Skip to main content
Top
Published in: Fluids and Barriers of the CNS 1/2023

Open Access 01-12-2023 | Intracranial Hypertension | Research

Transient intracranial pressure elevations (B waves) are associated with sleep apnea

Authors: Casper Schwartz Riedel, Isabel Martinez-Tejada, Morten Andresen, Jens E. Wilhjelm, Poul Jennum, Marianne Juhler

Published in: Fluids and Barriers of the CNS | Issue 1/2023

Login to get access

Abstract

Background

Repetitive transient intracranial pressure waveform elevations up to 50 mmHg (ICP B-waves) are often used to define pathological conditions and determine indications for ICP-reducing treatment. We recently showed that nocturnal transient ICP elevations are present in patients without structural brain lesions or hydrocephalus in whom they are associated with sleep apnea. However, whether this signifies a general association between ICP macropatterns and sleep apnea remains unknown.

Methods

We included 34 patients with hydrocephalus, or idiopathic intracranial hypertension (IIH), who were referred to the Neurosurgical Department, Copenhagen, Denmark, from 2017 to 2021. Every patient underwent diagnostic overnight ICP monitoring for clinical indications, with simultaneous polysomnography (PSG) sleep studies. All transient ICP elevations were objectively quantified in all patients. Three patients were monitored with continuous positive airway pressure (CPAP) treatment for an additional night.

Results

All patients had transient ICP elevations associated with sleep apnea. The mean temporal delay from sleep apnea to transient ICP elevations for all patients was 3.6 s (SEM 0.2 s). Ramp-type transient ICP elevations with a large increase in ICP were associated with rapid eye movement (REM) sleep and sinusoidal-type elevations with non-REM (NREM) sleep. In three patients treated with CPAP, the treatment reduced the number of transient ICP elevations with a mean of 37%. CPAP treatment resulted in insignificant changes in the average ICP in two patients but elevated the average ICP during sleep in one patient by 5.6 mmHg.

