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Upward movement of cerebrospinal fluid in obstructive hydrocephalus—revision of an old concept

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Abstract

Purpose

The specific pathophysiological processes in many forms of obstructive hydrocephalus (HC) are still unclear. Current concepts of cerebrospinal fluid (CSF) dynamics presume a constant downward flow from the lateral ventricles towards subarachnoid spaces, which are in contrast to neurosurgical observations and findings of MRI flow studies. The aim of our study was to analyze CSF movements in patients with obstructive HC by neuroendoscopic video recordings, X-ray studies, and MRI.

Methods

One hundred seventeen pediatric patients with obstructive HC who underwent neuroendoscopy in our center were included. Video recordings were analyzed in 85 patients. Contrast-enhanced X-rays were conducted during surgery prior to intervention in 75 patients, and flow void signals on pre-operative MRI could be evaluated in 110 patients.

Results

In 83.5% of the video recordings, CSF moved upwards synchronous to inspiration superimposed by cardiac pulsation. Application of contrast medium revealed a flow delay in 52% of the X-ray studies prior to neurosurgery, indicating hindered CSF circulation. The appearances and shapes of flow void signals in 88.2% of the pre-operative MRI studies suggested valve-like mechanisms and entrapment of CSF.

Conclusions

Neuroendoscopic observations in patients with obstructive HC revealed upward CSF movements and the corresponding MRI signs of trapped CSF in brain cavities. These observations are in contrast to the current pathophysiological concept of obstructive HC. However, recent real-time flow MRI studies demonstrated upward movement of CSF, hence support our clinical findings. The knowledge of cranial-directed CSF flow expands our understanding of pathophysiological mechanisms in HC and is the key to effective treatment.

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References

  1. Bhadelia RA, Madan N, Zhao Y, Wagshul ME, Heilman C, Butler JP, Patz S (2013) Physiology-based MR imaging assessment of CSF flow at the foramen magnum with a valsalva maneuver. Am J Neuroradiol 34(9):1857–1862

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Bock HC, Kanzler M, Thomale U-W, Ludwig H-C (2018) Implementing a digital real-time hydrocephalus and shunt registry to evaluate contemporary pattern of care and surgical outcome in pediatric hydrocephalus. Childs Nerv Syst 34(3):457–464

    Article  PubMed  Google Scholar 

  3. Boulton M, Flessner M, Armstrong D, Hay J, Johnston M (1998) Determination of volumetric cerebrospinal fluid absorption into extracranial lymphatics in sheep. Am J Phys 274(1 Pt 2):R88–R96

    CAS  Google Scholar 

  4. Chen L, Beckett A, Verma A, Feinberg DA (2015) Dynamics of respiratory and cardiac CSF motion revealed with real-time simultaneous multi-slice EPI velocity phase contrast imaging. Neuroimage 122(C):281–287

    Article  PubMed  Google Scholar 

  5. Chen L, Elias G, Yostos MP, Stimec B, Fasel J, Murphy K (2014) Pathways of cerebrospinal fluid outflow: a deeper understanding of resorption. Neuroradiology 57(2):139–147

    Article  PubMed  Google Scholar 

  6. Dandy WE (1919) Experimental hydrocephalus. Ann Surg 70:129–142

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Dandy WE (1938) The operative treatment of communicating hydrocephalus. Ann Surg 108:194–202

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Delaidelli A, Moiraghi A (2017) Respiration: a new mechanism for CSF circulation? J Neurosci 37(30):7076–7078

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Di Rocco C, Pettorossi VE, Caldarelli M, Mancinelli R, Velardi F (1978) Communicating hydrocephalus induced by mechanically increased amplitude of the intraventricular cerebrospinal fluid pressure: experimental studies. Exp Neurol 59:40–52

    Article  PubMed  Google Scholar 

  10. Dreha-Kulaczewski S, Joseph AA, Merboldt K-D, Ludwig H-C, Gärtner J, Frahm J (2015) Inspiration is the major regulator of human CSF flow. J Neurosci 35(6):2485–2491

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Dreha-Kulaczewski S, Joseph AA, Merboldt K-D, Ludwig H-C, Gärtner J, Frahm J (2017) Identification of the upward movement of human cerebrospinal fluid in vivo and its relation to the brain venous system. J Neurosci 37(9):2754–16–2402

    Article  Google Scholar 

  12. Dreha-Kulaczewski S, Konopka M, Joseph AA, Kollmeier J, Merboldt K-D, Ludwig H-C, Gärtner J, Frahm J (2018) Respiration and the watershed of spinal CSF flow in humans. Sci Rep 8(1):5594–5597

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Edsbagge M, Tisell M, Jacobsson L, Wikkelsö C (2004) Spinal CSF absorption in healthy individuals. Am J Physiol Regul Integr Comp Physiol 287(6):R1450–R1455

    Article  CAS  PubMed  Google Scholar 

  14. Faubel R, Westendorf C, Bodenschatz E, Eichele G (2016) Cilia-based flow network in the brain ventricles. Science 353(6295):1–4

