Topographic divergence of atypical cortical asymmetry and atrophy patterns in temporal lobe epilepsy

Bo-Yong Park^{1

2

3}, Sara Larivière¹, Raul Rodríguez-Cruces¹, Jessica Royer¹, Shahin Tavakol¹, Yezhou Wang¹, Lorenzo Caciagli^{4

5

6}, Maria Eugenia Caligiuri⁷, Antonio Gambardella^{7

8}, Luis Concha⁹, Simon S Keller^{10

11}, Fernando Cendes¹², Marina K M Alvim¹², Clarissa Yasuda¹², Leonardo Bonilha¹³, Ezequiel Gleichgerrcht¹⁴, Niels K Focke¹⁵, Barbara A K Kreilkamp¹⁵, Martin Domin¹⁶, Felix von Podewils¹⁷, Soenke Langner¹⁸, Christian Rummel¹⁹, Michael Rebsamen¹⁹, Roland Wiest¹⁹, Pascal Martin²⁰, Raviteja Kotikalapudi^{20

21}, Benjamin Bender²¹, Terence J O'Brien^{22

23}, Meng Law²², Benjamin Sinclair^{22

23}, Lucy Vivash^{22

23}, Patrick Kwan^{22

23}, Patricia M Desmond²⁴, Charles B Malpas²³, Elaine Lui²⁴, Saud Alhusaini^{25

26}, Colin P Doherty^{27

28}, Gianpiero L Cavalleri^{25

28}, Norman Delanty^{25

28}, Reetta Kälviäinen^{29

30}, Graeme D Jackson³¹, Magdalena Kowalczyk³¹, Mario Mascalchi³², Mira Semmelroch³¹, Rhys H Thomas³³, Hamid Soltanian-Zadeh^{34

35}, Esmaeil Davoodi-Bojd³⁶, Junsong Zhang³⁷, Matteo Lenge^{38

39}, Renzo Guerrini³⁸, Emanuele Bartolini⁴⁰, Khalid Hamandi^{41

42}, Sonya Foley⁴¹, Bernd Weber⁴³, Chantal Depondt⁴⁴, Julie Absil⁴⁵, Sarah J A Carr⁴⁶, Eugenio Abela⁴⁶, Mark P Richardson⁴⁶, Orrin Devinsky⁴⁷, Mariasavina Severino^{48

49}, Pasquale Striano^{48

49}, Costanza Parodi^{48

49}, Domenico Tortora^{48

49}, Sean N Hatton⁵⁰, Sjoerd B Vos^{4

5

51}, John S Duncan^{4

5}, Marian Galovic^{4

5

52}, Christopher D Whelan⁵³, Núria Bargalló^{54

55}, Jose Pariente⁵⁴, Estefania Conde-Blanco⁵⁶, Anna Elisabetta Vaudano^{57

58}, Manuela Tondelli^{57

58}, Stefano Meletti^{57

58}, Xiang-Zhen Kong^{59

60}, Clyde Francks^{59

61}, Simon E Fisher^{59

61}, Benoit Caldairou⁶², Mina Ryten^{63

64

65}, Angelo Labate⁶⁶, Sanjay M Sisodiya^{4

5}, Paul M Thompson⁶⁷, Carrie R McDonald⁶⁸, Andrea Bernasconi⁶², Neda Bernasconi⁶², Boris C Bernhardt¹

