DOI:10.2214/AJR.05.0654
AJR 2006; 186:967-976
© American Roentgen Ray Society
Staging of Bone Tumors: A Review with Illustrative Examples
Gregory S. Stacy1,
Ravinder S. Mahal1,2 and
Terrance D. Peabody3
1 Department of Radiology, University of Chicago, 5841 S Maryland Ave., MC2026,
Chicago, IL 60637.
2 Present address: Department of Radiology, Mayo Clinic, Scottsdale, AZ.
3 Department of Orthodaedic Surgery, University of Chicago, Chicago, IL
60637.
Received April 15, 2005;
accepted after revision August 10, 2005.
Address correspondence to G. S. Stacy.
CME
This article is available for CME credit. See supplemental data for this
article at
www.ajronline.org
or visit
www.arrs.org
for more information.
Abstract
OBJECTIVE. The radiologist plays an important role in the workup and
staging of bone tumors. The purpose of this article is to review that role and
to discuss recent changes to the primary malignant bone tumor staging system
developed by the American Joint Committee on Cancer.
CONCLUSION. Knowledge of staging parameters for the diagnosis and
management of bone tumors will help the radiologist to generate meaningful
reports for the referring physician.
Keywords: bone cancer • musculoskeletal imaging • musculoskeletal system • oncologic imaging
Introduction
Two systems are currently used for staging malignant primary bone tumors:
the Musculoskeletal Tumor Society (MSTS) system and the American Joint
Committee on Cancer (AJCC) system. Recent revisions to the AJCC system have
received little attention in the radiology literature. We review the
importance of proper selection of the appropriate imaging techniques for the
evaluation of a patient with a suspected benign or malignant bone tumor and
describe the radiologist's role in staging primary bone neoplasms, emphasizing
recent changes to the AJCC system.
The Initial Evaluation of a Bone Lesion
A patient may seek treatment for a bone lesion because it is painful, it is
associated with a palpable mass, it is associated with a pathologic fracture,
or it is discovered incidentally on an imaging study. The Appropriateness
Criteria [1], established
by the American College of Radiology, dictate that for the initial evaluation
of a bone lesion, radiographs should be the first line of imaging
(Table 1). Not only are
radiographs relatively inexpensive, but the differential diagnosis of most
primary bone tumors is generated based on features detected on radiographs
[2,
3]. Such features suggest
either benignity or malignancy and allow one to decide whether additional
imaging examinations, if any, should be performed. The next imaging step
generally depends on one of four clinical conditions: first, the radiograph
shows normal findings, but the patient has persistent symptoms; second, the
radiograph reveals abnormal findings and the clinician suspects metastatic
disease or multiple myeloma on the basis of the patient's history, laboratory
values, or both; third, the radiograph depicts abnormal findings, showing a
nonaggressive-appearing tumor; or, fourth, the radiograph reveals abnormal
findings, showing an aggressive-appearing primary bone tumor. An important
role of the radiologist is to assist the clinician to ensure that imaging is
performed in an appropriate manner.
Lytic bone lesions are often not detectable on standard radiographs until
the tumor has resulted in 30-50% loss of mineralization
[4]. If the radiograph shows
normal or indeterminate findings, but the patient has persistent localized
symptoms, additional imaging studies are frequently required. MRI is the
preferred imaging technique in this setting
[1]. It is the most sensitive
technique for detecting marrow-based lesions, and the anatomic detail seen on
MRI is superior to that of radionuclide studies
[5]. In addition, MRI may offer
a specific diagnosis other than that of a bone tumor (e.g., occult fracture,
osteonecrosis), whereas this is often not possible with skeletal scintigraphy.
If the patient's pain is not localized, then a nuclear medicine bone scan may
be indicated as a screening test for evaluating the entire skeleton.
A lesion seen on a radiograph may represent a focus of metastatic disease
from a known or unknown primary tumor, particularly in older patients. In the
setting of a known primary tumor, radionuclide bone scanning is the primary
imaging examination used to detect osseous metastases
[6]. Patients presenting with a
bone lesion on a radiograph who do not have a known primary tumor but are
suspected of having metastatic disease based on data acquired through history
and physical examination may also undergo bone scintigraphy to confirm whether
there are multiple foci [7].
