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Abstract

Background: Markers of phonological and articulatory processing, though at times difficult to identify, may be useful for the assessment of changes in the speech of people with mild cognitive impairment (MCI) and Alzheimer's disease (AD). Objective: To review the evidence on phonological and articulatory speech processing in older adults with MCI and AD and identify the most sensitive speech assessment tasks for detecting impairments in these abilities. Methods: This scoping review of the PubMed, Scopus, Lilacs, Web of Science, Google Scholar, ProQuest, and Embase databases was updated in April 2024. Studies of older adults with MCI and AD that evaluated articulatory or phonological aspects of speech were included in the review. Two independent reviewers used EndNote and Rayyan software to evaluate search results in a two-phase process, consisting of (1) title and abstract screening, and (2) full-text review. Results: Of the 163 studies retrieved, 41 were selected in Phase 1. At the end of Phase 2, 29 studies were included in the review. All studies included individuals with AD and only one also included participants with MCI. Normal phonological and articulatory performance was observed in MCI. In AD, phonological or articulatory alterations were associated with the speech assessment method, sample size, and diagnosis of atypical dementia. Conclusions: Phonological and articulatory changes may occur in AD but may be difficult to identify. Single repetition or naming tasks may be more sensitive for detecting these impairments.

Keywords

Alzheimer's disease cognitive dysfunction dementia language speech

Introduction

Phonological and articulatory impairments are common early symptoms of some types of dementia, including logopenic primary progressive aphasia, non-fluent primary progressive aphasia, and primary progressive apraxia of speech.^1–4 In typical Alzheimer's disease (AD), phonological alterations in language planning and articulatory alterations in phonetic-motor planning can be observed.^5,6 Studies that reported few impairments in phonological planning and articulatory processing in AD assessed participants using repetition tasks.^5,6 Studies that did not identify alterations in patients with AD evaluated speech using naming⁷ or discourse tasks.⁸

The description of behavioural markers of dementia and of the stages that precede the clinical presentation of the illness is highly valuable. Studies of the phonological and articulatory characteristics of speech in dementia focus predominantly on neurodegenerative illnesses with a clear early impact on oral communication that compromises independence in activities of daily living from the onset of symptoms.^1,2 In mild cognitive impairment (MCI), a condition characterized by cognitive decline determined by objective testing and an absence of functional impairment,^9,10 phonological and articulatory performance may be unaffected. No statistically significant differences in a sequential speech motion task were observed between people with MCI and those with subjective cognitive impairment or AD.¹¹ However, a study of individuals with and without cognitive decline suggested that anticipatory speech errors could be a phonological marker of cognitive dysfunction, as people with objective cognitive decline and no diagnosis of dementia or MCI exhibited mild phonological difficulties during the repetition of tongue twisters, displaying a unique pattern of anticipatory and perseverative errors.¹² Performance in sequential speech motion tasks can also be affected by AD, but these alterations are mild and do not result in a perceptible speech deficit in most cases of MCI or AD.¹¹ It appears that, in addition to the clinical diagnosis, the type of speech assessment task can help differentiate between phonological and articulatory impairments in order adults. Therefore, markers of phonological and articulatory processing, though at times difficult to identify, may be useful for the assessment of changes in the speech of people with MCI and AD.

MCI is associated with an increased risk of AD and a faster rate of cognitive decline.¹³ The early identification and differentiation of cases of cognitive decline with and without dementia is crucial for the timely implementation of cognitive interventions.¹⁴ As such, it is crucial that we determine the presence or absence of changes in phonological and articulatory planning in MCI and AD. It is unclear whether people with MCI experience alterations in phonological planning and articulatory processing, or which speech tasks can differentiate between such alterations in MCI and AD.

Language planning, including its semantic, morphological, syntactic, and, lastly, phonological aspects, takes place before motor planning.¹⁵ Alterations in the early stages of processing can contribute to difficulties in identifying and characterizing phonological and articulatory conditions in people with impairments in different stages of processing, especially when these impairments are mild. Phonological alterations in the selection and sequencing of phonemes, as in phonemic paraphasia, occur due to language impairment.¹⁶ These alterations in phonological processing include substitutions, anticipations, perseverations, transpositions, self-correction, and false starts.^15,17 Articulatory errors in the motor planning or programming stages are often seen in apraxia of speech, and occur due to issues in spatial and temporal motor commands causing sound distortions and slow speech, as well as extended segmental and intersegmental duration.^15,16 Figure 1 characterizes speech sensorimotor control.

Figure 1.

A model characterizing pathological speech sensorimotor control (following the four-level model of speech sensorimotor control, in Van der Merwe, 2009, 2021).^15,16

In light of these observations, this article aimed to conduct a scoping review of phonological and articulatory speech processes in people with MCI and AD, in addition to determining which speech assessment tasks are most sensitive to the phonological and articulatory impairments occurring in these conditions.

We hope to retrieve studies that rely on different speech assessment tasks to determine the presence or absence of various alterations in phonological and articulatory processing in the speech of people with MCI and AD.

Methods

This was a scoping review, developed based on the recommendations of the Preferred Reporting Items for Systematic Reviews and Meta-analyses Extension for Scoping Reviews – PRISMA-ScR.¹⁸

The protocol of this review was registered in the Open Science Framework (OSF identification number 10.17605/OSF.IO/Q3YDM).

Search strategy

The search was conducted on April 10, 2023, and updated on April 13, 2024. Studies were identified using a combination of controlled vocabulary, including Medical Subject Heading (MeSH) terms and Health Sciences Descriptors (Decs), and a series of free txt terms (Supplemental Material 1) such as ‘Alzheimer Disease’, ‘Cognitive Dysfunction’, ‘Articulation Disorders’, ‘Speech Sound Disorder’, and ‘Aged’, along with their corresponding translations in English and Spanish. Databases searched included Embase, Virtual Health Library (LILACS), PubMed/Medline, Scopus, and Web of Science. On the same date, a search of grey literature was conducted using Google Scholar and ProQuest (theses and dissertations) (Supplemental Material 1). We hand-searched the reference lists of relevant articles and contacted subject matter experts to refine the search strategy. References were managed and duplicates were removed using EndNote^®X7, following the Bramer method.¹⁹

Eligibility criteria

The inclusion criteria adopted in this study were defined according to the ‘PEOS’ acronym:

Population (P): Elderly people;

Exposure (E): Cognitive Dysfunction or Alzheimer's Disease;

Outcome (O): Articulatory or Phonological Disorders;

Studies (S): Primary studies – observational studies and case reports.

