Fibrous dysplasia (FD) is an uncommon bone disease that
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1 Resident Short Review Fibrous Dysplasia Nicole D. Riddle, MD; Marilyn M. Bui, MD, PhD Fibrous dysplasia is an uncommon bone disease. The diagnosis is usually not difficult, given the symptoms, radiology, and histology. The gene involved is the a subunit of the G-protein receptor. Recent innovation in molecular pathology has helped us understand the mechanism of disease pathogenesis. The treatment of fibrous dysplasia is limited to maintenance of maximum bone density. Surgical Fibrous dysplasia (FD) is an uncommon bone disease that has a rare but clear potential for malignant transformation. The diagnosis is usually not difficult given the symptoms, radiology, and histology. The histologic picture is classically of low to moderately cellular fibrous stroma surrounding irregularly shaped bone trabeculae without osteoblastic rimming, which matches the benign appearance on radiology. The gene involved in pathologenesis is the a subunit of G-protein receptors, found on chromosome 20. Recent innovation in molecular pathology has helped us understand the mechanism of the disease, pertaining to camp and WNT/b-catenin. The treatment of FD is limited to maintenance of maximum bone density via diet, exercise, and therapeutic medications, with many patients also choosing to avoid substances that lower bone density, such as caffeine and nicotine. Oftentimes, surgical reinforcement is needed for bowing deformities and fractures when they occur. Currently, there is no therapy for preventing disease advancement or for malignant transformation. CLINICAL AND RADIOLOGIC PRESENTATION Fibrous dysplasia is a benign fibro-osseous lesion, which may present in either monostotic or polyostotic forms. 1,2 The monostotic form occurs most frequently and represents approximately 75% of FD cases. This form occurs, in decreasing order of frequency, in the craniofacial bones, ribs, femurs, tibias, and humeri. The monostotic form of FD may present with pain or a pathologic fracture, usually in patients aged 10 to 30 years. The degree of bone deformity is relatively less severe compared with that of the polyostotic Accepted for publication April 27, From the Department of Pathology and Laboratory Medicine, Pennsylvania Hospital, Philadelphia (Dr Riddle); and the Department of Anatomic Pathology, Moffitt Cancer Center Hospital, Tampa, Florida (Dr Bui). The authors have no relevant financial interest in the products or companies described in this article. Reprints: Nicole D. Riddle, MD, Department of Pathology and Laboratory Medicine, Pennsylvania Hospital, 800 Spruce St, Preston Bldg, 6th Floor, Philadelphia, PA ( nriddlemd@gmail. com). reinforcement is used to treat bowing deformities and fractures as they occur. Malignant transformation of fibrous dysplasia is rare. Currently, there is no therapy for preventing the disease from advancing or for malignant transformation. (Arch Pathol Lab Med. 2013;137: ; doi: arpa/ RS) type. No clearly documented evidence supports the conversion from the monostotic form to the polyostotic form. 1,3 Approximately 20% to 30% of FD cases are the polyostotic form. The common sites of involvement for the polyostotic form are, in decreasing order of frequency, the femur, tibia, skull and facial bones, pelvis, rib, humerus, radius and ulna, lumbar spine, clavicle, and cervical spine. The lesions may be unilateral or, less commonly, bilateral. Approximately 60% of patients with the polyostotic form of FD are symptomatic before age 10 years. The initial symptoms are usually pain in the involved limb or limbs, associated with a limp if the lower extremity is involved, and spontaneous fracture. Occasionally, the lesion is found after skeletal survey for a high-alkaline phosphatase test when results of liver function tests are within reference range. Leg-length discrepancies of varying degrees occur in about 70% of patients with limb involvement because of the weakened structural integrity of the bone leading to significant bowing. 