A method of recording multimodality monitoring signals in patients with severe brain injuries using a bedside, single burr hole technique is described.
Intracranial pressure (ICP) monitoring is a cornerstone of the intensive care management of patients with severe acute brain injuries, including traumatic brain injury. While elevations in ICP are common, data regarding the measurement and treatment of these ICP elevations are conflicting. There is increasing recognition that changes in the balance between supply and demand of brain tissue are critically important and therefore the measurement of multiple modalities is required. Approaches are not standard, and therefore this article provides a description of a bedside, single burr hole approach to multimodality monitoring that allows the passage of probes designed to measure not only ICP but brain tissue oxygen, blood flow, and intracranial electroencephalography. Patient selection criteria, operative procedures, and practical considerations for securing probes during critical care are described. This method is readily performed, safe, secure, and flexible for the adoption of a variety of multimodality monitoring approaches aimed at detecting or preventing secondary brain injuries.
Severe brain injuries such as traumatic brain injury (TBI) or subarachnoid hemorrhage may result in coma, a clinical state in which patients do not respond to their environment. Neurosurgeons and neurointensivists rely heavily on the clinical neurological exam, but severe brain injuries may make it impossible to detect changes related to the brain's physiologic environment: elevations in intracranial pressure (ICP), decreases in cerebral blood flow, or nonconvulsive seizures and spreading depolarizations. These physiologic disturbances can lead to further injury, termed secondary brain injury.
After severe traumatic brain injury, elevations in ICP are common and may result in decreased blood flow and therefore secondary brain injury and neurodeterioration. Elevations in ICP have been documented in up to 89% of patients1 and neurodeterioration occurs in one-quarter, increasing mortality from 9.6% to 56.4%2. Therefore, the measurement of ICP is the most commonly used biomarker for the development of secondary brain injury and has a Level IIb recommendation from the Brain Trauma Foundation3.
The measurement of ICP was pioneered over 50 years ago4 using catheters that were introduced through a twist drill craniostomy (often referred to interchangeably as a burr hole) typically created in the frontal bone at the mid-pupillary line just anterior to the coronal suture and passed into the ventricles. However, these external ventricular drainage catheters (EVDs) require midline anatomy, which is not always present after severe brain injuries, and misplacement can potentially damage deep structures such as the thalamus. Although EVDs allow drainage of CSF as a potential treatment option, the hemorrhage rates from EVDs are 6–7% on average5,6.
Intraparenchymal pressure monitors are introduced via burr hole and are common alternatives and adjuncts to EVDs with hemorrhage rates of 3–5%7,8. These are smaller probes that sit 2–3 cm under the inner table of the skull, and allow for continuous measurement of pressure but without an option to drain cerebrospinal fluid, as do EVDs. Existing cohort studies9 and meta-analyses10,11 suggest that targeting ICP as a marker of secondary brain injury may improve survival; however, a randomized controlled trial comparing treatment of ICP based on neurological exam alone vs. measured ICP failed to demonstrate benefit12.
Advances in neurosurgery and neurointensive care have led to an understanding that brain physiology is more complicated than ICP alone. It has been demonstrated that autoregulatory function within the brain is impaired after brain injury13, leading to changes in the regulation of regional cerebral blood flow (rCBF). Further, the burden of nonconvulsive seizures14 and spreading depolarizations15 are being recognized using recordings from intracranial electroencephalography (iEEG) electrodes. Strategies to improve brain tissue oxygen (PbtO2) were shown to be a target for therapy and proved feasible in a large, multicenter Phase II clinical trial16.
This article describes a technique that allows for the simultaneous measurement of multiple modalities — including ICP, PbtO2, rCBF, and iEEG — using a simple, single burr hole placed at the bedside in patients with severe acute brain injuries requiring intensive care. Patient selection and surgical approach to this technique are included. This technique specifically allows for the placement of multiple probes to provide targeted monitoring of multiple physiologic parameters that may provide a more sensitive and specific early warning system for secondary brain injuries.
This protocol was developed as a standard of care. The retrospective use of data gathered during the course of care was approved through a waiver of informed consent by the University of Cincinnati’s Institutional Review Board.
1. Patient Selection
2. Preparation of Site and Skin
3. Preparation of Equipment
4. Drilling a Burr Hole
5. Inserting the Cranial Bolt
6. Securing the Probes
7. Verifying Probe Data
8. Patient Care
NOTE: Following the procedure, no further pain control is necessary and no prophylactic antibiotics are required.
