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Quantitative validation of a visual rating scale for frontal atrophy: associations with clinical status, APOE e4, CSF biomarkers and cognition

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Abstract

Objectives

To validate a visual rating scale of frontal atrophy with quantitative imaging and study its association with clinical status, APOE ε4, CSF biomarkers, and cognition.

Methods

The AddNeuroMed and ADNI cohorts were combined giving a total of 329 healthy controls, 421 mild cognitive impairment patients, and 286 Alzheimer’s disease (AD) patients. Thirty-four patients with frontotemporal dementia (FTD) were also included. Frontal atrophy was assessed with the frontal sub-scale of the global cortical atrophy scale (GCA-F) on T1-weighted images. Automated imaging markers of cortical volume, thickness, and surface area were evaluated. Manual tracing was also performed.

Results

The GCA-F scale reliably reflects frontal atrophy, with orbitofrontal, dorsolateral, and motor cortices being the regions contributing most to the GCA-F ratings. GCA-F primarily reflects reductions in cortical volume and thickness, although it was able to detect reductions in surface area too. The scale showed significant associations with clinical status and cognition.

Conclusion

The GCA-F scale may have implications for clinical practice as supportive diagnostic tool for disorders demonstrating predominant frontal atrophy such as FTD and the executive presentation of AD. We believe that GCA-F is feasible for use in clinical routine for the radiological assessment of dementia and other disorders.

Key points

• The GCA-F visual rating scale reliably reflects frontal brain atrophy.

• Orbitofrontal, dorsolateral, and motor cortices are the most contributing regions.

• GCA-F shows significant associations with clinical status and cognition.

• GCA-F may be supportive diagnostic tool for disorders demonstrating predominant frontal atrophy.

• GCA-F may be feasible for use in radiological routine.

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Abbreviations

MTA:

medial temporal atrophy

PA:

posterior atrophy

GCA:

global cortical atrophy

GCA-F:

global cortical atrophy – frontal sub-scale

SFG:

superior frontal gyrus

MFG:

middle frontal gyrus

IFG:

inferior frontal gyrus

ORB:

orbitofrontal cortex

DACC:

and dorsal anterior cingulate gyrus

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Acknowledgments

The scientific guarantor of this publication is Dr. Daniel Ferreira (Department of Neurobiology, Care Sciences and Society, Karolinska Institutet, Sweden). The authors of this manuscript declare no relationships with any companies, whose products or services may be related to the subject matter of the article. The authors thank Swedish Brain Power, the Strategic Research Programme in Neuroscience at Karolinska Institutet (StratNeuro), The Swedish Alzheimer Foundation, and the regional agreement on medical training and clinical research (ALF) between Stockholm County Council. AddNeuroMed is supported by InnoMed (Innovative Medicines in Europe), an Integrated Project funded by the European Union of the Sixth Framework programme priority FP6-2004-LIFESCIHEALTH-5, Life Sciences, Genomics and Biotechnology for Health. Data collection and sharing for the ADNI project was funded by the Alzheimer's Disease Neuroimaging Initiative (ADNI) (National Institutes of Health Grant U01 AG024904) and DOD ADNI (Department of Defense award number W81XWH-12-2-0012). ADNI is funded by the National Institute on Aging, the National Institute of Biomedical Imaging and Bioengineering, and through generous contributions from the following: Alzheimer’s Association; Alzheimer’s Drug Discovery Foundation; Araclon Biotech; BioClinica, Inc.; Biogen Idec Inc.; Bristol-Myers Squibb Company; Eisai Inc.; Elan Pharmaceuticals, Inc.; Eli Lilly and Company; EuroImmun; F. Hoffmann-La Roche Ltd and its affiliated company Genentech, Inc.; Fujirebio; GE Healthcare; IXICO Ltd.; Janssen Alzheimer Immunotherapy Research & Development, LLC.; Johnson & Johnson Pharmaceutical Research & Development LLC.; Medpace, Inc.; Merck & Co., Inc.; Meso Scale Diagnostics, LLC.; NeuroRx Research; Neurotrack Technologies; Novartis Pharmaceuticals Corporation; Pfizer Inc.; Piramal Imaging; Servier; Synarc Inc.; and Takeda Pharmaceutical Company. The Canadian Institutes of Health Research is providing funds to support ADNI clinical sites in Canada. Private sector contributions are facilitated by the Foundation for the National Institutes of Health (www.fnih.org). The grantee organization is the Northern California Institute for Research and Education, and the study is coordinated by the Alzheimer's Disease Cooperative Study at the University of California, San Diego. ADNI data are disseminated by the Laboratory for Neuro Imaging at the University of Southern California.

