Blood flow response to orthostatic challenge identifies signatures of the failure of static cerebral autoregulation in patients with cerebrovascular disease

Clara Gregori-Pla; Rickson C. Mesquita; Christopher G. Favilla; David R. Busch; Igor Blanco; Peyman Zirak; Lisa Kobayashi Frisk; Stella Avtzi; Federica Maruccia; Giacomo Giacalone; Gianluca Cotta; Pol Camps-Renom; Michael T. Mullen; Joan Martí-Fàbregas; Luís Prats-Sánchez; Alejandro Martínez-Domeño; Scott E. Kasner; Joel H. Greenberg; Chao Zhou; Brian L. Edlow; Mary E. Putt; John A. Detre; Arjun G. Yodh; Turgut Durduran; Raquel Delgado-Mederos

doi:10.1186/s12883-021-02179-8

Blood flow response to orthostatic challenge identifies signatures of the failure of static cerebral autoregulation in patients with cerebrovascular disease

Clara Gregori-Pla^*, Rickson C. Mesquita, Christopher G. Favilla, David R. Busch, Igor Blanco, Peyman Zirak, Lisa Kobayashi Frisk, Stella Avtzi, Federica Maruccia, Giacomo Giacalone, Gianluca Cotta, Pol Camps-Renom, Michael T. Mullen, Joan Martí-Fàbregas, Luís Prats-Sánchez, Alejandro Martínez-Domeño, Scott E. Kasner, Joel H. Greenberg, Chao Zhou, Brian L. EdlowMary E. Putt, John A. Detre, Arjun G. Yodh, Turgut Durduran, Raquel Delgado-Mederos

^*Corresponding author for this work

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Abstract

Background: The cortical microvascular cerebral blood flow response (CBF) to different changes in head-of-bed (HOB) position has been shown to be altered in acute ischemic stroke (AIS) by diffuse correlation spectroscopy (DCS) technique. However, the relationship between these relative ΔCBF changes and associated systemic blood pressure changes has not been studied, even though blood pressure is a major driver of cerebral blood flow.

Methods: Transcranial DCS data from four studies measuring bilateral frontal microvascular cerebral blood flow in healthy controls (n = 15), patients with asymptomatic severe internal carotid artery stenosis (ICA, n = 27), and patients with acute ischemic stroke (AIS, n = 72) were aggregated. DCS-measured CBF was measured in response to a short head-of-bed (HOB) position manipulation protocol (supine/elevated/supine, 5 min at each position). In a sub-group (AIS, n = 26; ICA, n = 14; control, n = 15), mean arterial pressure (MAP) was measured dynamically during the protocol.

Results: After elevated positioning, DCS CBF returned to baseline supine values in controls (p = 0.890) but not in patients with AIS (9.6% [6.0,13.3], mean 95% CI, p < 0.001) or ICA stenosis (8.6% [3.1,14.0], p = 0.003)). MAP in AIS patients did not return to baseline values (2.6 mmHg [0.5, 4.7], p = 0.018), but in ICA stenosis patients and controls did. Instead ipsilesional but not contralesional CBF was correlated with MAP (AIS 6.0%/mmHg [− 2.4,14.3], p = 0.038; ICA stenosis 11.0%/mmHg [2.4,19.5], p < 0.001).

Conclusions: The observed associations between ipsilateral CBF and MAP suggest that short HOB position changes may elicit deficits in cerebral autoregulation in cerebrovascular disorders. Additional research is required to further characterize this phenomenon.

Original language	English
Article number	154
Number of pages	12
Journal	BMC Neurology
Volume	21
Issue number	1
Early online date	9 Apr 2021
DOIs	https://doi.org/10.1186/s12883-021-02179-8
Publication status	Published - Dec 2021

Bibliographical note

Funding Information:
The funders did not have any role in study design, execution and data interpretation. This work was funded by Redes Temáticas de Investigación Cooperativa (RETICS-INVICTUS RD012/0014 and RD16/0019/0010), Fundació CELLEX Barcelona, Ministerio de Economía y Competitividad/FEDER (PHOTODEMENTIA, PHOTOMETABO, DPI2015–64358-C2–1-R, PRE2018-085082), Instituto de Salud Carlos III/FEDER (FIS PI09/0557, MEDPHOTAGE, DTS16/00087), the “Severo Ochoa” Programme for Centres of Excellence in R&D (SEV-2015-0522), the Obra Social “la Caixa” Foundation (LlumMedBcn), Institució “Centres de Recerca de Catalunya”, “Agència de Gestió d’Ajuts Universitaris i de Recerca”-Generalitat (2017SGR-1380), LASERLAB-EUROPE IV (EU-H2020 654148), Whitaker International Program of the Institute for International Education, T32 HL007954 Multidisciplinary training in cardiovascular biology, Marie Curie initial training network (OILTEBIA 317526), Marie Sklowdowska-Curie-COFUND (H2020, ICFOstepstone 2, 71329), “Fundació La Marató TV3” (201709.30, 201709.31), São Paulo Research Foundation (FAPESP) through 2012/02500–8 and National Institutes of Health (R01-NS060653, K24-NS058386, R24-HD050836, P41-EB015893, DP2-HD101400, U54-HD086984).

