Archives of Gerontology and Geriatrics 60 (2015) 206–209
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Archives of Gerontology and Geriatrics journal homepage: www.elsevier.com/locate/archger
Global cortical atrophy (GCA) associates with worse performance in the Montreal Cognitive Assessment (MoCA). A population-based study in community-dwelling elders living in rural Ecuador§ Oscar H. Del Brutto a,b,*, Robertino M. Mera c, Mauricio Zambrano d, Francisco Soriano d, Julio Lama e a
School of Medicine, Universidad Espı´ritu Santo – Ecuador, Guayaquil, Ecuador Department of Neurology, Hospital-Clı´nica Kennedy, Guayaquil, Ecuador Gastroenterology Department, Vanderbilt University, Nashville, TN, United States d Community Center, The Atahualpa Project, Atahualpa, Ecuador e Department of Imaging, Hospital-Clı´nica Kennedy, Guayaquil, Ecuador b c
A R T I C L E I N F O
A B S T R A C T
Article history: Received 10 July 2014 Received in revised form 18 September 2014 Accepted 21 September 2014 Available online 26 September 2014
Background/objective: Increasing numbers of individuals with cognitive impairment are posing economic threads to the developing world. Proper assessment of this condition may be complicated by illiteracy and cross-cultural factors. We conducted a population-based study in elders living in rural Ecuador to evaluate whether the MoCA associated with structural brain damage in less-educated populations. Methods: Atahualpa residents aged 60 years were identified during a door-to-door survey and invited to undergo MRI for grading GCA. Using a multivariate generalized linear model, we evaluated whether MoCA scores correlates with GCA, after adjusting for demographics, education, cardiovascular health (CVH) status, depression and edentulism. Results: Out of 311 eligible persons, 241 (78%) were enrolled. Mean age was 69.2 7.5 years, 141 (59%) were women, 199 (83%) had primary school education, 175 (73%) had poor CVH status, 30 (12%) had symptoms of depression and 104 (43%) had edentulism. Average MoCA scores were 18.5 4.7 points. GCA was mild in 108, moderate in 95, and severe in 26 persons. Total and most domain-specific MoCA scores were significantly worse in persons with moderate to severe GCA. In the multivariate model, mean MoCA score was associated with GCA severity (b = 2.38, SE = 1.07, p = 0.027). Conclusions: MoCA scores associate with severity of GCA after adjusting for potential confounders, and may be used as reliable estimates of structural brain damage. However, a lower cut-off than that recommended for developed countries, would be better for recognizing cognitive impairment in less educated populations. ß 2014 Elsevier Ireland Ltd. All rights reserved.
Keywords: Montreal cognitive assessment Global cortical atrophy Population-based study Atahualpa project Ecuador
1. Introduction The number of individuals with cognitive impairment is steadily increasing in the developing world (Llibre Rodriguez et al., 2008). This poses challenges and huge economic threads in regions where health resources are stretched to the limits. Accurate estimates of the burden of cognitive impairment are mandatory for public health planning in underserved populations.
§ Funding: This study was partially supported by Universidad Espı´ritu Santo – Ecuador, Guayaquil, Ecuador. * Corresponding author at: Air Center 3542, PO Box 522970, Miami, FL 331522970, United States. Tel.: +1 59342285790; fax: +1 59342280053. E-mail address: [email protected] (O.H. Del Brutto).
http://dx.doi.org/10.1016/j.archger.2014.09.010 0167-4943/ß 2014 Elsevier Ireland Ltd. All rights reserved.
Nevertheless, such assessment may be complicated by illiteracy and cross-cultural factors, which could make some of the most commonly used screening instruments non-reliable (Maestre, 2012). In this context, it has been suggested that the MoCA – a test created in developed countries – might overestimate the prevalence of cognitive impairment in subjects living in rural areas of developing countries (Go´mez, Zunzunegui, Lord, Alvarado, & Garcı´a, 2013). Lower cut-off scores or adjustments for regionspecific risk factors that may influence cognition have been proposed when using the MoCA in these populations. However, there has been no attempt to correlate cognitive performance with neuroimaging studies to evaluate whether – irrespective of cutoffs – MoCA scores actually reflect the severity of structural brain damage in less-well educated individuals. We conducted a
O.H. Del Brutto et al. / Archives of Gerontology and Geriatrics 60 (2015) 206–209
population-based study in community-dwelling elders living in rural Ecuador to correlate MoCA scores with severity of GCA as assessed by MRI.
