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Imaging to Assess Perineural Spread

Tumor extent along the peripheral nerve stroma (neural sheath) - via endoneurium, perineurium, or perineural lymphatics - is defined as perineural spread. Although this process occurs more frequently in a centripetal direction, toward the skull base foramina, perineural spread can extend along the opposite direction (i.e., centrifugal).

Perineural spread should not be confused with perineural invasion, which is the microscopic demonstration of tumor cells surrounding very small nerves branches, namely a process beyond detectability of radiologic imaging techniques, which is associated with increased risk of local recurrence and decreased survival when a major nerve is involved.

Though adenoid cystic carcinoma is very frequently associated with perineural spread, other malignant neoplasms of the head and neck may show this pattern of growth. Among them are squamous cell carcinomas arising from either the skin or the mucosal epithelium, desmoplastic melanoma of the skin, lymphoma, and virtually any salivary gland carcinoma.

The frequency of perineural spread in adenoid cystic carcinoma is highly variable in the different series reported in literature (15-60%) (VrielincK et al. 1988; Yousem et al. 2000). It is important to note that neurological signs and symptoms (dull pain, paresthesia) are not a reliable clue for early diagnosis of perineural spread. In fact, asymptomatic patients may account for up to 30-45% (Sur et al. 1997; Caldemeyer et al. 1998; Tomura et al. 1999). Moreover, tumor size or histological subtype should not be considered predictors of perineural extension as already observed by van der Wal et al. (1990). As a result, imaging plays a prominent role in the detection of subclinical spread of adenoid cystic carcinoma along nerve structures.

A key issue to improve perineural spread detection with imaging consists in selecting technical parameters that maximize both spatial and contrast resolution. While on CT few parameters have to be tailored to this purpose - as the choice of small FOV, thin slices (1-3 mm) and high-resolution bone algorithm - more variations are possible on MR. Apart from increasing spatial resolution similarly to CT (small FOV and thin slices), improved contrast resolution is strongly recommended, particularly by mean of fat-saturated T1 sequences after contrast agent administration. In our experience, 3D VIBE sequences provide an excellent solution by obtaining high resolution fat-saturated images in an acceptable study time.

On this sequence, the normal nerve is hypoin-tense, clearly detectable where it is surrounded by enhanced venous plexus, for example along bony grooves and canals - like the inferior alveolar nerve within the mandibular canal, the vidian, maxillary and mandibular nerves through respective foramina, or the hypoglossal nerve at the condylar canal. In addition, the enhanced hyperintense pterygoid plexus helps in identifying the branching of the hypointense mandibular nerve into its major trunks, outside the skull base foramina (Fig. 9.20).

The purpose of high resolution MR imaging is to demonstrate even subtle signal changes of the nerve itself and/or to detect asymmetric thickening of the enhanced signal surrounding the nerve.

In fact, at histology perineural spread is characterized by a chain of events that MR enables to detect earlier than CT. The progressive accumulation of neoplastic cells around a nerve leads to an increase of its diameter, more frequently segmental. A further step consists in the destruction of the blood-nerve barrier: when this occurs, extravasation of contrast material may be observed, resulting in asymmetric nerve enhancement. In most cases these changes are beneath the threshold of CT detection. As the nerve enlarges, foramina/fissures through which it courses are remodeled, widened and, finally, eroded (CurtiN et al. 1985; Woodruff et al. 1986; Curtin 1998). Therefore CT findings of perineural spread include widening/erosion of foramina/canals and asymmetric enhancement within the same foramina/canals (Fig. 9.21, 9.22). Also in this setting MR is superior to CT, as it enables to detect the neoplastic infiltration of medullary bone (Fig. 9.19).

Once tumor cells invade the perineural spaces, they can grow either along a centrifugal direction (to the periphery) or centripetally (towards skull base, Meckel's cave, and cavernous sinus) (Vrielinck et al. 1988). On enhanced SE T1 and CT images, this is reflected by the replacement of the fluid signal of Meckel's cave by solid and enhancing tissue and by the increase of the convexity of the lateral border of cavernous sinus.

Chronic atrophy of masticator, tongue or oral floor muscles should be considered an indirect sign of perineural spread: in such cases CT and T1 weighted images show degeneration of denervated muscles, in which muscular tissue has been variably replaced by fat tissue (Fig. 9.23). Also acute and subacute dener-vation changes are detectable by MR (Fischbein et al. 2001). They can be suspected in the presence of hyperintense T2 signal, abnormal contrast enhancement and increased muscular size, which is secondary to expansion of the extracellular space. As far as the process progresses to a chronic state, key findings of denervation are represented by fatty replacement and volume loss of the muscle.

Two factors may be advocated to explain MR false negative results, namely the presence of skip lesions and the resurfacing phenomenon (Ginsberg et al. 1996; Ginsberg 1999; Rice 1999; Ginsberg 2002).

