Brain blood and cerebrospinal fluid flow dynamics during rhythmic handgrip exercise in young healthy men and women

Tarumi, Takashi; Yamabe, Takayuki; Fukuie, Marina; Zhu, David C.; Zhang, Rong; Ogoh, Shigehiko; Sugawara, Jun

doi:10.1113/jp281063

Cited by 15 publications

(14 citation statements)

References 55 publications

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“…It must be noted, however, that this extrapolation does not account for many physiological factors that may vary during the course of 1 h, 24 h or even decades. In fact, recent studies have observed that exercise [ 28 , 29 ], blood flow and blood pressure [ 6 , 30 , 31 ], as well as sleep [ 17 , 32 ] and respiration [ 33 – 38 ] contribute to changes in CSF flow. Moreover, overlap of stroke volume measurements between consecutive cycles was not considered in this extrapolation and should be investigated in further studies.…”

Section: Discussionmentioning

confidence: 99%

Upright versus supine MRI: effects of body position on craniocervical CSF flow

Muccio

Chu²,

Minkoff³

et al. 2021

Fluids Barriers CNS

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Background Cerebrospinal fluid (CSF) circulation between the brain and spinal canal, as part of the glymphatic system, provides homeostatic support to brain functions and waste clearance. Recently, it has been observed that CSF flow is strongly driven by cardiovascular brain pulsation, and affected by body orientation. The advancement of MRI has allowed for non-invasive examination of the CSF hydrodynamic properties. However, very few studies have addressed their relationship with body position (e.g., upright versus supine). It is important to understand how CSF hydrodynamics are altered by body position change in a single cardiac phase and how cumulative long hours staying in either upright or supine position can affect craniocervical CSF flow. Methods In this study, we investigate the changes in CSF flow at the craniocervical region with flow-sensitive MRI when subjects are moved from upright to supine position. 30 healthy volunteers were imaged in upright and supine positions using an upright MRI. The cranio-caudal and caudo-cranial CSF flow, velocity and stroke volume were measured at the C2 spinal level over one cardiac cycle using phase contrast MRI. Statistical analysis was performed to identify differences in CSF flow properties between the two positions. Results CSF stroke volume per cardiac cycle, representing CSF volume oscillating in and out of the cranium, was ~ 57.6% greater in supine (p < 0.0001), due to a ~ 83.8% increase in caudo-cranial CSF peak velocity during diastole (p < 0.0001) and extended systolic phase duration when moving from upright (0.25 ± 0.05 s) to supine (0.34 ± 0.08 s; p < 0.0001). Extrapolation to a 24 h timeframe showed significantly larger total CSF volume exchanged at C2 with 10 h spent supine versus only 5 h (p < 0.0001). Conclusions In summary, body position has significant effects on CSF flow in and out of the cranium, with more CSF oscillating in supine compared to upright position. Such difference was driven by an increased caudo-cranial diastolic CSF velocity and an increased systolic phase duration when moving from upright to supine position. Extrapolation to a 24 h timeframe suggests that more time spent in supine position increases total amount of CSF exchange, which may play a beneficial role in waste clearance in the brain.

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Section: Discussionmentioning

confidence: 99%

Upright versus supine MRI: effects of body position on craniocervical CSF flow

Muccio

Chu²,

Minkoff³

et al. 2021

Fluids Barriers CNS

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“…These findings suggest that aortic stiffness and transmission of pulsatile flow into the microcirculation may lead to quantifiable changes in brain volume and increased WMH burden. A recent study conducted by Tarumi et al in young adults investigated cardiovascular variables and cerebral blood flow in response to repeated bouts of rhythmic handgrip exercise using phase-contrast MRI ( Tarumi et al, 2021 ). Using a similar relative intensity of handgrip exercise (30-40% MVC), HR, BP, CVRi, cerebral blood flow, and respiratory rate increased during rhythmic handgrip exercise despite no change in vessel cross-sectional area ( Tarumi et al, 2021 ).…”

Section: Discussionmentioning

confidence: 99%

“…A recent study conducted by Tarumi et al in young adults investigated cardiovascular variables and cerebral blood flow in response to repeated bouts of rhythmic handgrip exercise using phase-contrast MRI ( Tarumi et al, 2021 ). Using a similar relative intensity of handgrip exercise (30-40% MVC), HR, BP, CVRi, cerebral blood flow, and respiratory rate increased during rhythmic handgrip exercise despite no change in vessel cross-sectional area ( Tarumi et al, 2021 ). Thus, higher resistance in the cerebral vessels may attenuate an increase in cerebral blood flow and prevent cerebral hyperperfusion during rhythmic handgrip exercise, which may represent a compensatory myogenic response to a hypertensive stimulus in order to dampen pulsatile flow.…”

Section: Discussionmentioning

confidence: 99%

“…Previous work evaluating MCAv and MCA diameter in response to rhythmic handgrip exercise has demonstrated that MCA diameter may decrease by ∼ 2% in adults aged 20-59 years old suggesting active vasoconstriction in the cerebral circulation during rhythmic handgrip exercise ( Verbree et al, 2017 ). However, the cross sectional area of the internal carotid and vertebral arteries do not change in response to rhythmic handgrip exercise performed at 30-40% MVC in young adults ( Tarumi et al, 2021 ). It is possible that IHG exercise causes vasoconstriction of the MCA which may cause an increase in MCAv despite little or no change in cerebral blood flow ( Giller et al, 2000 ), though the effect of isometric versus rhythmic handgrip exercise on MCA diameter is currently unknown.…”