2. Methods The protocol and the informed consent were approved by the I.R.B. of Hospital-Clı´nica Kennedy, Guayaquil, Ecuador (FWA 00006867). The Atahualpa project is a population-based cohort study designed to reduce the increasing burden of non-communicable diseases in rural Ecuador (Del Brutto, 2013). The village was selected because it is representative of the region. More than 95% of the population belong to the Native/Mestizo ethnic group (Amerindians) and their living characteristics have been detailed ˜ aherrera, et al., 2014). elsewhere (Del Brutto, Pen For this part of the Atahualpa project, trained rural doctors conducted a door-to-door survey to identify all Atahualpa residents aged 60 years. During the survey, we assessed the CVH status of all participants by the use of the seven metrics proposed by the American Heart Association, including smoking status, body mass index, physical activity, diet, blood pressure, fasting glucose, and total cholesterol blood levels; each metric was categorized as ideal, intermediate, and poor, and the CVH status
207
was classified as poor if at least one metric was in the poor range (Del Brutto et al., 2013). Participants were also evaluated with the depression axis of the Depression-Anxiety-Stress Scale-21 (DASS-21), a consistent field instrument that quantitatively measures dysphoria, hopelessness, devaluation of life, self-deprecation, lack of interest/involvement, anhedonia and inertia, with seven questions that are rated on a four-point Likert scale ranging from 0 (not at all) to 3 (almost always) with a maximum total score of 21, and a diagnosis of depression in persons who have 5 points (Osman et al., 2012). In addition, a rural dentist performed an oral exam with emphasis on the number of remaining teeth; individuals were classified in two groups according to whether they have severe edentulism – defined as those who have less than 10 remaining teeth – or not (Del Brutto, Gardener, et al., 2014). Cognitive performance was assessed using the Spanish version of the MoCA test (www.mocatest.org, ß Z. Nasreddine MD, version 07 November 2004). The MoCA evaluates major cognitive domains: visuospatial-executive (trail making B task, 3-dimentional cube copy, and clock drawing) for a maximum of 5 points; naming (unfamiliar animals) for a maximum of 3 points; language (sentence repetition, and a phonemic fluency task) for a maximum of 3 points; short-term memory (delayed recall or words) for a maximum of 5 points; abstraction (verbal abstraction) for a
Fig. 1. FLAIR MRIs (TR 9000, TE 120, TI 2500) showing severity of GCA according to Pasquier and co-workers. From left to right, columns represent absent, mild, moderate and severe global GCA respectively. In mild GCA there is sulcal opening peripherally (thick arrows). Moderate GCA is characterized by widening along the length of the sulci (arrowheads). Severe GCA is present when there is gyral thinning (thin arrows). Images correspond to four different persons aged 60 to 65 years.
208
O.H. Del Brutto et al. / Archives of Gerontology and Geriatrics 60 (2015) 206–209
maximum of 2 points; attention and calculation (digits forward and backward, target detection using tapping, serial 7’s subtraction) for a maximum of 6 points; and orientation (time and space) for a maximum of 6 points. Maximum MoCA score is 30 points, with an additional point given to persons with 12 years of education (Nasreddine et al., 2005). We did not used a cutoff score for defining cognitive impairment, but the continuous MoCA score to avoid problems related to poor reliability of specific cutoffs. Persons who signed the informed consent and had no contraindications for the practice of MRI were moved to Guayaquil. All studies were performed with a Philips Intera 1.5 T (Philips Medical Systems, the Netherlands) at Hospital-Clı´nica Kennedy. MRI included two-dimensional multi-slice turbo spin echo T1-weighted, fluid attenuated inversion recovery (FLAIR), T2-weighted, and gradient-echo sequences in the axial plane, as well as a T1weighted sequence oriented in the sagittal plane. We used the preestablished brain imaging package delivered by the manufacturer to homogenize applicability by technicians; slice thickness was 5 mm with 1 mm gap between slices. A neurologist (OHD) and a neuroradiologist (JL) independently read all MRIs, blinded to clinical data. Primary interest was focused on the presence of GCA, using the visual scale proposed by Pasquier et al. (1996) (Fig. 1). Kappa coefficients for inter-rater agreement (n = 258) were 0.76 for severity of GCA, and disagreements were resolved by consensus. All analyses were carried out by using STATA version 13 (College Station, TX, USA). Descriptive statistics are presented as means standard deviations for continuous variables and as percentages with 95% C.I. for categorical variables. A p value of less than 0.05 is considered significant. Using a multivariate generalized linear model, we examined the association between GCA and MoCA score, after adjusting for demographics, education, CVH status, edentulism and depression.
