The Global Deterioration Scale for Down Syndrome Population (GDS-DS): A Rating Scale to Assess the Progression of Alzheimer’s Disease
Abstract
:1. Introduction
2. Materials and Methods
2.1. Study Design and Description of the Sample
2.2. Clinical Assessment
2.2.1. Cognitive Assessment
- The KBIT-II is a test designed for the measurement of verbal and non-verbal intelligence. It consists of two sub-tests that assess crystallized intelligence and fluid intelligence and allow the establishment of the level of ID.
- The Vineland II scale measures adaptive behaviors, including communication, daily living skills, socialization, and motor skills.
- The CAMCOG-DS comprises seven cognitive domains (orientation, language, memory, attention, praxis, abstract thinking, and perception). The maximum score is 109 points. The psychometrical properties are good: test–retest reliability = 0.92, ICC = 0.91, internal consistency = 0.70 − 0.93, and κ values of 0.95 and 0.97 versus DSM-IV [51] and ICD-10 [55] criteria, respectively. It is a reliable tool for the assessment of cognitive impairment in people with ID with and without DS with mild and moderate levels of ID.
- The BT-ID consists of 67 subtests grouped into eight cognitive domains (language, working memory, orientation, praxis, attention, executive function, visuoconstruction, and memory). It shows good psychometric properties: test–retest reliability = 0.91, ICC = 0.95, internal consistency = 0.70 − 0.93. It provides normative data for five groups based on intellectual disability level, age, and curricular competence.
- Planning and problem solving were assessed with the Tower of London—Drexel University: 2nd edition ID version [56]. Its psychometric properties are reliable for differentiation between subjects with mild and moderate ID, and are associated with other measures of executive functions. Additionally, it demonstrated sufficient evidence of reliability and validity in adults with Down syndrome.
2.2.2. Informants’ Questionnaires
- The behavior rating inventory of executive function, parents’ form (BRIEF-P) [30] measures executive functions or self-regulation in their everyday environments. It consists of two indexes: (1) Behavioral regulation index (BRI), composed of inhibit, shift, and emotional control scales; and (2) the metacognitive index (MI), composed of initiate, working memory, planning, organization, and monitor scales.
- The informant interview of the Cambridge examination for older adults with Down’s syndrome and other intellectual disabilities—Spanish version (CAMDEX-DS) [32]. It consists of (1) a structured interview with the informant/family member to collect information to detect a decline in the individual’s best level of functioning, their cognitive and functional impairment, and the mental and physical health of the participant, including depression, anxiety, paranoid symptoms, delirium, substance abuse, physical disability, hypothyroidism, cerebrovascular problems, and pharmacological treatment; (2) the CAMCOG-DS (see the cognitive test scale section in this article); (3) a guide for the clinical diagnosis of AD, capturing changes in daily adaptive skills (section A), memory (section B), other cognitive domains (section C1), personality/behavior (section C2) and confusional acute syndrome (section D); and (4) suggestions for the correct intervention in people with ID and dementia. In this study, the CAMDEX-DS was used only for clinical diagnostic purposes to avoid the risk of circularity.
2.2.3. Global Deterioration Scale for Down Syndrome (GDS-DS)
- GDS-DS adaptation
- Mandatory criteria
- Behavioral Regulation Index—BRIEF-P [30]. This questionnaire demonstrates that, in people with DS, a cut-off point of ≥ 55 allows the classification of stable subjects at the cognitive and behavioral levels (sensitivity = 90), while a cut-off point of <32 allows the classification of subjects with MCI (specificity = 0.90). For scores between 32 and 55, the diagnosis is more doubtful [28]. According to these data, the following cut-off points were assigned for our study: ≥33 would be a criterion for cognitive and behavioral stability (stage 1) and subjective cognitive and/or behavioral impairment (stage 2), and ≤32 would be a criterion for mild cognitive or behavioral impairment (stage 3) and mild, moderate and advanced AD (stages 4, 5 and 6, respectively).
- Regarding the total score of the CAMCOG-DS [32], it has become clear that a cut-off point of the total score = 68 allows the detection of AD in subjects with DS and mild ID (sensitivity: 80%; specificity: 81%), and a cut-off point of 52 (sensitivity: 85%; specificity: 81%) in those with moderate ID [32]. Additionally, in another study of subjects with DS and mild ID, a cut-off point of 82 (sensitivity: 80%, specificity 80.5%) differentiated between asymptomatic and prodromal AD, and a cut-off point of 80 (sensitivity: 75%, specificity 87.8%) differentiated asymptomatic and dementia AD. In the same study, for those with moderate ID, a cut-off point of 64 (sensitivity: 66.7%, specificity 72.3%) differentiated between asymptomatic and prodromal AD, and a cut-off point of 56 (sensitivity: 84%, specificity 84.3%) between asymptomatic and dementia AD [13]. The data of these two previous studies were incorporated for all the stages of the GDS-DS, according to the ID level and the CAMCOG-DS total score.
- The Guide to clinical diagnosis of the CAMDEX-DS—Spanish version [32]. The decline of daily life skills is decisive in the diagnostic process of AD, since in the MCI, these are preserved or only very mildly affected. Therefore, in our study, positive scores in sections B (memory), section C1 (other cognitive domains) or section C2 (personality/behavioral) were considered indicative of mild cognitive and/or behavioral impairment (stage 3). Furthermore, positive scores in section A (daily living skills), section B and sections C1 or C2 and negative scores in section D (acute confusional syndrome) are indicative of AD (stages 4, 5 and 6).
- Supporting criteria
- BT-ID: the orientation, semantic fluency (eating and drinking), formal fluency, delay verbal memory (stories) and visual discrimination subtests.
- CAMCOG-DS: abstract thinking subtest.