Selection criteria

Studies were selected according to the following inclusion criteria: samples of older adults with MCI or AD and characterization of phonological or articulatory speech processing.

No restrictions were placed on the year or language of publication.

Exclusion criteria were as follows: secondary studies; no assessment or description of phonological or articulatory speech processing; focus on stages that precede phonological planning (for instance, semantic or syntactic planning); samples of adults with subjective cognitive decline in the preclinical and asymptomatic stages of dementia, or with other neurological disorders; samples composed of children; or studies that analyzed speech without describing the performance of older adults with MCI or AD.

Articles were selected independently by two researchers (MLC and NCCR) using the Rayyan and End Note platforms, in a process composed of Stage 1: title and abstract analysis and Stage 2: full-text reading of selected articles. A consensus meeting was held at the end of each stage.

Data extraction

The first author extracted the following information from each article: authors; publication year; study country; study design; study objective; sample; instruments used to assess and characterize the phonological or articulatory aspects of speech; and results related to the phonological or articulatory performance of people with MCI or AD. The third author reviewed the extracted data. Information on the selected studies and their findings was organized in two tables, created by the first author and reviewed by the third author. Table 1 summarizes the characteristics of included studies, such as authors, publication year, country where the study was conducted, objective, sample, stage of phonological or articulatory processing evaluated, and speech tasks used for phonological or articulatory speech assessments. Table 2 presents the results of studies and is divided into three topics, two of which are central to our study, while the third is a complementary topic of this review. The topics are as follows: 1) results regarding the description of the presence or absence of phonological or articulatory alterations; 2) speech tasks assessed; 3) neuroanatomical and biomarker findings associated with phonological or articulatory processing.

Table 1.

Characteristics of studies included in this review on phonological and articulatory performance in Alzheimer's disease or mild cognitive impairment.

