4 Neoplastic Invasion of Bone, the Orbit and Dural Layers: Basic and Advanced CT and MR Findings

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4 Neoplastic Invasion of Bone, the Orbit and Dural Layers: Basic and Advanced CT and MR Findings

Roberto Maroldi, Davide Farina, Giuseppe Battaglia

R. Maroldi, MD

Professor, Department of Radiology, University of Brescia, Piazzale Spedali Civili 1, Brescia, BS, 25123, Italy

D. Farina, MD; G. Battaglia, MD

Department of Radiology, University of Brescia, Piazzale Spedali Civili 1, Brescia, BS, 25123, Italy

4.1

Introduction

In the sinonasal area several thick or thinner bony laminae divide the nasal cavity and paranasal sinuses from the orbit and the brain. These bone structures act as a barrier against tumor spread.

Conventional radiology and CT obtained ﬁ ndings suggesting bone invasion upon changes of the normal appearance of these interfaces (Som and Shugar 1980; Som et al. 1991; Lloyd et al. 2000). However, the single absence (lysis) of the mineral content of the lamina papyracea per se does not correctly predict, for example, orbital invasion at CT.

In fact, it is well known that the most effective barrier to the spread of neoplastic or inﬂ ammatory aggressive lesions beyond sinusal walls is the periosteum rather than the mineralized bony wall (Kimmelman and Korovin 1988). Therefore, neoplastic extent be-

yond the periosteum of the sinusal walls is critical for therapeutic planning.

Nevertheless, the limitation of CT in assessing the presence of a residual demineralized barrier (the periosteum) does not necessarily apply to MR.

In fact, though the mineral content does not give up signal on MR, the cortical bone – its periosteal covering included – can be adequately demonstrated using high resolution matrix and thin vox- els, because it appears as a homogeneous hypointense structure (Som et al. 1987) (Fig. 4.1).

This signal actually results from the sum of both cortical bone and its investing thin ﬁ brous periosteal layers. It can be recognized on MR independently of the degree of bone mineralization (Maroldi et al.

1996).

For all these reasons, the information provided by imaging should not simply regard the state of the mineralized wall, but it should be refocused on assessing the normality of the periosteum lining the bony “box.”

In addition, the bony interfaces between the sinonasal cavities and brain have a more complex structure, because the intracranial surface of these bones is covered by a specialized connective layer:

the dura mater. Like the periosteum, this layer prevents intra-cranial invasion by neoplasms or aggressive inﬂ ammatory lesions. The dura mater differs from the periosteum because in most cases it reacts in front of the advancing lesion by signiﬁ - cantly increasing its thickness and vascularization (Eisen et al. 1996).

As a result, the assessment of the relationships between tumor and the adjacent bony walls – lined by periosteum or by the dura – will include basic (regular vs. irregular demineralization) and more advanced ﬁ ndings (demonstration of the periosteum, changes of the dura mater layer).

As both focal invasion and the simple contact between tumor and the periosteum/dura mater layer signifi cantly infl uence the treatment planning, the meticulous assessment of these fi ndings is a relevant part of the imaging work up.

CONTENTS

4.1 Introduction 35

4.2 Patterns of Bone Invasion on CT and MR 36 4.2.1 Bone Remodeling 36

4.2.2 Cortical Destruction 37

4.2.3 Intra-diploic/Medullary Growth 37 4.2.4 Permeative Invasion 37

4.2.5 Sclerosis 38

4.3 CT and MR Findings of Orbital Invasion 39 4.4 CT and MR Findings of Skull Base and

Dura Mater Invasion 42 References 46

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4.2

Patterns of Bone Invasion on CT and MR

In the sinonasal area, the bone framework is com- posed not only of thin laminae (as the lamina papyracea or the lamina cribrosa) but also of thick osseous structures as the zygomatic bone or the pterygoid process and the great wing of the sphenoid.

The interaction between thin laminae or thick medullary bones and lesions with variable degrees of aggressiveness results in four patterns of bone changes.

4.2.1

Bone Remodeling

Bone remodeling consists of displacement and – usually – thinning of bony walls. In most cases, it is observed in tumors contacting very thin walls as cribriform plate, lamina papyracea, turbinates, and medial maxillary sinus wall. Bone remodeling is a continu- ously occurring adaptive dynamic process involving both osteoblasts and osteoclasts (Giacchi et al. 2001).