Publisher Copyright:
© 2021, The Author(s).

Keywords

Cerebral autoregulation
Cerebral blood flow
Cerebrovascular disease
Diffuse correlation spectroscopy
Diffuse optics
Mean arterial pressure

ASJC Scopus subject areas

Clinical Neurology

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Gregori-Pla, C., Mesquita, R. C., Favilla, C. G., Busch, D. R., Blanco, I., Zirak, P., Frisk, L. K., Avtzi, S., Maruccia, F., Giacalone, G., Cotta, G., Camps-Renom, P., Mullen, M. T., Martí-Fàbregas, J., Prats-Sánchez, L., Martínez-Domeño, A., Kasner, S. E., Greenberg, J. H., Zhou, C., ... Delgado-Mederos, R. (2021). Blood flow response to orthostatic challenge identifies signatures of the failure of static cerebral autoregulation in patients with cerebrovascular disease. BMC Neurology, 21(1), Article 154. https://doi.org/10.1186/s12883-021-02179-8

@article{9c320aafa1004c0ca680951be86799e3,

title = "Blood flow response to orthostatic challenge identifies signatures of the failure of static cerebral autoregulation in patients with cerebrovascular disease",

abstract = "Background: The cortical microvascular cerebral blood flow response (CBF) to different changes in head-of-bed (HOB) position has been shown to be altered in acute ischemic stroke (AIS) by diffuse correlation spectroscopy (DCS) technique. However, the relationship between these relative ΔCBF changes and associated systemic blood pressure changes has not been studied, even though blood pressure is a major driver of cerebral blood flow. Methods: Transcranial DCS data from four studies measuring bilateral frontal microvascular cerebral blood flow in healthy controls (n = 15), patients with asymptomatic severe internal carotid artery stenosis (ICA, n = 27), and patients with acute ischemic stroke (AIS, n = 72) were aggregated. DCS-measured CBF was measured in response to a short head-of-bed (HOB) position manipulation protocol (supine/elevated/supine, 5 min at each position). In a sub-group (AIS, n = 26; ICA, n = 14; control, n = 15), mean arterial pressure (MAP) was measured dynamically during the protocol. Results: After elevated positioning, DCS CBF returned to baseline supine values in controls (p = 0.890) but not in patients with AIS (9.6% [6.0,13.3], mean 95% CI, p < 0.001) or ICA stenosis (8.6% [3.1,14.0], p = 0.003)). MAP in AIS patients did not return to baseline values (2.6 mmHg [0.5, 4.7], p = 0.018), but in ICA stenosis patients and controls did. Instead ipsilesional but not contralesional CBF was correlated with MAP (AIS 6.0%/mmHg [− 2.4,14.3], p = 0.038; ICA stenosis 11.0%/mmHg [2.4,19.5], p < 0.001). Conclusions: The observed associations between ipsilateral CBF and MAP suggest that short HOB position changes may elicit deficits in cerebral autoregulation in cerebrovascular disorders. Additional research is required to further characterize this phenomenon.",

keywords = "Cerebral autoregulation, Cerebral blood flow, Cerebrovascular disease, Diffuse correlation spectroscopy, Diffuse optics, Mean arterial pressure",

author = "Clara Gregori-Pla and Mesquita, {Rickson C.} and Favilla, {Christopher G.} and Busch, {David R.} and Igor Blanco and Peyman Zirak and Frisk, {Lisa Kobayashi} and Stella Avtzi and Federica Maruccia and Giacomo Giacalone and Gianluca Cotta and Pol Camps-Renom and Mullen, {Michael T.} and Joan Mart{\'i}-F{\`a}bregas and Lu{\'i}s Prats-S{\'a}nchez and Alejandro Mart{\'i}nez-Dome{\~n}o and Kasner, {Scott E.} and Greenberg, {Joel H.} and Chao Zhou and Edlow, {Brian L.} and Putt, {Mary E.} and Detre, {John A.} and Yodh, {Arjun G.} and Turgut Durduran and Raquel Delgado-Mederos",