Author(s), year and country.	Study design	Objective(s)	Sample	Phonological (linguistic) or articulatory (motor) processing evaluated, tests used, and speech parameters assessed
Morris (1987), Canada²⁰	Cross-sectional	To investigate the association between articulation rate and memory span in people with Alzheimer's disease.	21 people with mild Alzheimer's disease and 21 matched control participants.	Phonological and articulatory processing. Digit span test. Articulatory rate during reading or number repetition. The number of digits spoken per second was calculated.
Murdoch et al. (1987), Australia²¹	Cross-sectional	To compare the performance of people with and without Alzheimer's disease on a language assessment battery.	18 people with mild Alzheimer's disease and 18 matched control participants.	Phonological and articulatory processing. The Neurosensory Center Comprehensive Examination of Aphasia battery, which includes 20 tests that assess comprehension, language production, retention of verbal material, reading, and writing. Verbal fluency subtest from the Western Aphasia Battery.
Massman et al. (1996), USA²²	Cross-sectional	To compare the neuropsychological performance of people with corticobasal degeneration and Alzheimer's disease with and without extrapyramidal symptoms.	21 people with corticobasal degeneration, 21 with Alzheimer's disease and no extrapyramidal symptoms, and 12 people with Alzheimer's disease and extrapyramidal symptoms. Groups were matched for age, educational level, and dementia severity (mild).	Phonological and articulatory processing. Several neuropsychological batteries, including: Boston Apraxia Examination assessment of ideomotor (buccofacial, limb) apraxia; Boston naming test; Verbal Series Attention Test (reciting the alphabet, counting backward, reciting days of the week and months of the year in forward and reverse order, counting backward from 100 by 3's, and alternately saying numbers and letters in order).
Chenery et al. (1996), Australia⁷	Cross-sectional	To investigate the progression of anomia in Alzheimer's disease and its association with disease severity and psycholinguistic impairments.	23 people with Alzheimer's disease: 8 with mild dementia, 6 with moderate dementia, and 9 with moderate-to-severe presentations. 23 control participants matched for age, sex, and education.	Phonological processing. Classification of errors in the Boston Naming Test. Error categories: semantic, phonological (phonemic, literal, and neologistic paraphasias, and phonemic letter cues), perceptual and no-relationship.
Croot et al. (2000), England²³	Case series	To analyze the speech of 10 people with effortful speech production, phonological disruption, or nonfluency with probable or autopsy-confirmed Alzheimer's disease.	10 people with Alzheimer's disease.	Phonological and articulatory processing. Conversational speech; single-word production in naming, reading, or repetition tasks; and automatic speech. Classification of phonological paraphasias, false start errors, word or phrase repetitions, circumlocutions, semantic paraphasias, and omissions.
Forbes et al. (2002), Scotland²⁴	Cross-sectional	To identify alterations in the spontaneous speech of people with minimal and mild Alzheimer's disease using a simple and complex picture description task, and to determine which errors may differentiate between patients and healthy older adults.	22 people with Alzheimer's disease (11 minimal and 11 mild) and 22 control participants.	Phonological and articulatory processing. Simple and complex picture description task. Assessment of 11 aspects of speech using a Likert scale ranging from 1 (severely impaired) to 7 (no impairment): melodic line, articulation, grammatical form, phrase length, paraphasias (phonological, semantic, and visual), word-finding difficulties, error monitoring, information conveyed, and information content.
Vliet et al. (2004), USA²⁵	Case series	To report on two cases of Alzheimer's disease presenting with phonological dyslexia.	2 people with Alzheimer's disease.	Phonological processing. Boston Naming Test, word association, category fluency, sentence repetition Analysis of phonological distortions (substitutions, additions, or omissions of one or more phonemes) during naming tasks.
Vliet et al. (2004), USA²⁶	Case study	To report on a case of Alzheimer's disease with severe impairment in nonword reading. To discuss the implications of current reading models based on a case of phonological dyslexia.	1 individual with Alzheimer's disease.	Phonological processing. Boston Naming Test; word association; category fluency; sentence, word, and non-word repetition; comprehension; spelling; reading comprehension; reading of words with regular and irregular spellings, and nonword reading; semi-directed interview; lexical decision; text reading; rhyme production and detection; multiple phonological manipulation tasks.
Forbes-McKay and Venneri (2005), Scotland²⁷	Cross-sectional	To collect normative data for an oral and written picture description task that assesses spontaneous language skills and determine the task's test-retest, inter-rater, and parallel form reliability. Additionally, cut-off scores were obtained and tested regarding their ability to detect subtle deficits that occur in the early stages of dementia.	240 healthy volunteers aged 18 to 90 years 30 people with Alzheimer's disease.	Phonological and articulatory processing. Analysis of melodic line, phrase length, articulation, grammatical form, phonological paraphasias, semantic paraphasias, visual paraphasias, word-finding delays, response to word-finding difficulties, information content, error monitoring, and information conveyed.
Gerstner et al. (2007), USA²⁸	Case study	To present a case of progressive loss of speech and other clinical features and neuropathological findings consistent with Alzheimer's disease.	One 87-year-old man.	Phonological and articulatory processing. Boston Diagnostic Aphasia Examination, assessment of orofacial movements and respiration, phonation, articulation, prosody, and diadochokinesis.
Warkentin et al. (2008), Sweden²⁹	Cross-sectional	To analyze articulation and pause times during a naming task and explore their association with cerebral blood flow in people with and without Alzheimer's disease.	49 people with Alzheimer's disease and 57 control participants.	Phonological and articulatory processing. AQT naming test by Harcourt Inc., containing 40 stimuli used to assess information processing speed. Acoustic analysis software was used to separate pauses from the remainder of participant responses, referred to as articulation time.
Weiner et al. (2008), USA³⁰	Cross-sectional	To analyze the clinical utility of language assessments of people with Alzheimer's disease performed by psychiatrists. To analyze the association between simple speech assessments and the degree of cognitive impairment in Alzheimer's disease.	486 people with Alzheimer's disease.	Phonological and articulatory processing. Analysis of articulation, word-finding ability, hypofluency, hyperfluency, and repetition by clinicians during the conduct of a mental status examination, in addition to a category fluency test.
Peters et al. (2009), Belgium³¹	Cross-sectional	To explore the underlying functional neuroanatomy of lexical-semantic and phonological processing in Alzheimer's disease.	10 people with Alzheimer's disease and 12 healthy adults matched for age and education.	Phonological processing. Repetition of words, wordlike nonwords, non-wordlike nonwords, and vowels.
Östberg et al. (2009), Sweden¹¹	Cross-sectional	To assess diadochokinesis rates in patients of a memory clinic.	89 people with mild cognitive impairment, 60 with subjective cognitive impairment, 58 with Alzheimer's disease, 13 with frontotemporal dementia, 7 with nonfluent primary progressive aphasia, and 9 with semantic dementia.	Phonological and articulatory processing. Sequential speech motion rate involving the repetition of the syllables ‘pataka’ for 10 s. Number of correct repetitions, transposed sequences, and incomplete sequences. Sequential speech motion rate was calculated as the number of correctly repeated sequences (’pataka’) per second.
Lira et al. (2011), Brazil⁸	Cross-sectional	To identify changes in the discourse of people with Alzheimer's disease.	64 people with Alzheimer's disease and 93 control participants.	Phonological processing. Description of ‘The Dog Story’ picture and analysis of lexical error subtype: word-finding difficulties, repetition, revision, semantic substitution, and phonemic paraphasia.
Cera et al. (2011), Brazil³²	Cross-sectional	To identify manifestations of apraxia of speech in people at different stages of Alzheimer's disease and analyze the similarities among these symptoms.	30 older adults with mild, 30 with moderate, and 30 with severe Alzheimer's disease.	Phonological and articulatory processing. Reading, automatic speech sequences, repetition, and connected speech tasks from the verbal and nonverbal apraxia protocol by Martins and Ortiz. Identification of substitutions, omissions, additions, self-corrections, attempts and starters, and repetitions.
