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Reduced cortical thickness, surface area in patients with chronic obstructive pulmonary disease: a surface-based morphometry and neuropsychological study

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Abstract

Neural impairments accompanying chronic obstructive pulmonary disease (COPD) have received growing research attention. Previous neuroimaging studies exclusively used volumetric methods to measure cortical volume as a whole rather than focusing on anatomical and neuropathological distinct indices. Here we decomposed the cortical architecture into cortical thickness (CTh), surface area (SA), and gyrification, for the first time, to provide a more integrative profile of brain damage in COPD. Clinical T1-weighted MRI scans were acquired in 25 stable COPD patients (mean age 69) and 25 age-matched controls. Images were processed using surface-based morphometry to obtain cortical parameters enabling more accurate measurement in deep sulci and localized regional mapping. Demographic, physiological, and cognitive assessments were made and correlated with cortical indices. Compared to controls, COPD patients showed significantly reduced CTh broadly distributed in motor, parietal, and prefrontal cortices, together with more circumscribed SA reduction in dorsomedial prefrontal cortex and Broca’s area (cluster-level P < 0.05 corrected). No abnormal gyrification was detected. Decreased CTh in parietofrontal networks strongly correlated with visuospatial construction impairment in COPD patients. Furthermore, thinner dorsolateral prefrontal cortex (DLPFC) best predicted poorer performance (r 2 = 0.315, P = 0.004), and was associated with lower arterial oxygen saturation. These data indicate that cortical thinning is a key morphologic feature associated with COPD that could be partly attributed to oxygen desaturation and contributes to COPD visual memory and drawing deficits. Surface-based morphometry provides valuable information concerning COPD, and could ultimately help us to characterize the neurodegenerative pattern and to clarify neurologic mechanisms underlying cognitive dysfunction in COPD patients.

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References

  • Antonelli-Incalzi, R., Corsonello, A., Trojano, L., Pedone, C., Acanfora, D., Spada, A., et al. (2006). Drawing impairment predicts mortality in severe COPD. CHEST Journal, 130(6), 1687–1694.

    Article  Google Scholar 

  • Antonelli-Incalzi, R., Corsonello, A., Trojano, L., Pedone, C., Acanfora, D., Spada, A., et al. (2009). Heart rate variability and drawing impairment in hypoxemic COPD. Brain and Cognition, 70(1), 163–170.

    Article  PubMed  Google Scholar 

  • Barnes, P. J. (2010). Chronic obstructive pulmonary disease: effects beyond the lungs. PLoS Medicine, 7(3), e1000220.

    Article  PubMed  PubMed Central  Google Scholar 

  • Barnes, J., Ridgway, G. R., Bartlett, J., Henley, S., Lehmann, M., Hobbs, N., et al. (2010). Head size, age and gender adjustment in MRI studies: a necessary nuisance? NeuroImage, 53(4), 1244–1255.

    Article  PubMed  Google Scholar 

  • Cavanna, A. E., & Trimble, M. R. (2006). The precuneus: a review of its functional anatomy and behavioural correlates. Brain, 129(3), 564–583.

    Article  PubMed  Google Scholar 

  • Courtney, S. M., Petit, L., Maisog, J. M., Ungerleider, L. G., & Haxby, J. V. (1998). An area specialized for spatial working memory in human frontal cortex. Science, 279(5355), 1347–1351.

    Article  CAS  PubMed  Google Scholar 

  • Dale, A. M., Fischl, B., & Sereno, M. I. (1999). Cortical surface-based analysis: I. Segmentation and surface reconstruction. NeuroImage, 9(2), 179–194.

    Article  CAS  PubMed  Google Scholar 

  • Dickerson, B., Fenstermacher, E., Salat, D., Wolk, D., Maguire, R., Desikan, R., et al. (2008). Detection of cortical thickness correlates of cognitive performance: reliability across MRI scan sessions, scanners, and field strengths. NeuroImage, 39(1), 10–18.

    Article  CAS  PubMed  Google Scholar 

  • Dickerson, B. C., Feczko, E., Augustinack, J. C., Pacheco, J., Morris, J. C., Fischl, B., et al. (2009). Differential effects of aging and Alzheimer’s disease on medial temporal lobe cortical thickness and surface area. Neurobiology of Aging, 30(3), 432–440.

    Article  PubMed  Google Scholar 

  • Dodd, J., Getov, S., & Jones, P. (2010). Cognitive function in COPD. European Respiratory Journal, 35(4), 913–922.

