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one lesions in children are very common and include true bone tumors and tumor-like lesions. More than onehalf of all childhood bone neoplasms are benign.1 The most common benign bone lesions in children are nonossifying broma, osteochondroma, cortical desmoid, Langerhans cell histiocytosis, unicameral bone cyst, and aneurysmal bone cyst. The most common malignant bone lesions are osteosarcoma, Ewing sarcoma, and metastatic disease, such as from neuroblastoma. The radiograph remains the cornerstone for evaluation of the pediatric bone lesion. Radiographs provide information on the location of the lesion within the bone, the presence and type of mineralized matrix, the nature of the interface between the tumor and the surrounding host bone, and the reaction of the host bone to the presence of the tumor.2 In conjunction with the age of the patient, the radiograph is key to the differential diagnosis of a bone lesion. However, cross-sectional imaging with computed tomography (CT) and magnetic resonance imaging (MRI) can provide useful additional information when the radiographic ndings are not diagnostic. The goal of this article is to review the role of cross-sectional imaging modalities and imaging characteristics of common benign and malignant bone lesions in pediatric patients.
greater contrast and spatial resolution of CT makes it more sensitive in detection of bone lesions. CT can also be used to supplement the information obtained from radiographs where radiographic evaluation is limited because of superimposing structures or complex anatomy (eg, axial skeleton). CT can provide exquisite detail regarding cortical destruction, nondisplaced pathologic fractures, subtle osteoid/chondroid matrix, and early periosteal reaction. CT has also been shown to be better than MRI in detecting the nidus of an osteoid osteoma.5 Another major advantage of CT is the ability to perform CT-guided biopsies and interventions, such as ablation of osteoid osteoma. Rapid advancements in multidetector CT technology allow for the acquisition of isotropic datasets while virtually elimi-
Imaging Modalities
Computed Tomography
Although radiographs are the mainstay for radiologic evaluation of bone tumors, one drawback of conventional radiography is its inability to detect early changes in bones with complex osseous anatomy. For example, 30%-50% bone destruction of a vertebra has to be present to detect alterations in bone architecture on plain radiographs of the spine.3,4 The
*Mallinckrodt Institute of Radiology, Washington University School of Medicine, St Louis, MO. University of Iowa Roy J. and Lucille A. Carver College of Medicine, UIHC, Department of Radiology, Iowa City, IA. Address reprint requests to Geetika Khanna, MD, MS, Mallinckrodt Institute of Radiology, Washington University School of Medicine, 510 S. Kings Highway,CampusBox8131-MIR,St.Louis,MO63110.E-mail:khannag@ mir.wustl.edu
Figure 1 Multidetector CT used for evaluation of vessels in a child with hereditary multiple exostosis. Three-dimensional shaded surface display from CT angiography shows the relationship of the lower extremity arteries with respect to the innumerable osteochondromas. (Color version of gure is available online.)
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0037-198X/12/$-see front matter 2012 Elsevier Inc. All rights reserved. doi:10.1053/j.ro.2011.07.008
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Figure 2 Hypermetabolism in a nonossifying broma on PET. Fluorine-18 PET-CT performed for staging in a 15-yearold boy with Hodgkins disease shows a hypermetabolic focus (arrow) in the distal right femur (A), which can simulate metastatic disease; (B) correlation with the low-dose CT reveals the lesion to be a well-dened, intracortical lytic lesion with sclerotic margins (arrow) consistent with a nonossifying broma.
nating the need for sedation even in young children. The isotropic datasets can be used to obtain multiplanar reconstructions in any plane. In addition, they can be used to generate 3-dimensional (3D) reconstructions that can aid in diagnosis and treatment planning (Fig. 1).6 This allows the patient to be imaged in any position, as dictated by the patients comfort level, and also eliminates the need for rescanning in orthogonal projections. However, before performing CT on a child, the benet of any anticipated additional information from CT should be weighed against the risk of radiation exposure to the child.
