Skip to main content
Top
Published in: Fluids and Barriers of the CNS 1/2020

Open Access 01-12-2020 | Stroke | Research

Extracranial versus intracranial hydro-hemodynamics during aging: a PC-MRI pilot cross-sectional study

Authors: Armelle Lokossou, Serge Metanbou, Catherine Gondry-Jouet, Olivier Balédent

Published in: Fluids and Barriers of the CNS | Issue 1/2020

Login to get access

Abstract

Background

Both aging and changes in blood flow velocity between the extracranial (intraspinal) and intracranial regions of cerebral vessels have an impact on brain hydro-hemodynamics. Arterial and venous cerebral blood flows interact with cerebrospinal fluid (CSF) in the both the cranial and spinal systems. Studies suggest that increased blood and CSF flow pulsatility plays an important role in certain neurological diseases. Here, we investigated the changes in blood-CSF flow pulsatility in the cranial and spinal systems with age as well as the impact of the intracranial compartment on flow patterns.

Method

Phase-contrast magnetic resonance imaging (PC-MRI) was performed in 16 young and 19 elderly healthy volunteers to measure the flows of CSF and blood. CSF stroke volume (SV), blood SV, and arterial and venous pulsatility indexes (PIs) were assessed at intra- and extracranial levels in both samples. Correlations between ventricular and spinal CSF flow, and between blood and CSF flow during aging were also assessed.

Results

There was a significant decrease in arterial cerebral blood flow and intracranial venous cerebral blood flow with aging. We also found a significant increase of intracranial blood SV, spinal CSF SV and arterial/venous pulsatility indexes with aging. In regard to intracranial compartment impact, arterial and venous PIs decreased significantly at intracranial level in elderly volunteers, while young adults exhibited decrease in venous PI only. Intracranial venous PI was paradoxically lower than extracranial venous PI, regardless of age. In both sample groups, spinal CSF SV and aqueductal CSF SV were positively correlated, and so were extracranial blood and spinal CSF SVs.

