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Cortical hypometabolism and hypoperfusion in Parkinson’s disease is extensive: probably even at early disease stages

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Abstract

Recent cerebral blood flow (CBF) and glucose consumption (CMRglc) studies of Parkinson’s disease (PD) revealed conflicting results. Using simulated data, we previously demonstrated that the often-reported subcortical hypermetabolism in PD could be explained as an artifact of biased global mean (GM) normalization, and that low-magnitude, extensive cortical hypometabolism is best detected by alternative data-driven normalization methods. Thus, we hypothesized that PD is characterized by extensive cortical hypometabolism but no concurrent widespread subcortical hypermetabolism and tested it on three independent samples of PD patients. We compared SPECT CBF images of 32 early-stage and 33 late-stage PD patients with that of 60 matched controls. We also compared PET FDG images from 23 late-stage PD patients with that of 13 controls. Three different normalization methods were compared: (1) GM normalization, (2) cerebellum normalization, (3) reference cluster normalization (Yakushev et al.). We employed standard voxel-based statistics (fMRIstat) and principal component analysis (SSM). Additionally, we performed a meta-analysis of all quantitative CBF and CMRglc studies in the literature to investigate whether the global mean (GM) values in PD are decreased. Voxel-based analysis with GM normalization and the SSM method performed similarly, i.e., both detected decreases in small cortical clusters and concomitant increases in extensive subcortical regions. Cerebellum normalization revealed more widespread cortical decreases but no subcortical increase. In all comparisons, the Yakushev method detected nearly identical patterns of very extensive cortical hypometabolism. Lastly, the meta-analyses demonstrated that global CBF and CMRglc values are decreased in PD. Based on the results, we conclude that PD most likely has widespread cortical hypometabolism, even at early disease stages. In contrast, extensive subcortical hypermetabolism is probably not a feature of PD.

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Acknowledgments

The present study was supported by the Danish National Science Foundation (Dansk Grundforskningsfond), and Danish Parkinson’s Disease foundation (Dansk Parkinsonforening).

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Authors and Affiliations

  1. Department of Nuclear Medicine, Aarhus University Hospitals, Aarhus Sygehus, NBG, Building 3, Noerrebrogade 44, 8000, Aarhus, Denmark

    Per Borghammer

  2. PET Centre, Aarhus University Hospitals, Aarhus Sygehus, NBG, Building 3, Noerrebrogade 44, 8000, Aarhus, Denmark

    Per Borghammer, Mallar Chakravarty & Albert Gjedde

  3. Center of Functionally Integrative Neuroscience, University of Aarhus, Aarhus, Denmark

    Mallar Chakravarty, Kristjana Yr Jonsdottir & Albert Gjedde

  4. Allen Institute for Brain Science, Seattle, WA, USA

    Mallar Chakravarty

  5. Department of Radiology, National Center Hospital of Neurology and Psychiatry, Tokyo, Japan

    Noriko Sato

  6. Department of Nuclear Medicine, International Medical Center, Saitama Medical University, Saitama, Japan

    Hiroshi Matsuda

  7. Department of Brain Science and Molecular Imaging, National Center for Geriatrics and Gerontology, Obu, Aichi, Japan

    Kengo Ito, Yutaka Arahata & Takashi Kato

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  1. Per Borghammer
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Borghammer, P., Chakravarty, M., Jonsdottir, K.Y. et al. Cortical hypometabolism and hypoperfusion in Parkinson’s disease is extensive: probably even at early disease stages. Brain Struct Funct 214, 303–317 (2010). https://doi.org/10.1007/s00429-010-0246-0

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