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Role of Magnetic Resonance Imaging in Evaluation of Trigeminal Neuralgia with its Anatomical Correlation.

The International Association for the study of pain (IASP) defines pain as an unpleasant sensory and emotional experience associated with actual or potential tissue damage or described in terms of such damage. IASP in November 2010 further extended to define neuropathic pain as "Pain initiated or caused by primary lesion or dysfunction of the peripheral or central nervous system (1). This is a modification of the previous definition of neuropathic pain which was described as "pain initiated or caused by a primary lesion, dysfunction, or transitory perturbation of the peripheral or central nervous system" (2). When compared to nociceptive pain, the persistence of neuropathic pain is longer, not quite responsive to pain medications, often debilitating and difficult to treat (3). Neuropathic pain is frequent with other predisposing conditions like diabetes, carpal tunnel syndrome, sciatica, Guillain-Barre syndrome, cancer, multiple sclerosis, kidney disorders, alcoholism, HIV etc. The prevalence and incidence of neuropathic pain is estimated between 1 and 10%, with few studies admitted that neuropathic component may be present in 35% of all painful syndromes (4). Smith BH and co-workers stated that the estimate of prevalence tends to be lower (1-2%) than those based on classic symptoms reports (5). Gustorff et al. from their prospective survey in 2008 showed that in Austria the occurrence of neuropathic pain was 3.3%, with an increase in prevalence (up to 26%) as the age increases (6). Van Hecke et al. believed that due to lack of universal evidences and protocols, a range of incidence and prevalence rates has been identified. They also suggested that future epidemiological studies should take note of mentioned factors (7).

Trigeminal neuralgia (TN)

Trigeminal neuralgia (Tic douloureax), is a chronic pain affecting the Trigeminal nerve. Burchiel KJ defined trigeminal neuropathic pain as constant unilateral facial pain that varies in intensity, is triggerable, and not curable (8). This is characterized by episodes of unilateral, lancinating, shock- like pains and are also intermixed with pain free episodes.

Clinical features for trigeminal neuralgia

International Headache Society had recently proposed strict clinical criteria for trigeminal neuralgia diagnosis and according to this, diagnosis only can be made when there are at least three attacks of unilateral facial pain occur fulfilling the following criteria such as (1) occurring in one or more divisions of the trigeminal nerve, with no radiation beyond the trigeminal distribution and (2) pain with at least, recurring in paroxysmal attacks lasting from a fraction of second to 2 minutes or severe intensity or electric shock-like, shooting, stabbing, or sharp in quality or precipitated by innocuous stimuli to the affected side of the face (9). Eller JL and co-workers, in their new classification differentiated TN into type 1 and type 2 which was earlier referred as classic or typical TN and secondary TN respectively. Type 1 is characterized by episodic pain whereas type expresses as pain which more than 50% of the time is constant in nature (10). It also has been theorized that in type 2, there is likelihood to detect a structural abnormality such as tumours or vascular malformations.

Imaging modalities in evaluation of trigeminal neuragia

A wide variety of imaging modalities were used in past for image evaluation of the cranial nerves. Pneumocephalography was the first cross-sectional imaging study used to demonstrate cranial nerves. This technique involves introduction of air into subarachnoid space around cranial nerves in order to allow clear visualization of nerves within the basal cisterns (11). Later, with advent of CT, the detail in visualizing the regions of cranial nerves has improved and further with injection of intrathecal contrast shows linear filling defects within subarachnoid space. But the visualization is limited to the cisternal or subarachnoid course of cranial nerves. But with advent of MRI, an imaging modality without using ionizing radiation and acquisition of multiple plane images it became standard mode of imaging of cranial nerves (12).

It is quite challenging to image of the cranial nerves as they are small with complex anatomy and cannot be easily distinguished from surrounding soft tissues (13,14). Being the largest cranial nerve trigeminal nerve can be visualized better with various modern imaging techniques (15). Computer Tomography gives better visibility of the foramina and the nerve exit but a right sequence of MRI is the preferable imaging for cranial nerves (16). Advances in MRI plays a vital role in presurgical evaluation of the trigeminal nerve.

