European Journal of Neurology 2012, 19: 666–671 doi:10.1111/j.1468-1331.2011.03635.x CME ARTICLE How subjective are subjective language complaints I. P. Martinsa, I. Maresa and P. A. Stilwellb a Department of Clinical Neurosciences (UNIC), Instituto de Medicina Molecular, Lisbon Faculty of Medicine (IMM), Portugal; and b Faculty of Medicine, University of Bristol, UK See editorial by Cappa, on page 665. Keywords: ageing, cognitive complaints, subjective cognitive symptoms, language complaints Received 23 September 2011 Accepted 8 November 2011 Background and purpose: Subjective language complaints (SLC) are common during ageing but have not been investigated in detail. We aim to determine their association with demographic and clinical variables and objective cognitive performance. Methods: A sample of 479 individuals aged 50 years or above (average 66 ± 9.1 years), followed in primary care, with no history of brain disorder were asked two questions concerning SLC, fulfilled a depression scale and undertook a battery of cognitive tests. Response to questions regarding proper name retrieval (PNR) and word finding difficulties (WFD) was studied and their contribution to each measure of the battery calculated by repeated linear regression analysis, adjusting for age, sex, education, living alone and depressive symptoms. Results: Word finding difficulties (47.6%) were more frequently reported than problematic PNR (10.9%). Both were more common in women, in subjects with depressive symptoms and in those living alone, but were unrelated with age or education. Both symptoms contributed significantly to the variance in tests of semantic fluency and episodic memory. PNR was also associated with immediate phonological memory. Conclusions: Subjective language complaints are especially common amongst individuals living alone and/or with depressive symptoms. They are associated with a worse cognitive performance in some memory and language-executive tests. Further studies are needed to understand their predictive value for cognitive decline. Introduction Language is essential for the adequate communication of thoughts, intentions, wishes and the success of social interaction. Failures in language expression usually cause embarrassment and may hamper interpersonal relationships. Although language is relatively resistant to ageing [1], there is evidence that word retrieval ability declines with age [2] despite the fact that elderly subjects are able to maintain or improve their vocabulary and knowledge of word meaning [2]. Such language complaints are often experienced as a tip of the tongue (TOT) phenomenon, Correspondence: I. P. Martins, Language Research Laboratory, Department of Neurosciences, Lisbon Faculty of Medicine, Instituto de Medicina Molecular, Hospital de Sta Maria 1600 Lisboa, Portugal (Telefax: 351 217 934 480; e-mail: [email protected]). This is a Continuing Medical Education article, and can be found with corresponding questions on the Internet at http://www.efns.org/EFNS Continuing-Medical-Education-online.301.0.html. Certificates for correctly answering the questions will be issued by the EFNS. 666 a state during which one is temporarily unable to produce a word despite knowing it and being able to partially access its visual form [3]. TOTs become more frequent as one ages [4] and seem to be particularly common for proper names [5] because these are pure referential and arbitrary expressions, without inherent semantic value [6]. In some people, difficulties with language production may become a source of concern and a reason to seek medical advice. Yet, the relation between subjective language complaints (SLC) and objective cognitive performance is not clear. Therefore, it is difficult for physicians to reassure patients who present with those complaints that their symptoms do not reflect objective cognitive impairment, given the hypothesis that they could signal the onset of a degenerative disease, such as AlzheimerÕs disease. In contrast with that lack of knowledge, there is a large amount of research about subjective memory complaints. This discrepancy may arise from the early involvement of episodic memory in the most common degenerative brain diseases and also the incorporation 2012 The Author(s) European Journal of Neurology 2012 EFNS How subjective are subjective language complaints of memory complaints in the diagnostic criteria for mild cognitive impairment (MCI) [7–9]. Cross-sectional studies examining whether peopleÕs memory complaints correlate with current cognitive performance have produced mixed results. Nonetheless, a systematic review of such studies [10] and a recent meta-analysis [11] have shown an association between memory complaints and memory impairment, as well as a high specificity, for both MCI and dementia. Longitudinal studies have also examined the association between current complaints and future cognitive decline. They have indicated that memory complaints, even in the absence of objective impairment on neuropsychological examination, can be an early marker of future cognitive deterioration [12,13] and possible progression to dementia [14]. Altogether, these data suggest that subjective memory complaints in otherwise normal older adults could be realistic self-observations of the initial stages of cognitive decline. Other cognitive complaints have received much less