Abstract
Hydrocephalus is the symptomatic endpoint of a variety of disease processes. Simple hydrodynamic models have failed to explain the entire spectrum of cerebrospinal fluid (CSF) disorders. Physical principles argue that for ventricles to expand, they must be driven by a force, Fishman’s transmantle pressure gradient (TMPG). However, the literature to date, reviewed herein, is heterogenous and fails to consistently measure a TMPG. The venous system, like CSF, traverses the cerebral mantle, and thus analogous transparenchymal and transvenous pressure gradients have been described, reliant on the differential haemodynamics of the deep and superficial venous systems. Interpreting CSF disorders through these models provides new insights into the possible pathophysiological mechanisms underlying these diseases. However, until more sophisticated testing is performed, these models should remain heuristics.
Similar content being viewed by others
Availability of data and materials
All data generated or analysed during this study are included in this published article (and its supplementary information files).
References
Andersson N, Malm J, Eklund A (2008) Dependency of cerebrospinal fluid outflow resistance on intracranial pressure: clinical article. J Neurosurg 109:918–922. https://doi.org/10.3171/JNS/2008/109/11/0918
Aso T, Sugihara G, Murai T, Ubukata S, Urayama S, Ueno T, Fujimoto G, Thuy DHD, Fukuyama H, Ueda K (2020) A venous mechanism of ventriculomegaly shared between traumatic brain injury and normal ageing. Brain 143:1843–1856. https://doi.org/10.1093/brain/awaa125
Bateman GA (2000) Vascular compliance in normal pressure hydrocephalus. AJNR Am J Neuroradiol 21:1574–1585
Bateman GA (2003) The reversibility of reduced cortical vein compliance in normal-pressure hydrocephalus following shunt insertion. Neuroradiology 45:65–70. https://doi.org/10.1007/s00234-002-0901-0
Bateman GA (2008) The pathophysiology of idiopathic normal pressure hydrocephalus: cerebral ischemia or altered venous hemodynamics? AJNR Am J Neuroradiol 29:198–203. https://doi.org/10.3174/ajnr.A0739
Bateman GA (2008) Arterial inflow and venous outflow in idiopathic intracranial hypertension associated with venous outflow stenoses. J Clin Neurosci 15:402–408. https://doi.org/10.1016/j.jocn.2007.03.018
Bateman GA, Bateman AR (2019) Differences in the calculated transvenous pressure drop between chronic hydrocephalus and idiopathic intracranial hypertension. AJNR Am J Neuroradiol 40:68–73. https://doi.org/10.3174/ajnr.A5883
Bateman GA, Siddique SH (2014) Cerebrospinal fluid absorption block at the vertex in chronic hydrocephalus: obstructed arachnoid granulations or elevated venous pressure? Fluids Barriers CNS 11:11. https://doi.org/10.1186/2045-8118-11-11
Bateman GA, Yap SL, Subramanian GM, Bateman AR (2020) The incidence of significant venous sinus stenosis and cerebral hyperemia in childhood hydrocephalus: prognostic value with regards to differentiating active from compensated disease. Fluids Barriers CNS 17:33. https://doi.org/10.1186/s12987-020-00194-4
Boon AJW, Tans JTJ, Delwel EJ, Egeler-Peerdeman SM, Hanlo PW, Wurzer HAL, Avezaat CJJ, de Jong DA, Gooskens RHJM, Hermans J (1997) Dutch Normal-Pressure Hydrocephalus Study: prediction of outcome after shunting by resistance to outflow of cerebrospinal fluid. J Neurosurg 87:687–693. https://doi.org/10.3171/jns.1997.87.5.0687
Castro ME, Portnoy HD, Maesaka J (1991) Elevated cortical venous pressure in hydrocephalus. Neurosurgery 29:232–238. https://doi.org/10.1097/00006123-199108000-00011
Chan DYC, Tsang ACO, Ho WWS, Cheng KKF, Li LF, Tsang FCP, Taw BBT, Pu JKS, Leung GKK, Lui MWM (2018) Emergency endoscopic third ventriculostomy for blocked shunts? Univariate and multivariate analysis of independent predictors for failure. J Neurosurg 131:1004–1010. https://doi.org/10.3171/2018.6.JNS1865
Chazal J, Tanguy A, Irthum B, Janny P, Vanneuville G (1985) Dilatation of the subarachnoid pericerebral space and absorption of cerebrospinal fluid in the infant. Anat Clin 7:61–66. https://doi.org/10.1007/BF01654631
