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M u s c ul o s kel et a l I m ag i n g • R ev i ew
Staging Bone Tumors
A C E N T U
R Y O F
wo systems are currently used graph reveals abnormal findings and the cli-
T
American Journal of Roentgenology 2006.186:967-976.
TABLE 1: Summary of Appropriate Radiologic Examination Procedures for Evaluation of Bone Tumors
Radiologic Examination Procedure and Appropriateness Rating
Nuclear Medicine Bone
Clinical Condition Routine Radiography MRI Scanning CT
Screening, first study 9: Absolute requirement 1 1 1
Persistent symptoms, but 9: Contrast may be useful: 4: Good option if patient 3: If MRI not available; useful
radiograph negative depends on expertise and cannot have MRI; to evaluate cortex and
institutional preference nonspecific (MRI more trabecular pattern
specific and sensitive)
Definitely benign on 1 1 1
radiographsa
Clinically suspected osteoid 9: Necessary; follow up with CT 6: CT is more useful but 6: Very sensitive but 9: Contrast not needed
osteoma if positive diagnosis can often be made nonspecific; good for
with MRI; contrast may localization if lesion is occult
improve nidus identification radiographically
Suspicious for malignant 9: Contrast can provide more 3: Probably not indicated 5: May be useful if MRI not
characteristics on information; useful for except to look for additional available or possible; useful
radiographs vascularity and necrotic lesions for evaluation of
areas calcification, cortical
breakthrough, and
pathologic fractures
Note—Modified from the American College of Radiology Appropriateness Criteria for Bone Tumors [1]. The appropriateness rating ranges from 1 (least appropriate) to 9
American Journal of Roentgenology 2006.186:967-976.
(most appropriate).
a Additional studies (MRI or CT) may be needed if surgical intervention is contemplated and further anatomic information is required.
sions show progressive growth and will thermore, MDCT, with its multiplanar capa- grade of the tumor, which is a histologic as-
need to be removed. MRI is usually the bility, is a reasonable substitute for those pa- sessment of cellular atypia and is related to
study of choice in these instances [11, 12] tients who cannot undergo MRI and can the tumor’s tendency to metastasize. The es-
because it will often show marrow and soft- provide exquisite 3D reformations for volu- timated metastatic risk of low-grade (G1) tu-
tissue involvement better than CT. CT re- metric and preoperative assessment [13]. mors is less than 25%, whereas that of high-
mains of value, however, in assessing sus- grade (G2) tumors is greater than 25%. This
pected cartilaginous neoplasms for the pres- Staging of Primary Bone Tumors staging system is summarized in Table 2.
ence of intralesion mineralization and Malignant Neoplasms In 1983, the AJCC [15, 16] developed a
degree of cortical erosion. A staging system In 1980, Enneking et al. [14] described a slightly different system for the staging of
of benign bone tumors is described later in system for staging bone sarcomas that was malignant bone tumors. Until recently, stag-
this article. adopted by the MSTS. Staging with the En- ing with the AJCC system was based on the
Radiographic characteristics of an ag- neking system is based on three criteria. The following four criteria: first, the extent of the
gressive bone lesion include a wide zone of first criterion is that of the extent of the tu- primary tumor, either confined by bone cortex
transition between the tumor and the sur- mor: The tumor is designated T1 if it re- (T1) or extending through cortex (T2); sec-
rounding normal bone, cortical destruction, mains confined to a single anatomic com- ond, the absence (N0) or presence (N1) of re-
aggressive-appearing periosteal new bone partment (intracompartmental) and is gional lymph node metastases; third, the ab-
formation (e.g., onionskin or sunburst ap- designated T2 if it spreads into an additional sence (M0) or presence (M1) of distant
pearance), and an associated soft-tissue compartment or compartments (extracom- metastases; and, fourth, the histologic grade
mass (Fig. 2). Lesions with aggressive ra- partmental). The second criterion is that of of the tumor. Low-grade tumors were desig-
diologic characteristics are often malignant, metastasis: The tumor is designated M0 if nated either G1 (well differentiated) or G2
although certain benign entities, such as os- there are no metastases and is designated M1 (moderately differentiated), whereas high-
American Journal of Roentgenology 2006.186:967-976.
teomyelitis and giant cell tumor, can also if there are either regional or distant me- grade tumors were designated either G3
appear aggressive. These aggressive-ap- tastases. The third criterion is that of the (poorly differentiated) or G4 (undifferenti-
pearing benign entities may be associated ated). Low-grade lesions generally are associ-
with additional radiographic or clinical fea- ated with a better prognosis than high-grade
tures that will support the diagnosis of a lesions. This staging system is summarized in
nonmalignant lesion. For example, there is a TABLE 2: Enneking Staging System Table 3. Note that this system did not have a
[14] for Primary Malignant
good chance that a nonmineralized radiolu- defined stage III.
