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Magnetic resonance imaging of the immature skeleton Peter Boavida, Lil-Sofie Muller and Karen Rosendahl Acta Radiol 2013 54: 1007 DOI: 10.1177/0284185113501945 The online version of this article can be found at: http://acr.sagepub.com/content/54/9/1007

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Review article

Magnetic resonance imaging of the immature skeleton Peter Boavida1, Lil-Sofie Muller2 and Karen Rosendahl3 1

Department of Radiology, Great Ormond Street Hospital, London, UK; 2Section for Paediatric Radiology, Oslo University Hospital, Oslo; Department of Radiology, Haukeland University Hospital, Bergen, Norway Correspondence to: Peter Boavida. Email: [email protected]

3

Abstract Magnetic resonance (MR) is unique in its ability to allow assessment of bone marrow, epiphyseal, physeal, and articular cartilage as well as tendons and ligaments. An understanding of skeletal maturation and the accompanying changes on MR is of utmost importance in pediatric radiology. In particular, it is important to recognize the normal spectrum related to ossification and marrow transformation. This review will include a brief description of main indications and common pitfalls in musculoskeletal MR in children. Also, we will focus on the MR appearance of the growing pediatric skeleton on the most commonly used sequences.

Keywords: Musculoskeletal system, radiography, magnetic resonance imaging, pediatric rheumatic diseases, bone marrow Submitted August 20, 2012; accepted for publication June 27, 2013

Indications for MR in the imaging of the musculoskeletal system in children Trauma AP and lateral radiographs are the mainstay of trauma imaging in an acute setting and other than in spinal trauma with neurological compromise, magnetic resonance (MR) has no place immediately after the injury. Instead, MR is valuable in assessing ligamentous and meniscal injuries and in post-traumatic complications, including epiphyseodesis (1). Physeal fractures Physeal fractures are common and are not infrequently complicated by growth arrest and MR is able to characterize these injuries and aid in determining prognosis (2, 3). The physis is involved in up to one-third of all pediatric fractures (4). The zone of provisional calcification is the weakest region of the growing skeleton and MR complements radiography in the assessment of fractures of the physes and is highly sensitive and specific in the assessment of these injuries (5). In addition, the diagnosis of unsuspected physeal fractures in for example examinations performed for assessment of the menisci or ligamentous structures of

the knee is not infrequent (6). Diagnosis of these injuries is vital as growth arrest occurs in approximately 15% of all physeal fractures and in as many as 40% and 20% of distal femoral and distal tibial fractures, respectively (2, 3, 7). An imaging protocol enabling optimal assessment of the physis includes coronal T1-weighted (T1w) images, sagittal fat-suppressed FSE PD, T2-weighted (T2w) and a threedimensional (3D) coronal fat-suppressed SPGR sequence (8). Findings include widening of part of the physis, metaphysal (Salter Harris type II), or epiphyseal (Salter Harris type III) fracture lines, periosteal elevation, and bone marrow edema (6). MR is also useful in imaging patients in whom physeal fractures have resulted in disruption of the physis and formation of bone bridges. Bony bridges appear as a low signal intensity interruption of the high signal intensity physeal cartilage (8). Proton density and T2w imaging demonstrate associated marrow and soft-tissue pathology and growth recovery lines are best imaged on the T1w sequence as a band of low intensity. Resection of bridges that comprise ,50% of the surface area of the physis results in a good prognosis with a return to growth (9). Larger bony bridges often require more extensive surgery. Disruption of the physis can also occur without the formation of a bony bridge and is characterized by thickening or irregularity of the physis. Acta Radiologica 2013; 54: 1007–1014. DOI: 10.1177/0284185113501945

