Open Access
05.04.2021 | Case Report - Brain Tumors
Provocation and prediction of visual peripersonal neglect-like symptoms in preoperative planning and during awake brain surgery
verfasst von:
Viktória Tamás, Gabriella Sebestyén, Szilvia Anett Nagy, Péter Zsolt Horváth, Ákos Mérei, Francesco Tomaiuolo, Giovanni Raffa, Antonino Francesco Germanó, András Büki
Neglect is a severe neuropsychological/neurological deficit that usually develops due to lesions of the posterior inferior parietal area of the right hemisphere and is characterized by a lack of attention to the left side. Our case is a proven right-handed, 30-year-old female patient with a low-grade glioma, which was located in the temporo-opercular region and also in the superior temporal gyrus of the right hemisphere. Upon presurgical planning, the motor, language, and visuospatial functions were mapped. In order to achieve this, the protocol for routine magnetic resonance imaging and navigated transcranial magnetic stimulation has been expanded, accordingly.
This article is part of the Topical Collection on Brain Tumors
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Introduction
Recent clinical studies suggest the important role of supramaximal safe tumor resection in increasing life expectancy of patients with low-grade gliomas. During extended resective surgery, it is of utmost importance to spare functionally eloquent areas. This goal is best achieved by awake surgery, aided by intraoperative neuromonitoring and cognitive assessment. Neglect is a severe neuropsychological/neurological deficit characterized by the lack of attention for the left side of the space. It develops as a result of a lesion at the posterior section of the inferior-parietal region mostly of the right hemisphere [1, 6, 8].
Case report
Subject
A 30-year-old right-handed female has been diagnosed with a suspected low-grade glioma of the temporo-opercular region and superior temporal gyrus of the right hemisphere, affecting both cortical and subcortical areas. The patient has provided an informed consent acknowledging purported defect in the visual field.
Anzeige
Mapping of the eloquent areas
Preoperative imaging workup included structural magnetic resonance imaging (MRI), diffusion tensor imaging (DTI) to evaluate white matter tracts and functional MRI (fMRI) to investigate neural correlates of the sensory language area.
Cortical mapping was performed with nTMS using Navigated Brain Stimulation system combined with the NEXSPEECH® module to locate the motor cortex, areas of language dominance, and those regions susceptible to neglect.
Although the patient was right-handed, language testing was necessary because the tumor was located in a Wernicke-homologue area, which (in a minor region) showed activation during comprehension of speech targeted fMRI testing. Mapping was performed on both hemispheres according to the previously published protocol [5] using trains consisting of 5 Hz/5 pulses, while the patient was performing an object naming test.
The examination of visuospatial capabilities was especially important because the tumor affected the neglect circle—although a less sensitive and less extensive region of it, while, in general, it was close to those structures which were widely associated with severe neglect syndrome [7].
Anzeige
During testing for neglect, 44 stimulation target points on the parietal region of the right hemisphere were defined, where a total of 140 stimuli were delivered while the patient was asked to evaluate the length of 80 differently mid-transected line (‘equal’; ‘left’ = left is longer; ‘right’ = right is longer). The pictures have been presented randomly. To aid the inhibitory effect a train of 10 Hz/5 pulses was used, with 100% of resting motor threshold.
Visual and verbal stimuli
Pre- and intraoperative mapping of neglect-eloquent areas were performed by a line bisection judgment task, referred to as the landmark task according to descriptions [2‐4].
Our own image library was built by the adaptation of NBS system. Horizontal black lines were split with a vertical line on a white background (Fig. 1).
Fig. 1
Line bisection judgment task, referred to as the landmark task to pre- and intraoperative mapping
×
Wrong judgment of length or the lack of answer were considered errors (neglect and non-neglect specific). Neglect-specific errors were categorized as follows: (1) longer left lines were named as equal; (2) longer left lines were named as longer right lines; (3) equal length lines were named as longer right. Non-neglect specific errors were categorized similarly: (1) longer right lines were named as equal; (2) longer right lines were named as longer left lines; (3) equal length lines were named as longer left.
Neuropsychological evaluation
Mapping of neurocognitive and other psychological functions was performed 2 days prior to, as well as 4 and 5 days after surgery.
A variety of neuropsychological tests were performed for evaluating global neurocognitive functioning. (See Supplementary mat. 1).
To assess visuospatial attention abilities and to detect neglect symptoms, line bisection test (visuospatial attention) and Bells Test (visuospatial attention) were included in our battery. These tests have been performed multiple times following surgery to monitor peripersonal visual neglect symptoms more closely.
Results
Preoperative phase
On fMRI, a right-sided subdominant activity appeared by the posterior-inferior margin of the lesion, besides the left-sided dominant Wernicke activation, which was not confirmed with nTMS (Fig. 2a).
