Utility of Contrast-enhanced 3D T1-weighted CUBE Fat Sat Sequence MRI to Evaluate Pathological Cranial Nerve Enhancement: A Cross-sectional Study

1. Assistant Professor, Department of Radiodiagnosis, IGIMS, Patna, Bihar, India. 2. Senior Resident, Department of Radiodiagnosis, IGIMS, Patna, Bihar, India. 3. Assistant Professor, Department of Radiodiagnosis, IGIMS, Patna, Bihar, India. 4. Professor, Department of Radiodiagnosis, IGIMS, Patna, Bihar, India. 5. Assistant Professor, Department of Radiodiagnosis, IGIMS, Patna, Bihar, India.

Abstract

Introduction: Abnormal Cranial Nerve (CN) enhancement can point towards an underlying disorder or disease severity. Therefore, the depiction of this feature is of utmost importance in the evaluation of various pathologies. Various Magnetic Resonance Imaging (MRI) sequences have a role in the early identification of such findings.

Aim: To study the spectrum of cases of abnormal CN enhancement on MRI and the role of contrast-enhanced 3 Dimensional (3D) T1-weighted CUBE Fat saturated sequence in evaluating pathological CN enhancement.

Materials and Methods: This cross-sectional study was conducted in the Department of Radiodiagnosis at Indira Gandhi Institute of Medical Sciences, Patna, Bihar, India. The duration of the study was two years, from June 2020 to June 2022. Study included 50 patients who presented with signs and symptoms of CN involvement or were referred for other pathologies with incidental detection of pathological nerve enhancement on 1.5 Tesla (T) MRI Scanner. The data was transferred to a Microsoft excel 2010 sheet and results were expressed in terms of frequency and percentages.

Results: The mean age of the study participants was 33.3±20.9 years. Male to female ratio was 28:22=1.27:1. Infections were the most common cause of abnormal CN enhancement 26 (52%) cases followed by demyelination 3 (6%) cases, haematological malignancy 4 (8%) cases, metastatic neural infiltration 5 (20%), primary neural tumours 4 (18%), Bell’s palsy 1 (2%) case, Tolosa Hunt Syndrome (THS) 1 (2%) case and idiopathic polyneuritis cranialis 1 (2%) case.

Conclusion: Contrast-enhanced 3D T1 CUBE Fat Saturation (FS) sequence is excellent in depicting abnormal CN enhancement, especially the cisternal segments.

1.5 Tesla, 3 dimensional, Magnetic resonance imaging

A total of 12 pairs of CN symmetrically originate from different parts of the brain, including the cerebrum (I, II CN), midbrain (III, IV CN), pons (V to VIII CN) and medulla (IX to XII CN) (1). MRI is the best imaging modality to anatomically map the CN and their pathologies. It can also detect changes in enhancement patterns indicating underlying pathology when their size or thickness is normal (1). The abnormal CN enhancement can be present in a variety of clinical conditions, which vary from infection to demyelination, granulomatous disorders, primary neural or brain tumours, and metastatic disease (2). Subtle neural enhancement can be missed on routine postcontrast 2D spin echo sequences due to its non volumetric nature. Hence, depiction of CN on routine postcontrast images is difficult and can be frequently missed. In this regard, 3D T1 CUBE sequence scores over the 2D sequence as it enables us to pick even subtle enhancements, which at times may be the only sign of underlying disorder (2),(3),(4).

The T1 CUBE is a 3D Fast Spin Echo (FSE) sequence that uses variable flip angle and higher Echo Train Length (ETL) train length. It reduces the acquisition time and acquires 3D volumetric data that can be reformatted into any plane without partial volume effect. The volumetric data helps in early detection of subtle neural enhancements which can be easily compared to the opposite side (3). There is also suppression of signal from small blood vessels by applying techniques like spatial Presaturation, double inversion recovery, and motion sensitising magnetisation preparation (4). Hence, signals from blood vessels at the brain surface are reduced (black blood imaging) leading to better delineation of meningeal or other pathological enhancement (3),(5). However, grey white matter interface is poorly distinct in CUBE images. The aim of the present study was to study the role of contrast-enhanced 3D T1-weighted CUBE FS sequence in evaluating pathological CN enhancement.

Material and Methods

This cross-sectional study was conducted in the Department of Radiodiagnosis at Indira Gandhi Institute of Medical Sciences, Patna, Bihar, India. The duration of the study was two years, from June 2020 to June 2022. Institutional Ethics Committee approval (1525/IEC/IGIMS/2020) was obtained.

Inclusion criteria: The patients who presented with signs and symptoms of CN involvement or referred for other pathologies with incidental detection of pathological nerve enhancement were included in the study. For e.g., complaints of vision loss if 2nd CN involvement, drooping of eyelid in 3rd CN palsy, extraocular muscle palsy in CN 3rd, 4th, 6th palsy etc.

Exclusion criteria: The patients with claustrophobia, cardiac pacemaker, cochlear implant, other MRI non compatible metallic implants, metallic foreign body and reduced glomerular filtration rate were excluded from the study. As study included contrast imaging in each case, pregnant females were also excluded considering lack of adequate safety data.