the location of the lesion, its extent, involvement of bone marrow, and the presence of an associated soft tissue mass. However, MRI is not specic because most bone lesions show low T1 and high T2 signal. To improve diagnostic accuracy, MR images need to be interpreted in conjunction with radiographs. In a prospective analysis of 87 consecutive musculoskeletal tumors, the tumors were correctly assessed only 55% of the time by MR alone, with malignancy overestimated in 39% of the cases when MR images were interpreted without radiographic correlation.8 MR is the imaging modality of choice for local staging of a suspected malignant bone tumor. The initial MRI should be performed before biopsy to prevent distortion by postbiopsy changes. In addition, MRI can help determine the optimal site and track for biopsy. The radiologist perform-
Figure 3 Peritumoral edema associated with a chondroblastoma. (A) Plain radiograph in a 17-year-old boy with knee pain shows an epiphyseal lytic lesion (arrow). The lesion is geographic with a sclerotic margin. A benign-appearing smooth periosteal reaction is present on the lateral aspect of the proximal tibia (arrowhead). (B) Sagittal T2-weighted image again shows the epiphyseal lesion with a hypointense rim corresponding to the sclerosis seen on the radiograph. Marked edema is present in the entire visualized tibia and surrounding soft tissues. Surgical pathology was consistent with chondroblastoma.
92 ing the biopsy should plan the biopsy track in conjunction with the orthopedic surgeon. At diagnosis of a malignant bone lesion, longitudinal MRI of the entire bone is recommended with T1 and fat-saturated T2-weighted images to evaluate for the extent of the lesion and detect any skip metastasis. For treatment purposes and pretreatment evaluation, the intraosseous extent of a bone lesion (in particular osteosarcoma) is most accurately measured and depicted on the T1-weighted images.9 Axial pre- and postcontrast images aid in delineating the extent of the soft-tissue mass, the compartments involved, and the status of the neurovascular bundle. The lack of radiation exposure makes MR particularly suitable for evaluation of the pediatric skeleton. Considerations when performing MRI in children include the need for sedation in younger children and the increased difculty in obtaining quality images on smaller body parts.
Tumor Matrix
The internal appearance of a tumor depends on its cellular composition and its presence or absence of tumor matrix. Tumors can produce osteoid, chondroid, or brous matrix. On radiographs and CT images, osteoid matrix has a homogeneously increased density with a cloud-like appearance, whereas chondroid matrix is characterized by the presence of stippled rings and arcs. Although the presence and type of matrix usually can be evaluated with radiographs, CT (with its high spatial resolution) can also aid in improved matrix detection and characterization. CT can also be used to determine the location of the tumor matrix, central versus peripheral, and to aid in differentiation of myositis ossicans from parosteal osteosarcoma. Mature osteoid matrix is located peripherally in myositis ossicans; however, the mature osteoid tumor matrix of parosteal osteosarcoma is seen centrally.18
Nuclear Medicine
Although bone scintigraphy and positron emission tomography (PET) are excellent for evaluation of metastatic disease or a multifocal process, their lack of specicity limits their use in the initial workup of a single bone lesion.10 Several benign bone lesions, such as brous dysplasia, nonossifying broma, and giant cell tumors have been shown to be hypermetabolic on PET (Fig. 2).11 Although bone scintigraphy remains an essential part of osteosarcoma staging, recent studies have shown PET to have higher diagnostic accuracy for staging of Ewing sarcoma.12
Soft-Tissue Mass
Cross-sectional imaging modalities are essential in detecting the presence of and the extent of a soft tissue mass. Although peritumoral inammatory changes can result in surrounding periosteal reaction and inammation in adjacent soft tissues, the presence of a large soft tissue mass in conjunction with a lytic bone lesion is characteristic of Ewing sarcoma in the pediatric population (Fig. 4).
Peritumoral Edema
Peritumoral edema can be present in both benign and malignant bone tumors. Peritumoral edema does not help in determining the aggressiveness of a lesion.14 In fact, some benign bone lesions in children can have extensive peritumoral edema in the bone marrow and surrounding soft tissues mimicking an aggressive process.13 These lesions include osteoid osteoma, stress fracture, chondroblastoma, and Langerhans cell histiocytosis (Fig. 3). Inammatory changes tend to be marked in the pediatric bone because of the presence of a loose periosteum which can be easily elevated. Tumor related edema may be the only or most prominent feature of osteoid osteoma, and in some cases can obscure the nidus on MRI.15 Peritumoral edema is most conspicuous on fat saturated T2-weighted or short tau inversion recovery (STIR) images.
