Visual Outcome of an Endoscopic Endonasal Transsphenoidal Approach in Pituitary Macroadenomas: Quantitative Assessment with Diffusion Tensor Imaging Early and Long-Term Results

doi:10.1016/j.wneu.2018.01.134

World Neurosurgery

Volume 112, April 2018, Pages e691-e701

https://doi.org/10.1016/j.wneu.2018.01.134 Get rights and content

Highlights

•
DTI-derived FA and MD values of the affected side may be helpful in estimating the response of visual improvement to the surgical therapy in the early and late periods.
•
The intermediate period which represents the postoperative first year was found the most prominent interval evaluating the prognosis of visual recovery. No significant improvement was seen in the late period (over 3 years).
•
Age, duration of the symptoms, and tumor volume affect the visual recovery however tumor volume seems to be the featured parameter.

Background

Postoperative visual recovery in patients with pituitary adenoma can be influenced by the duration of symptoms, age, and tumor volume. Diffusion tensor imaging (DTI) allows visualization of white matter structure along with quantitative information. The aims of our study were to predict the visual recovery process in the early and long-term periods and to define the parameters affecting the recovery course.

Methods

A total of 200 patients with pituitary macroadenomas underwent endoscopic transsphenoidal surgery between January 2009 and July 2016. DTI and visual analysis including visual acuity and visual field analyses were performed for these patients at 5 periods, which included 3 years of follow-up. The effects of age, duration of symptoms, and tumor volume on visual recovery were evaluated.

Results

Mean tumor volume was calculated as 8871 ± 2758 mm³ and mean symptom duration was 23.41 ± 3.72 weeks. Mean age of the patients was 43.8 ± 8.9 years in the full recovery group and 48.7 ± 15.1 years in the nonrecovery group. Visual field analysis results on a Humphrey visual chart showed a significant linear strong correlation with fractional anisotropy (FA) values and a reverse strong correlation with mean diffusivity (MD) values on DTI magnetic resonance. DTI FA and MD cutoff values for each group were respectively determined as 0.373 and 1386 (×10^–6 mm²/second) for the preoperative period, 0.423 and 1383 (×10^–6 mm²/second) for the initial period, 0.428 and 1265 (×10^–6 mm²/second) for the early period, 0.432 and 1238 (×10^–6 mm²/second) for the intermediate period, and 0.437 and 1198 (×10^–6 mm²/second) for the late period.

Conclusions

DTI can assess and predict visual recovery after endoscopic transsphenoidal surgery of patients with pituitary macroadenomas causing chiasmal compression. FA values lower than or MD values greater than the cutoff values of the specific period reflect poor prognosis. Tumor volume was found to be the featured parameter that affects visual recovery. The postoperative first year is the most prominent interval evaluating the prognosis of visual recovery.

Introduction

Visual field (VF) defects and loss of visual acuity are among the most important clinical signs of pituitary macroadenomas compressing the optic chiasm.1, 2, 3, 4, 5, 6, 7, 8 Impaired and disrupted signal conduction along the axons are the manifestations of axonal injury from a compressive chiasmal lesion.⁵ Several studies have assessed the degree of visual dysfunction and recovery after surgical decompression and reported structural and functional changes in axonal flow.8, 9

VF analyses in preoperative and postoperative periods provide a standard quantitative method of evaluating the progression of VF loss.¹⁰ Duration of recovery in VF after surgery in patients with pituitary adenoma remains unclear.

Diffusion tensor imaging (DTI) is a noninvasive and relatively new magnetic resonance (MR) technique used for assessing structural changes in optic pathways as well as white matter fiber structures.2, 11, 12, 13, 14 Thus, quantitative information can be obtained about the white matter structures.

