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Ann Indian Acad Neurol
Ann Indian Acad Neurol
AIAN
Ann Indian Acad Neurol
Annals of Indian Academy of Neurology
0972-2327
1998-3549
Wolters Kluwer - Medknow India

39113364
AIAN-27-378
10.4103/aian.aian_44_24
Original Article
Study of Language Function in Bengali-Speaking Population with Motor Neuron Disease
Das Siladitya
Laha Debal
Sengupta Prasenjit
Department of Neurology, Burdwan Medical College, West Bengal, India
Address for correspondence: Dr. Siladitya Das, Saila Kunja, Ramkrishna Pally, Near Chowdhury Chira Mill, Kalna Road, Burdwan - 713101, West Bengal, India. E-mail: siladitya.das007@gmail.com
Jul-Aug 2024
08 8 2024
27 4 378383
16 1 2024
26 5 2024
11 6 2024
Copyright: © 2024 Annals of Indian Academy of Neurology
2024
https://creativecommons.org/licenses/by-nc-sa/4.0/ This is an open access journal, and articles are distributed under the terms of the Creative Commons Attribution-NonCommercial-ShareAlike 4.0 License, which allows others to remix, tweak, and build upon the work non-commercially, as long as appropriate credit is given and the new creations are licensed under the identical terms.
Background:

Motor neuron diseases (MNDs) have been traditionally considered to spare cognition. But recent findings show that multiple domains of cognition including language can be involved in MND patients. Most studies on language patterns of MND patients were conducted in Western nations, but data on Indian population is limited. This study is an attempt to explore the language functions of Bengali-speaking MND patients from this part of eastern India.

Objective:

To determine the prevalence and nature of language dysfunction in MND patients.

Materials and Methods:

A single-center, hospital-based, observational, cross-sectional study. The Bengali adaptation of the Western Aphasia Battery was administered to 50 cases diagnosed with MND, attending a tertiary care hospital consecutively over a 1-year period, and fulfilling the inclusion and exclusion criteria for the study. Descriptive and inferential statistics were used for expressing results.

Results:

Eighteen percent of cases showed impairments in spontaneous speech. Fluency was impaired in 72%, and 22% cases showed impaired naming. Moreover, 20% and 26% of cases were impaired in repetition and comprehension, respectively. Reading and writing was impaired in 16% and 26% of cases, respectively. Significant difference was found in the primary language skill scores and aphasia quotient across age groups, while no significant difference was found in these scores across education status.

Conclusions:

This study describes the language profiles of Bengali-speaking MND patients from eastern India, and the findings are similar to previous research works, which have shown morpho-syntactic, lexical-semantic, and phonological errors in language function.

Motor neuron disease
language
Bengali Speakers
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pmcINTRODUCTION

Classically, the motor neuron diseases (MND) have been considered to be characterized by progressive limb, bulbar, and respiratory muscle function loss caused by selective degeneration of upper and/or lower motor neurons with relative sparing of rest of the nervous system. But studies have shown that nonmotor regions of the nervous system, including that of language, may also be affected in the disease process. Up to 35%–40% of amyotrophic lateral sclerosis (ALS) patients display language deficits within the spectrum of primary progressive aphasias.[12] Language and executive functions are linked in MND, with executive functioning accounting for 44% of variance in language abilities in patients of MND. Study of both executive and language functions in MND patients is important as “predominantly dysexecutive” and “predominantly linguistic” cognitive profiles have been proposed.[3] Several studies have shown errors in writing sentences to dictation, spelling, sentence construction, grammar, and object naming errors in primary lateral sclerosis patients.[4] Patients with pure lower motor involvement performed better in phrase construction tasks compared to pure upper motor-involved patients.[5] Marginally significant difference between progressive muscular atrophy patients and healthy controls was found in naming tests.[6] Verbal fluency tasks demonstrated a link between executive functions and language. Some studies have suggested that errors in syntax/grammar processing reflect problems in sequencing and organization, which are executive in nature.[7]

Prevalence of language dysfunctions in MND patients is difficult to ascertain, and extensive studies are absent. Most relevant studies on cognitive patterns of patients with MND were conducted in Europe, North America, Japan, and China. Due to unique clinical characteristics, socioeconomic, educational, and cultural backgrounds, studies on Indian populations with MND are necessary. The cultural, food, exposure, and physiologic characteristics of rural-based Bengali speakers from eastern India differ in comparison to people from other parts of India. Therefore, this study is an attempt to explore the cognitive profiles and language functions of patients with MND from this part of eastern India, which would help conduct further future extensive studies to elucidate the patterns of dysfunction in cognition and language among such patients.

