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Hong Kong J Radiol. 2017;20:64-75 | DOI: 10.12809/hkjr1716433

PICTORIAL ESSAY

Bone Surface Tumours and Tumour-like Conditions ACW Lee, KS Tse, KC Lai, MK Chan, WK Tsang, CK Shiu, SS Cheng, KW Tang Department of Radiology and Imaging, Queen Elizabeth Hospital, Jordan, Hong Kong

ABSTRACT lesions that arise from outside of the medullary canal can be referred to as bone surface lesions. The aetiology of these lesions may be divided into neoplastic and non-neoplastic. Distinguishing the exact origin of the bone surface lesion may be challenging. This article discusses the imaging features of various bone surface lesions, with emphasis on lesion characterisation and clinical features.

Key Words: ; ; ; Myositis ossificans; , ;

中文摘要

骨表面腫瘤和類腫瘤病症 李昭穎、謝健燊、黎國忠、陳文光、曾慧勤、蕭俊傑、鄭珊珊、鄧國穎

從骨髓管外起源的病變腫瘤可稱為骨表面病變。其病因可分為腫瘤性和非腫瘤性。要區分骨表面病 變的確切起源並不容易。本文討論了各種骨表面病變影像學特徵,特別是病變的特徵和臨床表現。

INTRODUCTION to the periosteum. Lesions that arise from within the Bone lesions can arise from within or outside of the cortex can be further subdivided into endosteal and medullary canal. The latter can be referred to as bone intracortical. An endosteal lesion arises from the inner surface lesions. The aetiology of these lesions may be part of cortex immediately adjacent to the medullary divided into neoplastic or non-neoplastic. Understanding cavity, whereas an intracortical lesion is centred within the clinical and radiological features of these tumours the cortex. A subperiosteal lesion lies between the and tumour-like conditions is helpful in establishing cortex and the periosteum. A lesion that arises from the the diagnosis and guiding further management. This periosteum is termed a periosteal lesion. Those that arise study was approved by the Kowloon Central Cluster / from the fibrous tissue superficial to the periosteum Kowloon East Cluster Research Ethics Committee. are referred as parosteal or juxtacortical lesions.1 Distinguishing the exact origin of the bone surface ANATOMY lesion on imaging may be difficult. Characterisation of The bone surface includes three main regions: the the lesion based on the composition and radiological cortex, the periosteum, and the fibrous tissues superficial features can help establish the diagnosis and guide

Correspondence: Dr Alexander CW Lee, Department of Radiology and Imaging, Queen Elizabeth Hospital, 30 Gascoigne Road, Kowloon, Jordan, Hong Kong. Email: [email protected]

Submitted: 21 Jun 2016; Accepted: 15 Nov 2016.

Disclosure of Conflicts of Interest: All authors have disclosed no conflicts of interest.

64 © 2017 Hong Kong College of Radiologists ACW Lee, KS Tse, KC Lai, et al further management. On plain radiograph, it is usually a lobulated, exophytic mass with central dense ossification adjacent to the COMPOSITIONS bone, and may encircle the bone when it is large. The most common neoplastic bone surface lesions are Cortical thickening with a relative lack of aggressive bone-forming and -forming tumours. Bone- periosteal reaction is a feature.8 A cleavage plane forming tumours include osteoma, , separating the tumour and underlying cortex, , paracortical , and corresponding to the interposed periosteum, may be surface . Cartilage-forming lesions observed on cross-sectional imaging. This feature may include periosteal chondroma, bizarre parosteal be useful in differentiating parosteal osteosarcoma osteochondromatous proliferation (Nora’s lesion), from periosteal or high-grade subtypes of surface and periosteal chondrosarcoma. Rarer bone surface osteosarcoma.8 neoplastic lesions composed of epithelial and osteofibrous components include adamantinoma. Periosteal Osteosarcoma Tumour-like lesions include myositis ossificans and Periosteal osteosarcoma (Figure 2) is the second cortical desmoid. commonest subtype of surface osteosarcomas, comprising 25% of all surface osteosarcomas.3,9 It BONE-FORMING TUMOURS commonly affects young patients in the second and Surface osteosarcomas can be divided into parosteal, third decades of life. Most frequent locations of periosteal and high-grade surface subtypes.2 Different involvement are the and , followed by the subtypes carry different radiological appearances, ulna and . The of the long is treatment options, and prognosis. the most common origin.9,10 The 5-year survival rate of 83% is better than that for conventional osteosarcoma, Parosteal Osteosarcoma but worse than that for parosteal osteosarcoma.11 Parosteal osteosarcoma (Figure 1) is the most common Histologically, it arises from the inner, germinative of the subtypes, accounting for 65% of surface layer of periosteum.8 osteosarcomas.3,4 95% of cases occur in the age-group of 15-40 years,5 with a female-to-male ratio of 3:2.6,7 On plain radiograph, it is typically a broad-based It is usually metaphyseal and frequently seen at the soft-tissue mass attaching to the cortex, without an posterior distal femoral shaft.1 abnormality in the adjacent medullary canal. Periosteal

