Journal of Surgical Oncology 2015;111:496–503

Contemporary Imaging of Soft Tissue Sarcomas BEHRANG AMINI, MD, PhD,1 AARON C. JESSOP, MD, MBA,1 DHAKSHINA M. GANESHAN, MD,1 WILLIAM W. TSENG, MD,2,3 AND JOHN E. MADEWELL, MD1 1

2

Department of Diagnostic Radiology, The University of Texas M.D. Anderson Cancer Center, Houston, Texas Division of Upper GI/General Surgery, Section of Surgical Oncology, University of Southern California, Los Angeles, California 3 Hoag Family Cancer Institute, Hoag Memorial Hospital Presbyterian, Newport Beach, California

Imaging plays an important role in the diagnosis, biopsy, staging, and follow‐up of patients with soft tissue sarcomas. General principles of imaging diagnosis of soft‐tissue sarcomas using radiography, ultrasound, CT, MRI, and PET/CT will be discussed, with emphasis on the role of location, internal fat and calcification, presence of myxoid stroma, and enhancement characteristics.

J. Surg. Oncol. 2015;111:496–503. ß 2014 Wiley Periodicals, Inc.

KEY WORDS: neoplasms, connective and soft tissue; sarcoma, soft tissue; gastrointestinal stromal tumors; radiology

INTRODUCTION

penetration, an issue that becomes especially important in central soft tissue lesions with potential for deep invasion (Fig. 2B and C).

Imaging plays an important role in the diagnosis, biopsy, staging, and follow‐up of patients with soft tissue sarcomas. Staging systems and follow‐up of the sarcoma patient are discussed elsewhere in this issue. General imaging principles, as they relate to sarcomas, will be discussed below.

CT

Imaging of soft‐tissue sarcomas should proceed in an ordered fashion. Imaging should be performed at a center experienced in assessment of soft‐tissue sarcomas. In the trunk and extremities, intravenous contrast is required for MRI assessment of the lesion and invasion of adjacent structures. Fat suppression should be obtained on post‐contrast sequences. Enteric and intravenous contract agents are typically needed for CT assessment of intra‐abdominal neoplasms.

CT can offer a fast 3‐dimensional view of a mass and its surrounding structures. In the trunk and extremities, its main application is in further characterizing the internal calcifications of a lesion as benign (Fig. 1), and in assessing the effect of a mass on adjacent soft tissues and bone. CT is the modality of choice in the abdomen and pelvis for general surgical indications and remains the best initial modality for assessment of intra‐ abdominal and intra‐thoracic lesions. The speed of acquisition of CT images is helpful in assessment of lesions in areas susceptible to respiratory motion (chest and upper abdomen). The widespread availability of enteric contrast agents for CT allows for optimal assessment of lesions within or close to bowel (Fig. 3A and B). However, advances in MRI technology can help alleviate the effect of motion, and the inherent superior contrast resolution of MRI obviates the need for contrast agents in most cases.

Radiography

MRI

In the extremities and peripheral trunk (e.g., shoulders and hips), radiography is generally needed for evaluation of soft tissue masses and bone lesions. Certain characteristic imaging features on radiography (Fig. 1) can obviate the need for further imaging work‐up, saving patients anxiety, cost, and time. In other cases, the degree of aggressivity of a lesion can be determined based on its effect on adjacent bone. Radiography is also helpful in assessment of primary bone tumors that present with large soft tissue masses. Radiography has little to no role in the primary evaluation of or intra‐ abdominal sarcomas, but can be helpful in assessment of complications, such as obstruction or perforation. Calcifications or bone erosions that would be easily seen in the extremities, are typically obscured by bowel gas.

MRI, due to its superior contrast resolution and large field of view, is the optimal imaging modality for characterization of a soft‐tissue lesions in the trunk and extremities (Fig. 4). Adequate MRI technique is vital, and is not consistently applied in imaging centers not accustomed to tumor imaging. MRI machines convert the response of protons (free hydrogen nuclei) to static and dynamic magnetic fields into images that reflect various chemical properties of the tissue under investigation. In contrast to CT, in which a single acquired image set is manipulated to generate images in different planes and windows (e.g., lung, bone, soft tissue), MRI usually requires acquisition of images using different input magnetic fields

CHOICE OF IMAGING

Ultrasound Ultrasound is inexpensive, readily available, and does not expose patients to ionizing radiation. The primary strength of ultrasound is its ability to confirm the presence of a suspected cyst and obviate need for further workup (Fig. 2A). It is also helpful in guiding biopsy once a primary or recurrent mass has been characterized. In most cases, however, ultrasound is not sufficient for initial work‐up or post‐ operative follow‐up of a soft tissue lesion due to its limited depth of

ß 2014 Wiley Periodicals, Inc.

*Correspondence to: John E. Madewell, MD, Department of Diagnostic Radiology, The University of Texas M.D. Anderson Cancer Center, 1400 Pressler, Unit 1475, Houston, TX 77030. Fax: þ1‐713‐792‐4973. E‐mail: [email protected] Received 11 July 2014; Accepted 14 August 2014 DOI 10.1002/jso.23801 Published online 27 October 2014 in Wiley Online Library (wileyonlinelibrary.com).

