Evaluation of volume measurements of neuroanatomical structures related to speech in multiple sclerosis patients

TL;DR

This study compares brain volumes in MS patients and healthy individuals, finding significant shrinkage in speech-related brain regions among MS patients.

Contribution

The study expands on previous work by measuring more speech-related brain areas and identifying significant atrophy in multiple lobes in MS patients.

Findings

18 out of 26 speech-related brain regions showed significant volume decrease in MS patients.

Whole brain volume was reduced in the MS group compared to controls.

Atrophy was observed in frontal, temporal, and parietal lobes related to speech in MS patients.

Abstract

Individuals with multiple sclerosis (MS) may experience various speech-related issues, including decreased speech rate, increased pauses, and changes in speech rhythms. The purpose of this study was to compare the volumes of speech-related neuroanatomical structures in MS patients with those in a control group.

The research was conducted in the Neurology and Radiology Departments of Malatya Training and Research Hospital. The records of patients who presented to the Neurology Department between 2019 and 2022 were examined. The study included the magnetic resonance imaging (MRI) findings of 100 individuals, with 50 in the control group and 50 patients with MS, who had applied to the hospital in the specified years. VolBrain is a free system that works automatically over the internet (http://volbrain.upv.es/), enabling the measurement of brain volumes without human interaction. The acquired images were analyzed using the VolBrain program.

As a result of our research, a significant decrease was found in the volume of 18 of 26 speech-related regions in MS patients. It was determined that whole brain volumes decreased in the MS group compared to the control group.

In our study, volume measurements of more speech-related areas were performed, unlike the few related studies previously conducted. We observed significant atrophy findings in the speech-related areas of the frontal, temporal, and parietal lobes of MS patients.

Full text

Introduction

Multiple sclerosis (MS) is a chronic illness characterized by inflammation in the central nervous system (CNS) [1,2]. This disease affects approximately 2.8 million people globally and is commonly diagnosed in individuals between the ages of 20 and 50 years. It is more frequently diagnosed in women than in men [3,4].

MS is characterized by clinical symptoms arising from lesions of the brain or spinal cord [1,2]. The signs and symptoms of MS vary depending on the location and size of the lesions in the CNS that lead to plaque formation. These differences are unique to each individual [5]. People who suffer from MS typically experience a variety of symptoms that can be quite debilitating. These symptoms may include feelings of exhaustion, physical discomfort, problems with controlling the bladder and bowels, difficulties with thinking and emotions, issues with seeing clearly, and challenges with speaking and swallowing. Unfortunately, these symptoms can significantly interfere with the capacity to perform routine tasks and engage in normal daily activities [6,7].

Individuals with MS may encounter speech problems. Today, the dual-flow model proposed by Hickok and Poeppel is used to understand the functional neuroanatomy of speech [8]. Motor and sensory areas in the dual-flow model include the gyrus precentralis, gyrus frontalis superior, gyrus postcentralis, gyrus frontalis inferior, and gyrus temporalis superior areas as a highly complex brain network also consisting of the lobulus parietalis inferior and gyrus temporalis medius structures, which are responsible for language functions and the auditory processing of speech [9].

People with MS may experience communication difficulties, especially with speech. This can negatively impact their ability to participate in conversations [10]. Speech disorders negatively affect social life and quality of life [11]. Speech is a delicate motor skill that demands accurate muscle coordination. It has been observed that 40% of individuals with MS experience dysarthria. Spastic, ataxic, and mixed spastic-ataxic dysarthria are prevalent clinical symptoms. The most common symptoms of dysarthria in MS are impaired voice control, rigidity, defective articulation and impaired emphasis, excessive loudness changes, and slow-paced speech. As the disease progresses, speech symptoms may become more severe [10,12]. Reproducible brain volume analysis techniques can measure and track brain atrophy over time [13].

The purpose of this study was to compare the volumes of speech-related neuroanatomical structures in MS patients with those in a control group.

Materials and methods

The research was conducted in the Neurology and Radiology Departments of Malatya Training and Research Hospital. The records of patients who presented to the Neurology Department between 2019 and 2022 were examined. Ethical approval was obtained with the decision of the Malatya Turgut Özal University Non-Invasive Clinical Research Ethics Committee numbered 2022/18-173 and dated 01.11.2022.

