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Published in: Child's Nervous System 5/2014

01-05-2014 | Review Paper

Normal pressure hydrocephalus as a failure of ICP homeostasis mechanism: the hidden role of Monro–Kellie doctrine in the genesis of NPH

Author: Asem Salma

Published in: Child's Nervous System | Issue 5/2014

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Abstract

Objective

The theme of this paper is to outline that the genesis of normal pressure hydrocephalus (NPH) is governed by the intracranial pressure (ICP) homeostatic principle. The development of this new concept is based mainly on rethinking the well-known Monro–Kellie doctrine in the way that ICP homeostasis mechanism is not only a mechanism that works to prevent pathologically high ICP but also a mechanism that aims to protect from pathologically low ICP.

Methods

The NPH-related literatures are reviewed and reinterpreted to generate a new paradigm for the cascade of pathophysiological events that leads to the genesis NPH, as well as the mechanism of clinical beneficial effects and complications of the shunting procedure.

Results

According to this new paradigm, the suboptimal cerebral perfusion that is associated with the impairment of the cerebral autoregulation is the initial step in the genesis of NPH. When the overall volume of blood that circulates intracranially is diminished, a chronic low ICP with episodes of pathologically low ICP occurs. Since the cranial vault is not collapsible, those episodes of low ICP are compensated by the accumulation of cerebrospinal fluid (CSF) to keep the ICP in normal ideal range. The impairment of brain toxin-flushing mechanism because of CSF pooling combined with the already-established suboptimal cerebral perfusion leads to functional disinhibition of the cerebral cortex.