Activation of this process is triggered by mechanical stress – exerted by expansile lesions – as well as by chemical mediators – released in both infectious and non-infectious inﬂ ammatory conditions. Bone remodeling is a sort of balance between the activity of osteoblasts and osteoclasts. As a result, thinning and displacement of subtle bone structures may be observed mixed with sclerosis of thicker sinusal walls.

The high spatial and contrast resolution of CT en- ables the detection of even subtle abnormalities in

the mineral content of the remodeled bone (Som and Shugar 1980) (Fig. 4.2). Whereas demineralization of thin cortical interfaces cannot be detected by MR, wall displacement and integrity of the periosteum may be demonstrated on condition that the wall does not contact air on one of its surfaces (Maroldi et al.

1996) (Fig. 4.1).

Basically, in normal sinuses there are two different physiological and anatomic conditions: air on one side, fat/ﬂ uid on the opposite one (lamina papyracea and orbital fat, cribriform plate and CSF); air on both sides (medial maxillary sinus wall).

In the ﬁ rst condition, the displaced and demineralized medial orbital wall or cribriform plate – with

Fig. 4.2. Bone remodeling of the posterolateral (black arrows), anterior, and medial maxillary sinus wall in an inverted papil- loma. White arrows point to demineralization of the inferior concha.

Fig. 4.1a,b. Coronal CT and TSE T2 MR of right ethmoid inverted papilloma. Moderate lateral displacement and reabsorption of the lamina papyracea (1) well detectable on MR image because of replacement of the air content within the ethmoid cells by thickened mucosa and tumor. Thinning of the fovea ethmoidalis (2) is correctly shown by the two techniques. Laterally, the orbital plate of the frontal bone (3) appears completely demineralized, its border undetectable. On MR, a thin hypointense line suggests that the lesion is still conﬁ ned by the periosteal/dural interface. Similarly, the thin lamella reaching the anterior ethmoid canal (arrowhead) and part of the medial maxillary sinus wall (4) are better shown by MR. Middle left concha (5)

a b

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their periosteal layers – can be detected by MR as hypointense (absent) linear signals enclosed in a sort of sandwich between the lesion (on one side) and the orbital fat and CSF (or dura and subarachnoid spaces), respectively, on the other side (Ishida et al. 2002) (Fig. 4.3). Of course, the proper frequency encoding direction has to be selected in order to avoid asym- metric appearance of cortical bone due to chemical shift artifact (Dick et al. 1988).

In the second condition, remodeling of the medial maxillary sinus wall or of the sphenoid sinus fl oor may be shown by MR if a suffi ciently thick mucosal layer invests the opposite surface or retained secre- tions fi ll the sinus (Maroldi et al. 1996).

The bone remodeling pattern can be observed in benign neoplasms and in some chronic inﬂ ammatory lesions as the mucocele and polyposis, less frequently in malignant neoplasms.

plasms as inverted papilloma and juvenile angioﬁ - broma and in malignant tumors (Som et al. 1991) (Fig. 4.4).

Fig. 4.3. Adenocarcinoma of the ethmoid, TSE T2 sequence.

Even if the lamina papyracea is laterally displaced, a continuous sharp hypointense interface separates the orbital fat from the mass (black arrows), indicating absence of periorbital pen- etration. The horizontal (white arrow) and lateral (vertical) cribriform plate are demonstrated because tumor and mucous ﬁ lling the frontal sinus contact the bone from below

4.2.2

Cortical Destruction

Cortical destruction is detected at CT as a break of the mineralized bone through its whole thickness, whereas on MR a defect of the continuous hypointense thickness of the cortex, replaced by solid tissue, implies invasion also of the periosteum (Maroldi et al. 1996). It can be observed in aggressive inﬂ ammatory lesions (both non-invasive and invasive fungal rhinosinusitis), some benign, but aggressive, neo-

Fig. 4.4. Squamous cell carcinoma of the left maxillary sinus.

