Cerebrovascular pressure reactivity monitoring using wavelet analysis in traumatic brain injury patients

A retrospective study

Xiuyun Liu, Joseph Donnelly, Marek Czosnyka, Marcel J.H. Aries, Ken Brady, Danilo Cardim, Chiara Robba, Manuel Cabeleira, Dong Ju Kim, Christina Haubrich, Peter J. Hutchinson, Peter Smielewski

Research output: Contribution to journalArticle

11 Citations (Scopus)

Abstract

Background: After traumatic brain injury (TBI), the ability of cerebral vessels to appropriately react to changes in arterial blood pressure (pressure reactivity) is impaired, leaving patients vulnerable to cerebral hypo- or hyperperfusion. Although, the traditional pressure reactivity index (PRx) has demonstrated that impaired pressure reactivity is associated with poor patient outcome, PRx is sometimes erratic and may not be reliable in various clinical circumstances. Here, we introduce a more robust transform-based wavelet pressure reactivity index (wPRx) and compare its performance with the widely used traditional PRx across 3 areas: its stability and reliability in time, its ability to give an optimal cerebral perfusion pressure (CPPopt) recommendation, and its relationship with patient outcome. Methods and findings: Five hundred and fifteen patients with TBI admitted in Addenbrooke’s Hospital, United Kingdom (March 23rd, 2003 through December 9th, 2014), with continuous monitoring of arterial blood pressure (ABP) and intracranial pressure (ICP), were retrospectively analyzed to calculate the traditional PRx and a novel wavelet transform-based wPRx. wPRx was calculated by taking the cosine of the wavelet transform phase-shift between ABP and ICP. A time trend of CPPopt was calculated using an automated curve-fitting method that determined the cerebral perfusion pressure (CPP) at which the pressure reactivity (PRx or wPRx) was most efficient (CPPopt_PRx and CPPopt_wPRx, respectively). There was a significantly positive relationship between PRx and wPRx (r = 0.73), and wavelet wPRx was more reliable in time (ratio of between-hour variance to total variance, wPRx 0.957 ± 0.0032 versus PRx and 0.949 ± 0.047 for PRx, p = 0.002). The 2-hour interval standard deviation of wPRx (0.19 ± 0.07) was smaller than that of PRx (0.30 ± 0.13, p < 0.001). wPRx performed better in distinguishing between mortality and survival (the area under the receiver operating characteristic [ROC] curve [AUROC] for wPRx was 0.73 versus 0.66 for PRx, p = 0.003). The mean difference between the patients’ CPP and their CPPopt was related to outcome for both calculation methods. There was a good relationship between the 2 CPPopts (r = 0.814, p < 0.001). CPPopt_wPRx was more stable than CPPopt_PRx (within patient standard deviation 7.05 ± 3.78 versus 8.45 ± 2.90; p < 0.001). Key limitations include that this study is a retrospective analysis and only compared wPRx with PRx in the cohort of patients with TBI. Prior prospective validation is required to better assess clinical utility of this approach. Conclusions: wPRx offers several advantages to the traditional PRx: it is more stable in time, it yields a more consistent CPPopt recommendation, and, importantly, it has a stronger relationship with patient outcome. The clinical utility of wPRx should be explored in prospective studies of critically injured neurological patients.

Original languageEnglish
Article numbere1002348
JournalPLoS Medicine
Volume14
Issue number7
DOIs
Publication statusPublished - 2017 Jul 1

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Wavelet Analysis
Wavelet analysis
Blood pressure
Brain
Retrospective Studies
Pressure
Wavelet transforms
Monitoring
Curve fitting
Phase shift
Mathematical transformations
Cerebrovascular Circulation
Traumatic Brain Injury
Arterial Pressure
Intracranial Pressure

ASJC Scopus subject areas

  • Biotechnology
  • Biochemistry
  • Molecular Biology
  • Cell Biology

Cite this

Liu, X., Donnelly, J., Czosnyka, M., Aries, M. J. H., Brady, K., Cardim, D., ... Smielewski, P. (2017). Cerebrovascular pressure reactivity monitoring using wavelet analysis in traumatic brain injury patients: A retrospective study. PLoS Medicine, 14(7), [e1002348]. https://doi.org/10.1371/journal.pmed.1002348

Cerebrovascular pressure reactivity monitoring using wavelet analysis in traumatic brain injury patients : A retrospective study. / Liu, Xiuyun; Donnelly, Joseph; Czosnyka, Marek; Aries, Marcel J.H.; Brady, Ken; Cardim, Danilo; Robba, Chiara; Cabeleira, Manuel; Kim, Dong Ju; Haubrich, Christina; Hutchinson, Peter J.; Smielewski, Peter.