Affiliations

¹ Multimodal Imaging and Connectome Analysis Laboratory, McConnell Brain Imaging Centre, Montreal Neurological Institute and Hospital, McGill University, Montreal, QC, Canada.
² Department of Data Science, Inha University, Incheon, Republic of Korea.
³ Center for Neuroscience Imaging Research, Institute for Basic Science, Suwon, Republic of Korea.
⁴ Department of Clinical and Experimental Epilepsy, UCL Queen Square Institute of Neurology, London, UK.
⁵ MRI Unit, Epilepsy Society, Chalfont St Peter, Buckinghamshire, UK.
⁶ Department of Bioengineering, University of Pennsylvania, Philadelphia, PA, USA.
⁷ Neuroscience Research Center, University Magna Græcia, Catanzaro, CZ, Italy.
⁸ Institute of Neurology, University Magna Græcia, Catanzaro, CZ, Italy.
⁹ Institute of Neurobiology, Universidad Nacional Autónoma de México, Querétaro, México.
¹⁰ Institute of Systems, Molecular and Integrative Biology, University of Liverpool, Liverpool, UK.
¹¹ Walton Centre NHS Foundation Trust, Liverpool, UK.
¹² Department of Neurology, University of Campinas-UNICAMP, Campinas, São Paulo, Brazil.
¹³ Department of Neurology, Emory University, Atlanta, GA, USA.
¹⁴ Department of Neurology, Medical University of South Carolina, Charleston, SC, USA.
¹⁵ Department of Neurology, University Medical Center Göttingen, Göttingen, Germany.
¹⁶ Institute of Diagnostic Radiology and Neuroradiology, Functional Imaging Unit, University Medicine Greifswald, Greifswald, Germany.
¹⁷ Department of Neurology, University Medicine Greifswald, Greifswald, Germany.
¹⁸ Institute of Diagnostic Radiology and Neuroradiology, University Medicine Greifswald, Greifswald, Germany.
¹⁹ Support Center for Advanced Neuroimaging (SCAN), University Institute of Diagnostic and Interventional Neuroradiology, University Hospital Bern, Bern, Switzerland.
²⁰ Department of Neurology and Epileptology, Hertie Institute for Clinical Brain Research, University of Tübingen, Tübingen, Germany.
²¹ Department of Radiology, Diagnostic and Interventional Neuroradiology, University Hospital Tübingen, Tübingen, Germany.
²² Department of Neuroscience, Central Clinical School, Alfred Hospital, Monash University, Melbourne, Victoria, Australia.
²³ Departments of Medicine, The Royal Melbourne Hospital, The University of Melbourne, Parkville, Victoria, Australia.
²⁴ Department of Radiology, The Royal Melbourne Hospital, The University of Melbourne, Parkville, Victoria, Australia.
²⁵ Department of Molecular and Cellular Therapeutics, The Royal College of Surgeons in Ireland, Dublin, Ireland.
²⁶ Department of Neurology, Yale University School of Medicine, New Haven, CT, USA.
²⁷ Department of Neurology, St James' Hospital, Dublin, Ireland.
²⁸ FutureNeuro SFI Research Centre, Dublin, Ireland.
²⁹ Epilepsy Center, Neuro Center, Kuopio University Hospital, Member of the European Reference Network for Rare and Complex Epilepsies EpiCARE, Kuopio, Finland.
³⁰ Faculty of Health Sciences, School of Medicine, Institute of Clinical Medicine, University of Eastern Finland, Kuopio, Finland.
³¹ Florey Institute of Neuroscience and Mental Health, University of Melbourne, Melbourne, Victoria, 3010, Australia.
³² Neuroradiology Research Program, Meyer Children Hospital of Florence, University of Florence, Florence, Italy.
³³ Transitional and Clinical Research Institute, Newcastle University, Newcastle upon Tyne, UK.
³⁴ Control and Intelligent Processing Center of Excellence (CIPCE), School of Electrical and Computer Engineering, University of Tehran, Tehran, Iran.
³⁵ Departments of Research Administration and Radiology, Henry Ford Health System, Detroit, MI, USA.
