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Research ArticleAdult Brain

Cerebrovascular Reactivity during Prolonged Breath-Hold in Experienced Freedivers

V.C. Keil, L. Eichhorn, H.J.M.M. Mutsaerts, F. Träber, W. Block, B. Mädler, K. van de Ven, J.C.W. Siero, B.J. MacIntosh, J. Petr, R. Fimmers, H.H. Schild and E. Hattingen
American Journal of Neuroradiology October 2018, 39 (10) 1839-1847; DOI: https://doi.org/10.3174/ajnr.A5790
V.C. Keil
aFrom the Departments of Radiology (V.C.K., F.T., W.B., H.H.S., E.H.)
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L. Eichhorn
bAnesthesiology and Intensive Care Medicine (L.E.)
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H.J.M.M. Mutsaerts
dDepartment of Radiology (H.J.M.M.M.), Academic Medical Center, Amsterdam, the Netherlands
eSunnybrook Research Institute (H.J.M.M.M., B.J.M.), University of Toronto, Toronto, Ontario, Canada
fDepartment of Radiology (H.J.M.M.M., J.C.W.S.), University Medical Center Utrecht, Utrecht, the Netherlands
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F. Träber
aFrom the Departments of Radiology (V.C.K., F.T., W.B., H.H.S., E.H.)
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W. Block
aFrom the Departments of Radiology (V.C.K., F.T., W.B., H.H.S., E.H.)
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B. Mädler
gPhilips GmbH (B.M), Bonn, Germany
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K. van de Ven
hPhilips Healthcare (K.v.d.V.), Best, the Netherlands
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J.C.W. Siero
fDepartment of Radiology (H.J.M.M.M., J.C.W.S.), University Medical Center Utrecht, Utrecht, the Netherlands
iSpinoza Centre for Neuroimaging (J.C.W.S.), Amsterdam, the Netherlands
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B.J. MacIntosh
eSunnybrook Research Institute (H.J.M.M.M., B.J.M.), University of Toronto, Toronto, Ontario, Canada
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J. Petr
jHelmholtz Center Dresden-Rossendorf, Institute for Radiopharmaceutic Cancer Research (J.P.), PET Center, Dresden-Rossendorf, Germany.
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R. Fimmers
cInstitut für Medizinische Biometrie, Informatik und Epidemiologie (R.F.), University Hospital Bonn, Bonn, Germany
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H.H. Schild
aFrom the Departments of Radiology (V.C.K., F.T., W.B., H.H.S., E.H.)
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E. Hattingen
aFrom the Departments of Radiology (V.C.K., F.T., W.B., H.H.S., E.H.)
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  • Fig 1.
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    Fig 1.

    Mean CBF during the breath-hold experiment. False color maps of cohort mean cerebral blood flow during 5-minute breath-hold. Selected transverse brain sections of the cohort mean CBF before, during, and after the 5-minute breath-hold challenge. The mean total GM CBF over all participants and over all phases was scaled to 60 mL/100 g/min. Likewise, the mean total WM CBF for all participants over all phases was scaled to 20 mL/100 g/min for WM.

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    Fig 2.

    Cerebral blood flow and partial volume–corrected relative spatial coefficient of variation dynamics. Baseline scan with normal ventilation starts at 0 minutes, the second and third measurement points represent 2 minutes and 30 seconds and 5 minutes of breath-hold, and the fourth and fifth scan phases at 7 minutes and 30 seconds and 10 minutes represent the recovery phase. A, CBF in gray matter voxels only (n = 15 participants, each represented by a color dot). B, The same for white matter only. C, Partial volume–corrected relative spatial coefficient of variation dynamics in gray matter. Y-axis: relative CBF spatial coefficient of variation defined as the ratio of the actual spatial coefficient of variation divided by the spatial coefficient of variation expected on the basis of anatomy (in arbitrary units [au]).

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    Fig 3.

