Uncovering precision phenotype-biomarker associations in traumatic brain injury using topological data analysis.

<h4>Background</h4>Traumatic brain injury (TBI) is a complex disorder that is traditionally stratified based on clinical signs and symptoms. Recent imaging and molecular biomarker innovations provide unprecedented opportunities for improved TBI precision medicine, incorporating patho-ana...

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Main Authors: Jessica L Nielson, Shelly R Cooper, John K Yue, Marco D Sorani, Tomoo Inoue, Esther L Yuh, Pratik Mukherjee, Tanya C Petrossian, Jesse Paquette, Pek Y Lum, Gunnar E Carlsson, Mary J Vassar, Hester F Lingsma, Wayne A Gordon, Alex B Valadka, David O Okonkwo, Geoffrey T Manley, Adam R Ferguson, TRACK-TBI Investigators
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2017-01-01
Series:PLoS ONE
Online Access:https://doi.org/10.1371/journal.pone.0169490
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author Jessica L Nielson
Shelly R Cooper
John K Yue
Marco D Sorani
Tomoo Inoue
Esther L Yuh
Pratik Mukherjee
Tanya C Petrossian
Jesse Paquette
Pek Y Lum
Gunnar E Carlsson
Mary J Vassar
Hester F Lingsma
Wayne A Gordon
Alex B Valadka
David O Okonkwo
Geoffrey T Manley
Adam R Ferguson
TRACK-TBI Investigators
author_facet Jessica L Nielson
Shelly R Cooper
John K Yue
Marco D Sorani
Tomoo Inoue
Esther L Yuh
Pratik Mukherjee
Tanya C Petrossian
Jesse Paquette
Pek Y Lum
Gunnar E Carlsson
Mary J Vassar
Hester F Lingsma
Wayne A Gordon
Alex B Valadka
David O Okonkwo
Geoffrey T Manley
Adam R Ferguson
TRACK-TBI Investigators
author_sort Jessica L Nielson
collection DOAJ
description <h4>Background</h4>Traumatic brain injury (TBI) is a complex disorder that is traditionally stratified based on clinical signs and symptoms. Recent imaging and molecular biomarker innovations provide unprecedented opportunities for improved TBI precision medicine, incorporating patho-anatomical and molecular mechanisms. Complete integration of these diverse data for TBI diagnosis and patient stratification remains an unmet challenge.<h4>Methods and findings</h4>The Transforming Research and Clinical Knowledge in Traumatic Brain Injury (TRACK-TBI) Pilot multicenter study enrolled 586 acute TBI patients and collected diverse common data elements (TBI-CDEs) across the study population, including imaging, genetics, and clinical outcomes. We then applied topology-based data-driven discovery to identify natural subgroups of patients, based on the TBI-CDEs collected. Our hypothesis was two-fold: 1) A machine learning tool known as topological data analysis (TDA) would reveal data-driven patterns in patient outcomes to identify candidate biomarkers of recovery, and 2) TDA-identified biomarkers would significantly predict patient outcome recovery after TBI using more traditional methods of univariate statistical tests. TDA algorithms organized and mapped the data of TBI patients in multidimensional space, identifying a subset of mild TBI patients with a specific multivariate phenotype associated with unfavorable outcome at 3 and 6 months after injury. Further analyses revealed that this patient subset had high rates of post-traumatic stress disorder (PTSD), and enrichment in several distinct genetic polymorphisms associated with cellular responses to stress and DNA damage (PARP1), and in striatal dopamine processing (ANKK1, COMT, DRD2).<h4>Conclusions</h4>TDA identified a unique diagnostic subgroup of patients with unfavorable outcome after mild TBI that were significantly predicted by the presence of specific genetic polymorphisms. Machine learning methods such as TDA may provide a robust method for patient stratification and treatment planning targeting identified biomarkers in future clinical trials in TBI patients.<h4>Trial registration</h4>ClinicalTrials.gov Identifier NCT01565551.
