imaging of juvenile idiopathic arthritis

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Pediatr Radiol (2006) 36: 743758 DOI 10.1007/s00247-006-0199-x MINISYMPOSIUM Karl Johnson Imaging of juvenile idiopathic arthritis Received: 19 October 2005 / Revised: 21 January 2006 / Accepted: 6 February 2006 / Published online: 2 June 2006 # Springer-Verlag 2006 Abstract Over the past decade there have been consider- able changes in the classification and imaging of juvenile idiopathic arthritis (JIA). Radiology now has a consider- able role in the management of JIA, the differential diagnosis, monitoring disease progression and detecting complications. The different imaging modalities available, their role and limitations are discussed in this article and the various disease features that the radiologist should be aware of are described. An approach to the imaging of the child with joint disease and in the monitoring of disease complications are also discussed. Keywords Joints . Arthritis . Inflammation . Juvenile idiopathic arthritis . Children Introduction Advances and improvements in musculoskeletal imaging have dramatically improved the service that radiologists can now offer the paediatric rheumatologist. The aim is to assist in the initial diagnosis of juvenile idiopathic arthritis (JIA), to detect any disease complications at an early stage and help facilitate the childs optimum management. As a radiologist there is a need to be aware of the value and limitation of the different imaging modalities used in the investigation of the child with bone or joint symptoms. Consideration has to be given to the age and stage of development of the child, the symptoms under investiga- tion and the clinical question being considered. The role of each of the different imaging modalities in JIA and the variety of pathologies that can be seen are discussed in this article, and an update of current radiological research is provided. Since the current JIA classification has only been in use since the year 2000 and is still not universally adopted, much of the research and published reports in childhood arthritis use the older juvenile chronic arthritis (JCA) and juvenile rheumatoid arthritis (JRA) classifications. In this article the term JIA is used exclusively but it is accepted that many of the quoted references refer to JCA and JRA [14]. The different classifications and the subgroups are compared in Table 1. Imaging modalities Radiography Conventional radiographs are the most readily available, quick and inexpensive method of evaluating a joint. For the rheumatologist they provide an important baseline inves- tigation and help to exclude other causes of joint pain and swelling such as tumours, trauma, skeletal dysplasias and infection. It must be remembered that in the paediatric skeleton there is often a significant cartilaginous compo- nent and radiographs are unable to accurately detect any damage or change to this cartilage [4, 5]. The major drawback of radiographs in JIA is that they cannot visualize synovial hyperplasia within a joint, so they are unable to provide any relevant information about the degree of inflammatory change. Those early radio- graphic changes that are visible reflect the hypervascularity and inflammatory response that accompanies this synovial hypertrophy. This can cause soft-tissue swelling, periartic- ular osteopenia and epiphyseal remodelling and widening. If the onset of JIA is relatively recent, any initial radiographs can be normal or only show minor non- specific changes [4, 6, 7]. Prolonged synovial proliferation will lead to cartilage loss and bone damage, which radiographically is seen as loss of joint space and erosive changes along the joint margins (Fig. 1). Progressive joint damage may even- tually lead to bony ankylosis, with resultant loss of function [6, 7]. The radiographic features of chronic JIA K. Johnson (*) Radiology Department, Birmingham Childrens Hospital, Steelhouse Lane, Birmingham, B4 6NH, UK e-mail: [email protected] Tel.: +44-121-3339735 Fax: +44-121-3339726

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Page 1: Imaging of juvenile idiopathic arthritis

Pediatr Radiol (2006) 36: 743–758DOI 10.1007/s00247-006-0199-x

MINISYMPOSIUM

Karl Johnson

Imaging of juvenile idiopathic arthritis

Received: 19 October 2005 / Revised: 21 January 2006 / Accepted: 6 February 2006 / Published online: 2 June 2006# Springer-Verlag 2006

Abstract Over the past decade there have been consider-able changes in the classification and imaging of juvenileidiopathic arthritis (JIA). Radiology now has a consider-able role in the management of JIA, the differentialdiagnosis, monitoring disease progression and detectingcomplications. The different imaging modalities available,their role and limitations are discussed in this article and thevarious disease features that the radiologist should beaware of are described. An approach to the imaging of thechild with joint disease and in the monitoring of diseasecomplications are also discussed.

Keywords Joints . Arthritis . Inflammation .Juvenile idiopathic arthritis . Children

Introduction

Advances and improvements in musculoskeletal imaginghave dramatically improved the service that radiologistscan now offer the paediatric rheumatologist. The aim is toassist in the initial diagnosis of juvenile idiopathic arthritis(JIA), to detect any disease complications at an early stageand help facilitate the child’s optimum management. As aradiologist there is a need to be aware of the value andlimitation of the different imaging modalities used in theinvestigation of the child with bone or joint symptoms.Consideration has to be given to the age and stage ofdevelopment of the child, the symptoms under investiga-tion and the clinical question being considered. The role ofeach of the different imaging modalities in JIA and thevariety of pathologies that can be seen are discussed in thisarticle, and an update of current radiological research isprovided.

