A quantitative model of the cerebral windkessel and its relevance to disorders of intracranial dynamics.

OBJECTIVE: Traditional models of intracranial dynamics fail to capture several important features of the intracranial pressure (ICP) pulse. Experiments show that, at a local amplitude minimum, the ICP pulse normally precedes the arterial blood pressure (ABP) pulse, and the cranium is a band-stop filter centered at the heart rate for the ICP pulse with respect to the ABP pulse, which is the cerebral windkessel mechanism. These observations are inconsistent with existing pressure-volume models. METHODS: To explore these issues, the authors modeled the ABP and ICP pulses by using a simple electrical tank circuit, and they compared the dynamics of the circuit to physiological data from dogs by using autoregressive with exogenous inputs (ARX) modeling. RESULTS: The authors' ARX analysis showed close agreement between the circuit and pulse suppression in the canine cranium, and they used the analogy between the circuit and the cranium to examine the dynamics that underlie this pulse suppression. CONCLUSIONS: This correspondence between physiological data and circuit dynamics suggests that the cerebral windkessel consists of the rhythmic motion of the brain parenchyma and CSF that continuously opposes systolic and diastolic blood flow. Such motion has been documented with flow-sensitive MRI. In thermodynamic terms, the direct current (DC) power of cerebral arterial perfusion drives smooth capillary flow and alternating current (AC) power shunts pulsatile energy through the CSF to the veins. This suggests that hydrocephalus and related disorders are disorders of CSF path impedance. Obstructive hydrocephalus is the consequence of high CSF path impedance due to high resistance. Normal pressure hydrocephalus (NPH) is the consequence of high CSF path impedance due to low inertance and high compliance. Low-pressure hydrocephalus is the consequence of high CSF path impedance due to high resistance and high compliance. Ventriculomegaly is an adaptive physiological response that increases CSF path volume and thereby reduces CSF path resistance and impedance. Pseudotumor cerebri is the consequence of high DC power with normal CSF path impedance. CSF diversion by shunting is an accessory windkessel-it drains energy (and thereby lowers ICP) and lowers CSF path resistance and impedance. Cushing's reflex is an accessory windkessel in extremis-it maintains DC power (arterial hypertension) and reduces AC power (bradycardia). The windkessel theory is a thermodynamic approach to the study of energy flow through the cranium, and it points to a new understanding of hydrocephalus and related disorders.

Brain Circuitry of Consciousness: A Review of Current Models and a Novel Synergistic Model With Clinical Application.

How consciousness arises in the brain has important implications for clinical decision-making. We summarize recent findings in consciousness studies to provide a toolkit for clinicians to assess deficits in consciousness and predict outcomes after brain injury. Commonly encountered disorders of consciousness are highlighted, followed by the clinical scales currently used to diagnose them. We review recent evidence describing the roles of the thalamocortical system and brainstem arousal nuclei in supporting awareness and arousal and discuss the utility of various neuroimaging studies in evaluating disorders of consciousness. We explore recent theoretical progress in mechanistic models of consciousness, focusing on 2 major models, the global neuronal workspace and integrated information theory, and review areas of controversy. Finally, we consider the potential implications of recent research for the day-to-day decision-making of clinical neurosurgeons and propose a simple "three-strikes" model to infer the integrity of the thalamocortical system, which can guide prognosticating return to consciousness.

Why don't ventricles dilate in pseudotumor cerebri? A circuit model of the cerebral windkessel.