2.3. Procedures
2.4. Statistical Analysis
3. Results
3.1. Sample and Demographics
3.2. Cognitive and Behavioral Data across the GDS-DS Stages
- Delay stories (BT-ID) between stage 2 (subjective cognitive and/or behavioral impairment) and 5 (moderate Alzheimer’s disease) and stages 3 (mild cognitive and/or behavioral impairment) and 5 (moderate Alzheimer’s disease).
- Formal fluency (TB-ID) between stage 1 (cognitive and/or behavioral stability) and 5 (moderate Alzheimer’s disease), stage 2 (subjective cognitive and/or behavioral impairment), stage 3 (mild Alzheimer’s disease) and stage 4 (moderate Alzheimer’s disease).
- Semantic fluency (BT-ID) between stages 2 (subjective cognitive and/or behavioral impairment) and 5 (moderate Alzheimer’s disease).
3.3. Reliability
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Englund, A.; Jonsson, B.; Zander, C.S.; Gustafsson, J.; Annerén, G. Changes in Mortality and Causes of Death in the Swedish Down Syndrome Population. Am. J. Med. Genet. Part A 2013, 161, 642–649. [Google Scholar] [CrossRef] [PubMed]
- Zeilinger, E.L.; Gärtner, C.; Janicki, M.P.; Esralew, L.; Weber, G. Practical Applications of the NTG-EDSD for Screening Adults with Intellectual Disability for Dementia: A German-Language Version Feasibility Study. J. Intellect. Dev. Disabil. 2016, 41, 42–49. [Google Scholar] [CrossRef]
- Tosh, J.L.; Rhymes, E.R.; Mumford, P.; Whittaker, H.T.; Pulford, L.J.; Noy, S.J.; Cleverley, K.; Strydom, A.; Fisher, E.; Wiseman, F.; et al. Genetic Dissection of down Syndrome-Associated Alterations in APP/Amyloid-β Biology Using Mouse Models. Sci. Rep. 2021, 11, 5736. [Google Scholar] [CrossRef] [PubMed]
- Wiseman, F.K.; Pulford, L.J.; Barkus, C.; Liao, F.; Portelius, E.; Webb, R.; Chávez-Gutiérrez, L.; Cleverley, K.; Noy, S.; Sheppard, O.; et al. Trisomy of Human Chromosome 21 Enhances Amyloid-b Deposition Independently of an Extra Copy of APP. Brain 2018, 141, 2457–2474. [Google Scholar] [CrossRef] [Green Version]
- Hithersay, R.; Startin, C.M.; Hamburg, S.; Mok, K.Y.; Hardy, J.; Fisher, E.M.C.C.; Tybulewicz, V.L.J.; Nizetic, D.; Strydom, A.; Mok, K.Y.; et al. Association of Dementia with Mortality among Adults with Down Syndrome Older Than 35 Years. JAMA Neurol. 2019, 76, 152–160. [Google Scholar] [CrossRef] [PubMed]
- Jack, C.R.; Bennett, D.A.; Blennow, K.; Carrillo, M.C.; Dunn, B.; Haeberlein, S.B.; Holtzman, D.M.; Jagust, W.; Jessen, F.; Karlawish, J.; et al. NIA-AA Research Framework: Toward a Biological Definition of Alzheimer’s Disease. Alzheimers Dement. 2018, 14, 535–562. [Google Scholar] [CrossRef]
- Head, E.; Lott, I.T.; Wilcock, D.M.; Lemere, C.A. Aging in Down Syndrome and the Development of Alzheimer’s Disease Neuropathology. Curr. Alzheimer Res. 2015, 13, 18–29. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hithersay, R.; Baksh, R.A.; Startin, C.M.; Wijeratne, P.; Hamburg, S.; Carter, B.; Strydom, A.; Strydom, A.; Fisher, E.; Nizetic, D.; et al. Optimal Age and Outcome Measures for Alzheimer’s Disease Prevention Trials in People with Down Syndrome. Alzheimers Dement. 2021, 17, 595–604. [Google Scholar] [CrossRef]
- Sinai, A.; Mokrysz, C.; Bernal, J.; Bohnen, I.; Bonell, S.; Courtenay, K.; Dodd, K.; Gazizova, D.; Hassiotis, A.; Hillier, R.; et al. Predictors of Age of Diagnosis and Survival of Alzheimer’s Disease in Down Syndrome. J. Alzheimers Dis. 2018, 61, 717–728. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Firth, N.C.; Startin, C.M.; Hithersay, R.; Hamburg, S.; Wijeratne, P.A.; Mok, K.Y.; Hardy, J.; Alexander, D.C.; Strydom, A. Aging Related Cognitive Changes Associated with Alzheimer’s Disease in Down Syndrome. Ann. Clin. Transl. Neurol. 2018, 5, 741–751. [Google Scholar] [CrossRef] [Green Version]
- Strydom, A.; Coppus, A.; Blesa, R.; Danek, A.; Fortea, J.; Hardy, J.; Levin, J.; Nuebling, G.; Rebillat, A.; Ritchie, C.; et al. Alzheimer’s Disease in Down Syndrome: An Overlooked Population for Prevention Trials. Alzheimers Dement. Transl. Res. Clin. Interv. 2018, 4, 703–713. [Google Scholar] [CrossRef] [PubMed]
- Lott, I.T.; Head, E. Dementia in Down Syndrome: Unique Insights for Alzheimer Disease Research. Nat. Rev. Neurol. 2019, 15, 135–147. [Google Scholar] [CrossRef]