Meilán et al. (2012), Spain³³	Cross-sectional	To assess the characteristics of expressive language impairments in people with mild Alzheimer's disease through regression analysis of acoustic speech parameters and performance in memory and language tests.	21 older adults with mild Alzheimer's disease.	Phonological and articulatory processing. A two-minute task involving reading a sentence aloud, completing a sentence, repeating sentences, and reading a paragraph of Don Quixote. Analysis of acoustic parameters including levels of fundamental frequency, shimmer, and jitter, and of aspects of prosody including time of voice, percentage with voice, percentage of voiceless segments, percentage of voice interruptions, percentage of phonation, and pauses in voice.
Cera et al. (2013), Brazil⁵	Cross-sectional	To investigate the presence of apraxia of speech and orofacial apraxia in people with Alzheimer's disease and determine whether apraxia severity is related to the severity of Alzheimer's disease.	30 older adults with mild, 30 with moderate, and 30 with severe Alzheimer's disease.	Phonological and articulatory processing. Boston verbal agility; reading, automatic speech sequences, repetition, and connected speech tasks from the verbal and nonverbal apraxia protocol by Martins and Ortiz. Identification of substitution, omission, addition, self-correction, attempt, starter, and repetition.
Chare et al. (2014), Australia³⁴	Cross-sectional	To assess the impact of new criteria for clinical diagnosis and explore clinicopathological correlates of frontotemporal dementia syndromes including primary progressive aphasias.	Out of 178 neuropathologically ascertained cases of frontotemporal dementia, 135 were reclassified using revised diagnostic criteria into behavioural variant, semantic variant, nonfluent/agrammatic variant, and logopenic variant primary progressive aphasia.	Phonological and articulatory processing. The presence of the following language features was analyzed: word-finding difficulties, apraxia of speech, agrammatism, anomia, impaired word comprehension, impaired object knowledge, phonological errors, impaired word or sentence repetition, impaired sentence comprehension, surface dyslexia, and dysgraphia.
Leyton et al. (2014), Australia³⁵	Cross-sectional	To identify specific and reliable linguistic markers of the logopenic and nonfluent variants of primary progressive aphasia; determine the linguistic impairments associated with a positive Pittsburgh compound B status; explore the clinical heterogeneity of these variants regarding imaging findings; and identify a specific linguistic marker for the diagnosis of logopenic variant primary progressive aphasia.	25 people with logopenic primary progressive aphasia, 23 with nonfluent primary progressive aphasia, and 15 control participants.	Phonological and articulatory processing. Aphasia Language Scale to determine the presence of motor speech disorders, phonological errors, agrammatism, and anomia; followed by naming, word and sentence repetition, and sentence comprehension tasks.
Funayama and Nakajima (2015), Japan³⁶	Case series	To present two cases of posterior cortical atrophy.	2 people with atypical focal cortical atrophy.	Phonological and articulatory processing. Sentence and nonword repetition, and subtests from the Standard Language Aphasia test by Hasegawa and colleagues (oral confrontation naming, word comprehension, auditory sentence comprehension, reading sentence comprehension, written naming, dictation of sentences, and calculation).
Mack et al. (2015), USA³⁷	Cross-sectional	To assess the distribution of word-finding pauses before the production of nouns and verbs in the speech of people with primary progressive aphasia and healthy adults, in addition to identifying neural correlates of these pauses.	12 people each with nonfluent and semantic primary progressive aphasia, 11 with logopenic primary progressive aphasia, and 12 control participants.	Phonological and articulatory processing. Narrating the story of Cinderella using at least 10 nouns and 10 verbs. The following variables were analyzed: words per minute, mean length of utterance, percent grammatical sentences, open: closed class ratio, noun: verb ratio, and total number of nouns and verbs produced. Pauses before the production of each noun and verb were recorded and timed. The overall rate of pauses was calculated as the percentage of words preceded by a pause, while the rate of pauses per word class (noun or verb) was calculated in the same way.
Ripamonti et al. (2017), Italy³⁸	Cross-sectional	To analyze alterations in reading, lexical decision, and repetition in people with Alzheimer's disease, primary progressive aphasia, and posterior cortical atrophy. To verify the impact of different psycholinguistic variables (word class, stimulus length, word frequency, imageability, and age of acquisition) on reading performance.	19 people with Alzheimer's disease; 6 with primary progressive aphasia, four of whom had the logopenic variant; 4 with posterior cortical atrophy; and 34 control participants.	Phonological processing. Reading tasks, word and nonword repetition, auditory and visual lexical decision tasks.
Cera et al. (2018), Brazil⁶	Cross-sectional	To identify the distribution of phonetic and phonological manifestations in the speech of healthy older adults and people with Alzheimer's disease and investigate whether these alterations point to the cause of impairments (predominantly phonetic or predominantly phonological).	30 older-adult controls, and 30 people each with mild, moderate, and severe Alzheimer's disease.	Phonological and articulatory processing. Word and sentence repetition task from the verbal and nonverbal apraxia protocol by Martins and Ortiz. Twenty-one phonetic and phonological manifestations were classified as phonetic-phonological: substitution-distortion, omission, addition, starter and attempt at the syllable level; likely phonological: vowel and consonant substitution, starter and attempt at the word level, self-correction, anticipation, phoneme perseveration and transposition; or likely phonetic: distortion, prolongation of vowels and consonants, prolonged intersegment duration, starter and attempt at the sound level, intrusion of schwa in consonant cluster or between syllables.
Beales et al. (2019), Australia³⁹	Case series	To investigate, using the error classification system described by Hohlbaum et al. (2018), the performance of people with different types of dementia (Alzheimer's disease, and semantic and logopenic variant primary progressive aphasia) on a sentence repetition task, and explore its correlation with digit span performance.	4 people with Alzheimer's disease, 4 with semantic primary progressive aphasia, and 4 with logopenic primary progressive aphasia.	Phonological processing. Digit span test and repetition test from the Arizona Battery for Communication Disorders of Dementia. Correct answers and errors, including word omissions, phonological errors, and morphemes altered by phonological errors.
Isella et al. (2020), Italy⁴⁰	Cross-sectional	To identify metabolic correlates of semantic, phonemic, and formal errors observed in people with Alzheimer's disease in a naming task.	63 people with Alzheimer's disease.	Phonological processing. Confrontation naming was assessed through a standardized instrument containing 80 stimuli, or 10 per category (animals, fruits, vegetables, body parts, furniture, tools, vehicles, and musical instruments) Errors were classified as phonemic (neologisms or pseudowords derived from changes in the phonology of the target word), semantic, or formal (real words with phonological, but not semantic, resemblance to the target).
Dong et al. (2020), China⁴¹	Case series	To investigate the linguistic characteristics of Mandarin speakers with Huntington's disease.	5 people with Huntington's disease and 5 with Alzheimer's disease.	Phonological and articulatory processing. Word and sentence comprehension, repetition, naming, category fluency, prosody, written naming, spontaneous writing, reading, copy and dictation.
Tetzloff et al. (2021), USA⁴²	Cross-sectional	To compare the frequency and severity of phonological errors in people with posterior cortical atrophy and logopenic primary progressive aphasia and determine the neuroanatomical correlates of phonological errors and language impairments in posterior cortical atrophy.	27 people with posterior cortical atrophy and 27 with logopenic primary progressive aphasia.	Phonological processing. Boston naming test and the repetition and fluency subtests from the Western Aphasia Battery. The presence and number of phonological errors were recorded, as were scores on the tests. Phonological errors: omission, addition, substitution, or transposition of phonemes.
Cera et al. (2023), Brazil⁴³	Cross-sectional	To determine whether phonetic and phonologic impairments occur in mild, moderate, and severe Alzheimer's disease.	30 people each with mild, moderate, and severe Alzheimer's disease and 30 control participants.	Phonological and articulatory processing. Verbal agility in the Boston test and word repetition task from the verbal and non-verbal apraxia protocol by Martins and Ortiz. Twenty-one phonetic and phonological manifestations were classified as phonetic-phonological (substitution-distortion, omission, addition, starter and attempt at the syllable level); likely phonological (vowel and consonant substitution, starter and attempt at the word level, self-correction, anticipation, phoneme perseveration and transposition); or likely phonetic (distortion, prolongation of vowels and consonants, prolonged intersegment duration, starter and attempt at the sound level, intrusions of schwa in consonant cluster or between syllables).