Since the current JIA classification has only been in usesince the year 2000 and is still not universally adopted,much of the research and published reports in childhoodarthritis use the older juvenile chronic arthritis (JCA) andjuvenile rheumatoid arthritis (JRA) classifications. In thisarticle the term JIA is used exclusively but it is acceptedthat many of the quoted references refer to JCA and JRA[1–4]. The different classifications and the subgroups arecompared in Table 1.

Imaging modalities

Radiography

Conventional radiographs are the most readily available,quick and inexpensive method of evaluating a joint. For therheumatologist they provide an important baseline inves-tigation and help to exclude other causes of joint pain andswelling such as tumours, trauma, skeletal dysplasias andinfection. It must be remembered that in the paediatricskeleton there is often a significant cartilaginous compo-nent and radiographs are unable to accurately detect anydamage or change to this cartilage [4, 5].

The major drawback of radiographs in JIA is that theycannot visualize synovial hyperplasia within a joint, sothey are unable to provide any relevant information aboutthe degree of inflammatory change. Those early radio-graphic changes that are visible reflect the hypervascularityand inflammatory response that accompanies this synovialhypertrophy. This can cause soft-tissue swelling, periartic-ular osteopenia and epiphyseal remodelling and widening.If the onset of JIA is relatively recent, any initialradiographs can be normal or only show minor non-specific changes [4, 6, 7].

Prolonged synovial proliferation will lead to cartilageloss and bone damage, which radiographically is seen asloss of joint space and erosive changes along the jointmargins (Fig. 1). Progressive joint damage may even-tually lead to bony ankylosis, with resultant loss offunction [6, 7]. The radiographic features of chronic JIA

K. Johnson (*)Radiology Department, Birmingham Children’s Hospital,Steelhouse Lane,Birmingham, B4 6NH, UKe-mail: [email protected].: +44-121-3339735Fax: +44-121-3339726

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are relatively slow to develop and their interpretation andcategorization has significant interobserver variability [8,9]. The early radiographic features of JIA are non-specific. A number of radiographic scoring systems forJIA have been developed, some of which have beenmodified from adult systems, but their use andacceptance is not universally agreed [6, 9–13]. In theauthor’s own institution the clinical assessment offunction and disability of a joint are usually moreimportant monitors of disease progress than any radio-graphic changes. Radiographs are typically only ob-tained for children in whom there is has been asignificant or rapid alteration in symptoms or whensurgical intervention is being considered. Radiographsare important in the assessment of bone maturationand evaluating any limb length discrepancy [14].

Sonography

Sonography is a simple, rapid and inexpensive method ofevaluating joint swelling. There is no radiation exposurerisk and in the majority of cases there is no need to sedatethe child. Technical difficulties can occur in the youngerchild with localized joint tenderness and pain as they willbe reluctant for the limb to be handled and moved. This willreduce their compliance and may make the US examinationmore difficult. The assistance of the child’s carers andsuitable distraction techniques are crucial. Additionally inthe small child, obtaining a satisfactory acoustic window to

allow a proper evaluation of the internal structures of a jointcan be problematic. The visualization of any intraarticularstructures is significantly improved by the use of high-frequency (12–15 MHz) linear probes. The consequent lossof depth with these higher frequencies is not normally anissue when imaging on the smaller scale of a young child’sjoint.

Sonography is more sensitive than radiography orclinical examination in the detection of effusions, synovialthickening and synovial cysts [15, 16]. Sonography willreadily distinguish between joint fluid and inflamedsynovium, the latter appearing as a thickened, irregularand nodular relatively hyperechoic (compared to jointfluid) lining around the joint space.

Serial US is useful in monitoring disease activity and inevaluating any response to therapy. An increase in the sizeand distribution of synovium suggests active disease, whilea reduction in the volume of joint fluid corresponds withclinical improvement. This change in fluid volume appearsto occur faster than alteration in the size of the synovium[16–20].

Colour Doppler will give an indication of the degree ofsynovial hypertrophy and enables assessment of its vascu-larity. In some cases, the use of contrast enhancement hasbeen shown to improve the detection and assessment of thisvascularity [21, 22].

Normal cartilage is seen as a hypoechoic structure with asmooth outline over the bone surfaces. When there is jointinflammation there may be thickening of the cartilage,which often then has a slightly irregular outline. In chronic

Table 1 Comparison of the different classifications and subgroups

Juvenile idiopathic arthritis(International League ofAssociations for Rheumatology)

Juvenile chronic arthritis(European LeagueAgainst Rheumatism)

Juvenile rheumatoid arthritis (AmericanCollege of Rheumatology)

Adultequivalent

Age at onset(years)

<16 <16 <16

Minimumduration ofsymptoms

6 weeks 3 months 6 weeks

Subtypes Systemic arthritis Systemic onset JCA Systemic onset JRA Adult Still’sdisease

Oligoarthritis OligoarticularPersistent Pauciarticular JCAExtended Pauci- to polyarticular JCAPolyarthritis Polyarticular JRA (RhF

does not alter theclassification

Rheumatoidarthritis

RhF-negative Polyarticular JCARhF-positive Juvenile rheumatoid arthritis (JRA)Enthesitis-related arthritis Excluded Juvenile spondyloarthropathies (including juvenile

ankylosing spondylitis, juvenile psoriatic arthritis,Reiter syndrome, arthropathies of IBD

Psoriatic arthritis Excluded Psoriaticarthritis

Other

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disease, erosions and cartilage thinning can also bedetected [15, 17, 19]. However, in the larger jointsvisualization of the whole of the articular surface maynot always be possible (Fig. 2).