1,2 Radiographically, the healthy bone is replaced with a more radiolucent, ground-glass appearing pattern, with no visible trabecular pattern. There may be endosteal scalloping of the inner cortex, but the periosteal surface is smooth and nonreactive. Fibrous dysplasia is often associated with a shepherd s crook deformity and may result in pathologic fracture (Figure 1, a). This curvature of the femoral neck and proximal shaft often causes a coxa vara deformity of the knee, which can be severe (Figure 1, b). Although the radiographic features can vary widely, this classic radiologic picture is pathognomonic of FD. Birth control pills have been associated with disease progression in some patients, suggesting an important role for estrogen in the disease process. Of note, pregnancy can also reactivate dormant lesions, more commonly with the polyostotic form than with the monostotic form. A small subset of the cases with the polyostotic form (~3%) occurs along with endocrine abnormalities and coast of Maine café-au-lait spots, a triad called McCune-Albright syndrome (MAS). The syndrome was named for 2 physicians, Donovan McCune and Fuller Albright, who separately described the triad in 1937; symptoms matching the description can be found in cases years earlier. 4,5 The most common endocrine abnormality is precocious puberty. 134 Arch Pathol Lab Med Vol 137, January 2013 Fibrous Dysplasia Riddle & Bui
2 This was once treated by removal of the active gonad and is now treated with antihormonal medications. The bony lesions, involved gonads, and café-au-lait spots are typically all on the same side of the body. Patients may have only 2 of the 3 characteristics, sometimes lacking the café-au-lait spots, and may have one or more of the numerous endocrine symptoms. The list of possible endocrine disturbances includes hyperthyroidism, adrenal disorders, diabetes, hyperpituitarism, and hypercalcemia. 6 8 A separate disorder, affecting approximately 1% of patients with FD, is Mazabraud syndrome. Those afflicted with Mazabraud syndrome have intramuscular myxomas associated with the bony lesion. 2 Both of these disorders are more common in women. 9 PATHOGENESIS, HISTOPATHOLOGY, AND ANCILLARY STUDIES The latest molecular findings in FD, and especially those for MAS, suggest it is caused by a somatic mutation early in embryonic life that causes a gene mosaicism. The earlier the mutation occurs, the more widespread the effects will be. The gene is located on band 20q13, an area that codes for the a subunit on G-protein receptors. 1,10 16 This mutation is also present in various endocrine tumors as well as FD. The G-proteins begin a cascade that ultimately leads to activation of the enzyme adenylyl cyclase that produces camp. In MAS, there is a missense mutation that causes the substitution of arginine in position 201 of the Gs-a gene Normally, there is an almost immediate deactivation of adenylyl cyclase and a break down of the camp. In MAS, that does not occur. Overproduction of camp leads to increased amounts of activity that affect each tissue differently based on its designated function. Café-au-lait spots are from overproduction of the enzyme tyrosinase, which is the rate-limiting step in melanin production. In FD, this mutation causes hyperproliferation and incomplete differentiation of marrow stromal cells to abnormal osteoblasts. camp also activates Fos, which inhibits osteoblasticspecific genes as well as stimulating cytokines that promote bone resorption by osteoclasts. Hypophosphatemia/phosphaturia, sometimes found in FD and MAS, is caused by excess secretion of a phosphatonin fibroblast growth factor. Similarly, most of the endocrine problems associated with MAS can be related to Gs-a activation. 11 In addition, activating Gs-a mutations have been shown to potentiate WNT/b-catenin signaling, and removal of Gs-a leads to reduced WNT/b-catenin signaling and decreased bone formation (Figure 2). Activation of WNT/b-catenin signaling in osteoblast progenitors causes an FD-like phenotype and reduction of b-catenin levels rescued differentiation defects of stromal cells derived from patients with FD. This suggests that activated G proteins have significant roles during both skeletal development and disease by modulating the WNT/ b-catenin signaling strength. 17 Fibrous dysplasia is generally a well-circumscribed, tangrey mass that is dense and variably fibrous with a gritty Figure 1. Radiograph showing ground-glass appearance with cortical scalloping and the classic shepherd crook deformity of the right proximal femur. Note the pathologic fracture through the left greater trochanter (a) as well as curvature of the shaft resulting in coxa vera abnormality of the knee (b). Arch Pathol Lab Med Vol 137, January 2013 Fibrous Dysplasia Riddle & Bui 135