Irregular destruction of the posterolateral wall (1). Tumor spreads into the fat content of the infratemporal fossa and inferior orbital ﬁ ssure (2). Arrowheads indicate the extent into the inferior limit of the superior orbital ﬁ ssure. Sclerotic changes of the alveolar process (3)

4.2.3

Intra-diploic/Medullary Growth

Intra-diploic/medullary growth relates to the char- acteristic path of intra-osseous spread demonstrated by malignant tumors and the juvenile angioﬁ broma (Fig. 4.5). The density and signal of the spongiosa is replaced by solid tissue characterized by trabecular destruction on plain CT and fat replacement on MR (Lloyd et al. 1999). This intra-osseous tissue usually enhances like the primitive tumor mass. For instance, the typical high enhancement of juvenile angioﬁ broma can be detected within the diploe (Fig. 4.6).

4.2.4

Permeative Invasion

Permeative invasion with or without sclerosis is a pe- culiar pattern observed mostly in lymphomas and in adenoid cystic carcinoma (Suei et al. 1994; Yasumoto et al. 2000). In this pattern, the most relevant ﬁ nding is the extensive replacement of the medullary bone even in the absence of evident cortical erosion.

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In this setting, a very subtle moth-eaten appearance of the hypointense cortical/periosteal lining can be detected only if proper CT and MR techniques are used. This model of sub-periosteal spread can be missed on plain and enhanced CT, particularly in adenoid cystic carcinomas, because only faint areas of denser spongious bone may be present. Conversely, MR is more sensitive because it combines the information provided by different sequences: on both T2 and plain T1, the fat tissue is replaced by hypointense signal; moreover, non homogeneous areas of enhancement can be demonstrated after contrast ap- plication, more evident when the fat-sat technique is applied (Fig. 4.7).

4.2.5 Sclerosis

Sclerosis is characterized on MR by the above-mentioned changes on T2 and plain T1 sequences, usually without any contrast enhancement. Extensive sclerosis can be, of course, obvious on CT (Fig. 4.5). This is a chronic inﬂ ammatory reaction of the spongiosa

Fig. 4.6. Persistent juvenile angioﬁ broma. In the GE Gd-en- hanced coronal image, the persistent lesion replaces the med- ullary bone of the greater wing of the right sphenoid (white arrows), and projects into the sphenoid sinus, the superior orbital ﬁ ssure, and into the choana (black arrows). Foramen rotundum (FR), pterygoid (vidian) canal (VC)

Fig. 4.5a–d. Recurrent myxosarcoma.

TSE T2 (a), plain CT (b), enhanced T1 (c), and enhanced CT (d). Intraspongiotic spread within the greater wing, pterygoid process, lateral sinus wall and ﬂ oor of the left sphenoid bone. Whereas plain CT shows lysis of cortical and diploic mineral content of the bone, TSE T2 demonstrates a hypointense interface (1) still separating the tumor from the subarachnoid spaces, indicating that the lesion is conﬁ ned to the dura. Neoplastic erosion extends into the lateral portion of the greater wing (opposite arrows).

Because of sclerotic changes, the medullary bone within the intersinusal sphenoid septum and the residual sphenoid sinus ﬂ oor is more hypointense on TSE T2 and enhanced T1 (2) than the ad- jacent pterygoid process (4). Residual pterygoid canal content (3), internal carotid artery (5), anterior clinoid with cortical rim and medullary content (target-like appearance) (6), maxillary nerve (7)

a

c

b

d

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present in a wide range of inﬂ ammatory and neoplastic conditions (Chang et al. 1992).

4.3

CT and MR Findings of Orbital Invasion

Most nasosinusal neoplasms invade the orbit through the ﬂ oor (maxillary sinus squamous cell

carcinomas) or the medial wall (ethmoid adeno- carcinomas). The other walls are less frequently in- volved by primitive tumors. In fact, it is more likely to observe this path of orbital invasion by recurrent neoplasms or metastases. Apart from the infrequent event of perineural spread along the infraorbital nerve, rarely tumors extend into the orbit through the ﬁ ssures or canals.