MR imaging

Over the past decade the increasing use of MR imaging andthe advances in more functional MR techniques haveimproved the assessment of joint disease in JIA. Theseadvances have allowed the radiologist to be more proactivein the management of the disease. MR imaging is superiorin detecting inflammatory changes in the joint and cartilagedamage than ultrasonography or plain radiography. It isable to accurately evaluate the later manifestations of JIA,including erosions, loss of joint space, cartilage damageand ligamentous involvement [4, 15, 23]. Recent advancesshow that a quantitative assessment of synovial hypertro-phy may be possible [24].

Patient preparation

As with any aspect of paediatric imaging it is important thatthe child is fully informed of the process as much aspossible. In the younger or uncooperative child, sedation orgeneral anaesthesia may be required. Often, in JIA, contrastenhancement is used, therefore either prior venous cannu-lation or the application of local anaesthetic cream isuseful.

Coil selection is important and the basic principle ofhaving increased signal-to-noise ratio and a small field-of-view should be applied [25]. Improved signal-to-noise ratiocan be achieved by the use of phased-array or send-receivecoils. Manufacturers now produce a wide variety of coilsfor numerous anatomical areas, including the temporo-mandibular, shoulder and knee joints and these should beused whenever possible. In the young small child wrap-around coils are often useful.

Choice of sequences

The choice of imaging sequences and whether standardspin-echo or fast spin-echo techniques are used is verymuch dependent on the radiologist’s own preference,experience and the routine practice in that institution.While it is not appropriate to dictate which sequencesshould be used, it is important the radiologist is aware ofthe pathological processes and clinical issues that need tobe adequately imaged in JIA [25, 26].

Imaging synovium

The inflamed thickened synovium is the principle patho-logical process in JIA, but it can be seen in a variety ofother diseases that include any other cause of arthritis,periarticular tumours and conditions such as Perthesdisease [23].

Within the normal joint there is a thin rim of synovialtissue lining the articular surfaces. This normal synoviumproduces a small amount of fluid to lubricate the joint and italso provides nutrients to the underlying relativelyhypovascular cartilage. Normal physiological synoviumis of low signal intensity on both T1-W and T2-W imagesand is seen as a thin smooth rim over the cartilage that is nomore than 2 mm thick, with no focal areas of irregularity ornodularity. This normal synovium will show some en-hancement following gadolinium administration [27–29].

The abnormal inflamed synovium seen in JIA is, incontrast, thickened, irregular and may have a wavy outline.It is low-to-intermediate signal intensity on T1-W imagesand high signal intensity on T2-W sequences. The signalintensity of this inflamed synovium may be similar to thatof any associated joint effusion on both T1-W and T2-Wstandard spin-echo sequences. The use of fast spin-echoand very heavily T2-W sequences will improve thediscrimination between joint fluid and synovium [15, 23,29–31]. Both will remain high signal but there will be more

Fig. 1 DP radiograph of the wrist of a child with JIA. There isminor periarticular osteopenia with some metaphyseal widening.There are some early erosive changes, particularly affecting the baseof the third metacarpal and carpal bones. There is some loss of jointspace around the carpal bones

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contrast between them. The optimum method for differ-entiating inflamed synovium from joint effusion is by theuse of gadolinium-enhanced T1-W sequences. The use offat saturation will reduce the signal from the adjacent fattymarrow and highlight the contrast enhancement. Alterna-tively the use of pre- and post-contrast medium adminis-tration subtraction techniques will improve synoviumdetection [4, 23] (Figs. 3, 4 and 5). Inflamed synoviumshows rapid enhancement after the IV injection of gado-linium and it is this rapid enhancement that helpsdifferentiate active hypervascular synovium from fibrousinactive synovium. Fibrous synovium enhances eitherheterogeneously or poorly [15]. There are some reportsthat indicate that the rate of uptake by synovium could beof use in assessing the degree of inflammatory responsewithin a joint [31, 32]. When performing post-gadoliniumadministration sequences it is important that the sequencesare performed within minutes of the injection of contrastmedium as synovial tissue has no tight junction orbasement membrane and gadolinium compounds willdiffuse into the joint space and gradually increase thesignal intensity of adjacent fluid [33]. This is usually not aproblem when imaging a single joint, but may causedifficulties if more than two joints are to be imaged duringthe same appointment. If more than one joint is beingimaged the post-gadolinium administration sequences onall the joints should be done consecutively. In children astandard dose of 0.1 mmol/kg is sufficient; higher doses ofgadolinium have been shown to a give limited benefit indetermining the quantity of synovial inflammation [34].