Imaging of Soft Tissue Sarcomas

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Fig. 1. Use of radiography in assessment of soft‐tissue masses of the extremities. A,B: Hemangioma on frontal radiography (A) and coronal post‐ contrast MRI (B) of the right forearm. Radiograph shows multiple well‐defined calcifications (arrowheads) in the interosseous space. Well‐defined remodeling of the cortex of the distal radius (arrows) suggests an indolent process. MRI, which was obtained prior to radiography, showed a heterogeneously enhancing soft tissue mass at this location ( ) with associated erosion and intramedullary extension (arrows) in the radius and ulna, that was concerning for a malignant neoplasm. Note that calcifications are not well seen on MRI. C–E: Heterotopic ossification (“myositis ossificans”) in a different patient. C: Frontal radiograph of the left hip shows a well‐defined, peripherally mineralized structure ( ) medial to the lesser trochanter. D: CT shows a mass ( ) in the adductor magnus muscle and confirms the peripheral pattern of mineralization. E) Contrast‐ enhanced axial MRI shows an enhancing mass ( ) in the adductor magnus muscle with ill‐defined enhancement extending to the adjacent muscles of the adductor compartment. (pulse sequences) to obtain images in different planes and to accentuate different properties of tissues. MRI machines with different static magnetic field strengths are available. Higher magnetic field strengths allow for faster scanning or higher signal to noise ratio. This trade‐off between time and signal is at the heart of all practical decisions made in selecting MRI sequences. Longer scan times can provide better images, but are more susceptible to patient motion (which is more likely the longer patients have to maintain

Fig. 2. A: Color Doppler ultrasound of a palpable abnormality at the lateral aspect of the right foot shows a well‐defined structure without internal echoes ( ) or vascular flow and with posterior acoustic enhancement (arrow) all findings indicative of a simple cyst. B: Ultrasound obtained for follow‐up of a desmoid tumor in the right gluteal region shows a lobulated intramuscular mass (white arrow). C: Post‐contrast axial T1WI in the same patient shows an avidly enhancing mass in the right gluteus maximus muscle (top, white arrow), as well as extensive intra‐pelvic extension of disease, including involvement of the piriformis muscle (bottom, black arrow), which was not identified on ultrasound. Journal of Surgical Oncology

a position). The machines most commonly in use have magnetic field strength of 1.5 Tesla (T). In general, low‐field (< 1 Tesla) devices are not suitable for oncological imaging. T1‐weighted images (WI) are typically assessed for delineation of anatomy and assessment of fat planes. On T1‐WI (e.g., Fig. 4A), fat is high signal (bright) and fluid (e.g., urinary bladder or cerebrospinal fluid) is low signal (dark). Muscle and tumor typically have intermediate signal and can be difficult to differentiate from each other. Gadolinium‐based contrast agents are added to enhance the difference between soft tissues and tumors. The diffusion of contrast through vessels leads to increased signal in highly vascular structures, which include neoplasms, as well as non‐neoplastic structures such as synovium or inflammatory tissues. T2‐WIs are typically used for sensitive assessment of abnormalities. On T2‐WI images, fat, fluid, and cellular material have high signal. In oncological practice, fat suppression should be applied to T2‐WI and post‐contrast T1‐WI to allow for sensitive assessment of tumor against the background of fat. The contrast between normal and abnormal structures can be increased by suppressing the normally bright signal from fat (Fig. 4B and C). Adequate fat suppression (FS) is vital for oncological imaging, and can be achieved using different techniques. Common techniques used for assessment of soft tissue sarcomas include spectral fat saturation (“fat sat”) and short TI inversion recovery (STIR). These sequences result in low signal of fatty structures (e.g., subcutaneous fat), but have different strengths and weaknesses [1].

Fig. 3. A: Axial contrast‐enhanced CT of the abdomen without rectal contrast shows a subtle mass (arrow) in the hepatic flexure, representing lymphoma. B: Axial contrast‐enhanced CT of the abdomen with rectal contrast shows the mass (arrow) to better advantage.

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Amini et al. (mucoid tissue, hemorrhage, proteinaceous fluid, and gadolinium) can be suppressed along with fat, and fatty tissues (e.g., fatty infiltration or tumors containing fat) may not be fully suppressed as expected. Knowledge of this pitfall is necessary for correct image interpretation. Because of the suppression of gadolinium signal, STIR imaging is not used with post‐contrast T1‐WIs. Adequate coverage of the anatomy of interest (“field‐of‐view”) is also important for complete imaging of the tumor and related structures. Longitudinal images are usually selected to optimize imaging of the tumor and relevant anatomy. In the extremities, anteriorly or posteriorly located lesions are best assessed using sagittal planes, while laterally or medially positioned lesions are best assessed using coronal planes. The region surrounding the lesion should be adequately covered in these longitudinal images to allow complete assessment of the extent of perilesional signal abnormality and effect on anatomy of interest. The nearest joint should be included in the field‐of‐view to serve as a reference for surgical planning, especially for deep lesions that can be hard to localize clinically.