(a) (b)

Figure 1. Parosteol osteosarcoma in a 37-year-old female who presented with an incidental finding of raised serum alkaline phosphatase level to 150 IU/l: (a) plain radiograph showing a large ossified mass centering in the left hemipelvis. (b) Computed tomography showing a lobulated lesion in the left ilium, (c) (d) with large ossified exophytic masses (arrows). A cleavage plane separating the tumour from the underlying cortex is seen. (c, d) T1- and T2-weighted with fat-saturation magnetic resonance images showing that the lesion contains multiple low-signal exophytic foci without intramedullary invasion (arrows). confirmed low- grade parosteal osteosarcoma.

Hong Kong J Radiol. 2017;20:64-75 65 Bone Surface Tumours and Tumour-like Conditions

(a) (b) (c)

(d) (e) (f)

Figure 2. Biopsy-proven periosteal osteosarcoma involving the anterior part of the proximal in a 65-year-old female who presented with a progressive swelling over the forearm: (a, b) radiographs showing a dense soft tissue mass attached to the cortex without abnormality in the adjacent medulla (arrows). No obvious periosteal reaction is evident in this case. (c) Computed tomography showing a dense periosteal soft tissue mass with matrix mineralisation (arrow). The bone marrow is normal. Magnetic resonance T1-weighted (d) pre-contrast and (e) post-contrast images showing enhancement of a well-defined periosteal mass after contrast administration (arrows). (f) T2-weighted image showing high signal intensity within the mass (arrow). No area of abnormal bone marrow signal is seen. reaction is common and can appear as solid non- moderate-to-dense fluffy, immature mass with broad aggressive cortical thickening or as aggressive Codman attachment to the cortex. Cortical erosion or thickening triangle, irregular or laminated forms. Periosteal may be present. There are several features that may reaction perpendicular to the osseous long axis and help differentiate high-grade surface osteosarcoma extending into the soft-tissue mass may also be seen.12 from parosteal or periosteal subtypes of surface osteosarcoma. A lucent cleavage plane between the High-grade Surface Osteosarcoma tumour and underlying cortex is a rare finding in high- High-grade surface osteosarcoma (Figure 3) is rare grade surface osteosarcoma, in contrast to parosteal and the least common subtype, comprising 10% of all osteosarcoma. Moreover, radiating spicules of periosteal surface osteosarcomas.13 It is more typically seen in reaction are less commonly seen than in periosteal the second or third decades of life,14 with a male-to- osteosarcoma.14 In addition, high-grade surface female ratio of 3-4:1.14-16 The lesion commonly affects osteosarcoma may involve the medulla or sometimes the diaphysis of bone, especially the mid or distal the entire circumference of bone,17 but intramedullary femur or in the tibial diaphysis. Histologically, a high- involvement or circumferential tumour involvement are grade surface osteosarcoma arises from the surface not typical features of periosteal osteosarcoma. of bone, with high mitotic activity identical to that of conventional high-grade intramedullary osteosarcoma.8 Osteoid Osteoma Osteoid osteoma (Figure 4) can be classified as On plain radiograph, it classically appears as a cortical, medullary, or subperiosteal subtypes based on

66 Hong Kong J Radiol. 2017;20:64-75 ACW Lee, KS Tse, KC Lai, et al

(a) (b)