OBJECTIVE: Pseudotumor cerebri is a disorder of intracranial dynamics characterized by elevated intracranial pressure (ICP) and chronic cerebral venous hypertension without structural abnormalities. A perplexing feature of pseudotumor is the absence of the ventriculomegaly found in obstructive hydrocephalus, although both diseases are associated with increased resistance to cerebrospinal fluid (CSF) resorption. Traditionally, the pathophysiology of ventricular dilation and obstructive hydrocephalus has been attributed to the backup of CSF due to impaired absorption, and it is unclear why backup of CSF with resulting ventriculomegaly would not occur in pseudotumor. In this study, the authors used an electrical circuit model to simulate the cerebral windkessel effect and explain the presence of ventriculomegaly in obstructive hydrocephalus but not in pseudotumor cerebri. METHODS: The cerebral windkessel is a band-stop filter that dampens the arterial blood pressure pulse in the cranium. The authors used a tank circuit with parallel inductance and capacitance to model the windkessel. The authors distinguished the smooth flow of blood and CSF and the pulsatile flow of blood and CSF by using direct current (DC) and alternating current (AC) sources, respectively. The authors measured the dampening notch from ABP to ICP as the band-stop filter of the windkessel. RESULTS: In obstructive hydrocephalus, loss of CSF pathway volume impaired the flow of AC power in the cranium and caused windkessel impairment, to which ventriculomegaly is an adaptation. In pseudotumor, venous hypertension affected DC power flow in the capillaries but did not affect AC power or the windkessel, therefore obviating the need for adaptive ventriculomegaly. CONCLUSIONS: In pseudotumor, the CSF spaces are unaffected and the windkessel remains effective. Therefore, ventricles remain normal in size. In hydrocephalus, the windkessel, which depends on the flow of AC power in patent CSF spaces, is impaired, and the ventricles dilate as an adaptive process to restore CSF pathway volume. The windkessel model explains both ventriculomegaly in obstructive hydrocephalus and the lack of ventriculomegaly in pseudotumor. This model provides a novel understanding of the pathophysiology of disorders of CSF dynamics and has significant implications in clinical management.

Bifrontal Biparietal Cruciate Decompressive Craniectomy in Pediatric Traumatic Brain Injury.

BACKGROUND: We investigated a novel surgical approach to decompressive craniectomy (DC), the bifrontal biparietal, or "cruciate," craniectomy, in severe pediatric traumatic brain injury (TBI). Cruciate DC was designed with a fundamentally different approach to intracranial pressure (ICP) control compared to traditional DC. Cruciate DC involves craniectomies in all 4 skull quadrants. The sagittal and coronal bone struts are disarticulated at the skull to allow the decompression of the sagittal sinus and bridging veins in addition to permitting cerebral expansion, thereby maintaining cranial compliance. OBJECTIVE: To characterize ICP control with cruciate DC in pediatric TBI. METHODS: We performed a retrospective review of TBI patients who underwent cruciate DC. We investigated mortality and preoperative and postoperative ICP. Group 1 underwent medical therapy prior to DC and Group 2 required immediate DC. RESULTS: Fifteen of 18 patients survived. In Group 1, mean preoperative ICP was 18.5 mm Hg and mean postoperative ICP was 11.5 mm Hg. In Group 2, mean preoperative ICP was 27.3 mm Hg and mean postoperative ICP was 15.0 mm Hg. CONCLUSION: Cruciate DC was associated with lowering ICP. We observed acute drops in ICP and long-term ICP control. The floating bone struts of the cruciate DC permits the decompression of the sagittal sinus and bridging veins, with maximal relief of cerebral edema.

Ventricular peritoneal shunt malfunction after operative correction of scoliosis: report of three cases.

BACKGROUND CONTEXT: Two of the most common disease processes associated with hydrocephalus in children are spina bifida and intraventricular hemorrhage of prematurity, both of which are known to be also associated with spinal deformity in later childhood. The occurrence of shunt malfunction after mechanical injury or stress to the hardware has been well documented. Newer techniques in the treatment of neuromuscular scoliosis, including anterior release with segmental fixation, have resulted in more powerful corrections of these large spinal deformities. A new potential cause of shunt malfunction is the aggressive correction of scoliosis. PURPOSE: To report patients with neuromuscular curves averaging 100° who were subsequently recognized to have perioperative shunt malfunction. STUDY DESIGN: Three case studies from a university hospital setting were included. PATIENT SAMPLE: All three children were young adolescents and had-long term shunts. Two of the children had spina bifida and a third had cerebral palsy. All children underwent anterior release of their scoliosis with posterior segmental instrumentation, with unit rods and sublaminar wires. All had significant correction of their scoliosis. OUTCOME MEASURES: Malfunctioning of the ventriculoperitoneal shunts were recorded. METHODS: Chart reviews of three cases were analyzed. RESULTS: Two children had shunt malfunctions within a month of their surgery, and one child had intraoperative recognition and externalization of the shunt. CONCLUSIONS: Older children undergoing repair of neuromuscular scoliosis are often preadolescents or adolescents who have the same indwelling shunt systems originally implanted in early infancy. The shunt may be brittle and calcified, and the peritoneal catheter may be short. The correction of scoliosis often results in an almost instantaneous growth of a few inches. Because of the potential difficulty in recognizing shunt malfunction in the perioperative period, consideration should be given for elective revision of the peritoneal catheter in children at risk.