attention despite the evidence that ageing is also associated with a decline in executive skills and language [1]. Indeed, most studies evaluating cognitive complaints have analysed total scores on subjective failures questionnaires, rather than focusing on individual complaints [13,15,16]. Notable exceptions that looked at SLC are the study by Fischer et al. [17], who showed that depressive symptoms in old age are strongly associated with increased language complaints, and Dave [18], who suggested that complaints about language, as opposed to memory or attention, predict future language decline. The purpose of this study is as follows: (i) to estimate the frequency of SLC in a sample of adults observed in primary care and its relation with socio-demographic and clinical variables and (ii) to determine whether there is an association between SLC and objective performance in neuropsychological tests. Method Study design and setting This study is part of a larger prospective longitudinal project [19] aimed to evaluate the cognitive profiles in ageing in a cohort of adults, followed in public primary care centres, without known brain disease. A detailed description of the project, population and method, including the cognitive battery used, has been reported elsewhere [19]. General practitioners (GPs) screened 544 volunteers, aged 50 or above, who were not suspected of dementia and were independent in daily living activities. Participants were further screened by the Mini-Mental State Examination (MMSE) [20] and were included if they 667 had a score above education-adjusted cut-off points (i.e. 22 for individuals with <12 years of education and 27 for those with 12 or more years of education) [21]. The study protocol was approved by the Ethics Committee of Lisbon Faculty of Medicine, by the Institutional Board of participating Regional Health Centres and by the National Committee for Data Protection. Informed consent was obtained for all participants. Procedures Clinical data were provided by the participantsÕ GP, namely the presence of vascular risk factors (i.e. hypertension, diabetes and hypercholesterolaemia). All participants were evaluated individually by a licensed psychologist. Socio-demographic information was collected, including age, sex, number of years of education and household company. This was followed by a cognitive evaluation and questionnaires for depression and cognitive complaints. Evaluation took place in a private office in the health centres. Subjective language complaints were assessed by two questions of the Subjective Memory Complaints Scale [22]. One of them was directed to difficulties in Ôproper name retrievalÕ (PNR), ÔDo you ever forget names of family members or friends?Õ, whereas the second referred to Ôword finding difficultiesÕ (WFD), ÔDo you ever have difficulties in finding particular words?Õ. The former had four possible answers (0 – No; 1 – Yes, but no problem; 2 – Yes, problem; 3 – Yes, serious problem), whilst the latter had two (0 – No; 1 – Yes). To make answers comparable and avoid scaling bias, PNR responses were dichotomised into absence (score 0 or 1) or presence (score 2 or 3) of problematic complaints. This division was suggested by Schmand et al. [22] and was adopted, given that these symptoms were not spontaneously reported and we were trying to differentiate clinically relevant complaints from minor ones. Depressive symptoms were evaluated by the 15-item version of the GDS [23]. Subjects were divided as with (GDS > 5) or without (GDS < 6) significant depressive symptoms according to a recognised cut-off point [24]. Participants were also classified as living alone or with household company. The original cognitive battery included 28 tests or measures directed to different cognitive domains [19]. For this study, we selected the 15 most frequently used measures to assess language, episodic memory and executive functions. Language testing included vocabulary [25], verbal fluency (animal and food categories and p-phonemic fluency) [26], naming famous faces [27] and digit span forward) [26]. Episodic memory was 2012 The Author(s) European Journal of Neurology 2012 EFNS European Journal of Neurology 668 I. P. Martins, I. Mares and P. A. Stilwell evaluated by the learning trials and long delay free recall of the nine-item version of California Verbal Learning Test (CVLT-9) [28] and by the memory for faces and immediate visual reproduction subtests of the WMS-III [26]. Attention and executive functions were assessed by the Symbol Search [29], Trail B [30], a Stroop [31] task of inhibitory control, digit span backward [26] and the Wechsler Abbreviated Scale of Intelligence (WASI) Matrix Reasoning [25] tests. Statistical analysis Frequencies were calculated for WFD and PNR complaints. Chi-square analysis and Spearman rank correlations were used to examine the association between demographic and clinical variables and SLC. Repeated multivariate linear regression analysis was used to determine whether there was an association between SLC and objective test performance, in which the dependent variable was the score obtained on each of the cognitive tests and the explanatory variables were age, number of years of education, sex, GDS score, household company and WFD and PNR complaints. The last four variables were entered in the regression dichotomised as explained