AIRP Best Cases in Radiologic- Pathologic Correlation
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1 Note: This copy is for your personal non-commercial use only. To order presentation-ready copies for distribution to your colleagues or clients, contact us at MUSCULOSKELETAL IMAGING AIRP Best Cases in Radiologic- Pathologic Correlation Maffucci Syndrome EDITOR S NOTE RadioGraphics continues to publish radiologicpathologic case material selected from the American Institute for Radiologic Pathology (AIRP) best case presentations. The AIRP conducts a 4-week Radiologic Pathology Correlation Course, which is offered five times per year. On the penultimate day of the course, the best case presentation is held at the American Film Institute Silver Theater and Cultural Center in Silver Spring, Md. The AIRP faculty identifies the best cases, from each organ system, brought by the resident attendees. One or more of the best cases from each of the five courses are then solicited for publication in Radio- Graphics. These cases emphasize the importance of radiologic-pathologic correlation in the imaging evaluation and diagnosis of diseases encountered at the institute and its predecessor, the Armed Forces Institute of Pathology (AFIP). Kristopher L. Foreman, MD Mark J. Kransdorf, MD Mary I. O Connor, MD Murli Krishna, MD History A 43-year-old man presented to the Department of Orthopedic Surgery at the Mayo Clinic Florida with a 2-year history of left knee pain. The patient described the pain as an aching, squeezing, and throbbing pain that worsened when he stood or walked but improved when he sat. Indeed, sitting was noted to be the only position that provided the patient with symptomatic relief. The pain awakened him at night and was associated with a subjective feeling of progressive weakness in his leg. Multiple nonoperative measures failed to improve the patient s symptoms. The patient s past medical history was significant, with a diagnosis of Maffucci syndrome having been made when he was 1 year old. The patient had undergone numerous surgical procedures over the course of his lifetime. Most significantly, he had received a previous diagnosis of and treatment for malignant transformation of cartilaginous lesions involving the cervical spine and left elbow. RadioGraphics 2013; 33: Published online /rg Content Codes: 1 From the Departments of Diagnostic Radiology (K.L.F.), Orthopedic Surgery (M.I.O.), and Pathology (M.K.), Mayo Clinic Florida, Davis 2E Radiology, 4500 San Pablo Rd, Jacksonville, FL 32224; and Department of Diagnostic Radiology, Mayo Clinic Arizona, Scottsdale, Ariz (M.J.K.). Received July 5, 2012; revision requested July 31 and received January 2, 2013; accepted January 3. M.I.O. has disclosed financial relationships (see p 868); all remaining authors have no financial relationships to disclose. Address correspondence to K.L.F. ( foreman.kristopher@mayo.edu). RSNA, 2013
2 862 May-June 2013 radiographics.rsna.org Figure 1. Anteroposterior radiographs of the left femur (a) and lower leg (b) show marked deformity of the entire limb. The osseous deformity is most pronounced in the medial proximal femur, with marked expansile remodeling and an enchondroma protuberans like appearance. The mineralized matrix demonstrates the typical features of cartilage with prominent areas of arc and ring mineralization. Figure 2. Anteroposterior radiograph of the knee shows subtle, ill-defined osteolysis (*) in the femoral condyles. Imaging Findings The patient s imaging workup began with radiography of the left leg, which demonstrated marked deformity of the entire limb (Fig 1). The osseous deformity was most pronounced in the medial proximal femur, where marked expansile remodeling was noted. The deformity in the femur was less prominent distally, but it was still significant. Mineralized matrix demonstrating the typical features of cartilage was seen throughout the femur, with prominent areas of arc and ring mineralization (Fig 1). Although the entire bone demonstrated tumor involvement, the midshaft was relatively spared. The extensive osseous remodeling of the proximal femur resulted in an enchondroma protuberans like appearance (Fig 1). Although the cartilaginous tumor burden of the distal femur was less than that seen proximally, the femoral condyles demonstrated a subtle, ill-defined area of osteolysis (Fig 2), a finding that indicates a more aggressive tumor biologic behavior. This area corresponded to the area of the patient s clinical symptoms.