note = "Funding Information: The funders did not have any role in study design, execution and data interpretation. This work was funded by Redes Tem{\'a}ticas de Investigaci{\'o}n Cooperativa (RETICS-INVICTUS RD012/0014 and RD16/0019/0010), Fundaci{\'o} CELLEX Barcelona, Ministerio de Econom{\'i}a y Competitividad/FEDER (PHOTODEMENTIA, PHOTOMETABO, DPI2015–64358-C2–1-R, PRE2018-085082), Instituto de Salud Carlos III/FEDER (FIS PI09/0557, MEDPHOTAGE, DTS16/00087), the “Severo Ochoa” Programme for Centres of Excellence in R&D (SEV-2015-0522), the Obra Social “la Caixa” Foundation (LlumMedBcn), Instituci{\'o} “Centres de Recerca de Catalunya”, “Ag{\`e}ncia de Gesti{\'o} d{\textquoteright}Ajuts Universitaris i de Recerca”-Generalitat (2017SGR-1380), LASERLAB-EUROPE IV (EU-H2020 654148), Whitaker International Program of the Institute for International Education, T32 HL007954 Multidisciplinary training in cardiovascular biology, Marie Curie initial training network (OILTEBIA 317526), Marie Sklowdowska-Curie-COFUND (H2020, ICFOstepstone 2, 71329), “Fundaci{\'o} La Marat{\'o} TV3” (201709.30, 201709.31), S{\~a}o Paulo Research Foundation (FAPESP) through 2012/02500–8 and National Institutes of Health (R01-NS060653, K24-NS058386, R24-HD050836, P41-EB015893, DP2-HD101400, U54-HD086984). Publisher Copyright: {\textcopyright} 2021, The Author(s).",

year = "2021",

month = dec,

doi = "10.1186/s12883-021-02179-8",

language = "English",

volume = "21",

journal = "BMC Neurology",

issn = "1471-2377",

publisher = "Springer",

number = "1",

}

Gregori-Pla, C, Mesquita, RC, Favilla, CG, Busch, DR, Blanco, I, Zirak, P, Frisk, LK, Avtzi, S, Maruccia, F, Giacalone, G, Cotta, G, Camps-Renom, P, Mullen, MT, Martí-Fàbregas, J, Prats-Sánchez, L, Martínez-Domeño, A, Kasner, SE, Greenberg, JH, Zhou, C, Edlow, BL, Putt, ME, Detre, JA, Yodh, AG, Durduran, T & Delgado-Mederos, R 2021, 'Blood flow response to orthostatic challenge identifies signatures of the failure of static cerebral autoregulation in patients with cerebrovascular disease', BMC Neurology, vol. 21, no. 1, 154. https://doi.org/10.1186/s12883-021-02179-8

TY - JOUR

T1 - Blood flow response to orthostatic challenge identifies signatures of the failure of static cerebral autoregulation in patients with cerebrovascular disease

AU - Gregori-Pla, Clara

AU - Mesquita, Rickson C.

AU - Favilla, Christopher G.

AU - Busch, David R.

AU - Blanco, Igor

AU - Zirak, Peyman

AU - Frisk, Lisa Kobayashi

AU - Avtzi, Stella

AU - Maruccia, Federica

AU - Giacalone, Giacomo

AU - Cotta, Gianluca

AU - Camps-Renom, Pol

AU - Mullen, Michael T.

AU - Martí-Fàbregas, Joan

AU - Prats-Sánchez, Luís

AU - Martínez-Domeño, Alejandro

AU - Kasner, Scott E.

AU - Greenberg, Joel H.

AU - Zhou, Chao

AU - Edlow, Brian L.

AU - Putt, Mary E.

AU - Detre, John A.

AU - Yodh, Arjun G.

AU - Durduran, Turgut

AU - Delgado-Mederos, Raquel

N1 - Funding Information: The funders did not have any role in study design, execution and data interpretation. This work was funded by Redes Temáticas de Investigación Cooperativa (RETICS-INVICTUS RD012/0014 and RD16/0019/0010), Fundació CELLEX Barcelona, Ministerio de Economía y Competitividad/FEDER (PHOTODEMENTIA, PHOTOMETABO, DPI2015–64358-C2–1-R, PRE2018-085082), Instituto de Salud Carlos III/FEDER (FIS PI09/0557, MEDPHOTAGE, DTS16/00087), the “Severo Ochoa” Programme for Centres of Excellence in R&D (SEV-2015-0522), the Obra Social “la Caixa” Foundation (LlumMedBcn), Institució “Centres de Recerca de Catalunya”, “Agència de Gestió d’Ajuts Universitaris i de Recerca”-Generalitat (2017SGR-1380), LASERLAB-EUROPE IV (EU-H2020 654148), Whitaker International Program of the Institute for International Education, T32 HL007954 Multidisciplinary training in cardiovascular biology, Marie Curie initial training network (OILTEBIA 317526), Marie Sklowdowska-Curie-COFUND (H2020, ICFOstepstone 2, 71329), “Fundació La Marató TV3” (201709.30, 201709.31), São Paulo Research Foundation (FAPESP) through 2012/02500–8 and National Institutes of Health (R01-NS060653, K24-NS058386, R24-HD050836, P41-EB015893, DP2-HD101400, U54-HD086984). Publisher Copyright: © 2021, The Author(s).

