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Shun Yao, Farhana Akter, Ru-Yuan Zhang and Zhouyue Li

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John W. Rutland, Francesco Padormo, Cindi K. Yim, Amy Yao, Annie Arrighi-Allisan, Kuang-Han Huang, Hung-Mo Lin, James Chelnis, Bradley N. Delman, Raj K. Shrivastava and Priti Balchandani

OBJECTIVE

The objective of this study was to investigate microstructural damage caused by pituitary macroadenomas by performing probabilistic tractography of the optic tracts and radiations using 7-T diffusion-weighted MRI (DWI). These imaging findings were correlated with neuro-ophthalmological results to assess the utility of ultra–high-field MRI for objective evaluation of damage to the anterior and posterior visual pathways.

METHODS

Probabilistic tractography employing 7-T DWI was used to reconstruct the optic tracts and radiations in 18 patients with adenomas and in 16 healthy volunteers. Optic chiasm compression was found in 66.7% of the patients and visual defects in 61.1%. Diffusion indices were calculated along the projections and correlated with tumor volumes and results from neuro-ophthalmological examinations. Primary visual cortical thicknesses were also assessed.

RESULTS

Fractional anisotropy was reduced by 21.9% in the optic tracts (p < 0.001) and 17.7% in the optic radiations (p < 0.001) in patients with adenomas. Patients showed an 8.5% increase in mean diffusivity of optic radiations compared with healthy controls (p < 0.001). Primary visual cortical thickness was reduced in adenoma patients. Diffusion indices of the visual pathway showed significant correlations with neuro-ophthalmological examination findings.

CONCLUSIONS

Imaging-based quantification of secondary neuronal damage from adenomas strongly correlated with neuro-ophthalmological findings. Diffusion characteristics enabled by ultra–high-field DWI may allow preoperative characterization of visual pathway damage in patients with chiasmatic compression and may inform prognosis for vision recoverability.

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John W. Rutland, Bradley N. Delman, Kuang-Han Huang, Gaurav Verma, Noah C. Benson, Dillan F. Villavisanis, Hung-Mo Lin, Joshua B. Bederson, James Chelnis, Raj K. Shrivastava and Priti Balchandani

OBJECTIVE

Vision loss remains a debilitating complication of pituitary adenomas, although there is considerable variability in visual impairment before and after decompression surgery. Growing evidence suggests secondary damage to remote visual structures may contribute to vision loss in patients with chiasmatic compression. The present study leverages ultrahigh field 7-T MRI to study the retinotopic organization of the primary visual cortex (V1), and correlates visual defects with cortical thinning in V1 to characterize consequences of pituitary adenomas on the posterior visual system.

METHODS

Eight patients (4 males and 4 females, mean age 44.3 years) with pituitary adenomas who exhibited chiasmatic compression and visual field defects, as well as 8 matched healthy controls (4 males and 4 females, mean age 43.3 years), were scanned at 7-T MRI for this prospective study. Whole-brain cortical thickness was calculated using an automated algorithm. A previously published surface-based algorithm was applied to associate the eccentricity and polar angle with each position in V1. Cortical thickness was calculated at each point in the retinotopic organization, and a cortical thickness ratio was generated against matched controls for each point in the visual fields. Patients with adenoma additionally underwent neuroophthalmological examination including 24–2 Humphrey automated visual field perimetry. Pattern deviation (PD) of each point in the visual field, i.e., the deviation in point detection compared with neurologically healthy controls, was correlated with cortical thickness at corresponding polar and eccentricity angles in V1.

RESULTS

Whole-brain cortical thickness was successfully derived for all patients and controls. The mean tumor volume was 19.4 cm3. The median global thickness of V1 did not differ between patients (mean ± SD 2.21 ± 0.12 cm), compared with controls (2.06 ± 0.13 cm, p > 0.05). Surface morphometry–based retinotopic maps revealed that all 8 patients with adenoma showed a significant positive correlation between PD and V1 thickness ratios (r values ranged from 0.31 to 0.53, p < 0.05). Mixed-procedure analysis revealed that PD = −8.0719 + 5.5873*[Median V1 Thickness Ratio].

CONCLUSIONS

All 8 patients showed significant positive correlations between V1 thickness and visual defect. These findings provide retinotopic maps of localized V1 cortical neurodegeneration spatially corresponding to impairments in the visual field. These results further characterize changes in the posterior visual pathway associated with chiasmatic compression, and may prove useful in the neuroophthalmological workup for patients with pituitary macroadenoma.

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John W. Rutland, Kuang-Han Huang, Corey M. Gill, Dillan F. Villavisanis, Judy Alper, Gaurav Verma, Joshua B. Bederson, Bradley N. Delman, Raj K. Shrivastava and Priti Balchandani

OBJECTIVE

Trigeminal neuralgia (TN) is a debilitating neurological disease that commonly results from neurovascular compression of the trigeminal nerve (CN V). Although the CN V has been extensively studied at the site of neurovascular compression, many pathophysiological factors remain obscure. For example, thalamic-somatosensory function is thought to be altered in TN, but the abnormalities are inadequately characterized. Furthermore, there are few studies using 7-T MRI to examine patients with TN. The purpose of the present study was to use 7-T MRI to assess microstructural alteration in the thalamic-somatosensory tracts of patients with TN by using ultra–high field MRI.