3 Figure 2. The WNT pathway has a regulatory role in normal bone formation. This pathway is affected by the integrity of Gs-a. Inactivating Gs-a mutations lead to decreased activity of WNT and bone loss. Activating Gs-a mutations lead to increased potentiation of WNT leading to a fibrous dysplasia type appearance. This has recently been shown to act in conjunction with camp/fos in fibrous dysplasia (FD) and McCune-Albright syndrome (MAS). quality due to the presence of bone trabeculae, although it is often curetted and not removed en masse. There may be prominent cyst formation, especially in older lesions. A glassier, blue-tinged appearance may be found in cases with chondroid metaplasia. Fibrous dysplasia has a classic histology of low to moderately cellular fibrous stroma surrounding irregular, curvilinear trabeculae of woven bone, which is arranged in a pattern commonly referred to as resembling Chinese characters (Figure 3). The stroma may be variably collagenized, and the ratio of fibrous tissue to bone can range from being totally fibrous to being densely packed with dysplastic trabeculae. The trabeculae may even contain transverse lines mimicking the Paget disease. A key feature is the conspicuous absence of osteoblastic rimming (Figure 4). Secondary changes, such as a metaplastic chondroid component or aneurismal bone cystlike changes, can include cystic degeneration with xanthomatous histiocytes and/or giant cells and myxoid change (Figures 5 through 7). These findings may make the diagnosis challenging; however, the overall features are bland and lack cytologic atypia, and usually, a classicappearing area is present for accurate diagnosis. Immunohistochemistry serves no purpose in the diagnosis of FD other than to rule out the possibility of a malignant lesion with a pertinent history. Human epidermal growth factor receptor 2, epidermal growth factor receptor, and CD117 are not expressed in FD by immunohistochemical studies. 18 The recurrent cytogenetic changes of FD are structural rearrangements involving 12p13 and trisomy 2 in a small number of case reports. 2 In addition, there are inconsistent chromosomal findings in FD, and the significance of that is unclear. 19 DIFFERENTIAL DIAGNOSIS The differential diagnosis of FD on radiograph varies based on location but includes nonossifying fibroma, osteofibrous dysplasia, aneurysmal bone cyst, adamantinoma, giant cell tumor, and low-grade central osteosarcoma. The histology is usually characteristic. However, it may be challenging for small biopsies or during intraoperative pathologic consultation. The histologic differential diagnosis is similar to the radiographic differential diagnosis, including osteofibrous dysplasia, fracture callus, nonossifying Figure 3. Hematoxylin-eosin stain showing the characteristic Chinese character architecture of trabeculae (original magnification 3100). Figure 4. Dense, fibrous stroma with atypical trabeculae and no osteoblastic rimming (hematoxylin-eosin, original magnification 350). 136 Arch Pathol Lab Med Vol 137, January 2013 Fibrous Dysplasia Riddle & Bui
4 fibroma, and low-grade osteosarcoma. Low-grade chondrosarcoma may be part of the differential diagnosis if there is a prominent chondroid component. Osteofibrous dysplasia and fracture callus can be difficult to differentiate, but the history and location should help, and they typically have prominent osteoblastic rimming around the bone trabeculae. Fracture callus should have a history of trauma, and osteofibrous dysplasia occurs almost exclusively in the tibia and fibula. Nonossifying fibroma resembles benign fibrous histiocytoma with a storiform arrangement of the spindle cells and occasional multinucleated giant cells. However, bone-matrix formation is absent. These cases can be hard to differentiate from FD clinically, radiologically, and histologically because some cases of FD have little bone trabeculae, or such trabeculae may not be present on a small biopsy specimen. Particularly when the mandible is involved, ossifying fibroma must be considered in the differential diagnosis. The cells in FD are generally bland; thus, it is rare that FD is confused with malignancy on either radiology or histology. However, there is always a chance that a lowgrade osteosarcoma or chondrosarcoma has been caught early enough that it does not yet have the typical aggressive features. As such, cases of FD must be examined carefully for evidence of malignant osteoid/cartilage, areas with