AJR 2003; 180:1681-1687
© American Roentgen Ray Society
Solid Variant of Aneurysmal Bone Cysts in Long Tubular Bones: Giant Cell Reparative Granuloma
Hakan Ilaslan1,2,
Murali Sundaram1 and
K. Krishnan Unni3
1 Department of Radiology, Mayo Clinic, Ch2-290, 200 First St., S.W., Rochester,
MN 55905.
2 Present address: Diagnostic Radiology, A21, The Cleveland Clinic Foundation,
9500 Euclid Ave., Cleveland, OH 44195.
3 Department of Laboratory Medicine and Pathology, Mayo Clinic, Rochester, MN
55905.
Received October 3, 2002;
accepted after revision November 11, 2002.
Address correspondence to M. Sundaram.
Abstract
OBJECTIVE. The purpose of this study was to determine the age
distribution, location, and imaging features of histologically proven solid
variants of aneurysmal bone cysts in long tubular bones.
MATERIALS AND METHODS. We performed a retrospective review of
imaging studies of histologically proven solid aneurysmal bone cysts in long
bones between 1961 and 2001. There were 30 cases comprising 29 radiographic,
six CT, and eight MR imaging examinations. The lesions were evaluated for bone
involved, location within a long bone, matrix, size, soft-tissue mass, and MR
imaging characteristics. The imaging findings were correlated with the
histologic findings.
RESULTS. The patients were 17 females and 13 males ranging in age
from 2 to 58 years (mean, 18 years). The bones involved were the femur
(n = 10), the ulna (n = 7), the tibia (n = 7), the
humerus (n = 2), the radius (n = 2), and the fibula
(n = 2). The lesions were five juxtaarticular, 13 metaphyseal, one
diametaphyseal, and 11 diaphyseal. The location was eccentric in 20 cases, of
which two were intracortical and two periosteal, and central in 10. Lesion
size varied between 1 and 7 cm. Thirty-three percent of lesions were
nonaneurysmal. Four lesions were mineralized. A soft-tissue mass was present
in four cases. Four lesions showed a permeative–lytic pattern simulating
a malignant process. Unusual findings included periosteal reaction and
development of a solid aneurysmal bone cyst in a preexisting fracture. MR
imaging showed solid elements in all cases and pronounced edema in 50% of
cases.
CONCLUSION. Solid aneurysmal bone cyst is a reactive nonneoplastic
bone lesion with varied imaging characteristics; one third of lesions are
nonaneurysmal.
Introduction
In 1983, Sanerkin et al. [1]
described a variant of aneurysmal bone cyst in which the predominant histology
was that of the solid material of a cystic aneurysmal bone cyst; those authors
used the term "solid variant of aneurysmal bone cyst"
(Fig. 1). Jaffe
[2] in 1953 and Lorenzo and
Dorfman [3] in 1980 described a
nonneoplastic hemorrhagic process in the jaw and the short tubular bones of
the hands and feet and termed the lesions "giant cell reparative
granuloma." In 1962, Ackerman and Spjut
[4] described two lesions in
the phalanges that they termed "giant cell reaction." The
histologic features of "solid" aneurysmal bone cysts and giant
cell reparative granulomas are similar, and the terms have been used
interchangeably in the pathology literature, where these entities have been
most frequently discussed [5,
6]. These lesions are
considered reactive and nonneoplastic, although they can lead to mistaken
diagnoses of malignancy [7]
(Figs. 1 and
2). Most musculoskeletal
radiologists are likely familiar with these lesions in the jaw and short
tubular bones of the hands and feet, but not in the long tubular bones because
of their relative rarity and scant discussion in the radiology literature. In
the English literature, we are aware of 31 patients with 32 lesions of solid
aneurysmal bone cysts in the long bones and only two case reports that discuss
MR imaging findings [6,
7,
8,
9,
10,
11,
12,
13,
14,
15,
16,
17]. The largest series in a
radiology journal of solid aneurysmal bone cysts in long tubular bones
comprises two patients [8]. We
found only one other study that examined this lesion when exclusively confined
to the long tubular bones [7].
