Abstract
OBJECTIVES:
Transcranial Doppler (TCD) has been evaluated as a noninvasive intracranial pressure (ICP) assessment tool. Correction for insonation angle, a potential source of error, with transcranial color-coded sonography (TCCS) has not previously been reported while evaluating ICP with TCD. Our objective was to study the accuracy of TCCS for detection of ICP elevation, with and without the use of angle correction.
DESIGN:
Prospective study of diagnostic accuracy.
SETTING:
Academic neurocritical care unit.
PATIENTS:
Consecutive adults with invasive ICP monitors.
INTERVENTIONS:
Ultrasound assessment with TCCS.
MEASUREMENTS AND MAIN RESULTS:
End-diastolic velocity (EDV), time-averaged peak velocity (TAPV), and pulsatility index (PI) were measured in the bilateral middle cerebral arteries with and without angle correction. Concomitant mean arterial pressure (MAP) and ICP were recorded. Estimated cerebral perfusion pressure (CPP) was calculated as estimated CPP (CPPe) = MAP × (EDV/TAPV) + 14, and estimated ICP (ICPe) = MAP–CPPe. Sixty patients were enrolled and 55 underwent TCCS. Receiver operating characteristic curve analysis of ICPe for detection of invasive ICP greater than 22 mm Hg revealed area under the curve (AUC) 0.51 (0.37–0.64) without angle correction and 0.73 (0.58–0.84) with angle correction. The optimal threshold without angle correction was ICPe greater than 18 mm Hg with sensitivity 71% (29–96%) and specificity 28% (16–43%). With angle correction, the optimal threshold was ICPe greater than 21 mm Hg with sensitivity 100% (54–100%) and specificity 30% (17–46%). The AUC for PI was 0.61 (0.47–0.74) without angle correction and 0.70 (0.55–0.92) with angle correction.
CONCLUSIONS:
Angle correction improved the accuracy of TCCS for detection of elevated ICP. Sensitivity was high, as appropriate for a screening tool, but specificity remained low.
Keywords: acute brain injuries, intracranial pressure, optic nerve, transcranial Doppler ultrasonography, ultrasonography
KEY POINTS
Question: How accurate is transcranial Doppler (TCD) with angle-corrected measurements, compared with TCD without angle correction, as a screening tool for the detection of elevated intracranial pressure (ICP).
Findings: This was a prospective study of diagnostic accuracy comparing TCD to gold standard invasive ICP monitoring. The accuracy of TCD evaluation improved with angle correction (sensitivity 100%, specificity 30%).
Meaning: Sensitivity of angle-corrected TCD for detection of elevated ICP was high, as appropriate for a screening tool, but specificity remained low.
Intracranial pressure (ICP) elevation may result in death or devastating neurologic injury. Invasive ICP (ICPi) monitoring remains the gold standard; however, disadvantages include cost, the need for specialized expertise, and complications such as bleeding and infection. There is an unmet need for an inexpensive, widely available, noninvasive ICP assessment tool. Noninvasive ICPassessment may be particularly useful as a screening tool in limited-resource environments for the purposes of triage to higher levels of care and urgent initiation of therapy. In this role, the sensitivity of the noninvasive technique to exclude life-threatening intracranial hypertension is most important.
Several point-of-care ultrasound (POCUS) techniques of noninvasive ICP assessment have demonstrated promise (1–7). Transcranial Doppler (TCD) permits assessment of cerebral blood velocities (CBVs) within large intracranial arteries. Estimation of cerebral perfusion pressure (CPP) using CBV measurement was first described by Czosnyka et al (4). While some studies of this technique have demonstrated promising results (2–5, 7, 8), others have suggested suboptimal accuracy (9, 10). The angle of insonation while performing pulse Doppler evaluation is of critical importance for accurate measurement of velocity (11). Prior studies have demonstrated that “blind” TCD evaluation may result in a steep angle of insonation relative to direction of blood flow, leading to underestimation of CBV (11–15). Since the estimation of CPP with the Czosnyka technique is dependent on accurate estimation of CBV, correction for angle of insonation, which can be measured using transcranial color-coded sonography (TCCS), may improve accuracy. The Gosling pulsatility index (PI), a TCD/TCCS measure that may reflect distal resistance, has also been evaluated for the detection of raised ICP (1, 3, 6, 9, 16–20).