Table 2.

Results regarding phonological and articulatory processing in Alzheimer's disease or mild cognitive impairment as reported by the studies included in this review.

Determination of the presence or absence of phonological or articulatory changes in Alzheimer's disease or mild cognitive impairment.
No changes in phonological or articulatory processes	In Alzheimer's disease or atypical dementia, 45% of studies that assessed phonological performance identified no impairments in these processing^{7,8,11,20–22,24–27,31,36,41} and 40% of studies that evaluated articulatory performance observed no impairments in these functions.^{11,20–22,24,27,31,36} The analysis of a digit reading and repetition task revealed significant differences between the performance of people with Alzheimer's disease and a control group in the repetition task; however, the author of the study noted that participants displayed normal articulatory rehearsal and articulation rates, which relate to phonological storage and the phonological loop, so that impairments should be attributed to semantic processing.²⁰ Murdoch et al. (1987) found that, although some people with Alzheimer's disease showed impairments in measures of repetition and articulation, their performance did not significantly differ from that of a control group and was indicative of normal phonological and articulatory processing.²¹ In studies of posterior cortical atrophy, atypical dementia, no impairment was identified.³⁶ Regarding mild cognitive impairment, no differences in a sequential speech motion task were found compared to groups with subjective cognitive impairment or Alzheimer's disease.¹¹
Evidence of mild phonological and/or articulatory changes	Studies that identified phonological and/or articulatory alterations in typical AD reported minimal, infrequent, or mild impairments and involved large samples ranging from 19–486 people with the disease.^{5,6,29,30,32,33,38,40,43} Isella et al. (2020) observed few phonemic errors, and only in 25% of participants with Alzheimer's disease.⁴⁰ Comparisons to a control group suggested that phonological manifestations are rare in Alzheimer's disease, as these were only detected with statistical significance in moderate (attempts at the word level and substitutions) and severe (self-correction and anticipation) cases.⁴³ The frequency and type of phonological and articulatory manifestations increased with disease severity, while scores in the verbal agility subtest of the Boston test decreased.⁴³ Regarding articulation, Weiner et al. (2008) investigated clinical impressions during the administration of a mental status examination in a large sample of people with Alzheimer's disease, comprising 486 participants.³⁰ Articulation and repetition impairments were uncommon and could not be used for the initial identification of the disease; however, they were associated with greater disease severity. A low prevalence of articulatory-based errors differentiated groups with and without Alzheimer's disease.³² Some of these manifestations (distortions, prolongation, and prolonged intersegment duration) were observed from the mild stages of the illness and increased with disease progression. Concerning acoustic speech parameters, the percentage of unvoiced segments was a predictor of neuropsychological scores in people with Alzheimer's disease.³³
Evidence of clear phonological and/or articulatory alterations	In studies that identified phonological and/or articulatory impairment in atypical dementia, these alterations were frequent and highly prevalent.^{23,28,34,35,37–39,42} Croot et al. (2000) and Gerstner et al. (2007) described cases of atypical AD characterized by progressive and frequent phonological and articulatory impairments.^23,28 In the study by Chare et al. (2014), most patients with frontotemporal dementia exhibiting phonological or articulation errors presented with Alzheimer's disease pathology and were re-classified into a diagnosis of primary progressive aphasia, with the logopenic variant accounting for the majority of cases.³⁴ The authors suggested that phonological errors may be more sensitive than anomia and reduced span in predicting primary progressive aphasia.³⁴ Leyton et al. (2014) and Tetzloff et al. (2021) identified a high number of phonological errors in most cases of logopenic primary progressive aphasia, ^35,42 and found these errors to be associated with posterior cortical atrophy.⁴² According to Croot et al. (2000), the presence of false starts and phonological paraphasias in automatic and overlearned sequencing tasks points to impairments in phonological and/or articulatory planning in Alzheimer's disease.²³
Speech tasks in the assessment of phonological or articulatory performance in Alzheimer's disease or mild cognitive impairment
Multiple speech tasks	Most of the studies included in this review used multiple assessment methods,^{5,20–23,25,26,28,30,32–36,38,39,41,42} including repetition tasks and, in the majority of cases, a naming-based task. Among the 18 studies that employed multiple speech assessment tasks, seven of the 10 in which phonological or articulatory impairments were observed involved samples with atypical dementia.^{23,28,34,35,38,39,42} Ripamonti et al. (2017) examined the speech of people with typical Alzheimer's disease and atypical dementia, concluding that alterations in auditory lexical decision were more characteristic of Alzheimer's disease and could indicate impairments in lexical-phonological input in the early stages of the illness.³⁸
Discourse task / connected speech.	Four studies administered connected speech-discourse tasks and performed a phonological and/or articulatory analysis of participant speech.^8,24,27,37 In a picture description task, Forbes et al. (2002), Forbes-McKay and Venneri (2005) and Lira et al. (2011) reported no phonological alterations in the speech of people with Alzheimer's disease.^8,24,27 Among all variables assessed in the description of simple and complex pictures, which included phonological and articulatory processing, only semantic processing was sensitive to the impairments associated with the disease, and over 70% of participants with Alzheimer's disease were accurately classified based on the complex version of the task.²⁴ Mack et al. (2015) analyzed pauses prior to the production of nouns and verbs during narrative speech in people with primary progressive aphasia and suggested that word-retrieval processes may differ depending on the type of task used (i.e., narrative versus naming).³⁷
Lexical task (naming or lexical decision).	Among the three studies that used only a naming task to assess people with typical Alzheimer's disease,^7,29,40 two (67%) reported impairments in phonological or articulatory processing.^29,40. Warkentin et al. (2008) observed slower naming in Alzheimer's disease than in a control group, largely due to an increase in mean pause time, with only limited differences in articulation time.²⁹
Repetition task	Among the 18 studies that used multiple speech assessment tasks, as cited previously in this table,^{5,20–23,25,26,28,30,32–36,38,39,41,42} eleven reported phonological or articulatory impairments. Three additional studies used only a repetition task^6,31,43 and alterations in phonological or articulatory processing were observed in all but the oldest of these studies. According to Croot et al. (2000), repetition and reading processes may be more preserved than those involved in naming, since the availability of auditory or orthographic information may help overcome word-finding difficulties.²³ On the other hand, the percentage of phonologically related errors was higher in repetition and reading than in naming tasks since the former provided information on the form of the target word and reduced lexical retrieval difficulties. In a study by Beales et al. (2019), no differences were observed between people with logopenic primary progressive aphasia and Alzheimer's disease in any of the parameters evaluated in a repetition task, except for phonological errors, which were absent in Alzheimer's disease.³⁹
Diadochokinesis and verbal agility	The only study that involved people with mild cognitive impairment did not observe a difference in sequential speech motion rates among people with mild cognitive impairment and Alzheimer's disease as compared to those with subjective cognitive impairment.¹¹ Only 10% of participants with Alzheimer's disease or mild cognitive impairment exhibited altered sequential speech motion rates, producing fewer than 3 syllables per second. Some people with Alzheimer's disease presented with mild apraxia of speech, displaying hesitations, repetitions, vowel distortions, and articulatory groping, none of which were seen in the speech of people with mild cognitive impairment. The authors believe that articulatory agility can be affected in the transition from mild cognitive impairment to Alzheimer's disease, especially in cases with atypical anatomical distribution of disease pathology in the brain, though these impairments are not so severe as to cause noticeable speech impairments in most cases.
Neuroanatomical or biomarker findings related to phonological or articulatory processing
Brain regions	Some neuroanatomical studies associated temporal, parietal and/or frontal regions in the dominant hemisphere to speech alterations in people with Alzheimer's disease^29,40 or atypical dementia,^23,31 as will be discussed below. According to Croot et al. (2000), atypical presentations of dementia characterized by frequent phonological errors are associated with neuropathological changes in temporal, parietal, or frontal perisylvian brain regions.²³ In a study by Warkentin et al. (2008), speech pauses were associated with reduced cerebral blood flow in temporoparietal regions in people with Alzheimer's disease.³¹ Peters et al. (2009) found that people with Alzheimer's disease rely on alternative neural networks for phonological processing due to a progressive loss of specialization of lexicosemantic neural networks, as demonstrated by reduced activity in superior temporal areas and increased activation of the left inferior temporal gyrus during word repetition.³¹ Mack et al. (2015) noted that the rate of pauses prior to different word classes (nouns versus verbs) in primary progressive aphasia was associated with several neuroanatomical findings, including greater atrophy in left frontoparietal regions.³⁷ Isella et al. (2020) reported that some participants with Alzheimer's disease exhibited phonemic errors during a naming task, and observed that these errors were associated with brain hypometabolism in the left supramarginal gyrus.⁴⁰
Biomarkers	In a study by Chare et al. (2014), the percentage of participants with Alzheimer's disease re-classified into frontotemporal primary progressive aphasia syndromes were as follows: 77% for logopenic, 30% nonfluent, and 15% for semantic variant primary progressive aphasia.³⁴ Leyton et al. (2014) reported clinical heterogeneity in a study of the logopenic and nonfluent variants of primary progressive aphasia.³⁵ Nevertheless, the two groups could be distinguished by the Pittsburgh compound B status, symptom manifestations and neuropathological findings. People with a positive Pittsburgh compound B scan were more likely to exhibit logopenic aphasia, phonological errors, and impaired sentence repetition. Additionally, this group of participants exhibited cortical atrophy in temporoparietal regions, the left parietal lobe, and the right superior temporal gyrus.