MATERIALS AND METHODS

A single-center, hospital-based, observational, cross-sectional study was conducted in the Department of Neurology in a tertiary care hospital in eastern India from January 2022 to February 2023, after proper permission was obtained from the Institutional Ethics Committee. Fifty consecutive clinically and electrophysiologically diagnosed cases of MND, aged above 18 years, with Bengali language as the mother tongue, attending the Neurology outpatient department and admitted in the departmental ward were chosen.

Cases with learning or intellectual disability, severe mental illness (schizophrenia spectrum disorders, psychosis, bipolar disorder, posttraumatic stress disorder with current flashbacks and/or hyperarousal, current substance abuse disorder, or active suicidal ideation), stroke, epilepsy disorder, organ failure, hydrocephalus, brain tumor or any other malignancy, complicated mild–moderate to severe traumatic brain injury, subjects on high dose of psychoactive medication, subjects with mother tongue other than Bengali, patients with renal disease or on dialysis therapy, and active coronavirus disease 2019-positive patients were excluded. Patients suspected to be having ALS were reviewed by the revised El-Escorial criteria. Demographic data, data on vascular risk factors, presenting symptoms, family history, clinical features, coexisting neurodegenerative clinical syndromes, severity of illness, neuroimaging, electromyography, and nerve conduction studies were the study variables.

Predesigned, semi-structured case record forms and informed consent forms were used. As Bengali-speaking patients were selected for the study, data of language examination in this study was taken according to the Bengali adaptation of the Western Aphasia Battery (B-WAB).[8]

Spontaneous speech was assessed by response to six questions and stimulus picture. Auditory verbal comprehension was scored based on the response to “yes–no” questions, asking the patient to point to real and pictured objects, forms, letters, numbers, colors, and body parts. Sequential commands were tested by commands of progressive syntactic complexity. Repetition was similarly tested by asking the patient to repeat words and sentences. Naming was assessed by object naming, naming of domestic animals, sentence completion, and responsive speech. Reading was assessed by asking the subjects to choose the best response after reading given sentences, perform actions after reading aloud given commands, match real objects and printed pictures placed in front of the patient with written word stimulus, match written words with picture stimulus, discriminate letters, and perform spelled word recognition tasks. Writing was assessed by asking the patients to write on request, checking the written output, asking them to write to dictation, asking to write alphabets, numbers, and copying of words of a sentence. Apraxia was tested. Constructional, visuospatial, and calculation tasks were also applied. Aphasia quotient (AQ) was calculated for every patient. Patient’s subscores for spontaneous speech, comprehension, repetition, and naming were noted. Individual subscores of “yes/no questions,” “auditory word recognition,” and “sequential commands” under comprehension heading were totaled and divided by 20. Score of repetition was divided by 10. Sum of total scores of naming subparts was divided by 10. These were compiled to get a total, which was multiplied by 2 to get AQ. Detailed general clinical and neurologic examination was done.

Neuroimaging and blood tests to rule out secondary causes of impaired cognition and language function were done. Magnetic resonance imaging (MRI) of the brain was done by GE SIGNA EXPLORER 1.5 T and computed tomography scan of the brain by Hitachi Scenaria 128 slice machines. Electromyography was done by RMS ALERON 401 and nerve conduction study by RMS ALERON 401. Blood tests for assessing secondary causes of impaired cognition, including complete blood count, erythrocyte sedimentation rate, and differential lymphocyte count, fasting and postprandial blood sugar, glycated hemoglobin, serum urea, creatinine, lipid profile, electrolytes, and liver function test were performed.

A flexible approach was followed for response collection, keeping in mind the individual patients’ physical abilities and limitations. Patients were divided into “Normal,” “Impaired,” and “Could not be assessed” subgroups based upon the response for each subtest. For those patients who had severe bulbar involvement, appropriate substitution test was tried by encouraging written response. Similarly, for “Yes/No” questions of auditory verbal comprehension subtest, either verbal or gestural response or response by eye blink was considered. Thus, the “Yes/No” question subpart could be assessed in cases with severe bulbar involvement also, as they responded by gesture or eye blink. Only cases with poor general health status could not be assessed. While in the auditory word recognition subtest and the sequential commands subtest, cases with poor general health status and severe limb involvement could not complete the whole subtest, those with bulbar involvement could respond. Those who could not complete the whole subtest were labeled as “Could not be assessed.” In some subtests, like those without appropriate substitution testing methods, or when subjects could not complete the subtest due to severe involvement of both bulbar and limb functions or overall poor general health status, the responses for those subtests were noted as “Could not be assessed” to avoid falsely counting them under the “Impaired” subgroup.