We describe and discuss, on the basis of location and morphologic features,
the varied imaging findings in 30 histologically proven cases of solid
aneurysmal bone cysts, eight of which underwent MR imaging.
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Fig. 1. —30-year-old woman with expansive lesion in humerus.
Photomicrograph of surgical specimen shows solid aneurysmal bone cyst with
scattered giant cells in background of spindle cell proliferation
(straight arrow). Amorphous lacelike calcification typical of
conventional aneurysmal bone cyst is present in lower mid portion of
photomicrograph (curved arrow). (H and E)
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Fig. 2. —15-year-old boy with lesion in femur. Photomicrograph of
biopsy specimen shows loosely arranged spindle cells with spicules of bone and
prominent osteoblastic activity that should be recognized as reactive pattern
typical of solid aneurysmal bone cyst. This appearance (arrow),
however, may be mistaken for osteosarcoma. (H and E)
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Materials and Methods
After obtaining approval from our institutional review board, we
retrospectively reviewed the imaging studies from 1961 through 2001 of
histologically proven solid aneurysmal bone cysts in the long bones of the
extremities. Cases were identified from the pathology data bank. Those with
diagnoses of solid aneurysmal bone cyst or giant cell reparative granuloma in
long bones were chosen for study. Age at presentation and sex were obtained
from consultation letters and medical records. The study included 30 patients
with lesions in long bones whose imaging included 29 radiographic, six CT, and
eight MR imaging studies reviewed by two musculoskeletal radiologists in a
nonblinded fashion. The lesions were evaluated for bone involved, location
within a long bone, matrix, size, soft-tissue mass, cystic fluid, solid
elements, edema, and fluid levels. Histopathology of the cases was rereviewed
to confirm the diagnoses and was correlated with imaging.
Results
The patients were 17 females and 13 males ranging in age from 2 to 58 years
(mean, 18 years). A history of trauma was present in three cases. The bones
involved were the femur (n = 10), the ulna (n = 7), the
tibia (n = 7), the humerus (n = 2), the radius (n =
2), and the fibula (n = 2). Location within the bone was 13
metaphyseal, 11 diaphyseal, one diametaphyseal, and five juxtaarticular (end
of long bone). The juxtaarticular locations were the ulna (n = 2),
the tibia (n = l), and the radius (n = 2). The lesion
location was eccentric in 20 cases, of which two each were intracortical and
periosteal, and central in 10. Twenty cases (67%) were
"aneurysmal" in appearance, expanding the cortex. Ten cases (33%)
had no expansion of the cortex ("nonaneurysmal"). The size of the
lesions varied between 1 and 7 cm (average, 3.4 cm). A patient with
osteogenesis imperfecta had repeated fractures preceding the development of a
solid aneurysmal bone cyst at the site of fracture (Figs.
3A,
3B). Of the 20 expansive
lesions, 12 had a clearly identifiable peripheral shell
(Fig. 4), and four had a
soft-tissue mass with no outer shell of bone
(Fig. 5). Five lesions were at
the end of a long bone (Fig.
6), one of which was nonexpansive (not illustrated). Of the
remaining nine nonexpansive lesions, five were in cancellous bone. Two of
these had a benign appearance (Fig.
7A) and showed considerable edema on MR imaging
(Fig. 7B). Three of the
nonexpansive lesions in cancellous bone ap peared to be morphologically
aggressive with or without a periosteal reaction
(Fig. 8A). One of these
lesions also showed considerable edema
(Fig. 8B) around the lesion
that extended well away from the lesion
(Fig. 8C). Two of the
nonexpansive lesions were intracortical
(Fig. 9) and two were
periosteal (Fig. 10).