In: PLoS Medicine, Vol. 14, No. 7, e1002348, 01.07.2017.

Research output: Contribution to journalArticle

Liu, X, Donnelly, J, Czosnyka, M, Aries, MJH, Brady, K, Cardim, D, Robba, C, Cabeleira, M, Kim, DJ, Haubrich, C, Hutchinson, PJ & Smielewski, P 2017, 'Cerebrovascular pressure reactivity monitoring using wavelet analysis in traumatic brain injury patients: A retrospective study', PLoS Medicine, vol. 14, no. 7, e1002348. https://doi.org/10.1371/journal.pmed.1002348
Liu, Xiuyun ; Donnelly, Joseph ; Czosnyka, Marek ; Aries, Marcel J.H. ; Brady, Ken ; Cardim, Danilo ; Robba, Chiara ; Cabeleira, Manuel ; Kim, Dong Ju ; Haubrich, Christina ; Hutchinson, Peter J. ; Smielewski, Peter. / Cerebrovascular pressure reactivity monitoring using wavelet analysis in traumatic brain injury patients : A retrospective study. In: PLoS Medicine. 2017 ; Vol. 14, No. 7.
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author = "Xiuyun Liu and Joseph Donnelly and Marek Czosnyka and Aries, {Marcel J.H.} and Ken Brady and Danilo Cardim and Chiara Robba and Manuel Cabeleira and Kim, {Dong Ju} and Christina Haubrich and Hutchinson, {Peter J.} and Peter Smielewski",
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TY - JOUR

T1 - Cerebrovascular pressure reactivity monitoring using wavelet analysis in traumatic brain injury patients

T2 - A retrospective study

AU - Liu, Xiuyun

AU - Donnelly, Joseph

AU - Czosnyka, Marek

AU - Aries, Marcel J.H.

AU - Brady, Ken

AU - Cardim, Danilo

AU - Robba, Chiara

AU - Cabeleira, Manuel

AU - Kim, Dong Ju

AU - Haubrich, Christina

AU - Hutchinson, Peter J.

AU - Smielewski, Peter

PY - 2017/7/1

Y1 - 2017/7/1

N2 - Background: After traumatic brain injury (TBI), the ability of cerebral vessels to appropriately react to changes in arterial blood pressure (pressure reactivity) is impaired, leaving patients vulnerable to cerebral hypo- or hyperperfusion. Although, the traditional pressure reactivity index (PRx) has demonstrated that impaired pressure reactivity is associated with poor patient outcome, PRx is sometimes erratic and may not be reliable in various clinical circumstances. Here, we introduce a more robust transform-based wavelet pressure reactivity index (wPRx) and compare its performance with the widely used traditional PRx across 3 areas: its stability and reliability in time, its ability to give an optimal cerebral perfusion pressure (CPPopt) recommendation, and its relationship with patient outcome. Methods and findings: Five hundred and fifteen patients with TBI admitted in Addenbrooke’s Hospital, United Kingdom (March 23rd, 2003 through December 9th, 2014), with continuous monitoring of arterial blood pressure (ABP) and intracranial pressure (ICP), were retrospectively analyzed to calculate the traditional PRx and a novel wavelet transform-based wPRx. wPRx was calculated by taking the cosine of the wavelet transform phase-shift between ABP and ICP. A time trend of CPPopt was calculated using an automated curve-fitting method that determined the cerebral perfusion pressure (CPP) at which the pressure reactivity (PRx or wPRx) was most efficient (CPPopt_PRx and CPPopt_wPRx, respectively). There was a significantly positive relationship between PRx and wPRx (r = 0.73), and wavelet wPRx was more reliable in time (ratio of between-hour variance to total variance, wPRx 0.957 ± 0.0032 versus PRx and 0.949 ± 0.047 for PRx, p = 0.002). The 2-hour interval standard deviation of wPRx (0.19 ± 0.07) was smaller than that of PRx (0.30 ± 0.13, p < 0.001). wPRx performed better in distinguishing between mortality and survival (the area under the receiver operating characteristic [ROC] curve [AUROC] for wPRx was 0.73 versus 0.66 for PRx, p = 0.003). The mean difference between the patients’ CPP and their CPPopt was related to outcome for both calculation methods. There was a good relationship between the 2 CPPopts (r = 0.814, p < 0.001). CPPopt_wPRx was more stable than CPPopt_PRx (within patient standard deviation 7.05 ± 3.78 versus 8.45 ± 2.90; p < 0.001). Key limitations include that this study is a retrospective analysis and only compared wPRx with PRx in the cohort of patients with TBI. Prior prospective validation is required to better assess clinical utility of this approach. Conclusions: wPRx offers several advantages to the traditional PRx: it is more stable in time, it yields a more consistent CPPopt recommendation, and, importantly, it has a stronger relationship with patient outcome. The clinical utility of wPRx should be explored in prospective studies of critically injured neurological patients.