Statistical analysis of data

Mean/standard deviation (SD)/proportion/range were calculated. One-way analysis of variance was used to compare means and SDs. P value < 0.05 was taken as significant. Microsoft Excel 2021 was used.

RESULTS

Table 1 shows the distribution of the patients according to demographic and clinical characteristics.

Table 1 Demographic and clinical characteristics of the cases (n=50)

	Number	Percentage	
Sex	
    Male	37	74	
    Female	13	26	
Education	
    No formal education	14	28	
    Primary	17	34	
    Secondary	16	32	
    Higher secondary and above	3	6	
Toxin exposure	
    With H/O exposure	19	38	
    Without H/O exposure	31	62	
Smoking history	
    Present	12	24	
    Absent	38	76	
Mode of onset	
    Bulbar	14 (M=4, F=10)	28	
    Limb	36 (M=33, F=3)	72	
    Pure UMN	Nil	--	
    Pure LMN	Nil	--	
    UMN and LMN	50	100	
H/O=History of, UMN=Upper Motor Neuron, LMN=Lower Motor Neuron

Eighty-eight percent (88%) of the study population was rural based, while 12% (12%) hailed from urban areas. The mean age of our study subjects was 49.24 ± 11.34 years, and the age range was 18–97 years. The male to female ratio was 2.8:1. The mean educational years was 4.38 ± 1.132. The group comprised people with different education levels, that is, education up to primary level, up to secondary level, higher secondary and above education, and no formal education. Mean duration of the illness of the subjects was 2.396 ± 0.838 years. Subjects who had history of toxin exposure due to occupational causes were mainly exposed to organophosphorus (n = 8), organochlorine (n = 5), pyrethroid (n = 3) insecticides, herbicides, and pesticides. One case was a painter and one was a carpenter; they were exposed to organic solvents. One case was involved in transport of multiple types of pesticides and insecticides. Smoking was the common addiction among the study subjects. Seventeen cases with toxin exposure could be assessed, while two could not be assessed.

Clinically, cases with limb involvement at the onset of the disease outnumbered bulbar-onset cases. Bulbar onset was more commonly found in female subjects compared to male subjects. All the cases had combined upper motor and lower motor neuron involvement.

In the present study, spontaneous speech could not be assessed in eight (16%) study subjects. In 33 (66%) cases, it was found to be normal with sentences of normal length, complexity, without definite slowing, halting, or articulatory difficulty, and with reasonable complete description of the picture. In the nine (18%) cases with impaired function, some articulatory errors, incomplete description of the picture, and decrease in response to the information content questions were found.

The auditory verbal comprehension test could not be assessed in six (12%) cases. Thirteen (26%) cases had impairment in this subtest. Difficulty was seen in answering “yes” or “no” to last five questions of the auditory verbal comprehension subtest. The subjects showed difficulty in responding to cards having letters and cards having numbers in the auditory word recognition subtest. No difficulty was noted in the other parts of this test. In the sequential commands subtest, cases faced difficulty in the commands involving two or more objects and containing prepositions and conjunctions. More commonly, difficulty was seen in the last six commands in the subtest. Thirty-one (62%) cases performed normally.

Repetition could not be assessed in eight (16%) cases. Cases with impaired repetition (20%) showed errors in the order of word sequence or incomplete repetition. They faced difficulty in repeating sentences with four or more words. Repetition was found to be normal in 32 (64%) cases.

Naming could be assessed in 42 cases. Among them, 31 cases could name the objects presented correctly or with minor articulatory error. The 11 cases with impaired object naming required phonemic cues, but they did not have recognizable phonemic paraphasias. However, word fluency was impaired in 36 cases. Among them, the mean ± SD word fluency for animals was 8.7 ± 3.2.

