Interventional radiologic techniques in the management of bone tumors

Introduction

As recently as 30 years ago the principle role of radiology in the management of bone tumors was almost exclusively diagnostic. A wide variety of new techniques have since been developed which allow radiologists to contribute to the management of bone tumors. These facilitate not only diagnosis but treatment of lesions, often replacing or supplementing other methods.

This review is divided into four sections. The first will be on image-guided bone biopsy. In many institutions virtually all bone biopsies are done under imaging guidance either with computed tomography (CT) or fluoroscopy, and less frequently magnetic resonance imaging (MRI) or ultrasound.

The second section is on therapeutic embolization. This is an important adjunct in facilitating complex and difficult surgery by minimizing the profuse bleeding that would otherwise occur. Embolization is also invaluable in palliating patients with lesions that are unresponsive or unavailable to other conventional techniques such as chemotherapy, radiation therapy, or surgery, either alone or in combination.

The third segment is dedicated to thermal ablation techniques used for bone tumor therapy or palliation.

In the last section we give an overview on vertebroplasty and osteoplasty, which particularly in the last 15 years has provided a new avenue for providing high-quality palliation of patients with difficult-to-treat destructive lesions of the spine and pelvis.

Image-guided bone biopsy

The first reported core biopsy of bone was performed by Ellis in 1947 [ ]. The first image-guided bone biopsies were carried out with the help of radiographs only and real-time, fluoroscopy-guided bone biopsy was subsequently introduced in the 1960s [ ]. Since then, with the accumulation of experience by radiologists, the improvement in biopsy needles and techniques, and the development of CT and MRI, image-guided bone biopsy has replaced open surgical biopsy as the method of choice for evaluating bone lesions [ , ].

Image-guided percutaneous bone biopsy has several advantages. It can be performed as an outpatient procedure under local anesthesia with or without conscious sedation, is straightforward in experienced hands, safe, cost-effective, and has a low complication rate [ , ].

The indications for percutaneous bone biopsy are:

• Lesion of unknown etiology

• Suspected metastatic lesion in patient with known primary malignancy elsewhere

• For diagnosis and sensitivities in suspected infections

• Symptomatic vertebral compression fracture when unclear if etiology is osteoporotic or neoplastic

• Cytogenetic evaluation of bone and soft-tissue tumors, which have seen recent rapid advances [ ]

The most commonly reported indication is metastatic bone disease [ ]. The current widespread use of CT, MRI, and positron emission tomography (PET) has led to a huge increase in the number of ambiguous bone lesions identified during the staging of tumors elsewhere, or as incidental findings on imaging. As a result, the demand for bone biopsy is steadily rising [ , ].

Contraindications to biopsy include inaccessible sites such as C1 and the odontoid process of C2, where the planned access route would traverse infected skin or soft-tissue, and an uncooperative patient [ ]. A bleeding diathesis has to be excluded as a postprocedural hematoma can cause unresectable spread of disease. A relative contraindication is a suspected hypervascular metastasis (such as hepatocellular carcinoma) in the spine; hemorrhage from such lesions may lead to cord compression and an open biopsy may be preferable [ ].

Every solitary bone lesion that requires a biopsy has to be regarded a potential malignancy. Biopsies of these lesions should only be performed in a center where there is multidisciplinary cooperation between the radiologist and surgical oncologist responsible for resection of the lesion [ ]. Compared to malignancies in other body parts it is unique in bone tumors that the biopsy tract is usually resected with the tumor due to a supposed risk of seeding the tract. However, the evidence for this is scant [ ]. It may be that using a percutaneous coaxial approach may eliminate the risk entirely. Nonetheless, in the absence of good data, we continue to advocate widely accepted principles [ ]. The biopsy needle path must be in the same location as the surgeon's planned incision for resection, so that the biopsy tract can be removed with the tumor; the shortest approach may not be ideal. If the needle traverses an uninvolved anatomical compartment or joint, a more radical resection or amputation may become necessary in an extremity that would otherwise be amenable to limb-sparing surgery [ ]. In one large series of sarcoma patients, the optimum treatment plan was compromised in 18% of cases due to poor technique, leading to unnecessary amputation in 5% [ ].

Prior to the procedure, any available imaging must be reviewed by the radiologist who will perform the biopsy [ ]. Additional imaging may be indicated. For instance, where multiple lesions are suspected, a radionuclide bone scan may identify a lesion which is easier and safer to biopsy [ ]. A PET scan can identify viable tumor in necrotic or sclerotic lesions, helping to guide the biopsy. If an MRI scan is required, this must be performed before the biopsy, to prevent the biopsy itself affecting the scan, for example, due to reactive edema or hemorrhage.