3 RG Volume 33 Number 3 Foreman et al 863 Figure 3. (a) Radiograph of the foot shows multiple small, rounded calcifications (arrow) representing phleboliths. (b) Clinical photograph shows a hemangioma on the dorsum of the foot (white arrow) and multiple superficial hemangiomas with the typical features of spindle cell hemangioma (black arrows), including multiplicity; dark blue-black color; a soft, raised, cerebriform contour; and a predominantly distal distribution. (c) Clinical photograph of the great toe more clearly depicts the features of spindle cell hemangioma. Virtually the entire visualized osseous skeleton showed involvement by cartilaginous tumors, a finding that is compatible with enchondromatosis. In addition, multiple soft-tissue masses containing small, rounded calcifications were present, findings that are indicative of phleboliths and associated hemangiomas and that confirmed the radiographic diagnosis of Maffucci syndrome. The soft-tissue changes were most apparent on the patient s foot and had the typical features of spindle cell hemangioma (Fig 3). Subsequent evaluation included computed tomography (CT) and magnetic resonance (MR) imaging of the left femur and knee. CT demonstrated the marked deformity and better defined the area of cortical destruction in the femoral condyles (Fig 4). CT also showed subtle, associated periosteal new bone formation laterally (Fig 4), a finding that was not readily seen at radiography. MR imaging of the left femur demonstrated the extensive replacement of normal marrow proximally by innumerable cartilaginous tumors, with individual lesions showing T1 hypointensity and T2 hyperintensity, findings that reflect the cartilaginous nature of the lesions (Fig 5). Corresponding areas of decreased signal intensity within the lesions representing the mineralized cartilage matrix were also noted. A large, heterogeneous,
4 864 May-June 2013 radiographics.rsna.org Figure 4. (a) CT image of the femur more clearly delineates subtle osteolysis (*) in the femoral condyles, as well as a small amount of periosteal new bone formation (white arrow) and cortical destruction with soft-tissue extension (black arrows), neither of which was appreciated at radiography. (b) Three-dimensional volume-rendered CT image more clearly depicts the osseous deformity. Figure 5. Corresponding T1-weighted (repetition time msec/echo time msec = 716/13) (a) and turbo T2-weighted (4300/76) (b) spin-echo MR images show the extensive replacement of normal marrow proximally by innumerable cartilaginous tumors, with individual lesions showing T1 hypointensity and T2 hyperintensity (arrows). Corresponding areas of decreased signal intensity represent the mineralized cartilage matrix. A large, heterogeneous, conglomerate cartilaginous mass is seen in the distal femur (*), with loss of the normal benign nodular architecture. Soft-tissue extension and cortical destruction (arrowheads) are again noted.
5 RG Volume 33 Number 3 Foreman et al 865 Figure 6. Contrast-enhanced fat-suppressed T1- weighted (741/13) spin-echo MR image shows lack of enhancement within the conglomerate mass (*), secondary to extensive myxoid change and necrosis, and more clearly depicts the enhancing soft-tissue component extending through the lateral cortex. Figure 7. (a) Photograph of the resected femur shows marked osseous deformity that corresponds to the findings at radiography (Fig 1a) and three-dimensional CT (Fig 4a). (b) Photograph of the bisected specimen shows extensive proximal tumor involvement by numerous benign, glistening cartilaginous nodules that range from a few millimeters to several centimeters in size. Note the difference in the gross appearance of the chondrosarcoma in the distal femur. (c) Radiograph of the bisected specimen also shows extensive tumor involvement, with subtle osteolysis in the distal femur corresponding to the chondrosarcoma noted in the gross specimen. conglomerate cartilaginous mass was seen in the distal femur, with loss of the normal benign nodular architecture of cartilage (Fig 5), as well as signal and enhancement characteristics suggestive of extensive myxoid change and necrosis. Contrast material enhanced imaging more clearly depicted the nonenhancing necrotic and myxoid change, as well as the enhancing soft-tissue component extending through the lateral cortex (Fig 6). Pathologic Evaluation At gross examination, the left femur was markedly distorted, demonstrating complete loss of the normal osseous architecture (Fig 7a). The bisected specimen showed extensive tumor involvement by numerous gray-blue nodules ranging from 5 mm
