Original Article
Spontaneous Low-Frequency Oscillations in Cerebral Vessels: Applications in Carotid Artery Disease and Ischemic Stroke

https://doi.org/10.1016/j.jstrokecerebrovasdis.2010.06.001Get rights and content

The etiology behind and physiological significance of spontaneous oscillations in the low-frequency spectrum in both systemic and cerebral vessels remain unknown. Experimental studies have proposed that spontaneous oscillations in cerebral blood flow reflect impaired cerebral autoregulation (CA). Analysis of CA by measurement of spontaneous oscillations in the low-frequency spectrum in cerebral vessels might be a useful tool for assessing risk and investigating different treatment strategies in carotid artery disease (CAD) and stroke. We reviewed studies exploring spontaneous oscillations in the low-frequency spectrum in patients with CAD and ischemic stroke, conditions known to involve impaired CA. Several studies have reported changes in oscillations after CAD and stroke after surgery and over time compared with healthy controls. Phase shift in the frequency domain and correlation coefficients in the time domain are the most frequently used parameters for analyzing spontaneous oscillations in systemic and cerebral vessels. At present, there is no gold standard for analyzing spontaneous oscillations in the low-frequency spectrum, and simplistic models of CA have failed to predict or explain the spontaneous oscillation changes found in CAD and stroke studies. Near-infrared spectroscopy is suggested as a future complementary tool for assessing changes affecting the cortical arterial system.

Section snippets

Etiology of Oscillations in the Low-Frequency Spectrum

Although spontaneous oscillations in the low-frequency spectrum in systemic blood pressure were discovered more than 130 years ago,29 the driving mechanisms responsible for these LFOs is unclear. Interventional studies have shown that neurogenic,31 metabolic32 and myogenic stimuli33 all affect LFOs. LFOs are believed to reflect changes in sympathetic tone34 based on human35 and animal36 studies, in which oscillations were found to be strongly attenuated by alpha-adrenoceptor blockade.

The

Functional Purpose of Oscillations in the Low-Frequency Spectrum

Very little data are available addressing the question of a physiological functional purpose of LFOs and VLFOs. Roche-Labarbe et al52 found associations between oscillations in the LFO range and spontaneous electroencephalogram bursts in neonates, suggesting that changes in oscillations are coupled to neuronal activity. In terms of blood flow and oxygen delivery, a mathematical model has shown greater oxygen conductance in vessels with an oscillating diameter compared with vessels with a

Measurement of Systemic and Cerebral Vessel Oscillations

Oscillations in the low-frequency spectrum in systemic MAP14, 21, 51 are commonly measured with a finger cuff system, using the volume clamp method of Penaz et al.55 TCD can be performed at the patient's bedside and provides high-resolution measurement of velocity of the middle cerebral artery (VMCA), which supplies each hemisphere with up to 80% of the flow volume to the brain.56 Because VMCA is easy to insonate, and the diameter of the MCA does not change even under strong blood pressure

Data Analysis of Spontaneous Oscillations

The most common approach to studying spontaneous oscillations is in the frequency domain, but oscillations can be analyzed in the time domain as well. A power spectrum can be calculated using a fast Fourier transform algorithm,60 where power reflects the amplitude of the oscillation at a given frequency. Data on coherence, phase shift, and gain between physiological oscillation signals can be obtained through computerized cross-spectral analysis.51 This analytical model investigates the linear

Oscillations in Carotid Stenosis Disease

Impairment of both static68 and dynamic68, 69, 70, 71 autoregulation has been found in CAD. However, manipulation-based studies require a certain level of compliance and can be stressful or even harmful to the patient. Therefore, several studies have investigated spontaneous dynamic autoregulation through transfer function and time domain analyses (Table 1, Table 2) in resting subjects without the need for any stressful manipulations.14, 17, 18, 19, 20, 26, 61, 72

The majority of studies

Oscillations in Ischemic Stroke

The presence or absence of CA in ischemic stroke seems to be critical to the maintenance of stable blood flow in the ischemic penumbra and to avoid excessive hyperperfusion.24 Olsen et al9 reported impaired CA in areas of the brain perfused by collateral circulation, believed to be the ischemic penumbra, compared with surrounding brain areas with normal CA. Global impairment of both conventional static75 and dynamic76 autoregulation also has been reported in stroke patients. Dawson et al76

Investigating LFOs by NIRS

Measuring changes in MCA blood flow velocity is only an indirect method of investigating oscillations, because fluctuations in CBF are caused by changes in small resistance vessels downstream from the MCA. NIRS is a noninvasive technique with a high time resolution that can measure relative changes in the concentrations of oxygenated (oxyHb) and deoxygenated hemoglobin (deoxyHb) at the cerebral cortex level.48, 80 Thus, NIRS measures local changes in cortical resistance vessels. The NIRS signal

Conclusion

The studies reviewed herein provide no clear link to the underlying etiology behind oscillations in the low-frequency spectrum. So far, no valid model can explain or predict the changes occurring in CAD and ischemic stroke, and there remains no gold standard for analyzing oscillations in the low-frequency spectrum. Analysis of spontaneous oscillations has demonstrated changes in patients with CAD and ischemic stroke compared with healthy controls both over time and after interventions in

Future Perspectives

Modeling of the complex interplay among modulations of vascular tone in different vascular compartments, blood flow, and delivery of oxygenated hemoglobin is likely required to guide the interpretation of data obtained from analysis of LFOs and VLFOs in cerebral vessels. This might lead to a standardized test for assessing oscillations in the low-frequency spectrum. Studies using both TCD and NIRS are warranted, because the complementary information regarding blood flow on the one hand and

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