Figure 3. High-grade surface osteosarcoma in a 46-year-old female who presented with thigh swelling for 3 months: (a) radiograph showing cortical thickening with dense sclerotic fluffy periosteal reaction at the mid diaphysis of right femur (arrow). No cleavage plane is seen between the tumour (c) (d) and underlying cortex, which is a differentiating feature from parosteal osteosarcoma. It also involves more than one half of the circumference of the bone, more commonly seen in high-grade surface osteosarcoma. (b) Computed tomography showing an expanded medial cortex of the femoral diaphysis, with spiculated periosteal reaction (arrow). Axial (c) T1-weighted and (d) T2-weighted with fat-saturation magnetic resonance images showing the tumour with deep intracortical involvement (arrows) but no intramedullary involvement.

(a) (b)

Figure 4. Osteoid osteoma in a 16-year-old male who presented with left pain: (a) the nidus is not clearly shown on radiograph. (b) Computed tomography showing a radiolucent nidus with central (c) (d) mineralisation at the left ilium (arrow), a characteristic finding of osteoid osteoma. (c) Magnetic resonance imaging is less useful in demonstrating the central nidus, but is better at showing bone marrow oedema (arrow). (d) Biopsy of lesion confirmed the diagnosis of osteoid osteoma (arrow). This patient was treated with two sessions of radiofrequency ablation and achieved a good response, with no analgesia required.

Hong Kong J Radiol. 2017;20:64-75 67 Bone Surface Tumours and Tumour-like Conditions radiographic findings. Cortical osteoid osteoma is the of life,26 and commonly involves the femur.27 Patients most common subtype.18 Classically patients complain usually present with insidious onset of pain and swelling. of nocturnal pain that can usually be relieved by nonsteroidal anti-inflammatory drugs. On radiograph, Periosteal chondrosarcoma are usually larger than it typically shows an intracortical nidus that is round benign periosteal chondroma. In a case series of 11 or oval and usually measures <2 cm in diameter.19 periosteal chondrosarcomas, none of the lesions were <3 It is usually radiolucent, but may also be calcified.1 cm.24 On radiographs, it may appear as a juxtacortical Cortical thickening and reactive sclerosis in the long soft tissue mass containing popcorn, spotty, peripheral bone shafts are typical. On computed tomography or ring-and-arc calcifications.28-31 They tend to be (CT), the nidus is usually well-defined and lucent, with more irregular and permeative on radiographs than central mineralisation. Surrounding cortical thickening .27,28,32 On CT, the lesion is juxtacortical, and periosteal reaction may be seen. Enhancement of and can be associated with intact, thickened, or eroded hypervascular nidus may be seen on contrast CT.20 On cortex. Peripheral enhancement can be present if magnetic resonance imaging (MRI), the nidus is of low- contrast is injected. MRI shows a juxtacortical mass to-intermediate signal on T1-weighted images, and of with T1-weighted hypointense and T2-weighted variable signal on T2-weighted images. Adjacent bone hyperintense signals. Intramedullary extension or marrow oedema may be present. Visualisation of the oedema may occur. Peripheral and septal enhancement nidus is better on CT than on MRI. However, MRI is following gadolinium injection is seen.30 better at demonstrating associated bone marrow and soft tissue oedema, joint effusion, and synovitis.21 Bizarre Parosteal Osteochondromatous Proliferation CARTILAGE-FORMING TUMOURS Also known as Nora’s lesion, bizarre parosteal Periosteal Chondroma osteochondromatous proliferation (Figure 8) is a rare, Periosteal chondroma (Figures 5 and 6), also known as benign exostotic osteochondromatous tumour that juxtacortical chondroma, is a benign tumour composed may occur in the hands, feet, , and long bones of of mature , and is the surface variant the upper and lower limbs.33 Recurrence is frequent of .1 It commonly affects the long bones (about 55%) following resection.33 Patients are usually in children and young adults, with a slight male in their third to fourth decade and both genders are predominance.22,23 The proximal humerus is the most affected.33,34 It usually presents as a minimally painful commonly affected site.23 On radiograph, it can be a pedunculated mass that enlarges slowly over months periosteal-based lytic lesion with internal chondroid or years,33,35 however a more aggressive growth pattern mineralisation. The adjacent cortex may be saucerised is also described.36 On radiographs, it may appear as with a varying degree of sclerosis. Marginal periosteal a calcified and osseous mass adjacent to the affected new bone formation may be present.24 On MRI, T1- bone, which may simulate an osteochondroma or other weighted imaging may show a hypointense signal and osteogenic tumour. At an early stage, the lesion can be cortical scalloping or saucerisation. It is hyperintense differentiated from osteochondroma or other osteogenic on T2-weighted imaging. Perilesional bone marrow tumours by the lack of medulla or cortical continuity oedema may be seen.24 with underlying bone. Nonetheless when mature, the lesion may appear to adhere to the adjacent bone with a As in intramedullary chondroid lesions, the pedunculated or sessile base, with the cortex of parent differentiation of a benign from low-grade malignant bone remaining intact.1,37 When it appears inseparable periosteal chondroid lesion is difficult. Larger lesion from the parent bone, it may mimic other benign size (>3 cm),25 intramedullary extension or oedema, or malignant conditions. is required for a and irregular soft tissue margins may suggest malignant definitive diagnosis. chondrosarcoma. Nonetheless, these features may overlap with those of benign lesions. On CT, the calcified and ossified masses show well- defined margins, typically without continuity with the Periosteal Chondrosarcoma medullary canal of the bones.38 Periosteal chondrosarcoma (Figure 7) is rarer than the benign periosteal chondroma. It occurs in a slightly On MRI, the lesion is classically described as cortically older age-group, mostly in the second to fourth decades based, without intramedullary extension. Tumour