Conclusion

The findings suggest that sleep apnea causes a significant proportion of transient ICP elevations, such as B-waves, and sleep apnea should be considered in ICP evaluation. Treatment of sleep apnea with CPAP can reduce the occurrence of transient ICP elevations. More research is needed on the impact of slow oscillating mechanisms on transient ICP elevations during high ICP and REM sleep.
Appendix
Available only for authorised users
Literature
1.
go back to reference Lundberg N. Continuous recording and control of ventricular fluid pressure in neurosurgical practice. Acta Psychiatr Scand Suppl. 1960;36:1–193.PubMed Lundberg N. Continuous recording and control of ventricular fluid pressure in neurosurgical practice. Acta Psychiatr Scand Suppl. 1960;36:1–193.PubMed
3.
go back to reference Droste DW, Krauss JK. Oscillations of cerebrospinal fluid pressure in nonhydrocephalic persons. Neurol Res. 1997;19:135–8.CrossRefPubMed Droste DW, Krauss JK. Oscillations of cerebrospinal fluid pressure in nonhydrocephalic persons. Neurol Res. 1997;19:135–8.CrossRefPubMed
4.
go back to reference Riedel CS, et al. B-waves are present in patients without intracranial pressure disturbances. J Sleep Res. 2021;30:e13214.CrossRefPubMed Riedel CS, et al. B-waves are present in patients without intracranial pressure disturbances. J Sleep Res. 2021;30:e13214.CrossRefPubMed
5.
go back to reference Jennum P, Børgesen SE. Intracranial pressure and obstructive sleep apnea. Chest. 1989;95:279–83.CrossRefPubMed Jennum P, Børgesen SE. Intracranial pressure and obstructive sleep apnea. Chest. 1989;95:279–83.CrossRefPubMed
6.
go back to reference Yokota A, Matsuoka S, Ishikawa T, Kohshi K, Kajiwara H. Overnight recordings of intracranial pressure and electroencephalography in neurosurgical patients. Part II: changes in intracranial pressure during sleep. J UOEH. 1989;11:383–91.CrossRefPubMed Yokota A, Matsuoka S, Ishikawa T, Kohshi K, Kajiwara H. Overnight recordings of intracranial pressure and electroencephalography in neurosurgical patients. Part II: changes in intracranial pressure during sleep. J UOEH. 1989;11:383–91.CrossRefPubMed
7.
8.
go back to reference Riedel CS, Milan JB, Juhler M, Jennum P. Sleep-disordered breathing is frequently associated with idiopathic normal pressure hydrocephalus but not other types of hydrocephalus. Sleep. 2022;45:1–8.CrossRef Riedel CS, Milan JB, Juhler M, Jennum P. Sleep-disordered breathing is frequently associated with idiopathic normal pressure hydrocephalus but not other types of hydrocephalus. Sleep. 2022;45:1–8.CrossRef
9.
go back to reference Kristensen B, Malm J, Rabben T. Effects of transient and persistent cerebrospinal fluid drainage on sleep disordered breathing in patients with idiopathic adult hydrocephalus syndrome. J Neurol Neurosurg Psychiatry. 1998;65:497–501.CrossRefPubMedPubMedCentral Kristensen B, Malm J, Rabben T. Effects of transient and persistent cerebrospinal fluid drainage on sleep disordered breathing in patients with idiopathic adult hydrocephalus syndrome. J Neurol Neurosurg Psychiatry. 1998;65:497–501.CrossRefPubMedPubMedCentral
10.
go back to reference Román GC, Verma AK, Zhang YJ, Fung SH. Idiopathic normal-pressure hydrocephalus and obstructive sleep apnea are frequently associated: a prospective cohort study. J Neurol Sci. 2018;395:164–8.CrossRefPubMed Román GC, Verma AK, Zhang YJ, Fung SH. Idiopathic normal-pressure hydrocephalus and obstructive sleep apnea are frequently associated: a prospective cohort study. J Neurol Sci. 2018;395:164–8.CrossRefPubMed
11.
go back to reference Stephensen H, et al. Objective B wave analysis in 55 patients with non-communicating and communicating hydrocephalus. J Neurol Neurosurg Psychiatry. 2005;76:965–70.CrossRefPubMedPubMedCentral Stephensen H, et al. Objective B wave analysis in 55 patients with non-communicating and communicating hydrocephalus. J Neurol Neurosurg Psychiatry. 2005;76:965–70.CrossRefPubMedPubMedCentral
12.
go back to reference Symon L, Dorsch NW, Stephens RJ. Pressure waves in so-called low-pressure hydrocephalus. Lancet. 1972;2:1291–2.CrossRefPubMed Symon L, Dorsch NW, Stephens RJ. Pressure waves in so-called low-pressure hydrocephalus. Lancet. 1972;2:1291–2.CrossRefPubMed
13.
go back to reference Krauss JK, et al. The relation of intracranial pressure B-waves to different sleep stages in patients with suspected normal pressure hydrocephalus. Acta Neurochir. 1995;136:195–203.CrossRefPubMed Krauss JK, et al. The relation of intracranial pressure B-waves to different sleep stages in patients with suspected normal pressure hydrocephalus. Acta Neurochir. 1995;136:195–203.CrossRefPubMed
15.
go back to reference Friedman DI, Jacobson DM. Diagnostic criteria for idiopathic intracranial hypertension. Neurology. 2002;59:1492–5.CrossRefPubMed Friedman DI, Jacobson DM. Diagnostic criteria for idiopathic intracranial hypertension. Neurology. 2002;59:1492–5.CrossRefPubMed
16.
go back to reference Martinez-Tejada I, Riedel CS, Juhler M, Andresen M, Wilhjelm JE. k-Shape clustering for extracting macro-patterns in intracranial pressure signals. Fluids Barriers CNS. 2022;19:12.CrossRefPubMedPubMedCentral Martinez-Tejada I, Riedel CS, Juhler M, Andresen M, Wilhjelm JE. k-Shape clustering for extracting macro-patterns in intracranial pressure signals. Fluids Barriers CNS. 2022;19:12.CrossRefPubMedPubMedCentral
18.
go back to reference Venes JLB. B waves—a reflection of cardiorespiratory or cerebral nervous systems rhythm? Childs Brain. 1979;5:352–60.PubMed Venes JLB. B waves—a reflection of cardiorespiratory or cerebral nervous systems rhythm? Childs Brain. 1979;5:352–60.PubMed
20.