Our objective was to prospectively evaluate the accuracy of TCCS for the detection of with and without angle correction.
METHODS
Approval of the University of Michigan institutional review board was obtained for the study, titled “Noninvasive ocular assessment of ICP,” original date of approval June 21, 2015 (HUM00098976). All procedures were followed in accordance with the ethical standards of the responsible committee on human experimentation (institutional or regional) and with the Helsinki Declaration of 1975. This study was part of a Department of Defense funded, multimodal noninvasive ICP assessment study of ocular ultrasound, transocular bioimpedance, and TCD. We report here the results of the TCD component of this study. Adult patients (age ≥ 18 yr) admitted to the neurocritical care unit (NCCU) at the University of Michigan with an external ventricular drain (EVD) or intraparenchymal ICP monitor were eligible. The study period was January 2018 through November 2021, with enrollment suspended March through October 2020 as a result of the COVID-19 pandemic. Exclusion criteria included the presence of any ocular pathology other than errors of refraction, since all patients also underwent assessment with ocular ultrasound and transocular bioimpedance. Additionally, patients with suspected or confirmed cerebral vasospasm were excluded from the TCCS component of the study. Patients were eligible following craniotomy. Patients or legally authorized representatives provided written informed consent for participation. ICPi monitoring was typically performed for a Glasgow Coma Scale less than 9 following traumatic brain injury (TBI) or hydrocephalus in any disease state requiring an EVD. In addition, invasive monitoring was used in any patient with acute brain injury where the physician was concerned about elevated ICP based on evaluation of the complete clinical picture.
The monitor was turned away from the operator for the duration of the ultrasound examination. The mean arterial pressure (MAP) measured from an intra-arterial catheter and simultaneous ICP measured from an EVD or intraparenchymal monitor were recorded by an assistant when the pulse Doppler signal was frozen for measurement of velocities.
All TCCS studies were performed with one of two POCUS machines—a General Electric (GE) Venue (GE HealthCare, Chicago, IL) with a 3Sc 1.1–4.7 MHz phased array transducer or a SonoSite M-Turbo (SonoSite, Bothell, WA) with a P21 5-1 MHz transducer. All studies were performed with a TCCS preset by an operator with greater than 10 years’ TCCS experience. The operator was required to indicate the adequacy of the temporal acoustic window on either side, along with prespecified minimal technical requirements for an adequate TCCS examination. These requirements consisted of the ability to visualize clearly on duplex imaging each of the following on at least one side: intracranial internal carotid artery, the carotid bifurcation with the origins of both the anterior cerebral artery and middle cerebral artery (MCA), minimum 1 cm length of MCA M1 segment that was approximately linear in 2D configuration to allow determination of direction of flow, and bifurcation of the MCA. Measurements were first obtained without angle correction. Using duplex imaging and pulse wave Doppler, a 3 mm sample volume was placed in the middle of the M1 segment. The operator visually approximated an angle of insonation less than 30° and did not measure a velocity if a “visually estimated” angle of insonation less than 30° could not be obtained. The operator attempted to achieve an angle less than 30° through adjustments in probe position within the available acoustic window, and placement of the sample volume on a target vessel location that allowed for the smallest insonation angle. However, the angle of insonation was not objectively measured at this time and could have exceeded 30°. The time-averaged peak velocity (TAPV), end-diastolic velocity (EDV), peak systolic velocity (PSV), and PI = (PSV–EDV/TAPV) were recorded at this location (Fig. 1A). Without moving the transducer, the angle of insonation at the same location of the MCA-M1 was then measured using the linear direction-of-flow indicator, and angle-corrected velocities measured using the software provided with the transcranial preset (Fig. 1B). The average of velocities on both sides was used to estimate CPP and average PI of both sides used in the analysis. The estimated CPP (CPPe), with and without angle correction, was calculated using the Czosnyka formula as: CPPe = MAP × (EDV/TAPV) + 14. The corresponding estimated ICP (ICPe) was calculated as MAP–CPPe. The average CPPe and ICPe of the two sides were the index measurements in the analysis of diagnostic accuracy, while the average invasive CPP (CPPi) and ICP of the two sides were the corresponding reference standard measurements. Patients with subarachnoid hemorrhage (SAH) underwent TCCS within 72 hours of ictus to minimize the risk of vasospasm.
