Musculoskeletal Tumor Imaging for Staging and Treatment Planning
- Author: Eu-Leong Harvey Teo, MBBS; Chief Editor: Felix S Chew, MD, MBA, MEd more...
The prognosis of patients with musculoskeletal tumors has improved markedly because of the advent of new chemotherapeutic drugs and regimens and as a result of advances in imaging and surgical techniques. Limb-salvage operations can currently be performed with better outcomes, while in the past, limbs with tumors were treated only with amputation. Accurate preoperative surgical staging of musculoskeletal tumors is currently possible because imaging techniques provide prognostic information and aid clinicians in choosing the most appropriate treatment option for the patient.[1, 2, 3, 4, 5, 6, 7, 8, 9, 10]
(See the images below.)
Surgical Staging of Bone Tumors
The aims of surgical staging are to determine the surgical margins of resection and to facilitate interinstitutional and interdisciplinary communication regarding treatment data and results.
The Enneking system for the surgical staging of bone and soft-tissue tumors is based on grade (G), site (T), and metastasis (M) and uses histologic, radiologic, and clinical criteria. It is the most widely used staging system and has been adopted by the Musculoskeletal Tumor Society.[12, 13, 14, 15] The system should be reserved for staging mesenchymal lesions rather than nonmesenchymal ones (such as the lesions of Ewing sarcoma, lymphoma, and leukemia), because the biologic behavior of nonmesenchymal tumors differs from that of mesenchymal lesions. For example, studies have shown that the site of occurrence of Ewing sarcoma is not a significant factor when tumor size is considered.
In the Enneking system, bone tumors are graded as follows:
G0 - Benign lesion
G1 - Low-grade malignant lesion
G2 - High-grade malignant lesion
Surgical grade generally follows histologic grade; however, a higher surgical grade may be applied if the radiographic features and clinical behavior of a lesion indicate an aggressiveness that is incompatible with its benign histologic features.
In the Enneking system, the site and local extent of bone tumors are classified as follows:
T0 - A benign tumor that is confined within a true capsule and the lesion's anatomic compartment of origin (ie, a benign intracapsular, intracompartmental lesion)
T1- An aggressive benign or malignant tumor that is still confined within its anatomic compartment (ie, an intracompartmental lesion)
T2 - A lesion that has spread beyond its anatomic compartment of origin (ie, an extracompartmental lesion)
Metastatic classification in the Enneking system is as follows:
M0 - No regional or distant metastasis
M1 - Regional or distant metastasis
Under the Enneking system, malignant tumors are classified into stages I-III, with further subdivisions into A and B. Grade 1 and grade 2 tumors are stage I and stage II, respectively. T1 and T2 tumors are stage A and stage B, respectively. Tumors with distant metastasis are stage III (see Table 1 below).
Table 1. Enneking System for the Surgical Staging of Malignant Bone and Soft-Tissue Tumors (Open Table in a new window)
|III||G1 or G2||T1 or T2||M1|
Staging of Benign Tumors
The Enneking staging system divides benign tumors into latent, active, or aggressive tumors (see Table 2 below). Latent tumors are asymptomatic and are usually discovered incidentally. They reach a stage of nongrowth after a period of slow growth. Active tumors are mildly symptomatic and may be discovered if pathologic fracture occurs or if the tumor is associated with mechanical dysfunction. Active tumors usually grow steadily. Aggressive benign lesions grow rapidly and usually are symptomatic and tender on palpation. Table 2. Enneking System for the Surgical Staging of Benign Lesions
Table 2. (Open Table in a new window)
|3||Aggressive||G0||T1 or T2||M0 or M1|
Limb Salvage Surgery and Staging
The aims of limb salvage surgery are to cure disease and to preserve limb function for the patient. The aims are usually achieved by using a combination of limb salvage surgery and adjuvant therapy.
Limb salvage operations are indicated if the following conditions are satisfied:
The tumor is situated in the extremities and/or the axial skeleton.
The tumor margins are amenable to surgery.
Only moderate soft-tissue extension is present.
The neurovascular bundles are intact.
Metastases are absent or amenable to curative treatment.
The patient is in good general health.
