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Differential Diagnosis of Cartilaginous Lesions of Bone

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Differential Diagnosis of Cartilaginous Lesions of Bone Differential Diagnosis of Cartilaginous Lesions of Bone David Suster, MD; Yin Pun Hung, MD, PhD; G. Petur Nielsen, MD Context.—Cartilaginous tumors represent one of the most Data Sources.—PubMed (US National Library of Med- common tumors of bone. Management of these tumors icine, Bethesda, Maryland) literature review, case review includes observation, curettage, and surgical excision or of archival cases at the Massachusetts General Hospital, resection, depending on their locations and whether they are and personal experience of the authors. benign or malignant. They can be diagnostically challenging, Conclusions.—This review has examined primary well- particularly in small biopsies. In rare cases, benign tumors differentiated cartilaginous lesions of bone, including their may undergo malignant transformation. differential diagnosis and approach to management. Objective.—To review common cartilaginous tumors, Because of the frequent overlap in histologic features, including in patients with multiple hereditary exostosis, particularly between low-grade chondrosarcoma and Ollier disease, and Maffucci syndrome, and to discuss enchondroma, evaluation of well-differentiated cartilagi- problems in the interpretation of well-differentiated nous lesions should be undertaken in conjunction with cartilaginous neoplasms of bone. Additionally, the concept thorough review of the imaging studies. of atypical cartilaginous tumor/chondrosarcoma grade 1 (Arch Pathol Lab Med. 2020;144:71–82; doi: 10.5858/ will be discussed and its use clarified. arpa.2019-0441-RA) artilage-forming tumors comprise one of the most are symptomatic or cause functional impairment, such as C common bone tumors, with enchondroma and osteo- restricted movement or complications from fractures. The chondroma encompassing the overwhelming majority of clinical management and prognosis depend heavily on the benign cartilaginous lesions and low-grade chondrosarcoma location and the pathologic diagnosis.2 With limited tissue, being the most common malignant cartilaginous tumor.1 the differential diagnosis may be problematic, particularly These tumors are characterized by the formation of a with regard to distinguishing enchondroma from low-grade cartilaginous matrix and can sometimes display overlapping chondrosarcoma. These tumors may display characteristic histologic features, which may pose a problem for diagnosis, clinical and radiologic features that allow for this distinction; especially in cases where histologic material is limited. however, the histologic overlap in the well-differentiated In the World Health Organization (WHO) fourth edition lesions can preclude a definitive diagnosis, and some studies 1 (2013) classification, cartilaginous tumors were classified have shown significant interobserver variability even among as either benign (such as osteochondroma and enchon- orthopedic pathologists.3 In a study by Eefting et al4 droma), intermediate (locally aggressive/rarely metastasiz- assessing interobserver variability, considerable variation in ing, such as chondromyxoid fibroma, chondroblastoma, the histologic assessment of cartilaginous tumors was and atypical cartilaginous tumor/chondrosarcoma grade 1), demonstrated (j coefficient ¼ 0.78). The greatest variability or malignant (chondrosarcoma grades 2 and 3 and other occurred in the distinction between enchondroma and grade high-grade chondrosarcomas). In the upcoming WHO 1 chondrosarcoma (j coefficient ¼ 0.54).4 classification, chondroblastoma and chondromyxoid fibro- This review discusses some of the more common benign ma have been moved into the benign category. No cartilaginous tumor belongs to the intermediate category. and malignant cartilaginous tumors as listed above. Additionally, the use of the term atypical cartilaginous tumor Furthermore, relevant clinical syndromes, including multiple is further delineated. hereditary exostosis (MHE), Ollier disease, and Maffucci Overall, benign cartilaginous lesions behave in an syndrome, are discussed, as the risks of malignant indolent fashion and do not require treatment, unless they transformation of benign cartilage tumors in these patients are increased. Accepted for publication September 10, 2019. OSTEOCHONDROMA From the Department of Pathology, Massachusetts General Osteochondroma is a benign cartilage-capped tumor Hospital and Harvard Medical School, Boston. The authors have no relevant financial interest in the products or arising on the surface of bones and is the most common companies described in this article. benign cartilage tumor of bone. More than 80% of Presented in part at the 11th Annual Midwestern Conference: osteochondromas are solitary; they are