Additional imaging studies may be warranted in these cases to locate a primary
tumor, including CT of the chest and abdomen, primarily to search for lung or
renal carcinomas [8].
Mammography may be considered in women. Laboratory studies are also often
performed, including a test to determine the prostate-specific antigen level
in men. Protein electrophoresis is recommended to detect myeloma, in which
case a radiographic skeletal survey is indicated for staging
[9].
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Fig. 1 —11-year-old girl with fibroxanthoma (i.e., nonossifying fibroma).
Note benign characteristics of lesion: narrow zone of transition, intact
cortex, lack of periostitis, and lack of soft-tissue mass.
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Solitary primary tumors and tumorlike lesions of bone are commonly
encountered by radiologists. The radiologist should attempt to classify the
lesion as either nonaggressive or aggressive on the basis of its radiographic
characteristics. Nonaggressive characteristics include a narrow zone of
transition between the lesion and the surrounding normal bone, an intact
(although possibly thinned) cortex, mature periostitis, and lack of an
associated soft-tissue mass
[10]
(Fig. 1). Such lesions are
usually benign. If the radiograph shows a nonaggressive bone tumor, additional
imaging studies may be required depending on the biologic behavior of the
lesion suggested by the radiographic findings and the potential need for
operative intervention. Chondroblastomas, for example, typically have a
nonaggressive, benign appearance on radiographs; however, these lesions show
progressive growth and will need to be removed. MRI is usually the study of
choice in these instances [11,
12] because it will often show
marrow and soft-tissue involvement better than CT. CT remains of value,
however, in assessing suspected cartilaginous neoplasms for the presence of
intralesion mineralization and degree of cortical erosion. A staging system of
benign bone tumors is described later in this article.
Radiographic characteristics of an aggressive bone lesion include a wide
zone of transition between the tumor and the surrounding normal bone, cortical
destruction, aggressive-appearing periosteal new bone formation (e.g.,
onionskin or sunburst appearance), and an associated soft-tissue mass
(Fig. 2). Lesions with
aggressive radiologic characteristics are often malignant, although certain
benign entities, such as osteomyelitis and giant cell tumor, can also appear
aggressive. These aggressive-appearing benign entities may be associated with
additional radiographic or clinical features that will support the diagnosis
of a nonmalignant lesion. For example, there is a good chance that a
nonmineralized radiolucent metaepiphyseal lesion in a young adult that extends
to the articular surface of the affected bone is a giant cell tumor, even if
the margins of the lesion are poorly defined and there is limited cortical
destruction. Similarly, an aggressive-appearing lesion with a central
sequestrum in an IV drug abuser likely represents osteomyelitis. If there are
no additional features to support benignity, however, then an
aggressive-appearing lesion should be considered malignant until proven
otherwise. If a malignant tumor is suspected, additional imaging is required.
In most cases, MRI is the best imaging technique for local staging because it
best shows features important for staging.
Although MRI is currently the best imaging technique for detecting
marrow-based disease and for delineating the osseous and soft-tissue extent of
a bone tumor, it is not as useful as conventional radiography for
characterizing the aggressiveness of most bone lesions
[1-3];
however, it may occasionally help with the histologic diagnosis in certain
situations (e.g., aneurysmal bone cyst, intraosseous lipoma). CT may be
preferred over MRI for the evaluation of cortical involvement or cortically
based lesions, such as osteoid osteoma, periosteal reaction, matrix
mineralization, and lesions in flat bones. Furthermore, MDCT, with its
multiplanar capability, is a reasonable substitute for those patients who
cannot undergo MRI and can provide exquisite 3D reformations for volumetric
and preoperative assessment
[13].
Staging of Primary Bone Tumors
Malignant Neoplasms
In 1980, Enneking et al.