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(a) (b)

Figure 5. Periosteal chondroma of the proximal humerus in a 1-month- old boy: (a) there is an incidental finding of a cortical- based lucent lesion at the proximal humerus on radiograph (arrow). Adjacent cortical saucerisation and sclerosis are present. (b) Magnetic resonance imaging showing a juxtacortical lesion with saucerisation of the adjacent cortex (arrow). No bone marrow oedema or adjacent soft tissue mass are present.

(a) (b) (c)

(d) (e)

Figure 6. Periosteal chondroma of the femur in a 22-year-old female who presented with a 2-month history of swelling: (a) radiograph showing a cortical- based lytic lesion with adjacent sclerosis and periosteal new bone formation (arrow). Internal calcification is evident. (b) Computed tomography showing a lucent lesion with sclerotic rim that is continuous with the elevated periosteum (arrow). Internal faint calcifications are seen. Magnetic resonance images showing an oval cortical-based mass with (c) isointense T1-weighted signal (arrow) and (d) hyperintense T2-weighted signal, with adjacent cortical erosion (arrow). (e) Peripheral enhancement (arrow) is seen on a post-gadolinium image. Excisional biopsy confirmed periosteal chondroma.

Hong Kong J Radiol. 2017;20:64-75 69 Bone Surface Tumours and Tumour-like Conditions

(a) (b)

(c)

F i g u r e 7 . Periosteal chondrosarcoma in a 37-year- old female who presented with a left mass: (a) radiograph and (b) computed tomography showing a juxtacortical mass at the proximal humerus metadiaphysis, with ring and arc calcifications. Cortical thickening and erosion are seen (arrows). (c) Whole-body showing increased tracer uptake over the left proximal humerus (arrow). Biopsy confirmed a periosteal chondrosarcoma.

involvement of the medullary canal can be seen in known as osteofibrous-like or juvenile adamantinoma, more aggressive forms.36 It is of low signal intensity is usually found in those aged 20 years or younger.41 on T1-weighted images. On T2-weighted image, a Patients commonly present with lower leg pain, hyperintense cartilage cap is sometimes seen. swelling, or deformity.