In a number of studies, predominantly in adults,contrast-enhanced T1-W sequences have been used toevaluate the severity of the inflammatory arthritis [31], andthis technique is now being used in children [24]. These

studies have quantified the number of joints involved,measured synovial volume, and also looked at the rate ofuptake of gadolinium within the synovium [32, 35, 36]. Incurrent clinical practice the presence or absence ofinflamed synovium is often all that is required by therheumatologists, but this may change with furtheradvancements in drug therapy. If a better measurement ofdisease activity is required then synovial volumes can bedetermined, but these are not typically part of routinepractice as they are particularly time consuming, in bothsequence selection and postprocessing. The use of dynamiccontrast enhancement measurements is still not generallypart of standard practice [32]. It is important that if thesenew techniques are to be utilized in routine clinical practicethere is proper reliability testing done to assess theirvalidity.

Imaging cartilage

In simple terms there are three types of cartilage in a child’sskeleton: growth, epiphyseal and articular. The amount ofgrowth cartilage present will obviously depend upon theage of the child. The epiphysis of the young infant istypically composed entirely of cartilage. Discriminationbetween epiphyseal and articular cartilage is important andis best achieved with T2-W and proton-density-weightedsequences, particularly fast spin-echo sequences [37]. OnT2-W images, physeal cartilage is of very high signalintensity while the epiphyseal cartilage is of high, butslightly lower intensity. The use of fat-saturated techniqueswill reduce the marrow signal from adjacent bone and mayimprove the imaging of the cartilage [4, 15, 37, 38] (Fig. 6).

Fig. 2 Sonography of a hip in a 13-year-old. a This synovium is thickened (3.5 mm) and b there is a large joint effusion

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The use of T1-W spoiled gradient-echo volume acquisi-tions sequences (spoiled gradient-recalled acquisition atsteady state, SPGR, or fast low-angle shot, FLASH;depending on the machine manufacturer) allows imagesto be analysed using multiplanar reformatting with verythin slices. There is good resolution of cartilage, which is ofhigh signal, with any defects appearing as low signalchange. These sequences enable the detection of subtlecystic irregularities and focal defects with relatively highsensitivity [37–39]. The volume acquisition also poten-tially allows volume and surface area measurements to bemade of the cartilage, which may be of potential value inassessing long-term therapeutic response. While thesesequences are very useful, they may involve a considerablylonger imaging time, which can cause problems, particu-larly when scanning the younger child, who may not bevery compliant. The use of parallel imaging techniques andimproved MRI technology has reduced scan times andthese volume sequences are becoming more routinely usedin clinical practice.

There is currently ongoing work that is looking at the T2relaxation times of cartilage. These specialized T2 mappingsequences allow an assessment of the biochemical andbiophysical changes in the extracellular cartilage and

provide information about very early degenerative damageprior to any erosive damage being seen by moreconventional imaging [40, 41].

Marrow oedema

Marrow oedema and soft-tissue oedema are best appre-ciated on STIR images; however, T2-W fat-saturatedimages will also give relatively good contrast. The use ofcontrast-enhanced, T1-W fat-saturated sequences willdetect areas of inflammation within joints [15].

Imaging strategies

There are no clearly defined imaging protocols for JIA. Thechoice of which imaging modality to use and its timing arevery much patient-dependent. These choices depend on theclinical problem and the resources available.

In simple terms, children will fall into two broadcategories: firstly those who present with a relatively acuteswollen joint (or joints) and in whom no firm diagnosis hasbeen made and secondly those children in whom thediagnosis of JIA is established, but in whom there has beenan alteration of clinical symptoms or there are questionsabout the effects of current treatment.

For the previously well child who presents with an acutejoint problem and who has been fully assessed by anexperienced paediatric rheumatologist, often only a radio-graph of the involved joint is necessary. This radiograph isimportant in excluding other causes of joint swelling, suchas trauma, osteoid tumours and dysplasias. In some cases,if the rheumatologist is confident of the diagnosis of JIA,no imaging may be requested at all. If confirmation of thepresence of an effusion is needed then both US and MRimaging have been shown to be more sensitive in theirdetection than clinical examination [15, 16, 19, 27].

In children, newly diagnosed as suffering from anoligoarthritis JIA, there are preliminary studies whichsuggest that MR imaging of clinically asymptomatic jointswill detect early synovitis. Follow-up of these casesappears to indicate that those children who had positivefindings on their MR images are at increased risk of diseaseextension and conversely a negative MR examination atpresentation appears to suggest a good prognosis. Thiswork indicates that MR imaging will play an increasingrole in the evaluation of patients with newly diagnosed JIAand in the investigation of patients in whom there areequivocal clinical findings [42].

Alternatively the request for imaging an acutely swollenjoint in a previously well child may be from a clinician whois less experienced in dealing with childhood arthropathies.In this circumstance, radiology needs to confirm any jointpathology and provide a differential diagnosis. Radio-graphs again are important in excluding bony lesions as acause of the swelling, but have limited value in confirmingthe diagnosis of JIA. Sonography and MR imaging are

Fig. 3 Sagittal, post-gadolinium administration, T1-W fat-saturatedimage of the knee in a child with JIA. The high signal intensityaround the infrapatellar fat pad (arrow) and the small area aroundthe distal femur (arrow) indicate enhancing synovium. The syno-vium has a slightly irregular outline and is marginally thickened,particularly around the menisci. There is some slight irregularity ofthe infrapatellar fat pad (arrowhead). These appearances areborderline abnormal. This patient went on to develop more severechanges with a significant joint effusion and elevated bloodinflammatory markers within 3 months of the MRI examination

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more sensitive than clinical examination in detectingsynovial hypertrophy and joint effusions [15, 23].