This study included the magnetic resonance imaging (MRI) scans of 100 individuals, with 50 in the control group and 50 patients with the relapsing-remitting MS subtype. There is no definitive clinical or laboratory diagnostic test for MS disease, but the McDonald diagnostic criteria are generally used today [14]. Therefore, diagnostic criteria entailed parameters obtained via clinical, laboratory, and imaging methods. Individuals with mental retardation, hemiplegia, diseases that could affect brain volume, or a history of head trauma or cranial surgery were not included in the study. The control group comprised healthy individuals who were admitted to the hospital for headache or dizziness and underwent MRI scans that showed no cranial pathology. These individuals did not have any illnesses that would affect their speech and had not experienced any events that would impact speech.

MRI was performed by taking axial T1-weighted images with an Amira 1.5-T device (Siemens, Erlangen, Germany). The MRI protocol was as follows: 3D T1-MPRAGE TR (repetition time), 2200 ms; TE (echo time), 2.79 ms; flip angle (declination), 8°; field of view, 250 mm; number of sections, 192; section thickness, 1 mm; matrix, 205 × 320. The acquired images were analyzed using the VolBrain program.

VolBrain is a free system that works automatically over the internet (http://volbrain.upv.es/), enabling the measurement of brain volumes without human interaction. It automatically performs volumetric brain analysis on T1-weighted images [15].

In our study, using VolBrain, the superior frontal gyrus and its medial segment, opercular inferior frontal gyrus, orbital inferior frontal gyrus, triangular inferior frontal gyrus, precentral gyrus, gyrus postcentralis, postcentral gyrus medial segment, superior parietal lobule, precuneus, gyrus temporalis superior, temporalis medius, and gyrus temporalis inferior volumes were analyzed.

2.1. Statistical analysis

The study’s sample size was determined via power analysis using the G*Power 3.1 program, which calculated the minimum sample size required to be 80, with a minimum of 40 individuals in each group [16].

Data analysis was conducted using IBM SPSS Statistics 25. The analysis included the calculation of descriptive statistics using metrics such as number, percentage, mean, standard deviation, median, and range. To compare independent groups, the Mann–Whitney U test was utilized.

Results

This study included the MRI results of 100 individuals, with 50 healthy individuals in the control group and 50 patients with MS, who applied to the hospital in the specified years.

No statistically significant difference was detected between the patient and control groups according to age or sex (p > 0.05, Table 1). The groups showed homogeneous distribution for age and sex.

No statistically significant relationship was found between disease duration and Expanded Disability Status Scale scores in the patient group (p > 0.05, Table 2).

Significant differences were discovered between the patient and control groups in bilateral gyrus frontalis superior, superior frontal gyrus medial segment, opercular inferior frontal gyrus, and gyrus precentralis volumes when comparing the groups in terms of the lobus frontalis (p < 0.05) (Table 3).

There were significant difference in the volumes of certain brain regions between the patient and control groups. The medial segment of the bilateral postcentral gyrus, the superior parietal lobule, the precuneus, and the right postcentral gyrus in the lobus parietalis displayed significant differences (p < 0.05). However, no significant difference was detected in the volume of the left postcentral gyrus between the two groups (p > 0.05) (Table 4).

A statistically significant difference was found between the patient and control groups in bilateral gyrus temporalis superior and right gyrus temporalis medius volumes in the lobus temporalis (p < 0.05). However, no statistically significant difference was found between the patient and control groups for left gyrus temporalis medius and bilateral gyrus temporalis inferior volumes (p > 0.05) (Table 5).

When the volumes of neuroanatomical structures in the right and left hemispheres were compared in the patient group, the opercular inferior frontal gyrus, precentral gyrus, and postcentral gyrus volumes showed statistically significant differences between hemispheres (p < 0.05) (Table 6).

In the control group, a comparison of the volumes of neuroanatomical structures in the right and left hemispheres revealed statistically significant differences between certain areas. Volume differences were observed in the opercular inferior frontal gyrus, triangular inferior frontal gyrus, postcentral gyrus, superior temporal gyrus, and inferior temporal gyrus (p < 0.05) (Table 7).

