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348

The Increasing Spectrum of Indications of Whole-Body MRI Beyond : Imaging Answers to Clinical Needs

Frédéric E. Lecouvet, MD, PhD1 Nicolas Michoux, PhD1 Adrien Nzeusseu Toukap, MD2 Ahmed Larbi, MD1 Bruno Vande Berg, MD, PhD1 Jacques Malghem, MD1 Perrine Triqueneaux, MSc1 Patrick Omoumi, MD, MSc, PhD3 Maria Simona Stoenoiu, MD, PhD2

1 Departments of , Institut de Recherche Expérimentale et Address for correspondence Frédéric E. Lecouvet, MD, PhD, Clinique (IREC), Cliniques Universitaires Saint Luc, Brussels, Belgium Department of Radiology, Institut de Recherche Expérimentale et 2 Department of , Institut de Recherche Expérimentale et Clinique (IREC), Cliniques Universitaires Saint Luc, Avenue Hippocrate, Clinique (IREC), Cliniques Universitaires Saint Luc, Brussels, Belgium 10, B-1200 Brussels, Belgium (e-mail: [email protected]). 3 Department of Diagnostic and , Lausanne University Hospital, Lausanne, Switzerland

Semin Musculoskelet Radiol 2015;19:348–362.

Abstract Whole-body coverage using MRI was developed almost 2 decades ago. The first applications focused on the investigation of the skeleton to detect neoplastic disease, mainly metastases from solid , and involvement by multiple myeloma and lymphoma. But the extensive coverage of the whole musculoskeletal system, combined with the exquisite sensitivity of MRI to tissue alteration in relation to different pathologic Keywords conditions, mainly inflammation, has led to the identification of a growing number of ► MRI indications outside oncology. Seronegative rheumatisms, systemic sclerosis, inflamma- ► diffusion-weighted tory diseases involving muscles or fascias, and multifocal osseous, vascular, or neuro- MRI logic diseases represent currently validated or emerging indications of whole-body MRI ► whole-body MRI (WB-MRI). We first illustrate the most valuable indications of WB-MRI in seronegative ► rheumatisms rheumatisms that include providing significant diagnostic information in patients with ► spondyloarthropathy negative or ambiguous MRI of the sacroiliac and the lumbar spine, assessing ► systemic sclerosis disease activity in advanced (ankylosed) central disease, and evaluating the peripherally ► dominant forms of spondyloarthropathy. Then we review the increasing indications of ► treatment WB-MRI in other rheumatologic and nonneoplastic disorders, underline the clinical ► inflammation needs, and illustrate the role of WB-MRI in the positive diagnosis and evaluation of ► biomarker disease burden, therapeutic decisions, and treatment monitoring. Downloaded by: the European Society of Musculoskeletal Radiology. Copyrighted material.

MRI combines exquisite anatomical resolution, excellent But over the past 2 decades, developments in hardware tissue contrast, and high sensitivity to bone and soft tissue and software have enabled extensive coverage of the whole alterations. For years, its focus has remained the targeted body using MRI within clinically reasonable time frames.1,2 study of a definite , , or anatomical area, using a Whole-body (WB)-MRI was first applied to assess the relatively limited field of view (FOV). A more extensive entire skeleton in oncology and emerged as a technique coverage of the body was hindered by long acquisition of choice for the detection and quantification of tumor times. involvement in metastatic disease to bone, multiple mye- – loma, and lymphoma.3 6 In this field, WB-MRI outperforms bone and radiographs for lesion detection, and P. Omoumi and M. Stoenoiu contributed equally to this work.