Conclusion

The study demonstrates that aging changes blood flow but preserves blood and CSF interactions. We also showed that many parameters related to blood and CSF flows differ between young and elderly adults.
Literature
1.
go back to reference Balédent O, Henry-Feugeas MC, Idy-Peretti I. Cerebrospinal fluid dynamics and relation with blood flow: a magnetic resonance study with semiautomated cerebrospinal fluid segmentation. Invest Radiol. 2001;36:368–77.CrossRef Balédent O, Henry-Feugeas MC, Idy-Peretti I. Cerebrospinal fluid dynamics and relation with blood flow: a magnetic resonance study with semiautomated cerebrospinal fluid segmentation. Invest Radiol. 2001;36:368–77.CrossRef
2.
go back to reference Czosnyka, Schuhmann M, Signoretti S, Czosnyka Z, Pickard J. Monitoring of intracranial pressure and assessment of cerebrospinal fluid dynamics. Daniele Rigamonti, The Johns Hopkins University School of Medicine. 2014. Czosnyka, Schuhmann M, Signoretti S, Czosnyka Z, Pickard J. Monitoring of intracranial pressure and assessment of cerebrospinal fluid dynamics. Daniele Rigamonti, The Johns Hopkins University School of Medicine. 2014.
3.
go back to reference Enzmann DR, Pelc NJ. Cerebrospinal fluid flow measured by phase-contrast cine MR. AJNR Am J Neuroradiol. 1993;14:1301–7.PubMed Enzmann DR, Pelc NJ. Cerebrospinal fluid flow measured by phase-contrast cine MR. AJNR Am J Neuroradiol. 1993;14:1301–7.PubMed
4.
go back to reference Alperin NJ, Lee SH, Loth F, Raksin PB, Lichtor T. MR-intracranial pressure (ICP): a method to measure intracranial elastance and pressure noninvasively by means of MR imaging: baboon and human study. Radiology. 2000;217:877–85.CrossRef Alperin NJ, Lee SH, Loth F, Raksin PB, Lichtor T. MR-intracranial pressure (ICP): a method to measure intracranial elastance and pressure noninvasively by means of MR imaging: baboon and human study. Radiology. 2000;217:877–85.CrossRef
5.
go back to reference Stoquart-ElSankari S, Balédent O, Gondry-Jouet C, Makki M, Godefroy O, Meyer M-E. Aging effects on cerebral blood and cerebrospinal fluid flows. J Cereb Blood Flow Metab Off J Int Soc Cereb Blood Flow Metab. 2007;27:1563–72.CrossRef Stoquart-ElSankari S, Balédent O, Gondry-Jouet C, Makki M, Godefroy O, Meyer M-E. Aging effects on cerebral blood and cerebrospinal fluid flows. J Cereb Blood Flow Metab Off J Int Soc Cereb Blood Flow Metab. 2007;27:1563–72.CrossRef
6.
go back to reference Schubert T, Pansini M, Bieri O, Stippich C, Wetzel S, Schaedelin S, et al. Attenuation of blood flow pulsatility along the Atlas slope: a physiologic property of the distal vertebral artery? Am J Neuroradiol. 2015;36:562–7.CrossRef Schubert T, Pansini M, Bieri O, Stippich C, Wetzel S, Schaedelin S, et al. Attenuation of blood flow pulsatility along the Atlas slope: a physiologic property of the distal vertebral artery? Am J Neuroradiol. 2015;36:562–7.CrossRef
7.
go back to reference Wåhlin A, Ambarki K, Birgander R, Malm J, Eklund A. Intracranial pulsatility is associated with regional brain volume in elderly individuals. Neurobiol Aging. 2014;35:365–72.CrossRef Wåhlin A, Ambarki K, Birgander R, Malm J, Eklund A. Intracranial pulsatility is associated with regional brain volume in elderly individuals. Neurobiol Aging. 2014;35:365–72.CrossRef
8.
go back to reference Zarrinkoob L, Ambarki K, Wåhlin A, Birgander R, Carlberg B, Eklund A, et al. Aging alters the dampening of pulsatile blood flow in cerebral arteries. J Cereb Blood Flow Metab Off J Int Soc Cereb Blood Flow Metab. 2016;36:1519–27.CrossRef Zarrinkoob L, Ambarki K, Wåhlin A, Birgander R, Carlberg B, Eklund A, et al. Aging alters the dampening of pulsatile blood flow in cerebral arteries. J Cereb Blood Flow Metab Off J Int Soc Cereb Blood Flow Metab. 2016;36:1519–27.CrossRef