[14] described a system for
staging bone sarcomas that was adopted by the MSTS. Staging with the Enneking
system is based on three criteria. The first criterion is that of the extent
of the tumor: The tumor is designated T1 if it remains confined to a single
anatomic compartment (intracompartmental) and is designated T2 if it spreads
into an additional compartment or compartments (extracompartmental). The
second criterion is that of metastasis: The tumor is designated M0 if there
are no metastases and is designated M1 if there are either regional or distant
metastases. The third criterion is that of the grade of the tumor, which is a
histologic assessment of cellular atypia and is related to the tumor's
tendency to metastasize. The estimated metastatic risk of low-grade (G1)
tumors is less than 25%, whereas that of high-grade (G2) tumors is greater
than 25%. This staging system is summarized in
Table 2.
In 1983, the AJCC [15,
16] developed a slightly
different system for the staging of malignant bone tumors. Until recently,
staging with the AJCC system was based on the following four criteria: first,
the extent of the primary tumor, either confined by bone cortex (T1) or
extending through cortex (T2); second, the absence (N0) or presence (N1) of
regional lymph node metastases; third, the absence (M0) or presence (M1) of
distant metastases; and, fourth, the histologic grade of the tumor. Low-grade
tumors were designated either G1 (well differentiated) or G2 (moderately
differentiated), whereas high-grade tumors were designated either G3 (poorly
differentiated) or G4 (undifferentiated). Low-grade lesions generally are
associated with a better prognosis than high-grade lesions. This staging
system is summarized in Table
3. Note that this system did not have a defined stage III.
The AJCC system was recently revised
[17], and for cases diagnosed
beginning January 1, 2003, the extent (T) of the tumor now reflects the size
of the tumor rather than its transcortical extension. Tumors 8 cm or less in
the greatest dimension are designated T1, whereas those greater than 8 cm are
designated T2. Patients with small tumors generally have a better prognosis
than those with large tumors. A new designation, T3, has been added to
indicate skip metastases—that is, discontinuous tumors in the primary
bone site. Furthermore, M1 has been subdivided into M1a (lung-only metastases)
and M1b (metastases to other distant sites, including distant lymph nodes).
Lung-only metastases, particularly a solitary pulmonary metastasis, appear to
convey a better prognosis than osseous or hepatic metastases. This new AJCC
staging system is summarized in Table
4. Note that there is now a defined stage III, representing a
tumor without regional nodal (N0) or distant (M0) metastases, but with a skip
metastasis (T3) in the affected bone. For high-grade tumors such as
osteosarcoma, a skip lesion portends a poor prognosis. Determining the effect
on survival of multifocal low-grade lesions, such as low-grade chondrosarcomas
or low-grade vascular tumors, has proven to be more difficult
[18]. This AJCC staging system
does not apply to primary malignant lymphoma of bone or multiple myeloma, but
is used for all other primary malignant tumors of bone (e.g., osteosarcoma,
Ewing's sarcoma).
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TABLE 4: American Joint Committee on Cancer Staging System for Primary Malignant
Tumors of Bone for Those Tumors Diagnosed on or After January 1, 2003
[17]
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Fig. 3B —58-year-old man with osteosarcoma. Fat-suppressed T2-weighted
coronal MR image of proximal femur better reveals extent of lesion
(arrowheads), which is well over 8 cm in length. This finding would
be classified as T2 using revised American Joint Committee on Cancer staging
system [17].
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In addition to providing assistance to the clinician to ensure that imaging
is performed in an appropriate manner, the radiologist has a role in
evaluating each of the parameters of the bone sarcoma staging systems. For
example, when assessing the primary tumor (T), reporting the size of the
neoplasm, particularly its greatest dimension, is important for staging using
the revised AJCC system. As stated previously, MRI is best for evaluating
tumor extent and therefore the size of the primary tumor
[19-21],
particularly if one cannot discern on radiographs whether the tumor is greater
than 8 cm in greatest dimension (Figs.
3A and
3B).
On the other hand, the Enneking system does not consider the actual size
tumor size, but rather whether the tumor is intra- or extracompartmental.
Intracompartmental tumors are those that are entirely intraosseous or
parosseous without intraosseous or extrafascial extension (Figs.
4A,
4B,
5A, and
5B). Extracompartmental tumors
are those that are intraosseous with soft-tissue extension or parosseous with
intraosseous or extrafascial extension (Figs.
