Telemetry-Based Neuromonitoring System Measuring Dynamic Intracranial Pressure Following Closed-Head Rotational Brain Injury in Swine
By Xu Meng, D. Kacy Cullen, Mohammad-Reza Tofighi, and Arye Rosen
The monitoring of changes in intracranial pressure (ICP) is of great significance in studies of the effects of traumatic brain injury and hydrocephalus. We have developed and tested a small fully embedded wireless ICP sensor, incorporating a novel antenna and packaging arrangement. In-vivo dynamic studies of continuous wireless ICP measurements in a swine model of closed-head rotational-acceleration induced TBI were performed; in addition we have demonstrated the robustness of this microwave pressure-monitoring system.
Traumatic brain injury (TBI) may result in devastating increases in intracranial pressure (ICP) due to vascular compromise and secondary sequelae causing edema. In fact, the monitoring and control of increased ICP is a major therapeutic goal across a range of TBI severities. Standard commercially available ICP measuring equipment uses a tethered fiber optic probe that penetrates the brain, and therefore can only remain implanted for relatively short time periods. This restriction presents considerable logistical, medical, and technological challenges to researchers, as well as hinders effective surgical interventions. This paper presents a small fully embedded wireless ICP device with subdural placement that simplifies the surgery procedure, while reducing the infection rate, the risk of hemorrhage, and the degree of tissue injury. Such a device may also simplify clinical management and research protocols by offering a means for semi-invasive and long-term ICP measurements following brain injury.
Figure 1: (a) ICP device configuration (top view) communicating with a USB based receiver. (b) ICP device bottom view with zoomed sensor view . (c) Schematic of implanted device contained above the skull with a 5.1 mm burr hole for sensor access to cerebrospinal fluid (CSF).
A modified eZ430-RF2500T board (Texas Instruments Inc., Dallas, TX), incorporating the capacitive microelectromechanical system (MEMS) sensor (Murata Electronics Oy, Vantaa, Finland) and a 3-V lithium coin battery (CR2032, 220 mA·h, 20-mm diameter, Panasonic, Secaucus, NJ), is used as a stand-alone wireless device . The wireless ICP network application consists of CC2500 2.4 GHz low-power wireless radio and MSP430 microcontroller (both from Texas Instruments Inc., Dallas, TX), and a custom designed annular slot antenna (to yield high radiation efficiency when embedded in tissue, with transmit data up to 18m for ~10-mm thick tissue layer), replacing eZ430-RF2500T's chip antenna, according to design considerations detailed in . The communication is based on the Texas Instruments Incorporated's SimpliciTI network protocol. The wireless ICP device communicates with an eZ430-RF2500 access point connected to a PC, sending the pressure and temperature information. All electronics and battery sit on one side of a titanium sheet with an open nozzle on the opposite side. A very small amount of silicone rubber is applied for attaching the different layers to form one unit and the entire device is fully encapsulated by a biocompatible medical grade epoxy (EPO-TEK 302-3M, Epoxy Technology Inc., Billerica, MA, Figure 1A and 1B), which is highly water resistance and is a relatively low loss dielectric at 2.4 GHz . Devices were implanted into anesthetized Yorkshire swine 24 hours prior to injury, which required a minimally invasive surgical procedure with the device placed over the skull with a 5.1-mm diameter transcranial burr hole to allow sensor contact with the cerebrospinal fluid (CSF) (Figure 1C). Non-impact TBI was induced via rapid head rotational velocity/acceleration using the Hyge pneumatic actuator. Head rotation was achieved in the sagittal plane at levels established to be moderate-to-severe (peak rotational velocities: 105-138 rad/s). Animals were sacrificed within 6 hours and the brains processed for gross and histopathology.
Accordingly, we were able to measure dynamic ICP changes using an implanted custom-built device in a swine model of closed-head rotational injury. Following implant, the baseline ICP readings were relatively stable over the 12 hours prior to injury at 15.6 ± 5.3 mm Hg (mean ± standard deviation) (Figure 2A). We found that closed-head rotation TBI induced a rapid and extreme ICP spike occurring directly upon injury (max ICP >115 mm Hg). Notably, device integrity and positioning remained suitable for dynamic post-injury ICP readings, which is impressive given the forces necessary to generate the rapid head rotation in swine (peak angular acceleration of over 50,000 rad/sec2). The acute elevation in ICP generally lasted for 40-60 minutes, followed by a gradual decline to maintain a persistently elevated level over several hours post-injury. This trend of an immediate ICP spike followed by persistently elevated levels has not previously been observed following closed-head injury. To confirm our measurements, the standard Camino ICP monitor (Camino 1104B, Integra Life Science, Plainsboro, NJ) was introduced into the parenchyma 1-3 hours post-injury (placed contralateral to wireless device). Over multiple trails, Camino measurements were within 10% of concurrent measurements with wireless devices, with differences potentially attributed to different placement (intraparenchyma versus subdural). Gross pathology (Figure 2B) revealed subdural hematoma in animals experiencing immediate ICP changes, whereas persistently elevated ICP was likely influenced by both cytotoxic and vasogenic edema.