Issue Theme Update on Advances in Copyright © 2015 by Thieme Medical DOI http://dx.doi.org/ Musculoskeletal Magnetic Resonance Publishers, Inc., 333 Seventh Avenue, 10.1055/s-0035-1564695. Imaging; Guest Editor, Patrick Omoumi, New York, NY 10001, USA. ISSN 1089-7860. MD, MSc, PhD Tel: +1(212) 584-4662. Increasing Indications for Whole-Body MRI Lecouvet et al. 349 it has become, along with positron emission eral joints that are predominantly involved in rheumatoid (PET), the modality of choice for disease staging and treat- or psoriatic . Moreover, the upper limbs are not – ment monitoring.7 10 well included in routine examinations because the elbows, Parallel to oncologic applications, WB-MRI was progressively hands, and wrist are frequently excentrated within the applied to detect and characterize other disorders affecting magnet.20 However, protocols are being developed, and bones, joints, tendons, entheses, or neurovascular structures in “optimizedheadtotoe” WB-MRI, including upper extrem- – a multifocal, multisystemic, or diffuse fashion.11 16 ities positioned on the belly or behind the back, have been In this article, we review and illustrate the validated and reported.21,22 emerging indications of WB-MRI in axial rheumatisms (mainly represented by spondyloarthropathies), systemic Rheumatologic Disorders disorders affecting muscles, fascias, or subcutaneous tissues, and multifocal benign proliferative or inflammatory disor- The most largely evaluated indications for WB-MRI in rheu- ders involving bones, joints, nerves, or vessels, either in matologic disorders are seronegative rheumatisms. WB-MRI isolation or in combination. has also become the imaging modality of choice in aseptic multifocal osteitis embedded in the synovitis, acne, pustu- WB-MRI Image Acquisition losis, hyperostosis, osteitis (SAPHO) syndrome, and its juve- nile form, chronic recurrent multifocal osteomyelitis (CRMO). The usual FOV for the MRI of an organ, joint, or spine Multifocal inflammatory muscle and soft tissue disorders, segment ranges between 15 and 40 cm, and routine exami- and systemic sclerosis are other recent indications. The nations have to address the clinical question within these technique enables the positive diagnosis and evaluation of spatial limits, using surface coils optimized for each ana- disease activity and extent, as well as the evaluation of tomical region. response to modern treatments. The more extensive coverage of the body has been made possible thanks to hardware developments (i.e., table dis- placement within the magnet, adaptation of coils with the Seronegative Spondyloarthropathies advent of multichannel and phased array technology), as well Ankylosing Spondyloarthritis as major advances in imaging techniques (i.e., sequence developments and gradient technology to speed up acquis- Disease Characteristics and Clinical Needs itions).1,17 The coverage of the entire body relies on the Axial spondyloarthropathies include ankylosing spondyloar- consecutive acquisitions of image stacks with a 25- to 45- thritis (AS), psoriatic arthritis, enteropathic arthritis, and cm FOV in the craniocaudal direction, with some overlap to reactive arthritis as well as “undifferentiated” spondyloar- allow the reconstruction of “fused” images. In daily practice, thritis. AS is by far the most frequent form of these rheuma- the examination may really cover the whole body “from head tisms, most commonly occurring in early adulthood, and to toe,” which may be indicated in disorders affecting the shows a strong association with the human leucocyte antigen distal portion of the lower limbs or be limited from “eyes to B27.23 Typical radiographic findings include erosions, new thighs,” which appears sufficient for the study of axial bone formation, and evolution to ankylosis, localized at the rheumatisms or oncologic conditions that mainly affect the diskovertebral junctions, the SIJs, but also at peripheral joints axial skeleton, while saving time.18 and entheses. Concerning the planes and sequences, the choice is Due to lack of specificity of clinical findings and limited guided by the indication. A coronal short tau inversion diagnostic effectiveness of imaging techniques available until recovery (STIR) sequence of the whole body drives atten- now (i.e., radiographs, computed tomography, and bone tion to tissue signal alteration in bones, muscles, or joints, scintigraphy), positive diagnosis may often be delayed. In Downloaded by: the European Society of Musculoskeletal Radiology. Copyrighted material. anditisusedtoshowactiveinflammatory lesions in parallel, new , mainly tumor factor α spondyloarthropathies. T1-weighted sequences are cardi- (TNFα) inhibitors, have been successfully used to treat AS. nal for the study of bone marrow and useful for the study of These treatments, however, are both expensive and poten- structural changes in rheumatologic disorders. The study of tially toxic, raising the need for more efficient diagnostic the whole spine in the sagittal plane using STIR and T1 tools. MRI covering the “central skeleton,” that is, the SIJ and sequences to detect characteristic lesions is mandatory in lumbar spine, has been established as the method of choice conditions where the axial skeleton is affected, such as for early diagnosis, treatment initiation, and evaluation of – spondyloarthropathies.19 Transverse T2 or STIR and T1- therapeutic response.24 26 weighted sequences serve for the study of muscles. The basic protocol may be supplemented by dedicated sequen- MRI in Ankylosing Spondyloarthritis ces,withlimitedFOVandspecific slice orientation, for MRI is the imaging modality of choice to detect both early, example coronal oblique sequences on the sacroiliac joints sometimes infraclinical inflammatory changes known as pre- (SIJs) and transverse or sagittal sections on the feet and structural changes (i.e., bone marrow edema [BME] adjacent to ankles in spondyloarthropathies.14 joints or disks, synovitis, enthesitis), as well as chronic structural The information obtained with current WB-MRI studies changes. The detection of BME on MRI, representing active remains insufficient for a detailed analysis of small periph- inflammation in the subchondral bone underlying SIJs, has