    Relationship of SpO2 and heart rate with CBF. A, Mean GM CBF (colored dots) and mean WM CBF (triangles) are both strongly correlated with absolute SpO2. Color encoding for A and C: green for baseline, orange for 2 minutes and 30 seconds breath-hold, red for 5-minute breath-hold, turquoise after 2 minutes and 30 seconds of recovery, and blue after 5 minutes of recovery. The same WM time points are right below. B, ΔCBF (here measured in GM) similarly correlates well to ΔSpO2 (all 75 single values). C and D, There is no strong correlation between heart rate and CBF in absolute values (C, mean) or ΔCBF and ΔSpO2 (D).

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    Fig 4.

    Scatterplot illustration of the relationship between cumulative breath-hold experience and CBF during the experiment. With the exception of 2 participants (divers 11 and 13, marked with arrows), there is a lower CBF during the experiment with more previous prolonged breath-hold events (cumulative breath-hold, >2 minutes and 30 seconds).

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    Fig 5.

    Energy metabolites and blood gases in brain and venous blood. A, Sample 31P-MR spectrum of 1 participant averaged over 2 minutes and 30 seconds of the late breath-hold phase (above), displayed together with AMARES-fitted spectral components (below). B, Brain pH as assessed by 31P-MR spectroscopy is near-constant during the entire breath-hold experiment. C, The PCr / (ATP + adenosine diphosphate) ratio measured by 31P-MR spectroscopy slightly decreases during breath-hold. D, PCr and β-ATP differences (Δ) from individual baseline values correlate with the pH differences from baseline, indicating that small tendencies toward acidosis and ATP depletion occur during breath-hold. E, Venous blood analyses reveal significant hypoxemia and hypercapnia development (left axis in millimeters of mercury) during breath-hold with fast recovery. Blood glucose (in milligrams/deciliter, left axis) and lactate (in mmol/L, right axis) rose during breath-hold and did not return to baseline. All values are expressed as differences from baseline.

Tables

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  • Anthropometric data of freediver volunteersa

    ParticipantLongest Breath-Hold until MRI (min)Start of Sport (yr before MRI)Estimated Breath-Holds >2 min 30 s per SessionSessions per MonthEstimated Cumulative Lifetime Breath-Holds >2 min 30 sAge (yr)
    110.611.3300.4163231
    25.51.578100836
    35.42.0112420
    45.411.0~08433
    55.02.00.12582440
    65.510.0~04438
    75.08.058384061
    85.51.50.543634
    95.07.0616806447
    106.29.067453626
    115.327.5151679,20064
    126.510.2122811,71251
    135.511.3101621,76035
    145.51.61810342032
    155.05.00.08342050
    Median5.58.068252636.0
    95% CI5.3–5.52.0–11.00.14–12.04.0–9.9630–630032–50
    Minimum5.01.500.41420
    Maximum10.627.5302879,20064
    • ↵a Participants were interviewed concerning the duration (start of sport) and intensity (freediving sessions per month) and the estimated frequency of breath-holding for >2 minutes and 30 seconds per session. The latter could be near zero in freedivers specializing in short high-frequency breath-holds. Some participants breath-held for >2 minutes and 30 seconds only as a qualification for this study; hence, their cumulative lifetime breath-holds of >2 minutes and 30 seconds before MRI were 4, while others very frequently underwent prolonged breath-hold.

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American Journal of Neuroradiology: 39 (10)
American Journal of Neuroradiology
Vol. 39, Issue 10
1 Oct 2018
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V.C. Keil, L. Eichhorn, H.J.M.M. Mutsaerts, F. Träber, W. Block, B. Mädler, K. van de Ven, J.C.W. Siero, B.J. MacIntosh, J. Petr, R. Fimmers, H.H. Schild, E. Hattingen
Cerebrovascular Reactivity during Prolonged Breath-Hold in Experienced Freedivers
American Journal of Neuroradiology Oct 2018, 39 (10) 1839-1847; DOI: 10.3174/ajnr.A5790

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Cerebrovascular Reactivity during Prolonged Breath-Hold in Experienced Freedivers
V.C. Keil, L. Eichhorn, H.J.M.M. Mutsaerts, F. Träber, W. Block, B. Mädler, K. van de Ven, J.C.W. Siero, B.J. MacIntosh, J. Petr, R. Fimmers, H.H. Schild, E. Hattingen
American Journal of Neuroradiology Oct 2018, 39 (10) 1839-1847; DOI: 10.3174/ajnr.A5790
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