DTI is an extension of diffusion-weighted imaging in which 6 or more measurements probe diffusion in different directions. Quantitative assessment for the characterization of axonal architecture can be performed via DTI fractional anisotropy (FA) and mean diffusivity (MD) measurements.¹⁵ FA is a measurement of anisotropy and represents the degree of variation among fiber tracts and reflects the integrity of the structures. The DTI parameters show alterations with an increase in MD, a measure of the average molecular motion, and a decrease in FA, a measure of the preponderance of diffusion direction when white matter tracts are destructed or when there is a change in the permeability of the axonal membrane.12, 15, 16, 17, 18, 19, 20, 21

In our earlier study of 72 patients with pituitary adenomas causing visual impairment on the preoperative and postoperative second day,¹¹ the sixth month showed a correlation among DTI-derived FA values of the optic nerves and visual parameters. We proposed that DTI-derived FA and MD values of the affected side may be helpful in estimating the response of visual improvement to surgical therapy in the early period. In our previous study, the number of participants was limited and progress was assessed up to 6 months. We therefore performed DTI in 200 patients with macroadenomas, including the 72 patients from the previous study, preoperatively, on the second postoperative day, sixth month, first year, and 3 years and extended the recovery course over 3 years in 4 periods. We updated our DTI cutoff values for each time interval and evaluated both early and late outcome. The degree of visual recovery was observed to correlate with age, tumor volume, and duration of symptoms. The aims of the present study were to determine the predictive factors affecting visual recovery and to evaluate the process of remyelination quantitatively using the cutoff values provided by DTI parameters and to define the duration of recovery in VF recovery after surgery in patients with pituitary adenoma.

Section snippets

Methods

A total of 1381 patients underwent endoscopic transsphenoidal surgery between January 2009 and July 2016 at Kocaeli University Pituitary Research Centre and Neurosurgery Department, Turkey.

Patients with pituitary macroadenomas causing chiasmal compression and who were operated on by endoscopic transsphenoidal approach initially in our department and followed up for at least 3 years were included in the study. Exclusion criteria included radiation therapy, reoperation because of recurrence or

Duration of Symptoms, Age, and Tumor Volume Results

Mean symptom duration in all patients was 23.41 ± 3.72 weeks, including 16.9 ± 13.5 weeks in the full recovery group, 19.3 ± 13.7 weeks in the partial recovery group, and 25.2± 7.8 weeks in the nonrecovery group. There was a significant difference among the groups in terms of symptom duration (P < 0.01).

Mean age of the patients was 43.8 ± 8.9 years in the full recovery group, 45.1 ± 13.6 years in the partial recovery group, and 48.7 ± 15.1 years in the nonrecovery group. When age was considered

Evaluation of Predictive Factors on Visual Recovery

Pituitary macroadenomas may compress anterior visual pathways and cause visual impairment.11, 13, 14, 17, 18, 23 There are conflicting reports in the literature that have shown few parameters to be predictive, including preoperative degree of visual loss, duration of symptoms, and size of tumor, which have been correlated with the postoperative recovery course. Some investigators have reported that age and preoperative visual loss are predictive parameters, whereas others did not find any

Conclusions

In this study, we updated our previous cutoff values of FA and MD parameters and added long-term results in a wider group of 200 patients. These cutoff values may predict the visual recovery at any period.

The intermediate period, which represents the first postoperative year, was the most prominent interval evaluating the prognosis of visual recovery. No significant improvement was seen in the late period.

Age, duration of symptoms, and tumor volume affect visual recovery; however, tumor volume

