Variants of Exostosis of the Bone in Children Randy Ray Richardson, MD

Home , Exostosis, Osteomyelitis, Periosteal reaction

xostosis of the bone is a common finding in children in the metaphysis or metadiaphysis and tend to grow away Epresenting with a mass in the extremity. The appearance from the physis. The most common location for these of a solitary exostosis of the bone can be characteristic and the lesions is in the lower extremity. The femur is the most diagnosis of an osteochondroma is often made without fur- common location followed by tibia and then humerus1,2 ther imaging. Multiple osteochondromas are seen in multiple (Figs. 2 and 3). hereditary exostoses. Osteochondromas can be in specific Radiographically these lesions appear either pedunculated locations such as the epiphysis in Trevor’s disease. There are with a stalk or sessile with broad cortical attachment. There is also several “osteochondroma-like” lesions that can occur as characteristic medullary and cortical continuity seen in both normal variants or as the result of trauma, congenital anom- types of lesions. The appearance of the cartilaginous cap is alies, systemic disorders, or various causes of periosteal reac- variable but can have rings of calcifications seen with other tion. In this article, we will review the imaging of the com- chondroid lesions. Radiographically, mineralization or ossi- mon osteochondroma and its associated diseases and then fication of the cap can be seen with skeletal maturation (Fig. focus on a variety of causes of bony exostosis that can have a 4). The thickness of the cap is typically measured by MRI and similar appearance. can vary widely in thickness based on skeletal maturation.1,11-12 Excision of the osteochondroma is typically definitive, al- Osteochondromas though recurrence has been reported in 2% of excised le- Solitary osteochondromas are common lesions and may ac- sions.13 count for up to half of benign bone tumors.1,2 An osteochondroma is an outgrowth of benign cartilage from the growth plate that undergoes endochondral bone formation. The eti- Hereditary Multiple ology of osteochondroma is not clear. Many believe an osteo- Exostoses (HME) chondroma to be a true bone neoplasm. This may be sup- ported by the increased incidence of osteochondromas in HME is one of the most common skeletal dysplasias in chil- patients who have undergone radiation.3,4 Others have sug- dren and, as the name implies, is an inherited disorder trans- gested that the outgrowth is a result of injury to the periph- mitted as an autosomal dominant trait. Males are affected eral growth plate as suggested in animal models where the more frequently than females due to incomplete penetrance growth plate has been traumatized and a typical solitary os- in females.14-15 The overall incidence is approximately nine teochondroma is produced.5-7 per million. Whatever the etiology (neoplastic or traumatic), patients Patients with HME are typically identified during the with solitary osteochondromas typically present with a non- first decade of life.16 Patients most commonly present with tender slow-growing mass. Occasionally, fractures of the pe- a palpable mass or deformity from angulation of an ex- dunculated osteochondroma can occur. Mass effect on adja- tremity. Short stature is seen in 40% of patients, although cent structures such as bone (especially when they occur in most patients still fall within two standard deviations of the forearm and leg), nerves, vessels, muscles, or even the the mean.17 The short stature is thought to result from spinal cord can also be symptomatic1,8-10 (Fig. 1). bowing and angulation deformity as well as the develop- Osteochondromas occur in any long bones that undergo ment of exostoses during peak growth periods of child- endochondral ossification. The lesions usually begin hood and puberty.18 growing at the growth plate and are most frequently found The osteochondromas of HME differ from the patients with solitary osteochondromas in that 90% of the lesions are of the sessile type19 (Fig. 5). Lesions in patients with HME Pediatric Radiologist, Phoenix Children’s Hospital, Mesa, AZ. Address reprint requests to: Randy Ray Richardson, MD, Pediatric Radiolo- have been described in almost every bone in the body exclud- gist, Phoenix Children’s Hospital, 553 N. Orange Street, Mesa, Arizona ing the calvarium. The most common location is about the 85201. E-mail: [email protected] knee (distal femur and proximal tibia). In fact, it is so com-

Figure 3 MR imaging of osteochondroma of the distal femur with mass affect on muscle. Figure 1 Osteochondroma of proximal tibia with mass affect on the ﬁbula.