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Ligamentous and meniscal injuries Medial meniscal tears are more common in children than lateral meniscal tears and MR has been shown to be up to 100% sensitive and 89% specific for meniscal tears in the immature skeleton (10, 11). The menisci should be of uniformly low signal on all sequences. Increased intra-meniscal signal in children is regarded as normal in morphologically normal menisci whereas extension of increased signal to the articular surface is diagnostic of an undisplaced tear (12). Bucket handle tears are among the commoner tears in children and findings include the “double PCL” sign where the displaced meniscal fragment is located under and parallel to the PCL. As in adults common errors in diagnosis of meniscal tears result from the failure to appreciate normal structures including the popliteal tendon, transverse meniscal ligament, and menisco-femoral ligaments of Humphrey and Wrisberg (10). Lateral discoid menisci are more common than medial discoid menisci (13) and both types commonly present with pain and “locking” in early childhood (14). A transverse diameter .15 mm of the meniscal mid-body is in keeping with a discoid meniscus and the diagnosis is therefore made on MR when there is continuity of the anterior and posterior horns on three or more 5-mm-thick contiguous sagittal slices (13). There is an increased incidence of tears, premature degeneration, and displacement in discoid menisci (10).

Infection Early diagnosis is of vital importance in osteomyelitis. Complications of infection include premature closure of the physis, slipped epiphysis, fracture, and septic arthritis (15). Over 90% of cases involve a single bone and the long bones are most commonly involved, particularly sites of greatest growth such as the proximal tibia (16). This can be explained by the fact that osteomyelitis typically arises from blood-borne infection following a bacteremia in infants and young children. Direct introduction of infection following trauma and spreading from adjacent structures is more common in adolescents (16). The metaphysis is frequently the first site that is involved as a result of the rich vascular supply that terminates in slow-flowing venous sinusoid pools in the intra-medullary metaphysis of the immature skeleton. In acute osteomyelitis, the pressure within the metaphysis is high as a result of the inflammatory process and there is outward spread of infection, extending into the subperiosteal space with periosteal elevation followed by involvement of the overlying soft tissues. Intra-medullary, subperiosteal and soft tissue abscesses can develop. In addition, involvement of the physis, epiphysis, and adjacent joint does occur via transphyseal vessels in infants up to 18 months after which age transphyseal vessels involute (16). The development of involucra and sequestra are the hallmarks of chronic infection. Plain radiography is indicated in the initial assessment but osseous changes are not apparent until up to 10 days

after onset (17). The earliest radiographic features include cortical scalloping which results from subperiosteal resorption followed by periosteal new bone formation. MR is the most sensitive modality for the diagnosis of osteomyelitis with a sensitivity of 97– 100% and specificity of 73– 92% and is particularly useful in pelvic and spinal osteomyelitis where radiographic changes can be challenging to identify (18, 19). MR allows assessment of the extent of the bone marrow, cortical and soft tissue changes and can identify early joint involvement. The earliest detectable changes on MR can be identified within 24 –48 h of symptom onset and consist of marrow edema with hyperintense signal in bone marrow and adjacent soft tissue on T2w and STIR sequences and low T1w signal (17). Features of myositis or pyomyositis on MR adjacent to the site of osteomyelitis have been reported in one series to be as high as 60% in infection secondary to a common strain of Staph. aureus (18). The use of intravenous contrast can facilitate the diagnosis of intramedullary and soft-tissue abscess. In addition cortical thickening, sequestration, and fistula formation are readily identified on MR.

Inflammatory conditions Juvenile idiopathic arthritis is a heterogeneous group of arthritides with onset before the age of 16 years and is the commonest chronic rheumatic disease in children (20). The disease is characterized by chronic synovitis resulting in progressive articular destruction. As with US, MR is able to assess synovitis but MR is unique in its ability to provide a comprehensive assessment of the entire articular unit. Contrast-enhanced sequences can demonstrate active hypervascular pannus and have been shown to be more sensitive in the diagnosis of articular cartilage destruction in the knee (21). There is some evidence to suggest that the detection of bone erosions in the wrist is superior on MR when compared with plain radiographs (22). However caution must be exercised when ascribing carpal bony cortical irregularities to bony erosions (see pitfalls section).

Malignancy A description of each of the MR imaging (MRI) characteristics of bony malignancy is beyond the scope of this review. Nevertheless MR is useful in staging primary bone tumors and to a lesser extent in assessing the extent of metastatic bony disease. When staging primary bone tumors it is important to image the entire bone as well as the adjacent joint as this enables accurate delineation of the tumor, identification of skip lesions, and involvement of the joint. Whole-body MR with diffusion-weighted sequences is also increasingly used to identify metastatic bony disease (23).