Conner ES, Foley L, Black PMcL (1984) Experimental normal-pressure hydrocephalus is accompanied by increased transmantle pressure. J Neurosurg 61:322–327. https://doi.org/10.3171/jns.1984.61.2.0322
DeFeo DR, Myers P, Foltz EL, Everett B, Ramshaw B (1979) Histological examination of kaolin-induced hydrocephalus: its implications in the therapy of animals with experimentally induced hydrocephalus. J Neurosurg 50:70–74. https://doi.org/10.3171/jns.1979.50.1.0070
Dutta-Roy T, Wittek A, Miller K (2008) Biomechanical modelling of normal pressure hydrocephalus. J Biomech 41:2263–2271. https://doi.org/10.1016/j.jbiomech.2008.04.014
Dwyer CM, Prelog K, Owler BK (2013) The role of venous sinus outflow obstruction in pediatric idiopathic intracranial hypertension: clinical article. PED 11:144–149. https://doi.org/10.3171/2012.10.PEDS1299
Eide PK, Saehle T (2010) Is ventriculomegaly in idiopathic normal pressure hydrocephalus associated with a transmantle gradient in pulsatile intracranial pressure? Acta Neurochir (Wien) 152:989–995. https://doi.org/10.1007/s00701-010-0605-x
Engel M, Carmel PW, Chutorian AM (1979) Increased intraventricular pressure without ventriculomegaly in children with shunts“normal volume” hydrocephalus. Neurosurgery 5:549–552. https://doi.org/10.1227/00006123-197911000-00001
Fishman RA (1966) Occult hydrocephalus. N Engl J Med 274:466–467. https://doi.org/10.1056/NEJM196602242740817
Ichelangelo G, Maiuri F, Naddeo M, Godano U, Mascari C, Broggi G, Ferroli P (2008) Endoscopic third ventriculostomy in idiopathic normal pressure hydrocephalus. Neurosurgery 63:62–69. https://doi.org/10.1227/01.NEU.0000335071.37943.40
Haar FL, Miller CA (1975) Hydrocephalus resulting from superior vena cava thrombosis in an infant: case report. J Neurosurg 42:597–601. https://doi.org/10.3171/jns.1975.42.5.0597
Hara M, Nakamura M, Kadowaki C, Watanabe H, Shiogai T, Numoto M, Takeuchi K (1985) Cerebrospinal fluid absorption mechanism–based on measurement of CSF flow rate in shunt tube. No To Shinkei 37:365–370
Hladky SB, Barrand MA (2014) Mechanisms of fluid movement into, through and out of the brain: evaluation of the evidence. Fluids Barriers CNS 11.https://doi.org/10.1186/2045-8118-11-26
Hoff J, Barber R (1974) Transcerebral mantle pressure in normal pressure hydrocephalus. Arch Neurol 31:101–105. https://doi.org/10.1001/archneur.1974.00490380049005
Holmlund P, Eklund A, Koskinen L-OD, Johansson E, Sundström N, Malm J, Qvarlander S (2017) Venous collapse regulates intracranial pressure in upright body positions. Am J Physiol Regul Integr Comp Physiol 314:R377–R385. https://doi.org/10.1152/ajpregu.00291.2017
Holmlund P, Qvarlander S, Malm J, Eklund A (2019) Can pulsatile CSF flow across the cerebral aqueduct cause ventriculomegaly? A prospective study of patients with communicating hydrocephalus. Fluids Barriers CNS 16:40. https://doi.org/10.1186/s12987-019-0159-0
Jacobsson J, Qvarlander S, Eklund A, Malm J (2018) Comparison of the CSF dynamics between patients with idiopathic normal pressure hydrocephalus and healthy volunteers. J Neurosurg 131:1018–1023. https://doi.org/10.3171/2018.5.JNS173170
James AE (1970) Normal-pressure hydrocephalus: role of cisternography in diagnosis. JAMA 213:1615. https://doi.org/10.1001/jama.1970.03170360013002
Keough MB, Isaacs AM, Urbaneja G, Dronyk J, Lapointe AP, Hamilton MG (2020) Acute low-pressure hydrocephalus: a case series and systematic review of 195 patients. J Neurosurg 1–9https://doi.org/10.3171/2020.4.JNS20476
Kim H, Jeong E-J, Park D-H, Czosnyka Z, Yoon BC, Kim K, Czosnyka M, Kim D-J (2016) Finite element analysis of periventricular lucency in hydrocephalus: extravasation or transependymal CSF absorption? J Neurosurg 124:334–341. https://doi.org/10.3171/2014.11.JNS141382
Larsson A, Moonen M, Bergh AC, Lindberg S, Wikkelsö C (1990) Predictive value of quantitative cisternography in normal pressure hydrocephalus. Acta Neurol Scand 81:327–332. https://doi.org/10.1111/j.1600-0404.1990.tb01564.x