Fluid-Fluid Levels
T2-weighted MRI has been shown to be most sensitive in detection of uid-uid levels (FFLs).19 Although FFLs have been classically described with aneurysmal bone cysts (ABCs), they can be seen with other bone lesions as well.20 Both benign and malignant bone lesions can have FFLs. Some examples include aneurysmal bone cyst, unicameral bone cyst, giant cell tumor, and telangiectatic osteosarcoma. The percentage of a bone lesion occupied by FFL has been shown to inversely correlate with the likelihood of malignancy (Figs 5 and 6).21 In a study of 83 cases with FFLs, ODonnell and Saifuddin21 showed that if at least two-thirds of the lesion contained FFLs 89% of the lesions were benign, whereas if FFLs were present in less than a third of the lesion, 67% of the lesions were malignant.
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Figure 4 Soft-tissue mass associated with an Ewing sarcoma. (A) Frog-leg radiograph of the pelvis in a 3-year-old patient with a limp shows a poorly marginated lytic lesion (arrow) in the left side of the sacrum with a compression fracture of the superior endplate of S1. The primary differential diagnosis includes Ewing sarcoma versus Langerhans cell histiocytosis. (B) Sagittal postcontrast T1-weighted image shows a marrow replacing process in the S1 vertebral body with a large soft-tissue mass extending into the spinal canal (*). The large soft-tissue mass is characteristic of Ewing sarcoma.
these lesions are usually central, elongated radiolucent lesions with well-dened margins. A pathologic fracture through a UBC can result in a fallen fragment, a pathognomonic sign of a UBC. Cross-sectional imaging is helpful if the radiographic ndings are atypical, such as a multilocular appearance, or when a UBC occurs in an atypical site. CT may be helpful in identication of a pathologic fracture or a fallen fragment. CT can also be used to evaluate the extent of the lesion in anatomically complex areas, such as the pelvis.22 On MR, the classical UBC appears as well-dened meta- or di-
Figure 5 Fluid-uid levels in telangiectatic osteosarcoma. (A) Anteroposterior radiograph of the knee in a 15-year-old patient with knee pain shows an aggressive appearing lytic lesion at the medial aspect of the metaphysis with sun-burst periosteal reaction. The lesion is poorly marginated and some osteoid matrix. (B) Axial T2-weighted MRI shows a marrow replacing process with cortical destruction and large soft-tissue mass. Scattered uid-uid levels (arrows) are present in the mass. Surgical pathology was consistent with telangiectatic osteosarcoma.
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Figure 6 Fluid-uid levels in an aneurysmal bone cyst. A 14-year-old girl presented with scoliosis and back pain. (A) Anteroposterior view of lumbar spine shows an expansile lytic lesion in the right transverse process of L4 (arrow). No internal matrix was identied. (B) Axial T2-weighted MRI shows multiple FFLs throughout the lesion, which involves the right transverse process, pedicle, and right side of the vertebral body. Surgical pathology was consistent with aneurysmal bone cyst.
aphyseal cystic lesion containing uid signal intensity with a thin rim of peripheral enhancement at the cyst wall on postcontrast images.23 However, UBCs can be multiloculated with heterogeneous intensity, uid-uid levels, and nodular or thick peripheral areas of enhancement especially in the setting of a healed or acute pathologic fracture.24 Aneurysmal Bone Cyst. Most ABCs seen in children are primary lesions with a peak occurrence around 16 years of age. Secondary ABCs can also be seen in children, after trauma, or with an underlying lesion, such as osteoblastoma, chondroblastoma, or simple bone cyst.25 ABCs typically arise in an eccentric metaphyseal location in long bones or the posterior elements of the spine. As indicated by the name, an ABC is an expansile, lytic lesion. ABCs usually have well-dened margins; however, approximately 15% will have poorly dened margins. ABCs have no internal matrix and consist of blood lled cavernous spaces. The expansile nature of the lesion may result in marked cortical thinning, so the cortex may become imperceptible on plain radiographs or MRI. If the ABC is rapidly expanding, it can have an aggressive appearing periosteal reaction mimicking a malignancy. On MRI, ABCs are low in signal intensity on T1-weighted images and high in signal intensity on T2-weighted images with low signal brous tissue lining the spaces. ABCs are characterized by the presence of FFLs, which are most prominent on T2-weighted images (Fig. 6). On postcontrast images, enhancement of the cyst wall and internal septations can be seen. Although solid components may be present within ABCs, the presence of solid tissue should alert the radiologist to consider a secondary ABC, or an alternative diagnosis, such as telangiectatic osteosarcoma.22