METHODS

Ten patients with TN and 10 age- and sex-matched healthy controls underwent scanning using 7-T MRI with diffusion tensor imaging. Structural images were segmented with an automated algorithm to obtain thalamus and primary somatosensory cortex (S1). Probabilistic tractography was performed between the thalamus and S1, and the microstructure of the thalamic-somatosensory tracts was compared between patients with TN and controls.

RESULTS

Fractional anisotropy of the thalamic-somatosensory tract ipsilateral to the site of neurovascular compression was reduced in patients (mean 0.43) compared with side-matched controls (mean 0.47, p = 0.01). The mean diffusivity was increased ipsilaterally in patients (mean 6.58 × 10−4 mm2/second) compared with controls (mean 6.15 × 10−4 mm2/second, p = 0.02). Radial diffusivity was increased ipsilaterally in patients (mean 4.91 × 10−4 mm2/second) compared with controls (mean 4.44 × 10−4 mm2/second, p = 0.01). Topographical analysis revealed fractional anisotropy reduction and diffusivity elevation along the entire anatomical S1 arc in patients with TN.

CONCLUSIONS

The present study is the first to examine microstructural properties of the thalamic-somatosensory anatomy in patients with TN and to evaluate quantitative differences compared with healthy controls. The finding of reduced integrity of these white matter fibers provides evidence of microstructural alteration at the level of the thalamus and S1, and furthers the understanding of TN neurobiology.

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John W. Rutland, Satish Govindaraj, Corey M. Gill, Michael Shohet, Alfred M. C. Iloreta Jr., Joshua B. Bederson, Raj K. Shrivastava and Bradley N. Delman

OBJECTIVE

CSF leakage is a potentially fatal condition that may result when a skull base dural defect permits CSF communication between the cranial vault and sinonasal cavities. Flow rate is an important property of CSF leaks that can contribute to surgical decision-making and predispose patients to complications and inferior outcomes. Noninvasive preoperative prediction of the leak rate is challenging with traditional diagnostic tools. The present study compares fluid configurations on early and late volumetric extended echo train T2-weighted MRI by using image tracings and sequence subtraction as a novel method of quantifying CSF flow rate, and it correlates radiological results with intraoperative findings and clinical outcomes.

METHODS

A total of 45 patients met inclusion criteria for this study and underwent 3-T MRI. Imaging sequences included two identical CUBE T2 (vendor trade name for volumetric extended echo train T2) acquisitions at the beginning and end of the scanning session, approximately 45 minutes apart. Twenty-five patients were confirmed to have definitive spontaneous or traumatic anterior skull base CSF leaks. Semiautomated volumetric segmentation of CSF intensity was performed on both CUBE data sets by using 3D-Slicer software, and volumes were subtracted to obtain accumulated CSF volume. These imaging-derived fluid accumulations were correlated with high- or low-flow states, as well as ultimate treatment outcomes including recurrences.

RESULTS

Of the 45 patients, 25 (55.6%) had definitive evidence of CSF leakage, and 22 (88%) of these underwent surgical repair. Patients with high-flow CSF leaks had higher early (4.058 cm3 vs 0.982 cm3, p = 0.04), late (4.58 cm3 vs 1.096 cm3, p = 0.04), and accumulated (0.53 cm3 vs 0.11 cm3, p = 0.01) fluid volume measurements than patients with low-flow leaks. The 5 (22.7%) patients who exhibited postoperative CSF leak recurrence had significantly greater early (6.30 cm3 vs 1.23 cm3, p = 0.008) and late (6.87 cm3 vs 1.45 cm3, p = 0.008) volumes. Accumulated volume was not significantly greater in patients with leak recurrence (0.58 cm3 vs 0.22 cm3, p = 0.07). Early, late, and accumulated volumes were significantly correlated with postoperative hospital stay as well as duration of postoperative lumbar drain placement (p < 0.05 for all measures).

CONCLUSIONS

High-resolution CUBE T2 MRI, coupled with precise volumetric segmentation and subtraction of sinonasal hyperintensity, not only demonstrated predictive value in differentiating low- and high-flow CSF leaks, but also correlated with postoperative complications such as leak recurrence. These findings may be useful in the clinical workup and neurosurgical management of patients with skull base CSF leaks.

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John W. Rutland, Joshua Loewenstern, Daniel Ranti, Nadejda M. Tsankova, Christopher P. Bellaire, Joshua B. Bederson, Bradley N. Delman, Raj K. Shrivastava and Priti Balchandani

OBJECTIVE

Endoscopic surgery is an effective treatment strategy for pituitary adenomas; however, intrinsic tumor properties such as tumor consistency can challenge or preclude gross-total resection. Preoperative characterization of tumor consistency may help to guide the surgical approach and to predict the extent of resection that is possible. Advanced radiological modalities such as 7T diffusion-weighted imaging (DWI) may be useful in probing biological tissue properties of pituitary adenomas. The objective of the present study was to examine 7T DWI as a novel method of measuring the consistency of pituitary adenomas.