Other common pediatric conditions Slipped capital femoral epiphysis (SCFE) is a common adolescent hip disorder characterized by the displacement of the proximal femoral epiphysis from the metaphysis

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Fig. 1 Slipped capital femoral epiphysis (a) T1w coronal, (b) T2w sagittal, and (c) STIR coronal sequences. Arrowheads and short arrows indicate bone marrow edema within the femoral metaphysis, evidence which supports a subacute/chronic presentation. The longer arrow in (c) indicates a small hip effusion. These figures have been reproduced with permission from University Hospital of North Norway (UNN), Tromso

through the physis (Fig. 1). The vast majority are idiopathic. Other cases can be attributed to endocrine disorders (24). Complications include avascular necrosis (AVN) and osteoarthritis. The determination of physeal stability is useful in predicting prognosis regarding the subsequent development of AVN (24). Pelvic radiographs of both hips in neutral and lateral views are the gold standard imaging modality if this diagnosis is suspected. Radiological predictors of instability are absence of metaphyseal remodeling and the presence of a hip effusion on ultrasound (24). MR is able to identify early changes in SCFE including diffuse physeal widening and marrow edema along the physis and can be useful in the patients with an atypical presentation or inconclusive radiographs (25). In addition, MR plays an important role in the early diagnosis of complications of SCFE, particularly in AVN where changes on plain radiography are delayed (26). Computed tomography (CT) also has a role although this is generally limited to preoperative planning in severe cases (25).

Essential sequences The underlying principles in MRI of the musculoskeletal system are definition of normal anatomy and detection of abnormal signal or enhancement. Essential sequences include anatomy defining imaging (T1w and proton density) and fluid sensitive sequences (short tau inversion recovery [STIR] and fat-saturated proton density). Post-intravenous and intra-articular contrast sequences are also useful in defining anatomy and characterizing disease.

imaging and this is particularly useful in non-sedated younger patients who cannot hold still for long. However, several studies have shown these faster sequences to be less specific and sensitive in the assessment of the menisci in particular (28, 29).

T1w: conventional spin-echo and fast-spin echo These sequences provide excellent anatomical detail and have the highest specificity for detection of bone marrow and post-traumatic abnormalities. T1w imaging can be acquired using spin echo, fast-spin echo, or gradient echo. Conventional T1w spin echo sequences demonstrate fat better than gradient echo imaging. Gradient echo sequences with fat suppression eliminate chemical shift artifact that can result in distortion of the cartilage-bone interface. It also provides greater contrast. Gradient echo is therefore useful in assessing cartilage and provides excellent contrast between articular cartilage and adjacent effusions which appear dark. The other key use of gradient echo is in the detection of hemorrhage. Ligamentous and meniscal definition, on the other hand, is poor on gradient echo sequences and hence the need to supplement these sequences with proton density imaging. T1w images are useful in distinguishing fractures from contusions as a fracture line can often be identified as linear low signal. Furthermore the exact extent of a bony tumor can be confidently identified on T1w imaging.

Water sensitive sequences Proton density (PD) Proton density sequences are characterized by a high signal-to-noise ratio and provide high spatial resolution. Proton density sequences without fat suppression provide exquisite anatomical detail and are excellent in demonstrating soft-tissue structures, particularly ligaments, tendons, the menisci, and cartilage. The use of fat suppression enables assessment of the bone marrow (27). The time of acquisition can be reduced with fast/turbo spin-echo

STIR and fat-suppressed T2w imaging are the most frequently employed sequences. STIR produces excellent uniform fat suppression and is ideal when a large field of view (FOV) is required. Fatsuppressed T2w imaging typically results in less homogenous fat suppression but is ideal when a smaller FOV is required such as in axial imaging and can cover a large volume quickly. The signal intensity of muscle is usually higher in STIR images than on T2w images and the detection of

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Fig. 2 MR of the proximal femur of a healthy 5-week-old infant. (a) Coronal STIR and (b) axial T1w sequences. The proximal femoral epiphysis is entirely cartilaginous, demonstrating homogenous intermediate signal in both sequences. These figures have been reproduced with permission from University Hospital of North Norway (UNN), Tromso

inflammatory change in muscle can be more difficult to detect on STIR.