PY - 2021/12

Y1 - 2021/12

N2 - Background: The cortical microvascular cerebral blood flow response (CBF) to different changes in head-of-bed (HOB) position has been shown to be altered in acute ischemic stroke (AIS) by diffuse correlation spectroscopy (DCS) technique. However, the relationship between these relative ΔCBF changes and associated systemic blood pressure changes has not been studied, even though blood pressure is a major driver of cerebral blood flow. Methods: Transcranial DCS data from four studies measuring bilateral frontal microvascular cerebral blood flow in healthy controls (n = 15), patients with asymptomatic severe internal carotid artery stenosis (ICA, n = 27), and patients with acute ischemic stroke (AIS, n = 72) were aggregated. DCS-measured CBF was measured in response to a short head-of-bed (HOB) position manipulation protocol (supine/elevated/supine, 5 min at each position). In a sub-group (AIS, n = 26; ICA, n = 14; control, n = 15), mean arterial pressure (MAP) was measured dynamically during the protocol. Results: After elevated positioning, DCS CBF returned to baseline supine values in controls (p = 0.890) but not in patients with AIS (9.6% [6.0,13.3], mean 95% CI, p < 0.001) or ICA stenosis (8.6% [3.1,14.0], p = 0.003)). MAP in AIS patients did not return to baseline values (2.6 mmHg [0.5, 4.7], p = 0.018), but in ICA stenosis patients and controls did. Instead ipsilesional but not contralesional CBF was correlated with MAP (AIS 6.0%/mmHg [− 2.4,14.3], p = 0.038; ICA stenosis 11.0%/mmHg [2.4,19.5], p < 0.001). Conclusions: The observed associations between ipsilateral CBF and MAP suggest that short HOB position changes may elicit deficits in cerebral autoregulation in cerebrovascular disorders. Additional research is required to further characterize this phenomenon.

AB - Background: The cortical microvascular cerebral blood flow response (CBF) to different changes in head-of-bed (HOB) position has been shown to be altered in acute ischemic stroke (AIS) by diffuse correlation spectroscopy (DCS) technique. However, the relationship between these relative ΔCBF changes and associated systemic blood pressure changes has not been studied, even though blood pressure is a major driver of cerebral blood flow. Methods: Transcranial DCS data from four studies measuring bilateral frontal microvascular cerebral blood flow in healthy controls (n = 15), patients with asymptomatic severe internal carotid artery stenosis (ICA, n = 27), and patients with acute ischemic stroke (AIS, n = 72) were aggregated. DCS-measured CBF was measured in response to a short head-of-bed (HOB) position manipulation protocol (supine/elevated/supine, 5 min at each position). In a sub-group (AIS, n = 26; ICA, n = 14; control, n = 15), mean arterial pressure (MAP) was measured dynamically during the protocol. Results: After elevated positioning, DCS CBF returned to baseline supine values in controls (p = 0.890) but not in patients with AIS (9.6% [6.0,13.3], mean 95% CI, p < 0.001) or ICA stenosis (8.6% [3.1,14.0], p = 0.003)). MAP in AIS patients did not return to baseline values (2.6 mmHg [0.5, 4.7], p = 0.018), but in ICA stenosis patients and controls did. Instead ipsilesional but not contralesional CBF was correlated with MAP (AIS 6.0%/mmHg [− 2.4,14.3], p = 0.038; ICA stenosis 11.0%/mmHg [2.4,19.5], p < 0.001). Conclusions: The observed associations between ipsilateral CBF and MAP suggest that short HOB position changes may elicit deficits in cerebral autoregulation in cerebrovascular disorders. Additional research is required to further characterize this phenomenon.

KW - Cerebral autoregulation

KW - Cerebral blood flow

KW - Cerebrovascular disease

KW - Diffuse correlation spectroscopy

KW - Diffuse optics

KW - Mean arterial pressure

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U2 - 10.1186/s12883-021-02179-8

DO - 10.1186/s12883-021-02179-8

M3 - Article

C2 - 33836684

AN - SCOPUS:85104104887

SN - 1471-2377

VL - 21

JO - BMC Neurology

JF - BMC Neurology

IS - 1

M1 - 154

ER -

Blood flow response to orthostatic challenge identifies signatures of the failure of static cerebral autoregulation in patients with cerebrovascular disease

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