Abstract
Background:
Literacy is more consistently reported than education as protective against dementia in developing regions.
Objective:
To study the association of verbal literacy, numeracy, and music literacy with dementia in older Black and White Brazilians with a broad spectrum of education.
Methods:
We studied 1,818 Black, Mixed-race, and White deceased Brazilians 65 years or older at death (mean = 79.64). Data were retrospectively obtained within 36 hours after death in a face-to-face interview with an informant, usually a family member. Dementia was classified using the Clinical Dementia Rating (CDR) scale. Three forms of literacy were ascertained: verbal literacy (10 questions: reading and writing), numeracy (3 questions: multiplication, percentages, and use of a calculator), and music literacy (1 question: reading music). Black (11%) and Mixed-race (23%) older adults were combined in analyses. Models adjusted for age and sex.
Results:
Dementia was identified in 531 people. Participants had 0 to 25 years of education (median = 4). More literacy was associated with lower odds of dementia (all p≤0.039). Participants that read music had about half the odds of having dementia. Participants in the highest quartile of numeracy and verbal literacy had respectively 27%and 15%lower odds of having dementia compared to the lowest quartile. Literacy was lower in Blacks (p < 0.001, except music p = 0.894) but the effect of literacy on dementia was similar (interaction p > 0.237). In secondary analyses, playing instruments without reading music was not associated with dementia (p = 0.887).
Conclusion:
In a large sample of Brazilians, verbal literacy, numeracy, and music literacy were associated with lower odds of dementia. The effect was similar across races.
INTRODUCTION
Latin America and the Caribbean currently have 56 million persons that are aged 65 years or older [1]. Brazil is the largest country in Latin America and ranks as the 6th country with the largest population of 65 years and older adults, more than 19 million, just behind China, India, United States, Japan, and Russia [1]. The sociological structure of race in Brazil is quite unique. Brazil has a specific category of “mixed” in the Census (IBGE –The Brazilian Institute of Geography and Statistics). Brazilians self-identify as Black, White, or Mixed (termed as “Pardos(as)”). The first author and two co-authors are all native Brazilians. For a variety of historical reasons, in Brazil, interracial marriages have long been and continue to be quite common, and those self-identifying as Mixed are quite frequent in the population. Brazil is also one of the most diverse countries in Latin America. The Brazilian Census uses a question on self-identified race that includes, among others, the categories White, Black, and Mixed. A total of 47%of the Brazilians self-identify as Mixed, 44%self-identify as Whites, and 9%self-identify as Blacks [2], making Brazil a rich environment to study racial differences.
Literacy is one of the cognitive abilities that may provide cognitive reserve and thus higher resilience to decline despite dementia-related neuropathology [3]. Literacy can be acquired from both formal and informal education. A large study on incident dementia including participants from Cuba, Dominican Republic, Venezuela, Peru, Mexico, and China found an overall additional independent effect of literacy, controlling for educational level [4]. Studies of Brazilians have found an association between illiteracy and a higher risk of dementia [5–7]. None of these studies with Brazilians have examined race differences in the effect of literacy on dementia, although this has been studied in other populations [8].
In addition to the more classic literacy (reading, writing, and numeracy), music literacy is an enrichment often available in higher-resourced schooling systems. Music instruction or playing instruments has been shown to be associated with lower odds of cognitive impairment and dementia, higher cognition, and more neuroplasticity [9–14]. Different types of literacy have been studied in the context of cognitive decline [15], but to our knowledge, this is the first study to examine music literacy and dementia in Brazilians. In fact, the majority of studies on music and dementia overall are from Asia, Europe, and the United States [16]. With great racial diversity and the culture of music among all strata of society (e.g. percussion instruments in the Samba Schools and string instruments in Pagode, a subgenre of Samba), the study of music literacy in Brazil can provide a unique contribution to the knowledge of the role of music on protection against dementia prevention among individuals of different races and with lower schooling.