Results

A total of 157 studies were retrieved in the literature search. Thirty-five of these were selected after Stage 1 and six additional studies cited by these articles were retrieved and included in Stage 2 of the selection process.^{6–8,23,28,32} Twenty-nine of the 41 studies evaluated in Stage 2 met all inclusion criteria and were selected for this review (Table 1). The literature search and study selection processes are shown in Figure 2. The studies excluded in Stage 2^12,44–49 and the reason for their exclusion are listed in Supplemental Material 2.

Figure 2.

Flowchart of the study selection process for this review, following the preferred reporting items for systematic reviews and meta-analyses extension for scoping reviews guidelines.¹⁸

Study characteristics

As can be seen in Table 1, a total of 22 cross-sectional studies^{5–8,11,20–22,24,27,29–35,37,38,40,42,43} and seven case studies were selected.^{23,25,26,28,36,39,41} Sample sizes ranged from 1–10 people for case studies and 18–486 for cross-sectional studies (Table 1). Twenty of the 29 studies involved participants with AD,^{5–8,11,20–22,24,27,29–33,38–41,43} while 14 had participants with atypical dementia.^{11,22,23,25,26,28,34–39,41,42} The only study involving a sample with MCI included 89 participants with this diagnosis in addition to other groups of people with different conditions, including AD.¹¹ Only 13 studies involved a neurologically healthy control group.^{6–8,11,20,21,24,27,29,31,35,38,43}

Articulatory and phonological performance in MCI or ad

All studies included an assessment of at least one phonological aspect and 20 studies provided some articulatory characterization.^{5,6,11,20–24,27–37,43}

Table 2 presents the findings related to phonological and articulatory aspects. Phonological performance was characterized as impaired in 16 (55%) of the studies^{5,6,23,29,30,32–35,37–40,42,43} and normal in 13 studies.^{7,8,11,20–22,24–27,31,36,41} Impairments in articulatory performance were observed in twelve articles (60%),^{5,6,23,28–30,32–35,37,43} while eight studies classified participant performance as normal. ^{11,20–22,24,27,31,36} The only study to include a group of participants with MCI¹¹ did not identify any phonological and/or articulatory impairment in these people.