Fig. 9.20a-e. Adenoid cystic carcinoma of right maxillary sinus. Five different axial levels from enhanced VIBE sequence, isotropic voxels of .5 mm. The inferior alveolar nerve is demonstrated (black arrow) as an oval hypointense structure surrounded by an enhanced venous pterygoid plexus. Two other branches of the mandibular are shown below the foramen ovale (arrowheads). Hypoglossal nerve (white arrows)

Asymmetric Pterygoid Venous Plexus

Fig. 9.20a-e. Adenoid cystic carcinoma of right maxillary sinus. Five different axial levels from enhanced VIBE sequence, isotropic voxels of .5 mm. The inferior alveolar nerve is demonstrated (black arrow) as an oval hypointense structure surrounded by an enhanced venous pterygoid plexus. Two other branches of the mandibular are shown below the foramen ovale (arrowheads). Hypoglossal nerve (white arrows)

Actually, microscopic tumor nests along the course of a nerve are undetected because below the threshold of MR imaging (Parker and Harnsberger 1991; Caldemeyer et al. 1998). Therefore, MR may show a discontinuity of perineural spread along the course of a nerve (skip lesions) as well as resurfacing of tumor immediately distal to a foramen or canal (resurfacing phenomenon). The last is secondary to compression of nerve and perineural tumor by the surrounding bone. For these reasons, nerve structures should be carefully scrutinized, both at preoperative MR and during surgery, along their entire course to decrease the risk of underestimation of tumor extension (Maroldi et al. 1999).

Fat Pads Along The Collar Bone Adenoid Cystic Pterygopalatine Fossa

Fig. 9.21a-c. Adenoid cystic carcinoma of right maxillary sinus. Same case as Fig. 9.20. a From right maxillary sinus the adenoid cystic carcinoma extends into fat tissue of masticator space (1), buccal fat pad and premaxillary tissue (2). Posterior invasion leads to involvement of both pterygoid muscles (3). The tumor spreads into the pterygopalatine fossa replacing fat tissue (black arrowhead); while on left side both fat and vessels are clearly shown within the fossa (white arrowhead). Enhancing tumor with plaque-like shape spreading into the nasopharynx is also present (4). b Tumor extends into the upper pterygopalatine fossa (asterisk), from which it spreads along the vidian (1) and maxillary nerves (2). Replacement of the liquid signal of the right Meckel cave indicates perineural extent reaching the trigeminal ganglion (3). Bone marrow enhancement within the right pterygoid process suggests possible permeative invasion. Laterally the adenoid cystic carcinoma invades the masticator space (arrowheads). c The neoplasm extends into the orbital apex (black arrowheads), and onto the orbital (white arrowheads) and the intracranial (white arrows) surfaces of the greater sphenoid wing c

In addition, false positive MR findings may occur when nerve enhancement is detected. Actually, the blood-nerve barrier may be disrupted in several conditions such as inflammation (this may hamper postsurgical and post-RT evaluation), demyelination, axonal degeneration, ischemia and trauma (Nemzek et al. 1998).

Beyond identifying the presence of perineural spread, MR is also expected to provide a precise map of all neural structures involved in each patient. Nemzek et al. (1998) obtained an accuracy of 63% for the complete mapping of perineural spread. In their series MR underestimation was in most cases related to the presence of skip lesions.

Adenoid Cystic Carcinoma Hard Palate

Fig. 9.22a-d. Adenoid cystic carcinoma of right maxillary sinus. Same case as Figs. 9.20 and 9.21. a Coronal VIBE shows invasion of right hard palate, lateral extent into the buccinator muscle insertion (1). Subperiosteal intraorbital invasion lateral to the infraorbital nerve appears as a round soft tissue mass (2). The intraorbital component reaches the apex (arrowheads on b). Enhancement along the greater wing of the sphenoid is present (3). c Perineural spread along maxillary nerve (4) and vidian nerve (5) and in the inferior portion of cavernous sinus (6). Abnormal enhancement of the pterygoid process (7). Tumor spreads into Meckel cave (8), and cavernous sinus, which shows a more convex lateral outline. Abnormal signal of the third cranial nerve is also present (9)

Fig. 9.22a-d. Adenoid cystic carcinoma of right maxillary sinus. Same case as Figs. 9.20 and 9.21. a Coronal VIBE shows invasion of right hard palate, lateral extent into the buccinator muscle insertion (1). Subperiosteal intraorbital invasion lateral to the infraorbital nerve appears as a round soft tissue mass (2). The intraorbital component reaches the apex (arrowheads on b). Enhancement along the greater wing of the sphenoid is present (3). c Perineural spread along maxillary nerve (4) and vidian nerve (5) and in the inferior portion of cavernous sinus (6). Abnormal enhancement of the pterygoid process (7). Tumor spreads into Meckel cave (8), and cavernous sinus, which shows a more convex lateral outline. Abnormal signal of the third cranial nerve is also present (9)

Abnormal SinusCancer Hard Palate Pictures

Fig. 9.23a-f. Adenoid cystic carcinoma of left hard palate invading the maxillary sinus. The young patient complained of left face paresthesias for about one year. a-b Plain CT and enhanced axial MR obtained at the level of the hard palate show permeative erosion of the pterygoid laminae (arrowheads on CT, black arrows on MR). The epicenter of tumor is located at the inferior portion of the pterygopalatine fossa (asterisk). a On CT, enlargement and subtle erosion of the opening of the greater palatine canal is demonstrated (white arrow). b Enhancement along the medial maxillary sinus wall indicates invasion on MR (arrowheads). Tumor reaches the nasopharynx (white arrow). Atrophy of masticator muscles is present. Masseter muscle (m); lateral pterygoid muscle (lp). c At the level of the upper pterygopalatine fossa, a more extensive erosion of its bony boundaries is present with destruction of the vertical lamina of the palatine bone (white arrow), and of the pterygoid process (black arrows). d-f Surgery proved perineural spread along left maxillary nerve (V2), ophthalmic nerve (VI), and mandibular nerve (V3)

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