Figure 1.
Transcranial color-coded sonography velocity measurement in the middle cerebral artery (MCA) M1 segment of a 33-yr-old man with severe traumatic brain injury. A, Without angle correction. Invasive intracranial pressure (ICP) measurement at this time is 24 mm Hg. Estimated ICP (ICPe) is 19 mm Hg. B, With angle correction (angle of insonation 26°). Invasive ICP is 24 mm Hg. ICPe is 25 mm Hg. DVD = digital video disc, EDV = end-diastolic velocity, MAP = mean arterial pressure, MI = Mechanical Index, PI = pulsatility index, PSV = peak systolic velocity, PW = pulsed wave, RI = Resistive Index, S/D = systolic/diastolic ratio, TAP = time averaged peak, TIC = thermal index cranial bone, TCD = transcranial Doppler, TT = transtemporal.
Descriptive statistics included proportion/percentage for categorical variables and median with interquartile range (IQR) for continuous variables. Differences in categorical variables between two discrete groups were tested for statistical significance with a chi-square test or Fisher exact test as appropriate. Differences in continuous variables between two discrete groups were tested for statistical significance with the Mann-Whitney U test. A Bland-Altman plot was constructed with the gold standard—CPPi or ICPi on the x-axis and difference between CPPi and CPPe or ICPi and ICPe (calculated with and without angle correction) on the y-axis. The mean difference and limits of agreement (LOA) between the two methods of measurement were calculated with a 95% CI. Receiver operating characteristic (ROC) curve analysis was performed to assess the accuracy of ICPe and PI between the two sides for the detection of ICPi greater than 22 mm Hg, a threshold extrapolated from the guidelines for management of severe TBI (21). The area under the curve (AUC) was calculated. An optimal threshold was selected with a minimum sensitivity greater than 90%, as appropriate for a screening test for potentially life-threatening ICP elevation. Sensitivity, specificity, positive predictive value (PPV), and negative predictive value (NPV) were calculated. The threshold for statistical significance was p value of less than 0.05. All statistical analyses were performed with MedCalc Statistical Software Version 20.218 (MedCalc Software, Ostend, Belgium; https://www.medcalc.org; 2023).
RESULTS
A total of 60 patients were enrolled, of these 55 underwent TCCS. Two patients with SAH (both enrolled > 72 hr from ictus) were excluded from TCCS for suspected vasospasm. A further three of 58 patients (5%) had insufficient temporal acoustic windows to permit visualization of all required elements of the intracranial vasculature on at least one side. Baseline variables of patients at the time of ultrasound examination are in Table 1. Ultrasound measurements in patients with and without ICP elevation at the time of examination are in Supplementary Table 1 (http://links.lww.com/CCX/B232), while TCCS measurements with and without angle correction are in Supplementary Table 2 (http://links.lww.com/CCX/B232). The median objectively measured angle of insonation at the time of angle correction was 22.5° (IQR, 14–32°) on the left and 28° (14–34°) on the right. Despite a subjective estimation of angle less than 30° by the operator in all patients, 25% of insonation angles on the left and 33% of insonation angles on the right were found to be greater than 30° when angle correction was performed.