3. Results The door-to-door survey identified 311 Atahualpa residents aged 60 years, 258 (83%) of whom underwent a brain MRI. Reasons for not obtaining MRI included refusal to participate (n = 26), severe disability (n = 11), claustrophobia (n = 8), and implanted pacemaker (n = 1); seven additional persons had died or emigrated between the survey and the invitation. Seventeen of the
258 persons who had an MRI could not perform the MoCA due to aphasia or severe visual or hearing impairment. Therefore, the present study included 241 persons. Mean age was 69.2 7.5 years, 141 (59%) were women and 199 (83%) had primary school education only. A poor CVH status was noticed in 175 (73%) persons and the mean SD number of poor metrics per person was 1.2 1. Thirty persons (12%) had symptoms of depression and 104 (43%) had severe edentulism. Mean scores in the MoCA were 18.5 4.7 points. A total of 229 persons (95%) had GCA, which was mild in 108, moderate in 95, and severe in 26. As only 12 persons had no GCA, they were grouped with those with mild GCA for analysis. Univariate analysis showed that persons with moderate to severe GCA were older, less educated and more often edentulous than those with none-mild GCA (Table 1). In addition, total and domain-specific MoCA scores (with the exception of abstraction) were significantly worse in persons with moderate to severe GCA (Table 2). In the multivariate generalized linear model, mean MoCA score was significantly associated with GCA severity, after adjusting for demographics, education, CVH status, depression and edentulism (b = 2.38, SE 1.07, p = 0.027). The contrast between none-mild and severe GCA represented a 12.8% (95% C.I.: 2–23%) change in the MoCA score.
4. Discussion Results of the present study show that MoCA scores associate with severity of GCA after adjusting for a number of confounders, and suggest that this field instrument may be used as an estimate of structural brain damage in less educated elders. The MoCA is a widely used screening instrument that assesses multiple cognitive domains anatomically linked to different cortical areas (Julayanont, Phillips, Chertkow, & Nasreddine, 2013 Chap. 6). However, volumetric MRI studies attempting to correlate MoCA scores with cortical abnormalities have been inconclusive (Paul et al., 2011). More attention has been given to worse performance in the MoCA scores associated with white matter lesions, but it has recently been demonstrated that cognitive impairment associated with white matter lesions is mediated by cortical atrophy (Zi, Duan, & Zheng, 2014). Studies conducted in Western populations suggested a MoCA cut-off score 25 to separate normal subjects from those with mild cognitive impairment (Nasreddine et al., 2005). Asian and Latin
Table 1 Characteristics of community-dwelling elders living in Atahualpa according to the severity of GCA.
Age, mean SD years Women, n (%) Up to primary school, n (%) Poor CVH status, n (%) Symptoms of depression, n (%) Severe edentulism, n (%)
Total series n = 241
None-mild GCA n = 120
Moderate GCA n = 95
Severe GCA n = 26
Significance
69.2 7.5 141 (59%) 199 (83%) 175 (73%) 30 (12%) 104 (43%)
64.8 3.5 70 (58%) 90 (75%) 84 (70%) 14 (12%) 41 (34%)
72.1 7.3 53 (56%) 86 (91%) 68 (72%) 13 (14%) 49 (52%)
79.2 7.5 18 (69%) 23 (88%) 23 (88%) 3 (12%) 14 (54%)
0.0001 0.468 0.008 0.153 0.726 0.019
Table 2 Mean SD total and domain-specific MoCA scores in community-dwelling elders living in Atahualpa according to the severity of GCA.
