Beyond the Resection: Surgical White Matter Transections Structurally Alter Preserved Brain Anatomy
Poster No:
1779
Submission Type:
Abstract Submission
Authors:
Philip Pruckner1, Remika Mito2, David Vaughan3,1,4, Graeme Jackson3,1,4, Florian Fischmeister5, Karl-Heinz Nenning6, Ekaterina Pataraia7, Christoph Baumgartner8,9,10, Christian Dorfer11, Karl Rössler11, Thomas Czech11, Gregor Kasprian5, Silvia Bonelli7, Robert Smith3,1
Institutions:
1Florey Department of Neuroscience and Mental Health, The University of Melbourne, Melbourne, Victoria, Australia, 2Department of Psychiatry, The University of Melbourne, Melbourne, Victoria, Australia, 3The Florey Institute of Neuroscience and Mental Health, Melbourne, Victoria, Australia, 4Department of Neurology, Austin Health, Melbourne, Victoria, Australia, 5Department of Biomedical Imaging and Image-guided Therapy, Medical University of Vienna, Vienna, Austria, 6Center for Biomedical Imaging and Neuromodulation, Nathan Kline Institute, Orangeburg, New York, United States, 7Department of Neurology, Medical University of Vienna, Vienna, Austria, 8Department of Neurology, Clinic Hietzing, Vienna, Austria, 9Karl Landsteiner Institute for Clinical Epilepsy Research and Cognitive Neurology, Vienna, Austria, 10Medical Faculty, Sigmund Freud University, Vienna, Austria, 11Department of Neurosurgery, Medical University of Vienna, Vienna, Austria
First Author:
Philip Pruckner
Florey Department of Neuroscience and Mental Health, The University of Melbourne
Melbourne, Victoria, Australia
Florey Department of Neuroscience and Mental Health, The University of Melbourne
Melbourne, Victoria, Australia
Co-Author(s):
David Vaughan
The Florey Institute of Neuroscience and Mental Health|Florey Department of Neuroscience and Mental Health, The University of Melbourne|Department of Neurology, Austin Health
Melbourne, Victoria, Australia|Melbourne, Victoria, Australia|Melbourne, Victoria, Australia
The Florey Institute of Neuroscience and Mental Health|Florey Department of Neuroscience and Mental Health, The University of Melbourne|Department of Neurology, Austin Health
Melbourne, Victoria, Australia|Melbourne, Victoria, Australia|Melbourne, Victoria, Australia
Graeme Jackson
The Florey Institute of Neuroscience and Mental Health|Florey Department of Neuroscience and Mental Health, The University of Melbourne|Department of Neurology, Austin Health
Melbourne, Victoria, Australia|Melbourne, Victoria, Australia|Melbourne, Victoria, Australia
The Florey Institute of Neuroscience and Mental Health|Florey Department of Neuroscience and Mental Health, The University of Melbourne|Department of Neurology, Austin Health
Melbourne, Victoria, Australia|Melbourne, Victoria, Australia|Melbourne, Victoria, Australia
Florian Fischmeister
Department of Biomedical Imaging and Image-guided Therapy, Medical University of Vienna
Vienna, Austria
Department of Biomedical Imaging and Image-guided Therapy, Medical University of Vienna
Vienna, Austria
Karl-Heinz Nenning
Center for Biomedical Imaging and Neuromodulation, Nathan Kline Institute
Orangeburg, New York, United States
Center for Biomedical Imaging and Neuromodulation, Nathan Kline Institute
Orangeburg, New York, United States
Christoph Baumgartner
Department of Neurology, Clinic Hietzing|Karl Landsteiner Institute for Clinical Epilepsy Research and Cognitive Neurology|Medical Faculty, Sigmund Freud University
Vienna, Austria|Vienna, Austria|Vienna, Austria
Department of Neurology, Clinic Hietzing|Karl Landsteiner Institute for Clinical Epilepsy Research and Cognitive Neurology|Medical Faculty, Sigmund Freud University
Vienna, Austria|Vienna, Austria|Vienna, Austria
Gregor Kasprian
Department of Biomedical Imaging and Image-guided Therapy, Medical University of Vienna
Vienna, Austria
Department of Biomedical Imaging and Image-guided Therapy, Medical University of Vienna
Vienna, Austria
Robert Smith
The Florey Institute of Neuroscience and Mental Health|Florey Department of Neuroscience and Mental Health, The University of Melbourne
Melbourne, Victoria, Australia|Melbourne, Victoria, Australia
The Florey Institute of Neuroscience and Mental Health|Florey Department of Neuroscience and Mental Health, The University of Melbourne
Melbourne, Victoria, Australia|Melbourne, Victoria, Australia
Introduction:
Resective neurosurgery is a cornerstone treatment for various neurological conditions. While traditionally regarded as a localized intervention, emerging neuroimaging evidence shows that it also structurally changes the non-resected brain(Arnold et al., 2023; Leiberg et al., 2023; McDonald et al., 2010). The relationship between local tissue removal and these downstream anatomical changes however remains poorly understood. In this study, we investigate the hypothesis that postsurgical changes to preserved grey and white matter are mediated by transneuronal degeneration(Cowan, 1970) - a process where neuronal populations deteriorate due to the loss of axonal input (Fig. 1A).
