The Journal of Bone & Joint Surgery

The Journal of Bone & Joint Surgery, Volume 87, Issue 7

Scientific Articles | July 01, 2005

Solitary Epiphyseal Enchondromas

Benjamin K. Potter, MD¹; Brett A. Freedman, MD¹; Ronald A. LehmanJr., MD¹; Scott B. Shawen, MD¹; Timothy R. Kuklo, MD¹; Mark D. Murphey, MD²

¹ Department of Orthopaedics and Rehabilitation, Walter Reed Army Medical Center, 6900 Georgia Avenue, N.W., Building 2, Clinic 5A, Washington, DC 20307. E-mail address for B.K. Potter: benjamin.potter@na.amedd.army.mil
² Department of Radiologic Pathology, Armed Forces Institute of Pathology, 6900 Georgia Avenue, N.W., Washington, DC 20306

View Disclosures and Other Information

The opinions and assertions contained herein are the private views of the authors and are not to be construed as official or as reflecting the views of the United States Army or the Department of Defense. All authors are employees of the United States Government. This work was prepared as part of their official duties and, as such, there is no copyright to be transferred.

Investigation performed at the Armed Forces Institute of Pathology and Walter Reed Army Medical Center, Washington, DC

The Journal of Bone and Joint Surgery, Incorporated

J Bone Joint Surg Am, 2005 Jul 01;87(7):1551-1560. doi: 10.2106/JBJS.D.02404

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Abstract

Background: Enchondromas originating in the epiphyses of long bones are rare. The purpose of the present study was to evaluate the prevalence as well as the radiographic and clinical characteristics of epiphyseal enchondromas among patients who had been referred to the Armed Forces Institute of Pathology and Walter Reed Army Medical Center.

Methods: We performed a retrospective review of 761 patients who had been referred to our two institutions over an approximately fifty-five-year period and who received a final diagnosis of enchondroma. All lesions had been biopsied, and the pathological diagnosis had been confirmed. Lesions of the hands, feet, or axial skeleton (253 patients) as well as lesions that appeared to originate in the metaphysis or diaphysis (475 patients) were excluded. Only enchondromas of the long bones that originated in the epiphysis were analyzed. The study group included thirty-three patients (twenty male patients and thirteen female patients) with a mean age of 26.7 years, including eleven patients with open physes. We performed additional descriptive analyses with regard to patient age, gender, lesion location, clinical presentation, and treatment as well as an extensive radiographic analysis.

Results: The most common locations were the proximal part of the humerus (ten lesions; 30%) and the distal part of the femur (six lesions; 18%). The most common presenting symptom was pain (twenty-three patients). Radiographic analysis demonstrated extensive matrix mineralization in association with twenty-three lesions. Twenty-eight of the thirty-three lesions were geographically well defined; of these, twenty-one had sclerotic borders, and seven did not. Although all lesions were centered and were predominantly located within the epiphysis, twenty of the thirty-three lesions demonstrated radiographic evidence of metaphyseal extension, including four of the eleven lesions in patients with open physes. Twenty-four lesions extended into the subchondral bone. The mean size of the thirty-three enchondromas in greatest radiographic dimension was 2.7 cm (range, 1.1 to 4.9 cm). Twenty-six of the thirty-three lesions were amenable to surgical treatment with curettage with or without bone-grafting, with only one recurrence. With the limited follow-up available, no lesion underwent sarcomatous degeneration.

Conclusions: Epiphyseal enchondromas are rare lesions. Although their biologic behavior appears to mirror that of conventional metaphyseal enchondromas, their proximity to the joint space may lead to more frequent painful symptoms, a propensity for physeal involvement, and the need for earlier definitive surgical intervention.

Level of Evidence: Prognostic Level IV. See Instructions to Authors for a complete description of levels of evidence.

Figures in this Article

Achondroma is any benign tumor composed solely of normal-appearing, mature hyaline cartilage¹. The term enchondroma usually is reserved for intramedullary chondromas as opposed to eccentrically located periosteal chondromas or soft-tissue chondromas². Enchondromas are the second most common benign cartilaginous tumor, after osteochondromas³. In contrast to chondrosarcomas, which most frequently affect the axial skeleton (the spine and pelvis), enchondromas have a distinct predilection for the appendicular skeleton and are the most common benign bone tumor of the hand, particularly the phalanges¹. The cartilaginous nodules characteristic of enchondromas may be hamartomatous proliferations rather than truly neoplastic lesions². Regardless of this distinction, enchondromas are uniformly benign lesions with limited potential for malignant degeneration, particularly for monostotic disease^1,4.