    Article  CAS  Google Scholar 

  15. Foerster P, Daclin M, Asm S, Faucourt M, Boletta A, Genovesio A, Spassky N (2017) mTORC1 signaling and primary cilia are required for brain ventricle morphogenesis. Development 144(2):201–210

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Friese S, Hamhaber U, Erb M, Klose U (2004) B-waves in cerebral and spinal cerebrospinal fluid pulsation measurement by magnetic resonance imaging. J Comput Assist Tomogr 28(2):255–262

    Article  PubMed  Google Scholar 

  17. Funk DJ, Jacobsohn E, Kumar A (2013) The role of venous return in critical illness and shock-part I: physiology. Crit Care Med 41(1):255–262

    Article  PubMed  Google Scholar 

  18. Greitz D (1993) Cerebrospinal fluid circulation and associated intracranial dynamics. A radiologic investigation using MR imaging and radionuclide cisternography. Acta Radiol Suppl 386:1–23

    CAS  PubMed  Google Scholar 

  19. Greitz D, Wirestam R, Franck A, Nordell B, Thomsen C, Ståhlberg F (1992) Pulsatile brain movement and associated hydrodynamics studied by magnetic resonance phase imaging. The Monro-Kellie doctrine revisited. Neuroradiology 34(5):370–380

    Article  CAS  PubMed  Google Scholar 

  20. Greitz D (2004) The hydrodynamic hypothesis versus the bulk flow hypothesis. Neurosurg Rev 27(4):1–2

    Article  Google Scholar 

  21. Kelly EJ, Yamada S (2016) Cerebrospinal fluid flow studies and recent advancements. Semin Ultrasound CT MRI 37:92–99

    Article  Google Scholar 

  22. Klarica M, Oresković D, Bozić B, Vukić M, Butković V, Bulat M (2009) New experimental model of acute aqueductal blockage in cats: effects on cerebrospinal fluid pressure and the size of brain ventricles. NSC 158(4):1397–1405

    CAS  Google Scholar 

  23. Klose U, Strik C, Kiefer C, Grodd W (2000) Detection of a relation between respiration and CSF pulsation with an echoplanar technique. J Magn Reson Imaging 11(4):438–444

    Article  CAS  PubMed  Google Scholar 

  24. Ludwig HC, Kruschat T, Knobloch T, Teichmann H-O, Rostasy K, Rohde V (2007) First experiences with a 2.0-microm near infrared laser system for neuroendoscopy. Neurosurg Rev 30(3):195–201– discussion 201

    Article  CAS  PubMed  Google Scholar 

  25. Ludwig HC, M K, Timmermann A, Weyland W (2000) The influence of airway pressure changes on intracranial pressure (ICP) and the blood flow velocity in the middle cerebral artery (VMCA). Anasthesiol Intensivmed Notfallmed Schmerzthe 35:141–145

    Article  CAS  Google Scholar 

  26. Murtha LA, Yang Q, Parsons MW, Levi CR, Beard DJ, Spratt NJ, McLeod DD (2014) Cerebrospinal fluid is drained primarily via the spinal canal and olfactory route in young and aged spontaneously hypertensive rats. Fluids Barriers CNS 11(1):12

    Article  PubMed  PubMed Central  Google Scholar 

  27. Novak R, Matuschak GM, Pinsky M (1988) Effect of positive-pressure ventilatory frequency on regional pleural pressure. J Appl Physiol 65:1314–1323

    Article  CAS  PubMed  Google Scholar 

  28. Oi S, Di Rocco C (2006) Proposal of “evolution theory in cerebrospinal fluid dynamics” and minor pathway hydrocephalus in developing immature brain. Childs Nerv Syst 22(7):662–669

    Article  PubMed  Google Scholar 

  29. Pettorossi VE, Di Rocco C, Mancinelli R, Caldarelli M, Velardi F (1978) Communicating hydrocephalus induced by mechanically increased amplitude of the intraventricular cerebrospinal fluid pulse pressure: rationale and method. Exp Neurol 59:30–39

    Article  CAS  PubMed  Google Scholar 

  30. Qvarlander S, Ambarki K, Wåhlin A, Jacobsson J, Birgander R, Malm J, Eklund A (2016) Cerebrospinal fluid and blood flow patterns in idiopathic normal pressure hydrocephalus. Acta Neurol Scand 135(5):576–584

    Article  PubMed  Google Scholar 

  31. Reitan H (2013) On movements of fluid inside the cerebro-spinal space. Acta Radiol Orig Ser 22(5–6):762–779

    Google Scholar 

  32. Ringstad G, Vatnehol SAS, Eide PK (2017) Glymphatic MRI in idiopathic normal pressure hydrocephalus. Brain 140(10):2691–2705

    Article  PubMed  PubMed Central  Google Scholar 

  33. Schuhmann MU, Kural C, Lalla L, Ebner FH, Bock C, Ludwig H-C (2019) 2-micron continuous wave laser assisted neuroendoscopy: clinical experience of two institutions in 524 procedures. World Neurosurg 122:e81–e88