6A,
6B,
7A, and
7B). Identification of skip
metastases is also important. Hence, we recommend that the MRI protocol
contain at least one coronal or sagittal sequence with a large field of view
that includes the entire affected bone to search for skip metastases
(Fig. 8). We use STIR images
for this purpose at our institution, but others prefer using T1-weighted
images; we are unaware of any prospective study comparing the relative
sensitivity and specificity of T1-weighted versus STIR images for the
diagnosis of skip metastases.
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Fig. 4B —24-year-old woman with telangiectatic osteosarcoma. T1-weighted
coronal MR image shows hemorrhagic tumor (arrowheads) in proximal
tibia without soft-tissue extension, making it intracompartmental; it would be
classified as T1 using Enneking staging system
[14]. Tumor is greater than 8
cm in length and would be classified as T2 using revised American Joint
Committee on Cancer staging system
[17].
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Fig. 5B —20-year-old woman with parosteal osteosarcoma. T2-weighted sagittal
MR image shows low-signal-intensity mass (arrow) abutting posterior
surface of distal femur. No intramedullary invasion is evident. This finding
would be considered intracompartmental and classified as T1 using Enneking
staging system [14].
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Fig. 6B —6-year-old girl with Ewing's sarcoma. T2-weighted MR image with fat
suppression shows abnormal hyperintense signal in marrow of femur with
associated soft-tissue mass (arrowhead); such extension constitutes
extracompartmental spread and would be classified as T2 using Enneking staging
system [14].
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Fig. 7B —16-year-old boy with parosteal osteosarcoma. T1-weighted sagittal MR
image shows tumor abutting posterior surface of distal femur (white
arrow) with extension into medullary cavity (black arrow); such
extension constitutes extracompartmental spread and would be classified as T2
using Enneking staging system
[14].
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Fig. 8 —16-year-old boy with osteosarcoma. Fat-suppressed T2-weighted
coronal image with wide field of view shows primary tumor in proximal tibia
(arrow). Note skip metastasis (arrowhead) in tibial
diaphysis distally. This finding would be classified as T3 using revised
American Joint Committee on Cancer staging system
[17].
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We prefer MRI to bone scintigraphy for the evaluation of potential skip
metastases because skip lesions that are close to the primary tumor may not be
easily resolved with bone scintigraphy. The remaining MRI sequences should use
a surface coil and the smallest field of view possible that includes the
entire lesion; this provides optimal visualization of soft-tissue extension,
including potential neurovascular and joint involvement. A sample MRI protocol
for assessing the primary tumor, therefore, would include, first, a large
field-of-view coronal or sagittal sequence covering the entire bone and,
second, several additional sequences with a small field of view to cover the
primary tumor in its entirety—for example, T1- and fat-suppressed
T2-weighted sequences performed in the axial plane and T1- and fat-suppressed
T2-weighted sequences performed in at least one orthogonal plane.
As a general rule, IV gadolinium administration is of limited value in the
evaluation of primary bone tumors because the contrast between the tumor and
normal marrow is sufficient without it
[22-24].
Occasionally, however, gadolinium will allow one to better identify areas of
solid tumor amid necrosis and hemorrhage, which is important for biopsy
planning, and joint involvement. Some investigators have shown encouraging
results using dynamic postgadolinium imaging to distinguish tumor from
reactive edema after chemotherapy and residual tumor from non-tumor tissue
postoperatively
[25-29];
however, this technique currently does not have a role in the initial staging
of the tumor.
Lymphadenopathy accompanying primary bone sarcomas is rare, and a dedicated
search for lymph node spread is thus rarely undertaken. However, after
assessing the primary tumor using an MRI or CT examination, the radiologist
should not forget to use the same study to search for any regional
lymphadenopathy that would upstage the disease from N0 to N1. The lung is the
most common site of distant metastasis from a primary bone sarcoma, and CT is
currently the technique of choice for the detection of pulmonary metastases
[15,
30] (Figs.
9A and
9B). Bone metastases are
uncommon at initial presentation of patients with primary bone sarcomas.