9.
go back to reference Schubert T, Santini F, Stalder AF, Bock J, Meckel S, Bonati L, et al. Dampening of blood-flow pulsatility along the carotid siphon: does form follow function? AJNR Am J Neuroradiol. 2011;32:1107–12.CrossRef Schubert T, Santini F, Stalder AF, Bock J, Meckel S, Bonati L, et al. Dampening of blood-flow pulsatility along the carotid siphon: does form follow function? AJNR Am J Neuroradiol. 2011;32:1107–12.CrossRef
10.
go back to reference Stoquart-Elsankari S, Lehmann P, Villette A, Czosnyka M, Meyer M-E, Deramond H, et al. A phase-contrast MRI study of physiologic cerebral venous flow. J Cereb Blood Flow Metab Off J Int Soc Cereb Blood Flow Metab. 2009;29:1208–15.CrossRef Stoquart-Elsankari S, Lehmann P, Villette A, Czosnyka M, Meyer M-E, Deramond H, et al. A phase-contrast MRI study of physiologic cerebral venous flow. J Cereb Blood Flow Metab Off J Int Soc Cereb Blood Flow Metab. 2009;29:1208–15.CrossRef
11.
go back to reference Bateman GA. Pulse wave encephalopathy: a spectrum hypothesis incorporating Alzheimer’s disease, vascular dementia and normal pressure hydrocephalus. Med Hypotheses. 2004;62:182–7.CrossRef Bateman GA. Pulse wave encephalopathy: a spectrum hypothesis incorporating Alzheimer’s disease, vascular dementia and normal pressure hydrocephalus. Med Hypotheses. 2004;62:182–7.CrossRef
12.
go back to reference Bateman G. Pulse-wave encephalopathy: a comparative study of the hydrodynamics of leukoaraiosis and normal-pressure hydrocephalus. Neuroradiology. 2002;44:740–8.CrossRef Bateman G. Pulse-wave encephalopathy: a comparative study of the hydrodynamics of leukoaraiosis and normal-pressure hydrocephalus. Neuroradiology. 2002;44:740–8.CrossRef
13.
go back to reference El Sankari S, Gondry-Jouet C, Fichten A, Godefroy O, Serot JM, Deramond H, et al. Cerebrospinal fluid and blood flow in mild cognitive impairment and Alzheimer’s disease: a differential diagnosis from idiopathic normal pressure hydrocephalus. Fluids Barriers CNS. 2011;8:12.CrossRef El Sankari S, Gondry-Jouet C, Fichten A, Godefroy O, Serot JM, Deramond H, et al. Cerebrospinal fluid and blood flow in mild cognitive impairment and Alzheimer’s disease: a differential diagnosis from idiopathic normal pressure hydrocephalus. Fluids Barriers CNS. 2011;8:12.CrossRef
14.
go back to reference Lim J-S, Lee JY, Kwon H-M, Lee Y-S. The correlation between cerebral arterial pulsatility and cognitive dysfunction in Alzheimer’s disease patients. J Neurol Sci. 2017;373:285–8.CrossRef Lim J-S, Lee JY, Kwon H-M, Lee Y-S. The correlation between cerebral arterial pulsatility and cognitive dysfunction in Alzheimer’s disease patients. J Neurol Sci. 2017;373:285–8.CrossRef
15.
go back to reference Lemaître H, Crivello F, Grassiot B, Alpérovitch A, Tzourio C, Mazoyer B. Age- and sex-related effects on the neuroanatomy of healthy elderly. NeuroImage. 2005;26:900–11.CrossRef Lemaître H, Crivello F, Grassiot B, Alpérovitch A, Tzourio C, Mazoyer B. Age- and sex-related effects on the neuroanatomy of healthy elderly. NeuroImage. 2005;26:900–11.CrossRef
16.
go back to reference Colon EJ. The elderly brain. A quantitative analysis in the cerebral cortex of two cases. Psychiatr Neurol Neurochir. 1972;75:261–70.PubMed Colon EJ. The elderly brain. A quantitative analysis in the cerebral cortex of two cases. Psychiatr Neurol Neurochir. 1972;75:261–70.PubMed
17.
go back to reference Rijnbeek PR, van Herpen G, Bots ML, Man S, Verweij N, Hofman A, et al. Normal values of the electrocardiogram for ages 16–90 years. J Electrocardiol. 2014;47:914–21.CrossRef Rijnbeek PR, van Herpen G, Bots ML, Man S, Verweij N, Hofman A, et al. Normal values of the electrocardiogram for ages 16–90 years. J Electrocardiol. 2014;47:914–21.CrossRef
18.