Fig.2
a Simultaneous left-sided dominant Wernicke activation and right-sided subdominant activity at the margin of the mass lesion. b Tractrogram of fiber network of FLS. c Tractrogram of fiber network representing the pyramidal tract. d Tractrogram of fiber network representing the tract system projected from the nTMS spots. e Errors in line bisection test during rTMS stimulation. Neglect specific errors are marked with yellow; non-neglect specific errors are marked with orange, delayed reaction times are marked with green
×
Anzeige
Superior longitudinal fasciculus (FLS) and pyramidal tracts were intact by using DTI and fMRI—a finding confirmed by nTMS examination, too (Fig. 2b–d). A cluster of neglect-like and not neglect-specific spots (4 targets) were identified at the inferior parietal region (Table 1; Fig. 2e). These spots were used for tractographic analysis and for navigation during surgery. Furthermore, activation of other areas (6 instances, e.g., frontal lobe) was recognized, although more scattered than at previously mentioned areas.
Table 1
Parameters of neglect and non-neglect specified errors
Total line length (mm)
Left side (mm)
Right side (mm)
Error
Neglect (yes/no)
196
106
90
Delay
Yes
159
82
77
Equal
Yes
196
92
104
Equal
No
106
50
56
Equal
No
Significant neurological and neuropsychological disorder, which refers to contraindication in relationship with the examinations, could not be detected at the patient. Neglect-like symptoms have not been observed and motor functions seemed intact.
Intraoperative phase
The asleep-awake-asleep operation was planned based on tractography and navigational MRI sequences. During the operation, frameless navigation-guided temporal craniotomy was performed; next functional areas were identified by bipolar fork probe using continuous cortical and subcortical stimulation. During intraoperative stimulation, we were not able to provoke speech error at the location (posterior portion of the superior temporal gyrus) according to nTMS results.
Initially, we barely found symptoms of neglect (1%) during intraoperative cortical mapping, while the rate of non-neglect specific errors was 22%. Contrarily, during the resection of the rear pole of the tumor, number of neglect specific errors increased significantly (+ 46%), while the number of non-neglect specific errors changed slightly (+ 3%). However, this location was further away from the area identified with nTMS as susceptible to neglect (inferior parietal lobule). Due to the transient manner of errors during the stimulation of this area, the resection was carried on. Using the acquired information, maximal safety was achieved during the resection. Postoperative MRI scan at 24 h confirmed total resection of the tumor (Fig. 3).
Fig. 3
a, b T1-weighted contrast-enhanced MRI scan at preoperative phase demonstrate typical appearance of a low-grade glioma without any accumulation of the contrast medium. c, d T1-weighted contrast-free follow-up MRI scan 24 h after surgery revealed gross total removal of the tumor with thin hyperintense line indicative of minimal blood accumulation in the tumor bed
×
Anzeige
Postoperative phase
MR imaging 24 h postoperatively
MRI showed postoperative changes with T1 hyperintensivity on the surface of the resection site as a sign of accumulated blood. FLAIR showed intensity of about 16 × 6 mm in size in the area constructing the lateral wall of the posterior horn the right lateral ventricle. Presence of some postoperative air in front of the frontal poles was described.
Neuropsychology
Twenty-four hours after the surgery a moderate ego- and allocentric visual neglect has been detected peripersonally, for the left side of the space, which was clearly observed in the behavior of patient (e.g., the bisection of horizontal lines were happened from right side to the left side) and also in the recorded tests (an obvious, average orientation of 2.5 cm for right side in the line-bisection test, and weaker performance with 40% in the Bells test due to the omission of the left elements). The patient lies on the right side of the bed, despite the fact that the surgical scar was also located on the right side of her head. Nevertheless, personal and/or extrapersonal neglect syndrome was not perceived by the clinical observation.
On the fourth day following the operation (more than 72 h later), visuospatial capabilities show a significant improvement (number of identified elements in the left visual filed was increased with 17% in the Bells test); however, vision problems are still indicated by the patient (“Something is weird”); therefore, a confrontational visual field exam was completed based on the Dean-Woodcock Neuropsychological Battery. Complete right and left side, as well as simultaneous (concomitant, extinction) testing of the upper, middle, and lower visual fields shows partial left homonymous hemianopia in the patient (total left: point = 0, “w” value = 415/severe; total simultaneous: point = 0, “w” value = 429/severe; total right: point = 24, “w” value = 488/normal zone).
It is of note that on the basis of surgical planning based on preoperative assessment of optic radiation as well as postop MR images such partial visual field defect could well have been anticipated upon gross total tumor resection.
On the fifth day, the homonymous hemianopia was still detected, while the symptoms (and behavior) referred to the neglect completely disappeared. The Bells test has already performed correctly, with similar search strategy as before the surgery, and no significant difference was observed between the length of horizontal lines that have been halved in the line-bisection task.
Regarding the other neuropsychological functions, the pre- and postoperative results were summarized in Table 2. The alteration in visuospatial attention functions was illustrated in Fig. 4.