- Benejam, B.; Videla, L.; Vilaplana, E.; Barroeta, I.; Carmona-Iragui, M.; Altuna, M.; Valldeneu, S.; Fernandez, S.; Giménez, S.; Iulita, F.; et al. Diagnosis of Prodromal and Alzheimer’s Disease Dementia in Adults with Down Syndrome Using Neuropsychological Tests. Alzheimers Dement. Diagnosis, Assess. Dis. Monit. 2020, 12, e12047. [Google Scholar] [CrossRef]
- Startin, C.M.; D’Souza, H.; Ball, G.; Hamburg, S.; Hithersay, R.; Hughes, K.M.O.; Massand, E.; Karmiloff-Smith, A.; Thomas, M.S.C.; Strydom, A.; et al. Health Comorbidities and Cognitive Abilities across the Lifespan in down Syndrome. J. Neurodev. Disord. 2020, 12, 4. [Google Scholar] [CrossRef] [PubMed]
- Rafii, M.S.; Ances, B.M.; Schupf, N.; Krinsky-McHale, S.J.; Mapstone, M.; Silverman, W.; Lott, I.; Klunk, W.; Head, E.; Christian, B.; et al. The AT(N) Framework for Alzheimer’s Disease in Adults with Down Syndrome. Alzheimers Dement. Diagnosis, Assess. Dis. Monit. 2020, 12, e12062. [Google Scholar] [CrossRef]
- Jessen, F.; Kleineidam, L.; Wolfsgruber, S.; Bickel, H.; Brettschneider, C.; Fuchs, A.; Kaduszkiewicz, H.; König, H.H.; Mallon, T.; Mamone, S.; et al. Prediction of Dementia of Alzheimer Type by Different Types of Subjective Cognitive Decline. Alzheimers Dement. 2020, 16, 1745–1749. [Google Scholar] [CrossRef]
- Rostamzadeh, A.; Bohr, L.; Wagner, M.; Baethge, C.; Jessen, F. Progression of Subjective Cognitive Decline to MCI or Dementia in Relation to Biomarkers for Alzheimer Disease: A Meta-Analysis. Neurology 2022, 99, e1866–e1874. [Google Scholar] [CrossRef] [PubMed]
- Dubois, B.; Villain, N.; Frisoni, G.B.; Rabinovici, G.D.; Sabbagh, M.; Cappa, S.; Bejanin, A.; Bombois, S.; Epelbaum, S.; Teichmann, M.; et al. Clinical Diagnosis of Alzheimer’s Disease: Recommendations of the International Working Group. Lancet Neurol. 2021, 20, 484–496. [Google Scholar] [CrossRef] [PubMed]
- Ismail, Z.; Smith, E.E.; Geda, Y.; Sultzer, D.; Brodaty, H.; Smith, G.; Agüera-Ortiz, L.; Sweet, R.; Miller, D.; Lyketsos, C.G. Neuropsychiatric Symptoms as Early Manifestations of Emergent Dementia: Provisional Diagnostic Criteria for Mild Behavioral Impairment. Alzheimers Dement. 2016, 12, 195–202. [Google Scholar] [CrossRef] [PubMed]
- Jiang, F.; Cheng, C.; Huang, J.; Chen, Q.; Le, W. Mild Behavioral Impairment: An Early Sign and Predictor of Alzheimer’s Disease Dementia. Curr. Alzheimer Res. 2022, 19, 407–419. [Google Scholar] [CrossRef]
- de Oliveira, L.C.; de Paula Faria, D. Pharmacological Approaches to the Treatment of Dementia in Down Syndrome: A Systematic Review of Randomized Clinical Studies. Molecules 2022, 27, 3244. [Google Scholar] [CrossRef] [PubMed]
- Videla, L.; Benejam, B.; Pegueroles, J.; Carmona-Iragui, M.; Padilla, C.; Fernández, S.; Barroeta, I.; Altuna, M.; Valldeneu, S.; Garzón, D.; et al. Longitudinal Clinical and Cognitive Changes Along the Alzheimer Disease Continuum in Down Syndrome + Supplemental Content. JAMA Netw. Open 2022, 5, 2225573. [Google Scholar] [CrossRef]
- Rösner, P.; Berger, J.; Tarasova, D.; Birkner, J.; Kaiser, H.; Diefenbacher, A.; Sappok, T. Assessment of Dementia in a Clinical Sample of Persons with Intellectual Disability. J. Appl. Res. Intellect. Disabil. 2021, 34, 1618–1629. [Google Scholar] [CrossRef]
- Benejam, B.; Aranha, M.R.; Videla, L.; Padilla, C.; Valldeneu, S.; Fernández, S.; Altuna, M.; Carmona-Iragui, M.; Barroeta, I.; Iulita, M.F.; et al. Neural Correlates of Episodic Memory in Adults with Down Syndrome and Alzheimer’s Disease. Alzheimers. Res. Ther. 2022, 14, 123. [Google Scholar] [CrossRef]
- Fonseca, L.M.; Padilla, C.; Jones, E.; Neale, N.; Haddad, G.G.; Mattar, G.P.; Barros, E.; Clare, I.C.H.; Busatto, G.F.; Bottino, C.M.C.; et al. Amnestic and Non-Amnestic Symptoms of Dementia: An International Study of Alzheimer’s Disease in People with Down’s Syndrome. Int. J. Geriatr. Psychiatry 2020, 35, 650–661. [Google Scholar] [CrossRef]
- García-Alba, J.; Ramírez-Toraño, F.; Esteba-Castillo, S.; Bruña, R.; Moldenhauer, F.; Novell, R.; Romero-Medina, V.; Maestú, F.; Fernández, A. Neuropsychological and Neurophysiological Characterization of Mild Cognitive Impairment and Alzheimer’s Disease in Down Syndrome. Neurobiol. Aging 2019, 84, 70–79. [Google Scholar] [CrossRef]
- Startin, C.M.; Hamburg, S.; Hithersay, R.; Al-Janabi, T.; Mok, K.Y.; Hardy, J.; Strydom, A.; Fisher, E.; Nizetic, D.; Tybulewicz, V.; et al. Cognitive Markers of Preclinical and Prodromal Alzheimer’s Disease in Down Syndrome. Alzheimers Dement. 2019, 15, 245–257. [Google Scholar] [CrossRef]