go back to reference Alperin N, Lee SH. PUBS: pulsatility-based segmentation of lumens conducting non-steady flow. Magn Reson Med. 2003;49:934–44.CrossRef Alperin N, Lee SH. PUBS: pulsatility-based segmentation of lumens conducting non-steady flow. Magn Reson Med. 2003;49:934–44.CrossRef
19.
go back to reference Burman R, Shah AH, Benveniste R, Jimsheleishvili G, Lee SH, Loewenstein D, et al. Comparing invasive with MRI-derived intracranial pressure measurements in healthy elderly and brain trauma cases: a pilot study: Comparing LPOP and MR-ICP in Controls. J Magn Reson Imaging. 2019. https://doi.org/10.1002/jmri.26695.CrossRefPubMed Burman R, Shah AH, Benveniste R, Jimsheleishvili G, Lee SH, Loewenstein D, et al. Comparing invasive with MRI-derived intracranial pressure measurements in healthy elderly and brain trauma cases: a pilot study: Comparing LPOP and MR-ICP in Controls. J Magn Reson Imaging. 2019. https://​doi.​org/​10.​1002/​jmri.​26695.CrossRefPubMed
20.
go back to reference Lotz J, Meier C, Leppert A, Galanski M. Cardiovascular Flow Measurement with Phase-Contrast MR Imaging: basic Facts and Implementation. RadioGraphics. 2002;22:651–71.CrossRef Lotz J, Meier C, Leppert A, Galanski M. Cardiovascular Flow Measurement with Phase-Contrast MR Imaging: basic Facts and Implementation. RadioGraphics. 2002;22:651–71.CrossRef
21.
go back to reference Bouillot P, Delattre BMA, Brina O, Ouared R, Farhat M, Chnafa C, et al. 3D phase contrast MRI: partial volume correction for robust blood flow quantification in small intracranial vessels: 3D Phase Contrast MRI. Magn Reson Med. 2018;79:129–40.CrossRef Bouillot P, Delattre BMA, Brina O, Ouared R, Farhat M, Chnafa C, et al. 3D phase contrast MRI: partial volume correction for robust blood flow quantification in small intracranial vessels: 3D Phase Contrast MRI. Magn Reson Med. 2018;79:129–40.CrossRef
24.
go back to reference Kim J, Thacker NA, Bromiley PA, Jackson A. Prediction of the jugular venous waveform using a model of CSF dynamics. AJNR Am J Neuroradiol. 2007;28:983–9.PubMed Kim J, Thacker NA, Bromiley PA, Jackson A. Prediction of the jugular venous waveform using a model of CSF dynamics. AJNR Am J Neuroradiol. 2007;28:983–9.PubMed
25.
go back to reference Voyiadjis GZ, Samadi-Dooki A. Hyperelastic modeling of the human brain tissue: effects of no-slip boundary condition and compressibility on the uniaxial deformation. J Mech Behav Biomed Mater. 2018;83:63–78.CrossRef Voyiadjis GZ, Samadi-Dooki A. Hyperelastic modeling of the human brain tissue: effects of no-slip boundary condition and compressibility on the uniaxial deformation. J Mech Behav Biomed Mater. 2018;83:63–78.CrossRef
26.
go back to reference Qvarlander S, Ambarki K, Wåhlin A, Jacobsson J, Birgander R, Malm J, et al. Cerebrospinal fluid and blood flow patterns in idiopathic normal pressure hydrocephalus. Acta Neurol Scand. 2017;135:576–84.CrossRef Qvarlander S, Ambarki K, Wåhlin A, Jacobsson J, Birgander R, Malm J, et al. Cerebrospinal fluid and blood flow patterns in idiopathic normal pressure hydrocephalus. Acta Neurol Scand. 2017;135:576–84.CrossRef
27.
go back to reference Henry-Feugeas MC, Idy-Peretti I, Baledent O, Cornu P, Lejay H, Bittoun J, et al. Cerebrospinal fluid flow waveforms: MR analysis in chronic adult hydrocephalus. Invest Radiol. 2001;36:146–54.CrossRef Henry-Feugeas MC, Idy-Peretti I, Baledent O, Cornu P, Lejay H, Bittoun J, et al. Cerebrospinal fluid flow waveforms: MR analysis in chronic adult hydrocephalus. Invest Radiol. 2001;36:146–54.CrossRef
28.
go back to reference Fall S, Pagé G, Bettoni J, Bouzerar R, Balédent O. Use of phase-contrast MRA to assess intracranial venous sinus resistance to drainage in healthy individuals. AJNR Am J Neuroradiol. 2017;38:281–7.CrossRef Fall S, Pagé G, Bettoni J, Bouzerar R, Balédent O. Use of phase-contrast MRA to assess intracranial venous sinus resistance to drainage in healthy individuals. AJNR Am J Neuroradiol. 2017;38:281–7.CrossRef