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been included as the main contributor to the positive diagnosis observed in the setting of degenerative disk disease, Outcome of AS in the Assessment of SpondyloArthritis International Measures in Rheumatology (OMERACT) and ASAS criteria re- Society (ASAS) classification criteria.27,28 Of note, current rec- quire at least three anterior or posterior corner elementary ommendations only include MRI of the SIJ, and not of the spine, lesions.31 MRI is also used for the evaluation of therapeutic for the diagnosis of AS.29 Thepositivediagnosticcriteriaarethe response using scoring of several systems developed for the SIJ or – detection of a BME area present on at least two consecutive the spine.26,32 35 sections or of two distinct BME areas on the same section of the SIJ.30 Current recommendations consider other acute changes WB-MRI Findings and Indications (synovitis, capsulitis, enthesitis) and structural lesions not suffi- WB-MRI may extend the detection of inflammatory cient for a positive diagnosis. Nevertheless, imaging the spine is changes to the whole spine, pelvic and shoulder girdles, often useful, typically showing BME affecting vertebral corners and lower limbs, often revealing multiple and sometimes – of the thoracolumbar junction. To avoid confusion with BME subclinical lesions11,36 39 (►Fig. 1). Screening the whole Downloaded by: the European Society of Musculoskeletal Radiology. Copyrighted material.

Fig. 1 WB-MRI for initial diagnosis of ankylosing spondyloarthritis in a 35-year-old man with a 3-month history of inflammatory pain, with negative radiographs, computed tomography of the sacroiliac joint (SIJ), and negative SIJ and lumbar MRI survey. (a–d) Sagittal T1 and -saturated T2- weighted images of the lumbosacral spine (a, b) and coronal oblique T1 and short tau inversion recovery (STIR) images of the SIJ (c, d) show no relevant abnormality. (e, f) Sagittal T1 and STIR MR images of the whole spine show subtle edema in two adjacent vertebral corners in the midthoracic spine (arrows). (g) Coronal STIR image of the spine confirms edema adjacent to vertebral end plates (arrows) and in left paraspinal tissues (arrowheads). (h, i) Three-month follow-up sagittal study of the spine shows appearance of nonambiguous inflammatory involvement of multiple vertebral corners, in the mid (T5, T6) and lower (T11, T12) thoracic segments (arrows).

Seminars in Musculoskeletal Radiology Vol. 19 No. 4/2015 Increasing Indications for Whole-Body MRI Lecouvet et al. 351 spine and in particular its thoracic segment increases by far active in patients with severe structural damage of the axial the number of detected lesions and diagnostic confi- skeleton42 (►Fig. 2). dence.40 The involvement of the lateral margins of end The ability of WB-MRI to detect evolution from active plates and costovertebral junctions, posterior joints, and inflammation to a quiescent or healed stage has been used for posterior ligaments is highly specificofAS.Anothervery response assessment in major clinical trials and now progres- important area is the thoracic wall, particularly the ster- sively in selected clinical situations.43,44 WB-MRI seems to noclavicular, manubriosternal, or chondrosternal joints provide nonredundant information in comparison with clin- (►Fig. 2). Most importantly, WB-MRI has shown that ex- ical and biological response evaluations, representing a tra-axial sites are involved in more than half of patients, promising biomarker to pilot the treatment in early stages with peripheral enthesitis and synovitis observed in as of AS, but also to detect active disease in chronic stages many as 77% of patients.24 The peripheral lesions may (►Fig. 2).21,45 include the hip, the knee, the foot and ankle, and the shoulder41 (►Fig. 3). The elbow, wrists, and hands are not Protocols and Practical Approach included in most WB-MRI examinations, but research is WB-MRI should include fat-suppressed T2 or STIR images ongoing to include the upper extremities in investigated (to detect active inflammation) and T1-weighted sequences FOVs.21,22 A major role of WB-MRI seems to be the identi- to detect structural changes. The injection of is fication of peripheral sites of active disease, both in the not performed routinely. Protocols include coronal T1 and early and late stages, as it is well known that AS can remain STIR images of the WB, sagittal T1 and STIR images of the Downloaded by: the European Society of Musculoskeletal Radiology. Copyrighted material.

Fig. 2 WB-MRI for diagnosis of disease activity in a 29-year-old man with advanced severe spondyloarthritis and inflammatory pain. (a, b) Coronal oblique T1 and short tau inversion recovery (STIR) images of the sacroiliac joint (SIJ) (a, b) show complete ankylosis of both SIJs (asterisks) with no sign of disease activity. (c–e) Zoomed coronal STIR images from WB-MRI study show active inflammation at the level of chondrosternal joints (arrows in c), bilateral hip synovitis (arrowheads in d), and left-sided lateral involvement of the thoracic spine (arrows in e). (f)SagittalSTIRMR image of the thoracic spine shows active inflammation (edema) involving the lateral and posterior aspects of multiple vertebral end plates (arrows in f).