TABLE 1.
Distribution of Variables at the Time of Ultrasound Evaluation
| Variable | All Patients (n = 63) | Patients Without ICP > 22 mm Hg During the Ultrasound Examination (n = 47) | Patients With ICP > 22 mm Hg During the Ultrasound Examination (n = 7) | p |
|---|---|---|---|---|
| Age, yr, median (IQR) | 54 (40–62) | 52 (39–61) | 54 (50–63) | 0.47 |
| Sex, female, n (%) | 32 (51) | 21 (45) | 5 (71) | 0.24 |
| Diagnosis, n (%) | 0.4 | |||
| Subarachnoid hemorrhage | 30 (48) | 24 (51) | 3 (43) | |
| Brain tumor | 12 (19) | 9 (19) | 2 (29) | |
| Traumatic brain injury | 9 (14) | 4 (9) | 2 (29) | |
| Intracerebral hemorrhage | 9 (14) | 7 (15) | 0 (0) | |
| Ventriculoperitoneal shunt | 3 (5) | 3 (6) | 0 (0) | |
| ICP (invasive), mm Hg, median (IQR) | 11 (7–17) | 10 (6–14) | 28 (24–35) | < 0.0001 |
| Cerebral perfusion pressure, mm Hg, median (IQR) | 83 (75–99) | 85 (75–102) | 66 (61–72) | 0.001 |
| Mean arterial pressure, mm Hg, median (IQR) | 99 (88–110) | 99 (88–110) | 97 (92–106) | 0.97 |
ICP = intracranial pressure, IQR = interquartile range.
Comparison of Invasive and CPPe and ICP
Multiple dot plots of CPPi/ICPi and CPPe/ICPe values, with and without angle correction are in Figure 2. Overall, ICPe values were higher than gold standard invasive measurements, while CPPe values were lower than the corresponding invasive measurements. The Bland-Altman plots of the CPPi–CPPe/ICPi–ICPe difference versus CPPi/ICPi without and with angle correction are in Figure 3, and again suggest that CPPe values were generally lower and ICPe values generally higher than the corresponding invasive values. Without angle correction, the mean CPPi–CPPe difference was 11.83 mm Hg (95% CI, 7.73–15.94 mm Hg) with lower LOA –17.93 mm Hg (–24.99 to –10.87 mm Hg) and upper LOA 41.60 mm Hg (34.54–48.66 mm Hg). With angle correction, the mean CPPi–CPPe difference was 12.46 mm Hg (8.71–16.21 mm Hg) with lower LOA –13.42 mm Hg (–19.88 to –6.97 mm Hg) and upper LOA 38.34 mm Hg (31.89–44.80 mm Hg). The mean ICPi–ICPe difference without angle correction was –12.49 mm Hg (–16.40 to –8.57 mm Hg) with lower LOA –40.87 mm Hg (–47.59 to –34.14 mm Hg) and upper LOA 15.89 mm Hg (9.16–22.62 mm Hg). The mean ICPi–ICPe difference with angle correction was –13.11 mm Hg (–16.54 to –9.68 mm Hg) with lower LOA –36.77 mm Hg (–42.68 to –30.87 mm Hg) and upper LOA 10.55 mm Hg (4.65–16.46 mm Hg).
Figure 2.
Multiple dot plot of invasive cerebral perfusion pressure (CPPinvasive) versus estimated CPP (CPPe). Without angle correction (CPPe) (A) and with angle correction (CPPe_AC) (B); invasive intracranial pressure (ICPinvasive) versus estimated ICP (ICPe) (ICP transcranial Doppler [ICPtcd]). Without angle correction (ICPtcd) (C) and with angle correction (ICPtcd_AC) (D).
Figure 3.