In the acute case, the knee has been the most frequentlystudied joint with MR imaging. This is as a consequence ofthe knee being one of the most commonly affected joints inJIA and also because it is relatively easy to image [4, 23,43]. The early MR imaging features of JIA in the knee jointare irregularity of the infrapatellar fat pad, lymphadeno-pathy and joint effusion. If these features are present withinthe knee then it is important that gadolinium chelate isadministered to confirm the presence and then fullydelineate the degree of synovial hypertrophy. If contrast-

enhanced sequences are not obtained then the presence ofsynovial hypertrophy may not be fully appreciated and thediagnosis of JIA delayed. The radiologist has an importantrole in suggesting the diagnosis of JIA as the clinician maynot be fully aware of the diagnosis.

Regardless of the type of referral, in patients in whomthere is an acutely swollen joint, the diagnosis of sepsismust always be excluded, and if sepsis is suspected promptjoint aspiration and/or lavage is mandatory. Infectionwithin a joint can be severely destructive, but earlyappropriate treatment is curative. Care must be taken inexcluding sepsis in the child who has received antibiotics

Fig. 4 Sagittal images of the knee of a 13-year-old girl. The T1-W(a) and T2-W (b) sequences both demonstrate a joint effusion(arrow) and lymph nodes (arrowheads). On both sequences it isdifficult to differentiate effusion from synovial hypertrophy. The

gadolinium-enhanced T1-W sequence (c) shows marked enhance-ment of synovium (arrow) within the knee joint. Differentiation offluid and synovium is much easier. The lymph nodes also enhance(arrowheads)

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for whatever reason as the diagnostic features may beminimized.

In the child with a known diagnosis of longstanding JIA,separate imaging issues are encountered. The imagingapproach should be patient-centred, and the radiologistand paediatric rheumatologist therefore need to have regularmultidisciplinary meetings to discuss the imaging findingsof each patient and plan further investigations as appropriate.

Routine radiographs of a child’s joints regardless of theirsymptoms at each clinic visit are not indicated, as they arepoor predictors of how the underlying disease is beingcontrolled, and any new features are relatively slow todevelop [4, 44, 45]. Once the diagnosis of JIA isconfirmed, radiographs are only indicated when there hasbeen a change in the child’s symptoms or alteration in theirmanagement. When there has been an acute change insymptoms, radiographs may demonstrate signs of atraumatic injury, intraarticular loose bodies or jointsubluxation.

If there are concerns about an acute inflammatoryreaction in a joint with underlying chronic changes, bothultrasonography and MR imaging can identify those jointswith a significant effusion that may be amenable toaspiration or intraarticular steroid injection, with MRimaging being the most sensitive modality for detectinginflamed synovium [4, 15, 16, 23, 39, 46]. However, thereneeds to be some caution in attributing all the synovialhypertrophy that is seen in a chronically affected joint tothe autoimmune process because synovial hypertrophy canoccur from the underlying degenerative process. Correla-tion with biochemical and haematological markers of jointinflammation will be needed in some cases.

Fig. 5 T1-W images of the temporomandibular joint (a) before and(b) after gadolinium administration. The contrast-enhanced imagehas been fat-saturated to show enhancement of the temporoman-dibular joint anteriorly (arrow) and a small enhancing nodule withinthe ramus of the mandible (curved arrow)

Fig. 6 Coronal, proton-density fast-spin echo image of the knee of a4-year-old boy. At the distal end of the femur the central ossifiedepiphysis is of low signal intensity, similar to that of the proximalfemur. This epiphysis is surrounded by high-to-intermediate signaldensity growth cartilage. Along the joint margins the articularcartilage is of slightly high signal intensity, as is the physis

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Fig. 7 Serial images of a 14-year-old child with severe JIA. a, bAP (a) and lateral (b) radiographs of the ankle demonstrate erosivechanges and sclerosis along the articular margins of the ankle joint.There is deformity of the ankle joint. c A coronal T1-W post-gadolinium administration fat-saturated image of the same ankleperformed within 1 week of a and b shows marked enhancement inthe bone and small enhanced cystic areas within the distal tibia.

The corresponding areas appear normal on the initial radiographs.d, e AP (d) and lateral (e) radiographs of the same ankle 12 monthslater. These demonstrate worsening erosive changes and furtherjoint destruction within the distal tibia, with subchondral cystformation. These subchondral changes are at the site of theenhancement of the MR image. This demonstrates the predictivevalue of MR imaging

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Radiological features

Soft-tissue swelling and joint effusions

Periarticular soft-tissue swelling is one of the commonestearly features of JIA and typically the diagnosis is madeclinically. On radiographs the detection is easier in thesmall joints of the hand and feet, where it is usually seen asfusiform swelling around the digits. In enthesitis-relateddisease the soft-tissue swelling can be eccentric andirregular [44, 45]. Sonography and MR imaging are moresensitive in delineating the swelling and any associatedeffusions [15]. A complication of some cases of JIA is thatthe child may develop persisting lymphoedema, typicallyof the lower limb, with soft-tissue swelling extendingbeyond the joint [47].