³⁶ Department of Neurology, Henry Ford Health System, Detroit, MI, USA.
³⁷ Department of Artificial Intelligence, Xiamen University, Xiamen, China.
³⁸ Child Neurology Unit and Laboratories, Neuroscience Department, Children's Hospital A. Meyer-University of Florence, Florence, Italy.
³⁹ Functional and Epilepsy Neurosurgery Unit, Neurosurgery Department, Children's Hospital A. Meyer-University of Florence, Florence, Italy.
⁴⁰ USL Centro Toscana, Neurology Unit, Nuovo Ospedale Santo Stefano, Prato, Italy.
⁴¹ Cardiff University Brain Research Imaging Centre (CUBRIC), College of Biomedical Sciences, Cardiff University, Cardiff, UK.
⁴² The Welsh Epilepsy Unit, Department of Neurology, University Hospital of Wales, Cardiff, UK.
⁴³ Institute of Experimental Epileptology and Cognition Research, University Hospital Bonn, Bonn, Germany.
⁴⁴ Department of Neurology, Hôpital Erasme, Université Libre de Bruxelles, Brussels, Belgium.
⁴⁵ Department of Radiology, Hôpital Erasme, Université Libre de Bruxelles, Brussels, Belgium.
⁴⁶ Division of Neuroscience, Institute of Psychiatry, Psychology and Neuroscience, King's College London, UK.
⁴⁷ Department of Neurology, NYU Grossman School of Medicine, New York, NY, USA.
⁴⁸ IRCCS Istituto Giannina Gaslini, Genova, Italy.
⁴⁹ Department of Neurosciences, Rehabilitation, Ophthalmology, Genetics, Maternal and Child Health, University of Genova, Genova, Italy.
⁵⁰ Department of Neurosciences, Center for Multimodal Imaging and Genetics, University of California San Diego, La Jolla, CA, USA.
⁵¹ Centre for Medical Image Computing, University College London, London, UK.
⁵² Department of Neurology, Clinical Neuroscience Center, University Hospital and University of Zurich, Zurich, Switzerland.
⁵³ Department of Molecular and Cellular Therapeutics, The Royal College of Surgeons in Ireland, Dublin, Ireland.
⁵⁴ Magnetic Resonance Image Core Facility, Institut d'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Barcelona, Spain.
⁵⁵ Department of Radiology CDIC, Hospital Clinic Barcelona, Barcelona, Spain.
⁵⁶ Epilepsy Unit, Department of Neurology, Hospital Clínic, Barcelona, Spain.
⁵⁷ Neurology Unit, Azienda Ospedaliero-Universitaria of Modena, OCB Hospital, Modena, Italy.
⁵⁸ Department of Biomedical, Metabolic, and Neural Sciences, Center for Neuroscience and Neurotechnology, University of Modena and Reggio Emilia, Modena, Italy.
⁵⁹ Language and Genetics Department, Max Planck Institute for Psycholinguistics, Nijmegen, The Netherlands.
⁶⁰ Department of Psychology and Behavioral Sciences, Zhejiang University, Hangzhou, China.
⁶¹ Donders Institute for Brain, Cognition and Behaviour, Radboud University, Nijmegen, The Netherlands.
⁶² Neuroimaging of Epilepsy Laboratory, McConnell Brain Imaging Centre, Montreal Neurological Institute and Hospital, McGill University, Montreal, QC, Canada.
⁶³ Department of Neurodegenerative Disease, Queen Square Institute of Neurology, University College London, London, UK.
⁶⁴ NIHR Great Ormond Street Hospital Biomedical Research Centre, University College London, London, UK.
⁶⁵ Department of Genetics and Genomic Medicine, Great Ormond Street Institute of Child Health, University College London, London, UK.
⁶⁶ Neurology, BIOMORF Department, University of Messina, Messina, Italy.
⁶⁷ Imaging Genetics Center, Mark & Mary Stevens Institute for Neuroimaging and Informatics, USC Keck School of Medicine, Los Angeles, CA, USA.
⁶⁸ Department of Psychiatry, Center for Multimodal Imaging and Genetics, University of California San Diego, La Jolla, CA, USA.