Magnetic resonance imaging

The primary imaging modality for evaluation of patients with trigeminal neuralgia is MRI (13). It has been used as an adjunct for planning the management of trigeminal nerve pathologies (17). The basic standardized procedure for those patients with symptoms of trigeminal neuralgia consists of T1 weighted spin echo sequences (in axial plane) with a turbo STIR (short tau inversion recovery) sequence (in coronal plane) (18). In order to visualize and analyse different segments of various cranial nerves, right sequences must be used. The choice of which is based on the tissue or fluid that is surrounding the nerve. [T.sub.2] weighted (T2W), proton- density and multi-echo fast field echo (m-FFE) gives better details of the cranial nerve nuclei and fascicular segment of cranial nerves. Heavy [T.sub.2] sequences were used to visualize cisternal segment of the nerve which is surrounded by cerebrospinal fluid (CSF) (16). Various sequences which are heavily T2W 3D- sequences such as CISS, 3D-TSE, b-FEE, DRIVE, 3D-FSE, FIESTA etc. provides very high resolution images, but they tend to produce artefacts at periphery of the image and therefore must be carefully chosen (18-22). High resolution contrast- enhanced Time-Of-Flight MRA images or high resolution 2D or 3D images shows better visualization of blood vessles around the nerve. Peripheral segments or terminal branches of cranial nerves which are surrounded by soft tissues are better visualized by T1W SE and TSE. Arterial spin labelling MRI is used to demonstrate the cerebral perfusion (23) in diseases like Migraine, Alzheimers, Cerebrovascular stroke but its not used in evaluating Trigeminal Neuralgia. Since a vascular component is involved in Trigeminal Neuralgia future studies using this sequence may disclose undiscovered etiological or contributing factors in trigeminal neuralgia.

Anatomy of trigeminal nerve to identify lesions in MRI

Trigeminal nerve is the largest cranial nerve. It emerges from anterior aspect of pons by two roots i.e. a sensory root that carries sensory information to brain from facial region and a motor root provides motor innervation to the muscles of mastication. There are four central brain stem nuclei that are (1) mesencephalic nucleus, mediating proprioception (2) main sensory nucleus, mediating tactile sensation (3) the motor nucleus provides motor innervation and (4) the spinal nucleus mediates pain and temperature sensation. They lie in tegmentum of lateral pons, along the anterolateral aspect of fourth ventricle and close to the root entry zone of trigeminal nerve (Figure 1). Both the roots (larger sensory and smaller motor) exit via the lateral pons as a common trunk. Sensory root becomes progressively flattened laterally and medially as it expands resulting in formation of ganglionic swelling i.e., the trigeminal ganglion. Compared to sensory moot, the motor root is relatively smaller in size and is situated anterior and medial to the sensory root, and it exits via foramen ovale. After the afferent fibers converges from three main sensory roots of the nerve ([V.sub.1], [V.sub.2] and [V.sub.3]) the main trunk of trigeminal nerve enters throught porus terminus, an opening into the dura mater while entering the Meckel's cave. From this point, the nerve carries it dural covering with it and the myelin sheath surrounding the nerve transitions from that derived from Schwann cells to that derived from oligodendrocytes, and this point of transition from peripheral to central myelin is referred as transition zone and the point where nerve enters pons is called as root entry point or zone (REZ) (24) (Figure 1). The nerve is usually compressed by the one of the neighboring arteries which can be superior cerebellar artery (25), anterior inferior cerebellar artery (26), basilar artery , vertebral artery, posterior inferior cerebellar artery and pontine artery (27). Neurovascular compression is graded on MRI based on the extent of the compression of the nerve and vessel (28). Grade I Mild contact between the nerve and blood vessel, Grade II Mild distortion /displacement of the nerve root by artery, Grade III Marked indentation of the nerve root by the vessel.

Demonstration of lesions at various levels in MRI

MRI is often used as a work up of patients with TN. To assess anatomical characteristics and patterns of neurovascular compression, brain gray matter volume and cortical thickness (CT) and diffusion imaging (diffusion tensor images) to assess brain white matter and trigeminal nerve microstructure structural MRI for TN uses high-resolution anatomical imaging (variations of T1and T2-weighted images) (29). To image trigeminal neuropathy, high field units (1T to 3T) are required as they provide better spatial resolution, better signal-to-noise ratio and shorter examination time (30). Table 1 is presented with details of various investigational studies on trigeminal neuralgia using Magnetic Resonance Imaging (MRI).