go back to reference Ainslie PN, Duffin J. Integration of cerebrovascular CO2 reactivity and chemoreflex control of breathing: mechanisms of regulation, measurement, and interpretation. Am J Physiol Regul Integr Comp Physiol. 2009;296:R1473-9.CrossRefPubMed Ainslie PN, Duffin J. Integration of cerebrovascular CO2 reactivity and chemoreflex control of breathing: mechanisms of regulation, measurement, and interpretation. Am J Physiol Regul Integr Comp Physiol. 2009;296:R1473-9.CrossRefPubMed
21.
22.
go back to reference Wilson MH. Monro-Kellie 2.0: the dynamic vascular and venous pathophysiological components of intracranial pressure. J Cereb Blood Flow Metab. 2016;36:1338–50.CrossRefPubMedPubMedCentral Wilson MH. Monro-Kellie 2.0: the dynamic vascular and venous pathophysiological components of intracranial pressure. J Cereb Blood Flow Metab. 2016;36:1338–50.CrossRefPubMedPubMedCentral
23.
go back to reference Ito H, et al. Arterial fraction of cerebral blood volume in humans measured by positron emission tomography. Ann Nucl Med. 2001;15:111–6.CrossRefPubMed Ito H, et al. Arterial fraction of cerebral blood volume in humans measured by positron emission tomography. Ann Nucl Med. 2001;15:111–6.CrossRefPubMed
24.
go back to reference Ito H, Ibaraki M, Kanno I, Fukuda H, Miura S. Changes in the arterial fraction of human cerebral blood volume during hypercapnia and hypocapnia measured by positron emission tomography. J Cereb Blood Flow Metab. 2005;25:852–7.CrossRefPubMed Ito H, Ibaraki M, Kanno I, Fukuda H, Miura S. Changes in the arterial fraction of human cerebral blood volume during hypercapnia and hypocapnia measured by positron emission tomography. J Cereb Blood Flow Metab. 2005;25:852–7.CrossRefPubMed
25.
go back to reference Dreha-Kulaczewski S, et al. Identification of the upward movement of human CSF in vivo and its relation to the brain venous system. J Neurosci. 2017;37:2395–402.CrossRefPubMedPubMedCentral Dreha-Kulaczewski S, et al. Identification of the upward movement of human CSF in vivo and its relation to the brain venous system. J Neurosci. 2017;37:2395–402.CrossRefPubMedPubMedCentral
26.
go back to reference Vinje V, et al. Respiratory influence on cerebrospinal fluid flow—a computational study based on long-term intracranial pressure measurements. Sci Rep. 2019;9:1–13.CrossRef Vinje V, et al. Respiratory influence on cerebrospinal fluid flow—a computational study based on long-term intracranial pressure measurements. Sci Rep. 2019;9:1–13.CrossRef
28.
go back to reference Ingvar DH. Cerebral blood flow and metabolism related to EEG and cerebral functions. Acta Anaesthesiol Scand Suppl. 1971;45:110–4.CrossRefPubMed Ingvar DH. Cerebral blood flow and metabolism related to EEG and cerebral functions. Acta Anaesthesiol Scand Suppl. 1971;45:110–4.CrossRefPubMed
29.
go back to reference Reivich M, Isaacs G, Evarts E, Kety S. Regional cerebral blood flow during REM and slow wave sleep. Trans Am Neurol Assoc. 1967;92:70–4.PubMed Reivich M, Isaacs G, Evarts E, Kety S. Regional cerebral blood flow during REM and slow wave sleep. Trans Am Neurol Assoc. 1967;92:70–4.PubMed
30.
go back to reference Reivich M, Isaacs G, Evarts E, Kety S. The effect of slow wave sleep and REM sleep on regional cerebral blood flow in cats. J Neurochem. 1968;15:301–6.CrossRefPubMed Reivich M, Isaacs G, Evarts E, Kety S. The effect of slow wave sleep and REM sleep on regional cerebral blood flow in cats. J Neurochem. 1968;15:301–6.CrossRefPubMed
31.
go back to reference Kuchiwaki H, et al. Pressure wave with apnoea evaluated by sleep level in patient with ventricular dilation. Neurol Res. 1988;10:105.CrossRefPubMed Kuchiwaki H, et al. Pressure wave with apnoea evaluated by sleep level in patient with ventricular dilation. Neurol Res. 1988;10:105.CrossRefPubMed
32.
go back to reference Sánchez-de-la-Torre M, Campos-Rodriguez F, Barbé F. Obstructive sleep apnoea and cardiovascular disease. Lancet Respir Med. 2013;1:61–72.CrossRefPubMed Sánchez-de-la-Torre M, Campos-Rodriguez F, Barbé F. Obstructive sleep apnoea and cardiovascular disease. Lancet Respir Med. 2013;1:61–72.CrossRefPubMed
33.
go back to reference Naito R, et al. Factors associated with the improvement of left ventricular systolic function by continuous positive airway pressure therapy in patients with heart failure with reduced ejection fraction and obstructive sleep apnea. Front Neurol. 2022;13:781054.CrossRefPubMedPubMedCentral Naito R, et al. Factors associated with the improvement of left ventricular systolic function by continuous positive airway pressure therapy in patients with heart failure with reduced ejection fraction and obstructive sleep apnea. Front Neurol. 2022;13:781054.CrossRefPubMedPubMedCentral
35.
go back to reference McNamara ME, Millman RP, Epstein MH, Fogel BS. The association of normal-pressure hydrocephalus with obstructive sleep apnea. Top Geriatr. 1992;5:238–40. McNamara ME, Millman RP, Epstein MH, Fogel BS. The association of normal-pressure hydrocephalus with obstructive sleep apnea. Top Geriatr. 1992;5:238–40.
36.
go back to reference Kuriyama N, et al. Retrograde jugular flow associated with idiopathic normal pressure hydrocephalus. Ann Neurol. 2008;64:217–21.CrossRefPubMed Kuriyama N, et al. Retrograde jugular flow associated with idiopathic normal pressure hydrocephalus. Ann Neurol. 2008;64:217–21.CrossRefPubMed
Metadata
Title
Transient intracranial pressure elevations (B waves) are associated with sleep apnea
Authors
Casper Schwartz Riedel
Isabel Martinez-Tejada
Morten Andresen
Jens E. Wilhjelm
Poul Jennum
Marianne Juhler
Publication date
01-12-2023
Publisher
BioMed Central
Published in
Fluids and Barriers of the CNS / Issue 1/2023
Electronic ISSN: 2045-8118
DOI
https://doi.org/10.1186/s12987-023-00469-6

Other articles of this Issue 1/2023

Fluids and Barriers of the CNS 1/2023 Go to the issue