Osteopenia

Both juxtaarticular and generalized osteopenia are rela-tively common early findings on radiographs. Thejuxtaarticular changes reflect localized hyperaemia aroundthe joint that causes trabecular atrophy and reducedendochondral bone formation. Juxtaarticular osteopenia

Fig. 8 AP radiographs of the left (a) and right (b) wrist in a girl. There were significantly worse clinical symptoms associated with the rightwrist, which as a consequence of an increase in vascularity has caused asymmetrical ossification of the carpal bones. The ossification isaccelerated on the right

Fig. 7 (continued)

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must not be confused with the metaphyseal lucent zonewhich can occur in childhood leukaemia [48].

A more generalized osteopenia results from the chro-nicity of the disease, widespread disuse atrophy and long-term steroid usage. This osteopenia will predispose thechild to fractures that most commonly occur in thevertebrae. DEXA and US scanning are currently used foranalysing, researching and guiding treatment of thisreduced bone mineral density [49].

Periostitis

Periosteal new bone formation is a relatively frequentmanifestation of JIA, occurring in any long bone, but ismost common in the periarticular region of phalanges,metacarpals and metatarsals. Periostitis can occur at anytime during the disease process and is believed to be aconsequence of inflammation of the joint capsule and theadjacent tendon insertions. The relative ease with which theperiosteum can be elevated and new bone formed inchildren is probably a factor for its increased incidence inJIA compared with adult rheumatoid disease. In some casesthe changes within the digits can be marked, causingenlargement and squaring of the bone. Diffuse swelling ofthe finger or toes with associated periosteal new boneformation is a classic feature of psoriatic arthropathy, oftenwith the bone changes preceding any dermatologicalfeatures [7, 8, 45, 50].

Erosions

Erosions are one of the endpoints of the disease process inJIA and indicate destruction of both bone and cartilage.Erosions often occur at the insertion site of the intraosseousligaments and at the sites of synovial reflection, as theseareas have relatively less overlying protective cartilage.Erosions can, however, occur at any point along the entirearticular surface of the bone [7, 8, 45, 50].

Radiographs are unable to detect any defect in either thearticular or growth cartilage and so are relativelyinsensitive to early joint damage. Radiographs also tendto underestimate the amount of erosive change within boneas they are relatively insensitive to trabecular bone loss(rather then cortical loss), which is the largest part of theerosion. In the young child there will be generalized loss ofjoint space, reflecting cartilage loss, prior to bony changes.This joint space loss is most commonly seen within thewrist joint causing crowding of the carpal bones [45, 50].

With ultrasonography, erosions are defined as a corticaldefect or break that is greater than 2 mm in width with anirregular floor and acoustic enhancement within theadjacent marrow, seen in both longitudinal and transverseplanes [51]. Sonography is superior to radiography indetecting cortical erosions in sonographically accessibleareas, but is less reliable in detecting intramedullary lesions

Fig. 9 AP radiograph of the ankle in a 6-year-old boy. There isfibula overgrowth and some soft tissue swelling as a consequence ofincreased vascularity

Fig. 10 DP radiograph of the right hand of a 15-year-old boy. Thereis some bone remodelling around the distal radius and ulna. There isradial deviation and carpal crowding

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and those within the centre of larger joints, where there isacoustic shadowing from overlying bone [15, 39, 51].

MR imaging is the most sensitive detector of erosivechanges, and it can clearly delineate between cartilage andbone defects [4, 15, 39]. Erosions are seen as well-circumscribed lesions that are hypointense on T1-W andhyperintense on T2-W images. Erosions will often showmarked enhancement following gadolinium administration[4, 15, 23, 52].

MR imaging is able to demonstrate ill-defined areas ofmarrow oedema and periarticular bone that enhance withgadolinium administration. These abnormal areas appearprior to any radiographic abnormality and it is believedthey represent areas of osteitis, which are a probablepredictor of erosive damage. Hence MR imaging is able todetect inflammatory changes in the bone prior to erosionsdeveloping, which may be useful in the development ofdisease-modifying therapies [53, 54]. For quantifying theamount of erosive damage within a joint, post-gadoliniumadministration sequences are the most sensitive [4] (Fig. 7).

Growth disturbances

In view of the immaturity of the paediatric skeleton, growthdisturbances are a unique feature of JIAwhen compared tothe adult inflammatory disorders. The cause of any growthdisturbances is variable and may be localized or general-ized. The effects of disease chronicity, prolonged steroidtherapy and immobilization will result in a generalizedgrowth retardation. Any soft-tissue and periarticular

inflammation, epiphyseal destruction and joint subluxationthat occur can be associated with muscle spasm that cancreate abnormal mechanical stresses on the bone which willalso influence osseous development [55].