·Figure 1
Methods:
We studied a surgical epilepsy case series of 60 patients who underwent either anterior temporal lobectomy (ATL, n=32) or selective amygdalohippocampectomy (SAHE, n=28). All procedures were performed by the same experienced surgeon at the Medical University of Vienna(Pruckner et al., 2023). Using a longitudinal imaging framework specifically tailored for robust analysis of diffusion-weighted and T1-weighted MRI data with gross resections, we mapped three key aspects of transneuronal degeneration for anatomical brain regions(Desikan et al., 2006): 1) The surgical transection of white matter; 2) the longitudinal change in cortical thickness; 3) the longitudinal connectivity change of non-transected white matter (see Fig. 1B). Using mixed linear effects models, we explored the relationships between fibre transections and downstream anatomical changes, characterizing the sequential progression of transneuronal degeneration along grey and white matter. Data from both treatment groups were pooled for this analysis, encompassing 2767 and 2434 brain regions, respectively (Fig. 1C).
Results:
Both ATL and SAHE resulted in extensive white matter transections (Fig. 2A), predominately affecting ipsilateral regions and most pronounced close to the resection site (Fig. 2B). Similarly, we found postsurgical atrophy to be most pronounced in proximity of resection (Fig 2C). Regression analysis confirmed a relationship between white matter transection and cortical atrophy, with every 10-fold increase of white matter transection corresponding to a 3% decrease in cortical thickness (R2=32%, p<0.0001; Fig. 2E). We also found widespread decreases in downstream connectivity mostly across the ipsilateral hemisphere (Fig. 2D). Regression analysis demonstrated a close association of downstream connectivity changes with white matter transection, with every 10-fold transection increase corresponding to a 7% decrease in connectivity (R2=58%, p<0.0001; Fig 2E).
·Figure 2
Conclusions:
The presented results demonstrate that structural effects of brain surgery extend beyond the immediate site of resection. Our transneuronal degeneration model attributes postsurgical changes as consequences of white matter transection, revealing a multi-synaptic network effect of resective brain surgery. Anatomical changes were well-described by our parsimonious quantitative longitudinal imaging pipeline, underscoring the potential of connectome-based predictive modelling to anticipate postsurgical changes prior to surgery. Beyond its clinical implications, the study is the first to provide empirical in vivo evidence of brain-wide transneuronal degeneration in the absence of pathological proteins, supporting leading theories of connectomic disease spread(Fornito et al., 2015).
Modeling and Analysis Methods:
Connectivity (eg. functional, effective, structural)
Diffusion MRI Modeling and Analysis
Neuroanatomy, Physiology, Metabolism and Neurotransmission:
Cortical Anatomy and Brain Mapping 2
White Matter Anatomy, Fiber Pathways and Connectivity 1
Keywords:
Cortex
Epilepsy
Neurological
STRUCTURAL MRI
Tractography
White Matter
WHITE MATTER IMAGING - DTI, HARDI, DSI, ETC
Other - Neurosurgery
1|2Indicates the priority used for review
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2. Cowan, W. M. (1970). Anterograde and retrograde transneuronal degeneration in the central and peripheral nervous system. In W. J. H. Nauta & S. O. E. Ebbesson (Eds.), Contemporary research methods in neuroanatomy (pp. 217–251). Springer Berlin Heidelberg.
3. Desikan, R. S. (2006). An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral-based regions of interest. NeuroImage, 31(3), 968–980.
4. Fornito, A. (2015). The connectomics of brain disorders. Nature Reviews Neuroscience, 16(3), 159–172.
5. Leiberg, K. (2023). Effects of anterior temporal lobe resection on cortical morphology. Cortex, 166, 233–242.
6. McDonald, C. R. (2010). Changes in fiber tract integrity and visual fields after anterior temporal lobectomy. Neurology, 75(18), 1631–1638.
7. Pruckner, P. (2023). Visual outcomes after anterior temporal lobectomy and transsylvian selective amygdalohippocampectomy: A quantitative comparison of clinical and diffusion data. Epilepsia, 64(3), 705–717.