In the present study, we examined the association of different forms of literacy including music literacy and dementia in a large sample of Black, Mixed, and White Brazilians with a broad spectrum of formal education enrolled at autopsy by their legal representative in the Pathology, Alzheimer’s, and Related Dementias Study (PARDoS). We hypothesized that higher literacy would be associated with lower odds of dementia, independent of years of education and other confounders. We also examined racial differences in these associations. We hypothesized the association is dependent on race after important demographics are considered.
MATERIALS AND METHODS
Decedents
PARDoS enrolls deceased older adults who died from natural non-violent causes in the state of São Paulo, Brazil, and includes cases originally enrolled in the Study of Ancestry and Neurodegenerative Diseases. Representatives of eligible deceased were identified, consented, and interviewed face-to-face by nurses within 36 hours of decedent’s death, after registering at the Autopsy Services or Hospital while waiting for funeral arrangements. Further details on recruitment were described previously [17].
From September 2016 to the date of submission, PARDoS enrolled a total of 1,949 proxy-declared Whites, Blacks, or Mixed Brazilian decedents age 65 years and older. The informants of the decedents completed the Cognitive Abilities as part of the study. Among these, 1,818 (93.3%) decedents had complete data and were included in the current analysis. Those not included had similar age at death as the analytic sample (mean of 79.64 versus 81.02 for included versus excluded, t[1947] = 1.71, p = 0.088), but did not differ in education (median of 4 for both included and excluded, Wilcoxon rank-sum test with continuity correction z = –1.252, p = 0.211), sex (53%versuss 60%for included versus excluded, χ2 [1] = 2.09, p = 0.149) or race (34%versus 38%of Blacks χ2 [1] = 0.97, p = 0.324). Their informants knew the deceased a similar number of years (46.75 years versus 46.23 for included vs. excluded, t[1509] = –0.40, p = 0.690). The study was approved by all local ethics committees and by the Brazilian national ethics committee (Comissão Nacional de Ética em Pesquisa, CONEP). Because the index cases were decedents, the study was determined to be non-human subjects research and thus IRB exempt in the United States.
Measures
The diagnosis of dementia proximate to death was obtained through the CDR as described previously [17, 18]. Informants answered questions about the decedent 3 months before death. Using the answers, 6 domains were scored: memory, orientation, judgment and problem solving, community affairs, home and hobbies, and personal care. Dementia status was computed using an algorithm based on the domains affected and level of impairment. Mild cognitive impairment or no-cognitive impairment was considered not demented.
Literacy, numeracy, and music literacy were assessed with items from a cognitive abilities questionnaire adapted and expanded from the Premorbid Cognitive Abilities Scale (PCAS) [19]. The intraclass correlation coefficient of the PCAS was previously tested using postmortem informant and showed good inter-informant reliability of 0.96 [19]. From the items (1 = yes, 0 = no), three forms of literacy were ascertained: verbal literacy, numeracy, and music literacy. Verbal literacy represents the average of 10 questions: 1) “read and understand short phrases”, 2) “read and understand articles in newspapers or magazines”, 3) “read and understand a prescription”, 4) “read and understand an entire book”, 5) “keep track of subtitles on a foreign film”, 6) “make a shopping list”, 7) “take a message”, 8) “fill out a form with personal data”, 9) “write a letter to someone else”, and 10) “find a phone number in an address book or phone book”. Numeracy represents the average of 3 questions: 1) “Calculate multiplications”, 2) “Calculate percentages”, 3) “Use a calculator to do simple operations”. Music literacy was represented by one question: “read music”. The polychoric alpha coefficient was 0.98 for verbal literacy and 0.92 for numeracy. Verbal literacy and numeracy were positively correlated with education (verbal literacy rs = 0.691, p < 0.001; numeracy rs = 0. 569, p < 0.001). Education was skewed with half of the participants with 4 years or less of education. Decedents that read music tended to have more year of education (upper quartile of 8 years versus 6 years, Wilcoxon with continuation correction z = 5.20, p < 0.001).