Total MoCA score, max 30 pts Visuospatial-executive, max 5 pts Animal naming, max 3 pts Language, max 3 pts Short-term memory, max 5 pts Abstraction, max 2 pts Attention and calculation, max 6 pts Orientation, max 6 pts
Total series n = 241
None-mild GCA n = 120
Moderate to severe GCA n = 121
Significance (p)
18.49 4.68 2.82 1.08 1.73 1.00 1.14 0.92 1.50 1.49 1.77 0.53 3.31 1.76 5.26 0.96
20.33 3.90 3.02 1.05 1.88 0.93 1.40 0.97 1.98 1.39 1.78 0.54 3.85 1.49 5.45 0.72
16.68 4.68 2.62 1.07 1.58 1.04 0.88 0.79 1.03 1.43 1.75 0.52 2.77 1.84 5.07 1.11
0.0001 0.004 0.019 0.0001 0.0001 0.661 0.0001 0.002
O.H. Del Brutto et al. / Archives of Gerontology and Geriatrics 60 (2015) 206–209
American studies recommended lowering the original cut-off score for diagnosing mild cognitive impairment in less-educated populations; however, these studies have not been based on neuroimaging correlation of cognitive performance in the MoCA, but on comparisons with results obtained in other neuropsychological tests (Go´mez et al., 2013; Lee et al., 2008). In the present study, persons with none or mild GCA have a mean MoCA score of 20 points (Table 2), suggesting that this is probably a better cut-off value for defining mild cognitive impairment in less-educated populations. Our results concur with a recent Indian study, where 48% of patients with mild cognitive impairment and abnormal neuroimaging had diffuse cortical atrophy on CT or MRI (Alladi et al., 2014). We did not use volumetric assessment of cortical gray matter but relied on a visual rating scale, and this is a limitation of the present study. However, the population-based design together with the homogeneous characteristics of Atahualpa’s residents and the model used for assessing the association between GCA and cognitive performance, argues for the strength of our results. A complete battery of neuropsychological tests for diagnosing cognitive impairment may be unfeasible in population-based studies conducted in rural villages of developing countries, and the MoCA appears to be a simple and reliable option to assess cognition in these underserved populations. Conflict of interest The authors have nothing to disclose. References Alladi, S., Shailaja, M., Mridula, K. R., Haritha, C. A., Kavitha, N., Khan, S. A., et al. (2014). Mild cognitive impairment: Clinical and imaging profile in a memory clinic setting in India. Dementia and Geriatric Cognitive Disorders, 37(1–2), 113–124. Del Brutto, O. H. (2013). Implications and expectancies of the Atahualpa project: A population-based survey designed to reduce the burden of stroke and cardiovascular diseases in rural Ecuador. Journal of Neurosciences in Rural Practice, 4(3), 363–365.
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Del Brutto, O. H., Gardener, H., Del Brutto, V. J., Maestre, G. E., Zambrano, M., Montenegro, J. E., et al. (2014). Edentulism associates with worse cognitive performance in Community-dwelling elders in rural Ecuador: Results of the Atahualpa project. Journal of Community Health. http://dx.doi.org/10.1007/ s10900-014-9857-3 Del Brutto, O. H., Pen˜aherrera, E., Ochoa, E., Santamarı´a, M., Zambrano, M., & Del Brutto, V. J. (2014). Door-to-door survey of cardiovascular health, stroke, and ischemic heart disease in rural coastal Ecuador – The Atahualpa project: Methodology and operational definitions. International Journal of Stroke, 9(4), 367–371. Del Brutto, O. H., Santamarı´a, M., Ochoa, E., Pen˜aherrera, E., Santiba´n˜ez, R., PowChomn-Long, F., et al. (2013). Population-based study of cardiovascular health in Atahualpa, a rural village of coastal Ecuador. International Journal of Cardiology, 268(2), 1618–1620. Go´mez, F., Zunzunegui, M. V., Lord, C., Alvarado, B., & Garcı´a, A. (2013). Applicability of the MoCA-S test in populations with little education in Colombia. International Journal of Geriatric Psychiatry, 28(8), 813–820. Julayanont, P., Phillips, N., Chertkow, H., & Nasreddine, Z. S. (2013). Montreal Cognitive Assessment (MoCA): Concept and clinical review. In A. J. Larner (Ed.), Cognitive screening instruments. A practical approach (pp. 111–151). London, UK: SpringerVerlag. Lee, J.-K., Lee, D. W., Cho, S.-J., Na, D. L., Jeon, H. J., Kim, S.