However, the presence of osteosarcoma metastasis may affect treatment;
therefore, skeletal scintigraphy is recommended for patients with osteosarcoma
[31,
32] (Figs.
10A,
10B, and
10C). Identification of
metastases would group the patient into stage III using the Enneking system
and into stage IVa (lung-only metastases, M1a) or stage IVb (other distant
metastases, M1b) using the AJCC system. PET has yet to find a place in the
algorithm of primary staging; however, it has shown promise in the evaluation
of chemotherapy response and posttreatment evaluation for recurrence and
residual tumor
[33-35].
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Fig. 10B —11-year-old girl with metastatic osteosarcoma. Skeletal scintigram
shows increased radiotracer activity in ulnar diaphysis (white
arrowhead), corresponding to primary tumor, and increased activity in
contralateral distal femur (black arrowhead) adjacent to physis.
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The radiologist also plays an important role in imaging-guided biopsies.
Obtaining an adequate specimen for microscopic analysis completes the staging
process and allows a histologic grade (G) to be assigned. The biopsy should be
performed after all imaging studies that might otherwise become compromised by
postbiopsy edema and hemorrhage have been obtained. The biopsy should be
attempted only after consultation with the surgeon who plans to operate on the
tumor because the biopsy track must be excised with the tumor and hence must
not contaminate additional compartments, neurovascular structures, or areas
that may be used for reconstruction.
Benign Neoplasms
Although not routinely used by radiologists, a staging system for benign
bone tumors that is based on the biologic behavior of the tumors as suggested
by the radiographic findings has been described by Enneking
[36]. Stage 1 tumors are
latent benign bone neoplasms that remain static or heal spontaneously. An
example of such a lesion is a fibroxanthoma (nonossifying fibroma,
Fig. 1). Further radiographic
and clinical observation is usually not required, nor is treatment for lesions
that are not at risk for or have not undergone fracture.
Stage 2 tumors are active benign bone tumors; their behavior shows
progressive growth, but extension is limited by natural barriers. An example
of such a lesion is a chondroblastoma (Figs.
11A and
11B). These tumors are
typically treated via curettage, and therefore additional imaging studies may
be required preoperatively to assess the tumor extent. MRI is generally the
preferred technique for assessing marrow extension, although CT may be
warranted in certain instances as described earlier.
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Fig. 11A —12-year-old boy with chondroblastoma. Knee radiograph shows
radiolucent lesion with sclerotic margins (white arrowheads) in
epiphysis of distal femur and with probable extension into metaphysis
(black arrowhead).
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Stage 3 tumors are locally invasive benign bone tumors; their behavior
shows progressive growth not limited by natural barriers. An example of such a
lesion is a giant cell tumor (Figs.
12A and
12B). These tumors are
typically treated via extended curettage or marginal resection with or without
adjuvant therapy, and therefore additional imaging is usually required
preoperatively. MRI is generally the preferred technique for assessing osseous
and soft-tissue extension.
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Fig. 12B —50-year-old man with giant cell tumor of bone. Fat-suppressed
T1-weighted coronal MR image of wrist after IV administration of gadolinium
chelate shows giant cell tumor with soft-tissue extension
(arrow).
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Conclusion
Proper selection of the appropriate imaging techniques for the evaluation
of a patient with a suspected bone tumor is crucial for successful diagnosis
and management; radiologists should work closely with the orthopedic
oncologists for optimal management of patients with primary bone tumors.
Recent changes to the AJCC staging system emphasize the importance of tumor
size over transcortical extension. Transcompartmental extension, however,
remains an important feature of the Enneking system. The new AJCC system also
addresses skip metastases. These features, which are important for staging,
should be evaluated by the radiologist and mentioned in his or her report. It
is not necessary for most radiologists to be intimately familiar with the
details of the two staging systems. In fact, if the radiologist is accustomed
to producing complete and descriptive reports when evaluating bone tumors,
then the recent changes to the AJCC system will probably not affect his or her
dictations. All radiologists, however, should be aware that imaging factors
heavily in the staging of bone tumors, and a basic knowledge of bone tumor
staging parameters will help the radiologist produce meaningful reports.
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Abstract
Introduction