Regarding resection margins, optimal surgical margins are 6 cm of healthy bone around the bone margins and 2 cm of healthy soft tissue around the soft-tissue extent of the tumor. If a malignant tumor is responsive to chemotherapy, smaller resection margins may be acceptable.
The Enneking classification correlates the tumor stage with the excision margins as follows:
Staging is as follows:
Stage 1 tumors - Intracapsular excision (or curettage) is adequate.
Stage 2 tumors - Extracapsular excision passing through the reactive zone is needed.
Stage 3 tumors - Wide margins of resection are required in stage 3 lesions (aggressive benign tumors). In areas that are not amenable to wide excision, marginal excision together with adjuvant treatment (eg, radiation therapy) may be acceptable.
Staging is as follows:
Stage IA - These tumors are treated with wide excision and are usually amenable to limb salvage procedures.
Stage IB - Such tumors may be treated with wide excision, but the choice between amputation and limb salvage depends on the estimated amount of residual tumor left behind after a limb salvage procedure.
Stage II - These tumors are high grade, are usually extracompartmental, and have a significant risk for skip metastases. They usually are not amenable to limb salvage operations and require radical amputation or disarticulation in most patients. However, bone tumors responsive to chemotherapy may be treated successfully using wide excision and adjuvant therapy.
Stage III - Tumors at this stage are responsive to chemotherapy and may be treated with aggressive resection. Those that are not responsive to adjuvant therapy should be treated with palliative resection.
Radiography is the initial imaging modality in the evaluation of bone tumors.[16, 17] Some benign lesions have characteristic radiographic features that make biopsy unnecessary. Examples include fibrous cortical defects, bone islands, simple bone cysts, bone infarcts, and typical variants, such as pseudocysts of the humerus and calcaneus. (See the images below.)
Radiographic features can also help in distinguishing malignant from benign bone lesions in many patients. Lodwick and colleagues established a radiographic grading system based on the analysis of the radiographic features of a bony lesion.[19, 20] The important radiographic signs for grading bone tumors is listed as follows, in order of priority:
Pattern of destruction - Geographic or not geographic, appearance of marginal interface zone
Penetration of the cortex by the lesion
Absence or presence of a sclerotic rim
Absence or presence of the expanded cortical shell, as well as its extent
The grading system developed by Lodwick and coauthors groups lesions into 3 grades.
Grade 1A, 1B, and 1C - Benign lesions with edge characteristics ranging from well defined to poorly defined
Grade 2 - Low-grade malignant lesions with invasive features; applies particularly to lesions demonstrating total penetration of the cortex
Grade 3 - High-grade malignant lesions with invasive, permeative, and destructive features
Another grading system divides bone lesions into 4 groups, each with individual management algorithms.[21, 22]
Group 1 - Radiographically benign lesions that do not require further investigation or treatment
Group 2 - Lesions with a high likelihood of being benign but that should be confirmed as benign by means of clinical or radiographic follow-up examination
Group 3 - Benign lesions that require surgical resection because of aggressive behavior or a risk of pathologic fracture
Group 4 - Aggressive-appearing lesions that should be considered malignant but on which a biopsy should be performed to confirm the diagnosis and histologic grade
In the staging of bone tumors, computed tomography (CT) scanning has a role in the detailed evaluation of local disease and in assessing the lungs for pulmonary metastases.
In evaluating local disease, CT scanning complements radiography because it can be used to assess disease in areas that are not easily visualized with radiography, such as the spine and pelvis. In addition, CT scanning is better for use in determining the type of cortical destruction that has occurred and in assessing whether matrix mineralization is present. CT scanning is also helpful in determining the internal contents of some lesions. (See the images below.)
Although magnetic resonance imaging (MRI) is generally accepted to be superior to CT scanning in the evaluation of local tumor spread, Panicek and colleagues have shown that CT scanning and MRI are equally accurate in the staging of local disease in bone tumors.
CT scans have been shown to be more accurate than chest radiographs in evaluating the lungs for the presence of metastases. However, CT scans may produce false-positive results when small lung nodules are detected. Follow-up CT scans are useful in monitoring the nodules.
