The correlation between pulsatile intracranial pressure and indices of intracranial pressure-volume reserve capacity: results from ventricular infusion testing

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OBJECTIVE

The objective of this study was to examine how pulsatile and static intracranial pressure (ICP) scores correlate with indices of intracranial pressure-volume reserve capacity, i.e., intracranial elastance (ICE) and intracranial compliance (ICC), as determined during ventricular infusion testing.

METHODS

All patients undergoing ventricular infusion testing and overnight ICP monitoring during the 6-year period from 2007 to 2012 were included in the study. Clinical data were retrieved from a quality registry, and the ventricular infusion pressure data and ICP scores were retrieved from a pressure database. The ICE and ICC (= 1/ICE) were computed during the infusion phase of the infusion test.

RESULTS

During the period from 2007 to 2012, 82 patients with possible treatment-dependent hydrocephalus underwent ventricular infusion testing within the department of neurosurgery. The infusion tests revealed a highly significant positive correlation between ICE and the pulsatile ICP scores mean wave amplitude (MWA) and rise-time coefficient (RTC), and the static ICP score mean ICP. The ICE was negatively associated with linear measures of ventricular size. The overnight ICP recordings revealed significantly increased MWA (> 4 mm Hg) and RTC (> 20 mm Hg/sec) values in patients with impaired ICC (< 0.5 ml/mm Hg).

CONCLUSIONS

In this study cohort, there was a significant positive correlation between pulsatile ICP and ICE measured during ventricular infusion testing. In patients with impaired ICC during infusion testing (ICC < 0.5 ml/mm Hg), overnight ICP recordings showed increased pulsatile ICP (MWA > 4 mm Hg, RTC > 20 mm Hg/sec), but not increased mean ICP (< 10–15 mm Hg). The present data support the assumption that pulsatile ICP (MWA and RTC) may serve as substitute markers of pressure-volume reserve capacity, i.e., ICE and ICC.

ABBREVIATIONSCI = confidence interval; dP = change in pressure; dV = change in volume; EVD = external ventricular drain; ICC = intracranial compliance; ICE = intracranial elastance; ICP = intracranial pressure; MWA = mean wave amplitude; Po = opening pressure; Pp = plateau pressure; Rout = resistance to CSF outflow; RT = rise time; RTC = RT coefficient.

Abstract

OBJECTIVE

The objective of this study was to examine how pulsatile and static intracranial pressure (ICP) scores correlate with indices of intracranial pressure-volume reserve capacity, i.e., intracranial elastance (ICE) and intracranial compliance (ICC), as determined during ventricular infusion testing.

METHODS

All patients undergoing ventricular infusion testing and overnight ICP monitoring during the 6-year period from 2007 to 2012 were included in the study. Clinical data were retrieved from a quality registry, and the ventricular infusion pressure data and ICP scores were retrieved from a pressure database. The ICE and ICC (= 1/ICE) were computed during the infusion phase of the infusion test.

RESULTS

During the period from 2007 to 2012, 82 patients with possible treatment-dependent hydrocephalus underwent ventricular infusion testing within the department of neurosurgery. The infusion tests revealed a highly significant positive correlation between ICE and the pulsatile ICP scores mean wave amplitude (MWA) and rise-time coefficient (RTC), and the static ICP score mean ICP. The ICE was negatively associated with linear measures of ventricular size. The overnight ICP recordings revealed significantly increased MWA (> 4 mm Hg) and RTC (> 20 mm Hg/sec) values in patients with impaired ICC (< 0.5 ml/mm Hg).

CONCLUSIONS

In this study cohort, there was a significant positive correlation between pulsatile ICP and ICE measured during ventricular infusion testing. In patients with impaired ICC during infusion testing (ICC < 0.5 ml/mm Hg), overnight ICP recordings showed increased pulsatile ICP (MWA > 4 mm Hg, RTC > 20 mm Hg/sec), but not increased mean ICP (< 10–15 mm Hg). The present data support the assumption that pulsatile ICP (MWA and RTC) may serve as substitute markers of pressure-volume reserve capacity, i.e., ICE and ICC.

Continuous monitoring of intracranial pressure (ICP) has an important role in the treatment of neurosurgical patients.8,9 The ICP is characterized by the static ICP, which is the pressure difference between the intracranial compartment and atmospheric reference pressure, and the pulsatile ICP, which are pressure waves created by cardiac contractions.2 Part of the reason for ICP monitoring is the desire to obtain information about the intracranial pressure-volume reserve capacity, which is defined by the intracranial elastance (ICE; change in pressure [dP]/change in volume [dV]). As expressed in the pressure-volume curve (Fig. 1), when ICE is increased, a minor intracranial dV causes a major dP.25,28,29 While monitoring of ICE or intracranial compliance (ICC; the inverse of elastance, or ICC = 1/ICE) gained much attention in the neurosurgical literature decades ago, it has been used clinically only to a very limited extent, related to the risk of adding/subtracting volume to the intracranial compartment.29 To overcome the risk aspect, minor repetitive dV was developed,31 while several other researchers examined how the pulsatile ICP could be used as an indicator of ICE and ICC.6,35,41 Raised ICP amplitudes could be indicative of impaired intracranial pressure-volume reserve capacity,2,3,6,20 but could also be affected by several other mechanisms such as altered vascular compliance and cerebral blood volume variability.5,39

FIG. 1.
FIG. 1.

