Volume of Lateral Geniculate Nucleus in Patients with Glaucoma in 7Tesla MRI
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Journal of Clinical Medicine Article Volume of Lateral Geniculate Nucleus in Patients with Glaucoma in 7Tesla MRI 1, , 2, 1 3 Ewa Kosior-Jarecka * y, Anna Pankowska y , Piotr Polit , Andrzej St˛epniewski , 4 2 1, 2, Mark Roger Symms , Paulina Kozioł , Tomasz Zarnowski˙ z and Radosław Pietura z 1 Department of Diagnostics and Microsurgery of Glaucoma, Medical University of Lublin, 20-079 Lublin, Poland; [email protected] (P.P.); [email protected] (T.Z.)˙ 2 Department of Radiography, Medical University of Lublin, 20-079 Lublin, Poland; [email protected] (A.P.); [email protected] (P.K.); [email protected] (R.P.) 3 Centrum ECO-TECH COMPLEX Maria Curie-Skłodowska University in Lublin, 20-612 Lublin, Poland; [email protected] 4 Applied Science Labs, GE Healthcare, Amersham HP7 9NA, UK; [email protected] * Correspondence: [email protected] The author’s contribution to the study is equal. y The author’s contribution to the study is equal. z Received: 27 May 2020; Accepted: 23 July 2020; Published: 26 July 2020 Abstract: The aim of the study was to assess the volume of the lateral geniculate nucleus (LGN) in patients with open-angle glaucoma in 7Tesla MRI and to evaluate its relation to RNFL thickness and VF indices. Material and methods. The studied group consisted of 20 open-angle glaucoma patients with bilaterally the same stage of glaucoma (11 with early glaucoma and nine with advanced glaucoma) and nine healthy volunteers from the Department of Diagnostics and Microsurgery of Glaucoma, Medical University of Lublin, Poland. Circumpapillary RNFL-thickness measurements were performed using OCT in all patients and visual fields were performed in the glaucoma group. A 7Tesla MRI was performed to assess the volume of both lateral geniculate bodies. Results. The LGN volume varied significantly between groups from 122.1 14.4 mm3 (right LGN) and 101.6 13.3 mm3 ± ± (left LGN) in the control group to 80.2 17.7 mm3 (right LGN) and 71.8 14.2 mm3 (left LGN) ± ± in the advanced glaucoma group (right LGN p = 0.003, left LGN p = 0.018). However, volume values from early glaucoma: right LGN = 120.2 26.5 mm3 and left LGN = 103.2 28.0 mm3 ± ± differed significantly only from values from the advanced group (right LGN p = 0.006, left LGN p = 0.012), but not from controls (right LGN p = 0.998, left LGN p = 0.986). There were no significant correlations between visual field indices (MD (mean deviation) and VFI (visual field index)) and LGN volumes in both glaucoma groups. Significant correlations between mean RNFL (retinal nerve fiber layers) thickness and corresponding and contralateral LGN were observed for the control group (corresponding LGN: p = 0.064; contralateral LGN: p = 0.031) and early glaucoma (corresponding LGN: p = 0.017; contralateral LGN: p = 0.008), but not advanced glaucoma (corresponding LGN: p = 0.496; contralateral LGN: p = 0.258). Conclusions. The LGN volume decreases in the course of glaucoma. These changes are correlated with RNFL thickness in early stages of glaucoma and are not correlated with visual field indices. Keywords: glaucoma; 7Tesla MRI; lateral geniculate nucleus 1. Introduction Glaucoma—a multifactorial disease involving retinal ganglion cells (RGC)—has been estimated as the second leading cause of blindness throughout the world [1]. Pathologically, dendritic damage, J. Clin. Med. 2020, 9, 2382; doi:10.3390/jcm9082382 www.mdpi.com/journal/jcm J. Clin. Med. 2020, 9, 2382 2 of 13 cell body shrinkage and death are ultimately manifested as a progressive loss of the RGC population, leading to clinical vision loss [2–4]. An increasing number of studies [2–5] have suggested that primary open-angle glaucoma (POAG) causes changes in the whole visual pathway, including the optic nerve, lateral geniculate body (LGN), optic radiation and visual cortex. Moreover, the early morphologic changes were detected in the central nervous system (CNS) in monkeys [4]. Multicenter studies showed that elevated intraocular pressure (IOP) is the major risk factor for the onset and progression of glaucoma and the only modifiable factor in treatment. However, some patients continue to progress despite the reduction in IOP levels [6], while others develop typical glaucomatous damage in the absence of elevated IOP (normal tension glaucoma). These data confirm that the pathogenic mechanisms underlying glaucoma are complex which shows the need to look for novel therapeutic strategies. The lateral geniculate nucleus (LGN) plays a role in the function of perception and cognition, including visual attention and awareness [7]. Most RGCs in the LGN form the major vision center relaying information from the eye to the visual cortex. In the LGN the complete contralateral