Resonant and notch behavior in intracranial pressure dynamics.

OBJECT: The intracranial pulse pressure is often increased when neuropathology is present, particularly in cases of increased intracranial pressure (ICP) such as occurs in hydrocephalus. This pulse pressure is assumed to originate from arterial blood pressure oscillations entering the cranium; the fact that there is a coupling between the arterial blood pressure and the ICP is undisputed. In this study, the nature of this coupling and how it changes under conditions of increased ICP are investigated. METHODS: In 12 normal dogs, intracarotid and parenchymal pulse pressure were measured and their coupling was characterized using amplitude and phase transfer function analysis. Mean intracranial ICP was manipulated via infusions of isotonic saline into the spinal subarachnoid space, and changes in transfer function were monitored. RESULTS: Under normal conditions, the ICP wave led the arterial wave, and there was a minimum in the pulse pressure amplitude near the frequency of the heart rate. Under conditions of decreased intracranial compliance, the ICP wave began to lag behind the arterial wave and increased significantly in amplitude. Most interestingly, in many animals the pulse pressure exhibited a minimum in amplitude at a mean pressure that coincided with the transition from a leading to lagging ICP wave. CONCLUSIONS: This transfer function behavior is characteristic of a resonant notch system. This may represent a component of the intracranial Windkessel mechanism, which protects the microvasculature from arterial pulsatility. The impairment of this resonant notch system may play a role in the altered pulse pressure in conditions such as hydrocephalus and traumatic brain swelling. New models of intracranial dynamics are needed for understanding the frequency-sensitive behavior elucidated in these studies and could open a path for development of new therapies that are geared toward addressing the pulsation dysfunction in pathological conditions, such as hydrocephalus and traumatic brain injury, affecting ICP and flow dynamics.

Intracranial pressure waves: characterization of a pulsation absorber with notch filter properties using systems analysis: laboratory investigation.

OBJECT: The relationship between the waveform of intracranial pressure (ICP) and arterial blood pressure can be quantitatively characterized using a newly developed technique in systems analysis, the time-varying transfer function. This technique considers the arterial blood pressure as an input signal composed of multiple frequencies represented in the output ICP according to the transfer function imposed by the intracranial system on the input signal. The transfer function can change with time and with physiological manipulations. The authors examined data obtained from canine experiments involving manipulations of ICP. METHODS: The authors analyzed 11 experiments from 3 normal mongrel dogs under conditions of normal ICP and with changes in ICP made by bolus injection, infusion, or withdrawal of cerebrospinal fluid by using time-varying transfer function. RESULTS: During normal ICP periods, the gain of the transfer function displayed a deep notch (> or = 1 log unit) centered at or near the cardiac frequency. In systems terms, the intracranial compartment under normal conditions appears to act as a notch filter attenuating the cardiac frequency input relative to other frequencies. Epochs of ICP elevation showed suppression of the notch, and the notch was restored when ICP returned to normal. CONCLUSIONS: The intracranial system in these animals could be considered to include a pulsation absorber for which the target frequency appears to be close to the cardiac frequency. One possible source for such an absorber mechanism might be the free movement of cerebrospinal fluid, implying that impairment of this motion may have important clinical implications in various neurological conditions such as hydrocephalus.

Communicating hydrocephalus in adult rats with kaolin obstruction of the basal cisterns or the cortical subarachnoid space.