A: The intracranial pressure-volume curve (elastance curve) describes the change in static pressure (dP) in response to a given intracranial volume change (dV), which depends on the intracranial volume load. The ICE (dP/dV) is increased when intracranial pressure-volume reserve capacity is reduced. The pressure-volume curve refers to the static pressure, i.e., mean ICP. Ventricular infusion increases the intracranial volume load and causes movement to the right on the pressure-volume curve. B: The present study examined the association between the ICE and the cardiac-induced pulsatile ICP, based on an assumption that pulsatile ICP changes with ICE. C: The hypothesis was that with increased ICE the single-wave amplitudes (A) and RTCs (= A/RT) increased, while the RT shortened. E = ICE.

In recent years, measurement of the pulsatile ICP, in particular the ICP pulse wave amplitude, has received renewed attention.13,17,21,33,40 This is related to the fact that computerized analysis of the ICP waveform allows for improved information about the pulsatile ICP.11,37 It remains a topic of debate as to how the various indices of pulsatile ICP analyzed with modern computerized methods are associated with the intracranial pressure-volume reserve capacity.5,7,21,24 Hence, further studies are needed to determine the association between pulsatile ICP and ICE.

In our department, ventricular infusion testing has been used in patients with questionable shunt-dependent hydrocephalus.26,27 During steady-state ventricular infusion testing, the intracranial volume load is artificially increased, and the static ICP determined. In 2007, we introduced a computerized ventricular infusion test, including determination of the pulsatile ICP (Fig. 2). In the present study, information about ICE was retrieved from ventricular infusion tests to further examine the association between pulsatile ICP and ICE. The hypothesis was that the pulsatile ICP correlates positively with ICE. The study also addressed the association between ICE and ventricular size measures.

FIG. 2.
FIG. 2.

A: A ventricular infusion test is illustrated by trend plots of mean ICP and MWA, incorporating the period before infusion (Po) and the period during infusion (infusion rate 1.5 ml/min). The Pp occurs at the end of infusion. Three 6-second time windows of the continuous pressure signal from the period of opening pressure (B), infusion period (C), and end of plateau pressure (D) illustrate the change in ICP wave morphology.

Methods

Patient Population and Study Design

The study included all patients who underwent ventricular infusion testing during the period from 2007 to 2012 within the Department of Neurosurgery, Oslo University Hospital–Rikshospitalet, Oslo. Oslo University Hospital–Rikshospitalet approved the study, and the Regional Committee for Medical and Health Research Ethics of Health Region South-East, Norway, was informed in writing, and had no objections to the study.

The aim of the present work was to examine the association between pulsatile ICP scores and indices of intracranial pressure-volume reserve capacity, i.e., ICE and ICC. The hypothesis was that pulsatile ICP correlates positively with ICE.

This study also addressed the association between ICE and indices of ventricular size. The rational for ventricular infusion testing in patients with possible treatment-dependent hydrocephalus is that increased ventricular size may be compensatory to reduced pressure-volume compensatory reserve capacity, which would be reflected in a negative correlation between ICE and ventricular size. The aim was not to examine the diagnostic value of ventricular infusion testing in hydrocephalus, nor the utility of the test in different types of hydrocephalus.

Pressure Monitoring and Ventricular Infusion Testing

Under local anesthesia, a small straight incision was made frontally on the right side. A bur hole approximately 1–1.5 cm was made, and underneath, a small incision in the dura. An external ventricular drain (EVD) with a built-in Codman ICP MicroSensor (Codman external drainage with ICP sensor, Codman/Johnson & Johnson) was introduced into the frontal horn of the cerebral ventricles. The distal end of the EVD was at the level of the foramen of Monroe/third ventricle. The bur hole opening was closed with bone wax to avoid CSF leakage.

The patient was transferred to the neurosurgical intermediate ward. The Codman ICP microsensor was connected to the Codman ICP Express monitor (Codman/Johnson & Johnson), and then connected to an analog-digital converter (Sensometrics Pressure Logger, dPCom), which was connected to a computer with the Sensometrics Software (dPCom) used for online recording of ICP signals (sampling rate 200 Hz). The monitoring was continued overnight until the next morning, when the ventricular infusion test was performed.

The patient was awake during infusion testing. Figure 2 shows one example of a ventricular infusion test. First, ICP was recorded for a few minutes, representing the opening phase (Po). Via the EVD, Ringer solution was infused at a standard infusion rate of 1.5 ml/min until a plateau pressure (Pp) was reached (Fig. 2). If ICP increased markedly without reaching a plateau, the infusion was ended.

Analysis of Pressure Measurements

The pulsatile ICP scores were computed online, according to a previously published method for automatic identification of cardiac-induced ICP waves.11 Briefly, the cardiac-induced waves were identified by their beginning and ending diastolic minimum pressures and systolic maximum pressures. For each cardiac-beat–induced ICP wave, the amplitude (“pulse amplitude”), the rise time (RT), and rise time coefficient (RTC) were determined (Fig. 1C). The ICP waveform indices mean wave amplitude (MWA), mean wave RT, and mean wave RTC were computed for subsequent 6-second time windows. Only 6-second time windows containing a minimum 4 cardiac-beat–induced waves were considered to be of good quality, and were used for the present analysis. The automatic method also identifies artifact waves due to noise in the pressure signal (e.g., due to patient movement, or sensor movement or dysfunction); artifact waves were thus omitted from the analysis. In addition to the pulsatile ICP, the static ICP (mean ICP) was also computed for each 6-second time window.