Bland Altman plots: CPPe and CPPinvasive. Bland-Altman plots of: invasive cerebral perfusion pressure (CPPinvasive)–estimated CPP (CPPe) on the y-axis versus the gold standard (CPPinvasive) on the x-axis without angle correction (A) and with angle correction (B); invasive intracranial pressure (ICPinvasive)–estimated ICP (ICPe) on the y-axis versus the gold standard (ICPinvasive) on the x-axis without angle correction (C) and with angle correction (D). CPPe_AC = CPPe with angle correction, ICPtcd = ICP transcranial Doppler, ICPtcd_AC = ICP transcranial Doppler with angle correction.
Accuracy for Detection of Elevated ICP
ROC analysis of ICPe for detection of elevated ICP (ICPi > 22 mm Hg) revealed AUC 0.51 (0.37–0.64) without angle correction, this improved to 0.73 (0.58–0.84) with angle correction. The optimal threshold without angle correction was ICPe greater than 18 mm Hg with sensitivity 71% (29–96%), specificity 28% (16–43%), PPV 13% (8–20%), and NPV 87% (65–96%). With angle correction, the optimal threshold was ICPe greater than 21 mm Hg with clinically meaningful improvements in accuracy—sensitivity 100% (54–100%), specificity 30% (17–46%), PPV 17% (14–20%), and NPV 100% (65–100%). ROC analysis of the PI for the detection of elevated ICP revealed AUC 0.61 (0.47–0.74) without angle correction, this improved to 0.70 (0.55–0.92) with angle correction. ROC curves of ICPe and PI with and without angle correction for the detection of elevated ICP are in Figure 4. Of note, these thresholds were selected to maximize sensitivity (> 90%), while achieving the greatest corresponding specificity. The accuracy of various other ICPe and PI thresholds for the detection of elevated ICP is in Table 2. An ICPe threshold of greater than 35 mm Hg with angle correction, for example, achieved a specificity of 91% and sensitivity of 33%.
Figure 4.
Receiver operating characteristic curves of the following measurements for the detection of invasive intracranial pressure (ICP) greater than 22 mm Hg. A, Estimated ICP (ICPe) without angle correction; B, ICPe with angle correction; C, pulsatility index (PI) without angle correction; and D, PI with angle correction. p values are for the null-hypothesis that area under the curve (AUC) = 0.5.
TABLE 2.
Accuracy of Estimated Intracranial Pressure and Pulsatility Index Thresholds to Detect Invasive Intracranial Pressure Greater Than 22 mm Hg
| Measurement | Threshold | Sensitivity (95% CI) | Specificity (95% CI) | Positive Predictive Value (95% CI) | Negative Predictive Value (95% CI) |
|---|---|---|---|---|---|
| Estimated intracranial pressure with angle correction | > 21 mm Hg | 100% (54–100%) | 30% (17–46%) | 17% (14–20%) | 100% (65–100%) |
| > 32 mm Hg (maximum Youden’s J) | 67% (22–96%) | 84% (69–93%) | 36% (19–58%) | 95% (85–98%) | |
| > 35 mm Hg | 33% (4–78%) | 91% (78–97%) | 33% (10–68%) | 91% (85–95%) | |
| Pulsatility index with angle correction | > 0.82 | 100% (54–100%) | 30% (17–45%) | 16% (14–19%) | 100% (65–100%) |
| > 1.09 (maximum Youden’s J) | 83% (36–100%) | 61% (46–76%) | 23% (15–33%) | 96% (82–99%) | |
| > 1.30 | 33% (4–78%) | 82% (67–92%) | 20% (6–48%) | 90% (83–94%) | |
| > 1.45 | 17% (0–64%) | 91% (78–98%) | 20% (3–65%) | 89% (85–92%) |
Diagnostic thresholds for estimated intracranial pressure (ICP) and pulsatility index for the detection of invasive ICP > 22 mm Hg.