    Article  CAS  PubMed  Google Scholar 

  • Dodd, J. W., Chung, A. W., van den Broek, M. D., Barrick, T. R., Charlton, R. A., & Jones, P. W. (2012). Brain structure and function in chronic obstructive pulmonary disease: a multimodal cranial magnetic resonance imaging study. American Journal of Respiratory and Critical Care Medicine, 186(3), 240–245.

    Article  PubMed  Google Scholar 

  • Eisner, M. D., Blanc, P. D., Yelin, E. H., Sidney, S., Katz, P. P., Ackerson, L., et al. (2008). COPD as a systemic disease: impact on physical functional limitations. The American Journal of Medicine, 121(9), 789–796.

    Article  PubMed  PubMed Central  Google Scholar 

  • Fischl, B., & Dale, A. M. (2000). Measuring the thickness of the human cerebral cortex from magnetic resonance images. Proceedings of the National Academy of Sciences, 97(20), 11050–11055.

    Article  CAS  Google Scholar 

  • Fischl, B., Sereno, M. I., & Dale, A. M. (1999). Cortical surface-based analysis: II: inflation, flattening, and a surface-based coordinate system. NeuroImage, 9(2), 195–207.

    Article  CAS  PubMed  Google Scholar 

  • Fischl, B., Salat, D. H., Busa, E., Albert, M., Dieterich, M., Haselgrove, C., et al. (2002). Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain. Neuron, 33(3), 341–355.

    Article  CAS  PubMed  Google Scholar 

  • Fix, A. J., Daughton, D., Kass, I., Bell, C. W., & Golden, C. J. (1985). Cognitive functioning and survival among patients with chronic obstructive pulmonary disease. International Journal of Neuroscience, 27(1–2), 13–17.

    Article  CAS  PubMed  Google Scholar 

  • Gong, Y. X. (1989). Manual for the Wechsler memory scale-Chinese revision. Changsha: Hunan Medical College.

    Google Scholar 

  • Gowen, E., & Miall, R. (2007). Differentiation between external and internal cuing: an fMRI study comparing tracing with drawing. NeuroImage, 36(2), 396–410.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grant, I., Heaton, R. K., McSweeny, A. J., Adams, K. M., & Timms, R. M. (1982). Neuropsychologic findings in hypoxemic chronic obstructive pulmonary disease. Archives of Internal Medicine, 142(8), 1470–1476.

    Article  CAS  PubMed  Google Scholar 

  • Graziano, M. S., Yap, G. S., & Gross, C. G. (1994). Coding of visual space by premotor neurons. Science, 266(5187), 1054–1057.

    Article  CAS  PubMed  Google Scholar 

  • Habets, P., Marcelis, M., Gronenschild, E., Drukker, M., & van Os, J. (2011). Reduced cortical thickness as an outcome of differential sensitivity to environmental risks in schizophrenia. Biological Psychiatry, 69(5), 487–494.

  • Huang, B. Y., & Castillo, M. (2008). Hypoxic-ischemic brain injury: imaging findings from birth to adulthood 1. Radiographics, 28(2), 417–439.

    Article  PubMed  Google Scholar 

  • Im, K., Lee, J.-M., Lyttelton, O., Kim, S. H., Evans, A. C., & Kim, S. I. (2008). Brain size and cortical structure in the adult human brain. Cerebral Cortex, 18(9), 2181–2191.

    Article  PubMed  Google Scholar 

  • Ino, T., Asada, T., Ito, J., Kimura, T., & Fukuyama, H. (2003). Parieto-frontal networks for clock drawing revealed with fMRI. Neuroscience Research, 45(1), 71–77.

    Article  PubMed  Google Scholar 

  • Jayalakshmi, K., Singh, S., Kalpana, B., Sairam, M., Muthuraju, S., & Ilavazhagan, G. (2007). N-acetyl cysteine supplementation prevents impairment of spatial working memory functions in rats following exposure to hypobaric hypoxia. Physiology & Behavior, 92(4), 643–650.

    Article  CAS  Google Scholar 

  • Jiao, Y., Chen, R., Ke, X., Chu, K., Lu, Z., & Herskovits, E. H. (2010). Predictive models of autism spectrum disorder based on brain regional cortical thickness. NeuroImage, 50(2), 589–599.

    Article  PubMed  Google Scholar 

  • Jones, P., & Agusti, A. (2006). Outcomes and markers in the assessment of chronic obstructive pulmonary disease. European Respiratory Journal, 27(4), 822–832.

    Article  CAS  PubMed  Google Scholar 

  • Joyner, A. H., Bloss, C. S., Bakken, T. E., Rimol, L. M., Melle, I., Agartz, I., et al. (2009). A common MECP2 haplotype associates with reduced cortical surface area in humans in two independent populations. Proceedings of the National Academy of Sciences, 106(36), 15483–15488.