The software automatically determines the ICE during infusion. In short, the pressure difference (D) is computed over 15-second time windows as the difference in mean ICP determined over 3-second periods at the end (Pn) and beginning (Pn−1) of the 15-second time window (D = Pn − Pn−1). Hence, while Pn−1 represents time 0–3 seconds, Pn represents time 12–15 seconds. During this 15-second period, the volume change is 0.375 ml (corresponding to an in fusion rate of 1.5 ml/min). Accordingly, ICE = (Pn − Pn−1)/0.375 ml. The software applies a moving time window, allowing an updated value every subsequent 3-second period. For each infusion test, the ICE and ICC represent the average of all named 3-second periods during the infusion period. The ICC is the inverse of ICE (ICC = 1/ICE).

During infusion testing, the resistance to CSF outflow (Rout) was also calculated as the difference between the Pp and the Po, divided by infusion rate ([Pp − Po]/1.5 ml/min).14 With regard to the overnight ICP recordings, a standardized recording time from 11 pm until 7 am was applied to compare the pressure scores between patients.

Assessment of Ventricular Size

Linear measures of ventricular size were determined based on CT or MRI images obtained at the time of ICP monitoring. As previously described,12 the linear measures Evan's index, third ventricle index, cella media index, and the ventricular score were calculated.

Statistical Analysis

The statistical analyses were performed using SPSS software (version 22, IBM Corp.). Associations between observations were determined by the Pearson correlation coefficient. Differences between groups were determined using 1-way ANOVA. Significance was accepted at the 0.05 level.

Results

Patients

During the period from 2007 to 2012, 82 patients underwent ventricular infusion testing in the department. Demographic information about the patient cohort is presented in Table 1. In all patients, the clinical indication was diagnostic assessment of hydrocephalus. None of the patients had shunts.

TABLE 1.

Demographic and clinical data of the patient cohort*

VariableTotal CohortSurgery GroupConservative Treatment Group
No. of patients827210
Median age in yrs (range)53 (19–78)53 (19–78)47 (29–66)
Sex (F/M)40/4236/364/6
Type of hydrocephalus (%)
  Communicating35 (43)30 (42)5 (50)
  Noncommunicating47 (57)42 (58)5 (50)
Gait disturbance53 (65)48 (67)5 (50)
Incontinence28 (34)26 (36)2 (20)
Cognitive impairment56 (68)51 (71)5 (50)
Headache42 (51)35 (49)7 (70)
Nausea12 (15)10 (14)2 (20)
Lethargy20 (24)18 (25)2 (20)
Visual disturbances13 (16)11 (15)2 (20)
Median duration of symptoms in yrs (range)2 (0.3–20)2 (0–10)1 (0.3–20)
Ventricular size (range)
  Median Evan's index0.4 (0.2–0.7)0.4 (0.2–0.7)0.4 (0.3–0.7)
  Median ventricular score108 (52–194)108 (52–194)99 (73–178)
Outcome after surgery (%)
  Responders57 (79)
  Nonresponders15 (21)

None of the differences between surgery and conservative groups were significant as determined by 1-way ANOVA for continuous data and by the Pearson chi-square test for categorical data.

Ventricular Infusion Testing

No complications in ventricular infusion testing/ICP monitoring were observed. The median volume of infusion was 16 ml (range 5.9–31.8 ml), which corresponds to a median duration of infusion of 10.6 min (range 3.9–21.2 min).

After diagnostic assessment, 72 patients underwent surgery, i.e., shunt surgery in communicating hydrocephalus and endoscopic third ventriculostomy in noncommunicating hydrocephalus (surgery group), while 10 were managed conservatively (conservative treatment group). Among the 72 surgically treated patients, 57 were clinical responders and 15 nonresponders. While 57 patients (97%) were responders and 7 were nonresponders among 59 patients with a presumptive abnormal infusion test, 5 patients (39%) were responders among 13 patients with a normal infusion test (sensitivity 92%, specificity 53%; positive predictive value 88%, negative predictive value 62%; diagnostic accuracy 83%, diagnostic odds ratio 11.9 [95% confidence interval (CI) 3.0–46.7]).

Table 2 presents the pressures scores for the different management groups during ventricular infusion testing. Significant differences were noted between the groups.

TABLE 2.

Comparison of pressure scores during ventricular infusion testing for the different management groups

Ventricular Infusion TestingSurgery GroupConservative Treatment Group (n = 10)p Value*
Responders (n = 57)Nonresponders (n = 15)
Mean95% CIMean95% CIMean95% CI
Opening phase
  MWA (mm Hg)3.63.3–4.02.11.7–2.52.72.3–3.1<0.001
  RT (sec)0.210.19–0.230.240.20–0.270.190.14–0.25NS
  RTC (mm Hg/sec)20.817.9–23.611.17.3–14.818.911.6–26.2<0.001
  Mean ICP (mm Hg)8.17.0–9.27.44.0–10.85.32.8–7.9NS
Plateau phase
  MWA (mm Hg)9.68.7–10.64.63.4–5.85.64.5–6.7<0.001
  RT (sec)0.260.25–0.270.290.25–0.320.240.21–0.270.04
  RTC (mm Hg/sec)37.234.2–40.217.111.9–22.226.020.8–31.3<0.001
  Mean ICP (mm Hg)24.222.1–26.319.015.1–22.916.813.3–20.40.005
Infusion phase
  MWA (mm Hg)6.35.8–6.83.52.7–4.34.43.7–5.2<0.001
    % MWA >5 mm Hg60.552.5–68.421.45.3–37.425.58.3–42.7<0.001
  RT (sec)0.240.23–0.250.270.24–0.300.220.18–0.260.03
  RTC (mm Hg/sec)28.125.6–30.713.79.9–17.624.417.7–31.1<0.001
  Mean ICP (mm Hg)16.315.1–17.514.110.4–17.812.69.5–15.70.05
  ICE (mm Hg/ml)6.15.4–6.83.43.0–3.94.33.2–5.30.001
  ICC (ml/mm Hg)0.470.43–0.500.660.59–0.740.600.50–0.70<0.001

NS = nonsignificant.

