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The INECO Frontal Screening for the Evaluation of Executive Dysfunction in Cerebral Small Vessel Disease: Evidence from Quantitative MRI in a CADASIL Cohort from Colombia

Published online by Cambridge University Press:  03 June 2020

Dorothee Schoemaker ,
Yesica Zuluaga ,
Anand Viswanathan ,
Markus Shrimer ,
Heirangi Torrico-Teave ,
Lina Velilla ,
Carolina Ospina ,
Gloria Garcia Ospina ,
Francisco Lopera  and
Joseph F. Arboleda-Velasquez
...Show all authors
Dorothee Schoemaker
Affiliation:
Department of Psychiatry, Massachusetts General Hospital, Harvard Medical School, Boston, MA 02114, USA Department of Ophthalmology, Schepens Eye Research Institute, Harvard Medical School, Boston, MA 02114, USA
Yesica Zuluaga
Affiliation:
Grupo de Neurociencias, Universidad de Antioquia, Medellín 1226, Colombia
Anand Viswanathan
Affiliation:
Department of Neurology, Massachusetts General Hospital, Harvard Medical School, Boston, MA 02114, USA
Markus Shrimer
Affiliation:
Institute for Stroke and Dementia Research (ISD), University Hospital, LMU Munich, Munich 81377, Germany
Heirangi Torrico-Teave
Affiliation:
Department of Psychiatry, Massachusetts General Hospital, Harvard Medical School, Boston, MA 02114, USA
Lina Velilla
Affiliation:
Grupo de Neurociencias, Universidad de Antioquia, Medellín 1226, Colombia
Carolina Ospina
Affiliation:
Grupo de Neurociencias, Universidad de Antioquia, Medellín 1226, Colombia
Gloria Garcia Ospina
Affiliation:
Grupo de Neurociencias, Universidad de Antioquia, Medellín 1226, Colombia
Francisco Lopera
Affiliation:
Grupo de Neurociencias, Universidad de Antioquia, Medellín 1226, Colombia
Joseph F. Arboleda-Velasquez
Affiliation:
Department of Ophthalmology, Schepens Eye Research Institute, Harvard Medical School, Boston, MA 02114, USA
Yakeel T. Quiroz*
Affiliation:
Department of Psychiatry, Massachusetts General Hospital, Harvard Medical School, Boston, MA 02114, USA Grupo de Neurociencias, Universidad de Antioquia, Medellín 1226, Colombia Department of Neurology, Massachusetts General Hospital, Harvard Medical School, Boston, MA 02114, USA
*
*Correspondence and reprint requests to: Yakeel T. Quiroz, PhD, Assistant Professor, Harvard Medical School, Departments of Psychiatry and Neurology, Massachusetts General Hospital, 39 1st Avenue, Suite 101, Boston, MA 02129, USA. E-mail: [email protected]
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Abstract

Objectives:

Executive dysfunction is a predominant cognitive symptom in cerebral small vessel disease (SVD). The Institute of Cognitive Neurology Frontal Screening (IFS) is a well-validated screening tool allowing the rapid assessment of multiple components of executive function in Spanish-speaking individuals. In this study, we examined performance on the IFS in subjects with cerebral autosomal dominant arteriopathy with subcortical infarcts and leukoencephalopathy (CADASIL), an inherited condition leading to the early onset of SVD. We further explored associations between performance on the IFS and magnetic resonance imaging (MRI) markers of SVD.

Methods:

We recruited 24 asymptomatic CADASIL subjects and 23 noncarriers from Colombia. All subjects underwent a research MRI and a neuropsychological evaluation, including the IFS. Structural MRI markers of SVD were quantified in each subject, together with an SVD Sum Score representing the overall burden of cerebrovascular alterations. General linear model, correlation, and receiver operating characteristic curve analyses were used to explore group differences on the IFS and relationships with MRI markers of SVD.

Results:

CADASIL subjects had a significantly reduced performance on the IFS Total Score. Performance on the IFS correlated with all quantified markers of SVD, except for brain atrophy and perivascular spaces enlargement. Finally, while the IFS Total Score was not able to accurately discriminate between carriers and noncarriers, it showed adequate sensitivity and specificity in detecting the presence of multiple MRI markers of SVD.

Conclusions:

These results suggest that the IFS may be a useful screening tool to assess executive function and disease severity in the context of SVD.

