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Articles, Neurobiology of Disease

Inspiration Is the Major Regulator of Human CSF Flow

Steffi Dreha-Kulaczewski, Arun A. Joseph, Klaus-Dietmar Merboldt, Hans-Christoph Ludwig, Jutta Gärtner and Jens Frahm
Journal of Neuroscience 11 February 2015, 35 (6) 2485-2491; DOI: https://doi.org/10.1523/JNEUROSCI.3246-14.2015
Steffi Dreha-Kulaczewski
1Department of Pediatrics and Adolescent Medicine, Division of Pediatric Neurology, University Medical Center Göttingen, 37075 Göttingen, Germany,
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Arun A. Joseph
2Biomedizinische NMR Forschungs GmbH am Max-Planck-Institut für biophysikalische Chemie, 37077 Göttingen, Germany,
3DZHK (German Center for Cardiovascular Research), 37075 Göttingen, Germany, and
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Klaus-Dietmar Merboldt
2Biomedizinische NMR Forschungs GmbH am Max-Planck-Institut für biophysikalische Chemie, 37077 Göttingen, Germany,
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Hans-Christoph Ludwig
4Department of Neurosurgery, Division of Pediatric Neurosurgery, University Medical Center Göttingen, 37075 Göttingen, Germany
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Jutta Gärtner
1Department of Pediatrics and Adolescent Medicine, Division of Pediatric Neurology, University Medical Center Göttingen, 37075 Göttingen, Germany,
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Jens Frahm
2Biomedizinische NMR Forschungs GmbH am Max-Planck-Institut für biophysikalische Chemie, 37077 Göttingen, Germany,
3DZHK (German Center for Cardiovascular Research), 37075 Göttingen, Germany, and
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    Figure 1.

    Regions of interest in the CSF ventricular system. Sagittal (A) and coronal (B) T1-weighted images with boxes indicating respective (C, D) magnified representations are shown. Selected regions of interest for the analysis of CSF flow comprise the lateral ventricle (a), third ventricle (b), aqueduct (c), and fourth ventricle (d).

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    Figure 2.

    CSF flow in the aqueduct during normal breathing. The traces represent real-time MRI signal intensity time courses at 50 ms temporal resolution, where relative signal strength (arbitrary units) is proportional to through-plane flow velocity. Although subject 6 (#6, male, 26 years) presents with pronounced cardiac-related pulsations, subjects 7 (#7, male, 43 years) and 8 (#8, male, 25 years) reveal a stronger, though variable, component that reflects a respiratory modulation of CSF flow.

  • Figure 3.
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    Figure 3.

    CSF flow in the third ventricle during forced inspiration. The series of images (magnified views) from top left to bottom right was selected from a real-time MRI movie at 50 ms temporal resolution (every seventh frame, subject 5). The corresponding period of 4.2 s covers one inspiration (2.5 s) in a coronal view through the third ventricle (compare Fig. 1D). Considerable through-plane flow is demonstrated by the marked MRI signal increase in the third ventricle during inspiration (arrow).

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    Figure 4.

    Inspiration drives CSF flow in the third ventricle. MRI signal intensity time courses for subjects 1 (#1, female, 43 years), 5 (#5, male, 19 years), and 6 (#6, male, 26 years) for a protocol comprising normal breathing (10 s) followed by eight periods of forced inspiration (black boxes = 2.5 s) and expiration (2.5 s) are shown. The two columns represent repeated measurements for each subject.

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    Figure 5.

    Inspiration drives CSF flow along the entire ventricular system. MRI signal intensity time courses for subject 7 (male, 43 years) for a protocol comprising normal breathing (10 s) followed by forced inspiration (black boxes = 2.5 s) and expiration (2.5 s) are shown. a, lateral ventricle; b, third ventricle; c, aqueduct; d, fourth ventricle (compare Fig. 1).

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    Figure 6.

    Breath holding abolishes CSF flow in the third ventricle. MRI signal intensity time courses for subjects 1 (#1, female, 43 years), 5 (#5, male, 19 years), and 9 (#9, male, 22 years) for a protocol comprising normal breathing and intermediate breath holding after inspiration (black bar = 12 s) are shown.