Significant differences between all the 3 groups were determined by 1-way ANOVA.

Significant differences between responders and nonresponders were determined by 1-way ANOVA with a Bonferroni-corrected post hoc test (†p < 0.001, ‡p < 0.01).

Association Between Pulsatile ICP Scores and ICE

There was a highly significant positive correlation between ICE determined during ventricular infusion and the pulsatile ICP MWA (Fig. 3A) and ICP RTC (Fig. 3B), but not between ICE and RT (Fig. 3C).

FIG. 3.
FIG. 3.

The association between ICE and MWA (A), RTC (B), RT (C), and mean ICP (D) was determined during the period of ventricular infusion. On each plot the fit line is presented and the Pearson correlation coefficient (R) and significance level (p value) are given.

With regard to static ICP, the correlation between ICE and mean ICP was not as strong, although significant (Fig. 3D). No significant correlation between ICE and Rout was observed (Fig. 4).

FIG. 4.
FIG. 4.

The association between ICE and Rout was determined during the period of ventricular infusion. The fit line is presented as well as the Pearson correlation coefficient (R) with significance level.

In 1 patient, ICE was measured simultaneously within the ventricular CSF and the brain parenchyma, with close to identical ICE (2.85 mm Hg/ml in parenchyma vs 2.92 mm Hg/ml in ventricular CSF). In another patient ICE was determined simultaneously from the epidural space and the ventricular CSF, showing close to identical values (4.06 mm Hg/ml vs 4.14 mm Hg/ml).

Association Between ICE and Ventricular Size

ICE determined during ventricular infusion correlated negatively with the linear measures of ventricular size, i.e., Evan's index (Fig. 5A), cella media index (Fig. 5B), third ventricle index (Fig. 5C), and ventricular score (Fig. 5D). Thus, increasing ventricular size was accompanied by reduced ICE.

FIG. 5.
FIG. 5.

Graphs showing the association between ICE and Evan's index (A), cella media index (B), third ventricle index (C), and ventricular score (D). For each plot the fit line is presented as well as the Pearson correlation coefficient and significance level.

Pulsatile and Static ICP Scores for Different Levels of ICC

Given the literature referring to an upper threshold of ICC of 0.5 ml/mm Hg as indicative of impaired compliance, the ventricular infusion tests with ICC < 0.5 ml/mm Hg (n = 36) and ICC ≥ 0.5 ml/mm Hg (n = 46) were compared. In the group with ICC < 0.5 ml/mm Hg, both the MWA (Fig. 6A–C) and RTC (Fig. 6D–F) values were significantly increased during the opening, plateau, and infusion phases. Mean ICP was not as strongly increased, although it was significantly different during the infusion phase (Fig. 6G–I).

FIG. 6.
FIG. 6.

The ventricular infusion tests (n = 82) with ICC either < 0.5 ml/mm Hg (n = 36) or ≥ 0.5 ml/mm Hg (n = 46) were compared regarding MWA (A–C), RTC (D–F), and mean ICP (G–I) at opening pressure (A, D, and G), plateau pressure (B, E, and H) and infusion period (C, F, and I). Each error bar is presented as mean with 95% CIs. Differences between the 2 infusion test groups were determined by 1-way ANOVA.

The overnight pulsatile ICP scores of MWA and RTC were increased in the group with ICC < 0.5 ml/mm Hg during infusion testing, as compared with the group with ICC ≥ 0.5 ml/mm Hg (Table 3). Hence, in the group with ICC < 0.5 ml/mm Hg, the MWA values were > 4.0 mm Hg and RTC > 20 mm Hg/sec, which we tentatively consider as abnormal. On the other hand, the mean ICP was normal (< 10–15 mm Hg) in the groups with either ICC ≥ 0.5 ml/mm Hg or ICC < 0.5 ml/mm Hg, even though mean ICP was significantly higher in the latter group (Table 3).

TABLE 3.

The continuous overnight ICP wave/ICP scores categorized according to ICC during the infusion test*

Overnight ICP scoresVentricular Infusion Testsp Value
ICC <0.5 ml/mm Hg (n = 36)ICC ≥0.5 ml/mm Hg (n = 46)
Mean95% CIMean95% CI
ICP-wave parameters
  MWA
    Average (mm Hg)4.54.1–4.93.93.6–4.30.04
    % ≥5 mm Hg31.220.8–41.517.910.5–25.30.03
  Mean wave RT
    Average (sec)0.200.18–0.230.220.20–0.24NS
    % ≥0.20 sec55.741.9–69.466.755.0–78.5NS
  Mean wave RTC
    Average (mm Hg/sec)26.122.3–29.820.718.0–23.40.02
    % ≥30 mm Hg/sec28.117.4–38.816.57.5–25.5NS
Static ICP
  Mean ICP
    Average (mm Hg)9.47.8–10.97.05.7–8.20.02
    % ≥15 mm Hg11.14.4–17.83.51.5–5.50.02

ICP scores recorded from 11 pm to 7 am. Significant differences between the 2 infusion test groups were determined by 1-way ANOVA

Discussion

The present results from ventricular infusion testing showed a significant positive correlation between the pulsatile ICP scores and ICE. There was a negative correlation between ICE and linear measures of ventricular size. During overnight monitoring, the pulsatile ICP scores MWA (> 4 mm Hg) and RTC (> 20 mm Hg/sec) were increased in patients with impaired ICC (< 0.5 ml/mm Hg) during infusion testing. Also, mean ICP was increased in this group (ICC < 0.5 ml/mm Hg), although mean ICP was within normal levels (< 10–15 mm Hg).