In addition to three literacy variables obtained from the cognitive abilities questionnaire, for secondary analyses, we also used an added item “Play a musical instrument with dexterity” in combination with an earlier question on the hobbies section “Did he/she play a musical instrument very well?”. The goal was to understand if playing an instrument without the cognitive exercise of reading music was also associated with lower odds of dementia. We created a variable with three categories: reading music (n = 102), playing an instrument without reading music (n = 75), and not reading music or playing an instrument (the reference).
The proxy-reported race was also obtained as Whites, Blacks, or Mixed, in line with the Brazilian Census [2]. In addition, the socioeconomic status and social class grouping were obtained using the Brazilian Association of Market Research Companies (Associação Brasileira de Empresas de Pesquisa –ABEP) scale [20, 21]. This scale considers different household goods and services that are relevant to the Brazilian culture including the number of maids working in the household and the number of color TVs, radios, bathrooms, cars, washing machines, VHS/DVD players, refrigerators, and freezers in the household. It also considers the level of education of the head of the household. [20, 21].
Statistical analyses
Initial analyses included a careful examination of the distributions of the variables. Race differences were examined using t-tests or nonparametric tests for variables that deviated from normality or chi-square tests as appropriate. In the analyses, Blacks and Mixed-race were combined in the Black group to ease comparison with previous literature especially from other countries which do not have an explicit census category of Mixed. There was no difference between Blacks and Mixed-race on age of death, sex, education, or any of the literacy items. We also modeled literacy using an ordinal model to examine sex and race differences adjusting for years of education.
We examined the effect of years of education in a logistic regression model adjusted for age-at-death and sex. We repeated the model replacing the term for years of education by each literacy type (three separate models). Next, we performed a series of sensitivity analyses. First, we tested whether the effect of literacy on the odds of dementia would be explained by race, socioeconomic status, or education. We reran the three separate models (with terms for each literacy), adding a term for race, socioeconomic status, and education. Because socioeconomic status, education, and literacy can be highly interrelated with socioeconomic status representing the opportunity for schooling [22], we perform a second set of sensitivity analyses. We examined the effect of literacy in a very homogeneous subset of individuals composed of 520 decedents in social class C that had 4 years of education (equivalent to elementary school education). These analyses adjusted for age-at-death and sex. Age and education were centered at the mean for ease of interpretation. Standard diagnostic methods were employed to verify that assumptions underlying the statistical models were adequately met. All analyses considered an alpha of 0.05 and were conducted using SAS/STAT software, Version 9.4 of the SAS® system for Linux.
RESULTS
Decedents were aged 65 to 110 years at death. About one-third were Black, half were women, and one-third had dementia. Most of the decedents belonged to social class C (3.4%in social class A, 35%in social class B, 55.1%in social class C, and 6.5%below social class C). Most of the informants were family members, primarily the sons/daughters of the decedents (71.8%) followed by grandchildren (9.1%), siblings (4.9%), and spouses (4.5%). Table 1 shows the key demographic characteristics of the decedents and informants. Education and sex distribution of the informants of decedents both with and without dementia were similar (both with 11 years of education and 53%to 55%of men). Informants of decedents with dementia were on average three years older (51.39, 95%CI = 50.39, 52.39 versus 48.45, 95%CI = 47.75, 49.15 years old) than informants of decedents without dementia.
Demographic characteristics of decedents and informants
aBlack includes 199 Blacks and 418 mixed.
