Roles of Cognitive Status and Intelligibility in Everyday Communication in People with Parkinson’s Disease: A Systematic Review

Abstract

Background: Communication is fundamental to human interaction and the development and maintenance of human relationships and is frequently affected in Parkinson’s disease (PD). However, research and clinical practice have both tended to focus on impairment rather than participation aspects of communicative deficit in PD. In contrast, people with PD have reported that it is these participation aspects of communication that are of greatest concern to them rather than physical speech impairment.

Objective: To systematically review the existing body of evidence regarding the association between cognitive status and/or intelligibility and everyday communication in PD.

Methods: Five online databases were systematically searched in May 2015 (Medline Ovid, EMBASE, AMED, PsycINFO and CINAHL) and supplementary searches were also conducted. Two reviewers independently evaluated retrieved records for inclusion and then performed data extraction and quality assessment using standardised forms. Articles were eligible for inclusion if they were English-language original peer-reviewed research articles, book chapters or doctoral theses investigating the associations between at least one of cognitive status and level of intelligibility impairment and an everyday communication outcome in human participants with PD.

Results: 4816 unique records were identified through database searches with 16 additional records identified through supplementary searches. 41 articles were suitable for full-text screening and 15 articles (12 studies) met the eligibility criteria. 10 studies assessed the role of cognitive status and 9 found that participants with greater cognitive impairment had greater everyday communication difficulties. 4 studies assessed the role of intelligibility and all found that participants with greater intelligibility impairment had greater everyday communication difficulties, although effects were often weak and not consistent.

Conclusions: Both cognitive status and intelligibility may be associated with everyday communicative outcomes in PD. The contribution of intelligibility to everyday communication appears to be of small magnitude, suggesting that other factors beyond predominantly motor-driven impairment-level changes in intelligibility may play an important role in everyday communication difficulties in PD.

Keywords

Parkinson disease cognition disorders speech disorders communication social participation international classification of functioning disability and health review systematic

INTRODUCTION

Parkinson’s disease (PD) is a common neurodegenerative condition that affects around 1.5% of people over 65 in Europe [1] with considerable worldwide variation in prevalence [2]. In light of the impact of PD on quality of life [3] and the global ageing population [4], PD should be considered a major healthcare challenge of the future. PD was originally characterised largely in terms of its motor features [5], which still form the basis of recognised diagnostic criteria [6 –8]. However, research has revealed a wide range of non-motor symptoms [9] including cognitive impairment [10] in over a quarter of patients.

Communication is fundamental to human interaction [11] and the development and maintenance of human relationships, including those developed in a healthcare context. Around 70% of people with PD report dissatisfaction with their everyday communication [12]. The International Classification of Functioning (ICF) [13] provides a useful framework for conceptualising the distinction between ‘speech’ difficulties at the impairment level and ‘communication’ difficulties at the activity and especially the participation level. Indeed, the extent of communicative difficulty at the ICF participation level may not be closely associated with severity of speech impairment at the ICF impairment level, such as intelligibility [12, 14]. Other factors beyond speech impairment, such as cognitive status [15], may play an important role in determining participation level outcomes, which we call ‘communicative participation’ following Eadie et al. [16].

In recent years, there has been increased focus on the benefits of service user involvement in the development and prioritisation of research in order to avoid mismatch of priorities [17, 18]. Miller et al. [19] conducted in-depth qualitative interviews with people with PD in order to identify the nature of speech and communication changes, using these terms in the technical senses defined above, and to assess what impact these changes had on their lives. In this study, “central concerns were not that voice was monopitch, sound contrasts difficult, or similar … Rather individuals focused on the impact changes exerted on ability to communicate [and] their view of themselves”. In contrast, the body of published literature for impairment-level speech changes in PD is much greater than that about communication and there is evidence that the ICF participation level does not form a major focus of many speech and language therapists’ assessment and intervention practices for PD [20]. Therefore, there appears to be a mismatch between the priorities of people with PD and those of researchers and clinicians.