- Esteba-Castillo, S.; Garcia-Alba, J.; Rodríguez-Hildago, E.; Vaquero, L.; Novell, R.; Moldenhauer, F.; Castellanos, M.Á. Proposed Diagnostic Criteria for Mild Cognitive Impairment in Down Syndrome Population. J. Appl. Res. Intellect. Disabil. 2022, 35, 495–505. [Google Scholar] [CrossRef]
- Dubois, B.; Feldman, H.H.; Jacova, C.; Hampel, H.; Molinuevo, J.L.; Blennow, K.; DeKosky, S.T.; Gauthier, S.; Selkoe, D.; Bateman, R.; et al. Advancing Research Diagnostic Criteria for Alzheimer’s Disease: The IWG-2 Criteria. Lancet Neurol. 2014, 13, 614–629. [Google Scholar] [CrossRef]
- Gioia, G.A.; Isquith, P.K.; Guy, S.C.; Kenworthy, L.; Baron, I.S. Behavior Rating Inventory of Executive Function. Child Neuropsychol. 2000, 6, 235–238. [Google Scholar] [CrossRef]
- Silverman, W.; Krinsky-McHale, S.J.; Lai, F.; Diana Rosas, H.; Hom, C.; Doran, E.; Pulsifer, M.; Lott, I.; Schupf, N.; Andrews, H.; et al. Evaluation of the National Task Group-Early Detection Screen for Dementia: Sensitivity to ‘Mild Cognitive Impairment’ in Adults with Down Syndrome. J. Appl. Res. Intellect. Disabil. 2021, 34, 905–915. [Google Scholar] [CrossRef]
- Esteba-castillo, S.; Dalmau-bueno, A.; Ribas-vidal, N.; Vilà-alsina, M.; Novell-alsina, R.; García-alba, J. Adaptación y Validación Del Cambridge Examination for Mental Disorders of Older People with Down’s Syndrome and Others with Intellectual Disabilities (CAMDEX-DS) En Población Española Con Discapacidad Intelectual. Rev. Neurol. 2013, 57, 337–346. [Google Scholar] [CrossRef]
- Krinsky-McHale, S.J.; Hartley, S.; Hom, C.; Pulsifer, M.; Clare, I.C.H.; Handen, B.L.; Lott, I.T.; Schupf, N.; Silverman, W. A Modified Cued Recall Test for Detecting Prodromal AD in Adults with Down Syndrome. Alzheimers Dement. Diagn. Assess. Dis. Monit. 2022, 14, e12361. [Google Scholar] [CrossRef]
- Robert, P.; Ferris, S.; Gauthier, S.; Ihl, R.; Winblad, B.; Tennigkeit, F. Review of Alzheimer’s Disease Scales: Is There a Need for a New Multi-Domain Scale for Therapy Evaluation in Medical Practice? Alzheimers. Res. Ther. 2010, 2, 24. [Google Scholar] [CrossRef] [Green Version]
- Morris, J.C. The Clinical Dementia Rating (CDR). Neurology 1993, 43, 2412.2-a. [Google Scholar] [CrossRef]
- Knopman, D.S.; Kramer, J.H.; Boeve, B.F.; Caselli, R.J.; Graff-Radford, N.R.; Mendez, M.F.; Miller, B.L.; Mercaldo, N. Development of Methodology for Conducting Clinical Trials in Frontotemporal Lobar Degeneration. Brain 2008, 131, 2957–2968. [Google Scholar] [CrossRef] [Green Version]
- Mioshi, E.; Flanagan, E.; Knopman, D. Detecting Clinical Change with the CDR-FTLD: Differences between FTLD and AD Dementia. Int. J. Geriatr. Psychiatry 2017, 32, 977–982. [Google Scholar] [CrossRef] [Green Version]
- Lessov-Schlaggar, C.N.; Del Rosario, O.L.; Morris, J.C.; Ances, B.M.; Schlaggar, B.L.; Constantino, J.N. Adaptation of the Clinical Dementia Rating Scale for Adults with down Syndrome. J. Neurodev. Disord. 2019, 11, 39. [Google Scholar] [CrossRef] [Green Version]
- Reisberg, B.; Ferris, S.H.; de León, M.J.; Crook, T. The Global Deterioration Scale for Assessment of Primary Degenerative Dementia. Am. J. Psychiatry 1982, 139, 1136–1139. [Google Scholar] [CrossRef] [Green Version]
- Reisberg, B. Functional Assessment Staging (FAST). Psychopharmacol. Bull. 1988, 24, 653–659. [Google Scholar]
- Sabbagh, M.N.; Cooper, K.; DeLange, J.; Stoehr, J.D.; Thind, K.; Lahti, T.; Reisberg, B.; Sue, L.; Vedders, L.; Fleming, S.R.; et al. Functional, Global and Cognitive Decline Correlates to Accumulation of Alzheimers Pathology in MCI and AD. Curr. Alzheimer Res. 2010, 7, 280–286. [Google Scholar] [CrossRef] [PubMed]
- Bobinski, M.; Wegiel, J.; Wisniewski, H.M.; Tarnawski, M.; Mlodzik, B.; Reisberg, B.; de Leon, M.J.; Miller, D.C. Atrophy of Hippocampal Formation Subdivisions Correlates with Stage and Duration of Alzheimer Disease. Dement. Geriatr. Cogn. Disord. 1995, 6, 205–210. [Google Scholar] [CrossRef]
- Bello López, J.; Piñol Ripoll, G.; Lleó Bisa, A.; Lladó Plarrumaní, A. Protocol de Diagnòstic i Tractament de La Malaltia d’Alzheimer. Available online: https://www.scneurologia.cat/wp-content/uploads/2019/01/Actualitzaci%C3%B3-Guia-M%C3%A8dica-d%E2%80%99Alzheimer-de-la-Societat-Catalana-de-Neurologia-%E2%80%93-2015.pdf (accessed on 26 December 2022).