Levine DN (2008) Intracranial pressure and ventricular expansion in hydrocephalus: have we been asking the wrong question? J Neurol Sci 269:1–11. https://doi.org/10.1016/j.jns.2007.12.022
Libby J, Marghoub A, Johnson D, Khonsari RH, Fagan MJ, Moazen M (2017) Modelling human skull growth: a validated computational model. J R Soc Interface 14:20170202. https://doi.org/10.1098/rsif.2017.0202
Linninger AA, Sweetman B, Penn R (2009) Normal and hydrocephalic brain dynamics: the role of reduced cerebrospinal fluid reabsorption in ventricular enlargement. Ann Biomed Eng 37:1434–1447. https://doi.org/10.1007/s10439-009-9691-4
Mase M, Miyati T, Kasai H, Demura K, Osawa T, Hara M, Shibamoto Y, Yamada K (2009) Noninvasive estimation of intracranial compliance in idiopathic NPH using MRI. In: Steiger H-J (ed) Acta Neurochirurgica Supplements. Springer, Vienna, pp 115–118
Meila D, Grieb D, Melber K, Jacobs C, Maslehaty H, Petridis A, El Habony R, Lanfermann H, Scholz M, Brassel F (2016) Hydrocephalus in vein of Galen malformation: etiologies and therapeutic management implications. Acta Neurochir 158:1279–1284. https://doi.org/10.1007/s00701-016-2836-y
Miyati T, Mase M, Kasai H, Hara M, Yamada K, Shibamoto Y, Soellinger M, Baltes C, Luechinger R (2007) Noninvasive MRI assessment of intracranial compliance in idiopathic normal pressure hydrocephalus. J Magn Reson Imaging 26:274–278. https://doi.org/10.1002/jmri.20999
Paciorkowski AR, Greenstein RM (2007) When is enlargement of the subarachnoid spaces not benign? A genetic perspective. Pediatr Neurol 37:1–7. https://doi.org/10.1016/j.pediatrneurol.2007.04.001
Penn RD, Lee MC, Linninger AA, Miesel K, Lu SN, Stylos L (2005) Pressure gradients in the brain in an experimental model of hydrocephalus. J Neurosurg 102:1069–1075. https://doi.org/10.3171/jns.2005.102.6.1069
Perry A, Graffeo CS, Fattahi N, ElSheikh MM, Cray N, Arani A, Ehman RL, Glaser KJ, Manduca A, Meyer FB, Huston J (2017) Clinical correlation of abnormal findings on magnetic resonance elastography in idiopathic normal pressure hydrocephalus. World Neurosurg 99:695-700.e1. https://doi.org/10.1016/j.wneu.2016.12.121
Pinto FCG, Saad F, de Oliveira MF, Pereira RM, de Miranda FL, Tornai JB, Lopes MIR, Ribas ESC, Valinetti EA (2013) Role of endoscopic third ventriculostomy and ventriculoperitoneal shunt in idiopathic normal pressure hydrocephalus. Neurosurgery 72:845–854. https://doi.org/10.1227/NEU.0b013e318285b37c
Portnoy HD, Branch C, Castro ME (1994) The relationship of intracranial venous pressure to hydrocephalus. Childs Nerv Syst 10:29–35. https://doi.org/10.1007/BF00313582
Portnoy HD, Castro ME (1993) Elevated cortical venous pressure in hydrocephalus. Neurosurgery 32:151–151. https://doi.org/10.1227/00006123-199301000-00029
Rekate HL (1993) Classification of slit-ventricle syndromes using intracranial pressure monitoring. Pediatr Neurosurg 19:15–20. https://doi.org/10.1159/000120694
Rekate HL (2005) Slit ventricle syndrome or syndromes: diagnosis and management. In: Cinalli G, Sainte-Rose C, Maixner WJ (eds) Pediatric hydrocephalus. Springer Milan, Milano, pp 335–349
Rekate HL (2011) A consensus on the classification of hydrocephalus: its utility in the assessment of abnormalities of cerebrospinal fluid dynamics. Childs Nerv Syst 27:1535–1541. https://doi.org/10.1007/s00381-011-1558-y
Rekate HL, Nadkarni TD, Wallace D (2008) The importance of the cortical subarachnoid space in understanding hydrocephalus. PED 2:1–11. https://doi.org/10.3171/PED/2008/2/7/001
Rekate HL, Williams FC Jr, Brodkey JA, McCormick JM, Chizeck HJ, Ko W (1988) Resistance of the foramen of Monro. Pediatr Neurosurg 14:85–89. https://doi.org/10.1159/000120368
Ringstad G, Emblem KE, Eide PK (2016) Phase-contrast magnetic resonance imaging reveals net retrograde aqueductal flow in idiopathic normal pressure hydrocephalus. J Neurosurg 124:1850–1857. https://doi.org/10.3171/2015.6.JNS15496
Ringstad G, Vatnehol SAS, Eide PK (2017) Glymphatic MRI in idiopathic normal pressure hydrocephalus. Brain 140:2691–2705. https://doi.org/10.1093/brain/awx191