Communicating hydrocephalus (CH) occurs frequently, but clinically-relevant animal models amenable to diagnostic imaging and cerebrospinal fluid shunting are not available. In order to develop and characterize models of subarachnoid space (SAS) obstruction at the basal cisterns (BC) or cerebral convexities (CX), 25% kaolin was injected in adult female Sprague-Dawley rats following halothane anesthesia; intact- or saline-injected animals served as controls. For BC animals (n=28 hydrocephalics, n=20 controls), an anterior approach to the C1-clivus interval was employed and 30 microl of kaolin or saline was injected. For CX injections (n=13 hydrocephalics, n=3 controls), 50-60 microl of kaolin was injected bilaterally after separating the partitions in the SAS. In BC-injected rats, kaolin was observed grossly in the basal cisterns but not in the cisterna magna or at the foramina of Luschka, indicating that communicating (or extra-ventricular)--not obstructive--hydrocephalus had been induced. Following ketamine/xylazine anesthesia, magnetic resonance imaging (MRI) of gadolinium injected into the lateral ventricle also demonstrated CSF flow from the foramina of Luschka. MRI also revealed that ventriculomegaly progressed steadily in BC animals and by 2 weeks post-kaolin the mean Evan's ratio (frontal horn) increased significantly (mean 0.45 compared to 0.31 in intact- and 0.34 in saline-injected controls; p<0.001 for each). CX animals exhibited kaolin deposits covering approximately 80% of the cerebral hemispheres and developed noticeable ventriculomegaly (mean Evan's ratio 0.40), which was significant relative to intact animals (p=0.011) but not saline-injected controls. Surprisingly, ventriculomegaly following CX injections was less severe and much more protracted, requiring 3-4 months to develop compared to ventriculomegaly produced by BC obstruction. No hydrocephalic animals demonstrated obvious neurological deficits, but BC-injected animals that subsequently developed more severe ventriculomegaly exhibited nasal discharges and "coughing" for several days following kaolin injection. The new BC model is relevant because the clinical presentation of CH in children is often associated with obstruction at this site, while the CX model may be more representative of late adult onset normal pressure hydrocephalus.

Improved cerebrospinal fluid flow measurements using phase contrast balanced steady-state free precession.

We present a demonstration of phase contrast balanced steady-state free precession (PC-bSSFP) for measuring cerebrospinal fluid (CSF) flow in the brain and spine, and a comparison of measurements obtained with this technique to conventional phase contrast using incoherent gradient echoes (PC-GRE). With PC-GRE sequences, CSF images suffer from low signal-to-noise ratio (SNR), due to short repetition times required for adequate temporal resolution, and the long relaxation time of CSF. Furthermore, CSF flow is often nonlaminar, causing phase dispersion and signal loss in PC-GRE images. It is hypothesized that PC-bSSFP can improve CSF flow measurements with its high SNR and insensitivity to turbulent flow effects. CSF images acquired from the two techniques were compared in 13 healthy volunteers. Three measures were used to objectively evaluate the PC-bSSFP sequence: the CSF flow percentage, defined as the percentage of the total CSF region exhibiting pulsatile flow, net stroke volume and SNR. Images acquired with PC-bSSFP demonstrated pulsatile CSF flow in 35.8% (P<.005), 11.2% (P<.05) and 27.8% (P<.0005) more pixels than PC-GRE in the prepontine cistern, anterior and posterior cervical subarachnoid space (SAS), respectively. Likewise, measurements of stroke volume in these regions increased by 61.6% (P<.05), 16.8% (P<.001) and 48.3% (P<.0001), respectively. Similar comparisons in the aqueduct showed no statistical difference in stroke volumes between the two techniques (P=.5). The average gain in SNR was 3.3+/-1.7 (P<.001) in the prepontine cistern, 5.0+/-0.2 (P<.01) at the cervical level and 2.0+/-0.4 (P<.001) in the aqueduct in PC-bSSFP magnitude images over PC-GRE images. In addition to the obvious advantage of increased SNR, these results indicate that PC-bSSFP provides more complete measurements of CSF flow data than PC-GRE. PC-bSSFP can be used as a reliable technique for CSF flow quantification for the characterization of normal and altered intracranial CSF flow patterns.

Amplitude and phase of cerebrospinal fluid pulsations: experimental studies and review of the literature.

OBJECT: A recently developed model of communicating hydrocephalus suggests that ventricular dilation may be related to the redistribution of pulsations in the cranium from the subarachnoid spaces (SASs) into the ventricles. Based on this model, the authors have developed a method for analyzing flow pulsatility in the brain by using the ratio of aqueductal to cervical subarachnoid stroke volume and the phase of cerebrospinal fluid (CSF) flow, which is obtained at multiple locations throughout the cranium, relative to the phase of arterial flow. METHODS: Flow data were collected in a group of 15 healthy volunteers by using a series of images acquired with cardiac-gated, phase-contrast magnetic resonance imaging. The stroke volume ratio was 5.1 +/- 1.8% (mean +/- standard deviation). The phase lag in the aqueduct was -52.5 +/-16.5 degrees and the phase lag in the prepontine cistern was -22.1 +/- 8.2 degrees. The flow phase at the level of C-2 was -5.1 +/- 10.5 degrees, which was consistent with flow synchronous with the arterial pulse. The subarachnoid phase lag ventral to the pons was shown to decrease progressively to zero at the craniocervical junction. Flow in the posterior cervical SAS preceded the anterior space flow. CONCLUSIONS: Under normal conditions, pulsatile ventricular CSF flow is a small fraction of the net pulsatile CSF flow in the cranium. A thorough review of the literature supports the view that modified intracranial compliance can lead to redistribution of pulsations and increased intraventricular pulsations. The phase of CSF flow may also reflect the local and global compliance of the brain.