As both the medial wall and the orbital ﬂ oor are very thin, they are often displaced by tumors arising

Fig. 4.7a-f. MR and CT of subperiosteal bone invasion. Recurrent adenoid cystic carcinoma of the hard palate. MR sequences: TSE T2 (a), Gd-enhanced VIBE (b), plain (c) and Gd-enhanced T1 (d). Bone window CT, plain study (e), enhanced CT (f). The anterior, medial, and posterolateral walls of left maxillary sinus are invaded through subperiosteal spread. Apart from areas of focal ero- sion (1), subperiosteal spread results in rather subtle CT changes: diffuse demineralization of maxillary sinus walls, and minimal soft tissue thickening along the external surfaces of the walls (2). Conversely, MR clearly shows tumor spread on both the inner and outer surfaces of the sinus, leaving the residual walls (hypointense on all sequences) between two layers of neoplastic signal (arrowheads in b). On TSE T2, subperiosteal spread presents as a plaque-like lesion with a multilayer appearance with a double hypointense layer (neoplastic) investing both sides of the bony walls, the inner being covered by the mucosa (intermediate-to- hyperintense signal layer). This pattern is clearly shown at the medial maxillary sinus wall (arrows), where the the diffuse bulging of the mucosa on left side is due to subperiosteal/submucosal invasion. The plaque-like neoplastic layer, which is hypointense on plain T1, enhances after Gd admministration on T1 and VIBE, similarly to the mucosa. Erosion and intramedullary invasion of the left petrygoid process is also shown (3). Mandibular nerve (4). Extent into the left nasopharyngeal wall is shown (5)

a

e

b

d

f c

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in the adjacent sinuses (Fig. 4.8). Chronic pressure exerted by the mass is usually associated with thinning and demineralization of the wall or erosion.

Surgical strategy is controversial in the presence of erosion of the lamina papyracea. According to some authors this condition indicates orbital exenteration (Ketcham et al. 1973). Nevertheless, criteria deﬁ ning the indications for orbital preservation or exenteration have changed throughout the last three decades.

Recent evidence in the surgical literature supports a conservative approach even in the presence of bone erosion on condition that the periorbita is not invaded (Lund et al. 1998; Cantu et al. 2000). More re-

cently, data provided by other investigators (Tiwari et al. 2000 Imola and Schramm 2002; ) advocate more advanced criteria for orbital preservation. An additional distinct fascial layer surrounding the periocular fat and separating it from the periorbita has been reported by Tiwari et al. (1998). Invasion of the fascia prevents orbital preservation. In the series by Imola and Schramm (2002), full thickness periorbital invasion was treated by microscopically assisted dissection, enabling even limited removal of the orbital fat.

Thus, imaging the periorbita is crucial for CT and MR. Prediction of orbital invasion has been based on the detection of positive findings graded through progressive steps: tumor contacting the periorbita (sensitivity of CT and MR 90%); fat obliteration (positive predictive value: CT 86%, MR 80%); extraocular muscle involvement (positive predictive value of MR 100%) (Eisen et al.

2000). Overall, CT proved to be more accurate than MR. By comparison, in our series of 49 sinonasal malignancies the absence of orbital invasion has been correctly predicted in 40 orbits with tumor contacting the wall more than 10 mm of length (negative predictive value of CT 75%, MR 100%) (Maroldi et al. 1996, 1997). Detection of a hypointense/absent linear signal indicating the periorbita was the more specific predictor with overall accuracy of MR significantly better than CT (95.4% vs 81%) (Fig. 4.9–4.13).

Fig. 4.8. Adenocarcinoma of left ethmoid abutting the lamina papyracea. Mild sclerotic changes combined with focal areas of erosion are shown

Fig. 4.9a-c. Squamous cell carcinoma of left maxillary sinus. On coronal TSE T2 (a) and VIBE (b), upward displacement of the orbital ﬂ oor by the tumor is observed. A hypointense interface between the mass and the orbital fat can be recognized (long arrows). Tumor invades the middle meatus (short arrows) blocking the anterior ethmoid. Hypointense ﬂ uid (high protein con- centration) within the ethmoid bulla (asterisk). On sagittal GD-enhanced T1 (c) a hypointense interface cannot be demonstrated, only the sharp limits suggest that the lesion is limited by the periorbita

a b c

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Fig. 4.11. Adenocarcinoma of right ethmoid sinus invading the orbit (arrows) through the erosion of the lamina papyracea and lacrimal bone. NLD, nasolacrimal duct