earlier. Comparisons were two tailed and considered significant with P < 0.05. Results Participants had a mean age of 66 years (±9.1; range 50–95), and the majority were women (60.3%). Mean educational level was 7.7 years (±4.1). Of all 479 participants, 478 completed the GDS and SLC questions, of whom 24% had a GDS score above 5% and 14.4% lived alone. Mean MMSE scores, SD and range by education groups were as follows: 26.3 + 2.2 (22–30) for 0–3 years of formal education; 27.9 + 1.7 (22–30) for 4–6 years of education; and 29.1 + 1.1 (25–30) for seven or more years of education. Half of the subjects (49.6%) complained of either type of SLC. Only 10.9% reported problematic PNR and 47.6% reported WFD. Neither type of language complaint correlated with age (rS = )0.028 and 0.017, respectively) nor with the number of years of education (rS = 0.028 and )0.05, respectively). Both were more common in women, in subjects with depressive symptoms and in those living alone (Table 1). None of the SLC correlated with cardiovascular risk factors. The two types of SLC had a mild correlation with each other (rS = 0.304; P < 0.001), considering all four possible answers to PNR. On the linear regression analysis, SLC correlated with objective performance on some cognitive tests, Table 1 Association between type of complaint and sex, household company and depressive symptoms Type of complaint Proper names % with complaints Sex Male 7.0 Female 13.1 Household company Alone 17.6 With company 9.7 GDS GDS > 5 20.0 GDS £ 5 8.0 Word finding v2 P % with complaints v2 P 4.2 0.05 35.5 54.6 16.1 0.01 4.0 0.04 60.8 45.3 6.0 0.01 12.9 0.01 72.2 39.9 36.4 0.01 controlling for age, sex, education, depression and household company (Table 2). Proper name retrieval had a significant correlation with the food and animal category fluency tests (P = 0.02 and P = 0.03, respectively), digit span forward (P < 0.001), CVLT-9 1–5 (P = 0.03) and immediate visual memory test (P = 0.03). WFD correlated with fewer tests, namely with food category fluency (P = 0.03) and CVLT-9 1–5 score (P = 0.03). Living alone had a marginal effect on objective performance on the food fluency test (B = )1.14; b = )0.09; t = )1.96; P = 0.051). The regression model was supported in all tests and measures, and the adjusted R2 accounted for between 17.2% (CVLT delayed recall) and 44% (WASI Vocabulary) of the variance in test performance. Discussion This study showed that SLC are common amongst adult and elderly individuals attending primary care and that they bear some relation with objective cognitive performance. In what concerns symptom frequency, the values found in our study were inside the range of subjective cognitive complaints cited in the literature (25–50%) in community studies [10]. However, WFD were more reported than PNR which was not expected because proper names are known to be more difficult to retrieve than common names [6]. Yet, these differences could also be attributed to the fact that the two questions used a different range of possible answers. In addition, Ôword findingÕ question did not specify the type of words Ôin failureÕ allowing for a broad interpretation, which might include proper names. Other studies performed with the same questionnaire yielded identical results 2012 The Author(s) European Journal of Neurology 2012 EFNS European Journal of Neurology How subjective are subjective language complaints 669 Table 2 Association between subjective language complaints and objective cognitive performance in neuropsychological tests Proper names Tests Language Category fluency (Food) Category fluency (Animals) Phonemic fluency (Letter ÔpÕ) Famous faces test WASI vocabulary Direct digit span Episodic memory CVLT (1–5) CVLT (20-min interval) Faces (WMS-III) Immediate visual memory (WMS-II) Executive and attention functions Stroop (interference) Invert digit span Trail B WASI matrix Symbol search Word finding B b T P B b T P )1.56 )1.39 )0.54 )1.31 0.65 )0.51 )0.10 )0.90 )0.04 )0.04 0.01 )0.14 )2.36 )2.19 )0.89 )0.10 0.40 )3.25 0.02 0.03 n.s. n.s. n.s. 0.00 )0.95 )0.50 )0.19 )0.79 )0.70 )0.69 )0.10 )0.53 )0.02 )0.04 )0.03 )0.03 )2.23 )1.24 )0.48 )1.00 )0.68 )0.68 0.03 n.s. n.s. n.s. n.s. n.s. )1.56 )0.16 )0.43 )5.36 )0.09 )0.03 )0.05 )0.08 )2.16 )0.63 )1.09 )2.14 0.03 n.s. n.s. 0.03 )1.01 )0.25 )0.39 )0.98 )0.10 )0.07 )0.04 )0.02 )2.18 )1.55 )0.91 )0.62 0.03 n.s. n.s. n.s. )0.33 )0.21 8.77 0.30 0.05 )0.01 )0.06 0.03 0.01 0.00 )0.26 )1.34 0.86 0.35 0.05 n.s. n.s. n.s. n.s. n.s. )0.56 0.05 1.93 0.62 )0.68 )0.03 0.02 0.01 0.05 )0.05 )0.69 0.49 0.30 1.14 )1.21 n.s. n.s. n.s. n.s. n.s. Repeated multiple linear regression analysis controlling for age, sex, living alone, education and depression (cut-off 5) demonstrated that PNR and WFD explained the variance of some language and memory tests. CVLT, California Verbal Learning Test. [22,32]. Thus, the frequency of complaints can be due to differences in the criteria used for sampling and assessing complaints. The two SLCs had a weak correlation with each other, suggesting that they do not represent exactly the same type of difficulty. Cognitive complaints are known to be more prevalent in women, in advancing age, and in subjects with subcortical white matter changes [33,34], yet we did not find any relation with age nor with vascular risk factors. This was also found in a sample with a much wider age range (from 18 