Conclusion

Recognizing the importance of ICP homeostatic mechanisms in the genesis of the NPH is a simple yet novel view that could change the way we look at NP and can give a basic and fundamental theoretical frame work to achieve better understanding of NPH.
Literature
1.
go back to reference Adams RD, Fisher CM, Hakim S, Ojemann RG, Sweet WH (1965) Symptomatic occult hydrocephalus with "Normal" cerebrospinal-fluid pressure. A treatable syndrome. N Engl J Med 273:117–126PubMedCrossRef Adams RD, Fisher CM, Hakim S, Ojemann RG, Sweet WH (1965) Symptomatic occult hydrocephalus with "Normal" cerebrospinal-fluid pressure. A treatable syndrome. N Engl J Med 273:117–126PubMedCrossRef
2.
go back to reference Bateman GA (2008) The pathophysiology of idiopathic normal pressure hydrocephalus: cerebral ischemia or altered venous hemodynamics? AJNR Am J Neuroradiol 29:198–203PubMedCrossRef Bateman GA (2008) The pathophysiology of idiopathic normal pressure hydrocephalus: cerebral ischemia or altered venous hemodynamics? AJNR Am J Neuroradiol 29:198–203PubMedCrossRef
3.
go back to reference Bradley WG (2000) Normal pressure hydrocephalus: new concepts on etiology and diagnosis. AJNR Am J Neuroradiol 21:1586–1590PubMed Bradley WG (2000) Normal pressure hydrocephalus: new concepts on etiology and diagnosis. AJNR Am J Neuroradiol 21:1586–1590PubMed
4.
go back to reference Bradley WG Jr (2008) Idiopathic normal pressure hydrocephalus: new findings and thoughts on etiology. AJNR Am J Neuroradiol 29:1–3PubMedCrossRef Bradley WG Jr (2008) Idiopathic normal pressure hydrocephalus: new findings and thoughts on etiology. AJNR Am J Neuroradiol 29:1–3PubMedCrossRef
5.
go back to reference Silverberg GD (2004) Normal pressure hydrocephalus (NPH): ischaemia, CSF stagnation or both. Brain 127:947–948PubMedCrossRef Silverberg GD (2004) Normal pressure hydrocephalus (NPH): ischaemia, CSF stagnation or both. Brain 127:947–948PubMedCrossRef
6.
go back to reference Di Rocco C, Di Trapani G, Maira G, Bentivoglio M, Macchi G, Rossi GF (1977) Anatomo-clinical correlations in normotensive hydrocephalus. Reports on three cases. J Neurol Sci 33(3):437–452PubMedCrossRef Di Rocco C, Di Trapani G, Maira G, Bentivoglio M, Macchi G, Rossi GF (1977) Anatomo-clinical correlations in normotensive hydrocephalus. Reports on three cases. J Neurol Sci 33(3):437–452PubMedCrossRef
7.
go back to reference 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(1):40–52PubMedCrossRef 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(1):40–52PubMedCrossRef
8.
go back to reference 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(1):30–39 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(1):30–39
9.
go back to reference Preuss M, Hoffmann KT, Reiss-Zimmermann M, Hirsch W, Merkenschlager A, Meixensberger J, Dengl M (2013) Updated physiology and pathophysiology of CSF circulation—the pulsatile vector theory. Childs Nerv Syst 29:1811–1825PubMedCrossRef Preuss M, Hoffmann KT, Reiss-Zimmermann M, Hirsch W, Merkenschlager A, Meixensberger J, Dengl M (2013) Updated physiology and pathophysiology of CSF circulation—the pulsatile vector theory. Childs Nerv Syst 29:1811–1825PubMedCrossRef
10.
go back to reference Toma AK, Stapleton S, Papadopoulos MC, Kitchen ND, Watkins LD (2011) Natural history of idiopathic normal-pressure hydrocephalus. Neurosurg Rev 34(4):433–439PubMedCrossRef Toma AK, Stapleton S, Papadopoulos MC, Kitchen ND, Watkins LD (2011) Natural history of idiopathic normal-pressure hydrocephalus. Neurosurg Rev 34(4):433–439PubMedCrossRef
11.
go back to reference Hayes J, Roguski M, Riesenburger RI (2012) Rapid resolution of an acute subdural hematoma by increasing the shunt valve pressure in a 63-year-old man with normal-pressure hydrocephalus with a ventriculoperitoneal shunt: a case report and literature review. J Med Case Rep 6:393PubMedCentralPubMedCrossRef Hayes J, Roguski M, Riesenburger RI (2012) Rapid resolution of an acute subdural hematoma by increasing the shunt valve pressure in a 63-year-old man with normal-pressure hydrocephalus with a ventriculoperitoneal shunt: a case report and literature review. J Med Case Rep 6:393PubMedCentralPubMedCrossRef