Within the axial skeleton the localized inflammatoryhyperaemia around joints can initially cause acceleratedgrowth, which causes epiphyseal enlargement and earlybone maturation. Around the knee this epiphyseal enlarge-ment will cause widening of the intercondylar notch andsquaring of the lower pole of the patella, which are classicradiographic signs of JIA, but which can also occur inhaemophilia [45, 50]. The initial growth acceleration thatoccurs in the early phase of the disease will cause a relativeincrease in the affected limb’s length. Within the hands andfeet there is earlier ossification of the growth centres of thecarpal and tarsal bones, which will result in a discrepancybetween the child’s estimated bone age and their chrono-logical age. In more longstanding disease, accelerated bonematuration promotes premature fusion of the epiphysealphysis, which ultimately will cause reduced growth anddecreased limb length. If the physeal fusion is asymmet-rical there will be a limb length discrepancy. The degree ofany deformity is worse with younger age of disease onset[56] (Figs. 8 and 9).

In a significant number of children the mandible isaffected by growth abnormalities. There is underdevelop-ment of the jaw (micrognathia) with limitation of bite, whichcan be a significant disability. Radiographic abnormalitiesinclude shortening of the body and ramus, flattening of thecondyles and widening of the intercondylar notch. Ante-gonial notching, which is a concave abnormality on theunder surface of the body of the mandible, is a recognized,but non-specific radiographic, feature of JIA. The notchingis a consequence of mandibular hypoplasia and muscleimbalances acting in the region of the angle causing alteredgrowth. The notching in JIA is typically short and close tothe angle of the mandible (gonion), while in some congenital

Fig. 11 Axial proton density fat saturated sequence of the knee in a13-year-old boy showing popliteal cysts extending around thegastrocnemius muscle

Fig. 12 Axial proton-density fat-saturated image of a 13-year-oldgirl. There is an effusion within the knee joint, which containsnumerous small rice bodies. These bodies are the small low signalintensity flecks within the relatively high signal intensity fluid

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disorders, which include Treacher-Collins syndrome, cam-pomelic dwarfism and neurofibromatosis, the concavity ismore obtuse [57–59]. Any mandibular growth changes mayor may not be associated with temporomandibular joint(TMJ) disease [60]. The use of dedicated TMJ coils hassignificantly improved the quality of MR imaging in thisarea and the use of open- and closed-mouth images will helpdetect any abnormal joint motion and intraarticular discdefects.

Joint deformities

Joint subluxation, dislocation and flexion/extensiondefects can occur in any joint, but are more commonlyseen in the hands and feet. Any of the pathologicalchanges seen in JIA, including erosions, ankylosis, largeeffusions, synovial proliferation, ligament disruption andmuscle imbalances can contribute to this deformity and,more importantly, cause loss of function. In morelongstanding disease there can be new bone andosteophyte formation around the joint margins which

can cause pressure effects on adjacent structures andlimit joint movement [7, 8, 45, 50].

Fig. 13 Lateral cervical spine of a child with JIA. There is fusionand bony remodelling of the facet joints from the C2 level down tothe C6 level. The bones are relatively osteopenic. There wassignificant restriction of movement

Fig. 14 MRI of the foot and ankle in a 7-year-old girl with anenthesitis. Sagittal STIR image of the ankle. a There is bone marrowoedema around the insertion of the Achilles tendon into thecalcaneum (arrowheads) with further soft-tissue oedema around theposterior aspect of the foot. b Sagittal post-gadolinium administra-tion fat-saturated sequence shows enhancement within the bonemarrow at the site of the Achilles insertion (arrowhead) and in thesurrounding soft tissues (arrow)

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In the hands, a variety of finger abnormalities occurwhich include Boutonniere deformity (flexion at theproximal interphalangeal joint and hyperextension at thedistal interphalangeal joint), swan neck deformity (hyper-extension at the proximal interphalangeal joint with flexionat the distal interphalangeal joint) and flexion deformity(flexion at both the proximal and distal interphalangealjoints). These changes are commoner in the polyarticularsubtype, particular the rheumatoid-positive group, andwhile they may be bilateral they are frequently notsymmetrical [61]. Similar changes are also seen in the feet.

In the wrist joint there is abnormal radial deviation,which is in contrast to the ulnar deviation that is seen inadult disease (Fig. 10). Subluxation and dislocation canalso occur in the carpal bones, with the hamate beingparticularly affected. MR imaging will demonstrate thedegree of subluxation and will identify any localized massof synovial tissue, which along with ligament laxity, isoften responsible for causing this subluxation [4, 7, 8].

Valgus or varus deformity can occur at the elbow or kneejoint, either as a consequence of asymmetrical epiphysealovergrowth or significant erosive changes. Due to thismalalignment, abnormal mechanical stresses will be placedon all the joints in the involved limb, which will compoundany deformity. Enlargement of the femoral and humeralheads, together with loss of joint space and remodelling ofthe acetabulum or glenoid may cause hip and shoulder jointsubluxation, respectively. The generalized osteopenia andweakened bone around the hip joint can also causeacetabular protrusion, poor iliac bone development andcoxa vara [62–64]. This is commoner in the older childwho is more continually weight bearing. It has beensuggested that in JIA the protrusion is more cephalic thanthat seen in adult disease. Osteonecrosis of the femoralhead can occur in JIA; this may be a consequence of eitherJIA or joint injections.