Ten of the studies that observed phonological and/or articulatory impairments involved people with typical AD,^{5,6,29,30,32,33,38–40,43} while eight involved participants with atypical dementia.^{23,28,34,35,37–39,42}

Studies that identified phonological and/or articulatory impairments in typical AD reported minimal, infrequent, or mild alterations and involved large samples of 19–486 people with the disease (Tables 1 and 2). In contrast, impairments were frequent and common in the eight studies with atypical dementia presentations that showed altered phonological and/or articulatory performance. Primary progressive aphasia, logopenic variant, was the predominant atypical presentation in studies that reported frequent phonological and/or articulatory impairment.^{23,28,34,35,37–39,42}

Phonological and articulatory speech assessment tasks

Table 1 shows that 18 studies employed multiple speech assessment tasks.^{5,20–23,25,26,28,30,32–36,38,39,41,42} Eleven of these (61%) reported phonological and/or articulatory impairments^{5,23,28,30,32–35,38,39,42} and most involved patients with atypical dementia.^{23,28,34,35,38,39,42}

Out of all studies presented in Table 1, three employed repetition-based assessment tasks,^6,31,43 and two (67%) of these studies reported phonological and/or articulatory impairments.^6,43 Among the four studies that assessed connected speech,^8,24,27,37 the only one (25%) that identified impairments involved participants with atypical dementia.³⁷

Of the three studies that administered only a naming task,^7,29,40 two (67%) reported impairments in phonological and/or articulatory performance.^29,40 Phonological and/or articulatory performance was normal in the only study that assessed speech using a sequential speech motion task.¹¹

With the exception of studies exclusively involving patients with atypical dementia, phonological and/or articulatory impairments in AD were identified in studies that administered multiple tasks,^{5,30,32,33,38} repetition-based,^6,43 and naming tasks.^29,40

Neuroanatomical and biomarker findings related to phonological and articulatory performance

In addition to the clinical findings related to phonological and articulatory performance, neuroanatomical studies involving people with AD and primary progressive aphasia have highlighted the involvement of temporal, parietal, and frontal areas of the dominant hemisphere in phonological processing.^{23,29,31,37,40} The studies reported decreased brain activity in the superior temporal lobe,³¹ the left supramarginal gyrus,⁴⁰ along with increased activation of the left inferior temporal gyrus.³¹

Furthermore, a positive Pittsburgh Compound-B scan was associated with phonological errors in atypical dementia with the logopenic variant of primary progressive aphasia.³⁵ A high percentage of people with logopenic primary progressive aphasia (77%) presented with AD pathology.³⁴

Discussion

This study aimed to identify, through a scoping review, the phonological and articulatory performance of people with MCI and AD, in addition to analyzing the speech tasks with greater sensitivity for the presence of phonological or articulatory impairments. The results suggest that the identification of phonological or articulatory performance deficits due to AD may be linked to the speech assessment task, sample size, and the presence of atypical dementia. Studies that reported alterations in phonological or articulatory processing, which were usually infrequent, involved large samples of people with typical AD. More common and frequent phonological and/or articulatory impairments were observed in studies of people with atypical dementia, especially logopenic primary progressive aphasia. A single repetition or naming task was the most sensitive method for identifying the presence of impairments in phonological and articulatory planning in AD. These findings will be presented and discussed below.

All studies that identified phonological and/or articulatory alterations in typical AD involved large samples and reported mild or infrequent impairments.^{5,6,29,30,32,33,38,40,43} Interestingly, since 2011, all cross-sectional studies with large samples of people with typical AD identified phonological and/or articulatory alterations. It appears that the assessment and identification of phonological and/or articulatory alterations in AD, that is, the differentiation of clinical manifestations related to the different stages of speech and language processing, became clearer after 2011. In 2009, a contemporary four-stage model of sensorimotor speech processing influenced by previous speech production models was published.¹⁶ In the same year, the characteristics of the differential diagnosis between phonemic paraphasias, aphasias, and manifestations of apraxia of speech were presented.¹⁷ This scientific evidence from 2009 was an important addition to existing knowledge of speech and language processing and phonological and articulatory manifestations. This factor is likely to have contributed to a better identification of phonological and articulatory manifestations in different speech samples. This certainly contributed to the increased identification of the presence of these manifestations in the speech of people with AD, despite the low occurrence of impairments. Furthermore, it is likely that greater scientific knowledge related to the most markedly altered aspects has contributed to the increase in studies on the less altered aspects in recent years.

Even the oldest studies included in this review reported a low occurrence of phonological and/or articulatory impairments in AD; however, in these studies, phonological and/or articulatory performance was classified as normal.^20,21 The differences between the performance of AD and control groups were mainly related to semantic aspects of processing.^20,21 Similarly, in 2009, the only study in this review to involve patients with MCI showed that only 10% of people with AD or MCI showed poor performance in a sequential speech motion task, suggesting that this measure alone was not sufficient to distinguish between participant groups.¹¹ Thus, the authors reported that articulatory agility is affected in the transition between MCI and AD but not to the point of causing perceptible changes in the speech of most patients.¹¹ As knowledge in this area evolves, new studies may be able to identify phonological and articulatory characteristics associated with MCI and considered outside normal standards. In short, this review observed that phonological and articulatory alterations occur with a low infrequency in typical AD, especially in studies with large samples. However, since 2011, these manifestations have become more easily detectable.

Studies that described more perceptible, common, and frequent phonological or articulatory alterations focused mostly on atypical presentations of dementia.^{23,28,34,35,37–39,42} Phonological errors comprise part of the diagnostic criteria for the logopenic variant of primary progressive aphasia, which explains the reported frequency of this alteration in this atypical dementia. Therefore, the findings of this review suggest that the perception and identification of phonological and articulatory speech changes in AD and MCI were influenced by sample size, by scientific developments on the topic, and the neuropathological and clinical characteristics of the underlying cause of dementia in the studied samples. Additionally, it is interesting to note that some people diagnosed with MCI or AD in adulthood may present with phonological and/or articulatory processing disorder during neurodevelopment. At the onset of cognitive symptoms in adulthood, the phonological and/or articulatory development disorder may make them more susceptible to alterations.