6 866 May-June 2013 radiographics.rsna.org Figure 8. (a) Photograph of the distal femoral specimen shows a benign cartilaginous nodule (black *), along with adjacent areas representing chondrosarcoma that have a variegated appearance, are gray to yellow in color, and have a gelatinous consistency (white *). (b) High-power photomicrograph (hematoxylineosin stain) of tissue from the gelatinous area shows focal hypercellularity compatible with a low-grade chondromyxoid neoplasm. to 2.7 cm in size (Fig 7b). The distal femoral specimen (Fig 8a) showed benign nodules of hyaline cartilage that were intimately associated with adjacent areas having a variegated appearance, gray to yellow coloration, and a gelatinous consistency. Microscopic examination of these areas showed focal hypercellularity within a chondromyxoid neoplasm (Fig 8b), a finding that was consistent with the diagnosis of a low-grade myxoid chondrosarcoma. Soft-tissue extension was noted in the lateral femoral condyle, a finding that was consistent with the findings at prior imaging studies. Discussion The syndrome of multiple enchondromas and hemangiomas that now bears his name was first described by Angelo Maffucci in 1881, in a report concerning a 40-year-old woman who had been hospitalized with a disease affecting both cartilage and blood vessels, resulting in more than 80 tumors of varying size, from a pea to a foetus head (1,2). The woman suffered from frequent hemorrhages as a result of the vascular tumors and died of complications following amputation of her left arm, probably from malignant transformation of a clavicular lesion (2,3). The term Maffucci syndrome first appeared in the medical literature in 1942, following a report by Carleton et al (3) in which the authors reported two new cases and reviewed the literature on the previously reported 18 cases. They chose the eponymous term Maffucci syndrome for this rare, congenital, nonhereditary disease entity, to recognize Maffucci s initial account of this condition (3 5). Maffucci documented all the essential features of this disease, including onset in childhood or adolescence, lack of a family history, development of multiple enchondromas leading to shortening and deformity of the extremities, formation of multiple associated hemangiomas, and malignant transformation of cartilaginous skeletal lesions (1). Although enchondromas and hemangiomas are the most frequently encountered benign tumors in Maffucci syndrome, patients can also develop lymphangiomas (6). Maffucci syndrome is extremely rare; in an analysis of 3000 primary bone tumors, Mirra (7) identified only two cases of Maffucci syndrome (0.07%), compared with 14 cases of Ollier disease (0.5%). Maffucci syndrome is usually diagnosed in the first decade of life, and often at birth (4). It affects all races and occurs with equal frequency in males and females (1). In one series, 25% of patients had clinical symptoms of Maffucci syndrome at birth, 45% had symptoms before age 6 years, and 78% had symptoms before puberty (1). Pathologically, Maffucci syndrome is classified as a mesodermal dysplasia, manifesting as a combination of enchondromatosis and hemangiomatosis (1). The cartilaginous tumors in Maffucci syndrome (and Ollier disease) are characterized by islands or columns of cartilage that are displaced from the growth plate, and that can amalgamate and become confluent (7,8). These lesions may normally demonstrate increased cellularity and decreased proteoglycans, suggesting low-grade malignancy to those unaware of the clinical history, and are considered dysplastic ;