to 92 years) using the same questionnaire [32]. According to that study, language complaints are less related with age than memory complaints. On the other hand, SLC were positively correlated with depressive symptoms and with living alone. Depression has been consistently associated with the total number of cognitive complaints [15,35]. They may result from a loss of self-esteem and increased focus on negative aspects of oneÕs life or abilities [36] because of the mood disturbance or depression-associated executive and memory decline [37]. Thus, it is important to screen for depression in patients presenting with language complaints. It was interesting to find that SLC were significantly more common in subjects living alone, a variable that was also marginally associated with a fluency test (food category). This might eventually suggest that maintaining regular conversations decreases language difficulties, which is in agreement with other findings about cognitive performance [38]. Indeed, social interactions can be viewed as natural forms of cognitive stimulation, whereas living alone would represent a situation of relative cognitive deprivation. Concerning objective cognitive performance, SLC were not only associated with tests that tackle language functions but also with a worse performance in learning and attention tasks. It is worth noticing that some tests like the CVLT 1–5 and digit spans are verbal tasks and may decrease with language difficulties. Semantic fluency tests were consistently associated with both SLC. A study performed in subjects submitted to temporal lobectomy [39] also found that word finding complaints correlated with semantic fluency but not with a Naming Test, nor with the Controlled Oral Word Association or other neuropsychological variables. In fact, semantic fluency tasks, contrarily to confrontation naming, not only require an access to semantic memory but also impose demands upon effortful self-initiated retrieval [40], which is more similar to spontaneous conversation. Compared to phonemic fluency tasks, those tests seem to be more dependent upon the integrity of semantic memory rather than on executive processes [41]. Furthermore, these tests are predictive of dementia in people with MCI [42]. Unexpectedly, there was no association between PNR and the ability to name famous faces, indicating that SLC may not have a strict relation with performance in the exact category that is the source of complaint. Although depressive symptoms could be fuelling complaints and were indeed correlated with both SLC, 2012 The Author(s) European Journal of Neurology 2012 EFNS European Journal of Neurology 670 I. P. Martins, I. Mares and P. A. Stilwell the association between symptoms and cognitive performance persisted after controlling for depression. It could be argued that these findings are related to a lack of sensibility of the test used to measure depression, but GDS was earlier found to have an overall sensitivity and specificity of 0.97 and 0.95 in a large geriatric community-living sample [43]. We acknowledge a number of limitations to this study. First, the two questions had a different scoring system, and as the question concerning WFD only had two possible answers, problematic complaints could not be defined in detail. Secondly, we only analysed two possible types of language complaints, and there may be more interesting and specific questions to analyse regarding language. Thirdly, the effect of depression on cognitive performance cannot be completely excluded, a limitation we tried to overcome by controlling for this variable in the regression analysis. Finally, because of the poor sensitivity of the MMSE to diagnose MCI or early stages of dementia, we cannot guarantee that all participants were cognitively intact and there may be a small number of participants with MCI or mild dementia in this sample. Nonetheless, some studies have shown that the use of MMSE to diagnose dementia in primary care has a negative predictive value of 95.7%, making it an acceptable tool to rule out dementia in this type of setting [44]. The low MMSE cut-off used is identical to the values established for populations with low levels of literacy [45]. Given these limitations and the population studied, results can only be generalised to adults without clinically evident dementia or known brain disease. Despite these limitations, this study is original, suggesting that (i) both SLC, WFD and PNR difficulties contributed to the variance in performance in some language and memory tests, independently of concurrent depressive symptoms, and (ii) SLC and cognitive performance are related with living alone, an association that has not been made before, suggesting that verbal interaction amongst ageing individuals might possibly be a modulator of cognitive awareness and performance. If these language findings are replicable, researchers and clinicians would benefit from asking older adults about perceived language decline. Further research is needed to investigate whether the endorsement of language complaints is associated with later decline. Acknowledgements The authors thank Fundação Calouste Gulbenkian for funding the present study (Project 0488) and are indebted to all participants, GPs and Health Centres Directors who collaborated in this study. 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