DISCUSSION
In this prospective study of diagnostic accuracy, the use of angle correction with TCCS improved the accuracy of ICP assessment. As appropriate for a screening test, sensitivity was high; however, specificity remained poor. Our findings are significant for several reasons. Most important, they emphasize the importance of gold standard invasive monitoring where indicated and available. Research into more advanced and innovative noninvasive tools is necessary. This is especially significant since earlier studies of these ultrasound techniques suggested high accuracy, leading to adoption in clinical practice at several centers, including our own, often as components of noninvasive monitoring protocols (22, 23). While TCCS may have a role in the multimodal bedside assessment of ICP and adequacy of brain perfusion when invasive monitoring cannot be used, it should not be used as the sole criterion for clinical decision-making. As part of a multimodality noninvasive assessment, TCCS may have a role in decisions on triage and urgent initiation of therapy in patient with severe brain injury in resource-limited settings, where invasive monitoring is often unavailable. Patients with acute liver failure, who are at risk for elevated ICP and bleeding with invasive intracranial procedures, may also benefit from noninvasive assessment (22). Low values of ICPe (< 22 mm Hg) and the PI (< 0.82), which demonstrate high NPV, in conjunction with other tools such as brain imaging and pupillometry, may help identify patients at lower risk for imminent deterioration from elevated ICP. While intermediate values are least useful, even values at the extreme should be corroborated with these other clinical data points, given the wide CIs in our study (Table 2). Consistent with prior studies, CPPe underestimated CPP while ICPe over-estimated ICP (Figs. 2 and 3) (2, 7). The multipurpose POCUS machines used in our study are widely available in ICUs and emergency departments (EDs) worldwide and can be used for rapid cardiopulmonary assessment in conjunction with neurologic assessment. TCCS requires specialized training but has been in widespread clinical use for several decades.
Our finding that measurement of angle-corrected velocities improves the accuracy of TCCS is consistent with prior data that demonstrates underestimation of CBVs when “blind” TCD is used, likely a result of excessively steep angles of insonation (11–15). Our study likely underestimates the error in velocities with “blind” (spectral Doppler only) TCD, since velocity measurements without angle correction in our study were nevertheless performed with TCCS and visual approximation of an insonation angle less than 30°. While this approach is common in clinical practice, our study demonstrates that meaningful variations in measured velocities may yet occur. Angle correction is not routinely used for some common applications of TCCS in the NCCU—such as screening for large-vessel cerebral vasospasm in SAH patients—since there is limited data on angle-corrected velocity thresholds (12, 15, 24), and clinical management if often driven by trends in velocities rather than point-in-time assessments. However, even moderate errors in measured velocities as a result of insonation angle can significantly alter the numeric value of a point-in-time assessment of ICP, which in this context serves as the basis for triage and initiation (or withholding) of therapeutic measures. The clinically meaningful improvement in accuracy observed with incorporation of angle correction in our study—an increase in AUC from 0.51 to 0.73, and sensitivity from 71% to 100%, with equivalent or better specificity—emphasizes the importance of measuring velocities that most closely approximate physiologic values, in this context.
Our results are comparable to the accuracy of the same technique reported in a recent multicenter study (8), where an AUC of 0.76 was achieved. The overall moderate accuracy of the CPPe technique in our study is consistent with other recent studies as well (9, 10), but varies from the results of earlier studies that demonstrated higher accuracy (4, 5, 7, 20). This may be similar to other POCUS techniques such as the measurement of inferior vena cava diameter to assess fluid responsiveness, where initial studies suggested greater accuracy than subsequent investigations (25). While the reasons for such variation are less clear, they may be related to sample size, study population, technique, and blinding of sonographers to the gold standard. While the PI is a relatively nonspecific measure, our study suggests that a low PI may have some value, as a component of multimodal assessment, in identifying patients unlikely to have life-threatening ICP elevation. This is consistent with the findings of some studies (1, 3, 6, 17–20), but not all (9, 16). While the PI achieved slightly lower accuracy than angle-corrected ICPe estimation in our study, it can be measured more easily and quickly.