Apostolova et al studied the use of single-photon emission computed tomography (SPECT), compared with planar bone scanning, in 271 patients with tumors of the spine and pelvis, and they suggested that SPECT be used in patients with equivocal findings on planar imaging. Retrospective image interpretation was performed independently for planar and SPECT scans. SPECT changed definite staging on planar images in fewer than 4% of patients, but in patients with planar equivocal staging, SPECT provided a definite diagnosis in more than 80%.
MRI has several advantages compared with other imaging modalities in visualizing and staging bone tumors. In particular, accurate depiction of the soft tissues allows sensitive detection of soft-tissue extension of and medullary involvement by a tumor. MRI can be performed in several orthogonal planes. The absence of ionizing radiation and beam-hardening artifacts are advantages of MRI compared with CT scanning.[25, 26, 26, 27, 28] MRI is the modality of choice for the imaging and staging of bone tumors.[29, 30]
Technical considerations for MRI
Technical considerations for MRI include the following:
Obtain magnetic resonance images before performing a biopsy.
Position the patient comfortably to minimize motion artifacts.
Sedation is often required in children.
Place a vitamin E or cod liver oil capsule over the site of interest.
Use the appropriate coils.
Perform the imaging in at least 2 planes.
Perform conventional T1-weighted and T2-weighted, spin-echo sequences because they provide reproducible images. Typically, pathology appears as areas of low signal intensity on T1-weighted images and as areas of high signal intensity on T2-weighted images.
Fast spin-echo sequences with fat suppression also are popular imaging sequences, and they are used in many centers because of the time-saving advantages (see the image below).
Short T1 inversion recovery (STIR) sequences provide fat-suppressed images with T1- and T2-additive effects (see the image below). STIR sequences are particularly useful for the detection of small lesions and bone marrow abnormalities.
MRI contrast agents
The intravenous administration of gadolinium diethylenetriamine penta-acetic acid (Gd-DTPA) increases the signal intensity on T1-weighted images by reducing the T1 relaxation time (see the images below). This feature is useful in distinguishing necrosis from an active tumor and in differentiating cystic lesions from solid lesions. Although some authors have indicated that MRI contrast agents do not improve tumor detection or staging accuracy, most authors have found that the administration of MRI contrast agents is useful in making difficult diagnoses.
Gadolinium-based contrast agents have been linked to the development of nephrogenic systemic fibrosis (NSF) or nephrogenic fibrosing dermopathy (NFD). The disease has occurred in patients with moderate to end-stage renal disease after being given a gadolinium-based contrast agent to enhance MRI or magnetic resonance angiography (MRA) scans.[33, 34] NSF/NFD is a debilitating and sometimes fatal disease. Characteristics include red or dark patches on the skin; burning, itching, swelling, hardening, and tightening of the skin; yellow spots on the whites of the eyes; joint stiffness with trouble moving or straightening the arms, hands, legs, or feet; pain deep in the hip bones or ribs; and muscle weakness.
Role of MRI in diagnosis
In many cases, MRI cannot provide a histologic diagnosis of soft-tissue lesions. However, some lesions have appearances that are usually characteristic enough for a histologic diagnosis based on the MRI findings. Examples of such lesions include lipomas, superficial and skeletal muscle hemangiomas, benign neural tumors, periarticular cysts, hematomas, and pigmented villonodular synovitis.
The most common soft-tissue lesions diagnosed with MRI are lipomas. They appear well circumscribed, homogeneous, and isointense relative to subcutaneous fat on images obtained with all pulse sequences. Thin, low-intensity septa also are sometimes seen in lipomas.
Some general guidelines regarding the relationship between MRI signals and histologic tissue types can be made, as follows:
Tumor tissue is usually low in signal intensity on T1-weighted images and high in signal intensity on T2-weighted images.
The mineralized matrix is seen as areas of low signal intensity on T1-weighted and T2-weighted images.
Areas of hemorrhage are seen as areas of high signal intensity on T1-weighted and T2-weighted images.
The measurement of T1 and T2 relaxation times are useful in determining the histologic features.
The imaging criteria that are used in differentiating benign from malignant lesions on radiographs and CT scans have been applied to MRI. Typically, benign lesions are well defined and sharply demarcated from the surrounding healthy tissue. Malignant lesions are typically more extensive and involve surrounding tissue to a greater extent than do benign lesions. However, MRI signal intensity alone is not reliable in distinguishing between benign and malignant tumors.
