Abstract
Three to 6 months after an acute coronary syndrome (ACS), cognitive impairment is observed in more than 30 % of the patients, mainly in executive functioning. The aim of this study was to investigate, using multimodal MRI, cerebral anatomo-functional substratum of executive dysfunction. Thirty-three patients were recruited 4 ± 1 months after a first ACS. Executive functions were evaluated with the Trail-Making-Test-B (TMTB) at baseline (ie 4 ± 1 months after ACS) and 6 months later (ie 10 ± 1 months after ACS). Using both time-points, we identified 3 groups of patients according to normative data based on age, gender and education level: 15 ‘cognitively normal’ patients without impairment at each follow-up, 10 ‘transient impaired’ patients with an impairment only at baseline and 8 ‘impairing’ patients with an impairment only at follow-up. We explored, in the whole-brain, the structural integrity using Voxel-Based Morphometry and Tract-Based Spatial Statistics and the resting-state functional connectivity using Network-Based Statistics. No structural difference was observed between impaired and cognitively normal patients. At the functional level, compared to the ‘cognitively normal’ group, the ‘transient impaired’ patients presented an increased functional connectivity in a network centered on middle-orbito-frontal regions, whereas the ‘impairing’ patients presented only a non-significant decrease of functional connectivity. Executive dysfunction in ACS patients is associated to functional but no structural characteristics, particularly to an increased functional connectivity in cognitive networks in transient impaired patients. Further studies with larger sample size are needed to confirm these results and to determine if these patients could be at higher risk for developing permanent cognitive disorders.
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Allen, M. D., Owens, T. E., Fong, A. K., & Richards, D. R. (2011). A functional neuroimaging analysis of the trail making test-B: implications for clinical application. Behav Neurol, 24(2), 159–171. doi:10.3233/BEN-2011-0278.
Almeida, O. P., Garrido, G. J., Beer, C., Lautenschlager, N. T., Arnolda, L., & Flicker, L. (2012). Cognitive and brain changes associated with ischaemic heart disease and heart failure. Eur Heart J, 33(14), 1769–1776. doi:10.1093/eurheartj/ehr467.
Amieva, H., Le Goff, M., Stoykova, R., Lafont, S., Ritchie, K., Tzourio, C., et al. (2009). Trail Making Test A et B (version sans correction des erreurs) : normes en population chez des sujets âgés, issues de l’étude des trois Cités. Rev Neuropsychol, 1(3), 210–220. doi:10.3917/rne.013.0210.
Ashburner, J., & Friston, K. J. (2000). Voxel-based morphometry–the methods. NeuroImage, 11(6 Pt 1), 805–821. doi:10.1006/nimg.2000.0582.
Bai, F., Watson, D. R., Shi, Y., Wang, Y., Yue, C., Teng, Y., et al. (2011). Specifically progressive deficits of brain functional marker in amnestic type mild cognitive impairment. PLoS One, 6(9), e24271. doi:10.1371/journal.pone.0024271.
Bainbridge, D., Cheng, D., Martin, J., Novick, R., & Evidence-based Peri-operative Clinical Outcomes Research (EPiCOR) Group (2007). Does off-pump or minimally invasive coronary artery bypass reduce mortality, morbidity, and resource utilization when compared with percutaneous coronary intervention? A meta-analysis of randomized trials. J Thorac Cardiovasc Surg, 133(3), 623–631. doi:10.1016/j.jtcvs.2006.11.019.
Bertrand, M. E., Simoons, M. L., Fox, K. A. A., Wallentin, L. C., Hamm, C. W., McFadden, E., et al. (2002). Management of acute coronary syndromes in patients presenting without persistent ST-segment elevation. Eur Heart J, 23(23), 1809–1840.
Bonavita, S., Gallo, A., Sacco, R., Corte, M. D., Bisecco, A., Docimo, R., et al. (2011). Distributed changes in default-mode resting-state connectivity in multiple sclerosis. Multiple Sclerosis (Houndmills, Basingstoke, England), 17(4), 411–422. doi:10.1177/1352458510394609.
Borst, A., & Theunissen, F. E. (1999). Information theory and neural coding. Nat Neurosci, 2(11), 947–957. doi:10.1038/14731.