Ventricular Infusion Testing

The ventricular infusion test has no widespread clinical application. In our department, ventricular infusion testing evolved from the use of lumbar infusion tests. The test primarily assessed shunt dependency in pediatric patients with hydrocephalus.26,27 Some other clinical researchers also used the ventricular infusion test to assess shunt dependency in patients with adult hydrocephalus.4,22 In patients with noncommunicating hydrocephalus, Tisell et al.38 found that preoperative ICE, determined during ventricular infusion, correlated positively with clinical improvement after third ventriculostomy. Since 2007, we have implemented computation of pulsatile ICP during infusion testing, comparable to the procedure performed during lumbar infusion testing.14

The current clinical indication for the test is to determine the need for shunt placement in selected patients with hydrocephalus, large ventricles, and questionable shunt dependency. The most common output of infusion testing is the Rout,4,14,27,30 which is computed from the static pressures ([Pp−Po]/infusion rate). It should be noted that it is presently unknown where the infused fluid is being absorbed. However, independent of the site of CSF absorption, indices of pressure-volume reserve capacity (ICE and ICC) can be determined during infusion testing. It was this latter output that provided the opportunity for determining how pulsatile ICP correlates with ICE in the present study.

Indices of Intracranial Pressure-Volume Reserve Capacity

The pressure-volume curve was established from studies in animals.25,28 The dP in response to dV, either as an addition or subtraction of volume, was expressed as ICE (dP/dV; Fig. 1). However, monitoring of ICE in the clinical context has not gained widespread application, not least because of the risk associated with artificial alterations of intracranial volume. To reduce risk, one approach has been rapid repetitive small changes in intracranial volume,31 which was implemented in a medical device for computation of ICC based on inflation/deflation of a balloon.32 Other approaches were to retrieve information about ICE/ICC from the ICP waveform (pulsatile ICP).6,35 More recently, ICE was derived from phase-contrast MRI.1

Monitoring of the static ICP (mean ICP) has served as an indicator of the pressure-volume reserve capacity, but may not be useful because mean ICP may be normal despite abnormal ICC.16,19

Association Between Pulsatile ICP and ICE

It is reasonable to further explore how pulsatile ICP associates with ICE. From a theoretical point of view, the pulse pressure is the pressure response to the intracranial volume change during each cardiac contraction. While the intracranial volume change is approximately 1 ml, our results suggest that the upper normal threshold of the pulse pressure amplitude is about 4 mm Hg. Consistent with this assumption, the ICP MWA increased when ICC became reduced. The present data from ventricular infusion testing support the previous results, showing a significant positive correlation between pulsatile ICP and ICE. In addition, the data extend previous observations by examining how the threshold values for pulsatile ICP and ICE/ICC relate.

There was no significant positive correlation between ICE and Rout in this study, which suggests no association between Rout and ICE. This observation is consistent with the results of others.30

Even though pulsatile ICP correlates positively with ICE and there is a proportional relationship between levels of pulsatile ICP and ICE, it is important to note that pulsatile ICP is not synonymous with ICE. This is because the pulsatile ICP and ICE are influenced by several factors, such as fluctuations in cerebral blood volume, blood vessel properties (vascular compliance), partial pressure of carbon dioxide levels, and properties of brain parenchyma (water content and cellular changes). However, despite this complex interaction of pathophysiological mechanisms, the present observations of a highly significant positive correlation between pulsatile ICP and ICE is of interest because pulsatile ICP is retrieved directly from the ICP signal used for computation of static ICP. Moreover, the ICP MWA can be measured epidurally with equal confidence as parenchyma measurements.10,18 Therefore, minimally invasive monitoring of MWA, indicative of ICE, is feasible.

Ventricular Size and Pressure-Volume Reserve Capacity

The reasoning behind today's ventricular infusion testing is an assumption that increased ventricular size may sometimes be a compensatory mechanism to improve the intracranial pressure-volume reserve capacity. Hence, during ventricular infusion, the intracranial volume load is artificially increased, which causes movement to the right on the pressure-volume curve, thereby increasing ICE and increasing the chance of detecting impaired pressure-volume reserve capacity. This assumption is supported by the present observations of a negative correlation between ICE and ventricular size, i.e., increased ventricular size was associated with reduced ICE. We have previously consistently not found any relationship between ventricular size and static or pulsatile ICP scores.12,36

The association between ventricular size and indices of pressure-volume reserve capacity most likely depends on the time of measurement during the disease process. While acutely increased ventricular size is probably associated with increased ICE, long-standing ventriculomegaly may be associated with the opposite. In the present cohort, the median duration of symptoms was 2.3 years prior to infusion testing. Further studies are needed to clarify how ventricular size relates to pressure-volume reserve capacity. Recently, we reported retrograde net aqueductal CSF flow (i.e., net direction of CSF flow toward the ventricles) in patients with normal pressure hydrocephalus; following shunting it was changed to antegrade aqueductal CSF flow.34