Contrast-enhanced imaging The following structures demonstrate enhancement: the normal physis, juxtaphyseal metaphysis, subperiosteal fibrovascular tissues, and epiphyseal vascular canals (1). Normal synovium enhances but is very inconspicuous. Contrast is particularly useful in inflammatory, vascular, and neoplastic processes including infection, juvenile idiopathic arthritis, and avascular necrosis.

Diffusion-weighted imaging Diffusion weighted imaging (DWI) is a functional MR sequence that uses Brownian motion to create tissue-contrast. DWI is not yet part of the standard imaging protocol in pediatric musculoskeletal imaging. However, it has been shown to have a role in detection of active inflammatory changes (30) and a possible future role in the detection of cartilage degeneration (31). DWI is also thought to have a high sensitivity for bone marrow pathology and is particularly used in adult oncology imaging. Tissues with high cellularity like tumors or inflammatory infiltrates will often have restricted water diffusion. This gives a high signal on DWI. DWI with body-background suppression (DWIBS) is a novel diffusion-weighted sequence particularly suitable for whole-body imaging designed for tumor staging and screening for metastases (23).

The normal pediatric skeleton Cartilage There are fundamental differences related to the imaging of cartilage in children compared with adult cartilage. Articular cartilage is avascular and has minimal cellularity instead consisting mainly of a collagen matrix and proteoglycans. Seventy-five percent of the volume of the hypertrophic zone of the physis is cellular (32). Physeal and epiphyseal cartilage is vascular. Physeal cartilage becomes avascular after the age of 18 months.

Fig. 3 Heterogenous hyperintense signal within the cartilage of the carpus just prior to ossification (a) T1w coronal and (b) STIR coronal sequences. The asterisks indicate carpal cartilage just prior to ossification

Epiphyseal cartilage This is the precursor to the bony epiphysis. The secondary physis is structurally similar to the primary metaphyseal physis and is responsible for ossification of epiphyseal cartilage at the secondary center of ossification. The signal of epiphyseal cartilage on T1w imaging is homogenous and intermediate and is relatively low on water sensitive sequences (Fig. 2) and this is likely to be related to tightly bound water molecules (32). As the epiphyseal cartilage transforms into bone, chondrocytes hypertrophy and this process is accompanied by breakdown of the macromolecules, which in turn release bound water. The result is a heterogeneous increase in the signal on water-sensitive sequences throughout the skeleton but which is most accentuated in the posterior aspect of the distal femoral epiphysis and in the trochlea of the distal humerus (Fig. 3) (33, 34). Another important change in epiphyseal cartilage signal occurs when a child begins to weight-bear. This is thought to be related to displacement of water occurring as a result of pressure releasing water from glycosaminoglycans which are a constituent of hyaline cartilage (33). This is evident in cartilage subjected to loading, particularly in the femoral epiphyses and results in a reduction in signal on water sensitive sequences (33). Epiphyseal cartilage is markedly vascular in early