Keywords

Executive functionScreening toolQuantitative magnetic resonance imagingWhite matter hyperintensityLacunesCerebral microbleedsEnlarged perivascular spacesNOTCH3Spanish
Type
Regular Research
Information
Journal of the International Neuropsychological Society , Volume 26 , Issue 10 , November 2020 , pp. 1006 - 1018
Copyright
Copyright © INS. Published by Cambridge University Press, 2020

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References

REFERENCES

Aguirre-Acevedo, D.C., Gomez, R.D., Moreno, S., Henao-Arboleda, E., Motta, M., Muñoz, C., … Lopera, F. (2007). Validity and reliability of the CERAD-Col neuropsychological battery. Revista de neurologia, 45(11), 655–660.CrossRefGoogle ScholarPubMed
Arango-Lasprilla, J.C. (2015). Commonly used neuropsychological tests for Spanish speakers: Normative data from Latin America. NeuroRehabilitation, 37(4), 489–491.CrossRefGoogle Scholar
Arthur, W. Jr & Day, D.V. (1994). Development of a short form for the Raven Advanced Progressive Matrices Test. Educational and Psychological measurement, 54(2), 394–403.CrossRefGoogle Scholar
Auer, S. & Reisberg, B. (1997). The GDS/FAST staging system. International Psychogeriatrics, 9(S1), 167–171.CrossRefGoogle ScholarPubMed
Baez, S., Ibanez, A., Gleichgerrcht, E., Perez, A., Roca, M., Manes, F., & Torralva, T. (2014). The utility of IFS (INECO Frontal Screening) for the detection of executive dysfunction in adults with bipolar disorder and ADHD. Psychiatry Research, 216(2), 269–276.CrossRefGoogle ScholarPubMed
Baez, S., Pinasco, C., Roca, M., Ferrari, J., Couto, B., García-Cordero, I., … Matallana, D.. (2017). Brain structural correlates of executive and social cognition profiles in behavioral variant frontotemporal dementia and elderly bipolar disorder. Neuropsychologia, 126, 159–169.CrossRefGoogle ScholarPubMed
Bahia, V.S., Cecchini, M.A., Cassimiro, L., Viana, R., Lima-Silva, T.B., de Souza, L.C., … Balthazar, M.L.F. (2018). The accuracy of INECO frontal screening in the diagnosis of executive dysfunction in frontotemporal dementia and Alzheimer disease. Alzheimer Disease & Associated Disorders, 32(4), 314–319.Google Scholar
Benjamin, P., Trippier, S., Lawrence, A.J., Lambert, C., Zeestraten, E., Williams, O.A., … MacKinnon, A.D. (2018). Lacunar infarcts, but not perivascular spaces, are predictors of cognitive decline in cerebral small-vessel disease. Stroke, 49(3), 586–593.CrossRefGoogle Scholar
Buffon, F., Porcher, R., Hernandez, K., Kurtz, A., Pointeau, S., Vahedi, K., … Chabriat, H. (2006). Cognitive profile in CADASIL. Journal of Neurology, Neurosurgery & Psychiatry, 77(2), 175–180.CrossRefGoogle ScholarPubMed
Chabriat, H., Joutel, A., Dichgans, M., Tournier-Lasserve, E., & Bousser, M.-G. (2009). Cadasil. The Lancet Neurology, 8(7), 643–653.CrossRefGoogle ScholarPubMed
Custodio, N., Herrera-Perez, E., Lira, D., Roca, M., Manes, F., Báez, S., & Torralva, T. (2016). Evaluation of the INECO Frontal Screening and the Frontal Assessment Battery in Peruvian patients with Alzheimer’s disease and behavioral variant Frontotemporal dementia. eNeurologicalSci, 5, 25–29.CrossRefGoogle ScholarPubMed
DANE. (2020). Estratificación socioeconómica para servicios públicos domiciliarios. 2020, from https://www.dane.gov.co/index.php/servicios-al-ciudadano/servicios-informacion/estratificacion-socioeconomica Google Scholar
Debette, S. & Markus, H.S. (2010). The clinical importance of white matter hyperintensities on brain magnetic resonance imaging: systematic review and meta-analysis. BMJ, 341, c3666.CrossRefGoogle ScholarPubMed
Desmond, D.W. (2004). The neuropsychology of vascular cognitive impairment: is there a specific cognitive deficit? Journal of the Neurological Sciences, 226(1–2), 3–7.CrossRefGoogle Scholar
Desmond, D.W., Moroney, J.T., Lynch, T., Chan, S., Chin, S.S., & Mohr, J.P. (1999). The natural history of CADASIL: a pooled analysis of previously published cases. Stroke, 30(6), 1230–1233.CrossRefGoogle ScholarPubMed