- Lladó Plarrumaní, A.; Santaeugènia González, S.J.; Melendo Azuela, E.M. Pla d’atenció Sanitària a Les Persones Amb Deteriorament Cognitiu Lleu i Demència de Catalunya (PLADEMCAT). Available online: https://salutweb.gencat.cat/web/.content/_departament/ambits-estrategics/atencio-sociosanitaria/docs/plademcat/plademcat-model-asistencial.pdf (accessed on 26 December 2022).
- Benejam, B.; Fortea, J.; Molina-López, R.; Videla, S. Patterns of Performance on the Modified Cued Recall Test in Spanish Adults with down Syndrome with and without Dementia. Am. J. Intellect. Dev. Disabil. 2015, 120, 481–489. [Google Scholar] [CrossRef] [PubMed]
- Krinsky-McHale, S.J.; Devenny, D.A.; Silverman, W. Changes in Explicit Memory Associated with Early Dementia in Adults with Down’s Syndrome. J. Intellect. Disabil. Res. 2002, 46, 198–208. [Google Scholar] [CrossRef]
- Ball, S.L.; Holland, A.J.; Treppner, P.; Watson, P.C.; Huppert, F.A. Executive Dysfunction and Its Association with Personality and Behaviour Changes in the Development of Alzheimer’s Disease in Adults with Down Syndrome and Mild to Moderate Learning Disabilities. Br. J. Clin. Psychol. 2008, 47, 1–29. [Google Scholar] [CrossRef]
- Janicki, M.P.; McCallion, P.; Splaine, M.; Santos, F.H.; Keller, S.M.; Watchman, K. Consensus Statement of the International Summit on Intellectual Disability and Dementia Related to Nomenclature. Intellect. Dev. Disabil. 2017, 55, 338–346. [Google Scholar] [CrossRef] [Green Version]
- Moss, S.; Ibbotson, B.; Prosser, H.; Goldberg, D.; Patel, P.; Simpson, N. Validity of the PAS-ADD for Detecting Psychiatric Symptoms in Adults with Learning Disability (Mental Retardation). Soc. Psychiatry Psychiatr. Epidemiol. 1997, 32, 344–354. [Google Scholar] [CrossRef]
- Rubenstein, E.; Hartley, S.; Bishop, L. Epidemiology of Dementia and Alzheimer Disease in Individuals with Down Syndrome. JAMA Neurol. 2020, 77, 262–264. [Google Scholar] [CrossRef]
- Association, A.P. Diagnostic and Statistical Manual of Mental Disorders, 5th ed.; American Psychiatric Publishing: Washington, DC, USA, 2013; ISBN 978-08-9042-555-8. [Google Scholar]
- Kaufman, A.; Nadeen, L.; Kaufman, L. Kaufman Brief Intelligence Test, 2nd ed.; Pearson, Inc.: Minneapolis, MN, USA, 2004. [Google Scholar]
- Sparrow, S.; Cicchetti, D.; Balla, D. Vineland Adaptive Behavior Scales-2nd Edition Manual, 2nd ed.; NCS, P., Ed.; Pearson, Inc.: Minneapolis, MN, USA, 2005. [Google Scholar]
- Esteba-Castillo, S.; Peña-Casanova, J.; García-Alba, J.; Castellanos, M.A.; Torrents-Rodas, D.; Rodríguez, E.; Deus-Yela, J.; Caixàs, A.; Novell-Alsina, R. Test Barcelona Para Discapacidad Intelectual: Un Nuevo Instrumento Para La Valoración Neuropsicológica Clínica de Adultos Con Discapacidad Intelectual. Rev. Neurol. 2017, 64, 433–444. [Google Scholar] [CrossRef]
- Organization(WHO), W.H. The ICD-10 Classification of Mental and Behavioural Disorders; World Health Organization: Genève, Switzerland, 1993; ISBN 9789241544559. [Google Scholar]
- García-Alba, J.; Esteba-Castillo, S.; López, M.Á.C.; Hidalgo, E.R.; Vidal, N.R.; Díaz, F.M.; Novell-Alsina, R. Validation and Normalization of the Tower of London-Drexel University Test 2nd Edition in an Adult Population with Intellectual Disability. Span. J. Psychol. 2017, 20, E32. [Google Scholar] [CrossRef]
- Krinsky-McHale, S.J.; Zigman, W.B.; Lee, J.H.; Schupf, N.; Pang, D.; Listwan, T.; Kovacs, C.; Silverman, W. Promising Outcome Measures of Early Alzheimer’s Dementia in Adults with Down Syndrome. Alzheimers Dement. Diagn. Assess. Dis. Monit. 2020, 12, e12044. [Google Scholar] [CrossRef]
- Fenoll, R.; Pujol, J.; Esteba-Castillo, S.; De Sola, S.; Ribas-Vidal, N.; García-Alba, J.; Sánchez-Benavides, G.; Martínez-Vilavella, G.; Deus, J.; Dierssen, M.; et al. Anomalous White Matter Structure and the Effect of Age in Down Syndrome Patients. J. Alzheimers Dis. 2017, 57, 61–70. [Google Scholar] [CrossRef] [PubMed]
- Krinsky-McHale, S.J.; Silverman, W. Dementia and Mild Cognitive Impairment in Adults with Intellectual Disability: Issues of Diagnosis. Dev. Disabil. Res. Rev. 2013, 18, 31–42. [Google Scholar] [CrossRef]