Reading and writing could not be assessed in patients with no formal education. Cases with severe bulbar involvement could not be assessed for reading but writing subtest could be performed, while the reverse was true for those with severe dominant upper limb involvement. Cases with both severe bulbar and limb involvement or poor health status could not be assessed for both. Reading could not be assessed in 15 (30%) cases, while writing could not be assessed in 17 (34%) cases. Twenty-seven (54%) cases performed normally in reading subtest, and 20 (40%) cases performed normally in writing subtest. Eight cases had impaired reading and 13 cases had impaired writing. Cases with impaired reading mostly faced difficulty in the reading comprehension of sentences subpart. Writing errors consisted of spelling errors and errors in modifiers.

AQ could not be assessed in eight cases. Among the 42 assessable cases, the mean AQ was 91.3 and SD was 10.52.

The mean AQ among assessable toxin-exposed cases (n = 17) was 90.6 ± 10.79, while the mean AQ among assessable non–toxin-exposed cases (n = 25) was 91.8 ± 10.51. No significant difference (P = 0.72) was found between the two groups.

The mean scores of the primary language skills and AQ of the assessable cases were calculated across age groups and are presented in Table 2. Significant difference across age groups was noted for auditory verbal comprehension task (P = 0.03), repetition (P = 0.02), naming tasks (P = 0.03), and AQ (P = 0.004) of subjects. No significant difference across age groups was noted for the spontaneous speech task (P = 0.544).

Table 2 Mean score of primary language skills and AQ across age groups

Subtest	18-30 years	31-40 years	41-50 years	51-60 years	61-70 years	>70 years	
Spontaneous Speech (total score=20)	19.5±0.7	18.11±2.14	18.8±0.67	18.2±1.13	19±0.81	18.5±0.707	
Auditory Comprehension (total score=200)	199±1.4	141.5±61	180±34.16	195±8.4	197.5±3	155±35	
Repetition (total score=100)	98.5±0.9	76.2±3.09	91.2±1.51	88.3±1.95	97.5±5	95±7.07	
Naming (total score=100)	88±2.82	78±1.52	87.3±2.23	88.8±0.54	93.75±7.5	87.5±3.5	
AQ	96.6±0.848	82.33±6.95	92.50±7.37	90.52±5.53	96±3.09	89±1.414	
AQ=Aphasia quotient

Out of 14 cases with no formal education, six cases could not be assessed. For the remaining eight cases, the mean scores of primary language skill and AQ were calculated. Out of 36 literate cases, only 34 could be assessed. The mean scores of primary language skills and AQ for these 34 cases were calculated and compared to those of the eight illiterate cases to get P values as shown in Table 3. No significant difference was found in the primary language skills between literate and illiterate subjects.

Table 3 Mean score of primary language skills and AQ across education status

Subtest	No formal education (n=8)	Literate (n=34)	P	
Spontaneous Speech (total score=20)	18.37±1.06	18.61±1.299	0.63	
Auditory Comprehension (total score=200)	185.5±18.35	186.6±23.99	0.90	
Repetition (total score=100)	84.12±21	90.61±15.99	0.33	
Naming (total score=100)	88.38±3.7	85.73±17.47	0.67	
AQ	94.2±5.35	90.61±11.35	0.39	
AQ=Aphasia quotient

DISCUSSION

Our study describes the language function in Bengali-speaking MND cases.

The mean age of our study subjects and the male-to-female ratio are similar to those reported in an Indian study by Nalini et al.,[9] where the mean age was 46.2 ± 14.1 years (age range: 18–85) and male-to-female ratio was 3:1. A study by Rai et al.[10] showed similar findings. We found female predominance (71%) in the bulbar-onset MND cases. Bulbar-onset ALS is reported to be more commonly found (70%) in the female population, especially in those aged above 40 years.[10] Our results are consistent with those of Sondhi et al.,[11] who showed limb onset in 72% and bulbar onset in 28% of cases and bulbar variety to be more common in female cases.