Erlemann and colleagues reported that dynamic imaging after contrast enhancement is approximately 80% accurate in differentiating benign tumors from malignant ones. MRI may be useful in distinguishing benign from malignant cartilaginous tumors.[39, 40] Low-grade chondrosarcomas have enhancing areas of fibrovascular septa with high signal intensity on T2-weighted images, between lobules of hyaline cartilage. Janzen and coauthors reported that the presence of abnormal marrow or soft tissue around a chondroid tumor is suggestive of chondrosarcoma, especially if bony destruction or aggressive radiographic features are lacking. Other benign lesions with characteristic MRI findings include osteochondromas, chondromas, aneurysmal bone cysts, and nonossifying fibromas.
Role of MRI in staging
MRI is the modality of choice in assessing local spread of tumor (Enneking sites T1 and T2). MRI can help in accurately detecting tumor involvement of neurovascular structures, muscle compartments, growth plates, and joints.
MRI is accurate in determining involvement of the neurovascular bundle (see the image below). MRA may provide additional information regarding neurovascular bundle involvement. MRA can help in assessing peripheral vascular branches and tumor neovascularity. By demonstrating treatment-induced changes in tumor neovascularity, MRI may also help in assessing a tumor's response to treatment.
Although MRI usually accurately depicts the intramedullary spread and soft-tissue extension of a tumor (see the image below), differentiating tumor edema from true tumor spread may occasionally be difficult. Typically, edema is seen as an ill-defined, homogeneous, hyperintense area with a featherlike appearance. Edema tends to follow the tissue planes; it has no mass effect, and unlike the distinct pseudocapsule of tumor tissue, it possesses a fading margin. The administration of Gd-DTPA also aids in the distinction of tumor tissue from tumor edema, because tumor tissue enhances and edema does not. Intramedullary spread and soft-tissue extension of a tumor are more accurately assessed with MRI than with CT scanning.
The accuracy of MRI in the evaluation of joint involvement is controversial (see the image below). Some authors have found MRI to be more accurate than CT scanning in demonstrating joint involvement, although Bloem and colleagues found that CT scanning and MRI provided similar results in their study. Enhancement of joint synovium after Gd-DTPA administration may mimic tumor involvement. Joint effusion alone is not diagnostic of tumor involvement.
Role of MRI in assessing the response to treatment
MRI is increasingly used to assess tumor response to preoperative chemotherapy (see the images below). This assessment is achieved by evaluating changes in a tumor's size, margins, signal intensity, and enhancement patterns.[44, 45, 46, 47, 48, 49, 50]
After chemotherapy, a poor tumor response with no reduction in tumor size usually indicates a poor histologic response; however, a substantial reduction in tumor size does not necessarily indicate a good prognosis. In most patients with Ewing sarcoma, a marked decrease in tumor size is an expected finding. MRI findings of residual soft-tissue components and tumor volume are usually correlated with the histologic response of the tumor to chemotherapy. Tumors that decreased in size by 25% and 75% after chemotherapy have a substantial overlap between good responses and poor responses.
Postchemotherapeutic MRI signal–intensity changes
MRI patterns are often unpredictable because tumors undergo necrosis, hemorrhage, edema accumulation, granulation-tissue formation, and fibrosis after chemotherapy.[39, 52] Some general indicators of a good response to chemotherapy include the following:
Decreasing signal intensity on T2-weighted images
A circumferential hypointense rim combined with a decrease in size of the soft-tissue component in patients with Ewing sarcoma
Increased homogeneous signal intensity on T2-weighted images in Ewing sarcoma (indicating tumor replacement by a hypocellular mucomyxoid matrix)
The intravenous administration of Gd-DTPA helps in differentiating remnant tumor from nontumorous tissue. Because of its greater vascularization, tumor tissue enhances more than does nontumorous tissue. However, the presence of vascularized granulation tissue, neovascularity in necrotic areas, or reactive hyperemia also may cause Gd-DTPA enhancement on static MRIs, making tumor-free tissue difficult to differentiate from tumor tissue.