EPITHELIAL AND OSTEOFIBROUS On radiograph, both types of adamantinoma share TUMOURS similar features. They are usually central or eccentric Adamantinoma osteolytic tumours in the diaphysis or of Adamantinoma is a rare malignant tumour composed the tibia, slightly expansile, with sharply or poorly of epithelial and osteofibrous components. It can be delineated margins. They frequently involve the classified as classic or differentiated. Classic type anterior tibial cortex, with septations and peripheral adamantinoma is typically seen in patients aged 20 to 50 sclerosis.42 They are commonly intra-cortical lesions, years.39,40 Differentiated adamantinoma (Figure 9), also but cortical destruction and extra-cortical soft tissues

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(a) (b) (c) (d) (e)

(f) Figure 8. Bizarre parosteal osteochondromatous proliferation in a 40-year-old female who presented with a bony mass in the little finger: (a, b) radiographs showing an exophytic bony that appears contiguous with the underlying bony cortex, without cortical destruction (arrows). Excision was performed, with recurrence noted 3 months after surgery. (c, d) Radiographs showing recurrence of the exophytic bony mass (arrows). (e) Computed tomography showing the exostosis without bone destruction, medullary continuity or associated soft tissue mass (arrow). (f) T2-weighted magnetic resonance image showing bony outgrowth with a cartilaginous cap that is hyperintense (arrow). No intramedullary extension is seen. Re-excision of the mass was performed, and pathology results confirmed the diagnosis.

Figure 9. A 17-year-old male (a) (b) who presented with left knee pain: (a) frontal and (b) lateral radiographs showing a large well- defined geographic lytic lesion at the proximal tibia at a subarticular eccentric location (asterisks), subsequently biopsied and proven to be a giant cell tumour. There is another smaller lytic lesion at the anterior cortical region of the tibial proximal diaphysis (arrows), demonstrating well-demarcated margins and peripheral sclerosis. No cortical destruction, periosteal (c) (d) reaction, or extra-cortical soft tissue is seen. On (c) sagittal and (d) axial computed tomographic images, the biopsy-proven giant cell tumour is again shown (asterisk). The smaller lytic lesion at the anterior tibial cortical region (arrows) is more conspicuous than on radiographs. It demonstrates slight expansion, thinning of the anterior cortex, well- defined margins and peripheral sclerosis. No periosteal reaction or extra-cortical soft tissue is evident. of this lesion showed differentiated adamantinoma. Wide excision with bone grafting was offered for this patient.

Hong Kong J Radiol. 2017;20:64-75 71 Bone Surface Tumours and Tumour-like Conditions may be seen in 15% of cases.43 Periosteal reaction is not frequently seen. Synchronous lesions in the ipsilateral On radiograph, it typically shows a saucer-shaped fibula need to be looked out for, as these occur in irregular radiolucent cortical defect with adjacent 10% to 50% of cases.39 As classic adamantinoma is a sclerosis and periostitis in the characteristic location of low-grade with potential for , the posteromedial cortex of the distal femoral condyle.49 surgical intervention is the management of choice.44 Diagnosis can usually be made on radiograph, but CT The treatment for differentiated adamantinoma is less may be used in equivocal findings. CT may demonstrate well-established. Some authors recommend observation focal cortical thickening and fragmentation at the of small differentiated adamantinoma in children, and insertion of the medial head of the gastrocnemius wide resection for progressing lesions.45,46 tendon. Symmetrical findings may be seen on the contralateral side.50 MIMICS OF BONE SURFACE TUMOURS This lesion may be mistaken for other surface aggressive Cortical Desmoid lesions such as osteosarcoma, chondrosarcoma, Cortical desmoid (Figure 10) is a benign, self-limiting , or . The classic clue is its fibrous or fibro-osseous lesion that is believed to be location, and the absence of other aggressive features related to chronic stress applied by the adductor magnus such as soft tissue mass or medullary involvement, aponeurosis or medial head of gastrocnemius. It is sometimes further supported by the history of trauma usually seen at the posteromedial surface of the distal or strenuous exercise. It is important to distinguish this femoral metaphysis at the attachment of the adductor benign entity from other aggressive lesions, as this is a aponeurosis to the medial supracondylar ridge.47 It ‘don’t-touch’ lesion, not requiring biopsy for diagnosis. commonly occurs in young males of 10 to 15 years old. It frequently heals spontaneously and may disappear by These patients may be asymptomatic or complain of 20 years of age. If biopsy is performed, the lesion can pain and soft tissue swelling. In some cases, a history of be mistaken for malignancy, resulting in unnecessary preceding trauma may be reported.48 .51

(a) (b) (c)

Figure 10. A lytic lesion in an 8-year-old female following right knee contusion: (a) lateral radiograph of the right knee showing a lucent lesion with sclerotic base at the posteromedial aspect of the distal femoral metaphysis (arrow). (b, c) Computed tomography showing a lytic area with sclerotic base at the posteromedial metaphysis of the distal femur, and at the insertion site of the medial head of the gastrocnemius muscle (arrows). No associated soft tissue mass is seen. Findings are typical of cortical desmoid, a ‘don’t-touch’ lesion, and biopsy should be avoided.