Table 2 shows a comparison of Black with White decedents on education and literacy variables. The racial groups had the same ranges of literacy and education (range of verbal literacy: 0 to 1; numeracy 0 to 1 and education 0 to 25 years), and sim-ilar ranges of age at death (Blacks: 65 to 110 years at death, Whites: 65 to 105 years at death). Whites, however, had higher median education and literacy (Table 2). Verbal literacy was higher for Whites, even after controlling for years of education (βadjusted = –0.404, SE = 0.101, p≤0.001) and there was a significant interaction between education and race (βinteraction = 0.111, SE = 0.034, p = 0.001) indicating that the race difference in literacy was higher among individuals with fewer years of education. That is, Blacks had less literacy (a negative effect) but the difference in literacy between Blacks and Whites with few years of education was larger than between Blacks and Whites with more education (a positive interaction effect). Results remained significant when socioeconomic status was added to the model. Men had more years of education (βunadjusted = 0.82, SE = 0.09, p≤0.001) and higher literacy (βunadjusted = 0.59, SE = 0.08, p≤0.001), but literacy did not differ by sex after controlling for years of education (βadjusted = 0.097, SE = 0.089, p = 0.273). This was consistent across race with similar results found when examining Blacks and Whites separately. The odds of dementia also did not differ between Black and White decedents (OR = 0.978, β= –0.0224, SE = 0.1164, p = 0.8474), controlling for sex and age at death.
Education and literacy by race
Test statistic are chi-square test, except for *Wilcoxon rank sum test with continuity correction z.
A total of 309 decedents had zero years of education (51%Black). As expected, they had zero median verbal literacy and numeracy and only 1%knew how to read music. However, some literacy was observed, especially in numeracy as 19%could multiply, 12%could calculate percentages, and 8%could do a simple operation with a calculator. Verbal literacy was extremely low but 10%could use a phone book and 8%could read a phrase.
All forms of literacy were associated with lower odds of dementia (Table 3). Participants in the highest quartile of verbal literacy had 15%lower odds of having dementia compared to the highest quartile. Participants in the highest quartile of numeracy had 27%lower odds of having dementia compared to the lowest quartile. Participants that read music had about half the odds of having dementia. The effect of all literacy types on dementia was similar between Blacks and Whites (Supplementary Table 1, ps > 0.237).
Logistic models with dementia as the outcome (n = 1.818)
Low education includes individuals with 4 or fewer years of education. High education includes individuals with more than 4 years of education and excluding no literacy (literacy < 0.15) or zero numeracy to reduce potential bias due to learning disability. *Three separate models adjusted for age at death and sex.
In the first set of sensitivity analyses, we reran the three models with each literacy type, adjusting age-at-death and sex and, in addition, adjusting for race, socioeconomic status, and education. All literacy remained associated with lower odds of dementia (all p≤0.010). In the second set of sensitivity analyses, we only examined a subset of individuals in social class C that had 4 years of educations. The median literacy and numeracy were respectively 0.80 (IQR = 0.60 to 0.90) and 0.67 (IQR = 0.34 to 1.00), and 6%read music. We reran the three models with each literacy type adjusting for age-at-death and sex. Literacy, numeracy, and music literacy remained associated with lower odds of dementia (all p≤0.034).
In a secondary analysis, we examined the effect of playing an instrument without reading music on the odds of dementia. We used a variable with three categories: reading music, playing an instrument without reading music, and not reading music or playing an instrument (the reference). The effect of reading music remained the same (OR = 0.48, 95%CI = 0.27, 0.85), while the effect of only playing an instrument was smaller and not significant (OR = 0.96, 95%CI = 0.56, 1.66, p = 0.887).
DISCUSSION
In this study with older deceased Brazilians with a wide spectrum of education, we found that multiple types of literacy, including verbal literacy, numeracy, and music literacy, were associated with lower odds of dementia. This adds to a growing literature suggesting that all forms of literacy are protective against dementia. We also show that the effect of literacy on dementia is similar across races. In sensitivity analyses, we showed that the effect was also significant in a group with homogeneous education (all with 4 years of education) and socioeconomic status (all social class C).
Education and literacy (including music instruction) are associated with a higher level of cognition [3, 23]. Education and literacy are thought to build cognitive reserve, which increases the ability to tolerate aging-related changes in the brain without developing clinical symptoms [24]. That can happen through both protective and compensatory mechanisms in a dynamic interaction of the brain and environmental stimuli. Imaging studies suggest that education changes the brain morphology and is associated with regional cortical thickness [25], brain size [26], and microstructural changes of the hippocampus [27]. There is, however, a threshold hypothesis supported by evidence from clinical and biological studies that indicate that there is initial protection against the clinical manifestation of dementia but after brain pathology reaches a critical level there is a more rapid cognitive decline [28], although these mechanisms are not fully understood.