Burggren, A. C., Renner, B., Jones, M., Donix, M., Suthana, N. A., Martin-Harris, L., et al. (2011). Thickness in entorhinal and subicular cortex predicts episodic memory decline in mild cognitive impairment. Int J Alzheimers Dis, 2011, 956053. doi:10.4061/2011/956053.
Castellazzi, G., Palesi, F., Casali, S., Vitali, P., Sinforiani, E., Wheeler-Kingshott, C. A. M., & D’Angelo, E. (2014). A comprehensive assessment of resting state networks: bidirectional modification of functional integrity in cerebro-cerebellar networks in dementia. Front Neurosci, 8. doi:10.3389/fnins.2014.00223.
Cheng, H.-L., Lin, C.-J., Soong, B.-W., Wang, P.-N., Chang, F.-C., Wu, Y.-T., et al. (2012). Impairments in cognitive function and brain connectivity in severe asymptomatic carotid stenosis. Stroke J Cereb Circulation, 43(10), 2567–2573. doi:10.1161/STROKEAHA.111.645614.
Chumbley, J. R., & Friston, K. J. (2009). False discovery rate revisited: FDR and topological inference using Gaussian random fields. NeuroImage, 44(1), 62–70. doi:10.1016/j.neuroimage.2008.05.021.
Damoiseaux, J. S., Prater, K. E., Miller, B. L., & Greicius, M. D. (2012). Functional connectivity tracks clinical deterioration in Alzheimer’s disease. Neurobiol Aging, 33(4), 828.e19–828.e30. doi:10.1016/j.neurobiolaging.2011.06.024.
Davidson, K. W., Kupfer, D. J., Bigger, J. T., Califf, R. M., Carney, R. M., Coyne, J. C., et al. (2006). Assessment and treatment of depression in patients with cardiovascular disease: national heart, lung, and blood institute working group report. Psychosom Med, 68(5), 645–650. doi:10.1097/01.psy.0000233233.48738.22.
Geerlings, M. I., Appelman, A. P. A., Vincken, K. L., Mali, W. P. T. M., van der Graaf, Y., & SMART Study Group. (2009). Association of white matter lesions and lacunar infarcts with executive functioning: the SMART-MR study. Am J Epidemiol, 170(9), 1147–1155. doi:10.1093/aje/kwp256.
Goto, T., Yoshitake, A., Baba, T., Shibata, Y., Sakata, R., & Uozumi, H. (1997). Cerebral ischemic disorders and cerebral oxygen balance during cardiopulmonary bypass surgery: preoperative evaluation using magnetic resonance imaging and angiography. Anesth Analg, 84(1), 5–11.
Hawellek, D. J., Hipp, J. F., Lewis, C. M., Corbetta, M., & Engel, A. K. (2011). Increased functional connectivity indicates the severity of cognitive impairment in multiple sclerosis. Proc Natl Acad Sci U S A, 108(47), 19066–19071. doi:10.1073/pnas.1110024108.
Hillary, F. G., Rajtmajer, S. M., Roman, C. A., Medaglia, J. D., Slocomb-Dluzen, J. E., Calhoun, V. D., et al. (2014). The rich get richer: brain injury elicits hyperconnectivity in core subnetworks. PLoS One, 9(8), e104021. doi:10.1371/journal.pone.0104021.
Hillary, F. G., Roman, C. A., Venkatesan, U., Rajtmajer, S. M., Bajo, R., & Castellanos, N. D. (2015). Hyperconnectivity is a fundamental response to neurological disruption. Neuropsychology, 29(1), 59–75. doi:10.1037/neu0000110.
Hudetz, J. A., Patterson, K. M., & Pagel, P. S. (2012). Comparison of pre-existing cognitive impairment, amnesic mild cognitive impairment, and multiple domain mild cognitive impairment in men scheduled for coronary artery surgery. Eur J Anaesthesiol, 29(7), 320–325. doi:10.1097/EJA.0b013e328354223d.
Kim, J., Kim, Y.-H., & Lee, J.-H. (2013). Hippocampus-precuneus functional connectivity as an early sign of Alzheimer’s disease: a preliminary study using structural and functional magnetic resonance imaging data. Brain Res, 1495, 18–29. doi:10.1016/j.brainres.2012.12.011.
Marijke Miatton, M. W. (2004). Updated and extended Flemish normative data of commonly used neuropsychological tests. Psychologica Belgica, 44(3), 189–216.