Bursitis and synovial cyst formation

Both US and MR imaging are more sensitive in thedetection of synovial cysts and bursae than either clinicalexamination or radiographs. The unexpected finding of asynovial cyst is usually an isolated finding. On post-gadolinium administration MR sequences there is enhance-ment around the wall of the cyst. The cyst may arise fromthe joint capsule or tendon sheath [65–67] (Fig. 11).

Soft-tissue calcification

The presence of soft-tissue calcification around a joint isnot an uncommon finding in JIA and is typically related tojoints that have had intraarticular injection of steroid.Calcification usually occurs within 2–12 months of theinjection [68].

Rice bodies

Rice bodies are believed to result from either synovialproliferation and degeneration or synovial microinfarcts.These result in small pieces (bodies) of synoviumbecoming detached and falling into the joint space. Thesesmall detached bodies vary in consistency, size and shape,and can contain coarse collagenous fibres, fibrin or elastin.Macroscopically they resemble tiny grains of rice. Ricebodies may occur in patients with other types of jointdisease, such as tuberculous arthritis, agammaglobulinae-mia and hypogammaglobulinaemia.

On US imaging there is a joint effusion of heterogeneousechogenicity. On MR imaging the fluid still has high signalintensity on T2-W sequences, but there are numerous,small non-homogeneous floating bodies of low signalintensity within it [69] (Fig. 12).

Fig. 15 AP radiographs of the sacroiliac joints in a teenager. Thereis sclerosis bilaterally indicating sacroiliitis

Fig. 16 A 12-year-old boy with sacroiliitis. Oblique-coronal, T1-Wfat-saturated images of the sacroiliac joints. There is widening andenhancement within the left SI joint. There is enhancement in thesurrounding bone. There is minor enhancement around the right SIjoint

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Ankylosis

The initial osteoporosis, soft-tissue swelling and synovialhypertrophy may cause joint space widening. In morechronic disease, particularly in those children who are RhF-positive, there will be gradual loss of joint space due tocartilage damage and bone erosions, which in the moresevere cases may lead to bony ankylosis. This is mostfrequently seen in the wrist joint and in the facet joints ofthe cervical spine [4, 7, 8, 45, 70]. In some cases it ispossible that a pseudarthrosis may develop to compensatefor the loss of function that occurs with the ankylosis [71](Fig. 13).

Ligament/tendon abnormalities

Inflammation around the sites of tendon and ligamentinsertion (enthesitis) can cause periosteal changes in thebone. The amount of new bone formation can be significantand result in either bony spurs or prominent osteophytes [7,45, 50]. On MR imaging this enthesitis is seen as highsignal at the site of tendon insertion on STIR sequenceswith further signal changes also being seen in the adjacentmuscle; there may be an associated bursitis. These areastypically show enhancement following gadolinium admin-istration. MR imaging can demonstrate fluid and inflamedsynovium around the tendon sheaths and may identifysubclinical tendon rupture [23].

Within joints, synovial hypertrophy will cause damageand atrophy of intraosseous ligaments. In the knee, whichhas been most actively studied, the cruciate ligaments canbe either mildly or severely atrophic and synovial prolif-eration extending over the meniscal surfaces is believed toresult in meniscal hypoplasia and degradation, which mayprecede a tear. These findings in the knee joint are morecommon in children who have had poorly controlled JIAfor at least 4–5 years, but they can occur in children with adisease duration of less than a year [23]. Around the wrist,ligament laxity can cause horizontal and radial deviation ascompared to ulna deviation encountered in adults. (Fig. 14).

Axial skeleton

Involvement of the cervical spine is commoner in thepolyarticular (RhF-positive) subtype, while lumbar spineand sacroiliac disease is more often seen in the enthesitis-related group, particularly in those children who are HLA-B27 histocompatibility antigen-positive.

In the cervical spine there is hypoplasia and squaring ofthe vertebral bodies with synovial proliferation around thefacet joints. The intervertebral disc space can becomenarrowed and irregular. In more severe longstandingdisease, ankylosis of the apophyseal and facet joints occurscausing significant immobility. Erosions can be seenaround the odontoid process, and the synovial proliferationaround the C1-C2 articulation can lead to ligament laxityand instability. On a lateral radiograph there will be

widening by 5 mm of the gap between the posterior edge ofthe anterior arch of the atlas and the anterior surface of theodontoid. This gap may show a dynamic change withflexion/extension views [4, 72].

In the lumbar spine there is more often sclerosis of thevertebral corners, loss of disc height, squaring of theanterior vertebral surface, syndesmophyte formation andbony ankylosis. Compression fractures can occur at anylevel of the spine, but are particularly notable in the lumbarand thoracic regions if there has been long-term steroid use.

Sacroiliac disease can be difficult to detect clinically andradiographs are also relatively poor at evaluating this joint.There may be joint space widening, marginal irregularityand sclerosis that can eventually lead to ankylosis. Any ofthese features may be unilateral, bilateral or symmetrical,but can be slow to develop and correlate poorly withclinical function [73–75].

MR imaging will demonstrate periarticular marrowoedema and show enhancement within the joint spaceand surrounding bone, reflecting an osteitis. MR imaging ismore sensitive than clinical evaluation in detecting sacro-iliac disease and better at discriminating between activedisease and chronic changes [74, 75] (Figs. 15 and 16).

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