- Pujol, J.; Fenoll, R.; Ribas-Vidal, N.; Martínez-Vilavella, G.; Blanco-Hinojo, L.; García-Alba, J.; Deus, J.; Novell, R.; Esteba-Castillo, S. A Longitudinal Study of Brain Anatomy Changes Preceding Dementia in Down Syndrome. NeuroImage Clin. 2018, 18, 160–166. [Google Scholar] [CrossRef] [PubMed]
- Sheehan, R.; Sinai, A.; Bass, N.; Blatchford, P.; Bohnen, I.; Courtenay, K.; Hassiotis, A.; Markar, T.; Mccarthy, J. Dementia Diagnostic Criteria in Down Syndrome. Int. J. Geriatr. Psychiatry 2015, 30, 857–863. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ramírez-Toraño, F.; García-Alba, J.; Bruña, R.; Esteba-Castillo, S.; Vaquero, L.; Pereda, E.; Maestú, F.; Fernández, A. Hypersynchronized Magnetoencephalography Brain Networks in Patients with Mild Cognitive Impairment and Alzheimer’s Disease in down Syndrome. Brain Connect. 2021, 11, 725–733. [Google Scholar] [CrossRef]
- Grissom, R.J. Probability of the Superior Outcome of One Treatment over Another. J. Appl. Psychol. 1994, 79, 314–316. [Google Scholar] [CrossRef]
- Elliott-King, J.; Shaw, S.; Bandelow, S.; Devshi, R.; Kassam, S.; Hogervorst, E. A Critical Literature Review of the Effectiveness of Various Instruments in the Diagnosis of Dementia in Adults with Intellectual Disabilities. Alzheimers Dement. Diagnosis, Assess. Dis. Monit. 2016, 4, 126–148. [Google Scholar] [CrossRef] [Green Version]
- Dekker, A.D.; Wissing, M.B.G.; Ulgiati, A.M.; Bijl, B.; van Gool, G.; Groen, M.R.; Grootendorst, E.S.; van der Wal, I.A.; Hobbelen, J.S.M.; De Deyn, P.P.; et al. Dementia in People with Severe or Profound Intellectual (and Multiple) Disabilities: Focus Group Research into Relevance, Symptoms and Training Needs. J. Appl. Res. Intellect. Disabil. 2021, 34, 1602–1617. [Google Scholar] [CrossRef]
- Devinsky, O.; D’Esposito, M. Neurology of Cognitive and Behavioral Disorders: Sistema de Descoberta Para FCCN. Available online: https://vpn4.ulusofona.pt:10443/proxy/059de34c/https/eds.s.ebscohost.com/eds/detail/detail?vid=11&sid=33a120e4-04f2-4927-b84b-ad716e0b3a54%40redis&bdata=JkF1dGhUeXBlPWlwLHNoaWImbGFuZz1wdC1wdCZzaXRlPWVkcy1saXZlJnNjb3BlPXNpdGU%3D#AN=176888&db=e000bww (accessed on 12 October 2022).
- Yew, B.; Alladi, S.; Shailaja, M.; Hodges, J.R.; Hornberger, M. Lost and Forgotten? Orientation Versus Memory in Alzheimer’s Disease and Frontotemporal Dementia. J. Alzheimers Dis. 2012, 33, 473–481. [Google Scholar] [CrossRef] [Green Version]
- Yamashita, K.; Uehara, T.; Prawiroharjo, P.; Yamashita, K.; Togao, O.; Hiwatashi, A.; Taniwaki, Y.; Utsunomiya, H.; Matsushita, T.; Yamasaki, R.; et al. Functional Connectivity Change between Posterior Cingulate Cortex and Ventral Attention Network Relates to the Impairment of Orientation for Time in Alzheimer’s Disease Patients. Brain Imaging Behav. 2019, 13, 154–161. [Google Scholar] [CrossRef]
- Bazydlo, A.; Zammit, M.; Wu, M.; Dean, D.; Johnson, S.; Tudorascu, D.; Cohen, A.; Cody, K.; Ances, B.; Laymon, C.; et al. White Matter Microstructure Associations with Episodic Memory in Adults with Down Syndrome: A Tract-Based Spatial Statistics Study. J. Neurodev. Disord. 2021, 13, 17. [Google Scholar] [CrossRef]
- Fernández, A.; Ramírez-Toraño, F.; Bruña, R.; Zuluaga, P.; Esteba-Castillo, S.; Abásolo, D.; Moldenhauer, F.; Shumbayawonda, E.; Maestú, F.; García-Alba, J. Brain Signal Complexity in Adults with Down Syndrome: Potential Application in the Detection of Mild Cognitive Impairment. Front. Aging Neurosci. 2022, 14, 988540. [Google Scholar] [CrossRef]
- Cole, J.H.; Annus, T.; Wilson, L.R.; Remtulla, R.; Hong, Y.T.; Fryer, T.D.; Acosta-Cabronero, J.; Cardenas-Blanco, A.; Smith, R.; Menon, D.K.; et al. Brain-Predicted Age in Down Syndrome Is Associated with Beta Amyloid Deposition and Cognitive Decline. Neurobiol. Aging 2017, 56, 41–49. [Google Scholar] [CrossRef]
- Paiva, A.F.; Nolan, A.; Thumser, C.; Santos, F.H. Screening of Cognitive Changes in Adults with Intellectual Disabilities: A Systematic Review. Brain Sci. 2020, 10, 848. [Google Scholar] [CrossRef]
- Lobo, A.; Ezquerra, J.; Gómez Burgada, F.; Sala, J.M.; Seva Díaz, A. Cognocitive Mini-Test (a Simple Practical Test to Detect Intellectual Changes in Medical Patients). Actas Luso. Esp. Neurol. Psiquiatr. Cienc. Afines 1979, 7, 189–202. [Google Scholar]