-K., et al. (2008). Brief screening for mild cognitive impairment in elderly outpatient clinic: Validation of the Korean Version of the Montreal Cognitive Assessment. Journal of Geriatric and Psychiatry Neurology, 21(2), 104–110. Llibre Rodriguez, J. J., Ferri, C. P., Acosta, D., Guerra, M., Huang, Y., Jacob, K. S., et al. (2008). Prevalence of dementia in Latin America, India, and China: A populationbased cross-sectional survey. Lancet, 372(9637), 464–474. Maestre, G. E. (2012). Assessing dementia in resource-poor countries. Current Neurology and Neuroscience Reports, 12(5), 511–519. Nasreddine, Z. S., Phillips, N. A., Be´dirian, V., Charbonneau, S., Whitehead, V., Collin, I., et al. (2005). The Montreal cognitive assessment, MoCA: A brief screening tool for mild cognitive impairment. Journal of the American Geriatric Society, 53(4), 695–699. Osman, A., Wong, J. L., Bagge, C. L., Freedenthal, S., Gutierrez, P. M., & Lozano, G. (2012). The Depression Anxiety Stress Scale–21 (DASS-21): Further examination of dimensions, scale reliability, and correlates. Journal of Clinical Psychology, 68(12), 1322–1338. Paul, R., Lane, E. M., Tate, D. F., Heaps, J., Romo, D. M., Akbudak, E., et al. (2011). Neuroimaging signatures and cognitive correlates of the Montreal Cognitive Screen in a nonclinical elderly sample. Archives of Clinical Neuropsychology, 26(5), 454–460. Pasquier, F., Leys, D., Weerts, J. G., Mounier-Vehier, F., Barkhof, F., & Scheltens, P. (1996). Inter- and intraobserver reproducibility of cerebral atrophy assessment on MRI scans with hemispheric infarcts. European Neurology, 36(5), 268–272. Zi, W., Duan, D., & Zheng, J. (2014). Cognitive impairments associated with periventricular white matter hyperintensities are mediated by cortical atrophy. Acta Neurologica Scandinavica. http://dx.doi.org/10.1111/ane.12262
Contents lists available at ScienceDirect
Archives of Gerontology and Geriatrics journal homepage: www.elsevier.com/locate/archger
Global cortical atrophy (GCA) associates with worse performance in the Montreal Cognitive Assessment (MoCA). A population-based study in community-dwelling elders living in rural Ecuador§ Oscar H. Del Brutto a,b,*, Robertino M. Mera c, Mauricio Zambrano d, Francisco Soriano d, Julio Lama e a
School of Medicine, Universidad Espı´ritu Santo – Ecuador, Guayaquil, Ecuador Department of Neurology, Hospital-Clı´nica Kennedy, Guayaquil, Ecuador Gastroenterology Department, Vanderbilt University, Nashville, TN, United States d Community Center, The Atahualpa Project, Atahualpa, Ecuador e Department of Imaging, Hospital-Clı´nica Kennedy, Guayaquil, Ecuador b c
A R T I C L E I N F O
A B S T R A C T
Article history: Received 10 July 2014 Received in revised form 18 September 2014 Accepted 21 September 2014 Available online 26 September 2014
Background/objective: Increasing numbers of individuals with cognitive impairment are posing economic threads to the developing world. Proper assessment of this condition may be complicated by illiteracy and cross-cultural factors. We conducted a population-based study in elders living in rural Ecuador to evaluate whether the MoCA associated with structural brain damage in less-educated populations. Methods: Atahualpa residents aged 60 years were identified during a door-to-door survey and invited to undergo MRI for grading GCA. Using a multivariate generalized linear model, we evaluated whether MoCA scores correlates with GCA, after adjusting for demographics, education, cardiovascular health (CVH) status, depression and edentulism. Results: Out of 311 eligible persons, 241 (78%) were enrolled. Mean age was 69.2 7.5 years, 141 (59%) were women, 199 (83%) had primary school education, 175 (73%) had poor CVH status, 30 (12%) had symptoms of depression and 104 (43%) had edentulism. Average MoCA scores were 18.5 4.7 points. GCA was mild in 108, moderate in 95, and severe in 26 persons. Total and most domain-specific MoCA scores were significantly worse in persons with moderate to severe GCA. In the multivariate model, mean MoCA score was associated with GCA severity (b = 2.38, SE = 1.07, p = 0.027). Conclusions: MoCA scores associate with severity of GCA after adjusting for potential confounders, and may be used as reliable estimates of structural brain damage. However, a lower cut-off than that recommended for developed countries, would be better for recognizing cognitive impairment in less educated populations. ß 2014 Elsevier Ireland Ltd. All rights reserved.