In light of this potential mismatch of priorities, it is important to conduct a systematic and comprehensive appraisal of evidence regarding the associations between i) speech and communication difficulties in PD and ii) cognitive status and communication difficulties in PD. This enables evaluation of how closely related the concepts are that form the respective priorities of people with PD and of researchers and clinicians. As no summary appraisal of available evidence was identified by a search of the literature, we decided to conduct a systematic review to address these research questions and report the findings in this article.

MATERIALS AND METHODS

We undertook a systematic review of studies investigating the associations between cognitive status and/or intelligibility and everyday communication in PD. PRISMA guidelines [21] were followed. Due to the heterogeneity of study designs and measures, a narrative systematic review rather than a quantitative meta-analysis was conducted. This study was a systematic review of existing literature and no human or animal participants were recruited. Therefore, no ethical approval was required.

Explicitly stated, our research questions were:

To assess associations between cognitive status and communication outcomes in PD

How many studies have assessed the relationship between cognitive status and communication outcomes in PD, taking the definition of communication outlined earlier?

Of the included studies, what proportion identified a statistically significant association between at least one measure of cognitive status and a communication outcome measure in PD?

Taking into account all relevant data presented in the included studies, is the evidence in favour, inconclusive or against with regard to the existence of an association between cognitive status and communication in PD and what does it say about the strength of this association?

Do the cognitive measures used in the included studies provide insight into which aspects of cognitive status might be most predictive of degree of communicative difficulty in PD?

To assess associations between intelligibility and communication outcome in PD:

How many studies have assessed the relationship between intelligibility and communication outcomes in PD, taking the definition of communication outlined earlier?

Of the included studies, what proportion identified a statistically significant association between at least one measure of intelligibility and a communication outcome measure in PD?

Taking into account all relevant data presented in the included studies, is the evidence in favour, inconclusive or against with regard to the existence of an association between intelligibility and communication in PD and what does it say about the strength of this association?

Search methods

Five online databases were systematically searched in May 2015: Medline Ovid (1948), EMBASE (1980), AMED (1985), PsycINFO (1806) and CINAHL (1982). The search strategy was designed by MSB and KHOD and formed 3 blocks: ‘Parkinson’s disease’, ‘cognitive status or intelligibility’ and ‘everyday communication’. Key terms were mapped to database-specific subject headings (MeSH) where available and exploded to include sub-categories. Items within the blocks were linked with an ‘OR’ Boolean operator and blocks were linked with ‘AND’. The full Medline search strategy is provided in the supplementary data accompanying this article. Supplementary searches were conducted by screening bibliographies of extracted articles and an online search engine (Google Scholar).

Eligibility criteria

For inclusion in the review, articles had to meet the following eligibility criteria:

Full-text original peer-reviewed research article, book chapter or doctoral thesis

English language publication

Empirical investigation

Human participants with PD, results being presented separately from other conditions

Explicit assessment of cognitive status or level of intelligibility impairment

Linkage thereof to oral everyday communication outcomes including communication-focused pragmatics

Results separable from any investigation of therapy, medicine or surgery

Titles and abstracts were independently assessed for potential inclusion by two reviewers (MSB and DW) and any disagreements resolved by discussion. Full texts were obtained where abstracts met eligibility criteria and were independently assessed by MSB and DW. Those meeting the eligibility criteria were included in the narrative synthesis.

Data extraction

Data were extracted independently for each included study by MSB and DW. Data were entered onto standardised forms capturing studycharacteristics and study measures and results respectively (see supplementary data accompanying this article), subsequently synthesised into a summary of findings table (Table 1). Where appropriate, articles were grouped into studies.

Quality assessment

Quality assessment was conducted using the Threats to Validity tool [22], which KHOD previously helped to develop. It was configured for the purposes of our review by MSB and KHOD. Quality was assessed independently by MSB and DW for each included study, enabling generation of a ‘Threats to Validity Table’ (Table 2) profiling the methodological performance of each study. Following Daley et al. [22], studies were assessed as at overall low risk of bias (High quality) if ≥70% of applicable quality items were assessed as at low risk of bias, overall moderate risk of bias (Moderate quality) for 40–69% and overall high risk of bias (Low quality) for ≤39%.