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spelling doaj-art-957f8e379b09490ea552d3058dddc1162025-08-20T02:20:41ZengPublic Library of Science (PLoS)PLoS ONE1932-62032017-01-01123e016949010.1371/journal.pone.0169490Uncovering precision phenotype-biomarker associations in traumatic brain injury using topological data analysis.Jessica L NielsonShelly R CooperJohn K YueMarco D SoraniTomoo InoueEsther L YuhPratik MukherjeeTanya C PetrossianJesse PaquettePek Y LumGunnar E CarlssonMary J VassarHester F LingsmaWayne A GordonAlex B ValadkaDavid O OkonkwoGeoffrey T ManleyAdam R FergusonTRACK-TBI Investigators<h4>Background</h4>Traumatic brain injury (TBI) is a complex disorder that is traditionally stratified based on clinical signs and symptoms. Recent imaging and molecular biomarker innovations provide unprecedented opportunities for improved TBI precision medicine, incorporating patho-anatomical and molecular mechanisms. Complete integration of these diverse data for TBI diagnosis and patient stratification remains an unmet challenge.<h4>Methods and findings</h4>The Transforming Research and Clinical Knowledge in Traumatic Brain Injury (TRACK-TBI) Pilot multicenter study enrolled 586 acute TBI patients and collected diverse common data elements (TBI-CDEs) across the study population, including imaging, genetics, and clinical outcomes. We then applied topology-based data-driven discovery to identify natural subgroups of patients, based on the TBI-CDEs collected. Our hypothesis was two-fold: 1) A machine learning tool known as topological data analysis (TDA) would reveal data-driven patterns in patient outcomes to identify candidate biomarkers of recovery, and 2) TDA-identified biomarkers would significantly predict patient outcome recovery after TBI using more traditional methods of univariate statistical tests. TDA algorithms organized and mapped the data of TBI patients in multidimensional space, identifying a subset of mild TBI patients with a specific multivariate phenotype associated with unfavorable outcome at 3 and 6 months after injury. Further analyses revealed that this patient subset had high rates of post-traumatic stress disorder (PTSD), and enrichment in several distinct genetic polymorphisms associated with cellular responses to stress and DNA damage (PARP1), and in striatal dopamine processing (ANKK1, COMT, DRD2).<h4>Conclusions</h4>TDA identified a unique diagnostic subgroup of patients with unfavorable outcome after mild TBI that were significantly predicted by the presence of specific genetic polymorphisms. Machine learning methods such as TDA may provide a robust method for patient stratification and treatment planning targeting identified biomarkers in future clinical trials in TBI patients.<h4>Trial registration</h4>ClinicalTrials.gov Identifier NCT01565551.https://doi.org/10.1371/journal.pone.0169490
spellingShingle Jessica L Nielson
Shelly R Cooper
John K Yue
Marco D Sorani
Tomoo Inoue
Esther L Yuh
Pratik Mukherjee
Tanya C Petrossian
Jesse Paquette
Pek Y Lum
Gunnar E Carlsson
Mary J Vassar
Hester F Lingsma
Wayne A Gordon
Alex B Valadka
David O Okonkwo
Geoffrey T Manley
Adam R Ferguson
TRACK-TBI Investigators
Uncovering precision phenotype-biomarker associations in traumatic brain injury using topological data analysis.
PLoS ONE
title Uncovering precision phenotype-biomarker associations in traumatic brain injury using topological data analysis.
title_full Uncovering precision phenotype-biomarker associations in traumatic brain injury using topological data analysis.
title_fullStr Uncovering precision phenotype-biomarker associations in traumatic brain injury using topological data analysis.
title_full_unstemmed Uncovering precision phenotype-biomarker associations in traumatic brain injury using topological data analysis.
title_short Uncovering precision phenotype-biomarker associations in traumatic brain injury using topological data analysis.
title_sort uncovering precision phenotype biomarker associations in traumatic brain injury using topological data analysis
url https://doi.org/10.1371/journal.pone.0169490
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