Qi, Z., Wu, X., Wang, Z., Zhang, N., Dong, H., Yao, L., & Li, K. (2010). Impairment and compensation coexist in amnestic MCI default mode network. NeuroImage, 50(1), 48–55. doi:10.1016/j.neuroimage.2009.12.025.
Reitan, R. (1979). Manual for administration of neuropsychological test batteries for adults and children: Tucson. AZ: Reitan Neuropsychological laboratories, Inc..
Roosendaal, S. D., Hulst, H. E., Vrenken, H., Feenstra, H. E. M., Castelijns, J. A., Pouwels, P. J. W., et al. (2010). Structural and functional hippocampal changes in multiple sclerosis patients with intact memory function. Radiology, 255(2), 595–604. doi:10.1148/radiol.10091433.
Selnes, O. A., & McKhann, G. M. (2005). Neurocognitive complications after coronary artery bypass surgery. Ann Neurol, 57(5), 615–621. doi:10.1002/ana.20481.
Seo, S. W., Lee, J.-M., Im, K., Park, J.-S., Kim, S.-H., Kim, S. T., et al. (2012). Cardiovascular risk factors cause cortical thinning in cognitively impaired patients: relationships among cardiovascular risk factors, white matter hyperintensities, and cortical atrophy. Alzheimer Dis Assoc Disord, 26(2), 106–112. doi:10.1097/WAD.0b013e31822e0831.
Silbert, B. S., Scott, D. A., Evered, L. A., Lewis, M. S., & Maruff, P. T. (2007). Preexisting cognitive impairment in patients scheduled for elective coronary artery bypass graft surgery. Anesth Analg, 104(5), 1023–1028 tables of contents. doi:10.1213/01.ane.0000263285.03361.3a.
Smith, S. M., Jenkinson, M., Johansen-Berg, H., Rueckert, D., Nichols, T. E., Mackay, C. E., et al. (2006). Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data. NeuroImage, 31(4), 1487–1505. doi:10.1016/j.neuroimage.2006.02.024.
Son, S. J., Kim, J., Lee, E., Park, J. Y., Namkoong, K., Hong, C. H., et al. (2015). Effect of hypertension on the resting-state functional connectivity in patients with Alzheimer’s disease (AD). Arch Gerontol Geriatr, 60(1), 210–216. doi:10.1016/j.archger.2014.09.012.
Tzourio-Mazoyer, N., Landeau, B., Papathanassiou, D., Crivello, F., Etard, O., Delcroix, N., et al. (2002). Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. NeuroImage, 15(1), 273–289. doi:10.1006/nimg.2001.0978.
Whitfield-Gabrieli, S., & Nieto-Castanon, A. (2012). Conn: a functional connectivity toolbox for correlated and anticorrelated brain networks. Brain Connectivity, 2(3), 125–141. doi:10.1089/brain.2012.0073.
Zakzanis, K. K., Mraz, R., & Graham, S. J. (2005). An fMRI study of the trail making test. Neuropsychologia, 43(13), 1878–1886. doi:10.1016/j.neuropsychologia.2005.03.013.
Zalesky, A., Fornito, A., & Bullmore, E. T. (2010). Network-based statistic: identifying differences in brain networks. NeuroImage, 53(4), 1197–1207. doi:10.1016/j.neuroimage.2010.06.041.
Acknowledgments
The authors are grateful to P. Perez, methodological coordinator, J. Asselineau and R. Sitta, biostatisticians from the USMR (Unité de Soutien Méthodologique à la Recherche Clinique et Epidémiologique) at the University hospital of Bordeaux in France for their methodological advices.
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All procedures followed were in accordance with the ethical standards of the responsible committee on human experimentation (institutional and national) and with the Helsinki Declaration of 1975, and the applicable revisions at the time of the investigation. Informed consent was obtained from all patients for being included in the study.
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Local funding (2007/31) was obtained for patient recruitment, MRI acquisition and patients follow-up.
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Bernard, C., Catheline, G., Dilharreguy, B. et al. Cerebral changes and cognitive impairment after an ischemic heart disease: a multimodal MRI study. Brain Imaging and Behavior 10, 893–900 (2016). https://doi.org/10.1007/s11682-015-9483-4
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DOI: https://doi.org/10.1007/s11682-015-9483-4