Experience in using this approach in 43 patients with severe TBI was recently published17. Patient selection limits the number of those eligible, but focusing on only those with TBI at a level I trauma center led to approximately 2 patients per month. This number is predicated on hospital volume and may increase if additional acute brain injuries are considered for monitoring, such as those with hemorrhagic stroke.
Placement may take place either in patients with non-surgical severe injuries or in those who have undergone surgery, depending on the preferences at an individual institution (Figure 1). This technique has been performed within a median of 12.5 h (interquartile range [IQR] 9.0–21.4 h) of injury and probes have been left in situ for a median of 97.1 h (IQR 46.9–124.6 h)17. Placement is typically within the non-dominant frontal lobe unless there is a contraindication. Three-quarters of bolts placed in dominant frontal lobe were placed contralateral to prior craniectomy. Nonetheless, in TBI, this strategy led to placement within an injured lobe the majority of the time. Misplacement was rare using this technique, occurring in only 6/42 (14.3%) of patients; device measurements were rarely affected17.
Bedside placement resulted in no adverse events at the time of bolt insertion. On follow up CT, small regions of peri-probe hematoma, pneumocephalus, or bone chips were found in 40.5% of patients17. However, mirroring the experience of other institutions18 that perform similar monitoring, only one expanding hematoma was considered to be a major hemorrhage. In this case, no surgical or medical intervention was recommended, and the patient outcome was felt not to be impacted. Across two cohorts including patients with TBI and subarachnoid hemorrhage, the overall rate of significant hemorrhage is 1.9%17,18.
Once devices are in place, device dislodgement may occur and has been described as being related to the size of the probes, length of time they remain in situ, and relative complexity of moving, transferring, and caring for this patient population. More than half of patients experienced dislodgement of at least one probe before the end of their recording period, mostly commonly the rCBF probe. Limiting transportation may mitigate this risk: the number of trips that patients took appeared to be associated with devices becoming dislodged or no longer functioning (Wilcoxon rank sum test, p = 0.03)17. Nonetheless, this technique has resulted in measurements of all modalities in more than 90% of placements and most probes remain in place and generate continuous data for >90% of the recording period.
Figure 1: Clinical and radiologic placement of multimodality monitoring probes. (A) Appearance of bolt with three probes, as labelled prior to securing the probes or wrapping for transport. (B) Scout CT images (coronal and sagittal, respectively) demonstrating the trajectory of the probes approximately 1.5 cm (Depth) and 2-3 cm (ICP/PbtO2, rCBF) below the inner table of the skull. (C) Axial CT after non-surgical severe TBI with excellent placement. Notice with standard windowing that the relatively dense probes may obscure subtle peri-probe hematoma. (D) Axial CT after surgical severe TBI demonstrating the placement of the bolt and probes contralateral to the hemicraniectomy site. (E) Incorrect (deep) placement of the probes after non-surgical severe TBI. Note that the probes are approaching the frontal horn of the lateral ventricle, indicating they are >3 cm below the inner table of the skull. This placement may affect measurements obtained by the probes, although shallow, rather than deep, placement is more liable to create problems with rCBF and PbtO2 measurements. Please click here to view a larger version of this figure.
Equipment | Measurement | Method of Measurement | Sampling Resolution |
Quad lumen bolt kit | NA | NA | NA |
ICP/PbtO2 probe | ICP | Mini-strain gauge | 125 Hz |
PbtO2 | Fiberoptic | 125 Hz | |
ICT | Thermistor | NA | |
rCBF probe | rCBF | Distal thermistor | 1 Hz |
ICT | Proximal thermistor | 1 Hz | |
K | Distal thermistor | per recalibration | |
Depth electrode | EEG | Platinum electrodes | ≥256 Hz |
70 Microdialysis bolt catheter | Lactate, pyruvate, glucose, glycerol, and glutamate | Enzymatic measurement of interstitial fluid | Hourly |
Table 1: Intracranial probes. The names of the probes used in this article and their measurements and sampling resolution. Please note that this is a representative list of probes that may be used for multimodality monitoring but does not represent an exhaustive list of the potential modalities that may be commercially available. EEG = electroencephalography; ICP = intracranial pressure; ICT = intracranial temperature; PbtO2 = brain tissue oxygen; rCBF = regional cerebral blood flow.