    Article  CAS  Google Scholar 

  • Kelly, P. A., Viding, E., Wallace, G. L., Schaer, M., De Brito, S. A., Robustelli, B., et al. (2013). Cortical thickness, surface area, and gyrification abnormalities in children exposed to maltreatment: neural markers of vulnerability? Biological Psychiatry, 74(11), 845–852.

    Article  PubMed  Google Scholar 

  • Kravitz, D. J., Saleem, K. S., Baker, C. I., & Mishkin, M. (2011). A new neural framework for visuospatial processing. Nature Reviews Neuroscience, 12(4), 217–230.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lahousse, L., Vernooij, M. W., Darweesh, S. K., Akoudad, S., Loth, D. W., Joos, G. F., et al. (2013). Chronic obstructive pulmonary disease and cerebral microbleeds. The Rotterdam Study. American Journal of Respiratory and Critical Care Medicine, 188(7), 783–788.

    Article  CAS  PubMed  Google Scholar 

  • Lerch, J. P., & Evans, A. C. (2005). Cortical thickness analysis examined through power analysis and a population simulation. NeuroImage, 24(1), 163–173.

    Article  PubMed  Google Scholar 

  • Luders, E., Thompson, P., Narr, K., Toga, A., Jancke, L., & Gaser, C. (2006). A curvature-based approach to estimate local gyrification on the cortical surface. NeuroImage, 29(4), 1224–1230.

    Article  CAS  PubMed  Google Scholar 

  • Miller, E. K., & Cohen, J. D. (2001). An integrative theory of prefrontal cortex function. Annual Review of Neuroscience, 24(1), 167–202.

    Article  CAS  PubMed  Google Scholar 

  • Miyamoto, O., & Auer, R. (2000). Hypoxia, hyperoxia, ischemia, and brain necrosis. Neurology, 54(2), 362–362.

    Article  CAS  PubMed  Google Scholar 

  • Ortapamuk, H., & Naldoken, S. (2006). Brain perfusion abnormalities in chronic obstructive pulmonary disease: comparison with cognitive impairment. Annals of Nuclear Medicine, 20(2), 99–106.

    Article  PubMed  Google Scholar 

  • Palaniyappan, L., Mallikarjun, P., Joseph, V., White, T. P., & Liddle, P. F. (2011). Regional contraction of brain surface area involves three large-scale networks in schizophrenia. Schizophrenia Research, 129(2), 163–168.

    Article  PubMed  Google Scholar 

  • Panizzon, M. S., Fennema-Notestine, C., Eyler, L. T., Jernigan, T. L., Prom-Wormley, E., Neale, M., et al. (2009). Distinct genetic influences on cortical surface area and cortical thickness. Cerebral Cortex, 19(11), 2728–2735.

    Article  PubMed  PubMed Central  Google Scholar 

  • Pauwels, R. A., Buist, A. S., Calverley, P. M., Jenkins, C. R., & Hurd, S. S. (2001). Global strategy for the diagnosis, management, and prevention of chronic obstructive pulmonary disease. NHLBI/WHO Global Initiative for Chronic Obstructive Lung Disease (GOLD) Workshop summary. American Journal of Respiratory and Critical Care Medicine, 163(5), 1256–1276.

    Article  CAS  PubMed  Google Scholar 

  • Pereira, J. B., Ibarretxe‐Bilbao, N., Marti, M. J., Compta, Y., Junqué, C., Bargallo, N., et al. (2012). Assessment of cortical degeneration in patients with Parkinson’s disease by voxel‐based morphometry, cortical folding, and cortical thickness. Human Brain Mapping, 33(11), 2521–2534.

    Article  PubMed  Google Scholar 

  • Pillon, B. (1981). Visuo-constructive deficits and methods of compensation: Results of 85 patients with cerebral lesions. Neuropsychologia, 19(3), 375–383.

    Article  CAS  PubMed  Google Scholar 

  • Qiao, M., Meng, S., Foniok, T., & Tuor, U. I. (2009). Mild cerebral hypoxia-ischemia produces a sub-acute transient inflammatory response that is less selective and prolonged after a substantial insult. International Journal of Developmental Neuroscience, 27(7), 691–700.

    Article  CAS  PubMed  Google Scholar 

  • Rakic, P. (1988). Specification of cerebral cortical areas. Science, 241(4862), 170–176.

    Article  CAS  PubMed  Google Scholar 

  • Rakic, P. (1995). A small step for the cell, a giant leap for mankind: a hypothesis of neocortical expansion during evolution. Trends in Neurosciences, 18(9), 383–388.