Figure 4 Ossiﬁcation of cartilaginous cap of a pedunculated osteo- Figure 2 Sessile osteochondroma of the distal femur. chondroma of the proximal tibia. 382 R.R. Richardson

mon around the knee that another diagnosis should be considered if the bones about the knee are completely normal.1 Other common locations include humerus, elbow, wrist, hip, ankle, ribs, hands, feet, and scapula. Vertebral involvement is rare but can occur and has been described arising from the posterior elements and from the vertebral body itself. The distribution of lesions can be bilateral and almost perfectly symmetric or unilateral and very asymmetric (Fig. 6). The difference in distribution patterns may be attributed to dif- ferent genetic types of HME.1,19 Radiographically the evaluation of the patient with HME cen- ters on deformity and possible complications. Deformation is most commonly manifested as bowing of the bones. Coxa valga is seen in the proximal femurs, which can lead to uncovering of the femoral heads.20 The forearm is frequently bowed with ulnar deviation and shortening of the ulna (Fig. 7). Growth distur- bance of the distal radius and ulna can also result in a Made- lung deformity of the wrist (Fig. 8). In addition to bowing of the leg, synostosis of the bones may occur when large osteochondromas grow together. This is typically seen in the distal tibia and ﬁbula but can occur in other parts of the body20 (Fig. 9). Progressive erosion of an adjacent bone can be seen especially in the forearm and leg where long bones are juxta- posed11 (Fig. 10). Figure 5 Sessile osteochondroma of the proximal humerus.

Figure 6 Symmetric bilateral exostoses in a patient with HME. Variants of exostosis of the bone in children 383

logically, the exostoses are identical to osteochondromas with a cap of hyaline cartilage and endochondral ossification. The distal femur, distal tibia, and talus are most frequently involved. The process is typically unilateral; however, there are several case reports of bilateral disease. Multiple bones of the same extremity are commonly involved and the lesions occur along the medial epiphysis more often than the lateral.25-27 Radiographically, small ossifications are seen along the medial or lateral aspect of a developing epiphysis or tarsal bone. The small ossifications eventually become confluent with the epiphysis, forming an asymmetric mass. Deforma- tion and angulation do not commonly occur; however, when present, they can be severe and debilitating (Figs. 12 and 13). Because the lesions occur in the epiphysis, arthrography can be used to define the extent of the lesion. Arthrography is also useful to distinguish exostosis from loose bodies seen in sy- novial osteochondromatosis.28

Posttraumatic Exostosis In children and adolescents partial or complete avulsion fractures commonly occur due to the inherent weakness of the apophyses compared with the tendons. Avulsion injuries at the musculotendinous junction continue to occur until patients reach their mid-twenties (Fig. 14). The heal- Figure 7 Shortening of the ulna with bowing of the forearm in a ing process of such injuries may leave a prominent exos- patient with HME. tosis of the bone, which should not be mistaken for an osteochondroma or any other neoplastic or infectious process.28,29 Entities such as Osgood–Schlatter and Sinding Complications seen with both solitary osteochondro- Larsen Johanssen, which have been mistakenly attributed mas and HME include fracture, vascular injury, bursa formation, neurologic compromise, and malignant transformation. The most worrisome of these complications is malignant transformation. For solitary osteochondromas, malignant transformation occurs in less than 1% of cases.1,8 In HME, the frequency is higher. Studies have shown a prevalence of malignancy ranging from 2 to 25%.1,8 The most recent studies seem to favor a prevalence of around 3 to 5%.21-24 Radiographic manifestations include increasing size of an exostosis after puberty, lucencies or indistinct- ness developing within the exostosis, destruction of cortical bone, and soft-tissue mass. Cross-sectional imaging is useful in the evaluation of the cartilaginous cap. Generally, a cartilaginous cap thicker than 1.5 to 2 cm in a skeletally mature patient should be considered worrisome for possible malignant degeneration. In children, the cartilaginous cap can be thicker, sometimes normally reaching a thickness of up to 3 to 5 cm21-24 (Fig. 11).