Nonetheless, the complexities of differentiating enchondromas from low-grade chondrosarcomas mandate a thorough understanding of the disease process and spectrum. The clinician needs an appreciation of the typical clinical, radiographic, and pathological manifestations of these tumors. An important step in understanding the characteristics of this, or any, bone tumor is identifying the segments of bone involved. It is widely believed that enchondromas exclusively affect the metaphysis and diaphysis, but several studies have documented cases of epiphyseal involvement by enchondromas in patients with Ollier disease and its variants^5-9. However, only fifteen monostotic epiphyseal enchondromas have been reported previously, to our knowledge^2,10-12. The existence of pathologically proven epiphyseal enchondromas represents an important diagnosis, although rare, in the differential diagnosis of radiolucent epiphyseal lesions.

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Figs. 1-A and 1-B: Anteroposterior (Fig. 1-A) and lateral (Fig. 1-B) radiographs showing a distal radial epiphyseal enchondroma in a skeletally mature twenty-year-old man who presented with a symptomatic "mass" due to expansile remodeling of the cortex. In spite of mild extension into the distal metaphysis, the center and the majority of the lesion were located in the epiphysis. Matrix mineralization of more than two-thirds of the eccentrically located lesion and well-defined, sclerotic margin are evident.

Materials and Methods

Our goal was to identify and analyze cases in which a solitary enchondroma appeared to have originated in the epiphysis of the long bones of the appendicular skeleton (or in the former epiphyseal region beyond the physeal scar in skeletally mature patients). After obtaining review exemption status from our institutional review boards for the use of existing specimens and records, we retrospectively reviewed the archives of the Armed Forces Institute of Pathology and Walter Reed Army Medical Center for the medical records, pathological reports, and radiographic studies of all patients who had been referred to our institutions over an approximately fifty-five-year period with a final diagnosis of enchondroma. Patients with a definitive diagnosis of epiphyseal chondrosarcoma were excluded, as such lesions have been previously described and may be more common¹². This review yielded 761 patients with a definitive diagnosis of solitary enchondroma. Two hundred and fifty-three patients with lesions involving the axial skeleton, phalanges, metacarpals, and metatarsals were excluded as enchondromas of the hands and feet are exceedingly common, are generally benign, and may involve the entire bone while the axial skeleton lacks well-defined epiphyses. Four hundred and fifty-three metaphyseal and diaphyseal lesions also were excluded, as were twenty-two lesions that appeared to originate in the metaphysis with secondary involvement of the epiphysis. In addition, cases of multiple enchondromatosis with epiphyseal involvement were excluded as this disorder also has been previously described in detail⁵. That is, only solitary long-bone lesions in which both the apparent origin and the majority of the chondromatous lesion were epiphyseal were included (Figs. 1-A and 1-B). The remaining thirty-three lesions were solitary enchondromas that originated in the epiphysis of the appendicular long bones. Thirteen of these lesions were briefly mentioned in previous reports from our institutions^11,12. The mean age of these patients was 26.7 years (range, seven to sixty-one years) at the time of diagnosis. There were twenty male patients and thirteen female patients. Eleven patients with a mean age of 13.3 years (range, seven to sixteen years) had open physes.

The clinical records were reviewed with regard to patient age, gender, presenting symptoms, and treatment. All lesions had undergone biopsy as well as radiographic and pathologic analysis by multiple musculoskeletal radiologists and pathologists. Enchondromas were defined as lesions with cellularity exceeding that of resting articular cartilage, with small nuclei, uniform nucleoli, and abundant cytoplasm. There was little, or very rare, mitotic activity, although limited numbers of binucleate lacunae occasionally were seen. Radiographic studies were evaluated to determine the size and location of the lesion as well as to evaluate several characteristics, including physeal status (open or closed), matrix mineralization (presence or absence, extent, and character), internal septations (presence or absence), epiphyseal centricity (centric or eccentric), type of bone lysis (geographic, moth-eaten, or permeative [according to the system of Lodwick et al.¹³], or sclerotic), periosteal reaction (presence or absence and character), expansile remodeling of bone (presence or absence and degree), erosion to subchondral bone, and evidence of metaphyseal extension.