One of the authors has significant statistical expertise. Institutional Review Board approval was not required because this study includes data from AddNeuroMed and ADNI, two public and available datasets for imaging research. Data collection was subject to ethical review and approval by committees from each participating centre. This study also includes data from the Memory Clinic at Karolinska University Hospital. This sample has been previously investigated and the study was approved by the Regional Ethical Review Board in Stockholm, Sweden. Written informed consent was not required for this study because this study includes data from AddNeuroMed and ADNI, two public and available datasets for imaging research. Data collection was subject to ethical review and approval by committees from each participating center. This study also includes data from the Memory Clinic at Karolinska University Hospital. This sample has been previously investigated and written informed consent was already available for all the subjects. Some study subjects or cohorts have been previously reported. Data from the AddNeuromed and the ADNI studies have been extensively used and reported. Given the amount of manuscript published using these two datasets, it is not possible to mention the number of patients previously published. This study also includes data from thirty-four patients previously investigated in the studies listed below.

- Looi et al. AJNR Am J Neuroradiol 2008

- Lindberg et al. AJNR Am J Neuroradiol 2009

- Looi et al. AJNR Am J Neuroradiol 2009

- Looi et al. Neuroimage 2010

- Looi et al. Psychiatry Res 2011

- Lindberg et al. J Alzheimers Dis 2012

- Lindberg et al. AJNR Am J Neuroradiol 2012

- Lindberg et al. Front Aging Neurosci 2012

- Walterfang et al. J Alzheimers Dis 2014

Methodology: prospective, cross sectional study, multicenter study.

Author information

Authors and Affiliations

  1. Division of Clinical Geriatrics, Center for Alzheimer Research, Department of Neurobiology, Care Sciences and Society, Karolinska Institutet, Novum, 5th floor, SE-141 86, Stockholm, Sweden

    Daniel Ferreira, Olof Lindberg, Carlos Aguilar, Lars-Olof Wahlund & Eric Westman

  2. Division of Medical Imaging and Technology, Department of Clinical Science, Intervention and Technology, Karolinska Institutet, Stockholm, Sweden

    Lena Cavallin & Tobias Granberg

  3. Department of Radiology, Karolinska University Hospital in Huddinge, Huddinge, Sweden

    Lena Cavallin & Tobias Granberg

  4. Institute of Gerontology and Geriatrics, University of Perugia, Perugia, Italy

    Patrizia Mecocci

  5. INSERM U 558, University of Toulouse, Toulouse, France

    Bruno Vellas

  6. 3rd Department of Neurology, Aristoteleion Panepistimeion Thessalonikis, Thessaloniki, Greece

    Magda Tsolaki

  7. Medical University of Lodz, Lodz, Poland

    Iwona Kłoszewska

  8. University of Eastern Finland, University Hospital of Kuopio, Kuopio, Finland

    Hilkka Soininen

  9. Department of Psychiatry, Warneford Hospital, University of Oxford, Oxford, UK

    Simon Lovestone

  10. Department of Neuroimaging, Institute of Psychiatry, King’s College London, London, UK

    Andrew Simmons

  11. NIHR Biomedical Research Centre for Mental Health, London, UK

    Andrew Simmons

  12. NIHR Biomedical Research Unit for Dementia, London, UK

    Andrew Simmons

Authors
  1. Daniel Ferreira
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  2. Lena Cavallin
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  3. Tobias Granberg
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  4. Olof Lindberg
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  5. Carlos Aguilar
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  6. Patrizia Mecocci
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  7. Bruno Vellas
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  8. Magda Tsolaki
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  9. Iwona Kłoszewska
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  10. Hilkka Soininen
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  11. Simon Lovestone
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  12. Andrew Simmons
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  13. Lars-Olof Wahlund
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  14. Eric Westman
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Consortia

for the AddNeuroMed consortium and for the Alzheimer’s Disease Neuroimaging Initiative*

Corresponding author

Correspondence to Daniel Ferreira.

Additional information

* Data used in preparation of this article were obtained from the Alzheimer’s Disease Neuroimaging Initiative (ADNI) database (adni.loni.usc.edu). As such the investigators within the ADNI contributed to the design and implementation of ADNI and/or provided data but did not participate in analysis or writing of this report. A complete listing of ADNI investigators can be found at: http://adni.loni.usc.edu/wp-content/uploads/how_to_apply/ADNI_Acknowledgement_List.pdf.

Appendix

Appendix

Fig. 5

Fig. 5
figure 5

Interaction between FTD subtype and hemisphere. GCA-F = global cerebral atrophy – frontal sub-scale; bvFTD = behavioural variant of frontotemporal dementia; SD = semantic dementia; PNFA = progressive non-fluent aphasia

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Table 6

Table 6 FreeSurfer 5.3.0 methods for cortical reconstruction and parcellation
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Table 7

Table 7 Detailed methods for manual tracing of frontal sub-regions
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Table 8

Table 8 Demographic characteristics of the three GCA-F groups
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Table 9

Table 9 Summary of significant clusters in analyses at the vertex level (AddNeuroMed + ADNI)
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Ferreira, D., Cavallin, L., Granberg, T. et al. Quantitative validation of a visual rating scale for frontal atrophy: associations with clinical status, APOE e4, CSF biomarkers and cognition. Eur Radiol 26, 2597–2610 (2016). https://doi.org/10.1007/s00330-015-4101-9

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