Keywords: Montreal cognitive assessment Global cortical atrophy Population-based study Atahualpa project Ecuador
1. Introduction The number of individuals with cognitive impairment is steadily increasing in the developing world (Llibre Rodriguez et al., 2008). This poses challenges and huge economic threads in regions where health resources are stretched to the limits. Accurate estimates of the burden of cognitive impairment are mandatory for public health planning in underserved populations.
§ Funding: This study was partially supported by Universidad Espı´ritu Santo – Ecuador, Guayaquil, Ecuador. * Corresponding author at: Air Center 3542, PO Box 522970, Miami, FL 331522970, United States. Tel.: +1 59342285790; fax: +1 59342280053. E-mail address: [email protected] (O.H. Del Brutto).
http://dx.doi.org/10.1016/j.archger.2014.09.010 0167-4943/ß 2014 Elsevier Ireland Ltd. All rights reserved.
Nevertheless, such assessment may be complicated by illiteracy and cross-cultural factors, which could make some of the most commonly used screening instruments non-reliable (Maestre, 2012). In this context, it has been suggested that the MoCA – a test created in developed countries – might overestimate the prevalence of cognitive impairment in subjects living in rural areas of developing countries (Go´mez, Zunzunegui, Lord, Alvarado, & Garcı´a, 2013). Lower cut-off scores or adjustments for regionspecific risk factors that may influence cognition have been proposed when using the MoCA in these populations. However, there has been no attempt to correlate cognitive performance with neuroimaging studies to evaluate whether – irrespective of cutoffs – MoCA scores actually reflect the severity of structural brain damage in less-well educated individuals. We conducted a
O.H. Del Brutto et al. / Archives of Gerontology and Geriatrics 60 (2015) 206–209
population-based study in community-dwelling elders living in rural Ecuador to correlate MoCA scores with severity of GCA as assessed by MRI.
2. Methods The protocol and the informed consent were approved by the I.R.B. of Hospital-Clı´nica Kennedy, Guayaquil, Ecuador (FWA 00006867). The Atahualpa project is a population-based cohort study designed to reduce the increasing burden of non-communicable diseases in rural Ecuador (Del Brutto, 2013). The village was selected because it is representative of the region. More than 95% of the population belong to the Native/Mestizo ethnic group (Amerindians) and their living characteristics have been detailed ˜ aherrera, et al., 2014). elsewhere (Del Brutto, Pen For this part of the Atahualpa project, trained rural doctors conducted a door-to-door survey to identify all Atahualpa residents aged 60 years. During the survey, we assessed the CVH status of all participants by the use of the seven metrics proposed by the American Heart Association, including smoking status, body mass index, physical activity, diet, blood pressure, fasting glucose, and total cholesterol blood levels; each metric was categorized as ideal, intermediate, and poor, and the CVH status
207
was classified as poor if at least one metric was in the poor range (Del Brutto et al., 2013). Participants were also evaluated with the depression axis of the Depression-Anxiety-Stress Scale-21 (DASS-21), a consistent field instrument that quantitatively measures dysphoria, hopelessness, devaluation of life, self-deprecation, lack of interest/involvement, anhedonia and inertia, with seven questions that are rated on a four-point Likert scale ranging from 0 (not at all) to 3 (almost always) with a maximum total score of 21, and a diagnosis of depression in persons who have 5 points (Osman et al., 2012). In addition, a rural dentist performed an oral exam with emphasis on the number of remaining teeth; individuals were classified in two groups according to whether they have severe edentulism – defined as those who have less than 10 remaining teeth – or not (Del Brutto, Gardener, et al., 2014). Cognitive performance was assessed using the Spanish version of the MoCA test (www.mocatest.org, ß Z. Nasreddine MD, version 07 November 2004). The MoCA evaluates major cognitive domains: visuospatial-executive (trail making B task, 3-dimentional cube copy, and clock drawing) for a maximum of 5 points; naming (unfamiliar animals) for a maximum of 3 points; language (sentence repetition, and a phonemic fluency task) for a maximum of 3 points; short-term memory (delayed recall or words) for a maximum of 5 points; abstraction (verbal abstraction) for a
Fig. 1. FLAIR MRIs (TR 9000, TE 120, TI 2500) showing severity of GCA according to Pasquier and co-workers. From left to right, columns represent absent, mild, moderate and severe global GCA respectively. In mild GCA there is sulcal opening peripherally (thick arrows). Moderate GCA is characterized by widening along the length of the sulci (arrowheads). Severe GCA is present when there is gyral thinning (thin arrows). Images correspond to four different persons aged 60 to 65 years.