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Fig. 3 WB-MRI in diagnosis of peripheral dominant form of spondyloarthropathy in a 19-year-old man. (a) Sagittal short tau inversion recovery (STIR) image of the whole spine shows subtle edema within the T12 anterosuperior vertebral corner (arrowhead). (b, c) Coronal oblique T1 and STIR images of the sacroiliac joint (SIJ) (b, c) show subtle signs of disease activity, consisting of edema in the subchondral bone marrow of the iliac aspect of the left SIJ (arrows in c). (d, e) WB-MRI coronal STIR images show active inflammation consisting of synovitis of the right knee (arrow in d) and of the posterior tibial tendon at the level of the right ankle (arrowhead in e). (f) Transverse STIR MR image of the right ankle confirms active tenosynovitis (arrowhead in f).

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Fig. 4 Role of diffusion-weighted imaging in detection of ankylosing spondyloarthritis involvement by WB-MRI study in a 40-year-old woman with human leucocyte antigen B27 positive serotype and high clinical suspicion but negative sacroiliac joint and lumbar spine MR studies. (a, b) Coronal reformatted diffusion-weighted image MR images (inverted gray scale, high b values, b ¼1000 s/mm2) show evident involvement of manubrio- and chondrosternal joints (arrowheads in a), as well as lateral involvement of the midthoracic spine (arrow in b). (c, d) Corresponding coronal short tau inversion recovery images: the detection of the lesions is much less evident.

whole spine, and high-resolution oblique coronal T1 and STIR AS but ambiguous nonconclusive findings at MRI of the images on the SIJ parallel to the long axis of the sacrum central skeleton (►Fig. 1). Second, WB-MRI is particularly (►Fig. 3). Diffusion-weighted imaging (DWI) is potentially useful in advanced disease to detect signs of peripheral useful because it easily shows active areas on high b values activity, especially in the presence of ankylosis of the central DWI, with increased apparent diffusion coefficient (ADC) skeleton (►Fig. 2). Third, WB-MRI covering the appendicular values on ADC maps (►Fig. 4).46,47 The underlying mecha- skeleton should be used as a first-choice technique to assess nisms of these signal characteristics are not completely clear. the peripherally dominant forms of spondyloarthropathies In practice, it is difficult to use WB-MRI to replace (►Fig. 3). Fourth, WB-MRI should be used for response conventional MRI, due to long scan times (30–60 minutes) assessment in the previous three situations. Finally, WB- Downloaded by: the European Society of Musculoskeletal Radiology. Copyrighted material. and because MRI of the spine and SIJ already enables a MRI has become the modality of choice for the evaluation reliable diagnosis in most patients.29 Covering the spine on of juvenile spondyloarthropathies in children and top of the SIJ provides much substantial information, adolescents.50 especially in patients with a negative MRI of the SIJ.19 This contribution of an additional spine MRI in the presence Psoriatic Arthritis of a normal SIJ is debated in the literature, qualified as “of Dedicated MRI examinations are more effective than clini- limited incremental value compared to the SIJ study” or, on cal and radiographic examinations for the detection of the contrary, as “bringing a positive diagnostic contribu- (teno)synovitis and enthesitis in psoriatic arthritis.51 tion in up to 20 to 50% of patients” with normal SIJ.48,49 A WB-MRI enables the evaluation of the spine and SIJ, and “limited” WB-MRI approach may also be considered, com- it reveals the frequent involvement of tenosynovial sheaths bining a classical SIJ protocol with sagittal imaging of the and adjacent bony structures. As in AS, WB-MRI may play a entire spine and coronal STIR images limited to the scapular role in therapeutic decisions and monitoring (i.e., initiation and pelvic girdles. of TNFα inhibitors and response evaluation).20 Recent In our experience, WB-MRI has four main indications in comprehensive body approaches have shown great prom- the context of AS. First, WB-MRI should be used as a second- ise in providing a global scoring based on the study of the line examination in patients with a strong clinical suspicion of spine, SIJ, but also of all peripheral joints and entheses.22