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Can Preoperative Diffusion Tensor Imaging Tractography Predict the Visual Outcomes of Patients with Pituitary Macroadenomas? A Prospective Pilot Study
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Visual impairment has been reported as the most common clinical manifestation of pituitary adenoma (PA) due to the compressive effect of the tumor. This prospective study aimed to evaluate the predictive role of diffusion tensor imaging (DTI) in the visual improvement of patients with PA, who were candidates for endoscopic endonasal surgery.
A total of 13 patients (male, 8; female, 5) with visual impairment due to pituitary macroadenoma were enrolled in this study. The DTI findings and visual parameters, including visual acuity (VA), visual field (VF), and visual evoked potential (VEP), were recorded for all participants before and 3 months after surgery.
Significant recovery was reported in both VA and VF following PA surgery (P < 0.001). The results of perimetry indicated recovery in all quadrants, except for the lower nasal quadrant of the right eye. The tumor volume showed no significant association with the preoperative optic nerve, optic tract, and chiasm fractional anisotropy (FA) or mean diffusivity (MD). The VA and VF recoveries were more likely in patients with a lower preoperative optic nerve MD. Besides, increased preoperative FA of the optic nerve was associated with a higher probability of VA recovery. No significant correlation was found between the optic tract MD and FA values and visual improvement. Overall, MD values below 0.0021 and FA values above 0.1689 could predict a good prognosis of VA recovery after surgery.
DTI may have a predictive value in estimating visual improvement in patients with PA preoperatively.
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Visual acuity (VA) and visual field defects (VF) are evaluated in the preoperative management of non-functioning pituitary adenoma (NFPA). The former is less studied than the latter.
To analyze preoperative factors, including adenoma volumetry, associated with reduced VA and postoperative improvement of VA over five years after surgery.
Eighty-seven patients who had primary surgery for NFPA were retrospectively reviewed. Eyes were categorized by best/worse preoperative VA. Ophthalmology review was performed before surgery, at three months, one to two years, and five years post-surgery.
Reduced VA in any eye was present in 55%. VA of the worse eye improved in 77% and normalized in 54%. The majority improved within three months. Additional cases with VA improvement were seen at 1–2 years after surgery. No further improvement was seen five years after surgery. Fifty percent of patients with, per definition, normal preoperative VA showed improved VA postoperatively. Tumor height above the sella in the sagittal plane was the best radiological predictor of reduced VA. Volumetry did not add to accuracy. Age, sagittal tumor height and visual field defects were risk factors of preoperative reduced VA. No predictors of postoperative recovery were identified.
Half of patients with reduced VA recover fully. All patients, independent of age and degree of VA reduction, may improve. No predictors of recovery were found. Early improvement is common and improvement beyond two years is unlikely. The frequency of reduced VA is underestimated. The present results could be of value in pre- and postoperative counseling.
Recommendations for the diagnosis and radiological follow-up of pituitary neuroendocrine tumours
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Los tumores neuroendocrinos hipofisarios (TNEH) constituyen un grupo heterogéneo de tumores cuya incidencia ha experimentado un aumento progresivo a la que han contribuido técnicas de imagen más sensibles y mayor experiencia en neurorradiología en este ámbito. Aunque la mayoría de los TNEH son indolentes, algunos presentan un comportamiento agresivo y puede aparecer recurrencia tras la extirpación quirúrgica. Los cambios introducidos por la clasificación de la Organización Mundial de la Salud en 2017 y las controversias terminológicas con relación a los tumores neuroendocrinos hacen necesario actualizar las recomendaciones para el diagnóstico, el manejo pre y postoperatorio, y el seguimiento de respuesta al tratamiento de los TNEH. Este documento multidisciplinar, iniciativa del área de Neuroendocrinología de la Sociedad Española de Endocrinología y Nutrición (SEEN), se centra en los estudios neurorradiológicos de imagen médica para el diagnóstico, pronóstico y seguimiento de los TNEH. Se describen los requisitos básicos y aspectos que deben cubrir los estudios con resonancia magnética nuclear y se propone un informe mínimo de radiología que ayude al clínico en sus decisiones terapéuticas. Este trabajo complementa así el consenso entre el Área de Neuroendocrinología de la SEEN y de la Sociedad Española de Anatomía Patológica para el estudio anatomopatológico de los TNEH.
Pituitary neuroendocrine tumours (PitNETs) constitute a heterogeneous group of tumours with a gradually increasing incidence, partly accounted for by more sensitive imaging techniques and more extensive experience in neuroradiology in this regard. Although most PitNETs are indolent, some exhibit aggressive behaviour, and recurrence may be seen after surgical removal. The changes introduced in the WHO classification in 2017 and terminological debates in relation to neuroendocrine tumours warrant an update of the guidelines for the diagnosis, preoperative and postoperative management, and follow-up of response to treatment of PitNETs. This multidisciplinary document, an initiative of the Neuroendocrinology area of the Sociedad Española de Endocrinología y Nutrición [Spanish Society of Endocrinology and Nutrition] (SEEN), focuses on neuroimaging studies for the diagnosis, prognosis and follow-up of PitNETs. The basic requirements and elements that should be covered by magnetic resonance imaging are described, and a minimum radiology report to aid clinicians in treatment decision-making is proposed. This work supplements the consensus between the Neuroendocrinology area of the SEEN and the Sociedad Española de Anatomía Patológica [Spanish Society of Pathology] for the pathological study of PitNETs.
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Citation Excerpt :
It is still not known whether the retinal vessel density damage occurs before or after RNFL and GCC loss or dysfunction; large-scale multicentre cohort studies are still needed to confirm this in the future. Anik et al. [38] reported that the rapid recovery of visual function in the early stage after relief of optic chiasm compression may be related to the recovery of myelinated axons that were not completely damaged and to myelin regeneration. Based on our findings, we speculate that more abundant blood flow in the optic papillary area before surgery may be more conducive to restoration of signal transduction and myelin regeneration.
Pituitary adenomas are known to cause optic chiasmal compression leading to visual field (VF) defects. Herein, we analysed the factors influencing early VF recovery following transsphenoidal surgery and explored the significance of retinal vessel density parameters in predicting prognoses. We collected data of 50 patients with pituitary adenoma and an abnormal VF prior to surgery. Patients were categorised into VF recovery (n = 25) and non-recovery (n = 25) groups within 1 week postoperatively. The VF, optic chiasm form, tumour volume, retinal thickness, and vessel density parameters were measured. The χ² test was used for single-factor analyses, and odds ratios (ORs) for each factor were calculated. Logistic regression was implemented to determine interactions between radial peripapillary capillary (RPC) density and other factors. Tumour volume (≥5 cm³, OR = 5.09), duration of visual symptoms (≥6 months, OR = 6.00), preoperative VF (mean deviation [MD] < -10 dB, OR = 6.77), thin retinal nerve fibre layer (OR = 9.04), ganglion cell layer complex thickness (OR = 7.67), and RPC density (whole ≤ 48%; OR = 15.58; temporal ≤ 49.3%; OR = 14.64) were found to be risk factors for postoperative VF recovery. After adjusting for these factors, RPC density was a dependent factor affecting VF recovery in patients with pituitary adenoma. RPC density seemed to be a stronger indicator than preoperative MD, tumour volume, duration of visual symptoms, or retinal thickness for predicting early VF recovery following optic chiasm decompression, thus helping surgeons determine the optimal timing of surgery and formulate effective treatment plans.
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: Conflict of interest statement: The authors declare that the article content was composed in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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Original ArticleVisual Outcome of an Endoscopic Endonasal Transsphenoidal Approach in Pituitary Macroadenomas: Quantitative Assessment with Diffusion Tensor Imaging Early and Long-Term Results