Figure 2: (a) Example ICP trace from wireless device before and after closed-head TBI in swine. ICP readings were stable prior to injury, but severe TBI induced an immediate spike that was persistently elevated for several hours. (b) Brain gross pathology - coronal section (arrows showing blood accumulation within the third ventricle, as well as within a cortical sulcus) .
In summary, we have demonstrated in swine dynamic ICP increases as an immediate consequence of non-impact head rotation injury, mimicking moderate-to-severe TBI, by using a novel wireless ICP device. This miniature, implantable device may be utilized with diminished risk of infection as a tool to diagnose and track ICP changes following TBI for a range of severities. Moreover, the capabilities of this platform neuromonitoring system may be expanded to include other critical physiological modalities including cerebral oxygen, temperature, and blood flow.
For Further Reading
1. X. Meng, K. Browne, S.M. Huang, C. Mietus, D. K. Cullen, M. R. Tofighi, and A. Rosen, "Dynamic Evaluation of a Digital Wireless Intracranial Pressure Sensor for the Assessment of Traumatic Brain Injury in a Swine Model," IEEE Trans. Microw. Theory Tech., vol. 61, no. 1, pp. 316-325, 2013.
2. X. Meng, M. R. Tofighi, and A. Rosen, "Digital Microwave System for Monitoring Intracranial Pressure in Hydrocephalic and Traumatic Brain Injury Patients", Digest of 2011 IEEE International Microwave Symposium, June 2011.
3. X. Meng, K. Browne, S.M. Huang, D. K. Cullen, M. R. Tofighi, and A. Rosen, "Dynamic Study of Wireless Intracranial Pressure Monitoring of Rotational Head Injury in Swine Model", Electronic Letter, Vol 48, Issue 7, p. 363- 364, March 2012.
4. A. Vander Vorst, A. Rosen, and Y. Kotsuka, RF/Microwave Interaction Mechanisms in Biological Tissues, Hoboken, NJ: John Wiley & Sons, Inc., 2006.
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February 2013 Contributors
Nitish V. Thakor is a Professor of Biomedical Engineering at Johns Hopkins University, Baltimore, USA, as well as the Director of the newly formed institute for neurotechnology, SiNAPSE, at the National University of Singapore. Read more
J. C. Chiao is a Greene endowed professor and Garrett endowed professor of Electrical Engineering at University of Texas - Arlington... Read more
Xu Meng (S'08) received a B.E. degree in electronics and telecomm. in 2006 and a M.S. degree in biomedical engineering in 2008 from the Beijing Institute of Technology... Read more
D. Kacy Cullen has B.S. and M.S. degrees in mechanical engineering, in 2002, and a Ph.D. degree in biomedical engineering from the Georgia Institute of Technology in Atlanta, GA... Read more
Mohammad-Reza Tofighi received his B.S.E.E. degree from Sharif University of Technology, Tehran, Iran in 1989, and his M.S.E.E. from Iran University of Science and Technology, Tehran, Iran in 1993. Read more
Arye Rosen received a Masters degree in engineering from Johns Hopkins University, a M.Sc. degree in physiology from Jefferson Medical College, and a Ph.D. degree in electrical engineering from Drexel University... Read more
Walker Turner received B.S. and M.S. degrees in Electrical and Computer Engineering from the University of Florida in 2009 and 2012, respectively. Read more
Dr. Rizwan Bashirullah received a B.S. in Electrical Engineering from the University of Central Florida and M.S. and Ph.D. degrees in Electrical Engineering from North Carolina State University. Read more
Changzhi Li received a Ph.D. degree in electrical engineering from the University of Florida in 2009. Read more
Ehsan Yavari received a B.S.E.E. degree from the Ferdowsi University of Mashhad, Mashhad, Iran, and a M.Sc. degree in electronics from Tarbiat Modares University, Tehran, Iran. Read more
Victor M. Lubecke received M.S. and Ph.D. degrees in Electrical Engineering from the California Institute of Technology, and a B.S.E.E. degree from the California State Polytechnic Institute, Pomona. Read more
Olga Boric-Lubecke received a M.S. degree from the California Institute of Technology, Pasadena, and a Ph.D. from the University of California at Los Angeles, all in electrical engineering. Read more