Brainstem

Five distinct anatomical portions of trigeminal nuclear complex and nerve in the brain stem can be identified (31). In MS plaques are hyper intense on T2W and hypo intense on T1W sequences. Sometimes, thin line of T1 hyperintensity can be seen attributing to free radicals and protein accumulations (31). Approximately 25% of infarcts acute strokes occurs in brainstem and infarcts involving the posterior inferior cerebellar artery territory may affect the trigeminal nuclei i.e. dorsal nucleus resulting in cranial nerve V symptoms.

Cisternal segment

In this segment, the portion of trigeminal nerve corresponds to the transition between central nervous system myelin to peripheral nervous system myelin. Lesions or pathologies involving this segment typically present with trigeminal neuralgia. This relative thinness in myelin lining of the nerve in this nerve makes it vulnerable to extrinsic compression (32). Compression of nerve by adjacent blood vessel (Neurovascular compression (NVC)) revealed focal demyelination in that region resulting in clinical features of TN (33,34) (Figure 2). Arteriovenous malformations, aneurysms, vascular loops, fistulas, vascular ectasias also exhibit symptoms of TN. Coronal or oblique sagittal T1- weighted MR images may demonstrate neurovascular contact with or without compression of cisternal segment of 5th cranial nerve. Structural MRI can be used to test whether NVC sufficiently explains TN aetiology. Satoh T and co-workers had categorized NVC into four categories based on the proximity of nerve with the vessel as severe, moderate, simple and none. Also, they found that in affected nerves of patients this proximity is severe, whereas in unaffected nerves of patients or in healthy individuals it is mostly a simple contact form (35). In MS- related TN, a plaque of demyelination at the region of REZ is seen, which results in gadolinium enhancement at MR imaging. In MR imaging of those with chronic inflammatory demyelinating polyneuropathy, enlargement of cranial nerves was seen at cisternal and peripheral extracranial segments. Schwannoma is common primary neoplasm that frequently affects cisternal segment along with other portions. On MR imaging, these lesions grow along the side of the nerve and may be dumbbell or saddle--shaped (36,37).

Meckel's cave and Cavernous sinus segments

Giant aneurysms in cavernous portions of internal carotid artery may cause compression of cranial nerves and one-third of cases with unruptured aneurysms has reported trigeminal nerve involvement (38). On MR imaging, narrowing of the cavernous portion of internal carotid artery is a common finding. Infrequently, inflammatory lesions effect the cavernous sinus and Meckel's cave is also seen. Symptoms of non-specific inflammation in these segments includes opthalmoparesis, pupillary dysfunction, paraesthesia of forehead etc. Meckel's cave comprises of 0.5% of intracranial tumors and most common lesions seen at this site are schwannomas, meningiomas and malignant nerve sheath tumors. The nerve may also be impinged upon by both benign and malignant lesions involving the cerebellopontine angle cistern and skull base. And also, some meningiomas (e.g., petroclival) that are extending into the Meckel's cave exhibits TN symptoms.

Peripheral Segments

The terminal branches of trigeminal nerve are most commonly involved in peri neural spread of malignancies of head and neck regions. Schwannomas involving the terminal branches are rare with common involvement of ophthalmic division was seen. Direct spread or metastases from distant malignancies can cause trigeminal neuropathy due to compression of the peripheral branches (38).

Magnetic Resonance Neurography (MRN)

This method provides better visualization of peripheral nerves over MRI i.e., small nervesowing to their size, surrounding vessels and muscles. The sequences in this technique uses fat suppression, which further enables the assessment of specific nerve morphological features such as calibre, internal fascicular pattern and the amount of perineurial--endoneurial fluid (39).

CONCLUSION

The root entry zone at the brain stem is the most common site of the lesion followed by the cistern segment, Meckel's cave and the peripheral nerve. The nerve anatomy, site of the lesion in the course of the nerve and the vessel compressing the nerve is well appreciated in an MRI. But the vascularity and the contribution of the cerebral perfusion in that region towards Trigeminal Neuralgia is not well explored. To analyse and to confirm whether cerebral perfusion plays a role in the pathogenesis of the disease an arterial spin labelling MRI would be the imaging of choice. If cerebral perfusion has any contribution then the treatment protocol would vary else it will add more evidence towards the earlier demyelination hypothesis in etiopathogeneis of Trigeminal Neuralgia.

http://dx.doi.org/10.13005/bpj/1640

(Received: 17 July 2018; accepted: 07 January 2019)

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M. Subha and M. Arvind

Department of Oral Medicine & Radiology, Saveetha Dental College & Hospital, Saveetha Institute of Medical & Technical Sciences, Saveetha University, India.