Discussion

Since brain volumes and neurological functions are linked, speech disorders caused by MS and the volumes of speech-related brain regions may be related.

Many individuals with MS experience cognitive impairments. They may also display language difficulties, such as dysarthria or reduced fluency. Dysarthric speech, a motor speech disorder, is frequently seen in MS patients due to damage to the central and peripheral nervous systems [17]. According to the literature, symptoms of MS may include speaking slowly, making explosive sounds without joining syllables, and improperly stressing certain syllables due to a lack of coordination of speech muscles [18]. Our study was carried out retrospectively based on MRI data and no tests were conducted to evaluate speech and language disorders in the patients.

Brain atrophy is one of the essential findings in MS disease. Brain volume decreases progressively in MS patients. Research has found a notable connection between atrophy and neurological functions. For instance, certain cognitive abilities, such as visual-spatial memory and verbal memory, are linked to the size of particular areas of the cortex [19]. Furthermore, studies have indicated that issues like fatigue, memory capacity, depression, anxiety, and muscle difficulties are linked to brain volume [20–23]. In our study, significant atrophy findings were observed in the speech-related areas of the frontal, temporal, and parietal lobes of MS patients.

Studies have shown that 45% of MS patients have speech disorders [11]. Individuals with MS may experience various speech-related issues, including a decrease in speech rate, increased pauses, and changes in speech rhythms. Additionally, weakness in tone of voice and difficulty initiating speech are common speech impairments associated with MS [24]. Previous studies reported aphasia-like symptoms such as difficulty in naming objects or remembering words, decreased verbal fluency, repetition of words, and impaired spelling [25].

Measurements of various regions in the brains of MS patients were examined in previous studies. Pagani et al. [26] reviewed the MRI images of 466 MS patients and 279 healthy controls. In that study, a significant level of atrophy was detected in the right superior frontal gyrus, bilateral gyrus precentralis, and pars orbitalis section of the inferior frontal gyrus in MS patients compared to the control group. Similarly, in our study, bilateral gyrus precentralis volume decreased and bilateral volume loss was observed in the gyrus frontalis superior. The volume loss in the pars orbitalis part of the inferior frontal gyrus was not significant. In addition, in our study, the opercular part of the inferior frontal gyrus was significant in volume in the MS group compared to the control group. Among the findings of Pagani et al. [26], while the gyrus postcentralis, gyrus temporalis superior, and inferior were atrophied bilaterally in MS patients, the gyrus temporalis medius was significantly reduced only in the right hemisphere. Similarly, bilateral gyrus temporalis superior and right gyrus temporalis medius volumes were decreased in our study. The gyrus postcentralis volume was significantly reduced only on the right side. The change in the gyrus temporalis inferior was not significant.

In our study, the volume losses observed in the frontal, precentral gyrus, and precuneus of MS patients are similar to previous findings in the literature [27–29]. In addition, some studies have reported a decrease in left gyrus temporalis volume in MS patients [27,30]. In our study, only a reduction in the volume of the gyrus temporalis superior from the left temporal region was observed. In addition, no significant difference was found between the right and left temporal gyrus in the MS group.

As a result of our research, a significant decrease was found in the volumes of 18 of 26 speech-related regions in MS patients. It was determined that whole brain volumes were decreased in the MS group compared to the control group. However, the volume of the right gyrus temporalis medius was increased. Some functions in brain regions may be more dominant on the right or left side. Studies show that the right hemisphere has various language functions, but when the right is surgically removed, the left hemisphere can undertake those tasks [31]. The left gyrus temporalis medius being affected due to MS may have caused a compensation mechanism to develop in the right gyrus temporalis medius, which is associated with similar tasks [32].

In this study, volume measurements of more speech-related areas were performed in comparison to the few related studies conducted previously. Our study’s findings will contribute to future research. While our results are noteworthy, future studies could involve larger sample sizes and broaden the research by exploring the variances among different types of multiple sclerosis. Moreover, conducting speech tests on patients and investigating the correlation between their performance and brain volume could yield valuable insights.