    Article  PubMed  Google Scholar 

  34. Spijkerman JM, Geurts LJ, Siero JCW, Hendrikse J, Luijten PR, Zwanenburg JJM (2018) Phase contrast MRI measurements of net cerebrospinal fluid flow through the cerebral aqueduct are confounded by respiration. J Magn Reson Imaging 40:2583–2512

    Google Scholar 

  35. Takizawa K, Matsumae M, Hayashi N, Hirayama A, SANO F, Yatsushiro S, Kuroda K (2018) The choroid plexus of the lateral ventricle as the origin of CSF pulsation is questionable. Neurol Med Chir (Tokyo) 58(1):23–31

    Article  Google Scholar 

  36. Takizawa K, Matsumae M, Sunohara S, Yatsushiro S, Kuroda K (2017) Characterization of cardiac- and respiratory-driven cerebrospinal fluid motion based on asynchronous phase-contrast magnetic resonance imaging in volunteers. Fluids Barriers CNS 14(1):25

    Article  PubMed  PubMed Central  Google Scholar 

  37. Williams B (1981) Simultaneous cerebral and spinal fluid pressure recordings. Acta Neurochir 59(1–2):123–142

    Article  CAS  PubMed  Google Scholar 

  38. Williams B (1981) Simultaneous cerebral and spinal fluid pressure recordings. Acta Neurochir 58(3–4):167–185

    Article  CAS  PubMed  Google Scholar 

  39. Williams H (2008) A unifying hypothesis for hydrocephalus, Chiari malformation, syringomyelia, anencephaly and spina bifida. Cerebrospinal Fluid Res 5:7

    Article  PubMed  PubMed Central  Google Scholar 

  40. Yamada S, Miyazaki M, Yamashita Y, Ouyang C, Yui M, Nakahashi M, Shimizu S, Aoki I, Morohoshi Y, McComb J (2013) Influence of respiration on cerebrospinal fluid movement using magnetic resonance spin labeling. Fluids Barriers CNS 10(1):36

    Article  PubMed  PubMed Central  Google Scholar 

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Conflict of interest

The authors declare that they have no competing interest.

Author information

Author notes

  1. Steffi F. Dreha-Kulaczewski and Hans C. Bock contributed equally to this work.

Authors and Affiliations

  1. Department of Neurosurgery, Section Pediatric Neurosurgery, University Medical Center Göttingen, Robert-Koch-Str. 40, 37075, Göttingen, Germany

    Hans C. Bock, Awad Alaid & Hans C. Ludwig

  2. Department of Pediatrics and Adolescent Medicine, Division of Pediatric Neurology, University Medical Center Göttingen, Robert-Koch-Str. 40, 37075, Göttingen, Germany

    Steffi F. Dreha-Kulaczewski & Jutta Gärtner

Authors
  1. Hans C. Bock
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  2. Steffi F. Dreha-Kulaczewski
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  3. Awad Alaid
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  4. Jutta Gärtner
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  5. Hans C. Ludwig
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Contributions

HCB and AA performed the endoscopic part of the studies. HCL designed the study, conducted the study including endoscopies, and wrote the manuscript. SDK conducted the study and wrote the manuscript. JG conducted the study and wrote the manuscript.

Corresponding author

Correspondence to Hans C. Ludwig.

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Electronic supplementary material

Supplementary table

: Clinical data of 117 pediatric patients with obstructive hydrocephalus and assessment of pre-, intra-, and post-operative CSF dynamics. MRI category: see Table II; G: gender; yrs: years; HC: hydrocephalus; Intraop.: intraoperative; CM: contrast medium; X-ray: C-arc X-ray; m: male; f: female; OH: obstructive hydrocephalus; LH: loculated hydrocephalus; TU: tumor related hydrocephalus; iso4 v: isolated 4th ventricle; AC: arachnoid cyst; CF: cyst fenestration; ETV: endoscopic third ventriculostomy; SP: pellucidotomy; AP: aqueductoplasty; 1: yes; 0: no; NA: not applicable; *: of CSF; **: prior to surgical intervention (DOCX 46 kb)

Endoscopic aquaeductoplasty in a 4-year old preterm child (24th gestational week) with isolated 4th ventricle due to post-hemorrhagic hydrocephalus (see Fig. 4c). Neuroendoscopy was performed using a rigid Paediscope (Aesculap, Tuttlingen, Germany). The video shows the floor of the 4th ventricle at the craniocervical junction after its microsurgical opening. Note the upward-directed membrane fluctuations. They occurred synchronous to inspiratory ventilation cycle according to the observations of the neurosurgeons H.C. Bock and H.C. Ludwig.

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Bock, H.C., Dreha-Kulaczewski, S.F., Alaid, A. et al. Upward movement of cerebrospinal fluid in obstructive hydrocephalus—revision of an old concept. Childs Nerv Syst 35, 833–841 (2019). https://doi.org/10.1007/s00381-019-04119-x

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  • DOI: https://doi.org/10.1007/s00381-019-04119-x

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