of treatment with anti-TNF-α drug in patients with rheumatoid arthritis: a prospective cohort study.
Rheumatology (Oxford), 50 (2011), pp. 506-512
[174]
P. Mandl, E. Naredo, P.G. Conaghan, M.A. D’Agostino, R.J. Wakefield, A. Bachta, et al.
Practice of ultrasound-guided arthrocentesis and joint injection, including training and implementation, in Europe: results of a survey of experts and scientific societies.
Rheumatology (Oxford), 51 (2012), pp. 184-190
[175]
J. Cunnington, N. Marshall, G. Hide, C. Bracewell, J. Isaacs, P. Platt, et al.
A randomized, double-blind, controlled study of ultrasound-guided corticosteroid injection into the joint of patients with inflammatory arthritis.
Arthritis Rheum, 62 (2010), pp. 1862-1869
[176]
K.R. Luz, R.N. Furtado, C.C. Nunes, A. Rosenfeld, A.R. Fernandes, J. Natour.
Ultrasound-guided intra-articular injections in the wrist in patients with rheumatoid arthritis: a double-blind, randomised controlled study.
Ann Rheum Dis, 67 (2008), pp. 1198-1200
[177]
W.L. Sibbitt Jr., P.A. Band, N.R. Chavez-Chiang, S.L. Delea, H.E. Norton, A.D. Bankhurst.
A randomized controlled trial of the cost-effectiveness of ultrasound-guided intraarticular injection of inflammatory arthritis.
J Rheumatol, 38 (2011), pp. 252-263
[178]
W.L. Sibbitt Jr., A. Peisajovich, A.A. Michael, K.S. Park, R.R. Sibbitt, P.A. Band, et al.
Does sonographic needle guidance affect the clinical outcome of intraarticular injections?.
J Rheumatol, 36 (2009), pp. 1892-1902
[179]
W.L. Sibbitt Jr., L.G. Kettwich, P.A. Band, N.R. Chavez-Chiang, S.L. deLea, L.J. Haseler, et al.
Does ultrasound guidance improve the outcomes of arthrocentesis and corticosteroid injection of the knee?.
Scand J Rheumatol, 41 (2012), pp. 66-72

Please cite this article as: Möller I, Loza E, Uson J, Acebes C, Andreu JL, Batlle E, et al. Recomendaciones para el uso de la ecografía y la resonancia magnética en pacientes con artritis reumatoide. Reumatol Clin. 2018;14:9–19.

28 September 2015.

Copyright © 2016. Elsevier España, S.L.U. and Sociedad Española de Reumatología y Colegio Mexicano de Reumatología
Idiomas
Reumatología Clínica (English Edition)
Article options
Tools
es en

¿Es usted profesional sanitario apto para prescribir o dispensar medicamentos?

Are you a health professional able to prescribe or dispense drugs?