7 RG Volume 33 Number 3 Foreman et al 867 hence, the term dyschondroplasia is often used to describe these lesions (7). The classic 1973 study by Lewis and Ketcham (1) provides a basis for the distribution of skeletal lesions. In their analysis of 98 cases, they found that the hand was most frequently involved (88%), followed by the foot (61%), lower leg (59%), femur (53%), humerus (42%), forearm (41%), pelvis (21%), and vertebrae (10%). Although each individual enchondroma is at limited risk for malignant transformation, the risk is much greater in patients with Maffucci syndrome, with the numerous cartilaginous tumors producing severe deformities and large conglomerate masses, as in our case (9). It is important to note that in patients with Maffucci syndrome, both the bone and soft-tissue lesions are at risk for malignant transformation (4). Although (as in our case) chondrosarcoma is the most frequently encountered malignant tumor in these patients, other tumors have also been described, including angiosarcoma and fibrosarcoma. In a series of 105 patients with Maffucci syndrome that focused on the number and type of neoplasms that occurred, there were 24 malignancies (23% of cases), including 16 chondrosarcomas, two gliomas, two mesenchymal ovarian tumors, and one case each of hemangiosarcoma, lymphangiosarcoma, pancreatic carcinoma, and fibrosarcoma (1). A recent multicenter study of 161 patients with enchondromatosis found that Ollier disease (n = 144 [89%]) was seen over eight times more frequently than Maffucci syndrome (n = 17 [11%]), with chondrosarcoma developing in 40% and 53% of affected patients, respectively (10). Whereas enchondromas are quite common, enchondromatosis is rare, with Maffucci syndrome and Ollier disease being the most common subtypes of the extraordinary group of lesions characterized by enchondromatosis (11). Other less well-known members of this group include metachondromatosis (enchondromatosis and osteochondroma-like lesions), spondyloenchondromatosis (enchondromatosis of the pelvis or long tubular bones associated with vertebral dysplasia), and cheirospondyloenchondromatosis (enchondromatosis with platyspondyly), as well as other less clearly delineated types (11). Most lesions, including Maffucci syndrome, are nonhereditary, and the genetic basis for the different forms of enchondromatosis is largely unknown (11). The MR imaging findings in our case accurately reflect the underlying disease. The tumor is composed of a coalescence of cartilaginous nodules that are no longer identifiable as individual structures, except at the periphery of the tumor. Centrally, the lesion demonstrates extensive myxoid change, with increased signal intensity on fluid-sensitive images (Fig 5). Myxoid change in a cartilaginous tumor may have a gelatinous gross appearance (Fig 8) and is strongly suggestive of malignancy (12). The radiographic features that suggest malignant transformation of solitary enchondromas of long bones have been well described and include (in descending order of frequency) soft-tissue extension, deep endosteal scalloping (greater than two-thirds of the cortical thickness), periosteal reaction, cortical destruction, pathologic fracture, extensive endosteal scalloping (more than twothirds the length of the lesion), cortical remodeling, and cortical thickening (13). The odds ratio favoring chondrosarcoma over enchondroma varies for each of these features, ranging from 78.5 for soft-tissue extension to 4.3 for cortical thickening (13). Although radiography is the appropriate initial imaging study for the assessment of patients with Maffucci syndrome, the skeletal deformities inherent in this disease make identification of these radiographic features challenging. The characteristic soft-tissue component of Maffucci syndrome is hemangioma. Classically, this was considered to be cavernous hemangioma; however, spindle cell hemangioma is now known to be the most common vascular tumor associated with Maffucci syndrome (14,15). Spindle cell hemangioma was initially described as a unique vascular tumor by Weiss and Enzinger (16) in 1986, an acral vascular lesion with combined Kaposi sarcoma like and cavernous hemangioma like features. Initially believed to be a tumor with limited metastatic potential and termed spindle cell hemangioendothelioma, it is now regarded as benign (14) and is termed spindle cell hemangioma by the World Health Organization (17). The lesion is frequently multifocal, affecting the subcutaneous tissues of the distal extremities (14). Our patient had innumerable soft, red-blue, acral spongy masses consistent with spindle cell hemangioma (Fig 3); however, these masses were not biopsied. The fact that spindle cell hemangioma has only recently been described, more than a century following Maffucci s original report, is likely the cause of the delayed recognition of the association between this distinctive vascular lesion and Maffucci syndrome (14). In addition to benign vascular tumors, hemangioendothelioma and angiosarcoma have also been described (14,15,18). The final diagnosis was Maffucci syndrome with malignant transformation of an enchondroma