Previous studies have shown the association of pesticides, herbicides, and organic solvents with the pathogenesis of MND.[121314] Consistent with these evidences, we found one-third of our study subjects to have been exposed to toxins such as organochlorines, organophosphorus, pyrethroids, and organic solvents. In contrast to the existing studies where both male and female subjects were reported to be affected, all our toxin exposed cases were male. This may be due to occupational and social patterns prevalent in this part of rural India. One-fourth of our study subjects were smokers. Smoking has been considered a risk factor for ALS in previous studies.[15]

In our study, we found language dysfunction in MND patients in the form of lexical-semantic, morpho-syntactic, and phonological errors. These findings are similar to the results reported in the existing literature.[16] We found evidence of difficulty in using action verbs in our subjects from their description of the stimulus picture. Previous observations show that the motor and premotor cortex play important roles in production of verbs describing bodily actions, and impairment of motor cortex in MND cases can lead to impaired action verb or body verb production.[17] Impairment of the picture description subtask in our MND cases not only suggests lexical defects, but also semantic errors. The picture used in B-WAB has been depicted keeping in mind the cultural appropriateness of this region. Our cases could not describe the objects, indicating semantic impairment. We found evidence of semantic defects in our study subjects from impairments of word fluency and object naming tasks also. This is consistent with previous studies.[181920] Rakowicz and Hodges[18] mentioned that the errors of naming were more semantic rather than phonological, and some of their patients showed category specificity.

Our cases showed spontaneous naming difficulties in object naming task, but had improved performance on phonemic cueing, indicating primary word retrieval impairment, which depends upon executive functioning. This is similar to the findings of Pinto-Grau et al.,[21] who showed improvement of naming function of their ALS cases with phonemic cues.

Our cases showed morpho-syntactic errors. We found impairment in both semantic and grammatical comprehension. Previous works have shown presence of impaired syntax comprehension in MND cases across different languages.[182223] Polar questions in Bengali can be formed by adding a polar question particle (PQP) along with change of intonation.[24] Our patients faced difficulty in answering questions formed by using the PQP “ki” in the “yes–no” subpart of auditory verbal comprehension subtest. They also showed errors in answering the “yes–no” subtest questions, where comparison between two objects was made by using the Bengali post-position “theke.” Bengali simple sentences morpho-syntactically have a head final or subject–object–verb order.[25] But barring the first two questions of the sequential commands subpart, the other commands had more than one object and verb. Difficulties of our cases in following commands containing two or more objects or having prepositions or post-position morphemes in the sentence reflect impairment of syntactical analysis and grammar. These findings are similar to that of Yoshizawa et al.,[26] who showed that grammatical or syntax comprehension abnormalities are more common for modifier words which can be prepositions or particles. Relation of executive dysfunction with errors of syntactical comprehension and associations of agrammatism with ALS-frontotemporal dementia continuum have been described in several studies.[32327]

Our cases show phonological component errors. Sentences in the repetition subtest use several consonant clusters and germinates. Our subjects demonstrated errors in repetition subtest, especially in sentences with more than four words in them. However, phonemic paraphasias were not seen in our cases, unlike previous studies.[16]

Our study found that over half of the subjects had normal reading function. This finding is similar to those reported in previous studies.[182228] Spelling errors among the subjects in whom writing could be assessed consisted mainly of errors in Bengali vowel modifiers. Pinto-Grau et al.[21] found spelling errors for regular words, while their ALS cases could spell correctly pseudo-words. But due to lack of irregular words in Bengali language, we could not assess the spelling for irregular words. Other studies show similar findings.[4] Educational level affected the reading and writing assessments of our subjects.

We correlated the primary language skills and AQ scores between literate and illiterate subjects in our study and found no significant difference. Correlation of the AQ scores between toxin-exposed cases and cases with no toxin exposure also showed no significant difference. Existing literature describes separately the effects of toxin exposure in pathogenesis of MND and the role of toxins in cognitive impairment. But there are no studies assessing the effect of toxin exposure on cognitive and language function in MND patients.

Our study had some limitations. It was a single-center, single-observer–based study and had small sample size. Longitudinal follow-up of the cases was not done. Other study designs with healthy controls would have yielded more information. As consecutive cases were taken, cases with dysarthria, severe limb involvement, and both limb and bulbar involvement were not excluded. Many cases not being able to complete several subsections of the test battery is also a limitation. Level of education of the patients was also a limiting factor. As premorbid education has an impact upon cognition as well as language functions, the study would have yielded more information if more subjects with higher secondary or above education level were present. There is lack of well-validated Bengali-translated versions of cognitive and language assessment tools for patients with MND, especially for assessment of language function in illiterate subjects. As such tools are lacking, further studies utilizing functional imaging like functional MRI and positron emission tomography can be conducted. The areas of brain activated in language processing in cases of MND can be assessed and elaborated in future studies using functional neuroimaging.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.
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