Study Procedure

Analysis of data of pathological CN enhancement in 50 patients who were imaged on 1.5T MRI Scanner (OPTIMA 450w, General Electric, and United States) was done. Routine MRI brain sequences including T1, T2, Fluid-attenuated Inversion Recovery (FLAIR), Diffusion and Susceptibility Weighted sequences (DWI and SWI) were acquired. In addition to these, contrast enhanced conventional 2D spin echo T1 FS in three planes and 3D T1 CUBE FS sequence in sagittal plane were also taken after injection of gadolinium-based MRI contrast (dose-0.1 mmol/kg body weight). The imaging parameters of 3D T1 CUBE sequence given in (Table/Fig 1).

Statistical Analysis

The data was transferred to a Microsoft excel 2010 sheet and results were expressed in terms of frequency and percentages.

Results

The mean age of patients was 33.3±20.9 years. Male to female ratio was 28:22=1.27:1. Overall, the most common cause of abnormal CN enhancement N=26 (52%) cases in the study was infections with CNS tuberculosis being the most common. The various pathologies are summarised in the (Table/Fig 2) and the spectrum of various CN involvement and their associated pathologies are summarised in (Table/Fig 3).

(Table/Fig 4) illustrates normal CN anatomy on 3D T1 CUBE postcontrast MRI. In the present study, 17 patients were of CNS tuberculosis with 16 having multiple nerves involvement. The 3rd CN involvement was most common and seen in 15 (88%) cases. The 12th nerve was least commonly involved, seen in 1 (5.8%) case only (Table/Fig 5),(Table/Fig 6),(Table/Fig 7). In cases, where optic nerve involvement was seen, perineural enhancement along the optic nerve and optic chiasma was the most common feature.

Discussion

The CN are lined by connective tissue sheaths including endoneurium, perineurium, and epineurium. The tight junctions in the endothelium of endoneural capillaries and in the inner layers of perineurium, maintain the blood-nerve barrier and its disruption leads to leakage of contrast material resulting in perineural enhancement (2). The geniculate, tympanic, and mastoid segments of the facial nerve may show enhancement due to the presence of perineural and epineural venous plexuses, however, the intracanalicular-labyrinthine segment does not normally enhance (2). Similarly, trigeminal ganglion and proximal portion of its divisions do not normally enhance, however, surrounded by enhancing perineural vascular plexus. Enhancement of cisternal portion of the CN is always abnormal (6). The various pathologies which can show abnormal CN enhancement include neoplasm, infections, inflammation, autoimmune, demyelinating, granulomatous, postradiation neuritis, infarction, brain contusion and primary nerve tumours (6),(7),(8).

TBM and found that, 3rd nerve palsy was the commonest (56.9%) followed by 2nd (52.8%), 6th (4.2%) and 8th nerve palsy (13.9%). A 25% of patients had more than one CN involvement (11). The findings of the present study were quite similar to the study done by Li X et al.

Viral infection: Viral meningoencephalitis can also present with involvement of CN (Table/Fig 8). Optic Neuritis (ON) and orbital apex syndrome, although rare, may be seen in herpes zoster ophthalmicus. Presence of unilateral optic nerve enhancement or trigeminal nerve complex in postcontrast study can also be seen. Enhancement can be best visualised in 3D TI CUBE sequence and thus, strengthen the diagnosis and support clinical findings of sensory or visual disturbance in patients with herpetic rash [Table/Fig-9,10].

Viral neuritis and labyrinthitis present with unilateral acute vertigo or hearing loss with associated nausea and vomiting. The cisternal segment of vestibular nerve or labyrinth appear hyperintense on T2 and FLAIR images and showed enhancement in postcontrast sequences, better appreciated in 3D T1 CUBE images (Table/Fig 11) (8).

Fungal infection: Fungal infections of CNS can manifest as meningitis, cerebritis, abscess formation, cryptococcoma, and vasculitis depending upon the immune status of the patient (12). Intracranial extension of disease from infected paranasal sinuses can lead to cavernous sinus thrombosis, involvement of the optic nerves with variable signs and symptoms. These findings are best evaluated by MRI and even subtle nerve enhancement can be picked up by post Gad 3D T1 black blood imaging (Table/Fig 12),(Table/Fig 13).

Lyme’s disease: Lyme disease, also known as borreliosis, is caused by the bacteria Borrelia burgdorferi and the vector of the disease is ixodid tick (Table/Fig 14). The disease may cause focal lesions in the white matter of brain, nerve root or meningeal enhancement and may affect other organ systems.

Bell’s palsy: Bell’s Palsy (facial palsy) doesn’t require imaging in typical cases. MRI is done in atypical cases like gradual-onset palsy, slowly progressive palsy, facial palsy accompanied by spasm, recurrent palsy, unusual degrees of pain, and the presence of multiple cranial neuropathies or other neurologic symptoms. In post Gad scan, enhancement of facial nerve is most pronounced in the region of the geniculate ganglion, without nodularity. If nodular enhancement is seen, then other causes should be sought (Table/Fig 15) (13).