12.
go back to reference Klinge PM (2012) Idiopathic normal pressure hydrocephalus–neurosurgical management of dementia! Med Health R I 95:86–87PubMed Klinge PM (2012) Idiopathic normal pressure hydrocephalus–neurosurgical management of dementia! Med Health R I 95:86–87PubMed
13.
go back to reference Nakamizo A, Inamura T, Inoha S, Kuba H, Amano T, Sasaki M, Fukui M (2002) Occurrence of subdural hematoma and resolution of gait disturbance in a patient treated with shunting for normal pressure hydrocephalus. Clin Neurol Neurosurg 104:315–317PubMedCrossRef Nakamizo A, Inamura T, Inoha S, Kuba H, Amano T, Sasaki M, Fukui M (2002) Occurrence of subdural hematoma and resolution of gait disturbance in a patient treated with shunting for normal pressure hydrocephalus. Clin Neurol Neurosurg 104:315–317PubMedCrossRef
14.
go back to reference Kamiryo T, Hamada J, Fuwa I, Ushio Y (2003) Acute subdural hematoma after lumboperitoneal shunt placement in patients with normal pressure hydrocephalus. Neurol Med Chir (Tokyo) 43:197–200CrossRef Kamiryo T, Hamada J, Fuwa I, Ushio Y (2003) Acute subdural hematoma after lumboperitoneal shunt placement in patients with normal pressure hydrocephalus. Neurol Med Chir (Tokyo) 43:197–200CrossRef
15.
go back to reference Missori P, Coppola G, Paolini S, Pierelli F, Curra A (2012) Intraparenchymal haemorrhage after a cerebrospinal fluid tap-test for secondary normal pressure hydrocephalus. J Clin Neurosci 19:914–916PubMedCrossRef Missori P, Coppola G, Paolini S, Pierelli F, Curra A (2012) Intraparenchymal haemorrhage after a cerebrospinal fluid tap-test for secondary normal pressure hydrocephalus. J Clin Neurosci 19:914–916PubMedCrossRef
16.
go back to reference Poca MA, Solana E, Martinez-Ricarte FR, Romero M, Gandara D, Sahuquillo J (2012) Idiopathic normal pressure hydrocephalus: results of a prospective cohort of 236 shunted patients. Acta Neurochir Suppl 114:247–253PubMedCrossRef Poca MA, Solana E, Martinez-Ricarte FR, Romero M, Gandara D, Sahuquillo J (2012) Idiopathic normal pressure hydrocephalus: results of a prospective cohort of 236 shunted patients. Acta Neurochir Suppl 114:247–253PubMedCrossRef
17.
go back to reference Catananti C, Mastropaolo S, Calabrese C, Silveri MC, Onder G (2010) A case of normal-pressure hydrocephalus associated with rheumatoid arthritis. Aging Clin Exp Res 22:189–191PubMedCrossRef Catananti C, Mastropaolo S, Calabrese C, Silveri MC, Onder G (2010) A case of normal-pressure hydrocephalus associated with rheumatoid arthritis. Aging Clin Exp Res 22:189–191PubMedCrossRef
18.
go back to reference de Oliveira FF, Cardoso TA, Sampaio-Barros PD, Damasceno BP (2013) Normal pressure hydrocephalus in the spectrum of neurological complications of systemic lupus erythematosus. Neurol Sci 34:1009–1013PubMedCrossRef de Oliveira FF, Cardoso TA, Sampaio-Barros PD, Damasceno BP (2013) Normal pressure hydrocephalus in the spectrum of neurological complications of systemic lupus erythematosus. Neurol Sci 34:1009–1013PubMedCrossRef
19.
go back to reference Filippidis AS, Kalani MY, Nakaji P, Rekate HL (2011) Negative-pressure and low-pressure hydrocephalus: the role of cerebrospinal fluid leaks resulting from surgical approaches to the cranial base. J Neurosurg 115:1031–1037PubMedCrossRef Filippidis AS, Kalani MY, Nakaji P, Rekate HL (2011) Negative-pressure and low-pressure hydrocephalus: the role of cerebrospinal fluid leaks resulting from surgical approaches to the cranial base. J Neurosurg 115:1031–1037PubMedCrossRef
20.
go back to reference Hamilton MG, Price AV (2012) Syndrome of inappropriately low-pressure acute hydrocephalus (SILPAH). Acta Neurochir Suppl 113:155–159PubMedCrossRef Hamilton MG, Price AV (2012) Syndrome of inappropriately low-pressure acute hydrocephalus (SILPAH). Acta Neurochir Suppl 113:155–159PubMedCrossRef
