Skip to main content

Advertisement

SpringerLink
Log in

Measurement of choroid plexus perfusion using dynamic susceptibility MR imaging: capillary permeability and age-related changes

  • Functional Neuroradiology
  • Published:
Neuroradiology Aims and scope Submit manuscript

Abstract

Introduction

The cerebrospinal fluid (CSF) plays a major role in the physiology of the central nervous system. The continuous turnover of CSF is mainly attributed to the highly vascularized choroid plexus (CP) located in the cerebral ventricles which represent a complex interface between blood and CSF. We propose a method for evaluating CP functionality in vivo using perfusion MR imaging and establish the age-related changes of associated parameters.

Methods

Fifteen patients with small intracranial tumors were retrospectively studied. MR Imaging was performed on a 3T MR Scanner. Gradient-echo echo planar images were acquired after bolus injection of gadolinium-based contrast agent (CA). The software developed used the combined T1- and T2-effects. The decomposition of the relaxivity signals enables the calculation of the CP capillary permeability (K2). The relative cerebral blood volume (rCBV), mean transit time (MTT), and signal slope decrease (SSD) were also calculated.

Results

The mean permeability K2 of the extracted CP was 0.033+/−0.18 s-1. K2 and SSD significantly decreased with subject’s age whereas MTT significantly increased with subject’s age. No significant correlation was found for age-related changes in rCBV and rCBF.

Conclusion

The decrease in CP permeability is in line with the age-related changes in CSF secretion observed in animals. The MTT increase indicates significant structural changes corroborated by microscopy studies in animals or humans. Overall, DSC MR-perfusion enables an in vivo evaluation of the hemodynamic state of CP. Clinical applications such as neurodegenerative diseases could be considered thanks to specific functional studies of CP.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Czosnyka Z, Owler B, Keong N, Santarius T, Baledent O, Pickard JD, Czosnyka M (2011) Impact of duration of symptoms on CSF dynamics in idiopathic normal pressure hydrocephalus. Acta Neurol Scand 123:414–418

    Article  PubMed  CAS  Google Scholar 

  2. Serot JM, Peltier J, Fichten A, Ledeme N, Bourgeois AM, Jouanny P, Toussaint P, Legars D, Godefroy O, Maziere JC (2011) Reduced CSF turnover and decreased ventricular Abeta42 levels are related. BMC Neurosci 12:42

    Article  PubMed  CAS  Google Scholar 

  3. Silverberg GD, Heit G, Huhn S, Jaffe RA, Chang SD, Bronte-Stewart H, Rubenstein E, Possin K, Saul TA (2001) The cerebrospinal fluid production rate is reduced in dementia of the Alzheimer’s type. Neurology 57:1763–1766

    Article  PubMed  CAS  Google Scholar 

  4. Silverberg GD, Mayo M, Saul T, Rubenstein E, McGuire D (2003) Alzheimer’s disease, normal-pressure hydrocephalus, and senescent changes in CSF circulatory physiology: a hypothesis. Lancet Neurol 2:506–511

    Article  PubMed  Google Scholar 

  5. Redzic ZB, Segal MB (2004) The structure of the choroid plexus and the physiology of the choroid plexus epithelium. Adv Drug Deliv Rev 56:1695–1716

    Article  PubMed  CAS  Google Scholar 

  6. Faraci FM, Mayhan WG, Williams JK, Heistad DD (1988) Effects of vasoactive stimuli on blood flow to choroid plexus. Am J Physiol 254:H286–H291

    PubMed  CAS  Google Scholar 

  7. Redzic ZB, Preston JE, Duncan JA, Chodobski A, Szmydynger-Chodobska J (2005) The choroid plexus-cerebrospinal fluid system: from development to aging. Curr Top Dev Biol 71:1–52

    Article  PubMed  CAS  Google Scholar 

  8. Tauc M, Vignon X, Bouchaud C (1984) Evidence for the effectiveness of the blood–CSF barrier in the fetal rat choroid plexus. A freeze-fracture and peroxidase diffusion study. Tissue Cell 16:65–74

    Article  PubMed  CAS  Google Scholar 

  9. Zheng W, Blaner WS, Zhao Q (1999) Inhibition by lead of production and secretion of transthyretin in the choroid plexus: its relation to thyroxine transport at blood-CSF barrier. Toxicol Appl Pharmacol 155:24–31

    Article  PubMed  CAS  Google Scholar 

  10. Deane R, Segal MB (1985) The transport of sugars across the perfused choroid plexus of the sheep. J Physiol 362:245–260

    PubMed  CAS  Google Scholar 

  11. Chen RL, Kassem NA, Redzic ZB, Chen CP, Segal MB, Preston JE (2009) Age-related changes in choroid plexus and blood–cerebrospinal fluid barrier function in the sheep. Exp Gerontol 44:289–296

    Article  PubMed  CAS  Google Scholar 

  12. May C, Kaye JA, Atack JR, Schapiro MB, Friedland RP, Rapoport SI (1990) Cerebrospinal fluid production is reduced in healthy aging. Neurology 40:500–503