In addition to the presence of phonological or articulatory alterations, it is interesting to observe the type of speech assessment task used in the studies. The majority of studies employed multiple speech assessment tasks (including naming, repetition, reading-based and other tasks).^{5,23,28,30,32–35,38,39,42} These studies administered repetition tasks as part of a larger test battery, but the sensitivity of these tasks in detecting phonological and/or articulatory alterations was smaller (56%) than that observed in studies that used a repetition task on its own (67%).^6,43 Repetition tasks seemed to facilitate lexical access by providing participants with the form of the target word, resulting in a higher percentage of phonologically related errors.²³ Therefore, repetition tasks appeared to minimize the interference of other processing stages in the individual's response and were more sensitive to the identification of phonological and articulatory alterations in AD compared to connected speech tasks and larger test batteries. Among studies involving naming tasks, a similar level of sensitivity (67%) was observed in the identification of phonological and/or articulatory impairments. Thus, despite the limited number of studies with only a repetition or naming task, the findings of this review suggest that a single task, either repetition- or naming-based, is more sensitive to phonological or articulatory speech deficits.

Speech assessments that are sensitive to identifying phonological or articulatory speech errors in typical AD have analyzed various parameters: the number of manifestations or phonological and/or articulatory errors;^{5,6,32,38,40,43} acoustic analysis findings, particularly unvoiced speech segments;³³ and duration of naming pauses.²⁹ In naming tasks, which involve several stages of language and speech processing, the analysis of silence and articulation periods revealed differences between people with AD and control participants. Findings such as those of Warkentin et al. highlight the importance of tasks that analyze parameters related to speech rate and prosody.²⁹

Sequential speech motion tasks evaluate articulatory agility, which is related to speech rate. The only study investigating the phonological and articulatory performance of people with MCI did not observe a statistically significant difference between groups with MCI and AD on a sequential speech motion task.¹¹ Yet some participants with AD appeared to display characteristics of apraxia of speech, such as hesitations, repetitions, distortions, or articulatory groping, none of which was observed in participants with MCI.¹¹ On the other hand, the performance of people with subjective cognitive decline, a condition that occurs in the absence of cognitive test abnormalities,⁵⁰ differed from that of the AD group, but not the MCI group.¹¹ Therefore, it appears that the progression of overall cognitive impairment may be accompanied by changes in speech performance, even if these changes are difficult to identify. Furthermore, it appears to be easier to differentiate between groups with more distinct cognitive profiles, such as subjective cognitive decline and AD, and articulatory agility tasks may be particularly sensitive in this regard.

Lastly, the results of this review show that, among studies that involved the phonological assessment of people with AD and other atypical dementias, 52% identified impairments, while studies that performed articulatory assessments observed impairments in 60% of cases. The higher percentage of studies that identified articulatory impairment corroborates the findings of a study that identified articulatory manifestations from the mild stage of AD, while errors caused specifically by phonological factors were more easily identified in the moderate and severe stages of the disease.⁴³ These observations suggest that articulatory alterations more clearly differentiate speech performance in AD, especially in the early stages of dementia. Additionally, the percentage of unvoiced speech segments was a predictor of neuropsychological scores in people with AD.³³

Thus, according to studies that used a variety of assessment tasks, especially single repetition or naming tasks, there is evidence of phonological and articulatory impairment in the speech of people with AD.

On a similar note, some neuroanatomical alterations observed in AD have been associated with changes in phonological processing performance, such as decreased brain activity in the superior temporal lobe³¹ and the left supramarginal gyrus⁴⁰ and increased activation of the left inferior temporal gyrus.³¹ These findings demonstrate the importance of assessing phonological and articulatory aspects of speech as part of the longitudinal monitoring of cases with diagnosed or suspected MCI, typical AD or atypical dementia, allowing for the early identification of such alterations.

Our results should be interpreted with caution due to the lack of studies involving samples with MCI and the fact that most of the studies reviewed employed multiple speech assessment tasks.

Conclusion

This review found no evidence of changes in phonological or articulatory speech processing in MCI compared to people with AD or subjective cognitive decline.

People with AD may exhibit alterations in phonological or articulatory performance, albeit the prevalence of such manifestations is lower in typical AD than in atypical dementia presentations. In AD, single repetition or naming tasks appear to be more sensitive for identifying phonological or articulatory-based speech impairments as compared to multiple tasks or connected speech tasks.

Supplemental Material

sj-docx-1-alr-10.1177_25424823241290698 - Supplemental material for Articulatory and phonological performance in people with mild cognitive impairment and Alzheimer's disease: A scoping review

Supplemental material, sj-docx-1-alr-10.1177_25424823241290698 for Articulatory and phonological performance in people with mild cognitive impairment and Alzheimer's disease: A scoping review by Maysa Cera, Paulo Henrique Ferreira Bertolucci, Nathani Cristine do Carmo Ramos, Camila de Castro Corrêa, Carla dos Reis Piffer Vilela and Karin Zazo Ortiz in Journal of Alzheimer's Disease Reports

Footnotes

Acknowledgements

The authors have no acknowledgments to report.

ORCID iDs

Maysa Cera

Paulo Henrique Ferreira Bertolucci

Nathani Cristine do Carmo Ramos

Camila de Castro Corrêa

Carla dos Reis Piffer Vilela

Karin Zazo Ortiz

Author contributions/CRediT

Maysa Cera (Conceptualization; Formal analysis; Investigation; Project administration; Writing – original draft); Paulo Henrique Ferreira Bertolucci (Project administration; Supervision; Writing – review & editing); Nathani Cristine do Carmo Ramos (Data curation; Formal analysis; Investigation; Project administration; Writing – review & editing); Camila de Castro Corrêa (Conceptualization; Data curation; Project administration; Writing – review & editing); Carla dos Reis Piffer Vilela (Writing – review & editing); Karin Zazo Ortiz (Project administration; Supervision; Writing – review & editing).

Funding

The authors received no financial support for the research, authorship, and/or publication of this article.

Declaration of conflicting interests

The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Supplemental material

Supplemental material for this article is available online.

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