Clinical Thresholds for Indices of Pressure-Volume Reserve Capacity

While thresholds for ICE remain unclear, several studies have referred to impaired ICC when ICC is < 0.5 ml/mm Hg.23,42 In clinical practice, we consider an average MWA of > 4–5 mm Hg as indicative of abnormality. Evidence in favor of this concept was obtained in various groups of patients and clinical settings, including patients with subarachnoid hemorrhage,13 normal pressure hydrocephalus,17 pediatric hydrocephalus, and idiopathic intracranial hypertension.15 In the present study, the group with ICC < 0.5 ml/mm Hg during infusion testing had significantly higher overnight MWA values (4.5 mm Hg, 95% CI 4.1–4.9 mm Hg), as compared with those with compliance ≥ 0.5 ml/mm Hg. Accordingly, the present observations support our concept of reduced ICC when MWA is > 4 mm Hg.

The static ICP (mean ICP) was significantly higher in the group with ICC < 0.5 ml/mm Hg during infusion, but it is difficult to use in the individual patient as mean ICP was within normal thresholds (< 10–15 mm Hg) in both ICC groups (ICC < /≥ 0.5 ml/mm Hg).

Conclusions

In this study cohort, there was a significant positive correlation between pulsatile ICP and ICE measured during ventricular infusion testing. In patients with impaired ICC during infusion testing (ICC < 0.5 ml/mm Hg), overnight ICP recordings showed increased pulsatile ICP (MWA > 4 mm Hg, RTC > 20 mm Hg), but not increased mean ICP (< 10–15 mm Hg). The present data support the assumption that pulsatile ICP (MWA and RTC) may serve as substitute markers of pressure-volume reserve capacity, i.e., ICE and ICC.

Acknowledgments

I thank Hugo Pripp, PhD, Department of Biostatistics, Epidemiology, and Health Economics, Oslo University Hospital, Oslo, for statistical help during preparation of the paper. This study was completely funded by the Department of Neurosurgery, Oslo University Hospital–Rikshospitalet, Oslo, Norway.

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    Eide PKSorteberg W: Diagnostic intracranial pressure monitoring and surgical management in idiopathic normal pressure hydrocephalus: a 6-year review of 214 patients. Neurosurgery 66:80912010

  • 18

    Eide PKSorteberg W: Simultaneous measurements of intracranial pressure parameters in the epidural space and in brain parenchyma in patients with hydrocephalus. J Neurosurg 113:131713252010

  • 19

    Fukuhara TLuciano MGBrant CLKlauscie J: Effects of ventriculoperitoneal shunt removal on cerebral oxygenation and brain compliance in chronic obstructive hydrocephalus. J Neurosurg 94:5735812001

  • 20

    González-Darder JMBarcia-Salorio JL: Pulse amplitude and volume-pressure relationships in experimental hydrocephalus. Acta Neurochir (Wien) 97:1661701989

  • 21

    Howells TLewén ASköld MKRonne-Engström EEnblad P: An evaluation of three measures of intracranial compliance in traumatic brain injury patients. Intensive Care Med 38:106110682012

  • 22

    Kasprowicz MCzosnyka ZCzosnyka MMomjian SJuniewicz HPickard JD: Slight elevation of baseline intracranial pressure after fluid infusion into CSF space in patients with hydrocephalus. Neurol Res 26:6286312004

  • 23

    Kiening KLSchoening WNLanksch WRUnterberg AW: Intracranial compliance as a bed-side monitoring technique in severely head-injured patients. Acta Neurochir Suppl 81:1771802002

  • 24

    Kim DJCzosnyka ZKasprowicz MSmieleweski PBaledent OGuerguerian AM: Continuous monitoring of the Monro-Kellie doctrine: is it possible?. J Neurotrauma 29:135413632012

  • 25

    Löfgren Jvon Essen CZwetnow NN: The pressure-volume curve of the cerebrospinal fluid space in dogs. Acta Neurol Scand 49:5575741973

  • 26

    Lundar T: Shunt removal or replacement based on intraventricular infusion tests. Childs Nerv Syst 10:3373391994

  • 27

    Lundar TNornes H: Determination of ventricular fluid outflow resistance in patients with ventriculomegaly. J Neurol Neurosurg Psychiatry 53:8968981990

  • 28

    Marmarou AShulman KLaMorgese J: Compartmental analysis of compliance and outflow resistance of the cerebrospinal fluid system. J Neurosurg 43:5235341975

  • 29

    Miller JDGaribi JPickard JD: Induced changes of cerebrospinal fluid volume. Effects during continuous monitoring of ventricular fluid pressure. Arch Neurol 28:2652691973

  • 30

    Munch TNBech-Azeddine RBoegeskov LGjerris FJuhler M: Evaluation of the lumbar and ventricular infusion test in the diagnostic strategy of pediatric hydrocephalus and the therapeutic implications. Childs Nerv Syst 23:67712007

  • 31

    Piper IRChan KHWhittle IRMiller JD: An experimental study of cerebrovascular resistance, pressure transmission, and craniospinal compliance. Neurosurgery 32:8058161993