Tumors of Bone
cent metaepiphyseal lesion in a young adult The AJCC system was recently revised
that extends to the articular surface of the af- Stage Tumor Metastases Grade [17], and for cases diagnosed beginning Jan-
fected bone is a giant cell tumor, even if the IA T1 M0 G1 uary 1, 2003, the extent (T) of the tumor now
margins of the lesion are poorly defined and IB T2 M0 G1 reflects the size of the tumor rather than its
there is limited cortical destruction. Simi- IIA T1 M0 G2 transcortical extension. Tumors 8 cm or less
larly, an aggressive-appearing lesion with a in the greatest dimension are designated T1,
IIB T2 M0 G2
central sequestrum in an IV drug abuser whereas those greater than 8 cm are desig-
likely represents osteomyelitis. If there are III T1 or T2 M1 G1 or G2 nated T2. Patients with small tumors gener-
no additional features to support benignity, Note—T1 = tumor is intracompartmental, T2 = tumor ally have a better prognosis than those with
is extracompartmental, M0 = no regional or distant
however, then an aggressive-appearing le- metastasis, M1 = regional or distant metastasis, G1
large tumors. A new designation, T3, has
sion should be considered malignant until = low grade, G2 = high grade. been added to indicate skip metastases—that
proven otherwise. If a malignant tumor is
suspected, additional imaging is required.
In most cases, MRI is the best imaging tech-
nique for local staging because it best shows
features important for staging. TABLE 3: American Joint Committee on Cancer Staging System for Primary
Although MRI is currently the best imag- Malignant Tumors of Bone Before 2003 [16]
ing technique for detecting marrow-based Stage Tumor Lymph Node Metastases Grade
disease and for delineating the osseous and IA T1 N0 M0 G1 or G2
soft-tissue extent of a bone tumor, it is not as IB T2 N0 M0 G1 or G2
useful as conventional radiography for char-
IIA T1 N0 M0 G3 or G4
acterizing the aggressiveness of most bone le-
sions [1–3]; however, it may occasionally IIB T2 N0 M0 G3 or G4
help with the histologic diagnosis in certain III Not defined
situations (e.g., aneurysmal bone cyst, in- IVA Any T N1 M0 Any G
traosseous lipoma). CT may be preferred over IVB Any T Any N M1 Any G
MRI for the evaluation of cortical involve-
Note—T1 = tumor confined to cortex, T2 = tumor extends beyond cortex; N0 = no regional lymph node
ment or cortically based lesions, such as os- metastasis, N1 = regional lymph node metastasis; M0 = no distant metastasis, M1 = distant metastasis; and G1
teoid osteoma, periosteal reaction, matrix = well differentiated (low grade), G2 = moderately differentiated (low grade), G3 = poorly differentiated (high
mineralization, and lesions in flat bones. Fur- grade), G4 = undifferentiated (high grade).
TABLE 4: American Joint Committee on Cancer Staging System for Primary appear to convey a better prognosis than os-
Malignant Tumors of Bone for Those Tumors Diagnosed on or After seous or hepatic metastases. This new AJCC
January 1, 2003 [17] staging system is summarized in Table 4.
Stage Tumor Lymph Node Metastases Grade Note that there is now a defined stage III,
IA T1 N0 M0 G1 or G2 representing a tumor without regional nodal
IB T2 N0 M0 G1 or G2 (N0) or distant (M0) metastases, but with a
skip metastasis (T3) in the affected bone. For
IIA T1 N0 M0 G3 or G4
high-grade tumors such as osteosarcoma, a
IIB T2 N0 M0 G3 or G4 skip lesion portends a poor prognosis. Deter-
III T3 N0 M0 Any G mining the effect on survival of multifocal
IVA Any T N0 M1a Any G low-grade lesions, such as low-grade chondro-
IVB Any T N1 Any M Any G sarcomas or low-grade vascular tumors, has
proven to be more difficult [18]. This AJCC
IVB Any T Any N M1b Any G
staging system does not apply to primary ma-
Note—Tx = primary tumor cannot be assessed, T0 = no evidence of primary tumor, T1 = tumor 8 cm or less in
greatest dimension; T2 = tumor more than 8 cm in greatest dimension, T3 = discontinuous tumors in the primary
lignant lymphoma of bone or multiple my-
bone; Nx = regional lymph nodes not assessed, N0 = no regional lymph node metastases, N1 = regional lymph eloma, but is used for all other primary malig-
node metastasis; Mx = distant metastasis cannot be assessed, M0 = no distant metastasis, M1 = distant nant tumors of bone (e.g., osteosarcoma,
metastasis, M1a = lung, M1b = other distant sites; and Gx = grade cannot be assessed, G1 = well differentiated Ewing’s sarcoma).