METHODS

Thirteen patients with pituitary macroadenomas underwent 7T MRI, including a DWI image acquisition. Tumor apparent diffusion coefficient (ADC) was normalized to the adjacent temporal gray matter ADC. All patients underwent resection, and a single neurosurgeon blinded to ADC values rated tumor firmness from 1 (least firm) to 5 (most firm) using objective criteria. The tumor specimens were evaluated histopathologically for cellularity, collagen content, and vascularity by a neuropathologist who was also blinded to ADC values. The tumor ADC was correlated with intraoperative consistency rating, histopathology, and extent of resection. Receiver operating characteristic (ROC) curve analyses were performed to identify thresholds to predict tumor consistency.

RESULTS

Corrected ADC values were significantly correlated with both tumor firmness (r = −0.60, p = 0.029) and the extent of trichrome staining (r = −0.72, p = 0.009) such that greater ADC values were associated with both decreased tumor firmness and decreased collagen staining. Correlations between ADC values and tumor vascularity were not significant (r = −0.09, p = 0.78). Corrected ADC values in totally resected tumors (1.54) were greater than those in subtotally resected tumors (0.85) (p = 0.02), and ADC values were greater with moderate tumor cellularity (1.51) than with high tumor cellularity (0.8) (p = 0.035). There was a trend-level association for partial resections to exhibit greater tumor firmness rating (3 vs 1.7; p = 0.051). Finally, the degree of trichrome staining positively correlated with tumor firmness (r = 0.60, p = 0.04). The optimal threshold for predicting intraoperative consistency rating was an ADC ratio of 0.87 (sensitivity 80%, specificity 100%, area under the curve [AUC] 0.90; p = 0.043). The optimal cutoff for distinguishing the extent of resection was 1.19 (sensitivity 85.7%, specificity 83.3% AUC 0.833; p = 0.046).

CONCLUSIONS

The authors’ results suggest that a high-resolution ADC of pituitary adenomas is a sensitive measure of tumor consistency. 7T DWI may hold clinical value in the preoperative workup and surgical management of patients with pituitary macroadenomas.

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John W. Rutland, Javin Schefflein, Annie E. Arrighi-Allisan, Daniel Ranti, Travis R. Ladner, Akila Pai, Joshua Loewenstern, Hung-Mo Lin, James Chelnis, Bradley N. Delman, Raj K. Shrivastava and Priti Balchandani

OBJECTIVE

Predicting vision recovery following surgical decompression of the optic chiasm in pituitary adenoma patients remains a clinical challenge, as there is significant variability in postoperative visual function that remains unreliably explained by current prognostic factors. Available literature inadequately characterizes alterations in adenoma patients involving the lateral geniculate nucleus (LGN). This study examined the association of LGN degeneration with chiasmatic compression as well as with the retinal nerve fiber layer (RNFL), pattern standard deviation (PSD), mean deviation (MD), and postoperative vision recovery. PSD is the degree of difference between the measured visual field pattern and the normal pattern (“hill”) of vision, and MD is the average of the difference from the age-adjusted normal value.

METHODS

A prospective study of 27 pituitary adenoma patients and 27 matched healthy controls was conducted. Participants were scanned on a 7T ultra–high field MRI scanner, and 3 independent readers measured the LGN at its maximum cross-sectional area on coronal T1-weighted MPRAGE imaging. Readers were blinded to diagnosis and to each other’s measurements. Neuro-ophthalmological data, including RNFL thickness, MD, and PSD, were acquired for 12 patients, and postoperative visual function data were collected on patients who underwent surgical chiasmal decompression. LGN areas were compared using two-tailed t-tests.

RESULTS

The average LGN cross-sectional area of adenoma patients was significantly smaller than that of controls (13.8 vs 19.2 mm2, p < 0.0001). The average LGN cross-sectional area correlated with MD (r = 0.67, p = 0.04), PSD (r = −0.62, p = 0.02), and RNFL thickness (r = 0.75, p = 0.02). The LGN cross-sectional area in adenoma patients with chiasm compression was 26.6% smaller than in patients without compression (p = 0.009). The average tumor volume was 7902.7 mm3. Patients with preoperative vision impairment showed 29.4% smaller LGN cross-sectional areas than patients without deficits (p = 0.003). Patients who experienced improved postoperative vision had LGN cross-sectional areas that were 40.8% larger than those of patients without postoperative improvement (p = 0.007).

CONCLUSIONS

The authors demonstrate novel in vivo evidence of LGN volume loss in pituitary adenoma patients and correlate imaging results with neuro-ophthalmology findings and postoperative vision recovery. Morphometric changes to the LGN may reflect anterograde transsynaptic degeneration. These findings indicate that LGN degeneration may be a marker of optic apparatus injury from chiasm compression, and measurement of LGN volume loss may be useful in predicting vision recovery following adenoma resection.