increased cellularity, and atypical nuclei. TREATMENT The treatment of fibrous dysplasia is limited to maintenance of maximum bone density via diet, exercise, and therapeutic medications, such as bisphosphonates and parathyroid hormone analogues. The side effects of bisphosphonates include fever and reflux, and with longterm use, significant osteonecrosis with associated fractures may occur. In severe cases, surgical reinforcement of bowing deformities may be performed. In addition, internal or external fixation of fractures may be done as they occur. The orthopedic surgeon may use bone grafts in these cases, and cortical allografts are preferred because they are absorbed slower than autografts or cancellous allografts. Leg-length discrepancies are often treated with shoe lifts because the mechanism for externally lengthening bones is often not viable in weakened FD bones. Figure 5. Dense, fibrous stroma typical for fibrous dysplasia with adjacent cartilaginous metaplasia (hematoxylin-eosin, original magnification 350). Photo courtesy of Carrie Inwards, MD. Figure 6. Significant xanthomatous changes in a case of fibrous dysplasia (hematoxylin-eosin, original magnification 350). Photo courtesy of Carrie Inwards, MD. Figure 7. Diffuse, myxoid stromal changes (hematoxylin-eosin, original magnification 350). Photo courtesy of Carrie Inwards, MD. PROGNOSIS Fibrous dysplasia is generally considered a benign, pediatric disease, which usually becomes dormant by adulthood. However, patients with FD should be made aware of the real potential for malignant transformation (1%) The frequency of malignant change is increased with the polyostotic form of FD, especially in patients with MAS (~4%), Mazabraud syndrome, or prior radiation exposure Identifying malignant transformation in FD may be difficult because of the nature of the benign disorder (the pain, fractures, and radiologic findings). Rapidly increasing pain without apparent trauma or a significant rapid change in radiologic appearance, especially in mineralization, should alert the clinician to further investigate Computed tomography scans can be helpful in recognizing malignancy as well as in determining their extent. In the monostotic form of FD, the skull and facial bones are most common sites to develop malignancy. In the polyostotic form, the common sites are the facial bones, femur, and tibia. However, any area affected by FD may develop malignancy. The most common malignancy in- Arch Pathol Lab Med Vol 137, January 2013 Fibrous Dysplasia Riddle & Bui 137
5 cludes osteosarcoma (~70%), with fibrosarcoma (~20%), chondrosarcoma (~10%), and malignant fibrous histiocytoma (~4%) occurring less frequently. 22,25 28 If the malignancy is identified at an advanced stage, it does not respond to conventional chemotherapy. However, with early diagnosis, the prognosis of secondary sarcoma is comparable to that of de novo cases. 29 Once FD is diagnosed, routine follow-up should be done on a yearly basis with x-ray examination. In addition, the patient should know to bring any changes in symptomology (increased pain, weakness, deformity) to the attention of their physician. At the present time, there is no long-term, clinical follow-up of a large series of cases, to our knowledge, in the literature. However, such study would be helpful because many cases do not burn out in adulthood but, rather, are reactivated. CONCLUSION Fibrous dysplasia is a benign disease of bone with rare potential for malignant transformation. Typically thought of as having a good prognosis, there is a wide range of severity in patients, with some being minimally affected, whereas others have significant deformities and numerous fractures. Recent and ongoing research has given us a better understanding of the pathogenesis of fibrous dysplasia with the advancement in molecular pathology. Fibrous dysplasia is caused by a gene mutation on chromosome 20, affecting the region of Gs-a subunit, and leading to an overproduction of camp. In addition, studies have shown involvement of the WNT/ b-catenin signaling pathway. Presently, treatment is limited, and it is possible that, with further understanding of the pathogenesis, we can better manage these patients. References 1. DiCaprio MR, Enneking WF. Fibrous dysplasia: pathophysiology, evaluation, and treatment. J Bone Joint Surg Am. 2005;87(8): Fletcher CDM, Unni KK, Mertens F, eds. Pathology and Genetics of Tumours of Soft Tissue and Bone. Lyon, France: IARC Press; World Health Organization Classification of Tumours; vol Horvai A, Unni KK. Premalignant conditions of bone. J Orthop Sci. 2006; 11(4): Albright F, Butter AM, Smith P. Syndrome characterized by posterities fibrosa disseminate, areas of pigmentation and endocrine dysfunction, with precocious puberty in females: report of five cases. N Engl J Med. 1937;216(17): McCune DJ, Bruch H. Osteodystrophia fibrosa: report of a case in which the condition was combined with precocious puberty, pathologic pigmentation of the skin and hyperthyroidism, a review of the literature. Am J Dis Child. 