Caption: Fig. 1. Diagrammatic representation showing the convergence of three sensory brances of trigeminal nerve into Gasserian ganglion. Adapted from article of Hughes et al. (15)

Caption: Fig. 2. Shows the NVC at cisternal region by Superior Cerebellar Artery(2a) and Vertebral Artery(2b)

Caption: Fig. 2a. Indentation by SCA at the cisternal region of right trigeminal nerve

Caption: Fig. 2b. Close contact by vertebral artery at cisternal region of right trigeminal nerve
Table 1. Investigational studies on Trigeminal neuralgia using MRI

S.no   Title of Publication                    Author

1.     Preoperative evaluation of              AMmoto H
       neurovascular compression in            et al. (2002)
       patients with trigeminal neuralgia
       by use of three-dimensional
       reconstruction from two types
       of high- resolution magnetic
       resonance imaging

2.     Vascular compression of the             Peker S, Dincer A,
       trigeminal nerve is a frequent          Necmettin PM
       finding in asymptomatic                 (2009)
       individuals: 3-T MR imaging
       of 200 trigeminal nerves
       using 3D CISS sequences.

3.     MRI sequences for detection             Leal PR,
       of neurovascular conflicts in           Froment JC,
       patients with TN and predictive         Sindou M.
       value for characterization of the       (2010)
       conflict (particularly degree of
       vascular compression)

4.     Microvascular decompression             Sekula RS
       for elderly patients with               et al.
       trigeminal neuralgia: a prospective     (2011)
       study and systematic review
       with meta-analysis

5.     Trigeminal neuralgia due to             Lutz J
       neurovascular compression:              et al.
       high-spatial-resolution diffusion-      (2011)
       tensor imaging reveals
       microstructural neural changes

6.     Pre-operative MRI/MRA for               Vergani F
       microvascular decompression             et al.
       in trigeminal neuralgia: consecutive    (2011)
       series of 67 patients

7.     Pre-vascular demonstration of           Zhou Q
       neurovascular relationship in           et al.
       trigeminal neuralgia by using           (2012)
       3D FIESTA sequence

8.     Magnetic resonance imaging              Antonini J
       contribution for diagnosing             et al.
       symptomatic neurovascular contact       (2014)
       in classic trigeminal neuralgia:
       A blinded case-control study and
       meta-analysis

9.     Neurovascular study of the              Docampo J
       trigeminal nerve at 3                   et al.
       t MRI                                   2015

10.    Preoperative MRI in                     Tanrikulu L
       neurovascular compression               et al.
       syndromes and its role in               (2015)
       microsurgical considerations

S.no   Methodology

1.     Assessed the value of
       three-dimensional (3-D) images
       reconstructed from 3-D
       constructive interference
       in steady state (3-D-CISS)
       and 3-D fast inflow with
       steady-state precession
       (3-D-FISP) images for the
       visualization of neurovascular
       compression in patients with
       trigeminal neuralgia

2.     The authors aimed to assess
       whether individuals without
       symptoms of trigeminal
       neuralgia exhibit vascular
       compression of the trigeminal
       nerve. This was investigated
       using ultra-high-field MR
       imaging.

3.     As pre-operative visualization
       of the neurovascular compression
       (NVC) by MRI is vital for
       therapeutic decision, they
       investigated the predictive value
       of MRI for detecting and assessing
       degree of vascular compression
       in trigeminal neuralgia

4.     Prospective study and systemic review
       with meta- analysis was conducted to
       determine whether Micro Vascular
       Decompression (MVD) is safe and effective
       treatment in elderly patients with trigeminal
       neuralgia (TN). An MRI image of the
       brain was taken.

5.     A single-shot diffusion-tensor
       echo-planar sequence was used along
       15 different diffusion directions,
       with a b value of 1000 sec/[mm.sup.2] and
       a section thickness of 2 mm. For
       anatomic correlation, 0.6-mm
       isotropic three-dimensional fast imaging
       employing steady-state images were
       acquired for coregistration with the
       functional diffusion-tensor maps.