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childhood and this is observed after the administration of intravenous contrast where contrast can be seen within vascular channels for several minutes (35, 36). Other important features to recognize relate to the morphology and signal of the secondary ossification center. Initially this is spherical and later becomes hemispheric with the orientation of the flat base abutting the physis (36). In some bones such as the distal femur the secondary ossification center is composed of a single focus whereas in other bones, such as the distal humerus, there are multiple foci that eventually coalesce (35). Initially the marrow within the secondary ossification center is hematopoietic in nature and transformation to fatty marrow occurs within months (see marrow section). Physis The cartilage of the physis has a greater cellularity and relatively higher free water content than the adjacent nonossified epiphysis and as a result has a uniform intermediate signal intensity of T1w sequences and a higher signal than the non-ossified epiphysis on heavily T2w watersensitive sequences. The zone of provisional calcification that is related to the metaphyseal aspect of the physis has a low cellularity and water content and should be evident as a continuous low signal intensity line on all sequences. The physes in infants and young children is a flat disc and it is normal for this to become undulating later in childhood (37). Nevertheless the physis should be of a uniform thickness and focal physeal thickening indicates disruption of enchondral ossification. Likewise discontinuity of the zone of provisional calcification is an indication that the physis is damaged. Bone cortex The bony cortex is of low signal on all sequences. The periosteum parallels the bony cortex and has a very loose attachment to the cortex along the diaphysis but is attached tightly to the physis. There are extensive vessels coursing through the cortex and subperiostal space and these are conspicuous on postcontrast sequences. This arrangement in childhood predisposes to the formation of subperiosteal collections that can readily form as a result of involvement by tumor, infection or hemorrhage. The physis is surrounded by perichondrium that is a fibrocartilaginous structure that plays a vital role in the circumferential growth of bone and is particularly prominent in the newborn and young infant. The perichondrium is continuous with the periosteum and is strongly attached to the physis, acting as a barrier to the longitudinal spread of subperiosteal disease (38). Bone marrow Bone marrow is the main site of hematopoiesis and as such is highly cellular. At birth, hematopoietic marrow, otherwise known as red marrow, is present throughout the entire skeleton. The cartilaginous epiphyses and apophyses lack marrow until they ossify and once ossified they contain red marrow.

Ossification of the phalanges and of the tarsus begins in fetal life whereas the carpus begins to ossify at approximately 3 months after birth (39). The transition from red to fatty marrow begins shortly after birth with progressive conversion of red to yellow marrow starting in the distal phalanges of the upper and lower limbs and extending proximally into the axial skeleton. The conversion of red to yellow marrow occurs in parallel in the long bones within the first decade and starts at the diaphysis and progresses toward the metaphysis. Epiphyseal marrow conversion occurs within 6 months of the radiological appearance of the ossification center (40). Red marrow is composed of approximately 40% adipocytes and 60% hematopoietic cells and on a molecular level this equates to 40– 60% lipid, 30– 40% water, and 10 –20% protein. Ninety-five percent of yellow marrow consists of adipocytes and the chemical composition is 80% lipid, 15% water, and 5% protein. The fatty component in red marrow accounts for the fact that its signal is higher on T1w sequences than that returned of muscle and intervertebral discs. Conversely the signal is lower than muscle on fat-suppressed T2w imaging. An exception is in very young children where the fat content can be lower. Yellow marrow is almost entirely composed of fat with an almost 95% adipocyte content and therefore has a similar signal to subcutaneous fat. The composition and anatomic location of bone marrow change significantly with age. At birth red marrow is present throughout the skeleton. The transition from red to fatty marrow begins shortly after birth with progressive conversion of red to yellow marrow starting in the distal phalanges of the upper and lower limbs and extending proximally into the axial skeleton. The conversion of red to yellow marrow occurs in parallel in the long bones within the first decade and starts at the diaphyses and progresses toward the diaphysis. Marrow reconversion occurs at times of physiological stress and involves fatty marrow transforming into red marrow. This process can be patchy and asymmetrical (41, 42) but generally begins in the axial skeleton and later involves the axial skeleton in an opposite fashion to marrow conversion.

Common pitfalls Marrow lesions Several studies have highlighted the presence of focal altered marrow signal at different sites in healthy children that can be misinterpreted as contusions or tumor. The best documented results from residual red marrow in the proximal metaphysis of the femora and humeri and is characterized by low T1w signal which should not be lower in signal than adjacent muscle (Fig. 4). These pseudo-lesions typically have a flame shape with a base adjacent to the physis and have straight vertical margins with no mass effect on the adjacent yellow marrow (41, 43). The background trabeculation is not distorted. This contrasts with contusions and tumor in which well-defined lesions and distortion of the trabecular pattern are typical.

