Exploring serum glycome patterns after moderate to severe traumatic brain injury: A prospective pilot study

BackgroundGlycans play essential functional roles in the nervous system and their pathobiological relevance has become increasingly recognized in numerous brain disorders, but not fully explored in traumatic brain injury (TBI). We investigated longitudinal glycome patterns in patients with moderate...

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Main Author: Stefania, Mondello (author)
Other Authors: Sandner, Viktor (author), Goli, Mona (author), Czeiter, Endre (author), Amrein, Krisztina (author), Kochanek, Patrick M. (author), Gautam, Sakshi (author), Cho, Byeong Gwan (author), Morgan, Ryan (author), Nehme, Ali (author), Fiumara, Giacomo (author), Eid, Ali H. (author), Barsa, Chloe (author), Haidar, Muhammad Ali (author), Buki, Andras (author), Kobeissy, Firas H. (author), Mechref, Yehia (author)
Format: article
Published: 2022
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Online Access:http://dx.doi.org/10.1016/j.eclinm.2022.101494
https://www.sciencedirect.com/science/article/pii/S2589537022002243
http://hdl.handle.net/10576/44609
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author Stefania, Mondello
author2 Sandner, Viktor
Goli, Mona
Czeiter, Endre
Amrein, Krisztina
Kochanek, Patrick M.
Gautam, Sakshi
Cho, Byeong Gwan
Morgan, Ryan
Nehme, Ali
Fiumara, Giacomo
Eid, Ali H.
Barsa, Chloe
Haidar, Muhammad Ali
Buki, Andras
Kobeissy, Firas H.
Mechref, Yehia
author2_role author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author_facet Stefania, Mondello
Sandner, Viktor
Goli, Mona
Czeiter, Endre
Amrein, Krisztina
Kochanek, Patrick M.
Gautam, Sakshi
Cho, Byeong Gwan
Morgan, Ryan
Nehme, Ali
Fiumara, Giacomo
Eid, Ali H.
Barsa, Chloe
Haidar, Muhammad Ali
Buki, Andras
Kobeissy, Firas H.
Mechref, Yehia
author_role author
dc.creator.none.fl_str_mv Stefania, Mondello
Sandner, Viktor
Goli, Mona
Czeiter, Endre
Amrein, Krisztina
Kochanek, Patrick M.
Gautam, Sakshi
Cho, Byeong Gwan
Morgan, Ryan
Nehme, Ali
Fiumara, Giacomo
Eid, Ali H.
Barsa, Chloe
Haidar, Muhammad Ali
Buki, Andras
Kobeissy, Firas H.
Mechref, Yehia
dc.date.none.fl_str_mv 2022-08-31
2023-06-20T10:31:36Z
dc.format.none.fl_str_mv application/pdf
dc.identifier.none.fl_str_mv http://dx.doi.org/10.1016/j.eclinm.2022.101494
25895370
https://www.sciencedirect.com/science/article/pii/S2589537022002243
http://hdl.handle.net/10576/44609
50
dc.language.none.fl_str_mv en
dc.publisher.none.fl_str_mv Elsevier
dc.rights.none.fl_str_mv http://creativecommons.org/licenses/by-nc-nd/4.0/
info:eu-repo/semantics/openAccess
dc.subject.none.fl_str_mv Traumatic brain injury
Glycosylation
Glycomics
Glycomarkers
Biomarkers
Serum
LC-MS
Prognosis
dc.title.none.fl_str_mv Exploring serum glycome patterns after moderate to severe traumatic brain injury: A prospective pilot study
dc.type.none.fl_str_mv Article
info:eu-repo/semantics/publishedVersion
info:eu-repo/semantics/article
description BackgroundGlycans play essential functional roles in the nervous system and their pathobiological relevance has become increasingly recognized in numerous brain disorders, but not fully explored in traumatic brain injury (TBI). We investigated longitudinal glycome patterns in patients with moderate to severe TBI (Glasgow Coma Scale [GCS] score ≤12) to characterize glyco-biomarker signatures and their relation to clinical features and long-term outcome. MethodsThis prospective single-center observational study included 51 adult patients with TBI (GCS ≤12) admitted to the neurosurgical unit of the University Hospital of Pecs, Pecs, Hungary, between June 2018 and April 2019. We used a high-throughput liquid chromatography–tandem mass spectrometry platform to assess serum levels of N-glycans up to 3 days after injury. Outcome was assessed using the Glasgow Outcome Scale-Extended (GOS-E) at 12 months post-injury. Multivariate statistical techniques, including principal component analysis and orthogonal partial least squares discriminant analysis, were used to analyze glycomics data and define highly influential structures driving class distinction. Receiver operating characteristic analyses were used to determine prognostic accuracy. FindingsWe identified 94 N-glycans encompassing all typical structural types, including oligomannose, hybrid, and complex-type entities. Levels of high mannose, hybrid and sialylated structures were temporally altered (p<0·05). Four influential glycans were identified. Two brain-specific structures, HexNAc5Hex3DeoxyHex0NeuAc0 and HexNAc5Hex4DeoxyHex0NeuAc1, were substantially increased early after injury in patients with unfavorable outcome (GOS-E≤4) (area under the curve [AUC]=0·75 [95%CI 0·59-0·90] and AUC=0·71 [0·52-0·89], respectively). Serum levels of HexNAc7Hex7DeoxyHex1NeuAc2 and HexNAc8Hex6DeoxyHex0NeuAc0 were persistently increased in patients with favorable outcome, but undetectable in those with unfavorable outcome. Levels of HexNAc5Hex4DeoxyHex0NeuAc1 were acutely elevated in patients with mass lesions and in those requiring decompressive craniectomy. InterpretationIn spite of the exploratory nature of the study and the relatively small number of patients, our results provide to the best of our knowledge initial evidence supporting the utility of glycomics approaches for biomarker discovery and patient phenotyping in TBI. Further larger multicenter studies will be required to validate our findings and to determine their pathobiological value and potential applications in practice. FundingThis work was funded by the Italian Ministry of Health (grant number GR-2013-02354960), and also partially supported by a NIH grant (1R01GM112490-08).
