Probabilistic Fiber-Tracking Reveals Degeneration of the Contralateral Auditory Pathway in Patients with Vestibular Schwannoma

BACKGROUND AND PURPOSE:Vestibular schwannomas cause progressive hearing loss by direct damage to the vestibulocochlear nerve. The cerebral mechanisms of degeneration or plasticity are not well-understood. Therefore, the goal of our study was to show the feasibility of probabilistic fiber-tracking of the auditory pathway in patients with vestibular schwannomas and to compare the ipsi- and contralateral volume and integrity, to test differences between the hemispheres.MATERIALS AND METHODS:Fifteen patients with vestibular schwannomas were investigated before surgery. Diffusion-weighted imaging (25 directions) was performed on a 3T MR imaging system. Probabilistic tractography was performed for 3 partial sections of the auditory pathway. Volume and fractional anisotropy were determined and compared ipsilaterally and contralaterally. The laterality ratio was correlated with the level of hearing loss.RESULTS:Anatomically reasonable tracts were depicted in all patients for the acoustic radiation. Volume was significantly decreased on the hemisphere contralateral to the tumor side for the acoustic radiation and diencephalic section, while fractional anisotropy did not differ significantly. Tracking did not yield meaningful tracts in 3 patients for the thalamocortical section and in 5 patients for the diencephalic section. No statistically significant correlations between the laterality quotient and classification of hearing loss were found.CONCLUSIONS:For the first time, this study showed that different sections of the auditory pathway between the inferior colliculus and the auditory cortex can be visualized by using probabilistic tractography. A significant volume decrease of the auditory pathway on the contralateral hemisphere was observed and may be explained by transsynaptic degeneration of the crossing auditory pathway.

Vestibular schwannoma, also known as acoustic neurinoma, is a common intrameatal and intracranial tumor evolving from the eighth cranial nerve with an incidence of 10–15 per million per year.¹ The tumor usually arises from Schwann cells within the vestibular part of the eighth cranial nerve. The benign tumor is characterized by a slow growth pattern for years.^2,3 The slow-but-steady increase in size causes progressive damage to the neurons of the eighth cranial nerve, leading to hearing impairment, tinnitus, and vertigo.^4–6 Typically the vertigo symptoms are transient, while hearing impairment can progressively deteriorate toward unilateral deafness ipsilateral to the lesion side. To estimate the extent of hearing loss, examination of tone audiometry and speech discrimination is crucial.^6–9 Large tumors involving neighboring structures such as the fifth or seventh cranial nerve or even the brain stem and cerebellum may cause facial paresis and numbness, cerebellar ataxia, or corticospinal tract–related sensorimotor deficits. There are various classification systems, but tumor extension is usually classified on the basis of the size from T1 (intrameatal localization) to T4 (compression of the brain stem).¹⁰ Treatment options include surgical removal of the tumor and radiation therapy. During the past decades, the surgical goal has shifted from gross total resection toward optimal functional outcome.^8,11Despite surgical tumor removal, improvement of hearing is unusual, even if anatomic preservation of the eighth cranial nerve has been achieved and resection has led to decompression of the nerve. Apparently, the cochlear nerve itself and possibly cortical and subcortical auditory structures have a low potential for regeneration after nerve damage. In contrast, the function of the damaged vestibular nerve is compensated by the integrating circuitry of the equilibrium: The latter involves the vestibular, visual, and somatosensory systems¹² and therefore provides a more robust reserve for compensation. Although functional outcome has been the treatment focus, the interest was limited to the individual nerve structures, while the cerebral mechanisms of degeneration or plasticity of the associated white matter tracts and cortex areas are rarely investigated and understood.The first studies by DTI, in unselected hearing disorders, succeeded, in some cases, in illustrating abnormality of white matter integrity of the auditory pathway. Wu et al¹³ found decreased fractional anisotropy (FA) at the contralateral inferior colliculus and lateral lemniscus in 19 patients with non-tumor-related sensorineural hearing loss. Chang et al¹⁴ reported abnormalities of fractional anisotropy in several parts of the auditory pathway when comparing 10 patients with sensorineural hearing loss with healthy subjects. Both investigations indicated a transsynaptic degeneration of the auditory pathway. An association between DTI-derived measures and abnormalities in brain stem auditory-evoked potentials was illustrated in preterm infants.¹⁵ These previous investigations measured DTI-derived parameters like FA or radial diffusivity by using ROI analyses. While the feasibility of fiber-tracking has been shown previously in auditory pathway investigation,^16–18 this method has not been hitherto applied to the auditory pathway in patients with vestibular schwannoma. A detailed analysis of the white matter microstructure of the auditory pathway and of possible abnormalities in patients with vestibular schwannoma does not exist, to our knowledge. Therefore, the primary goal of our study was to show the feasibility of probabilistic fiber-tracking of partial sections of the auditory pathway in patients with vestibular schwannomas and to quantify the volume and integrity of these sections ipsi- and contralateral to the tumor side to test for differences between the hemispheres. The secondary goal was to identify associations of the integrity of the auditory pathway with audiometric measurements, including speech discrimination and the electrophysiologic brain stem–evoked potentials.