21.
go back to reference Kitami K, Suzuki A, Hadeishi H, Nishimura H, Yasui N (1986) Normal pressure hydrocephalus after subarachnoid hemorrhage–with regard to pathogenesis and factors influencing the efficacy of shunt surgery. No To Shinkei 38:781–788PubMed Kitami K, Suzuki A, Hadeishi H, Nishimura H, Yasui N (1986) Normal pressure hydrocephalus after subarachnoid hemorrhage–with regard to pathogenesis and factors influencing the efficacy of shunt surgery. No To Shinkei 38:781–788PubMed
22.
go back to reference Mangat HS (2012) Severe traumatic brain injury. Contin (Minneap Minn) 18:532–546 Mangat HS (2012) Severe traumatic brain injury. Contin (Minneap Minn) 18:532–546
23.
go back to reference Mokri B (2001) The Monro-Kellie hypothesis: applications in CSF volume depletion. Neurology 56:1746–1748PubMedCrossRef Mokri B (2001) The Monro-Kellie hypothesis: applications in CSF volume depletion. Neurology 56:1746–1748PubMedCrossRef
24.
go back to reference Chang CC, Kuwana N, Ito S, Ikegami T (2000) Impairment of cerebrovascular reactivity to acetazolamide in patients with normal pressure hydrocephalus. Nucl Med Commun 21:139–141PubMedCrossRef Chang CC, Kuwana N, Ito S, Ikegami T (2000) Impairment of cerebrovascular reactivity to acetazolamide in patients with normal pressure hydrocephalus. Nucl Med Commun 21:139–141PubMedCrossRef
25.
go back to reference Chang CC, Kuwana N, Noji M, Tanabe Y, Koike Y, Ikegami T (1999) Cerebral blood flow in patients with normal pressure hydrocephalus. Nucl Med Commun 20:167–169PubMedCrossRef Chang CC, Kuwana N, Noji M, Tanabe Y, Koike Y, Ikegami T (1999) Cerebral blood flow in patients with normal pressure hydrocephalus. Nucl Med Commun 20:167–169PubMedCrossRef
26.
go back to reference Miyamoto J, Tatsuzawa K, Inoue Y, Imahori Y, Mineura K (2007) Oxygen metabolism changes in patients with idiopathic normal pressure hydrocephalus before and after shunting operation. Acta Neurol Scand 116:137–143PubMedCrossRef Miyamoto J, Tatsuzawa K, Inoue Y, Imahori Y, Mineura K (2007) Oxygen metabolism changes in patients with idiopathic normal pressure hydrocephalus before and after shunting operation. Acta Neurol Scand 116:137–143PubMedCrossRef
27.
go back to reference Momjian S, Owler BK, Czosnyka Z, Czosnyka M, Pena A, Pickard JD (2004) Pattern of white matter regional cerebral blood flow and autoregulation in normal pressure hydrocephalus. Brain 127:965–972PubMedCrossRef Momjian S, Owler BK, Czosnyka Z, Czosnyka M, Pena A, Pickard JD (2004) Pattern of white matter regional cerebral blood flow and autoregulation in normal pressure hydrocephalus. Brain 127:965–972PubMedCrossRef
28.
go back to reference Mori K, Maeda M, Asegawa S, Iwata J (2002) Quantitative local cerebral blood flow change after cerebrospinal fluid removal in patients with normal pressure hydrocephalus measured by a double injection method with N-isopropyl-p-[(123)I] iodoamphetamine. Acta Neurochir (Wien) 144:255–262, discussion 262–253CrossRef Mori K, Maeda M, Asegawa S, Iwata J (2002) Quantitative local cerebral blood flow change after cerebrospinal fluid removal in patients with normal pressure hydrocephalus measured by a double injection method with N-isopropyl-p-[(123)I] iodoamphetamine. Acta Neurochir (Wien) 144:255–262, discussion 262–253CrossRef
29.
go back to reference Owler BK, Momjian S, Czosnyka Z, Czosnyka M, Pena A, Harris NG, Smielewski P, Fryer T, Donovan T, Coles J, Carpenter A, Pickard JD (2004) Normal pressure hydrocephalus and cerebral blood flow: a PET study of baseline values. J Cereb Blood Flow Metab 24:17–23PubMedCrossRef Owler BK, Momjian S, Czosnyka Z, Czosnyka M, Pena A, Harris NG, Smielewski P, Fryer T, Donovan T, Coles J, Carpenter A, Pickard JD (2004) Normal pressure hydrocephalus and cerebral blood flow: a PET study of baseline values. J Cereb Blood Flow Metab 24:17–23PubMedCrossRef
30.