Cartilaginous Lesions Osteochondroma. This is a relatively common benign lesion that arises when growth plate cartilage becomes displaced to the metaphyseal region. Osteochondroma is an extension of the normal bone and shows continuity with the periosteum, cortex, and marrow of the underlying bone. The most common site is around the knee joint followed by the proximal humerus. Most osteochondromas can be diagnosed radiographically, by their characteristic cortical and medullary continuity with the native bone.26 Cross-sectional imaging is helpful when the radiographic appearance is not characteristic, when the anatomy needs to be better delineated, such as in the axial skeleton, when preoperative planning is required, or when one needs to evaluate for radiographically occult complications (Fig. 1). The 3D imaging ability of CT and MRI allows optimal depiction of the pathognomonic cortical and medullary continuity of the lesion with the parent bone. This is particularly true for lesions located in areas of complex anatomy, such as the axial skeleton, and for lesions with a broad stalk. Osteochondromas can cause local complications because of mass effect, such as bursitis, compression of the neurovascular bundle, and pseudoaneurysm formation. Sonography is a relatively inexpensive imaging modality to evaluate for complications, such as vascular compromise, pseudoaneurysm formation, or bursa formation. Cross-sectional imaging is helpful to evaluate for complications like fracture or malignant transformation. MRI is the best imaging modality to assess the thickness of the hyaline cartilage cap of an osteochondroma. Although a thickness of more than 1.5 cm has been suggested as an indicator of malignant transformation in the skeletally mature individual, increased thickness of the
95 cross the growth plate to involve the adjacent metaphysis.28 On radiography, the lesion appears as an eccentric, lytic lesion with a geographic border. Stippled calcications within the lesion may be visible, reecting chondroid matrix. On MRI, the lesion appears as a lobulated low T1 signal and heterogeneous T2 signal lesion. Calcications within the chondroid matrix will appear low signal on both T1 and T2 images, whereas the noncalcied cartilage appears T2 hyperintense (Fig. 3). Chondroblastomas can have a characteristic peripheral thin hypointense rim on MRI that corresponds to the radiographic marginal sclerosis around the lytic lesion.29 MRI will typically show extensive edema in the surrounding bone and soft tissues, and marked reactive synovitis can also be present. Osseous Lesions Osteoid Osteoma and Osteoblastoma. Osteoid osteoma (OO) is characterized by a radiographic appearance of an intracortical nidus with a variable amount of mineralization, by cortical thickening, and by reactive sclerosis. Cross-sectional imaging is useful if the radiographic ndings are atypical, the OO is located in a region of complex anatomy (eg, the posterior elements of the spine), and for image-guided intervention.30 The differential diagnosis of an osteoid osteoma includes other intracortical lesions, such as stress fracture and intracortical abscess. On the basis of cross-sectional imaging, OO can be classied as subperiosteal, intracortical, endosteal, and intramedullary. Thin-section CT images obtained with a bone algorithm and viewed in bone windows with multiplanar reconstructions are useful for identifying the nidus. The authors of some studies have shown that CT is superior to MRI in depicting the nidus of OO.5 On CT, OO is characterized by a well-dened round or oval radiolucent nidus. A variable amount of mineralization may be seen
Figure 7 Osteoid osteoma nidus detection on CT. A 13-year-old boy with right hip pain. (A) Axial T2-weighted MRI shows a large right hip joint effusion with femoral neck edema. There is suggestion of a T2 hyperintense lesion along the posterior cortex with a central hypointensity (arrow). (B) Axial CT image clearly shows the lytic nidus (arrow) with central mineralization at the posterior cortex of the right femoral neck.