6.     Presented a protocol for preoperative
       investigation of TN patients and
       correlated the MR findings with
       surgical evidence of vascular
       compression, in order to calculate
       specificity and sensitivity of
       preoperative MRI and MRA

7.     Evaluatedthe value of high-resolution
       three-dimensional
       FIE STA imaging in the visualization
       of neurovascular relationship in
       patients with TN.

8.     To assess the accuracy of MRI in
       distinguishing symptomatic from
       asymptomatic trigeminal
       neurovascular contact (NVC).
       Examiners evaluated whether the
       trigeminal nerve displayed NVC in
       the REZ or non REZ, whether it was
       dislocated by 38 the vessel or displayed
       atrophy at the contact site.

9.     Prospective study
       aimed to show a novel
       visualization method
       to investigate compression
       of trigeminal nerve using
       3D FIESTA and
       3DTOFMRA.

10.    To minimize the risk of recurrent
       TN, vascular structures in
       anatomical relation to trigeminal
       nerve root at lateral pontine
       aspect should be decompressed
       maximally. New MR techniques,
       their chances and potential
       impact were evaluated.

S.no   No. of patients             Inference

1.     24 consecutive patients     3-D reconstructions from
       with trigeminal neuralgia   two types of high-
       underwent preoperative      resolution magnetic
       3-D-FISP and                resonance images
       3-D-CISS imaging            (3-D-CISS and 3-D-FISP)
                                   are very useful for creating
                                   preoperative simulations
                                   and in deciding whether
                                   to perform surgery in
                                   patients with trigeminal
                                   neuralgia.

2.     100 subjects were imaged    It concluded that it was
       using a 3-T magnet and      first study to have
       high-spatial-resolution     evaluated NVC of the
       three-dimensional (3D)      trigeminal nerve in
       MR imaging with             asymptomatic individuals
       3D constructive             using 3-T MR imaging.
       interference in             Their findings strongly
       steady-state sequences.     suggest that vascular
                                   compression of the
                                   trigeminal nerve is not
                                   necessarily pathological.

3.     91 consecutive patients     Combination of high
       with a preoperative         resolution 3D T2-weighted
       MRI using 3D                with angio-MR-TOF
       T2- weighted and            is a reliable
       angio-MR-TOF.               technique for detecting
                                   NVC and predicting the
                                   degree of compression
                                   in NVC.

4.     36 elderly patients         Concluded that majority
       (mean age 73.0 [+ or -]     of elderly patients
       5.9 years) and 53           with TN can safely
       nonelderly patients         undergo MVD.
       (mean age 52.9
       [+ or -]8.8 years

5.     20 patients with            Diffusion-tensor imaging
       TN and evidence             enables the identification
       of neuro vascular           and quantification of
       contact were                anisotropic changes
       examined                    between normal nerve
                                   tissue and TN-affected
                                   trigeminal nerves.
                                   Correlation with
                                   anatomic 3D fast
                                   imaging employs excellent
                                   delineation of cisternal
                                   segments of tn.

6.     Out of 92 patients who      Preoperative MRI has both
       had MVD for primary         good sensitivity and positive
       TN, 67 who underwent        predictive value. Specificity
       a preoperative MRI and      and negative predictive
       MRA according to            values were limited
       protocol were               in this series.
       included

7.     37 patients with            Anatomical relationships
       unilateral typical          defined by this method
       TN.                         can be useful in surgical
                                   planning and predicting
                                   surgical findings as it
                                   enables accurate
                                   visualization of
                                   neurovascular contact
                                   in patients with TN.

8.     24 classical TN             Concluded that trigeminal
       patients and a              REZ NVC, as detected by
       similar number              MRI, is highly likely to
       of age- matched             be symptomatic when
       healthy controls.           it is associated with
                                   anatomical nerve
                                   changes.

9.     80 patients, 30             The use of combination
       with unilateral TN          of these sequences
       and 50 without              enables quick and
       symptoms of                 efficient visualization
       TN (control                 and assessment of
       group)                      relation between
                                   trigeminal nerve
                                   and neighbouring
                                   vascular structures.

10.    8 patients, in which        High resolution MR
       7 were with TN and          images provide reliable
       one with vertigo            and detailed information
                                   on corresponding
                                   intraoperative anatomy.
                                   So application of these
                                   techniques can be an aid
                                   to indication, planning
                                   & teaching purposes.
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