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At MRI, the disease has a variable imaging appearance Multifocal Aseptic Musculoskeletal “ ” Disorders depending on the age and activity of the lesions. Findings consist of focal lesions of bone marrow infiltration with The Synovitis, Acne, Pustulosis, Hyperostosis, and frequent periosteal reactions during the active phase, with Osteitis Syndrome and Chronic Recurrent Multifocal subsequent appearance of sclerosis and fatty involution Osteomyelitis during the chronic phase. Along with the typical location of The SAPHO syndrome was first described in 198752 to the lesions and frequent involvement of joints adjacent to characterize an inflammatory clinical condition presenting bone abnormalities, the concurrent observation of active as a common denominator the aseptic involvement of and quiescent lesions may help differentiate this entity bones and joints with characteristic skin lesions, most from multifocal infectious disease or tumoral frequently palmoplantar pustulosis and acne conglobata. involvement.55 It mainly affects adults in their 30s or 40s. The pathogene- WB-MRIfacilitatesearlydiagnosisbydetectingmultifo- sis remains unclear, with infection by Propionibacterium cal osteitis, with a suggestive distribution, often with some acnes inconsistently demonstrated and a probable genetic lesions being asymptomatic and located in the peripheral predisposition.53 skeleton, and typically of varying age56(►Fig. 5). The SAPHO syndrome can involve any skeletal site. CRMO mainly affects children and adolescents, and it is Involvement predominates in the sternocostoclavicular characterized by chronic aseptic inflammation responsible and sacroiliac regions (70–90%), the spine (30%), and the for prolonged fluctuatingpaininassociationwithmultifo- anterior chest wall (70–90%). Other sites can be involved: cal bone lesions. The diagnosis is often difficult and long bones, flat bones, and large and small joints including delayed because clinical findings, biological tests, and the SIJ (13–52%).54 radiographs are nonspecific.57 WB-MRI outperforms Downloaded by: the European Society of Musculoskeletal Radiology. Copyrighted material.

Fig. 5 WB-MRI in SAPHO syndrome (multifocal aseptic osteitis) in a 40-year-old female patient with multifocality. This case illustrates the close connection between bone involvement and disks, sternal, and sacroiliac (SIJ) joints. (a–c) Radiographs of the hands, right hip, and SIJ show hyperostosis of the distal phalanx of the right thumb (arrow in a), of the right greater trochanter (arrows in b), and of the iliac aspect of both SIJ (arrowheads in c). (d, e) Coronal and sagittal short tau inversion recovery (STIR) images of the WB-MRI study show sternal involvement (arrow in d), of the midthoracic spine (arrow in e), and of the SIJ (arrowheads in e). (f) Midsagittal STIR image confirms involvement of vertebral corners on each side of the same midthoracic disk (arrow) and extensive involvement of the sternum (arrowhead). (g) Oblique coronal images STIR on the SIJ show extensive edema within the iliac portion of the joints with no sacral or joint space involvement (arrowheads).