hemifield of vision is represented and parallel central visual pathways are segregated into anatomically distinct magnocellular, parvocellular and koniocellular channels. The axons of the RGCs associated with the temporal half of the retina do not cross in the optic chiasm and transmit their signal to the ipsilateral LGN. In contrast, the RGC axons from the nasal half of the retina decussate in the optic chiasm and transmit the signal to the contralateral LGN. The axons of LGN neurons form the optic radiations projecting to eye-specific columns in the primary visual cortex [2]. In this study, we aimed to include the patients with the same stage of glaucomatous neuropathy in both eyes assessed according to visual field parameters, something which has never been taken into consideration in previous studies. We hoped that this approach would diminish the doubts caused by the fact that the part of nerve fibers crosses the optic nerve in the chiasm, so different glaucoma stages in both eyes theoretically affect the two LGN unequally. Glaucomatous visual losses can be prevented with early diagnosis and treatment; however, affected individuals are typically asymptomatic until the advanced stages. Additionally, although standard automated perimetry (SAP) is the gold standard test of visual function in glaucoma, histological studies have indicated that large numbers of RGC are lost before statistically significant visual field abnormalities [8]. Therefore, there is still a need to look for more sensitive and specific diagnostics methods to be used in glaucoma. Magnetic resonance imaging (MRI) has been used to analyze the visual pathway in glaucoma in previous studies; including morphologic examinations [9,10] and functional measurements [11]. MRI of high resolution with morphometric assessment of LGN and further visual pathway may give the valuable structural diagnostic option in glaucoma, supplementing the typically used structural measurements of retinal nerve fiber layer and optic disc and functional examination by visual field. The assessment of the utility of MRI techniques in glaucoma diagnosis needs to be further studied. Li [12] showed that fractional anisotropy–an index derived from diffusion tensor imaging–can be a measure of glaucoma damage in the optic tract. Lee et al. [13] performed volumetric measures of the LGN in 7T MR with proton density weighting. The higher signal-noise-ratio at 7T allows the acquisition of images with increased spatial resolution [14]. This facilitates precise and possibly better delineation of the LGN based on high-resolution anatomic datasets when compared to standard MR imaging at 3T. The aim of the study was to assess the LGN volumes in patients with bilaterally the same stage of open-angle glaucoma in 7Tesla MRI and to evaluate its relation to RNFL thickness and VF indices. We acquired 7T MR images using Silent [15]—a three-dimensional version of RUFIS [16]—with magnetization transfer weighting. The LGN can be clearly seen on these images, facilitating accurate volumetric study. J. Clin. Med. 2020, 9, 2382 3 of 13 2. Material and Methods The study design was approved by the local Ethical Committee Board at the Medical University of Lublin (approval number KE 0254/149/2018). Informed consent was signed by all participants before inclusion and the study was performed in accordance with the tenets of the Declaration of Helsinki. The studied group consisted of 20 open-angle glaucoma patients and 9 age- and sex-matched healthy volunteers from the Department of Diagnostics and Microsurgery of Glaucoma, Medical University of Lublin, Poland. All studied patients underwent ophthalmic examinations: best-corrected visual acuity (BCVA) assessment, slit-lamp biomicroscopy, Goldmann applanation tonometry, gonioscopy, central corneal thickness and clinical stereoscopic optic disc evaluation. Additionally, visual field examination (perimetry) and optical coherent tomography scanning (OCT) were performed. Standard Automated Perimetry (SAP) was performed using 30 2 Swedish Interactive Threshold Algorithms (Humphrey ± Field Analyzer II, Carl Zeiss Meditec, Dublin, OH, USA). Global indices, such as mean deviation (MD) and Visual Field Index (VFI), of the last reliable SAP were chosen for statistical analysis. Peripapillary retinal nerve fiber layers (RNFL) were measured using OCT (Stratus, Carl Zeiss Meditec, Dublin, OH, USA). The neuroretinal rim area was measured in 4 sectors (temporal, superior, nasal, inferior) and globally as mean RNFL thickness. Glaucoma was defined clinically as glaucomatous optic nerve head morphology combined with typical, reproducible defects in SAP. The glaucomatous defect on SAP was defined based upon a glaucoma hemifield test result qualified as outside normal limits and with the presence of at least 3 contiguous test points