(low grade), G2 = moderately differentiated (low grade), G3 = poorly differentiated high grade), G4 =
undifferentiated (high grade). In addition to providing assistance to the
clinician to ensure that imaging is performed
in an appropriate manner, the radiologist has
American Journal of Roentgenology 2006.186:967-976.
A B
A B
Fig. 7—16-year-old boy with parosteal osteosarcoma. Fig. 8—16-year-old boy with osteosarcoma. Fat-
A, Radiograph shows ossified mass along distal femoral diaphysis. suppressed T2-weighted coronal image with wide field
B, T1-weighted sagittal MR image shows tumor abutting posterior surface of distal femur (white arrow) with of view shows primary tumor in proximal tibia (arrow).
extension into medullary cavity (black arrow); such extension constitutes extracompartmental spread and would Note skip metastasis (arrowhead) in tibial diaphysis
be classified as T2 using Enneking staging system [14]. distally. This finding would be classified as T3 using
revised American Joint Committee on Cancer staging
system [17].
A B
ing the AJCC system. PET has yet to find a rovascular structures, or areas that may be barriers. An example of such a lesion is a
place in the algorithm of primary staging; used for reconstruction. chondroblastoma (Fig. 11). These tumors
however, it has shown promise in the evalua- are typically treated via curettage, and there-
tion of chemotherapy response and posttreat- Benign Neoplasms fore additional imaging studies may be re-
ment evaluation for recurrence and residual Although not routinely used by radiolo- quired preoperatively to assess the tumor ex-
tumor [33–35]. gists, a staging system for benign bone tu- tent. MRI is generally the preferred
The radiologist also plays an important mors that is based on the biologic behavior technique for assessing marrow extension,
role in imaging-guided biopsies. Obtaining of the tumors as suggested by the radio- although CT may be warranted in certain in-
an adequate specimen for microscopic anal- graphic findings has been described by En- stances as described earlier.
ysis completes the staging process and al- neking [36]. Stage 1 tumors are latent benign Stage 3 tumors are locally invasive benign
lows a histologic grade (G) to be assigned. bone neoplasms that remain static or heal bone tumors; their behavior shows progres-
The biopsy should be performed after all im- spontaneously. An example of such a lesion sive growth not limited by natural barriers.
aging studies that might otherwise become is a fibroxanthoma (nonossifying fibroma, An example of such a lesion is a giant cell tu-
compromised by postbiopsy edema and Fig. 1). Further radiographic and clinical ob- mor (Fig. 12). These tumors are typically
hemorrhage have been obtained. The biopsy servation is usually not required, nor is treat- treated via extended curettage or marginal
should be attempted only after consultation ment for lesions that are not at risk for or resection with or without adjuvant therapy,
with the surgeon who plans to operate on the have not undergone fracture. and therefore additional imaging is usually
tumor because the biopsy track must be ex- Stage 2 tumors are active benign bone tu- required preoperatively. MRI is generally
cised with the tumor and hence must not mors; their behavior shows progressive the preferred technique for assessing os-
contaminate additional compartments, neu- growth, but extension is limited by natural seous and soft-tissue extension.
A B C
Fig. 10—11-year-old girl with metastatic osteosarcoma.
A, Forearm radiograph shows osteosarcoma of ulnar diaphysis (arrowhead).
B, 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.
C, Knee radiograph shows histologically confirmed osteosarcoma metastasis (arrowhead) in distal femoral metaphysis.
Conclusion changes to the AJCC staging system empha- and mentioned in his or her report. It is not
Proper selection of the appropriate imag- size the importance of tumor size over necessary for most radiologists to be inti-
ing techniques for the evaluation of a patient transcortical extension. Transcompartmental mately familiar with the details of the two
with a suspected bone tumor is crucial for extension, however, remains an important staging systems. In fact, if the radiologist is
successful diagnosis and management; radi- feature of the Enneking system. The new accustomed to producing complete and de-
ologists should work closely with the ortho- AJCC system also addresses skip metastases. scriptive reports when evaluating bone tu-
pedic oncologists for optimal management of These features, which are important for stag- mors, then the recent changes to the AJCC
patients with primary bone tumors. Recent ing, should be evaluated by the radiologist system will probably not affect his or her dic-
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F O R YO U R I N F O R M AT I O N
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