- McGirr, A.; Nathan, S.; Ghahremani, M.; Gill, S.; Smith, E.E.; Ismail, Z. Progression to Dementia or Reversion to Normal Cognition in Mild Cognitive Impairment as a Function of Late-Onset Neuropsychiatric Symptoms. Neurology 2022, 98, e2132–e2139. [Google Scholar] [CrossRef]
- Creese, B.; Arathimos, R.; Brooker, H.; Aarsland, D.; Corbett, A.; Lewis, C.; Ballard, C.; Ismail, Z. Genetic Risk for Alzheimer’s Disease, Cognition, and Mild Behavioral Impairment in Healthy Older Adults. Alzheimers Dement. Diagn. Assess. Dis. Monit. 2021, 13, e12164. [Google Scholar] [CrossRef]
Inclusion Criteria | Exclusion Criteria |
---|---|
≥39 years old | Severe sensory impairments |
Both sexes | No reliable informant |
Mild or moderate intellectual disability | Untreated anemia |
DS confirmed karyotype | Vitamin B12 deficiency |
Uncontrolled hypothyroidism | |
Behavior disorder (comorbid, affecting normal functioning) | |
Uncontrolled sleep disorders | |
Substance abuse | |
Previous central nervous system alterations | |
Relevant drug treatment |
Stages | |
---|---|
1 | Cognitive and behavioral stability All must be present I. BRIEF-P BRI index: ≥33 II. CAMCOG-DS total: ≥83 (mild ID); ≥65 (moderate ID) III. Any CAMDEX-DS diagnostic criteria (no A, B, C1 or C2) |
2 | Subjective cognitive and/or behavioral impairment All must be present I. BRIEF-P BRI index: ≤33 II. CAMCOG-DS total: ≥ 83 (mild ID); ≥65 (moderate ID) III. CAMDEX-DS diagnostic criteria: B or C1 or C2 |
3 | Mild cognitive and/or behavioral impairment (I and/or II) + III must be present I. BRIEF-P BRI index: ≤32 II. CAMCOG-DS total: ≤82 − 69 (mild ID), ≤64 − 57 (moderate ID) III. CAMDEX-DS diagnostic criteria: B or C1 or C2 ≤2 supporting criteria |
4 | Mild Alzheimer’s disease (I and/or II) + III must be present I. BRIEF-P BRI index: ≤32 II. CAMCOG-DS total: ≤68 (mild ID), ≤56 (moderate ID) III. CAMDEX-DS diagnostic criteria: A, B, C1 or C2, no D ≥2 supporting criteria |
5 | Moderate Alzheimer’s disease (I and/or II) + III must be present I. BRIEF-P BRI index: ≤32 II. CAMCOG-DS total: ≤68 (mild ID), ≤56 (moderate ID) III. CAMDEX-DS diagnostic criteria: A, B, C or C2, no D ≥3 supporting criteria |
6 | Advanced Alzheimer’s disease (I and/or II) + III must be present, or III and V I. BRIEF-P BRI index: ≤32 II. CAMCOG-DS total: ≤68 (mild ID), ≤56 (moderate ID) III. CAMDEX-DS diagnostic criteria: A, B, C1 or C2, no D ≥3 supporting criteria Incomplete or no administered neuropsychological examination |
GDS-DS Stages | Primary Diagnosis |
---|---|
1. Cognitive and behavioral stability 2. Subjective cognitive and/or behavioral impairment | 0. Cognitive stability |
3. Mild cognitive and/or behavioral impairment | 1. Mild cognitive impairment |
4. Mild Alzheimer’s disease 5. Moderate Alzheimer’s disease 6. Advanced Alzheimer’s disease | 2. Alzheimer’s disease |
Total | Cognitive Stability | Mild Cognitive Impairment | Alzheimer’s Disease | p | |
---|---|---|---|---|---|
n | 83 | 48 | 24 | 11 | |
Age | 46.65 (39–63) | 45.10 (39–43) | 47.46 (39–61) | 51.64 (43–63) | 0.01 * a |
Gender | 0.41 | ||||
Male | 46 (55.4%) | 24 (50%) | 16 (66.7%) | 6 (54.5%) | |
Female | 37 (44.6%) | 24 (50%) | 8 (33.3%) | 5 (45.6%) | |
ID level | 0.61 | ||||
Mild | 49 (59.1%) | 29 (60.4%) | 15 (62.5%) | 5 (45.6%) | |
Moderate | 34 (40.9%) | 19 (39.6%) | 9 (37.5%) | 6 (54.6%) |
GDS-DS Stages | p | |||||||
---|---|---|---|---|---|---|---|---|
Total | 1 | 2 | 3 | 4 | 5 | 6 | ||
Cognitive/Behavioral Stability | Subjective Cognitive/Behavioral Impairment | Mild Cognitive/Behavioral Impairment | Mild Alzheimer’s Disease | Moderate Alzheimer’s Disease | Advanced Alzheimer’s Disease | |||
n | 83 | 9 | 18 | 25 | 10 | 14 | 7 | |
Age | 46.65 (39–63) | 46.44 (40–61) | 44.72 (39–54) | 45.60 (39–54) | 46.60 (42–52) | 47.43 (41–54) | 54.14 (49–63) | 0.02 * a, * b |
Gender | 0.15 | |||||||
Male | 46 (55.4%) | 8 (88.9%) | 11(61.1%) | 10(40.0%) | 4(40.0%) | 9 (64.3%) | 4 (57.1%) | |
Female | 37 (44.6%) | 1 (11.1%) | 7 (38.9%) | 15 (60.0%) | 6 (60.0%) | 5 (35.7%) | 3 (42.9%) | |
ID level | 0.08 | |||||||