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Fig. 2: Diagram of the long, tubular bones of the extremities, demonstrating the locations of epiphyseal enchondromas in the thirty-three patients in the present series.

Results

The most common locations of the thirty-three solitary epiphyseal enchondromas were the proximal part of the humerus (ten lesions; 30%), the distal part of the femur (six lesions; 18%), the proximal part of the femur (five lesions; 15%), and the proximal part of the tibia (four lesions; 12%) (Fig. 2). The most common presenting symptom was pain (twenty-three patients; 70%). Three patients presented with a pathologic fracture, and two presented with a so-called mass due to expansile remodeling of superficial lesions in the distal part of the radius or distal part of the fibula (see Appendix). No patient had a true soft-tissue mass. The lesion was discovered incidentally in five patients (15%). Constitutional symptoms were reported by only a single patient, in whom an epiphyseal enchondroma was incidentally discovered during evaluation of adjacent osteomyelitis.

Twenty-six patients (79%) were managed with intralesional curettage with bone-grafting of the lesion. There was only one instance of tumor recurrence following this modality of treatment; the recurrence was attributed to incomplete curettage and the lack of adjuvant therapy (e.g., phenol or cryotherapy) and was successfully treated with repeat curettage and bone-grafting. Six patients with a mean age of 25.7 years (range, thirteen to thirty-five years) who had been managed definitively at other institutions underwent resection of the involved epiphysis because of concerns about possible malignancy prior to referral for definitive diagnosis. Two of these patients underwent reconstructive hemiarthroplasty of the hip (one patient) or shoulder (one patient). Two patients had resection without reconstruction of the distal part of the ulna (one patient) or the proximal part of the fibula (one patient), and one patient underwent resection followed by allograft reconstruction of the distal part of the radius. One thirteen-year-old girl underwent resection of the distal part of the fibula followed by fusion of the ankle syndesmosis. Although we believe that these treatment modalities were, in general, unnecessarily radical, they highlight the potential difficulties of making this diagnosis.

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Figs. 3-A through 3-D: A forty-nine-year-old woman who had a distal femoral epiphyseal enchondroma in the lateral femoral condyle. Figs. 3-A and 3-B Anteroposterior radiograph (Fig. 3-A) and lateral tomographic scan (Fig. 3-B) showing the lesion. Minimal matrix mineralization and internal septations and no cortical expansion are evident. The lesion has eroded to subchondral bone but does not cross the closed physis.

Plain Radiographic Imaging

Routine radiographic studies were available for all thirty-three patients (see Appendix). Because of the historical time frame of many of the cases, advanced imaging studies were available for only nine patients (Figs. 3-A through 3-D). The adjacent physis was open in eleven of the thirty-three patients. Matrix mineralization with the characteristic "rings and arcs" appearance was present in twenty-three lesions (70%), whereas internal septations were appreciated in nineteen (58%). Eighteen lesions (55%) were eccentrically located, and fifteen (45%) were centered within the involved epiphysis. Twenty-one lesions (64%) were noted to have Lodwick et al.¹³ geographic 1A margins, with well-defined, sclerotic borders, and an additional seven lesions had geographic 1B margins, with well-defined borders without adjacent sclerosis. Four lesions were diffusely sclerotic with flocculent matrix mineralization. One lesion demonstrated geographic lysis with poorly defined borders and without evidence of sclerosis (geographic 1C margins). Eight lesions were associated with mild or moderate expansile remodeling of the cortex, whereas none were associated with extensive expansile remodeling of the cortex. Additionally, twenty-four lesions (73%) involved the adjacent subchondral bone. Finally, although all of the lesions predominantly involved the epiphysis, twenty lesions (61%) demonstrated radiographic evidence of metaphyseal extension, including four of the eleven lesions in patients with open physes (Figs. 4-A and 4-B). The mean size of the greatest dimension of the lesion margins as measured on plain radiographs was 2.7 cm (range, 1.1 to 4.9 cm).