RESULTS

Database searches yielded 4816 unique records. Sixteen additional records were identified through supplementary searches. Figure 1 shows the PRISMA flow chart depicting each stage of study identification. After reviewing abstracts, 41 were suitable for full text retrieval. Following thorough evaluation, 15 articles [12 , 23–34] (12 studies) met the eligibility criteria.

Summary of studies

Eight studies assessed only cognitive status as a predictor of communicative difficulties, two studies only assessed intelligibility as a predictor and two studies assessed both cognitive status and intelligibility as predictors. Ten studies used a cross-sectional design, one used a cohort study design and one used a mixed methods design. Five studies were conducted in the USA, four in the UK, two in Canada and one in New Zealand. Two studies were assessed at low risk of bias, five at moderate risk of bias and five at high risk of bias (Table 2). The three most common threats to validity were a lack of participant representativeness (11 studies, 92%), concerns over task or stimulus order effects (11 studies, 92%) and a lack of sample size rationale (10 studies, 84%). The approach to intelligibility assessment undertaken by each study is profiled in Table 3. The findings of included studies are summarised below and provided in full in the Appendix.

Cognitive status

Ten studies assessed the role of cognitive status and 9 found a positive result, defined as a significant association between at least one measure of cognitive status and one measure of everyday communication. Of these nine studies, one [25] was assessed at low risk of bias, four [15 , 34] at moderate risk of bias and four [23 , 32] at high risk of bias. Five [28 , 34] of these studies provided evidence that greater impairment of cognitive status is associated with greater impairment of conversational pragmatics. Hall et al. [28] found that Mini Mental State Examination (MMSE) [35] score was strongly associated with score on the Rating Scale of Pragmatic Communication Skills [36]. McKinlay et al. [30] found that measures of working memory and processing speed, but not attentional set-shifting, predicted pragmatic communication on the Test of Linguistic Competence-Extended [37]. McNamara et al. [31] found that Stroop [38] and Tower of London [39] test parameters were associated with score on the Pragmatic Protocol [40]. Monetta et al. [33] found that verbal working memory and verbal fluency predicted aspects of the Discourse Comprehension Test [41]. Pell et al. [34] found that the ability to make enriched social inferences on The Awareness of Social Interference Test [42] was associated with working memory capacity and frontal lobe functioning.

Three studies [15 , 29] found an association between cognitive status and narrative organisation and/or turn taking. Alpert et al. [23] found that a composite dementia score was negatively associated with frequency of internal pauses and frequency of simultaneous speech and positively associated with mean length of internal pauses. Ash et al. [24] found that reverse digit span, letter-guided fluency, category fluency and Stroop time were associated with communicative parameters from the analysis of story narration. Lesser et al. [15, 29] found that while PD subcortical dementia and PD with Lewy body dementia groups did not differ overall with regard to conversation analysis parameters, people with PD and Lewy body dementia had more difficulty orienting the conversation partner to a new topic and retained fewer pre-morbid communicative situations.

One study [25] found that worse Montreal Cognitive Assessment (MoCA) [43] score was associated with greater impairment of everyday communication as measured the Communicative Participation Item Bank (CPIB) [44] but not the Communicative Effectiveness Survey (CES) [14]. Sub-domain analysis was reported. MoCA ‘Naming’ sub-scale was identified as a predictor of CES score, while MoCA ‘Executive and Visuospatial’ and ‘Attention’ subscales were marginal predictors of CPIB.

One study [12, 32] had a negative result. It was assessed as high quality and investigated the association between cognitive status and communicative effectiveness as measured through a semantic differential questionnaire.