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Fig. 4 The asterisks indicates residual red marrow in the metaphysis of the tibia and femur in a healthy 12-year-old boy. (a) STIR coronal and (b) STIR sagittal sequences. These figures have been reproduced with permission from University Hospital of North Norway (UNN), Tromso

Studies in asymptomatic and healthy children have demonstrated the presence of foci which are hypointense on T1w sequences and hyperintense on fluid sensitive sequences in the ankle and foot as well as in the carpus (44, 45). In one study 50% of children aged 5 –15 years (mean, 9.7 years) exhibited these marrow signal changes in at least one of the carpal bones (Fig. 5) (45). The significance of this is uncertain but one theory is that the high signal represents bone marrow edema from “microtrauma” occurring after normal activity, due to the relative plasticity of the growing knuckles. Similarly, another study has documented focal bone marrow edema related to the central portion of the closing physis of the femur, tibia, and fibula in adolescent knees and the authors concluded that this is a normal physiological finding and should not be mistaken for disease (46). It has also been postulated that small patchy areas of high signal on water sensitive sequences could represent “islands” of residual red marrow. Bone marrow edema (BME) is a non-specific expression on MRI and only refers to a finding with specific signal characteristics (47) regardless of the histological characteristics of the tissue. It is not unlikely that the “BME” seen in healthy children represents a different entity to the ‘BME’ caused by inflammation. The problem is that the BME signal caused by physiological processes is indistinguishable from BME signal caused by inflammation on standard fat-suppressed T2w sequences making it difficult to differentiate normal findings from pathology based on the MRI alone. Marrow can appear diffusely hyperintense on STIR sequences and this can simulate tumor infiltration particularly in children aged ,5 years. This occurs as fat and fluid can contribute to increased signal and correlation with T1w imaging is essential. Restricted diffusion is also shown to be a normal finding in healthy children, even in an asymmetrical pattern (48). It is likely that cellular red marrow within the axial skeleton and proximal femur accounts for some of the high signal seen on the DWI but also growth zones with high cellularity showed restricted diffusion in the cohort of healthy children. To date methods for distinguishing physiological causes from pathological causes of restricted diffusion in

Fig. 5 The arrows below indicate “bone marrow edema” in the base of the fifth metacarpal in a healthy 11-year-old boy. (a) T1w coronal and (b) STIR coronal sequences. This was considered to be non-pathological in nature and may represent a normal variant. These figures have been reproduced with permission from University Hospital of North Norway (UNN), Tromso

Fig. 6 T1w coronal sequences demonstrating carpal bony depressions in healthy children. The arrows indicate carpal depressions in the (a) hamate and lunate of a 13-year-old boy and (b) scaphoid of an 11-year-old girl. These are normal variants. These figures have been reproduced with permission from University Hospital of North Norway (UNN), Tromso

children are lacking hence using DWI as a screening tool for marrow involvement may lead to over-diagnosing of disease. Further research is needed to find MR techniques that increase the specificity of alterations in bone marrow on MRI in children. Cortical irregularities Bony cortical depressions are frequently identified in the hands of healthy children and the number increases with age (Fig. 6) (45). Similar appearances have been noted in the tarsus (44). These cortical irregularities are therefore normal but can be misinterpreted as erosive disease in inflammatory diseases such as juvenile idiopathic arthritis and distinguishing the two entities can be difficult. Features including loss of joint space on a plain radiograph, adjacent BME, and pathological synovial enhancement are useful in ascribing these depressions to erosions (49). Epiphyseal ossification The secondary epiphyseal ossification center can be composed of several small foci that then merge with adjacent bone. This is the normal appearance in the distal humerus

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but can occur elsewhere and can be misinterpreted as osteochondral defects particularly in the femoral condyles. The posterior location and absence of BME in the adjacent bone are useful features distinguishing normal growth from trauma-related changes.

Conclusion MRI is an extremely valuable tool in the diagnosis of pediatric musculoskeletal disorders and understanding its role alongside other more conventional imaging modalities is vital if we are to realize its full potential. The accurate interpretation of MR relies heavily on a thorough understanding of normal physiological change in the growing skeleton and the wide spectrum of normal MR variants. Conflict of interest: None.

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Magnetic resonance imaging of the immature skeleton.

Magnetic resonance (MR) is unique in its ability to allow assessment of bone marrow, epiphyseal, physeal, and articular cartilage as well as tendons a...
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