PMID: 35333312
PMCID: PMC9128824
DOI: 10.1093/brain/awab417

Topographic divergence of atypical cortical asymmetry and atrophy patterns in temporal lobe epilepsy

Bo-Yong Park et al. Brain. 2022.

. 2022 May 24;145(4):1285-1298.

doi: 10.1093/brain/awab417.

Authors

Affiliations

¹ Multimodal Imaging and Connectome Analysis Laboratory, McConnell Brain Imaging Centre, Montreal Neurological Institute and Hospital, McGill University, Montreal, QC, Canada.
² Department of Data Science, Inha University, Incheon, Republic of Korea.
³ Center for Neuroscience Imaging Research, Institute for Basic Science, Suwon, Republic of Korea.
⁴ Department of Clinical and Experimental Epilepsy, UCL Queen Square Institute of Neurology, London, UK.
⁵ MRI Unit, Epilepsy Society, Chalfont St Peter, Buckinghamshire, UK.
⁶ Department of Bioengineering, University of Pennsylvania, Philadelphia, PA, USA.
⁷ Neuroscience Research Center, University Magna Græcia, Catanzaro, CZ, Italy.
⁸ Institute of Neurology, University Magna Græcia, Catanzaro, CZ, Italy.
⁹ Institute of Neurobiology, Universidad Nacional Autónoma de México, Querétaro, México.
¹⁰ Institute of Systems, Molecular and Integrative Biology, University of Liverpool, Liverpool, UK.
¹¹ Walton Centre NHS Foundation Trust, Liverpool, UK.
¹² Department of Neurology, University of Campinas-UNICAMP, Campinas, São Paulo, Brazil.
¹³ Department of Neurology, Emory University, Atlanta, GA, USA.
¹⁴ Department of Neurology, Medical University of South Carolina, Charleston, SC, USA.
¹⁵ Department of Neurology, University Medical Center Göttingen, Göttingen, Germany.
¹⁶ Institute of Diagnostic Radiology and Neuroradiology, Functional Imaging Unit, University Medicine Greifswald, Greifswald, Germany.
¹⁷ Department of Neurology, University Medicine Greifswald, Greifswald, Germany.
¹⁸ Institute of Diagnostic Radiology and Neuroradiology, University Medicine Greifswald, Greifswald, Germany.
¹⁹ Support Center for Advanced Neuroimaging (SCAN), University Institute of Diagnostic and Interventional Neuroradiology, University Hospital Bern, Bern, Switzerland.
²⁰ Department of Neurology and Epileptology, Hertie Institute for Clinical Brain Research, University of Tübingen, Tübingen, Germany.
²¹ Department of Radiology, Diagnostic and Interventional Neuroradiology, University Hospital Tübingen, Tübingen, Germany.
²² Department of Neuroscience, Central Clinical School, Alfred Hospital, Monash University, Melbourne, Victoria, Australia.
²³ Departments of Medicine, The Royal Melbourne Hospital, The University of Melbourne, Parkville, Victoria, Australia.
²⁴ Department of Radiology, The Royal Melbourne Hospital, The University of Melbourne, Parkville, Victoria, Australia.
²⁵ Department of Molecular and Cellular Therapeutics, The Royal College of Surgeons in Ireland, Dublin, Ireland.
²⁶ Department of Neurology, Yale University School of Medicine, New Haven, CT, USA.
²⁷ Department of Neurology, St James' Hospital, Dublin, Ireland.
²⁸ FutureNeuro SFI Research Centre, Dublin, Ireland.
²⁹ Epilepsy Center, Neuro Center, Kuopio University Hospital, Member of the European Reference Network for Rare and Complex Epilepsies EpiCARE, Kuopio, Finland.
³⁰ Faculty of Health Sciences, School of Medicine, Institute of Clinical Medicine, University of Eastern Finland, Kuopio, Finland.
³¹ Florey Institute of Neuroscience and Mental Health, University of Melbourne, Melbourne, Victoria, 3010, Australia.
³² Neuroradiology Research Program, Meyer Children Hospital of Florence, University of Florence, Florence, Italy.
³³ Transitional and Clinical Research Institute, Newcastle University, Newcastle upon Tyne, UK.