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The Journal of Neuroscience: 35 (6)
Journal of Neuroscience
Vol. 35, Issue 6
11 Feb 2015
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Inspiration Is the Major Regulator of Human CSF Flow
Steffi Dreha-Kulaczewski, Arun A. Joseph, Klaus-Dietmar Merboldt, Hans-Christoph Ludwig, Jutta Gärtner, Jens Frahm
Journal of Neuroscience 11 February 2015, 35 (6) 2485-2491; DOI: 10.1523/JNEUROSCI.3246-14.2015

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Inspiration Is the Major Regulator of Human CSF Flow
Steffi Dreha-Kulaczewski, Arun A. Joseph, Klaus-Dietmar Merboldt, Hans-Christoph Ludwig, Jutta Gärtner, Jens Frahm
Journal of Neuroscience 11 February 2015, 35 (6) 2485-2491; DOI: 10.1523/JNEUROSCI.3246-14.2015
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Keywords

  • CSF flow
  • driving force
  • inspiration
  • real-time magnetic resonance imaging
  • respiratory regulation

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  • Possible breakthrough in the study of CSF flow imaging
    Vineeth K. Sukrithan
    Published on: 05 June 2015
  • Published on: (5 June 2015)
    Page navigation anchor for Possible breakthrough in the study of CSF flow imaging
    Possible breakthrough in the study of CSF flow imaging
    • Vineeth K. Sukrithan, MD

    Congratulations to Dreha-Kulaczewski et al. on this novel study measuring CSF flow in real-time without the need for intrathecally injected tracers. The paravascular glymphatic pathway for CSF flow described by Illif et al. (2013) may be critical to our understanding of neurodegenerative diseases. Alzheimer's disease (AD) has been shown to be associated with increase in the size of perivascular space when compared to age mat...

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    Congratulations to Dreha-Kulaczewski et al. on this novel study measuring CSF flow in real-time without the need for intrathecally injected tracers. The paravascular glymphatic pathway for CSF flow described by Illif et al. (2013) may be critical to our understanding of neurodegenerative diseases. Alzheimer's disease (AD) has been shown to be associated with increase in the size of perivascular space when compared to age matched cohorts (Sagare et al. 2012), which implies that this system may be acting like a sink (Nedergaard, 2013) for the removal of misfolded proteins such as beta-amyloid. Perturbations in the functioning of this system may be an important part of the pathophysiology of neuro-degenerative diseases. In this context your study raises some intriguing questions.

    1. If negative intrathoracic pressure is indeed the major driver for CSF flow, is it impeded by mechanical ventilation? Mechanical ventilation has been specifically associated with the occurrence of delirium in the ICU (Shehabi et al., 2010), which has been reported to be associated with long-term cognitive dysfunction on a spectrum similar to AD (Pandharipande et al. 2013). Could reduced CSF flow be the missing link?

    2. Illif et al. (2013), in a murine model, revealed markedly slow CSF efflux kinetics in the pineal recess, olfactory bulb, and hippocampal fissure. Intriguingly, these are regions critical to regulating the sleep cycle and are known to be among the earliest affected in AD. Are CSF flow kinetics at the pineal recess different in the elderly and in patients with AD? The answer to these questions are critical to understanding both ICU-Delirium and the progression of neurodegenerative disease.

    References

    Iliff JJ, Lee H, Yu M, Feng T, Logan J, Nedergaard M, Benveniste H. Brain-wide pathway for waste clearance captured by contrast-enhanced MRI. J Clin Invest. 2013 Mar;123(3):1299-309. doi: 10.1172/JCI67677.

    Nedergaard M. Neuroscience. Garbage truck of the brain. Science. 2013 Jun 28;340(6140):1529-30. doi: 10.1126/science.1240514.

    Pandharipande PP, Girard TD, Ely EW. Long-term cognitive impairment after critical illness. N Engl J Med. 2014 Jan 9;370(2):185-6. doi: 10.1056/NEJMc1313886.

    Sagare AP, Bell RD, Zlokovic BV. Neurovascular dysfunction and faulty amyloid ??-peptide clearance in Alzheimer disease. Cold Spring Harb Perspect Med. 2012 Oct 1;2(10). pii: a011452. doi: 10.1101/cshperspect.a011452.

    Shehabi Y, Riker RR, Bokesch PM, Wisemandle W, Shintani A, Ely EW; SEDCOM (Safety and Efficacy of Dexmedetomidine Compared With Midazolam) Study Group. Delirium duration and mortality in lightly sedated, mechanically ventilated intensive care patients. Crit Care Med. 2010 Dec;38(12):2311-8. doi: 10.1097/CCM.0b013e3181f85759.

    Conflict of Interest:

    None declared

    Show Less
    Competing Interests: None declared.

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