Fazekas, F., Chawluk, J.B., Alavi, A., Hurtig, H.I., & Zimmerman, R.A. (1987). MR signal abnormalities at 1.5 T in Alzheimer’s dementia and normal aging. American Journal of Roentgenology, 149(2), 351–356.CrossRefGoogle Scholar
Gleichgerrcht, E., Roca, M., Manes, F., & Torralva, T. (2011). Comparing the clinical usefulness of the Institute of Cognitive Neurology (INECO) Frontal Screening (IFS) and the Frontal Assessment Battery (FAB) in frontotemporal dementia. Journal of Clinical and Experimental Neuropsychology, 33(9), 997–1004.CrossRefGoogle Scholar
Greenberg, S.M, Vernooij, M.W, Cordonnier, C., Viswanathan, A., Salman, R.A.-S., Warach, S., …Microbleed Study Group. (2009). Cerebral microbleeds: a guide to detection and interpretation. The Lancet Neurology, 8(2), 165–174.CrossRefGoogle ScholarPubMed
Huijts, M., Duits, A., Staals, J., Kroon, B., de Leeuw, P., & van Oostenbrugge, R. (2014). Basal ganglia enlarged perivascular spaces are linked to cognitive function in patients with cerebral small vessel disease. Current Neurovascular Research, 11(2), 136–141.CrossRefGoogle ScholarPubMed
Hurford, R., Charidimou, A., Fox, Z., Cipolotti, L., Jager, R., & Werring, D.J. (2014). MRI-visible perivascular spaces: relationship to cognition and small vessel disease MRI markers in ischaemic stroke and TIA. Journal of Neurology, Neurosurgery, and Psychiatry, 85(5), 522–525.CrossRefGoogle ScholarPubMed
Jory, J.I., Bruna, A.A., Muñoz-Neira, C., & Chonchol, A.S. (2013). Chilean version of the INECO Frontal Screening (IFS-Ch): psychometric properties and diagnostic accuracy. Dementia & Neuropsychologia, 7(1), 40.Google ScholarPubMed
Joutel, A., Corpechot, C., Ducros, A., Vahedi, K., Chabriat, H., Mouton, P., … Maréchal, E. (1996). Notch3 mutations in CADASIL, a hereditary adult-onset condition causing stroke and dementia. Nature, 383(6602), 707–710.CrossRefGoogle ScholarPubMed
Jouvent, E., Mangin, J.-F., Porcher, R., Viswanathan, A., O’sullivan, M., Guichard, J.-P., … Chabriat, H. (2008). Cortical changes in cerebral small vessel diseases: a 3D MRI study of cortical morphology in CADASIL. Brain, 131(8), 2201–2208.CrossRefGoogle ScholarPubMed
Jouvent, E., Viswanathan, A., Mangin, J.-F., O’Sullivan, M., Guichard, J.-P., Gschwendtner, A., … Pachaï, C.. (2007). Brain atrophy is related to lacunar lesions and tissue microstructural changes in CADASIL. Stroke, 38(6), 1786–1790.CrossRefGoogle ScholarPubMed
Kloppenborg, R.P., Nederkoorn, P.J., Geerlings, M.I., & van den Berg, E. (2014). Presence and progression of white matter hyperintensities and cognition: a meta-analysis. Neurology, 82(23), 2127–2138.CrossRefGoogle ScholarPubMed
MacLullich, A.M.J., Wardlaw, J.M., Ferguson, K.J., Starr, J.M., Seckl, J.R., & Deary, I.J. (2004). Enlarged perivascular spaces are associated with cognitive function in healthy elderly men. Journal of Neurology, Neurosurgery & Psychiatry, 75(11), 1519–1523.CrossRefGoogle ScholarPubMed
Moreira, H.S., Costa, A.S., Castro, S.L., Lima, C.F., & Vicente, S.G. (2017). Assessing executive dysfunction in neurodegenerative disorders: a critical review of brief neuropsychological tools. Frontiers in Aging Neuroscience, 9, 369.CrossRefGoogle ScholarPubMed
Nelson, H.E. (1976). A modified card sorting test sensitive to frontal lobe defects. Cortex, 12(4), 313–324.CrossRefGoogle ScholarPubMed
Pantoni, L. (2010). Cerebral small vessel disease: from pathogenesis and clinical characteristics to therapeutic challenges. The Lancet Neurology, 9(7), 689–701.CrossRefGoogle ScholarPubMed
Potter, G., Morris, Z., & Wardlaw, J. (2015). Enlarged perivascular spaces (EPVS): a visual rating scale and user guide (pp. 1–48), Available at: http://www.sbirc.ed.ac.uk/documents/epvs-rating-scaleuser-guide.pdf Google Scholar