Advanced Imaging

Conventional tomographic scans were available for four patients. These scans reflected similar lesion characteristics as observed on plain radiographs and confirmed the epiphyseal origin of the lesions (Fig. 3-B). Bone scans were available for seven patients. These scans showed homogeneous uptake of isotope in all lesions; however, the degree of uptake was less than that in the anterior superior iliac spine in four patients (57%) and equal to that in the anterior superior iliac spine in three patients (43%), demonstrating relatively limited enhancement^12,14.

Computed tomographic scans were available for three patients (Fig. 3-C). Mild endosteal scalloping was noted in two of the three patients. The third patient had scalloping of more than two-thirds of the thickness of the cortex, but only over a small portion (less than one-third) of the lesion's width. Neither expansile remodeling of bone nor cortical destruction was appreciated, and no pathologic fractures were noted on computed tomographic scans. Furthermore, cortical thickening was not found and there was no soft-tissue extension or cortical breakthrough.

Magnetic resonance images were available for five patients (Fig. 3-D). These studies revealed homogeneous epiphyseal lesions with low signal intensity on T1-weighted images and mildly heterogeneous lesions with high signal intensity on T2-weighted images. No soft-tissue masses or extension were apparent.

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Fig. 3-C: Axial computed tomographic scan confirming the absence of mineralization or septations as well as the subchondral cortical erosion.

Gross and Histologic Pathology

Biopsy specimens invariably demonstrated gross tissue with a tan-white, glassy, and cartilaginous appearance. All lesions demonstrated findings consistent with a diagnosis of enchondroma, specifically, islands of cartilage with small nuclei and abundant cytoplasm surrounded intermittently by shells of lamellar bone. Occasional active chondrocyte proliferation and focal areas of cellular atypia were noted, but no histologic evidence of overt malignancy was seen. As noted, patients with a final diagnosis of low-grade chondrosarcoma were excluded; however, the majority of these patients had been referred to us because of the difficulty in distinguishing between these two lesions. We believed that the radiographic and histologic characteristics of these lesions were consistent with an epiphyseal enchondroma in each case.

Discussion

Origin of Epiphyseal Enchondromas

In 1943, Jaffe and Lichtenstein² proposed that enchondromatous nodules are actually displaced rests of normal physeal cartilage cells. This is still the most widely accepted theory regarding the genesis of enchondroma. With continued growth, these normal proliferative cells are relocated to the metaphyseal and diaphyseal bone. This variation from normal chondrocyte hypertrophy and apoptosis probably represents not a true neoplasia but rather a developmental anomaly leading to regionally confined or generalized dysplasias⁵. Many of these nodules may regress and undergo partial calcification, producing the characteristic radiodense areas of mineralization seen radiographically. The number of rests and the rate at which they are aberrantly displaced determine the number and size of the enchondromatous nodules. Typically, multiple small cartilaginous nodules are formed; these nodules tend to coalesce and to become interspersed with areas of normal marrow fat. Furthermore, these islands often develop enchondral ossification, which is the basis for the radiographic "arcs and rings" pattern. Coalescent lesions characterized by benign islands of cartilage and a trabecular encasement pattern are pathognomonic of benign enchondromas^4,12.

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Fig. 3-D: Sagittal T2-weighted magnetic resonance imaging scan demonstrating homogeneous high signal intensity throughout the enchondroma.

The actual mechanism for the longitudinal displacement of these proliferative rests has not been definitively demonstrated; however, the leading hypothesis was well summarized by Brien et al.¹⁵ on the basis of their investigation of specimens taken from children with Ollier disease. Those investigators postulated that the enchondromatous rest starts as a dysplastic nidus within the physeal proliferative zone, which then progresses vertically downward toward the metaphysis. When this dysplastic nidus reaches the primary ossification zone at the metaphysis, having already survived the zone of hypertrophy and its apoptotic terminal end, the nidus is then pinched off from the physis. The lesion then begins to migrate into the metaphyseal bone with continued growth.

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Figs. 4-A and 4-B: A Oblique (Fig. 4-A) and lateral (Fig. 4-B) radiographs showing a distal fibular epiphyseal enchon-droma in a thirteen-year-old girl who presented with a symptomatic mass associated with expansile remodeling of the cortex. The central lesion demonstrates extensive matrix mineralization and ex-pansile cortical remodeling with extension into the distal metaphysis across the open physis.