    Article  CAS  PubMed  Google Scholar 

  • Rosas, H., Liu, A., Hersch, S., Glessner, M., Ferrante, R., Salat, D., et al. (2002). Regional and progressive thinning of the cortical ribbon in Huntington’s disease. Neurology, 58(5), 695–701.

    Article  CAS  PubMed  Google Scholar 

  • Ryu, C. W., Jahng, G. H., Choi, C. W., Rhee, H. Y., Kim, M. J., Kim, S. M., et al. (2013). Microstructural change of the brain in chronic obstructive pulmonary disease: a voxel-based investigation by MRI. COPD: Journal of Chronic Obstructive Pulmonary Disease, 10(3), 357–366.

    Article  PubMed  Google Scholar 

  • Salat, D. H., Buckner, R. L., Snyder, A. Z., Greve, D. N., Desikan, R. S., Busa, E., et al. (2004). Thinning of the cerebral cortex in aging. Cerebral Cortex, 14(7), 721–730.

    Article  PubMed  Google Scholar 

  • Schaer, M., Cuadra, M. B., Tamarit, L., Lazeyras, F., Eliez, S., & Thiran, J. (2008). A surface-based approach to quantify local cortical gyrification. IEEE Transactions on Medical Imaging, 27(2), 161–170.

    Article  PubMed  Google Scholar 

  • Schou, L., Østergaard, B., Rasmussen, L. S., Rydahl-Hansen, S., & Phanareth, K. (2012). Cognitive dysfunction in patients with chronic obstructive pulmonary disease–a systematic review. Respiratory Medicine, 106(8), 1071–1081.

    Article  PubMed  Google Scholar 

  • Ségonne, F., Dale, A., Busa, E., Glessner, M., Salat, D., Hahn, H., et al. (2004). A hybrid approach to the skull stripping problem in MRI. NeuroImage, 22(3), 1060–1075.

    Article  PubMed  Google Scholar 

  • Sled, J. G., Zijdenbos, A. P., & Evans, A. C. (1998). A nonparametric method for automatic correction of intensity nonuniformity in MRI data. Medical Imaging, IEEE Transactions on, 17(1), 87–97.

  • Tomaszewski Farias, S., Cahn-Weiner, D. A., Harvey, D. J., Reed, B. R., Mungas, D., Kramer, J. H., et al. (2009). Longitudinal changes in memory and executive functioning are associated with longitudinal change in instrumental activities of daily living in older adults. The Clinical Neuropsychologist, 23(3), 446–461.

    Article  PubMed  Google Scholar 

  • Weimar, C., Goertler, M., Röther, J., Ringelstein, E. B., Darius, H., Nabavi, D. G., et al. (2007). Systemic risk score evaluation in ischemic stroke patients (SCALA). Journal of Neurology, 254(11), 1562–1568.

    Article  PubMed  Google Scholar 

  • Zhang, H., Wang, X., Lin, J., Sun, Y., Huang, Y., Yang, T., et al. (2012). Grey and white matter abnormalities in chronic obstructive pulmonary disease: a case–control study. BMJ Open, 2(2), e000844.

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang, H., Wang, X., Lin, J., Sun, Y., Huang, Y., Yang, T., et al. (2013). Reduced regional gray matter volume in patients with chronic obstructive pulmonary disease: a voxel-based morphometry study. American Journal of Neuroradiology, 34(2), 334–339.

    Article  CAS  PubMed  Google Scholar 

  • Zilles, K., Armstrong, E., Schleicher, A., & Kretschmann, H. J. (1988). The human pattern of gyrification in the cerebral cortex. Anatomy and Embryology, 179(2), 173–179.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This work was supported by National Natural Science Foundation of China (Project No. 31071041; 81171324), Bureau of Science and Technology of Hangzhou (20090833B10) and Health Bureau of Zhejiang Province (2009A168).

Ethical standards and patient consent

We declare that all human studies have been approved by the Research Ethics Committee of Xiamen university and have therefore been performed in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki and its later amendments. We declare that all patients gave informed consent prior to inclusion in this study.

Conflicts of interest

Ji Chen, In-Tsang Lin, Haiyan Zhang, Jianzhong Lin, Shili Zheng, Ming Fan, and Jiaxing Zhang declare that they have no conflict of interest.

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Chen, J., Lin, IT., Zhang, H. et al. Reduced cortical thickness, surface area in patients with chronic obstructive pulmonary disease: a surface-based morphometry and neuropsychological study. Brain Imaging and Behavior 10, 464–476 (2016). https://doi.org/10.1007/s11682-015-9403-7

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