  • 32

    Portella GCormio MCiterio GContant CKiening KEnblad P: Continuous cerebral compliance monitoring in severe head injury: its relationship with intracranial pressure and cerebral perfusion pressure. Acta Neurochir (Wien) 147:7077132005

  • 33

    Qvarlander SLundkvist BKoskinen LOMalm JEklund A: Pulsatility in CSF dynamics: pathophysiology of idiopathic normal pressure hydrocephalus. J Neurol Neurosurg Psychiatry 84:7357412013

  • 34

    Ringstad GEmblem KEEide PK: Phase-contrast magnetic resonance imaging reveals net retrograde aqueductal flow in idiopathic normal pressure hydrocephalus. J Neurosurg [epub ahead of print December 4 2015. DOI: 10.3171/20156.JNS15496]

  • 35

    Robertson CSNarayan RKContant CFGrossman RGGokaslan ZLPahwa R: Clinical experience with a continuous monitor of intracranial compliance. J Neurosurg 71:6736801989

  • 36

    Sæhle TEide PK: Association between ventricular volume measures and pulsatile and static intracranial pressure scores in non-communicating hydrocephalus. J Neurol Sci 350:33392015

  • 37

    Smielewski PLavinio ATimofeev IRadolovich DPerkes IPickard JD: ICM+, a flexible platform for investigations of cerebrospinal dynamics in clinical practice. Acta Neurochir Suppl 102:1451512008

  • 38

    Tisell MEdsbagge MStephensen HCzosnyka MWikkelsø C: Elastance correlates with outcome after endoscopic third ventriculostomy in adults with hydrocephalus caused by primary aqueductal stenosis. Neurosurgery 50:70772002

  • 39

    van Eijndhoven JHAvezaat CJ: Cerebrospinal fluid pulse pressure and the pulsatile variation in cerebral blood volume: an experimental study in dogs. Neurosurgery 19:5075221986

  • 40

    Wagshul MEEide PKMadsen JR: The pulsating brain: A review of experimental and clinical studies of intracranial pulsatility. Fluids Barriers CNS 8:52011

  • 41

    Wilkinson HASchuman NRuggiero J: Nonvolumetric methods of detecting impaired intracranial compliance or reactivity: pulse width and wave form analysis. J Neurosurg 50:7587671979

  • 42

    Yau YPiper IContant CCiterio GKiening KEnblad P: Multi-centre assessment of the Spiegelberg compliance monitor: interim results. Acta Neurochir Suppl 81:1671702002

Disclosures

Per Kristian Eide has a financial interest in the software company (dPCom AS, Oslo) manufacturing the software (Sensometrics Software) used for analysis of the ICP recordings.

If the inline PDF is not rendering correctly, you can download the PDF file here.

Article Information

INCLUDE WHEN CITING Published online February 26, 2016; DOI: 10.3171/2015.11.JNS151529.

Correspondence Per Kristian Eide, Department of Neurosurgery, Oslo University Hospital—Rikshospitalet, PB 4950 Nydalen, 0424 Oslo, Norway. email: peide@ous-hf.no.

© AANS, except where prohibited by US copyright law.

Headings

Figures

  • View in gallery

    A: The intracranial pressure-volume curve (elastance curve) describes the change in static pressure (dP) in response to a given intracranial volume change (dV), which depends on the intracranial volume load. The ICE (dP/dV) is increased when intracranial pressure-volume reserve capacity is reduced. The pressure-volume curve refers to the static pressure, i.e., mean ICP. Ventricular infusion increases the intracranial volume load and causes movement to the right on the pressure-volume curve. B: The present study examined the association between the ICE and the cardiac-induced pulsatile ICP, based on an assumption that pulsatile ICP changes with ICE. C: The hypothesis was that with increased ICE the single-wave amplitudes (A) and RTCs (= A/RT) increased, while the RT shortened. E = ICE.

  • View in gallery

    A: A ventricular infusion test is illustrated by trend plots of mean ICP and MWA, incorporating the period before infusion (Po) and the period during infusion (infusion rate 1.5 ml/min). The Pp occurs at the end of infusion. Three 6-second time windows of the continuous pressure signal from the period of opening pressure (B), infusion period (C), and end of plateau pressure (D) illustrate the change in ICP wave morphology.

  • View in gallery

    The association between ICE and MWA (A), RTC (B), RT (C), and mean ICP (D) was determined during the period of ventricular infusion. On each plot the fit line is presented and the Pearson correlation coefficient (R) and significance level (p value) are given.

  • View in gallery

    The association between ICE and Rout was determined during the period of ventricular infusion. The fit line is presented as well as the Pearson correlation coefficient (R) with significance level.

  • View in gallery

    Graphs showing the association between ICE and Evan's index (A), cella media index (B), third ventricle index (C), and ventricular score (D). For each plot the fit line is presented as well as the Pearson correlation coefficient and significance level.

  • View in gallery

    The ventricular infusion tests (n = 82) with ICC either < 0.5 ml/mm Hg (n = 36) or ≥ 0.5 ml/mm Hg (n = 46) were compared regarding MWA (A–C), RTC (D–F), and mean ICP (G–I) at opening pressure (A, D, and G), plateau pressure (B, E, and H) and infusion period (C, F, and I). Each error bar is presented as mean with 95% CIs. Differences between the 2 infusion test groups were determined by 1-way ANOVA.