cartilage cap is a recognized feature in the growing child and should not be viewed as a nding of malignant transformation in skeletally immature patients. Enchondroma. Enchondromas are a relatively common benign tumor of bone in children characterized by formation of hyaline cartilage.3 They are most commonly seen in the second decade of life, and are most commonly found in the small tubular bones of the hands and feet. These typically appear as central, well-dened, expansile masses that cause endosteal scalloping. The presence of chondroid matrix is a characteristic nding, although it is present in only approximately 50% of enchondromas. On MRI, enchondromas appear as T1-hypointense and T2-hyperintense lobulated lesions with small foci of low signal corresponding to the stippled calcications within the chondroid matrix. Enchondromas can occur in association with venous malformations (Maffucci syndrome). Although Maffucci syndrome carries a risk of malignant transformation of enchondroma into chondrosarcoma, this is unusual in the pediatric age range.27 Chondroblastoma. Chondroblastoma is a rare benign tumor of immature cartilage, with a peak incidence between 10 and 20 years of age. Nearly one-half of these tumors are diagnosed in skeletally immature patients. Chondroblastomas have a predilection for the epiphyses of long bones and epiphyseal-like regions, with the bones around the knee joint being most commonly affected. Chondroblastomas can often
Figure 8 Healing nonossifying broma on MRI. Sagittal T2-weighted MRI with fat saturation shows a cortically based well-dened lesion (arrow) that is hypointense to muscle. The surrounding marrow signal is normal. This nding is consistent with a healing nonossifying broma, which is a common incidental nding.
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Figure 9 Cortical desmoid on MRI. A 4-year-old boy was referred for MRI of femoral lesion seen at an outside institution. (A,B) Axial T1- and T2-weighted MR images of the knee show cortical irregularity (arrow) at the origin of the medial gastrocnemius. This is a characteristic location and appearance of a cortical desmoid. (C) Plain radiograph of knee in a different child shows a subtle lucency with a sclerotic margin (arrow) at the medial aspect of the distal femoral metaphysis cortical desmoid.
within the nidus. The nidus is surrounded by reactive sclerosis, periosteal reaction, and new bone formation. On MRI, the nidus has low to intermediate signal intensity on T1weighted images and variable signal intensity on T2weighted images depending on the amount of mineralization. Extensive surrounding edema in the adjacent bone marrow and soft tissues is often seen with OO, and the signicant surrounding reaction can make it difcult to identify the nidus on MRI. Intra-articular osteoid osteomas, most commonly seen in the hip joint, show minimal reactive cortical thickening but can cause synovitis that may be confused for an infectious or inammatory arthropathy (Fig. 7). Osteoblastoma differs from osteoid osteoma in having a nidus larger than 1.5 cm in diameter and usually showing more variable histologic ndings.3 The most common location of osteoblastoma is in the posterior elements of the spine; hence, cross-sectional imaging is invaluable in the evaluation of these lesions. CT demonstrates a lytic lesion with osteoid matrix and periosteal reaction. MR signal characteristics can be variable depending on the amount of mineralization, though surrounding marrow and soft tissue edema are typically present.
Fibro-Osseous Lesions Fibrous Cortical Defect and Nonossifying Fibroma. Fibrous cortical defect (also called benign cortical defect) and nonossifying bromas (NOFs) are the commonest benign lesions of the pediatric skeleton, often seen incidentally on radiographs. They have a characteristic radiographic appearance with an eccentric, cortically based, well-dened lytic lesion with marginal sclerosis. As the lesions heal, increasing sclerosis is seen. They are most commonly seen in the metaphysis or metadiaphysis of the long bones. Although the 2 lesions are identical histologically, the term brous cortical defect is preferred for lesions 2 cm in size. Given the common occurrence of NOFs in children, it is not unusual to encounter them as incidental ndings on MRI (Fig. 8). The MRI appearance of NOFs varies with the developmental stage of the lesion and correlates with the radiographic appearance. In the developmental stage, NOFs are bright on T2-weighted images. As the lesions mature, they become low in signal on T2 images because of hypercellular brous tissue and hemosiderin deposits.31 On MRI, the lesions are typically hypointense on T1-weighted images. T2 signal varies based on the degree of hypercellular brous tissue, with lesions being
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Figure 11 Neuroblastoma with metastatic disease to bone. A 2-year-old girl presented with limp. (A) Anteroposterior view of the left hip shows a moth-eaten appearance to the left femoral neck with interrupted periosteal reaction (arrow). A band of sclerosis (arrowhead) is present in the midfemoral neck. (B) Coronal T1-weighted MRI shows loss of normal marrow signal in the proximal epiphyseal ossication center (white arrow) and the proximal metadiaphysis. Metastatic deposits are present in the distal femur (black arrow) as well. A hypointense line in the femoral neck (arrowhead) represents a pathologic fracture. Patient was found to have a left adrenal neuroblastoma.