Intelligibility

Four studies assessed the role of intelligibility and all found a statistically significant association between at least one measure of intelligibility and one communicative outcome, representing a positive result by our definition. Two [12 , 32] were assessed at low risk of bias, one [14, 27] at moderate risk of bias and one [26] at high risk of bias. Barnish [25] found that conversational sentence intelligibility was a significant predictor of both CPIB and CES, accounting for 43% and 19% of the variance respectively, while read sentence intelligibility did not significantly predict these communication outcomes. Coates and Bakheit [26] found that there was a significant difference in intelligibility scores between those who complained of everyday communication difficulties and those who did not. Donovan et al. [14, 27] found a significant association between intelligibility and CES, although it accounted for only 15% of variance. Miller et al. [12, 32] found that intelligibility was a weak (r = –0.23) but statistically significant predictor of communicative change according to a semantic differential questionnaire at baseline but not at follow-up.

DISCUSSION

The systematic review reported in this article is the first to address the contribution of either cognitive status or intelligibility to everyday communication difficulties in PD. Of the ten studies that assessed the role of cognitive status, nine found evidence of this association and the other study [12, 32] relied on MMSE, which has been demonstrated to be insensitive to milder cognitive impairment in PD [45, 46]. The balance of evidence is in favour of an association between cognitive status and everyday communication in PD including communicative participation, conversational pragmatics and narrative organisation/turn-taking. With regard to the implication of specific cognitive functions, there is preliminary evidence that executive function might be implicated, although before any conclusions can be drawn this requires further exploration in future studies, which may also seek to assess neural correlates using imaging techniques. Of the four studies that assessed the role of intelligibility, all found evidence of a significant association. However, the strength of association differed regarding on the nature of the intelligibility assessment and the communicative outcome measure. Overall, the contribution of intelligibility deficits to everyday communication difficulties appeared of modest magnitude.

The first key conclusion of this systematic review is that we found evidence to suggest that both cognitive status and intelligibility may be associated with everyday communicative outcomes in PD. The second key conclusion is that the contribution of intelligibility to everyday communication, while statistically significant, appears to explain a relatively small proportion of the variance in everyday communication outcomes. This, in turn, suggests that other factors beyond predominantly motor-driven impairment-level changes in intelligibility may play an important role in everyday communication difficulties in PD.

These conclusions must, however, be viewed as preliminary since there are several key limitations in the identified body of literature. Firstly, most included studies were cross-sectional, which preclude definitive inference of causality [47] since they provide no information on the time sequence of the hypothesised exposure and outcome. Secondly, only two of the 12 studies (17%) were assessed at low risk of bias and five (42%) were assessed at high risk of bias, suggesting that study quality in this field of inquiry may be problematic. Thirdly, only 2 studies (17%) reported a sample size rationale and the median number of people with PD included per study was only 18.5, showing that most studies used small samples. Therefore, many included studies may have limited statistical power and be limited in their generalisability beyond the sample.

Everyday communication is fundamental to successful functioning [11], and difficulties in this area are both common [12] and seen as a priority by people with PD [19]. However, established paradigms in the conceptualisation and treatment of communicative difficulties in PD have focused predominantly on impairment-level motoric alterations in speech. For example, evidence from surveys of UK speech and language therapists has shown that everyday communication, especially at the participation level, does not form a major focus of many therapists’ assessment and intervention practices for PD [20] and progressive dysarthria more generally [48]. This is despite clinical guidelines [49] and a belief by both clinicians [48] and people with PD [19] that communicative participation is important.

Indeed, the number of studies eligible for inclusion in our systematic review is relatively small. The vast majority of studies assessing speech in PD have not looked at changes beyond the ICF impairment level. The reasons for this focus are unknown, although they may parallel a similar situation in clinical practice [20, 48]. One possible explanation is the lack until relatively recently of any self-report measure that solely measured communicative participation [16]. CPIB offers the prospect of addressing this shortage. CPIB was developed using item-response theory [50] and subsequently validated in PD in the USA and New Zealand [51] as well as the UK [25]. In light of its relatively recent development, CPIB was only used in one study [25] included in this review. Studies varied considerably in terms of the outcome measures used and many measures did not adequately distinguish ICF Activity and Participation level effects. Moreover, the studies by Hall et al. [28], McKinlay et al. [30], McNamara et al. [31], Monetta et al. [33] and Pell et al. [34] used outcome measures that focused on specific aspects of pragmatic communicative functioning, which may not be generalizable to other aspects of everyday communication. Issues of measurement need to be addressed in future studies.