    Article  PubMed  CAS  Google Scholar 

  13. Gideon P, Thomsen C, Stahlberg F, Henriksen O (1994) Cerebrospinal fluid production and dynamics in normal aging: a MRI phase-mapping study. Acta Neurol Scand 89:362–366

    Article  PubMed  CAS  Google Scholar 

  14. Serot JM, Bene MC, Faure GC (2003) Choroid plexus, aging of the brain, and Alzheimer’s disease. Front Biosci 8:515–521

    Article  Google Scholar 

  15. Serot JM, Bene MC, Foliguet B, Faure GC (2000) Morphological alterations of the choroid plexus in late-onset Alzheimer’s disease. Acta Neuropathol 99:105–108

    Article  PubMed  CAS  Google Scholar 

  16. Bouzerar R, Chaarani B, Pottie O, Gondry-Jouet C, Zmudka J, Serot JM, Baledent O (2012) Imaging of the choroid plexus using perfusion MR imaging: is it possible? Paper presented at the ISMRM 20th Annual Meeting, Melbourne, Australia, 5–11 May

  17. Sorensen AG, Tievsky AL, Ostergaard L, Weisskoff RM, Rosen BR (1997) Contrast agents in functional MR imaging. J Magn Reson Imaging 7:47–55

    Article  PubMed  CAS  Google Scholar 

  18. Boxerman JL, Schmainda KM, Weisskoff RM (2006) Relative cerebral blood volume maps corrected for contrast agent extravasation significantly correlate with glioma tumor grade, whereas uncorrected maps do not. AJNR Am J Neuroradiol 27:859–867

    PubMed  CAS  Google Scholar 

  19. Donahue KM, Krouwer HG, Rand SD, Pathak AP, Marszalkowski CS, Censky SC, Prost RW (2000) Utility of simultaneously acquired gradient-echo and spin-echo cerebral blood volume and morphology maps in brain tumor patients. Magn Reson Med 43:845–853

    Article  PubMed  CAS  Google Scholar 

  20. Benner T, Heiland S, Erb G, Forsting M, Sartor K (1997) Accuracy of gamma-variate fits to concentration-time curves from dynamic susceptibility-contrast enhanced MRI: influence of time resolution, maximal signal drop and signal-to-noise. Magn Reson Imaging 15:307–317

    Article  PubMed  CAS  Google Scholar 

  21. Knopp EA, Cha S, Johnson G, Mazumdar A, Golfinos JG, Zagzag D, Miller DC, Kelly PJ, Kricheff II (1999) Glial neoplasms: dynamic contrast-enhanced T2*-weighted MR imaging. Radiology 211:791–798

    Article  PubMed  CAS  Google Scholar 

  22. Press WH, Teukolsky SA, Vetterling WT, Flannery BP (eds) (2007) Numerical recipes: the art of scientific computing. Third Edition edn. Cambridge University Press, New-York

    Google Scholar 

  23. Yeom KW, Mitchell LA, Lober RM, Barnes PD, Vogel H, Fisher PG, Edwards MS (2013) Arterial spin-labeled perfusion of pediatric brain tumors. AJNR Am J Neuroradiol. doi:10.3174/ajnr.A3670

    Google Scholar 

  24. Zimny A, Sasiadek M (2011) Contribution of perfusion-weighted magnetic resonance imaging in the differentiation of meningiomas and other extra-axial tumors: case reports and literature review. J Neurooncol 103:777–783

    Article  PubMed  Google Scholar 

  25. Ances BM, Liang CL, Leontiev O, Perthen JE, Fleisher AS, Lansing AE, Buxton RB (2009) Effects of aging on cerebral blood flow, oxygen metabolism, and blood oxygenation level dependent responses to visual stimulation. Hum Brain Mapp 30:1120–1132

    Article  PubMed  Google Scholar 

  26. Restom K, Bangen KJ, Bondi MW, Perthen JE, Liu TT (2007) Cerebral blood flow and BOLD responses to a memory encoding task: a comparison between healthy young and elderly adults. Neuroimage 37:430–439

    Article  PubMed  Google Scholar 

  27. Asllani I, Habeck C, Borogovac A, Brown TR, Brickman AM, Stern Y (2009) Separating function from structure in perfusion imaging of the aging brain. Hum Brain Mapp 30:2927–2935

    Article  PubMed  Google Scholar 

  28. Martin AJ, Friston KJ, Colebatch JG, Frackowiak RS (1991) Decreases in regional cerebral blood flow with normal aging. J Cereb Blood Flow Metab 11:684–689

    Article  PubMed  CAS  Google Scholar 

  29. Stoquart-ElSankari S, Baledent O, Gondry-Jouet C, Makki M, Godefroy O, Meyer ME (2007) Aging effects on cerebral blood and cerebrospinal fluid flows. J Cereb Blood Flow Metab 27:1563–1572

    Article  PubMed  Google Scholar 

  30. Good CD, Johnsrude IS, Ashburner J, Henson RN, Friston KJ, Frackowiak RS (2001) A voxel-based morphometric study of ageing in 465 normal adult human brains. Neuroimage 14:21–36