What we don't (but should) know about hydrocephalus.

In an effort to identify critical gaps in the prevailing knowledge of hydrocephalus, the authors formulated 10 key questions. 1) How do we define hydrocephalus? 2) How is cerebrosinal fluid (CSF) absorbed normally and what are the causes of CSF malabsorption in hydrocephalus? 3) Why do the ventricles dilate in communicating hydrocephalus? 4) What happens to the structure and function of the brain when it is compressed and stretched by the expanding ventricles? 5) What is the role of cerebrovenous pressure in hydrocephalus? 6) What causes normal-pressure hydrocephalus? 7) What causes low-pressure hydrocephalus? 8) What is the pathophysiology of slit ventricle syndrome? 9) What is the pathophysiological basis for neurological impairment in hydrocephalus, and to what extent is it reversible? 10) How is the brain of a child with hydrocephalus different from that of a young or elderly adult? Rigorous answers to these questions should lead to more effective and reliable treatments for this disorder.

Decompressive craniectomy in pediatric patients with traumatic brain injury with intractable elevated intracranial pressure.

BACKGROUND: Care of pediatric traumatic brain injury (TBI) has placed emphasis on maximizing cerebral perfusion to prevent ischemia and reperfusion injury. A subset of patients with TBI will continue to have refractory intracranial pressure (ICP) elevation despite aggressive therapy including ventriculostomy, pentobarbital coma, hypertonic saline, and diuretics. Decompressive craniectomy (DC) is a controversial treatment of severe TBI. It is our hypothesis that DC can enhance survival and minimize secondary brain injury in this patient subset. METHODS: Patients younger than 20 years treated at a level I regional trauma center between November 2001 and November 2004, who met inclusion criteria for the Brain Trauma Foundation TBI-trac clinical database were included. All patients with a mechanism of injury consistent with TBI and Glasgow Coma Scale score of less than 9 for at least 6 hours after resuscitation and who did not die in the emergency department are entered into a clinical database. Patients who arrived at the study hospital more than 24 hours after injury are excluded. RESULTS: There were 30 patients with TBI identified. The mean Glasgow Coma Scale score at presentation was 8 with a range of 3 to 13. Six patients underwent DC for intractable elevated ICP. Of 6 patient's postoperative ICP, 5 were less than 20 mm Hg. One patient required a return to the operating room where further débridement of brain was performed. All patients who received a DC survived and were discharged to a TBI rehabilitation facility. CONCLUSION: Although this is a small sample, DC should be considered in patients with TBI with refractory elevated ICP. Long-term follow-up of this patient population should consist of neuropsychiatric evaluation in conjunction with measurement of social function.

A model of pulsations in communicating hydrocephalus.

The traditional theory of communicating hydrocephalus has implicated the bulk flow component of CSF motion; that is, hydrocephalus is generally understood as an imbalance between CSF formation and absorption. The theory that the cause of communicating hydrocephalus is malabsorption of CSF at the arachnoid villi is not substantiated by experimental evidence or by physical reasoning. Flow-sensitive MRI has shown that nearly all CSF motion is pulsatile, and there is substantial evidence that hyperdynamic choroid plexus pulsations are necessary and sufficient for ventricular dilation in communicating hydrocephalus. We have developed a model of intracranial pulsations based on the analogy between the pulsatile motion of electrons in an electrical circuit and the pulsatile motion of blood and CSF in the cranium. Increased impedance to the flow of CSF pulsations in the subarachnoid space redistributes the flow of pulsations into the ventricular CSF and into the capillary and venous circulation. The salient features of communicating hydrocephalus, such as ventricular dilation, intracranial pressure waves, narrowing of the CSF-venous pressure gradient, diminished cerebral blood flow, elevated resistive index and malabsorption of CSF, emerge naturally from the model. We propose that communicating hydrocephalus is the result of a redistribution of CSF pulsations in the cranium.