CT and MR Angiography

Fig. 4. A: Axial T1WI of the left elbow showing a mass with a clear fat plane (between arrows) separating it from the superficial fascia. The mass contained small internal high signal areas (arrowhead) and biopsy revealed pleomorphic lipoma. Note that the majority of the mass has intermediate signal similar to that of the adjacent muscles. B: Post‐ contrast axial FS T1WI of the left lower leg shows a mass with areas of confluent (white  ) and reticular (black  ) enhancement, the latter representing myxoid stroma in this myxoid liposarcoma. There is loss of the fat plane between the mass and the anterior tibial artery (arrowhead) suspicious for mural involvement, as well as frank erosion of the cortices of the tibia and fibula (arrows). Note that the mass has high signal on this post‐ contrast image, which allows for differentiation from adjacent muscles. C: Post‐contrast axial FS T1WI of the proximal thigh shows an enhancing intramedullary mass ( ) with a relatively intact cortex and a large soft tissue component, representing Ewing sarcoma of bone. The deep femoral artery (black arrowhead) is encased by the mass. The deep femoral vein is not visualized in its expected location (white arrowhead), indicating vascular invasion or severe luminal stenosis. Note that the mass has high signal on this post‐ contrast image, which allows for differentiation from adjacent muscles. D: Post‐contrast axial FS T1WI shows a peripherally enhancing mass (white arrow) in posterior soft tissues of the left shoulder representing basal cell carcinoma. There is involvement of the skin, subcutaneous fat, and the deltoid muscle. A satellite nodule (black arrow) is present anteriorly with invasion of the adjacent trapezius and levator scapulae muscles. The fat suppression was performed using fat saturation technique. This technique is susceptible to field inhomogeneity which typically occurs at the edges of body parts (arrowheads).

Spectral fat saturation, which is sometimes incorrectly used as a synonym for the more general term, fat suppression, provides quick imaging, which is helpful for reducing artifact from patient motion. However, fat saturation is susceptible to inhomogeneities in the magnetic field, which are typically seen at the edges of the body part under study (Fig. 4D). Failure of fat suppression can be identified by noting high or intermediate signal in fatty structures. Spectral fat saturation can be used with both T1‐ and T2‐WIs. STIR provides more uniform fat suppression over the imaged area and can be used with low‐field‐strength magnets, but results in longer scan times or lower signal to noise ratio. In addition, the fat suppression with STIR is somewhat nonspecific. This means that non‐fatty tissues Journal of Surgical Oncology

CT and MR angiography (CTA and MRA) can be obtained in cases where the diagnosis of a benign vascular lesion is being considered or when better imaging of the vascular anatomy is needed for diagnosis (see below) or surgical planning. The choice often depends on availability and local experience. In general CTA has higher spatial resolution and lower cost compared to MRA. It also can be performed quickly (typically 5–10 min compared to 30–60 min). Radiation exposure is a concern in the trunk and proximal extremities, especially in women, children, and adolescents, but negligible in the distal extremities.

FDG PET/CT 18

F‐fluorodeoxyglucose positron emission tomography/computed tomography (FDG PET/CT) provides an additional dimension to oncologic imaging by combining the anatomical detail of CT with the ability to assess metabolic activity by FDG PET imaging. The principle of FDG PET imaging is based on the theory that malignant tissues tend to have high metabolic activity and accumulate FDG to a greater degree compared to most normal soft tissues [2,3]. FDG PET/CT is most often performed from either the skull base through the proximal thighs or from the cranial vertex through the feet and has the ability to characterize the primary lesion as well as assess for additional sites of malignancy. The intensity of FDG uptake can be assessed semiquantitatively by measurements of standard uptake value (SUV), most often in the form of maximum SUV. PET/CT has become widely utilized in evaluation of many types of malignancy, although its role in the setting of soft tissue sarcomas is less clear. FDG/PET does have the ability to differentiate benign tumors from high‐grade soft tissue sarcomas, but cannot reliably distinguish benign tumors from low‐ or intermediate‐grade sarcomas [4–6]. For this reason, FDG PET/CT is not routinely utilized for evaluation of indeterminate soft tissue masses. Most soft tissue sarcomas are FDG‐avid, but uptake can be variable. For example, myxoid liposarcomas, are typically non‐FDG avid (Fig. 5A and B). While the degree of uptake has not been consistently shown to correlate with the histologic grade of soft tissue sarcomas, FDG PET has been shown to be helpful in guiding biopsy [7]. The degree of FDG‐avidity has also been shown to correlate with clinical outcomes, including overall and recurrence‐free survival [8,9], and patients with localized extremity soft‐tissue sarcomas with a maximum SUV of 6 have been found to be at a significantly higher risk for recurrence compared to patients with a maximum SUV of

Contemporary imaging of soft tissue sarcomas.

Imaging plays an important role in the diagnosis, biopsy, staging, and follow-up of patients with soft tissue sarcomas. General principles of imaging ...
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