We also show that the effect of all three types of literacy on dementia did not differ by race. To our knowledge, racial differences in the effect of literacy on dementia have not been examined in older Brazilians. The two racial groups had similar benefits from literacy. However, since all types of literacy, except music literacy, were lower in Blacks, this group may benefit more from intervention on literacy. A recent literature review including studies of children with low socioeconomic status suggested that programs that integrate both linguistic and metalinguistic skills are more effective [29]. It also mentions initiatives such as the Venezuelan program “Mochila Mágica” (or the “Magic Backpack”) that lend books and train teachers and parents to support reading at home.
Most of the Brazilian population attending school are enrolled in the public system: 83%of elementary students and 88%of secondary students. Brazil also has free public early child education/daycare for poor families. Although in recent decades inequality has been declining in Brazil [30], high levels of inequality persist and are reflected in the education system. While an upper-middle-class child will have access to education similar to the top education of any developed country [31], the poor struggle to get a few years at an under-resourced primary school. Given the educational inequalities, one year of a private school located in a prosperous neighborhood is not equivalent to one year in a public school located in the poor outskirts of large cities or in remote rural areas. A study examined admission test scores for a federal university in the Northeast region (Universidade Federal de Pernambuco) and found that public school students’ scores were on average 4 to 17%lower than the scores of private school students [32]. On top of the educational inequalities, other factors such as nutrition and childhood stress can also contribute to the literacy inequalities. Although these inequalities in Brazil transcend race, Black and Mixed-race individuals are disproportionally affected by them. We found racial differences in literacy in almost all indicators. Black and Mixed-race individuals were found to have lower verbal literacy, especially among participants with fewer years of education. Although we adjusted for socioeconomic status, our information is limited and does not reflect the resources the person may have had earlier in life.
This study has several strengths. The study includes a large sample size of both Black/Mixed-race and White Brazilians with a wide spectrum of education. It uses informants, mostly the decedent’s children, who knew the deceased for many years. In aging research, informants are commonly used to obtain information on older adults with cognitive impairment and after death. The study also used measures, such as PCAS and CDR, that have been validated as a proxy report and are commonly used with informants in prior research with Brazilians [33]. The study also has limitations. By design, individuals with lower education are over-represented in our study. Although this gives us important variability to study, this is not, however, a population-based study, and generalizability may be limited. In addition, although literacy in the study of dementia is often obtained using reported abilities like reading and writing, literacy was not obtained from proficiency examinations. It is always possible to have some bias and inaccuracies. The decedent may not have shared some information with the family member serving as the informant. For example, they may have learned to play an instrument earlier in life and never mentioned that to their children. Recall bias may also create inaccuracies when data is collected retrospectively [34]. Therefore, the effect may be underestimated as the reference group has more variability. Similarly, the CDR may have a bias, although the window of reference (3 months before death, instead of a lifetime) makes this less likely. Since this study is cross-sectional, we cannot test temporal order. Finally, the question used to assess the role of reading music is just a first look into this research question for this population. Although standard musical notation includes bar lines, treble, and bass clef, other forms of music notations such as guitar/lute-playing and percussion instrumentation include chord designations, string/fingering notations (tablature), or linear representations of strikes. This variability is not captured here. Therefore, further studies can help confirm and extend these findings, including prospectively collected data or studies including brain pathology.
Footnotes
ACKNOWLEDGMENTS
The authors acknowledge that some of this work was performed at the Sao Paulo Autopsy Center and in the Gerolab at FMUSP, Sao Paulo. All data contained in this manuscript were collected by staff funded by NIH grant R01AG54058. All data was collected by electronic systems set up and run by the PI and his staff at the Rush Alzheimer's Disease Center, Rush University Medical Center, Chicago.