208
O.H. Del Brutto et al. / Archives of Gerontology and Geriatrics 60 (2015) 206–209
maximum of 2 points; attention and calculation (digits forward and backward, target detection using tapping, serial 7’s subtraction) for a maximum of 6 points; and orientation (time and space) for a maximum of 6 points. Maximum MoCA score is 30 points, with an additional point given to persons with 12 years of education (Nasreddine et al., 2005). We did not used a cutoff score for defining cognitive impairment, but the continuous MoCA score to avoid problems related to poor reliability of specific cutoffs. Persons who signed the informed consent and had no contraindications for the practice of MRI were moved to Guayaquil. All studies were performed with a Philips Intera 1.5 T (Philips Medical Systems, the Netherlands) at Hospital-Clı´nica Kennedy. MRI included two-dimensional multi-slice turbo spin echo T1-weighted, fluid attenuated inversion recovery (FLAIR), T2-weighted, and gradient-echo sequences in the axial plane, as well as a T1weighted sequence oriented in the sagittal plane. We used the preestablished brain imaging package delivered by the manufacturer to homogenize applicability by technicians; slice thickness was 5 mm with 1 mm gap between slices. A neurologist (OHD) and a neuroradiologist (JL) independently read all MRIs, blinded to clinical data. Primary interest was focused on the presence of GCA, using the visual scale proposed by Pasquier et al. (1996) (Fig. 1). Kappa coefficients for inter-rater agreement (n = 258) were 0.76 for severity of GCA, and disagreements were resolved by consensus. All analyses were carried out by using STATA version 13 (College Station, TX, USA). Descriptive statistics are presented as means standard deviations for continuous variables and as percentages with 95% C.I. for categorical variables. A p value of less than 0.05 is considered significant. Using a multivariate generalized linear model, we examined the association between GCA and MoCA score, after adjusting for demographics, education, CVH status, edentulism and depression.
3. Results The door-to-door survey identified 311 Atahualpa residents aged 60 years, 258 (83%) of whom underwent a brain MRI. Reasons for not obtaining MRI included refusal to participate (n = 26), severe disability (n = 11), claustrophobia (n = 8), and implanted pacemaker (n = 1); seven additional persons had died or emigrated between the survey and the invitation. Seventeen of the
258 persons who had an MRI could not perform the MoCA due to aphasia or severe visual or hearing impairment. Therefore, the present study included 241 persons. Mean age was 69.2 7.5 years, 141 (59%) were women and 199 (83%) had primary school education only. A poor CVH status was noticed in 175 (73%) persons and the mean SD number of poor metrics per person was 1.2 1. Thirty persons (12%) had symptoms of depression and 104 (43%) had severe edentulism. Mean scores in the MoCA were 18.5 4.7 points. A total of 229 persons (95%) had GCA, which was mild in 108, moderate in 95, and severe in 26. As only 12 persons had no GCA, they were grouped with those with mild GCA for analysis. Univariate analysis showed that persons with moderate to severe GCA were older, less educated and more often edentulous than those with none-mild GCA (Table 1). In addition, total and domain-specific MoCA scores (with the exception of abstraction) were significantly worse in persons with moderate to severe GCA (Table 2). In the multivariate generalized linear model, mean MoCA score was significantly associated with GCA severity, after adjusting for demographics, education, CVH status, depression and edentulism (b = 2.38, SE 1.07, p = 0.027). The contrast between none-mild and severe GCA represented a 12.8% (95% C.I.: 2–23%) change in the MoCA score.