Seminars in Musculoskeletal Radiology Vol. 19 No. 4/2015 Increasing Indications for Whole-Body MRI Lecouvet et al. 355 radiographs and , and it represents an weakness due to from limitation of movement effective nonirradiating substitute for these methods. The because of increased skin thickness, fibrosis, and joint con- most frequent locations of inflammatory lesions are the tractures; imaging is also expected to help in this differential metaphyseal and juxtaphyseal regions of the long bones, diagnosis. pelvic bones, and the spine, with nonexceptional observa- tion of vertebra plana.58 The lesions are most frequently WB-MRI in Systemic Sclerosis located in the lower limbs, often distributed in a suggestive WB-MRI appears very promising in SSc and its localized symmetrical fashion.12 The clavicle, thoracic wall, and forms to detect musculoskeletal involvement, which is spine are other frequent locations and are sometimes frequently symmetrical and multiform, present in > 50% asymptomatic. Sacroiliitis, synovitis, and joint effusion of patients, consisting of synovitis, tenosynovitis, myositis, are not exceptional on WB-MRI studies.50 The characteris- fasciitis, or enthesitis.13,62,63 WB-MRI findings at the in- tic fluctuation and recurrences of the lesions over time flammatory stage of localized consist of thick- often enable a confident differential diagnosis from tumor ening of the dermis and infiltration of the subcutaneous and septic osteomyelitis, obviating a biopsy in many pa- fatty tissue, with a decreased signal intensity on T1-weight- tients.14 Patient follow-up using WB-MRI also shows the ed images, increased signal intensity on STIR sequences, persistence of active lesions despite so-called clinical and enhancement on postcontrast T1-weighted images. remission. Beneath the infiltrated skin, fascia and muscles can be involved, showing variable degrees of inflammation as in Systemic Sclerosis the subcutaneous tissues. WB-MRI has also been used to monitor treatment and was Disease Characteristics and Clinical Needs shown to be sensitive to changes in the severity of subcuta- The severe disease formerly known as scleroderma is now neous thickening, fascial thickening, and fascial enhancement called systemic sclerosis (SSc) to underline the systemic in patients responding to a - and prednisolone- features that oppose it to localized scleroderma, and to based treatment.64 emphasize the fibrosis process that can involve virtually all The muscular sites predominantly affected are supposed organs, not only the skin and subcutaneous tissue as in to be the proximal regions of both extremities on the basis morphea.59 SSc is one of the most devastating systemic of clinical evaluation.65 However, WB-MRI in our experi- rheumatic disorders. The severe form of the disease is ence (►Fig. 6) and in a published series shows that muscu- characterized by intense inflammation, followed by fibro- lar involvement can be widespread, including shoulder and sis, involving not only the skin and subcutaneous tissue pelvic girdles, but also the thoracic and abdominal walls, but also other major organs, such as the , the esopha- and distal limbs.13 The MRI pattern is mostly symmetrical gus, the gut, and the kidneys, leading to multiple organ and often generalized. failure in the worst cases. Different types of morphea In conclusion, WB-MRI in SSc provides original and rele- (plaque morphea, linear morphea, bullous morphea, deep vant information with only limited correlation with clinical morphea, pansclerotic morphea, and generalized morphea) and biological parameters. The detection of inflammatory are referred to as localized scleroderma. The MRI lesions may help in the identification of patients with a bad features are described separately for SSc and localized prognosis and at risk of severe organ damage, and in the scleroderma. monitoring of treatment (►Fig. 6). Long-term studies are SSc is a complex disorder in which clinical manifestations ongoing to further determine the sensitivity of WB-MRI to only represent the top of the pathophysiologic iceberg, which -induced changes and support its added value as an explains the need for objective prognostic factors. Tendons, imaging biomarker. joints, and muscles are involved in 40 to 80% of patients that Downloaded by: the European Society of Musculoskeletal Radiology. Copyrighted material. has an impact on their quality of life. Moreover, joint and Inflammatory Disorders of the Skeletal tendon involvement as detected clinically predict overall Muscles and Fascias disease progression, as shown in the EUSTAR cohort.60 Thus early detection of joint and tendon involvement may WB-MRI has been evaluated in a large variety of multifocal identify a subset of patients at risk for disease progression. inflammatory muscle disorders including idiopathic in- However, clinical examination underestimates the frequency flammatory and fasciitis. The role of WB-MRI of synovitis and tenosynovitis, with a potential role for WB- is also emerging in other rare disorders involving muscles MRI in this indication. Another relevant clinical manifestation or fascias, and in muscular dystrophy or other genetic is the presence of “tendon friction rubs,” which have prog- disorders. nostic value and are associated with the progression of skin fibrosis. Skeletal muscles are involved in 14 to 96% of SSc Idiopathic Inflammatory Myopathies patients.59 Muscle involvement has prognostic value, corre- lated with vital organ damage, in particular myocarditis and Disease Characteristics and Clinical Needs fibrosis.60,61 Most patients have symmetrical proximal (PM), (DM), and inclusion limb weakness, although distal weakness can be present at body myositis (IBM) are the distinct expressions of idio- clinical examination. But it can be difficult to distinguish pathic inflammatory myopathies (IIMs), a heterogeneous

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Fig. 6 WB-MRI work-up of diffuse systemic sclerosis in a 44-year-old woman presenting tendon friction rubs, synovitis, tenosynovitis, and reduced range of motion in shoulders and ankles. Myositis was suspected because of slight elevation of creatine phosphokinase levels, but clinical examination was not conclusive. (a, b) Coronal (a) and transverse (b) short tau inversion recovery (STIR) MRI images reveal extensive musculoskeletal involvement with predominant involvement of the muscles and fascias at the scapular and pelvic girdles and of the thoracic wall (arrows), with moderate infiltration of the subcutaneous tissues (arrowheads). (c, d) Corresponding images after treatment with mycophenolate mofetil and rituximab show an almost complete disappearance of WB-MRI abnormalities. Downloaded by: the European Society of Musculoskeletal Radiology. Copyrighted material. group of muscle disorders consisting of an autoimmune and thoracic muscles, and the diaphragm. DM affects the reaction against skeletal muscle, and presenting with muscles but also the skin, as the name indicates. A typical chronic and progressive symmetrical muscle weakness. facial heliotrope skin rash is present along with muscle The involvement of muscles in IIMs may be either isolated, weakness and pain.66,67 PM affects young adults and con- associated with extramuscular features, or associated with sists of isolated symmetrical muscle involvement and the other connective tissue disorders such as antisynthetase absence of skin involvement. IBM mainly affects older male syndrome (ASS), SSc, Sjögren syndrome, erythema- patients, may be asymmetric, and most commonly starts in tosus, rheumatoid arthritis, or mixed connective tissue distal muscles, especially extensors of the knee and flexors disorders.66,67 of the wrist and fingers. Patients with DM and PM present with muscle weakness In addition to muscular involvement, , arthri- that is more pronounced proximally, impaired muscle tis, and tenosynovitis are common in patients with ASS, endurance, and excessive muscle fatigue. The onset is involving the hands, feet, wrists, and ankles, and may be the usually subacute or insidious, and the distribution is typi- first manifestation before muscle or lung involvement cally symmetrical. In addition to musculoskeletal involve- become clinically apparent. For this reason, patients with ment, patients may have eating, swallowing, and ASS may get a first diagnosis of primary inflammatory respiratory disorders due to involvement of the pharyngeal arthritis or rheumatoid arthritis. In these cases, MRI is