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Fig. 3B. —2-year-old girl with osteogenesis imperfecta. Radiograph
obtained 6 years later shows development of solid aneurysmal bone cyst at site
of radius fracture with healing of ulnar fracture. Expansive mineralized
lesion with solid rim erodes into ulnar shaft.
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Fig. 4. —Lateral radiograph of ankle in 13-year-old girl shows
unmineralized, well-marginated, expansive, eccentrically located osteolytic
lesion in distal tibia with narrow zone of transition and uninterrupted
peripheral shell (arrow).
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Fig. 7B. —24-year-old woman with solid aneurysmal bone cyst. Unenhanced
coronal fast spin-echo fat-suppressed MR image (TR/TE, 5035/30) shows solid
lesion with few cystic foci and considerable edema surrounding lesion.
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The typical MR imaging appearance was of a lesion slightly hyperintense to
muscle on T1-weighted sequences and having a heterogeneous, predominantly high
signal intensity with scattered areas of low signal intensity on T2-weighted
sequences. In one patient, the lesion was hypointense to muscle on T1-weighted
images. All lesions appeared solid, with two showing solid and cystic areas
and fluid–fluid levels (Fig.
11A). Edema in the adjacent bone and soft tissues adjacent to the
lesion was a common feature that was seen in 50% of cases (Figs.
7B,
8B,
8C, and
12A). In the sole patient in
whom gadolinium was used, the lesion showed marked enhancement with a
heterogeneous appearance (not shown).
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Fig. 11A. —11-year-old girl with solid anuerysmal bone cyst. Unenhanced
sagittal MR image (TR/TE, 2265/90) shows solid (curved arrow) and
cystic (open arrow) components in distal tibial lesion that crosses
growth plate into epiphysis (straight arrow).
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Fig. 12A. —11-year-old boy with solid aneurysmal bone cyst. Unenhanced
sagittal MR image (TR/TE, 2800/23) of distal leg shows extensive bone and
soft-tissue edema surrounding small intracortical tibial lesion.
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Four lesions showed a partially mineralized matrix on radiography or CT
(Fig. 10). All others were
entirely osteolytic (Figs. 4,
5,
7A,
8A,
11B, and
12B). MR imaging and CT showed
soft-tissue masses in four cases. An unusual finding was a periosteal reaction
in three lesions, two of which are shown (Figs.
8A and
12B). Pathologic fracture was
uncommon, seen in only one case.
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Fig. 12B. —11-year-old boy with solid aneurysmal bone cyst. CT scan
shows fibular periosteal reaction that presumably results from surrounding
inflammatory response or previous trauma. Tibial lesion is associated with
solid periosteal reaction.
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Discussion
Giant cell reparative granuloma and the solid variant of aneurysmal bone
cysts have primarily been seen in the craniofacial and small tubular bones of
the hands and feet [1,
2,
3,
4,
5,
6]. These lesions, considered
reactive and nonneoplastic (Figs.
1,
2,
3A,
3B), have been of problematic
interest to pathologists and treating surgeons because they can be mistaken
for giant cell tumors, brown tumors of hyperparathyroidism, and osteosarcoma,
usually the fibroblastic or low-grade subtypes
[7,
18]
(Fig. 2). Over the past 20
years, the English literature has reported 32 lesions of solid aneurysmal bone
cysts in long bones described in 31 patients; this number is probably an
underestimation because of the lack of wide recognition and underreporting. We
discuss our findings in 30 patients.
In our series, the patients' age range was 3–58 years (average, 18
years) (Fig. 13) with a slight
female predominance (male:female, 1:1.4). The most commonly involved bone was
the femur (33%), followed by an equal number of cases in the ulna and tibia
(23%). The lower extremity (n = 19) was involved twice as frequently
as the upper (n = 11). The predilection for the lower extremity and
the femur in particular is in keeping with findings from the compilation of
previous reports [6,
7,
8,
9,
10,
11,
12,
13,
14,
15,
16,
17]. However, there have been
only four previous case descriptions of solid aneurysmal bone cysts in the
upper extremity and one textbook illustration
[6,
9,
12,
15,
18]. All previously described
lesions have been eccentric in location and expansive, with variable
aggressive features, as was our most common pattern (Figs.