Rosman NP, Shands KN (1978) Hydrocephalus caused by increased intracranial venous pressure: a clinicopathological study. Ann Neurol 3:445–450. https://doi.org/10.1002/ana.410030516
Sahar A, Hochwald GM, Ransohoff J (1969) Alternate pathway for cerebrospinal fluid absorption in animals with experimental obstructive hydrocephalus. Exp Neurol 25:200–206. https://doi.org/10.1016/0014-4886(69)90044-2
Sainte-Rose C, LaCombe J, Pierre-Kahn A, Renier D, Hirsch J-F (1984) Intracranial venous sinus hypertension: cause or consequence of hydrocephalus in infants? J Neurosurg 60:727–736. https://doi.org/10.3171/jns.1984.60.4.0727
Satow T, Aso T, Nishida S, Komuro T, Ueno T, Oishi N, Nakagami Y, Odagiri M, Kikuchi T, Yoshida K, Ueda K, Kunieda T, Murai T, Miyamoto S, Fukuyama H (2017) Alteration of venous drainage route in idiopathic normal pressure hydrocephalus and normal aging. Front Aging Neurosci 9.https://doi.org/10.3389/fnagi.2017.00387
Shapiro K, Fried A (1986) Pressure-volume relationships in shunt-dependent childhood hydrocephalus: the zone of pressure instability in children with acute deterioration. J Neurosurg 64:390–396. https://doi.org/10.3171/jns.1986.64.3.0390
Shapiro K, Kohn IJ, Takei F, Zee C (1987) Progressive ventricular enlargement in cats in the absence of transmantle pressure gradients. J Neurosurg 67:88–92. https://doi.org/10.3171/jns.1987.67.1.0088
Shulman K, Ransohoff J (1965) Sagittal sinus venous pressure in hydrocephalus. J Neurosurg 23:169–173. https://doi.org/10.3171/jns.1965.23.2.0169
Sood S, Barrett RJ, Powell T, Ham SD (2005) The role of lumbar shunts in the management of slit ventricles: does the slit-ventricle syndrome exist? J Neurosurg Pediatr 103:119–123. https://doi.org/10.3171/ped.2005.103.2.0119
Sood S, Lokuketagoda J, Ham SD (2005) Periventricular rigidity in long-term shunt-treated hydrocephalus. J Neurosurg Pediatr 102:146–149. https://doi.org/10.3171/ped.2005.102.2.0146
Steinbok P, Hall J, Flodmark O (1989) Hydrocephalus in achondroplasia: the possible role of intracranial venous hypertension. J Neurosurg 71:42–48. https://doi.org/10.3171/jns.1989.71.1.0042
Stephensen H, Tisell M, Wikkelsö C (2002) There is no transmantle pressure gradient in communicating or noncommunicating hydrocephalus. Neurosurgery 50:763–71; discussion 771–773. https://doi.org/10.1097/00006123-200204000-00016
Wagshul ME, Eide PK, Madsen JR (2011) The pulsating brain: a review of experimental and clinical studies of intracranial pulsatility. Fluids Barriers CNS 8:5. https://doi.org/10.1186/2045-8118-8-5
Yin LK, Zheng JJ, Zhao L, Hao XZ, Zhang XX, Tian JQ, Zheng K, Yang YM (2017) Reversed aqueductal cerebrospinal fluid net flow in idiopathic normal pressure hydrocephalus. Acta Neurol Scand 136:434–439. https://doi.org/10.1111/ane.12750
Zahl SM, Egge A, Helseth E, Wester K (2011) Benign external hydrocephalus: a review, with emphasis on management. Neurosurg Rev 34:417–432. https://doi.org/10.1007/s10143-011-0327-4
Zuurbier SM, van den Berg R, Troost D, Majoie CB, Stam J, Coutinho JM (2015) Hydrocephalus in cerebral venous thrombosis. J Neurol 262:931–937. https://doi.org/10.1007/s00415-015-7652-4
Author information
Authors and Affiliations
Contributions
MCK collected and analysed the data, wrote the draft, and revised the manuscript. TG provided critical interpretation of the data, helped draft and revise the manuscript, and provided study supervision. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Ethics approval and consent to participate
Not applicable.
Consent for publication
Not applicable.
Competing interests
The authors declare no competing interests.
Disclaimer
All authors approved the final submission and all authors agree to be accountable for all aspects of the work.
Additional information
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Castle-Kirszbaum, M., Goldschlager, T. Transmantle and transvenous pressure gradients in cerebrospinal fluid disorders. Neurosurg Rev 45, 305–315 (2022). https://doi.org/10.1007/s10143-021-01622-1
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10143-021-01622-1