AB - Background: After traumatic brain injury (TBI), the ability of cerebral vessels to appropriately react to changes in arterial blood pressure (pressure reactivity) is impaired, leaving patients vulnerable to cerebral hypo- or hyperperfusion. Although, the traditional pressure reactivity index (PRx) has demonstrated that impaired pressure reactivity is associated with poor patient outcome, PRx is sometimes erratic and may not be reliable in various clinical circumstances. Here, we introduce a more robust transform-based wavelet pressure reactivity index (wPRx) and compare its performance with the widely used traditional PRx across 3 areas: its stability and reliability in time, its ability to give an optimal cerebral perfusion pressure (CPPopt) recommendation, and its relationship with patient outcome. Methods and findings: Five hundred and fifteen patients with TBI admitted in Addenbrooke’s Hospital, United Kingdom (March 23rd, 2003 through December 9th, 2014), with continuous monitoring of arterial blood pressure (ABP) and intracranial pressure (ICP), were retrospectively analyzed to calculate the traditional PRx and a novel wavelet transform-based wPRx. wPRx was calculated by taking the cosine of the wavelet transform phase-shift between ABP and ICP. A time trend of CPPopt was calculated using an automated curve-fitting method that determined the cerebral perfusion pressure (CPP) at which the pressure reactivity (PRx or wPRx) was most efficient (CPPopt_PRx and CPPopt_wPRx, respectively). There was a significantly positive relationship between PRx and wPRx (r = 0.73), and wavelet wPRx was more reliable in time (ratio of between-hour variance to total variance, wPRx 0.957 ± 0.0032 versus PRx and 0.949 ± 0.047 for PRx, p = 0.002). The 2-hour interval standard deviation of wPRx (0.19 ± 0.07) was smaller than that of PRx (0.30 ± 0.13, p < 0.001). wPRx performed better in distinguishing between mortality and survival (the area under the receiver operating characteristic [ROC] curve [AUROC] for wPRx was 0.73 versus 0.66 for PRx, p = 0.003). The mean difference between the patients’ CPP and their CPPopt was related to outcome for both calculation methods. There was a good relationship between the 2 CPPopts (r = 0.814, p < 0.001). CPPopt_wPRx was more stable than CPPopt_PRx (within patient standard deviation 7.05 ± 3.78 versus 8.45 ± 2.90; p < 0.001). Key limitations include that this study is a retrospective analysis and only compared wPRx with PRx in the cohort of patients with TBI. Prior prospective validation is required to better assess clinical utility of this approach. Conclusions: wPRx offers several advantages to the traditional PRx: it is more stable in time, it yields a more consistent CPPopt recommendation, and, importantly, it has a stronger relationship with patient outcome. The clinical utility of wPRx should be explored in prospective studies of critically injured neurological patients.

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