Others Langerhans Cell Histiocytosis. Langerhans cell histiocytosis (LCH) is a benign round cell tumor that may present as solitary or multiple bone lesions.34 The skull, femur, vertebrae, pelvis, and ribs are the most common sites of involvement. In the tubular bones, lesions are typically metaphyseal or diaphyseal in location. Radiographically, these lesions typically appear as lytic lesions without matrix. The zone of transition can be narrow or wide, and the lesions can have a more permeative appearance. MRI is helpful in determining the extent of marrow involvement and in assessing the surrounding soft tissues as the primary differential diagnosis is osteomyelitis or Ewing sarcoma. The absence of an associated soft-tissue mass favors LCH over Ewing sarcoma. Although skeletal surveys remain the most widely used imaging modality, whole-body MRI using STIR sequences has been shown to be useful for detection and follow up multifocal skeletal involvement with LCH.35
Malignant Tumors
Osteosarcoma Osteosarcoma (OS) is the most common primary malignant bone tumor in children.36 The tumor generally occurs in the second decade of life and typically presents as a painful mass. Pediatric OS is usually metaphyseal and medullary in origin. The most common site is in the long bones of the lower extremity (especially around the knee joint), followed by the humerus. Plain radiographic ndings include a lytic, blastic,
Figure 10 Fibrous dysplasia on CT. Coronal maxillofacial CT image shows characteristic ground glass expansile lesion of the left maxilla consistent with brous dysplasia.
98 or mixed aggressive bone lesion with indistinct margins, cortical destruction, aggressive periosteal reaction, and a soft tissue mass. The tumor is characterized by production of osteoid matrix. MRI is crucial for local staging of the malignancy to determine the extent of marrow involvement, transphyseal extension, intra-articular extension, and the extent of soft-tissue disease. Longitudinal imaging of the entire bone should be performed as skip metastasis can be present in approximately 15% of cases.37 Axial T2-weighted and postcontrast MRI help determine the soft-tissue compartments involved and the status of the neurovascular bundle. The presence of uid-uid levels suggests the telangiectatic variety of osteosarcoma. Ewings Sarcoma Ewings sarcoma, a primitive neuroectodermal tumor, is the second most common primary malignant bone tumor in children. It is more common in whites than blacks with a peak occurrence in the second decade of life. Ewings sarcoma occurs in the axial and appendicular skeleton with about equal frequency, whereas the vast majority of osteosarcomas occur in the appendicular skeleton.38 Within the long bones, Ewing sarcoma commonly occurs within the diaphysis or metadiaphysis.36 On radiographic evaluation, it has a variable but usually aggressive appearance. Imaging ndings include a permeative, mixed lytic/sclerotic appearance with cortical destruction and aggressive periosteal reaction (spiculated or onion peel). Ewings sarcoma does not usually produce a mineralized osteoid matrix as seen with osteosarcoma. As in osteosarcoma, MRI is crucial for local staging and evaluation of skip lesions. Ewing sarcoma is hypo or isointense to muscle on uid sensitive sequences because of dense cellularity. A lytic bone lesion in a child in association with a large soft-tissue mass should raise concern for Ewing sarcoma (Fig. 4). Metastatic Disease The 2 most common primary pediatric malignancies to present with metastatic bone lesions are neuroblastoma and leukemia. Neuroblastoma is the most common extracranial solid neoplasm of childhood. The most common site of metastasis in neuroblastoma is the bone marrow, occurring in 50%60% of cases at presentation.39 On plain radiographs, metastatic disease appears as a poorly marginated lytic lesion, which may have a moth-eaten appearance. In the axial skeleton, metastatic disease can result in a sunburst pattern of periosteal reaction. MRI helps to determine the true extent of marrow involvement. Neuroblastoma metastases are T1 hypointense, T2 hyperintense lesions that enhance on post contrast images (Fig. 11). They may be associated with cortical destruction, periosteal reaction, and extraosseous extension. Metastasis can occur in both the axial and appendicular skeleton, with the metaphysis being the most common site of disease in the appendicular skeleton.
References
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Conclusions
Plain radiography is the most important initial imaging modality in the evaluation of pediatric bone lesions. The plain
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