go back to reference Takaya M, Kazui H, Tokunaga H, Yoshida T, Kito Y, Wada T, Nomura K, Shimosegawa E, Hatazawa J, Takeda M (2010) Global cerebral hypoperfusion in preclinical stage of idiopathic normal pressure hydrocephalus. J Neurol Sci 298:35–41PubMedCrossRef Takaya M, Kazui H, Tokunaga H, Yoshida T, Kito Y, Wada T, Nomura K, Shimosegawa E, Hatazawa J, Takeda M (2010) Global cerebral hypoperfusion in preclinical stage of idiopathic normal pressure hydrocephalus. J Neurol Sci 298:35–41PubMedCrossRef
31.
go back to reference Tanaka A, Kimura M, Nakayama Y, Yoshinaga S, Tomonaga M (1997) Cerebral blood flow and autoregulation in normal pressure hydrocephalus. Neurosurgery 40:1161–1165, discussion 1165–1167PubMedCrossRef Tanaka A, Kimura M, Nakayama Y, Yoshinaga S, Tomonaga M (1997) Cerebral blood flow and autoregulation in normal pressure hydrocephalus. Neurosurgery 40:1161–1165, discussion 1165–1167PubMedCrossRef
32.
go back to reference Iliff JJ, Lee H, Yu M, Feng T, Logan J, Nedergaard M, Benveniste H (2013) Brain-wide pathway for waste clearance captured by contrast-enhanced MRI. J Clin Invest 123:1299–1309PubMedCentralPubMedCrossRef Iliff JJ, Lee H, Yu M, Feng T, Logan J, Nedergaard M, Benveniste H (2013) Brain-wide pathway for waste clearance captured by contrast-enhanced MRI. J Clin Invest 123:1299–1309PubMedCentralPubMedCrossRef
33.
go back to reference Iliff JJ, Wang M, Liao Y, Plogg BA, Peng W, Gundersen GA, Benveniste H, Vates GE, Deane R, Goldman SA, Nagelhus EA, Nedergaard M (2012) A paravascular pathway facilitates CSF flow through the brain parenchyma and the clearance of interstitial solutes, including amyloid beta. Sci Transl Med 4:147ra111PubMedCentralPubMedCrossRef Iliff JJ, Wang M, Liao Y, Plogg BA, Peng W, Gundersen GA, Benveniste H, Vates GE, Deane R, Goldman SA, Nagelhus EA, Nedergaard M (2012) A paravascular pathway facilitates CSF flow through the brain parenchyma and the clearance of interstitial solutes, including amyloid beta. Sci Transl Med 4:147ra111PubMedCentralPubMedCrossRef
34.
go back to reference Farag E, Abdou A, Riad I, Borsellino SR, Schubert A (2005) Cerebellar hemorrhage caused by cerebrospinal fluid leak after spine surgery. Anesth Analg 100:545–546PubMedCrossRef Farag E, Abdou A, Riad I, Borsellino SR, Schubert A (2005) Cerebellar hemorrhage caused by cerebrospinal fluid leak after spine surgery. Anesth Analg 100:545–546PubMedCrossRef
35.
go back to reference Hara T, Matsuda M, Watanabe S, Nakai K, Yamamoto T, Matsumura A (2013) Remote cerebellar hemorrhage after removal of a supratentorial glioma without perioperative CSF loss: a case report. Case Rep Surg 2013:305039PubMedCentralPubMed Hara T, Matsuda M, Watanabe S, Nakai K, Yamamoto T, Matsumura A (2013) Remote cerebellar hemorrhage after removal of a supratentorial glioma without perioperative CSF loss: a case report. Case Rep Surg 2013:305039PubMedCentralPubMed
36.
go back to reference Hempelmann RG, Mater E (2012) Remote intracranial parenchymal haematomas as complications of spinal surgery: presentation of three cases with minor or untypical symptoms. Eur Spine J 21(Suppl 4):S564–S568PubMedCrossRef Hempelmann RG, Mater E (2012) Remote intracranial parenchymal haematomas as complications of spinal surgery: presentation of three cases with minor or untypical symptoms. Eur Spine J 21(Suppl 4):S564–S568PubMedCrossRef
37.
go back to reference Akai K, Uchigasaki S, Tanaka U, Komatsu A (1987) Normal pressure hydrocephalus. Neuropathological study. Acta Pathol Jpn 37(1):97–110PubMed Akai K, Uchigasaki S, Tanaka U, Komatsu A (1987) Normal pressure hydrocephalus. Neuropathological study. Acta Pathol Jpn 37(1):97–110PubMed
38.
Metadata
Title
Normal pressure hydrocephalus as a failure of ICP homeostasis mechanism: the hidden role of Monro–Kellie doctrine in the genesis of NPH
Author
Asem Salma
Publication date
01-05-2014
Publisher
Springer Berlin Heidelberg
Published in
Child's Nervous System / Issue 5/2014
Print ISSN: 0256-7040
Electronic ISSN: 1433-0350
DOI
https://doi.org/10.1007/s00381-014-2385-8

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