It is our belief that the pathogenesis of primary epiphyseal enchondromas can be explained by extension of this theory. Rather than occurring in the vertical cellular columns leading to the primary enchondral ossification center (i.e., at the physis-metaphysis interface), the error that produces epiphyseal enchondromas must occur in the vertical columns leading to the secondary ossification center, which is responsible for the radial growth of the epiphysis.

Recent genetic studies of enchondroma genesis support these theories. The Indian hedgehog-parathyroid hormone-related protein (Ihh-PTHrP) pathway is critical to the normal development of enchondral bones as well as to the regulation of the proliferation and differentiation of growth-plate chondrocytes¹⁶. A mutation in the type-I PTHrP receptor constitutively activates Ihh signaling in vitro and has been demonstrated to cause enchondroma development in transgenic mice¹⁷. It is probable that a similar disturbance in humans results in the failure of physeal chondrocyte apoptosis and in continued proliferation as the mutant chondrocytes migrate from the growth plate with continued physeal growth. Other studies have demonstrated that the chromosomal and genetic mutations in enchondromas and chondrosarcomas are nonrandom^18,19 and that the specific abnormalities may have diagnostic and prognostic importance with regard to tumor behavior in vivo^20-23.

Clinical Behavior of Epiphyseal Enchondromas

Epiphyseal enchondromas, like conventional enchondromas, are characterized by a lobular chondroid matrix containing benign cartilaginous cells with prominent matrix calcification. They manifest as lucent, well-demarcated, round, or oval lesions and occasionally as expanded radiolucent lesions with thinned cortical margins that may be susceptible to fracture. All of our patients demonstrated clinical and radiographic characteristics that were consistent with a benign enchondroma of epiphyseal origin, and the diagnosis was pathologically confirmed in all cases. Previous reports of enchondromas with epiphyseal involvement have consisted mostly of patients with multiple enchondromatosis^2,5-12. The only previous reports on more than one solitary epiphyseal enchondroma included ten¹¹ and three¹² patients from the present series. The former report was only a brief abstract. Our findings demonstrate that monostotic enchondromas may arise primarily in the epiphysis of long bones, with or without extension into the metaphysis and independent of physeal status. It has been suggested that 2% to 5% of enchondromas have epiphyseal origins^4,15, but published support for these statements is lacking. In the present series, epiphyseal enchondromas constituted 4.3% (thirty-three) of all 761 enchondromas and 6.5% (thirty-three) of those involving the long bones of the appendicular skeleton. However, Dahlin and Unni²⁴ reported only one enchondroma that was definitely of epiphyseal origin in their series of 245 lesions. Therefore, we believe that our series is affected by a selection bias secondary to the referral basis of our practice. Thus, although epiphyseal enchondromas are potentially more common than previously appreciated, they probably are less common in clinical practice than our series suggests.

The skeletal distribution of these epiphyseal enchondromas was largely consistent with the findings described in previous reports on conventional enchondromas^1,4,24,25, although lesions of the humerus were somewhat more common than those of the femur in the present series. Although it has been suggested that as many as 40% of solitary enchondromas may be associated with some form of pain⁴, a significantly larger proportion (70%) of the lesions in our series were associated with pain, qualifying them as clinically atypical enchondromas. We attribute this difference to the close proximity of the epiphyseal lesions to the joint space and the frequent involvement of subchondral bone. Although previous large clinical series of enchondromas have consisted of surgically treated or, at least, pathologically proven enchondromas^1,4,24,25, the percentage of lesions in the present study that required definitive surgical treatment (97%; thirty-two of thirty-three) was much higher than might be expected for a similar series of conventional enchondromas. This finding also may have been due to selection bias in our series as well as to the greater need for pathologic diagnoses, given the atypical location of these lesions. The mean size of these lesions in greatest radiographic dimension (2.7 cm) was substantially less than that reported for typical enchondromas located in the metaphysis or diaphysis (6 cm)⁴. Finally, in contrast to conventional metaphyseal enchondromas, twenty (61%) of the thirty-three epiphyseal enchondromas in the present series crossed the adjacent physis, including four of the eleven lesions in patients with open growth plates.