Issues regarding how intelligibility was assessed in included studies also need to be considered. As profiled in Table 3, the four studies that assessed intelligibility shared some commonalities but also had some considerable differences with regard tointelligibility assessment. All four studies conducted all or most of the recordings in participants’ own homes. This is likely to offer a more realistic real-world recording environment than a studio recording, but would lack the extent of background noise encountered in certain common everyday communicative situations such as cafes and community centres. Two studies [14 , 27] did not address stimulus organisation, while Barnish [25] used a blended presentation approach using Latin Square [52] allocation of stimuli to assessors and a randomised presentation order to minimise stimulus exposure effects and learning biases [53, 54] and Miller et al. [12, 32] randomly assigned whole recordings of speakers to assessors. Two studies [14 , 27] presented stimuli in context, one study without context [12, 32] and one study [26] did both. One study [25] used a large pool of assessors without expertise in speech disorders, one study [12, 32] used a small number of assessors without expertise in speech disorders and two studies [14 , 27] used a small number of expert listeners. All four studies used transcription tasks. Intelligibility assessments may lack comparability across studies and task-specific effects may limit generalisability. It is possible to suggest that intelligibility assessment tasks may overestimate the deficit when transferred to everyday communicative situations, which in turn could in part explain the weak association between intelligibility and everyday communication outcomes. However, this is not supported by the finding of Barnish [25] that conversational speech intelligibility predicted communicative outcomes, while read speech intelligibility did not.

If confirmed in further, more rigorous studies, the findings presented in our systematic review that intelligibility does not appear particularly strongly associated with the degree of everyday communication difficulties in PD, and that other factors such as cognitive status may play an important role, would present a challenge to prevailing assessment and treatment practices. Further research is required to confirm these findings. It is recommended that future studies i) are designed in accordance with rigorous quality assessment tools, ii) have sufficient sample size to address issues of statistical power and generalisability and iii) use prospective cohort designs to offer greater insight into temporal relations. Moreover, the investigation of communicative outcomes could be embedded into large cohort studies of the general natural history of PD to provide access to larger, more representative samples. In addition, if research in this field could agree upon a standard set of cognitive, intelligibility and communicative measures, this could facilitate meta-analysis.

This systematic review has a number of key strengths. Firstly, it is the first systematic evaluation of the extant body of evidence relating intelligibility and cognitive status to everyday communication in PD. Secondly, searches covered five key bibliographic databases with supplementary searches to minimise risk of selection bias. Thirdly, rigorous standardised screening and data extraction techniques were used. Fourthly, quality assessment was conducted with a tool that was specifically designed for use in assessing observational studies. Fifthly, review procedures were conducted independently by two reviewers as a quality assurance measure. There are, however, a couple of limitations that should be considered. Firstly, only articles published in English were considered. However, English is the primary international language of scientific communication and there is evidence that potential language bias does not significantly affect the result of systematic reviews [55]. Secondly, the heterogeneity of study methods, including both exposure and outcome measurement, precluded the use of meta-analysis, which could have provided a pooled estimate ofeffect size.

ACKNOWLEDGEMENTS INCLUDING SOURCES OF SUPPORT

We acknowledge funding from a University of East Anglia (UEA) PhD studentship to MSB, during whose PhD at UEA the idea for this systematic review was conceived and an early version conducted. The idea for this systematic review was conceived by MSB (Chief Investigator), KHOD, SMCH and ZRB. Project management was conducted by MSB. Searches were designed by MSB and KHOD and then executed by MSB. Screening, data extraction and quality assessment were conducted by MSB and DW with advice from KHOD. All authors contributed to the interpretation of the findings. MSB wrote the first draft of the manuscript and all authors contributed to revisions and approved the submission.

CONFLICTS OF INTEREST

The authors have no conflict of interest to report.

Footnotes

Appendix

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