Our study has several limitations. The sample size was relatively small, and the population studied relatively heterogeneous. While a homogenous population may be better suited to demonstrate proof of concept, our goal was to assess the generalizability of this technique across a variety of conditions in which life threatening ICP elevation can occur. POCUS machines—rather than full-function machines—were deliberately selected as they are widely available in ICUs and EDs, and familiar to practitioners in these settings. Our findings support our clinical experience, demonstrating a high success rate for good-quality TCCS studies with these machines. Only 5% of patients had an insufficient acoustic window, comparable to results with dedicated TCD machines. We performed point-in-time assessments of MAP and ICP, whereas these are dynamic measurements prone to physiologic variability, signal quality control, and drifts in zero pressure reference level for ICP. We did not study variations with repeat measurements of TCD velocities by the same operator. We did not study other techniques of ICP assessment with TCD. The Czosnyka formula was selected as being the most widely studied, and feasible without specialized software or equipment. TCCS studies were performed by an experienced operator and our findings may not be reproducible with inexperienced sonographers or those without dedicated training in TCD/TCCS.
In conclusion, angle correction improved the accuracy of TCCS for the detection of elevated ICP. Sensitivity was high, as appropriate for a screening tool, but specificity remained low.
Supplementary Material
Footnotes
Supported, in part, from Department of Defense grant W81XWH-16-DMRDP-CCCRP-PFCRA
The authors have disclosed that they do not have any potential conflicts of interest.
Supplemental digital content is available for this article. Direct URL citations appear in the printed text and are provided in the HTML and PDF versions of this article on the journal’s website (http://journals.lww.com/ccejournal).
REFERENCES
- 1.Bellner J, Romner B, Reinstrup P, et al. : Transcranial Doppler sonography pulsatility index (PI) reflects intracranial pressure (ICP). Surg Neurol 2004; 62:45–51; discussion 51 [DOI] [PubMed] [Google Scholar]
- 2.Cardim D, Robba C, Bohdanowicz M, et al. : Non-invasive monitoring of intracranial pressure using transcranial Doppler ultrasonography: Is it possible? Neurocrit Care 2016; 25:473–491 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 3.Cardim D, Robba C, Donnelly J, et al. : Prospective study on noninvasive assessment of intracranial pressure in traumatic brain-injured patients: Comparison of four methods. J Neurotrauma 2016; 33:792–802 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 4.Czosnyka M, Matta BF, Smielewski P, et al. : Cerebral perfusion pressure in head-injured patients: A noninvasive assessment using transcranial Doppler ultrasonography. J Neurosurg 1998; 88:802–808 [DOI] [PubMed] [Google Scholar]
- 5.Schmidt EA, Czosnyka M, Matta BF, et al. : Non-invasive cerebral perfusion pressure (nCPP): Evaluation of the monitoring methodology in head injured patients. Acta Neurochir Suppl 2000; 76:451–452 [DOI] [PubMed] [Google Scholar]
- 6.Zweifel C, Czosnyka M, Carrera E, et al. : Reliability of the blood flow velocity pulsatility index for assessment of intracranial and cerebral perfusion pressures in head-injured patients. Neurosurgery 2012; 71:853–861 [DOI] [PubMed] [Google Scholar]