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observed, predominantly involving the scapular and pelvic girdles.71 IBM shows diffuse muscle edema in the involved muscle groups.71 WB-MRI most importantly identifies sites of active muscle to guide a biopsy for a histologic diagno- sis, hereby reducing the high false-negative rate of blind biopsies.72 Muscle biopsy is indeed cardinal to confirm the inflammatory origin and activity of the disease, to identify IBMfromDMandPM,andtoruleoutmetabolicmyopathies and muscle dystrophy. Finally, WB-MRI represents an excellent tool for evaluating the response of these diseases to treatment73 (►Fig. 7).

Neuromuscular Disorders MRI, and more recently WB-MRI, has been used in geneti- cally inherited neuromuscular disorders. The basic obser- vations are the same as those seen in inflammatory disorders, consisting of edema at the early stage and fatty and fibrotic replacement at the chronic stage.74 The main role of WB-MRI is to study the distribution of involved muscles or muscle groups, which may be characteristic, for example, in Duchenne and Becker diseases, and in myotonic dystrophies.68 WB-MRI may also guide muscle biopsies and monitor the global fat content to follow the evolution of the disease.75

Fig. 7 WB-MRI in dermatomyositis in a 25-year-old woman with a (Shulman Disease) recent history of eyelid and face rash, arthralgia, and diffuse muscle First reported in 1975 by Shulman, this rare disorder pain and stiffness. (a, b) Coronal whole-body short tau inversion is characterized clinically by symmetrical painful sclero- recovery (STIR) images show marked increased signal intensity of derma-like indurations of the skin and histologically by multiple muscles, predominantly involving the thoracic and pelvic fl girdles (arrows), and adjacent infiltration of the subcutaneous tissue lymphocytic and eosinophilic in ammation, and thicken- 76 (arrowheads). ing and fibrosis of the fascias. WB-MRI enables an ex- haustive work-up, supports the diagnosis by showing suggestive findings, helps guide the biopsy (that requires sampling of involved fascias with adjacent subcutaneous tissues and muscle), and finally provides follow-up of the particularly useful to disclose the extra-articular features disease under treatment (►Fig. 8). In the typical forms, WB- of the disease (i.e., myositis or fasciitis) and ultimately MRI shows abnormal increased signal intensity and thick- correct the first clinical diagnosis. ening of the fascias on T2 and STIR images, and enhance- ment on postgadolinium sequences.77 Less typical WB-MRI of Inflammatory Myopathies presentations are characterized by involvement of hypo- WB-MRI enables a comprehensive detection of changes in dermic tissues or muscle fibers adjacent to the involved Downloaded by: the European Society of Musculoskeletal Radiology. Copyrighted material. signal or size in muscles or perimuscular tisses.68 Typical fascias.78,79 abnormalities are high signal intensity on fat-suppressed fluid-sensitive sequences and enhancement in the active phase, and spontaneous high signal intensity on T1-weight- Multifocal Bone, Nerve, and Vascular Lesions ed sequences in the chronic inactive phase. Changes in Multifocal Bone Lesions muscle size consist of atrophy or (pseudo) hypertrophy.69 Therefore, WB-MRI can be used to confirm the diagnosis of Sarcoidosis muscle involvement and is helpful to determine the phe- Sarcoidosisisamultisystemdisease of unknown etiology notype of the disease on the basis of the involved tissues characterized by noncaseating granulomas involving mul- (muscles, subcutaneous tissue, or fascias) and on the basis tiple organs. WB-MRI is increasingly used for the detection of the preferential topography of the abnormalities within of hepatosplenic, but also bone, node, and muscle le- the body (i.e., the trunk, girdles, proximal or distal limbs) or sions.80,81 Apart from peripheral lesions, multifocal in- within the muscle itself (central, peripheral, or diffuse volvement of the axial skeleton is frequent and may involvement). In DM, it shows the concurrent involvement mimic metastatic disease.82 However, the coexistence of of the muscles and subcutaneous tissues; the fascias may active and quiescent (fatty) lesions may help in this differ- also be involved70 (►Fig. 7). In PM, isolated muscle edema is ential diagnosis.83