Trevor’s Disease Trevor’s disease or dysplasia epiphysealis hemimelica is another process where exostosis of the bone is seen in children. No inheritance pattern has been established. In Trevor’s disease, there is cartilaginous outgrowth typically involving tarsal bones or epiphyses of long bones. Histo- Figure 8 Madelung deformity in a patient with HME. 384 R.R. Richardson

Figure 9 Synostosis of exostoses of the distal fibula and tibia. to osteonecrosis, now are considered to be part of this Myositis ossificans from trauma is a well-established spectrum of partial avulsive injury to the apophysis.30 The cause of soft-tissue calcifications. When the injury is deep, resulting exostosis from a patient with chronic Osgood– the periosteum of the bone can be involved and ossifica- Schlatter disease can be dramatic (Fig. 15). tion can attach to the bone. The result of this process can be mistaken for an osteochondroma (Fig. 16). Synostosis can even be seen when myositis ossificans occurs between bones that are closely apposed. This can look similar to

Figure 10 A large osteochondroma of the proximal ﬁbula causing erosion of the lateral tibial metaphysis. Figure 11 MR imaging of a thick cartilaginous cap in an adolescent. Variants of exostosis of the bone in children 385

Figure 13 Postsurgical appearance of the same patient after resection of the osteochondroma.

sis, which may often be separated from the rest of the phalanx by a lucent line32,33 (Fig. 17). Bizarre parosteal osteochondromatous proliferation (BPOP) is a rare, benign lesion that was ﬁrst described by Nora and coworkers in 1983 in the hands and feet of young

Figure 12 Exostosis of the lateral epiphysis of the proximal tibia with associated valgus deformity in a patient with Trevor’s disease.

patients with HME where two large osteochondromas fuse together.31 Subungual exostosis is an uncommon lesion that can appear very similar to an osteochondroma. The exostosis occurs at a nail bed of a digit of the hand or foot. The great toe is most commonly affected. The lesion is thought to be due to trauma with a reaction similar to myositis ossificans. Histologically they consist of trabecular bone with a cap of fibrocartilage. Radiographically they appear as a lobulated bony protuber- ance emanating from the nail bed.1 Turret exostosis is another type of posttraumatic exostosis specific to the proximal or middle phalanx of the hand. Ra- diographically the lesion appears to develop from disruption of the periosteum with formation of a subperiosteal hema- Figure 14 MR imaging of the avulsive injury in a patient with toma. Radiographs demonstrate a broad-based bony exosto- Osgood–Schlatter disease. 386 R.R. Richardson

Figure 17 Turret’s exostosis of the 1st proximal phalanx.

Figure 15 Chronic Osgood–Schlatter disease. Normal Variants and Congenital Anomalies adults. The lesion is characterized by heterotopic bone rising Mistaken for Osteochondromas from otherwise normal cortex, typically without evidence of The supracondylar process of the humerus may be easily periosteal change or medullary contiguity (Fig. 18). BPOP is mistaken for an osteochondroma. It is simply an outgrowth believed to be the result of minor blunt trauma to the affected of bone that occurs along the anteromedial surface of the area.34 distal humerus and is typically oriented toward the joint, whereas pedunculated osteochondromas are oriented away from the joint (Fig. 19). A persistent portion of the coraco- brachialis muscle may insert on the process. It can also serve as an anomalous origin of the pronator teres muscle. Patients with this anomaly may develop symptoms from compression of the median nerve by the ligament of Struthers, which originates from the supracondylar process and inserts to the medial epicondyle.35 Other similar bony processes occur throughout the body such as the os intermetatarsale, which occurs between the first and second metatarsals, and the trochlear process of the calcaneus, which can be very prominent. Congenital anomalies can produce osteochondroma- like lesions. In patients with diastematomyelia a bone spur can form within the central canal (Figs. 20 to 22). This can be differentiated from an osteochondroma by the presence of a tethered cord with the cord split into two halves at the level of the bony spur. This is best depicted on MR imaging. Innumerable normal variations and normal appearances of bone exist in children that can have an appearance similar to osteochondromas. The oblique view of the first metatarsal in young children has a prominent exostosis- like process distally, which is normal (Fig. 23). Another Figure 16 Myositis ossificans attached to the periosteum of the distal common finding in children is spurring around the growth ulna in a patient with healing fractures of the distal radius and ulna. plate that occurs with partial or incomplete closure along Variants of exostosis of the bone in children 387