Fig. 4.12a–c. Sinonasal non-Hodgkin lymphoma. Permeative pattern of invasion through the lamina papyracea (black arrows) and extent into the maxillary sinus along the bony walls (white arrows). The horizontal and lateral (vertical) lamella of the cribriform plate are well demonstrated on TSE T2 [short black arrow on (a)]. Focal dural enhancement is appreciated on (b) at the level of the orbital plate of the frontal bone (white arrow). Lacrimal sac dilatation (asterisk)

a b c

Fig. 4.10a-d. Spindle cell naso-ethmoid carcinoma. The hypointensity of the lamina papyracea/periorbita can be appreciated only in its anterior third (black arrowheads). In the posterior two thirds of the medial orbital wall, neoplastic spread through the lamina papyracea/periorbita (black arrows) appears as several short solid ﬁ nger-like projections into the orbital fat. An ethmoid cell wall – same thickness of the papyracea – can be adequately detected by MR (white arrowheads). Invasion of the right nasal bone (white long arrow). In the same patient as (a), TSE T2 (b), Gd-enhanced T1 (c) and VIBE (c) coronal planes show invasion of the medial orbital wall with solid - and enhancing - tissue (arrowheads) replacing the orbital fat medially to the rectus inferior muscle (1). Invasion of the lateral orbital ﬂ oor (small white arrows on b and opposite arrows on c) is also present. The signal void of the infraaorbital artery is surrounded by tumor (2). Ophthalmic artery (3), minimal dural thicken- ing at the fovea ethmoidalis (4)

a b c d

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Although preoperative imaging may aid in surgical planning, in ambiguous cases of orbital invasion the intra-operative mapping of the orbital wall, with gross examination or frozen sections, is necessary.

Orbital invasion is considered a negative prognos- tic factor, even though some authors specify that decrease in survival may reﬂ ect the wider extension of lesions invading the orbit (Shah et al. 1997).

4.4

CT and MR Findings of Skull Base and Dura Mater Invasion

Assessment of the deep extent of sinonasal tumors toward the dural layer is one of the issues that sig- niﬁ cantly inﬂ uence the treatment planning.

Like in the invasion of orbital walls, bone destruction of the skull base is better demonstrated by CT. However, here the imaging ﬁ ndings differ from those observed in the other bone interfaces of the sinonasal area because when the skull base is invaded, the dura mater usually shows abnormal thickening and enhancement that can be due either to neoplastic invasion or to inﬂ ammatory, non-neoplastic reaction.

Since dural invasion implies both a worse prog- nosis and a surgical resection not limited to the eroded bone, the goals of imaging focus on estab- lishing the depth of skull base invasion (Kraus et al. 1992b; Shah et al. 1997).

MR has been reported to be more precise than CT. Early observations emphasized the usefulness of T2 (and T1 sequences) in separating the low signal of bone from the high signal of CSF (Fig. 4.14).

Thickening and enhancement of the dura mater invaded by tumor were mentioned by Weissman and Curtin (1994). Other investigators reported that enhanced MR sequences could demonstrate leptomeningeal invasion (Volle et al. 1989; Kraus et al. 1992a). Moreover, in the series by Ishida et

Fig. 4.14. Naso-ethmoidal adenocarcinoma, intestinal-type, TSE T2. Upward displacement of the right fovea ethmoidalis (1) due to a small mucocele underneath (showing hyperin- tense signal) secondary to tumor (that shows homogeneous intermediate intensity). The tumor abuts the right medial or- bital wall, remodeled, but not invaded (2). Because of ﬂ uid retention within the contralateral posterior ethmoid cells, the papyracea/periorbita is well demonstrated (3). Opposite ar- rows point to the right residual vertical lamella of the middle concha. Olfactory tract (4)

Fig. 4.13a,b. Squamous cell carcinoma of left nasal cavity with extensive orbital inﬁ ltration. Invasion through the bony/periosteal hypointense interface of the fovea ethmoidalis (1) with mini- mal enhancement of the dural layer.

Residual vertical lamella of the middle torbinate (2)

a b

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al. (2002), as well as in our own, speciﬁ c changes in the appearance of the hypointense/absent signal of bone and the overlying dura proved to correctly predict dural invasion.

A key diagnostic observation concerns the signal intensity of the three structures located at the interface between the ethmoid roof and brain at the anterior cranial fossa: cribriform plate and its double periosteal covering, dura mater, subarachnoid space.

On enhanced sagittal and coronal MR spin echo T1 or 3D GE fat sat T1 sequences the three layers give rise to a “sandwich” of different signals (bone- periosteum complex, dura, CSF) (Ishida et al.