29.
go back to reference Brown WR, Thore CR. Review: cerebral microvascular pathology in ageing and neurodegeneration: Cerebral microvascular pathology. Neuropathol Appl Neurobiol. 2011;37:56–74.CrossRef Brown WR, Thore CR. Review: cerebral microvascular pathology in ageing and neurodegeneration: Cerebral microvascular pathology. Neuropathol Appl Neurobiol. 2011;37:56–74.CrossRef
30.
go back to reference Bateman GA, Siddique SH. Cerebrospinal fluid absorption block at the vertex in chronic hydrocephalus: obstructed arachnoid granulations or elevated venous pressure? Fluids Barriers CNS. 2014;11:11.CrossRef Bateman GA, Siddique SH. Cerebrospinal fluid absorption block at the vertex in chronic hydrocephalus: obstructed arachnoid granulations or elevated venous pressure? Fluids Barriers CNS. 2014;11:11.CrossRef
31.
go back to reference Uflacker R. Atlas of vascular anatomy. an angiographic approach. Philadephia: Lippincot, Williams and Wilkins; 1997. Uflacker R. Atlas of vascular anatomy. an angiographic approach. Philadephia: Lippincot, Williams and Wilkins; 1997.
32.
go back to reference Alperin N, Hushek SG, Lee SH, Sivaramakrishnan A, Lichtor T. MRI study of cerebral blood flow and CSF flow dynamics in an upright posture: the effect of posture on the intracranial compliance and pressure. Acta Neurochir Suppl. 2005;95:177–81.CrossRef Alperin N, Hushek SG, Lee SH, Sivaramakrishnan A, Lichtor T. MRI study of cerebral blood flow and CSF flow dynamics in an upright posture: the effect of posture on the intracranial compliance and pressure. Acta Neurochir Suppl. 2005;95:177–81.CrossRef
34.
go back to reference Bateman GA. Vascular compliance in normal pressure hydrocephalus. AJNR Am J Neuroradiol. 2000;21:1574–85.PubMed Bateman GA. Vascular compliance in normal pressure hydrocephalus. AJNR Am J Neuroradiol. 2000;21:1574–85.PubMed
35.
go back to reference Beggs CB. Venous hemodynamics in neurological disorders: an analytical review with hydrodynamic analysis. BMC Med. 2013;11:142.CrossRef Beggs CB. Venous hemodynamics in neurological disorders: an analytical review with hydrodynamic analysis. BMC Med. 2013;11:142.CrossRef
36.
go back to reference Sisini F, Toro E, Gambaccini M, Zamboni P. The oscillating component of the internal jugular vein flow: the overlooked element of cerebral circulation. Behav Neurol. 2015;2015:170756.CrossRef Sisini F, Toro E, Gambaccini M, Zamboni P. The oscillating component of the internal jugular vein flow: the overlooked element of cerebral circulation. Behav Neurol. 2015;2015:170756.CrossRef
37.
go back to reference Mitchell GF, Gudnason V, Launer LJ, Aspelund T, Harris TB. Hemodynamics of increased pulse pressure in older women in the community-based age. Gene/Environment Susceptibility-Reykjavik Study. Hypertension. 2008;51:1123–8.CrossRef Mitchell GF, Gudnason V, Launer LJ, Aspelund T, Harris TB. Hemodynamics of increased pulse pressure in older women in the community-based age. Gene/Environment Susceptibility-Reykjavik Study. Hypertension. 2008;51:1123–8.CrossRef
38.
go back to reference Levy Nogueira M, Lafitte O, Steyaert J-M, Bakardjian H, Dubois B, Hampel H, et al. Mechanical stress related to brain atrophy in Alzheimer’s disease. Alzheimers Dement. 2016;12:11–20.CrossRef Levy Nogueira M, Lafitte O, Steyaert J-M, Bakardjian H, Dubois B, Hampel H, et al. Mechanical stress related to brain atrophy in Alzheimer’s disease. Alzheimers Dement. 2016;12:11–20.CrossRef
39.