Highlights

Background

Methods

Results

Conclusions

Introduction

Section snippets

Methods

Duration of Symptoms, Age, and Tumor Volume Results

Evaluation of Predictive Factors on Visual Recovery

Conclusions

Am J Ophthalmol

Magn Reson Imaging

Neuroimage

J Neurol Sci

J Magn Reson

Neurotherapeutics

Neuroimage

Exp Neurol

Neuroimage

Neuroimage

Chiasmal syndromes

Curr Opin Ophthalmol

The time course of visual field recovery following transphenoidal surgery for course of visual field recovery following transphenoidal surgery for pituitary adenomas: predictive factors for a good outcome

J Neurol Neurosurg Psychiatry

Neuro-ophthalmology for neuroradiologists

AJNR Am J Neuroradiol

Dynamics of visual improvement following chiasmal decompression. Quantitative pre- and postoperative observations

Acta Ophthalmol Scand

Transsphenoidal decompression of the optic nerve and chiasm: visual results in 62 patients

J Neurosurg

Visual defects in patients with pituitary adenomas: the myth of bitemporal hemianopsia

AJR Am J Roentgenol

The time course of visual field recovery and changes of retinal ganglion cells after optic chiasmal decompression

Invest Ophthalmol Vis Sci

Predictive factors for vision recovery after optic nerve decompression for chronic compressive neuropathy: systematic review and meta-analysis

J Neurol Surg B Skull Base

Predicting impairment of central vision from dimensions of the optic chiasm in patients with pituitary adenoma

Acta Neurochir (Wien)

Evaluation of early visual recovery in pituitary macroadenomas after endoscopic endonasal transphenoidal surgery: quantitative assessment with diffusion tensor imaging (DTI)

Acta Neurochir (Wien)

Quantitative fiber tracking analysis of the optic radiation correlated with visual performance in premature newborns

AJNR Am J Neuroradiol

Visual pathway impairment by pituitary adenomas: quantitative diagnostics by diffusion tensor imaging

J Neurosurg

Original Article
Visual Outcome of an Endoscopic Endonasal Transsphenoidal Approach in Pituitary Macroadenomas: Quantitative Assessment with Diffusion Tensor Imaging Early and Long-Term Results