4,
5, and
11B); to our knowledge, no
previous descriptions of juxtaarticular, nonexpansive, or intracortical
lesions have been reported (Figs.
6,
7A,
7B,
8A,
8B,
8C,
9). Two previously described
cases were seen in a subperiosteal location
[6,
13]
(Fig. 10). Mineral was
identified in 40% of lesions in the Rizzoli Institute series
[7], compared with 14% in our
study group (Fig. 10). We had
no case of bilateral involvement
[14] or of a secondary solid
aneurysmal bone cyst developing in a preexisting lesion
[6,
17]. Pathologic fractures and
periosteal reactions were uncommon (Figs.
8A and
12B). We had only one example
of this reactive nonneoplastic lesion arising at the site of a previous
fracture (Figs. 3A,
3B) and have not encountered
such an example in the English literature. The sequence of events illustrated
in this patient is consistent with the prevailing view that solid aneurysmal
bone cyst is a reactive nonneoplastic lesion.
On MR imaging, most lesions (7/8) were slightly hyperintense to muscle on
T1-weighted images and were heterogeneous, with predominantly high signal
intensity with scattered areas of low signal intensity on T2-weighted
sequences. Areas of low signal on T2-weighted images are consistent with
mineral in the lesion. Perhaps the most interesting and significant finding
was the presence in all MR images of a solid lesion, of which two showed
admixed cystic areas and fluid–fluid levels
(Fig. 11A). Pronounced edema
in the bone and soft tissues adjacent to the lesion was seen in four (50%) of
eight MR examinations (Figs.
7B,
8B,
8C, and
12A). On MR imaging, profound
osseous edema has been associated with osteoid osteoma, osteoblastoma,
chondroblastoma, and eosinophilic granuloma
[19]. The cause for edema in
bone or soft tissues in solid aneurysmal bone cysts or several of the other
benign lesions is unclear. It has been suggested that in osteoid osteomas and
chondroblastomas, prostaglandins and COX-2 ([cyclooxygenase-2] an isozyme of
COX that is necessary for prostaglandin synthesis) are responsible for
clinical and imaging inflammatory response
[20,
21,
22].
Solid aneurysmal bone cyst has a broader and more variable radiographic
appearance than previously described. Perhaps our most surprising finding was
that one third of the lesions were nonaneurysmal on imaging. No location in a
long bone was exempt. The metaphyseal and diaphyseal portions of the long bone
were the favored locations, but lesions were also found at the end of the long
bone, in the cortex, and on the surface. Thirty-three percent of lesions were
found in the upper extremity. On MR imaging, profound edema was a feature of
the smaller lesions; and on the limited MR imaging studies available of the
larger lesions, solid and cystic elements could be identified with or without
fluid levels.
Radiographically expansive, eccentric lesions with or without a shell are
indistinguishable from conventional aneurysmal bone cysts (Figs.
4,
5, and
11B) and, rarely,
telangiectatic osteosarcoma. Histologically, however, solid aneurysmal bone
cysts tend to be mistaken for fibroblastic or, more commonly, low-grade
osteosarcoma [7,
18] and not for telangiectatic
osteosarcoma. Hence, the imaging differential diagnosis with this pattern of
presentation is histologically easily resolved. If MR imaging is performed and
solid and cystic elements are identified in an expansive osteolytic lesion
(Fig. 11A), the diagnosis of
solid aneurysmal bone cyst may be considered. Although we did not encounter
any cases of secondary solid aneurysmal bone cysts in preexisting lesions,
their occurrence has been reported. In such instances, MR imaging alone is
unlikely to distinguish a secondary solid aneurysmal bone cyst from a de novo
solid aneurysmal bone cyst. The radiograph should permit detection of a
preexisting lesion such as fibrous dysplasia, neurofibroma, or enchondroma,
which are the only lesions (to our knowledge) thus far described with solid
aneurysmal bone cysts in long bones
[6,
10,
17].