Mild | 49 (59.1%) | 4 (44.4%) | 15 (83.3%) | 17(68.0%) | 4 (40.0%) | 6 (42.9%) | 3 (42.9%) | |
Moderate | 34 (40.9%) | 5 (55.6%) | 3 (16.7%) | 8 (32.0%) | 6 (60.0%) | 8(57.1%) | 4 (57.1%) |
Cognitive and Behavioral Assessment | Rho |
---|---|
BRIEF-P | |
BRI index | −0.17 |
CAMCOG-DS | |
Total score | −0.70 ** |
Abstract thinking | −0.39 ** |
BT-ID | |
Orientation | −0.78 ** |
Free delay memory (stories) | −0.37 ** |
Semantic fluency (eat/drink) | −0.38 ** |
Formal fluency | −0.54 ** |
Visual discrimination | −0.11 |
GDS-DS Stages | p | ||||||
---|---|---|---|---|---|---|---|
1 | 2 | 3 | 4 | 5 | |||
Total | Cognitive/Behavioral Stability | Subjective Cognitive/Behavioral Impairment | Mild Cognitive/Behavioral Impairment | Mild Alzheimer’s Disease | Moderate Alzheimer’s Disease | ||
BRIEF-P | |||||||
BRI index | 40.99 (35–47) | 47.00 (39–49) | 40.00 (36–47) | 36.00 (30–42) | 40.00 (36–45) | 37.00 (36–51) | |
CAMCOG-DS | |||||||
Total score | 72.00 (55–88) | 84.00 (76–87) | 82.50 (76–87) | 71.00 (60–78) | 61.50 (50–71) | 49.5 (44–55) | ** a, ** b, ** c, ** d, e ** |
Abstract thinking | 2.00 (0–4.5) | 4.00 (1–5) | 4.50 (0–5) | 2.00 (0–4) | 1.00 (0–4) | 0.00 (0–1) | * b |
BT-ID | |||||||
Orientation | 91.00 (48–109) | 103.00 (97–113) | 109.00 (102–114) | 91.00 (73–108) | 46.00 (35–49) | 28.50 (21–40) | ** a, ** b, ** c, ** d, ** e, ** f |
Delay stories | 2.00 (0–4) | 3.00 (2–6) | 3.00 (2–5) | 3.00 (1–4) | 1.50 (0–4) | 0.00 (0–2) | * d, * e |
Semantic fluency (eat/drink) | 9.00 (6.5–12) | 10.00 (9–12) | 10.5 (8–13) | 10.00 (8–11) | 9.00 (5–13) | 6.00 (5–8) | * d |
Formal fluency | 2.00 (0–4) | 3.00 (2–4) | 4.00 (2–6) | 2.00 (1–4) | 0.00 (0–3) | 0.00 (0–1) | ** b, ** c, *** d |
Visual discrimination | 18.00 (16–19) | 18.00 (16–19) | 18.00 (17–20) | 18.00 (16–19) | 16.00 (16–19) | 18.00 (16–19) |
GDS-DS Stages | ||||||||
---|---|---|---|---|---|---|---|---|
1–2 | 2–3 | 3–4 | 4–5 | |||||
P | PSest | P | PSest | P | PSest | P | PSest | |
BRIEF-P | ||||||||
BRI index | 0.395 | 0.60 a | 0.061 | 0.67 b | 0.183 | 0.61 | 0.567 | 0.51 |
CAMCOG-DS | ||||||||
Total score | 0.938 | 0.51 | 0.010 * | 0.80 c | 0.027 * | 0.69 b | 0.088 | 0.68 b |
Abstract thinking | 0.595 | 0.56 | 0.139 | 0.63 a | 0.549 | 0.51 | 0.129 | 0.65 |
BT-ID | ||||||||
Orientation | 0.314 | 0.62 | 0.002 ** | 0.78 c | 0.000 *** | 0.94 c | 0.057 | 0.71 c |
Free delay memory (stories) | 0.775 | 0.53 | 0.663 | 0.54 | 0.331 | 0.55 | 0.467 | 0.56 a |
Semantic fluency (eat/drink) | 0.856 | 0.52 | 0.265 | 0.60 | 0.906 | 0.49 | 0.114 | 0.63 a |
Formal fluency | 0.364 | 0.61 | 0.011 * | 0.73 c | 0.118 | 0.66 b | 0.716 | 0.44 |
Visual discrimination | 0.733 | 0.54 | 0.367 | 0.58 | 0.363 | 0.56 a | 0.305 | 0.58 |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2023 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Rodríguez-Hidalgo, E.; García-Alba, J.; Novell, R.; Esteba-Castillo, S. The Global Deterioration Scale for Down Syndrome Population (GDS-DS): A Rating Scale to Assess the Progression of Alzheimer’s Disease. Int. J. Environ. Res. Public Health 2023, 20, 5096. https://doi.org/10.3390/ijerph20065096
Rodríguez-Hidalgo E, García-Alba J, Novell R, Esteba-Castillo S. The Global Deterioration Scale for Down Syndrome Population (GDS-DS): A Rating Scale to Assess the Progression of Alzheimer’s Disease. International Journal of Environmental Research and Public Health. 2023; 20(6):5096. https://doi.org/10.3390/ijerph20065096
Chicago/Turabian StyleRodríguez-Hidalgo, Emili, Javier García-Alba, Ramon Novell, and Susanna Esteba-Castillo. 2023. "The Global Deterioration Scale for Down Syndrome Population (GDS-DS): A Rating Scale to Assess the Progression of Alzheimer’s Disease" International Journal of Environmental Research and Public Health 20, no. 6: 5096. https://doi.org/10.3390/ijerph20065096
APA StyleRodríguez-Hidalgo, E., García-Alba, J., Novell, R., & Esteba-Castillo, S. (2023). The Global Deterioration Scale for Down Syndrome Population (GDS-DS): A Rating Scale to Assess the Progression of Alzheimer’s Disease. International Journal of Environmental Research and Public Health, 20(6), 5096. https://doi.org/10.3390/ijerph20065096