Percutaneous bone biopsy may be performed under ultrasound, fluoroscopy, CT, MRI, or CT fluoroscopy guidance. While ultrasound has the advantage of being fast, inexpensive, and free of ionizing radiation, it has limited use in bone biopsies unless there is complete cortical destruction with extension of a lytic tumor into soft tissues [ , ]. Like ultrasound, fluoroscopic guidance allows real-time imaging of the biopsy needle as it is advanced into the lesion. However, it is difficult to assess the depth of the needle unless biplane fluoroscopy is used, and it does not allow visualization of soft-tissue abnormalities. Therefore, it is generally limited to superficial, easily visible lesions or biopsies of spinal tumors when performed as a component of a vertebroplasty procedure. MRI-guided biopsy is not widely available; however, the available literature suggests that it is a safe and accurate alternative [ ]. The main advantages over CT-guided biopsy are the absence of ionizing radiation, the ability to see lesions that are invisible on other imaging modalities (e.g., edematous marrow lesions), and better contrast resolution without intravenous contrast medium [ , ]. A considerable disadvantage is its cost, as MRI-compatible needles and instruments remain relatively expensive, and MRI scanner time availability. In addition, the materials used in the biopsy needles are softer and blunter than the standard stainless steel equipment, making sampling of sclerotic lesions more difficult [ ]. CT fluoroscopy combines the real-time capabilities of fluoroscopy with the contrast resolution and depth information provided by CT, with recent advances in equipment demonstrating reduced radiation dose to the patient and comparable accuracy to CT [ , ].

Currently, CT guidance remains the technique of choice for percutaneous bone biopsy [ ]. Almost every part of the skeleton can be reached [ ]. It retains superior spatial resolution to MRI [ ], is relatively cheap [ ], and biopsies typically take less than 1 hour to perform. It is widely available, reliable, and accurate [ ].

Depending upon the location, size, and appearance of the lesion, fine-needle aspiration (FNA) or core biopsy may be performed. FNA can be carried out using a spinal or Chiba needle, usually with a cytotechnologist being present for evaluating sample quality. While exact tissue diagnosis is difficult with FNA, cytological classification into benign, low-grade, and malignant lesions shows high sensitivity and specificity [ ]. Especially for bone lesions with typical radiological features FNA can help establish a diagnosis without the need of open biopsy [ ]. For the diagnosis of metastatic disease and infection FNA is usually sufficient, whereas core needle biopsies are preferred for assessing the lesion's architecture, cell type, and histologic grade, which are needed for assessment of a primary bone malignancy [ ].

There are a variety of commercially available core biopsy needles for use in bone lesions (e.g., Osteo-Site, IZI Medical, Owings Mills, Maryland, USA). Bone penetration sets utilizing a coaxially inserted drill for penetration of the cortex with specifically adjusted trephine-type biopsy needles are also available and have high popularity in the literature (Arrow OnControl, Teleflex, North Carolina, USA) [ , ]. Additionally, when a lytic bone lesion is encountered, a soft-tissue spring-loaded side-cutting core biopsy needle (e.g., Tru-cut spring-loaded biopsy gun, Baxter Healthcare Corp., Deerfield, Illinois, USA) may be useful. When a lytic lesion is surrounded by intact cortex, a combined approach can be performed, using an 11G or 13G bone biopsy needle to make a window through the cortex through which a 14G or 16G Tru-cut needle can be inserted coaxially for sampling of the soft-tissue component [ , ]. A large gauge is preferable in these situations to maximize core size, as maneuverability is restricted when anchored in bone.

CT-guided bone biopsy is an extremely safe procedure, with reported complication rates ranging from 0% to 7.4% [ ]; complications requiring treatment are more frequent following spine biopsy [ ]. The most commonly encountered complications are outlined in Table 55.1 [ ]. Apparent neurologic injury following biopsy is most commonly related to the infiltration of local anesthetic, and resolves spontaneously within 3–4 h. Permanent injury to nerves, nerve roots, or the spinal cord is relatively uncommon but is more likely to be encountered during biopsy of spinal lesions. Thoracic spine biopsy is the most prone to complications such as pneumothorax, cerebrospinal fluid leak from a thecal sac laceration, and paraplegia [ ]. Fracture is an uncommon but well-documented risk following bone biopsy, particularly in weight-bearing bones like the femur ( Fig. 55.4 ), and should be discussed with the patient when obtaining consent.