Tumors or tumorlike lesions found at the end of long bones have a limited
differential diagnosis that, depending on patient age and whether the lesion
reaches the joint surface, often includes giant cell tumor or chondroblastoma.
The solid aneurysmal bone cysts found in this location (16%) resembled giant
cell tumors and chondroblastomas. However, two of the five juxtaarticular
lesions arose in the ulna, a rare site for a giant cell tumor
[23]
(Fig. 6). Nevertheless, it
would be unreasonable to proffer a diagnosis of solid aneurysmal bone cyst
over giant cell tumor or chondroblastoma in these cases. Pathologists must be
aware that a giant cell reparative granuloma or a solid aneurysmal bone cyst
may arise in locations associated with giant cell tumors; if the microscopic
features favor giant cell reparative granuloma, such a diagnosis should be
rendered despite the location being favored by giant cell tumor.
In terms of treatment, both lesions are treated by curettage, with more
aggressive curettage reserved for giant cell tumor. The appearance and
location of the lesions in this group, which were all intracompartmental, are
unlike those of an osteosarcoma. Conversely, all solid aneurysmal bone cysts
not found at the end of a long bone will not be confused with giant cell
tumors by radiologists, and correlation with radiographs will prevent a
histologic interpretive error.
The diagnosis of solid aneurysmal bone cyst is virtually impossible to
consider in nonexpansive (nonaneurysmal) cases and in those lesions arising in
the cortex and periosteum (Figs.
7A,
7B,
8A,
8B,
8C,
9 and
11A,
11B). However, such lesions
would not support a histologic diagnosis of low-grade osteosarcoma, which is
most commonly mimicked by a fibrous dysplasialike radiographic pattern and has
a soft-tissue mass or cortical destruction
[24,
25]. The intracortical and
subperiosteal locations are interesting but nonspecific and add to the growing
list of tumor and tumorlike lesions that may arise from these uncommon sites.
However, if the lesion is aneurysmal and shows solid internal consistency on
MR imaging, a solid aneurysmal bone cyst should be distinguished from a
conventional aneurysmal bone cyst. A recent illustration of a periosteal solid
aneurysmal bone cyst shows the solid internal composition on an MR image
[6].
Radiologists need to be aware that the reactive, nonneoplastic lesion of a
solid aneurysmal bone cyst may contain mineral and is an appearance entirely
consistent with that microscopic diagnosis (Figs.
2 and
10); more than one third of
lesions designated as solid aneurysmal bone cyst are nonaneurysmal (Figs.
7A,
7B,
8A,
8B,
8C,
9 and
11A,
11B).
Finally, we have no strong view as to whether "solid aneurysmal bone
cyst" or "giant cell reparative granuloma" should be the
preferred term. The incongruity of describing a lesion as a "solid
cyst" was acknowledged, but the term has been retained by the authors
who introduced it and also by other pathologists because it aptly describes
the microcopic appearance [1].
MR images may show the solid and cystic components of this lesion, which are
helpful in considering the diagnosis of solid aneurysmal bone cyst. The
contradiction, from an imaging standpoint, is the appellation
"aneurysmal" to one third of lesions that are nonexpansive.
"Giant cell reparative granuloma" is also an inexact term, because
granulomas are never seen in this lesion.
Regardless of the favored term, radiologists must be familiar with the wide
range of imaging features and the microscopic difficulties that may be
encountered in separating solid aneurysmal bone cysts from giant cell tumors
and subtypes of osteosarcoma.
Acknowledgments
We gratefully acknowledge the secretarial support of Linda Greene in the
preparation of this manuscript.
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Abstract
Introduction