Figure 18 Bizarre parosteal osteochondromatous proliferation (BPOP). (Reprinted with permission34). (A) Radio- graph of humerus after shows no fracture. Soft-tissue swelling is seen in lateral aspect of upper arm. (B) Six months later, radiograph of humerus shows development of myositis ossificans. (C) Twelve months after injury, axial CT shows peripherally calcified soft-tissue mass (not shown) consistent with myositis ossificans. Cortically based lesion is seen without medullary contiguity, consistent with BPOP.

the periphery of the physis. These epiphyseal and metaph- of the diffuse ossification of ligamentous insertions result- yseal spurs should not be mistaken for exostosis of the ing in metaphyseal exostoses. Fortunately, these systemic bone or fractures36 (Fig. 24). Anomalies of the digits have disorders with soft-tissue ossification and osteochondro- a wide variety of appearances with duplications, supernu- ma-like lesions often have characteristic findings of the merary, and bifid digits as well as other various types of hands and other laboratory data to differentiate them from polydactyly36 (Fig. 25). HME.37

Systemic Disorders Periosteal Reaction Systemic disorders such as pseudohypoparathyroidism, There are many causes of periosteal reaction that can cause pseudopseudohypoparathyroidsim, tumoral calcinosis, bone formation and exostosis that can appear similar to os- and myositis ossificans progressiva can have osteochon- teochondromas. Potential etiologies include a parosteal os- droma-like lesions and can be difficult to differentiate teosarcoma, osteoid osteoma, and osteomyelitis. Parosteal from hereditary multiple exostoses. In particular, myositis osteosarcoma with its typical sessile attachment to the exter- ossificans progressiva, a rare progressive familial disease, nal cortex can radiographically mimic an osteochondroma. can have an appearance strikingly similar to HME because Patients with a parosteal osteosarcoma (Fig. 26) are usually 388 R.R. Richardson

Figure 21 Axial CT of a central bony spur in a patient with diastematomyelia.

combination of imaging and clinical and histological evaluation.39 Figure 19 Supracondylar process of the humerus. In summary, exostosis of the bone is a common ﬁnding in children. Despite the many normal variants, posttraumatic lesions, systemic disorders, and various causes of periosteal older and present with a painful mass. Also, in contrast to reaction that can mimic osteochondromas, the diagnosis of a osteochondromas, parosteal osteosarcomas arise from the solitary osteochondroma and HME is often established with- cortex of the bone and do not commonly involve the medul- out advanced imaging because of their characteristic conven- lary cavity.38 Even so, deﬁnitive differentiation is usually a tional radiographic appearance.

Figure 20 Saggital CT of a central bony spur in a patient with diastematomyelia. Figure 22 MR imaging of a diastematomyelia. Variants of exostosis of the bone in children 389

Figure 25 Biﬁd distal phalanx.

Figure 23 Oblique view of the foot shows a prominent exostosis-like process distally in the ﬁrst metatarsal.

Figure 24 Normal variant epiphyseal spurs of the distal radius in an adolescent. Figure 26 Parosteal osteosarcoma of the distal femur. 390 R.R. Richardson

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