Demyelination: Demyelinating ON, usually presents with painful loss of vision in young or middle-aged adults. It can present as an isolated or with Multiple Sclerosis (MS) in most of the cases. A 50% patients presenting with isolated ON develop MS later in the course of the disease (14). Demyelinating ON can present in MS, Neuromyelitis Optica Syndrome Disorder (NMO-SD), Acute Disseminated Encephalomyelitis (ADEM) and anti MOG antibody disease. In NMO-SD ON, intracranial, chiasmal and optic tract involvement is seen while in MOG ON, intraorbital ON involvement is seen with peri optic fat stranding [Table/Fig-16,17] (15). Optic neuritis is not common in ADEM while MS presents with frequent optic nerve involvement, most commonly intraorbital and intracanalicular segments. In demyelinating ON, the nerve shows increased T2 signals with some degree of enhancement on postcontrast study (15).

Neoplastic: Primary Nerve Tumours-schwannoma is the most common primary CN tumour which can develop in any CN except those which lack schwann cells (I and II). Vestibulocochlear nerve (VIII) is the most commonly involved followed by trigeminal (V), facial (VII), glossopharyngeal (IX), vagus (X), spinal accessory (XI), and hypoglossal (XII) nerves (16). The CN tumours appear heterogeneously hyperintense on T2 weighted images and showed avid postcontrast enhancement with or without presence of non enhancing cystic/necrotic areas (Table/Fig 18),(Table/Fig 19). Other group of tumours includes optic pathway gliomas and esthesioneuroblastoma (Table/Fig 20) (17). The optic nerve sheath meningioma arises from arachnoid cell layer and not from neural structure, hence not included in the present study.

Malignant nerve tumors-retinoblastoma is a malignant tumour that involves the eyeball and may spread along the optic nerve up to the optic chiasma (Table/Fig 21). Perineural spread of malignancy can occur in various head and neck malignancies like adenoid cystic carcinoma, squamous cell carcinoma, mucoepidermoid carcinoma, basal cell carcinoma, rhabdomyosarcoma and other sarcomas (18). Leptomeningeal spread of tumours can present as multiple CN involvement as seen in primary intraaxial tumours like medulloblastoma, ependymoma, oligodendroglioma, and glioblastoma or secondary tumours (leukaemia/lymphoma, breast, lung, renal and prostate carcinomas and melanoma) (1),(8). Neural involvement can manifest in the form of thickening, irregularity and/or enhancement of the CN and their branches, which is best appreciated in 3D CUBE T1 contrast FS sequence (Table/Fig 22),(Table/Fig 23),(Table/Fig 24),(Table/Fig 25),(Table/Fig 26),(Table/Fig 27),(Table/Fig 28),(Table/Fig 29),(Table/Fig 30). Also, associated signs like enlargement of cranial neural foramina, obliteration of perineural fat on T1 TSE images, muscle denervation presenting as T2/STIR hyperintensity or fatty infiltration of muscles can be seen [Table/Fig-31] (18),(19).

Tolosa hunt syndrome: Schuknecht B et al., evaluated 15 patients with painful ophthalmoplegia and found enhancing soft tissue with lateral bulging contour of cavernous sinus in all patients. Associated signs were internal carotid artery narrowing, extension to superior orbital fissure and orbital apex and complete resolution of findings with steroid treatment on six months follow-up (20). In the present study, findings were similar and marked improvement of symptoms was seen after starting of steroids and on follow-up [Table/Fig-32].

Idiopathic polyneuritis cranialis: It is a rare disorder that can affect multiple CN. Torres AR et al., described the disorder in a young male who presented with multiple episodes of different CN palsies. The most common nerves affected are IV, V, VI and VII CNs. Its aetiology is multifaceted such as inflammatory, infective, autoimmune, toxin mediated, vitamin deficiency, granulomatous, connective tissue disorders or idiopathic (21). In the present study, no aetiology was found in work-up [Table/Fig-33]. [Table/Fig-34] summarises all aetiologies of pathological CN enhancement and how to differentiate them.

Limitation(s)

The limitations of the study include small sample size diseases like neurosarcoidosis atypical infections affecting the CN were not included in the study.

Conclusion

Presence of nerve enhancement is a strong predictor of underlying pathology and may be the only sign of disease in MRI brain studies. Clinical history with other associated findings on imaging help in reaching the final diagnosis. A 3D CUBE T1 sequence helps in picking up even subtle nerve enhancements, hence, should always be a part of brain MRI imaging.

DOI and Others

DOI: 10.7860/JCDR/2023/58770.18016

Date of Submission: Jun 30, 2022
Date of Peer Review: Oct 05, 2022
Date of Acceptance: Mar 29, 2023
Date of Publishing: Jun 01, 2023

AUTHOR DECLARATION:
• Financial or Other Competing Interests: None
• Was Ethics Committee Approval obtained for this study? Yes
• Was informed consent obtained from the subjects involved in the study? Yes
• For any images presented appropriate consent has been obtained from the subjects. Yes

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