usually diagnosed Update Course in Surgical Pathology; September 14–16, 2018; by the second decade of life. There is a slight male Milwaukee, Wisconsin. Corresponding author: G. Petur Nielsen, MD, Department of predominance. They typically arise in the area of the Pathology, Massachusetts General Hospital, 55 Fruit St, Boston, MA metaphysis of long bones derived from endochondral 02114 (email: [email protected]). ossification, most commonly the distal femur, proximal Arch Pathol Lab Med—Vol 144, January 2020 Differential Diagnosis of Cartilage Lesions—Suster et al 71 Table 1. Comparison of Features Distinguishing Osteochondroma From Secondary Chondrosarcoma Arising in Osteochondroma Features Osteochondroma Secondary Chondrosarcoma Size Average 3–6 cm, although may grow larger than Often larger, although smaller lesions (,10 cm) 20 cm have been identified Symptoms Usually asymptomatic or related to mechanical Pain unrelated to movement or nocturnal pain symptoms/fracture Growth May display growth until growth plates close, Continued growth after skeletal maturity; then should remain stable sudden acceleration in growth of bone and cartilage cap components Cartilage cap thickness Usually less than 2–3 cm Generally thicker cartilage cap of more than 3– 4cm Microscopic findings Endochondral ossification with overlying mature Large lobulated cartilaginous nodules separated hyaline cartilage and a relatively well- by fibrous septa, increased cellularity, nuclear demarcated fibrous sheath. Chondrocytes atypia, mitotic activity, and overt infiltration show minimal atypia. No infiltration of soft into soft tissue or through the medullary tissue or infiltration of underlying bony connection into the underlying bone with trabeculae encasement of bony trabeculae tibia, and proximal humerus, but they can also arise on the thick cartilage cap with prominent calcifications, soft tissue surface of flat bones, such as the ilium or scapula.1,2,5–7 invasion, infiltration of the stalk, erosion of bone, and tumor Although initially believed to be a developmental invasion of the underlying bone are features of malignant anomaly, it has been shown subsequently that sporadic transformation (Table 1).1,2,9,11,16,17 osteochondromas harbor homozygous EXT1 and EXT2 Osteochondromas are usually observed or resected in deletions within a subset of chondrocytes within the symptomatic patients. Symptoms may be due to mechanical cartilaginous cap, indicating that it is a neoplastic process.3 issues, impingement on adjacent nerves, development of a Additionally, families with MHE have been shown to harbor bursa on the surface of the cap, or a pathologic fracture germline mutations in the EXT1 or EXT2 genes.8,9 through the stalk. Radiographic findings in osteochondroma show that osteochondroma arises from the surface of the bone with MHE (OSTEOCHONDROMATOSIS) continuity of the cortices and of the medullary cavities Multiple hereditary exostosis is an autosomal dominant (Figure 1, A and B), often pointing away from the nearest condition in which patients develop multiple osteochon- joint. Rarely, osteochondroma is sessile with a broad-based dromas by the second decade of life. Approximately 60% of stalk.10 Magnetic resonance imaging (MRI) is the most patients have a family history. Multiple hereditary exostosis useful imaging modality for assessing the thickness of the has an incidence of approximately 1 in 50 000 and, in rare cartilaginous cap, which can be variable.11,12 patients, presents as part of a separate genetic syndrome, Grossly, osteochondroma contains a cartilaginous cap and such as trichorhinophalangeal syndrome or Potocki-Shaffer an underlying stalk. The outer layer consists of a thin fibrous syndrome.1 It is now known that germline alterations in the sheath overlying the bluish gray cartilaginous cap (Figure 1, EXT1 (8q24) or EXT2 (11p11-p12) gene drive the disease. C). It is important to document the maximum thickness of this cap. Microscopically, this outer fibrous layer is the Similar to nonhereditary osteochondromas, aberrations of perichondrium. The cartilage cap is of variable thickness and the EXT genes lead to dysfunctional proteins exostosin 1 at the base undergoes endochondral ossification (Figure 1, and exostosin 2 and the subsequent failure of heparin sulfate 1,2,11 polymerization required for normal cartilaginous develop- D). The chondrocytes within the cap are usually 4,5,9,18 organized in a similar fashion to the normal growth plate. ment. Both the cellularity of the cartilage and the size of the From an early age, these patients present with multiple chondrocytes increase within the deeper layers of the cap, osteochondromas, which continue to grow in size until with the chondrocytes arranged in a vaguely columnar skeletal maturity with the closure of the growth plates. fashion. The cartilaginous matrix at
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