³⁴ Control and Intelligent Processing Center of Excellence (CIPCE), School of Electrical and Computer Engineering, University of Tehran, Tehran, Iran.
³⁵ Departments of Research Administration and Radiology, Henry Ford Health System, Detroit, MI, USA.
³⁶ Department of Neurology, Henry Ford Health System, Detroit, MI, USA.
³⁷ Department of Artificial Intelligence, Xiamen University, Xiamen, China.
³⁸ Child Neurology Unit and Laboratories, Neuroscience Department, Children's Hospital A. Meyer-University of Florence, Florence, Italy.
³⁹ Functional and Epilepsy Neurosurgery Unit, Neurosurgery Department, Children's Hospital A. Meyer-University of Florence, Florence, Italy.
⁴⁰ USL Centro Toscana, Neurology Unit, Nuovo Ospedale Santo Stefano, Prato, Italy.
⁴¹ Cardiff University Brain Research Imaging Centre (CUBRIC), College of Biomedical Sciences, Cardiff University, Cardiff, UK.
⁴² The Welsh Epilepsy Unit, Department of Neurology, University Hospital of Wales, Cardiff, UK.
⁴³ Institute of Experimental Epileptology and Cognition Research, University Hospital Bonn, Bonn, Germany.
⁴⁴ Department of Neurology, Hôpital Erasme, Université Libre de Bruxelles, Brussels, Belgium.
⁴⁵ Department of Radiology, Hôpital Erasme, Université Libre de Bruxelles, Brussels, Belgium.
⁴⁶ Division of Neuroscience, Institute of Psychiatry, Psychology and Neuroscience, King's College London, UK.
⁴⁷ Department of Neurology, NYU Grossman School of Medicine, New York, NY, USA.
⁴⁸ IRCCS Istituto Giannina Gaslini, Genova, Italy.
⁴⁹ Department of Neurosciences, Rehabilitation, Ophthalmology, Genetics, Maternal and Child Health, University of Genova, Genova, Italy.
⁵⁰ Department of Neurosciences, Center for Multimodal Imaging and Genetics, University of California San Diego, La Jolla, CA, USA.
⁵¹ Centre for Medical Image Computing, University College London, London, UK.
⁵² Department of Neurology, Clinical Neuroscience Center, University Hospital and University of Zurich, Zurich, Switzerland.
⁵³ Department of Molecular and Cellular Therapeutics, The Royal College of Surgeons in Ireland, Dublin, Ireland.
⁵⁴ Magnetic Resonance Image Core Facility, Institut d'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Barcelona, Spain.
⁵⁵ Department of Radiology CDIC, Hospital Clinic Barcelona, Barcelona, Spain.
⁵⁶ Epilepsy Unit, Department of Neurology, Hospital Clínic, Barcelona, Spain.
⁵⁷ Neurology Unit, Azienda Ospedaliero-Universitaria of Modena, OCB Hospital, Modena, Italy.
⁵⁸ Department of Biomedical, Metabolic, and Neural Sciences, Center for Neuroscience and Neurotechnology, University of Modena and Reggio Emilia, Modena, Italy.
⁵⁹ Language and Genetics Department, Max Planck Institute for Psycholinguistics, Nijmegen, The Netherlands.
⁶⁰ Department of Psychology and Behavioral Sciences, Zhejiang University, Hangzhou, China.
⁶¹ Donders Institute for Brain, Cognition and Behaviour, Radboud University, Nijmegen, The Netherlands.
⁶² Neuroimaging of Epilepsy Laboratory, McConnell Brain Imaging Centre, Montreal Neurological Institute and Hospital, McGill University, Montreal, QC, Canada.
⁶³ Department of Neurodegenerative Disease, Queen Square Institute of Neurology, University College London, London, UK.
⁶⁴ NIHR Great Ormond Street Hospital Biomedical Research Centre, University College London, London, UK.
⁶⁵ Department of Genetics and Genomic Medicine, Great Ormond Street Institute of Child Health, University College London, London, UK.
⁶⁶ Neurology, BIOMORF Department, University of Messina, Messina, Italy.
⁶⁷ Imaging Genetics Center, Mark & Mary Stevens Institute for Neuroimaging and Informatics, USC Keck School of Medicine, Los Angeles, CA, USA.
⁶⁸ Department of Psychiatry, Center for Multimodal Imaging and Genetics, University of California San Diego, La Jolla, CA, USA.