We believe that all of these unusual trends in the behavior of epiphyseal enchondromas can be attributed to their epiphyseal location as opposed to biologic differences. Specifically, the close proximity to the joint space and the limited potential medullary space for growth may result in earlier pain, smaller lesions at the time of presentation, and greater need for definitive pathologic diagnosis and surgical treatment. Likewise, a higher proportion of these lesions (55%; eighteen of thirty-three) were eccentrically oriented within the epiphysis, which again may have been related to the epiphyseal anatomy and to the less longitudinal orientation of the adjacent cortical barriers to lesion extension.

Physeal Involvement

While the resistance of cartilage to tumor invasion is well known, Kuettner et al.²⁶ proposed the hypothesis that physeal cartilage is resistant to both tumor angiogenesis and tumor cell invasion because of a unique collagenase inhibitor. This theorem was later confirmed by others^27,28. Enneking and Kagan²⁸, in describing the epiphyseal extension of metaphyseal osteosarcomas, reported that the physis did act as a barrier to tumor spread, although it did not ultimately succeed in restraining the malignant tissue in most cases. Spira and Farin²⁹ reported that the most common method of extension was direct penetration through the epiphyseal plate along vascular channels or lateral penetration in continuity with epiphyseal vessels passing through the perichondral ring. The actual mechanism of tumor inhibition by the cartilaginous epiphyseal plate in skeletally immature individuals remains unknown⁹. It follows that the presence of growth-plate cartilage may play a role in limiting extension of conventional metaphyseal enchondromas to the epiphysis. However, in the present study, four of the eleven patients with open physes demonstrated metaphyseal extension of the lesion. Additionally, although we did not specifically examine the epiphyseal extension of juxtaphyseal metaphyseal enchondromas, we excluded twenty-two patients who demonstrated epiphyseal extension of metaphyseal lesions, including seven patients with open physes.

It is generally believed that, in these rare instances of epiphyseal involvement, extension of a lesion from the metaphysis into the epiphyseal end of the bone occurs secondarily, after closure of the physis^5,30. However, we noted metaphyseal extension in 61% (twenty) of the thirty-three epiphyseal lesions in the present series, suggesting that physeal violation of enchondromas may be more common than previously appreciated.

Malignant Potential

The risk of sarcomatous degeneration of enchondromas increases in proportion to the amount of dysplastic tissue (that is, the number and size of lesions) present in the patient^31,32. Gabos and Bowen⁵ described what we believe to be the only reported case of malignant degeneration of an enchondroma with epiphyseal involvement. To our knowledge, no patient in our series later demonstrated evidence of malignant degeneration following the initial diagnosis, and patients with a primary definitive diagnosis of chondrosarcoma were excluded from our series. These patients were excluded because, in addition to having been previously described in greater numbers¹², retrospective attribution of epiphyseal chondrosarcomas to malignant degeneration of epiphyseal enchondromas would have been speculative at best. However, as much as 40% of chondrosarcomas may show evidence of persistent, benign enchondroma tissue, suggesting that a substantial proportion of chondrosarcomas probably originate from enchondromas⁴.

Distinguishing between enchondromas and low-grade chondrosarcomas on the basis of their radiographic and pathological features can be difficult. One of us (M.D.M.) and colleagues¹², in an effort to identify clinical and radiographic features that most reliably distinguished the two types of lesions, reviewed a patient population that overlapped with that of the current study and included three of the same patients. That investigation of ninety-two enchondromas and ninety-five chondrosarcomas revealed several features that may assist in the differentiation of enchondromas from chondrosarcomas: pain, patient age, tumor size, deep endosteal scalloping (involving more than two-thirds of the cortical thickness along more than two-thirds of the lesion), cortical destruction, a soft-tissue mass (on computed tomography or magnetic resonance imaging), periosteal reaction, and marked lesional uptake on bone-scanning. The authors suggested that these findings allow for an accurate clinical distinction between chondrosarcoma and enchondroma, without the need for biopsy, in 90% of cases. Of note, an epiphyseal lesion was significantly more likely to represent a chondrosarcoma than an enchondroma in that series (p = 0.009)¹². Other authors have attempted to classify the lesions on the basis of their rate and pattern of gadolinium enhancement on magnetic resonance imaging, with varying success^33-35. Mirra et al.³⁶ developed criteria for distinguishing between enchondromas and low-grade chondrosarcomas on the basis of histologic findings, a notoriously difficult task. They found that enchondromas were defined by normal rests of hyaline cartilage separated by normal marrow with intervening plates of normal lamellar bone, whereas chondrosarcomas demonstrated a confluent mass of cartilage, separated only by fibrous bands, that permeated the marrow and "trapped" lamellar bone.