Reitan, R.M. (1971). Trail making test results for normal and brain-damaged children. Perceptual and Motor Skills, 33(2), 575–581.CrossRefGoogle ScholarPubMed
Reyes, S., Viswanathan, A., Godin, O., Dufouil, C., Benisty, S., Hernandez, K., … Czernecki, V. (2009). Apathy: a major symptom in CADASIL. Neurology, 72(10), 905–910.CrossRefGoogle Scholar
Romero-Vanegas, S., Vargas-Gonzalez, J.C., Arboleda, H., Lopera, F., & Pardo, R.. (2014). Validation of the ineco frontal screening in a colombian population. Alzheimer’s & Dementia: The Journal of the Alzheimer’s Association, 10(4), P726.CrossRefGoogle Scholar
Schirmer, M.D, Dalca, A.V, Sridharan, R., Giese, A.-K., Donahue, K.L, Nardin, M.J, … Wasselius, J. (2019). White matter hyperintensity quantification in large-scale clinical acute ischemic stroke cohorts – The MRI-GENIE study. NeuroImage: Clinical, 10, 101884.CrossRefGoogle Scholar
Schirmer, M.D., Giese, A.-K., Fotiadis, P., Etherton, M.R., Cloonan, L., Viswanathan, A., … Rost, N. (2019). Spatial signature of white matter hyperintensities in stroke patients. Frontiers in Neurology, 10, 208.CrossRefGoogle ScholarPubMed
Silva, T., Monteiro, L., & Lopes, E. (2014). INECO Frontal Screening: an instrument to assess executive dysfunction in schizophrenia. The Spanish Journal of Psychology, 17, E19.CrossRefGoogle Scholar
Staals, J., Booth, T., Morris, Z., Bastin, M.E., Gow, A.J., Corley, J., … Wardlaw, J.M. (2015). Total MRI load of cerebral small vessel disease and cognitive ability in older people. Neurobiology of Aging, 36(10), 2806–2811.CrossRefGoogle ScholarPubMed
Stromillo, M.L., Dotti, M.T., Battaglini, M., Mortilla, M., Bianchi, S., Plewnia, K., … De Stefano, N. (2009). Structural and metabolic brain abnormalities in preclinical cerebral autosomal dominant arteriopathy with subcortical infarcts and leucoencephalopathy. Journal of Neurology, Neurosurgery & Psychiatry, 80(1), 41–47.CrossRefGoogle ScholarPubMed
Tombaugh, T.N, Kozak, J., & Rees, L. (1999). Normative data stratified by age and education for two measures of verbal fluency: FAS and animal naming. Archives of Clinical Neuropsychology, 14(2), 167–177.Google ScholarPubMed
Torralva, T., Roca, M., Gleichgerrcht, E., Lopez, P., & Manes, F. (2009). INECO Frontal Screening (IFS): A brief, sensitive, and specific tool to assess executive functions in dementia–CORRECTED VERSION. Journal of the International Neuropsychological Society, 15(5), 777–786.CrossRefGoogle Scholar
Torres, V.L., Vila-Castelar, C., Bocanegra, Y., Baena, A., Guzmán-Vélez, E., Aguirre-Acevedo, D.C., … Moreno, S. (2019). Normative data stratified by age and education for a Spanish neuropsychological test battery: Results from the Colombian Alzheimer’s prevention initiative registry. Applied Neuropsychology: Adult, 1–15.Google ScholarPubMed
Wardlaw, J.M., Smith, E.E., Biessels, G.J., Cordonnier, C., Fazekas, F., Frayne, R., … Benavente, O.R. (2013). Neuroimaging standards for research into small vessel disease and its contribution to ageing and neurodegeneration. The Lancet Neurology, 12(8), 822–838.CrossRefGoogle ScholarPubMed
Wechsler, D. (1999). WAIS-III escala de inteligencia de Wechsler para adultos. Madrid: TEA Ediciones.Google Scholar
Welsh, K.A., Butters, N., Mohs, R.C., Beekly, D., Edland, S., Fillenbaum, G., & Heyman, A. (1994). The Consortium to Establish a Registry for Alzheimer’s Disease (CERAD). Part V. A normative study of the neuropsychological battery. Neurology, 44(4), 609–609.CrossRefGoogle Scholar
Yesavage, J.A. & Sheikh, J.I. (1986). Geriatric Depression Scale (GDS): recent evidence and development of a shorter version. Clinical Gerontologist, 5(1–2), 165–173.CrossRefGoogle Scholar
Yilmaz, P., Ikram, M.K., Niessen, W.J., Ikram, M.A., & Vernooij, M.W. (2018). practical small vessel disease score relates to stroke, dementia, and death: the Rotterdam Study. Stroke, 49(12), 2857–2865.CrossRefGoogle Scholar