1937; 54(4): Zacharin M. The spectrum of McCune Albright syndrome. Pediatr Endocrinol Rev. 2007;4(suppl 4): Chanson P, Salenave S, Orcel P. McCune-Albright syndrome in adulthood. Pediatr Endocrinol Rev. 2007;4(suppl 4): Daneman A, Daneman D. McCune-Albright syndrome. J Pediatr Endocrinol Metab. 2007;20(12): Zoccali C, Teori G, Prencipe U, Erba F. Mazabraud s syndrome: a new case and review of the literature. Int Orthop. 2009;33(3): de Sanctis L, Delmastro L, Russo MC, Matarazzo P, Lala R, de Sanctis C. Genetics of McCune-Albright syndrome. J Pediatr Endocrinol Metab. 2006; 19(suppl 2): Diaz A, Danon M, Crawford J. McCune-Albright syndrome and disorders due to activating mutations of GNAS1. J Pediatr Endocrinol Metab. 2007;20(8): Lietman SA, Schwindinger WF, Levine MA. Genetic and molecular aspects of McCune-Albright syndrome. Pediatr Endocrinol Rev. 2007;4(suppl 4): Sargin H, Gozu H, Bircan R, et al. A case of McCune-Albright syndrome associated with Gs alpha mutation in the bone tissue. Endocr J. 2006;53(1): Imanaka M, Iida K, Nishizawa H, et al. McCune-Albright syndrome with acromegaly and fibrous dysplasia associated with the GNAS gene mutation identified by sensitive PNA-clamping method. Intern Med. 2007;46(18): Pollandt K, Engels C, Kaiser E, Werner M, Delling G. Gs-alpha gene mutations in monostotic fibrous dysplasia of bone and fibrous dysplasia-like lowgrade central osteosarcoma. Virchows Arch. 2001;439(2): Riminucci M, Robey PG, Bianco P. The pathology of fibrous dysplasia and the McCune-Albright syndrome. Pediatr Endocrinol Rev. 2007;4(suppl 4): Regard JB, Cherman N, Palmer D, et al. WNT/b-catenin signaling is differentially regulated by Ga proteins and contributes to fibrous dysplasia. Proc Natl Acad Sci U S A. 2011;108(50): DeMers NM, Schlauder SM, Bui MM. Immunostain patterns of HER-2, EGFR and CD117 in fibrous dysplasia: a six-case series and literature review. J Orthop. 2009;6(2):e Dal Cin P, Sciot R, Speleman F, et al. Chromosome aberrations in fibrous dysplasia. Cancer Genet Cytogenet. 1994;77(2): Ruggieri P, Sim FH, Bond JR, Unni KK. Malignancies in fibrous dysplasia. Cancer. 1994;73(5): De Iure F, Campanacci L. Clinical and radiographic progression of fibrous dysplasia: cystic change or sarcoma?: description of a clinical case and review of the literature. Chir Organi Mov. 1995;80(1): Doganavsargil B, Argin M, Kececi B, Sezak M, Sanli UA, Oztop F. Secondary osteosarcoma arising in fibrous dysplasia, case report. Arch Orthop Trauma Surg. 2009;129(4): Hansen MR, Moffat JC. Osteosarcoma of the skull base after radiation therapy in a patient with McCune-Albright syndrome: case report. Skull Base. 2003;13(2): Healey JH, Buss D. Radiation and pagetic osteogenic sarcomas. Clin Orthop Relat Res. 1991;(270): Jhala DN, Eltoum I, Carroll AJ, et al. Osteosarcoma in a patient with McCune-Albright syndrome and Mazabraud s syndrome: a case report emphasizing the cytological and cytogenetic findings. Hum Pathol. 2003;34(12): DeMers Riddle NM, Yamauchi H, Caracciolo JT, et al. Chondrosarcoma arising in fibrous dysplasia: a case report and review of the current literature. Pathol Lab Med Int. 2009;1: Hoshi M, Matsumoto S, Manabe J, et al. Malignant change secondary to fibrous dysplasia. Int J Clin Oncol. 2006;11(3): Unni KK, Inwards C, Bridge JA, Kindblom L, Wold LE, eds. Tumors of the Bones and Joints. Silver Spring, MD: Armed Registry of Pathology, and Washington, DC: Armed Forces Institute of Pathology; Atlas of Tumor Pathology; 4th series, fascicle Bielack SS, Kempf-Bielack B, Heise U, Schwenzer D, Winkler K; Cooperative German-Austrian-Swiss Osteosarcoma Study Group. Combined modality treatment for osteosarcoma occurring as a second malignant disease. J Clin Oncol 1999;17(4): Arch Pathol Lab Med Vol 137, January 2013 Fibrous Dysplasia Riddle & Bui
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