Other Diagnostic Considerations

Epiphyseal enchondroma must also be distinguished from clear-cell chondrosarcoma, chondroblastoma, and epiphyseal osteomyelitis. Clear-cell chondrosarcoma shows a lobulated chondroid appearance, prominent clear tumor cells, and osteoclast-type giant cells⁹. Chondroblastoma can be distinguished from epiphyseal enchondroma by the presence of benign-appearing cartilaginous islands in a background of chondroblastic cells lacking cellular atypia⁹. Furthermore, osteomyelitis of the epiphysis has been well described as a distinct form of osteomyelitis in children^37,38, and the radiographic characteristics of an epiphyseal abscess are manifested by a lytic focus, which is generally well demarcated¹⁰. The value of clinical presentation in distinguishing lucent lesions may be limited to cases of acute osteomyelitis.

Strengths and Weaknesses of the Study

One of the weaknesses of the present series was the retrospective nature of our review. The referral nature of our series precluded long-term follow-up, and it has been suggested that five to ten-year follow-up is necessary in order to absolutely exclude recurrence and sarcomatous degeneration^4,36. As the majority of patients had received surgical treatment at other institutions, we cannot comment on the adequacy of curettage or the use of appropriate adjuvants. It is also possible that some of these so-called solitary enchondromas actually were due to occult enchondromatosis, as skeletal surveys were not performed for any patient and surveillance or diagnostic bone scans were available for only a minority (seven) of the thirty-three patients. Likewise, because of the time frame associated with our historical review, advanced imaging studies were not available for the majority of patients. However, the consecutive series from which we isolated these epiphyseal lesions was quite large and spanned more than five decades, and the present study represents by far the largest clinical series of epiphyseal enchondromas described to date, whether solitary or multiple in origin.

In conclusion, epiphyseal enchondromas, although uncommon, represent a distinct clinical entity and deserve consideration in the differential diagnosis of radiolucent or chondroid epiphyseal lesions. The natural history of epiphyseal enchondromas seems to parallel the benign course of the more commonly occurring metaphyseal-diaphyseal lesions. However, the close proximity to the joint space may lead to relatively increased complaints of pain, a propensity for physeal involvement, and the need for earlier surgical intervention. In the absence of symptoms, the atypical location of these tumors also may justify earlier biopsy for pathologic diagnosis as opposed to the serial radiographic observation that is warranted for many metaphyseal and diaphyseal enchondromas. Close radiographic follow-up or early surgical treatment of these lesions appears warranted.

Appendix

Tables presenting the clinical and radiographic characteristics of all enchondromas in this series are available with the electronic versions of this article, on our web site at (go to the article citation and click on "Supplementary Material") and on our quarterly CD-ROM (call our subscription department, at 781-449-9780, to order the CD-ROM). ?

Acknowledgements

The authors did not receive grants or outside funding in support of their research or preparation of this manuscript. They did not receive payments or other benefits or a commitment or agreement to provide such benefits from a commercial entity. No commercial entity paid or directed, or agreed to pay or direct, any benefits to any research fund, foundation, educational institution, or other charitable or nonprofit organization with which the authors are affiliated or associated.

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Topics

biopsy ; cancer ; chondrosarcoma ; bone transplantation ; cartilage ; chondroma ; diaphyses ; enchondromatosis ; femur ; epiphysial cartilage

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Benjamin K. Potter, Brett A. Freedman, Ronald A. LehmanJr., Scott B. Shawen, Timothy R. Kuklo, Mark D. Murphey; Solitary Epiphyseal Enchondromas. The Journal of Bone & Joint Surgery. 2005 Jul;87(7):1551-1560.

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