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Fig. 8 WB-MRI work-up of eosinophilic fasciitis in a 70-year-old woman with and arthralgia, and painful skin induration of the chest and limbs, occurring after unusual exercise. (a–e) Coronal (a, b) and transverse (c–e) short tau inversion recovery images show diffuse increased signal and thickening of the fascias of the chest and abdominal wall, and of the girdles and limbs, involving the superficial and intermuscular fascias, with to a lesser extent involvement of the subcutaneous soft tissues. No evident myositis is present. A diagnosis of eosinophilic fasciitis was made on a biopsy specimen obtained in her calf.

Langerhans Cell Histiocytosis Multifocal Cartilaginous Tumors WB-MRI outperforms radiographs and bone scintigraphy Multiple exostoses may be followed up for the detection of for the detection of lesions in pediatric histiocytosis and in (lesions at risk for) malignant transformation by WB-MRI, but rare cases of adult multifocal eosinophilic granulomas.84 the measurement of the cartilage cap thickness requires a Downloaded by: the European Society of Musculoskeletal Radiology. Copyrighted material. The findings consist of multiple areas of bone marrow smaller FOV.88 replacement.85 As for sarcoidosis, the coexistence of active and healed lesions (partial fatty transformation) may sug- Peripheral Nerve Lesions gest the diagnosis, which however often requires histologic WB-MRI has been used for the detection, measure- confirmation. WB-MRI appears more sensitive than PET for ment, and follow-up of extensive neurogenic lesions lesion detection in pediatric forms, but PET might be (►Fig. 10). In type I neurofibromatosis, WB-MRI is superior for treatment monitoring.86 used for a global quantification of tumor load in plexiform neurofibromas and prospective patient follow- Ischemic Lesions up for the detection of malignant transformation or de novo WB-MRI may play a role for the preclinical detection of appearance of malignant peripheral nerve sheath ischemic epiphyseal lesions in relation to the classical tumors.89,90 systemic causes of osteonecrosis, mainly lupus, hemoglo- binopathies and high-dose corticoid intake in severe rheu- Vascular Disorders matologic, oncologic, or hematologic disorders15,87 Multifocal or extensive vascular diseases or malformations (►Fig. 9). maybestudiedandfollowedupbyWB-MRI.91

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Fig. 9 Multiple bone infarcts in a young patient with sickle cell disease. (a, b) Coronal T1 whole-body images show diffuse abnormal low signal of the bone marrow involving the spine, pelvic bones, and long bone diaphyses in relation to chronic anemia. (c, d) Coronal short tau inversion recovery whole-body images show the presence of multiple ischemic areas surrounded by a high signal intensity line, corresponding to infarcts in multiple epiphyses and diaphyses (arrowheads). The same technique may detect multiple ischemic lesions induced by high-dose or chronic corticoid intake. Downloaded by: the European Society of Musculoskeletal Radiology. Copyrighted material.

Fig. 10 WB-MRI work-up of extensive plexiform neurofibroma in a 30-year-old woman. (a) Coronal and (b–d) transverse T2-weighted image of lower portion of the body shows multinodular lesion along the course of the right sciatic nerve, extending from the lumbar plexus to the popliteal fossa (arrows). Another subcutaneous lesion is seen (arrowhead). This examination is repeated at regular intervals to rule out the appearance of a malignant lesion.

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Conclusions and Perspectives 11 Althoff CE, Appel H, Rudwaleit M, et al. Whole-body MRI as a new screening tool for detecting axial and peripheral manifestations of – The major application of WB-MRI in rheumatology remains spondyloarthritis. Ann Rheum Dis 2007;66(7):983 985 12 Fritz J, Tzaribatchev N, Claussen CD, Carrino JA, Horger MS. Chronic the study of seronegative spondyloarthropathies, mainly recurrent multifocal osteomyelitis: comparison of whole-body AS. Recent developments offer the promise of more exten- MR imaging with and correlation with clinical and sive and accurate detection and staging of the disease, in laboratory data. Radiology 2009;252(3):842–851 terms of anatomical coverage (with the study of peripheral 13 Schanz S, Henes J, Ulmer A, et al. Magnetic resonance imaging joints becoming feasible) and in terms of protocol refine- findings in patients with and musculoskel- – ment with a probable increasing role for diffusion-weight- etal symptoms. 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