Dynamic, contrast-enhanced magnetic resonance images are better than static images for determining a tumor's response to chemotherapy (see the images below). Images in patients who respond well to chemotherapy show a reduction in enhancement, whereas those of patients who respond poorly show little or no reduction. Images should be acquired by using short time intervals because reactive changes may show contrast enhancement indistinguishable from that of tumor in the later phases of enhancement.
Parametric first-pass imaging and subtraction MRI have been used to increase the detection of early arterial enhancement of residual viable tumor.
The use of magnetic resonance spectroscopy with phosphorus-31 in assessing changes in tumor metabolism and in monitoring changes in spectra has been evaluated. There are still limitations to this technique because of the difficulty of obtaining representative spectra in all locations in the tumor, the contamination of tumor spectra with phosphorus in adjacent soft tissues, and the technique's insensitivity to tumor heterogeneity.
Role of MRI in detecting recurrence
The differentiation between tumor recurrence and chronic posttherapeutic changes remains a difficult challenge. In general, recurrence is suggested when T1-weighted imaging demonstrates a hypointense lesion, which then enhances after Gd-DTPA administration and appears hyperintense on T2-weighted images. Chronic, posttherapeutic changes in a nonnodular lesion have low to intermediate signal intensity on T1-weighted images and lack high signal intensity on T2-weighted images.
Static, contrast-enhanced MRI may not always be helpful in distinguishing recurrent tumors from posttherapeutic changes because the latter may also show enhancement after the administration of Gd-DTPA. Dynamic, contrast-enhanced MRI may be beneficial by demonstrating early enhancement in tumor tissue that is not seen in posttherapeutic changes.
Fatty marrow may reconvert to hemopoietic marrow in children with osteosarcoma who have been treated with chemotherapy and granulocytic colony-stimulating factor. When such reconversion occurs in a patient, the marrow's appearance on magnetic resonance images may resemble that of a recurrent tumor, although reconverted marrow usually appears bilateral and symmetric. The reconverted marrow's signal intensity is similar to that of skeletal muscle, unlike the signal-intensity characteristics of a recurrent tumor.
Tumor recurrence may be hard to detect when orthopedic implants are in close proximity to tumor sites. Orthopedic implants may cause susceptibility artifacts, making evaluation of the surrounding tissues difficult. Susceptibility artifacts occur at interfaces of structures with markedly different magnetic susceptibilities. Pure titanium orthopedic implants are nonferromagnetic, whereas some alloys are ferromagnetic. Susceptibility artifacts may be decreased by optimally positioning patients with orthopedic implants, by switching the orientation of the frequency- and phase-encoding gradients, by using the smallest voxel size, and by choosing fast spin-echo sequences. Susceptibility artifacts are more severe in gradient-echo sequences and in sequences with a long echo time.
Radiologic Studies and Intervention
Nuclear medicine studies
Radionuclide bone scans are commonly obtained by using technetium-99m (99mTc)–labeled diphosphonate to stage bone tumors.
Radionuclide bone scanning has a role in detecting metastases, skip lesions, lesion multiplicity, and postoperative tumor recurrence. Bone-forming, metastatic lesions in the lungs (eg, osteosarcoma) are occasionally detected with bone scintigraphy (see the image below).[54, 55, 56]
Areas showing increased tracer uptake in the skeleton should be evaluated by using radiography. Further evaluation with CT scanning or MRI may be necessary if plain radiographic findings are negative. Biopsy may be necessary if a positive result might change the patient's treatment.
Soft-tissue masses and the soft-tissue components of bony tumors may be visualized by using ultrasonography (US). The histologic diagnosis of the lesions usually cannot be made by using US. The aim of US in the evaluation of musculoskeletal lesions is to confirm the presence of a lesion, to determine if the lesion is cystic or solid, to assess the relationship of the mass to the surrounding structures (eg, neurovascular bundle), to evaluate the vascularity of the mass, and to guide interventional procedures if indicated.