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(a) (b) (c)

Figure 11. A 12-year-old female who presented with left forearm swelling for a month, without any history of trauma: (a) a rapidly appearing ossified mass over the proximal ulna was found on radiograph (arrow). (b) On computed tomography, a completely ossified mass is showing (arrow). In this case, the ossified mass was inseparable from the underlying bone. However, no other suspicious features such as cortical destruction or aggressive periosteal reaction are evident. (c) Serial follow-up radiographs showing remodelling of the ossified mass that gradually resolved 2 years after presentation (arrow).

Myositis Ossificans matures, complete ossification of the mass may be Myositis ossificans (Figure 11) is a pseudotumour that demonstrated.54 As in plain radiographs, recognising arises from muscles. It is a benign and self-limiting the imaging features that favour benignity is important, entity but can mimic an aggressive surface bone lesion. as pathological distinction between myositis ossificans It is most commonly seen in young adults, affecting the from osteosarcomas using may be difficult.54 large muscles of the extremities.52 Approximately 60% Serial radiographic follow-up and conservative to 70% of cases are associated with previous trauma.53 treatment with non-steroidal anti-inflammatory drugs It usually presents as pain and soft tissue mass, or as an are appropriate for most patients. incidental finding. Contrary to malignant bone tumours, pain is most severe in the early course of the lesion.53 CONCLUSIONS Bone surface lesions are not frequently encountered, and On radiograph it is usually shown as faint calcification making a correct diagnosis based on imaging alone is within 2-6 weeks of symptom onset. A more sharply often challenging. Biopsy is often required to establish circumscribed bone mass may appear after 6-8 weeks. a pathological diagnosis to aid in further management. Differentiation from malignancy can be challenging, Recognising the clinical and radiological features of but there are features that can help in suggesting the tumour-mimics can help minimise unnecessary invasive diagnosis. A centrifugal maturation pattern may be examination or intervention for benign lesions. observed in myositis ossificans, with more mature denser bone seen in the periphery of the mass. REFERENCES 1. Seeger LL, Yao L, Eckardt JJ. Surface lesions of bone. Radiology. Secondly, a complete lucent zone between the lesion 1998;206:17-33. cross ref and underlying bone on at least one of the projections 2. Schajowicz F, McGuire MH, Santini Araujo E, Muscolo DL, may be seen in myositis ossificans, whereas incomplete Gitelis S. Osteosarcomas arising on the surfaces of long bones. J separation may be seen in parosteal osteosarcomas due Bone Joint Surg Am. 1988;70:555-64. cross ref to the presence of a pedicle extending from the tumour 3. Huvos AG. Juxtacortical osteogenic . In: Bone tumors: diagnosis, treatment, and prognosis. 2nd ed. Philadelphia: WB from the parent bone. Intact bone cortex despite the Saunders; 1991:157-77. presence of periosteal new bone formation is another 4. Song WS, Jeon DG, Kong CB, Cho WH, Lee SY. Outcome of re- 53 excision for intralesionally treated parosteal osteosarcoma. J Surg feature that points to benignity. Oncol. 2011;103:264-8. cross ref 5. Vigorita VJ. Periosteum. In: Orthopaedic pathology. Philadelphia: On CT, a rim of peripheral calcification with central Lippincott Williams & Wilkins; 1999. p 275-87. area of low attenuation may be seen next to the 6. Hewitt KM, Ellis G, Wiggins R, Bentz BG. Parosteal osteosarcoma: bone in the early phase at 4-6 weeks. As the lesion case report and review of the literature. Head Neck. 2008;30:122-

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