PMID: 35333312
PMCID: PMC9128824
DOI: 10.1093/brain/awab417

Abstract

Temporal lobe epilepsy, a common drug-resistant epilepsy in adults, is primarily a limbic network disorder associated with predominant unilateral hippocampal pathology. Structural MRI has provided an in vivo window into whole-brain grey matter structural alterations in temporal lobe epilepsy relative to controls, by either mapping (i) atypical inter-hemispheric asymmetry; or (ii) regional atrophy. However, similarities and differences of both atypical asymmetry and regional atrophy measures have not been systematically investigated. Here, we addressed this gap using the multisite ENIGMA-Epilepsy dataset comprising MRI brain morphological measures in 732 temporal lobe epilepsy patients and 1418 healthy controls. We compared spatial distributions of grey matter asymmetry and atrophy in temporal lobe epilepsy, contextualized their topographies relative to spatial gradients in cortical microstructure and functional connectivity calculated using 207 healthy controls obtained from Human Connectome Project and an independent dataset containing 23 temporal lobe epilepsy patients and 53 healthy controls and examined clinical associations using machine learning. We identified a marked divergence in the spatial distribution of atypical inter-hemispheric asymmetry and regional atrophy mapping. The former revealed a temporo-limbic disease signature while the latter showed diffuse and bilateral patterns. Our findings were robust across individual sites and patients. Cortical atrophy was significantly correlated with disease duration and age at seizure onset, while degrees of asymmetry did not show a significant relationship to these clinical variables. Our findings highlight that the mapping of atypical inter-hemispheric asymmetry and regional atrophy tap into two complementary aspects of temporal lobe epilepsy-related pathology, with the former revealing primary substrates in ipsilateral limbic circuits and the latter capturing bilateral disease effects. These findings refine our notion of the neuropathology of temporal lobe epilepsy and may inform future discovery and validation of complementary MRI biomarkers in temporal lobe epilepsy.

Keywords: asymmetry; cortical thickness; gradients; multi-site; temporal lobe epilepsy.

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Figures

**Figure 1**
**Topography of atypical cortical asymmetry and atrophy patterns in TLE.** (A) Atypical inter-hemispheric asymmetry of cortical thickness and regional cortical atrophy between individuals with TLE relative to controls, calculated using ENIGMA-Epilepsy dataset. Blue regions indicate significant ipsilateral versus contralateral cortical thickness asymmetry/atrophy in TLE relative to controls. Patient hemispheres are sorted into ipsilateral/contralateral to the seizure focus. (B) Effects (i.e. asymmetry index and cortical thickness) are stratified according to seven intrinsic functional communities and major lobes. (C) Associations between epilepsy-related findings and microstructural/functional gradients calculated using HCP dataset. Cortex-wide microstructural profile similarity matrix and scree plot describing connectome variance after identification of principal eigenvectors are shown. The first principal eigenvector (microstructural gradient) is shown on the cortical surface. Spatial correlations between the principal microstructural gradient and TLE-related effects (i.e. atypical cortical asymmetry and atrophy) are reported with scatter plots. (D) Identical analysis to C but based on functional gradients. Cing = cingulate; DAN = dorsal attention network; DMN = default mode network; FPN = frontoparietal control network; Front = frontal; Ins = insular; LBN = limbic network; Occ = occipital; Par = parietal; SMN = somatomotor network; Temp = temporal; VAN = ventral attention network; VN = visual network.

**Figure 2**
**Consistency of atypical cortical asymmetry and atrophy.** (A) World map of data acquisition sites. (B) Spatial correlations between topographic gradients and atypical cortical asymmetry/atrophy patterns of all sites. (C) Schema describing the computation of patient-wise consistency probability. The number of patients with large deviations of cortical features (i.e. atypical inter-hemispheric asymmetry or regional cortical atrophy) was counted. (D) Consistency probability of atypical cortical asymmetry and atrophy. (E) Spatial correlations between consistency probability and topographic gradients.

**Figure 3**
**Associations between cortical features and clinical variables.** (A) Probability of regions being selected across 5-fold nested cross-validation and 100 repetitions for predicting duration of epilepsy using atypical asymmetry index (*left*) and regional atrophy (*right*). Correlations between actual and predicted values of epilepsy duration are reported in the scatter plots. Black lines indicate the mean correlation and grey lines represent the 95% CI for 100 iterations with different training/test datasets. (B) Linear correlations between gradients and selected probability. (C) Spatial correlations between duration of epilepsy and atypical asymmetry index (*left*), as well as cortical atrophy (*right*) in highly probable (selected probability > 0.5) regions. (D–F) Identical analysis to **A–C**, but with respect to age at seizure onset. MAE = mean absolute error.

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References

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Topographic divergence of atypical cortical asymmetry and atrophy patterns in temporal lobe epilepsy

Affiliations

Topographic divergence of atypical cortical asymmetry and atrophy patterns in temporal lobe epilepsy

Authors

Affiliations

Abstract

Figures

References

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Grants and funding

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Full Text Sources