This article provides the practical elements of a method for introducing multiple probes into the brain follow acute brain injury in order to facilitate a multimodal approach to understanding the physiology underlying secondary brain injury. The existing Brain Trauma Foundation guidelines suggest the use of intracranial pressure monitoring in specific patients after trauma (Level IIb)3, although there is evidence to suggest that this is variably practiced even at high-volume level I trauma centers19,20. This may be in part due to the differences between techniques (ventricular drainage vs. parenchymal probes), anatomy (the presence of midline shift or slit-like ventricles), and practitioner preference. In any case, evidence is mounting that the measurement of ICP alone may be inadequate for the detection and mitigation of secondary brain injuries.
The insertion of multiple probes through a bolt provides a reliable way to monitor patients for the length of time required for critical care, and while dislodgement or discontinuation occurred frequently, this was in part related to patient transportation. After initial experience, additional safeguards included in the current protocol were implemented, such as strain relief measures. By way of contrast, tunneled probes may be more susceptible to traction and dislodgement because the length of the probes does not allow for the subgaleal fixation used to keep EVDs in situ. Some have argued that tunneled probes may be beneficial and can be adequately secured in order to avoid magnetic resonance imaging (MRI) incompatibility and artifacts, but many probes are not MRI compatible regardless of fixation21. Importantly, the use of multimodality monitoring is designed to provide time-resolute data during the acute period in which many patients are unstable to travel to MRI. Patients described here underwent monitoring within a median of 12.5 h and were monitored for a median of 4 days after trauma, which allowed for advanced imaging within a reasonable time frame.
The use of a single cranial access point reduces procedural risk, and strict patient entry criteria limits the potential for medication- or coagulopathy-related complications. The rates of minor hemorrhage reported here were in line with the documented incidence of peri-probe hemorrhages in the EVD literature22,23, although these are not uniformly reported. The rates of significant hemorrhage using the method described here are lower than those reported in the EVD literature and only slightly higher than the rates of significant hemorrhage associated with single intraparenchymal monitors. In addition to a relatively low overall operative risk, the use of a single, standardized burr hole is a bedside procedure, which allows this technique to be carried out in critically ill patients too unstable to move to an operative suite and by practitioners with bedside procedural privileges, such as neurosurgery house staff or neurointensivists.
There are several limitations that arise using a single burr hole placed at Kocher's point for neuromonitoring. First, the size of the burr hole and the use of a bolt preclude the placement of additional monitors, such as strip electrodes used as the gold standard for the detection of spreading depolarizations according to recommendation from the co-operative studies on brain injury depolarizations (COSBID) collaborative24. Second, the spatial resolution of intraparenchymal monitoring may not be adequate to detect the signatures of secondary brain injury that occur remote from the probes. While the majority of the time monitors were placed near injured cortex, this approach is limited to frontal lobe monitoring, which may miss lesion development or evolution, for instance, in temporal or parietal cortex. Although this approach does not provide a global assessment of brain tissue, the ability to continuously monitor a vulnerable brain region provides the advantage of real-time patient care decision making.
The method presented here is flexible in allowing for multiple probes based on the equipment available to local sites. For instance, probes that measure microdialysis may be added to the fourth port available via the bolt without substantially modifying the existing protocol. Similarly, probes may be excluded if necessary.
In conclusion, a technique for multimodal monitoring after acute brain injury using a single bedside burr hole is described. This technique is flexible, provides reliable, clinically-actionable data that can be used by neurosurgeons and neurointensivists at the bedside within hours of injury.
The authors have nothing to disclose.
The authors wish to acknowledge the leadership of Dr. Norberto Andaluz (University of Louisville) for his role in spearheading this technique. We also wish to acknowledge the hard work of the neurosurgical residents who refined the technique and the neurocritical care nursing staff who have embraced this new technique for the benefit of their patients.
Cranial Access Kit | Integra LifeSciences | NA | Cranial Access kit |
Neurovent PTO | Qflow 500 | NA | ICP/PBtO2 catheter |
Qflow 500 Perfusion Probe | Hemedex, Inc | #H0000-1600 | rCBF catheter |
Qflow 500 Titanium Bolt | Hemedex, Inc | #H0000-3644 | Cranial access bolt |
Spencer Depth Electrode | Ad-Tech Medical Instrument Corporation | NA | iEEG |