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spelling Exploring serum glycome patterns after moderate to severe traumatic brain injury: A prospective pilot studyStefania, MondelloSandner, ViktorGoli, MonaCzeiter, EndreAmrein, KrisztinaKochanek, Patrick M.Gautam, SakshiCho, Byeong GwanMorgan, RyanNehme, AliFiumara, GiacomoEid, Ali H.Barsa, ChloeHaidar, Muhammad AliBuki, AndrasKobeissy, Firas H.Mechref, YehiaTraumatic brain injuryGlycosylationGlycomicsGlycomarkersBiomarkersSerumLC-MSPrognosisBackgroundGlycans play essential functional roles in the nervous system and their pathobiological relevance has become increasingly recognized in numerous brain disorders, but not fully explored in traumatic brain injury (TBI). We investigated longitudinal glycome patterns in patients with moderate to severe TBI (Glasgow Coma Scale [GCS] score ≤12) to characterize glyco-biomarker signatures and their relation to clinical features and long-term outcome. MethodsThis prospective single-center observational study included 51 adult patients with TBI (GCS ≤12) admitted to the neurosurgical unit of the University Hospital of Pecs, Pecs, Hungary, between June 2018 and April 2019. We used a high-throughput liquid chromatography–tandem mass spectrometry platform to assess serum levels of N-glycans up to 3 days after injury. Outcome was assessed using the Glasgow Outcome Scale-Extended (GOS-E) at 12 months post-injury. Multivariate statistical techniques, including principal component analysis and orthogonal partial least squares discriminant analysis, were used to analyze glycomics data and define highly influential structures driving class distinction. Receiver operating characteristic analyses were used to determine prognostic accuracy. FindingsWe identified 94 N-glycans encompassing all typical structural types, including oligomannose, hybrid, and complex-type entities. Levels of high mannose, hybrid and sialylated structures were temporally altered (p<0·05). Four influential glycans were identified. Two brain-specific structures, HexNAc5Hex3DeoxyHex0NeuAc0 and HexNAc5Hex4DeoxyHex0NeuAc1, were substantially increased early after injury in patients with unfavorable outcome (GOS-E≤4) (area under the curve [AUC]=0·75 [95%CI 0·59-0·90] and AUC=0·71 [0·52-0·89], respectively). Serum levels of HexNAc7Hex7DeoxyHex1NeuAc2 and HexNAc8Hex6DeoxyHex0NeuAc0 were persistently increased in patients with favorable outcome, but undetectable in those with unfavorable outcome. Levels of HexNAc5Hex4DeoxyHex0NeuAc1 were acutely elevated in patients with mass lesions and in those requiring decompressive craniectomy. InterpretationIn spite of the exploratory nature of the study and the relatively small number of patients, our results provide to the best of our knowledge initial evidence supporting the utility of glycomics approaches for biomarker discovery and patient phenotyping in TBI. Further larger multicenter studies will be required to validate our findings and to determine their pathobiological value and potential applications in practice. FundingThis work was funded by the Italian Ministry of Health (grant number GR-2013-02354960), and also partially supported by a NIH grant (1R01GM112490-08).Elsevier2023-06-20T10:31:36Z2022-08-31Articleinfo:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articleapplication/pdfhttp://dx.doi.org/10.1016/j.eclinm.2022.10149425895370https://www.sciencedirect.com/science/article/pii/S2589537022002243http://hdl.handle.net/10576/4460950enhttp://creativecommons.org/licenses/by-nc-nd/4.0/info:eu-repo/semantics/openAccessoai:qspace.qu.edu.qa:10576/446092024-07-23T13:53:38Z
spellingShingle Exploring serum glycome patterns after moderate to severe traumatic brain injury: A prospective pilot study
Stefania, Mondello
Traumatic brain injury
Glycosylation
Glycomics
Glycomarkers
Biomarkers
Serum
LC-MS
Prognosis
status_str publishedVersion
title Exploring serum glycome patterns after moderate to severe traumatic brain injury: A prospective pilot study
title_full Exploring serum glycome patterns after moderate to severe traumatic brain injury: A prospective pilot study
title_fullStr Exploring serum glycome patterns after moderate to severe traumatic brain injury: A prospective pilot study
title_full_unstemmed Exploring serum glycome patterns after moderate to severe traumatic brain injury: A prospective pilot study
title_short Exploring serum glycome patterns after moderate to severe traumatic brain injury: A prospective pilot study
title_sort Exploring serum glycome patterns after moderate to severe traumatic brain injury: A prospective pilot study
topic Traumatic brain injury
Glycosylation
Glycomics
Glycomarkers
Biomarkers
Serum
LC-MS
Prognosis
url http://dx.doi.org/10.1016/j.eclinm.2022.101494
https://www.sciencedirect.com/science/article/pii/S2589537022002243
http://hdl.handle.net/10576/44609