2002).

If a malignant sinonasal neoplasm approaches the ACF ﬂ oor, three different conditions may oc- cur: (a) the neoplasm appears in close contact with an uninterrupted, hypointense cribriform plate or fovea ethmoidalis (Fig. 4.15); (b) the neoplasm erases the hypointensity of the cribriform plate, extends into the ACF and displaces an uninterrupted, hyperintense and thickened dura (Fig. 4.16); (c)

the neoplasm encroaches the dural hyperinten- sity without erasing the hypointense signal of CSF (Fig. 4.17, 4.18); (d) the neoplasm extends beyond the dura encroaching the hypointense CSF and invades brain tissue (Fig. 4.19).

This last sign is easier to detect if the signal intensity of the neoplasm is lower than the enhanced dura surrounding the invaded segment (Maroldi et al. 1997).

Resectability of tumors invading the brain does not stand only upon the assessment by imaging of the depth of tumor extent into the brain or on the detection of bilateral brain invasion. It requires a thorough evaluation of several other issues, the most important being the histotype and patient’s performance status. Patients with limited brain invasion treated by craniofacial resection are reported to have non-signiﬁ cant decrease in survival compared to those with dural invasion only.

Contraindications to surgery other than brain invasion are considered to be the involvement of the internal carotid artery or of the cavernous sinus (Shah et al. 1997) (Fig. 4.20)

Fig. 4.15a,b. Ethmoidal adenocarcinoma, intestinal-type, plain (a) and Gd-enhanced T1 (b). The black signal of the planum eth- moidalis/fovea is continuous and regular [opposite white arrows on (a)]. Mild and uniform enhancement of the dura is detected after Gd administration [white arrows on (b)]. Invasion of medial wall and part of the ﬂ oor of the orbit (black arrows)

a b

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Fig. 4.16a–e. Naso-ethmoidal SCC, T1 after Gd administration. Intracranial invasion with dural thickening and subtotal dural inﬁ ltration. a Minimal dural thickening at the periphery of the lesion (1), normal frontal bone appearance at the orbital roof (2). Focal thickening of the dura (3) more hyperintense than the tumor’s signal (4). b No sign of dural layer trespassing at this level, bone has been eroded (black arrows). Mild dural thickening (1). c–e On the sagittal planes, bone erosion and subtotal replacement of the hyperintense signal of the focally thickened dura suggest intracranial extradural invasion. Posterior sphenoid sinus wall destruction with hypophysis invasion is present. Blockage of frontal sinus drainage is associated with mucous retention and mucosal thickening

a

c e

b

d

Fig. 4.17. Sinonasal undifferentiated carcinoma, Gd-enhanced T1. Midline invasion of the anterior cranial fossa ﬂ oor (white arrows) without dural thickening (intracranial intradural spread). No sign of brain edema. Lamino papyraces (opposite arrrows)

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Fig. 4.18a,b. Adenocarcinoma of the ethmoid sinus, Gd-enhanced T1. a Tumor and the enhanced dura have similar signal in- tensity. The thickened dura is seen investing the planum ethmoidalis posteriorly to neoplastic invasion (arrow). b Intracranial intradural spread without brain invasion (arrows)

Fig. 4.20. Recurrent SCC of the posterior ethmoid, Gd-enhanced GE coro- nal plane. Encasement of right internal carotid artery (arrows) with cav- ernous sinus invasion

a b

Fig. 4.19a,b. Recurrent adenoid cystic carcinoma, left max- illary sinus was the primary site, Gd-enhanced GE-T1 se- quences. Galea capitis (1) and temporal muscle (2) invasion.

The intracranial mass arises from spread through the greater wing of the left sphenoid [black arrows in (a)]. Intracranial intradural spread exhibits a mushroom-like appearance.

Double layer enhancement along the inner surface of the temporal and parietal bones (3) may be correlated to dural spread (it does not extend into the sulci), the more hyperintense layer abutting brain tissue, and to sub-periosteal spread, the less hyperintense layer closer to the bone. Intra-diploic enhancement is present: compare abnormal (4) to normal (5) diploic signal. Bone is clearly invaded at the temporal fossa (6). A cyst-like mass is demonstrated on the posterior aspect of the intracranial tumor (7)

a b

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