    Article  PubMed  CAS  Google Scholar 

  31. Williams DS, Detre JA, Leigh JS, Koretsky AP (1992) Magnetic resonance imaging of perfusion using spin inversion of arterial water. Proc Natl Acad Sci USA 89:212–216

    Article  PubMed  CAS  Google Scholar 

  32. Carr JP, Buckley DL, Tessier J, Parker GJ (2007) What levels of precision are achievable for quantification of perfusion and capillary permeability surface area product using ASL? Magn Reson Med 58:281–289

    Article  PubMed  Google Scholar 

  33. van Gelderen P, de Zwart JA, Duyn JH (2008) Pittfalls of MRI measurement of white matter perfusion based on arterial spin labeling. Magn Reson Med 59:788–795

    Article  PubMed  Google Scholar 

  34. Rmeily-Haddad M, Baledent O, Stoquart El Sankari S, Serot JM, Bailly P, Meyer ME (2011) The kinetics of 18f-fluorodeoxyglucose uptake in the choroid plexus. Int J Imaging Syst Technol 21:107–114

    Article  Google Scholar 

  35. Farrall AJ, Wardlaw JM (2009) Blood-brain barrier: ageing and microvascular disease—systematic review and meta-analysis. Neurobiol Aging 30:337–352

    Article  PubMed  CAS  Google Scholar 

  36. Shu Y, Liu M, Chen S, Chen X, Wang J (2011) New insight into molecular interactions of imidazolium ionic liquids with bovine serum albumin. J Phys Chem B 115:12306–12314

    Article  PubMed  CAS  Google Scholar 

  37. Serot JM, Foliguet B, Bene MC, Faure GC (2001) Choroid plexus and ageing in rats: a morphometric and ultrastructural study. Eur J Neurosci 14:794–798

    Article  PubMed  CAS  Google Scholar 

  38. Masseguin C, LePanse S, Corman B, Verbavatz JM, Gabrion J (2005) Aging affects choroidal proteins involved in CSF production in Sprague-Dawley rats. Neurobiol Aging 26:917–927

    Article  PubMed  CAS  Google Scholar 

  39. Gerrits PO, Kortekaas R, de Weerd H, Luiten PG, van der Want JJ, Veening JG (2013) Spumiform basement membrane aberrations in the microvasculature of the midbrain periaqueductal gray region in hamster: rostro-caudal pathogenesis? Neuroscience 228:128–138

    Article  PubMed  CAS  Google Scholar 

  40. Gerrits PO, Kortekaas R, de Weerd H, Veenstra-Algra A, Luiten PG, van der Want JJ, Veening JG (2013) Spumiform capillary basement membrane swelling: a new type of microvascular degeneration in senescent hamster. Neurobiol Aging 34:1277–1286

    Article  PubMed  CAS  Google Scholar 

  41. Preston JE (2001) Ageing choroid plexus-cerebrospinal fluid system. Microsc Res Tech 52:31–37

    Article  PubMed  CAS  Google Scholar 

  42. Bersani G, Garavini A, Taddei I, Tanfani G, Pancheri P (1999) Choroid plexus calcification as a possible clue of serotonin implication in schizophrenia. Neurosci Lett 259:169–172

    Article  PubMed  CAS  Google Scholar 

  43. Farkas E, De Vos RA, Jansen Steur EN, Luiten PG (2000) Are Alzheimer’s disease, hypertension, and cerebrocapillary damage related? Neurobiol Aging 21:235–243

    Article  PubMed  CAS  Google Scholar 

  44. Ostergaard L, Aamand R, Gutierrez-Jimenez E, Ho YC, Blicher JU, Madsen SM, Nagenthiraja K, Dalby RB, Drasbek KR, Moller A, Braendgaard H, Mouridsen K, Jespersen SN, Jensen MS, West MJ (2013) The capillary dysfunction hypothesis of Alzheimer’s disease. Neurobiol Aging 34:1018–1031

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

MRI operators at University Hospital, Amiens, France, are gratefully acknowledged for their technical contribution.

Conflict of Interest

We declare that we have no conflict of interest.

Author information

Authors and Affiliations

  1. Image Processing Department, University Hospital, CHU Nord Place Victor Pauchet, 80054, Amiens, France

    Roger Bouzerar, Bader Chaarani & Olivier Balédent

  2. Radiology Department, University Hospital, Amiens, France

    Catherine Gondry-Jouet

  3. Geriatric Unit, University Hospital, Amiens, France

    Jadwiga Zmudka

Authors
  1. Roger Bouzerar
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Bader Chaarani
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Catherine Gondry-Jouet
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jadwiga Zmudka
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Olivier Balédent
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Roger Bouzerar.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bouzerar, R., Chaarani, B., Gondry-Jouet, C. et al. Measurement of choroid plexus perfusion using dynamic susceptibility MR imaging: capillary permeability and age-related changes. Neuroradiology 55, 1447–1454 (2013). https://doi.org/10.1007/s00234-013-1290-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00234-013-1290-2

Keywords

Search

Navigation