go back to reference Mitchell GF, Vita JA, Larson MG, Parise H, Keyes MJ, Warner E, et al. Cross-sectional relations of peripheral microvascular function, cardiovascular disease risk factors, and aortic stiffness: the framingham heart study. Circulation. 2005;112:3722–8.CrossRef Mitchell GF, Vita JA, Larson MG, Parise H, Keyes MJ, Warner E, et al. Cross-sectional relations of peripheral microvascular function, cardiovascular disease risk factors, and aortic stiffness: the framingham heart study. Circulation. 2005;112:3722–8.CrossRef
40.
go back to reference Del Corso L, Moruzzo D, Conte B, Agelli M, Romanelli AM, Pastine F, et al. Tortuosity, kinking, and coiling of the carotid artery: expression of atherosclerosis or aging? Angiology. 1998;49:361–71.CrossRef Del Corso L, Moruzzo D, Conte B, Agelli M, Romanelli AM, Pastine F, et al. Tortuosity, kinking, and coiling of the carotid artery: expression of atherosclerosis or aging? Angiology. 1998;49:361–71.CrossRef
41.
go back to reference Eide PK. The correlation between pulsatile intracranial pressure and indices of intracranial pressure–volume reserve capacity: results from ventricular infusion testing. J Neurosurg. 2016;125:1–11.CrossRef Eide PK. The correlation between pulsatile intracranial pressure and indices of intracranial pressure–volume reserve capacity: results from ventricular infusion testing. J Neurosurg. 2016;125:1–11.CrossRef
42.
go back to reference Craven C, Toma AK, Khan AA, Watkins LD. The role of ICP monitoring in patients with persistent cerebrospinal fluid leak following spinal surgery: a case series. Acta Neurochir Wien. 2016;158:1813–9.CrossRef Craven C, Toma AK, Khan AA, Watkins LD. The role of ICP monitoring in patients with persistent cerebrospinal fluid leak following spinal surgery: a case series. Acta Neurochir Wien. 2016;158:1813–9.CrossRef
43.
go back to reference Al Khaja KAJ, James H, Veeramuthu S, Tayem YI, Sridharan K, Sequeira RP. Antihypertensive Prescribing Pattern in Older Adults: implications of Age and the Use of Dual Single-Pill Combinations. High Blood Press Cardiovasc Prev. 2019;26:535–44.CrossRef Al Khaja KAJ, James H, Veeramuthu S, Tayem YI, Sridharan K, Sequeira RP. Antihypertensive Prescribing Pattern in Older Adults: implications of Age and the Use of Dual Single-Pill Combinations. High Blood Press Cardiovasc Prev. 2019;26:535–44.CrossRef
44.
go back to reference Sartoretti T, Wyss M, Sartoretti E, Reischauer C, Hainc N, Graf N, et al. Sex and age dependencies of aqueductal cerebrospinal fluid dynamics parameters in healthy subjects. Front Aging Neurosci. 2019;11:199.CrossRef Sartoretti T, Wyss M, Sartoretti E, Reischauer C, Hainc N, Graf N, et al. Sex and age dependencies of aqueductal cerebrospinal fluid dynamics parameters in healthy subjects. Front Aging Neurosci. 2019;11:199.CrossRef
45.
go back to reference Azhim A, Akioka K, Akutagawa M, Hirao Y, Yoshizaki K, Obara S, et al. Effect of Gender on Blood Flow Velocities and Blood Pressure: Role of Body Weight and Height. 2007 29th Annu Int Conf IEEE Eng Med Biol Soc. Lyon, France: IEEE; 2007. p. 967–70. http://ieeexplore.ieee.org/document/4352453/. Accessed 12 Dec 2019. Azhim A, Akioka K, Akutagawa M, Hirao Y, Yoshizaki K, Obara S, et al. Effect of Gender on Blood Flow Velocities and Blood Pressure: Role of Body Weight and Height. 2007 29th Annu Int Conf IEEE Eng Med Biol Soc. Lyon, France: IEEE; 2007. p. 967–70. http://​ieeexplore.​ieee.​org/​document/​4352453/​. Accessed 12 Dec 2019.
Metadata
Title
Extracranial versus intracranial hydro-hemodynamics during aging: a PC-MRI pilot cross-sectional study
Authors
Armelle Lokossou
Serge Metanbou
Catherine Gondry-Jouet
Olivier Balédent
Publication date
01-12-2020
Publisher
BioMed Central
Keyword
Stroke
Published in
Fluids and Barriers of the CNS / Issue 1/2020
Electronic ISSN: 2045-8118
DOI
https://doi.org/10.1186/s12987-019-0163-4

Other articles of this Issue 1/2020

Fluids and Barriers of the CNS 1/2020 Go to the issue