Table 2
Results of psychological tests
Preoperative assessment
Postoperative assessment
Cut-off scores
RAVLT1
7
6
6.7
RAVLT2
9
9
9.9
RAVLT3
9
10
11.4
RAVLT4
11
12
12.2
RAVLT5
12
11
12.7
RAVLTB
4
3
6.5
RAVLT6—immediate recall
11
8
11.2
RAVLT7—delayed recall
8
10
11.1
RAVLT—recognition (correct answers)
15 (+ 9 false intruses)
13 (+ 0 false intruses)
14.2
Five-point test (correct patterns)
13
16
> 10
Five point test—number of perseverations
0
0
< 2
Verbal fluency task—phonological part (FAS)—SUM
38
40
≥ 30
Verbal fluency task—semantic part (animal, vehicle, vegetable)—SUM
The alteration in visuospatial attention functions (the appearance of neglect-like symptoms). a Line bisection test—preoperative phase. b, c Line bisection test—postoperative phase. d Bells test—preoperative phase. e–g Bells test—postoperative phase
×
Conclusion
In this work, we have identified a complex pre-, intra-, and postoperative protocol for the assessment of neglect in conjunction with awake surgery upon gross total removal of a low-grade glioma. Navigated—MRI-based—transcortical magnetic stimulation has been included as integrated part of the preoperative workup and planning.
According to the pre- and intraoperative assessments and the results presented in this case, the applied paradigm was useful for identifying eloquent areas of visuospatial attention and had predictive value for the development of postoperative neglect-like symptoms. In addition to neuromonitoring, this was further improved by the surgical strategy followed in the intraoperative. Our case report supports the literature data that lesions of the superior temporal gyrus play less role in the appearance of permanent neglect-like symptoms, but rather can result in transient changes. The paradigms established here should aid supramaximal safe resection of tumors aiding prolonged survival and better quality of life of our patients.
Declarations
Ethics approval and consent to participate
All procedures performed in this study involving human participant were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards. For this type of study, formal consent is not required.
Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Mit der Zeitschrift Die Chirurgie erhalten Sie zusätzlich Online-Zugriff auf weitere 43 chirurgische Fachzeitschriften, CME-Fortbildungen, Webinare, Vorbereitungskursen zur Facharztprüfung und die digitale Enzyklopädie e.Medpedia.
Bis 30. April 2024 bestellen und im ersten Jahr nur 199 € zahlen!
Mit e.Med Neurologie & Psychiatrie erhalten Sie Zugang zu CME-Fortbildungen der Fachgebiete, den Premium-Inhalten der dazugehörigen Fachzeitschriften, inklusive einer gedruckten Zeitschrift Ihrer Wahl.
Mit e.Med Neurologie erhalten Sie Zugang zu CME-Fortbildungen des Fachgebietes, den Premium-Inhalten der neurologischen Fachzeitschriften, inklusive einer gedruckten Neurologie-Zeitschrift Ihrer Wahl.
Mit e.Med Orthopädie & Unfallchirurgie erhalten Sie Zugang zu CME-Fortbildungen der Fachgebiete, den Premium-Inhalten der dazugehörigen Fachzeitschriften, inklusive einer gedruckten Zeitschrift Ihrer Wahl.
Provocation and prediction of visual peripersonal neglect-like symptoms in preoperative planning and during awake brain surgery
verfasst von
Viktória Tamás Gabriella Sebestyén Szilvia Anett Nagy Péter Zsolt Horváth Ákos Mérei Francesco Tomaiuolo Giovanni Raffa Antonino Francesco Germanó András Büki
Patienten, die von Ärztinnen behandelt werden, dürfen offenbar auf bessere Therapieergebnisse hoffen als Patienten von Ärzten. Besonders gilt das offenbar für weibliche Kranke, wie eine Studie zeigt.
Akuter Schwindel stellt oft eine diagnostische Herausforderung dar. Wie nützlich dabei eine MRT ist, hat eine Studie aus Finnland untersucht. Immerhin einer von sechs Patienten wurde mit akutem ischämischem Schlaganfall diagnostiziert.
Wenn unter einer medikamentösen Hochdrucktherapie der diastolische Blutdruck in den Keller geht, steigt das Risiko für schwere kardiovaskuläre Ereignisse: Darauf deutet eine Sekundäranalyse der SPRINT-Studie hin.
Ist die Tau-Last noch gering, scheint der Vorteil von Lecanemab besonders groß zu sein. Und beginnen Erkrankte verzögert mit der Behandlung, erreichen sie nicht mehr die kognitive Leistung wie bei einem früheren Start. Darauf deuten neue Analysen der Phase-3-Studie Clarity AD.
Update Neurologie
Bestellen Sie unseren Fach-Newsletterund bleiben Sie gut informiert.