8 868 May-June 2013 radiographics.rsna.org into a low-grade chondrosarcoma. The patient underwent a complete femoral resection and reconstruction with use of a left total femoral implant with a rotating hinge knee joint and bipolar hip articulation (Fig 9). The patient did well in the immediate postoperative period, with only minor wound-healing issues that subsequently resolved. Unfortunately, the patient developed left upper extremity pain during clinical follow-up, and results of subsequent imaging of the left arm were consistent with a chondrosarcoma of the left proximal humerus. To date, the patient has declined any further surgery. Disclosures of Conflicts of Interest. M.I.O.: Related financial activities: none. Other financial activities: consultant for Zimmer and Stryker. References 1. Lewis RJ, Ketcham AS. Maffucci s syndrome: functional and neoplastic significance case report and review of the literature. J Bone Joint Surg Am 1973; 55(7): Ciranni R. A forgotten Italian pathologist: Angelo Maffucci ( ) and his scientific thought. Virchows Arch 2006;449(4): Carleton A, Elkington JS, Greenfield JG, Robb- Smith AH. Maffucci s syndrome (dyschondroplasia with haemangeiomata). Q J Med 1942;11(4): Available at: /content/11/4/203.citation. 4. Resnick D, Kyriakos M, Greenway GD. Tumors and tumor-like lesions of bone: imaging and pathology of specific lesions. In: Resnick D, ed. Diagnosis of bone and joint disorders. 4th ed. Philadelphia, Pa: Saunders, 2002; Fanburg JC, Meis-Kindblom JM, Rosenberg AE. Multiple enchondromas associated with spindle-cell hemangioendotheliomas: an overlooked variant of Maffucci s syndrome. Am J Surg Pathol 1995;19(9): Kransdorf M, Murphey M. Imaging of soft tissue tumors. 2nd ed. Philadelphia, Pa: Lippincott Williams & Wilkins, 2006; Mirra JM. Intramedullary cartilage and chondroidproducing tumors. In: Mirra JM, ed. Bone tumors: clinical, radiologic, and pathologic correlations. Philadelphia, Pa: Lea & Febiger, 1989; Resnick D, McAlister W, Herman T. Osteochondrodysplasias, dysostoses, chromosomal aberrations, mucopolysaccharidoses, and mucolipidoses. In: Resnick D, ed. Diagnosis of bone and joint disorders. 4th ed. Philadelphia, Pa: Saunders, 2002; Rosenberg AE. Bones, joints, and soft tissue tumors. In: Kumar V, Abbas AK, Fausto N, Aster JC, eds. Robbins and Cotran pathologic basis of disease. 87th ed. Philadelphia, Pa: Saunders Elsevier, 2005; Figure 9. Postoperative anteroposterior radiograph obtained during follow-up evaluation of the femoral reconstruction shows a left total femoral implant with a rotating hinge knee joint and bipolar hip articulation. 10. Verdegaal SH, Bovée JV, Pansuriya TC, et al. Incidence, predictive factors, and prognosis of chondrosarcoma in patients with Ollier disease and Maffucci syndrome: an international multicenter study of 161 patients. Oncologist 2011;16(12): Pansuriya TC, Kroon HM, Bovée JV. Enchondromatosis: insights on the different subtypes. Int J Clin Exp Pathol 2010;3(6): Unni KK. Dahlin s bone tumors: general aspects and data in 11,087 cases. 5th ed. Philadelphia, Pa: Lippincott-Raven, 1996; Murphey MD, Flemming DJ, Boyea SR, Bojescul JA, Sweet DE, Temple HT. Enchondroma versus chondrosarcoma in the appendicular skeleton: differentiating features. RadioGraphics 1998;18(5): Weiss SW, Goldblum JR. Enzinger and Weiss s soft tissue tumors. 5th ed. Philadelphia, Pa: Mosby Elsevier, 2008; Fukunaga M, Suzuki K, Saegusa N, Folpe AL. Composite hemangioendothelioma: report of 5 cases including one with associated Maffucci syndrome. Am J Surg Pathol 2007;31(10): Weiss SW, Enzinger FM. Spindle cell hemangioendothelioma: a low-grade angiosarcoma resembling a cavernous hemangioma and Kaposi s sarcoma. Am J Surg Pathol 1986;10(8): Sangueza OP, Kasper RC, LeBoit P, et al. Vascular tumors. In: LeBoit PE, Burg G, Weedon D, Sarasin A, eds. World Health Organization classification of tumors: pathology and genetics skin tumors. Lyon, France: IARC, 2006; Yáñez S, Val-Bernal JF, Mira C, Echevarría MA, González-Vela MC, Arce F. Spindle cell hemangioendotheliomas associated with multiple skeletal enchondromas: a variant of Maffucci s syndrome. Gen Diagn Pathol 1998;143(5-6):
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