Although color Doppler ultrasonographic evaluation of the mass is unreliable in determining the histologic diagnosis of the lesion and whether the lesion is benign or malignant, color Doppler US is a useful tool for monitoring the regression of tumor neovascularity induced by therapy in patients with musculoskeletal sarcoma. When the clinical findings suggest the recurrence of a soft-tissue sarcoma, US can be used as the initial imaging technique for evaluation. US can also be used in addition to MRI when susceptibility artifacts secondary to orthopedic hardware (including prostheses) prevent the evaluation of specific areas.
Currently, angiography is used only occasionally to evaluate neurovascular bundle involvement. Its role has largely been replaced by cross-sectional imaging modalities. Angiography still has a postoperative role in decreasing hemorrhage through the embolization of tumor-supplying vessels (see the images below).
Positron emission tomography scanning
Positron emission tomography (PET) scanning was developed in the 1960s and has increasingly been used in some centers for detecting and staging malignancy. PET scanning can be used to image tumor metabolism because of the detection of photons emitted from tissue after the intravenous injection of a pharmaceutical, such as 2-[fluorine 18]-fluoro-2-deoxy-D-glucose (FDG).[58, 59, 60, 61, 62, 63, 64]
These photons are detected by the PET scanner and reconstructed into a 3-dimensional image. Tumor metabolism is higher than that of normal tissue and shows higher FDG uptake. In bone tumors, the degree of FDG uptake is related to the histologic grade of the tumor. However, increased FDG uptake in a tumor does not necessarily indicate malignancy, because increased uptake can also be seen in benign bone lesions, such as nonossifying fibromas, fibrous dysplasia, giant cell tumors, eosinophilic granulomas, and aneurysmal bone cysts.
According to Bischoff et al, combined FDG-PET-CT reliably differentiates soft tissue and bone tumors from benign lesions. The authors performed a retrospective study to determine whether integrated FDG-PET and CT (FDG-PET-CT) is more accurate than the 2 modalities interpreted separately. Sensitivity, specificity, and accuracy for CT alone was 81%, 84%, and 83%. Sensitivity, specificity, and accuracy for PET was 71%, 82%, and 76%. Sensitivity, specificity, and accuracy for FDG-PET-CT was 80%, 83%, and 86%.
PET has been shown to have a sensitivity similar to that of serial CT scanning and MRI for detecting lesions and for distinguishing postsurgical scarring from recurrent tumors. However, the specificity of PET is higher than that of serial CT scanning or MRI.
In evaluating musculoskeletal sarcomas, when it comes to detecting recurrent tumor, FDG-PET scanning has higher sensitivity and specificity, as well as a greater positive and negative predictive value, than does iodine-131-meta-iodobenzylguanidine (MIBG) scanning.
In summary, PET scanning appears to be better than CT scanning and MRI in depicting residual or recurrent tumor after treatment. The main disadvantage of PET scanning is the high cost of the equipment, which limits the modality's availability.
Image-guided biopsy is less expensive and safer than open biopsy. The biopsy site should be located where the needle tract will be excised in future surgery, because of possible tumor seeding along the needle tract. Fluoroscopy with C-arm guidance, CT scanning, and MRI can be used to locate the most appropriate biopsy site. The primary advantage to fluoroscopy is its ability to create dynamic images.
CT-guided biopsy is usually employed if the lesion is located in a complicated part of the anatomy, such as the upper thoracic spine or pelvis (see the image below).
For aspiration cytology, a fine-gauge needle is used. For a lesion that predominantly consists of soft-tissue components, a cutting needle is usually chosen. For bone tumors, a combined trephine and cutting needle is utilized. The needle tract should pass through the bony and soft-tissue components of the tumor, allowing for complete histologic examination. Hemorrhage, infection, and trauma to surrounding tissues are complications of biopsy.
Imaging plays a crucial role in staging bone tumors. Radiography, occasionally with the aid of CT scanning, is required for the detection and diagnosis of bone tumors. CT scanning and bone scintigraphy are useful in depicting pulmonary metastases and the multiplicity of lesions, respectively. MRI is the modality of choice in staging bone tumors because it can accurately depict the local spread of tumor to surrounding tissues. Contrast-enhanced MRI may be helpful in detecting viable posttreatment tumors.
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|III||G1 or G2||T1 or T2||M1|
|3||Aggressive||G0||T1 or T2||M0 or M1|