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Eide PKKerty E: Static and pulsatile intracranial pressure in idiopathic intracranial hypertension. Clin Neurol Neurosurg 113:1231282011

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Eide PKSorteberg W: Association among intracranial compliance, intracranial pulse pressure amplitude and intracranial pressure in patients with intracranial bleeds. Neurol Res 29:7988022007

17

Eide PKSorteberg W: Diagnostic intracranial pressure monitoring and surgical management in idiopathic normal pressure hydrocephalus: a 6-year review of 214 patients. Neurosurgery 66:80912010

18

Eide PKSorteberg W: Simultaneous measurements of intracranial pressure parameters in the epidural space and in brain parenchyma in patients with hydrocephalus. J Neurosurg 113:131713252010

19

Fukuhara TLuciano MGBrant CLKlauscie J: Effects of ventriculoperitoneal shunt removal on cerebral oxygenation and brain compliance in chronic obstructive hydrocephalus. J Neurosurg 94:5735812001

20

González-Darder JMBarcia-Salorio JL: Pulse amplitude and volume-pressure relationships in experimental hydrocephalus. Acta Neurochir (Wien) 97:1661701989

21

Howells TLewén ASköld MKRonne-Engström EEnblad P: An evaluation of three measures of intracranial compliance in traumatic brain injury patients. Intensive Care Med 38:106110682012

22

Kasprowicz MCzosnyka ZCzosnyka MMomjian SJuniewicz HPickard JD: Slight elevation of baseline intracranial pressure after fluid infusion into CSF space in patients with hydrocephalus. Neurol Res 26:6286312004

23

Kiening KLSchoening WNLanksch WRUnterberg AW: Intracranial compliance as a bed-side monitoring technique in severely head-injured patients. Acta Neurochir Suppl 81:1771802002

24

Kim DJCzosnyka ZKasprowicz MSmieleweski PBaledent OGuerguerian AM: Continuous monitoring of the Monro-Kellie doctrine: is it possible?. J Neurotrauma 29:135413632012

25

Löfgren Jvon Essen CZwetnow NN: The pressure-volume curve of the cerebrospinal fluid space in dogs. Acta Neurol Scand 49:5575741973

26

Lundar T: Shunt removal or replacement based on intraventricular infusion tests. Childs Nerv Syst 10:3373391994

27

Lundar TNornes H: Determination of ventricular fluid outflow resistance in patients with ventriculomegaly. J Neurol Neurosurg Psychiatry 53:8968981990

28

Marmarou AShulman KLaMorgese J: Compartmental analysis of compliance and outflow resistance of the cerebrospinal fluid system. J Neurosurg 43:5235341975

29

Miller JDGaribi JPickard JD: Induced changes of cerebrospinal fluid volume. Effects during continuous monitoring of ventricular fluid pressure. Arch Neurol 28:2652691973

30

Munch TNBech-Azeddine RBoegeskov LGjerris FJuhler M: Evaluation of the lumbar and ventricular infusion test in the diagnostic strategy of pediatric hydrocephalus and the therapeutic implications. Childs Nerv Syst 23:67712007

31

Piper IRChan KHWhittle IRMiller JD: An experimental study of cerebrovascular resistance, pressure transmission, and craniospinal compliance. Neurosurgery 32:8058161993

32

Portella GCormio MCiterio GContant CKiening KEnblad P: Continuous cerebral compliance monitoring in severe head injury: its relationship with intracranial pressure and cerebral perfusion pressure. Acta Neurochir (Wien) 147:7077132005

33

Qvarlander SLundkvist BKoskinen LOMalm JEklund A: Pulsatility in CSF dynamics: pathophysiology of idiopathic normal pressure hydrocephalus. J Neurol Neurosurg Psychiatry 84:7357412013

34

Ringstad GEmblem KEEide PK: Phase-contrast magnetic resonance imaging reveals net retrograde aqueductal flow in idiopathic normal pressure hydrocephalus. J Neurosurg [epub ahead of print December 4 2015. DOI: 10.3171/20156.JNS15496]

35

Robertson CSNarayan RKContant CFGrossman RGGokaslan ZLPahwa R: Clinical experience with a continuous monitor of intracranial compliance. J Neurosurg 71:6736801989

36

Sæhle TEide PK: Association between ventricular volume measures and pulsatile and static intracranial pressure scores in non-communicating hydrocephalus. J Neurol Sci 350:33392015

37

Smielewski PLavinio ATimofeev IRadolovich DPerkes IPickard JD: ICM+, a flexible platform for investigations of cerebrospinal dynamics in clinical practice. Acta Neurochir Suppl 102:1451512008

38

Tisell MEdsbagge MStephensen HCzosnyka MWikkelsø C: Elastance correlates with outcome after endoscopic third ventriculostomy in adults with hydrocephalus caused by primary aqueductal stenosis. Neurosurgery 50:70772002

39

van Eijndhoven JHAvezaat CJ: Cerebrospinal fluid pulse pressure and the pulsatile variation in cerebral blood volume: an experimental study in dogs. Neurosurgery 19:5075221986

40

Wagshul MEEide PKMadsen JR: The pulsating brain: A review of experimental and clinical studies of intracranial pulsatility. Fluids Barriers CNS 8:52011

41

Wilkinson HASchuman NRuggiero J: Nonvolumetric methods of detecting impaired intracranial compliance or reactivity: pulse width and wave form analysis. J Neurosurg 50:7587671979

42

Yau YPiper IContant CCiterio GKiening KEnblad P: Multi-centre assessment of the Spiegelberg compliance monitor: interim results. Acta Neurochir Suppl 81:1671702002

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