- 7.Rasulo FA, Bertuetti R, Robba C, et al. : The accuracy of transcranial Doppler in excluding intracranial hypertension following acute brain injury: A multicenter prospective pilot study. Crit Care 2017; 21:44. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 8.Rasulo FA, Calza S, Robba C, et al. : Transcranial Doppler as a screening test to exclude intracranial hypertension in brain-injured patients: The IMPRESSIT-2 prospective multicenter international study. Crit Care 2022; 26:110. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 9.Robba C, Cardim D, Tajsic T, et al. : Ultrasound non-invasive measurement of intracranial pressure in neurointensive care: A prospective observational study. PLoS Med 2017; 14:e1002356. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 10.Cardim D, Robba C, Czosnyka M, et al. : Noninvasive intracranial pressure estimation with transcranial Doppler: A prospective observational study. J Neurosurg Anesthesiol 2020; 32:349–353 [DOI] [PubMed] [Google Scholar]
- 11.Eicke BM, Tegeler CH, Dalley G, et al. : Angle correction in transcranial Doppler sonography. J Neuroimaging 1994; 4:29–33 [DOI] [PubMed] [Google Scholar]
- 12.Krejza J, Kochanowicz J, Mariak Z, et al. : Middle cerebral artery spasm after subarachnoid hemorrhage: Detection with transcranial color-coded duplex US. Radiology 2005; 236:621–629 [DOI] [PubMed] [Google Scholar]
- 13.Krejza J, Mariak Z, Babikian VL: Importance of angle correction in the measurement of blood flow velocity with transcranial Doppler sonography. AJNR Am J Neuroradiol 2001; 22:1743–1747 [PMC free article] [PubMed] [Google Scholar]
- 14.Lepic T, Veljancic D, Jovanikic O, et al. : Importance of angle correction in transcranial color-coded duplex insonation of arteries at the base of the brain. Vojnosanit Pregl 2015; 72:1093–1097 [DOI] [PubMed] [Google Scholar]
- 15.Swiat M, Weigele J, Hurst RW, et al. : Middle cerebral artery vasospasm: Transcranial color-coded duplex sonography versus conventional nonimaging transcranial Doppler sonography. Crit Care Med 2009; 37:963–968 [DOI] [PubMed] [Google Scholar]
- 16.Behrens A, Lenfeldt N, Ambarki K, et al. : Transcranial Doppler pulsatility index: Not an accurate method to assess intracranial pressure. Neurosurgery 2010; 66:1050–1057 [DOI] [PubMed] [Google Scholar]
- 17.Gura M, Elmaci I, Sari R, et al. : Correlation of pulsatility index with intracranial pressure in traumatic brain injury. Turk Neurosurg 2011; 21:210–215 [DOI] [PubMed] [Google Scholar]
- 18.Kaloria N, Panda NB, Bhagat H, et al. : Pulsatility index reflects intracranial pressure better than resistive index in patients with clinical features of intracranial hypertension. J Neurosci Rural Pract 2020; 11:144–150 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 19.O’Brien NF, Maa T, Reuter-Rice K: Noninvasive screening for intracranial hypertension in children with acute, severe traumatic brain injury. J Neurosurg Pediatr 2015; 16:420–425 [DOI] [PubMed] [Google Scholar]
- 20.Robba C, Pozzebon S, Moro B, et al. : Multimodal non-invasive assessment of intracranial hypertension: An observational study. Crit Care 2020; 24:379. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 21.Carney N, Totten AM, O’Reilly C, et al. : Guidelines for the management of severe traumatic brain injury, fourth edition. Neurosurgery 2017; 80:6–15 [DOI] [PubMed] [Google Scholar]
- 22.Rajajee V, Williamson CA, Fontana RJ, et al. : Noninvasive intracranial pressure assessment in acute liver failure. Neurocrit Care 2018; 29:280–290 [DOI] [PubMed] [Google Scholar]
- 23.Sheehan JR, Liu X, Donnelly J, et al. : Clinical application of non-invasive intracranial pressure measurements. Br J Anaesth 2018; 121:500–501 [DOI] [PubMed] [Google Scholar]
- 24.Mariak Z, Krejza J, Swiercz M, et al. : Accuracy of transcranial color Doppler ultrasonography in the diagnosis of middle cerebral artery spasm determined by receiver operating characteristic analysis. J Neurosurg 2002; 96:323–330 [DOI] [PubMed] [Google Scholar]
- 25.Orso D, Paoli I, Piani T, et al. : Accuracy of ultrasonographic measurements of inferior vena cava to determine fluid responsiveness: A systematic review and meta-analysis. J Intensive Care Med 2018; 35:354–363 [DOI] [PubMed] [Google Scholar]
Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.