4. Discussion Results of the present study show that MoCA scores associate with severity of GCA after adjusting for a number of confounders, and suggest that this field instrument may be used as an estimate of structural brain damage in less educated elders. The MoCA is a widely used screening instrument that assesses multiple cognitive domains anatomically linked to different cortical areas (Julayanont, Phillips, Chertkow, & Nasreddine, 2013 Chap. 6). However, volumetric MRI studies attempting to correlate MoCA scores with cortical abnormalities have been inconclusive (Paul et al., 2011). More attention has been given to worse performance in the MoCA scores associated with white matter lesions, but it has recently been demonstrated that cognitive impairment associated with white matter lesions is mediated by cortical atrophy (Zi, Duan, & Zheng, 2014). Studies conducted in Western populations suggested a MoCA cut-off score 25 to separate normal subjects from those with mild cognitive impairment (Nasreddine et al., 2005). Asian and Latin
Table 1 Characteristics of community-dwelling elders living in Atahualpa according to the severity of GCA.
Age, mean SD years Women, n (%) Up to primary school, n (%) Poor CVH status, n (%) Symptoms of depression, n (%) Severe edentulism, n (%)
Total series n = 241
None-mild GCA n = 120
Moderate GCA n = 95
Severe GCA n = 26
Significance
69.2 7.5 141 (59%) 199 (83%) 175 (73%) 30 (12%) 104 (43%)
64.8 3.5 70 (58%) 90 (75%) 84 (70%) 14 (12%) 41 (34%)
72.1 7.3 53 (56%) 86 (91%) 68 (72%) 13 (14%) 49 (52%)
79.2 7.5 18 (69%) 23 (88%) 23 (88%) 3 (12%) 14 (54%)
0.0001 0.468 0.008 0.153 0.726 0.019
Table 2 Mean SD total and domain-specific MoCA scores in community-dwelling elders living in Atahualpa according to the severity of GCA.
Total MoCA score, max 30 pts Visuospatial-executive, max 5 pts Animal naming, max 3 pts Language, max 3 pts Short-term memory, max 5 pts Abstraction, max 2 pts Attention and calculation, max 6 pts Orientation, max 6 pts
Total series n = 241
None-mild GCA n = 120
Moderate to severe GCA n = 121
Significance (p)
18.49 4.68 2.82 1.08 1.73 1.00 1.14 0.92 1.50 1.49 1.77 0.53 3.31 1.76 5.26 0.96
20.33 3.90 3.02 1.05 1.88 0.93 1.40 0.97 1.98 1.39 1.78 0.54 3.85 1.49 5.45 0.72
16.68 4.68 2.62 1.07 1.58 1.04 0.88 0.79 1.03 1.43 1.75 0.52 2.77 1.84 5.07 1.11
0.0001 0.004 0.019 0.0001 0.0001 0.661 0.0001 0.002
O.H. Del Brutto et al. / Archives of Gerontology and Geriatrics 60 (2015) 206–209
American studies recommended lowering the original cut-off score for diagnosing mild cognitive impairment in less-educated populations; however, these studies have not been based on neuroimaging correlation of cognitive performance in the MoCA, but on comparisons with results obtained in other neuropsychological tests (Go´mez et al., 2013; Lee et al., 2008). In the present study, persons with none or mild GCA have a mean MoCA score of 20 points (Table 2), suggesting that this is probably a better cut-off value for defining mild cognitive impairment in less-educated populations. Our results concur with a recent Indian study, where 48% of patients with mild cognitive impairment and abnormal neuroimaging had diffuse cortical atrophy on CT or MRI (Alladi et al., 2014). We did not use volumetric assessment of cortical gray matter but relied on a visual rating scale, and this is a limitation of the present study. However, the population-based design together with the homogeneous characteristics of Atahualpa’s residents and the model used for assessing the association between GCA and cognitive performance, argues for the strength of our results. A complete battery of neuropsychological tests for diagnosing cognitive impairment may be unfeasible in population-based studies conducted in rural villages of developing countries, and the MoCA appears to be a simple and reliable option to assess cognition in these underserved populations. Conflict of interest The authors have nothing to disclose. References Alladi, S., Shailaja, M., Mridula, K. R., Haritha, C. A., Kavitha, N., Khan, S. A., et al. (2014). Mild cognitive impairment: Clinical and imaging profile in a memory clinic setting in India. Dementia and Geriatric Cognitive Disorders, 37(1–2), 113–124. Del Brutto, O. H. (2013). Implications and expectancies of the Atahualpa project: A population-based survey designed to reduce the burden of stroke and cardiovascular diseases in rural Ecuador. Journal of Neurosciences in Rural Practice, 4(3), 363–365.
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