The diagnostic accuracy of CT-guided bone biopsy, which is defined as the proportion of cases in which the biopsy diagnosis is in concordance with the clinicopathological diagnosis, has been reported to vary from 74% to 96% [ , , , ]. Similar accuracies have been reported with MRI-guided bone biopsies [ ]. The most commonly reported reason for an inaccurate image-guided biopsy is failure to obtain sufficient tissue for analysis [ ]. Other reasons include sampling of necrotic areas within a tumor, sampling of the lower-grade component of a heterogeneous tumor [ , ], or crushed sample [ ]. To avoid this, biopsies should be obtained from several different areas within a lesion. Where possible, the outer margins of the tumor should be biopsied, with central areas avoided due to the possibility of necrotic tissue yielding a nondiagnostic sample [ , ]. Another factor negatively affecting the success of a biopsy is when lesions are benign or low grade [ ]. An experienced pathologist is necessary for interpretation of the samples as nonaggressive lesions like stress fractures can imitate a malignant appearance histologically.

When imaging-guided percutaneous biopsy has been performed by an experienced team but is nondiagnostic, repeat percutaneous biopsy is of limited use. A low threshold for proceeding to open biopsy is recommended [ , ].

Technique

Informed consent is obtained from the patient, including an explanation of the small risks of hemorrhage, infection, tumor seeding, and fracture. Location-specific risks like pneumothorax for rib and spine lesions should be addressed. The potential need for a repeat percutaneous or open biopsy is also discussed. The biopsy is planned with the surgeon who will be performing the resection, ensuring that uninvolved compartments are not traversed while also checking that the proposed path is free of major vessels, nerves, pleura and peritoneum. In the authors' experience, conscious sedation is usually adequate and well tolerated, even when deep or painful lesions are being biopsied. The patient is positioned appropriately on the CT table with proper fixation of the biopsy site to inhibit involuntary motion and a metal marker taped to the skin. A preliminary scan is performed; the appropriate slice selected and marked using the laser guidance of the CT gantry. The distance from the skin marker to the bone lesion is measured and the angle at which the needle will have to be introduced is estimated. The skin and subcutaneous tissues are infiltrated with 1% lidocaine with a 25G needle. A small number of CT slices are performed at this site to check the position and angle of the needle. Some CT scanners have the ability to perform a gantry tilt, which may be helpful in aligning the tract to the gantry where the path is less axially aligned. Then the periosteum is infiltrated, if necessary with a longer needle, and preferably with a longer duration local anesthetic such as bupivacaine. This minimizes the discomfort the patient will feel during penetration of the cortex and reduces the chance of patient motion during the procedure. An incision is made in the skin; while this need only be large enough to allow the needle to be inserted, we routinely make this at least 5 mm so that the scar from the biopsy is unambiguous when the surgeon performs the definitive resection. A coaxial needle guide is inserted along the same path as the anesthetic needle and anchored in the cortex of the bone. Through this, the bone biopsy needle is introduced and either manually pushed through the cortex, especially if the cortex has been pathologically thinned, or drilled into the lesion ( Fig. 55.1 ). Multiple cores are obtained; different regions of the tumor can be sampled without repositioning the needle by making slight changes to the angle of the outer needle guide. In very dense sclerotic lesions often the first sample is the best, as on subsequent biopsies the biopsy needle always follows the previous needle track. If using a drill, it is recommended to take multiple small bony cores of 2–3 mm as the heating effect or impaction from the drill could burn or crush samples. When dealing with a predominantly lytic lesion, samples are obtained with soft-tissue biopsy needles (Tru-cut) once any overlying cortex has been penetrated ( Fig. 55.2 ).

The procedure is similar whether extremity or spinal lesions are being biopsied. Several approaches have been described for biopsy of vertebral tumors [ , , ]. In the lower cervical spine and the thoracic spine, a posterolateral or transpedicular approach can be used. In the lumbar spine, a lateral approach is also feasible ( Fig. 55.3 ). For upper cervical spine lesions, transoral or transpharyngeal access is necessary. If a disc sample is required, an inferior approach may be helpful in reducing the angle required .

Therapeutic embolization

Embolization is the intentional fluoroscopic-guided, transcatheter occlusion of blood vessels. Early attempts at applying this principle predate the discovery of X-rays. As far back as 1831, physicians placed large needles into aneurysms in an attempt to induce thrombosis [ ]. Most of the pioneering work on modern techniques of catheter-directed embolization was carried out by neuroradiologists with a landmark achievement by Lussenhop and Spence who successfully occluded a cerebral arteriovenous malformation under radiographic guidance [ ]. Technical advancements in recent years have increased the potential for safe and effective treatment of life-threatening hemorrhage with an endovascular approach [ ]. In addition, the application of this endovascular therapy can be extended to nearly every organ system with a vascular abnormality or tumor.

The earliest report of embolization of hypervascular bone tumors was described by Feldman et al. [ ]. Hypervascular metastatic disease is the commonest bone abnormality to be managed using embolization. Embolization is used when reducing blood supply has a therapeutic or adjuvant affect.