Section: Limitationsmentioning

confidence: 99%

“…Together, IHG exercise and post-exercise ischemia provide insight into the cardiovascular responses to muscle mechanoreflex and metaboreflex activation. Isometric and rhythmic handgrip exercise responses have been used to evaluate cardiovascular risk in a variety of populations ( Ide et al, 1998 ; Giller et al, 2000 ; Ranadive et al, 2017 ; Miller et al, 2019 ; Tarumi et al, 2021 ). We have previously reported that women with a history of preeclampsia (who have an elevated risk of cerebrovascular disease and cognitive decline) demonstrated a greater cerebral blood flow velocity response to IHG exercise ( Miller et al, 2019 ), despite similar increases in BP ( Ranadive et al, 2017 ), compared with women without a history of preeclampsia.…”

Section: Introductionmentioning

confidence: 99%

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Sympathoexcitatory Responses to Isometric Handgrip Exercise Are Associated With White Matter Hyperintensities in Middle-Aged and Older Adults

Pearson

Miller

Corkery

et al. 2022

Front. Aging Neurosci.

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Vascular dysfunction may occur prior to declines in cognitive function and accumulation of neuropathology. White matter hyperintensities (WMH) develop due to cerebral ischemia and elevated blood pressure in midlife. The purpose of this study was to evaluate associations between cardiovascular and cerebrovascular responses to sympathoexcitatory stimuli and WMH burden in cognitively unimpaired middle-aged and older adults. Sixty-eight adults (age = 63 ± 4y, men = 20, women = 48) participated in this study. Participants completed isometric handgrip exercise (IHG) exercise at 40% of maximal voluntary contraction until fatigue followed by a 90s period of post-exercise ischemia. Heart rate (HR), mean arterial pressure (MAP), middle cerebral artery blood velocity (MCAv), and end-tidal CO2 were continuously measured throughout the protocol. Cerebrovascular resistance index (CVRi) was calculated as MAP/MCAv. WMH lesion volume and intracranial volume (ICV) were measured using a FLAIR and T1 scan on a 3T MRI scanner, respectively. WMH fraction was calculated as (WMH lesion volume/ICV)*100 and cubic root transformed. Multiple linear regressions were used to determine the association between cardiovascular and cerebrovascular responses to IHG exercise and post-exercise ischemia and WMH fraction. Multiple linear regression models were adjusted for age, sex, apolipoprotein ε4 status, and total work performed during IHG exercise. During IHG exercise, there were significant increases from baseline in HR (25 ± 12%), MAP (27 ± 11%), MCAv (5 ± 10%), and CVRi (22 ± 17%; P < 0.001 for all). During post-exercise ischemia, HR (8 ± 7%), MAP (22 ± 9%), and CVRi (23 ± 16%) remained elevated (P < 0.001) while MCAv (0 ± 10%) was not different compared to baseline. There was an inverse association between the percent change in HR (r = −0.42, P = 0.002), MAP (r = −0.41, P = 0.002), and CVRi (r = −0.31, P = 0.045), but not MCAv (r = 0.19, P = 0.971) in response to IHG exercise and WMH fraction. There were no associations between responses to post-exercise ischemia and WMH fraction. Lower sympathoexcitatory responses to IHG exercise are associated with greater WMH burden in middle-aged to older adults. These findings suggest that individuals who demonstrate smaller increases in HR, MAP, and CVRi in response to sympathoexcitatory stress have greater WMH burden.

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Exercise MR of Skeletal Muscles, the Heart, and the Brain

Hooijmans,

Jeneson,

Jørstad

et al. 2024

Magnetic Resonance Imaging

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Magnetic resonance (MR) imaging (MRI) is routinely used to evaluate organ morphology and pathology in the human body at rest or in combination with pharmacological stress as an exercise surrogate. With MR during actual physical exercise, we can assess functional characteristics of tissues and organs under real‐life stress conditions. This is particularly relevant in patients with limited exercise capacity or exercise intolerance, and where complaints typically present only during physical activity, such as in neuromuscular disorders, inherited metabolic diseases, and heart failure. This review describes practical and physiological aspects of exercise MR of skeletal muscles, the heart, and the brain. The acute effects of physical exercise on these organs are addressed in the light of various dynamic quantitative MR readouts, including phosphorus‐31 MR spectroscopy (31P‐MRS) of tissue energy metabolism, phase‐contrast MRI of blood flow and muscle contraction, real‐time cine MRI of cardiac performance, and arterial spin labeling MRI of muscle and brain perfusion. Exercise MR will help advancing our understanding of underlying mechanisms that contribute to exercise intolerance, which often proceed structural and anatomical changes in disease. Its potential to detect disease‐driven alterations in organ function, perfusion, and metabolism under physiological stress renders exercise MR stress testing a powerful noninvasive imaging modality to aid in disease diagnosis and risk stratification. Although not yet integrated in most clinical workflows, and while some applications still require thorough validation, exercise MR has established itself as a comprehensive and versatile modality for characterizing physiology in health and disease in a noninvasive and quantitative way.Evidence Level5Technical EfficacyStage 1

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Brain blood and cerebrospinal fluid flow dynamics during rhythmic handgrip exercise in young healthy men and women

Cited by 15 publications

References 55 publications

Upright versus supine MRI: effects of body position on craniocervical CSF flow

Upright versus supine MRI: effects of body position on craniocervical CSF flow

Sympathoexcitatory Responses to Isometric Handgrip Exercise Are Associated With White Matter Hyperintensities in Middle-Aged and Older Adults

Exercise MR of Skeletal Muscles, the Heart, and the Brain

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